Journal of Experimental Marine Biology and Ecology: Daniel H. Green, Peter J. Edmunds, Xavier Pochon, Ruth D. Gates

Journal of Experimental Marine Biology and Ecology 384 (2010) 1829
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Journal of Experimental Marine Biology and Ecology

j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j e m b e
The effects of substratum type on the growth, mortality, and photophysiology of

juvenile corals in St. John, US Virgin Islands
Daniel H. Green a, Peter J. Edmunds a,, Xavier Pochon b, Ruth D. Gates b
a
b
Department of Biology, California State University, 18111 Nordhoff Street, Northridge, CA 91330-8303, USA
University of Hawaii, School of Ocean and Earth Science and Technology, Hawaii Institute of Marine Biology, PO Box 1346, HI 96744, USA
a r t i c l e
i n f o
Article history:
Received 23 July 2009
Received in revised form 5 December 2009
Accepted 7 December 2009
Keywords:
Growth
Juvenile
Photophysiology
Scleractinia
Substratum
Symbiodinium
a b s t r a c t
Coral larvae are selective with regards to the surfaces upon which they settle, but little is known about the
outcome of these choices. In this study, we explored the implications for juvenile scleractinians (b 40-mm
diameter) of growing on igneous versus carbonate rock on the shallow reefs (5-m depth) of St. John, US
Virgin Islands. Surveys revealed that juvenile corals occurred at densities of 16 colonies m 2 and were
distributed on igneous and carbonate rocks in proportion to the abundance of these surfaces, suggesting that
larvae do not discriminate between rock types at settlement. Repeated surveys demonstrated that all
juvenile corals (i.e., pooled among taxa) grew 41% slower on igneous versus carbonate rock between January
and August, but not between August and January when the growth was statistically indistinguishable
between rock types. Although the growth of the most common juvenile coral, Porites astreoides, was similar
on both substrata, the photophysiology of this species was affected by the type of rock. The maximum
relative electron transfer rate (rETR, a proxy for photosynthesis) of P. astreoides was down-regulated 30% on
igneous compared to carbonate rock. Phylogenetic analyses of the Symbiodinium community sequence
proles within P. astreoides revealed signicant differences between substrata, with a greater diversity of cooccurring ITS-2 sequences in corals growing on carbonate compared to igneous rock. While substratumdependent patterns in the characteristics of juvenile corals suggested there is selective value to the
settlement choices made by larvae, these trends did not translate into differences in survival, at least over the
time scale investigated. It remains uncertain what features of the rocks affected coral performance, but
differences in the temperature of the rock may be an important feature during the warmest period of the
year.
2009 Elsevier B.V. All rights reserved.
1. Introduction
In marine systems, populations of most organisms are strongly
affected by recruitment and post-settlement events (Sutherland,
1990; Menge, 2000), and for benthic taxa with pelagic larvae, high
recruitment is inuenced by pre- and post-settlement processes
occurring in pelagic and benthic realms, respectively. Pre-settlement
events in the water column are poorly understood because they are
difcult to study (Underwood and Keough, 2001), however benthic
inuences on post-settlement processes are better studied and
include substratum type, rugosity, orientation, and chemical signatures (Rogers et al., 1984; Raimondi, 1988; Pawlik, 1992; Baird et al.,
2003), as well as exposure to physical factors such as ow (Eckman,
1983) and temperature (Pechenik, 1984). Reef corals have a life cycle
that is split between the benthic and pelagic realms, and much is
Corresponding author. Tel.: + 1 818 677 2502; fax: + 1 818 677 2034.
E-mail address: peter.edmunds@csun.edu (P.J. Edmunds).
0022-0981/$ see front matter 2009 Elsevier B.V. All rights reserved.
doi:10.1016/j.jembe.2009.12.008
known about the substratum choices made by their larvae as they end
their pelagic phase (Mundy and Babcock, 1998; Raimondi and Morse,
2000; Harrington et al., 2004), and the types of microhabitats into
which this behavior places juvenile corals (Edmunds et al., 2004;
Norstrom et al., 2007). Surprisingly however, there is little empirical
evidence that the well known substratum selection by coral larvae
translates into benets for the juvenile colonies into which some of
them will grow (but see Harrington et al., 2004).
Once coral larvae are competent to settle, they descend to the
benthos and begin substratum selection (Baird et al., 2003). The
choice of an area for settlement can be driven by positive geotaxis
(Vermeij et al., 2006), phototaxis (Mundy and Babcock, 1998) and a
preference for specic wavelengths of light that assist in identifying a
suitable depth for settlement (Mundy and Babcock, 1998). In shallow
water, these behaviors usually result in settlement in cryptic
microhabitats, such as beneath settlement tiles, but in deeper areas,
coral larvae favor less cryptic locations (Rogers et al., 1984). Once in
an area that is suitable for settlement, coral planulae select surfaces
based on their chemical and physical properties (Morse et al., 1984).
In many cases, crustose coralline algae (CCA) provide the cues, with
D.H. Green et al. / Journal of Experimental Marine Biology and Ecology 384 (2010) 1829
different CCAs offering cues of varying strength (Harrington et al.,

2004), either because of a chemical inducer within the algae (Morse
et al., 1984), or the presence of bacterial lms on the algae (Negri
et al., 2001). In light of this deterministic substratum selection, it is
reasonable to infer that such traits are under strong selective pressure
because they affect coral tness. While tness consequences of
substratum selection have been demonstrated for benthic invertebrates such as barnacles (Herbert and Hawkins, 2006), rotifers
(Kuczynska-Kippen, 2005), and polychaetes (Sebesvari et al., 2006),
comparable evidence for scleractinians is rare, apart from a few
studies that have tested for differences in survival of recruits among
surfaces differing in orientation (Babcock and Mundy, 1996; Mundy
and Babcock, 2000), types of CCA (Harrington et al., 2004), or
densities of adult corals (Edmunds, 2000). One study that sought to
test the tness consequences for juvenile corals of growing in open,
cryptic or vertical surfaces did not identify effects for growth or
survivorship (Edmunds et al., 2004).
The objective of this study was to test the effects of settlement to
different substrata on the physiology and tness of juvenile corals.
The opportunity arose to test these effects in St. John, US Virgin
Islands, where juvenile corals ( 40-mm diameter) have been
monitored on shallow (b6-m depth) reefs for more than a decade
(Edmunds, 2000, 2004, 2007), and are found in large numbers on both
calcium carbonate and igneous rock. The ecology and geology of reefs
in this region are well known (Rogers et al., 2008), and along the
south coast of St. John, fringing reefs occur in sheltered habitats where
ow speeds are typically b5 cm s 1 (Horst and Edmunds, in press),
and the substratum is dominated by igneous rock that forms
underwater cliffs and boulders (Rankin, 2002; Rogers et al., 2008).
In the vicinity of Great Lameshur Bay, the majority of the igneous rock
is phenocryst-poor keratophyre, with traces of plagioclase phyric
keratophyre, volcanic rock and bedded tuff, basalt, and basaltic
andesite (Rankin, 2002). In addition to the igneous rock, the fringing
reefs also include calcium carbonate from dead scleractinians and
other calcifying taxa such as bivalves and certain algae (hereafter
referred to as carbonate rock). However, there is little accumulation
of a carbonate framework, at least in shallow water (b6-m depth).
Juvenile corals occur at mean densities of 16 1.2 corals m 2
(SE, in 2007) on the fringing reefs of St. John, but their densities vary
among years and are associated with seawater temperature
(Edmunds, 2004). While monitoring these corals as part of a longterm program (Edmunds, 2002; Edmunds and Elahi, 2007), we
noticed that the igneous and carbonate rock differed in several ways.
The igneous rock was darker and smoother than the carbonate rock,
and in the afternoons during August (when the surveys were
completed) igneous rock was warmer to the touch than carbonate
rock, and both seemed warmer than seawater. Given the strong
effects of temperature on corals (e.g., Middlebrook et al., 2008; Jokiel,
2004; Randall and Szmant, 2009), and the likelihood that during the
summer corals live close to their upper thermal limit (Coles and
Brown, 2003), we wondered whether the differences in substratum
temperature were sufcient to affect the success of juvenile colonies.
This reasoning served as an impetus for the present study, and here
we describe analyses conducted to test the effect of substratum type
on juvenile corals, specically to test the hypothesis that their growth
and mortality are independent of the rock type upon which they
grow. To gain insight into traits that might cause the success of
juvenile corals to vary, for each rock type and for the most common
genus of juvenile corals (Porites), we assessed photophysiological
performance. To determine whether substratum temperature could
mediate the success of juvenile corals, we measured the temperature
of the rock and seawater with thermistors. We also identied the
endosymbiotic dinoagellates (Symbiodinium ITS-2 sequence composition [sensu Stat et al., 2009]) within juvenile P. astreoides to
determine whether they differed between colonies growing on
igneous versus carbonate rock. As P. astreoides in the Caribbean
19
contains several Symbiodinium ITS-2 sequences, including A4, A4a, B1,

