The Duguetia Alliance Where The Ways Part - Ol.87 (2), Pp.234-245

.
Annals
of the
Missouri
Botanical
Garden
2000 fr
Volume 87
Number 1
The Annals, published quarterly, contains papers, primarily in systematic botany,

contributed from the Missouri Botanical Garden, St. Louis. Papers originating outside the Garden will also be accepted. All manuscripts are reviewed by qualified,
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THE
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Volume 87
Number 1
2000
Annals
*
of the
Missouri
Botanical
Garden
OUR UNKNOWN PLANET:

RECENT DISCOVERIES AND
THE FUTURE.
INTRODUCTION'
P. Muk Richardson'
i.h pi in
n ,,, '
ml i ><> !, iv lom-s. Can we es
". <
are out there to
be discovered? An international group of experts has
1 t: ', , i-d to St. Louis to give their thought* and
pi,;!,, t<ot,\ al.mil //('> i>il>,H,!','>L, ('"< <</ li.ido^y. I'l,-
the world to be discovered. The finding of this seei

idline news to biologists, as was the discovery of the Wollemi Pine
and several new large mammals, discussed in the
following page-. l|ouc\el. ilie legulai and conlillued reporting of new species usually attracts less
attention. For example, one of my former students
recentl) published five new species in the limine
Had genus Cryptanthus (Ramirez, 1998). To my
M/."/is,f(,'- >>'/ , ."'v/v,' ,>' </" <
,','',. v/ ,/ ;>/,'..;
mis in the U.S.,

Austin1,,a, ,rhl the 1'i.pi, s, !o in-sh'iuli i /.!>>s mammals, and last, but not least in every sense, extremoplulrs and othci huclena.
Kivei advertising tin
45'1' Annual Systematics Symposium.
In February 1998 I was in London, and purely
Sociclv on eoelneaullis. e\[terl|\ delivered b\ |V|.
Korev. Later that veil ni\ wd.au
. . - n i|. - -~by a coelocanth specimen in a delight!"
marine
ally off the southwe:
^.nicliwanls from tin
ro Islands. However,
i !- II .1 in Indonesia.
portant than the discoveries which make headline

news because the new species of Cryptanthus are
the result of full i
- ul.-d < ismns oi the genus
ba-ed :m :i< Id. In i i ii !.-fL .n I lanoiaton studies
The leaders can |U<h
11.> i - I - in the following papers that eolll|il se (he published proceed ngs
The 1998 Annua] Systei
fered from tin
t in that there were ten
speakers rather
ual seven. This allowed
I'm ;i gr. atei . h -,
'This and tht eigi.l

o I
hat toil
it .n
I.
i
!
llu loth \nniial Systematics S\ mposium ol tin
Missouri llol.uii,,. 1 ml .. (>,, ! ,l,n,.>n -'/..,/ , ,' , i >> <
,,',', I .
I
i| 0,111m WHS held 9-10
Oclnhei. I'.""J;. ;Mhc Mi^!>uri l!i>(aine:il <.:ir.h-n in N I ...uis. M is-.'iii i I - \
The symposium was supported in part l.y the National Science Foundation under grant number l)Kli-> 12(11 10. I
thank Peter Haven for helping to select i line .
i i
i
I Ii I mill I ml ici e\|>ert staff for wonderful
help in organizing a
urn
i: In.
. i .
i rl ira \
I. !. n
i
i ii n
<l for the cover of the
I harden. P.O. Pox 2W. St. Louis. Missouri t.oloo. l,S.
ANN. MISSOUJ
87: 1-2. 2000.
e cov-
tegrate their analyses ami discuss criteria for es-
begau
lablishmenl of higher taxa.

The plant talks came after lunch. Iain Prance
inloiui. .1 lli. .iii.h.
.in.) now llic readers) tliat
llie mi ml x-i (il angio-peiins i- .tiri.nlh mi.In. sliliialed, and lie confident!*, predicted llial there are
in fact between 300,000 and 320,000. He used
the PCR methodology so necessary for current molecular systematics techniques. Literally,
the book on molecular systematics of plants had to
be rewritten within six years (Soltis et al., 1992,
1998). Microbes were followed by Richard Brusca's
fascinating talk on arthropod diversification, and
this made me think of eating deliciously tasty large
crabs caught in the River Jurua in Acre, Brazil.
Next was Kbbe Nielsen's discourse on insects unfortunately not included in the published proceed-
specific examples of the discovery of palms in Madagascar and other areas, as well as detailed studies
<>f all genera in areas in Brazil and Brunei, to develo
P ,lis <ase for an intensification of the rate of
collection to confirm Ins predictions before it is too
la,<
"- Barbara Prigg^s talk <.n botanical discoveries
in
Australia contrasted the media attention given to
th
^ 'li^'very of a new genus of conifers compared
'" ''" "'ichai ismalic discovers of 01 new species
j" ^ Rstionaceae and allied families. Finally,
Hai : na Killei mad.- the surprising .
that the rate of discovery of new plants in the Ur
ed States and Canada has been constant for the p
century and shows no evidence of tapering off.
Mike Donoghue gave a very entertaining s
stimulating after-dinner talk, emphasizing that
current age of discovery may be different from e
Her ones, but it is both richer and more illumin
ing. It is the duty of all systematists to capture I
ings CM
irreni knowli
ol in shwater fishes
was the subject ol John l.iindh.ag and his col
pletely known, I wonder if the diversity of fishes
we ate alongsid.
..
i. ,. ,i
nnl . rab ma\
have h.-en species nev\ In scii nee Km hllialeb. lhe\
were photographed before they went into the frying
pan. Iea\ nig soun . lu.-s al I. a-a* l<> their existence
Last in the animal line of talks was John MacKinnon, who told us about new ungulates being discovered in Vietnam and his predictions about
where future finds will likely be made. The morning
session ended with some wonderful video footage
i 11
r
,
.,
,
.iiiiL
''"'' s
roni l.yiii Vlargulis i. 1 i
i i
I
.
but see her books Five Kingdoms: An Illustrated
Guide to the Phyla of Life on Earth (Margulis &
portantlVi tne
public at large,
Literature Cited
Maûlis. I.. P*t;; Ssmhioiic Planei: A New Look at Kvolulion. liaMc Hooks. New V.rk.
_
\ S.-liwut/ I'l'i," |m KIMMID S \ II
l\k
lustrated Guide ... th. Pin I., t I ,t
ail, I ... man.
San Francisco.
Schwartz, 1998) and Symbiotic Planet: A New Look

nl I . /'/ n> (M ugi L-. l')(>Ji) W Inle not everyone
^ZtL^'u- ' 'md' .',me nom.aichima I','! I l!i''""l l'.T

va|.(| (). ' ^ .'{. ., ["- .,., ,
will agree with Margubs's concept of monophyly,

there is no denying that she has added a very in-
N.llis. P. S.. I). I\. Noltis c\ J. |. Doyle (Kdilors). 1992.

Molecular S>siemaiies of Plants. Chapman* Hall. New
teresting viewpoint to overall discussions of biodi-
.or '
versity, and at tilt - III. lm

1
i II il
appeal for all biologists and paleontologists lo in-
Molecular iMsl.analirs ol Plants II I )\ \ Seciuen<anKluwer. Huston
. .
..
EXTREMOPHILIC BACTERIA
AND MICROBIAL DIVERSITY1
Michael T. Madigan*
W.v.w pmkarsolic mirruoiânisris mriah ; "'i'\t tctni nr. ; onmcii! -" hainlais m *lnc! Mine chemical or physical
v.ui il>l( |s| <hll< 's sionili' ai l'\ fi >III ill il loi rid in ll (hilars lli il -,upp..il pi ml in. imni d lift (,r< al strides have been
made in recent years
n\ of them turn out to
peratures are perhaps di rm-l h <n MI
ll
i
i I
ill!
Ilnli
n
- n. . d
niad. heat slal.lc md
their evolutionary po i n
I
h I
I . i II ..
I
MI
. I I. i< |( r i.il diw r-it\
improves, prirnariU i
i
r
I
ml di\ersil\ and from
new advances in isol nion ami I
' i
r\ div< rsity on Earth
does not reside in pi
I
now great interest in
niini'i: lli ii'Mv -. IK I i ( s .in, . - ,,r I nlli - sin ilh >i ( . II- . i ,s,
bum . Im..|i>js a'( n la ( d an is
Kr\ n-oriis: cvlrcmopliilie II.KII"I;I, evolutionan lnslor\. inicrolii I di\ ccsih, prokaiyoles.
Since the days almost 100 years ago when Robert

Koch and his assoei ites is lated i\r- first pure cultures of bacteria,
>
iologists
rid wide I
been isolating laboratory cultures of literally thou- "i. difl
J ' i I
11
tl lude, of course,
most of the causative agents of infectious diseases,
but more important from the standpoint of the web
of life on Earth, many of the bacteria that carry out
critical chemical reactions that form the "life support" system for plants and animals (Madigan et al.,
2000). Despite the diversity of organisms that are
already known, it is now clear that microbiologists
have only seen the tip of iceberg; most microorganisms that exist in nature, in particular the bacteria,
have not yet been obtained in laboratory culture!
Indeed, with the In
in
lai
n
biologists have explored a variety of microbial habitats and have detected not only new species of bacteria, but new genera, families, orders, and even
phyla (Barns et al., 1994; Hugenholtz, et al., 1998).
Imagine finding a new phylum of plants or animals
today! The challenge for microbiologists now is to
isolate these organisms, learn about their basic biology, and harness their vast genetic resources for
the benefit of mankind.
(/real
demerit li
[
<l<
ih field of microbial diversity in recent years because of the
new-found ability of microbiologists to experimenthe evolutionary relationships of
bacteria. This giant leap forward emerged from the

tools of molecular biology, especially as regards the
e\el pment of rapid gene sequencing methods and
powerful algorithms for the comparative analysis of
nucleic acid sequences. But for these advances to
impact microbial evolution, a gene or genes that
reflected the evolutionary history of an organism
had to be identified. Such an evolutionary "Rosetta
Stone" had long been sought, but not until the advent of comparative ribosomal RNA sequencing as
a rapid and specii
means I<>i deducing bacterial
phylogenies (Woese, 1987) did microbiologists have
the tool they needed to classify bacteria in a nanural fashionthe way botanists and zoologists had
classified their subjects for over a century using
imarily |
i ristb s such as bones

or leaf arrangements as evolutionary guideposts.
Two key concepts have emerged from comparative molecular sequencing of ribosomal RNAs: (1)
that cells evolved along three major lineages, the
Bacteria, the Archaea, and the Eukarya, instead of
just two, the prokaryotes and the eukaryotes (Fig.
1); and (2) that the evolutionary difference between
a mouse and an elephant (or between Chlorella and
Trillium, for the more botanically oriented) pales by
comparison to the evolutionary distance between
want to mention, like Pseudomonas and Bacillus.
The first of these conclusions, that prokaryotic
life contains two major evolutionary lineages, is
slowly but surely becoming mainstream thinking
among microbiologists, and is even gaining support
h of M. T. Madigan is supported by National Science Foundation grant OPP 9809195.

of Microbiology and Center for Systematic Biolo
I I .1 6
3
hern Illinois University, Car3 62901-6508, U.S.A. madigan@micro.siu.edu
ANN. MISSOURI BOT. GARD.
87: 3-12. 2000.
Microbial Life Forms

Macroorganisms
figure 1.
A phylogeneti*
Extremophilic Bacteria
from maerobiologisls as e\ ulenoed in lh< inclusion

of tliis concept in recent I -'
I
i
& Johnson. 1999; Haven et al.. 1999). However.
the second com I
pnte
relationships of piokar\oles (Fig.

information to <
speeilie nucleic acid probes as a i
fying and tracking s
different plants or animals can be extremely closely

related in a tnolecul
n
i i
en.se, has been
for many a harder pill to swallow. If one steps back
for a moment and considers that it is not the evolution of the mouse and the elephant, or the alga
and the flowering plant, as intact entities, that molecular sequencing speaks to, but instead, the evolutionary history of the cells that make them up, it
is easier to understand why the bulk of evolutionary
change has occurred in the prokaryotic world; prokaryotes have existed for some 3.8 billion years,
ogy has been to take these tools into various extreme environments and probe for the di\ersil\ of
'i'i< : 1 ii;< h. - i i I n< t ill. in horn these sludiw, which historically followed by many years more
classical enrichment and isolation approaches, has
been an awareness that extreme environments are
not a place for "hangers on," but instead are habitats that flourish with microbial life, especially prokaryotes (Bams et al., 1994; Horikoshi & Grant,
l
"8; Hugenholtz et al., 1998). The rest of this
while the mouse and the elephant have only very

recently evolved
1 h rge 1
PaPer wil1 trY to introduce the reader to some of

these organisms and their homes, and discuss what
Prokaryotes ruled the Earth for at least 2 billion

years before the modern (organelle-containing) eu-
laboratory studies of these remarkable prokaryotes

' r^vaM for our understanding of the physi-
karyotic cell appears in the fossil record. And
<><h<''n'<al
inela/oans (multi-i < !

uanimals) have
only existed for some half billion years or so. So by
EXTREMK ENVIRONMENTS AND EXTREMOPHII.ES
the lun. tlu si !_
.
.
...
,
/.oolov.isis cocsuler ihe
....
of
plants and
! n
,
,
...
.
evolniionan di\ers:f!caiion
.
cells
.-..<
in
....
diffe:enl
Microbiological cxamuialion ol e\li.-me en\ iror'

merits ha- ...i'ii..l i am n I-J.II
-- change in prokaryotes is not manifest in morFor what
thai
.
'
h imam
.\onld
.,
.,
< oi sulci
i i
. s.lret: o:
ii
i-
uninhabitable: extremes of heat or cold, pH, sahnity, pressure, and even radiation. As previously
nvironments are inhabited by
ol microorganisms, most of
n>
In contrast to higher organisms prokaryotes have

show great genetit
divergence. However, unlike la/o is. . volutionvariation.
a is all--:
,., ... . ,..l.l I. .,
wa\s to
i<: i>e lughb dhergenl organ sins.
and the elephant ai
phologieal
hfe
n i
.
.
.
,
. (..i c\;imple. w;is - urn \
appears lo ilx
>
,.,-,.,
had alrcaiK occurred. Diversification ol lhe mouse

oi' ai :angifig
hmits t(
...
presell. ,
^^'^ ZZn\
philes" (Horikoshi & Grant,
^^ 199?. Ma(Hgan ^ ^
Qren
199g)
Seyera] c]asses ()f
2000;
Madigan
,xtn.m()|llll|(.,
n-eogni/ed in mierobiologv. and laboratory cidlmcs
tena maintained a very small s.ze and changed

relatively little (compared with metazoans) in mor-
of representatives
f,,lol,,LV l""^' billinnx ol v. .,- ol evolutional

history. But that is not to say they did not evolve.
Molecular sequencing tells us that they have indeed evolved but that the product of this evolutionary change is invisibleinstead of big changes in
size or shape, evolutionary change in the prokaryotes focused on metabolic diversity and the genetic
capacities to explore and eventually colonize every
conceivable environment on Earth, including extreme environments. Tims we must go to the genes
of the prokaryotes to see their true phylogenetic
diversification, and with advances in nucleic acid
sequencing, this world is now beginning to open up
(Madigan et al., 2000).
l sinr cmnpar.nne nbosotiial HN\ seoueneing
microbiologists can now not only construct natural
,,,,,e term, usually a word with Greek or Latin

foliowed by the combining form "phile,"
"Wing." Thus there are thermophiles and
hyperthermophiles (organisms growing at high or
very high temperatures, respectively),psychrophiles
(organisms that grow best at low temperatures),
acidophils and alkaliphiles (organisms optimally
adapted to acidic or basic pH values, respectively),
barophiles (organisms that grow best under pressure), and halophiles (organisms that require NaCl
for growth) (Table 1). Instead of trying to be inclusive here, as literally hundreds of different species
could be included, the organisms listed in Table 1
are the current "record holders" in each of the exIremophiie eategoi ie.-. The column of most interest
in Table 1 is the
labeled optimum," for here
n)
of each class are known (Table

Organisms in each class are denoted by a de-
rootg
Greek for
Table 1
Classes and examples of extremophiles".

Descrrpt.ve
Genus/species
Extrem
Minimum
Optimum
Maximum
Temperatu re
High
Hypertherniophile
rs\clini|>liil<-
Pyrolobm futnaru
Polaromonas vacuolate
100 C
ll.T'C
pH
Low
High
Acidophile
Mkaliphil.
^^:!rego-
Pressure
ISaruph lc
MT41 (Mariana Trench)1'
500 aim
Salt (NaC
Halophile
Halobacterium salinarum
15%
0.06
it becomes clear that t

ly tolerating their lot, but that they actually do best
in their punishing habitats; indeed most actually
0.7 (arcy
10(207, NaCll'1
.2
700 atm (4C)
>1000 atm
25%
32% (saturation)
forms.
require their extreme condition(s) in order to reproduce at all.
L,FE
Extremophiles are of interest to both basic and

applied biology. In a basic sense, these organisms
; biological secrets, such as
omolecular stability
r constructing macromolecules stable to one or another extreme (Madigan & Oren, 1999). But in an applied sense,
these organisms have yielded an amazing array of
enzymes capable of catalyzing specific biochemical
reactions under extreme conditions (Adams & Kelly, 1995). Such enzymes have served as grist for
industry in applications as diverse as laundry detergent additives (proteases, lipases) and the genetic identification of criminals (Taq DNA polymerase and its use in the polymerase chain
reaction, PCR).
Another important realization that has emerged
from the study of extremophiles is that some of
these organisms form the cradle of life itself. Many
extremophiles, in particular the hyperthermophiles,
lie close to the "universal ancestor" of all extant
life on Earth (Fig. 1). Thus, an understanding of
the basic biology of these organisms is an opportunity for biologists to "look backward in time" so
to speak, to a period of early life on Earth. This
exciting realization has fueled much research on
Although thermophilic bacteria

growth temperature optima between 45C and 80C)
have been known for over 80 years, hyperthermophilic bacteriaorganisms with optima above
80Chave only been recognized more recently
(Stetter, 1996). Following the pioneering work of
Thomas Brock in the 1960s and 1970s (reviewed
in Brock, 1978), Karl Stetter and co-workers at Regensburg (Germany) have proceeded to isolate over
30 genera (> 70 species) of hyperthermophiles.
AT
HIGH
TEMPERATURE
National Park (Brock, 1978). By contrast, Stetter'*

group, whose focus has been on isolation and culture, has isolated many of the hyperthermophiles
known today, including Pyrolobus fumarii, a re
markable prokaryote that can grow up to 113C (Ta
ble 1, Fig. 2) (Blochl et al., 1997).
Thermophili
n
organ as can be isolated
from virtually any environment that receives intermittent heat, such as soil, compost, and the like,
But hyperthermophiles thrive only in very hot and
constantly hot environments, including hot springs,
both terrestrial and undersea (hydrothermal vents),
and active sea mounts, where volcanic lava is emitted directly onto the sea floor (Stetter, 1999). It is
also strongly suspected, and some supportive evidence exists, that hyperthermophiles reside deep
the cliiirm. v,. ulinli ar. <.||en i.M|\ about 0 " cm

thick, show a temperature gradient from about
300C inside to 2C outside. Because prokaryotes
williin the earth, living a buried existence and reiving on gcntlieniial heat lor their metabolic activities and reproduction (Stetter, 1999).
The most extreme of known hyperthermopl il<-.
those with temperature optima above 100C, have
come from submarine Indiolhermal vents (Stelter,
1996, 1999), and examples include P. fumarii
(Blochl et al., 1997, and Fig. 2) and the methanogen Methanopyrus i.andlrii (Kurt it al., 1991). Both
\reliaea (fig. I) and an- chemolithotroph i >! n
isms that use inorganic compounds as energy
sources), using molecular hydrogen, II as their
electron donor (energy source), reducing either
NO, (P. fumarii) or CO, (M. kandleri) as electron
acceptors to grow 1>\ anaerobic respiralioi (Madi
gan et al.. 2(MK); Stetter, 1999). Besides requiring
vive temperature- -uh-laul iall\ al.ove their upper
gmwili i. rri|.. I.IIUK limits, making a conventional
autoclave regimen ( I ."> mm. at I2IC) insufficient
for sterilizing cultures of either species!
Both P. fumarii and M. kandleri originated from
hydrothermal vent chimneys (Blochl et al., 1997;
Stetter, 1999). These are precipitated iron mineral
deposits that form as extremely hot water (up to
lOOT.) containing various minerals emerges from
deep-sea hydrolhermal \eni- (note that although
this water is superheated, it does not hod because
ol the h\<lrosiatic pressure of the waler column,
usually 2<>00-:i<HM) in, that overlies these vents).
Although the water that emerges is too hot for life,
peraturc exist across the chimney wall leading to

idi i I).i iilats for various species of heat-loving
bacteria.
Using nucleic acid probe technology several
morpholep all'
A bacteria have been detected
i
hcrmal vent chimney walls (Harmsen et
al., 1997), suggesting that ihcsc compact thermal
gradients may contain many different microbial
ions in addition to those already isolated.
my botanical friends reading this paper, I
e remiss if I did not point out that P. fumarii
kandleri are good examples of primary prololallv divorced from sunlight, a capacity
widespread in the microbial world. Besides growing
at almost unbelievably high temperatures, P. fumarii and M. kandleri are also autotrophs, capable
. grow ( g in a simple anaerobic mineral salts medium supplied with C02 and H2; neither sunlight
noi ;i k. \ pi In. ' ol photosynthesis. ()., s required
for either organism Indeed, il lias been hypolhe
si/., d thai ! iv 1 ' ie I hi' process of photosynthesis
11,-1
the inaiMi HK.m \,\ which new ..rg.mre materia
was synthesized on Earth (Madigan et al., 2000).
For an organism to grow at high temperatures
especially as high as those of the hyperthermo
bill
-cussed here, all cellular components, in
heat stable (Adams & Kelly, 1995; ]
Antranikian, 1998; Wiegel & Adams, 1998; van de
Vossenberg et al., 1998a). The thermostability of
i'ii/\ rues iron un HIS I y perther rnoph lies, referred
(Adams & Kelly, 1995). The structural featui

dictate thermal stability in proteins are n
understood, but a small number of noncoval<
ently makes the inside of the protein "sticky" and

thus more resistant to unfolding, a small surfaceto-volume ratio, which confers a compact form on
lire protein, a reduction in glycine content that
tends to remove options for flexibility and thus inIrud ict i ; id t\ ti lh. ninlei ul-. and exh nsive ionic
ature (Ladenstein & Anthranikian, 1998). In addition to these intrinsic stability factors, special
proteins called fhupemnuts are synthesized by hypertheruiophiles Chapcrnriins film lion to bind heal
denatured proteins ami refold diem into ll eii a. the

loiin. Tin lin nitosiHiic is a t v pe oi < hapemriiti ilia!
is widespread anion- hvperlh. tmoplules capahle oi
growth above 100C, like P. fumarii and M. handled (Stetter, 1999).
Several factors may combine to prevent DNA
from mi iling m I \ : erll ermopli |. -. I lowevet. if.
two i
I n|
i ii
mv- pp.-at to be the enzyme reverse DNA gyrase, which catalyzes thepas'/>.' - -up' ron inn oi v -,.'.1 ein il i I '\ \ ;hv on
I last. liolihv (< l diem oplii cs eoril J'n I A, \ g\ rase.
an enzyme that supercoils DNA in a negative twisted lasliion). ami vai urns lvp< s of 1 \ \ 1.1mill g pro
[ proti u- (Mad -an X
Oren, 1999; Pereira & Reeve,
plnsieoehemical reasons, positively supercoiled
DNA is more resistant to thermal denaturation than
is negatively supercoiled DNA. And the fact that
reverse -v rase so ms In hi llie i,f,i\ protein thus iai
found universally among hyperthermophiles (re
gardlcss oi llieii m. laholi. pattern! (Wadigai A,
Oten. I'J'X)) points to an important role lor it in tinheat stability of DNA.
Several hvperlliermophiles contain DNA binding
tm I. m- ll at ip| ' n i pi.iv a o,|i i, MI mil HI im.
DNA in a double-stranded form at high
i
lure. Sot
I tin
i i
to the core histories oi eukarvnli. . < |> aid imiriii I

to wind and compact the \)\ \ uiio r.iicl.-osomedike
structures (Pereira & Reeve, 1998). Others have no
structural relation liip l< h > n< hut when bound
to l)\ \ alter its structure in such a way as to signiiieaulU raise its melting temperature (Viadigan t\
Oren, 1999). It is likely that the combination of
positive supetco lei- oi' l)\ \ along with pioleins
ill .1 [Hi v ell! i ?\ \ ll i III g s a 111.I| .1 -oi ilioii lo l;ie
maintenance and integrity of DNA in hyperthermophiles.
Heat can also affect membrane stability. As all
olog i
III organisms living at moderate
l(i.
temperatures cell membranes are constructed i < m
[he l\ fii.-al ""lipid Ii Liver'" model liv drophnhie ics
idues (fatty acids) inside oppose each other and
residues |sn, ii a> glveetol ptiosphale) lie at the surface of the rih irei m. i;! and 111 ;w r< pla-m. n-sp. e
Iii. Iv. maintaining contact with dm ;iqn* oils phase
Ii one applies suilieienl iiea! lo s n-li a memhiane
the
f the membrane will
pall apart, leading m memm ane damage and ev
loplasmic leakage To prevent this from occurring
at very high temp i
in - h erthei nmphiles have
evolved a novel membrane structure. Instead of
h itiuiig a memhr uie as ; lipid !.,'<<i\< >. i- nisi ths
cussed, som,- hvp. "hei,: opl i',s , >.,,, ,,,!;, |,!Mj
the opposing Indrophohic residues from each lave:

oi 'he i .-mhraue togedm; \\,v,\ de \os~en;erg el ah.
1
" M
n I |
> - 'iiver instead of a
bilayer, and prevents the membrane from melting
\lthough the precise chemistry of lipid monolayer membranes can vary some-
AT
Low
TEMPERA
>w about life at tht

Cold
the oceans, which make up over
! .arm's Miri.n '- tn litilaiti ai a\ era-;.- I
about 2C. And vast land masses are
in /. i
I lo
,alf the
old, or even
cold temperatures are no barrier
is various microorganisms flourish
in ice (Horikoshi &

Grant, 1998; Madigan & Marrs, 1997). Many mien >: ii |sii - ha. i !.-mi - ilated capahle i i growth
at refrigerator temperatures (4-8C). These are usu;ll\ /;>,- /,",/,.;</./.',;. i i arum, ll al ihl gh l.nev are
hi
I growth in the cold, they grow better at
warmer temperatures, usually 25-35C. True psyii:i<>ph>!>s. <i.Ti . .1 ii- ",! igani-stiH that grow hrsi
at 15C or lower, are usually only present in perparli.ailar. the Antarctic (Horikoshi & Grant, 1998).
A variety of microorganisms including algae and
Inta
ihe
ocean water thai remains frozen for i
year. Sea ice is the >iahil. I lo: one well < haiaelei
/ed iia.'el um. !'old! <><<>,i,a> ; .iritolnla. ihe genus
name indicating its affinity for cold temperatures
(Irgeiis el al . \'>'H>). l\>l(ito!athis ninitilntn -reus
op! ma l\ r II and Im Is :. , p.< i.iiim - i| ,:,\e 1 'I (]
too warm for growth (Table 1). Other psyclirnphdos
very sensitive to warm ug. -real can- mils! hi (aken
ill dieii I-.-" ; all and < ihl re lo ;.n '- ell! klllll g lliertl
low as room temperature.
\n understanding of the hiot hemistry and mohacteria is in a
much earliei slag, thai: dial of ihe hv periheimo
oi psvehroplnles. : appeals ilia! lln ir pnileuts function optimally at low temperatures because lliev are
uch a way so as to maximize lle\-
Extremophilic Bacteria
prnlt IDS from ;is\chmp.'tilt s are typically more polar and less
[ml
p< ' dtermophilt s. ,,
I, ,,
|i(. i
i-,ai
>i.-t.-iri~
mn |r>u I it* < Uy
also as-
sists in their relative flexibility.

Resides
keeping then
:
< hioul i c~
.,-
,iln i
Interestingly,
enzymes functional. ps\
I.. Joj .-,|
|.lnles, even tin
fiolil.-nis to con-
loin-ram
would
lira?)
I)
in,;.
I'I
in
i:
fats,
can
stay
softer llian
in
However, just as
otitenl
.IM
of
butter al
unsaturated
cold
tempera-
tures, psvchrophilcs legulalc (he cliernical composition
of
ihci:
membranes.
n<
ml tig, ii
purlimdai
the length and degiee <>i unsntnral inn nl la'h acids,
thus
mien
.1
itic
processes,
even
&
at
temperatures
Grant,
1998).
below
freezing
Applications
of en-
acidity
survive
inside
In
their cells,
keeping
p| I
the
. .' ipl i-u.i.
keeps
protons
I "i
m. ml.mm
from
out.
it
The
.)'
In -
passively
on
-u-ii'
l-i it
the
cell.
entering
membrane have
ii - ,in otih
re I lin ils tniem Ms
in acidic
iibove an external pH of about 4 the P.
,'J-:it,,t>
\\
where
acid
i.t pH 5, and it is
However, studn show a that
to keep them sufficient I \ fluid to allow for transput!
(Horikoshi
great
destroy such important molecules as DNA.
They
jo
m. mli an
i iianswen i
-po-ilam i i.sU
d'-i'in_ia.s
iinest -.ns cmceniim.- ih<
-uelal
z\n es f OMI psNc:i:'o;)liilcs i:icl:ide da- raid (<] in
olism of P. oshimae and other extreme acidoplules
dustiA. wlit II
concern
how
dm II a
-sp ralion and n
producers
t n
of
I wiirl
cold-water
i'ii .i i.
laundry
detergents
(see
more on this helow).
its
ihey generate a proton
involving
moli\e
lore.-
a'a d issue- o| |!.n< cne-g.-i
membrane-mediated
proton
translo-
cation (van de Vossenberg et al., 1998b).

Various acid-tolerant enzymes from acidophiles,
primarily ones located on the cell surface or ones
excreted ft..in the cell inlo the acidic milieu, have
Many extremophiles have evolved

at
extremes of pH:
the
alhaliphiles
these
are
(Horikoshi
to mow
the acidophil'a
&
Grant,
1998).
hest
been
anil
identified. These are primarily as animal-feed sup-
Al-
plements
though extremely acidic or alkaline (helow pH 3 or

above pH
10) habitats are rare on earth, in such
studied
and
where
potential
the
industrial applications
cn/ymes
I unction
to
break
down inexpensive grains to more nutrition dh

eficial forms directly in the animal's stom.nl
I- i
Smm
environments one can find a variety of microorgan
enzymes have been widely used in the poultry in-
isms dim in<' in i-ln mis'.-A
dustry
'I c ecu ah nt
;l i>. 'i<-n
acid or soda lime. Highly acidic environments ran

resul:
naliuallv
from
geochemical
activities, such
as from the oxidation of S02 and H2S produced in

lioiheti
metabolic
III
activities
of certain
irs, and from the
acidophih-s
them-
selves. For exam

terrain
I
M!', he'
to he ', the latter of which pre-
+ 3H+), or by oxidizing HS
ticularly
where
H).
active
exposure
i- nl
cipitates out as Fe(OH), (Fe"
have been
shown to reduce feed costs
and the time necessary to get birds to market.

Kxtreme alkaliphiles live in soils laden with soda
(nation) oi
in soda lakes where the pH can rise to
as high as 12. Natronobacterium gregoryi (Table 1),

for exampli
I1
"M
lake located in the Kilt Vallej of \fiica;N. gregoryi
Tin.'!',) /':',";> /,/,<,. nd.ths can g. Metal--
-^ SO,2-
and
+ 3H..0 -> Fe(OH),

to SO,2
(HS
+ 20,
Thiobacillus ferrooxidum is par-
in
surface
coal
mining operations
to oxygen of pyrite
coal scam tngêts
(FeS2)
in
grows optimally at a pH of about 10 (Table 1) (Horikoshi
&
Grant,
1998).
In
the
opposite
scenario
from the acidoplules. alkaliphiles have to contend

with the problems associated with high pH. Above
a pH of 8 or so, certain biomnlecnles. nntm.lv i!\ \
break down. Con-- -| lent
tk.
id >ph I. -.
ill
the
id pi ><!u< lion '<.in the an iu-
bolic activities of tins and related bacteria. Runoff

from these habitats can often have a pH of less than
brane that make
2. fin !ing cm ditioi s for furl I er acidophile a. li\ ily,
be stiiblc to high pH. Indeed, many such enzymes
The most acidophilic of all bacteria known thus
have been studied and a number have found in-
fas
is I'icropliiiu.s oshimae.
whose pi I optimum In:
n- , i i!
ipf
niu I
Ii
ihe I ninth\
de
i ichetl" contain pn.!eas, - and lipases .;, ,,/, m. > dial
ature optimum, 60C) so this organism must be sta-
degrade
stains) that function at
ons
Cultures of
gents that
II
lerget
Picmpiiilns nsliimuc
is also a thcminphile (temp.-!
ulusli
p.
growth is just 0.7 (Schleper et ah, 1995) (Table 1).
are "enzyme en-
proteins or fats, respectively, in clothing
tions (1 lonkosh, ,\
the high pll of soapy solu-
(aanl.
I'^-'l
..
'!'
II
il
active enzymes from thermophil

philes have been discovered and c
better target detergent additives to
Uesides keeping theii cytoplasm i :t
! h.
alkaliphiles have other biological problems in cor
tend with. For example, consider the problem <
membrane-mediated hiocncrgel us protons ex
truded to the external 8urfa< -
ter a sea of hydroxvl ions. Nevertheless, bioehen
ical studies of this problem have shown that
tioloti HIKII
<-< i
n , I i .lined by extrem
alkaliphiles and dmes -.n
I ill. . nei -\ -i. . |im
virgradi<
of Na ' , lather than I ! , dri\es this key I uneiiei g. |,,
process in extreme alkaliphiles (Horikoshi & Grant,
1998). This i*. | i .
.using when one
consid i that many (but not all) extrem*
philes are also extreme halophiles (see below), requiring high salt as well as high pi I lor ineial .ohsiu
and reproduction.
Another remarkable group ol exlremnphiles are

the halophiles -. >r . 111 l-l 11-. adapted to vre.w bes| in
salty solutions (Oren, 1999; Ventosa et al., 1998).
\nd I'm extreme halophiles like Ihtlnbm ,'ri >t;m. .
"salty solution" means anywhere from 25% NaCl
up to saturation (Wl'Yt NaCl) (Table I) llalupl, I! c
iiueiooiLiani-ins abound in ii\|"silu . lakes -,mh
as the Dead Sea, the Great Salt Lake, and solar salt
evaporation ponds. >neh lakes are often colored red
In the dense microbial on i u Hi. s >,\ pigim i l .:
halophiles such as Halobacterium (Javor, 1989).
Other habitats loi h,il..plnli. c
I.MIMMH- in
elude highly salted foods, saline soils, and undci
ground salt deposits. b> dale, a .. -\ l.ni;<- nun |,ei
of h.iloplubc baclena hav. been giown in culture
the Eukarya (Kamekura, 1998). However, the a"
<-liaeal halophiles as exemplified b\ /lal<>baclciit/m
species remain the most halophilic organisms
Halophiles are able to live in salty conditions by
preventing dehydration of their . vloplasm, They *\n
this by either producing large amounts of an internal organic solute or by concent! nee in ] i
or iri.irgainc solute liom llieir em imiimeiit (lion
koshi & Grant, 1998; Oren, 1999). The term "compatible solutes" is often used to describe organic
osmolvtes, ol winch lliere are several types, but not
1999; Oren, 1999). For example, as its os-
luob.c.
chaeon Halobat tt
,(k
&|
ssolved KC1 in the cytoplasm of Halobacterium cells is present at a concentration equal to or slightly above that of tin- dis
solved NaCl outside, and in this way cells maintain
the tendency for u.ilei |..entei an.I thereby prevent
dehydration. \s would be expected from such a
sall\ cytoplasm. .n/Aiiics that function inside of
el
f Ha obcu terium havi yoked to i< <]
' tins
large dose ol K lor catalytic activity. Ii\ contrast,
membrane 01 cell wall positioned piolem- in Hal
obtutrituiii require Na' and are typically stable
only in the presence of high Na' (Madigan <\ Oren.
1999).
Appli,
ude
those that can break down \ iseou- mil. rials pics
ent in oil wells {ml is olten (omul in geographic
strata that contain salt I as well as en/.ymes that can
cam out desnahle iianslorniatioiis in highly salted
foods. In addition, some halophiles that produce
i/.cd fo i the pioiluclioii ol these solutes as skin
supple mcts i Madigan & Oren, 1999).
Omit: EXTREMOPHILES
Extr emophilic microorganisms adapted to
pressure or which show no dcletcnoiis . II.. I- from
exposure to high Levels ol radiation are also known.
'
u' mil
ganisms thai grow best under
pressure greater than I atmospheic. I \lrein. b.n
oplulis arc the most ml. icstuig in this regard as
the) actual 1) reijimc pressure. mid ln some cases.
extreme pressure, for growth (Table 1). Strain
MTU, lot example, a baeleiinm isolated Irom ma
line sediments m 11 < Manana lieueh n. ,u the I'lnl
ippines (a depth of greater than 10,000 m), requires
at least 500 atmospheres of pressure in order to
grow and grows optimalb at .00 almo-pliei.- (and
at a temperature of 4C because strain MT41 is also
a psychrophile) l>e< aus. laboratory cull me of extreme barophiles is lath.i diiln nil. eornpaiali\eb
bllle is known ah.'ill ill. n impoituul bioinole. uhs.
However, although probably all ma< lotiiole. -ules in
extreme barophili-s need to be biochemically lai
Ion d |.i 1 igli pressuie to MIIIII extent, ex pi I llllellts
with moderately barophilic bacteria, some of which
can be grown without pressun . hav. poinled lo nutrient transport proteins in the cytoplasmic memnodifications in order t
(Horikoshi i
The
ray,
bacterium
Deinococcus
radiodurans
is
an
yield
the
data
needed
to confirm
1992). This remarkable organism can survive
30,000 Grays of ionizing radiation, sufficient to lit;
ei
shatter
its
chromosome
into
hundreds
of
; benefit for human-
karyotes undoubtedly 1
posure to as little as 5 Grays). A powerful DNA
kind than we will extr
repair machinery exists in cells of D. radiodurans
organisms. Antibiotics.
thai is able In piece the shattered chromosome back

i >eth< i
m ! yi<
markable
been
vi ibb
radiation
proposed
II-
Because of its re-
resistance,
Deinococcus
has
as a cleanup agent for the biore-
medialion of toxic
materials
m contaminated soils
that are also radioactive from the leakage of radioaclive materials: these conditions exist primarily at
nuclear weapons production sites.
KxrniAioiMi
: EVOLI
A focus of research
tered on the hyperthermophiles. As discussed earmophiles I: 14-21.
some hyperthermophiles have evolved relatively little from their ancestors present on earth over 3.5
Brock, T. D. 1978. Thermophilic Microorganisms and I
I lair
II. J. M.. I). Prieur & C. Jeanthon. 1997. Dis-
billion years ago (Figs. 1, 2). If true, an understand-
v. ii . lime > - - >. ,lu it. .1 !.
ing of the biology of hyperthermophiles may yield
.v'mi- . - f h.bndi, il ir,
Appl. Environm. Microbiol. 63: 2876-2883.

the
philes
have
genomes
been
of several
sequenced
hyperthermo-
(Madigan
&
Oren,
. -
lack counterparts in other organisms suggests
& W. I). Grant. 1998. ExtremophilesMi-
.riiln.il Life in Extreme Kiivirunniciits. Wiley. \,-u Wk.

,
1999), and the large number of genes they contain

thai
I'., C. Pitulle, K.
been partially revealed. As if living in boiling water

isn't
enough, just
imagine
what
other
tricks
L.
Hershberger & N. R.
Pace. 1998. Novel division level bacterial diversity in

a Yellowstone b
that their biological secrets have at this point only
I,,
n ol. 180: 366-373.
Irgens, R. L., J. J. Gosink & J. T. Staley. 1996. Polaromtfuis r<in/ol,il,i ;:>
MH. N|>.
iinv.. :i psyei
ij.f
i . ma
hy-
perthermophiles might be able to perform!

Javor, B. J.
As previously mentioned, the excitement in mibial
'i,
be
tl
<.li it
davs eomes from the fact that
history of the prokaryotes can now
experimenlallv
determined
Microbiologists no
1989.
'I
n,
m m,
..
\\
.. .,
o!.)U',y :IIKI liu--r.M hcmi-,lr\ Spiinger \< if:!'.- He. I

kamekuni. \l. I'*'!! hncsily nl extremely halophilie
bacteria. Kxtremophiles 2: 289-295.
Kurr, M., R. Huher, H. Konig, H. W. Jannaseh. II. fncke.
A. Trincone, J. K. Kristjansson & K. O. Stetter. 1991.
longer ha\<
on
to proposi
s|,. ulation oi
.dm
b icll
--II.
given
us
exciting
tations. Thus, in the final analysis bacterial diversity will likely dwarf that of all of the rest of biology,
Amer. 276: 82-87.
in
. into the diversity
1999. The.
extremophiles. Curr. Opin. Microbiol. 2: 265-269.
JI;ii|iMi,\ J. P.ke,.2(MK>. IJ.ock l'.,..lo,.s
ril Microorganism*. 9|f <-,| IV, ii. , II,ill. I pp< i Saddle

River, New Jersey.
Murray, R. G. K.
perhaps by several orders of magnitude. But only
ill mo- en-. ;.r<mnij
Madigan, M. T. & B. L. Marrs.
& A. Oren.
enormousindeed it is beyond our wildest expec-
nxb
MI.
l lib. rmopli l< - N.ihihty md n/\m,i

gin./Biotechnol. 61: 38-85.
1994; Hu-
the
news that the diversity of the microbial world is
continued and e\:
.| liil
Ladenstein, R. & G. Antranikian. 1998. Proteins from hy-
to the boiling point of water. Advan<
to natural environments (Barns et al.,

genholtz
in>\el j'l.'.ip
at 110C. Arch. Microbiol. 156: 239-247.
in
I,,,,:!. Tin
\.
tan ill',
Balows, II
Democoecaceac. Pp.
I'riiper, M. Dworkin,
W. Harder & K-H. Schleifer (editors), lb-
I'rnk.n vole-.
2nd ed., A Handbook on the Biology of Bacteria: Eco-
physiology. l-.ol.ilmn, identification. \ ppl ications.

Spnngc-Verlag. New York.
Oren, A. (editor). 1)<
C In ini-n v
of Hypersaline Knvironnients. CRC Press. Boca Raton.
Florida.
Pereira, S. L. & J. N. Reeve. 1998. Histones and nudeosomes in archaea and cukarva: \ comparative analysis. Exlremophiles 2: 141-148.
Raven, P. H. & (,. R. Johnson. I<<>" Biology. 5th el.
I5/M.-I
I i Hul ,|
I
, R. F. Kvert & S. K. Eichhom. 1999. Biology of
Plants, 6th ed. W. H. Freeman, New York.
Schleper, C, (,. Puhlcr. I. H..I/. \. < .ambacorla. I). Janekovic, U. Santarius, ll-P. klenk * Vv. /illig. 1995.
I'n-miiliiliis gen. i.<\.. lam. no\.. a novel aerobic heterotropin, il.. ..... I, I,
.... ..
.1 composing
archaea capable of growth around pH 0. J. Bacteriol.
177: 7050-7059.
Sleiic Ik (I \>><H IKpeMh.-.mopl.ilic prokarvolc,.
\-\:\\> \li.-.!,M.I. Rev. IB: 149-158.
. 1999. Volcanoes, hydrolhermal venting, and the

origin of life. In J. Marti cK (,. J. Krnest (editors]. Yol. anoe. and ili< Kmirorim.nt Cambridge Univ. Press,
Cambridge. England (in press).
Ventosa, A.. J. J. Nieto A A. Oren. 1998. Hiologv of moderately halophilic aerobic bacteria. Microbiol. K Molec.
Biol. Rev. 62: 504-544.
Vossenberg, J. L. C. M. van de. A. J. M. Driessen * W.
\. Konings. I 99Ra. The csscn< e .,( being cxtrcmopl.il.,-:
The role of the unique archael membrane lipids. Kxlremophiles 2: 165-170.
,
. W. Zillig & W. N. Konings. |99HI>. Bioenergetics and cytoplasmic membrane stability of the
extremely acidophilic, thermophilic archaeon. I'irrophilit.s oshimar. Kxtremophiles 2: 67-74.
\\,. .. 1 I HI \\ W \dams (Editors). 1998. ThermophilesThe key- to Molecular Evolution and the Origin of Life? Tayior and Francis, London.
\\ <>,-. <!. R. I !7 .Bacterial evolution. Microbiol. Rev.
51:221-271.
UNRAVELING THE HISTORY

OF ARTHROPOD
BIODIVERSIFICATION1
Richard C. Brus,
i arthropod phylogeny ;
arthropod diversification began m ll
ceans comprise a phylogenelic

myriapods. all could have evolved out of an ancieu
ire thai l.nislacea compi ise a paraphs le| ic (axon and insects tn
li . ! i
.1
ii
;iu
UNHWKI.IM;
MKTA/.OAM PHYI.()(;KNY
Despite great progress made in zoology during
phylogeny. For example, whereas some molecular
the 20th century, there remain many fundamental,

unanswered questions concerning metazoan evoliitionary history. The origins and relationships of
uianv annual phvla remain imcleai oi in dispute
In large part, this stems from the challenge of recovering unambigii i |l I
i ii signals from
ancient lineages. Recent molecular and paleotitological studies suggest that major splits among the
Metazoa occurred in the Precambrian, some perhaps nearly a billion years ago (Wray et al., 1996;
Ayala et al., 1998; Seilacher et al., 1998; Li et al.,
1998). In part, it may also be because the field of
*<''** havr supported the long-held close relaInmslnp between annelids and arthropods |\\ heeler
et al., 1993), recent studies have not done so (Lake,
i" " ; '
i
1'"' Kernisse, 1997; Aguinaldo et al., 1997). Furthermore, the discovery of
new nun ilph
i
din i
nnd un< nlal body
plans, continues to occur. The first edition of Linnaeus's (1735) Systema Naturae listed 14 groups
that we now recognize as distinct animal phyla. To,Jay, we recognize 34 animal phyla. Three former
p|)y|a haV(. rerent]y ],et,n sunk: Pentastomids are
m)W place(] within the Arthropoda (aHied with the
comparative morphology has lost popularity (and

employmenl opportunities). And finally, the emerg^fiî5-.'"I; ' . " '" " .
T if.i'fltlT
the data
alyzed and the phylogenetic inference methods
used. For example, prior to 1997 most molecular
uudvses urn I isi on small numbers of taxa and
1
e. usually the inherently problematic 18S rDNA gene. Recently,
however, new (and I irgerl m. ieeulai ial i sets ha v.
r conserved nuclear
genes, mitochondrial gene order, and gene duplication data. Because it is unlikely that a single
gene will recover the full phylogeny of Metazoa, the
future will no doubt see analyses of multiple gene
sets.
MaxiUopoda),
and vestimentiferans and pogonoph-
orang are nQw regarded as annelids (probably high.
^ modified P^haetes) (McHugh, 1997; Brusca &

Brusca, in press).
Most of the large-bodied animal groups were discovered by the end of the 19th century. We are now
rack of discovery of microscopic m<
new animal phyla have been disct
1956: Gnathostomulida (1956),
(1983)' and Cycliophora (1995). There is a correhition between the discovery of new animal phyla
and their body sizes: phyla described in the period
of 1901-1920 have maximum body lengths of 310 mm; phyla described in the period of 19411960 have maximum body lengths of just 1 mm;
ported in part by an NSF-PEKT grant (DEB-9521649) to the author. Special thanks go to the indefatigable Peter Kaven
for encouraging the writing of this paper.
-Columbia University. Biosphere 2 Center. P.O. Box 6,89. Oracle. Arizona 85623. U.S.A.
87: 13-25. 2000.
pi... la ! BClibed in the 1980s and 1990s have maximum body lengths of less than 0.5 mm. Most of
the small-bodied phyla are meiofaunal, although
cycliophorans live as commensals on the mouth appendages of various marine crustaceans (Funch &
Kristensen, 1997). The discovery of these minute
> reduced or othen
^^Ph*
Tiilobila: Karlx Cambrian In IVrmian
plio-ana: barb Ordmn lan/Silurian lo present
n\ |>t<riia: l,;ir l\ (>rd.n i< ian through mid IVrmian
I'vcnoiionid >:. I "..-MMIMI I.- fir
Unislac. a: Karly Cambrian (.
Ilevapoda: I .ovver Devonian I
\1vri; jFoda: I f.f.n îlnri, i !;
lecular biologists have not yet extracted gene sequences from them. I predict that the discovery of
hrf-ctCtuSCPiC
PHyla Wm C ntinUe f r 3n0ther
ReC6nt W rk Wa
( ^ner'
1996 SU
> êstS
that even
, ;,'
,.
..
i
,
1 he . lialleliê- -I liriMVelinj. ..llllli.ll I.IIVI.IL'.'IIV
.
, . . ,
,V
i
are not unique to molecular b.ology, small animals,
die I
.
i i i
eanibn n i in in led
^ Crustacea>
s
!""-
kii"F J
L i

111
1- TV.
' phylogenetic issues at all levels. The
evolutionary history of the Arthropoda has been one
of the most ehalh _ g issues hi. gists sti
with throughout the 20th century. What follows is
an update (as of mid 1998) on what we know about
arthropod evolutionary history.
v er S
'T\
L- I
. i_
I J .L
|!|
""
'
biologists have asked the
question, "How has die incredibly successful diversification of arthropods conic ;ihoul?" Wli\ are
there so many arthropods? Is there something "spe
cial" about these animals? What is the phylogetictie fusion ol il* \ ft I rnpoca/ Sp. c licalK. arc
the arthropods monophyletic and what are the relationships of the major arthropod groups to one
another? There have been four great challenges to
LRTHROPOD EVOLUTION: BACKGROUND

,,,.
,.
,.
lliei. re live eleark distinguished group-.. irinn Is: Inlobitcs (exlinct sine, the end of llie l'aAnnn J
u J
\ /-U r
-r
-ozoic; ~ 4000 described species): .heln ci i|..rmes (horseshoe crabs, eurvplends. arachnids,
pvenogoiiids:
/b.OOO described living species;-;
crustaceans (crabs, shrimp, isopods. and I In u kin;
~ 50,000 descnl- d ring species); hexapods (insects and their kin; 878,000 to 1.5 million desci ihed liv ing sp< cies); and m\ riapods |eeiiliped< s,
millipedes, and their kin; ~ 14,000 described living sp.ee les). \ml, ihcie are two lose a.lie- ol tin
arthropods, tardigrades (water bears) and onychophorans [I'fripalns and their kin). The close re
lation-hi bet
illi In,in
d i and the ArthropBrusca, 1990), and recent molecular work co
lies |o -aipporl a sister -gr. 'lip lel.ition-lnp be|u,.,,
.L
u i tn
\ i i^ TL
,H S
r
v'
'
I J
' .
'W
'_
. '_ ' '
llion described arthropods, known
.
i
ii
.
roni viiliia
I
roriin.'iils .
I
mates
,
-1 1
1
1
>
.,
ol uii.lcLed
din.p... - I.--, i nge from 3 to
..
rp,
Ji
j /rp , , ,,
lm
100 million. The arthropods I ladle 1) comprise
about 85% of all described metazoan species.
The arthropods also encompass an unparalleled
range of structural and taxonomic diversity, have a
rich fossil record, and have become favored animals of evolutionary developmental biology Arlhro-
i
rl\
'
"I I'M lal< ^t I'ni
i
i
irllrroix : I. a perhaps
I""- ' "-'- '" "' ^'-' '""1 "> - "I"-' stions. (1) I ntil
,
, ,
/
.
, ,,
:. .
"'^ ,:'! hvpelh.-i - "'" "''" I'"' evolution based
. . ,
,. . ,
*
r
/o\
principles ,,| ,
|
a l;
We have a very incomplete understanding of arllnopod d-ve|opnii ni. il i. igh this is niprnv mg
<I ii. klv unh the adv n! ..) irii.li eiilar d. vcl..pmi nlal
biology. (3) There has been a paucity of comprehciisivc studies based on fossils from the earliest
.u-i - ..I .nlhii.po.l cvli.li-iii i|al< I'lei anil.naa and
early Paleozoic). I I) It is ap; ircnt d ! h Ji l< < Iof liori..p|,i-v CM--; .,nioi _ ihe . i r 1111 > -| > I - In |ii-t
the past 10 sears, ma or iiis< nveri.s iiave begun lo
address ach of dies. . halleuges. as discuss, d he
Work by the great comparative biologist Robert
Snodgrass in the 1930s established a benchmark
'
'
II"
'
n.-h. I ihl< 2 s us a
,- all 1.11 .11r lli<
i a i i ii
i
i
e , assiti
hi e.i i.., \- at
a that
iiai
F the arthropods
tInn. and il
=* this clas'-ih
-.till finds in most
,11^,0,
^
r
iti...leu. l.iologN (e\!l.ooks. 1 h. Snodgrass
classilie
,
.
,
,
,
cation emh
'
(1) Arthropods comprise a monophyletic taxon.
(2) M
i] ids and
I
n i sister group, a
taxon called Atelocerata (= Tracheata, or Uniramia of some authors). The Atelocerata have
been united by several seemingly powerful at-
iss l\cnogonicla. I
(a) A tracheal respiratory system.

(1)) Uniramous legs.
(c) Use of Malpighian tulmles for excretion.
(<1) Loss of the second head appendagesthe
second antennae (as the name Atelocerata implies). Vestiges ol the anlagen of this appendage
can he seen dining the embryogem ol some
insects (e.g.. Shai.n I'' > '. Umkinosei !'>(>>)
(3) The Crustacea and the Tracheata form a sister
group. the Mandihnlataa name thai Snodgiass himself coined.
for a bnel period ol time in the mid-centurythe
concepl ol a po
ha
oned
mainly hy S. Manlon and l>. \ndeis,,M. .-moved
some popularity (Manton. 1973. 1977; Manton &
Anderson, 1979; Anderson, 1979), and Anderson
view of arthropods placed the rmriapods, hexapods,
and onychophosis in a separate lineage (Mantoifs
phylum "Uniramia") \Mlh an origin apart from the
rest of the arthropods. However, this idea, based on
Hawed phylogenetic argumentation and a
\i\r Hi. mors of scientihe testing and modern
......
. . ..
f
Lixi
metliods ol plivlogenetic inlerence (see below). In
, ",
i
. irv,
addition to plnlogenetic analyses, studies o| Permian diaphanopleroid insects (Kukalova-Peck,
,,
.
,,,-, ^ , i , ., , , .,
i
1991a. I>. 1992: Kukalova-Peck & Brauckmann,
.
,
,
...
1<wi
1990) have shown thai earlv pt.-i \ LM.|.-> |.I..|MI>I\
possessed polvratnous appendages, further underniiuing the Manton \ndeisi.n I niramia hypothesis
Additional sup|)orl lor arthropod monophvlv has
come from studies of compound eves using a mono-
nn.il nli
i < d J_> i i
i
tein (3G6), to crystalline ccr.es, ,
elements in a variety of insect a
inas (Edwards & Meyer, 1990).
It was not until the late 1980s that Snodgrass's
Ion
n
i
to he seriously questioned with: (1) the appearance
ol explicit n .
netic analyses, (2) the discovery of the amazing potential of homeobox genes in arthropod development and evolution, (3) the emergence of
i >l. . ul.i :, i-e i <'.<.Ill)] il .11 \ i|e\ eli.nil nl.ll lnol
. ... .
..
'
. .
n
i>: I I i'l!
- .\i ! \ .1 ev:| iisite m-v\ < ai:
. .
.
.
X,
,
* , .
, ,
""^
Pi ,!
Morphological phylogenetic studies of the arthn

pods are summarized in Table 3. Overall, thes
analyses suggest three imp-.riant conclusions:
(1) The arthropods are a monophyletic taxon.
(2) The relah.>'!-i i
Ml. ' iiswicea to the insects
.
. .
..
.
.
0
and myni od
in
tous; that is, Snod,
.
, .
grass s M.,,,,Mm!,la i- a laxon ol questionable
,. ,.
,.
.
'
.
.
.
,
.
,
L
r
<3 ">' "K.nophvlv ol the- Atelocerata (insects \
. " .
.m
mynapods is also questionable.
J
I
>
M
' i _ M
I'''1'
i Hi "
n I is analysis a tiuinher ol arthn>|
i
I si
i longing to the "Vendian lamia," Iroin the latest I'recambrian (= Ediacara Period) that had generally been regarded as
"problematica." I le also indud, ! _ ' u ' i n

thropods, and various modern taxa. He cor
ided
I i
, I
\illi ' ' '
H.I , i I.ii.
i i,
Kdiacataii arthropod-like fossils arc. in fact, true
arthro|iods, and (< | die anoin.docands sand their
kin) fall out very close to the base, and are probably
the most primitive known atlhn-pods \nomalo. at
ids were giant pie,! l ai h. d . c U i in I. i, tl I In v ,i .
known from both the Precambrian and the Cambrian, and they were probabh the hugcsi jriedu'crs
of that time (Briggs, 1994; Chen et al., 1994).
The most recent phylogenetic analysis of arthropods was based on u H itin, i
n< s of (he . < r
tral nervous system (Strausfeld, 1998). Strausfeld
used 100 oonsene, i i il h narte i i I I
of a variety of scj: n.-m 1 , .
lies to reconslruct plivlogcnetii
I n i nd ip> u i:r- lh, riI opods. His analysis suggested that inset ts and < instaceans , ompiisi
are a | >1\ phv I - -I i -onp i... hih-p.-d- and diplopods are not sister taxa), and that pyenogonids
are true cliche,-t i!< - Tl < mr.si tiift.-trt.iril uei;roi:a
- lapoti i[titles of (aiislacea-lnsocta are elements
of the optic lobes
tures of the midlitx
i - ' neuropils associaled with the eoinpoiind eyes. I hi- analysis cori..|>< i it< ' - tdu i in i t',|oLn. I d. M iiptive work In
I
i- I r
In i
oniiecti\es arc pioneered by
i.
.vheteas in die centipede Eth,
,
l.i,.
I, . I connectives are pionrered from neurons in the brain that send their
axons posteriorly, to set up the parallel connectives.
This difference between centipede and insect-crusia- . u \< ntt.tl iicumi- -v-,|, m- is compounded hv
i
II. tn it segmental neurons in
. nh,K d< - i- |i>i < . Ii'l< M in 'i, v dial IOI.IK1 1:1 in
embryonic development of the brain and thoracic

j n J
i - -m_ -i
I il inity between crustaceans and insects (Harzseh et al., 1997; Therialios et ah. 1095; Whitington et al., 1991). Paulus
i I
,
, mphyly on the basis
mi/ation of photoreceptors .m,1 ihi-i - l< -I I il< - . "U in compound and
single -lens eyes. He further noted that insect and
crus|;1icean ommatidia, with their developmentally
fixed numbers of cells, share more fine structural
chara,-ters than either do with the chilopod ommatidia (which comprise .
of elements).
Strausfeld et al. (1995), which also concluded that
MOLECULAR PHYLOGENKTI
arthropod group.
Ml arthropotl central nervous systems use the
same I
lamental embryonic plan of coiistruclion
(Whitington et al., 1993; Thomas et al., 1984;
1
' ' > 'I
'
tilal distim
tion between the early embryonic development of
the myriapod nervous system and thai of insects +
Molei-ulai phylogenetic studies of the Arthropoda are summarized in Table 4. Field et al. (1988)
sequenced a short segment of 18S rRNA but used
representatives ol |tis| 10 phyla (only 4 of which
were arthropods). Despite its limitations, the Field
et al. work was pioneering. Il was the first molec-
crustaceans was recognized some time ago. Whitington et al. (1991 I lourid that in inserts and cms-
ular phylogenetic study to test the monophyly of the

arthropods, which it supported, and the work ini-
Arthropod Biodiversification
Hexapoda
(Tracheata)
\\ heeler et ill.
Wiiuiepeniiinekx e
Frie.lrich & Ta.il/
l;;s ,l>\\
KK-la + I'(
IMS rl)N\
a stream of follow-u p studies, continuing to

IS rh"\ \ sequences, and later the 18S rDNA
tself. Each subsequent study lias tended to
ore taxa and longer lucleotide sequences for
a base, but until ven recently most also continuec to rely on the 18S g ne. Problems associated
witn ili li:S -HI.-, n>.' ..: short gone sequences.
and s ingle-gene phylogen -tic inferences are well
know and need not be repeated here. Furthermore, although there are now over 300 metazoan
1 *>S seq iei <- ;r, lilabl. . nost published phylogenies have been based on fewer than 20 sequences
(Eem sse, 1997). This is despite studies that sugdated
use 1
gentuse ir
curat, k identilv ihe rout node of a large lac. (I .e

cointre et al., 1993a. b; Sanderson, 1996; Hillis,
1996). In spite of methodol..: -.1 and
firnblenis. inn- n:olecidai stud es are begii n i:g
to converge on sin . -i.n I
a I is ms II '
as Spears and Abele (1997) pointed out, ". . . in the
crusade for understanding relationships among
emstaeeaii aii.l olhet arthropod lineages, the rDiYA
data represent but a relic, and not the Holy Grail
itself."
The most recent 18S sequence data suggest thai
insects share fewer -im lariti.-s with tin myriapods
than they do with the Crustacea. Spears and Abele
(1997) analyzed 31 18S s
suits suggested that ;
were mo >ph\leli< \\''ien ill<-\ '.move. I the ""prole
lematic" long-branched crustacean taxa iHemipe
dia, Cephalocarida, Mystacocarida), a myriapod +
chelicerate clade emerged first, with insects as the
sister group to a paraphyletic Crustacea. The

Spears and Abele analysis also strongly -i,\ nl-'d
malacostracan mnnophv l\. Kernisse (1997) analyzed 103 sequences and concluded that (1) the
Arthropoda are monophyletic, but only if the tardigrades are in.
<> .1-1
mother 18S artifact), and (2) hexapods are more closely related to
crustaceans lliai ih--s an l<> m\ napnds Keîm and
Shultz (1997) made a complete and welcome break
with the IMS <;eili . Using sequences from Iwo nlhei
11ucleai genes, the elongation factor (EF-la) gene
and the RNA polymerase II (POLII) gene. These
trees w.-re robust . > tne-i l\ u; agn < IT eril --. ill lh<
18S work, concluding that: (1) Arthropods are
monophvletic, (2) Crustacea are paraphyletic. and
i3l insecls arc not the sister group of the mxriapods.
but arose from within the Crustacea.
Re < lit work !>\ I icon ei ;d. ! ]'0.> examux d I i
gene sequences, but the linear arrangement of mirial genes. This new type of data corroborates the gene sequence work and recognizes a mitochondrial gene arrangement that is unique to the
In summary, the majority opinion from the molecular research, and the most recent opinions from
both the morpln
cular work, recognize four key features in arthropod phylogeny:
(1) Arthropods are monophyletic.
are natural groups.
(3) Crustaceans
(4) Crustacea are Id
nsliln
I In
taxon.
_
,
,
, .
. .
n.
These last three conclusions are in conflict with
,_
.
. ,
.
, , ,
rp,
l;>0 \< n- i m< i ! Ill . [ s< .'I
I. I i
I ' mi
mi
/ ..
..
.
r .
,.
,
piofouml mipbeaii ni- .-I lne-e n< w -lihli- s ,n.
Ili.i!
\
, , . ,
.,
.....
t u- mom ho ogu al attributes Imkmu insects to mu
,
. ,
,
,
l|"
K
1-
0 U-'l
I
,6 .
'II !
..
L< IM . ,
& Ii ni
I HI
x
< gs Ii h ill - i. in I\I lj

il. il
.
,. '
*
insects an a.tualh "IKiug <! Mac-aiis
,
,
same sense lliat birds in Ilviny B reptiles)
F
;
IIIOUS
. .
i 1 I il
,
;11. ihe
EMERUNG VIEWS FROM DEVELOPMENTAL STI DIES
The unique combination ol segmentation and

jointed appendage- in- II ..
nhmpods to develop modes of lot
K
region specialization, unavailable |o other melii/.oan
phyla. We now know that the fates of these segmental units and tl
pp. i
_
ire under the
ultimate orchestration .
nii< . i
.nes. I'he-e
genes select the critical developmental pathways to
be followed by cells during morphogenesis. Homeobox genes determine such basic body architecture as the dorso-\. i
I ni In
i.
.
oi
body axes, where body appendages form, and the
general types ol app i
'
nn (\\ernf A
Patel, 1997; Panganiban et ab, 1997; Shubin et ab,
1997). Homeobox genes can either suppress limb
development, or iiiodih i to i r it. alternative appendagi morphologies \ rnvviii. body of evidence
suggests that these unique genes have probably
played major roles in the evolution of new body
plans among arthro| : u<
i \1. i/oa in general
(Davidson et al., 1995; Williams & Nagy, 1995;
Panganiban et ab, 1995).
The degree to which homeobox genes have been
conserved is remai'.
nd n .
.1' ihem probably date back al l<
<
i for exam
pie. homologues il fn /' - (, gem seem to dictate
where eyes will d
ill
n al phyla. Paxcts) and deube experimentally interchanged and still function
correctly. Homeobox genes modulate the expression
ol dozen ni nn i n II i, <] i, i i d.
lopmeii
tal genes whose prodiiet- I
[ih.genesis. The
profoiu l.-i iitiou
ol. alia >l ii.nin .!
n.-s
lies in this hierarchical nature. Variation in the output of these multigene networks can arise at many
levels. simpK h\ liiik.-riiu- with lh<- ielali\e liming
of gene expressionan evolutionary process we
know as heterochrony. To understand the profound
potential of homeobox genes to drive evolutionary
change, considei th
I
>
i<
B5 I 7(1 dillereiil
i. - i ghl 1>< i. gulaled b\ the
product of a single homeobox gene, the llltrabithorax (Ubx) gene (Carroll, 1995).
A good exampf . !
I ill. i
,
i
i >
*
.
.
,
.
\ '
li" ii 'I"
i
null., ili I II ii
i ili
. , .
, , , ,c.
.
,
l
insects. \|
I
l ,-s n) oeeiu on lai
\ae ill \arniiis insects m several orders, and tnev
'"
'I
...
erpillai-
'!..!- .I' Hi. .-.I. i I |...:..|ilei-.i, i.e.. catAll

\l :..I-UM
111
. In
.u
.ilmosl
_ 1
eeilainU
,
ni
lots. Hence prologs
III,!, ll.lM I. ap|
'ili : 111 -il. i h.; . Mi- .1- il . il < l
'
\l
,.
,
.
doptera through something as simple as the de-reII
F)ressio" of an *"H-t^stra] limb development program

(i.e., they represent an atavism). We now know that
pro]. >, f'oi mation is initial. J l>\ a change in the regillation and expression of the BX-C gene complex
(i.e., the Bithorax complex, which includes the Hox
genes I in aha 1 and >ii>,iil\ d i tig emhmigenesis
(Carroll, 1995).
Molecular and dc\ elnpmeul il bio|og\ abo seem
to haw hiok.
the arguments over
niigui- <>! uniiamoii-, and buamous limbs (e.g., Popadie et ab, 1996; Panganiban et ab, 1995, 1997;
Shubin et ab, 1997; Emerson & Schram, 1997). We
now know that limb branching is a second-order
phenomenon, probably orchestrated largely by the
homeohos gen. Dishil-h-ss (Dll). II,i- -ingle gene
initial.-. de\cl..pinenl ol unbranehed limbs in insects and branched limbs in crustaceans. Antibodies that recognize Dll proteins show expression at
the tips ol insect limbs and also in biramous crustacean limbs (Panganiban el al.. 1()(>.>) brain he.I
limbs an formed when the nine is expressed c<topically in Drosophila (Diaz-Benjumea et ab,
1994). In fact, Dll occurs in many animal phyla,
where it is expressed at the tips of ectodermal body
outgrowths in such dilfeienl structures as the limbs
of vertebrates, parapodia and antennae of polychad, worms, lube feet of echinoderms, siphons of
timicales, and appendages of arthropods. Furthermore, recent work suggests that whether an arthropod mandible is "whole-limb" (i.e.. built ol mam
segments) or "gnathobasic" (i.e., built of only the
basaluiost segments) also depends on the expression of the gene Distal-less. Thus, Dll is expressed
i I
I
I lor multisegmentcd) jaws of' myriapods, but not in the griathobasie jaws of crusta<-eans and insectsstill further testimom to the
probable sister-group relationship of insects and
Crustacea.
T|IK
PAI.KONTOI.OGICAL DATA
Recent work has shown the fossil record of arthropods dates back to the early Cambrian, or perhaps the late Pieeainbriaii \nd. bv the mid-Paleo-
Arthropod Biodiversification
TableS.
Someimpo, tanl Pro umbrian and Cambrian arthropod Lagers^n fa,
Name
Age
Principal location
J | g
Upper Cambrian (-510 MYA)

Middle Cambrian (-520 MYA)
Lower Cambrian (-530 MYA)
Arthropods arc also the first land animals |',>, which

we have a geol .
I ibandeira et al.,
1988; Kukalova-Peck, 1990), and by the Late Silurian the fust i.-tn-sfi all scorpions and mvrianods
crc a In a<l\ preset t. In lac!, hotl; t -i r< stnal audi
marine mvriapods have been reported from this period (Almond, 1985; Hahn et al., 1986; Labandeira
et al., 1988), although molecular data suggest that
myriapods might have arisen as early as the Cambrian (Friedrich & Tautz, 1995). The first centipede
fossils occur in the Upper Silurian (~ 414 MYA)
and. alone with tt fgoiioi.ulnd uaeltmds. , a , t it.
|0()()|. The first millipede fossils ne< in in Devonian
deposits (Almond, 1985; Robison, 1990); they are
similar to ihi e\l m< g. mis < ;<t!<-:\n.-,,..s 'M . e ,-\
al., 1984) and are contemporaneous with the first
terrestrial mites, pseudoseorpioiis. and s rp:om
(St0rmer, 1969, 1977; Shear et al., 1987), as well
as the first hexapods (Greenslade, 1988). The earhesl MIIPWII fossil hexapods in hristlelails and eo|lembolans iroin ."V'0-million \ ear-old (,asp< r riu I
stone (I .ahandeira et ah. l()8oi. Sen > good re, oh
of these early creatures now e\ 1st. and I he presence
ol these predatoiv arthropods suggests that complex
terrestrial ecosystems won- i; place a I least a- curb
as the late Sihui. u l'< in ip- iln n .-I i up. 1 ml
ancient arthropod basils are those m which e\en
the soft parts of the animal were preserved- the
so-called ancient Lagerstatten (Table 5).
I h.ese ancient fossils >ia\ e p ished die a; " oi oi
igin for the arthn p...| |. k ! .. I
i i
MU
and den pro', me its web M'.., .ISV laipott.i'if d -.\.t
on earb arthropod anaiomv ai d evol iti. n. I la sextraonlinai \ :aima- an i ow : ling as that Cms
iaeea pionahl\ predate the appearance of trilobites
ii tin
<-- I i. HI
i II in. ii
< - to a long-held
belief that trilobites were the most ancient arthropods. The recently exploited Chengpang i.nma oi
south China is Lower Cambrian, about 10 million
years older than flu \11- ii 11- (ambti.m limg. ~Shale fauna (Chen et al., 1994). The Chengjiang
fauna is very wel | esei ed ad neludes ,i
,|
100 species of animals, many without hard skele-
Southern Sweden
British Columbia
Southern China
Ediacara Hills. Aust.
gess Shale, and it de

were already far advanced by this early date.
The spectacular recent discovery by Klaus Mtiller and Dieter Walossek (Mtiller, 1983, 1992; Mtiller
& Walossek, 1985; Mtiller et al., 1995; Walossek
& Mtiller, 1992, 1997) of microscopic arthropods
from the Upper Cambrian Orsten deposits of Sweden, has brought to light a rich fauna of minute
crustaceans, crustacean larvae, and various cms
taeean Ilka irth
\
i
I
i
i I
is Skdra, a cephalocarid-, or mystacocaim IM'
adults have been recovered (the nauplius larvae are
OIIK a (ample hundred microns long; adults air
about 1 mm in length) (Mtiller & Walossek, 1986).
SLuni. and main other Orsten ( a ustacea. were sure Iv "iciot HOI d arum lis u< | nrilih. modem m n n.
mi lofauiial crustaceans.
Fossils from this Cambrian site in Sweden have
been collected since the days of Linnaeus, who acluall described I u irsl fossils from this area in
1757 (trilobites and conodonts). However, a brandnew kind of collecting began with Muller and Walossek s work in the 1980s. This new Orsten material
is all microscopic, three-dimensional fossils. The
f >, rib p<
low little or no signs of decomposition. Thev preserve details less than 1 micrometer III si/,e (e.g., elltleillar pores, the bristles on
setae). Do/ens of Orsten microcrustacea have so far
been described. The recovery of these 111 ree-d imetisionally preserved animals and the developmental
series that have be. n lound (with successive larval.
in ml< md .II In li
us m animals |, ~s 11 I.I M I
mm in length) have provided us with information
on the detailed i
-arthropods. The Orshows [| ;i; ! JIII,! i mi < .ri.st.n ea a id ad
the a
pound eyes, a head shield, naupliar larvae (with

ages on the second
i I Hi
tes (tin s
Taken together, this recent paleonlological work

corroborates Whitinglon's observations long ago
al
III. r.iiire--. Shale lauua. thai during Cambrian times the non-trilobite arthropods were both
morphologically more varied and tnon- numerous
than were the trilobites (despite popular belief). We
also now know that arthropods have probably bee.
the dominant animals in terms of species diversity
localities dial have vielded p< ntastomids, and thus

gaoled as parts ol earlv
lish-likc vertehrates)
mids.
TllF. ()\n CHOI'IIOH \
As wi,1
< l-'nastomids. onvchophorans, too, were
l>art (,< t,,(' blazing, early-Cambrian, explosive ma'""' 'hvcs.heation. They have been found in Burf?-'ss Shale-ivp,-faunas al s<-x.-ral localities, in Cam-
since the Cambrian. Arthropods comprise over onethird of all species described from Lower Cambrian
l
>"1' <UV** <'"" <;1""" and Siberia, and in the
Relish (hstrn lain,a (\umguaug & Weiguo, 1988;
Xiaiiguang i\ Jiiuviian. I'l.'l"': bainsk.'ild <X Hon.
Briggs and Fortey (1989) cladistically analyzed

23 of the Cambrian artl.ro,
taxa. plus 5 extant
groups. Their tree placed the Crustacea at the very
base^ as a paraphvleli, sequence ol lava, and
1991
>- A,1(1' w' ow k,1,,w ,hat Conway Morris's
'"""'ll "'""-'"" '<" "I IMh'cigenia (from the
Bu,
^'ss S[ialt'> ha(l the animal turne<l "fs.dc-down.
l^",iskr.ld and Hou (199 ]) recently turned Hallu-
placed the trilobites and chelicerates neaV die'top

of the tree. The most recent molecular work does
"8" over a"d found a se<(mtl Pair of le8s' co<luillu

^ " Mas a" "xhopl.oran with long dorsal
not conflict with this tree, in viewing the Crustacea
s )in, s A,1(l th( re is now an

l
' "
'
<>vchophoran known
from the Chengjiang deposits of China with side
plates and spines (Ramskold & Hou, 1991). Aysheaia (also from the Burgess Shale) was
initiall\
described by Walcott as an annelid, but it, too, is
-cub.',| species, all of which infest various telra|)ods. including two cosmopolitan species that
lilies liiimatis. Th.- blood-sucking adults uihabil ic-piralorv tract-, of their hosls. where they anchor
ihemselves bv means of then hookhkc head appendage-. I'MI veais it was |..-lie\od that pentastomids were allied with the onychophorans as vermiform, pre-arthropod creatures. However, several
recent molecular studies (using 18S gene sequences) have revealed the pentaslomids to be hi-hlv
modified crustaceans (Ab.de et al., 1989, 1992;
Garey et al., 199(>). Corroborative independent
work over the past lew years has come from cladistic analyses of sperm and larval morphology,
nervous system analomv. and .uli.-ular fine structure (Wingstrand. 1972, 1978: Stmvh. I 8 I: Slord,
& Jamieson, 1992). Furthermore. Midler and Walosseks work on the Swedish Orslr/i fauna proves
that the pentastomids (and also the tardigrades) had
appeared al least b\ the I Ippcr Cambrian, long before the land vertebrates had even evolved (Midler
& Walossek, 1988; Walossek & Midler, 1994). So.
we must ask what the original hosts of these parasitic crustaceans might have been. Walossek. Midier, and even Stephen .lav (and.I have noted dial
Conodori! fossils aie common in all the Cambrian
Let us now return to our twe i fundamental queslions regarding arthropod evolu tion: Why are there
so maiiv arthropods, and what is the plivlogcnetic
hislorv of the arthropods? As t 0 the first question,
I propose six < jver-arching seen arios, each complex
(1) The numerical superiority of arthropods is not

a recent event. Recent fossil discoveries, and
mole, iihn .-|... k data, inform us that arthropod
diversification began very early in the history
of the Mela/n;,. m the I'recambrian, and by the
Cambrian lli.'arthropods were probably already
the most speciosc metazoaii phylum on earth,
Arthropods have been on a powerful phylogenetic trajectory for well over 600 MY. They
have had a great deal of time to radiate, and
with the exception of the trilobites and the eurypterids. all the maioi lineages have survived
and continue to radiate.
(2) Their great si/e range, .specially on the smaller
end of the scab-, adapts arthropods for a great
variety of ecological niches. The Cambrian Orstm deposits tell us thai a whole fauna of interstilial/ineiolaunal arthropods already existed
as early i
i
r
smallbodv -size niches are filled in a great
main specialized environment- today. We find
high diversities of minute arthropods in habitats
such as marine sediments, coral reels, among
that Crustacea are a paraphyletic group, and that

the Crustacea and Insecta are very closely related
to one another, hut not to the Myriapoda. In fact,
the insects appear to have arisen from within a
crustacean stem line. Kurt her. recent molecular ami
I0--1I .lata are I..--1 iitiiii- to -uggot that the trilo-
itive plants, and on the bodies ,,| even kind ol

animal imaginable. There are even arthropod
laiinas that live strictly on the gills of oilier
crustaceans (mites and small crustaceans).
Small insects and miles ha\e exploited virtually
every terrestrial mierohabitat available.
(3) The close relationship and coevolulion with
flowering plants (on land) and algae (in aquatic
environment) have been a powerful force in
the radiation of the arthropods. It is not jusl the
insects that have been on a ^.evolutionary tra-
oiu-lucoan> all might ha\e emerged from crustaeean stem-line ancestors. This view of ,1 paraphvletie Crustacea spinning off a series of oilier major
arthropod lineages might explain why morphologists have been unable to come to agreement on the
sister-group relationships of the major arthropod
lineages, lb-solution ol 1111 - conflict will come, 1
predict, within the next two decades, with further
understanding of the genetic regulation of developmenlal processes, examination of new nuclear
and mitochondrial genes (and use ol multiple -,IK
algae as both a living substrate and a food

souree and show strong evidence of coevolution.
(4) The arthropods (insects) were the first flying animals, and the ability to fly led them into niches
other invertebrates simply could not penetrate.
(5) Metamerism (the serially repeated body segments and appendages of arthropods) provides
an enormous amount of easily manipulated
body plan material upon which evolutionary
processes can act. Civen the great age. sheer
diversity, and 0111 emerging knowledge of regulatory genes in these animals, a high level of
homoplasy is no longer surprising.
(6) The potential for major changes in bo.lv plans
due to variations in homeobox genes, and the
downstream genes they regulate, is just beginning to be realized, but this potential is clearly
enormous. There seems little doubt that changes in homeotic genes over time have profoundly
affected arthropod evolution. Considering the
number and position of limbs in arthropods,
and the flexibility of homeobox and regulatory
switches, il is little wonder that arthropod anatomical diversity seems so endless.
eladislie anaUses include fossil species, partieularly the growing series of Chengjiang. Oish'n. and
related arthropods.
is the phylont the Arthropodsit seems the

arthropod bod\ anil homeobox gene
have produced an even higher level
it! mol< :ularclassifications. Ul the evidence

sts that the arthropods are monopliv letic
ver. fossil data, recent comparative neuroaneal research, and molecular data all suggest
\ Sl>KCl I.VTtox,
The realization that insects might have arisen out
of an ancestral crustacean stem line leads to many
new implications concerning arthropod evolution,
For example, given this scenario, one could search
about among the Crustacea for a likely ancestor to
die insects and in doing so recognize the presence
of a "fixed" l9-segmented body plan in insects and
certain crustaceans (or more likely a 20-segmented
plan in each. kukalo\a-Peck. 1991a, b; Scholtz et
al., 1994; Scholtz, 1995). All insects are fixed on
this body plan. Of all the crustacean higher taxa,
this body plan consistently occurs only in the subflass Eumalacostracathe crabs, shrimps, isopods.
and their kin. Thus, if the insects did evolve from
a crustacean ancestor, one might speculate that
diey could have evolved from a eumalacostracan.
Examining the Eumalacostraca for a possible insect
ancestry, there is only one group that is truly terrestrial, has evolved gas-exchange tracheae (granted, probablv convergently to those of insects), has
reduced/lost one pair of antennae (antennae one reduced in oniscideans. antennae two reduced in
hexapods). and has slrietb miirainous walking legs
(as do the insects)the terrestrial isopods (Isopoda: Oniscidea). Could it be that insects are not only
flying crustaceans, but living isopods?
The concept of a l.umal.i. .->ti.u a Insecta sj>tei
group relalionship finds strong support in the comparative analoniv ol arllirop.id .enlial nervous systerns. Development of the compound eye follows
ill

nii'li.
useets and enmalacostracans (llalnci X Tokai'ski. in press). In
addition, die opin I l>< - i>l | l< r ,
i.-. h and
eiiinahieosliaeans an- distinguish
l>> nested retinotopic neuropils, each of which represents the
whole eye. In these two taxa, these neuropils comprise an anatomically distinct lamina, medulla, and
lobula complex (Strausfeld, 1996). The presence of
these structures in pterygote insects and eumalacostracans was viewed as a homology indicating a
sister-group relationship between these taxa by
Osorio and Bacon (1994) and Nilsson and Osorio
(1997). Further, eum 1 i< -h i ins id ii li.n - t a
been examined also possess a distinctive form of
neuron, called a bushy T-cell, which was first recognized in insects on the basis of its characteristic
lendritii
i
sil ulated near the inner face of the
medulla (Strausfeld, 1976). Bushy T-cells in insects
a close mala
ing differences i
tions of the gone
not support an isopod + insect sister-group relationship. The oldest known isopod fossils are only
300 million years in age (Phreatoicidea: Hesderella,
Carboniferous) (Brusca & Wilson, 1991). However,
a recent anal\
i, an phylogeny suggests the isopods might have had their origin considerably earlier than this (Wilson & Keable, in
press), ami furl
i of this unconventional idea may be warranted.
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. Subclass Branehiopoda. Kongel. Danskc Yido.sk. Sclsk. Biol.-Skr. 22: 1-66.
\iiiiiepeiinii-k\. B.. T. Backeljau. I.. V Mackcy. J. \1.
Brooks. H. de Wachter. S. Kumar & J. K. Carry. 1995.
18s rRNA data indicate thai Aschelminthes are poly. ....I.- \lolrc. Biol. & Fvol. 12: I 132-1 137.
.
. V. Van de Peer* R. De Wad,In. |<)92.
Structure of the small ribosomal sub.mil K\ \ of the
II
-' >
[.'I
II
analysis of the Metazoa. Federation of European Biochemical Societies 309: 123-126.
Way. G. A.. J. S. I,unto,, Kl.ll. Shapiro. !"')(,, Mo
1989. F.arh Cambrian arlhn

I
-,M animal, gen. nov. from ChengPalaeontol. Sin. 28: 207 21.V
SO MANY FISHES, SO LITTLE
John G. Lundberg,* Maurice Kot
TIME: AN OVERVIEW OF
frald R: Sm)th/ êlaf Lr.,\:

Stia.ssriy. (iiid \nthony C. Gilr
RECENT ICHTHYOLOGICAL
DISCOVERY IN
CONTINENTAL WATERS'
The species of craniate animals (hagfishes + vertebrates) are probably the most thoroughly documented of all the large clades in the tree of life.
Yet new species of living craniates are described
frequendy, and most of these are fishes. In a recent
tally, Eschmeyer (1998) found that about 200 fish
species are described annually.
,-,. ,
i ii
-i
fishes are water-dwelling cranial.-s with prima
,, r .
i
.
nent gills borne on the walls of pharyngeal arches
by it hthyologists Chara t. rized u this w.i\. tin total

numl)er of living fish species is about 25,000 and
accounts for roughly 50% of the extant species richness oi e
& Craniata, while the other half are tetraP^8 (Nelson, 1994). Thus delimited, fishes are not
a
>nopMti<- group because then subgroups axarranged along a phylogenetie "ladder" below the
let ra nods (Kiti. I |. I'd
|onl
I
.
, ,
, , . .
however, belong 4to one clade: the Actim.ph-ngi. or
ray.finned fishes. There ^ at least 2;U(M) |mr|
actin0pterygian species (Nelson, 1994). The species
richness of the ray-finned fishes strongly contrasts
with the present species poverty of the other higher
fish clades (Fig. 1).
or pouches. Fishes have median fins supported by

cartilaginous or bony rays, and most have paired
fins, but never limbs bearing digits (Bond, 1996;
Helfman et al., 1997). Uniquely, fishes are studied
aties Symposi
ii' 
In invilin; us to participate Wc thank our many colleagues

iM-iipl \ll>. iid \kama, Cristina Cox Kemandes,
Steven Norris, Lynn Parenti, Mario C. C. de

l'oledo-Pi,a Cm I'rugels. I' I. I i
k. II
,
, Stan Weil/man and
MI
s rex iewers Kdilors Amy IV
Pherson and Victoria I lo
, V1U<, Press olleied us patient ami v\i>< issi ,1 01. , llin.ii Ii the editorial procc
of the Museum 0/ /
1/
, \, ademy 0/ \<ilunil S< inucs. Philadelphia; a
I..
I
111.I Kvliiii..n.irv llidl,,.v I).,- I iiiwisitv ol \ri/..n.i IUCM.U \n/ona ,">a721. U.S. A.
' Route de la Baroche 12, Case postale 57, CH-2952 Cornol, Switzerland.
Museum of /i,(ilo\. I imersih <>i M 1. III-HI. \tn \i'< MI In: ,: II! I (W, U.S.A.
Department of lcl.ll.Vdl .j . Vn
. 111 VI ,,-uin ol Natural llisloiy. \e Wk. \. u Vdik 1(M)24. U.S.A.
6
Department Of Zoology, The Natural History Museum. Cronmell Ii I. London S\\ . ..HI). United Kingdom.
;
87: 26^-62. 2000.
Ichthyological Discovery
The large-scale -i-ciliij.',i-jiI disl ribiil ion ol li-dies

is strongly bimodal: 58% offish species are marine,
41% (about 10,000 species) live principally in
freshwater, and only about 160 (~ 1%) regularly
migrate between salt and fresh water (Cohen, 1970;
McDowell, 1988). This diversity of freshwater fishes
that freshwater makes up a tiny amount, only about
0.01%, of Earth's water supply. Thus, Horn (1972)
calculated that freshwaters hold a far greater "density" of fish spe.
- hen if;. . . ,-ansgreater by
7.">0t) tin
linl
course, most marine species
live in a relatively small volume ol seawatcr in the
productive photic zone, especially around coral
reefs.
In this paper we focus or' the diversity of fresh, and swamps. In addition to
nbers, freshwater fishe;
interesting
to us because of their trem<
IUS variety in form,
fishes provide evofunction, and habit. Freshw.
lulronai) biologists vvilli son
(Endler, 1983) and sticklebacks (Bell & Foster,
1994), divergence and specialion, e.g., Laurentian
Great Lakes whitefishes (Smith & Todd, 1984) and
North American Great Basin fishes (Hubbs & Miller, 1948; G. R. Smith et al., in press), reticulate
.'011111101!, , i.
( o-L.ii !, tUyeno & Smith,
1972), species flocks (African cichlids, Stiassny,
this paper), and Lake Titicaca Orestias (Parenti,
1984a; Costa, 1997), and the historical developtei of biotas
t s< il<
rami rional, e.g., postglacial age North America (Bailey & Smith, 1981)
to continental, e.g., North America (Patterson,
1981; Grande, 1994) and Africa-South
(Lundberg, 1993).
Here we are particularly interested in
panding knowledge of freshwater fish
amounts, natures, and sources ol recent iefilh\olog

ical discoveries and prospects for the future. Our
first concern is with the new sp ops, newly found
ordinary characteristics of phenotypes and
al histories, and new understanding of the procontrol rates of speciation and extinction. The major sources of previously unseen fishes
are explorations in biotically uncharted waters, especially in remote tropical areas, and in i
to-sample aquati. habitats such as deep river channels, cataracts, and leaf litter. Yet survey work at
, tng isiti d -it. in h as the African Great Lakes
and Amazon margins, continues lo yield many new
species. Unrecognized and even formerly unseen
species are routinely found in the course of thorough laMMiornn -.iiivhe-. . ^.i < i..ll\ in revisions of
species-rich, freshwater groups oi oslar ioph\sans.
atherinomorphs, and percomorphs. Another source
of recent species
- i j
us i o
oi
pi
i 1 pi i. lie.
\p| II .n ol species criteria that eNiplia-i/o diagn..-.i|. his ..r di-lim In.
ol populations over traditional gcographi. all\ wide
spread, polytypic species results in an increase of
ed species.
Following some additional background informai
i-i.-.l iii.iii
i
< ialist, we take a
regional approach lo show, asing fr< shwalei fish di
versity and recent discoveries. Based on our indi-
South and Central America, KottelatEurope and

tropical Asia, Siiassny
Africa. Gill
Australia
and New Guinea.
di clades include species that

reshwater. All
iriipn species reproduce in freshwater; some rein, oi Hi. o wh.-r.-a- ..ifiei- migiale to the sea to
U-i-A. Mod. rn Imiglishes arc restricted to freshwater.
Several spec es ol sharks, sawfishes, aid rays regularly enter freshwater, and the Potamoti
la
are a moderate!) :
I sling rays confined to South American rivers and lake-, S. or.-s of
actiiioptengiaris n< in In diwat. r. I am liai . x
gars, carps, piraitfishes, pikes, trouts,
ticklebacks, black basses, sunfishes,
larlers ci h ids bellas
ml i MI UIIK S II hioti.
success
is measured
by species numbers ami
breadth iif overall distribution, the dominant group

of freshwater fishes is ihc Olophvsi (Osturmphvsi in
older literature). Otophvsi contain foin iiiouophv(carp-. minnows, barbs, suckers, loaches) of North
America. Kurope. \sia and Africa. presently with
roughly 2700 species; (2) Charac.formes (tetras, piranhas), now with at least 1300 species, distributed
today in the Nootropics and Africa, and formerly
extending to Kurope and the Arabian Peninsula; (3)
(iymnotiformes (electric eel and knifefishes) of
South America with over 00 described species; (I)
Sihuilormes (catfishes) currently with mote than
I 100 specie- and an overall distribution including
sils from Seymour l-laml tCrande i\
1086).
Kastman.
Freshwater fishes play important roles in a variety of hiogeograplur -Indies. Some are endemic
markers thai delimit regional biotas. Kisli spei ics
are censused in delei minal urns of regional and
global patterns ol species richness or biodi\eisil\.
Kai-h lade ol lish. - ha- Ii1
i
i | i
history. Many freshwater fish clades are component- ol biotas that share with others common viearianl or <lisp<
I I
.
iapli
11 i i
Mails lish species and higher la\a -one as bloli.
indicators of former connections anion- regions
from watersheds to continents.
Monophyletie groups of strictly freshwater fishes
have special significance in continental b .
phy because they te,|uire freshwater for dispersal.
and thus their distributions are correlated with the
evolution ol I i,
I i a
,i I
I- I In di < i< ,
to which fishes are physiologically and behaviorally
higher ta\a ol fishes are comm.mK giouped according to their observed present and presUi I
histoncal habilal and physiological -aliiulv loler
ances (Myers, 1938; Darlington, 1057). So-called
""primary" freshwater fish groups, such as most olophvsnns. spend then entire lives in Iroshu. !< i hah
itats and are physiologically incapable of coping
with seawaler. It is important to know the phv lo
ubgroiips within
, ade
-how strict primary freshwater distributions (Patterson. 1975; Lundberg, 1993).
"Secondary" freshwater fish taxa, such as cyprinodontiforms and eichlids. are usually limited to
freshwater, especially lor reproduction, and have
figure 2. Kslimaled iimiih. i nl living lish -pecics r

the major freshwater faunas. Ha-c map created hv Vm
Corporation's Palo Alto Research Center, Map Viewer.
their greatest diversity ami abundance there, but

occasional individuals or member species may be
found regularly in coastal saltwater habitats. Secondary freshwater fishes might, therefore, disperse
through the sea. "Peripheral" fishes are marine
groups that include -pe< ics with indiv idua
thai
may move sporadically into freshwater or species
example- include helling-, anchovies, nee Icli-he-.
puffers, pipefishes, drums, gobioids, and soles. Ml
continental ichthyofaunas include peripheral
groups wilh persistent freshwater populations, and
the freshwater faunas of many islands comprise entirely peripheral fishes. I'hc-o are generall) regarded as "marine dispcrsants" but. unless or even if
their closest uiliagroiip relatives arc known to be
resident maiirie la\a. petiphcral fishes should not
automatically be ignored in <
nental faunas.
DISTINCTNESS OK FRESHWATER ICHTHYOFAUNAS
At the scale of continents (and Alfred Wallace's

Zoogeographic Realms) ichthyofaunas differ greatly
ness (Kig. 2). \ustialia and Kauope each have hundreds of lish specie-. North America has somewhat
more than 1000, tropical Asia and Africa each have
about 3000. and there ma\ b< more th u ' '" i-h
species III the American tropics. Kspe< iallv at the
thoroughness of our knowledge of conlim ml Kh
faunas. Illghei level l;iv
line dllleieii.es arc
mostly caused hv the long and distanl isolation of
the freshwater* of most continents. Differences in
species diversity probably have more to do with
tailors that control both terms of biological diversification: speoialiou and e\liueliori. Differences in
the extent of knowledge of species result from different histories of exploration and study, as well as
species richness. It is not surprising that we know
Volume 87, Number 1
more about the less divers*' European. North \mer

ican, and Australian faunas, than the rirli African.
in pi< ill '< i i III -mill American assemblages.
longing to 35 genera in 2 1 mostb marine families)

occup\ rivers and lakes ourrentK or receiitb draining to the Arctic, eastern Pacific, Caribbean, and
western \tlantic. The numerical 1\ dominant families are: Cyprinidac (305 species), IVrndae (172),
The North American fieshwaler fish fauna occupies the N.-arctic Kealiu: from Canada and Mas
ka, south to the Transvoh arm Axis south ol die
\1e\ican I'lateau (Fig. 2). Over 1050 spe ies lc.-..
Fig. 3) in about 175 genera and 32 primarily freshwater families (plus a few freshwater species be-
(75).
iK).
(48), Goodeidae (40), Fundulidae (37). Cenlrarehi
dae (32), Atherinidae (35), Cottidae (27), and Ciehlidae (21). These 11 families make up about 307,
Historical Ecology, and North American Freshwater

Fishes edited by Mayden (1992). Regional biogeography was thoroughly analyzed in Zoogeography
of North American Freshwater Fishes edited by Hocutt and Wiley (1986). Systematic accounts and
distributional records have been documented in
about four dozen r . ion a. pr< neial, or state fish
monographs and the Atlas of North American Freshwater Fishes (Lee et al., 1980). Nine families and
128 genera an- now udoinio to N..rlh \niem ,!., but
some (e.g., Amiidae, Hiodontidae) were more widespread in the past. The principal intercontinental
ii Li- ionships of most of the fauna (e.g., Cyprinidae,
Catoslomniae. Salmotiidae. Ksoeidae, Percidaej arc
with Eurasia, whereas the Characidae, Pimelodidac i vprmoif .uiidac Fiindnlidac Pi fumhiliilac
Poeeiliidac ami ( aehlidae liavi rieotri.pii al relationships (Patterson, 1981; Grande, 1994).
The combined fauna of Atlantic and Gulf of Mexico drainages is several limes as diverse as the I'aeilie diamaia- launa beciusi it- land an a ^ Lata i
and has been geologically and climatically
stable during die Ceno/.oi. . Ih Mississippi liasm
versity; its fauna is the larg. -t uitl
eei
The Eastern Highlands, mostl\ in tin Mississippi
drainage, have the most distinctive fishes with 57
sp.-ei.-s (Mayden, 1985, 1987). Diversity decreases
with distance awa\ from lh< Mississippi Basin
heartland. The vast noil In in gl
ted areas are depauperate I.e. aus<- DI Lug vvinteis ami slow postlaeial r.-eolon ilioi (Fig. 4; see also C. L. Smith,
P)8.')) Western and southern lamias are depaupei
lal,.||K IMM,-.-. Il,et;-.lt Itîntllubb-^ Mill.-,.
1948; Hubbs et al., 1974) and Colorado River faunas, in western Mmtl America, have the low. si diversilv, but highest end. inism (Miller, 19.r>)|, ovei
50%, indicating a high extinction rate (G. R. Smith
Freshwaters of the United Slates were thoroughly
explored in the 19th century and the first half of
ili< Ji>ih n in
\l nl \i n.
nu.iws, and suckers
that are elevated to species status base." oi *'
ph\log. -netic and e\oiulioiiar\ species concepts
(Mayden & Wood, 1995). An unusual recent discovery was Scaphirhynchus suttkusi Williams &
Clemmer, a new species of sturgeon from the Mobile Kasin Molecular data have also revealed di
\erse populations of salmons, tnuils. and wlntefish
es (Bernatchez & Wilson, 1998), some of which are

s\mpalii< I ml rclogioalb diflerent. Some ol these
forms III species concepts based on inferred genetic
and ecological difference- between populations dial
spav\u II different limes and places. With emphasis
on historical processes of origin, however, G. R.
Smith el al. ( iW.Vi defined spi ci.-s ;is IIIK ages separated from each othei b\ geneliealb based inor
|.hologi. al. ivproduc! \e. ecologi. al. oi b.-lia\ ioral
ong-1
North Amen
lis!, f
freshw
Th. iiiostmagiiilieeril.il. Th,/>.>//<ltormr\ Hm!og\
of the Threespim S
ited by Bell and
Foster (1994), and Native Trout of Western North
America, by Behnke (1992). Two of North America's
famous iciieliial fishes and their fossil relatives.
paddlefishes (Polyodontidae) and bowfins (Amiidae), are compreheiisi\ei\ Irealed b\ (bandeand
Bemis (1991, 1998). Also notable as popular as
well as soicutificalb valuaiih Irealmenls arc The
Handbook of Darters by Page (1983) and The American Darters by Kuehne and Barbour (1983). The
faun i lia- aU.. b. n.-tit- d b-.m outstanding e, ,,|()gi< a! and . wilul nar\ lieahses. such as thai b\ Mat
thews and Heins (1987). The field eagerly awaits
the appearance ol the Frrslnviilci I'ishi-s .', \U vim

in preparation by Robert R. Miller.
IJeeause rSj>t-t 11 \IIMT it-.-iii lisli species arc well
deseiibed. llic most i-\< ilitii; rei .nl discoveries arc
nl i u.lulionarx relationships and patterns. New in
skills on relationships are the result of research in
im.leeulai ami ni< \ a I J
I I ngeny, an area of
syslematies substantively pioneered by North
American ichthyologists (Wiley, 1981; Burr & Mayden, 1992). Systematic summaries of most of the
iniporlanl groups can be found in Mayden (1992).
Tin luglici level s\ sternal ics of representative fish
taxa is treated in Stiassny et al. (1996). Nineteen
of die 2 I i n-h.'si N Mill \ii - in an fan i i--s I ,n <
(Burr & Mayden. I)>2 ',Ji \1 ... d
_ ' I
Ingeiietic papers mi North \iintiean fishes have
been published, but much more eladislie work is
needed (Burr & Mayden, 1992: 59). Unexpected
recent discoveries include the close relalioi sli p nl
the live-bearing Goodeidae (Fig. 30) of the Mexican Plateau In tl
i
i
mi! /
petrichthys of the Great Basin (Parenti, 1981; Webb,
1998) and tin- relationship nl
.
Elassoma (Fig. 3R), to the sticklebacks (Johnson &
Springer, 1997). Other relationships, based on DNA
sequences, include spinedace (Hubbs & Miller,
|Mi)U; ai "I < ii k < liiihs among vprunds (Simons X
Mayden, 1997), and Pacific trouts and salmons
among salmonids (Stearley & Smith, 1993; Philips
& Oakley, 1997). In addition, studies of phylogeny
have revealed
ll .
u Hi
<-,.
ogres
sion on evolutionary pallerns of North American

freshwater fishes (G. R. Smith, 1992; Dowling &
Secor, 1997).
Nev\ evolutional ana \ -i-s relate palt.-ms in fish
diversity through time to the geological control of
rates of evolution ami extinction. In leclouieally
fragmented and volcanicalb >
. i
-. Imjli
fns-al ami hVccnl North \ineiicai: fishes stiggesls
that they have not evolved siibslanlially in response
suits are consistent with those based on disemerv
of early to middle Cenozoic fishes closely related
and similar In e\lanl species in North America and
South America (Cavender. 1986; Wilson & Williams, 1992; Lundberg, 1998). Molecular and morphological data in their geological context indicate
thai amnionic change and speciation are much
slower than geological and climatic changes (G. U
Smith et al., in press). These result- surest thai
i les) post-glai lal species assemblages in glaciated
likely to be ecological c
interspecific interactions.
Studies H tales ,.| lish evolution wen- piotiei-red
by Hubbs and Miller (1948) in the Great Basin.
The) post-pluvial r-olation
tin the past 10,0(10 years) of populations assumed
in pluvial times (e.g., Kocher & Stepien, 1997).
Current studies negate the assumption of genetically uniform species (G. R. Smith et al., in press).
Studies of I'lioeem ami I'leislocctie morphological
changes in the Great Basin show that the early,
those documented by Hubbs and Miller (1948,
1974) do not usually lead to new species (Bell et
al., 1985; G. R. Smith et al., in press). The isolation
of small populations in rapidly changing environments promotes rapid changes, but over the long
term these appear to be short-term fluctuations
within slow trends (Fig. 5; Bell & Haglund, 1982;
Bell et al., 1985).
fossil disco\. ii. - -uggesi that tin modern North
i . i I
obably date back more than
65 million years to the Cretaceous, most genera to
the Miocene, and species mostly to the Pliocene or
er than one branch per million years per clade in
rivers
pending on the family) but may be more
rapid in lakes (Echelle & Komfield, 1984). Molecular evolution (Kocher & Stepien, 1997) may be
stochastically constant within 10-25% error; for
certain mitochondrial genes, it varies from 0.5%
sequence divergem < , < t ill on .ears in salmonids
to about 1%/m.y. in cyprinids and cyprinodontoids
(Fig. 6; G. R. Smith et al., in press). The above
estimates mgges thai adaptivt evolutionary responses to the current global ecological crisis are
unlikely.
; of mitochondrial gem
V from 0.5% to 1% per mi
, cyprinids. and cyprinodont
synapomorphies of earliest known fossils can l>e us<
identify the internode segment or part of the lineaj
Prospects for future ichthyological discoveries in

North Viicn-v include some new -p.-. is in Mi - ii o
and important advances in our knowledge of patterns and processes of lish diversification.
The vast Neotropical ichthyofauna, estimated to

contain between 5000 and 8000 species (Schaefer,
1998; Vari & Malabarba, 1998), inhabits the freshwaters of South and Central America (Fig. 2), with
a hauill'il ol . ii I h.U. pun, |,did n'ii-di. -. u d
ernmost U.S. The great major
belong to one of five dominant groups: eharacifomis. -i urilonn-. J.MI uo'ifoni s. v p:ii oiiotil is mis.
or cichlids.
lams Karth"s most diveise i n ci in iisli (:HII .;. lhal
certainlv far exceeds 1000 species. The Orinoco,
I'aiana. ami olhci large, tropical i vis How nig to
the \llantic are also species-rich. Fish diversity
.hops diarpK in the watersheds emptying into the
Caribbean and Pacific, and southward into temperate South America where the taxonomic composition also changes markedly. Central American
dishwaters contain mughlv 'MM) -penes (bussing.
1976). In this region the San Juan Basin of Nica;
-I Iii.- i has the most diverse fauna
with about 54 species (Bussing, 1985).
Neotropical cichlids and g\mnotiforms are endemic, monophyletic clades. On the other hand,
Neotropical chaiacifoniis (Vari iX Malah ri-a.
1998), siluriforms (de Pinna, 1998), and eyprino-
1 iiomis (Cosla. I'98| -ad. oonlam several separnVlv mor,o;>h\ le' ; ~I;!L-H U| - vv itli an oinpleteb
known cxlraliinilal lehilmnslups Some Neotropical
fish clades have their closest relatives of today in
African freshwaters (Lundberg, 1993; Vari & Mal;:: ul> .. I"."1... de I'II aa. \'>,K',): imglish. nrapaima.
etenolueiid + erythrinid and some charamd char,- ilotli s. i!<.I !< .1 . nlllshes. iploclic lold and poeciliid ovprinodontilmuis. cichlids. and nandids. A
lew of the Ncoto rh
. |>
-iid
is are most
elos.-U related to North American taxa (Parenti,
1981). Many Neotropical fishes, including imlividnal species and some small clades, have their proximaie idalm- and presumed aneesln in coastal
marine waters, e.g., river sting ra\s, vat ions herrings and anchovies, drums, soles, nee Iclisl -.
ad a puffer.
el\ -nirprisli g ifiai no eompri lletisive
ad\: nee. i
The ma iv. i ,;,' , ._ . : / '-'. -
I -. lam v, i. P'1*;;)
|" I<> ill. i si lliotoiigli ishngevei retrieved of

'I;-' I'll oniial- .Ifipl e.| !o ill lis[,e~ Hid also oiitailis
an extensive liihliogiapm c.| <!>, nplive n alhvolo
gy. The electronic version of the Catalog has great
K iaeil laled an esi a ale ol Hie historical account
) " pil >ll-l.ed < - , in. i <>: N. olmpie J lislies
Tin symposium vohmie i'in lutein and Ciassijicn
tion of Neotropical Fishes (Malabarba et al., 1998)
contains 28 papers that summarize much up-todate svêmalio \ now le:.-. l high. - Nootropil a
The discovery of Neotropical fish species became
an active enterprise by about 1825 and it continues
at a high rate. The latest ca. 50-year trends in species desi liphon fin tin Y ni o| i. a -i lii il .rni . is chaiai ifortn.s. < v pi modontoids, and
cuhlids are shown in Figure 7 (data from Eschmeyer, 1998). Overall about 1400 species were described during this period, and the vast majonlv 1
these are consiilined valid I sing ihe recent estimates for total Neotropical fish species richness.
In - ai 'inn! oi discov. ; . and des. upturn could rep
resent about 25% of the whole ichthyofauna.
The levels of recent discovery and estimates of
total species richness for the five major groups are
truly impressive. I "In- siluriforms are the richest of
the major Neotropical groups with at least 1400
species (Nelson, 1994). Between 1950 and 1997,
5 3E 5
ill
id
IJ
i *ii
222:2::=r::
r 2:2::
- Year periods ending in date shown

cies descriptions 1950-1997 lor eharaciforms, silurifo
data from Eschmeyer (1998). Kadi whole fish icon r<
.uid new field samples. Thus, any estimate of the

total species riehm ~> ;.! Neotropical catfishes is
now imprecise, but close to or more than 2000 species should he expected.
\1.)1.. ! ,< < <".;. ( i(IO I > Vi eogll /.eci *" i \ ;illi! species
of electric fishes; Campos da Paz and Albert (1998)

al,
t
eed 100 s
iKIIIS (if 3 I liew "', IPTItlligenera were published,
ddilional 32 undeseribed
. ii !- -!il!i i ! I-. estimate
- of \( ntropii il ha; . the high rate i
co\er\ ol lllKli-si 'lit--! -;>ec|< s.
Nelson (19)1, ,
nated an overall total of 1300
characiform species, and Vari (1998) predicted that
far greater than 2000 exist overall. Of these only
about 225 are African. Between 1950 and 1997,
over 450 characiform species were described in tin
, and although annual rates of descripvary, there is no indication of reduction. Experts working with cha: iiomi !a\..noii:\ ate auan
in\ dozens oi undescribed fonns.
uth and Central American c\ prinodontifnnns
estimated at about 375 species (Huber, 1998;
Nelson, 1994). From the Nootropic 203 expriuniloni specie- nave N-.-;I .I. ~ i il.<<I since 1950. and
of these over 80% (166) were published after 1974.
These numbers would be higher if new species in
shared and < '...eh alcd gemaa from Mexico, the
U.S., and the West Indies were included. Neotrop i .i cicl lids are not as species diverse as Uriean
eii'lilids. bin dieii II inihers aie high and nu i.-asiiiKullander's current (1998) estimate is that the total
will be about 450 Neotropical cichlids, of which
more than 100 are undescribed. About 30% (134)
of the estimated total have been described since
1974.
The continuing high level of discovery of fish
species in the Neotropics ina\ he explain.
i\ !><
onil.in i i HI (
- J II onnt of field and
cally complex, and undersampled fauna (see also
Vari & Malabarba, 1998). We could cite dozens of
recent esan p e- uj i aim oi..,-, ral d seo\er\ coining
out of small and nu nl.ni.il |.> Lt-e. in, i~.; In 'd
exploration throughout the Neotropics. However,
the recent history of ichthyological exploration in
Venezuela illustrates the gH\i< Magnitude of discovery, on one Ian
In
< I i
ilK < omplex re
Clonal scale, thai - sli ! possihh in man\ areas .;

South \nieriea. About 30 years ago Ma-. Le< ia
(1970) published the first comprehensive list of Venezuelan freshwater lishes, which included 474
species. In 1997 Taphorn et al. were able to revise
the Venezuelan list Upward tO 1065 species (a
125% increase) based largely on the combined results of much survey work carried out (luring the
mately 25 years,
i.noun-Is involved in <les.nl>
> has increased over the years,
all! gh -' ina\ \\.i\<- reached a plateau. Using
tuple, for the 10
quarter-century peimds beiwcei 1758 and 1990
ihe i. ir !) is nl iiufh-r - ..i >peci. - d< s< lipl nils . re
4, 5, 9, 18, 12, 31, 28, 38, 64, 57, and in the 7
years since 1990 already 54 authors have been involved in dcs. rilaiig characilonns. Kclween ll*:./(
and 1997, 228 authors contributed to papers des. rilaiig approximately (O0 spe. irs of Neotropical
,i- -iliuilomis, gymnotiforms, cyprinodoi lilonns, and ichlids. As expe. led, authorship
prodllctiv il\ of -p, ,.,:-, desei pti>Ti.- '..('(< - [remeil
douslv: the rang, ol deseriplions across aulhoi is
1-102, with a strong mode of 1 description per author, and a medi
. ^
....
. ..
h
id vidu.ils were sole or co-authors of al least 10
species deseriplions and. iciuarkahlv. the total contribution of these 7 persons accounts for over half
(524) of the 960 recent descriptions.
A general pattern of biodiversity is that species
n Neotropical lisli diversity is

vident at different r nks. For example, differences
in tin- amounts ol species discovery among cattish
families are correlated with the species richness of
those families (Fig. 8). The same relationship appears to hold at the genus level with the very large
genera (lot MI,<;,IS, U; >/,/<,',(,, /',-. hi>:n i, ,'.-;.. s, and
W/( of all Neoliopi. a si liriini m sped. - desei ilied during lh> lasl
geii<-ia I > i>i>;,u;, v II \;'ifs\,,'<n :. ,,<,. (\ .//,, I,mm ,
Curimata, Astyanax, and Creagrutus account for
about 30'/ ol the species described in the same
Kxomplifying the great yield of new species that
eai> I- '. laid I-' in d< plh -hid- I i> lativ. U -an I'I
bodied characiforms, Vari and Harold (1998) have
raised the species number of Creagrutus (east of
the Andes) from 15 to 56, a 373% increase. ReI
-pecies level seems more ofher of r
opical fish species. Kullander (1980),
100
descrihed during the lasl ca. 2a vr. based on dala iroru

Ksrlmirve, (I')'),".). \p
\sp,ed,mdae. Al - Astrohlepidae, Au = Auchenipleridae (including \gen. iu-i.lar
and Cenlrom.K hh.lacl. < a
Call,, Iilli\ ida<-, Ce
< ielopsidae. Di
Diploinvslidae. Do
Doradidae. Lo
lx>rieariidae. Pi = IWIodidae, Sc = Sr.ilophinda.-. IV
for example, reported that by 1977, 31 nominal

spe, ies ol the . ichlnl genu*- \pUtOgT01 I
I KJ
been described, of which he judged only 20 to be
valid. In his 1980 revision, Kullander added 18
i,< %
rogia/ed M> overall and
estimated that the g
1997 an additional 17 s
been described, about a 50% i
years following I
hand, revisionary work may s
specificity that might yield a i
number of recognized ham-..
widely distribuu
' nominal species, Silfvergrip (10,, i pm
posed dial onK I I -penes are valid (lh< aulhor
described 3 of these in the work).
Whereas the numbers of new species are high
and the common taxa are becoming more so. the
qualities of recent ichthyologi. al discoveries in the
tity. Neotropical fishes are famous for their diversity
nfd el ami I n| I i. appai Hi New -p. ci. - ilh -'i ik
HI
i -in i
i i i
u- ae < oiiiiuon.
Among characiforms the most unusual recently
found dietary specialist is the serrasalminc Ossubtus xinguense (Fig. 9A; Jegu, 1992), a species from
feeds
phytes, especialK I'nirnii'H'inn. Dining i , .level-
ductive marginal savannas (Lundberg el al., I(J.">7|.

Providing an example of an odd newK dis<-o\ered
structure possibly related to electrolocation of piv\.
The evolution of small t<

is commonplaces among Neotropical fishes (Weitzman & Vari, 1988). It is no surprise that v.rv small
fishes arc discovered relalivclv late in survey work;
40 of the 85 little species listed by Weitzman and
Van were described in the latest 1*5 \eai period,
more than twic<- that ol the previous quarter century, and several more have been discovered re
nils thai (.ill . >s > ... pn
h I ll< 11 si/e criterion of 1_'(> mm. In the Neotropies the evolution of
siluriforms, and cyprinodonliforms, and there are a
handlul ol remarkably small engraulids (Amazonsprattus scintilla, Moberts, 1981) and gobioids [Mi
-|
s. \1\, i-. I''_\i Weitzman and
Vari (1988) pointed out that miniature species of
most taxa live in slow-flowing or still waters. The
most strikingly modified small and mini ilun catfishes, however, are found in >v> iflly flowing and
often deep, river channels. ,\amples of these include the aspredinid Micromyzon akanuii (Fig.
10A; Friel & Lundberg, 1996), a blind, nearly pigmentless. heavilv armored species that matures al
npiixnl lli.- snout, jaws, and gill chamber .il Oysuh

tliat the mouth and blade-like teeth are directed at
the planl- attached to the roekv substrate. An interesting twist was added to tin- ea-c with the discovery of a parasitic isopod li\ in- in the -ill t li.itn
ber of the fish dial also develops a contorted
morphology presumably in response to its host's
cursive ontogeny (Thatcher, 1995).
Most gvmiioiilorms have generalized diets of
small invertebrates ,,, fishes. However, the recently
d. -scribed genus Mn^nsliTmiri has (big. (>l: Lundberg et al.. 1996) includes two species ol Amazon
basin apleionotids dial, with -oallv enlarged jaws
and teeth, feed on Ih. lads ol olh.-r electrn fishes.
Another "new" specialist among electric knife fishes is Rhahdolichop.s zareti (Lutidberg & Mago-Leceia, 1986), from deep channels nl die Or
-o. that
feeds mostly on alloehthonous zooplankton washed
into the river's niaiiislem channels from the pro-
catfish species. Rathycetopsis oliveirai (Fig. 10B;

Lundberg & Rapp Py-Daniel, 1994) is a deep-water
ca. 35-mm cetopsid catfish that has completely lost
its eves and pigment but has eiiormouslv hvpeitro
phied olfactory organs. Theie an- iwo new groups
ol very -mall, mieiophthaliiiic. channel-dwelling pimelodids: llorinnnznn retrupinmitus (Fig. IOC;
Stewart, 1986), with wing-like pectoral fins, and an
undeseribed (lade with at least loin sp. i-s bearing
[In. kciied bones and skin studded with sensory organs.
At the other end of the size spectrum, there are
species. Toledo-I'l/a (l<>'>7: Tole, lo-Piza et al., in
pn-ss) ha- determined thai ihe well-known fangloollicd . vno.lonliiie ll\(/ri>/\ius. long considered
monotypic. contains al leasi lour species of which
two arc mules, rib. d. I.undbeig and Akama (1999,
and in prep.) have identified an unrecognized species ol "golialh" . atlish, Braihyplatystoma (Fig.
10D), in the central and lower Amazon. This important species is now known to reach close to a
new mod,- ..I reproduction l'i>r eharacifoi ins. These

fishes arc convergently sexually dimorphi. . with
males <le\ eloping a \ariet\ (if specialized, court
-I i;> :elaled l alire- (if lh< . ,n .1 'ill- -in li ih bent
fin rays with hooks and fleshy tissues that appear
to be glandular (Fig. 11 A; Burns et al., 1995, 1997:
Malabarba v\ Weilzn.au, 1999). Almost all male
lines d> velop a cutaneous caudal
i! In to pn.diK e a ph. romone, and the
gland -. surrounded |.\ hxperln pined scales and in
senile species putative pumping" muscles. Oddly.
although il e ai ill.- lack an\ n|>\ ions ml niiml lent
organ. man\ (if these species are internal fertilizer-.
The known limits of sexually dimorphic characteristics are being stretched In -nine Neotropical
fishes. He..ail ...II.-. lion- made (luring the highwater season near Manaus have tinned up breeding
ectric fishes and morphologically
nominal Ih'drmo^nalhiis cxoilim.
(Copyright John G.
sus. male alx.nl >(I mm long (reproduced with permission
base*I on a large, hypermorphieally long-snouted

male of A hasrman, (Cox rernandes, 1998; Cox
I .in.m,|e- v\ l.imdbeiu. I()><)). The nominal, monohpie Ocdcmo^nnlhtis ryoi/on is based on large
males of Sternanhogiton ruittcrrri that develop
stiong externalized teeth, perhaps lor use in combat
over mates (Kig. 1 I b; Cox hi iiandes Ox limdberg.
in prep.). Ferraris et al. (1986) described a bizarre
lorieanid armored , alfish, Neblinichthys pilosus
(Fig. 11C), in which males develop on their snouts
Among i
greatest scientific interest ,
llllseell fishes ilia! icpiesenl
Volume 87, Number 1
above the family l
. These discover!
in broad changes in higher classification. The loricarioid Scoloplax dicra (Fig. 12A. B: Bailey cv liaskin, 1976) was first described as a new subfamily
of l.orir atiidae. but was soon elevated to family
rank by Isbriicker (1980). Three more Scoloplax
species were described by Schaefer et al. (1989),
and Schaefer (TWO) determined that this elade is
the likely sister taxon of the vast assemblage of
Lorieariidae + Astroblepidae.
The Trichoimcleridae presently include about
200 species (perhaps over 100 in the large genus
Trii-honnrirriis) arranged in eight or nine subfamilies (de Pinna, 1998). The most widely known triclioiuvct.-rids are the Vandinis" .i "parasitic eatfishes" thai feed within the gill chambers of larger
fishes on blood and epilhelia. (Candinis finally
earned their notoriety lot sup|)osed inarbertent entry into the urethra.- of humans with the first medically verified case of such behavior in Brazil in
1998.) Of more scientific interest, however, is the
recent explosion of systematic knowledge ol the
perplexing diyersity of trichomvclerid-. \lllmugh
16 of the 27 trichomycterid species described between 107.") and 1997 belong to Trichoma hnis. the
remaining 11 ( UY/i) are placed in new or previously rare, poorly known genera and subfamilies.
The highly derived Trirhogenys (Fig. 12C, I); Britski y\ Ortega, 108.*) has been placed in its own
subfamily by Isbriicker (1986). Two newly described genera. Copionodon (Fig. I2F. F) and GUiphyroporna, form a small, pie .i,,morphic elade of
three species that de Pinna (1992) placed as the
sister laxon to all other Irichomycterids. The subfamilies Sareoglanidinae and Glanapterv ginae.
known from very few specimens, contain perhaps
the most extraordinarily specialized and diminutive
eatfishes in the world (Fig. 12G, H). In addition to
major range extensions, in jir-1 the last decade the
ranks n| ||,e sareoglanidines were increased by fruit
new monotvpic genera (e.g., Fig. 12K, L; de Pinna,
1080; de Pinna & Stan.es. 1000; Costa & Bockmann, 1991b; Costa, 1994), and two species and
one genus were added to the glanaptery gines |(|c
Pinna, 1988, 1080; Costa -X Bockmann, 1994a). It
is IK, surprise dial this temaikahle . 1111 p I ideal loll of
triehomvi-tei id diyersity at the genus and familygroup le\e|s has caused a significant revision of our
phvlogenetie understanding (de I'inna, 1992, 1998;
Stiassnv <X de Pinna. 100 1). This case emphasizes
the major impact that taxon sampling can have in
Neotropical fish -v -lemal ies (sec also Schaefer.
1998).
evidence in known elades often lead to altered phyloueiieiie arrangements and classifications. Fxamples include the eatfishes Helogenes, discovered to
be closely related to the Cetopsidae (de Puma iX
Vari, 1995). and Ihpophihnlmus (Fig. 13A), which
is now confidently placed within Pimelodinae instead of in isolation in its own family (Howes, 1983;
Lundberget al.. 1001). The first examinations (only
within the last three sears) of skeletal specimens of
the monotvpic, rio Sao Francisco endemic Com>rlnnrhos conitosttis (Fig. I3B) haye rc\ealed that
this supposed pimelodid. described in 1840, does
nol belong In an\ diagnosed fauub gioi p o| s ,,
iforms (Bockman, de Pinna & Ferraris, pers.
comm.. pers. obs.). There are noteworthy recent
lugliei level < I iseov ei ies in other Neotropical grouj)s
as well. Stiassnv (1001) has found synapi n e f u,
that unite New World eiehlids as the monophyletic
sister taxon of some African cichlids. On the other
hand, there is increasing evidence ol multifile 'ter-taxon relationships between African and South
\meiicaii charai ilorni and cyprinodontiform elades
(Parenti, 1981; Vari, 1995; Buckup, 1998; Costa,
1998).
Thus, at every level knowledge of Neotropical
fishes continues to grow at remarkable rates: niyrlionships. and their richness anil novelty of cha
aeteristics and natural history. Prospects U
iehthyologieal discovery in South and Centr;
\nienea continue to be as high as ever.
roughly one-third ol the Paleare,,,- Realm (Fig. 2).

I he ma|oi groups accounting for most (ca. 80%) of
the lish species are < vpi inidae (129), Salmonidae
(54). Coregonidae (4.3), Gobiidae (31), Cobitidae
(21). Petromvzontidae (11), Clupeidae (11), and
Percidae (11). The "classical" checklists of European Ireshwalci fishes are outdated and reflect a
stale ,.| knowledge and species concepts ol 30 10
years ago. Maitland (1976) listed 215 species for
1 urope west of the I ralsand I 70 species in Europe
Kottelat (1997) recognized 358 species in Europe
(excluding the former U.S.S.R.). an increase of
111%.
Northern Furope, much of it glaciated 1 i ng i
Pleistocene, has low fish diversity, usually with only
2 or 3 native species in any watershed. The number
ol species increases In the south. North of the Alps
from France !< 10
cies is relatiyeb
i
n
in I ul ' ' p
|i aiube basin, with
Figure 12. Ret

radishes. A, \i. The seoloplaeid Scoloplax dirra. seale li.ns I
1976). C, I). The trirhogenine Triilio^cnys loiiuifiiinis limn
'auroglams (rouldingi. ahoul T.\ nun Ion.. freprodu.
seoloplaeid a
h permission from Bailey & Baskin
>rtega, 1983). K, F. The copionodontiiw
Pinna, 1992). G, II. The glanapterygini
Figure l.'i.
I!
ii
: species-poor as.: sp< c i - in ill. Balkan Pi i

in the river basins of the Italian Peninsula, and 26
in the Iberian Peninsula. The only endemic Euroi
I
i
11
HUM., -iritiform Valeneiidae. with two species. This fauna has its elosesl
relationships \ilh \sia. North America, and north
The outlier ,iutie-~ ui European lish sysieinati. s
were provided in the 16th century in Pond.
I.lhl! ,,V pi s<7''i//.% { 1 .V> I) aril! <r.-slier"s ,Vt<7/<Vf/o,
aquatilium (1560) and Fischbuch (1563). Modern
European ichlhvologv started with Peter Artedi's
Ichthyologia (1738), whose system and nomenclature were adopted by Carl von Linne in 1758.
II
thus enjoyed 450 years of stud
double thai <: ati\ oil t eoiiiu ental lish taiina). tun
would expect that
itive. This is not
the ease, and even the most basic question, "How
many species?," has no easy answer. That approximately 2000 names have been applied to European lish spei iea suggests that their taxonomy is
not simple (Kottelat, 1997). As with North America,
the discovers ol pre\ lously unknown fish species in
European waters is now uncommon. How then do
we aeeouut for great increase in the numbei ol \alid
European lish -pe, ies proposed In Koilelai (IW7)?
First.
. Twenty s
; wen' discovered in European wat
"... .....I I"":; .'i.l -.ui, III known species are

still unnamed. These are cyprinids, cobitids, and
gobiids of small to very small size (3 to 10 cm).
Most were found i -< ntheii] Kurn|
i the Hi.'i '. -ii
Italian, and P.alk.n p.-nimula-. hi I' >''':. Iw. o. .v
cyprinids and one new cobitid were described from
the Ib.rian Peninsula.
Second, several
> .-',-> ih, I b\ earlier .t\i
thois arid eonsid. rod nva hi b\ later authors. ! >.,
since been demonstrated to be distinct. This also
mainly concerns species from southern Europe. For
example, the species of the eyprinid genus Scar
(limits ha\ ill I . . I i. ,n. I - - uonymsofS. eralmus. It appears that at least five species
should be reo .gin/.-.I. s..m
' which are conspicuously distinct from S. erythrophthalmus (Fig. 14)
(Iliadou et al., 1996; Kottelat, 1997: 82).
Another interesting case is the goldfish Carassius
iginally described from Germany in 1782.
This species is
id. red as either
the wild form <! the goldfish, a total goldhsl , ot a
liybrid. These theories mior, tin lapanese lilera
ture on morpholep
aid I IHI.IMH- .1 _ ,', di
of Carassius in east Asia, all of them distinct from
C. gibelio (see Hosoya, in Nakabo, 1994, for a summary). They ignore the fact that C. gibelio was apparently recorded in European waters as early as
1549 (Kentmann's Codex; Hertel, 1978), long before goldfish were first imported to Europe in I(>1 1
or 1691, and maybe even before it was imported
from China to Japan (between 1502 and 1748). The
hybrid theory does not seem to have support. So
given our, urn-nl knuwledg. . there is no alien al vflic!i<> as a distil . i spo
Third, application of the Phylogenetic Species
uept (PSC) has played a role in increasing the

nber of recognized species (Kottelat, 1997). In
j view, a species is "an irreducible (basal) chis-
pattem of ancestry and descent" (Cracraft, 1989:

l i Most earlier work on European fishes either used some soit ol in.; '
Ki, .j
I ^| . i, s
Concept or, more frequently, was not explicit regarding concepts, lieliniijons. and eritetia. [inconsistencies in application of criteria are common.
Detailed studies of geographic variation and systematica te\< al Hi'
iisl ,!,> -ii
often has been
imdeieslimal. d. and :l ore i~ ne tl core! cal oi pracSubspe. ics of earlier authors that satisfy species
PSC i
I'llllhc:. si,me Iradillotialb ivr i< ai/ed subspecies
<! imi'.eci s ctlon- oi e itic-. ami tin -nil ties s, |-|
:ie abandoned !, < aiiso lla re i - an sense in recognizing ,itb Iranb ilelined units.
The systematic - ol - ilm mids ami .no gm ids I as
been noloiionsK difficult because of real or perceived In . Ji degrees ol . haracl. I plasticity and iaill
ure to find consistent morphological differences
allioti. populations Mnsi , ai 1 ei in alments ;i\,aided
dealing cnii. all\ with the svsic mai < s oi salmouids
aid
in i I I
i
I I-ailed in a much underestimated number of species. Some "classical"
lists merely lliellliie a single eoi'egoiild I.IXOll. "f ,./
egonus sp." The species-level systematics of these
families is still I'm fmm tes,,h ,-,|. |(1;! a pragmatic
. i db ig >f tl II in i
- | < ssible. Using a few
simple concepts and definitions, Kottelat (1997)
tentali\c]\ re, o<.
! I I in >u |
tic evolutionary units within I Ii,- g> mis t'.otvunttH* n I ,umpe llial
can be recognized as species (cf. 7 species recognized by Blanc et al., 1971), and 27 within the
genus Sdimi) id. > recognized In St< ai lc\ i\ >III In.
I'>'l.',|. ,,nclu: comparisons often show constant
differences in morphology and in color patterns,
and this is now supported |,\ mole, ul.u daia ;.-g.
Bernatchez & Dodson, 1994; Bernatchez et al.,
1992). The distinctive endemic species of Salrrw
proy i<le examples (big. l.">j \iiiin g these, N. trullti
(Klnne basin) am: S. rluxinnrtoa- (Kbum- basin; <>
cur in creeks onb a few kilometer- apiirl alon; il e
land. 'I hesc sp, . i, - |
, .. . . ,
i
l|
treated as different on the basis ol , o|o
a a.I
moipliologi.. i lai I , oiiol.mated nv inolcclllai Cila
Some may object that it will be impossible to
handle the large number of names that application
of the I'Sl ; wil i.rodij, .-. 1 -n- Is. !iowe\.-r. Iiol lue
Figure 15. Examples of three endemic and one wideranging species of Kiiropcan Salmo. A. Salmo rarpio.
juvenile. I.",.', rum long, enileiini In I ake l.arda. Itab. IL Salmo prnsti'rus. 2.'io linn IHIIU. endemic In tin Lake
I'r.spa basin, (aeece \ll,ai,ia-l-\ KOM.
(.. Salmo rho(hniriiM's. .Mia linn long, endemic to the Hhoiie ha-ui. iiughi ;i
l C. (Copyrights
as species. The piobl, n
tificially squeezing all

pigeonhole risks con
about species di
one species are mixed wit
sing e
blui
Sain
n i an\ I ik. s ..! -i i-a'.ll -'. in n in. -lo, ks 11 lilt have
been classically considered ;is different "lornis" of
a single species. In many cases, the "forms" are
not only morphoi . i. .11 did
but b;i\. different habitats, prey on different organisms, have different spawning season- ,uu\ spauian.
in.
and are genetically distinct (but few ha\c been m
vestigated on this last aspect). Under am species
concept. lhe\ are different species, and several of
these "polymorphic species" thus are groups of
ntly, the
- pi'obabb i
of Suhvlinus of bake Thingvalla in Iceland. Europcati examples arc tli<- Salmo of Lough Mclvin (Ireland) and Lake Ohrid (Albania and the former Yugoslavian Republic of Macedonia) and the
Coregonus of Lake Konstanz and bake Thun.
AFRICA
According to current estimates, Africa (Fig. 2)
semi-arid area than

great ma|oi
fish hiodivcrsity is concentrated in the tropical,
moister (and historically forested) regions,
Roberts (1975), building on foundations laid by
Boulenger ( 1905) and Pellegrin (1911, 1921), divided Africa into 10 so-called ichthyofaunal provinces i.-fleeting bioad areas of endemicity. Greenwood (1983) has likened the state-of-the-art to
bioaccountancy rather than bmgeographic anabsis.
recently that the bioge-
and Levequ, {\9<)7) notr(j
harbors some 2850 species arrayed, depending
ography of African freshwater fishes remains poorly
While perhaps not as rich in species as <

ical regions, what Africa lacks in terms of raw num-
f()r m()st
bers it makes up for in an ichthyofauna that ineludes some striking example. ..I e volutiouarv
phenomena ranging from relictual "living fossils"
and strange morpholugu al
al-s. to ..unnmgb
diverse species ||,
,|| sp<-
si()ns ()ften encompassing thousands of kilometers

,. , ,,..,, ,
.,..., but perhaps most import;m)K .,.,. js ., profoun(1 lack 0f ade(,uate hvpoth^ )()[. |[H. ,,,,, I,,,,,,,,,, .|a.m,hips of the spe^^ ' ^.^ these shortcoming^ the
( ^
nation rates and adaptive radiations. It is noteworthy that \friean fish d.vers.U ,s marked In an inMI I
I i
| I I. Li lietK allv
sulaied I;I\;I I isla-s Mich as !s ci rs il'oh pVl lh< !.
lungfishes (Piotopteridae). the butterfbfish (Pantni!o:illdael. weaisiv . icclm elepliailiflshe-. ( Montr.
ridae). the dcnli h \u i i ii (I) n. . i;.i laei i i
ill. II i IK
I I in II i ill i i, i
.
aid km rids
today only in African (reshwaters. Perhaps
of the two major freshwater fish radiations: the otophysan e\prinirb. chara. hums, and silunfoiim
and the percomorph cichlids. In Africa an inter
-mi i! . i HI. mi. i ii. I m . ! I) . en riverine an<
lacustrine con n
- - I1 iornii t ar ilmn
niaied b\ oloph - a - < pniau- . !.
n m i- i
, !rw r|ci ii'i ii" .'a'l'sh f.unil r- M linn:; -. M: > h k
, and Claroteidae), along with mormyrids
cvprinodontiforms (particularly in rivers of west and
central Africa). On the other hand, Africa's many
lacustrine ecosystems, particularly those of the
\axd
are poorly knov/n^ ancJ rang)L exten.
i(.,lthvolamial
(_
pr()vin(.es as currently recognized

^ 1997, for an up-to-date "mn.-rvW
i ip;
KM.
I: [ subd.\ it ling I m i. h
nihil units I n-
.|ueslioiiablv. the fauna is pbvlogenetiealb richest

and most varied in the rivers of tropical west ami
central Africa, with numbers attenuating in the
provinces to the north anil south ol the tropical
band. However, iii terms of raw species numbers,
it is the cichlids of the lakes of east Africa that
dominate the continent's inland waters.
Overall African fishes exhibit a very high level
of endeimsm: almost lOOtf at the species level an.I
upward of 40% at the familial, no doubt a reflection
of the long-term stability and isolation of the Afri-
lationship i- with
\sia (e.g., Notopteridae, Cypri-
""l;"'- bagralae. S, bilbenlae. (ilarudae, Chann.dae,

V'labantida.-. Mastacembehdae. Seatt.phagnlae.
p'lloimlme clupeids. and etropline cichlids), al-
Great Rift Valley, are almost completely dominated

by remarkable adaptive radiations of eiehlid specjes
,m)U
^> links uith Sollth America (e.g., Lepidosiren"lae, arapain.id osleoglossomorphs, some characiforms, siluriforms. cyprinodontiforms, and cichlids)
Given the enormous size of the African conlinent, an ichthyologieal tally of 2850 species, although unqueslionablv an undceM unate of actual
species richness, is remarkably low. By way of partial explanation, the common vision of Africa's mland waters as eha i
great Nile, Niger, Congo (Zaire), and Zambezi Rivers is
misleading. In fact, over 90% of Africa's rivers are
L
1 '. II '.'
I III ii'd nil >
low oulv seasonally. Surprisingly, Africa has more arid and
and Europe (some cvpr.nid genera) are also evident

in a h-w chides. I nfortunately, our current understanding of the phylogenetie relationships of most
African chides is insufficient to enable historical
interpretation of many distributional data,
While the first \li nan fishes to reach European
collections were assembled by the French naturalist
Michel Adanson during his stay in Senegal (1749I7.)."i). much earlv explorali
n Africa was centered on the Nile, a river that has played a major
role 111 the liislors >! Mediterranean civilization (so

Beadle, i"'7i, Ici .in . xccllriii discussion of early
exploration of Africa's inland waters). Daget (1994)
recounted .m amusim
needi.n iti which it is
lailiicd ih.il en ( -i iltr..\ S:iml I lilaiie's 11 lull ilom
the Napoleonic Campaigns in Egypt (1799) his fish
collections were deposited at the Paris Museum
When Ciniei examined for the first time the exIraoidiuaiA l.iclni il'o/yp/rrus), he is reputed to
have declared, "Tin- alum is nistiliealion lot the
v\ lial- \ 1 I In importance of
llilolic i -.lies. ill. teal li.-îi u 1 . <( ni,.drill Vi 1.Ml
1. hthvoiogv aie perhaps best maiked hy the publication of Cuvier and Valenciennes" multi-volume
Histoire naturellr ties pois.sons (1828-1849), in
which about 140 African fishes were described.
Some .">() sears lal. I! .-a I! nil. 1 g. 1 puhl sli, d li
four-volume Catalog (1909-1916) he was able to
record over 1400 species. And by 1991, with the
: iibli. aliori .1 lll a.-1 11 ai . xlirmelv useful series
of checklists (Daget et al., 1984, 1986, 1991), the
tally had risen to about 2850. Although Houl.mgci%
(Catalog remains the only pan-African faunal study,
lished. Two in particular, Leveque et al. (1990,
1992) for most of west Africa and Skein. ; l<n",|

lor southern Africa (including the Zambezi province), have comprehensive coverage. \ :! ! >" 1 l\.
much up to dal< n 1 n-nal inleiiu ilion t- U lie l 11111
in Teugels et al. (1994), and references to major
(visional studies are to be found in Leveque
(1997). As was noted earlier, the great majority of
MM. an specie- an members of just two groups: the
otophysan cyprinids (ca. 475 species in 2.'! an 1).
haiai ilo1 iir- I. h nan.I- 11 .11 nil aiiiuds with ca.
208 species in 39 genera), and clariid (ca. 71 species in 12 genera), elarioteid lea. 98 species in 18
genera), and mochokid (ca. 167 species in 10 genera) catfishes; and the percomorph cichli.l."70
species in 143 genera). Together these seven lamilies comprise more than two-thirds of the contiDespil
LMK.
.it. 1-I1. s. and mans surprises no doubt remain. At the most basic level, monitoring species
numbers (Fig. 16) illustrates the cumulative .lis
covery rates for three typical African lisli . lades
and. as elsewhere HI tropical freshwater*, species
discovers .
MM.
Lake
r 120 stenotopic
rock-dwelling eichlid species (Fig. 17)
nex1996; Seehausen et al., 1998). The qui
pected discovery i.l this extraordinary tad
, not
only d,i- major implications for our undo
cling
of die evolulionary dynamics of Africa'
hlid
flocks (Kaufman et al.. 1997: Turner, 1997) and
their conservation (Kaufman. I(>92: Kaufman &
Ochumba, 1993; Seehausen et al., 1997), but it also
illustrates that even in supposedK n el I-sampled locales there still remain many unknowns.
KipialK illustrative is a iei.nl study oi the ( loss
River drainage of Cameroon and Nigeria. Although
the Cross was considered reasonably well sampled
when Teugels et al. (1992) thoroughly reviewed recently collected and historic.il material in museurns, they found that previous figures imderesli
mated true di\ersil\ In more tri.ni 70'/r

1996). Even after that comprehensive s
taxa are tunniii; up I'or example, Stiassny, S '! :
i. and In IIM.f (in |i. p i are describing an enigmatic new genus of cichlid fish recently collected
in the Cross (Fig. 18). This taxon, which is highly
distinctive in appearance, displays a fascinating
combination of character states that render its phylogene
pioblemalical and may r
in sigi
e eiehlid- la major elade o
ships ,
rican
tance)
of the
that of the Lake Rermin spiecies flock (Fig. 19).
Lake Bernini, a small Cameroonian crater lake of
little more than 0.5 km2 has recently been determined to be home to the continents first species
ll..< k ol substrate-spawning tilapiines. The flock in-
I:
i:
#?
|:
Before 1992 study
After 1992 study
eludes the small.-st known lilapia. Tilapiu .umlrntr.

a species that attains sexual maturity at only about
25 mm. The discovery of endemic cichlid flocks in
small crater lakes in the Camen.onian highlands
provides a marvelous series of models for the stud\
ol' evolutionary divei- li< iilum ai d speciation inechanisms (Trewavas et al., 1972; Stiassny et ah,
1992). For example, Schliewen et al. (1994) recognized the Lake Bermin and bake Barombi Mbo
cichlid flocks as providing the most compelling ex-
atii(.l.> ol pmhahlc -unpatrir speciation known

among vertebrates.
The cichli.l radiations of the east African lakes,
likened to "living laboratories of evolution," provide some of the most extraordinary examples of
vertebrate spe. i il
adaphv< ladiation, and ecomorphological diversification known on the planet
and have intrigued biologists since their initial discovery at the end of the last century (e.g., Moore,
lOO.i; Fryer & lies, 1<)72; Fryer, 1976; Greenwood,
sequencing techniques and analytical methods haresulted m a plelhora of studies ;iiincd at unravelling plnlogonetic. hiogeograpluo. and speciation
mechanisms among these fishes (e.g.. Stnrmhanei
& Meyer, 1992; Meyer. 1993; Kncher et al., 1993;
Schliewen et ah. 199k Kornfield & Parker. 1907:
Verheyen et ah, 1990. and references therein). The
results have heen stimulating to the field geneialU.
have added significantly to our underslanding ol
evolutionary modes and specialion meehanisms ol
the lake cichlids. and have served to highlight the
important roles lor hold morphological and mol. <
t new discovery
among svinpatric species suggests that indi\ iduals

exploit dillereuees in waveform, polarity, and duration to identify ihe species and se\ of signalers.
Plavhack experiments using eompuler-s\ nthesized
FODs have confirmed then importance in reproduetive isolation and sex reeognilinn (Hopkins 0\
Bass, 1981). There are even individual differences
in FODs that are sufficient to permit the tracking
of individuals and their movements in small
streams monitored daily (Friedman e* Hopkins.
1990). thus enabling non-intrusive ecological monitoring of populations.
Electric catfishes (family Malapteruridae) are endemic to Africa and are one of the continent's ich-
t work that coin-
theh peculiar ahilitv !> prodin e -limning discharg-
Another recent discovery < considerable interest

and evolutionary implication s found in Ethiopia's
hake Tana, (lie highland MM ce of the Blue Nile,
In an elegant series of laxon nie and ecomorphological studies of trophic dive ification. Nagelkerke
and his colleagues have est; ilished the existence
of an ecologically and icproduelively segregated radiation of I I spei-ies el the cypiinid genu- Hii'lnis
(Fig. 20; Nagelkerke et ah! 1994; Nagelkerke,
1997). Since die demise of the Lake Lanao cyprinid
radiation in the Philippines, the hake Tana Hock
heroines the planet's only remaining lacustrine cypLest the
lited to Africa's lakes
west and central \irica (Hopkins, 1981; Moll, r,

1995). This is especially well illustrated for species
in the genus Bnaiomxrus from Oahou (Fig. 21).
where 11 new species have heen disco\ered hy reconlini: distinctive electric organ discharges I Uves-Gomes & Hopkins, 1997) and detailed morphological stud\ iTeugels X Hopkins, 1998;
I, ugeU i\ Hopkins. Ill prep.). MotlllMlds generate
elei tne pulses man\ limes per second for purposes
of active electrolocation, and as a coiise(|iieuee species-typical and sex-specific signals arc broadcast
Figure 21. Mormyrid <livorsitv in (lit- Ivindo Uiver (( aho.i). Species-specific Flectric Organ Discharges (K()l)s)
arrayed in middle columns. (With permission and modifie< alter Hopkins. I<l.)
|'\ U|> 1" > >(l\ in Luge - (.< t -1 II i. r i -_ The first species
was f rni.-i 11 \ described 200 years ago as SUuriis
(now Mtihiplninus) rh; in, us. and lor much of the
time since then a single species was recognized.
However, electric oatlishes are widely distributed
across Mil. a. ami earelul re\ is arv work (Norris,
in prcp.i has recovered a complex of upward of 20
species pre\iolisl\ unrecognized m nillscllin colic.
tioiis and cataloged simplv under llie name \l. ,-lrr
trims. Interestingly, the diversity of electric ealfi-di
specie's matches that of other groups conforming to
the hasie division of iehthyofaunal province's of the
continent. 1 > \on. 1 laxononm diversity. Morris has
uncovered a large amount of ecological and ana
tomical variety. For example, some taxa are highly
depressed bottom-dwellers, others are firsilorm and
presumably active swimmer's. |>\ far the most astonishing discovery in this family is a clade of
dwarf forms in which females can he gravid at sizes
as small as <> cm, a size range in which specimens
of othei" species show lilll g, , . .! ,| ,| i:. ,, <i|iali< i
Most of the dwarf catfishes have reduced cephalic
and lateral line systems, elongate adipose fins, arrd

a highly iiiuisiial three ohamh. red -w in Ma; d< i
The liuiction of the three chambered bladder is as
yet unclear, but Mori is h,s suggested thai it may
play a role in the acoustic biology ol these lishes.
either in sound reception or production, or both.
There is little doubt that a similar taxonomic
complexity will he lev.-aled whet, othei supposedly
widespread "species." such as the enigmatic char
acoid Hepsetus odor, are subject to the same sort of
critical review. Mew species, and even whole new
and documentation will continue to require effort
and render important results. |',,,l without doubt the
greater scientific challenge will be the unraveling
ol the phvlogenelic relationships ,,l the African ichihvolaima. Such information is critical to our understanding of tin evolutionary history ol the fauna.
the geologic history and relationships of the continent, and increasingly, as an aid in informing conservation work. In all these aspects, this is a lask
that has hardly begun.
The Malagas) region has lori lx.ni...

as a biotie entity distinct from that of mainland
Africa. The region includes the Grande He of Madagascar and its offshore islands, the volcanic Mascarenes and Comores, and the granitic Seychelles.
As noted by Roberts (1975) the region, which is
something of an enigma to biogeographers, harbors
a highly endemic ichthyofaima. More recently
Stiassny and Raminosoa (1994) provided a review
of the fauna and, in addition to recognizing mam
<>! die Malagasy endemics as occupying phylogenetic ally basal positions in their respectiv<' chides.
ral
niilics in \sian freshwater is explained by
the existence in adjacent seas of the highest fish
family diversity in the world. The northern tropical
Asian iehlhynfauria lias some affinities with that of
northern temperate Asia, with which it shares some
cyprinid and cobitoid lineages, but on the whole,
tropical Asia shares several lineages with Africa
(e.g.. Notopteridae, several cyprinid lineages. Bagridae, Schilbeidae, Aplocheilidae, Nandidae, Anahaiilnlac (.hanindae. Ma-la< embelidae).
An estimated tola maul> n ; species for tropical
Asian freshwater fishes is 3000. More precise fig-
of the families currently represented in \lnea and

India. Because ol i
n
. the Malagasy
ichthvolanna is not treated in detail in this essay.
For more information on the Malagasy ichthyofaima
see Teugels et al. (1985). Stiassnv and Raminosoa
(1994), and Benstead et al. (2000).
v
east \siailna i
i Mekong. Bed River
basins and intermediate areas, Hainan. Mala\ Ten
insula, the Philippines and Indonesia eastward to
the Moluccas), where 2100 valid species are presently known (Kottelat, in prep.). However, considerable differences exist in our iohthyologieal knowledge among regions and coimtries because of
l'l{()l>K;\l \s| \
incomplete surveying and variable ichlhvological

practices among countries.
The Indian ichthyofaima remains in need of indepth systematic s|M,|\. K<-< <-til work on Sri Lankan
and southern Indian fishes indicates that many speci.-s thonghl to lie widely distributed and oonspeeilic with s|>eeies originally described from northeastern India aie in fact assemblages of allopatric
species (I'ethiyagoda, 1991; Pethiyagoda, pers.
com..,.: MK. pers. obs.). In Kerala (South India)
10 :'()> ol the li.slu s in am basin of reasonable
size are likely to be undeseribed (Pethiyagoda i\
kottelat, 1994). Habitat deterioration in this region
poses a sen,MI- threat to most species, including
those that are poorly known or unknown,
The development of ichthyology in China has
been largely independent ol that in the rest of Asia,
but many scientific names applied to China's freshwalei lishes are taken from adjacent faunas without
adequate comparison. Survey work is very incompi. le. .specially m tb< hillv in i- n, ih. s.,nlh.
Species diversity is uiidereslinialed especially for
small NIZCI
nnpl
hi loach identified
n >
i I i I
I
in issemblage
of at I
lall a dozen spe.K
I iifoihuialoly. ceo
nomic changes irr recent years have made illegal
ic lislinii.' widely a\ ailable everywhere. This
poses a serious threat to the survival of most enderrric hill stream fish communities. In 1996 one of
us (MK) observed in western Sichuan that most
smal streams surv ev e-1 wen ivilhoiil lish
Knowledge of the ichthyofaima of tropical Asia
is still in an exploration arrd discovery phase. The
As treated here Tropical Asia approximately

eqrrals the Oriental Realm, extending from the Indus basin eastward to South China and to the Moluccas (ca. "Wallace's Line"') m Indonesia \Vi. 21.
II.. dominant u'ou
na
nd secondary
freshwater families are Cyprinidae (about 1000
species), Balitoridae (about 300), Cobilidae (about
100), Bagridae (about 100), Osphronemidae (85);
and among periph.
hi la. (al I
300). This pattern applies principally to the mainland areas and in the insular parts to the major
river basins draining onto the continental shelf. On
oceanic islands and on the mainland in streams not
draining to the continental shell, the proportion of
primary freshwatei fishes is lower, and there is an
increase irr representation of peripheral families. In
the Moluccas, Sulawesi, and most Philippine islands, there are no primary freshwater fishes, and
gobies constitute al I hall ol In. ml in,I ti-li laun i
While recognizing an element of arbitrary taxo, fish families an ofugh siiiidt to higher-leyel laxonomu
las \ distinguishing featun of the
inland fish fauna is its high number
been recorded from inland waters, either as permanent, temporary, or occasional residents (ci\ 4550 in Africa and about 55 in South America). Thirly-lour of these families are primary oi secondary
division freshwater fishes, and 18 are endemic to
Southeast or tropical Asia. The remaining 87 f;mi-
to sonu- 370 known by mid-l9>7 (kottelal. I 9981

This represents an increase of about 80% in about
11 weeks of fieldwork. Some 85 of these species
were unnamed, though many were known at the
time of the fie Id w
I
tin m ire loa< lies
cl 'I e taiuilv balitondai [ha! mfalm lull slnaii s
and have a relatively HI a I dish . hulion area, often
restricted to part of a single river basin. Similar
figures can be recorded for inos! \siai countries
(Kottelat & Whitten, 1996b). The situation is likely
similar (but much more acute) in Vietnam, where,
as in China, i< litl
Survey efforts in little-known areas and poorly
sampled 1 amlat- continue to \ield new discoveries.
Kottelat et al. (1993) listed 964 species known in
1"'(,J
oin w< ten Ind i. -MI inland waters. An
addendum published in 1996 added 79 species described in the interval, and others have been discovered but not yet reported. Changes in systematic
or nomenelatural status affected 56 other species
(Kottelat & Whitten, 1996a). Fieldwork in reason1 or 2 new species per i
al day of fieldwork, but
also in the discovery of an almost equal mimbei ol
lion problems involving earlier known
liunirlithys
from these habitats.
Most are HI.all fishes: lighting
!,!
.,,,..,
'
in tin
(, s
peal
i I
\ par'
dailv
swamp is ll.hiif,
J_i
|.|
in, ||| | h|
earthworm eel (Kottelat & Lim, 1994). This family

was considered eudeiii c to bile I .ak<- in Myaimiai,
but it is now known from about a dozen species
with an overall wide range in Asia. liili
//,,'">.i,i, .,,i,;,
,s
|h.
stu illt s|
h ,i
Imi'lld
,>'l
action or loss of scales, lateral line, fins, ar

limber of cranial bones. It has fossorial habit
)ils around the swamps.
an
V-ian
lUkv, i..
MI
II.
/////,
lie lip.
al
species is an undescribed goby, Gt>bu>i>W;'.-. :i.i i

Singapore, that reaches about 10 mm SL. Miniatures provide one of the most striking examples of
discovery of a new fish clade, die family Sundasala
I i.
2 ''
i b< il basci
on two species
in 1981 by Roberts. These are tiny (25 mm SL) and

transparent
fishes
with
many
reduced
structures,
and, in places, they are extremely abundant. Four

I in
their
sp< , ics hav<
first
discovery,
been found on born, o si
and
Sieherl
(1997)
provided
evidence that the group is related to hern n- ;'
lu
peidae).
At the other end of the size scale, occasional

large-sized species are still being described. Some
of
were reported by
only
aid mum ions diminutive e\ prin .Is
interesting discovery
from
In tropical Asia, asm Africa and Soul h \i erica,

discovery ol miniature species is fairl) common.
yprinids (Fig. 23b). Ihinionclhi />rllu,iMany
i.l,t lion Mvatmia: am: lim,n,is tiucm.s Mom north
east Thailand are adult at about 12 mm SL, and
i
"Sundalaiid"" (Java. Hornet.. Sumatra. Malav Pea

insula) has a rich fauna (total ca. 1200 species).
This is due to its historical fragmentation into
smaller solaled basins and very d verso habitats
i.in,-,in-, from coastal mangroves to high .;lhi .! One unusual habitat type has been discovered to
harbor a very specialized and diverse fauna. This
is the p> at sw
i
. ii/ed by a peatlike -oil (not ma.f ot -pl| ,.. mini, but <
with a morphology !
peat bogs, (
tral "lake." The black i
lakes is darkly tinted by tannin and has a ven
pH (3 to 5). Once thought to be depauperate. I
are now more than 100 species known exclus
monoplcroidcs.
swamp (photo by Peter K. L Ng; drawing In Kelvin Urn).
in recent years that

i
nd described
early
they
In
explorers, but
it is
have been carefully
\sia an impressive e\-
.) I
i
lli- 23 \i. the
Mekong sting ray known to science since 1880 but
just named in L990 I[Monkolp] asit & Roberts,
1990). This immense I,s|, ,., attain a disc width
weight ol <>()() kg.
Probably Southeast Asian fishe
are the species flocks
antral Sula lakes (Mab
enigmatic iK.udlrlish.'-. Siui<!asal<in\ plat],

:\:A mm I.n-. (C.ipv rights Maurice Koltrl.it.I
consisting ol 2(> known native species, all hut 4

endemic to this system. Within this lake system.
two units can h< .'I ti v in I il I il
I
(>
ntoa: onh 2 <MIThe lisli spi-cH-s include '*> endemic Hemiramphidae (halfbeaks), 6 endeinii- Gnbiidae (gobies). 3 endemic Ory/iidae (t iec(ishes). I 1 endemic Tehnathnon-endemie species (one
each in the families Tclmatherinidae. Gobiidae.
>\ il.i n .nl i,
\n i it i I i< I II'
ik. - also con
ili it ids
MM i"
lad
ii
r< I.rules, and (mic-
rophytes (Kottelat, 1990b, c, 1991; Larson & Kottelat, 1992; Bouchet, 1995).
The I'amiK Tebuathi i iiii<I;u i< hides live genera,
two endemic to the lakes, one with eight species
endeiiiie In the lakes plus one riverine species occurring also in an adjacent basin,
olhci monotvpic genus from Misool, an island off

Irian Java (the Indonesian part of New (anneal
(Aarn et al., 1998). While the larvae of all telmalhermids are "pelagic." the adults live close to
the bottom and II. Militate spawners. They are
strongly sexually dimorphic (big. 21 \). and males
of several species exhibit color polymorphism. One
species iTrlmatlirima /irognatha, big. 2 Mil apparently feeds ,,n (m-ravs and scales ,>| other species.
) preys on eggs 0f othei
The other lakes of central Sulawesi, lakes Poso
and bindii. have l<-- dn.a-e hdi faunas. Lake hindu apparenlU hosts a single native species. Xrnopoecilus sarusinorum (Adrianichthvidac). while
Lake Poso is inhabited by two endemic Gobiidae.
three endemic \dt iani< hlhv idac. and Iwo endemic
Orv/iidae (Kottelat. 1090a). The Adnanichthvidae
are noteworthy for their breeding behavior. Although originally recorded as live-bearers, it now
appears (Fig. 25A) that the female carries a clutch
ol eggs with hei pelvic lins. in a ventral depression
of the belly, for about 10 days until they hatch.
Adrianiclithyidae are closely related to Oryziidae. which are known from India to Japan and Ti-
dae (13 species, e.g.. Fig. 251?). ( A pi mid;

e.g., Fig. 25C), Cobitidae (2), Synbranehid
Gohiida.-lll. an.l < lariidae(l).
perhaps better
Australia and New Gu
l faunas than for
heir freshwater ones. Neverthele . freshwater fishs of Australia and Vw (-iiin.-.i arc di-linctiv c. ineresting, and have been the subject of significant
i!i
.
I di-t o\ci\ c\ei die past 20 or so
of oddly specialized
1
f-'-lili/l.'d. chiuW eggs. H
mor, in fresh ami brackish

\dnaiiichthyidae are known on Sulawe I if-t
pail of the island ilia uolen h.dii l!i,
Ionics suggest was earlier
er hand, the distiih i
hat
I In I < rinid spec ics

i half of Sula
>cted i
I))| |.
OB oi I
I sill pi - 111"
dial at leas! '*> I species (son,.- andcsci ibed) o( cave
fishes are known from this region and many more
should be expected. Some of the largest kaisls
if i - V
I I
ue|\ been explored speleologii-alK Si\tceii spe. ics oi eavi ashes are known
from China, seven from Thailand, four from India
(three actually from wells), two from Indonesia, and
one each tioin Malaysia and Laos. Most ol these
b<
\
l ii i waters, but
five cannot be Ii k-i| wiih
-iiil.ur species
and are treated as distinct genera. Noteworthy is
the cyprinid genus Sinocyrlochcilus, which has
evolved independently at least seven hypogean species in China (Guizhou, Yunnan, and Guangxi provinces). The epig
usually lound asMi. ialed with -:>i H^ ot in streams
under overhanging ioek\ sii ir-. *v(neh make I hem
I i i
>ted" to colonize cave habitats. The known
ea\( lisht s in \sia Ii long to 'tie I mi IK - K.il I. i i
fl th
,.ghl>
continental I'.S \.. \us|,al,a (Fig. 2) is generally
characterized by lower lo|)ographical relief, lower
rainfall, and a much less extensive system of rivetdrainages. However, largely as a consequence of
the latitudinal spread ol the country (from about
1040'S to about 4340'S), and of the influence of
Australia possesses a wide variety of freshwater
habitats. These include artesian spiings and
ephemeral de9erl lake- and streams (Great Australian Bight, Lake I'Aie. an.I other internal drainages); tropical streams that undergo extensive flooding
during summer monsoonal rains (northwestern \ustralia and Gulf of Carpentaria drainages); rainforest
streams (northeast coast); , oaslal streams arid sanddune lakes (east coast); and alpine lakes (Tasmania). The Murray Dailiug Mivei System is bv far the
largest in \uslraha. extending soiilhwestward about
1900 km from the interior of southern Queensland
to the Southern Ocean.
Stretching around 1600 km, New Guinea is the
world's socorid-largest island (Fig. 2). fbogi
i ipli
ically and geologically. New (dum-a is divided into
inore-or-less northern and southern provinces, separated by an extensive mountain chain along the
long axi- ol the island. This mountainous topography, in combination with high rainfall, results in
numerous drainage s\steins, and a large array of
II Iplain lak.large highland r

Australia and New Guinea are much more than
just adjacent land masses, as they have been connected throughout most of their history. The Salmi
Shelf, beneath the shallow A.afura Sea and Torres
Strait dial now sepaiale the two areas, was emergent until as recently as about <>(>(>() years ago during the latest glacial lowering of sea level, and
southern New Ciimom streams were confluent with
those of the adjacent I
Volume 87, Number 1
Australian freshwater fishes were reviewed by

species: sul)si (]u< M 'i l> i H I.-
ml iv-
i I!
freshwater ta\a in tin- eountrj are the g

d fam
tin - Kleolndidae and Gobiidae (ahout 50 species),
the superfamilv Galaxioidea. an austral group of
salninriifnrni lishes related lo the northern smelts
(26 species), Tera])ontidae, an Indo-We- Pacific
gt'Olip ol pi ll
ft >
II- II - l__ -|
I'
i.
ith
dae. a farniK ol
ill
i
n I I n m
niacin
South \IIII in ,11
HI \[
ii h
2II
i II--), V]
II
n \ii-lulun New (hiinean endemic family (hut, see l>< low
I ilaci
!
I
(16 species and -ah-poi .-->. I'lolosidae. an hido
West Pacific catfish famib (about 1 5 speeiesl. and
\lheritiidac. a wmliiwide a:tiennoinorpn l.iiniK I I >
species and -u!.-.
i<--; Olln d:-l ineti\ e component- include tin- (Queensland lungfish. \accratn
dm forsteri (Neoceratodontidae), and the bonytongue (osti-oglossidi species, Scleropage.s jardinii
and S. leichardti.
Freshwater fishes of New Guinea were reviewed
by Allen (1991), who listed 520 species, including
sonic esluarine forms; subsequent cnllecliu;
ml
i L5s
(53 s
tc-l. \riidae. a em unitropu al catfish family (21
spi . ies), I'erapo d II Id sp ii -). ( .halidlda. I
Vail., idae). an Indo-West Pacific familv of -mall,
pen Ii like fishes (15 species). Pseudomugilidae, a
familv of alhermomorph fishes endemic to Australia
and New Guinea (13 species), and Plotosidae
species). Most of these taxa arc also spo
eies-rieh in northern Australia, emphasizing the
historical link between the areas; indeed, about 50
northern
Th.
\uslralia. and mam of these are restricted
II
in '
I.
.1
a< ti\ il\
in
Australia and New Guinea can be gauged censer

. aim l\ Iron il., 'II,III:KT <>i i . . -tit K described spe
eies and subspecies. Since 1970 about 70 Australian (33% of the total) and about 125 New Guinean
(36% of the total) freshwater fish species and subspecies were described or are awaiting description.
Increased md. - n I i, r i Ii -I watei fish s\lemalies and distributions in the region has largely
i
ami
i
-Wemal
| I
|, < i mcpii -
input from ait

uaihciilar. dm mg lh<
hd
b\
i < III ( oil, , tin;;
pmle-.Mon.nl
i- -
ahd ,
a d uquuii-l-. In
,;-,: Imee <u eaC.es a ;.io:nim I
increase in interest m keepingfreshwater fishes has
eties (e.g., Australia New Guinea Fish Association.

peditions. Aquarist interest has particularly concentrated on the endemic rainbow fishes (Melano
tacniidac. fig. 261. and this, in combination with
taxonnmic and field studies by G. R. Allen, has
species recognized in this family: of the 67 species
and subspecies oiiii.iitly recognized, 38 (57%) are
either undescribed or wen- described since 1970.
Other significant new discoveries in recent years
have included: Oxvclcotris caeca (Fig. 27A), a blind
I.nil.lid gobioid from sink holes and caves in the
Upper Kikori River. Papua New Guinea (Allen.
199(>); two new giant petviehths id- of the genus
Waccullochella from coastal drainages of southern
Oueenslaiid and noilhern New South Wale- (Mow
land. I'><):*): Scaturiginichthys rermcili/>irim.\. a new
genus and species of pseud, nuiigi lid from an artesian spring in central western Oneen-lutid (Imanl
soil' et al.. 1991): four new gobiids of the genus
..cms (fit:. 27Pi lioin aile-ian -pmig
systems in central Australia (Larson. 1995); and
numerous lacustrine atherinid, eleotridid. and trnlatotaeniid species endemic to \arioii- lake -\-tcmin New Guinea (e.g.. Allen & Hoese. 1986: Crowlev
et al., 1995; Allen, 1995, 1998; Allen & Renyaan,
1996).
There also have been significant advances in our
understanding of the phylogenetie relationships ol
Australian and New Guinean freshwater li-ln -. fm
example. Johnson (1984) diagnosed a monophyletie. freshwater Pcieichthvidae that included the
southern South American genera I'cnichtlns and
caw duelling "ohioid. ().\ \rli;>lns (ami. 10, mm lung.

In.ni I'.ipn.i N.-vv < a.incn ihascd on Mien. 1000).
II. One
of ill. ailr-ian -.pring-dw. llin
I i
/W<Airt/*>rilbisMloii VI. in. k ^ Nhmili l' |i
I). Cudopsis miirmoniliis (based on \1-tr uk iK Sclimida,
10551). K. Tlir humming sala.nanderf.sli. h-pido^daxias salamandriHiles. I i Wr-i.-m \u-n.ilia i < . >| .\ 11 -111 bv
/<>./,/ |hg- 27C). 6W,y>.s/.y (Kig. -'VIH. AVW/.l. Sannopcnn \dni.n

I"
i', '
ill
'
in i I ill. i (luce combined into a probably paraphyletic Macquaria by
MacDonald (1978) and most recent authors). Previously (e.g., Gosline, 1966). the Perci.hthv idae
had been a catchall for basal pcrciform taxa that
IIKhided, among others, marine genera now assigned to the \ci-oponiatidae, Serranidai Moi m
dae. and l'nl\] i
.
I i
Ii
I
i
sized that the southeastern Australian (..,-'
sister to the southwestern Australian Bostockia, and
that these genera form a (lade with the dii
Kdcliu. .\iiiinnlhrrimi, and \ounopciro (pi
in the Kuhliida.
of Cudopsis wei
Hi.-, ml .
been variously placed in its own order (S<
1962), allied to ophidioids (Gosline, 1968), a
cated to a monotypie percoid superfamilv (Nel:
1976), or suggested as a possible relative of
perciform suborders Trachinoidei or Blennio
(Rosen & Patterson, 1969).
No Australian freshwater fish has altrader
much attention from systematise as the southw
ern Australian salaniandei hsh. Irpidt>i><ilii\i<is
(imanilroidcs (fig. 27k). Originally described <
galaxiid (Mees, 1961), subsequent authors hav<
ther retained it wilhiii the (,ala\ndae |oi al |.
I!, I Ih,
do), ,
G i
id
I
I
i i |
ill..us lot lh< l,i\on. SIH Ii as
the sis|,-|- ul a elade consisting of the Northern
families Esocidae and Urnbridae"(Rosen, 1974), or in an unresolved trichotomy with the Salmonidac and Neoteleostei (Kink,
1984). However, recent studies have nested the genus v\ i 1111 II the gala\ioids. Johnson and Patterson
(1996) concluded that Lepidogalaxias is the sister
of the Tasmania!! genus Lornim, these together
forming the sister nl a elade consisting of the typical Galaxiidae plus the southern South \meriean
genus Aplochiton. Williams (1997) concluded that
'./. i- llh -i~l.-i of a elade consisting of
ih. typical (ialaxiidae and the Aplochitonid.i. (Hie
latter including Aplochiton + Lovettia).
No less controversial in recent years has been
tlit I'"sili.in and composition ul the family Melauolaeniidae. This has particularly centered around
the \usiiahan New (uiin.-an lamilv Pseud..mugil
idae, the western Indonesian and New (-inn.an
family Telmatherinidae, the Madagascan family Bedotiidae, the southeast \sian Phallostclhidac and
the West Pacific Dentatherinidae (e.g., Allen, 1980;
Parenti, 1984b; St.assnv, 1990; Saeed et al., 1994;
Dyer & Chernoff, 1996; Aarn & Ivantsoff, 1997).
fhere has been a substantial increase in our understanding of the biology of \uslralian and New
thiiuean lieshvvalei lislies in i.cenl veais Particularly not.-worthy have been several studies on the
h.olog.v ..- ih. , -' i- ni. _ ,| , i, ,.| /,, ,,/.,-,//,n,./
solum,uuiroidcs (re\icwed by Berra & Pusey, 1997).
Unfortunately, two unwarranted assumptions
about the nature of Xustralian New (hhnean freshwaler fishes prevail in recent literature (e.g.. Allen.
1989; Pollard et al., 1990; Berra, 1998): (.) the fauna is luglilv n
i i I
i I i I i- .11 i
I
by spcci.s that have recently evolved from marine
devalue the significance of
uii<|u<stinnablv premature.
For example, Allen (1989: 8) noted that Australia

li;i- remarkably :
.
i
the continental U.S.A. However, no less remarkable
is the difference in effort devoted lo the taxonomy
of the two faunas.
Clearly, there is need for much more survey work
to be done in Australia and New Guinea, as some
areas remain pool I' i.-dlp
i idaib in Irian
Jaya). However, perl i
n i
n
il i
I
i i
e careful study of the n
species, as it is highly Ink. !\ thai n < Ii -lud\ will
lead to a significant increase in the number of recognized species. For example, geographic variation
has been reported in various \ustialian freshwatei
fisbes, including representatives of the Atherinidae,
Fleotrididae, Oalaxm i
' ilosidae. Me
lanotaeiiidae. Tci.ip- in i
l'.-i i< hl:i\ nlae. Metropinnidae, and Pseudomugilidae. Indeed, one melanotaeniid species. I
<i^>,ihi li.ibeen divided into as many as .'{."> geographii lomis.
each with highly restricted, allopatric distribution.(Hieronimus, 1998).
While it is clear that the taxonomic revaluation
of widespread species will benefit from recently developed molecular techniques (e.g., Rowland,
1993; Musyl & Keenan, 1996; Jerry & Woodland,
1997), it is likely tl
i caul advances
>\ i I
In
il
ii
gv. but
for example, Vari's (1978: fig. 9) phylogeny of the

, ili< i< M< -i ol ll
la are exclusively
freshwater an*I restricted In \ustralia. New Guinea,
and several other Condwanaland fragments in the
hido-Australian area. Three of the four genera with
marine species ( Mrsopristes, Terapon, and Pelates)
are relaliveK widely distiibuted in the Indo-Pacific,
but occupy relatively derived positions in the phyI < n ll | n
i
|. il ion of the fourth "macies, an \uslrnlian freshwater species, and a
soutliern Mew Cumean and Australian euryhaline
speeies) is unresolved, but il could be near basal,
Iripnilirnipon, the basal-most genus in the phylogeny, is exclusively freshwater. Therefore, one interpretaliou o| available evidence, following a center
ol origin concept, suggests that terapontids are
freshwater fishes, with several relatively recently
e\ obe.I marine species.
\\ liereas nianv previous authors have acknowledged that a small component of the AustralianNew Guinean freshwater fish fauna probably has a
relationship with Gondwanaland (e.g.. galaxioids.
and the osteoglossid genus Scleropages). then is no
justification for n priori rejection of such a relationship for the other taxa. For example, although
lli< Vuslralian IWriehthv idae ;
ften cited as be-
ralhei
ing recently evolved marine invaders, this is largely
from a sounder philosophical view of species and

associated systematic method. Much could be
gained from carel Di ri
i M i n i | i-
>l
characters already at hand, such as coloration char
a consequence of the previously loose definition of

the family, and Johnson's (1984) cladistic definition
of the lamilv (sec above) suggests that percich111\ id-, loo. predate fragmentation of Gondwana-
eties." (Coloration characters, when not supported

by other characters, have generally been dismissed
hv 'id
ii- i r en " i ii
ti and IV u
Guinean freshwatei fishes, although such premature judgment is unjustified; a similar problem exists for Indo-Pacific shore fishes; see Cill. 19,)9.i
There is urgent need for such studies in order that
species be properly conserved and managed.
One could argue about the biogeographic relevance of whethei il In I
i fish
( '
and New Guinea are of marine aneotrv or not. ait is incorrect to equate a marine habit with mobility and a random biogeography. Indeed, there are
many endemic Australian marine lish taxa How
ever, even if marine ancestry was an issue, the as-
I nforlunatelv. pli\ logenetic information is lacknig for most \listiali.in and New Guinean freshwalei fish taxa. but the need for such studies is
obvious.
In summary, the past few decades have seen signilie.ml advances in our understanding of the systenuities, biology, and distribution of Australian and
New Guinean freshwater fishes. However, there is
need for continued work, particularly in the revaluation of purported widespread species and in
phv logenetic studies. There is every reason to prediet that such studies will lead to a significant increase in recognized diversity, and a conclusion
tli.it the ireshvvalei li.shes aic just as distinctive and
historicalb/biogeographieallv informative as mars of Australia
simply
not -i,|
. nl< d
il i> true thai m n

also
11
oi
bl
ie domii
. v idem e
>il
include marine species (e.g..
aponl idac. and < .<=.
W Inle
< I'lolosidae. Tei-
nin|. ii do.-s i oi au'i c al <; Ilk
habit is ancestral. Consider,
species are being found and described at rates as

high as any in the hi-loiv ..I iehlhvolomcal <-x|I<>
ration. Many rccetitK discovered fishes exhibit
highly unusual characteristics, and some represent
previously unknown lineages (described as new
genera and family-group taxa). New fish species are
still found occasionally in Europe and North America, where the ichthvulaiinas are .dreads well documented. Phylogenelie -Indie- ol hslies from all
over the world cominr.nlv reveal unsuspected higher-level evolutionary and bioge.igraphieal relationships. Investigations of even long-known fish sp(des continue to di-<m ei novel characteristics ami
strange life histories. In addition, a- the extent and
patterns of fish diversity and relationships arc more
thoroughly documented, we are licller able to detennine the correlates and causes of fish diversification in evolutionary time.
These are also limes ol serious concern for the
present and future health ol populations, species.
and communities of freshwater fishes and other
aquatic organisms (e.g.. Stiassny. 1999). \ recent
analysis of the North American situation by Ricciard. and Rasmussen (1999) estimates the extin
lion rale loi freshwater annual- at five tunes ll
terrestrial fauna and similar to that for tropical rai
loresl-. Man\ human activ itic- are increasingly (lis(M-\ll,sie, eial.. I'Kl.xMincklej & Deacon, L991
Warren & Burr, 1994; Harrison *\ Stiassny, 1999).
\\ heiever human population- an- large or expanding, so increase dam- ami impoundments, dredged
and straightened channels, erosional runoff and turbation. and the harmful waste products of mining,
industry, agriculture, and urban growth. These mi
pacts have unintended but negative and sometimes
devastating effects on aquatic habitats and life.
Consider the vast extent of interruption ol natural
river flows and fish movement, and allele :,<-i il i.
attended the prolileiatioii of dams, \ccording to the
World Commission on Dams (1998), in 1997 there
were an estimated 800,000 in the world, and "more
than 45,000 of these dams have been categorized
as large (dam height more than 15 meters above
the natural river bed)." Among other horrific aspects of an ecological catastrophe centered on
freshwater, witness, in the veais following diversion
of the Amu Darya and Syr Darya rivers, the total
collapse of the Aral Sea biota (including a fishery
dial once produced 15.000 metric Ions per annum).
Freshwater fishes are important and valued resources for food, spoil, ornament, and biological
control. Like -o mam other resources, pop i :: onarid some species of freshwater fishes are already
nverexploiled. Well documented cases of overfishmg include several species in the Laurcntian Croat
Lakes (S .Smith. I(><8> and the large pimelodid river catfishes of the Amazon (Barthem & Goulding,
1998). Freshwater fish communities and species
also have been placed in harm's way by introductiotis of non-native species. Here, too, the problem
is current and global in extent. Some of the best
known examples are the sea lamprey in the Laurenlian (deal Lakes. Mile perch in Lake Victoria,
\lrican tilapia eichlids and American largemouth
has- in main parts of the world, and trouts in Andean rivers, flic world's most s|)ectacular species
flock of cvprinid fi-he- in Lake Lanao in the Philippines went to extinction Inllowiug introduction of
several exotics. Lake Diandu in Viniiaii. China.
formerly held about 25 native species (12 endemic
in the lake). About 10 species live there now, but
most are introduced. All the lacustrine endemics
arc gone, in- '
\nii>
(lianchien.sis, which was described about 25 years
after the last living specimen was documented,
Human dependencies on and benefits from
aquatic specie- and the communities and biotas
lliev form arc mam. and some arc critical, including
and indicators of water quality. Daunting
and IIK leasing a- the threats arc to freshwater biotas around the world, efforts must be made to redue.- and miligat. Im r mp.i. I- bv ru >x.| -; v. an a. mate ai | thoi
OUgh !"! > ine knowledge of species-level diversity
is essential. Si,, h 1 . >w 1, !. . - al- * fund, menial
for research in systematies, ecology, and other sciences. The freshwater fish fauna- reviewed herein
exemplify how much we are still discovering iboiil
species ,[\H\ higher-level diversity, and sic, . it
much more remain- to be discovered. Fishes arc.
of course, among the better known components of
freshwater biota-. Lain so the pace ol habitat
change is so rapid thai il i- bk.-b that some, possibly many. In 1
1 i
i
before they are known to exist. What else will disappear along with those unknown casualties.'' How
much do we not yet know of the species of aquatic
invertebrates, green plants, fungi, protists, and pro
karyotes? We do not know, ami possibly will never
they play(ed) in their communities.
Fishes, because they are better known and relatively casv lo monitor, serve a- nidi, aim oii;au -it to monitor the health of aquatic ecosystems. But lo
achieve the needed baseline knowledge
i i
freshwater fish species will

[> '!.'.
tillThere are praiseworthy and
llial support I>i<.11. surveys arid discovery, e.g., the
IS NSF liiotic Sur\c\ and Inventories Program.
universities promote the enterprise, hut the task remaining will depend on lhi in L no II. li < ol harlh's 'iln.' hiola is an mi
mense and urgently needed joh, hut one that will
yield a uniquely wonderful result.
.1 risk \,uat. Sri. 38(12): 1539-1561.

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hnke. H. J. 1002. Native Trout of Western North '

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-& T. R. Haghn.d. 19 . Fine scale temporal v
>IM.I the Miocene stick
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cgcls. (.. (,. iK C. I). Mof)kins. 199B. Morphological ami

osleological evidence for the generic position of MorMormyridae). Copeia I99H: 199-201.
, J.-F. Guegan & J.-J. Alharet. 1001. |;,|.,,,,l
Shiozawa & R. P. Evans. In ,
lliston. Smithsonian Institution Press. Washington.

D.C.
Smith. S. II. 1008. Species succession and lisherv e\-
.< , (,<>:>,
Geographical overviews presented at the PABADI Svmposium, Senegal, 15-20 November, 1993. Ann. Sci.
ZooL \liisee l!.,\al d.- r\fri<|uc I entrale Teruiren.
Belgique, Vol. 275.
, (;. McC. Beid & B. P. King. 1992. Fishes of the
Stearic). K. F. & (,. B. Smith. 1003. Ph\logen\ of the

Pa< ill. i. uls ml - ilmoiis \()nii>tl,\h, < us) mil u. in I.I
of the t.uniK Sail, ML,.-. Trans. \me,. I ,sh. Soc. 122:
I 33.
I'Oi. \ new (limclodid catfish from the
of the Klo \a|)o. eastern Kella.lo, (Pisces;
. Proc. Aca<l. Nat. Sci. Philadelphia 138:
s Hhrorles (Atherinomor
Novit. 2993: 1-14.
arelationships of the f'am
:lae: An overview. Pp.
ditor), Cichlid Fishes: B
. Chapman Hall. Londoi
s21:7P>90. The medium is the message: f'reshuater
ersily in peril. Pp. 53-71 in J. Craeraft & V. Griflilors). The Living Plane! in Crisis: Biodivorsily
& A. Mever. I'W. Cichlids of the east African
Sci. Amer.. February 1999: 04-69.
& M. C. C. de Pinna. 1994. Basal taxa and the
f cladistie patterns in the evaluation of eonservariorities: A view from freshwater. Pp. 235-249 in
.......a \lll(3/1): 293-304.

za, M. 1997. Systematic Bevision
ic (Teleostei:
alio.,. The (.
Menezes & C. Mendes dos Santos. In
HI ol die ueolropieal lisli genus Hydrolycus
Characilorm.-s: ( \ nodoiilinae) with the
I Ivvo new species. lelhvnlogical Fxplor.
Fresh wat
J. Corbet. 1072. Icological
Trewavas. K.. J. Green &
studies on crater lakes in west Cameroon. Fishes of Barombi Mho. Zool. J. Linn. Soc., London, 167: 41-95.
Turner. G. F. T. 1007. Small Irv go big tune. New Sci.
2093: 36-40.
Uyeno. T. & C. B. Smith. 1072. Telmploid origin ..( the
\ in I,' P l'7::
III. I< i ipoti p.nh.s
IP,OHIM
bra
Bull. Amer. Mus. Nat. Hist. 159(5): 175-340.

. 1995. The neotropical fish family Clenoluciidae
. 50: 235-2 19. Clarendon Press

)soa. 1994. The fishes of the i.
133-149 in G. C. Tei
. F. Guegan & J. J. Mbaret (editors). Biological I
ity of African Fresh- and Brackish Water Fishes.
e Boval dc l,'Afri(|ue Centrale Terv
. 275.
studs. Sinilhsonian Cor.lr. Zool. 504: 1-97.

. 1998. Higher level phvlogenetic concepts within
1 II 122 in L. B. Malabarba, B. K. Beis. B. I' \,,,. C
A. S. I.uccna & Z. M. S. Lueeiia (cdiloisi. Plulogeny
and I Tis,plication of Neotropical Fishes. Mus. Ci. Tecnol. PUCKS. Porto Alegre.
& A. S. Harold. 100;;. The genus Cn-u^rulus (Teleostei: Chaiacilor s: Ch.iracidael: Monopoly, re I a
tionships, ami undetected diversity. Pp. 245-260/// L.
I! Mal-=b:.rb.-,. I!. F. Beis. B. P. Van. C. A. S. Lucena
& Z. M. S. Lucena (editoisl. Pin logem and Classification of Neotropical Fishes. Mus. Ci. Tecnol. PI CBS.
Porto Alegre.
& L. B. Malabarba. 1998. Neotropical ichlhsoln
i;.> (.,, i.
Alison & F. Mago

F. \A Marea (edide Venezuela. Ser.
i. Tecnol.. Merida.
Beis. I!. P. \ari. C. \ S. I ,,,, ,\ / \1. S luce,,.,

(.<-. Plnlogem and Classification of Neotropical
fishes. Mus. Ci. Tecnol. PICKS. Porto Alegre.
Verheyen. F... L. Biibcr. J. Snocks & \. Meyer. 1000. Mitochondrial phylogeography of rock dwelling cichlid
L & B. M. Burr. 1994. Status of freshwater
& H. I'. Vari. 1488. Miniaturization in South
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. 1998. Phvlogenclic Studies of the Kan.il>
(Teleoslei, Cypr modoi.hlo, m,s|. I mwwn
in .U im,I dissertation, Ann Arbor.
. * S. V. fink. 1985. Xenurohryeon.n phy1
i:'";"m I'1" '"'
'"
s Heh-oste, Characidae). Snu.hsoiuan Con.r.
Uiol. So.'. Wash.'101: 444-W>5.

V\ ilcy. K. (). I<>;;|, Pl.yloenHi, .; The Theory and Prac,,. | \>\n |;,(.,.| . Systematica. Wiley, New York.
Wi|s()|1. M V. H. & R. R. C. Williams. 1992. Phylogenet ic, hiogeographic ami ecological sigmficance of early
fossil records of North A,,,,-,,.,,,, Iiv.lm.ilci fishes. Pp.
,,^, ,, m |{ , ^^ (t.(ilt,,rK Sys.ema.ics, llis.or-
l ?"?<**: '""* NoJh American Kreshwater Kishes.

Stanford Univ. Press, Stanford. Cahlnniia.
, R. R. (i. 1997. Bones ami muscles of the susi the galaxioids bepidogalaxuis siil,un,in
droides (Teleoslei: Osmeriformes) and their phvlogenetic
significance. Re. Austral. Mus. 49(2): 139-166.
World Commission on Dam.. I'>'>8. Inlemet site address:
http://www.dams.org/
"A
M..~M
1998. Relationships of the
Tecnol. PUCKS, Porto
NEW MAMMALS IN THE 21st

CENTURY?
Out of the several million species of animals

nown to inhabit this planet, only a small number
re mammals (just over 4600) and birds (11,000);
et these are the creatures the general public best
now, like, and show most concern for. That there
emain over 10 .n.ll.o
see
nsee.s to d,sover and name ma, I.e. n,a ,,..1,.,. th.s
oes not mak< th,
I
lists sir the |o|> ..I de-cnl
\u
Mil
John MacKinn
extant (Wetzel et al
^ ^
IP
'K
.i-
\ .
,
as a ]ob neaiK
|'pI
r
In
,'[.
'II
,'.,
'U'l;l
;>ll
r
-
l<
^^
,
I I
I-
Disc,,verit.B
m
(<
-I'Srri
i
IM V,
(J<
mugeum and cata,oged

of
ill.'
II
III
>:
-. l !-.'.
'I
>
'i
Iiew
birds
have
been
equally
( rf ^ ^ p^^
^ ^ ^^ ^ ^ ^ Qn
_.
I - ,1!
, . ,
!il!>N
,
li.lH
,
U-i'l
,
...
il<-s<-nl)i il
sl,1(e
.:
' )2,
,
F loied
6
wltM
ilxr
c
ol
,.
< 11 i
rl
,h, s,
'
._
'
lK in
ln
the
nrkr.,,
leSS
,.
"
I \\ - I i r l'>'' I I Vim
. \ .
.'
'
i finds Jay tor years i
ogni/.
...
recognize. I as IHH
K;illl
Sulawesi macaques. Some
Z()ologists believe(1 the large mammals were, by and
lonns
J
...
. ,.
,
en creatures still to be found.
Ever since Linn.en
. i ! -cribing and
-.1 which
i i Man
M
i
*u
counting .L
the species with
l'
"
1975) A few new species wen-
a(]de(] by taxonomists splitting known forms: Mri_

f;an colobine monkeys,
pink
riiinpec
mselineli. C.nrjio-
,s
groups, the species discovery

, but for the
,-blooded vertebrates, espoc.ally the large
mammals, the curve is leveling off (Medellfn &
Soberon, 1999), and we can hazard some guesses
as to how many more species there are still to find.
dacus eos, Vaurii

I
I Sillem's mountain fi
mL
The
bein
ha<1
1>een
rmlgus centralas-
Collected 62
?ears before
as new in the Museum
g
f Am"
(Roselaar, 1994).
' a completely new, large mammal was
reco nized
sterdam
In
last
1992
Medellfn and Soberon (1998) estimated another

247 mammals, mostly small, will be discovered betvveeii l(>*>2 and 2032
found
in the North Annam

mountains in the Vu
Quang Nature Reserve of Vietnam: the Saola or Vu
Quang ox. Assigned to its own genus. I'scmltirxw
During the first three decades of this century,

only a handful of new large mammals were discovered. The finding .,! ..k..pi. (>/,,.,<, johnsloni, in
1901 in the forests of Cong,, created enormous popular interest and speculation that this was the last
great new mammal. But other new African finds
were quickly made: giant forest hog. llvlochoerm
meinertzhageni, in 1904, and Mountain Nyala, Tragelaphus Imxtonl in 1910, before the African vein
started to dry up. In 1937, Urbain described the
Kouprey, Noribos Miiurli. a large o\ ,,( Cambodia,
actually found in a zoo in Paris. During the next
DNA showed d
"' <>* was iJ primitive member of the
<'<>w and goat family Bovidae (Dung et al., 1993).
Two sets of the unique horns were initially found
hanging as a hunter's trophies in a Vietnamese vil'age. Subsequent morphological and genetic studies
Have shown the animal is so unlike anything else
that it should be regarded as a new subfamily. A
great amount of media interest was devoted to the
find, but it took two years before anyone actually
saw the animal alive, when two young animals were
caught by farmers and brought to Hanoi,
The find was exciting for several reasons. It
il\ limn!;u li helped highlighl tin

status of the negl. . If.] \nuai M umla i - I!. a
But most of all, it made people realize we really do
not know all our large mammals, and it is still worth
looking for more.
Subsequent surveys in Vu Quang turned up a
second new ungulate. I hi- gianl muni
1/
muntiaais nupmngeiusis (Tuoc et al., 1994). The
finds were made in the same ullage as was found
the t\pe speemieii nl' the Saola I'ln- 'annljae spc
it did not inateh ll
.1
Muntiacus (Groves & Grubb, 1990). Further DNA

studies have shown the new genus max I
i'i
al., 1998). There is some argument (Schaller &
Vrba, 1996; Groves & Dawson, in press) as to
wh.'thei Wimliitcus should !.. e.lel'mcd to accommodate the giant munljac This cervid mammal differs 11
the other seven known muntjacs by its
larger size, short pedicles, arid much larger, more
,/,.-, ,,!,,, ,;.;,'> rt.h de-. lib. d I'otll I ailibudia oil

the basis of several sets of unique -pn.i
(Peter & Feiler, 1994). But the failure of efforts to
find the animal alive suggest we ma\ be loo late |o
see or save this species. A new tree kangaroo (the
bondege/ou) was discovered in the Jayawijaya
Mountains of Indonesian Nev
N
lan
seven new marmosets (the latest being ' i,',";,
nutiiesi ,\iu\ (]. nigriceps) were added to ill- mammals lisl III llia/il I
I
b 1-1 I iln - '
/'
r
rondoensis and G. udzuntun
have been described from Tanzania. A new horse
was reported in the popular press from \ i ang.
Are we on a new wave of discover)? In fact, the
ills.-OV< IV <)! IK
I
III II
I I .111, [ I II >
i i i... ' 'H lli' cenliirv. More ihan a hundred new
mammals have been dcs.nl
ml
.
much public attention (Wilson & Reeder, 1994).
These have beet
huts, and insec-
Uolh Saola and giant muntjae v

lams i< vealing a i < |..\giu\ iiuiiil|ae. Mnn!-,u ,
ftisis (Giao et al., 1998). In Laos, the Roosevelt's tiiiinljai ! ; i. i.. is known from only one
specimen! was rediscovered together with a bearded pig, Sus bin
id\ known from
only one lost specimen in Shanghai Museum)
(Schaller & Vbra, 1996). A new striped rabbit was
also found in Lao- (foimerlv thought to be a Sufound in Vu Ou,
I'
icserves in Vietnam, and still awaits scientific description, \nothei
smail inuiH|ac has also been found in the central
\i i i Mountains of Vietnam, awaiting analysis
in
if lion Hi il
p< i- . otiiin !
Vu Quang, itself in a remote evergreen part of
the North \nnam Vloi mams ...a I ie ii<ud< belwi . i,
Vietnam and Laos, continues to reveal novelties.
Two new spe.aes of fish have nisi been described
there (WWF, 1996).
North Annam was already recognized as a small
pocket of local endemism with such local specialities as < >v\s!oii palm i>. i I ' '
, ;/;,,v, ,>,, ; ;<
';;i,r-i^s \ n luam.'se phe '- ml /.;.*,,, ,/ ,/','
wv an<l - iol\ 1' ibl.|< i. \',f, '/ ," u,-hi'tli. I he-e new
llll'L ol Ulnle-eliLi <:' Ml 11 III 11 lL idll s|jail!l< ill''', to
the biological and
These exciting new discoveries in Vietnam and
Laos seemed to stimulate a new wave of search and
disco\er\ aioimd the world. \ new anlcl,.;.. . /',,,
WIII
Li
I'IMIs |!|
I,. \n
mi- ol Vietnam and Laos do
seem to be a nth. and still not full) explored,
source of diversity. It is one of the world's overlooked "biodivcisilv hotspols." The spectacular
mammalian finds an largelv <\n<- lo a time warp in
an aiea where zoological exploration had !<- a i Id
ical trouble. But these finds do give us clues about
where to find yet more new species.
Despite being in one of the most populated regions of the earth mil a J i h<
il
l<
it< .1
bv bold ehemii i ' i . . I vsic .1 liomba:dme<il lining the Vietnam War, the North Annam M.iaii: inare nigged, difficult to access, uiiallraii i\ c loi ag
in iiltiit. . and ecologically isolated from much drier
surrounding lowland forests. Highland peaks are
small and separate, les.uibl
- i I i n lag
ol . veigr.eii uioiilau.' i- and-. Tin- region is part of
slabil
i I
climatic oscillatiot
I asands of years
Ig 11 linor vertical movement in the steep t

et al., 1998). These are conditions ide
cation of local endemic species as well
arvival of primitive and relict forms. Tl
is both a classic Pleistocene refuge ,
iu re e of new vertebrate radiation.
Th.f> following kev characters can be idenlif
Volume 87, Number
ators of the likelihood of a given geographic

still hiding undiscovered forms:
area of long geological stability:
jv:: ci iio;tn a :i< hnoss;
I region of long-term humid conditions
(Pleistocene refugia);
remote and poorly explored;
semi-isolated and archipelago-like habitat
(/nit- -n idn a-t (una muri! ui - i t n i i Mi

mountains, Mt. Kerinci (Sum
i
VI
k:i
(Borneo), Taiwan, Mt. Victoria (Burma), West Javan
tin i.iimi-. ûlaw. -i. 'be PI ll p-.M'M -. md Ihi \1 1
lneaii island- Contrast these with liie geneiali/.ed
Vsian large mamm :ll fauna ni ! plnmi il'.ir, -V ,
wi'/;;'/%). IIJI i [Bun'lfiu !i^:>\). a-opaid i/'-/"/'.i'',
purring, gain [Bos <iuiirus), wild hoar {Sns saoju).
sambar deer (Cervus unicolor), and red muntjae
[Miinliurns riinntiiih). whieli ... a. t broadb from
north i -i India to Borneo, and through a huge
i.in-,e I . i It 1' i A,\ .A IIMI I IIMI ,11 difteieiiees. These
latter large mam n.i
ihl .nstitute a fauna
that has followed Man south and east through \- a.
bencl:::i:g from h m an ..pel n g and ni.initif. of hie
forests and displacing the anginal, mole evergreei;
forest fauna. Glimpses of this richer fauna can be
seen in the fossil i.ioid of ill. Siuaak- r rorin
In Africa, one also finds that e ndemism ar id species richness are concentrated a round relic
green mountains and Pleistocene i refugia: w cs, Vfrican rainforest. Mt. Cameroon, e astern Rift forests,
and cast Tanzanian forests and naountains. In contrast, the huge forests of the Coiigo basin and the
huge savanna plains of east and southern U-i. a
The new mammals of the 21s-i rcn'i i :,vill he
found in the still unexplored regions thai in eel the
criteria mentioned above of isolaltion, tending to be
tropical and evergreen systems. and lying within
the regions of high species diversity or end< mism.
Such unexplored areas remain iin northeast India.
Burma, Laos, southeast Tibet, nlorthwest Yunnan,
south Philippines, New Guinea, peripheral inountains of the Amazon Basin, isol; lied ..,...>::ains of
Central America, as well as smaller neot topical
drainage systems.
- explored taxa and the less
spectacnlai
.1 in
n oic diliieull
small
mammals
cause they are mostly diurnal, can mostly he recognized in the wild at long range or by vocalization.
and because tin
rid is mans.
h
pi
;< -siona: aiiiaicui In dwaleliers. In contrast, most
\er\ difficult to identify. And However, the scientist now has several important
new lo,.|s to help predict ulnae species are likeb
in be an.I also to record. < ah h. am! disl ugiiisli s;ie
cies. Satellite imagery allows habitats to be more
easily recognized and mapped, which enables potential species distributions to be determined. Aulomalie cameras allow shy secretive animals to be
i
rd< d rape n
Icrs am - i ...
I - III
.
. ali/alions to be used for identification and to distinguish between forms. GI'S ig m pa
I
honing s\ stems) allow much greater accuracy in
liK-ahlv information, which enables a tighter definition of species habitat requirements. IT (information feclinologv \ alk.ws mm hi faslci cour.i.ai - >n
biologists access to areas previously only accessible by major expedition. DVV
analysis provides a whole new high-resolution technique loi disci m i ..i ng iclaiionships between popi
i
nd species.
For instance, the common (/rant's gazelle (Ga,!,"' "iiinti) ol Kasl \lricii resolves into at least
three different species on the basis of DNA differences (P. Vlctaildel. pels, ni
.|. The whole nill. i
i- i spi m.-i-t lis. d on. < igain some
species seem morphologically very distinct, but
IlN\ reveals lliey are not. (Mini species are inorologii
id to he \eiv difu I. nt . m in Ill
I forts to define objective morphological ciilena loi defining species start to
break down. Whether one adopts a biological spe. ies i oin epl M
. i ics i onc-ept, it
is expected that good species in nature maintain
discrete breeding. However, more and more evidence of cross-l r.
wild spei ic- is
discovered. Most organisms accept alternatives if
the perfect mate is not available, and breeding
among closely related species does result in hybridi/.alion. \ I! memb. -s n| | a. familv Ccrvidae can
be made to hybridize with all other members in
captivity (Arctander, pers. comra.). However, even
wide, stable hybrid zones can be accepted without
invalidating species status if hybrids remain at a
disadvantage II
V\ ith birds, for
instance, it can usually be demonstrated by playback
second species or a hybrid. As more of tin-si- >;><

cies come under DNA scrutiny we will be able to
move closer to a phylogenetic species concept, and
many forms mm placed
18 ttively within one
species will split.
The question of where species begin and end
heroines more rompl iraled when legal aspects 1..
. nine II \ol\rd I'.n | >r. ,[e<-| inn. mttrol of lr.nl. -. ;im!
ownership of |
least recognized unit i
Species evolve from i
gradually from one to two through isolation. There
is no objective cut-off point. We must accept that
(Mil rriti ri;i arc rathe] s ilijeetisi am! no! <-nt|s -I.->it
across it,,- l)n;inl. We niusl tv)."I'm- satislaolorv nm
* ) to label I
in ividual. The question of "How
old taxonomists' puzzle of "What is a species?"

The world loses species and genetic variety at
& P. Grubb. 1990. I

<;. A. Buberick & A. H. Buberick
itnrs|.
IVonghoni* and \iitleis. Sprinoer-Verlag. New N
1997. The Kingdon Fieldguide to ,
Mammals. Academic Press. New York.
Medellin, R. A. & J. N.brm... \'><><>. Predictions o
1 diversity on f.
Cons
fin Ticrkundc Dresden l'X.50): 2l7-2r>3.

ioselaar. C. S. 1994. Notes on Sillem's Mountain-finch, a
recently described species from western Tibet. Dutch
Birding 16: 20-26.
M-hallei. C. B. K K. S. \r|,a. P>"<>. Description ol the
our lists gnm lonon and longer and we should he

on guard lest a sense of loss is dulled by new dis-
skills are sorely needed. Monitoring biodiversity

as important as describing biodiversity
L. Martin & P. Myers,

in Paraguay.
Science 189: 379-381.
Wilson, I). E. & I). M. Beeder (editors), \<><>1. Mammal
of the World: A Taxonomic and < icugraphie
Beference.
ton, D.C.
. WWF News Release 27 Sep. 1996.
THE TROPICAL FLORA

REMAINS
Ghillean T. Prance,* Henk Beentje,* Jo

Dransfield,2 and Robert Johns2
UNDERCOLLECTED1
ABSTRACT
i I'I ' . I
lanii 1 ml* ns. km. in main parts of the tropics reveals the extent to w hieh they
Keren! I i
n Madagascar. Cameron n, Lao P.D.R., and Brunei
dereolleeled and poorly stl
1 85 new specie
1)
II
|
1
1
iny novelties, for e;cample, in Madaga
examples f
i
I
-Nldir-. o' Mrall
as the Ducke Forest Rese
itensive studies of restricted an a- ate i nade. The
,-,
M species that are being de scribed, an a
nd the rate of additions to
rently being underestim,ated and that th
I'l:',:, \r,,l
larl IMlur, n :{(l.(MH)an.l:W().(KX) species. In onlt
ial thai ur continue to int.
- of collection befo
Key words: Amazonia, biodiversity, Brazil. Bin nei Darnssalani. Cameroon, conservation. 1
ao P.D.K.,
Madagasca r, New Guinea, palms, troj ,ICS.
The purpose of this paper is to show, with examples from a few places, that the tropical flora
remains severely undercollected and that many
new species of am
nln tie to lie (liscovered and described every year. The destruction of tropical hal la * boll n i
is <>l" rainforest
and in savannas continues at an alarming rate
and this before we have completed the inventory
of what exists. As a result of the incomplete inventory, we seem to be underestimating the total
number of seed plants in the world. We have
identified a few areas of the world where further
collecting is urgent and destruction of vegetation
is continuing at alarming rates from a variety of
causes. It is our hope that this will encourage
greater efforts in both collection of material and
habitat conservation before it is too late. The areas described are places in which the Royal Botanic Gardens. Kew, is involved, and they serve
as examples of what is also occurring in many
other places and in many different ecosystems,
both tropical and temperate.
'
THE MATA ATLANTICA OF BRAZIL
We commence with this area because its deabout 6% of the Atlantic coastal rainforest of
Brazil remains intact. It has been devastated
, the Inslhulo Y,
i.
mainly In tin -stall

cacao plantations
and sugar cane fields as well as by other types
of farming. Many studies have shown the high
level of endemism in this area. For example, Mori
et al. (1981) showed from a sample of 127 trees
described in Flora Neotropica monographs llial
.">.' .Vv were endemic to the Mata Atlantica.
There is no doubt that some of these locally described species are now extinct. However, recent
collecting in the remaining fragments of this ecosystem continues to turn up many new species
arid also interesting disjunct distributions. Two
examples of this are Brodriguesia santosii R. S.
Cowan and the new genus Harleyodendron, with
its single species H. unifoliatum R. S. Cowan
(Cowan, 1979, 1981). An interesting range extension is the recent first collection of Anthodiscu.s (Caryocaraceae) in the Mata Atlantica, a genu
* that was previously only known from the
Guianas, western Amazonia, and the Choc6 in
Colombia. Ant ho disc us amazonicus Gleason was
found in the forests of Bahia (Prance & Mori,
1980) and added vet another Amazonian disjunct
to
^ mY <il'd b>' Uma <1953>-If the remnants
of the Mata Atlantica are yielding so many novcities, what have we lost in the 94% of the region
remnants, now
vital for the fi
mel Hopkins, and all the Beserva Ducke team
Card. ns. Kew. liichmond. Slurry \\\<) .V\B. United Kingdom.
ANN. MISSOURI BOT. CARD.
87: 67-71. 2000.
Table 1. New specie* I

<I in the KM) kite Reserva
Florestal Adolpho Dueke. Manaus. Brazil in the course of
preparing a flora.
,
Famj|v
:
1945 for the Flore de Madagascar et de.s Comores

by Jumelle and Pemer de la Bathie, acknowledged
experts on palm taxonomy. The volume described
f
sp;.." s
''1,)0'"'"'"'
"
Areeaceae
Lecvthidaceae
Passifloraceae
Chrysobalanaceae
Rubiaceae
Other families
i
,'J
3
2
2
9
Likt- many tropical countries with a half-finished

flora< t|. families that have been treated in such
floras are incomplete. The Palmae were written in
based on serapp\ *pe(mien* and therefore the keys

failed to work lor most ta\a. Consequently, palm
information for Madagascar was confused, and this
ôr a family in which many clhiiobotanical uses
recorded: palm* an ii-i (I for food, construction, basketry, m.-d
and many other items in
Madagascar.
When Uhl and Dransfield (1987) published their
were
monumental Genera Palmarum, their main probships were in Madagascar. Therefore Dransfield
embarked on a series of field trips to the island,
l)ut
TtlK RKSKRVA Fl.OKKSTAI. Al)OI.F() DlCKK,

A\l\/o\\s, BltAZII.
collected areas in Amazonia. In 1993, we set out

to prepare a Flora and a field gu.de to the rescne
and initiated intensive collecting. The preliminary
list from the INPA herbarium database contained
825 species (Prance, 1990), and so we assumed we
were working with a flora of about 1000 species.
Mve years later we now have 2175 specs to be
ncluded in the Flora (M. Hopkins, pes. con.m.i.
rhis includes over 50 new species (see Table 1).
rhis work shows the value of the intensive study of
i -mall M a >! ' :o i. a 'me-i n d ll c value of lie
das. The recently published Morula of the fores.
. a^,.^ Iqmtos, Peru, published^by the
olanioal (,arden,
cal flora that has helped to improve
he botanical inventory of an ana (\
nez, 1997). In order to complete the
/ of the tropics, we need many i
V "".',''/'' "!' ;'"'" "]"' '
> '
detailed flonstic studies of small areas.
*<><>'< started discovering so many new species

l additional inv*tciie* thai he decided a special
Madaa*cai |)io|.rl wa- needed. With funding from
V],.| )(||la|(|v ,.|Vs|;ml,mls ([ k) . pn)Jr(, was set
U]K an|| H(.nk Ht.(.nt)(, sta,V(] w()rkmg f()]. {[ jn
an(
This 100-knr forest reserve near Manaus i ,,.tral Amazonia was believed to be one of the best-
the
a*
in---
Madagaseai is another place that is notable both

lot its high level of endemism of plants and animals
and for the rapid destruction of the natural vegetation. It is also badly undercollecled despite the
recent efforts of both the Mi.*.*oun and Kew gardens. The latter has made a recent study of the
palms, which serve as an example of what remains
robe done and what can be found when specialists
l a particular group of plants.
1991
He
,;.,,
m Vl.,daua>e.H
travelillB al] over
,,,
lor a year and a half,
east (,)ast in searrh ()f palms.
The results of this fichlwoik phis fuilhci visits

by Dran-lield showed how much vve did not know:
.' new gcneia ami !'.') new species were discovered
(Dransfield & Bee.itje, 1995). These included the
^.^ sma,|rs( pa|m {l)yftxis u,mussima fcenX]e,
,(.^ ,ll;m ;) ,,,, ,,,..,,, , ,U(, jM)-ft.et-high c
î.
,u ., T/_;~-/_ /
L.._... -.
Voanioala, Ism urophoe
utiia mraka Beeiii|c and an ama/uig aquatic palm.
The latter, Ravenea musicalis Becntje. ha* seeds
ia| ^ m ^ ^ A sma)1 bump ^ ^
fish> ,,.,, wj||I< am, ^.^ ^ ^ which then
sinks. The seed has already developed a half-inchlong hooked seed leaf within the fruit (a strategy
analojious to several mangroves), and this hook
call he* <>N projections on lli. -lie.mil.ed. enabling
the *eedluig lo *tail root nig. The w on v mg ihiiig is
^ ^ ^ mi|> ^.^ (<( ^ m a sing]e ^
in which 450 trees have been counted. Many of the
newly discovered palms have very restricted distribution. and coii|)led to the threats to the vegetation
where they occur, this emphasizes two things: the
need to conserve, and the need to inventory such
dwindling habitats.
Vet another new genu*. Sutranala, was known
from a lew tens of trees in a single reserve; on a
recent trip, Dransfield visited a second newly discovered site, bringing the known numbers to the
low hundreds. Why are such palms so rare? In the
rase ol Sdtniimld. flun- IS an intriguing hypothesis.

