Journal of Human Evolution 48 (2005) 219e236

Africas wild C4 plant foods and possible

early hominid diets
Charles R. Petersa, John C. Vogelb,)
a

Anthropology Department and Institute of Ecology, Baldwin Hall, University of Georgia, Athens, Georgia 30602-1619, USA
b
477 Kay Ave, Menlopark, Pretoria 0081, South Africa
Received 31 December 2003; accepted 16 November 2004

Abstract
A small minority of Africas wild plant foods are C4. These are primarily the seeds of some of the C4 grasses, the
rootstocks and stem/leaf bases of some of the C4 sedges (especially papyrus), and the leaves of some of the C4
herbaceous dicots (forbs). These wild food plants are commonly found in disturbed ground and wetlands (particularly
the grasses and sedges). Multiple lines of evidence indicate that C4 grasses were present in Africa by at least the late
Miocene. It is a reasonable hypothesis that the prehistory of the C4 sedges parallels that of the C4 grasses, but the C4
forbs may not have become common until the late Pleistocene. CAM plants may have a more ancient history, but oer
few opportunities for an additional C4-like dietary signal. The environmental reconstructions available for the early
South African hominid sites do not indicate the presence of large wetlands, and therefore probably the absence of
a strong potential for a C4 plant food diet. However, carbon isotope analyses of tooth enamel from three species of
early South African hominids have shown that there was a signicant but not dominant contribution of C4 biomass in
their diets. Since it appears unlikely that this C4 component could have come predominantly from C4 plant foods,
a broad range of potential animal contributors is briey considered, namely invertebrates, reptiles, birds, and small
mammals. It is concluded that the similar average C4 dietary intake seen in the three South African hominid species
could have been acquired by diering contributions from the various sources, without the need to assume scavenging or
hunting of medium to large grazing ungulates. Eectively similar dominantly dryland paleo-environments may also be
part of the explanation. Theoretically, elsewhere in southern and eastern Africa, large wetlands would have oered early
hominids greater opportunities for a C4 plant diet.
2005 Elsevier Ltd. All rights reserved.
Keywords: Carbon isotopes; Paleodiet; C4 forbs; C4 sedges; C4 grasses; CAM plants; Ecology; Papyrus; Paleoanthropology

) Corresponding author.
E-mail address: chaspete@uga.edu (C.R. Peters).
0047-2484/$ - see front matter 2005 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jhevol.2004.11.003

220

C.R. Peters, J.C. Vogel / Journal of Human Evolution 48 (2005) 219e236

Introduction
The two Australopithecus species that were
recovered from cave breccias in the Transvaal,
South Africa, before and immediately following
World War II were thought to have had dierent
diets. Paranthropus robustus, with its massive jaws
and large molars, was considered to have been predominantly a vegetarian, while Australopithecus
africanus, with its more humanlike dentition, was
thought to have been omnivorous, and perhaps
included a fair amount of esh in its diet
(Robinson, 1954). The demonstration that carbon
isotope studies on the bones of prehistoric humans
indicates aspects of their diet (Vogel and van der
Merwe, 1977) opened up the possibility of
throwing some light on the diet of the early
hominids. The technique is based on the fact that
the tissue of plants that utilize the four carbon
mode of photosynthesis (C4 plants) has a relatively
high content of the rare stable carbon isotope 13C,
which uniquely distinguishes these plants from
those using the more common three carbon
photosynthetic pathway (C3 plants). Furthermore
the isotopic signal is passed on to the animals that
feed on these plants (Vogel, 1978).
The application of photosynthetic systems in
the African context results from the nding that,
although woody plants are typically C3, the vast
majority (O95%) of grass species in the savannas
and bushvelds of the warm summer rainfall
regions of southern Africa are C4 plants (Vogel
et al., 1978; Ellis et al., 1980). This also has been
found to be the case in eastern Africa (Cerling
et al., 1997). As a consequence, in these regions, the
bones of grazers, such as the zebra and wildebeest,
have a carbon isotope composition that clearly
distinguishes them from browsers, such as the
girae and kudu (Vogel, 1978; Ambrose, 1986), as
well as from predominantly vegetarian omnivores
like the chacma baboon (Lee-Thorp et al., 1989).
The isotopic values found in carnivores that prey
on ungulates show the relative amount of C4
grazers in their diet (Lee-Thorp et al., 1989).
The early hominids that have thus far been
investigated are from southern Africa. They show
13
C values intermediate between that of a C3 and C4
diet, which has been interpreted as indicating the

consumption of C4 grass eating vertebrates and/or

insects (Lee-Thorp and van der Merwe, 1993; LeeThorp et al., 1994; Sponheimer and Lee-Thorp,
1999; Lee-Thorp, 2000). Van der Merwe and
Tschauner (1999: 514) concluded that the isotopic
evidence suggests that meat, whether scavenged or
hunted, was an important element in the diets of all
hominid species after 3 Ma. The question arises,
however, whether C4 plants may have contributed
to the diet of these early hominids. Previously, these
plants have not been considered systematically.
The present analysis of wild edible plants intends to
provide a preliminary assessment of this possibility.
It also leads us into a discussion of some of the
limitations and issues involved in the isotope
approach to evaluating early hominid diets.

Methods
Evaluation of the plausibility of a C4 plant food
diet for early hominids requires a broad perspective on the taxonomy and ecology of C4 plants.
Our approach was initially the dicult one of
reviewing an extensive but often unsystematic
literature on the identication of C4 species. That
approach was problematic because of limitations
in available listings, screening methods, and
taxonomy. However, a comprehensive review of
the higher taxonomic distribution of C4 photosynthesis then became available (Sage et al., 1999).
This encouraged us to start again, with a more
general taxonomic perspective.
The rst step in the analysis presented here is
a brief overview of the worlds C4 families, along
with descriptive statistics on the number of C4
genera found in those families. This step is
important for clarifying the limitations of the
analysis as applied to African plants. Not all of the
species in the C4 genera identied by Sage et al.
(1999) have been screened for photosynthetic
pathway, and the unvouchered botanical status
of many screenings results in additional uncertainties, but the general patterns at the generic level are
strong enough to permit a preliminary application
of the analysis to African plant taxa. Where the
genera appear to be exclusively C4, the untested
African species are treated here as probably C4.

C.R. Peters, J.C. Vogel / Journal of Human Evolution 48 (2005) 219e236

The second step is identication of the C4

genera that are also recorded as providing native
wild plant foods in sub-Saharan Africa. The most
comprehensive compilation of the wild food
plants, including updated taxonomy, is Peters
et al. (1992). For this work, the data base has
been supplemented as additional information has
become available. The emphasis of this compilation is on eastern and southern Africa, but tropical
western Africa is also included. The extensive
nature of the composite compilation also helps in
developing a perspective on the C4 vs. C3 plant diet
comparison.
The third step is identifying likely plant parts
for a potential African C4 wild plant food diet.
Our analysis is based on human usage (as opposed
to that of other primates) because of the catholic
plant usage in this extant hominid, coverage of the
types of environments thought to have been
occupied by early hominids, conrmatory redundancy across many of the records, and the
relatively sound taxonomic status of the corrected
data base. This approach also allows us to focus
with some condence on the most common plant
parts that might be eaten, since our theoretical
question is not about rare acts of consumption,
but rather, regular acts that would be detectable
isotopically in small samples of early hominid
fossils. Other researchers may expand this analysis
using the plant food lists of other primates,
possibly the chimpanzee and baboon for example
(cf. Peters and OBrien, 1981), assuming the
taxonomy of the plant food species has been
checked and updated (cf. Peters et al., 1992). Most
of the wild plant parts eaten by humans may be
consumed raw, but exceptions are noted by
information on special processing and records in
the literature on poisonous plants (e.g., Watt and
Breyer-Brandwijk, 1962; Verdcourt and Trump,
1969; Storrs and Piearce, 1982; Van Wyk et al.,
2002).