and C1a (LaJeunesse, 2002; Banaszak et al., 2006; Thornhill et al.,
2006; Warner et al., 2006), and different Symbiodinium strains can
express different physiological traits both in hospite and in vitro
(Kinzie et al., 2001; Rowan, 2004; Little et al., 2004; Iglesias-Prieto
et al., 2004), we reasoned that variation in Symbiodinium sequences
might play a role in determining the success of corals on substrata
having different features.
2. Methods
2.1. Overview and study sites
Juvenile corals (colonies 40-mm diameter [Bak and Engel,
1979]) on igneous and carbonate rock were studied at three locations
(Donkey Bite, Yawzi Point, and Tektite) on the fringing reefs
surrounding Great Lameshur Bay (Fig. 1). These locations were used
to sample the fringing habitats at 5-m depth, but were not utilized as a
factor in the analyses. To assess the relative abundance of rock
surfaces suitable for coral settlement, the percentage cover of igneous
and carbonate rocks was measured at the three sites. The effects of
rock type on the growth and mortality of juvenile corals, as well as the
photophysiology of juvenile Porites were investigated at Yawzi Point
and Tektite. The temperature of the substratum was recorded at Yawzi
Point, and colonies of juvenile P. astreoides were randomly sampled
from igneous and carbonate rock at Donkey Bite and Tektite for the
analysis of Symbiodinium genotypes. In all cases, rock surfaces with
similar ambient light regimes were selected for sampling of juvenile
corals.
Fig. 1. Map of St. John, US Virgin Islands, showing the location of the Virgin Islands
Environmental Resource Station (*) and the three study sites (Donkey Bite, Yawzi Point,
and Tektite) within Great Lameshur Bay.
20
2.2. Relative abundance of rock surfaces and distribution of juvenile

corals
To distinguish between random versus selection as the mechanism
determining the distribution of juvenile corals, the area of igneous and
carbonate rock surfaces was assessed and the number of juvenile
corals on each rock type measured. Rock types were assessed in
randomly positioned 1 m2 quadrats (n = 10) along a 40-m transect
placed on the 5-m depth contour. Hard substratum was distinguished
as either igneous or carbonate rock. In the survey areas, the hard
substratum was mostly composed of roughly hemispherical shaped
boulders of various sizes, and it was therefore possible to approximate
their area from an equivalent-sized hemisphere. The diameter of each
boulder was measured (1 cm), and the proportion of the boulder
within the quadrat estimated to the nearest 10%. These measurements
were used to estimate the area of igneous or carbonate boulders
within the quadrat. The number of juvenile corals on each rock type
was quantied by genus using 0.25 m2 quadrat placed randomly
along the same transect (n = 42).
The objective of these surveys was to determine the areas of
igneous and carbonate rocks that were available for coral recruitment,
and therefore suitable substrata were dened liberally to include rock
surfaces that were apparently vacant, as well as those encrusted with
algae, sponges, and other invertebrates. We assumed that these
organisms could die or be removed to expose surfaces suitable for
coral settlement. The cover of igneous and carbonate rocks was
averaged across all quadrats, and the mean cover (cm2) of each rock
type was used to determine the number of juvenile corals expected on
each surface based on chance. The actual distribution of juvenile
corals was compared to that expected by chance using a 2contingency table, rst for all of the juvenile corals (i.e., all genera
pooled), and then for Porites, the most commonly encountered genus
of juvenile corals.
2.3. Growth and mortality

To test for variation in growth and mortality of juvenile corals on
igneous and carbonate rocks, colonies of Porites (mostly P. astreoides),
Agaricia (mostly A. agaricites and A. humilis), and Siderastrea (mostly
S. siderea) were censused over 57 months on both rock types. Initial
surveys were conducted in August 2006, and were repeated in January
2007, August 2007, January 2008, and August 2008. The 57 month
interval was selected to explore within-year variation in coral success
based on duplicate samplings for AugustJanuary and January
August. These periods were climatologically different, with August
January coinciding with frequent hurricanes and seasonal cooling, and
JanuaryAugust largely free of intense storms and coinciding with
seasonal warming (Lehmiller et al., 1997; Winter et al., 1998). To
census juvenile corals, colonies on igneous and carbonate rock were
selected as they were encountered while swimming along transects
placed along the 5-m depth contour. Each colony was marked with a
numbered aluminum tag that was attached to the adjacent substratum using underwater epoxy (Z-Spar, A788). Approximately 40
juvenile coral colonies, the majority of which belonged to the genus
Porites, were tagged on each rock type at the start of each sampling
period.
Tags were relocated using an underwater metal detector, and coral
skeletons with live tissue were scored as alive. Those that were dead
in place, or missing, were scored as dead. The size of live corals was
determined as the average of the largest and smallest diameters of the
basal portion of tissue, as measured with calipers (1 mm), and
growth was calculated as the difference between initial and nal
mean diameter. As the sampling intervals varied slightly among
sampling periods, growth rates were adjusted proportionately to
6 months (i.e., mm 6 mo 1).
Growth rates were compared between substratum types (xed

factor), sampling periods (xed factor), and years (random factor)
using a three way, model II ANOVA. Where interaction terms were not
signicant (at p N 0.25, Quinn and Keough, 2002), they were pooled
with the error term for signicance testing. The mortality of the
juvenile corals (the number alive versus dead) was compared
between substrata using contingency tables. In both cases (growth
and mortality) two sets of analyses were completed where sample
sizes (number of tagged corals) permitted, rst for juvenile corals
with all coral genera pooled, and second, for Porites alone.
2.4. Photophysiology
To test for differences in photophysiology for juvenile corals on
igneous and carbonate rock, two analyses were completed using
Porites astreoides. We selected this species because it is the most
abundant juvenile coral on shallow reefs in Great Lameshur Bay, and
the distinctive color of the yellow morph (Gleason, 1998) allowed for
species identication of small colonies. First, light-adapted quantum
yield of PSII (PSII) was recorded at midday as a measure of photosynthetic efciency. PSII refers to the proportion of the light
captured by PSII that is used for photochemical processes during lightadapted conditions, and therefore it provides a measure of linear
electron transport and the capacity for photosynthesis (Maxwell and
Johnson, 2000). PSII is sensitive to light exposure (Maxwell and
Johnson, 2000), and can only be used for comparative analyses under
a constant light history. Second, because the initial measurements of
PSII proved inconclusive for distinguishing the effects of substratum
type on juvenile corals, rapid light curves (RLC [Ralph and Gademann,
2005]) were used to analyze relative electron transfer rate (rETR) as a
function of photon ux density (PFD) for corals on each substratum.
These relationships provide a comprehensive indication of the
capacity of Symbiodinium to utilize light, and the relationship is
analogous to photosynthesis versus irradiances responses based on
oxygen evolution or carbon xation (Ralph and Gademann, 2005). All
measurements of photophysiology were completed using a Diving
PAM (Walz, GmbH) tted with an 8-mm diameter sensor, and the
settings for this instrument remained constant for all determinations.
PSII was measured annually in August between 2003 and 2006
(i.e., over 4 y), as well as in January 2007, and each set of measurements (i.e., within each month) was obtained between 12:00 and
13:00 h on four sunny days to ensure that corals were exposed to
similar light histories. The corals were selected at random with
regards to the substratum type and were on near-horizontal surfaces
at 5-m depth. Preliminary analyses revealed that PSII did not vary
signicantly among sunny days within each month (see Results), and
therefore the results were pooled by day to compare among substrata
and periods. A two-way, mixed model ANOVA was used to compare
PSII among substrata (xed factor) and sampling year (random
factor, based on August samplings between 2003 and 2006). A
separate two-way, xed-effects ANOVA was used to compare PSII
between sampling period (xed factor, August 2006 versus January
2007) and substrata (xed factor). The second analysis was intended
to gain insights into seasonal variation in PSII between substrata,
although without replication at the seasonal level, the outcome must
be interpreted with caution.
RLCs were applied to juvenile P. astreoides in August 2007 and
January 2008, and measurements were completed between 12:00 and
13:00 h on sunny days. Using RLCs, the relative electron transport rate
(rETR = PSII x PAR, where PSII is the photosynthetic yield and PAR is
photosynthetically active radiation) is computed after 10 s exposures
to 8 irradiances (Walz, 1998 [Ralph and Gademann, 2005]) that were
adjusted to 1644 mol photons m 2 s 1. A limitation of this procedure is that such short exposure to the light intensities does not
allow rETR to fully equilibrate (Ralph and Gademann, 2005).
Nevertheless, the results allow a comparison of relative effects of
treatments on the capacity to utilize a range of light intensities for