The fruit oiidocarp i- hard and -hows strong flanges, unlike any other palm endnearpapart from a
few taxa from New Guinea, distributed by cassowaries. The hypothesis is that Sdlranald was distributed bv the giant elephant bird, the roe of the
Thousand and One Nights, the Aepyomis of science:
a bird now extinct, though its subfossil eggs are still
found on Madagascar. Then-lore, because byno;///s
is extinct, long-distance dispersal of Satranala does
not lake place am more, and its area of distribution
le meantime. With information from projects such

s these, focused conservation can take place next
> general COIIM-I \ at ion. and -ave specie-. Will I
Palms are one of the groups of plants that one

might expect to be well known and well collected
because they are often both large conspicuous
plants and almost all are used in some wav by local
peoples. On the other hand, non-specialist collectors have tended . itli. t to avoid collecting palms or
to make poor specimens because of the special difficulties of collecting such large leaved and often
spiny plants. A brief summary of three recent held
projects involving John Dransfield shows what still
remains to be done in the field to gel even a basiccatalogue of palms.
With relatively few species (about 20 in all I. tin

compared with Southeast Asia (Lhl & Dransfield.
1987). The rattans that do occur are certainly conspicuous and are sometimes visible in great thickets along roads in perhumid anas ,,f equatorial \frica. They remain poorly understood, largely
because they have rarely been adequately collect
genus Laccosperma (ca. 5 species) there was one
large-diameter species. I.d,-ttspennti set midi/lorum
(P. Beauv.) Kuntze. Beccari had described a second
large species, L. acutiflorum (Becc.) J. Dransfield
las \n< islioplniiiun aeiitijlorum Mecc.l. based on
very poor material. Subsequent workers have been
content to include the latter as a synonym with /..
setiiidli/ldiiiiii. Dining fieldwork in December 1997
near kribi in Cameroon. Terry Sunderland and

John Dransfield found extensive population- along
the main road of two clearly distinct, easily sepanamed taxa. They found it astonishing that two taxa
so clearly distinct, could have been confused; no
doubt the difficulty of collecting these spin\ plantwas responsible foi then pom- n-pi-esi'illation in her
baria. Terry Sunderland is now conducting a critical
survey of all African rattans to put their taxonomy
in Lao P.D.R. As a result of a preliminary survey

of rattans bv the Lao Forestry Department, funded
by the International Development Res
rattan iti Lao I'D.IT. but these have yet to be critically named. In order to provide a firm base lor
future rattan development in the country, the Lao
forest Department, together with Oxford Forestry
Institute and Koyal Botanic Gardens, Kew, has
-tailed .1 new critical survey of Lao rattans and eco
logical work aimed at understanding the demography of Lao rattans. This is funded by the UK Darwin Initiative. One <>! the first and most surprising
results <,f the survey is that the premier large-diameter cane that i- being harvested in huge quantities in Lao, much of it being shipped oyer the
border to Vietnam, appears to be an undeseribed
Until the start in 1988 of Kews project to prepare a checklist ol Ihe plan'- ol i-iuuei. there were
a mere 17 palms recorded for the country. Yet this
small nation has one of the highest collecting indii < s I.a |ht vvl ol
I ili /
, 1/
utirid n gion
just
of statistic
thai added to the difficulty
just the sort
soil of
slatiin justifying further
: of the Reserva Ducke, indwork in a relatively well collected area
by specialists always yields results. By the end of
the project in 1995 the palm list had risen from 17
to 140 different species, showing that almost half
the Bornean palm flora occurs within the well protecled forests of Brunei. During fieldwork several
unusual new laxa wen unearthed, including the
smallest species of Liiistonu, L exigua J. Dransfield, the handsome Pinanga yassinii J. Dransfield.
Peninsula |
Howev*
' mil K I aisen 11 owia< . .11 I.
Of all the places in the tropics, New Guinea

probabK n mains the 1 asl known This is coi la inK
>-\ idetit Tom die results of recent li< Idwork orga
rn/ed In kew in Irian Jaya, where a large rumihei
of llie (dllections turn out to be new species. In
Irian Jaya, colli'*
licnsil
h
ess than 2.") specimens ha\c been collcctcii ( 1
100 km2, and there are only slightly under 140,000
colli clions horn a ti iriiorv niili an est mated Nora
of 25,000 species. The neighboring Papua New
gpei u ii us pei 100 km and is a so poorly known.
New Guinea offers a particularly large range of
habitats because ol it- rugged topography, where
\on can go from coastal mangrove to the glaciei on
Mount Jaya in a distance of only 110 km. The flora
vanes from tropical rainforesi to high alpine New
Guinea is a cent.
tropical groups such as tree ferns {Cyathea and
DU
.1. Pandanaceae (a recently collected new
species has thick flcdn, fruih -melling brads that
are eaten by bats. ,-! n !
n p obabh Is . hua
lore)
i Mvristicaceae (for example, the recently
desciibiil rmtmej spi-i ics \l\r;s;n n;n,;;;:ni,\ \\
J. de Wilde).
Fieldwork in Irian Jaya is also turning up many
interesting new records such as the recent collection of Ternstroemia magnified Stapf ex Ridley,
Kiel
is thought to b<
istrib ii d from the Malay
The importance of collecting these basic data

ah .ul the plants ,,f Vw (iuiuea has be. n ortipiia
sized by the fact that Robert Johns has been able
to prepare maps of proposed conservation areas for
1
n Java and Papua New Guinea. These
maps are based largely on plant and vegetation da!a
assembled as ine tesuii ol lohiisV, colic. : iit> acti\
ities. This application to systematic data is a vital
activity in an ana where it is not too late to conserve large tracts ,,! I i-.
which is now under severe prcssuie bom belli mm
How
MANY SPECIES TO GO?
cies of angiosperms in the world is 250,000 and

was otijj nalb I a-ed on : aloidat ion lt\ Sti bbius
(1974) and continued or cited bv many other authors, including myself (Prance, 1977; Groombn ig. I'>02|. Hi.-sc calculations were based on a
family-by-famib
and provided a
good estimate based on data of the 1970s. However,
considerably. Data in Table 2 show the descriptive
activity of botanists between 1989 and 1997, during which period 21,097 new species wen- de;
.-i I" ' I niili. 'in >n
I . ''n i ,11 rate has not decline! over the nine years involved. This is backed
up by data from other sources: for c\an
";
of the species treated in Flora \eotrop
a too
grapl s arc new < V\ in \\;\\ l< I'hnmas. pei>. < utmii 1
there is ob\ioiil
. <
done, if an average of about 2350 species are being
added eacl pear; md secondl) despite the many
. 1981. New taxa of l.nutmi

.!. i
deae from Bahia, Brazil. Brittonia 33: 9-14.
Dransfield, J. & H. Beentje. 1995. The Palms of VladaPalm Society 11 MSO, Norwich.'
,
we are still describing species at the same rate.

The fact that we have added 21,097 species over
nine years, and also the comparison between 1970
and 1997 data for a few s,
A \
> <
leads us to con< In
there ;m
I
i
300,000 and 320,000 species of i
oolril M I-
I!
I.,
1 I ,1
,1 l!|..dm-.s,|N
S|.,
tus of the Karth's Living Resources. Chapman iV Hall.
Mori, S. A., B. M. Boom & G. T. Prance. 1981. DistriData from both the undercollected areas deribcil here and (IK- studs (l the rati- ol des< nplion
the field inis necessary to conli.'ii
I
i - <id
i
sources into fielduoi !> in I .! - i |. i mn
and not be tempted to divert them all to the equally
important and e\< ilingnew techniques of moloeiilui
systematic*. More detailed studies ot selected small
areas in the trop
k<
I
inai
new species as well as most useful demographic
da\l limit iho-e t ll.lt ,iie alte.idv d.-cilLed. I In
more complete t lit inventory is (lie hettei the data
VMII I
lor
stamable i
for i
. nasial foosi ti(< sp,-. n- Hull..ma ii 2(1 lil .

Prance. G. T. 1977. Floristic inventorv ol llic Iropics:
Where do ,
sla.ulV
\.,. \1iss(.,i |!e[. (,n-.l. .. !
(..<)
. 1990. Floristic composition of the forests of c,

tral Amazonian Brazil. Pp. 112-140 in A. Gentry (<
itor). Four Neotropical Forests. Yale Univ. Press, N
Haven.
& S. A. Mori. 1980. Ueview. Anthodisrus (Ca
549-560.
itebbins. G. L 1974. Flowering Plant,: Kw.lm
the Species Level. Kdward Arnold. London.
Jhl, N. W. & J. Dransfield. 1987. Genera Pal
' F.-1 .i 1 "i-.
../
'.ill. -
Based
,,n
tin-
work
. II ]'><>:. I -Unlade las Hcsenas Bi,

to-. Peni. \llpahuavo-Mishana F.\ploi
plorama Lodge. Mnnnar. S\sl. B..I. Mis
WHAT IS SIGNIFICANTTHE
WOLLEMI PINE OR THE
SOUTHERN RUSHES?1
Barbara G. Briggs
of the charisma seal.' arc the southern rushes. \ n-I rnl ia'- i. lal i\ <l\ i
trolepidaceac, Kcdeiocoleaceac. Anartlu iaceae). Despite
In I In- Poaceae. these li.nl been greatb neglected lui ,>\
. DNA sequencing of plastic! genes gave surprising results,
two new plant families -! <ul I i , ,
,|. New findings are contrihuting to helter understanding ol the an
related families and Soi
I
,
n, lntig the new rare species allows focus on their con;
needs. Many new species are still being recognized in Australia's flora, among flowering plants and conifers a
other groups. Wollemia and the southern rushes exemplify the significance of these new finds and newly di
understanding of relationships. In each rase the significance of the discoveries is realized only in the conte
knowledge of organisms and their evolution that comes from research in many fields.
Keywords: Araucariaceae. Vislralia. conservation. Uesliotiaceae. N.ulhern Hemisphere floras. Wollemia.
WOLLEMIAA CHARISMATIC SUBJECT FOR
RESEARCH
largely protected from wildfire, although one tree

showed evidence of fire, followed by resprouting.
.,,_..
In 1994 my colleagues ami I at the National He,-
The trees are mostly emergents overtopping both a

^^ ft.m ,
;m(, a
rf closed forest
l
"-! of New South Wales ii, SvJn.v tea ized that
I
we had been given a remarkable opportunity
the
(!isci)\er\ of a new nianl -.IH-CIC-. :L<I would catch
. ,.
^ ,
.
...
.' .
.
..
public and scientific attention in a truly outstanding
Endl. and Ceratopetnlum apeluli

,
,
,
Ill <
K'Sel.M.ihi
-' :": |U Nil - . Til^ ^ }^ ^ ^ ^ ^ ^ ^ ^
Wd
?duCe f f
leaV6S
unless a l,reak
l'rurs
>\
cr>
' ^^ t0 8 l
in t,u :ano
' <
Py-
matUrit
Davul Noble of the New South Wales National

Parks and Wildlife Service had found about 40
0~ annn
trees of a |)reviousK unknown species,
soc k~
named Wollemia nobilis W. G. Jones, K. D. Hill &
J. M. Allen, a new member of the conifer familv
extensively. The family appeared in the late

Triassic, with a peak of diversity in the Jurassic and
Araucariaceae (Jones et al., 1995). This rare and

highly restricted species had been discovered about
200 km northwest of Sydney, in a deep gorge
bounded by sandstone cliffs (McGhee, 1995; Duffy,
1997). Such a site would differ from most of the
surrounding area in the constancy of water supply,
* continued decline since the end of the Cretaceous

(Miller, 1977). Some of the earliest Araucariaceae
are reported from the Northern Hemisphere, and
fossil pollen with 4raumria-like features is widespread in both hemispheres in the Jurassic and
Cretaceous. Its present survival in the south is thus
more equable climate, and especially in being
relictual, rather than implying a Gondwanic origin
The lossil
studied
'I thank my colleagues John Benson. Sue Mullock. Ken Hill. \dam Man haul. I'aiiicia Meagher. Cathy Offord.
Carolyn Porter, and Brett Summerell for discussions and for making availab
I'
il \l. <.. rlv
assisted with the illustrations, while Vville Mar. haul. Hindu, ol ih. I'KIMII l,e, ba, mm. and Bruce Fuhrer gave
permission to use photographs.
-' Royal Botanic Cardens. Mrs Maequaries Road. Sydney 2<XX>, Australia. bgb<" rbgsyd.gov.au.
87: 72-80. 2000.
Wollemi Pine or Southern Rushes?
(Gilmore & Hill. 1"'

hi et al., 1998). Before the discovery of Wollemia, the family was
known from Sou
'
'
eastern Australia, New Guinea, and. in
!
rich diversity, in New Caledonia. Two extant genera
had been re< i gi - '..
nd \gathis.
The newly discovered Wollemia created a senmi 1 li
i- i ii d i
nil- largeup to 40 m
tallthat it was almost unbelievable that it had
II111 Ik ed w iili fossils that connected to anciei : ri < >i 11 is.
back to the Jurassic (li-. 2). and this in an age
when dinosaurs have an unrivalled fascination for
adults as well as children. Its habitat, in deep
ni( i.ii'
\ I'II -. in 'd ! IIMI -i -uu-lei ap|n al.
What followed would not apply to the average
newlv found species.
A media conference was called to announce the
discovery. This limuidit a response thai e\eeedei)
our expectations: il was brielb Iron I page news m
the press an mm
. king lurlhei infill nial i il . lelc; prepared, feal si ing
!I'
-1 I - 'jii'-nt resean Ii.
i|
i nl
il
i i N
sh. I')');,
aiM|
in moniioi ihteaS n:d

>n- all. eting its survival.
Sine! protocols lot MSI|- !O lh< habilal were eslale
lished. espeeia l\ < aaiign.g shoes at entry to the
site, to avoid bringing in pathogens. Approvals to
Milton Silverman, who had gone from San Francisco with Ralph Chaney in 1948 to collect the
dawn redu I < l/c/./vo//, out j."'i ;</.A/O,/. >!,-. \\;\ A,
W. C. Cheng) in western China, wrote in congrat
ulate us on our efforts and the discovery, which was
iiii! -I ironic considering how much more accessible our find had been than theirs. The name
"Wollemi pine" was coined so that we would not
ery of a plant that had not yet been bolanioallv
i atned. "11 e ititn pid iravi >T~ in I J ina had coined
"dawn ie. Iwoi ;l p. ilk I . ii.-- Mrhr,- 7,,,'.'r, . !:,.
umn in reporting their eo||e<
which, shortly before, had been discovered and

compared with fossil species.
Horticultural research and propagation started
immediately, using cuttings and -cods (Fensom iX
Cretaceous (Macphail et al., 1995; Chambers el al.,

1998). The most recent fossil records of this pollen
type, from Bass Strait, are about 2 million years
,,||,i..
Offord, 1998; Offord et al., 1999). The aims were

to learn the propagation requirements, establish a
conservation population in cultivation, and even-
was
ally to safeguard the species by widespread use

I horticulture. As i
was found to be plagiotropic, with plants raised
from cuttings of lateral branches mostly continuing
to grow horizontally, whereas those from erect stems
continue erect growth. Advertisements for commercial partners in rawing large numbers of plants
lnciiuhl main t>n.|>o-.aK When ;i suing tree was
lanted m the F
na in Sydney,
. .
.
. "
,
.
'
tins v\as done v\itli ooroiiiom In a semoi ^ncni
ment member, and the plant was enclosed in a very
stout cage
Offers to collaborate in a diversity of research
approaches flowed in, 30 within two weeks of an-
An endophytic fungus, Pestalotiopsis guepinii,

isolated from Wollemia (Strobel et al., 1997)
taxol, which ha:
and found to produce

properties
and is effective in controlling (
fungi. The r
to common pathogens were studied (B. Summerel^ p(Ts (.()mm }
More than 5Q tax& of fungJ
haye been recovered from the trees and their im.
mediate gunoundi
in a survey that cultured fun.
^ ^^
^
^ ^
',,-,
,
, ,,
tibility
...
. , r
.
,
thought to lie i\|.|eal I..I ,1 lie. specie:, I] s||i ;i .Hi
'
.
ronment> but compansons are uncertain since
tree s er,es nave been
P
examined so compre-
^^^ 0f thf^ 50 fu"gal taxa' 9 are thought to

""described species. Some roots are densely
be
nouncing the discovery on the TAXACOM listserver (Brooks, 1997). Studies of genetics, chemical
constituents, embryology, and anatomy, as well as
filled
with
endophytic fungi whereas ectophytic
fungi are found in other cases, an unusual condition
observed also in other conifers (McGee et al.,
associated fungi and insects were soon focused on

Wollemia. Sequencing of the plastid gene rbcL (Gilmore & Hill, 1997) confirmed the distinctness of
Wollemia, although different analyses using different ranges of otlu
phylogenies for the Araucariaceae. Gilmore and
Hill (1997) and Stefanovfc et al. (1998) found Wollemia to be sister to Agathis, with those two genera
1999).
Other studies have focused on Wollemia especially because it is so rare and vulnerable (Benson,
1996; Offord, 1996). Wollemia was found to be susra cinnamomi, which has been introduced and is
spreading in southeast and southwest Australia,
confirming the need for strict protocols for site vis-
trast, Setoguchi et al. (1998), using the same sequence data for Uo>''
, u > unbim
w it I i I i
ferent range of other conifer taxa, concluded that
Wollemia^ diverged before the separation oiArauy
Comparison of Wollemia', adult and juvenile fo' - '
i
tld C.,1
.,-,,:!.
living and fossil Araucariaceae (Chambers el al.,
1998) helped in the interpretation of fossil Arau-
among
individuals, although more than 800 loci

with AFLP fingerprinting. There
evaluated
were
may be some clonal spread, since plants

findings
^
,
interpreted as
, e
,argely
extended genetic bcllleiii ek

\iinl!i:.\ .ii d
\KU
I'M
> i
the
long time, an
lmimar\ data on
aim. w hi - s'uimirig some \ ana
si a <, and seed, lis tree an Inlei Inn- was described

as unique (Hill, 1997), differing from previously
family as a whole (Peakall, 1998).
aceae. Male and femalecones are each terminal

a first-order, short-lived lateral branch, and coppuing is a consistent feature. Leaf anatomy has been
studied (Burrows & Bullock, 1999) and so has reproduction (Offord et al., 1999). The pollen was
found to be indistinguishable from the fossil pollen
form-genus Dillwinites, which is recorded in AusI New Zealand extending back to the late
in the media and from

scientists justified? This
question resonated especially when answering
questions about the scientific significance of the
fi
nd, while in my view the slender silhouettes of
other members of the Araucariaceae towered over
trees of lesser stature on the skyline of Sydney's
Royal Botanic Gardens. That question will be considered ill.
i
l .
Was the concentration of attention on Wollemia
THE SOUTHERN RUSHES
The Restionaceae and allied families in Australia, the southern rushes, are as much in need of
charisma as Wollemia is blessed with it. The flowers
i- nspi(
- >ulh small scarious bracts,
glumes, and tepals (Fig. 3) and with the leaves reduced to sheathing scales (Meney & Pate, 1999).
They occur exclusively in low-fertility soils and in
arid or seasonal!) waterlogged sites, habitats avoid alli<
r
daceae, the plai
Through si
have brought
gleet over the first half of this century. Before then,
the three great < i luu - << \ustralian botany
had made a good start on their discovciy and ebissilieation. Bolx-il Brown, naturalist on the first eir
cumnavigation of Australia in 1801-1803 described seven genera and 47 species of
Resiionaoeae that arc ciit'reiitly recognized (Brown.
1810). A further 10 species were named by Ferdinand Mueller (1873), whereas George Bentham
(1878) recognized 71 species. B> the early 1960s,
when L. A. S. Johnson and I started our investini.cr,
< l.ii.l c
86. Around thai time also David Cutler of the Royal
Botanic Gardens, ken, made extensive anatomical
investigations (Cutler, 1969). It became clear that
the generic classification was entirely inadequate
(Cutler, 1969, 1972; Johnson & Briggs, 1981;
Briggs & Johnson, 1998a) and that many specimens
matched no named species.
Clearly this neglected plant group would present
a fi nil' - !' Id -i in. ;. disc iveries, but it far excei
I expect a us. The cries have been
both new species and new i.
i i
ilionships. necess tatiug a radiea re< iassilication.
In recent decades, great swathes of country had
become n
.iccc--.il.lc. e-pccialls in the sandplains of \\e>t
I
i
I onal ones. Even

the largest of all Australian restiads, with flowering
stems over 2 m tall, is among the recenth discovered species vet to be formal!} named, Investigation
of supposedly satiable species often showed these
to be assemblages of several allied species, each
with a distinct , c distribution ard ecological range.
The s'liMh brought to light 51 new species, moslh
from the south of Western \uslralia. Jus! when we
ought
in Restic
, colleagues in Western
Australia found a further 10 species (Meney et ab,

1996). There was notably little hybridization among
the species; the dig
Restionaceae show an exceptionally high j
waiting publication.
The new view of Australian Restionaceae did not
top at species. When this study began, 29 Austraian species were named within the genu- Restio,
>ut it became clear that Restio was a membei ol a
roup of genera limited to Africa and Madagascar
Cutler, 1972; Johnson & Briggs, 1981; Linder,
985, 1991; Briggs & Johnson, 1999). Therefore,
all the
s (Briggs i
showed a patt
,"'1 I'oto that in Proteaceae, Fabaceae, Ericace;
area," in thru post-( iondwariii florisiie richness.
The history of climates, migrations, and survivals
has left different traces on the African and Australian continents, so that Africa h is I irg< t u ib<
i i
species in relatively few genera, but Australia has
i d ' rsit) of groups appropriate for recognition as
gi II. ra This pattern has shown even when the same
... i
studied groups in both continents, rather
than being an artifact of difli ent genei
com
(Belei Weston, pers. comm.; Nigel Barker, pers
comm.), although it is not apparent when Proteaceae of the Cape Region are compared with only
the southwest of Western Australia (Cowling & Lamont, 1998). Our case led to the description of the
rather alarming number of 16 new genera of non\friean Best ionaeeae (Briggs y\ Johnson, ]i)t)i\n\
Morphological cladistics (Linder et al., 2000)
and DNA data both indicate that an early division
within Bestionaeeae is between the African clade
and the Australasian clade (though the DNA data
give only weak support). This would be consist) nl
- . ii single species in South America. \i>ixi<is
,,.', . .'" nsis (Gay) B. G. Briggs & L. A. S. Jol uson.
is extremely similai to the New Zealand i. .similis
(Edgar) B. G. Briggs & L. A. S. Johnson, indicating
long-distance dispersal. Moreover, \podaswid (recently segregated from Leptocarpus; Briggs & Johnson, 1998a) includes foredune coastal species and
is the only notably salt-tolerant genus of the famib;
I is singularly well suited to establish success! ill,
aftei dispersal.
Sequencing of plastid DNA was done in parallel

v, ilh n:.>'|r>."|. ,gic ! .Hid cs and ga\e a f M I I IK T unexpected result, evidence that two new plant families should he recognized (Briggs el al.. 2000).
rd /.i.'
ire -in.ill genera, of two and
three species. respectlv eh (one juries of each gehad never been questioned, even when they were
the subject of detailed anatomical investigations
(Gilg, 1890; Cutler, 1969). But
D\\
sequence data (from rbcL, and from the tin\, itilron
with the trn\. tinV spacer) are consistent in groupi i i i i
i i I KM
I < ! I HI sii|)|Mni) with
Anarthria (Fig. 4) rather than with Beslionaceae.
That grouping is shown in a lackknilc consensus
tree (rem an.ibsis of the total sequence fiom these
I)\ \ regions and is further supported In the pros
i (Fig. 4).
Although further investigations are needed and
pro. ceding, it appears that the Anarthria clade | bi
the s|s|.-| group
to Beslionaceae. That position appears to be held
In Centrolepidaceae. Such close affinities, or even
inclusion of Centrolepidaceae within Restionaceae.
have been suggested on morphological and -niln\
oh.gical mounds (llamann. 1962, 1975; Kellogg &
Linder, 1995: Under et al.. 2000) and now have
some support (although not robust) from ariahses
of DNA data (Fig. 4; Briggs et al.. 2000). It has
been suggested that Centrolepidaceae are neotenoiis. wilh maluie plants showing some similarities
to seedlings of related families, although then in
florescences are very different.
Despite the evidence that Ilopkinsia, Lvginia,
and \riarlliria form a clade. |IK\ share no synapomorplues of morphology, anatomy, fla\ononis.
pollen, or seeds, except for features that are either
plesiomorphie within the I'oales or widespread in
the ordei. Similarly, studying these genera in light
of the DNA data showed that those features that
they have in common with Restionaceae are plesii.m.iiphics. although each has distinctive autapoinorphies. llt>i>l,insia has a reduced carpel number and succulent indchiseeiil fruits. Lyginia shows
a distinctive arrangement of thick- and thin-walled
cells interspersed in the chlorenchyma. sloping stomates. fused stamen filaments, and highly distinc-
Anarthria lacks a sclerenchyma cylinder in the

culms and has unreduced, ensifonii leaves and also
large chromosomes (Briggs, 1966). Such chromosomes are, in general, associated with large ge featu (Be,
logg. I)>7: Bennett K Lctd,. 2000). \\ ithont some
morphological basis there appears to be no case for
enlarging \narthriaceae or describing a single new
lamik toi Ilopkinsia and Lyginia. The most logical
course is the recognition of "Hopkiiisiaccie" and
l.sgiiuaceae." ami these new families are being
d( -i lib--,I i In i-v.- ^ Johnson, in |ness|.
The families mentioned above, Restionaceae,
(.en 11,,I e|,i da, cic.
\iiarthriaceae,
"I lopkinsiaceae," "Lyginiaceae," together with the Fedeioeoleaeeae. Joinvilleaceae, and Flagellar!.i< cae. appear to be the closest relatives of the Poaceae
(Dahlgren et al., 1985; Chase et al., 1993; Duvall
et al., 1993; Briggs et al., 2000). These are all families with primarily Southern Hcmisphcie distribution. I-'specialb notable is their high concentration in the southwest of the Australian continent:
six of the eight families occur in that region and
four are limited to it. Together with nine other families the\ (-(institute the Poales as recognized by the
Angiosperm Phylogeny Group (APG, 1998). Three
of the other families are primarily in the Southern
Hemisphere (Hvdatellaceae. placed here but with
little evidence. Prioniaceae, and Thurniaceae).
while six arc distributed in both hemispheres |l\peraeeac, Fi locaiilaceae. J iiiicaceae. Sp.uganiaccae. T\phaceae. and \y ridaceae). The concentration of allied families in the south has led to the
suggestion that the I'oaceae itself had a southern
origin (Doyle et al.. 1992), although these distributions could also he icln tual. as uilh the \raii-
iit'vv species and genus in a recognized plant family,

but an exceplionalK .li.ui-sfii.iti< and interesting
find. In Restionaceae and its allies we have some
raphvllum suhs|. mcuohtrhuim. (cm,

els ( a. I nun long: photo Fi. Kuhrer.
s ea. (> nun wide: photo B. Kuhrer.
531
, 82 P^
JtH
|_75_,
DesmocMu.c.s
Harperia,a:er,ora
Cottoca,y,9,a
! families. Neither of these example's is typical

Memia created unprecedented public, media,
scientific interest. It raised public enthusiasm,
ml kn .-.ledge of environmental and
biodiversity conservation issues. Its importance ami
rarih make it a vvonderlui example in eraieatioi
programs am: politii/a contexts 1: has cmphasi/ei!
. vane, of findings mlh, I!es|i,, ..eeae. The historical kogeographv oi world floras. especiaM\ lhos
of the Southern Mem spin re. provides a context for
discoveries in both these groups; findings in these
gro ips. in ti.it . elai ilv ;ispe< ts oi' !ne dev. lopmeni
\l'(,
in species survival and given a focus for programs

to explain tl . i.atun o< Molov). al le- m I lo m
\ estimate Us significance and conservation there lias
been research in systematica i I
ti
.atioi.ships. palaci.tilf.io!.\. ce.)|i.L'\. -en. ' . s. plait
pathology, mycology, and plant propagation; this
has helped to publicize the role of all these disciplines (Hill, 1996). School groups, government
members, and the general community are enthusiastic about seeing the plants, so it has raised the
profile of our ho'.aim gardens ami oi tried s. ei:;:fi.
and cduealioual piogiam-: it ha- also been i tn.i|. >r
profile raiser for the New South Wales National
Parks and Wildlife Service. Wollemia has oontribearia< < ae and eomfer-mveorrli /al
survival has added to the picture of long i rra
ii in
i kips > ven a step in the
nii'ii tl I
regional replacemet
Hi wt in- pi ami- \l|.
i
lei d< -I period of small
popul iln ii si/, . it shows no di-i < iinlil. ii,ii t-pianl
genetic diversity.
Our other example, Restionaceae and allies, was
probably the most neglected of all substantial Ausliahau 11..vs. riui- pi.ml M..U|>S and so wa- the ticli-
i,
in
V\
U,
Ci
n ordinal
|). MM, i - MI f.-i
ler-a
1514.
Benson, f \{>(><). flu. al.-ned hy discovery: Research and

.
I i ,\ \|le I',,
Maxwell (editors). Back
Hire,i
Sydney.
r.enkam. (.. I78. Flora
II-.. I'*",-, s s,, ,;, ,. A .

from the Brink: Refining the
. . r-. Process Surrey Beatty.
Australiensis. Vol. 7. Peeve.
tralian monocotvledons. Contr. New South Wales Natl.

Herb. 4: 24-34.
v. classiliealioii oi non Vlnean Ii. -Vonae.-.

a 8: 21-31.
-&
. 1999. A guide to a new classi:
leslionai ear and allied families. Pp. 25-56 i,
iey & J. S. Pate (ed . I V I, ,1, n, 1,'u l
,e arid
ki owl< de <>f relationships within the Heslionaceae

< iardi. s ai install, e al tin distinction between the
intercontinental links that date from at least Gond
wanic times and those that may represent relatively
recent lonjj distant < dispersal. In addition in greater understanding of Southern Hemisphere floras,
there is improved understanding of relationships
among the families of the Poales, with the recognition of the Anarthria clade and further c
stration (Fig. 4) of the closeness of Ecdeiocoleaceae
to Poaceae, in agreement with Doyle et al. (1992).
Both example n. -i.-i ik anl but in each case
the significance of the discoveries is only fully realized in the context of knowledge of organisms and
their evolution that has been established by research in many fields. The history and antiquity of
the Araucariacea. m 4 > H. /'< , / so notable. Similarlv uli nishij
tin Poacea. adds to the rel-
I ' >'
l!l (..ml 8> -,il V>1

Bennett, M. D. ft I. I. I.eilch. 20(H). Variation in nuclear
I .vgm.aeear. I
Ss.len.alles an.! K Inl ,,- ,: M :,..:- -i,. CSIIJO. VI ,

imok> V IW7. The weh in the (,aniens. Pp. 66-68 m
B. Diekman, E. Higginson, F. Sutton & H. Webb (edilors). Keologv al tlx C.itlinjr Kdge. \alare Conservation
""" vS. Wales, Sydney.
- Hollil
IBM).
Insulae Van Diemen. J. Johnson, London,
iurrows, G. E. & S. Bullock. 1999. Leaf anatomy of Wollemi I'm. \\\H nu ,:>I>,1'\ \l.lliear . . ,) \i.-le, .1.
Bot. 47: 61-68.
Chambers, T. C, A. N. Drinnan & S. Mclxmghk. P >>:',
So."i< rnorpl.olo.ijeal ie.iiun - .,1 V\o!l, in, Pan- |tl.r//r-mw
) Creta159:
H. G. Hills, Y-L. Qiu, K. A. Kron, J. H. Rettig. E.

Conti, J. D. Palmer, J. R. Manhart, K. J. Sytsma, H. J.
Michaels, W. J. Kress, K. G. Karol, W. D. Clark, M.
Hedren, B. S. Gaut, R. K. Jansen, K-J. Kim, C. F. Wimpee, .1. F. Smith, G. R. Furnier, S. H. Strauss, Q-Y.
Xiang, C. M. Plunkett, P. S. Soltis, S. M. Swensen, S.
E. Williams, P. A. Ca.lek, C. J. Quinn, L. E. Eguiarte,
ern families Mvrtaceae Proteaceae and Restionaceae

Pp. 429-469 in A. Keast (editor). Ecological BiogeogJones. W. <;.. k. I). Hill & J. M. Allen. 1095. Wollemi,,
the Araucariaceae. Telopea 6: 173-176.
Kellogg. E. \. X II P. Finder. 1995. Phylogeny of Poales.
Pp. 511-511' / P. .1. Budall. P. .1. Cribb. 1). F Cutler
Barrett, S. Dayanandan & V. A. Albert. 1993. Phyloalirs and Fvolution. Royal Botanic Gardens, kew.
Gard. 80: 528-580.
Cowling. K. M. & 15. B. Eamonl. 1998. On the nature of
Condwanan species (locks: Diversity of Protcaccae in
mediterranean south-western Australia and South Africa. Austral. J. Hot. 46: 335-355.
Culler. 1). F. 1909. Juncales. Pp. 1-357 in C. IS. \1.-l.-all.(editor). Anatomy of the Monocotyledons IV. Clarendon
. 1972. Vicarious species of Bestionaceae in Africa, Australia and South America. Pp. 73-83 in I). H.
h.-bl-. n i: M
aceae. Contr. Bolus Herb. 13: 209-264.

. B. G. Briggs & L. A. S. Johnson. 2000 li Mion
aceaea morphological phylogeny. Pp. 639-661 in K.
L. Wilson & D. Morrison (editors), Systematica and
Macphail, M., k. Hill. A. Partridge. E. Truswell & C. Foster. 1995. "Wollemi Pie" Old pollen records for a
I. II. I'. CI,lloU\ p |. Vo. 1985. The
. J., J. L. Davi
. Soreng. I). Gary
C ,i
origin of the grass family (Gramineae). Proc. (Natl. Acad.
Sei., U.S.A. 89: 7722-7726.
Di.fb. \1. \'f)~. Daw Noble and die Wollemi Pine. Pp.
I 77-186 in D. Foster el al. leclitn.s). Crossing the Blue
ralist Charles Darwin lo novelist David Foster. Duffy Si
Snellgrove, Potts Point, N.S.W.
Dmall. \l li.. \1. I. CI, gg. M. W. Chase, W. D. Clark, W.
J. Kress. H. G. Hills. E. E. Eguiarte. J. E Smith. B. S.
Gaut, E. A. Zimmer & G. II. Learn. Jr. 1993. Pin lo
genetic hypotheses for the monocotyledons constructed
from rbcL sequence data. Ann. Missouri Bot. Gard. 80:
607-619.
Fensom. G. & C. Offord. 1998. Propagation of the Wollemi
dig. E. I8<M). B. i
xerophilen E; M!I.' ;l .' li. Vi:,
13: 5} I (.()(,.
obilis) and a molecular phylogeny
Telopea 7: 275-291.
Embryologie der Centronerku
- l'.ai
un.l Bliile,islamic UM.I die svstemalische Slellung der
Familie. Ber. Deutsch. Bot. Ges. 75: 153-171.
. 1975. Neue l-nlersuclumgen zur Embryologie
und Systematik der Centrolepidaceae. Bot. Jahrb. Syst.
96: 154-191.
Hill. K. I). 1996. The Wollemi Pine: Discovering a living
fossil. Nat. Resources 32: 20-25.
I""
f.ll
-i
UM
il,
Bestionaceae from Western Australia. Telopea 6: 649-
Vlueller. I. 1873. Eragmenta Phytoj

8, fas.-. 62. Government Printer.
Nash, S. 1997. Wollemi Pine Speei
Offord, C. A. 1996. Conserving the Woll.-mi Pun:

legral.-d approach. Danthonia 5(2): 12-14.
. C. I.. Porter. P. F. Meagher & G. Errington.
Sexual leprodu. lion and earl\ pi.nil growlh ol illI'm, III //.-.
Peakall. B. !*! il ,. . - .
-enetic diversity in
an ancient relie. the Wollemi Pine: Implication* lu,conservation theory and practice. P. 86 in Genetics Soc.
Austral. 45th Conf. Abstr., Sydney.
Seioguelu. IE. I. \. Osaua. J.-C. Pintaud. T Jaffre & J.M. Veillon. 1998. Phylogcnetic relationships within ArBot. 85: 1507-1516.
Nei.uiov i, . S.. M Jager. J. I i.-nts.-h. .1. Bn.utin & M. Mas>e|,,i. |098 Plnlogenetie relationships of conifers inferred from partial 28S il>\ \ gene sequences. Arner. J.
Bot. 85: 688-697.
Sirobd. C \.. V\. \l. lies,. J.-V I.,. E. Ford, J. Sears, B.
S. Sidhu & B. Summerell. 1997. festal,,lin/isis ^nepinii.
a laxol-producing endophvte of the Wollemi Pine. WalIvmin lUilis. \uslral. J. But. 15: 1073 1082.
FLORISTIC SURPRISES IN
NORTH AMERICA NORTH OF
MEXICO1
Barbara Ertte
ABSTRACT
Contrary to recurrui
no evidence of tapt-nn- oil Hn
I,,.
i
IN
, , ,
no has heeii lullv explored and
paiticularly evident in western and southeastern North America, where dramatic
Furthermore, the same level of ongoing discovery also characterizes other aspects of floristic information. iu< hiding the
on individuals and organizations operating outside ol academia. wild declining opportunities for formal training in
perception ol flonslics as rote data compilation, when it is in la-
-el
iu,ili-i.
h con!
I of a massive attempt
The incompleteness -.1 our Holistic knowledge takes on eiitieal -1. 11111. ;11H e in an <-ra when decisions are being made
that will irrevocably determine the fate of our national floristic heritage. I - .
li tance can cut multiple
\\a\s. in- itasiuu II - ii - I rm-pl i - nil 'HI ,n li
.
Ill
il.ll ,-- i
I I, I lodiw isii\ Uthougli
\ield a vastly unpi
i II n i. ku
edge base for informed decision-making.
Key words: biodiveisitv. florist i.-s. North America, vascular plant flora.
Underlying much of our current land-use management planning, legislation, funding allocations,
,still hiring decisions :s the assumption thai he- flora
of North America north of Mexico (for brevity's
sake, hereafter referred to simply as "North America") has been fully explored, cataloged, and
mapped, at least to the extent that is needed for
informed decision-making. Or, to the extent that exceptions are allowed, it is assumed that such
knowledge accumulates in the form of static data
sets, descriptive rather than truly scientific in nature, and further that the existing academic infrastructure is adequ I
-Idi
i
ih< gaps
i
floristic knowledge. This paper sets out to challenge
these assumptions, as well as the equally common
perception that floristic surveys inevitably represent a threat to private landowners. The first half
of the paper provides testimony to the wealth and
diversity of ongoing floristic surprises in North
America, whereas the second half addresses the
factors that influence these discoveries and the resultant implications.
bow
i. --i.
- I.
ibi.s region is a rich
source of ongoing novelties. An effort lias neverthcless liini man.- i in- hide examples from other
geographic areas and representing other groups traditionally studied by botanists: bryophytes, algae,
fungi, and lichens. The proportional representation
of examples should not be taken as an accurate
reflection of actual discoveries among areas and plant groups, or of their significance to
science or land-management issues,
ASSUMFHON
I . I|.l
Ml, ,1 ill,
( . lo HI
I 1'
' p
IP
I HI
IN III
FILLY CATALOGED FLORA
The perception that the vascular plant flora of

North America has been fully explored and cataloged has a surpi in: i long history, as analyzed
from our current state of knowledge. As early as
1858, Thomas Bridges, an Englishman collecting
in California, wrote the following to Sir William J.
Hooker (quoted in Jepson, 1933):
The majority of statistics and examples that form

the basis of this paper are derived from the author's
personal expertise and vascular plant focus. The
resultant western North American bias should not,
1: Tut:
",',',;!,",",,','','
' " "J ,| ,'!', ,"
'f'.'n
,
' n-'nlmts I was par,,
,',. |.,|M,ur. c
um|,.r ,|,
Douglas. Hartweg, Jeffrey, Lobb and other travelers
tiany
III
111
I,a , II III I
II
jl
nil
III
till
.1
.
: i
tahlv U.S. \ews and World Report (Tangley, 1998) and Scirnrr \eus (\liliu-. IW<.
University and Jepson Herbaria, University of California, Berkeley, California 94720-2465, U.S.A.
87: 81-109. 200
As it happens, the "gleanings" left by Bridges's

predecessors comprised the majority of Califon i
flora as currently known. In fact, the number of
known species increased by one-fourth during the
in Cal loriua. have stood the test of lime lMc\augh.

1983).
A marvelous anecdote relayed by Heller (1908:
12-13) from one of his correspondents shows just
haw well < lis. ot|. .a| a a ~ ill. geiH a; 1., l|,-( that tile
North American flora had been fully cala >g.<l h\
the end of the 19th century:
subsequent two decades under the auspices ol tl

California I ".<-magical Survos, primarily due lo the
efforts of William H. Brewer and Henry Nicholas
Bolander. The two-part hot am. a] reporl o the I a]
ifomia Geological Survey (Brewer et al., 1876; Watson. 1880), which represented (he first coniprehou
ally or omithologi,
sive flora of California, included full entries for

approximately 3450 vascular plant taxa. This contrasts both with the initial estimate of 2000 (as noted in Whitney's introduction to the first volume)
and the latest tally of 7036 vascular plant taxa recognized as oceui' .
ultivation in California (Hickman, 1993). Not only were there only
half the number of taxa known in 1880 as in 1993,
respondence within the apparent overlap, primarily
due to misapplied names ;in. ion-p i _
ductioris.
As it happens, Bolander was himself guilty of
seriously underestimating what still lay i
lie found, ullin III challenged Uphotlso Wood'claim ol collecting 1 \lH) spe< ies of flowei ing plants
on a journey from San Diego up the coast and
through northern California in 1866. In an address
to the California Academy of Natural Sciences,
"Trofessoi Bolander con^ :;.'<! it probable that
there were not ov\< n i i - planiactually existing in lli.il part ->l California" (Leviton
& Aldrich, 1997: 87). On the contrary, well over
\, ! ton
these in the botany?' "No." Study (if the specimens and

consulting the botany followed on the teacher's part,
in the botany. They are not good for anything on that
I!
As a final example in the botanical lore, one of

i .a c's M |
- VI i i - I |,.ncs, is said to
have commented that "he felt sorry for all mi n<

generations of botanists becaus. In | !> i
1 I
named all the western American taxa. and there
would be nothing left for them to do" (S. Welsh,
pers. coram. 1998). To the contrary, the rate of discovers of rare pi. I-, u Jon. -'- fi HI . base >! I tali
uk in the 1980s
(Stone, 1998; Fig. 1).
- ieiica is over apparently has an inherent persistency to the point of
becoming a psychological phenomenon worth in_. in its own right. In the words of Stan
Welsh (pers. conim, l(>08). "Kadi major pul li< alioi
on western [ilanis ha- hit the mipiession th.i; all
divisions of California
[1993] by R. L. Moe, pers. coram. 1<>0;
,
how many of these Wood actually encountered is
admittedly another matter.
Bolander's attitude was in full sway several decades later, when Katharine Brandegee accused
Edward Lee Greene of conflating California's flora.
be discovered, that everything worth naming has

been named." The percept ioi s ol ific I * >t I > entun
lia\e accordingly become tlie dogma of the 20th
t < til in \. i uh aiii the .run on u Mil. a -land ing is thai
the flora of North America has, with the rare exception, been fully explored, cataloged, and
mapped (Reveal, 1991). At its worst, the attitude
that anyone describing rrew species of
plants from \oilh \mei a u.is u di.lgmg m spech ideation, rather
than practicing valid science.
Against this tide, there have admittedly been
mark, in that a respectable 70% of Greene's

of the botanical report of the
Volume 87, Number 1

Floristic Surprises
I ;.-<l::;,i ;i Si.r* c\ .A ( a donna. W.U-.oi ! I;'.o0| u

ilicah-il. "' I 'in i. siill remains ; i r n p 11 opportunity lo:
good bolam.al wi.ik at almost am lo. ality nm.'ii:
the mounlains. hills, and valleys of the State, to
which it is hoped that these volumes may prove
I toll: an ifirri :a,.- ami an aid." Via. 11 a summation
lecture of a syni|i 1la 1! ladonm I' -1
1
Classification, Lincoln Constance (19<>1) 1 < a
'\M;i!i\ otherwise informed p< rsons assume llial '!ie
California for the two decades from 1968 to 1986,

an average of 11 taxa per year. Taylor (p<a-., comm.
1998) has continued the analysis, dcrnoiistiulim'
dial die rale of discovery remains constant (Fig. 2).
exploratory phase of botany is essential!) complete;
plant taxa arc still waiting in the wings in (adifornia

alone (Fig. 3).
begins to taper off right now and follows the curve

displa\ed l\ more lulls cataloged parts <.| \ 1 n 111
America <c.g the nortlicasteni United States), a
(2) llartnuin Kelson (IWH)

<l) Shrrurf X Taylor >J<m7l
Possibly the first s
III I1 1 I i| engt to tilt < 0111-
that of Shevock and Taylor in

1987, provocatively titled "Plant exploration in
California: The front ier is still here." In it, the authors tallied 219 v scular plants describetl from
Furthermore, although California clearly lead

the pack, a recent publication by Hartman and VI
-..in il'"'.':; dcmonshales the p.a\asiveness of or
r. I n 1I I 1 I . 1 1 \orlh \meric;
For the two decades from 1975 through 1994,
total of 1197 vascular plant taxa were described a
100
80
60
o
40
20
1750
JgftM
1800
1850
1900
1950
2000
YEAR
. W. Taylor, unpuhlis
IICU 1(1 science, l-illlîllU. Iiolll 111. '!), .I\ f >|. p-IKTVi ::
formae and nothotaxa (collectively referred to as
"novelties"). The 603 full species comprise 3.21%
of the 18,781 currently estimated to occur in North
America (1998 estimate provided by Flora of North
America North of Mexico). The overwhcln n<, mi
jority are from the western and southeast mi I nited
States, but essentially all states and provinces conIribulrd lo the lotal (including a iorma limn Khode
bland, lindera benzoin f. rubra R. L. Champlin).
Most are angiosperms, but 78 pteridophyles and U
gymnosperms are represented.
Other statistics compiled by Hartman and Nel-
Number of holotypes by political unit (excluding

formae and nothotaxa). Top 10 = California (217),
I lah (183), Texas (70), Nevada (63), Arizona (57),
Oregon (42), New Mexico (41), Florida (38), Idaho
(33), and Wyoming (32).
Families with the greatest number of novelties
1
lop 10 = Asteraceae (186), Brassicaceae (91), Fabaceae (84),
Scrophulanaceae (46). Polvgonaceae (46), Poaceae
(44), Cactaceae (36), Liliaceae (30), Apiaceae (27),
and Lamiaceae (26).
Authors of novelties. Top 10 = S. L. Welsh (118),
R. C. Rollins (62), J. L. Reveal (45), R. C. Barneby

(32), G. L. Nesom (26), N. H. Holmgren (25), W
H. Wagner (24), B. L. Turner (23), S. Goodrich (19),
and B. Ertter (18).
Taking into considei
, thai novelties are subsequi K accepted as worthy of
Mailman and Nelson ac-
ated the acceptance rate in a vaworks, ranging from 63% to

98%, with somewhere around 90% apparently being the norm. This may in fact be an underestimation, if a recent study by Windham and Beilstein
(1998a, b) is any indication, ironically involving the
hv; leading authors ol novelties |eSt anyone assume that Welsh's impressive total (nearh liouble
that of Rollins's) results from a bad case of species
conflation, Windham and Beilstein give strong evI i
ial Welsh erred on the conservative side in
at least one instance. Not only did the elegant convergence of micromorphological, molecular, and
other evidence show that Welsh mistakenly lumped
some of Rollins's species of Draba (Brassicaceae),
but furthermore indicated thai Rollins himself had
confused taxa that were morphologically convergent
g 3000
I
jiooo
1800
1900
2000
Although it is impossible to know exactly how

much remains unknown, a calculation based on
Taylor's method of extrapolation has at least some
conceptual validity. If Taylor's extrapolation of
300+ still-to-be i -> ilar plant novelI .-- in i .i iloni i i- .K ii . irxi it the 1:6 ratio of
Calilnniia-to-North America novelties remains ion
stant, then at least 1800 more novelties can be expected for North America. If half are hrl-i edg d
species (as in Hartman and Nelson's analysis), then
nearly 5% of the North American vascular plant
flora is still undescribed!
/ >) \ou id . aid! , hints and fungi
COMMA
of endemic plant* of the (i.ilifornia region ami an
(fig. and caption prepared by I). W. Taylor). The *olid

throuuh piihlicaih.ii ol The Jepson Manual (Hickman,
1993). The data set includes those endemic taxa as recognized in Hickman (1993) or Skinner and I'avlick
(199 1). phis some IS! laxa found in the Oregon portion
of the California Floristic Province. 120 laxa found in
erra Vvada p..lti i
' i I!
le<l curve (dashed line) w as ohtamed In
i ai t -lunation mod. In
I n .1
with a cumulative h.gislh assumption
The assi
\. t id.l I he li|heat iv e nonlinII

M)
oi rune shape.
rican conifers (Taylo,
he-n doseiihed hereon I "< > I
;I1I
|9J 11 ?
1955, averaging nearK f><) pet voar.'I nc\ predicted,

will diminish once Flora of !\:nrth America Nor!!; of
Mexico (FNA) is completed. It is accordingly worth
noting that Taylor's statistics do not show a comj.aral.h .fop {> I., .u IML' 'II. if >[.< aiant < .4 /'/'/ Jenson Manual (Hickman, 1993); if anything, the appearance of an up-to-date flora has spurred
essi ntial fieldwork and increased the likelihood of
i. < ogni sing a novelty as such. There is at least one
<"> ilready that the appearance of a generic
treatment in FNA is independent of ong
.- die
coveries: Warren H. and Florence Wagner (1994;
pers. comm. 1998) report that they have already
a<-. nil dated M\ new species of Hon u'linun tic\..nd
the 30 included in their treatment for FNA (Wagner
& Wagner, 1993).
Comparable statistics have not previously been

published for non-vascular plants and fungi, but
I I '
i I! i
i
Stotler have comi raw numbers on mosses and
i< spcctivck. k IK making ihctn a\a laid.- Cot ll is
paper. From 1975 to 1998, a total of 63 mosses
were described from North America, including 12
sp< ies (M. Crosby, pers. comm. 1998). This
represents.''. I T'/e "ii (he 1 :323 s| iccics est! mat' I I ni
FNA, almost the same percentage as for vascular
plants (3.21%). Liverworts tell a similar story, with
19 novelties <|< -,
- 20 years, representing 3.44% of the current tally of 553 (R. Stotler, pers. comm. 1998).
from the Index Nominum Algarum, maintained by Paul Silva and Richard Moe
(pers. comm. 1999), indicate that at least 63 marine
macroalgae have been described from the North
American coastline since 1980, with an incomplHc
cataloging of pre-1986 publications. This clearly
indicates that algae are also still being actively discovered and identified, perhaps at even higher percentages than for vascular plants. Comparable sumntaries have not been generated lor lichens or fungi.
nrhii b m general Lag
> I i i
iscular plants in
terms of systematic research.
[Note. Although it is now well established that
lineages (green, red, and brown), and that fungi are
lated I
(e.g., the topic of a keynote symposium on "Phytogeny of Life" at the XVI International Botanical
Congress), there is no evidence thai tins, J mips
are being evicted from herbaria or the research
realm of botanists. I . n inclusion in this paper is
furthermore jusl
geoning move to
treat Imopln t< - ;t| ,\ | r|n n-. ami p >l ntia K :i;ugi
and algae, under the same conservation umbrella
-ii.-, id.ln-ss .1
I1 i- p
.1 i.lcvance to all.]
Although the statistics cited above are impreslikingb

e, ,1I1
.II1R1,
new
new
discoveries a.r
are lenns,,,.,,.,
represented.
.,,.,.,
compared In ciApticalb distinct variants of marginal significance. In aildress tins (|iieslion, a selection nf tin- miwl drainalic ol tin- newb discovered
and/or described taxa arc presented here, drawn
from among the 1197 novelties tallied by Hartman
and Nebon and numerous old. is published since
1994. Choosing among the wealth of riches was one
of the more challenging parts of preparing this pa. I'h 11 sultanl < lion es in org tni
iwitig categoi ir>:
d 1
< I) Monotypic genera

Five species covered by Hartman and Nelson
were distinctive enough to be described as n< w
monotypic genera: Apachena chincahuemis C. T.
Mason (Crossnsi.ni
m
W. H. Earle (Cactaceae) (subsequently included
within C.,ir\pliuiitli,i b\ Benson | 1 ')821). Dedeckera
eurekensis Reveal & J. T. Howell (Polygonaceae),
Shush,itira 1,uh in,ita K\ert & Constance (Apiaceae), and Yermo xanthocephalus Dorn (Asteraceae). Apaeheria and Cochisea are from \rizona.
Shoshonea and Yermo are from Wyoming, and Bedeckera is from California. Apachena. found in the
Chiricahua National Monument in 1973. became
the second genus assigned to the family Crossosoinatacea. (Mason. l()7.Yi )erma whosi closest
probable relatives grow in deciduous forests in
eastern North America, is known from a single remote population I
(! along a proposed pipeline
- in the Wyoming desert (Dorn, 1991). Shosh-
omies of downtown
Cody, Wyoming (Fvert & Constance. 1982; R. HartI9<>8). The distinctive summer; shrub Dedeckera was discovered by conMary DeDecker (Reveal &
son, 1994), with one population
3 of a scientific
Bishop. Califorlson's publica1 of vascular plants
both Brassifrom California. The first was Sihampsis
ttii S. Boyd & T S. Ross, with three separate
f doing an
ely well-hot-
if. rriiii I Boyd & Ross, 1997). The second was also
discovered by a consultant in an area pn>p..s. d !
d< .eh.am i !, .*. illin caisli ii .l lulcrsl.aic I lighwav
>r.
jn
^^
S;IM
Jo;
V;(||(n
(|||uma|K
s,
M,.|(M,
, .
. x ,
,
i
<>if bcin^ \el din in* > i < mil
u In. . i I irnpean ai m.al.
it was dclerniined instead to represent a unique
new species and was according described as
/</ sv .';,(,an,i . ./.''/-/';,'. ./ \i-""ln lil> 1/ ( \I-Hn liba/.
1999).
Looking beyond vascular plants, newly discovnew genera are particularly common amii- 1 ,1.
< H (lie U> -t . :oalg: e 1 |i .. alio.,, . eight were dis
iii'lur enoii.L 'i to : 1 !|i sci it.. i| as new genera:
'"M/ I. K. Lee, J. A. West &
llonntM I- 1mm ( ahti una. !',> ..<!.ami,i>it, > ,11ns,en
M. J. Wynne and Orculifilum denticnlatum S. C.
l.indstr. Irom \laska; Callnlarnla trijurcata C. \\.
S< Inn id
1 1
pom Searles from
North Carolina; Chlorojackia pachyclados R. Nielsen & J. A. Correa from Nov 1 So.
parnaldia oregonica Sheath, Whittick & K. M. Cole
from Oregon; and Verosphacela ebrachia E. C. Henry from Florida.
Among bryophytes, (hohrvnm ogalalense (',. I..
S. Merrill (Pottiaceae) was also recently discovered
and described as a iiionolvpic genus (Merrill.
1992). Although it was subsequently transferred to
I/,.. ,,,., , 1/
1"** - n- distinctiveness as a
species remains noteworthy. The new moss is furthermore remarkable in making its a|)pearance in
tin Creal I'l
1
wist relatively depauperale in both mosses and new discoveries in
general.
(2) Charismatic megaflora
The award for most publicity for a recent diseovery goes to the Shasta snow-wreath, \eriusia
clifionii Shevock, Ertter & D. W Taylor (Rosaceae),
whose serendipitous discovery in 1992 in northern
California made both The New York Times (2 Februarv l<><).,) ami the Frankfurter Allgemeine (30 December 1992) based on two aspects of particular
significance (Shevock et al., 1992). First, the Shasta
snow-wreath was the second species in a genus that
had previously been known as a single rare species
in the southern Appalachians, over a thousand
miles away. This disjunct distribution, indicative of
a Tertiary relict, was, however, less puzzling il an
the second aspect: namely, that this never-beforecollected shrub was locally co-dominant (with poison-oak) along a well-traveled highway, 25 miles
northeast of Bedding, California. Once a focused
Floristic Surprises
search was under taken. seveial additional pnpula

tions were readih I... at.-.I. cue adjacent to a developed can iî'.uiid. \ - , f irther attojiiaK. the
earrenfU know a rai g. lie-, largelv . -, ith i one ,->! i|
few areas (Redding quadrangle) whose vegetation
types were con < I.
M| -I
ml
n 11- i
(Weislander et al., 1939); nevertheless, Neviusia
was not among the abundant vouchers.
As an eastern example of "charismatic megaflora," a 5-7-m-tall n.sa
In1
-nil.
1
covered in Arkansas in 1970 and initially identified
as either a Crataegus or an Aronia, was subsequently desi nlie-I :i~ \h-s;)i!H.s fiux-vms I'lepp(Phipps, l(>(>0). As such, it was a surprising acd
tion to a previou I
n i > |.n
tn
kn
.
i h
from Europe, the medlar Mespilus gen:
I
Siiiiser: in : i-oz.vme -tud - supporled llie nielli
sion of the n. w specie- wi
i
al., 1991). Described as being "of exceptional
l>ea itv." rmh '-> udividuals aie known from a single 22-acre grove.
Another contender for most charismatic recent
discover) from eastern North America is the Kentucky lady's siip|
mlm kiense C. F.
lu-ed |( >>< lidacc .;.. among the tallest and showiest
species in a gt tn
rently known from several southeastern states, it
was not described until 1981, long after the author
had first encounli red it cultivated in a garden
(Reed, 1981). The most recently discovered population, in coastal Virginia in 1995, is only 150 km
as the crow flies from the center of Washington,
D.C. (Weldy et al., 1996).
(.'>) Botitnnnl "hot spots"
A jackpot of undescribed species is occasionally
ged terrain, which set the stage for an often |>cv\il
dering expression of island biogeography in a condn< tltal setting. In such area-, an uniisiia, -ubsliale
or isolated mounlainlop has the potential of harboring a unique suite ol endemic plants, and the
'list botarn-,! to re -eh ili site an re q a bonanza
of floristic surprises.
As it happens, my own career as a profess oua
taxoiiottii-i l LMII when i hid the jood loilune of
participating ii t| diseoverv ol one such botanical
treasure trove while >li I an umiergrad-aale. thanks
to a newly built gravel road in the early 1970s that
made Leslie Gulch in southeastern Oregon a two
hour drive b\ passengei < ai Iron Hoise, Idaho. The
Glad, Ivesia rhypara Ertter & Reveal, I

i ichardiae J. W. Grimes & Ertter, and Phacelia
lutea var. machenziorum J. W. Grimes & P. L. Packard (Grimes, 1984). Some of these species are so
dist n< Im dial tin i relationships i. main in. lear.
whereas variants of several other species might
prove to be taxonomically distinct upon further
in! 1 ad ii> ii I s lie Gulch turns out to be the
I
ode" for several other species that had
been known previously from only a handful of populations: Trifolium owyheense Gilkey, Astragalus
sterilis Barneby, and Eriogonum novonudum M.
Peck.
Alas, Leslie Gulch is now overshadowed by the
latest "hot spot," the Ketona Glades in Bibb County, Alabama. In 1992, a group of environmental
consultants undertaking a rare plant survey by canoe on the Little Cataba River came upon a caliindes.allied laxa: Spigelia gentianoides Chapman
ex A. DC. var. alabamensis K. Gould, Onosmodium
sp. nov., Erigeron strigosus var. nov., Dalea sp. nov.,
'
, <ris sp. nov., and Silphium sp.
nov. Ill addition. - veial stale- n cords lor Alabama
1994; Gould, 1996).

The rugged southern Sierra Nevada in California
tin* r n
' i single day on a remote marble ridge in 1996: Heterotheca monarchensis D. York, Semple & Shevock, Gilia yorkii
Shevock & A. G. Day, and a still-undescribed Eriogonum. The ridge also harbors the only known
California populations of three mosses (J. R. Shevock, pers. comm. 1998).
(4) In our backyards
Although the majority of new discoveries are encountered in relatively remote sites, a surprising
number appear around significant population centers, even those with major herbaria and a long
exploration. Among the more
dramatic of these "in our backyards" examples are
the following:
Morefield's leather-flower, Clematis morefieldii
Krai (Ranunculaceae), was discovered in 1982 by
a budding botanist who practiced by collecting
u iijin ash-flow tuffs of Leslie Gulch have thus far

Senecio ertterae T. M. Bark lev
Huntsville area. Morefield himself, inspired by this
earlv experience, went on lo become botanist lm

ill.." Nevada Naliu.il 1 let it;i-< Program
Not far from Las Vegas, Nevada, in the course
of a Holistic suivcv of Red Rook Canyon National
' . t>-*(>
The highly localized population, within sight of the
Las Vegas casinos, occurs on an edaphic island of
sandstone surrounded In limestone. The species is
distinctive enough that it might justifiabh he treated as a monotvpi L'OIUS (\rs
i\ Lean. \'!i>2)
Approximately 25 miles west of downtown Los
Angeles, California, a few miles north of the trends
community of Malibu in the Santa Moni<
Moun
tains, Baccharis malibuensis R. M. Beauch. &
Henr. (Asteraceae) was discovered in 1988 (Beaueliatnp vX I leimekson, lWlb. beauchnmp had earlier described another Baccharis, B. vanessae R. M.
Reaucli.. from the midst n| housing de\elopmeuts
ill central San Ma-go Counts ! li.-uucliuinp. 1'>};(>).
Only about si\ miles from one of the main herbaria in Utah, on cliffs behind some summer cabins, Violafranksmithii V II. Holmgren (Violaeeae)
was discovered in l^J'.O K a "moderi da\ natural
ist" who was monil >nug ili< re ;>l n - I <u nn In
1992). Dis1998).
A short distance outsidi oi Wemib Naiiona
I'ark. among ||u most-visited narks in the United
States, the slim -
Shevock & G. A. Allen (Liliaceae) wa
in 1996, bringing to three the number
io a: cud. mil /'.'/ \thnmium in the lower Sierra Nevada (Shevock & Allen, 1998). In addition to being
the only New World species of the genus with
scented llowois. /-.'. I,I\!I>H is intriguing in being a
candidal. !'i the E; M!sfi>nr:in, once reported to occur in Yosemite Valley (Brandegee, 1891), where
no representative- oft IK- genus arc current K known
(D. W. Taylor, pers. comm. 1998).
In spite of growing less than 10 miles from
i S
uia, in an extensive] v botanized county with a recently updated flora (Howell, 1970), Calochortus tiburonensis A. J.
Hill (Liliaceae) was not discovered until 1972. The
species is so distil
I
.
I
lenges ihc , urrenil\ ai c. |>ic<; mfragi n<ai. las- fi
panding p ipul ilmn . i nh is II id this species not

been not ced BOOI ,
might very well have become
extinct without ever having been recorded."
Nestled among the Lick Observatory complex

on Mount Hamilton, within easy reach of the University of California at Berkeley, the California
Academy of Sciences, and Stanford University,
ii.ihdtuni, ,!.>,:< >!''';..: Constance <\ Krllci ( \piaceae) was not described until 1996, too late to be
included in Hartman and Nelson's synopsis. Its loi. ih!!'. liv i vsil< if vvci .Ji i gra| ! er. % gel Hai < ock
(Constance & Ertter, 1996).
(5) Species-rich genera
Lomatium, with 10 n
listed in Hartman
I : ' ha> undergone extensive speeiation. resulting

a an ai cud mi c o! lughb localized cndeimc spe
oies thai an sill being discov <-red at a sleadv rate.
!
ilb
. . ins the largest
number of novelties (43) listed in Hartman and
Nelson, due in laigt (iail to Ine < lloi's .: Rupert
Rarnoln. \slKi^,ihis is a so worth highlighting for
illi. poleulia: me In anal v il ic oi 'he i ew ills, ov IT
of at least one Old World
responses (e.g., Chang et al., 1983; Kosuge < l a I..

'><).">) bunt iiu
liiisccnlv ipproaches a case of
wing fiction, in that the hypoth.
covery of a cure for cancer in the form of \.\trti^
alius, only in this case a North American species.
plays a key roh u I mane I I
n-tini i/ed n
noslicalioii of nal *vould happen .1 all laxoi omists
and their works suddenly disappeared (Isely, 1972).
Penstemon (S. >plm na< W hen U tu a. coriiiligK represent
v.ilued t-liliiioti- to th, CM-IUIL penstemon palette
lo> ri ck i ai ; tun: i i !; ic -!s|s. ;i| |, a~f lit the < \lenl
cation" (Hill, 1973: 104). The protologue furthermore noted, "Th

> , i
us|
i
that they can be brought into cultivation without
species . . . was discovered in such a bolanioalb

H -1
igg
i
I for a very careful look at au\ aieas that ate threatened In d. >< Iopuienl or other disturbance, espeeialh near ex-
" -I
- i '"I
R
n .
discovered and d.-scribed
:i> aim. i ' .1 l> >M<C,-..>M<, u
I
I il itions. In the In-even species have been
subsequent lo the l')o-l
the hih inioaninin !'','>>.->i.
Floristic Surprises
lins, 1993), nearly h

by Rollins himself
the book itself. As massive a compendium as this
was, three additional species were discovered almost 1-ffolC I'll" Plk v\.ls l||V /. ,'V-N'. /, Kolll'l- .HI.*
L pulchella Rollins from Montana (Rollins, 1995),
and L tuplashensis Rollins, K. A. Beck & Caplow
from the Hanford Nuclear Reservation in Washington (Rollins et al., 1995). A short two years later,
;i fourth species, L vicina J. L. Andersoi ..
I
& Rollins, was published, with the epithet chosen
in reference to the fact that the type locality was
behind the home of a neighbor of one of the coillColoi
sheep pasture (Anderson et al., 1997; J. Reveal,
pers. comra. 1998).
Arabis (Brassicaceae): The appearand- of Kol
I.ii-"- I ! ''''I . . ii | i -I i in il-- triggered the de- i | tion >i I -in
four new Arabis from Canada,
Alaska, and Greenland, as well as reports of numerous range extensions from the same region, all
in the same publication (Mulligan, 1995). This example is signifn i
. ng that the northern l.r,iu<:. - n< .il-.. -i.ll i." lloi 11 -ui|)ii-r-. ni
spite of their generally fewer numbers of species.
Farther south, Arabis hirschbergiae S. Boyd has recently been described from southern California, a
stone's throw from a major highway (Boyd, 1998).
All of these species are additions to the 17 novelties listed by Hartman and Nelson.
Eriogonum (Polygonaceae): With 38 entries in
Hartman and Nelson, Eriogonum has also proven
to be an ongoing source of novelties, with one new
species discovered on the Hanford Nuclear Reservation across the river from the new Lesquerella,
as part of the same botanical survey (Reveal et al.,
1995). An even more recent and dramatic example
is provided by a pair of Friends of the Jepson Herbarium weekend workshops on Eriogonum in California in the summer of 1997, taught by Eriogonum specialist James L. Reveal. Of the 35
|..iiin-i|.ant-. iii-i., ]_. i . I HI l, in ists and consultants, 3 ended up providing Reveal with additional
shouJ schedule a workshop on how to describe
new species! In addition, Reveal confirmed that the
variant of E. nudum Benth. that is the host plant
for a federally listed butterfly, the Lange's Metal
Mark (Apodemia mormo langei J. A. Comstock) is
ilscll ii uii |.--<-iili.-d t i II l)ii'iging up to three
i Dun
Ii ill
'. ni ' iiln
I 'i
.ii iplex on the edge
of the Sacramento River delta in central California,
less than an hour's drive from Berkeley; the other
two are Oenothera deltoides Torrey & Fremont
subsp. howellii (Munz) W. M. Klein and Erysimum
apii itum (Douglas) Greene var. anûslaliuh
(Greene) Rossbach, both federally endangered.)
Carex (Cypei
i
I hat
111
i
21 nov< mi - listed in Hartman
and Nelson, an average of 2 per year, are found in
eastern North America. Carex lutea LeBlond, for
example, was discovered in 1991 in North Carolina.
where it is a ran- i - n < I u.-t -a HI
i in
by limestone. It is furthernior ph l . <; interesting in being a southern outlier (by 750 km)
ol a mi iniilxireal -| les i omple\. possili \ a relict
lioiii tin Hei-toeelie. Associates ol' <". hlint include
numerous other rare species, including Venus flytrap and an urn I.
i
II
i I I.
I i I
1994).
Another recently described sedge, C. juniperong, Reznicek & Crins, is known from
A h !\ (lisjni.'i I ii.ij uhitioti- ni. I )i ::u n. i lliio. and
Kentucky Mthough locally a groundlayer dominant, it was presumably overlooked because the in(
florescence- are i
he I
appear unexpectedly early in the season. In the
I lotiiie. the authors noted, "The recent discovery of this distinctive new species in a supposedly
botanically well-known area suggests that even the
II.
i"
\oi
urn ia i- not as wellknown a- l- < oiiin id
i,| >- I ' (
lint;
I
1993).
(6) Scientifically significant discoveries
On top of the importance < 1 italogillg th< i m lponents of biodiversity for their own sake, many of
the recently described species have carried signif
\
, < liftonii and Carex lutea, pose interesting
biogeographic puzzles. Others, including Unla kcru
eurekensis and Calochortus tiburonensis, provide the
key to unraveling phylogenetic questions (Reveal
& Howell, 1976; Reveal, 1989a; Hill, 1973). Dedeckera is also significant as an ancient lineage
.have
F Keek's revision of Ivesia (Rosashockleyi S. Watson was thought

the Sierra Nevada of California
T/irii,)"!, ifir-* inltn ftiuni hutai. mil \ !!!<!!!i>n

s
istinct outlier in
i previously un-
lachiana Farrar & Mickel.

The liverwort genus Pelliu (Metzgeriales). perhaps second onb to Man Imnlin in the amount of
altentinu previously given to liverwort genera, nev-
vation analog on unusual edaphic sites (Ertter,

1989). The low-elevation complex consists of several closely related entities with widely disjunct
distributions: /. rhypara Ertter & Reveal var. rhypara, /. rhypara var. shellyi Ertter, and /. paniculata
T. W. Nelson & J. P. Nelson. This example of island
ertheless provides a case where a critical look at

the "common" species in the field yields unexpected results. Prior to 1981, only four species were
recognized worldwide; in relatively quick succession
> however, two new ones were published from
eastern North America (P. megaspora R. M. Schust.
'. ItpjHl'ilf llUI'lil I
biogeographv in a < oniuienlal setting is ml. tpieiec

of Pleistocene-driven isolation and
le lineage retreating to isolated
' and the other finding a compausual edaphic sites at lower elevations Molecular investigations with < mrislnpner
Baysdorfer (California State University at Hayward)
ultant evolutionary pattern.
Verrucaria tavaresiae R. L. Moe is noteworthy
lot only in being one of the few known marine lihens, but also the onlv lichen known with a brown
ertidal "zone" around San" Fânc^'Sliforma

(Moe, 1997).
Calycadenia hooveri G. D. Carr (Asteraceae),
deseribed in l''7.i. possesses a eiilomo-ome
rangement almost ! nti(,.,
f other species in the genus.
-: ctions of chromosomal
urn >s un i e >olu n is I on
.
molecular phylogenies of Calyvudema show that
the ancestor of both aneuploid species lineages
(which comprise tin bulk of the genus) had a chromosome arrangement similar or identical to that of
C. hooveri or C. villosa. Without C. hooveri, the reconstruction of chromosome evolution would have
been equivocal (Carr, 1975; Baldwin, 1993).
Probably the most surprising discovery involving Mortli \tneih an ferns has beet. lite reaiiz.it on
that several species of Hymenophyllaceae and \iltariaceae in the eastern United States exist primarily as gemmiferous gametop
north of the range of the sporophytes or, in a couple
of cases, with sporophytes produced rarely il ever
(Farrar, 1993a, b). Although vegetatively reproducing gametophytes have been known since 1888,
their relative abundance (10% of all fern species
worldwide) and significance has only become appreciated relatively recently (e.g., Farrar, 1974).
Once gnmetophvtes became the large! oi all. -til ion.
R
three new species were discovered in the early

1990s: Hymenophyllum ta\t<", te Fan u & Rain<
1991
])> and one more is currently being described
^rom Miss
' "
'
The
bryophyte Tahahia has been a puzzle since
its
discovery in 1951, at which time it was consid..Hcv
aiehegi.nial n alei al \\;\ - kmnMi. and alt. mpls l
ure
- Sporophytic plants of T. ceratophylla (Mitt.)
Grolle
were
finall
y encountered in 1990, in the
cour se of fieldwork in the Aleutian Islands
,
' ^
"1
' "
"'s i,,entity as a moSS <Smith &
'
son
99 !i In essence. Horisin <li>
-.idled in 'I lran-1. ; il i genu- bom one division
sl
(HePatoPMa)
to a
ther (Bryophyta)!
"> <>THKR KINDS <)K FI.ORISTIC SURPRISES

,
iiii"
i
J
.
.
.
.
. ,
!. ,
imagination, th.-v M'|.[.-s,til onb III. up ol the ice^ ^ ^ g
^
rf ^.^
.,
,
.
. c
.
.
.
i
i
i
the conipieli. N-I\< 11.l01tn.iH0M lL
that i- linK
I-ii
f<>r ^
difficuh ^.^ m a .(,(.n|l(l(,l|U ,.
formed mamu.y
y^n mun, om|)|(, tha m|r
b
knowledge of what species exist is our knowledge

()f where
they
o(.(.U].
w,i;)t
,,..
habUat
require.
ments are, and similar questions that can only be

answered by extensive fieldwork coupled with critical taxonomic analysis.
An excellent example of the incomplete and nonstatic nature ol Hoii-ai. inlorir.alioti i~ provided h\
tile recent 1\ ie\ 1-1 : il. r.( .! Mi>-oi;i . n vvlm b the
number of plants known to occur in a relatively
well-studied state (with one of the oldest and largest
herbaria in the country) has increased by nearly
12% since 1963, two-fifths of them native (Yatskievych, 1999). Current research on the flora of
Mount Ki.il.lo. ,u i-ol.iied m.mm.IIII and popular
state park situated 25 miles east of San Francisco.
lamatic increase.
In spite of the high quality of the original Holistic
i II it. iwerman, 1944), a recent updah (I'.ouei
liter, in press) has increased d
-,
taxa by 25%, approximately half of which are na-
Furthermore, several species in the 1944

iiK-ni haw been deleted oi replaced, as a res lit
isidentified vouchers ' * laitgei < m in>
On the other hand, locally occurring variants
Enogonum. h>,v
I
I
andfw/m
have the potenti. I i 1- m . i n ! - i ! , i
(Ertter & Schultheis, 1998).
Some of the main categories of "floristic surprists" ollii : than uovelt <> are the followmg:
by the direc
eomn: I <)<)}'.
^^J
|lM , ,,,
,
,
^ _
_
_
^
was slipped i
|,.,,, ,,,.,,,. <;|iristi: />,.
\\ I
In,MM |( n> phvll.i.
Nlllllh
f / j "Presumed e
Grants Progra
lus to gel a warm hoclv
cies is the rediscovery of species that had been

llioughl to be exlincl. \ recent exampli i:(\ibfor
nia is that of the Ventura Marsh milk-vetch, AsI'.i^.il'^
;>.< ;;<>sl,s, ': ,,,-,
Cray
'. a i
'./'.,>> ^ ". >
~ e\. lllllg as the icdlsl oyoiv of ^loh-
(Hv.lk) Manx (Kaha. acl. .Cm h was :e, . r111> (> u;d
^"IÎT
c\ti:ici lor W years Local newspaper coverage re
ferred to "A botatn< il < MI reel
" \ <
< ,
ty Star, 21 Aug. 1997) and "The Elvis Presley of
i
-ML
ii:s" ,'/>',
Hiiriuini \ew.s-Press, 15
Aug. 1997) The wildlife biologist who found the
. Kate Syrnonds, was quoted in o
gone that used to be aroun.
somethirij. thought l" be gone :li it i- h
ls hkr ;1 SV{
' " '''

' 'hance for the species
amento Bee, 15 Aug. 1997). Ironically, ** -i
toimei
.,l
h. Id
u.i-l.
dump. disp. II
notion that significant discoveries occur only

pristine habitats.
Coiiu identallv, another recently rediscover
Californian Astragalus, A. agnicidus Barneby, v
also associated with disturbance. In this case
y
,
. .
'
perceiyeil |n\i< itvJ to livestock (tigrn
\ , .. x
,
/ .
cidus = "lamb-killing") reappeared vvh i
iggii:-:
;
a
i
germination
seeds that had lain dormant for decades (Hiss
Pickart, 1992). This example also serves to ill,
trate the difficulty of determining presence yen.
-1r . .
Ii .1 --lit, h i
id. i,
.,
i IJ
.
'
! evident.
The systematic search for selected subsets of the
ll() plant-- and annua s thai arc considered [nib utially extinct in the United States was given a majoi
boost recently by the Canon Exploration Grant:
Program directed In The Nature Conservancy iSlolenbiug, I'"'1., \nori mous \**'K>
Ml mgl i deirig niaiori
.
en rel.
i
late.
there have been enough satisfying sr
v ids liee. considel ihe followu g slot
Inlo ll
species that? gi
.,1 h ,-, ,, iiraii. n: i
">atic for who knows In
species, but of potentially equal im-
pli-atinis for land management, is the rediscovery

of globally rare species that had been considered
regionally extinct (i.e., extirpated). Kxciteiin-nl on
the MCTKIOCIIIO National forest in (California has
around the l()9(> discovery of several popuiati((ns'ol'th;f(.1|t,;1|K ,,,,,,,,.,1 //,.//
A. Cray (Lobeliaceae), previously known from
brnia only on the basis ol a single fragment
cted in 1928 (Isle, 1997). Interpopulational
m tic studies are currently under wav to compare
h California planK u,th those in Washington, IdaF
*
ho. and Montana. In addition, another plai
had been thought extinct in California. <
sum pusillum Ral. (Ophioglossaoeae), was recently
located adiaeeril to one llowellia population (D.
Isle, pers. coram. 1998).
Even the reappearance of a not-so-rare species
6v
appeared can be newsworthy, a- evidenced In the

,
, ,,
,
. ,
attention given to a population of Mini
Linill. found on the outskirts ol Corvallis, Oregon
(Holden, 1999). Although this species remained
relatively common in the Central Valley of California, it had been assumed to be locally extinct in
Oregon. As with Astragalus agnicidiLs, the reapc \/il
I
A
1
in
pearance ot Mimuius tricolor after nearly 10 years
nonstrates how long a species can persist in the
:d bank, and accordingly how difficult it is to
(2) Distributional discoveries

More prosaic but gauung significance tin
sheer weight ol riuinh<i~ i- tin constant sire;
imlk a< < u t n u I < 11 < in the iinm ol f HI I .at ium specimens. A reeentk verified. < uriouslv ovei looked < \
ample ii. til-- ,|I'|S(I Herhaimm tJKI'Sl is a specimen of Luzula piperi (Coville) M. E. Jones
(,|unea< .-an northwestern ('alii in i.i ! l-'niuHc
349), over 600 km south of the nearest previously
reported occurrence in northwest Washington
(Hitchcock & Cronquist, 1973). A good example
1mm eastern North America is Sriiiznniii,i ^Lihrn
(E. P. Bickncll) |{.-|
i-. I
raccae), the only
'in,-. \ pop ilali.in I., si:.I iti ;*ifl . elambei n v. nv.-i
a sandstone cliff in southeastern Kentucky, is 250
km (mm die nearest of the previously known lo-tal plain of the
southeastern United States (D. D. Taylor, 1994).
More problematic is the recent discovery of Limi
uiceae) in a seasonally fallow field in west-central California (Buxton & Ornduff, 1998). Previously known only as a
rate cinlcmic .'I - -ul Ii. a-aVi i. \,m< m .1 l-i.nnl in
Canada, L. macounii was at one point
i
I
i. (Hi
k. ''ol). What is currently under
debate is whether this represents a surpnsitij. (lis
persal event, i p
i -I
i
i
la
i>.
(Iisjnnci III on idenci thai iddil ional populations
might
ris in i it irening sites (A. Ceska, pers.
comm. 1998). Ornduff (pers. comm. 1998) supports
tin dispersal h\ potliesis. citing tin r.v< is,- example
of Lasthenia minor (DC.) Ornduff (Asteraceae) being loinid in iM'illiw-i. in \\a-!iiiivl'ii. "Vi i 1000
lation in central ( i ii i
;Y,is
field in which th. f I,I.MI.i p..
et al., 1994). The

lation was found,
which was pi ok
i i
British Columbia population, was - il>-
K
plowed prior to planting cabbage (Buxton & Ornduff, 1998).
single species within North P
range extensions: specie;s previously kn own only

from Eurasia that arc determined to occm in North
America as well, not as introductions liui as natuins. William Weber (pers.
rally occurring . . t
comm. 1998) addressed I In- large number of Asiaue-Koi k\ Mountain Hi-ijunctions, many recently
located, with the commeiit: "J. D. Hooker was , er
tainly right when he was shocked to set: some of
his Asiatic things on his five days in the> Rockies
[in 1877]; sadly, Asa Gray evidently was on a va< ihoi./pi. MI. aid didn't recognize that tbere might
sineled to tin an In and aipuie regions, however.

but can also he
1
spent,sen- Irmii I. \a> and \t zona prev IOIISK eonfused with Dpi
n
/ Piaiill
(Ophioglossaceae) turned out to be cons per In H itfa
the vudes-pieud Old World species (). ;<<>t \pit vHuin
A. Br. (Zech et al., 1998). More recently, Eleocharis
H I i II
I has been determined to I., i al v< ,u,J w ii. sin. ad u; horeal North
\merica (S. (,. Smith i\ I'. Cregi i, n prc| . l''0;d,
noteworthy in vascular plants, they are more routine in hryophytes and lichens (B. Muni,, peis
comm. 1998). Even here, however, some examples
stand out in m d . (lend, sn, h ,b \^:% ,!;i old
< niitvhes. das lichen was unexpectedly encountered on an old retaining wall connected to the
building that houses the COLO herbarium in Boulder, Colorado (Weber, 1996). The account of the
discovery of this population amusingly addressed
the quandaiv et how le ol.iam a >;.-. enl specimen
tion of Facilities Management staff.
Conifers are perhaps the best-mapped group of
plants in North America (e.g., Little, 1971), being
holh conspicuous :iml economic ali\ significant.
Nevertheless, recent fieldwork by David Charlet
has determined that 43% (90) of the 207 coniferbearing mountain ranges in Nevada harbor at least
one more conih
12% (24) have had two to four species added to
til. knowi c Miipl. m.-nl I K I I I \pproacl ing ilu
i angle, : tl 22 s
ol conii'ei known io no in in Nevada, 14 OCCUr on
at least one mon
i
. thai i I n i
ously been reported, resulting in 15 new county
records in Nevada's 13 western-size counti. s |( iharlet, 1996, pers. comm. 1998).
On the Pa< it
I. on.i
i
i
shore banks that rise to within 30 m of the surface
are uveal lig a hitherto uiisllspei led and rcmai k
ahlv iiiiili'im ass, m|,| ,,,, ,,| uourid 10 species ..{
marine macroalgae (seaweeds), extending from Puget Sound to northern Baja California. Included in
th< as* mblage are noteworthy range extensions
such as Pleurophycus gardneri Setch. & D. A.
Saunders (Laminariales), before 1970 recorded
only as far south as Oregon but now known to be
dominant at depths of 40 m off the centra! < ia I dorma coast (Kjeldsen, 1972; P. Silva, pers. comm.
Volume 87, Number 1
rated during the Charlet
1998). Although the kelp is readily identifiable, the

existence of these southern popn hit Kins was not ap
- i
ints grow at depths that are
midisl irticd li\ ci oh iil -tiiir/s aid arc accord
ingly seldom cast ashore.
Probably the biggest distributional surprise in
fungi i- llx disco... r\ 'n A the ooccrr. nee ci ninslinHnns .ilifc. jr.urn ' in. il . n nj i1 -,(.<<]. s dn< i
sity below ground, as determined by molecular
analysis of hyphal fragment- in the soil, can be
completely independent (Gardes & Bruns, 1996).
As a result, detei
11
I I -in h mi i
 i ili i )> d
i < il i plants and bryophytes.
(3) Declines and invasions
VHM
receding ex imples involve
inges in the distributions themselves. On the one hand are signife.mlK ..I ni.i.i-iK'd ranges, in which historical occurrences documented by herbarium vouchers no
longer reflect current distributions. An example is
afforded In ffntirlia enncata Lindl. subsp. >>/"<
"
I. II Krcl
ae), in which a
significant portion of lite hislnr cal \ documented
range has disappeared under Greater Los Angeles
(Enter, 1995). This kind of distributional attrition
I. - .|.\i<.u- ...ii- i\ noii iriipll itions, but is ex-
emely difficult to become cognizant of, sucl

is theoretically possible for a species to go e
efore its endangered status has even been n
On the flip side, and often contributing t
ecline of native species, is the spread of sp
ito areas where they did not historically occui
i. The sheer numbers ol ncvvK reported noncan be mind-boggling, though it is difficult

mine which are new occurrences and which
mply been overlooked, given that naturalecies are historically undercollected. Vind Cusick (1998) documented 70 additions
)hio flora, and also emphasized the fact that
' ..: flora- is d_\naiii c. .* lii
rishing, and occasionally
i |
nig I \. u in tin n gion around tin I nil. d
States' national capital, which has been rather sys(>(X)s, recent surp] it re< i Is a M
I
n I iding two native
Carex), five of which came from the grounds of the
Agriculture Research Center in Beltsville (J. Reveal, pers. comm. 1998).
In California, over 70 non-native species are currently known to have become naturalized hevond
i"-e included
- '
1/ muni (Hickman,
1993; F. Hrusa, pers. comm. 1998). As dramatic
evidence of how difficult sucli new occurrences arc

ld keep ahreasl of. at least I') occur within an
hour's drive of tin building in which Tin
Manual was edited. Five are even fully naturalized
in die Berkeley campus natural areas {Geranium
rotundifolium L., Geranium lucidum L., Geranium
puipiin-iiin \\\\ <t
I
in!
Hedera helix L. sulisp. ranariensis (Willd.) Cout.),
and at least three others have already achieved significant pest status in local parklands {Dittrichia
graveolens (L.) W. Creuter, Limnohium laevigatum
Willd., and Maytenus boaria Molina). The dynamic
nature of California's non-native flora, as well as
the difficult) ol ol
..11
jmanek and Randall (1994).

F. win NOT F()l ND UFFOKF?
The preceding examples should serve to empha
size that the era of significant floristic discoveries
in North America north of Mexico is far from over,
despite perceptions extending back to the mid-19th
century. Even the initial cataloging of novelties is
incomplete, to the extent that conspicuous shrubs
ah.no highways are still being discovered and described as distinctive new species. The comprehensive mapping of known species, including newly
invasive pest plants, is equally erratic, at a time
when such information i- son l> ..< , del to make
sound science-based land-management decisions.
The inevitable question arises as to why so much
ol our Holistic heritage a - remained unexplored,
II cataloged, and unmapped. The principal iiisv,, i
is relativeK -ti i hil
i
big job! As a result, and as mam ol lln p;.-. mils examples I.-,] I-,.
a primary factoi
mli bull IL I > < n.
Il< i-i
disc,,\. ries is the number ol people who are acli\el\ scoiuinu ih Held l-'i ri iialek. ih - i- |.\ i o
means limited to professional scientists in academ-
of "Icscnplm" science, .ire mil intiiusicalK scientific, at least as contrasted to the more overtly
> \
mi n I
i
IT.i
mptinii has direetly influenced hiring, funding, and promotional decisions, which in turn determines research priorities. Although die lull structure of m\ arguuient is
i ,ii tin seopi ol tin currenl paper, I will nevertheless posit that science is most defunleK involved in all aspects of taxonomy and floristics,
complete with the full panoply of falsifiable hypotheses and scientific methodology, even when
theSe are not explicitly expressed.
|>|SCR1I>TIYF IIYI'OTIIFSFS
The assumplion dial ...MI zing and "describing" novelties is a simple descriptive process reflects an outdated understanding of biodiversity as
consisting of discrete, pre-Darwinian quanta, lackig significant internal \ariation and separated from
Qne another by inviolate boundaries (Enter, 1997a).
This was noted by Constance (1971: 22) over a
quarter-century ago: "Although the doctrine of
Special Creation' of species has lacked any scientific status for a hundred years, many people
sr(.m stiU to be linking in terms of a finite number
of {)\,)vv^ (.n.aU,d once and for all, and which merely have to be recognized, described, and named."
Much of the confusion has a sernantic underpinn[n^ m that "describing" a species is by no means
equivalent to "describing" a concrete individual
can be ex anf,
ed
into the
complex hypothesis:
ie institutions, but instead depends heavilv on the

collective efforts of agency biologists, environmen1995; Yatskievych, 1999). Representatives of this
diverse group are highlighted in a later section of
i ,
I l''',H''
However, the number ol people actively searchmg is onl\ one aspect ol ilonsli. discoveries. The
remaining portion ol this papci accordingly addresses other assumptions that have influenced the
cataloging of North American plants, both histori< ally and currently.
coded as species-set Alpha beta. As hold support for

a,1<1
corollary of this hypothesis, all members of speciessel Alpha hrl
til
|
I i< , i
attributes X. V. and /. whereas all members of other
Species-sets in genus-set Alpha arc hypothesized to lack
mis combination of biological attributes."
Furthermore, not only are species and their circumscriplioris best understood as complex hypotheses, but so also are such seemingly "factual" statements as "Leaves (2.4)3-5(6.1) cm long," which is
Floristic Surprises
i long but
the 3-5 cm range.'
In both eases, the first phrase is oh
less ciimh. rsmth I i I
|
led vc rsion mon
clearly expresses the fact that nested hypotheses
uibsequ. rit
_. ivolved, all of which
testing HIM! i:'.<!|;!|. alien v
,\ collections of
lifie;)lioii of ;ui indiv nlu.tl specimen

!o leflecl ill.- i nmplesities ci sc!-assi;
"The specimen in hand possesses
biolog e.il ,1'ributc- thai el aracl. ' f/
the set Alpha beta."
pie and straight

n.
las
-i >
'fliers h in'. i;i\rn on i. e, mpon< tit- can lie a significant intellectual challenge. As a result,
ahlmlJuh
ITil mt l\
di-linel species are slill
being
encountered, the majority of recently described

novelties are determined to be such oidy after an
extended and detailed comparison with other species, often requiring a wholesale re-thinking onent of natural diversity" that falls within "the biological parameters of the current species concept," based on
some vet-ioTe detent ineil
suite nl diagnostic l.i-
An excellent example is provided by Potendlla

r<>r, /: ,", I
in i
l!> -
n u I i< h i HI ti(lt
. ol
lections had accumulated and been > arnuisb identified as (= assig i I l

p
- > i i '
icea Rydb., P. pensylvanica L., or P. breweri S.
1
i '
i
b\urns nature of
it an undescribed spefrom the fact that an
the actual range

between initial collection and date of pu
in that the earliest collection is not always chosen
as holotype. Monardella beneolens Shevock, Ertter
& fokerst (Lan i
i ). for example, was typified
on a 1986 collection (Shevock, Bartel & York
11727), but included among the paratypes was an
1896 collection (Purpus 1866) that had languished
i
i i
i
i
I . -[> i< - i ilder for nearly a
century (Shevock et al., 1989). This example also
illustrates that the distinction between a novelty
based on a new discovery and one resulting from a
novel i i ill- sis i I
sting specimens is not always
clear-cut, in thai tin . . III. . Mori ,.| an nn l< - rib. !
Mo
!
on
1986 "Inter-Ina itutional Haybaling 1
i
red the herbarium
search that uncovered the older specimen.
Nor does the proposing, testing, and rejection of
! hypotheses end once new species are defied
era, but with widely overlapping ranges and similar

habitat requirements" (Cronquist, 1977: 64). As it
turned out, my doctoral work not only pro\ ided support for all of lb
- ...
sized species except one, but gave evidence of three additional novelties (Ertter, 1986). Although I enjoy the notoriety
that comes with being able to say that I proved Art
Cronquist wrong and got him to admit it, I will also
submit that his was a perfectly legitimate hypothesis based on the information available to him at
failed to uncover the novelt) (Johnston, 1980). The

species
is a. Ii.-ili
priate diagm -h.
put.
Mn
i. on. c the appro-
afti bai.-s are h ujihghled.
In fact, it is more the norm than the exception

for the first few collections of a species to be shoehorned into existing species-sets, generally with
modifications to the "biological attributes" hvpolh
eses. Shevock and Tavlor ( I(>o7i. lea example, not
121 i
. hetw
ed i
anum specimen
f California novelties, with an average of 11
in even greater span is noted by Hai
on (1998), with the oldest holotype .
dividual identities depend on the larger context

As a result, the binomial Juncus kelloggii Engelm.
codes for three very different entities, depending
on whether it is in the context of Hermann's, Cronquist's, or Ertter's model. In this example, sufficient evidence has been accumulated to support
. A contrasting example is pre1, a partial list of corresponding
nomically challenging genus Po-
Holmgren (1997). II I
tilla pensylvanica
i.
> ,
\ .. .
,, i | s,,, ,k
il.li.h. .1 |')r,
Potentilla pensylv;
|.l,rdeL-n,.mrd|
[to be determined!
-elliformis
standards, of taxonomists not being able to "get

their acts together," but is rather a reflection of
four equally valid models for which insufficient
evidence currently exists to strongly support one
over the others.
An even larger-scale example of a floristic model
is provided by the numerous differences between
Potei
Iffi
list of California taxa as summarized in The Jepson Manual (Hickman, 1993)

and the contemporaneous Inventory of Rare and
Endangered Plants of California (Skinner & Pavlik,
1994). As analyzed by Skinner and Ertter (1993),
the differences result not from one or the other being intrinsically "wrong," but from legitimate philosophical differences in the rationales behind the
two publications. The goal of the Manual was to
maximize the likelihood of unequivocal identification, while that of the Inventory was to highlight
Volume 87, Number 1

2000
Ertter
Floristic Surprises
units fp,atdive.i.ylhalmerited _
collectors accordingly rely on the network of taxonomie specialists, who in lorn rel\ on tile analytical
resources represented in herbaria and liolaniral 1
lii'arii s. as vseli as . stabhslied and iniiovali'.i : chnnlogies. These resources, along with tla cii-,|odi
anship and transmission of the extensive legacy of
taxonomic *novvledg< . skills, ana ) hniqiK V. have
traditionally fallen within the domain of plant taxonomy in an aead< n i< -i 11 i r. in< i idim n - m I
museums and botanical gardens.
attention. These different goals resulted in different

models; in those situations where there was legitiii for alternate taxonomic hypotl - - I
Manual tended to lump vvh< re tin ftirrntar\ tend* d
lo split, so as to avoid "lamentation over taxa that
are shown to be distinct only after their disappear
ance" (Skinner & Ertter, 1993: 27).
D. NOVELTIES IN WAITING
\i
1 eless. even within an Inn-tit
model emplinsi/ir.g (!: smallest ded nsiba- mats as
for scientifically legitimate, peer-reviewed publication of novelties
,11
proposed taxonomic hypothesis. For example, the
Draba study by Wit Ih in tnd Heilstcin ! 1 ()()'<
)
discussed in an earlier section, clearly demonstrates how sophisticated an analysis is often required even foi th<
gm
i
Iv
distinct species. In
,
>
ic
highlighted novelties pro\e that radically (iifferenl
result, ferreting out the remainder will require not

only continued exploration, but also increasingly
rigorous scientific analysis.
Because of this, there currently exists an unknown number (50? 200? 500?) of potential novcities from North Vm< ri-ilul
u '
h
'
'</.
''
'
.
\i
Lomatium, and
in fact have as a rule of thumb that any complex
group that has not been intensively monographed
recently is likely to harbor undesenbed novelties.
However, all of these possibilities an
sibilities, and will require a signific
ol resear. a fiorl ;n d< ! r 11 a A' Im \ arc i g..roiisl_v
-u port
, a .i in
i |i. dieses. In other
r for many r
. .
.
.
.
.
.
liell
I>. > n >
i i m
I ot riot, hill tll<
existence of persons with sufficient expertise.

tivation, and time to undertake the necessary
entific analysis.
To ?<-. apilulare. ahhoiinh the initial di-co\er\ ol

novelties does nol rc(|uirc professional Iraining, ihe
analysis of potential novelties is another matter, in
which scientific expertise plays a crucial role. Most
97
A. THE ROLE OF REGIONAL FACULTY

Although university-based faculty are only one
category of pi
lise (\ersus, for exI

i
iff and museum-based professionals), they are highlighted here on the grounds
I
I
~-i led to provide the
ha k....
. ,
, ,
, nomic analysis described in the previous section, especially faculty
at those universities with large herbaria that occur
in the regions where most novelties are being disco\eicd I a 'las , -out. vl. it is 11 luminal ing to nnalv /e
id Nelson (1998): "Individuals who authored six
' more novelties < i North \mciicau ;; aril- d umg
the past two decades," according to the categories
in Table 2. Of the 56 individuals listed, the two
largest categories, both in number of individuals
and number of novelties, are "Kmeritus (or nearly
so)" and "Deceased." Together, the two categories
account for 60% of the novelties described from
1975 through 1994. In contrast, faculty who are
currently mid-career account for only 6% of the
novelties.
To pursue the specific question of novelty description by regionally based faculty further, I
polled plant systematists at universities who
match. I
lh<
1 lowing criteria:
(1) Located in the contiguous western United
States (Arizona, California, Colorado, Idaho,
Montana, Nevada, New Mexico, Oregon, Texas,
Utah, Washington, Wyoming), a region with a
high rate of ongoing c
(2) l.ocatct
universitv
liege with an her,
.
,
nnnnn
barium of ai l> I-I Jn noil -|. n ,- i, i
senting the equivalent of a fully equipped laboratory for doing taxonomic research on the
local flora.
(3) Self-defined as vascular plant system ai si (vei
sus ecologist, plant population geneticist, etc.)
OR serving as .J i < lor/, iralor of th
, al
mental herbarium.
i fl Department-based (versus adjunct) fncullv ap
uthors describing fewer tl
ico from 197a through IW4." The first column gives the to
column is the sum total ol novelties des< rrhed h\ these n
included in the tally, nor are novelties described b\ 'lie-e n
The specific question addressed was whether

. i. I r.-sp .inl. i - li i.l des< iibcil .1) zero, (b) one, or
d ) more lb.HI i;ii'- vas.adat |.l;mi riovltv from - in
where within die contiguous western i idled Sml. s,
The numbei of responses to this survey was gratify li-. I.ui the colhite.l results ( laid. d| ;in dmugl :
provoking. Of the 56 persons included in die survey, over half had not described a single no\elt\
region, an.I o\ r half of the remainder had
scribed a single
eltj (o,
i). In several
this solitary western
tun clu was- described dui ing die course of graduate
work inil (L<-; since attaining, facullv stal i- On v 10
qualifying faculty members in the entu. region
have il.-s- ribed mon dian one novelty from the region, and several of these persons are within a
handspan of years from retiring.
Furthermore, of the 48 western universities wild
significant herbaria, 5 eiuicnlK lack faciilh level
vaseulai I'lanl -yslemalisls. including '2 diat Irons,
tile largest herbaria loi l!l I respective slates (I diversity of Montana. Missoula: I'niv eisil v of (Nevada.
Reno). In Oregon, the two primary herbaria were
recently combined. Imiiualiug llie position ot I'laui
svsteiiialist at die I uiyerstlv of ( Ip-goi . b igerie.
One state (Colorado! eurrci tl\ lacks a faculty-level
plant systematist who has published
from lb.' rem..n, whd. ioui edicts ; '
Monlaua. Nevada. W'asliinglonl . an claim
i described a
described from 1975 through 1994,

per year, with no evidence of tapering
an cK Vlson, 1998).
The purpose of this survey was not to call into

; ic-tiet, the scientific productivity of the responl. ids. who ace all acliveb (luisiiiug a eouitneiidable
diversity of significant research in plant systemati. s. including d< M-I bu : au\.-lln - lean ottiei parts
of the world. Nor is it intended to slight the signi!'
icant contributions of individuals outside the admittedly narrow survey criteria, profess i
nd
otherwise. The survey does, however, undermine
am assumption dial faeu Iv I. .el plant systematise
at the best-equipped w sien UMIK isiii. > comprise
jor | col of expertise in ongoing
I HI- to
uoveltv-rich regional flora.
Moreover, there is evidence that this is not a
statistical curiosity, but rather an indication that the
current academic infrastructure actually d
mi
agi s such rain, p.c on. S.-v< ra r< spoud.-nls ind
aled li.l they knew of undescribed regional novelties, but could tint justify the research time and
I required to publish the
i respond, nt, "the value of
isfaction of university
- that could be generated in
Volume 87, Number 1
Table 3. Participation of un iitwiscul |l it *stcmatisl !a< il in l!i eonligiioii

ml liled Stairs in the
description of regional im- III llm , imp !,l In-ddaiaM '
I i-<! miml i ol universities or colleges in each
state with significant herbaria (defined here as at least 20,000 specimens). Column 2 is the number of department3, 4, and 5 are the number of persons in column 2 who have described, respectively, (a) zero, (b) one, or (c) more than
one \asrnlai plant novelty from anywhere within hi contig
m Unite* States, including novelties in press.
Percent representation n n li
i i
I. H
>j\en in parenthesis after summary totals. Column 6 is the total
number of novelties from each state published 1975 to 1994, tallied in table 8 of Hartman and Nelson (1998).
period of time." In effect,

gional novelties is not only
tually counterproductive to
the current acadei
i
the fact that the amount of
the publication of reof little value, it is accareer development in

,
I'ai.nl-M illy.
time and effort it takes
to publish a noveltv < i I. i

I. i
I
nee*!
ed for other resean
h
.i .(self provides
evidence that describing novelties is not the trivial
activity it is routinely perceived to be.
I find it illuminating to compare the preceding
quote with another, from nearly a half century ago:
"If taxonomy and taxonomists are to regain some of
their lost prestigeand they have lost a great
dealit seems obvious that mastery of a local flora,
an ability to recognize characteristic members of
the more common plant families, a familiarity with
the rules of nomenclature, and the capacity to write
descriptions are bound to prove woefully inadequate" (Constance, 1951: 229). We have apparently
come full circle, where the skills that were once
the sine qua non of a practicing taxonomist have
apparently gone ln>
ii
ite" to being
irrelevant. Or, at best, these former skills are assumed to come as part of the "systematist package," overlooking the tenet otherwise well known
to biologists that "you get what you select for." Admittedly, the above analysis is only a single slice
in IK. In i il n
rtli less strongl sn i sis i lat
tht
gic
ing selected for within academia, and as a consequence are de facto being selected against,
<;. \\ no is
IH>I\<;
Tilt; WORK?
The question then arises: If not faculty-level systematists at the best-equipped regional universities,
who is responsi
I
g the 41 novelties
per year in the contiguous western United States?
Obviously there are numerous people who are discovering and describing western novelties other
than those targeted here, who I have neither surveyed nor otherwise statistically analyzed. The major categories, however, would include the following: emeriti plant systematists; museum-based
plant systematists, often with adjunct appointments
at nearby universities; faculty-level plant systematists at less well-equipped regional university and
colleges (i.e., with herbaria having less than 20.000
specimens ,
utside of the region;
non-faculty research and curatorial appointments;
non-systematists (e.g., ecologists, population geneticists); government agency biologists; biologists
working for the private sector, mostly as environmental consultants; and amateur enthusiasts,
Certainly the academic and museum-based cat-
egories play signifii ml ,!, -. which sh >u! ! i oi |>.

td( r<
d<'il. What I wish to draw attention to
at this point, however, is the high degree of participation by professionals and amateurs outside of
academia, many of whom have an exceptional eye
fer novelties and a serious commitment to floristic
undertakings. As representative examples, some of
the more out standi r
i.
I.:. I Mow:
(1) Government agency biologists
Beginning with his stint in 1979 e
1
C
M
I .
/ l-i
I
I.
Ihe %-.|ii.)iii National hnreM I lilormn I nn - l{.
" '
' l(
' '
' "
""' !
moss named in his honor, 12 others that he has
authored, and several undescribed novelties in various stages of publication. Many of his earlier novelties were encoutili red !> In- I < mjj I hi in- l>o|
anist each year on newly constructed portions of
the Pacific Crest trail, which ended up bisecting a
population of Allium shevockii VfcNeal thai is still
one of the only populations known. While n i i ning
a focus on the
kl*** " l" "'
"**'""
IIJIKN , <xpance o
Lewinsky-Haapasaari & D. II. Nonis (()
lliolnclia.-eac; being the most recent add tmi to his
|>o'i iii oi - i ill
III prolol >i> u credits Shevock
"opening the eyes of the junior
I
i,ii
/
brvopli\|e iiches
ol the southern >ierra. a sigiufiid-en
- i
considering Morris's extensive
expertise with the California brvoilora (Lew nsk\
P NT
,,W1,>, .'I
I
llaapasaan t\ Morns. rJ<)8) Shevock s agenev r:i,,,
, ,
i.
i '>
. .
'
I
I
he prepared
plants for the Sierra Nevada Ecosystem Project
(Shevock, 1996), and he has recently moved
Associate Regional Director of the National
Park Service. Shevock's botanical explorations are
accordingly now confined lo weekends and vacations, but have not noticeably slowed as a result.
On a 1996 foray (a.k.a. "death march") to an isolated marble ridge, he and protege Dana York (botanist for Death Valley National Park) discovered
three novelties in a single day: Heterotheca monarchensis D. A. York, Shevock & Semple, Gilia yorkii Shevock & A. G. Day, and a still-undescribed
Eriogonum.
(2) Environmental i-i^hii'ints
of James D. Jokersl. who
I to retrieve the family canoe,
of one of the persons who did
environmental consulting into
for skillful, well-trained bota-
u -is "A hile , I- i^ f'i III

! i the emironmental consult
I u & - '- - Associates. Jokerst nevertheless found time to develop expertise in
the Lamiaceae, preparing treatments of several genera in The ./>',' " 1/ i " ; (Hickman, 1993), ineluding the notoriously difficult Monardella (Magney, 1996). He also authored or coauthored three
novelties: Acanthomintha obovata subsp. cordata
Jokerst, Monardella beneolens Shevock, Ertter &
I iu ' l'< : >i < II > > nda Jokerst. While
doing a botanical survey in 1985, Jokei
Ill lI'.U. 1< .1
'
ILL
/,,
.o
poslhiunoush iiaiiici! m I i- fionoi iXmooiit I\M
Vlor,\ /
x/
1m, ' *
gan, 1998).
According
to ,r
1998), the clover "was found i
Heller had collected at sevei
in general are playing

cities, as the person-, rtiosi hkeh lo have access to
poorly botanized areas. As prime examples, the discoveries of }erni,<
'
'
",,
lahlmi;.. .i m: V <-,, ,i'.,i,:. w, t.- i oi n< led
^ environmental survey efforts. Unfortunately, a
great many In ilk
i
il nits lack the training
recognize potential noveld may in fact be discouraged from taking
mechanically g
"'
iar<
'
r
}
. l>'
.
.
. [
' " n site. Ihis pra. lice is hased .,n ihe d,w! pre\ ionsK
,
, ... .
is ,
,, , l|
, ||k, I OC.
..
., .
.
..
at issiai [:.11 a! DC.A- w ilh :lie (heme ol
l!""-!"' sin-prises.
\s ~uniii.an/.ed by S. Boyd
(pers. comm. 1998), discoverer of Sibaropsis
velties in the course of doing
'""
. ,
ktlOwll .,
'
(l
ni'f'cnce.
surve s
y -Tnere is the strong possibil

gems arc heing overlooked hy
times under-trained, botanical c
ci.-s. It
0v<
dci
loc
(3) /
Among the more unexpect* i
I th< un ' ui nthusiasts is Lowell Ahart (Geary, 1978), a sheep
rancher who started out cataloging the plants of his
ranch and has since moved on to county floras, eollaborating with retired zoology professor Vern Oswald (e.g., Oswald & Ahart, 1994). Two plants from
his ranch have been named after him (Juncus leio-
spermus var. ah art 11 \ . .

>'
>
i
ter), and an Eriogonum is also being named in his
honor (J. Reveal, pers. comm. 1997). When Ahart
mlii the amies
/ to my attention, begging that someone provide a name for it so
he could complete the checklist of his ranch, it had
actually been known for some years but had been
assumed to represent yet one more introduced Eurasian annual. However, by then a worldwide monograph of the Paronychiinae was available (Chaudhri, 1968), making it evident that an anomalous
undescribed species was involved, whose affinities
al < -ill unclear (Ertter, 1985).
(4) Other para-academics
. ,.
.
,,i
V final
impl< - e\perlis MIISKI. ,f
n| in
..
. V
, '
.... .
,
.
is nroviden b\ Arnold (.km i Liehni. who lias ;u
e<l <li :! in I-..' H -, ii <J of. mis profes'irr
-ri *ii. en
(e.jj
i it. i
-l n it Ihe New
t
1 T
A \ F
Villast several
.1
York Botanical
Garden).
For the
however. Ti< Inn lias earned his living a.- nell r
tain and limousine driver at the Peppenni] (lasin
in Reno, Nevada, doing his botanizing on his days
off. At lasl eonnl he has nevertheless rtia-h the !\pe
collections of 19 species (Holmgren, 1998), approximately one per year, several of which are
. Probably the most significant is
L D ii.u
i
M
I
c
Stroganowia
tiehmu Rollins, the single North
i representative of i
fined to central Asia (Rollins, 1982). It also qualifies as another "in our backyards" discovery, not
encountered until 1980 even though occurring onlj
l few miles IT a well-lnneled liighwa
ininles
&
3 -_0
D IS THE POOI SUFFICIENT?

These highlighted individuals are only a sampling from a large ...
i I md dedicated
individuals operating outside of an academic setting, including some who not only discover but analyze and describe their own novelties. When these
para-academies ate - i 11>i d
- i m
n
d
systematists, faculty at smaller institutions, and
non-facultv lesean i -i I
i muhl
Ii
argued that the e\i- n-_ |

Hi-e i- -ufh
cient, and that faculty systematists at the larger
universities should appropriately be encouraged to
address avenues of i - rch tnat
nnot I handled
by others.
While confirming my enthusiastic support for a
diversitv of individual research interests w lliin ;ieademia, and likewise for the active participation of
individuals outside of the academic mainstream. I
will nevertheless argue (as have others, such as
kn
berg, 1997) that a core of professional plant
systematists will continue to play an indispensable
role in the task of discovering, analyzing, and de
scribing the remaining unknown element in th<
North American flora, as well as critically evalu
ating new information accumulated about previous
ly described species. In other words, rather thar
being made redundant by the para-academic net
work, an active core of professional systematists i>
integral to the proper functioning of the network
Furthermore, a significant percentage of this professional core needs to be housed at the large regional herbaria, especially in the West and Southeast where the majority of floristic discovery is
occurring.
I n< oin ions argument lor aradei ,, p,-,rlieip,ii ion
., , f
.
/
.\ .
.-. ol C.IIIIV. u- i>ro\ nie t!i. lonna <\ -iemal i. -tain
'
.
. ,
. . .
chldll .
. - ,
,
-,,
-.
sultai
more i
reality that regionally based professional systematists represent the essential source of quality con-
-academies who anaK/.e and describe their own novelties

general 1\ do so only after a period of "apprentice*hip" with
.
regionally based, practicing

&
..
.
:gard, it is unsettling to r
many of the regional professionals who provided
early encouragement and training to the current
crop of active para-academics are now retired or
ed. A prime example
.', _.
\.
.*! ,..
A J
r
John Thomas Howell of the California Academy of
Science^, win
I
.
ml encouragement
t0 m St
f the individuals highlighted above.
Howell also represents the category of museumbased research staff that is becoming increasingly
important in maintaining the role of the professional core. As significant as this contribution is. however, museums and botanical gardens are too few
in number to provide complete regional coverage,
and are also less likely to be involved in formal
training. At the same time, the suggestion that deMiipti\< -\ -t.-m. it n - should be relegated to smaller
imm IMIICS and colleges runs counter to the fact
that the major herbaria are generally at the larger
universities. The continued participation by major
regional universities is therefore essential to the ongoing task of discovering and analyzing the regional
flora. If this task is m fact incompatible with acadeir.ic realiii> ei n. afil, l.i. mg laei ll-. (and not just a matter of erroneous percep
then it is imperative that alternate ways to t
such participation be investigated, perhaps i
Approaching the situation from a different angle,

used here to refer to the material resources (i.e.,
regional herbaria and associated libraries); tl
damerilal knew .-:-;> . skills, and techniques !ni Ho
ristic analysis; and the setting of scientific
dards, generally in a peer-reviewed ci
Custodianship of this legacy, developed ov<
eral centuries, has traditionally fallen within the
<!
in
' plant taxonomy in an academi
but to what extent the con

aiiah/.iu^, and descrihing regional no\(-ltics. what
ever their professional oredenlials and self iiienli
ties might be.
ern North America), the majority of newly desc filled spe< ies (|uali(\ loi some level ol sensitive
species status, with immediate implications for
land management a. Inilies on |.u|.lie and pin lie
lands. IVol.loli s can al ~e i: negative \ affected
landowners develop the impression that so-called
"amateurs" are behind newly described rare speeies witho li ill. h lekll J, >! s. -e ll \ .aneliol ed e\
Even for those species that aren't novelties, a
la. k ! siiflieieut iiioiniation 01 then la\onoun and
distribution interfiles with effective conservation
, in ii~ Ih i j.n I ol'this in Mem can be seen
in the list generated by Skinner et al. (1995) of 182
rare California plants for which further taxonomic
i. i i in. ti
H
1.
and another 44 that require
addil onal disti ihalionnl ii loi'mation helore tlieit
conservation status can be properly assessed. The
implications ol tins knowleda;. -.>:; hecome apparent in the face of decisions '
m l nu n u!<
now which will irrevocably determine the fate of
much of oui nati
i ian
\
s,
n
,,f
ahove. i which larg< i j n i \-1 - lies that lions. 11 a|oi

herbaria Strugs I < l. ,-'
ih.-n upkeep while sin:ultaiH'..iisK rvlejiating desm ptne svstematics to
I. ss url!-cqiii|.[. i! of we I-- hinted institutions. ('<-
transfei d Soristic survey work to the domain of

-.
rent I
. i- also a potenital prohlem il'il is not accompanied In lh< ttauslei
of associated ski
s). Paradoxically,
;
lit
I. matics, one outc(
aelualK he a net decrease in the scientific
uiiderh IM- the analysis and d< seriplioii n
ASSUMPTION
4:
In other words, we risk losing a significanl pel

i-entaî ol o n fl< i isii, I eiimi;. ' M "t sheei igno-
THE PROPERTY RIGHTS CONFLI
Furthermore, what are the broader ramificat

of allowing
to take place
i ( olleclnc
labor of love
an academically supported undertaking?
or worse, the days when new
j.roi. -.- ma
discoveries were of concer
us. Although there a
Juncus tiehmii Ertter
numerous excepl
many plants (and ither or rusm I that would qualify for some lev< ol
ui
ii
it p..ssihl
represent iij '>'/> of die Nordi Vmenean llora ihased
on Taylor's extrapolations as previously dismissed)
and including some of the rarest of the rare, are
ciirronlh !<-. . i\ i-iiL' \'l ) all. i I on h< rails. ihe\ have
not yet been di-,
i .
our own backyards.

In support of this statement, an increasing nuinhei oi novelties in North America, as in other parts
of the world, an I., n-i i!is< meiod "in front ol the
Imlldo/.ei." The l\pe loealilv of \crinsia ciifionii.
for evample, is threatened by a limestone quarry,
i
in
mis Yermo was discovered as
part of a survey along a proposed pipeline route.
The narrow endenn /
t a,
ill Howell]
11 ii
i
a Killer il{o-.,i ae) was still in
manuscript when plans to build a dam that would
light (Ertter, 1988). Cearwthus ophiochilus S. Boyd,
T. S. Ross & L. Arnseth (Rhamnaceae) was found
nil t I
--ii i.in letilal II i study of a proposed development in southern California (Boyd et
al., 1991). Even more recent!-,., il t\pe population
of
an
IT
undeseribed
I'scudoslcHtimi
Kabeler.
in.
prep.)
staging area
lot
an
u;h
(K.
lound
active
Mailman <X
adjacent to the
losing sire,
surveyed for sens live species prim
poloutia K
io approval for
limber harvest, liul uol foi in described fa\a. A new

larweed currentb
iaiiloi 'li.i. alsi
pmei
summarizing hei
popihillols ..1
keniaceae)
efforts |,, g;nn acres- to reporled
F:,i;i!,< t,!,i
on
the
r,hif>!>>hl,
private
' ore|[
ranehlands
(I I.III
of Zapata
Coiiniv, Texas, stale I lolaiusl ! aaia Janssen( u Jans
sen & Williamson, 1996: 3) shared these insights:
Icirm d-'s. nt ,j f>. MII I iveimoie.
falls itilo l!i - cait -m. o. curring as
ix
lr uioisco Bay
Area
(Baldwin, 1999).
I
i feihaiaioh,. there is ;(lso i v deuce of potential
i;o\i
iii.
In mi i HI
ii.
be described. This may be the ease with an a

scribed Eiiognnnm
nienlionoo
lies that had heen searing them lor so long. Thc\
they could even
eded to vent, so I
>
let them. They had no one
n llie protiKoguc ol
E. capistratum Reveal var. welshii Reveal (Reveal,

!
i
ilation in southw.'-|i
(i
hiano !I;|N possihiv
|e< |, i lituinatcd !>-,
'I;e
Encouragingly, this stage was the prelude to a

I
success story. Janssen's patience, honesty, and willingness to listen eompas i
paid .
In
mg the access
needed to aeqill
hi Irci '
! ie iiulido/.. i
di-cov. ;i< s. t-xf-it injj; as

mmunity, can be
a d ( idi dlv
in i i.
in
ii
in]
i
led
pensive complication m
Deed .
ii
HI
x l.iti'. e ',
I-
of the
I,.'\I,I>
> I
Ventura
I, MIS
In.
| . icntially very ex-
mghl otherwise have
[orwaxl and : rofilah
'I
V1at-I
nd
i
-ii i -Ml
lnilkvelcli
-at. /f/'M'%^v,ni;M
it
redis< men
t \sl>,i^n!, ;>>,
not. d
how
tin
pi HI'
'
1st
lliut onal and other
In log
data on a plant that occurs almost exclusively on private land, and subsequently in working
idi th
i
. develop a voluntary conservation plan. As a result, F. johnstonil is eunentlv
In
i:g
removed
fjotn
da-
endangered
species
list.
with many of the ranchers now taking i> . mate

pride in ""their" rare plant (Janssen. pers. comm.
1998; see also http://www.tpwd.state.tx.us/news/
news/980518a.htm).
was mis ii:- trouble" and h;t<l "'thrown a kink" in
the developer's plans to build $300,000 homes surrounding a man-made lake (Sacramento Bee, 15
Aug. 1997). Fanned by negative publicity and
prop, -hi ghis a hoi ales, lla
lies and devi lopi i. n
iaii e(| ;>\
c- >ia-
ih
.i lit n
disoovei \
in Io -'iiraieK
I n
i, .n d at properiv > aliv 11
lie severely
cur-
of siirll Uliw. Icome snipils
led :c a sign hi ai : pnlan/a' on
between
privat-
l< ,\ >
i -
ind
iiboeates ol
diversity
protection. This in turn has often resulted
bio-
in a refusal to allow floristic surveys on private

Ian
11 nl portions of relatively unexplon
i
il .
i.Id harbor novelties
, ad pop i ..: iics
ilnei
-a jmfh ai '
, nl -.
The scale of the fear and distrust has even led

to the paradoxical
... n
i -
irH -I
ili II
situation
a. ie
in
ue
which
local
thousands" of
lamb
a
so-
called rare plant on their properties, while simultaneoiislv

needed
to
refusing
to
justilv
less
tions, frank icsluuonv
allow
the
stringent
Io e\arll\
scientific
survevs
management
op-
this situation, and
that can build up in the absence of tn

sin
- ol idi
.
. the contrary, is
provided by Janssen and Williamson (1996). In
fact that the fundamental floristic work in Kern

County, California, currently a property-rights
In
taken by a local rancher, Ernest C. Twisselm
i I
.
. i
tiia boianv
have re. < nllh
I!. en acknow ledgi tl
n the
form of a newlv dis.

runi
or, TwLsselmannia (Al-Shehbaz, 1999). Twisselmann's interest n
1 by an outbreak
of nitrate poisoning in his cattle (Mc< ait
k.
1973), eventually led to the publication of two floras (Twisselmann, 1956, 1967) and the discovery
of several new species (e.g.. \rinm hi
mannii J. T. Howell. Eriogonum temblorense J. T.
Howell & Twisselm.). The acknowledgments to his
I''
vate
pro\ ide insight

properiv
undertaking.
thai
lav
into the x sp<
behind
the
success
of
his
ol UK Helclwork.
D. FLOmSTIC SURPRISES OH "NO SURPRISES"-.
right foo]igh
When all ig gaid and done? the best
guarantee .,:' "\o Si) II M'i s< -s"' (liie nickname ln a

^ ^^ .^J^ . ^^ conseryation
The Frankenia johnstonii example is only one

among many in v\ln
plans) is complete information up front,
mation base, sometimes paid for by the private

stakeholders, worked in their favor, eitliei h\ pro
viding sufficient scientific evidence for reduced
!t.i.< IN i slain I u l< nil ling) or li n r i i g
the 111 I _
.
''. .les need to be
brought together for impact, but currently exist only
in scattered docunu
I
Granted, there is a ill
in l<
n a tan Ii lai
ily that wishes to continue a way of life requiring
large open spaces, and a developer who needs to
subdivide and buili
1 i
11ize an investment. Even in the I in
> >
> i gali
consequences of floristic ignorance can cut both
ways, increasing the risk of misplaced mitigation
efforts as well as the unintentional extinction of
species,
As a society, we have acknowledged thai the pet
petuation of our biodiversity heritage is a highly
desirable goal, for pragmatic, aesthetic, and ethical
reasons. Within this
l.
|
comes how to accomplish this goal as fairly and

effectively as possible. Unfortunately, instead of
making the necessary hard
MOM on a solid basis of complete scientific l inwleclgc ol'allelci
its
involved, we are fo
the "best available scientific evidence*' is often a
woefully inadequate reflection of the actual data
needed for the kind of far-reaching decisions that
are currently mandated.
A common quandary, for example, is determining
whether a species is truly as rare as existi
,
dence indicates In the < i
ces, it is sometimes argued that, if the scientific evidence is incomplete, then no land-management constraints
can be justified. This argument, however, runs
counter to the fact id ,i ill ega di
i i
i ml
ing those addres-nu n ronm i i
ssu \ an
based solely on best evidence available at the time
of the decision, will
\ nor supposition having a legitimate role. One can speculate
that a species is more widespread than the currently available scic
<
idieates, but a
decision based on this speculation without hard evidence to back it up is no more justified than is
ruling on a defendants guilt strictly on speculation
that the person might have done the crime. Given
this, it is readily apparent that operating from a
maximally comprehensive and accurate information
base is vastly preferable to acting in ignorance, and
ASSUMPTION
5:
THE OVERWHELMING CHALLENGE
Within this framework, the significantly preferilil ipli-m to isoi

ii, il
i ment-driven surveys
would be a proaelive. comprehensive effort to address the existing gaps in our floristic information
i
I for an undescribed
|l il >i i i nili. il population of a sensitive species to be discovered after significant funds have
already been expended on a proposed project lega newly disi i
'is "complicating
' < npii i
ralions" I
lli _<'_ >
r<
in Utah, having been found at the site of the men's
downhill race course (Deseret News, 22 Aug. 1998;
Windham & Bellstein, 1998b)]. There is furthermore a distinct sense of unfairness in having the
short si raw (all loth, landowm risl ol llie last refuge
of a once-common species, which only became endangered wliei tieighl
tldowners had devel u parcels first.
Avoiding sin I siiualions is m fact a primary goal
behind the current focus on developing regional
conservation plans on which to has.- land-managein til d i ions Mil nigli
1 lent in principle, in
< n d< fie ient in addi
i ition, in large part
because of the assumption that obtaining the relevant species-sp < die I)..risti. it formation is too formidable a challenge to pursue. This in turn leads
to the argument
i lot mation (e.g., sat.
, .
s) serves as an adequate substitute to field-hascd. species-s])c-cific
floristic data. A dramatic counter to this argument
is provided by the Shasta snow-wreath (Neviusia
cliftonii), in which a relativelv conspicuous shrub
inpletely overlooked by one of the most com .
i
mi
o> . t-, ever undertaken
( I
(Weislander et al, 1939). As a bottom line, largescale land-management plans that address only
dominant and formally listed species have the potential of alio i
rem. nlal disappearance
of all other species in the region, including any
undescribed novelties, without even leaving a record of their previous existence,
The challen
|
ivel) addressing the
species-specific gaps in the floristic information
base is indeed I..MM MU.
I
the assumption that
it is an overwhelmingly unrealistic goal is based in
large part on tl
e\ lously addressed.
In particular, il ran danlU be said that the asi ' 'in

' !. |>ii ' i ! test, given the
,
acknowledge incompleteness of existing floristic

knowledge base;
assign value to'floristic information commensurate with the effort required to generate it and its
value to society at large;
ensure that essential academic resources are
available at regional level;
foster the network of professional and para-pro|rs>ii;nal expertise;
t
th
t ainine a d
articin t'
f
;;;;;;;, il(
;*;; it;,;; ',;;;;;;,;;_
ti ;u:;;,
able scientific standards;
depolan,,- .vlatinns i.h private landowners, with
H ad, m
,
,
,
.... essential
,
' ,
,
i i<a it ml fIramework;
disperse Holistic information in a framework that
addresses the particular needs of all part i, ipants.
have been up to is nothing less than one of the

i
i
< ois ever undertaken:
namely, a centuries-long, internationally collaborative effort to model global biodiversity If this
does
not
wnat
qualifV as "Big Science," I don't know

does! The significance of this undertaking
takes multi le forms
'
startin
with the
fundamental
desire to know what other forms of llfe share thls
planet with us, the only island of life we know for

iertain exists in the
"Averse. The resultant model

also forms the
foundation underlying other branches of
biological knowledge, and it follows that the
êr tne fundat
mem- of R w.
T^,
i983). Most important,
w ^ ourselvejs in an e,ra when cni\d<

"""s "'", h"u'- ,na'l,' ,hal *'" ,,,',,'n|nn"' t,,r ,a
"{ Mv "" the P1**'1' ]S imPerative that these d.
cisions be m ill. lit. in .s| , ii,r I. i
.U1
nj
Furthermore, the challenge of obtaining the spes-speeihe floristic information needed to make
Several possible prototypes incorporating one or

more of these elements have already been developed. The Rocky Mountain Flora Project, for example, demonstrates the scale that can be accomplished by focused floristic surveys within an
academic setting (Hartman, 1993). In contrast, the
Oregon Flora Project depends less on graduate student projects and more on existing and newly generated information from an extensive network of academic a"-ncv and native plant society sources
critically anah zed 1
al
science-based land-management decisions in North

America north of Mexico, although formidable, is
not beyond our grasp. However, the viability of the
essential professional taxonomic infrastructure
needs to be ensured, and the undertaking apPoached as a seriously supported collaborative effort
combining academic and para-academic resources at the
regional level. If not, then we risk
losin
g 5% of the floristic diversity in the North
^" '"'
' ' ' 'ince alone, as well
as unfairl
y allocating the conservation costs for bio-
systematists (Sundberg, 1997). The 1980 peak of

novelty description in Utah, as shown in Figure 1,
resulted in large part from the collaborative activities of regional academics, agency biologists, and
environmental consultants, and similarly collabo"haybahng expeditions" have taken place in
diversity in general.
A
quote b? Thomas Bridges opened this paper,
expressing his amazement that there were still unnstlc
prises in North America in 1858. I will
end with a more accurate
perception by Dieter
XX
'^ , '
"
"
'
' ' ; ^ Colorado flora
.1984,
ransmitted by
Idaho (Big Horn Crags) and the southern Sierra Nevada. In the San Francisco Bay area, a regional
checklist was specifically designed to facilitate and
encourage the participation of para-academics in
1998 :
l am
are
>
ye
continually
iscovere .
floristic inventory efforts (Ertter, 1997b). In that

ol these efforts, and the discovery of "floristic s
\i K\>>\\ I ! M.M
prises" in general, have proceeded with minimal

institutional support in an increasingly avocational
network, one can only speculate as to what could
potential!) I>< .<
ii i
>k
of a wellid i
i
i
undertaking, taking full advantage of both professional and para-academic networks.
This paper would have been significantly depauperate, if not outright impossible, without the openhanded sharing of favorite examples, photographs,
personal anecdotes, survey responses, and other
itude of persons, to
whom I am accordingly indebted and deeply grateful. In particular I must express my deep appreci-
ation lor (lie gciicrosilv ol (hose individuals who so

11fill slides ol photogenic novelties, and/or provided
tne with niipulilislied (1^1110 lli;il pm\ uled .1 < nln a I
~hitistir.il underpinning loi Mils paper: James \ffolter, Steve Boyd, Thomas Brims, Hoy Buck, Adolf
Ceska. David Charlet, Beth Corbin, Raymond
Cranfill, Marshall Crosby, Cliarmaine Delmatier,
Ronald I.. Ilailmaii. Noel I Inlmgren. bred lltnsa.
David Isle, Gena Janssen, Patrick Leary, David
Maguey, Richard I.. Moe. James I). Morefield, Jan
Nachlinger, Elizabeth Neese, James L. Reveal, Anton A. Reznicek, James R. Shevock, Raul Silva,
Frank (Buddy) Smith, R. Douglas Stone, Raymond
Stotler, Dean W. Tavlor. John Taylor, Michael Vincent, and Carol W. Witham. Other individuals who
contributed in various ways are Lowell \harl.
James R. Allison, Kelly W. Allred, Ihsan Al-Shehbaz. Bonnie \1110s. Tina \\ers, Bruce Baldwin.
\lar\ Barkvvorth, Kathryn A. Beck, Peter Bowler,
Gregory Brown. Richard Brummitt, Ste\en Brimfeld, Thomas Carlson, William Carr, Terri Charlet,
Curtis Clark. Lincoln (ionslanec, A ll\ son Das is. II
len I)<'an, I)<-imis Desjardin, Heidi Dobson. I)a\id
L. Dyer, Wayne Ferren, Stuart Garrett, Arthur Gibson, Ann Halford. Richard llal-c. Can Natulan.
Walter Holmes, bam HuHord. C. baigoue Join-.
David Keil, Sylvia (Tass) Kelso, Les bandrum. Malt
bavin. Aaron biston. Timothy bow rev, Don Mansfield. Michael Mai.cuso, Niall McCarten, Lucinda
McDade, Dale W. McNeal. Brent Mishler, Joseph J.
Molter, David Morgan, Walter (Tony) Moroseo, Barbara M in ia\. David Mimav. Kathleen Vlson. I'i\
an Ness, Wesley Niles. Richard Olmstead, Brad Olson, Robert Ornduff, Vernon H. Oswald, Jose L.
Panero. b'obcrt Patterson. James B. Phipps, Jackie
Poole, Daniel Potter. Jerry Powell. leresa Preiidusi.
Richard Rabeler, Thomas Ranker, Peter H. Raven,
Moui(|iie 1). Reed, Andrew Sanders, Michael Sanderson, Kristina Schierenbeck. Lisa S. IUIIIIM IS.
I.eila ^liult/. Bei\l P.. Simpson. Michael < '.. Simpson, Alan R. Smith, S. Galen Smith, Douglas Soltis.
Brian Speer, Bruce Stein, Kingsley Stern, Scott D.
Sundberg, David Tibor, Arnold (Jerry) Tiehm. Carol
A. Todzia, Billie bee Turner, Florence Wagner. Wai
ren H. Wagner, Phil S. Ward, William A. Weber,
Steve Weller, Stanley L. Welsh, Jun Wen, Charlie
Werth, Dieter Wilken, Hugh Wilson. Michael Windham, Lindsay Woodruff, Richard Worthinulr.n. Vlichael J. Wynne. \,,n Yidon. James Xarucchi. ami
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A NEW AGE OF DISCOVERY1
\UMI{
Michael J. Donoghu.
William s
\<:r
Whereas pa
smaller spatial scales and in more extreme halita(s. some of v\ hi<-h are surprising close a
M latioiisl ps in,: i, ojiapihie. ranges
i _.
uri<;i.i -lioiiahh.
JI-
n I -i
'
\
\lthough
I i
h-
uaniil
HI.hug
the tree of life o
yet underutilized, mechanism
" > * I-
diseoven. biodiversity. I ilii^'ii"! aphv. exploration, new species, phvlogeriv.
We tend to regard "the age of discovery" as

something long since past. Whether the phrase refers to the colonization of North America in Irai >
Beringian migrants, arrival of the Moa Hunters and
Maoris in New Zealand, or (most likely) the forays
of European explorers into the New World from the
15th century onward, depends on one's sense of
history and focus. However, there may be general
attributes of all previous ejxx
evaluate whether any particular period reall) qua]
ifies as an age of discovery. We will argue thai the
present era most certainly deserves this title.
Briefly consider the most recent of these ages of
discovery, which began in the late 1400s. European
exploration of the Americas, Australia. Africa, and
the South Pacific brought to light an extraordinary
number of new species. Even more 1 in
I ttl
these were species quite unlike am known l-fnt<
(Fig. 1), the kangaroo, and the
name only a few. David Quammen (1996)
. imagine what it must have been like to
In ine^t major lineages the i

eies being described is not fall
numbers have acliiallv been lis
to late 19th century (before v
ilillienlt. Mill- . Fcim.il ; lies ioi naming species had
not been de\eln| I Si ipiisinub. p< diups. tl is n
eludes the groups that we tend to think of as being
For <
h< det
new mammal species is on the rise (Wilson vK
Beeder, 1993), and this is not, as one might initially
rppose, primari
fitting of known
species as a eons. ,p ,
,
ilccidai mark
ers. Instead, it appears to lie directb correlated
with sci ions exploration of new areas (Morell,
1996). For instance, fieldwork over the last decade
ii (I:, \iin, in ! moniilaiiis ..n th, Ixadei <>t < nlral
\ lelnani mil ! .ii- I -J- I'.'., lid:' '.< I -hi s--, rial l:n:'t
1 illustrations. We are especially grateful to Steve Solheim. who helped inspire

this work by introducing us to the Museum of Jurassic Jcchiiologv. and who opened his own bibliographic \\ lerkammern for our us, II,
,
,,
,
n it, r ials m advance
Cadle. Kov Caldwell I
i- <
Halanveh. David H I
Rust- Vlittern
Mark Moll
Akiko Okusu, Jim I'
I.I
Gustavo Romero, George Schatz,
Wolcott, Patricia Wright
I i/
2
Harvard Dnive.s,'
|
'Current address |
Illinois 60605-2496, U.S.A.
n
i ( i!
, I
In I )o\ le. fhomas Kisner. Frank Glaw, Ken
I
I If no \<h knoll love, I .. , ., Santiago Madrinan My Martin.
I
I
Dail
i. Da Mektenl Ronald Nils l,im.
I
-vol
id Kick Ree. Mick Richardson, Robert Hidgely,
David Wake, Doug Weehsler. Mark Wilkinson, Bill Wilier*. David Wilson. Catherine
/ii
I
I. pel with the preparation of the figures.
.me. Cambrid
lassachusetts 02138, U.S.A.
I'rograms, The Field Museum. 14(H) S. kikeshore Drive. Chicago.
87: 110-126. 2000.
,ed by Mbreel.l Dine. Jl ill, Inn.' these jnii.nl- were first discovered
inn ion. In,.,, ,ni original |iimt al ill.- \nes Monan Center. 1-'.^-; \rl \III-<-II.II.
Nearly two centuries later. I.|M... -ecing a rhii.oc.TO..-. Join. Kvelyn remarked. "It
* Sum.-, than an> other Reast amongst us ... but in ni\ (>|.iiiinii nothing was -..
I -kin. began to lie -tinl.lir.l Willi impendrahle Seales. like J Target of eoate ol nuile. Ion. ..led
certainly a very wonderful creature, of inimci.se slrenglli in the neck and nose especially"
mammal- a -peeie- of lio\i.l. I'scinlorx \ tiiihctinhensis (Dung ct al.. 1993). and at least three species
of muntjao deer (Schaller & Vrha. 1996; Giao et
al., 1998; MacKinnon. 2000 this issue). Moreover,
tlie rate of description of new mammal specie- has
risen despite decreased attention to taxonomy and
. 1994).
Amphibians provide another wt
xample of the rising rate of speei
^law & Kohler, 1998; see Fig. 2).
""
scribed in 1998 from Brazil. Mexico. Nepal, and

New Zealand.
The same trends in discovery (if not formal naming) doubtlessb applv in I.-- well -Indie.I groups,
such as plants, fi-h.-s. iiise.|s. miles, nematodes,
and especially bacteria (enbactei iai and \iehaea
(archaebaeteria, e.g.. Pace. 1907: Fnlirman iK
Campbell, 1998; Mad.urn.. 21)00 this issue), al(e.g.. s.r Gaston. 1091. on insects; Prance et al..
2(100 tin- issue, on vascular plants). If there were
;"
molecular m. llx-.b i I! ni i -pe. ics concepts.

Ilaiikci: ! 1009) documented this point, citing David
W.iiv.' i l,',<i) discovery of a new hingless salai ml . I-..MI PI. ^ ii
ml.mis, less than
30 miles from Los Angeles, as well as species de-
dise.ivery and naming of new taxa were shorter.

then the rate of description would surely be far
higher. Many new species have already been collected, or are already known lo be new. but remain
iindescnbeil simpb lor lack o| expertise and time.
Plant monographers, for exaiiij.le. can show any ell-
rions visitor ,i n. arbv specimen eabim 1 c .ntaii nng

undescribed species.
By the criterion of the number of new species
fifing :;,-s, iiiir-l, we believe lli.ii the present coinpares favorably with any time since the mid-1700s.
But how surprising are the new species llial are
!
_
entury? Are we
i i
i i <
leient, or are we
just filling gaps in an already well-known range of
variation? John Horgan, author of The End of Science (published by Helix Books, in 1996), presents
the latter view:
think al.oul ih. diversitv an.I e\ olution of life. Un

fort U I tely, this is much harder to qiiai;:d'\ thai
I descriptions o
i .
iI ,
M
i i
li ips of iheii iiiformativeness with respect to our undeisiai ding ol
evolution, is the rate of description of m v. Im-li.
taxa. As Brusca (2000 this issue) shows, the description of new animal phyla does not appear to
,d Ihal
This will sound absurd to those actively engage,

,
the discover) ol new life forms. hut swcl a "dot! ng
nation is n idi spicad both w Him die sci. otitic cm
mnnity and the public at large.
To counter Horgan s naive but evidently persuasive claim, we need to consider criteria whereby a
new species would <|ualilv as ""real.v snrpn-Miig.""
Pei haps ih.- piimarv criterion should he whethei a
new species fuiidametiiallv expands die u,n wo
considered by the rek
lai iliat phyla are from one another. The niajo: iU[
ferenee is that these new organisms are, on the
who!.-, smaller, which means we are having to look
more closelv. Sometimes, as ill the case of Nanaloricus mysticus of the recently described meta/i an
phylum Loracifera (Kristensen, 1983), this has eni I. . a lnl s< rnlinv ol an obs< un <
i i <ci
i
i ' i
i i I it 11. twi < ii sand grains
other cai
r less right under our noses,
animal referred to
- dl -. I bed III I1'' ". . Iroin
a specimen collect. <l < i the mandible of a Norwegian lobster (Funch & Kristensen, 1995).
New "classes" of animals, sometimes with enormous significance for our understanding of major
lineages, are als<
. I
ribed at a regular
pace. Kxamples unhide ihe Keinipedi.; williu
Crustacea, discovered in a marine cave in the Bahamas (Yager, 1981), and the Concentricycloidea
within echinoderms, found <
i
deep waters off the coast of New Zealand (Baker et
al., 1986).
In angiosperms there are excellent examples,
mainly in the form of new families erected to ac.Mi, in. I Hin i HIinary new species. For example, recall the excitement gen ml I
mi. and L. D. G6mez (Ticodendraceae) from ' iosla Hlea (( aunt /, I .aurifn iX ,n
mez P., 1989, 1991), and the subsequent realization
that these trees occupy wet montane forests from
southern Mexico to central Panama (Hammel &
Burger, 1991). But the most spectacular case is
' i
w hismatica K. Martinez and
Ramos.'This species of Triuridaeeae-like monocot
was described in 1989 in the new family LacanI i i i
(nun main I . oll< < led in the Lacandon
region of Chiapas, Mexico (Martinez & Ramos,
1989). Astonishingly, its stamens arc on the very
inside of the flower (at the apex of the receptacle).
surrounded by the carpels (Marquez-Guzman et al.,
I"'."' -..-Ii" . i I In .1-.
.1 . only a few years
ago, came as a complete surprisenothing about
the other ca. 250,000 species of angiosperms predicted this brand new flower architecture. It also
provides a unique opportunity to test the "WW.
model" for genetic determination of flower organ
identity (Coen & Meyerowitz, 1991; Vergara et al.,
1999).
If the description of higher t ixa were our only

means of assessing the surprisingness of recent .lis
covcries. we would miss man\ o( the most exciting
funis The sescial examples below highlight radically new life forms (as different, we believe, as
those discussed above), which were described onl\
as new genera or as species within existing genera.
These cases prm :'- a drama' c < minder of the arbitrary nature and inadequacy of the Lmnaean
gauging the degree of disparity,
ataceae). This remarkable new species. (,. <i</ihih

ca, develops its fruiting bodies and spores underwater, often beneath a layer of ice covering lakes
in a zone between the Patagonian steppes and the
Andes. As it appears to be the only known agaric
to sporulate underwater, the term "unusual" is
clearly an understatementthis is a brand-new
In 1976, Escobar et
al. described the genus Limnoperdon to accommodate the only known "aquatic" (actually, floating)
nuilbad. which they found in marshes adjacent to
the I'niversity ol Washington in Seattle.
Amphibians also provide excellent examples of
recently discovered lifestyles. In 1973, a new genus
and species of leptodaetylid frog. Rheobati
I
wa le ribed on the basis of animals found
in streams near Brisbane, Australia (Liem, 1973).
Shortly thereafter, Corben et al. (1974) documented
itilrachus exhibited a unique form of parental care. Brooding of the embryos and young
takes place inside the stomach until the tadpoles
or invenile frogs an- eventually (some eight weeks
after ingestion) "propulsively ejected" through the
mouth. This brooding mechanism is otherwise cm
pletely unknown in vertebrates. Furthermore, it requires special physiological mechanisms to turn off
the secretion of gastric juices, which otherwise
would kill the young. In 1983, Tyler et al. reported
tl .ii
i'.-iaglandin secreted by the larvae inhibit
acid production in the female's stomach "in a manner not seen elsewhere in the Animal Kingdom."
Despite the potential medical significance of this
remarkable phenomenon, further study will not be
ais to be extinct
in the wild (Laurance et al., 1996).
In 1996, Nussbaum and Wilkinson described a
new species and genus of caecilian (Amphibia:
' ru
inona), Atretochoana eiselti. As the\ documented (also see Wilkinson Si Nussbaum, 1997),
this is the largest inndess temped, by far! It is 74">() em in length, while the next largest, a plethodontid salamander, is about ' , tins size, al around
cavity in this animal, and its many oilier weird era
nial features allow an exceptionally wide gape (see
I'm. 11. I'hese modifications are presumably asso
dated with a novel feeding mechanism, but the nal-
In 1995, with very little fanfare, Dennis Desjardin and his < ,.1 . ji
-,. n;.t J
ti m
I p
fael. this extraordinary beast was

in a museum in Vienna and was
only a single specimen collected from
i South \meriean locality sometime in
1
i
H
the existing fun.
; time in a jar in a Brazilian collection
ane from Argentina" within

hula (Tricholom-
(Wilkinson et al.. 1998). Ironic-ally. it. too. lacks a

specific collection locality.
Other newly discovered specie* highlight how
much we still have to learn. From Bacteria, consuler Proclilonx >>< cus. dis.>-\ 11. d .in 1 \ about a decad.ago. Of great interest owing to the presence of both
chloroph\ll a and b (as in i^reeii plants), it is known
now to be a major conipoiieiit ol the ph> toplankton
in tro(iical and subtropical seas, and among the
world's most important priinan producers (setFuhrman & Campbell, 1998). Moreover, the ability
o|' l'n>rlili,r<><;>crus to thrive in a wide range of light
conditions seems to he explained by the existence
ol eloseb related but <[iiite distinct species, living
al ilillcrent depths (Moore et al.. 1998). Also of
potentially huge ecological significance are new
disease-, -ausing bateria. for example, a uewb discovered species of proteobacterium (related to
" "
i i i
rnas*,i\< coial
die-offs in Florida's reef communities (Richardson
et al., 1998).
soyphozoan jellyfish Chrysaora arhlyos (sec Fig.
31)). This specie was described |>\ Joel Martin and
colleagues in 1(>('7. hascd mi font specimens eolof 1989, and some photographs from northern Baja
1 ',: ill', MI is (Mai I in et al.. I''("7l. ( )ne . il' se\ eial species in llns genus. ('.. <u-lil\i)s is remarkable by virtue of hemg enormous. In fact, with a hell measuring over 1 m in diameter, this is the largest
invertebrate described in this oenlurv. rivaled in
size only by the giant squid and an arctic jell\li>h
described in the 1800s (J. Martin, pers. coram.).
ished ashore in 1989, it has
manner Kurycea sosorum. This species was described in 1<)(>'> bom specimens collected in the
i us V11111 i. within the <it\ ol \nstin.
Texas (Chippendale et al., 1993). Known only from
!
opular swimming spot, and therefore in
to attract considerable attention in Austin. Subsequent exploration ol iiearbv springs, some located
within Vustin housing d,-\, lopments. has mined up
dozens of new species (I). Hillis. pers. comni.). Description of these species, from a rclati\.-K small
area well endowed with herpetologists, will increase
Just as r
rous new amphibians are coming to
light, so. too. are novel pathogens that prev upon
them (Hanken, 1999). A new genus and species of
chytrid fungus, Batrachmhytrium da,
described very recently (Longcore et al.. 1999), appears to be a major proximal'' cause of mass mortality events in frogs around the world (1'x-rv.ei el
al., 1998; Morell, 1999). Being the only chytrid
known l<> |II. \ on vertebrates, tin- new species also
greatlv expands our understanding of a major and
ubiquitous fungal group (I,oogenic el al.. I'>('>:
Pessier et al., 1999).
Seed plants also provide fine examples. Wollemia
nobilis W. G. Jones, K. D. Hill & J. M. Allen, the
sister group of Agathis (Gilmore & Hill, 1997) or
tutes a genuine act of discovery. Viewed in thb

light, it is count
i
haw too strong i
id in 1994 growing in the Wollemi National Park,
. 200 km northwest of Sydney, Australia (Jones
al., 1995; Briggs, 2000 this issue). How could a
ge tree, with such distinctive architecture, growl near the largest city in Australia, have escaped
lection until 1994?
At
\i..lr.
colleagues wen <>;i\ /in- llial < .: hallos.-, ol an i >< ]. 1
proteaceous tree made in the 1960s and 1980s from
northeastern Oueensland represented a new spe(H tir\a A. W. Douglas & B.
Hyland. These 40-m-tall plants, seemingly endemic
to rainforests in the Bloomfield River watershed,
are the sole repr. - i li m anpa
id
I
iin age el Prod iee.n . llie I iiolheoid. ae (I >oi,glas.
1995; Douglas & Hyland, 1995). Its fruits are nearly identical to 60-million-year-old fossils of Xylocaryon lockii F. Muell. (Holden, 1995).
Neviusia cliftonii Shevock, Ertter & D. Taylor
(Rosaceae, Kerrieae) provides a similai
(Ertter, 2000 this issue). This species was described in 1992 from material collected south of
Ylounl S'ia>la in iiorthei n ( ai if'oi rua (She-, neN el a .
I(.'()2|. \ though ni i- a rathe- conspicuous and locally abundant shrub and grows at several localities
in an area where the \eg. tali
been mapped, it seems never to have been colli el
ed before 1992. As the authors speculated, the
:>f : u-.oreoak in die \ icinity may have
ci ng lades Tl es. !. M\ Hi. s an piei cs of the sam<

undei \ HIS j i'o),-, :. a line \. und< istai 11nu llie en
I lie.
\.id i
da ongoing ag.
discovery far richer, and certainly far more powerful u connection with praciieal pioi>|, nis s.ioh a-. lot , v iniph . I fie choice and
design ol nalure reserves and the search lor MM iiil
natural products. In general, knowledge of phylogenetic relationships brings with it the power of
predi. lion Pre logeia in -esoat. !i should therelnie
, addil
ompetilni with, the stlld\ I
Consequently, it is of great interest to consider,
as we have for species. both the rate of discovery
i
< ss of these new
discoveries. Unfortunately, we know of no straightforward way to quantify these things. There is little
I
e rate of discovery, and databases such as TreeBASE (http://phylogom hai vaida (i i/lre. base!, w I i< I could evetilu
grown too unevenly to provide an accurati measure
I
a.
discovery. Nevertheless, the rate appears
to bi gMmu
| I in III
i shows no signs of
tapering off (Sanderson et al., 1993). At least this
is the case if the umib.
grows in proportion to the rapidlj in ii ising num
ber of phylogenetic analyses being pi ish, .
Judging by its resemblance lo an Kocene fossil from

P.nlish t .ohniib, i \ . ;,//<<'),, is pnibabb a i< IK t ill
this area (Shevock et al., 1992). Its closest living
relative, Neviusia alabamensis A. Gray, is known
from only a few localities in Alabama and Arkan-
. noislcnl l\ enough ; lew,-- .:; ii ir- important !o a|>

predate that even if this were now possible, the
number of eludes act i ill , I. i iug named is far less
than the number of clades being discovered, or
even the number of clades identified with great
confidence. Keliiclan to fen-,; I \ nam. chides
The ongoing age of discovery differs importantly

from earlier episodes I., -nine ol the attention being paid to phylogeny. The phylogenetic notion of
es of evidence all A. ; rig

i
nd Use trust) increasingly accurate phylogenetic inferences. Although bioiio.. isi|\ i- si ,11 . oinmi.rh . qnaied a ith
the enumeration of species (ai
within species), the idea has t
diversity is not just about species, at the tips of the
tree, but about the whole tree of life. Thus. |md i j
r,k. ar.l other levels (Baum et al, 1998; Hibbett & Donoghue, 1998). Related to this is the realization that
there are not enough familiar ranks in the Linnaean
system to do justice to the many nested clades being discovered even in average-si/ed phvlogeiianalyses. In practice, the current nomenclati
coil< s (e.g (,r. lit. r et al.. I*)')
i
i
mail!
naming clades onlv after relationships th
igl t
Ific group m ,;u. shon I .!>, been a 'I .-: well c-taa-
Volume 87, Number 1

2000
Donoghue & Alverson

New Age of Discovery
lished, as opposed to encouraging the naming of

vscll-Mipporlrd new clade- as the\ arc discovered.
Even within mammals, where one supposes that

many relationships have long since been established with certainty, there have been some majoi
surprises in the last few years (de Jong, 1998). Our
favorite case concerns the position of elephant
shrews and golden moles. Once considered insectivores, these are now seen to be united with aardvarks, hyraxes, sea cows, and elephants, which implies extraordinary morphological radiation within
a basically African clade (Springer et al., 1997;
Stanhope et al., 1998).
Within green plants, molecular phylogenetic
usually one or a few at a time (Hibbett & Donoghue, 1998).

The sui-prisingness of recent discoveries is also
hard to judge because prior views on relatedness
have often not been expressed unan
enough. \e\ rrtbele-s. i| l:-. <;<; j | ilia! mati\ eutirelv
unexpected discoveries have been made. We now
appreciate, for example, that "prokaryotes" are not
a single branch, but two (or more) major branches.
with lineages o| \nhaea probabb more closely reled > eukai
an they are to Bacteria (e.g.,

Pace, 1997). Likewise, we can say
confidence that animals and fungi (Baldauf &
Palmer, 1993; Wainright et al., 1993), and possibly
also slime molds (Baldauf & Doolittle, 1997), are
more closely related to one another than they are
to plants or any other eiikarvoles.
V\ III
ll s< I . . I. 1 ,| I I,I
d\ UK ' s in < Mil
un i -i nling of life, such discoveries may not
tig since relationships of the
major lines of life have always seemed obscure.
What about within metazoan animals and green
planth. < | i l< . l
ihenres have been lii tter developedhave any really surprising results
emerged (rote reeenl slucit -v
The
i lineages havi
where;,- ii ha- Ion:.: beer a~-i:iiii ' \\ a1
.HIM
d-
molluscs (as evidenced by segmentation and the

i istence ol" s< i rL 1 111 i in. < liate onycophorans),
ttilli h reeenl ev idence pi n|s instead lo the existence of a euthrocozoan or lophotrochozoan clade,
which includes annelids and molluscs, to the exclusion of arthropods (Eernisse et al., 1992; Halanych et al., 1995).
More astonishing, perhaps, is the possibility of
an ecdysozoan clade, which includes all of the
melius animal-, ate! lln '. ton unite- u-'hn p< -1
with such groups as onycophorans, tardigrades, and
even nematodes (Aguinaldo et al., 1997; Giribet &
Ribera, 1998; Knoll & Carroll, 1999). And within
arthropods (Fortey & Thomas, 1997; Brusca, 2000),
there is mounting evidence lor the union of Crustacea and insects and even the paraphyly of Crustacea with respect to insects (and possibly the other
major arthropod groups as well). Among other
ibiiii.-. 'hi- implm- . i ii',. i^.-nl e-.oh.tn i -r ,i, j
tations to life on land (tracheal systems, Malpigl ian
ally the Atelocerata).
117
mention only a few (see Doyle, 1998, for others).

The whisk-ferns, Psilotaceae, now appear to be related to Ophioglossales (e.g., Hasebe et al., 1995;
Manhart, 1995: Wolf. IWTi. as opposed to being
remnant rhyniophytes or related to some group of
leptosporangiate ferns, as suggested previously.
Within ferns, the aquatic and heterosporous Salvitiiaeeac and Marsileaceae, long viewed as unrelated, now appear to be directly linked (e.g., Pryer et
al., 1995; Wolf et al., 1999), a connection also supported by fossil evidence (Rothwell & Stockey,
1994). Within angiosperms, the tricolpate or eudicot clade. recognized first in morphological analyses (Donoghue & Doyle. 1989; Doyle & Hotton,
1991). lias been rather consistently upheld in molecular studies (e.g.. Chase et al., 1993; Rice et al.,
1997; Solhs et al.. 1998: and even the highly unresolved parsimony jackknife anabsi- ol kallersjo
et al., 1998). This represents a real departure from
the traditional view that caryophylids, hamamelids,
and othei major lineages were derived independently from magnoliids (e.g., Cronquist, 1988). Other sin puses include Drosera and Nepenthes being
related to caryophillids (Albert et al., 1992), a
clade including almost all plants with mustard oils
(Rodman et al.. 1990). and a connection of woody
Hamamelidaceae and Cen-iiicnlnlium with herba
ceous Saxifragaei ac and relatives (Soltis ei Sollis.
1997).
Some of the most interesting early results, such
as the basal position ol dcratopfnUiim within angiosperms in r/>rl. analyses (e.g.. Chase et al..
1993), have not been consistently recovered as additional data have been brought lo bear but other
seemingly weird results have been upheld. Of
these, we are most excited about the possil
tj thai
Proteaceae, Platanaeeae, and Nelumbo are posilioue.l neat the base of eudicots, and may form a
clade (Chase et al., 1993; Rice et al., 1997; Soltis
et al., 1997; Hoot et al., 1999). Based on outward
appearances, one would never guess thai these

plants are closely related, and a direet relalionslnp
of the three had never heen suggested. On closer
consideration, this , ran: 1 - il
1!
Mi in
a morphological standpoint, though il has proven
am names an ,.1: >f l 1. li > rl.i. !.- by means of phylogenelie l.-lmi11<>ti- (e.g.. a "node-based" dofinilion, such as "the least inclusive clade that contains species X and species Y"; de Queiroz &
Gauthier, 1992, 1994). This, we believe, represents
1 major and very positive shift away from arbitrary
lecisions about rank and the need to appeal i- an
coram.).
thority (e.g., Cronquist, 1988; APG, 1998) concern-
Although many phylogenetic problems have

been convincingly resolved in recent years, the relationships of many groups remain unclear. In most
cases, this reflects lolhu g moic than 1 inited aliention, and we can expect s|t lighllorw ml solutions
Yet, in some other cases, relationships remain unresolved despite considerable attention. For exampie, it is fair to say that relationships among major
mammal lineages are >t il I up in the air ide Jon-j,.
1998). Likewise, relationships among major seed
plant groups ha\e still not been satisfactorily resolved (Doyle, 1998; Hansen et al., 1999; Winter
et al., 1999). Will
s. perhaps the
most remarkable confusion -in .and- II I tl--i \.
While the position of most ol the other parasitic
groups has fallen into place, the relationships of
h'afllesiales remain highly uncertain, despite great
efforts on the part of Nickrent and colleagues
(Nickrent et al., 1998). In fact, at this stage it is
still unclear whether Rafflesiales are eudicots. or
are instead more closely related I
ic or another
nionosiilcate group (as 11\tlnoraeea.- now appear to
be related to Aristolochiales/Piperales). A remarkably accelerated rate of evolution ol the nueleai
ing the circumscription of taxa. One would immediately know, for example, whether or not
"Bombacoideae" is included in "Malvaceae." if
I,old naincs were jj,i\ *n ph\ logenelie definitions and
il 1 parlieu
vpothesis were accepted (Baum et al., 1998; Alverson et al., 1999);
without phylogenetic definitions. Iiotanical authorities could and 1 I
disagree about this,
even if tlie\ accepted the same underlying phvlngen\ for their nomenclatural decisions,
Finally, as emphasis shifts toward phylogenetic
knowledge, the need to database such information
will become increasingly obvious, both lo track progress and lo rendci phy logcnel ic discoveries accessible to a verv wide variety of potential users. Several complementary efforts have been initiated to
keep track of and synthesize this information. 111eluding TreeBASE (see above) and the Tree of Life
project (http://phylogeny.arizona.edu/tree/phylogeny.html). However, owing to the exponential increase in phylogenetic research, and limited support for these projects, they have not been able to
keep pace and are therefore still inadequate for
mam purposes. \\c hope thai this situation will im-
artifacts in phylogenetic analyses (e.g.. placement

of Bafflesiales al the very base of angiosperms;
Nickrent & Starr, 1994; Nickrent & Duff, 1996).
What can we expect in the near future? First.
and most obviously, the discovery of chides is still
in its infancy, and many more breakthroughs are on
the horizon. W- expect that even the most recalciIrani problem-,, including those jiisl IrillJn ;.
sion ol phylogenetic data sets as a co-requisite of

publication (see, e.g., Myrologia), perhaps also
linked with the registration of clade names. In any
case, this is a problem that the s\s|ematics eommunity will need to address in order to capitalize
on the major investments being made in phylogenetic research.
will eventually yield to more data and belter rrieth-
AITEYI'ION TO
Second, we trust thai moic attention will be paid

to the naming of newly discovered chides, so as to
The present age of discovery also differs in the

attention being given to geographic ranges. Collec-
rapidly. unambiguously, and with as little tinmenclatural disruption a- possible, for this purpose we
quite recently. Recall, for example, Darwin's difficulties in reconstructing (after the fact) the islands
ich his Galapagos finches were actually collooted (Sulloway. 1982). In contrast, we now place
greal value on detailed, accurate specimen labels
and on dalaba
ilormation. Many of
the most imporl il
1 -.lions In
h< >
n
an
of biodiversity depend heavily on such information.
such as the distribution and relative "hotness" of
above). Fortunately,
ing developed as a
result of a workshop held al the Harvard Herbaria
in \11g11sl 1008. This will soon be available via I he
internet for evaluation and. n i- iiiicnlly, for formal
use. In this system there are no categorical ranks.
GEOGRAPHY
Volume 87, Number 1
60
L
2 3 4 5 6
10 11 12 13 1415 16 17 18 19 20
Number of specimens
mts. 'Hie data represented in this graph uei
car). Afiuristd. Cmillhriid I l\i icaceae).
diversity hotspots (Red. 1998). or the existence of

refugia in Amazonia (Nelson et al., 1990). Morenntni. !- >,v I. t\<A,-. such a- estimating the impact of
human disturbance on species loss (e.g.. Pitntn et
al., 1995), arc impossible without reasonable
knowledge of geographic distributions.
Where, then, do we stand in our knowledge of
geographic ranges? This question is difficult to answer, since baseline data have not been compiled
M ii i|i| i i in. I In n I lov\< vet. there arc sex
era I reasons to believe we arc still very far from
having an accurate picture. One elcar iudh ation is
the fact that main species are known from one or
a few museum collections, and these are often old
and lack sufficiently detailed locality data. The
I ii I
ill
> ',', win. h v\c
liii-l'I ; li-.:: above, provides a striking example:
WMI/C,
neithci of the two collections of this remarkable

species provides locablv data more specific than
"South America."
Data collected by Madrinan-Kesttvpn (l<>'>(>|
Iroin iiionouraphic treatments of 15 tropical plant
edly common. Of the 317 species he considered,
122 |.'.;;..V/r) were known from just one specimen.
52 (l(>.4<7r) from two specimens, and 2(> III.2'/I
from three specimens. That is. more than hall were
It is possible, of <
yever. in most cases

ubsequent fieldwork indicates otherwise. Detailed
ata on tins point have not been assembled, but we
now that in most groups of organisms every field
ip\ields range extensions, sometimes major ones.
\ good example i- provided 1>\ recent fieldwork in
a small corner of (v)inghai. China"- fourth largest
province, with an area of around 720,000 km2
(about ()'/, larger than (he stale of fexa-). before
an expedition in 1995, only four bryophyte species
were reported in ill. literature fur all ol Oinghai.
Three weeks of moss collecting by Benito 'Ian in
"rtisliu lYcfecture alone v ielded 57 genera and 109
species (Tan & Yu, 1997). Two of these species
were new to science, three were previously miknown in China, and ten collections represented
major range extensions within China.
Even in groups of organisms and in places that
have been better collected. ke\ elements have often been overlooked. In 1998. our colleague in the
Harvard Herbaria, Gustavo Romero, collected Erismu i,iiniiii Spruce ex Warm. (Voehysiaceae) from
the Isthmus of Pimiehin (belweeu the Orinoco and
\mazori basins) in \enezuela. The lirst collection
of this species from Venezuela had been made
only the year before, from the same area; previously, it was known from a few collections along
the Rio Negro in Colombia and from Brazil. What
makes this remarkable is that Alexander von
Humbolt and \iu
hard Spruce.
Alfred Wallace, Llewelyn Williams, Julian Stey T ii.ii k. Bassett Vlaguire. and others, all worked
here, but none of them collected Erisma japura.
despite the fact that it appears to be the dominant
tree in the non-flooded forests of the area. Individuals range to 35 m in height and over 1 m in
diameter, and have conspicuous u uiged fruits that
are used as a source of starch b\ local people {(,.
ton, was discovered less than 20 wars earlier (Maguire & Ashton, 1977).
Examples like these are surely common, bill are
they really very surprising? After all, one could argue that these are not organisms about which we
thought we ha<
i
i I . gin with. Ila\e
we learned anything really new about the distributions of organisms that we thought we knew well,
organisms of great enough interest that conscious
efforts had been made to find them and establish
their ranges?
Again, the answer is a definitive yes! The most
striking recent case concerns die eoelacanth. IJI
timeria chalumnae. Thought to have been extinct
since the I'ppcr Crela< cons, and of 'great evolutionar\ interest from the standpoint of ihe origin of totrapods, a specimen was caught off the coast of
South Africa in 1938. After an intensive search, a
second specimen was found in 1952 near the Cornoro Islands, northwest of Madagascar (Thomson,
1989). Since then, more than 100 additional speclimns have been taken of ih< now endangered fish
in the vicinity of the Comoro Archipelago, but uowhere else. It therefore came as a great shock
when, on the 30th of July, 1998, a eoelacanth was
caught in a gill-net off the coast of north Sulawesi.
Indonesia, almost 10,000 km away from the Comoros (Erdmann et al, 1998; see note p. 126). Other
populations ma\ exist between the two sites, but in
any case this discovery reminds us how little we
know about the distributions of even large and wellpublicized marine organisms.
Similar lessons are provided by the rediscovery
of species thought to have become extinct in recent
time. Botanists will be aware, for example, of the
rediscovery of Takhtajania perrieri (Capuron) Baranova iK J-K l.erov in northeastern Madagascar,
about 150 km east of the spot where the original
Two other discoveries, also of large neotropical

trees, emphasize that our knowledge of the distribution of many (lades is -till rudimentary, fiupliliocarpon caracolito Hammel & IN. Zamora was described in 1993, primarily on the basis of
collections from Costa Rica's Osa Peninsula (Hammel & Zamora, 1993). Its closest relative appears
lo be h'()i(h)luilr\s {Lepidobotrvacoae) of the Gabon-Cameroon region of Africa. In a similar case.
I'scmloinonolcs tm[icnl>t>sii A. C. I.ondono. E. Alvarez & Forero was described in 1995 from the
Colombian Amazon (Londono et al., 1995). This is
only the second New World species of the otherwise
Old World Dipteroearpaeeae, which dominate the
Iropical forests ol \sia. The othei neotropical species, Pnkumiinacii
I iguire & \sh-
(Schatz el al., 1998). Being of great interest from

the standpoint of angiosperm evolution (as the only
modern African-Madagascar representative of the
vesselless Winteraceae), botanists from the Missouri Botanical Garden and their Malagas) colleagues
had tried in vain since 1974 to relocate Tkht<ij<i
nia. A Malagasy collector stumbled upon a population of over 250 adults while doing inventory
work in 1994, and study material has been made
available to botanists around the world. Molecular
phylogenetic analyses now suggest thai
is the sister group of the rest of the Winteraceae
(E. Ziminer, pers. comm.).
Even better known rediscoveries involve vertebrutes, especially mammals. Again from Madagasear comes the storv of the rediscovery of the greater
Volume 87, Number 1
(Wright, 1988),
which was thought to have become extinct in 1900.
\ II-, m<. anitn il was pun-iuised in a marke! n: \'H,\,
l)Ut -(Hill C-(M|.. '
, I I" I
I 1 Ml i I ' > J
a small population found in the wild. In 1986, two
rxp.diiions, one led by Patricia Wright from the
United States and the other by Bernhard Meier of
Germany, were successful in locating it again. This
set the stage for detailed studies of beh.r. mi
.
ecology, which led in turn to the realization that
there were actually two separate species invoked.
The new species, which they called tin
i<i
I . if
.mui, H. aureus (Meier et al., 1987), appari-nlk -penalizes on new xhools of the bamboo
plant, exceptionally rich in the poison cyanide.
Two fungal examples further emphasize the potentially great importance of such disco\ cries. The
mil . . in N
uxt d< x< nb< d
in 1957 (in the genus Cvstodrrma). was rediscovered in 1992 during the course of systematically
a i| i in
i
iii
I I
ill spin. < hemlock forests on ihe ! !, ::ipie I', nn- il<: < >: \\ i-l in
ton (Redhead et al., 1994). As shown in Figure 3c,
< >
in i
lies were found growing from
the cap of another agaric, a species of Galerina.
This observation provided the crucial clue to the
i il III. i noil of the lifestyle and morphology of an
N
a i
i
|
ei n x \\( i< initially described as having "protoearpie tuber-."
sometimes mysteriously resembling the tissues of
distantly related mushrooms. Owing to the OlympicPeninsula specimens, these structures are now understood to be deformed hosts, and Sijiiam'mitu is
now e< Ognized to be onl) the second agaric genus
in which all species are obligate parasites of other
basidiomycetes.
In 1994, a group of Cornell students taking a
field mycology course in upstate New York encountered unusual fruiting bodies growing out of
the backs of dead beetle larvae. These turned out
to be the ascomycete Cordyceps subsessilis. Propagalion I this material in the laboratory, revealed
it to be the fornn i
i il ti< \ i - u.il st.igi II.-ho
moinl i ,.| -I. mold /<',, . , /,.- /",,..,. :;;/!,I;,,I<, ,n I
produces the imi urn u pi -i
compound cyclosporin, a billion iloJIai <!i ug n.-< d in prev nting ll;rejection of transplanted organs (Hodge et al.,
1996). This knowledge makes possible, for the
What developments do we anticipate wi

spect to geographic ranges? Most obviously.
be critical to contini d <i
i-ui< < n. . Iu<
poor approximation ot the entire

distribution. A critical step will, therefore, be the
development and application of models for estimating real geographic ranges from sets ol collection -ilex. |-OI|I,I n I .i
- nl - have be. n made
in this area with the development of Geographic
Information Systems (GIS) and models such as
those underlying BIOCLIM/BIOMAP, for example
(see Austin, 1998; Scott & Jennings, 1998).
Another exciting prospect entails improved connections between geographic and phylogenetic information. This would not only rev< I ii i I
studv of historical biogeography, but would also
provide a genuinely new perspective on the dislriand managemenl issues (e.g.. Vane Wright et al.,
1991). \lread\ there are concrete examples, involving a range of organisms and spatial scales, for
instance, phylogenetic analyses point to Papua New
(Hibbett & Donoghue, 1996). Analyses in Asteraeeac and eureiilioiiid beetles highlight the significance o| southern temperate regions in relation to
global biodiversity (Morrone et al.. 1996). Similarly,
in the north temperate zone the l'a< ili< Northwest
harbors a varietv ol species of tremendous phylogenetic significance (I). Wake. pers. eomm.). such
frogs (Ford & Cannatella, 1993). Ultimately, we envision a concatenation of databased geographic information (especially predicted ranges along the
lines of BI()(.U\1/m<)\l\['l with databased phylogenelic uiloriiiation (along the lines of TreeBASE). vmong man) other things, this would enable the vvide-scal<- application of phvlogenetic
measures of diversity (e.g.. Williams et al., 1991;
Faith, 1992).
Cox.
. I in
in our already comprehensive

ve have failed, ournumber and significance of recent discoveries is debatable. What is
not debatable is that we have failed to effective!)
deliver news of the
111111:11
\cries to those
outside of our community. As we have suggested,
there are a varictv 1 i - 1 1ii- mcl
1
limited ability to eompdc iiiion:..ii 011 on the 1111111ber of newly discovered species and clades, or to
convey the surprismgness ol n, discoveries. We
also are limited by a system of nomenclali ill
ib
oration of the tree of life. These issues need lo lie
confronted directly, and soon.
In the meantime, there are several avenues
along which we can advance- public awareness and
appreciation of biodiversity. Perhaps most obviously, we can highlight exactly how it is that understanding and piote. IIU bi "I 1 ISI
1- 1 1 1 1
own best interest, even economically. It is hard to
imagine a more compelling statement of this eonnection than the "Teaming with Life" document
prepared recently by the Biodiversity and Ecosysterns Panel of the President's Committee of Advisors on Science ai J ). ,!,,_ (PC AS I ILnei
et al., 1998). Big an b >hl i<
1 . it
I
covery projects .11,
, 1
1 -in to capture
the public's imagination. For example, we see
enormous educational potential in the All Taxa
Biodiversit) Invei
VII
by the Great Smoky Mountains National Park
(vvww.discoverlile.org). Several of the projects to
be sponsored as part of the DIVLRSITAS International Biodiversity Observation Year (IBOY) in
2001 (www.icsu.org/diversitas) have similar pot
tial: for example, retracing key voyages of ]
ages of discovery (by Darwin, Banks, von Hi
boldt, and Wallace). 01 a-s.iiibling an enormous
tree of life and soin 1
'
Hi .1 - .1 1 1- 1
In a fine analysis of the i<-'i

' m _
versity, Kiester (1997) drew attention to the existence of a wide range of biodiversity experiences,
contrasting those centered on the immediate, tangil
i n ties..1 <>l indi\idual organisms with those invoking a sense of the vastness or
power of nature (what Immanuel Kant called "sublime" experiences). It we pa\ olosei attention to
such distinctions, the range of experiences triggered by biodiversity discoveries could siireK be
expanded, and their impact could be far greater on
ie ;,i
ion of nature and the discovery
process itself,
In view of this, we should renew our attention to
how new discoveries are brought forward in natural
history museums and elsewhere. We are delighted
In recent experimentation with museum exhibits.
especially those inspired b\ the "wornlei cabinets"
of the past (Hutchinson, 1965; Weschler, 1995).
I 1 illeelions ol raritiesnatural objects often
commingled with works of art and assembled in
sceiuiiu
I
1
I las uon In |p put the observer slightly, but very constructively, ofI balance. I'erhaps the premier modern experiment of this type is
David Wilson's Museum of Jurassic Technology in
1 1 - \ ... I -
1
w- I ler. 1995). By playIn I -n Ulu 1 1
1 m boundary between reality and fiction. W ilson seems to have hit upon an
unusually successful way of stimulating doubt and
wonder. Today's natural history museums, which
ted certainty or finality about our knowledge of the world, would benelit from careful scrutiny of the Wilson model.
There is great power, we believe, in the mystery
and strangeness of life, and in deeply appreciating
bow little we still kll ow about it. The
nt of bilties no w coming to light ma\ proi ide
alogical 1
the very besl way to tap that power.
grandeur to the public, or launching major intere
Aguinaldo. A. M. A.. J. M. Turbeville, L. S. Linford, M.

C. Rivera. J. R. Carey. R. A. Raff & J. A. Lake. 1997.
Evidence for a elade of nematodes, arthropods, and otli-
ie project of discovering the diversity of life. How-
possibh i
befuddlement
,\ organisms n- pi red dining !.t great age of discovery7 \\ hat is 1
ear-old children \
history museum for the first time? Along these lines
we are encouraged by several recent developments.
-d
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ffljim
3 1753 00300 5409

Flora of the Venezuelan Guayana
Located in the southeastern half of Venezuela, the Venezuelan Guayana is the core i
what has been called "The Lost World." The area is dominated by massive t
known as tepuis and includes many endemic species and genera, with much <>1 the area slill
in pristine condition. There are nearly 10,000 species in the flora area, and over half will be
illustrated by line drawings.
Volume 5 of the Flora of the Venezuelan Guayana is now available from Missouri Botanical
Garden Press:
Berry, P. E., K. Yatskievych, and B. K. Hoist, editors. Flora of the Venezuelan Guayana.
Volume 5, Eriocaulaceae-Lentibulariaceae. 1999. ISBN 0-915279-71-1. 842 pp. 270 genera,
1304 species treated. 707 line drawings. $67.95.
Also available:
Volume 1, Introduction. 1995. ISBN 0-88192-313-3. 320 pp. of text, plus 44 pp. of color
plates, 10 b/w photos, 51 line drawings. $52.95.
Volume 2, Pteridophytes, Spermatophytes (Acanthaceae-Araceae). 1995. ISBN 0-88192-3265. 706 pp. 1285 species treated. 618 line drawings. $67.95.
Volume 3, Araliaceae-Cactaceae. 1997. ISBN 0-915279-46-0. 774 pp. 1113 species treated. 628 line drawings. $67.95.
Volume 4, Caesalpiniaceae-Ericaceae. 1998. ISBN 0-915279-52-5. 799 pp. 1329 species
treated. 621 line drawings. $67.95.
CONTENTS
Symposium of the Missouri Botanical Garden
Introduction to the Symposium
Extremophilic Bacteria and Microbial Diversity
Unraveling the History of Arthropod Biodiversification
Continental Waters
P. Mick Richardson
Michael T. Madigan
Richard ('. Brusca
John G. Lundberg,
Maurice Kottelat, Gerald R. Smith, Melanie L. J. Sliassny & Anthony C. Gill

The Tropical Flora Remains Undercollected
Ghillean T. Prance, llenk Beenije,
What is SignificantThe Wollemi Pine or the Southern Bushes?
Barbara G. Briggs
Holistic Surprises in North America North of Mexico

Barbara Enter
A New Age of Discovery
Michael./. Donoghue & William S. Alverson
Annals
of the
Missouri
Botanical
Garden
2000^
Volume 87
Number 2
Volume 87, N
Spring 2000

contributed from the Missouri Botanical Garden, St. Louis. Papers originating outside the Garden will also be accepted. All manuscripts are peer-reviewed by qualified, independent reviewers. Authors should write the Managing Editor for information concerning arrangements for publishing in the ANNALS. Instructions to Authors
are printed in the back of the last issue of each volume and are also available online
at www.mobot.org (through MBG Press).
Editorial Committee
Editor,
Managing Editor,

Roy E. Gereau
Peter Goldblatt
Gordon McPherson
Aida Kadunic
Senior Secretary
P. Mick Richardson
Henk van der Werff
66044-8897. Subscription p
$130 per volume U.S., $140 (
$165 all other countries. Foi
Volume 87
Number 2
2000
Annals
of the
Missouri
Botanical
Garden
REPRODUCTIVE BIOLOGY
OF ERYTHRINA CRISTA-GALLI
(FABACEAE)1
Leonardo Galetto* Gabriel Bernardello

ne c
v p
'*
; Speroni,*
'iele:' Jofand
'jAlfredo
^ Berdw
L
Gabriela
Argentina and I rugu i

a major burst in No\.
secreted l>\ buds. \\ h n ,ii
u. \ i la <>l Newstrom et al., with

ninant nectar with its
i n
lit
i opened, most (> 50%) of the total nectar was available to pollinators. As
showed that this -p, . i

I
nd-selled ones (autogamy and geilonngam
Who-im.
I nI
- !
.. i .
n i.ni | fruit mass, total seeds
per fruit mass, meai
. <
.
.;
mi
i
||'
"
'
'I
rs set seeds in natural
populations Ibmeiioptt iaiis i< ii|
,m sp,-< i<-s) assiduonsU visittdthe
trees in all the areas sampled and can be assumed pollinators. Almost 93% of recorded flowers were visited by bees,
with the rest visit* d b
, ., .
I
i
.
I
.,
,
i lor the genus and
. lui i< I. n/. d i~piI
lil
I
I iI
i ii I
I
II - 111 lit honed as major
pollinators lliisob- i
.
I i
t pit ,. nt an intermediate step from entomophily
I
il
nl I
I i i M | IMI (. | i
ol / rythrina).
Keywords
hie. In.
I .
I
II.. \u i \ isitors. nectar features, nectary.
Ecological and evolutionary success of the legumcs lias been strongly related to highly successful biotic pollination mechanisms, utilizing mostly
bees, birds, and bats (Kalin Arroyo, 1981; Schrire,

1989). Although much is already known about the
pollination biology of Fabaceae, as indicated by
'This work was supported by funds from CONICKT. CONICOR, ANPCYT, and SECYT (UNC). Two anonymous
reviewers improved pi in
>n . i
n.i
ii|
Ii ill
.
m< u
.1 i "
especially gratelul to
\ictoria Hollowell lot her haul work .is scientific editor on earlv versions of this paper. Carolina Ton.- and Cecilia
Eynard are thanked lor helpful comments on il, ,,
ij
I Nil kindly prepared Figures
! -.i
! In,
. \ ... -. I
lihetl the insects
-'l.isiituto Multidis. ,, I
, ICC.,'
,li
ii,
n
I <X i doba, Argentina,
I ~. ii.l.i .1. II...I. I-.-I.I. IK ( s I v i.,.. Kfsicas v Naturales, Universida.f \. ... .1 ! i nr,loi,a. .".(MM) Cordoba.
Aw. MISSOURI BOT. GARD. 87: 127-145. 2000.
Kalin Arroyo (1981) and Schriie I 1989). then data

are too narrowly lo. used to liable a detail. <l svn
thesis. Thus, we emphasized a thorough analysis of
several aspects of the pollination biology in several
popul tin ii- 1.1 ..ii. I. inline species.
Erythrina crista-galli L. was chosen because this
genus is well known from a number of st in in - !
references following). Erythrina comprises admit
112 species, mostly arborescent and panlropioal.
l.ui also extending into warm-temperate areas, siieli
as Argentina (Krukoff & Barneby, 1974). It is as-lglletl I., [he l.irg. ,. e. . jtlf .1111< ;! 11\ -aginl'i. ai p.lpl
llonoid Iribe Bhascleae lieceiil < pDNA restriction
site anah ses -.! iln> ii i|.i ,u--e~| lh.it F.i ..'/*,'., highly derived (Doyle & Doyle, 1993; Bruneau et
al., 1995). The diversity of floral morphology u ay
be associated *\ illi iliflerei . . - ii pull nation -y -terns (Bruneau, 1997). Among the primarily enlomophilous I'ha-eohae. EiMiutnu is ilypha in he
ing ornithophilous (Neill, 1987; Bruneau, 1997),
providing good examples ol adnptaliui to diilcici i
types of birds (Proctor et al., 1996). It shares with
llici bin I
illn ! groups the red or orange,
rles.s II
i
tar. and diurnal
anthesis (Proctor et al., 1996; Bruneau, 1997). Most
Allierii .Hi -.peel.-, ,n< p, .111 rial. I l-v hi; llll'il re. I -II uld- ..I h id- tend h
be species specific (cf. Bruneau, 1997).
Phylogenetic hypotheses considering morphological and cpMlN A restriction site ebarael. rs -aigg.-si
that shifts from passerine IHMI to hiiiiimmghiid ;.ol
linatioi! ha\e
irrnl s, uial limes in the genus
(Bruneau. 1997) ' .
... ulli is included
in a paraphyleti
Nuith American
species that are basal in the genus (Bruneau &
Doyle, 1993; Bruneau, 1996). Thus, a detailed
study e( til. n pie III! live biology nl till- speeies
may pun ide (dues |o the e\ oluiion ol the pi llin.ii MI
hiologs within the genus.
Erythina crista-galli is native to southern Brazil,
Bolivia. 1'aragnay. I mgiiay. and \rgenl ma as far as
the Rfo de La Plata, having the southernmost distribution (or the genus in the \iucl leas. The species
consists of trees to 10 m tall, with non-tubular,
large, red flowers ol ornamental, economic, and medicinal interest (Burkart, 1987). It is cultivated
throughout the world in frost-free climates (Krukoff
& Barneby, 1974) and is the national flower of Argentina and Uruguay.
Scattered reports arc loun
biology, miiub. t.-;i!.|tiiiL- ibi.il *. i-iti -_ bleeding
system, or nectar chemical compositioi
K :i
1906; Schrottky, 1908; Werth, 1915; Pickens,
1931; Ali, 1932; Fryxell, 1957; Faegri & van der
Pijl, 1971; Ra
1978; Toledo &
1981; I. Baker & H. G. Baker, 1979; H. G. Bak
& I. Baker, 1983, 1990; Neill, 1987, 1988), but
study has been comprehensive. Herein, we addre
tin lol .wing questions lor several |
E. crista-galli, broadly t
flower in relat
(3) What i
(4) What is the secretory pattern, the sugar composition of nectar for a single flower's duration,
yvith respect to the neetai slai ding crop".''
I >! W h ii .- tin ll.-i ill. -; MIS. ! i.e. tni reiui.yal '
(6) What is the breeding system of this species?
(7) Are iheie hint dilb-teiice- produced by the
different pollination treatments-.'
Ileal v
.what
frevisits, and what is tlieir polli-
Fieldwork was conducted

158 adu
itidi\ nlnals In n !. I.I nalur.d p..|iulatini:s and tluei
cultivated ones (Table 1, Fig. 1). Cultivars were
considered because there is high fruit and seed
predation l>\ beetle-. (( airciilionidae, AraptUS SpOTViana, 1965) in natural populations.
curing data. Vouchers for all seven populations
deposited in CORD, UNR, and MVFA (Table
recorded in 1994-1995 for
five of the seven populations (see Results). Data
in. hid. (I pel od- ..I bud pm.iuclii n. majur and ad
ditional flowering events, fruit production, and seed
dispersal. In population ARG-ER1, a detailed
study of 10 tics was performed at the same time.
Flowers from population ARG-ER1 were fixed in
I \.\. !< h\.hated t| rough .m cth\l aleohol/xy lol scries, and cnib. tl\< ! n : latin '. -f ids then aaa
cross and longitudinal views were cut at 10-(Xm
intervals and stained with safranin and astral bin.
(Johansen, 1940). To localize stomata or starch
grains, nectary tissue was cleared with NaOH (10%
aqueous solution), washed with acetic acid : water
(I :3).:
ution (Johansen, 1940). Drawings were
a camera lucida attachment to a Zeiss
I
.; iaph- were taken on a
Volume 87, Number 2

2000
siM hr E
MvT(sur
Population
abbreviation
Galetto et al.
Erythrina crista-galli
" *v - h,,"Md ai CORD (
129
Jaletto), UNR (Vesprini), and
1 , .,1,1.,. -. ,n h, (number of Inrs studied)
Latitude and longitud
ARG-KR1
Argentina. Entre Rfos Province, Dept.

Victoria. Isla Charlie. Golrttn 27-t. Yesprini s.n. (41)
3255'40"S
6036'67"W
ARG-KK2
Argentina. Entre Rfos Province, Dept.

Parana, National Park Pre-I)lta. Galetto s.n. (18)
3205'36"S
604()'48"W
ARG-Chaco
Argentina. Chaco Province, Dept.

Capital, Resistencia, Galetto 382 (7)
273()'03"S
5856'48"W
URU
Uruguay. Dept. Colonia, Balneario

Astilleros, Speroni s.n. (80)
3425'31"S
5733'59"W
CULT-1
Cultivar. Argentina. Cordoba Province,

Dept. Capital, Argiiello, Galetto 381 (3)
3119'12"S
6418'36"W
CULT-2

Dept. Capital. Alta Cordoba. G<detto 79 (2)
3122'12"S
6409'02"W
CULT-3

Dept. Capital. Observatorio. Galetto 380 (7)
3127'00"S
6412'01"W
Vi pb - i - !
.in; Kodak T-max
film, 100 ASA.
Pollen and ovule numbers from 15 randomly
chosen (lowers from population ARG-ER1 were
counted (1 to 3 flowers from seven trees). All ten
anthers belonging lo a snide preuuth- -.d flower
were softened in 1 N HC1 for 12 hours at room
lempemtiiie. transferred to a known volume of lactie acid : glycerin (3 : 1) in a test tube, and mac. The
ated with a glas
tii/e.l using .i vortex mixer, and a samph ol knowi
volume of this -nlutioii was phn ed in a In r:io.w< n
eter. The grains within six randomly chosen senates
were eouriled. and the total niimher of grains per
flower was then calculated. The ovary was directly
dissected under a Zeiss stei.-n miemscnpi are! die
e\ub s counted. Pollen si in ihili'v. :s al mdh a! u
ol pollen viability, was . alrulal.-d walli aniline blue
(1% mass/vol) in 100 grains per flower, corresponding ir sampling lor pollenA . idt
Experimental fnldwork was done from October
to April for three reproductive seasons, 1993 to
1996. In all cases, flowers in bud stage were tagged
for identification. They were bagged using paper
bags to prevent pollinator visits and nectar robbers.
Flower longevity was determined in three populations (ARG-ER1, URU, and CULT-1) for randomly
chosen bagged flowers by following their development until they began to fade.
Nectar was extracted with capillary glass tubes
without removing 'I < llnweis (mm the plant, avoid
ing damage to the nectaries. Two variable
immediately taken: volume (in ud)
micropipettes and sugar
tal mass) with a pocket reft ctometer (Atago, Japan). The amount of sugar produced was expressed
in milligrams and was calculated after Reams and
Inouye (1993). In Table 3, dates, population identification, samples, individuals, and those flowers
analyzed were recorded. St-parali.ni ,i sugars was
by gas chromatography following methodology indicated in Bernardello e al. (1994). Sugai ratio (r)
was calculated as sucrose/fructose + glucose (H.
G. Baker & I. Baker, 1983) and the
(hr) as glucose/fructose. Nectar samp ) for sugar
analysis were colli -led h an tin Ion; anlliesal -âges for flowers, from dilten nl populations, and from
different periods
! - I
ing season. Tests
foi amino at id-. lipids, pin nnh alkaloids. ,u,d reducing acids were also performed on nectar drops
placed on Whatman #1 chromatography paper (H.
G. Baker & I. Baker, 1975). A histidine scale was
used to quantify amino acids (H. G. Baker & I.
Baker, 1975).
Nectar secretion pattern was determined during
one reproductive season (1994-1995) in population
ARG-ER1 (4 trees) and population CULT-1 (3
trees), using eight bagged-flower sets of 5 to 8 flowers in each population. Data were taken once for
each set, allowing the nectar to accumulate until
the measurement. The studied period covered the
perlnrmeil twice a da\ (two untouched new sets
were used each day, at 8:00 and at 19:00 hr re-
i Botanical Garden
ii
Set
ntrol l
yet involved within li< ~ \
HI | I >d) ! i;>. in
order to i-<utip.ii ll . n -i.lt- i inaleU. -eK were
subjected to 1 to 4 measurements according to the
scheme suggested by Torres and Gal. tl
>
Data on the total mg of sugar produced by sets 1
to 4 were compared by a one-way analysis of variance (ANOVA), at the 0.05 significance level.
The standing crop of nectar was evaluated by
measuring aeeimiulaled ne.-tai (volume, eoneeiilration, and mg of sugar in the
I. s< 0 I
I
from individual flowers that had been fully exposed
to (lolliuatoi- h.ita VV.-JC t.ind.niiU e..l|e<-|iil I; mi
open flowers (anthesal stages 3 and 4) from Feb-
i i M it, I I '!,
. utipl n
-even trees (N =
10 flowers/tree) from population ARG-ER1.

Different hand-pollinating treatments were applied to sets of 1- or 2-day-old flowers (N = 1019). Data were taken in population ARG-ER1 (8
trees, 1994-1995/1995-1996), population URU
(13 trees, 1994-1995), and population CULT-1 (3
trees, 1995-1996); the number of flowers used is
included in Tables 5-7. Flowers were treated as
follows: (1) autonomous self-pollination (buds
(lialid-pr.llu
dehisced antln
.gamous crosse
(> ma-ruh.l, .1 !i:u l ; :i||juale,| (I \ers Willi | llei
Volume 87, Number 2

2000
Galetto et al.
,,,a<lKe,
1995.
131
November 1994 to April
Flow.sring (dates/period)
Population
ARG-ER]
Major
Additional
11/02-12/f 11
I i/o;, 11/:'10
12/30-03/11
01/10-03/15
CULT-1 to 3
located at least 200 m awaj I; (5) tests foi apomi (stigmas and anthers were clipped at flower opening), and f>l ofili'iU I||.I^.-I -i I- ,\. :< I nr< d md
left open to flower visitors).
Fruit set was recorded 6 to 7 weeks after treatment with the following features measured: fruit
length and mass, total seed mass per fruit, seed
number, mean seed mass, and percentage <>l seed
germination. Seed samples were plated in I'elri
dishes lined with filter paper and watered regular!\
at room temperature for two months. To obtain the
seed germination percentage, the germinated seeds
v. re mitt : it 1 ividetl by the number of seeds
used. Pre-emergent reproductive success or I'KKS
(Wiens et al., 1987) was calculated as (# of fruits
obtained/* of treated flowers) X (mean # of seeds
per fruit/mean # of ovules per flower).
Flower visitors were identified during 1 to 3 flowering periods (1993-1996) in five populations
(ARG-ER1, ARG-ER2, ARG-Chaco, URU, CULT1) with an average of 49.8 hours of observation per
population. Visit
lected and/or photographed for identification. Relative abundance was
quantified in population ARG-ER1 on one day. The
number of individual visitors and flowers visited
were recorded. The inflorescences were observed
for a total of 7 hr., in 30-min. periods beginning at
06:00. All observe is
111mi a fixed spot
from which 42 flowering branches of three trees
could all be monitored.
Fruit qual
raits \
>
iretl by f-tests or
one-way analyses of variance (ANOVA) combined
with Ronferroni test at P < 0.05. Analogous nonparametric methods (Mann-Whitney, Kruskal-Wallis, and Wilcoxon rank tests) were used .-.!; n th*
assumptions required for parametric methods were
not met (Sokal & Rohlf, 1995). The statistical program package SPSS (1992) was used for these anal-
(daSd)
(dates/period)
12/01-03/11
12/10-04/12
12/20-03/27
01/21-03/11
01/2') 01/12
01/20-03/27
2). \d.|]liniWlll\. to .-I of ;l e trees prevented .'.tie <r

es of lower amplitude in January through March. This second flowering was
very variable among individuals and even among
branches of the same tree. Detailed anabsis on
population ARG-ER1 showed that, although there
is a general sym
ig. ai
seed dispersal periods within each population,
beginning and the peak of II
. '
observed plienologv corresponds to the sub-annual
frequency (lass of Newstrom et al. (1994), with at
least two cycles per year seen in spring and summer. Within the latitudinal boundaries of the study,
this pattern appeared stable, although there were
minor differences among the individuals within a
population (Fig. 2).
Flowers in Et\li,iimi 'nsln^tiih ate resupinate.

red, odorless, diurnally open, lasting for 3 or 4
days. They were bmm n iaccrues (pictured in Fig.
3A) with a mean of 51.67 13.06 flowers per raceme (N = 46, 17 trees, populations ARG-ER1,
ARG-Chaco, CULT-1, CULT-2). Raceme axes are
generally erect, but may be pendulous or intermediat. ill I sili.tn. p' in: ipa l\ !! :bc "We? bi n aeAnthesis proceeds acropetally and, as a result,
there are many open flowers simultaneously in each
The calyces are bowl-shaped and fleshy. The
standard is broad, elliptic, and rigid; the wings are
a- .MII ..[
i
ui
-I
.-I ealed by the calyx, while the keel is falcate and acute at apex.
Anthers and stigma may remain exposed at floral
summit (Figs. 4, 5A). The androecium is pseudomonadelphous with 10 stamens, arranged as 9 longer + 1 shorter. The anthers are dor-it >d id
rutrnrseU dehiscent. The ovary is stipitate and pubesceti Mth a glabrous style and capitate, moist
stigma (Fig. 5A). Flowers average 15.25 1.61
ovules and 878,485 144,770 pollen grains (a
pollen/ovule ratio of 57,605). Pollen viability is
high (96.45% 2.70).
TREE#
NOVEMBER | DECEMBER | JANUARY

2
12
19 26 1
10
17
24 30 7
16 21
| FEBRUARY | MARCH
28 4
11
25
11
Ô-^
2
x7-^
^T-^
-*****
x^Tx
_T_
^-^^
. -
^7^
->
/s.
-=*==
MMM*
^^N
**_*****
******
-,
^-^
Q\
10
r.\
a*********^
*******
,^
*****>
.-.
March IW5). Dots i
Floral ontogeny has been subdivided into four

stages, as illustrated in Figure 4: (1) 4-5-cm preanlliesal l.iiu! reads \n open, with ill. standard on
[il. el
II
Imj; i o ll parts (time: 0
hr); (2) corolla standard beginning to unfold from
its base, initiating the .nillit sis (lirsl dav. time: 3 to
12 hr); (3) fully open flower, 5-6 cm long with standard entireh spread (the device ol spreading ol die
standard is variable, reaching its maximum when it
is perpendicular to the keel; 2nd and 3rd days,
time: 24 to 36 hr); and (4) 3- to 4-day-old flowers
beginning to fade (3id
h 1
time: 36 to 64
hr). Flowers of most populations typically went
through all these stages. However, many flowers
from population ARG-ER1, and
<>n
I |{l . leim.ined in stage 2,
A structural floral nectary is located in the reeeplaele between stamens and ovary (Fig. 5), and
is supplied by vaseulai luui I1 i
-\'\ - I h
ind xylem (Fig. 6). It is a small ring, slightly
divided at the apex into 10 lobules. Histologically.
the external part of the ring is composed ol 10 to
14 layers of secretory tissue with small cells highly
stained. In contrast, the internal ring portion is
composed of 22 to 26 parenchymatous layers with
H. DrhlMVnl IVllil
larger, less slaine.l .Us. an.I ili v.is. ula: |, n,l .(Fig. 6). Stomata are found mainly in the upper part
of the lobules. The basal part of the fused stainmal
filaments delimits a nectariferous chamber where
the exudate accumulates, protected linn
vapora
Flowers produced nectar with a m

entration of 21.8% (Table 3). Nectai
as consistent among the different populatic
sample] (Table 3). Nectar sugars were glucose,

fructose, and sucrose. Mean percentage of sucrose
was lower than 2% or absent, whereas the percentage of hexose sugars was higher than 98%, and
always with more glucose than fructose (Table .'>).
All samples had amino acids in variable concentrations (from traces to 1.9 mg/ml, i.e., 9 in the
histidiiu - le) S
pies from Uruguay (population
URU) had the lowest amount, while the ones from
population ARG-ER1 had the highest (Table 3).
Phenols were always detected, whereas alkaloids,
reducing acids, and lipids were not. In population
CULT-1, we analyzed the sugar composition

throughout the flower lifetime (Table 4). The sugar
proportions data obtained for the different flower
Bfl also si
t flower lifetime (Table
ln-ai.|in.
:{> i.
, 1975). S/(F + G) = sugar

Ratios
PopuU.ion
ARG-ER]
ARG-ER]
ARG-ER 1
\R<; KK2
ARG-ER2
\RG KK2
AGR-Chaco
URL
IRl
I Rli
Cll.T-1
ci 1:1-2
Cl IT-3
Mean of means
Da*
Dec-94
Mai 95
Mar-96
Nov-05
1 )ei-Of)
Jan-W>
Ian 96
Dei 96
.hlll-05
Jan 95
1 ),<-).-,
Jan-96
fcl,-0(,
1 (9)
2(10)
3 il.ii
1 (10)
1 <!.-
1 (7)
1 (22)
1 (10)
1 (IT,)
1 (I")
3(12)
2 (16)
4(17)
US
Cone %
22.0
21.4
19.5
2 1.3
21.5
-*
).2
11
3.3
22.5
""p^'
31.5
41.9
36.0
36.1
36.0
2.8
1.1
1.1
1.0
2.6
30.7 0.7
2.5,1
19.9
'..h7.ir
67.5
58.1
63.8
62.7
64.0
S/
(F + G)
G/F
3.0
1.1
1.0
1.4
2.6
68.4 0.7
69.4 2.7
71.8 ' 2')
23.2 '
19.
21.8
a drier habitat (CULT-1). Most of the total nectar

was secreted by buds. As soon as the flowers
opened, nectar was available l > [i lli 11 11 i~ Fi 7)
Some differences were seen between the flowers of
the two analyzed populations. In population ARGER 1, the flower nectar volume was higher (Fig. 7A),
the nectar concentration lower (Fig. 7B), and accordingly, the amount of sugar secreted by a flower
wiis comparable {V"\. 7(1). Willi respect to nectar
changed with a little decrease at the end of the
flower lifetime in both populations. In contrast,
some differences between the populations were
found for flower nectar volume and sugar mass patterns. In population CULT-1, there was a short neclai 1 css.it 10] 1 1 >. run 1 alter llmv.-f opening which lusted for 12 hours, followed by a new nectar secretion
period on the first night. Only then did the resorption phase begin (Fig. 7A, C). In population ARG-
.2 j 0.3
0
.7 d
1.2
37.3
34.5
40.6
37.1
35.4
1.0
1.5
1.3
1.2
0.9
third day, whereupon a

gan (Fig. 7A, C). The
similar in both populati
ulation ARG-ER1, -0
CULT-1.
1 resorption period be-
Figure 8 shows the amount of sugar produced b

scN subject! iS to dilferenl numht is o| removals 1
the two studied populations. Very little or no nect<
was removed al 1
I
Pals (Fig. 8). One
way ANOVA results indicate that removal had n
significant differences 1
sets (population ARG-ER 1:
61.6 1..
65.9 ()..
57.5 0.<
(.2.0 < 2..
Volume 87, Number 2
open Mowers Sign llleaill I \ differed from di.il ohtiliii( (I from bagged 1- or 2-day-old flowers: volume
(36.4 39.8 and 158.3 36.0, respectively; U =
126.5, P < 0.00001) and milligrams of sugar (7.4
8.6 and 31.1 7.8, respectively; U = 184, P
< 0.00001). However, they did not differ with respect to concentration (17.7 5.8 and 18.3 1.4,
respectively; U = 1543, P = 0.06).
_5
Hand-pollination tests confirmed Erythrina crlsta-galli to be self-compatible (Table 5). Artificial

autogamous (Tosses were more successful ilian g !
pi.I id..n- sin vve : that I
s llian
I'
ol the Mowers sel Iruil in llns way (Table 5). Natural

fruit set was always lower than fruit set from hand
crosses, except for population ARG-ER1 (Table 5).
These legume pods are brown, arcuate, and coriaceous lo siil,in

'i! - an- b\ die Ivvo mat
-ins (Kig. 'Ml*, and presenting I to (> si-rds. The
seeds are brown molded with black, dry, and hard.
In spite of low natural fruit set (< 6%, Table 5),
individuals oltcn vielded thousands of seeds because of die large number of both flowers produced
pei plant, and seeds produced per fruit (Table 6).
Fruit set obtained bv geitonogamous hand-pollination was the lowest and significantly different
IIOIII autogamous hard-pollination, but not from
fruit set obtained by hand cross-pollination (Table
6). Reproductive success for
c 4
population CULT-1: F|:, ,,,, = 0.45, P = 0.13).

itly, there were no significant differences
lation level (t = 1.36, P = 0.18).
Howe. ,,,, iage . ilu. - <'
I-- -la
:KIIU:
eatments were not significant. Fruits c

lained bv hand-pollinatio
lation CULT-1 were con
(Table 6). All variables s
ences. exeepl tor seed number per fruit. Highest
value- toi Iruil Length and mass, seed number and
seed mass pei Iruil.
an seed mass, and s< d germination percentage were observed in xenogamous
fruits and seeds (Table 6). In contrast, the lowest
mean seed mass and the lowest soil g
-
- i- ]
were obtained on seven trees from population ARGER1. One-way ANOVA comparisons showed no
significant differences among lire sampled trees ling
of nectar sugars: P|(, :| = 0.79, P = 0.58; nectar
volume: F, 117| = 0.24, P - 0.96). Nectar data from
mass, seed number and seed mass per fruit, mean

seed mass, and seed germination percentage (Table
7). Fruits from cultivated trees (populations CULT1 to 3) showed the highest values for most variables
id
30
TI
.2 25 j
- -
2" 15-j
Population
CULT-1
I!
ARG-ERI
Flower sets (# of nectar removals performed)

Kipuiv H.
His
'
Mil
Vrgentiiia. Knlre Kios.
er
and seed mass per fruit, mean
ed
l percentage; Table 7).
Germination
tion percentages of seeds from open-pol
lar to those obtained for exfruits, but were consider,e of geitonogamous and
les 6
'
)-
Aiuiii.tis visiting the flowers for nectai

umented only during daylight hours. Visi
: Cl'IT-l = \i
M-M II ..
menopterans and hummingbirds consistently

ed the populations of these trees in most o
areas sampled (Table 8, Fig. 9B-H). The r
...... ... .- ...r~
bees (Xylocopa nigrocincta, Fig. 9C, X. ordinaria, Fig. 9D, and othei
Xylocopa) as well as honeybees {Apis mellifera, Fig.
9G, H). Four species of hummingbirds were noted
(Table 8), with Hylocharis chrysura and Chlorostil
bon aureoventris (Fig. 9B) most frequently observed
One species of perching birds (the epaulet oriole
Emberizidae, Icterus cayanensis, Fig. 9A) was oc
butterflies, wasps, ants, and beetles were occ
or during the heat of midday (> 30C). Hy-
Table 5.
ally seen as incidental
visitors (Table 8).
Fruit sets
3.308 (120)
1100(80)
).1<>7 (7(>)
3.014 (145)
3.132 (1245)
0.139 (323)
0.05(1121')!
;,,,.r
(1_W{J,
0.008 (597)
0.054 (4102)
Volume 87, Number 2

2000
Galetto et al.
139
dp_sfrom
Table 6. Reproductive succe sand fruit and see

ifferenthand-ollinatio n treatments in E crista
galli from population CULT-1. E
ccess, data are means
ori test results. Reproductive success = (# of fruits obtained/* of treated llowersl '
(mean # of seeds per fruit/mean # of ovules per flov er), n, - no! sign ficant, ** = P < 0.01 *** = p < o.OOl.
Variable
Fruit set (flowers treated)
1-1 nil length (cm)
Fruit mass (g)
Total seeds per fruit mass (g)
Ovule number
Reproductive success
Autogamy
0.308" (120)
17.8 2.91.2 0.615.1 2.0
0.092
Geitonogamy
0.1001'
14.4
2.2
1.1
(80)
3.5''
1.0"
0.6-
3.3 1.6
33.4 11.3''
88.2 * 12.0'
0.023
Monkeys (Cebidae, Allouata caraya) were observed

in population AGR-Chaco breaking and eating
flowers. Although destructive, these actions may
produce some accidental pollinations.
ed only for popula
Visit.
tion ARG-ER1. Almost 93% of the flowers registered were visited by hymenopterans (42.9 and
49.9% for honeybees and carpenter bees, respectively) with the remainder by hummingbirds
(7.2%). Considering flower number of a tree visited
by a single individual, carpenter bees and hummingbirds averaged a mean of 5 flowers per tree
(4.7 2.9 and 5.0 2.5, respectively). By conaging over 21 flowers per tree (21.3 7.5).
Hummingbirds and bees can be con-: l
fective pollinators, be. a i > the) contacted both anthers and stigma while taking nectar (Fig. 9B-G).
However, we did not compare their effectiveness.
Regardless of the flower visitor, the average time
elapsed in each visit was 10 to 30 seconds per
flower (range: 1-50 seconds). They usually visited
many open flowers of several inflorescences in each
tree before going to the next one. The remaining
Xenogamy
0.197-'' (76)
22.8 1.94.3 0.6'
2.0 0.7''
5.9 2.1
34.2 10.1''
93.3 7.2^
0.087
Statistical tests
= 10.76**
= 13.39***
Fp
Wl]
/'\,
HI
hv
F
=
, =
16| =
%1 =
F 1B1 =
v
X* =
F
v
h]
4.79**
1-73 ns
3.12 ns
6.08**
12.58***
4.38 ns
contact both fertile whorls due to their small size.

In population ARG-ER1, holes made by unknown
primary nectar robbers were detected; these holes
were used by small wasps to take nectar.
C
Our
<l>ser\aliims indicate that hummingbirds
wer
were
widespread visitors while orioles were rare
an(j local, but bees were even more frequent than
and
nun
imingbirds. Hummingbirds usually foraged in

^
upper branches of the trees, taking nectar by
inserting their bill between the standard and keel
while hiijefiin^ aitlhi rs and stigma with ihcir Iliads
(Fig. 9B). Chlorostilbon aureoventris showed territorial behavior in population ARG-ER2.
Carpenter bees displayed a particular behavior
recorded for all populations of E. crista-galli. They
usually forced open preanthesal flowers (stage 2,
Fig. 4) with their proboscide. This \va-
- .: Iicance in the flowers of populations ARG-ER1 and
LRU that did not display natural flower opening.
When these insects visited the flowers, they first
opened them in..vnii; downward between the standard and tin keel. I hen, while looking for the nee-
18.0 t 3.0"1'
2.9 t 1.0
t 0.7
4.5 _ 1.8'
38.5 _ 8.1
52.1
15.0
F|2 io7
-;
= 7.16**
= 5.6***
=
=
=
t =
-4.3*
12.23*
52.63*
2.79**
ole \h,rrus rnvnnensi* (Viellot)] Iron, population \K(,-KU2. / & Ul'resnayc)| Iron, population CUI.T-I. C. Carpenter bee
I), Carpenter lur (Were/,,/ tmluiuna Smillil from p. >| in Lit ii >n
. respectively. The 1-cm bar in C is valid forC-C. Abbreviations: \\\(,Y\VZ
I I I I I
they touched the anthers and t

r hack. Iniiislc r lin^, llic pollen.
llifera (Fig. 9G, H) was c >. of the i]
isitors in all the ;
in peak blooming. They occasionally Ion
thesal flowers. Honeybees arc id. onl\ pollinalois
that collected pollen, in addition to nectar. numb
early in the morning from 7:00 to 9:00 hr. Landing
on the apex of the androecium. they collected pollen, moving around the anthers and touching the
stigma with their pollen-laden In ail- and lor. \tn(Fig. 9G). Then, they moved downward in the (lower
\r.'ntina.
[)is< I
The Mowers ol Et\thrimt <iistu gtdli present a
nectars l\pe eliaraelerislic ol I'apilionoidcac (e.g..
Fahn, 1979; Davis et al., 1988, and references
therein). Net tar secretion possibly occurs via the
niodilied -loniala ol the no. iar\ through which nee
lai Hows. The pic-en.< ..I -idinata is a common
feature ol Moral nectaries of legumes (Davis et al.,
Table 8.
Flow. >r visitors observed at E. crista-gaUi during t he day.

Population
Visittors
Hours (days)
ARG-ER2
ARG-ER1
18(6)
7(1)
CUIT-l
URU
44(11)
4(2)
L0.5 C !)
60 (10)
18 (6)
<in>rl.r.,n>, X Liln-siuive)
Hylocharis chrysura (Shaw)
llchi,i:m>tr! furriji'i iShaw )
/. ,< , , hh <<
tilhi . ''
( v i
II.
Brachygastra lecheguana I
Vespoidea (n" species)
Muscidae (n" species)

Syrphidae (n" species)
Studies on the nec-
ered (2245'S, 4825'W; cf. Gottsberger et al.,
tary stomata of Viciafaba L. demonstrated thai theii

m,i|<-r luru-ticri- -.-.in li. I" tlm-e "t as-h'1! J m i r
escape from llir ghnid and perhaps enhancing re-
1984).
With respect to nectar secretion pattern, there
were some ditlereuces between the analyzed populations. Habitats are assumed to play a role in the
dil'iereiK-es found in nectar secretion between the
]')
I i
..
al.scirptii n of uncollected nectar (Davis & Gunning,

1993). Erythrina rnsta-galli secreted dilute and
hexose-dominant nectar, with a remarkable constancy in its sugar proportions within the sampled
area. Nevertheless, when comparing our data with
previous studies, some differences appear in the
nectar sugar composition. I. Baker and H. G. Baker
(1979) noted traces of melezitose and maltose,
whereas Gottsberger et al. (1984) found a much
higher amount of sucrose (ca. 45%). This would
indicate that the - soim mtiaspecific variation in
nectar sugar proportions, particularly when data
from the northern Brazilian population are consid-
populations, since trees from Entre Rfos (population ARG-ER1) live near the Parana river, a more
humid habitat than that of trees from C6rdoba (population CULT-1). The fact of presenting most nectar
at flower opening is unusual and unknown for other
Erythrina species. As far as we know, it had been
recorded only for some Indian bird-pollinated Loranthaceae (Davidar, 1983) and for the South American bee-pollinated Mandevilla pentlandiana (A.
DC.) Woodson (Apocynaceae, Torres & Galetto,
1998). On the other hand, the observed decrease
in nectar volume and solute in 3-day-ol

Mowers can be inferred as resorption, based upon
tbe constancy of nectar concentration throughout
anthesis. Then' are some species of other families
wilh Mowers that last 4 days, with a similar neclar
-i i n I
t< sorp i [i i i
i
in. Ii ire visited
by a great varictv of flower visitors (Combretaceae:
Ucmanlello " I
1(><H: I.oiaritliaceae: Rivera et
al., 1996; Apocynaceae: Torres & Galetto, 1998).
Most previous data on E. crista-galli report or
suggest bird pollination, cither b\ Inmiii in.: nl(Knuth, 1906; Schrottky, 1908; Werth, 1915; Pickens, 1931; Ali, 1932; Gottsberger et al., 1984) or
bv hummingbirds and passerine birds (Toledo,
1974; I. Baker & H. G. Baker, 1982; H. G. Baker
& I. Baker, 1983, 1990). In particular, orioles have
been IrequeiitK re, orded as visitors anil pollmaloi..I Ei \ll,!i'i,i -pe. ii - Iron ill. \mci icas i [t i>in; a
et al., 1979; Morton, 1979; Toledo & Hernandez,
1979). In contrast, Hymenopterans have been rarely mentioned as possible visitors for the genus (Toledo & Hernandez, 1979) or for E. crista-galli (Ali,
1932; Faegri & van der Pijl, 1971; Duncan in Raven, 1974; Parodi, 1978). Monkeys have been reported elsewhere as visitors in a few New World
El >!;;; I ,\.i fie^ci I ! (>M I saw how lllli; inotikevon Erytlinna species from I'aragu.i), and Janson el
I 1 !*>:;; i indie .[ .1 Ii.i ill! v,n> ol two specie- trom
Peruvian forests were an important tood source lotStudies on Mowers and their animal visitors have
led to the assumption that there are revolutionary
ili
' ipa between nectar trails and | ; in totvpe. Seveial an! iors luxe d
i - In la:
I n M
and concentration of flowers attracting dilleretil
guilds of pollinators. In general, they
lininniiiivbiid , nd h .i;, v< ; I. : doners present huge
.en: nnl if dilute nectar, especia ll\ relative |o nectars of bee flowers (e.g., Baker, 1975; Pyke & Waser, 1981, and references therein; Cruden et al.,
1983; Opler, 1983). Nevertheless, and under laboiaroi v . on lilion-. in.ini iin:d>uds. honevealers. anil
I
i
iven a eh.nee of sugar solutions have
been found to prefer the highest sugar concentrations offered at an equal volume presentation
(Hainsworth & Wolf, 1976; Stiles, 1976; Tamm &
Gass, 1986; Mitchell & Paton, 1990). On the other
hand, studies on the sugar composition of nectar
showed that humn.iruJ'ird tleweis produce a slides, -dominated m elai while those associah d wild
passerine birds produce nectar dominated b\ glucose and fructose (H. G. Baker & I. Baker, 1983,
|wuO). ~-iia,.u prel.rciices ol hummingbirds bave
been examined in previous studies, which have
found that they preferred sucrose solutions instead
ol equivalent inonosaci Ii illdi solutions (Stiles.