Results
The C4 syndrome is apparently restricted to the
owering plants, or angiosperms (Sage et al.,
1999), the dominant class among the seed plants.

221

It is known to occur in a small minority, only 18

(Sage et al., 1999), of the worlds approximately
405 angiosperm families (Mabberley, 1998). In
each of these 18 families, C4 genera are also
a minority (Table 1).
The worlds 18 C4 families are broadly represented in sub-Saharan Africa, but, in some cases,
none of their C4 genera are represented in Africas
wild food plants (Table 1). In other cases, the C4
genera are present in Africa but the species of food
plants recorded there are C3, not C4. For the
dicots, 8 families and 12 genera provide C4
candidates for sub-Saharan Africa (Table 1). In
a few additional cases, the photosynthetic status of
the African food species remains uncertain: the C4
genera contain both C3 and C4 species, and, with
the exception of a few cosmopolitan weeds (e.g.,
species, occurring broadly in the Old World
tropics), the African taxa have not been tested.
Our analysis focuses on the 12 dicot genera known
to have at least one C4 species recognized to be an
African wild food plant. For these genera and
species, there is a consistent pattern in the plant
parts reportedly eaten. Eleven of these 12 genera
(Table 1) provide a potherb, leaf, or vegetable
(sometimes whole plant). In some cases, the leaves
are reportedly eaten raw (Portulaca), while others
are reportedly boiled with multiple changes of
water to remove a bitter taste (Cleome: Pooley,
1998; Maundu et al., 1999). The next most cited
dicot plant part is seed, representing two of the 12
genera.
For the monocots, two families, Cyperaceae
(the sedges) and Poaceae (the grasses), provide
African wild plant foods. Here the photosynthetic
assignment of the genera is usually well attested.
Together, the Cyperaceae and Poaceae account for
nearly 80% of all C4 species worldwide (Sage et al.,
1999), and the African taxa are relatively well
studied.
For the Cyperaceae, the genus Cyperus contributes most of the African wild food plants that are
sedges. The giant sedge, Cyperus papyrus, with its
edible rhizome, base of the new aerial shoot, and
mature culm base (Peters, 1999), is the most well
known species, and, after some initial false-starts
(Moss et al., 1969; Tregunna et al., 1970), is now
recognized as a C4 plant (Krenzer et al., 1975;

Table 1
Worldwide occurrence of C4 photosynthesis in angiosperm families and C4 genera from those families also represented in the wild food
plants of sub-Saharan Africa and plant parts eaten for probable C4 species1
Angiosperm
subclass

Dicotyledones

Family (C4 genera/total

number of genera in
family worldwide)

C4 genus also recorded in the wild

food plants of Africa (estimated, or
observed [*], number of C4 species
in genus worldwide: for genera
with known C3 species/total
number of species in the genus)

Plant parts eaten in African species

that are probably C4, and three
additional cases where C4 status
remains uncertain, i.e., may be C3
(number of such species currently
on record)

Acanthaceae (1/250)
Aizoaceae (5/126)

Blepharis (80)
Gisekia (5)
Sesuvium (1*/12)
Trianthema (17)
Zaleya (6)
Achyranthes (1/7)
Aerva (1*/10)
Amaranthus (60)
Celosia (1*/45)
None
Heliotropium (6*/250)
Cleome (2*/150)

Seed (1)
Leaf (1)
Potherb (1; may be C3)
Leaf (1)
Vegetable (1)
--Potherb (1)
Leaf (4)
----Fruit:berry (2; may be C3)
Potherb (1)

None
None; note: Chenopodium is C3
Euphorbia (250/1500)

----Gum, leaf, rootstock

(3; may be C3)
Leaf, twigs (1)
Seed, leaf, root (2)
--Leaf (2)
--Vegetable, leaf, ower (2)
Seed (1)
Rootstocks, stem base, leaf base (7)
Stem base (1)
--Seed (9)
Seed (2)
Seed (1)
Seed (2)
Seed (4)
Seed (4)
Seed (6)
Seed (1)
Rhizome (1)
Seed (1)
Seed (1)
Rhizome (1)
Seed (8)
Seed (1)
Seed, young leaf (2)
Seed (1)
Seed (2)
Seed (5)
Seed (1)
Leaf (1)
Seed (2)

Amaranthaceae (11/74)

Asteraceae - Compositae - (8/1500)

Boraginaceae (1/120)
Capparidaceae Capparaceae - (1/34)
Caryophyllaceae (1/88)
Chenopodiaceae (ca. 45/105)
Euphorbiaceae (1/300)
Mollugineceae (2/14)
Nyctaginaceae (3/33)
Polygonaceae (1/45)
Portulacaceae (2/20)
Scrophulariaceae (1/280)
Zygophyllaceae (3/30)
Monocotyledones

Cyperaceae (28/131)
Hydrocharitaceae (1/16)
Poaceae - Gramineae (372/ca. 800)

Mollugo (3*/35)
Boerhavia (2*/20)
None
Portulaca (40)
None
Tribulus (25)
Zygophyllum (1*/80)
Cyperus (ca. 500/650)
Mariscus (200)
None
Brachiaria (ca. 100)
Cenchrus (22)
Cynodon (10)
Dactyloctenium (13)
Digitaria (ca. 220)
Echinochloa (ca. 35)
Eragrostis (ca. 350)
Eriochloa (ca. 30)
Imperata (8)
Leptochloa (27)
Leptothrium (2)
Miscanthus (ca. 20)
Panicum (ca. 260/370)
Paspalum (ca. 320)
Pennisetum (80)
Rottboellia (4)
Setaria (ca. 110)
Sporobolus (ca. 160)
Stipagrostis (50)
Themeda (18)
Urochloa (ca. 120)

Collated from Sage et al., 1999 (and personal communications) and Peters et al., 1992, with some additions and corrections.

223

C.R. Peters, J.C. Vogel / Journal of Human Evolution 48 (2005) 219e236

Jones and Milburn, 1978; Hesla et al., 1982). At

the other end of the size spectrum, three of the
widespread dwarf sedges with edible tubers or
subterranean bulbs (Peters, 1994) are also reported
to be C4 taxa (Cyperus esculentus, C. rotundus, and
C. usitatus; Hesla et al., 1982). Other C4 sedge
species may provide additional cases of edible
stem/leaf bases and rootstocks, but lack of reports
and personal observations (CRP) suggest the
possibilities are rather limited. There are other
C4 Cyperus species that provide morsels to eat,
including the following: C. articulatus, new roots
and the culm base of the young aerial shoot (both
somewhat astringent); C. dives (syn. C. immensus)
and C. longus, base of the young leaf and the base
of the young culm. The new growth of papyrus
roots also provides additional morsels, available at
the edge of oating vegetation along channels or
sudd. None of these can be expected to provide
more than a very minor supplement for all but the
most specialized plant food diet.
In the African Poaceae, 18 of the 21 wild food
genera recognized in Table 1 provide seed. This is
sometimes a famine food when domestic crops fail.
Two of the 21 genera are reported to provide
edible rhizomes; they can be eaten raw (Peters,
1999). Two of the genera are reported to have

leaves that are eaten. Grass leaves are rarely

recorded as eaten by humans, even as famine food.
Ecology of Africas wild C4 food plants
Composite sketches of the probable ecology of
the three main sets of African wild C4 food plants
can be synthesized from the literature cited in
Peters et al. (1992) and the following sources: for
dicots, Jerey (1961), Verdcourt (1961), Heine
(1963), Elers et al. (1964), Nabil El Hadidi
(1985), Townsend (1985), Agnew and Agnew
(1994), Whitehouse (1996), Pooley (1998), and
Maundu et al. (1999); for sedges, Peters (1994) and
Peters (1999); for grasses, Clayton (1972), Clayton
et al. (1974), Clayton and Renvoize (1982), and
Gibbs Russell et al. (1991).
Leaf dicots
The dicot taxa that might contribute leaves to a
C4 diet are forbs, prostrate annuals to semi-woody
shrublets. For the most part, they are wide-ranging
in their geographic and elevational distributions
(Table 2). The common ones are weeds (mostly
annuals), occupying disturbed areas in a variety of
habitats, and on a variety of soil types (often
sandy). Along paths, near homes, and in cultivated