photosynthesis.
The results of RLCs were compared between substrata by
generating best-t curves of rETR versus irradiance, and statistically
comparing the curve parameters between corals on igneous and
carbonate rock. Best-t curves were obtained using least-squares
regression to t a three-parameter, non-linear function with two
exponentials that incorporated declining photosynthesis at high light
intensities (Platt et al., 1980) (Eq. (1)):
P = Po + Ps 1 expI = Ps expI = Ps
where P is the rate of photosynthesis (i.e., rETR), Po is the intercept of

the best-t curve on the Y axis, Ps is a scaling factor dened as the
maximum potential rate of photosynthesis, is the slope of the initial
linear portion of the curve, I is the irradiance, and is a linear measure
of the reduction in P at high light intensities. In some cases, the corals
displayed no signs of reduced P at high light, and in these cases the
data were tted with a simplied function (Eq. (2)):
P = Po + Pm 1 expI = Pm
where the parameters are the same as for Eq. (1), except that Pm is the
photosynthetic capacity at saturating irradiance. In Eq. (1), Ps is a
theoretical value that does not reect the actual maximum rate of
photosynthesis. In these cases, the actual maximum rate of photosynthesis was calculated from the best-t curves. All best-t curves
were obtained using a least-squares routine in Systat 11 running on a
Windows platform, and the curve parameters were compared between substrata using one-way ANOVA.
2.5. Temperature of the substratum and the seawater
To measure temperatures, a 12-bit instrument based on a HOBO
Micro Station Data Logger (model H21-002) equipped with three
temperature sensors (model S-TMB-M006, 0.2 C accuracy and
0.03 C resolution) (Onset, Bourne, MA) mounted on 6-m cables
that could be implanted in holes drilled into the rock was used. The
sensors were calibrated against a NIST certied, mercury thermometer (ERTCO, model 1003-FC-BF). In August 2005, spot measurements were made during 24 h deployments, and starting in 2006,
measurements were made over a year to provide a longer temporal
context for the comparison of the temperature of the rocks and
seawater.
For the spot measurements, the logger was tted into a waterproof
housing, and the cables passed through bulkhead connectors. Two
positions at Yawzi Point were chosen to provide access to igneous and
carbonate rock at 5-m depth, and the logger was installed from 1316
August 2005, to 1718 August 2005, respectively. One sensor was
suspended 25-cm above the benthos, and the other two were
embedded in holes drilled 2-cm into the rock. The sensors were
imbedded using a heat sink compound (Radio Shack #276-1372), and
the logger was programmed to record every 10 s. For the 1-year
deployment, the same logger was encapsulated in rubber and
installed at 5-m depth at Yawzi Point on 1 August 2006. As with the
spot measurements, one sensor was in the seawater, one in igneous
rock, and one in carbonate rock, although for this installation the rock
sensors were secured with epoxy (Z-Spar, A788). The logger was
programmed to sample every 10 min and was recovered on 2 August
2007.
To characterize the temperature from spot measurements, the
data were analyzed to determine the greatest difference in temperature of the two rocks, relative to seawater. For year-long records, the
data were characterized by the daily range in temperature. This metric
was separated by season (astronomical Summer, Fall, Spring, and
Winter) and tested for differences among the two substrata and
21
seawater using a two-way ANOVA with thermal microenvironment

(i.e., the two rocks and seawater) and season as xed factors.
2.6. Genetic analysis of Symbiodinium
Twenty colonies of juvenile P. astreoides were selected for
Symbiodinium genotyping, with ten from each of the igneous and
carbonate rock at 5-m depth at either Donkey Bite or Tektite.
Symbiodinium sequence proles were identied by cloning and
sequencing the ITS-2 marker following published protocols (Stat
et al., 2009; Pochon et al., 2010). Symbiodinium community sequence
proling describes dominant and rarer ITS-2 sequences present in
each coral, and differs from other studies that target dominant ITS-2
sequences only (e.g., LaJeunesse 2002).
Chromatograms of DNA sequences were inspected using Sequencher
4.7 (Gene Codes Corporation, Ann Arbor, MI, USA), aligned and edited
using BioEdit 5.0.9 (Hall, 1999) and identied using Basic Local
Alignment Search Tool (BLAST) in GenBank. Only sequences obtained
from 3 independent clone libraries were used in the downstream
analysis. The remaining clone singletons were assumed to be artifacts or
rare intragenomic repeats, and the nucleotide at the site of polymorphism converted to the consensus. A single ITS-2 rDNA alignment was
created for phylogenetic analyses, representing edited Symbiodinium
sequences derived from our clone libraries together with all known
clade A Symbiodinium ITS-2 sequences recovered from GenBank, as of
May 2008 (cf. LaJeunesse et al., 2008). A statistical parsimony network
was generated using TCS 1.21 (Clement et al., 2000), and delineated
with 95% certainty. The gaps in the network were treated as a fth state
with the alignment edited so that the entire indel was considered a
single mutation.
An analysis of molecular variance (AMOVA) was carried out on
two datasets using Arlequin 3.1 (Excofer et al., 2005) to evaluate the
genetic variance among Symbiodinium ITS-2 sequences in corals from
igneous and carbonate rocks, as well as between Donkey Bite and
Tektite. Our dataset meets the assumptions of AMOVA for a nonstandard system because they comprise sequences generated using a
marker that is both intra and intergenomically variable and as such,
the sequences in each clone library are not independent from one
another. Therefore, AMOVA is used here to test for variability in the
ITS-2 sequence proles (not Symbiodonium spp. compositions). The
site contrast was used to test for site-specic patterns that would
preclude a single test for substratum effects. The rst analysis compared the ITS-2 sequence diversity between igneous and carbonate
rocks regardless of sites, and the second compared the ITS-2 sequence
diversity between sites regardless of rock type; in both cases the
analyses tested the hypothesis of no difference in sequence diversity.
The AMOVA included 10,000 permutations, and the distance matrix
was computed using Jukes and Cantor (1969) as the best-t model of
evolution for our ITS-2 alignment, and previously obtained using
Modeltest 3.7 (Posada and Crandall, 1998). AMOVA's were followed
by exact tests of allele differentiation (Raymond and Rousset, 1995)
for each contrast ( = 0.05, Markov chain steps = 10,000). The
additional exact tests were conducted as a means to further evaluate
the conclusions obtained from the AMOVA.
3. Results
3.1. Relative abundance of rock surfaces and distribution of juvenile
corals
The surveys of substratum availability revealed that types of rock
differed in abundance (F1,58 = 20.61, p b 0.01), with each quadrat
averaging 6213 565 cm2 of igneous rock, and 2837 483 cm2 of
carbonate rock (SE, n = 30). Surveys for juvenile corals revealed
290 juvenile corals in 126 quadrats, with 64% on igneous rock and 36%
on carbonate rock. The number of juvenile corals on each rock type
22
did not differ signicantly from the number expected based on