1976; Martinez del Rfo, 1990a; Stromberg & Johnsen, 1990). Physiological studies on New World
nectarivorous passerine birds have shown a correlation between the sucrose aversion with
relative
. lack of suerase activity (Martinez lei liio
et al, 1988, 1989; Martinez del Rio, 1990b). However, recent studies >u Old Wodd passerine birds
have shown that tln\ possess lnli efficiency in sucrose absorption, and Old World counterparts do
not reject suen.se m tavoi of he\ose sugars (Downs
& Perrin, 1996; Lotz & Nicolson, 1996; Downs,
1997a, b).
In addition to nectar traits, red flowers can be
largcK considered as bird-adapted because insects
have little or no sensibility to red (e.g., Proctor et
al., 1996; Vogel, 1996). However, recent literature
ILL. N that red flowers are not invisible to bees
as previously thought (Chittka & Waser, 1997). In
particular, for Papilionoideae a conspicuous UV reflectance/absorbance patterning was den
1
n>i mellitophilous sp< cies b ii n< I for ornithophilous
ones (Kay, 1987). Because flowers of E. crista-galli
lack UV patterns and showed little or no UV reflectance (Kay, 1987), red flowers of this species
should be seen not only by hummingbirds but also
b\ carpenter bees, the most frequent Mown visitor.
The two woody subfamilies Caesalpinioideae and
Miinosoideae and primitive woody tribes of the
I'apil .mi d. i" ha\ i II - ; -II ml,in . d - It-im < m1
bilitv has been
(Kalin Arroyo, 1981). It is possible that its loss

occurred as a consequence of the peeuh i in ol
tripping in papilionoid flowers, because this meclioutcrossiiiii in many self-compatible legumes
Arroyo, 1981). Nevertheless, the level of oi
ing will be primarily correlated with the
flower display, enhancing the possibilities
k:.lii
mi. -'i - Il II- w II sail !t..tu nil.-: How. i is.is -I. :ence of pollen.
Previous data on some species indicate that both
. ilibility are present in Erythnna (cf. Kalin Arroyo, 1981; Neill,
1988). According to Fryxell (1957), E. crista-galli
is self-incompatible, but later reports (Raven, 1974;
Neill, 1988), confirmed herein, indicated that it is
i
i bl,
Wording to Cruden and Lyon
(1989), facultatively xenogamous species are self. ompalibl. . ..dap', d lot . .-- pi .lluulioii. pie-eulin
ii,
i
iyed autogamy, and
most show h < h Inn! ; ml -', d --i f'acullath e \c
iiaânn - < . nsiden : mixed mating nsh m in
which the level <: pollinator activity is the primary

pollination (Cruden & Lyon, 1989). Facultative xenogamy has been correlated with a moderately high
pollen/ovule ratio (i.e., ca. 700; Cruden, 1977). Although E. crista-galli presented a pollen/ tvule c iti<
(> 57,000) that coincides with Cruden's (1977)
class lor obligate xenogamy. we considered this
species ,l- I... ...
.- because il 1self-compatible, the flowers are adapted for crosspolhl IM .11. I.I1 .ill ) llll . I l.i h \ li I
I I ll .
reseenee size .ill
-In
h
11 i i
< in i
my). Empirical evidence suggests that numerous
plant species have evolved a mixed reproductive
strategy (Richards, 1997). An evolutionarily stable
s!raVg\ eari slevi [up I'm mi < <l mating, because selling as well as outcrossing can confer fitness benefits
onto offspring (Holsinger, 1991).
Pollinators pre!
il
rgc inflorescences because they provide a larger signal to attract
lli.-tn aml/.H .-ilei uit .itei ].ell. n an.) neelar reuaub
(e.g., Stephenson, 1979; Augspurger, 1980). When
a plant displays numerous flowers simultaneous,
geifonogamv ma\ ...nil il lln pollinator moves between flowers. Although plant attractiveness to pollinators often increases with the number of flowers
open at one time, display size also bears mating
costs to the plant '
il design and display that mitigate the mating costs of autogamy but
thai plollMli tin bell.Ills of .llli.i:i.-e.| pol m il ,i il
traction may be widespread, given that most auinia pollinate plant displ.n
.- tal to many flowers each day (Harder & Barrett, 1996). Some
l< dm tions on the E. crista-galli reproductive strategy can be made when fruit set as well as fruit and
seed parameters from hand- and natural-pollinations are compared, particularly when these results
are related to mHoreseenee size, to the number of
ni-.lv open flowers per tree, and to the
foraging behavior of the flower visitors. The possibibl
' . .
i lining natural selfing would
explain the low natural fruit set and low seed germinability observed in E. crista-galli. That quanural pollination are more similar to those from
selfed flowers than from crossed ones can be related to significant pollen flow within a tree mediated
by the flower visitors. Results indicate that E. crista i ..'.'- show , K p' id i HI
|.l iilv. which allows
this species to reproduce successfully despite variation in the quality and quantity of the pollinator
guild.
Cladistic analyses of Erythrina based on morpholo
I and cpDNA characters suggest that E.
and lies sister to
Hi. remaining .-p.-< 'M> uiUuii ill. germ - i limn. ,m

1996, 1997). Within the primarily entomophilous
tribe Phaseoleae, there is some agreement that Erythrina is bird-pollinated (Raven, 1974, 1977; Bruneau, 1997). Most Erythrina species in the Americas are pollinated by hummingbirds, although
p. May lards an also oiiiiaoii \ isilors and pollinators of several taxa (Neill, 1987; Bruneau,
1997). In an article on the coevolution of birds with
Erythrina (Bruneau, 1997), E. crista-galli was included within a basal clade with E. fusca Lour, and
E. falcata Benth. with this clade characterized as
. hummingbird-pollinated. However, for E.

crista-galli, we observed not only birds, but also
bees as significant visitors and pollinators.
CONCLUSIONS
Erythrina crista-galli, like the other species in

the germs (Nell
I 1
I
low fecundity and high rates of flower and fruit
abortion. Its showy red flowers produce hexosedominant nectar and are assiduously visited primarily by hymenoplerans (carpenter bees and honeybees) and also by hummingbirds (four species),
all of which can be assumed as pollinators. In natural populations, several traits related to pollinator
behavior, e.g., high number of simultaneously open
flowers per tree, high nectar production per flower,
would favor pollen flow within trees. If this is true,
a reproductive consequence such as inbreeding depression could oe. in. An outcome of this situation
might be the low quality of selfed seeds compared
to seeds derived from outcrossed flowers.
Knowledge of directional changes in pollination
and breeding systems can provide valuable clues
for reconstructing phylogenies (Kalin Arroyo,
1981). As the genus Erythrina seems to be wholly
self-compatible (Neill, 1988), information on shifts
in pollinators may be valuable. This highly derived
genus was pre\n.ii-|\ considered to be ornithophilous within the primarily entomophilous Phaseoleae
(Doyle & Doyle, 1993; Bruneau et al., 1995). Cladistic analyses in Erythrina included E. crista-galli
in the basal clade (Bruneau, 1997). However, our
data indicate that flowers were primarily visited by
bees. This may indicate that the pollinators for this
basal clade have departed from entomophily, typical of Phaseoleae, to ornithophily, more typical of
Erythrina. Further studies on the reproductive biology and frequency of visitors are needed on the
other members of this basal Erythrina clade for
confirmation of this. Our results suggest that the
P -I
i I
I
sp. eies is i omplex, that the species have a wide array of visitors.
and that
mor.
d u
, .
clarity their evolution.
l<>
ip . I
> Mm m .1 mi-ll. I
32-37.
Davjs
&
,,
(;imning
stomata of the llui.il nectars ul

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enng plants. Oecologia 71: 501-509.
THE LONG-PROBOSCID FLY

POLLINATION SYSTEM IN
SOUTHERN AFRICA1
Peter Goldblatt* and John C. Manning*
ABSTRACT
Some 14 species of long-proboscid III.- (Dipt.-ml in two families. \emesli inidae and laliaiudae. with elongated
mouth parts are known to pollinate specie. j several plant families most uupuilaiith (-eraniaeeae, Iridaceae. and
Orehidaceae, across southern Africa. Uong-proho- id h ;.o!lin |i. n appears to comprise three discrete guilds nl Hies
in the genera Prosoeca, Moegistorhynchus, and Stenobasipteron (Nemestrinidae) and Philoliche (Tabanidae). Flies in the
three guilds are on the wing at different limes nl the \c.u and pollinate diller.-nl suites ol plant species, sometimes
with different Moral characteristics. I lie three pollinator guilds operate loi the most part in different parts of the
subcontinent. Where there is geographical overlap, the periods of activity differ. Plants pollinated by long-proboscid
flies have flowers with an elongate, cylindrical Moral inhe. niostb ?,?, <>() cm long, a perianth of specific colors and
marking, a floral reward of nectar, and lack floral fragrance. Pollen is not eaten l,\ these Hies, and anthers and pollen
are often crypliealh colored, flowers arc usually zygomorphie and bilabiate, and the petal or tepal lobes have charaeieristically shaped nectar guides. Willi lew exceptions, the flowers offer ample nectar of sugar concentration iiiainb
and pollination is i
I
i
n ' l.nal miniii r\ and dc< eption. In long-proboscid fly pollination systems, placement of pollen on the insect's hods is highh specific, and there are at least si\ mutually exclusive sites of (>ollen
deposition on an insect's body. When two or more long-proboscid-fly-pollinated plant species co-occur, each typically
and that differential pollen deposition sites ate important lor pi,mis pollinated by long-proboscid flies. Since these flies
are the sole or main pollinators ol al least 120 plant species and the inferred pollinators of at least 80 more species
in southern Africa, they must be considered keystone species in the ecosystems where they occur.
Key words: co-evolutmi
. I
I.
.
, n I
us. pollination.
\ (lose assficialie.ii between die form ;unl e..|or

of flowers and polli
Iweei the sal\i I lniM-rlU. {<;.<;;,:\ {.Veneris) ml

nug aperies with
is well known. ( or
among species th.it rely on the same pollinator class
led to the recognition of floral syndromes (e.g., Vogel, 1954; Faegri o,
i
'
species with moq (
share the same pollinator species constitute a pari ation guild, an extension of the term
loii ili. same
class of resources in a similar way (Root, 1967).
Likewise, insect species using a particular group of
plants as a food resource in a similar way may ilso
be regarded as a guild. A guild is thus a functional
unit independent of taxonomie considerations, as
are floral syndromes. Although a number of pollination syndromes have been identified in the southern Vlnc.ui lloia (\
i
have been described. The most sinking of those
that have been documented is the association be-
I
-<>n & Bond, 1994).
Others in< huh lln
. i.itiei .l several plant species with magenta to violet-colored flowers and the
t
ung & Goldblatt,
ml. ol pi nil s(
willi cream to pale
pink flowers blooming in autumn that depend on P.
/<<
(Manning & Goldblatt, 1995), and the Moegistorhynchus longirostris
guild of the west coast of South Africa.
Pollination by long-proboscid flies is a relatively
i
n
ti
i I in southern Alrica by Marlotb (1908) and later described in somewhat more detail by Vogel (1954). In their review
of insect pollination in the Cape Flora of South Africa, Whitehead et al. (1987) were the first to really
mation as a unique
pollination system, although very little was then
known about either the flies or what plant species
1
This research was supported l,\ National Geographic Society Grants 4H1(V<>2. 5408-95. and 5994-97. We grateliilb acknowledge the work ol M.-K. van Wvk. band Alrikaans I Diversity. Johannesburg, who provided the analyses of
sugar nectars. We also thank Peter Bernhardt and Dee Patersou-Jonos l, helpful comments .luring the preparation of
the papei. and Vlervyn bolter and Cameron and Rhoda MoMaster for their help and hospitality in the field.
2
B. A. Krukoff Curator of Africa- I!.. m<. \b .
I'.ei meal Ganl.vi. I'.O Box 2'"*. SI. loiiis. Missouri OiJWiO0229, U.S.A.
3
Compton Herbarium. National botanical Institute. Private bag \7. Claremout 7735. South Africa.
87: 146-170. 2000.
the\ pollinated. Thus. l()ii^,-|>r()!)osci(l !lv pollination

has only been regarded as a class of pollination
system comparable with that of the major pollinator
groups or syndromes, bird, bat, bee, butterfly, and
in on fly, since the late 1980s Muscid/
carrion fly pollination, also called myophily, is claslnc. bowl- or salver-shaped flowers of pale or dull colors, readily
accessible nectar, and well exposed sex organs
(Faegri & van der Pijl, 1979). Pollination by Diptera is, in fact, diverse and cannot be usefully re-i..n '!< <l i- i -11 JJ< pollmiiior -\ -nil < if ' I" r
myophily is already distinguished from general
myophily because the flies in the syndrome have
;of do
with flow t> ith ill col i-s (,. ii with mottled pigmentation, and hairy or frilled petals or tepals.
Long-proboscid fly pollination (or rhinomyophily,
viz. Rebelo et al., 1985) may readily be distinguished from classical myophily and its sp.-( . li . il
derivative, sapromyophily, and differs in all criteria
enumerated by Faegri and van der Pijl for this myophily. Long-proboscid fly flowers are typicall) zygomorphic, normally have an elongate floral tube,
and have bright coloration. The s
sented in a wide range
concealed within or above the mouth of the tube,
or are elongate and held distant from the source of
the nectar reward in a unilateral, arcuate (adaxial)
ed to the Himalayan Region (Fletcher & Son, 1931; Dierl,

1968) and southern Africa, where the system has
received a fair amount of attention since 1990 (e.g.,
Goldblatt et al., 1995; Manning & Goldblatt, 1996,
1997; Johnson & Steiner, 1995, 1997). So-called
lon^-prol
I II
II i
i I
i 11. <l in tin lit
erature, for example, by Grant and Grant (1965) in
California, refers to bombyliid flies with probosces
less than 15 mm long and differs from the pollination system we regard as long-proboscid fly pollination. Here we review long-proboscid IK pollination, report additional examples
I nation
long-proboscid flies, and assess the importance of
the system in the southern African flora relative to
other pollination systems.
REVIEW OF LONG-PROBOSCID FLY POLLINATION
H-- itin il li i\i i loiiih p.irts ii least 15 mm long

and a body length of more than 15 mm. Fifteen
species in two families, Nemestrinidae and Tabanidae, are known to have mouth parts this long, 14
of them restricted to the southern African region,
Lesotho, Namibia, South Africa, and Swaziland
(Fig. 1, Table 1), and one to the Himalayas (Dierl,
1968). Adult morphs of these flies depend largely
or exclusively on floral nectar for their nutrition and
are avid foragers of nectar-rich flowers (female Tabanidae also require a blood meal). Their visits to
the flowers of some plants result in the passive accumulation of pollen or pollinaria as they brush
against anthers, and in turn, the passive traasfei
ence of pollen or pollinaria to stigmas during visits
to other flowers of the same species. Most other
Nemestrinidae and Tabanidae have substantially
shorter mouth parts and, although they also feed on
nectar and pollinate plants, they are not known to
be the only pollinator(s) of any plants. Instead they
share pollen resources with other insect taxa including long-tongued bees, Lepidoptera, hopbine
beetles, and bee flies (Bombyliidae) (Goldblatt et
al., 1995, 1998b, in prep.). The tabanid, Philoliche
aethiopica, and the acrocerid flies, Psilodera
i
(Goldblatt et al., 1997; Potgieter et al., 1999), have
gth, mostly 12-15
mm long, and they are provisionally exclude d from
consideration here: their shorter mouthparts prevent them from foraging effectively on flowers of
plant species that have exclusively long-proboscid
fly pollinators.
Long-proboscid flies are large-bodied insects,
typically measuring 15-24 mm from the tip of the
abdomen to the I
scis. Mouth parts
are as long as, or often substantially longer than,
tin' insect's body, the most extreme exam < I
u
Moegistorhynchus longirostrisindividuals along
the Cape west coast have been recorded with probosces up to 100 mm long (Fig. 2). Foraging behavior is similar in all species, irrespective of family or genus, and although flies have been described
as hovering while foraging (Struck. 1907). tins is
not the usual pattern. Our observations show that
flies firmly grasp tepal or petal lobes or other floral
organs as they forage for nectar and while doing so
they continue to vibrate the i l irings
: U (Gold
blatt et al., 1995; Goldblatt & Manning, 1999) (Fig.
3A-D).
Foraging patterns vary, but our observations
show that long-proboscid flies are seldom flower
on a particular floral form and may visit a particular
species more frequently than any other, more often
their foraging appears to be random, and foraging
26
28
30
32
34
:J::::iri:::lS
W -' *
j4 2315 23,6 23,,
?3,8
23*. U * Mte K*3
rftm
1. The f'rosacea pcringiieyi guild. 2. The
liUumm guild. The ranges of guilds 1 and 2 c
bouts may inchu

cies, some of which CVIMI have different shapes, siz<-s. and i-ulurs. Tins emphasizes llial long prnl -., . :
flies can and do U w on i w I. i ,i j> d -1 m .Long-tubed flowers, however, are the only ones that
oiler a secure reward, and because of their size, a
-'. ii a tly larger reward, and one that is not
ailhwesleni Cape.
Plants that depend on long-proboscid flies for
/one. which e..v. is Ih ivsl ol llh subcutllmenl (big

1). Prosoeca gm,.
widest range and
extends from the Northern Province of South Africa
I in. _!, islern southern Africa to the Kleinswartberg in the south (at the interior edge of the winlerrainfall zone), a distance of over 1500 km. In contrast, and di spiti | lin in i
arch in the area,
P. rubicunda is known from one specimen from the
southwestern Cape, while P. nitidula is restricted
to the Cape Peninsula at the extreme southwestern
ically and morphologically (Table 2). They range

from seasonal perennials, mostly gcoph
,itl
conns, bulbs, or tubers (Amar> llidaceae. Iridaeeae.
Orchidaceae, some Geraniaceae), to shrubs i Ericaceae, some Geraniaceae, Lamiaceae, Scrophulariaceae). No annuals or trees have so far been found
Floral characteristics. Flowers of most species

have in common a long floral tube (Figs. 4, 5) (we
use the term here to include a corolla or perianth
tube, tepal spurs of orchids, as well as the recepi. < il. i Lib. o! /', ',/'_-,.,. .II, I. 1-... lb . M-irilinp 20
nun. and asnalh produee ample r. ciat Notable exceptions are Arisl
,
| Inda eae) and species
I laeeae). whit h
Proboscis length, peak n
ii
cunda that its inclusion in the \h>,

<!:< guild is tentative
Moegistorhvnihus. Prosoeca. Stonobasipterou: T;]li;uiid;ie I'hilolirln: WRZ
rainfall zone. *Note tli.ll v\e nvai I 1(' , -.;, ,< ml 1/ ;>-.-/I/VW/N ir.ich km
Proboscis length
MI,:
Months on
12.. lo ii:>i
WRZ: Northern Cape (Cal\inia Disi
Moegistorhynchus-Philolic
\\ KZ: Western and Northern Cape e
M. sp. nov.
PI,Hotirhe gutosa
P. rubicunda
ca. 21
liS-M
21-27
18-28
ea. 21
(1)
('
(7}
(.r>)
(1)
WRZ: Western Cape

WRZ: Western Cape, mainly interior
\\ KZ: Western Cape, coast and interior
WRZ Western Cape (only Cape Peninsula)
WRZ: Western Cape (only Caledon District)
[an
Sep.
Oct,
Jan.
Prosoeca ganglbaueri gu ild

P. ganglbaueri
(17-)25-42 (12)
Jan, -Apr.
P. InngitM-nms
;; M) ci
20-46 (7)
18-30 (5)
Mar. -Apr.
Pel,. -Apr.
Feb. -Apr.
Stenobasipteron wiedm,mnii
have floral tubes lessi than 10 mm long.

with short floral tubes have elongate stamen s so that
Flower colors fall into two major groups (Goldblatt et al., 1995; Manning & Goldblatt. !'>,.
1997). In northern Western Cape Province and Namaqualand flowers are typically intensely dark red
to purple or vioh I willi pal
- guides (Fig. 4).
In the rest of southern Africa, however, these colors
are rarely associated with long-proboscid fly flowers. Instead, flowers are usually shades of cream to
pink, with pink to red nectar guides (Fig. 5). A few
species may have pale blue or mauve flowers, but
species of Nivenia (Iridaceae) are exceptional in
having deep blix perianths. Wain with lew exceptions, the nectar guides consist of longitudinal
streaks. Flower form is usually zygomorphic and
(Figs. 4G-L, 5F, G) or with decUnate stamens and
style (Figs. 4D-F, 5B-E). A few species of Erica,
II -.>> r
',
t,
ilea, and one of
l.'i;>ei:,-a.si,i have ui'i
tphi. ll>.u< r- \\JL- 1 \
C, 5A).
Anthers and pollen are often unconventionally
pigmented and frequently match the color of the
SRZ & WRZ: Northern Province to K Western

Cape incl. Lesotho
WRZ: Southern Cape
SRZ: Mpurnalanga
SRZ: Mpurnalanga and KwaZulu-Natal
perianth, or are simply a dull blue-gray to mauve

(Goldblatt et al., 1995). Some Gladiolus and Tritonid species with cream flowers, however, have dark
purple pollen (Goldblatt & Manning, 1999). It has
been suggested that unusually colored pollen is an
example of crypsis, making the pollen less conspicuous to pollei [nllecluiu iri-ccls :Y|:Mimnv A
Coldbl ill 1'('<>I lii /'././'_.>.* //, -pci ics. anthers
u are bright red to orange and may contribute to the floral signal to flies (Goldblatt et al.,
iw<)~>). especially if the petals are weakly marked.
Scent production is ,.,. iTabl. 2). In the Iridaceae only liabiann âmhurma has strongly scented
flowers, while B. framesii often has lightl) fragranl
Mowers. In the Amaryllidaceac, species of Brunsvigia typically have a light sweet fragrance.
\ f ll'l. II a U tl it.lllb
-pel (.' I I r -pr ,|,l.-. '
fly pollinated plants is the range of stamen orientation and length, which are
site of deposition of pollen on the body of a fly.
i
iphie flowers have symmetrically disposed stamens either held close to the mouth of the
floral tube, or in Erica, within the tube. In Aristea
spiralis the anthers are held 16-20 mm from the
ral tube Mrenin species eitln r have tin
anthers held at least 10 mm from the mouth of the
tube, or in the distylous N. argentea and Y. slam-
We propose recognizing three separate pollination guilds or systems within the long-proboscid i!\
belong to each
system show little or no overlap with those of other
systems in plants visited or season on the wing,
although there is some overlap in geographic range
(Fig. 1). Within each system there are well-defined
guilds of plant species that have one or occasionally
two fly species as their sole pollinator. A few plant
species may be pollinated by different fly species
in different parts of their ranges. Thus, Lapeirousia
lenoid* is ] Lin
I only by Prosoeca peringueyi,
but L. jacquinii may be pollinated by P. peringueyi
or, on the Bokkeveld Plateau, by Prosoeca sp. nov.
Likewise. /.. lain', ', I i> : . . n :
r.l- : a- | I in il-
siphon stamens of the pin (long-styled and shortstamened) morph are held just above the apex of
the floral tube. In zygomorphic flowers, the stamens
are unilateral anil -itI ? at. rJ, (arching above the
mouth of the tube), as in most Iridaceae, or declinate (arching below the mouth of the tube), as in
Pelargonium (Fig. 4D-F), Geissorhiza (Fig SB), and
the iii.i -.llids Brunsvigia and Nerine. In the latter
ed by Moegistorhynchus longirostris at some sites,

by Philoliche gulosa at others, and by both flies at
one site (Manning & Goldblatt, 1997). The occaM .ii 1 pre*
I
1 i |
I scid fly species at
a few sites has also been documented by Goldblatt
and Manning (1999) both in Western Cape and
Mpumalanga Provinces, but this appears to be a
relatively infrequent situation.
1. The Prosoeca peringueyi guild includes two fly
-( . ii - I' :< '.:.'"<./ ain I /'.-..w. . t |> r f . v. ' 1. 11 > 11
1). With complementary ranges in southern Namibia and Namaqualand to the Olifants River Valley
and the Western Karoo in South Africa (Fig. 1),
these two flies are active from July to late September. The range is thus restricted to the western half
of the southern African ^
hs of the yea
5 of species v
1 Iln
two genera, the filaments are extended forward for

35-^0 mm, so that the anthers are held at least this
distance from the nectar source. Stamen length is
notably variable in Pelargonium, species of which
have anthers held close to, or up to, 15 mm from
the mouth of the floral tube. Pollen depos tii
on
in
lies is dorsal in species with arcuate sta-
oi B
dun :
sole
i ,.li tors (Goldblatt et al., 1995; Manning &
Goldblatt, 1996).
Plants in the guild (Table 2) stand out in having
ides of magenta,
deep p upli -. violet, die lower, or all the petal or
tepal lobes in the case of actinomorphic flowers,
with cream t< yellow markings and areas of darker
I
I
- are often relatively small, 12-15 mm long (e.g., Lapeirousia jac-
mens and ventral in species with declinate stamens.

When anthers are held close to the mouth of the
species of Babiana belonging to the guild
of mauve to violet or cream.

The floral tube in most species of the Prosoeca
perin
l ûild is at least 20 mm long, and usually
in the 30-45 mm range. All members of the guild
flower in the late winter to late spring, late July to
1
- |
,
,ill\ restricted to
the southern African west coast and near interior
(Namaqualand and the northwestern Cape, South
Africa, and southwestern Namibia). Some plant
species in the guild have somewhat wider ranges
than theii pollinate! - ; ml loda\ repvnd ice ,. \ i !!,
only by autogamously produced seed in the parts
of their ranges where no pollinating flies occur (e.g.,
Lapeirousia jacquinii, Sparaxis metelerkampiae)
(Manning & Goldblatt, 1996; Goldblatt et al., in
2. The Moegistorhynchus-Philoliche guild,
named for the most conspicuous fly genera in the
system, includes six or seven fly species. The two
tabanids, P. rostrata and P. gulosa, have the widest
ranges, collectively extending from southern Namibia to the southeastern Cape (Fig. 1). The three
Moegistorhynchus species and the one or two Prosoeca species of the system have narrower ranges
in the southwestern Cape (Table 1). Flies of this
system are most]
icl
e -pring to early
summer, mid September to November, but are still
on the wing until January locally at higher elevations. Species pollinated by this group of flies mostly have a similar floral presentation, and the particular pollinatoi depends on geography. The same
species may be pollinated by up to three different
flies over its entire range. Although the geographical ranges of the Pr. peringueyi and Moegistorhynchus-Philoliche systems overlap in western southem Africa, they overlap very little in period of
activity of fly species and, as far as is known, not
at all in plants pollinated.
Plants in the Moegistorhyru
'
1
mostly have flow i
,-!,!
white to cream,
usiialU with pink undertones, or pale to .hep pink
(Fig. 5). Nectar guides are deep pink or red, occasionally with a white streak in the center of each
dark mark. On the southern African west coast,
flowers often have relatively large tepal lobes, 3050 nun Ion- u-.e.. Chiduiiits fmîish, - >, , ;,>< ,
Pelargonium longicaule), but Babiana tubulosa,
Lapeirousia anceps, and P. appendiculatum have
fairly small, inconspicuous tepal or petal lobes, up
to 15 mm long. The longest floral tubes (60-110
mm long) are found in wesl c< ist populations of G
angustus, L. anceps, and P. appendiculatum, and
these species are associated exclusively with a sin-
d pollinator, Moegistorhynchus longirostt;-. I in n

this fly has a proboscis at least 65 mm long, whereas in central Namaqualand, to the north, it has a
ji bosi i- only 37-45 mm long. Populations of G.
angustus and L. anceps elsewhere have shorter
tubes and are pollinated by Philoliche species,
which have correspondingly shorter probosces.
Several plant species from the Roggeveld and
Hantam areas of the western Karoo including Ba
biana spathacea, Disa karooica, and Romulea syringodeoflora (white-flowered race), as well as several species of Pelargonium, all of which have
cream to white flowers with red markings and elongate floral tubes, present a problem in the context
of long-proboscid fly pollination. Although !
bloom from October to early December, when Philoliche gulosa and P. rostrata are on the wing, and
have flowers that appear to be adapted for pollination by long-proboscid flies, no long-pn s
nl
species have been captured or recorded in this
area. Can the legitimate pollinator(s), whether one
of these Philoliche species or another ll\ species.
be extinct local 1
-
In S. D. Johnson
Too little is known about the Western Cape species, Prosoeca rubicunda, to confidently place it in
one of the long-proboscid fly guilds, but its apparent period of activity, January, suggests that it may
be a local extension of the Moegistorhynchus-Philoliche guild, which is centered in Western Cape
Province. Several plant species from the CaledonBredasdorp area of the winter-rainfall zone that
flower in the summer, from November to January,
including Nivenia concinna, N. stokoei, and Tritoniopsis flexuosa (Iridaceae) and Pelargonium cau<
i
c). have no known pollinator
although they have flowers that conform closely to
the long-proboscid fly type.
3. The Prosoeca ganglbaueri guild, named for the
most widespread and common fly species in the
system, operates in the southern summer and autumn, from January to April, and largely in eastern
(Fig. 1), but also in the eastern half of the winterrainfall zone that receives appreciable summer precipitation. As treated here, the P. ganglbaueri guild
includes four fly species (Table 1). While P. ganglbaueri extends from Northern Province southward
to the Kleinswartberg Mountains in Western Cape
Province, P. longipennis is restricted to the southern
Cape coastal belt. Because of the opposed seasonalilv there is virtually no overlap in plant species
with the P. peringueyi and Moegistorhynchus PhiI>>!< !,. s\ -stems The ' 'MIT- ei ;||o liii , /'/ev. ' a >,<>
ind P. ganglbaueri, in the south of its
>
*
D
range, overlap the eastern half of ihr range ol Hies

belonging to the Mocgiî, . :
I'l;;
guild. Inn tin- MIPHIII-. oi .).), ilv oi ifit- tli.-s n tin
two systems differ.
Guilds of plant species pollinated by Prosoeca
>i. P. longipennis, and P. robusta overlap
i'Iuta occur within the ranges of P. ganglbaueri and P. longipennis: h
pollii
have been found on both P. ganglbaueri and Pr.
robusta, and both flies have been captured while
foraging on Gladiolus calcaratus and Wal mio
iiiht'-,-;. I ikewi-e. /' ^./',^,l.>i'; an ! /' .'"<<<<., .. '<
nis have been observed and captured pollinating
Pelargonium dipetalum in different parts of its
range. No overlap has so far been encountered in
the species pollii
nii. ami lurh.-i nive-l igalion IM.IV -II...\ llii- lU n presents a gudd separate from the P. ga
guild of flies.
Flowers pollinate.I |>\ Hies in the f'/osocra -<;/,
uully [link with dark pink to
red markings, but Zaluzianskya microsiphon has
cream petals, pink on the reverse, and
<,//< r/'.;"-v ha-s win!. Il-iw< i- \':,n:>, ,,v.,;,,<'.,.," iunusual in having actinomorphic, unifon
I
blue flowers, at least to the human eye. Thus, in
general flowers pollinated by flies of the P. gangllxiurti guild resemble lh:>~e pollinated l)\ Hies of
the Moegistorhynchus-Philoliche guild. Species
pollinated by P. longipennis, a fly restricted '<> the
southern Cape coastal belt, have flowers with relatively small petal or tepal lobes, mostly ca. 10 mm
long, and a corolla or perianth that ranges from
eieam ( |i.di p.nk u -..limn. I-U..IK iM, !. tk.
pink or red on tin low, '
.
i
or Upper \I'rl<i!L->>i, :in,\. 01 all lilt lel>.'- iO.//../>,'/, /.
leptosiphon) (Manning & Goldblatt, 1995). Flowers
pollinated by Stenobasipteron wiedmannii are
shad
if pale blue, mauve, or pink {('
Manning, 1999; Potgieter et al., 1999) and usually
have small tepal or petal lobes, but species pollinated by P. ganglbaueri and P. robusta often have
Fi.oh
REWARDNK
Nectar volume. Nectar production is usually

ample, and quantities mostly range from 1.1 to 5
pd per flower in a standing crop (unbagged flowers)
ita about to forage
ON
Triionin fltil
(Table 3). Large-flowered spei ies liki Gladioli

gustus and G. undulatus may produce up to 10 ud
of nectar per bloom. Aristea spiralis is unusual in
having lloweis thai i I lei less Mian 0.5 pi of nectar.
Ihsu <ir<n <>>>;>. I). !><n i ,>i,t/,<i. and I). t>;c<,>>!:>!<;
,.-U,>",,!' s, ',. </e/.' /;,
:'
aid /!> *;! flit,' ...,...',-,.
produce no nectar (Table 3) and evidently depend

lei tin i' po lin lioi n: i. ( eil. t (it r flowers eloseb
resembling those ol |liei rtiembi Is oi i|j. .i ;.".; , e
tive pollination guilds (Goldblatt et al., 1995; Johnson & Steiner, 1995, 1997; Manning & Goldblatt,
1997).
Nectar sugar chemistry. In species of the Iridaceae, Lamiaceae, and Orchidaceae, nectar is sucrose-rich to suci - d i iin i) r lie ol sucrose to
hexosc sugars greater than 1sec Table .'.). hut
nectar in most species of Pelargonium examined is
hexose-rich or hexose-dominant. Nectar sugar concentrations are mostly in the 20-30% sucrose
ilent range, but may be as low as 19% (Ro{8% [P. incrassatum) (Table 3). Two speei. 1/,-s.
I
i.iiusn.il
.dl , <
IK ( I It ol
low sugar concentration, less than 18%
Pollen placement on the body of a fly appears to

be an important consideration in long-pro isi S i
pollination systems. At all sites that we have ini of plant species utilizing a
[ii I M id fly for ihcir pollination
appears to be closely correlated with the nuiuher
of pollen deposition sites (Manning & Goldblatt,
1996, 1997). Typically the frons and base of the
proboscis, the dorsal part of the head and thorax,
and the ventral part of the thorax and abdomen are
i < ! >
! !
i
species for pollen deposition
(Fig. <>l. In the ease of some Orchidaceae, pollinaria
are usually deposited near the base of the proboscis
(Johnson & Steiner, 1995, 1997). The need for speeitie sites lot pollen oi pol 11 nai mil i deposition is
presumably related to the behavior of long-proboseid file-, which are not llowei constant. Instead.
they visit llowei- ol different species in an apparently random pattern on foraging bouts (Goldblatt
et al., 1995; Goldblatt & Manning, 1999). The depnllei
ollinated 1>\ li.ng-ldiii'.iK-d !li<- .in.in-, ! ! -in!.' V 're\ iations: b = blue

d markings; p = pale pink or deep pink with red or purple nectar guides: \
contrasting pale nectar guides); wh = white. Scent indicated by - = absent;
For tube length we give only the functional length, not total lengthin H.
acaulescent species, the lower part of the tube is closed and only serves to
rial species inferred on I
I i i
l|
.n
ong to particular
1, are listed in parentheses. References, column eight, are as follows: 1 =
ddblatt
(19%); 2 = Manning & Goldblatt (1997): 3 = Goldblatt & Manning
Goldblatt et al. (1995) and Manning & C
ohnson
&
Steiner
(1995);
6
=
Johnson
&
Steiner
(1997):
7
=
Struck (1997);
(1999); 4 = Goldblatt et al. (1999); 5 =
8 = Manning & Goldblatt (1995): 9 = V gel (1954); 10 = Goldblatt & Bernhardt (1990); 11 = Potgieter et al. (1999);
12 = Goldblatt & Manning (new c lata; for methodology Be te Goldblatt et al. (1998a), Goldblatt & Manning (1999)).
Table 2. Floral characters of plai

with light throat; cr = pale cream wi
Flower
Sym-
SPi
<!>>;: ! Uakei
ecklonii Klatt
flabelllfolia G. J. 1
var. longibracteata (
Goldblatt & J. C. Manni

silenoides (Jacq.) Ker Gawl
violacea Goldblatt
Pollinator
Mouth
part mm
Floral
tube mm
M) .v>
35 io
33-39
3.W.0
25 2',',
25-28
27-32
2(^30
HI- r>
30 35
30-35
32-35
K) 50
10 (,5
15 50
15 50
35 15
11-50
10-15
IO- 15
40-50
10 50
Reference
Volume 87, Number 2
Ph. mstmta
Ph. rostrata
Ph. gulosa and
Ph. rostrata
Ph. gulosa
llotilniiultis .lac<|.
monticola G. J. Lewis ex
Goldblatt & J. C. Mannin;
rhodanthus J. C. Manning
& Goldblatt
n/a
50- 75
n/a
21 32
21 32
n/a
M. longirostris
22-31
22 31
n/a
n/a
67, 72
Ph. m.Mmla
and Ph. gulosa
23 27
18 20
27,-27
27-31
17-19
L8
20
17,
2:'
22
22 :?1
IK-21
(,7,-70
27,-27
22 2 1
22 30
22-30
07-70
22 21
18 21
30-31
17-18
25-27
18-20
18-20
70-110
32-37
32-37
45-60
45-60
22-30
22-30
23-27
27,-27
23-25
7,2 77,
37,-40
23
25
20
33
33
35-40
37,-10
fabricii (I). Delaroche) K
crispa (L. f.) Ker Gaw

mil /'/; ,//,.
"A. rostrato
and P/i. gulosa
ftabelllfolia (D. Delarc
29-34
27-31
17-18
30-34
P/i. rostrata
junonia Bolus. / /
. M n
I. <
'..,,, ', ,
I (
23-27
,
i, m i
40-48
45-55
45-55
45-55
32-38
- ill I.
>'ni<lf\ (I..) L'Her.. I'.
suburbanum Cliff., fi tetragomun (L.f.i l.ll,-,. It,-I.M . n.-: K6M*JWI brachystachys G. J. Lewis . sfHithacea (L.f.) Ker
Gawl., Geissorhiza callista Goldblall. 6'. longifolia (C. J. L.-wis) Coldhlatt, G. sc/iinzit (Bake
/;/;// (...l.ll.l ill f. /.../,' i....'
,/,,, | Bolus, f, Mjfi^/Hs (G J Lewis) Goldblatt & J. C.
Manning. I.\ia Jurala Ker GiwL /. splrndida G. Lewis, hipeirousia macospallia Bak.. /.. simulans Goldblatl & J
C. Maimiini. / ,,-i,;,n!u <,oldl.l.ill \". " ,;_< >,/.<, . \.
Br., 7: tugwelliac I . B.liis. lloô/,,,/ ,/,//,/ Klall. It. strictiflora Ker Gawl. Orehidaceae: Disu karooici Johnson <S
t Li.. I). >
Pr.
I'r.
f,
I'l
Pi
ganglbaueri
langipennis
1 , . >,. . lis
izangtbaurii
langipennis
34-36
38-10
3H 10
55-60
55-60
ca. 60
12
8
8
38-10
50-60
1.
, mn
wiedmannii
ganglbaueri
ganglbaueri
ganglbaueri
38 10
20-23
38^0
23-29
27-30
31-12
28-32
50-60
28-40
52-60
40-45
35-40
36-52
40-50
8
3
3
3
3
3
12
18-30
23-25
32-35
27-31
25 37
ganglbaueri
ganrlbanen
ganglbaueri
ganglbauen
23-25
32-38
ganger,
2:^-25
ca. 40
. ganglbaueri
33-35
3<> 15
10-1.5
40 15
bilineatus G. Lewis
Pr Ion Dennis
engysiphon G. Lewis
' ,
St.
Pr.
Pr.
Pr.
32 10
22 2*>
24 2^
22 2'*
19.6(2.3)
33-35
20-30
20.6(1.1)
25-30
25-30
microsiphon (Kuntze) K. Schum.

Inferred mrmlit i
I I
", /^^-, ',k.i ,
\m ii I 
krigei W. F. B.irk. i
Pr. ganglbaueri
33-35
3()-42
12
ill
> < IIM
'
/-, <<i
ill. -n
i ,i .)///( II CI.. Wii;wi';i
s, /,-,,,'*'/*'..' '< -ii M I I M I I dw. ii I
il.indau) C. B. CI.
.|.| i ,. .. .
,,_,. //..,/// .Sruj.. <;. sp. nov.. \rrinc filamctilosa W. F. Barker, N.
'
^ Bmtl D.iu In
/ r cerinthoides L. (pink form).
urn Oberm., G. saxatilis Coldbh.ll & J. C. Manning. C'. scahndu.s <;<>!< 11il.-ni X .1. I.. Manning. Hesperantha coccinea
(Backh. & Harv.) Goldblatt & J. C. Manning, H. curvula Hilliard & Burtt. H. hutchingsii Hilliard & Burtt, H.
< . ><:,.' I: k. -i Ilillli II. .\ Hi' II. II ,., , ' .. i: ,1. . \ -.
;/i N.F. Br.. /V. stokoei L. Guthrie, Radinosi
ylto,
<
i iliiL ii
I Li
I mil i I
-.uma occulta N. E. Br. Lamiaceae:
Synro/ostemon derm/lnri/s Benth . s I:H, "u.il.u* K..nki i \~l,|.\. s .. ',
I M
'
E. Br., I m*dia Codd, 7: succulenta (Dyer & Bruce) L. E. Codd. Orchid;..,.,. : l),s rhodaniha Schltr., D. 5<mco/a
Schltr., Satyrium hallackii Bolus. NOTEHasp
Milliard & Burtt may belong here, but although
il dors ha\r an rl..n>',ilr prnalilli lui.r. Ihr iui.r I^rll is .-.IrrliK l\ n.
transfer to stigmas.
"M ophlll
!.././>
.
.
ll. II II II III rd (/' i
.
Ml
I !
I I /
s
I
rlngueyiMuseum record).
(ieiam.i
/'
,vv (I..) E'Her. (Ph. mstrata\t)g,cl 1954); P. dcnlicultiium (iiiu.lrnliliril II
McDonald in Struck, 1997); P. suburbanu
flyvan Jaarsveld in Struck, 1997).
same site on the in^. l"s hi ;, ,v<ul 1 fi \i < r 11 \ n sult in insect visiN i iln _ |
. ,n : Iis.li [tollination
as a result of stigma clogging by foreign pollen.
In the Prosoeca peringueyi pollination guild pollen deposition on the ventral head or thorax is effected by Pelargonium species, on the frons or dorsal thorax by Lapeirousia species (normally one or
two species of a genus is present at any site), and
on the dorsal thorax by Babiana species (also normally only one species present at any site) (Manning & Goldblatt, 1996). Pollen of Hesperantha latifolia, occasionally part of the guild using P.
peringueyi as pollinator, is J, p Sil< d on the lateral
and upper ventral thorax. In P. incrassatum and P.
sericifolium, which are sympatric at some sites in
Namaqualand and are both pollinated by P. peringueyi, pollen contamination is avoided by placement of their respective pollen on the ventral head
or ventral thorax of P. peringueyi, the result of
shorter or longer filaments in these two species.
This pattern is repeated in the Moegistorhynchus
longirostris-Philoliche pollination guild (Manning
& Goldblatt, 1997). Pollen deposition on the distal
- nli n tl i
is II. . I. >l
"rlargonium spp. (either P. praemo
'
aule) or Geissorhiza
spp. (either G. confusa or G. exscapa) and on the
proximal ventral thorax or lower head by P. tabu/./
I >< |> -i n i ib< h -. i, effected by Lapeirousia anceps, the dorsal head or thorax by Tritonia
crispa at some sites, and by Gladiolus undulatus,
G. angustus, oi
i
ll i th< re Ixia paniculata
is unusual in having short stamens held within the
mouth of the tube, and its pollen is deposited on
the frons an>UJ
baa
proboscis. Species
of Orchidaceae that have stalked pollinaria are
probably not directly involved in competition for
pollen deposition, but the number of species of Orchidaceae at any site is usually limited to one.
Pollen deposition in the Prosoeca ganglbaueri
guild follows this general pattern. For example, anthers of Brunsvigia, Nerine, and Pelargonium spp.
brush different parts of the ventral head, thorax, or
abdomen, depending on stamen length, while pollen of Gladiolus and Watsonia species is deposited
on the dorsal thorax. Orchid pollinaria are placed
near the base of the proboscis. Pollen placement
Goldblatt & Manning

Long-Proboscid Fly Pollination
by Hesperantha species, which mostly have symmetrically disposed, divergent anthers, is less well
defined but is always on the lateral or ventral parts
of a fly's body. Pollen of the important long-proboscid fly plant, Zaluzianskya microsiphon, is deposited on the ventral head as the anthers are held at
the abaxial side of the mouth of the floral tube.
of the perianth tube where they readily brush

against the body of a large bee as it forces its upper
body into the upper part of the floral tube while
extending its proboscis into the lower part of the
tube. The perianth may be almost any color, but is
not often red or cream, and the flowers are frequently scented (Goldblatt et al., 1998a). Long-proboscid fly flowers of the Moegistorhynchus-Philol-
EVOLUTION OF THE SYSTEM
*cê an(^ tne Prosoeca ganglbaueri pollination

systems merely require a shift in flower coloring
toward the pale pink to cream end of the color
spectrum, the acquisition of darker, linear nectar
guides, and an elongation of the narrow part of the
floral tube to exclude nectar feeders with mouth
parts less than 15 mm long. Nectar quality, especially sugar constituents, is much the same as is
found in long-proboscid bee flowers, but nectar volume is typically much greater and sometimes more
dilute. For example, flowers of bee-pollinated species of Gladiolus have nectar volumes between 0.5
and 4 u,l compared with 1.8 to over 10 p.1 in longproboscid fly pollinated species (Goldblatt et al.,
1998a; Goldblatt & Manning, 1999).
It is noteworthy that fly diversity is higher in the
geographically much smaller winter-rainfall zone.
Three fly species range over all of eastern southern
Africa, whereas there are 10 fly species in the two
long-proboscid fly guilds in the winter-rainfall zone,
Some of these flies are relatively widespread, but
Moegistorhynchus sp. nov. and Prosoeca sp. nov., P.
rubicunda, and P. nitidula have very narrow ranges
and moreover, except for P. sp. nov., they appear to
be rare, at least as far as one can judge from the
few specimens known,
Associated with butterfly pollination by Vogel

(1954) in his keystone work on pollination systems
in the flora of southern Africa, long-proboscid fly
pollination appears to have no direct connection
with that strategy. Butterfly and long-proboscid fly
pollination have some similarities, notably including plant species with odorless, long-tubed flowers.
The two systems are, however, independent of one
another, and no species of either group of insects
share the flowers of any plant species. Moreover,
butterfly pollination in southern Africa (excluding
the highly specialized Aeropetes butterfly system
Johnson & Bond, 1994) is frequently a part of generalist systems that use other insects, including
bees, hopliine scarab beetles, and settling moths
(Goldblatt et al., 1995). In the Iridaceae, phylogenetic studies in Gladiolus, Lapeirousia, and Sparaxis show that long-proboscid fly flowers are nearly
always most closely related to ancestors pollinated
by long-tongued bees (Apidae) (Goldblatt et al.,
1995, in prep.; Goldblatt & Manning, 1999). Species of Gladiolus pollinated by long-proboscid flies
fall in taxonomic sections where long-proboscid bee
pollination is ancestral and in which butterfly pollination may not occur. In the only section of Gladiolus in which butterfly pollination (by the specialist pollinator, Aeropetes) is significant, section
Blandus, butterfly flowers most likely evolved from
long-proboscid-fly-pollinated ancestors (Goldblatt
& Manning, 1998). Pollination by the Aeropetes butterfly does not occur in Babiana or Lapeirousia,
genera in which long-proboscid fly pollination is
especially common, nor in Ixia or Sparaxis, or Tritonia.
in most families in which long-proboscid fly pollination occurs, a shift from bee to long-proboscid
fly pollination appears to be relatively straightforward, involving shifts in perianth color and marking
pattern, elongation of the floral tube, and loss of
floral odor if present in the ancestor. For example,
in most Iridaceae, long-proboscid bee flowers are
zygomorphic and have a funnel-shaped perianth
tube of moderate length, with the upper flared portion about as long as the cylindric basal half. Unilateral arcuate stamens are held above the mouth
TERMINOLOGY
There is unavoidable confusion when comparing
long-proboscid fly and long-proboscid (or longtongued) bee pollination. Long-proboscid fly pollination, according to our definition, includes flies
with probosces in excess of 15 mm and usually
much more. Few long-proboscid bees have probosces longer than 12 mm. Moreover, acrocerids, tabanii
mm ]
cid flies to contrast them with short-tongue flies that
lap fluid. Rebelo et al. (1985) coined the term rhinomyophily, which is useful but not favored by
many biologists who prefer more direct terms (e.g.,
bird pollination vs. ornithophily, etc.). Struck
(1997) favored the term hoverfly pollination, but
that has the disadvantage of misrepresenting the
typical behavior of the flies, which grasp floral organs whenever possible while foraging although
*4k
/^F
Volume 87, Number 2
Goldblatt & Manning

they do hover while inserting the proboscis into a

floral tube. We have no solution to offer and suggest
long-proboscid fly pollination for the syndrome involving flics with prohosees usuallv exceeding 15
mm, and short-proboscid fly pollination for the syndrom.' involving Hies with I me sucking mouth parts
usually less than 15 mm long. Flies with lapping
mouth parts would be excluded from this definition.
I'll'-i infusion between luii pi [|...scid fly and longproboscid bee syndromes as regards length of
mouth parts seems unavoidable.
for a preferred type of nectar This reflects the con

elusions of van Wyk (1993) and van Wyk et al
(1993) that the nectar sugar characteristics of flow
ers are highly conserved and that nectar sugar pat
though it seldom rises above 32% sucrose equivalent and seldom dips below 20%. The two species
of Hesperantha in the Prosoeca ganglbaurii guild
low 20%. Concentrations above 32% may make the
Vc i
I CONSIl
lilable for flowers polliAlthough m

nated by Diptera suggest that flies favor nectar with
hexose sugars predominant (Baker & Baker, 1983,
1990), these authors did not distinguish between
flies with short, lapping mouth parts and those ith
long, sucking mouth parts. Recent studies, howeii
er, show that nectar of plants with flower- adapted
for pollination by long-proboscid flies is often sucrose-rich to sucrose-dominant (Goldblatt & Bernhardt, 1990; Goldblatt et al., 1995; Manning &
Goldblatt, 1996, 1997; Goldblatt & Manning,
1999). The broader survey here in general coutums
this observation, but the data indie ale thai ibis ma\
simply be the result of the taxa involved. Most Iridaceae belonging to subfamily Ixioideae (which includes most species pollinated by long-,
flies) have sucrose-rich nectar as do all species of
the family with flowers adapted for pollination by
bees. Significantly, nectar of Aristea spiralis, the
only species of Iridaceae with long-proboscid fl)
flowers and not a member ol I
id<
h is hi
rich nectar. It also produces nectar from perigonal
nectaries (Goldblatt & Manning, 1996), unlike species of Ixioideae, which have septal nectaries
(Goldblatt, 1990, 1991). Flowers of some other families with long-proboscid fly flowers (e.g., Lamiaceae, Orchidaceae) also have sucrose-rich nectar.
However, Geraniaceae does not follow this pattern;
species of Pelargonium that have been examined
(Manning & Goldblatt, 1996, 1997) have, with the
exception of P. cortusifolium. hexose rich to i
dominant nectar. Among long-proboscid fly flowers
then, nectar sugar chemistry may simply be a reflection of system
i
nectary type, and
not the result of selection by long-probe i I i<
liii!>,<
xi IMIIIII.II
ill I
.'
.<">. ..,,*,<
,!, inn
-I /.. notiHKi
-1
K >
..>,,,<<
CO-EVOLVED SYSTEM
As suggested by Feinsinger (1983) for sphinx

moths, it seems that long-proboscid flies and their
flowers have probably evolved through reciprocal
selection. Frequent visits from long-proboscid Hies
select for long-tubed flowers, which in turn select
for longer-pro! 10- id llieipabl of reaching the
nee tar within the tubes. This pattern fits the Red
Queen effect (van Valen, 1973; Futuyma, 1979), in
which species may coevolve indefinitely, some bethe process, or else arrive at a
n. Evolution within
be all that simple.
1 of long-proboscid flies appear
Populatic
to be highly erratic (Goldblatt et al., 1995; Goldblatt & Manning, 1999), a situation comparable to
that for sphinx moths, as noted by Gregory (19631964). But whereas shorter-proboscid moths visit
these flowers, taking advantage of nectar welling up
in I he lubes, there do not seem to be alternative
sh 11 1 1 I
1 insects available for most longjin bos< 1 1 H flow PI o use this resource when their
prima
p illinators are not available. Instead, those
long-proboscid fly flowers that are self-incompatible
11 I i :nl to reproduce or reproduce poorly in certain seasons at certain sites (Goldblatt & Manning,
1999).
Fail-safe mechanisms for self-pollination appear
to be quite common among species pollinated by
long-proboscid flies. We know now that of the ten
species of l,,iprinnisin with flowers adapted for pollination by long-proboscid flies, four at least are
11. //// UDItsUi
f I*, cmssiraiili (', L

'i,,,,!! - I h,!
mgirostris and I'liiloliclw gutosu.
\.
I iff
Ji! if
11
^
illl!
;.|<s# 1
1 -a " i *
!!fll
sIlP.
I Illl
i illl
Mil
IJSiJ
3
!31IIS I
#
|
I J
4d^^^
144
^,U^4 vi
I *U
<5 i |
f ftf^
M I ? 1
Jllll
J
*1;
|
-- &E ^ ^ -
1 f Si
"s-Îi
J. h. i T
= : _ r L
"
ni
IIIII^ * |^
^ 1 1
Ujlj
Plf=
1 ^ II f
:
- = = -=
z -e * j =
IliS
||lli1|| Hill ill5 flttl |l 'I
33
1 1
U
cJ.oi.A
;';;:
'*
3H 13^
î 4
3" 4
fUjJlil1 iilljlltittl
u
I m ill' Ss>33 III II
j
3 HJ His
& a* m
2S3
l.tTii
U5
S S C4
53 e
522333
3 SI
3333
jjijlUPiHlWHijtlln!
;5
ssi iS3;
- - i i g 4 6
'1
1
jj
111
* i 1333
7
333
r? rs S
27.7 il.Oi
27.3 (1.3)
27.2 il.li
2 3 313' 3 3
J a 1.1.
3 3
j-lltljll fJtj|iIl|jilIHii|H1
i I i
322
lilllllj
it
1 ill!
in: ijif11
^^
^^
JJ
G1(_MJ>
^^
^^T
-^
^^S^^^X
^^^^,'^b
j^r^
^^
~ J\
j^
(\\//
jd'
' *r<5
g ^^
y^
</
y^0^^H\
j&r
"ÊS^
4f
\\
though in Pelargonium sell compatibility appears

lo be tin- rule (Slrij. k. 1(V.7). autoâmx > anno! noi
mally take place because of mechanical protandry.
There is 111 tctni. tin barn. : |o ^nh no-amou- ; ol
lination in this i
n whi- h i florescences produce numerous flowers contemporaneous!;, bul pol
lination must be mediated by an external agent.
Proboscis length is typically shorter than the floral tube, a feature that long-proboscid fly pollination snare
s with sphinx moth pollination. This ensures that a visiting insect must push its body into
flowers so that its proboscis will extend as deeply
as possible into the tube and reach the nectar reservoir. Orchid genera are one notable exceplion. In
lecepl
It
ol l>
i
ili
i>
conis
com ex
pl
(Johnson & Steiner, 1997), spur
lengths may be shorter than the proboscis length
andpollinaiia.M. ittach. ! lo th< ippor llurd ol ll.<
probos. is. (Ilia i e\t epiions ait \rstca \j>inilis and
species of Brunsvigia and Nerine that are pollinaleil
by long-proboscid flies; in these taxa floral tubes
are less than 10 mm long. These flies, however,
and probosces long
gh that they will consistently brush against anthers and aecuiii
I pollen on their
abdomens. Nectar produced
by such short-tubed flowers is obviously accessible
cite, tut pollination \>\ lie.--, m \;i-,ho
N/..V,///S.
We
have not recorded visits to any other of these shorttub, t! spe. ics b\ ins. els oilier than lout; probos. itl
Hies. The onsitlerabl. distant c >! the anthers from
tube also makes it unlikely that
even large bees i
in such flowers because
much shorter than the filaments.
incompatible (Goldblatt et al., 1995, and unpublished data). At least one species of Hesperantha
(H. latifolia) and the Ixia and Sparaxis species
known to be pollinated by long-proboscid (lies are
facultatively autogamous, whereas in Gladiolus self
incompatibility appears to be frequent (Goldblatt et
al., 1998a, in prep.). Some p..] i.l iti n- ol t. .,> < species with long-proboscid fly flowers have set no
capsule-: (or three years lor which we have observations when their pollinators were absent. Al-
Attention was first drawn to long-proboscid IK

by Fletcher and Son (1931), who
briefly des
of) Roscoea purpurea (Zingiberaceae) by ih
ui
fly Chorizoneura
boscis 50-60 mm
long). Subsequently, Dierl (1968) described in detail the behavior of this fly in the course ol its visits
to flowers (presumably foraging for nectar: on Ros
coea. The Himal
istit ally rich and
includes several plant sp. cies with loi^-tub. .1 llowers that may also be pollinated by this fly, e.g.,
olher species ol Rn.sn>r,i ami Riuxioiicmlio!) spp.
(Kricaceae). This pollination guild awaits more exon. Involving different fly genera
, the Himalayan system presum-
TAXONOMIC DISTRIBUTION OF LON<;-PROBOSCID

FLY POLLINATION
According to our survey, at least 83 species have

I" < ri -d
11. | i 1
1 - ili U h\ long-proboscidflies.Basedontheirne.it!- Itiii. il Moral prcsentation, it seems reasonable to infer that at least
90 more species also have this polli
Even if this figure is grossly underestimated, there
seems no doubt that long-proboscid fly pollination
is 'I relalis ! nit
imp Mm < in the flora of
southern Africa, which comprises over 20,500 species of flowering plants (Goldblatt, 1997). Nevertheless, long-proboscid fly pollination assumes
dies in southern \iti< a. (ieranuu < a<- and lnda< e
Precise figures are not available for Gerani i
but Struck (1977) has estimated that 25% of the
southern African species of Pelargonium are pollinated by long-piob<>-< "I IIn - ilthough the exact
definition of the system thai I
clear. In Iridaceae we have more accurate fig in s
Some 105 of the approximately 1025 species in
southern Africa appear to have this pollination svs
tem exclusively and one
antha coccineaS. D. Johr
istea spiralis, Watsonia borbonicaTable 2) may
have a combined long-proboscid fly and other insect pollination. Thus, about 10% of southern African Iridaceae have adopted this pollination strategy. This is substantially more than the estimated
64 species (6.3%) of the southern African [ridace
that are predicted on the basis of floral morpholog)
to be pollinated by sunbirds (Goldblatt et al.,
1999a).
Among the Iridaceae, long-proboscid fly pollination appears to be most well developed in Lapeirousia, in which 10 species, or 30% of the total
in temperate southern Africa, have flowers pollinated by long-proboscid flies. The system is also
well developed in Gladiolus (Goldblatt & Manning,
1999; Manning & Goldblatt, 1999), in which 27
species are considered to have flowers adapted for
this particular pollination strategy (17% of the
southern African species), and long-proboscid fly
pollination is inferred for between 10 and 20% of
the southern African species ol five other larê gen, Babiana, Geissorhiza, Hesperantha, Ixia, and
Tritom
fly pollir
Brownleea and Disa, and we have yet to i

significance in Amaryllidaceat
strategy seems likely in Acanthaceae, but it has yet
to be confirmed in that family. In the remaining
families in which it occurs, long-proboscid 8j pollination is decidedly rare and is evidently confined
to just one or a few species. Curiously, evolution of
the system seems highly labile in several genera of
the Iridaceae and in Disa (Orchidaceae). In Disa
and Gladiolus it has evolved repeatedly in different
., 1998; Goldblatt & Man-
Long-proboscid fly pollir

single ii
range, clearly are at more significant risk than those
that are pollinated by several different insects
(Bond, 1994). Long-proboscid flies may be regarded as keystone species, for several plant species
depend on particular flies for their pollination and
sexual reproduction. Conservation of plants with
lion > I th< i | ' ilin itOfB, an undertaking fraught with
Both Nemestrinidae and Ta;x life cycles. Tabanidae have
larvae that require wetland
habitats for their larval development, which may
take place some distance from sites of the plant
species on which the adults feed. Female tabanids
also require a blood meal during their adult phase
before egg-laying can proceed. This makes the
presence of suitable host mammals essential. Neidae have an equally complex life history.
Although no details of the life cycles of long-proboscid flies are known, all members of the Nemestrinidae so far studied have parasitic larvae, often
on locusts. Obviously, large, relatively undisturbed
sites with a diversity of habitats are necessary for
the completion of the life cycles
and tabanids.
I"
'
I.M'*"- pP- H7-141 in
Little (editors), Handhook of Kxl Biology. Scientific arid Academic
Jot. 39: 157-166.

>art of pollinator and dUi.crser disruption on |
inction. Philos. Trans., Ser. B 344: 83-90.
J,
,!
\\
I.I.MI.
f
!"(.!.
\,| urn .,
1, ,
i,
. ,n '
<-<
K X L van der Pijl. 1979. The Principles of
I in I
1 .
In
.ill I'll s,. \.U \olk.
Feinsinger, P. 1983. Coevolulion and pollination. Pp.

282-309 in D. J. Futuyma & M. Slatkin (editors). Coevolution. Sinauer. Sunderland. Massachusetts.
Fletcher. ['. 15. & S. K. Son. 1931. A veterinary cnlo-
Futuyma, D. J. 1979. Fuilulionary 1d. rland. Massachusetts.

Goldblatt, P. 1990. Phylogeny and
. Missouri Bot. Card. 77: 607-627.
An overview of tin
h '
n
ol die southern Mncan Irida. c.w I io-ili.
ic diversity in die Cape Floin ol
rsity & Conservation (.: 350 .577.
1000. Pollination biology of NivI heterostvlous sell
I.III.
i the fynbos of South I
poll
systems. Khmer Academic Cress, Dordrecht.

& K. K. Steiner. 100.5. Cong p.ohos.-id ll\ pollination of two orchids in die Cape Drakensberg mountains, South Africa. PI. Syst. Evol. 195: 169-175.
&
. 1997. Long-tongued fly pollination
..pl
I ' (..,.. '.I 15 5:!."
, H. P. Under & K. S. Steiner. 1908 <
and radiation of pollination systems in Disa (Orchidaceae). Amer. J. Bot. 85: 402-111.
damiing. .1. C. X C Ooldlilatl. 1005. Cupid comes in
guild in th, (Kc'b.-.g \cld Fl 81(2): 50-52.
&
. 1996. The Prosoeca peringueyi (Dip
tera: Nemeslrinidae) pollination guild in southern Africa: Fong-longued Hies and llieir tubular llowers. Ann.
Missouri Bot. Card. 83: 67-86.
rostris (Diptera: Nemeslrinidael pollination guild: Cong
tubed flowers and a specialized long-proboscid fly-poll southern Africa. PI. Syst. F\ol. 200:
r.M.o.
I"
Ixioideae). Ann. Missouri |{..|. (.aid. <">3. 31i "if. I.

&
. 1998. Gladiolus in Southern Africa.
&
. 1999. The long-proboscid IK pollination system in Gladiolus (Iridaceae). Ann. Missouri
Bot. Card. 86: 758-774.
,
& P. Bernhardt. 1995. Pollination biology of hipt-inuiva subgenus l.npemiusui (Iridaceae) m
long-tongued fly pollination. Ann. Missouri Bot. Card.
82: 517-534.
,
&
. 1997. Notes on the pollination of Gladiolus brevifolius (Iridaceae) by bees (Anthophoridae) and bee mimicking flies (I'silinlcra: \<locendae). J. Kansas Fntomol. So.-. 70: 297-304.
of lice-pollinated Glailioltis species (Iridaceae) in southern Africa. Ann. Missouri Bot. Card. 85: 492-517.
, P. Bernhardt & J. C. Manning. lOOJit, Colli...-.
ii
les by monkey beetles (Scarabaeiilae: Ii aid mac: Hop ill.i) ... soulh, in \fnca \un.
. .1. C Manning iK C Uei::hardl. IOOO;I. 1., i,|,-inr
of bird pollination in the Iridaceae of southern Africa.
Adansonin ser. 3. 21: 25-40.
Grant, V. & K. A. Grant. 1965. Flower Pollinati
he
t'hlox Fan.ib < olim.l.ia Univ. Press. New York.
Gregory, D. P. 10(, l"i ) !l, 1 m
.,,
1
1,
On ja.-eae). Aliso 5: 357-384, 385-
Potgieter, C. J.. I .1 Edwa.ds. I! M Miller & J. van

Staden. 1999. Pollination of seven I'lectrarithu.s spp.
Evol. 218:99-112.
Kebelo. A. G.. W. R. Siegfried & F, G. H. Oliver. 1985.
Collin; on .,1 />;,-,( spears in ll,e soa'l, >yrstr-n Cape
S.African J. Bot. 51: 270-280.
Root, R. B. 1967. The niche exploitation pattern of the
LI . gnatcatcher. Ecol. Monogr. 37: 317 350.
Struck. M. 1007. Floral divergence i '
rica: Ecological and evolutionary considerations. PI.
S\st. E\..l. 208: 71-97.
Valen. I.. Van. 1073. -\ new evolutionary law. Evol. Theory 1: 1-30.
Vogel, S. 195-1. C i
I.
|.< II ,-iC I lenient.der Sippengliederung. Col. Stud. 1: 1-338.
I \ B I II t
me, K \ .. Kel, I
I 'I
Insect pollination in the Cape Flora. Pp. 52-82 in A.
C. Rebelo (editor). A Preliminary Synthesis of Pollination Biology in the Cape Flora. CSIR. Pretoria.
em \fll(.ill Cl| .1 .. . I
II
.- Ii.
S I
& Ecol. 21: 271-277.
, C. S. Whitehead. H. F. (dan. I). S. Hardy, E. J.
van Jaarsveld & G. F. Smith. 1993. Nectar sugar composition in the subfamily Alooideae (Asphodelaceae).
Biochem Syst & Ecol. 21. 249-253.
WOOD ANATOMY OF
MACKINLAYA AND
APIOPETALUM
(ARALIACEAE) AND ITS
SYSTEMATIC IMPLICATIONS1
Alexei A. Oskolski*
Porter R Lowry IP
of Maclcinlaya (shrubs from Queensland. Australia), using light and scanning electron microscopy, to investigate their
intervessel pits, ranging fi.mi 5 to (. pan bmh >
i < h
1 i| - 1
il u
i lill'is. m-augtegales in
1
> ,
'
il
i i
n uehv ma; non-septate fibers: rays composed of mostly upright and square cells; and brown
deposits in the vessels. Differences in wood structure between the genera appear lo be related to habit. The results
confirm recent molecular sequem e data suggesting tint b.
. ' 1/
..,,, loin, i iiioiiopln li-li< >:rnup.
Evidence from wood anatomy neither validates nor refutes the hypothesis that these two genera are intermediate between
Araliaeeae and Apiaeeae and oiler, no < lear indication of the group's phylogenetic position. Several wood characters
(small intern ssel pit- tlmk hbn w ill- non-septate fibeisl suggest a i.lili
n
..* Ihhuhini and
suggested by Phlllkett. Ilol between then
I oil,
I.
Ill II. ill el
i both ra\ and axial parenchyma. pre\iouM\ reported onb once in Tntmi I, i,-i>,-!>iliim li.iill.

and Mackinlaya F. Muell. within Araliaeeae have
been difficult to ass< -- i- i _ r I it i< .rial approa, lies
based on morphoIn:.
Eteci
ti lies using molec-
two species, both endemic to New Caledonia (Lowry, in prep.). Mackinlaya species are branched,
s\ rtipodiaI shrubs w itli simple And palmately lobed
or palmately compound leaves. Apiopetalum spe-
lutionary relatioi -hips I mi

.
e\act placement
remains unresolved I' i\- sp , , , ,,i \J
(including .Anomopa
i lb) Philip
son (1979), extending from Queensland, Australia,
through the Solomon Islands, Bismarck Archipelago, New Guinea, and Celebes to the Philippines
(see also Philipson, 1951). Apiopetalum comprises
exclusively simple leaves.

MI
>I>
.-S proposed for Araliaceai (Bentham, 1867; Harms, 18941897; Viguier. 1906; Hutchinson, 1967; Tseng & Hoo,
1982; Takhtajan, 1987), Apiopetalum and Mackinlaya have been placed in a separate tribe Mackinlayeae, which has traditionally been distin-
ct \kadenuselier \ustaiisehdienst. DAAD). We thank P. Baas and an anonymous referee for valuable comments and
suggestions on an
ihmiial .1 n rn n rip aid
1
Inn
[ I >i n
l| d i
i ' u-> mil loi his collaboration during field
n N
I 1
1
raba We are grateful to the following persons for assistance
provided: E. S. Chavcluna,l/e. 11. (.. Ki, liter. K. John. t:h. Wa.tkus. T. I'otseli. .1. \1. Villon. I'h. Moral. T. Jaffre, J.
West, B. Hyland, B. Gray, and K. Jensen. Assistance was provided to the first author by the following: Ordinal,at fur
II I I i I
I
i
I
I ,,
I
i
in-a .It
I I I
lli..
i
I
' ii in.I tin Hot IIIK al
Museum, the V. IK
i
!
-II- extended in New
Caledonia by the sta
n - > 1 i nnement et de la Gestion des Pares et Reserves.
Province Sud. and lb. I
. io ,1
,
, ib'iu.l
I I I he. I'loun, e Nord. We also thank the Museaim
National .I'Mistoire Naturell. n Paris. tli<- CSIKU
i I
I Hon), the Sydney botanical Garden
and the Australian Nairn
II ii n iui. in' lime, - 1
.
lie Id ..I
. upp.ni M
s(.S rant TiT'i.VX). The
second aulhoi s field an
i
I
> |
I n
-I I
I i| ro\ i in. nt (,i ml
BSR83-14691. an ASPT Herbarium Trawl \ward. the Mi^mri Botanical Garden, and the Division of Biology and
\le.li. al Sci< rices ol Washington I niversih. N. I < in.
I.i in ,1 Mn II.i \ I lr i i i liol II i! I
ii i. .1 th< Russian \.a.l. my ol Science. Prof. Popov Str. 2.
197376 St. Petersburg. Russia. oskolskiC" A01818.spb.edu.
Mi MI.I I. ,
I
.1
I
I.
-i
i
,
'
1,1 Lor; and l.abor"" National <rilistoire Nat,,,, lie. I<> rue Buffon. 75(X)5 Paris, France, lowry@mnhn.fr.
BOT. GARD.
87: 171-182. 2000.
guished on only a few floral hai U ' I

p in I Ij
the presence of valvate, clawed petals. While
Mackinlayeae have been recognized in nearly all
classifications since that of Bentham (1867), this is
more a reflection of sparse information on Apiopetalum and Mackinlaya than any real confidence in
thru [-elatedness. Wr .|u nol r uisidei similarities in
the form and position of the petals as sufficient o\
idence to support the hypothesis that Apiopetalum
in I \t
inlaya form a monophyletic as
' .
and additional dala are required lo clarify then position within Araliaceae.
Apiopetalum and Mackinlaya
been regarded as most closely related to the welldeliiied ujoup comprising \hoih.u urpu.s, Drlarinra.
and PseudoM iadi
he M
'
irpeae), which is
centered in New Caledonia (Lowry, 1986a, b). Although the monotypic genus Pseudosciadium was
included in Mackinlayeae by Harms (1894-1897)
because of its valvate, clawed petals, Baillon (1878,
1879) originally suggested that it was most closely
related to Delarbrea and Myodocarpus. Baillon's
initial interpretation has been supported by recent
systematic studies, ami dala from the fruit structure
(Lowry, 1986a, b) and wood anatomy (Oskolski et
al., 1997) indicated that Myodocarpus, Delarbrea,
and Pseudosciadium form a monophylett
i-- i
blage. Results of recent phylogenetic analyses
based on matK, rbcL, and ITS sequence data (Plunkett, 1994; Plunkett et al., 1996a, b, 1997, unpub;
lished data) further support the hypoth
these three genri i I. r
a dislin I. hasalh bran I.
ing clade within Apiales. Tin-. -,
a als<
that Apiopetalum and Mackinlaya comprise a second, isolated clade within the order.
Apiopetalum and especially Mackinlaya resemble
mari\ \piaeoae in < erlain lealuies. s icli as the presence of clawed petals, inflexed anthers in bud, a
bicarpellate gynoecium, and a petiole base that
forms a dilated sheath extending around 'In entin
circumference of the stem (the latter two characters
oecui onh in Markinlaya) On ibis basis. I'hilip-on
(1970) and Rodriguez (1957, 1971) regarded Apiopetaluin and \]ackin!ava as possible intermediates
between Araliaceae and Apia- .
ili-mill
garded as sister groups. In tire mol
liar stu
i
exact position of the Apiopetalum-Mackuii ,
within Apiales varies depending on the gene sequence and the type of analye
I
rees,
lade is sister l<> \piaeeac (coriipr isni^ subfamilies
Apioideae and Saniculoideae, but excluding many
genera traditionally placed in Hydrocot loidea
whereas in other analyses the t
to the clade .
can provide useful

complementary data for assessing relationships
anion-; the iii i < la of \raliai ea< . as shown h\ sevi ral
previous studies (Oskolski, 1994, 1995, 1996; Oskolski et al., 1997). Until now, no information on the
wooij analoiin lor either !;>;,,<>,./,,/../,, ,,r Yhtckinlava
has been available. The present study surveys the
wood anatomy ol
[piopetalutn and
two of the five species of Mackinlaya. The results
are examined with regard to hypothesized relationships between these lienera. as well as with Xlxoilo
carpus, Delarbrea, and Pseudosciadium, core Araliwoody Apiaceae (Bupleurum,
Heteromorj)ha. St.-
M hidendron, Eryngium, Gymnophyton, Asteriscum, and Trachymene).
moir-
MATERIALS AND MI
Most wood specimens examined were collected by

the authors and G. M. Plunkett; one sample of Mackinlaya macroscia
led by B. Hyland
(CSIRO Division of Plant Industry, Atherton), and
another was taken from a plant at the Sydney Botanic Gardens. Voucher herbarium specin* - Iron
New Caledonia are deposited at MO, NOU, and P,
and from Australia at QRS and MO. For the following ilest nptiitrts, it, ases where multiple samples oi
a species were examined and a feature was seen in
only a portion of the material, the corresponding collect ions an- in healed m square bra< kels. Wood samples wen taken fn.rn Irlink- ti \;>i"pi-talnm (from a
primary branch in A. velutinum [3854]), and from
basal port ns ol -terns , \hick\n'htMi.
Standard procedures for the study of wood strucii,dies a ail.sumicroscopy (SEM) were prepared i ording to Exley et al. (1977). Descriptive terminology and measurements follow Carlquist (1988) and the IAWA
List o| Mien.seopii Feahiii s for Hardwood Identification (IAWA Committee, 1989), except that for
the (liainetei ol intt I vessi 1 pits llh with al diinen-
opposite and sealariform pitting.

Kisi I.is
1. APIOPETALUM (FI(;S. 1-4, 8-12; TABLES 1, 2).
'
> /- bull
\i w
Growth rings ;
i . 1 .
|
1) and A. velutinum [4700], and distinctly marked
b) !ill!i- -in-aggregates and marginal axial paren i n
forming I ng< ntial lines and narrow bands
near llicir boundaries (Fig. 2) in c
[4700]; and 27 to 50 per mm2 in other samples). Vessel walls 2-7 M-m thick. Tyloses not observed. Vessel
element length (320-)620-820(-1140) [ua. Perforation j.|,ii. -in pi.1 in ni, ill in >n , |, and scalariform
up to 18 in A
Hum [4798]), and
reticulate (Figs. 9 and 10), rarely double, in
oblique iml wall-, h ter\e-se| pils alt-mate (1 ig. 1 I I.
rarely opposite to scalariform, 3-5(-6) u,m in vertical
diameter, n-uuded oi oval with lens |o slit-like a|>
crimes. \essel-ra\ and vessel-a\ial parenchyma uluitli distin. i borders: similar to intervessel pits in size
and shape (mostly scalariform in \. ,.
I L'.".|l. or iiml itrralK <>iri| < nrn 1 d:.ii/i.|.l,ill\ I., v.-itically elongated pits on the ray cell walls abut 2 to
5 pits on the vessel walls), with lens- to slit dike apertures surround e,
tures (Fig. 12). Helical thickenings absent.

\asiceiilnc and vascular Iraeheids not obsi r\ed
Fibers libriform, thick- to very thick-walled (5-22
u-m), non-septate, with lew simple lo minuleb boi
dered pits with slit-like apertures in radial walls.
Axial parenchyma scanty in A. glabmtum : * 7
and A. velutinum [4700], somewhat more abundant
in oilier spe. linens, botli paratracheal (appeals most
ly as solitary parenchyma cells in A. glabmtum
[3375] and A. velutinum [4700], or incomplete pareiiclmna -heaths n< ai u-sseU ai ethers) ami , ;.
tracheal (diffuse in A glabratum [3375] (Fig. 1) and
t relutumm | 1 ,'MIJ|. dilluse-in-aggtegates or murgin,il parenchyma (Fig. 2) in both other specimens!.
Strands composed of (2)3 to 5(7) cells.
bavs (3) 1 i:> 01 1U. per nun. urn- and rnulh~en.it. .
mostly 3 or 4 cells wide in A. velutinum (Fig. 4),
and 4 or 5 cells wide in A. glabratum (Fig. 3) (up
to 8 cells wide in A. glabratum [4798]). Ray height
coiiunonU exceeding I mm in !.. ^ttihttitiini la; lo
2.9 mm high in A. glabratum [4798]), and usually
formed mostly by square and
ell
lla
(up lo ()) marginal rows ol upright cells, and usiinlh

! -h--.nl
II- -.I -cjuare to upright shape. Uniseriate rays composed of upright cells, rarvh w\\\i
--on..- -uhlan -(jiiaie .ni'! fit. null, ut i ell-. IV- >>n
I ML- titi J v. ill <.| ra\ -'II- rounded and oval, very
small (1-2 (im diam.). Radial canals absent.
Crystals (
few (1 to 3) large prismatic crystals with numerous
!
small ones) common in ra\ cells
oat
I
square and upright ones) in A. glabratum [4798] and
! . iin ,m \ 1700], and in young parts of stem (near
the pith) in A. velutinum [3854] (Fig. 8), occurring
rarely in A. glabratum [3375]. Crystals present also
in non-chambered axial parenchyma cells of A. relutinum [3854]. Brown and yellow deposits contailied III a few vessels in both species e\amnied
. 5-7, 13M ,
,
i >
i
.
i<
II- m-l
\l S
TRALIA. Queensland: Bellenden Ker. TOO
lands (Jap, 1120 m, Plunkelt 1520: Isabella
fall-, ea. ,H0 km NW of Cooktown. 180 m. I'lm.l.rtt /. /'I
\1. macm.sciadn, (K Muell.) K Muell.: AI-S I'M-\ 1.1-\.
Oueon-laiid: without precise locality. 1100 in. Ihhunl
, I 0 ,
I I 1497 Gillies Lookout mud.
I'iunLni t.VJh: cult, in Svdne\ Botanical Garden (NSW
208585). voucher for original colleclion: Wrshm ft til. <
(At SfKM.IA. I.I I-.,,,.;,
.
Ker, Mt. Bartle
Frere; deposited at NSW).
Growth rings absent or distinct (Fig. 5),

marked by lines of marginal parenchyma.
Vessels rounded, very narrow (tangential diameter 9-31 urn in M. macrosciadea [15281] and 2052 u-m in other samples), not numerous (20 to 44
per mm* in M. confiisa [1512 and 1520]), to rather
numerous (40 to 72 per mm2 in M. confusa [1549]
and M. macrosciadea [1526 and 938], to 70 to 107
per mm2 in M. macrosciadea [1497 and 15281]),
solitary and in radial multiples of 2 to 5 (up to 17
in M. macrosciadea [15281]). Vessel walls 2-5(-8)
|xm thick. Tyloses not observed. Vessel element
length (270-)520-770(-1024) jxm. Perforation
plates scalariform with few (up to 14) bars and also
rarely simple in M. confusa (observed in M. confusa
[1549] only), or mostly simple (Fig. 14) and somelime- s-ilariform with few (up to 6) bars (Fig. 13)
in M. macrosciadea, occasionally reticulate, in
.l.t | n- ana !MII. i 'al nd walls. Intel vessel pils
transitional to alternate (transitional ones more
common in M. macrosciadea [1497 and 1526], and
M. confusa [1512]), rarely opposite, 3-6 |xm in vertical diameter, rounded or oval with slit- to lenslike apertures commonly surrounded by shallow,
groove-like wall sculptures (Fig. 14). Vessel-ray
and \essel-axial parenchyma pits with distua t borders, similar to intervessel pils in size and shape,
or unilaterally compound (then horizontally to vertically elongated pits on the ray cell walls corresponding to 2 or 3 pits on the vessel walls Helical
lliii kenirigs absent.
Vasicentric and vascular tracheids not observed.
Volume 87, Number 2
By
IIP! if---'
mm Hi!.
ion. jimwlh ring> absent. n\ial parenchyma -.canty paratraeheal and difi'ii!
tangential section. l-.Vserialo rays composed mostly of square and upright
(near the pith). Scale b
f8/
i ~ i ~ i ~i
* ' *
*3-2-2e22
Jill" Li
M7*3 *! ""1!21!3 :
I I :
? i =
f c- a.
2
I.I
|
I
*
I 1 1 1
1 s s s
1^ f22 3 f f& is |g |5
hin
Volume 87, Number 2
Oskolski & Lowry
I :>l
\niilliei nl
(>20 1.11!))
1074 23.1
(810-1390)
1321 ' 28.3
(870-1610)
1203 27.6
(870-1620)
Plunketl 1520
M. confiiMi Hemsl.,
Plunkett 1549
1076 32.2
1730 13301
i (F "-.In.
1022 i 21.0
1730 I300j
Plunketl 1497
M. macrosciadea (F Muell) F. Muell
Plunketl 1526
1013 ' 22.2
M. macrosciadea (F. Muell) F. Muell,

Hyland 15281
li, -O 1010;
\l. inacmsciadca (F. Muell) F. Muell.

Weston et al. 938
722 24.0
(420-1060)
. I,i" -ill ui I
f cell; 3, Height of rays
I.!. - bhriform, thin- to thick-walled (walls 3

5(-8) juLm thick), non-septate, with rather numerous
simple to minutely bordered pits wit] I
ertures in radial walls.
Axial parenchyma scanty paratracheal (appearing as solitary parenchyma cells near vessels), diffuse, and margin il -in In i< - t urm u n > i n ' !
tangential lines (Fig. 5) and narrow hands near
boundaries of ibe tamvth nn^s. Strands eomposrd
of 3 to 6(7) cells. Helical thickenings rarely present
(M. macrosciadea [938]) on inner walls of the axial
parenchyma eells in conlael Willi vessels (Fig. 1.3).
Rays numerous ((14)18 to 21(24) per mm), unil eells
rav.
very long (up to 20
rows), formed by upright and solitary square cells,
ml
i ti portion usually as wide as uniseriate
ones, i omposed of square and a few procumbent
cells (Fig. 6). Pits on tangential walls of ray cells
rounded and oval, very small (1-2 p,m diam.). Heheal tin. ken rj.-. iel\ ; n ,< nl in M. macrosciadea
[938] on in
I both upright/square and proeutnbenl ra\ cells in eontacl with vessels (Figs. 7,
16). Radial canals absent. Crystals not observed.
Brown and yelln
i
! in a leu to
main vessels in both species examined, and also
in cavities of many fibers and parenchyma cells of
M. macrosciadea [938].
Disci
acrosciadea [938].
; 1 mm in M. conIf. macrosciaden
iposed of upright and
few square cells. Alternation of
Very little variation was observed in wood struce within the Apiopetalum and Mackinlaya spe:s examined. Apiopetalum glabratum differs from
A. velutinum by higher and wider rays (Table 2).
Mackinlaya co
-a Jtil
from M. macroscia-
10
Figures 9-12. Scanning electron micrographperforation plate. 10. .1. irlulinum, hmry MS
plates. 1 1. A. glabrutum. hmry .W7~>. alternate i
with lens-like apertures surrounded by sru
dea by the predomini ince <l si alarilonn perforation

plates with more nu
ma, but more sani|)lcs must bo
studied before the irriportance of lliis character can
be interpreted.
Helical thickening s mi the walls of both ra\ and
axial parenclnma were obsei \ ed rarely in one >.irtiple of Mackinlaya macrosciadea [938] (Figs. 7, 15,
16). This feature generally appears in tracheal elrhrids. libers), and has also been reported very
rarely in axial parenchyma of some Trigoniaceae
(Heimsch, 1942), Ancistocladaceae (Gottwald &
Parameswaran, 1968), and Chrysobalanaceae (ter
Welle, 1975). The presence of helical thickenings
in ray cells appears to have been reported previ-
ously onlv tm I'lt^nnid *cri,va 1115k (Meimsch,

1942: 133). In the sample of Mackinlaya, helical
iliit kenin- - an \< mill n pan-ncliy ma cells adjacent
Mackinlaya and Apiopetalum can be clearly disni.'11 -In
from uric anothei on the hast- of tin n
i\ I 'ill. r. mi'- on in in several features,
rays, the ahsenc

! difiux in a<;uregaies axial parenchyma, and tli
ils in the ray and
axial parenchyma cells in Mackinlaya (Tables 1-3).
The very narrow and relatively numerous vessels,
and the 1- or 2-->
i I
l'
probably on el led \s ill the shrubby liabil ol the
species studied and the correspondingly small di-
Volume 87, Number 2
Dvl^
.1 \!
-16. Helical thickenings ii
cell. Scale bar in Figui
ameter of their stems. Other shrubby Araliaceae

such as species of Oplopanax and Astr<>l>
kolski, 1994, 1996) have mean values of vessel diameter and frequi n< v. as ,< II a;- 1 ray width, similar
to those observed in Mackinlaya. Thickness of fiber
walls, the type of axial parenchyma, and the occurrence of cryslals ii
.lis appear to reHect relationships icon than dilh lences in habit or
habitat (Oskolski, 1994, 1996), and could be of possible taxonomic value (Table 3).
Despite these differences in llieir wood II .<,
Mat l,t/>l<i..i .III> I \;>;>>i /ili,in als., -ban a number
ol -ijiinlh aril le.ilnn - I'll. s. nulml. lh. -mill in
paratrachea) and apolrachea! (diffuse and difh.sen iggregai - lh. lm> oi 11 111 ig only in Apiopetalum) axial parenchyma, non-septate fibers, a pre-
dominance of upright and square cells in the ray

composition, and brown deposits in the vessels. Although each ol dies.- characters has also been obser\ed in other genera of Araliaceae and Apiaceae,
then combined occurrence in Mackinlaya and Apiopetalum is notable for the order Apiales (Table 3)
and supports the suggestion that these two genera
are (los.lv related. Diffuse and diffuse-in- . .;
gales paienclnma is lound alone only in species of
Myodocarpus, Dclarhrca. and
<
occurrence ol both diffuse and paratraeheal axial
pareneliMiia is known only from three New Caledonian species of the pan-tropical genus Srhrfjirra
(Oskolski & Lowry, in prep.). All other representatives of Apiales examined to date have only a
siii;J< p. :cn. >'. iir.i l\ pi I In o-occiirreiiee oi apotracheal and paratraeheal axial parenchyma could
ffl
I!
lit
J
1 = 5-
EBB-
Ml
II
self's
-JJS
dd
II
111
IB .
Ill
| --- -lit
:H
IJ]
II
EB-
,*
, *
cu eu
s s
Pi
-ill
it?"
? == ;
ill
w
m If11!i!
m
nn
lis
till II
II
x e
till 3
I.
SI 111
fiff
' ib
lit HI If! I if! ti is h
Volume 87, Number 2
thus be regarded
i apomorphy for Mackinlaya
and Apiopetalum.
IJesid- - dill i-t ;n:IAidilfiiM-in-aggregates axial
parencl .ma. several other wood-anatomii d itures art- also shared among Mackinlaya, Apiopetalum, and the assemblage comprising MyodocarDelarbrea, and Pseudosciadium, such as the
presence of small trusts, pit-. I In- Jiata, ii i
or. us nowhere else within Araliaceae except in
the Australian endemic Astrotricha (Table 3), which
may also be a basally branching lineage of Apiales
as indicated l>v recent molecular sequence data
from ITS (Mitchell & Wagstaff, 1997; G. M. Plunkett, pers. comm.h I). ... . r I
.-....-i I ;-
i'iui differs s'rongh from llial of ]la>-kinhi vn ami
mi. notably in its axial parenchyma and
ray hpi -. an . ,h< ]i< -. in <ii heln ,1 llu< k. tun.',
on the vessel walls (Oskolski, 1996). Species of
Mackinlaya, Apiopetalum, Myodocarpus, Delarbrea,
and Pseudosciadium also form very thii I
non-septate fibers, which are unusual within the
order Ka< Ii of these wood characters may he a synapomorphy within Apiales (Table 3), supporting the
I
>
[>l
lliance that contains these five genera. They could likewise be
-vu.ple-doliinrphl, III lliaf lhe\ o.iai.' mdi pendeir:-,
(hill not teuelhrl) in oilier groups wilhin die ordi I
(Table 3), suggesting the possibility of parallel evontioii. \\>~
. -I
-- ! Ificult at present
because we lack - illi< lent da: i >>n U.HKI t. alii . (especially the size of intervessel pits) for nearly all
genera of woody Apiaceae.
These similarities notwithstanding, wood anaiorm
of \l,i< /,. ."<\MU and \;>;,>;;.liuir. is ne\i ttlx les*. ;,:
i- i i
rom that of Myodocarpus, Delai
Psriidtisci'idiiui!. In addition lo the eo-occurrcnee ol
hod. |. natra. li.-al and apolr.u In al idiltn-. and :l
r ggj
iaI parenchyma, ray types also
s
differ. In Mackinlaya and Apiopetalum, rays are heterogeneous. ,\ ill, hod; uprighi and sq lare a- %dI iprocumbetil i ells: ihev are homogeneous with exeln
sively procumbent cells in the other genera. Furh II M , . and Apiopetalum have brown
and yellow depos
i h<
ssels and lack radial
canals. Wood anatomy thus supports the inclusion of
these genera in a monophyletic Mackinlayeae (Table
3), and refutes the inclusion of Pseudosciadium
(Baillon, 1878, 1879), which is most closely related
to Myodocarjius and especially Delarbrea (Lowry,
1986a, b; Oskolski et al., 1997; Plunkett, 1998, unpublished data).
Using generally accepted trends in wood evolution
(Bailey & Tupper, 1918; Frost, 1930a, b, 1931; Carlquist, 1988; Baas & Wheeler, 1996) to determine
h ii i ' i . I nil . ~i MI I
iir. - n iti o|,-d as
plesiomorplue tor Muckinhiva and \piopctalum.

These include predominanl K scalar ifnrm perforation
plates and relaliveb long \essel elements, whereas
shoi'l vessel elements with exclusively simple pel
foration plates of woody Apiaceae (Metcalfe &
Chalk, 1950; Rodriguez, 1957; Greguss, 1959;
v
cl < agruber, 1990) are regarded as apomorphic.
Average vessel element lengths are 651-822 u.m in
Apiopetalum and 518-770 p,m in Mackinlaya 1fobli
1). within the range seen in most other Araliaceae,
which vary from 650 to 900 u,m. The lowest reported
averages are 366 p,m in Oplopanax horridum (J.
Smith.) Miq. and 374 u,m in Eleutherococcus sessiliflorus (Rupr. & Maxim.) S. Y. Hu, with the highest
of 1339 Jim reported in Schefflera gabriellae Baill.
(Oskolski, 1994, 1996; Oskolski & Lowry, in prep.).
By contrast, vessel elements in Apiopetalum and
I/./- ',>:'!,;\.i an di-ht . ih |oi -. i lhaii in nooih \piaceae, which have average values that are generally
less than 400 p,m. A notable exception is Heteroirborescem (Thunb.) Cham. & Schlecht.,
v.l. .. averagi vessel lengdl readies _>02 U-ltl (Hod
riguez, 1957). Wood features characteristic of Mackinlaya and Apiopetalum, such as the occurrence of
diffuse and ililtu- -m-.igy.i, -ales apoir.n heal panai
chyma types, small intervessel pits, and heterogeneous rays with
mi
. i
posed of upright and square cells (Kribs's (1935) IIA
typel. have not been reported among the woody Apiaceae examined, including species of Bupleurum,
II,', ,;h,' n', s>, i. /""/. u >>,,i \!\;>h;'l<-:>d;,i;: l".\"
gium., Gymnophyton, Asteriscum, and Trachymene
(Table 3), among others (Metcalfe & Chalk, 1950;
Rodriguez, 1957; Greguss, 1959; Schweingruber,
1990).
Wood anatomical features thus confirm that
Mackinlaya and Apiopetalum are closely related
and occupy an isolated position within Apiales, as
proposed h\ I'lunkeii r.'i'Kl) However, wood char
acleis neither validate nor refute the h
that the two genera under study are intermediate
between Araliaceae and Apiaceae (Philipson, 1970;
Rodriguez, 1957, 1971), nor do they offer a clear
indication of the g
in the order. Based <
identify any reliable s
to support a sisti
'
talum-Mackinlaya (lade and core Apia< <
ludirijj in, i uiemli. - .i - j|>l n nlv Hydrocotyloideae), as suggested by Plunkett (1998), nor
between them and core Araliaceae (excluding Myodocarpus, Delarbrea, and Pseudosciadium). However. the
die slush
ot W KMI >!lilciiire is of limited us.
ever,
s
in assessin
Apiopetalw
inlaya group, as defined by Plunkett (1998, pers.

* \
,
coram.), or between them and nearly all >l tin- other
1
'
''
'
'
''ous
Several wood characters (small intervessel pits,
third, fiK*,r walk nnn.PntptP fih*rl ,1,, ii<r>at
|,'!><'1' v ^<'"';>"< *"'^ "' IMurbtc,

(Walia.end. \ll,-rl,nia4: 169-201.
,<>5a Anatomy of t
(
|; lV ,
(halk
cotyledons. Vol 2 Clarendon Press (Moid
Mitchell. A. I). & S. J. Wagstaff. l'WT. Phylogen.
lationships of /
'
I'
and the alliance (
:.,!,.
Oskolski, \ \
"
1/
i
rarpus, Delar-
6rea, and Pseudosciadmm, as previously hypothesized (Plunkett et al., 1996a, b, 1997).
Literature Cited
Baas, P. & E. A. w heel.
I
id reversibility in xylem evolution. A review. IAWA J. 17: 351Bailey! I. W. & W. W. Tupper. 1918. Si,.- v ....1
li < ! < n cells. I. A comparison between the secondary
.mnospcrms and an;54: 149-204.
149Baillon, H. 1878. Recherches nouvelles sur les vraliees
et sur la famille Ombelliferes en general. Adansonia 12:
125-178.
. 1879. Ombelliferes. Histoire des Plantes 7: 66256.
Renthaiu. G. I8(>7. \n,li.,eeae. //,.- (,. R.-iilham X J. I).
Hooke.. Genera Plantar,,,,, I : 9.3 I -9 47. I ...veil Reev e.
Williams t\ Norgale, London.
Carl|i.isl.S. 19,",;!. Ce.mpaiatKc \\ I \.
v Springer-Verlag, Berlin.
Exley, R. R., B. A. Meylan & B. G. Butterfield. 1977. A
|
'
urn
I (i ill surfaces on wood sampies prepared for the scanning electron microscope. J.
Microscopy 110: 7.5-78.
Frost, E U. 1030a. S|
ah ifionin . . . ... 1 .. \ w I.
dicotyledons. I. Ongi
u -s,l Km. (,a/. 89: (.7-94.
. 1930b. Spcc,al,znl, in seeondaiN yvlcm , dicotvlcdons. II. Evolution of end wall of vessel segment.
Bot. Gaz. 89: 108-212.
. 1031. Specialization , se, ,,darv svlem in dicotyledons. III. Specialization of lateral wall of vessel
segment. Bot. Gaz. 90: 88-96.
Gottwald, H. & N. Parameswaran. |0<>!', Has sokundare
Xylem und die systematise-he Slellung der Aneistrocladaceae und Dioncophyllaceae. Bot. Jahrb. Syst. 88: 40-
holzer und Straucher.

Harms, H. 1804-7. Araliaceae. In: V EnglerS K. Prantl
(editors), I)u ,
in,hen III. 8: 1-62.
\\ I
.maun. Leipzig.
Hems,!,. C. Jr. 1012. Comparative anatomy of the secondary xylem in the Grun.ales and Terebinthales of
: 83 lOii
s 2: 52-81. (
I tee. 1080.
lures for hardwood identification. IAWA Bull.. .
210-332.
vribs. I). \. 1035. Salient lines of structural specialization in the wood rays of dicotyledons. Bot. Gaz. 0(>;
547-557.
X)wry, P. P., II. 1086a. A Systematic Study of Three Genera of \raliaeeae Endemic to or ( entered on New C< "
edonia: Delurbrea. Myodtxarpus. and I'seudoscuidiu,
Ph.D. Dissertation. Washington University. St. Eouis.
N1,.,,,.
IOOI
Svst. Evol. 208: 121-138.

W I \na >mv ol \ral
<
Ko-
"'"" 'J ' '

,^,-J:,
,
^1215
. 19%. A survey of the wood anatomy of the Araliaeeae. Pp. 00 I P> '" I V- Donaldson, A. P. Singh,
I! <, |; id. |.| ,
I \\
I, ..,. (cdilois). Recent
Advances in Wood Anato.m New /,-alan.l hiv-l Research Institute, Rotorua.
, p p Lowry |[ & H. G. Riehter. 1007. Swemalic
laxa
'
Philipson. W. R. 1
0f Old World t
IV'! \9: (A-15.
. |97(). Constant ;md variable features of the APaliaccae. Pp. 87-100 in N. K. B. Rohson. 1). I . Culler
& M. Gregory (editors). New Research in Plant AnatoAcademic Press. New York & London.
_. 1Q79. Araliaceae, part 1. hi: C. G. G. J. van
Steenis l-cn. n.l -. Ie 1 Ho.; Malcsiana, Sen I, 9: 1](,",. Martin... \,|l,ll. I).. \\. Junk Publishers. I he
Hague. Boston. London.
Plunkett. (,. \1. | 00 |. \ MoleeulnrI 'hv logenetic \pproach to the "Family-Pair Dilemma" in Apiales and
Cyperales. Ph.D. Dissertation. Washington State University. Pullman.
. 1008. Endemic araliad genera from New Caledonia and their implications for phylogenv and laxonom\ in \p,ales | \piaeeae and Vraliaceae). \mer. J.
Bot. 85 (6. suppl.): 151.
D. L. Sollis v\ P. S. Soltis. I 996a. Higher level
relationships of Apiales (Apiaceac and Vraliaeeac)
based on phylogcnctic analysis ol rbrL sequences.
Amer. J. Bot. 83: 499-515.
&
. 1996b. Evolutionary palterns in Apiaceac: Inferences based on i,nk sequence
data. Svst. Bot. 2 1: 477^105.
&
l997- Clar.lical..... ol llie

family-pair relationship between Apiaceac i
my.
/'/'', '^
,
,
llf
' ' l,b ;}}l- ,7,': >;-* .
"TT'1971" he relationships of the Ur
\ ' ' > <,<l ^"h Fhe B\oloJ* a,nd,
^3-91" Ac!,''lV-7,'iV. Pn'ss I'.'.nl.l N"\, w '
Schweingri.be.. I. II P'Oil \,,al.,,,e eu.opa.sehe, I
lalomv of European Woods. Verlag Paul llaupl.
>vs|ein.i Magnoliophvtorum. Naui I;.I . i. |
C. Il<>... |o:ti.
for the family \raliaceae. \cla Phvtotax. Sin. 1
129.
V i^ni-i-_ P l'U(. Ke. herclx-s anatomiques sur
's.f.eation .1.- Vral.ae.es. Ann. Sci. Nat. Bot. I
210.
CARLOS SPEGAZZINI
(1858-1926): TRAVELS AND
BOTANICAL WORK ON
VASCULAR PLANTS1
ml-, including his :

plicate! l\ lli- hick or spareil;
Spegazzini published ca. 1(H) papers on vascular plan
nbing ca. 1UOO new taxa. A list of the new genera, species, and infraspeeific la\a
egazzini was professoi
,.
>.
,
I i
iuenos Aires in Argentin
onal Department of Agriculture, first head of the herbarium of Museo de La I
nist. plant collections. Spega/.zini. travels, vascular plants.
Carlo Luigi Spegazzini, or "Carlos Luis" Spegazzini (the Spanish translation of [us name !>> which
he was recognized in Argentina and in llic rest of
the world), was a leading figure in Argentinian natural history, lor both his oncological and vaseidai
plan! studies. Sp.-gazzini ^,i> one -.1 tin ra;l significant explorers of Patagonia in terms of the volume of his collections. He also traveled and collected extensively in almost all of Argentina, from
northern Salta to southern Tierra del Fuego.
This botanist, who was atl
b
\iiniii.iti Le.la -in. < 'ii u :- a wi.ug -hid. n- in
Italy (Spegazzini, 1884a), is best known for his
work in mycology, although his vasculat plant svsleniaiics is of ccpiivalenl iiiiportance. His heibai
urn o| as( ulat plants. . ode, led L\ dims. Il and b\
other collectors, reaches 100,000 specimens (Molfino, 1929), and he described approximately 1000
new taxa during his career. In the process. Spegazzini published more than 320 papers, of which ca.
]< i
hermore, he was
a teaching piolessoi ol bo) m\. zoology, n in.: i dog\.
geology, and phytopathology . iralor ol the Mm -lerio df \gnoultuia de la Naoion bet hai u;in. iii-l
head of the herbarium of Museo de La Plata, and
founder of the Arboretum of the Facultad de Ciencias Agronomicas y Forestales in La Plata city.
Biographies of Carlos Spegazzini considering his
mycological work have been published previously
(Scala, 1919; Hauman, 1923; Molfino, 1929, 1951;
Arambarri & S|HI
l !-tails of his travels and botanical work on vascular plants are still
liiido.: im.-nlcl Tin- infoni ahoii. incladm- I ispecimens and publications, is provided herein.
BIOGRAPHICAL SKETCH
s
A detailed biography of Cai
in ha
been published by Jose Molfino (1929), a botanist
who married one of Spegazzinis daughters. We present here a briei
lm<
-p.-. izzini's life, as it
pertains to his botanical endeavors.
Carlo Luigi Spegazzini (Fig. 1) was born on 20
April 1858 at Bairo in Torino, in northern Italy. He
took courses in the School of Viticulture and EnolLI
ii" . . il in Veni.-. liah) where he graduated in 1879. There, he met Pier Andrea Saccardo
(1845-1920), professor and founder of the Scuola
Pad
(Lazzari, 1973), who would
be a major milu.
i i
reer. Soon after _
I i lm
huikm ih il I... u i
1
We are grateful lo Jorge Crisci. Conovc a Daw-on. Susan; "rem,. Mam. Iron--- I \11a-c. de La Plalal. < aista\ >
ic-lmg (In-liliilo Darumion). Hugh litis. Bob Kowal. Mark Wetler (L'ni\er-il\ of \\ i-cniisin Madison), (duseppe Mi iganelli (I nivcrsita di Siena), and frank Horsman (The Natural lliston
Ihc manuscripl. We are indebled lo Daud Hoiillord (Harvard University)
for assistance wilh Spegazzini"- infraspecilii a\a from the Cra\ Herbarium Card Index, and two anommou- re\ ie\w-ra- supported in this research by the National C.-ographie Sneielx (Cianl
igaciones Cientflieas y Teenieas (CONICKT).
ulares. Museo de l.a Plata. Pasco del Ifosquc. I<)(l() I .a Plata, \rgcn-
. 87: 183-202. 2000.
Aires Provin. i ). and prolessoi ar.il Itiri| K.t ar v dean

in tli. facultad de Agroiioima 11 inversilv i>| La I'la
ta). Two years Lilt i. Ii< u;i- ILM-M .
II i i
Department of Botany in Museo de La Plata. At the
same time, Spegazzini was a student aid v- li I
ol Agrieultun . .ht;:iriil)>: Ills .!i -I. . <.n '2'A I >eeember 1897 (Ragonese, 1986).
In 1898 Spegazzini was designated curator of the
1 l.11 iiJiii ..I die Mini-'
d< Wnciillura de la
Nacion, in Buenos Aires (currently the Herbarium
<f the histituto de Recursos Biologicos, INTA), and
HI tin- lollownig \ea! fie loliiideii llir A r Lor. turn <>l
the Facultad de Agronomfa in La Plata. In 1900 he
.. i- ippnintt i I'm! -or in the Facultad de Farmacia y Bioquimi. a. at llie I diversity of La Plata.
He was a leader in the study of agriculture in the
country. In his research in tl
Id in A
Qti
he discovered a fungus that attacks grape vines
(/'/W.M;;I,.,"> nH'-ohi). the I >.) In urn llial causes a
ilisea-r ol sinj.ii rat.i (/,',/. ,7/,;> \./.</,,/;;. alid iuiigi
falfa plants (Uromyces striatus).
During the years 1912 to 1914 he returned to
Europe (Spegazzini, 1916a) to work in herbaria and
also to visit Ins mentor and friend Pier Andrea Saceanlo On. ol h - lasl hoi inn al ... 'is ilies on I April
I'L'.i. w.i- tin I..mid ill. ii ol a -< i. -iliti< |oun al in
Argentina, Rerista Argentina <lt liolann-a. |l nlorlunatelv. all. : Sp, ga//ud's death the |oiinial ceased
pl.-ted hv otliei llali.in scientists, ^pi ga/zuii de, id

ed to move to another land. In December 1879, he
disembarked in buenos Aires harbor. It is interesting to note that the period from 1850 to 1923 was
ehara I. rized by the arrival in Argentina of a large
number of European naturalists (Ringuelet, 1960;
ILigonese. l(i;*f>i fliey came nialiih frotti (,n manv
(Hermann Burmeister in 1857, Paul Lorentz and
Georg Hieronymus in 1870, Fritz Kurtz in 1884),
Italy (Domingo Parodi in 1875, Spegazzini in 1879,
Auguslo Scala in 1909), Russia (Carl Berg in 1873,
Nikolai Alboff in 1895), Switzerland (Theodor
Stuckert in 1869), and Belgium (Lucien Hauman
in 1904).
Tli. Spegazzini story in Argentina evol\. s lion,
two ioituuale . inuinstaiiees: Ins anbouiidcd . lidiu
siasm for the natural sciences, and a scini'iln alls
young country waiting to be discovered. In the year
after arriving he made his first field trip and publishcd his first new s|!ecies ,,| vasriilai plant. Cu
bomhti austral is Speg, I Y, nipliaeaeeue) (Spegazzini,
1880). In 1885, he was appointed professor in the
liislilnto \gronomico de Santa Calalma (liuenos
disease. Ii his w II h< -i< na t ;i lh. house to science

bolanv beatini hi.-, i ame -. urn nllv hisiiluta 'If IU>
tdnica Carlos Spegazzini, LPS; Holmgren et al.,
1990). He also donated his library (ca. 6000 books
and [iap. isL - leiililn nisti umnil-. am! p< sson.il
heihann ol luni I nd va-ridai : ' nls ( \niu wnous.
1930).
Carlos Spegazzini was an active field worker

ihioiighoiir hi- lite lh.- pun. ipal e\p< ditiotis and
eolleeiitiL in- i
rlined n Table 1 and Figures 2 and 3. Only the most representative ol his
Ircqiieril . olle. hug Hips aiouud lh< . ities ,,( La Plata and Buenos Aires ar. cited in Table 1.
Spegazzini collected and also received specimens from other collectors (see Table 1) and his
own children, Etile, Propile, and Rutile Spegazzini.
His preferred area of collecting was Patagonia, the
southern lip ol \i -. i:!n a i . i;d irj M< nd. /a. NeU(|iien. Rio Negro. ( huhul. Saul I an/.. : ml 1'ieira
del Fuego (Fig. 3). The countries adjacent to Argentina, on the other hand, were scarcely visited
for collecting.
One of the first remarkable trips Spegazzini made
was in 1881, two years after his arrival in Argen
tina. On Decembei L8 he embarked as a botanist
representing the University of Buenos Aires, in the
xpedihon of Lieutenant Santiago Bove aboard the
ship Cabo de Hornos. Spegazzini, as well as a geologist, a geographer, and a zoologist, departed from
Buenos Aires heading for Isla de los Estados am
Tierra del Fuego, the si
st part of America.
After arriving at Punt;
Chile, Spegazzini,
Fuego. A storm caused their shipwreck, but Spegazzini saved some of the plant collections by
swimming to the coast and burying them in the
(Spegazzini, 1884b). Spegazzini returned to Buenos

Aires on 27 September 1882. As a result of this
adventure, Spegazzini collected 1108 specimens
(
fungi, lichens, and vascular plants). Fortys later, in January 1924, he returned to
Cabo de Hornos in Chile where he discovered very
different conditions. Tin- Native Indian populations
TT
r-T
/\ \
\
I
! V 'Li
I
1
Sierras de Cura Malal
j
:.
^
^
Sierras deTandil
!lX^V^Coloradoil2 \#
^ /
L
X ^-^JSfe^ ' <^ *"% Sierra de la Ventana
|.o|)iil;ilions ;)i ll)i
L>1<>:
mg lilies lllcrc. t!
cies (Molfino, 1929).

Some trips were undertaken by order of either
the Argentine government or commercial citities
For instance, he went to Chaco to install an alcohol
factory; to Tucuman to study the sugar cane disease; to western Argentina to analyze I In uli< ultural industry; and to noilli
. -caicli lot am! -hnls plants lh: I |>in<!iicc ruhhci. In
all these trips he looked for the opportumlv to col-
irlo Spega
Nov. 1880
Dec. 1880
Dec. 1881-Nov. 1882
1883
Early 1883
Mar.-Nov. 1883
1887
1889
1889
Dec. 1889
1890
May-June 1890
1891
1892
Jan. 1894
Mar. 1894
Sep. 1894
Jan.-Mar. 1895
i n
i-i ul ii (.1 on
>l!
IIII
< pcditio
.iih hi
nun
of other collectors vvh<
C. Spegazzini and D. Parodi; Argentina. Prov. Buenos Aires: areas surrounding the city of Buenos Aires (e.g.,
Boca del Riachuelo, Palermo, Recoleta, San Jose de Flores, Isla Maciel, Puente Alsina, Montes del Tordillo,
Montes Grandes, Montes del Real Viejo).
C. Spegazzini; Argentina. Prov. Buenos Aires: General Lavalle, Magdalena.
C. Spegazzini in Bove's expedition; Argentina. Prov. Santa
Cruz: Rfo Gallegos, Rio Santa Cruz, Salinas, Isla Pavon,
Misioneros, Cabo Vfrgenes. Prov. Tierra del Fuego: estrecho de Magadan, s. Isla I L- 'istados. Punta Porpesse,
Cabo Negro, Gregory Bay (Bahia San Gregorio), N coast
of the province, Ushuaia, Cabo Posesion, Cerro de los
Caracoles, Bahia Sarmiento, Gente Grande Bay, Punta
Anegada, Isla Isabel. Chile: Punta Arenas.
C. Spegazzini; Uruguay. Arroyo de San Juan, Cuareim.
C. Spegazzini and A. Onetto; Argentina. Prov. Santa Cruz:
Rfo Santa Cruz region.
C. von Giilich; Argentina. Prov. Misiones: Rio Piray-Guazu,
C. Spegazzini; Argentina. Prov. Buenos Aires: isla Santiago.

C. Moyano; Argentina. Prov. Chubut: Rio Carrenleufu, Teka
-choique, Rio Senguer, Lago Fontana, Rfo Chubut, Lago
Musters, Colonia Galesa.
E. Fischer; Argentina. Prov. Chubut: Cabo Raso, Puerto
Rawson, Peninsula de Valdez.
C. Spegazzini; Argentina. Prov. Buenos Aires: sierras Cura
Malal.
O. Mauri; Argentina. Prov. Tierra del Fuego: Canal Ultima
Esperanza.
A. Tonnellier; Argentina Pro
I
I R
Rawson.
C. Spegazzini; Argentina. Prov. Buenos Aires: San Nicolas.
C. Spegazzini: Argentina. Pro-. Buenos \ircs: Tandil
C. Spegazzini; Argentina. Prov. Salta: La Vina.
C. Ameghino; Argentina. Prov. Santa Cruz: Rfo Deseado,
San Julian, Canaddn 11 de Septiembre, Rfo Salado.
C. Berg; Argentina. Prov. Rfo Negro.
C. Spegazzini; Argentina. Prov. Tucuman: Famailla.
Nov. 1895
C. Spega//itn. .
Ventana in valle de las \<
Dec. 1895
Late 1895-Early 1896
E. Fischer; Argentina. Prov. Chubut.

C. Spegazzini and S. Venturi; Argentina. Prov. Salta: Cuesta
de Trancas.
i
i nl
Sierra de la
I unquist and
Spegazzini, 1880. 1914b,

1917c
Spegazzini, 1917c
Spegazzini, 1883b, 1896,
1897b, 1901c, 1902b;
Spegazzini. I Ml 7c
Spegazzini, 1883a
Spegazzini, 1883a, 1916c
Spegazzini, 1905
Spegazzini, 1897c, I
Spegazzini, 1897c; I
seus, 1915
*
*
*
Spegazzini. \'H).'
*
*
Spegazzini, 1897b,
1901c 1902b
Spegazzini. 1901c
Spegazzini, 1895a,
Spegazzini, 1897a, 1
Spegazzini, 1902b
Venturi, 1925
San Julian.
koslovvski: Wntina. Prov. Chuhul: I .ago Fnntana.
,. \ 11 ...if; Wgenlina. I'r..\. Ti.ua ,1.1 Fuego: Sall Sebastian.
:. Spegazzini; Argentina. Prov. Buenos Aires: Torn|uist. Sierra de la Venlana. Bin tie l.a Plata, Isla Santiago.
). Mauri; Argentina. IVov. Neuquen: Bio Miimiii.'-\.-iiquen.
',. Fischer; Argentina. Prov. Chubut: Cabo Raso.
:. Spegazzini; Argentina. Prov. Salla: Cuesla tie \i. a Iran
eas. Painpa Crantle. Uuel.rada tie < uiachipas. An.l.laioCa. In. Calavalc M..I .-Calavalc. \. vado tie Caelii. I,a
Vina, cuesla tie San Antonio, lsonza-Tintfn, entre TalaMontero, Colalao.
i. Ameghino; Argentina. Prov. Santa Cruz: Rio Chico
il In n,i u i, ik. Km. Ik .ok). Pago Argentino (Karr-aik).
:. Spegazzini; Chile. Prov. Atacama: Atacama desert.
:. Spegazzini: Argentina. Prov. Buenos Aires.
:. Spegazzini; Argentina. Prov. Calainarca. Prov. Cordoba.
Prov. La Rioja, Prov. Mentloza, Prov. Salla. Prov. San
Juan.
I. B., 0. B., <). P.. V. B. (sic); Argentina. Prov. Santa Cruz:
1901c
Del Villo el al.. IWi!
Del Villo el al.. I'WK
Spegazzini. 1901c, 1905
Spegazzini. 1902c: Del
Vitto et al., 1998
Spegazzini, 1901c,
1902b, c
Spegazzini. I897d.
1899b, 1901d, 1916c,
1917a. b. c. d, 1921a.
1923c, 1925b
Spegazzini. 1901c, 1902.

*
Spegazzini, 1901b, c
Spegazzini, 1898
Spegazzini, 1902b
]. Ameghino; Argentina Prov. Santa Cruz: Pan de \/ucar.

Rio Chico (Fmel-kaik, El Paso), Laguna Sera. lii.. Santa
L897 Feb. 1898
C. Spegazzini; Argentina. Prov. Buenos Vires: I,,,,,, S linen

<.s \ins \ Patagonia. San Bias, Carmen tie Palagt)iies,
mi de Picdias. Salina del I nglrs. lies Cams. | a Vide

Barrancoso. Prov. Meu<iuen: l.agt> \alinrl lluapi. I.agti
Traful. Liguna Blanca. Prov. Rio Negro: areas of Bit) Colorado and Bio Negro. Salina tie Pietlras. Puerto Nuevo.
confluence Bio l.imav antl Bit) Neuquen. Choele Choel.
Comas Negras.
:. \1o\ano: Vrgenlina. Prov. Rio Negro.
i. Spegazzini: Argentina. Prov. Buenos Aires: sierras tie
Tandil.
'. Lahille; Argentina. Prov. Chubul: Peninsula tic Valtlez.
Caleta Porfirio.
]. Ameghino; Argentina IW. Santa Cm/: Bio Chico (kumen-aik, Chonkenk-aik. cerro kmanaich. Fmelk-aik. Boron-aik, Parr-aik, Sehuen-aik), Pagt) Vietlma (Orr-aik).
Lago Argentino (Karr-aik). Bit. Sehuen (Pan aikl. Collo
San Jorge, Rio Santa Cruz.
*
Spegazzini, 1901a
1902b, c
Carlos Spegazzini
;;<>;;- i-vi, i:;<>('
. Paso de
(1, !
. Km Chill
\. Illi'ii: Vrgenlina. Prov. Chiil.ut: Pago Muster:-.. Choique
I aiiqiH-ri. Vngostura. between Trelew and Paso de los InT. Stuckert; Argentina. Prov. Cordoba.
C. Am. -I
\i
!
< I M ish-rs Prov.
Santa Cruz: l,ago \
im: iKan
uli
Ri .
Deseado. San Jorge. I-ago Buenos Aires, Collo - in |l j
Rio Chieo.
A. Tomiellier: Argentina. Prov. Chubut: Trelew. Rawson, Rio
Chubut.
K. Pahille; Argentina. I'rov. Km Negro: Colfo San Mattes.
Prov. Chubut: Caieta Porfirio.
N. Illfn; Argentina. Prov. Km Negro: Bolson. Prov. Chubut:
Pago Musters. Teka-di,|,ie. Carrenleufu. Teka-choique.
C. Moyano; Argentina. Prov. Chubut: Carrenleufu.
C. Spega/./ini; Argentina. Prov. Buenos Aires: Sierras de
(.lira Malal. Tornquist.
Late 1899-EarIy 1900

Dec. 1899-Jan. 19(H)
Dec. 1899-Mar., June
K Basaldua: Argentina. Pro\. Chubut: Trelew, Rio Chubut.

C. Burmeister; Chile. R.'o Aisen.
0. Asp; Argentina. Prov. Neuquen: Sierra de Maiehol. Valle
frolope. liio Manzano, Codihue. Pilahuinco. Kfo Kiero.
o de los BagI". >ilve~|n; \rgentiiia. Prov. Santa Cruz: Km Santa Cruz.
Lago Argentine
N. Mini: \rgenlina. Prov. Chubut: Km Carrenleiilu. between
Cholila and Colonia Kxle Ootubre.
Spegazziii
-p< îzzir
-p.-;.:i//.i,
huapi). I'rov. Santa Cruz: Km Chieo. between Km I >e-ea

do and San Julian.
K. Ilauih.il: Argentina. Prov. Santa Cruz: Sierra de los Bag-
,. Fernandez: Argentina. Prov. Neuquen: Pago Nahuel
Spegazzini. 1902b. e
,. Mini; \rgenlina. Prov. Chubut: Lago Blanco. Corcovado.

Puerto Rawson, Carrenleufu, Teka Choique, Nafofo-Cahuellu. Cholila. Manantiales.
>p
\rgentina Pt..v Kueiio> Vires: Tandil.
'. Clareu: Argentina. Prov. JUJIIV: Puna of Santa Catalina.
:. Burmeister: Argentina. I'rov. Chubut: Manantial de la
Subida. Chile. Rio Aisen.
!. Spegazzini; Argentina. Prov. Mendoza: Punta de Vacas,
road Vlendoza- Villav iccneio. road Puenlc del Inca. Laguna de lx>s Horcones, valle del Aconcagua, Cerro Leones,
Las Cuevas, Canad6n de los Horquillones.
. Lahille; Argentina. Prov. Neuquen: Fort in Roca.
I. Ilauthal: \rgentina. Prov. Chubut: Rio Senguerr.
:. Spegazzini: Argentina. Prov. Chaco: Ipaguayo.
. Spcga mi. Vrgenlu
I'M" salla K o Peseado.
Spegazzini, 1902b
Spegazzini, 1901a
*
Spegazzini, 1902c
Spegazzini, 1901d,
1917a, b. c, 1925a
Spegazzini, 1902b
Del Vitto et al., 1998
*
Spegazzini, 1916c
1904
Dec P>0| Mar. 1905
C. Spegazzini; Argentina. Prov. San Juan.

C.Spegazz.ini: \i>ienlina. Prov. JIII'IIV: Si,.rra de Santa Barbara, Sierra clc Calilegua. Prov. Salla: Rfo Pes.ado. Rio
San Francisco (Ledesma), Rio Berniejo.
Kiesling, 1994
Spegazzini. 1916c.
1917a. 1921a. 192.'
Feb. 1907?
I.ale 1907
Perico. Ledesma. ^luto. Rfo Saiicelito. Prov. Salta: Oran,

Valle dc hernia. Sierra de Santa Barbara. Santa Cornelia.
Sierra de Mar/ Cordo. Sierra de Zenta. Rio Santa Marfa.
Prov. Tueiiman: Tali. Parque Roca. Prov. Mendoza: cerro
de los Cordobeses.
C. Burnieisler: Argentina. Prov. Santa Cruz: Puerto Deseado.
C. Spegazzini: Argentina. Prov. Vlisiones: ln.ni Santa Ana to
Barracon and Bio San Antonio. Puerto Ksperanza (Rio
Parana), Posadas, Campina de \merico. San Pedro. Iranan. \.u an-(iuazii. Garupa. Arroyo Dorado. Campo de
la> Cm a-.. Ccrro Pesegueiro. Campo Grande. Cerro Bonito, Rfo Bossetti (Rfo Grande). Rio Acaranguay (Campo
Grande), Loreto, Layado.
C. Spegazzini: Argentina. Prov. Calamarca: Pie.lra Blanca.
P. Spegazzini: Argentina. Prov. Buenos Aires: isla Martin
Dec. 1909
J. Argerieh; Argentina. Prov. Riieiio- \ir.-s: 1 station Arger-
Dec. 1909-Mar. 1910
P. Spegazzini: X.ge.ilir.a Prov. Catamarea: Ancasli. Ambalo.

Andalgala, Huillapina. Poman. Rfo Tula. Prov. Mendoza:
quebrada de los Horcones. Cacheula. Prov. Salla: ^.iI11;i
Corn.-lia. Sierra de Santa Barbara. Prov. Tucuman: \lpachiri, Cochuma.
C. Spegazzini: Argentina. Prov. Klitre Rfos: Ibicuv.
C. Spegazzini; Argentina. Pmv. Jujuv: >aul;i Cornelia, Sierra
de Santa Barbara, Lecher6n Negro.
Spegazzini. 1916b.
1917c. 1923a
Dee. 1905
Dec. 1906-Mar. 1907
Mar. 1911
Nov. I'M I
1917c, 1923c, 192J

c
*
Spegazzini, 1909, 191
1917a, b, c, d, 192
1925b
Spegazzini, 1917b
*
Spegazzini. 1917a
*
Jan.-Feb. 1914
C. Spegazzini; Argentina. Prov. Mendo/a: Ri,. Blanco del
Spegazzini, 1914a
June, Oct. 1919, Feb.

1920
C. Spegazzini; Paraguay. Asuncion. Puerto Sajonia. Rio Pa.

aguay. San Antonio. Pacu-cua. road San l.orenzo-San
Spegazzini. 1921a, b.
1923a. c
Feb. 1922
Summer 1923
J. Molfino; Argentina. Prov. Vlisiones: San Javier. Apostoles.

C. Spegazzini; Argentina. Prov. Buenos Aires: Isla Marin
Garcia.
C. Spegazzini: Argentina. Prov. Tierra del Fuego: llaberton
(Shamanes), Isla Grande, Upataia, Ushuaia, Bahia
Orange. Puerto Shell. Chile. Cabo de Homos. Isla lloste.
Jan. 1924
Jan. 1926
A. Raffaelli; Argentina. Prov. Rfo Negro: S Rfo Negro. Tala-
myself to fulfill nix official l">-
*
Anonymous, 1925
Spegazzini. 1924; Mo.
1983
Spegazzini, 1926
Carlos Spegazzini
His partners on the field trips described Spegazzini as a true naiui ih-a HI . ulhu-i i-ln md r..
found connoisseur ol die flora and fauna, which tic
described in simple language, making each expedition an excitim
no, 1929; Parodi, 1961).
As a result of
iiu <
editions i
h\ Cailos Sp. gazzini and h\ Ids . o| uboia'nrs. lis
number of vascul i plants in > _ i mi - ) , ' i
ium reached 100,000 specimens (Molfino, 1929).
This i
is not su
ne bears in mind
that he was able to collect 30,000 specimens in a
single trip (Venturi, 1925). Due to the abundance
of fungi and vascular plants collected, Spegazzini
maintained the majority of them as a personal herbarium at home. Several European and North
American institutions <,. re i [. rested in purchasing these valuable collections after Spegazzini's
death, but all offers were rejected. Around 1966
(Kiesling, 1984), the collection of vascular plants
was transfered from LPS to the Herbarium of Museo de La Plata (LP), also in La Plata city.
^ . i/zini are estimated at ca. 700 specimens in LP. Staff of this
herbarium (Katinas et al., in prep.) are currently
d<-\i loping a ca;al'-gar of 11 - .. - >|-i ma ris. (Mint
main in Museo de Botanica Juan A.
i Buenos Aires (BAF), in the Instituto
de Recursos Biologicos (INTA) in Buenos Aires
(BAB), as well as in the Museo Botanico in C6rdoba
(CORD). Other herbaria with Spegazzini rasculai
plant specimens are: BAE, BR, E, H, IAC, K, L,
MICH, NY, PAC, PAD, S, U, W, and Z (Stafleu &
Cowan, 1985).
Two additional Spegazzini collections of interest
type specimen ol (>! \zof>sis hiculoi (Vald) Speg. var.

media Speg. collected by Carlos Spegazzini in 1899
should be cited: C. Spegazzini s.n. (ex LPS 12517
in LP). The name of the collector is frequently not
I. but can usually be determined by reference to the year and locality (Table 1). The date
of collection usually consists of the month and the
the year is accompanied by the
Spegazzini as "
labels of the specimens collected by Carlos Ameghino in San Julian-Rfo Deseado. There are two probable meanings for this Latin term (Steam, 1996):
(1) Ver = spring, a m iter gem ric
of die third
declension. le/>- corresponds to die ablative singular, i.e., "by the spring," "with the spring," or
"from the spring"; and (2) Vere (also vero, revera)
an adverb meaning "truly, in fact, rightly, exactly."
Following other annotations of Spegazzini as "Vere
1894" (Spegazzini, 1895b) for fungi collected in
October-November (Southern Hemisphere spring),
it seems that the most reasonable interpretation of
this term is "spring."
For some labels of Patagonian specimens, there
is no citation of the contemporary political provinces. From 1878 to 1884 the Argentine territory
south of Rfo Colorado (ca. 40S latitude) to Cabo
Goboniaoion i
Only in
1884 \
renl provii
lofLa Pampa, Neuquen, Rfo Negro,
Chubut, Santa Cruz, and Tierra del Fuego. Another
problem with some of these Patagonian plants is
with the specimens collected by C. Moyano in Chubut in 1899. As Moyano did not write the corresponding labels, Spegazzini annotated the labels
with probable localities. As he explained (Spegazzini, 1897c):
tographs al ca< ti. The rolled ion oi living types H

practically lost, except for one specimen of Cereus
still growing in his house, now the institute (Kiesling, 1984). His collection of cacti photographs
that correspond to type and non-type specimens
(Kiesling, 1984) is deposited in the Herbarium of
i (LP)labels are annotated by Spegazzini or
, with a few referenc<
to the locality. He used the initials C. S. for t
plants he collected, and other initials to differe
tiate other collectors: C. A. (for Carlos Ameghin
N. I. (for Nicolas Illin), T. F. (for Tonini del Furi
of Spegazzini's herbal
The type specimens frequently have tin original

Latin descriptions made in Spegazzini's I indwril
uig Mui if ih.!'- npli..u were written directly in the field or during the specimen preparation (Fig. 4). It is also very common to find the
J***,^ &C^- v. /W*r-*~-V.
-/, ^/&*^fi*~~~ tê*--*-?^
botanist's accompan .,, ,!, -. i

, liaracterized by
their precision and simplicity (Fig. 5). Some sets of
the original ^]>. v
1.1 lln-li iln n- in housed in
BAF, as is the case with some cactus species (Kie-
sling, 1981). The eiia

<>l more than one speeimen and locality in the original laxa descriptions
(species, varieties, and tonus) is common, and
therefore Spegazzini's type collection is mainly
Volume 87, Number 2
'
<HM?,
made up of syntvpes. Tvprs air housed in a scparate collection in LP, but it is probable that some
types still remain in the general herbarium. The
search for these specimens is another step in the
production of the catalogue mentioned above.
Sl'K(. \//l\Ts
PI
r.l U \ 11> >\S
Carlos Spegazzini published 332 papers from

1878 to 1926, and ca. 100 refer to vascular plants.
Almost all of them were published in such Argen-
Table 2.
New taxa in then
(DIM
I .
|IH!HI
nl
.1,
(Anonymous, 1997). and the Gray Can! Index Database.

in parentheses. Spcga//.hii i- I iu- .a
h< iil;.
l.<<
'.
iL
-|
mi
,i- . m-d
in lnde\
Kccnsis
The number ,.l lava ,1.>. ribed in each taxonomic category is
.f all name- excc|il where marked. The designation of comb, illeg., comb.
nov., comb, superll.. Iioin. illeg.. noin. illeg..
inval.. noin. nud.. and a change in the aiilhoritv of the name other
than Spega/zim l.narked with *) follows Znloaga et al. |1WI) and Znloaga & Morrone (19%. 1999a, b).
AIZOACEAE. Species (1): Tetragonia ameghinoi Total (1).

Al.ISM ATACKAK. Species (1): Kchiiindnrus palogoni, us. Total (1).
AMARANTHACEAK. Genera (11: Amarantellus. Species (1): Amarantellus argciinus.
\ma,anthus cristulatus, A. vul-
gatissimus, Amarantus edulis. Infraspecific taxa (1): Blutaparon portulacoides var. commersonii*. Total (6).
AM WW I.I.ID \,
\l.. Species i.vi: Zephuanthes l,l,i, ,a. Z. melanopolamica. Z. oxilepala. Infraspecific laxa (2):
,,'.!
'
,, /
|,
, |
. |
ANACARDIACEAE. Species (U: Lilhrea chiclnloK Svluuus cbichila. S. /ongifolio ll indl.) Speg. comb, nov., S. praecox. Inlid-pei IIK
lax
,u<a. Total (5).
APIACEAE. Genera (1): Notiosciadium. Species (1.1):
comb. nov.. M. patagonicum.

I <>, in
d
no,
<
\sicnsaum Jimbriatuni.
\otiosi ludium ;>
,/,
t le a
M'OCi \ \( |
\I. ralentinii.
Lorella ameghinoi, A. bold, A. fuegi-
^>nt, a
Inhaspcilu
taxa I h
.,
ana var. patagonica. Total (18).

\|
Species :>J:
I mi
ii
\spido\perma chakensis. A. crotalorum. A. horeo-kebracho. A. missionum. Rauvolfia
i i
'.o-blanco var. pendula. Total (6).
AQUIFOIMCKAK. Species (I): Ilex lucumanensis no,,,, nud. Total (1).

ARACEAE. Genera (1): Lilloa. Species (2/: Lilloa pitki. Staurostigma vermicida. Total (3).
ARECACEAE. Species (2):
Maximilian,, aigenhnasis.
M. orenocensis. Total (2).
ARISTOLOCHIACEAE. Species (2): Aristolochia melanoglossa.

\SCI.I I'I \lt \( I
\l
(.i n
i I i
l>
s. , ,
\. ttuckertii. Total (2).
j.
latum siiarcolens hum. ill.-g.. 1 incchnicun, b,
ita;:u,hii. 0\ \pe
I ml
:axa (1): I'hilibertia gilliesii var. pubescens.
To-
tal (6).
ASTERACEAE. Genera (2)
,:;.//-,,
.'
1//".
'
,,
:,anoi
'
minlcm
i
\
palogoni, it^
'
H. struthionum. H. tehuelches. Hieracium tliub

inoMitiai.
I'I
)l
puirb
'on,,i.
,
ISIS.
stiuthm
//. m\anoi, H. mustersii. H. patagonicus,
, phala. I., patagonica. Mutisia chubutensis, M.

\. chubutensis.
' ,
V. patagonica.
V. pentacaenoides. I'ei,
' ,
>
_ >'',
>
\ chubutensis. S. colu-huapensis. S. diabolicus. S. inutilis. S. julianas. S. music,MI. S. sagittal IOI, Strongylomopsis juegiana. \ernonia oreophila. Infraspecific taxa (37): Baccharis trimera var.
< liiliotit, bum .,
var. l\pica. Chm/uirogo argent,;i var. dusenii. Krigeron gayanus var
I,o
t I'd,,
leptopi
Hi,-on,
i
IOI.
"
'
ana var. integri/'olia (Seh. Hip.) Speg. comb. nov.. H. rariegata var. acutibracteata. H. rariegata var. glaucescens,
II. i allegata var. nana. II. inriegata var. typica. //. rariegata var. pinnatifida. h-uceria ibari var. glahiata. i. ibari
iciiata var
azorelloides
var. tehuelches. S. iiijimaiiis var. pentada,I \lus (I'hil.l Speg. comb. nov.. .S.
axillaris var
contractu. A. pata-
uiidhowlan var. oraneosula. Solidago
linearifolia var. brachypoda. Total (97).

UK(.()M \CEAE. Specs (I I: /!ron( a.genluwnsis.
Total (I).
BIGNONIACEAE. Species (1): 7-om arellanedae. Infraspecific taxa (II: -Ir^/iV/ polentillaefolia var. australis. Total
(2).
cpsi, aides. Hchinosp,
trichium diffusion horn
///. Heliotmpiitin lithosperinifoliiini. Oxyosmyles ri.scosissima, Volenti

Speg. comb. nov. Infraspi cli.- i.i .. ;
\mM,iel,ia angustijolia var. /
lii, kV>|!
( I
\l
i , MM
(Ji
I)
comb, nov., Z>. #/<//
-,
sis, D. glebaria Speg. ex 0. K. N

*
inil
I/, ,-/,
//' î,,11,1,1
>
'
''
I, l s
-\
"i
,,
'
li
i i
I!
I I
ihiibiilrn-
. '<//</ spru
<-\ ().
) Speg. comb, nov..
il
alum
Kubscan
'(wsn var. ma/or, D. karr-aikensis
Gil
5p
<
II
>
BROMELIACEAE. Specie ((>):
luopoi/mi
/^
I I
mo.
,
^,
II
'/<//
i-
,
^
'
ii
"^
..
>
>
!>
u,
h h<,>m
var. media, O. karr-aikensis var. minor, /J

I
/.', M
...
i
>/</)/.' '
pi>, >lu
hi
ml
7<uiir var. subgla_
"
xltibrum, S.fuegian - \ n
uluticum. S.
1,77m/e,i thvrsigera, Puya flora, P. formosa, Tillandsia chlorantha, T. euosma, Vriesea
CACTACEAE. Genera (4): Aylostera, Brittonrosea, Maihueniopsis, Parodia. Species (113): Auslrocactus dusenii*, A.
interteMic.
s>>
i -
B. lamellosa, B. la,
ill
.in1
luosa. B. arrigens, B.
,'
',
'
'
h,>t, r,n anthd.
m//;, B. violaciflora,
'
'(/s ,y/n hnialiiiiL
E. baldianus, E. cachensis, E. caespitosus, E. mtiimanmsis horn, ill.-g.. E. chionanthum, E. famatinensis. E. hae-
nuscula, E. uillm
Cvmti
'.
, unzzinu K. Schum. ex Speg.*, Erailea bruchii, F. odieri, F. pulcherrima,
' ",, "
'',..,,
/.,,'
"-
i -i
O.i.
, i
,-',,."'!.;,.. .,',,
,.'
>
,
"
'.
.'
.,". /
,,;,',
I,
',;,.
,<//, M..
/, ,
,,,!
il
.-,
'
/'
-/-.
' ,.//,',
o, ",l,l '
><
"
i
n,
'
(I
-A
f>
I
'
Ma,luiouiop
l>i>ntirrnsi\
,
V,./.VM//-
, /
!,.,.,,,,!,
(1
-p. -. comb, nov., f? poro/,
ml
U\a (35): Cereus
i on nodes, E. i
'
'
lioHua
"
.'
.,//, ,,/,;
'
I
n
I Speg. comb, nov., G.
,"..'.;. .
i>
i- .
;/ "c
"7 ./ '
/' ..
',,,',..-
.i
(Speg.) Speg. comb, nov., ?*'/>/;'

I o-ipuh Id on
,;
ill
,,,<<
f> ,""..'/.,
>'
i -|
i
l
"
in,i >< ,
-|
,--'- s, ,
HI
,',<,,
gon. Speg. ex Moss,
,//,,
dimlenuita \;ir.
.',')!. i.'iiona
i
puis
nlomeratus sax. iner-
mis, T. glomeratus var. oligacanthus. Total (152).

CALYCERACEAE. Species (12): fioopis ameghinoi. Ii. rluihuiensis. II fdifolia, B. leptophylla, B. patagomca. B. raffa 11
( < 11 >
I
i |. <
',
II
i i
II
i _'
'i
>
'
' >. ,
'
II
i: Downingia pusilla*. Total (1).
lutnisis, N. patagoni
oliu Mihiuidiim \;ir.
Table 2.
Continued.
CARYOPHYLEACEAE. Genera (I):

ubutense (Speg.) Speg.
< '.
.
Hi i | . ill.
(I'lnl ) S| i; ,,i,,|, tlo\ . IT/..:"
Philippirll,,. Series (7): Lychnis urgent,na. I., chubutensis. L patagonica, Meeomb. nov., M. patagonicum (Speg.) Speg. comb, nov.. Philippiella patagonica,
l.i\;i 11 I): Arenaria serpens var. andicola*, Arenaria serpens var. micmplnlla
,<>
i ,
,
\ i.h l-|
il
! <
/s \ n patagonica
Mil \n|Mi|i|\i I \l Species I IK) \tiiplr> amcglnno, \. argent,na 1. esposlo, 1. flarescens horn, illeg.. A. frigida,
\. macroslyla. I. mendozuensis. 1. platens,s. \. robuslu Speg. num. mid.. 1. sugittifolia. A. rulgalissima, Chenopo, i ". / C unlarcticiim (Hook, f.) Speg. coml). snperfl., C.fuegianum. (.. scubncaule. Hahnbergia tweedii
l\1..ri>siiilcs Viii
ides \&i chilensis* ( ambrosioides vat graveolen.s: (Willd.l S|
ml).
nov., C. ambro\ii,
n /v/xra, C. scabricaule f. megalospcrma, C. scabricaule f.
. '/
.
lohtisla, Isrchea fruticosa var. hrachxphylla. Lfmticosa var. megalospenna. Salicornia
eorticosa var. procumbens, S. eorticosa var. /v/xoi IK.MI. m\al.. ,\ huh,,,.a \.u <l,>,;,ngii i\.<>n-n\/ \ Niederl.) Speg.
comb, nov., S. fruticosa var. macrostachya. Total (38).
CONVOLVULACEAE. Species (3): Convolvulus phiigena. C. plain,,;,!,,. Ip,,n,ca .ugentmensis. Total (3).
Kl.ATTNACEAE. Species (I): ^//i;ie ////.*. Total (1).

ERICACEAE. Species (3): Pernettya chubutensis, I' paiagomca. I', piulippiana. Total (3).
Kl CIO Pill ACEAE. Specs ( I i: Eueryphin palagomca. Total (1).
EIPHORBIACEAE. Genera (I): WHW/. Species (<)): WAe/i" patagonica. \porosclla chacoensis (Morong) Speg.
cum. K *///'''< ' salicormoides (Speg.) Speg. i

M triphyllum, P. rallis-pulchrae. P. rillositm. Pirottantha modest a, r
ca, Pterocarpus valentinu. Ram,e
,m argenttnen\e. \uchellia
Arn.) Speg. comb, nov., Eiria platensis, V. sent ell,,
na. Iiilraspecific taxa (64): 4c<
var. panic,-ps. A. praecox f. armata, A. praecox f. inermis, A. riparia var. argcnlinensis. Adesmia filipes var. o/rtim./ I lnt,d,s\.u nonnalis \ lol,nd<\\M pctiolulala. A.
laic,ides \.u />/)/<(/ 1 palatini,a \.n ',.;.ml>. nov..
I. ngidiim vai >>,,
I ,..,:,,,:
II
-/ s
I nniiip'i \.u Icjouupa
\.
'tat,i \ar. glaberrima. //. trifoliata \ar. glandulosa. H. trifoliata var. microphylla. //. trifoliata var. nor/.
'i/(/.s CKVVU \;u. patagonica. /,. magellanicus \ar. glances,-ens. I magellan
icus var. owplnlla. I ,
,
.
.. w ew> var. normalis, L
Volume 87, Number 2

2000
1. inn n,it[i,i 1
Katinas et al.
Carlos Spegazzini
197
! i\jui(i I lutea f. aroma (Gillies ex Hook. & Arn.) Speg.
pal I idiflora. V. vicina var. tricolor. Total (164).

EEACOURTIACEAE. Species (1): Hanara glandulosa (Desv.) Speg. comb, nov. Total (1).
ERAPNKEM \CE\E S|
Inlia-pecifii tiiv.i |.'i|: /

(V; miiroplnlla \.n
i
!
Inuita, F. microphylla v
co. Total (6).
GENTIANACEAE. Species (1): Erythraea ameghinoi. Infraspecific taxa (5): Gentiana magellanica var. darwi
|Ste<l.) Speg. eomb. nov.,

II \IOIMIVr\<:E\H. Genera ill: llaloplntu,
HYDNORACEAE. Species (2): Prosopanche
var. hetl/rciiiidii. I', burmeisteri var. w/zwr. Total (4).
IR1DACEAE. Spec n .
chiiim striatum vat ;> ; , ,!.,. (I'ln I Sp,-g o>mb. nov. Total (4).
JUNCACEAE. Species (1): Luzula patagonica. Total (1).
.11 \C\GIY\CK\K. Species (1): Tnglodun monanllws. Total (1).
LA MlACI \l Spec n -,
ln(r.i^p-c tin la\a(l):.
.i Utuoniiiia danrt
nom. inval.. 1/. ,/,'inm, ur. nrcsccns. Total (7).

LENTIBULARIACEAE. Species (1): Ihnculana plalensis. Total (1).
LILIACEAE. Genera l_'l ',,, ^p<<i.-.|7l limdiaea amcghtnni H palagoni,
s
illcg.. Schickendantz,(,
"
- .eg.) Speg. comb, nov.,
phytlum. T. pulchellum. Infraspecific taxa (2): Hrodiaea patagonica var. angustdnba. Tritrleia /
gustiloba. Total (11).
LOASACEAE. Species (1):
pinnatifida var. gracilis. Total (.'<).
LYTHRACEAE. Species (1): Pleurophora
MALVACEAE. Genera (1): becanophom. Spec
(l'hil.)Speg. comb, nov.,
(Micron I Speg comb, nov., S. tefiuelcfu ! S I
specific lava (4): Sphaera
MARTI VIACEAI Species I I: Craniolaria argeniina. Total (1).
MELASTOM \T\CEAE. Species (1): CVmWw platcms. Total (1).
MTSODENDRACEAE. Species (1): Misodendrum patagonicum. Total (1).
\1<)K \< I \l Spec .-(II /
Inliaspecilu laxa (I ) liiostiuiuu ,
i '
Total (2).
MYRTACEAE. Specie. ( 1): Chpimmhrs lillni. (.'. ,.mV/n7. /V,,^,,,,, -;///,. A.', pcmrcbi Parodi ex Speg. & Girola.
Infraspecific taxa (1): Tepualia sdpularis var. philippiana (Griscb.) Speg. comb, nov. Total (5).
WVII'M \K \CE \E. Species I I I: Cahomhn austmhs. Total (1).
:ies (1): Oenothera pygmaea. Infraspecific taxa (3): Oenothera odorata var. glabrescens, 0. odor:cies (11): Chloraea albo-rosea Kraenzl. ex Speg.. (,. ,-hu-a Speg. ex Kraenzl., C. cholile.nsis
C. hookeriana Speg. & Kraenzl.*, C. hystrix Speg. & Kraenzl., C. phoenicea, C. pleistodactyla
']. praecincla Speg. A Ki .
I /,
.
autantio-lateritia. ResiSpeg. & Kraenzl. Total (11).
4): Plantago carrenleofueiisis. P. oxyphyl la, P. pulrinata. P. tehuelcha. Iii('r<ispt>c-ifittaxa (10): Plantago nun
i
I' m>i"hm<i vai wano-,,! " P mantima var. pauciflora, P.
nnosuros var. /m/u. ^ mw-M/ms var. latifolia. P. nnosuros var. tara.xacoidrs. P. patagonica var. gracilescenS, P.
patagonica var. minuscula, P. patagonica var. /V/HCH nom. inval.. /^ pauciflora var. taraxacoides. Total (14).
I'll \1B\GI\ACKAK. Species (I): Static- iHitagonivn. Total (1).
I'0\(4\l Sp.-cn
12) I
'1 mo\anoi. \. p\nigra. 1. santacritzensis \ tehuelcha.
'.,.'.. I
.
i - .,/, s/ (7. w/A</. Cortaderia dioica (Spreng.) Speg. comb. nov.. Grxptocblons spatacea nom. nud., Deyeuxia ameghinoi. I), freticota. I).
, E. leptostachyus, E. patagonicus, Eestuca chubutensis, E pampeana. I. p\mgca. I:
, Glyceric, antarctica, G. fuegiana. G. U
, , 1
. , .- .
5'
'<
<, -s|.t g comb, nov., OryJO/MW bicolor (Yahll Sprg. comb, IHH.. '>. <iiiseba,hn. O. hachelii ( \rochav.l Speg. comb, mn.. C^. lasiantha (Griscb.) Speg. comb. nov.. (A Irjocarpa. <>. lejopoda. <>. napastaeri.sis. <). ovata. 0. panicoidrs (I^rni.) Speg. comb. nov..
0. ruprechtiana (E. Desv.) Speg. comb. nov.. 0. stipaidrs (Tri... K Itiipr.l Sp,-. <-.>nih. nov.. (V. tuberculata (E.
/^ rnnacra. P. puiigioiiijolia. P. \agamca. Sarastana antarctica (Labill.) Speg. comb. nov.. Spartuia patagonica.
Stipa ambigua, S. ameghinoi. S. urcacnsis. S. aicchai alctar. S. argrntina. S. argrntinrn.sis. S. bariornsis. S. brachy
lespitosa (Griseb.) Speg. comb. nov.. ,S. c, '
\ chm ensis S. coidobensis.
, S. dasycnemis. S. iaacilis. S. b\psophila. S. hvstericina. S. jujuyensis. S. juncoides.
S. Irptotbrra. S. Iiulans ((.n-cb.l Speg. comb. nov.. N. mol/inoi. S. nana. \ mibicola. S. arropbila. S. pampagran
s
dvnsis. S. pamp'uii- <.-,,> N pwlanlba.
N
S. piiclclirs S. sanliu
|
d. 1
S
ilaevis, S. tehuelches, S torquata S uruguaycola,
(Desv.) Speg comb run [nfraspecifi< taxa (73) lm>/i'.v
airoides var. ftaeeidifolia, A. moyanoi var. mayor, .4. moyanoi var. plicatifolia, A. moyanoi var. puberigluma. Bromidium andinus var. scabrivalvus, Bromus andinus var. scabrivalvus. B. coloratu.s var. rinpara. B. unioloides var. /u'r-
. Irjocarpa var. /
var. braclnn
rlala. P scab, n.l,
w \ai. brachvsper.< s bra, li\, hae-
imnor. S. plumosa var. gracilis. S. plumosa var. f/nv/Vv/. N. pluniosa var. micnna. S. setigcra var. bi.spidula. S. xctigera i. pallida. S. setigcra I. puipurascrns. S. setigcra ('. versicolor. S. speciosa f. m_;or. .S. sfieciosa var. minor, 5.
tenuis var. argentine (Speg.) Speg. comb. nov.. .S. /,v////.s var. />/<//. .S. terwis.sima var. oreoplula (Speg.) Speg.
lasiopoda. I', tnagellaniciim var. pubiflara (Steuil.) Speg. comb. nov.. 7! niagrllanicum var. secunda (J. I'resl.) Speg.
i (Speg.) Speg. eomb. nov. Total (6).

POLYGONACEAE. Species (3): Goccoloba argrntinrn.sis, Eriogonum ameghinoi. E. bonarren.se. Infraspecific taxa (1):
Pt>l\gonum speclabile var. patagonica. Total (4).
PORTULACACKAK. Specio Ci): Cabnulnina chubutensis, C. i
petala, P. platensis. P. rasa, Tali,am paraguayense. Infraspecific t
oleracea var. mac/anil*
! >. .
u ;-,,, , -. >'.
I l,,h ! I i.
Table 2.
Continued.
RAM NCI I \( I !
-}
I.I
IN
(Speg.) Speg. coml). nov.. R. pcduncularis var. albojfiana. Total (12).

RHA\1\ACK\K. Species (1): MM,/,/ ,,,,,/m,,*. />. r,,.w,/ (Miers.) Speg. coi "
Speg. comb, illeg.. I), intcgrijalta. Intr.isp.-cilic ta\a I ll: Collctiu jerox var./
carpa, C. lineata var. mclanocarpa. C. lineal,i var. xanlhocarpa. Total (8).
ROSACEAE. Spe( it- (l()i I. <
am, xhinoi
\1. ,',
nov.. T. ameghinoi (Speg ) Sp, g < oml. run lull i>p. . iln
IIX.IIIJI
\, a,
1/
<spt t; ) î" t:
">ma
< oml.
\ pinnatifida
villosa, Margyricarpu.s sctosu.s var patagonna letragln, /,,-

lawtarpa, T. acanthocarpum var.
lasiocarpa, T. acanthocarpum var. leiocarpum. T. acanthocarpum var. w.
,/-;///; var. /v/xra
nom. inval. Total (22).
RIBIUI \l Spe< es ( I ) Orconolus iialatio) cus I nh i-|" < ill- I i\.i I I I (iulium aparinc vai pscudoapaiin, I.II- ' i
Speg. comb. nov. Total (2).
S\\1M)\CI \l (,. n, ... .1.- Ucchamlfiaio. Species (1): Irec/iarafetoia uruguayensu. Total (2).
SANTAI \( I \l S|
s (2) li
ii/ i a iiataaonica MU.
tandilemis (Kuntze) Speg. comb, nov., Quint ha
i
n ink nov.. (>. chilcn.se
var. ffiajus (Brongn.) Speg. comb. nov.. (> i//,/.,,
n
< / tun (li.-i
-< comb. nov. Total (6).
SAPOTACEAE. Species (2): Sideroxsion ligustrinum. V muiijolium (Mart.) Speg. comb. nov. Total (2).
SAXIFRAGACEAE. Inlraspccilic laxa |3>: Saxijmga caespitosa MU: paroni,. S. magellanica var. trilobata, S. trigyna
var. patagomca. Total (3).
SCHOPHl I.ARIACEAE. Infinspecfio laxa VlY. Cntcrohnia hrllidijnlia var. angustijolia. C. lanecolata var. glabrata.
Total (2).
SIMAROUBACEAE. Species (11: 1'icasma pah amargo. Total (1).
SOLANACEAE. Genera (3): Benthamiella, Panlacantha, Saccardophytum. Species (27): Benthamiella aeuttfalta. II.
-;;:ii'v//;!/./f,s. /'
iong:j:'ha. >
puitig->;if;:
p i ,;././;. //-./.-/.v.
.'
palagnia, a. ( >,/,;., aiue.jhi lh:, is
Speg. comb. nov.. f.
dophyton p)cnoplt\'
>
< ha Infraspecific taxa (7): Fabiana patagonica
var. brachyloba, F patagonica var. foliosa. F. patagonica var. gracilis I', patagonica var. ni/ni/. r\ patagonica var.
IV/HWI num. inval., Nicotiana alpina var. deserticola. A. r///x>i</ var. patagonica. Total (37).
TR(l'\lM)l \CKAK. Species (1): Tropaeolum patagonicum. Infra-pecilie laxa ill; Tiopueohun polvphvllum var. mc(.surn. Total (2).
VALERIANACEAE. Species (7): /V,v//i7,.s ,v,rm. /> clanonijoUa (Phil.) Speg. comb, nov., regu/aris, 5a/kariac/oita i\ahli Speg. comb. nov.. \atcriana honanensis. \. chubulensis. \. moyanoi. Infraspecific taxa (3): I'hvllaclis
YKRBKNACKAE. Genera (I): l/my>vreH. Species (I.",): /,i/V>/ ,/r,i7-//i7 (Benth. & Hook, f.) Speg. comb. nov.. Mon-
tandilensis. Infraspecific taxa (3): l-'''-...

1 //ura var. angustiloba, V. flava v
Total (19).
VIOLACEAE. Species (I): Viola argcntincnsis. Infraspecific taxa (5): V/o/ nuiculata f. calliantha. V ma,
tenuifolia. \. microphvlla (.fimbriate/. 1. mtcrophvlla I. maeropoda. I. microphvlla f. micropoda. Total (
Xil.orih I l.\CE \E. Specie* 111: //urn, unwghinoi. Total (1).
nCOmill ACKAE. Infraspecific laxa (1): Lxopodium scariosw
<li II .1- Mi-
I I I
,
,
,
'.-, /,,arm var. ai
l
otal
nei
i , .
inl is
laxa .01 \l
tinian journals as 1 . <

- . x
Argentina, Comunicaciones del Museo Nacional de
Buenos Aires, P/n s;
u <l /.'. > .- .'. ' /'..- .,''/../ '.
Agronomia de la I n
.
\
il ,1c LAI Plata.
There are two papi i istii
ll<TS|
i i
I \\\:
I
.K one ranges from 1878 to 1919 (Scala,
1919) and the other from 1919 to 1926 (Molfino,
I ** * 1 In -ubn <
^>-_i mi's publications are
diverse: algae, fungi, vascular plants, anthropology,
I
ml nn i> n
(I
k on vascular plants
deals Willi agrit ulture. (lorislies. morphology, paleo

botany, phytochen i~h\. phv|o| lliology, taxonomy,
lanical travels, and xylology.
Although his taxonomic work on vascular plants
in Cactaceae (Senet, 1926; Kiesling, 1984), Faba. ear. Oi hidaceae, and Poaceae. As mentioned |.\
Hauman (1923), his publications of new taxa have
been subject to criticism because many erf them
were based on la\a already deserihi d by oilier hi i
anists. Table 2 shows a total of more than 1000
names at the rank of genus, species, variety, suhvariety, and form 11I.
- . //ini new names
in Index Kewensis (Anonymous, 1997) and the Gray
Card Index Database. Relevant literature (Zuloaga
et al., 1994; Zuloaga & Morrone, 1996, 1999a, b)
has been consulted for determining the current stathem resnhed in illegitimate or invalid names, or
illegitimate, superfluous, or new combin itioi
more detailed analysis of the vascular plant names
published by Carlos Spegazzini will be obtained
with ihe production of ihe type speeimens catalogue
(Katinas et al., in prep.).
Carlos Spegazzini made some local fioristie studies, mainly wrthi
ie Provh
(hi
\
such as in La Plata eilv, and in ihe mountain ranges
of Tandil and Ventana. Although he started the first
floristic study of the flora of the whole Buenos Aires
Province, he did not finish this work.
Most of his travel accounts were first written as
reports loi Ins sponsoring institution, and lh< n usn
alls published ill eonletuporarv journals. His accounts ol the hips were thorough ami amusing, with
plerilv ol details ranging from lus salary to the pi s
iogeographv of tin- area. When he died, manv publications remained unfinished, e.g.. a new issue of
Rriisln !<g,'7'/<;--. /. tint,mt'-ii. n onogiaphi<- >l Ilnfamily Commelinaceae in Argentina, a monograph
i I ili. genus /',.>,;.., (fabaeeae), a work on the
genus Snifi-io iAsleraceae). a floia ol I'aiagoiua.
and a . :ilalogue ! lli< vasculai planls oi Argentina
with their scientific and vernacular names, including the Indian names (Senet, 1926).
Carlos Spegazzini was a hard worker who published practically every year of his scientific life,
with 1925 being his most productive (with 20 papersl. just one veai before his death
Carlos Luis Spegazzini was an influential force

in th<- bolanii al community of Argentina. As a professor he nurtured enthusiasm anil dedii ition
aim ng his students. o\|, riding his influence beyond
bolarucal iiislnn lion and < neourageii i nl Inspired

by his knowledge of agriculture, he helped to solve
many serious pest problems in Argentina More
x
gazzini's fascination with l'ata.
I
him to the creation of one of the most interesting
and ompleli colic, tinns :1 vascular planls oi 1 his
pari ol tin woiltl i li- licih [I'liirn of v asculai planls
malion that contributes t

day loss of biodiversity. His work has been pivotal
I
.1 science in Argentina and a
genera
lis
-i im e ot plant
. i fun I systematic*. Those in the botanical comiiiuiiitv wilt, km i% 1 : rlos >pegazziru i-rnphasi/.-d his
eleai iiilgment, accessibility, and sense of duty.
The Institute and Arboretum in La Plata, his lectures, his publications, and prolific herbaria form
the (lackbont ol tin ! gacv of * ,arln- Spegazzini. an
llah in hot .ni-l who livid Wintina as his own
Literature Cited
Ano.ivnio.is. 1925. Movimiento social. I'hvsis (Buenos
Aires) 7: 135-138.
. 1930. Inauguration del Museo Spegazzini Re
vista del Museo tie U Plata 32: 387-394.
. 1997. Index Kewensis ,,n (.1) Horn, version 2.0
for Windows. Oxford Univ. Press, Oxford.
\raml.am. \ \ *\ 11 \ >,.in.-di I""., I nlns | ms Spegazzini: Micologo. Revista Museo (Argentinal 2; 15 17.
Del Vitto. A.. L. \1. Petenatti X M. \. Con,;! I '<',.
Argentina. Pp. 167-265 in M. N. ( on. a (tin ) Flora
Palag.uii.-a. \ol ,", l\T\. Km
\in-s. Argentina.
. Physis (Buen.
L. C. Barnett (Editors). 1990. Index Herbariorum. Part I, The Herbaria
of the World. .", ,-d. Bemium Veg. 120.
losses. C. C. 1915. Algunas planta* d,- Cab., has,,
(Chubut). Plivsis (Buenos Aires) 1: 534-540.
Ciesling, R. 1984. Recopilacion, en
todos los trahajos o refereneias s
eadas por el Dr. Carlos S
Ouilmes. Buenos Aires. Argentina.
-. 1994. Hisloria del eoi.oeimiento de la flora sanjuanina. Pp. 8-15 in R. Kiesling (editor), Flora de San
73. Sli.nadella Mieologia Italiana. Ltl. Ai

urnia S. A. S., Trento, Italia.
. Carlos Spegazzini: Su vida y su obra. Ai
. Argent. 108: 7-81.
. Semblaii/.a del doctor Carlos Spega/.zir
Ragonese, A. 1986. Desarmllo de Ins esiudms botanicos

. imesiigaeiones sobre pastizales naturales en la Reptiblica Argentina. Ed. Libro del <;. til .nai i<>. Buenos
Aires. Argentina.
Ringuelet, F. J. 1960. Bosquejo historico de los naturahstas e\trati|er.)s en \i t;e,ii ma. Unlet III del I .aboratorio
de Botamea. I'aeullad de \gmnomia. I nhersidad \acional de U Plata 4: 3-67.
Scala, A. C. 1919. La labor cientffica del doctor Carlos
Spegaz/ini. Anales Sue-. Ci. Argent. 88: 231-237.
Senet, R. 1926. La labor del doctor Carlos Spegazzini.
Diario La P.ensa. edieion del I ,|e agosto. Buenos Aires, Argentina.
Spegazz,,,,. C. L. 1880. Planlae aigenlmae novae vel eri-
. 1905. Flora de la provineia <le Buenos Aires.

Anales del Ministerio de Agricultura, Scccion Biologfa
Vegetal I: 1-161.
. 1909. Al traves de Misiones. Kevista Far.
Agron. Univ. Nac. La Plata 5: 9-95.
. 191 la. N.biv algnnas parasiias lauero-'.amiens
de la liepnbli
i ill
ti-il - Sic Ci. Argent. 77:
3-8.
. 1914b. Notas y apuntes sobre plantas venenosas
para los ganados. Anales Soc. Ci. Argent. 77: 159-164.
. 1914c. Li
1 i > \
i nueva variedad de
.-audio. Anales Soc. Ci. Argent. 78: 71-73.
. 1916a. Una nueva cspecie de Cachi\u\o del
Peru. Pl,>.sis (Buenos Aires) 2: 241-244.
' '< ' I"

i ' "' NIIIIII i \neri.ae instralis. Anales Soc. Ci. Argent. 16: 1-16.
!
I- I 'in
|.II
illt eollezioni
botanichc tatte in Patagonia e nella Terra del Fuoco.
Pp. 3-16 in S. Bow. Kappnrlo. (.eimva. Italia.
. 1884a. Costumbres de los Patagones. Anales
Soc. Ci. Argent. 17: 221-240.
forme C. A. Agard var. andicola Speg. n. var.). Physis

(Buenos Aires) 2: 282-283.
. 1916c. Algunas Orquidaeeas argentinas. Anales
Mus. Nac. Hist. Nat. Buenos Aires 28: 131-140.
. 1917a. Ramillete de plantas argentinas nuevas
o interesantes. Physis (Buenos Aires) 3: 37^17.
. 1917b. Ramillete de plantas argentinas nuevas
ales Soc. Ci. Argent. 18: 3-16.

. 1895a. El polvillo de la caria de azucar en Tucuman. Revista Azucarera (Buenos Aires) 16: 5-29.
155 179.
. 1917c. Ramillete de plantas argentinas nuevas
o interesantes (conclusidn). Physis (Buenos Aires) 3:
.
lM7d. Fspigando en el hcrbano. Ini|>tenia \
li'.'W). I'lanlae flei hiegiam a Caioln Spegaz/

1882 colleclae. Anales Mus. Nac. Hist. |N
>s Aires 5: 39-104.
1897a.
32/33: 591-633.
[897b. Plantae Patagoniae auslralis. Kevista
ron. Univ. Nac. La Plata 30/31: 485-589.
. 1899a. Nova Addenda ad Floram Patagonicam.
. 1923b. Nola sobn \l|i s ,1, 11, -, i Iii .,.

Aires) 7: 135-138.
. 1923c. Acaeieas Argentinas. Bol. \, ad. Nae.
Ci. 27: 162-334.
. 1924. Kelacion de un paseo hasta el Calm de
Tandil. Id. Sessc, Larranaga y Renovales. La Plata y
. 1925a. Slipeae platenses novae v. criticae. Revista Argent. Bot. 1: 9-51.

. 1925b. Calliandras Xigmlmas. Kcusta \rgenl.
Bot. 1: 180-199.
. 1901b. Slipeae platenses. \nales Mus. Nac.

Montevideo 19: 1-56.
. 1901c V i
1! ii I i i 1 1. I i.n 1 ii
ni ill
Bot. 1: 111-117.
Stafleu. F. A. K IL S. Cowan. 1985. Taxoiiouu.- I.ilcature. Vol. :,. pp. 77() 78.-,. Bol,,,. Scheltema and Hol-
. 1901d. Plantae novae nonnullae Americae Auslralis. III. Comun. Mus. Nac. Buenos Aires 1: 312-324,
343-350.
. 1902a. Nova Addenda ad Floram Patagonicam.
II. Anales Mils. Nac. Hist. Nat. Buenos \i.es 3/4: 135
308.
Stearn. W. T. 1996. Botanical Utin. Timber Press, Portland, Oregon.

Yenturi. S. I(>25. Superehenas Spegazzmiaiias. n pains \
mas pains. Miguel \ ioletto v Cia.. Tucuman, Argentina.
Zuloaga. F (). & (>. Morrone (Editors). 1996. Catalogo
de las plantas vasculare* de la Kepublica Argentina. 1.
1
Pit iidoplisl i. (,
i
. i
'MI i . [ ii . I*. u >
tralis. I. Comun. Mus. Nac. Buenos Aires 2: 46-55.

. 1898. Sobre una nueva enfermedad del lal.acu.
Oh ma Oman . \; u ! .1. la i.e. in. i i ,1, Buenos \i-
\
11 i, .,,) 1999a. Calalognde I.
tas vasculares de la Repiiblica Argentina. II. A
eeae I'.uplmi l.iae. , | I lirnl \ ledoneae). Monog
Bol. Missouri B..I. Card. 74: 1-621.
:<
iK.lilun,! ;')',h C;,|; =!,,,
nl.i', wiM-lilillr- <lr la lu|ullira \i;aai| i na
'. a. A,u [ Ir.llar a- (Da'c-I". !. Imparl \ln .
. \li^.Miri Hot. (,anl. 74: (>2.V12W.
PHENETIC SIMILARITY
PATTERNS OF DIOECIOUS
SPECIES OF POA FROM
ARGENTINA AND
NEIGHBORING COUNTRIES'
ABSTRACT
Dioecious species of
I'IXI
an rn
Dioicopoa, are found

I ... '
present treatment < . ,
!
species and three \ai
pattern among species based on Iui<
i \ \mencdn with a total of 41 taxa in South America. 1 1 in North America. 2
, .
n .1
'
,\. and I iiiguav I'he

I'luiU-scven taxa (34
n waled a phenetic
p.-( i,-, a-, well a- specie-, ( ornplexe-.
ein. Bivariate analyses showed other non-linear patterns of variation. These results, together
dtulws. weie used to selec l diatmo-h. . h IU.-I- N.IIII In
!
I
ui|or source of species
.,. ,.),.:!
Poa L. is one of the largest genera within Poaceae, including over 200 species according to
Hartley (1961), Nicora (1978), and Kellogg (1985).
Additionally, Clayton and Renvoize (1986), Soreng
(1990), Watson and Dallwitz (1992), and Anton and
Connor (1995) mentioned 400 to 500 taxa within
Poa.
Poa is distributed worldwide, particularly at high
altitudes and latitudes in both hemispheres; the
taxon is largely absent from low areas of tropical
regions (Hartley, 1961). It is a recognizable, welldefined (Clayton & Renvoize, 1986; Nicora & Riigolo de Agrasar, 1987; Soreng, 1990), and monophyletic genus (Hartley, 1961; Kellogg, 1990).
Interspecific variation in Poa is due principally
to quantitative diagnostic characters (Kellogg,
1990). Discrete morphological variables are mostly
unreliable, often varying widely with the environment, and even within a single plant (Kellogg,
1985; Riia, 1996). Species are frequently grouped
into complexes based on their morphological similarities. These species complexes further comprise
different chromosome numbers (Akerberg, 1942;

Kellogg, 1985). Taxonomists who have studied the
genus (Bor, 1952; Marsh, 1952; Torres, 1969, 1970;
Vickery, 1970; Nicora, 1978; Moore, 1983; Kellogg,
1985; Tateoka, 1985; Edgar, 1986) agree on the
difficulty in delimiting taxonomic boundaries within
Poa. Clausen (1961) and Soreng (1990) both consid
ilil i
hromosome number
itI
j<>-M()n as well as
apomixis. Pin i
rticity as stimulated by
environmental variability also obscures species delimitation within Poa (Vickery, 1970; Giussani &
Collantes, 1997).
Breeding systems are highly diverse within Poa.
Perfect flowers are typical, but dioecism, gynomonoecism, and gynodioecism are also found among
American species (Anton & Connor, 1995). Apomixis on exclusively pistillate plants or facultative
apomixis on perfect flowers are both well documented (Connor, 1979, 1981; Kellogg, 1987).
Evolution of dioecism within Poa could have derived from gynodioecious species, following species
1
I am grateful to Universidad de Buenos Aires (UBA), Institute de Botanica Darwinion (IBODA), and Consejo
Nacional de Investigaciones Cientificas y Teenieas (OOMCKT). which supported this research as part of my Ph.D.
dissertation. I acknow
, , .
I.. I
..
- . n lh< i.-< an h and critical comment- on the
manu-c npl. O \I. II- I . .
n u I i
u-,. ii|.| \1 |{ i oil
I
r
i il I
. I , i . . i
and E. Nicora who encouraged this research. I am grateful to the curators of B \ \. B \B. CORD. I.P. LPB, and SI for
specimen loans. I als. ! i i
i.
imenK and \ u
>
II loi her careful reading
ions !li
li
i . - manuscript.
' lii.iiluto <!> Botanic;. Darwiiron COM' I- I. L.h-ml -u 2(10. Camilla <|e Coin o 22. San Uidio ! I <> 42). Buenos Aires.
87: 203-233. 2000.
migration from North to South America (Anton &

Connor, 1995). Dioecism is well represented in the
Americas: 11 dioecious species are distributed in
the Northern Hemisphere, while 41 range southward. These South American species were generally treated as Poa subg. Dioicopoa (E. Desv.) J. R.
Edm., although Soreng (1998a, b) considered them
within Poa sect. Dioicopoa E. Desv., to conserve
Poa subg. Poa as monophyletic. In order to maintain a uniform treatment of the genus Poa, the taxonomic delimitation proposed by Soreng (1998a, b)
and based on a phylogenetic approach will be l<
lowed.
South American dioecious species are mainly
distributed in Argentina and Chile (Marticorena &
Quezada, 1985; Zuloaga et al., 1994). Parodi
(1936) and Rosengurtt et al. (1970) cited three endemic species for Uruguay: P. arechavaletae Parodi,
P. uruguayensis Parodi, and P. megalantha (Parodi)
Herter. Smith et al. (1981) and Longhi-Wagner and
Boldrini (1988) mentioned one endemic species in
southern Brazil: P. reitzii Swallen. Nicora (1995)
described one new species from Paraguay, P. pedersenii Nicora; and Hitchcock (1927) and Renvoize
(1998) cited one dioecious species in Bolivia, P.
buchtienii Hack. Although it was originally intended herein to consider all South America] p< ies
of Poa sect. Dioicopoa, some taxa were not included
due to the lack of materia] or difficulties in the
identification of doubtful taxa, especially with Chilean material, and endemic species of Uruguay and
Brazil.
Partial taxonomic revisions of some South American taxa (Parodi, 1936; Torres, 1969, 1970; Nicora, 1978; Moore, 1983) used quantitative characters as diagiii>-ti
<
lliough there was
much overlap in their character ranges among species. Differences in pistillate floret hairiness were
also utilized for species classification, with staminafc specimens, wliicli are neneralh tdaln ous, dis
counted (Nicora, 1978).
The aim of this study is to analyze the pattern of
morphological variation within Poa sect. Dioicopoa
based on pistillate and staminate plants. Grouping
from multivariate analyses was used to look for sim
ilarity among taxa and this, along with
tu rj
ol
types, helped circumscribe species and establish

synonymy when necessary. An identification key is
presented as the result of numerical analyses. This
key is based on groups of sel< cted charai ters thai
are strongly correlated, while unique i
were only used when they presented cons
discontinuities.
cies and liner van. !i< s was analyzed. A lisl of species is presented herein as Appendix 1 at the end
of this manuscript. Species in
ed
i
derive from the following regional taxonomic treatments: Nicora (1978) and Moore (1983) for Patagonia; Torres (1969, 1970) for Entre Rfos and
Buenos Aires, Argentina; Parodi (1932, 1937,
1940, 1950, 1961, 1962) and Zuloaga et al. (1994)
for Argentina; Hitchcock (1927) and Renvoize
(1998) for Bolivia; Smith et al. (1981) and LonghiWagner and Boldrini (1988) for Brazil; Marticorena
and Quezada (1985) for Chile; and Parodi (1936)
and Rosengurtt et al. (1970) for Uruguay.
Three hundred seventy-s
,",00 s
, lln ..
were analyzed and i.yarded as operational la\onomic units (Oil si for numerical analysis (Appendix 2). The number of specimens considered per
species van.- , md ,I.J, hi their n presentation in
herbaria. Some endemic species are represented l>\
e other widespread spej or more. Types of all
taxa were seen, and most of these were included in
the numerical analysis. Only types of Poa bonariensis (Lam.) Kunth, P. iridifolia Hauman, P. lanuginosa Poir.. P
Rendle, and P. stuckertii
(Hack.) Parodi were not recorded. An attempt was
made In cover lh. i i.l lanue ol umrpholo-m al variation used \>\ earhei a it hi is to disci muriate lava.
and to reflect distributional range for all species
considered, Voucher -pe. linens arc deposited in
the following herbaria: BAA, BAB, CORD, LP,
LPB, and SI.
Forty-four morphological characters, including

anatomical and
< haracters, were
measured I'm (Ins numerical analysis Oi these. 2(>
are quantitative multislate characters and 15 are
discrete variables (see Appendix 3). Most of them
were considered diagnostic in previous la u mi
studies (Torres, 1969, 1970; Nicora, 1978; Moore,
1983). Others were added to increase the character
\.y. :
l.ral
tion from the blade midregion. Epidermal characters represent the average of 10 measurements trorn
the abaxial epidermis 1 the leal blade midregion.
Epidermal and anatomical characters follow the
a Ellis (1976, 1979). Rej measured on the tallest
plot with the OTUs linked by lines representing

their minimum total distance (Clifford & Stephenson, 1975). MTS was performed on dissimilarity
matrixes derived from taxonomic distana
ffi-
Ills.: |;iMI\ \Ttn\ \\lo\<: ' \\o\o\lle KNTITIKS

I'h.-lit tic similarities were examined by principal
component analysis (PCA). This ordination techii' ,in ri pr< 8( tits distances between major groups
more accurately than any clustering method
(Sneath & Sokal, 1973). A correlation coefficient is
suggest* 'tor mixed data with predominantly quantitative multistate characters (Crisci & Lopez Armengol, 1983). Numerical analysis was performed
transformed by the Pearson-moment correlation coefficient on a similarilv matrix, which was used to
obtain the principal components. The basic data
matrix is deposited in the Facultad de Ciencias Exaetas \ Naturales, I niversid.nl de Hucmi- \ires.
Argentina (Giussani, 1997: appendix B), and is also
available from the author upon request.
PCA analysis was repeated several times in order
to drtc( I different morphological patterns nilhin the
spe( -s idii ! Inward his Jill lent steps of multivariate analysis were followed:
(1) A single species or M; nlai ~|
... . were recognized by means of PCA.
(21 l!ach species or species group was characterized b\ the contribution of each character to the
first live principal components.
(3) Distinctive species or species groups were
separated and le-arialvzed to recognize another variation pattern.
l I) Species that were not initially delimited were
Taxonomic groups were first defined by PCA and

then considered as a priori groupings foi I
Lm
inant analysis or DA (Sneath & Sokal, 1973; Affifi
& Clark, 1984). DA was performed to identify levels of certainty within previously recognized groups
as well as to sell > I li ign S|K >I U I lers ! i-. I m
stand.lidi/eil < oclln KM I- ol the c;
ru.-.il oi labh i >
I- i mi ni n .1 -is
'i
those characters
that contributed mosl to the variability of the first
five components of the PCA (r > 0.5) and that had
the least correlation among each other (r < 0.5)
were included. The only discrete characters analyzed by DA were those of diagi os
ueforpi
vious classifications (Torres, 1969, 1970; Nicora,
1978; Moore, 1983), but quantitative multistate
characters were preferred.
The empirical method (Affifi & Clark, 1984) was
used to estimate ^..odn.-ss of ht of tin elassiii, allot
, lla ,lis<
re-analyzed until all taxonomic entities assorted

into species con
.
.
dependent species.
Invariant characters were removed before PCA
nd standard deviations for quantitative

as well as mode for discrete variables,
laleil loi each sp. i ies ,md species comi were plotted to reveal
to the relatively low variability seen in the first five

prim pal
imp mi nts. For this purpose, a Euclid ii lis a - . ii itrix derivirii>, from the first five PCA
axes was compared with a similarity matrix by a
eophenetio correlation coefficient 'Sneath X Sokal.
1973). Two dissimilarity matrixes were obtained
based on two indexes tav.iii.rrni distan- - < oeffi
i ill ml M mhatl n disl m .
ilh rT, and rM the
hi..- -ol ,1 A I! ,hll |w/, \a..aliori of a single

character was also analyzed to considi
I
phism between pistillate and staminate plants.
Thus, averages of pistillate and staminate plants
ven
I i . I I'.i II
t I sis was used to di
te. morpholoiiji al paltern> based on different liai
acli'i combination-, \lter numerical :II!,IKM> were
cophenetic correlation values, respectively. Of

these, only the highest scored value is presented.
Minimum spanning tree or MST procedure (Gower & Ross, 1969; Rohlf, 1992) was additionally
used iii ! van me the sin ilarils relationships amorii!,
OTl s. Tins distance tree was imposed on the PCA
completed, diagnostic characters were selected,

and a key to identify species or taxonomic com!
s manually constructed.
Numerical analyses were made using either
NTSYS-pc (Rohlf, 1992) or STATGRAPHICS (Stalistical (Graphics Svstem b\ Slati--lieal t.raphio
Corporation, 1992).
Taxonomic groups were selected based on the

distribution of OTUs in the first five axes of PCA,
-in* c distort! >i of these axes was less than 10%.
The Poa dolichophylla Complex, the Poa bergii Complex, and Poa schizantha. Ordination
of all 376 OTUs on the first five axes, utilizing 44
characters, would account for 52.4% of total variability \lili
small
variability, PCA distortion was low: rM = 0.92.
The first three principal components showed two
groups of similar species. Axes I and II show the
!'>>,, floliriiniihviia complex, conlahimj. /' di>'ii<J>i,>
/)/r>//./ Hack., P. pilcomayensLs van ruin a idea Hack., P. stuckertii, and P. iridifolia (Fig. 1).
These principally grouped along the negative edge
of axis I. From anaKsis of clini
r loadings. Ifi
are characterized by long leaves, blades, and
sheaths; plant stature over 50 cm tall; broad blades;
long and broad panicles; numerous vas. it him
dies with sc lerenchyma girders on both abaxial and
ada\ial epidermis; short and ': in:, ale ligul. -.
groups of sclerenchyma cells extending on abaxial
and adaxial . pidermis al hladi aa: in: small slon at: : anil diorl spikeh 1-.. - nines. Ilnrets. and lod
The seeond species group was defined by axes
I, II, and III and comprises three taxa: P. bergii
Hieron. var. bergii, P. barrosiunu Parodi, and P.
s li'.,i;.'i.>i 1'i'odi ^Miiiiin,- li mi these species
clustered at the positive end of these axes (Fig. 1).
Thev also present long leaves, blades, and shealhs.
tall ['hints, and long panicles. However, these spe us a, distil g ii.vln ..: h.an ill. pie\ ions gr mp h\
longi : hgnles. :hi. k- : blatl. s. laig. i stomata. longer spikelets, glumes, and Hon
n
...
ing on the first glume, as well as numerous vascular
himdles witl -el. : ncl . ma girder- on|\ on abavial
. pideimiThe second group was analyzed separately. PCA
was performed on a subset of 33 OTUs based on
39 morphologn
bergii var. bergii,
P. barrosiana, and P. schizantha share some attributes that were revealed as invariant characters before PCA was performed: long rhizomes (HAB 2,
see Appendix 3), no viviparous florets (FLOv 0),
- tHAIbet 0), no
vascular bundles
Giussani
Phenetic Patterns in Poa Sect. Dioicopoa
palled J:-. :SISI 2] Tlie>e iirsl fixe components

accounted for 55% of total variation; meanwhile,
distortion of PCA was low: rv = 0.93. N m uillun I hi /! .Vvfr'
complex was also sappotted. h;ia:-t- 2 dam- < 11 "I
distribution on the first three prir.eip I . omponer.ls.
el.ara U rizi groups Sp.-i a- within I /'. a'o/a /a;

I ".. a .inplex have wide leaves and blade mai<iin>
Poa i lizantha falls on the negative end of axis I,

and toward the positive ends of axes II and III. It
is clearly defined by a smaller plant size; smaller,
narrower, ami :hniiin IM\< -,. -an ;|l r lertile structures; long and rigid callus hairs; and convolute
blades. Il also has -mallei -iontala ual hull form
cells onl\ -ditdtlb i a i dilier. nlial. <l trom :>f:na
epidermal .-i-lls. \ il ai <lu rphisin between pistillate and staminate plants of the P. berg} < >mpl<
was also distinguished, ['olilla'c specimen-, -- .
ciate with the positive end of axes I and III: they
are larger plants, with more hairy florets than sta-
thinner long cells. These groups appeared a] propriately classified by discriminant (unci
s.
Kightv-eighl pereetil of specimens ol (lie /' tloli
i omplex, 85% of the P. bergii complex,
and 100% of P. schizantha correctly assorted to the
a priori groups.
Discrimination among taxonomic entities. The

Poa dolichophylla complex, the P. bergii complex
\i. <><t^:; .111.1 l> !i,ii',<sia:in>. I'. <> i, o /"/'a,', and a
remaining group of miscellaneous species comprised the four a priori groups for an initial discriminant analysis. Standardized oneftieieril val les
tor the Iirsl ihree canonical variables wen- us.d 'o
with a group of sclerenchyma cells extending on

the adaxial and abaxial epidermis; the P. bergii
complex has iiaie blades, -heaths, lemmas, stomala.
as well as numerous glume nerves. Poa \./-.;:,;a//, >
erized by intermediate ligule, lemma, and
Mar -uhiia. Inii; speeim. ns oi |he /' a <!><lirl>

plex, and P. schii mi llie original data matrix, the 302 remaining specimens were re-analyzed with the
original 44 morphological and anatomical harac
ters. The first five PCA axes accounted for 49% of
total variability; in spite of this percentage, distortion was low at rM = 0.89.
OTU distribution on the first three axes of PCA
discriminates three groups of species (Fig. 3):
GROUP A, constituted by P. bonariensis, P. buchtienii, P. calchaquiensis Hack., P. lanigera Nees, P.
'".,'./ /' \ui>rihtm\. ;
j),i!(io(,i)icii var. nciiqiiina \icoia. /' pnlrrsfnu. I'.

nsi.s Hack., /? montevidensis \rechav..
and fl resinulosa Nees ex Steud; GROUP B, coni- us.
I
-|H-I inn n- .il
'iguluris Nees ex
Steud.; and GROUP C, which includes P. alopecurus (Gaudich.) Kunth, P. boelckei Nicora, P. pogonantha (Franch.) Parodi. /
(Speg.) Parodi, P. superbiens (Steud.) Hauman &
Parodi, and P. tristigmatica E. Desv. ex Gay.
Analysis of character correlation with the first
three PC \ axes revealed that species of Group A,
placed uii llie positive end ol a\i- 1 and tin iies;ati\<
end of axis III, are charade
lades;
idumes. florets, and lodieules. I,roup \\. on the positive end of axes I and III but the negative end of
axis II, also has shortei s|iikelels and Hon is. h || is
distinguished by its longer ligules, filiform leaves,
florescences. Species of GROUP C aligned on the
ii
livi end of axis I but the positive end of axis
II. These species are distinguished by their larger
spikelets, jinnies, and Hotels; wider, thick, i blades:
additional vascular bundles with sclerenchvina
girders on both abaxial and adaxial epidermis; and
priori groups used for the

n
(DA). Specimens assorting to Group A and B separaled alotij; the ins1 :\mniiical uniable. Tbev are
i/ed by long blades, long hairs along lemma nerves, and sharp leai bla
ipices. Spi ii iioi ( iroup i ', arc distinguished b\ longer -luttie> /',,,.,-;.< v separated by the second canonical vari1
l< i- I - i n II by a long ligule and numero is vascular bundle- vvi'h scleteni livma jj,itders
only on the aba
'.roup A is also
eri/ed
-ociated with the
second variable. All groups were assigned by the
classiliealion procedure with the percentages of
correct classification being 86%, 90%, and 80% for
The Poa bonariensis Complex, Poa lanigera,

Poa pilcomayensis var. pilcomayensis, and the
Poa resinulosa Complex. Species assorted
within Group A include P<><:
111 tiH, l". Clllci),! jmrl.S.S. l" /:,'<;-,7 I. /! /,
sis, P. patagonica var. neuquina, P. pederseni
pilcomayensis var. pilcomayensis, and P. r
Tll.ll pin hellc rela!lonsfii| - urn- II \i st e.llcil In
: Patterns in Poa Sect. Dioicopoa
PCA. A data matrix was based on 84 OTUs and 4

variables. Only 1 character out of the 44 was ir
, ii ni tin bsence of viviparous florets (FLOv (
see Appendix 3). The first five components ac
counted for 53% of total variability. PCA distortio
was low, being rM = 0.94.
A plot of the first three principal
showed four distinct groups of species (Fig. 4). The
P. resinulosa compl. ons -I- ol P. buchtienii, P.
P. bonariensis, P.
Two other groups each consist of two independen
taxa, P. pilcomayensis var. pilcomayensis and P. Ian
igera. The P. resinulosa complex, located at tht
negative end of axis I and the positive end of axis
III, comprises specimens of relatively small stature
with small stomata, narrow blades, as well as short
el spikelets, glumes, and florets. The P. bom
complex distributed to the positive end of axes I
and III. This complex includes rhizomatous, larger
plants, with longer stomata, wider blades, as well
as larger spikelets, glumes, and florets. Vascular
bundles with sclerenchyma girders are more numerous in blad<
ross section I \m pilcomayensis
var. pilcomayensis and P. lanigera both fell at the
negative end of axis III. They share flat, narrow
blades. However, P. lanigera i
i i , -! .
ilo
the first principal component by its longer glumes,
Ilords. and spikelets than are seen for P. pilcomayensis var. pilcomayensis.
S[.1 nn.iis within the P. resinulosa complex, inP. calchaquiensis, P. pedersenii, and P. resinulosa, were separately re-analyzed.
PCA revealed a sexual dimorphism among speciindividuals presenting smaller
late ones. The first five PCA axes acco
54% of the whole variance, and the cophe
rel
oefficient showed a low PCA disl
.itrd
among OTUs \
This P. bonariensis group distributed on PCA axes
I, II, and IV and was also sustained on a minimum
spanning tree (Fig. 5). Staminate specimens, in
smaller spikelets, glumes, and florets, as well as
less hairiness on these florets.
Discrimination am
priori groups for DA corresponded to those obtained from PCA: (1) P. bonariensis complex; (2) P.
resinulosa complex; (3) P. pilcomayensis var. pilcomayensis; and (4) P. lanigera. Two groups were separated along the first two canonical variables. The
d by a rela
ely long ligule ind subconvolute blades. The P.

;x is characterized by large panicles and glumes, wide paleas, numerous silii
suIn rose paired cells, ami vasculai bundles will >rlerenchyma girders on the abaxial epidein
pilcomayensis var. pilcomayensis and P. lanigera
aligned along the third canonical variable. Poa lanigera has broader paleas and hairier lemma nerves
ih in l\ pilruttia >>'nsts. Piscriniiuanl clarification :!
the a priori groups showed a good fit: 92% of specimens for the P. resinulosa complex, 90% for the P.
Iiitriiiricnsis (omplex, ^"I'A lor l\ iiilconiaycnsis. and
75% for P. lanigera were correctly assigned. Some
misidentified specimens of the P. resinulosa complex associated with the P. bonariensi* compl
Others off! pilcomayensis were related to /' lam
gera. Some specimens of P. lanigera intermixed
The Poa alopecurus, Poa j

Poa tristigmatica Complexes. PCA ordination
of specimens of Group C revealed two species
i:ii.iipiii;l-. Tli. !'<>., j>i:<'ii'iiith.i ...iiipl.x ( en>i-N.
of P. pogonantha and P. prichardii, nrfo n as specimens of P. alopecurus, P. boelckei, P. shuka, P. supcihtcns, and /' InsJiîwit;',, lall into the second
group. OTU distribiiiion (Fig. <>l is based on PCA

axes I, II, and IV. Analysis of character loadings
revealed that sp<
- . ; i
,< P. pogonantha
complex are characterized by viviparous florets and
I-mi; pauiel.s. but ie\\ liave selneiielivnia girders
associated with vascular bundles. A second species
grouping features larger plants, longer ligules, as
well as longer glumes, florets, and lodicules. The
first five PCA axes explained only 47% of total variation. Nevertheh s- iis= list ution remained low, rM
- 0.87.
Specimens of P. alopecurus, P. boelckei, P. shuka,
P. superbiens, and P. tristigmatica were individually
analyzed. Ordination along the first three principal
component axes revealed two groups of species
(Fig. 7): a P. tristigmatica complex with two species, P. boelckei and P. tristigmatica; and a P. alopecurus complex including P. alopecurus, P. shuka,
and P. superbiens. The P. tristigmatica complex associated with the positive end of the first component
axis due to smaller plants, leaves, and fertile structures. The P. alopecurus group principally located
at die opposite side ul axis I. associated with target
plants, leaves, and fertile structures. Pistillate and
it i: it<
(> it u i
>i P. boelckei and P. tristig-
Volume 87, Number 2

IV
Poa pogonantha complex
tf-.
/ m -"IJjJfcr-'
<*^>
Ki-Mire <; Seon.l -.-I ..I i-:iiIli-,;irK;I. a;;,
oftoniintha. P. iiriclinnlii. P. siiuka, P. si>t-rl>
iHinpl.A |l'<;. 111!: i> Hratlv .lUliii}.iiisli-<l li
'lot of 76 imimilii.il- - '

|<
urns. P. horhkei. P.
I P. tri.slifimalic<i) on the I. II. and l\ l>< \ axes. The P. pogonantha
remaining species. See I i n,
-i i- n i i - xplanation <>l labels.
matica differentiated on axis II (Fig. 7). Pistillate

plants present wider glumes and florets, longer lodicules, and thicker blades than staminate specimens. PCA distortion was low, at rM = 0.92, although the first five axes accounted for just 49% of
total variability.
When based only on specimens of the P. pogonantha complex, PCA revealed morphological differences between pistillate and staminate individuals. Pistillate specimens have hairy calluses, hairy
lemma nerves, and vascular bundles with scl< renchyma girders on both abaxial and adaxial epidermis. Staminate sp rim .- nguished by having more nerves on the first glume and
well-differentiated bulliform cells. The first five
axes accounted for 57% of total variabilis illi
PCA distortion being low, rr = 0.92. Only three
variables, navicular apices (API 1, see Appendix
3), no vascular bundles with few sclerenchyma
cells (SCLin 0), and group of sclerenchyma cells at
blade margin not extending on abaxial and adaxial
epidermis (CAP 1) were invariant and removed
from the matrix before performing PCA.
Discrimination among taxonomic entities. DA
was performed to discriminate relevant groups
emerging from the second ordination set. A priori
groups were delined as: 111 the /' ,V .A :<,/. "/.';< --' - "t"
plex (P. boelchei and P. tristigmatica); (2) the P.
pogonantha complex {P. pogonantha and P. prichardii); and (3) the P. alopecurus complex (P. alopecurus, P. shuka, and P. superbiens). Characters
that best reflect specific differences were selected
lull
iiig; s i lard
ti ii'tits (if canonical variables. The P. tristigmatica complex is characterized by broad glumes, paleas, and blades. The P.
pogonantha complex is defined by long spikelets in
- i
.n with viviparous florets, and long blades.
Finally, the P. alopecurus complex has more n >d< s
on the panicle along the principal axis, as well as
more nerves on the first glume. These groups classified correctly: 91% were related to the P. tristigiiiplex; 82% to the P. pogonantha complex; and 96% to the P. alopecurus complex.
Specimens of species previously analyzed were

, from the data matrix. The 121 remaining
OTUs were then considered for this subsequenl
study. PCA was performed; the first five components accounted for 48% of total variability. PCA
ii
a was low, r, = 0.91. A group w
lifb-r
entiated along the I, II, and V axes, including P.
bergii var. chubutensis Speg., P. boecheri Parodi, P.

hubbardiana Parodi, P. lanuginosa, and P. patagonica Phil. var. patagonica. According to their
character loadings, these species have longer
leaves and inflorescences, wider and thicker
blades, and larger stomata than the remaining spe
lair ami <lauinialr >|ccimi-iis of /' Inihhanana as

well as the P. lunii^niosa <-triplex I'islillalc planls
arc more- robusl. with Iniii;. i spikclt-ts, ^lumrs, am!
florets, with these florets being distinctly hairy.
The first five components accounted for just 52%
< 1.1*1. (.
Poa hubbardiana and the Poa

Complex. The previously defined group (Poa
bergii var. chubutensis, P. boecheri, P. hubbardiana,
P. lanuginosa, and P. patagonica var. j><,
was further analyzed by PCA. Figure 8 is based on
the first three principal components. Two groups oi
species appear, with sexual dimorphism being the
main source of variation within these groups. Caes-
species is differentiated because it has a short ligule, small stomata, and long hairs lying between
the nerves of the lemma. A P. lanuginosa comph a
(P. bergii var. chubutensis, P. boecheri, P. lanuginosa, and P. patagonica var. . ago\ i i princi] i
ly distributed along the positive edge <>l axis III,
Examining their character loadings, this group is
defined by long ligules and small florets. Axes I
and II showed a clear dimorphism between pistil
Discrimination among taxonomic entities. Species

of the P. lanugin
i
ubbardiana, and
the remaining specimens were used as a priori
groups for DA. The first two canonical variables
clearly discriminated these groups. The P. lanugi;."<,(< romp!, s pii -i i::s hui^ [uunch - m<l lariic stniiiala /'>'.: hiii>l)ti!'liti'iri i l\v,ulcs, and sharp blaili apices. I '.lasMheaiion of llic
groups showed a few mismatches. Nevertheless,
91% of specimens of the P. lanuginosa complex
were correctly classified. Meanwhile, 78% of ex-
< omplex, a new

ui Jin lion u ilysis ,'. i- performed on the 78 remaining specimens l>;ised on I-3 morphological \ariables. One invariant character was excludt d I fore
performing PCA: groups of sclerenehyma cells at
blade margins do not extend on abaxial and adaxia]
epidermis (CAP 1, see Appendix 3). The first five
PCA axes explained 49% of total variability, with
PCA distortion being low, rM = 0.91.
OTU distribution on the first three axes showed
a group of three caespitose species, P. holciformis
Presl, P. huecu Parodi, and P. indigesta Parodi (Fig.
9). Specimens for those spi
- in
ml ol a
3 III. They are distinguished by their
relatively long leaves and inflorescence, and relatively wide, thick blades. Spikelets, glumes, and
are glabrous.
Three species were independently analyzed: P.
- is, P. huecu, and P. indigesta. These are
recognized as single discrete entities on the first
three PCA axes. Poa indigesta is the largesi n sue
among the three taxa, and also has the longest, widest, and thickest leaves. Poa holciformis is differentiated from P. huecu by its longer spikelets,
glumes, and florets, and wider blades. The first five

components analyzed accounted for 59% of total
. but their distortion was very low, with
rM - 0.93.
ittori among taxonomic entities.
flu previous three species were considered the a priori
groups to discriminant analysis. Standardized coefficients of canonical variables revealed P. indigesta to present long blades, abundant cuticular
prickles, and broad panicles. Poa holciformis is
characterized by long lemmas and ligules. In contrast, P. huecu, at the opposite site, has shorter lemmas and more nerves on the first glume. Classification of specimens based on discriminant
(unctions showed a good fit to data. One hundred
percent ol ili. specimens of a priori groups were
included in P. huecu and P. indigesta, respectively.
Eighty-three percent were correctly assigned to P.
OS here associated
with P. huecu.
The Poa denudata and Poa rigidifolia Complexes. Upon the removal of P. holciformis, P.
huecu, and P. indigesta, a new PCA involving the
54 remaining specimens and using 41 morpholog-
holciformis, P. huecu, P. indigesta
ical variables was conducted. Three characters

were excluded as invariant for the whole group. Apice blades are all navicular (API 1, see Appendix
3), viviparous florets are absent (FLOv 0), and all
groups <: sclerciichviua cells at bl.nle margin.- :
not extend on abaxial and adaxial epidermis (CAP
11. The iirsl liu principal oniponem- < < un'c I
for 50% of van.in. i iinonj -p< uncus, yielding a
low distortion for the analysis of r, = 0.91.
Distribution of OTUs is represented on the first
three principal components (Fig. 10). Specimens
an- gathered into two groups. The Poa ligidifolia
i it pic v (as leiincd by < auss; ni el al., 1996) consists of P. dusenii Hack., P. ibari Phil., and P. rigiill/olta Steild. I he /! iii'nii<i,l!il coin; l-\ c{i|ll|!lisi stem I
uapiensis Nicora.
The P. rigidifolia complex principally associated
with the negative end of axis I. This complex is
distniiMiislii 'I b\ lougi r spikclei>, glume-, am) !:
rets than seen in the /' denudata complex. Conversely, P. dcnudutii and P. nah,,,!:,,aj>a nsi-, li.e.e
wider blades, and
ma girders on both sides of the- vascular bundles. Minimum spanning tree or IV1ST
technique confirmed species groupings. This techIIK| ie v.,i- pcrlonncd because- |\\n spci-iincns. the
types of P. dusem, and /' / !^<<!,/,'!ia. app< m I i-nlati il from their re-pei live groups, \nal\sr~ ol mm
imum distances among these OTl - showed rela-
tionship ol tile isolated Ivpes to the /' rigidifolin

complex (Fig. 10).
Specimen ordination for only the P. denudata
complex, P. di i
iJ/
,">,
showed a clear dimorphism among pisti >
m<l
si
i
individuals along the first three principal
component-.. Pistillate -p< cimeu> ate haiach nzi d
by hairy florets and longer leaves, inflor- -. < i < -.
Disi-fiiniiiiitiofi ait,<tt,
Specimens of both the P. rigidifolia and the P.
,< ,,"< ila < mi I.
M
insidered as a priori
groups for DA and were characterized by analysis
of standardized coefficients. The P. denudata urnplex presents lorn I
.
r_( - omata, and broad
panicle-,. Meauv,liili . liu >'. I'ûiijalia complex
lion percentages
showed a good fit between groups: 90% were included in the P. denudata complex, and 94% correctly classified into the P. rigidifolia complex.
:ies, as well as independent species,

lalysis revealed the correlation bet pairs of morphological and anatom-
Volume 87, Number 2

1
li
ilws Plot of 54 indivi
distances between imli -I ii
mi tin- niitiiniuin span
complex is represented on Nark lal.els (DLI. IK. RI). and the P.
Figure 1 caption for explanation of labels.
leal rhara. Ier>. I'airwise combinations were drawn

for fertile characters (GLUle, GLUw, LEMle.
LEMw, PALle, PALw, LODle, and LODw) as well
as paired combin.il
plant sizes (LEAle, BLAle, SHEle, HEIG, PANle,
PANn, PANw, BLAw, SCL2). All analyses showed
linear relationships. Fertile characters are continuously distributed along the whole range of variation.Incontrast.lNplant size present a conspicuous <!e oninni
main
groups (Fig. 11). One of these main groups contains
plants of large size including the P. dolichophylla
complex (P. stuckerh
i
sis
var. calamagrostoid
bergii complex (P. barrosiana and P. bergii var. bergii), the P. bonariensis complex (P. bonariensis, P.
mtmtcvidcnsis and
n.
an i /' . in . -.-ill- p.j n - in .un-li ihe second group and include all remaining species.
Another series ol |. iii vis. h u u I< i < mi i iii..n
showed a non-linear pattern of variation. Four taxonomic groupings are shown in Figure 12 and are
based on the relation between ligule length and leaf
long leaves. Finally, a fourth group consists >: -j

ries with long ligul.-s lull -li.irl raves. \ similar
grouping pattern was observed from the relation
ship between ligule length and any other charade
related to plant size (LEAle, BLAle, SHEle, HEIG,
PANle, PANn). Another important character cornbination involves leaf length and stomata size (Fig.
13). Here, groups of species assembled according
to: (1) small stomata but long leaves. {2) large sinm<i I <<.-. i.
e.
<_. stomata but short
leaves, and (4) short leaves but stomata of medium
size.
Univariate analysis considered the average (for
i
Lea) or mode (for discrete variables) for all complexes and individual species, as
well as pistillate and staminate specimens, separately. Sexual dimorphism was noted on fertile
characters related to spikelet, glume, and floret, as
well as floret hairiness. Table 1 shows a list of seI. h d h. i> n [in -< tiling the range of variation among complexes and species, as well as sexual dimorphism within entities,
length. One group includes species with short ligules but long leaves; a second species group, by
contrast, has short ligules and short leaves. A third
group combines species with both long ligules and
DISCUSSION
Taxonomie pn I. - . illm !\><i were accurately
expressed by Bor (1952: 7-8), and his words re-
i Poa Sect. Dioicopoa
:cent au-
. While many species are <
... is one
amic stur -
cies about
5
groups <
= that their evolutionary hisen so complex that they do not lend themX by present taxonomic
, One cannot rely upon a single
This study of Poa sect. Dioicopoa utilized multivariate taxonomic techniques, as well as univariate and bivariate analyses, to better understand the
morphological variation patterna different methodology from traditional taxonomic treatments.
Analyses of both pistillate and staminate specimens
denote complexes of species of great similarity, but
it was also possible to clearly recognize some valid
species. A multivariate key for identification among
taxonomic entities ol I'D, l> >pon was produced (see key herein).
Identification of varieties for three species analyzed here could not be supported. Thus, Poa bergii
and P. bergii var. chubutensis, P. patagonica and P.
patagonica var. neuquina, and P. pilcomayensis and
P. pilcomayensis var. calamagrostoidea did not
group together by similarity and were either ineluded in different species complexes or maintained as independent entities. Poa bergii was
grouped with P. barrosiana in a P. bergii complex,
while its variety P. bergii var. chubutensis associated
differently within the P. lanuginosa complex. Poa
patagonica was more similar to species ol the /!
lanuginosa complex than to its variety P. patagonica var. neuquina, which clustered within the P.
bonariensis complex. Finally, P. pilcomayensis was
m - I
in I pr i
III
hili in
ii i i
comayensis var. calamagrostoidea related to a P.
dolichophylla complex.
Poa schizantha, a particular case within Poa
and
noso,
Argentina (Parodi, 1940). It is recognized by present results as a single species, related to the P.
bergii complex. The three species (P. barrosiana, P.
bergii, and P. schizantha) were found in similar environments and geographic areas. However, P. schizantha is clearly distinguished by a particular bilobed lemma, an interrupted panicle, and a
different anatomical blade structure; among other
characters, it lacks a well-developed midrib and
bulliforni cclU. In -i i
- Miild ui . by
hybridization or odd mutation. Possibly, its off-
spring had low fertility and, whatever the case, it

has never been collected again.
Plant stature of less than versus greater than 50
cm was a significant criterion by which to disc i immate Species within Poa sect. Dioicopoa. Plant
height correlates with characters such as leaf blade
and sheath length, panicle length, and number of
nodes per panicle (Fig. 11). Other characters, of no
hnear variation, also address species discontinuities. Ligule length divides Poa sect. Dioicopoa into
those species with short ligules (less than 2(-3)
mm) and those with long ligules (more than (3-)4
mm),
Plant habit did not show, despite traditional
treatments (Parodi, 1936; Torres, 1969, 1970; Nicora, 1978), a clear pattern of variation, nor any
character correlation that could clarify the taxoimniic structure within Poa sect. Dioicopoa. Some
species could be differentiated only by the presence or absence of a rhizome. For example, species
of the P. resinulosa complex, P. pedersenii and P.
resinulosa, are caespitose, while P. buchtienii and
P calchaquiensis are rhizomatous. Parodi (1936)
suggested that the rhizome is systematically valuable, dividing Poa sect. Dioicopoa by rhizomatous
and caespitose habits. Later, Hunziker (1978) observed that crossings of r
species of Poa produced fertile offspring, a
the pattern of inheritance depended on the species
that were crossed. Therefore, it remains preferable
to group otherwise similar i
pitose species
Sexual dimorphism was the principal source of
variation within species and taxonomic complexes
of Poa sect. Dioicopoa. Thus, it was necessary to
establish ranges of variation for reproductive characters in pistillate and staminate specimens separately. Sizes of spikelets, glumes, and florets, as
I
hairiness of florets, indicated u
ences between pistillate
ditionally, hairiness oft
considered a useful dis
1970; Nicora,
usually glabrou
interspecific lira
staminate specimens. '
variation in hairiness of pistillate florets within, and
among, analyzed groups. Therefore, these characters are less informative for interspecific variability.
Callus hairiness on pistillate florets could be a synapomorphy for the whole genus or part of it (Kellogg, 1990), and is also valueless for interspecific
variation. The absence of hairs on pistillate florets
occurs only in P. huecu, P. holciformis, and P. indigesta. Both pistillate and staminate anthoecia in
i>< ! ,/' '-'
,.
TiM
Il ii i 1. n
b.
discrete characters. I'i corresponds to number of

umber of st; nnnatespecnnens. Character abbrev ationsasi .Append. 3.
dmensana.vzedpers
(I.EAle)
(UGle)
Plant
height
(HEIG)
Panicle
length
(PANle)
Nodes/
Panicle
(PANn)
16.11)
56.9
, 2.28)
( r>.n
16.3
< 4.13)
6.5
( 1.81)
67.1
i 2().59)
28.9
r (..26)
Blad.
(BLAw)
(STOM)
(!) I5|
15
,11 20)
( * 0.35)
( 0.0055)
0.049
(+ 0.0051)
(10-181
i * 0.2"I
(9-14)
(0.18)
( 0.44)
( 0.0044)
0.041
( 0.055)
(Pi = 23, St =
(Pi = 4. St = 5)
(Pi = 6, St = 3)
(Pi = 2. St = 1)
(Pi = 5, St = 5)
(Pi = 20, St = 14)
P. ligularis
(Pi = 12, St = 9)
(Pi = 5, St = 5)
P. pogonantha
(Pi = 14, St = 9)
(Pi - 19, St = 20)
P. rigidifoha
(Pi = 23. St = 15)
(Pi = 5, St = 1)
P. tristigmatica
(Pi = 14, St = 9)
these three spei i. -
( 11.62)
18.8
( ' 8.32)
40.8
(33.5-48.0)
24.3
( 10.56)
25
( 10.21)
22.6
( 11,78)
( tl.lh
5
( ' 2.2)
7.9
((..3-8.7)
! ' 0.28,!
7.8
( 13.51)
34.5
( 11.94)
57.6
(40-71.7)
36.2
< 13.48)
38
7.4
29.8
0.8
33.3
( 10.4.3)
37.7
( 16.37)
32.3
( 17.71)
17.2
( ' 8,(>8)
38.7
( 8.25|
16.5
, 6.581
18.8
(+ 12.36)
9.7
(6.17)
28.1
( 6.45)
( 5.57)
( 2.15)
( 1.08)
+
1.01)
4.7
l 1.65)
7.3
l 2.31)
(8-13)
(0.21)
(10-10)
15
(15 20)
13
III) 18)
13
(O 18)
(0.17)
(1.11-1.76)
1.5
l 0.46)
(7 20)
(031)
,8-14)
(0.31)
(6-12)
(8 10)
l 11.30)
0.76
1 < 0.22)
,6-14)
13
1" 131
( 0.17)
0.8
, ' 0.2(|
(+ 0.22)
( 0.0051)
0.040
( 0.0049)
0.048
(0.042-0.046)
0.040
( 0.0039)
( 0.0048)
0.038
Ii 0.0037)
0.037
, 0.001',
0.03(,
( 0.0042)
0.037
( * 0.00.V.I
0.038
( 0.0028)
( < 10.05)
. 1
absence of hairs in these taxa could represent a

loss vvitli ivsprd to the evolution ol the entire genus, as suggested by Kellogg (1990) for other species of Poa. Pistill.if .iritiu i i.i ! /' '>".".-'.,.,,<,,. >
are remarkably hairy, and clearly differentiated
from other species. Its woolK li.nrs mi Ih<' floret
callus are numerou- loim. n.l t<d.I< *J \lnl< ! non and between palea and lemma nerves are curled,
Out of the 34 species analyzed, only 8 were dis-
. ,imi(.
methods:
Poa
holciformis, P. hubbardiana, P. huecu, P. indigesta,

P. lanigera. /'
'
'. nmayensis, and P.
achizantha. The remaining species showed congruen! morplii.loiih--. ^-[.-almi: into species cornplexes by phenelic similarities. Any hierarchical
a- - -.
\u lies was not consisI I lh
in
-p. ie- alignments. The validity
of species assorting into complexes remains contro. Foi
Table 1.
Extend**
a length
Mle)
Glume length
(GLUle
Hairs on callus
(1 Meal)
Hairs on nerves
(HAI rv)
Pistillate
Staminate
Pistillate
Staminate
Pistillal.
Staminate
Pistillate
Slan.iiialr
6.8
( 1.16)
6
1.27)
7.5
(+ 0.08)
4
( 1.42)
(0 1)
4
(0-4)
2
(0-3)
(0-3)
( 1.25)
1.00)
3.2
A 0.18)
i 0.99)
5.3
i 0.71)
5.3
i 0.18)
(0-3)
4
(0-1)
10 3|
3
[2 3i
2
(0-1)
(0-4)
( 0.62)
( 0.73)
3.4
( 0.72)
4.7
( 0.69)
5.8
( 1.31)
3.4
( 0.67)
0.39)
2.9
0.78)
0.72)
1.2
0.51)
2.8
0.70)
2.5
( * O.o8)
5.4
( 0.77)
4.|J5)
( 0.63)
4.5
( 0.95)
| 0.25)
4.5
( 0.33)
3.6
1= M.53.
(0-4)
0
( 0.80)
5
(- 0.23)
<U3)
3.6
( 0.67)
2.9
( 0.37)
2.7
0.35)
2.5
0.51)
(0.79)
(i 0.53)
5.8
i ' 0.<>0|
4.8
i- 0.8,3)
( 0.24)
(0-4)
"
(0-1)
(2-3)
(0 2)
(0-4)
(2-3,
(0-1,
(2 3)
2
(0-4)
4
2
f 1.28)
(+ 0.51)
7
( 1.12)
6
( 0.59)
(0-1,
(0-3)
( 0.71)
0.12)
( 0.79)
((,43)
( 0.95)
5.7
I l.32i
5.5
( 0.86)
0.82)
( 0.70)
( + 0.85)
(0-1)
2
5.6
5
( 0.97)
( 0.83)
(0-4)
()
(0-4)
(0-3)
,0-2)
M,
2
(1-2)
(0-2)
(0-4)
HU3,
(0 2i
) 2i
( 1.51)
+ 0.00)
(CM.
(0.08)
('()42)
4.7
(0.01,
(0 2)
(0-2)
2
(2-3)
0
3
1
(037)
(0-1)
(0-4)
similar variation pattern for several characters, not

a single one. In general, morphological variation
pic-t tils hat liscotilinuilii's idn linr species,
tal discontinuities. Preci

and anatomical variation
also correspond to Giusi
>ecies is clearly associated with i

lism. Morphological variation within only pistilte plants or staminate specimens, correlated with
ivironmental factors, appears significant only at
if inlrasperinc level. By these criteria, sympatnr
jecies of Poa sect. Dioicopoa within the same taxlomic complex are synonymized herein. One n< >'
iriety of P. rigidifolia is further propox !
\ sexual dimorphism associated with environmen-
TAXONOMIC TREATMENT
10 21
(1-2)
(0-1)
nges of morphological
:stablished herein and
i (1997).
Poa alopecurus (Gaudich. ex Mirb.) Kunth, Revis. Gramin. 1: 116. 1829. Arundo alopecurus
Gaudich. ex Mirb., Ann. Sci. Nat., Bot. 5: 100:
1825. TYPE: Falkland Islands, East Falkland:
Port Louis, 14 Feb.-28 Apr. 1820, C. Gaudichaud s.n. (holotype, P not seen, isotype, US
78849 [fragment ex P] not seen).
(Speg.) Parodi, Bevista \rgenl. \-mn JD(li:

180. 1953. Festuca shuka Speg.. Anales Mus. Nac.
Hist. Nat. Buenos Aires 5: 95. 1896. TYPK: Argentina. Tierra del Fuego e Is. del Atlantico Sur: Ushuaia, Isla de los Kstados. Port Vancouver. Blossom
Ba\. C. Spcgazzini s.n. (holotype. LPS 14322 not
seen: isotype, LP!).
Poa superbiens (Steud.) Haunian & Parodi. Phvsis (Buenos
Aires) 9: 311. 1929. Mm su,,c,!ncns Steud.. Svn. PI.
Glumac. 1: 424. 1854. TYPK: Chile. Magallanes:
Sandy Point. Dec, W. Lechler 1194 (holotype. P not
seen; isotype, BAA fragment!, US 2095872 <x III).
Cosson P not seen. US 7931 1 ex W not seen).
Tins
southern portion i ! Pa' igoma. ovcriug ni'sl, m ami >< ulhrrn tedious ol
Santa Cruz, western areas of Tierra del Fuego e
Islas del Atlantico Sur, Argentina, as well as
boundary zones of XII Region. Chile.
Poa bergii Hieron., Bol. Acad. Nac. Ci. 3: 374.