Table 2
Common ecological characteristics of Africas wild C4 plant food genera: dicot leaf taxa and grass seed taxa (cf. Table 1)1
Angiosperm
subclass

Geographic distribution

Elevation

General habitat

Edaphic moisture regime

Leaf-food dicot
genera (10)

10 genera have one or more

food species that occur in
both eastern and southern
Africa. Many taxa extend
beyond Africa

Seed-food grass
genera (18)

15 genera have one or more

food species that occur in
both eastern and southern
Africa. Many taxa extend
beyond Africa

9 genera have one or

more food species that
occur from the coast
to 1000 m elevation or
more. Only a few taxa
are found above
2000 m
15 genera have one or
more food species that
occur from the coast
to 1000 m elevation or
more. Only a few taxa
are found above
3000 m

10 genera have one or

more weedy food species.
Generally, the natural
associations are those of
grassland, and open areas
in bushland and
woodland
14 genera have one or
more weedy food species.
The associations are
mostly those of open
habitats, but light shade
and marshland settings
are also reported. Soils
sandy or clay

5 genera have one or more

food species that are found
in seasonal wetlands. Status
of other genera unclear,
e.g., Portulaca. Some taxa
appear limited to dry
(sandy) sites
13 genera have one or more
food species that are found
in seasonal wetlands. Few
taxa appear limited to dry
(sandy) sites

1
Synthesized from: dicots, Jerey, 1961; Verdcourt, 1961; Heine, 1963; Elers et al., 1964; Nabil El Hadidi, 1985; Townsend, 1985;
Agnew and Agnew, 1994; Whitehouse, 1996; Pooley, 1998; Maundu et al., 1999; grasses, Clayton, 1972; Clayton et al., 1974; Clayton
and Renvoize, 1982; Gibbs Russell et al., 1991; plus references cited in Peters et al., 1992.

224

C.R. Peters, J.C. Vogel / Journal of Human Evolution 48 (2005) 219e236

elds, they can be found in grassland (heavily

grazed sites), openings in woodland, and at the
edge of forest. Although some information is
lacking, common sites also include seasonal wetlands (Table 2), ranging from places with temporary pools of water in what are otherwise drier
environments, to stream sides and oodplains. A
reconstruction of their natural place in relatively
productive settings would probably include disturbed ground at the edges of seasonal wetlands.
Perennially well-drained sites would likely be less
productive, except in higher rainfall areas. The
seasonal pattern would probably be fast vegetative
growth early in both subtropical summer rain and
bimodal tropical rain climates, a rain-green type of
plant response.
Rootstock sedges
The three dwarf sedges that might contribute
rootstocks to a C4 diet are stoloniferous perennials. Cyperus esculentus and C. rotundus are well
known weeds of cultivated ground, especially
irrigated lands. They are wide-ranging in their
geographic and elevational distributions. The third
dwarf sedge considered here, Cyperus usitatus, is
limited to eastern and southern Africa, but covers
a broad range of elevations (up to ca. 2500 m). In
nature, all three species are locally abundant on
seasonally inundated ground (clay and sand),
especially lake fringes and edge of river oodplains. In amplied contrast, the giant sedge,
Cyperus papyrus, is found in continuously inundated sites. Broadly distributed in Africa, over
a range of elevations from near sea level to ca.
2000 m, this freshwater sedge can not compete
with the large grasses on sites subject to seasonal
drought. The other Cyperus species mentioned,
C. articulatus, C. dives, and C. longus, are robust
perennials widespread in African wetlands, with
C. longus apparently tolerant of sites subject to
seasonal drought.
Seed grasses
The grass taxa that might contribute seeds to
a C4 diet are herbs, tufted annuals to spongy
oating or reedlike perennials. Most of them are
broad ranging in their geographic and elevational
distributions (Table 2). The common ones are

usually weeds (sometimes perennials) and/or include seasonal wetlands in their habitat associations. Echinochloa is characterized by freshwater
hydrophytes and marsh grasses on clay soils.
Eragrostis can be locally common on moist sandy
soils. Panicum and Sporobolus are found on
a variety of soil types, but generally prefer damp
situations. Limited but similar information on
many of the genera suggest a reconstruction of
relatively high natural productivity on seasonally
(briey) inundated disturbed ground, e.g., well
grazed pasture at the edge of wetlands. The
seasonal pattern would probably be vigorous
vegetative growth early in the rains, followed by
setting of seed before loss of soil moisture. As the
spiklets begin to dry out they easily shatter and the
seed is dispersed. This may occur while the ground
is still wet. Intensive grazing by a variety of
herbivores may follow, rst on the sandy, then
clay, soils as the ground dries out. Dry season
disturbance may also occur, e.g., warthogs digging
for grass rhizomes.
C4 plant food values and deleterious side eects
The fresh young leaves of the edible forbs are
good sources of moisture, minerals, and vitamins
(sometimes including vitamin C), but because of
their high water content, they provide very limited
amounts of carbohydrate and protein, and almost
no fat (Wehmeyer, 1986; Maundu et al., 1999).
The fresh tubers, bulbs, and rhizomes of Cyperus
are primarily sources of moisture and carbohydrate (Wehmeyer, 1986; Peters, 1999). Fresh grass
seed is a source of minerals and some vitamins,
and is high in carbohydrate, but intermediate in
protein (which may not be balanced in amino
acids; Ward, 1971), and low in fat (Wehmeyer,
1986; Maundu et al., 1999).
Potential deleterious side eects from ingestion
include digestion inhibition (dicult to evaluate)
and toxicity (relatively easy to document). Very
few of these plants can be expected to be
poisonous, although many (if not most) have been
used as medicinals (Watt and Breyer-Brandwijk,
1962). Those that have been reported as poisonous
are forbs and grasses that develop toxic principles
(especially hydrocyanic acid) under conditions of

C.R. Peters, J.C. Vogel / Journal of Human Evolution 48 (2005) 219e236

wilting, and grasses infested with ergot (Watt and

Breyer-Brandwijk, 1962; Verdcourt and Trump,
1969). The dwarf sedges are also problematic. It is
unlikely that the mature tubers of Cyperus
rotundus are edible. They become woody, taste
like turpentine, and are said to contain toxins
(Peters, 1994). Cyperus esculentus and C. usitatus,
on the other hand, are said to be constipating if
eaten in excess (Jacot Guillarmod, 1971). Perhaps
only a handful of these small tubers or bulbs can
be eaten at one time.