random settlement to surfaces that differed 2.2-fold in abundance
(2 = 3.64, df = 1, p = 0.06), and therefore, their distribution did not
support the hypothesis of preferential substratum selection by coral
larvae. For juvenile Porites, 134 colonies were found, with 57%
on igneous and 43% on carbonate rock; this distribution also did
not differ from that expected based on chance settlement alone
(2 = 2.99, df = 1, p = 0.08).
3.2. Growth and mortality
Over each of the four census periods, between 33 and 80 juvenile
corals were tagged and found 57 months later, and b15% of the tags
were lost. Of the corals that were tagged and found, the most common
genera were Porites (4876% of tagged corals), Agaricia (1533%), and
Siderastrea (818%), and these genera were equally represented over
each of the study periods (2 = 10.55, df = 6, p = 0.10). For the corals
alive at the end of their census period, the majority (78%) increased in
size, and only a small number (22%) decreased in size, mostly because
their tissue retreated from the edge of the skeleton. The growth rates
of all juvenile corals ranged between 12 mm 6 mo 1 (i.e., some
shrank) and 16 mm 6 mo 1, and were unaffected by the initial colony
size (D.H. Green unpublished data).
In the three way, Model II ANOVA comparing growth of all juvenile
corals among substrata, sampling periods, and years, the three way
interaction and most of the two-way interactions were not signicant
(p N 0.25), and were pooled with the error term (Table 1). The effects
remaining in the model demonstrated that growth differed between
rock types in a manner that varied between sampling periods and
years (Table 1). These interactions were caused by: (1) higher growth
on carbonate compared to igneous rock from January to August in
both 2007 and 2008, yet similar growth rates on both rocks from
August to January of 2006/07 and 2007/08, and (2) growth rates that
were reduced 41% on igneous compared to carbonate rocks between
January and August 2007, with the same trend intensifying the
following year (January to August 2008) with colonies shrinking on
igneous rock (at 0.12 mm 6 mo 1) while they grew on carbonate
rock (at 4.27 mm 6 mo 1) (Fig. 2). For P. astreoides, mean growth
rates ranged from 0.1 mm 6 mo 1 to 4 mm 6 mo 1, but growth was
unaffected by substratum, sampling period or year (Table 1). When
the analysis was repeated after excluding P. astreoides in order to
elucidate the role of this species in the overall trend, strong seasonal
and substratum effects were again observed; the substratum x period
interaction was signicant (F1,57 = 4.16, p = 0.05), although no other
main effects, or interactions were signicant (p N 0.05).
Table 1
Statistical results of a 3-way, model II ANOVA comparing growth rates (mm 6 mo 1)
among sampling periods (AugustJanuary versus JanuaryAugust, xed factor), years
(2006/07 versus 2007/08, random factor), and substrata (igneous versus carbonate
rock, xed factor) for (A) juvenile corals (pooled among taxa), and (B) Porites
astreoides. Interactions terms that were not signicant (at p 0.250) were pooled with
the error term for the purpose of signicance testing of the factors and interactions
remaining (Quinn and Keough 2002).
Taxonomic group
Source
df
MS
A. Pooled taxa
Substratum
Period
Year
Substratum Period
Substratum Year
Error
Substratum
Period
Year
Substratum Period
Substratum Year
Year Period
Error
1
1
1
1
1
197
1
1
1
1
1
1
133
139.81
138.63
3.45
112.48
79.37
14.66
50.48
148.32
0.20
31.05
25.45
22.70
15.29
1.76
9.46
0.24
7.67
5.41
0.41
b 0.01
0.63
0.01
0.02
1.98
6.45
0.01
2.03
1.67
1.49
0.39
0.24
0.91
0.16
0.20
0.23
B. Porites astreoides
Fig. 2. Growth rates (mm 6 mo 1) of juvenile corals on igneous and carbonate rock
during the four sampling periods. Sampling periods span August (A) to January (J) and
January to August of three years (2006, 2007, and 2008). Values plotted are means SE
with sample sizes as shown.
Of the corals tagged and found again at the end of each census
period, 828% were dead (n 3 census periods). These mortalities
translate into only a small number of colonies that were scored as
dead, and this precluded an analysis of mortality by genus. For all
juvenile corals, the numbers that were categorized as alive or dead
was independent of rock type for all four sampling periods (2 1.57,
df = 1, p 0.21). These results did not differ among sampling periods
(2 test of homogeneity, 2 = 0.89, df = 3, p N 0.95) and therefore,
they were pooled among periods (Table 2). Overall, the fate of
juvenile corals (i.e., whether they were alive or dead) was unaffected
by the substratum type (p = 0.24).
3.3. Photophysiology
For juvenile P. astreoides, comparisons of PSII among days within
one sampling period showed that the values were indistinguishable
(F4,74 = 0.02, p = 0.51), demonstrating that daily light regimes had
consistent effects on PSII. Therefore, sampling day was not used as a
factor in the analyses of PSII. The mean values of PSII ranged from
0.37 on igneous rock in August 2006, to 0.48 on igneous rock in August
2007 (Fig. 3), but it was unaffected (p 0.10) by substratum in the
contrasts among years and between seasons (Table 3). PSII did
however, vary among years and seasons, but in both cases it was
unaffected by interactions with the main effects (Table 3). Higher
values of PSII were recorded in August of 2003 than in August of
20042006, and in January 2007 versus August 2006 (Fig. 3).
RLCs were prepared for 6 juvenile P. astreoides on igneous rock, and 9
on carbonate rock, and revealed a consistent response with rETR
Table 2
Contingency table displaying the number of juvenile corals scored as alive or dead on
igneous and carbonate rock after 6 months. Due to small sample sizes, results are
pooled among four sampling periods between 2006 and 2008. The fate of juvenile
corals was independent of the rock type they were growing upon (2 = 1.36, df = 1,
p = 0.24).
Igneous
Carbonate
Total
Alive
Dead
Total
124
81
205
17
17
34
141
98
239
Fig. 3. Light-adapted photosynthetic quantum yield (PSII) of juvenile Porites astreoides

on igneous and carbonate rock for August samplings in each of 4 years (20032006),
and one January sampling in 2007. Separate analyses were used to compare PSII
among years using the August data, and between seasons using the August 2006 and
January 2007 data (Table 3). Values plotted are means SE with sample sizes as shown.
increasing rapidly with irradiance to 500700 mol photons m 2 s 1.

Thereafter, rETR either declined at higher irradiances (i.e., it was
photoinhibited [Fig. 4]) or stabilized at a maximum value. A reduction
in photosynthesis at high light was observed in the majority of corals on
both igneous (n = 4) and carbonate (n = 5) rock, and was prominent in
the overall mean response on both rock types (Fig. 4). Of the parameters
describing the best-t curves, only rETRmax differed signicantly
between rock types, and was 30% lower on igneous compared to
carbonate rock (Table 4).
3.4. Temperature
The spot measurements of temperature were completed over two
periods in August 2005, and revealed that the temperature of both
rock types, as well as the seawater, increased from 7:00 to 14:00 h,
and decreased from 14:00 to 21:00 h, thereby creating daily
temperature variations of 0.13 C to 1.20 C over the 5 measurement
days. Igneous and carbonate rocks were slightly warmer than the
seawater during the morning, with the greatest difference of 0.36 C
occurring at about noon.
The year-long temperature record (August 2006August 2007) for
igneous rock, carbonate rock, and seawater revealed seasonal
variation of 3.2 C between summer and winter, and strong diurnal
warming that occurred throughout the year (Fig. 5A). Diurnal
warming was evident in the seawater as well as the rocks, and was
Table 3
Results of a 2-way, mixed model ANOVAs comparing PSII for juvenile Porites astreoides
between substrata (igneous versus carbonate rock, xed factor) and (A) among
sampling years (random factor), and (B) between seasons.
Time contrast
Source
df
MS
(A) Among years
Substratum
Year
Substratum Year
Error
Substratum
Season
Substratum Season
Error
1
1
3
424
1
1
1
105
4.72 103
0.21
4.73 103
0.01
0.01
0.23
0.02
0.01
1.00
30.93
0.69
0.50
b 0.01
0.41
0.62
33.57
2.74
0.43
b 0.01
0.10
(B) Between seasons
23
Fig. 4. Results of RLCs applied to Porites astreoides to quantify the relationship between
relative ETR (rETR) and light intensity (PAR) for juvenile colonies on igneous and
carbonate rock at 5-m depth. Values shown are mean SE (n = 9 [carbonate rock] and
6 [igneous rock]) and the curves are the best-t relationships to the mean values, as
determined using least-squares techniques to t non-linear functions (refer to text for
details).
generally greater in spring (e.g., April, with values of 0.520.54 C)