1879. TYPE: Argentina. Rfo Negro: boca de
Rfo Negro, C. Berg 205 (holotype, CORD!).
Poa barrosiana Parodi. Phvsis (Buenos Aires) II: 134.
1932. TYPK: Argentina. Buenos Aires: Vli.amai. 31
Jan. 1930, L R. Parodi 9820 (holotype, BAA!; isolype. US 89694 not seen).
Poa bergii inhabits costal dunes of Buenos Aires
and Rio Negro provinces, Argentina. It may extend
-iiui1.11 d.Jii in- n ! ruguay and Brazil.
Poa bonariensis (Lam.) Kunth, Revis. Ciamm. I:

115. 1829. Festuca bonariensis Lam., Tabl.
Encycl. 1: 192. 1791. TYPE: Argentina. E.
Bonaria Circa Monte-Video, inter rupes et
maritimas, 1767, E. Commerson s.n. (holotype,
P not seen; US 2875384 ex P not seen; isoBAA
/ manlcridcnsis \rechas.. \nales Mus. Nae. Montevideo 1: 479. 1897. TYPK: Uruguay. Montevideo: en
parajes hiimedos, Nov., Arechavaleta 5101 (lectotype, designated by Parodi (1936), MVM not seen:
isolectotype. fragment LP!, type photo, LP!).
Nieora. Hiekenia
1(18): 107. 1977. HPI'.: \,
partamenlo Lacai. s.in \la,h,
hai :!<>;> . (hoinup.. i:\ \'i
Distributed in the northeastern Buenos Aires
province, tins species reaches its southern limit at
il..' -vsl.m ol Tauddia and Si< rra- Australes. Il extends to the north and east, into southern Entre
Rfos, Uruguay, and Brazil. One of its synonyms, P.
patagonica var. neuquina, was found in a Cipres
forest near San Martin de Los Andes. iNcixpicn.
dispiiic! I:..in il- m iifi ar<-a ol dish ilnitioti.
Poa denudata Steud., Syn. PI. Glumac. 1: 259.

1854. TYPE: Chile. Valdivia, W. Lechler 578
(holotype, LE not seen; pistillate fragment,
BAA!; isotype, US not seen).
I'm, nuhuclhmqncnsis Nieora. Hiekenia 1(18): 106. 1977.
TYPK: Argentina. Neuquen: Departamento Us Ugos. Peninsula Cmetrihue, 1 Nov. 1949, 0. Boelcke
X J. II. Iluu:ik,; .11.',:: (holotype. BAA!).
Poa denudata grows in western Neuquen, Rfo
Via'< . and i iliuh il. \-j'< i lina. ai -I along the ( ,hi
lean boundary in Regions VIII to X (Toledo & Zapater, 1991), near lake margins, among rocks, or in
below elevations of 1000 m.
Poa
Poir., Encycl. 5: 91. 1804. TYPE:

Uruguay. Montevideo: E. Commerson s.n. (holotype, P not seen; fragment BAA!, US 88769
Poa bergii Hieron.

Agron. Univ. Nac. La Plata 3: 628. 1897. TYPE:
Argentina. Chubut: Departamento Klorentino
A.neghino. Calx. Mas,,. (.. Spcga:z,nt Will (hololspe.
LP not seen; fragment BAA!).
Poa hoi'rln-ri Parodi. Bevista Argent. Agron. 2!'.: 100.
1961 |1962|. TYPK: Argentina. Mcndoza: Departamento San Rafael, Valle del Atuel. Kl Sosneado. 35
lat. S, 4 Oct. 1955. T. W. Hochcr. J. P. Hjerting & K.
Rahn H01 (lo.lolv,... |i\ V: i-oiM,r. C not seen).
Poa patagonica Phil.. Anales L ni\. Chile 94: 168. 1896.
TYPE: Chile. Departamenlo I lluna I -,n ,an/a. Lag..
Pinto, 11 die. 1877. H. Ibar s.n. (holotype. SCO not
seen: fragment BAA!. IS 88748 fragment ex SCO
Poa lanuginosa is a widespread species, distribalo.l in \igt i i n.i Ir.ini > - S lln -h ;>| .- >n I'uaia
del Fuego. It grows in highly degraded soils, and
on dunes ami sands -nils n Pala-onia.
Poa pogonantha (Franch.) Parodi, Revista Argent. Agron. 20: 180. 1953. Festuca pogonantha Franch., Miss. Sci. Cape Horn, Bot. 5:
387. 1889. TYPE: Argentina. Patagonia, Port
Eden, 24 Jan. 1879, Savatier 1844 (holotype,
P not seen, fragment ex P, BAA!; isotype, US
s.n. fragment and photo ex P not seen).
Poa prichardu Hemlle. J. Bol. 42: 324. 1904. TYPK: Argentina. Santa Cruz: Lago Argentino. Monle Buenos
Aires, 1900-1, //. Pilchard .s.n. (holotype, BM not
seen; fragment BAA!).
This species occurs in humid forests of Rio Negro, I i iluit. Santa Cruz, and Tierra del Fuego, Argentina (Nieora, 1978), and in the XII Region of
Chile (Toledo & Zapater, 1991). This area is ini-halrd vsilliin fit. >ol i.mtarcl it- pli\ logeograpliic
province (Cabrera & Willink, 1973; Cabrera,
1994).
Poa rigidifolia Steud. var. rigidifolia, Syn. PI.

Glumac. 1: 260. 1854. TYPE: Argentina. Tierra del Fuego e Is. del Atlantic Sur: Islas
Malvinas, Is. Soledad, Pto. William, Sep.
1850, W. Lechler s.n. (holotype, P not seen;
a tristigmatica E. Desv., in Gay, Fl. Chil. 6:

419. 1853. SYNTYPES: Chile. Magallanes,
Cordillera de Talcarengue, Feb. 1831, Gay 49
(P not seen; fragment, BAA!, US 88717 fragment not seen); Bahfa Duclos, Estrecho de Ma-
fragment BAA!, US 88734 fragment not seen).

velekei Nicora. Hickenia 1(18): 104. 1977. TYPE:
Due to the results obtained in this research, the
/' rigt'.tijoint ( IIM|II< \ i;-. considered ,i single la\onomic species. Two varieties are proposed in agreement with the previous study of Giussani et al.
nrima del refugio. I8<><> I8.il , 1 1 I - I, I'"7 I 1/

V. Coma el al. 5926 (holotype. BAB!).
(1996). Pistillate individuals of each variety showed
rom Mendoza to Tierra del Fuego. It-- d>

hibnlioii d an a tall- uillun lh< \ l>> indiii i |i| \l. -
-kuninale -fH-riiiH-! -,. .ilihmiiili . <a r.-l.i! i<,n l turm
geographic province (Cabrera & Willink, 1973;

Cabrera, 1994), ranging from 1600 to 2000 m in
Neuquen, and at 500 m, or higher, at the highestlal hide ai.-as ol '! HTM del I- -. I'oa !>oricln i was
pti .lo.iv in<! - nv ii i in. i ' v, i-
IIILII
.lli : l-
liliati and -tamma'i pi mi - !',><; _',//.'/.... n

idifolia includes P. spiciformis (Steud.) Hauman &
Parodi (= P. poecila Phil., Giussani, 1993), previously synonymized by Giussani and Collantes
(1997). It is distinguished by the woolly hairs on
the floret callus but an absence of hairs between
the palea and lemma nerves on pistillate floret.-,
thinner blade*, longer di.alhs. I ionics, an:! nladeaild -tllall. I -loin.il.i ill.Hi pi-lllL'i -peiilllen-, of P.
! var. ibari.
Poa rigidifolia var. ibari (Phil.) Giussani, comb,

et stat. nov. Basionym: Poa ibari Phil.. VnaleUniv. Chile 94: 170. 1896. TYPE: Chile. Departamento Ultima Esperanza, Lago Pinto, Jan.
1844, H. Ibar s.n. (holotype, SGO not seen;
isotype, BAA!).
I'oa dusenii Mack., in Dusen. Ark. Hoi. 7(2): 8. 1908.
TYI'K: Argentina. Santa Cruz: Ma/.are.l.. |>.ntmti.
4741'S, Jan. 19()5. Dusen .lilH (liolotvpe. \\ not
seen; fragment BAA!: isotvpes. US 89702 not -een.
US 1161178 not seen).
Poa rigidifolia var. ibari is characterized 1>\ not
having woolly callus hairs on the floret callus but
having them on, and between, principal palea and
lemma nerves of pistillate florets.
Further treatment of morphological and ei
sion i)l character assessment can be found in
sani and Collantes (1997). Poa rigidifolia inhabits
steppes of Chubut, Santa Cruz, and Tierra del Fue
go. and suinlai en\ linmneui a tie uhb:i w- i I 11.Poo i!:i.liioh.t
II
v ./ .
i pre-enl in subhumid austral areas, whereas P. rigidifolia var. ibari
1996; Giussani & Collantes, 1997).
collected only in Cerro Chapelco at approximately

1800 m.
For the remaining P. dolichophylla and P. resinulosa complexes, species show allopati
bution, and a study of population variability and
their ecological relationship is required to resolve
taxonomic problems. In addition, types of older
named taxa, particularly those of Philippi, need to
b. studied. Uoi dii- I \ my has not yet
been established.
However, the P. dolichophylla complex is well
segregated from other species within Poa sect.
Dioiiopoti. Species distributions are clearb distinct
bio-eoio phi.-allv, I'on doiii-'hoj,h\ii't and /* ;>:h-.<
mayensis var. calamagrostoidea inhabit Sistema de
Cumbres Calcli j in
\ n i.ija-Famatina in
northwestern Argentina (Gonzalez Bonorino, 1958).
t-rtii is restricted to central Argenlii a. on
hills of Cdrdoba and San Luis, reaching 1500 m.
This taxon is associated with lowland humid sod-.
Poa iridifolia occurs in the Sierras Australes and
Tanddia. in Buenos Aires, Argentina ((ion/alez
Bonorino, 1958).
Species of the P. resinulosa complex are morphologically similar but inhabit disjunct areas. Poa
resinulosa grows in central Argentina, between 30
and 45S, in steppes, on stony, dry soils (Nicora,
1978), and in the Sierras de Tandil and Ventana,
in Buenos Aires. Poa pedersenii was only collected
in Yhu, Paraguay. Poa < ah b
Argentinian Puna (the southern extreme of the Peruvian-Bolivian Altiplano) in Jujuy, Salta, Tucuman, and La Rioja and could also be spread over
Catamarca. Poa buchtienii is distributed on the Altiplano and the Cordillera Oriental of Bolivia.
Morphological
. omplcxes must
!< addressi d l>\ population ill md bio :><J. ai -I H!I -
In better resolve the decree of simihmlii

ohotuic bomnlai ies anion*; these species
within Poa seel. Dioicopoa.
Stomata infrequent on ahaxial epidermis.

0.03-0.037 mm long (0.034 (0.027
0.042))
Poa dolichophyllti complex
with herbaceous sheaths, panicles contracted
I
2-3.5
1,-
' .
!l
'
4)). Glume I, 1-3-nerved, Pi: 3.7-5 mm

long (4.3 (3.4-5.4)). St: 2.8-3.7 mm long
(3.2 (2.1. In. Pi and Si. 11. 0-O.U ...... w .d.
(0.7 (0.0-0.0)). Lemmas. Pi: 4.5-6 mm
long (5.3 (-1-6.7)1. Si: 3.8-1.2 mm long
(I (3.7 1.5)): Pi and St, 0.85-1.1 mm
wide(l (0.8 1.3)). Ideas. Pi: 3. 1-1.2 ......
long (3.!! (3 1.0)). Si: 3.1-3.6 mm long
have in hand hull, , nil ,

,. I i ,
mi.MIS of llie population examined. When only a pistillate
speeimen is available. "\niMlii.eeiniis -|ie<ies from Poa
'-
'* '
-37)): nodes per ,

13-18 (16(10-20))
Plants 15-55 rm tall (32.1 (1.3 75)1;

leaves 5-35 em long (20.5 (3.5-54.5)):
blades 5-20 .-in long (12.H (1.3-37));
sheaths 1-12 cm long (7.0 (1.7-22)): panicles 5-13 cm long (8.6 (1.7-29)); nodes
per panicle, 9-13 (11 (6-20))
Ligules truncate to ohtust 0.6-2 ......
.5-6 cm wi
(0.4
(0.8 lOli: al.axi.
Stomala Iic<| ill ..n adavi I epidei in is

0.042-0.050 mm long (0.017 (0.037
0.054))
Poa bonarien
Plants with long and deep rhizomes. I'islil,>;<[. 5.5-1 I ., loo^ : .-i ,13 I2i:. 38 mm wide (5.1 (2.2 10)). Glume I. 35-m.xed: Pi: 1-0 mm long (0.5 (3.610)), St: 3-6 mm long (4.4 (2.8-7)): Pi and
St: 0.7-1.45 mm wide (I (0.6-1.7)). Lcm, Pi: 5-9 mm long (0.0 (4.2-10), St:
4-7
St:
0.9-1.6 mm wide (1.3 (0.7-2.2)).
Pi: 4-6 mm long (4.8 (3.3-6.7)), S
5.3 mm long (4.2 (3-6.3)): Pi an
0.8-1.3 mm wide (0.06 (0.5-1.8))
spikelets 3-fl owered: Pi: 4,5-6 ...... lonj(S;
t ): Pi ami Si:
1 .6-3.5 mm wide.
Glume 1. 3-n.e.^.-d. Pi: 3.5-1
nun lm.
Si: 2.5 ...... long: Pi: 0.7-0.8 mm wide

(St: 0.5 mm wide).
Lemmas. Pi: 4-5 mm
long, St: 3 i nmlong; Pi and St: 0.9-1.1

,leas. Pi: 3.5-1 mm long, St:
(1.5-10.611: panicle 1.5-3

3
......
I,i,-
Pi: 0.6-0.8 mm wide. Si:
0.5 ...... wi, le. Restricted to Zapala. Neu-
1 staminate spikelets 5.5-8.5
open panicles at maturity. Leaf blades flat

and .annate. 3.5-8 mm wide ((..(> (1.813)). Glume 1. 1-nerved; pistillate (Pi)
and staminate (St) glumes 2.5-1 mm
long (3.2 (11 5.2)). 0.4-0.7 mm wide
(0.0 10
'>..,)
I I
'II
I.
lid si
Hill II
ii
i. ii' I
'a
II.
15-35
I i ill
.,
(1.2 (2.2 6.3M. Uuine 1. 3-mrvcl: Pi:
1-
5 (3.6-6.8)). St: 3-5 mm lo.i

(3.8 (2.8-5)); Pi: 0.8-1.1 mm wide (0.05
(0.07
1.23)1. St: 0.7-0.9 mm wide (0.82
III
mas 3-4.5 mm long (4 (2.5-5)). 0.7-0.9

mm wide (0.8 (0.6-1.1)). Pistillalc and sta
minate paleas 2.5-3.5 mm Ion- (3 (2
3.81). 0.15-0.65 ...... wide |0.5 (0.35
I I.8.I. Keel and marginal nerve hairs of
tillal
- wh< n present, less than 0 5
-
mm long (6.
i I
,.
(4.2 7.5)1. St: 4-5.5 mm long (4.7 (3.95 81): Pi and Si: 0.0-1.2 mm wide | 1.2
(0.7 2.2)1. I'..leas. Pi: 4-5 mm Innu 1.2
(3.3-5.1)). St: 3-1 mm long (3.6 (3-5.2));
Pi a..d Si: 0.8-0.9 mm wide (0.83 (0.5lagouia and Cino. \igentiiia
Pan lanugiru
Pistillate and staminate spikelets 8-11 mm
Volume 87, Number 2

; Patterns in Poa Sect. Dioicopoa
O 12)1. 3.5-8 mm wide II, (3 K

. 3-5 (T)-nerved, Pi: 6.5-9 ir
(6-10)). St: 4-6 mm long (5 (
1.1-1.45 mm wide (l.c
.7)1.
St: 0.8-1.1 nun wide (1 (0.7-1,1)). Lemmas, Pi: 7-9 mm long (8 (6 10)). Si: 5-7
...... lout; (6 (4.5 8)); Pi and St: 1.1-1.6
.urn wide (1.4 (1-2)). Paleas, Pi: 4.6-6
mm long |5.I I I 0.7l). St: 3.6-5.3 mm
long I 1.7 |.3.3-().3)): Pi: 0.9-1.3 mm wide
(1.1 (0.7-1.8)). St: 0.6-1.1 mn. wide (0.0
(0.6-1.7)). Plants of coastal dunes of Huenos
Ligules 5-10 mm long (7 (2-15)). Pis
n or less. Slaminate lloret glabrous or

i and central regions of Argentina
Poa ligulans
Ligules aeuminale. 3-8 mm long (5.7 (I

7
2 to 3 i
Florets frequentK viviparous. (,liimi- I. Pi:

5.5-8 mm long (6.2 (3.7-9)). St: 4.5-6.5
(5.2 (3.6-8)). Lemmas. Pi: 6-8
mm long 7.1 (5.5-0.2)1. St: 4.7-7.5 mm
;4.4-9)). Paleas, Pi and St: 4-6
mm long (.5(3.7 .7 ): Pi and St: 0.7-1.2
mm wide (0.0 (0.5-1.5)). Plants of Patagonian Andes mountains; also widespread on
M
e; 15-25
em long (20.7) (13-29)). Leal Na.les ,uhconvol.ite: 0.14-0.21 mm thick (0.17
[0.12 0.21)1. liiilliform eell> mil differentiated, ahaxial epidermal prickles long, numerous. Lemma bilobed, pistillate (loret
ii
I
I.in I I - 1111 i i
11 11
5-15 ... lo.m i

iJ 20))
conduplicatc; 0.15-0.35 ...... tl.iek (0.25
(0.11-0.5)). Kullilonii cells well .liflcrciili-
lillate floret .alius glabrous or with woolly

and long hairs; keel, marginal nerves, and
Li
[ M I l r II
I I
II
1111
brous or scarcely pubescent
Plants caespitous. Glume I. Pi: 2.7-4 mm
long (3.5 (2 1 1,1)1. Si: 2.2-3.2 mm long
(2.75 (2 3.5)|: Pi and St: 0.45-0.8 mm
wide (0.7 (0.4-1.1)). Lemmas. Pi and St:
3.5-5.5 mm long (4.4 (3-0. lit: Pi and St:
0.8-1.1 mm wide (1 (0.6-1.3)). Paleas. Pi
and St: 2.3-4 mm long (
and St: 0.55-0.8 mm ,
(0.65 i
0.9))
Plants caespitous or 1.
(,lumc I. Pi: 4-8 mm long (5.0 (3.2 9|,.
St: 3-7 mm long I 1.8 (2.,, 11.211: Pi and
St: 0.7-1.2 mm wide (0.0 (0.5 |. 1),. |,-,iruis. Pi and St: 5-7 ...... long ((> (I i',5)):
Pi and St: 1-1.5 mm wide (1 2 (0 7 2.2)).
Paleas. Pi and St: 3-6 mm long (1,5 (2 O
0.7)): Pi and St: 0.7-1.2 ...... wide (III.
<
H,
l.l
II
..:
:n
long (4.4 (2.8-6.3)). Lemmas. Pi: 4.5-6.5

...... long <d i 1-7.1)). St: 4-6 mm long (5
(3.7-7.3)). Paleas. Pi and St: 3.5-1.5 mm
long ( I (2.o (.)); Pi and St: 0.65-1 mm
wide (0.75 (0.5-1.4)). Plants of Patagonian
. Ligules 2-5.5 mm long (3.6 (1.2-9)).

Plant 18-38 em tall (20(15-02)): leaves
8-18 cm long (14 (5.5-30)); leaf blades 510 en
Bill.:) (3 I 5)). 0.25-0.40 mm
thick (0.53 (0.1 I 0.5.1. .heaths 4-8 cm
long (0 ,2.5 lot). Stomata 0.044-0.053
mm long (0.048 (0.042-0.002)1. Glume I.
Pi: 1.5-0.2 ...... long :^.r, (3.7-7)). St: 45.3 mm long (4.5 (3.6-5.6)). Lemmas. Ii:
5.8-7.8 mm long (6.7 (5.5-9)). St: 4.76 ...... long |5.l (L1-0.7D. Paleas. Pi and
St: 4-5.5 r
cm long (13,1 (2.2 30)), 0.20-0.28 mm

thick (0.25 (0.17-0.36)); sheaths 6-14 cm
long (10 (2.5-22)). Stomata 0.036-0.046
mm lonu (0.0 12 (0,032 0.052)). Glume I.
Pi: 6-8 mm long (6.8 (4.8-9)). St: 4.7-7
mm long (( (1.3 8.2)1. lemmas. Pi: 6.58.5 .u.ii long (7.5 (5.7-9.2)1. St: 5.5-8
mm long (7 (5 9||. Paleas. Pi and St: 1.56 nun long (5.2 I 1.2 6.711. Southeast Pala
gonia and Chile
Poa alopecur
12(10). Leaf blades 2-3 mm wide (2.6 (1.8-4)).
- glabrous or with hairs 0.5 mm
Pi and St: 3.5-5 mm long (1.1 (2.(>-5.3)):

Pi and St: 0.7-0.8 mm wide (0.75 (0.5-
ely pubescent. Steppes o

!0-50 cm tall (38
(13-<>1)); panicles 7-14 cm long (10.3
(I..") |).!!||: panicle n,|,v I 1-15 (13 (018)). Leaws 15-35 cm long (25 (7.2 17)):
,-al V.>:,, 7-27 < long (17 (1.7 3.5)1.md
0.23-0.3 1 ,,,.,. thick 11)3! (0.18 -0,11)):
sheaths 1-11 cm long (8.25 (2.5-20)); ligules 5-11 mm lorn; (7.!t (5.3 U, 1)1. Sliii i!, O.OI 1-0.051 mm long (0.048
l<) 01 "I On i(i , , | i, | n ,, .jn;i| nerves el
Planls eaespitous or long-rhizom.iloiis. Leal

blades 1-2 mm wide (1.0 >.'' 3.2)1. Sin
mata 0.032-0.040 mm long (0.037
(0.(127 0.0 U.it. Spikelets. Pi: 4-6.5 mm
g (5.0 |3..-. r.2)|. St: 1-5 ...... long (1,0
(3.4-5,1)). (duinr 1. Pi: 2.5-3.5 ...... Ion-;
(3 (1.8-1.8)1. St: 2-3 ...... long (2.5 (1.5
3.3)); Pi and St: 0.1-0.7 ...... wide (0.5 !
(0 35 1)1. Lemmas. Pi: 3-5 mm long (LI
(2.8-5.4)). St: 2.8-3.5 ...... long (3.1(2.8
LI)). Palcas. Pi and St: 2.5-3.5 mm long
1.8-3.7
Leal I
wide (3.1 (2 1.1)1. Si,.mata 0.037-O.OM
in... I
010 (0.030 O.OlOll. Spikelets.
Pi: 6.4-7 mm long 10.8 mm (0.3 7.2|(. Si:
4.5-6 mm long (5.0 (4.8-0.3)). Glume I.
Pi: 3.5-4.5 mm long ( 1.2 (3.8-1,0)). St:
2.8-3.5 mm long (3.2 (2.8-3.01): Pi and
St: 0.5-0.8 mm wide |0.o7 (0.10 ().>.
Lemmas, Pi: 4.8-5.8 mm long (5.3 (1.7
0)). St: 3.5-1 mm long (3.8 (3.2-4.1)). Paleas. Pi: 3.2-1 mm long (3.0 (3.1-4.1)).
St: 2.8-3.5 ,,., long (3.2 (2.8 3.81)
I ... I. .....I
7-1 I U! (i, ' 1): I >;, 518 cm long (10.2 (3.5-30.5)): leal blades
3-8 cm long (5.f. (13 2 11). 0.15-0.23
mm thick (0.10 (0.110.28)); shealhs 2-7
cm long (1,0 (1.7-11.8)); ligulcs 3-7 ......
long (4.7 (1.I-I0.3M. si. M, n i 0.0330.044 mm long (0.038 (0.030-0.054));
keel and marginal nerves of pislilhi. lion I
. Callus of pistillate llorels hairy, with woolly,

lotiii hail's, inlcrcoslal epidermis zones of
II
I 015). Plants eaespitous. Inflorescences usually n

longer than leaf length. I.igules obtuse. O.f:
I ...... long I.I (0.5 1.0)>. St,.mat., scar,
on abaxial epidermis. 0.33-0.040 m.
long I ' ..(0.027 00151) 1,-al blades wi
M -
tillalc specimens: sheaths 3.5-6.5 cm

long, blades 0.8-0.1 1 mm thick, and s|,,i::l;,O.OL'MU>38 mm long: on sliiininale
specimens: spikelets 5.4-7.8 nun long m
leaf blades 1-1.5 mm long. Sul.humid ln-
with woolly, long
hizomalous. Inllorescenees longer

mg 12.2 (0.5 5.8)1. Stumata lieqnenl
abaxial epidermis. 0.035-0.045
g (0.012 (0.03 1-0.055)). Leaf blades
\ navicular to obtuse, l-'lorets usually
I'nn riîilifitlin \ar. /
. Glume 1. Pi: 2.54.5 mm long (3.4 (1.8-4.8)). Si: 2-3.5
mm long (2.7 (1.5 3.8)1: Pi and St: 0.450.8 ...... wide (0.58 (0.33-1)). Lemmas. Pi:
3-5.5 mm long (1.5 (2.8-0)). St: 3-1 mm
long (3.5 (2.8-4.1)); Pi and St: 0.6-1 mm
wide (>.. 8 (0.5.1 1.2)). 1'aleas. Pi and St:
2.8-3.8 mm long (3.1 (I... 1.1 ii: Pi and
St: 0.4-0.7 mm wide (0.54 (0.3-1))
Florets usually viviparous [not in /' Uul>i>
"Hv in I', drnu.huo] CI,
Pi: 1-7 , ... long (5.1 (3.3-7.5)1. St:
long (1.5 (2.0 7.5)): Pi and
St: 0.7-1.1 mm vide (0.82 (0.52-1.3)).
Lemmas. Pi: 4.5-8 m
St: 4-6.5 mm long (i
0.9-1.3 mm wide (L
- with short or long. wo..IK hairs:
18'.
blades conduplicate: 0.15-0.24 mm thick

(0.20 (0.17-0,18)). (dume I, 1-nerved.
Lemmas. Pi and St: 0.7-0.9 mm wide
(0.8 (0.05 1.2)). Palcas. Pi and St: 0.1.50.7 mm wide (0.6 (0.4-1))
I'ua resinulosa compi
Plants eaespitous. Leaf blades Hat; 0.130.17 mm thick (0.15 (0.13-(I. IP.)). Glume
L 3-nerved (I). Lemmas. Pi and Si: 0.60.7 mm wide (0.0.5 (0,5 I-0.80)). Palcas. Pi
St: 7-20 mm In,,.- i I
19'.
i . t, J.! ,
is
6.5 mm long (5.6 (3.9-7.5)); Pi and St:

0.7-1 mm wide (0 ')
.(. I I 3)1 l,,,n.is.
Pi: 5.5-8 mm (7 (5-8.8)). St: 5-6.5 mm
(6 (4.8-6.9)). Pistillate floret callus with
short or long, woolly hairs
Poa pogonanllia
Vmpatou- H..i< i IU
.-ion illv present. Spikelets. Pi and St: .",-7 mm long
(6 (5-7.7)). Glume I. Pi: 3.5-5 mm long
(4.3 (3.3-5.3)1. Si: 3-1 ...... long (3.6 (3[
I'): P nd St: U.6-U.K ...... id,
<0.51-0.83l). Lemmas. Pi: 1.5-5.5 mm
long (5.3 ( 1,3 >.;;>). St: 1-5 ..mi long ( 1.5
(4-5.2)). Pistill
. i . ,11.
.ml
woolly hairs
Poa denudata
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n
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'' '
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,.;>h\l(u Hack. (DO)
. Hack. (DU)
P. holciformis J. Presl (HO)
i Parodi (HB)
P. iridifolia Hauman (IR)

P. lanigera Nees (LG)
1
;. lugin a Poir. (LA)
P. I teutons Nces ex Steud. (LI)
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'<' . ,,,:', hi,
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,1 !
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I
I
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r;1 t
the World. C \ B International. Wallmgford, U.K.
/nloa-a. F. ().. E. O. Nicora. Z. E. Rugolo de Agrasar, 0.
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de la lamilia Poaceae en la Republic., Wgentina. Mou-
!i parentheses correspond
Parodi (BA)
PI,,.:,. I he on. (BE)
chubutensis Speg. (BU)
, ..,.,_,.,,,. a Phil. (PA)
\ , i iPI i
\ pilcomayensis Hack. (PI)
' ,..., - nil I r if c I I ii li IP" ,)
liendle (PR)
'. resinnlosa Nees ex Steud. (RE)
- Mend. (RI)
* schlzantha Parodi (SC)
i/iuia (Speg.) Parod, (SKI
>. stuckertii (\\-M\.) Parodi (ST)
> superbiem (Steud. I Hauman K Parodi (SI i
i E. Desv. ex Gay (TR)
\lTI Ml\ 2.
Specimens listed here were used as OTUs in the phen. li. .IIIUINH-. Hi, x ,,. soil, J
ii .11 I. | .
or specie- complexes .is identified in this research. Prcets corresponding to the species abbreviation as set m the
Malvinas represents a similar location to the I

lands on specimen labels.
Poa alopecurna
ARGENTINA. Santa Cruz: Depto. Giier Aike, Entre
Glcncrossv P|;1. \lla. 51 lO'S. 71 T-3'W. 1976, LotOW *
i\Bl |\l. I
N|. I
m.-aal norte de 28
de NoMembre. 5I3.VS. 7211'W, 13 Jan. 1976, Lalour et
al. 382 (BAB) |SK. P,|: ruta 3. a B km al W de Rfo
Gallegos, 5137'S, 00 25'W. 5 Nov. 1077. rt,' X II, n.lr.
(B B SK. Pi and St|: Kstanca Gem, Castillo, La. 1077.
et al. 1367 (BAB) |SU. St.]: Ugo Argent.no. I'm Ho Ban
dera. 50 IBS. 72 17 \\. Correa el al. 3032 (BAA) [SI .
Pi|: Estancia Las V iscaehas. (run Las \ iscaehas.
5046'S. 720r\\.2. Ian 1077 \im\oet
I
I
[SI . Pi]: Cerro sin nombre, 5046'S, 7208'W, 29 Jan.
1077. \m,u, ,! al. 2(,U iB\B) |Sl . Pi|. Tierra del Fuego Isla <ll Allai.li.-,, Sur: Mas Malvmas. Isla Soledad. .,2'O0'S. .VrOO'W. C,au,livhaa,l C. s.n. I \rundo alo
/''' U! U,. < : Ill II - Mill. -.Il'.-.p . I'. \ \. fl.lL'lrerlf ! | \l .
Pi|: bias Malvinas, 52WS, 5900'W, Hooker s.n. (Fes,, , < an, >el ,.. -y Hook f.. Isolvp. . V. \ \
Mil
| \L. Pi and Sl|: I shnaia. Is. de los Kslados. Port \ancouver. 5L10S. 0P2()'W. Spegazzim s.n. (/.,
Speg.. isolvpe. |.P) |SK. Pi|: Canal de Beagle. Isla dc los
Carolines. 5I52'S, 6818'W, Vervoorst 161 (BAA) | AL.
Si|; Islasdeios Estados. Bnliia EibcrH. 54'50'S. !>l 2.YW.

2 Nov. 1971, Durffcy et al. 1301 (BAB) |AI, Sl|: Islas tie
l.,s Esiados. Puerto Vancouver. 5449'S, 6420'W, 16 Jan.
1
I.M. \ N|: Islasdeios Estados, Puerto Cook, 5450'S, 6420'W, 4 Jan. 1934, Casr,2<> (BAB) [AL St]: Is. de los Fstados. Pto.
o.,k .1 l<'s
| ,,
i
(Sll |SK. I'i|. Bahia rhetis, Region del Rio del Fuego,
I I -s. ,," . W \1 , |'.< //... .... A . . ...
">'/ i:\i: ; \i f I
M ii'
i>
i
(,.-,.w,v\\. N Feb. <)(;:. \h>:r /,';-7ii-;\Bi|\i.. N . lb

molino, 5450'S, 6753'W, 21 Dec. 1932. ',,//.,
7579 (B\B) ! V . Sl|. CHIEF. Mill Itrpinn: San.h Point.
5310'S, 7054'W, W. Lechler 1194 (Aira superbiens
S II I ,- i ,,. I'M
,,,., ||SI l'i| Islol, I'm. I.uisa.
,'
-
\
I \ |\| N| >iena
Baguales, Ea. La Cumbre. Co. sin nombre. 50 I2'S.
72 22'W, L8 Dee. 1975, Boelcke et al. 682 (BAB) [AL, Pi
and St]; Punto Bella Vista, 5130'S, 7315'W, 5 Dee.
1979, Roig et al. 5097 (BAB) [AL, Pi]; Estaneia Cerro
, i!
I! ... - " ,
i
14 Jan 1^77. Uitour et al. 1493 (BAB) [SK, Pt]; Laguna I i; . ,.
5128'S, 7227'W, 12 Jan. 1977, Latour et al. 136\ (B ^B)
[SU, St.]; Seccion Tres Pasos, Hotel, 5125'S, 7229'W,
14 Jan. 1977, Latour et al. 1600 (BAB) [SI . Pi|: hitour
et al. 1574 (BAB) [SU. Pi].
\UOF\T1\\. HlirH.,, Vice,; Balm. BhlK a. Pinna

\
';. ." - i.J "I W I. . l-iiij >.,.
; ',
(B\I!|[I!E. Pi|: P:irl..:<;.- ,;,! D,.,rr-Kn. \1-l,- llermoM,.
3859'S,61 L7'W, 50 Oct. 1 OB I
H ||i
Pi and St], 31 Oct. 1985. Villamil 3413 (SI) | UK. Pi|. 6
Nov. 1986, Villamil 4291 (SI) [BE, Pi]; Camino a Monte
<>< !;< i
.,.
;.. ,H |i:i p,| ,M. , i. <
breraetal. 17061 ,1 P)|i:i l'i| .,/.. . ., ,./ , I
|l'
Si | i...- ., . ,' ..-.
:
ill". |l!l. -i|. 2 1 \..v
I".,; / .
,v v
. ,' - I I- !',) |- l- t . .. I llegrini. Pellegrini. 3616'S, 6310'W, 28 Nov. 1940, Call.P). [BE, Pi]; Partido Coronel Rosales, Pehuen-Co, 3900'S. 6133'W. 19 Nov. 1962. Cabrera X
f
II
|
I
I inn. \1e,la,,o>
3850'S, 6242'W, 6 Nov. 1940, Cabrera 667 ' I
Pi]; Partido Cm i
'
i h nn u '.. 0, ->
5651'W, 11 Dec. 1950, Cabrera 10707 (LP) |BF. Pi|:
Partido Tres Arroyos, Claromeco, 3852'S, 6004'W, 8
Nov. 1986, Villamil I2H iS i II.I.. I*i|- Partido Ceneral
\hara1lo. Miramar. 3!V 10'S. 57 52'\\. 31 Jan. 1630. />,,m,h " ' ' ! li..|
l: \\i |BA. Pi]. 11 Nov. 1636. Cabrera 5555 (BAA) |B\. St|. Sep. I'22. Ilauman 57t,2
(BAA) [BA, Pi]; Partido Loberfa. Quequen, 3832'S,
5842'W, Jan. 1630. Cabrera 1317 (Sll [BA. St|. Feb.
I :../......... ; i i: \\) | BA, St], 7 Nov. 1943, Boelcke
s.n. |SI)|B\. P , ]N| I .. i I ... , ' I'M. MI,.Inn \ln
d.-l Plata, 3800'S, 57 34'W; 9 Dec. 1947, Bod-A-v :*.'"(BAA) [BA, Pi], Jan. 1923. Barros 4898 (BAA) [BA. Pi].
6 Dec. 1647. line!,
1
K .. N.-^ro:
Adolfo Alsina, medanos en la bora del Km Vgm.
1! <>3>. (2 i;r\\. /,',,:, ;.vr, ih. loU|.c. con |BI . I .|
URUGUAY. Col,..,,,.
i I... In
2.VS. 5752'W, 12
Oct. 1936, Cabrera 3872 (BAA) [BE, Pi].
\K;i VI IN \. Buenos Wcs: Bio \ icdma. Sep. 1934.

Huium-lei U)'nn\ Vl |BY ;'i .- :l s, : |>,lrtlI]<, \v, II.,,.,,!.,.
Avellaneda. 3440'S, 5823'W, 14 Oct. 1922, Parodi
4747 (BAA) [BN. Pi and St]: Partido Dolor,-. Laguna S.vigne. 3612'S, 5744'W. II Oct. 1662. Cam, I HiWi
|BY Si |: Partido La Plata. U Plata, en el Jardm /,,.>!
ir... .'. I ..VS. 5757'W, Nov. 1962, Torres 1023 :1 P) | Ml I
M i
o; >. ,; i..\\ I : \. |'.2 r ,.,. f . . . . .
iSl) |\1d. Pi|. Entre Rios: Depto. Gualeguavchu. E.
Carbo. 3309'S. 5914'W, 23 Oct. 1949. Bud;.*
' ;:'
iSh [BN. Pi]: Paranacito. 3342'S. 5901"vV. Oct. 1646.
Ragonese & Crovetto 25 (BAB) [BN. Pi and St]; Medanos.
3325'S. 5904'W, 2 Dec. 1930, Parodi 9445 (BAA) [BN.
Pi and St|; Delta inferior. Arroyo Martin./. 33 ".2'S.
.:: ;<s'V\. OH I'M). /;.-/,,;/ /...-'.'/ oi, :\in. si|./.,-,/,
i504.? (SI) [MO, St]; Depto. Gualeguav. la \.-r,lc
3309'S. 5920'W, 21 Oct. 16 pi
Pi]; Depto. La Paz, Arroyo Feliciano, 3044'S. 56 .',;; \\.
17 Oct. I6H0. Uufioz 1353 (Sll |\IO. Pi and Si|. >,.qiu'-n: It. pi... Facar. San Martfn de Ix)s Andes. 10 Id's.
71 21 W. 30 Jan. 1959, Ruiz Leal 20315 (holoH , . B\\i
[PN, Pi[. 6 Jan. I)
I! \ \i |P\. Pi|. 22
Jan. 1966, Eskmhr 59] (B\A) |P\. Pi|: Cerro al Norte
de San Martin de los Andes. 40 I0S. 71 21 W. 10 Dec.
1946, Dawson 1287 1/2 (BAA) [PN, Pi]. URFGFAY.
luimcdos. Nov i
II i i
I h
HI
[MO. Pi and St|: Fra\ Bentos. 33 10'S. 5815'W. 5 Oct.
1934, Meyer 1037 (BAA) [M0, St]. Soriaiu.: Wu.
Grande, Paso de Los Loros, 19 Nov. 1937. Rosengurtt
2294 (BAA) [M0, St].
Poa denudala
ARGENTINA. Neuquen: Depto. Picunches. Pino
Hachado. Oiilla afluentc \rro\o Haichol. 3840'S.
70 51 V\. 21 Jan. 1963, Valla et al. 3024 <B\ \i |DF. Pi
and St); Depto. Fos Fagos. Villa Pnerlo Manzano. 10 1<>'S.
71 37 W : Dr.
"
<H\
M [1)1 Pi nidSt|
Cerro O'l.onnor, 4049'S, 7137'W, 25 Nov. 1603. Dim,
.''" il \\) |DE. Pi and Si|; Isla Victoria. 4054'S.
7134'W, 11 Nov. 1946, Perrone 15212 (BAA) |NA. St|:
...
. I
hi,
I".
/..
,, .>
!'>
,v I
|DE. Pi|: Peninsula Ouetrihue, 4052'S, 7138'W. 1 Jan.

p. . B\A)[NA. Pi
and St|: Pnerlo San Patricio. I0 52'S. 7138'W, 7 Nov.
p>;i. /;;.,., :;"] n\ \ \\\. M . 30 \ .-. PM2. nm //..
(BAA) [NA, St]. Rio Negro: Depto. Nahuel Huap,. F..g<.
(iuliemv.. II"OB'S. 71 "20'W. 28 Oct. 1949. Boelcke &
Hunziker3418 (BAA) [DE. Pi and St]. CHIFE. X Regi6n:
Valdivia. 3949'S. 7314'W. Ischler W. 578 (BAA. fragment) [DE. Pi].
Poa dolichophylla complex
Poa dolichophylla: ARGENTINA. La Rioja: D.-pi,,
Ea.natina. Sierra Famatina. Mina El Oro. 2855'S.
6731'W, 6 Feb. 1956, Calderdn 1115 (BAA) [DO. Pi], 7
Feb. 1956, Colder,
'
V |
'i| In, ,.,, .,.:
Depto. Chi.-ligaMa. I.a Ban.lerila. rnta 65, 2720'S.
6600'W. 14 Oct. 1966. Boelcke et al. 5505 (BAA) [DO.
Pi and St|; Depto. Tafi. Bajo de Anfania. 27 U.S.
6534'W. 6 Aug. 1906, Lillo 5066 (isotvpe. BWi |DO.
Pi|: \iille Calcliaqui, Penas Azules, 2635'S. 65 10\\. 27
.I.,,,. l'i;;. /, /, v. ,i \\i ,ii o i-,| < ,.,, I I Negrito. 2d r'S. 05 I L\\. 19 Jan. 1964. Giusti et al. 2868
|R\ \) | DO. I'i|; U Puerta, 29 Jan. 1933. /',,/, 10801
11.1') 11 ID. S||; \alle Caleliaqm. I'enas Azules, 2635'S.
05 I0'\\. 27 Jan. 1933. I'annl, 10027 lit \ \l |l>0. Pi a.id
St]. P. iridifolia: ARGENTINA. Hu.no. We*: P.nti.l,.
Balearee.QuintaSagenave,3752'S,5815'\\. 12 2.5 (M.
. ,i!\\ |ii; s,| r. ,II .,,,i
Plata.
,, ,,V
Dee. 1930. /
L938, (
65 21'^
ti.I.> Tamlil. Sierra <le las
Nov. 1940. Cabrera 6810
.VMtB'W !()\n
Nov. 1933. /;-/,., > > ,,
37 20'S. ,,9()ir\\. I Nov.
i 4756 (SI) [IK. St]; ParAnimas. 37"29'S. .,9 |}','\\. 21

(SI) |IK. P,|; land,I. 37 20 S.
iK\\)|IK.St|. I.",
iSli|li:
.|:S;.-,
,
1919. Huken 21 (SI) [IK. St|;
. Nov. I93B, Cabrera 4687 (SI)

111!. Pi|; Cm, ,1.- la \enlana. 38 IK'.'S. (>147'W, 7 Oct.
1939. Cabrera 5886 (SI) |IK. Pi|. 9 Nov. 193.", 0,,/,/,,,,
17 K, (Si! | IK. St|: C.-no Napo.la. b.Maneia Lamina.
33 Oil's, ol |.7'\\. 17 Nov. 1972. t,o,nez et al. 11719
(I". \ \l |IK. l'i| /'/>'''"''"" \,-,,M; v I ../,,,w. . ,-,. /',', ' \li
(.1NUNC T.i.uniaii: Deplo. Cl.i.ligasta. Lstamia Las
Pavas. Puerto El Ravo. 27"|9'S. 0.5 5.5'U. Mar. 192 1. |,-
tun 81)77 (SI) |PC. St|. Venturi 8074 (SI) |PC. P,|: I >,-,,(.,.
I! mrailL Oueh.ada :|. I l.'io <,l.....|o. : . |9'S .,. 22'W,
2( \ug. 193'). l/ewv I 1080 iK-W) |PC. Pi ami St |: Our
brada .|e Loirs. 20 50'>. 0.5 21'\\. 3 Nov. 1929. lr,,/(/
9066 (LP) [PC. St|: Depto. Uouleros. Onebrada <le los
S..S..2- 09 s ,,
|.
|PC. Pi|: Depto. Taff. Bajo de Anfama. 27k>'S. 0.3 31 \\.
6 Sep. 1906. I Alio 5064 (isolvpe. SI fragment) |PC. St |:
Pun la <l<> San Javier, 2646'S, 6521'W. Dee. 192.3. \m
tun 2510 (SI. LP) |PC. Pi ami Sl|: Depto. Lamas. Plava
del no de la llova.la. 20.3 1'S. 06 21'W. 23 Nov. I "2 I.
\ heile, 1855 (K\ \l |PC. Pi|. /'. stuekerln: ARGENTINA.
< ..nlnha: D.plo Poelio. Cainuio a los Gigantes. Cerro
Klaneo. proximo al K.'o Juspe. 3 I 27'S. 6 I 3,",' \\. 5 Dr..
1958. Nicora 6642 (BAA) [ST. Pi|: Depto. San Alberto.
Pampa.le \. Iiala. 3 I 3(.'S.(,| l.VW. 10 Nov, 1923. ///.
en 107,05 (KAA) |ST. St |. I |. De. . |92o. /',,// 7582
(KAA) |ST. P,|. I'anxli 7021 (BAA) |ST. Pi and St|: La
Pusta. 31 li,'s.| 15VA.7 D
[ST St|. 9 Dee. 1993. Cussani s,m2 (SI, | ST. St |. f.iussani
Coineeluuiioiies. 32 3 I'S. (,3'01'\\. 13 Nov. 1925, Castellanos s.n. (KAA) |ST. P,|: Depto. Prin^le,. La Carolina.
32 19S. (69(>'\\. 8 Nov. 1940, Rurkart I 0787 (BAA)
[ST, Pi].
30 IT'S. 70'20'W. 2", Jan. |00l. Hoe/eke el al. 11175

|K\\. K\K) [IK l. Pi|: Deplo. Miliar Surra .1.- Celiieo.
30 21'S. 70 31'W. 29 Jan. 1970. tfoe/eAe rt /. /4087
||{\\) |ll(). Sl|. Yieim.e.il.. de la .-..rdillera .1.-1 \ lento.
3646'S, 7031'W, 2 Feb. 1964. Roeleke et al. 11540
(BAB) |HO. Pi anil St). CHILE. In Cordillera ehilensibus,
Haenke s.n. (isotype, BAA fragment) [HO, Pi].
\|, < o,,lba D, .1,. - , Ml ,.-.., .,!

\eliala. al bajai <!< la Pampa de \. Iiala. 3 50'!-\
6445'W. \-A Dee. 1926, Parodi 7501 (boloi-.,
p.\\i
|HB. Pi|: Sierra dr Aebala. 31 3o'S. 6| L3'\\. 15 Nov.
1878. Hiemnvmus s.n. (BAA) [HB. Pi and St]; Pampa de
V bala. la Posla. 31 3,,'S. ,,1 I3'\\. 9 |).,, 1995, Giussan, ,,, (SI) |HB. St I San Luis: De,
I.aeal.ueo. Sierra
de Comechingones. 32 3 IS. 6.5 01U. 23 Nov. 1923. Caslellan,,, ,.,,. |B\\)|HB. St |; Depl... la I apilal. Ciudad.
33 HfS. (.(> 22'\\ I'u.-o,!, 'r.',., ||'.\\| ||||i. > : Depl...
Pringl.-s. La ( ai..lina. 32 19'S, 6606'W, 8 Nov. 1940,
72 (SI) | UK. Pi and St |; liiukarl 10781 (SI)
ARGENTINA. Mendoza: Depto. Us Heras. Puente

del Inea, \alle de los llo.eones. ,32 30'S, 6955'W, 12
Jan. P63. /;.; (I, I
!1 -i|| N, o.p.e.i
Depto. Cl.os \lalal. Cajon (.rande. Cordillera del \ ient...
36 58'S, 70 30W. 23 Jan. 1933. Regimes, 1. 281 I (ho
lolvpe. KAA) III . Pl|. Cajon de \treueo. Cordillera <lel
Viento, 3658'S. 79 10 \\ 23 I , I"' A' .
(KAA)[HU, Sl|. ( ajon inferioi del \nm, lu,l
1
P>. I /, . ' '
I \ \ |lll
P| D, pi.. \i,in.
, , ' I - o .- \ _- | r |..
,.
,
;,.(KAKl IN . Sl|: \no\ luleimera. . Mo mo sur, 36 23'S.
7037'W. 28 Jan. I<>70. Hoc/eke n al. I 1020 (II. \|!i i||l .
Pi|. K; .. Cahenle.. Km \a.vareo. 36 I2'S. 70 37' \\. 3 I
Jan. 1964, Boeleke et al. 11424 (BAB) |lll. Pi|: Deplo.
Zapala, Zapala. 3,3 33 >. TOOIW. ///., lo5nl (SI)
|lll. P,|: flSauee. 36 02'S. ,0()0'\\. II Dee. 19.32. Cabrera 11175 (LP) |HU. Pi].
ARGENTINA. Neuquen: Depto. Zapala, Zapala,

ivpe. KAA) |IN. Pi and S||. 5 Keb. 1920. I\,m,l, 2721
(BAA) [IN, Pi].
I'oa haletfarmis
AR(;ENTINA. Mendoza: Deplo. Las Heras. Las Cue;,... I!. l.iL..,, M.lii.,, <;, ,-.. I I I.M.I',.1 ;;> !"'s ,0 03'W
10 Jan. 1963. lioeteke el al. 9720 (BAB. SI) | HO. Pi and
St|; Depto. San Carlos. I..-. Paramillos. .amino a Laguna
Diamante. 3 1 10'S. 69 33'\\. 23 Jan. I<>89. <.;, Sosa
215 (SI) |HO. Pi|; 6 km W Refugio Militar General Alva,ado. 3 1 10'S, 6945'W, 17 Jan. 1963. lioebke ,; /.
|i \H [HO I i| N. M.jii.r, I i lo . i,,s \lalal ( a
j6n del Arroyo del eni.e. 36 "43'S. 70 2.3'\\. 27 Jan. 1961,
lloehke rt al. 11265 (BAB) [HO. P,|: \egas del I'elau.
.amino a Kiseos Rayos. 3654'S, 7020"v\. 21 Jan. I9(,l.
lioelekeetal. 11 157 (It A A ) | IIO. Pi and Si |: K iseo, Kav os.
eonflueneia Arroyo Olletas eon el Arrovo Cunleiiv,,.
ARGENTINA. Buenos Aires: Partido Pehuajd, Pehuajo, 3548'S. 61 ,2 \\. 13 o,-t I-CO. />,
(SI) |I.C. Sl|: Parti.lo Tigre. lime. IN(4U1. 3 1 23'S.
5835'W, 13 Oet. 1946. hm/hmrin 527, (SI) |l (.. M|. Kntre Rios: Depl,,. L.d.-raeion. l.d.-raeion. 3I()I'S.
37 33 \\. 23 Sep. 1961. Rurkart 22427 (BA A) |I.C. Pi and
St]; Salto Grande. 3L13'S. 37 56'\\. Klll.l. 1950. ////
(Mi ||l. P,|: II.

I I,inlav. Conee,
n del
Uruguay, 3229'S. .,.'{ I |\\. 17 O, I. 19 |9. /,',/,., : 7<><,
(K\\)|IG. Pi and S||. P\l! \CI W \ll Para..a: M1.,
Teresa. 21 I3S. 5I2LW. 1 Aug. 1945. lie,,on, 1700
(BAA, SI) [LG, Pi],
(isotype, BAA) [LG, Pi s
Hen
I Oct.
Pinamar. 37()7'S. .50 51 '\\. i:5 ().-l. 1973. ZW/m 2/5

(LP) |LA. Pi]; Partido Junin, Medano Grande '.I 27'S.
OlOI'VV 17 Oct. 1910. Cabrera 6.503 (I.P) |I.A. St |; Par3809'S, 61"'.V,'\\. i. <>, i I'..'
IP-! I
Sl|. Cliiihut: Deplo. Km Songticrr. Fstancia La I,unit,,.
14 IPS. 70I5'\\. IK Jan. 1949. Norm//,, .W/o iliWi
[PA. Pi|: Hfo Max.). I Ma,,,,,, Zooleoma Mallin. PI la, ho.
15 II'S. ;016'W. 4 Fell. 1^54. Grondona 3545 (BAA)
[HO. Pi|: Depto. Floro.ilino Ameghino. Calm Raso.
H2ii\ (>5 ip\\. >..-.- o,v; ihololvpe. B\\ liagmeiil) |Bl . Pi|. Jan. 1922. Cielhe, ' i 1. I P. \ \ ) |P\. PI .
Vlriidoza If.-|
- i I! la.J. \allc del \tuel, Kl Sosneado. 3.5 05'S. 0934'W, 4 Oct. 1955. Roche, el al. 301
(hololvpe. BAA) I HO. Pi and St|. Neuquen: Depto. I.os
Lagos. Nahucl Huapi. Fstancia Fort in (,ha, abu.o.
11 O.VS. 71 WW. 3 Nov. 1949. Boelcke & Hunziker 3492
(BAA) |LA. Pi|: Deplo. Mmas. Conilueneia rios Pichi,elcke et al. 13676 (
VA) |LA. Pi
3657'S, 7045'W. 14 Jan. 196 , Boelcke et al. 10772

(BAA) |LA. Pi). Rio Negro: Drpi... Uollaneda. ruta 22.
50 kin ante. ,lc Chocl chocl. 3910'S, 6505'W. Bacigalupo V. & \icora E. 1165/ 1/2 <BA\> | H(). Pi|: Deplo.
\,,,|nnu. Hfo Chic,,. 4I42'S. 7()27'W. 9 Nov. 1949.
.W.;r5/ iHAM [HO. Pi and Si|: llcpt,,. \wll;, I,,.
riila 250. 120 km antes ,lc Ocneral Concsa. 39"45'S.
05 2o'\\. 7 Nov. 1972. llacllialnfloA Mrora 11676(BAA)
[LA. Pi|; Isla Chocl Cliocl. orilla del Hfo Nog,,,. 39' lO'S.
05 30'\\. 7 Nov. 1972. llarâiupoX: Wo/,/ //o5/|BA\)
[LA. Pi and St|: Choel chocl. 3910'S. 05()5'W. Baeigalu;>n A \,cm 11651 (BAA) [BO. St]; Depto. Pi, In Mahuida.
a 20 km S dc Hfo Colorado. 39'03'S. 0L20'W. 7 Nov.
1905. Correa & Mrora 3168 (H \ \ I 11 \. Pi and S| | Santa Cruz: Depto. Magallanes, San Julian. 5 km al sur por
22 '
963,
Canea el al '63 <! I i |l
Pi|; l),-|-.|o. (
H(o Cine. Kstablecimiento Us Vegas, 5007'S, 0837'W.
Nov. 1922. Dauber 165 (BAA) [PA. Pi and St]; Orilla del
Hfo Chic, ruta 3. 49 49'S. Ott37'W. 3 Deo. 1971. Boelcke el al. 15315 (HAH) |BL. Pi|; Depto. Desea,!,,. Puerto
IWado. Canadon ,1.1 \ni,n;
17 PVS. 0.5'54'W. 12
Nov. 1905. Correa & Mrora 3317 (BAA) |P\. Si |; |),.pt.
Lago Argentino. Campos dc Bilbao. Monte Buenos Aires.
;,()3;:s. 72 r.rw..'. hi,, 101 I. //, ,., /. 152 (H\\)
|PA. St|; Depto. Hfo Chico. Canadon Leon. IHlO'S.
70 lO'W. Mi,,. P>;,2. Cilladin, III (It \\) |P\. Sl|. (,11a
dun 21 IHW) I Ml . Pi|. Tierra del Kliego e Isla- del
, N\\ ,le Hfo Crandc 5.341'S. 075()'\\. 3 Jan. I'XA
,ore 1493 (BAA) |P\. Pi|. (dill I Nil He-ion:
-.to. eerca del origen del no, 52(X)'S, 7224'W. 1 I Dec.
77, Ibar s.n. (holotype. BAA fragment) [PA, St].
\I!(,PMI\\ It,,, ,,- \,- I! ,i, , I

1 , i
Palua Blanea. 3H IPS. 02 lO'W. Honshu, 552 Itvpe.
H\\ rragnie.illlLI. Si |. Clara: 34 il'. denudala
Hall. H\ \ fragment) [LI, St]. Chubut: Deplo. Hiedma.
Puerto Madmi. Uguna Blanea, 4247'S. (,, 02W. I.'!
Oel. 1000. Ilclilie, A- lleeskuw I 132 (SI) | LI. Si |. 30 Oct.
I' " /:,,//,

/ - (si, |i i p, i , ,,, s..,.., ,, io
km de Puerto Mad
. 22'W. 11 Oct. 1995.
Bertiller 3395 (SI) [LI. St], Bertiller 3411 (SI) [LI, Pi];
Depto. Hawson. Trelew. 4315'S. 0519'W. 10 Oct. 1940.
Soriano 1867 (SI) [LI. Pi]. La Pampa: Depto. Chical-Co,
Cerro Los (inanaros. Oct. 1900. Cano 1119 (BAB) [LI.
Sl|; Deplo. I Irae.Hl. F.lltre Alreiico v Ouchlie. 37'05'S.
01 1 l'W. 10 Jan. 1995. Ragonese & I'iecinini 18205
(BAB) [LI, Pi]. Mendwa: Depto. Pas Moras. Pucsto Pa
Obligaeidn, 20 Nov. 1943. Coras 20>>7 (SI) [II- Pi|. Neqm'n: I ' |
,
d, la , iud id de
Neuquen. 3858'S. 6803'W, Jan. 1978. Leon 2232 (BAA)
[LI. Pi], Iron 2257 (BAA) |LI. Pi and St]. Rio Negro:
Deplo. Uellaneda. ruta 22. 50 km antes de Chocl Chocl.
.JO | OX 0505 \\. (, \m. 1072. Hangalupo & Nicora
11646 (SI) [LI, Pi]; Depto. Conesa, ruta 251 a 13 km al
N d, (.< n< , il t or ,
, in .
Hio Coloradi
91 illWl |LI. Pi and
S||; Deplo. San \ntmo. Sierra Grande, 4138'S, 0523'W.
I'iecinini X Irguizamon 1610 (BAA) [LI. Pi]: ruta 3 a 8
com 3193 (BAA) [LI. Pi and Si |. Santa Cruz: Deplo.
I
n
I li
I7 2,x ,./ ,12 \\ i
(BAA) [LI, Pi and St].
,,,,
'
ARGKNTINA. Entre Rios: Depto. Con<rdia. Panjue

Hivadavia. 3123'S. 58()LW. 22 Sep. 1901. liurkari
22456 (SI) [PI, Pi and St]; Depto. Gualegua\. La \erd.-.
21 Nov. 1949. Hurkart 13(11,1 (Sli | II. Pi and Si |: Islas
Lech,-uanas. Delia medio Irenle a Ha.nallo. 33 20'S.
0001'W, 30 Dec. 1941, Burkart 12874 (SI) |PP St|: Dep
to. Victoria. Isla del Frances frente a Hosano. 32 57'S.
00 30 \\. 1.5 Dc. 1037. Ihnkail 3351 (SI) | PI. Pi in.l Si |.
Burkart 8817 (SI) [PI, Pi].
Poa pogonantha
II i,|i,
* oional Los Alerces, Laguna Cisne, 4230'S.
7151'W, 10 Dee. 1902, Roquero 5389 (BAA) | PG. Pi|:
Dept,,. Hfo ScMjijien. Pago Fontana. Fstancia la Pep,la.
I 1 .55 S. 70 5i!'\\. 20 Jan. 1090. .Sunano 5662 IllWl
| PH. Pi|: l.ao fontana. Lolc 15. II 50'S. 71 30\\. 1/,//
IJ\\i|PH. P.
|N|. Ma,I,noli
& Boggiano 15079 (BAA) |I'H. S||. II Pel,. 1932. (.as
tellanos 9966 (BAA) PR, P1J, Hartmoli & Boggiano
15077 .11 \\ 11 . (BAA) |PH. St]; Uigo Fontana, Fstancia La Pepita,
II :,-,'>. 7()58'W, 29 Jan. 1900, Soriano 2613 il'.Wi
| PH. Pi|; Depto. Tehuelches. Lago Vintter, 4358'S,
71 3.3'\\. 2 Pel,. 1989. Sieora 9473 b (SI) |P(,. Sl|: Lag..
Mutter, plava arenosa. 13 .5!','S. 71 33'\\. 7 Feb. 1989.
\icnra 9537 (SI) |PG. Pi]. Rio Negro: Deplo. Hanloche.
Panpic Nacional Nahucl lluapi. \ enl i-..pie,o fnas.
4111'S, 7149'W, 13 Jan. 1952, Boelcke & Correa 5500
(HAH) |PC. Pi and S||: !,,,, I,,,.. || ()LS. 71 |9'\\.
8 Jan. 1952, Boelcke & Correa 5373 (BAB) [PG. Pi|. IM
eke & Correa 5380 (BAA) |P(5. Pi |; Lago Hoca. Arrovo
Apoc. 11 2.3'S. 71 47'W. 20 Jan. 1952. Boelcke & Correa
6045 1/2 (BAA) [PG. St]. Tierra del Fuego e Islas del
111.mi,,.. Sur: Depto. I -huaia. Glaeiar Mailialcs.
51 15'S. (} |;;\\. 9 |),e. 1902. Correa et al. 5365 (BAA)
[PG, Pi]. CHILE. XII Region: Lago Azul. 5 L 27'S.
18'W, 10 Jan. 1977. Moore & Pisano I 77.) (BAB) |PG.
Si |
; Islas Wollaston. Calela Lientur. 5544'S, 6719'W, 23
mnil-Malal. 3940'S. 7122'W. Neumeyer 31 (BAA) |HE.
i. 1980, Pisano 5112 (SI) [PC. St]; Estanria Cerro Cas-
Pi and Si |. Deplo. Los Lagos. Kslaneia FortinChacabu.ro,
o, Cerro Solitario, 512()'S, 7237'W, 18 Jan. 1977. La-
II 02'S. 71
San Martm de los Andes, camino entre h.log v Ma-
I , W
-.'
.11 \ \
|BI. Pi and
r et al.
St]. Santa Fe: Depto. Vera, Calehaqiif. 2954'S. 6018'W.
1739 (BAB) [PC, Pi]; Peninsula W desembo-
7 June 1965, Alonso 866 (SI) [RE. Pi].
!'<! liiji'.!ili70;'
AB(;FN TIN A. Santa Cruz: Deplo. Cher Aike. Estaneia
/',,, luahiu-nu: BO
IM \
Liticaea. Isla del Sol.
I si I'JIZ: M.mm kapa. . !
K>'03'S. (,) 10'W 2(> Jan
if...
P>8(>.
Ol
km hacia el nevado Illimani,

1983. IM, >:
FCl'I'.l
1640'S, 6745'W,
P,|
19
On.ro: Avaroa en-
tre Cl.allapala v
lolapalea. 192()'S. 0050'W. Feb. 1979.
Ceballos
236
et
OG33'W.
al.
Feb.
(SI)
[BT,
Pi];
La
Paz,
l'i|: 12 ki,
P.
... 1 -i
IV.lo-.: -.-
I!..
I.
il
>2. /',., ,v
Tariju:
:--..'./.
//,'.'; ii Pi:. |i;i
...I N|
Mile/ Cerea de Cobres. 2138'S, 6447'W, 29
\>n,(>. liustinn Oil <I.PB||BT
aiaensis:
\ H( d.NI I N A. Jujuj : Deplo. |)|J. Manuel
Bel-
1971. Corn;, el al. 6100 (SI I |0L. Si]:
U-pto. II. mahnaea. Vl.na
Feb. 1972. Rulhsai
\g,ular. 23 I2'S. 1,5
II'W. 23
(B\ M |CL. Pi|: A bra entre
lruva e Iturbe. 2258'S. 0521'W. 25 Jan. 1972. Ruthsatz

(B
\| |< L. S||: Deplo. Santa Bail.a.a. 1,1 Lne.le.
2207'S, 6526'W, 18 Feb.
1972, Cabrera et al. 22230
(BAA) [CL. Pi|; Deplo. S.isques. Cerro Tnzgle. 2326'S.

0<>30'W. 3 Mar.
19h7.
I'mnl.ava. \olean.
Feb.
Chic...
22O0'S.
Werner 7f> < 1.1*1 |( I . Pi |: Deplo.
M.ra del Paraguav. 23 55'S. 03 27'W.
1927. \enln
1005 (SI) |CL. St|: Deplo. Yavi. Yavi
0,3'28'W.
Mar.
|B\M|CL. Si|:0!ueladade K
2(1 I.I.
1903
Cab,,
1940.
Merer
11920
.em. 22 I8'S.0.3 3.VW
(Ml |' !
I .|
-all .
'
Cerro
Punla
(-mesa.
|B\B)
P'7(..
Estanria Punla
Menra -L., ,1
UK
)/-,'/
\\) |l;l. Pi and Sl|: enl.e I staneia (ileneross v
.,,... -I Ills 71 12 W. II De,

el al.
Ii
sle de K.laneia I'nnta del Monte, eniee a
1970. lalau,
1057 (BAB) |RI. St]: Estanria Primavera. rnla 293.
5127'S, 7215'W.
al.
000
|07o. hit.mt et al.
(BAB)
(><) KVW. II
-i|:
l.'i;. .
|KI.
(BAB)
Sl|:
Bajo
IPX! iBMO |l!l.
La
Leona.
51"3I'S.
Nov. 1977, Roig & Mndez 2437 (B\B)\\U.

I. '.
., ..
-Ian. i i V
as. 5I45'S. 70"I()'W.
I'i and Si |. /' ealrha
gian... (.amino de liiiella de Alto L.zano a Tiraxi, 2405'S.

6540'W, 3 Nov.
,(.'\\.
Pi]; Punta Lovola. 31 3ll'S. (.<> 1 I W. <3 Dee. P>7(>. Lalau,
'..
el
Jar,
Latorre.
530 |B\B| |BI. Pi|:
Seecion Magan. 31 32'S. 71 33\\. 1077. /,,- A
|)||. liuehlien <>. 21(>7 (svnlvpe. BAA)
liana On.ro. K>20'S. 0805'W 0 Mar. 1993, Peterson et

1271 I ill'BiiB
mesela
Loyola, 5144'S. (..",
1836'S,
|BL Si|: Poop... a 4.5 km al norte de La Paz. sol.re la mla
al
Kiver.
1976, Latour et al.
Uberman 1289 (LPB) [BT. St]; Murillo, l.a Pa/-Calae
Jan.
Slag
5132'S, 7205'W, 25 Jan. I97P
| HI. I'i|: Kslaneia Punta Alta, 5143'S. 7158'W. 21 Jan.
[RI,
St|:
10 Dee.
Estanria
-,.!., \
Pas Buitrer-
1975. Arroyo et al. 410
(aiakenken
Aike.
5L27'S.
0918'W. 11 Nov. 1977. Roig & Mtndez 24H5 i\)\\\>\ \i\

Pi and St |. Tierra del Kuep. e Ish.s del Atlanluo S.ir:
Deplo
Bio
Grand.-.
oi\:\ ,\\. 20 N.n.
Kslaneia
El
Salvador,
1971. lioelckeet al.
5339'S,
15093 (BAB) [BJ
Pi|; 51 km N de San Sebastian. Estanria (allien. 32 53'S.

(,0 30'W. 21
Nov. PGI. Hoeteke el al.
Pi|: Kslaneia Seeutida

7.V>7
ll?\ \l
| It I.
\rg.-ntiua. Jan.
Pi|:
Mas
32 OO'S. 39(H) W. Sep.

Slend.J,
70
,1 W.
19.3;',. Ca^rlianus
Porl
William.
1,330. hrhle, s.n. (P. rigidifolia
tvpr.BU fragment) [BJ.KJ. CHE E
gion: Aestate. Mai

,sotvpe.
15150 (BAA) [RI.
Mabinas.
B\\
I93(.
Ph
Iragmenli | RI.
Get.
187,2.
KB Re-
I I,,I
I'.|: Sn.dv
hrhle,
1008b
Point. 33 10'S.
(Aim
spiciformis
Steud., holotype, BAA fragment) [RI. Pi].
Cuaehipas, Pampa Grande, 2552'S. 6530'W. Ma.. I-MM).
I
ill'. II.., n........ D. pt.. I.il
Cutiibre> (.alehaquies. 2o33'S. (,3 KI'W. 29 Jan. 1907.
/,//, .."". i,,i..p.. I;\\I |I.I. N| / ,/<;...,/. i'\i;\
GUAY. Caaeuazu: Yhu, 2501'S. 5558'W. 19 >.,,. lJMJ.
Poa rigidifolia var. ibari
Pedersen 15049 (holotvpe. SI) |PK. P, an.l St|. /' n-sirn,
Giiakenken
losa:
O:\IM \\)\ . Pi|; mla 3. eruee eon eamino a Puertr, Gov le.
ARGENTINA.
Buenos
Aires:
Part,do
General
MJGI'.N TIN \.
P.iewredon. Eslaneia la Bra\n. Siena de \;,lde/. 37 3 PS.
3L05'S.
3BD0'W.
(B AM | IB.
Part,do
1.3 Nov.
1977. lioelrkeel al.
lorn,|.list. K>laneia Cl.iea \
701 (SI) |KK. P,|;
Kslaneia Fort in Cha-
Chuhut:
ll'39'S. 00'KI'W.
Deplo.
19 Del.
\,ke.
(,9 27'W.
P,|.
31 23'S.
2 1
09 18'W
Nov.
E>lan.-ia
PH,',.
| IS I _
P.
and
Si |
18 Nov.
1981.
CI...I...1: D. pi
I II
71 Ol'W. ialnlir s.n.

Los
Alerees.
B,o
.1.
.Ii
lliWl |l!l.
Pereev.
Cerro
Sum. a. HHI\
Pi|:
Parque Nacional
Ceballos,
4255'S,
arro 192 (BAA) [BK. St]; Depto.

Languifleo, Rfo Teeka. Pampa Glnra.
cormi
et
,.,
al.
2133
2790
El.as.
31 2 I'S. 71 2 I'W. 20 Jan. 1978. Roig et al. 2865 (BAA)
W 20
. 51^
i | IB. Pi]; Cumbre
V,-
llamil21I0(S\)\H\, si |. \ ,llam,l 207,1 (SI||KK. Pi and

N|
uel.nl.
1915 (BAA)
/.
! Mancia Mamim-Co.
Cerro del Potrero. 38 0.3S. Ol 3o'W.
Ro,g
La Cailola -eeeion San
co, Cerro La Vieja, 3806'S, 6214'W, 17 Nov. 1981. Villa.;,./ 20, 'I iSII
Aniegliin...
1946. Soriano
[Dl . Pi an.l St|. Santa Cruz: Deplo. Giier \ike. I >!.,a
13 28'S. 70 "51'W
8 Nov.. Skottsberg s.n. </' derolorata I'M-., isotype. BAA
37/7 i
1978.
See.,..,, San
Antonio. 5124'S, 71.'
Rain el al. 2750 (B A M| IB. Pi and Si|; Esian.iaCon.lo,.

31 7,0'S. 09 | |'\\. 8 Dee.
1070. Ixitour el al. 377 |BM0
[IB. Sl|; Bajo La Leona. 31 3 I S. (,<> Ii. W. |977.o/>*

Mtndez
2436
(BAB)
|IB.
31 23'S. 70 32'W. 21 Jan.
Sl|;
Estanria
Los
Vas.os.
1978, Roig et al 2877 (BAB)
|IB. St]; Depto. Ugo Argenlino, mla 40. a 100 km al NW

10 k, i
P)|'i
ill.
M.i,
2"
//,, //, HOIK! |SI IKK. M|
I -
.,.!
II'W.
Nov.
de La Esperan/a l.ae.a lago Argenlino, 5021'S, 7140'W,
Mend../a: Mend.:,-;,.
Correa et al.
(BAA) [DU. Pi and S
(all,.; v.,,. (isotype, BAA, fragment) [RE. Pi|. Neuquen:
Depto. Deseado. Patagonia oriental.-. .id
Depto. Huiliehes. Parque Nacional Ixinin. a lagoTromen.
4705'S.
393 1'S. 71 32'W. I.alnlle el al. 00 (BWl |BE. Pi and
W)12'W
Jan.
1905.
Dwtn
ru.-.n, i.r.,-.,,!,,, ;; ns's.... I2'\\. i:; Nov. i.;? (,<,

et al. 2590 (HAA) |I)H. Pi and Sl|: Depto. Rfo Chico,
2
i". I ' -. .1 I \\ <;, A \, .... '.-/ (B\\||DI I'i
ami St|. CHILE. Ml K.-gion: I ,ago Pinto, 5200'S,
22 i .,1 i ' i /. , i /. / i in isi\|-. in A
fragment) [IB, Pi].
i; ',,, 1,1 m , " II - <1 i< w \ , I'M /

<>; lB\Bl | SI I il
in I i
In I,. Ilennoso. en
las dunas mantimas, 3859'S, 6117'W, 8 Nov. 1940. /V
rorfj 73672 (holotvpe. I1W. SI) |SC. Pi), ftirorfi 7.3673
(BAA) |SC. St|. /'
- -
<i: I. |SC. Pi|- C4
i
,,-lla 14402 (BAA)
[Sc, Pi].
Poa tristigmatica
ARGENTINA. Chiihut: DeparUinienln Bio Sengiierr.
Pampa de Chalfa, Estancia La Media Luna. 47,3.VS.
7127'W, 3 Dec I<n:i. \illawil 223h iSI) |TB. Si|: I..,-,,
I ,i Plata. II ,1'S .1 iTW I/,.,.,-,../. A Hoggiano 15073
(BAA) | IB. Pi|; Depto. Tehuelches, Gobernador Costa a
Km I'M,,. H07'S. 705.V\Y. 14 Dee. 1972. hriaut a al.
3588 (SI) [TB. Pi]. Neuquen: Depto. Licar. Ccrro Chapel.-o. .-.. ,
I<M)9'S. 71 2(>'\\. 27, hi, \<>-\.<:m>
n at. 5<)2f> </'. boelckei Nicora, holotype, BAB) [BK. Pi],
Corn;, rial. 5928 ( B \ B) | BK. Pi |: (lord,',,, <l.-l (lerro (:l.apeleo. Porte/.uelo Trahunco, Faldeo S, 4009'S. 7120'W,
13 I'M,. I'lTJ*. (.
I!||BK.N|:< e,t( hapel
eo. I0()<)'s ,1 '
iP.\\l|P.K P | 2.. In I .. /s
'
'. ' |!\M BK.
M ' ' '
ti:
|l i - |
fcuc/* 599-3 (BAA)
[BK, l'i|. 12 |an L961 Led H
(BAA) [1
P,|: Deph,. \luias. Pa. del \1aeho. ,'U, 2CS. 7 [IIWl |TR. St|: l.a-una Wvarco Cam,,,,..
Cajon Beiiilez. ,,as Puerta Vieja. -V. 17'S. 7041'W. 1
Nov. V>7U.nrlrb-rtl. 11281 <B\ \||TB. Pi |: Cordillera
del Viento. cruzada de Trieao Malal al Cajon de Butalo.
.'if. 7,'S. 70M0'\\. 3 Nov. 19.,1. lioclcke et al. 11568
(RAP) | IK. N|: Cajon del PortiI ... 2..00 in. 3f> I2'S.
70"3<A\. -.1 I., i I -I ..
....
, ' -, ||TI,
Pi and Si|: Colllle,, ,:, \ i,-,.i o/ada de Trieao Malal
al Caj6n de Butalo. en vertiente, 3658'S, 7030'W, 3 Nov.
I
IIC St |: Depto.
,,,,,. ( |,al-. ,',7 19'S. 7106'W, 3 Feb. 1930, Hirschharn 23 (B\ \) | IB. Pi and St | Rio Negro: Depto. Na
huel llnapi. CerroCatedral,4105'S,7145'W. lei,. I97M,
/'.
I.. \ | I I, P /'
I M i | II
P,|. CHILE. Ml Region: Cordillera de Taleareguc. lei,
IB3I. C<i\ 19 (/! tnstigmatica V. De-v.. in Cav. svntvpe.
H\\ fragment) |TB. Pi].
I i I i,jih il I \l, , m) I Ins ,s , va.iablechaidctc.

within Poa sect. Dioicopoa, although there is a conspicuous discontinue between larye-si/.ed species
with sheath and leaf blade length, plant height. paniele length, and number oi nodes on principal panicle
axis. The highest value. 93 cm. was measured on P.
sponded to P. rigidifolia.
3. Sheath length (SHEle. em). The highest value found.
39 cm, corresponded to P. bergii and P. stuckertii,
P. rigidifolia.
4. Leaf blade length (BLAle, cm). The highest value
found, 61 cm, corresponded to P. dolichophyila, while
idi folia.
I i ul I in ili (II I
, in
baractei pri s, ills i
copoa into short-liguled species and long-liguled

ones. The longest ligule, 19.6 mm, was measured in
P. hergii: the shortest. 0.20 mm. in P. pedersemi.
" -
"'
'
'
"i
. Specie
Leaf blade apex (API). Navicular or obtuse (1); sharp
or acuminate (2). Poa sect. Dioicopoa is characterized
. Blade outline (OLTIi). Flat ( I): condiipli, ale i2>: eon

volute or subconvolute (3). Species of the P. dolichophyila comph
subconvolute blade, probably associated with the t
sence of bulliform cells; blades in other species v*
Loai ,1,duplicate to subconvolute.
Blade width, measured on the adavial epidermis I
Ivveen blade margin and midrib (BLAw. mm). Tl
10. Blade maximal thickness between abaxial and adaxial

epidermis layers (BLAt. mm). This character frequently correlates with stomata length. The maximum
imum value. 0.10 mm. in /; pilcomtnensis.
11. Bulliform cell development (BULc). Not to little difseel. Dioicopoa presents bulliform cell groups at both
tha is the only species that lacks bulliform cells.
while these are generally little differentiated in P. po-
Bounded to pointed cap. <
rgin (CAP).
out sclerenchyma e
Mdermis (1): crescen
abaxial MIX! adaxial epidermis (2) (terminology of

states a- ill Kill-. 1(>7(.|. Poa sect. Ihoicopoa gener-
5 cm). 'I'll. /'

., .', picrnK broad
panicles (5 ii mil. which arc usually expanded.
margin, seen in cross section. Tenninal sclerenchymaloiis caps are eomn Iv rounded lo pointed like in
P. rigidifolia, with species of the P. dolichoplnlla
complex presenting; a crescent-shaped cap.
. [Number oi vascular bundles with selerenclivnia girders on both adaxial and abaxial epidermis (SCI.2).
Nighr-l value, nere recorded in species of the P. doli, honlnlln complex (45). whereas minimum values of
only 1 or 2 were found in P. rigidifolia. P. ligu/aris.
This varies from 20 in (he P. dolichophylla complex,

P. bergii. P. bonariensi.s. P. ligularis. and P. indigesta.
to only 6 in P. alopecurus. P. pogoiianlha. and P. tig
idifolia.
2<>. Length of terminal. wcll-dcy eloped spikelet ol a
branch panicle (SPIIe. mm). Well-developed spikelels
were selected iron, the uppe. hall ol a panicle, particularly from terminal spikelets of a branch. Spikelet
length and correlated measures do no) usually \ar\
. Number of vascular bundles with a sclerenchvma
in P. pogonanlha (28 mm), although it is associated
commonly levy il or 2i in the P. dolichophylla complex. but are more numerous (5 to 8) in P. bergii.
. Number of vascular bundles with a sclerenchvma
girder only on adaxial epidermic iSCI.ad). Rare in
Poa sect. Duucopoa. they are often present (3 to 5)
in the P. dolichophylla complex.
were found in /'. bt-rgii and P. schi:antha (12 mini.

with the shortest among species of the /' dolicho
phyila complex (2.8 mm),
27. Width of terminal well-developed spikelet of a branch
panicle (SI'lw. mml. This character correlates with
flower numbi-i pel spikelet The broadest spikelet was
recorded in P. bergii (10 mm).
ig the bundles (SCLin)

species of Poa sect. I
vascular bundles corn
monlv present among species of Poa.
. Viviparous florets (KI.Ov). Absent {()): present (
Stomaia length (STOM. mm). This character, usually
indicative for different ploidy levels, presents three
opecurus, P. bergii, P. bonariemis. P. holciformis, P.
indigesla. P. laitiiffiiiosa. P. pogonanlha, and P. Irisphyila complex. wh<
18. Thickness of the Ion
0.033
Abaxial epidermal prickles (PRIC). Absent to infreerally fre(juenlly distributed on abaxial epidermis, al
complex, P. bergii, P. hubbardiana, P. lanigera, P.pilSilico-suberose cell pairs on intercostal epidermis
(SISU). Absent to infrequent (1); frequent to numerous (_'). Nlieo-siiberose paired cells are the usual
condition in Poa seel. Ihoicopoa, though they are infrequent in P. latngera ami P. pdcotna unsts
"""
v ii i v i: i i -^
Plant height, measured bom the longest culm of lettile planls (IIKIC. cm). Culms Usually exceed leaves.
' 7 are as long as
lex (136 cm); the
Nest plant, in P. rigidifolia (6 cm).
iberofculm nodes (CI I.Ml. Tins v,ic between
id 3 in small plants and 4 to 5 in taller plants.
icle length (PANIe. cm). The longest panicle (37
ichophylla; the shor
rigidifolia.
measured on widest panicle (PANw,
length and width. This character set varies among |

lillate and slaminale plants. The longest glumes w
observed on pistillate specimens of P. bergii (K
mm) and P. alopecurus (8.9 mm). The shortest glun
phyila (1.38 mm).
' margin ;i.l v. ininl. I'liis x a, ics I,,,,,, (.: mm in
dolichophylla and P. honariensis to 1.45 mm in
,ing the first glume s

^///commonly presents' '.'dimics ol em,' il"l.'nIlls' '
^
,|n
p |||(
Equal to I (0|: less than 1(1): more than 1 (2). The
second glume is generally shorter than the lower lemma '" !'" *<'<' Oioicopoa.
''-! Numb.-, of nerves o ||,c first glume (Cl.Un). Clumes
in Poa sect. Oioicopoa generally present a principal
Poa bergii features two ailililion.il marginal nci\es (in
total, 3 to 5, up to 7).
'iV Prickles
h. raclulla (RACH). Absent to infrequent
(0): frequent to numerous prickles (1). Poa sect. Dioicopoa generally [.resent these [trickles on rachilla and
within species of Poa s
rigid an.) short, less lli.m 1/2 of the llorel I

1 and long, more ih,in 1/2 of the lloivl (2): woo
less than 1/2 of the floret |3|: woollv a
P. n-sumlosa -<MII|>l-v 10.54 mm).

:W. I'al-a length iPU.Ie. mm). The shortest palca was r
corded on a staminate specimen of the P. resinuloi
imen of P. alopevurus (6.72 mm).
.-{<. I'-ilea widlli I .el,-., I, lim,.||'\l w. r ,ml !), iphi-
dimorphic characler between pistillate and staminate

florets. Pistillate florets usually have a hairy callus in
Poa sect. Dioiropoti. and pistillate florets of only P.
indigesta, P. huecu, and P. holciformis are completely
13. Hairiness aloof
anna nerves (II \ln
than 0.5 mm (3). Pistillate florets of Poa sect.

vojHui are characterized by the presence of hai
principal and marginal nerves that are 0.5 mm
or less. Poa bonariensis. /'. lanigcra. P. ligulai
lanuginosa. I' i,
gonantha, P. rigidifolia, and tristigm
mm long). The shortest lodieules were i
bonariensis and P. ligulans (0.25-0.33
. Lodicule width, including lobes (LODw.
0.2 mm and 0.7 mm wide, being raoi
* florets of P. ligularis and /
STUDIES IN ANNONACEAE
XXXVI. THE DUGUETIA
ALLIANCE: WHERE THE
WAYS PART1
ABSTRACT
Results of a cladistn
mil
i. [In I. nil .n
IN
il . i i
i n
'
tiflia ilharict I \ ruioti.it . a| ...rtt-tl elatles: a Fusaea clade. comprising Fusaea. Ihiekeauihus. b-lestudoxa.
and Fseudartabolns. and a Ihiûelia .IK) compn HI;' .ill \r,i r.sjii. :il ami Urican -petit-- ol ' l)uf>uetiu. Support lot
the past diMim I
. i
| , . I.
i i- i. - n- d lo it -.oh t it lalionsliips
between and within I
'
',.,..,,,
i Med thai the t iitical
reassessment of classical morphological characters, and the search for new ones. may well athanee phylogenetic resKey words:
AHIIOIUK
i i<
I idi-u
The classification of the \nnonai at

i hall. 1 ...
workers on this family with t
KnrU hi.-s.~iii. ilions ol tl lannh, a- in 1 lookei and
Thomson (1855). emphasize identification and only
incidentally reflect phylogerly. This also apt If- lo
a more recent classification (1 hii< hmsoti. I^dl).
However, at higher, tribal levels, these t wo classifications have little in coirmnon. To date., the classification by Fries (1959) resolves most s ihgl'olips
Exclusively on th has ol ml >
it.
ml lit I
characters, he distinguished two - iblamihes. ihn c
ngs. The composition ol many ol these genu-- groups has hern
amended afler phem-lit n ilvse- ill ...
mil Imit
morphology (van Heusden, 1992; van Setten &
Koek-Noorman, 1992; Koek-Noorman et al., 1997),
and phylogenetic anal
_,.,logical and palynoh

: '
I
I \ Le Thomas,
1994, 1996, 1997).
One o( Kties's genu groij)
\\i<-[)
I
liance, comprising West \I m md iropi I \inerican genera. The composition of this alliance remainetl untouched to date except tin the exclusion
of Malmea and the inclusion of the monotypic gei
: n s< th n c\ h >< k \ootm
t . tl I
l'>L>). t;|,a,,i, if,t l.aimesol lln genera belonging to this alliance include valvate sepals, imhncalf petals, .int
il ' in.
ml lilt presence of a
nidmi.-iil n\ .IMI. \1>-I tlis!ini inc tin the alliance
is the presence t:.| ps. ( Hlos\ nc.irpt .il- fniils. 'Hies,,
arc aggregalrs .- ishpilal. carp.d-. which heroine
fused with en. aiicllii i and/or adnatr lo the icccp
tacle. Genera usually considered to fit into the Duguetia alliance are the Neotropical genera Duck
,
1 , i / <
'! -pp.), and Fusaea (2
spp.l. logetht i with Irtrstudo.ui (.'i spp.), Pachypodanthium (4 spp.l. ami I'seudartabotrys (1 sp.) from
West Africa (van Setten & Koek-Noorman, 1992;
Le Thomas et al., 1994; Koek-Noorman et al.,
1997). Van Heusden (1992) dissentingly placed
Duguetia and Pachypodanthium in one informal
group, separate from Duckeanthus, Fusaea, Letestudoxa, and /
iplus Afroguatteria,
Enicosanthellum, and Disepalum) in another.
l'lm
th
n p it opinion on the circumscriplion oi
Ihiûa,
illianct -.-ems to prevail. Yet
closer examin.
".-, problems. Recent
clathslic analyses (Doyle & Le Thomas, 1994,
1995, 1996, 1997; Doyle et al., 2000) array Du' Ifsludoxa, Fusaea,
r Scientific Research (NWO; grant no. 805-40.201)

nch, Heidelberglaan 2, 3584 CS Utrecht, the Neth-
Avv Missot m BOT. GARD.
Pseudosyncarpy, which otherwise only occurs in

the Annona group, is an obvious synapomorphy for
this "Duguetia clade." During pseudosyncarpous
fruit development the postgenital aggregating of the
carpels can occur through two processes, viz. the
lateral fusion of carpel walls, and the inclusion of
the very basal parts of the carpels into the fruiting
receptacle. The former case has been extensively
documented for the genera Annona and Rollinia by
Briechle-Mack (1994). The fusion of carpels starts
with dovetailing of the epidermal cells of adjacent
carpels, and ends with complete fusion. The fruiting receptacle does not contribute to the aggregating of the fruit. A similar fruit development has
been described for Fusaea (Chatrou & He, 1999).
The inclusion of the very basal parts of the carpels
into the fruiting receptacle (see Svoma, 1998) originates from acropetal development of the receptacle
after flowering has been completed. This type of
aggregating of the fruit is present in all species of
Duguetia, whereas the degree of lateral fusion of
the carpels varies from completely free to completely fused among the species of this genus. Thus,
both origins of pseudosyncarpy occur within the
Duguetia alliance and can be traced when closely
inspecting fruit morphology. Pseudosyncarpy
should therefore be considered as a non-homolog< us similarity. However, the fruit type can be incorporated into analyses in a more straightforward
way by unravelling it ontogenetically (Patterson,
1982). In this analysis we will consider the differential origins of pseudosyncarpy, separating it into
two morphological characters (see Data and AnalA family-wide phenetic analysis based on flower
and fruit morphology resulted in inclusion of Duckeanthus, Letestudoxa, Pseudartabotrys, Fusaea, and
Pachypodanthium in one cluster (Koek-Noorman et
al., 1997). Duguetia appeared in another cluster,
together with Guatteria and the Annona group. Nevertheless, the overall similarity between all genera,
including Duguetia, was perceived so strongly by
the authors that the signal appearing from the
phenogram was ignored, and all genera were
grouped together in a tentative scheme of genus
groups. In the same paper, Koek-Noorman et al.
(1997) concluded that some of the principal characters used by Fries (1959) for the distinction of
genus groups, viz. sepal and petal aestivation, barely contribute to their phenetic clustering.
The following paradox thus emerges: a genus
group, or clade, has long been recognized intui-
tively but is weakly supported by morphological evidence. Schatz and Le Thomas (1993) stated that
confusing phylogenetic patterns based on macromorphological character distribution within Annonaceae have been clarified during the past two decades by new palynological and karyological
evidence. In spit* ol its VJ r .1 vali<lit>. lias si itr
ment cannot be applied to the Duguetia alliance.
Karyological evidence is too scattered to be unequivocal (Doyle & Le Thomas, 1996). Palynological data reveal too many autapomorphies among
the genera of this alliance to be illuminating. Based
wholly on palynological data, Walker (1971) even
erected the informal Fusaea subfamily, accommodating Fusaea and Duckeanthus, but placed Duguetia in another subfamily. Walker's data were reinterpreted by Le Thomas (1980-1981) and Le
Thomas et al. (1994). However, Le Thomas et al.
(1994) did not clarify the phylogeny of the Duguetia alliance with pollen ultrastructural data, but
conversely discussed the implications of their resulting phylogciiK B ! i if;, evolution of pollen morphology.
Doyle and Le Thomas (1996) stated that given
the high level of morphological homoplasy in Annonaceae, only molecular analysis might be able to
resolve higher-level relationships. The Duguetia al
liance was addressed by van Zuilen (1996) with her
listii analysis of trnh-F sequences, combined
Willi morphological rlianu-lcrs. favoring llic inclusion of Duguetia, Fusaea, Pachypodanthium, and
Pseudartabotrys as one clade. Duckeanthus and Le
testudoxa were not included in her analysis.
Except for most seed characters, many of the
morphological characters used in the above-men
tioned analyses still are conventional characters ir
a Friesian vein (e.g., Fries, 1934, 1959), whicl
ol el,j
Moreover, regarding the reticular
acter expression in Annonaceae, tl
el at which a phylogenetic analysis is performed
determines th< character choice. Contrasting with
a family-wide phylogenetic analysis, an analysis at
the tribal or genus group level requires different
data matrices informative only for the particular
group examined, as was elegantly shown by Johnson and Murray (1995) in their analysis of the tribe
Bocageeae.
In this paper we address the phylogeny of the
Duguetia alliance sensu Koek-Noorman et al.
(1997) and Le Thomas et al. (1994), by conducting
a cladistic analysis based on leaf, flower, fruit, and
seed characters, many of which have not been used
in cladistic analyses of Annonaceae before now. We
provide the rationale for the recent submersion of
Dii'-hcaiiilius >;u:ntlilUmis \\. K. I'V.

Duguetia argentea (R. E. Fr.) R. E. Fr.
Duguetia asterotricha (Diels) R. E. Fr.
Duguetia barteri (Benth.) Chatrou*
huii.i n onfinis (Engl. & Diels) Chatrou*
l)u^f!<(> >>'.,}
, i, u Oi 1!. |)< till
Duguetia furfuracea (A.St.-Hil.) Benth. & Hook.f.
Ditaurlia incDtiSfiii-iia Sagot
Duguetia lanceolata A. St.-Hil.
<l>"w
(Dugrib)
lD"uii|l
(Dugspi)
(Dugsta)
!ll:.,,,M,i>
(Fusion)
(Fusper)
(Letbel)
(l.etglal
Duîirlia r,,'!r:rl,s,s V >-|cg , M.,,1-, <K K .on

Duguetia riparia Huber
Dl u
,i nana Mart.
Ditûrlia s.'wntlii (Kngl X Dirls) I ihalmii :
Ditgurtia uiiiflnra (DC. ex Dunal) Mart.
Fusaea longifolia (Aubl.) Saff.
Letestudoxa bella Pellegr.
/< '< S/V./.-K.- .,'-,/ ' ., 1 1) 'l-.i J .K l!i i. -nr
imiginosa Le Thomas
Pseudartabotrys letestui Pellegr.
!>- 'I (nm.in '.i-iii; 0 = phloem an
}>>
')
10
curb In. homes; 0 = absent, 1 = present

inflorescence position: lciiiiin.il on short a
iiifloresi Cllt I ll
ill ol ' - I nl i |>
I-
|it dii el .IIIMI| i
! (i (I
i I
19style; 0 = t
20 -slyles coherent lis interlocking papillae; 0
i -".Icn'iH'Imn.i -.un-i-un.'i <.; > . I in ! ;!..
;.lil.-m an. /. < -
ary shoot; 0 = never, 1 = sometimes, 2 = always (ordered)
flowering receptacle; 0 = n
= yellow to orange, 2 = pi,
1 = subentirely connate.
nt
basal carpels fused with fruiting receptacle: 0 =
2.V
fruiting receptacle protruding between carpels; i

-direction of aril libers: 0
010000000120000000000110
020001000021020000000110
011001000020000101000110
010000000020000110000110
000110110121011020110001
000110110121011020110001
100100110011121120100011
100100100011?21?20100011
10010010001122192010????
100100000011101120101001
(Pselet)
22
21
123456789012345678901234
000000000000000000100001
000010200001001020110011
020001000020000000000110
010000000120020700001110
011001002120000101000110
011001002120000101000110
011001000020000101000110
020001000020200100000110
010000000020000101000110
020001000020200100000110
010000001010000000000110
(Ducgra)
(Dugarg)
(Dugast)
(Dugbar)
(Dugcon)
(Dugdil)
(Dugfur)
(Duginc)
(Dugkn)
iD.,u...-..i
toward distal end oi
Pachypodanthium into the synonymy of Duguetia

(Chatrou, 1998). Species formerly known as Pachypodanthium will hereafter be referred to as "African species of Duguetia." A biogeographical ques-
as well as for most Anm

Thomas, 1993).
tion comprises whether the break-up of West

5 event for this subgroup
The data matrix include:

acters (Table 1). All specit
DATA
AND
AIVMA SKS
/ -irstudoxa,
ed in the analw- (For vo
! presented for the first 1

!
, with the following
- sec Appendix 1.)
All 4 African species, and 11 Neotropical sp< i ies

of Duguetia are selected out of ca. 95 that constitute the genus. Annona sericea is included as outFirst.
for i
eluded in a clade that is directly linked to the
pseudosyncarpous clade on the basis of sequence
data (van Zuilen, 1996). Furthermore, of the genera
that appear close to the pseudosyncarps in van Zuilen's i aljrsis, Annona is the only genus with pseuis fruits
-illi seeds provided with a rudimentary aril. Therefore, the scoring

of characters 22-24 for the outgroup is enabled.
The character set has been designed to incorporate
i
'
'
morphological and anatomical data from different plant parts. It comprises 17
binary characters and 7 three-state chai
01
the latter charai
li.n ter 9 is quantitatively ordered, scoring for the relative abundance
of the particul.it i I . -.
;Miiion within a
In i h >ii 'I
i
- pertain to genera,
the characters are scored at the species level. This
allows the scoring of several characters with ituon
sistent character states within a genus. Characters
3, 6, 8, 9, 10, 11, 12, 13, 14, 16, and 18 are heterogeneous within a particular genus, while homogcnti.ii- uilhiti .rmlliri Du^'i'-ti.t | >.. M 11 i i
pie states for all of these characters except for
li in me charactei !, while one of the other, nongenera is scored uniformly. Scoring at
the species level also permits us to address the
question of the relationship between the Neotropir . s of Duguetia. Bootstrap values of a previous phylogenetic analysis of Duguetia
inspire little confidence in tin- chides found, nor in
most of the sections of Duguetia as recognized by
Fries (van Zuilen et al., 1995). Therefore, our
choice of the 11 species for our analysis is such
i
ii.ition within the
genus well. We decided to include Letestudoxa lanuginosa in the analysis, despite the fact that its
fruits are unknown, and therefore characters 21-24
could not he scored. Inclusion may possihlv allow
more insighl into the evolution of flower color (charai let 13). as L. lanuginosa has its flower color in
common with only two species of Duguetia (D.furfuracea and D. lanceolata). The missing values for
characters 21-24 do not present any problem for
the analysis, as they are simply treated as uninfor-
Chai
7: histology < the primary vein. JJetails hereon can be found in van Setten and KoekNoorman (1986). In their survey of leaf anatomy of
Annonaceae, Duckeanthus has not been taken into
account. We sectioned leaf parts of D. grandiflorus
according to the same methods as described in van
Setten and Koek-Noorman (1986). The histology of
the primary vein of Duckeanthus shows a pattern
that is hitherto unknown in Annonaceae. The phloem only abaxially accompanies the xylem (Fig. 1A).
This pattern is an autapomorphy of Duckeanthus,
and we scored it as a separate character state.
Character 8: curly trichomes. Curly trichomes
have been described for Fusaea (Chatrou & He,
1999) and Letestudoxa (Chatrou, 1998). In both
genera these trichomes occur on the lower side of
the leaves, on the petioles, and on the young twigs.
In Letestudoxa they occur on the outer side of the
calyx as well. Besides curly trichomes, normal
straighl trichomes occur as well in both genera.
Character 9: position of inflorescence. Two African species of Duguetia exclusively have terminal
inflorescences on reduced axillary leafy shoots. Le
Thomas (1969) described them as axillary for D.
barteri. Two Neotropical species of Duguetia (D.
neglecta and D. riberensis) exhibit the same position
of the inflorescence, though not in all cases. Hence,
the latter two species have been scored as 1. The
position of the inflorescences in other Duguetia
species is terminal on leafy twigs, and never on
reduced axillary leafy shoots.
Character 10: inflorescence, abnormal displacement of prophyll. This phenomenon has been described for inflorescences of Fusaea (Chatrou &
He, 1999), and is also present in four species of
Duguetia. Normally subsequent fertile prophylls alternate at angles of 180. In Fusaea, D. asterotricha, D. barteri, D. confinis, and D. riparia the | ro
phylls alternate at angles of ca. 90 only.
Character 11: shape of bracts. Cucullate bracts
have been documented for Fusaea by Chatrou and
He (1999), and have been found in all species of
Duguetia, except for D. neglecta, which ha 61
ceous bracts.
Character 17: sclerified stamens. Van Heusden
(1992) mentioned the occurrence of indurate (more
or less lignified) stamens in Duckeanthus, Fusaea,
Letestudoxa, and Pseudartabotrys. We made medial
cross sections for at least 10 stamens per species,
staining with Astra-blue and Safranin, to .heck for
were found: (1) srhreiichvma is either absent; or
Othei
i traders have hardly been documented, or
[/; ;': :il Sclerenchyma

H Phloem
ES3 Xylem
1'. I | Parenchyma
ifj,ui'<-
I), _/ .
- I. i
< .,'
-Il
,. r _ | ,1, ,
.n,
In,
I.
in,
....
. tlll< If mi
ii
^ . i
II 111- . I-
/ -
ll. II.
I IM
It. (
llljj r i[ilii
,ving direction of aril fibers. I). Directed Inward proximal end of seed: Fusaea longifolia. K. Directed Inward
Ml end of seed Ihif-i, >iu , ,////; -, il, bars: \C = 0.1 mm; D, E = 1 mm.
le, as well as on the outer side between the the3 (Fig. IB, C). Only Duguetia uniflora showed an
ermediate pattern, with sclerenchyma found only
1 20: styles. For Annonaceae,

Fusaea has
tinct ovaries, styles, .inc! sit
mas. Its transition between ovary and style is indicated by a constriction, and by differences in epidermal outgrowths, and in shape in transversi
section. The stigma can be discerned from the style
by differences in color and epidermal outgrowths
(Chatrou & He, 1999). The same pattern occurs in
Duckeanthus, Letestudoxa, and Pseudartabotrys. As
in Fusaea, the styles of Duckeanthus interlock by
means of papillae. In those species of Duguetia examined, a clear distinction can be seen between
the ovary and the apical part of the carpel, but
subsequent transitions are absent. Therefore a style
is considered to be absent in these genera, in spite
of their presumed presence according to van Heusden (1992) and Doyle and Le Thomas (1996).
Characters 22 and 23: fruit type. Among fruits
of different species of Duguetia, different degrees
of fusion of the ear; els i
it. However, in all species the fruiting receptacle protrudes between the
carpels by acropetal growth (Svoma, pers. comm.
1996). In fruits with a low degree of carpellary fusion this is very noticeable, especially when dried.
Here, the surface of the receptacle shows shallow
com-iivilirs in which the carpels are loosely positioned. Yet even in fruits with a high degree of carpellary fusion (e.g., Duguetia furfuracea, D. barteri)
the protrusion of the receptacle between the carpels
is discernible. Fruits of Duckeanthus and Letestudoxa have free, stipeless carpels, attached to the
in a functional syncarp (Schatz & Le Thomas,
1993) similar to those of Duguetia. An important
dif'feivnei between fruits >:' Duckranthii* ami /'
testudoxa on the one hand, and those of J .
on the other, is the position of the basal sterile carpels. In the latter genus, these basal carpels inseparably coalesce with the fruiting receptacle and
constitute a proximal collar on the fruiting receptacle. In Duckeanthus and Letestudoxa, the basal,
sterile carpels contribute to the function. I sj
and readily detach from the fruiting receptacle.
Character 24: direction of aril fibers. Arillate
seeds are found in all species of the Duguetia alliance. The aril is considered to be rudimentary
(van Setten & Koek-Noorman, 1992) as it covers
considerably smaller parts of the seed than seen in
species of the tribe Bocageeae. Among the Dugue-
liit alliance, the aril develops from the base of the

testa, distinguished from the other parts of the testa
In its closely packed, long parallel cells (Garwood,
1995). We found that these rudimentary arils further assort into two types. The first type has the
long, parallel cells directed toward the distal end
of the seed, while in the second type they are directed proximally (Fig. ID, E).
The data were analyzed using PAUP version
3.1.1 (Swofford, 1993). Heuristic searches for most
parsimonious trees were performed by random stepwise addition with 100 repetitions, the Tree-Bisection-Reconnection (TBR) branch swapping algorithm, and the MULPARS and STEEPEST
DESCENT options in effect. Only minimal trees
were retained, and zero-length branches were broken down with the COLLAPSE option. The use of
either the DELTRAN or the ACCTRAN optimization criterion produced identical tree topologies
Bootstrapping was performed with the TBR swapping algorithm, simple addition sequence, and 250
repetitions. The relative robustness of the clades
i
i (8 ssed additionally by performing a decay
analysis (Bremer, 1988; Donoghue et al., 1992) for
all clades of the strict consensus tree. Character
evolution was analyzed using MacClade 3.04 (Maddison & Maddison, 1992).
le island through
liffering from the
f branches (Madsistency index (CI) of 0.65 and a retention index
(RI) of 0.85 (Fig. 2). Bootstrap values are indicated
above the nodes for each clade of the consensus
tree that is maintained after bootstrap analysis.
Bootstrap values ^ 50 are given. Bootstrap values
> 70 are considered to be high. Our eons, osus tree
satisfactorily meets the conditions under which
bootstrap values > 70 correspond to a probability
of > 95% that the corresponding clade a curatel)
reflects the true phylogeny (Hillis & Bull, 1993).
Only the condition of internodal change of < 20%
is not fully met: the basal nodes with bootstrap values of 95 and 88 both have an internodal change
of 25% of the characters. Decay values are indicated below the nodes. We were unable to realize
a decav analysis m which trees of Ian < s2
Dugneg Amer.
Dugrib Amer.
52
d1
87
A,
Dugbar Afr.
Dugcon Afr.
Dugdil Afr.
Dugsta Afr.
Duguni Amer.
Ducgra Amer.
81
d2
I
d>2 I
88
d>2
77
d2
65
d2
Fusion Amer.
Fusper Amer.
Letbel
Afr.
Letgla
Afr.
Letlan
Afr.
Pselet
Afr.
Table 2.
clade
Syna|>nmoi|>liirs loi ihc combiiw <l Dugufiiu-I- 'usaea clade, and for the Duguetia clade ai hi the / n.Mir.i
in Table 1 is included in parentheses.
Duguetia clade
from this search exceeded the maximum number of

trees that PAUP can retain.
The high amount of synapomorphy, as expressed
by the high RI, the high bootstrap values, and the
highest decay values for (1) the clade formed by all
species of Duguetia (Duguetia lade),
clade formed by Duckeanthus, Fusaea, Letestudoxa,
and Pseudartabotrys (Fusaea clade), arouse high
confidence in these clades. These results disapprove placement of all six genera into one clade or
alliance (Doyle & Le Thomas, 1994, 1996; KoekNoorman et al., 1997; Le Thomas et al., 1994), and
support the distinction made among them by van
Heusden (1992). The inclusion of Afroguatteria,
Disepalum, and Enicosanthellum into the Fusaea
group by van Heusden (1992), however, is contradieted by strong evidence, both from general morphology as well as from molecular evidence (Doyle
& Le Thomas, 1994, 1996; Koek-Noorman et al.,
1997; Doyle et al., 2000).
African species of Duguetia form a relatively distinct clade with Duguetia riberensis within Duguetia. Continued recognition of Pachypodanthium
would have rendered Duguetia paraphyletic, and
consequently Pachypodanthium species recently
have been transferred to Duguetia (Chatrou, 1998).
In the past Pacini> .
, .-!..,,
..! ,.<!
to be different from Duguetia primarily on the basis
of wood anatomy and palynology. Vander Wyk and
Canright (1956) pointed out a difference in vessel
density, being low for Pachypodanthium and high
for Duguetia. Increased sampling has rendered the
argument untenable (Ter Welle, pers. comm. 1997).
Pollen grains of the African species of Duguetia
possess an extremely reduced exine consisting of
only spinules. Le Thomas et al. (1994) interpreted
these spinules as homologous with verrucae in the
Neotropical species, which also show varying exine
reductions. Both pollen and wood indicate that Duguetia, despite its uniform appearance and its presumable monophyly (van Zuilen, 1996), remains a
Fusaea clade
variable genus. Such is also demonstrated by our

data matrix, with by far the largest part of the homoplasy deriving from Duguetia. The type of trichomes (character 2), asymmetric leaves (character
3), inflorescence position (character 9), and position
the th
(cl Meter 18) represent features in
our data matrix for which the African species seem
anomalous. These aberrant character states are also
encountered in a small subset of the Neotropical
species of Duguetia. This reticulate nature of character expression, which was also found in a study
of Duguetia leaf anatomy (Bakker & Visser, 1994),
requires broader sampling of species; this is under
way in a forthcoming analysis of Duguetia (KoekNoorman & Maas, in prep.).
What are the character states that identify the
combined Duguetia-Fusaea clade, the Duguetia
clade, and the Fusaea clade? We traced all character states at the ingroup node, as well as at the
internal nodes basal to the Duguetia clade and the
Fusaea clade, respectively. The Duguetia-Fusaea
clade is only characterized by traits that appear
extensively within the Annonaceae, either by parallelism or by mosaic retention. Examples of these
features include attributes such as trees, simple trichomes, symmetric leaves, free or basally connate
sepals, and white to cream flower color. Thus, the
Duguetia-Fusaea clade is not characterized by any
synapomorphies (Table 2). The only character state
that comes close to being synapomorphic is cucullate bracts, present in all Duguetia (except D. neglecta) and in Fusaea. However, it is one step more
parsimoni >n~ I i mume parallel evolution in Duguetia (and a subsequent loss in D. neglecta) and
in Fusaea. The Duguetia clade and the Fusaea
clade are characterized by four and three synapomorphies, respectively (Table 2).
To resolve relationships within the Duguetia-Fusaea clade we added some characters to the matrix
that are novel, and which do not appear in the majority of other Annonaceae. This novelty does not
impU ill. change <il (Hit- cliat.K ter slate to aiiothei

character state, and consequently these i harai ters
,ir< liltn nil i. |i..|;ui/i- l>\ nliiroup comparison.
This affects inflorescence character 10, implying a
sympodial development of the inflorescence. The
lack of any fertile inflorescence bracts in the tribe
Bocageeae, and the presence of lower b
do not produce axillary buds in most Xylopia and
many Guatteria, illiMral. tin j .aneity of sympodially developing inflorescences in Annonaceae.
Character 20 for stylar papillae can only be scored
pels are provided with a styli I*
Lai
<
acters 22 and 23 require the presence of pseudosvncarpcii- ftuiK. uln.li onl-id-- '!. ui -ii| under
study are only present in Anonidium and in the
Annona group. Arillate character 24 can only be
scored for a small group of genera where the seeds
possess a rudimentary aril (van Setten & KoekNoorman, 1992).
Considering this, outgroup comparison is difficult to use to polarize the set of characters at hand.
Possible oiitgroup lava mav lie seleeled from previous phylogenetic analyses. Doyle and Le Thomas
(1994) found Toussaintia and the xylopi
nected basall) to the pseudosyncarps, all of them
together forming a monophyletic group. Van Zuilen
(1996), based on limited sampling, however, found
the Duguetia-Fusaea clade attached to a clade
comprising I'rnn
>hma, Monodora,
Annona, and Rollinia. All these genera suffer from
the comparative lack of the above-mentioned char
a( ters. The only exceptions are genera from the Annona group, win h I m
podially developing
mentary arils with the Duguetia alliance.
The character set as herein
i ed U
iblia
\e monophyly of the combined DuguetiaFusaea clade, and cannot yield a corroborated positioning of the clade within the Annonaceae, as
the selected characters obscure the choir. < i outgroup taxa. For the monophyly of the combined Du
guetia-Fusaea clade we rely on Doyle and Le
Thomas (1996) and Le Thomas et al. (1994).
Our study, as well as the cladistic analysis of the
tribe Bocageeae (Johnson & Murray, 1995), shows
that the search for new morphological characters
viih hul. _ ii tahu. can be illuminative for anal\ses al low laviiiimiif level 1'lie eon-Lined IhiÛClia-Fu.sacii clade (tin ""pseudoNynearps": s|. vs r.o
Considering the geographical distibution of the

taxa (Fig. 2), the | tti < is straightforward, deriving
from the break-up of Gondwana. Both the Duguetia
clade and the Fusaea clade apparently existed before this event. Within the Fusaea clade, closer
phylogenetic relationships correspond with geographical proximity. Fusaea and Duckeanthus
evolved as the Neotropical representatives, and Letestudoxa and Pseudartabotrys as the African ones.
We cannot address whether the biogeographic isolation of the African species of Duguetia corresponds with their constituting a separate clade
within Duguetia, or whether some of the African
species have closer sister-group relationships with
Neotropieal s|,e, ies \iialvses inel nlmg more species :>: tins g, mi whi< h will have to resolve this.
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I.
\ ,, ,.
; Neotropics. Bot. Jahrb. Syst. 108:

17-50.
&
. 1992. Fruits and seeds of Annonaceae. Mo pho'i ', iini i - -!_'. . in. I.i i I I u . . n
.
..I
.ten li
,i ...
|j,.s
in
\,
Poiiifi. l.'i |ir<>;>:ram *ii
paign, Illinois.
.1 i ,\ ' !:
!
' ii.ii. I
56. The anatomy
and relationships of the Annonaceae. Trop. Woods 104:
Walker. .
117: 1-
152.
leusden, E. C. H. van. 1992. Flowers of Annonaceae:
Mnrpholog,.
.,,. \\ I).
H,!,
lioth. Bot. 142: 1-101. E. Schweizerbart'sche Verlagsl.iieliliaiidlimg, Stuttgart.
202: 3-131.
:mlen. C. M. van. 1996. Patterns and Affinities in th.
Duguetia Alliance (Annonaceae). Molecular and Mor
phological Studies. Ph.D. Dissertation, Utrecht Univer
sity, Utrecht.
, J. Koek-Noorman & P. J. M. Maas. 1995. A
|)h\logenelic anaksis olI Duguetia (Annonaceae) ha.sei
PI. Syst. Evol. 194: 173-188.
[rmona sericea Dunal

FRENCH GUIANA. Saint-Maurice-Region de Saint
Laurent, Piste d\|. .
11256 (P, U, US). CI VAYA. East Berbice-Corentyne:
near Thompson's farm (Timehri). 31 Oct. 1981 (fl, fr),
Maas et al. 5932 (NY. U, WU). Upper Demerara-Berbice: vieinitv of Mabura Hill, trail from Mabura Hill-Linden road to Denier
I i. I . 2i
u I '
i .u
I.
Maas et al. 7144 (K, P, U, WU). SURINAM. Marowijne:
,de.,|, r,,id iica- Mongol ipoc. |(> June I9.,| 1(1 l.i.ck vf,|.
MM I , \l M/l I I \ Bob'var: Street
Alcabala Casa Blanca towards Isla Anacoco, 28 Julv 1981
(yfr), Aymard et al. 313 (MO).
II Vm;i/<nias I l(
i| .per Rio Negro, 9
Mar. 1944 (fr). Baldwin 3584 (S. I S): ( am ,n ,..> i r, ,
Rio Negro, 13 Oei
i
W/ III. K BB S.
I s,
,,
li | lt o
b o \
. O
llll
.1 II III. Il
.11
llha
Marajo). near Carapana, 18 Oct. 1987 (fl), Maas et al.

<>772 (NY. I). Maas et al. 6778 (NY. U): Ilha das Flores,
Rio Negro, 17 Feb. 1959 (fr), Rodrigues (S).
."
gentea (R. E. Fr.) R. E. Fr.
BR \/!l,. Amazonas: km 124 of Manaus-Porh. \clho
Hwy., 25 Mar. 1974 (fr). Campbell et al. P20915 (G,
INPA. I ): Carapa.K . . ,.;.. |{.o N.-r, . 17 Oct. P!7 ill).
Maas et al. 6764 |\).h. COLOMBI \. Amazonas-Vau|..:s:
in, \paporis. Jino Goje. between Bio I"n.;., .;,u
.pevaka. Cano Unguya. alt. 250 m, 3-11 Sep.
1952 111. frl. Curru, Harriga 14366 (COP. IS). YFNF/l PI.A. Amazonas: San Carlos de Rfo Negro. 21 Mar.17 Apr. 1981 (yfr). Delaseto C. el al. 9425 ,\ PM. Isla
alt. 120 m, 31 Jai
n
(MO. U. VEN).
Duguetia asterotricha (Diels) R. E. Fr.
BRAZIL. Ainazonas: km 118 of Manaus Caraearai
Hwy., Mar. 1976 (fl), D. CoSlho & Damiao 7<>7 (INPA):
Reserva Florestal Ducke, alt. 80 m. 16 Jan. 1990 (fr),
.
;,. A U
','
,'L'il ). ibidem. 18 Jan. 1990 (fl),
Cenm & \elson 09219 il ): Manaus. 2 km from lain
mazinho, 18 Nov. 1975 (fl), 0. P. Monteim I\1>\5:<5I8
lINPA): km 70 ol Ma.uu, Il DNII i I U\.. 31 May 1994
(fl). Webber 1477 (HUAM). PERU. Loreto: Mishmacu.
near lquitos, Oct.-Nov. 1929 (fl), Klug 86 (F. NY. US).
Duguetia barteri (Benth.) Chatrou
(
II
ICON
Cntre-Sud
I Ihe Nyong River.
40 km SE of Yaounde, all. 550 m. 9 \x.

l.-le, Jtil3 ;BB. K. :' \\ ',
1 Of. I
if.-). Ihr
Pit,,,,-al: riidil bank of One:,,
a CaMasok, alt. 350 r

I'M.-'.
M K. A ',., ., / > I \l!i.\ Of:

IUIHIO: Ipaâ. 10 km S ,.| Menken. M.iall l-Llll.l HI
Ivindo River, alt. 500 m, 27 Nov. 1971 (fr). HlaM llfi f
II Si: Ipassa. 10 kn h .... \1 ,- ,u I indo Rb er. alt. .100
in. I I Via.. I'-'.-.
Il
MCI R \ Undo:
Muluia Rn.i ll>.i|.
kn I.'. .!- II \1- l":l I .
Taylor 13 (FHO).
i _
.
Diels) Chatrou
CAMEROON. Centre-Sud: ca. 16 km from Kribi.
Kbulowa mad. liicmi plautal i- m. Kir k. F.ees! Res, i-.r,
3 Feb. 1969 (fr), 0: SV\ of I .amha.ene. near
Lake Ezanga, Conoco drilling site, alt. 20 m. 3 fob. 1001
(lit Mrl'hnsun /.",/'>. (M()| NAanga: III km on Maarah,
River, 7 Aug. M>'
,,/n ,/e PoZ/ 7360
(WAG) O-omie-Maritiu.e: Rabi. N of Shell camp. all.
50 m, 26 Nov. PXM (II. fr). \\,eritiga A- /w, \,-/. .M''^
(WAG).
ihiituclui ailaliens Chatmu A lb p< tin
GABON. Centre-Sud: forest reserve of Kienke Kribi,
Ebolowa km 16. . I in. PW.R <f>). />.,;/ /0/":l!R! I iitoral: l.ombe. Tissongo, 7 Aug. 1976 (fr). Mckev & Julian 194 (K). Ngouim ..,.
. \lomla In Vno. 5
km on - ilh.-r MCI.- ol Kcml.ch , i lau - alt aOO m. .'Ojr11
i. i
.
U
i MO. P. WAG).
i> -i I f I I ml, X Hook.f.
BOLIVIA. Santa Cruz: Prov. Velasco, Serrania de
Ho ii 1
0 m I . I!' 7 III. fr). Thomas et
al. 5578 (U). BRAZIL. Bahia: 15-20 km from \ndarai.
trito Federal: 20 km
i 111). /W;( A ,W
rizonte, alt. 700-1000 m, 26 A.
erstrom 5572 (NY, S, SP, TEX).
km E of turn-off for Mineiros, 1 Feb. 1986 (fl, fr), Andersson & Hagberg 1635 (GB, U). Mato Gross,,: Mun.
" lampo CI.II de. roai: lioni ( a- ipo Claude to 1,'r. I,. ,f 112
Job lO<. II |,| //..,<,'..,' A O, ."., ,J. '.r - I .
Minas Gerais: Sen i do I ,|.
eo. u km N of Gouveia
o. . .a,l u, I)
...
i. 12.".
i 0 Apr. 1973 (fl.fr).
W. R. Anderson et al. 8585 (F, MO, NY, RB. I . LIB. IS).
San Paul*.: fa/end, I loilambra. 3/> km \ ol Campi as.
alt (.HI- ,. 2.= Feb P>7<. (lb. Shrphi-n! A" Chbs I 12 It,
(K, MG, NY). PAIUCI \Y Amambav: i k.-i - .1 II la
, 25 r
19\
. F, G,
i Sagot
BRAZIL.^
.
Rio Araguari. ct
-/. 3/0.>V; (N^).
sin of Rio
LoMibeias. '', k::i up III.. Mapu.-na I i < "i>eii.i l'..i
teira,30Mav 197 1 il. l>22 id I (\ \. I |.
FRENCH GUIANA. Mt. Bellevue de I'Inini, alt. 7(H) m.
17 Aug. 1985 (fr), de Granville et al. 7580 (B. CAY. P. V).
all. 0 100 in. I \
F, K, LZ, MO, U, ULM, WU). SI HIWM. Nassau Mis..
ftfanmijneRiver,alt.430-520.,,. 31 Dee. pr.nin.cw

an & Lindeman 39044 (NY, S, U, US).
Dm
nlata A. St.-Hil.
BRAZIL. Minas Gerais: Ugoa Santa, 8 Mar. 1865 (fl.
fr). Warming s.n. (C. F. K. NV P. S|. Parana: Snips. 2<
5o Paulo: Mun.
I "'l !; -. IV|iua '.I
I :.,
i.-ill; Sta loll ol M< lil .11,1
I : ill! /</./ , al.
Vu, Arboretum, alt. 5(K) m, 22 S. \
8043 (LZ, U, UEC, ULM, WU).
i-lrda Sandw.
GUYANA. Base of Mt. Makarapan, near rapids of Makarapan Creek, 15 Sep. 1988 (fr), Maas et al. 7433 (B,
BBS, F, MO, NY, U, VEN. WIS); Mabu.a Mill Nature
Reserve, 25 Aug. 1990 (fl, fr), Polak et al. 28 (U); Labbakaora Creek. Ti-ei t.i.
I
| il River. 2() An?;.
I"3. (ff),Sandwith 1214 (G, K. NU SI KIN AM. \r,,i of
Ka .ali bo lam project, along road between km 2 < in I 311.
I S-p. 102,0(11.1,1 ImJeman, Crbrts-van Rijn et al. 59 (F,
K, NY, U).
1
tarensis Benth.
2d.lub I (,". i,',!. /,-../.., ,<,./ <
''/;,INP\.
\ii. bi;\
mares, 11 Sep. to 26 Oct. ]

.A,a/,,.// 'l!\l
K C, K. LF. MICH, MO, 1
Mirim. 13 Dee. 1000 (II). Du.-h- \H.7,I |BM. C. \K,I.
l.OI.OMRIV 11,-la: Nr:r:i =1 la Mae;ll, ,,.,. CahoCieno.
alt. 600 m, 12 Jan I n i i
,,
i
|COI
S. I S). ECl \DOR. Napo: I,, Jova ,le ls Saeh -.1' .,,,.,
1993 (
230 .
./ (MO). Gl VAN A. Kanuk
l(K)m, 13 Feb. 10
,
<,l,setal. 184 (K,
I . WIS). Mill Huam.co: I'aehhea. \\ ol Puerto Inea.
alt. 250-300 m, 14 Sep. 1982 (fr), Foster 8778 I Ml). I I
l.i.lclo: Pi.-, \1:., :;.: . I uo Morain. 0 ."> k'tl from : onlhl
ence with Rfo Nanay, alt. 100 m, 15 Nov. 1984 (fl, fr),
Maas et al. 6298 lAMAZ. K. I . ISM. W ISi I ,-avali:
I , , , boM P , ,11, , h, I,.,
Mm, , 2.0,,, 2 N
1984 (fl). Mam et al. 6180 (L. ISM). AF.M/l I I, \
" ' n E of San Fernando de Atabapo. N bank
.1 I!,,. O:io.'o. all 0, . 1 \1..:., :,, ,!,.)_ /.,,;,,,;,,.,, ,,/,
17183 (MO, U).
Ihiguetia tiherensis \risic. e\ Maas & Boon
\l Ml/.! I I \ \p.ue: Distr. San Fernando, mouth of
II I ".Mr. P'.-cti /i,,...,,-A l...;, .... - ;j."',\Hl. 1 .
Itol.Aar: I'ucilo O d /. San --l,. \p,. 100 I |ll|. \nsle
llll!. I \I-Ni Gmirii-o: margins of Rfo
Oriluco. 5 km . t i
,1
i
[
",il
V
Tamavo 5087 (HBG, VEN).
ftagn,
BOLIVIA.
Cachoeiras Tres S and Fortaleza, 3-16 km abo-.e n ntb.
lul
"(;: (il l-al
',.,/ al "I 2 lIM'A \1 I.
tmasonaai Reserva Forestal Duck.-, km 20 ol
Manaus-Itacoatiara Hwv., 12 Oct. 1995 (Il
Maas et al. 308 (INPA, U). Para: Belem, hYsrrxa Mo
cambo, 8 Nov. 1995 (fl, fr), Maas et al. 8360 i'!M'\ K.
17.. MG. MO. NY I .1 I.M. WIS). COLOMBIA. Caqnetfc
Oi ,
,.i,! i I I I
L.aio
20 No.
P'OI (' |
!)>,;,, .,- .,., .', i, rl
al. 1669A (U). FRENCH GUIANA. (Hap,., k biwr.

(.rand,- Roche. Mill (ialesoca. 3 I Jllb l'H.9jll Ol.i, u,
7:725 |C \Y P. I ). SI KIN AM. S of Juliana top, 13 km N
of Lucie River, alt. 350 m, 9 Aug. 1963 (II). Irwin / '
54639 (B, F, G, M, NY, P, US).
\ B.-ni
350 m, 14 S<
lacuma. SI ol San Borja. all.
i. !'!(
.
.
.
\l(i. NY, U). Ama-I <
I' '.,, . ', .,
Zmas: \lu, Sa Paul
..I KM, Solimoes. II Sep.-26 Oct. 1936 (II. In. A, /,/>
8102 I \. KM. F. G. K. LK. MICH. MO. NY. P. S. U).
COI.OMISI \. \,a,nnas: Om-Bva.la \i;ir;i. 2 hours N of
Felicia, n. ii Id.. \i ,
M
!7.|;. PC a')./:,,,,
(Mil). Ill \l>OB. Napo: 4 km N of Coca, alt. 250 m,
17, s-|,. l'>:;<, Hi, ,/,. ,. i u-,i. ./ ,MD i i ri I:I
Loreto: 7 km SW of Iquitos, 30 July 1972 (f "'
/572 (AAU. C. F. MO. N A. %A ). I cayali: Prov. Coronel
IWl.llo. Cinrlrn, Uexnndm. ca. 8 km W of Bosque von
ll,l...ldt. all. 27,0 ,. 2 Nov. 1984 (fl, fr), Maas et al.
6183 (MO. U. USM, WIS).
IhtfitirlHi staudtii (Engl. & Diels) Chatrou
i Wll BOO . I i||,,r:il: D. ,1.1 I i Bosorvo. J isson
go Slu.B \roa. Transect B. June 1976 (IV). Waterman ,<
M,k< ,',79 il i. CFYIB \l \FBICW REPUBLIC. Sangha Fconomique Prefecture. Nda' ... i :
,. :.
alt. 350 m. 1 Apr. 1988 (fr), Harris & Fay 416 (MO, P).
CONGO-BRAZZAVILLE. Sangha: W slope of Mt. Nal.cina. alt. (()()-9(M) in. 15 Nov. 1991 (fr). Thomas et al.
.'7,77 <M<. (. M10\ VVol.-u-Ni.ni: liii ,
!( I n,
932
,1.1 /. Testa 9\
(ISM. 1510 l\0 .
I IN
km N ..( Sassan. i
I | i.lou
20.1
vm III hi /.,
Il I Ii
..MB
Bong: Bong range. 15 Aug. 1962 (II. fr), Voorhoeve 1176
1! CI, ki MIIIIKI: \ir I. \U
1 '.II..,, J"'. |. . 1'.2
ill), \norhom- 891 (V\ \G>. NIGERIA. Calabar: Oban, 9
Mar. I>59 ill). Talbot 1494 (BM, Z).
Ih, ,. i, .unflora (DC. ex Dunal) Mart.
Bl.'\/ll. \maz
i>: Bin l.-.ina. 18 Nov. 1945 (fl),
Fries 21407 (F, IAN, K, NY, US); Igarape Taruma-Acu,
30 km N\\ ol M MI MI
F < 01
'
al J >2 (I . II.M) IJIM lima II'i
II n n MI In f Bin
llapera. 8 June 1989 (fr), Mori et al. 20424 (U). VENE/l II \. \mazon i' II
125 ,. 13 Julv 1942 (fr). IL Williams 15859 (A, F, G,
NY, RB, S, US, W).
Tasaea lo/ii:iii)!ia (Allhl.) Saff.
BOLIVIA. Beni: km 13 <>l Bibevalta-Cuayaramerin
road. 19 Nov. 1989 (fl). Daly et al. 6260 (MO. I ). BB \1 Dee. 1984 (fl). Mori ft al. 17100 (NY, U).
km 155 of Manaus-ltacoatiara Road, 16 Dec. 1974 (fr),
Gentry & Ramos 13345 (MO, U). Rondonia: V
Bio Ml, ll.lo MUM,
l,,
.11)
Kw ./,
/ ,
G. MK II. MO. NY. S. I ). Koraima: Serra da Lua, 21

Jan. I9>9||| lF). 1'ianeeetal. 9367 \\\. I (.COLOMBIA. Antioquia: Mun. Caucasia, road to Nechf, 14 km
from I .nueasia II
I
Boad. Hue.cuda I a ( .and
leria. all. 50 m. 21 Nm MO.
1250 [l[i)\.. MO. \V I i. Santander: Puerto Parra-Campo Capote. 10 Dec. |97<) 111. III. Rrntena \rnaf-a rt al.
2136 (COP. HH\): Yaiipcs: vioinih of Mini. 20 Mas
M>7(> Hi). /arurrlii 1607 (OOP. GIF K). FBENCII CI I
\NA. Pes Faux Claires, near Crique Tortue, alt. 200 m,
10 Feb. 1993 111). !/./</, rt al. 8066 (P). CFYAN \. Upper
iver, alt. 200 m, 2 Feb. 1991 , i

2313 ll I. PFBU. Loreto: Jenaro Herrera, HAP, Arboretum, alt. 120 m, 25 Oct. 1994 (fl buds. vfr). Chatmu n
al. 2 |\M-\Z. L. ISM. \\t ). \la.lre ile Dios: Marque
Naoional del Maiii'i. II O-l. 1986 (II buds) Faster rt al.
11824 (U).
u uma R. E. Fr.
I" \ ., P7-< it, . //...-/.... / :Lv. MO, ||,.. \\
Sira Mis.. 26 km v
I
Field station, alt. 260 m, 1 Id,
, i
I i. di 2
.0 m. 2 i On I99| (s(,).
Rainer 244 (U, WU). Loreto: Rfo Napo, Sucusari. Fxi..i|
u.p. all I 10 m. 3 Nm MX) | (II Buds. IV).
Chatrou et al. 7 (AMAZ, NY, U, USM, WU); Andoas. H,o
Pastaza near Ecuador border, 15 Aug. 1980 (II. In. 6,.,/n
il MO
i
I
Naiila voad. 12
Dec. 1988 (fl, fr), Vdsquez & Jaramillo 11378 (M0, U.
USM).
- ua\
bella Pellegr.
.Ml BOON , MI.,-S...I:
. ,m \alley, 25 km E
ol eoni'iuenl of Vein B \i v an I
\kum linn.
Mi
;u
I'J: >lo
wa, 5 Mar. 1970 (Il

IB P G\BO\
: 70
30 ,
(.-I.
VGl: 12 km SI ol
Umbarene, 3 Oct. 1968 (III. Bretelet 5805 (WAG).
Ngounie: Moucongo, 19 Oct. 1926 (Hi. /, /,-,/;, n 1 .7.
iBI
Ouooiie-\1nriiiiiM :
.2.'.-. ,.
' II |.'! (II)
,',J|\\\(,|. Bal.i.
U ....... A
\., /., J--i7i\V\..i.
I 11 on & Repetur
GABON. Woleu-Ntem: ca. 10 km on T( hinibele-Assok road. alt. 630 m, 14 Sep. 1994 (fl buds). Hreteler
I
it., le. on lake border near dam,
1
lal \P.
H> kr
I
..II
I. h.i. -.. ,
!'.
79;|\\\(,);l ,-i.
K.n .,.! i..ad. all. 570 in.
24 Jan. 1983 (fr), de Wilde 198 (WAG).

ant^m
I
Wolru NI.M,
n p.;; ||,. IA.
i I;. M0 B. Oyem. 7 Max 193 1 II). /, Testa
9570 (P).
Pseudartabotrys letestui Pellegr.
f,\BON. Kstua.K
I
: ul MI vesevveWonga-Wongue, ca. 100 km S of Fibrin ill.-, all. 100 m. 3 Mar.
M'."-. : .' il -..' ". /:' i\\ V.: Of-., --Mai-iliiiie:
Bal.i-Kou.iga. E of Rabi, 29 Oct. 1991 (fl), Breteler &
lanuLlal l(/2i! l\\ \Gl. II. II i.'Cl. SILCII Hi C iiM.M 7camp, 24 Nov. 19'
,1 V
iBBi: Babi
1.5 km along pipeline to Echira, alt. 40 m. 24 Nov. Vm
r), Wiermga & u
T3 (* iG); 22 km along a
t
Had I
in \ d
.
mil n Ion Mt- ill
150 m, 3 Dec. 1986 (fl), de Wilde et al. 9136 (P, WAG);
I i
v , III. al,.,,. |
i ,
n, ill 8,0 m 22
Jan. 1993 ill. fr). de Wilde & ran der Maesen 10888
(WAG).
Koch and Ihsan A. Al-Shehbaz*
MOLECULAR SYSTEMATICS
OF THE CHINESE YINSHANIA
(BRASSICACEAE): EVIDENCE
FROM PLASTID AND
NUCLEAR ITS DNA
SEQUENCE DATA1
\IMI:
\<:r
Sp. ( H s dl lh, ( Inn

associated with ( <>< h
n | In I I II.
-
n I ii
'i
ill i
i
II
Ii
i lh
i pi
i I .
n ,
n
.
Ilin I
,
i
Ill, ,.,! m ,n , lost |\

hlmim ami detailed
II lm>! mi llu authoritv
pii'sriit plnlogenetie slntb is based on the analysis of the ITS (internal transcribed spacer regions of the nuclear
nlioM.in.il D\ \ in.: lii
I I i | I
I in i i
|
n >
I
ill i ,1 !
.MI, , ompaii-il. ami
i
.1
'
i
i.Ki However, incongruencies when nil>\
I
'in between these two
lineages. We followed .1 concept lo combine .ill lava ol I'M
i . : m- , NIIIKI. Our results from
phvlogenetn .in.ib-.i-. it . i md . pi >\ \ u| | till
... . n .. I,; h
nil.
' ,
il Ho-ippn father than
> lb ' , /"''..;
- ^ - -IIMC-I! .1 I \ II. ill. ..II pi. .i >iis .,i,l- inKeywords: Brassieae-a
, '
II ul
,
i l
.ohilinn )intmm.
Many authors follow Schulz (1936) and SchultzeMotel (1986) in dividing Cochlearia into the seci us/'.\
'<>'",< n , l!i tdaucocochleriaO.
E. Schulz, Cochlearia (= Eucochlearia Prantl), and
Hilliella 0. E. Schulz. As shown by Koch et al.
(1999a), however, this secti t
highly artificial. Section Cochlearia is widely distributed in Europe and the circumpolar region,
whereas section Glaucocochlearia, which was
raised to the generic rank by Pobedimova (1968),
i- restricted lo southwestern Europe. The lalh : section consists of C. glastifolia L. and C. megalosperma (Maire) Vogt, as well as C. aragonensi* (loste
& Soulie\ which was only recently included (Koch
et al., 1996), although considered to be distantly
related to the other two species (Koch et al.,
L999a). Section Cochlearia consists of a species
complex that demonstrates hij
aptation and geographic distribut
ell differences bclwecfl pin logcitcticalh sister la\.l
are often weak and poorly defined (Koch et al.,
1996). Both sections Cochlearia and Glaucocochli-nriii are losek related to llie genus loU'tpsidntin
Rchb. (Koch et al., 1999a). Section Pseudosempervivum, which is centered in the Middle East and
clearlv uiirelalcl lo (orhlcai hi, is most rlosek related to Masmenia F. K. Mey. and Noccaea Moench
(Koch et al., 1999a), both of which were segregated
by Meyer (1973, 1979, 1991) from Thlaspi L. s.l.
The family of Brassicaceae is divided into several tribes and subtribes. Most of them are highly
attili. ial. such as tribe Arabideae (Koch et al.,
1999b) or Lepidieae (Zunk et al., 1996). Following
classical tribal concepts. Cochlrotid sect. Pseud,>
sempervivum, sect. Cochlearia, and sect Glaucocochlearia are members of tribe Lepidieae. Species
originally assigned by Schulz (1923) to section Hil
" id I a, and Cochleariella) were

excluded from Cochlearia by Pobedimova (1970),
who did not assign them to any genus. However,
these species have recently been placed in three
Chinese eiideuiii genera. Yinshanm Y (!. Ma ci V
Z. Zhao, Cochleariella Y. H. Zhang & Vogt, and
Hilliella (0. E. Schulz) Y. H. Zhang, each of which
was assigned lo a differenl suhtrihe The genus )in
shania (Ma & Zhao, 1979) was placed in subtribe
ioi providing sonic of the samples. The cniali

\ PE, TAI, Tl, TNS. US, W. and WU are thank*
; \gricullural Science. Gregor-Mendel-Slr. 33. A
Box 299, St. Louis, Missouri 63166-02 W. IS. A
. 87: 246-272. 2000.
. B, BM,
I \ST.
Descurainiinae, tribe Sisymbrieae. The genus

Cochleariopsis (Zhang, 1985), renamed as Cochleariella (Zhang & Cai, 1989), was placed in subtribe Cochleariinae, tribe Lepidieae, along with Hilliella s. str. (Zhang, 1986). Although a few studies
on taxonomy, evolution, and origin of these genera
(Zhang, 1987; Zhang & Xu, 1990; Zhang, 1993)
have been made, nothing was said about their sysand European taxa of Cochlearia. Zhang's (1987)
li isioii A Yin.shiinin (excluding Hilliella) into two
sections and two series and Zhao's (1992) classification of Yinshania (including Hilliella) into two
sections and six series, were shown by Al-Shehbaz
et al. (1998) to be highly artificial. In fact, one of
the species assigned by Zhang (1987) to Hilliella
and by Zhao (1992) to Yinshania was placed by AlShehbaz and Yang (1998) in the synonymy of Cardamine fragariifolia 0. E. Schulz.
On the basis of a comprehensive morphol >gi<
survey of Yinshania, Hilliella, and Cochleariella,
Al-Shehbaz et al. (1998) reduced the latter two to
synonymy of Yinshania, and concluded that there
subdivisions that do not
reflect the phylogenetic
genus of 13 species.
They also demonstrated that morphological characters previously used in the delimitation of species
(e.g., density of papillae on the fruit valves, fruit
shape, and seed number per fruit) are highly variable among and within different populations of the
same species. Furthermore, differences in the comprrssion ol trinl (len-li vs. latiseptalr ur anûstiseptate) that were emphasized heavily by earlier
authors (e.g., Schulz, 1936) in the delineation of
genera were not found to be taxonomie.di
ISI ful
in the Yinshania complex. As shown by Koch et al.
(1999a), the placement of heavy emphasis on fruit
compression has led to the artificial integration of
several taxa into Cochlearia sect. Pseudosempervivum instead of Thlaspi s.l. In fact, terete and var-
fruit morphology is taxonomically insignificant.

Morphological convergence and parallelism are
widespread in the Brassicaceae (Dvorak, 1971;
Meyer, 1973; Avetesian, 1983; Endress, 1992), and
the dependence on such characters to construct
phylogenies often leads to erroneous conclusions
(Sytsma, 1990; Meyer, 1991). Recent molecular
analyses (e.g., Warwick et al., 1992; Price et al.,
1994; Mummenhoff & Koch, 1994; Zunk et al.,
1996; Mummenhoff et al., 1997; Koch et al., 1998a,
b; Koch et al., 1999a, b) have i
setter understanding of the classifidelimitation, and phylogenetic rethe Brassicaceae. A preliminary

study (Koch et al., 1999a) utilizing ITS nrDNA and
cp trnL intron sequence data of four species oi the
Yinshania complex (including Hilliella and Cochleariella) clearly showed that the complex is linn
lated to Cochlearia. In this analysis it has been
shown that ITS and trnL intron sequence data provide sufficient sequence variation to distinguish
significantly between Yinshania and Cochleariella/
Hilliella accessions with both data sets. In order to
gain a better insight of the phylogenetir relal n
ships within this Chinese complex, we examined
sequence variation of the internal spacer regions
(ITS1 and ITS2) of nrDNA (Baldwin et al., 1995;
Campbell et al., 1995) and of the cp trnL intron
(Bohle et al., 1994; Gielly & Taberlet, 1994; van
Ham et al., 1994; Koch et al., 1999a), and compared the derived moleculai phylogei
oncepts based on morpholog
This approach provided us with the opportunity to
characterize species lineages and to anal) n w ion
gruencies between different data sets in order to
test hypotheses of gene flow over lineages and chloroplast capture.
Leaf material for DNA extraction was obtained

from herbarium specimens (Table I), mosl which
were provided and determined by Zhang Yu-hua
(Institute of Materia Medica, Zhejiang Academy of
Medicine, Hangzhou, People's Republic ol China I.
We did not examine vouchers to verify Zhang's deienninations. The samples represent a broad sp< <trum of species of Yinshania, Hilliella, and Cochleariella. Cardamine flexuosa With, and Rorippa
palustris (L.) Besser served as the outgroups. The
DNA sequences for the outgroups were obtained
from Franzke et al. (1998).
The total DNA for the outgroups was isolated

from leaf tissues following the CTAB (cethyltriammoniumbromide) method of Doyle and Doyle
(1987), as modified by Mummenhoff and Koch
(1994). DNA extraction from herbarium material
was performed in a mini preparation in Eppendorf
K action lubes trom .'(..._, dried tissue. Tissue was
ground with sand and prewarmed 2X CTAB-buffer.
illi111 I! 1111II i till!
jsli
i j i i I, .IHIiS.ii
- ! 11!, If H ia
Mill
ft i i s
Ill ]1M H !! 1 111! 5
EMI! Ill Wii!!
i III 111HIII i i! I
iIII!HI
Hi lit
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11
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IS!
IIII
:=:
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111
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ja
>-
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I | t*t*|8|84 lit]
i and DNA isolation from herbarium specimens followed Koch et al. (1996).
Double-stranded DNA of the complete ITS region, in. hiding the 5.8S rDNA gene, was amplified
by 30 cycles of s mn tri P< 1! using ITS primers
initially designed by White et al. (1990) and modified by Mummenhoff et al. (1997). The 18F primer
(5'-GGAAGGAGAAGTCGTAACAAGG-3') is located at the 3'-end of the 18S rDNA gene, and
primer 25R (5'-TCCTCCGCTTATTGATATGC-3')
is located at the 5'-end of the 25S rDNA. It has
been reported that PCR selection of rDNA paralogues has occurred (Buckler et al., 1997). However, PCR selection might have only been important in high G+C content sequences (Buckler et
al., 1997). Sequ<
s from }innd // - /
(Koch et al., 1999a) are comparable in G+C content to sequenc < . <
hi. h l'<|,'
selection was probably weak (Wendel et al., 1995a).
The resulting amplification product included ITSI.
5.8S rDNA, and ITS2. Only those PCR products
were cloned into the pGEM-T-Easy cloning
(PROMEGA) that showed a single band on ethidium bromide stained agarose gels. Two cloned ITS
regions from two independent PCR
sequenced (forward and reverse) with both amplification primers and I wo universal primers located
in the flanking sites of the pGEM-T-Easy vector (t7forward: 5'-gtaacgatttaggtgacactatcg-3, ml3-reverse: 5'-agcggal i i
ltd i i _.a-3). This means
that every single clone was sequenced four times
to avoid sequence errors. The trnL (I'AAl uiiron
sal primer B49318 (5'-CGAAATCGGTAGACGCTACG-3') located at the 3'-end of the tmL(UAA)5'exon and A49855 (5'-GGGGATAGAGGGACTTGAAC-3') located at the 5'-end of the tmL(UAA)3'exon (Taberlet et al., 1991). The PCR profile used
to amplify the trnL intron followed the following
profile: hot start with 5 min. at 94C, and 35 cycles
of amplification (1 min. 94C, 45 min. 50C, 45
min. 72C), final elongation step for 10 min. 72C,
and storage at 4C. DNAs were cycle-sequenced
using the Taq DyeDeoxy Terminator Cycle Sequencing Kit (ABI Applied Biosystems, Inc.). Products of the cycle sequencing reactions were run on
an ABI 377XL automated sequencer (ABI Applied
Biosystems, Inc.). Material from accession numbers
22-26 (Table 1) was only used for
trnL intron sequence, becau
ITS regions failed totally.
lo ihose of Sim/pis. niba I.. lHalligebi i & Capesius.

1989) and other Brassicaceae (Mummenhoff et al.,
1997; Koch et al., 1999a). DNA sequences were
aligned by hand. Parsimony analyses were performed with unordered Fitch parsimony and
weighted parsimony with a transition :transv< rei m
weighting of 1.0:1.08 using PAUP version 3.1
(Swofford, 1993). The BRANCH-AND-BOUND algorithm was used to find maximally parsimonious
trees. Bootstrap analysis (Felsenstein, 1985) was
performed using 1000 replicates and the HEURISTIC search algorithm with the MULPARS option.
We combined the GAPMODE = MISSING option
iln ilii en in >f tin aps is t<I hilonal presence/
absence characters (Downie & Katz-Downie, 1996).
iii'
ecreases the number of equally parsimonious trees because of the redundancy resulting from having two sets of scored characters for
the same indel events |tyn|circhowski el al., 1993).
that produce a more general graph that indicates

different possible phylogenies are useful (Huson,
1998). One such method is the Split Decomposition
introduced by Bandelt and Dress (1992) and its
variations. In order to visualize conflicting phylo.. ii.
-:mials, we analyzed all ingroup ITS sequences (see Fig. 6), using the software program
SphtsTree version 1.0.3. (Huson & Wetzel, 1995
shareware ftp://ftp.uni-bielefeld.de/pub/math/splits/).
trnL intron data. DNA sequences were aligned
by hand. Parsimony analysis was performed with
PAUP (version 3.1; for options, see ITS data). Gaps
were treated as additional unweighted binary charaelers. Thesi âps were coded usiiii; sirii I ritena:
gaps must occur at the same position and have the
same aligned length to be treated as homologous,
and no splitting of one gap in two or more characters was performed (Koch et al., 1999a). Bootstrap analysis was performed as described above.
derived an ITS phylogeny with sequences from

Capsella rubella Reut. (Koch et al., 1999b), Arabidopsis thaliana (L.) Heynh. (GenBank U43224),
Yinshania acutangula (0. E. Schulz) Y. H. Zhang,
Htulmmi vulgaris R. Br. (EMBO X98632). Canto

mine flexuosa With. (Franzke et al., 1998), Thlaspi
arvense L. (Koch et al., 1999a), Cochlearia aestuaria (Lloyd) Heywood (Koch et al., 1999a), Brassica
oleracea L. (GenBank AF039994/AF040038), and
Sinapis alba (EMBO X66325). DNA sequences
were aligned by hand, and the alignment is shown
in Figure 4. Alignment positions 109-160 were removed from subsequent analysis. Parsimony
yses were performed with unordered Fitch parsimony using PAUP version 3.1 (Swofford, 1993).
The BRANCH-AND-BOUND algorithm was used
to find maximally parsimonious trees with the GAPMODE =NEWSTATE option. Bootstrap anal
(Felsenstein, 1985) was performed using 1000
licates and the HEURISTIC search algorithm
ployed with the MULPARS option. A decay analysis (Bremer, 1988) was performed in addition
the bootstrap approach, in order to assess the c(
tlili-Iirc tll.ll could he placed 111 tile moi,oph\l\
eludes. Deca\ indices (HI) were estimated according to Baum et al. (1994).
Hi>i i.is
The total length of the alignment with accession

numbers 1-21 and outgroups Cardamine flexuosa
and Rorippa palustris is 464 bp, with 283 and 181
nucleotides in ITS1 and ITS2 spacer regions, re ii- ly. The alignment required 36 (7.8%) gap
positions, including the outgroups, and is shown in
Figure 1. Sequence data were submitted to GenBank with accession numbers AF100793AF100852 (Table 1). One third of these gaps is
located between positions 117 and 133 in the ITS1.
This region was completely excluded from subsequent analysis. Additionally, we excluded n icleotide position 465-467 and 473-484 from subsequent data analysis because of an ambiguous
alignment (Fig. 1). Gaps from nucleotide positi< 11-14 and 293-294 were treated as one single gap,
respectively. The number of introduced gaps is
comparable to a phylogeneti
I s.l. with 4.8% of the sites (Mummenhoff et al,
1997). In Krigia and outgroups, Kim and Jansen
(1994) had to introduce gaps in 3.9% of the sites.
Total lengths of ITS1 and ITS2 are nearly identical
(Hilliella alatipes (Hand.'-Mazz.) Y. H. Zhang & H.
W. Li var. micron , i H Zhang |
) .
rinilnrum (Dunn) Al-Shehbaz et al.], accession no.
10) and 457 bp (Cardamine flexuosa and Rorippa
palustris).
l'hvlngenctie analysis using hitch parsimony, in-
cluding the additional 0/1 matrix for the gap posi

tion, resulted in 24 most parsimonious trees (MPTs)
with a length of 538 and a consistency index (CI)
of 71.4% (66.9% if autapomorphies are excluded).
Of the 264 variable nucleotide positions, 166 informative positions were in the ITS1 region (including 48 autapomorphies) and 98 in the ITS2
I
us. J i
p"
i liii *>). Four out of
36 gap positions
ihin IK <>ki sequence alignment are unique to a particular sequence (Rorippa
palustris 2 gaps, ace. no. 3, and ace. no. 14). A
the MPTs revealed a ratio of 1.00:1.08. Therefore,
we used a weighted parsimony approach with a
transversion), which resulted in one MPT that is
i i
21 \llTs from the Fitch
parsimonj with a consistency index of 67.7% (CI
57.9% if autapomorphies were excluded). We present the MPT from the weight)
rail
inch length (Fig.
2). Bootstrap values are provided from 1000 replicates using the weighted parsimony approach. For
most taxa we identified only one ITS sequent < type
u.lhu a -.ingl. -u'. im.-n 1 . u //,//,'. /'./ !,, h <!,m, *! Y. H. Zhang (ace. no. 13), Cochleariella zhejiangemis (Y. H. Zhang) Y. H. Zhang & R. Vogt (ace.
no. 21), Yinshanio
no. 5), Y. henryi
(Oliv.) Y. H. Zhang (ace. no. 7), and Y. furcatopilosa
(K. C. Kuan) Y H. Zhang (ace. no. 8), we found
two very similar ITS sequences among the two
clones sequenced. In the case of accession numbers 13, 5, 7, and 8, ITS1 and ITS2 regions differed
by only
:!,',M/;,ge'<^ Afr. I,.. 21'. til. two IT^ t\p. *. Item
the same individual differed by 15 mutations,
which might indicate that two different ITS loci
were cloned and sequenced. Both sequences clustered within the sunn < lad. . It: Ifilln l!<; /nm>in<>:
des (Dunn) Y. H. Zhang & H. W Li (ace. no. 17),
we detected two ITS sequences from a single individual that clustered m dlllerenl eludes ( Klgs. 2.
6). Both sequences differed by 76 mutations. The
ITS In clearly support a separation of two chides
consisting of Yinshania sensu Zhang (1987) and
ochleariella. Different accessions from
one taxon (sensu Al-Shehbaz et al., 1998, refer to
li< 2) grouped it itl.K nt positions in the case of
i
' : . -.
i< e. no. 20. not i lated to ace. nos.
18, 19, 21).
Using the taxonomic concept of Al-Shehbaz et
al. (1998) and merging Hilliella changhuaensis Y.
H. Zhang, H. guangdongensis Y. H. Zhang, and //.
lichuanensis (ace. nos. 11, 12, 13, respectively) into
//, lu-!i)i<uif"i,si>. oni\ a. eessiriii number- '. 1 and M
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grouped together by ITS d;

12 (H. guangdongensis) is unrelated to these accessions based on ITS data. Similarly, H. warburgi
(0. E. Schulz) Y. H. Zhang & H. W. Li (ace. nos
18, 19), Cochleariella zhejiangensis (ace. nos. 20
21), and H. fumarioides (ace. no. 17) merge into Y
fumarioides (Dunn) Y. Z. Zhao, as proposed by AlShehbaz et al. (1998). ITS sequences from K fumarioides sensu Al-Shehbaz et al. (1998) are found
in three different positions among the Hilliellal
Cochleariella clade (Fig. 2).
bers AF100853 through AF100881 (Table 1). The

lengths of trnL intron sequences range from 311 bp
in Hillit "<i rirulorum to 514 bp in Cardamine flexuosa. Of the 38 variable nucleotide positions in the
alignment, 12 sites are autapomorphic. In addition,
one of the seven gaps is autapomorphic. Phylogenetic analysis resulted in two MPTs with a length
of 53 steps and a consistency index of 92.5%
(90.0% if autapomorphies were excluded). One
most parsimonious tree is shown to demonstrate relbe generated easily by drawing branches that are
indicated in Figure 2 by heavy bars with zero
length. Bootstrap values are given from 1000 repDiscrimination of a Yinshania clade from a Cochleariella/Hilliella clade is not as obvious with trnL
intron data as compared to ITS sequence data (Fig.
2). In the trnL tree the branch setting of the Yinshania clade as a sister group to the Hilliellal Cochleariella clade is not highly supported, and bootstrap value for this branching point is less than
50% (Fig. 2). Removing additional gap characters
from the matrix parsimony analysis resulted in one
MPT with the Yinshania clade as a sister group to
H. hunanensis (ace. no. 16), H. guandongensis (ace.
Figure 2.
Comparison
enumeration in bi i \
>f tin
ITS-cjrriv
<l'.l<
no. 12), C. zhejiangensis (ace. no. 20), and H. alatipes var. micrantha (ace. no. 10). Remaining Hilliellal Cochleariella taxa appeared in this analysis
for trnL data excluding gap information as a sister
group to these two clades. Nonetheless, integration
of Yinshania qianningensis Y. H. Zhang into the
Hilliellal Cochleariella clade is significant for trnL
data, in contrast to its segregation by ITS. Estimation of decay indices (DI) using the trnL intron
matrix without gap information revealed a high value, DI = 3 + , for the branch setting of the Yinshania clade. Different accessions of C. zhejiangensis (ace. nos. 20, 21) did not group closely together;
this has also been documented for the ITS data
(Figs. 2, 6). Hilliella changhuaensis, H. guangdongensis, and H. lichuanensis do not group together
in the cpDNA-based tree as proposed by the morphology-based concept combining them in H. lichuanensis (Al-Shehbaz et al., 1998); the same discordance holds for H. warburgii, C. zhejiangensis,
and H. fumarioides. Based on the trnL sequence
data, they are not combined in one single clade that
could be named as H. fumarioides as proposed in
the revison of Al-Shehbaz et al. (1998).
Both phylogenetic trees (ITS vs. trnL data) from

Figure 2 show some congruencies (all following arguments are also true when comparing the strict
consensus trees from Fitch parsimony, which could
be easily deduced by drawing branches ind
t< d
by heavy bars with zero length):
(1) Hilliella guangdongensis [sensu Zhang],
which has been merged in H. lichuanensis sensu
Al-Shehbaz et al. (1998), is separated from remaining H. lichuanensis sensu Al-Shehbaz et al. (1998),
and it is more closely related to H. hunanensis, a
taxon that was recognized by Al-Shehbaz et al.
(1998).
(2) Hilliella warburgii and Cochleariella zhejiangensis are not integrated into H. fumarwi,i< : sensu
Al-Shehbaz et al. (1998), but (3) r
with those from the/n
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Volume 87, Number 2
Koch & Al-Shehbaz
of H. warburgii and C. zhejiangensis formed one

single cluster with no separation of H. warburgii
versus C. zhejiangensis. This is in agreement with
previous concepts combining both taxa, C. zhejiangensis and H. warburgii, in one single taxon. These
congruent ITS and trnL intron findings demonstrate
that both Y. lichuanensis and Y. fumarioides species
complexes, treated as well-defined taxa according
to the morphological revision of Al-Shehbaz et al.
(1998), do not form monophyletic groups by molecHowever, some incongruences among the two
molecular data sets could be detected: (1) Yinshania qianningensis grouped either inside the Hillu Hal
Cochleariella clade (trnL intron data) or into Yinshania s. str. (ITS data); (2) H. rupicola (D. C.
Zhang & J. Z. Shao) Y. H. Zhang also clustered
into two different subgroups within HiUieUalCoch
leariella.
The alignment of ITSl-5.8SrDNA-ITS2 is 644bp

in length (Fig. 4). Within the ITS1 region (bp 1301) there are 143 variable nucleotide positions
(including 62 autapomorphies). The ITS2 region
(position 456-644) contains 85 variable nucleotide
: -ili. i - (including 57 autapomorphies!. The 5.8S
rDNA gene, located between both spacer regions
(bp 302-155), contains 11 variable nucleotide positions (including 6 autapomorphies). Because of an
ambiguous alignment, nucleotide positions i;r
153 and 460-484 were removed from the original
data matrix (Fig. 4), resulting in a final data matrix
of 412 bp.
Fitch parsimony analysis resulted in one MPT
with a length of 288 steps and a consistency index
of 79.5% (66.5% if autapomorphies are excluded).
The phylogenetic tree (Fig. 5) showed closer relationships of Yinshania to taxa from tribe Arabideae
sensu Janchen (1942) (Arabidopsis (DC.) Heynh.,
Barbarea R. Br., and Cardamine L. were used to
represent tribe Arabideae). However, Cochlearia
(including species loosely affined to the Yinshania
complex) and Capsella rubella were placed by
Janchen in the tribe Lepidieae, where they had
been put by Hayek (1911) and Schulz (1936). Our
ITS data do not support this latter placement. A
molecular analysis of Arabidopsis, Arabis L., and
their relatives shows a close relationship of Capsella rubella to Arabidopsis thaliana (Koch et al.,
1999b). Also demonstrated is the polyphyly of Ar. The
Little is known about the cytology of Yinshania.

Zhang (1995, and pers. comm.) counted 2n = 12
for Y. qianningensis Y. H. Zhang [= Y. acutangula
sensu Al-Shehbaz et al., 1998], Y. henryi (Oliv.) Y.
H. Zhang, and Y. furcatopilosa (K. C. Kuan) Y. H.
Zhang, 2n = 42 for Hilliella yixianensis Y. H.
Zhang, H. paradoxa (Hance) Y H. Zhang & H. W.
Li, and H. changhuaensis [ Y. lichuanensis sensu
Al-Shehbaz et al., 1998], and 2n = 44 for H.
shuangpaiensis Z. Y. Li [= Y. rupicola sensu AlShehbaz et al., 1998]. These data correspond to the
ITS-derived phylogeny, in which the diploid ).
qianningensis, Y. henryi, and Y furcato]
gether with Y. acutangula, are separated from the
polyploid Hilliella. Within polyploid Hilliella. the
Hilliella taxa with 2n = 42 are combined. Hilliella
... iensis (represented in this study by ace.
no. 4, Fig. 2) with 2n = 44 did not group closely
to the known 2n = 42 taxa !representi
in llnstudy by ace. nos. 2, 11, and 15, Fig. 2). However,
pi'.-llinn.ar. Il lein.im- p..--iHe lli.ii tin //-,'''<./,'.//
l/a group could also be represented by
polyploid taxa with In = 42 and 44. Base chromosome number for this hexaploid group is x = 7,
instead of x = 6 as in the Yinshania group. A few
taxa uidnn tlie ///>'/,,1/,!><<>< *'./e./',.//</ clade may he
aneuploids (2n = 44) that derived from In = 42.
Seine int.-resting I. alures etneip \\ I . n lo| < logics of the ]ihylogenetic trees are compared to the
geographic distri
ia sJ. Geographi-"l'n an I' ITS si i
pes from taxa of
the four main clades within Hilliella/'Cochleariella
do not tollou iheii phvlosAenetic relationships I fig.
7), and they are randomly mixed in Southeast China
in the provinces of Guangdong, Jiangxi. /h- i n .
Anhui, Hubei. an I
n Sielin in. However, they
are separated geographically and phylogeneticall)
from the Yinshan,:! -lade It >m Hunan, Xizang, and
Sichuan. Taxa from the Yinshania clade extend the
di>l:il i,tint la !he -onthui -I. \ mised listi ;l nit ion
of DNA types also holds for the trnL data. No geo_' i 11ii I i i i i ii pi ist III i i pes could be observed among taxa from the HiUu 11 \J(
h ' ot U i
clade (Fig. 8). Based on trnL intron data Y. qian(a< e. no. 1) from Sichuan inte^,i t. into
the //'//'. ila i .< /,'... './/./ I id< < .. i'_i ipln illv.
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Inn II lii
- I HI ii HI t . . ii In i i
il
ii liMances wen- calculated
|>i ,_ an, TRKECON (van de Peer & de Wachter, 1994) under the Kimura model (Kimiira. 1980). (,a,s were
mil. ami
n Ii II i M -i | i nu I
illm
I
I il i
i I
Ii
'I
igroup taxa. The DRAW-KQl AL-KI)<,KS
ITS /Ofi^
41
-
f ' /\
^vf*
^^rîl ^>V# ^ /
^ IcSD ( 0/V
/^
j
/
/
^" \
1
258-
^T"" ^ Vi^n/
^J
^'^ ^"Pacific Ocean 2oi.

/
.. Ihl
n n
6o km
^*\
105 \
I
\
100
Distill i I .
\J^&as4-
Figure 7.
>
Hilliella- /*"
CochlearieRti
<pj
95
/l
>/
( \W>
1
in.
115
I
-
, ,i, , .
-MI.us
120
\
limit i -luil\ in Cli
nicies ami IM>\< iii well
i n
nl i H
\Inch are combined to a single group in Figure 8 (plastid i
data). Phylogenetic relationships are shown schematically in the upper left box and follow Figure 2. For llie )insht
clade phylogenetic relationships are shown to demonstrate the position <>l I
>' |). arulangula sf
\l-SI,elil,a/| lace. no. I) (refer to Fig. 2).
this accession lies close to a siniilai plastome l\pe

(ace. no. 15) from the Hilliella/Cochleariella clade
(Fig. 8). Upon comparison of the ITS and trnL inIrou-derivrd phylngenies, taxa thai showed different positions in the phylogenetic analysis (e.g., H.
rupicola, ace. no. 14; H. fumarioides, ace. no. 17:
one additional ITS sequence copy) were located at
I In- I'ctiler ol the )lilli<'llii!Cochif(irii-li(i distnl.u
tional area. We interpret these results as a first bio_ graphic 11 .Iffiiiiii-nt.ilii.i
Iii.11 -.Mlh II
pnlvpl mis //".,', ..." amid i i no. 17) [inssessed a trnL intron type similar to samples from
surrounding areas. I In .. I I - | . - found in that
particular individu I wen- alsi
ics.ail i nlja. i
regions and from different specie-. From llillirlla
rupicola (ace. no. 14) we could isolate an ITS DNA
type, which is aU..
accession numbers 10, 16, 17, and 20. Irn\ t rori
DNA type from accession number 14 also corn-
sponds to trnL intron DNA types from 2, 3, 11, 13,

17, and 20.
MoKI'HOI.ouc At. V\HI \TM>\ \\|> T
WOMIMII;
CONSIDERATIONS
As in numerous other cases in tin Brassiraceae.

mnrpholopi. .il dit|.-;viili.ition anient; and within socalled genera and taxa of the Yinshania s.l. com:
|
I haracters to draw
sharp and uncontroversial generic boundaries,
Flower morphology in the entire complex is of no
predictive diagnostic value, even for the separation
ol p.
\\ -J I hbaz et al., 1998). Only leaves
AIU\ fruits nil.-i eliar.n leis useful for the separation
of species, and all taxa appear to be not well de^
. t al. (1998), seed
llptUtf i d numbt I pel locule, cotyledonary posit inn. ilevel..pmenl of the fruit septum, type (if any)
Volume 87, Number 2
1 trnLyO Yi^ki^
\/
1' p?
<î
/l
Hilliella - J
' A-.1
bS
^Y^ / C3) JTW
<^^^ yi^^K
^j
95
f
100
/
P'""! .^^Pacific Ocean

600km
/
y-*\
105 \
r
X
LjJ^
i
on Wn.s/mm.i an,! //,//,

//,../,
illirllti-Coclilciiriflla chid i
ell siipppnrled ii\ liigli bootstrap

r left box and follow Fig i ' I'"
n of Yinshania qianmnz
\
of fruit compression, fruit shape, development of

papillae on the fruit valve, and trichome type, all
are unreliable in dividing the complex into the genera Yinshania, Hilliella, and Cochleanelh,. In fact,
no single character or set of characters can be relied upon to subdivide the complex into gei erii o
infrageneric taxa. The recognition of a single genus
is, therefore, taxonomically expedient, as there is
no single character setting one clade apart from
another. Even pustules on the testa surface of the
valves, which were assumed to be a good character
to separate Yinshania (pustules present) ; u //./
liella (Zhang & Xu, 1990), appear not to be congruent, failing to provide a good argument to split
Yinshania into several genera (Al-Shehbaz et al.,
1998).
,CLl
H5
i
20oJ
120
i
,-. ssmns under study in

. i ml. three plastid fail, types
values in Figure 2. Phylogenetic
ih ) iiisiianin elade ph\ logeuotie
>
' er.su AI Slielilm/| Inn
Xu (1990). This analysis considered distribution,

altitude, and habit, but also morphological chariii- lesi i in- I nt-. lull-in-i euces, flower details, silicles, seeds, and cotyledons. They concluded that minute pustules on the testa surface of the
valves were a good character to separate Yinshania
from Hilliella. Comparison of our molecular phy% ith this cluster analysis based on 32 morphological and 3 ecological characters demonstrated the lack of congruency between morphological
and nioieriilar i vol ilion. dins cluster analysis separated Yinshania sensu Ma and Zhao (1979) from
H
-ensu Zhang and Li (Zhang, 1986) (a similar resolution to the ITS data). Taxa such as H
paradoxa, H. lichuanensis, and H. changhuanensis
<
1
1> ;lated to each other (as confirmed by
molecular data by ace. nos. 11, 13, and 15 herein).
However, this morphological cluster analysis lis
grouped H. guangdongensis (ace. no. 12 herein)
this group (Y. lichuanensis clade, Fig. 2). Foi
luill) [Noli i III.II
III.irk. I- ;l I.'
_'
l.lll
ill
.HI '.111.
as a xv.-IIij|i|M)i!i-.| jjoup u.
11 >l i. >li ><_ n al ln-|.
analysis (Zhang & Xu, 1990). In
Hilliella there is little mm:
i
Willi mil molecular data: ! 1 ) //. ;uu m/n,,,-, //. !,,,:<
liiitticnsis. anil // !ichuiinriisi.\ ; re rlosel\ related
to each nlliei (as ), lirll!i(incilS!\ > lade. Kig, -">: (2)
//. h'i/i'inrtiM> ami //. >;;,,.,;',, . miiped m-dlita on
the ITS tree (but not based on *mL data, Fig. 2).
No further correlation could be observed. None of
tlm three data sets (ITS. /.",-, I . inlron. im>r| thologv I
is powerful eno igh to elucidah ph\ Ingenetie -.-rial
lot the \vh(l< species complex I loivv .a. significant
correlations could I
hen cpDNA- and
nrDNA-derived pbylogenies were compared, dividing the /
'
ide into several
subgroups (Fig. 2) clearly
atives from Hilliella/Cochleariello
eeplion o| ) .. .
,CHI
The phylogeny based on plastid trnL intron seqnellce data relleels the maternal linages IK cans.
plaslids are mini iled matt i nalh in most augm
sperms, including the Brassicaceae (Harris & Ingram, 1991; Reboud & Zeyl, 1994). Introgn ssmn
oi a chloroplasl I \ pi- . Iiaraoi. ristic tin the //,'/;< //,./
Cmhlrnricllii clade into )snsiunt),i ifiannin^rnsis
possible gene flow between both
ise ol the highly pol\ pic d gonial . - al
. // ;>i/'nil,H'i II /,.('_",,,/.'"v,'s ai d
//.. Jui(i!iî><ii<,ri'ii\ (represented h\ ace. nos. 2. 15.
11, and 4, respectively, in Fig. 2) with multiple
rDN.A loci, and the assumed hybridization within
i
< Iln c lade and even with the
)in\liamii lad. . there is a high pinluhihtv oi . on
certed ITS sequence evolution. In principle, there
are three diHerenl ways that two dim-rent ITS copies evolve within
-in r lis indi\ i.iil I I ) imidiree'i i
>in .!>!. ihiiion |. ul to the loss of one
. op\ and fixation <:)' the second (del. led in //. >,//>
kola ace. no. 14, herein; and in Gossypium, Wendel
et al., 1995a); (2) both ITS copies are still present,
which might be mostly the case in young . 1 i I i
genous taxa (dot. led in // inn
aides ace. no. 17,
and ('.. jiriiatiifciisis ace. no. 21. lip, 2: m Kn^m.
Kim & Jansen, 1994; in Arabidopsis, 0'Kan< el al.,
I'l()f0:
..(<! (.-!) ."..n,-cried e\o| tin i
leads to a new
ITS type that represents a mixture of the two original ITS sequences (in Gossypium, Wendel et al.,
1995b; in Microseris, van Houten et al., 1993; in
Microthlaspi, Mummenhoff et al., 1997). The third
type of concerted evolution might have happened
in H. sinuata (ace. no. 3). This accession showed a
plastome type more similar to //. shmu
(ace. no. 4). However, ITS sequence types from pulequence types from //. lunula
(ace. no. 9) and It
(at e. no. I) exhibit some additive features found in //
(ace. no. 3). Comparing these three sequences,

there are 39 variable nucleotide positions (21 in
ITS1 region, and 18 in ITS2 region). Within the
ITS1 region, 17 out of 21 variable nucleotide positions (81%) are identical among the two H. sinuata accessions (nos. 3, 9); H. shuaiu
shared onh tin. . miitulim > with //.. smutila la. <
3). Within the ITS2 region both H. sinuata accessions have only one nucleotide position out of 18
paiensis (AW. no h shared I pns
s \i\\\ , ; aiili
H. sinuata (ace. no. 3) and two positions with H.
sani'ilu (a. c. no ':>: I lie-e lindiii- s u dieate th it
ITS type of H. sinuata (ace. no. 3) consists of a
mixture of ITS types from relatives of //
/.,.',/o\ |m..stl\ II">2 region) and //. iinuota (ITS1
region). The DVI-I ill sequence divergence between
I
'>,,<> o, nsis (m i no 1) and // \in '<
et
no. 9) is 7.8%.
Concerted evolution of ITS DNA loci has been
-
i tal
Hint -
It
mi
th.
lb
(O'Kane et al, 1996; Mummenhoff et al., 1997;

Koch et al., 1998b; Franzke et al., 1998) and other
families (Wendel et al., 1995a, b; Buckler et al.,
1997). Sequence divergence values of ITS types
from putative parents, giving rise to hybrids in
which eoneerleil evolution has been observed,
i.uip. d horn .'. I". I 1/'. ;a!l,!,^;>, mini', am v,. \J.
perfoliatum, Mummenhoff et al., 1997), 5.0% (Car</<iminc umaia \~ '.. riruhtii-, :iiirt . Kran/kt et ah.
1998), to 6% (Arabidopsis thaliana vs. A. arenosa,
O'Kane et al., 1996) comparable to a value of 7.8%
loiiiid anions // J, .,.",.-.<>( ' :>,< \. t~u- // v/,".//,/
We conducted a split decomposition analysis to
visualize eonlliclmt: phv lo-em li.
signal indicating
concerted evoluti
_
.
Cochleariella chide (Fig. 6). Tins ,maK-.- .-l.-aiK
indicates hybridization with subsequent concerted
evolution of ITS regions in H. sinuata (ace. no. 3).
< (oiiccrled evohiiioi ol IT"- sequences greatly influences any interpretation of the ITS phylogeny.
Since diploid members of the Brassicaceae such as
Arabidopsis thaluma typically show 2 NOR loci,
one could assume that in hexaploid Hilliella/Coch

leariella taxa at least 6 major NOR loci are present.
Therefore, sequencing of two individual ITS clones
is not a sufficient survey to find all putative ITS
types from a single individual. This undersampling
leads to an underestimation of ITS type ti< n
i- -!! - \i
- gt - if hybi ]i IIinn and concerted
evolution.
We found evidence suggesting concerted evolution ,md .|.'-. 111.ill 'Li.' .'Vltr||.]r- // !!),/.i,!>-<
acc. no. 17, H. rupicola ace. no. 14, H. sinuata ace.
no. 3) of possildlt }i 1. nil iiK i
i~i
.< II. II
concerted evolution of ITS sequence. The overall
amount of sequence divergence between taxa in
this study demonstrates a relatively high age for the
different lineages. In fa. t. sequence divergenee . ;I
ues are much higher when compared to those obtained in infrageneric studies of closely related species of other Brassicaceae (e.g., Cochlearia s. -it
< 1.75%, Koch et al. (1999a); Noccaea < 4.5%.
Mummenhoff et al. (1997); Cardamine < 4.5%.
Franzke et al. (1998)). Within the Yinshania clade.
sequence distance values range up to 6%, bu
in the HilliellalCochleariella clade they rang
high.-
\l Shehku. ., V K (. >. ,- ]<>i\. Notes on Chinese

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Mmhania, llillirlln. and CochlearieUa in China. Acta
Sci. Nat. Univ. Intramongol. 23: 561-573.
/unk. K.. K. \lumiiM-,.l,..tf. M. Ko.l, ,\ H. Hurka. 1996.
Phylogenetic relationships of Thlaspi s.l. (subtribe
hi -ti mi'. I.epidie.ie) and allied genera based on
chloroplast DNA restriction site variation. Theor. Appl.
Genet. 92: 375-381.
MOLECULAR CONFIRMATION
OF UNIDIRECTIONAL
HYBRIDIZATION IN BEGONIA
X TAIPEIENSIS PENG
(BEGONIACEAE) FROM
TAIWAN1
>i iiiiiii.ii '
j..//,,, tint -liii
i! .
Ching-I Peng2 and Tzen-Yuh Chiang*
. ..II cl.'-.l f I -: -til *e\e.\il
piematurely
ILMMIII
,.. n
hybrid oiisin Moipli.il

i ill i i
L II! in
i
li i, i
11
i
I
j
i ill il Inliii.li/.ition
showed that such plants are F! hybrids (2n - 11 l tv\. . '"
!
I
mine (n = 30) and B.
aptera Blume (n = 11), both of which are widespread in Taiwan and sympatric in most of their ranges. These hybrids
were nim.il /,'.
il , MI--- I lu..n llu putative parental species (
resulted in germinable seeds and healthy F, plants only when B. formosana v
f the atpB-rbcl. spacer of chloroplast DNA confirmed that unidirectional hybridiz
jptera have been detected. Abortic
i the parental species.
atpB-rbcl, noil
. In
'
_.>!:
hup, i,'lists.
.1 hybridization, natural hybrid. Taiwan.
Natural hybridization, one ol the most iidlueiilial

processes that increases species diversity and sta( -s.itv via genetic recombination or introgression (Arnold, 1992, 1993), occurs
frequently in plants (P. S. Soltis & D. E. Soltis,
1991; P. S. Soltis et al., 1992; Arnold, 1997). Studies on the origit
'
netic composition frequently raise fundamental
questions concerning reproductive barriers, survivoiship and illness ol the hybrids, ai <! m< . \\, in i
i n ti ulate evolution. In many cases (e.g., Louisiana Irises; Arnold & Bennett, 1993) natural selection may favor hybrid plants of specific maternal
origin. It is essential to study the genetic makeup
of natural hybrids in order to elucidate evolutionary
processes and the ecological adaptation ol these
plants.
It has been abi i '
rah d that natural
hybridization plays a major role in the evolution of
species groups or complexes (Ludwigia: Peng,
1988, 1990; Iris: Arnold et al., 1990; Glycine:
Doyle et al., 1990; Helianthus: Rieseberg et al.,
1990, Rieseberg, 1991; Gossypium: Wendel et al.,

1991; Senecio: Harris & Ingram, 1992; Allium:
Ohsumi et al., 1993; Leucaena: Hughes & Harris,
1994; Arabidopsis: Mummenhoff & Hurka, 1995;
>hium: Baldwin, 1997; and Argyranthemum: Francisco-Ortega et al., 1997). Natural hy:>i ::i/aliou uc-. u> lr<-ijiirii'U u Iniuane-e /V_ >;<i
(Y. K. Chen, 1988; Peng & Chen, 1991; Peng &
Sue, 2000), which may have resulted in the high
level of endemism of this genus on the island
(66.7%; cf. C. H. Chen, 1993), while causing difficulties in clarifying }>liv I. _ <
..
(see Rieseberg & Morefield, 1995).
Begonia X taipeiensis Peng was recently described as an..
n,i. I
id llVi 0. Nn
2000). Geographical distribution, low level of pollen slainability, and intermediate moipli
cbaraclers between B. formosana (Hayata) Masamune and B. aptera Blume initially suggested such
an origin. Begonia aptera [sect. Sphenanthera
(Hassk.) Warl
distributed in northern Taiwan,
en : I I Huang. The authors thank Chian-Yi Sue for nsse

llisl
;
.1 l.;>.
I>IO<>.
wan. Both species occur in wide altitudinal ranges

(50-2000 m). They frequently co-occur throughout
their range of overlap (Fig. 1). The flowering periods are March to December for B. formosana, June
to August for B. aptera, and April to December for
B. X taipeiensis. Two discrete populations of Begonia X taipeiensis were found mixed with its putative parents in the Taipei Basin of northern Taiwan. Begonia formosana is characterized by having
creeping rhizomes with ascending to erect flowering
stems, broadly ovate, lobed leaves, 2-locular ovaries, and unequally winged capsules, the abaxial
one being very pronounced. In contrast, B. aptera
is a tall, cane sp.-- ics l.i kirn hmi mil I tin nnes.
has lanceolate leaves, 3-locular ovaries, and rounded, wingless capsules. Begonia X taipeiensis has
short rhizomes, intermediate plant height and leaf
shape, and 2-locular ovaries (thes< <
. M.n, II.
highly reduced and without locules) with diminutive wings. Like all other species of Begonia, B. X
interflorally protandrous. At <
s abundant flowers of
both sexes. All staminate flowers observed develop
normally up to their late bud stages and then drop
i ii before they open. All Begonia of Taiwan are
frequently pollinated by blowiI
(< illiph
hover flies (Syrphidae), and honeybees (Apidae) (Y.
K. Chen, 1988). Plants of Begonia often grow along
moist stream banks. Their light seeds float and are
carried easily by water curre
> '- ' /' .
.it. |.tlln;illl\ < i l-f nt -ii 1 Willi ill. .inl ..I wind |\an
der Pijl, 1972).
Traditionally, morphologic
.

I
chromosome cytology have |
mation in revealing putative parents. Nevertheless,
such data are not sufficient to determine the direction of hybridization and to detect genetic variability. Recently, many convincing studies using moIt'cular irc!itii.|iirs Mich as comparison .,| KII.P
patterns of ribosomal DNA (Arnold et al., 1990;
Stein & Barrington, 1990; Rieseberg, 1991; P. S.
Soltis & D. E. Soltis, 1991; Hughes & Harris, 1994;
Mummenhoff & Hurka, 1995) and those of organelle DNA (D. E. Soltis & P. S. Soltis, 1989; DeMarais et al., 1992; Garcia & Davis, 1994; Wang
& Szmidt, 1994; Brochmann et al., 1998), coupled
with experimental hybridizations (Hodges et al.,
1996), have been conducted to address reticulate
or polyploid evolution (D. E. Soltis & P. S. Soltis,
1993). Chloroplast and mitochondrial jemmies. !
inf.:, maternally inherited in most organisms (Clnn
& Sears, 1985; D. E. Soltis et al., 1990), have been
useful 111 elucidating the line, H..II ol -cue flow be
tween populations (Whittemore & Schaal, 1991)

and in detecting the maternal origin of natural hybrids (Wendel et al., 1991). Thus, in this study, a
noncoding spacer region between the genes rbcL
and atpB of the chloroplast genome, which has
been used as a molecular marker at the species
level (Golenberg et al., 1993; Chiang, 1994; Manen
& Natali, 1995; Chiang et al., 1998), was sequenced.
In this study the following questions will be addressed: (1) Did B. X taipeiensis originate from interspecific hybridization between B. aptera and B.
formosana? (2) Do hybrids with alternate maternal
origins have the same survivorship? (3) Do hybrids
backcross with putative parents and produce viable
offsprings? (4) Is the frequency of occurrence of
natural hybrids a reflection of the ease of experi-
Major herbaria in Taiwan (HAST, NTUF, TAI,

TAIF, TNM) were consulted to determine the distribution and phenology of Begonia X taipeiensis
and its putative parents, B. formosana and B. aptera. Living plants of the hybrid and its associated
putative parents were collected from two localities
of Taipei County, Hsichih and Wulai (Fig. 1). Additionally, a plant each of B. formosana and B. aptera from Chiufen and Nankang, respectively, where
B. X taipeiensis was not found, were collected for
comparison (Fig. 1). All plants were grown in the
experimental greenhouse of the Institute of Botany,
Academia Sinica, Taipei, for cytological and molecular examination and for experimental hybridization. Begonia palmata D. Don, a congener colli cted from Hsitou, Nantou County, was used as an
outgroup. Herbarium vouchers were deposited at
HAST (Table 1).
Experimental self-pollinations of B. aptera and

B. formosana were done. Reciprocal crosses were
carried out between B. formosana and B. aptera
from the same localih and from different localities
in the greenhouse. Begonia X taipeiensis collected
from the wild was used as a pistillate parent for
ba< kcrossing with both putative parents. The fact
that Begonia X taipeiensis shed staminate flowers
prematurely precludes the possibility of using it as
a pollen donor. Seeds (F, progeny) were grown to
maturity to examine the fertility of pollen grains
and for cytological study.
*}
276
Annals o the
_and,,5t uiaiivepare s
Table 1. Material of Begonia Xtal

barium vouchem are deposited al HAST.
laxa
localities
Vouchers
AJ009601
AJ009602
AJ009600
2. Hsichih, Taipei Co.

i. Nankang, Taipei Co
13899
IMUt,
U,320
/oiYo
if.i.v;
16321
16292
AJ009599

3. Chiufen, Taipei Co.
Peng 13915
Peng H>3I<>
Leu 867
1. Chitou, Nantou Co.

2. Tengchi, Kaohsiung Co.
Peng It,Mil
Peng h,r,;i
AJ(X)7745
A J 242856

1. Wulai, Taipei Co.
B. formomna
B. pahnuta
EMBL
accession no.
Peng
I'm/,
Peng
Peng
Peng
Peng
Peng
ft x taipeiensU
B. aptera
for cvtologica and n .leeular analysis Her-
AJ223092
>
!,,(.(
VICO'K.Oa
AJ009604
AJ(X597
Experimental hybrid:
Bfxa-\: B. formost na X B. up era = Leu 867 X Peng 16153
BfXa-2: B. formosa na * Ii. p era = Peng 139IS X Peng 16153
Flower buds to be examined for meiotic behavior

were fixed in a 3 : 1 mixture of 95% ethanol and
glacial acetic acid and stored in the refrigerator.
I'not ic -lamina, tin bud- u.'t.' li\ili(iK/i i| lot >
8 min. at 60C using a 1 : 1 mixture of concentrated
HC1 and 95% ethanol. They were then squashed in
FLP orcein (Jackson, 1973). Somatic chromosome
counts were obtained from actively growing root
lips |IK treated lor 3 to 4 hr. in 8-hydroxyquinoline,
ill ii fixed as above for at least 10 min. The root
tips were then hydrolyzed in 1 N HC1 for 8-10 min.
at 60C and squashed in FLP orcein. All analyzable
. hi"in.i-inn . ..!il.j.iii.iti..'i- m.islb ili.ikiiu-i- or
inelaphase l! were documented with camera i.i, ida
drawings oi photomicrographs usuii; Kodak I'analomic-X lilms. Negatives and drawings are deposited at the Institute of Botany, Academia Smica.
DNA isolation, PCR, and nucleotide sequencing.

Iresli tissue of young shoots was ground in liquid
nitrogen and stored at -70C for DNA
Genomic DNA was extracted following a CTAB
methodology (Doyle & Doyle, 1989). PCR was performed in a volume of 100 u.1 reaction using 10 ng
of template DNA, 10 u.1 of 10X buffer, 10 u.1 MgCl2
(25 mM), 10 u.1 dNTP mix (8 mM), 10 pmole of
each primer, 10 u.1 of 10% NP-40, and 2 U of Taq
polymerase (Proincga, Madison, U.S.A.; cf. Chien
et al., 1976). Tin react mi
is pi ran in I i n
AJ242857
AJ242858
MJ Thermal Cycler (PTC 100) as one cycle of

naturation at 95C for 4 min., 30 cycles of de
turation at 92C for 45 sec, annealing at 52C
1 min. 15 sec, and extension at 72C for 1 n
30 sec, followed by a 10 min. extension. Template
DNA was denatured with reaction buffer, MgCl,
NP-40, and ddH20 for 4 min. (first cycle), anc
' -I d 'ti iei mill,.alialel ] , , , \rbcL-l, 5'-AA
CACCAGCTTTA(G)AATCCAA-3'; atpB-l, ACA
TCT(G) A A(G)TACT(G)GG ACC A ATA A-3'; (Chiang
et al., 1998)], dNTPs, and Taq polymerase were
added to the above ice-cold mix. Reaction was restarted at the first annealing at 52C. PCR fragments were eluli I n-n
Hi Ii I'n
I ' I! I'I > ' i
Punln ation Kit i Uoeln uijaa Mannli. am. (iennaiiv;
cf. Vogelstein & Gillespie, 1979). PCR products
vvete limited In a pT Thine T-vcclot jNnvagi n. Mad
ison, U.S.A.; cf. Marchuk et al., 1991) and cloned
in competent E. coli DH5a. Plasmid DNA was extracted iom iiaai~.lu.na':. i] all- al d si i|l|enc< il Willi
P labeling e\|i I -ii.il/lcimitialini: i, ictnm (Sanêi
et al., 1977) using/mo/ DNA Sequencing System
(Promega, Madison, U.S.A.; cf. Murray, 1989). For
DNA alignment and phylogenetic analysis. Alignment of nucleotide sequences was performed by Clustal V program (Higgins et al., 1992)
and improved by eye. Parsimony phylogenetic anal-
yses were performed by using the Phylo eneti

Analysis I sing Parsimony Program (PAUP, version
3.1.1., Swofford, 1993) with the branch and bound
algorithm. Neighbor-Joining (NJ) analysis by calculating Kimura's (1980) two-parameter distance
was also performed using Molecular Evolutionary
Genetics Analysis Program (MEGA, version 1.01,
Kumar et al., 1993). Confidence of clades reconstructed was tested b\ bootstrapping (I'Vlseustein.
1985) with 1000 replicates (Hedges, 1992). The
nodes with bootstrap values greater than 0.70 are
IJMII. H
-upporled with > 95% probability
(Hillis & Bull, 1993). In NJ analysis, completeand-partial (CP) bootstrap technique was used to
eonerl the- bias [conscrvativciiess) nl the standard
trap approach (Li & Zharkikh, 1995). A gl
test (Huelsenbeck, 1991) of skewed tree-length distribution was calculated from 10,000 random trees
generated by PAUP in order to measure the information content of the data. Critical values of the gl
test were obtained from Hillis and Huelsenbeck
(1992). The fit of character data on phylogenetic
hypotheses (Swofford, 1991) was evaluated by the
consistency index, CI (Kluge & Farris, 1969), and
the retention index, RI (Farris, 1989). The statis>C1 v < dete,
ing to the method of Klassen et al. (1991). The
number of nucleotide substitution, which is the
number of transitional and transversionaJ substil t
tions per site, was calculated following the methodology of Wu and Li (1985).
RESULTS
In all experimental geitonogamous selfing attempts made on Begonia formosana and B. aptera,
fruits with 95-100% viable seeds were consistently
obtained. Plants of B. fonrn
KM
lavs lor fruit maturation, when a- diose of />'. uplrni
required 90-150 days. Begonia formosana and B.
aptera were crossed reciprocally in the experimental greenhouse. Nearly all crosses using B. formomature fruits with 80-90% plump seeds 35-45
days after pollination. Such seeds were viable and
flowering artificial F, hybrids were readily obtained
from them. The level of stainable pollen in these
F, plants was extremely low (ranging from 0 to 5%),
which agrees with that of the naturally occurring B.
X taipeiensis. When B. aptera was used as the pisfruit drop occurred ca. 60 days after artifici Ipob
Experimental hybrids betwe
B. aptera were grown to maturity. They flowered

annually and have persisted in the mist greenhouse
since the summer of 1995. The plant height in
these artificial hybrids was within the variation
range of naturally occurring B. X taipeiensis. The
ni !. i , li : i ->U resembled B. X taipeiensis
in habit and details of vegetative as well as floral
characters. When plants of Begonia X taipeiensis
collected from the wild were backcrossed (as pistillate parent) to B. formosana and B. aptera, respectively, fruit set was successfully obtained.
However, five backcrossing attempts made with B.
formosana and 11 such attempts with B, aptera produced fruits with zero or negligible plump seeds
that failed to germinate.
UIHOUOSOVIK CYTOLOGY
I'II
. ii.. i- >fudii-- re\ealed a mei
number of n = 11 in B. aptera, n = 30 in B.
formosana, and 2n = 41 in B. X taipeiensis (Peng
& Sue, 2000). Like B. X taipeiensis, exjx rimental
hybrids of B. formosana X B. aptera consistent
have a somatic chromosome number of 2n = 41.
\lso. abnormalities in ehromosom. configurations
were observed. M
ti< hromosome configurations
B. fo,
h of 854 base
pairs of the atpB-rbcL spacer were obtained from
B. X taipeiensis and its putative parenl
Fifteen
iriabl
i swen found betweei sequences (Table
2). That this chloroplast spacer has, on average,
34.0% A and 36.1% T agrees with one of the common pi. perties, i.e., AT-rich, of most n..in-odmg
spacers (Li, 1997). Differences in the rate of nucleotide substitution (Table 3) among species of Begonia we sampled ranged from 0.0017 (between />'.
aptera and B. formosana) to 0.0056 (between B.
aptera and B. palmata) (mean = 0.0033).
Of the three individuals of B. formosana we examined, two had identical nucleotide sequences
(Tables 1, 2). The third collection from Chiufen
{Leu 867) differed at two different positions (bp 191
and 762). Interpopulational variation was present
in B. aptera at bp 275 and 794. In our study, sequences of this chloroplast spacer for all three species were highly conserved, with 15 variable sites
(2.1% of 854 bp) (Table 2). Begonia formosana
shared with B. aptera 7 derived characters (at sites
43, 44, 251, 252, 280, 568, 743). Two autapomor-
.--"1
LjJ
ft
I |..uiv 2.
Yin
. Telophase II. Bai equals 10 |xm ( \. Begonia
Table 2. Variable sites fthe

species. Dots indicate that i< u
Taxa/Sites
LIN
ft /)/cra 16321
ft aptera 76276
e sequences of the atpB-rbcL ipacei re iono thecl or plasl DNAofB

/6.;i'/.
sequences are identica 1 to those for Begonia
"'"' '
i()i
2,1
' 2
270
275
286
298
;,7i
;,7o
568
7 3
762
1i
V,
<;
c
c
B. aptera 76292
B. taipeiensis 15106
B. taipeiensis 13899
BfXa-l
B.formosana 13915
B.formosana 16319
B. formosana 867
B. palmata 16831
r
r
i
i
<
3. Pairwise e
I). 1. B. aptera 16321; 2. B. aptera 16276: 3. B. aptera 16153: 4. B. ap
ifi,.si.s /.-.V;W: 7. B. taipeiensis 16320; 8. BfXa-2: 9. B/Xfl-/: 10. A /orm.
12. B.formosana 867; 12 . B. palmata 16081; 4. fl. /w/m/ 76837
1
11
10
12
13
14
(1.0017 0.0017 0.0017 0.0017 0.0028 0.0017 0.0017 0.002:; o.oo.v.

0.00,0
0.0056
0 056
0.0017 0.0017 0001 0

0
I 00017 0.0017 0.0028
0.0000 0.0000 0.0000 0.001 I 1,0000 O.O(KH) 0.0011
0.0000 0.0000 0.0011 (
O.(XXK) 0.0000 0.0011 (
0.0011 0.0011 0.0000 (
phies, at positions 371 and 376, in B. formosana

distinguished it from B. aptera.
The sequences of Leu 867 and Peng 13915, both
B. formosana, differed at two sites. The genetic
uniqueness of tin
<
<
to the F, offspring, i.e., B/Xa-1 and BfXa-2, respectively, when they were used as maternal parent
in experimental crosses. We sampled two collections of Begonia X taipeiensis, Peng 13899 and
15106, both associated with B. formosana, Peng
13915, from the same locality. Both Begonia X
Disci ssi<
. I Ml I ..
"^^
II, M
eria, B. formosana
and B. aptera were initially suggested as the putative parents of B. X taipeiensis (Peng & Sue,
2000). Cytological data showed that both the experimental hybrids between ft formosana (n = 30)
and B. aptera (n = 11) and the naturally occurring
B. X taipeiensis have the same chromosome num-
taipeiensis specimens were found to have identical
hcr
sequences (Table 2) with the experimental hybrid

(BfXa-2)
*P*S wi,h n = 30 in Taiwan- which is the hiShest

chromosome number among these Begonia. Chro15, 18, and 19 are
known for other members of Begonia c
Parsimony analysis i
5 of 16 steps (Fig. 3),
< 0.01), and an RI of 0.958. A gl statistic of
-1.468 indicated a slgnificant signal (P < 0.01).
rp.
t
.
n?Z\
J i
llir M uu
S''i}ibor-Joini
11
l.\
MEGA based on the Kimuras two-parameter d.stance (Table 4), ,,
.I.,IS,I,I
u,.h .he parsimony
trees, but with higher resolution. Three major

clades in both parsimony and NJ trees (Figs. 3, 4)
obtained in these analyses were supported significantly by bootstrapping: the clade of B.formosana,
B. X taipeiensis, and an experimental hybrid
(BfXa-2), the clade of B. formosana (Leu 867) and
an experimental hybrid (BfXa-1), and the clade of
B. aptera. Within the first clade the monophyly of
the subgroup composing the maternal parent (B.
formosana, Peng 16319), the hybird offspring
(B/Xa-1), and another B.formosana (Peng 13915)
was Iso siiniilii ill -supported
<Y"
ol
2n
" ^
4L
begonia formosana is the only
1988 A
chromosome number of n =
U
/'"'J'""'"U^ '" "" > ^'J' * T
anu B
- Palmata (Y. K. Chen, 1988; Peng & Chen,
_ __^
.
ill
.
^ for &
^
^ baged
rfft x
on
tengive
Wc dlstnbulion of the specie, Ex.

heUwoA
and
examination
of
herbarium
matenaJ n.v(,al(,(, tha( the ranges of R aptem and
formosana
taipeiensis
cies
at ca
iargely
overiap and that piants of B_
usually co-occur with these two spe60_200 m in eievation. 0n the other
hand, & palmata, mainly a montane species of

higher altitudes (ca. 600-2100 m), is geographically and altitudinally disjunct. Based on data from
experimental crosses, cytological observation, and
geographical distribution, we conclude that B. X
taipeiensis represents Fl progeny from natural hybridization between B. formosana and B. aptera.
Baptera 16321
Baptera 16276
Baptera 16153
Baptera 16292
Btaipeiensis 15106
Btaipeiensis 13899
Btaipeiensis 16320
Bfxa-2
Bformosana 13915
Bformosana 16319
Bfxa-1
B formosana 867
Bpalmata 16081
Bpalmata 16831
s recovered by PA UP f
Volume 87, Number 2
Peng & Chiang

Begonia x taipeiensis Peng
B taipeiensis 16320
B taipeiensis 13899
B taipeiensis 15106
Bfxa-1
B formosana 867
B palmata 16081
B palmata 16831
\M) lAHHIMI.NTAI. HYBRIDIZATION

Identical sequences of the chloroplast atpB-rbcL
spacer between B. X taipeiensis and B. formosana
suggested that the former had a maternal
n
from the I.ill.-I I imltiM lioii.d hv In idi/ IIMTI L .IIU
rise to the natural hybrid B. X taipeiensis is con<ii':iii:i with the resiilt> tiorri re. iprncal crosses in
which viable F,'s were obtained only when B. formosana was used as the pistillate parent. Experimental crosses using B. aptera as the maternal parent resulted in precocious Inn! drop, possibly as a
result of genetic disharmonies. A similai i
tion was made on Lousiana irises (Arnold & Bennett, 1993), in which unidirectional hybridization
was documented using cpDNA haplotypes. Naturally occurring iinidmelioriul hybridi/atmi: su,n
gests that hybrids of reversed parentages may have
(liilennl survivorship, because organelle ênomemay contribute genetic information that critically
affects the survivorship of their progeny.
her organisms, such as in Hylo3.012; Chiang, 1994) and Rubiaceae (K = 0.027; Manen & Natali, 1995), the
ehloroplasl -cur!!, variation between sperh - ! !',<
gonia appears to be low. The li~
I ties'.
i derived sites (371 and

376) and that of B. aptera supported by a shared
derived site (298) indicated, however, that this
spacer is an appropriate marker at species level.
The low level of interspecific variation in chloroplast DNA in Taiwanese Begonia may be ascribed
.atural hvbn li/aiion
I (Liu, 1999), which facilitated the morphological evolution and evolution of
nuclear DNA via genetic recombination (based on
our preliminary assessment of RAPD and nrDNA
ITS sequence data). The possibility that the evo*i. i passed :hal oi die -lilorcplast I )\ \ was Miuilarb
mstrated in oaks with frequent natural hybrid. i\\l ii
Seba, . IWIi.
r.ii'i-.i, \.s/.s
Natural hybrids may be considered to be impoverished genetically (cf. D. E. Soltis & P. S. Soltis,
1993; Arft & Ranker, 1998). Whether natural hybrids are more or less fit relative to their parents is
a controversial issue (Arnold & Hodges, 1995). Expci mi ulal h\ hi idi/.ition in this -hub revealed that
there are very few if any pre- and post-/.
i
productive barriers between these Begonia. We
il
IK
is
Mfli
ISI
would expect natural hybrids when species of Begonia, such as B. aptera and B. formosana, co-occur and have overlapping flowering periods. Begonia taxa are also well known for their capability for
vegetative propagation: they easily proliferate from
fragments of stems, rhizomes, or leaves. Hybrid
populations of B. X taipeiensis, however, are of sporadic occurrence (Fig. 1). Furthermore, such hybrids drop staminate flowers precociously and are
completely seed-sterile. Their sterility, small population size, and rare occurrence suggest that they
are less fit than the parental species, B. aptera and
B. formosana. Many recent studies also indicate
that natural hybrids are usually less competitive
than their parental species, unless a novel niche
can be explored (Arnold, 1993; Arnold & Hodges,
1995).
Begonia X taipeiensis was not known until very
recently (Peng & Sue, 2000). It is seed-sterile, of
limited distribution, and co-occurs with its parental
species. Because it sheds staminate flowers precociously, we used it as an ovule donor to make experimental backcrosses with both of its parental
species to test the possiblilty of introgression. Such
attempts consistently failed to produce viable
seeds. This, plus the sterility in B. X taipeiensis,
led us to suggest that it can only persist through
recurrent hybridization. Many recent molecular
studies also suggest that recurrent hybrid tatioi
events may occur over short spans of time (Ashton
& Abbott, 1992; D. E. Soltis & P. S. Soltis, 1993;
Arft & Ranker, 1998).
Although B. X taipeiensis is highly sterile, significant genetic variability could have been incorporated and accumulated into this hybrid from genetically distinct parental species (cf. Arft &
Ranker, 1998). In nature, B. X taipeiensis with low
frequency of fertility, which may not have been detected due to limited sampling, may occur. Similarly, the low level of viable seeds in backcrossings
did not rule out the possibility of introgression in
wild populations. Further study with wider and
more intense samplings will be able to provide insight into the impact or potential of rarely occurring
events on the evolution of Taiwanese Begonia.
In conclusion, when analyzed in concert, the
data suggest that the formation of the natural hybrid
B. X taipeiensis occurs via pollen transfer from B.
aptera to the maternal species, B. formosana. Unidirectional hybridization suggests that differential
survivorship exists between hybrids with reversed
maternal origins. Even considering the ease with
which experimental crosses are obtained, natural
hybrids appear less fit than the parental species in
this study, based on their sterility.
Arft, A. M. & T. A. Ranker. 1998. Allopolyploi I origi

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M. Baskin2 and Carol C. Baskin2
VEGETATION OF LIMESTONE
AND DOLOMITE GLADES IN
THE OZARKS AND MIDWEST
REGIONS OF THE
UNITED STATES1
easier., I nihil Slates is forest iShreve, 1917; Braun,

1950; Kuchler, 1964), long-persisting plant commimri- - d .muni, 1 U In il ... m- tnî. .sp, : m- mi!/
or crvplogains occur in areas where bedrock is exposed and/or soil depth in most places is too shallow
to support ho. - oi 4,11.:;-, K\ llli|lr- oi ihese oil: pi
ie climax rook outcrop romii, indies m. hid,- tin mid
Appalachian shale barrens (Piatt, 1951; Keener,
1983; Braunschweig et al., 1999), granite outcrops
nl tin s..iil[i.-as|i-ni pi,-(11111)111 |Oo>lmi_, e, \nd, ison.
1939; McVaugh, 1943; Keever et al., 1951; Burbanck & Piatt, 1964; Palmer, 1970; Shure, 1999),
and the cedar (limestone) glades of the Central
(Nashville) Basin in Tennessee (Quarterman, 1950;
Baskin & Baskin, 1985; Somers et al., 1986; Drew,
l((M I and ol the southeastern United States in general (Baskin & Baskin, 1999).
The terms "ceil i J nl - m
inn slom (oi dolomite! -Jades" are also used lo desci il,< -r.iss/j<,i \,
dominaled openings o\ei shallow lim.-stniie oi do
lomite soil on ridgetops and side slopes in the
Ozarks (Steyermark, 1940; Erickson et al., 1942;
Kucera & Martin, 1957; Ladd & Nelson, 1982;
Nelson & Ladd, 1983; Nelson, 1985; Fig. 1) and
Midwest (e.g., Curtis, 1959; Kurz, 1981; Aldrich et
al., 1982; Heikens & Robertson, 1995). Thus, the
use of these teim> :n llie < '/alk- ( \ikansas. Missouri), Midwest (Illinois, Indiana. Ohio. Wisconsin!.
and Southeast (see fig. 12.2 (map), p. 208 in Baskin
A Raskin. i">"<!> i s |.,-ci n.leipn led to mean thai
cedar glade vegetation is the same in the three regions (cf. Curtis, 1959; Kuchler, 1964). However,
cedar glades of the southeastern United States are
dominated by ('., sii mi in i mi i I _
- riinariK
^ .. , !>.
-./
.
id in .-,- of the Ozarks/
Midwest are dominated by C, perennial .
pi mi.il ih N '"',:,/. 'i ., '-.m u ,.;,.i',it, iHiskth et al..
1994, 1995). In a recent review of the literature on
cedar glades of the southeastern United States, Baskin and Baskin (1999) concluded that: (1) Sporo''',./..> i /j,'i'",//.-,' > i- ih, m.- important species in
this limestoni
mite rock outcrop vegetation
type; and (2) neilh.-i S< hiza< livrium scoparium nor
any other perennial grass sp<-< ics is an important
omponeiii of the vegetation. No such review of
i|iiantitaiive mloni ation has |rii published on tinvegetation of calcareous glades in the Ozarks and/
or Midwest.
Thus, the purpos, ,:1| ihi- papei is lo review the
literature on the v< getation of limestone and dolomite glades in tin ' ik> and Midwest. In particular, quantitative and/or qualitative evidence is
piesenl, d 'ha' 11 d. - d \ ''<' ."/,.',' n, v, ../.,/-,.///, is
Aw. MISSOURI BOT. GARD. 87: 286-294. 2000.
tallii DC. Berchemia scandens (Hill) K. Koch is a

i
M ,, /",;>, < ,,s , :> ^t.Ulii,)
THE OZARKS
Steyermark (1940; see also Steyermark, 1959)

recognized five climax vegetation associations (sensu the polyclimax theory) of the Missouri Ozarks
; i ilii in.. . ,1. -. rihed stages in primary succession leading to each of them. He also recognized
sevrial subclimaxes in these seies. However, these
|.iesuined sue. esMiinal sequences probahb i. present vegetati
The open 1
Missouri Ozarks are the first two stages of what
-Mevem il'> 1 'i [ii sented as a six-stage sere beginning on bare, rocky slopes and ending with a
sugar maple-win
Umax: (1) BouteImm i uiitpiiuiui,/ (Mi.-hx.) Ion. Rudbcckiu inissouriensis Engelm.; (2) Rhus aromatica Ait.-Diosginiana L.-Juniperus virginiana L. (with a
redeeilar subclimax persisting
slopes and knobs
.;;
iuginosa (Michx.)
Pen. Viburnum rufidulum Raf.; (4) Ulmus alata
MH-II
'
oliniana Walt.; (5) Quercus
muhlenbergiiEngelm.-Fraxii
I
ith
Q. muhlenbergii forming a subclimax on southern
and western exposures); and (6) Acer saccharum
Marsh.-Quercus alba L. Climax vegetation in the
White River region of southwestern Missouri may
be Q. muhlenbergii-Cotinus obovatus Raf. Thus, the
pioneer stage in this sere is a limestone (or dolomite) glade (sensu Steyermark, 1940: 392) ". . .
of prairie species. . . ."
Bouteloua curtipendula and
Rudbeckia missouriensis (B. curtipendula, Psoralidium tenuifiorum (Pursh) Rydb., and Silphium laciniatum L., or b
u Vit. and B. curtipendula in some parts of the Ozarks). In addition
to I C ardii md B ..<< , , ,, other important
C, grasses on tin - gl d
i
'inicum virgatum
L., Sorghastrum nutans (L.) Nash, Schii
i x . bolus neglectus Nash. Imporlaul I'orbs include \gtnv fiigtrttca (L) Hose, \lliiim
stellatum Roth., Aster oblongifolius Nutt., Calamintha arkansana (Nutt.) Shinn., Dalea purpurea
\eiil., l-',rhiimi-eti imllnhi (Null.) Null . /,'. patado.xn
(Norton) Britt. var. paradoxa (an Ozark cedar glade
eulenuel. llcd\<ili.\ ni^ricin , I am.! bosk. He'll
Nutt.) Torr., Oenothera macro:, and Polytaenia nut-
and other woody plants invade these limestone (or

doloinili I d.ule- l:n,'t,< t:>s , ;>^:iihin,i t\pnall\ hecomes the most conspicuous plant, especially on
eroded dopi
ind
bald knobs," forming what
Sir-,'."iin.irk relerred to ,is "cedar glades," "red cedar glades," or "red cedar balds." These terms indieali sealteied red. edar trees in a matrix of herhareous vegotaliun dominated h\ pmirie grasses, in
particular A. gerardii, P. virgatum, and S. scoparium. In the W le
!
i
ill
leu
Missouri. ./. n>ti!iii,t'hi aud/oi I). ; ugjniurui uia\
invade limestone glades and become the dominant
-p. i it's. S.i^.ilr,:-- Hi!', I:mi |\uM I \ee-. ma\ co-occur with D. virginiana as a pioneer woody species.
Other investigators also have found that prairie
grasses are the dominants of cedar glades in the
Ozarks of Missouri. Kucera and Martin (1957) repoit. d S. !,;,/, Ii .,','."' w .//..i.M-.m (, ill. doininanl
p
B5% fn
b of 1 erbaceous cover)
in cedar glades in the Ozarks of southwestern MisLoealK donunaut grasses included A. gerardn, H. rurtipciiduhi. V nr^,iitini. S>>;iia.<lriim nit
tans, Sporobolus heterolepis (A. Gray) A. Gray,
Tridens flavus (L.) A. Hitchc, and the C, summer
annual Spurohohis iic^lccliis. Ilcdyolis m^ritaii* was
the itio-t nop..M ml Inrl-i ...n- In .1 l\'ln,s mo
matica the most common shrub, and Juniperus virginiiinti !'!<' most > oruiuoi, Iree < )lhei t\ pical \\ood\
speeies included Bumelia lanuginosa, Cotinus
ohoidtas. Ihti.s;>\i,>* > ai:j >>. in l. ll<;\ I,; :!<,; Walt..
and Rhamnus caroliniana Walt. Hicks's (1981) results of a vegetational analysis of seven stands of
open cedar glades with < 30% woody plant canopy
>, < : !stages 1 and 2 in Steyermark s scheme of
xerareh succession I., a -aigai maph w 1 ii 1 oak climax) in the Hercules Glades Wilderness Area in
southwestern Missouri were quite similar to those
of Kucera and Martin (1957). Schizachyrium scojminnii was tin di n in ml spe. ics. an I //. ni^tinins.
Rhus aromatica, and /. virginiana were the most
important herbaceous di. ol. shrub, and tree, respectively (Table 1). Schizachyrium scoparium had
the highest percent importance value (%I.V.) in all
seven stands sampled by Hicks.
Hall (1955) determined frequency of herbs +
seedlings and of sprouts of woody plants 0.27 m or
I
' ' lght and the number of Junipi
" ma seedlings/sa ings in an open dolomite glade
in the Missouri bolanieal Garden's Shaw Arboretum, near the north
tn
I -! I of the Ozark Pla-
Baskin & Baskin
Species
9H.V
Scliizachyriuni scoparium (Michx.)