The African C3 wild food plant comparison

Before an overall judgment about the plausibility of a C4 plant food diet can be made, a general
comparison with the potential C3 plant food diet is
needed. This is crucial for contextualization.
The vast majority of Africas wild food plants
are C3. These plants provide the wild plant food
diets characteristically consumed by the higher
primates, including humans. There are 145 families
(33 monocot, 112 dicot) and several hundred wild
African species known to have been utilized by
humans (Peters et al., 1992).
The wild C3 food plants of Africa provide food
types both similar to and dierent from the C4
food plants. Similar food types include leaves,
rootstocks, and a variety of seeds provided by C3
herbaceous and woody plants. In both growth
form and habitat distribution, these plants are not
as restricted as those of the C4 syndrome. Some are
found in the same general habitats as members of
the C4 group, e.g., seasonal and perennial shallow
freshwater wetlands. Others are common where C4
plants are not, e.g., riverine forest and woodland.
The wild C3 food plants also provide food types
not occurring in the potential C4 African plant
food diet. Some of these may be of minor
signicance, e.g., nectar, gum, mushrooms. Others
are clearly very important. Notably signicant are
the eshy fruits and nutlike oil seeds that
constitute important core staples in the potential
wild plant food diet of sub-humid and semi-arid
Africa. The fruits are provided by numerous trees
and shrubs covering a variety of habitats (e.g.,
Peters et al., 1984; Peters and OBrien, 1994). They

225

are good sources of carbohydrates (sugars),

minerals, and vitamins. The proteinaceous nutlike
oil seeds are a special category of staples. In
woodland savanna plant species, the nutlike seeds
are part of an edible fruit, often a keystone fruit
species for a variety of mammals (Peters, 1993).
The nutlike seeds are rich in fat and protein, and
an additional source of minerals and vitamins. For
early hominids, they could have provided supplementary nutrients needed to put on fat reserves
seasonally (Peters, 1987). In terms of landscape, C3
food plants are found almost everywhere. In the
general habitats occupied by C4 food plants, C3
food plants also occur. It is dicult to envisage an
environment with C4 food plants without important C3 food plants nearby. One exception might
be a vast marsh, dominated by papyrus.
We conclude from this analysis that the
hypothesis of a plant food diet for early hominids
with C4 plants contributing the majority of food
intake appears unlikely. The other extreme, the
hypothesis of a plant food diet for all practical
purposes devoid of C4 plants is not as easy to
evaluate. C4 plants could have contributed a secondary or minor amount to an early hominid plant
food diet depending on whether the relevant C4
plant taxa had evolved the C4 syndrome by the
geologic epoch in question, and whether the
hominids exploited the kinds of environments
where those plants are both relatively abundant
and productive.

C4 plant evolution
The earliest unequivocal C4 grass is from the
late middle Miocene (ca. 12.5 Ma) of California
(reviewed by Cerling, 1999). For Africa, the
evidence for C4 grass in the Miocene is indirect.
Stable carbon isotope analyses of East African
paleosol carbonates provide indirect measures of
local C4 biomass (Cerling, 1992). Combined with
carbon isotope analysis of fossil tooth enamel
(Cerling et al., 1997), they have been used to draw
conclusions about changes in the evolution of C4
vegetation in Africa. Isotopic values from paleosol
carbonates sampling the late Miocene to the
terminal Pliocene (from ca. 10 to 1.8 Ma) are

226

C.R. Peters, J.C. Vogel / Journal of Human Evolution 48 (2005) 219e236

interpreted as indicating that C4 plants made up

a signicant portion (but less than 50%) of the
plant biomass. The isotope values for equid and
elephantid fossil tooth enamel change from what
can be interpreted as essentially pure C3 diets to C4
dominated diets between 7 and 8 Ma. It is
a reasonable assumption that this C4 biomass
and these C4 diets were grasses.
There is no paleobotanical evidence for C4
sedges, but it is a reasonable hypothesis that their
prehistory parallels that of the grasses. The long
Niger Delta pollen sequence indicates that sedges
became an important element of the grasslands
and/or freshwater marshes in that region after
ca. 6.6 Ma (Morley, 2000).
There is no paleobotanical evidence for C4
forbs. Molecular studies suggest that some C4
members of the Chenopodiaceae may have their
origins in the Miocene (ca. 11-21 Ma; work in
press previewed by Sage, 2004). Taxomonic and
physiological considerations suggest that C4 dicots
may not have become common until the Pleistocene (Ehleringer et al., 1997).

CAM plants
A further category of plants, those that exhibit
Crassulacean acid metabolism (CAM), also may
have contributed to the C4 dietary intake of the
early hominids. Our review of these plants has
relied primarily on the material in volumes 30 and
114 of the Springer series Ecological Studies,
Analysis and Synthesis (Kluge and Ting, 1978;
Winter and Smith, 1996).
Although CAM is diversely represented among
the vascular plants, most CAM plants are succulent species inhabiting dry regions or tropical
forest epiphytic bromeliads and orchids. A few are
submerged aquatic macrophytes, e.g., Isoetes.
Smith and Winter (1996) provide a list of plant
genera containing species capable of CAM. In
most cases all of the member species have not been
screened, and the CAM status of African species
reported elsewhere as edible usually is not conrmed. African CAM genera with wild edible
species are best considered as possible candidates
for a CAM contribution to early hominid diets.

A number of considerations narrow the eld of

likely candidates for wild African CAM plant
foods. Some of the taxa are only weakly CAM,
very close to normal C3 plants, or facultatively
CAM under conditions of severe drought, so their
C4 carboxylation may make little contribution to
long-term growth and standing biomass. Some of
the species reported to be edible may be toxic
(these normally are cooked), or have toxic
conspecics that are dicult to distinguish in the
wild. This is notably true for CAM dicots. In the
end, only a handful of CAM genera might be
signicant candidates for what would be a minor
contribution to a plant food diet outside of the
Kalahari, the Karroo, and the Cape coastal
region.
The edible corms of the quillwort Isoetes may
oer the possibility of a CAM contribution in
seasonal wetlands. Aloe owers and nectar may
have been exploited in locally dry habitats, such as
sparsely vegetated ridges and rocky hillsides. (Aloe
leaves are reported to be edible, but they are also
used as a purgative.) Among the herbaceous
dicots, Ceropegia, Pelargonium, and perhaps Plectranthus remain as candidates. A number of
Ceropegia species (Asclepiadaceae) have edible
tubers. A number of Pelargonium species (Geraniaceae) have edible leaves, but they can be bitter
and may be eaten only in small amounts.
Plectranthus (Labiatae, nom. alt. Lamiaceae) is
a poorly studied genus with one apparent CAM
species (Kluge and Ting, 1978, their Table 1.2),
and other well known species once broadly
cultivated in west-tropical, eastern, and southern
Africa for their (somewhat bitter) small tubers.
Unfortunately, there is no known fossil record
for CAM (Ehleringer and Monson, 1993; Raven
and Spicer, 1996). Taxonomic distribution does
indicate ancient polyphyletic origins from C3
ancestors.

Assessments of the carbon isotope composition

in fossil hominids and their interpretation
The normal procedure for determining the relative 13C content in animals is to analyze the
organic collagen contained in bone samples. The

227

C.R. Peters, J.C. Vogel / Journal of Human Evolution 48 (2005) 219e236

bone from the early hominid sites has, however,

lost virtually all organic matter and what remains
is the inorganic apatite. While this apatite does
contain some carbonate ions from which the
carbon can be extracted for analysis, it is unsuitable because the porous bone invariably incorporates diagenetic calcium carbonate that usually
cannot be distinguished from the original carbonate. To overcome this problem, the largely
impervious tooth enamel has successfully been
used by Lee-Thorp and co-workers to establish the
C3/C4 status in material from the Transvaal cave
sites of South Africa. The data reviewed here is
taken from the publications of this group. (For
references see Lee-Thorp et al., 2000.)
In Fig. 1, the relative 13C content (expressed as
13
d C values; see gure caption) of tooth enamel of

selected species from three early hominid sites in

South Africa is represented. The isotope data
clearly separate the ungulate taxa into two categories that correspond to the separation of modern
browsers and grazers. The presence of ve species
of grazers with high C4 dietary intakes indicates
that open grassland or bushveld with C4 grasses
existed in the area around Makapansgat at that
time (see environmental reconstructions, below).
The variability of the d13C values in a uniform
group of animals is the result of the following
factors: (1) variations in the 13C content of plants,
(2) the probable averaging of these values by the
animal, (3) the variations in isotope fractionation
during ingestion, (4) the variation caused by
diagenesis, and (5) the accuracy of the isotope
analysis. There are too few analyses of the

50

100%C4

Makapansgat Member 3 (3 Ma)

Browsers
Grazers
Australopithcus africanus
Sterkfontein Member 4 (2.7 Ma)
Parapapio spp.
Swartkrans Member 1 (1.7 Ma)
Browser
Grazer
Papio spp.
Theropithecus sp.
Panthera pardus
Paranthropus robustus
Homo ergaster
-12