than winter (e.g., December, with values 0.390.42 C). The daily
range in temperature differed among seasons (F3,1083 = 16.755,
p b 0.010), and there was a trend for it to differ among thermal
microhabitats (F2,1083 = 2.849, p b 0.058), although the differences
were extremely small; post-hoc analysis revealed that igneous rock
had a higher mean daily range in temperature compared to seawater
(t = 1.96, df = 730, p = 0.03) (Fig. 5). There was no interactive effect
of season and thermal microhabitat in determining the daily range in
temperature (F6,1083 = 0.62, p = 0.720). The mean daily range in
temperature tended to be larger for igneous rock compared to
carbonate rock, and for both rock types compared to seawater (Fig. 5).
3.5. Genetic diversity of Symbiodinium
Between 9 and 13 ITS-2 sequences for Symbiodinium in clade A
were recovered from clone libraries for each coral (n = 20), and
represented 212 sequences, with 107 for carbonate rock and 105 for
igneous rock. Sixteen distinct Symbiodinium ITS-2 sequences were
recovered, including 10 singletons (data not shown) and 6 sequences
retained for phylogenetic analysis (Table 5). The two dominant
genotypes, A4 and A4a, co-occurred in most (n = 16) corals,
representing 105 and 55 retrieved sequences, respectively. A4
sequences were present in all samples, and were approximately
twice as common as A4a, regardless of sampling site and substratum
type. The remaining four ITS-2 sequences (i.e., A4.1, A4.2, A4.3, and
A4a.1) did not match any GenBank sequences, and co-occurred with
A4 and A4a genotypes in 80% of corals sampled on carbonate rock, and
40% on igneous rock. These new ITS-2 sequences appeared to be rare in
all investigated samples, except for three corals from carbonate rocks,
in which sequences A4.1 and A4a.1 dominated (Table 5). The unrooted
phylogenetic representation of ITS-2 Symbiodinium sequences from
both the present study and Genbank, shows that the 'A4-cluster' is well
separated from other clade A representatives, with 7 and 11 base-pair
differences from A1 and A3b, respectively (Fig. 6). As many as 96% of
the 105 Symbiodinium sequences from P. astreoides on igneous rocks
matched either A4 or A4a sequences, whereas for P. astreoides on
carbonate rock, only 61% (n = 65 sequences) of the 107 sequences
matched A4 or A4a; the remaining 42 sequences matched one of the
4 other sequences (A4.1, A4.2, A4.3, or A4a.1). The GenBank
24
Table 4
A comparison of the parameters describing the best-t curves applied to the rETR versus PFD results for Porites astreoides on carbonate and igneous rock at 5-m depth (see Fig. 4 for a
graphical display of the results). Either a three-parameter, non-linear function with two exponentials that incorporated photoinhibition (9 corals), or the same function simplied by
excluding photoinhibition (6 corals), was tted depending on whether photoinhibition was observed. = the slope of the initial portion of the curve, = the slope of the
photoinhibition component (when observed), rETRmax = the maximum rate of photosynthesis, Po = Y intercept of the best-t curve, and e = electrons. F, df, and p display the results
of one-way ANOVAs comparing the parameters between each substratum.
Parameter
Carbonate rock
Igneous rock
mol e s 1[mol photons m 2 s 1] 1)

mol e s 1[mol photons m 2 s 1] 1)
rETRmax mol e s 1)
Po mol e s 1)
0.71 0.02
0.10 0.04
143.8 13.0
0.49 1.86
0.62 0.09
0.39 0.19
101.3 14.1
1.11 2.78
(9)
(5)
(9)
(9)
accession numbers for each Symbiodinium ITS-2 sequences used in

this study were: A1 (AF333505), A4.1 (FN429760), A4.2 (FN429761),
A4.3 (FN429763), A4a.1 (FN429762), A1a (EU449030), A3 (AF333507),
A3b (EU449043), A4 (AF333509), A4a (AF499778), A5 (AF333508), A6
(AF186058), A7 (AY239360), A8 (AY258468), A9 (EU449028), A10
(EU792882), A11 (EU449041), A12 (EU792883), A13 (AF333504),
A15ab (EU792884EU792886), A15c (EU792887), A16 (EU792888).
The AMOVA showed that a signicant portion of the genetic
variance (Pvar = 6.78%, p b 0.05) was found between rock types, with
most of the remaining variance (Pvar = 93.22%, p b 0.01) within these
groups (Table 6). Therefore, substratum type inuenced the associ-
(6)
(4)
(6)
(6)
df
1.10
4.23
4.67
0.04
1,13
1,7
1,13
1,13
0.31
0.08
0.05
0.85
ation of Porites astreoides with either specic and/or different

proportions of Symbiodinium ITS-2 sequence compositions. Corals
from carbonate rock consistently harbored a greater number of ITS-2
sequences than those from igneous rocks (Table 6, Fig. 6). For
example, 2 to 5 co-occurring sequences were found in corals from
carbonate surfaces, but only 1 to 3 (with A4 and A4a co-occurring in
the majority of these cases) in corals from igneous surfaces. In
contrast to the strong substratum effect on the genetic diversity of
Symbiodinium ITS-2 sequences, the AMOVA revealed that only 1.9%
of the genetic variance was associated with the two sites, regardless of
the substrate types. Therefore, P. astreoides harbors a similar diversity
of Symbiodinium ITS-2 sequences at Donkey Bite and Tektite. Exact
tests conrmed the results of the AMOVA for both contrasts: (i) a
signicant proportion of the genetic variance was explained by rock
types (12.14%, p b 0.1), and (ii) only 2.6% of the genetic variance was
explained by sites (p = 0.08).
4. Discussion
The objective of this study was to evaluate the success of juvenile
corals on a Caribbean reef to test the hypothesis that the substratum
they settle upon affects their performance. The reefs of St. John were
used as a model system because high densities of juvenile corals are
Table 5
Symbiodinium ITS-2 sequence proles identied in juvenile colonies of Porites astreoides
from igneous rock [n = 10 colonies] and carbonate rock [n = 10 colonies] sampled at
two sites (Donkey Bite and Tektite). Frequencies refer to the number of times each
Symbiodinium sequence was recovered from each clone library (i.e., reference number).
Symbiodinium ITS-2 sequences A4.1, A4.2, A4.3, and A4a.1 were deposited in GenBank
(refer to text for accession numbers).
Site
Donkey bite
Substratum
Igneous
Carbonate
Tektite
Fig. 5. Temperature of seawater and the rock substrata during the study. (A) The daily
temperature of igneous rock over one year that began on 1 August 2006 (black line) and
the daily temperature of seawater (gray line). (B) Daily range in temperature (daytime
maximumnighttime minimum) for the three thermal microhabitats studied; means SE
shown, based on 363 replicate days.
Igneous
Carbonate
Reference
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
Frequencies of Symbiodinium ITS-2

rDNA sequences
A4
A4a
A4.1
A4.2
A4.3
A4a.1
6
10
3
2
5
7
6
4
3
6
7
8
6
6
10
8
3
2
4
5
3
3
7
8
4
2
1
5
2
2
4
2
4
3
3
1
1
1
8
8
1
1
1
2
1
Fig. 6. Statistical parsimony network of 21 ITS-2 rDNA sequences in Symbiodinium clade