Nash
// ,' . nigricans (1 am 1 1 osl>
Sporobolus neglt in % h
Carex sp.
LOO
100
KM)
Panicum virgatum L.
LOO
L0.47
9.47
7..i7
7.:'o
6.40
thogynus Michx.
LOO
5.10
2.57
\mlropugon gerardii Vit.
1.75
1.51
sa Torr.
Sporobolus heterolepis (A. Gray) A.
Gray
Palafoxia callosa (Nutt.) Torr. &
A. Gray
iltalhanus Roemer &
Schultes
H liottoj iiim U ncllitin (Null.) I'orr.
Oenothera macrocarpa Nutt. subsp.
Dalea purpurea Vent.
>
ip
Berchemia scandens (Hill) K. Koch

\mlmchnc phvllnntlwides (Nutt.) J.
Coulter
Mimosa quadrivalvis L
Vitis aestivalis Michx.
< otnus (hummondii C. Meyei

Quercus prirwides Willd.
HERBS
1.44
71
1.41
86
1.51
86
86
1.11
teau. Understory species with the highest frequencies were Sporobolus neglectus (100%), Carex
crawei Dewey (90%), Schizachyrium scoparium
(80%), Hedyotis nigricans (75%), Euphorbia corollata Engelm. (60%), and Rudbeckia missouriensis
(55%). The total number of juniper seedlings in the
glade was 6694, and 99.7% of these were in the
0.46-m or less height class. Average number of juniper seedlings per m2 was 0.84. Hall (1955: 177)
stated, "The Glade is a 'prairie' association with
Andropogon scoparius [= S. scoparium] and Rudbeckia missouriensis contributing most to its aspect
and Andropogon scoparius and Sporobolus neglectus
contributing most to cover." Hall concluded that
this dolomite glade was an edaphic subclimax, as
did Erickson et al. (1942) for the dolomite glades
of the northeastern Ozarks in general.
The flora and qualitative community ecology of
limestone and dolomite glades (as well as that of
sandstone, chert, and igneous glades) of the Missouri Ozarks have been studied extensively by Nelson and Ladd (1982, 1983) and Nelson (1985). Nelson and Ladd (1982: 5) stated, "Characteristic
dominant vascular plants of these [dolomite] glades
include Andropogon scoparius, Bouteloua curtipendula, and Sorghastrum nutans"; and for limestone
glades, "Dominant vascular plants on these glades
are Andropogon scoparius and Bouteloua curtipendula" (Nelson & Ladd, 1982: 5). Nelson (1985) listed A. scoparius and B. curtipendula as the dominant
plants on limestone glades and A. scoparius, B. curtipendula, and Sporobolus heterolepis as dominants
Ver Hoef et al. (1993) quant
vegetation of 32 glades on Emir
dolomites in southeastern Mis
liiimelia lanuginosa (Michx.) I'cis.
glades i.e., 10- 10

li
= 31.6. Other important species on the dolomite
glades were Andropogon gerardii, Calamintha arkansana, Carex meadii, Coreopsis lanceolata L., Echinacea pallida, Fimbristylis puberula (Michx.) M.
Vahl var. puberal, '.
i
ms, Liatris aspera
Mi. I;\ , l.intri\ c\lindniccii Michx.. Punicum ririinturn, Rudbeckm i
.. > -.inurn terebinthinaceum Jacq., Smilax bona-nox L., Sorghastrum nutans, Sporobolus clandestinus (Biehler) A. Hitchc,
and S. niginijlorus. The most impel lanl u K >)cies on these gla
i '
M nrginiana, Bumelia lanuginosa, Diospyros virginiana, Pinus echinata Miller, Quercus prinoides Willd., Q. stellata
Wangenh., and Ulmus alata.
Keeland (1978) quantitatively sampled the vegetation of 13 calcareous glades in the Ozarks of
northwestern Arkansas. He recognized four general
community types, which in an apparent sueccssional sequence are: i 1 | grass atnl cedar; i'l) cedar: {'M
cedar-hardwood; and (4) hardwood. Keeland (1978:
12) described the grassland-cedar type as "... a
grassy slope with a few scattered woody species."
Further, it ". . . is the typical Ozark cedar glade as
described by Hall (1955) and Kucera and Martin
(1957) in Missouri and Hite (1959) in Arkansas"
(Keeland 1978: 9). For the representative stand of
this typ describi I b} Keeland, Juniperus virginiana and Quercus stellata were the most important
overstory tn es, Rhus glabra L. the most important
shrub, and Schizachyrium scoparium the most important herb. Overstory tree basal area on this cedar glade was low, ca. 4.8m /ha. S
parium also was the most important species in
limestone cedar glades quantitatively sampled by
Logan (1992) in the Buffalo National River area in
the Ozarks of northwestern Arkansas (Table 2).
Skinner (1979) placed 0.01-m2 and 0.1-m2 quadrats around indii lual plants I the Ozark cedar
glad* endemic Penstemon cobaea Nutt. var. purpureus Pennell, Centaurium texense (Griseb.) Fern.,
ind Stenosiphon li ifo/iu ( Nutt.) Heynh. to determine species associates (as well as other site liaraclerislics) of these ilut rare plant spu cies in lirncrtoi
glad ofth< outhwestern Missouri Ozarks.
,S/..-,w./.,.//,s if\J,;-li;s had the hl-hc-l |i.-tt.-lil .i. currence in quadrats of both sizes placed around
Penstemon and Centaurium, and Schiza \
scopariun had thi highest percent occurrence in
those of both *-i - pi I .1 m i lid V , ,, . ; Ilt
which giows m dcc|ici soil (15.7 6.1 cm, mean
SD) than Penstemon (10.9 5.6 cm) or Censcoparium was considerably higher in the 0.1-m2
than in the 0.01-m2 quadrats: 22 vs. 5, 37 vs. < 5,
Schizachyrium scoparium
(Michx.) Nash
Juniperus virginiana L
Helianthus hirsutus Raf.
Andropogon gerardii Vit.
Quercus stellata Wangenh.
Ulmus alata Michx.
Quercus prinoides Willd.
imifusa (Raf.) Raf
Dalea purpurea Vent.

!,!,,., , "..,. i ,
i ,iui
i, ..'.' / llii
(Mi< h i
MacMillan ex Robins. & Fern.
Xhiindaiicc scale from I to .r. 1 = rare (onh

two individuals present): 2 = occasional; 3 = fre
common: and ."> = abundant (widespread with h
and 59 vs. 16 for ,

Stenosiphon, res]
fh
rease in percent
occurrence of S. neglectus with increase in size of
quadrats was less dramatic: 46 vs. 32, 58 vs. 33,
and 11 vs. 10 for Penstemon, Centaurium, and
Stenosiphon, respectively (Skinner, 1979).
In a dolomite glade in the Ozarks of southeastern
Missouri, two contiguous 7 X 7-m sample plots
within a whole-glade sample unit of 100 contiguous
7 X 7-m plots dominated by Schizachyrium scoparium and classified as "glades" (i.e., open glades)
were divided into 200 70 X 70-cm plots (Ver Hoef
et al., 1993). At this small scale of sampling, the
glade was divided into rocky glade, shallow soil
glade, glade, and deep soil glade zones. Sporobolus
vaginiflorus was the dominant species in the rocky

glade and shallow soil glade zones, and S. scoparium in the glade and deep soil glade zones (Ver
Hoef et al., 1993). However, in two other dolomite
glades in southeastern Missouri sampled by Ver
Hoef et al. (1993), as described above, S. vaginiflorus was not an important species.
Results of studies by Skinner (1979) and Ver
Hoef et al. (1993) support a statement made by
Kucera and Martin (1957: 290) in their study of
glades in the Ozarks of southwestern Missouri:
"Andropogon scoparius [= Schizachyrium scoparium] was the principal dominant; Sporobolus neglectus was generally frequent and locally abundant." Hall (1955), Hicks (1981), and Logan (1992)
also found that either Sporobolus neglectus or S. vaginiflorus was a relatively important species in the
Ozark glades they studied. Nelson (1985) listed S.
neglectus as a characteristic plant of dolomite
glades, but not of limestone glades, in the Ozarks
of Missouri. Thus, both quantitative and qualitative
locally dominant within the larger prairie-like community on limestone and dolomite glades in the
Ozarks. As such, cedar glades of the type described
for the southeastern United States (Baskin & Baskin, 1999) occur in microhabitats within xeric lime
stone prairies of the Ozarks.
Schizachyrium scoparium also is the dominant
plant in Ozark glades in terms of dry mass producannual herbage production on glades ungrazed for
4 and 21 years was 312.2 and 241.5 g/m2, respectively, according to a study by Buttery (1960). Production by S. scoparium on these two exclosures
(the term used by Buttery to mean areas fenced off
to prevent cattle grazing) was 175.2 and 112.3 g/
in. respectively, and by Sporobolus neglectus 24.7
and 7.9 g/m2, respectively. In the 4-year exclosure,
production by Andropogon gerardii and Sorghastrum nutans was 52.2 and 34.8 g/m2, respectively,
and in the 21-year exclosure 29.2 and 74.7 g/m2,
respectively. Thus the C+ perennial grasses 5. scoparium, A. gerardii, and S. nutans produced 84%
and 89% of the total herbage on the 4- and 21year exclosures, respectively (Buttery, 1960). Regarding herbage production on grazed glades, Buttery (1960: 235) stated, "In 1956, as now, the
glades outside the exclosures were producing about
400 pounds of oven dry herbage per acre [44.9g/
m2], mostly the less desirable baldgrass [S. neglectus] and black-eyed Susan (Rudbeckia hirta L.) with
a scattering of the more desirable little bluestem
(Andropogon scoparius Michx.) and Indiangrass [S.
THE MIDWEST
been reported in Wisconsin, Illinois, and Indiana.

S h :achyrium scoparium was the most prominent
ground-layer species in what Curtis (1959) called
cedar glades in Wisconsin, with a presence of
100% and an average frequency of 38%. Other
species in tin urouml lavei ,\ ith relatively high values for presence and average frequency were the
C, herbaceous perennial forbs Aquilegia canadensis
L., Anemone cylindrica A. Gray, Dalea purpurea,
Tradescantia ohioensis Raf., Euphorbia
Arenaria stricta Michx., Solidago nemoralis Dryander, Antennaria neglecta E. Greene. Vioi pedata
L., and Scutellaria leonardii Epling; the C4 perennial passes Andropogon gerardii, BouteloUQ hirsute
Lagasca, and Bouteloua curtipendula; and the G,
perennial grass Koeleria pyramidata (Lam.) P.
Beauv. (Curtis, 1959: table XVI-10, appendix, p.
573). The most important tree species was Jwupe
rus virginiana (Curtis, 1959: table XVI-11, appendix, p. 574).
.S - ... \rium scoparium had a frequent \ of HO100% in 30 of 32 limestone glades sampled by Kurz
(1981) in Illinois. Other important grasses were the
perei nials Bouteloua curtipendula, Sorghastrum
nutans, and Sporobolus aspera (Michx.) Kunth. The
important forbs were the CAM leaf succulent Agave
virginica; the C, perennials Aster obit
Brickellia eupatorioides (L.) Shinn., Echinacea pallida, Euphorbia corollata, Hedyotis nigricans, and
Physostegia virginiana (L.) Benth.; and the C, summer annual Croton monanthogynus Mich- S
chyrium scoparium also was the most important Bpecies in the limestone glades of sou the:
studied by Heikens and Robertson (1995).
Limestone glades have been reported from five
counties in southern Indiana (Aldrich et al., 1982;
Bacone et al., 1983; Homoya, 1987; Maxwell,
1987), and they obviously are dominated by perennial prairie grasses. For example, referring to a
limestone glade in Perry County, Bacone et al.
(1983: 368) stated, "Indian grass (Sorghastrum nutans), big bluestem {Andropogon gerardii) and little
bluestem (A. scoparius) are common grasses.*1 Referring to two cedar glades in Clark County, Maxwell (1987: 413) stated, "Little bluestem dominates
both glades as a xeric, bunch-grass surrounded by
patches of rocky pavement."
The Ozarks and Midwest limestone and dolomite
-cribed above are similar vegetali ' li i,
Table 3. Average percent frequency of nat

taxa in 147 1 X 1-m quadrats in five stands of *
rie vegetation on the Peebles dolomite in Adam;
Ohio. Only plants with a frequency of >20% i
(calculated from data in Braun, 1928).
component of the vegetation of limestor

Indiana (Aldrich et al., 1982; Bacone e
Homoya, 1987; Maxwell, 1987).
MIDWEST GLADES
/.'.
,/ (Nees) Lindau
Silphium trifoliatum L.
Bouteloua curtipendula (Michx.) Torr.
Thaspium sp.
Pycnanthemum flexuosum (Walt.) Britton,
Stems & Poggenb.
s //,- !<> plattensis Nutt.
Sorghastrum nutans (L.) Nash
Comandra umbellata (I I Nutt.
29-8
Andropogon gerardii Vit.

/,.:;.. ophru (A. Gray) Fern.
Delphinium exaltatum Ait.
what Braun (1928) called xeric prairies on Silurian

Dolomite in Adams County in southern Ohio. Here,
prairie grasses, primarily Schizachyrium scoparium,
also are the dominant plants (Table 3). Interestingly, Braun pointed out that although there is some
overlap in species composition between the xeric
prairies of Adams County and the cedar glades of
the Nashville Basin, the vegetation is different.
Neither annual species of Sporobolus nor of other
dar or limestone glades that have been sampled
quantitatively in Wisconsin (Curtis, 1959)
nois (Kurz, 1981; Heikens & Robertson, 1995)
However, in one of the xeric prairies, Agave Ridge,
on Silurian dolomite in Adams County, Ohio,
pled by Braun (1928), 5. vaginifiorus had <
quency of 68% in 25 1-m2 quadrats. The
of this prairie were Schizachyrium
(100% frequency) and Bouteloua curtipendula
(84% frequency). Braun referred to Agave Ridge
and one of the four prairies she sampled on Peebles
Dolomite as being more xerophytic than the other
three. However, the average frequency of S. vaginifiorus on the five Peebles dolomite prairies was
only 14.8%. Neither is S. vaginifiorus an important
Martin (1955: 106) stated that ". . . even the

thin-soiled areas [in the Ozarks of southwestern
Miss HI -i arc being invaded by eastern redcedar
(Juniperus virginiana), winged elm (Ulmus alata),
and associated drought-tolerant trees." Using 1938
and 1975 USDA aerial photographs showing limestone and dolomite glades in southwestern Missouri, Kimmel and Probasco (1980) found a dramatic
decrease in glade area with 0-15% woody cover
and
corresponding increase in glade area with
50-100% woody cover. Lowell and Astroth (1989)
used USDA aerial photographs to study natural
succession of glades to forest in the Hercules
Glades Wilderness Area (southwestern Missouri)
from 1938 to 1986. They found that "Even those
areas most favorable for glades [Gasconade soil,
305-365 m (a.m.s.l.), south or southwest slopes]
continue to convert to forest" (Lowell & Astroth,
1989: 78). The area most favorable for glades and
occupied by glades decreased from about 285 ha
to about 200 ha (30%) via conversions of glade land
to forest (see fig. 3 in Lowell & Astroth, 1989).
Using 1955, 1966, and 1984 aerial photographs,
Ver Hoef et al. (1993) also showed that the sizes of
dolomite glades in the Ozarks of southeastern Missouri had decreased due to woody plant invasion.
Kimmel and Probasco (1980) concluded that the
most important reason for the increase in woody
plant cover on open glades between 1938 and 1975
was that the U.S. Forest Service had not used fire
to manage glade (cattle) range. Lowell and Astroth
(1989: 78) thought that their study ". . . appears to
support the theory held by some ecologists (USFS,
pers. comm.) that the glades are not a naturally
occurring ecotype[?] which can maintain themselves independent of fire and/or human intervention." Likewise, Ver Hoef et al. (1993) attributed
woody plant invasion into calcareous glades in
southeastern Mi- urn u fin - ippression. Fire freigh in the Missouri Ozarks in preset(Guyette & McGinnis, 1982), and fire
probably played an important role in the origin and
lestone and dolomite glades in
According to Curtis (1959), cedar glades in Wisconsin: (1) may have originated by invasion of redcedar into a dry prairie on sites protected from fire;
and (2) would in time succeed to oak forest.
Volume 87, Number 2
Heikens (1991) speculated that, in the absence of

fire, the perennial grass-dominated limestone
glades in southern Illinois would succeed to barrens ("savannas"! ,111.1 lln-n I'. Inn -I.
By studying aerial photographs of limestone
glade areas in southern Indiana, Aldrich et al.
(1982) and Bacone et al. (1983) determined that
Aldrich et al. (1982: 484) stated, "Aerial photographs document the continuing shrinkage of these
glades [in Harrison County], as they were nearly
double their present size in the 1940s." Bacone et
al. (1983: 372) stated, "The aerial photographs
show a remarkable decrease in size [of the forest
openings in Perry County] in the last forty years
due to encroachment of woody species."
Braun (1928: 425) thought the xeric prairies in
Adams County, Ohio, ". . . antedate settlement by
white man and are undoubtedly primary." However,
using USDA aerial photographs taken in 1938,
1950, 1965, and 1971, Annala et al. (1983) and
Annala and Kapustka (1983) found that prairie has
succeeded (is succeeding) to forest. For example,
prairie openings in the Lynx Prairie Preserve,
where the soils are "shallow and poorly developed"
(Annala et al., 1983: 22), covered 47% of the Preserve in 1938 but only 16% in 1971 (Annala et al.,
1983; also see Fore & Guttman, 1996). Based on
lack of difference in opal (phytolith) mass between
soils presently under prairies and those presently
under cedar-hardwood forests on dolomite in Adams County, Boettcher and Kalisz (1991: 127) concluded that ". . . the long-term vegetative history
has been generally uniform over all areas on dolomite regardless of present occupancy by prairie
or forest." Further, ". . . the distinction between primary and secondary prairies has little meaning
since prairies only occur on areas of dolomite, and
prairies and forest have alternated over time on
these areas" (Boettcher & Kalisz, 1991: 127).
.
KKM\
The vegetation of limestone and dolomite glades

in the Ozarks and Midwest is dominated by C4 perennial prairie grasses (primarily Schizachyrium
scoparium), and burning or some other method for
removal of woody plant invaders is required to prevent succession to forest in these rocky, calcareous
openings. Thus, they differ from cedar glades in the
southeastern United States, in which the dominants
are C, summer annual grasses (primarily Sporobolus
vaginiflorus), and
management (Baskin & Baskin, 1999). The &
ture of the vegetation of the limestone and dolomite

glades in the Ozarks and Midwest is much more
similar to the xeric prairies on Silurian dolomite
described by Braun (1928) in Adams County, Ohio,
;ind to IIH- .\(-rii |-rairi>s <m Mississippian limestone
described by Baskin et al. (1994) on and adjacent
to the Kentucky Karst Plain, than it is to what traditionally has been called cedar glades in the
southeastern United States. Kuchler's (1964) vegetation map of the United States shows the same
vegetation type for cedar glades in the Ozarks and
in middle Tennessee-northern Alabama. However,
ample evidence is available in the literature to
show that the glade vegetation of these two regions
is quite different. Thus, we suggest that the rocky,
3, anthropogenic, prairie-grass-ii sin i: i< !
o|)i'i in-s in tin Ozarks ami Midwesl |.<-railed xerir
limestone prairies, in contrast to cedar glades,
which are an edaphic climax dominated by Ct summer annual grasses.
.Hi r :lm. < il.-.l
Baeolle K \1. I).

<!2
roc. Indiana Acad. Sci. 91: 4B0-185.
Annala, A. K. <S L. A. Kapustka. I9B3. II, -...-..,
Ius|.,r, ol loresl ere-oaelimetil ! -. \eral rclirt piailio
of the edge of Appalachia preserve system. \ L i iComiU. Ohio. Ohio J. Sci. 83: 109-114.'
, J. D. Dubois & L. A. Kaputska. I<. Prairies
Aldrich. J. EL, J.
CHIMIN. Ohio. Ohio.I. Sci. 83: 22-27.

Baeone. I A.. L A. Casebere & M. D. Hutchison. 1983.
U.'liP- l I , . - .i ! ' ,.\ I I
ilhlMM ll - I ]
diana. Proc. Indiana Acad. Sci. 92: 367-373.
Baskin, J. M. & C. C. Baskin. 1985. Pile ryle ,..-..logy
I linn il pl in) -|- . -,(,-. ii h ,-if n I i . I -i i. ;.l W !
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Junk. Dordi
&
. 1999. Odi
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1 iiiK'd Mates. Pp. 206-219 in R. C. Anderson, J. S.
r'rjlisl,i\ J Vi IJaskiiile.nioisi.Si.wiiin.-i-.. Ram-ns. and
|{ M '- On. , , 'l.ni I .in iiiniii
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111.
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Boettcher, S. E. & P. J. Kalis/.. 1901. The prairie ol the
P. I .in e Braun Preserve, Adams County. Ohio: \ soil
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Braunselmeig. S. H., E. T. Nilsen & T. F. Wiel.oldi |<x><>
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in Ii
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C. Anderson, J. S. Fralish & J. M. Bask,,, .
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l{
l<>;
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>-
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d, B. D.
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,
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', ' , ' ', '
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v. Biol. Notes No. 15.
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v.-diiigs ol Ihc siMl, North
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|();,').
G-eiahonal history of the Ozark forest.
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ihc Interior. Midwest
Region. Omaha.
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Cooperative Agreement C \<>(,|!l 8 8008.
N PS
Mall relifetime
Purchase
I'A. ll;ill-f
iuary2(XK) was 5.(M)2.1-'--: :.'... MHO
296
Annals of the
The Garden's herb; Ilium is closely associated will l its database m anagement system. TROPICOS. The charts below
n.lar year 1999 and as ve
summarize some of Ule statistics from TROPICOS t
the specimen records in TROPICOS are primarily based on MO specimens, meaning llial about twe.ilv-four percent of
lty-nine percent of the vascular plants (an increase
the bryophytes (an in< rease of about four percent ove
of about two percent) in the herbarium are now computerized, with an overall total ol about Iwenlv \U\ percent Ian
percent).
, !'; )
!WI,
iTO
""
TKopims records-1999 additions

Bryophytes
ascular Plants
18,638
1,290
2.1.T,
55< t
63
1.343
Specimen!,
Types
Bibliography
95,617
25.016
18,828
28,81<
18,660
2.333
Total
114,255
26,306
20,963
29.366
18.723
.,.676
rROPICOS rec ords-Year-Knd 1999 Totals

Bryophytes
Specimens
79.489
67.181
Ni >' i1 ',-.|f .i h. nTypes

Ulhllo^tnpiix
Specimens in herbari um
ascular Plants
Total
30.061
o.;!2(,
20,606
1,339,708
747.611
370,118
, K),385
2 15.1.-.7
58,025
1,419,197
844,798
1,202
777.376
231.983
78,(>31
330,1 L8
4,672,010
.5.002. 2ii
In TROPICOS. I.tcrature
e completion ol I I ,', ' ', -., ('.',, 1/ ." (,> .< .-, n
1 acceptance of the 58,000 valid names of moss :
in lilt- Rrv opinio Herbaiiuin :, ill he adju-li-<: to
I 13,000 species are re

dard.
- Marshall
! :,n .!.,, .10. :>(MMI
Orchids
Guatemala. Species are listed in alphabetical order
Orchjdsof Guatemala:
together with synonyms or species names used in
I ORCHIDS
older treatments, and their geographic, elevational,

and habitat distribution in the country are
UATEVIALA
Checklist
described. Where identification of species new to
Margaret A. Dixi
Guatemala may be difficult, distinguishing
Michael W. Dix,
characters are briefly described. The list, based

on extensive field collections and herbarium
m
This study
represents a o
recognized sp
Icones Pleurothallidinarum
XVIII: Systematics of
Pleurothallis
XIX: Systematics of
Masdevallia Part One
Carlyle Luer, MBG Press. 1999.
Carlyle Luer, MBG Press.
Icones Pleurothallidinarum^ contains section
Available March 2000.
Pleurothallis subsections Antenniferae,

Longiracemosae, and Macrophyllae, and
parts to treat the genus Masdevallia. It begins

with a 10-page introduction to the genus with a
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occupying about one-fourth the volume of the book.
basic concept outlined in lcones-2, but with
The species treated are characterized by a usually
significant revisions. Part One consists of only one
many-flowered, racemose inflorescence, which is
subgenus (Polyantha) of two sections (Alaticaules
reduced to a single flower in a few species. Many of
and Polyanthae), which altogether contain 104

species, about one-fourth the total number in the
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Miss.),.
Botanii
C.inlc.
' Mdnira Giussam
Marshall R. Crosby
Annals
of the
Missouri
Botanical
Garden
2000 fr
Volume 87
Number 3

at vvvvvv.mobot.org (through MBG Press).
Editorial Committee
Editor,
Managing Editor,
Diana Gunter
Associate Editor,
Aida Kadunic
Senior Secretary
Gerrit Davidse
Roy E. Gereau
Peter Goldblatt
Gordon McPherson
P. Mick Richardson
Barbara Mack
A dm in istrative Assistant
Henk van der Weiff

Ihsan A. Al-Shehbaz
s the requirements of ANSI/NISO Z39.48-1
Volume 87
Number 3
2000
Annals
of the
Missouri
Botanical
Garden
THE REDISCOVERY OF A
MALAGASY ENDEMIC:
TAKHTAJANIA PERRIERl
(WINTERACEAE)1
George E. Schatz*
o\er> ol Takhlujania prrrirri (Capuron

/interaceae in the Al'riea/Madngascai r,
For most of the 2()lI

>
(Gapunm) Baranova & J.-F. Leroy stood as the Holy
Grail of Malagasy botany. Numerous expeditions
searched in vain h> !
b- living member of the ancient family Winteraceae in the Afri< > \] ii i. i-., .i; ii L ! i
i' i M ' i iim.inui Special
Ko
i \1 (I i
ar. where, in
1909, Henri Perrier de la Bathie collected the only
known specimens. With hundreds of square kilometers of intact forest protected within the Manongarivo reserve, the species must surely still exist
there! Nevertheless, the dozens ol botanists who as-
:, ;-)()
il
Ml \ntsatrotro to
meter elevation cited on Perrier de la Bathie's
handwritten labels, passing through what is infamously acknowledged to be the most dense zone of
terrestrial leeches in all of Madagascar, have all
(ailed to relocate Takhtajania.
By the spring of 1997, I commenced work on the
Generic Tree, Flora of Madagascar (Schatz, in
press). The Tree Flora will serve as a revision and
expansion of Rene! Capuron's 1957 Essai
d'Introduction a I'Etude de la Flore Forestitre de
Madagascar, a work existing only in mimeographed
\l the Missouri Botanical <,anlrn. I Hi.ink I" II. K.iven and I'. I'. I.nun II lor til.- o|)l
flora, and V. Hollowed and P. I'. bowrv II for helpful comments on the manuscript. In
have always extended the most cordial hospitality during m> \ isils to the l.alioratoire de
fieldwork was conducted under collaborative agreements between the Missouri botanical Garden and the bare
el Zoologique de Tsimba/.a/.a and the Direction de la Becherche Forestiere et Piscicole. FOFIFA. Antanana
agascar. Fieldwork would have been impossible without the assistance ol the World Wide Fund for Natu
thanks go to Jean Marc Garreau and Desire Bavelonarivo at their Andapa office. I gratefully acknowledge
extended by the Government of Madagascar (Direction General,- de la Gesti.m des bessources Forestieres)
lale pour la Gestion des Aires Protegees. This research was conducted with -upport Iron l.S. '
e Foundation grant. 1)1 I? ':!'!. |<> .,,! I)FH-X)27()72. and gnuils Iron, the National Tropical Bot
i Botanical (iarden. P.O. Box 299, J
OUR]
BOT. GARD.
87: 297-302.
form. Although it would be another six years before

lie des. iibed Hiilihm ;i<Tii,'t' j " 'lal.hl'i/ati.'ii !<!>
eri] (Capuron, 1963), by 1957 Capuron had already
determined that Perrier de la Bdthie 10158 constii i
i
record oi the family Winteraceae in Madagascar, including a description of
the family in his Essai, as represented
M
gascar by "In sen I ome el ime seul< .-spree: I'.uis
bia Perrieri R. Cap." (p. 96), with the furth< I note
that "La famille est nouvelle pour Madagascar;
l'espece provient du massif du Manongariv*
(p,
104). In Paris during March of 1997, I decided to
write the description of Tahhtajania for the Tree
Flora, and, that to do so, it was high time that I
examine the type specimen. After several inquiries,
two sheets of Perrier de la Bdthie 10158 were located in the office of Thierry Deroin. He, with the
late Jean-Francois Leroy (1915-1999), had recentl\ slud ed tin- \asculalure oi 11 < m;ii\ utilizing the
type material (Deroin & Leroy, 1993). Over the
course of several days as I wrote my generic desoriplion, I stared |>et indioalb al (hose enigma!!.
specimens collected nearly 90 years earlier. While
wondri eg uli.llie. |h< -pen.-- might still exist. I
had to conclude my treatment of the genus with the
msallsl; etor> stalemolll lb l! tle>| (. I ameroils al
en i-
ad not been seen again. Two
months later, back in St. Louis, with the images of
those type specimens still very fresh in my mind's
eye, I opened th
-papers of a colmade in 1994 from the Anjanaharibe-Sud Special

Reserve by the Malagasy collector Fatija Ra-oa
vimbahoaka, and, eureka, there it was! In an instant, I realized that Tahhtajania had indeed been
seen again, but not where we had been looking lot
it. Set into motior
of events culminating in the following papers.
FROM "INDET." TO POLITICAL CARTOON: ONE
SPECIES' HISTORY
The first documented human contact with Takhtajiiiim occurred in Ma\ I'M)*) on the ManongariYo
Mas-il ID northw. -lern Madagascar, a chance event
preserved for all time as two herbarium spe, mien*
{Perrier de la Bdthie 10158) deposited at the Museum Nationale d'Histoire Naturelle in Paris. Both
Capuron (1963) and Leroy (1978, 1993) transcribed the locality data on Perrier de la Bathie's
handwritten label as "Massi
the same trip to 2000 m, despite a maximum altitude for the massif of 1876 m at the summit ol Mi.
Antsatrotro. Given this, and that Takhtujania is now
known to range from 1100 to 1550 m altitude at its
-a cuud known iocaii!\ linn llie \ti|anahai ibe Sud
Special F
rtiall) explain why it
I - n - I1
ii
i Man mgarivo: we may
well have been looking for it at too high an elevation! Accompanying the two type sheets enclosed
within a red Type folder are Perrier de la Bathie's
field notes. These were reproduced in full by Leroy
(1978), and reveal that Tahhtajania first entered our
collective botanical consciousness as a "famib in
del.""; based upon it- eai. -iam.i,, and man rhai
acteristics. Perrier suggested both "Annonaceae?"
and "1 lilleii ;> . aev
i T, ':>!'< '</!." be I .>. II _> tin
-in
gle carpel to correspond to a carpel of a flower with

free carpels. A later annotation (with a
preprinted partial date of "193 ," the specific vear
bit i>i ..Li affixed to one of the sheets by J. Ghesquiere, a specialist in Annonaceae, rejei i
that family by noting simply "Magnol.," perhaps as
an ordinal placement. Leroy (1978) cited undated
aid Di -. h H Hi tnh tl lit! iugh he may have
been the first to recognize the correct lamiU place
ment, these notes no longer accompany the type
specimens. Nevertheless. Tahhtajania remained
nameless lor 54 years until Capuron (!'>(..!) lot
malb des<nbed it as Huhhia jn-rrieri. Such a lag
I me bi Iwe. '( held colli fin I arid It- actual deseripally slow pace of botanical studies.
Having finally received a name, Bubbia perrieri
soon became the focus of additional studies on pollen (Straka, 1963; Lobreau-Callen, 1977) and leaf
anatomy (Baranova, 1972; Bongers, 1973). These
-Indies report. .1 . n pale oi hi. hoioii ... ulpah (In
h la ûlcate) pollen apertures and an anomocytic stomatal cell arraiigemenl. both features
auoma oa- *ilhu hie \\ aiha ea> hi. I!:MI ennii: on I- corroboial. il In '.MI m K. aim- ..: Samp- m.
respecluelv). Stimulated b\ these novel findings,
Leroy (1977) e\p a .<l ir i<
monS obser\alion
ol a brlobed -hi/ana aa l!nl>l,i ;,;>,;> and dariugb
ulai ovary comprised of two united carpels; he also presciently
ngg.
'
llaceae. For Leroy (1978), such radical differences clearly merited
ilisiincl I igher-taxon status, and thus a new genus
was ,le-,,.|l.ei /;,,''. ! >>,>)!>?! < .1: U f >t I !.!'< ,lt!|.'
Tahhtajania perrieri (Capuron) Baranova & J.-F.
Leroy, and the new genus became the type of a
wholly new subfamily Takhtajanioideae. When
Vink's (1978) studies of the ovary concurred with

his bicarpellate hypothesis, Leroy felt sufficii otrj
vindicated against Tucker and Sampson's (1979)
cautionary skepticism in the journal Science that
his enthusiasm knew no bounds. In 1980, he raised
I
i ! family Takhtajanioideae to the rank of family: Takhtajaniaceae, indeed, from a in iK ind< i
to a family apart!
Meanwhile, numerous botanists failed to relocate
ia at the Manongarivo Special Reserve.
Capuron collected there extensively in 1954, including the upper slopes of Mt. Antsatrotro, but
then he apparently never returned. In 1966, he
stayed closer to the main road from Maromandia to
Ambanja that passes ca. 10 km to the west of the
Reserve boundary, and fully 25 km west of the upper slopes of Antsatrotro. Vink (1978) recounted
that Capuron told him that the type locality was
completely deforested, a curious remark given the
vast area of intact forest present still today (Gautier
et al., 1999). Several years later, Josef Bogner (M)
searched for Araceae on the southern slopes of Antsatrotro north of Bejofo, and the late Al Gentry
walked in from the road to as high as 300 m altitude in 1974. Then, at the behest of Leroy, Raymond Rabevohitra (TEF) once again searched the
upper slopes of Antsatrotro in 1979, but found no
trace of Takhtajania. Beginning in May of 1989
(Schatz, 1989), the Missouri Botanical Garden has
conducted numerous expeditions to Manongarivo,
and since 1994, Laurent Gautier (1997, 1999) has
headed Geneva's ongoing inventory efforts there.
For all who made the arduous pilgrimage to Manongarivo, Takhtajania would remain elusive.
Some 150 km to the southeast of Manongarivo,
also in 1994, Fanja Rasoavimbahoaka began work
as a local collector at the Marojejy Strict Nature
Reserve (now a national park) i
Sud Special Reserve in conjun
GAP (the National Association fr
of Protected Areas)/World Wide Fund for Nature
protected areas project. That May, he ascended a
trail used by local gem and crystal hunters leading
west from the abnialui -,I ill t-,.
Vndranotsarabe,
which had served as a camp, gravel depository, and
water source during the building of the road connccting \i!"! ip.i ami Bralari ui.i In il Inserts tin \n
janaharibe-Sud Reserve. Unbeknownst to him, he
lected /..'. u a in flower (Fig. 1; additional
ii i i - <>' Vakiitajunia n I
iml on the web at
http://www.mobot.org/MOBOT/Madagasc/winterac.
html), exactly 85 years to the month after Perrier
de la Bathie's original collection from Manongarivo.
Later that same year, a multi-disciplinary study of
altitudinal variation, sponsored by WWF and head-
ed by Steve Goodman (1998), used this same trail

to access the summit of Anjanaharibe-Sud. In fact,
they established their 1200-m "Camp 2" right
amidst the Takhtajania population. Expedition botanist Desire Ravelonarivo collected fruiting Takhih in September and November, and all
of the expedition members must have walked by
Takhtajania numerous times along the trail.
This brings us forward to that fateful day in May
1997, when I opened the newspapers containing F.
bahoaka 303. The first person to whom I
showed the collection was Peter H. Raven, who had
launched MBG's activities in Madagascar several
decades earlier, partly in hopes of finding Fnhhii,
jania again. He suggested that I immediately prepare an announcement of the rediscovery for the
journal Nature (Schatz et al., 1998). I then dispatched e-mails to Paris and Madagascar, sounding
the call to action. Several weeks later, members of
our Malagasy staff including Sylvie AndriamboloI" i
i iarmie Raharimampionona, and Pierre Jules
("Cora"} Kakoiema a/a a< i i mpai ii'il Desire hark
to the Takhtajania locality at Anjanaharibe-Sud,
photographing its flowers ami mil. .im<: the first lot
of specialized research materials that would be utilized in the following new studies. The following
month, a specimen for the Komorov Institute in St.
Petersburg was presented to Armen Takhtajan at a
special birthday celebration for him in St. Louis;
born just one year after Perrier de la Bathie first
collected Takhtajania, he had waited 87 years for
its rediscovery.
Since then, Takhtajania has been revisited numerous times. The journey from Andapa to Andranotsarabe by 4-wheel-drive vehicle takes three
hours, if it has been relatively dry the previous
days. However, subjected to over 3600 mm of rainfall per year, portions of the road are deteriorating
rapidly, and landslides threaten continued access
to the population. Having arrived at the trailhead,
one must gently climb little more than 200 m in
elevation through beautiful forest. Even when it is
rainingwhich it often isthe leech population
does not even begin to compare with that of the
slopes of Mt. Antsatrotro at Manongarivo. In less
than an hour, one enters Takhtajania's realm, the
ittened ridges followed by the trail, and
the uppermost portions of the steep slopes falling
away on either side of the ridges. With its large,
glossy, dark green leaves clustered toward the apex
of vertical stem-.
ids out in the understory, its slender trunk often leaning severely
after surviving the impact of fallen debris. Extending over eleven square kilometers, this second re1 ikhtajania population appears to be thriv-
ing; Birkinshaw and colleagues (1999a) have

estimated a MI nil! itn el 12.020 imliv [duals i< pres< iithig ill
I -- - i i u li I.: ihundant seedlings.
In his 1998 New Year's address to representatives of the diplomatic community, the President of
ladag.ascar. Ihdiei Ua'siraka. urraidod TaUiidjn
nia as a national treasure that dated hack to the
time of the dinosaurs. His remarks immediately
hen the atletili
' i i imnl i< n - Minis
ters, at that time, of the Environment, and Waters
and I uresis, C. Vaohita and R. Rajonhson, respectiveK. accompanied In the D r< etors o-l l'io li.. -i'-.
Valorization, and Ecotourism at ANGAP, M. Faramalala ,ind J. llakoloai MM. 'ospeclnely, all made
the long trek to s
Shortly thereafter,
a political cartoon appeared in one of the daily Antananarivo newspapers depicting a Malag is\ \i lag
i
I i a i
' i n-! " ii(I fortune in the
first panel: "Je suis riche! Riche! Riche! . . . J'ai
. . . J'ai . . ." ("I am rich! Rich! Rich! ... I ... I
. . ."), and then in the second panel, holding a pot!
Hi
'
I ..'-, tmiu jwrricri. "".I"ai
"). Ironically. TdUildjnnid
fei i'. \e\erdio|e~s. '/.//. /' In;,: h './ out III lies to s 111 lie
piomaionlb on the pnliiit al landscape. Iia>. u g ><<
chosen a-> the em! I n I
M i i I-I u"s . xhibil at
EXPO-2000 in Hanover, Germany (during the summer of 2000), highlighting the governmentV eoni' ":' - HMi'rihle <\r\< I1 pairn' an grams.
I
lujanin has provided wonderful new research opportunities, the first results
of which are reported in the following collection of
papers. James Doyle sets the stage by reviewing the
fossil history of Winteraceae. Sherwin Carlquist
confirms die ,< --c'l. -- nature of Tdkhldjunia wood,
whereas Taylor Feild and his colleagues examine
the condition of vesselless wood from an ecophysKeexamining foliar anatomy,
Richard Keating reports mostly brachyi
i i II i
i J I a - 11
i it.- 11
riginal reports of
an anomocytic arrangement that contributed to the
initial |i.sfifi, anon oi i:en. 'i< -i ii is joi I'd! !,>,,.t'>, i
furthermore, he summarizes a unique nodal anatoii " /;/ ;i, ,
l\ lei Faidress and his coli
'
og\, by virtue of
i
.
.nforms most closely to Pseui/oK-imri , md y.\gnii>mutt, in part, due to its small,
earls -i up! n ing in\olneie .anil . : ',;! anther sacs. Il
was these two features that induced Capuron (1963)
to describe the species origin

bid whi( h is no iiicaiiled
uwn
I Furlhei
ploi nig ta il >v\< is. \ndn v\
|)oi|s| c'.amines the ontogeny of perianth pails in
Winteraceae. His comparati\e sequential dala suggest that the similarities of an early-rup nun:
volucre and perianth arrangement exhibited by
ill
-.,,_. ,,,, reflect the plesiomor(ihic slate, md !1
p il i si, i in the two genera
is non-homologous. His results further imply that
the enveloping late-rupturing involucre of Tasmannui ,iu d Dtim > s 1 .- r-.oh ! ii ! pendeiill\ in each
genus. Delving deeper into the flower, Bruce Samp. n . , II
i II , i
I L.II
i I ipcrliin-s in po|
ii of Tul
- i
i'
_ eurliei reports
to) apertures: lie also finds possible evidence lor
asynchronous pollen mitosis within a tetrad -mnla;
!
to that m Drin,
i I
Ii - i ' I"
and Bruce Sampson report embryological features
indistinct from other Winteraceae, but well distinguished from probable sister Canellaceae. Thierry
edian carpellary bundle to the lateral bundles in

aturing ovaries during fruit development. At the
tological level, Friedrich Ehrendorfer and M.
xmment a "diploidi/cd," possibly paleoletraploid. chromosome number of 2n = 36, which
can only be understood in relation to the paleopolyploidy exhibited by other Winteraceae (n = 13 to
n = 43) by presuming numerous extinction _,-.
An analysis of molecular sequence data by Ken
Karol and coll
isal and sister to
_ \\ interaceae, a result consistent with
! crov's sublamilial designation. Reported elsewhere are studies of the habitat of Tahhtajania (Birkinshaw et al., 1999b), and an assessment of its
risk of extinction (Birkinshaw et al., 1999a). Later
this year, Rivolala Andriamparany concludes his
studies of the rcproductuo facing;, o| TaUilajama
perrieri at the University of Antananarivo under the
direction of Elizabeth Rabakonandriana and Len
Thien of Tulane University.
dermis in tfie Magnohaceae and some related families.

Taxon 21: 447-169.
liiilinshau. C. I), Rawlonamo. |{. \ndriai,ipaian\. S.
Rapanarivo, E. Rabakonandriana. (,. K. Schat/ X I.. 15.
Thien. 1999a. Risepie (lVxlinction du TiilJihijiinin /></
rieri. Rapport Final I., September. Antananarivo.
. 1999b. I.'habitat <lu Takhtajania fterrirri. Rapport Final II.. October. Antananarivo,
lionners. .|. \1. I<>7'.. I pidciinal leal cliarariri- <>| llicWiiileraceae. Rlumea21: .5H1-411.
Capumn. I!. I<>57. F-sai Întroduction a I'Etude de la

Flore Forestiere de Madagascar. Inspection G^nerale
. 1903. Contributions a I'etude de la (lore de Madagascar. XI1. Presence a Madagascar d'un nouveau repnWntani (Hubhia perrieri R. Capuron) de la famille
do Winleracees. \dausonia. n.s.. 17: 373-378.
Deroin, T. & J.-F. Feroy. 1993. Sur Finterpretation de la
vascularisalion ovariennc de Tukliluwniit (\\ mteraeee-).
Compt. Rend. Acad. Sci. Paris, Ser. 3, Sci. Vie 316:
725-729.
S I. <-i '. le M.iiKin-.iiiu. (\o d ( 'ue 1 di M;i l.r- : n I
Monocotylcdonac. Documents EFB n 5, Geneva.
. 1999. Inventaire floristiquc de la Reserve Spc'ciale de Manongarivo (Nord-Ouest de Madagascar): Dicolvledonac. Dociitncnls KFM n 6, Geneva.
, C. Chatelain X M. S(>i<-lii.-r. P99. Delore-tadiachronique des deTrichments sur le pourtour de la
Reserve Speciale de MiiiimiKaruu (\\\ de Madagascar!.
Pp. 255-279 in H. Hurni & J. Ramamonjisoa (editors),
African Mountain Development in a Changing World.
<
dm.HI. S. |.-din.i i. I '><)}!. \ Moral and launal inventory

of the Reserve Speciale d'Anjanaharibc-Sud. Madagascar: With reference to elevational variation. Fieldiana,
Zool., n.s., 90: 1-246.
in \\ iiilcraecac (Magnoliales): Evolutionary implications. Science 196: 977-978.

. 1978. I in- -.oiis-lainilK- i i MI.H- i > i <, ;-
teraceae endemique a Madagascar: Fes Takhtajanioidcac. \dansonia. n.s.. 17: 383-395.
. 1980. Nouvelles remarques sur le genr.
hijuiut) (\\ intcraccae Takhtajanioideac). Ada
n.s., 20: 9-20.
. 1993. Origine et Evolution des Plantes a
Masson, Paris.
I.ohreanCaller,. I). 1977. Fe pollen du liuhbi,, /;ncn
R. Cap. Rapports palvnologiques avec les autres genres
de Winleracees. Adansonia, n.s., 16: 445-^60.
Schatz. (i. E. |98<> III, , ,
, ;,' ,, . .... ,.,,,..
aceae). Bull. Nail. Trop. Bot. Card. 19(4): 117-118.
Takhtajarua perrieri rediscovered. Nature 391: 133Straka. H. 1903. Cher .lie mogliche phylogeneh.-, lie Bedeutung der Pollen Morphologic der madagassischen
Bubbia perrieri R. Cap. (Winteraceae). Grana Palynol.
4: 355-360.
Tucker. S. C. & F. B. Sampson. 1979. The gvnoecium of
wi.Ueraceous plants. Sci.-i.e.- 203: 920 <)2 l'.
Vink, W 1978. The W mtcraceac of th- Old Wo, Id. III.
Notes on the ovary of Takhtajama. Blumea 24: 521! On the very day
i Allen Press. Madagasi n
HI
li
III
In -pt , mi. n- -nil ill h. II
in January, 1990. b\ l.io \Md\ There ua- l,i>

u
fruit! As before, I immeili.ilek dispalchc.l T mail alert to
our Madagascar office-, as well a- to die Wildlife Oonser-
l,.il,.n,ir lean.li.i ol \1BG. ha- now returned Irom the held

only three plants oi liil.lilniiiiiiii out -p.u-< I
...-.-i.
adult, one sterile adult, and one seedlinglocated ea. 0
kill nortli.-a-l ol
) in
Vrnba,,,/..,,., \\., ..!',;.'-
MOO
<
.C INI I l"l . o
I , .
'
111
'
I'-'ll
, I
'It
hility of a second, tiistinct (axon within Takh-
PALEOBOTANY,
RELATIONSHIPS, AND
GEOGRAPHIC HISTORY OF
WINTERACEAE1
ABSTRACT
n of the history of Winteraceae. Phylogenetic analyses link Winteraceae with Canellaceae. nested
1 Piperales, implying that their lack of vessels is derived rather llian primitive. The
Ylbian (Early Cretaceous) of Northern Gondwana (Cabon. Israel), are
underlain by thickened endexine but finer sculpture than modern
item-lineage leading to crown-group Wmleraeeae. I\.irl\ (.retaeemis
Afropollis and Schrankipollis, which have also been compared with Winterai-eae. are prol>al>l\ not related. The distribution of Wtilkeripollis implies that the winteraceous line originated in tropical, possibly dry, environments, like th.i-e
ol modern Canellaeeac. rather than equable temperate and upland tropical habitats like those where Wmleraeeae oeem
i Australia i
spread south into the temperate zone. <
could have dispersed to Australasia via either South America t
Oosperms, biogeography. Cretaceous, paled..:
Winteraceae have long attracted students ..I angiosperm evolution and biogeography because of
their putatively primitive morphology and disjunct
Southern Hemispl re distribution | \ustralasia,
South America, Madagascar). Emphasizing their
vesselless wood .in.
I i iplicate) carpels,
Thorne (1974) consid i
*
primitive living angiosperm family. Others (Walker
& Walker, 1984; Cronquist, 1988; Takhtajan, 1997)
argued that Magnoliales such as Degeneria are
more primitive: although these have vessels, they
also have plicate carpels, plus gymnosperm-like
monosulcate pollen with a continuous tectum and
granular infratectal
is Winteraceae
have putatively more advanced pollen shed in per-
, logeny. Tertiary, '
tectal structure. \h r
i li
i
i
us
arose in the area of Southeast Asia and Australasia
(cf. Takhtajan, 1969), Smith (1973) postulated that
Winteraccae originated in Malesia and migrated
south through Australasia and Antarctica to South
(ignition that Southeast Asia and Australasia are

juxtaposed portions of two supercontinents, Laurasia and Gondwana, which were widely separated
during the rise of angiosperms in the Early Cretaceous. Since only two species of Winteraceae occur
outside the former limits of Gondwana (Drimys
ensis L. f. in Central America, Tasmannia
piperita (Hook, f.) Miers in the Philippines), which
could be "spillovers" after South America and Australasia collided with Laurasia in the Tertiary, Winteraceae were soon offered as one of the best examples of a taxon with a Gondwanan distribution
(Schuster, 1972, 1976; Raven & Axelrod, 1974).
Paleobotanical discoveries and phylogenetic
analyses of the past two decades have shed new
light on the history of Winteraceae and other angiosperm taxa. The purpose of this paper is to review the fossil record of Winteraceae in the context
of the phylogenetic results, and thus to present an
updated synthesis of the evolutionary and geographic history of the family, as background for dis
cussion of TuLhtujanhi. Of special int. rest is fossil
America and west to Madagascar. This scenario was

challenged by the theory of plate tectonics and rec-
pollen evidence extending the wir

into the Early Cretaceous, i
, Sharma Gaponoff, Jean-Michel
"l Klse Marie Friis and an
California 95616, U.S.A.
MISSOURI BOT. GARD.
87: 303-316. 2000.
nviron-
it might also !>< the cm iromnent where loss of vessels would be least disad\antageous. Donoghue and
Doyle and Feild et al. (2000) suggested that vessel
Phylogenetic analyses have confirmed the posion of Winteraceae among magnoliids, now recogized as a basal paraphyletic grade of angiosperms
elow monocots and eudicots (the 95% of dicots
However, they
us of vesselless
wood, at least in Winteraceae.
Based on a morphological eUliMi.- analysis of
primitive angiosperms, Young (1981) concluded
that Winteraceae and other vesselless taxa are nestcil well within tin- angiosperms, so it is n
simonious to assume that vessel- arose in
.. . ins was connrmcu ,.y me auatvs.s
md Doyle (1989), which placed Magnoliales in a restricted
structure, at th<
remaining groups (including Winteraceae) united
by columellar structure. Winteraceae were linke<"
with llliciales {Illicium, Schisandraceae) and i
some trees (lauellaeeae. based on palisade exolest
a similarity of Winteraceae. llliciales, and Cane
laeeae noted by Corner (1976). Winteraceae an
III
1
had also been associated I
V:ib
I I'M-} based in part on their coarsely rctirul 1
pollen s( ulpture. and were subsequently linked 1
the morphological cladistic analysis of boeont
io.her "mnlariiv 7 WinteraceaeandCanel.aee
,,.,
'
since embolisms caused bv freezing would be restricted to one tracheid rather than expanding to fill
whole vessel. This is especially plausible for Trochodendrales (nested among lower eudicots with
vessels: Chase et al., 1993; Hoot et al., 1999; Sa-
volainen
et al., 2000), which were common in the

Late Cretaceous and Tertiary of northern Laurasia
1991) Carlquist (1983, 1987, 1988,
19%) ,,..,| S(.veral arguments against the loss
(Crane et al^
0f
vessels and for multiple origins: the parallel naadvancement trends within vessels: the im-
ture of
suit of movement from dry to mesic (Young, 1981)

or from aquatic to terrestrial habitats; the fact that
^.^ ;m> ;i|nms| ||u( m)t
lete,
lost in Ehe.
^
P
eyen [n extreme habltats;
and tne lack
/tra.
11 id dimorphism in vesselless angiosperms. Howone argument oi Uailey and Nasi (I'M I) and
^^ J{sj"^ ^hTcWteltic
plugs of Winteraceae ,
of vessels, appears to be incorrect. Feild et al.
(1998, 2000) showed experimentally that plugs do
vice to promote 111110II ol water in cloud loies! halt
iy aspects of earlier cdadistie schemes now
evision ;h a result ol 11
.
anal SeS
>
" StudieS of Partial rRNA s^ (Ham"
bwWanunc, 1992; .).e c d 1994) rooted an-
leaf venation (Hickey, 1977), with secondary veins

that are poorly differentiated from higher vein orders and loop repeatedly insidethe margin (Mickey
PPenns not ,n woody magnoliids but in paleoherbs

<" with Nymphaeales basal, as did more recent
morphological analyses (Doyle et al., 1994; Doyle,
& Wolfe, 1975). However, this may be a symplesiomorphy rather than evidence for direct relationship; similar venation occurs in Early Cretaceous
angiosperm leaves and has been considered primitive (Wolfe et al., 1975; Doyle & Hickey, 1976;
Hickey, 1977).
1996) Mm h mo,v
'
*'**"*"*' *"<<* (>f rbcL (Chase
et al
- ,W:i> l^'1''1 <>"""/'/'.//'"" at the base of
the
angiosperms. However, this rooting was quickly
suspected to be a long-branch effect (Qiu et al.,
1993
? Donoghue, 1994). This view has been confirmed by analyses of 18S rDNA (Soltis et al.,
Since vessels are often viewed as unambiguously

advantageous in allowing more efficient conduction.
these cladistic results stimulated debate on the
functional plausibility of loss vs. multiple origins of
vessels. Donoghue and Doyle (1989) argued that
loss might be less deleterious than assumed, since
yesselless wood would be derived from wood with
very primitive vessels, not advanced ones. Winteraceae and other vesselless angiosperms usually oe-
199
?), CPITS (Goremykin et al., 1996; A. V. Troitsky, Pers- comm. 1998), phytochrome genes (Mathews & Donoghue, 1999), and atpB (Savolainen et
al., 2000), all of which root angiosperms among a
series of taxa including not only Nymphaeales but
also several woody magnoliid taxa: Amborella, Austrolxuh - I In ule- and ;
.1 on studies of rbi L
by Renner, 1999) Trimeniaceae. Significantly, these
taxa occur together as a clade in rbcL trees (Chase
cur in cool, wet habitats; Carlquist (1975) argued

that this is the only environment where they can
persist, but Donogh ! H .! |i -. , < l'o'9) noted that
et al., 1993). Endress (1987) and Donoghue and

Doyle (198(b
<//</ and Trimeniaceae with Chloranthaceae, but Chloranlhaceae
Volume 87, Number 3
now appear to he an isolate '

the basal grade.
All molecular n I - - !
I i. ii li I. i1 id
relevant taxa have separated Winteraceae from IIliciale> ,ltl(i inked || em * ill) I ,um laeeae i( aiase
et al., 1993; Soltis et al., 1997; Mathews & Donoghue, 1999; Savolainen et al., 2000), making up a
group that I will call Winterales. Ml gems except
18S (Soltis et al., 1997), for which the sampling of
i
- was less complete, place \\n
a clade with three other orders as defined by APG
(1998): Laurales (Calycanthaceae, Monimiaceae
-.L C,omi>rtt'H. I leniandiai eac. 1 anracr:;- . \1: j
mil .J. - }';,,<"<(>,(. II itianlan-:i .- . a- ./'..< v -, /
Mynslieaeeae. Magnoliaeeae. \nr ounceae). ; 1 I'n
|M lali - (I'iperace.ae. Sa iri,r;irf,u . V i-*-:l<... !u.i. <
Lactoris). Based on rbcL (Chase et al., 1993) and
rbcL plus atpB (Savolainen et al., 2000), the sister
group of Winter,i
M
s; based on phytochrome genes (Mathews & Donoghue, 1909) and
atpB (Savolainen et al., 2000). their sister group i>
Piperales.
Like the morphological trees, the molecular trees
iinpb that Vun'eraeeae are secoialarib \ esi-,elless.
although mtereslingb lhe\ suggest that llie absence
of vessels in Amborella is primitive. They also call
into question the view that the carpels of Winteraceae are pruni
\iish
.
i II
I'll
not pin ale arpels (Endress & Igersheim, 1997), implying that
the |>lieati condition is del \ed. Igersheim and KM
dress (1997) also refuted statements that the carpels of Winteraceae and Degeneria are not completely closed (Bailey & Swamy, 1951; Karnes,
"<
tually, their margins are postgenitally
These molecular challenges to morphological
I idi-ll. it -idt- app.-a' l-i I" -aip; i i < \
MII
inary analyses of an expanded morphological data
>< 1 (I I i _
I
I III III
U aid eudlents
(Doyle & Endress, in prep.), incorporating gvnoecial data of Endress and Igersheim (1997, 1999)
and Igersheim and Endress (1997, 1998). These
i
eiales near Austrobaileya and

associate Winteraceae with Canellaceae, based on
(
Phylogenetie analyses hav< also led lo e\ph< il

hypotheses on relationships within Winteraceae.
Vink (1988) presented two morphological iiee-. of
the family, which differed in rooting: one with las
; standard assumption that the
ancestral chromosome number is n = 13 (as in 1
mannia) and n = 43 (as in other members) is d
rived; the other with Takhtajania basal, based <
its elongate
llrinns Inked as a clade, which he preferred. b\eai

^ ink assumed lh
*//,. i/iia has n 43,
based on its large pollen size (Praglowski, 1979),
he suggested that n = 13 in Tasmannia is not ancestral but iler;\ed I nun 43. This poses a problem if the closest outgroup is Canellaceae, which
have n = 11, 13, and 14 (Kubitzki, 1993). In both
i-.- /:'/.;..,; I,:<!>,;>. /\^,^\t,,'n, ,m. I M's,, i
mum formed a clade, linked with Pseud
Two species of / _ _
i/ .
, . i
;.,/,!,< <;.<>, Ha II d.lh I ll< in lh< ie-l el the I.IIIIlK
in having monad pollen grains (Sampson, 1974);
the position of /
i the family implies that these are secondarily derived from tetrads.
The first limited rbcL data (Chase et al., 1993)
were more consistent with the first of Vink's (1988)
trees in placing Tasmamua below Dtinns and />V/
liolum, but they did not address the position of
Takhtajania. Analyses of rDNA ITS sequences by
Suh et al. (1993) d owed II llsllalb low div< rgi nee
within Winteraceae, indicating either an implausibl\ recent age for the family or a slowdown in ITS
e\olutioii. and the presence of two ITS sequence.-,
in Bubbia, Belli
"/.and Exospermum, apparently reflecting an unusual persistence
of polymorphism in ITS. Although unrooted, the
tree obtained was consistent with the basal position
of Tasmannia and the existence of a />''
The rediscovery of Takhtajania has allowed
Karol et al. (2001

la/ania in analy-e- el ITS and tm\.-V spacer sequences horn \\ inleraeeae and Canellaceae. Analyses of trnl.-V indicated that eith- i
Tasmannia could
be ba-al in Winteraceae. but Takhtajania was basal
in trees based on ITS and the two data sets combined. Other relationships within the family were
the same as those found by Suh et al. (1993). These
results are consistent with Vink's (1988) view that
the inflorescence-, of TaiJila/aniii are primitive.
However, the finding thai the chromosome number
una ma\ be n = 18 (Ehrendorfer & Lambrou, 2000) refutes his suggestion that n = 13 in
Tasmannia is derived from n = 43, which does
appear to be a synapomorphy of Drimys and the
remaining groups.
FOSSIL RECORD
There are several old reports of fossil white
analysis of leaf architecture, and they have i
leraceae have lire; nl u "ln-l rank"" cnalion ( I Ink

ey, 1977), whicli has li.ru <OHM.ICI.MI |>riiriitiv. for
aiigiosperins (lliek.v <X Wolfe. I')73). I.ut ollrerw is.-
i of these deteriiiui.itions, lor example In showing the stoiualal

pint:- ;-II.IM< ler -lie .ii'e\ <\ \.i-i.
1944; Feild et al., 1998).
Some leaf reports are from areas where Winteraceae occur lo.la
in I
MI. I
I p. II. n is known
in the fossil record (cf. below). Berry (1938) des.iili. .1 /'
;>,, <ri>nica from the early Miocene
of Argentina, said to resemble Winteraceae in havlii- a papillose" lower surface; the \enalion is coni 1
sistent with \\ ml i
i. i ,n I
i !
i,
I
agnostic.
Dusn
(1908)
described
Drimys
antarctica from the Paleoeene ( \skin. 1()92) of Seymour Island on the \ntarclic Peninsula; the irregular spacing and angles of the secondary veins are
consistent with Winteraceae. Dearie (1902). minted by Praglowski (1979) as Card (1902) and possihlv the source of an unreferenced remark b\ berry (1938), reported Drimys leaves from the Tertiary
of New South Wales, but the fragment illustrated
has no distinctive features. Leaves of W intei aceae
have not been recognized in more recent studies of
rich Australian Tertian. Moras (Carpenter et al..
1994; Christophel, 1994; McLoughlin & Hill,
1996; R. S. Hill. pers. comrn. 1999), which have
ritical methods of leaf i.lcnlificati.
used I
More couv iucilig is a report bv Poole and Francis
(2000) of vesselless wood described as Winteroxylon jamesrossi I. Poole & J. E. Francis from the
mid-late Santonian-early Campanian of James Ross
Island on the Antarctic Peninsula. Although the exact combination of pitting, rav. and paren. hv ma
feature- does I lot ... cur .IIIV modern genu- of W lllteraceae. all a
i i
eh i lli i in 1
in!
Vesselle .IMLIn- I
i
I
./ ft... l|o.|f Illegal i iph
n
ol mod o A int. ra. . i. m.l
fossil records of u i nteroi.l pollen. Chauev and Sanborn (1933) described Oligocene leaves from
Oregon as Drimys arnericana R. W. Chaney & San.lilfcrs from that of Winteraceae in having thicker,
more distinct secondary veins. Page (1979) compared vesselless \\.,d Iroill the Late < .ivla. eons
(Maastrichtian) of California with Old World Winteraeeae; she separated it from New World Drimys
and Trochodendrales based on its abundant parenchyma. Gottwald (1992) described vesselless wood
from the Koeene of Cermany as Winteroxyion mun-
wood of Poole and Francis (2000) that they assigned their material to the same genus. If these
fossils are vvinlera* < oils lli
. In
'
I
ill
familv extended into Laurasia, as in Mexico and
vl.il
II
-ihility that they
represent extinct vesselless lines not direcllv related to Winteraceae should also be considered, given
the absence of nioie diagnostic winteroid pollen,
the abundance of Trochodendrales in the Farlv Tertiary of Laurasia (Crane et al., 1991), and the presence of leaf cuticles with similarities to ! '.'i
in the lower Potomac Group (Upchurch, 1984). Extinct vesselless lines should lie more common if the
lack of vessels in W mlciaccae is primitive, since
this would imply that the anceslnts ol mam oilier
taxa lower in angiosperm phylogeny were also vesselless.
The record of Winteraceae has been solidified
and greatly extended by palynology. based on ulcerate tetrads eloseU comparable to the familv
(Figs, la, 2). Unlike the wood, the distinctive features of the pollen are clearly derived and thus
more indicative of this particular clad* . W inter.ml
tetrads are a persistent but minor element in latest
Cretaceous ami Tertian rocks of Australasia (Dettmann & Jarzen, 1990), consistent with the low pollen production and subordinate ecological status of
\\ interaceae today. Such pollen was tentative!) reported (without illiistr.
tit bv < i.mwell (197)1
from the Paleocene of Seymour Island, an
I
by Couper (1960) from the Oligocene of New Zealand as Pseudtmintern sp. Couper's material was
named Pseudowinterapollis by Krutzsch (1970);
similar tetrads from the latest Cretaceou- lliioimli
Miocene ol southeastern \iistralia were named Ge'iiirs (with three species) by Stover and
Partridge (1973), who were apparently unaware of
Krutzsch's article. Martin (1978) indicated that the
closest match for the Australian fossils i- I'I^,,,;,,
nia. Mildenhall and Crosbie (1979) extended the
range of Pseniinwintenijudlis. which lli. \ considered most similar In Pseudou intern, from the latest
Cretaceous through the Pleistocene of New Zealand. As noted by Suh et al. (1993), since phylogeu. tie analvses indicate that Pseudau intern is
nested within the family, these data iiuplv dial
crown-group Winteraceae (i.e., the .
uller (1981) in his critical review of pollen evimce for extant angiosperm families. In Australaa, the oldest record is from the mid-Campanian
Doyle
Paleobotany of Winteraceae
of tli< <>lua\ basin of -,, ilheastei :i \usl i';ili;i (Hell

mann & Jarzen, 1990). Winteraceae are also known
from the Maasti !i
a o
' . i
ILII I
Miocene of central Australia (Twidale i< Harris.
1977; Harris & Twidale, 1991; Macphail et al.,
1994) and the Oligocene of Tasmania (Macphail &
Hill, 1994). However, since the early report of
Cranwell (1959), Winteraceae do not seem to have
boon dhst-n.-.l n 'I
II1 i Moras from Antarctica (Truswell & Drewry, 1984; Truswell, 1991;
Askin, 1992).
Mildenhall and Crosbie (1979) also reported
loose :il,crate 1" Iratl- am! i: onacs, nana <; H<in<s,
pollrnili-s. rroni i I! . ( H igo. TIC lhioi|p|i I'leistocene
<:f \ v. /( al; ail. w\\ el: ill. . . onpamd with the rnoi
\ Z\L
- impsoii, |'>, 11.

Since ph\ logene!ie anabsos iudii ale lhal aionad
|.i an
',
. ' , n is one of the most apical
branches in the family (Vink, 1988; Suh et al.,
1993; Karol et al., 2000), this record is evidence
that emui. gmnp \\ iri|ci;ii'ca< I! ail diversified to a
high '!.. I>\ 'In Oligocene. These c
would further support the view of Suh et a
that the low divergence of ITS i
from Tertian beds (considered earb Miocene) of

the Cape region in South Africa (Coetzee, 1981;
Coetzee & Muller, 1984; Coetzee cK IVagh.wski.
! Ttikhtujiinia is the
iuted asseniblaj
"Win
teraceae in the African-Madagascan region. The
same Moras contain other taxa that no longer ocean
m mainland Africa but persist in Madagascar: Ascarina (Chloranthaeeae), Casuarina, Cupanieae
Sapirt lac* le), and Sarcolaenaoeae. llowe\ei. according to Coetzee and Muller (1984) and Coetzee
and Praglowski (1988), these fossils are most similar not to pollen
' ' "
i it rather to thai
of the Australasian genera Tasmannia ("Drimys" pi,"(:>!,;)
and
/.',,'V/,w
\" /; ^<>L < n'.'ti,"
,>>>> s ,;.,,/, ir
Although pollen of Drimys occurs at low frequencies in the Qualernan of Chile (e.g.. Ileussor.
1981), there have been few reports of uinteroid tetrads from older sediments in South \mcrica. although such rocks have been e\lensi\e|_\ studied
(cf. Askin & Baldoni, 1998). Apparently the oldest
are grains identified by Baldoni (1987) as Gephyrapollenites calathus Partridge from the PaleocencEocene of Argentina. Barreda (1997) reported
'"//,
i/wri Krutzsch from the Oligo-Miocene of Argentina; she provided SEM figures
I- in,,,,- 2. I're-Qoater
a.id I-ran. i, |20(M)|. Tup. Kark (aviar.-ous (base map 120 My, ]
ceous and Tertiary (base map 50 My, Kocene: Scotese, 1997); 1
Oliôcene, Miocene, Pliocene. See lexl lor references.
-how ii ii i tetrad closely <

sciii|>tnrc anil |n'r-ni< c <>j a vvel: dclincd antiiiius.
The stratigraphic and geographic range of win:. tuiii 11-1 <-n i\,ts - - \ 11 -1 .l.-ij diamalii :ill\ l>\ Walkei
et al. (1983), based on tetrads in two cores from
the late Aptian-early Albian of Israel. At this time
(Fig. 2), Israel was part of the Northern Gondwana
1 to Winteraceae and vesselless wood of Poole

i- \ptian: S.-otesc. 1W7). Bottom. I-ate Cretaii i M
in'Iih.ui: 2: Paleocene. Kocene: ,V.
province of Bivni ( 1'.'7i!. which -n.d!l.! 111.

Early Cretaceous equator and included all but the
southern portions of Africa and South America. In
c()ini;i>l. I :ili < !'<!.id ,, i. 'I'crli.UA. and Hi a rill >ccurrcnccs ol Wmtcraccac (except those in Central
America and Malesia) are in regions that belonged
to Brenner's Southern Gondwana province in the
Kark Cretaceous. The Israeli (chads, designated

WalkeripollLs sp. A by Doyle et al. (1990a), resemble pollen of modern Winteraceae in having a
ion i a I ulcus consisting of' a crura! pore surrounded
by a thicker annulus, underlain by a safranin-staining ring that Walker et al. (1983) assumed was
. endexine, as in many modern Winteraceae (Praglowski, 1979). However, Walker et al. iniciprctc!! diem as moie prim live than living Wei
teraceae becausi
I
Still oldci winleroid pn len was des n! d b\
Doyle et al. (1990a, b) from the Cretaceous of Gabon. i- H./'/,. >,;.<!:,> rohoiirnsis J. \. I )o\ Ic. I lotion
& J. V. Ward (Fig. lb). These tetrads appear to be
even more primitive in having a slightly elliptical
aperture (presun
i
r I (mm a sulcus)
and fox eolalc sculpt ite. witl -ma I U el f p. lo
tions only. Transn
i
Microscopy (TEM)
aed
In d,
mfirmed that the
annulus. These gram- were lo ual :n oi k ni - in
pie, from an interval (Zone C-VII) near the end of
filling of the nascent South Atlantic rift with coni
'auk common in
this -,nnpl< I In n si-1 ih< tm < w i- (Hi do. ! d I.
Doyle et al. (1977, 1982), who assumed that they
were tetrad-producing variants of Tucanopollis crisopolcrisis (Begali. kcsiigui iK \. S Sanies) UVjaa
a common angle-.
beds, which also
has a round, sculptured ap< nitre. The age of Zone
C-VII and its equivalents in Brazil was originally
considered early Aptian (Doyle et al., 1977, 1982),
but Regali and Viana (1989) and Doyle (1992) argued that it is late Barremian, based in part on
reports of two associated new groups, [fro
Iricolpate pollei . in independent !\ dated late Bar
remian rocks in Morocco (Giibeli et al., 1984) and
England (Penny, 1989) (and more recent I\ l-niel:
P. J. De Haan, unpublished Ph.D. thesis, Botany,
Univ. California, Davis, 1997).
Compared with modern Winteraceae, both Walkeripollis gabonensis and W. sp. A are anomalous in
being calymmate (Van Campo & Guinet, 1961),
with the tectum partially continuous between adjacent monads of the tetrad. In this respect. llie\
appear more ad\an< en titan tl acaki anil- t. na
of the modern taxa, where the tectum stops at the
junction between monads. Since the circulai apei
ture and coarsei >'
suggest that this species is phylogeneticalk closei
to modern Winteraceae than W. gabonensis, Doyle
et al. (1990b) inferred that the calymmate condition
and reversed to acalymmate in modern Winteraof sculpture. The fact
that Walkeripollis i-. cak annate max he gn.ua;]- |oi

caution in relating it to Winteraceae, but W sp. A
is aluios! | MI ( . ik ntenncdiale In Iwrn 11. yaho
nensis and modern Winteraceae, and both species
are only weakk
sing that the reversal required would be minor. The fact that both
His species have a conspicuous annulus,
like TnlJ.hli'l'ti'l. />/'.. 11'>!!>.'";;,. ud />:... t"
urn species with monads (Praglowski, 1979), suggests that the lack of a well-differentiated annulus
in Tasmannia, Pseudowintera, Bubbia, Exosperi '
-pe, ie> with tetrads is derived. Absence of an annulus seems loose]\ correlated with smaller aperture size. Exospermum and
i i
IU
'''e III haxing
fine sculpture, but their position in morphological
and molecular phylogenies (Vink, 1988; Suh et al.,
1993; Karol et al., 2000) implies that this condition
is secondarily derived.
Winteroid tetrads may be more widespread in the
Early Cretaceous than reported so far. In the middle
\lb. u kliafji member of the Wasia Formation ol
offshore Saudi Arabia, S. L. Gaponoff (pers. coram.
1990 & 1999) found a single tetrad, which is similar to Walkeripollis sp. A in sculpture but looser
and apparently acalymmate, suggesting that it is
still more closely related to crown-group Winteraceae. IHII so far there is a gap in the record of such
pollen through the first half of the Late Cretaceous.
A possibly related pollen group consists of foveolate-reticulate, ulcerate monads from the early
Aptian to Albian of Israel, described b\ Brenner
md I'.ickod (l'l<2| a- lu'H'n,>;;,<!,';>!., .yc, ,,!,,>:."G. J. Brenner & B -koil 'III-a sciilptun- -.i.ajghk
similar to that of Walkeripollis sp. A; the ulcus is
covered by an o| i lum i< im et lain by a darkstaining area interpreted as endexine. Because
these monads predate W. sp. A in Israel. Brenner
(1996) interpreted them as representing a more
primitive, pre-tetrad state; however, they are probably younger than W gabonensis. It is possible that
these grains are related to Winteraceae, but there
are enough differences to make this view souiewh.it
speculative. They are much smaller than the monads of Walkeripollis. the ulcus ]s proportionally
smaller, and the endexine forms a solid patch rather
than a ring around the border of the ulcus.
Doyle et al. (1990a, b) also suggested that two
other Cretaceous pollen groups may be related to
Winteraceae: Afropollis, which is abundant from the
late Barremian through the early Cenomanian of
Northern 1.
w m i md \,'not, ';>,>,'>'> ion |.
Aptian of Egypt and Maryland. Afropollis varies
from operculate or zonasulculate in the oldest species to inaperturate in younger ones, with a loose
erculates have typical J

below llli- K tl< II
V /, (.i ,;,,. i ,
bill ,
i finely sculptured. The
parison with \\ inl. iiu ;it- v\as based primarily on
the fact that \fi<
s mil Walhnipollis gabonensis all have finely segmented
and tend toward circular shape and a round aperture, with the zonasulculus presumahly derived In
broadening f an operculum. Based on a eladislic
analysis of tlle.se lossils and pollen ol I . : Win
teraceae and Illiciales, Doyle et al. (1990b) inferred
that \fropollis and St hnuikipollis belong to
tinct sister group of Walkeripollis, Winterace;
Illiciales. The two Walkeripollis species wet
cessive branches of the sleni-lmeage leading to
both Winteraceae and Illiciales. based on the elliptical aperture of W. gabonensis and the liner scul|
tllle ol both species. The Iricholomosillcate C*s\r
trieolp.it.-") monads ol Illiciales were linked wit
tine, implying that they are secondarily derive
from tetrads. Because this analysis pla< "
,;..,-';,\ ..:i i!i sti ii linear In W nleiaee; , and III
Doyle
(1990b) speculate.I that the plants producer ll-i/7,
t-i i poll is still had vessels.
This scheme can no longer be defended.
only the tetrads seem securely related to W
ceae, and molecular evidence against a relali
of Illiciales and Winteraceae has become
whelming (cf. above). Doyle et al. (1990a, b) acknowledged that the winteraceous affinity of Afropollis and Schrankipollis was more specu
They noted that \fiopnllis is anomalous in having
a thick endexine all around the main, as in gymii..-,pciino is -ceil | lauls. raliiei than under the aperture otib, as In Winteraceae and most other magnoliid ai giosperms. Because other characters ol
I
HI I
ig.os
us md l . in-,, i
leu magnoluds do have a thick endexine. they suggested that the endexine character may not rule out
er, Friis et al. (1999)

found Afropollis in separate pollen sacs with
features. A similar combi-
I ale Triassi, I a u op >l|. (..nil. I gi o ip. win. I I iotnet (1989) interpreted as angiospermous, but which
Doyle and Hotton (1991) and Doyle and Donoghue
!lM"'.;i
iggested is related to the angiosperm
crown-group but more primitivei.e., on the angiospern sl.an hu. age liv Ihe s;u,;.- reasunaig. 1/
.1 the angiosperm
stem lineage that persisted into the Cretaceous.
These doubts do not apply to Schrankipollis.

i<
it has only a little endexine under the aperture, but
uuhoal 1/;../',,//-> to rik I .v l'i \\ nileiaeeae. there
is little reason to associate it with the family.
Scenarios for origin of the tetrad pollen of Winteraceae also need revision in light ol mole, ulai
ad mi I I ologi. al e\ id. n. . that < anellaeeac are
the sister group of the family. I'ollen ol Canellaeeae
is small, round, and monosulcate, with occasional
trichotomosulcate \ariants (Wilson. 1964; Walker,
1976; J.-M. Groult. unpublished D.K.A. thesis, Museum National d'Histoire Naturelle, Paris, 1998).
Its e\ine structure vanes from gr;
lai with a continuous scabrate tectum {Capsirodendton) l.> coluliiellar and either foveolate (most general or retici i [(::.;n>tmnsni<i). Walker (l<)7<>) assumed that
the granular extreme is primitive, as part of a general trend in augiospernis ;i- a whole. This would
imply that columcllae arose independently in Canellaeeae and Winteraceae. The idea that granular
structure is primitive in angiosperms was supported
by the analysis of Donoghue and Doyle (1989),
il.s at the base of the angiosperms, but in more recent analyses, where Magnoliales are nested within woody magnoluds. their
LI n: i at structure is a reversal. Canellaeeae are
rooted (iillerenlb 111 trees based on ITS and trn\,F (Karol et al., 2000), but the unrooted tree is the
same, and Capsicodendron is not basal in either
tree. This suggests that the common ancestor of
Winteraceae and Canellaeeae had small, round,
inonosuleale pollen with columcllae and loveolale
sculpture, a type common in the Early Cretaceous.
Sum poll, II iua\ go back in die liist ai giosp, rins:
lor example, it occurs in the near-basal genus Austrobaileya (Endress & Honegger, 1980). These data
SS, |, | |),,\ || , t
al.. I ,M" I l>
1
i j i I. II in nphology, a phylogenetic analysis would place Canellaeeae below
'lis. so vessels could have been lost at any
point on the line leading to crown gr< n. A il
ceae, either before or after Walkeripollis.
(d
III.I;
vi'itic
HISTOID
\\n Kcoio<.i( \i
Fossil dala suggest that the stem-lineage leading

to W lllei ice.i, . , ,,i, s, ( , ,| |,.. U-(,'.', o'/'o.'.'o on-'
inated in the tropical zone of Northern Con.Iwana.
This is consistent with the view of Raven and Ax< 'ii c ( I'l'f It thai ai gi
-j- ''I"- as
\ who
lig I alcd
in this region. The Early Crelaceous eluuale m ihe

classic areas of Gabon and lira/.il has been interpreted as hot and dry (Brenner, 1976; Doyle et al.,
Doyle
Paleobotany of Winteraceae
1977. I9M2L based ,,, >l:e low frequency of spores,

abundance of ( ,
nfer family Chein |
I iceae, noted for its xeromorphic vegetative
linn ill olc.^.v t ;IIKI i-pln'ilroiil poller; pel i|,-,l l. m 1
fin I -in t;il. v. < ( 1 i i '
i,! II
desert plants!, and the presence of thick Aptian salt
deposit.-, which in,i! k :!.< I;: -I iuf.u i f in n in.. w,;<<
into the rift. However, there is evidence for wetter
conditions in the Middle East and northern South
about 15 degrees to the south: less common Clas
'
fern spores and
Araucariaceae, and occasional coals (Do\le et al..
1982; McCabe & Parrish, 1992; Brenner, 1996).
I i
i
"
mollis occurs in both areas,
-i
. - i
i i i
i. til pi,HI- i I Id loleiate -ome
range o| ia u*-ill 'I lie la. i 'In' Ii ia>';< ,-.,, i - i,.. ,
a rill se(|iieiiee raises the possibility that it- parent
plants were growing in cooler upland areas flanking
the nit. lloue\er. models for rift evolution predict
that relief would decrease with time, and although
the pi. sence ol ll:-.t<
I- pod
l pace.His pollen
ii-i i that there were high elevations near the
rift in the earliest Cretaceous, such pollen had disapp<
! I.v il . tut \\,ill ','.,. -' - pix i<
Barremian (Doyle et al, 1982).
This scenario also fits the present distribution of
probable miigroups ol V iriler;;eeae. Canella. eae
are entirely African. Madagasean. and \iiierican.
and Walker (1971) and Raven and Axelrod (1974)
i i- I
.I liiei
\ ml
i i ondwanan origin.
a IK. they are more tropical than Winteraceae. and lhe\ extend into drier enviroiun. ni (Km
bitzki, 1993). The second outgroup to Winleraceae.
whether Magnoliales or Piperales, is less well establ -lied Hi Aral r M.i.'i ol .1. s .no the sc. on< I
outgroup, it may be significant that rli,-\,. at/Ai. and
branch in this group is Myristicaceae (Chase ei al..
1993; Savolainen et al., 2000), which have a geographic distribution that also suggests a Northern
Gondwanan origin (Walker, 1971; Raven & Axelrod, 1974). Myristicaceae are also a lowland tropical group, and although then species diversity is
highest in Asia, Walker and Walker (1981) argued
that their most primitive members are the \ladagascan genera Mauloutchia and Hi..hi.
ii
'i Ii i i J1
III
ii ed stamens (a
view confirmed by a morphological cladistic analysis by H. Sauijii. I
in.| ibh-d I IN \ thesis.
Univ. Pierre et Marie Curie, Paris, 1999).
Hii:-, belli tils:- Ii (list) ibillioils :i!lil ally ] igern hi
r. -.i.i- -uggest that the temperate, Southern Gond-
\\
uthward migratic
ol plants derived from a stem-lineage in the lowland

tropics, [n the Early Cretaceous. Southern Gondwana was characterized by I'odooarpaeeae, Araucariaceae, and abundant spore-bearing plants
(Brenner, 1976; Herngreen et al., 1982; Dettmann.
1994), suggesting cool, wet conditions like those
where Winteraceae grow today. These data may fit
the hypothesis discussed above that vessels were
lost in cool, wet environments because of their susceptibility to embolisms caused bv freezing (Donoghue & Doyle, 1989; Feild et al., 2000).
A major unresolved problem is when exactly
Winteraceae moved into the temperate zone, and
by what route. After the records of Walla<:<,-:<>, i
the Early Cretaceous, the line is not known until
the Santonian-Campanian ol \ntarctica. represented by Winteroxylon wood (Poole & Francis, 2000),
and the Campanian-Maastrichtian of Australia and
New Zealand (Stover & Partridge, 1973; Mildcnhall
& Crosbie, 1979; Dettmann & Jarzen, 1990), represented by coarsely reticulate tetrads resembling
clown group Winteraceae. These lelrads seem well
established in Australasia, and there arc no records
ol them III tin- tropics (although given the rarity of
earlier reports the significance of such negative evidence can be questioned). Migration to Southern
Gondwana would pose lillle problem in I he Early
Cretaceous, when the continents were still largely
connected (Fig. 2). However, by the time the crowngroup is first recognized, ocean barriers had become much wider, especially between Northern
Gondwana and Vustralasia. Possible scenarios may
be considered in terms of continental positions , a.
6 My before the Campanian (Fig. 3; Scotese. 1997).
One route to Australasia might be through South
\inerica and \ntaretica. which was attached to
\uslralia until late in the < aetaeeous. On paleogeographic grounds, it is more likely than not that
the stem-lineage occurred in Smth \merica. In the
Early Cretaceous, Brazil and Gabon were two sides
of the same rift valley, and given the rarity ..! Wall,
<>ripollis. the lack of reports from Brazil is probably
not significant. However, if the crown-group -pread
South Atlantic in one direction or the other to explain its Tertiary and Recent occurrences in Africa
(Coetzee & Midler. 1984) and Madagascar (Takhtajania). This scenario implies that near-basal lines
of Winteraceae occurred in South America in the
tively nested position of the American genus Drimxs in the family and the ranl\ ol reports ol pnwinteroid pollen in S.ulh \iiierica
<(!. -|> le i;iutM'K!ii> ::: IK nolo-i, ,i studies; el'. \skin

& Baldoni, 1998), as compared with Australasia.
Vhd.iL.iM .! i-M'iJu.rii I). -.11 In split into Kasl
' ;<:ii.lwai : ( \l.n: i,;M at. 11 I :.. \*ilairlica. Australasia I an.I West Gondwana (Africa, South America)
in the Middle Jurassic (Rabinowitz et al., 1983).
However, for sonic tunc Madagascar and India,
which bclc.iijcil io [I,, Soiiih.-iii Gondwana province in the Early Cretaceous (Brenner, 1976; Herngreen et al., 1982; Dettmann, 1994), formed a block
that might have acted as a stepping stone between
\lina and Australasia and/or Antarctica (Kig. 3).
This scenario might fit molecular evidence that
TnUilaj.mia is basal in Winteraoeae (Karol et al.,
L'I in 'l
,
old i. pi. s, n| a I,ranch that
stayed near the original Northern Gondwana ;
while the rest of the family was derived from a
branch that dispersed to Australasia. Drimys could
b' a line thai dispersed later from Australasia to
South America via Antarctica (Kaven & Axelrod,
1974). consistent with its position in the family.
If, however, Winteraceae in the Tertiary of South
Africa were related to modern Xnstralasian genera
(Coetzee & Midler, 1984; Coetzee & Praglowski,
group and many local extinctions. The discovery of

wiiiteraeeoiis wood in the Late Cretaceous of Antarctica (Poole vK Francis, 2000) also suggests it
would be premature to favor one scenario over an1

ii < rai ea< leached Antarctica ver\ early, from which they could easily spread
Io cither Australasia oi Soul Ii America. Heller evidence on the phylogenetic position of known (irefossils, could greatly clarify the geographic luslon
of the family.
COLLISIONS
The stem-lineage leading Io Winteraceae is one

of the oldest recognizable angiosperm lines, ex i I i
hack to the Barremian stage of the Karlv
Cretaceous in [Northern < iondw ana. Modem Win
ieraeeae appear to be derived from a line that
spread from the tropics into the southern temperate
latest Cretaceous and Tertiary, but the details are
uncertain. Major priorities are to fill in the Late
Cretaceous record and to elarifx the time of appearance of crown-group Winteraceae in AfricaM i I
i
I S:arl \iin i ii i I lopefully this paper will alert palynologists and
paleobotanists working in the Gondwana continents
II and megafossils, and thus
conlnbulelo; more detailed
historv of this iiportant family of primitive angio-
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Tin-
separation of Madagascar ami \ln, .,. Science 220: (.769.
Raven, P. H. & D. I. Axelrod. 107 1 \g,osperm l.iogcographv and past continental movements. \un. Missouri
Bot. Card. 61: 539-673.
Regali. M. S. P. & C. F Viana. 19B9. Fate Jurassic-EarF
Cretaceous in Bra/.ilian Sediment,ir\ Basins: Correlation
Renner. S. S. 1909. Cm,, iptmn and phylogeny of

the Faurales: Evidence from molecular and morphological data. Amer. J. Bot. 86: 1301-1315.
Sampson, F. B. 1974. \ new pollen type in the WinterSavolaiiieii. V. M. W. Chase. S. IF Hoot. C. M. Morton.
1). F. Soltis. C. Haver. M. F Fa%. \. V De Bruijn. S.
Nillivanc\ V-I.O.ii. 20(H). Phylogenetics of flowering
rlu-l. gene sequences. Sxsl. HloL |9; 306-362.
Schuster. K. M. 1972. Continental movements. "Wallace's Fine" and 1 < unili in \
> 1 - > .1 -[> i-
Upchurch, G. R. 1984. Cuticular anatomy of angiosperm

leaves from the Power Cretaceous Potomac Croup. 1.
Zone I leaves. Amer. J. Bot. 71: 192-202.
Van Campo. M. i\ P. < .niuel. I<0|. Fes pollens composes.
Eexemple des \li,nusi,r,s Pollen & Spores .',: 2111
218.
Vink, W. 1988. Taxono.m in Winleraccae. Taxon 37:
691-698.
Walker, J. W. 1971. Pollen morphology, phytogeography.
and ph_\logcn\ ol the \nnonaceae. Coiilr. Cra\ Herb.
the pollen ol primitive angiosperms. Pp. 1 1 12-1 137

in I. K. Ferguson & J. Muller (editors). The EvoluLondon.
& A. C. Walker. 1981. Comparative pollen morphology of the Madagascan genera ol \l \ risi n aeeai
[Mauloutchia. Hrorhoneura. and Haemal,xlen.hoin.
&
. 1984. Ultrastrueture of Power Creta-
ceousangiospcnnpoUen and the origin and early evolulion of flowering plants. Ann. Missouri Bot. Card. 71:
464-521.
, (;. J. Hrriiiirr & A. (i. Walker. MMl. Winl.-.ae\i<lt in < of a ru.i
220: 1273-1275.
ili;il
ii |
i 11 i Mini
S,
Wilson TK 1964 Comparative morphology of the Cah

i":
Wolff. J. A.. J. A. Doyle & \. M. Page. 1075. Tlie bases
of angiosperm phylogenv: Paleobotany. Ann. Missouri
Hot. (ianl. 02: 801-824.
i,
selless? Syst. Bot. 6: 313-330.
WOOD AND BARK ANATOMY

OF TAKHTAJANIA
(WINTERACEAE);
PHYLOGENETIC AND
ECOLOGICAL IMPLICATIONS1
Sherwin Carlquist*
voody root 4 cm in .[in. Icr. ,n I . M .ill, r stem with only a little secondary growth. The wood lack
ind is vesselless. Tracheids bear biseriate or Irisenatc circular pits or seal.inform pits on end wa
nrcular pits on sid,
i I
'
u ' ' 11 il In ' ni i - in lacking on lli. inner surfaces of In
>arench\ma is ver\ sparse. Mulliseriate and uriiscnatc ra>> are about equalR abundant, an,I both ar
ipright cells except tin .. in.il ni..t i >i pn ii.nl n .11 in null is, i i.ite ia\s. Kthereal oil cells
ire absent in rays. Bark contains sclereid nests and ethereal oil cells. Wood features closely matel
imiiiiia or Dunns, in agreement with conclusions reached on the basis of molecular data. Cmnparaliv
>l Winteraceae othc r i in . ',<, i
n li I in
I < HUM
/
, ,n,c with those
pccies b\ lacking features found in temperate Winteraceae (growth rings, warted trachcid surfaces.
Wood of Winteraceae has been surveyed at the

species level f'oi ill genera rM
I'l
herbarium spe, u
I
hitherto available did not have sufficient secondary xylem for
satisfarton stuck: turns are often ol iiiinled value
in determining the nature of wood anatomy of a
species. Rediscovery of Taki
described in an accompanying paper of this series
(Schatz, 2000 this issue).
Winteraceae have traditionally been regarded as
retaining numerous character states primitive for
dicotyledons (e.g., Dahlgren, 1975; Takhtajan,
1987; Thome, 1992). Recent molecular studies
(e.g., Qiu et al., 1993) place Magnoliales. which
Another pin I
i
'
e has I
I
' i
sellion (e.g., Young,
1981) that woody groups of vesselless dicotyledons
(Amborellaceae, Tetracentraceae, Trochodendraceae, Winteraceae) may be secondarily vesselless
ran
ih.ui i m.i:ii\ -.,.
latter view (e.g., Bailey, 1944) has been widely propagated,
Ecological questions also are of significance. The
presence of growth rings, warted inner wall surfaces
of tracheids, and helical thickenings in secondary
xylem tracheids characterize more temperate species of Drimys (Carlquist, 1988a), Pseudowintera
(Patel, 1974; Meylan & Butterfield, 1978), and Tasmannia (Carlquist, 1989). These features are lack-
but place other orders of flowering plants (notably

paleoherbs) as basal to Magnoliales. \ primitive
status among du ol\ I i i \
\
advanced by Taylor and Hickey (1992). Wood of
Takhtajanid is of potential interest in assessing the
position of Wintet.i i
I
i
/
nia within Winteraceae can be assessed on the basis of wood anatonn tee u
I character states
within the farmU ^re sidbcientk diverse that a kej
could be constructed on the basis of wood dat
alone (Carlquist, 1989).
sites, as shown by Belliolum (Carlquist, 1983a),

/',
'
<-nm m (Carlquist.
i
' ,
i bpuist, 1981). The
ecology of Takhtajania, which grows along a moist
ridge in monti
gascar. has been described in an accompanying paper (Feild et al.,
2000 this issue).
Information is offered on bark anal <>m \ <>l Tnhh
tajania here Thil nfonnatio] may serve for corn-
1
The writer is grateful to George E. Schatz of the Missouri Botanical Garden and to the collectors cited for providing
the material ol Tokhhijania.
2
Santa Barbara \\
i'l Mission Canyon Road, Santa Barbara, California 93105, U.S.A. Address
87: 317-322. 2000.
The first collection of Takhtajnnia perrieri (Capuron) Baranova & J.-K. Lero\ made available lo
me is documented l>\ the collection Pierre Jules
Rakotomalaza et al. 1342 (MO). The collection locality is in th< x
V MI lb -< i .<
southwest of Andapa in norlliea-len Madag^scai
(Si Siai/. 2000!. [ICIIL- ; i mgi in wlih I. mati\ of the
id and covered
with lichens. This collodion provided li(|iiid-|.reserved material of a woody stem 3.5 cm in diameter
and a portion of a stem with onb a little secondary
growth. A so ond .Hi
i >m m
i'.hns
Birkinshaiv 483 (MO), provided a liquid-preserved
stem 4.5 cm in diameter and a root 4 cm in diameter. \ll ol these materials were origin
served in formalin-acetic alcohol and were transferred to 50% aqueous ethanol.
Sections of the smaller stem and the larger stems
and the root (all with both bark and wood) were
prepared according to the schedule of Carlquist
3.5
, 1.5 .
microtome. Some of these sections w/ere dried beIween glass slide-,, s-.niti r-coated. ; ind examined
with scanning electron microscopy (SKM). Other
sliding microtome sectionsi were Plained with a sa|ranin-fast green combinati on and mo unted in Canada l>al-ani. Macerations < if the wooc l of the larger
steins and of the root wer c ptepan d with Jeffrey's
1 1 ii' 1 a IK. -iained wid -adaini . Mi a n tracheid diametei is based upon 1 in.
1 imeter of (recheids. Thickness of radit
used for measiircmeiils of wall thickne ss. Means are based on
25 measurements except for trachei d wall thickness, in which wall portic >ns judged to he Ivpieal
were used.
ANATOMICAL RESULTS
cm in diameter unless otherwise indicated. Quantitative data for the two large stems were not considered significantly different from those of the
large toot (except lor tracheid length), so only data
on the ~|em 3.3 cm in diamelci form the basis for
the description below.
Growth rings absent (Fig. 1). Tta. hearv elements
all tracheids (Figs. 1, 2, 5-9). Mean trachei,I length
(largest stem), 3002 p.m. Mean tracheid length
(root), 3821 u,m. Mean tracheid lumen diameter, 38
pin. Mean tracheid wall thickness, 4.3 u,m. Lateral
pits (Figs. 7, 8). End walls ol tracheids will, biscrialc circular bordered pits or scalar! lot m pits
(Figs. 5. fi). the latter sometimes more crowded than
shown in Figure 5. Pit membranes present in end
wall pits (Fig. 6), both in stems and in root. Tracheids with sealarifoiin pits less ommmi than
those with circular pits on end walls formed in
stna I gro ips w illi no anpax ai patiein ol disltibu
tion within the wood. Tracheids with sealarilorm
i
ill
i i_
iculi ;| uioii i omiiiou in the root
studied than in the stems. Circular pits with narrow b elliptical apertures (Figs. 8, 9), pit cavities
about 9 p,m in diameter as seen in face view. A
i
i
aracteristic elongate elliptical linn areas oriented transversely to
helically on inner wall surfaces; dies, arc not like
llnekenings reported in Pseiulowintera and
one species of Tasmannia (Carlquist, 1989). Warts
absent on tracheid wall inner surfaces (Figs. 5, 8).
I'll \:ii gi nerally more abundant on radial!, ni.ni
\ . i I- IMII . i I
III pilln i i . be seen on radially oriented and diagoiialb oriented tracheid
walls. Axial parenchyma very scarce (Fig. 7, left),
distnl,nied in a diffuse fashion and composed of
strands of five or six cells. Rays multiseriale and
uniseriale (Fig. 2). about equalb frequent (if biseriate rays are in ludci! iimiy aiulhseriale tavs).
Miillisciiale rays are more common than the photograph of Figure 2 suggests because there are long
to five cells in width at widest point
(Fig. 2),
n multiseriate ray width 2.5 cells,
riate ray height, 4176 jxm; mean uniseriate ray height 1473 p,m. Uniseriate rays composed of erect cells; multiseriate rays composed
mostly ol square to erect cells, a lew procumbent
cells present (Fig. 3). and the ray type of the species thus intermediate between Heterogeneous I
and Paedomorphic I (Carlquist, 1988b: 179). Ray
ells will, thick lignified walls, most pits bnrdeted
as seen either in sectional (Fig. 4) or face view.
I! id i
i II d. \eloped on pits n| langentially oriented ray cell walls. Some ra\ cells with dense,
granular, dark-stammn contents interpreted here as
tannins (Figs. 3, 4). Ethereal oil cells and sclereids
At the periphery of the phloem, a sheath ol fibers

develops (Fig. 10). These can be termed proiophln
cm libers. Fibers were not observed within the see"iloein. In bark of the larger specimens.
nests ol thick-walled bra. h\s. h rcids (not ilhistral-
Volume 87, Number 3
cell- are upright: a lew -quart and procumbent cell- are near top of photograph. 4. Portion of ray cells from rat
section -howm-i I>OKI( it il pits m s, < lional n
n
I
in
i i
i
n
I ion scale above Y
mm 1
ELJLB
mmtVfmii
i 5-9. SEMphotogui 11
1 ,1 I I 1 1 in
.,,.[, 1 ,m 1 if.
I utionôl liilihiajdin
-.">. Krul wall of trach.
'
I . n< il 11 pit- 6 S( alariform .it
from end wall of tracheal of radial section, to show presence of pit membranes, which have heen fracture
. . Inside surface of two tracheids from radial section
circular pits in tracheids at left; traoheid to right of cei
1 scales at upper left (bars = 10 u.m). Fig. 7.
100th. 9. Tracheids from radial sectio

illy elongate elliptical thin areas. Figs.
Fig. 'A: Fig. l^. scale above Fig. 4.
Volume 87, Number 3
Phellem is notably thick on the older stems studied (Fig. 11). As seen at higher magnifications, the
walls of the phellem cells are clearly lamellate.
Presence of gi
h in
n nee of warts on
i.Mt-r \\all> il lnieli< :.-,. ;,r<- !lir of I i ; -1 cal thick
1
i - d i i J i
in habitats of particular species
of Winteraceae (Carlquist, 1989, and papers cited
therein). Takhtajania lacks all of these features.
From this evidence alone, one could cond i i I ; i
./ grows in a frost-free zone, in contrast
to the habitats of, for example, Pseudowintera.
Length of vess< :
lated to ecology
in vessel-bearing dicotyledons (Carlquist. 1975). In
tively small tree. The greater length of trach

the root as compared to those of the sten
accordance with data by Patel (1965) that re
sel elements are longer than stem vessel el
in dicotyledons at large. Sections and mace
suggested that scalarilorm end-wall pitting u
was somewhat more abundant in tracheitis <
as compared to those of stems.
In the summary of woods of Winteraceae (Ca1

I i
>o9), a key based on wood of the genera
other than Takli)
i< ented. Now that
./ wood has become available, one can
place this genus in the key. Takhtajania falls closes: in J'uMi-anaiii. h i tl : :n i"!. -' a! i l<< m pil
ting appears in some tracheids (at least in the earlier years of secondary xylem formation),
te rays average between 2.1 and 1.1 cells
at widest point, procumbent cells are scarce in mul
Z^Z^y'DnZ i" .tailêrS In _^; '^l^L, of ft*,,. . .. ,W,
having more abundant f m ! r nils in ra\s.

These results are interesting in that the molecular
data now at hand (Kami et al.. 2000 this issue)
show greater
s.milari.v between Tukhlajania and
&
_
.
n
a.
i *
T/L

Tasmannia or Drimys than between lalililajama
and either Bellio
<
spcrmum, Pseudowintera. or Z\gi>g\num. In \ ieu of I he fact that
molecular results (Karol et al., 2000) show Takhtajania to be basal within Winteraceae, wood fea-
,...| \liso 12: 81-95.

. 1988b. Comparative Wood Anatomy. Sprit
Win*:. Berlin an<l Heidelberg.
~ ] '"'"" ^""'1 ;'>"""'> '^"'"'7"-1"
wood anatomy of Winteraceae. Ahso 12; 2... 2...
| ,.,1,1 .,,.,, |( \| | |.):;, \ ^M,., ,,j , | , ,i, ;,ij<
-tiat. tin .1
t|u angiospcmis to l>< used to den
tures of Takhtajania, as well as those of Drimys and
Feild. T. S.. M. A. Zwieniecki & N. M. Holl.rook. 2000.
than those of the
|IU
' V|IM Missouri Hot. Card. 87: 323-334.
Karol. K. C. Y. Sub. C. K. Schatz & K. A. Zimmer. 2000.
Molecular evidence lor the ph\ logeiietic posilio" <''
,
lukhlapin
pared to bark of oilier Winteraceae because lew
data have been accumulated on bark anatomy in
mI1
the family (Metcalfe, 1987). Esau and Cheadle

/i^r,^ 1
1
! 1
,
, ,
r ,v
(1984) have desr.il.ed secondary phloem of Winteraceae in detail, but were not concerned with
broader aspects of bark in the family.
Literature Cited
^""" '"
rihosomal and ehloropfisl ync sparer M'<|uciiecs. \n,i.

Missouri Hot. Card. 87: 414-432.
M
ll,
M |, !!l
\"
J"";"'" "'M
^"'"M ' '' ."'
| '
Nul, ')! '
Magnohales, Ilhciales, and Laura I. -. (.Ian ndnn
Press. Oxford.
Mevlan. B. A. & B. C. Butterfield. 1978. The structure
of New Zealand woods. I). S. I. H. Bull. 222: 1-250.
Wellington, New Zealand.
secondary xylem in roots and stems.
HOI/IOIM
hung I1':
. 1974. Wood anatomy of the dicotyledons indigenous to New Zealand. 1. Winteraceae. New Zealand J.
Bot. 11: 587-598.
IU, Y.-L., M. W. Chase, D. H. Les & C. R. Parks. 1993.
Molecular phylogenetics of the Magnoliidae: Cladistic
ICS.
. 1981. Wood anatomy of Zygogynum (Winteraceae): field ohsen at ions. Bull. Mils. Natl. Hist. Nat.
I'aris. B. Adanson.a. ser. 4. 8: 281-292.
. 1982a. K.xosperwum slipitalum |Winteraceael:
Observations on wood, leases, flowers, pollen, and fruit.
VHso 10: 277 289.
. 1982b. The 11-e of ethylene diamine in -.olleumg
hard plant structures for p.ual'l'm sect ioning. Stain Technol. 57: 311-317.
I
' < '"'I
',"./ !\\ niter.i
eeae)andanoteonlloyyering. J \rnold \rl.r.64: 161169.
. 1983b. Wood anatomy of Hubhia (W interaceael.
analyse- of nucleotide se.|iicucos of the
pl.i-li.l
-cue
rht.^ Ann. Missouri Hot. (,ard. 80: 587-606.

Schal/. ( .. K. 20011. The red,.coders of .1 Malagasy enJemie: Takhtajania perrieri \\ interaceac Ann. Missouri
Hot. Card. 87: 297-302.
Takhtajan. A. 1987. Svstema Vlagnoliophy lomin. Olicina
Kditoria "NAUKA." St. Petersburg.
Taylor. I). \\. ^ I.. J. Mickey. IW2. I'hy logenetic evidence lor the herbaceous origin of anniosperms. 11.
Syst. Evol. 180: 137-156.
limine. I! f. I'XP ( la-sificul ion and geography ..I the
flowering plants. Bot. Bev. 58: 225-348.
Young, D. A. 1981. Are the angiospernis primitively vesselless? Svsl. Bot. 6: 313-330.
WINTERACEAE EVOLUTION:
AN ECOPHYSIOLOGICAL
PERSPECTIVE1
iew partly arises from iheir lack of xylein vessels. fSeeause xylem \
s, limited to wet forest habitats where their traeheid-based wood do*
sion of the Winleraceae fossil record into the Early Cretaceous s

gical history than can he deduced from their current distribution.
functional significance and selective |.rewires underlying the pal
onsistent with their ecological success in wei. temperate environme
The first angiosperms liave liccn traditionally

portrayed as slow-growing trees characterized 1>\
"primitive" morphological features and confined to
wet tropical environments (Bailey, 1944; Takhtajan,
1969; Carlquist, 1975; Cronquist, 1981). According
II, a-l modified desi-erdeiits <: tin- >i\ polhi i . .n i
giospcrm ancestor (van Tiegh.-m. I'>()(); ' homp-oi
& Bailey, 1916; Bailey & Thompson, 1918; Bailey,
1944; Smith, 1945; Takhtajan, 1969; Thorne,
1974). A major reason for this association is the
Tieghem, 1900; Bailey & Thompson, 1918; Bailey,
1944; Cronquist, 1981; Carlquist, 1983, 1987,
1996; Gifford & Foster, 1989), although the presence of other pulativek primitive morphological
aspects of their morphology and ecology would not

be disadvantageous (Bailey, 1944, 1953; Bailey &
Nast, 1945; Smith, 1945; Takhtajan, 1969; Carlquist, 1975, 1983). In particular, Winteraceae have
been d s. ribed a- iimih d lo uuderslon habits well
"!
Eakhri Bazzaz. Chuck Nell. Tun Umdrihh.

.Ionian. I illine O'liricn. I'orler I* I .own
2
suited In then presumably inefficient xylem, with

thou survival further enabled by the evolution of a
distinctive leaf-level feature, i.e., waxy pluggi d -I>
mata (bailey, 1944, 1953; Bailey & Nast, 1944;
Baranova, 1972; Carlquist, 1975, 1996; Cronquist,
1981).
Recent findings on the phytogeny of angiosperms
and the paleoeeologv and physiological ecology of
Winteraceae challenge the idea that Winteraceae
represent an unchanged lineage (Young, 1981;
Donoghue & Doyle, 1989; Doyle et al., 1990; Chase
et al., 1993; Crane et al, 1995; Soltis et al., 1997;
Nandi et al., 1998; Feild et al., 1998; Doyle, 1998,
2000; Mathews & Donoghue, 1999). Our goal in
this paper is |o review Winleraeeae's ecological
characteristics in relationship to historic;, changein then distribution and climatic associations. In
particular, we fo. n- on how physiologii 8
combined with paleoecological and biog. .
I
Jim.-
en
e^-i-lb-- .. i..l
l'| .
imjiact of the re-
discovery of Tahhtajania perrieri (Capuron) Baranova & J.-F. Leroy (Schatz et al., 1998) on our understanding of the ecological evolution of the
\\ intent! eae will also be onsidered.
'I
\U ( <.l.l>. Michael I lonoghue. Jim l>mlc II. <
I HI
ill
fell,I. languv .hlfic (,n
II. George Schatz. Leonard Thien, and Matt Thompson.
Department of Organismic ami Evolutiouan Hiologv. Cambridge, Massachusetts 02138, U.S.A. Author for corr
.:.
VIA
:;.U. :><>i)n.
Bubbia (?33 species)
Australia, Lord Howe Island, New
Shrubs, treelets, to large trees (15 i
>ntane cloud forest, ma

rainforest, paramos
1 subtropical lowland r
forest, tropical montane cloud forest

Subcanopy trees in subtropical lowland
rainforcM and montane cloud forest
ECOLOGICAL CHARACTERISTICS OF LIVING
WINTERACEAE
found only in cool montane forests of northeastern

Madagascar (Schatz et al., 1998).
Winteraceae, with 65 species in four to six genera (Smith, 1942, 1943a, b; Vink, 1988; Suh efal.,
1993), are a dive
|
,h
-leaved epiph\tes.
terrestrial alpine shrubs and scramblers, large-
Wi
^rêae are most diverse in subtropical re-
^S <**- 197< 977' 1985' ^ buJ ^"

icall
y more successful in terms of their abundance
temperate environments. Within the subtropics,
Winteraceae are found in areas with abundant pre-
leaved understory treelets. and medium-sized (~

20 m tall) trees (Smith, 1942). Although generally
limited to wet habitats (rainfall > 1200 mm/year).
;Pltatlon and/or 1(>W evaporative demand such as

6 rivers< in understory habitats, and in everwet
'
- I 1942, 1943b; Vink,
they can be found in a variety of habitats ranging

from subtropical montane mossy rainforests to cool
coastal and montane temperate rainforests, and
subalpine and alpine shrubberies. Tasmannia Ianceolata (Poir.) A. C. Smith is an exception that occurs as a small tree in moist sites such as gullies
and stream margins in dry sclerophyll-dominated
woodlands (rainfall about 800 mm/year) in Tasmania. The current distribution of Winteraceae follows
a southern Gondwanan geographic pattern with
most species and genera in Australasia (Table 1;
Raven & Axelrod, 1974; Schuster, 1976; Raven,
1980), excepting Drimys granadensis L. and Tasmurium piprrita Hook., which currently extend into
regions outside of Gondwana. Drimys is the sole
genus represented in the New World, where it occurs from cold, we I VI .. I
imtoiests in southern Chile and Argentina to the tropical and ternperate highlands of Mexico (Veblen et al., 1995).
Finally, the monospecific genus Takhtajania is
1970 1977 1985 1993

'
<
'
' ***. 1995>- Populations
of man
y Winteraceae such as most Bubbia and
Zygogynwn species in the subtropics consist of
onl
y a few individuals (Smith, 1942; Vink, 1977;
Pellmvr et al
- 1990)- A potential contributing factor to tms
lw density may be the tendency for limited seed
production due, in part, to infrequent pollin
ator visits (Sabatinca moths, Palontus weevils;
Pellmyr et al., 1990). Most species of subtropical
Winteraceae are tolerant to shade and occur as understory treelets (1^1 m tall) and infrequently as
subcanopy trees (to 10 m tall) that become established late during succession (Vink, 1993; T. S.
Feild, unpublished obs.). Many of these treelets
have exceptionally large leaves (15-30 cm in
length is n<>l
uillv in Belliolum)
compared to other Winteraceae from cooler climates, which cause plants to appear "top heavy"
and susceptible to breakage (Vink, 1970, 1993; T.
S. Feild, unpublished obs.). Another characteristic
alon
m
Volume 87, Number 3
nnd
vegetatively by stem sprouting. Tasmania
in New Guinea is reported I
'! . .
,
!\
11. cics are known
to reproduce by subterranean stolons (Smith,
1943b; Vink, 1970). Profuse stem sprouting, resulting in multiple-branched plants,
bia, Drimys, Pseudowintera, Takhtajania, and most
species >: T>isn,iir,n;a (\irik. I'>70; l.'aleigl e: a...
1994; T. Feild, unpublished obs.; G. Schatz, pers.
coram. 1998).
The view of Winteraceae as an ecological I \ r
cled group is iiii(i< H!' to i
nle with its high
mperate rainforest habitats (ca.
vith frequent frost and some
. \\ mleraceae species can
dominate the understory and subcanopy as well as
grow in exposed habitats. For example, Drimys winteri forms dense -u
,
kcts in coastal Chilean temperate rainforests ami o< curs Ire i icr' itrunk diameter (Lusk, 1993). Winteraceae are also
pint and alpine
communities of Australia, Chile, New Guinea, and
New Zealand, where freezing can occur at any time
of the year (Vink, 1970; Barry, 1980: kirkpalmk.
1983, 1997; Veblen et al., 1995). All four major
a Drimys. Pseudowintera. and Tasmannia. as nt'eind I'min mole
nlar phylogetielic :.>ia', -- isa g ITS rl)\ \: Snli et
,
al.. 1 >93) contain specie- thai grow as small-leaxed
il.au i<e an. I i i, 11.111.1.
lieel.uU. p. become estah-
lished (Rebertus & Veblen, 1993). However, with

distance from the coast, Drimys abundance decr< ases rapidly, perhaps reflecting a reduction in
water availability (Rebertus & Veblen, 1993). Early
other temperate taxa. Tasmannia lanceolata is an
abundant colonizer of open fields on the central
hasali plateau of Tasmania. whi< h lias IV'<pi'iit frost
in the winter (Read & Hill,
forms dense thicket
dry sclerophyll woodlands (~ 800 mm rainfall a
year), and on slopes of wet eucalypt gullies (Vink,
1970; Raleigh et al., 1994). Tasmannia piperita
dominates forest ,
, rainforests and
i ei eha'e:- n le lros| s)i iekeii grasslan<ls 3000 m) in New Guinea (Vink, 1970;
:'
min piperita is also common
on landslide-exposed soils in montane habitats
(Hope, 1980).
To understand Wir
al iudi\
11 it I .pa '.II
temperate
ical patterns of Winte]
I (ilogtl ' I
(< 1-3 cm long) shrubs and small trees in high-
sidered. The extensive recovery of Winteraceae

lossil polli-n ii,
I
hat Tertiary and
Hope, 1980; Nunez et al., 1996). In Tasmania, Tasmarmia lam eolatn occur- a> ,,,
shrub (e.g., approx. 45% cover) on roek\ scree
slopes well above the eucalypt and Nothofa{
lines, where it is found alongside conifers such as
Diselma (Cupressaceae) and '*
I
paceae) (Gibson et al., 1995; Kirkpatrick & Bridle,
1999). Drimys granadensis grows as a multiple
bra
rai eae) dominated wet paramos of Colombia (Smith, 1943a). In
New Zealand, Pseudowintera colorata and P. traversii grow in the eompan\ of < oi iters on alpine plateaus and mountain tops, where they are gregi
a
colonizers of landslides (Stewart & Harrison, 1987).
Within these temperate habitats, Wintei
appear to be good competitors. Rebertus and Veb.nil'"'' r< [ ' . ia in P , > , interi produced a
siil.-I mti il rain of viable seeds, and seedlings grew
rapidly in response to forest gap formation, impedof Nothofagus
vessel-bearing angio. Drimys apparently requires large-scale dis-
Winteraceae (Coetzee & Muller, 1984;

Coetzee & Praglowski, 1988; Dettmann & Jarzen,
1990; Doyle et al., 1990; Dettmann, 1994; Macphail et al., 1994; Doyle, 2000). The oldest AusI i
i
I i ' i I - .
in southeastern \iistra(Detb
i 0), indicating that, at 80 Ma BP, the g< graphi.
range of Winteraceae corresponded to the Southern
Gondwana flora province of Brenner (1976). This
region was a moist, i iol temperate re- u domaial
ed |,\ i r.nifers (Podoearpaeeae, Araucariaceae) and
lalei included tin mstral mgiosper ms \<>ih<>tai:sis
and Proteaceae (Axelrod, 1984; Dettmann & Jarzen, 1991; Spicer et al., 1993; Srivastava, 1994;
Hill & Scriven, 1995). Specht et al. (1992) suggested that during the Late Cretaceous. Wintera. . no Ion- w ill Ii III etiiai < :ie. I!r\ ( Xrnulo1 ,a >ir\,
and Proteaceae, were understory shrubs growing in
temperate lowland forests (mean annual temperature ~ 12C) (loin in
I
i "Ii
ips .im\ protea
ceous trees (<-.g.. '
W
>iia) fhese lot
Winteraceae shared a similar
Winteraceae
figure I.
I
Phylogenetic hypothesis tor lli.
I, , il
al.. I',','l Nolle A is
node li represents the
ttmleraeeaeas well a^
|>..Men taxadislnlmled
i.-iaimn
I
l'><0) .,1,1 I an. Ila.eae K.has,- et
the split from Canellaeea. . while
lineage t ll.lt ga\e Use le all e\t.ini
l.aleCrelaeeuns anil Tertian fossil
in \iistralasia (I )> le et al.. IWO).
Australia and Antarctica: h.meyei, HO modern analog of this forest community exists today (Specht
et al., 1992; Dettmann, 1994; Hill & Scriven,
1995).
Understanding of the elimatic and geographic
distribution of W i > .. , . . greatly enhanced
l>\ the discovery of considerably older winteraceous
pollen (Late Barremian-Early Albian, 125-105 Ma
BP) in several localities well to the north of Southern Gondwana (e.g., Israel and Gabon (Walker et
al., 1983; Doyle et al., 1990; Brenner, 1996)). Cladislic similes of these fossils indicate that the
plants that pmdu. ed ihcni w. < niore [Mini live than

I IK coiiiiiion al)< estoi ol I .ale < aviaeeniis. |, than.
and modem genera ol Winteraceae (Fig. I: Doyle
et al., 1990). Surprisingly, these putatively related
tetrads occurred within the Cretaceous subarid
tropical liell .; i .."i -r imlu ma Doyle et al..
1990; Srivastava, 1994; Brenner, 1996; Doyle,
2000). A major implication of these fossils is that
the Late Cretaceous Winteraceae and their extant
i> - nd< in - i
p<
i I i inch from an inilialK tropica I n. e . thai -pre: d -oalhwaid Men
Northern Gondwana (Fig. 1; Doyle et al., 1990).
Thus, the Austral
I include the current center ol Winteraceae diversity such as \ev\
Caledonia, (Vink, 1993), arc not the cradle of Winteraceae evolution (Dettmann & Jarzen, 1990;
Doyle et al., 1990; Dettmann, 1994).
A Northern Gondwanan origin suggests thai early
Winteraceae were lik.lv to have experienced substantial changes in climate during their migration
into the Southern Hemisphere. Two migratory
routes into \usiia . ,ia -.; |>< a: :>l,n. -ml. . based on
known distributions ol fossil winteraceous pollen
(Fig. 2; see Doyle, 2000, for more discussion). In
the first of these scenarios. \\ iiileraceae reached
\ustralasia through an overland dispersal corridor
thiil in. hided temperate South America and Antarctica (Raven, 1980). An alternative scenario is
that the wet temperate Winteraceae lineage originated and radiated in Africa during the Middle
Cretaceous (Coetzee & Praglowski, 1988) before
dispersing first to Madagascar, and then via overwater dispersal into temperate \ustralia with Antarctica providing an overland route (Fig. 2B). Presently, it is not clear which of these scenarios is
more piokih e I > < an ..- ol ih. huge temporal g;ip
(~ 25 Ma) in fossil pollen data between the first
appearance of winteraceous pollen in northern
Coiidvsuna and the occurrence of fossils res. nil.I ug
<l ' le
et al., 1990; Dettmann, 1994; Macphail et al.,
1994; Doyle, 2000). Local extinction of Winteraceae, implied by fossil pollen in Africa and central
Australia, makes interpretation of their biogeography especially problematic (Coetzee & Muller,
1984; Macphail et al., 1994). Regardless of the
route taken to reach Aiisi I ,
||ei
re core Hid M-I - thai <-\i ail W nleracoae were den\ed from an ol igm ilK hop .-.A In , age i . ' in
grated into relatively
', features of this family i
A. South American Origin
B. African Origin
Approximate present day

continental/island boundaries
Land
Center of origin for modern Winteraceae
Two |>alftfni;r.ifihic- In polioses for the center

fossil pollen closeh it -till)] ing n
ikhlajania in Madagascar, dispersal to Africa
Noriheni < ioiidvvana (1). To accoui
Irmpetale \\ inleraceae in Africa (possihly

ustralasiai regions (2 and .''.!. Stars indicate
tides and/
oi :hc stoMiata ate sunken ml > 'lie aiiasia I. il -in
face (Bailey & Nast, 1944; Baranova, 1972; Bongers, 1973). Perhaps llic most vii*i;ig '!..n !- i
xeromorphv i> I lit
ore with a granular
imposed of eutin and wax (Fig. 3; Bailey
; i
& Nast, 1944; Baranova, 1972; Bongers, 1973;
Feild et al., 199f' 11
i
i
n
. ,i i
for the characteristic white reflective appearance of
the urn lei surfaces of Winteraceae leaves (Bailey &
Nast, 1944).
The diversity of stomatal ornamentation found in
Winteraceae is enormous (Bongers, 1973). In Takhplugs i
(Fig. 3A;
1972; I
ofs
guard cell runs (Ymk. 1970; Bongers, 1973). The
ahaxial epidermal surface- ol l)nm\s
Miers and sonic entities of Tasmannia piperita are
covered with dense overarching papillae formed
from extensions of the eutieular laver (Smith,
1943a; Bailey & Nast, 1944; Bongers, 1973). Finally in some Rubhia and Zygogynum species, the
stomatal apparatus is completely buried under a
mat of encrusting wax rodlets and an additional
(Bongers, 1973; Metcalfe, 1987; Vink, 1993).
A long-held belief has been that stomatal plugs
ml tl
ihei
i
roim |>hi< leaf features
of Winteraceae function to restrict water loss (Bai-
stoma of Takhtajania perr

waxes. The s in.ila. which arc unhealed l.\ the .
/:.
el',, '.",.,
> ,xm (A & C) and 20
ley, 1944, 1953; Bailey & Nasi, 1944; Baranova,

1972; Carlquist, 1975; Cronquist, 1981). As anti proposed to have
r the presumed inferiority
of a traeheid-based transport system (sec below;
Bailey, 1944, 1953; Bailey & Nast, 1944; Baranova, 1972; Carlquist, 1975; Cronquist, 1981; Sperry,
1995). Stomatal plugs also oeeur in most Southern
Hemisphere euiiiiei-.. such as Araucatiaeeae, (aiptessaeeae. Podnearpaeeae. a^ well as maris northia
k.i.
i
plugs and the
absence of xylem vessels (Jeffree et al., 1972; Yoshie & Sakai, 1985; Wells & Hill, 1989; Stoekey et
al., 1992; Carlquist, 1996; Stoekey &
1993; Stoekey & Frevel, 1997; Brodribb & Hill,
1998; Stoekey et al., 1998).
The hydraulic compensation argument has been
appl ed to \\ mleraeeae loi mam \eai -.. despih tin
afifecl i
- ,f I. a: g
iheir name suôS, -l->tn '> plugs are not solid.

but riddled with air-filled pore- formed between
lubes el . II! ii an ! -i ii a I u â\ > i -I ib (I'M iu'< IS.
1973). Although a porous construction is necessary
locked in .illume.it- oi pt<>>
III
, | nati-.piralii.ti i.
tarding effects. Recently, Feild et al. (1998) examined how these structures influence water loss
rates from Drimys winteri var. chilensis (DC.) A.
Gray leaves. Comparisons of plugged and "un>lugg< <l " le i\. s (leaves (nun which si
I i I i->
rid -- i ii. .1 , nil. sl.it waxes were experilllenl;.;ll\ iviii. '. ed) :' 'ii inflated that n del aign relali- c liiinii.lih !o .' ' I |i| ic- nosed ,i te|;,|i\cb small
resistance to leaf water loss (Feild et al., 1998).
Maximum stomatal conductances of Drimys leaves
with sintml,Jl ping- were about MY/, lower than
leaves from which the stomal.d plugs had been exi.tno\cd. Maximimt conductances of
naves (approx. 100 mmol H20 m 2 s '),
although lower than inanv lowland rainforest trees
and crop plants, were similar to those reported from

other montane < oud lores! angiospcnns (Feild et
al., 1998). With exposure to progressively greater
e\ apnral \' den and, ll:e water loss rain- of Dr.iti s
leaves with plugs compared to ones without plugs
markedly div ergce. I ttplugged leaves \hihiied :
70' r di rime n -lonial I ontjui t.mce w :, ;:<. . ,i>ing ambient re la! m h m
(from 105to35mmol
observed in Tnsn,, ,,. . <n <>l<n Small trees of

T. !.!-.. Jiiid that occur in eucalypt gallery forest
understory and subcanopy, where they encounter
frequent leaf wetting from canopy drip, have wax
rodlets associated with their guard cells. In con1
I I his species growing on exposed ridge tops m alpine healhlands, which could
reported for a wide valatal occlusion. In cons of plugged leaves (le-
n i l\ benefit from
lack any epicuticul
matal apparatus (Feild, unpublished obs.).
These functional considerations provide a new
perspective of the selective forces that may have
Win-eae. The observation that stomatal plugs, at
t in Drimys, do not apparently protect leaves
i drought is not consistent with the idea that
nd the guard cells that uncouples the guard

cells f
it conditions, or plugs may retard
by physically interfering with
lents (Feild et al., 1998). Regardless of the exact mechanism, these results provide
i .
i. al evidence that stomatal plugs in Drinivs cannot IK I nlanls \v ilh vessels

(such as some Myristiraiêae and Epacridaceae;
Koster & Baas, 1981), an.d without vessels (as in
many rainforest conifers). All these plants occur in
wei i<:. si habitats. In addi lion. .Kiel vesselless angiosperms such as Amborella, Tetracentron, Takh-
riety of plants lacking

trast, stomatal conduct
creased 10% over tl
humidity, from 100 to 90 mmol H20
et al., 1998). The mechanism
plugs prevent stomatal closure
sible that plugs may interfere
of stomatal plugs appears to be related to the occurrence of Winteraceae in areas that are generally
wet (rainforests and cloud forests). One of the inevitable consequences of frequent rainfall and
cloud cover is prolonged welting of leal surfaces
(Brewer & Smith, 1997). Because C02 diffuses
through water 10,000 times more slowly than in air,
water films on leal surfaces can create a high resistance to C02 diffusion into leaves for photosynDrimys leaves exposed to mist demonstrated that
stomatal plugs allow relatively unpertuibed photoi 1 i
i
i
IK ti leaves are < \pos< d to mist
(Feild et al., 1998). Specifically, photosynthetic
electron transport rates decreased app
n i i
* of Drimys leaves that lacked
i;.-d gas .--.a hatige \\h. ! Ic i, is a:v wet because water droplets are repelled from the stomatal
apparatus (Feild et al., 1998). These water-epidermis u ieiai I mris k'<-p tin stomatal pore and ititercellular spaces from heitig filled .villi wafer, which
can occur when leaves are exposed to fog (Brewer
& Smith, 1997). Further support for the efficacy of
stomatal waxes in shedding excess water has been
II i 11 plugs or other waxy structures obstructing

the stomatal apparatus (Fig. 3A; Metcalfe. 1087:
Brodribb & Hill, 1998).
Perhaps the best-known feature of Winteraceae

is the lack of v
their wood (Bailey & Thompson, 1918; Cronquist,
1981; Gifford & Foster, 1089). Instead, the waterconducting system of Winteraceae is composed entirely of tracheitis \csscls are also absent in a
number of other angiosperm groups such as Amborella (1 species), Tetracentron (1 species), and
Trochodendron (1 species). Tracheitis are xylem
cells that lack cvtoplasm Mich thai their lumen provides an unimpeded path for water flow. Water
between tracheids. however, requires
cell wall:
1983). The primary path for wate
tween Iracheids ate pi! depressions in the secondary wall, which although porous
provide some
1983). In
ducting tubes generally larger than tracheids both
in
ami diameter (Carlquist, 1077): Ximmermann, 1983). Vessels consist of files of cells, with
med a vessel element, thai unlike tracheids

bslatiliallv tiio<liliel axial walls or perforates that allow for a more open pathway of
(Bailey, 1944; Carlquist, 1975;
1983; Gifford & Foster, 1989). Ves-
tracheids, sueh that the pit i

dmlv/ed l.etween the end walls of adjacent eells
(Ciflord X Foster, 1989). Vesselless wood has tra!a
-i.1,-,,-,1..
lure i an-nospe,n,s uan Tieghem, 1900; Bailee A
Thompson, 1918; Bailey, 1944, 1953; Carlquist,
1975, 1983; Cronquist, 1981). What has propelled
tins idea is the assumption that vessels represent
such an adaptive advantage thai llicii suhse.|uenl
loss is highly improbable (Carlquist, 1975). With
the evolution of xylern vessels, botanists have argued lli.il the i ath ai ginspern S were J e to . q.lni:
habitats wild uncertain water supplies and develop
growth-enhancing traits such as large, undissected
leaves and greater gas exchange rates (Carlquist,
1975; Doyle & Donoghue, 1986; Bond, 1989). By
wet cloud forest habitats

(Carlquist, 1975, 1983, 1987).
The view that Winteraeeae are primitively vesselless has been challenged by phylogcnctic analyses (Young, 1981; Donoghue & Doyle, 1989;
Chase et al., 1993; Mathews & Donoghue, 1999).
Cladistie analyses indicate that the first angiohad
whii
were subsequently lost i
lines (Young, 1981; Donoghue, 1989; Donoghue &
Doyle, 1989; Doyle, 1998). Although molecular
phytogenies impl
m<l Nvmphaeales
are likely to be t
I9))|. belli Wuilera.eae and Troehodendrales are
nested within clades containing plants with vessels.
Winteraeeae are most closely related to Canellaceae, and Trochodendrales are included within eu<licots (Chase et al., 1993: Soltis et al., 1997). To
assume irreversible vessel evolution requires more
evolutionary steps by additional independent origins of vessels in angiosperms (Young, 1981; Donoghue & Doyle, 1989). While the parsimony debt
incurred by assuming that vessels cannot be lost
was not overwhelming, this conclusion implies thai
the functional arguments lor such an assumpt
should be examined (Donoghue & Doyle, 1989;
Mathews & Donoghue. 1999). The cladistie arguments supporting vessel loss in Winteraeeae have
. y.lui .ii.ii v los. ,,| vessels, other than a shift to

aquatic environments, as this would entail a shift
to an inefficient hydraulic system (Carlquist, 1983,
1996). However, claims about the likelihood of vessel loss m Winteraeeae need t.. be evaluated in a
physiological context.
In support of this view, Donoghue and Doyle
(1989) argued that little support exists for the view
that vessel loss m Winteraeeae is likely to have
been selected agamsl. first, the forests with low
evaporative demand where most Winteraeeae currently occur were suggested to be the type of habitats, where anv decrease in xylern transport Capacity by vessel loss would have a relatively small
effect (Donoghue, 1989; Donoghue & Doyle, 1989).
Donoghue (1989) also suggested that the first vessels, hypothetic-ally present in an ancestor of Winteraeeae. were presumably of a primitive moiphol
ogv containing numerous sealarilorm partitions,
limited in number, and in a background ol functional tracheids (Donoghue, 1989; Dom uh A
Doyle, 1989). At this stage of low evolutionary spevessels may not have been
difficult, entailing <
branes. For e
consequences of
having only tracheids versus having both tracheids
when Winteraeeae are
relatives, ('.a
nellaceae. Most Caiiellaceae vessel elements are
similar in si/e and overall shape to Iraelieids of
Winteraeeae (Wilson. I'X.O). T.acheid diameters
(16-69 pm; Patel, 1974; Meylan & Butterfield,
1982; Carlquist, 1981, 1982, 1983, 1988, 1989) of
Wuiteracae overlap with the lower range of vessel
element diameters reported from Caiiellaceae (20140 ixm; Wilson. I960; Metcalfe, 1987). Xylern
conduits in Winteraeeae and Canellaceae differ in
that the pit membranes are retained in Iraelieids of
W inleraoeae. while in vessel elements of Canellaceae scalariform perforation plates are developed.
Some Winteraeeae species show an intermediate
i dt! in where the tracheal pit iiieinbr; s are
partially dissolved, forming relatively large porosi< ..vipatal :v
irlei
Although it is difficult to determine the importance of specific selective pressures in the past,
functional and physiological studies can indicate
what factors might have been involved. Combined
niation from historical biogeogr.i: I . ear
tional analyses al-o provide a context toward inter-
|>r< Mug jih-. i igenelie mien nee- about the past eculogical and cliinal
i
i i
l>
et al., 1990). One common characteristic of the current distribution, ee. n il i >
nee, and paleomigratory patterns of \\ mteraceae is an association
with cool, wet temperate environments. Paleoclimatological evidence suggests that at the time Winteraceae moved into Australasia, these southern
high-latitude regions may have been colder than
previously suspect.
ding some regions with persistent snow cover and frozen ground
(Rich et al., 1988; Ditchfield et al., 1994; Sellwood
et al, 1994; Stoll & Shrag, 1996). Where freezing
temperatures are common, traeheids appear ad\ antageous over vessels in terms of their resistance to
freezing-induced <a- iri i ill
. II. 1967; Sucoff,
1969; Sperry & Sullivan, 1992; Sperry et al., 1994;
Tyree et al., 1994; Davis et al., 1999). When stems
free/.e, the insolubility of dissolved gases in ice resuits in air bubble.
...
act as nueleation sites for the formation of air-embolisms blocking the movement of water through
stems (Hammel, 1967; Sperry & Sullivan, 1992;
Hacke & Sauter, 1996; Davis et al., 1999). The
probability of a freeze-thaw event resulting in xvlem embolism correlates with conduit volume
(Sperry & Sullivan, 1992; Sperry, 1995; Davis et
al., 1999). This is because a greater conduit volume
results in both rnon m m n i - ai ! I i r
i i
bles, which can easily expand to fill the entire xy
lem conduit during the thaw of xylem sap.
Most conifers are resistant to freeze-thaw-in
duced captation irrespective of the number o
Ireo/ing cents experienced because of their tia
- system (Hammel, 190<: Sucoff. l96);Kohso,,etaL l'J8:Sp-m vN -nil,van.
1992; Sperry etal., 1994). In traeheids, the bubbles
produced in frozen sap are sufficiently small that
\
,,,,,.
.
the-, are collapsed |,\ surface iension din n- ili.r.i
to that of co-occurring conifers such as Ihselma.

I
Drinns u interi in
southern Chile is also reported to he more tolerant
to frost than Nothofagus species growing in the
same environment (Alberdi et al., 1985). One part
of the observed tolerance of Winteraceae to freezing
may be the ability of a tracheid-based xylem to
avoid freezing-induced limitations on stem water
transport.
Despite the central position of xvlem structure in
discussions on the evolution of Winteraceae, no
published reports exist for the hydraulic performance in the held. Clearly, comparative studies of
xylem properties and water flux rates under field
conditions are needed. However, the selective forees on wood evolution are not confined to hydraulic
efficiency. Safety, with respect to avoidance of air
embolisms, and mechanical strength are two additional selective pressures on the direction and pattern of xylem evolution in plants (Tyree et al.,
1994). Certaiulv smaller x\ lem conduits ..il. r higher resistance to water flow. Nonetheless, in colder
climates traeheids appear to increase the overall
hydraulic capacity by minimizing embolisms by
liee/e-lliau e\enls (Sperry et al., 1994; Davis et al.,
1999). This advantage for small-diameter xylem
conduits for evergreen woody plants subject to
freezing temperatures may explain the loss of ves-
ologv. historical biog. n-raphx.

I'^-'"'"^ challenge the long-held belief that Win*raoie * il" unchanged and relictual angios erm hnea e
P
.,
Further
'nvestigati
.;
i Winteraceae
u
morphological
; with respect to their natural environments
iliriue to inform (lis
.,.1 i
g "
ing. In contrast, many vesselled angiosperms, and

espeeialb those wiili large conduit volumes, cm
bohze extensively following one or more freezethaw events (Sperry, 1995; Pockman & Sperry,
1997; Davis et al., 1999). The tradeoff between vulnerabilitv to freezing-indaeed cavitation and conduit size may have infl tenced the direction of xylem evolution in Winteraceae (Donoghue & Doyle,
1989; Donoghue, 1989). Indeed, Winteraceae have
'
.
,
, ,
r
,
been documented to be relatively more frost tolerant compared to co-oecurnng plants with vessels.
Sakai et al. (1981) demonstrated that the freezing
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\lberdi. M..
Altitudinal
Nothofagus
v "^<" 0: 21-30.
\xeh(.d. I). I. 1<)!!1. \n ml.M.c l.iii-n of I rcl.i. cu-aii.l
Tertiary ,)i()ta in |)olar regions Paiaeogeogr. Palaeoolimatol. Palaeoeeol. 45: 105 147.
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& B. C 1- Swamy. 1951. The conduplic
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!a,l'|u -I- S. 1075. Ecological Strategies of \x Km \-At)
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Xylein Structure and the As-
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ANATOMY OF THE YOUNG

VEGETATIVE SHOOT OF
TAKHTAJANIA PERR1ERI
(WINTERACEAE)1
M,-:.,,!,-.!! -
Richard c. Ke
! i- weaklv differentiated. Petiole bases arc vascularized by three

ire pseiulosiplionostelie and lia\e little scleronchyma. Within I
appear to be nearest this level of specialization, mostly on the
Phylogenists have long considered Winteraceae

to be among the least specialized in the angiosperms (cf. Taklil; |.in. I'>*>T>. \mong analyses supIII
i I i
n
'
I !-M| on tin pn sence of vesselless wood (CatUpiist. ]')83: van
Tieghem, 1900), a mixture of sieve-element plastids
(Behnke, 1988; Behnke & Kiritis, 1983), pleomorphic floral structure (Krbar & Leins, 1983; Endress, 1983; Vink, 1988), and paleoantarctic distribution (Smith, 1945). Takhtajania, the rarest and
most recently recognized genus, has been known
only from dried type material. It is isolated from
other Winteraceae geographically and morphologically. Only recently has liquid-preserved r t I ; 11 < r i. i i
hen available in support of a detailed studv ol itmo p i I
I
i
m\ The most important questions to be initially considered were (1) what is the
place of the genus among its likely neighbors, and
(2) what is its level of specialization within the
woody Ranales.
The original Takhtajania collections wen- made
in Madagascar in 1909 by Perrier de la Bathie.
I'li.-v aw a ted examination a! V a - il'i until ( .apuron (1963), finding them to represent a new taxon
of Winteraceae, named the .
rieri. Later study of the leaves by Baranova led to
.
fieri'and its recognition as the
> mi I
M i
',!/ (< apurnnl
Baranova & J.-F. Leroy. At the same time, it was
placed in a new subfamily Takhlajanioideae bv l..i
oy (1978). The species rt

s geographically isolated from other known genera of the family.
After repeated attempts over the past 25 years
to find more material. Malagasy parataxonomist
Fanja Rasoavimbahoaka located a second population ol Takhtajania in 1994 about 150 km east of
the original locality. Then in spring 1997, the new
locality was r<-\ wit.iI b\ parataxonomisl P. J. Rakt
1 /
1 Chris Birkinshaw who collected liquid-pie-ened flowering and vegetative material.
For more detailed information regarding the mlere-imi; collection history of this taxon, see Schatz
(2000 this issue).
At the Missouri Botanical Garden, the preserved
material-- were divided among several investigators
who are contributing observations on wood and repmdinlive organ-*. This contribution includes ob-enation- on leaf vasculature from clearings nd
tran--cclions of the leaf lamina and midrib. p< tiob
and nodal anatomy, and other anatomy of the young
vegetative shoot.
MATERIAL AND METHODS
Specimens of vegetative and flowering material

wen- collected in the Anjanaharibe-Sud Special
Reserve southwest of Andapa in northeast, in Ma !
agasc ai as lollows /' ./. RahotomtUaza et al. 1342,
and C. Birkinshaw 483, 1445'S, 4928'E, at 1200
m altitude m a perhumid forest with abundant moss
,a,ik Thomas K Wil-ou. Miami I mvcisilv. Oxford. Ohio, for u-eful

i
i. ii KII i.l -..in. - impl. - I lis,, ll ink \\ I St, in and an a
.-ouri lUamcal Oarden. P.O. Box 2W. St. Louis. Missouri 63166. T>
ANN. MISSOURI BOI
field preserved in 50% ethanolie FA A and transferred to 70% ethanol upon arrival at the Missouri
Botanical Garden. Leaf clearings were made by an
improved method (Keating, unpublished) where
specimens were placed in cold (room temperature)
5% NaOH and then microwaved. The 750 watt
magnetron was set on defrost cycle, i.e., pulsed
Leaf out I in,

I
2\) with , dc< nn.nl
(Fig- 2B). Length/width ratio 4-5:1. Cuticle
'' I |"de,u- . . IU munded p-b^nal I 1 '>
base
""'
l Vw
) (FiS- 2C)- In some areas of older leaves cu"

g
dividers between cells,
3-7 ixm wide. Stomata abaxial only, guard cell
ticular flan es form thick
power, 2 seconds on/off for three cycles of 20 seconds. This promoted uniform clearing and avoided
boiling, which is quit.- destructive of soft tissues.
The NaOH-covered specimens were then placed in
Pairs with lm&hs 22-29 u,m, widths 18-21 jrni,

mo l
commonly brachyparacytie with four adjacent
subsidiary cells that differ only in position from
normal
epidermal cells (Fig. 2C). Occasionally ca.
a 45C oven for 48 hours during which time- clearing was completed. Specimens were immersed in
cold (room temperature) 5.25% sodium hypochlorite (Clorox) for 30 minutes until the specimen
was white. After three gentle tap water rinses, the
20%
''' *lomaUl llilv<' 5 r 6 subsidiary cells, but
""" brachyparaeytic- with regard to the presence
<* *w epidermal cells always parallel with the
guai(1 evils. Mesophyll: cells of adaxial palisade
zone
appearing compact and shortly lobed with ca.
specimen was soaked in FKI (0.2/2.0%) (v/v) in

15% ethanol for two hours until uniformly brown.
Without further aqueous rinse, the specimen was
changed to 20% CaCl2 solution and then mounted.
Within minutes, dark magenta veins contrasted
against a transparent background in the cleared
specimens.
>' sPace- SPongy tissue with numerous

cavities 2-3 X as broad as cell diameters. Air
ca 60%
P
- Venation pinnate, looped brochidodromous. Intercostal areas irregular. Higher-order venation showing incomplete and very irregular
areolation (Fig. 2D), 0-6 vein endings per areole
(Fig* 2E). Areole -i/es: smaller ones ca. 340 u,m
Cross sections of leaf lamina and midrib, petiole,

node, and \oung stem were made In hand microtome- as well as free-hand and mounted in CaCl2.
Seme seelions were mounted unstained in glycerine. Most were stained in c-resyl violet acetate, toluidine blue, Schiffs reagent, or 1..KI. Differentiation of these' dyes is sharp in the strongly ionic
CaCl2 (Herr, 1992; Keating, 1996). Two additional
specimens of liquid-preserved young stems with attached leaf base-s we,e pa.allui-cnl.edded. serialsee tioned transverseK on a rot a IT microtome at 10
u.m, and stained in Safranin-0 and Fast Green FCF.
CBSER\ mONS
10% air (avit
air
s a(>e
isohedral; larger ones ca. 2610 X 1248 \un.

LEAF TH \\SS| <TIO\
Structure weakly dorsiventral (Fig. 3A). Midrib:

'ine shallowly concave adaxially, deeply convexrounded abaxially. Cuticle smooth, thickness .5-7
M-"' (Fig- 3B|. < uii< ulai Manges absent or narrow
between epidermal cells, up to 18 |xm deep. Epidermis: ,-e-lls thin and cuboidal on both surfaces.
Stomata level with surface. Guard cells small,
oblique to and oriented toward the surface in rei
i |
i -i
lis, which subtend
tne
guard cells internally (Fig. 3D). Outer cuticular
ledge well developed ;it steunalal opening: internal
ledge not present or much smaller. No cuticular
out
The young stem expands massively withm 5 7

mm of the shoot tip causing the apical in.iistems
t-
alveolar deposits occlude the stomata! openings,

llvpndermis generally absent although adaxialmost layer of mesophyll may lack chloroplasts in
i (Fig1A). Young prime>nl i I. n i : i ph I

i el
iole bases that show early cell division and expansion. lale-rall\ am '
'i\
causes petiole: bases to remain partially fused at the
shoot apex level and to form polygonal shapes (Fig.
1C). The axillary bud is, in two observations, an
outgiowth of the adaxial side ol the- petiole of die
7ih primonlium (fig. ID). No \aseulai eonue-elious
eoulel be- followed, nor was any bud development
visible in the true axil of mem- mature nodes.
mesophyll, forming a graelual transition to spongy

tissue. Spongy cells in lowe-r me-sophvll hori/.ontalK
elongated with irregular long lobes. Chloroplasts
most densely packed in adaxial mesophyll c-ells,
gradually becoming more dispe-rseel in abaxial me-oplivll. Vii e-avilies: most larger cavities abaxial
and aligned o\ei stomata as deep substomatal ca\ilie-s extending above the- center of the- mesophyll
(Fig. 3A, D).
Midrib vasculature usualb ."1 bundles arranged

in a V-shape, one abaxial bundle and 2 or 3 lateral
bundles on earl - \ I. _ - bundles nceui
with 10-12 files ol i
i IL
1 i. i .
i ill
a convex procambial boundary. Phloem: crescentshaped strand with weak or no visible differentiation of sieve elements and companion cells. Cells
show no alignment or regularity of pattern in cross
section. Bundle sheaths a single layer of thinwalled cells, little modified from spongy tissue.
Sclerenchyma: lateral-most bundles in midrib have
1-2-layered extraxylary fiber cap outside phloem.
Secondary bundles with two lateral hbei -hands al

phloem and small strand capping xylem. Secretory
tissue: slighlb enlarged oil cells frequent in me( ,11 (Fig. 3C, E). Tannin cells in midrib area in
discontinuous row bounding phloem; some dark
smaller cells within phloem. Starch grains either
common throughout cells of the lamina, or grains
niostb in s|>ong\ cells and not numerous. In midrib, starch grains packed in ground tissue internally
adjacent to xylem points. Grains less common but
often well developed in all ground tissue in vicinity
of vascular strands.
free vein ending -I I ,-.,! , I, .n iim-l.mt i,

it..|.Mf,Tt a.vole mid five vein emlin-s. Scale lines: \. M = 1 cm: C = 50 jim; I) = 200 (Jim: K = 3(K) (xm.
Outlir
rete dis
smooth, thickness 3.6-7 |xm. Epidermis: cells
small and cuboidal, diameter ea. 22 pm. Ground
tissue: cells spheroidal, diameter 26-70 pm, loose|
aerenchyma. Intercellular air spaces at cell comers comprising
10-20% of ground tissue. Venation: 3 to 7 collateral vascular bundles arranged in V-shape (Fig.
3F). Xylem -.
i
!
.units lead to organizci! files of mi lawlem, ii)i In three cells wide
per protoxylem point. Xylem production ends at
-traighi <-i !.;>:,dlv cui;v< - . an I. J : m.ac. i . w
I unci iptieal phloem strand. Phloem: sieve elements and companion cells in tiers 1-2 cells wide.
I.mrm <<llal.nn.l .'il n .-.ii ! tl-Mie. the-e not
differentiated from ground tissue except by dark-.taining eonlei Is. Tannin . e I- i.md.mib scattered
abaxially or in radial rows adaxially. Starch grains
common in cells adjacent to vascular bundles.
Outline terete. Diameter ea. 1 cm. (.uti.le

smooth, thickness, ca 3.5 pm (Fig. 4A). Epidermis:
cells small and cub<
1 Chloi in h\ma ehloio
plasts very common in outer cortex. Cortex: ground
tissue cells mostly spherical, loosely packed with
mm i HI- i i i i i
- i . IllI i ll\ elongate, 2-3X
. II iiiaiTien . in it in---
.i \n space ca. 20% of
cortex. Pith cells polygonal and somewhat larger
than cortical parenchyma cells; air cavities 5-10%
of pith. Vascular bundles collateral. Xylem: distinct
protoxylem points at pith boundary but xylem
< 111 i k h develops < an bi; I grow In | I'odia m.
|>- i
T | >li< i is tele within 90 pm of pith I
Phloem: sieve element arrangement irregular. Companion cells not easily distinguished in cross secIan:. \\ dest pith ravs with slight tendency toward
I i dilation in il l < i m I i I ugisi lion, metaphloem
sieve element length up to 395 pm. Earb secondary sieve element lei il g'la 2'H) (iin Siev. plates
broadened, (lompanioi cells shot: or mostb as long
as sieve elements, highly variable in shape and
Sclerenchyma: no extraxylary fibers present in
small stems. In one sample, ca. 9 mm diameter,
o. . asmi I .in; . ill- I i lound phloem pe-
\. In longisection, these single

. o\erlap and .; ? contiguous for at least longer
than 2 cm. In same larger specimen, sclerotic la\. r
i, -
-ii
i I
.i
in. ler
Sclerotic
cells in 1-3 layers, heavily liquified, with up lo 20

isotropic wall layers especially well developed on
iMI * and o iter : < i icliti d v\al - Tannin cells scattered and common in all ground tissue. Starch
grains rounded, single or in clusters (Fig. 4B).
1. m liameter 9-13 |im. Grains common
i ugh
out pith and in sheath of 5-10 inner cortical cell
Stem outline in the vicinity of the

ul.nl
I mile il. In llle vi lill:J -!em
procambium appears to be a nearly c
observed in what will beeom.
young active cambium shows three t
traces vascularizing die leal base, i.e., the node
would be called three-trace, tri-lacunar (Fig. 4C)
using the origin.i
.
i idigm begun byJeffrey (1898) and carried into dieot nodal ana!om\
bv Smiioil i l()|4). However, the two specimens observed here show some intriguing dillerenecs. The
oldei si.an sections show most leaf traces appearing
double, that is, there are two proto-xylem points
causing the development of two paired traces. They
may cause a node to appear 2:2 :2, 2:2 : 1, or 1 :
2:1 (Fig. 4D, E, F). In the younger stem pieces,
which were paraffin-sectioned at 10 pm. this observation was confirmed less frequently. \h.v iun
ming the vasculature through several node- showed
Nothing was found to indicate that the individual

leaf traces, especially the median trace, have components that occur in different sympodia of the vasculature. In this material, leaf traces were well defin.-d through at least four nodes before entering a
leaf base. New leal traces appeared to arise from
undifferentiated interfascicular procambium. More
material, sectioned at closer intervals- will be needed to identilv vein sv mpodiuni branching patterns.
Following the leaf base distally from the node, the
three traces are observed to relate in a V appearance, whether or not they appeared as double at
e TS showing divided I
the nodal level. Distally, in the leaf base, the two
oguuim (Samps,,,,.
traces. Using Sugiyama's (1979) notation the Takhtajania node can be most usually figured (moving
distally into the petiole) as L-M'M-L => L-M-L =>
L'L-M-L'L. In the base of the petiole and continuing up to the lamina, the resulting li\e traces form
a marked V of closely associate i
- i I n '.>, I'IIwith the median trace forming the base of the V.
Axillary buds do not appear among the first 4-5
leaf primordia. They occur removed from the axil,
high on the adnxial -(, . >| <> nig petioles (Fig. ID).
No vascular connections to axillary buds were de-
ment of this leaf structure among the Ranales. Bailey and Nast (19441)) noted that thicker, more coriaceous leaves in Drimys have large selereids in
the mesophvll between \.i-.ul.n bundles, and Rao
and Das (1979) also reported nests of selereids in
the family, by their absence, Takhtajania shows
simpler structure. In most Old World genera of
Winteraceae, all foliar vascular bundles are corn-
l.eal '\eiialioti i
ah.in families
with elliptic leaves with entire margins. The pinnate, festooned bmehidodrnmous structure, a.cm
panied by imperfect and \ariaUc areole structure,
produces a low first-rank leaf (cf. Hickey. 1977:
158).
Metcalfe (1987) noted much variability in cuticle
texture and sculpturing in Winteraceae, and Tnklitajania\ smooth, unsculptured cuticle seems diagnostic within the family. Bongers (1973) noted
that leaf cuticles of Takhtajania and some Drimvs
species lack the alveolar layer present in all other
Winteraceae. However, Baranova (1972) noted that
"Group 2" Winteraceae, Bubbia, Belliolum. Pseudowintera, and Zygogynum, also have ordinary (=
non-alveolar) or more or less grainy cuticles. Kxisting data are not a useful guide to relationships
until comparable observations can be made across
the genera. The known leaf venation trends are not
sufficiently refined I
ne to oft.-, an opinon on
whether Takhtajania is more or less specialized
than other winteraceous species.
Leaf surface observations ilo not confirm Karanova's (1972) report of the existence of mostly anomocytic stomata in Takhtajania; instead, stomata
are mostly brachvpaia. vtic as is true of other winteraceous genera. This removes a major argument
fo, snhlainih-lcvel segregation of the genus. Also.
stomatal apertures are said to be occluded with alveolar material (Metcalfe. I'>;;7. bongers, 1973;
Baranova, 1972), but this is not true in Takhtajania
or in Drimys {Tusm
look. (Bongers,
1973).
In genera studied In- i
in hidiu
' ''>.
nia, mesophyll in the family is reported to be not
clearly differentiated ito pair- d aid spongy mesophyll, e.g., Exospermum (Carlquist, 1982) or Zyg-
1983). This weakly bifacial
Observations on nodal anatomy are not as systematically powerful as they could be, partially due
to persistent use <i| the sjphonosiele paradigm (see
review by Beck et al., 1982). partially to unsolved
iheorelical concerns regarding the reality of cauline
vasculature, and partially to the difficulties in relating nodal traces to stelar vasculature. At least for
three-trace ia- i
ving open archite<
ture, the following discussion predicates that vascular patterns arc best recognized as a cylinder of
eustelic sympodial bundles of varying niimbei. Followed from a proximal to distal direction, all of
these bundles become leaf traces at regular intervals. In terms of their origin, all so-called cauline
bundles are first identified as leaf traces. They
probably connect basipetalb to existing leaf trace
sympodia.
As seen Iron In. . . i i I.I.S older nodes and two
short pieces of stem lip available in the present
study, nodal structure places Takhtajania among
It.
i
m families II. n/
ing noted that nodes in Bubbia sp., Drimys colorala
Raoul, D. winteri J. R. Forst. & G. Forst., Canella
alba Murray, and Warhurgia ngandrnsis Sprague
are so similar that they can be described as one.
All five species showed a 2/5 phyllotaxy, which is
also coufiri e. i
lienzings specimens
showed distinct helicoid sympodia where every 5th
leaf is supplied by a median trace from the same
svmpodium. I'lus seems possible but could not be
quite confirmed from currently studied
material. The relationship of 3 traces vascularizing
a leaf to similar sets of traces above and below that
node appears somewhat unpredictable and irregular
in the available material (Fig. 5).
\bout "> mm below the apical meristem, in a
region of closely spaced nodes, the vasculature of
the young stem (onus a eustele consisting of precociously matured xylem strands, here interpreted
Volume 87, Number 3
from "interfascicular parts of the hypothclic;il. ran

line |)iiman vascular cylinder." Also, Beck et al.
(1982: 795) stated, "There are 5 protoxylem strands
in Drimys winteri that apparently represent axial
bundles
" Both of these conjectures cannot be
related to the present observations. In 7ônly leaf traces can !< discerned when following
vasculature through 4-5 nodes. There are no sets
<>f > pmloxylem strands at any level.
Beck et al. (1982: 795) also stated that, while
tarn i-
a 'VH i iln l n :ru I <>d< d la:, ,,, , , ,
i D. winteri one lateral t
.,:i . ,(1,r.
the s
acent axial bundle."
ania can be observed or interpreted this
a similar line of reasoning, Howard (1974)
hat some workers refer to cauline bundles
e that persist in the stele through several
This definition appears somewhat arhilrar\
lolloped through several nodes,
leaf
. at least in these raualian genera
' 5.
Takhtajania pcrricri: diagram of -hoot
il -eclroii-. KuMelic bundle- appear in<: a- -
as leaf traces, embedded in a e\liudei of procambium. Usually, the clearly defined vascular bundles
occur in pairs or threes, rather than as singles. The
'! -hows
that lateral and median leaf traces arise independently. All of the closely associated trace pairs do
not arise from different sympodia as far as can be
followed. All are superficial bifurcations arising
distal to their identih as -ingle incipient traces in
the proeambial cylinder.
An urgent need is the diagramming of the vasto see if the type of sympodial arrangement of terminal traces am
u<
i i In
i n i
I. i
i families can be
confirmed. From the three short siem pieces available for this study, such an integrated pattern canAs noted above, several relevant studies have to
he translate : from [he ca :ie \;is< ulature concept.
In Bailey and Nast's (1941a: 215) study of the Winteraceae, the\ MILL- I. I i > it i li
,i. i II. - . -.
Takhtajania, nor does it agree with Benzing (1967).

In that work, it can be seen that the essence of
vascular sympodia is that all so-called cauline I.undies arc leaf traces, and the number of nodes along
the way between a bundle's origin and its orientation into a petiole base does not change this defiranalian shoot were interpreted consistently in
terms of the primary vascular system in order to
avoid artificial concepts and terminology (Esau,
1965).
The present observations of a pair of tract's related to the median gap are a first report lor \\ m
teraceae, nearly fulfilling Takhtajan's (1964, 1969,
1991) conjecture of a hypothetical nodal type,
-perm-, but 1 I !n 11 n "- f .-d
n of a 1:2:1 set
of traces varies from Takhtajama's potential for
having pairs at the lateral gaps also (2:2:2, 1:2:
2). Swamy (1949) demonstrated pairs of bundles
present in the cotyledonary node of Degeneria (1:
_ I t
I/./.
I (pan- of median
b mdle- and s: r file ;l-:. i I tho-e |a\a ha\c multilacunar mature nodes. ()h-er\ alion- b\ Mai-d.ai
and Bailey (1955) on Clerodendrum, and by Bailey
and Swamy (1949) and Dickison and Endress
(1983) on Austrobaileya described double leaf traces where the components arose from independent
. Other observations by Canright (1955)
and by Ozenda (1949) on Liriod-
rmiiori. I nino.AuA \nnnn i lesei i bei I I liree-lrace or

multitrace nodes when- the i >:n, > (/.'^<"./",/'./1 <;;v,-<;,/ v, -<ii
i
tm .! hi iiio
i< nod( has i tin di in tia< c
that pmduees two small lateral traces which then
degenerate: L-M-L => L-mMm-L =* 'LL-M-L'L. In
in there are no aborted later;
traces, but, otl <
are closer than those in most other genera to the
pattern found here. If one considers multiple independent nodal traces to represent the least special /i d i ondiii.
ri'iiis, as do Ozenda (1947), Sugiyama (1979), Neubauer (1981),
and I, then the Winteraceae are not close to the
angiosperm basal lines in this character. Finally, as
noted above, because ol the lilleteul assui'iplioMs
brought to past studies in nodal analoinv. carl\
trends of -pe. .,1
n .u :l
,\ leraceat will rethe iauiib generates descriptions based on one cur-
closest to Takhtajania. Such a pattern fits close to

the base of Bailey and Nast's ( I') !.">) proposed
Stem transsectional histology is quite simple.

The uniform ground tissue of the cortex and pith is
unexceptional. The earlv development of interfascicular cambium quickly produces an iinml. n | I
ed cylinder ol'cambial derivatives. This was termed
the pseudosiphonostele by Bailey and Nast (1948),
On
the pith side of t
ev bniler. the |
nferentially dis
dary xylem accui
culence through the 1 cm diameter stage, the largest material available in this study. (See Carlquist.
this volume, lor details regarding secondary vasculature development.)
One unusual histochemical feature involves tissue lignification. In the presence' of metaehmiiiati.
chlonde niountant (see Hen. I')"2: Keating. !)<)(,).
Superimposed on the basic three-trace architecture, several genera of Winteraceae develop quite
complex petiole vasculatures. Bailey and Nast
(I'M i| Mi p.s. d '-.: Ildcp. II I. III. p! ii.-~.iiil. In I )of specialization in the Drimys node: (1) three
strands leading to numerous derivative bundle--,
and {'!'< three strands fusing to form a single vascular arc in the petiole. The three traces found in
/>'< //; "';.'.(. /;,,:'//'/. / 'i *w- I:::I,H'. and AM >L >,;</,';;
divide to form three abaxial bundles and "mmierous smaller bundles ineyiJaih a-innged in an ad
axial position" (Metcalfe, 1987: 6). This seems to
be a development parallel with Bailey and Nast's
(1945) first Drimys pattern. Likewise. Mil. all.
(1987: 6) described the bundles as being "amphicribral, hippocrepiform or appearing as divided
hi.n.II. -. with th n \\le>n iinii- lai ing one another."
Carlquist (1982: 281) characterized such a pattern
in / ,- sf,;,,',i ^l,f;int,,n- MnJI
lc>h p. 11. > . ami n nit bs as iiav f\v "pe. uliai cuch - oi b indies"
as well as nests oi scle-vub ,M || , mesopie, II. bo:b
characters not found in I'nihtninnm.
Dehay and Ghestem (1969) illustrate distal petiole vasculature lor three genera of W uin-raccie
F.M,sj,ciiiiiini, with its cinulat or semicircular traces in an irregul. i pa-ten
,
', ,
, ,
, \-.
narked differentiation o
lln i '
|
| . I- I,, be poorlv
I aide.I. -ptr \\\\v . von. tin Inn is t,| \\ |em. fiber walls, and cuticles. I >mg several .letecllon systems (cresyl violet acetate, Toluidine blue. S luff's
reaction, iodine-pnia.-.iuiii nubile. . i ; I .
i
ol) few purely eellulosio-hemicellulosic walls were
found. There seems to be at least a modest amount
o: I i in itioi on all i ells except sieve elements.
ck of c
udied .
menl. : on and ..!- e..l;u -le-mainl plugs, lack of
selereid development and sparing formation of e\I. - I i libers, absence of other histological - i
ciali/alious. as >,. :! I ,i- |s ._., ,= , |,|lh isolation sop
gest that the plant should be interpreted as
' mil not partic ularlv i lose to other
198J proposed n lationships In t< mis ,.| t, hitive
specialization, it would appear that Dunns (which
shews .|nj|e ii . ,bl< '-'s leluri I ami In <>,!<!;;>,i am
likely closest neighbors to Tahliliijaiiia.
\hij,n In.1.ii KIM In. in.i|i i In-' i_a - '.Mih Mun

Hales and Nymphaeales being the most derived.
Further. ilhn tin M:iutic-li.i i-s. 'l;.-\ mi.mi I I'.
laceae and Winteraceae appearing closeh related
Conclusions by Wilson (1965) and Benzing (1967)
supported ici o^nilioti >>\ similar lies |>< -luern ihes<
families l>ased on comparative anatomy. However,
characters in the Cancllaceae are varic
(lisi!ii."!i\<-l\ diffi rmil iloral morpholep at I nal
orny, particularly fusions in the androecium (Wilson, 1966). Vascular structure differences include
the presence of vessels, considered more specialized than the vesselless condition. On the other
hand, sieve elem
oblique to vertically oriented end walls with multiple sieve areas (Wilson, 1965) and are much less
special zed '! an l!io-e <;u,:
and other Winteraceae (Zahur 1959).
Some characters are compatible hut iiiconchi
sive. Sieve element size ranges are about tin same
in both families (Wilson, 1965). Observations on
sieve-element plastids (Behnke, 1988) record the
I
...
_ variable with overlapping Ppmtcin Ivpes. Wilson (1905! encountered the same
ddli. nlties in attempting to trace the obscure origins of nodal architecture in the young stem of Ca" .'! - i I i'
ha l< \ and Nasi
(1945) emphasized the relative isolation of Winteraceae when they noted that, while variatii n i
the family is wide, there is no overlap with other
ranaliai far nl -u -n_ il d I i this context, Canellaceae could be most closeh i< ! s <
Bongers, J. M. 1973. Epidermal leal

Winteraceae. Blumea21: 381-411.
Canright. J. E. 1955. The comparativ > morphology i
relationships of the Magnoliaeeae. 4. Wood and nod
anatomy. J. Arnold Arbor. 36: 119-140.
Capnron. It. I(>03. Contribution- a IV-lude de la llore i
Madagascar. XII. Presence a Madagascar d'nn noine;
represenlanl iliubbiu perricri ]{. Capnron) de la famil
des Winteracees. Adansonia n.s. 3: 373-378.
Carlquisl. S. 1982. Exospermum stipilaltiin (Winter,
Aliso 10:277-289.
. 1983. Wood anatomy of Bubbia (W inleraceae)
with comments on the origin of vessels in dicotyledons.
Amer. J. Bot. 70: 578-590.
Delias. C. & A. Chestem. 1009. Cararteres de lappareil
s,. l\J. France 116: 165-169.
Dickison. W. C. & P. K. Kndress. I''!!.'. Ontogeny ,,l llie
I ,|.e,,.'p I')!!,-; ll,< carls Moral dewlopment oiAuslrohaileuK Hot. Jahrh. 103:481-497.
Krhar. C. & P. I.cins. I 983. /ur Sequel,/ von Bliilennrganen hei einiger Magnoliiden. Bot. Jahrb. Syst. 103:
Ksan. K. 1065. Vascular Differentiation in Plants. Holt.
n Valley Formation (Early Tertian)

i Dakota. Geol. Soc. Amer. Mem. 150.
, B. A. 1974. The stem-node-leaf co
licotyledoneae. J. Arnold Arbor. 55: 12
E. C. 1898. The morpholmiv nl the
in the angiosperms. Trans. Roy. Can.
morphology
Taxon 21: 447-469.

eek. C. B.. B. Schmid
morphology and the
i Press, Oxford.
auer. H. F. 1981. Ober Knotenbau und Blattgrundkularisation bei Dikotylen. Beitr. Biol. Pflanzen 56:
.221: 1521
1523.
piques. Publ. Lab. <l.- IT.eoIr Nun,,. Sii|... Ser. Kiol.

I as,. II. Mass,.,.. Paris.
,)iu. Y-l... M. W. Chase. I). H. Pes K C. K. Parks. 199.'?.
Molecular phylogenetics of llie Magnoliidae: Cladistie
analvses of nucleotide sequences of the plaslid gene
rbcL. Ann. Missouri Bot. Card. 80: 587-606.
iao. T. A. & S. Das. 1979. Peal' sclerodsOccurrence
and distribution in the angiospenns Pot Not. 132:
31<J 324.
iamrwnn F R 1 9HS A new sneeies of /v^/rv/nm, (Win-
plmlogv ,,[ ihr 11.,,,,,,,;,,,-,,.. J. \r|,| \rbor. 30: 1038.

Takhlajan. A. I.. 1964. Foundations of lh,- Pu.lutimiary
Morphology of Angiosperms. \kad. Nauka SSSH. Moscow and Leningrad |in Russian].
W- Flowering Plants. Origin and Dispersal.
s
"
I
I I
Washington, D.C.
~- >^' Evolutionary Trends in Flowering Plants.
Columbia Lnrx. Press. New York.
IW7' Diversits and < Tallica! ion of Flowei irig
,,|
'* ( "'","1"'1 l
u,")' m,....,-.'' "T5 3<>I>
,W Vw V< k
"
>cha.Z, C. E. 2000. The rediscovery of a Malagasy en-
T,
;W """''"' V"" ^
""" ,"" '""/',, ,
,
, ,
,
Mno... P. \\. 1914 Investigations on the phvlogenv o
ll,e angiospenns. I lhe analoim | lhe node as an aid
in the classification of angiospenns. \iner. J. Hot. I:
\o,k \\ P.::::
r .57:
im , \\ ,,.,,.
691-698.
^^ .,, K |(>()- T,|r
,,o]
m^
of lhe
Canellaeeae. II. \n.
v ol die u.ung stem and node.
^n))T j |}(), ^. 3f><>_378
33"322.
imith, A.C. 194.,. (
|.l >
nhn ollheWmteraceae. J. Arnold Arbor. 26: 48-59.
>ugiyama, M. 1979. \ rompaialm- sh.ib ol lhe nodal
anatomy in the Magnohales based on the vascular svstern in the node-leaf continuum. J. Far. Sci. Univ. Tokvo
III. Hotany 12: 199-179.
.' 1966.' The comparative morphology of the Canellaeeae. IV. Floral ...... ph. .,,,,.v , , , .. !..- ,,.
Amen j. Bot. 53: 336-343.
Z:i|,i.r. U.S. IT,'). < ompaial iv e sludv of secondary phlo,., | }23 species ol woods dicotyledons belonging to
f!5 fa.,., lies. Cornell I m, \gric. Fxp. Sla. Mem. 358:
1-160.
^m^^
"
'
FLORAL STRUCTURE OF
TAKHTAJANIA AND ITS
SYSTEMATIC POSITION IN
WINTERACEAE1
Peter K. Endress,* Anton Igershe

F. B. Sampson,* and George E. Schc
ABSTRACT
Floral structure of Takhtajania perrieri, the sole species of Winteraceae in Africa/Madagas. ar. was studied and
nerous in the inner perianth region
. The outer t rpal pair is congemlalK muled, an.
in l.u.l. At ll
are postgemtallv unite*
nt in. accompanied by starch consumption. 1 he dimerous
the i-luli shaped stamel
nature of the unilocular gvnoecium is coufirnie<l. The normal
usual paraoarpoiis gvnoecium with parietal placental ion.
u-r. die total evidence of floral featu
The ovules are larger t han those in other Winter
il lit- lic-t in the l\nt<li>icinlrr<i/Z\{:n<:\iuiiii cladc. uInch
in the Winteraceae. With
is sister to the Tasmaruiia/Drimvs cladc.
mteraceae.
Keywords: ami roe. lum, floral anal
floral morphology,
outer perianth region a
g>M<,<
' ' "' ' ' l,U"J' lG-
i i
I'!.i mova & J.-F.
Leroy is the sole surviving species of Winteraceae
in the Yladagascan/African region. It achieved notoriety because t.| i
. , .
o
,
I
loeular g\noecium, which is unique for Winteraceae, a feature that was noticed only 70 years after
the discovery of the plant in Madagascar (Leroy,
1977, 1978). For almost 90 years the plant was
known only from the type colic
I ' l'>i
. h
contained onk M,I
rai I
I il. and it was
thus thought to be possibly extinct. The rediscovery
(re-collected in 1994 and determined in 1997;
Schatz et al., 1998) offers the possibility for detailed studies ol the disputed lima structure and a
comparison with tli'
. >
Winteraceae.
Since the unusual gynoecium structure of Takhtajania has puzzled botanists, it seems appropriate
to give a short introductory survey of the previous
interpretation- In I
it ion of T. perricri, the g\no< < inn
it.
(Capuron, 1963). Because of the small floral involucre and the api< . I
i
e-
cae, Capuron (1963) associated the plant with Bubbia and placed it into that genus as Bubbia perrieri,
Baranova (1972) later found that the leaf epidermis
i
W mteraceae. It was
her suggestion that it could lie a separate genus
that prompted Leroy (1977, 1978) to restudy the
flowers (see also Leroy, 1993). To his surprise, lit
found the gynoecium to be bicarpellate, syncarpous
hut unilocular. This was at first questioned by
Tucker and Sampson (1979), because its external
shape scarcely differs from single carpels of some
other Winteraceae. However, Vink (1978) confirmed its bicarpellate nature, but interpreted the
two longitudinal furrows of the gynoecium as being
dorsal in each carpel (because they alternate with
the placentae) and not lateral, as Leroy (1977) contended. This was later also accepted by Leroy
(1980) and Deroin and Leroy (1993).
Study of the scarce floral material of the type
specimen concentrated on the puzzling g\ norciimi.
whereas the other floral organs received less attention. The aim of the present study is thus to provide
1
We are in.lelittd to
II
< i
M IIII I I
I
. II
i i
Id a-t ar I'oi material
of other Winteraceae we thank \. \1. Ju.icosa. I'. Leins. and T. K Stuessx. I'.K.I also lli.ink- H. I'. VI. Hyland for his
support during lieldwork v.illi W
i
it Norlli.-m Once .island, and I' Moral <. \1< I'licrson, and the late H.
Mackee in New Caledonia. We arc indebted to (,. K. Kickards lor kindK providing oonfoeal microscope photographof a . It an d g\ not < mi
I
i ul I I u I
ii| |
I vi n-t loi inn int. nit
sections, and 0. Yind .
i
-.iil I.
It
n il -i- KB.S. thanks the School of Biological Sciences. WW.
for financial assistant-.. This studs i- pari of a project of P.K.K. supportc.l b\ the Swiss National Foundation (Nr. 3100040327.94).
' Institute of Systematic Hotanv. I nixersitx ..I /unci,, /oil ikcr-ira-c 107. 8008 Zurich. Switzerland.
'School ol Uiologual s, ionic \ ,t I. ma I niv.isn
,i ' b... ,u I
I lington, New Zealand.
'Missouri Botanical Garden. P.O. Box 290. St. Louis. Missouri 63166-0299. U.S.A.
87: 347-365. 2000.
i ,1. tailed i!es< in.ii.a. nl llic I]

and anatomy c
that of other Winteraceae, especially the putatn
I
- nin and Driinvs.
Flowers fixed in FAA \
-I icif : nil' - I!I;HI n and aslrabl ie. Sonic of the

flowers were embedded in Kulzers Technovit 7100
(2-hydroxyethyl iuelhaer\ late), sectioned at 6 |xm
or less, and stained wild ruthenium red and toluidinc hliic (for details of procedure, sec Igersheim
& Endress, 1997). For scanning electron micro-.;>< [Sl\\l| studi.-s. inc .specimens were dehydrated in cthanol and acetone and sul t u i i
Willi gold. Tin ennfocal tun n >->, ope pho!o<,rapfis

were taken by G. K. Rickards, School of Biological
Sciences, Victoria Irimrsih ol Wellington, from a
jsnoe. urn (..' a tfm. l.n.l uriiii. diateb before anthesis) cleared in 5% KOH at 40 for approximately
3 days and stained with ethydium bromide (1 microgram per ml).
Phylogenetic analysis was performed with
PA UP* vers. 3.1.1, using the heuristic search option, algorithm TBR (tree bisectio
branch swapping), and MULPARS (
equall) parsimonious trees) in effect. Consensus
trees of shortest trees were gained by iv,, . ii .<
with a rescaled consistency index (CI) of original
The flowers of Takhtajania are ca. 1.5-2 cm

aeioss and lia. e -.pi. acii'.i : d perianth parts at an
thesis (Schatz et al., 1998) (Fig. 1). From the behavior of the stamens (see below) they are pmhabK
protogynous.
Floral Structure
stoatl ol one organ in each ;iJt< ' dating poihnn. mil

thus there are double positions instead of single
i organ positions
in flowers, see Endress, 1987, 1996). Then there is
i In
s b\ an additional oiiU. ;M.I
In urn n ..- whorl of stamens
may be incomplete on one side because of the
asymmetric shape of the floral apex.
These switches in merosity do not always take
place at the same site. All eight flowers studied
begin ill' i in J ! i i - I i ting whorls of te[>,)!-. followed by a 4-merous whorl of tepals (b\
louhle positions on the broader sides). In most
flowers, the next whorl of tepals is 5-merous. Then
two 5-merous whorls of stamens lollow. The third
of the flower (because the floral apex is slightly

died the transition to 5-mery was
ond whorl of the androecium. One
and one had three 4-merous whorls
epals, and in both of them the first whorl of
Floral phyllotaxis in Winteraceae is mmmonU

irregular. Fliere haw been liilli veal iitteiupts to <|ei'i\e
I
i
.1
up- from a spiral
or whotli (I pattern (sec discussion ! In /J./'/'/a/. ',,
OIIK scarce herbarium material \\>\< previously been
studied, and it - a >( surprising laal in each ol the
of flora :
ilcipivl
:(1)
outer SIN pen; nth parts decussate, stamens in lluee
4-merous whorls, one carpel (Capuron. I%3>: 2)
outer six perianth parts decussate, inner organs spiral, two carpels (Baranova & Leroy, in Lorn. I<>7i!i:
(.',) p< nanlii pails In lour H m< |.u- whorls, stamens
) carpels (\ink.
eight floral
deli i Ill i e
ateii Organ posihoi: is soMicwhai mi

stable. However, there is a more or less whorled
pattern with changing merosity from the outside to
the ceuler al the ll.mi I l'he ia.|i rnios| Ii ,ral org iiiare in tiimerons allcrnaiing wheals. Then ihere is a
switch to f-memos aid mating ulna Is Tao o-Mill is
that after a 2-merous whorl
ppeai
n
Thus the number of floral organs in the eight

floral buds studied was: tepals (14-)15(-18), stamens \2 16. carpels 2. The previous counts b\ (",apuron (1963), Baranova and Leroy (in Leroy, 1978),
and Vink (1978) are all in this range, except that
Vink found only 12 perianth parts.
nonly have 2 (rarely 3) outer

perianth organs that are more or less eongenitally
united and form a tight cover over the floral bud.
which is often called the imolucro or ealyptra (e.g.,
Vink, 1988). The other perianth organs are free or
more rank some outer ones are (always postgenitally?) united. Terminology of the periaiwa
erature. The involucre or ealyptra was variously interpreted to be made up of bracts or sepals. The
other perianth organs were variously calh d it-pa
sepals, or petals (e.g., Nast, 1944; Capuron, 1963;
Leroy in Leroy, 1978; Vink, 1978;
Gottsberger et al., 1980). There is no clear distinction between sepals and petals either in Winteraceae or in other basal angiosperms. Therefore, we
including those of th
(Hiepko, 1965; Endress, 1996).
In 'UiLltiiijanm, the outer two tepals
eongenla >, lai |. .1 a: a i MI an u \. In. ;<. ^ i
they foiro a more or less horizontal platform, which

is somewhat elongai. <l n iiie plane <>l ils two tepals.
The next inner four tepals (two pairs) form the topograplucal peripheiy of old floral buds. The miter
two slightK overlap the inner two. In the overlapping region they are postgenitally united for about
half of their length b\ int.-rd.ailahon of the cuticle
(Figs. 2, 4A, B). As the flower opens this bond ruptures, and these four tepals are the first to spread.
On their outer surface these four tepals are smooth
and have a thick cuticle; on their inner surface they
:
an papillate Millie I
m->
surfaces. This papillate epidermis is tanniferous. as
are the one or two cell layers below the epidermis.
The margins of these tepals are not tanniferous; the
cells are less vacuolate and have relatively large
nuclei (Fig. 4C). From their appearance they seem
to be secretory, and in microtome sections bluestaining secreted material is often concentrated
around the tepal margins. This secretion was also
observed in the field in June 1998 by G. Sehatz.
In the colored photographs of an open flower in
Schatz et al. (1998) and in Sehatz (2000 this issue).
the red petals have white margins that correspond
to this secretory zone. The material imesiigaled
contained insect (limps?) lanae in the flower Imds.
i the tepals
especially
: three vascular
r tepals have
ilar strand
.
VNDKOKCIliM
At anthesis the stamens have apical extrorse anthers on club-sbap
lilameni i >n idest short l\
below the anther). Thus the thecae are basally
spreading and almost horizontal. At the transition
from the female to llm male phase of anthesis. the
lilaments < longali in I
i i<
llm kt n in tin
upper part, while the anthers shrink as lhe\ open
(Fig. 5). As a result, the proportions of the stamens
change considerably during anthesis. The filaments
are more or less circular or slightly broader than
thick in transverse section. The epidermis is slightl\ papillate ami mm. oi less lariuiferoiis Taninlerous tissue also occurs in scattered patches below
the epidermis but is largely lacking in the center
of the filament. Phis tanniferous region extends up
to the ventral surface of the anther connective. Oil
cells are present. Cells with oxalate crystals are
vascular bundle. The tissue around the vascular

bundle eonlains .11 >Mr 1.i.1111 slareh before the filainent expands. Alter expansion the starch has disappeared (Fig. 6). Expansion of the filament goes
hand in hand with cell enlargement,
<;YN<)KCII
The g\ noeeium is disy mmelrie and club-shaped

(Fig. 71), K). It consists of two congenital!) united
carpels (Leroy, 1977; Vink, 1978). In young floral
wo carpels can clearly be distinguished (Fig. 8A, B). At anthesis each carpel has
a longitudinal furrow on its dorsal side (Fig. 7A,
D). There are stomata on the outer surface (Fig. 7F).
The gynoecium has a single locule. In the terminology of Leinfellner (1950) the entire ovary is symplicate: there is no synascidiate part at the base,
The inner surface of the gynoecium is secluded
from the outside |,v a completely postgenitally
fused slit, which at the surface extends as a line
between the two carpels (Figs. 3A, 9B). In the middie this line is crossed by a more or less distinct
transverse furrow (Fig. 7B). The entire slit is surrounded b> die stigma, which forms a large convex
cap atop the gynoecium. The stigmatic zone is more
dian plane of the carpels (Fiji. 71). IT The broadest
part of the gynoecium. the ovary, is slightly above
mid-length. Abo\e the ovary (here is a massive pari
with the common pollen lube transmitting tract
(Figs. 3A-D, 9A-E). Below the ovary is a relatively
long solid base, the common siipe of the two carpels
(Fig. 3I-K). Although the ovary is unilocular, the
placentae of the two carpels are obliquely directed:
the meet in the center )f the locule Fi
Y
<
( g- 7G>- ThT
form an arch, which is deepest in the middle (Fig.
9A).
Kaeh carpel i
I
i
i ular bundle, which
extends up to some distance above the locule,
where it may branch (Figs. 3A, 7G). The branches
end about halfuav between the lewd of the placenla< and tin stigma I a< h < arpel also has two or
more Literal bundles, which are sometimes separate
from the floral base (Figs. 3D-K, 7G). They flank
the placentae and serve the ovules. They are conneclcd with tin- dorsal bundles outside of the plaeentae and may also show connections between
each other (I' .
'><
I'h.
is.d bundles com
monly have two xylem portions that are directed
toward each other and two phloem portions directed
away from each other, which gives the appearance
of two bundles (Fig. 3D-K). However, they probably originate from a single bundle. The same dou-
Floral Structure
figure :$.
Takhtajanm pcrrieri. Gynoecii
inner surfaces not fused. C. Zone abo\e o\ar\. lateral carpel \. i - < 1 J 1. i r bundles merge with dorsal bundles. I).
Upper placental zone. K. Lower placental /one. - I <)var> with all ovules.
(,. II. (Ivan base. I-K. Solid base
of gynoecium with rearrangement of \a-<ular bundles. Scale bar = 0.5 mm.
hie appearance ;ils<> occurs in sirong lateral bundles. Tims the ovules are served primarily b) the
Literal bundles, and not l>\ the dorsal l.undlcs (in
contrast to the interpretation by Deroin & Leroy,
1993; see discussion) (Fig. 7G).
III. >tiVmalie surface is iinirellular-papillate and
secretory (Fig. 7C). Also lire p l< n :uh< I: u-mii
; the i
thai !
down to the placentae na- age iniccllidai j ,ij.1.
lae (Fig. 9E). Tin
,< arc tanniferous
and the sevi ral c. Ill
.
ot Ih
i I I
m
still more so (Fig. 9A, B). Below the region of the
pollen lube transinilling tissue, the inner surface of
t two layers ol tannifells. II,n
rous cell groups. The gynoecium
s ethereal oil cells. Cells with oxj present. The inner layers of the
tin abundant starch. Stomata are
e surface of the gynoecium, espeT part. Stone cells were not found
31 flowers studied we found (5-)6-7(-8)
s per gynoecium (1 with 5, 9 with 6, 16 with
with 8 ovules). Capuron (1963) and Leroy
i) mentioned 5-11 ovules for the type mate-
rial; however, ni the figures by Vink (1978) ant

Dcroiu and I .. to\ ( I1'1-'.!) lucre are oiiU loin o\ ill.ill a gwioeeium. The ovule- are pen<leiil and an
arranged in two lines. They are bitegmic, craiucellar, and anatropous (Fig. 10). They are ca.
p.m long. Ovule width/length ratio is 0.6. The
cellus is ca. 280 p,m broad. The micropyl
formed by the inner integument (Fig. 10). The o
integument is semiannular, and the inner is arm
(Fig. 10A, B). However, of the 31 gynoecia udied
we found two in which one of the six ovu
<).)!)
ones and had a long funicle. In trans'

the ovules are wedge-shaped because t
on both sides of the double placei
wedged together (Figs. 3F, 9F). The <
ment is 45 cell layers thick, and th
II laser- thick. Tanniferous tissue o<
in the periphery of the ovule (
raphe, especially around the vascular bundle).
DlsCl SSION
NLMBKR AND PHY1.I.OTAXIS OK FLORAL ORGANS
Lability of floral organ number and phyllotaxis,
and the tendency toward some irregul
0k
w
0
d the anthers are open an<
emale phase. B. Male p
XL
. C, D. From above.
usuimiclry. is .
taxisseemstobepredomni.il
I
in Winteraceae (Vink, 1970, 1977, 1978, 1985,
1993b; Endress, 1986, 1987). From the record in
iii. I I.
in-. Ih
. ins to be an interesting exception with more or less regular spiral
floral phyllotaxis (Hiepko, 1966; Erbar & Leins,
1983). However, Ronse Decraene and Smets (1998)
mentioned chaotic floral phyllotaxis also lo: l)rn>i\.\
winteri. Doust (1997) shed light on this seeming
contradiction by his observation that terminal flowers in Drimys winteri have a more or less spiral
pattern, while lateral flowers have more chaotic patterns due to initial asymmetries of the floral apex
(see also Vink, 1970); Doust (1997) also found that
\. !>,- i I -l.i Miih-
i'l - !|-:<-J. ilai n\. tli.a.
I'll.;-, :l,e,
decu
melons alleiiialitm whorls and sonieliines. In additional double positions, to whorls with a higher
n nl
i in - I Ins w is .
i e to hi- ( omiiion
for Pseudou intern (less con
(Vink, 1970), and for Zygogynum (Vink, 1977,
1983, 1988). As shown here, it is also present in
luL'tiajanni.
i inflated by cell e
IS. Male |h;w. C. I) Crnlral part of A and I
Hi' around \a-eiilai liunillc: dark dot-l.
I>
shorter than in Drii

'
are protective organs for the buds. In Drimys and
TiLsmanma the involucre encloses tin olhei floral
parts until the flower opens, while in Zygogynum
and Psnidouintera it ruptures very early and the
'
pidrnnis was tanniferous and not papillate in those genera. Tepals
an vvl
i I)
< \ < nisi of larg<
intercellular spares in the mesoplnll. which form an
optical tapetum that reflects incoming light. Tal.h
1988). The next inner whorl of tepals is postgenitally

united in Tiikhtdjanid. Such union is also reported
for some Zvgog\m
-|
i
I ,i i i
I
W'II
teraceae (Vink, 1985, 1988; although without indication whether it is postgenital or congenital). We
did not find tepals with secretory margins in Drimys
red tepals, as do some species of Zygogynum, but

those have much thicker tepals (see Thien, 1980;
'nil \'Y-K\ ) h d ilion
I'tlhtujariia, some other
Winteraceae contain starch in the tepals, which, at
least in som< .
'
'
ties, thrips) (Pellmyr et al., 1990; Thien et al., 1990).
Volume 87, Number 3
Club-shaped f
/.i.-.i:',;.>',;; li Drums and even more so In 7!/.vmanniti the filaments are tliititi.i and the lliecae
are less terminal and more lateral (Bailey & Nast,
1943a; Sampson, 1987; Endress & Hufford, 1989;
Endress, 1994).
The behavior of the stamens of Takhtajania durii,:. antli. si- \ ilh . lentil ion :n:<l -pe< >;/><!,! u\ Saaip-o:i | ['>;'(>: and Llo\d and
Well- I \<><^'. and lot /it-"-' \;:<u:: <"./. ',- < , \ n L /..
>. and Z. pancheri by Carlqui
(1981
1982, 1983). Carlquist (1982) also noted the deII. discuss. (I lilam. nl . vj.atis on ill the context of
flower opening l>\ pressure ol ill. slauiei.s How
ever, we found tin
i
i i ld:in,.-:il
i- n
onh ll el llowel opening, ill ill. Iial -Itioll In n llle
female to the male phase ami interpret it as associated with pollen presentation (see also Sampson.
1980, for Pseudowintera). boss of starch ma\ be
con. lal. d Willi rapid . < 'I giowih in this phase, as
also unhealed i>\ <.ail<|iiisi (l'),"^) |.,r '/.\>>:\ \ sum,
stipitatum. It should also be studied whether starch
loss is here associated with scent production, as
this often occurs in osmophores (Vogel 1990). Pellmyr et al. (1990)
scents in Willi.-i i, . . lo- | . In itioti but did not
mention the source of the scents (see also section
on perianth).
Since the thecae in Takhtajania are on top of the
club-shaped filaments, the position of the thecae is
highU obli-jiie ;e almost tn n/oiiiai (also in /'>,;.'. i/ ; -.. ind Z\i!,<>ii*'
Id. tefore, in trans-
obliqueU. \s a consequence, the eildoil.e- u;m.

which is one-layered, may appear to be two- or
more-layered (see Swamy, 1952, for /i-,";.<>.;.
baillonii), while in reality it is only one-layered.
The gynoecium of Takhtajania is peculiar. Although it is biearpellate and unilocular, it is not

paracarpous in the normal sense with parietal planhhquc ic almosi horizontal. I'h. rehire. the placentae of both carpels are separate and are onl\ con
ligi.o i - at ilr. n " iph I..- a I a-c- rims. pla. en
tation is not laminar (as opposed to Leroy, 1993)
but has a normal linear configuration. The stigma
is topographically apical, but morphologically it
fused) entrance
into 'h. nlei a I sp; c ol il < two . aip. Is I'he slig
ma is not commissural either (as opposed lo l.em\.
1980, 1993), because the entire orifice is stigmatic
and not only the lateral parts, although the stigthan in the median region. Thus, it corresponds to
This unique biearpellate unilocular gynoecium of

T,i!,i-iii;,in:u .odd !,..< < \ obed tioin a uniearpellale ancestor. I nicarpellale gvnoeeia are known
from species of Ttismanniti. I'scndou uitrtu. and
Zygogynum (Bubbia) (Sampson, 1963; Vink, 1970,
1983, 1993a; Ueda, 1986). In these species, sometimes two carpels instead of one carpel develop in
a II
1 >an
i .\ K
i. I1 '70). In such gynoeeia. the available space for two carpels i- I in
ited so that they may form a unilocular paracarpous
structure, as San
I
i l 1'iTUi -I
, .
i
,'
,'"i' intern traversii Dandy. Furthermore, in
Volume 87, Number 3

Floral Structure
Zygogynum two (or three?) central stigmas of a gynoecium may be confluent (/. htiillonii. \mk.
1993a). A dorsal furrow in lire carpels as in Takhtajania also occurs in Tasmannia lanceolata (Leinfellner, 1965; Vink, 1970; Leroy, 1980). The position of llu- furious is dorsal because they alternate
with the two placentae in the bicaipellale. -\noaipous g\noei nun of Tukhtnjania. In the free carpels
o rasaut'inHi. ih I'm low li s opposite Kic placonla.
The significance nl ihe furrows is riot clear: dehiscence of the mature fruits has not been reported.
on more than one genus of the VUutcraccac thai

ill the studies l>> Bailey and Nast (1943b, 1945)
and Bailey and Swamy (1951) especially focused
on the vasculature; (2) the studies by Tucker (1959,
1975), Tucker and Gifford (1964, 1966a, b), Sampson (1963), Sampson and Kaplan (1970), and
Sampson and Tucker (1978) concentrated on the
morplii My c-al n< aii iioiineal I. . elopmenl of earpels, vascularization, and placentation; (3) the studies by Leinfellner (1965, 1966a, b, 1969) primarily
dealt Hid il e out. an,! i nei moij holug\ and pla
centation: (4) the slud\ In Igershcim and Kmlrcss
( I'*'.'; I I", .a:-., 'il
In their discussion, Deroin and Leroy (1993)

mi nil .in d ih< ipn d pi H < nl ! <>l /-/; l,',i,>i.'u,i as
peculiar. This differs from the gynoecium in paiapai is n. I lc.\\c\ei. I is i o! pecnlun . ilhn: \\ mlci
.iccae. because the majority of them have "apical"
placentae (because of their more or less horizontal
direction).
How docs the gynoecium of Tuklilajania compare
Willi thai m < tin i An nl- i
i i part from its peculiar syncarpy)? Several .mlI
m III i. I a.ili -
an ! I I-.I >l't:-
ol r a
pels and ouiles in comparison wilh that m other

I .ml- liner (1965, 1966a, b, 1969) and Tucker
and Gifford (1966b) found an unusually high variabi i!\ ol carpel -hap.- it, \\ ml. ia- e .* Iroiii lughh
ascidiate ! largck plicate. \on-ascnliato cup. i:
ildj<tnia are only known from 71
(see also frame. I()')()). However, lliese are not dii.'i lb c.aiparable, because the non-aseidiai. -\ ape
in .
iintim ma) be caused by its s\ncarp\.
Volume 87, Number 3
Guioecilliu va-cubltine oj Takhtajania is not <liiIctenl I mm lhal In oilier W inleraceae. The ovules
are served primarily by lateral bundles (see also
Vink, 1978), and not predominantly by the dorsal
bundles as contended by Deroin and Leroy (1993).
< :.;'|..-!:- in \\ .i-:s 5.< < ar ^M!< iall\ ha\ r -i iio:s: I . i< il.-sv bundle. \\lii ii li.i.-. Miiiici ii i s lici n < h uae
terized as "double," or there are two dorsal bundles, such as in Tasmannia (Tucker & Gifford,
1964); in addition, there are two ventral (lateral)
nundl.-s IISMII ah-d wild the placentae, vvhirh ma\
merge into one bundle in the ascidiate basal part
of the carpel. Dorsal and lateral vascular himal,
may be connected by secoudar\ bundles later in
development. In a critical study Tucker (1975)
snowed lhal o\ul< s an piincipalk >rr\ed b\ lateral
earpellais '.axilla- handle- i:i -pecie- of Dunns
and Tasmannia. In contrast, Bailey and Nast
(1943b) had described the ovules as being vascularized parlb b\ brain tics nl lire dorsal strands, nnl
partly by anastomoses between dorsal and ventral
strands. It seems to be a peculiarity that the ovular
asridar -trands dilTetvriliale relat \el\ late, when
llie dorsal and \onlral \ aseulai bundle- ,!< ia< 1far differentiated. This is probably due to the fact
pels are already relatively massive and the primary
vasculature is rela:r,eh ah aiiced in de\ .-lapm i
As a consequence, the ovular traces eonneet with
secondary vascular bundles between the lateral and
dorsal main strands that have formed later. However, the connection with the lateral
1 I
dies is still there (Tucker, 1975; see also Ucda,
1978). Likewise, in Takhtajania, the ovules are
served by lateral vascular bundles or by connecMII
' i
. i .
lii
I I ii ral ones (and not
by dorsal ones as Deroin & Leroy, 1993, deThe ovules of Takhtajania are much larger at
lldied
ods"). The ovules of Takhtajania are 900 p,m long,
belvvcen '>->! pari in Tasnairaaa insipala and <<2
P-H I'l A_"_; . it"' hill', "I , | Mi- III 1 l> ol<
with the low number of ovules per ovary in Takhtajania and lla difltaeni au'lnie. hire of tin- bicaip. lati a ilo.-n i > 'i
i- i nipared to the ovary
in free carpels. In morphology and histology (esilar to those of olln \\ inleracca- w >
n i
1905; Bhandari, 1963; Sampson, 1963; Bhandari
& Venkataraman, 1968; de Boer & Bouman, 1974;
Prakash et al., 1992; Imaichi et al., 1995; Igersheim & Endress, 1997; Svoma, 1998).
Before recognition of Takhtajania. Tasmannia

and Drimys were considered to be the basal
branches in \\ u
nnia was favored
as the basalmost cladc because of its low chromo
some numbers (Ehrendorfer et al., 1968) and the
conduplicate carpels (Smith, 1969) long viewed as
a model for an archaic carpel form (Bailey & Swamy, 1951). Drimys was considered as the closest
neighbor of Tasmannia because of many morpho!U-,II ,n similar iiies In incl. lor MHHC lime lasman
nia was subsumed under Drimys. However, chromosome studies by Ehrendorfer et al. (1968)
piomptcd Smith (1969) to reinstate Tasmannia. The
ITS studies by Suh et al. (1993) supported the split
between the two genera. They also supported Tasmannia as sistei i
-fih
II i
Dunns in the basal position, followed by Pseudowmlrra and Zygogynum (the latter including /.'///;
i I
' iu:,
i- | toposed b\ \ ink
(1985) on morphological grounds; see also Vink.
1 <)<).,!,). Kubitzki and Reznik (1967) found a persisteut difference in leaf flavonoids between Drinns
and Tasmannia. The isolate,
nia, as well as the unity of the group Huhhm /,'
liolum, Exosperm
urn. was emphasized by Williams and Harvey (1982) based on the
leal fla\otioid patterns. However, they interpreted
s the n
5 in the famil\. On I lie basis of leaf epidermis
i (1972)
considered tin i; i>, I dlcliolotm lo be l>< I ween iht
mys/Tasmannia and Bubbia
lalln
I emphasized the isolated position of Bubbia perrieri.
After Takhtajania was recognized as a separate
genus, Vink (1988) explicitly proposed a basal position in the laniiK loi it. lo|
If
r.fin
Drimys clade. A basal positn i
had
also been implied by Leroy (1978) by the erection
of a subfamily Takhtajanioideae and later even a
separate family Takhtajaniaceae (Leroy, 1980).
laniiK status was later not accepted by other authors and was also rejected by Leroy (1993). Even
before Takhtajania was erected as a genus and was
still mi luded in Bubbia a- B. pcrrii-ri. bonpa(1973) found that alveolar material was present on
I he leaf surface of Winteraceae except foi las/nan
nia and Bubbia perrieri. In contrast, in view of its
very large pollen tetrads and its particuia pollen
structure (Lobreau-Callen, 1977), which may indicate polyploidy, Bubbia perrieri was considered lo
be related to Be
correlation ol > limn
Degeneria vitiensis
Zygogynum pancheri
Zygogynum baillonii
Zygogynum stipitatum
Zygogynum tieghemii
-
Takhtajania perrieri
'
Pseudowintera colorata
'
Pseudowintera axillaris
Drimys winteri
Drimys confertifolia
Drimys granadensis
'
Tasmannia piperita
Tasmannia membranea
Tasmannia insipida
'
Tasmannia lanceolata
igure 11. CLHIUJII i

H
.
lit (I. wilh Dfgnicrui a> outgimip. based on 13
resrntative floral feature-,. -Iimwiif /.// hhiimun m -<. .1 in i .
>nn < ladt (I'M \' \ I I. IMMIM-IK
rch, TBR: consensus i,,v i :\ slmiirsi trees unl, CI <).7(.r>. HI <).i!O.J. uain.-d U nu.^lmn- uiih rescaled CI of 25
>.1est trees til length 2<) with CI 0.621 and R[ 0.788).
Floral Structure
Canella alba
Pseudowintera colorata
Zygogynum tieghemii
Zygogynum pancheri
HZ
Zygogynum baillonii
Drimys granadensis
Drimys winteri
Tasmannia membranea
Tasmannia piperita
HZ
Tasmannia insipida
Tasmannia lanceolata
resenlati\e floral features, shewing Takhtajania nested in the I'saidoiantrra/ZvgogYnum chide (I'ALT .''
search. TBR: consensus tree of 20 shortest trees with CI 0.713. M 0.868. gained by reweighting with
70 shortest trees of length 30 with CI 0.600 and Rl 0.769).
some number and pollen size in Winteraeeae,

Hotchkiss, 1955). Praglowski (1979) emphasi
the special similarity of its pollen tetrads with th
of Drimyx.
From the results of the present com
study of flowers of Tahhtajania and other Winteraceae some new features come ml.' the discussion.
The particular club-shaped stamens and almost
I HI
ii I i
11 i i I In i lii i ,i. are shared i
Arnold Arbor. 24:^0-346.

1943 b.
the Winteraeeae. II. Carpels.
472-481.
&
. 1945. The eomparaliv
shared with Pseudowintera and Zygogynum species. The fusion of the tepals following the involu-
tlll^T?"^'^ ^^ "
Arnold Arbor. 26: 37-17.
B.C. L. Swairiy. 1951. The eonduplicat
pv\ ,,f dicotyledons and its initial trends of spec
t'<>n. Amer. J. Hot. 38: 373-379.
1972. Systematic
. in the Magnolia, eae and -onic related famili.
21: 447-469.
Bhandari, \. \. 1963. Embryology ol l\nnl,nnnien, <
lomta.\ vessclless dicotyledon. Phytomorphology 1
ere i- shared with

m<
peci
Red
.
,
,
. ,
r,
tepal color is shared with some Zygogynum species. This and the large pollen grains may indicate
'
' ., . ,
,_,, .
.
_
& H \ k li i
1968. Embryology olt I)
IV, ,,, , Ull(,u x.I>.., I' 5<><)-524.
Boer, R. de & F Bonmati. 1974. Integumentary sludi
Pseudoivintera and Z\gog\mim. The presence ol an

involucre that is short and protective only in young
floral buds is shared with Pseudowintera
ogynum. The presence of whorls of 4 or I
that Takhtajania constitutes a clade with the Pseu.'./. '.','../ /.^.'i.' ;;,::,, v .. ip .nddai i /.,>', ./.- i
Drimvs group is sister to this clade (see ul-n fig.
i"
tl,e , oK ar i, a
J i; ; .')'
n '
\\[ ^rimys "

23: 19-27.
J. M. 1973. Epidermal leaf chara<
2.2 in Vink, 1988). This is also shown by a cladbased on representative Moral

(Fig. 11; Appendixes 2, 3) and with Degeneria as
an outgroup,
sister group of Winteraeeae in preliminary cladistic
anaKses based on gynoecium structures llm-udi a I
(Karol et al., 2000

1 Canellaceae. But ever
with Canellaceai as an < u
* nested in a Pseudoivintera/Zygogynum cladt
in the morphological analysis (Fig. 12; Appendixes
2, 3). If this scenario with Canellaceae
Winteraeeae stands corroborated, the ;
view with Takhtajania basal in Wi
bo better supported. Takhtajania
nellaceae having red flowers with whoii-d p-o I.
taxis and only a sh
pals. They also share a bicarpellate, paracarpous
d:fh ii ii detail.
Canellaceae ha\e vertical parietal placentae and
>: i - >\ ah . . . ii itu. rop\ lc. but
Svst. Evol.
1987. Floral phyllohms ;
Jahrb. Syst. 108:
l,,(" slia|i.'s. si/,-s and evolutionary t
115: 429-
Bot.
./ has obliquely horizontal separate placentae that meet at their morphological base, and
anatropous ovules with micropyle formed by the inner integument; see Igersheim & Kndrcss !ll)'7i
Thus the paracarpous g\ iioeeium is unlikely to be
a synapomorphy for Takhtajania and Canellaceae.
In addition l<> mole, ulai studies, the kar;
Hufford. 1989. The div

Linn. Soc. 100: 4
Frhar. C. & \\ Feins. 1983. /ur Sequ.
ganeii bei einigen Magnoliid.
433-449.
Frame, D. 1996. Carpel <
sipida (Winteraeeae). Int. J. PI. Sci. 157: 698-702.
ColU.erg.-r. ... I. Sillierbauer-< aitlsberger & F. Ehren-
Volume 87, Number 3
l.glo.pcl'..,1 .',>;>, ,'IN/,/,I, I *.\ HI

11-39.
Harden. C. J. |9<>0. \\ n,l,-m,r;,e. I',,. 125-127 //, (.. .
Harden (editor). Flora of New South Wales I. HON;
Botanic (,aniens. Sydney.
Iliepko. P.
|9(>5.
!,
I . . I,, louche IMP
ell
Iwicklungsgeschichtliche Untersuchungcn iiber da

Perianth bei den Polycarpicae. Bot. Jahrb. Svst. 84
559-508
. 1966. Das BlUtendiagramm von Ifrinn* wim,-,
J. R. et G. Forst. (Winleraceae). Willdenowia 4: 22F
1955. Chromosome i
I lot.'ll
I |
.Hei
(edilor). World Pollen and .Spore Mora !!. \lm.|ni>l M

WiU-ll. Sloekholm.
Prakash. Y. A. P. Pirn & F. IP Sampson. 1992. \nther
and ovule development in Tasmamiiu (\\ mi,;,,, , ,,, i
Austral. J. Bot. 40: 877-885.
Ho>e Perraene. P. P. & K. P. Sn.ets. 1998. Notes on the
evolution of androeeial organisation in the M
Sampson, F. B. 1963. The floral morphology ,,l
mlrra, the New Zealand member of the vesse
trraeeae. Phvlomorphology 13: 1(13 J23.
. 1980. Natural hybridism m/'vWo,,,,*
" v Zealand " ~
nl
1 M i- i - <|u< n. . s \nn
\1i*,nuri Hot. Card. 87: 414-132.
viil.il/.ki. K. X IP He/.nik. 1907. Flavonoid-Mii-lei dei
iiber die Familien.'Beitr. Biol. Pfl. 42: 445-170.
cnlellner. \\. 19.50. IW Hauplan des ssncarpen
oernni... iUcn: Hot. /. 97: 403-130.
CMI-
lonnigcn Pla/enta ii
Wintera. Osterr. Bot. /. 113: 84-95.