-10

-8

-6

-4

-2

Fig. 1. The relative 13C content of tooth enamel of selected species from three early hominid sites in South Africa, expressed as the
parts per thousand (&) deviation from the PDB reference standard. The horizontal bars show the range for each group and the short
vertical lines give the average for each group. The approximate C4 carbon contribution to the diet is indicated on the top of the
diagram. From top to bottom: Makapansgat Member 1. Browsers: the averages and total range of eleven ungulate species, identied
as C3 plant consumers on the basis of the data (n Z 37). Grazers: the averages and range of ve ungulate species classed as C4 plant
consumers, as above (n Z 18). Austalopithecus africanus, four specimens. Sterkfontein Member 4. Parapapio spp., ten specimens
consisting of P. broomi, P. jonesi, P. whitei. Swartkrans Member 1. Browser: ve specimens of Tragelaphus cf. strepsiceros. Grazer:
three specimens of Connochaetes sp. Papio spp., ve specimens of P. robinsoni and three of P. ingens. Theropithecus sp., ve
specimens. Panthera pardus, seven specimens. Paranthopus robustus, six specimens. Homo ergaster, three specimens. Data compiled
from Lee-Thorp et al. (1994, 2000), Sponheimer and Lee-Thorp (1999), Luyt (2001).

228

C.R. Peters, J.C. Vogel / Journal of Human Evolution 48 (2005) 219e236

individual species shown in the gure to provide

meaningful standard deviations. An estimate of
the natural variability can, however, be obtained
from the 37 analyses of those ungulate species
from Makapansgat Member 3 that are identied
as C3 plant browsers. The total range of the values
is 3.6&, which means that the standard deviation
would be about 1&. The 18 analyses of the
ve ungulate species identied as C4 grazers
cluster tightly, except for one outlier value of
d13C Z 4.5&, which is probably because that
animal (Redunca darti) had a substantial intake of
C3 vegetation. The interpretation of the hominid
data is based purely on the dierence between the
values for the contemporary browsers and grazers.
Most of the isotope values for the hominids lie
outside the ranges of the browsers and grazers,
indicating a mixed C3/C4 diet.
The four specimens of Austalopithecus africanus
from Member 3 at Makapansgat (ca. 3.0 myr old)
give an average d13C value that indicates ca. 25%
of their food carbon was of C4 origin (Sponheimer
and Lee-Thorp, 1999). The relatively wide spread
of the individual values suggests that this species
was able to utilize a variety of food sources.
Interestingly, and perhaps surprisingly, the nine
samples of Paranthropus robustus teeth from the
three members at Swartkrans Cave (1.1-1.8 Ma)
give practically the same average 13C content, thus
also indicating a ca. 25% C4 dietary component;
as do the three teeth of Homo ergaster from
Member 1 at Swartkrans, which dates to 1.7 - 1.8
Ma (Lee-Thorp and van der Merwe, 1993; LeeThorp et al., 1994, 2000). Furthermore, the ten
specimens of Parapapio baboons (P. broomi,
P. jonesi, and P. whitei) from Sterkfontein Member
4 (Luyt, 2001) show an average similar to those
of the three hominids, albeit with a considerable
spread in values. On the other hand, the eight
values for Papio baboons (P. robinsoni and
P. ingens) from Swartkrans Member 1 reveal little
evidence of C4, while Theropithecus darti (which is
considered to be ancestral to the geleda baboon
that lives largely on grass in the Ethiopian
highlands) predominantly depended on C4 plants
(presumably grass).
For comparison, the carnivores also need to be
considered. Seven specimens of leopard (Panthera

pardus) from Swartkrans Member 1 have been

analyzed (Lee-Thorp et al., 1994, 2000). The results, also shown in Fig. 1, have a range similar to
that for the hominids. In addition, seven specimens
of hyaenid from the same member at Swartkrans
and a single sample of lion (Panthera leo) from
Member 4 at Sterkfontein (Luyt, 2001) also
give similar values: d13C range 9.2 to 4.8&,
and a value of 7.0&, resectively (not shown in
Fig. 1). All of these results indicate a partial
contribution of C4 grazers to the diet of these
carnivores.
In contrast, two samples of leopard and four
of lion from Member 2 at Swartkrans have
given d13C values of 5.3 and 3.8&, and 3.3
to 0.5&, respectively, indicating very strong to
nearly pure C4 dietary intakes (Lee-Thorp et al.,
1994, 2000). This suggests open grassland hunting
with few browsers available for these felines, so
that a major change in the environment after
Member 1 times can be inferred. The only hominid
fossils that have been reported from Member 2 are
two specimens of P. robustus. They give d13C
values of 10.0 and 8.1& which fall into the
range of those from Member 1. This may be taken
as an indication that the C4 component of their
diet was not derived from the consumption of
ungulate esh.
The similarities seen in d13C values do not
necessarily mean that the dierent species had
similar diets. The dierent ways in which the C4
component might be acquired need to be considered. Earlier studies of dentition and masticatory
features (cited by Lee-Thorp et al., 1994, 2000) did
in fact suggest that the diets of the three hominids
diered. Further possible dietary sources of C4
biomass could come from a variety of animals.
Although often acknowledged, these sources have
not yet been considered systematically.
Alternative sources of C4 carbon for early
hominids diets
Taking a broad perspective, Table 3 suggests
that there are a number of possible sources of C4
carbon for early hominid diets. For the plant
foods, the relatively high productivity of freshwater wetland environments is an important theme.

C.R. Peters, J.C. Vogel / Journal of Human Evolution 48 (2005) 219e236

229

Table 3
Possible C4 foods for early hominid diets1
Lifeform
Plants
C4 sedges

Examples

Notes on potential contribution to a C4 diet

papyrus

perennial marshland rootstock, shoots and culm base: papyrus

potentially the most important C4 plant food species

C4 grasses

seed grasses

rainy season production: especially disturbed ground and

wetland margins; high potential competition

C4 forbs

amaranthus

rainy season production: especially disturbed ground and

seasonal wetland; high potential competition

Animals
C4 plant eating
invertebrates

termites, locusts (earthworms,

millipedes?, land snails?)

wet season swarms (consume both C3 and C4 plant material?)

C4 plant eating reptiles

tortoises

usually eat both C3 and C4 plants

C4 insect eating reptiles

lizards: agamas, skinks (?)

usually eat both C3 and C4 insects

C4 plant and insect eating

birds
C4 plant eating mammals
micromammals

weavers, quelea, bishops (eggs

and nestlings)
grass mice and rats

eat green grass seed plus insects; mass nesting in rainy season

birth peaks (litters) in rainy season

small ungulates

various

usually eat both C3 and C4 plants, depending upon season and

habitat; birth peaks; G mass aggregations

medium to large
ungulates

wildebeest

includes migratory grazers with mass drownings resulting in

low carnivore competition carcass gluts; mass aggregations with
rainy season mass calving

1
Animal notes based on Ward, 1971; Boutton et al., 1983; Senzota, 1983; Alden et al., 1995; Capaldo and Peters, 1995, 1996;
Kingdon, 1997.

Although many other animals would be potential

competitors for the grass seed and forbs, large
areas of papyrus rootstock may not have been
subject to such consumer competition.
Animal sources for the C4 component of an
early hominid diet are theoretically diverse. We
may not have to assume that the early hominids
were hunters with humanlike capabilities. The
possibilities of C4 insects, reptiles, birds, and
rodents recognized in Table 3 are notable because
potential competitors for these foods probably do
not include large (potentially dangerous) mammals. Comparative isotope analyses of food chains
are not available, but the strength of the C4
component in these cases probably depends on
habitat, i.e., the relative dominance of C4 grass
and sedgelands. Again, a gradient of seasonal
freshwater wetlands, or a large tropical wetlands
complex with oodplains and perennial marsh

probably would be the ideal environment for

generating a strong C4 component from most of
these potential dietary sources. We have not been
able to include sh in this analysis because of the
lack of relevant isotope data.
The small ungulates are not a clear case.
Generally they are mixed feeders and many are
predominantly browsers. Among the medium to
large ungulates, however, there are a number of C4
grazers. Prehistorically, some may have had synchronous calving, and some may have seasonally
experienced mass drownings and other calf losses
during migratory crossings of rivers and small lakes.
The possibilities suggested in Table 3 point to
a number of pathways for achieving a partial C4
hominid diet. Without positing special hunting
capabilities, the possibilities of a predominantly
C4 diet would appear to depend on special
combinations of environmental opportunities.