A, including 6 sequences from the present study (see pie charts and Table 5) and 15
previously published sequences recovered from GenBank. The diameter of pie charts
corresponds to the number of independent coral samples in which a given Symbiodinium ITS-2 sequence was found, the actual number being shown in parenthesis. The
sectors of the pie charts correspond to the proportions of ITS-2 sequences obtained at
each sites and on each substratum (summarized in legend) based on 212 sequences.
common at this location (Edmunds, 2004), and the substratum in

shallow water provides settling sessile taxa with a choice of surfaces
that are either carbonate or igneous rock. These surfaces are relatively
smooth, thereby making it easy to detect small corals and creating a
tractable system for exploring the effect of settlement surfaces on the
success of juvenile corals. While the abundance of carbonate and
igneous rock on the reefs of St. John is unusual compared to
Table 6
Statistical results of the analyses of molecular variance (AMOVA) for Symbiodinium ITS2 sequence proles, taking into account the number of mutations between molecular
haplotypes (Excofer et al., 1992). A hierarchical AMOVA partitions the total variance
into covariance components due to inter-groups (carbonate versus igneous, or Donkey
Bite versus Tektite), intra-groups (20 colonies), and intra-individual (212 ITS-2
sequences) differences. The AMOVA was run on two distinct datasets to test Hypothesis
1, Porites astreoides growing on carbonate and igneous rock have identical symbiont
sequences, and Hypothesis 2, P. astreoides growing at Donkey bite and Tektite have
identical symbionts sequences (refer to test for further details). Var. Comp. = variance
component, Pvar = percentage of variation. Hypothesis 1 is rejected (p b 0.05), and
Hypothesis 2 is accepted (p N 0.05).
Hypothesis Source
1
df
SS
Var. Comp. Pvar
Between rock types

1
5.922 0.040
Among corals within
18 28.991 0.109
rock types
Within coral colonies
192 86.063 0.448
Between sites
1
2.816 0.009
Among corals within sites
18 32.097 0.126
Within coral colonies
192 86.063 0.448
6.78 0.028
18.34 0
74.88
1.86
21.59
76.76
0
0.212
0
0
25
carbonate-dominated reefs in the Florida Keys (Jaap et al., 2008),

Jamaica (Goreau, 1959), numerous Pacic atolls (Riegl et al., 2008)
(and elsewhere), a similar substratum composition is found in other
locations including the Solitary Islands of Australia (Hopley, 2009),
Grenada (PJ Edmunds personal observation), and parts of the
Hawaiian Islands (Fletcher et al., 2008). Together, our results from
St. John reveal that the success of juvenile corals can be affected by the
substratum upon which they grow, with corals on carbonate
compared to igneous rock growing faster over the winter/summer,
maintaining a greater capacity for photophysiological response to
varying light regimes, and supporting a wider diversity of Symbiodinium genotypes. These effects, however, depend on environmental
conditions, with the conditions found during the summer/winter (i.e.,
between August and January) eroding the growth advantages of
settling on carbonate rock. While our results demonstrate that the
settlement surface can affect the performance of juvenile corals,
particularly P. astreoides which was most abundant in our study, the
short-term (i.e., over 6 months) selective value of these effects remain
unresolved as small colonies survive equally well on both rock
surfaces.
Tropical reef corals produce pelagic larvae that exhibit acute
substratum selection (Baird et al., 2003), often favoring crustose
coralline algae for settlement (Harrington et al., 2004). While it is
unclear whether larvae cue to organic materials released by the algae
(Morse et al., 1984), or to microbial ora growing on the surface of
algae (Negri et al., 2001), the evidence is clear that several CCA species
are attractive to coral larvae, with some (such as Titanoderma
prototypum) serving as unusually potent cues (Harrington et al.,
2004). The effects of these biological and chemical cues are
augmented by small-scale topographic complexity (Nozawa, 2008)
and substratum orientation (Rogers et al., 1984), with recruitment
enhanced on rugose surface (Harriott and Fisk, 1987; Nozawa, 2008),
and in cryptic locations in shallow water (Rogers et al., 1984). Against
this backdrop, the shallow fringing reefs of St. John provide an
interesting case where coral recruitment is high (Edmunds, 2004), yet
much of the substratum is relatively smooth igneous rock with a low
cover of CCA (Edmunds, 2002), and a smaller fraction is rugose
carbonate rock formed from dead reef corals, upon which CCA are
common. Even a simple analysis achieved by touching and inspecting
these surfaces suggests that the carbonate rock is characterized by a
rougher and more porous structure (caused by antecedent corallum
features), cooler temperature, more CCA, and paler color than igneous
rock.
In light of the apparent differences between igneous and carbonate
surfaces, and the established settlement preferences of coral planulae,
we suspected that the physical differences between rock surfaces
would have a selective value to coral recruits, and therefore that
juveniles colonies would be more abundant on one of the rock types.
This assertion was not however, supported by the distribution of
juvenile colonies (neither pooled by taxon nor for Porites alone),
which occurred on carbonate and igneous rock simply in proportion
to their abundance. While this outcome is consistent with the
hypothesis that coral larvae do not discriminate between carbonate
and igneous rock at settlement, the focus of our surveys on juvenile
colonies (i.e., 40-mm diameter) leaves open the possibility that one
rock is favored over the other by settling planulae. Conceivably, such
an effect could be evident only in very early life stages (e.g., newly
settled spat) and subsequently might be eroded by post-settlement
events.
Even though the distribution of juvenile corals was statistically
indistinguishable between settlement surfaces, carbonate and igneous rock are functionally unequal with regards to coral growth. The
growth of juvenile corals over the four periods investigated is
comparable to values previously recorded in this location (Edmunds,
2007), although they are lower than many others already in the
literature (e.g., Bak and Engel, 1979), possibly as a result of a decadal-
26
scale decline in the growth of juvenile corals (Edmunds, 2007). As

some of the corals shrank in size over the census periods, especially on
igneous rock between January and August 2008, the mean overall
growth rates ranged from 9.45 mm 6 mo 1 to 11.99 mm 6 mo 1,
which are equivalent to about 18.90 to 23.97 mm y 1. Although
these growth rates were pooled among genera, the similar representation of the most common genera (Porites, Agaricia and Siderastrea)
over each sampling period, and their similar growth rates (Edmunds
2007), makes it unlikely that taxonomic effects confounded the
substratum contrast. However, one consequence of the slow rates of
growth is that the juvenile colonies were probably relatively old (cf.
Bak and Engel, 1979), with an estimated age as high as 713 y
(Edmunds, 2007). This is biologically signicant as it implies that the
temporal scale of this investigation may have been mismatched to the
tempo of events affecting corals on differing substrata. Therefore, the
differences in coral performance did not translate into effects on
survivorship, at least for the size class studied. A study of greater
sampling intervals (e.g., 1 y) would have a greater capacity to test
for substratum-dependent effects on survivorship, particularly if the
sample sizes were sufciently large to employ an analytical tool more
powerful than contingency tables, for example, survivorship analyses
using Cox's Proportional Hazard Model (Cox, 1972). Interestingly, the
absence of a microhabitat effect on the survivorship of juvenile corals
in at least one other study (Edmunds et al., 2004), together with
evidence that the microhabitat (i.e., type of CCA) can have strong
effects on coral spat (Harrington et al., 2004), suggests that the
survivorship consequences of microhabitats may only be expressed in
new coral recruits, rather than larger and older size classes.
Juvenile corals on carbonate rock had a growth advantage over
juvenile corals on igneous rock between January and August, but not
between August and January, and this effect was accentuated in 2008
compared to 2007. These two seasons differ in physical conditions,
with JanuaryAugust characterized by gradually rising seawater
temperatures (0.4 C month 1), routine winter storms, and light
rains (b11 cm month 1), and AugustJanuary characterized by a
period of rapid seawater cooling (0.5 C month 1), heavy rainfall
(up to 16.5 cm month 1) (rainfall data from www.sercc.com/
climate), and occasional intense hurricanes (Lehmiller et al., 1997;
Winter et al., 1998). Together with seasonality in coral biomass and
photophysiological performance (Brown et al., 1999; Fitt et al., 2000;
Warner et al., 2002), a strong thermal dependence of coral
calcication (Jokiel and Coles, 1977) and faster growth in the summer
compared to the winter (Weber et al., 1975, Barnes and Crossland,
1980), it is not surprising that juvenile corals, overall (i.e., pooled
between rock types), grow faster from August to January, than from
January to August. Based on the separate analysis of P. astreoides
growth, which did not reveal an effect of substratum, the effect of
substratum for all juvenile corals is likely to be caused by the other
genera that were common in the present analyses (i.e., Agaricia and
Siderastrea). Presumably, the growth of Agaricia and Siderastrea is
sensitive to the features of carbonate and igneous rock that cause
them to be functionally dissimilar with respect to juvenile coral
success, and if our thermal mechanism is correct (described below)
the sensitivity to temperature of their growth rates may be a
prominent feature of this effect.
It is challenging however, to account for enhanced growth on
carbonate (but not igneous) rock in JanuaryAugust (but not August
January), but this interactive effect may originate in the difference in
the roughness and thermal conductivity of the rocks. For instance, the
rough surface of the carbonate rock, and its occurrence as small
boulders created by the death of corals, might affect turbulence
patterns in the benthic layer (Shashar et al., 1996) and modulate coral
metabolism (Shashar et al., 1993). In the case of turbulence, the
contrast between carbonate and igneous rock may then be more acute
in the winter when storms create strong water motion that facilitates
the formation of small-scale turbulence. The importance of such
turbulence to corals might be further accentuated in the winter,