. 1966b. W ie sind die \\ interaeeen-Karpelle tatsachlich gebaut? IIP Die Karpelle von Hul,!,
siwimum mid Zygogynum. Osterr. Bot. Z. 113: 245-264.
. 1969. Uber die Karpelle versehicdem r Magno
bales. VIII. Cberblick iiber alle Familien der Ordnung.
Osterr. Bot. Z. 117: 107-127.
.erov. J.-F. 1977. A compound ovary with open carpelm
in
lM.:i! u .1
i!
I 'ii M'.
in |.li' i
tions. Science 196: 977-978.

. 1978. Pne sous-famille IIK.IH.U piqix de Win
teraeeae endcmique a Madagascar: Pes TaUii;i|,im..i
1980. Nouvelles remar<|ue> -
mannia (W inte.aceac). Taxon 18: 28f>-290.

Slrasbuigci. I-!. I 90.5. I )Ie Samerianlage VOn Dfimys winter! unci die Fndospermbildung bei Angiospermen. Flora 95: 215-231.
Suh. V.. P. B. Thien. II. K. Heeve & F. A. Zimmer. I'X).',.
Molecular evolution and plnlogenetic implications of
internal transcribed -pace, sequences of ribosomal
I)N\ in Wmteraeeae. \mer. ,|. Hot. 80: 1012-1055.
Svoma. F. 1998. Studies on the embryology and gwioe-ii- \n
ae. PI Svst. Fvol. 209: 205-229.
Swamv. B. (,. P. 1052. Some aspects in the embryologj
of Zygoguium bailloni. Proc. Natl. Inst. Sri. India Ii
18: 399^106.
Thien, P. B. 1980. P. ms ol pollination in the primitive
angiosperms. Biotropica 12: 1-13.
. (. Pel
,iX C
Pr.U-aeeli.itlde
. pollil>7.
es. \dansonia. n.s., 16: 445-460.

I I.
Con
11
II >.
-. S. C. 1959. Ontogcn ol the i

(lower in Drimys winlen var. chilensis. Univ. Call
I. Bot. 30: 257-336.
- 1975. Caipellary vasculature and the ovular vas
r supply in Oram. Amer. J. Bot. 62: 191-197.
-& F. M. Gilford. Jr. 1964. Carpel vasculanzatio
'rimys lanveolata. Phytomorphology 14: 197-203.
,lo ;\ ol W nil. I.I
-e I.II :;n ilomv of the flowering shoot. J.

. 25: 454-466.
(lower of Drimys lamrulala. Amer. J. Bot. 53: 133
11 - j i n HI 11! I j i î i j:
! i i i I (- Mjti 9-i H i ^ !
J
i u* i * ti I=IM
:5 is^31111 i.
Joo
^ o ^
os-gô
0
oo-c^-oô
ôooooo oooôoo^^
ooooooo
ooo^ô
Vm *M\h ?iSl3J|3!|Jlig f 1 1 111 -
- oo
-----
-OOO-^
..-gooo.o^
J:.
__o OÔÔ^C.
-oooô o------
-ooo-~o ooo^ôo
Degeneria vitiensis
Zygogynum pancheri
^ccc^.o
Zygogynum baillonii
,-
ooo.oôoo
^ôooooo
oog^ô,-
Zygogynum tieghemii
o~-ôo~
ooooooo
rasmannia insipida
rasmannia lanceolata
ll|l|l|ljljllI11ijl|lljip|!|l|l|l ij[
--g----o
fasm-mnia piperita
-jti
Tasmannia membranea
'^
Hbi ii?
0 0
-ÎTH.I^!
- = -.:
Drimys winteri
S.tJlI - ;
Drimys .canadensis
-itV.*.Mtt*-
i.lN '-.:" ^ ^<iM 13 2 1 I:
Volume 87, Number 3

2000
Endress et al.
Floral Structure
ment: (0) 0-3, whorled; (1)4 or more, whorled; (2)
0. Pollen diameter (polar axis) (I'raglowski. 1979): (())

18 pm or less; (1) 19 pm or more.
7. Carpel number per flower (\ink. I'M), Simp-on -1
al.. I9:;;:): :>, <.. more: (l) i or 2.
2. Involucre (congenially united outermost tepals) in

advanced floral buds (Vink, 1993b): (0) shorter than
other tepals; 1 1 1 as long n> or longer than other tepals.
1 i in il i'\ union of the tepals following the in-
9. Sclereids in ovary wall: (0) absent; (1) present.

10. Ovule number per carpel: (01 .'!... less: (1) 9 or more.
11. Ovule length at anthesis: (0) 600 pm or less: (1) more
Appendix 3. Characters used for eladistic analysis.
COMPARATIVE FLORAL
ONTOGENY IN
WINTERACEAE1
Andrew N. Do
differences in floral architecture between taxa.
These differences
I Z\ii-t>i!\niii)i anil F.xospcrnuim being considered
Wiuteraceac
have
Ion-
been
considered
to
he
ol I
I
j < J (i i
dies and have
played an important role n
i understanding of
the evolutionary history of angiosperms (Bessey,
1915; Bailey & Nast, 1945; Cronquist, 1988). Their
importance can be traced to the possession of a
suite of morphological character stales thai haw
been presumed to be primitive for flowering plants.
Foremost among these has been a simple flower
construction of mai \ live >:uK an I the occurrence.
at least in some taxa, of eondupb. .
ip.-l- ;llail\ iK Nasi, I'M.'il. {'. luplicate carpels reflect the
theory that angiosperms evolved carpels by the
folding of an ovule-bearing leaf (Bessey, 1915; Bailey & Nast, 1945; Cronquist, 1988). Tubular (ascidiatc) carpels can also be lound in \\ inleiaceae
(Tucker, 1959; Leinfellner, 1965, 1966; Frame-Purguy, 1996).
In recent angio^p
. t
. .
are one of the first branching lineages (Qiu et al.,
WW: \andi et al.. I ')>;',). and the Moral morpliology of the family possesses many characteristics
that may elucidate the features of lloral
Ii-ring mam Useful and insighllul cniiiiiiriih. I thank (.corgi- Schat/. (MO| lor the -lit of I.
iiini. and Hruo- Sampson |\ id.ma I ni\ei-il\ ..I Wellington. \eu /.-aland! lor gifts ,.| h
-
. '
>,,,,,
.<
-Department of Biology, f ame-silx f MI--,UI,I
ml,,
e\nlution
in basal angiosperms .Tin- i.eeui redr-co\or\ of the

only Winteraeeae In.in Madagascar. Tahhtajania
perrieri (Sehatz et al.. 1998), allows examination of
all extant genera in the family,
Other papers in this issue ol the \nn<il.\ discuss
the ph\ logenelii placement ,>f Tulditn/nriiu within
Winteraeeae and detail il- Moral and vegetative
morphology. Its floral morphology is unusual in the
family because of the iiiui|ue s\ neat pollale gynoecitim (Leroy, 1977), and recent collections have allowed the structure ol the i!\noecium to be cornpreheusbeb examined for the first lime (Endless
et al., 2000). As a complement to the detailed analysis of Takhtajania (other papers, this issue), floral
morphology and ontogeny in Zigogynum bailloni,
Bubbia houeana, Pseudou intern axillaris, Pseudowintera col,
'
,in, colula. Tnsman,'/,/ in.I Dtintw innlcn are presented.
Analysis of the mature floral morphology of other
species ol /.,
<n\ h \>>\p,-rmum \s
also presented.
i i
l,ii,ilti
and l\ a.\illa,
St. I,mi^. Si. loin,. \l,s, (,.W2\.
Volume 87, Number 3
Comparative analysis of ontogenetic data can

help in a--. --H .
ill.
i-
-- ibl<
. i. - .1
'I
floral structures. Data from Moral ontogeny may also

shed Ij.at on two persistent systematic questions
within the family. One of these is whether the genei-i Hi,!>!>:, /! ,',',>tii. . I' ,,";;: n,--,, . inl/nvr1
um are best regaided
rat
< n. la 01 a- out
large and variahll _. ,,n- !>... ,.! /, .'>';
were combined by Burtt (1936). Vink (1985) comblr.'d l,u > i u . h In . /.' , ', ,- I /
^ " >,<
. -i.l /.\go- . <>.. into m. pan.!. .I Zygogynum s.L,
with the arguin. r
lers ihat separate
the genera (degn . <>l
ti i <>i petal- and of
carpels) were variable anil overlapping between
them. In tin- paper data have been recorded under
Ihllinu! iii-lu.JiUL !',';''!.!:;; I. E ws/>- < :::,,;>:. aud
Zygogynum s. str. so as to highlight possible distinctions between them. The other systematic question is whether Tavniinrtia should be considered a
v
separate genus or a section I "
i ll
Vink, 1970, 1988; Sampson et al., 1988). In this
paper data on Tasmannia are presented separately
from that for Drimys.
These results are part of a more compr. I
r
study of floral development in Winteraceae (Doust,
1997; Doust & Drinnan, 1999; unpublished data).
The focus in this paper is on early ontogen. h. pal
terns, especially of sepal and petal initiation.
M.VI'KRIALS \M) Ml-'.THODS
Freshly collected buds and flowers were either
dissected immediately or fixed in FAA (formalin,
in 70% ethauol. Preparatory to dissection fixed
buds were delixdrated in an ethauol concentration
series (70%. 85%. 95^1 and stained for greater
visibility with 1% acid fuchsin in 95% ethauol. Excess stain was removed from the buds b\ .Lub
washing in 95% ethanol for three days before dissection. Several changes of 100% ethanol were
used to rid the specimens of all water before critic.rl
point drying. After drying, specimens were mountbc-ci. h> in.' inai:. Jin. irh'-i ,-. I. I ': Id . i H il i: XI.'M) scanning electron microscope. Herbarium
specimens of a number of s(
i I
i were . xamui. .1 al M< >
The number of buds and flowers dissect.,I and a
list of voucher specimens are given in Table 1.
RESLI.TS
The Mo.
have a tubular ealyeine calvplra. which encii. lethe young bud but ruptures as the bud expands.
The remains of this calyptra are thereafter persistent around the base of the flower. The calyptra
bears two sepal tips, which are oriented al right
angles to the subtending floral bract in lateral Mow
ers but which are variably oriented in terminal
flowers (Fig. 2A). The next organs to be initiated
are two opposite decussate sets of petals, the fourbases of which are valvate and connate while the
lips are lice and imbricate The tips of the lirsi initialed paii of lh.se two pans of petals overlap those
of the second. The first pair of petals in lateral flowers is usually oriented parallel (rarely perpendicular) to tin orientation of the lateral sepals t Fig. 2\).
It was not possible to discern the orientation of the
first petal pair relative to the sepals in terminal
flowers. The two pairs of decussate petals become
connate basally as they grow. They max also be
more or less fused post-genitally toward the apices
ol the petals. An adaxial groove is formed al the
boundary between the connate regions of adjacent
petals because the adjoining tissue is tliinnei than
the petals themselves. When the petal tips are disected awax from the flower an invagination of the
dermal tissue is also clcarlx e\ ident when the
boundary region is observed on the longitudinal
edge of an individual petal (Fig. 2B, C). The four
outer petals rupture along the boundarx groovewhen the flower expands al anthesis.
following the I,
two pairs of petals,
petals are initiated (Fig. 2B). On rare occasions
fewer or greater numbers of petals max be found in
these whorls. The petals in both inner whorls haxe
narrow bases and grow throughout as ootnplelelx
free structures. The arrangement of the petals imostly regular, although the si/.es of the petal primordia in the inner two whorls vary, apparently according to the space available for them. The second
inner whorl of petal primordia is initiated almost at
whorl, and. with continued expansion of the meristem. members of the two whorls rapidly become
tiii in-hable and the petal bases appear to be
in one whorl of eight. However, the middle whorl
completely overlaps the inner whorl at its apex.
MV\ < \l : noM \. lini.-.v lil.-u.

>., I" ' !>:.s! <<:>. (MELl I. ,
Dec. 1967. Sampson (WELTU). 7 Dec. 1967. .Sw/,i/i (W EITU).
NEW CALEDONIA. Near top of track from Sarramea to Plateau de
Dogny. Dec. 1996. Doust 026 (MELl I; Old lumber road S of road
leading from Cascade de Cm to Koiudc and La Koa, 10 Dec. 1993,
McPherson 6121 (MO).
NEW CALEDONIA. Forested slopes of watershed of Riviere des Pirogues. N of Noumea-Yale road. 15 July 1981, McPherson 3945
(MO); Thy River valley, ca. 12 air km NE of Noumea, McPherson
3082 (MO).
NEW CALEDONIA. South of Tliio on coastal road, between Nimbo
and Camboui Rivers, 26 Apr. 1984. McPherson 6517 (MO); road N
of Canala to Prokomeu and Kouaoua. 20 Apr. 1983. McPherson
5621 (MO); Prokomeo Region. N of Canala. 28 Dec. 1983, McPherson 6222 (MO).
AUSTRALIA. Lord Howe Island: 2 Nov. 1963. Green (WFLTU), 8
Dec. 1968, Chinnock (WELTU).
NEW CALEDONIA. Mt Panic, ca. 20 air km NW of Hienghene, 31
Mar. 1981. McPherson 3605 (MO): Mandjelia. above Pouebo. 30
Jan. 1984, McPherson 6280 (MO): I'oucbo: Mont Mandjelia, 6 Mar.
1979, MacKee 36654 (MO).
NEW CALEDONIA. Ponerilmuen: Mont Aoupinie, 8 Sep. 1976,
MacKee 31875 (MO): Mt Panic, ca. 20 air km NW of Hienghene,
20 July 1980, McPherson 2882 (MOl; along old lumber road to top
of Mt. Me Ori. above katrikoin. 6 Sep. 1980. McPherson 3045
(MO).
NKW CALEDONIA. MasMf de Boulinda. ca. 8 air km \ of Pova. 22
May 1980. McPherson 2602 I MO): Mont laom: Crete Est, MacKee
38150 (MO).
NEW CM EDONIA. Haute Amoa. 9 O.-i. D7I. MacKee .'I loo I MOl:
Sep. 1982.
i lo;';; (MO); Dureim loo:, i Mil i.
(Baill.) Tiegh. ex Morol
son 5929 (MO); Bogucn Km-, Valley. aLg In
lington, 3 Nov. 1996, Doust 891 (MELLI); Akatawara Road. Upper

Hutt Valley, 4 Nov. 1996. Doust 802. 801. 895 (MELU); Kakanui
Ridge Road, S. Tararuas. 4 Nov. 1990. Doust 895 (MELU).
NEW ZEALAND. North Island: Kakanui Ridge Koad. S. Tararuas. 4
Nov. 1996, Doust 896. 807. 800 (VILLI ); S. Tararuas. 1995. Sampson (WELTU).
AUSTRALIA. Victoria: Bemm River. East Cippsland, 5 Aug. 1995,
Doust 832 (MELL): Mt. Maccdon. 23 Dec. 1990. Doust 932
(MELU); Mt. Donna Huang. Yarn. Ranges National Park, Nov. 1997
Doust 991-1007 (MELU).
AUSTRALIA. Victoria: Mt. Donna Buang, Yarra Ranges National
Park. Nov. 1997. Doust 081 W3 (MELU): Lake Mtt... May 1995.
Doust 782 (MELU).
AUSTRALIA. New South Wales: Point Lookout. 30 Aug. 1981.
Sampson & Foreman (NSW I: Point Lookout. 15 Sep. IM}5. Samps,,,
& Williams (NSW).
AUSTRALIA. Nen South Wales: Dilgrx. 28 Nov. 1983, Williams
l NSW i: Moffat falls. 8 Nov. 1986, Sampson (NSW).
AUSTRALIA. New South Wales: B(

1965. Sampson (NSW); Doyles Riv
Foreman (NSW).
Zoology building. On. \<m. Dnusl 1127 mo (MKLl ) (.nit.
MADAGASCAR. Pref.-.tme \niiileliu Sous-prefecture Andap
follow
mill; linn. Tin te an usually eigh; stamens in each
!
IK
uncus in the first whorl altern.
i
ii i 'L!I [i I Li-'- M ned from the two
nine: whorls ol petals ( big. 2D). Succeed r- who Iof stamens alternate with each preceding whorl,
ami ill' r- arc isiialh ilu- -am. riiirnli.-i of stamens
in each whorl. The last whorl of organs initiated
i II- both stamens and carpels, and the larger
size of the carpels often leads to a reduction in the
total number of organs in this whorl (Fig. 2D). The
carpels are connate but there are no connections
between the stigm ili. in-- n .1 thus no common
pulleii-lrarisinilliiig tract Ilgersheim X Kndre--.
1997).
Ill HHIA HOWKAXA
Each flower of Bubbia howeana has a calycine
calyptra lh.it protects the bud cat \ in development
but which ruptures as the bud expands. The renin I ilu b
MI
(lower. The calyptra initiates
as two laterally placed free sepals but attains most
ol lis growth b\ ill. a-lion oi an annular meri-lem
und i ith the sepal tips. Two outer d< . us>alc
pairs of petals are initiated next, with the first of
these two pairs el ; i 1- n m< .1 . i p!
to the sepal tips. The two outer decussate pairs of
petals in the flowers of B. howeana are free
throughout their growth, and they tightly wrap
in i i .1 11
bud an
rotect it as it develops (Fig.
2E). An inner whorl of petals is next initiated with
four or rarely five petals, followed by a second
whorl of petals and/or stamens (this whorl is shown
as the outermost whorl of stamens in Fig. IB).
Three or four alternating whorls of four or five stamens are then n i
i b\ three to -ax
free . arpels arranged eilhei symmetrically or more
irregularly.
I" i
'-
/>_ .-
."
"'./
' >'
a.
/.'
' '
i '
,',:
In Zygogynum bailloni the lateral sepals arc followed h\ a pair of lateral petals (Figs. 1A, 2A),
whereas in Bubbia howeana the lateral sepals are
followed by a pair of medial petals (Figs. IB, 2E).
I Ih S. < otill 1st in
I
i
,1 |
in
n > ' i
were examined in herbarium specimens of a number of species of Zygogynum, Bubbia, and the related genus Exospermum (Vink, 1985), and the results are given in Table 2. There is a clear
<lis|in< linn in p. tianth pah. ml
n Bub
i
the on.- hand and Zvgog\num and Exospermum on
the other, with lateral flowers of all species ol Bubbia examined having lateral sepals and medial first
petal pair and lateral flowers of all species ,,)' "/Auogvnum and Exospermum examined having lateral
sepals and lateral first petal pair. The two groups
I IX>\\ I \TLR.A AXILLARIS A
r.i:>i;\! ;
No material of the earliest developmental stages

for either species of Pseudowintera was examined.
However, at a somewhat later stage the buds are
enclosed in a < al\c me calyptra that has two Lateral
sepal tips. !'. R. Sampson (pers. conim.) and \ ink
(l<)70) reported that three sepal tips may be present. The calyptra encloses the bud during early
development bul ..as.-s gn.wth while the bud is
still small. After the calyptra is ruptured by the
expansion of the developing bud two or three lobes
persist around the base of the flower. The pattern
of initiation of the petals is somewhat variable, and
(ID
E. Tasmannia
lanceolata (male)
G. Tasmannia
xerophila (male)
ca)
F. Tasmannia
lanceolata (female)
H. Tasmannia
xerophila (female)
81 >
&
I. Drimys winteri
(terminal)
J. Drimys v
(lateral)
00
Volume 87, Number 3

2000
Doust
dil
i in size of the petals may inch il
they are initiated sequentially (Fig. 2F). However,
the petals are often in two de<
- I
i ?ui
ther petals in a whorl inside these first four petals.
(llhei patterns, such as spirals and whorls of three,
TASMANIA IANCKOIATA AND T. XEROPHILA

I llh
ill I II
II
II
II
ill!
sepal and petal

both male and mmaie flowers | ill I .., 11:11 Pie numb, i
.1 . i^.nis . an d l'( i In l,is!"a "1, > ",i'n ,;:,,: ,\
sepals are initiated at the lateral poles of the mer!
istem.
II wed by the initiation of two more sepals
situated medially (adaxially and abaxially) (Fig. 3A,
B). The abaxial sepal is at first only a line of tissue,
but a flap develo
m in later develap-ll! I ll -la_. s |r, /./s.7,r/,-,'.'.. . ',; ' ,/ in ' I
other species of Tasmannia examined (Table 1) only
medial -rpa - are mtialed. the adaxia s. pal mi
tiating before the abaxial sepal (Fig. 3D, E). The
eonli aed
owiii ol
both species OCiTfloiaf meri,t,.
371
Comparative Floral Ontogeny
,':" that th
ml
al.; t:a
organ So lie initialed in pishllale flowers of T. lanccnidhi a single tern inal carpel i- mi! aa <i . Itci lh<
initiation of the petals, while in other species a
number of lateral carpels are usually initiated (T.
insipida only initiates one or occasionally two carpels). The position of the first four of these lateral
eai |M - allernah - w th tin positions ol ll:e i;t< >I . I
sepals and lateral petals (Fig. 3F). When more than
two
.. .
p<-;a:s
,
r
"whorl
: iv
.
m hated
...
ol llie meiiia
lli< s
.
alternate
11,1
Willi
L
the
and lateral petals in
ated for t
carpels (Fig. 1H).
The
inflorescences
of
posed of a niniibei ol raeei
Drimys
s<
winteri are comlilorescenees w ll li
.1 terminal and up to eight lateral flowers. In terminal flowers the ealyeine eabptra initiates as a
in-j o1 1 is-me noimd be appioxin ateK circular Mo
ral meristem (Fig. 4A), whereas in lateral flowers
two sepal tips are initiated lateralh with reaped to
the subtending floral bract (Fig. 4B). These sepal
li
P8 * subsequently borne aloft by the growth of
i cal>( ine ring ol tissue around the floral i
grows as a cylindt
bearing tl
I
apex. The eabptra encloses the bud until
In all species of Tasmannia p.mils are

soon after the sepals and alternate with
Tasmannia lanceolata four petals alternate
mannia two lateral petals initiate perpendieuhu to
the two medially placed sepals (Fig. 3E). In all spe
cies further petals may be initiated alternating with
the previous whorls. (Note that in Drimys piperita
[Tasmannia] s.l. [as defined by Vink, 1970] staminate and pistillate flowers of the same entity [specics] may have different numbers ol petals [P. V.
Stevens, pers. comm.]). In staminate flowers in Tas-
considerable dela\ between initiation of the calycine calyptra and the corolla; petal primordia apP<'" oK when the calyptra has almost enclosed
the floral meristem. At this stage the floral meristem
is large and domed, and petals initiate low down
on the flank of the dome (Fig. 4C). The initiation
nl stamens follows the petals without delay. A number of tiers of stamens are initiated on the almost
tion follows directly on from the initiation of the

petals (Fig. 3C). The arrangement of the stamens
may be variable, as the shape of the meristem is
ngle sterile carpel is the last
of carpels follows the stamens without delay and,

as the growth of in I u n
I em ceases, the carpels eventually develop all over the flattened apex
of the dome (Fig. 4D). The a
Figure 1.
General 1/
il
m i< h ol lli.
ia\a examined
Tlie^ ;e diagrams give only the main outline of
floral ii i.tiation for am species. In all diagrams

the top of the diagram and the sublending floral
ttom. Organs positioned
âns positioned 111.sdially < ire at the top an.: 1 bottom of the diagrams.
1 these patterns can he found. es| ecially in Drimys. . Pscudowinlcra, and in the numbers of stamens
nly the
and the others hav e been indicated by broken circle s. Drawings an
whorls have been shown

n to scale relativ e to each other.
Sure 2. A. Zvf!Of!Yiutm hmlloni: a terminal and lateral bud, with the lateral hud (left) showing the lateral
ion of both the sepal lip |I.S| and the lirsl pair ..( outer pel.,U I I ). The ,eeod pair ..I .ul.-r ,..-t;il>. perpend leula.
s relative to the sepal 'tips ,. nut , lea. s. al<
1 mm
It / luulh.m a vonng hud with raUpt... ...
. I" s
I
,1
, , I
'II
-_,
idiom: a longitudinal view of the hasal region of the edge ot ;
-,(M) pm
D. Z. badloni: late bud sU

irregular arrangement of th
of second v
, i
iMhd S. .1,
2<M)pm
('
ile, pei..l -,|.m\mg the -.mooll. eo\er.ng of
I ealvptra and petals removed, showin
Is as they begin to enlarge (outer pet;
inner petals = IP2). Scale = 500 p,n
.liter petals (2) is also visible. Seale =

3 mm. F. Pseudowintera colorata: a young bud wi
almost opposite petal 3 but petal ."> (|>5) appears I.
Cable 2. Perianth pal

n | i I miaiion in -cm. species n! Z\gog\num. Exo^n-rm
e observed from the fresh an. I herbarium specimens detailed in Table 1. Positions noted
r of petals arc itd.iti\ < to the -.ublending Moral brael.
f petals
l;ui,h,
Ih.
Petal c
Z\gog\num ha,!!,,ni
Zygogynum bicolor
Zygogyruim pomiferum
less regular whorls or spirals.

- ,//; i,',\
\ i : /,',',-; -
The llo\\i-i il 'inhhutjaiiui ncrricri has a twof;;[>.<! abeine rakplra ui'l tne lobes oriented la!
erally with respect to the subtending floral bract.
Vlthotigh no soling buds at earl\ stages were available it is likeK lb il tin
calyptra initially
encloses the bud before rupturing as the bud increases in size. Fragments ol the cabcine cabplra
are persistent around the Moral base m flowering
ind I'miling stage-. The mhain.n ol this cab ptra
is followed by initiation of the outer petals in two
< issal | lirs \ltei ih. iniii iion of the outer two
pairs of petals an inner whorl of four petals is mi
tiated, the positions of the inner petals alternating
with the positions of ihe loin otii.-r petals. This is
followed by the initiation of a further tetramerous
whorl of petals. The outer petal pairs are imbricate
ping edges (as shown by Endress et al., 2000), and
[he basal adaxial la< e of the oinci p< lab i- pan; IIfused to the abaxial faces of the petals in the first
inner whorl of petals (Fig. 4E, F). Occasionally
more than four petals may occur in each of the
inner two whorls of petals; sometimes this is because the fifth petal is in the position of one of the
stamens of the first androecial whorl. Usually two
before initiation of the gynoecium. The sun-arpons

gynoecium is terminal, and its i orph lof is full
described by Endress et al. (2000). The overall
structure of the flower comprises three sets of opposite decussate whorls followed by alternating te
tramerous or pentamerous whorls, am I ending it
the formation of the terminal
In all species of Winteraceae the calyx forms a

lubiilai calyptra, which completely encloses ihe
bud for at least a short time during development.
The presence of the calyptra appears to be a synapomorphy for Winteraceae, as neither of the likely
outgroups of Canellaceae or Degeneriaccae (Sub et
al., 1993; Nandi et al., 1998; Karol et al., 2000;
Endress et al., 2000) possess such a tubular structure enclosing the bud.
In Drimys winteri, Tasmannia lanceolata, and T.
xerophila the calyptra grows with and encloses the
bud until anlhesis. abcising as the flower opens.
However, in Z)g<
MI/'
'.//'/ the cal\|>Ira < n< los< - tin hi..I mil i
i . d< \< lopment
arid is ruptured as the bud enlarges. The remnants
of the ruptured calyptra persist around the base of
the flower and can still be seen in flowering and
In
: tag. - i
l\ -tag. - >>\ tile Hon. is oi '/;,/,/;
I i i i I il11, lor study, but the
mature flower shows remnants of the calyptra
around the base of the flower similar to those found
in Zygogynum. /:*./,,,,. u d l's>-u<lou>intera. This
implies that in T. perrieri the calyptra encloses the
bud only in early development. Other species of
Zygogynum, Exospermum, Bubbia, and I'.sen,ION
iiitrm also have a calyptra that encloses the bud
onb during early development (Sampson. I'.><>.<:
Vink, 1970, 1977, 1983, 1988).
The first stage in the development of the calyptra in nearly all flowers in the family is the initiation of two or more sepals. The exception is in
the terminal flower of Drinn*. '<>>
[.II
other species of Drimys as well), where the calyx
initiates as an annular primordium surrounding
pairs of sepals. Scale = I(X) pan. C. '/.' hmcrolata: semi-mature hud with ealyptra remo\ed -.bowing the initial ion of
four petals (P) and a nuruher of whorls of stamens (S). A sterile carpel will he the last organ to he initialed. Scale
200 |xm. D TIIMII
I
,
I tin adaxial sepal (ADS) and th< meristem (M)
/: urn/,/,,/,,: hoth adaxial (ADS) and ahaxial (ABS) sepals have been initialed and two petals (P) have now been
initialed in lateral positin
rnal
itli h. .epals. Scale
100 pan
I T. u-mplnla: a \oung hud w ill) the sepals
removed, showing four carpels (CI that have been initialed in positions alternate with the medial sepals and lateral
the floral meristem. In the lateral flowers of D.

winteri two sepal ti - ' i
I i 1
uJmg, II
ral bract are comrn
.
-rfore the bulk
of the growth of the ealyptra takes place via an
annular merist.m. The initiation ol sepals lateral

'
I
In -II
I hi
I i- also seen in lateral
flowers ol Zy^
um fiuhbiu, and
Pseudowintera. A ealyptra also forms in terminal
Ji
E^-V WW
LS
:LS ^
Wri
t'1
^^ytk j^-VM "B^T
IUMBBI
IHHIHV^^V
Figure 4. A. Drimys uintcri: .1 lerminal fl.mei I MI.

.rimordium (CX). Scale = 100 u.m. B. D. winteri: a
00 pm. C. D. min/m: a lateral bud with the calyx 1
irimordia being in no particular relationship to the an
5
(C) in this
,ged in a spiral patt.

1,
,.
11
'
.1
.111
>WM
f petal primordia (P). with the
sepals. Scale = 100 u^
) u,m. E. Takhtajani
. , , i
I,
,.. i ,!l
ill lb.' s.'pnls 1- iiiclcar, li TusuHii.nin iuiw;,j.iU!
ro lateral sepals are initiated. Thus the pat-
lateral sepals are initiated as well as a fu 1!

1
of medial sepals. In T. xerophila only two medial
sepals are im11.1' I I 1 1 > . 1 -. n 1 n
sepals, two medial sepals, or two lateral

followed by two medial sepals. By itself,
the pattern of
hii-mui.
/xr<^M,'ti::.
el eight petals (!' g
Hnl.l.td.
and
I\< ;:!.<>: <!>!>-;a.
stamens
each
~1\\). Succeedin;.', whorls ol eight
alternate with
I at Ian I hati with 'ias'uuini'ii. The pattern shown bv
eight petals (Figs.
'lasmiitunii lanrr<>!atd
organ arr.nigeiiiei:1 an
i 'v..
:il.'i;il sepals and Iwo
medial sepals) is intermediate i . iween the flowers

!
.dose of the rest
The
pattern of initiation
of
species
of
the
pseudo-whorl of
(Ten seen in tin
ZygogMium
\i)\\(,\.
(pers. olis.; Kndiess.
and
I'li.-s.
lair.ei flow
/\T"v>; <;,;<;,,
hav e piev ioiislv
li. :i explained as the result of the combii at on ol
of the genera in the family.
manrtiit and lh;m\s IM;I\
ers
1A, 2D). Irregularities in floral
of the
sepals
in
Tas-
help decide wlielhei these
asymmetry of the floral apex and the

-ui.il
[irniiordia
relative
to
the
initiation of
size
of the floral
apex (Endress, 1986). Another cause of irregular

(Smith,
1988).
1943a,
Smith
b;
Vink,
(1969)
1988;
Sampson
segregated
et
Tasmannia
as
separate genus from Drimys because of differenees

i
. 'iM ...-,, ii
nliei
(/.
id, n =
13, Dri-
mys, n = 43; Ehrendorfer et ah, 1968), and sexuality of the flowers {Drimys is bisexual. 7.
is
unisexual
did.a
&
and
i ! ni.-d \
Harvey,
m-i
in 'I ivom
1982).
I l><
Vink
and re< ..ml.in. .1
''
(1970,
that proleets the hud

eonslruetion
I><- f
/.
th n
-p
'
,
'
by
Suh
et al.
IL'OiH i) '/,
(1993)
ng the . alv plra
and
-lameii to . arpel
a whoi I
: m tin i
pro iuclinii < an
peilinb ill.
pailern
of primordial position.
initiation in
/u.^'i'i"./. -iiiI / o>\ ' /run: (laieial -. pals
laleial
first pair of pet.i
in. >nc|..., h.i

Dunns,
I
um
s.
ter
observing
sir.,
and
Karol
the decision by Vink (1985) to combine /./
et al.
nig In
Exos,
hhid
/,
into an ex-
'ygugynum s.l. Vink made his decision althat
the
s. pa rate die gel el

als and
carpels)
main
(i! gn i
,,,-
characters
>] , .a II.il
\anable
used
ol ill.
within
each
variability was observed
in the present study for
the tree. The differences in position of sepal initi-
species ol
However, the position of the sepals and firs! pan
consistent
of the
with
molecular
>orts the branchand
is
Tasmannia being a sepai.Ce g i
is
d mi Dnm\s. Tins impl <-, thai

caUptra
phvlogenies,
Ine possession of a
that encloses the bud until anlhesis
ma\
to
pel
genus
and transitional between genera (Vink, 1985). Such
ation betweeti th<

ing pattern
sepals, medial first pair of petals) was also noted
Drimys do not appear as sis-
ter taxa, but as -
from
in
by Vink (1977). This difference does not support
:i >ve Ins.Mlal llowi is. Ill the rnoh eldai pi \ l< -on es
presented
:ia
1988,
n .1
I
I r i r 11
(A'TtiMi.annia.
ml ! anlh.-sis. tin
ol
the observation
stamen and
The difference in sepal and petal
d opposition ! \\ i!lian:s
However,
i u nts is that the changeover from petal to
occur within one whorl. The different sizes of the
inn genera also
I'**'.'-;) disagreed w ill ill.- .cgregalioi
li a i ,.
ah,
'/\ i
i
petals indicates that the three genera fall into two

I >ll is
/lu,.i
',
.,
Tins suggests thai

1
. I
jt uv
i m tlii
<
be
II ,| i/.'.,''' ,-/
.! u:: igeoiis to Us.
to reexamine the homoloj
I p. I
have evolved independently in these two genera.

A basic pattern of sets of decussate and whorled
organs is also found in flowers of Tasmannia. There
ate two distinct variations in this basic pattern of
Flowers
arranged
in
in
Winteraceae generally have
pairs
ami
pattern in the flowers

of
whorls.
In
most
organs
eases the
- !. i.-in iii.-d b\ the position
the sepals, and. in general, -m . . . din
whorl. This is (IK
is.
where a lateral pa i I
u, /,
-epa - is T lowed !n
pals
is
initialed
. ni w iihii
followed
il
IB, D,
2E). A number of whorls of petals, stamens, and
liow. h oi
i'a-.m.in
by a medial pair. A te-
li ma ion-- .v a >r! > 1 p> ".il |.: lln
whorls of organs alternate with the previous pair or
and lateral pairs of petals (Table 2; Figs.
iloial organ arrai g. i
nia. In Tasmannia lanceolata a lateral pair of se-
.1
- ihei
in ] at- <!.
positions of the four petals alternating with
those
ol
dual,
flowers), or a carpel (female flowers) are then
the
initiated.
loin
In
mordia an
[siiiMo-dia ii'ir
eurs in Zygogynum and Exospermum, except that
(which
mav
sepals.
lurlhei
Tti
petals, stamens
two
sepal
pri-
in haled uiedi illv. follow. .' bv two petal

,i... laterally. A whorl of four organs
be
petals,
stamens
|male
flowers],
or
the sepals and the first pair of outer petals are par-
< aipels
allel with each other (they are both lateral with re-
nating with the "whorl" comprised of the pair of
spect to the subtending floral bract) (Table 2; Figs.
sepals and the first pair of petals
1 A, 2A). In the large flowers of Z. bailloni the two
also be initiated. The similarity in floral organ ar-
. whorls of
petals initiate al-
ind act as one pseudo-whorl
' Ii ale
lowas|;
tin i
niliah d
allei
Ylore organs can
s(
tWO Sp< , II s
Volume 87, Number 3

2000
Doust
organs are followed by a tetramerous whorl of orgaiis. The differences arc in the position of the first
pair of organs (lateral sepals in T. lanceolata vs.
medial sepals in T.
.'/ i i
i tlie identity of
the second |.an >l
i
ul- in T. Ianceolata vs. lateral p< t h in
.
i ".III iii
species of Tasmarmia examined onform to the pattern shown by T. xerophila.
The initiation ot the perianth in Pseutlau intern
is consistent with the general pattern described
above. There is usually at least one pair of decussate organs, the laterally positioned sepals, but
there may also be one or two decussate pairs of
petals alternate with the sepal tips. Vink (1970) and
F. B. Sampson (p<
, led that three
sepal tips may also occur, along with trimerous
whorls of petals and stamens, as illustrated by Vink
(1970, fig. 3e). A transition to spiral arrangements
of the stamens and u
Is -I rlint dth tin innermost petals also has been observed.
The floral arrangement in Drimys winteri is unI
I here appears
pa
i
i
gements of petals.
stamens, and carpels), and some flowers of Pseuil<
llenialing w ilh the
sepals but further petals eillier in whorls or spirals).
A basic pattern in the family of four petals altern i i
lid
I li
il-n postulated l>\
Vink (1988). Thus the similar patterns of floral organ arrange im i H
< rrirn and liuhhia
hoireana show die general relationship in the (amily rather than being evidence of a special shared
relationship.
Both Zygoi
rieri have fused
ii T > > i
Sin h fusion does not
generally occur in the corolla of the flowers of the
other genera in the family and may provide evidence of a shared
lain u i;>. The method of fusion of outer petals in Z. bailloni is both through
connation in the basal regions as well as variable
amounts of post-genital fusion in the otherwise free
apical regions. In the species of Zygogynum that
display basally connate petals the mode of connation may be the result of coalescence of the margins
to be no relation-du
n of the lateral
sepals or calyx and the succeeding petals. The lack
of relationship in lateral flowers may be because
the delay between initiation of the two organ types
may deprive the petals of positional information
from the sepals. There is, of course, no positional
information given by the calyx in terminal flowers,
as the calyx is initi . i
mi
i
encircling the floral meristem. There is also a variety of whorled and spiral floral organ arrangements in D. winteri, implying that petal, stamen,
led by sepal
of the pri;
(ii!
aed results; Krbar &
of the petal primordia as they grow, whereupon the

epidermis in the region of connation disappears,
However, in T. perrieri the petals cohere only
through post-genital fusion of the cuticles, the fusion occurring by the interdigitation of the cuticles
in the overlapping petal areas (as documented by
Endress et al., 2000). Interdigitation of the cuticles
ua- also observed to occur between the bases of
the outer p I I H ! die basal portions of the next
inner whorl of petals. Post-genital fusion as it occurs in T. perrieri may be likened to a cohesion of
the petals rather than a true connation as found in
the basal portion of the out)
This makes it possible that the morphological similarity between the fused outer petals of the two
AFFINITIES OF TAKHTAJANtA
CONCLUSIONS
mid perrieri was originally described as

a species of Bubbia by Capuron (1963), and its
floral architecture is similar to that of Bubbia howeana. Both species share a decussate pattern of the
sepals and first two pairs of petals, followed bv a
whorl or whorls of petals and several whorls of stamens in fours or fives. However, the basic pattern
of decussate pairs of organs followed by whorls of
:
organs has been shown to hi
-i11
the family, with exceptions being found only in the
relationship between the sepals and the first pair
of petals in Z\gm.
i
i
terminal flowers of Drimys winteri (no decussate organs), the lateral flowers of D. winteri (opposite se-
The study of the ontogeny of the flowers of Wi

teraceae re\ea
I iota iiahmg patterns and inn
peeted coniph >:\ The underlying pattern of floi
organ arrangement is one of sets of decussate a
whorled organs, occasionally turning to >pirals
Drinn.s am
I ht lei em e*, within t
basic pattern include the number and position
sepals and the position of the petals relative to t
sepals. In all species irregularities in floral ap
symmetry and in the size of organs in a whorl m
perturb the regular whorled or spiral pattern, lea
gnlai floral organ <
rangements. There is a clear morphological di\ isi
in the family between those taxa that retain t
caUeine < alyptra until unl

i I ' - < , n d
Drimys) vs. those where the ealyptra is ruptured
carl\ in dcvelupmcnl [llnbinu /\^>>ûi'i:n /'.'UM
pcimuni, Psrin!
ever, differences in tin- position and mitnln-r ol sepal- !>c|v\eeli 7as!H,l.'lli>,l I<llir>;i!(!l<l. T. iC!,<;>li >!,t.
and Drimys winteri suggest that the two genera
should not be combined into one. Differences in
tlie position of tin
' relative to the
sepals suggest thai Exospermum
are (li-lmel
hum huhdin
I'M
,
.
.
-,,,,
ul orlei!
inaimeiiiei:! oj the ll.ual
deriissah
icân-
a:
and
,. ; //,,"
tajania perrieri is closest to that of species of Hubbia, but this pattern is common throughout the family and does not serve as evidence of a special
F
\ .
. . ,
.
,
,
fusbnTf L ,ul7
'
and
Z\<!ui/\nuni.
.
'"""
These
observations
.n
' '"
'
'" '
i!
'
' "
'
'"'
'!
' '
.
'
"
'
" *
Igersheim. A. & P. K. Kn.lress. 1997. Cynoecium diversity and systematic* of the Magnoliales and winteroids.
Bot
- > Unn- S'- 12,: 213-271.
Kami. K. (,.. VS.ili. (.. I . Nh.H/. X I-.. W.ein.,.
I .'!). I
'"", '
post-genital and !.
I the cuticles,
whereas that in Z. bailloni is primarily by connation of the basal region
of the petals. These differ5
ill
ences do not support a close .,1 ilmitsl, p hcween
Ttiklilajtimu
!jV-" '.^"|,;r|)ar. c. & p |,.ms. \<m;). /, Sequenz von Bllltenorganen hei einigen Magnoliiden. Bot. Jahrb. Syst. 103:
433-449.
'
''
genetic position of
rihosomal and ehloroplasl gene spacer sequences. Ann.

^MU^- * '**> i<; >"^ ';* "';" " n-K.1,,,,11,
talsachhehgebaut? I. Die karpelle von Dnnns. N-klmti
Tasmmuim. Oesterr. Bol. /. I 12: 554-575. "
p)(>(>.
W ie sind die \\ inloraeeen-karpelle lat-
are congruent with the niolecuhu phvlogeny of Karol et al. (2000), where Takhtajunia is basal, and
sachlich gehaut7 III. Die Karpelle vim linhbui. lirlliol

'<"' ^"^" j^ "' / '-/"'"""" '""I ^gogynum. Oes-
its unique syncarpellate gynoecium autapomorphic.

1 he ontogenetic data presented in this paper are
a step toward understanding the evolution of floral
form in Winteraeeae. On the basis of robust inter-
JZ }t l<>77 " \ compound -van with open carpels

in Winteraeeae (Magnolialcsl: Ew.lulionarv implications. Science 1%: 977-978.
Nandi. 0. I.. M. W. Chase & l>. K. Endress. 1998. A
pretations of phylogenetic relationships within the

in
.1 her papers, this issue), an understanding
of the evolution of diverse and variable floral forms
within such a well-defined uionophvletic group will
also advance our understanding of the evolution of
ÎÎS '
'
Mi ri Bot" cd
^-. p5- ->p>
Oi, Y-L. M. W. Chase. I). H. Pes & C. It. Parks. 1993.
Molecular phylogenetics of the Magnoliidae: Cladistie
m..K-- ol ^,, I
.id,.^pUnd gee
the flower in basal angiosperms.
Sampson. T h"
Literature Cited
'
. 1! phol.^f Pseudow-
teraeeae. Phytomorphology 13: 403-423.
phologv of Ihe Winteraeeae. II. Carpels. J. Arnol.l \r|mr 24: 172 181.
-&
. ' 1945. The comparative n.orph gv
morphology and laxonomic position of Tasmannia glauci/olia (\\ interaeeae). a new Australian species. Austral.
J- "<" /'*<>; '*>"> 413.
\rn<ild \rhor. 20: 37-47.

Bessey, C. E. 1915. The phvlogenetie taxonomv of flowering plants. Ann. Missouri Hot. Card. 2: 109-161.
Burtt, B. L. 1936. Bubbia haplopm B. L. Hunt. Winteraceae. Hooker's Icon. PI. 34: t. 3315. 1-3.
Capuron, R. 1963 \ll I'resenc, i Madagascar (fun
1998. Tnkhlajuiun pnru-n red ^covered. Nature 391:

133-134.
Smith. \. C. 1943a. The \mcrican species of Drimys. J.
Arnold Vrbor. 24: 1-33.
19431). Taxonomie notes on the Old World speies ol Winteraeeae. J. Arnold Arbor. 24: 119-164.
des Winteracees. \da.,son,a 3.\/> 378.

Cronquist, A. 1988. The Evolution ami Classification ol
(Winteraeeae). Tuxon 18: 28<. 2<>0

Sufi. V. I.. B. Thien. II. E. Peeve K E. A. Zimmer. 1993.
flowering Plants. 2nd ed. fhe New lotl Botanical Car-
ust, A. N. L. 1997. Variability and pattern in the flowers of the Winteraeeae (Magnoliidae). Amer. J. Bot. 84:
40. [Abstract.)
& A. N. Drinnan. 1999. Floral form and ontolanical Congress 917. | Abstract.]
irendorfer. E. E Krencll. E. Huheler & W. Saner. 1968.
Molecular exolutiou
and
pin logenelic
implications ol
DN \ in W iuteraceae. \incr. .1. Bot. 80: H

Tucker. S. C. 1959. Ontogeny of the infloi
flower in Drimys winteri var. tlulcnsts. I nc
Bot. 30: 257-336.
Pseitdouinlrni and Drums
Blumea 18: 225-354.
Morpholo-\ a
/.Mtui!\m,n, \l.ii|ir!(ii ><i\ and IMMH, omy. Blumea 23:

_l < J.li
. 1983. The Wintera ceaeofthe Old World IV. The
Australian species of Bubbia. Blumea 28: 311-328.
. 1985. l<;e Winlr .
ks Bubbia to /\f!,lfiM,im t. Blumea 31: 3955.
. 1988 . Taxonomy in Winter. lCeae. Taxon 37:
/;,-
<><>]
(><)!>,
^Vascular Plants, Vol.2 Flowering Hants

s, Magnoliid. Hamanu
nilies. Springer-Verlag, Berlin . Heidelberg.
THE POLLEN OF
TAKHTAJANIA PERRIERl
(WINTERACEAE)1
phologv and ulliastrii
iM
leiov
lli,
M.iLi* is\ menihei
raceae, were studied and compared with pollen of oilier members of this primitive angiospcrm lariiiK.
)ermaiietlt tetrahedral tetrads, which are the largest
m the lamib.
\- in Ihmns .nul I'srmlowinlrm. the
expanded into protuberant papillae, suggesting premature commencement of growth of the pollen tubes.
circular or slightly oval, and
il
is concluded thai
previous icporls ..I colpale and Iruholo
eolpale
I leclale columellale and most eolumcllae have characteristic expanded bases where they join the foot
in some other genera, the aperture is surrounded by an annulus. with an underlying thickened endcxine
eiidexine. suggesting thai pollen milo-is is a-\ nchronou- uillnn a tetrad, a- in l\rn,lniniilri(i and Dunns.
ic deposition of inline after pollen mitosis. On the basis of ils pollen morphology. Takhtajania seems most
The rediscovery I /
- rricn (Schatz
et al., 1998) has pi .1 d . \>\ < 1 1111 Iv to stuck
liquid-preserved .1
11.1I loi
time. Although there have been three quite detailed
studies of the pollen of this plant (Straka, 1963;
Lobreau-Callen, 1977; Praglowski, 1979), they
were based on dried material from (he type specimen, collected nearly 90 years ago. These three
authors disagreed on the interpretation of some aspects of the pollen of Takhtajania.
TiiUitn/aiii.t pollen s in p.-rmaiK-nl [ci 1-literal
tetrads, a feature that occurs in all other members
of the \\ inleraeeae. with the exception of four species of Zygogynum, which have monads (Sampson,
1974; Praglowski, 1979; Vink, 1993). Monad pollen in these Z)goii\num species seems |o have
evolved from tin
teli
In
111 (S
up
MI
Doyle et al., 1990a, b). Previous studies on the pollet, of Takhlajania indicated that its pollen tetrads
are larger than those of other Winteraceae. It has
been claimed, too, that a few apertures of Takhtajania are of the trichotomosulcate type, with a
three-slit sulcoid aperture, in contrast to the invariably round or oval apertures of other members
of the family.
I thank I'I It r li 1
are tendered to Harry
m I
~
na based on liquid-preserved
material. This will enable further comparisons to
be made with the pollen of other genera of Winteraceae, which were studied in detail by Praglowski
(1979). It should be noted that the material used
in the present study was obtained about 150 km
southeast of the original type collection. This raises
the slight possibility that some differences between
po.len in ta< . 10 1- ,r1 : pieseiil studies may be the
result, not only of dried versus preserved material,
but also of differences between the two populalions
of Takhtajania. For as Smith (1943), Vink (1970),
Ehrendorfer et al. (1979), and others have demonstrated. there can be considerable morphological
11
bill
11
i[ 1 I
IK
of some species in
the Winteraceae. However, such differences have

not been demonstrated for their pollen grains. Generic names used follow those of Praglowski (1979),
except that as recommended by Smith (1969) Tasmannia is sul
set. Tasmtinnia.
The merging of Bubbia, Belliolum, and Exospermum into Zygogynum (Vink, 1985) is therefore not
followed in the present paper.
i I
Martin and Karen Header for assisling with (lit- eleciron microseopv.
Inn d
I
">|
I thanks
wish to thank Dallas
Mildcrihall for assistance Willi ac.-tobsis of the pollen and John Dawson and Use Breilwiesei lot translating papers in
Krench and (ierniaii. respectively. The School of Biological Sciences. \ it tor 1,1 I niveisily of Wellington, kindly provided
'School ol Biological Sciences. \ ictoria I niversily of' Wellinglot
NN. MISSOURI BOT. GARD.
87: 380-388. 2000.
Figures 1-6. Takl .,..

.
'-I \1 i
i t
apertural papillae (scale liar
III am). -2. Pollen
apertural papillae visible (scale bar = 10 u,m). 3.
indicated b\ a-leii4
in m
I I I
--It till polh u M i i i | inn i
ii In I H
i | I ml!
11 1
I
'.II
i ! I m three of the four protuberant
tetrad with the uppermost pollen grain in polar view and all four
Apertural region of a pollen grain in lateral view. Antutlus region
i I a |-i ale bat = ."> aril).4. Pollen tetrad with a
. nl i | iM i
in i
i HIII Inn the aperture in polar
torn into a colpus-like shape (scale bar = 10 ixm). 6. Center of a pollen tetrad with portions of three pollen grains
m). 9. Takhtqjania penieri (TEM):

ling the erulcxine, a black arrow indicating the intine, i
ell, which has a central nucleus (scale bar
r, IJL.,,). -10. Tukhtujania [x-rrieri (TEM):
e (scale bar = 1 |xm).
MATERIAL AND METHODS
Flowers and fW
ijama penieri
(Capuron) Baranova & J.-F. Leroy were collected
{P. J. Rakotomalaza et al. 1342) on 13 June 1997
from the Anjan.ih i
^
tsiranana, Madagascar, and fixed in FAA.
Mature and nearly mature pollen lot scanning

<lei-iu.il I'll. I'.ISI o|i<- (SI M I s||l.|\ Has (|-li\(ii-a!('()
; an <>thyl a|t.()|1()l/a(.,.tone st.ries, critical-point
oate.l with a thin layer of gold, and
examined with a Philips 505 SEM. Pollen for transI VI) study was postfixed in 1% 0s04, dehydrated, embedded in Spurr's
driedi sputter-
resin, sectioned, and stained with uranyl acetate

and lead citrate. Some mature pollen for light microscopy (LM) was ,..
11<I
me was dehydrated in a TBA series, embedded in Paraplast,
sectioned with a rotary microtome at 10 pin, and
stained with haematoxvlin, safranin, and fast green,
Measurements of external pollen features were
based on LM using acetolyzed material to enable
comparison with ol i
i V nteraeeae described in the pollen monograph of Praglowski

(1979); 50 tetrads were sampled.
For comparative purposes, pollen tetrads of
Pseudowintera colorata (Raoul) Dandy, obtained
from native forest, Brown Cow Ridge, N.W. Nelson,
New Zealand (voucher WELTU 12949), were examined under SFM. with treatment and fixation as
for Takhtajania.
RESULTS
The most striking I i

!
II i
li '
I
Takhtajania, which is shared by some other members of the family, is an expansion of the aperture,
suggesting premature commencement of growth of
the pollen tube (Fit;
1 I
i on
in the size of these "protuberant papillae" (Bailey
i\ \ast. 1943) even between grains of the same
tetrad. which m.n
.
'
<
of hydration of individual pollen grains. The surface
of the apertun nn i
contrast to a surroii
I
us
(Fig. 3). A few tetrads were observed in which one
or more of the polle
'
how a bulging
of the aperture (Fig. 4). Sections of tetrads revealed
that such grains wen; sterile. Sometimes the apertare membranes of these pollen grains were torn
(Fig. 5), with the ruptured part varying in shape.
The tetrads are of the acalymmate type (Van
Campo & Guinet, 1961), "in which each individual
pollen grain is encompassed by its own ectexine
which is tisualK i i, I ' I I
l< ped in the septal part" (Praglowski, 1979: 4), as in other WinterI
i
I edra) tetrads, radially symmetrical, heteropolar, seiniteclate. and
rounded to rounded-triangulai in polar view (Fig.
I
i
'lutes, mostly
round (ulcerate), although a few were oval. In hiteral view, each pollen grain has a hemispherical
distal (exposed) face (Fig. 1), excluding the shape
of the apertural protrusion, and a proximal region,
where the grain is joined to the other three members of the tetrad. .
c flattened inclined rather triangular surfaces converging near
the "geometrical centre" of the tetrad. Praglowski
(1979: 4) defined ihi ,,- "the point at the centre of

the free space between four coalescing pollen
grains of a tetrahedral tetrad."
Diameter ol l ii.i
l:i
\ ip< rim il protrusions, which are destroyed bj acetolysis. li.VM'i pin
(mean 74 pm); polar axis of individual pollen
grains 23-33 pm (28 u-m); largest diameter perpendicular to the polar axis 50-60 pm (55 pm).
More than 90% of the apertures examined were almost ex; nil
I neter (including llie
surrounding annulus) of 13-25 p,m (20 (xm); mean
diameter of apertures, excluding aniuiliis. 12.5 n_m.
The few oval apertures observed ranged from 6 X
10 (Jim to 8 X 11 pm. Width of annulus ca. 2.5-6
pm (Fig. 4).
The reticulum on exposed surfaces of the tetrads
has mostly medium-sized lumina with shapes ranging from square, rectangular, or polygonal to oval.
circular, and irregularly curved sinuous outlines
(Figs. 1, 2, 4-7). Muri forming the reticulum are,
therefore, straight or curved and not invariably
i I n_
li'i J
- il
nnd in pollen from
herbarium material. As Praglowski (1979) noted,
there are about 25 to 30 lumina in a pollen grain
seen in lateral view (Fig. 1). Some lumina are
smaller near the borders between members of the
tetrad (Figs. 1, 6, 7) and, as in all members of the
family with tetrad pollen, (he reticulum (or perforate tectum in Exospermum) is completely interrupted near where individual grains are fused (Figs,
O
lumellae were observed supporting the muri. Lobreau-Callen (1977)
noted that rarely the columellae are d u pi i coin me I
late, although Praglowski (1979) commented this
was not clearly confirmed. Columellae are cylindrical, not quite as wide as the muri, and they are
usually splayed out at their proximal ends forming
a rounded flattened cushion, which joins onto the
foot layer (Figs. 3, 6). The outer surface ol the foot
layer is mostly smooth, but at intervals there are
-n
entations of varying
size (Figs. 1-7). Thickness of the sexine was 4-6
pm and the nexine up to 1.5 p,m, excluding thinner
parts near the aperture of each pollen grain.
ULTRASTRUCTURE
Extraseptal ectexine is 5-7.0 pm thick, excluding thinner region-- neat apertures. Muri are elliptical to obovate in cross section and generally about
1.5 pm wide and 1.2-2.2 pm high, with a height/
width ratio of 1:1 to 3:2. Columellae ca. 2-A p,m
in height, i.e., as high as or higher than muri. In
extraseptal parts, the foot layer is continuous except
in apertural regions of the tetrads and is thickest
Ileal the exposed I'ln^c- gram-., whe!
!
it is 0.5-1.0 (JLII In- '
in .
I.
n< -1 . -- i
ll e
:11111 i <
Lie .1(1(1 lei Hi.'in I l-'i-. )). ]j dec Teases i
thickness toward the distal aperture of each polle

grain (Fig. 9). In septal parts (where the member
of a tetrad are c million--!, if. ! i i lav n is damn
0.1-0.4 (Jim. The inner surface
i smooth to undulate (Figs. 9-11).
Coherence between members of a tetrad is achieved
li\ fusion of short eoliiinella-like elements extend-
n,u from il loot I i',.-(- ..( adjacent ;>ol en plains

(Figs. 9-11). In a few places there are small breaks
in the foot layer in septal regions, which are
"plugged" by endexine in mature tetrads (Fig. 10).
Beneath the foot layer is an endexine that is consnlcrabU lliumer than the loot layer, except near
the aperture (Figs. 9, 12). In septal regime, it iapproximately one-third the thickness (0.1-0.2 ixm)
of the foot layer and even at low magnifications is
readily distinguishable by its greater electron den-
Pollen of Takhtajania perrieri
sity (Figs. 9-11). In extrasep il n g ms, ludii _

the annulus, it is ca. 0.2-0.3 pm in thickness, li
reaches a comparatively massive thickness of up to
3 (xm in the annulus region, and here it is made
;i|i > i <
>i
-- '
in I i
in nts more or less
tangentially aligned (Fig. 13). Near the external
fringes of the annulus and somewhat beyond this,
the endexine has an outer, more homogeneous pari
and an inner regi. i i i -i- \w <>i n. j il u J<>lui'.-Kirated by electron transparent spai es giving it a spongy appearance (Figs. 9, 12).
The intine, which underlies the endexine, is of
septal regions
similar thickness to the I.IVr
(0.05-0.2 jim) and ha
It is usually readily distinguishable from the endexine, even at low magnifications (Fig. 9), because
of its lower electron density. As Figure 12 illusll
'
ere it reaches up
to 1.8 p,m, and as commonly occurs in other Winteraceae (Praglowski, 1979) it loses its homogeneous appearance. There is a further increase in
thickness of the intine in the apertural papilla region to up to 2.4 pm, where the wall appears t<>
consist entirely of intine (Fig. 14). It can he seen
that in these thicker regions, outer parts of the intine have inclusions of a vesicular-like nature,
'' li is mimon i -n lai
g ms of many angio5
(Fig. 14).
Ills, ! >SIO\
It would seem that artifactual splits in the aperture in dried pollen, which had been obtained
from the type specimen, similar to that shown in
preserved pollen in Figure 5, led Straka i ! ><
1975) to describe the pollen of Takhtajania as colp,|. mil Minn-tune- ii, >i lorn .. olpate. Figure lc
in Straka (1963: 357) is a phototnicrograpl
a triradiate tear in the aperture membrane, which
is labeled as a "trichotomocolpate" aperture. Similarly, Lobreau-Callen (1977: 447) illustrated what
was termed a colpate (slit-shaped) aperture in a
photomicrograph (plate 1, fig. 4), which is very similar to the torn aperture shown in Figure 5 of the
present paper. Praglowski (1979: 19) also noted apertures were different from other Winteraceae in
their great variation in shape "ranging from pori to
cofpi." It is concluded, therefore, that previous reports of these varied types of apertures in Takhta
jania are incorrect, and that it resembles other
members <>l die lamiK u posses-dug round or some
what oval apertures. The study by Lob re an < .1 n
(1977) was the only previous one to illustrate pol r

ol 'lakhnsjiuiui mi.!, t SEM. and two ol In- i I lustra
tions (plate 2, figs. 1 and 4) do show a bulging
-i
I ii
i
I
i il
In I dial pollen
was obtained from dried herbarium material. It is
unfortunate that it has become well established in
the literature tha lukiu i; u, , \ n l< n is sometiim s
i I i i i < - i | a II
I II
) ite), but one can
I" I II
da I
i
sed on previous
vxo: ki : - ul e;i -! i . 11 g |.o en Iroiti a l\ pe specimen
collected in 1909. On the other hand, true trichotomocolpate apertures are well defined. For example, the reeentb dis, ... led gi mis \n<iroslia. a new
basal angiosperm from the early Cretaceous of
North America and Portugal, has some pollen
grains with cleat \ debit ilcd ami alttaclivels ori m ui. d ii id li!
olpale apertures (Friis el al..
1997).
The present investigation supports previous stud" dial /.,-',/'/ I;,I,\ i ha- iderabl- la ,-.. ; I. adthan other membi is oi lln i.imih HIUM' pull, n a ibeen examined. Endress et al. (2000 this issue)
suggested that the presence of these large tetrads
mas indicate poKploidv. as indicated tin some other Winteraceae by Hotchkiss (1955). Straka (1963)
stated that the acetolyzed pollen tetrads were 60
p,m in diameter; Lobreau-Callen (1977) noted their
mean diameter was 57.4 p,m, without citing the
range of sizes; and Praglowski (1979), who gave
mean and size range for the pollen ol most other
Winteraceae examined, gave a single size of 65 pm
l
diamctei lor tin
I
\
i i I
cause of the limited material available. The range
of tetrad size obtained in the current study (65-83
pin) extends the upp. i lime- ul hie - /.. i uigi . bui
no tetrads were found as small as those measured
by Straka (1963) and Lobreau-Callen (1977). The
mean (74 pm) is considerably higher than that given by Lobreau-Callen (1977). It should be empha-I/.I d lhal .i< IoK- - can increase the size of pollen
units by 30% or more, and the extent of the increase may depend on methods of acetoKsis used
(D. C. Mildenhall, pers. comm. 1999). In fact, tells ol 1
,
hnl -i
ell dried bs the
critical point method for SEM (Figs. 1, 2, 4, 5, 7)
had a diameter (excluding the apertural papillae)
averaging ea. 47 pm. It is highly probabh iha< die
tetrads of other Winteraceae undergo a similar increase in size with acetolysis. Thus, Pseud,> mh
colorata, which had tetrads with a mean diameter
of 50 pm following acetolysis (Praglowski, 1979),
measured ca. 35 pm under SEM, when material has
been dried by the critical point method (unpub
shed
Lobreau-Callen (1977) and Praglowski (1979)
made detailed comparisons between the pollen of

. 'i< I.I in the family. Lobreau-Callen (1977) concluded that based on its
structure and sculpture, its pollen is closest to that
of /;
in.
.
,mia can be dis;
i'i!'ii.i-'ii i !.-. i!i. .Id:. i< nee PI -i
:I.M|.I ih i ,
in the ml. in.il
in h are large in
I
..mid lor several

genera in the family that if these gaps are still open
at the time of poll, n grain miiosis and then lore lli.
loin members ol a tetrad share a common cytoplasm, division into tube and -en.-rah
I till
in each pollen grain is synchronous within a tetrad,
e.g., in Belliolum (Sampson, 1981). It is probable
thai pollen grain milosis is asyui in < o u
In
each tetrad ..I Tokhlojonio. because the small and
inlre<|iieiit gaps ill ill- eeii >.iu. I mi ug ill.
pjae
are plugged with endexine, which is formed before
. winch is formed subse1981), or large

gaps may remain open m n alme U leads, a- i I Ins
trated by Praglowski (1979) for Bubbia howeana (F.
Mi.el .1 fiegh Vssumnig llial InU.iojinud has ,ISM
chronous pollen mitosis, it shares this feature with
l\ni>tt>n;nirm and l>niii\s. Wnelnei or not this indicates a relationship between lliese three genera
depends on whether asynchronous mitosis, the
adaptive significance of which is not obvious, has
e\ol\ed independently in these ta\a. f'lll'liril ....
dns jeal in has 'ini been m\ e.-,| igaled ill all species
in the family, and future studies may demonstrate
that it is not consistent within a genus. For exampl. . although as\ n, I n now- d i-ion occurs in all
three species of Pseinlaicintent. onl\ one species of
Drimys has been examined (Sampson, 1981). It has
been suggested that the asynchronous type has
c\ob eii Iron hie s\ nehfoilni; , (Sail pson. ir'.M !.
In contrast to other Winteraceae, Drimys, Takhtajaniu, and Pseudowinte.ru share protuberant ap. ii i I lapdlai \< ii li ma\ ol ma\ not indicate a
relationship between the genera, depending on
vvhelln i <H not In
laraeteii
i I d i i
i
dently in these three genera. Bailey and Nast
(1943) noted that van Tieghem (1900), who studied
pollen of all genera (exchid
ili'- igh Ii. pro\ nled i o ilais:ia: on-, loin d d r d
pollen of the three New Wmld
he examined formed prolub. i: n; papd . wl --a
/. N'"./'/..i\
l\- I,>..,!,!;.I
/>',,<>/*.,
li.-'l,,>,,,'
I'.i
,:,;>, nnmn. and /u;?v: MIIIDI. I> iilc\ md \.is| ( P> Idl
..iifiini- d ihes. Hsu I-,. ! |,., u'l. fresh and pn
served pollen of all thw

have the papillae (Fig.
',.. possess ,m ,i
(Figs. 3, 8) with smaller
in contrast to tin m paiaiiu-K -mooitisartae. d
animli illustrated for species of Drinns (sens,1
Smith. l'Xi9) by Lobreau-Callen (1977) and Praglowski (1979). Tetrads of Pseudowintem differ from
dio-< o! /,/.,-'.,%,',,,,, a .. a. i lib I i. kn _ \; n ded
tips to their columellae where they touch the foot
layer and in possessing numerous small perfora(Fig. 8).
Praglowski (1979), while agreeing that Tukhtujuniu pollen differs considei.ob li nn I >: <>' IUti>
hid. the genus in wIn. h Tokhlujuniu perrieri had
first been placed (Capmoti. 1963). disagreed with
the conclusion of Lobreau-Callen (1977) that it was
closest to pollen of Belliolum. Praglowski (1979)
i
I the \ahie ol the ratio between the width
of muri and the diameter of bacula (columellae)
used by Lobreau-Callen (1977) for intergeneric
: in .n and concluded its pollen was closest to
I) irnys (syn. Drimys sect. Drimys) I obreatiCallen (1977) also had noted similarities between
.'.,",. i a \ l>
is pollen. Coetzee and Praglowski (1988) described two types of fossil \N intcaceae pollen resembling To
ii.ii tin Miocene ol S.tith \friea. This diseo\er\
and the Early Cretaceous occurrence of Winteraceae pollen in Israel (Walker et al., 1983) led them
to suggest that the Winteraceae had a West Gondw man .i igm and an arU iill. n nl ilioi:. j ss bb
in \lri.a. before migration to Australasia an M !
agascar. They suggested furthermore that a dispersal route from the south . .add p .! ibl
i
the close resemblance between the pollen of Tukli.
*
oild. Doyle et al.
(1990a) noted that extinct relatives of the Winter1
i
i important i aiiponent of
I'.arK Cretaceous tropical floras and extended into
teraceous affinity of Ajropolhs has. Iiourvn. been

ipiesiioned by briis et al. (1999).
I Itrastructural detail in pollen of the Winl.ia
ceae (e.g., intine and endexine structure, endexine
fine structure) does not seem
between genera (Praglowski. I(>7(). and unpublished pers. obs.). However, further studies are
needed to confirm this, utilizing freshly collected
pollen and TEM fixation techniques.
Table 1, which includes information from Praglowski (1979), the present study, and un; nl isa. i
H^
1 1*1.
is.
7 7' - 7
.':
|
| 1^
I
"1
~
H i
.
|
|
y.
lllllllf
iliJiiiiiiKiilii
It'll characters of the genera. Assuming that !

or all similar characters arc not the result of
vergent evolution, the pollen
closely resembles that <>l l\<-u,imt intrru
mys. Endress et al. (2000) reached somewhat different conclusions when considering the
dence of floral features and considered III.H
l',ll !<!l,,IT.n III- |iev| in !; I\.;i<!nn ,>! 1,1 /.,:':
!\,>iti UN Indue. IL,''>:",i !..''',"':,n, and />.,>/>. <
mum) clade, "which is sister to the Tasm.n,>,,,/!),
mys clade." Ili>|
1 provide further
i Takhtajai
other \\ inleraeeae.
Ha,lev. I. VV. & C. G. Nasi. I<

lid -lai:,c i
Arnold Arhor. 24: 340-340.
Campo, M. Van & Ph. Guinet. 1961. Les pol
posees.l.'evemple de- \1 imnxac-cos. Pollen
200-218.
Capuron. R. 1963. Presence a Madagascar d'ui
<les \\ min:ir,v>.
. \. X .1. Praglow
'; ;. \ , .
c<l|
/nmnoeolpat, poll,,, (.,,, \U 225 211

, K. R. Pederscn & I'. K. Crane. I9<M>. |.l\ an
giospenn diversification: The diversity of pollen associated with angiosperm reproductive structures in Karly
Cretaceous floras from Portugal. Ann. Missouri Bot.
Card. 86: 259-296.
"..
Proc. Linn. Soc. New
Lohreau-Callen. 1). 1977. I.e pollen du /,'

R. Cap. Rapports palvnologiques avec les autres genres
de W interacees. Adansonia. n.s. 2, 16: 445^60.
Praglnu-ki. .1 1979. \\ mlcaeeae. Pp. 1-38 in S. Nilsson
(editor). World Pollen and Spore Mora 8. Ahnqvist &
\\iks< II. Stockholm.
Sampson. F. 8. 1974. \ new pollen Ivpe in the Winteraeeae. Grana 14: 11-15.
within permanent pollen tetrads of the Winteraceae.
Grana 20: 19-23.
Sehatz. G., P. P. Lowrv II &
1998. Takhlajania /><
IX, 133-134.
Smith. \. C. 1943. The \i,,,.-an specie ,,f Drums. J.
Arnold \rhor. 24: 1-33.
. 1969. A reconsideration of the genus /.;.:.- :r,m.i
i \\ inleraeeae). Taxon 18: 286-290.
Slraka. II P'C.l. f |,e, die miiglielie plivlogerielische Bedeutung der Pollen Morphologic der tnadagassischen
Bubbia perrieri R. Cap. (Winteraceae). Grana Palynol.
Ta\oi,om\. morphology, and

Bot. 77: 1544-1557.
,<l i.r:, i..
. 77: 1558-
Tirendorfer, K, I. Silherbauer-Gottsherger & C. Gottsherger. 1979. Variation on the population, racial and spe;rica. PI. Syst. Evol
132: 53-83.
Kndress. P.
1)14:259-297.330-361.
ink. W. 197(1. The Winteraceae of the Old World. I.
Pseudouintera and Drums Morphology and taxonomy.
Blumea 18: 225-354.
. 1985. The Winteraceae of the Old World \ / \ospermum links Bubbia to Xygogynum. Blumea 31: 39.In: P. Moral K U.S. Maekee
Flore de la Nouvelle-Caledonie 19: 90-171.
Naii.Mi.il .111 i-i,
\atuivlle, Paris.
/..C.J. Brenner K A. (,. Walker. 1983. Win-
I "'';
EMBRYOLOGY OF
TAKHTAJANIA
(WINTERACEAE) AND A
SUMMARY STATEMENT OF
EMBRYOLOGICAL FEATURES
FOR THE FAMILY1
p present the first report on the embryology of la
Hiroshi Tobe2 and Bruce Sampson"
I!
id lm- il> data to those already known fr
ly to evaluate the pio .-. . I i- I |><

i , i ,1 '
,
<,ui in the family and a possible sister-group ivh
eeti Winleraeeae and (ianellaeeae. which were reeeiilb suggested by molecular evidence. Con1p.111-.u11- w
een the famihe-. -ho
. - w. II with other Winteraceae embrvologu alK basing ti<
res to support its basal position in the family. Although Winleraeeae and Catiellaeeae share a number
yological features, including an exotestal seed coal. Winleraeeae are clearly distinct by virtue of the
res: the outermost one of the middle la\eis and even pari ol the connective tissue in the anther developm
tegument alone I rather than by two mli guments as in (land laccae): an exoslomc formed a
tcropylar part of the tegmen composed of variousb cnlaigcd. thick walled cells: and the
eae are thus a well-, iiued
I
I1 n
le-pite their modern widesprea
lie diversification in embryological characters.
The Winteraceae are a relatively small wood) di

cotyledonous family. c< m; in n,
i. m <,. species
assigned to Dnm*
>
Tasmannia, and Zygogynum sensu lato (including
Belliolum, Bubbia, and Exospermum). They are
broadly distributed from the Philippines to Tasmania and New Zealand, South and Central America, and Madagascar (Vink, 1993). Because of its
relict Gondwanan distribution as well as its (listinctive primitive-type floral morphologies, the fain
ily has long attract- '
. IVMMM IK IS
of plant evolution and morphology. Within the fam xtant species
T. perrieri (Capuron) Baranova & J.-F. Leroy in the
Africa/Madagascar region, has been considered
most isolated, and in fact it differs from the three
other genera in having flowers with two carpels
united to a paracarpous gynoecium, instead of free
carpels or a numb*
i| Is i
carpous gynoecium. Takhtajania thus has been
placed in a subfamily of its own, Takhtajanioideae,
and the other genera in another subfamily \\ interoideae (Leroy, 1978; Takhtajan, 1997).
Takktajania has been very poorly understood m

general with respect to its morphological and e\o
lutionaty traits because only a single collection
made in 1909 had been available for research until
recent times (Leroy, 1980). A number of trees were,
however, rediscovered at the Anjahanaribe-Snd
Special Reserve (1445'S, 4929'E) in Madagascar
in 1994 (see Schatz et al., 1998; Schatz, 2000 this
issue). An extensive collection was subsequently
made lot motph .
I
u omical. ovlologioal.
and molecular studies (for many results, see other
articles in this Annals issue).
In this paper we present the embryology of Tal.htajania, which has not been studied before. Taking
the data from this study togethei with those from
the four other genera (Drimys, Pseudowintera, Tasniannia. and Z\g(>i>\mim s.l.i. which have already
been studied relatively well, we will summarize cmcal features of the whole family \\ ml. i i
ceae. Molecular evidence based on combined sequence data from mitochondrial atpl and matR,
plastid atpB and rbcL, and nuclear 18S rDNA has
revealed that Winteraceae are sister to Canellaceae
'We are grateful to Porter P. Lowry II and George K. Sehat/ lor then efforts to colled the materials used in this
study, and to Peter H. Raven for hi- siippoil and iwiiit.mi menl to complete this Miidv.
Department of Botany, Graduate School of Science, ku.io I nne.silv. Kyoto 60(1-8502, Japan.
'School of Biological Science Victoria I iioersitv ol Wellmgto,,. P.O. B..\ 600. Wellington, New Zealand.
37: 389-397. 2000.
with support of 101
due, and that

iiliin the Winteraceae (Qiu et al., 1999). We will discuss whether
or not the sistcr-g
i
teraceae and Canellaceae is supported, whether or
not the basal position of Takhtajania in Winteraceae is supported, and lieu W interaeeae are a eoherent group distiii.
rem tli.<
i I n-eae
shape of resull
elrahedral. Unfortunately, no buds could be sectioned that would have
showed stages in the division of the 1-celled mi
uilion of vegetative
(tube) and generative cells. Two different l\pes of
division have been found. In the synchronous type,
vvhicli occurs -.
,.1 Zygogynum S.I.,
the inn lei ol all lour pollen grains within a tetrad
MATERIALS AND METHODS
because there are cytoplasmic connections through
Flower buds and fruits of Takhtajania perrieri in

various stages of development were collected at the
",
^^^
A"jal.;.nanb.-N,d (vouchers: Raknlnm
asynchronous
,1 li. -.
,.,\l
s
ea.
'.;.
Ravelonanvo s.n. in 1998; all at MO) and fixed with

FAA (five parts stock formalin; five parts glacial
acetic acid; 90 parts 50% ethanol). Twenty-eight
flower buds, four open flowers, and 17 fruits were
dehydrated through a /-butyl alcohol series, embedded in Paraplast (melting point 57-58C), and
sectioned using a rotary microtome following standard paraffin methods. Sections cut at about 6-10
u,m thickness were stained with Heidenhain's haematoxylin, Safranin-O, and FastGreen FCF, and
. ] r . 11
T>
r
mounted with kntell.m. 1 . . vaniin.- iL
their fine struc-
,;|, ,
division
^^ ^
19gl.
of
the
/)Jr, and fteunuclei is
microspore
because there are no gaps in the inM(.h ^j a{ ^ (jme (Samps()n<
Q{
prakash
et
1992)
It has been suggested
that the asynchronous type
has evolved from the
synchronous, and in view of the basal position of

TakhtaJanm
it
would
therefore be of interest to
know if u tQO ha the synchronous type of pollen

mitosis
/p-
pollen
^\
grains are 2.celled
at the time of shedding
OYU.ES, M CEI.I I S. VM; \!l ;. \(.\\ll l(i 1!'- I
ture, several anthers were embedded in Spurr's resin after dehydration through an acetone series and
long
sectioned with glass knives using an ultramicro-
(Figs 1 2'Si
tome. Sections cut at about 1-2 u.m thickness were
They ar'e anatropous at
stained with Toluidine blue 0.
sinucellate. The archesporium is 1-celled (Fig. 10).
OBSERVATIONS
The archesporial cell divides periclinally to form

the primary parietal cell above and the primary
ANTHERS AND MICROSPORES

The small anther is supported by a more or less
laminar lilaun nl (lig I), ai
(Figs. 2, 3). Prior to m aturation the anther comprises 5 to 6 cell-layers: ai . [iideimis. an . rid..die
cium, 2 to 3 middle layers, and a tapetum (Fig. 7).
Because of the lack of younger flower buds, it is
not certain how the anth er wall developed. The tapetum is glandular, am I its cells are 2-nucleate
(Fig. 4). During maturati on. the pulermal cells ate
enlarged to some extent but nearlv collapsed even
tually, and the endotheci urn develops fibrous ! i . -.
enings (Figs. 8, 9). The middle layers mostly degenerate, but like the ei idolhe. nun. the outermost
lavei usuallv develop- libioiis thicki nings ;f'igs. 11.
9). Part of the connectiv e tissue may also) develop
lihrniis ihii k<-nmgs (fi;y. 8). Anther dehiscence
takes place by longitudinal slits, with each slit
theca (Fig. 9).
Meiosis in the mi rospore uiotl
I
, ,
panied by simultaneous cytokinesis (Fig. 5). The
arly in develonment six to seven ovules with a

fumde
maturity (Fig. 15) and eras-
sporogenous cell below (Fig. 11). While the primary

parietal cell In !
ili l<
.< iiclinally into more
cells, the primary sporogenous cell develops into a
I I has ovules have one enlarged megas|
.-II below a longitudinal
row of five to si\ parietal cells I hi
i< i- n
mothei cell undergoes meic-sjs lo piodnee a lineal
tetrad of megaspores (Fig. 12). In t
tetrad the chalazal megaspore fund
and develops successively into a 2-, 4- (Fig. 13),
i.l
nucleate embryo sac. Thus the mode of the
ritlllivn -ac ! velopn nl [- el the I'. \go| Iln \\ p<
\M 1 igai \/> il "nl.".'! -,.). I is . <ilil nuclei in seven
cells: an egg cell. i>. s\ n,-ignis, two polai nuclei.
and three antipodal cells (Fig. 14). The i _ i ,. I
enibrvo sac is . lipoid in >hapc and positioin d al
the i
(tug. 15) The anlegenerate before or soon after fertilization
(Fig. 14).
During m< u
is. sunn
pulermal .< Is i the nucellus <hvide periclinally to form a 2-eell layered nucellar
Figures 1-9. Dev< p

I 1 mthei
il aicrospoi
in Takhta
l
i lin.il
, lion (I of flower
howing a small anther. 2. Transverse section (IS) ..I Mower showing dehiscing anthers. 3. TS of anther. 4. TS
ytokinesis. 6. Microtome sections of 2-celled mature pollen grain* in tetrad.
7. Micr me sect ion of young anther
howing wall structure. 8. TS of older anther showing that fibrous thickenings develop in the outermost one of middle
lyers and even in part of the connective tissue as well as in the endothecium. 9. Microtome section of dehiscing
nllicr. \l.l>re\ialioiis: an. antlier: <(.. connccti\e tissue: end. endollieeium: ep. epidermis; me. microspore mother cell:
!m in' Figs. 4-7!
ule. 17. LS of mature owile showing Ihr rniempylar pari.

18. I ,S of mature ovule showing the thiekuess .if
eguments. Ahhreualions: .ml. antipodal cell; arc arehesporial <-e|l: dm. degenerating megaspore; es. embryo sac-;
. f"iim lioiial megaspore; ii. inner integument; mi, mieropyle; mme, megaspore mother eell; n. mielen-. ol rmbno sic;
in f,g. 18. 1(H)! n, ,,, !
, I!..
id !.)
I.M
ligs. !0-'l4.'
Volume 87, Number 3
Fig. 22, 200 (xm in Figs.
[l:,,,M-,j
Collaf)se()
Crushed except fibrous

outer cell-layer
Cnished except fibrous

outer cell-layer
dipn.l.il cll.cellar cap
1 ccll-LmTcl
i ccll-Lucrcl
cell-lavered
cell-lavered
2(-M
2i-:ii
:i(-4)
;ii-U
cellcellccll.ell-
(Drums winteri)
walled;
IVrsisl.nl. iln, k-wal
No (except Cinnamosmaf
1 \ot< sldl
4-6 cell-layers thick
Uglified, palisadal
(1968), Corner (1976),

De Boer & Bouman
(1974), Prakash et al.
(1992), Sampson
longitudinal MIIK.II ol an oviil. l

m I ngl (Paiameswaran, 1962, fig. 25 on p. I ,3) -uggrsls tliat
the ovule is campylotropous rather than anatropous.
' Wording In Corner (1976: B6). the description ol Paramedian I I'W.l I suggests lh.it the large seed of G7HHWNW
\ceonling to ( orner (1976 K6|
Baillnn .1. s, n!
v. -n il ml round the hilum of Canella, but later authors
4
According to Parameswaran (19611. Cimmmasma \< . maerocarpa and C. madagascariensis) has ruminate processes
in seed coats, which are not known in Canella >
mil
, <>,.<
iml Warlmrgia
-Based on earlier observations. Corner (1976: 6) noted thai the exotc-ta is composed ol' sclerosed cells (except
Ciniiamosmal am ill i i <
I ||
i c\otcstal. The structure of the seed coat of Canellaceae has been studied very
poorly, and m
I i ill 1 . < ih
I coal is needed for critical comparison.
' flic following la-. < I. b. 11 -mh I loi some or part of the embryologies] characters of the genera of Wi nl eraceae
other than l,ikht,i,a>
>." iB I Bnitll \ < Niiilli M ornei 1976). Dunns {Tasmaiuua) piperita
Hook. f. (Corner. 1976). D. uinteri iBI
I
191.!'.: I I, lioei K Bouman. 1 67 1). I'semlouintera eolorata
(Baoul) Dandv (Bhandari. 1963; Corner. 1976). I>. axillaris (J. K. foist. X (,. forsl.) Dandv (Sampson. 196.3). three
species of Tasnutnnia
li
n bailloni Tiegh. (Swamy, 197,2). and /. stipilatum Baill. (syn.
Exospermum stipilatum) (Smissen, 1993). Unless otherwise stated, embryological lea In res presented above are common
'The presence of an obturalor is reported in all three species of Tasmannia studied hy Prakash et al. (1992) but is
1
\ccordmg lo ( ortKT (1976: 2!!2l in -.//,/,
concerned" in the formation of the mieropvle. Ho

sources a\ailable lor this character m \\ inlerceac i
cap. Cells of the nucellus remain around the mature

embryo sac (Fig. 15). An obuturator is formed near
the iiiicn>|>\ le (Fig. 15). \ hypostase is not formed.
INTEGUMENTS
The mule is bitegmic
outer integument (I ,
ri:u ing an inner an

> IK) N iher the mncr
nor outer integument arc- multiplicative. The inner

integument is .3-. . I li.. -J ibis.:. 18) from the beginning to older stages of development except at
the apical part where it is about 5- to 7-cell-layers
thick (Fig. 15). Some cells of the inner epidermis
of the inner integument may, however, divide in
places to increase the thickness, so that the inner
integument is 4-cell-layered in places. The outer
integument is 4- to 5-cell-layered from the beginning to older stages of ovules (Fig. 18).
By the fertilization stage the inner integument
always develops beyond the outer integument to
cover the tip of the nucellus, so that the micropyle

is formed 1>\ the inner integument alone (Figs. 15,
17). However, after fertilization, the tesla (developed outer iutegi n i il
1 p.s further and reachc> ,
. .
loped inner integument) (Figs. 19, 20). Therefore, when looked .t in
feeds. *e micropyle appears to have been formed
b
> 1>",,' ""'
in,
*r ;"1'1
,ht
"
ou,, r
" "*K'-
F.NDOSPKRM AND EMBRYO

Fertilization is porogamous. Endosperm formation ab initio is of the Cellular type. No free endosperm nuclei have been observed in young seeds,
Compared to the whole size of the nucellus, which
is enlarged after fertilization, the embryo sac composed of cellular endosperm is small and narrow
(Figs. 20, 21). In nearly mature or the oldest seeds
available, the endosperm is positioned in the center
of the seed and is surrounded by a massive nucellai

tissue, which appears to be degenerating (Fig. 19).
We did not examine embryogenesis in detail in
this study, but fragmentary observations of early
and late embryogei
i J
n
nnrnialh to foim a I lui i
il
'|
I) h |fi
nearly mature or oldest seed- available, we could
not observe a dicotyledonous embryo. The seeds
seem to be released from a fruit before the globular
embryo develops into a dicotyledonous stage.
' ' i
md t rassinueellate;
arehespoi nun I < >'lied; parietal tissue 5-6 cells
thick, tetrads of megaspores linear or T-shaped;
mode of embryo sac formation of the Polygonum
t
I
'
I he mature embryo
. IM-H
I.
fi I.
I 11
ilpp. l legion o| ail
enlarged nucellus; 2-cell-layered nucellar cap
lm
I
ihaled: an obturator
formed; ovule or seed not pachvchala/al: inner integument 3(-A) cells thick, and outer integument
I ") cells lliiek: both integuments not im.h
a
..
,
.
IT
i
.
i
\. a I\ 'ii ilii...' -o ,1- ai. . lupoid ml -omevvhat
i /r,A
-i
i
i
angular (Figs. 19, 22) without any appendages such
as an aril or a wing. The seed coat is formed by
belli 11
i in lhe |
I i'. . 11 the tegmen and
endothelium not formed; micropvlc formed

.
A I
uuiei n i:.. 111- ' n i 11,.- le. I nit covered by an
^ ^ ^T^^,,
tili/atioii. The legmen is 3- |o f-i ell-la\ers thick.

andth. .eslais I
,
>,
As the seed dcvel, .
K
,
i-ii
i i o '
elongate to issiin
I
I i
1 '
- II I
i
i lh' n
the
endotesla are rectatuiil ii i -> ip. md launmifer
ous (Figs. 25-27). On the other hand, none of the
cell Livers ol the legmen exhibit ati\ particular spe lali/ai on and piob ib \ d. g.en.-tate n collapse ex
eepl at the niicropvlai part. Cells of the micropylar
part of the legmen are variously enlarged and thickwalled to form a persistent cap-like struct i:. (big.
20). The seed coat is thus exotestal (for terminology
of seed coal types, see Corner, 1()7(>: Sehniid.
1986).
iii
Fertilization porogamous; endosperm formation

of ab initio Cellular type; mode of einbrvogcm of
me.I |\pe (III Drinns icintrri J. H.
0
h
^ * (' , "^\> '"
'
<
"
* "% fma" ^'' ^ ' -otestal havmg
'"'- <<' hrm the most
-.,.,
,.
r
specialize,! mechanic il ,|iuel n. ; c< I ol mesoleski
'
...
.
III.
based c
Canellace;
eeae in general, including having an exotestal seed
coat (Table 1). Based on the presence of lignified
exotestal cells (except in Cinnamosma), Corner
I I
'
ie seeds ol ( anella< ( ae ap-
In Table lembiv I
are summarized in comparison with those of the
other Winteraceae as well as of the Canellaceae.
bmbnnlogiealh 'IhL'nhijaiiKi agrees u,-|l with the
four other geneia
Drinns. Psvu(louuilcHi. Tdsnnunna. ami /, \r>._;,num s.l.). No
ters suggest the distinctness of
the other Winteraceae and its
basal position i i
I1
features of the fan11
i
<l as follows.
Anther letraspoiangiate: anllici wall develop
ment of the Basic type (unknown in Takhtajania);
the anther epidermis becomes collapsed; the endothecium, the outermost cell-layer of the middle
layers, and occasionally part of the connective Issue
I
I i i I I . i lli keriin
i i i i I I 111 I i I
degeiieratiug. and ip<
du i
ip.-tal
I
leiacea, In addition, according to llubc (pers.

eomm. in Kubitzki, 1993), seeds of Canella alba
Nees are exotestal, with a collapsed tegmen and
nucel his. abuin lai ii and I Inn u. died endosperm free
of starch, and a small and slender embryo, and they
agree with those of Winteraceae laud Illiciales).
However, information on the seed coat structure of
Canellaceae is still exlremelv limited for critical
h tin s< < d coat structure of
several species of Canella and Cinnnnwsma has
been brii-iiv siimniai i/<-<| |( ]ai ner, I <>7<)). its dev elopment has never been documented. Therefore the
exact structure of any species of the Canellaceae is
not clear enough to verify how the seed coat structun- of the Winteraceae resembles or is different
III"

lai 11ies share exactIv dislinct seed
the prcilominaut shape ol microspore tetrads leirahedral; mature pollen grains 2-celled.
perales sensu lain (Oiu el a!.. 19<)<)). Canellaceae

need further detailed studies ol these features.
Despite the lii. '

i hie for the Canell,i eae. the uhnle lain l\ \\ nlenieea- I- eh al |\ .:ntinct from it, and all the five genera of the family
share a few characteristic features that are not
found in Canella
. in Winteraceae
film u~ In.4 i u; - cur in the outermost one of
the middle layers (and occasionally even in part of
the connective tissue) as well as in the endotheeium, while they occur only in the endolheeian m
Canellaeeae; the micropyle is formed by the inner
integument alone in \\ mlera. <;[<". bill
s f ; ni< <: h\
, Canella is formed after fertilization in

at by the fertilization stage as in
Canellaeeae; ovules are anatropous in Winteraceae
systematic posili,,,, in Winteraceae. Ann. Missouri

Card. 87: 347-365.
Johri, B. M., K. B. Ambegaokar & P. S. Srivastava.
(..imparativc
Kuhit/U K.
Fmln y olog\
I<^',.
ol
Angiospernis.
( .inclhicce. Pp. 200-203 in K.
bitzki et al. (editors), The Families and Genera of

cular Plants, Vol. 2. Springer-Verlag, Berlin.
Leroy. J.-F.
1978.
Une sous-famille monotypique de ^
teraceae endemiqiie a
1980.
Madagascar: Takhlajanioic
Nouvelles remarques snr le genre Tak
tajania (Winteraeeae-Takhtajanioideae). Adansonia 2

9-20.
\clolii/k\. F
I92(..
\naloiiiicder \iiginspermernSame
K. I.inshaner llandhneh der Pflanzenanatomie Vol. 1

Cebriider Borntraeger, Berlin.
Parameswaran, N.
1961. Ruminate endosperm in the C
rr. Sci. 30: 344-345.

hut < ani|>\ loini|o
teraceae have a
in I ",:i .-I
persistent
i.- ae: -eels of \\ in-
will) :: cells, ulm !i is
Floral
morphology
and
embryology
mieropylar part of the
tegmen composed of variously enlarged, tliiek
55: 167-182.
not < ;>ni|od in ( ianel la. < ae:
the exotesta is p.
L9
. I.. I.nn c
,mannia
<! b\ radially en-
(Winteraceae)
Austral. J. Bot. 40: 877-885.

larged, lignilied exole.slal .< lis m Winteraceae I.ill
not palisadal in Canellaeeae. These distinctly em

h . dogi MI l< it
-i |
i In coherence of the
Wmteia. <
i-
iii.li.dih_
hi) l.i<h-,'i, i
ii d
n.hi
Qiu, Y.-L, J. Lee, F. Bernasconi Quadroni, D. E. Soil is

P. S. Soltis. M. Zanis, E. A. Zi
nlaiiiei.
M.
W.
Chase.
elear genomes. Nature 402:

Sampson. F B.
]0(,3.
The earliest
angio-
KM- 107.
The floral morphology ,.l Psemlnn
intern: The New Zealand member of vesselless Winteraceae. Phvtomorphology 13: 402^-23.
within
permanent
pollen
Grana 20: 19-23.

. G. K.
The ,
denne:
tetrads of
the
Winteraceae.
Tukhta,,na prrrwri (\\ inleracea
souri Bot. Card. 87: 297-302.

. P. P. Lowry II & A. Ramisamihanti
wana. and their d< -> enderiis niigrated from there lo
the southern temperate zone and eventual I>
IW.
il
the distinctness of the Winteraceae from the Canellaeeae.

As discussed above, there is no emhi
evidence to disli .
nin from the remainder of the family. In other words, Winteraceae
are a well-defined group embryologically. Ancestral
Winteraceae date back to the lianeinian stage ol
the Early Cretaceous in tropical Northern Gond-
rediscovered.
Natu
to tin
current distribution areas (Doyle, 2000 this issue).

Ilovve
^ family I
sified
seiiini.l. I,'.
ical
\<)l\(>.
On Cornelian and oilier
perspective and
lerminologieal
Faxon 35: 476-491.

Smissen. R.
1993.
Some aspects of the embryology, morum stipitalum. U.S.

i of Wellington, New
I'.li.ihlm
l-io-
nh
<
- I i
..
I. II
iwamy. B. G. L.
.
i
hide,
303-316.
& R. Venkataraman.
l<Wi.
Fmbrvol,,,..
10'7.
Nail
Inst
Diyershy a.,,1 I .lassili. at
Sci.
I leu
ering Plants. Columbia Univ. Press, New York.
I'.'To. The Seed- ol Dicotyledons. 2 vols.
Some aspects in the embryology
18:309-406.
akhtajan. A.
.,1 lh
mys winteri. J. Arnold Arbor. 49: 509-524.

Corner. K. J. M.
1052.
of' Zu>of!U><im bailioni V. Tiegh. IVoc.
( ambridge.
ink.
W.
1070.
The Winteraceae of the Old
World
I.
Pscudawintera and DrumsMorphology and taxonomy.

Blumea 18: 225-354.
in the Polycarpi. ae
III
Drinns u inliri I W inlera. ci.
Doyle, J. A.
II II
2000.
Insiorv
Schatz.
I'
h...
2000.
A.
Morphology and taxonomy. Blumea 23: 219-
Paleobotany, relationships, and ,-<.

of Winteraceae.
Ann.
Missouri
Hot.
Card. 87: 303-316.

Kndress.
1977. The \\ ,,,teraceae ol the ( >!d World _, A _
<>lism,m
Acta Bot. Neerl. 23: 19-27.
Igeisheim.
H.
.Sampson vV
(;.
K.
Floral structure of Takhtajania and its
1993. Winteraceae. Pp. (.30-638 , K. KuhiiAi.
NOTES ON THE VASCULAR

ANATOMY OF THE FRUIT OF
TAKHTAJANIA
(WINTERACEAE) AND ITS
INTERPRETATION1
I tin- vascular skeleton of the Takhtajania gynoecium tlid not alter fundamental!), hut there i:
eviouslv recognized in Annonaeeae and Magnoliaceae. Lack of sclerificalion (only some pillis trait is correlated with wider mor|.hogenHi< potentialities: sviicaipv and likely dehiseene
About 20 yeai
i
![<!i.
i .
i
i aipuron) Baranova & J.-F. Leroy from Madagascar (Leroy, 1977,
1978, 1980; Vink, 1978) catalyzed a phase of research and analysis
1 ulion of the
gynoecium of Winleraceae ;ui.! ol Magnoliales in
general. More recently, Leroy (1993) presented a
brief synthesis ol tin debate n-sullmu Imm lliis discovciy. which was all the more interesting; since the
information available at the time gave him even
reason to believe thai tile v..-nils 1,i!,h 1 >t;,in!,t was
extinct. However, after considerable effort, Malagasy Ion sti is and llu ir col
o
1
'1
soiin botanical Uuden found living plants of T.
perrieri in 1997, and thereby made il possible to
undertake a -Indv ol the vascular anatomy of the
fruits o( this species. The results presented here
thus represent an unexpected continuation of an
earlier study ol die gvnoe. i.ai >l llus plai - | 1, ,, tl
& Leroy, 1993).
MATERIALS AND METHODS
The fruits examined in this study were collected

by C. Birkinshaw (483, MO) in the AnjariaharibeSud reserve. They were fixed in the field in KAA
and then transferred in the lab to a glvi i n i In i
nol: water solution for storage. One fruit was dehydrated using tertiary butanol and embedded in
paraffin duelling poml
(>0'< d as Mg stand,ml pn>-
eedu res (Gerlach, 1984

transverse sections, which were stj
ly with 0.5% aqueous Astrablue and 10% Ziehl's
fuchsin, and then dehydrated using acetone and
mounted in Eukitt.
A similar protocol was used for an older flower
from the type material (Perrier de la Bdthie 10158,
Plall. : i si, u.il ioi h-i'ii I"'.- a.picous ammonia.
postfixation in FAA, and the preparation of 8 pm
sections (Heroin K l.eroy. I <><).'{). ( a.mparison of tlic
material from these two sources was thus, faciliial
;M) I'M. logtaphs ,\ci, p ( an ;i i.sing a Zeiss pholornii [..scope ,., ah ;,,
.mvy lilh i and lllnrd Pan K
Plus 50 ASA film.
OBSERVATIONS
The material available contained only the later

i igi - i liuil development (Fig. 1). The series ,,f
fruits showed that: (1) no growth, either m length
oi thickness, occurs outside the gynoecium: (2) a
basal stipe(s) observed in the fruit must have
formed during an earlier stage, as little if any further elongation can be seen in the late series studied here, and the stipe is not vet diflerciitiuied ai
anthesis (Vink, 1978), although its vascularization
can already be detected (Deroin & Leroy, 1993);
(3) the ovarv locale (1) does, however. grov> . oi sid
crank, and - ;h\ mm.-!: i. ill in ihe plane of the two
carpels, one of win. Ii < long ih s r ore ;han llu oilier.
1
I express my gratitude to Pete Powry (MO) for his Kngli> h translation of 1 he original dial 1. Maun 1 'rame (Montpellier.
France) for her kind help in literature and discussions, as well as the anonymous reviewer lor Ins careful eorreel s
lahoialouc de I'luiicroga,inc. \h,s,um National d'Histoire Naturelle, 16, me Huffon. P-75005 Paris, franc,-, deroin@mnhn.fr
87: 398-406. 2000.
5 mm
flower (Fig. 2). The highly elliptic stele, with 15

vascular strands (Fig. 2 V). gives use to 2 median
sepals (Fig. 2B, C), and then their lateral bundles
(Fig. 2D-G). The stele, which then becomes circnl.ii MiA hn i : I v iii'-iluli iiin . n.s-, s,, , 'i<i ;| u
2H), gives rise farther up (Fig. 21, J) to all of the
27 in all). The histological changes that take place
unification of the
xylem (vessels -
I is in) and formation ii i i i)i III i i III il III ita at the level of
the corolla and the androecium. No secondary phloAt the extreme base of the stipe (Fig. 2K) the
gynoecium appears to lack cork, and the stele divides (Fig. 2l,-<>) in connection with the dorsal sutures of the carpels. Higher in the stipe (Fig. 2PS) the stele condenses in the plane of the sutures.
forming two symmetrical lines of bundles. Two di\id<
'in ui ir|M I.
undl.-s can thus be recognized, as often seen in Winteraceae, which are
fused to the niei i n-la i
In dies to form meli
I
I11.
i synlateral bundles
ill, v. I nli are relatively narrower at this l.\cl. Ilie

stele then becomes more complex (Fig. 2T) b\ giving rise to meridian-lateral traces, whereas the -utures extend far to the interior by a well-differenii.ilcd < pidermis (i :. !(!I The center is obliterated
by large-celled parenchyma. although al anthesithis level is hollow (Deroin & Leroy, 1993, figs. 1,
3).
At the base of the locule in the fruit (Fig. _'( )
the lateral and m< -1 n lain il ..!- I,|,I i/.ilioti- .i
much more de\<
complexes, whereas the inverse is true at authesis.
Up to the mid-level of the locule, these divided
dian-lateral bundles (1, 2,
whereas the lateral carpellary
separate (Fig. 3A-E, 11, and
Fruit dehiscence proceeds
and 3, Fig. 3A-C),

bundles are generally
12).
from the top down as
erals or next to the synlateral. No specialized tissues can be seen at this level (Fig. 4F). The vascularization at the top of the fruit is formally
identical to that observed in the ovary (Fig. 5A, C,
5B, D). It should be nc

comprised only of the m
2 of carpel 2. The medial
PHP) (ft )( a
I'ifiliu 2
Wn .1
ynlatrral; I. 1', 2. 2'. median I;
Fruit Vascular Anatomy
Volume 87, Number 3
in the wall, and the placental bundles fuse back

with the median bundles to form vascular arcs al
and a2 (Figs. 31, J. 5F). Tin- vascularization conli
h-appears along
with the latter.
I I
uioecium that
take place from anthesis to formation of fruit appear
to be minor. The ovary wall (Fig. 4E) shows a rather
ordinary slructurc al m .! height: a thin epidermis
that is highly luchsiu la in.!. ! reugh(tut the locule and covered with a fairly thick hypodermis that
is almost palisadal in places: and lacunar parenchyma ca. 15 < ell!
i
stainable secretory cells as well as cells with calcium oxylate cr\The vascular bundles are surrounded by a crown
of highly fuehsiu-slainable cells and are largely
comprised of met.i
hloem that are
separated bv 3 to 5 layers of eambial cells. The
protoxylem is crushed and the protophloem is
transformed into selenlied libers with a lumen that
is sometimes narrow (Fig. 4A, B). No secondary
formations are present in the gynoecium.
At all levels the external epidermis clearly extends to the center of the divided medians (Fig. IC.
D).
DISCUSSION
On the basis of this studv. Ii\i impoilanl fcaluies
of the fruit of lakh
in
i1
identified:
(I) \\ interaceae appeal to be characterized in
general by floral vascularization that lacks a cortical system, and in w u a -ecotnian vas. ulai slructures are absent (Nast, 1944; Deroin & Frame,
1998). By contrast, lignification of the xylem anil
the appearance of phloem libers are dearly delayed
n
i
otii| i d I ii III I
I i
ospermum oi /vgofl>
M \ I
I
I "' .
in which differentiation o< eui- al anthesis. The total absence of s<-ler.-uchvma i T< i kh I ajania, especially in the fruit wall, appears to be unique within
the family, based on the work of Harvey (1982:
164). This type of unspecialized histology is also
found in the syncarpous gynoecia of AnnonaceaeMonodoroideae (Deroin, 1997), although at anthesis.
makes it easier to interpret the vascularization at

the base of the gynoecium and thus its morphology.
In the lower half of the gynoecium the stele divides
to form two closed steles (Fig. 2K-P), which in fact
clearly represent an incomplete fusion of the peltate bases of the two carpels. This peltation was not
visible at anthesis (l)em,n X Ferny. |<M>3) and <>nb

appears later in the dev<
whereas it is r;
i I
pi ib;ibl\ primitive
in other Win
I
Iner, 1965, 1966a,
1966b; Endress, 1994; Igersheim & Endress,
1997).
Several very small, isolated bundles are found in
lli< m hillai pao n
i i h 2()-P) of the fruit
llial are not vet present at anthesis, but which are
likely homologous with the basal plexus of the gynoecia in Annonaceae and even in Magnoliaceae
(Deroin, 1999). Higher up, the steles open once
i
in. hack around
the median complexes, which divide, as is generi \ interaceae.
(3) From a strictly vascular perspective, the syncarpy found in Takhtajania is not particularly advanced, as confirmed by the organization of the
stipe and (he i i a.
in. us. which arc often
disjointed (Fig. 2U, II', and 12'; Fig. 3E, II, and
12). In this respect tin situation is similar to that
found in \h>n,
nth. (Annonaceae)
(Deroin, 1997).
(4) Fruit dehiscence in the material studied is
initially difficult to interpret, as the splitting could
i aling action of the
fixative, which would account for the irregularity of
tn
e opening. Nevertheless, the simple fact that this
svnearpous membei ol VFignoliales has dehiscent
fruits. Moreover, the possible occurrence of delnseence in the met iearps of apocarpous \\ interaceae
is still poorly understood (Harvey, 1982: 167), and
was not report, i! lot is nc>ei- .1 ihe family in New
Caledonia (Vink, 1993).
Oti
i
dm
u of the epidermis
between the halves of the divided median bundles
.
is i
I I isceuct at this level, which
i ,
1
I
Ylagun|iacea< and
even some archaic Annonaceae such as Anaxagorea and Xyloput III. pieseticc of apical vascular
arcs (Fig. 31, J, al, and a2) linking the placental
zones, which are present in all Winteraceae studied
to date (Bailey & Nast, 1943; Nast, 1944; Ueda,
I".". II
. !* J
himys (Tucker & Gifford, 1964; Tucker, 1975; Doweld, 1996), does not,
however, favor dorsal dehiscence.
(5) The vascular rearrangements (lining fruit >\rvelnpMiem (big. <* cml in: ll X ih' nutritive role is
transferred from the median . arpellary bundle (A)
to the lateral bundles (B), a phenomenon that appears to be very generalized among Annonaceae
(Deroin, 1997) and Magnoliaceae (Deroin, 1999).
Tl
1.1 i i
_ t
n
I the meridian-lateral bundles of the first and second orders (Fig. (>.
1, 1', 2, 2'), whi

hen
i
in Urge part to
ih- iipical plaeenlal bund <> (bu>, <>. r.V, il;. I i
to a vascular pattern that is functionally comparable to that of the carpel in Ambavia gerrardii
ill.nil I r I liomas. ,i lalhei pnmr,-.. M I.IL-I-. \<\
nonaceae, in which the ovules are fed by the meridian-lateral traces (Deroin & Le Thomas, 1989).
In the case of Takhtajania (Fig. 6B). eight fun<
' otiiil mei ! n latcr;i Inn !l<
I lour per carpel)
feed the eight seeds, with an additional role being
played by the synlateral traces. The remaining four
til. i a,ii lateral traces, of the third order, most
likely represent the relictual vascularizations of
fom additional ovules. \\ Idle the < loseb ivhiled ve
nus Bubbia has an average of 12 ovules per carpel
(Uarvev. I(>!;_'- 111 . ih> -emi- /// l;iu;,c<. i ..; ;.. >
to have undergone a reduction in the number of
ovules (to 4 per carpel in the material studied),

perhaps following fusion of the carpels. This reduetion does not appear to have occurred in the
syncarps of Annonaceae-Monodoroidea< (Deroin.
1991), and instead a salts is m the distinctive pla nl 11, i il \\ nleiaeeae
Study of the fruit of Takhtajania shows that only

modest changes have taken place in the organization of the ovary, but that they are nevertheless very
instructive. The latent peltation of the carpels and
the formation of a very short stipe resemble the
{
, leaipell lie a pi ai ; ol.s g_\ I oe< iw>n o! I mix uisoi r,i
luzonensis A. Gray, a primitive Annonaceae (Deroin, 1988). and
arl\ appearance
f svnc.UpV .!> ill \l :mi:;|. < if Motlode-loidca. i [),

lively pen carpel structure. Tin- vaseul u :
. i
fie seed- shows .1 ii. ! r. :! |.ci.-ii wbi< ' j .iialh -
tern very near that of Bubbia, a rather few-carpelled

and thus archaic genus (1 to 11 carpels after Harvey, 1982: 148). In these two g.-nera the dehiscence
was at lirst dorsal, as dciiKnislrati'd l)\ the opi.lerin,il dilh-rentiation at the median trace level, the
ventral dehiscence being restored in '/.V.''</,//,//,.',,
because ol the imperfection in vascular syncarpy.
vv lli a dchis, em Tiii-., ao\\e\< i. I;ISI inll.r s\ nearpv
is yet more ad\ai
d .u /
l.aa ai 1/
sometimes even with an ultimate reduction and disappearance ol synlaleral traces (Deroin, l(>()7).
When consul< ring the cniitii n n Iron
1
i,
to the fruit, this morphological and functional convergence among < ,ou.lw nai \1 gaolial.- i j > | * iri . Inv.liliglil i-i< ii si an-il tlispi i -ill s\ iido n . ikeb
aearpv. Compt. H.
31(.: 727) 72".
olutive potentialiti
. Compt. Rend. Acad. Sri. Paris. Ser. 3. Sei.
309 I
On the origin of the carpel as eviDovvcld.
denced by its vascular skeleton. Phv tomorphologv 40:
387-394."
Kn.lress. P. K. 1991, Diversity and Evolutionary Biology
of'Tropical Flowers. I ainhi id-e I ni\. Press. Cambridge.
Ccrlach. I). 1984. Botan ' '
Harvey. W .1 l')2 ^-le,,,.,!,, N,.d ,.
Tiegheni and Related Genera. Unpublished Thesis.
diversity of Reading.
Igersheim. A. e\ P. K. Endless. |W7. G\ noeciiim diverBot. J. Linn.Soc. 124: 21:^271.
Leinfellner. W. 1965. Wie siml die Winlerace, kai| lie
fonnmen Pla/.cnla in den karpellen von tens.

Wintera. Osterr. Bol. /. 113:84-95.
. 1966b. Wie siml die Winteraceen-karp
sachlu-h gehaut? IIIDie Karpelle von Bubb
(Urn, Bol./. 113: 2lo 2(.l
. 1967. Cher die karpelle verschiedener
bales. V. Pleodendnm (Canellaceacl. Osterr.
114: 502-507.
Leroy, J.-F. 1977. A compound ovary with open
..I. >- I. \\. A <:. (.. Y.M. I'M,', ll comparative morphologv of III.- Winleraeeae. II Carpels. .1. \riiold \i
bor. 24: 472-181.
Icioin. I'. l'i;;[i. \speets anatomic|ues et l>iol< -<r.< ,J,
I,, linn ,:
' monaeees. Unpublished Thesis, Lniverif Paris II. Orsay. 590.
-. 1991. Distrihiition of stigmata- plate putlerns
.Ser. 3. Sei. Vie 312: 561-506.
rigin of the p
its hearing mi lli,- intcrpr.-lalion of the magnolia

is gvnoeeium. Svst. Oeogr. PI. 68: 213-224.
-& D. Frame. 1998. Flower vasculature in Magaceae, Annonaceae and Winleraeeae: Lessons in
lions. Science 196: 977-978.

. 1978. Une sous-famille monotypique (
tcraccae cndemique a Madagascar: Les Takhl
deae. Wl.msonia. ser. 2. 17: 383-395.
tajania (Winteraceae-Takhlajanioideae). Adansonia.
ser. 2, 20: 9-20.
. 1993. Ilisloire des Iravauv sur le Takhtajunia.
Pp. 109-119 in Origine et Evolution des Plantes a
Fleurs. Masson. Paris.
Jast. C. (J. 1914, The comparative morphology ol the
Winleraeeae. \l \ascular anatomy ol I he (lowering
shoot. J. \,ol,l \rhoi. 25: 151-466.
i. C. 1975. Carpellarv vasculature and the ovular
supply in Drimvs. Amer. J. Bot. 62: 191-197.
& E. M. Gilford. 1961. Carpel vascularization of
Drimvs lanreolala. Phvtoinorphologv 14: 197-203.
1978. Vasculature in the carpels of Belliolum
pancheri (Winleraeeae). Acta Phytotax. Geobot. 29:
119-125.
.'ink. \\. I97H. The Winleraeeae of the Old World. III.
Notes on the ovary of Takhtajunia. Blumca 24: 521-
uni on the Family Magnoliaceac, Guanzhou, P. R.

Onth.
. 1993. Winleraeeae. In: P. Moral & H. S. Maekee

(editors), Flore de la Nouvelle-Caledonie 19: 90-171.
Museum National d'Histoire Naturelle, Paris.
CHROMOSOMES OF
TAKHTAJANIA, OTHER
WINTERACEAE, AND
CANELLACEAE:
PHYLOGENETIC
IMPLICATIONS1
F. Ehrendorfer* and M. Lambrou*
Viîii \< i
2n = 56
IIH
pos
.in. si/.i arid he-
Chromosome numbers available for all other Winteraeeae and the related Canellaceae (Winterales)
,eral su< c ri |.|
i
. mil parallel descending dysploid series coupled with much
:>lain the kai\oloic ,il itu
.1 li il inoiiuliht I. u surviving taxa.
iiielliKT.ii chromosoiin in il i ilinl, ill ,m
luiicn . I - il
M I
hnania. \\ I nleraceae
Tdkht.i.un.n >.ii-ti K ipuo.io Iliiinu-. i 0\ I I

Leroy was discovered in 1909 by Perrier de la Bathie in the Massif du Manongarivo of northwestern
Madagascar, where the population is now extirpated.
Only in 1963 was it described as Bubbia perrieri by
Capuron. After 85 years, its rediscovery in another
locality of northwestern Madagascar, 150 km to the
east, in the Anjanaharibe-Sud Special Reserve
(Schatz et al., 1998) has made it possible to collect
material for a first karyological study of this fascinatiug r<li<t plant. After several failures with fixations of untreated roots and flower buds (smallest
about 2 mm diam.), already too advanced for the
study of microsporocyte meioses or pollen mitoses,
preliminary results were finally obtained on mitotic
chromosome number and morphology, as well as interphase nuclear structure from preheated runt tips.
This breakthrough has stimulated a critical compilation of all chromosome counts (and additional
kaiyolog
ilii-ri-0 published s
ir on th
families of Winteraeeae and Canellaceae. That
these families are related and somewhat isolated as
Winterales within the Magnoliid assemblage (sister
to Piperales sensu lato) has been well supported
recently by plastid, mitochondrial, and nuclear
DNA sequences (Soltis et al., 1999; Qiu et al.,
1999). The aim of the present report is to summa-
i/. I'I, lil pi '

uifil. i. I- 11.1.
I .lit i <i
all taxa of Winterales (Table 1) and to compare
them with available information from DNA data as
well as other evidence (see Vink, 1970, 1985,
1993; Kubitzki, 1993). Thus, we hope to contribute
to a more unified picture of the evolution and ph\logenetic history of the two Winterales families.
MATKHIALS AND
1
Weare very giatehd i . ! I! n hi hi iul
-i
1
>poii
the material foi OUT k
I
literatim andoth. ma I.
D - h
i I m
nil i
I ihl
support is acknowlcd <,,
>
nni \. il i
i
J
Department of Hi
I
i
\NN.
METHODS
The material used for our study was collected bv

C. Birkinshaw, 7-11 September 1997, at the Anjanaharibe-Sud Special Reserve, 1445'S, 4929'E,
at an altitude of 1100-1300 m. Juvenile plants less
than 20 cm tall but exhibiting adult leaf morphology were observed growing adjacent to reproductive
adults. Ten of these were transplanted into containers and transported to Antananarivo. This population is represented by the fruiting voucher C. Bir~
- et al. 483. At the time that root tips were
fixed for the present study (June 1998) only two of
the ten plants remained alive; both of these have
subsequently died.
Root tips were pretreated in a 0.059r solution o(
colchicine for 3.5 hours at room temperature, fixed
in a 1:3 mixture of glacial acetic acid and 96%
ethanol, and stored in a deep-freezer until required.
I1
id
I In
- h i i i | ilieular for collecting

\u II as for help with
i
n ilipaitmeiit financial
h-< iplmatx I < olnn illh^, ,,, h
I'.otain I. mxersity of Vienna. A-1030. Kennwcg
Inn
. <;u
Miôi lii R(.i.
CVKM.
7:
KIT
ll.'i. 3HH)
11
.11
E Ijl
J ii J jlliîll*! Si
1'
11
11111 1 1 111 1
I If I II I f 111 i
I
fc
s
'.
'S,QQ
I 1 if
II
CQ
o^ fc
OH,
OH.
to.o,
oô
fji i jj j i ill iiiipii
Ila m*
Volume 87, Number 3
Ehrendorfer & Lambrou
.1 T - >
HI Sj
I i.
J* s ||
Ill
tWj
1 1 Jill?
n
111
QQQ!
|I
11
1111
II
II
Is?
'-i
-=; :
jg J
! 1 HI? f
!3 j! -3
OS
EKKggjg
iflJltlll'i III-IJ IjSil. l?J
Chromosome preparation by the air-drying methi v\as peifotnx i! ;nr.ii It,..', lo I ,ebci Dili Sehwei/
r (1988), except that the root apices were softened
1 an enzymatic solution (2% cellulase plus 20%
ectinase) at 37C for 3 hours. The slides were
tained in a DAPI (4'-6-diamidino -2 phenylindole)
slution of 2 u.g/ml in Mc Ilvain's buffer pH7 for
0 minutes and mounted in Mc Ilvain's buffer pH7
lus glycerol 2 :1 (see Schweizer & Ambros, 1994).
! .!/ 1 hlhoplan fluorescence microscope with hllei
block A for DAPI epiluminescence. Microphotographs were taken on Kodak TMAX 400 film.
RKSI ITS
Well spread earlier and later mitoses and interphase nuclei from pretreated root tips ol 7n ''.. -
pi-nirn nr -,1 i.\\| in I"' 'jac ' . I'll. fill.. .' belong to
nod
typ
> the proximal and e\identl\
which remain ; < oiidens. n ijui 'in, nl.-rphas<- and
form about 36 larger and smaller chroi - I
(Fig. lb, c). These chromocenters exhibit a certain
tendency toward n< , I >m
li, i ij rh n ul
I
in those ol lai-oi si/.-i and an > n licddcd in a very
\\t\ikl\ staii .'.! ninmdni hi no is n alii - 1 him .:. tin
base and early metaphase condensation of
chromosome .e-n . nl- in a pioximal distal dnoc
lion b<-comes apparent v\ilh ihc dista ieions hrsl
visible as fibrous altachmi r.ls (!',;. lah This process
Is rim... uiied low id !he cue ol metapl asc | |-'lg I I,I.
just before the onset of anaphase.
From the careful inspect
111
; I.C | jj^ g I"

:' 3 i. _f 5 ' z i> ">'>'> " 86a: Gyrocarpus type) for many
Magnoliid orders such as Maiiiioliales (MagnoliCalycanthaceae, etc.). Within Winteraeeat

Chromosome
Canellaceae
Figure 1.
DAPI stained rhromosmn
trialc- ompniahle kar\n|ogi< al da:n iiv -ill Innlird.

but Drimys s. sir., in spit< > I i - urn I high i In
I >-,.,, . i:nn;|). '. rviinr- '|liit -ilni .11 k.n 1 >li 11 si
(Morawetz, 1984). Thus,
n :l - :vs|)'ct to the place1 the Winteraceae, and of
Winterales. In-. 1
Mil VI mi .1
s and l.aurales.
into the Magnoliid assemblage. Nevertheless, these
karyological features may vary quite considerabk
within orders and families (e.g., Cassytha within
LLII.H.--, Uk.nl.:. k'7): I a>;<>i<-,^ .ml '!,;,:> :>
thus within Annonaceae: Morawetz, 1986a, b, 1988).
Hi'- also applies h W intei'aceae :> .11
j
MI
nan aial imp iMished observations li di. al. llial Va-,
a;ah!',<! not enk J.a 1.!(- hor .,11 oilier memberof
the family by its low chromosome number (x = 13),
but also by mm li 1,
an 1, 1 -. n . - and int< 1phase nuclei thai correspond rather to type B of
Okada (1975). Together with the molecular evidence
(Suh et al., 1993; Karol et al., 2000 this issue; Kig.

.'( t| 1- argue- -hough ..1- una the . .-i naiai -. and >\ \ quantities in the
tueriibers of Winterales and other Magnoliids are
necessary before we can better understand the karWhat are the phylogenetic implications of the
chromosome number 2n = 36 established I > . ',
tajania relative to other members of Winterales?
The main evidence compiled in Table 1 is comigure 2 with our present knowledge about
the evolutionary divergence of the order. Tinshows that from four extant clades three (1-3) have
remained on a low ploidy level: (1) Takhtajania (n
= 18) and (2) Tasmannia (n = 13) within Winteraceae, and (3) Canellaceae (n = 14, 13, 11). Clade
( l! has hecom. slabil /ed o-i ,i >i i - IM I j >< J % | ;.id l.-s

el (n = 43, rare
. 1111 ddi MI1, I . loi
oo: and includes all remaining \\ interaeeae, i.e.
Drimys, Pseudowintera, and the Zygogynum s.l
group of closeb
I
d
h is obvious thai
. ..iisid tabic e\oli;lioi;ai\ changes and u.-1in i<.11e\lremel\ long geological histor\ of \\ ml. ,,)!,-,
(since the Lower Cretaceous: see Doyle, 2000 this
issue) inusl have ivsu l.-d i-i | In- ptesc-nt da\ h gh \
reliclual pattern of the Winterales.
There is some evidence that polyploids have becnuie dlploidl/ed l>\ cons di table i c-111,. 1 i, i i1->. ol
their karyotypes (Drimys: Morawetz, 1984; Takhtajania: see above) and now appear as "paleopolyploids." In addition, chromosomal rearrangenicnls
must have led to dysploid and/or
36
37
38
39
(Grant, 1982).
According to the ITS and trnL tree (Sul
1993; Karol et al., 2000), Takhtajania with
and Canella with n = 14 are the mos
branches of Winteraceae and C.anellaceae,
lively. If paleoletiaplouK is postulated for t
extant relicts, then n = 13 in Tasmannia (Winteraceae) as well as n = 13 and n 11 in the re[ I
'i initiated by descending dysploidy. The origin of the liighK
polyploid Winteraceae clade (4) with n = 43 (paleo-12*?) was evidently linked with a remarkable
duplication event in the ITS region (Suh et al.,
1993; Karol et al., 2000). The present diversity
center of this clade is in Australasia, i.e., former
eastern Gondwanaland, from where it (mild have
i. acli.-d \eu / al.m : u uh I'M <! " ';:!;,i trid aUo
South America via Antarctica (?) with Drimys.
In retrospect, Winterales correspond in then evolutionary pattern lo olhci impi. al. .,. .:. and "has
aP \ngios|>i-rni groups -IK! rendoiJei. I'Po. I'Wi ,
"
I
I MI :. aluies of stasigenesis (evolaionai -, " rosinnP ana a c\;a:< li..:o. bul also -how
signs of very active and recent eco-geograpl H al ia
diation (e.g., in Drimys: Ehrendorfer et al., 1979;
Tasmannia: Vink, 1970).
Volume 87, Number 3

Chromosomes of Winteraceae i
Canellaceae
Borgmann, E. 1964. Anteil der Polyploiden in der Flora

des Bismarckgebirges von Ostneuguinea. Zeitschr. Bot.
52: 118-172.
Carr, G. D. & (,. \l Hi i n
<>, I hi n .. mi nu
bers of New Caledonian plants. Ann. Missouri Bot.
Card. 73: 486-189.
Darlington. C. I), i i. P. Wylie. 1955. Chromosome Atlas
Doyle. J. A. 2000. Paleobotany, relationships, and geographic history of Winteraceae. Ann. Missouri Bot.
Gard. 87: 303-316.
In ii-l.ii! ,
!" I
.nu significance of chroprimitive Angiospenns. Pp. 220-240
no I. Origin
.'
Id. In. oi >l
lumbia Univ. Press, New York.
. 1987. Differentiation trends
, Pp. 227-237 in K. M.
in C
* , i
in tropical woody
Urbanska (editor).
p.m ill. , h \u i. - . i i . ii - Is .. \\ ii
South America. PI. Syst. Evol. 132: 53-83.
Geber, G. & D. Schweizer. 1988. Cytochemical heterochromatin differ.
,
- allxi (Cruciferae)
using a simple air-drying technique for producing chroniosoiiic spreads. PI. Syst. Evol. 158: 97-106.
Goldblatt, P. 1977. New or noteworthy chromosome
63: 889-895.
irant, V. 1982. Chromosome number patterns in primitive angiosperms. Bot. Gaz. 143: 390-394.
lair, J. B. & E. J. Beuzenberg. 1966. Contribution to a
land J. Bot. 4: 255-266.
tetrad size in the Winteraceae. I'roe. Linn. Soe. New
South Wales 79/80: 47-53.
Carol, K. G., Y. Suh, G. E. Schatz & E. A. Zimmer. 2000.
.'. ' ",
jti/it in II - .. iinii i
ni i in . from nu. I. n
Miss,,,,,, i;..t I.:,MI. .":. ii i 132.

Lubiteki, \L 1993. Canellaceae. Pp. 197-200/,/ k Ku
bitzki. .1. (;. Hohwer c\ V. Bitlrich (editors), The Families and Genera of Vascular Plants, Vol. 2. Flowering
PI i.l- Du olsl. dons \1 ,_. oh d H in II . i I < I ( II
vophvlhd fannies. Spring, i Verl.ig. I'- rhn. Ileid< 11 < .
Evol. 159: 49-79.

Oeehioni. P. 1945. 0 numero de cromosomios em "Cap,. <';,,/, 'it" l!...|r.gu. si i 'I ,r. \2
. 1948. Contribuicao ao csiudo da iamiha "Canellaceae", estudo citol6gico. Arq. Jar. Bot. Rio de Janeiro 8: 97-103.
Okada, H. 1075
u . n .. .1 . , i .1 lu.J
,i .
IV.hr.irpicae. J. Sri. Hiroshima Univ. Ser. B, Div. 2,
Bot. 15: 115-200.
Qiu, Y.-L., J. Lee. F. Bemasconi-Oiiadroni. I). F. Soltis.
P. S. Soltis, M. Zanis, E. A. Zimmer Z. Chen, V. Savolainen & M. W. Chase. 1999. The earliest angiosperms:
non.es. Nature 402: 404-107.
Halter. J. A. & C. Milne. 1973. Chromosome numbers of
some primitive Angiosperms. Notes Roy. Bot. Gard. Edmbiirgli 32: 423^128.
Raven. P. H. 1975. The bases of angiosperm phylogeny:
Cytology. Ann. Missouri Bot. Gard. 62: 724-764.
& D. W. Kyhos. 1905. New evidence concerning
Evolution 19: 244-248.
Schatz. G. F., P. P. Lowry II & A. Ramisam.l..,- i....
,.
I<'ii!. /hUiia/un,,, perrieri rediscovered. Nature 391:
ix, 133-134.
SelnM i/er. I). & P. F. Ambros. 1994. Chromosome banding, stain combinations for specific regions. Pp. 97-112
in J. R. Gosden (editor), Methods in Molecular Biology,
Vol. 29. Chromosome Analysis Protocols. Humana
S.IHs. P. S.. II. L. N.ltis K \1. W. Chase. 1999. Angio-
. ,;
h,l,! .,
Strasburger, F. 1905. Die Samenanlage von Drimys Winter! mid die Fndospertnbildung bei Angiospcrmen. Flora 95: 215-231.
Suh, Y, L. B. Thien, H. E. Reeve & E. A. Zimmer. 1993.
Molecular evolution and phylogenetic implications of
internal transcribed spacer sequences of ribosomal
DNA in Winteraceae. Amer. J. Bot. 80: 1042-1055.
Sun, B. Y, T. F. Stuessy & D. J. Crawford. 1990. Chromosome counts from the flora of the Juan Fernandez
Islands. Chile. III. Pacific Sci. 4: 258-264.
Tanaka, R. 1971. Types of resting nuclei in Orchidaceae.
I Jul. Mag. (Tokyo) 84:
I the (
L970
:a 28: 225-354.
1985. The Winteraceae of the Old World, V.
>rmum links Bubbia to Zygogynum. Blumea 31:
n....il\ plantsr1 I lei- i- ./>_>. .sii . i -i t -|> nu < . k u \ .1 > p. Dunns ,\\,le.. . ) PI V, si I , II, J' ; ,
. 1986a. Remarks on k.i . il ..il
i ii
patterns in tropical woody plants. PI. Syst. Evol. 152:
49-100.
. 1986b. Systematics and karyoevolution in Mag-
Genera of Vascular Plants \oi. cotyledons. Magnoliid, Hamam

Families.
Flowering Plants, DiHeidelberg.
MOLECULAR EVIDENCE FOR
Kenneth G. Karol, Youngbae Suh,<
THE PHYLOGENETIC
POSITION OF TAKHTAJANIA
IN THE WINTERACEAE:
INFERENCE FROM NUCLEAR
RIBOSOMAL AND
CHLOROPLAST GENE
SPACER SEQUENCES'
%Zabefh A^Zimme^
I
.
,ii ,
I I, ml
,
|
II I- l
I
I...- ,. .,
u.lr.n
nbosomal UNA, as well as the non-coding trnL-trnF spacer regions of the ehloroplasi D\\. were determined and
Winlerareae. I suit; i i <
i - l!i
, .
. ,
.. |
' ,,!,,;. I uiiitimodcri-
Takhtajaniti in a basal position -i-l.-i to tin e I i .. i

u
I li m li lli< ..\ei il! lopolog) within the
Winteraceae was mostly congruent between nuclear and clilt.roplast data sets, the lm\ . luiY data resulted in lower
support values in comparison to the ITS data, and failed to resolve basal relationships in the family, yielding alter amine
generated liv nuclear data alone, hut demonstrate.;
and clilompl is| h
familial phylogenetic relationships for Canellaceae.
Keywords: Canellae. i
il i
I I;
pi >N
>,
uj port for a basal branch leading to Takhtajania, as

i
'-
known until rccciilK from only a single rollerlion mail< in l,,<'"> hi! 1.1.!,<>,.i .!,'! h.i- I.MIbeen an enigma among tin basal uigiospenii latuilv
Winteraceae (Leroy, 1978). Its rediscovery in 1994
(Schatz et al., 1998) has provided the opportunity
to reevaluate those
attires anomalous within the family, as well as to explore the
phylogenetic relation- :>l ibis -olaled, odi..ma I
Malagasy endemic. Based upon morphological
characters, two alternative hypotheses have been
proposed regarding the position ..i Tiii,iita;</niti
within the Winteraceae: (I) Takhtajania is a member of a clade also comprising Pseudowintera, Belliohuu. /'/.'/''/i/ /' tov'e'fu."//i and /,^,"/ii lllie
I
d
lull. .1
dr. i.
d I i m i\ l><
quired to infer infra-
,min \\ mlei.ie. i.
lallei oin in.

r
i.
i . .
mgl
_< nils A..... i/,. .< - I i \ ink I'><>8: Kndrcss et al.,
2000 lliis issue): >i [2) l'niJi!<iintiia represents the
sister taxon to the remainder of the Winteraceae
(Leroy, 1978; Vink, 1988). The aim of the present
study is to ml.
i< position of TakhIn
-Molecular sequence
d:ila
A previous mod-colar p>h\ I. genetic study (Sub et
al., 1993) utilized the internal transcribed spacer
(I I S) region of die run I. ai i il)osomal I >N \ (ru I )N \!
to address questions of generic relationships in the
Winteraceae. Tissue of Takhtajania, however, was
IIII.IX nlible In addition to pi, s, ,,i in- i [di\ IMU<-M\
We thank Peter Raven for his enthusif
thorough critical reviews of the manuscript. This wor

and bv a Smithsnman/M. lion l!.i! . m i award for our project on basal aimiosperm relationships, flu
submitted by KGK in partial fulfillment of the requirement* lor I'UIOloO at the I imersitv of Maryland.
Laboratory of Molecular Svslematics. National Museum of Natural History. Smithsonian Institution.
D.C. 20560, U.S.A.
'Current address: Department of Cell Biology and Molecular Genetics. University of Maryland. College
land 20742, U.S.A.
1
Natural Products Besearch Institute. Seoul National University, Seoul, 110-460, Korea.
' Missouri botanical Garden. P.O. Pox 2W. St. Louis. Missouri. (..5166-0299, U.S.A.
87: 414-432. 2000.
for the family solely through ingroup analysis, Suh

et al. (1993) identified a single gene duplication
event in the Zygogynum s.l. clade, a possible molecular marker for the inclusion (or exclusion) of
"
ui within the Belliolum/Buhhi,, i
mum/Zygogynum assemblage.
If an ITS duplication event either was not identified in Takhtajania or occurred independently,
then outgroup analysis would become critical for
invesligating its relationship to lis.- remainder oi hi.
family. Both morphological and moleculai (rbcL)
eladislic sludies. which examined i elal:: .n-s i: iini'iif; haâl anmi-penti--, have i*i-iilifi*'-: ( anellaceae (represented in these studies by Canella
alone) as a putative sister taxon to Winteraceae
(Donoghue & Doyle, 1989; Qiu et al., 1993; Chase
et al., 1993). Canella also appeared to be closely
i.l.i ed \\mi< raceae on the basis of secondary
metabolites (Gottlieb et al., 1989). Canellaceae are
i '
I of six genera found in tropii
(Warburgia), Madagascar (Ci
tropical America (Capsicodendron
dron in South America, Canella and Pleodendron
in the Caribbean) (Cronquist, 1981). Although Suh
et al. (1993) had encountered difficulties in the
alignment of ITS sequences between Canella and
W iiiler,;. , ;ie. i; n;i- !< eid< .1 ': rcattempl aliginnenl
ilti 3i in. ( I i; i. I tional representatives of CaThis paper reports on the implications of new
I I->-!'] n I . data lei Ihi !,i.i;,ir,!,i and tin llvt oilier genera of Canellaceae; Canella ITS sequence
had been previon
!
nmed by Suh et al.
(1992). In addition, sequence data have been generated for two tandem chloroplast cm <
I (q
DNA) spacer regions, and analyzed both si paraleU
and in combination with the ITS sequences. The
first spacer is a group I intron and is located between the conserved trnL (UAA) 3' exon and trnh
(UAA) 5' exon. The second, an intergenic spacer,
is lot ated between the trnL (UAA) 5' exon and intV
(GAA) (Taberlet et al., 1991). Restriction fragment
length polymorphisms of this molecule have been
Mexican pines (Perez de la Rosa et al., 1995). Sequence data generated from the trnL-F region also
have been utilized lo resolve pin <>enelic -elalion
ships at both the species level (Mes & Hart, 1994)
and the generic level (Compton et al., 1998;
McDade & Moody, 1999). Several studies (Gielly
et al., 1996; Molvray et al., 1999) have demonstrated the utility of combining the ITS and ton] ! spac
er sequences for phylogene
, ITS ;
nL-F .
Idi all iiencia n| both W int< ia< car and ('anellae. a.
The species included in this study are presented

in Table 1, alont.' >\ lii .on. hei infom ! on. hl< i
ture citation, and GenBank accession numbers for
bolh I he ITS and trnL-F spacer sequences. This list
genera in both the Winteraceae and Canellaceae.
In the instances where ITS has been determined
previously (all Winteraceae [Suh et al., 1993] ex.
tajania, plus Canella [Suh et al., 1992]),
identical DNA extracts were used to amplify and
sequence the trnL-F spacers.
SEQUENCING
Standard CTAB methods of DNA isolation (Doyle
& Doyle, 1987) were used to obtain total genomic
DNA for polymerase chain reaction (PCR) amplification. To generate ITS amplicons, PCR was performed using plant specific primer ITS5 (Suh et al.,
1993) and universal primer ITS4 (White et al.,
1990) under the conditions described in Suh et al.
(1993). To generate the trnL-F spacer amplicons,
PCR was performed using universal primers "c"
and "f (Taberlet et al., 1991), also under the conditions described in Suh et al. (1993).
Sequence data were generated from PEG (polyethylene glycol) purified double-stranded PCR
products (Morgan & Soltis, 1993) with the dye-terminal,
i
ol lor the ABI
>7.v> \ Se<|iieneei ( \p.pli
hi ,- -terns, Inc.). The
entire forward and reverse strand of ITS was deleiprimers (see above) and primers ITS3 (White et al.,
1990) and C5.8S (Suh et al., 1993). To determine
the sequence for both strands of the trn\A: spacers.
: ideation primers were used as well as
primers "d" and "e" (Taberlet et al., 1991). The
resulting chromatograms were edited with Sequencher version 3.1 (Gene Codes, Inc.); regions
. oiie-p.mdni- t > !!.. atnpl ! alien pi imers were deleted. The final edited consensus sequences were
SEQUENCE AL1GNM
Table 1
List of s
imens u ed in this stud with localit

d voucher in
n, ITS literatu e citation for
nd GenBank accession numbers for both ITS and miL- F.
|)IV\ H.llsK |)lllllisll(-(l SC(|UCIICCS. .
c
Species
Voucher
Genbank ITS
ITS cita
7lt
Winteraeeae
- ' >
.,1,1, (Baill 1
New Caledonia, Mt. Koghis,
LBT 205, NO
Vink (= Zygogynum panch
eri (Baill.) Vink)
<plonii (Baker 1.)
of Canala, LBT 204, NO
Dandy (= Zygogynum
cmnlonii 1 Baker f.) Vink)
Dnmys tomtm J.R. Forst. & G. South America. Chile. (BerkeFont
ley B. G.) 45.307, NO
New Caledonia, Mt. Pani6, LBT
Tiegh. ex Morot (= Zygo202, NO
Forst. & G. Forst.) Dandy

Pseudowintera colonitn lUaoul)
Dandy
. prrrieri (Capuron)
Baranova & J.-F. Leroy
New Zealand, N. Island, Akatarawa, LBT 300, NO

New Zealand. N. Island. \katarawa, LBT 301, NO
Madagascar. Anjah.m
Suh ct al.,
\<m
WOO 111')
\<m
AY004123
Suh et al., IW3
AY004I20
\<m
UOOH2I
AY004135
AY004143
AY004138
AY004141
Suh et al.. l<*>3
AY004142
1.1 !.; pel
Vl 004140
aza et al. 1342, MO

Tasmannia insipid,, IMli e\
lunreolata (Foir.)
A.C. Smith
Zygogynum acsmithii Vink
Z\gng}mim balansac Tirgli.
(= Zygogynum pomiferum
Baill. subsp. balansae
(Tiegh.) Vink)
Zygogynum bicolor Tiegh.
ton, LBT 108, NO

Australia, (Berkeley B. G.)
60.0052, NO
New Caledonia. Mts. near Lac
Enhuit, LBT 201, NO
New Caledonia, D/.umac Mts..
LBT 203, NO
New Caledonia, Plateau de

Dogny, LBT 200, NO
Suh et al., 1003
AY004127
\<m
AY004122
AY004139
Suh et al.. IW
AY(X)412()
AY004137
Suh et al., 1003
AY004118
AY004135
Suh et al.. l<)<)2

This paper
1.03844
tt(MHI32
AY004152
AY004149
Vl 004131
AY004148
U 00II30
AY004147
AY004144
AY004145
Suh et al.,
Canellaceae
..V./.e/.u winlerana (L.) Gaertn. South America. LBT 124, NO
Capsicodendron dini.sii
South \menca. Butzkv vl al.
(Schwacke) Ocehioni
11521, US
c - ; :':,ilron ekmanii Sleu- homilliea;' l. [Hll.ll . -\irnann
rner
6866, SD
Madagascar. Lurry 4991, MO
(Baill.) Tiegh.
Huil'iurjsi sululans ((,. Berlol.)
Chiov.
AY004 ISO
! 111-. |>,:l|:rl
This paper
Puerto Rico. Axrlmd 1071:3.

MO
AY004151
. ././/./.,// //.'//. MO
Nuclear ITS. The alignment of Winteraeeae

ITS sequences of Suh et al. (1993) was used as a
guide to easily incorporate the Takhtajania ITS sequence. The paralogous copies (GenBank
AY004111-AY004117) of the ITS region as determined by Buckler et al. (1997) were not included
in the alignment.
Alignment of ITS sequences within (iauellaceae

also was easily determined by eye. Alignment of
Canellaceae with Winteraeeae sequences into a
single data set required additional information to
generate a plausible alignment. One region of ITS
1 and another in ITS 2 were unalignable across
both families, though these regions were alignable
among families. These regions were treated as nonoverlapping insertion/deletion (indel) events in the
final data set. Inferred indel regions were included
in all phylogenetic analyses with the resulting gaps
Putative secondary structures of ITS 2 were determined for each taxon employing tin minimun
free-energy program mFOLD (Zuker, 1989) using
constraints previously described by Hershl
i
and Zimmer (1996). In their study, the putative secondary structure of Canella ITS 2 was determined,
and this structure was used as a guide to determine
structures for all remaining Canellaceae.
Chloroplast trnL-F. The trnL-F spacer regions
were easily aligned by eye within and between I I
families, with the resulting indels treated i.jrntically to those in the ITS data set.
Combined data set. The aligned ITS and trnLF spacer sequences were then combined into ;i single data set. Two partitions were defined (ITS and
trnL-F) and subjected to the data partition
geneity test (Farris et al., 1995). A thousand replicates were performed and the resulting P-value
was used to determine if using the combin<
data
set for phylogenetic reconstruction would be approIn summary, three data sets were examined
the ITS data set consisting of the ITS 1, 5.8S, and
ITS 2 regions; (2) the trnL-F data set consisting of
a group I intron, the 5'-trnL exon, a non-coding
intergenic spacer region, and partial sequence of
tin !'; :ii..| \A) ;.i ounbiried data - I eor.sisi m-.' -: \r,tn
the ITS and trnL-F regions.
conducted using ^
l.Obl or4.0b2 ol PA1
lor ,
Maximum parsimony.
logenetic reconstruction under maximum parsimony (MP) was conducted by utilizing the Branch and
Bound search option in PAUP* with TBR branchswapping, MULPARS, and ACCTRAN options active. Characters were assigned equal weights
a
nucleotide positions (Fitch, 1971). Robust ne-- >1
cladistic linkages was evaluated with 1000 bootstrap replicates (Felsenstein, 1985: Sanderson.
1989). Decay values (Bremer, 1988; Donoghue et
al., 1992) for each node were calculated using the
TOPOLOGICAL CONSTRAINTS option in PAUP*.
Maximum likelihood. The strategy employed
utilized the likelihood-ratio test statistic (l.ls.-nstein, 1981; Goldman, 1993; Yang et al., 1995) to
determine the best model of DNA substitution for
models considered include the general t

ible model (GTR, equals REV of Yang, 1994a),
Hasegawa et al. (1985; denoted HKY85), Kimura
(1980; denoted K2P), and Jukes and Cantor (1969;
denoted JC69). Equations for calculating likelihoods under these DNA substitution models are
given in Swofford et al. (1996). An iterative procedure to first evaluate models an
T" [Gu
1995; Waddell & Penny, 1996]).
For the combined data set, a set of models was
i. <
lii
i i
- ilalih that the relative rates between the two molecules differed sig
nil a:ill- I I is el i-s of n ..dels assigns sites to classes and then estimates the relative rate for each
class separately (Felsenstein, 1991; Goldman &
Yang, 1994). Sites were assigned to two classes (ITS
and trnL-F). This model is denoted as "+ SS."
For each data set, a maximum likelihood heuristic search with TBR branch swapping was then performed using parameters estimated from the tree
with the best likelihood score under the best model.
If the resulting tree was differ, i
n hi
.. M
that of the original tree, the resulting tree was used
to further optimize the model parameters. With parameters re-opt isearch of ten rej
etitions of random taxon addition ai ! I I5K l>i aie
appii t was performed using fully defined mod*
parameters. Bootstrap methods (Felsenstein, 198!
Sanderson. 1989) with 1000 replicates were pe
formed to estimate robustness of nodal support.
Ri-:si i.is
v.herbaria.harvard.
Nuclear ITS. ITS sequence alignment proved to

be a relatively simple task within both Winteraceae
and Canellaceae. With the exception of two regions,
one in ITS 1 (bp 1143-1163) and the other in ITS
Table 2.
ml m>\
I!
List of the iMM-ninn/del.-ii,

I
I I
Iti
ITS)
n ill
ii mi
idcll c. m, |,.i il- //nl l/l Is ,., (,,, j ,|aia

n. i I . i (
type (I = parsimony-informative, U = umnloim

species where indels wen I id in nul.-tl Hi
I7> l.'U
207 212
217 27>:>
2o2-25(,
27.7 2d 1
282 286
,517
it. i in ih
. ml III
!
H
1 .1 .
M-I.
Character name (A-X
in I
I I. r
li ll>|>) ( ll.il.K It I
. i|>|>t tl on IVs- ' and 2a), and the

Huhhia , omÛmu, Dw
Dnmys wmtrri.
YYinteraceae/Canellaceae
(Ti, Tl, Tp), b = (Tl, Tp),

= Tl
, Pc, Pa, Be, Bp, Es, Za,
1! ! H8
58f)-.WI
590 694
Winteraceae/Canellaceae
Winteraccae/Canclla<
Winteraeeae, Cd, Cw
Wltllci.K r.ir/Caiirli.K
Winlcraccar/Cane
Dw
Winterareae/Canel
Ce. Cw, I'm

Cd, Cm, Cw, Ws
Be, Bp, Es, Za, Zba, Zbi
I'a. IV. Br. Es. Za. /I,a. Zhi

Wi nteraceae/Canel laceae
Winteraceae/Canellaoeae
Cd, Ce, Cm, Pm
3..
|.,:'.<>
1540
1543-1544
1545
1553-1554
1573 1575
i.vi:. i.vie
He. lip. (>, Cm, Es, Pm, Ti, Tl,
Za, Zba, Zbi
lie, lip. Cm. Ks. Ti. Tl. Za.
I (.<>.-' I(,<>,
17(H) 1701
1707-1722
1717-1718
1719-1720
I72<> 1727
l ;:',/. I , r
1750-1759
1757-1758
2 (bp 1690-1722). id. 1 .

ill. v n imili,was also relatively straightforward. The two problemalie regions were partitioned equally between
the two families as non-ovei lap
Is
(e.g., positions 1143-1153 were coded as gaps in
Winteraceae and positions 1154-1163 were coded
as gaps in Canellaceae). The effect of this was to
reduce the probability of incorrect homology as-
m . I..I
. imiii.
I. retaining potential
phylogenetic information within each family.
Putative secondary structures for ITS 2 were determined for each sequence, and these structures
were generally consistent with the final alignment
(data not shown). An apparent contradiction between secondary -in. hire and DNA alignment was
found in the v5 region (see Hershkovitz & Zimmer
[1996] for details) and corresponds to bp 17041734. Although this region consistently formed a
bulge in secondary structure analyses across all individuals, the base composition and sequence
length clearly differed between families (11-15 bp
with 46-60% G/C in Winteraceae and 7-16 bp
with 75-85% G/C in Canellaceae). This result further supports treatment of this region as non-overlapping indel events. No known secondary structure
exists for ITS 1; consequently, structural . i
i: :
supporting the alignment of ITS 1 could not be gen>| 115
identified .
[TS
alignment, of which 53 (46%) were parsimony in
formative, 38 (33%) were autapomorphic, and the
remaining 24 (21%) were homoplastic. Table 2 presents these indels along with position information
and the species where indels were found.
Chloroplast tvnL-F. The trnL-F spacer regions
were easily aligned by eye within and between families. Overall, a total of 24 indels (Table 2: A-X)
were identified in the alignment. Of them, 9
(37.5%) were parsimony-informative, 12 (50.0%)
were autapomorphic, and the remaining 3 (12.5%)
were homoplastic. Especially noteworthy was indel
P (Table 2) with 105 bases present in the Winteraceae, including Takhtajania, but this indel was not
present in the Canellaceae.
Combined data set. Two partitions of the combined alignment were defined, (1) trnL-F (bp 1987) and (2) ITS (bp 988-1778). These partitions
were tested for congruence with the data partitionhomogeneity test (1000 replicates) and yielded a P
value of 0.367. This result fails to reject the null
hypothesis of congruence between the two partitions. Therefore, all phylogenetic analyses were
)Oth the ind vidua
PATTERNS OF SEQUENCE EVOLUTION

The aligned combined data set was 1778 characters long. Positions 1 to 987 represented the
trnL-F chloroplast sequence region; posil
to 1778 represented the ITS nuclear ribosomal seUnlike the situation for certain genera of Winteraceae (Belliolum, Bubbia, Exospermum, and Zygogynum), no polymorphisms were detected in the
ITS sequence for Takhtajania or any member of the
Canellaceae.
The ITS 1 sequences in Winteraceae ranged
from 238 bp in Takhtajania to 252 bp in Drimys.
In Canellaceae, ITS 1 sequences ranged from 244
bp in Capsicodendron to 274 bp in Pleodendron.

The 5.8S coding region was 164 bp in all individuals of both families, although it was only 163 bp
long in Canella. ITS 2 sequences in Winteraceae
ranged from 215 bp in Pseudowintera colorata to
228 bp in Belliolum, with Takhtajania having a 222
bp sequence. Canellaceae ITS 2 sequences ranged
from 187 bp in Cinnamodendron to 211 bp in CaThe Winteraceae chloroplast group I intron sequences ranged from 490 bp il
to 508 bp in Takhtajania perrieri. In Canellaceae,
these sequences ranged from 477 bp in Canella
winterana to 495 bp in Cinnamosma madagascariensis. The 5' trnL exon sequences were 50 bp in
all individuals of both families. The intergenic
-..; icct M qin HITS n W iiiierarejr i.ii <-d from "*u0
bp in Drimys to 368 bp in both Tasmannia insipida
1
lajania perrieri. All Canellaceae sequences were markedly shorter, ranging from 247 bp in
Wfi'twiijiu s,,ln!iins l<> 2.V) lip ii C.iihrUn tanlri
innamodendron ekmanii, and Pleodendron
ma ranthum. The 40 bp partial trnF exon sequences were identical in length u ill indi i-li I > ' !
Nuclear ITS. Using the Branch and Bound

search procedure in PAUP*, with equal weighting
of positions and Canellaceae selected as the out-,. if., .i -.ii j! ui: -I : ai-irriun <HH lift . i I. .'< -t< j>s
(366 steps exclud i .
rma e< haracters) was
obtained with the ITS data set. The consistency index (Kluge & Farris, 1969) was 0.8221 (0.7623
excluding uninformative characters) and retention
index (Farris, 1989) was 0.8793. Overall, 317 variable nucleotide positions were counted; of these,
206 (or 26% of the 791 total characters) provided
parsimony-informative changes.
To assess robustness of these results, the bootstrap
procedure (1000 replicates) and decay analyses were
run in PAUP* (TOPOLOGICAL CONSTRAINTS
were used to determine deeav values ioi each imd< I.
These results are shown in Figure 1.
A polytomy including Belliolum, Exospermum,
and Zygogynum (Zygogynum s.l.) was supported as
monophyletic and sister to Bubbia by a 97% bootstrap value and decay index of + 4. The Bubbia +
Zygogynum s.l. clade was monophyletic and sister
to Pseudowintera (represented by two species,
monophyletic in 99% of the bootstrap iterations
[decay = + 5]), supported by a 100% bootstrap
value (decay = + 10). Drimys was sister to this
Kiglllt
Slllglt
I!
> I ) II
ini MI1U.J
nt
,i
II .till ,.. I , ill
il*-
III
ll ,
i I lit
I in
'
l>/
0.41221 |0.7iil>3 cu-hiding , in informative characters), and retention index = 0.8793. Length of combined tree = 593
steps (434 step-, e\< i .
i
.
n.l. \ = 0.8381 (0.7788 excluding uninformative
characters), and retention index = 0.8994. Numbers to the left of the slash represent those generated from ITS dala
alone, while numbers to the right of the slash represent those generated from the combined data set. Branch lengths
shown above brancht
I
I
11 i i i H I > - i values shown below branches, respectively. Dark
assemblage in 95% of the bootstrap iterations (de

cay = + 3). Tasmannia (represented by two species) was monophyletic with 99% bootstrap support
(decay = + 8) and sister to the Drimys + Pseudowintera + Bubbia + Zygogynum s.l. clade in
86% of the bootstrap iterations (decay = + 3).
Takhtajania was found sister to the remainder of
the Winteraceae with a bootstrap value of 94% (deIn the Canellaceae, Cinnamosma and Warburgia
formed a clade sister to Capsicodendron in 73% of
the bootstrap replicates, with a decay index of +
3. Cinnamodendron and Pleodendron formed a
\v< II i" ported clade (100% of the bootstrap icp
li< .lies, decay = + 25) sister to the Capsifixirtu-hmi
+ Cinnamosma + Warburgia clade in 88% of the
replicates (decay = + 7). Finally, Canella was
found sister to the remainder of the family with
84% bootstrap support (decay = + 4).
Chloroplast trnL-F. Using the Branch and
Bound search procedure in PAUP*, with equal
!
i .
it
K eae selected as
the outgroup, two most parsimonious trees of 103
steps (67 steps excluding uninformative characters)
were obtained with the trnL-F data set. The consistency index was 0.9223 (0.8806 excluding uninformative characters), and the retention index was
0.9657. Overall, 90 variable nucleotide positions
were counted; of these, 55 (or 5.6% of the 987 total
i h.iiM ters) provided parsimony-informal rre chang
es. These two trees are presented in Figure 2 along
with bootstrap values and decay indices.
With the exception of alternative equally parsimonious hasaI relationships, the topoloti\ generated
by the trnL-F sequence data for Winteraceae was
not in conflict with the tree generated by the ITS
lower bootstrap support values. The polytomy of
Belliolum, Exospermum, and Zygogynum (Zygo^ i '/,,'/- I >. \p indf d to im hn!> !',,>',,, i .'I . h'-(l
strap and decay = + 2). The two species ol Pseu
dowintera were unresolved with respect to each
other and to the Bubbia + Zygogynum s.l. polytomy, and together these were only weakly supported as monophyletic and sister to Drimys (69%
bootstrap and decay = + 1). The two species of
/.. ..'., ,.i rti i. -in ii, 1
upp nied as sister taxa
in 98% of the bootstrap iterations (decay = + 5).
Finally, the trnL-F sequence data could not resolve
basal relationships within the family; both Takhta.- 2b) as sister to
; Winteraceae were equally parsimo-
droit CuiV'/t bootstrap and decay = + 2). the lopol

ogy generated by trnL-F data resulted in much
lower levels of bootstrap support, and, moreover,
a fundamental split between Old World
and New World lineages. Thus, rather than being
sister to the remaining Canellaceae as suggested by
the ITS-based phylogeny, Cam >""< was neste< with
in a weakly supposed clade of New World yj-n< a
To force such a division of the family into Old
World and New World clades requires an a Id tionaJ
11 steps in the ITS-based phylogeny.
Combined data set. Using the Branch and
Bound search procedure in PAUP*, with equal
weighting of positions and ail Canellaceae genera
selected as out<;i
tree of 593 steps (434 steps excluding uninformative characters) was obtained with the ITS/trnL-F
eoinhihed data set. The consistency index was
0.8381 (0.7788 excluding uninformative characters) and the retention index was 0.8994. The topology derived from this combined data set was
identical to that generated from the ITS data alone.
The branch lengths, bootstrap values, and decay
indices are presented in Figure 1.
Overall, with the addition of the trnL-F data,
bootstrap values either remained similar or increased in compa -n villi llx II"
,
eny. Within the Winteraceae, the most notable increases resulted in stronger support for basal
lationsl ips in the family. The position
aster to the rest of the family
was further strengthened (ITS = 94% bootstrap and
+ 8 decay index vs. combined data = 99% bootstrap and + 11 decay index), as was the position
of Ittsnunnim as lh< riexl branch mlhin ihe la:mK
The combined data set provided especially strong
support for the inclusion of Drimys in the clade
consisting of all other members of the family and
sis
'
ITS = 86% bootstrap and +
3 decay index vs. combined data = 97rA ' : it j
and + 6 decay index). Within the Canellaceae,
creased only slightly with the addition of the trnLF data (Fig. 1).
Maximum likelihood
Nuclear ITS. For the ITS data set, the best
model of DMA substitution was the general timereversible model with a proportion of sites assumed
to be invariable and equal rates assumed across
variable sites (GTR + I). With this model, parameters were fully optimized using the tree generated
in h (Pig. 1). With the model
leuristic search v\as con
Zygogynum bicolor
Exospermum stipitatum
Zygogynum acsmithii
H.
Zygogynum bicolor
- Exospermum stipitatum
- Warburgia salutaris
Capsicodendron c
- Pleodendron macranthum
I 1000 rrplicnl.-
diiclrd thai i
was identical
tree (Fig. 1). '
ter values di<
using the sin
ree trees, one of which

> the most parsimonious
ees were used to further
. The resulting parameom those generated by
parsimony tree. Thus,
ten heuris
tea (with random taxon additi
multrees, and steepest descent active) were o
ducted using the parameters defined in the inii
search. These ten random taxon addition searcl
generated a total of four equally likely trees (In
3371.16), one of which is presented in Kigmv .
uiî i- v> i 111 i 11 Winteri generated by the MP

er to the remainder of
the Winteraceae. The four trees differed in the position of Canella in the Canellaceae. Either Canella
was sister to the Warburgia + Cinnamosma + Capsicodendron clade, or sister to the Cinnamodendron
+ Pleodendron clade, or sister to the remainder of
tin- lamiK, or, finally, in an unresolved polytomy

with the three above-mentioned clades. Although
Canella is incl
rithii
monophyletie Canellaceae in 100% of the bootstrap iterations, bootstrap values do nol snppoil
i. solved phylogenetie
posil
>1 ( am ";> ithin the family.
Chloroplast IrnL-F. For the trnL-F data set, the
best model of DNA substitution was the HKY85
model with a proportion of site

variable and equal rates assui
variable
sites (HKY85 + I). With this
were fully optimized using the two trees generated
from the parsimony search (Fig. 2a, b). With the
I
i
ristic search was
conducted that resulted in a single tree identii a i
topology to one of the four most likely trees generated from the maximum likelihood ITS search
(Fig. 3a). Using this tree, parameters were re-esti>
\.lines were used
midlives. ;iiid sl.-epest doseeni active). The result
of these searches generated a single most like! 11
1996.3473), ^
b along with 1
The single 1
search was identical to one of the two trees generated by the maximum parsimony analysis using
trnL-F with one exception. The placement of Canella sister to Pleodendron and Cinnam
was not -iip|'i Mi-d. lb,tin 1. ' 1/;.\.. <'. - <
'i, in.> nm. in.I II (,"'.. . .. . ,
1)ported as an un1.-1 I I 11 In 1 mi i'i '''
.1 IIH bootstrap iterations. Cinnamodendron and Pleodendron were
supported as sister taxa in 87% of the bootstrap
iterations, and lii
'
.
is found in an unresolved trichotomy with the two above-mentioned
clades in a monophyletic Canellaceae in 100% of
the bootstrap replications. Within the Winteraceae
an uiiieMiU.d |.<.1\|MMI\ m< hi.iiti:. />.,'-'.. /.' '
bia, Exospermum, and Zygogynum was found to be
sister to the two species of Pseudowintera in 71%
of the bootstrap replicates. In 78% of the bootstrap
iterations, Drimy.s joined the above in a monophyletic elade, but was only weakly supported In a
54% bootstrap value as sister to them. There was
less than fjll'/i bootstrap support lor llio basal |
sition of Takhtajania sister to the remainder of WinCombined data set. For the combined data set,
the best model of DNA substitution was the general
time-reversible model. Among site rate variation
was accommodated for by dividing the data into two
partitions (ITS and trnL-F), thus allowing among
site rate variation to be estimated for each molecule
separately (GTR + SS). With this model, parameters were optimized using the tree generated from
the maximum parsimony search (Fig. 1). With the
model parameters defined, a heuristic search was
1 ti-It- most likely tree
ising llie same data sel (Fig. I ). This tree was used
0 further optimize model parameters. The resulting
:s did not differ, and thus ten heu-
and steepest descent ;
add.)
ve) were conduct, d 1 -1 ithe initial search. These
single most likely tree (In = -5508.26165). The

bootstrap values are presented in Figure 3c.
In general, with the exception of support for Canella as basal within Canellaceae, the bootstrap
values were con1 tli->
1 1 a I
ih
parsimony analyses of the combined data set. In
ili
was sister to the
remainder of the Canellaceae in 85% of bootstrap
il- <
11-. win 1.-a- lb
h1 ill 11 >' analyses recover, d ibis relalioti-diip 11 01 Ik ..:; , o! die bo ib ha;)
DISCUSSION
In the initial molecular phylogenetic study of

Winteraceae, Suh et al. (1993) found it difficult to
align the ITS region with certainty for several exemplar outgroup species. The present study increased generic sampling in Canellaceae from a
single exemplar (Canella) to a representative of all
genera, which go all\ iai il laled in molog-. .!--.-.inoie slowb e\ol\ ing trnL-V ehloroplast regions, for
; >II. Ii 1 o dil'bcnlh in aligninei I was encountered,
wen- investigated. With Canellaceae as the outgroup, the rooting of Winteraceae is no longer ambiguous. Phylogenetic analyses of ITS and combined YTS/trnL-F DNA sequences provided a
well-resolved m
. lor the Winteraceae that placed Takhtajania sister to the remaining genera in the family. Analysis of trnL-F sequence data alone failed to resolve the basal
topology within the family, with either Takhh.i;ani,i
1 1 ous as the basal
branch. Nevertheless, the addition of trnL-F sequenc es to a coil
\Y<
I I
1
1 1 I
111 increased support values for the same topology
I 'In
in 1 Uses of each of the three data sets mirrored those obtained linoiigli ma\ Kin in t u- uri..-i<
ITS and trnL-F sequences provided generally
weaker support for phylogenetic relationships within Canellaceae. Although parsi n I
IS
dal.i :ev. a ed 11 odeiale snpp..rl lin a ba-a p isil on
of Canella sister to the remaining members of the
family, parsimony analysis of trnL-F data weakly
suggested a fundamental New World/Old World
split in Canellaceae. Parsimony analysis of the
- onih i:. d 11 olecnl 11 data s I rc-adiod in a |opo|og\
I
I
n raled I
-
lx data alone, with

- ipport and iden-
and therefor.
ileal decav values Maximum like lihooi! aualv M-S of

poor i-csolutioii these nioleeules provide
mating basal relationsliips in Canellacea.
theless, ITS, combined YTS/trnL-F, and all maxiiinini likelihood analyses strongly suggest that the
southeastern Brazilian endemic (uips'u
forms a clade with the \fm i W i
iII
in.I < "inrmmosmu
The alignment of ITS and (mL-F sequences for
the 12 species of Winteraceae and 6 species of Canellaeeae revealed numerous probable insertiondeletion events. When mapped on the trees, these
mil.'Is liiini-l e.l > I
'
i\
rl lot < . rlain
chides. A total of .57 indels (29 ,., ITS [Fig. 1] and
8 in trnL-F [Fig. 2a]) support the separation of Winlerneeae from Canellaceae. Three ITS indels suppoii the monophx l\ ..I !'-,< miou inh-ta. ami Ihn e riil
lereut ITS indels support the monophvlv of the
/.\i<,r-\!l,i. t',<''!;<>'<::n,. /', '%;- w/,,v //,.
ml />, ,'_ ;<,:.>;,; I ;I>M nil >lagc. ( hie III.lei each III
both nuclear and chloroplast sequences (Figs. 1
ami 2a. respeclivclx ) Nippon ilielllsion oj l)r;m,,s
in the Zygogynum s.l. + Psciulnu intrni clade, ami
thus pro\ ide addii anal r\ idem r al iK di-*l mclne-in
ae. (our ITS indels support the sister relationship between Cin;;,,>,,<l,->i,ii,,r, ami /'/<>->/.'>./" ' .\li<n i- i -im>|.
ITS indel supports a sister relationship between Afa .in II
i.l \i laga
i innamosma. The
basal position of Canella in the family is lurlhei
IIs mil
hat support the
tiiouopli\ l\ oi llie re it .nmnji g< nera . .1 < ;.uiellaeea.
None ol the indi - loin ! in lh< !f,'i\ . f ( .atlellaiav
sequences were ph\ log. netiealiv niormaiiv e In its
tal, 139 indels were scored overall and 114 (82%)
were consistent with the trees generated from tinsequence data. The remaining 2 -'- i l
1 isli.
and in some eases difficult to score. For example,
in lrn\,-Y sequences, long adenine mils occurred al
3ers in closelv related taxa. The length
mpletely encloses the

(Doust, 2000 this 18in Canellathe ruptured, persistent in-
!
>
I
I i I
I- 'p red tepal color, present in Ctiiii-lhi and oilier Canellaceae, as well as
;rn s.l. species,
inn; be the ancestral condition, with the evolution
of white tepals through llie loss of pig , . .
and/or the acquisition of an optical tapetum (Endress et al., 2000 this issue) occurring a number of
times independently.
The historical biogeographical implications of
in in a basal position sister to the rei a i I- j.-nera of the Winteraceae have been discuss..I in ihe context o| die distribution of fossil
Winteraceae (Doyle, 2000 this issue) and ecophysiological constraints (Feild et al., 2000 this issue).
It is reasonable to assume that the has
. . !
leading to Tukhtajuniu became isolated in Madagascar after reaching there from continental \h ici.
ml also la;.I \la<!aga-< n m i\ a w pla-.'-d a prom
the lllid-Cretaceolls. The presence of tv

southwestern Cape possibly referable to
and the most advanced Zygogynum s.|. .
more puzzling and pioblemalie (Coet/ee X
lowski, 1988). With South Africa relatively i
from both South America and Antarctica fr
mid-Cretaceous onward (Smith et al., 1994).
I .1
\1 i
Zygogynum s.l., Pseudou intent, and Tuklilujani

exhibit a short, early-rupturing involu n n : !
congerniall) fused two, 01 rarelj three, outermo
pi-i ami parts, which could as well be consider.
the "ealw") dial is persistent in fruit vs. the coi
<Ii: Nin in liulh Ihnii is al .1 'iiismannin wl eie i!
ill' nial.-K a !n nils, la'e-rapl n i g i v > m -ai :x
conies as long as llie full) developed next inn.
I - i.l
!'.>.! i ii.i to that point in time, or
gascai max have . ontinued to serve as a COIInigi
101
need Winteraceae
parison to the Southern Gondwanan pattern of raiiiali.ii II \\ inleta. eae. lla pi.
naai < phv !<>g<
netic hypothesis of infrafamilial rcl:h >-i p
within Canellaceae suggests an "inverted" Northern
Gori.lwanan biogeographical ln<|or\. Masai cla.les of
Canellaceae are centered in northern South America and the West Indies, with a more advanced
clade exhibiting a southeastern Brazil/African-Malagasy split related to the middle Cretaceous sepa-
ration of South America and Africa (Goldblatt,

1993) and a subsequent dispersal event to Madagascar. Thus, the modern-day sympatric occurrence
of the two Malagasy endemic genera Cinnamosma
(Canellaceae) and Takhtajania (Winteraceae) may
well be the end result of vastly divergent biogeographic histories.
. \1. kiillcisjii. \ (;. KI..}.cX I . Unit. Il<>, T:-.:
ladistics 10: 315-319.

Feild, T. S., M. A. Zwieniecki & N. M. Hoi!,-.., I
(.
live. Ann. Missouri Bot. Card. 87: 323-334.
Felsenstein, J. 1981. Evolutionary trees from DNA sequences: A maximum likelihood approach. J. Molec.
Evol. 17: 368-376.
. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783-791.
. 1991. I'M II' '
Inference Package),
version 3.4. Seattle.
Fitch, W. M. 1971. Toward defining the course of evo-
tru t n Evolution
> & T. P. Holtsford. 1997.
.1 DNA: Divergent pui'Moi-M-,
i. Genetics 147: 821-832.
Chase, M. W, D. E. Soltis, R. G. Olmstead, L
D. H. Les, B. D. Mishler, M. R. Duvall, H. A. Price.
H. G. Hills, Y.-L. Qiu, K. A. Kron, J. H. Rettig, E
. J. R. !
J.
. Clark, M.
v ,, II -nil i: I! limner.
Y. Xiang, G. M. Plunkett, P. S. Soltis, S. M. Swensen,
S. E. Williams, P. A. Gadek, C. J. Quinn, L. E. Eguiai
E. Golenberg, G. H. Learn, Jr., S. W. Gral
. S. C. H.
Barrett, S. Dayanandan & V. A. Albert. '.
genetics of seed plants: An analysis of n
I
f n the plastid gene rftcL. Ann. Missouri Bot.
Card. 80: 528-580.
Coetzee, J. A. & J. Praglowski. 1988. Winteraceae pollen
tf-HII ill'
llv . I
\1 <>
II'- <(
I!' I lll'-ll-. .If.
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Compton, J. A., A. Culham & J. L. Jury. 1998. ReclasMIH aln
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Taxon 47: 593-634.
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Doust, A. N. 2000. Comparativt
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Doyle, J. A. 2000. Paleobotany, relationships, an.
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Card. 87: 303-316.
Doyle, J. J. & J. L. Doyle. 1987. A rapid DNA isolat
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& Z. Yang. 1994. A codon-based model ,,l ,, le
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Molec. Biol. Evol. 11: 725-736.
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1989. Chemical dichotomies in the Magnolialean com
plex. Nordic J. Bot. 8: 437-444.
Gu,X.,Y.-H. Vu& V\. II. I,. I))5. MaMinun, likelihood
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and s i<'.,
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Amer. J. Bot. 86: 249-260.
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, L. B. Thien. II. E. Reeve & K. A. Zimmer. 1993.
Molecular .volution and phylogenetic implications of
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'I
niniliJ
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BOOK REVIEW
Ribeiro, J. S. da S. et al. 1999. Flora da Reserva

Ducke. Guia de indentificacao das plantas vasculares de uma floresta de terra-firme na Amazonia Central. 800 pp. Softcover. ISBN 85-2110011-76. INPA (Brazil) and DFID (U.K.). Retail
price: $50 U.S. (through http://www.balogh.com).
I am not normally one to gush praises on a new
flora book, but this one deserves a score of 12 on
a scale of 0 to 10 (I admit to giving extra credit on
my exams). Why such a high rating? Because this
book excels in a number of important criteria, such
as high information content, richness of graphics,
pages, high degree of innovation, reasonManaus in central Amazonian
Amazon basin and neighboring countries.
downfall for some will be the Portuguese
the book is so graphics-oriented and self-guiding
that it is still very useable by readers not famil- "
with that language. Still, an English transl.
'
,\
: welcomed by many.
i field guidein the true sense; you can actually bring into the field wi
you and use to identify forest plants. In fact, it co
veniently comes with a transparent, thicl . I
jacket that wraps around the open face of the bo<
s~tnp.~Ne~at7lt is "designed for ease" of use" that is,
non-technical and focused mainly on vegetative
characters, since so often the plants (especially the
trees) one encounters in tropical forests lack flowers
or fruits at the time of one's visit. The flora covers
2175 species of vascular plants, each one illustrated by color photographs that are diagnostic of that
particular group. For instance, nearly all trees have
small photographs of the outer bark, a bark slash
(to show exudates or inner cortex characters), an
entire leaf, a detail of leaf venation, and often some
other distinguishing feature such as a leaf gland or
pulvinus. The species er
elude images of flowers or fruits, but at the beginning of each family, there are composite plates
showing a large part of the diversity of flowers and
fruits in the family members of the reserve (take a
look at pages 152 to 155 to be amazed by the closeup photos of Lauraceae flowers and fruits!).
The Ducke Reserve is a 10 X 10 km forest preserve situated on the outskirts of Manaus. It has
cultural experiments over the past decades, but has

now become a virtual island of forest amid the suburban sprawl of the capital of Brazilian Amazonia.
The much broader geographical utility of the flora
derives from the habitat diversity that is present in
the reserve. There are four main vegetation types,
associated with different soils and drainage patterns: (1) hilltop plateau forest> with clayey soils
and good drainage; (2) slope forest, actually a gradient from the hiUtop forest down to more sandy
and poorly drained soi\s lower down;
narana;> or what might also be called
(3) "campi_
"Amazonian
spodosol
caatingai" lower forests on white-sand
soi|s; an(, (4) baixio> or alluvia] plains along

streams that have poor drainage and are often wai <I. Only small streams traverse the reserve,
so it lack:> the '
, , ,
id the illustrated glossa^!^Z^^24 to 95. TheT

II ; 'i,!'
lll<l iliel !::
'11,1,1:. - i -1, .(!'
photographs of particular characters,

, ,
'
.
,
, , ,
leaf glands, exudates, stilt and tabular root variations, leaf types and shapes, among many others.
1
i .
i
chnique of nested diagram boxes with the characters written in or somer ' . M
it lead to groups
oi species that can be perused and compared (there
are short diagnostic text descnptions to accompany
the
Sophies). Another endearing aspect of the book
ls feature boxes or
' vignettes, interspersed in partlcular famihes For
stance, "nder Clusiaceae, a
ft ature box
'
(P- 253> illustrates and narrates the recentl
y Polished story of parakeet pollination in
Moronobea coccinea. There is also a valiant attempt
at a ra l<1 k
" P
<7 that L1S<1'S ll,tl'' clred markings
on
the right-hand margin of species pages to narrow
down a series of
criteria listed on pages 94 and 95.
I* is a great concept, though somewhat awkward in
Let me cite a personal example of how useful
this book is as a field guide. During a recent trip
to San Carlos de Rio Negro, Venezuela, some 1000
km to the north, Gerardo Aymard and I collected a
sterile canopy tree with bipinnate leaves, clearly a
legume and to our eyes likely an Abarema jspecies,
but one we had never seen with such huge, "dixiecup"-like petiolar glands. Returning to Caracas, I
Aw. MISSOURI BOT. GARD. 87: 433^434. 2000.
Flora of the Venezu
,.,,.,
r,
ums
|| ,s
vv,-11
known (Nelson
through the entire lam l\ a! the National llerhari in;

(VEN), to no avail. It took me a mere five minutes
to follow the keys through the Ducke Reserve book
and come across a very likely candidate, Abarema
adenophora. Upon consulting Barneby and
Grimes's (1996) superb monograph of the genus, I
confirmed the identification, the first report for Venezueja
el al . \>>(H)} lhai Manaus is llic epicenter of plant

collecting efforts in the Amazon, and that other
parts of the basin are so woefully undercollected or
in fact totally tmsampled that any such conclusions
stand on very slippery ground.
The
se small details aside, this book is a truly
masterful work, many years in the making, and deserving of all the praise and wide distribution it can
get. Mike Hopkins, one of the 14 authors listed on
ih< li' page, merits special credit loi macaging
cuss the diversity and phytogeography of the re-
the
serve. As one of the causes explaining tin- hh
,.
.ii-
* li
ili\cisil\ ol lU
Hie ai.-a. ttie\ discuss an.I aclualU depict a hypothetical Ple.stocene Lago Amazonas
teaching from the base of the Andes to nearly the
mouth of the Ama/<
rough the present-day Orinoco River to the Caribbean rather
ProJect
,!
and
overseeing the team of very capable
" '
wi 11- i ill a tin i i

^^
'
'
'' ""! """St of the
i ....
i. < Hi..
r HI i.
,.
^ 43Q ^ ^
. ^ USA
U2 m
Literature Cited
than into the Atlantic. The original paper postulating llns lake (I'Yailev el al.. I!"?;;.5;) presented sonic
evidence of the existence of a lake in the upper
\inazon mi Acre Stale, close to the border of Peru
and Bolivia), but their extrapolation of the extent
of the lake to the lower Amazon and draining out
through the Orinoco was and continues to be highly
speculative. However, a recent paper by Oliveira
^1^'^*]]"^ Mem. New York BoT GarZll.

1-292.
rYailey. C. I).. K. L. Lavina. A. Kaney & J. P. de Souza
j,""'^1/
,,,,,,,,,, | |,,,,.,.,.u,in. \,.,", \m,1/(lI1. |,;? |): i p;_
143.
and Daly (1999), whose interpretation the Ducke
NH
book repeats, takes this shaky concept and makes

it appear as wid<
k<
the
same section of the book steps into the "refugia"
t^?Z ^^r^^^t
345: 714-716.
Oliveira. A. A. de & I). C. Daly. 1999. Geographic dis-
quagmire, asserting that the area of Manaus is a

.
'
.
f
.
, ,
....
r
species refugium cliaractenzed by a high degree of
Icc il ,'i demisni w ill) elements IV nn main dillcrcn!
M
*""-
|{
vv
,ril,ulio
<:
v <:
h rr, i i
' ' ' '-
V1
v da Silva & M
- '
" of.\ref ^'ws -""Z ' "* region of Manans. Brazil: Implication- lor regional dm-r-ih and
Biodiversity and Conservation 8: 124511" '
(,,ns(.rva,i()n.
|1 3 00300 514
Orchids
Orchids of Guatemala:
Guatemala. Specie
j in alphabetical order,
A Revised
material, includes 734 taxa, of which 207 are new
records or recently described species not reported
ISBN 0-915279-66-5, iii +62 pp.
MSB78
Pleurothallis
$20.00
XIX: Systematics of
Icones Pleurothallidinarum-] 8 contains section

subgenera Pseudostelisand Acuminatiaou 182
CD
CD
CO
GO
CD
CO
Icones
| cones Pleurothallidinarum-)
F
9 is the first of four
parts tco treat the genus Masdevallia. It begins
a 10-page introduction to the genus with a
withal
pages with 172 line drawings, and with the addenda

subgenus (Polyantha) of two sections (Alaticaules
reduced to a single flower in a few species. f\
species, about one-fourth the total number in the

MSB76.
$35.00.

; ons. For persons interested,
future rearrangements can be made, and additions
MBG Press Orders,
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Missouri
Botanical
Garden
Press
CONTENTS
Investigations into the Systematic Botany and Phylogenetic Relationships of Takhtajania perrieri
(Capuron) Baranova & J.-F. Leroy (Winteraceae)
The Rediscovery of a Ma
George E. Schatz 297
Paleobotany Relationships, and (Geographic History of Winteraceae ... James A. Doyle 303
Wood and Bark Anatomy of Takhtajania (Winteraceae); Phylogenetic and Ecological
Implications
_
Sherwin Carlquist
Taylor S. Feild, Made} A. Zwieniecki & A. M Holbrook
Anatomy of the loung Vegetal i\e Shoot of TakJitajania nerrien I \\ interaceac)
Richard C. Keating
Floral Structure ol TuLht,ijunin and Its Systematic Position in Winteraceae
Peter k. Undress, \nlan Igvrsheim. r. II. Sampson & George E. Schatz
317
323
335
347
Andrew A7. Doust
366
The Pollen of Takhtajania perrieri (Winteraceae)

F. B. Sampson
Embryology of Takhtajania \\\ interaceac) and a Summary Statement of Embryological
380
Comparative Floral Ontogeny in Winteraceae
Hiroshi Tobe & Bruce Sampson
389
Notes on the Vascular Anatotm oi the Fruit of To khtajania (Winteraceae) and Its Interpretation
Thierry Deroin
398
Chromosomes of Takhtajania, Other Winteraceae, and Canellaceae: Phylogenetic Implications

F. Ehrendorfer & M. Lambrou
Features for the Family
407
Molecular Evidence for the Phylogenetic Position of Takhtajania in the Winteraceae:

Inference from Nuclear Ribosomal and Chloroplast Gene Spacer Sequences
Kenneth (r. karol, Youngbae Suh, George E. Schatz & Elizabeth A. Zimmer
Book Review. Fbra da Reserva Ducke by J. S. da S. Ribeiro et al., reviewed by Paul E. Berry
414
433
Annals
of the
Missouri
Botanical
Garden
2000 *
Volume 87
Number 4

at www.mobot.org (through MBG Press).
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Gerrit Davidse
Roy E. Gereau
Managing Editor,
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Diana Gunter
Associate Editor,
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Barbara Mack
Administrative Assistant
Henk van der Werff

Ihsan A. Al-Shehbaz
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The mission of the Misso uri Botanica 1 Gard.
@ This paper meets the n
,ver and share knowledge abo
Volume 87
Number 4
2000
Annals
^
of the
^K
Missouri
Botanical
Garden
PHYLOGENETIC
RELATIONSHIPS WITHIN
THE TRIBE JUSTICIEAE
(ACANTHACEAE): EVIDENCE
FROM MOLECULAR
SEQUENCES, MORPHOLOGY,
AND CYTOLOGY1
la A. McDade,' 7
E. Masta,'2 and
rine M. Riley2
ABSTRACT
We used molecular sequence data from the nuclear ribos omal int ernal transcribed spacers and from the intron and
iouships within the large (ca. 2000 specie-), wideI'he partition homogeneity test indicated thai the
ranging, and taxonomically difficult tribe Justicieae (Aeantl
data sets for the two loei were congruent, and separate analyses of the
h of it strongly supported. Justicieae are strongly
data set provides a higlilx re-obed fi\polhcsis ol'relations!]
araplnlelic grade are refilled as follows: \Pscuilcranthemum lineage (lsoglossinae {Tctnimcrium lineage |miilli
sis are supporte<l b\ data from rnorphologv and
(\lolog\. and some conform to earlier classifications of tin
There are, however, a number of novel asF>ects.
tic; the Old World members form a grade and the
NolabK. the large genu. Justin,, |ca. 700 species) is not mi
M-lei-gronp relationship between Ihclipleriiiae and the New World " justicioid" lineage is novel, and we cannot identify
similar genera) by all but phylogenetic criteria, is strongly su pported as a basal'm.-mbcr of l)i< lipterinae. an<l cvtofi.gical
mlv modestly supported as monophvletic and mav.
d by having four staminal elements (four stamens
in fact, represent a series of basal lineages. These plants ai
all Acanthaceae. Additional evidence (both taxa
and characters) will he necessar\ to resolve this uncertain!
ion of relationships within monophyletic lineages.
and these relationships arc discussed in the context of nonliales, molecular sequences, morphology, nr ITS.
Kcy words: Acanthaceae. cp tnA.-lruY. c_\tolog\. Ju-licn
phylogenetics.
1
For help in acquiring plant materials we thank K. Balkv rill, M.-J . Balkwill, M. Butterwick, A. Faivre, M. Foote, W.
llaher. I'. Jenkins. J. MacDougal. K. Olmslead. I{. Oniduff. li. Scollaml. D. Shindclman. B. Tankcislev. M. Turner. T.
Van Devender, and M. Zjhra; ARIZ. CAS. and MO; C. Mar
ig \rboretum and Botanical (.aniens. Mildred f..
flowers, and the staffs of tin- Duke I rmersitv greenhouseMathias botanical (harden. Waimea Arboretum ami Botanica 1 Cardci .. and Witwatersrand National Botanic Oarden. We
thank D. Swofford for making available lest versions of PAUP*. 11. Maddison for making available test versions of
ANN .
Miss.OUR] BOT. CARD. 87: 435-458. 2000.
"I will not sa\ thai . . . [my| i lassificalion ol tin

Justicieae ... is perfect. On the contrary, I am convinced that it is no more than a tentative effort"
(Bremekamp, 1965: 30).
The tribe Juslicieae i- tlie largest and aiguablv
most systematically challenging lineage in the plant
family Acanthaceae. Juslicieae comprise about
2000 species, and their nearly worldwide distribution essentially matches that of the family as a
whole. As documented by Lindau (in 1895) and
supplemented by numerous other contributions
since that turn il
,
habit and floral) and palynological diversity within
the tribe is consid.
i
relalionships, and affinities of Justicieae have been
controversial ever since Lindau's (1895) comprehensive inlraiamilial classification of Acanthaceae.
Lindau grouped Juslu I,I I., and several of its presumed close relatives into a tribe characterized by
having an androecium of two stamens and "Knotchenpollen" (2- or '.\ apertiirale pollen with I to .!
rows ol insulae on each side of the apertures). The
fact that several taxa of Lindau's Justicieae do not
have this type of pollen whereas several genera with
two stamens and "rvnoloheiipolleu" were classified
III oilier inbi-s I-\ I .indaii is indicative of problems
uilli his classification.
Tribe Justicieae was classified by Lindau as part
of "Imbricatae." a supralrilial group thai was defined by imbricate corolla aestivation. This pattern
of aeslivalion is likelv primitive lor \caiilhaceac.
and Imbricatae are a heterogeneous group, as has
been recognized for some time (Bremekamp, 1965)
and confirmed by recent phylogenetio work (Hedren et al., 1995; Scotland et al., 1995; McDade &
Moody, 1999; McDade et al., 2000). Further, Scotland et al. (1994) showed that there is more than
one variant of imbin ale aeslivalion among Vanthaceae. Other authors have detnonslrated that aestivation varies within r
_. iM u .! low et al.. in
press) and even within genera (Schonenberger &
Lndrcss. |<>)8) such that its use as a defining character may be unwarranted. Moreover, Lindau's
(1895) tribes and subirihes <>l Imbrn alae, including
Justicieae as described above, are not (dearly cir-
cm
bed mot pi
n .ill
manv m dispa
rate assemblages. The character basis for the classification is inconsistent in that characters used by
Lindau in Ins keys sometimes conflict with those
t:i| I ...In d.
i [
ihes or genera ineluded therein. For example, Isoglossinae are charaeteri/ed as having two stamens, but plants of some
genera placed in this subtribe by Lindau have four,
Many of Lindau's taxa contain a core of genera that
w
_ with an odd assemblage of others. For example, his Diclipterinae
fuss., Hypoestes Sol. ex R. Br.,
Periestes Baill. (= Hypoestes), and Peristrophr \ees.
ignized as cohesive by essen-
to Carlowrightia A. Gray and Anisaamthus !\ees.

which were placed by Lindau in Graptophylleae,
than they arc to othei I iicliplerinae. These probI> mis have made it difficult for subsequent students
of \canthaceae t cl.issilv tuwlv described genera
with any confidence, such that Lindau's classifieation is not widely used.
Bremekamp il(">r>! outlined a revised infrafamilial classification of Acanthaceae, but did not always specify the generic composition of his tribes
and subtribes. In a major realignment of taxa, he
included -i\ of the tribes placed by Lindau in Imbricatae (Asvstasieae. Graptophylleae. Isoglosseae,
Juslicieae. (hlnnlonemeae. Pseiideranlhciiieacl into
an expanded Justicieae with three subtribes (Justiciinae, Rhytiglossinae, and Odontoneminae). Justiciinae and Khv liglossmae i.i substitute name for
Lindau's Isoglossinae) were distinguished from
Odontoneminae on the basis of an androecium of
two stamens with no staminodes. Justiciinae were
further distinguished by presence of a rugula (a
. hannel in ihe upper lip ol the corolla in which the
style rests during anthesis), whereas plants with
lenticular biporate pollen were assigned to Rhvtiglossinae (= Isoglossinae). Most of the remaining
Juslicieae were plated in Odontoneminae. Plants
belonging to this last group retain the plesiomorphic state of one or more ol ihe characters that marked
|..iilnllv M.|,|Mlcl U M.ir.N IN.III III. I s National Si icnee Foundation I.. I \ V HI I! \Mi ."..(CMT. 1)1 B BSB<)7()7(/M). and from the Univcrsilv of An/ona small grants program. I'KDs collecting aclivilies were partially funded
by ihe Ill-house Research I initl and I m.kiv I'l.-ld lo--car.li fund of ill. California \cademv of Sciences, the Oracle
Corporation, the American Philosophical S.uiclv. and ihe Christensen Research Institute. The University of Arizona
Research Training Croup in the Analysis of Biological Diversification iNSK DIR-'M \AMyI. BIH-OMI22 k>) and the
University of Arizona's Undergraduate Biological Research Participation program supported KMR.
Departments of Kcologv and revolutionary Biology, and Plant Sciences. I mveisih ol \ii/oria. Tucson. Arizona
85721, U.S.A.
' Department of Botany. California Acailemv of Sciences, Cohlen Calc Park. San f ram,s<o. California 94118, U.S.A.
Volume 87, Number *
Br. rnekamp'- other two sublrihes. including absence of a rugula, androecium with four staminal
rl< incut- iloi.r :< r'll. -':(]; u< .1: :-,\\\
ever. JasM.nina. ai d (Id.ml uiemin.ne. in |.ar:iciilar.
1
- 1
f plants
icli thai little is
I
1
i.ni.In- ] I
classifying to this level.
Further, it is clear that although Justiciinae and
\\ a\ li^lossinae (
Isoglossinae! are hk.-b r 1:-u L <
by synapomorphies and may be mon 1
>
1 minae are not and are thus likely not
monophyletic.
and as used herein) do not end at the
-ub'ribal |e\ I. The li:l|.< includes a 1 unih< r ai .-tiera that are not I
I
11 gm- I
hrelated genera (including Justicia with ca. 700 species; see Graham, 1988, who noted a conservative
estimate of some 600 species at that time). This
often makes roiil
difficult at best.
In sun 1. there is a great deal to be learned about
;vLii|.,tid 11:- 1:1 Luis r ,-hl\ disuse Inn a-- el \ 11
lb ,, ,;
has affirmed the monophyletic
standing el re . ' msli ]s belwe. n Ji.sl : 1. ae an

the three other main lineages of Ae.
(McDade et al., 2000). Justicieae and Ruellieae
sensu lato (s.l., i.e., sensu Manktelow et al., in
press) are sistei lava. Harlerieae (including Whilto these two together, and \canthoideae (sensu
Bremekamp, 1965) are sister to the first three together. The nionophvlv of each of these, as well as
the pattern of relationships among them, is supported 1>\ molecular sequence data and, in some
cases, by morph.
Ov Mm...!.. !<)<)'> \1 inktelow et al., in press). There
has. how, ver. h. 1 li'd
_ - -- 1 1 1 1 r~!
1 ig
relationships within Justicieae. Based on admittedly sparse samp I
1
' I
plants. McDade and Moody (1999) and McDade et
al. (2000) propo- '
- ,1 .lineages of Justicieae. Other authors, notably Daniel (1986), Daniel and Chuang (1993), and Daniel et al. (1984,
1990), have informally proposed that certain gro ips
of genera are closely related, but these
have not been in the context of phylogenetic analyses nor have they been formalized.
Here we present a phylogenetic analysis based
on molecular sequence data from two regions (the
nuelcai ribosomal ITS and chloroplasl ln:\.-!n<\
spacer and intron) for a reasonably representative
sample of Justicieae. We discuss

the context of evidence from othei
ing morphology, chromosome nui
graphic distribution.
\V. <ihlaii:.-d -r.|nta).es lor species representing

all oj 1 indan"- I I .*'**'.~iI suprageniri. < i\a nl Imbi
catae that were 1
ekamp (1965) in
Ins .Inslici.-at . Ii addil 101 . we alh 1 ipied to - 1111
two or more species of the larger genera of Justicieae, with emph
' I lie: 111 in both
the Old and New Worlds, e.g., Justicia, Dicliptera.
From the very large genus Justicia, we include.I
i 0-1,1/. 1 by Graham (1988). To root our hypothesis of relationships among Justicieae, we used two
members of each of the other main lineages of
Acanthaceae s. str. as milgroiips: Ruellieae s.l. (one
species ea. ll ! /v
i s
' i '
(one species eai l
and Acanthoideae (one species each ..1 1,
II -I \ hi '. ,. 1 \ pemllX I I. We in. haled ill.
most distantly r<
1111 ihese lineages
lor winch we had material and were able to obtain
sequences. This should have the effect of "breaking" long branches (sensu Felsenstein, 1985) and
thus increase confidence 111 mil results I see *,ra\beal, 1998).
For most samples, DNA was extracted from fresh

leaf material or material dried in silica gel; recently
collected herbarium specimens were the source of
DNA lor the nan.lining species (Appendix I I. Total
genomic DNA was extracted using the modified
CTAB method of Doyle and Doyle (1987). Some
acanths have pign,. 1
i
:- that apparently
complex to DNA; this was dealt with by purifying
the DNA, as described by McDade et al. (2000).
I S
11 nl ( omprising
itsl, the 5.8s gene, and its2 (Baldwin, 1992; Baldwin et al., 1995) was amplified. Early in this project, we used the "universal" primers "itsl" and
"its5" (Baldwin, 1992). As noted by McDade et al.
IL'OU')
-I
1 ,
1
'I
lb these primers
yielded fungal contaminants. Using primers
"C26A" and "N-ncl8S10" designed for plants (Wen
& Zimmer, 1996) effectively ended this problem.
Optimal polymerase chain reaction (PCR) condilion- in ampl l> !.. 11 I < -stranded D\ \ -. ai i< ,: - >n 1
what among taxa, and we used a "touchdown" tern-
lilt |irnirs.pcr.ilUK- cycling prohle !< <

: .j.i! I. int! I'C.H conditions tor cad
McDade et al., 2000). For the trnL-trnl s.q,;, UC
a fragment comprising llic tniL nitron
exon. and the iiilerg.nn spacer belwe.
and llic IrnV gene of the chloroplast ;
me (Ta
berlet et al., 1991) was amplified using the V and
"f" primers designed by these same authors. Standard PCR techniques were used I" amplih .! i
stranded DNA.
Sequences were generated on ABI automated sequencers at the University of Arizona DNA sequencing facility using initially the same primers
as in amplification. Tliis yielded high quality se
quences for essentially all of the cp trnL-trnF PCR
templates and lor alioiil two-thirds of" tin nr l'l>
samples. However, the nr ITS region is extremely
G-(i rich in many Acanlhaceae (see McDade et al.,
L'OOce ml |ol\-C or -I, strings - 5 bp long are
present m some taxa. DNA polymerase frequently
was unable to read through these long repeats of
(is or (is such that incomplete sequences were obtained. When onl\ a partial //N I sequence was obtained using primer "N-ncl8SlO" (anchored in the
18s ,|>\ \ -en,), we attempted to complete the sequence using primer "(:26A" (anchored in the 26s
rl)\\ gene). For some templates, neither the sequencing reaction pinned with "\-IIC 1 .'!S1 (I" nor
that primed with "C26A" yielded a complele sequence. When tins oct lined, we se<|nenced using
internal primers "its2" and "its3" (Baldwin, 1992),
willed are anchored in I In- 5.8s gene and \ield se
qiience lor //\ I and /7v2, respective!} Both strai fi
were sequenced except when sequencing with one
primer \ielded a complete sequence with no ambiguities |c;i. 'J of the cp trnL-trnF templates and
1
i of nr I IS templates) or when sequencing with all
available primers did not yield completely overlapping lorward and reverse sequences (five of the nr
ITS templates).
I'ilectropherograms ol all sequences were proofread manually. Overlapping portions were reconciled by reverse-complementing one, aligning the
two, and double-checking any
against the electropherograins: in
Sequences were aligned separately by eye in

SeqApp (Gilbert, 1994), and then moved into
MacClade version 4.0all (Maddison & Maddison.
IW)|. These are available on request from LAM.
As documented by McDade et al. (2000), the nr
ITS region is quite divergent among .
15%.
201:.
..-.-'
i
l.nce between Justicieae and
the six taxa used as outgroups. The six outgroup
taxa were thus scored a- missing for those nucleoiide positions. Mos| ol '| |..l ,| ' >' . nn<Mii^ data
for the ingroup are in the highly conserved 5.8s
gene. Most of the remaining missing data arc in the
',,.',,' ._,;, -i'/,. a aid .>/..//'''.;.;."/.''',> r,i: .,,"'.-/;/> !.
these sequences could not be completed despite
attempts using all available primers. Aligrm n) <>i
llic ill ITS sequences required lilt I ...111. I ion of mailV
gaps, most of which were one or two bp n
nglh.
restricted to a single taxon, and in highly variable
and/or G-C rich regions ol the sequences. However.
II indels were shared bv two oi more taxa, had
coMl onl.nit 5' and .'V termini, and did not overlap
gaps in the sequences for other taxa. Into, mat ion
on these indels was added to the matrix as presThe cp s
taxa, including outgroups, despite the fact that,
noted by McDade and Moody (1999), this region
prone to length mutations. Seventeen parsimony i
id to the matrix as presen. . /absence .
! cp locus, 3.2% of data
arc mi>siug; almost all of the missing data are in
llic relatively conserved 5' end of the intron.
Data matrices were analyzed separately using
PAUP* 4.0b2 (Swofford, 1999). All parsimony
analyses were conducted using rigorous heuristic
searches, i.e., 20 random addition sequences (all
analyses found a single island sensu Maddison,
I'l'M) and TBR swapping; gap- were treated as
missing data. Multiple most parsimonious (MP)
In addition to standard measures of til of chartention itidex), the strength of support loi
IIHIH
(Felsenstein, 1985) and decay or Bremer indices

(Bremer, 1988; Donoghue et al., 1992). For the nr
ITS matrix, bootstrap (BS) values reported are bom
200 full heuristic replicates with 20 random addition sequences and TBR branch swapping. The cp
data provide poor resolution in some distal . uliou.! f
logeny such that most bootstrap replicates
generated enough Ml' trees |o swamp computer
memory; it was thus n,,t possible to use rigorous
branch swapping methods. Instead. 8S values are
from 1000 replications with 500 random addition
sequences each and no branch swapping. For both
data sets, decay values for each branch were de-
Table 1.
Charactf
) and chloroplast trn\.-ln>V (52 I
193-278
356
209(0.59)
175(0.49)
0.8-31.5%
0.66-0.77
211-234
288
176(0.61)
114(0.40)
0.5-33.2%
0.66-0.77
lermmed by firs I i- i "1 n < 1 i

n prepare i set
of trees each with a single branch rt -r,\\< .!. I I
410-512
044(860')
421(0.49)'
308(0.36)'
0.5-23.8%
0.67-0.76
347-521
629
165(0.26)
73(0.12)
0-9.6%
0.33-0.38
224-332
473
160(0.34)
78(0.16)
0-15.9%
0.36-0.42
710-4524
1103(1191-')
347(0.31)*
167(0.15)*
0.4-10.9%*
0.35-0.38*
globally shortest trees is the decay index (DI) for

the branch in question.
We obtained sequences for only one of the two
loci for 13 taxa (see Appendix 1). Four of these
\
i. ./. (omata, Aniii ed for nr ITS
but not the cp locus because sequences obtained
In
i i i I
i | L
i tin more slowlv
evolv in<_ i p o. i- <-.
i be < ss'-tilialb II variant i
these compared to close relatives (-ee MeDade el
al., 2000). DNA of the other taxa could not be amthe missing locus or more than VA of the
sequence was missing even after attempts to se-
ed int.. I'M P* asconstrai.it trees, and the program

was asked to find the shortest trees consistent with
the topology in question. The difference between
the length of these trees and the globally shortest
tree- provides an indication of the parsimonv cost
(in terms of additional evolutionary transitions) involved in accepting the alternative hypothesis.
To compare patterns of molecular evolution between loci and among lineages, matrices of pairwise
HKY85 distances for both loci and for the combined sequences were output from PAUP* and
moved inlo JMP (Sail & Lehman, 1996) for analysis. The relationship be|w. - n ;: i:\\|s,> JM m e- I i
the two loci was examined using correlation, bates
: I i voiirioti 'A i ii
mipured brlw. , n selected sistel
lineages using a modified relative rates test (Sanch
& Wilson, 1973). Distances between members of
t relative w
tabulated, and i
> compare
inchided iti tbe analysis .si the locus loi wliii li coin
plete (or nearly complete) data were avail
were pruned Iron I
mbminj.
Tbe data sets thus primed to include complete sequences for the same set of 55 taxa (49 Justicieae
+ 6 outgroups) were combined into a single NEXUS file using the file editing capabilities of PAUP*.
The nr ITS and cp trnL-trnF data sets were tested
lor congruence using Karris et al.'s ||995> Incoi
gruence Length Difference test (implemented in
PAUP* as the partilmi homou-nclv |.-s:|. I'lixlo
genetic analyses of the combined data sets were
Within the nr ITS region, itsl and its'2 are roughly simdar in variability except that its] has more
informative indels than itsl (Table 1). The cp trnLtrnF spacer is considerably more variable than tin
trnL3' intron, and the spacer is likewise more
prone to indels
i I
hlference is nol
marked. Whether considered in terms of overall
vanabh -I'I - i j. t n ou\ i ;< ituati\e sites, the nr
conducted as described above; bootstrap values

(200 replicates with 5 random addition sequences
each) and i\rc.i\ indices las previously described)
were generated for each branch.
i I
ii
I
II ses were evali
i
1 '
i
.
re trees that reflect the relationship- .III-IIII.
-I These were load-
ITS region is twice as variable among these taxa as

the cp trnL-trnF region (Table I), Similarly, maximum pairwise distances are more than twice as
great for the nr ITS sequences as for the trnL-trnF
data. Across all taxa, pairwise distances for the two
loci are positively correlated (r = 0.669, rJ = 1176,
P < 0.0001), suggesting that although the two loci
tires, aiu! tin pi .1 i i
I i i iI i
; lineages will be discussed below
Results of the partition homogeneity test indicate

that the two data sets arc not incongruent (P =
<).''. : : t mllier. ex. . ji ,i> . -. ir < U l.i\,i lot which st
qiienee data from 011K out' locus were available,
the topology obtained from the combined data set
ill I I iff. t- from llie trees obtained from the
sfparalf data sets (not shown) only in degree of
resolution or in weakly supported portions. For example, the nr ITS data do not resolve /'
T. Anderson as part ol Isoglnssinae, but do not support any othei plaeement ,1 this taxon Similarly.
the ep //7;I.-//7(F data do not resolve re!a' mushj| among most spent s t>i ( Hi! \\ .rid In.<.;.'< in. ,\ herea ,
the nr ITS data provided a fully (but weakly) supps among these
taxa. As expected, given congruence of the data
sets and increased number of characters in the
combined data set [308 and 218 parsimony informative characters in the nr ITS and cp Iriil.-lniV
data sets, respectively, for a total of 526 in the combined tlala set (mile that these tallies of parsimony
informative eharaeteis are from the data sets
pruned to include taxa for which both sequences
were available)], branch support increases marketlb in the combined topology For all of these reasons, discussion of relationships is based on the
outcome of the combined analysis.
Figure f presents the strict consensus of most
parsimonious (Ml*) lie.-- produced by analysis of
the combined data sets. Note that only major linehigher level patterns of relationship; Figures 2 and
3 provide detail on relationships within lineages. In
tified here largely conform to previously, recogn
,1
taxa. we use names ol these established taxa; when
lineages have not been previously recognized or
named, we use informal names.
The combined analysis provides strong support
for monophyly of Justicieae (Fig. 1, BS = 100, DI
17}. Within Justicieae, five lineages are mnderiimage, BS = 75,

DI = 2, to very strongly, e.g., the Tetramnuim lineage, BS = 100, DI = 28. supposed is lIKMiophs
Iclic. Tin l\< .,
i- sislt i to all
other Justicieae. which are strongly supported as
monophvletic (BS - 100, DI = 12). Isogloss.nae
are moderately well .supported as mom-pin bin IBS
- 82, DI = 3), and as sister to all Justicieae excluding the /'-,
i .cage (BS = 89,
DI = 3). The Tetramerium lineage is verv strongly
supported as monophyletic; this group is sister to a
i
fiyletit lineage th it im hides Dull
i . .
and Justi, ni and dose relatives. These taxa, i.e., all
Justicieae above
lineage exclusive
of Dicliplerinae and inclusive of both Old and New
W nit I plants, will be referred to subsequently as
"jllslicioids." The labels .W World "justicioids"
olds" will be used to refer to
. - flu 'justieioids" and Dicliplerinae lineage is -lough ~u\
ported as monophyletic (BS = 97, CI = 6). There
is strong support for monophyly of the New World
"jusiicioid" lineage (BS = 100, DI = 12) and of
Dicliplerinae (BS = 100, DI = 9), and for the sister-group relationship of these lineages (BS = 94,
DI = 7). However, Old World "justicioids" are
placed as a paraphvletie assemblage below New
World "justicioids" + Dicliplerinae.
Figures 2 and 3 are strict consensus trees showin : placement of all included taxa. ai d : :>n|sitap
and decav support tor all branches. Taxa lor which
sequence data for only one locus was available
have been addetl to Flames 2 and 'A u>ing stylistic
conventions, i.e.. blanches are angled and taxon
labels and support values A]l- mill, aid in smaller
tvpe. to signal that the result is based on partial
data. <hie randomly chosen Ml' tree is presented
as Figure 4 to illustrate branch lengths.
Pseuderanthemum lineage. There is only modest support for inonophylv of this lineage from the
combined analysis (BS = 75, DI = 2). Nr ITS data
indicate that Spathacanthus Baill. belongs here,
and that tin- two included species are each other's
closest relatives wilh strong support (Fig. 2; BS =
89, DI = 4). Our data do not resolve relationships
Phylogeny of Tribe
New World
"justicioids"
Diclipterinae
Old World
"justicioidsM
Tetramerium
Lineage
Isoglossinae
Pseuderanthemum
Lineage
idles are in the combined analysis (nr ITS + cp trnl.-trnF); tax

' 'nner, angled branches with smaller l\|>el'arc labeb.
lliurbcri and Streblacantfiits cordatus. whereas only nr ITS data wert
pithnulus and >'. rosrits: sec Appendix I). Hold, large ty|>efacc bo
analysis; those in smaller typeface are from the analysis of the nr ITS data a
J. brandegeana
Poikilacanthus
Megaskepasma
Justicia caudata
J. longii
Harpochilus
.3=
if
Dicliptera sp. 9194

D. suberecta
D. resupinata
Hypoestes aristata
H. phyllostachya
Peristrophe
Rhinacanthus
Justicia betonica
Justicia sp. 9024
Justicia sp. 9010
Justicia sp. Zjhra 983
J. extensa
J. adhatoda
Anisotes
Duvernoia
j Rungia
Metarungia
analysis (i.e., nr ITS H
which data for only otic locus was available arc added on thinne
typeface bootstrap and decay values are from the combined analysis
e in smaller typeface ar
of either the nr ITS or cp trn\.-lrnV dala set. The positions of Just
trt'V) are rcsobed ini< n -I
ii| f.mt. d. whereas ./.
: and J. spicigem |nr ITS ft
liiti.inii basal i nips in lin- lineage \i.< . V-i;'/?.;; <n

thus (nr ITS only), Herpetacanthus Nees, Asystas,
Blume]. The two representatives of Asystasia ar
however., stronÛ Mipporled as nioti pn\ l< li< . I lit
;m:il\-< a and I).
species also share two unique indels. one in

genie region. Further, there is considerable t
ular divergence between the two Asystasia sp
and between \sysiasni and other members
15^ Justicia caudata

, Megaskepasma erythrochlamys
Poikilacanthus macranthus
.Harpochilus i
VDicliptera resupinata
JLL-I). suberecta
"" .Dicliptera sp. 9194
H. phyllostachya
~
Hypoestes aristati
.Rhinacanthus gracilis
Justicia betonica
Justicia sp. Zjhra 983
^Justicia sp. Daniel 9024
Justicia sp. Daniel 9010
L. Anisotes madagascariensis
Duvernoia aconitiflora
Rungia klossii
54
Metarungia galpinii
-LL Hoverdenia speciosa
Anisacanthus thurberi
, Carlowrightia arizonica
'
Tetramerium
_ Gypsacanthus nelsonii
22, Chalarothyrsus amplexicaulis
Henrya '
Pachystachys lutea
Streblacanthus cordatus
Ecbolium syringifolium
Isoglossa grandiflora
Isoglossa? sp. Daniel 9106
Razisea spicata
i^t? Stenostephanus silvaticus
- -E S. chiapensis
Ptyssiglottis pubisepala
Mackaya bella
12 Chileranthemum pyramidatum
Odontonema tubaeforme
" ' nia microphylla
Pseuderanthemum alatum
Ruspolia seticalyx
Rutty a fruticosa
Daniel 6737cv
chosen! of the I
s using ACCTKAN o
Pseuderanthemum lineage (note branch lengths in