230

C.R. Peters, J.C. Vogel / Journal of Human Evolution 48 (2005) 219e236

Theoretically, the outstanding case would be

a papyrus marsh (a source of wet and dry season
plant food) in a landscape mosaic that included very
large rainy season aggregations of mass nesting
birds and mass calving ungulates with C4 diets.
Environmental reconstructions
and C4 opportunities
Reed (1997) systematically considered the possibility of the presence of wetlands in her
reconstructions of the paleoenvironments surrounding the South African early hominid cave
sites. Her method is based on a combination of
mammalian functional morphology and large
mammal community structure. None of the South
African fossil sites exhibit evidence for extensive
wetlands nearby. For the late Pliocene Makapansgat Valley during Member 3 times (ca. 3 Ma), the
reconstruction includes a stream (fossil Hippopotamus), associated riparian woodland, with wooded
valley sides, and predominantly bushland interuves. In addition, there is evidence for a very
limited amount of wetland in the form of edaphic
grassland. This is based on a small percentage of
the faunal assemblage containing grazers that have
a masticatory morphology similar to modern
grazers (e.g., waterbuck, bualo) that inhabit
(mostly seasonal?) wetlands (see also Sponheimer
et al., 1999). The possible form of these edaphic
grasslands is not discussed, e.g., whether they
might have been on stream banks, small ood
plains, or vleis (dambos).
For the Sterkfontein/Swartkrans valley (Blaaubank River Valley), the reconstructions of Reed
(1997) resulted in a similar conclusion. There is no
evidence for extensive paleo-wetlands associated
with these Plio-Pleistocene sites. The reconstruction for Member 4 at the site of Sterkfontein (ca.
2.6 - 2.8 Ma) is that of an open woodland with
areas of bushland and thicket. Only a small
percentage of the large mammal fauna consists
of wetland grazers. Also, there is evidence for
lianas in the fossil woods from Member 4 of
Sterkfontein (Bamford, 1999), indicating the presence of some mesic closed woodland or gallery
forest. The reconstruction based on the micromammals (Avery, 2001) indicates that there was

grass along the valley streams or river, bush with

grass on the valley hillsides, and grass with some
bush and trees on the surrounding plains.
The reconstructions based on the large mammal
fauna of Members 1-3 at the site of Swartkrans
(Reed, 1997) also indicated that there was very
little wetland in the Blaaubank River Valley in the
early Pleistocene (ca. 1.0 - 1.7 Ma). The reconstructions include a stream or river (fossil hippopotamus, otter, and water mongoose; Watson,
1993), with patches of edaphic grassland (including a vlei-like area and some reed beds; Watson,
1993), plus riparian woodland, with the vegetation
of the surrounding landscape ranging from wooded grassland to open savanna. The reconstruction
based on micromammals (Avery, 2001) is riverine
grass and trees, with grass, bush, and trees evenly
indicated for the hillsides, and grass the main
vegetation (with some bush and trees) on the surrounding plains.
Thus, similar to what we see today, the
Makapansgat and Blaaubank Valleys of the PlioPleistocene were not landscapes that supported
extensive wetlands. It is theoretically doubtful that
the small amount of wetland that probably was
present could have contributed more than a moderate amount to the C4 component of an early
hominid diet. And in fact, for the Member 1
deposits of Swartkrans, strontium isotope analysis
of a portion of the fauna including Paranthropus
and Homo indicates that, with the exception of the
riverine rodent Mystromys, they fed away from the
immediate riverine environs (Sillen et al., 1995,
1998; Lee-Thorp and Sillen, 2001). C4 plant food
opportunities would appear to have been relatively
limited. It is perhaps all the more surprising that
C4 foods contributed ca. 25% to the Paranthropus
diet. C4 seed- and insect-eating birds nesting in
small colonies along the river, but foraging in the
surrounding plains, and C4 grass-eating termites
are perhaps the potential C4 foods that most
readily come to mind for such open veld or
dryland settings. Evidence for the former is lacking
(the family Ploceidae is not in evidence in the
Swartkrans avifauna that has been analyzed;
Watson, 1993), but the possibility of the latter is
oered by the termite foraging hypothesis of
Backwell and dErrico (2001).

C.R. Peters, J.C. Vogel / Journal of Human Evolution 48 (2005) 219e236

Is it possible that Paranthropus was an

opportunistic omnivore?
Omnivores consume both plant and animal
material as food. A remarkable taxonomic variety
of animals are omnivores. Among the birds, the
mainly vegetarian ostrich is an example of an
omnivore that includes insects, small vertebrates,
and animal bones in its diet (Holtzhausen and
Kotze, 1990; Alden et al., 1995). Among the
mammals, examples of omnivores include a variety
of small carnivores, the bushpig, Papio baboons,
and some of the rodents (Kingdon, 1997). Each of
these types of animals has a specialized or well
dierentiated feeding morphology, but also a generalized capability for opportunistic feeding behavior that is well developed in some species.
Omnivory may help to explain some of the
similarity in the average isotope value of the three
South African early hominids. One can easily
hypothesize that early Homo was omnivorous.
Australopithecus africanus has also been hypothesized to have been an omnivore, while Paranthropus robustus and P. boisei have generally been
thought of as vegetarians (complementary reviews
in Grine, 1981, and Peters, 1987). However, there
are theoretical grounds for hypothesizing that
these Paranthropus species may also have been
omnivorous.
Mann (1981) suggested that, by analogy with
the dietary patterns of hunter/gatherers and
chimpanzees, all the early hominids were basically
omnivores, while still accepting the idea that the
specialized masticatory system of Paranthropus
was an adaptation to foods dierent from those
exploited by Australopithecus africanus and early
Homo. Mann (1981) also cautioned that we do not
know the extent to which Paranthropus was a toolmaker, and that the exact nature of their niche(s)
remains unknown. With regard to their potential
niche, Peters (1981) has argued on the basis of
masticatory capability that, if A. africanus was an
omnivore, then Paranthropus was a super-omnivore. Their hypertrophied postcanine teeth and
musculoskeletal masticatory apparatus would
have made them more capable than A. africanus
of orally processing a broad spectrum of foods
that require little incisal or canine preparation. In

231

this light, questions about the evolutionary origins

of the Paranthropus masticatory autopomorphies
should be treated separately from questions about
the potential niche breadth of the animal. Theoretically, the fundamental trophic niche of an
animal includes all that it is biomechanically and
chemically capable of consuming, while its realized
niche is what it actually manages to consume in
real-life situations when the full circumstances of
environmental variables come into play (Hutchinson, 1957). Considering their apparent morphological capabilities and potential geographic range,
it can be argued that Paranthropus probably
practiced a broad-spectrum type of primate diet,
eclectic and opportunistic with a strong tendency
to omnivory (Peters, 1987). This line of reasoning
also theoretically applies to subadult individuals.
The blunt, relatively unworn cusps of the postcanine teeth of young Paranthropus individuals
are, for example, well suited to breaking a variety
of hard seeds and small bones (Peters, 1993;
Lucas and Peters, 2000). The more powerful
jaws of the young Paranthropus, compared with
A. africanus and Homo, might have given them
a weaning advantage in masticating a broader
range of foods (Peters, 1979). At low densities,
early Homo could have geographically overlapped
with Paranthropus, utilizing similar resources processed to diering degrees artifactually. Thus, the
interpretation by Sillen (1992), Lee-Thorp and van
der Merwe (1993), Lee-Thorp et al. (1994, 2000),
and Sponheimer and Lee-Thorp (1999) that the
trace element and isotopic results for Paranthropus
are evidence for omnivory is plausible on theoretical grounds.