because at this time of the year, the mass of their tissue is greatly
enlarged (Fitt et al., 2000) to create longer internal diffusion pathways
for the transport of metabolites, and therefore turbulent boundary
layers might be especially important in promoting the exchange of
nutrients between the tissue and the seawater. Alternatively, the high
thermal conductivity of igneous compared to carbonate rocks
(Clauser and Huenges, 1995), and the effect of porosity (which is
high in reef carbonates and reduces thermal conductivity (Clauser and
Huenges, 1995), creates the possibility that warming seawater
between January and August (Fig. 5), interacts with the thermal
characteristics of the rocks to create a subtle effect of temperature that
reduces the growth of juvenile corals on igneous rock.
The feasibility of a thermal mechanism in mediating the growth
of juvenile corals on carbonate and igneous rocks depends on the
sensitivity of their growth to temperature, which is unknown for St.
John, and the thermal microenvironment created in situ on the rocks.
Such a thermal mechanism has a precedent in the marine environment, for in the Gulf of California the post-settlement mortality of
the inter tidal barnacle Chthamalus anisopoma depends on whether it
settles on basalt or granite rock, with the effect possibly related to
differences in temperature of the rock (Raimondi, 1988). Additionally,
on shallow coral reefs, slight differences in the color of corals (much
like those between carbonate and igneous rock) are sufcient to cause
measurable differences of a biologically signicant magnitude in the
temperature of the corals (Fabricius, 2006). More recently, Jimenez
et al. (2008) have shown that the shape of benthic organisms and the
ambient ow regime around them, interacts to create a complex
thermal regime in shallow water, with massive corals up to 0.6 C
warmer than the seawater and embedded in a thermal boundary layer
whose thickness is ow dependent. Our measurements reveal
differences in the thermal environments (i.e., the daily range in
temperature) of carbonate rock, igneous rock, and seawater, but the
magnitude of this variation (Fig. 5) is so small that it is unlikely to
have biologically signicant effects. These minor differences contrast
with the differences in temperature that we detected simply by
touching the surface of carbonate and igneous rock, and we suspect
that the discrepancy is a result of the resolution of the tools we
employed, and their deployment in holes drilled 2 cm into the rock. It
is likely that further application of more sophisticated tools (e.g.,
Fabricius, 2006; Jimenez et al. 2008) for measuring the temperature of
the surfaces of substrata on coral reefs might prove valuable in
determining why juvenile corals perform in dissimilar ways on
different rocks.
Further insights into how the substratum might affect juvenile
corals were provided by the analysis of photophysiological performance in juvenile P. astreoides. These analyses demonstrated that
PSII did not vary between corals on carbonate and igneous rock in
winter or summer, but that the maximum rate of photosynthesis (as
assessed by rETR through the use of RLCs) was reduced 30% on
igneous rock in the summer (RLCs were not determined in the
winter). We limited this portion of the study to P. astreoides, as
juveniles of this species are common on both rock types in St. John,
and it provides an unusual example of a coral that is currently
increasing in abundance both locally (PJ Edmunds unpublished data)
and regionally (Green et al. 2008). Thus, juvenile P. astreoides are
representative of the contemporary juvenile coral community, and
the results from this species have broader value when set against the
current success of P. astreoides in the Caribbean. The analytical tools
selected for these contrasts address different aspects of the photobiology of the Symbiodinium within P. astreoides. PSII assesses the light
harvesting efciency of PSII under a light-adapted state (Genty et al.,
1989), and RLCs characterize the relationship between photosynthesis and light, with photosynthesis assessed as rETR (Ralph and
Gademann, 2005). Importantly, RLCs describe the ways in which a
light-adapted plants responds to differing irradiances (Ralph et al.,
1999), and evaluate the physiological exibility with which they

respond to changing light, although they do not describe a fully
equilibrated response (Ralph and Gademann, 2005). As eldwork for
the present study progressed, RLCs were employed when it became
clear that PSII alone was insufcient to fully explore the effect of
substratum on juvenile corals.
The ve sets of measurements of PSII, that were completed over
5 y demonstrate that this parameter differs among years and seasons
(August versus January), but was unaffected by the substratum. PSII
is strongly affected by the preceding light history (Maxwell and
Johnson, 2000), which probably explains why it differs among the
four Augusts between 2003 and 2006, and also exhibits seasonality
(Ulstrup et al., 2008), which is consistent with the variation observed
between August 2006 and January 2007. To accommodate the
sensitivity of PSII to preceding illumination (Maxwell and Johnson,
2000), our measurements of PSII were completed between 12:00 and
13:00 h on clear and sunny days. The preliminary analysis, which
demonstrated that PSII did not vary among such days within a
month, makes it unlikely that the results for this variable were biased
by dissimilar daily light histories. Therefore, the measurements of
PSII demonstrate that under constant midday irradiances (i.e., when
photosynthesis has fully equilibrated to these conditions), there are
no photophysiological implications for juvenile P. astreoides of
growing on carbonate or igneous rock. Thus, the lack of a substratum
effect on PSII of P. astreoides is consistent with the growth results for
this species (described above), although this outcome does not imply
that the functional relationship between these processes is anything
but complex (Allemand et al. 2004). Indeed, since growth for all the
juvenile corals combined varied between carbonate and igneous rock,
it would be interesting to test the hypothesis that such effects are
associated with substratum effects on the photophysiology of other
coral taxa.
When detected through the use of RLCs, depressed rates of
maximum photosynthesis at high light intensities are indicative of
down-regulation of photosynthesis (Ralph and Gademann, 2005;
Ralph et al., 2002), and the process is interpreted as dynamic and
protective (Demmig-Adams and Adams, 1992). We suspect these
differences were detected with RLCs rather than with the initial
measurement of PSII under ambient light conditions, because RLCs
include irradiances that are greater than those typically observed at
the study depth (5 m). Presumably, these higher irradiances, together
with properties of the rock substratum (described below), led to
substratum-dependent differences in PSII and, therefore, rETR
(which = PSII x PAR). These changes in PSII are not the same as a
reduction in photosynthesis as a result of non-photosynthetic
quenching, as these pathways require more time to activate than is
usually provided during RLC analyses (Ralph and Gademann, 2005).
Thus it is reasonable to infer for P. astreoides, that corals on carbonate
rock have a greater capacity than those on igneous rock to
accommodate in benecial ways a range of light intensities up to
1644 mol photons m 2 s 1, but have a reduced need for short-term
protection of the photophysiological machinery. These effects are
illustrated by the high rETR on carbonate rock, with the absence of
substratum effects on the parameter of the response curves
suggesting that the differences between surfaces is not related to
photoacclimation (sensu Falkowski and Dubinsky, 1981). In fact, a
measurable photoacclimatory response between adjacent corals at
the same depth, but on carbonate and igneous rock, is unlikely given
the identical down-welling irradiance that such corals would receive.
As irradiance regimes are similar on each rock at a single depth with a
common orientation, the putative protective value of down-regulating photosynthesis on igneous rock is likely to be in response to a
factor other than light. Although the present study cannot resolve this
effect, it is tempting to speculate that it is related to the thermal
regime of igneous versus carbonate rock. For tropical reefs corals, high
temperature is well known for its harmful effects (Jokiel, 2004) and its
27
positive synergy with high light intensities in causing damage to