Fig. 4). Above this unresolved y-nnp of basal i;cnera, there is weak
.
"
no Ilai\ .is
sister to all others (BS = 68, DI = 2), and strong
support for nioiiopli\l\ of the lineage above Much-
am (BS = 100, DI = 12). This last group include

one Malagasy species {Daniel C),"')'." i) thai rune
sponds to specimens at 1' llial wen annotated a
"Justicia petiti Benoist." It does not, however, ap
pear that Benoist ever formally described this tax
ribed
with another name. There is little molecula]
gei:< e uidiin ;li<- . 1 11 " . _- - b<>\ r I/-,; !,<r,n Inofe diorl
branch lengths, Fig. 4), and only the sister taxa
A';
1 nil
! Ituttxa Harv. are resolved with
strong support (BS = 99, DI = 5).
rgek conforms to
1 imlau's ! I.">() ', Isoglossmae Is :! ':<"
combined analysis as monophyletic with modest
support (BS = 82, DI 3). The group of genera
I < v, /' ,<v, !_/-. I;;K i- ,-\'r< tin l\ -'n ILK -n(>|i> l> <l
as monophyletic (BS = 100, DI = 15). The Old
I
i
Otrst. may not be monophyletic: a putative species of Isoglossa (i.e., Daniel
9106) is more closely related to Stenostephanus
Nees, Razisea Oerst., and Brachystephanus Nees
(BS = 100, DI = 9) than to /. grandiflora. The nr
ITS data place Old World Brachystephanus with
New World Razisea + Stenostephanus. with strong
support (BS = 99, DI = 7; note that these support
values are from the nr ITS analysis alone). The two
sp. . ies (il Stcmistrpharws arc placed together, but
with only modest support (BS = 80, DI = 1). There
is, however, strong -\: p al ini n . n
. 1
.1 /-,
se + Stenostephanus (BS = 100, DI = 12). Short
hiai - li ' miths .ii-i >ui> IMI , .; aid >'< ,.%'.,"' ,
(Fig. 4) indicate that then- is little molecular divergence among these three species.
Tetrameriuiti lineage.
The Telramerium lineage
is extremely strongly supported as i
(BS = 100," DI = 28). Nr ITS data indicate that
Schaueria Nees is part of this lineage but do not
resolve its relationships. Further, the nr ITS data
place the two -.
pled species i.t 1 ,
ill,
ng tin i ,. p data not
available for S. roseus and A. puberulus). There is
nr -upport for monophyly of a lineage above
f < huhuti, km/ laid "> /../.'.-' //-, i' I I ^ dili lib)
(BS - 91, DI = 5), and moderate support for the
lineage above Hoverdenia Nees (and Mirandea
Rzed., nr ITS data only) (BS = 75, DI - 4). The
combined data set provides strong support lor sisi
.1
i. I i i n-'i i
,f >
'
anthus + Pachystachys Nees (BS = 95, DI = 5) and Chalarothyrsus Lindau + Henna Nees ex Benth. (BS = 94,
DI = 4), and nr ITS data provide moderate support
for Hoverdenia 4 Mirandea (BS = 78, DI = 3; note
thai these values are from the nr ITS data alone).
Although there is weak support for the internal
nodes of the phylogeny distal to Pachystachys +
^hrh'ou ./." > imioplivk <1 i lii,i aue IMJ idim
nerium, Carlowrightia, and
Gypsacanthus E. J. Lott, V. Jaram. & Rzed. seems
highly likely based on a shared deletion in the
spacer region <
n\
S,nY
150 bp i
"Justicioids" and Diclipterinae. There is strong

support from the combined analysis (Fig. 3i lor ,i
clade comprised of much of Lindaus (18<>.a) Diii. ioids" (i.e., species of Justicia and the allied genera Rin,-:. X.
K. Mev. ex Nees, Anisotes Nees from the Old World; Harpochilus Nees,
Meiins'i.rpastha I mdan. ai : Cai ,uu-,tn:h'is I indau
from the New World) (BS = 97, DI = 6). Within
this lineage, the representatives ol 'Justicia are mil
monophyletic. Instead, the Old World species are a
I araphv lit it .--. li I ig. iiial I- basal U the I ti-l j>
terinae (as here circumscribed, see below) + the
New World "justicioids" lineage. New World Justicia are monoph
;.s7/i are included. Old World genera tra. placed as a series of lineages basal to Old World Justicia, with
strong support for Rungia + Metarungia (BS = 94,
DI = 6), for monophyly of all others above ibis pur
(BS = 94, DI = 5), and then weak support for
pre. ise placement of Duvernoia, Anisotes, and the
Old World representatives of Justicia.
There is strong support for monophyly of the Diclipterinae + New World "justicioids" lineage (BS
= 94, DI = 7), and very strong support for monophyly of each of these lineages (Fig. 3). The lineage
referred lo here as Diclipterinae largely conforms
, the .
HI.,,
canthus Nees (not part of Lindau's Diclipterinae! is
s;:oiii: \ siippoil. <l is a 1: is ,| member ol the lineage, with very strong support for monophvk ot all
included taxa above Rhinacanthus (BS = 100, DI
= 32). Hypoestes is monophyletic with strong support (BS - 93, DI = 6), and the cp trnL-trnF data
place Peristrophe as sister to Hypoestes. The genus
Dicliptera is monophyletic, including both Old and
New World members. Especially above Rlunaean
thus, branch leu
mger in Diclipterinae than in adjacent groups (Fig. 4). Using Justicia betonica as the outgroup, a relative rates tesi
indicates that sequence divergence in Die
!
is highei than in it- sister group (the New World
Th 3
idered separatelj (m ITS: t = 3.229, 13 df, P =
O.OOkO; cp trnL-trnF: t = 3.89, 12 df, P = 0.0021)
as well as for the combined data (t = 3.838, 9 df,
P = 0.004).
New World "justicioids" (i.e., representatives of
1
urn md /'c
. Willi strong
support (Fig. 3, BS = 100, DI = 12). Nr ITS sequence data place J. brandegeana as sister to Po-
:h strong support (BS = 87, DI =

4, nr ITS data alone), and place J. comata and J.
.sfiii igeta as part H ll lade 'I . ' nr; id--.- .1 i iilln-i
New World Justicia, hut without resolution. Figure
1 indicates lli.il Iu-.-n,. fi U i _ d. - aiv pJiI< short
among members of the New World "justicioid" lineage, and a relative rales lest shows lower levels of
sequence divergence ill tins . lad. romp: -d to lis
Disc,
SSIOXJ
Justicieae are strongly supported as monophyletic in our analy>i>. and tins ha- heen conlinned in
olhei analyses with richer samples of other A. anthaceae (McDade & Moody, 1999; McDade et al.,
2000) 'I In- li -nil I- uppolled hv I iicl.-i.llde - ll)
stitutions as well a- l.\ indels all Jusliciea. included here share three indels in the cp locus. Un:
usual tricolporali
" ile pollen grains
(see figs. 7-10 in Daniel, 1998a) occur in all lineages ol Justicieae as here delimited | Ithough
shifts to other types of grains are MIM|
I i.
for some elades'as discussed below). Pollen
ol tin- hpe are not known among Acanthaceae outknown in olhei- angm-peim-. We h.-ic propose lliis
character as a synapomorphy for Justicieae. Bremekamp (1965) proposed that this pollen type chari; |.-M '- - plant- ol In -nihinbe ( Monioncii: II.H . 1
t surprising that his ta>
ut instead assembles
phylel
Lack of hygroscopic trichoi

phy. Seeds of plants of Huellieae s.l.. the sister
group of Justicieae (see McDade et al., 2000), have
hvgros. opi. irichotnes (exceptions are genera previously included n I oulei idi ae al d Incliandiei
eae. which have apparently lost these slim tuns).
Seeds ot plants ol Baileneae I \\ hltfieldieae (these
together comprise the sister group ol Justicieae I
Ruellieae s.l ; se. M iiikl.low et al.. in press) also
eeplions in which they have apparently heen lo-l
seenndaiilv. I low ever, there is evidence that die h\
groseopie III. home- dilfel helweeli Buellieae sd.
and Baileri.ae I \\ hillieldieae such that they are
not likely homologous (Grubert, 1974; Scotland et
al., 1995; Manktelow, 1996). If this is the case,
then the common ancestor of these lint ag - would
have lacked hvgi
|
h In
B
i lit
>l
tin | i .genetic status of the character, la. k of h\: >
U JH i - !i-li aia.i-i - li.-i ,'!. ai I: .m
plan?- ol tin oiln : l\>u I n< ages, with just a lew

exceptions. Acanthoideae also lack hygroscopic Irichomes on the seeds, but these plants lack also the
i pi rn . ph - I1! 'i link the other three lineages
ol \eanthaeeae s. sti.. i.e.. Bin llieae s.l., Barlerieae. Justicieae (e.g.. cystoliths, articulated stems,
colporate or porate pollen) and are thus tmlikelv to
he ( onliised with them.
Pseuderanthemum lineage. The position of
these taxa as basal within Justicieae is clear from
our dala. but then- is ;i !- modes! siippoti |..t then
monophvlv. Further, we know ol no ineij I ologi. a
synapomorphies for the entire lineage. Compared to
ilhei I i H eae. these plants have an androecium
of four staminal elements (all lour max he lertile or
two may be reduced to staminodes). However, this
is no doubt plesiomoiphn lot Justicieae: il is hvi ill I amiales
s.l. (i.e., sensu Olmstead et al., 1993), and the other
main lineages ol \eantliaeeae include taxa Willi
this trait. Additional dala will be ueeessan, to lest
by our data. There is little divergence among most

ol these taxa lor the |oi i examined here, and it will
be ueeessan louoik uid inoi phological characlers
or more rapidly ev..bing I... i I., make progress in
unraveling these phylogenetic relationships.
There is some corroborating evidence for those
aspects of relationships within the /\e//./< /anihe
mum lineage thai do emerge from out analysis.
\\ hereas plants placed in unresolved fashion at the
base of the lineage have four lertile stamens, two
of these are reduced lo staminodes in plants of the
Mackaya-Ruttya clade. Further, although chromosome numbers have not been determined lor Chileranthemum Oerst. or for the unidentified Malagasy
laxon represented bv Daniel 67,'i7cv, all other genera in the Mackaya-Ruttya clade appear to have a
base chromosome numb.a of \
21 (Daniel iV
Chuang, 1989; Daniel et al., 1990; Daniel &
Chuang, 1993. W<">|. The oul\ chromosome number known for Mackaya (Old World, 2 species), n
- 12. is from a single count by Daniel and t 1 i u J
(1989); n = 42 has not been recorded for any other
g.-tins in the lineage. A chromosome complement
of n = 21 has been infrequently reported in genera
representing various other lineages within the family, but doe- riot se.iii to characterize other large.
suprageneric groups. Below the Mackaya-Ruttya
clade in tin ,'*
In i
li
HI
some counts are not available for lln/,.-;.., ,- ,(New World, ca. 10 species) or Spathacanthus (Neo-
tropical, 3 species), and x = 21 may thus be a

synapomorphy for a more inclusive lineage. Interestingly. \sY.\tttsia (Old World, ca. 50 species) lias
x = 13 and inclu l<
i
u
nip il pi
l , i
atives of that number (Daniel, 2000). Several authors have suggi
I ial \
is s i| h
n
orphic for Acanthaceae (Grant, 1955; Raven, 1975;
Piovano & Bernardello, 1991; Daniel & Chuang,
1993). If so, x = 13 has evolved via both polyploidy
loidy, and x = 21 may represent a hexapioid derivative of this base number.
There is very strong molecular support for the
I Yd clade but, within that
clade, the onl\
that of Ruspolia and Ruttya as sister ta\a. Tin si
two genera differ from others in the ChUeranthe>,>., RUIIYU clade in having monothecous stamens. Riispci!,! f \iiiea and Mad; gascar. 1 sp.-t icsj
and Ruttya (Africa, 3 species) arc clearly closely
relaled based on both mob ridai ai:<l mnipho .-. n i
evidt in i ind in
ial in
i
i I
i
hnisnolia \. M.-i-ase iK de Wei. r-- known between
them.
Hi 'slyly has been reported or observed by
TFD or LAM in all genera of the Chileranlhemum
Ruttya clade except Ruttya (based on the limited
mati ria available. j| is n:.; possible to determine
whether Ihuut'l >>,":,'<: >\J> eolleeled bom a lieterostv Ions population). Given that this trait has only
reeeiillv been observed III lu, .''.'iirl (hAM. pels,
obs.l. its absence in Rutlui may reflect lack of
study rather than absence of the character. Heternshb i- otherwise unknown among Waeiha.-eae
. As noted
bv !)., I I !'*'-,,,,. di.tm. r,.w .men,, t I,:1, ,.,.'/
mum (New World, 3 species), Odontonema Nees
(New World, ca. 30 species), Oplonia Raf. (American tropics and Madagascar. 11 species), and
i
pical, ca. 60 species) pertain prnnatih to d Here:, -es in form of the
corolla, which likely represent adaptations tor difvary at low laxonomic level in Acanthaceae (e.g.,
Ezcurra, 1993, for Ruellia; Graham, 1988, for 7^!>ri<i). We km w nl tin diagin -in mo: pimlog e:d |< atures for these gen.
ml 'b.- in mophyly of each
should be tested.
Based on both mob eulai and mi i \ liolmm a
data, it seems clear that Daniel 67.'i7cr should not
be placed in Justiria: like olh.
ants in the Pseu,', intk mum lineage, it has an androecium ol four
plus two staminodes i: this < ;i-r. m contract '. J'is!;ria. which
lack- st;unu:odesi. a d ti ,: si: male m-\a| -ei.di > e|

pale p>Leii iv,l;n 'i is rate in JusHcni). lake manv
\ia! i a . plants, its taxonomic placement requires
ddiimnai sinib . mi: H -a.i's do not indicate a cleat
generic assignment lor the species.
The Pseuderanthemum lineage is a taxonomically
heterogeneous group. in< hiding representatives of
Lindau's (1895) tribes Asystasmae ( IsYstasia. Spa
i ', , a".'''i-/v . < .lapl-iphv lb ie |/,'I/,NM,;, /1. I sod >-,-, |,
I//-,-/.! I,if,;/,!), >!,). ' !..ni..f,< II . ae | I,In l.-lhrr:,,
\},:> l.tii,:. il,i>ni!.,,,i l\'ii>Mi and (>;>1<<;<I ,i!hus Nees)], and Pseuderanlln tmae
nlhemum). To complete our und. i-tamb
- lineage and to test its monopln a -ia
tus, it will be important to include represrn; iliv. of all Justieieae that have four fertile stamens or
two stamens and two staminodes. As will be eleai
from his clas'-ilir an , ;>l die ::n in 'hi a d la m.
Lindau (1895) distributed plants with four staminal
elements in a number of tribes including Vi
sieae (e.g., Asw.
Nee-. ;,,) TholtHi: /. >?>; I!a II i ; ddlbon to lliose
already included here). Graptophylleae (Graptophyllum Nees), Isoglosseae (Podorungia Bailb,
I in ' i / ,
. Il nil ) ' d >n
lonemeae I/.'.///.., ',,;,; ball, i . /','.,.;/ I,.!;.)!: s I'M nlii..
Filrlhi Miq.). and Pseuderanthemeae (Codonacanthus Nees). Many of these genera have not been
studied in the century since Lindau's (KITH classification was proposed. Mole recclltlv described
genera with four staminal elements in< h '
ceacanthus Wassh. and Pulchranthus V. M. Baum,
Reveal & Nowicke. Based on our results we predict
that plants in most of these genera will he placed
.libit as p.ui o| .i itmnophvleln !'>> <'> r,n,!i,< una,
lineage or
of basal lineages within Justieieae. It would also be useful to lest tumopln b
cialU lliose that aie panlropical in distribution
(/
; nlhemum) or that have disjunct ranges
gas\ and 9 New World species). Given the i
ing exact taxonon
the Pseuderanthemum lineage comprises aboul
As uoled hovi .vhelhi I
: the Pseuden
phyl.
stroll- support In i i oat an ibsis ioi uioiinpin l\ oi
all other Justieieae. These plants have an androecium of two stamens; that is, with only two exceptions of which we are aware, they have lost even
staminodial remnants of the other pair. Remai .11
ul
I '
n o pla< ed as a member
of the Tetramerium lineage, see below) have four
dilheeous stamens. Two species .( /'/1 ^'gm ,i>>
(lien placed as the basal member of lsoglossina< .

see below) arc reported I" !ia\e small <i roiiaian!
staminodes (Hansen, 1992).
Isoglossinae. Lindau's (1895) key to tribes and
subtribes distinguishes Isoglossinae based on the
anthers and "Giirtelpollen" (i.e., girdled pollen).
However. II I'
I
1
'I
ing genera to it, he included also some plants that
lack this pollen type and have four stamens (e.g..
, Kadi !. \- discussed below, our results s igi:esl dial l.mdau was correct m
recognizing a group marked by girdled pollen. He
was also coticct in assigning additional genera that
lack tin- ssnapi
'
ssinae, but erred
in at least some assignment.-. . g.. Ills a member of* the Pseinleranthemiini lineage.
In our analysis, Ptyssiglottis (southeastern Asia
to I'apiiasia, 33 species) is placed in Is,
wilh rn iderate suppoit. I IK -I ;>l.ml - ha', i iilln muaiithers and a di\er-il\ ol pollen types including
die basic type loi I i-ii. c. . ,'i i; ..J: orale iie\apsi i.doeolpate pollen), but not lb
- in- Isri- I. ssinae" (Hansen.
1992; see below). Ptyssiglottis was placed by Lindau (1895) in Pseuderanthemeae, probably on the
basis of its pollen. As delimited by Hansen (1992)
i i
L
' i r n i n i with the two
exceptions noted above of small or remnant staminodia. We are. howe\er. unable to point lo clear.
non-molecular synapomorpln. - I I.KIH-- I.I
.-. i i,to other Isoglossinae. Hansen (1992) treated Ptyssiglottis a- a nieitibei ol Isoglossinae but did not
describe svnapomorphies supporting the relationship ll would be well to test the present I . :. in - that Ptyssiglottis is part of Isoglossinae by additional data (DNA sequence or otherwise). If this is the
between more typical Jnslicieae and "con Isoglossinac." which are marked In distinctive- pollen
morphological -\ napomnrphie-.
"Core*" Isoglossinae (i.e.. Isoglossn through Sten
ostephanus) are extremely strongly supported as
monoph\letic in our analysis. In addition to se([uence data, this elade is marked In three imiipic
and unreversed md. Is (two in the nr ITS locus).
These plants also appear to share Lindau's "Giirtelpollen." which is typically biporate with pores
thai aie surrounded In a more or less circular region. The two circular regions are separated from
one another by a peripheral ban.I (continuous or
interrupted) of van ing width. This type of pollen is
described and figured by Daniel (1999) for Stenostephanus and Razisea. Similar pollen has been
described in />/,/.// \\<<-;>ii>u>n\ ! I''ig'.ieirvdo Oi kellh-
Lueas. |9 and Is.^lnssa (Muller et al., 1989;

Raj, 1961, as Rhytiglossa Nees ex Lindl.), although
al least the lormei yini^ -hows ,,ion- diversity in
features such as aperture number. The identity ol
Daniel 9106 from Madagascar has yet to be determined, bill preliminary examination of its pollen
reveals biporate pollen like that of other "core" Isoglossinae, and its macromorphological characteris'ii s si;gg -I 'I- |>la<". MI. ul u Is >,L'i>>.<,: Ill il indei d
represents a species of this genus, then the two
specie- ,,l /\nglass<i included in our analysis do uol
form a monophv
'
is more closely related lo Stenostephanus, Razisea,
aid /''... ' . '. .'.'. /' N 'li in lo / n- ,' ,' "'--',, Inlei
estingly, in addition to sequence support I'm tinrelalionslnp, Daniel (>1U(> also shares hvo indels in
the trnL-trnF region with Stenostephanus + Razisea
k-. The nr ITS data support
ir.oiioplr.lv ol /;.,'.<., '.yW,,/,,>.- ,nopi< a, \ln. aand
Madagascar, 13 species) and Neotropical Stenostephanus (ea. 75 species) and Razisea (4 species).
These three genera share monolheouis anthers as
logical synapomorphy. The New World
members of this siiblineage have been divnled into
a series ol small grin ta i< He- lint: lem irk ible lloral
diversity (e u . '
I i
eraeantliiis Wassb.. Kalhre\enella landau). Wood
(1988) treated most of these as congeneric with Habracanthus Nees, and Daniel (1995b, 1999) further
<|| bi'li -' // .,. ,. ,,o,./..,, ,\ ,||, s:t ,, . , ,,/..,-,, , \,.._
ineiiclalural changes arc gradually being made lo
relied this recasting of generic limits, e.g., Wasshausen (1999). Our results indicate that there is
considerable merit to this approach and confirm
that Razisea is pari of" this group as well (Daniel,
1999). However, investigation of relationships
among the New World species using molecular data
will require a locus evolving more quickb than
those we have studied (note short branch lengths
in Fig. 4).
Isoglossinae, as here defined, are particularly
poorly known cvtologically.
by us, chromo,
for only five species. It is noteworthy that die Neo!
tropical genera v
Razisea appear
to share a couuiiei
hi. io- ,, umber of n = 18
(Daniel. 1 W>>. No chromosome numbers have been
reported lor th. II," _, , /,
His and onb a single count (n = 17)
has been reported for the Old World genus hallos
sa (widespread in Old World tropics and subtropics.
ca. 60 species) (Daniel & Chuang, 1998).
To delimit Isoglossinae clearly, it would be well
lo include representatives of other genera that lack
Pie s\ liapomol ::! lr- ' I i.I' Iliad '"< ol. " I -. .gl >-- nae.
Genera that were included in this suhtrihe by Li

dau (1895, 1897) and that would appear to be part
of "core" Isoglossiuai- as defined here inclui
;,,/.,,v,,s ,,. ., I' ,;,-.,,, an.I th, ,: ;/,.., \U ,ii|(
These, and otln in
il
with two dithecous stamens and "Giirtelpolle
(e.g., Conocalyx Benoist, Sphacanthus Benoi;
should In' added, keknowh dging at t c <-s
Mi nophyly of the larger genera of lso
should be te-l. d. mi Iiidinv /':.^v:',',.:;n Is.. ... ,w
and S!f>ri<>.s!c;t);ti!>;i.s. \lori:tph\ K af e.'.w, / \sl<-;il,ii;:iis
should be tested, and tin Usel licit -s ai ma u1 an na
this genus separate from Stenostephanus also merits
evaluation. Broad-scale studies of a number of taxa
have demonsli il.d I
genera in wideb
iphic regions are
often congeneric (e.g.. Stena
\>-> >
driopsis S. Moore. Vollesen, 1992; Oplonia-Forsythiopsis Baker, Steam, 1971; Mendoncia Veil, ex
Vand., Afromendoncia Gilg ex Lindau, and Monachochlamys Baker, Benoist, 1925).
Mono:il:\!, ol .ill la~la ieae a!>o\ < these In -I lv,a
lineages tii/'
hut igt and lso

glossinae. Fig. 1) is moderately supported (BS =
89, DI = 3), but we know of no non-inoleciilar
synapomorphies that mark this lineage.
]'' r.iriM i uai <<:--i;-y
Se jueia data -tiongb
sapper; inonoptc, U ol dins lineage: indeed, it is one
of the most stroi !
1 ides in all of JusM ,,
ticieae. In addition to sequence data, all of the
plant- ii luded n aa:
la - -is uiiiq ieb shan in<
itidels in the in ITS region. The genera sampled
here were placed by Lindau (1895) in diverse
tribes: \s\stasieae (Chalarothyrsus, part (A'flrnr\u
[as Solenoruellia Baill.]), Graptophylleae {Anisacanthus, Carlowrigl
'
ys), Isoglosseae
!/;/.-.',,,..). ,1 d Ud. n'el .'III. ..' |/-. /.o/,a..'-. //.>:.'.
^/<-m'</. Srli.uirnu, Strchhinmthus. Tetramerium (in:"1 it ii-iu //.'/w; 11. Despite landau's treatment and
the lad that we can identify no clear tion-moleeulai
-sii poiaorplnes lor the lineage, a group correndnu
i,
I tin iled here has been
eonsistenlb identified based on monographic and
cytological studies (Daniel, 1986, 1990; Daniel &
Chuang, 1993; Daniel et al., 1984). A chromosome
number of n = 18 seems to characterize the entire
group, with additional diversity in some genera
een reported to
have n = 14 (one count), 18 (six counts), and 20
lone count): ehrotno-nii.t dal; an lacking lor //,.
nirh
in
sn
<i\. Because n = 18 also oc. iu> in Isogh'.-- ii.n and la a lew spi-.-ii :- d jus!,. -,.-.
it i- IiHi nil I"
i ii is a synapo-
n or| V lot th
- II. ige or for a more
inclusive group. These plants share a number of
traits that are symplesiomorphic at this level wilhin
1
Justii a a- tin >l
i I
i
I I
.Ipati pollen la
pli
lusticieae); an androecium of
two bitheeous stamens and no staminodes (a synI
\ lor Justicieae above the Psei
parallel, inserted
at more or less the same height on the filament.
and inapp.-ndagi d id <> the. al haraderislios are
, ai iousb a edifies; i inair- m< ia! < is of die "justiThe placement of Chalarothyrsus within the Teintm, num line ig. i- aapi i-mg in thai thtv- planl ieranthemum \ineagt . as here tlehti
II
I
a chromosome complement of n = 18 (contra n =
21, which characterizes the Pseuderanthemum lineage, see above). We can onb com hide that there
was a reversal to four functional stamens in I Inevolutionary history of plants ol this unispe.-itic genus from western Mexico. Given that occasional
flowers with atypical androeeia have been observed
in a number of species of Acanthaceae (TFD &
LAM, pers. obs.), such a reversal does not seem
especially improbable. Further, trees placing Chalarothyrsus with the Pseuderanthemum lineage are
68 steps (3%) longer than the MP trees.
Within the Tetramerium lineage, most aspects of
relationships are not strongly supported. Monophylv of all included genera above Echolium (Old
World, 22 species) [+ Schaueria (New World, ca.
10 sp.t us), nr ITS data only] is strongly supported,
and thai I 1" w. < ,s lli o i h \,, >,' ,. i".
i
moderately well supported. We are not able to identify clear non-molecular synapomorphies for these
lineages. There is moderate to strong support for
sister relationships between llorenleiuu [Mexico. 1
species) + Mirandea (Mexico, 4 species) (nr ITS
onb). I'.irlivstarhys (West Indus and South America, 12 species) + Streblacanthus (Central and
South America. 4 species), and Chalarothyrsus +
11
i,
> i \.
th an
. i i-
2 -peeli -I bill.
again, non-molecular evidence is lacking. A clade

ii i I .
il )
,
i1 i igl Ih-ni MI (Fig 2i
is not especially strongly supported by sequence
data (BS = 66, DI = 2), but is marked by a unique
22 bp deletion in the nr ITS region. Similarb. a
clade composed of the New World genera Anisacanthus (ca. 20 species), Tetramerium (28 species),
/ (21 species), and Cypsacanthus (1
spot ies) is onb
1
upp.-tle,
<|
,
a
but, as noted above, these plants share a > 150bp
deletion ill the trnl-lml spacer. This shared tie-
ngb i .. i
ophyly and also
explain- I IK WI
III
|i
I.ila: llic
ep region that is absent in these four genera is the
most variable of the cp loeus (i.e., the most likely
Source <>| micleolid. ,111 >-f1' I j' li ills among i >( !cl
atives). The paucit) of morphological evidence lot
fl.ii ndups in llie Tctrunu-rium lineage reflects
Daniel and Chuang's (1993) statement regarding
problematic genem delimitations anion- these
plants ( Generic 1 ui:d n es (e !ilii< nl) al best and
arc 11 lost I \ has. d on dill, n n. . - in ll u
>g\ ih I ! i;. < ; ,id [pi I ici! to (( I li atois (e.g.. bees
and flies in Cm
id//
liinls in \nisacanthus). Among genera in this lineage, onb Hcnisa and <!lia/,m>tli\r\us have unaiiii
| m iiplm
i < , fused biai tcoles and
pollen hails in the loiinei. seeds fused to the capsule valves in the latter) that are not likely related
Interestingly, this Tetranwrtum lineage is almost
exclusively New World in geographic distribution.
Mc\ic<> is cspccialK rich in its members and scleral genera an endi inn tin re |I.I C.h.t
Cxp.'-ii, i,'i//>/.'v. Ili,rri,i<m,i \brm><ici. \;>i;<i:::>siu-,
ma T. F. Daniel; (the last is not included in our
sample but in doij
I
Ion
n n on tin basis
nl liiaciom uphologii il. pah nolngi. al. ai d . vlolog
ical similarities; Daniel, 1988, 1990)] and others
have their greatest coticeiilration of species in Mexico (e.g., Anlsat a
m llcitr\a. Tc
tramerium). Ecbolium is the only Old World member in the present sample, but its placement hen
is not surprising: Vollesen (as cited in Balkwill &
Balk will, 1998) and Daniel (1998b) have suggested
that these plants are congeneric with the North
American )catcsia Small, a genus mil in. Ii,d< d in
our analysis but which clearly belongs in this lineage. The ( Hd World
ICI i M j '!.:'
" I in
d;ai
' ill t., and Calycacanthus K.
Schuni bk. b also belong h< re and should be included in future work (the same is true of New
A I
li!'.
- mil, d above).
Assuming that we are correct about placement of
these genera in the ' ..';.in < ;., Iinc.i-_ the group
includes about 150 i
/nv1,. ',<\'\
/',,.' !>, , -,.,', < ",,. '-., ,u, \\ ,i ,.
|ihvl\ ol the "insticioids" and I)iclipterinae lineage is -Irougly supported in the combined anabsis
(recall that "justicioids" is used here to include
Justicia and allied genera, both Old and New World
in distribution), \niorm these plants, there is a
in ilkcd lendcni v ici ., i. as< d < oin|)le\ilV III ailother Justicieae. Thus he 'I , a
serted at different height;
usually i
perfectly parallel; basal appendages of various

shapes and sizes occur on the llieeae in many species. This lineage is also marked by evolution ol a
rugula: a channel like structure mi the internal surface of the upper lip formed by parallel ridges of
-Mic. During anthesis, the style lies in this
rugula, sometimes fitting so snugly thai force is required to dislodge it. II wc arc correct in placing
the evolution of the rugula here, then this structure
is lost in Diclipterinae (as here delimited) above
I
ilt-
. i
t included
in Diclipterinae are placed either as part ol a rionm MI. ph\ C'I _ .|e dial u lie b - i )ld Woil : " u>
ticioids" or as part of a clade, the New World "justicioids" lineage. As will be clear from the
lollop III; discus -ion. . I.; ua ', M- oldll ins lli.il gcncric delimitations ar
cioids," adding the ,
ticia are monophyletic.
he taxa represented
in our analysis are not monophyletic, nor do the
species of Old World Justicia that we have included
form a monophyletic lineage. However, it is interesting that all other Old World "justicioids" are
basal to the six Old World species of Justicia that
ire llic I.dr ! Tin sislei i. i irlallon d ip I ehv en
i
I, oiropii s. t i 20 spe< ies) md M
gia i Africa. 3 species) is strongly supported in our
analysis. These plants share i placenta that IIMS
clasticallv li'om the base ol llic capsule al maluiitv
(this trait is also found in Dicliptera, sec below). In
I
.
.i distinctive
hyaline or colored border. There is strong support
' i: ipbvlv of the lineage above Run-in t Mc
tarungia, but we know of no non-molecular evidence for this relationship. Relationships among
olliei i >li! Woi lil ' i i-ii, onb ' ,ie i:ol -Inn glv -up
ported by our analysis, although it is interesting
l!i
tl
''
v Justicia are moderately well
supported as monophyletic (BS = 68, DI = 4).
Conclusions regarding relationships among Old
Wodd "justicioids" arc unwarranted based on our
liinil
le (10 of at least 300 species) and the
pattern ol relationships among these.
Further, all Justicia species from the Old World ie
monophyletic in trees that are only four steps
(0.2%) longer than the MP trees. Similarly, con-.hamim: all < 'Id Woi d "" | u -1 n oids" to moiiophv Iv
requires only eight additional steps (0.3%) compared to the shortest trees. On the other hand, evidence from indels -ngve-ls ihal the present hypothesis is correct in placing some Old World
"justicioids" closer to the Diclipterinae + New
World jiisticioid" lineage than to oilier Old World
"iusticinrds." Tin three species of Malagasy J ash

cia and /. betonica share a 3 bp indel in the cp
locus with the Diclipterinae + New World "Justine ds" lineage, and these plus J. externa share a
7 bp indel, also '
h the 1
terinae + New World "justieioids" lineage.
Students of \calilliaceae have dillc-l uL<; opinions
1
of a number of genera that
are clearly closely related to Old World Justicia
.g.. \h>i,crhir,i Ifeehsl , \ili;n:<l<ia Mi I . \ulju>
1 in I IN u
V\ 11 >;;*/ .v.'g/m.sa Oerst., Ascotheca Heine, Trichocalyx Balfi., Chlamyhnmlia
Lindau, and Sarojusticia Breinek.). Addi
:
sentatives of these groups will both expand our
sample of Old World "justieioids" and test their
validity as genera. The geographic range ..1 Old
World ' justieioids" is extensive (Africa through
dec sample : here Cue have irel id, d on i Ml

Malagas',, and south \siar; sp.-tw-s) These plaetpresenl a series ol nil rami mg biogenic aph -pall, r
that can be usefully addressed once we have a well
nsoh ed phs IOJA<-II\ lor a dense-: and grog:; i j 11 i a I .
broader - . mph 'I lie phs Intern In -I; his ,i /;/ ,',, e
is discussed furlher under "The Jusliria Problem."
below.
Strong support lor mormphyls ol die I >i< ip.lei
nae
,
in age is perhaps
the most surprising component of our results. To
oil! knowledge, ihis : Til i. ,:\ d a :: I as aol pre, ->u- I.
been suggested, and we cannot identify any clear
non-molecular synapomorphies to corroborate the
jiieiu e data. Certainly this hypo I
i
re I
nships should be
tested with additional data.
mi- is stroi
upport from our
analysis for a moi:oph\ I.-lie Hi -II pierinae. including
/,'.'/;;..,',-'/',,- I hi- In ag . i iilnnns to the core of
I .indaifs : I !> Tit 1 h. Iip'ei a:a in which he placed
l'rui;t>pl;c. //t/<ocv/c\. aid /'r/.'cs.'.'v I
//,/<.-. .v. in addition to Dicliptera. However, Lindau included
also Tanum riuin and R'tnîa In :< . we have shown
thai diese genera have relationships elsewhere in
Juslieieae. Further, lie placed Rh in acanthus in
Odnnloriemiim. In lad. Rhinacanthus (Old Woi d.
c,i. 2(1 speei.si shares a rugula with "justieioids"
and lacks a numli
I lh 'ei i/i ihclipl. da e
Nonetheless, nml,-, ilai I Him uding two unique
ami unreversed indels in the cp locus) strongly sup: oi'i Rim,a. ,,;,,'/./.. as a tin in! i i ol the- lira age. ami
evlnlogical data corroborate das placement I >i< I p
in
m I i tin
.
seem to share a
l)ase chromosome < oinplenieiit ol \
la., \lthough
ibers of n = 15 and n = 30 are
ticieae n = 15 is known only in a few species of

Justicia. Among Rhinacanthus, Peristrophe, and
Hypoestes, n = 15 and 30 are the most commonly
reported numbers. Many Old World Dicliptera have
n = 13, but n = 15 is known from both Alriean
! M i
-\ -pe< a- iKaur, 1970; Daniel, unpublished data). We thus suggest that n = 13 represeiirs d\sp|.nt! evol ili.m loan //
I/>. Il lel'.-sl ingk,
all New World species of Dicliptera for which
counts have been obtained have n = 40 and thus
appear to be ancient polyploids (Daniel, 2000;
Daniel & Chuang, 1993).
Diclipterinae above Rhinacanthus are one of the
M >-i -ugly supported lineages in our analysis;
these plants are a -o well in n ke : !-. m.it phol.igie I
-vnapomorphies. Corollas of these plants lack the
i igida lhal I-. olhcrnise liai.l. Iti slit- of the "justieioids" and I 'ii
, i
_
'/-,., >
,,<; >//? aid ihfii,;>.',;,i al diare a specialized l\pe
ol' compound inflorescence (Balkwill & Getliffe
Norris, 1988). Additionally, in these three genera
180 degrees of
been lost secondarily in a number of New World Dicliptera. Inlerestinglv. in some species of New World Diclip
tera, the corolla is resupinate through a full 360
degrees ill tin st plants, tin
ilia
p<
I
normalK oriented, but this is not achieved in the
normal way (Daniel, 1995c).
The two species of Hypoestes are strongly supported as each others closest relative, and cp data
place Peristrophe sister to these two, again with
strong support (Fig. 3; these taxa also share an 11
bp indel in the cp locus). Hypoestes (Old World, ca.
150 species) differs from Peristrophe (Old World,
ca. 25 species) and Dicliptera (Old and New World,
ca. 80 species) by having monothecous anthers. We
know of no non-molecular
mark the Hypoeste
Chloroplast data (including three indels, one ca.
50 bp long) place all five species of Da
gel her. and the combined data set provides simi:g
support for monophyly of the three species (including two from the New World and one from the Old
World) tor which we have sequence data for both
genie regions. Species of I)irliptera have fruits with
elastic dehiscence of the placentae; this distinguishes ihtan from oilier Juslieieae except Rungia
+ Metarungia, which also have this trait, as noted
above. Our results agree with the conclusions ol
Balkwill and Getliffe Norris (1988) in indicating
that elastic placentae evolved separately in these
two groups; subtle differences in the trait are to be
sought. In fact, fruits of a number of other genera
lact'ular that separate from the fruit wall, hut

t considered elastic (Daniel, 1986, 1990).
characters merit further comparative stuck
Acanthaceae to ider
Diclipterinae, with an estimated diversity of 300
species, have not siilh r I ! >in li [> ilit i ill. i i
small genera observed in other lineages of Justicieae. Ihrhj>ir,,i and Ihjmrsirs arc- large genera
whose monophvlv should be tested. I -
terestlllg I- til
tera has a cytologic al correlate1, as noted above;
phylogenetie work within this genus is certainly
"Ju
On,
suggest the existence oi a monophyletic group that

includes all N<
\\ i ! /
mil members of
related genera. In addition to sequence1 support lor
this relationship, all taxa share two indels in the cp
locus. Generic limits among New Worl
"|usii
eioiels" have been unsettled lot some time. For example, among species included here, /. brande"i-mut was described onginalb in Hcin;>ci,,iir . in!
subs, ,|i nib moved to its own genus, ('.<,
Hremck.. b\ I!
treated III Si/ilmnuiiiiMd until this -roup was stud
ied by Hilsenbeck (1990). Our analysis indicates
di.ii -ohmerging lb. s, o,.i:, : I, Justii HI was warranted. Ill her mltagenei
i i i i ii
Graham (1988) included these and many other genera in Justicia. Daniel (1991) noted that Poikilaninthus (ca. 11 species) has but little to distinguish
it from New World Justicia except pollen i >rph<
ogy, as was also noted by Raj (1961) and Breinekamp (1965). In fact, among species of New World
Justu nt there is already a remarkably rich diversity
of pollen morphology (Daniel, 1998a). Megaskepasma, with a single Neotropical species, is a plant
with spectacular magenta bracts, long white corollas, and pollen that is similar to at least one species
of Poikilacanthus (Daniel, 1991, 1998a). Finally,
//,
:s ..', spei irsl is a poorlv knu i guais
endemic to Brazil with liigl.b specialized corollas.
\b ' I 'I
I i"
HIS between tins genus and
Justicia have not been lulK investigated.
We estimate that the New World "justicioid" lineage includes about 100 species, with much siill
remaining to be discovered about species-level div ci sit \ In this context, our sample of eight species
One I iding the lluc-c1 for which we have only nr ITS
data) is extremely sparse. On the other hand, our
above, such that we regard the hypothesis that the
entire group is monophv letie as robust. However.
species representing other genera, both currently

recotmi/.ed as well as those already svnonvmized
with Justicia, should be included (e.g., Schastiano
Schaueria Nees, Clistax Mart., Chaetochlamys LinI -ii. *
>
II- nisi Tabus
cina Baill.). On the other hand, as indicated b\
branch lengths in Figure 4, there is remarkably little molecular diversity among the sample,I species.
For both the nr ITS and trnL-trnF sequences. New
World "justicioids" have lower rales of divergence
than their sister group (Diclipterinae). These- low
levels of molecular divergence contrast with species
diversity (the New World "justicioid" lineage is as
q.ecics rich as any other lineage of Jusli. ieac). as
we-ll as with morphological and cytological disparity. Plants of this lineage range from prostrate herbs
to trees, have comllas from a few mm to at least
8.5 cm in length, and have a startling range of diversity in pollen morphology (Daniel, 1998a). At
least 1 1 different chromosome numbers, ranging
from n 11 to n - 31, have been reported lot
New World species of Justicia alone. It is remarkable that this explosion of morphological and cv'olngi '. Il diversity IS not rellecied b\ III..I : 111. I ill
Out results mdi 'i ll-.ii
The Justicia problem
tic, that New World Justicia is monophyletic only if a number ol other "justicioids" are included, and that Old World species
o| Jiislicia are unlikel) to form a u. <-; ! ". hi i
group whether or not other "justicioids" are included. Clearly, a great deal remains to be learned
about phvlogenclic relationships of plants described in this genus. Even species-level diversilv
remains poorly documented among "justicioids":
Index Kewensis (Davies, 1991, 1996) reports 81
1986 and 1995.
The results of our analysis point to a strong phylogenetic distinction between Old and New World
justicioids.'" despite the fact that thev -hare main
macroniorphological characteristic-, have similai
range ol pollen types. Constraining New + Old
World "justicioids" to monophvlv requires 32 additional steps (1.5%) compared to the shortest
trees. There arc- no established benchmarks against
which to evaluate an increase- ol 1.5% in treelength, but note- that decay indices (Figs. 2. 31 indicate that only Dielipl. rinae above l\i
would be resolved in trees 30 steps long, i thai il
MP trees. That is, trees in which all "justicioids"
based on study nl 2'>.> spi-no <>: the genus, Graham

(l(>8<ii recognized l(> sections. IntereslingK. '!.)
ham's work seems to have presaged our results in
thai iiiine of hel sections have specie- in both liemi
spheres (7 are restricted to the Old World, 9 to the
New World). However, the characters used to disi i the sections often seem extremely fine
[e.g., the distinctions between the Old World sect.
Justicia and the New World sect. Drejerella are
based on con.II
|..r in tti
rsiis i
(less than 25 mm versus more than 35 mm)]. We
have thus tended to view her work as a monumental
-[i
i
In i
i i/ing variation among species
ii
l>i
I prclimiuai
Our sample of
us' H -" doe- n.'.j ix-i
i .aluation of Graham's (1988) sections, but she seems to have been
correct in separating New and Old World members.
Clearly, our own contribution can be viewed as preliminary as well in that we are still far from a full
ini()erst;uidiiifj <>f tela: onships among .ill "justi-
The morphological diversity among Justicieae j

well as the-lice- .
.
p in terms of nun
I.- i (I -p. i- - ha- -nadc coming to terms with ii
Iralnha! I'-latn.ri.-lnp- iji.rr dial!eng:ng. Ii: -u. ' i
verse groups, die simplicit\ ol icolec-.ilai -e : i< i data siinplili<-s comparisiin. More importantly, ]
l the foregoing dii

ctly diagnosed Diclipte
and I lossiriae (although he placed in both of
the
uiilribes some genera that we demonstrate
belong elsewhere! bill oil). I ivi-c shllltled i -ici-.- i I
rather thoroughly. Bremekamp (1965) was likewise
correct in recogn i
sinae) and Justiciinae. The fact that he did not inil ulc 1 i|> bpl. i mac m the latt. - mirrored b\ oui
i i '
synapomorphies
llial -appc-rt the embedding <) ! Iicbp:. i it
in 1S
inekamp's Jus: iciin i- (em "j i-lii mid-""). Bremekamp's ( >d()n!niiciiiiiiae lhu> i li.d. ii I m ! ; in...
< \rcp- IV>lh.)i<l!,li:;^). ill) /-//,;,,
in. ._
and the Pseuderanthemum lineage, a non-mono1
iphological basis
cently, Balkwill and Getliffe Norris (1988) present. .:! a assiti.-alioi; toi -,, ithcm \lrican \canthaccac
that improves upon Rrvmcknmp"- cks-iii. alien 1..
removing Diclipterinae (again, as here defined ex-
. cpl ihal Hhin,!< mtihits - phi. < .[ wiln t lit i |u-l

ciinae) from Odontoneminae. These authors also
recognize Isoglos
lour Old World
"(II-1!- leld-"" phi- Ki-ii,,!- ,!hll,li\\. Hid '[(,.nl..in
minae. This latter group includes elements of our
im lineages. Finally, our results corroborate the findings of McDade and Moody (1999) and McDade et al. (2000)
. .
. lades within Justicieae, while expanding
the sample of Justicieae consid--: ibb In |>,i: 11<a.lai
these earlier analyses included no Old World "jusAs discussed throughout, our results are limited
in a number of ways. First, although much of our
phylogenetic hypothesis is remarkably strongly
supported, a lew kc\ aspects are not. Notably, establishing the phylogenetic status of the Pseuderanthemum lineage with confidence requires additional research effort. Second, in some lineages
(notably most ol
mini lineage and
New World "justicioid" lineage), the genii regionexamined bere do not provide sufficient variation
to elucidate relationships with confidence. It will
be necessary to add another, more rapidly evoking
locus to our niolci ular tools in order to unravel relationships in these groups and at lower ta\onomic
levels than explored here. Third, sampling remains
insufficiently dense to address all of the interesting
phylogenetic problems in Justicieae. nolahb with
regard to Old World "justicioids." Stating this
framework to which additional taxa can be readik
added to address specific questions regar
relationships. In addition to taxa whose
- permit predictions about their placement
framework, a few present character cornthat defy predictions (e.g., Leandriella
R.tioist with biporate pollen similar to "core" Iso.ln-lH icae). Fourth, in many cases, our knowledge
,1 M... pn log- . p, II, i !(.-;.. and . \|.,li g\ unotiv luticieae remains inadequate for the sort of largescale, comparative project that we have undertakof the present study in continuin
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trnL-trnF; NA = not available), .
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When plants ir
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llj
||.11
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lie phvlogenelie
1
list- Jllstieieae
Stenandrium pilasnluw iS. I. Blake! T. I. Dan,el:

AK 169758. AF001827; Mexico. Son,,,a: W-cnra
Muiiieipio. El Ki|>or. Van Defender & Keina G. 97434 (ARIZ).
\phelandra ramfumen.si, Duikee: \Fl6<7<>0. \F00lB2':
Panama. San Bias: near Mandinga. Rio Mandinga.
MeDade 852 (DUKE).
Buellieac 8.1.
>>ai,rl,e:i speciosa Leonard: AF169385, \r'003H3;Cul
tivated. Duke University greenhouses. Durham.
North Carolina, U.S.A., Accession No. 66-462 (native to South America), MeDade 1180 (ARIZ).
Ruellia californira llb.se) 1 M lohnst
\l 16770 1.
AF063115; Cultivated. I ni\. Arizona campus. Tucson. Arizona, U.S.A.. MeDade 1157 (ARIZ) (native
Harleria lupulma l.indl.: Al-100751. AF289758: Cult

valed. San Francisco Conservatory of Flowers, Sa
Francisco. California. U.S.A.. Daniel s.n. (CAS) (ru
live to Mauritius).
h-pidagallus villasa lledren; \Fl06752. \ F003 I 2 I: N -o
land et al. (1605) ||)\\ provided lis B. Olmstea
(University of Washington) and R. Scotland (Oxfor
stasia gangetica (L.) T. Anderson; AF289793,

AF289748; Cultivated. Nelspruil. Mpumalanga,
South Africa. Daniel & Balkuill 958b (CAS) (widc-pread in I lid World tropics and siihlmpies).
p.: \F28<>7<U. U289749; Madagascar. Fianaranlsoa.
Ranomafana National Park, Daniel 9129 (CAS).
h'ranlhemum pyramidatum (Eindau) T F. Daniel;
A1289797. AF289752; (HS) Mexico. Chiapas: Municipio I*a Trinitaria. Breedlove & Daniel 70767
(CAS).
del (>757a; AF289799, AF289754: (HS) Cultivated.
San Francisco Conservatory of Flowers. San Francisco. California. U.S.A.. Daniel 6737cv (CAS) (native
to Madagascar).
vetaeanthus stenophvllus Gomez-Laur. & Grayum;
A1-280705. AF289750; (HS) Costa Rica. Limon: Reserva Biologfa Hhov Cerere. Ilerrera 3855 (ARIZ).
kaya bella Harv.; AF289796, AF289751; Cultivated.
U.S.A.. Daniel s.n. (CAS) (native to southern Africa).
mtonema tubaeforme (Bertol.) Kuntze; AF169748,
AF063127: Cultivated, Duke University greenhous-
(id 1:1.1. MeDade 1182 (MJI/Miiiilu

Oploma mieioplnlla |l.am.) Steari
AF280753; (HS) Cultivated, San Fi
Ihn.lull 731k, (C\S) (native to'the West I
AF06.H30; Cultivati
tU-lfi.'., i/r/>,i/e //,' (ARIZ) (native to North ami
Ku.s/>o/ia setiealyx (C. B. Clark,) Miliie-Kcdl..: Ml!: WOO.
AF289755; (HS) Cultivated. Waimea Arboretum an,!
Botanical Garden, Oahu, Hawaii. U.S.A., Daniel &
Butter,, iek 0035 (CAS) (native to Africa).
limn,, ft aliens,, Liudau: \F28'{0I. \ F289756; Cultivated. San Francisco Conservatory of Flowers, San
Francisco. California, U.S.A.. Daniels./,. (CAS) (native to Africa).
>/,-" ,. n.ihus hoffmannn Liudau: \K2H9802 \\ IN
Costa Rica. San Jose: Reserva Biologica Caiaia. W,.
r/ /.'7 (ARIZ).
S.,uurill,s I, -..nan I: \F2880:i. \ F280757: (I IS| Mex
ico. Chiapas: Fl Triunfo Biosphere Reserve, Daniel
el al. 840.1 (CAS).
///;,., /;:/,.",> il null \ ii. , I.

\i :'": :.:-i
AF28071I: Cultivated. I ni\. \n/ona. Tucson. Arizona. U.S.A.. MeDade 1178 (ARIZ) (native to South
iiu nelsonii F. J. Loll. \. Jaram. \ U/,-,1..
AF289779. \F2897W: Mexico. Puebla: Muuicipin
Coxcatlan. Daniel 8357 (CAS).
/////WJ I;/M//.IM> Nee> ex Henih.: \l 0,0843. AF06.H25:
Mexico. Sonora: near Alamos. Jenkins 89-432
(ARIZ).
Ihrmlenia V<"-" Nees \F28<)777 \r28" \\\ (IIS)
firmer 3739 (CAS).
l///r ,g//xe l!/l : \I-280783. N A: (HS) Mexico. San
/;/,,.;7/ r (CAS).
I\ieh\sicl,\s lutea Nces: AF169844. AF063128; Cultivated. Duke University greenhouses. Durham. North
Carolina, U.S.A., Accession No. 84-055 (native to
Peru), MeDade 1181 (ARIZ).
Seluiucna ealieolneha (Link & Otto) Nces; \ I 280,82.
NA: (HS) Cultivated. Homestead. Florida. U.S.A..
Foote s.n. (CAS) (native to Brazil).
*l,vl,la.-a,,ths eardalus Liudau: U28078I. U 2807 12:
8203 (CAS)1.
Inslephanus Isallii \ees: \F2897O0.

car. Fianaranlsoa. Raiioinafana Yitior
W 9/07 (CAS).
kw grandiftora C. B. Clarke: AF289788. AF289745;
(HS) Cultivated. San Francisco Conservatory of
Flowers, San Francisco, California, U.S.A., Daniel
s.n. (CAS) (native to eastern tropical Africa).
.;,,. . \| ::;).;;" U2::<>.
Park. Daniel
9106 (CAS).
Btvssiglottis pubisepala (l.indaul B. Hansen; \F28i787.
\F2R>744: (HS) I'apua New Guinea. Madanu. ca. I',
km SSW of Madang. Daniel 0030 (CAS).
A'a^xe,, spieata Ocrst.: \FI(>0848. \F00.1 I.'. I: Costa
Rica. Heredia: I-a Selva Biological Station, Hummel
7974 (DUKE).
Slenoslephanus eluapensis I. F. Daniel: AF2R>7<>2.
AF289747: Cultivate,!. San Francis,-,,. California.
U.S.A.. Hreedlove & Burns 72688ev (CAS) (native to
S. silralieus (Nces) T. F. Daniel: AFI00747. AFOtvSI.'W:
(HS) Costa Rica. San ,|n,e: Barque Nacional Braulio
Carrillo, Ma.v 7800 (MO).
ImM/,,,,,//,,,, puberulus (Torr.) Henr. & F. J. Lott:
AF289778. NA; Cultivated. Univ. Arizona campus,
Tucson, Arizona, U.S.A., MeDade 1179 (ARIZ) (native to southwestern I .S. \ and northern \lr\icoi.
I. lliurben (Ton.) \. Grav: \FI(>WK>. \F(X,.5I22: I .S. \.
Arizona: Pima County. Tucson Mountains. Van Derender 88-150 (ARIZ).
CarhmngliUa arizomea \. Grav: \ F I (M'5 l>. \ I 0(,:; I 2.'..
Jenkins 89-24 (ARIZ).
Chalaiollmsus amplexieaulis Fi.ldau; AF289780,
AF289740; (HS) Cultivate,!. San Francisco Observatory of Flowers, California, U.S.A., Daniel & Bartholomew 4842gh (CAS) (native to western Mexico).
Eebolium s\ringifolium (Vahl) Vollesen; AF289786,
AF2807I3; (MS) Madagas.ar, loliata. Taolanaro.
Daniel & Biitteruuk 0733 (CAS).
San Francisco Conservatory of Flowers. San Francisco, California, U.S.A.. Daniel s.n. (CAS) (native to
Peru).
Teliamenum nenosuin Nee-: \FH.M7. \ I ()(,:! I 33:
U.S.A. Arizona: Puna County, near Patagonia.
MeDade & Jenkins 1154 (ARIZ).
herein indicate that this is not a monnphvletic group
but rather a grade).
AF289772.
sates
madagascariensis
Berloist:
AF280783: (IIS) Madagascar. Toliara: ca. 20 km N
of Toliara. Daniel & Hutteneick 0730 (CAS).
289774. AF280735;
Cultivaled. Roodcpooil. V\ ihvat. rsrand National Botanic (harden. Cauleng. South Africa. Daniel et al.
"31,1 |C\S) (native to soothe,,, Africa).
Jusl/eia adhalnda I..: \F28>773. \ F280734: Cultivated.
/;,
00-393 (ARIZ) (native to southern Asia).

elomea I..: AF289770. AF28073I; Cnlliva
nesbcrg. (.auteng. South Africa. Daniel c.
J. externa T. Anders
ed, San Franc
. Daniel s
tive to eastern tropical Africa).
J. sp. 9024. AF289768. AF280720: Madagascar. Fianaranlsoa. Raiioinafana National Park. Daniel 9024
(CAS).
J. sp. 9010: AF289700. AF28<C30: Madagascar. Fianaranlsoa. Ranomafana National Park. Daniel 'Hllli
(CAS).
./. sp. 983: AF289767. AF289728: Madagascar. Masoala
Peninsula, \nUininn I o,e.|. /jhn, ''83 (CAS).
Melarungia galpini, |( Baden) ( Bad. .. \l .".077l>
AF289737: Cullivalcd. Johannesberg, Gauteng.
south \lii.a. Daniel <>3JJ i( \S) (native to South
Africa).
Rungia klossii S. Moore: \l-2il". . . \I2!'.<I. w, dIS)
s gracilts Klotzsch; AF289766. AF289727:

led. San hanoi^n Con-ei wilorv ol Flow.-is.
incise... California. I S. \.. Daniel s.n. [C \^l
to Africa).
/>. , ttiu rslu-rgensis K. Balkwill, NA, AF289725; Witwatersrand National Botanic Cardcn. (.;ml.-n-. South
Africa, Daniel et al. 9357 (CAS).
I), rrsu/unala (Vahl) Jnss.; AF169841. AF063124; U.S.A.
Arizona: Pima County, Santa Catalina Mountains,
Van Devender 84-269 (ARIZ).
I), suberecta (Andre) Bremek.; AF289763. \F2J!>722:
Cultivated. Tucson Botanical Garden. Tucson. Arizona, U.S.A.. McDade 1176 (ARIZ) (native to Uruguay).
I), sp. 9194; AF289764. AK2H9723: Madagascar. Fianarantsoa. Ranomafana National I'.irk. Ih,i.-I '>/<>!
(CAS).
Ilvpoestes arislala R. Br.: AF289765. AF2B9726; (HS)
Cultivated. Mildred I-.. M.illn;i> Botanical Carden.
Los Angeles, California, U.S.A., Daniel s.n. (CAS)
(native to tropical and southern Africa).
//y/-.s7.-> plrvUnslachya Baker; AF169842. AF 167703:
Cultivated. Univ. Arizona. Tucson. Arizona. I .S. \..
McDade 1232 (ARIZ) (nat:
Peristrophe hvs.sopifolia (Bu
\HK:',I2J: Cultivated. \1i
-k X U. B. Sm.; \F289759.
izona. I .S.\.. Star, r.32 I \l!l/l (native to Mexico).
caudata A. Gray; AF169837. AF063134: Mexico. Sonora: near Alamos, Faivre 64 (ARIZ).
comata (I..) Cam.: AF280760. NA: Costa Rica. Heredia:
I.a Selva Biological Station. Faivre 59 (ARIZ).
Hi) nb.; VI U59839, \F(k.3l ;-,. I S.\. Xri/ona:
Pima Countv. Tucson Mountains. Iwi Defender 87307 (ARIZ).
/S.hlldL \F2R976I. NA: Cultivalcd. I
il D

c .;. i \i /.:
askepasma enlhrochlamys Lindau: AF169840.
\ I-'003 I ><r. Cultivated. Wilson Botanical Garden.
, Costa Rica. McDade 253 <|)l KF) (nai South America).
u; AF 169838, AF07066;
(HS) Costa Rica. Alajuela Proi
>erve. Ilaber 707 (MO).
Ani.seanthits puheriiliis
Asystasia gangetica
Asystasia sp. (Daniel 9129)
Brachyslephanus lyallii
i
",,i (inzonua
Telrameriiim lineage
(,,,-.,,
,.,
Darnel tuATci (I iiiil.-iitifinl)

Dicliptera extenta
Dielipterinae
I), resnpinala
I), suberecta
D. sp. (Daniel 9194)
Di.lipleri.uie
Old World "justioioids"
Kcbolium syringifolium
Telrameriiim lineage
Cypsaranlhm nel.sonii
Henna insularis
Isoglossaf sp. [Ik
./. >P. i//A,,, 9ti:i)

Mackaya bella
I'tysiglotti.s pubisepala
Sparlhacanlhiis hoffnu
Sirehlaranllui.s contain
A PHYLOGENETIC ANALYSIS
OF DICOMA CASS. AND
RELATED GENERA
(ASTERACEAE:
CICHORIOIDEAE:
MUTISIEAE) BASED ON
MORPHOLOGICAL AND
ANATOMIC CHARACTERS1
\r.Mis w i
llir -.Tin- Dnomti and the related genera Achymthalamus. Ervlhrorc, Asteraceae). which share a series ol morphological characters of' the
corolla, ray floret epidermis, anther appendages, and style branches. \ matrix of 77 morphological and anatomical
characters was used for the auabsis. The genera Gochnaha and Oh/enburgia were used as outgroups. The topology of
the resulting consensus cladogram suggests that the genus Diroma appears paraphylelic. A clade including IHroni.i
and Pasacriirdixi appears monophyletie with subgroups elearb defined I >\ .1 lame number ol -\ na|)omorplues. These
several genera. The genera Pleiotuxis. Acliyrolliah."
>!mliim form a monophyletie group. Issues relating
specie, groups, are brielb discussed.
Mutisinnc) of Bremer (1994) is considered by this

author to be one of the most difficult groups to ovaluate phylogenetically within the Mutisieae. According to Bremer (1994), it is characterized by its corolla distinctly divided into a narrow tube and wide
wit}
agascar.
Prior to Bremer's (1994) "Dicoma group," similar
groupings had been proposed by Jeffrey (1967) and
Grau (1980). Indeed, Jeffrey considered this group
limb, its non-mutisioid ray floret epidermis pattern.

its acuminate apical anther appendages, and its
<> '* <>* "' '' ""*' (li^"1(t wi,hin the Mutisieae.
Hansen (1991) suggested that most of the genera
mos.h subapualK ,.il..^ stvle branches. It comprises Dicoma itself, with 50 species occurring in
tnbe
tropical Africa, Madagascar, and South Afr.ea. a.l
"''' "'"< f" -;;"<"';''/-. "" <^ epideimd
_
< >.
I loll i:i. 1--
&
1. -
.
11
.
I
f.
'.
'
.
rn
1.
and D. tomentosa Cass, is present , India and Pakistan). Other genera of tins group are Knthmrrphalum Benth. with about 12 species occurring
throughout tropical Africa (particularly tropical
East Africa), Achyrothalamm 0. H.offm. with a single species from Kenya and Tanzania, Pleiotaxis
Steetz with about 25 species occurring throughout
tropical Africa, Pasaccardoa Kuntze with 4 species
,,f
^ *""'P l" m"v'(l trom th<> Mutisieae to the

Cynarear (Carduearl. \U< support ....-h.dcd (a)
a broader limb; (c) bilabiate lb.v\.-rs with uppei

11111
1
_.
1
-ii
1
/
!
. 1: ' .ibsi IIIt lr. r|)l
m ,;,,,,,-,. , ,,,.,, ., are [ong a(, r()il,(1;
|Iuill,M.rt> ,();5): aml ((|) stvll. l)nUK.ht,s Wllh sul).
api<.a| swt.r|)lllg
h.lirs. Karis of al.'s (1992) cladistic

0f the subfamily Cichorioideae indicated
,|,a| }),mu,. Krvthmcephulum, and Pleiotaxis form
monophyletie group within the tribe Mutisieae, in
accordance with traditional views (sec Hoffmann.
1893a; Cabrera, 1977).
ana|ysis
my stay at the Natural History Museum of .Stockholm, to an anonymous reviewer who contributed decisively to improvement of this article, to the keepers of the herbaria mentioned loi the lo;
I study material, to Alfredo Lopez
( I'okio) for the illustrations, and lo i.\n Norman for the Knglish translation of this manuscript.
-' I.aboralorio de Hotanica, h'ai ultade de Farmacia. I niversidade de Santiago. 15706 Santiago de Compostela. < .ali.ia.
ANN. MISSOURI BOT. GAUD.
87: 459-481. 2000.
i 5 Q Q 5 Q Q Q C
111
if= -
II
.1
Is
II
^ E I
--^ 2
--1-:
E M.
ar
'
.=
ill
liittiiJ
I Related Genera
i*
H* 4
l-s
}ll
I I til
tot!
it
ir i 5** t
i Hi? if i
iiiyiLi
i?|ii ? J
i ^11Js t tig
is gi|t|
fell*! ji |;i^
l||lll|l!ll|?|1|ll IffIf
- ~
iJ i
!
"
|1i litfl x ill
tr|!llillll|IIi1illl! mil ilfl
1 11
111
i is jlil % hi
I ii ijij j |:
Jill
III 111 1| I HI
Marginal vascular
-nl.marginal Ise,
(Fig. 3-1 and 3-2)
absent (0) / preser t(l).
Apex of the disc corolla lobes with thick-bundled
veins (0) / without thick-bundled veins (1).
Stamen insertion in disc corolla: at the tube/throat
i (0) / near the corolla base (1).
.->-3)/aeutc|lMr'igs. 5-1 and 5-2).

Sporoderm thick (0) / thin (I).
Pollen smooth to slightly granulate (0) / echinate (1).
IW2I and disc florets aclinomorphic (3).

!2. Marginal florets hermaphroditic (0) / neuter (1).
!3. Corollas as long as or only slighth longer than tl
Disc corolla tube gradu,
abruptly dilates into limb
Disc corolla lobes erect t
Disc floret epidermal cell cuticle ornam.-ntati
tisioid (0) / slighlK transversely oudiilale-sl
nearly smooth (1) / conspicuously longitudina
ate and transversely ondulale ("iiitesliiie-liki
Style branches straight (0) / conspicuously curved (1)

Style branches short (0) (Figs. 6-1 and 6-2) / long (1
(Figs. 6-3 and 6-4).
Stylar sweeping hairs absent (0) / reaching or almos
reaching the bifurcation (1) (Figs. 6-1 and 6-2) / in I
long group not reaching the bifurcation (2) (Figs. 6
4) / in a subapical tuft (3) (Fig. 6-3).
Stylar sweeping hairs of similar length (0) (Fig. (i-l )
longer than the rest (2) (Figs. 6-3 and 6-4).

Disc corolla margins not sclerified (0) / scleri
mh simple
58. Dis
;i(). Cypsela of marginal Morels without rosli

rostrum (1).
()(). Cypsela smooth (0) / conspicuously r
c.s. Cypsela twin hairs simple (0) / twin hairs bifurcate

(1) / absent (2).
()i. Twin hairs all aroun<l the evpsela (0) (Fig. 7-2) / between ribs (1) (Fig. 7-1 and 7-3).
Twin-hair bases not bulbous-glandular (0) / conspieuousK bulbous-glandular (1).
Twin hairs of the cypsela base similar to those of the
other parts of the evpsela (0) / conspicuously enlarged
(>;>.
67.
Cypsela with biseriate glands (0) / without biseriate

glands (1).
Immature testa with similar proportion of needle crystals and square to short-rectangular non-oriented
crystals (0) / with long-rectangular crystals oriented
Mature testa pattern: Gorhnatia type (0) / Erythrocephalum type (1) / Dicoma type (2) / Dicoma welwitschii type (3).
Testa epidermal cells with the lateral and basal walls
strengthened (0) / only the basal walls strengthened
71. Pappus of bristles (0) / scales (1) / bristles and scales

(2) / absent (3).
Pappus bristles seabrid to barbellate (0) / plumose
73. Pappus clement persistent (0) / caducous (1).
tionships w 11tnii Dn-ntna. with the aims of identifying generic and iiilragcncric Mibdivisions and of
t.^r.-sing )\\c \ ll:ll'\ i I the - ll >d y IN m- piv. IOI1-K
proposed by Leasing (1830, 1832), De Candolle
(1838), Harvey (1865), Hoffmann (1893a), Wilson
(1923), and Pope (1991) (see Table 1). Another objective was to obtain preliminary i
tin g. . gi.ipbic I II ii in mil ' M I.lie
species grouj)s wit I
The [ilnlogenelic analysis was based on morpho1' . II. i

i i I. i m il study of specimens from the
BM, C0I, K, M0, and S herbaria. A number of
species of Dicoma were selected as representative
>l the various morphological tvpes present within
this heterogeneous genus as follows. First, the seven species of the group 1 denominate the "D. ses. ip" (see Results) an i<| .i<<ritat i\ < of a
.1 l\ p< observed in a total of 19 species, including D. aura ulala Hutch. & B. L. Burtt,
1
"
weileri S. Moore.
Second, the species D. mccoli/cra \\ ild. and D. ca
pensis Less, are representative of a morphological
Ivpe observed in 7 sp.eies. including D. macrocephala DC, D. cuneneensis Wild., and D. schinzii 0.
II i
Finally, D. anomala Sond., D. aethiopica S.
Ortiz & Rodr. Oubina. and D. montana Schwick.
are representative of a inorpbologie.il tvpe observed
in some 10 species not considered in the present
analysis, including D. galpinii Wilson, D. popeana
S. Ortiz & Rodr. Oubina, and D. somalcnsc S.
7 1.
75. Pappus and involucre of the same length (0) / pappus

overtopping the involucre (1).
7<>. Pappus erect to erect-patent after fruiting (0) / patent
77.
(0) / pappi of marginal florets much longer than those
of disc florets (1) / internal pappus bristles of marginal
florets as long as pappus of disc florets, and external
pappus of disc Morels (2).
While studying African taxa of the Mutisieae

(Asteraceae), particularly Dicoma Cass. (see Ortiz
& Rodrfguez-Oubina, 1994, 1996, 1997; Ortiz et
al., 1998; Rodrfguez-Oubina & Ortiz, 1995, 1997),
I nvesligalrd |ib\ logeuelu l. h;:| -di p> w Itllll D,
coma, and between this genus anil related taxa.
The principal aims of the work reported here
were to investigate the relationships between Dicoma ami other genera and the phylogenetie rela-
genus (see Table 1).

A total of 34 species were included in the study:
the single species of \cli\rotiatlamiis. '2\ species of
Dicoma. 3 species ol Er\liiroi cphalnm. 3 species
ill f'asaccanloa. and 3 specieol Plciotaxis (see
Table 2). I also studied Dicoma anomala Sond., D.
zeyheri Sond., and D. capensis Less, in the held in
South Africa. Gladiopappm vernonioides Humbert
was not included, since I was unable to obtain material of ibis taxon.
A total of 77 morphological characters were studied (see Table 3). For microscopic exaniin Inn llo
ral parts were first boiled in water with a surfactant,
then mounted in Hover's solution |Anderson, V>o\).
\'\w\\ r\ and acheiie sections were cut b\ hand with
razor blades. Some character- inilialK considered
were excluded from tic ai d\- - because they were
the same in all species including outgroups, such
as endothelial cell wall thickening organization
iDotm. i. I<><>:>|. which was always polarized, and

cypsela vein union (Karis et al., 1992), which was
always .il tin- has*-. Sonic oi these eli;ir;i. lei-. reCharacter 8. Many of the species studied cominonlv show more or less braclilorm leaves.
denominated "subtending leaves" (Pop.. 1'(>I.
1992), at the hase of the capitula.
Character 13. Many of the species studied
have two dark stupes running along the phyllaries.
Character 14. Examination of cross sections of
the ph\ Maries allows loin moiphological types to be
distinguished, most notablv on the basis of the arrangement of selerenehymal fibers. In the first type,
the selerenehymal Iihers lorin a more or less continuous mass occupying the inner pari oi the phvllary (Fig. 1-1). In the second t\pc the selerenehymal fibers, though likewise situated in the central
part of the phyllarv. I
i eh arlv distinct groups
separated by a very lax parenchyma, which appears
to be aeriferous (Fig. 1-2). In the third type, the
selerenehymal Iihers are concentrated toward the
abaxial lace of the phvllarv: in the . entei. whii h is
basically occupied by parenchyma, there are several vascular bundles reinforced with selerenehy-
mal Iihers iFig. 1-3. 1-1). In the fourth type, the

nujorih oi selerenehymal Iihers ate eilhei on the
adaxial lace or in the midnh ol tin abaxial lace.
where they protect the vascular bundles (Fig. 1-5).
Character 21. Dicoma carbonaria, and to lesser extent I). o/i'dc/nlhi. have capitula in which all
florets arc zygomorphic, with one of the corolla
lobes separated from the others by a much deeper
incision and without an expanded limb: this morphological type seems transitional between the actinomorphie and the huulale type arid is similar to
ily Barnadesioideae, such as Chuquiragu Jiiss.. /),/syphyllum Kunth, and Schlechtendahlni less.
(Hoffmann. l'MMa; Cabrera, 1977; Bremer, 1991).
""True ray" florets have n<> adaxial lobes and a 3lobed lamina.
Character 26. This character was initially
studied in ray florets (Baag0e, 1977, 1978), but in
my opinion is also informative for species thai have
disc florets only. Indeed, Hansen (1991) studied
of species of the various genera considered in the
present study (despite the lad thai the study in
question centers on tav florets,. This character has
d" respectively, though
likl
1992) is equivalent to Hansen's "rugose pattern of
longitudinal hands" (Hansen, 1991). In the characterization of GOCIUIHIKI and \rtivrntlmlamiis I
have followed Hansen's (1991) approach, classifylese two genera as "muti-
ypologies was not clearly defined i

Character 28. Some species have long twin
glandular hairs with a small apical gland on the
corolla (see Kans et al., 1992: 418, fig. 4H). In the
rest of the species considered the disc corolla hairs
Figure 6.
Apical part t
s bifurralion (Oleoma sessiliflom Han.
with sweeping hairs in a subapical tuft, with a subI il),, untu Ixmpueolemis Buscal. & Vluselil.. Beckett
hairs not reaching the bifurcation, these with a subsweeping hairs conspiciiousb longer than the i est (Oleoma tomentosa, Nordenstam 2454 (S)). SH:
are "short glandu n tia;r-" M!1: ;i large apical gland

(see Kans et al., 1992: 418, fig. 41). Rarelv (either
in the first or second type) "twin hairs" are present
that arc ha>i. alK similar to the non-mvxogenic
short ovoid twin 'hairs of Karis et al. (1992: 418,
liii. 18). win. h ate \er\ short and which lack a
conspicuous apical gland.
Character 29. Disc corolla simple hairs are
long simple bans uith one oi luo basal cells (see
Karis et al., 1992: 419, fig. 5E).
Character 32. The marginal vascular tissue of
the lobes of the corolla of disc florets is thick in
some taxa, made up <f mum wssels und surrounded h\ sclcrctichym.il libers (Fig. 3d und 3-2). In
junction. In D. carbonaria and D. oleaefolia, by

contrast, the stamen filaments are inserted practically at the base of the corolla. The prescme ,.| luo
clearly distinct states is not in agreement with Karis
(1993), who reported that this character varies little
within each of the tribes ,,f the subfamily Asteroideae (except in the tribe Astereae) and is thus of
comprised of lew.-1 ves-rls and without se|.rendumal fibers (Fig. 3-3 and 3-4).
Character 34. Some species show accessory
veins of variable length in the corolla lobes, running more or les- p.ndid !> ibe litargmul/suhmar-
tions, while the ramifications of the rest of the anther tail are alw,
,, < I
3-2 and 5-3). In
other taxa, however, such apical ramifications are
Character 35. In s
isc corolla lobes fo
ense bundle (Fig. 4) (see Karis et al., 199
Character 36. In most of the species -
Character 44. Dicoma carbonaria and D.

oleaefolia share an mlen-lnm , haracteristic. the
tails ol adjacent pans ol anthers being joined, with
their ramifications or hairs interwoven. The anthers
oi th< remaining species arc clcarh separated.
Character 45. In many taxa the apices of the
absent (Fig. 5-1).

Character 55. In several taxa the stylar sweeping hairs reach (or almost reach, or extend beyond)
the point of bifurcation of the style branches. In
most of the other species considered, the stylar
sweeping hairs form a short subapical lull thai
Hansen (1991) and Bremer (1994) considered characteristic of the species of ibe "Dicoma group." In
i Botanical Garden
h-
CD
DL
tomrntosd and I), uchi ilschii, a third pal

observed: the sweeping hairs cxlcml from
) the apex toward the bifurcation, but do not
Character 62. Many of the studied taxa have

unicellular < yps. hi-siufa
_> i
iiitaininga resinous material. These may be located between the
ribs on the rib walls (Fig. 7-3), between the ribs in
ill. intercostal gr..o\t s. M i:n lain- I cairum HI- :
ei am n : I I hi- < vpsela (Fig. 7-1), as in the D. car)>,>,/>:>i ^loiip. huott.'i :>,;<: <>^: -due-,-, i i-inplm.
<>g\ inlermediate between types 1 and 2, and was
coded as inapplicable for this character.
Character 63. Simple twin hairs have the two
Is joini
i
i i
ii'- have the two
cells separated (Karis et al., 1992: 418, fig. 4A).
Character 65. In some species the eypsela twin
hairs have a conspi. i i
i Hi . i- _ n In! n I
In other species the base of the eypsela twin hairs
may he sonu ulia
i.l us hu i- i
. i J u '
Character 66. In Pasaccardoa grantii and P.
jeffreyi, the twin hairs of the lower part of the cypcies all hairs ..I I he . vpsela are similar.
Character 67. Biseriate glands are composed
of two rows of ( IIi
i
II
ril apical head.
.mil ncciii in llie eypselas of many nf ihe taxa anal\/ei|. In man) cases these arc not easy to see and
often are situated between the siiperficia LI.CT:(sec character 62).
Character 68. Subepidermal calcium oxalate
crystals an- observed in the immature testa of all
species. They arc siibsequentlj hidden from view
h\ the epidermis of the mature tesla. In some species needle-shaped crystals and square to shorticct.iii-.ulai' crystals, without uniform orientation.
are present in roughly equal proportion (Fig. ''-Ii.
In others, by contrast, almost all the crystals are
narrow I\ rectangular and oriented in the same direction (Fig. 9-2).
Character 69. The first character state corresponds to the tesla type defined by Grau (1980) for
Cochiuititi Itesta with lateral and basal walls of the
epidermal cells strengthened). Similar but not identical morphologies are observed in Pascu ardoa
grantii, P. jeffreyi, and some species of Dicoma: in
these cases the testa morphology is simi
Gochnatia type, but the cells of the epidermis are
ol irregular shape, not linear. The second character
state is the Erythrocephalum type as defined by
Grau (1980); in addition to Erythrocephalum, the
species of \ch\iolluihimus and Pleiotaxis fall into
this category (basal walls of the epidermal cells of
cells a lacunose appearance in I
by the same author (basal walls of the epidermal

cells of the testa strengthened with ribs). The fourth
eliaiaetet slate, observed in I), ncl'icitsfhii and P.
baumii, is very sinn
I in die other
species of Pasaccardoa, except that the epidermal
cells of the testa are traversed by thick bands. We
have not been al>l<
' >
in ill. (>
-..
i
1 i nil
i iiil.nK. k u-
is et al. (1992) were unable to determine whether

or not the testa of the species of this genus is "collapsed." The testas of the two species of the D.
carbonaria group show a morpholog\ similar to
Grau's (1980) Perezia type (testa with epidermal
cells not stn r
I
h lud\ ol additional
m il< rial is n< < < ssary to confirm this.
Character 70. In some species the lateral and
|!3 en
38*3
sB 23 J
E E 3
HH
M H
61 ft ft 1)
2
1H
tna ^
&kl "
HI
'H o mm
OI
o a-H
-H +J BI
o J
<U3Ea54J-Hm-HOC<UHC(0a)
* -H -H -H TJ T) TJ -H
[) H
it O 1) -H -H
T) -H -H
-H
OT3-H<UCn(0O(U
C -^ ft k II
II
D 11 H
j3<U4J4J4J>,-H-H-Hrt<didOOOOOOOOOOOOOOOOOOOOOOOO
slash) and c/i bootstrap support (after the slash). I.cllc,- in parciilhr-..^ alter Dirom
which each species belongs. Sections proposed by Hoffman (Ici'Wa) (before the slash): S. Stcirocoma; H. Rliigiothamih
K. Kiuiuoma; VI, Shuledium; H. Ilwhstettcriu; I's. Psiloroma: H. UrarliMirlitirmiim: I'l. I'l, !,>,,,ma. Sections propos
basal walls of the epidermal cells of the testa are

strengthened with a highly characteristic morphology, U-shaped in cross section and similar to that
of Grau's (1980) (,<>ri)>>, nut -uijuoiip. In the remaining species only the basal walls arc thickened
with ribs.
Character 71. I'
lisent in Achyrothalamus. In the n i i mi
, i. i - I..MI d
by rather fine brisl I
speeies oi Dicoma
i
in l>
bangueolensis and D. tomentosa, or by scales only
- i i ',t , . phnhin ! . >Ioa ">,, !>
witschii, D. spinosa, and D. relhanioidcs.
Character 73. Erythrocephalum has a pappus
of narrow caducous scales, while in all other species considered the pappus is persistent.
Character 77. In most oft!
p<
n
the program PAUP* 4.0 (Swofford, 1998). Cladograms were gen i

juristic search with
the TBR (tree Insect ion-reconnection) branchswapping algorithm with random additions (100
replicates). Support values for each clade were obtained by jackknife analysis (100 replicates) (Farris
et al., 1996) and bootstrap analysis (Kelsenstein.
I . > - i
jhi
1 mis. 1969) was perins where the relai I
i i i
haracters was reduced. All multistate characters were treated as
ilii
I i
vcre coded as polymorphic for some l< nil In the data matrix, unknown character states were indicated with "?",
and inapplicable character states were indicated
with a dash.
the pappi of th
that make up the
capitulum are all of similar length. In Dicoma niccolifera and D <<//
florets are much longer than those <>l the di>< Horets. In D. elegans, the internal pappus bristles of
the marginal florets are as long as the pappus of
the disc florets, while the external pappus bristles
of the maiginal florets are much longer than the
pappus of the disc florets.
Polarization of ch
rmined by the
outgroup < ompjn-< l mi the d ON vt i
1
i >
trous & Wheeler, 1981; Maddison et al., 1984), using Gochnatitt Kunll
'
. a Less, as outgrou
Id I
HIII
In
I. \] ii-i i
in Karis et al.'s i I' '_'
i
\ are basal to
the taxa included in the ingroup. Gochnatia is a
heterogeneous genus with nearly 68 species (Bremer, 1994), mostly from the Americas, though also
Asia. For outgroup u
I led ."> species

of Goclmalia. representatives of three of the five
sections of the genus (G. amplexifolia (Gardner) Cabrera, G. attenuata (Britton) Jervis & Alain, G. cor,',(.' I
'
|. i'.i- cv
Alain, and G. picam'nc (I >\, \ limeucz) with simila
habit to those of the Dicoma group. Oldenburgia i
a genus of four species endemic to the Cape area
in South Africa, from which three species [0. grandis (Thunb.) Baill., 0. papionum DC, and O. paradoxa Less.) were selected.
Characters with onlv two stales of which one was
autapomorphic were not included in llie analysis.
Wagner parsimony analysis of the data matrix
(Table 4) was performed on a PC with the aid of
RESULTS
I
ilfsis Yielded six equally most
p
grains, each 186 steps long,
with a consistency index (CI) of 0.513, and a retention index (RI) of 0.82, including in both cases
the only uninformative character of the matrix. The
si
oi differences. One
of the six cladograms is shown in Figure 11.
Analysis with successive weighting gave two
I
r
I.I
il majoi-c hide topology to the six equally most parsimonious cladograms (and the corresponding strict consensus
i. i I
i ,
i I out successive weighting. However, the two successive-weighting cladograms differed from the no-weighting strict consensus tree in
the internal topology of the major clades.
In the strict consensus tree (Fig. 10), the first
division split (a) the first cdade. comprising the
genera Pleiotaxis, Achyrothalamus, and Erythrocephalum, from (b) the genera Dicoma and Pasaccardoa. The second division split (a) the Mad.i'_a-. in endemics I), carbonaria and D.
Dicoma and Pasaccardoa. The third division split

(a) the seven species of the Dicoma sections Pterocoma DC, Maclcdium Less., and PSHIH-OIIHI
Harvey, hereinafter referred to as the D. sessiflora
group, from (b) the remaining species oi Dicoma
plus the three species of Pasaccardoa. The fourth
division gave the last two major clades, one comprisii
'/ , ,
i
d the Pasaccardoa
eler clislriluilioii. diameter iiunibering follow?
species, the other comprising the species 1 refer

to as the D. tomentosa group.
In general, the live major .lades revealed by the
analvsis are ade(|iiaiel\ ~u|>p.>i (. d In jackkitife ual
bootstrap values isee Fig. 10), and the results of

the analysis can therefore he considered sufficiently
reliable to provide a basis for elu. idalimi of phvloêiie! i> i > I . I : <y<-:, s - \i\:,.\i^ ilie genera and >pe-
DISCISSION
The results of the analysis reported here contradict those of Karis et al. (1992), in that Erythro, ,y../' //,;<.. ai .| i'lcinia ,, - pp. I :;<*,!.'.,::;,,*,, ini| /'; >//,-, -/,/., ///,; const il III.- a
ni(iiio|ili\lctic group (see Fig. 10), the members of
which share a mimliei ol apomnrplu. i haraelers.
some ol which are exclusive (such as anthei tails
with siihroimded lo subacute apex, or slvle branches separali d) \\ i:l
h
mi
ai il ,*'";, <,,!<> \<> '.>; i-ai h l>< \ aiaphv Idle. Ncvcrllicles-. < oiiliinialioii ol llii- would require a dadistic
anab-)- ol these three genera alone, with considcralion of all or most of the species indue d ,\ilh I
them; the present study Ionised on the species ol
Dicoma and on the characters relevant to the taxonom\ ol this genus. Such an analysis should try
to identify other characters that although of little
diagnostic value in the present study might be of
value in an analysis of these three genera alone.
Despite these reservations, it is of interest that
\. I,M.>!>;.>!,i<:r- aid /,'' >:h:.i, > i-'ht'-itt, -houe.l cub
minor differences (characters 16, 19, 26, 31, and
71); of these characters, die absence of a pappus
(character 71) is the most widely used to distingm-li between \iii\i,>l!iiii(i!ini\ and /'.'/ \lhroccf>l>a!
urn I which has a caducous pappus). In this connection, our obsi
lli
are present on the e\ p-, I , d b /, t ".//.,,/'<,;*. aid
haracl. i stale consul, r. d apomoiphic. as observed

in D .,;''.'.:/'..' .aid /> ,'/.,,-,/,.,',./ dm ild in a w ider context probably be viewed as a reversion to a
more primitive type; like Cabrera (1959), Bremer
(1987), and Karis et al. (1992), I consider the most
primilive stat.' to be that in which all florets are
aetinomorphic] (character state 21.2), (b) disc corollas much long, i lli ii itc. >l i > IL*.'.. I i. (c) disc
corolla veins separated as far as the corolla base
(31.2), (d) stamens inserted close to the base of the
naves ol die corolla remain
separated to the base of corolla, as in certain species ol th. genu- s
I'di.i Ihdi
lands (Carlquist, 1957; Bremer, 1994), one of the
ems! pi ihilc get . i, ..i posslbb the mosl primitive genus (Hansen. 1991; Karis et al., 1992; Bremer, 1993a, b, 1994) of the Mutisieae] (36.1), (e)
anther projected beyond the corolla. (I) anthei lads
ol couiigiioiis aith.-rs joined (41.1), (g) style with
lour veins i 1'*. 1 ). (In superb, lal c\|)scla glands disposed in a continuous layer all around the cypscla
(62.1), (i) pappus much longer than involucre
(75. I ). and (j) pappu- brisl r- | al.nl .it 1. : find ng
(76.1). All of these s\ napoinoipluc characters, some
rel. ( ng to -e|e\ .ml a-| eels ol (lo| I lli. I ; ! ..In- \. in
gether with a sen.
>! plosiomoiphic characters not
observed in the remaining species of Dicoma (such
as the presence ol resin duct-, the absence ol stardiapcd c.ilcuun oxalate crystals in sub.pidei mal
cells of the corolla, and the presence of narrow style
blanch nerves), support the consideration of the I),
carbonaria group as a clearly di-lui.i .lade, and
raise the possibility dial these I wo arborescent
M dagas m i ndemii - -1 1.1 b. cn-id. i. .1 a- a
separate genus. This would entail resurrecting the
g. I is ( '!i,isc!iii ^ Mo. |. . il.-s. I died b> d.ls aillhot
that these hairs are apparently identical to those

previously considered to be diagnostic of Er\thio
cephalum and Ihaloseris (Karis et al., 1992). The
presence ol these halt- in I. n lolliaiamus do. - nol
seem lo have been taken into account when deciding to consider this taxon as a separate genus, prvsuuiabb because they have nol previousb been detected: there is no mention of them in the original
description of the genus (Hoffmann, 1893b), and
Bremer (1994) described the cvpselas of Achyroth-
(M. i. 1906) for <

i
(D. carbonaria). I
am unaware of other species of Dicoma with floral
those observed in the D. carin of these characters, as men-
The clade comprising Dicoma carbonaria and D.

oleaefolia (the "/). carbonaria group") (see Fig. 11)
.> w. II define : and c u -eparaled from llie remaining sp, eies ol Di< >../ Impel lanl apoii ..rplii.
ehaiacler stales shared b\ these species include (a)
c ipiliilniii :<< ;dl floiels /v; .n: i| In. jsince ill* sub
lainib I'.amad. - aide: c ;s .,ne of the mosl priruil \<
group- within the \sleraocae (Bremer, 1994), the
s
Mi
>j>adus (see Cabrera, 1977; Bremer, 1994). This raises the possible , il ai die i. . Imnsli p bclw<-. n da \h -an Mi,
tisieae and the more primitive South American
I i
on
this 11 ib. i
I if.- . lo-. i than
is currently admitted. This would be consistent with
the hypothesis of Bremer (1993a, b, 1994), whereby
the Asian species of Mutisieae were derived from
but without expanded limb, stamens inserted dose

to the base of the corolla, abundant long simple
bans on llie corolla surface). Th.se characters suggesl a relationship with the g.nera of the Barnadesioideae (nolal
('.buquiraga, and
"V ):'.. Ii,', ;;-i,:*n!,,,. .md the llkewis, pnualm ^. M 11 ll
the South American species as a result of westward

spread across the Pacific. It is also possible that
the primitive characteristics of the D. carbonaria
group reflect the isolation and protection from competition that has aff<
I
in ol many other plant and animal
n Mad gas. ar. Of the
Din una species not
i i
'
. .
the only taxon showing some degree of external
morphological similarity to the species of the D.
carbonaria group is D. incana (Bak.) 0. Hoffm.,
likcwisi irbores .
agascar; note, however, that floral morphology characters in this species le IT. llli
i n M| palleni lor
the genus.
The next clade (see Fig. 11) comprises two
clades, one of them including the seven species
that I refer to as th<
.p lh l 1111-
eluding innermost phyllaries more or less entirely

(17.1), and corolla with long twin glanill i i i
2H.lL Oil
i
i
(a, rharaeters
are homoplastic (CI < 1), due either to parallel
, marginal veins of
lal or almost marginal position, base of the twin hairs of the cypsela
verv ei.n-.pi. noii-l, 1 > i! I < . i . i ' lai ..i ton MI
sions to the plesiomorphic state (e.g., innermost
phyllaries shorter than the contiguous outer series,
IKI antrorse branches at the apex of the anther tails).
Plesioinorphie characters shared b\ the memberof this group include marginal veins of the disc
corolla lobes broad e...>,<;. ,|. (
ib> absent or
very slender (6O.O1 mil twin hairs a I
i
cypsela (64.0). Conn n In i ih it I
!>
group constitutes a distinct entity within Dicoma,
or possibly a separate genus, will require a more
id< d in ilysi- i oi iii I I i species in the
group. It is worth noting that some of the species
of this group are more adapted to woodland con11 il ions than those of the D. lomcntnsa group Iwlnef
together with D. welwitschii and Pasaccardoa, constitutes its sister group); the species of the D. tomentosa group, though sometimes occurring in
woodland habitats, are generally better adapted to
dry, open sites, and even sub-desert or desert habitats (see Lisowski, 1991; Pope, 1992).
The members of this latter clade (see Fig. 1 1)
share a number of apomorphic characters including
(a) a conspicuous phyllary midrib (12.1), (b) disc
corolla lobes recurved at apex [the corolla lobes
have a recurved apex, with the apices of the anthers
and the pistil exserted; this may reflect the adaplalion of most sp.-.ies nl 'this -roup to d< -.. ri .. -ub
desert environ in- .

n h i pollinators are very
scarce, so that there is selection in favor of at least
partial anemophily (see Whitehead, 1969; Lane,
1996)] (25.1), (c) cypsela ribs conspicuously strong
(60.1), (d) cypsela with twin hairs between the ribs
(as also observed in the D. carbonaria group, and
uiabK i
_ parallel evolution) (64.1),
ai I
dermal layer of the
testa) with long-rectangular crystals oriented in the
same direction (<.'!. I i I li - :i.>up splits into two
I idi - on. in which I). in-licitschii appears as a
sister group of the three species of Pasaccardoa,
and anolher comprising the D. tomentosa group.
The latter might be referred to as Dicoma s. str.,
since it contaii
Ivpi -|
- ol
the genus.
In view ol the topology of the cladogram (Figs.
10-12), one possible approach would be to transfer
the species of the genus l'<isaccard<ia to Dicoma.
Alternatively, Pasaccardoa could be maintained, in
view of its various synapomorphic characters, one
non-homoplastic (cypsela of the marginal florets
with rostrum} and others shared with oth. r -pe. i<>
but not with the members of the D. tomentosa group
(disc corolla tube abruptly dilating into limb, inargin of the disc corolla lobes conspicuously sclerified, no antrorse branches at the apex of the anther
tad
pappu- ..I -< d< s) I'ltsm < ardoa also has a
number oi relt
|
.
phies including presenee of a cylindrical disc floret cypsela, and Gochnatia-xype testa. This view is supported by the fact
that 1). icchcitschii. which the analysis indi. aled to
be a sister group to Pasaccardoa, shows a number
ol character states different from those of the D.
i
n
.hie (phyllary seler. in h\mal libers , onccntralcd on the abaxial face,
margin of the lobes of the disc corollas conspicuously sclerihed. absence of antrorse branches at the
apex of the anther tails, testa of D. lcchntsclui t\pe.
pappus of scales) and some plesiomorphic (eapitulum wider than 20 mm, absence of dark stripes
a ion:, the ph\ llan.-s. and Literal and basal walls ol
testal epidermal cells strengthened). Some of these
characters are shared with the species of Pasaccardoa. However, the inclusion of D. ueluitschii
within Pasaccardoa does not seem to be justifiable.
in view of the marked differences with respei I to
the species of this genus, notably P. grantii and P.
jeffrcyi. These two species, in addition to P. procurnbens (not included in the present analysis), appear to form a highly homogeneous group, with exelusive synapomorphic characters (such as twin
hairs of the cypsela base conspicuously enlarged.
and cypsela surface glands positioned between the
-ibs iii tin iritereosla IM-.-OM--) mdclhi pen,o.|,>i
florets, marginal florets tii-ut.-r. and cvpsela of the

Miaiji.iii.il florets .
witsc/iii shows a series of apomorphic characters
Anderson, L E. 1954. Hoy,
including apex of the disc corolla lobe without
(,
^J'}"]
' ,
,,
:.; the
thick-bundled veins, disc Morel cvpsela obconie.

and testa of D. weluits
I
domain may
, 1(lll(ll).l| |'y | |> | ;<), \ || Heywood, J.

horned I*. I.. Turner (editors). The Biology art
thus indicate that D. welwitschii (from the central

plateaus ol Angola, and also present in Z<
islr
distinct genus. Nevertheless, this possibilil

have to be confirmed by an analysis including all,
oi u.ailv all, species of Dicoma.
Of the previously proposed sections of the
Dicoma, Dimorphae and Barbellatae of Wilson
(1923) are clearly paraphyletic (see Table 1, Figs.
10, 11). Considering the sections accepted by Hoffmann (1893a), the results of the present analysis
/
.
i n
i
i
an m I- >i l
. i i- * i . I ' i... ,' ,. .,.,.":
Baker (D. nachtigalil) \!,n
|C. <s I DC. {D.
spinosa and D. relhanioides), and Pterocoma DC.
>
<)f l h
iposi,ae
. , 5
- ';
1078. Taxonoinie
Aca dern c Pre
/f:
ieae. ami S. ,lt < iot . . Boi. Tidsskr. 72: 125-174.

- : _' 11 > j ,
tati\lf'th7ee^
436-445.
1W.U. Inlereontinental relationships of African
a,ul Sm,,h
American Arteracea
1
graphic analysis. Pp. KH !>' ! I* Coldblatl (e.lltor).
| , | , , ,| K<-latioiis.hips belw<
\menca. Vile Univ. Press. New
1994. Asteraceae. Clad
(sect. Plumosae Wilson) (D. sessUiflora, D. zeyhen,

and D. saligna).
Other sections, such as Steirocoma DC. (D.
pensis and D. niccolifera, but not D. elegans) and
Rhigiothamnus (Less.) DC. (D. picta and D. fruticosa), may be t
plivl. i
lm.never, and apart
^^^^^3"^
Cabrera. \. I.. 1959. Revision of the genu- l>
A >
(Coinpo>ilae|. Kexisla \1,i. |.a Plata. Seee. Bol. 9: 21-
J monotypic sections Hochstetleria (DC.) 0.

D. schimperi) and Eudicoma DC. (D. to, the species of my D. tomentosa group do
,
.
, , .
4
r
:ar to form coherent monophylet.c groups
Candolle. \ P d( . 1838 Prodromus systematic naturalis

regi vegetabilis, Vol. 7. Treuttel & Wiirtz, Paris.
^'.Iquist. * 1>57. Anatomy of the Guyana Mutisieae.
Mem. New Vuk Bol. (.aid.1'; Ill 1.0.
^^ K j ,%2 ^ fibn|U8 |aver jn ,. e amhers of
le to any ol the sections previously de-
<;()m|,-,i. Vw PI.M.,1 I.I 150-153.

Eldenas, P. & A. A. Amlerberg. 1000. \ eladislie analysis
,.. nvpomes.,c ma, u.ese pxecur'"" " 'I emmoiphi.- I.IXU with
(such as >. spinosa,
Z). relhanioides, D. grandidieri, and Z). cana). The
remaining species of the D. sessiliflora group, with
P>7.. Muiisieae >\siematie reuew. Pp.

H. Heywood. J-B. Harborne K H. I.. Tun
klune. P(Mo. Par-imoin |a. kkiiilmg outperforms neighbor-joining. Cladistics 12(2): 09-124.
, ,,,.,- (,,.,,. |,mils ,,, |0,,,||r>:
\ approach using ihr b strap. Evolution 3): 783
791.
Crau, J. 1980. Die lesta der Mutisieae uml ihre sysieF(.|st.ns|(.m
'"^X^t^""'
Mi
"- "'"
Sl
""'
Mu
'h
scarcely coriaceous, scarcely spiny, and more or

less broad leaves {!>.
,
,
.*' ,iligna. and D.
zeyheri) probably originated from that lineage in adaptation to moistet. shadier conditions. The origin
HailM.~
of this group, and of the genus as a whole, would

thus appear to have been in Madagascar and southem Africa, as found by Eldenas and Andenberg
1893a. Tubiflorae-Mutisieae. Pp 333-350

in H. C. A. Engler & K. A. K. Prantl. Die Natiirli
l>lla,./..-,,lamilien 4(5). W. Englenu
Cornpositae almanac. I. Tribus !
. Svst. 15: 530-517.
Hu.nbert, H.7963. Flora de Madagascar et des Comores.
(1996) for the genus Anisopappus (which

ilar distribution and ecology to Dicoma). On this
hypothesis, the remaining species of the
M \~I001. ||lv|ogrnetics studies in Composiiae

tribe Mutisieae. Opera Bot. 109: 1-50.
. ^- "^ I'-""; < ;
;' " 'V- 44-530 in
Volume 87, Number 4

2000
Ortiz
Oleoma and Related Genera
481
d'Histoire Naturelle. I.aboraloire fie Phanerogamic. ParJ. Bot. 16: 277-2!i 1.

Jeffrey, C. 1967. Notes on Compositae. II. The Mutisieae
in East Tropical Africa. Kew Bull. 21: 177-224.
tion. PI. Syst. Evol. 186: 69-93.

. M. Kallersjo & K. Bremer. 1992. Plnlogeneiic
iBot. Card. 79:416127.
Lane. \I. . 1996. Pollination biolog\ of Compo^tac Pp.
61-71 in P. 1). S. Caligari & I), j. N. Hind (editors),
"
"I
l|
>
II
'"
'
ill
tl
'in
||,l:
i,..
|{o\al Bolanie (hardens, Kew.

sing. C. F. 1830. The Synanthereis herbarii Begnii Bei
i.-a.-l. Wdic J. Bot. 16: 583-584.

.
& M. Tadesse. 1998. A taxonnmic revision of Dicoma (Asteraceae: Cichorioideae: Mutisieae)
440-459.
Pope. (',. V. 1991. Notes on Dicoma Cass. (Compositae).
Kew Bull. 46: 699-709.
. 1992. Flora Zambesiaca, vol. 6. part 1. Flora
Onhina, J. & S. Ortiz. 1995. Two new species
Linn. See. 119: 59-64.
&
. 1997. A new species of Pleiolaxis
-n.i
"
"
"-"-
'
"I
'
'
lot, Berlin.
991. I.es \steraceae dans la Flore d'Afrique
477^179.
Nevcns. P. k PO
i ., i
,...uil\ of character
Suoifonl. I). L. 1998. PAUP*. Phylogenetic Analysis I s 'I

1 'ii\ I'.in.l olllrl inethodsl. \riHiin 1. Nnaiici
Haddison, W. P., M. J. Donoghue & D. R. Maddis.
1984. Outgroup analysis and parsimony. Syst. Zool.
83-103.
Watrous, L. E. & 0. D. Wheeler. 1681. The ,
lental considerations.
Evolution 23: 28-35.
genus Dicoma. Bull.
Misc. Inform. Kew 1923: .
THE EVOLUTION OF
NON-CODING CHLOROPLAST
DNA AND ITS APPLICATION
IN PLANT SYSTEMATICS'
sliand mispairiiig: (2) insertions and deletions linked mill sccondaiv

with hairpins and stem-loop structures: (4) localized or extraregional ii
substitutions. These tun1.it ion- -rem In lie largely a I'unetion ol sei|ii.
hoinoplasious in a parsimony topology; therefore, mutations in non-eo.
seiibed here a- slrueliiied. nomandom. and non-iii(lepi-nileiil events. I
..II a eolleetive under.
ling ol genie l>\ \ evolution and may
gnment and homology ass
.lotion for such aspects of phvlogem estima
i ol mdels as phylogenetic eharaeters, and
There is growing interest in comparative analysis

:.l ll. in . oiling , [llomplusl Ir.e.fi ending c pi >\ \ I sr
quences for plant -\-lemaln -Indies at low taxoliolllie levels. Iv. < >gn i 11..; >l ill. limitalini
I ni:
ing (genie) DNA for resolving
I
-dn
il tin >
levels itispir. d
and uiteigenie spacers lor pliy logenetic utility. Unit premise that
non coding unions . -.pen.-nee limited or no selective pressure and are likely to evolve at rates latin pa
tig those of genie regions (e.g., Curtis &
Clegg, 1984; Wolfe et al., 1987; Palmer, 1987,
1991; Olmstead & Palmer, 1994; Bohle et al.
I'KM). There was also an expectation thai non-cod-
stematies studies currently in progress include a

olei nlai coiiipoiient ol coinparal ive analysis ol
m-eoding cpDNA sequences. A considei il-h
nount of work already puhlished has d.inonslral1 the potential ph\ log.-nelic utility ol discrete rion-
omments on an earlier version o

ir review of the manuscript: Victoria Hollowell for h
sightful comments contributed to the clarity
-Centre for Plant Biodiversity Research. \u
tralia. Second affili
t.kelchneKo'pi.csir.
, i, u;i... ;;;..
rodlllg teg|:>l> 111 '!
;-l||.,i ,|, ,|
I f i.
Unl.-tniV
spacer (e.g., Gielly & Taberlet, 1994; Mes & t'Hart,

1994; van Ham et al., 1994; Sang et al., 1997; Cros
et al., 1998; Bayer & Starr, 1998), the trnT-trnh
spacer (Bohle et al., 1994, 1997; Small et al.,
1998), the rpoA-petD and rpsll-rpoA spacers (Peterson & Seberg, 1997), the atpB-rbcL spacer (Golenberg et al., 1993; Hodges & Arnold, 1994; Natali et al., 1995; Samuel et al., 1997; Savolainen et
al., 1997; Setoguchi et al., 1997; Hoot & Douglas,
1998), the rbcL-psal spacer (Morton & Clegg,
1993), the psbA-trnH spacer (Aldrich et al., 1988;
Sang et al., 1997), the accD-psal spacer (Small et
al., 1998), the rpll6-rplU and rps8-rplU spacers
(Wolfson et al., 1991), the intron surrounding rnulk
(Johnson & Soltis, 1994), the rpoCl intron (Downie
et al., 1996a, 1996b; Asmussen & Liston, 1998;
Downie et al., 1998), the rp/16 intron (Jordan et al.,
1996; Kelchner, 1996; Kelchner & Clark, 1997;
Schnabel & Wendel, 1998; Baum et al., 1998;
Small et al., 1998), the trnL intron (Sang et al.,
1997; Bayer & Starr, 1998; Kajita et al., 1998; Bay-
ideas in this paper,

ium, CSIRO Plant Industry. C.I'.O. Bo>
of Botany and /oology. The /
er et al., 2000), the rpsl6 intron (Liden et al., 19

Oxelman et al., 1997), and the ndhk intron (Sn
et al., 1998).
The literature above not only reveals profoi
alignment possibiliti
(indels), regions of ]
mology assessment i
ami llit < .innti . <>t ,. al ed "hot spots" of inferred excessive mutation, frequently to the point
of saturation ana loss id phylogeuelic signal I1-...
best to proceed with the phylogenetic analysis <>l
such regions should b. a lopic of. onsidcrable concern (see Golenberg et al., 1993; Downie et al.,
1996a; Kelchner & Clark, 1997; Sang et al., 1997;
Downie et al., 1998).
ending regions .:!' the < hloroplast is tar more complex ihau pt.-\M.u-l\ Mipp.i-e.l l'...|h uitioii^ ami
intergenic spacers are thought to embody a considciahle degree ol -aanicrie.- sir iclure. somelimes m
a manner similar to that of ribosomal DNA (rDNA).
_
regionalized se-
events. Sequence-dii
events may persist as "inula
,
n
I
chner, 1996; Kelchner & Clark, 1997), dramaticallossibility of reversal or parallel
parative sequence aiiah-ibased largely on observational comparative stu

of coding sequence data. Considering that these a
today's commonly employed tools for phylogeny t
timation based on DNA sequences, there has be
as yet remarkably 1
sequence data
i-coding DNA. Comparative studies
oi' non-coding cpDNA sequences during n
decade in particular (e.g., Palmer, 1985; Blasko et
al., 1988; vom Stein & Hatchel, 1988; Wolfson et
al., 1991; Golenberg et al., 1993; Gielly & Taberlet,
1994; Morton, 1995a; Downie et al., 1996a; Kelchner & Wendel, 1996; Kelchner & Clark, 1997;
Sang et al., 1997) have allowed inference of specific underlying mutational mechanis s cespnns
bin lor generating si quence diversity in non-coding

regions of the chloroplast genome. Unfortunately,
these m< < hauisne- an nil. :i nnnked. bill 'arch in
corporated, into the analysis.
Recognition of the potential of structured molecnon-coding cpDNA regions to imbelieve, critical for the
pment of functional molecular systematic reh based on non-coding sequence data. Toward
id, I endeavor here to illustrate the following:
regions are highly structured and
evolve non-randomly and non-independently; (2) this structure may be used to align
the sequence matrix and better asses-. I
(3) the resulting gaps in the aligned matrix may
out.mi ph\li)uem In alls impntlaiil uifoimahon and
-hould he used in . ph\ Indent In . na \sis: at d I t!
the mode of non-coding sequence evolution described here may have potentially serious repercussions for the accuracy of genetic-distance, maximi.m d i id i id. aaa pa: -mini -, analyses, and lor
1
.
Ira|
i
a 1
kknil'u
let hniques. A description of pi of
i ! m Nanism
il h.iu-i mliiii;
se(|uence evolul
is followed by a discussion of
the appropriateness of current alignment and anal\sis protedures, with the expectation that it may
provide a more informed approach to the applica-
This article is not intended to be a complete re;w of literature pertaining to the evolution of in>ns and intergenic spacers in all genomes of an
brief review of
non-coding cpDNA regions,
suggested
ion has lor the assumptions underlying modtployed today hv plant molecular s
The strength of any phylogeneti

r homology i
Thus, the molecular systematist strives to maximi
character homology by the careful alignment
DNA sequences in a data matrix. Fundamental
any alignment procedure of non-coding cpDNA g
quence data should be a familiarity with mutatior
mechanisms directing molecular evolution in no
coding regions. Recognition of these mechanisi
i generators of specific mutations can be a po
lor
eri J
A widely reported mechanism of length mulalinn

in non-coding i -1.11- - I lln li nnplast is slippedp:ii
SSM
SSM
thought to be a
within iii.n-eodmg region- ol the ehlornpla-l. MM
[oeli.-iidi ..II. and nacli ai grnom, - lei;., l.exinsun X
Gutman, 1987; Hancock, 1995; Wolfson et al.,
1991; Kelchner & Clark, 1997; Sang et al, 1997).
1 til-ill i:i Mali in- : iv import 11 |
< oiling -..-queiiee c\ nliition and >ia\r I-- n -uggi si
ed to occur at hast as frequently as base substitutions in some chloroplast non-codin.
(Curtis & Clegg, 1984; Wolfe et al., 1987; Zurawski
& Clegg, 1987; Clegg & Zurawski, 1992; Golenberg et al., 1993; Gielly & Taberlet, 1994; Clegg
et al., 1994).
Slipped-strand mispairing is thought to proceed
I.N a localized mi>painiig. ol -in- [e-st I anded DV\
in regions ol sequence repeats, as either a siring ol
:a an run e ihd- rep. al- oi i; ndeir.lx arrang. d n il
tibase repeat units (Palmer, 1991; Wolfson et al.,
1991; Cummings et al., 1994; Hancock, 1995; reviewed by Levinson & Gutman, 1987). Diagrams of
proposed SSM mechanics can be found in Levinson
and Gutman (1987) and Wolfson et al. (1991). Be aiise \/T rich legions ol bacteria! geiionx s are
particularly suseeplibl. ii. slipp, d strand niispan
llig ll.exnisnti i\ (i Itlliai . I'JoTg one eollld expert
a similar ellcel in the A/T-rich con coding ivgionof the chloroplast genome (Wolfson et al., 1991).
This is not lo irriplv llial SSM a. Is uniquely on A
and T nil. leoh 1
ling sequence
matriees often infer inserted repeats com an m:
and (i nucleotides, sometimes as pure strings o| (,
or C. iiioiioiiueleolidi' repeats.
Strings ol mononucleotide repeats, particularly of
A or T, appear frequently in non-coding p-hN \
and slipped -Irand mispairing max |..olciitial \ gen
rule length inulalioiis within these -it ugs The dil
ficulty in assessing homology of length
long -lung- ol repeat,-, whethei mouorun Icolid. o:
miiltmu.deohde repeats, derixes troni the niereasmg potential for further length mutation relative to
string length (Streisinger & Owen, 1985; Golenberg
et al., 1993; Kelchner & Clark, 1997; Sang et al.,
1997). Subsequent SSM activity may either generate additional repeats of the initial sequence or delete sequence su-< ptihli 1 -lipped ran mi
palling. Perhaps an equilibrium might exist
between ihe probability of inserting subsequent

lenglh i! ilaMoiis ai d tin piob.ibihlx ol lemox ing
sc(|iicncc from the repeat string. Whethei -in h an
I al I-1111111 is present or not, there may be a competitive' phenomenon that keeps the lenglh of tandem repeated sequence units continually in flux.
bVpii s. illation ol long rep.-al strings 111 1 on-, odii g
"d therefore be a "snaptions and deletions at that locality.
It follows that a point substitution within a long
string of mononucleotide repeal units could act as
si bih/ing la 1 to:, di-i ipi 1 g si- pie\ i< u- imiiormity and loweri
ol lurther SSM
. Such a substitution would -hrerllx influence
,-ti-uing mutation- a: llu region ai -I is me . \ anplof a non-independent character mutation in noncoding DNA. II the situation were reversed, with a
1101, l,.-!ii..
. .
jiMiK e l>< coming a string of
repeat units, the likelihood of an SSM event would
increase and could nidi,- i irlli- : non independent
mritali 1 I
ill
i 1 -li -1 i mux il ol 11 pi aled
sequence by slipped-strand mispairing.
As an aid to alignment, SSM-generated insertions and deletions can be used In position and
determine number of gaps. A quick study of a repeal unit or the flanking sequence of a gap may be
. imiigh lo i\< lermmr il -lip) 1 I -liaiid iiu-p- iirnig the likely progenitor of an observed length muta -n < trra-lonalk e\ iden. . -I ill SSM . . ell! max
110I be ipp ireiil. parli. ilaiU il 1 d.-lel. d -e<| rem r
is not a direct repeat of its flanking sequence, or if
fkelchm
Striking to both intergenic spacers and introns

in the chloroplast genome is the presence and number of probable secondary striielures referred to as
"st, an-loops." Stem-loops are believed to occur durug -ingle -handing r\ei Is win n a . rted rep. ats
meet to form a region ol pairing (tin- -I. im surmo ml- d li-, linn 11.|. 1. . ding, sequence (the loop).
widely discussed for ribosomal DNA, with ITS and 18S rDNA regions being of particular interest to the plant systematist
(see Baldwin et al. (1995), Soltis et al. (1997), and
Soltis & Soltis (1998) for discussion of secondary
structures in th-
gioi.- ml In 1 I
.g- in
mpln ; lmn>!
Probable stem-loop secondary structure is corns' nix n pe.rli d 11; non . 111 g icgx.i > 1 ug an llai
genomes (e.g., Michel et al., 1989; Buroker et al.,
Kelchner
Non-Coding Chloroplast
DNA Evolution
1990; Golenberg et al., 1993; van Ham et al., 1994;

Gielly & Taberlet, 1994; Natali et al., 1995; Rigaa
et al., 1995; Downie et al., 1996b; Kelchner &
Wendel, 1996; Kelchner & Clark, 1997; Sang et
al., 1997; Downie et al., 1998). Gielly and Taberlet
(1994) reported several probable stem-loops in the
tml.~ln>\ reg .in ul the eh nnplasl genoim . ua lud
ing nine highly probable stn
i I
intron itself. All other introns in the chloroplast genome- .if l.iti'l pl.iuK ale 1-l.i^silii'c, a- (,|(>M|> II idIrons and share a diagnostic secondai \ struct n< :>l
-l\ *i'll delined -tern loop ii .m.lili- I Koli. la el A .
1988; Michel et al., 1989; Downie et al., 1996b;
Downie et al., 1998). Diagran
found in Michel and Dujon (1983), Michel et al.
(1989), and Downie et al. (1998).
Loop regions of stem-loop secondary structures
ate often associated with hoi spots for mutation in
non-coding regions, i I , ! nucleotide substitutions
and indel events (vom Stein & Hatchel, 1988; Aldrich et al., 1988; Golenberg et al., 1993; Gielly &
Taberlet, 1994; van Ham et al., 1994; Clegg et al.,
1994; Ferris et al., 1995; Downie et al., 1996b;
Kelchner & Clark, 1997). Indels located in probable i
'
equentl) inserted or deleted repeat units likely the result of SSM. Howi.gil
i a! loop, ihey may occur anywhere along a -> .n

arv structure. For example, Kelchner and Clark
(1997) detected what appeared to be an entire deletion of a small - 1
< < I partway up the
-MI In -mil
IO] -. ..I 'I pre- i I. in a\ be removed in
some taxa without compromising the favorability of
a stem formation. Occasionally, small
the stem itself will be deleted, decreasing the
length, though perhaps not to an extent that would
innihil it< | ossil l< secondary structure formation.
Very large loops are often associated with regions
of chaotic or "lalni.
i .
i
n
lararl,
of many non-coding cpDNA sequence matrices
(e.g., Golenberg et al., 1993; Downie et al., 1996a;
Soltis et al., 1996; Kelchner & Clark, 1997; Baum
et al., 1998). Homology assessment here can be
difficult or impossible
preach ol removing these regions In mi !
trix before phylogenetic analysis is

adopted.
being highly i
cleotidi
pcalcd sequence composm?

conserved in character (Learn et al., 1992; Gielly
& Taberlet, 1994; Downie et al., 1996a, 1996b;
Kelchner & Clark, 1997), particularly when stems
are long and possess highly favorable energy of formation values (AG values; see Kelchner & Wendel,
1996; Dumolin-Lapegue et al., 1998). . SI Ijll. IICC
>|i :< i ail;
' is pane i
r to ribosomal RNA and rDNA secondary

(e.g., Curtiss & Vournakis, 1984; Wheeler
& Honeycutt, 1988; Dixon & Hillis, 1993; Soltis &
Soltis, 1998), a nucleotide substitution occurring in
a stem sequence of a non-coding cpDNA region
could compromise secondary structure formation.
Compensatory mutation may then occur to preserve
the potential for structure formation I Kelchner.
1996; Kelchner & Clark, 1997). Although sequence conservation may be present merely as a
Lap- the < ase in
i i i i
P .
I
j
I secondary strucsuggests secondary structures are integral to proper
functioning ol tin nitron (Clegg et al., 1986; Learn
et al., 1992; Downie et al., 1996a). Experimental
e-. ideme has shown some of this structure is essential for auto-splicing mechanisms in Group I
and II introns (Bonnard et al., 1984; Kohchi et al.,
1988; Dujon, 1989; Cech, 1990; Michel & Westhof,
1990; Hibbett, 1996).
Identification of probable secondary structure
coding sequences by improving gap positioning and
the appraisal of character homology. Ga|
by inverted repeats and regions relatively rich in G
aspect as possible stem- of seeAs noted, regions of chaotic
e correlated with loops, so the
boundaries of a chaotic region will frequently coricspi i ! Willi in-, cited re( . its dial can form a stem.
even if they do not directly neighboi the chaotic
region. Computer programs such as OLIGO (Rychlik & Rhoads, 1989), MULFOLD (Jaeger et al.,
1989; Zuker, 1989), and GCG's Stemloop (Genetics
Computer Group, Madison, Wisconsin) can assist
in h<- d< I
,i ' . .
, ,
i Inn in iiod-i od
ing sequences. A search can be conducted by hand,
particularly if a published data set exist- loi the
region. Free energy of formation values (AG) can
[ . caie i!:.t' d v. lh - me ot tin ; i isn software as an
appraisal of the likelihood of formation of a partic-
ular secondary structure (sec kelchner <

(1996) for an example where AG values
plied to parallel inversion events in their
Minnie inversions of lour to six base pans have

been linked to small stem-loop secondary structures cotumolilx lelened !o ;is hairpins (kelelinei
& Wendel, 1996). Hairpins consist of a stem composesi .1 Ileal l\ ad|aeei i invt -led i pea!- pitid leana sleindoop -In,, hire .v illi pari adar h -mal lenp
Tins loop may become inverted by recombination,
and the inversion mav be so small that it either
. -< ap. - iiolii e -I li n g allgmn. nl | k. I -linci A Wen
del, 1996; Kelchner & Clark, 1997), or the inverted
sequence matches particular bases of the uninverted se<|ueiice. i.
! .
-mg array of minute gaps (see Golenberg et al., 1993).
Identifying minute inversions can require careful
.1 i i. i i
_ i
i
ii
In mis of" an alignmeiil program have not heen 11porously explored.
Candidates toi a hidden inv. '-ion are several adjacent nueleolitle snbslilutioiis, a series of tiny
gaps, or a gap that demonstrates no repeat aspect
to its sequence structure. \ llernalu elv. one could
investigate these probable secondary structures b\
hand or with a se.niidarv structure computer program. Failure to recognize minute inversions in a
phylogenetic analysis, d
and Wendel (1996) and
ysis of Non-Coding Sequence Data.
Finally, small inversions associated with hairpins
ma\ be In-lib susceptible to reversal and parallelism within a sliidv group, even at the interspecificlevel (Kelchner & Wendel, 1996; Kelchner &
Clark, 1997; Sang et al., 1997; Dumolin-Lapegue
et al, 1998). This susceptibility to reversal or par-
(Kd
& Clark, 1997)the nearly ad-
Nucleotide substitutions are generally reported

as being more common in non-coding than in coding regions (Wolfe et al., 1987; Zurawski & Clegg,
1987; Olmstead & Palmer, 1994; Hoot & Douglas,
1998; however, see Sang et al., 1997, for an excephoni Sapi : ,imdv. ,i iiimb. r .1 studies report nucleotide siibstilulions is being ;us| equal to or less
frequent than length mutations in closely related
taxonomic groups (Curtis & Clegg, 1984; Wolfe at
al., I<>87; Xuransk, K Clegg. V'tW. CI. g,. K Z

rawski, 1992; Golenberg et al., 1993; Gielly & Taberlet, 1994; however, see Small et al., 1998).
Percent AT content is quite variable in non-coding cpDNA regions, though it is general
Ingl
than the average value for the chloropla-i genome
(Shimada & Sugiura, 1991; Downie at al., 1996a;
Small et al., 1998). Because of their high AT content, iion-geiiic regions must make a significant
. on:: ibulion In the hn h oxerall lirqiiem v of \ and
T in the chloroplast genome. Kajita et al. (1998)
reported an \T content ot lu'Vi in the Ir/A.-trnY
spacer and trnL intron, Kelchner and Clark (1997)
reported 70.5% AT composition in the intron of
old. lopl.is! gene //./Id in ban,! . :>-. and Small el al.
(1998) found an incredible 77.1% AT content in
lli. utieigenic spacer trnT-trnL in Gossypiiim. I n. i ill.. II llus unequal tendenex toward AT richness in noti-gi i
h M pi -I I '\ \ ha- several as
\el undetermined implications tor phylogenetic
anabsis nl non-ending sequence data. At a minimum, it introduces a strong base composition bias
into the analysis.
Substitutions may demonstrate rather high levels
of homoplasy in non-coding cpDNA region- due to
the frequency of inferred multiple-hit sites (nucleotide sites experiencing multiple substitution
eveulsi. Multiplc-lnl sites occur even at very low
estimates ol percent sequence divergence (Kelchner, 1996; Kelchner & Clark, 1997), suggesting
that the accepted coding region estimates of
"around 10-15%" sequence divergence foi optimal
phylogenetic signal may be inadequate measures
for phylogenetic utility of a non-coding region.
1'iet l-t underst udi \i
h\ \
> regions mav tlilspacer. Stem sequence ;

pennit mutations, resulting in noii-randel.-.b d - iibuletl and uon-intlepeiideiit nucleotide
-ubstili;: : HI- Sl.il -li. al -g n In n ->i tliileiein d
inulalion rales in loops relative to stems may be
tested lor- an adequate distribution mod. | see < Mm
stead et al.'s ( |'*'.'i , -1 : n -t. . I istit mulatioii in
:h< tiloroj I i-l gi i;. - /,!',\ aid ;- I I. vet ha- rarely, if ever, been performed on non-coding cpl)\ \
In addition to secondary structure affecting the
Kelchner
DNA Evolution
s and neighboring base composition in non-cod5 regions (Morton, 1995a, b; Morton et al., 1997;
volainen et al., 1997). The correlation suggests
it nucleotides flanked by A and/or T will demstrate a significant tendency toward transversion
. Such a tendency limits possible nuclereplace ents
itea in reasing the

s of parallelism and reversals, particularly if
e experiences multiple hits. One would also
I
data sets of high AT content.
an extra-regional or genomic scale has been suggested between adjacent or IU trl! . i | s in ill
h >rop]
genome (Howe, 1985; Palmer et al., 1985; Palmer
et al., 1987; Blasko et al., 1988; Ogihara et al,
1988; Milligan et al., 1989; Kanno & Hirai, 1992;
Kanno et al., 1993; Morton & Clegg, 1993; Hoot &
Palmer, 1994). In the conte>l I >>n . .-'iti quence comparison, such a large-scale recombination involving the particular region of study could
result in imlels of surprising size thai contain sequence content not readily identifiable in origin.
Recombination events may operate on a finer
scale within a discrete non-coding region. Occasionally one infers extensive deleted sequence in
an alignment with no apparent mechanistic explanation, presence of a small or moderately sized inversion, or a large insertion showing little congrueriee ii -i i . i In
-,< |ii< nt-i i ill. i N,. n
mutations suggest intramolecular recombination.
and they frequently occur in the loop regions of
probable secondary structures. Sequences involved
in stem-loops may be particular!) susceptible to recombination events due to the conserved inverted
repeats and mutational!- I
ibli
I ten i
such structures cmil ' ,,<>,
bination with other stem-loops, particularly with
those existing in complementary sequent*; position.
Recombination involving the entire loop of a secondary structure may occur, particularly in structures with long stems, resulting in minute or moderate-sized inversions in both intron and intergenic
spacer regions (Natali et al., 1995; Kelchner &
Wendel, 1996; Kelchner & Clark, 1997; Sang et
al., 1997). Such incidents are often homoplasious
(Kelchner & Wendel, 1996; Kelchner & Clark,
1997; Sang et al., 1997; Dumolin-Lapegue et al.,
1998) due to the persistence of the mutational trigger; in this case, the hairpin stem.
Intramolecular recombination is a notable alternative to slipped-strand mispairing as a source for
certain inserted or deleted tandem-repeat length

mutations (Palmer, 1985; Blasko et al., 1988).
However, Wolfson et al. (1991), Sang et al. (1997),
and Kelchner and Clark (1997) suggested SSM is
a more likely mechanism for length mutation in
their studies of chloroplast introns and intergenic
spacers.
ALIGNMENT
There are many philosophies for sequence alignment, and much of the literature centers on the
jMi'|i' i i|i| in- ,ili >M
iiif.n . i -Miftware for this
purpose. The structure present in a non-coding
cpDNA sequence makes it an excellent example for
discussing what I believe to be the fundamental
lem of most computer alignment programs: defining the nucleotide as a discrete and independent
character. The identification of secondary structure
and mutational mechanisms in the data may greatly
improve on current algorithmic alignments of gaps,
lli i- -xi
n i nl .1 h.it .. ' i I,..MI i.i_
Many have found software, particular!) versions
of CLUSTAL (Higgins et al., 1992; Thompson et
al., 1994), to be of help at least initially with the
.J . >
i
< nc es. The alignment
is then subjected to an "improvement by hand" to
position gaps (e.g., Samuel et al., 1997; Downie et
al, 1998; Bayer & Starr, 1998; Kajita et al., 1998).
This procedure saves time if the sequences are similar in length, but when indels become numerous
in the data matrix the diffii dties of alignment draii.iii. all>.
n
I InI- iuse most alignment
software initially regards each character in the matrix as an independent unit, unless otherwise specified by particular position or gap weighting
schemes defined by the user. The software is in<
rmining when mutations other than
it ions have arisen, such as non-independent
.
, i,
, .
s correlated with
SSM and secondary structure. Appropriate weighting for these mutations that could be incorporated
into an alignment algorithm is, at present, undeveloped.
The Elision method of Wheeler et al. (1995) attempts to improve gap placement and indel homology by alignment software. The Elision method uses
standard alignment algorithms to produce a series
of competing alignments based on varying gap
weighting schemes. These competing alignments
are then combined in a single matrix and an analysis is performed, with the effect that support is
increased for aligned regions that most frequently
appear among the various gap-weighlin
This method aims at objectivity, but makes no im-
provemenl on thf alignment ilgi lillun's mahilit\ !O

assess mutation types other than independei ! point
siibsliti.lions Mul.ilion- .1. (ion oding n gions are
influenced by surrounding sequence structure and
lf('.|uriil!\ occur not as independent has*- miit.iti<>ull.e insertion of a repeal unit (Kelchner, 1996; Kelchner & Clark, 1997). The likelihood that many
non-coding mutations arc derived from sequence
Iraginents tli.il .m- inserted, deleted, inverted, or
otherwise rearranged, negate- llie assumption <i
discrete, independent nucleotide characters uiider- \sell as any ex-
ment. Nucleotides i 1 lower-case l'|,1

ferred insertions;
the probable progenitor seep
in Examples 4 and 5, call t
sequence of interest.
pro-! milo i -iablish putalbe homology ol . h ir

acters in their data matrix should experiment with
a wide variety of v ip - J
v options. fliese options, honey t. ma\ not reveal the underlying inn
lalion I in. haiusni- ... . >- .umg sequence reart:a.:r>. in. atin chloiopla^t i on . oding n gums Hi. \
ina\. fiou.-v. t. facilitate the i ipid alignment oj -eg
incuts of the mati i ill it si
iisistenl sequent c
nie:
ions of variable
length that require special consideration.
Alternatively, some have avoided alignment programs entirely ai
ning sequences hy
hand (e.g., Golenberg et al., 1993; Hodges & Arnold, 1994; Kelchner & Clark, 1997). This approach facilitates a careful study of the matrix as
it forms and increase- llie researcher's familiarity
Willi mill ;lx>n- in lh. -.-.iNi-rice- llii.cy.-i. ili:-ii
nielli by hand. especially wlieii dealing with eonhe presence of a
great tiuinliei -I leng'h mutations, can he tedious
and time consuming.
Kelchner and Clark (1997) suggested that awareness of the proposed mutational mechanisms active
in non-coding regions can be useful for inferring
and positioning gaps and ultimately in assessing
homology. Golenberg et al. (1993) were the first to
detail a criterion for aligning gaps in non-coding
cpDNA matrices. Based on their example, Kelchner (1996) and Kelchner and Clark (1997) modified ili! alignment ri J. rion loi c hloroplasl ;<<; :i
intron sequences. Hoot and Douglas (1998) also revised Golenberg et al.s(1993) method of gap alignprocedure for defining gap categories. Although
nomenclatural system is not requisite for gap trp*
ment in a phylogenetic analysis, it may be ed ,
in
collating information of inferred muta
DNA studies.
cpDNA is a direct ie|
>l
in
hhoring sequence
("Type la" gap; Golenberg et al., 1993; Hoot &

Douglas, 1998). These often take the form of variahle length strings of a itionoiiuel. olide repeat unit
(Example 1).
EXAMPLE 1.
1. TTAAAAAAAAA---TTGA
2. TTAAAAAAAAAA--TTGA
3. TTAAAAAAAA
TTGA
4. TTAAAAAAAAAAAATTGA
i i
i ill. otidi - 1 hen-fore, such regions are ei'!;. t removed from cori.-ideral ion as [ml. nlial pin
log. iielie characters (a conservative approach! .a
ir. haled US rii.leil ga] i h.ll e|ei- .em .pi ( .hug to
length of the repeat string (often becoinu ; highly
aouii pla- .as ll the < ui:te\l ol : n suiting It p .log\ I
:.i hen oloi \ is . \acerbated l.\ [ft I. nlial
nzymatic processes during PCR
i. h can also geneiale k ii i;11>it- length it p. al -li n g> mtl, pendent l
ill. It mplnl. "s ,e.|lienee col si I ill. u 'ft lien strings
ol
Ijaeeiil
niiicl. otidc repeats are highly variable in length in a matrix and reach or exceed the
range d. inonstraled ahoy. . lhe\ b< come u or. likely
lo espei lent e li.rthi i S^M n ulat on. for tins reason, it is perhap- ,, .
i I I, to remove such
an as from > or sideralit i in a pi \ log. tn-li m ilvsiInsertions can also be multinucleotide repeat
units of a neighboring sequence, as tlen
in Example 2 by the inserted repeat unit ataaa
("Type lb" gap; Golenberg et al., 1993; Hoot &
Douglas, 1998).
EXAMPLE 2.
1. ATAAAACAAA
GAGCG
2. ATAAAATAAAataaaGAGCG
3. ATAAAATAAA
GAGCG
4. ATAAAATAAA
GAGCG
An inserted repeat of this nature could be extensive in length and may be difficult to recognize as
a repeat unit during alignment (for example, I have
identified a 73 bp inserted repeat [unpublished
data] in the trnT-trnL intergenic spacer in Myoporaceae). A repeat unit by its very nature shares nucleotide content and order with flanking sequence;
therefore, multiple gaps may be inferred by pairing
segments of an inserted repeat with its progenitor
sequence. This is particularly problematic if the in!
sertion or its progenitor has experience I
quent nucleotide substitutions.
Even when a single gap is inferred, pos
a repeat unit. Example 3 is reproduced from Kelchner and Clark (1997) and demonstrates how a
repeat unit may be obscured in a sequence matrix
EXAMPLE 3.
repeat unita common mutation type in non-coding regions. If alignment options B or C were used
for phylogenetic analysis, the content of the insertion would be of unexplainable origin (though still
possible) and the potential of incorrectlv assessing
i ii i. otide homology in the region may be considerable.
Any of the gap positions in this particular example would not affect a topology generated from
these four taxa, but gap positioning may have a
significant effect in a larger matrix of more distantly
related taxa. The position of the gap in alignment
3A and detection of the repeat unit may also be
relevant in determining a weighting scheme for
these non-independent characters.
Length mutations may overlap with one another
to create a progressive-step indel. In the more extreme cases, appraisal of homology in these region
can be very difficult, or impossible (Palmer et al.,
1985; Downie et al., 1996b; Kelchner & Clark,
1997). Example 4 demonstrates a prob I | i
gressive-step indel in which two possible placements exist for the repeat TTGA. Note that the underlined sequence is a direct repeat of the
preceding sequence TCGTAATTGA in the matrix.
EXAMPLE 4.
-AACAGA
-AACAGA
2. GGTTATAA
ATTAACA
TTGA
AATCGTAATTGA TCGTAATTGA TCGTAATTGA ttgaAACAGA
1. GGTTAT
GA ATTAACA
2. GGTTAT
AA ATTAACA
3. GGTTATAA tataa ATTAACA

C.
1. GGTTA
TGA ATTAACA
2. GGTTA
TAA ATTAACA

Alignment possibilities A, B, and C were equally
probable using CLUSTAL W (Thompson et al.,
1994). Only alignment A reveals the insertion is a
If part of the underlined TTGA in sequences 3

and 4 is moved from its current politici i ign
with ttga in sequence 5, the possil
ttga sequence is a direct repeat of the preceding
sequence may be obscured; however, this alignment
; i< would not be impossible. As the preceding
sequence to the underlined 10 bp repeat does not
contain this additional ttga repeat, we can infer
that two separate events have given rise to an initial
10 bp insertion in sequences 3 and 4, followed by
an additional 4 bp insertion in sequence 5. Whether ttga itself or the preceding TTGA is the subsequent inserted mutation is impossible to determine. In this case, either alternative alignment of
the TTGA unit would cause no effect in a phylo- ii< ii
i il -i- i i- M,I - in i slant here to distially informative nucleotide substitutions were
present in either of the repeat units in Example 4,
i'lr-r -aitSslil itioi - -ll,, ||,| \u- \. H,!r:: t|,.| ,
; .1 \
Inp-tictic inalssis on die l.nsis lli.il rim leolide ho

mologv of the repeals is not discernable.
The example above suggests that homology may
be unhealed |>\ die length of insertions or del, lions
ill a gap. although -i.. li an i iai plinti is not without risk. Exampl
possible alignments ol die gati repeat unit (represented individually by sequences 2. 3. and 1) with
the insertion in sequenee 1.
sequence 1. Sec|i ,
2
' i..bablv -hate a
imilai
igu
i o-peal of the | .ceding sequence
Tl'\ \T. T! . events, al ; ncd as lln . are in Kxample
6A, are probably non-homologous. A re-aligninent
could be performed to accommodate the two separate indel events (Example 6B), even though the
infers an additional gap (see Hoot & Douglas,
1998).
EXAMPLE 6B.
EXAMPLE 5.
1. CAGATTGATTGATTATTATACTGATTATGC
1. GGTTAAT
2. CAGATT
gattATGC
2. GGTTAAT ttaat
ATGC
3. GGTTAAT ttaat
ATGC
4. GGTTAAT
TCTATCT
5. GGTTAAT
TCTATCT
3. CAGATTgatt
4. CAGATT
gatt
5. CAGATT
ATGC
Again, actual homology is impossible to assess

with confidence, for then- exist three GATT repeat
units in the insertion in sequence 1. In eases like
this, homology is often inferred on the basis of
length of indel and minimum number of gaps required to position the repeat. Hence, the gatt repeal- in sequences 2, 3, and 4 would be aligned
one above the other and on one side of the gap to
reduce the number it uil.-ind indel events. When
I Is i- characters, this would be a rea-oiiahle Mihiti.in m lieu ol oilier evidence for indel
i
all uoald be treated is homologous lor those- sequences that contain it.
I\qnal eiigth ol insertions ie.ii.. tiol he strong evidence of their homology (Kelchner, 1996; Kelchner & Clark, 1997; Hoot & Douglas, 1998). Con-
tctat TCTATCT
TCTATCT
TCTATCT
There is a hazard that minute inversions (Kelchner & Wendel, 1996) can be completely obscured in a matrix if they introduce no gaps during
llnranci:'. pa: : ."in u '. 1 hen a' \. gap weighln /
schemes have not been rigorously pursued. If pre-ei,- and II re -ogru/. d in a d ila matrix, uiiriute inversions may oMiutagh a particular mutation by
ul ipr, ting ill, II gl< iniilalion event (an inversion)
as inulliple apoinorplues ol adjacent IIIK leolide
-1..I!"'-' lain us. I\\ impli 7 hi h.w illiislrates a siluaTTGG to CCAA (from Kelchner & Wendel. 1996).
EXAMPLE 7.
? CCAA AATATTA
3. TAATATT CCAA AATATTA
EXAMPLE 6A.
4. TAATATT TTGG AATATTA
1. GGTTAAT tctat TCTATCT

2. GGTTAAT ttaat TCTATCT
3. GGTTAAT ttaat TCTATCT
4. GGTTAAT
TCTATCT
5. GGTTAAT
TCTATCT
Alignment of the insertions in Example 6A results in the pro! iblv n i-l k< n In II.<;.> \ ,.| in I, -.
in sequences 2 and 3 with that ol sequence 1. The
soiled repeat ol the sequence to the right ol the
gap, TCTAT.
explanation,
events, than
km I.', lv.
This would be a more parsimonious

in terms of total number of mutation
to infer a single inserted repeal lol
r i j| i li' '.I,, I, ,|id, -ii.::'-' :MI II i - i!i
5. TAATATT TTGG AATATTA

If the inversion is of sufficient length to introduce
mill I
ip- in the matrix (see (,olenl>erg el al.,
1993; Sang et al., 1997), two possibilities can oc. II.i tin" gaps ,, ill ': < misal gned h parts ol the inverted sequence sharing spurious sequence similarity with the uninverted sequences: or. there will
he inference of an inserted sequence ol unknown
origin (in reality, the inverted nucleotides!, which
corresponds with a deletion in the homolo... i en
in il<
ici i .
I i. a p . i dilv will lead to
ma. eural,> assessment of homology and mav potentially have a considerable ellecl on phylogeny es-
events will hk< II.

u
- !
structures, speciln ,i!l>, v. iili 1<.|> regions of stemloops (Kelchner, 1996; Downie et al, 1996b; Kelchner & Clark, 1997). Identification of flanking sequences involved in [i issih c -lein form; h:n: . cidd
locale the boundaries for the region and aid in
aligning the indels. Discerning probable SSM
ceplible siics ran also be informative lot thi- irilcr-
ol .dm II ma) obsi un evolutit nary history.

(3) Inversions may show high levels of parallelism and reversal, II,-I ihen plivlogenetic utilih max
not be particular!) robust. I ndeiected minute inversions may be buried within a data matrix and
base substitution
swiapomoipliics instead of a single mutational
ence of parallel and reversed insertions or delePerhaps methods of gap or character weighting
ami alignment based on mechanism- of MI. \;.i I. .JI
can be incorporated into software designed lor non
i oiling sc(|ii< ncc alignment, parlii ilatb b>, i < lulling an evaluation of AG values for probable -,,ii i i - - uctures. However, the diversit) ol rates
and types of molecular evolution in non-coil in-: regions may he proton in
\- -1 I! coding DNA, we
are far from und<
es directing nonc< in,!. :n ilar * .on
i
' 'gree that we can,
v. .lit am < rlain;\. assign pinbab lilies f:> ci. :r>
i '.insid. rini. ilia1

fundamental !> tin
alignment
al
da
sequent c data
< nlire pic, logci v <>' rca'
ANALYSIS OF NON-CODING SEQUENCE DATA
i , . id llg sequel), e dala.
\; i r ihese are the following:

i i I Slipped-slrand mispai: mg < in be the result
oi persistent mutational 'm.in- (especially when
ihc n igg. ! - seqinn
is >< .11 I in the stem of a
II
i
i
UL Tins can introduce
i lisms and reversals into any
phv logcli.t ; slimalions lb; I include - p coded
< I i i I
in I
i id
Mi Hi11 I indel events in a
I
i ,
-.
i mology of length
mutations. Non-independence of these mutations
ighting of nucleotide characters linked in a repeat unit, if each
base is treated as a character in an analysis. Weight
of the unit taken as a single character is also an
issue if the unit is included in the analysis as a
Cod< d gap character.
(2) Secondary structure shows nonrandom mu-ible
influence of neighboring bases. A parlicida: has,

may experience substitution events multiple times
in chisel) related lineages, reaching saturation long
before the expected saturation level lor the remaining sequence. A base-composition bias toward A/T
content is clear!) present m non-coding epDNA.
Selective pressures exerted on non-coding regions may lie largely a function of the plivsical
structure of the sequence and possible functionality
is
.a p.
-I's sholll II
:
I - ail" ill. steps
laki i to a ign lliei: seqia in e i| da in order to provide necessary information for the assessment of
their proposed reconstructions of phylogrnics.
phv logone; c .ci il\ -i- ::! n
(4) Nucleotide substitutions may be under peculiar constraints not fully understood. There is evidence of a bias in non-coding regions involving
methodology developed for coding sequence, which

quence evolution, transition/transversion ratios, and
initiation probabilities, is inappropriate for the
analysis of non-coding regions.
Plivlogenetic estimations based on genetic distance measures ol non-coding opDNA sequences
must be approached with can . Superficial application of models for maximum likelihood (ML; Felsetisiein. 1981) or neighbor-joining (NJ; Saitou &
Nei, 1987) could easily produce erroneous phyloderlying the methodology are violated.
For example, most models consider a nucleotide
site as the unit ol cvohilii i 11! ilaud A I k- aw il-l
er, 1992), a consideration that is contradicted by
the mode of non-coding sequence evolution. Simplistic models based on the commonly calculated
Kimura estimates (Kimura, 1980) and Jukes-Cantor
mi.
Ink,
I I
I '' '< '', --lime an equal
25% frequency for each nucleotide type throughout
the sequence and generate base mutation probabilities from this assumption. Because r -coding
I \ \ -gions can demonstrate much higher A/T
content, this assumption is clearly contradicted.
Furthermore, transition/transversion ratios in n<>n'<h I-
v,; '! -
"
^' '
' "'-
'' i ibb
from coding
ones (see Hoot & Douglas, 1998),

vary between <
chloroplat
erogeneity is highly probable, especially if regions
and hot spots for mutation exist in
Annals of the
the data. The presence of multiple gaps in an

aligned matrix presents an additional hurdle for
distance analysis, and iiidels themselves are difficult to incorporati
ctcrs
( .Ui||.[. tllli.
-II:- 'I
and cnmpulaliorm
. ; i ; .1. jil.M- .
ei
.1!
\j
: C
fI V K . . I
,,
the initial Jukes-Cantor estimates to allow for varying base frequencies (e.g., Tajima & Nei, 1984)
should be employed. Transilion/lraiisversion ratios
can be estimated directly from the non-coding sequence matrix by pairwise sequence comparisons
(e.g., Yang & Voder. '>'>lh. I n u iting the circularity occasioned by measures derived from a topology. More refined distance models that incorporate these problems stand a better chance of
reflecting the mull molecular evolution in non-coding sequence data. Such refined
models may therefore estimate a more accurate
|h\lou-u\ thai better recovers the evolutionary history of the characters.
With ML, transition/transversion estimates are
dependent on whether among-site rate variation has
been incorporated in the model and can be sensitive to the accuracy of the topology used for their
estimation (Sullivan et al., 1996). Among-site rate
helerouetieitv in the data is often assumed |,> hi
eithei a negative binomial or gamma distribution
function, and confirmation can be assessed stalls
ticill\. Such rate heterogeneity is likely present in
non-coding sequence data din- to the effects of secondary structure on mulalion likelihoods. Hates ,,|
variation al sites are usually expected to fit a gamma distribution model (Yang, 1996), and a parameter (a) can be determined to define the shape l
that underlying function in an ML anabsis (see
Yang (1994) and Yang (1996) for thorough explanation). However, Sullivan et al. (1996) suggested
a estimates are strongly affected by the topology
used for their estimation. Therefore, to improve the
abdih ot a model i
.i
to recover the "correct" phytogeny, a must be cab
culated directly from the data matrix; this should
be done by pairwise comparison, which can be a
computationally intensive or even impossible procedure as the number of taxa increases in the matrix (Yang, 1996; Sullivan et al., 1996). Poor estimation of a can easily result in a misleading
phvlogenetic hypothesis (Yang, 1996; Sullivan el
al., 1996).
Other problems associated with non-coding
cp|)\ \ sequence data may be very difficult to address. || at hast some of the mutation m non-coding
sequences occurs in linked units, then the nonindependence of these nucleotide characters directly affects the subsequent analysis. At present,
there is no rel I >

i
i i . stimate to
rate such non
aclers in a
model. Most work on parameter estimates
els lias been based on coding sequence
ijof|S.
. || . ! ! M I ! - : I. . .
| ,. . [
| e | ]. -I I
\ | |<
incorpodistance
for modobserva-
I I UK | I le .ISpect S
lion in non-coding regions,
Determining probabilistic estimates for non-coding cpDNA mutations is, at this time, difficult;
therefore, the accurate assessment of the underlying mode of evolution for maximum likelihood aualysis may be impossible. As Yang et al. (1995) discussed iti detail, the accuracy of ML in recovering
an evolutionary history is strongly dependent on the
evolutionary model applied. Thus, for non-coding
cpDNA sequence data (as well as genie sequence
data), deeper understanding of the manner of evolution in these regions is required before an accurate model loi \1I
: .
analysis can be applied.
The frequent alternative to distance measures
and maximum likelihood is parsunouv anabsis
Heuristic parsimony searches can be considerably
last, r mil l< ss
i
I
intensive than a
maximum likelihood anabsis with the parameter
adjustments described above; however. thev arc often much slower than a distance anabst- 1'aisimonv aiial\-e- that contain no weighting schemes
for transition/transversion bias and non indepen1
lion of matrix i haractcrs may be as vulnerable to reeoveiy of an inaccurate phylogerry as
similarly simplistic distance models. It has been
1 that parsimony's potential irr some cases
to recover a correct topology decreases significantly
described here irr non-coding cpDNA. And though

it has been proposed that the reliability of parsirrioiiv estimates increases witl
Teasingniimbei
of la\a included in an anabsis n-.g.. Wakeh \. 1,>,W;
Sullivan et al., 1995; Yang, 1996), it is unclear if
this effect is independent ol possible among-site
rate variation.
Parsimony specifies no particular probabilistic
evolutionary model, but like all phylogenetic estimation methods it is mlluciiced hv iioii-uidependeuce of characters. This problem can he allev laled
to a degree if mutations such as inversions arid inserled or del. ted repeals arc recognized as nonindependent events and are either excluded from
the anabsis or coded separafeb as described helow. Any non-independent evolution of neighboring
nucleotides in a sequence would . reatc an artificial
weighting effect for these positions in a parsimony
Kelchner
DNA Evolution
in lysis in i onsiders each i icleotide an independently evolving character.

Various weighting schemes have been proposed
to counter this effect. Weighting has been applied,
tor example. Ir. compensatory tnutatioi s . ssneialed
with secondary structure in rDNA (e.g., Wheeler &
Honeycutt, 1988; Dixon & Hillis, 1993; Baldwin et
al., 1995; Soltis et al., 1997; Soltis & Soltis, 1998).
Tiial weighting schemes have also bei n applied to
titioned analyses may prove useful in locating and

determining the degree of problematic liomoplasv
affecting resolution in competing topologies.
Minute inversions should be identified and removed from the analysis, to be added as present/
absent characters at the end of the matrix (Kelchner
& Wendel, 1996; Kelchner & Clark, 1997). This
non-coding sequence data from the ch

(e.g., Downie et al., 1996a; Liden et al., 1997).
However, Olmstead et al. (1998) reasoned that an
erroneous weighting model increases the ch;
thai tin < orreel topology is ex. ludi <! from the ii os1
esolution, but would i

by the analysis. Development of defensible w
ing schemes for non-coding sequence data
necessarily come from evidence provided by
parative analysis of non-coding regions throu
the chloroplast genome, and may be specific
Lit
hi
of misdiagnosing
an appropriate weighting -a heme loi -i;|'-< I- it 'I
Therefore, it is perhaps sen-ibl. lor i \ ai.pl a I weighting to non-codii- -. a- nee characters until we have further e\idence to support a particular weighting scheme.
Insertions and deletions have been shown to be
of considerable phylogenetic value (e.g.. (mh-nberg
et al., 1993; Mes & Hart, 1994; Natali et al., 1995;
Downie et al., 1996a; Kelchner & Clark, 1997; Oxelman et al., 1997; Sang et al., 1997; Liden et al.,
1997; Downie et al., 1998; Bayer & Starr, 1998),
and one should consider including gaps a- coded
, i. a i - i i
liarai i |
nded to the sequenei matrix (e.g.. I lodge-. <K \im.ld. I''(l; Kelchner & Clark, 1997; Sang et al, 1997; Downie et
al., 1998; Hoot & Douglas, 1998; Bayer cK Starr.
1998). Selection of gaps to be included in the analysis, however, is somewhat subjective in that oplimalb ..iilv those h niilh miitalmiis usually lnnolba-.ed
i
i
 uence matrix can
be an interesting and informative approach to

studying the degi. i 4
- t] iti< I provided by point
-i siiintioii nr i; I lion alone (e.g., Kelchner,
1996; Kelchner & Clark, 1997). A similar analysis
I
'videiK e of
the homology of inserted sequences is convincing.
Chaotic regions or other areas where homology assessment is de< in
II
- I I
I - ild hi . X. bided
from the data matrix before analysis (see laden et
al., 1997) to avoid this mistaken claim of nucleotide
homology.
Bootstrap (Felsenstein, 1985) and ja< kkmb
(Farris et al., 1997) analyses, frequently misunderstood to be direct measures of phylogenetic accuracy, are only as sound as their underlying analysis
procedure. \s with coding sequences (see Trueinan.
1993; Hillis & Bull, 1993; Bremer, 1991: Mishlc.
1994; Brown, 1994), both support measures can be
atle. ted b> the non-independent structure present
in non-ending sequences. The structure invalidates
a requirement o| ihe statistic thai each nucleotide
be a discrete and independent character.
Bootstrap and jackknife analyses are a re-sammeasure how robustly the data in the matrix support a particular topology. The concept is sound.
bill the statistical integrity of both measures relies
on lb. assumption that each nucleotide is an iniiv .Ha I charaeli i. dial . ael . h; l ictei evolves randomly and independently, and thai the matrix represents a sample of a much larger population of
characters evolving in identical fashion (Felsenstein, 1985). Due to the non-independent structure
existing in non-coding regions, and tin
I .a!
unique series of evolutionary constraints acting not
orib. n i ituiu ,;.iai . i -c i<.ia,_ i> gmns bill also on
us of a region, each of these assumptions
may be violated. Sampling from within such a data
> sampling a nonrandom and non-in; larger popula-
in theory, cover all possible error due to reduced

character sampling in each replicate, hut the
strength of the hoolstr.ip lest is weakened if the
characters are not accurately defined. If a character
in some cases is not an imli\
i
ahle secondare -liu. in should he routinely idenI if icd and used as an important source of information to aid in aligning chaotic or labile reg s ol
the data matrix. Prior to phylogenetic analysis, all
matrices should he carefullv reviewed for obscured
make bootstrapping and jackkniling accurate as

measures of data support for a topology are not satisfied. An analysis would produce an unequal
weighting etle. t on subsets of the data in each resampling dm to
'
I
character definition.
\ noii-rcsampliii
I
lows assess-
misaligned repeat units.

Important for understanding molecular evolution
in uou-coding I)\ A is die concepi oldie mutational
trigger (Kelchner, 1996; Kelchner & Clark, 1997),
i specific sequence pattern that creates the foundation for a mutational event. Such triggers often
remain intact after generating a mutation, and then
ment of data support for individual (lades is the

Bremer Support measure (BS. or "decay" analvsis;
Bremer. 1988. I()(M: Donoghue el ah. 1'>('2: lor
application to large data sets, see Baum et ah,
1994; Morgan, 1W7). The measure is a function
only of the recovetabditv ol .lades in topologies
piogressiveK on.- step longer. Bremer support has
the possibility .1
h< .Herts ol character definition issues discussed above for bootstrapping if the modi I i i : .im the ph>Iogen\ estimation considers the variable nature of character
definition in a nucleotide set.
Oxelman et al. (1999) demonstrated that bootslrappmg and BS evaluate dillerenl parameters of
presence can easily occasion a repeated, paralleled,

or reversed mutation event. Triggers may likely be
responsible lor much of dn- lioinoplasv of gap characters inferred in studies at any taxonomic level;
those applying non-coding sequence data to moleculai systematica should be aware of their occurrence and effect.
liiloriiiation ol die kind presented here can increase the predictive value of mutational events in
non-coding DNA. For example, Kelchner and Wendel (1996) suggested that minute inversions associated with hairpin secondary structures described
in non-coding cpDNA could occur in similar situations in other genomes. Diimolin-I.apciuie el al.
the data matrix, and are thus not directly comparable measures (though BS values, when high, may
be imperfectly correlated with bootstrap and jackknife values). BS values cannot be viewed as probabilistic estimates themselves (Oxelman et ah,
1999), and an inability to adapt the measures to a
standard scale that is universally applicable renders the technique of dubious worth to some systcmatists. However, the innovation by Oxelman et
al. (1999) that includes minimal branch length values with each BS value does, in a non-standard
way, improve the comparative mlormalion capacity
of the measure. This procedure mav he more meaningful and informative than bootstrap and jackknile
values for non-coding cpDNA data.
(1998) recently reported just such an event in the

mitochondria of oak populations of southern
France. Hence, recommendations proposed in this
paper for the phylogenetic analysis of non-coding
cpDNA sequences may likely apply to data from
non-coding regions of nuclear, and particularly mitochondrial, genomes.
Choosing an appropriate non-coding region for a
particular taxonomic level is essential for maxiniizing its utility as a phylogenetic tool, but there is no
mlallihl. method loi determining what that "proper" degree of mutation is for a particular study. A
region's utility mav van between plant groups thai
arc assumed to occupy the same evolutionary level,
and data from multiple non-coding regions, when
CONCH SIONS
ar)r
In summary, great care should be given to the

alignment and assessmenl of non-coding sequence
data. There is considerable evidence now that noncoding regions are highly structured, non-randomly
evolving DNA; thus, alignment by current randomized algorithmic software is rarely adequate. An undcrslatiding of the proposed mechanisms of mutation acting on non-coding sequences is critical for
the positioning of gaps and the belter assessment
of homology of indels and |
I siibslitulions. Prob-
y m phylogenetic utility (see Small et ah, 1998).

In light of the mutational mechanisms outlined in
this article, at least one concern seems |iis|ilied: il
the laxonomic level is too high, one would expect
saturation of multiple hit sites and concealment of
multiple hit indels in any non-coding region, decreasing Us uiilMv as a phylogenetic tool,
The perceived intricacies of molecular evolution
and their bearing on phylogenetic analysis, both in
non-coding and coding regions (for genes have
well-known me. haui-lr. biases as wellthe codon
position being just one example) can be discour-
Kelchner
DNA Evolution
iiilmed i
ah-iimnr and anahsis -li.- ill! rnhaim. llm plr, 1.
grnrlic aiihh ami a.. irar\ of rum foiling <ml>N \
data. It should be noted that in almost all systematic studies has. ill i i ram-, oding, rpl J.N \ s'-qimin
es. 111. authors pro!, ss to hav.
i ml i I'd i n | .
! .,. nt in ml..tn ilion ii. ili< ii.l I i , ..in i iK ain lower-level phylogenetic
Clearly there is a need to
ing of molecular evolution
regions similar to lha< \vhi
analyses.
develop an understandin non-coding cpDNA
h r\isls fni rldmoplas'
genie DNA. Conl

I
)ii-coding sequence evolution may eventually produce a more
halam . (! p>..,-.-ss lor llm dmi mei I n.,| ph% I ...
imii, anal\si,- <>: rmii-.-odnig -r:;n
software ma\ he able |o incisure and assess prohahilili. s asso. ial<-d u lh parti.ml. r
mechanisms and incorporate this inf'or
llm alignment (:>. . ss. This u mid I..- ,
aid to those systematists who wish to
coding, inol. rulai tools 1?) ill. field n( pi
Vldricl,..].. II. W.Cliermm K. Merlin & L. Christopherson.

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/nrawski. (, X \1. T. Clegg. 1987. Kvolulion ol lugherplant chloroplast 1)N A-encoded genes: Implications for
-I, iicture-lunrtion and pin logcmlie studies. Annual
Rev. PI. Physiol. 38: 398- I 18.
ALLPAHUAYO: FLORISTICS,
STRUCTURE, AND
DYNAMICS OF A
HIGH-DIVERSITY FOREST
IN AMAZONIAN PERU1
This paper describes the results of a flonslie iri\-ul<n-\ al ihe \llpalma\o Ueserw. near Iquilos in Amazor
Two long-term one-hectare plots were established using a pre-detemiined sampling grid, with each individua
liana over 10 cm diameter collected at least once. e\cepl lor palm-. I'll.- plots weir ic-oensused alter ."> years ti
is and 89 species: no other family repn

ptional floristic diversity, both the structi
uitos area and to Amazonian Peru, wlii
Biologica de Allpahua\o. < cica de Iquitos. en la \inazoiua I'eniana. \lli
M'
cstablecieron dos parcelas de
I bosque. El t
; especies de arboles y lianas cr;

itiia, floristies. inventory. Neotropics
1
We gratefulK ackni.-.l : n.vh: .:. m i in ih.n Mippnrl Irom Inst ituto de I m est igacones de la Amazonia Peruana
(IIAl') lor permission to work in Allpahuayo Heservc and for logistical support for our work; the John D. and Catherine
T. MacArthur Foundation for long-term support of the Missouri Botanical Gmlen"- lloristic and ecological research at
research in \-na/,.uian IV, m,:,nl # .l72->- .,-,,1 lli. I K. \atmaf Fin ironmenl Research Council lo. a Uesearch
Fellowship (OP). Melchoi \guilar. (iesar (iramlez. liosa ( )rliz de (ientrx. \estor Jaramil lo. Drum- Milanowski. John .1.
Pipolx III. Pegg\ Stern. Ileuk \an del Weill, and \riuro \ a-quez Mailinez ai-led in establishing. in\eiitorying. and
re-eensusing the \ lip lim r .. pi, .i . !!, i naninii determinations were provided bv numerous -\ -t fjn.it i-1 - at \|(l and other
herbaria, and we are especially grateful to: C. C. Berg (BG); T. Pennington, Sir G. Prance (K); \. Cliamlerhali. I!.
Gereau, R. Liesner. J. .1. Pipob III. G. Scl.alz. C. las lor. \l. funana. II. van de, \\, ,11. and the late A. H. Gentry (MO);
D. Daly, S. Mori, and M. Stern (NY). The maps were drawn by A. Manson al lli<- N liool ol Geography Craphies Unit.
UniversiU of I eeds. Wr I
I
Si. G Prance, and H. van der Werff for their conslruclm- suggestions to
or. CARD. 87: 499-527. 2000.
II I IV !'|S||\
much of the tropics. Yet
biological
hampered by inadequate baseline informati
Thus, sufficient data on the numbers, kinds. ;
abundance of most major plant and animal taxa
not available. Moreover, knowledge of species
sociations and biogeographic distributions of t
remain meager (McNeely et al., 1990; National J
ence Board, 1990; National Research Council
l><)L>: IMiillips & Raven, 1996).
In the Neotropics, the extraordinary species rich
ness. our limit' -I
in
.ii
physical
ble barriers l<> ph\ tigeographic investigation. Traditional biological inventory efforts that relv mostlv
on .nl hoe colli .
' i
.i
I I
m . i i
llorisii, niiderslainliiii. b\ i eneraling aige numbers

of new iolleetions that are associated with site-spe ilu ci ologic al information Botanical institutions
play a vital role in initiating and su|>| HIT. 'Inwork, and contribute essential expertise for ensuring accurate voucher determination. Equallv. ecological inventories general.' much hiogrograplncal
data of relevance to nioti,.gr,iplii< mil ph\ I..gen. ti.
studies. Such eco-lloristic research has recently
been initialed in several tropical countries, including '1
-.nil own t al 1(>97 I! lift Messmer, 1999), Colombia (Rudas, 1996), and
Peru (Gentry, 1988a, b). This paper reports the results of a similar research program at the Allpahuayo Reserve, near Iquitos in northern Peru.
studies i anuol address the knowledge gap alone.

Alternative methods are < r il i. al to improve our understanding of the l.ieL.I- del. MM in III- species nimposition and the ecological dummies ..| in pi. il lei
est ecosystems. Ill recent years there has been
growing seientilie interest in more ecological, plotbased work as a means of understanding tropical
forests (e.g., Gentry, 1988a, b; Phillips & Gentry,
I'>"1; Phillips et al., 1994; Dallmeier & Comiskey,
1998a, b). This approach can contribute . .
i
STUDY SITE
The Allpahuayo Reserve (357'S, 7326'W) lies

southwest of Iquitos in Amazonian l'< MI. between
the blackwater Rio Nanay on the northwest and tin
Iquitos Yuita road to the southeast (Fig. 1). This
2750-ha reserve is administered by the Peruvian
Institute for Amazonian Research (IIAP). The climate is humid and hot (with the mean annual pr i mi ind an average temper-
High-Diversity Peruvian Forest
HHH = hhhH'l-lH"lMIHIM =
1!Hi
It!
p
IT?
' xll
IJI
|,|a|B|a|.|a|a|Bh|a|3|a|a|a|,|,|,-R:
|B|,|aH*H*HH = M-IHlre^R'
fit
HI
"31
atureof26C;Mare
,.!))}! \\ ihuayo Reserve
lies between 110 m and 180 m above sea level.
Kdaplue conditions are \ ,1 ri.ihl. . representing a mo
saic ol patches ranging in texture from clayey to
posited in two Peruvian herbaria (AMAZ, USM)

and at MO, with partial collections existing at HAP
and llir I tmeisidad \-raria I ;i Molina |M()I.. as
well as distnl inn
n Ian
q>ocialists world-
almost pure sand, and in draina$
wide.
froi
iter-
is mature, old-growth lorest. although some fialiii

trees [Ocnomrpus bataua Mart.) have been cut to
harvest their fruit
I
i
Misliana i (nnpii~<
>0
km of Iquitos when die Missouri Botanical Garden
has been conduct in- ilonu-leui Holistic inventory
ration of IIAP
and Explorama Tours S.A. (Vasquez, 1997). The
other two sites, Reserva r
(ACEER), have rati
ill
il
il
cdili-acs and
floristie composition h
, i I - ,
nr
(
evei iloneis ei (rails .<t plot species were seen, but

in common with other tropical plot inventories most
"
only l>v sterile material. At MO every collection number was first
identified to family by the first author and Ron
Liesner, with each family -el dien distributed to
family specialists (Anacardiaceae, Apocynaceae,
Rignoniaceae, Rurseraceae, Chrysobalanaceae, Dilhniaeeae. Fabaceae, Lauraceae, l.ee\diidaeeae.
Mai
luaeeae, Melastomataceae, Meliaceae, More. Myi
I
Rubiaceae, Sabiace.ie. Sapinda.
. \inlaceae). For
Mishana is e\treme|\ species-rich, with more than

]{)'/'( o| the plant species reported from the whole
of Peru (Brako & Zarucchi. I'*''..) recorded here
(Vasquez, 1997).
most species at least three fertile Peruvian collections were noli

\H >>. mosl deriving from the Iquitos Florula project (Vasquez,
1997).
Re-census of both plots was done in February
METHODS
'><>() in grid
in the Allpahuayo Reserve, sufficiently far from the
Iquitos-Nauta road (> 2 km at its nearest point) to
1996 witn l e
'
^ re-measurement of all trees and lianas. Plants 11 i
I
uiterveiiiiiy, period
ol 5.25 years were noted as such, with evident
cause of death. Each new recruit into the 10 cm
DRII class was measured, tagged, and given a
the research station (3 km) to allow us to commute

daily. Within the sampling grid, two long-term plots
were established in a predetermined location within the grid (Fig. 2) to eliminate subjective bias.
Each plot is 20 X 500 m, with each plant > 10
cm DBH (diameter at breast height, 1.3 m) marked
with sequentially numbered aluminum tags. Additional narrower samples of 2 X 500 m with all
plants > 2.5 cm DBH collected but not tagged were
madc at pre-deterniined points in the -rid: the re-
vouchers distributed to herbaria as for the original

collections.
In order to maximize potential comparability
with other forests, diversity values for each plot
were expressed in terms ol I.>111 species richness
and Fishers Alpha, using various subsets of our
data. We estimated -species richness"the sum of
the number of tree speciesas this measure is easily understood and widely reported from other foresls. \\o also estimated fisher's Alpha, where:
...
il
i ation. Phe linear nature of all our plots
species
richness
F
\h>ha
'
hill
v
oleics/\lpha)
v
'
means that they each traverse a mixture of edaphic

formations. Soil conditions within the grid ranged
from poorly to adequately drained clay soiU ("Shapaja") to well-drained white sand soils at topographic high points ("Varillal").
In the long-term plots, every tagged plants
height was visually estimated and its diameter measured at 1.3 m with diametci tape. Herbarium collections {Vasquez 14592-15829) were made in
1990 and 1991 from every individual plant (except
loi pa n tree species, winch were only collected
Fisher's Alpha values from small tropical forest

tree samples provide good estimates of the overall
diversity of each forest (Condit et al., 1998). Both
species richness and Fisher's Alpha values were
calculated on a per-area basis (i.e., for each onehectare plot), and on an aica-independent basis
(i.e., for the first 500 stems encountered in each
plot) in order to remove the complicating effect ol
varying stem density. Finally, each diversity index
was also estimated separately for all woody stems,
and lor lives alone.
once each) using extendable aluminum collecting

poles and, where n
'
lot < limbin- trees. \ lull set of duplicates is de-
In order to compare stem densities of individual

|
iveragi pel heotar. values
were calculated. The most speciose families across
Table 1. Allpahuayo forest dive

species richness and Fisher's Alpha
details.'
;;;;::
1990. for stems > 11 3 cm diameter in 1-ha plots. The values given for
the mi nimum and the most likeh ( leilinoh estimates, respectively. The
dv St,
nd lianas), and (B) for trees only. See text for further
Fisher's
Alpha
Species
Species per
first 500
Vlpha. lii-l
5(H) stems
1 \l Ml woody stems
281/293
Plots 1 and 2 combined
(>:; i
1277
l<0 1,".!!
[90/208
233/242
S64/280
Old
ooa
122 1
!64/27 i
290/295
433/444
>:\/-2M
233/242
250/255
170/1B5
199/ !08
228/23J
102/1 7f>
186/195
(B) Trees only

Plot 2
our whole sample were tabulated on the basis of

the total sp, cii-s reeo
'
degree of departure from randomness m
i
i
i) will
|. < t to soil type was
using a binomial test based on the rela
fith which individuals were rec
(dl I I sj' , ,|
Standard
i and total basal area of stems > 10 cm DBH)
computed for each hectare plot. Annual morstaixlard pr< , .lures :hat use l-.^.iritlmii.
u. : .-|:.
re, 'inlmeiii lh:,,.igh , arb u:\. tit-:\ pel :<! I f'fi li |>
et al., 1994; Swaine & Lieberman, 1987), and computed - |
111
i
K stems and for
lor each period
en
presented by the mean
mortality rates (Phillips, 1996).
be,
(I!) sPK(.ll->
I;I:II\ISS
\N
\ iu-i i-,
Because of the difficulties with identification

there is some uncertainty about the exact number
ol species in our samples. We estimated a "most
likely value" for species richness (S) by multiplying
the number of unidentified plants per sample that
could not bi alien HI 1 i in | '. ~\u . les |/ I by the
ratio of species:iinlivi<luals lor the plants in that
sample that were identified to species or morphospeeies [/{). and adding tins value to the number ol
morphospecies and species concepts actually dis-
RKSI ITS AMI DISCI SSI<>\
Of the 1277 plants in the plots in 1991, L00

were identified to family, 1249 (97.8%) to genus,
and 1168 (91.5%) to species (Appendix 1). We
made 1160 collections from the two plots, ol which
1053 (90%) were sterile, 22 (2%) were in bud, 33
(3%) were in flower, and 52 (5%) were in fruit. The
high proportion of sterile material complicated the
identification process. Vai nmph'l.- id, uliii ; : '=11
was possible only because of the large number of
fertile collections from Allpahuayo and nearby lolitiea
0 ! I
tnp 1 n at MO. For most
of tli utuderilihcd spe, ics. it was possible |o alio
cate collections to morphospecies (i.e., to allocate
ii e -lioi - to a is orpholngic .1 -|ie, ics concept, al-
. 1 1 - |) 1
M
II steii
n lui liees alone.
These reveal tha In V111 riu
plots are some of
the richest 1-ha samples ever reported. The best
estimate of Fisher's Alpha for trees in our plot 2
2 (
'In. . ver re, ordi d loi trees
> 10 cm DBH in 1-ha plots, comparing with 221
at Yanamono in Peru (Condit et al., 1998), 211 at
Cuyabeno in Ecuador (Condit et al., 1998), and 191
in Allpahuayo plot 1 (this study), all of which are
ipper \iiiazc.ruati sites, b i. 1111s ol : ubb dn do
suits of numbers of species per 500 stems, the Ml-
pahuayo plots art- surpassed only In Van.ii

i
(Phillips et al., 1994). There are also some published inventory results of. \ain>usl\. lianas. hemi
epiphytes, trees, and saplings from this part of
Amazonia (e.g., Gen i
Jl <;;'>i l> \{>')'2 Valencia
el al., 1994; Clinebell et al., 1995; Duivenvoorden
& Lipps, 1995). Tin
ii.
rial he region's unflooded forests generally have globall) exceptional
levels of diversitj fol woody plants.
\\ illiin-i oitimunih ("alpha-""! diversity n neotropical forests is closely correlated with clonaln
conditions, with the richest forests found in the hot
and aseasonal equa
I Clinebell et al.,
1995). High levels of local diversity may also be a
consequence of eh
i
hi'. i< i
pographieal and soil formations in western A ma1995) with "mass-effect"
from adjaEach All; substrates, of
i to the
high diversity values, as some species ate appaienllv specialized on each particular soil type (cf.
(c) below). However, the Allpahuayo plots were
placed without regard to forest type, so these di
versitv values arc j
;
loi
st 1-ha
patches within the Allpahuayo forest. Data are also
available from one 0.1-ha sample of plants ' 2.5
cm DBH, purposively laid out at Allpahuayo by A.
Gentry and the first author so as to only sample
clay soil forest ii
. ,
.
i, i< .nin'n.tt ,. \li)/;nl ,,,. ,., ,,..,../.-,,;'_. /
:
\
-I- (Gentry, 1988a).
Fa
, eies-rieh, and even

when healed individually tin :hree 1< guun -.uhl 1111
ilies each hav
'
species as the other
>| in-. 1 i .
taiudit (Moi - ae, Lauraceae, Arinonaceae, Burseraeeae).
The plots each traverse two contrasting soil
types, richer clay soils (the "Shapaja" series) and
pool while sand soils (the "\anllal" series), and llie
-.IK.III local edaphic e..nliasis might he expected to
ie>ult HI -mm llen-n. 1 1, i ii.i
. linn lln
plots. Because of the high diversity, lew s|iecies
were sampled frequently enough in the two plots to
allow us to test the extent to which they are habitat
i di-l
I
.MI. among the 56
species that were relatively common, with five or
more individual plants in the two hectares, a binomial test reveals that a greater number are confined to one soil type or another than would be
expected undei a mi I model ,,| cuidom distribution
(Table 3). This analysis reveals a large number of
species that an apparent specialists on the poor
white sand soils (for example, Macrolobium microcalyx, Ocotca .
\li /i/\r</>/n,vc</. Ta!
I a sniallei
s||\ confined to the
relatively rich clay soils (for example, Leonid glycu.ir/xi. I.m<! >,
'
>riir/<-hlrt,i sLnldiiana, Table 3B). Note that these results are not
proof of specialization, since apparent specialists
could arguably be constrained to one patch of forest
by chance alone, especially if they have poor dispi .1, in. .h,iu 1,1- Ihm.vei. a parallel study at
gentry.html). Here 275 species of trees, lianas, and

hemiepiphytes wei
i
u lol mdnidii
ving a Fisher's .Alpha due of .'!!(>. the higl ->: species richness and Fisher's Alpha value of all Gentry's 227 0.1-ha samples worldwide (Phillips &
Miller, in prep.).
Allpahuayo (Vormisto et al., 2000) demonstrated

that the local-scale distributional pattern of soil
types is closely related to plant distributional palterns, not only for tree species but for other plant
groups as well, and these spatial patterns are congruent anion:, hllen n
ip
This research conas in- th ;I the lot- .1 dl-li Ii IIK I d [) litem- of mam
(c) KI.OKISTIC COMPOSITION
plants within
\llpal no plots are influenced
by edaphic conditions. The high diversity of the
\||
I..
I,
. onlv due to high
intra-community diversity, but also derives from the
contrasting edaphic conditions evident within each
plot.
The Allpahuayo forest is not only very speciesrich, but also has a very low degree of dominance
by any one species. The ten most common species
together represent less than 20% of all stems (Table
2.A). Most <! die tamilies ihal physically dominate
the forest (Table 2B), such as Fabaceae, Myristicaceae, Euphorbiaceae, Sapotaceae, and Moraceae,
do so by virtue of having many species almost all
of which are present al a very lew density. The palm
family is atypical in that its status as the secondmost stem-dense family is due mostly to the high
density of one -pet i
\(>
'1
The most speciose families in our entire Allpahuayo sample (Table 2C) are the same families that
(n)
ST,UCTLRE
AND
DYNAMICS
Although the Allpahuayo plots are exceptionally

species-rich, they do not appear to be particularly
remarkable in terms of then physical structure.
This is indicated by the fact that both their stem
density and tre< basal area appear to be well within
The 10 species will
subsp. bataua
h\i:nth<rti ;</</
M\ lih- l; .:cMr
1 nfil'iir!
1 ill nil . . IKuphorl.ii.reae

Apocynaceae
I'almae
Macrolobium microcalyx
Diclinanona tessmannii
Muranda child
Sencfcldera skulrhiaria
Aspidosperma excehum
Astrocaryum macrocalyx
Top 10 species
All species
B. The 10 families with the highest density of stems >
Burseraeeae
: i milhe-
The values given are f.
Lecythidaeeae
Myrtaceae
All families
262/273
I.W/IM
Table 3. Fdaphic specialists in the Mlpahuayo plots. for all species with
was conducted to lest the null hypothesis of random distribution with respect t
Fuphnrb.accac
f.upln.,1.,.,.-. .,
Fabaceae (Caes.)
fabaceae (Caes.)
fabaceae (Caes.)
fabaceae (Caes.)
fabaceae (Caes.)
Fabaceae (Pap.)
I/<!<<! ctiianrnsis
Micranda elala
\hirrolobium bifblium
Macrolobium microcalyx
Sclerolobium bracteosum
Tackigali pt ycboph ysca
Tachigali tesmannii cf.
Swartzia racemosa var. kl
Kn-.M ,-.,.
(hnlia ,i, tplnlla

lixrsonima slipulina
Irynnlhcra ulci
Neea floribunda
Oenocarpus bataua subsr
Prunus detrita vel sp. aff
Sapotaccae
Chrysopliyllum bombycim
Malpi.-hiacea\Unsi,caccac
B. Specialists on clay ("Shapaja" soils).

Kuphorbiaceae
Cmueveiba rhytidocarpa
Nealchornea yapurensis
Senefeldera shutchiano
F.liplu.d.uceae
flacourliaccae
Lindackeria paludosa
ire from this study (Allpahuavo. 1990 census) or other sources (Mishana. Tambopata, Y
\nangu, Jatun Saeha. Belem. San Carlos de Kio Negro: Phillips et al.. 1994; Cusco Amaz
Plot 2: Liana and stranglei
Plot
Plot
Plot
Plot
1:
2:
1:
2:
Tree basal
Tree basal
Liana and
Liana and
area
area
strangler basal area
stranger basal area
mortality
reerui.menl
Annual gain
1.76%
2.21'<;
0.48%
O.o7'/,
2.08%
2..'12%
1.92%
2.2<v;
8.29%
7.24%
8.57%
8.43%
:. (><)',
Annual turnover
data for liana basal area (lianas are rarely systematically censused in ecological plots, and liana hasal area is even more rarely reported), so it is not
possible to compare Allpahuayo with other forests
in this respect. Elsewhere (Phillips et al., 1998) we
reported that tree |.
,;-.,..
creasing in the majority of Amazonian plots censused since the mid-1970s, which we interpreted
as beiii}; a pn-,-d>li . lit ! . I |..n-- . i I nil
Mm
ic ri-mig atmospheric concentrations of carbon dioxide. In this context it is interesting to note that
by 1996, both plots at Allpahuayo had experienced
small net increases in basal area (by 0.1% and
1.9%) over the 1990 values shown in Table 4, in
spite of some illega ' Hint ii p in lre<
ilhin a
few of the sub-plots. Clearly a longer census interval will be needed to confirm whether the small
change in forest structure is part of a long-term
trend at Mlpahuayo, or simply part of a pattern of
random fluctuation around a long-term stable state.
To estimate .it mi I I I MI
I >il hi
ml _i<
!
rates we excluded the sub-plots where palm trees
were cut (Table 5). Stem turnover and basal area
turnover functions measure slightly dilferenl alln-
averaged close to 2% per year in the first half of

the 1990s. This rate is not unusual by the standards
of western Amazonian forests, but it is higher than
the average turnover rate for other tropical moist
forests ( 1.5% per year based on studies at 40
i
I'll lips, 1996). Based on our small
sample of lianas and stranglers, large climbing
plants appear to turn over notably faster than trees,
hi
- . i w u
In- a i 1
i - that these organisms may have shorter canopy residence times than
most trees. Whether this pattern is repeated elsewhere remains to be seen, but if faster turnover of
lianas and stranglers is a general property of Amazon forests it would have implications for plot
luili
most o
i In
II i >i
limbers. We may
be overlooking a component of the forest that is
m<>
-ml
l
ian has been appreciated.
cerned with population dynamics (i.e., the mean of

population mortality and recruitment rates), while
basal area turnover is concerned with basal area
dynamics (i.e., the ii i n I I
da im<i\ili
ml
recruitment plus growth of existing trees). Over the
long-term an old-growth forest would be expected
to have similar values of each, and at Allpahuayo
the turnover rates of tree stems and basal area both
ecologist the benefits are clearwithout the eollaboration of botanists in the field and the herbarium
it is impossible to characterize patterns of diversity
if
I ii] i in most tropical loresK.
let alone explore the factors that determine these,
As forests become more vulnerable to widespread
i n
- - such as fragm< ntation and
climate change (Laurance et al., 1997; Phillips,
CONCLUSIONS
Our floristic and ecological results at Allpahuayo
well demonstrate the ecological and systematic
benefits that can result when we concentrate our
1997), plots arc also needed l iniiiiilui- these impacts on biodiversity. Systci
!'
mi
2.a
ileus therefore oiler . ssenlial expertise for understanding the biological effects of global change.
For 11 <- syslcmatisl 01 lloristic monographer, establishing permanent sample plots can help in undeisi.mtlmg llie lor ll llou The precise ng,nt ol . en
logic 11 -unpling forces researchers to look equally
at every plant that meets pre-determined criteria.
In contrast, perip \U In botai mi ;., n ,i\ ; nalo^ lln
weedy, common, obvious, and accessible
n
>
while missing rarer or larger plants, especially canopy tie. x. liai '
I
venlories can therefore reduce the spatial, lavonomie. life-form, and even seasonal biases prevalent in
herbaria (e.g., Nelson et al., 1990), especially win r.
! into a larger intensive colleeh
Thus, a comparison of taxa in Vasquez (1997) with
those listed in Brako and Zarucchi (1993) shows
that the intent.
i
M<-i
| n
plots and surrounding forest at several h|i.it:>- d has yielded nearly 250 taxa new to Peru. At Allnized
h to
1998) and
Lauraceae (3 species including a new genus; \
der Werff, 1993, 1997), while the repetition of p
Kalliola, R.. K. Ruokolainen, H. Tnomisto. A. I.im.a & S.

\laki. \{>(K\. Mapa gcoccologico ,1.- la zona .).- li|inlos s
variacion amhiental. Pp. 443^57 in R. Kalliola & S.
Flores Parian (editors), Geoecologia \ Dr-u-ull,, \ma
/onieo. Turku. Finland.
Kallunki. J. A. 1W4. Revision ol Ruputu, Aubl. (C.spariinae, Rutaceae). Brittonia, 46: 279-295.
I auranee. \\. F. S. F I auranee. I.. \. Iciieua. .1 M It in
km tie Meiona. C. Gascon <K T. F. l.o\e|os. I>97. Riomass collapse in Amazonian forest fragments. Science
278: 1117-1118.
Ix>wry. P. P.. II. (i. K. Sehalz & P. R. I'hillips.m. I1'')?
Maiviiuu. .1. \'>'K\. (.1 itologi'a <le la zona lie Iquito.s,

Peru. Pp. 35-57 in R. Kalliola K S. I I,,,,-. Pa,.;,,, ledilors). Geoecologia \ Desarrollo Amazonico. Turku. Finland.
McNeelv. J. A. K. R. Miller. V\. \. Meiil. R. \. Ylittermeicr
& T. B. Werner. 1990. Conserving the World's Riodiversity. IUCN, Gland, Switzerland, and Island Press,
(National Research Council. I'>'>2 ( onsen
1994; Vasquez, 1997).
IM>>
Hmdi\cr-
Yilinnal \eadeinv ol Sciences Press. Washington. H.C.

National Science Hoard. I'*K>.
ol Riluteal Hue,
sitV: A Global Crisis Requiring International Solutions.
National Science Board. Washington, D.C.
trou. F. W. 1W8. Changing geneia: Svsleiual ic sli

i Neotropical and West African Annonaceae. He
im Division, Utrecht University,
lebell, R. C, II, 0. L. Phillips, A. H. Gentry, N. '.
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, S. Ixx> de Fao, J. V. LaFra

K P. S.
from 50-ha plots. Pp. 2 17 2(7 / F Dallmeier & J.
Comiskey (editors). Fung-Term Monitoring of Biological
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Dallm.-ici. I. eK .1. Comiskey (editors). I'H'ia. Forest Bio
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Series Vol. 20. UNESCO, Paris.
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. and the Caribbean:
UNESCO, Paris.
Duivcnvoorden, J. F & II. I.ipps. 1995. A land-ecologic
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Gentry, A. II. 1988a. Changes in plant eommmnlv dm
345: 714-716.
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Conservation 23: 235-248.
. 1997. The changing ecology of tropical forests.
Biodiversity and Conservation 6: 291-31 1.
& A. H. Gentry. I'')l Increasing turnover
through time in tropical forests. Science 263: 954-958.
& J. S. Miller. In prep. Global Patterns ol I on si
Diversity: The dataset of Alwyn Gentry. Monogr. Syst.
i Bot. Card.
-& P. H. Raven. 1996.
tropical forests. Pp. 141-K
, Neotropical Biodiversity a il Conservation. Occas.
ical Garden I. Mildred
.. Matin.is Kolaiii. al Caid.-n. I.os Angeles.
, P. Hall, A. H. Gentry, S. A. Sawyer & R. Vas[uez. 1994. Dynamics and species richness of tropical
ain forests. Proc. Natl. Acad. Sci. U.S.A. 91: 28051809.
, Y. Malhi, N. Higuchi, W. E Laurence. P. Nunez
, P. J. & N. Messmer. 1999. Structure and

HonstN composition of the vegetation in the Reserve
\aturellc Int.-.air I ' , i I, !. I . \1 dagascur. Fieldiana: Zoology, n.s., 94: 51-96.
Rudas L., A. 1996. Estudio Florfstico y de la Vegetacion del
I
MN Diesis. I iiu.
nil .
. i
i
Swaine, M. D & D. Lieberman. 1987. Note on the calculation of mortality rates. J. Tropical Ecol. 3: ii-iii.
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I
I
\ l.ir.na. W.
Danjoy & Z. Rodriguez. 1995. Dissecting Amazonian
biodiversity. Science 269: 63^66.
Valencia. R.. H. Balslev & G. Paz * Mir,.,. I'H. High
tree alpha-diversity in Amazonian Ecuador. Biodiversity

and Conservation 3: 21-28.
Vasquez M., R. 1997. Fl6rula de las Reservas Biologicas
de Iquitos. Monogr. Syst. Bot. Missouri Bot. Card. 63.
Vormisto, J., 0. L. Phillips, K. Ruokolainen, H. Tuomisto
"DO \ comparison ol small-scale
(listrilputioii palt. in- <>l font plant groups in an Amazonian rainforest. Ecography 23: 349-359.
Werff, H., van der. 1993. A revision of the genus Pleumtlnnutn (Lauraceae). Ann. Missouri Bot. Card. 80:
39-118.
. 1997. Sextonia, a new genus of Lauraceae from
South America. Novon 7: 436-439.
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A SYSTEMATIC TREATMENT
OF ACACIA COULTERI
(FABACEAE, MIMOSOIDEAE)
AND SIMILAR SPECIES IN
THE NEW WORLD1
Jennifer T. Jawad,* David S. Seigle

and John K Ebinger
*
\USTU \t T
Detailed descriptions, habitat preferences, geographic ranges, and representative specimens are given (or tin- \'A lava
of the Acacia coulteri group from Mexico, Central America, and the southwestern United States. These species form a
distinct group within \<a<ia series \ulgares. lacking prickles and iisiialh I i
il. -. \ principal components analysis (PCA) of vegetative and floral features shows that the specimens examined form discrete units in plots
species. The taxa within this group are phenetiealK similar.
. n
< .1: . . .
no-.. These data also
have restricted ranges (A. compacta, A. dolulmsiai Inu. I d

.1 1 ruêlliana, A. sericea, and A.
willai(liana), but ll
Ii
I
in -in
I
r,< 1 < 1 1 u 1 an. I 1. 1 I 1
Ii
d uoithei n Mexico
(A. acatlensis, A. coullen. 1. wammifcra. and 1. salazan ). or south into Central \meriea ! I. centralis and A. usumaKey words:
\cacia coulteri group \ ,, 1,1
\c,Kid Miller seri
II
\\ îics liei Ii. (K.t
I///^//e.s. I'ai.acca
1 e.i.
1 lit
| Ii In
, i.iph
-.in- j.ui- .1 jimii.M
I, mp nenis auab sis
11
1 diets
Peduncles
tributed in tropical ami subirnpienl ivet to dry habitats, in both the Old and New Worlds. Series Vulgares broadly corresponds to subgenus Aculeiferum
Vassal (1972), according to Pedley (1978). Later,
I'e.llev 1 l'>;;<>i s i
I
axils, and flow.

ids ..1 . \lindii. al
spikes. Legumes of series Vulgares are relatively
large, strongly flattened, usually dehiscent, and
with a single row of relatively large seeds. This se, |||, t \cacia series,
be elevated to g. 1 .
1
negalia Raf. More recent systernalic -indies suggest
that Acacia series Vulgares may not represent a
moiiophyletie group M 'I i.if jpi 11 t\ Maslin. I'*"'..:
Clarke, 1995).
Most species o| [cacia s.ti.s \ulgarcs an ol diverse habitat, liabi
111
I !
1
i.-nn-li\
Most are shrubs or small trees, though some are
tree-lianas, with branches s. rambling over other
vegetation. Most species are armed with pinkies
on the stems, leaf peli I s. 11 .1
hises. Leaves arc
bipinnately compound with deciduous stipules, and
n nul Filicimn
h\ the presence of
prickles that are scattered along the stems and
sometimes I In leal raeliis.es (Benlham, 1875).
I,</.-/.-/ series I nlâres can be divided into several informal "species groups" based on overall
istence, the pres.-nee 01 abs< nee of prickles, petiolar gland shape
ami structure, as well as inflorescence shape. At
present. however, these informal groups within the
series have not been established to be monophyletie units. The taxa of one of these groups of phenetically similar species, "the Acacia coulteri
1
We acknowledge support by tin- National Science foundation (INSF HSU H2-ir>274 and NSK PCM-82-17114), the
United Slates Department of Agriculture (OICD 58-319K-0-01 1). ihe American Philosophical Society (I)SS 1992). the
University of Illinois Research Hoard (1W|). and the Rupert Rarnehy \uard l.\ the New York fiolai.ieal Carden for
DSS in 1997. We also thank the curators of the many herbaria that sent specimens, and l.ourdcs Kieo and Mario Sousa
graduate intern bv the ll..w.ud UMLII.- I ..mid.

I'll, .I-M.,,,,,. of David Clarke. Kurt Potgieter, Karin Readel,
Catherine Class, and ' I
Ii 1 1 ilo
I, 1 . I I * 1 n. 11 . the res, ,.|, ^ -r.-.il lv appic. iate.1 I'lie comments and
positive criticism of Richard Spellenberg and an anonymous reviewer are much appreciated.
-' Virginia Institute of Marine Science. Cloucester Point. Virginia 23062, U.S.A.
'Department of Plant Biology, University of Illinois, Urbana, Illinois 0I8OI. U.S.A.; author for correspondence,
d-seigler@uiuc.edu.
4
Emeritus Professor of Rotanv. Kastern Illinois University. Charleston. Illinois 61920, U.S.A.
87: 528-548. 2000.
Volume 87, Number 4

2000
Jawad et al.
Acacia coulteri Group
shrubs
group" (B/laslin & Stirton, 1997), are .
or small trees with persistent stipule- and Bowers
in rvlm.l rical spikes. Except for minoi lilllflCI). I>
in flower size and occasionally pubesct
are quite similar, with a tubular calyx and corolla.
with which spi < !.- (l tin 1 cnuii, <; grnu| in ,;.ily confused is 1.
H - < Mten. herbarium
specimens of this last species lack prickles, and
tliitsr -|MM .if?' ii- lhal lack prickle- an- sup.-tlii lath
similar to some members of the A. coulteri group.
Their separation is straightforward, however, as A.
,, nil ,,>> h - | >. i - > I * dial arc consistently less
than 25 mm long, and the single petiolar gland is
dark brown and shallowly volcano-shaped. In largeleaved species of the A. coulteri group with which
A. macilenta might be confused, the petioles exceed
25 mm in length and have petiolar glands that are
light green or yellow and not volcano-shaped,
i m< . | - ml leniifi
mi if ta\a of the A. coulteri group have been unclear in the past. No functional keys that permit accurate identification of
these taxa have been published. Surprisingly, in
most herbaria, up to half the specimens of this
group of species were misidentified. Further, a cladistic analysis based on molecular data from chloroplast restriction site analyses (Clarke, 1995), and
cladistic analyses by Catherine Glass and Das id S.
Seigler based on morphological data IunpuhlisheiI)
suggest a more ancient origin of these taxa than
other species of Acacia series Vulgarcs. Otherwise.
there are no comprehensive studies on the phylogenetic relationships of the Acacia coulteri group.
diorl-stalked pisl 1 I li< I species . h< I ,,,'

teri group range from Arizona, south through Mexico into Costa Rica. They are morphologically distinct from other species ol .!<
I "_.
(Bentham, 1875; Standley, 1920; Britton & Rose,
1928).
Many sterile and fruiting specimens of spec u-s
of the A. coulteri group have been misidentified,
adding to the ta\on< i
lowering specimc-n^
.-Ifiiia can easily be distinguished from spicate species discussed
in this work. In contrast to the A. coulteri group;
\lbizia uu\ Lysil,
'
nflorescences.
Although inflorescences of Piptadenia species are
spicate, these flowers have 10 stamens with straplike filaments and oblong anthers that are larger
than those of Acacia. Stamen filaments of flowering
ing condition. Most fruiting specimens of Piptadenia can be recognized by stamen remnants at the
base of the fruits; its strongly venose fruits appear
distinct from those nl Iracm species, especially if
comparative material is available. Careful search of
most Piptadenia specimens reveals the presence of
prickles, which are completely absent from all
members of the A. coulteri group, as well as from
members of the genera Albizia and Lysiloma. Two
spicate species of the latter genus, L. acapulcense
m I / tamtam, are - >uu limes eonl is.-d with members of the A coulteri group. For these two species.
the two parallel sutural ribs are fused around the
periphery of the pod; these ribs often separate from
the valves (Barneby & Grimes, 1996). Vegetative
specimens of st-\( i
'
- may be confused with Acacia species of this group. Some Lysiloma species haw
i
it
least on young branches) that are never found on
the species treated in this work. Finally, vegetative
specimens of Alhwi
by the palmate/pinnate venation present in the leaf |. "
(X Grin
' '
The only other member of Acacia series Vulgares
MATKKIALS AND METHODS
About 500 Acacia specimens, obtained limn 27

herbaria (A, ARIZ, ASU, BM, BR, CM, DS, EIU,
F, G, GH, ILL, ISC, LL, MEXU, MIN, MO, MU,
NY, POM, RSA, SD, TEX, UC, US, VT, WIS), were
studied to determine the geographic ranges and
morphological variation of the species in the A.
coulteri group. These specimens were initially separated into groups based on the similarity of morpholonieal characteristics. After removal of duplicate and incomplete specimens, only 15 to 25
specimens of most groups remained available for
subsequent analysis. Only unambiguous specimens
were scored and are indicated in the exsiccata.- h\
an asterisk. Of the original specimen pool, 237
were scored for 1 floral and 14 vegetative characters (Table 1). All characters were measured for
each specimen (three or more measurements) and
'
\ <
mit the use of scored characters. The data were
then analyzed bv principal components anabsis
(PCA) using NTSYS-pc version 1.70 (Rohlf, 1993).
2. Petiole pubescence (I = glabrous or nearly so, 2 =

I .ill HM ii l< Ml with appressed hairs. A
woolly pubescent]
3. Petiole length (1 = (MO mm, 2 = >I(MW mm.
4. Small purple glands on petiole, rachis, and pinna
rachiscs(l = absent, 2 = present).
f>. Petiole gland structure (I = sessile, 2 = stalked.
= absent).
6. Petiole gland apex (1 = llaltened, 2 = doughnui
shaped. .'? = globose. 1 = absent).
7. Rachis length (1
absent. 2 = 1-20 mm, 3 = >2
Number n! leallel |
l.eallet pubescence I I
glabrous or nearh so. 2
Data were transformed by a square root tram

mation (Sokal & Rohlf, 1969). Groups were i
lyzed separately, in various combinations, and
mulfaii. ouslv
Because cyanogenesis has previously *
in many Acacia species, and is sometimes useful
laMiMnmically (Sciglcr & Ebinger, 1988, 1995;
Clarke et al. 1989, 1990), all specimens were testllic higl-Augc nicil>d(fc,gKN Anger. I'>(,(>; Tantisewie et al., 1969). Seigler et al. (1978) reported
;l !. \\
ilCll.,111 III
leased
weakl)
and 1.
During
gave a
spt fllllf Us
,,<!',(, ir,.-, tllal '.
cyanide, and Conn et al. (1989) reported

i sitiv< yanide tests foi both A. acatlensis
roalti;, nsii g iii'-li . .m-di ici! |.-.ii tuab i i.il
ibc present study, no material examined
positive-test for c yam
u al
ill
When the entire set of 237 specimens was analyzed using PCA, the first tin.
nents accounted for 28%, 18%, and 17% respec-
tive^ .., u:V/c of total variance (Tables 1, 2). The

amount of variance contributed by the remaining
on if )tni. ills im inisbc I -\< w \ It MII ill. third principal c poncnt onward. The best perspective loi
ilis|
I the phenetie groupings was seen in the
oiduiahori based oi ibc set oiid and 'I if I prim ipal
I
. - plot, 13 distinct
groups, corresponding to the 13 previously defined
species can be observed, although the dala clusters
ol some groups arc proximal. Perianth pubescence,
'I 'i
|I ' AI
in
iik |. harat lers
15, 9, 1) were the tnosl iuiporlanl characters for
! for the first print axis (Table 1). Petiolar gland apex,
petiolar gland structure, and the numbei ol pinna
pairs (characters 6, 5, 8) were most important Im
the second principal component axis. The most important characters for the third principal compo!: ib. !,(characters 11, 2, 10).
between
leal
The clusters on this plot do not o

I
I i -I, Li. I,| lid. I'M .'[it toi 1.
sis said A. (loin h.
. irlv overlap on
this plot, each of the clusters is clearly separated
from the others (Fig. 1). In addition, the OTUs of
' arb group arc closclv spaced, indicating that the
species arc homogcia m.s.
In addition to those herbarium specimens borrowed, the present treatment is also based on exit i;si\t -o|ie. ] oils ' ud ohseiv ' nis ol di. s. laxa
Volume 87, Number <

^
O
I \A. coulteri
V \
A. salazari
\\
\ \
dolichostachva
A. acatlens
A. usumacintensis
in Mexico and Central America by one of the authors (DSS) on 15 trips during 1975-1998. Only
the most reliable, diagnostic characteristics were
used to distinguish i
Nil

I I
acteristics were measured carefully, and are ineluded in the descriptions, flower variation and
character overlap precludes using them for distinguishing species. Extensive lists of representative
specimens are incl
ens are commonk iinsiileiitili.'d. Also, all specimens used in
the PCAs arc included in the list of representative

specimens (designated by an asterisk after the herbarium abbreviation). Synonyms and types are in ludcd. along with maps showing the geographic
distribution of each species (Figs. 2, 3).
Occasionally, a few flowering specimens lack
leaves, or have extremely small leaves, making it
difficult to determine the number of leaflets per
pinna and the number of pinnae per leaf. Even with
these specimens, the number of pinnae per leal'of-
ichostachya
tmacintensis
Mexico. Belize, and Guatemala. The distribution of 1. centralis in the test of Central America is not shown.
ten can be determr

i
in-; lca\cs.
or by counting the number of pinna scars on an old
rachis tliat ma\ he prr-eiil. In excess ol .">()<) specimens were examined in tins study and lew lacked
leaves altogether. Most ol these were cither \cacm
acatlensis or A. sericca. Minute purple glands on
the young stems and peduncles of hot h laxa distmguish them from other memhers of this group of
species. Acacia acatlensis is then separated from A.
sericca hecause the former's ealsx and lloial hracls
an- only lighllv appressed pubescent, whereas, in

the latter. the cul\\. corolla, and floral hracts are
densely SCIIC.MII> puheseenl. Two other species
have these small purple glands and occur within
the same geographic range. Acacia campacta is a
small shruh with short shoots, and .1. mammifera
is a small tree with flowers that have cream-colored
corollas with a purplish tinge. However, these are
only uncommonly found in flowering condition
without leaves.
KE\ TO SPECIES
la.
Pinnae mostly with more than .'i(> pairs ol leaflets, especially ihose near the middle of the rachis.
2a.
I'.-t i.d.it gland(-) llallene.l. usually located .MI the lower thud of the petiole: leaflet apex obtuse to broadly
Ah.
Leaflets mostly less than 1.2 mm wide: most leaves with 0 or fewer pairs of pinnae
2. 1. dolichostachya
2b.
I'etiolar gland(s) saucer-shaped to cup-shaped, usually located on the upper half of the petiole, rarely
lacking long hairs on the lower side at the base

4b.
lb.
A.
1. acatlensLs
Minute purple gland- ah-enl: leaflel- u-uall\ with lung hair- on the lower side at the base
Pinnae mostly with lewet than .'>(> pair- ol leaflet-, or pinnae absent.
5b.
Leaves more than M) mm long: short shoot- ah-enl: pinnae -oinelun. - absent in
6a.
\racm willardiana.
Leaflets appressed to erect pubescent on both surfaces, usually densely so: uiiiinle purple glandcommon on the rachis and pinna raehises.
7a.
Petiole ami rachis densely
pubescent with erect hair- about <>..'? mm long: petiolules less
than 2.1 nun long: fruit pubescent

7b.
6.
I. scu,,;i
Petiole and rachis glabrous or with short, appressed hairs: petiolules more than 2.0 mm
*
+
x
durangensi
Acacia mammifera
Acacia millefolia
Acacia russellian,
fc fV>
A-
8a.
Petiolar glands r
8b.
Petiolar glands s
in"70 mm long.
s exfoliating and papery; petiolar glands absent

jminate
11. A. salaz
i's smooth to furrowed, nol e\lolialing: p.-tiolai
il lieneatli: raeliis and pinna raehises puberulent
12. A. coul
raehis and pinna raehises as well as perianth
1. Acacia usuiiiaciiitensis I.undell, Contr. Univ.

Michigan Herb. 4: 8. 1940. TYPE: Mexico.
Tabasco: Boca Cerro on the Rio Usumacinta
above Tenosique, 1-5 July 1939, E. Matuda
3550 (holotype, MICH!; isotypes, K!, LL!,
MEXU!, MICH!, NY!).
Tree to 30 m tall with bark dark gray, shallowly
furrowed; twigs brown to greenish brown, not ll< \
uous, glabrous to lightly puberulent; short shoots
ahsent. I.ca\es alternate. 00-200 mm long; stipules
herbaceous, light brown, narrowly triangular, to 2.2
X 0.5 mm near the base, glabrous to lightly pulieruleiii. persistent; petiole adaxially
i i
grooved. 30-70 nun long, glabrous to lightly puheiul.nl; petiolar gland solitary, usually located on
the lower third of the petiole, sessile. eomrnoiiK
elli|ilieal. I -() mm long, flattened, glabrous (Fig.
4B); rachis adaxially grooved, 50-140 mm long,
glabrous to lightly pubetuleul, a sessile, sauoersha|.e.l gland, 1.0-1.9 mm across, between the upper puma pan: pinnae 7 to I.> pairs per leal. .V.
90 mm long, 5-12 mm between pinna pairs;
petiolules 1.7-3.0 mm long; leaflets (33i3o to 55
pans per pinna, opposite, 1.0-1.6 mm bet van:
lets, oblong. 1-7 X 1.2 1.0 nun. glabrous lateral

\ tins obvious, wild a mi.heiii an.I I lo .1 smaller
veins In.III tin base, base oblique, margins ciliate,
.red c\ lindrieal -pike 50 I I
clusters; peduncle 7-15 X 0.7-1.1 mm. puberulong, puberulent, early deciduous. Flowers s,..ssile.
creamy-white; calyx 5-lobed, 1.1-1.5 mm long,
denseb appressed pubescent; corolla 5-lobed, 1.82.5 nun long, densely appressed pubescent; stamen
filaments 4-6 mm long; ovary glabrous to lighlK
pubescent, on a stipe to 0..3 mm long. Legumes
light yellowish brown to dark brown, straight, flattened, oblong, 90-250 X 20-33 mm, cartilaginous.
aiisvers.-lv striate, glabrous, eglandular, dehisi-nl; stipe to 22 mm long; apex acute. Seeds unieriate. no pulp, dark reddish brown, oblong to
val. si.ongly flattened, 8.8-10.0 X 7.0-9.0 mm,
mooth; pleurogram U-shaped, 3 1 mm across.
lowers: April-June.
Distribution.
Moist
tropical
forests,
along
elevations iii Belize. (malcuala. and the states of

i in . Ii. ( 11 .111.1- < )a i
I ihasco, and Veracruz, Mexico (Fig. 2).
nam 'oinpo'ici:) nl Ion iaial tropic; I t;ni:T>r>.' - in
l.nah tua. > an 1 -<> 11Ii. :n \h \a ... \o -.pecimen-. ot
this species have been observed by the present authors farther south than Guatemala and Belize.
Specimens labeled /
gua are the result of confusing
ions species of Lysiloma. Act
specimens are commonly inisidenlilied as /,. <
pulcensis (Kunth) Benth. Thompson (1980), in e
vision of Lysiloma, annotated the type of A. \
macintensu as L. acapulcensis. This specimen
Matuda 3550), however, is A. usumacintensis, 1
ing numerous separate filaments remaining at
! of the fruits.
Reprea
111 I l/I'. Kl Cavo Dist.. Berique Viejo. Km Mop.m. Cm,
treras 7089 (CAS. F. 1,1.. MO*. M ): sicinitv Oorgeville.
Western hnv.. Duvcr 12662 (MO. I S*l: \alenlin. Kl (,.v...
/,,/,// (,:!.->(, (K (-11. MICH*). CI \TKM\I.\. l/.abal:
Puerto Barrios, ea. 20 km from town mi llie mad |., \],i
.In.i- Maisliall Castillo & Marshall 72.':* (MO \ ^ I
IVlen: I a. a in loll, alioul 2 km S. Cmiitrms 3167 i< \^.
I-'. I.I.K MO): Maeanehe. Cwiln-ms 7*179 {V. MICH*. I S):
D..s I iiL-u.ias. 19 Apr. 1969. Cimtrrms 8356 (F*. 1,1.. MO):
I'ikal. in ramonal on Mam I'la/a. /,,/,/,// /.l,'//,' M W.
I. I.I.. MO. Ml: likal. around \y,ada l,kal. /..,.///
/.W.'* |F*. IF. NY): SaNaxrhe. in eon./al about 5 km S
ot Milage. I.IUKIVII 111971 I K FF. MO. \ I *): Cadrna-.. on
river bank bordering Rio Craeios. IMMMI A f <;'/.',
/'W.,'.,' (I . II.. \\,. MIAMI). Campeche: Fl tormento
Fseaircga. Sous,,. Cahrrra. Dnridsr A Clmler 12369 (IFF.
MO i < hiapas: \\ s,d, ,1 I a,,,,,., Muama, I. of San
Quintfn, Hreedlove 33387 (OS*. MICH. MO): 20 km al side la d.-M union San Javier Frontera Fchevema haeia Rio
I . .
/ I'a 77,', (I IFF.
K.leVo. San Juan Chamnla , ammo a Kean. 1/,,,/me. .V

Giron 6288 l\|OC Ml . Oaxa.n: I!
Bam!,,, al O
deSalinaCruz. l/rirn7,e-nl; iMOO. Tal>;iM-o: Man. lial
fo. Calzada 2385 (V*. M I: la I'a I ma. lialan.-an. 1/.;///,/u
3-121 (K MICH". WIS). Wra.-ni/: M,MO. M,natulan. In
mas al SW de Fa Garganta. S. km al \V de Uxpanapa.
i >bos& Vavarret, 112 il MM II MO IIA.
2. Acacia dolichostachya S. F. Blake, Proc. Bml
Soc. Washington 34: 43. 1921. Senegalia dolichostachya (S. F. Blake) Britton & Rose, N.
Amer. Fl. 23: 112. 1928. TYPE: Mexico. Yucatan: Las Bocas de Silam, May 1916, G. J.
Gaumer & Sons 23329 (holotype, F!; isotypes,
F!, G!, K!, NY photo!).
brown to greenish brown, not flexuous, glabrous;

diorl shoots ihs II Fcavi
liernate, 10-120 mm
long, slip lies beib.
on... light brown, uannwlv In
angular, to 1.3 X 0.3 mm near the base, glabrous.
persistent; petiol,
o\|\ grooved, 3080 mm long, glabrous; peliolar gland solitar\. located on the lower half of the petiole, sessile, circular to more commonly elliptic, 1.0-2.5 mm long,
llalletied or will - ighlk iai>ed maigius. glahmu
(Fig. 4C); rachi-
laxi
20-62 mm long,
0.6-1.5 mm across, between the pinnae ol the upper 1 to 2 pinna pairs; pinnae 2 to 6(8) pairs per
leaf, 40-75(90) mm long. 49 mm between pinna
pairs; petiolules 2.5-4.0 mm long; leaflets 36 to 65
pans per pinna, opposite, 0.7-1.1 mm between leallets, oblong, 3.5-5.5(7.5) X 0.8-1.3 mm, glabrous,
lateral veins usually not obvious, only one vein
from base, base oblique, margins ciliale. apex acute
to obtuse. Inflorescence a loosely flowered cylindrical spike 20-90 mm long, 1 to 3 from the leaf
duncle 3-10 X 0.5-0.9 mm, glabrous to lightly puherulent: involucre absent; floral bracts linear, to 1
mm long, glabrous to lightly pubescent, usually not
deciduous. Flowers sessib-. creamy-white; oalvx 5lohed. 0.5-1.0 nun long. liglilK appressed pubescent; corolla 5-lobed, 1.2-2.2 mm long, lightly appre.ssod pubescent; stamen filaments 3-5 mm long;
ovary glabrous, on a stipe to 0.3 mm long. Legumes
light yellowish green to light brown, straight, flattened, oblong, 80-130 X 13-20 mm, cartilaginous,
transversely striate, glabrous, eglandular. dehiscent; stipe to 12 nun long, apex acute to acuminate.
Seeds not seen. Flowers: April-July.
Distribution. Common in thorn-scrub thickets,
and disturbed dry forests in the lowland- ot lInstates of Campeche, Quintana Ron, and Yucatan
(Fig. 2).
Restricted to the Yucatan Peninsula, Acacia dolI'hosiailiva appears to be a relatively common
component of thorn-scrub thickets and disturbed
sites. The fact that most leaves have fewer than
seven pinna pairs separates A. dolichostachya from
most other species of this group. Other species with
six or fewer pinna pairs differ by having pinnae
with fewer than 35 pairs of leaflets, along with
smaller leaflets (A. compacta), much longer petioles
- I
', imi). >i pubescent haves (A. mammiConsidering the restricted distribution of this
species, the only other taxon that A. dolichostachya
might be confused with is A. usumacintensis. Both
taxa have more than 35 pairs of leaflets on each
I 11
ILL
I iltcn. .1 |.< 'lol ii glands ..in tin- Inwci
ILIII
oi
mill i .!: I hr\ aic rasib - r\ >,i; . ,!e!lch,>s

huh \> llian 1.3 mm long),
less distance between the leaflets on the pim:a i
chis (less than 1.2 nun), ami small.-i sepals (moslb
less than 1.0 mm long).
Representative specimens.
MEXICO. Campeche: 4
Chan & Ucan 1023 (UC*); a 12 km al K de Constitucion,
Hancho San Kelipe. ;
;/.>/; (MOM: a 12 km al K de Carrillo Puerto, ruml.,, a

NW de I aillllo I'll, rtc. solne cl rami
i \ iim. Chin,.
Cahreia X Cahrera If Hit) (MUM; >-n el km 2 del rain,,,,,
!
;i ,:'lm<le,lX:H,,,,n,lil.->\\\0*)::\- I mi. S of Kilipr
I an,ll.i I'uerto. Ihcyer. Spcllman. \aiighan & Wunderlin
25,", (MOM. ", km ill \ d.- Puerto Morelos. Crelhe,. (Jam,
X- Hans 1331 (MOM: a (. km al \ ,!e Puerto (lr Mo.elo>
a Ca.ie.in. Sou.sa. Telle: & Cahrera I WW (MO*): a IK
lumal I. ( arrillo I'll,-it,,. sobte rarr.-t.-ra Mrrida OaCorla.

felle: X- Cahreia 2012 I MO*): a 10 km al S de Tuliim.
7W/re * r;fcfYT 2032 (MO. M *): a I r> km al \ ,lc lia-
Puerto, Ucan & Fk >res W5 ll CM. Yucatan: 11.