Discussion and conclusions

Analysis of Africas edible wild plants indicates
that the leaves of some forbs, the rootstocks and
stem/leaf bases of some sedges, and the seeds of
some grasses are possible candidates for a theoretical early hominid C4 plant food diet. However,
these plant foods are not commonly encountered
or abundant in dryland settings, and a variety of
C3 plants oer alternative sources of nutrition. It is
easier to imagine a hominid diet devoid of C4

232

C.R. Peters, J.C. Vogel / Journal of Human Evolution 48 (2005) 219e236

plants than one dominated by C4 plants. The type

of landscape where wild C4 plant foods would be
relatively abundant is that of a mosaic of extensive
seasonal and perennial shallow-freshwater wetlands. Extensive marshes dominated by the giant
sedge Cyperus papyrus are a special case. Acknowledged as a food source by the ancient
Egyptians, the young shoot and mature culm
bases and heart-of-rhizomes from extensive stands
of papyrus might have provided a dominantly C4
plant food diet. However, reconstructions of the
settings around the South African early hominid
cave sites indicate only limited possibilities for
herbaceous wetlands. These reconstructions do not
suggest extensive wetlands where C4 plants would
have been a major part of the potential dietary
environment. Other parts of southern, southcentral, and eastern Africa, where extensive
freshwater wetlands existed, were probably much
more productive in this regard.
The stable carbon isotope analyses reviewed
here indicate that early South African hominid
diets did have a signicant C4 component. But it
was not dominant. It is estimated to have averaged
ca. 25% for all three hominid species sampled,
Australopithecus africanus, Paranthropus robustus,
and Homo ergaster. Some caution in interpreting
the isotopic data is warranted. The samples are
small and the minimum number of individuals
represented has not been presented in the original
reports. There are dierences in variation across
the species, even with these small samples, that
may be signicant. The samples span unknown
temporal durations, with varying degrees of
contemporaneity among the specimens and species
within a particular deposit.
Keeping these cautionary points and potential
diculties in mind, perhaps the most striking
things about the paleo-isotopic data in Fig. 1 are
that: 1) the overall patterns of herbivory (browser
vs. grazer) and dierent types of carnivore
(leopard vs. lion) meet expectations based on
modern species; and 2) the similarity between the
three species of hominids is unexpected, given
general assumptions that A. africanus was
an omnivore, Paranthropus was a specialized vegetarian, and Homo ergaster, like H. erectus, was
more carnivorous than either Australopithecus or

Paranthropus. The rst increases our condence

that the isotopic approach applied to this fossil
material is sound. The second makes us wonder
what might have gone wrong in the isotope
analysis or in the conceptualization of early hominid ecology. Considering a faulty conceptualization as more likely, one possibility is that we have
not recognized the probable similarities in food
encountered in these South African environments
by the foraging unit of a hominid mother and her
immature ospring, whether Paranthropus or
Homo. All females and all subadults of the South
African early hominids considered here may have
been similar enough in body size and locomotion
to encounter and consume similar foods on their
foraging rounds. Because of similarities in nutritional needs, they may have concentrated their
foraging eorts at these sites on a similar subset of
the rather limited environmental suite(s). This may
help explain apparent similarities in their diet.
Accepting the ca. 25% C4 dietary estimate for
all three hominid species at these sites, some
hypotheses need to be developed as to how that
percentage theoretically could be met. We suggest
that those hypotheses should be framed in a way
that allows for a range of percentages around
a mean value such as 25%, recognizing the
possibility of signicant individual dierences
(see A. africanus in Fig. 1). That framework
should also recognize the possibility of more than
one way of getting to the mean value, so that
hominid population and species dierences might
in principle be accommodated. As a starting point
we can oer the following theoretical formulation
of possibilities for a 30% C4 contribution to
a subadult hominid diet based on minor potential
C4 food categories:
5% C4 input from sedge stem/rootstock, green
grass seed, and forb leaves
5% C4 input from invertebrates
5% C4 input from bird eggs and nestlings
5% C4 input from reptiles and micromammals
5% C4 input from small ungulates
5% C4 input from medium and large ungulates.
This type of formulation maximizes the diversity
of food species, i.e., both food-species-richness

C.R. Peters, J.C. Vogel / Journal of Human Evolution 48 (2005) 219e236

(Table 3) and evenness of contribution. The exact

numbers are not as important as the species
richness of the formulation. Also, the underlying assumptions can be relaxed and explicitly
manipulated in a variety of ways. For example, in
the case of the assumption of limited wetland plant
foods, a question about the possibility of additional sites could be raised, shifting the focus
further out into the surrounding landscape, with
the possibility that, locally, hominid foraging radii
could have extended further than in most of the
other mammals. CAM plants also could have contributed a minor component to the diet, if habitats
or microenvironments of drier aspect were included, and/or if Isoetes were present in seasonal
wetlands. Plausible formulations would, of course,
change dramatically if, for example, a Serengetilike plain or an Upper-Zambezi-like wetland
complex were added to the environmental reconstruction.
The formulation also helps to highlight the
many uncertainties remaining in developing a more
rened interpretation. The C4 status of many of
the food items (see Table 3) remains uncertain.
Their potential availability and annual reliability
remain largely unknown, although most, if not all,
may be predominantly wet season foods.
The place in the formulation where hominid
species dierences perhaps are potentially the
strongest is the C4 component from medium and
large ungulates. This input might be acquired
through hunting or scavenging, but either method
is more likely an adult male rather than subadult
capability, so food sharing is another underlying
assumption. Detailed isotopic study of the full age
range of hominid subadults may help to clarify the
situation, especially the periods of weaning vs.
post-weaning. For the adult, if 25% of the diet
were to be ascribed to the meat of C4 grazers, it
would be reasonable to assume a more or less
equal contribution from C3 browsers, and such
a large dependence (ca. 50%) on meat would be
dicult to accept for any of these early hominids.
We therefore cannot support the conclusion of
Van der Merwe and Tschauner (1999) that the
isotope values suggest that scavenged or hunted
meat was an important element in the diets of all
South African hominid species after 3 Ma. Rather,

233

we favor an interpretation that the C4 component

of the diet of these hominids was made up of
a mixture of the various C4 sources, probably to
varying proportions for the dierent taxa.
When we began this investigation we assumed
that edible wild plants might have contributed
a high proportion of C4 carbon to an early hominid
diet. For the South African sites, this turns out not
to be the case. Carbon isotope dierences between
these hominid species also appear to be minimal.
We conclude that this nding may be the result of
omnivorous behavior on the part of the subadults
of all the hominid species, similar types of (or
limitations in) environmental opportunity, and
a mixture of various C4 sources masking dierences in preferred dietary resources across hominid
taxa.

Acknowledgements
We thank J. M. Maguire for her help in the
initial stage of the project, and R. F. Sage for
assistance with the C4 plant species assignments
and general encouragement, which helped revitalize the project midway. Partial support was
provided by the Anthropology Department, University of Georgia, U.S.A., and the CSIR, South
Africa. M. K. Bamford and M. Murray-Hudson
provided opportunities for observations in the
Okavango Delta, Botswana.
References
Agnew, A.D.Q., Agnew, S., 1994. Upland Kenya Wild Flowers.
East African Natural History Society, Nairobi.
Alden, P.C., Estes, R.D., Schlitter, D., McBride, B., 1995.
National Aubudon Society Field Guide to African Wildlife.
Alfred A. Knopf, New York.
Ambrose, S., 1986. The isotope ecology of East African
mammals. Oecologia 69, 395e406.
Avery, D.M., 2001. The Plio-Pleistocene vegetation and climate
of Sterkfontein and Swartkrans, South Africa, based on
micromammals. J. Hum. Evol. 41, 113e132.
Backwell, L.R., dErrico, F., 2001. Evidence of termite foraging
by Swartkrans early hominids. Proc. Natl. Acad. Sci. 98,
1358e1363.
Bamford, M., 1999. Pliocene fossil wood from an early hominid
cave deposit, Sterkfontein, South Africa. S. Afr. J. Sci. 95,
231e237.