photosynthesis (Jones et al., 1998). Perhaps the ability to down
regulate photosynthesis at high irradiances is particularly important
for corals on igneous rock on summer days when bright days coincide
with calm water and high temperatures and creates the potential for
photophysiological damage. In light of the difference in rETRmax
between rocks for P. astreoides, it initially is surprising that this does
not translate into differences in growth. However, the relationship
between photosynthesis and growth (calcication) is complex and
poorly understood (Allemand et al. 2004), and since it is likely to be
mediated by HCO
3 , which mechanistically is distant from the
processes occurring in PSII (which dictate the values of rETR), there
are numerous biochemical reactions that could result in a real (or
apparent) decoupling between rETRmax and growth.
In the nal part of the study, we examined Symbiodinium ITS-2
sequence diversity in juvenile P. astreoides from carbonate and
igneous rock, and completed the analyses in two near-by locations
to broaden the generality of these specic ndings. The objective was
to determine whether substratum-dependent variation in juvenile
corals could be attributed to genetic differences in their Symbiodinium
ITS-2 sequence composition, and the study was completed with the
premise that P. astreoides is an effective model for other juvenile
corals. Of the 20 samples of P. astreoides analyzed, all contained
Symbiodinium sequences A4, A4a and/or a number of closely related
variants (Table 5; Fig 6). All corals contained A4, and 80% contained
A4a, suggesting that these are paralogous loci (A4 and A4a). This was
expected given that A4a is the most common Symbiodinium sequence
in P. astreoides based on ITS2-DGGE surveys (Warner et al. 2006;
Banaszak et al., 2006; Thornhill et al., 2006). We also uncovered
Symbiodinium sequences A4.1, A4.2, A4.3, and A4a.1 in 8, 3, 4, and 3
coral colonies, respectively, and most of these were collected from
carbonate surfaces. The general topology was identical to a previously
published analysis of clade A sequences (LaJeunesse et al., 2008), and
clearly showed that the sequences recovered in our study were either
identical to the dominant sequences A4 and A4a, or were closely
related to them. Whether these sequences represent distinct Symbiodinium species, distinct populations of a single species, or
intragenomic variants within a single species or group of species
remains an unresolved issue (Apprill and Gates, 2007; Thornhill et al.,
2007; Correa and Baker, 2009; Sampayo et al., 2009; Stat et al. 2009).
Nevertheless, the statistical analyses clearly show that corals growing
on carbonate rock contained a higher number and a greater
proportion of co-occurring ITS-2 sequences than corals on igneous
rocks, a pattern consistent for both sampling sites.
The differences in Symbiodinium sequence proles between corals
on carbonate and igneous rock might explain in part, why aspects of
the photophysiology of P. astreoides differ between the rock surfaces.
For instance, Symbiodinium ITS-2 sequences A4 and A4a within P.
astreoides have previously been shown to have higher photosynthetic
efciencies (as assessed by Fv/Fm and PSII) than Symbiodinium in
other corals, and are more resistant to photodamage when exposed to
temperature stress (Warner et al., 2006). Since these are the nearexclusive forms found in P. astreoides on igneous rock, whereas
colonies from carbonate rock harbor a wider diversity of Symbiodinium, perhaps this pattern is reective of a slightly more challenging
physical environment on the igneous rock as a result of subtle thermal
effects as described above. Investigations of Symbiodinium phenotypes are still in their infancy, but there is evidence of physiological
differences among genetically distinct Symbiodinium that map onto
with ecological patterns, such as the vertical distribution of the hosts,
or the specicity of the host-Symbiodinium association (e.g., IglesiasPrieto et al., 2004; Warner et al., 2006). However, the function of ITS-2
sequences does not necessarily correspond to photobiological traits,
at least when they are analyzed outside of their host environment
(Hennige et al., 2009). Resolving the causes and consequences of
genetic variation in the Symbiodinium harbored within reef corals is
28
widely recognized as a research priority in order to better understand

how reef corals might respond to global climate change (Stat et al.,
2006). However, as the present study illustrates, there are also basic
aspects of coral ecology that will benet from a clearer understanding
of the functional signicance of genetic diversity within the Symbiodinium communities of individual coral species. Signicant scientic
discoveries often have their origins in the synthesis of multiple studies
of limited scope, and resolution of the role of Symbiodinium diversity
in the response of corals to climate change may turn out to have roots
in the study of its utility in discrete ecological niches.
Acknowledgements
This research was supported by the University of Puerto Rico, Sea
Grant Program (R-101-1-06), the US National Science Foundation
(DEB 03-43570, DEB 08-51441, and OCE 04-17412 to PJE and OCE 0752604 to RDG), California State University, Northridge (CSUN), the
Swiss National Science Foundation (PBGEA-115118 to XP), and the
School of Ocean and Earth Science and Technology at the University of
Hawai'i. Coral sampling was completed under permits issued by the
Virgin Islands National Park (VIIS-2006-SCI-0011 and VIIS-2006-SCI0012). We thank K. Marsaglia for geological advice, N. Formel for
assistance with the winter sampling, C. Didden, W. Goldenheim, H.
Putnam, M. Maheigan, and N. Colvard for assistance with summer
sampling, M. Ehinger and C. Bird for statistical advice, and the staff at
the Virgin Islands Ecological Resource Station for making our visits
productive and enjoyable. Comments from R. Carpenter and M. Steele
improved an earlier draft of this paper. This research would not have
been possible without scuba infrastructure made available by S.
Prosterman, and logistical support by V. Powell. This is contribution
number 158 of the marine biology program of CSUN and HIMB
contribution number 1380. [SS]
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Journal of Experimental Marine Biology and Ecology: Daniel H. Green, Peter J. Edmunds, Xavier Pochon, Ruth D. Gates

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Journal of Experimental Marine Biology and Ecology: Daniel H. Green, Peter J. Edmunds, Xavier Pochon, Ruth D. Gates

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Journal of Experimental Marine Biology and Ecology 384 (2010) 1829

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Journal of Experimental Marine Biology and Ecology

The effects of substratum type on the growth, mortality, and photophysiology of

different CCAs offering cues of varying strength (Harrington et al.,

contains several Symbiodinium ITS-2 sequences, including A4, A4a, B1,

2.2. Relative abundance of rock surfaces and distribution of juvenile

2.3. Growth and mortality

Growth rates were compared between substratum types (xed

treatments on the capacity to utilize a range of light intensities for

where P is the rate of photosynthesis (i.e., rETR), Po is the intercept of

seawater using a two-way ANOVA with thermal microenvironment

did not differ signicantly from the number expected based on

Fig. 3. Light-adapted photosynthetic quantum yield (PSII) of juvenile Porites astreoides

increasing rapidly with irradiance to 500700 mol photons m 2 s 1.

(A) Among years

(B) Between seasons

generally greater in spring (e.g., April, with values of 0.520.54 C)

mol e s 1[mol photons m 2 s 1] 1)

accession numbers for each Symbiodinium ITS-2 sequences used in

ation of Porites astreoides with either specic and/or different

Frequencies of Symbiodinium ITS-2

Fig. 6. Statistical parsimony network of 21 ITS-2 rDNA sequences in Symbiodinium clade

common at this location (Edmunds, 2004), and the substratum in

Var. Comp. Pvar

Between rock types

carbonate-dominated reefs in the Florida Keys (Jaap et al., 2008),

scale decline in the growth of juvenile corals (Edmunds, 2007). As

turbulence to corals might be further accentuated in the winter,

1999), and evaluate the physiological exibility with which they

positive synergy with high light intensities in causing damage to

widely recognized as a research priority in order to better understand

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