N of Dzibilehaltum ti ini on road from Merida lo Pi,
- I2'H iMil. WM: t.O kmal
era '1 I/.IImi, M, in 1 .
-era 13203 ( MO*): ne.
\ LL, MICH*. MO. 1 S): 7 km al S de V.xraba. \ar<
s & Isely 574 (CAS, 1F* MO).
3. Acacia a<atl nsis |;< i ; i. London J. Bot. 1:
513. 1842. Senegalia acatlensis (Bentham)
Britton & Rose, N. Amer. Fl. 23: 112. 1928.
TYPE: Mexico. Puebla: Acatlan, May 1830, G.
Andrieux 396 (holotype, K!, F photo!, MICH
photo!, NY photo!, TEX photo!; isotypes, G!,
US!).
Senegalia siihmonlana Hrillon X Hose. \. Amer. Id. 23:
113. 1028. TYI'K: Mexico. Oaxaea: Cerm San \n
tonio, alt. I8(K) m. 12 Oct. 1907, C. Conzatti 2046
(holotvpe. US!; isotypes. F!. MKXU!, NY!). IBritton
and Hose (1028) listed the type as Conzatti 25,346.
specimen was erroneously printed 25,346."]
Shrub or small tree to 15 m tall with bark dark
gray, shallowly furrowed; twigs light brown to
gr.-< iiisli blown, not Ik a., i-. r I ibmus lr ighlk p i
hei limit; dmri slioi is absent. 1 ea\< s allcuale. "

I.")() nun lm:g: stipules |; rbaceu is. ighl bn mi.
narrowly litn-ar. In 3 0.M mm IM'.II the has.\ usual \ glal ! is. pi isislri : pi ! i. >[. ; d . ill I s d I ,u l\
grooved, 15-40 mm long, glabrous, but commonly with iinnu'e [unpli dan I-. p. M..I.11 Jmd
In
i
I.
ii h l
. i pun, i pairs 01
,ili .; the ippi'i lialf :>f lln p. Moli . sessile, nearly
circular to slightb elongated. 0.7 -2.3 mm long.
saucer- to cup-shaped, glabrous, rarely absent; raehis adaxially grooved, 20-110 mm long, glabrous
lr. Imf,!l\ puberul. nl 'ii d isualb with ininule pur
pie glands, a ses-dr. cup-shaped gland, 0.4-0.9
mm across, between the uppei puma pan; pinnae
7 to 30 pairs per leaf, 25-60 mm long, 3-7 mm
I.. IHIVI, piiui i pans; peholules 1.0 2. I nmi long;
Ii. ailds .'.(> to (>{) pans pel i iin,,i. >pposite. 0.5 1.2
mm between leaflets, linear, 2.5-4.8 X 0.7-1.1
mm, glabrous and commonly light greenish purple
sii all,-: -, eitis from ihe b.is. ., ! is. iibln|uc. margins
cence a looseb Mowercl c\ lindi led spike 10 100
mm long, 1 to 4 from the leaf axil; peduncle 5 10
X 0.5-1.0 mm. glahi
I lill | .1 , i nl n d
c immoii - '.Hid - ;!||eii-..l mini,', p is ::! g ; lids: in
volume absent: Moral brads lunar, to 1 mm long,
early deciduous. Flowers sessile, creamy-white; calyx 5-lobed, 1.0-1.6 mm long. I hi! ippi
d pu
bescent; corolla 5-lobed, 2.1-2.8 mm long. Iightb
appressed pubescent; stamen filaments 4.5-6.5 mm
long; ovary glabrous, on a stipe to 0.1 mm long.
Legumes light to dark brown, straight, flattened, ob :
! 2"i mm
lilaginous, transversely striate, glabrous, eglandular. dehiscent;
stipe to 20 mm loiiiC. ape\ bloadls acute. Seeds
uniseriale. no pulp, dark reddish brown, oval,
strongly flattened, 7-10 X 4.5-7.2 mm, smooth;
pi, i.m'.iain 1 -shaped, 1.2-2.3 mm across. I lowers:
M.nch .lime
Distribution. Dry, deciduous, tropical forests
and thorn-scrub forests between 500 and 2100 m
elevalions m the slates ol Chiapas. Cuerrero. Jalisco, Mexico, Michoacdn, Oaxaea, and Puebla,
Mexico (Fig. 2).
Acacia acatlensis is very similar morphologically
lo 1. centralis. Hi tli aie \\i !e|\ ilislnb it- , I n so ill,
ern Mexico, although A. centralis has been collected more frequently in the very south of Mexico and,
unlike 1. acatlensis. it occurs across the border in
Guatemala and countries to the south (see Fig. 2).
These two species are difficult to separate, and it
is possible that they should be considered as subspecies of a single species. The two can be sepa-
Volume 87, Number t

filled based (.11 the preset...- 01 absen. . ol iniiiiih

purple glands that are common at the base ol the
leaflets, in the grooves of the rachis and petiole,
and not uncommon along the axis of the inflorescence in A. acatlensis. Rarely these glands are
clear, la< king the purple color, hut are easib <>bserved under mauinliealion. None of these minute
J in I- ,ven found on -;pe. .mens if .4. centralis examined. No other characteristics could be found
thai . onsist. nil
| i i.
i
i
n I, i !
most specimens of A. centralis have leaflets with
long hairs at the base on the ventral surface. These
hairs are particul n
i l u
i <i I. ini falling off as the leaves mature.
hid in- K
. (less
. ()a011 the leaves, \raciu iirallrnsis is easily separated

from A. mammifera, which has fewer than 33 pairs
ol leallets per pinna, leaflets that are eommonb
more than 1.5 mm wide, and a stalked petiolar
p< tioli - unl h
from A. acatlensis.
- lln- spi
ii -
KrnHsmlaluc spmmcns. MKXICO. Chiapas: a 4 km

ill SV\ <le loliman. *ousa. Konoimoortln. (.ortes A lln
ndndei 11824 (MO*, VEX). Guerrero: Tari.i. Covuea
Dist. Hinum "55 IDS. (ill. MICH. Xt. I S): en el Puerto
Kl Salad.,, a 7 km al \ de Tlapa cammo a Hi.amuxtitlan.
Marline: Khli |M<). Il\-i. Jalisco: 2 km al \\ <le Kl
Mnador. 10 km ill XK ile Kl Coreol.ado. carrel,-.a \i.llan
( ;L..I<I.IKI|.M.I. Magallanes 2/69 (MO*): a 20 km al Xtt de
S;in Patricio, \hif-,
<
20 km XK of Villa... Mrlmigh 23271 <MICH*. MO. N^l ): Uarranca ,le l.os
121 I MICH*). Mexico: Pungaiainhn. Trmas.iiltepcc Disi.. Hiniun 1717 (K 1,11*. MO. \Y. IS). Mirhoaran: 3 km al S de Jimgapeo. Soto. \ttirolcn. .\7n/
X- I'izanas ,",573 (\1K\l *>. Oaxara: 5 km -ol.ie I., <lesM.-ieion ii Uarranca de I .ON Calalia/.os. \guilar 220 (NY*
i Huajuapan, Cabada
Ramos & Magallanes 11 (CAS*. II.. MO): 3

pan. (hlu flermude: 2"I iMKXl*): Tomellm Canvon.
Pringle 5885 (CH. MICH. IS*. \ T): cerca ,le Tonala.
Rzedowski 34920 <C\S'. MO): S.ilmk. a la. Hi.ii.a-. .lei
i .-no (.,..,..:..la. Torres. Torres. Carte: X Man,,,, <>2l\
iMOMiK.iliTilOnentc.lelCerrotauengola. Torres. Tones.
Te-lle: & Marline: 400 (MO*). I'uehla: Trprji de H..driguez, Felger 85-38 (MO*): 20 mi. SK of Aoatlan on hwv.
190. Seigler & Maslin 12692 (EIU*, ILL).
4. Ac
lia centralis Britton & Rose, N. Amer. Fl.

L13. 1928. TYPE: El Salvador. Near San
idor, 1923, S. Calderon 1774 (holotype,
XV isotypes, BM!, F!).
Tree to 25 m tall with bark dark grayish brown,
verliciilK fissured, rough and scaling; twigs light
! own Li vici i ish hfiivvn. i ' ll M.-> is. it.osih !.)
btous. short shoots absent. Leaves alternate, 70herbaceous, light brown,
4.5
the base,
idal>tou>. persistent; petiole adaxially shallowly
grooved, 18-46 mm long, glabrous to lightly pubenileut; petiolar fflan.1 -olilarv. located on the
middle part of the petiole, sessile, usually circular,
1.0-2.6 mm across, saucer- to cup-shaped, glabrous, raclus adaxialb umo\e.l. 10-150 mm long,
"labrous lo puberulent. a sessile, saucer- to doughnut-shaped gland, 0.6-1.3 mm across, between the
pinnae ol the upper 1 to 2 pinna pairs il-i-. Ill:
pinnae (7)1 1 to 24 pairs per leaf, 30-70 mm long,
3-9 mm between pinna pairs; petiolules ().{! 1.5
mm long; leaflets 40 to 60 pairs per pinna, oppo3.0-5.5 X 0.6-1.1 mm, glabrous except for usually
some long hairs at the base beneath, lateral \eir.s
obvious, with a midvein and 1 to 2 smaller veins
from I he base, base oblique, margins cihatc apex
narrowly acute to acuminate. Inflorescence a loosely flowered i \ lindi leal spike 60-140 mm long, 1 to
.'; Irom lli> leaf a\i<. ,,r it. terminal racemose clusters; peduncle 4-10 X 0.5-1.0 mm, glabrous to
lightly puberulent; involucre absent; floral bracts
linear, to 1 mm long, pubescent, early deciduous.
Flowers sessile, creamy-white: cabx 5-lobed. 0.7
1.3 mm long, lightly appressed pubescent: corolla
5-lobed, 1.8-2.5 mm long, lightly appressed pubescent; stamen filaments 4.5-6.5 mm long; ovary
ulabroiis. on a stipe to 0.3 mm long. Legumes light
brown, straight, flattened, oblong, 100-160 X 1628 mm, cartilaginous, transversely striate, glabrous.
i II
r, dehiscent; stipe to 20 mm long; apex
broailK acute to obtuse and usually api. ulate
N.eds uniseriate, no pulp, dark reddish brown.
nearb circular, strongly flattened. 6-9 mm across.
smooth; pleurogram U-shaped, 1.5-3.0 mm across.
Mowers: April-August, and sporadically throughout the year when moisture is available
Distribution. Lowland forests, and moist disturbed sites below 1300 m in Guatemala, El Salvador. Honduras. Nicaragua. Costa Rica, and the
stales ol Chiapas, Jalisco, Oaxaca, and Sinaloa,
Mexico (Fig. 2).
A tall tree, sometimes entering the canopy of
iiioisi lowlan ' lot. s' I, t, -.; entxilis is also a
coll.- -hulls ale lioln t ;|.|si(|.-s. ilislnihrtl j>as! i :IV -.

an.I gallery loresls. In addition to its close morphological similarity to Acacia acatlen.sis di><ussed
above, .1. centra
acacia species in southern Mexico. Of these, it is
easily separated Irom 1 com
ml 1
/era. as these species have fewer pinna pairs per
leaf (fewer than 7) and fewer leaflets per pinna
(fewer Ili.in 30). The .-reel hairs of A. sericea, the
larger I. allots ol 1 ,, .,, ,/,,./, ,-M., ant I I he exlol I
aling hark ol 1. *,//,izari can he used to distinguish
these species from \. centralis.
The authors have frequently encountered specimens of 1. centralis dial .v etc annotated \ihi:iu i.io
poides (Benth.) Burkart. Flowering material of these
two taxa is easily separated by the filarm-i i.I<
and leu ei slat
i , )
| ninii, i
rial ml
sterile specimens also can he separated, as in A.
centralis, llie leaflets arc less than 5.5 nun long and
have an aeuminate apex, whereas in Albizia niopoulcs. the leaflets are longer, mostly more than 5.5
mm long, and the apes is I.madly acute to obtuse.
Representative specimens. COSTA RICA. Guanacasle: viemilv ol (.ana-. Ihiiihvnn.ur 77~> I f ' I: Smla
l!i,sa Nahniul Park. Jon:,;, IO.',7,7, (MOM. Punt :iren:i.:
San Luis village, llaher - Hello 1628 (MO*). LL SALVADOR, vioinilv of Oomasagua. \llen X \rmoin 727,7 (L
LL. NY. US*). 01 VI KM \l.\. IVlrii: Lamina Vixja.//"/
HlfJ/l tf Miwf 2,no If. Ill /ncapa: <n,il.,n. /J, ,.-..-/
;>/ (A. K (ill*. MO. NY. I'C. IS. \T|. NONIHKAS.
.'.'..' ,\>
I'arai.o: I
km
- l I I
P.M...-.
W,./,
/.,-;/ |\. \1I< ll>. M. I si. Jalis.-o: r, km a! SI- ,le La

Ms,
I'm ^,M HarlnK
Nai.tepec. UacDoucull II27UI (MICH. M *); between Lrmon and /. le. l/, 7>oag// .s.. (NY*. US) Sinaloa:
\lY\Ol \ !.(..: \
ira, Pu.ila LI Dia-
A Hi.-. \ \lliei. LI. I'M

81. 1928. Tll'K: Mexico. I >axaea: Toinellm. N-pl.
L905, 7. /V. flow /0082 (holotype, NY *!. F photo!.
MO photo!).
Shrub or small tree to 3(4) m tall with bark dark
ma\. Making off in llini strips; twigs light brown to
dark reddi di br. wi . -hghlb II. xin.us. pubescent to
glahioi.s uli, ii \oiitii M ilh mill il> p 11 pl> i lands;
short shoots coiniiioiib present above the nodes, to
3 mm long, covered with aeuminate stipules and
old leaf bases. Leaves alternate, also coinnioiib
clustered on the short shoots, 5-30 mm long; stipules herbaceous, light brown, narrowly linear, to 3
X 0.4 mm near the base, usually glabrous, persistent; petiole ada.xiallv grooved. 2.7, I 1.0 mm long.
iisuallv pubescent and with minute purple glands;
i d solitary. lo< at. d il oi just below tinlower pinna pair, sessile. . u< ular. 0.4-1.1 mm
'i. Ill >. ra. his
adaxialb grooved, 0-20 mm long, usualb puhes..er slmped gland. (1.2 ().(> intn i. ross. occasionally
present between the upper pinna pair: pinnae 1 to
O pans per leaf. O I!, mm long. 2 5 mm between
pinna pan-: peliolnles 0.5-1.1 mm long; leaflets 9
to 22 pairs per pinna, opposite, 0.5-0.9 mm distance between leaflets, oblong, 1.4-3.0 X 0.5-0.9
mm, glabrous above, usually hghtlv pubescent beneath with lonu hairs, lateral veins not obvious.
only one vein from the base, base oblique, maigius
usualb ciliatc apex acute to obtuse. Inflorescence
a loosely flowered cylindrical -pike 30-70 mm
long, solitary (rarely 2 to 3) from the leal axil: peduncle (i Id X 0.4-0.7 mm, usually pubescent and
with minute purple -land-, involm re absent; floral
bracts linear, to 1.5 mm long, pubescent, early deciduous. Flowers sessile, creamy-white; calyx 5lobed, 1.1-1.7 mm long, densely appr.-ssed pubescent; corolla 5-lobed, 2-3 nun long, densely
appressed pubescent; slamen filaments 5.5-7.5 mm
Legumes light yellowish brown, straight, flattened,
oblong, 50-120 X 10-16 mm, cartilaginous, transversely striate, ujahious. .-glandular, dehiscent;
stipe to 8 mm long; apex acuminate and usually
beaked. Seeds unisei late, no pulp, purph-li blown.
near circular, strongly flattened. 5-8 nun across.
smooth: pleurogi in I shaped. 1.3 2.2 mm across.
Flowers: April-July.
i in the states of Puebla

(Fig3).
Acacia compacta, a much-branched shrub thai
rarely exceeds 3 m, has a very restricted di-lrih.
lion, occurring i - i
h . \ i
jam
Oaxaca. Even there it does not appear to be a common species. relahveU llltle inalenal I- -1 j i_ .:..! I
ncd is from xeric
habitats, usually on rocky slopes and in washes.
where A compan
k. Is Kieo \r. e
& Rodriguez, 1998). The short shoots at many of
ihe node-, small ! ilk I- In i stl I -- ! n 2 "> n n
long), leaves that are less than 30 mm (mostly less
- .
ih the apex acuii.male al:d beaked, .-epaiale 1. . .>mm ,-,.. |. ,, ,,[,
km al SK de San Rafael. Sousa, Sousa & Basurto 10430

(CAS*. TLX): Cerro Tepetmja al Stt .le \MNU. 1,-nonn
I ''/. (( \s I; [ardni Roia,
I, < a, I i. . a, v
Su< ideal i- .1, / i| I i!
In-'
A Mat-da 7I I liS \. TLA ! I: Janlin Rotamco <le Caetaeeas
\ Sueuleiiias (le Zapotitlan de las Sa""
A Mania 70(> (RSA*).
er members of this group. The presence of short

-hoots is probnhk an adapt hoi: :e \ei r ,ndi' ore.
Acacia compacta shows variation with regard to
several important characteristics. Leaf size is highly
variable: the leaves that develop on the short shoots
are nsualK smallei and have shorter petioles and
4: 85. 1910. TYI'K: Mexico. Puebla: Cerro de Solunte, alt. 700O-8(KK) ft.. June 1909. C. A. Purpu.s
3863 (holotype. UC!. MKXU photo!: isotvpes. RM!.
MO!. NY!, US!).
fewer pinna pairs; whereas the leaves that form on

times reach a length of 14 mm, and 5 or 6 pinna
pairs develop along the rachis. The shape and
simetuie <:(' (hi p.e'iolal -lam! is also -oini v, >i: i , a'
iable. The majority of the specimens have a sessile
i ii< r land that is doughnut- or loin
although a lew specimens have a -i.iIk- p
Ceia-rall
h.-s J i
are ioiuid on young leaves forming on the short
shooK. o|>it i h A\- - \i ,\. -e~-d< . di I. Jn ill -h ip< d
glands. It is possible that Acacia compacta may
rarely hybridize
alkc! petic
. ,,,imn,s
,.(i,
s.',
>,
MLXICO Oaxaca: 52 km
'. I
Ml \i
II \
km al W de San (..,l..i.-l. Salma* A Ramos F-3857

(ARIZ*. F. MKXl . I!S\); I 1 km al \ delaiieollan. .S;,.,.
Martinez. Telle; A- Magallanes .>W I [C \>-. I S. V\ ISl: a
0 km al !\W de Cuadalupe Los ()l,s. ,. sea a 10 km al
\\\ <le Cui, .il.i M, ' '
1/
!>'-,.
' 'V.
(,<>I2 (MICH*). Puebla: Mrededores del la,l, \Y del
pueblo do Axuseo. Cluantx. Salinas A- Dorado F-2466
1 Mil/. MO. RS\*|: en la des\iacion a San Luis Atolotitlan v Los Reves Metzontla. Medrano. Chiang. Darila A
I,,', ,.,'', \RI
MO l. II'. km .d \W deTeotitlan
del Camiiio. i I. Ii . m <
Km: A Since, F 1172 (MO*): vicinih of San Luis Tultillanapa. l':Vns !l"3 (L Oil*. MO. XV I C. I S): ., km
al SK de San Rafael. Rico. Kama* A" Hernandez 2U,
(CAS*. MO): Cem. de La Ksealera. Kjiilo (le San Jose
I I
.
i< \s\ MO): 1 km
.,1 \L.-I. del limite estatal Oaxaca-Puebla por la eanetem
lluaiuapan ,le Leon-Tehuacan, Salinas & Dorado F-3199
(K*); a 2 km al SL ,le San Rafael. cerea de los limites
Puebla-Oaxaca. Sousa & Sousa 10105 (ARIZ*. TLA): a 2
;ns & Galeotti, Bull. Acad.

Roy. So
10(2): 311. 1843. Sene:ns & Galeotti) Britton &
Rose, N. Amer. Fl. 23: 111. 1928. TYPE:
Mexico. Puebla: Tehuacan, alt. 6000 ft., May
1840, H. Galeotti 3345 (holotype, BR!; isotypes, K!, P!, MICH photo!, NY photo!).
;
.,, ,-- !w-!>!,;,:,
ii .;i I
I ni\
lil irni
Pul I
Bol
Shrub or small tree 3 to 4(6) m tall with bark

dark gia\. erac ked ml liss ued. Lie ku . ,v. \ i d
1 -.i\ a:g d, rk :a;rpli-h L-oun. sm.!(>lh areas: twigs
dark brown to purplish brown, not flexuous, glabrous to lightly pubescent; short shoots absent.
Leaves alternate, 30-120 mm long: stipules herbaceous, light brown, narrowly linear, to 4 X 0.4
mm near the base, glabrous to pubescent, sometimes tardily deciduous; petiole adaxially grooved,
10 30 mm long. dens. I\ pi.beseen: uith erect bans
and scattered mim.h pun
-.lands: petiolar gland
-,. tar'., loi al( d a OIIIJ lh< iq.pei ! Il T the petiole.
sessile, circular to elliptic, 0.6-1.2 mm long, sau- ip lii ip
ped, glabrous, sometimes absent; rachis adaxially grooved, 15-100 mm long,
pubescent with civet hairs and scattered minute
i
J aids, a sessile, saucer-shaped gland, 0.51.1 mm across, between the pinnae of the uppei I
or 2 pinna pairs; pinnae 5 to 13 pairs per leaf. 25lules 1.5-2.1 mm long; leaflets 14 to 35i 11) pairs
I . : im an. ..pi.osile. (1.7 I. ' mm mlei wd !-- ' a
obvious with only one vein from the base,

base oblique margins ciliate, apex acute to obtuse.
Inflorescence a densely flowered cylindrical spike
30-80 mm long, solitary Iron
n
cle 3-20 X 0.7-1.2 mm, densely pubescent with
erect hairs, involucre absent: floral bracts lineal, to
3.5 mm long, densely pubescent, deciduous. Flowers sessile, creamy white; calyx 5-lobed. 1.5-2.2
mm long, denseh pub< - mil with en-el hairs: corolla 5-lobed, 2.0-3.0 mm long, densely pubescent
with erect hairs; stamen filaments 6-8 mm long;
nous, on a stipe to 0.3 mm long. Legumes
light \ ill.nv ish brown, srtaighl. Ilall.'iicd. oblong.

90-170 X 15-24 mm, cartilaginous, transversely
striate, pubescent, eglandular but usually with mii lite |>ui|)l< gland- wlieii voting, ilt'liisft'iit; stipe to
14 mm long; apex acuminate and apiculate to 5
mm long. Seeds uniseriate, no pulp, dark | iplish
brown, nearly circular, strongly flattened, 5.0-8.5
mm across, sn i
tat
shaped, 1.5-2.5
mm across. Flowers: February-June.
Distribution. Rocky desert and dry thorn-scrub
forests from 1100 to 2000 m elevation in Puebla
and Oaxaca, Mexico (Fig. 2).
A small tree, mostly 3 or 4 m tall, Acacia sericea
is known from southeastern Puebla ami adjacent
Oaxaca. Il occurs at higher elevation, usuallv above
1100 m elevation, in desert at
Mosi . nil. ttions are from roadsides, usuallv n th\.
<i
ih i habitats, and many are from the
i
acan valley (Rico Arce & Rodriguez, 1998). Based
Acacia sericea is distinct from most other members nl this group. The dense, erect pubescence on
most pails uf I he plant makes it easv In distu g lish
llus ta\nn. The leaf rachis. the pinna rachis. ami
u.s i ilb 'h.- pt hole an dens, h puheseen| with ef.-< i
hairs that exceed 0.3 mm in length. The leaflets are
mostly pubescent with erect to slightly appressed
pubescence, win a- the maliae liuils are -lim' pu
besceiit. Also, the calyx and corolla are pubescent
with creel hairs, as are iIn- lloral bracts, which are
commonly longer than those found in other members of this group.
Acacia sericea possibly hybridizes with A. acal/cnsis III areas vvheie thev are svmpalrit. Occasional specimens were encountered with reduced
pubescence ami main leaflet pan- per pinna, char..
I< (I mill
,/
>,?!> ;,-,.>
Represenlalire specimens. MKXICO. Oax

ml,-not .le Sal.ime. Di-lneM ,|, Cuicallan. Conzalli 3321
(M *); Cuesta tie rata \ tcja. Smith 130 ((,11*); a H km al
INK de Teotitlan del Camino. earretera a Huautla. Sousa
W>23 (C\S. MIA I, MO. I CM; a 12 km al N tie Touab
tepec. .S,*.v & Mafsal/anes 8017 (ISC*); a B km al M'
tie Teotiilan del Camino. en el camino a Huautla, Sousa,
Martinez, Telle: X Uaâllanrs .,3'tf, (C\S. MK\l i*. IS.
WIS): a <) km al NK de Teolitlan tlel Camino. Sousa. Mar
One:. Telle: X Uaîllanes 3102 (C \S*. I S): a <) km al
\ tie la tlesviaeion a Touallepee. Sousa. Itaim:s A I'eii
0131 ,C\S. MO MC V\ 1^1: .-, .'J km ;il K-\ K tie Teottl l.u,
del Camino. eaiiuno a II,nulla. Sous,,. Telle:. Cn-rmdn &
Rao 3033 (C\s'; Canada de Car. i/alillo. Cent. Verde.
Tenorio, Romero, Martinez & Tenorio 6983 (K MIA I *):
7.0 km al K tie leolitlan. earrelem a I luautla de Jimenez.
I3nes X MarOnr. t,l<> ARM . \l(l,. IN.. Ma: Cerm-
F-2024 (MO, NY*); Tehuacan, Conzatt, 2I7<> (I*. IS); .'

mi. N of the cilv Imuls cl Telinaean. Hansen. Hansen A
W 1728 | lb. MICH. IS*. WIS): about 10 mi. \ of Te
Imaeaii on in mi n id lo.v.ne Oi i,"il :,i
Contreras 1320 (MK\l . \\*y. Cerm de Solumta, I'urpu.
3863 (MO*): Tehuacan. Purpus 3843 (V. MO, M *. I C
I S): Tehua.-a... I'tupus I0o!i2 (N \. I S*|: Acalepee. SW
Zapotitlan. Sousa 2668 (CAS*. IS): ba.lera W tie Cerrt
(.ramie Mpio. Caltepec. Tenorio Romero 3121 ((. W;l
chtendal) Britton & Rose, N. Amer. Fl. 23:

112. 1928. TYPE: Mexico. Hidalgo: Barranca
de Acholoya, C. Ehrenberg s.n. (holotype,
HAL!; isotype, UC!).
i rnv. -ha low b iis-urei!. I w ig- hghl brown to purplish browi , uol fle\iiou>. usn ilb jaili.ii.l uf aid.
short shoots absent. Leaves alternate, 30-130 mm
long: -.':] il.-> herha. eons, light bmvvn. tiarrowb Iriangular, 2.5 X 0.6 mm near the base, glabrous to
puberulent, persistent, peli.
8-50(70) mm lot
i-hlb puberulent and
(oininonb with minute purple glands, petiolar
gl: ml s..l lafv. In. ah-,! I. 'u.vii :l . lovvei pinna pallor rarely along the upper half of the petiole.
stalked, circular, 0.4-0.8 mm across, apex globose,
glabrous (Fig. 4D); rachis adaxially grooved, 10-70
mm mm:,, puberal.-nl and < ommonlv with iiuimle
I i"
a
i I
I- 1 J ii d with a globose
apex, 0.4-0.6 mm across, between most pinna
puis: pinnae 1 to 6(9) pairs per leaf, 30-85 mm
long, 6-15(25) n m '
mi - pairs; petiolules
2.0-2.8(4.5) mm long; leaflets 10 to 26(33) pairs
pei pinna, opposite. I ,"> mm between leaflets, oblong, 4-12 X 1.5-3.5(4.5) mm, loosely pubescent
on both surfaces with appressed hair-. . oninionb
purplish above, light green to purplish green beneath, lateral veins obvious wilh a midvein and 1
to :> smaller veins bom the base, base oblique, margins ciliate, apex obtuse to broadly acute. Inflorescence a loosely flowered cylindrical spike 30-90
mm long, solitary (rarely 2) from the leaf axil: peduncle 6-15 X 0.7-1.1 mm, puberulent and with
minute purple glands; involucre absent; floral
bracts linear, to 1.4 mm long, pubescent, earlv deciduous, blowers sessile, creamy-white; calyx 5lobed, 1.3-2.0 mm long, lightly appressed pub.scenl: corolla 5-lobed, 2.2-3.5 mm long. lighllv
appressed pubescent; stamen filaments 6.5-8.5 mm
Legumes light yellowish brown to dark ineeuish
Volume 87, Number 4

oblong, 80-240 X 18ely striate, glabrous,

eglandular, dehiscent; stipe; to 12 mm l>tl
j.<
acuminate iinl isiialh Leaked Seeds UIUM-I ml' . im
pulp, dark brown, nearly circular, strongl) Battened, 8.0-10..") ii
L: pleurogram Ushaped, 3-4 mm across. Flowers: April-June.
Distribution. Thorn-scrub forests and from the
j
kels, and rocky
slopes from 1300 to 2700 m elevation in eastern
\l> i< i li.n Ii. -in.- el I m ndipas and Nuevo
Leon south to Oaxaca (Fig. 3).
Acacia mammi
i
lislribul. <l ih
out the central part of Mexico from the state of
U
.
! Nuevo Leon. It
does not appear I" be a common species, however,
many of the collections being from near the same
localities in the various states. All colleelions examined are from above 1300 m, many from near
tlie piiuori-jiaupei /.oin . m (torn :nek\ slopes anil
(lr\ lln. k. !-. in..-IK as-i.ci.iied with I In >i ri -i rub
Segetalini;. Tlie jew pinna pails, ill. Ialr'< e :lli I
i;h ap|
I1 i lli sii.-liK es, the dull purple color on the upper surface of the leaflets, the
naimwb inangidai stipules, am! the si Ik. : pi 11
lil
in I
I
i- lie \cacia mamThis wide-ranging species is not extremely varlabh nun |)liolo-M alb. b;il oi:< iiiusual specimen
from Puebla, Mexico, was encountered \E. M. Mm
tinez S. 21665 (MEXU)]. This was a small, compact
plant with the small leaves and leaflets of A. compacta, but was similar to A. mammifera in lacking
short s|](.(,K. ha\ II,g narrow I\ tiiaiiguhu stipules, a
s!alk (I p< iiolai gland uilh : bulbous ape\. ,n. i
i
* nt on both surfaces. Occurring at an elevation of 2300 m, this
specimen was probably outside the natural range of
A. compacta. The status of this possible hvbml iiiusl
await additional field studies.
ReprcsenLttue specimens. MKXICO. Guanajuato:
Rancho Beltran. 10 km al S de Xichii. Ventura & Lopez
(,77r, |C.\>. Ml At *i. Hidalgo: Barranca de Tuzanapa.
, , i, HI
i Ml ' I ' I in nn-asjr lolantongo. Cardonal. Hernandez .3775 (MO*); 6 km al N de
Zoquital, Hernandez, Cortes & Hernandez 6036 (CAS,
U
'..,.Ml \l
M(. - ,
la Mesa. Rose. Pointer & Hose <HJ(, ((,11. W I S* |. Nuevo L.-011: a 2 1 km al S lie ( .1 I IM.IM -. < - .. './'.
|M<). \V,:): i'ai
la Boca, .amino a Cola d. Cahall..
I! I , I M I I I '
.
\ \l
i 930 (CAS, MO, MU*. WIS); a 4 km al
e la earretera Tama/ulapan-Clii
Diaz, Rico, Torres & Cedillo 333 (CAS*, MO).
i: Manama Honda al NW de Caltepee. Tenorio &
Romero 5777 (ARIZ*. CAS. CM. II V \\ ISi: ( ,. T,

pear. 0. al K de el ilaneho de Tlacuiloltepec. Tenono .\
.;'./ lM<> . KM II \l On.Teh,.-..: IIM.II! .'Ml
I
1 1 1
.
1
.1
1
\moles. MeVaugh
10364 (GH, LI . MICH*. MO. TEX. I Si: .V I km al I'.-n
ienle de La I'arada. Serrm 117 (CAS*. Ml XI ): C.esla
,
- l I
KM San I ,..s |M.,
km \\ of jet. of hwy. 86 with roads to Rayon ami I ianlemis.
82 kin \\ f V lies, Roe & Roe 2220 (N\ *. \\ IS:. |aiH.inlii.a-: <(,. .") km N of I.a Jova de Salas. trail to Caral.aneliel. Martin /2V (MICH*): 8 mi. K of Dulees Nomhres. Merer < Ropers 2641) (GH. MO*): 15 km al N de
Tula. Puig 4741 (MEXU*).
8. Acacia durangensis (Britton & Rose) Jawad,
Seigler & Ebinger, comb. nov. Basionym: Senegalia durangensis Britton & Rose, N. Amer.
Fl. 23: 112. 1928. TYPE: Mexico. Durango:
San Ramon, 21 Apr.-18 May 1906, E. Palmer
107 (holotype, NY*!, MEXU photo!; isotypes,
F!, MO!, UC!, US!).
.:. ... i .11 ,
Shrub (
trunk dark gra\ di Ih .\l\ I u .-.I. tw - Indil
brown, not flexuous, puberulent; short shoots absent. Leaves alternate, 65-160 mm long; stipules
herbaceous, light brown, narrowly triangular, to 2.5
X 0.7 mm near the base, puberulent, persistent;
petiole adaxially grooved, 30-50 mm long, pubergland solitary, located near the middle of the petiole, sessile, elliptical, 1.1-2.2 mm across, apex irregularly raised, glabrous (Fig. 4A); rack adav
ally grooved, 50-130 mm long, puberulent and
usually with minute purple glands, a sessile, flattened gland. 0.4-0.8 mm across, between the pinna.- of the upper I to 2 pinna pairs; pinnae 6 to 13
pans per leaf, 60-85 mm long, 8-14 mm between
pinna pairs; petiolules 2.5-4.0 mm long; leaflets 28
to 36 pairs per pinna, opposite, 1.3-2.1 mm between leaflets, linear, 5.0-7.5 X 1.3-2.1 mm,
-' I- pi I" -< I i HI both surlac.-s Willi appressed
hairs, commonly purplish above, light green to purplish green beneath, lateral veins obvious with a
midvein and 1 to 2 smaller veins from the base,
base oblique, margins ciliate, apex obtuse to acute.
Inflorescence a loosely flowered cylindn I pik<
60-120 mm long, solitary (rarely 2) from the leaf
axil, or rarely in short racemose clusters; peduncle
5-15 X 1.0-1.8 mm, puberulent; involucre absent;
floral bracts linear, to 1 mm Ion:, [ml i - ut. nl
-silo, creamy-white; calyx 5lobed, 1.0-1.4 mm long, dens.lv appressed pubescent; corolla 5-lobed, 2.0-2.5 mm long, densely apn lilat nts 5.5-7.5 mm
Legumes dark reddish brown, straight, flattened,
oblong, 80-120 X 16-22 mm, cartilaginous, transversely slriat.

lab
i i . I'_ ii
HI, , nl n
.glandular, dehiscent; stipe to 10 mm long; apex
aciiiiuii.ile ami usn.ilK beaked. Seeds not seen.
Flowers: April-June.
Thorn-scrub forests and dry thickets, 1600 to 2200 r
rango and Chihuah
(Fig- 3).
durangensis are avail; l.lr li,| -lll.h : we s;,\\ llie l\ I an ! Iwo others This
is the only species ol' this group known from Durango, ami il or,airs in a region that has been poorly
collected. Superlicially. 1. durangensis is similar to
A. mammifera, the leaflets being purpli-h >
light gn .II beneath, with obvious veins am: I >- I
pubescent on both surfaces with appressed hairs.
Leaves with 6 to 13 pinna pairs, pinnae with 28 to
36 leaflets, and the sessile petiolar gland that is
elliptical in outline and with a raised ape\ separate
this laxon from l'he pefiolai
n
is the most distinctive feature of .1. .//.
i tlh i -1 e
i, - nl lln- . tniip ha\ r j Hal ot do i<_-Inn,I
shaped gland, oi tin gland is stalked. In A. durangensis, in conlra-l ilie -e--ile gl.md appears as
an elliptical mound, with a few indentations. On
herbarium specimens, this gland has a puqile color,
and rarely a few long hairs on its surface.
Though none were observed on the few specimens available, it is possible that plants ol \eacia
durangensis occasionally may have prickles. If present, this would suggest that A. durangensis is more
elos.lv related to 1 mat ilei
I i I i i m i
ol the [niria series Vulgares that comim i !
av.
prickles. Ms... the pel iolar gland of A durangensis
is similar to those found in many memberof \ca
cia series Vulgares.
Representative s/>ecime,
& Gerson 12774 (MEXU
MEXICO.
urango: Kl Pino 20 km de
lei de Cn.ces. Mp, I.,sell,la. 2 I UN. I()549'W, Ten, , II \

. Romero & Haimi
9. Acacia willardiana Rose, in Vasey & Rose,
Contr. U.S. Natl. Herb. 1: 88. 1890. TYPE:
Mexico. Sonora: rocky islands and ledges on
the coast of Guaymas, 1-2 Apr. 1890, E.
Palmer 164 (holotype, US!).
I'ro.so/us hcterophvlla Ueiilham. London J. Hot. 5: 82.
1846. Senegalia heteroplnlla (Bentiiam) nrilton X
Rose. N. Amer. Kl. 23: 1 14. 1928. TYPE: Mexico.
Sonora: Aha. 1830. T. Coulter s.n. (holotype, TCD)
|not Acacia hetero,,l,ylla Willdenow, 1806].
Tree to 10 m tall with
dish v. liow. xlolialh g 'ii.l papei ; \\\ tt - light gia\.

becoming dark reddish purple, not flexuous, glabrous; short shoots absent. leaves allcrnale. 30
400 mm long: stipules herbaceous, light brown,
narrowly linear. 1.1 X 0.2 mm near the ha-e. glabrous, tardily deciduous; petiole flattened, not
grooved. 20 100 mm long, usually glabrous; petiolar gland solitaiv. located between to jnsl below
the lower pinna pair, sessile, circular, 0.3-0.7 mm
a- i os-,. doi.j In us' sli .)., d. glal
i- 4'ig. K <): raehis
llallened. not grooved, 0-100 mm long, glabrous,
glands absent; pinnae 1 (rarely 3) pair per leaf, 1680 mm long; petiolules 2.5-8 mm long; leaflets 4
to 20 pairs per pinna, opposite. I 5 mm distance
between leaflets, oblong to elliptic, 3.0-7.f>( 12.0) X
1.0-2.3 mm, glabrous to rarely lightly pubescent
> ilh app:, -s< d I aiion !i >ih -uda. . -. lateral \ems
not obvious with only one vein from the base, base
oblique, margins lightly filiate. apex narrow I \ acute
to acuminate. Inllorescenee a looseK II.,wend , vIII.ii
I -pike .30-90 mm long, solitaiv It
tinleaf axil, or in short racemose clusters. Peduncle
5-25 X 0.4-0.8 mm, glabrous or nearly so; involucre absent: floral brads linear, to 1 mm long, glabnne ': livl tlv ; ul i -cent, earlv deciduous. Flowers sessile, creamy-white; calyx 5-lobed, 1.3-2.2
mm long, glabrous; corolla Vloh.d. 2.1 3.0 nun
ious; stamen filaments 6-8 mm long; ovary glabrous, on a stipe to 1 mm long. Legumes light
yellowish brown, straight, llallened. oblong, 70-180
x 8 22 mm. ehartaceous, irregularly striate, glabrous, eglandular. dehiscent; stipe |<> I I mm long:
apex obtuse. Seeds imiseriate. no pulp., dark blown,
nearlv circular, si rough llalten.d. 6 II mm a. toss.
smooth; pleurogram usually absent, when present.
1 -shaped, about 2 mm across, blowers: lehruarv
ite to red-
Distribution. Arid hills, rocky slopes and washes in desert scrub vegetation between sea level and
500 m elevation in Sonora, Mexico (Fig. 3).
A common species at lower elevations in the
stale of Sonora. \caci<t icillardiana is a very obvibeeaiise of it nearlv whit
n <l
I papery, exfoliatir
this species ii
miens are from the vicuntv of (.mmnas. The niali.iih ol d., -p.. i lint lis la. k puma. . winch ate earlv
deciduous; only the elongated, flattened petioles
persist. Although flowering is common I mm f< h-
member*
reach 400 mm in length, and the leaves with usually only one pair of pinnae, though rarely two or
three m,i\ In' : tvseiil. [In- speeds da- \er\ small.
i rilib '
!ii" i- -li| i.l' -. | 1.1 mm long or lessi.
and itir ii ni valves air pap-ax wild moie iiu gidai
-"i i a IK -ti- I han those found in other members of this
gi<> ip, '[ IK diara- tei I-IK paper>. >-\\'n\ lal mg hark ishared only wild
, n-s oi this group
restricted to central Mexico.
Bentham (1846) tentatively assigned this taxon
to Prosopis heterophylla based on a sing!, i i in
specimen. He suggested that the general habit of
the plant was more like thai
other gen is. mil rri.-ni ioned (lie ahno-l ph\ Modi
nous \erlii al expansion of the petiole. Based on
downing malm: I. \a-<-\ :,nd Rose i i ",' HI i iv: h,-, :;
that this taxon was an Acacia and used the name
i
- I-nlh.im's name was preoccuVassal (1972) noted that A. willardiana is a spe. ies widi
he
had
nidi.-utii
seen
ph\ dock- and suggested that.
How
mi
ii
\\
i n
>n
!ia\e plai ed this speed - in the- "J iliflorae." Vassal

d this species to be a member of his section
Hi '. "./" ."'"//,
hav<
it'ii
.-
to
-id -ii in n
iiu-
S;i
,/.'.,,
predominantly
group. In oin \ lew. Iiomologx h.-rv.cci
-i,'
|.i
itwiiiuut sin idd he i \amined nice td< i...|gld\. I'm
ther. in most ,.td. i daraeteristics, this species differs little from other members of the A. coulteri
group discns-ed in llir presci:! si ni\
Representative
speeimens.
MEXICO.
Sonora:
rocky
lull \ of C,nomas. Iilakh>\ H82t){\*\ *>: C> mi. from tup

l.l.nirnm,ur
lovua lull at Cuaunas. Ihnnnn r>7 \ WW/* V.
Pallia .1.- Sat, Carlos. , a. 2 1 km \\\
ol (aromas. t.arir,
ol
Hotel I'Lc, ,!,
Cortes. Miramar. Felger 551.1 (ARIZ*): Isla Tihnron. / - /

ger9151B (ARIZ*. SI)): Sierra Seri. Has, K.-mla. Feign.
Drees & Moser 74-8 (ARIZ*): Balua Colorado, anoso al K
hase
of
Mom.
Colorado.
il.'S \ ' i. 1 II-. n,i,
i i
Felger
- i
&
In
Hamilton
15638
Cd. Obregon. Gentry 14483 (ARIZ*. IS): If) mi. S of II, r-
mas near dvvv.
15. Hennekson
!: 5 mi. \ ol Cua\
1565 (RSA ' ):
i: imrnmave tower. o<) mi. \ of Navi-
|,..i. Joseph s.n. I \RIZM: hillside \ of (aiaymas, Knobloch

2325 (SI)' I: Cawnas. San Carlos \hn. road In Catch 22
hoard,
hm.lrum
limestone .|iiarrx
Ian,hum
6315 I \SI *.
\1().
RS\l:
SK of I lormosillo. Martin s.n. I \RIZ*):
\i.lilla Maud, laiasmas llarhor. Moran
strongly flattened, 6.2-9.5 mm across, smooth:

pleurogram U-shaped, 2-3 mm across, flowers:
Jun. \i,gusl,
Palna Sin
Carlos. Howard & Sphon s.n. (RSVS: H.-rinnsillo. ./,*

22l5 (MO. PCM
looseK How. red cylindrical spike 30-75 mm long,

solitary (rarely 2 to 3), from the leaf axil; peduncle
5-15 X 0.3-0.8 mm, glabrous to lightly puberulent: involucre absent; floral bracts linear, to 1.3
mm long, glabrous to lightly pubescent, early deciduous. Flowers sessile, creams-white: calyx 5lobed, 1.1-1.6 mm long, glabrous; corolla 5-lobed,
2.0-2.7 mm long, glabrous; stamen filaments 4.56.5 mm long; ovary glabrous, on a stipe to 0.4 mm
long. Legumes light yellowish brown, straight, flattened, oblong, 70-170 X 12-21 mm, chartaceous,
irregularly striate, glabrous, eglandular, dehiscent;
stipe to 12 mm, apex acute to obtuse. Seeds un-
P o. / elger. liiissrtl
& Kleine 11588 (ARIZ. SI)*): Sierra Bojidua.ame SK l
mosillo. Centra X Kngnul 551 I ( \Sl
Shrub or small tree to 3 m tall with bark gray,

smooth when young, becoming fissured into square
plates I 2 cm across: twigs light brown to greenish
brown, not flexu i
i i I
II
i I
id ii
short shoots absent. Leaves alternate, 60-230 mm
L
-Iipules herbaceous, light brown, narrowly
linear, 6.5 X 0.5 mm near the base, usually glabrous, persistent; petiole adaxiallv grooved, 30-75
mm long, usu II
hroi
I
-land
i
rachis adaxially grooved, 50-190 mm long, glabrous to lightfv pubescent; a stalked gland with a
globose a pi \. ().'.'> 'I " mm . ross. between tin- pinnae of the upper 1 to 2 pinna pairs; pinnae (2)6 to
14 pairs per leaf, 30-55 mm long, 10-28 mm between puma pairs: peliolules 2.0-4.0 mm long; leaflets 20 to 35(37) pairs per pinna, opposite, 0.8-1.6
mm between leaflets, oblong, 2.0-6.5 X 0.7-1.4
mm, glabrous above, lightly pubescent beneath
with apprcssed hairs, lateral veins not obvious with
only one vein from the base, base oblique, margins
Australian
l(n- ph\ lloile-
of that group and the apparent petioles of A. wil-
& Kellogg 3246 (SI)*): .a. >/. mi. S\\
Acad. Arts 21: 427. 1886. Scncgalia millr/olia

(S. Watson) Britton & Rose, N. Amer. Fl. 23:
111. 1928. TYPE: Mexico. Chihuahua: Hacienda San Jose, near Batopilas, Aug. 1885, E.
Palmer 45 (lectotype, designated by Isely
(1969), GH!; isolectotypes, MEXU!, NY!).
11)17 (SI)*. I S.
WIS);rte. 15, <

( Mil/.. \SI '):
\I2.><> < \I:I/!I
S. Watson, Proc. An
Distribution. Desert grasslands, rocky slopes,

is i i> I scrub, and open oak woodlands from
700 to 1700 m elevation in southern Arizona, south
through Sonora to western Chihuahua, Mexico (Fig.
3).
sm M
less than 3 m tall,
Ih'jolia is relatively common in desert
io I ml
I d. .
-M ib .. . lation in extreme
southern Arizona and adjacent Sonora, Mexico.
Commonly colled, d along lln strep sides and
Hoots oi canyons, t. millcfolia i

. nidi, aling scattered indiv nkalthough numerous specimens are available from
throughout most of the geographic range of this taxon. no specimens, other than the type collection,
an- known from < Inlm ill i: fli - laxon may be extremely rare in southwestern Chihuahua, or it is
ible ll
i on lli< Ivpt -|M i
Ibis . oil. <-li<
10.1
cast ol ;|||\ -| , 11111 II- (>| 1 '
by the present authors.
Acacia millcfolia is distinct from other members
al tin- group, as '1 la. k- a | >. liolai gland n i< I pus
scsses a stalk.-d racliis -land between the upper
pans ..I pinnae, flic only other taxa of this group
within the range ..I 1 tiiilU <<
and A. russelliana. Aetna millcfolia is easily dislii. li has papery,
bark and leaves with only 1 to 3 pinna
pair-. I.edicts vvidi appressed hairs, die stalked racliis -lands, and the persistent stipules of 1. mil
lefolia separate it from 1. russelliana. In addition.
i
i . a
1
i i I lo md above 700
Representative speeimens. VI PA ICO. Sonora: 3 km by

road S of Naro/ari. Feller .*5W> (WW/*. MICH. SI)); 1
mi. \ ot ( olonia Oaxaca, Hastings & Turne, 6.-_'., i MO/.
SD*); 5 mi. K of Mil.a \enle. Slae,e hT.yi if'\ MM:!!.
\l(i: lii.. IS.m-pe. Colon,.. Oaxaca. While ?> ^\\^\/^.
<,ll. MICH): Canon ,1c llavispe. While .W/> I VH I/.. (.11.
MICH*): > mi. W of La Angostura. While lull i Mil/.
(ill. MICH*): Puerto del Molino CH.emado. K of Colonia
M...vl.,s. While /.>// | Mil/*, (ill. MICH): ., mi. S ol Div,-a.l.-,s. Wiîns 71,'u (\. MO/. CH. 1 *. I C. IS).
I .S.A. Arizona: Cochise Co.: lonthills ol Ihe IVIo.Kalio
\lu. I-J2S \i-.Vll- S:\-l. Kim;;; s.n. (Mil/*). Pima Co.:
HON Canvon. Sanla Kila Mis.. Gonddaifi H<> .>
MO/0:
< & Pee6fc5 /0467
.1.1.11. MICH.
'ti/lMO. POM.
Ophii
i. \\ ol Sonoila.
> T-25 (ARIZ*); Sag.
/},, X (,un:el 7!i III (\KIZ':. SD). Santa Cm/ Co.:
/.;"/( Mil/*). Ne* Mexico: Hidalgo Co.: about 0.5 mi.
I
WIC
. Acacia salazari (Britton & Rose) Lundell,

Contr. Univ. Michigan Herb. 4: 8. 1940. Senegalia salazari Britton & Rose, N. Amer. Fl.
23: 113. 1928. TYPE: Mexico. Michoacan:

Xochiapa, 13 Apr. 1912, F. Salazar s.n. (holotype, US!; isotypes, MEXU!, NY!).
Tree to 15 m tall with bark yellow to red or light
gray, exfoliating and papery; twigs greenish brown
lo light reddish brown, not llcxuous. usually glabrous; short shoots absent. Leaves alternate. 50
180 mm long; stipules herbaceous, light brown,
narrowK linear, 4.5 X 0.6 mm near the base, glabrous, persistent; petiole adaxiallv grooved. 20
O.dll. ...in I..ii'. . lin-lb . I. I l .11-. p- i -.1.11 : land
solitary, located between the lower pinna pair, sessile, nearly circular, 0.5-1.3 mm across, globose to
I. . . In in -'. ip. d i . i ' on m.i-t It .iv i -. i.II In-adaxiallv grooved, 35-140 mm long, glabrous to
bglitlv pidx raleiil. .! sessd. . doughnut- to saucer- |
land 0 ">- I 0 mm a< ross. between the pinnae of the upper 1 or 2(3) pinna pairs; pinnae 7 to
18 pairs per leaf, 35-63 mm long, 4-12 mm between pinna pairs: petinlules 2. I 1.0 mm long; leaflei-, 20 lo .').'! pel pinna, .pposttc. 0.0 1.5 mm between leaflets, linear, 2.5-6.4 X 0.9-1.3 mm,
i.-n.i.C lighlb f!i;!i< -cenl .-. ill ,.; pres-ed hails hei.eatl . inn:., ml % I! ghl mr.-n -I: purple and glabrous above, lateral veins usually not obvious with
only 1(2) veui(s) from the base, base oblique, matgins usually ciliate. apex narrowly acute to acuii a
liiilnrcM-eiicc a loosely flowered, cylindrical
spike 45-110 mm long, 1 to 3 from the leaf axil,
or rarely in terminal racemose (lusters: peduncle
5-10X0.5-1.0 in
ighll
I oiul.nl: involucre
absent; floral bracts linear, to 1 mm long, puberiilent, early deciduous. Flowers sessile to rarely short
-' pita!. . . teamv white: rah - . I..bed. 1.5 2..'5 mm
long, lightly appressed pubescent: corolla 5-lobed.
2.5-3.5 mm long, lightly appressed pubescent: -la
i li laments 4.5-7.0 mm long; ovary glabrous, on
a stipe to 0.3 mm long. Legumes yellowish brown,
straight, flattened, oblong, 115-180 X 21-35 mm,
cartilaginous. Itatisvcrs.lv striate, glabrous, .-glandular, dehiscent; stipe to 13 mm long: apex ..bins.-.
Seeds imisenatc. no pulp, dark reddish brown, circular to oblong, strongly flattened, 10.0-14.5 X 72 in
i
i
i I
i p. .) I 2 3.0 mm
across, flowers: \pril June.
Distribution. Thorn-scrub thickets, and disturbed dry forests from near sea level to 1800 m
(but mostly above 1000 m) elevation in the states
of Guererro, M. s
M
VIor. los. < >.i\a< a.
and Puebla, Mexico (Fig. 3).
A small tree, not exceeding 15 m in height, Acacia salazari is restricted to dry habitats, particularly
thorn-scrub forests of southern Mexico. Many collections arc horn abov. 100*) m el. valiou. bul a
li'W iinli\ iilu.ilan n [Killed bom near sea level,

\cacia salazari is similar to 1. acallcn-iis will
range. Both have leaves with many pinna pairs, and
leaflets of similar size that are lightly pubescent
wiU) appii ->ei| hair.- Iiein alii and . ..nitnor.b i ; III
greem-h purple and glabrous above. Acacia am
lht)s<\ however, has minute purple glands don- lh
petiole, rachis, and al llie base ol most leallels; p nnae with more than 36 panit I
that are mostly less than 2.0 mm long; and dark
gray, fissured bark. Acacia salazari, in contrast,
lacks the small purple gland and usually has fewer
than 38 pairs of leaflets per pinna, petiolules that
usually exceed 2.5 mm in length, and yellow to
i Idi
>.uk that is papery and exfoliali
- n
sju-i miens Willi a inixlnn al rhara. lensli. - el the ..
two species suggest that they probably hybridize in
Although A. salazari is similar to other species
ol tin.-. ,-r<nt| from -iiuilierii Me\i. i . par'a-al i , \
centralis mil 1. usuniih '!!!%!%_ (he papers, exlol
;ilin<; bark allows ioi C.IM separation. Also, boll o
these species have pinnae with more than (36)40
leaflet pairs, whereas A. salazari has 38 or fewer
leaflet pairs per pinna. \cm
lame. Ilallem d [>> M'.lai -hind- that are located on
the lower half of the petiole, while Acacia salazari
c-oii:monl\ lacks p. tmlai plaiuls ) a-n i al ;. p. I
iolai 11 a: ids are found on a few leaves of some specimens; these are globose to doughnut-shaped, and
located between the lower pair of pinnae. Thoe
P'1'iolar glands altogether. On the remaining
mens, only <
id.md.-. and l
iy are globose, not doughnut-shaped
most taxa of this group. Acacia sallillefolia are the only taxa in this
lly lack petiolar glands.
Guerrero:
,
banks \ of Chilpancingo, Clark 72.35 (MO*): 21 km al
\E ,le Clnlpancinpi. Del^nlu & Garcia 1085 (C\S*. K
MEXl . MO. W. WIS): a 20 km al \ ,le Chilpanei,,,,,.
rann.m a l-uala. Martinez 557 (V*,: X le Zumpango del
Km. Hi,,, X lutnk 201 |C \S! ). 2 I kin al \ ile Ziinipanj....
.1(1 Win liacia Iguala, Torres, Tenorio & Rom,;,, I'll
(CAS*, MO). Mexico: El Jumale. a 1 km al S despnes
del cru/ern Sin \n II
<M ) Mielioacan: between Rio Tepalcatepec and \rlea-a. Uc\,iunh 22521) |C\S. MICH*. MO. NY); en Us
C.ina-. eerea de la desviacinn al Infiernillo. carrelera Nuew, llalia I'lasa \/.l,l. .W 1081 |C-\S. MO*): carrelera
Nueva Italia-Arleaga. Soto & Aureolea 7715 Ml \l i
\lori .
!
'(> lU *). Oaxaca:
Ranc-ho ElMe/quii
,
- I I olitlan. Soma 6934
(C\S. MO. SI). ICM: Teotillan del l.atnino. en la orilla
del I'ueblo. Sousa. Telle:. German & Km, ,",<)(,<> |C\S.
MO*); a 3 km al E-NE de Teotillan del ( a,nam. rarrelca

a II.. Mill... S,,usa, TdUz, Germdn & Hie,, 8()7<> H \S
II \i. I'ueblu: 2(1 MIL SE ol Irhuacan on road to Teotitlan
del bniiiNu. Uiderson & Anderson 5332 (MICH I: >,5 km
nelo 25 (MO*): Piaxtla. Huerta s.n. <M *): just \ "I C..\.,.''..
II \ I
1 I i .,,
<
lr
N I , J ..>.../
5418 (MICH*. MOl: livsx. IX). 17 mi. bom the Oaxaca
border in I'nebla. Troll, Case, Thurm. Dunn. Hess & Dziekanouski 140 (MO, NY*).
12. Acacia coulteri Bentham, in A. Gray, PL
Wright. 1: 66. 1852. Senegalia coulteri (Bentham) Britton & Rose, N. Amer. Fl. 23: 112.
1928. TYPE: Mexico. Hidalgo: Zimapan, T.
Coulter s.n. (holotype, K!, F photo!, GH photo!,
MEXU photo!, MICH photo!, MO photo!, NY
photo!. 1 S photo and fragment!).
gray, shallowly furrowed; twigs light brown to
greenish brown, not flexuous, glabrous to lightly api
b
bsent. Leaves alternate, 50-150 mm long; stipules herbaceous,
light brown, narrowly linear, 2.1 X 0.4 mm near
the base, glabrous, tardih deciduous; petioles
adaxially shallowly grooved, 25-55 mm long, usually lightly appressed puberulent; petiolar gland
solitary, located on the upper thud ol the petiole
aid oi ma ids in-' below die iiisi pinna pair, sessile, nearly circular, 0.5-1.6 mm across, do vA,w.\shaped. glabrous. rarcK absent |Ki. IK); rachis
shallowly grooved adaxially, 20-100 mm long,
lighth puberulent, a sessile, cup-shaped gland,
nae 5 to 11 pairs per leaf, 40-90 mm long, 6-12
mm di-taiice be|xx..ri puma pan-, p. tr .bib--, .>-..
mm long; leaflets 18 to 35 pairs per pinna, opposite, 1.5-2.3 mm interval between leaflets, oblong,
4.5-7.5 X 1.4-2.1 mm, glabrous above, lightly appressed pubescent beneath, lateral veins obvious
with a midvein and occasionally one other vein
from the base, base oblique, margins ciliatc apex
broadly acute to obtuse. Inflorescence a loosely
flowered cylindrical spike 50-90 mm long, 1 to 4
from the leaf axil, or rarely in terminal racemose
clusters; peduncle 7-13 X 0.5-1.0 mm, usually
puberulent; involucre absent;
luaai
1 mm long, puberulent, early deciduous. Flowers
creamy-white; calyx 5-lobed, 1.2-1.6 mm
long, lightly appn
I pul i s < I it; corolla 5-lobed,
1.9-2.6 mm long, lightly appressed pubescent; stamen filaments 5.0-6.5 mm long; ovary glabrous, on
a stipe to 0.4 mm long. Legumes light yellowish
brown to dark brown, straight, flattened
100-185 X 16-25 mm, cartilaginous, transversely

sli J. . -_;labroi;s. . glandulai. lrlii^( nil; slip.- |o 15
mm long; apex acute to acuminate. Seeds uiiisoriate, no pulp, dark reddish brown, circular to nearly
oblong, strongly flattened, 7.3-10.5 X 5.5-8.5 mm,
smooth: phurogram I -shaped. 2.2-3.5 mm across.
Flowers: April-August.
Distribution. Open dry forest, dense thornscrub thickets, and dry rocky slopes below IJUH) m
elevati >n in the foothills and mountains of northeastern Mexico in the states of Coahuila. (aiaua
juato, Hidalgo, Nuevo Leon, QuereMaro, San Luis
I'olosi. in,I bunaulipas (f ig '>
Abundant in northeastern Mexico, Acacia coulteri is a e moil . < TII| .< -rit-iil .-I 'claim l\ :\\\ forests
and Ihorti-scrub thickets. Many ol th<- collections
are tmm roadsides and rockv pastures. This ta\on
is .111111111.1111 in the states ol bunaulipas and San
Luis I'olosi'. becoming |, common to the south.
Acacia cuilteri is similar morphologically to A. russelliana, which is common in Sotmra and parts <>f
Sinaloa. Acacia i usselliana is usually a small shrub
or imdefslotA Iree lhal rarelv exceeds I in in height.
[caciii nissclliaua has usually been considered as
coiispecilic with 1. iimltcii. brillon and Rose
(1928) being the only authors that recognized the
two as distinct. Both of these taxa have leaves with
lower than 12 puma pair-, pinnae with fewer than
35 leallel pairs, petiolules that exceed 2.1 mm in
length, and idi riti
11< 1
J i 1
I
jji iia
1. coulteri hi. i
bescence on the
lower leaflet surface, peiianth. ami the rachis and
pinna lacluses; .1 russelliana, in contrast, being
glabrous throughout.
The stipules of Acacia coulteri seedlings are decidedly spmeseent, but are only weakly rigid alter
the hist l.al stage, and become progressive!) smaller and less rigid on older plants (Vassal, 1972).
Because this species lack- prickles and because of
correlations of the cotyledonary petiole and shape,
as well as certain other features. Vassal placed 1.
coulteri in his subgenus Acacia, a group roughly
.I % .i "!" to I'M nil, III "- i I.", !_; b,,< to series Cumsig-
Liga. Ventura v' /,../-' >"' tMFAl ''l. Ili.L.L..: M> ki

al N\\ de Zimapan. Conzalez 2.<7>8 (l)S. II \1I< II
INuevo Leon: jungles. \ of Linares. Clark 6819 (MO*
KI Ccca.lo. s.iHli.iiii.. ////,/,. 21102 iM \ TIAl; Sien
,lc la S.lla. fringe 2549 (A*. CM, L (,. (ML MO. M
I
Ou.relaro: I >kmalSI
de \gua /area. Hubin lt>77, iMICIL. MO. TKX. WIS).
San Luis I'olosi: 10 mi. W of Tainuiii on the Tani|iico
\all.-s huv. Civldi/nJd X-Johnston ~>!(>l ! MM .11 '. II A I:
Minas .le San Halael. I'urpus 5181 (L*. O. (ML MO. Ni.
I C. IS): If) km \Y of Ta.m.in. Seigler. Clarke X l>^,rin
Diaz Cedilla X I
< i.nino a la mina
LI Iteniiielie. \ ieloiia. Jimenez 6 7 ( \1 L\ I! ( ); ()() mi. \ of
& Stanford 6867 (CU, DS, F, GH,
. MO.
. IS);
r 4498 (F, MICH, NY. TE
mez Farias. Martin 71C (J
aura, km 658-60 between
Manic. Moore. Ji. A" Wood. Jr. .it
Victoria. Mlson 4421 ((Ml. NY.
'"/
',
Contr. Univ. Michigan Herb. 4: 7. 1940. Sencoalla russclliana button & Rose, N. Amer.
Fl. 23: 112. 1928. TYPE: Mexico. Sinaloa: vicinity of San Bias, 22 Mar. 1910, J. N. Rose,
P. C. Standley & P. G. Russell 13204 (holotype,
US!; isotype, GH!, NY!).
1
'
light brown to
greenish brown, not flexuous. glabrous; short shoots
absent. Leaves a I. :i:a!e. i >0 Nil mm ha . ; -lipiileheibaccMis. ligbl brown, narrowly linear, to 2.5 X
0.4 mm near the base, glabrous, tardily deciduous;
petiole adaxially shallowly grooved, 20-50 mm
long, glabrous; petiolar gland solitary, located near
the middle of the petiole to just below the lowest
puma pair, sessile, usually circular. 0.4-1.5 mm
across, doughnut- to um-shaped. glabrous, sometimes absent; radus shallowK grooved adaxially,
30-90 mm long, glabrous, rarely a sessile, doughnut-shaped gland, 0.4-0.9 mm act
upper pinna pair; pinnae (2)4 to 1 pails pel leaf.
35-70 mm long, 5-12 mm betw
petiolules 2.0-3.5 mm long; leafle
per pinna, opposite, 0.9-1.8 mm <
ablong, 4.0-7.5 X 1.3-1.
Jab,
te, apex obtuse to broadly

acute. Inflorescence a loosely llowered cylindrical
spike 25-60 mm long, solitary (rarely 2 to 3) from
the leaf axil, or rarely in terminal racemose clusters; peduncle 1-10 X 0.4-0.7 mm, glabrous; involucre absent: Moral hi ads linear, to I mm long.
glabrous, earl\ <le 1 !,. - II . .

---.ile. creamywhite; calyx 5-lobed, 1.0-1.4 mm long, glabrous;
corolla 5-lobed, 1.7-2.5 mm long, glabrous; stamen
filaments 5-7 niiii 1 i
i
i
u
2 > tun
!
In
fiiisl
irown to dark
brown, straight, flattened, oblong, 55-170 X 1627 mm, cartilaginous, transversely striate, glabrous,
eglandular, dehiscent; stipe to 15 mm long, apex
acute to obtuse, sometimes beaked. Seeds uniseriate, no pulp, reddish brown, circular to oval,
stronglj flattened, 6.8-9.6 X 5.1-3.0 mm, smooth;
pleurogram U-shaped, 2-3 mm across. Flowers:
March-August.
tively widely spaced. The proposed hybrid is similar to A. ru.s.si '

i i i i-_ stipules to 2.5 mm
long, petioles that are round in cross section and
\A\\\
I.IM.II
<
-iiglmut-shaped petiolar gland, and leaves with 2 to 11 pairs of pinnae,
Few specimens are available for study [Gentry
14337 (MICH, US), Gentry 14420 (LL, MICH, US),
Gibson & Gibson 2101 (ARIZ, ASU), Rose, Standley
& Russell 13317 (US)]; field studies will be necessary to determine the status of these specimens.
QJ
\ JJ
Jj "
'
," j
UC) ên^ db'lSla-
Distribution. Dry, deciduous, tropical forests i<>

thorn-scrub and desert-scrub vegetation, mostly on
rockv slones from near sea level to about 700 m
,
.
.
.
'Q
.
elevation in southwestern Sonora, and extreme
northern Nnal
Ml i. if'iI
A small shrub or understory tree not exceeding
8 m in height, Acacia russelliana is a common species of Sonora and parts of S.naloa. Occurring at
vaehtsle about Bahfa Tnpoloba.npo' Cenln I 13m (1 S*i:

Cerros del Kuril.. 18-24 mi. \ of l.os Mochis. Gentry
17t>35 il.l *): near Yacht Hotel Topolobamp... Hosting A
Turner 64-103 (SI)*); vicinity of Culiaca... Rose. Stadle}
^
Sonora: 34 km K of Hermosillo
on road to Sahuaripa, Felger. Aronson & Shnuda 81 201
(S|>/ri,x*); foothdls at S end of Sierra Libre. 12.3 ,m. S
o{ La ?a\ma on \\*y. \5, Felger & Reiehenhacher 85-1 OH 1
(TEX*); SW of Ures. Felger 3000 (ARIZ, LL*); Rfo Sonora 22 2 mi
- '>> road E of Mex- 15 on road to Ures'
" ' 'lu" ' '"'
elevations below 700 m, it appears to be a common

component of des<
in
1
i1
i HI.
and is also found as an understory tree in tropical
, ,;w, & Mclntosh 4618 (NY*. TKX); summit of

Cerro I'neto. 13 km L of \avajoa. Sanders. Halhnei
Charlton. Clarke S.- Mayor 9286 (SI)*). Rfo Ma\o area. ()
nd Ke.se (1928) were the first to recogmze this taxon, all p

i l,-r>
considering it to be conspecific with Acacia coulteri,
a species of northeastern Mexico. It is easily dis4.
. ,
, ,
. .
0 (SI)*. TKX); ISavajoa. summit of Cerro Malers. Devender. Devender. Meyer & Pitzer 12767
,<;AS*. MO. TKX. \\ IS); Alamos. Cerro La Luna. Sanders.
Friedman. Spenger X Kossaek 13260 (CAS*, MO, TEX);
mossing of Rfo Sonora. 23 mi. NK of Kl Sacaton, V)
Mill
;
I err., Lie In
,-',,
brous; A. coulteri, in contrast, has leaves that are

lightly pubescent beneath with appressed hairs,
and the petiole and rachis are lightly puberulent.
, ., the Muador. Mam.-.

ila 10202 (K. C -\.s. \10. M
Devender & Lindquist 94-828 (NY*); crossing the Rfo So;/' 13 mi.S of Lies. Wiggins 7320 (A, DS, F, MICH,
LC. IS*); 13 mi. S..I La Pahna. between Hermosillo and
Wiggins & Rollins 228 (A, LL. DS*. MICH.
\K>. \>. ICK
many other vegetative parts of the plant.

Also, the perianth
- i
I
iI i .
I i brous in A. russelliana.
The only acacia species of this group found within the range of Acacia russeliia
ana
and A millefolia. Both taxa are easily separated
irorn I ',. .,',',(., \ ' illanlianii b is. Ireinely
Ini;
latt. ned petioles topped with 1 to 3 pairs of
pinnae, and A. millefolia by the stalked gland with
a bulbous apex between the upper pinna pair, the
fl|
,,
.ill
tinguished from this taxon by being essentially gla-
J(
^ ^
j|(.riture (jt(J(|
*^g ^r^1^^^^^^
Vol. 74. Part 1.
Rentharn. C. 1842. Notes on Mimoseae, with a sync
f *pecies. London J. Rot. 1: 318-392, I" I 528.
/JiM(' . '
long, usually persistent stipules, and the missing

pel iolar gland.
It is quite probable that Acacia russelliana or-
^' ir,:^' bVusion'of the order Mimoseae. Tr

Linn. Soe. London 30: 335-664.
Hrilton. X. L. & J. N. Rose. 1928. ""
casionally hybridizes with A. willardiana in thornscrub forests on the arid, rocky slopes at lower el
evation in extrem. i. i . n sn l--i \b i
II
few specimens available suggest that the probable
hybrid is similar to A. willardiana in being a small
tree with exfoliating, papery bark, petioles that
100 mm in length, and pinnae
with fewer than 26 pairs of leaflets that are rela-
^^j0*" A ^
Chappill, J. A. & R. R. Maslin. 1995. A phylogen.
"
7 M. Crisi
. J. Dovle (editors), Advc
7: Phylogeny. Royal Botanic Gardens
Clar k
H D 1995 S
; ;, y
f ^
* Gummiferae (Fabaceae: Mimosoidt
Dissertation. Department of Plant Biology. I
csiana (ral.ate.ie: \1inio-oideacl .

om Mexico, the southwestern L). S
n. Syst. Bot. 14: 549-564.
|VI'S>S-p.-|. \ernon 1.70. \ppli
soideae) species complexes in \

15.
.515.
Conn. F. K.. It. S. N-iglrr. li. |{. MaslinX J. Dunn. 198
Cyanogenesis in Acacia subgenus Aculeiferum. Phyt
<l.rmi>ln 2,".: 817-820.
Fcigl. K & V. A. Auger. I9<>(,. Replacement ..I h.-u/idii
by copper cthylacctoacetate and tetra base as spot-te
r hydrogen cyanide and cyanogen. Analyst9
282-284.
United States: I. Nativ*
Isely. D. 1969. Legui
Acacia. SI DA 3: 365-386.
Maslin. B. K. & ('.. H. Slirlon. 1997. Generic and infrageneric classification in Acacia (Leguminosae: Miniosoideae): A list of critical species on which to build a
comparative data set. Bull. Groupe Int. Etude Mirnosouleae. 20: 22-44.
I'cdlev. I.. 1078. A revision of \cacia Mill in Queensland.
Auslrobaileva I: 75-234.
. 1986. Derivation and dispersal of Acacia (Fegui V;, .../
Tehuacan-Cuieatlan.
acacias (Fabaceae, Mimosoideae. Acacia, series Gummiferae) of the New World. Ann. Missouri Bot. Card.
82: 117-138.
. J. K. Dunn. K. F. Conn & C. I.. Ilolslein. 1978.
Texas. Phvtochemistrv 17: 445-140.
Sokal. li. K. \ I. J. liohll. I".,'). B,melrv. W. H. Freeman. San Francisco. California.
Standlev. I. C. 1920. Trees a
-1721.
. H.. II.
. Buijgrok & R. Hegnauer.
ingen weileren Sippen.
I .>. Nail. Herb. 1: 63-90.

seminologiques a Fetude
et phylogenique du genr. Acacia. Bull. Sue.
Toulouse 108: 105-247.
iVilldenow, C. L. 1806. Sp<
cia) 4 (2): 1049-1093.
MM.
Y.l.
A REVIEW OF GAMOSEPALY
IN THE BRASSICACEAE AND
A REVISION OF DESIDERIA,
WITH A CRITICAL
EVALUATION OF RELATED
GENERA1
ABSTRACT
Gamo>e|>al\ I
eported in 12 genera of the Brassieac
" Desideria and

presenled. A new IKIIIU- ill. I
During work on the Brassicaceae (Cruciferae) for

id*' /'/(),'(/ >; ( hi'i'i //.',-./ > \< :><ti. HI i A'."., <' ka
.-//v'.."/. li !!-..ni'i- .-\i<l.'nl #IMI llie limils ol M\CI;II
I 1.(!'. II': -.,. i is :i and ( ; i;lral \-aan gt nei ue.-d. :: , il.< il
evaluation, and lli<
i
many species and
lllliaspc. ihc laxa llord.i! ad; istiiii ill-.. Tlir g< laaa id
dressed HI llie present pa pet are Chn^lnini ( iai il
Desideria Pamp., Ermania Cham, ex Botseh /.
iopsis II Mara. KiUMmntLs Hots,*!,.. /<;.;-.' . |<
\
\le\.) Ihof.lk. \h!<i:i"l.',>" (eiene. >>',> <,-.
^ i|n\a. ana S<ii'm.sluiiini,!>i Mnselil flie\ exhibit overlapping -itntlaritio in <e\eial characters, and iheii
lead- ha\e often !> en onl i.s.-d.
Because Desideria was based on a species with
a gamosi palous calyx, a review of game pal) it
- pre-ent. d to del. nn n< uli. if. i
genera. The study led to the revision ,| \>, .;.
and also critically evaluated the limi ts of several
presumably related genera.
GAMOSEPALY IN TH K BRASSICACEAE
Gamosepaly has been reported in at least 12

genera of the Brassicaceae from Asiia and South
America. It was first reported by Oliver (1893) in

Braya uniflora Hook. f. & Thomson. Hooker and
Tiiom>on (1861) and Hooker and Anderson (1872)
did not report gamosepaly in the species even
though the type collection has all flowers and fruits
with persistent, united sepals. Schulz (1924) transferred llie specie.- to llie moliolypic l'\ fnnjtlililiilis
0. E. Schulz, a genus restricted to China and Kashmir (Jafri, 1973; Kuan, 1987; Hajra et al., 1993).
Desideria inirnliilis Pamp. (China, Kashmir, Tajikistan) is the second species reported to have a
gamosepalous calyx, and it too was placed in a
monotypie genus (Pampanini, 1926, 1930). Hedge
(1968b) described Sisymbrium gamosepalum
I1 :.. .i
:
,"/,-M />,// / 11. d'_< lilh ol
species was transferred by Al-Shehbaz and O'Kane
(1997) to \eoiondariu Hedge & J. Leonard. Sisymbrium L. (ca. i ><> species; Al-Shehbaz, unpublished) is represt n|cd |.\ indigenous species on all
Australia and Antarctica (AlShehbaz, !'){{). whereas Neotorularia includes
about 15 species di-lnliiil.'d primarily in Central
Asia and1 the Mi ddle East (Al-Shehbaz, unpub-
' I am most gratefulItoZhuGuanghuaan (1 Song Hong for their help in the tram dalion of Chinese te\l ami herbarium
Henk van der Werff. Gerrit Davidse. Nicholas
ilkina for help with tl le Russian liter;
problems
fa-land, and Michael Gilbert for their ad>
Warwick. I
uscript. I also thank the cui ators and
paper. I am grateful t<o Oliver Appel and Ji an '\ 1;:.' 11IMI . I al, r \> for :> inging to my attention gamose|ial\ in Cihuhsm
i Botanical Garden, P.O. Box 299, St. Louis. Missouri 63166-0299, U.S.A.
87: 549-563.
lished: S-> \m!>;f.im and \< >>!,>tn!>in.-i . aeli nicliid. nnh ;l - llgle -pe. it-.- <\ llll ;i - ill li -. | i;l lolis ;il\ \
Two additional species of Desideria, D. pamirica
I..mi T.mk.slan (Suslova, 1973) and D. nepalensis
from Nepal (Hara, 1975), were described with a
gamosepalous calyx. The reports of gamosepalv in
l 'hii\l,>!r,i .. upo.sn \>\ Jain ! 1",.'}. i ' k<//.;<'.-'.'/a>ri.
sis by Wu and An (1994), and D. pamirica are
un plants til' I), mirabilis.
Gamosepalv was first reported from South America by Al-Shehbaz (1990b) in Brayopsis Gilg &
MuscliL ;i genus of six species of which only B.
:;.-;;,,< hn'hi \\ MM i ' i (Helix ' has i;n I. <l ~i p,ilAn examination of olh.t South American species
revealed gamosepaly in ( <//.
I
Sclml/ I A[)]cl, pers. coiiiin.) and Eudema Jriesii 0.
I' Sel ill/ ; Mailmiv I al ude, p. -, : mini ' hmlf
in,: I Intnl.. A Himpl. n dial, s six speei. s dislril
iilcd from Kcuador into Argentina and Chile (AlShehbaz, 1990a), of which only E. fnesii has a
in i
ill
1 i
i iitudysia 0. E.
( IK in
Schulz is a monotypic genus endemic to Peru
(Schulz, 1929, 1936).
Gamosepaly has rceenlK been discovered in one
of six species ol Ml. HUM,,lax n / < i_>,:< ,.' ,i "> Hax
ek & Hand.-Mazz., P. watsonii Al-Shehbaz of Sikkiin \l -Shehl
_
and In one ol six spe< i. s
ol Mi. I lim.dax 'in : nil < '.. tilral \- ; n / 7,<)..'.< i.'/</,/>."
0. E. Schulz, P. jafrii Al-Shehbaz (Al-Shehbaz,
_'
Ithoiigh lh. ivpe collection of the latter
has plants with free and united sepals. Soimslan
bachia xerophyta (W W. Sm.) Comber (China) also
has calyces with either free oi completely united
sepals, wliei.-as S. <mn>sci>a!a A l-Shdil >a> Ix (i
Yang (China), which is known only from the type
collection, has united sepals
2000b).
At least one of the approximatcK 150 species of
Erysimum L., E. siliculnsum (M. Bieb.) DC, has a
I Ion? . al\ x l'li<- s| . i, - was pie\ iousb
recognized in Syrenia Andrz., a genus thai I place
in the svnom in\ ot /*.; >
> >. Il i ik. I\ thai -em.
ol (he spe. ics related to E. sdtcttlosum also have
g in - -. |i l< II- . alvces. but 1 have not exainined adequate material of those.
In all four species of Pugionium Gaertn. (northii n ( h na. Mongolia, md ad a< < I i Sib< rial \\ issi i)
the sepals are connate. \s |h, fruit develops, the
caKx ruptures basalh along the lines of sepal conFinally, the genus Gamosepalum Hausskn. was
imlialb Mi.-a-li! us ha\e a gamosepalous caKx
(Schulz, 1927b, 1936). However, careful examination of its component species revealed that the se-
pals are free, but thex appear connate because of

interlocking stellate trichomes (Dudley, 1964).
In conclusion, two generalizations can be made
_ imosepaly. F irst. the union .1 -. pals
evolved independently several times in the Hrassieaeeae. It is not known whether it evolved one or
more times within Desideria, but a ph\ I. .<-in li<
study based on molecular data should reveal that.
With the critical examination of more genera of
Brassicaceae, it is likely that more spe. i.s with
I S. cm.I. gamosepalv alone cannot be used to define the boundaries of genera because it ... curs m seveial genera
in which the majority of species have free sepals.
Therefore, in the present delimitation oi Desideria
gamosepalv is ignored as a generic character, and
Mic i v .'( II - i i ties ll .1 l. Ii:ii:-h p- el spe, i, Nothing is known about the inheritance of
mosepaly in the family, but the occurrence of plar
with free and united sepals in the same populati
of Phaeonychium jafrii is a good lead for condui
character.
I'ampanini (1026) established the monotypic Desideria solely on the basis of having a gamosepalous
calyx. Although he indicated that I), miiahilis resembles what was then known as Cheiraun-us him
alavensis Cambess., Schulz (1927a, 1936), Botschantsev (1955, 1956), and Jafri (1955) regarded
gamosepaly as an anomaly and reduced D. mirabilis to synonymy of C. himala\cn\is. a species that
Schulz and Botschantsev assigned to Ermania and
Jafri to Christolea. However, these authors overlooked the significant features (-re below I that distil r i ! these two species. With the description of
i
ill mi 1
i, 11
i (Suslova, 1973;
Hara. I'>75). the genus was recognized as distinct
in subsequent floristic works (e.g., Czerepanov,
1995; Hara, 1979; Pachomova, 1974; Yunussov,
1978). and it remained to be delimited primarily
on the basis of having a gamosepalous calyx.
A critical evaluation of all genera related to Dellns- paper leads to the conclusion that
the genus should include 6 of the 10 spe. i.-s treated in Ermania In Schulz ( |93t). of the 10 species recognized in Ermania bv Hot
<n,s <
(1955), and 5 of the 13 species assignee! to ChrisItilrn h\ Jain (l')55). The species recognized by
those a ilhois in ('hns.'oh u oi Eimniiia and excludI
''
ii the present account are: Par-
rya
o
M u
nd Ci
'/n/s albiflorus T.
Anderson, which now belong to Phaeonychium (AlShehbaz, 2000b); Z>ra/>a parryoides Cham, and Melamdion boreale K. i.. Greene, which an- assigned
to Melanidion (see below): I
Cambess., which is retained in Christolea; and Parginosa Hook. f. & Thomson, which is
placed in Eurycarpus Botsch. (Al-Shehbaz & Yang,
2000a).
As herein delimited, Desideria consists of 11 Himalayan, Chinese, and Central Asian species cliaracterized by having well-defined basal rosettes,
slender and rhizo in -lil
i
orbicular or flabellate to broadly ovate or obovate, often dentate
and palmately veined basal leaves, simple and/or
;ar-lanceolate lati>ss section, nonto
rulose and strongb veined valves with disiinel marginal veins, valve apices united with the replum,
often obsolete styles. 2 lobed stigmas, and aeeinii
henl cotyledons. A combination tl I'm its reetanga
lar in cross section . Ives will prominent marginal
1
I
in
entate leaves often palmately
veined rcadih distinguish Desideria from the olhei
genera discussed in this paper.
In his description of Draba parryoides, Chamisso

(1831: 533) stated, "DRABA? parryoides n. sp. vel
potius novum genus e solo fructu, deficiente flore,
haud rite definiendum. Drabis dolichocarpis subjungimus pro tempore plantam aliquando fors jure
meritoque nomine inventoris ERMANIAM parryoidem slutandam." Several workers (e.g. S< I ulz,
1936; Botschantsev, 1955; Hedge, 1968a; Suslova,
1972; Ovczinnikov & Yunussov, 1978; Greuter et
al., 1993) considered the above statement as a valid
publication of the genus Ermania, while others
(e.g., Jafri, 1955, 1973; Jurtsev, 1975; Berkutenko,
1988; Czerepanov, 1995) did not. According to Article 34 of the Code (Greuter et al., 2000), Chamtion of the genii- I
% 1ml
. I'>-><
i
description of Ermania. it was m German, and the
germs remained invalidly published until Holsi han
tsev ( I95<a) pro\ i([r-,\ the Latin diagnosis, Therefore.
II
-Iers to Ermania proposed by Schulz
(1927a, 1933a, b, c) and Botschantsev (1955) remained invalid. As it is presently delimited, Ermania includes onh E. /lairyoides (Cham.! Bols. h..
the generic type, and all other specii s assigned to
it beloi
. r
i
(i does not occur
in the Himalayas and Central Asia and, therefore,
lied I
i placed in De-
Although superficially resembling some species

of Desideria and Christolea. I . ap
i
most closely related to Melanidion boreale E. L.
Greene. Both species have Arctic and subarctic
. nl
>n (the Russian Far East for the former
and Alaska, Yukon, and Northwest Ten' i
the latter) and are similar in habit, foliage, pubescence, flowers, and fruit morphology. Hulten (1945)
was lb. first to pom! oul tins . lose r.-lationship. ai:d
n '..n-li ir.-i| M. ::-li- |.. / ' /;,.; :.,/ Im' hi-li m>
i
il egitimate because Ermania was invalidly
publisln d. 'Flic prine pal dil'h rem e |>< lueeu thesi
species is that E. parryoides has latiseptate fruits
(Hatlened parallel |,i the s. (>lnm| and I/, bo;< air i a
ii
plate fruits (flattened at a right
the septum), but this difference is not as signihcaui
- oni e I in.! i 11. i i ise there are many genera of
the Brassicaceae with both fruit types. Drury and
Rollins (1952) and Rollins (1993) reduced Melanidion to synonymy of Smelowshia C. A. Mey, but
their circumscription of the North American Smeliinskid was so broad ihal x.ru- ol the species recognized are doublliilb coi g neric. Il 1/ !><>;, ,iir
and E. parryoides were kept in a genus distinct
from Smelowskia, as I presently support, then Ermania would have to be abandoned and the earlier
I 11-In 11 1/.
These two spe es wil bi dealt with in : subsi can ni pubb. al a

In his original description of Cheiranthus himalayensis and Christolea crassifolia, Cambessedes
(1844) did not indicate anything about their relalionship or similai In - lo e.n li other. I lowi \ ei. J dri
'),).)) phi
i ti- in ii
.. r I other species in
Christolea and adopted a broad generic concept
that im hided -pet ic- pn s<-nlh assignee lo ||-,e g. a
era C/,',-M'O''I,</, /A V. /r.'i.i / m \. //" v. M, :',:,;',:>,!:
Parrya R. Br., and Phaeonychium. With such a
i I I limitation, several additional genera, especially Pegaeophyton and Pycnoplinthus, could
have easily been included in Christolea without exloin
!
_ i n
ben
i
liuther. Unfortunalelv. JalriV dolim iation of Cbristolea was eloseb
tollowi
i ['in. i I1 MI
- nl floras (e.g., An,
1987, 1995; Hajra et al., 1993; Huang, 1997b;
Kuan, 1985).
<., /umikov and Yunussov (1978) also adopted
a rather broad concept of Ermania by including
Christolea and Oreoblastus as sections. These authors differed from Jafri (1955) primarily in their
dec ISIOII about the elieelne d, ie of valid pil lii a
tic
: Ermania. In my opinion, their vasiL IK i
erogeneous generic cm urns, i. II HI- .>l I

'.,',.
ni Eunatiia ire :ma. eeplahh f.7;/,istnlci consists ol
two species, the Himalayan C. crassifolia and the
Chinese endemic C. niyaensis Z. X. An. ai <1 it dit
Ices from Vfltin
i n ! i _ '
Ii
ing many-leaved steins, nonrosulate lower leaves,
exclusively simple trichomes, incumbent cotyledons, apiculate anthers, ami h
i i .
seeds. By enntras 1.', , .,
I - leafless stems.
well-developed basal
, ! - l mlritic trichomes
mixed wild -in i
i
> in i
i
ln]in v
aecumlieiil cotyledons, obtuse anthers, and longi-
< "In,si,,;, I A li.iv iv
IMIII.-
:.-.
MI
g il.ir in cross see-
tion, valves will

ginal veins, and
valve apices muted wild lli<- icpliiiu It..tin Chris
loir,I I>,:si,!,;>,t -11.11. I - li\ ha\ nig a n< I -dev, lop. si
hasal rosette, usually leafless stems, slender and
rhizome-like caudices, often palmately veined
leaves, iinntorulos
mi
iigil.idm Jl orient,
biscriatc seeds, and ic. iiml cut . ol \ I. dons 1'-, con
Irasl. Chnstolai das nonrosulate lower leaves, leafy
stems, compact and woody caudices. pinnatelv
veined leaves. strongly Inrulose fruits. transversely
oriented uniseriate seeds, and incumhenl cotvledons. Tin- Himalayan mil < . filial \sian Drs'.ii >in
also differs from tin- \n In
ilmn In lacking the dendritic trichomes and having
sessile 2-lohed -li-in -. -u;.olh IiuiN. Ins. tiale
seeds, atld loothed neelaries la. kin- the median
:d.m I- M hn.hi,."' d is d. ndiili. Iricdoincs. entire
and capitate stigmas on distinct styles, lorulose
flints, uniseriate 01 rarelv subbiseriate seeds, and
annular nectaries wild well-developed median
glands. A comparison of It, suh ,,, Witd I In presum-
witdoiil maiginal veins, I.- tadlv anceolate to ob1

bph in , ross -. < lion wi II
mas mind narrower than the slvle. Hv contrast.
almost always has dentate, p.dinatclv
veined leaves, prominently veined valves with well
i is. Inn .11 to Inn aidant . olate fruits reelaiigular In cross section, obseurelv
I l I oi i vim.hit stvl. s. and disiin, |. often
2 lol
stigmas as broad as the style.
OREOBLASTUS
Although Jafri (1973) admitted the artificiality of
his delimitation oi Christ ol en. lie (p. 1 .">.")) correctlv
slated llial. ""liven if. Clmslnlcii Caml). (s. str.) and
l-'itnaniit lid.mi e\ | Unlscliaiilsev | Scliul/ Is. sir.)
u. ecnsidt n
is sej nah g. ii.;..' In liav IIM Ire. instead <>i lulled sepals. .1
deciduous instead of persistent calyx, and septal.I the persisleiil calyx 111 several specimens llial sd,
111 1 in- d 1 1 '
hluslns. and the
holotype of her D. pamirica (Suslova, 1973) has
septate instead of eseptate fruits, though id. septa
are perforated hul never lacking. Kxeept lor having
free instead of united sepals. Oirohlnsius is indislitigiusliahle IK 11 Ih-suh-au. \s nidn it- d il.ov. .
ably related genera is summarized in Table 1.
In establishing the genus Eurycarpus, Botschantsev iCTtS) separated il from Ennnnin In having
hiseriate instead of Uniseriate seeds, broadly lanceolate instead of linear fruits, entire instead of
denlale leaves, m I. ii1 - in -I. id ..I l.-alv si apes.
However, lie ;n t|
I
I
i 1 - Iv tin type sp( cies of hold genera because most of the differences
above do not hold if one compares Eurycarpus with
the ten species Bolscdanlsev recognized in Ermaniti. As indicated above, eigdt of Bolschantsev's ten
species ol Ermunia are presently assign. : < /
sal,Tin. \ comparison ol' Dcsidcria with Eurycarpus
(two species) sensu Al-Shehbaz and Yang (2000a)
shows that the latter differs by having entire and
The presence vs. absence of a tooth on the median stamens was consid. -II In ame (e.g., Schulz,
1936; Hara, 1974; Golubkova, 1976) as an imporlaut generic character. In my opinion, tin- Icatuie
alone does not justify the segregation ol ueuera.
Toothed and toothless lilamenls are louii.l in Don
tostemon Andrz. ex C. A. Mey. (Al-Shehbaz &
Ohl.a. 2000). whereas winged or wingless, toothed
or toothless, an . |
n

i in i 11 i
:
aments are found in Alyssum L. (Al-Shehbaz, 1987;
Dudley, 1964).
Although Hara (1974) provided a detailed discussion to dishngiasli /- n,,;/,,,,j,.,,, Ii M / >/i,a;n,i
and related genera, the single character that sets
ipart is the presence ol a lateral tooth
tn the lilain. ills of median stamens. On the basis
of ill older . damctcis. F< tiu,io, :" ."aim! .11 I laia
Gamosepaly in Brassicaceae
?2
if JI
MI.
!|
llini III!1!!:-
I If .1 is
i lilt Irliil
lllllf
i 1 s I lit.
iMJIi1!! til! fill
ii
! I i
fil AuU
|j
ill,
1 ill! iPJiii siii1

!
Ml =
4i inJ
mi jliili:
ipim llii
iifj
I
I
IJ1 -I.si!
i E
n 33
, t
I 1
t 1:1 3:11 _ f
vj]
111- s -
I Jl
I I:i
i jiif ii nil mi
it , .1
if 1 II I
ill!1 i! I! iifj
I 111! !! III! III!
is perfc.-llv ,,t I,,,.,.,- it, hr.i,h;,. In la. I. Ham inill. .lifl lh;il /'. <><;.,!-, n-x-mbli - ihsuifun las /'<>,
rja) pumila in vegetative characters. A close examination of flower and fruit characters clearly
shows that the two spe, ies an
igen. rii . and I ,
..,,,.
- n .
mamopsis is reduced herein to synonymy of De.sif/erm. Unfortunately, both species have the same
epithet, and E. pumila is named hereafter as D.
haranensis. The median filaments of both D. pumila
and D. haranensis are dilated, and only the latter
species shows a minute to prominent tooth on the
median staminal filaments.
SOLMSLAVBACHIA AND LE10SP0RA
Deside
I(<:
' '">> " " Han,. I Jap. It..i
Oi
' "'
5?
''"'
Su
,(>:2
()]n
I') 198. 1974. TYPK:
'/" H;uHara/SJ
, .
h
Moscow & Leningrad)
,,, IUI^ ,, ,, ,, ,. ,;. ., h
Suslova.
Herbs perennial, with a slender, often manybranched, rhizome-like caudex often covered with
remains of basal rosettes. Trie-homes simple and/or
mixed with short-stalked forked ones. Stems simple, leafy or leafless, sometimes absent. Basal
leaves petiolale, insulate, simple. 3- to 9(to 11)-
On the basis of fruit morphology, Dendena is

most closely relal, .
>
., .) ,pp 8
to thed
endemic to China ami I - M. d.

I!
...
and Sikkim) and the Central Uian and llunalavan
Letospora (6 spp.). All three genera have fruits
,
,
,
||mm||
|i(||h
|v|,s
,,!,sal 0,,, s
" ' ,n,in' r toothwl- uh^ssile or P^0"
liU
; '" i;'l's,'"L li"'* 3" ,(> 30-floweretl, dense
"r ^ bracteate throughout or ebrac.eate.
bose, elongated or not elong^-'
are adnate apically to the replum. Upon maturity,

the fruit falls off the plant and its apex remain:
lanliK .It-Ins, int. The due- uinia also have ob
solete or no styles, and their fruit valves are strongIv angled at the margins and completely conceal
ilowers sohtai
the replum. These combinations of characters are

not found in any Himalayan or Central Asian genn-i <>l tin- Brassicaceae
Desideria is easHs separated from Solmslauhachia by having palmately veined leaves apicallv 3to 9(to ll)-toothed, ovate to oblong anthers often
less than 1 mm long, and forked trichomes sometimes mixed with simple ones. By contrast. Solmslaubachia has entire, pinnatelv veined leaves, lmear-oblong anthers more than 1 mm long, and
exclusively simple trichomes.
< ol,ten P*1*1? V*ined' Pfsistin6 whle r

'>'> 1-l.nN-s pers.sl.,... Caulme leaves smnlar to
on
Ped,cels
,a
f " "" -" ""- ""** membra

Ple< P^le-green, or rarely white, sometimes yel'"^h '" k'^ "' |,UI< - |lL"1'' "1",va,t" ,() patulate,
P
subemarginate; claw stmnglv ddlerentiated from ! I i
il> |
-i.- ,H lonpr than sr-
a ex obtuse to
Pals- Stamens 6, erect, tetradynamous; filaments

win
^'ss ()r rarely winged' toothless or rarely

toothed, free, dilated at base; anthers ovate to oblon
g' not apiculate at apex. Nectar glands 2 and
la,r,al
- (" ' ;u,(l ' "Ml11" "' <mlsu[r 1,as('s ol a11 sla"
* niiMlian nectaries present or absent. Ovules
to 70 per ovary. Fruit dehiscent siliques, linear
to lanceolate, latiseplate, rectangular in cross secdves papery, with a
10
eral pair nonsaccate, palmately veined leaves apically 3- to 9(to ll)-toothed, oblong-linear anthers
0.4-l(-1.6) mm long, and capitate, slightly 2-lobed
brous or
Leiospora often has Mmed ,., maimed seeds, miequal sepals with the lateral pair strongly saccate,
entire or marginally dentate leaves, linear anthers
2.5-3 mm long, and conical, prominently 2-lobed
stigmas with connivent, decurrent lobes.
absent; style obsolete; stigma capitate, slightly 2lbed. Seeds uniseriate or biseriate, wingless, oblong to ovate, often flattened; seed coat obscurely
reticulate, not mucilaginous when wetted; cotyledons aecumbent.
I
' stern China, and
adjacent central Asia.
TAXOMOMIC TKKATMKNT
Pilose> smooth, adnate with replum at fruit

apex; replum rounded, often concealed by valve
margin; septum complete, perforated, or reduced to
5a.
Leaf trichom. i>

nil u.,:l
long; petals 6-8 mm long
MK
I n n l!i in
i I
mifil
petals 11-14 mm long
,ers (3 to)6 to 30 in a raceme.
7a.
inm wide. prominentb reticulate veined

9. I), baiogionensi
nm wide, obscurely veined.
i
i i 1 .i!>
1
lit
,. sepals 3-4 mm
8. D. pumil,
[i in
>
i
| ill . i
II.
| ils 6-7 mm long;
7. I), [imlifi;,
Stem and pedicel iricliomes toiled
2. D. stewarti
seeds biseriale, (1.5 >l.i!2| 2.3) - 1 1,1mm

I. I), /,/,, ve,,w
Hb. 1 .nil li.uar. (O.JJ-ll-1.71-2) mm wide; petals I 5( 5.5) X 1.3 2.5 mm; seeds uniseriate, 0.8-1.1 X 0.5-0.8 mm
3. I), lineari
Racemes ebracteate.
forked, mixed with short simple ones
6. I), hamnrnsi
or distinctly forked.
< (Cumlicss.) Al-Shehbaz, comb. nov. Basionym: Cheiranthus himalayensis Cambess., in Jacquemont, Voy. Inde
4: 14. 1844. Ermania himalayensis (Cambess .:
0. E. Schulz, Notizbl. Bot. Gart. Berlin-Dahlem 9: 1080. 1927. Oreoblastus himalayensis
(Cambess.) Suslova, Bot. Zhurn. (Moscow &
Leningrad) 57: 652. 1972. TYPE: [W Tibet.]
In il 1 " ii
in n I
I! i kioubrungi
.. rp _,_ . .
I7. t
j
ghauti in lartana -n >
'
T-700 n. 1 x
T>! .
izi T>n
1782 (holotype, P!; isotypes, k!. P!>.
^
Plants 4-20 cm tall, densely pilose throughout
subglabrous. Trichomes simple, to 1.5 mm long.
tnple, pilose or glabrc
fleshy, pilose or glabrous, persistent; petiole 0.41.6(-3) cm long, not ciliate; leaf blade broadly obovate to spatulate, 4^14 X 3-9 mm, base cuneate
to attenuate, margins (3 to)5-toothed. apex acute.
. .,
.
,.
!
,
Stem leaves similar to basal or linear to lanceolate,
5-17 X 1-4 mm, often entire, short petiolate to
subsessile. Racemes 6- to 25-flowered. hraclcilc
throughout; bracts similar to stem leaves but small,
,
, ,
er, sometimes adnate to pedicel. Fruiting pedicels
pair 2-^ mm long; anthers ovate, ca. 0.6 mm long.

Ovules 7 to 12 per locule. Fruit lanceolate to linear-lanceolate, (1.7-)2-3.5(-4) cm X (3-)4-6 mm,
strongl) flattened; valves pilose or glabrous, distinctly veined; septum complete, membranous;
style obsolete; stigma 2-lobed. Seeds brown, ovate,
(1.5-)1.8-2(-2.3) X 1-1.4 mm, biseriate, minutely
reticulate.
.
_,
.
.
n,
I
.enrig June through August,
,
1^.1
T /
rruituu
y
, p
, ,. ., .
., .
Habitat and distribution. Alpine tundra, open
hills, sandstone scree; 4300-5300 m. China (Qing- Xizang), India, Kashmir, Nepal.
hai
CHINA. Qinghai:
, MNv\|>7
s|( u|| ,,,..
Baingoin Xian, Whale Lake, Wu, Ohba, Wu & Fei 4075
(Kl Y MO. I'll I . I M.....,-,-,. 11 I I'V 8056'E, G. & S.
964
7
i0ET
^
> MO); NW Tibet 3455'N,

82 211 . I'd,, 111 1
^ Qinghai.XiJng Team ,
, ,,
l,i.\i=,mf! Tram 7(i-<M)(,l .kl \. I'I 1. /., li.-sbm-: &
/li,m lh, Itnum il'l 1 l\HI \ 1'iinjab: Uhul, kangra,
B:,,;i La<h
'" K<"'l: 67:iH (GH)- KASHMIR. Harnag, UpI
I.l.i -ill- - ..;.-/ "/" (I. <.. k. Mil M.I'M
[
.n ^^ ^^ Dhampus ^
ascending, straight or curved, 3-10 mm long, pilose

or glabrous. Sepals free, oblong, 3-4 X 1.2-1.5
mm, caducous, pilose or with a terminal tuft of
and Fren(.h pass. Wald 65 (BM);
Thorong La. Ma.-svan.li

Valley. WBeath 1486(E); Naurgaon, Marsyand,. UcHcath
l4<)( K
> < >: Annapurna Himal. between N Annapurna Gla-
bans, base no, saccate, margins membranous. Petals purple or hlai

, ell
-I
enter, broadly
spatulate, (6-)6.5-8 X 3^1 mm, apex subemaxgin
ate; claw 3-4 mm long. Fila.n. t.i- wlut.. -ii/ii!
dilated at base, median pairs 3^1 mm long, latera
*$
^PO^V^^^GHT
'Cefa"'
roll.vli-.il> ol Dcsi,!>,:,, dncans {l,\on II. Si,un(

Slaintw, 3211) woe .il.-.1 by Jafri (1973) a
('h;>sii>:.n liuiKiiiiu-nsis. III.I ill. I:i-i hso \\ri. li>
:H>.->:>.
c.| |.\
llr<l-.
M ' 't i.':. i) . i- I ;<.!>, i
>:in,il;,<, >.
1 h
i be readily separated by petal size

...llh. a,,l
key). Mixed collections of the two species (e.g.,
Koelz 6738) are not uncommon, but no intermedial.-.- have been louii.l. Roth -|-< ii-s . an In distinguished from ihr related f). slant rtii by having leal'
.mil >lcm trirliom
.
i i i I
n pi. instead ol
forked.
Desideria himalayensis was reported (as Christolea) Itoin Xinjiang by An (1995), but I have not
seen an\ mat. 11 ,1
i
China. O
lection (Polunin, Sykes & Williams 37) was cited
by Hara (1979) as this species, but this collection
clearly belongs to Desideria linearis.
Desideria himalayensis was erroneously illustrated in Jafri (1973) with ebracteate inflorescences. It
is likely that the plant illustrated belongs to D.ftabellata, a specie- tli.it oeeui m
idei n \L
isl.in. I hma. k\rg\/stan. and Tajikistan bill i- not
vet report. .1 Inn k i a
I), sleintrlii. and l> linearis are the only three species ..I Desideria thai consistently have racemes
braeteate throughout.
2. Desid,
ewartiiff \ndeismii \I-Sh, hl,a/.
comb. nov. Basionym: Cheiranthus steward! T.
Anderson, in J. D. Hooker, Fl. Brit. India 1:
132. 1872. Ermania stewartii (T. Anderson) 0.
E. Schulz, Bot. Jahrb. Syst. 66: 98. 1933.
Roy. Bot. Gard. Edinburgh 22: 53. 1955. Oreoblastus stewartii (T. Anderson) Suslova, Bot.
Zhurn. (Moscow & Leningrad) 57: 653. 1972.
TYPE: Kashmir. Ladak, 15,000-16,500 ft., /.
L Stewart s.n. (holotype, K!; isotype, E!).
Plants 8-20 cm tall, densely pilose. Trichomes
k. I i uelv soul, smipli in ai ill. sit in
has.-. Stems simple, pilose or glabrous. Basal leaves
sublleshy. pilose, persist, lit; petiole 2-10 mill loll-.
not filiate: leal blade hroadb ohoxate to -patnlale.
gins 3- to 5-toothed or subentire. apex acute. Stem
es 8-
15-flowered, brad
, often adnate to pedicel. Fruiting pedicels asnding, straight or slightly curved, 4-12 mm long,
lose. Flowers not seen. Ovules 7 to 12 per locule.
uit lanceolate to lanceolate-linear, 1.7-3.5 cm X
-5 mm, strongly flattened; valves pilose or gla-
branous; style obsolete; stigma 2-lob.d. Seeds

brown, ovate, 1.4-2.2 X 0.8-1.1 mm, biseriate, minutely reticulate.
Phenology.
Flowering unknown. Fruiting in
Habitat and distribution. Scree slopes; 41005000 m. China (Xizang), India, Kashmir.
Selected specimens examined. CHINA. Xizang: Ali,
Geji, Qinghai-Tibet Team 76-8652 (PE). IM)I \ I'.mjal.:
Desideria stewartii is a very rare species known

thus far from the few collections cited ubow. Reports ol the species from China (Kuan. I'K'ur. An.
1987) are most likely based on misidentili.d plants
..I I) inmalayensis.
Jafri (1973) doubted the distinction of Desideria
stewartii from D
lli as Christolea),
citing one collection, Stewart 9349, under the former instead ol the lallei species. I have not -cell
any flowering material of the species, and the description of the flowers by Jafri (1973), which was
followed by Hajra et al. (1993) and An (1987), was
almost certain!) based on a small Howeim- branch
of D. linearis mounted on the holotype sheet of D.
In overall aspects of foliage and fruit, Desideria
slatarlu most closely resembles I). I,imala\ensis.
However, D. stewartii is readily separated b\ the
presence ol forked, stalked, intermingled trichomes
instead of exclusively simple straight ones.
3. Desideria linearis (N. Busch) Al-Shehbaz,
comb. nov. Basionym: Christolea linearis Y
Busch, in Komarov, Fl. URSS. 8: 636. 1939.
Ermania linearis (N. Busch) Botsch., Bot. Mater. Gerb. Bot. Inst. Komarova Akad. Nauk
S.S.S.R. 17: 166. 1955. Oreoblastus linearis
(N. Busch) Suslova, Bot. Zhurn. (Moscow &
Leningrad) 57: 652. 1972. TYPE: Tajikistan.
Pamir: Schugnan, Abchary, 2 Aug. 1904, B.
Fedtschenko s.n. (holotype, LE!).
Ermania parked (). K. Sehulz. Reperl. Sp. \..\ I.Y-III
Veg. 31: 333. 1933. Christolea parked (<>. K. Sehulz)
Jafri. Notes Roy. Bot. Card. Edinburgh 22: .",2. 1955.
Oreoblastus parkeri ((). K. Sehulz) Suslova. Bot.
Zhurn. |Moscow & Leningrad) 57: 653. 1972. Syn.
nov. T\ EK: Kashmir. Sonamarg. Euderwas, 13,(X)0
ft.. II Aug. 1928. K. R. Stewart 9H74A (holotype.
B!).
Ermania kashmiriana Darft Naqshi. J. B..ml.a\ \al. Hist.
Soc. 87: TA 1990. Svn. nov. \\ RE: Kashmir. Shalimar, Sonamarg (Sind Valley), 39(K) m. 20 Aug.
1983, G. H. Dar 7786 (holotype. KASH).
I ,;,i,nu,i I,-,, inn,,. Ih, A Yi.phi. I. I! >mki\ N.il. Mi l

Soc. 87: 277. 1990. Syn. nov. TYPE: Kashmir. Bali. I N n ,, |Siii<
ill ) 52 K) m, 2 Sep. 1982,
G. H. Dar 3934 (hololype, KASH; isotvpes, KASH.
MO!).
Plants 4-15 cm tall, densely pilose throughout
!:. s ihgl ibmns. Tru-homcs sin ; It-, to ! .A nun .en.Sterns simpb . pilose i i gl ihroiis. B.i-al leaves oi
llesliv. pilose or glabrous, persistent; petiole 2-7
(-12) mm long, not ciliate; leaf blade broadly obovate to spatulate, 4-15 X 2-12 mm, base un
.
to attenuate, nun, i'i- '
. Hoodie. I i
.1 -ah
. Polunin. Sykes & Williams 31 (HM). TAJIMNTAY Pamir: \ slope. ,,\er /or-Cliecliekl\. 12 \ug
I v,.,.
'.,,/,, w/ ll I | ( l.h, klK in
er /oi-Cheehekty, /vailora 228 (LE).
Although I have not seen the holotype of Er>!>ttnni kitstiftiir./'nt ih. i i eaiiai !--: r ip! oi i d
lustration, as well as the examination of a paratype
(Dar 8301), clearly support the placement ..I die
species in synonymy of Desideria linearis. Dar and
Naqshi (1990) compared E. kashmiriana and E.
,\ith D. stewartii and D. himalayensis (all
as F.nnania). h i! tin \ fail, d to r. lad :hen m.> < t
to Z). linearis. In my opinion, . kachrooi is only a
i i i- !
i
i i<-> within a gi\-
stem leaves but smaller, often adnate to pedicel.

Fruiting pedicels ascending, straight, 2-8(-12) mm
long, pilose or glabrous. Sepals free, oblong to
ovate, 2-3 X 1-1.5 mm, caducous, pilose or with
a terminal tul't oi hairs, has. not su eali . m ug lis
membranous. Petals purple ..
base, narrowly spatulate, 4-5(-5.5) X 1.5-2.5 mm,
apex rounded; claw 2-2.5 mm long. Filaments
while. sligrillv dilated ai liase. mediai: pan - 2
3.5 mm long, lateral pair 1.8-2.5 mm long; mthers
ovate, 0.4-0.5 mm long. Ovules 8 to 13 per locule.
Fruit linear, (1.5-)2-3.5(-4.2) cm X (0.8-)l-1.7
(-2) mm, flattened; valves pilose or glab .-. Iiliiictlv \eined; septum complete, men I a im< i
style obsolete: stigma 2-lobed. Seeds brown, ovate,
0.8-1.1 X 0.5-0.8 mm, uniseriate, minutely retic-
Phenology. Flowering June through August.

Fruiting July through September.
II
tuition. Gravelly or sandy
slopes, scree, gravelly moraine below glacier;
3200-5200 m. China (Xinjiang, Xizang), Kashmir,
Nepal, Tajikistan.
Selected specimens examined CHINA. Xinjiang:
Velieng \ian. /,/ linshcna el at. 1127!! (IT.) l'ag<l..m
baseli-Pamir. Pistan near Saryokol, Alexeenka 2,2V [I.hi.
X /.: Hti
i
.' om.son *.n |I5M. G. Gil. K.
P); Ali, Qinghai-Xizang Team 76-7948 (HNW I'!. IM)I \.
run,,I, I ,| I y
, i:, I l, La. Koeh 6738 (GH).
K \MIM||{. Ishkuman Aghost. Set,mid 2449 (G). Chitral:
hasp,,, illaehinl. .H(.2'\. 72 27'K. I,van It ( \. K): Simla.I. S ,,[ Shah Jmali Pass. Slainlon 3055 (Kl: Dorali Pass,
hulk., \allev. Slainlon 3241 |K|: \niarnath. Stainton 8709
ill: Nmamai-g. Luderwas, Stewart 9874 (H. (,. MO), kai akorrim: I .>I;IIVSI i.la. ie L:r ; , aip. !. - mi. I . .1 \au '.
I'olunui 6133 (BY1): karakoiimi. O.I. 1877. Clarke s.n.
(M. I.a.lak: abme Stuk. Maurrll <>2 iK): Zanskar, glacier
S.a.lik. .5IA. 7() K. I)eit,,l,e 27 <Pl Thui region: ea.
2(H) km NW of Gilgit. near watershed -epn-.a an- (, h-.l
from Chitral. Hraadhead 39 (E); Taklung IA Koeh 6500
((ill). NEPAL Naur Pass. Lowndes 1159 (BM); 5 mi. S of
popul ition of which one can find glahr J- n ;

pubescent plants. In general, plants oi Ih-side,,,,.
including D. linearis, that grow in parti. din.Id
areas. esp< .1!
'
n I. rs. often have
the apex of the caudex elongated so thai the leaf
rosette appear^ much less congested.
Several authors (e.g., An, 1987, 1995; Kuan,
1985) followed Jafri (1955) in listing Desideria linearis as a synoi
these authors erroneously recognized C. parkeri as
a distinct species In m\ opinion, the last species
is onl\ .! glab:
ai hair of/A linearis, in fact, C
parkeri is based on Ermania parkeri, an invalidly
species assigned to the invalid Ermania
(see Greuter et al. (2000) under Article 43.1).
Although Jafri (1973) main
keri, he correctly indicated that it is not different
from the earlier |
<
,a las Christolea)
tin, uris. a sp. . ie.- d a' he did not r< < i-.ni/i loi I'ah
istan and Kashmir. However, Suslova (1972) maintained both species las Oreoblastus) and separated
them mainly by the presence in the former of a
subapical tuft of hairs on the sepals instead ot its
absence in 1). linearis and I), himalayensis. Obviously, this distill. Hon is artificial, and all taxa have
pubescent sepals that often are more dens.lv ham
below the apex. The restriction of trichomes to the
sepals and leaf apices is quite frequenl in glabn
enl I
' himalayensis.
Schulz (1931) considered Desideria linearis (as
Ermania parkeri) to be closely related to E. albiflora (T. Anderson) 0. E. Schulz, but the nearest relative of the first is D. himalayensis. As shown by
Al-Shehbaz (2000b), E. albiflora belongs to the genus Phaeonychium 0. E. Schulz.
Desideria I in,
i i
variable in the occurrence and density of the indumentum, fruit
width, length, an
i.duu him aid number of leaf
I.-, til. I low.-\. i. in - uain hoi al main ; I iior i lii.
s.n. (I 1 . \|()|; \kl \ian. Oiaornong. S. G. Wit. ).

II. Wit & ). In loll (IINWIl kl \). kMiCW.STW
Semirechie; Przewalsk, river kavehe. .".(> Jul\ PUT
Shtshbin s.n. (IT'.). 2 Aim. I'M.'}. Ctnmznnil.ms.,,. |\1<.
Tianshan: Glacier ka.ndi. Brorherel ." ,). I AJIklSl\\. Shu-nan: I- Hukl.ara. near l\,~ (.aim (.kislnnv.
Tuturin 150 (\. I.I I I'amir: knm-h.K l,l;inn.U/,mH191 (LE).
SLIUI
4.
Desideria flabellata (Regel) \1-Shehha/.

comb. nov. Basionym: Parrya flai
- l; I
Bull. Soc. Imp. Naturalistes Moscou 43: 261.
1870. Christolea flabellata (Regel) N. Busch,
in Komarov, Fl. URSS 8: 330. 1939. Ermania
flabellata (Regel) O. E. Schulz, Bot. Jahrb.
Syst. 66: 98. 1933. Oreoblastus flabellatus (Regel) Suslova, Bot. Zhurn. (Moscow & Leningrad) 57: 651. 1972. TYPE: Southern Tian
Shan. Dschaman-Daban, Sewerzow s.n. (holotype, LE!).
Huang CG-81-154 (lioloiype, IINWP!).

Plants greenish, 415 cm tall. Trie-homes simple,
straight. I" 1.5 linn long. Stems distinct, simple.
densely pilose. Basal leaves subfleshy; petiole 2-7
mm long. pil<isc; leal Made llabcllate to broadlv
obovate, rarely spatulate, 0.6-2.5 X 0.3-2.5 cm,
pilose, base
to 9(to ll)-toothed,
acute; teeth to 10 >
basal. Karelins 7
l<> 12 ilouered, ebracteate.
Fruiting pedicels as.ending, straight to curved,
(0.5-)0.7-1.5(-2.5) cm long, spreading pilose. Sepals lice, narrowly oblong. 5-8 X 1.5-2.5 mm. often pei-istent. pilose, base not saccate, margins
membranous. Petals purple, broadly spatulate. 1.1
1.5 cm X 3.5-6 mm, apex subemarginate; claw 79 mm long. Filaments white to mauve, slightly dilated at base, median pairs 4.5-6 mm long, lateral
pair 3^1 mm long; anthers oblong, 0.9-1.3 mm
lorijj. Ovules 7 to 12 per locule. Fruit lanceolate to
lanceolate-linear, (1.7-)2.5-3.5(-4.5) cm X 2.5-5
mm. strongly flatten.-.1: valves pilose. distinctly
veined: septum complete, membranous; style obsolete; stigma 2-lobed. Seeds brown, ovate, 1.3-2
Phenology. Flowering early July and August.

Fruiting late July through earlv September.
Habitat and distribution. Alpine gravelly
slopes, moraine slopes; 3300-5100 m. Afghanistan,
(Tina (Xinjiang). kvtgv/sl.m. Tajikistan.
Kush. Gilbert 88 (K). I'arvan: Panjshir, //<./. A" II

drib,, .././ (Kl. Kai.isa: Mir Sinn, are:i. Gibson 211 ill
Takliar: klh-l ,, h-i ,,. vnll.-v I".. hani-Tai. I. ol 'Chun
duk. I'ndlnh //;;;- M.i, CHINA Xinjiang: Kashgaria,
In every aspect of trichome morphology, flower

size and color, and habit, Christolea pinnatifida is
mdis'iiiimish ihli ir..m pi.mis el l)<s.,i> i ,, '!,!<">< I,",i
In. The t\|ie ol I he lorn,, i has in ii nits and is rather
immature. It dill.
mi Ivpical plants
of D. flabellata by having slightly elongated, spatulate leaves instead of typically Habellate ones.
Huang (1997a) considered C. pinnatijidit lo be related to C. kanil.orumcriMs. but the latter is a svnonym of D. mirubilis and has sepals typically milled
instead ol li
glandular n
!
Desideria nor
has any glandular trichomes oi papillae.
5. Desideria ineana (Ovcz.) Al-Shehbaz, comb.

nov. Basionym: Christolea ineana Ovcz., Sovetsk. Bot. 1941(1 & 2): 151. 1941. Ermania
ineana (Ovcz.) Botsch., Bot. Mater. Gerb. Bot.
Inst. Komarova Akad. Nauk S.S.S.R. 17: 164.
1955. Oreoblastus incanus (Ovcz.) Suslova,
Bot. Zhurn. (Moscow & Leningrad) 57: 652.
1972. TYPE: Tajikistan. Darvaz: Mt. Masar,
glacier Abdul Gassan, 11,000-12,000 ft., 23
July 1899, V. I. Lipsky 1936 (holotype, LE!).
Plants 4-15 cm tall, densely tomentose throughout. Trichomes shori-sialked forked and simple, to
1 mm long. Stems simple, tomentose. basal I. aves
subfleshy, canescent, densely tomentose. persistent:
petiole 0.5 2 mm long, not filiate, unexpanded and
not papery at base; leaf blade broadly obovate to
spatulate, 4-13 X 2^8 i
bracteate. Fruiting pedicels ascending, straigh

7 mm long, tomentose. Sepals free, narrowl)
long, 5-7 X l.|
. Petals
purple with palei
18 X 4-6 mm, apex r
filaments white, slightly dilated at base, median
pairs 5 <i mm long, lateral pair 3-4 mm long; anlln is iiiovvlv oblong, 1.2-1.5 mm long. Ovules 25
to 35 per locule. Fruit linear, 3-6.5 cm X 2.5-3.5
mm. strongb flattened: valves tomentose. distinctly
! 87, Number 4
2 I
Phenology.
ssn. oblong, 1.2-
Flowering July. Fruiting July and
Hi
Hon. Alpine gravelly areas,
3300-4600 m. Endemic to Tajikistan.
Selected specimens examined. TAJIKISTAN. Pamir\lay: Sauk Data valley. Ikonnikor 1787H(\.E). Bukhara:
Darsaz. rati".- of IVler-lh.--( .real, glacier \ereshkav. 2>
July 1899, Lipskys.n. (G, LK).
6, Desideria haranensis Al-Shehbaz, nom. nov.
Replaced nam. ' if, />
, , ' - III I I i i
J. Jap. Bot. 49: 200. 1974, not Desideria pumila (Kurz) Al-Shehbaz. TYPE: Nepal. Ca. 5 mi.
SW of Saldanggaon, 26 June 1952, very loose
scree, 19,500 ft., N. Polunin, W. R. Sykes &
L. H. J. Williams 24 (holotype, BM!; isotypes,
A!, BM!, E!).
Plants 2-6 cm tall. Trichomes simple, straight,
to 0.5 nun long, mixed on leaves with short-stalked,
unequally branched forked ones. Stems erect, simple, pilose to hirsute. Basal leaves fleshy, persistent; petiole 2-12 inn
ii
-.pars Is to .lens. I\ pi
lose with simple It ieliomes. eili.ite at base, not
expanded or papery at base; leaf blade broad Is
ovate, suborbicular, to obovate, 3-13 X 3-11 mm,
-e cuneate or obtuse, margins 1- to 5-toolbed. apex obtuse. Stem
leaves absent. Racemes 3- to 8-flowered. ebraeteale. Pedicel divaricate, straight, 412 mm long, pilose. Sepals tree, oblong, 3.5^4.5 X 1.7-2 mm, caducous, pilose, base not saccate, margins
membranous. Petals white tinged vvitli greenish
blue, obovate, 6.5-8 X 3^4 mm, apex obtuse: class
3^4 mm long. Filaments white, flattened, suhapiii toothed, median pairs 3-4 mm long, lateral
pair 2-3 mm long; anthers oblong, 0.9-1.1 mm
long. Ovules 5 to 7 per locule. Immature fruit linear, flattened, sessile, straight, retrorsely pilose:
septum complete; style-like apex glabrous, to 1.5
mm long; stigma capitate;, subentire. Seeds not
Phenology. Flowering in June.

ition. Scree slopes; 50005900 m. Endemic to Nepal.
Desideria haranensis is named in honor of Hiroshi Hara (5 January 1911-24 September 1986),
an eminent Japai - I
mi
I the discoverer of
this species and D. nepalcnsis. The new name is
propos.-d l < i i-t lh. 'I m-l. ..'/,-,
tin |o Dcsii/ena s\o ild ere, I. a homotiv n: oi /J , ,nr.

ila (Kurz) Al-Shehbaz, which is based on the earlier
p ihhslied Pan MI juiiinin iki.:/. Ii! i'l).
Desideria haranensis is a very rare species
known thus far only from the two collections cited
above. It is most closely related to D. pumila, from
which it is distinguished by having papery instead
.I' dii kisli ( iioiai Ii I-. -. loolhi (I in.-h I I oi |o.,l|i
less filaments, subentire instead
2 >b<
h i
and several-flowered racemes instead ot solitary
7.
Desideria prolifera (Maxim.) Al-Shehbaz,

comb. nov. Basionym: Parrya prolifera Maxim., Fl. Tangutica 56. 1889. Ermania prolifera
(Maxim.) 0. E. Schulz, Bot. Jahrb. Syst. 66:
98. 1933. Christolea prolifera (Maxim.) Ovcz.,
Sovetsk. Bot. 1941(1 & 2): 151. 1941. Oreobtaxtns proli/crus (Maxim.) Suslova, Bot. Zhurn.
(Moscow & Leningrad) 57: 652. 1972. Christolea prolifera (Maxim.) Jafri, Notes Roy. Bot.
Card. Edinburgh 22: 53. 1955. TYPE: China.
Tibet: Kon-chun-ua, 14,500 ft., 3 July 1984,
N. M. Przewalshi s.n. (holotype, LE!; isotypes,
K!, P!, PE!).
Plants scapose, villous to pilose. Trichomes simple, straight, to 1.5 mm long. Stems absent. Basal
leaves suhfieshy; petiole (0.2-)0.8-2(-3) cm long,
persistent, sparsely to densely pilose or villous, eiliate, somewhat papery at base; leaf blade broadly
ovate, suborbicular. obovate, to spatulate, 2-10
(-15) X 2-9(-12) mm, villous or pilose, base obtuse to cimeate, margins (3 to)5- to 9-toolln :. ran Is
Flowers solitary from basal rosette. Pedicel ascending-divaricate, straight, (0.2-)0.5-1.5(-2.5) cm
long, s illoiis. Sepals free, oblong, 6-7 X 2-2.5 mm,
usually persistent, pilose, base not saccate, mai in
membranous. l'etal> purplish green, broadly obovate, 1.1-1.4 cm X 4-5 mm. apex sub. marginal.-;
claw 6-7 mm long. Filaments while, dilated at
base, toothless, me.han pairs 46 mm long, lateral
pair 3^4 mm long; anthers 1.2-1.6 mm long. Fruit
linear to linear-lanceolate, (2.5-)4-6.5(-7.2) cm X
(3-)4-5 mm, flattened, sessile, straight; valves obscurely seined; replum and valves pilose to villous;
septum . ompl. i
i i - i n
|.il i. 2
lobed. Seeds oblong, 2.5-3.5 X 1.4-1.7 mm.
Phenology. Flowering July and August. Fruiting July through September.
ind distribution. Scree slope-, sib
ceous shist; 4700-5900 m. Endemic to China
(Qinghai, Xizang).
JSOUI
al rosette. Pedn da
n liti-
IH.II
-i
i lil
3- 10 nun long, pilose. Sepals free, oblong, 3^1 X

1.5-2 mm. caducous, pilose, base not sat tale, niai. (,. X S. Miehv Om/OH ;()KT. M<: \ue Shan
a 470 (HNWP). Xizang: Nyainqenlangula Shan. \ <>l DaniMiim. 3()"3<)'Y 915'E. (,'. # .S.
MerV, SW9.5//4 (COET, MO); Mekong-Salwecn divide,
pass K of /oiigang/VXangtla. 2">'I2'Y 980'E, /JK-W
m,o ;ot:f. \i<. i),.,..i;, SI,.-,. Mas,. \i.-, ?,W:/-<
7*/-/ 7r.///; ,..' /;',.; ikl Y I'E): liim \ia.i. f,u Teng Shan,
Qinghai-Mzanf! Iron, 11172 ikl M: /hr.,,,.1,. >.<,..,./....
7I6e/ 7im 655V (KUN); peak of Sengge. neai s|
|u .
Yubrong, 24 July 1951, Aufschnaiter s.n. (BM)
Maximowi.
, 'p
ii. I /y
(as Parrya) with D. himalayensis and Z>. flabellata
,11 l ill'.. |ss, HI lllrll ll^'HlgUI-tnHg 'I.IS,1. IrT- Bo! 'l
I). !<!;. 1,1 llld /> ,'/./,V /',// 5 ll,l\C -mill,II lloVV.-|
size ami theii < alvces lend to persist. The principal
feature separating llicm is that the flowers in D.
flnlx li.ihi in ariang. .! in distiia : ra. emes. whereas
in I) ],>Hlr,-,, ih, v aie -nli!ar\ Irom the liasal ro-
8. Desideria pumila (Km, \!l <U, hi.:.

. -mi
iiov. Basionym: Parrya pumila Kurz, Flora 55:
285. 1872. Christolea pumila (Kurz) Jafri, Fl.
West Pakistan 55: 157. 1973. Vvedenskeyella
pumila (Kurz) Botsch., Bot. Mater. Gerb. Bot.
Inst. Komarova Akad. Nauk S.S.S.R. 17: 176.
1955. Solmslaubachia pumila (Kurz) Dvorak,
Folia Prirodovcd. Fak. Univ. Purkyne Brne,
Biol. 13(4): 24. 1972. TYPE: Kashmir (as Tibet). Rupschu, 15,000-18,000 ft., F. Stoliczka
s.n. (holotype, CAL?; isotype, K!).
/nnan,,, Loch,, <>. K. Srhulz. Bepe.t. Sp. Nov. Begin Veg.
31: 332. 1933. TYPE: Kashmir. Bupshu. kvensa hi.
19,000 ft., 9 July 1931. Waller Koch 2231 (holotvpe.
B!).
tuna Botsch., Bot. /hum. (Moscow i\" I mm
grad) 41: 730. 1956. Based on the invalidlv published (see helow) K. Injuria Botsch., Bot. Mater.
Gerb. Bot. Inst. Komarova Akad. Nauk S.S.S.B. 17:
164. 1955. Oreoblastus bifarius (Botsch.) Suslova.
Boi. /hum. (Moscow & Leningrad) 57: 652. 1972.
holdt Batige. Ulan-Buluk. 42(H) m. 30 June 1894. Wi
Rohoiaivsk, s.n. (holotvpe. I.E!).
Plants seapt.se. pih.se to tomeiitose. Trichomes
simple, straight, to 0.5 mm long, mixed on leaves
with short-stalked forked ones. Stems absent. Basal
leaves fleshy; petiole 2 10 mm long, persistent.
densely pilose with simple ti if homes, filiate, expanded and papery at base; leaf blath I
Ih
ovale, sul.orl.itnl.it. ol.ovate, to spatulate, 2-14 X
1-11 mm, densely tomentose or pilose, base obtuse, margins 3- to 7-toothed to repaiid. apex <>l>-
: in- men bianoas
P. lals are;
IM\
W hIi>-
'- : i, phsh
green, broadly obovate, 6-8 X 3-4.5 mm, apex

i l> ii ughiate; claw 3-4 mm long. Eilameiits
whit. . diluted a! bast . loolhless. median pans 3 I
mm
mg. laleial paii 2 2.5 mm long; anthers nai-
.. .1 nig, 0.9-1.2 mm long. Ovules ca. 7 per

lociile. Immature liuit oblotig lir.eai I . line n l.m
ceolate, 1-2 cm X 2-3 mm, flattened, sessile,
straight, rctrorst
plum; valves glabrous; septum complete; style obsolete: sligma capitate, 2-lobed. Seeds not seen.
sbisl;
12(10-5800 m. China (Xinjiang.? \./ang).
Kashmir.
Botschantsev's (1955) description of Ermania biJaria was invalid 1 . i i-.. '.. [ I i - I the species in
what was ih. n an n
I g. mi- \\ hen
he (Botsehantsev, 1956) validated Ermania, he listed A', Injuria with full reference to Ins eaili.i work.
Therefore, the correct date of the valid publication
of . bifaria should be Botschantsev's 1956 instead
(1955) recognized two species in
Vvedenskeyella Botsch., of which the generic type,
V. kashgarica Botsch., has been transferred to
Phaeonychium (Al-Shehbaz, 2000b). The second
species, which is based on Pdirvil pumila, is asIgl .a! ben ': l)< ;<', ',-'. \pp irrmU. Ii.a-r! .mis.
did not examine the type material of P. pit mi la. as
. . i.lei .1 lion in-, des. I iplioli ol ibe same species
sainia In having a thick and compact instead of
slender and rhizome-like caudcx, pinnatelv veined
instead ,.f often palmately veined leaves, incumbent
instead of t
Desideria pumila was said to occur in Xizang
(Kuan, 1985; An, 1987), but 1
material olhei than the tvpes cited above, which
were collected ,'n i:
iisidi nil tin
h'u; 4 i. ku-hinir. Jain I 1073)
-p. i ic- (as (J,!, ;:.,'.',/) It) be \er\
closely relaletl if indeed different from whal Incalled C. lanuginosa (Hook. f. & Thomson) Ovcz.
However, the last species is clearly unrclai. l In I)
Al-
9. Desideria baiogoinensis (K. C. Kuan & Z. X.

An) Al-Shehbaz, comb. nov. Basionym: Christolea baiogoinensis K. C. Kuan & Z. X. An, in
C. Y. Wu, Fl. Xizang. 2: 388. 1985. TYPE:
China. Xizang: Baiogoin, 5100 m, 18 June
1976, K. Y. Lang 9460 (holotype, PE!; isotype,
PE!).
Plants scapose, villous. Trichomes simple and
lii.il stalked forked, straight, to 1 mm long. Stems
bscnl B - 1 i.
cs subdesli
x-tiole 0.4-1.6 cm
long, persistent, villous, ciliate, somewhat papery
at base; leaf blade broadly ovate, suborbicular, or
obovate, 4-8 X 3-6 mm, villous, base obtuse to
cuneate, margins 3- to 7-toothed, apex a< tile. Stem
leaves absent. Flowers solitary from has,! rnsi-lh
Pedicel ascending-divaricate, straight, 0.5-2 cm
long, villous. Sepals free, oblong, 4-6 X 1.5-2.5
mm, usually persistent, pilose, base not sac<
margins membranous. Petals purplish, broadly
ovate, 7-1.2 cm X 3.5-4.5 mm, apex subemarginate; claw 4-6 mm long. Filaments white, dilated at
base, toothless, median pairs 3.5-5 mm long,
eral pair 2-2.5 mm long; anthers 1-1.2 mm lo
Ovules 15 to 20 per locule. Fruit ovate to lane
late, 1-2.5 cm X 6-9 mm, flattened, sess
<
cs
ininci
rh ulate veined; replum and valves villous; septum complete; style
0.5-1 mm long; s m;i c;j|
J-lobed. Seeds oblong, 1.5-2 X 0.8-1.1 mm.
.''..
>gy.
Flowering June and July. Fruiting
July and August.
Habitat anil distribution. Open sand and gravel; 4700-5600 m. Endemic to China (Qinghai, Xiz-
\-lrded Vw, imrt^n amined. lll\ \. Xizang: Vmdo

\MII. Ian Ih;hu ItHtl'J <\\\\\\\ kl \| 15 r, m \,.,
Lang Kaiyong 9469 (PE). 9487 (KLJN): Tumain, Yang
a rig Team 177
(IINWPl
h,in
i .
|.li
'ill i li in n
(..I..
ti ,
'_
! i I
'..
I.
X S
\\ij
Uieht
i .oi.r. \K.
The species was inc ud

hai (Huang, 1997b), but :
terial from that province.
: Flora of Qing-
10, Desideria mirabilis Pamp., Bull. Soc. Bot.

Ital. 1926: 111. 1926. Christolea mirabilis
(Pamp.) Jafri, Fl. West Pakistan 55: 160. 1973.
TYPE: [Kashmir.] Karakorum; above Caracash
Valley, Chisil Gilgha Pass, 5360 m, 28 June
1914, G. Dainelli & 0. Marinelli 2 (lectotype,
here designated, Fl, photo!).
. TYPE: Chi25 July 1989. Karakorum-Kiinliai Expedition 51(10

(holotype, HNWP!, listed as NWBI).
/ i
- i \ -vii i; isi io
163. 1973. Syn. nov. TYPE: Tajikistan. Pamir: above
Czeczekty, near Zor, 4900 m, 10 Aug. 1970, T. Suslova s.n. (holotype, LE!).
Christolea suslovaeana Jafri, Fl. West Pakistan 55: 158.
1973, not Christolea pamirica Korshin.sk>. Men.
Acad. Imp. Sci. Saint Petersbourg, ser. 8, 4: 89.
1896. TYPE: same as that of Desideria pamirica.
Plants 2-10 cm tall. Trichomes simple and to 1.5

mm long, rarely mixed with forked ones. Stems disiple, densely pilose. Basal leaves subfleshy; petiole 3-15 mm long, densely pilose, not expanded or papery at base; leaf blade flabellate to
spatulate-orbicular, (2-)5-15 X 3-9(-15) mm, pilose, base cum
acute; teeth to 8 mm long. Stem leave
basal. Racemes 8- to 20-flowered,
Fruiting pedicelending
-lit to curved, 510 mm long, spreading pilose. Sepals united, (2.5-)
3.5-5.5 X 1.5-2.5(-3) mm, persistent, densely pilose, base not saccate; calyx lobes ovate, unequal,
0.5-2 mm long, margins membranous. Petals purple to purplish green with yellowish base, obovate,
5^8 X (1.5-)2.5-3 mm, apex obtuse; claw 2.5-4
mm long. Filaments white, sligl
median pairs (3-)4-5 mm long, lateral pair (2
)2.5-3.5 mm long; anthers oblong, 0.5-0.8 mm
long. Ovules 12 to 18 per ovary. Fruit linear, l-2(-^3)
cm X ca. 2 mm, slightly flattened to subterete;
valves pilose. <lii
I'turn perforate or
reduced to a narrow rim, membranous; style obsolete lo 0.7 mm S.-M:'. -ii-.n;.i '2 \< I< 1 <fi1.5-1.8 X 0.8-1 mm, papillate.
Phenology. Flowering July and August. Fruiting August and early September.
Habitat and distribution.
Gravelly slopes;
4000-5000 m. China (Xinjiang), Kashmir. Tajikis-
Srtevted specimens examined.
KASHMIR. Karako-
-I .Inn- I'M i "

V 1/.,..,-, J ,,,!,. Ih I \|l
KISI W. I'a,ir: lt;1,lakhsl.;,.i ML. , lose l river Maldzhuran, Tzvelev 700 (LE); Badakhshan Mt.. 7 km N of Pass
! I.I
,., / reic, l<)6(h ill I H.MIAIWII.U, Ml IK,
sin of river Pshart. Tzvelev 535 (LE); valley of river Chunjabay, Kuzmina 6060 (LE): Cheekektv slope, 19 Aug.
I
ikov s.ru (LE).
Although Pampanini (1926) did not cite am colic tlnlis Wlllllli ill. oMjiin, I .(:^,'('.j.:.->n il Ih -, U-t,
eding discussion
ran- membranous. I'd ds '.'purplish, obovale. 1 I

rd. .IIHI he (I' 111 . mi i I'l i()l i i tin details nt
these three syntypes.
By their reduction of Desideria mirabilis to synoii\ rm . 1 ( !:<;>,ixlh<!.-, I<:i>htla\e;;s;s (as /','.'//o//,M in
Christolea), Sehulz (1927a, 1936), Botschanlsev
(1955, 1956), and Jafri (1955) overlooked the fact
that the latter species has bracteate instead of
ehracteale racemes, septate in-lead of eseptate
fruits, tree instead of united sepals, and limi- '
1.5 mm instead of ca. 2 mm wide. The differences
lielvveen the |\\.. spi i h - an
. i .
I ihanl to imagine tllc\ ne cmispi eille
Although they correctly noticed that the sepals
i'i (
'
i i mli d. \\ n and
An ( 109 !) were pioli
in i in I '
dhili.s, a species endemic to the Karakorum Mountains and indistinguishable m even aspect from
.lain ( l<)55) did not mention the connation of sepals in hi- origi
;
I -ugh the illustration clearly shows gamosepalous calyces. By contrast, his (Jafri, 1973)
dliistiatinti .lid not di<w gam sepal\ aecurateb.
though holh illus1iali..ris wcie hased on the s<line
specimen. However, lie mentioned that the sepals
are "rarely connate below." Jafri (1955) suggested
that C. scaposa is related to C. prolifera, while he
(Jafri, 1973: 158) indicated that the species is
closely related to Desideria suslovaeana e\cepl for
"the absence o| septum and slight difference in
abl. In i: /' s:,i, u :),;al,,':.- ai d is u related to l>
ptoli/ern. The laltei has solilan Mowers and deciduous polvsepalous i.ibces. wheieas /'
hastheflowersinracenies.il I
i lei
- j
11. Desideria nepalensis H. Hara, J. Jap. Bot.

50: 264. 1975. TYPE: Nepal. Barum Valley,
17,700 ft., 26 May 1954, L. W. Swan 71-72
(holotype, BM!).
Plants 2-3 cm tall. Trichomes simple, straight,
to 1 mm long. Stems mmute. simple, glabrous Baal leaves siibfleshy; petiole 2-5 mm long, sparsely
pilose with simple trichomes, filiate at base, not
expanded or papery at base; leaf blade broadly obovale to subflabellate. 2-3 X 1-3 mm, densely pu-
2-4.
ehracteale. Pedicel ascending, straight, 3-5 mm
long, solitan from basal rosette, spreading pilose.
Sepals united. T> <i .'. 1 mm. densely pilose. base
not saccate; eal\\ lobes ovate. 1.5 2 mm long, mar-
13 X 5-6 mm, apex obtuse; claw 6-7 mm long.

Filaments slightly dilated at base, median pairs
4.5-5.5 mm long, lateral pair 3^4 mm long; anthers
>bl nig. " "' 1 I tun; 11 11, i ' )\ il e n iinbei. Iiillls. and
seeds unknown.
Desideria nepalensis is known only from the type
collection made at an altitude of about 5400 m. It
is ic.ulib distinguished from I), mmdiilis b\ its
much larger flowers (see key).
.1. \m..M \rl,r. (>8: 185-240.

. 1988. The genera of Sisymbrieae (Crueilerae:
1990b. limyopsis gamosepabi (ISM-M. irea. a

able new species with gamosepaloiis calvx. Ann.
ri Bot. Card. 77: 843-844.
2000a. A revision of Pegaeophston (BrassicaEdinburgh J. Bot. 57: 157-170.
2000b. A revision ol 111< genus l'li,ie<>n\rbiiiiii
caeeae). Nordic J. Bot. 20: 157-165\
r. 1997. Arabidojisis t'cinosr/xilu
- X S.
.'.:
.,,.1 I'.ip. B..t. (in press).

stolen. In: T. V. Clieo (editor). Fl.
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1955. I)e Crueiferis nolae erilieae. Bot.
Mater. Gerb. Inst. Komarova Akad. Nauk S.S.S.H. 17:
160-178.
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Pakistan and Afghanistan. Bot. Zluirn. (Moscow & Leningrad) 41: 728-732.
CaniLi-sseiles. J. 181 1. I'l.iNl.ie ratmie-. quas in India or
ientali eollegil Victor Jacquemont. Pp. 1-56 in V. Jaequemoi.d (editor). Voyage dans Pintle etc. 1828-1832.
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Dar. G. H. & A. R. Naqshi. 1990. New plant taxa from
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274-279.
Drury, W. H.. Jr. & R. C. Rollins. 19.12. The North \m,-rlean
re,,,,-,
,,
dora 54: 85-119.
Kuan. k. C. 1985. Crueiferae. /,,.- C. Y. Wu (editor). Fl.

Xizangica 2: 323-411. Science Press. Beijing.
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Dudley, T. R. 1964. Synops.s of the *,..,. t/^wm, J

Arnold \rbor. 45: 358-373.
|'
'
I
"'
J,1" fcngutica. Imperial Academy of Sciences Press, St.
Golubkova. V. P 197.
|( I IK lit 1.1. t
\<>\ .1-11
1.1
IJ'1-I '.II
Greuter W R K I.
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,1.
i
K.rk& P.CSu II,
,
I. >i loi 1 \tanl I'liul ' II i i . inn i < J. 129.
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'" " N'"1-"1
P. C. Silva. J. F. Skog. P. Trehane, N. J. Turland & I).
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eastern Himalaya (15). .]. Jap. B..I. 19 193-205.
eastern Himalaya (16). J. Jap. Bot. 50: 263-271.
. 1979. Crueiferae. In: H. Hara & L H. J. Willia.n, (edih.rsi Vn
.
, n
I I
of Nepal. Bull. Brit. Mus. (Nat. Hist.), Bot. Publ. 810:
Hedge, L C. 1968a. Arabidieae. In: K. H. Rechinger (editnr^
I
\L . I .
I,
I ... I
to, . Fl
I I. Iran
I,an. 57.
193-218.
Akadem.sche
Uruck-u.
ri | Mtalt, Graz.
. 1968b. S,sM, I ,
k II C..I
,
I
,
Fl. Iran. 57: 309-342. Akademische Druck-u. Verlagsanstalt, Graz.
Hooker. J. I). & I. Iht.m
I II
Indicam. Crueiferae. J. Linn. Soc, Bot. 5: 128-181.
&T. Anderaoi L872. Cruci
In: J. D. Hooker
(editor), Flora of British India, 1: 128-167. L. Reeve,
Huang. R.F. 1997a. New plants of Crueiferae from Qinghai, China. Acta Ph ...
:
,(, ,91
19971,
. h: S ft I in (editor), Fl. Qinghaiica 1: 410-10
1, , I .., I
Pu I, ',
House, Xining.
Hull, n I I'M, I .
i
I
! .-. lundslnn
,,'
Jafn,S.M.H.195o
the spec.es m N.ft
"" '
'
!l
'
itors). II WeM P ik I
:-,
,
,al reference to
II
' '''
> I
|,!
"
-'
N,, Xs I Mi It,I
tor). Flora Arctica UKSS. 7: 01-04. Leningrad.
^ ,, N & s Yliussov 1978 Ermania. Fl.

)
,
|(|MW)| S(
s
Leningrad
|u<.'tloinoVa. M. <;. ]<,7t. iMsideria. In: A. I. Vvedensky
I,.I
Cons,,,, ,. .,. \sii, \1e,liae 1 157-156
Academy of Sciences of LzSSR. Tashkent.
Pampanim. |{. |<>2(, lh-si<lr,i minibilis Pamp., gen. et
sp. nov., nuova Cmcifera an.i.nala del Caracorum | Asia
Centrale). Boll. Soc. Bot. Ital. 1926: 107-111.
. 1930. \JH flora del Caracorum. Pp. 1-290 in G.
Damelli (editor). Speditione italiana de Filippi nell
Himalaya, Caracorum et Turchestan Cinese (19131914). Ser. 2. vol. 10. Nicola Xanichclli. Bologna.
Rollins. R. C. 1993. The Crueiferae of Continental North
Schulz. (). K. 192 I. Crueiferae Siswnbrieae. In: A. Engler
;
'<lll<>r>- l>(1'11
' '
' '
"
'
' [
"' Leipzig.
"
' ' (
", ' '"
',
Berlin-I)afile.;, 9 1037 109.x

' L '
NotizbL Bo..
< n,'
,
(||
" '
'
ll
"'
" '/'''' >
^
I. m' 10:
109-111.
, , ( ||(.M.n UTM |edener
i, M IMI, ,1
, I >
II
,.M
564
_
-
1. 193] S(.lu.lle Cruciferen aus Kashmir. Repert.

,
{{ 330-334.
'J33aK.ii
\..l
.1 , neue Cattungen. Sektionen und Arten der Cniciferen. Bot. Jahrb. Svsi. (,(r.
91-102.
Sp
.33:183-191.
1933.. ,
aus Kashmir. Repert.
Spec. Nov. Regni Veg. 31: 330-334.
' ' "
"
' I ngler & K. Prantl (ed.tors) Nat Pflanzenfam., ed. 2., 17B: 227^,58. Verlag
\on \\ ilhelm Kngelmann, Leipzig.
Nislova. I. V I" 2 - - -, ,,. ,,, , ll lamib Crueifer'
I
ad) 57: 647-653.
,,,-^
WWena Pamp. in
,
,(): l60_165.
v
Wu t II. X /. V \n. 1994. Two new species of Chinese
(l,suJ,u \
II
MII \2 577-580.
. . .. /,, | \ (h, /1I1Mlko\ X s
Academy of Sciences. Leningrad.
ADAPTIVE RADIATION OF
POLLINATION MECHANISMS
IN IXIA (IRIDACEAE:
CROCOIDEAE)1
Peter Goldblatt,' Peter Bernhardt,* and

'
?
John C Mannin
ABSTRACT
representim, < \ unpl'
ii ill i
npiil.i
|i -in !i
i]
in
i tin
..ill
11 \m
,, , mi- ol ")J -p< i. -
distinct systems exploiting insects of four insect orders (Coleoptera. Diptera. Hymenoptera, and I.epidopierai l\in
bright colors contrasting with dark "beetle marks" and are pollinated exclusively by hopbine scarab beetles. Kour/vm
species with nariowb i
>
i
|
' H
I
Inn
II., robiM id lln-s | \/efii.\t()rh\iuliu\ Itniuiio-,
in,1 | u I I i
i.lil
I p. i
nil (ml In
.
in,I mod.-l neetai
volumes, appeal to !
-I I i I lh pi i in i u !. II. i
'
. I
... . ation of hopliimbeetles and tab; I
< mar I. tenuifolia) The remaining species ate
largeh pollllilttd
>
nlli | I
II
'<
|i II
in
>!
.1
nit s\st<ms Species
!
pollinated by Anlhoj-I
I
'
'
,',/n/es I i!im<i\.<i< I
have cup-shaped flowers that secrete nectar. Salver-shaped flowers of/, flexuosa secrete no nectar, but are pollinated
by pollcn-colle< luy !
II
I
u
d with vertical lloral
dehiscing incompletely from the base. Oulgmiip ,. .

n i . n .
i .
II i lion svslem in l\m is
the one in which flowers are cup-shaped, produce m-elar. in-1
ui.-il
i
:
.
- Kxaggeration
of the perianth into an elongate tul
n n ,, i, p|, nectar, or the closure of the perianth tube and absence of nectar.
or the development >l I
I i.li i
in-i bei
, I I
. ill I
m
i lated to their derived
Key words:
Apidae. Hopliini, Iridaceai
M;urocvolution ol lh.' African Iridaceai depends

in part on the plast
pollinatiot
tisms.
Nivenia (10 spp.) appears to be one of the few genera of any size in which species are pollinated primarily by two pollinator gn>ii|
I > - | >i>',- nl
flies (Nemestrinidae) or long-tongued anthophorine
bees (Goldblatt & Bernhardt, 1990). In contrast,
the larger genera of African Iridaceae are characterized by a di\
,
For
example, hipcirous
insists I spi i.-s pollinated
by long-proboscid flies, bees and butterflies combined, or moths (Goldblatt et al., 1995). Romulea
species exploit scaial
relic.11 i
,1
i i _
bees or, in one case, nemestrinid flies (Goldblatt et
al., 1998a; Manning & Goldblatt, 1996, and unpublished). The ma -
pen
l<
ippear to be pollinated primarily by nectar-feeding
anthophorine bees (Goldblatt et al., 1998b), but recent fieldwork also indicates that some red-flowered
Suppoit foi llu- in I
I.
mi
>Hi.
> un
.''
-;.<
ed by the large butterfly Aeropetes (Johnson & Bond, 1994), while ot In i -species
are dependent on andrenid bees, a combination ol
these bees and hopbine beetles (Goldblatt et al.,
|'"<<.
In. pr..h.i- nl II - iin.ih^. oi buds | a>ldblatt & Manning, 1998). The adaptive radiation of
floral characters thus appears to have played a
prominent role in evolution and speciation within
African Iridaceae.
l.xin i moderah -d/rd emis <>l Iridaceae subfamily Crocoideae Burnett, Outl. Bot.: 451 Jun.
1835. (syn. Ixioideae Klatt, 1866 as subordo
I i. i > , t , i is - - n
.1! -|, cries (Lewis, 1962;
de Vos, 1999; Goldblatt & Manning, 1999, 2000).
The genus extends from Namaqualand in the northwest of the subcontinent to Eastern Cape Province
near Grahamstown in the east, a range that coincides almost exactly with the southern African winter-rainfall zone. Species diversity is highest in the
in.,i ili
' B. A. Krukoll ( uialoi ol \t- .
GARD.
87: 564-577. 2000.
,. >i . ml I
i i if lii -i.i.
i L'lalclulK a. knowl-
ml. n, P.O. Box 299. St. Louis. M,>-,, Ml(><>.
Pollination Mechanisms i
geographical center of this zone, the Western Cape

Province. At first glance, Ixia appears to exhibit
only moderate floral diversity compared, for example, with the ca. 245 sub-Saharan African species
of Gladiolus, the 52 species of Watsonia, or the ca.
40 species of Lapeirousia. All Ixia spe iea havi
radially symmetric perianths and relatively small
flowers 1.5-3 cm in diameter, typically arranged in
a dense spike at the apex of a slender flowering
stem. The androecium is also symmetric in the majority of species, and the style diverges into three
branches near the mouth of the floral tube, at or
below the level of the anthers. On the other hand,
Ixia flowers vary remarkably in the range of perianth color and pigmentation patterning, perianth
nusual aspect of floral varmost Iridaceae are longitudinally dehiscent a

mounted on long filaments, species of Ixia sul
Dichone have short, stubby filaments and short,
thers of all but one of the nine species of this subgenus deh)tsce incompletely, and are more or less
basally poi ose in some species (Lewis, 1962).
Field stiidy of the pollination systems of a range
of Ixia species was undertaken to obtain additional
information about the evolution of adaptive mechanisms, to provide insights into the way the flowers
of Ixia species function, and to help understand the
seeming cctntradiction in apparently simple and not
particularly diverse floral morphology and a range
of quite distinct pollination systems.
Direct observations are presented on 20 Ixia species made during the years 1993 to 1999 in the
field and in living collections at Kirstenbosch Botanic Gardens, Cape Town. Observations on the
pollination biology of Ixia were made in the course
of other field research in the southern spring at
various sites (Table 1) in the southwestern Cape
and the western Karoo, South Africa, areas of Mediterranean climate with wet winters and dry summers. Observations of insect foraging involved 410 hours per plant species and included recording
of both floral attractants (pigment patterns, scent),
the mode and timing of anthesis (opening of individual buds), anther dehiscence, expansion of stigmatic lobes, the behavior of insects on the flower,
and the taxonomic diversity of floral foragers. The
range of species studied includes examples from all

infrageneric taxa (de Vos, 1999) and all the major
demic, which has long-tubed yellow flowers borne
at ground level and a subterranean ovary (Goldblatt
& Manning, 1993).
Floral scent was noted in the field and in cultivated plants. Scents too weak to be discerned by
the human nose were recorded after individual
flowers were picked and placed in clean, lidded
glass jars and stored in a warm place. The contents
of each jar were smelled after a minimum of 60
minutes (Buchmann, 1983).
$ed flowers in the field, reflecting

ion and depletion, but some spein the laboratory where no inflowers. Nectar sugar chemistry
are unlikely to be affected significantly, as opposed to sampling bagged flowers.
Ideally both bagged and unbagged flowers should
be sampled. Studies on nectar characteristics of
Lapeirousia (another southern African genus of Iridaceae-Crocoideae) suggest that n
tion is not affected using unbagge
were excluded (Goldblatt et al., 1995). Nectar volume is expected to be lower in unbagged versus
bagged flowers, but sampling of nectar of unbagged
flowers in populations being visited by pollinators
reflects a realistic situation that confronts a particular pollinator in the field. To collect nectar whole
flowers were picked and nectar was withdrawn from
the base of the perianth tube with 3 u.1 capillary
tubes after separating the ovary from the perianth
base. The percentage of sucrose equivalents in
fresh nectar was measured in the field or laboratory
on a Bellingham and Stanley hand-held refractometer (0-50%) from five or more individuals per population, unless fewer individuals were available.
Additional nectar samples were dried on Whatmans
filter paper no. 1 and sent to B.-E. van Wyk, Rand
Afrikaans University, Johannesburg, for HPLC nectar chemistry analysis.
INSECT OBSERVATION, POLLINAT1
Observations of insects on Ixia flowers included

whether insects contacted anthers and stigmas
while foraging. Insects observed probing the floral
tube or brushing the anthers or stigmas were captured and killed in a jar using ethyl acetate fumes.
Table 1.
ites and voucher information for species stud ,ed. Vouchers are housed
Mil. lull,,- , cnllrrtor-i). All study sites are in South Africa.
Specie,
H0<
Vo, tchcr
Study site
. Morpb.xu,
ldblatt & J. C. Man
L. f.
miae M. P. de Vos
Western Cape, near Darling

Western Cape, near Hot Kiver
Western Cape. I.androslkop
Western Cape, near Middelpos
Goldblatt & Mannhifi 10338

Goldblatt 10674
Oliver & Oliver 11461
Thompson 1550
Goldblatt & Nanni 11202
Burgers 1229
Goldblatt & Manning 9789
Preterms 75
Goldblatt & Manning It an
. ,' ,
I Manning I3u8
Wr^lcrn -. .ape. neat (ircvlon

Western Cape, Rondeberg
Northern Cape. Nieuwoudtville Water-

Goldblatt & Manmng 10 120
Western Cape. Mi unci's l';i->

Western Cape, Worcester district, near

Goldblatt & Manmng >><!
i. ,r, Andr.*.
Western Cape, Versveld Reserve. 1Dar-
Goldblatt & Manmng IU35H
/. flexuosa L.
1. lutea Eckl. (site 1)
(site 2)
(site 3)
Western Cape.
Western Cape,
Western Cape,
Western Cape,
Western Cape,
Western Cape,
erfontein
Western Cape,
Western Cape,
Western Cape,
Mot River
Darling Nature Res
Kland-lx-t- Kami
Piketberg
Waylands, Darling
Clanwilliam. harm Ys-
Gold hi all 10671

Goldblatt 11151
near Leipoldtville
Bainskloof
Strand
Goldblatt & Manmng 10321

Lewis 5678
Goldblatt & Manmng II Oil
Western Cape, Darling, Wavlands

Western Cape, near Caledon
Northern Cape, Bokkeveld Plateau
Scci.on //v/i.s
. IHllllillhllil \y Delarnche (Mir I
(site 2)
(site 3)
/. versicolor G. J. Lewis
c <',///.,/ .'
i' :>itni,g
'.a:-:'>
i,
\. Manning 10349
Subgenus Dichone
1. scillaris L (site 1)
(site 2)
Western Cape, Lion's Head, above
Barker 2214
Western Cape, Darling Nature Me. erve
Goldblatt U96A
Pollen was removed from

after specimens
were pinned. To prevent c
alion .1 il body
of an insect with poll
nothoi m tin
same jar, each insect was 'wrapped in tissue as soon
as it was immobilized by jar fumes. Body length
and proboscis length of insects were recorded from
captured specimens. Capturing a bee or fly at any
site appeared to reduce the insect population significantly. We therefore killed as few insects as neeessary to obtain spin. t - lot
l.nliiici m and
bodies involved gently scraping pollen off the body.

including th e scopae or corbiculae ol bees, with a
dissecting; needl e (see Goldblatt et al., 1998a, b).
! pi .1 . - tvas collected on
The residue trot I i
glass slides and mounted in 1-2 drops of Calberla's
fluid (Ogden et al., 1974). In the case of flies, which
are comparatively large insects, sites of pollen deposition are quite discrete for a particular plant visited, and pollen species can usually be identified
vvilltoul ro i-~, io nmmscopi. examination. Pol-
pollen load analysis. Removal of pollen from insect
len grains were identified microscopically by com-
parisoil
'Men grain preparations made from plants flowering at the study
sites. Ixia pollen grains are recognized by their
large size, perforate-seabrate exine. and n:< n u
cate aperlun .villi prominent ! handed operculum,
the la'ier |.-aii;r- u i(|ii> .is ;-:i' ;;> is known ((roldblatt et al., 1991).
Insect specimens were identified by R. W.
II -, ( \fiidae|. I ni\et>it\ ;l Kansas, H. Dombrow, Worms, Germany (Scarabaeidae), and J. C.
Manning (Diptera, Lepidoptera). Voucher specimens are deposited at the Natal Museum, Pietermaritzburg, South Africa, or the Snow Entomological Museum, [,awn-nee. Kansas
Flunil phenology and life spoil. Speeie-.nl !\:<,

n
i
i I
n I i i
hytes of small to
ii
i
i
111 v 15-40 cm high (Fig. 1).
Individual i
u
- i . 1<
i-upl< or branched
flowering stem annually, and flowering i - lose]
synchronized in a population. Inflorescences are
spikes with helically arranged flowers (Lewis,
1962). With a few exceptions, flowering occurs in
late winter and spring (August to October) (Table
2). This coincides with the period of optimal plant
growth, during or soon after the main raim season
The pattern of flower buds opening on an inflorescence is acropetal. In all species a mature bud
. inds in the early to late morning, and the open
flower typically lasts three or four days. Flowers
open sequentially, usually one day apart, hence
there are often three or four flowers open at any
time on an inflorescence. At sunset the tepals
loosely close to enfold the anthers and stigmas. Tepals unfold again the next day, between 08.00 and
12.00 hours, depending on species and to some ex
tent on ambient temperature. On cold (< 15C) c
overcast days they may unfold partially or not i
all.
Flowers of all species studied show weak mechanical protandry. In most species the anthers deh
longitudinally within one to four hours af
the tepals first unfold (Fig. 2A, B, C). In these SJ
i of Ixia species arrange.I .. -.>i.lui- I ibucr l\pe. f = presence, - = absence.

Lire volumetrically. Conventional perianlli lubes are cylindrical and hollow (indicate
\ug.-Sep.
. latifolia
yeUov
'. rapunculoides
/. mriclcikumpiac
starting from the base (Fig. 2D). Pollen in these

species is not shed but remains within the anthers
unless actively removed by an insect. The time of
bient temperature anil humidity, and anthers dehisce later in wet cool conditions. The three stylar
lobes, the distal ada\ial surfaces of which ompris.
the stigmas, are held together when the flower first
opens, but they diverge later during the same day.
We did not determine
ity ourselves, but Horn (1962) i
of species are self-. < IU| utlbl. . Uichidinu Ixitt :,
ill,iht and / jioiiSltii ';./. which w. re ~imii< I here.
but have reduced fruit and seed production when
selfed by hand compared with xenogamous crosses.
Horn also reported that /. odorata was sclf-incompatible. Mechaui. al selling is restricted in Ixiti sell
huts by the spatial reparation of anther- and s|ig
Floral presentation and
Open flow
ers are typically held erect to subercct in a burly

congested spike I i
Iiflora (sect. Mor--" "tudied here, has elongate, lax spikes,
while
wnue species of subgenus Dichone have comparatively sturdy stems and flowers held h
I I
and relatively widely spaced on the spiki axis, (xia
odorata is one of two species examined that produces an odor, and the flowers have a sweet scent
reminiscent of coiiinier, lal cullivais ol i ,'.-./</ <>,!<:ata. In the other scented species, /. flexuosa, the
flowers have a sour, acrid, n u4
> 1< l unpl< i u
Floral presentation (including shape, pigmenta
tion, attractants, and rewards
ij
! IntofoUi
main categories (Table 2), although the basic perianlh plan i- alwa\ s svuinietii. al anil a. tin uiioipliii
The first category, of WHICH /. mujuuu aim i. tapunculoides (seel \h;>hi\tu) an typical examples,
have cup- or salver-shaped flowers (Fig. 3). The
;
i
I ' e is funnel-shaped with a hollo-. ,
ylindric basal half and a flared upper half, this
ranging from fairly wide and 7-10 mi

mouth. The cylindrical part of the 1
the flared portion. The stamens are
. "/ // i
> i >, ti >;, '
nli miil
n li I
(li-tiiscinj! from tlin I
and located around the center of the flower and

either within the wide part of the floral tube or are
shortly to fully exserted. Anthers are extrorse with
loculicidal dehiscence, and the pollen adheres to
the dehisced anther locules (Lewis, 1962). The
\ MH*
":%
-*.>
..
'
>J
13
I4
S*\. If7*>
^
'"#'1t -4%3
J
style is central in .ill -|

in
h nl< - i >n ill
into three lobes tk> end i I i n the filaments
or the lower half of the anthers, depending on the
level at which the style divides. Perianth coloration
in flowers of this group is usually pink to mauve or
blue but may somel
ik or magenta
in forms of /. latifolia. The fragrant flowers of /.
odorata are yellow ami a n i ul
i i I r 1 r
<l
ed together, collectively forming the prominent signal to pollinators. Ixia aurea and /. tenuifolia are
exceptional anions. 1'n- -|
- w ill lula.lai ll-u. i 1
_
la
I
in the latter with a dark reddish center.
A second flower category is exemplified by Ixia
/miici folia (Fig. 1) and /. fumiculata (Figs. 2C, 4)
and is found in all
,
j i
2). The floral tube is hollow, cylindric, much exceeds the tepals. and has a narrow diameter ca.
1.5-2 mm wide. The style and stamens are ecutrally placed. The anthers may be included in the
luhe {I. panictilata) or. more commonly, are exsert1 :/
I
ianth color in
these tubular flowers is white, cream, or pink,
sometimes more darkly pigmented around the
throat. All the tubular flowers are unscented.
In the third flora
i
i il
|i\ l\ia ma
(ii/ala (sect. /via), tin perianth h-nns a broad. Hal
salver. I\pieall\ 2i diamei
ils
extended horizontal
i lli
[
ifilil
n lima
lube iFig. 2B. />>. I'l
and completely filled by the style and closed off at the mouth by
coherent or coalescent filaments, contains no neetar, and functions as a pedicel, supporting the tepals and stamens. The perianth color is remarkably
diverse among species of this group, ranging from
white or cream to pink or mauve, or dark red, purpie, turquoise, or il
I
i How. but flowers are usual I \ I
central marking, >ot,
'
mmils
and occasionally the anthers, i.e., beetle marks sensu Goldblatt et al. (1998a). Other authors (Steiner,
1998a, b) have restricted the term beetle mark to
describe markings that more closely resemble a
beetle, but our broa
II ie
longitudinally dehiscent anthers are centrally
placed and the poll I
nil
.,',.:
! .
mi ,-ually small flowers
lor this group, ca. 1.5 mm in diameter, and they
are fragrant and borne on particularly slender, wiry
peduncles. Its crowded inflorescences tend to droop
and wave in the wind, unlike the erect spikes of
other species in the group.
The last floral category, represented by Ixia scil,
il _ I lneled to species of subgenus
Ihrimnr (Lewis. I(>()2). The perianth is salvershaped and pale to deep pink, often darker pink
h.v.aid I|I.- - -1 - - .-I ill. ||..-.M I I he flowers are se.
uted. The perianth
tube is filiform with the tube wall enveloping the
style in a tight, continuous sheath. The tube contains no detectable nectar. The stamens are fully
;
,
on short, somewhat
stubby filaments. The anthers are 3-4 mm long,
IISI llv as lout
I
il m
-. and inflated and
ha
I
I >< luseenee is delayed and begins
from the base and does not reach the anther apices
(I ig _I ';. Ii
i
11 lit is are more or less
unilateral, and lie slightly below horizontal, perhaps due only to gravity. Pollen is retained within
anther locules and not exposed as it is in anthers
of most other l id i ae I b< anthers have been described as subdidvmous Lewis. I(>(>2> imlii itmg
dial lhe\ hav viilua Ik n. connective tissue,
We were unable to include Ixia acaulis in the
i
i d flu speeies ma\ represent an additional
floral category. Plants are unique in the genus in
being acaulescent, and the long-tubed, yellow flowers are borne at ground level with the ovary held
below ground (Goldblatt & Manning, 1993). Ineluded in section Hyalis by de Vos (1999), /. acaulis is unlikely to be pollinated by the long-proboscid Hies that visit other species in the section for
the floi
NK.CTAR
PROFILE
Nectar, when present (Table 2), is produced in

septal nectaries in Ixia species, as in the entire
subfamily Crocoideae (Goldblatt, 1990a, 1991).
Nectar is secreted from minute, circular pores at
the top of the ovary, flowing directly into the base
of the perianth lube, and is typically retained in
tube. 4 (top right). /. paniculata. with |>aleit darker, eenlral markings and large anthers. la (bottom right I. I\i,i
I on the >|iikes. and nodding anthers.
Table 3. isleelar properties of selected Ixia flowers. Fru = fn ictose. (Jlu = glucose, Sue = sucrose. Nectar sugars
in 1
.
i il -ludv -in
analyzed by B .-F. van Wyk. Sample size indicates number of flov vers(ofdifi . i HI
%(
Nectar
Specie.
Sample
size
volume
uj (n)
% sugar
(SD)
Fru
1.7-2.9
0.4-1.3
1.1-1.6
3.9-5.7
1.1-1.5
27.6(2.5)
38.5(3.6)
29.8(1.8)
26.1(2.7)
28.0(1.0)
17-21
16-19
27-28
. inrlclcrkaiiipiiii
f different sugars
Mean Suc/Glu
20-25
17-23
29-37
54-63
58-66
35-44
h\a. I. scillaris: tubes f
the loner pari <>l the I ib. III. length ol die |.er
anth tube varies among the Ixia species liable 2)
i:
examined, ranging from 4 mm in /. scillai
mm in /. paniculala. In species with
fiinnel
shaped lube, the lower, slender part is mostly 4-8
mm long. Nectai i- present in (lowers of groups 1
and 2 but is nut produced in ihe /,,<( -.<-,, >./.,/,,
fly, Prosoeca sp. in

il \2 mm I
i .
for nectar on /.
I
K
i
i ,
, i it- latsi while continuing to
vibrate its wings.
Among the species of category 1, those with a
i ii >.-, upp, ; Hoial Inn.' iu. i- ,1 dllielellt range ol
itiseel usiiors. /,-;, iirtmhilo c- visit, d b\ the but-
group or in subgenus Dichone. Nectar volumes are

mostly 1.5-3 u,l,
and rarely exceed 5 u,l (Table 3). In the long-tubed
/
.
' - i;i<>np nectai si-in lion ranges from
1.1-1.6 u,l (in /. paucifolia) to 3.9-5.7 u.1 (in /.
paniculata). The nectar is sucrose-rich to sunns. dominant with -i
. u
ig up 25-35% of
the total volume of fluid (Table 3).
terfly Colias electo (Pieriidae). This insect lands on

the tepals and its head contacts anthers and stigma
lobes while il extends its proboscis into the floral
tube. The small-flowered and short-tubed Ixia or,. ni:ii:> ha- a p.i: I i.ul.,1 b i:a:i >u lloral lube, and il
appears to be visited only by ibis insect.
Ixia aurea and /. tenuifolia are visited by a combination of sborl-prnb..s. . ! : ibanid Hies. \h>sum\ia
11 ibo-i i- 3-5 mm
long), respectively, and hopbine beeiles (Scara-
MKCIIANISMS,
Pollination strategies vary among Ixia species

ami largely coi idale .\ ilh I hi- mod. oi II. ral : i<
seiilalion. Tb< re .i[.p. ai - l. be a convl ilion I! l
i rat. gory 1 and the
width oi the II; i
| i
i I
11 uith lube Species with a wide, cup-shaped upper lube are pollinated pninaiiK In Ieinale \n!h(>i>iu,t,i ,lire:s;<s,
a large bee (body I 1 17 mm long) with a relatively
long proboscis, 6.5-8 mm long (Goldblatt et al.,
1998b). These bees land on the flower and brush
both the anthers and stigma lobes as limy push
theii he ids ml . tb. Il..r il up. \'h'h<>!>h<>>>t (:. <-,->.
pes is a polvlei ii
individuals were found to carry the pollen of coblooming Fabacca.-. S.ihm sp. I Famiaceae). IA>I>I>S
I
I
II eae (including
Hesperantha, Moraea) in their scopae.
One bee, captured on / hililoliu. cairn d din e ;;;.!
linai ; i ol '\ihn'itti Inimiir I mill |< belli :,x < aei oi
its Iron- We have al-.. captured the nemestrinid
baeidae) (Table 5), while P. atricornis alone was

i apmied on / %/.,"'..;, .<;;>,!, I h. I.iii an : ill. - lot
aged for nectar on, and carried mixed load- of pollen of, Ixia, On
".. la. i] ill\
aciiilhaeeac). and Asteraceae. Beetles ignored the
lie. tar m the 11,.- I I I , |. . ii
. lusbi l\ on pollen, and contacted both dehisced anthers and stigma lob. - ulul. lot ii.mi. > >|>ul.ilinv oi < im mini m
agonislie behavior (see Goldblatt et al., 1998a).
These beeiles also carried mixed loads <>l Ixia, Or
n I'.oih ih.s.I
I labamd lb. - aid tin hopliim b. .
lli i-airii
p..II.-n II In lors.il id ventral parts
of then bodies as well as the frons. Poll.n ..1 I\ia
sal part of the thorax in the tabanids, reflecting
Ixia flowers.
Tubular flowers (category 2) were visited by longprobos. id Hies, eilher \eiuesinnidai m Tabaiudae.
with probosces between 18 and 70 mm long liable
Volume 87, Number 4

2000
Table 4.
Compai
I-,:>H
Goldblatt et al.
Pollination Mechanisms in Ixia
.i tin- b-ngi'n of pn i.ini h ail.,-
the range- found by sampling flowers of 10 inoi\ idualI'ol ltl-t i 1- onlv tin
IN
i Ii il
I
.II
1 r .
Table 5. Pollen load analvsis of captured inserts on Ixia

species. Scarabacidae: Anisocheliis, Chasme. HeWrochelus.
/.;".,.. 1,,:;, !><;,>,,:,;, !', !,ln, !;, S ,/-.,,.'.,. . \|;
id.-a: Apiil.n !,
s l\u hsmelus. Mel1
Peri.inlh
573
IN
1 i
1',
Jin ti to ih. in-., t-
I'lohos-
Plant
length
length
LpanicuUua
65-75
67-70
/.,,<:/,/,.,
.',() :{2
16-28
22-24
18-22
Insect species
Number of
insect raiTM.i;
...,ll,-n lu.-.dl-l
"Ejsr*"
Philoliche gulosa
P. gulosa
ll. These flics -rasp the tepals with their tarsi and
. hi 1c continuing to vibrate their
II _- hi: l . .i )
and species of several genera of Iridaceac (including llii>;u:>,s, <;<',i,h,>/,!<. î^,i;hi:,l. .aid I <>;:;,> .
sin species). One specimen of Moegistm/.'./,.<';.also carried one pollinarium of Z)a draconis (L. f.)
S
(Oi hidaceae), also a member of the guild of
plant species that depend on this particul ir il\
i
pollen dispersal (Manning & Goldblatt, 1997; Johnson & Steiner, 1997).
blowers :i| category '-, so. lion i\i,i (with a s.dvrrshaped p
| ,- ( \i>, v ..../,'.<,,-./ ( (,,,.i v iti,,,. i,l |i..|l. n load
analyses oj bet-tics raptured on spc irs of ill* Ixia
maculata group show unust
behavior, visiting flowers of a range of species including other Iridaceae (e.g., Gladiolus, Moraea,
Romulea), Asteraceae, Monsonia (Geraniaceae),
Prismatocarpus pedunculatus (P. J. Bergius) A. DC.
(Campanulaceae), Spiloxene capensis (L.) Garside
(Hvpoxidaoeae). and Oniilhogaliim spp. V\'hcn -\;>is
mellifera visited /. flexuosa it contacted the stigniaii. lobes whili scraping anthers for pollen. Captured individuals of Apis mellifera carried pure
Ii i
4 Ixia | < I- n i hei 1 < lies and in their
corbiculae (Table 5).
\
ii - II
i
I' unskloof, we noted a possible example of Batesian mimi n (\, > '< ' in
pun: winch has pale mauve flowers with a darker
central area, and co-blooming Therriatilhus ixioides
G. J. Lewis (alsi Ir dae ,< . t\ith ,\hitisl flow, is
also with purple markings in the rrnln, rlosrh re-
Siilêmis Ixia: Section Morphixia

| Heterorhelus arthriticus ]
[Lepithrix ornatella]
\Mesonivin edentiiln]
'. capillaris
[Anlhophora diversipes 9 ]
[Philoliche atricornis)
f, latifolia 1
[Anthophora diversipes 9 ]
popln 2
[Pachymelus peringueyi
Section HyalLs
scinble nut' anotht i as icgaids floral pros, illation.

and they appear to he visited indist i imnialch In
the same beetle /'
'
I >!li sp. . i< s have
a lililorm floral luhe in which ihe slvle is tightb
enclosed by the walls of the tube. In T. ixioides
ii i I n i i 11
i ii
i MI
I i.| mil are visible at the mouth of the tube. This suggests that
the species may offer a secondary reward ami ma\
have a more gei
n ^-lem ihan /.
mtirlcrhttnipiac, wliich does not offer nectar.
Category 4 flowers of subgenus Dichnne (with secund. saker-shaped llowers and basalb diliisc.nl
aiilhersi appear to I>c pollinated In female Amegilla
I \pidaci. These bees have bodies 10-12 mm long,
thus smaller ilia
I
,'i:\ip<:s, although
they also have an elongated proboscis M.oldhlall et
al., 1998b). These bees cling to the anthers of Ixia
s ,':!!,< v, full- I..(aging > \cl l-l\. U lor pollen. I'ollen removal is accomplished In thoracic vibration
in winch lli. I i i I i
i
i
i . - tin ( har.K
teristic high-pilchcd whin, (s.iisii Buchmann,
1983). A bee did not remain on an indi\ id i fl , i
of /. sail,,ris tor longer than I ..> seconds. The head
of a bee appeared to contact one ol the three extended slvlai lob.s while ii grasped the anthers.
rollen load anaKscs ol \mcgilla captured on /. scillaris (Table 5) showed that the bees also foraged on
II i i i i
I
i - . I
i I ab it . .ir\ and
Mimilliti (Polvgalaeeae). An interesting aspect of
the pollination of /. saltans is that although the
anlheis arc promineiitb displa\e.l and evidently attractive to bees other than Amegilla, the melittid.
mi(ita, as well dsAndrena sp. and Colletes
sp. seen visiting (lowers and clasping tin anlhers.
tilt I not carry pollen ol I he spot aes. This is v idenlK
a reflection of these bees' inability lo vibrate then
wings at the necessary frequency to dislodge pollen
from the anthers.
I al on n >|ri:h tie -.cub. <l n !,,;>< >;<>a.^,i H ioldl i;ill

et al., 1995), Moraea (Goldblatt et al., 1989; Goldblatt & Bernhardt, 1999), and Gladiolus (Goldblatt
& Manning, 1998; Goldblatt et al., 199hl. Specifically, pollination systems in moderate lo largesized genera ol Iridaecae in Mrica diveige as different species in the same genus exploit different
pollen vectors. Lapeirousia (Goldblatt, 1990b;
Goldblatt & Manning, 1992) has specialized species that utilize long-proboscid Tabanidae. \emestrinidae, or sphinx moths, as well as species wilh
gencialisl systems that include various long-
toilglied lie,-:-,. bee files ( Bollll) vll i( Lie i. alld blitier

flies. Pollination in the much larger genus Gladiolus. Willi -nine 2 11 s ih-Siharan Uncail species, is
dominated |>v long-tongued anthophonne [sees. Im!
po'lei lim !>\
.11^ i t'n - nl \ mt'strinidae and
Tabamda. . l)n laiia bnitiith \>i,>, . ,'/v .'..'',,v ;,,
night 11 v in mi.lh-. and -nnlii:d- ! \ .'-. , ;/ -|.p !
has also been observed in several species. Moraea
speeies appear to be pollinated primarily by bees
nl i i i gated or extended mouth parts (Goldb l
et al., 1989). However, recent work by Steiner
(1998a) and Goldblatt et al. (1998a) shows that several southwestern Cape species are }>ollii aled
hopbine beelle-. wild.- i.tln I ~pe. ie- .ill | " >l 11 M.il. d
only by pollen-collecting bees, or a combination of
bees, mil- id and -e.il L iphaud iln -. and ii tphme
beetles (Goldblatt & Bernhardt, 1999). Like these
other genera of the Indue, ae. /w,/ also has species
adapted to a range of pollination systems. The flowet- .it l\l.i -peel. - tlni- -how dllleiciil -e|- ol i or
related morphof..
HI- that represent
< o-adaptalimi- with dilt.-ieut lloi.il |..iaL--~
Pollination by hopliine beetles in Ixia parallels
II
r
,
,
! oilier genera of
the Iridaceae. As in Monica insi U res Gi Ibla
cf. lurida Ker-Gawl., M. tulbaghensis L. Bolus, and
M. villosa (Ker-Gawl.) Ker-Gawl. (Goldblatt et al.,
1998a; Steiner, 1998a), the flowers of the Ixia maoup have darkened floral markings and
large areas of flat surface, brightly colored pollen,
and little or no nectar. Pollination by lieetar-lorajiiiiLi intli phorin b - in some species ot l\m
parallels thai in Uarara in< linata. ri.anv fJ,;,-!;.>hr
specie-, and !<:[>< ,!<>i,s>a ,.'; </'.. ala Y K. Hi. |(,oldblatt et al., 1989, 1995, 1998b). These Ixia species
also have Mowers broad enough In ::('<; a la:i;:mi
plailonn. piLiia nla'pui pall, ri.- mo-llv in the pink
i . ..1 n i ,i g<
IIK ( i -pi no I- stamens, and nectar
retained at the base of a floral tube.
The adaptive
lination mechanisms in Ixia. huvv.-ver. appears [ess diverse ihan
in Lapeirousia or (,
\
ei moth nor bird
pollination appears to occur in the genus. While
!
icill ih>llII |..;i i
i
iib.-d here in Ixia, I.
oricnlaiis is delinilek not pari ol die southern African red-flowered, -uminei -blooming \fn>pc>rs
butterfly guild described by Johnson and Bond
(1994).
Th.- unique feature of pollination ssstem- in /wo
is represented b\ I ll ui.u-nal bn '/ p llui iln II - . tern in subgenus Dichone. In other genera of Iridaceae in southern Africa there is a divergence be
liolus are nectariferous, and large antho:s forage on gullet- or flan-shaped flowers
(sensu Faegri & van der Pijl, 1979). Gladiolus
ilus (L). Delaroche) Barnard and G. stellatus G. J. Lewis have stellate flowers, and Andrena
>|. (ii l/i.'s ii,,-!;,;, i - up. pollen Inuii pn nan. nl.
exserted anthers (Goldblatt et al., 1998b). A similar
divergence is also found in bee-pollinated species
of Moraea (Goldblatt & Bernhardt, 1999).
The genus Ixia actually exhibits three different
modes of bee pollination. The nectar-bearing tube
and cup-shaped Moral system ol seel ion \hir;>inxia
ii
be] >llen-rich, nectarless, salver-shaped Hoi a
system of /. flexuosa parallel systems described in
Gladiolus (Goldblatt et al., 1998b). However, buzz
Mn
I !' -' ' I
i -I - 1 i- l>: tunic hanoi
been observed in any otber genus of the Iridaceae
to date. Harris
I
porose or porate
anthers are found in the Iridaceae, but Buchmann
(1983) did not mention buzz-pollinated flowers in
the fainiK in bis review of the subject. Buchmann
showed how varied pore position may be on a solitary anther but did not mention basal pores or basal dehiscence. Buzz pollination in subgenus Dichone has evolved independently, adding another
example to the widespread convergence within the
been reported within the petaloid monocots in Cyanella (TecophilaeaceaeDulberger & Ornduff,
1980), Echeandia (AnthericaceaeBernhardt &
Montalvo, 1979), Dianella (Hemerocallidaceae
Bernhardt, 1995), Dichopogon (Lomandraceae
Bernhardt & Burns-Balogh, 1986; see Bernhardt,
1996, fig. 3), and Xiphidium (Haemodoraceae
Buclimaun. 1980). In these taxa hlamenls are relatively short and anthers are inflated. Buzz-pollinated species of Ixia, however, have one unusual
character found only in a few buzz-pollinaled an
giosperms such as the Australian Caleclcsia :|>a
sypogonaceae) and Hibbertia (Dilleniaceae). In
ihese last two la\a lli. -f\ lar lobes div rge. lormim
a triangular perimeter outside the centrally placed
anthers (Bernhardt, 1986). We presume that this
alignment of sexual organs may encourage cross
pollination, as a bee should contact stigmatic surfaces before it vibrates the anthers.
Flowers of Ixia flexuosa appear to represent a
secondary shift to bee pollination within the predominantly beetl,
Mn
.ii Ixia. The flowers have the mm
ine beetle-pollinated species of the section, but the
flowers are relatively small, ca. 15 mm in diameter,
s pink) and without .1 prominent central mail. features not :i nmallv a-soeiated with ho
pliine pollination (Picker & Midgley, 1996; Sterner.
1998b; Goldblatt et al., 1998b). The entire inflorescence ol'ti li ih'oi p- III!
es a! out ill tin wind
on .1 slender peduncle, making the flowers poor
to oiler polle,
o foraging bees. Api-.

i
which we have seen actively colled nig pollei )n the species. The corbiculae of
liee> -aj lured on / /.'Vwmsu , ..nlamed [)i;re load.of l\i,i pollen.
Outgroup comparison with the genera most
eloseh Hied |o /',.-,/. .S/i./x/.t ;\. illd Trit'mit) (I cWls.
I W>2:'Goldblatt et al., 2000), suggests that the anwhii i ll mm- are ip -Taped, produce nectar, and
.is. pollinated h\ hu-. 11 tli .] h 'line bees. This is
the ple-milioiphie pollination sil l|eg\ 111 SliiHd >..<>
and Tritonia aeeording to current views on the evolution of these genera. In both genera a zygomorplne. hil 11.1 il> llms.-i dial pt iduees nectar is believed to be ancestral, as it probably is for the
entire subfamily Ixioiodeae (Goldblatt, 2000). All
Ixia species hav. . ladialK -s IUI:i< trie- perianth, a
maioi s\napomorpli\ lot llie melius, blowers ol species nt section- \!,,);>h, 11,i 11 d //).//(> stil] pr.idu-
nectar in a hollow |.i-r i.inili lube. Spe. mli/ation loi
[1
I wo major direeAn emphasis on nectar as the sole reward ac. ompaim d b\ an e|..m ilmn . I ihe lloi.d lube haoccurred in species ol section llyalis and is the
only system known to be utilized by any species of
the seolion. This pollination system .- tnosl lugl h
developed in Ixia paniculata, which has a floral
lube up lo '...I 7fp 11 in Ion- and is the onU specieol the section visited b\ M L
> ,
rostris. Other member- ol ihe section uliliz. shorlm
pi ob .- id Tabauid.ii In n. ilh. : t"h i.imi! \ 1- p.o I- 11
. [ -uuied. an : ai [her- l /, /m/m uinln are aclualb
com aled wilhu llic Moral lulu . a n ode il preseii
tation also found in /. fucata Ker-Gawl. (Lewis,
IDOL'S. 011 which w. lia\ e no! captured . 111 s insects.
A second din
<
1
has been the reduolii 1 >1 ihe p. liarilh lube in widlh
He. ll. polbMalii.il 1- a -tialc^ adopted by many

-oat hi in Mm an i eta Ion I geoph\|es. as well as annual and perennial Asteraceae, and is known 11 ihe
Iridaceae in.tm'
\! .
,,
(Sweet) Goldblatt, and Romulea (Gnldhlatl K Manning, 1996; Steiner, 1998a; Goldblatt et al., 1998a,
2000). Pollination by hopliine beetles also occurs
in other genera, either alone or in combination with
other insects, usually nectarivorous, shmi i !.. id Tabaimlae (e.g.. -pen.-, nl Sjianni.s) or with
pollen-collecting female halictid and andrenid bees
and 1/.', t),<'!,<.;! (< v. spe. 11 - ! A'"'",.''../ <!!,!
iolus meliusculus (G. J. Lewis) Goldblatt & J. C.
"d mi 11 . llopli in b. (1. 1 Ilin 'don. however, appeal- In b. paitioul ills well d. \ clope.l in l\id seel.
Ixia, a taxon that appears to comprise a .lade defined by the moip m
...
lion- a., laled
with the pollination system. These include the reduelion in the diaineler ol the perianth tube, which
is filiform and tightly sheaths the style, and the
closure of the apex of the tul
hi
I ha-.
hi
ainenls. inserted al ihe ba-e .! lh< top .1- ami Ten
mill. .1 below 01 .'ii'.(. I\ N< -lai production is also
suppressed, and the floral tube, a plesiomorphic
structure in bid
1
i| 11
1 1
1 I
functions as a slalk lot tin pelaloul. S.IIM I -ha| ed
part of the flowers. Additional adaptation- include
the dev. lop.menl ol hrighl Moral pmm. nlalioi . 111.-I
ly orange, yellow, red, or purple, ollen with dark
centers that appear to represent beetle marks, a
.million I. al u< ol be.-lie li .w< : - I'ick. : A Midi
ley, 1996). Ixia aurea and /. It-niiifnlia (sect. \Un
oil
1. ina kable example within the geII...th sp. cms lia; c a narrow l\ iuntiel -hap. d Moial
tube that contain- m . l,m. bu: lh. Moral pimm-nlation is like that ol specie- of section Ixia, being
deep yellow to orange, and with a dark center in /.
They are pollinated by a combination ol
inphine : cellos and ill. lab mid Hie- i/momim .-/
lid /'
I bis s\stem 0II1 rs
.1 sinking parall. I Willi ihe bi . lb pol in ilim -\tem in Sparaxis species (Goldblatt et al., 1998b,
20i.Mi| 111 which small am.omils ..I neelai are also
While there are far fewer species in Ixia complied lo 6/m/'.../N .aid \],'an;). I- >111 ri. 111 .11 -\-len.ol Ixin are relatively diverse The dhersih of pol-
seclion l\i,i aiupl. :> >ll. n 1- po|u, ,,| |,\ I. imilu

Mowers primarily
appear lo constitute -am- toi the asseinbb ami ma!
ing of species of hopliine beetles. While these beetime on flowers either crawling over the perianth or
changes in floral characters based on changes in

pi a
...1 the presence or absence of nectar,
Moral lub. . ami 11
i 1 I'
It In- . nee. \\ ith
the exception of the mode of anther dehiscence, all
other floral modifications in Ixia parallel those
!
foul d m albe : genera " 'I < famih
Volume 87, Number'
literature Cited
"'"''""I1-. ''
, R Bernhardt & J. C. Manning. 1989. No
"'';,,
|:
'
,l>" '" "'""
""
' '
<.,,',,
/ato (Dilleniaceae). PI. Syst. Evol. 152:231-241.

. IOT, p,
,
,
11
, ,
<)
-2()- ,
'
. 1996. \nili,
tnal pollination
220 m W.G. D'Arcy&R^C Keating (editors).
UnivPress cZhriZ' Fm.hn.l
"'""
(:ambrid e
family
96l
if/,//
,,',,,',
il ill i
I1 .
in in n
I i HI.
!<!.('
> i
In
-: llaeinudoraceae) i
. 53: 685-699.
983 Ii,,// polbnation in angiosperms Pp 73i
.,!
n
,1
i I
.,
r,.
-i
.1
I..',
,,,, ,,,, |..
Mi.>nri
p ,.,,,,,,,
JI
>n,
Mot. Card. 78:

m~
[>()|||natm|
:.i:V.:;i.
71.
-
&
\.m.
ogy of Lapeirousia subgenus Wrou,m (Iridi,
-&RBun,s
.
II
mimesis in 77.*/vmi/rri. PI. Svst. Kvol. 151:97-101.
& E. A. Montalvo. 1979. The pollination ecology
in 'mi inn
,l,,d ., . .F
V1 .. ^
Kmi.l.-...-.
< I.
II
New York.
Dulbergei. K. & R. Ornduff. 1980. Floral mor|)holog> and
philaeaeeae). \e\\ Phvtol. 86: 445-456.
Faegn. K. & L van der Pijl. 1979. The Principles of
I
.' I
I
Africa. Ann. Missouri Bot. Card. 85: 492-517.

. P. Bernhardt & J. C. Manning. 1998b. Pollination
|.\ monkej beetles (Scarabae da Ho i
pel oi I
geophyt ii south* rn Vfi ca. Inn. Missouri Bo I *rd
_ _,
c Manni
& p Bernhardt. 2000. Adaptive
n
...
.,
v
n
\
' ';tl o'HI'nation *>.. m- ,n S,,,,,,, us ke, . . ,ule,
ra ,
(Iridaceae: Ixioideae). Adansonia sex. 3, 22: 57-70.

uris, J. A. 1905. The Dehiscence of Anthers by Apical
Pores. I'll.I) Dissertation. Washington I mvcsilv. Si.
h U . a, ,.,.
I
.
f ^.'"S êsea.rc',, " S"'" ' Vln''"'
|'
",:' -.lin.e.spMiuM.mpat.lMbtvm/^
I . y,,,ws Ker. */,,,, Mand Zantedescfua
Spreng. J. S. African Bot. 28: 269-277.
Wôn. S- W. J. Bond 11 Red flowers and butteHlyponu^tmnmthefynbosoSonthAnca.. ,..,-
-. 1991. An overview of the systematic*, phvlogenv
îmal Interactions in Mediterranean-Type Ecosystems.
" lÔb "N:

Ixioidcac) , tio,,
/.,
'
77-430-484
and biologv
,. .,
n j
Mor n
1 -
I,,,N
148 m M.
,1
n.
ill
|_74
in
Iridaceae. ( onlr.
-. 2000. Phvlogenv of the Iridaceae and the relationships of Iris. Ann. Bot. (Roma) 46: 1-16.
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biologv of \compatibility Israel J. Bot. 39: 93-111.
(Iridaceae) uilh a -
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tion and
solution of floral spur length in the Disa dracoms

complex. Kvolution 51: 45-53.
'<ls- (" ' l962- South Afr,can Indaceae. The genus
Ixm. I. S. African Bot. 28: 45-195.
Manning. J. (.. K P. <,oldblall. I9<X,. I'he I'rosnrra ,H;
& J. C. Manning. 1992. SvMemalics of the southern African Lapeirousia corymbosa (Iridaceae: Ixioideae) complex (sect. Faslifrinh,) and a ncu species of
sect. I'anindatu. S. African J. Bot. 58: 326-336.
&
. 1993. Ixia acaulis, a new acaulescent
species of Iridaceae: Ixioideae from the Knersvlakle.
\ama,|,ialand. Soulh UYiea. Won 3: 148-153.
&
. 1996. Aristeas and beetle pollination.
Veld & Flora 82: 17-19.
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. 1998. Gladiolus in Southern Africa.
Fernwood Press, Cape Town.
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. 1999. New species of Spam.xis and
Aria (Iridaceae: Ixioideae) from Western Cape. Soulh
"' anthem Africa: Long-tongued flies and their tubular

n Mi
&
1997. The Uorpstorhynchus lon^m,,
"'* (Diplera: Vmestnmdac) pollination guild: Longtubed (lowers and a specialized long-tongued fly-pollination system in southern Africa. PI. Syst. Evol. 206:
51-69.
Ogdem K. C. (,. S. Bavnor. J. V. Havers & D. M. I^wis.
1974. Manual of Sampling Airborne Pollen. Hafner
Press. London.
Picker. M. I). & J. J. Midglev. 1999. Pollination l.\ monkey beetles (Coleoptera: Scarabaeidae: Hopliini): Flower and color preferences. African Fntomol. 4: 7-14.
Neiii.-r. k S. 199,';., Beetle pollination of peacock moraeas in South \ln. ... PI. Svst. Iv.,1. 209: 47-65.
Bothalia 29: 59-63.

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the vascular plants of the Cape region of South Africa.
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South African orchid. \mer. J. Bot. 85: 1180-1193.

\os. VI. P. dc 1999. I.ua. Pp. 1-87
(editor). Flora of Southern Africa, v
2 Ixioideae. fasc. 1. National Bota
: 47-56.
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ANNALS OF THE
MISSOURI BOTANICAL GARDEN
VOLUME 87
.' \ml.i-r (.loss. Tins is .in aiiil-iiir
|..I|M-I
drsinnr.l I.
\ hY
AL-SHEHBAZ, IHSAN A. (See Marcus Koch & Ihsan A. Al-Shehbaz)

ALVERSON, WILLIAM S. (See Michael J. Donoghue & William S. Alverson) .
BASKIN, CAROL C. (See Jerry M. Baskin & Carol C. Baskin)
M. & CAROL C. BASKIN. Vegetation of Limestone and Dolomite
Glades in the Ozarks and Midwesl Regions of the United States
BASKIN, JERRY
(See Ghillean T. Prance, Henk Beentje, John Dransfield &

Robert Johns)
BEENTJE, HENK.
(See Leonardo Galetto, Gabriel Bernardello, Irene C. Isele,

Jose Vesprini, Gabriela Speroni & Alfredo Berduc)
BERDUC, ALFREDO.
(See Leonardo Galetto, Gabriel Bernardello, Irene C.

Isele, Jos6 Vesprini, C.ibm-hi Sprioni <S \lir< lo Itrnh,
BERNARDELLO, GARRIEL.
(See Peter Goldblatt, Peter Bernhardt & John C. Man-
BERNHARDT, PETER.
IY, PALL
E. Book Review. Flora da Reserva Ducke by J. S. da S. Ribeiro
cs, BARBARA. What is Significantthe Wollemi Pine or the Southern

JCA, RICHARD
C. Unraveling the History of Arthropod Biodiversification

13
CARLQUIST, SHERWIN. Wood and Bark Anatomy of Takhtajania (Winteraceae);

I'lnloornHi, n 1 Kmlogi< il Implications
317
W, JIFKE KOEK-NOORMAN & PALL J. M. MAAS. Studies in

Annonaceae XXXVI. The Duguetia Alliance: Where the Ways Part
234
CHATROL, LARS
(See Ching-I Peng & Tzen-Yuh Chiang)
273
R. Statistical Summary of Some of the Activities in the

Missouri Botanical Garden Herbarium, 1999 _
295
CHIANG, TZEN-YUH.
CROSBY, MARSHALL
F. (See Lucinda A. McDade, Thomas F. Daniel, Susan E.

Masta & Katherine M. Riley)
435
Notes on the Vascular Anatomy of the Fruit of Takhtajania

(Winteraceae) and Its Interpretation
398
DANIEL, THOMAS
DEROIN, THIERRY.
DONOGHUE, MICHAEL
J. & WILLIAM S. ALVERSON. A New Age of Discovery

110
DOLST, ANDREW
DOME, JAMES
N. Comparative Floral Ontogeny in Winteraceae
\. Paleobo -
- . -
<.
, ,
366
History of Win-
(See Ghillean T. Prance, Henk Beentje, John Dransfield

& Robert Johns)
_
DRANSEIELD, JOHN.
67
EBINGER, JOHN E. (See Jennifer T. Jawad, David S. Seigler & John E. Ebinger)
EHRENDORFER,
F. & M. LAMBROU. Chromosomes of Takhtajania, Other Win-
K., ANTON ICERSHEIM, F. B. SAMPSON & GEORGE E. SCHATZ.

Floral Structure of Takhtajania and Its Systematic Position in Wintera-
ENDRESS, PETER
KIM HI;. BARBARA.

FEILD, TAYLOR
1 . i
Floristic Surprises in North \merica North of Mexico ...
S., MACIEJ A. ZWIENIECKI & N. M. HOLBROOK. Winteraceae
i
1
l\ rspective
C. ISELE, JOSE VESPRINI,

GABRIELA SPERONI & ALFREDO BERDLJC. Reproductive Biology of Erythrirm crista-galli (Fabaceae)
...._
GALETTO, LEONARDO, GABRIEL BERNARDEI.I.O, IRENE
C. (See John G. Lundberg, Maurice Kottelat, Gerald R. Smith,

Melanie L. J. Stiassny & Anthony C. Gill)
GILL, ANTHONY
GlUSSANi, LILIANA MONICA. Phenetic Similarity Patterns of Dioecious Species

of Poa from \IL'
ind Neigh]
I ountries
& JOHN C. MANNING. Adaptive Radiation of Pollination VI.-el misiiis in / . Iinhu-i i. Crocoideae)
GOLDBLAIT, PETER, PETER BERNHARDT
Gil
HOLBROOK,
N. M. (See Taylor S. Feild, Maciej A. Zwieniecki & N. M. Hol-
brook)
(See Peter K. Endress, Anton Igersheim, F. B. Sampson
& George E. Schatz)
IGEBSHEIM, ANTON.
C. (See Leonardo Galetto, Gabriel Bernardello, Irene C. Isele,

Jose" Vesprini. Gabrida Speroni X Alfredo Berduc)
ISELE, IRENE
JAWAD, JENNIFER T, DAVID S. SEIGLER & JOHN E. EBINGER. A Systematic

Treatment of Acacia coulteri (Fabaceae, Mimosoideae) and Similar Species in the New World
(See Ghillean T. Prance, Henk Beentje, John Dransfield &
Robert Johns)
JOHNS, ROBERT.
G., YOUNGBAE Sun, GEORGE E. SCHATZ & ELIZABETH A.

ZlMMER. Molecular Evidence for the Ph\ logenelie Position of Takhtajania in the Winteraceae: Inference from Nuclear Kibosomal and Chloroplast One Spacer Sequences
KAROL, KENNETH
G. GUTIERREZ & SILVIA S. TORRES ROBLES. Carlos

Spegazzini (1858 l(>20): Travels and Botanical Work on Vascular Plants
KAUNAS, LILIANA, DIEGO
KEATING, RICHARD
pciTicn (Wit
C. Anatomy of the Young Vegetative Shoot of Takl
A. The Evolution of Non-coding Chloroplast DNA ,
:HNER, SCOT
\ppli< atmn in Plant Systematic*
& IHSAN A. AL-SHEHBAZ. M..I

^ lies of the Chinese Yinshania (Brassicaceae): Evidence from Plastid and Nuclear ITS
DNA Sequence Data -
KOCH, MARCUS
KOEK-NOORMAN, JlFKE. (See Lars W. Chatrou, Jifke Koek-Noorman & Paul J.

M. Maas)
MAURICE. (See John G. Lundberg, Maurice Kottelat, Gerald R.
Smith, Melanie L. J. Stiassny & Anthony C. Gill)
KOTTELAT,
LAMBROU,
M. (See F. Ehrendorfer & M. Lambrou)

P., II. (See Alexei A. Oskolski & Porter P. Lowry II) .__.
LOWRY, PORTER
LUNDBERG, JOHN G., MAURICE KOTTELAT, GERALD R. SMITH, MELANIE L. J.

STIASSNY & ANTHONY C. GILL. SO Many Fishes, So Little Time: An
Overview of Recent Ichthyological Discovery in Continental Waters ......

MCDADE, LUCINDA A., THOMAS F. DANIEL, SUSAN E. MASTA & KATHERINE M.
RILEY. Phylogenetic Relationships within the Tribe Justicieae (Acantha-
ceae): Evidence from Molecular Sequ<

MAAS, PAUL
Maas)
3, Mo
ology, and Cytology
J. M. (See Lars W. Chatrou, Jifke Koek-Noorman & Paul J. M.

__
MACKINNON, JOHN.
New Mammals in the 21st Century?
MADICAN, MICHAEL
T. Extremophilic Bacteria and Microbial Diversity
MANNING, JOHN
C. (See Peter Goldblatt & John C. Manning)
MANNING, JOHN
C. (See Peter Goldblatt, Peter Bernhardt & John C. Manning)
E. (See Lucinda A. McDade, Thomas F. Daniel, Susan E. Masta

& Katherine M. Riley)
__
MASTA, SUSAN
A Phylogenetic Analysis of Dicoma Cass, and Related Genera (Asteraceae: Cichorioideae: Mutisieae) Based on Morphological and
Anatomic Characters
ORTIZ, SANTIAGO.
A. & PORTER P. LOWRY II. Wood Anatomy of Mackinlaya

and Apiopetalum (Araliaceae) and Its S\sternal!.' Implieali n-
OSKOLSKI, ALEXEI
& TZEN-YUH CHIANG. Molecular Confirmation of Unidirectional Hybridization in Begonia X taipeiensis Peng (Begoniaceae) from Tai-
PENG, CHING-I
PHILLIPS, OLIVER
L. (See Rodolfo Vasquez Martinez & Oliver L. Phillips)
T, HENK BEENTJK, JOHN DKANSEIELD & ROBERT JOHNS.

The Tropical Flora Remains Undercollected -...
PRANCE, GHILLEAN
KICII
\i;i)so\, P. MICK. Our Unknown Planet: Recent Discoveries and the Future, the 4<S'h Annual Systematics Symposium of the Missouri Botanical
Garden. Introduction to the Symposium
M. (See Lucinda A. McDade, Thomas F. Daniel, Susan E.
Masta & Katherine M. Riley)
RILEY, KATHERINE
S. TORRES. (See Liliana Katinas, Diego G. Gutierrez & Silvia

S. Torres Robles)
ROBLES, SILVIA
SAMPSON, BRUCK.
SAMPSON,
(See Hiroshi Tobe & Bruce Sampson)
F. B. The Pollen of Takhtajama perrieri (Winteraceae) ._...
.____
.._.._
F. B. (See Peter K. Endress, Anton Igersheim, F. B. Sampson &

George E. Schatz)
SAMPSON,
SCHATZ, GEORGE E. The Rediscovery of a Malagasy Endemic: Takl

perrieri (Winteraceae)
-
SCHATZ, GEORGE E. (See Peter K. Endress, Anton Igersheim, F. B. Sampson

& George E. Schatz)
E. (See Kenneth G. Karol, Youngbae Suh, George E. Schatz
& Elizabeth A. Zimmer)
SCHATZ, GEORCE
SEIGLER, DAVID S. (See Jennifer T. Jawad, David S. Seigler & John E. Ebinger)
R. (See John G. Lundberg, Maurice Kottelat, Gerald R. Smith,
Melanie L. J. Stiassny & Anthony C. Gill)
SMITH, GERALD
(See Leonardo Galetto, Gabriel Bernardello, Irene C. Isele, Jos6 Vesprini, Gabriela Speroni & Alfredo Berduc)
SPERONI, GABRIELA.
L. J. (See John G. Lundberg, Maurice Kottelat, Gerald R.

Smith, Melanie L. J. Stiassny & Anthony C. Gill)
STIASSNY, MELANIE
Sun, YOUNGBAE. (See Kenneth G. Karol, Youngbae Suh, George E. Schatz &
Elizabeth A. Zimmer)
& BRUCE SAMPSON. Embryology of Takhtajania (Winteraceae)
and a Summary Statement of Embryological Features for the KamiK
TOBE, HIROSHI
& OLIVER L. PHILLIPS. Allpahuayo: Floristics,

Structure, and Dynamics of a High Diversity Forest in Amazonian Peru
VASOUEZ MARTINEZ, RODOLEO
(See Leonardo Galetto, Gabriel Bernardello, Irene C. Isele,

Jose Vesprini. Gabriela Speroni iK Alfredo Berduc)
VESPRINI, JOSE.
A. (See Kenneth G. Karol. Youngbae Suh, George E.

Schatz & Elizabeth A. Zimmer)
ZIMMER, ELIZABETH
ZWIENIECKI, MACIEJ A. (See Taylor S. Feild, Maciej A. Zwieniecki & N. M.
3 1753 00288 9852
Orchids
Guatemala. Species are listed in alphabetical order,
Orchids of Guatemala:
together with synonyms or species names used in

material, includes 734 taxa, of which 207 are new
records or recently described species not reported
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...... Lucinda 1. MrDadr. Thomas F. Daniel, Susan E. Masta & [Catherine M. Riley
4.^5
A Phylogenetic Analysis of Dicoma Cass, and Related Genera (Asteraceae: Cichorioideae: Mutisieae) Based on Morpholngh al and \natnmic Characters
Santiago Ortiz
459
The Evolution of Non-coding Chloroplast DNA and Its Application in Plant Systematics
Scot A. Kelchner
nian Peru
Rodolfo Vdsquez Martinez & Oliver L Phillips
482
499
A Systematic Treatment of Acacia coulteri (Fabaceae, Mimosoideae) and Similar

Species in the New World
Jennifer T. Jawad, David S. Seigler & John E. Ebinger
A Review of Gamosepaly in the Brassicaceae and a Revision of Desideria, with a Crit-
528
ical Evaluation of Related Genera

Ihsan A. Al-Shehbaz
Vlaptive Radiation of Pollination Mechanisms in Ixia (lndaccac: Cmcoid.-ae)
549
Peter GoldblaU, Peter Bernhardt & John C. Manning
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Index to Volume 87

The Duguetia Alliance Where The Ways Part - Ol.87 (2), Pp.234-245

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The Annals, published quarterly, contains papers, primarily in systematic botany,

Henk van der Werff

(ISSN 0026-6493) is published quar-

& Management, P.O. Box 1897, Lawrence, K

terl) bv the Missouri Botanical Garden, 2345

66044-8897. Subscription price is $130 p<

Tower Grove Avenue, St. Louis, MO 63110.

volume U.S., $140 Canada & Mexico, $165 a

Periodicals postage paid at St. Louis, MO and

other countries. Four issues per volume. Tl

additional mailing offices. POSTMASTER: Send

s the requirements of ANSI/NISO Z39.48-1992 (Permanence of Paper).

OUR UNKNOWN PLANET:

the world to be discovered. The finding of this seei

M/."/is,f(,'- >>'/ , ."'v/v,' ,>' </" <

mis in the U.S.,

portant than the discoveries which make headline

'This and tht eigi.l

87: 1-2. 2000.

tegrate their analyses ami discuss criteria for es-

lablishmenl of higher taxa.

Schwartz, 1998) and Symbiotic Planet: A New Look

^ZtL^'u- ' 'md' .',me nom.aichima I','! I l!i''""l l'.T

will agree with Margubs's concept of monophyly,

N.llis. P. S.. I). I\. Noltis c\ J. |. Doyle (Kdilors). 1992.

teresting viewpoint to overall discussions of biodi-

versity, and at tilt - III. lm

Molecular iMsl.analirs ol Plants II I )\ \ Seciuen<anKluwer. Huston

Since the days almost 100 years ago when Robert

bacteria. This giant leap forward emerged from the

i ristb s such as bones

h of M. T. Madigan is supported by National Science Foundation grant OPP 9809195.

ANN. MISSOURI BOT. GARD.

87: 3-12. 2000.

Microbial Life Forms

from maerobiologisls as e\ ulenoed in lh< inclusion

relationships of piokar\oles (Fig.

different plants or animals can be extremely closely

while the mouse and the elephant have only very

PaPer wil1 trY to introduce the reader to some of

Prokaryotes ruled the Earth for at least 2 billion

laboratory studies of these remarkable prokaryotes

karyotic cell appears in the fossil record. And

inela/oans (multi-i < !

EXTREMK ENVIRONMENTS AND EXTREMOPHII.ES

the lun. tlu si !_

Microbiological cxamuialion ol e\li.-me en\ iror'

-- change in prokaryotes is not manifest in morFor what

In contrast to higher organisms prokaryotes have

,., ... . ,..l.l I. .,

i<: i>e lughb dhergenl organ sins.

and the elephant ai

had alrcaiK occurred. Diversification ol lhe mouse

Seyera] c]asses ()f

n-eogni/ed in mierobiologv. and laboratory cidlmcs

tena maintained a very small s.ze and changed

f,,lol,,LV l""^' billinnx ol v. .,- ol evolutional

,,,,,e term, usually a word with Greek or Latin

of each class are known (Table

Classes and examples of extremophiles".

MT41 (Mariana Trench)1'

it becomes clear that t