234

C.R. Peters, J.C. Vogel / Journal of Human Evolution 48 (2005) 219e236

Boutton, T.W., Arshad, M.A., Tieszen, L.L., 1983. Stable

isotope analysis of termite food habits in East African
grasslands. Oecologia 59, 1e6.
Capaldo, S.D., Peters, C.R., 1995. Skeletal inventories from
wildebeest drownings at Lakes Masek and Ndutu in the
Serengeti ecosystem of Tanzania. J. Archaeol. Sci. 22,
385e408.
Capaldo, S.D., Peters, C.R., 1996. Observations of wildebeest
Connochaetes taurinus (Artiodactyla, Bovidae) crossing
Lake Masek (Serengeti ecosystem, Tanzania), including
one small drowning. Mammalia 60, 303e306.
Cerling, T.E., 1992. Development of grasslands and savannas in
East Africa during the Neogene. Palaeogeogr., Palaeoclimatol., Palaeoecol. 97, 241e247.
Cerling, T.E., 1999. Paleorecords of C4 plants and ecosystems.
In: Sage, R.F., Monson, R.K. (Eds.), C4 Plant Biology.
Academic Press, London, pp. 445e469.
Cerling, T.E., Harris, J.M., MacFadden, B.J., Leakey, M.G.,
Quade, J., Eisenmann, V., Ehleringer, J.R., 1997. Global
vegetation change through the Miocene/Pliocene boundary.
Nature 389, 153e158.
Clayton, W.D., 1972. Gramineae. Flora West Trop. Afr. 3,
349e574.
Clayton, W.D., Renvoize, S.A., 1982. Gramineae (Part 3).
Flora of Tropical East Africa. A.A. Balkema, Rotterdam.
Clayton, W.D., Phillips, S.M., Renvoize, S.A., 1974. Gramineae (Part 2). Flora of Tropical East Africa. Crown Agents
for Oversea Governments and Administrations, London.
Ehleringer, J.R., Monson, R.K., 1993. Evolutionary and
ecological aspects of photosynthetic pathway variation.
Ann. Rev. Ecol. Syst. 24, 411e439.
Ehleringer, J.R., Cerling, T.E., Helliker, B.R., 1997. C4
photosynthesis, atmospheric CO2, and climate. Oecologia
112, 285e299.
Elers, L., Graham, R.A., DeWolf, G.P., 1964. Capparidaceae.
Flora of Tropical East Africa. Crown Agents for Oversea
Governments and Administrations, London.
Ellis, R.P., Vogel, J.C., Fuls, A., 1980. Photosynthetic pathways and the geographical distribution of grasses in south
west Africa/Namibia. S. Afr. J. Sci. 76, 307e314.
Gibbs Russell, G.E., Watson, L., Koekemoer, M., Smook, L.,
Barker, N.P., Anderson, H.M., Dallwitz, M.J., 1991. Grasses
of Southern Africa. National Botanical Institute, Pretoria.
Grine, F.E., 1981. Trophic dierences between gracile and
robust australopithecines: a scanning electron microscope
analysis of occlusal events. S. Afr. J. Sci. 77, 203e230.
Heine, H., 1963. Acanthaceae. Flora West Trop. Afr. 2,
391e432.
Hesla, B.I., Tieszen, L.L., Imbamba, S.K., 1982. A systematic
survey of C3 and C4 photosynthesis in the Cyperaceae of
Kenya, East Africa. Photosynthetica 16, 196e205.
Holtzhausen, A., Kotze, M., 1990. The Ostrich. C.P. Nel
Museum, Oudtshoorn (S.A.).
Hutchinson, G.E., 1957. Concluding remarks. Cold Spring
Harb. Symp. Quant. Biol. 22, 415e427.
Jacot Guillarmod, A., 1971. Flora of Lesotho. J. Cramer,
Lehre, Germany.

Jerey, C., 1961. Aizoaceae. Flora of Tropical East Africa.

Crown Agents for Oversea Governments and Administrations, London.
Jones, M.B., Milburn, T.R., 1978. Photosynthesis in papyrus
(Cyperus papyrus L.). Photosynthetica 12, 197e199.
Kingdon, J., 1997. The Kingdon Field Guide to African
Mammals. Academic Press, London.
Kluge, M., Ting, I.P., 1978. Crassulacean Acid Metabolism:
Analysis of an Ecological Adaptation. Springer-Verlag,
Berlin.
Krenzer, E.G., Moss, D.N., Crookston, R.K., 1975. Carbon
dioxide compensation points of owering plants. Plant
Physiol. 56, 194e206.
Lee-Thorp, J.A., 2000. Preservation of biogenic carbon isotopic
signals in Plio-Pleistocene bone and tooth mineral. In:
Ambrose, S.H., Katzenberg, M.A. (Eds.), Biogeochemical
Approaches to Paleodietary Analysis. Kluwer Academic/
Plenum Press, New York, pp. 89e115.
Lee-Thorp, J.A., Sillen, A., 2001. Chemical signals in fossils
oer new opportunities for assessing and comparing dietary
niches of South African hominids. In: Tobias, P.V., Raath,
M.A., Moggi-Cecchi, J., Doyle, G.A. (Eds.), Humanity
from African Naissance to Coming Millennia: Colloquia in
Human Biology and Palaeoanthropology. Firenze University Press, Firenze (Italy), pp. 321e325.
Lee-Thorp, J.A., van der Merwe, N.J., 1993. Stable carbon
isotope studies of Swartkrans fossils. In: Brain, C.K. (Ed.),
Swartkrans: A Caves Chronicle of Early Man. Transvaal
Museum Monograph No. 8, Pretoria, pp. 251e256.
Lee-Thorp, J.A., Thackeray, J.F., van der Merwe, N.J., 2000.
The hunters and the hunted revisited. J. Hum. Evol. 39,
565e576.
Lee-Thorp, J.A., van der Merwe, N.J., Brain, C.K., 1989.
Isotopic evidence for dietary dierences between two
baboon species from Swartkrans. J. Hum. Evol. 18,
183e190.
Lee-Thorp, J.A., van der Merwe, N.J., Brain, C.K., 1994. Diet
of Australopithecus robustus at Swartkrans from stable
carbon isotope analysis. J. Hum. Evol. 27, 361e372.
Lucas, P.W., Peters, C.R., 2000. Function of postcanine tooth
crown shape in mammals. In: Teaford, M.F., Meredith
Smith, M., Ferguson, M.W.J. (Eds.), Development, Function and Evolution of Teeth. Cambridge University Press,
Cambridge, pp. 282e289.
Luyt, J., 2001. Revisiting the palaeoenvironments of the South
African hominid bearing Plio-Pleistocene sites: new isotope
evidence from Sterkfontein. M.A. Thesis, University of
Capetown.
Mabberley, D.J., 1998. The Plant Book. Cambridge University
Press, Cambridge.
Mann, A.E., 1981. Diet and human evolution. In: Harding,
R.S.O., Teleki, G. (Eds.), Omnivorous Primates: Gathering
and Hunting in Human Evolution. Columbia University
Press, New York, pp. 10e36.
Maundu, P., Ngugi, G.W., Kabuye, C.H.S., 1999. Traditional
Food Plants of Kenya. National Museums of Kenya,
Nairobi.

C.R. Peters, J.C. Vogel / Journal of Human Evolution 48 (2005) 219e236

Morley, R.J., 2000. Origin and Evolution of Tropical Rain
Forests. John Wiley & Sons, New York.
Moss, D.N., Krenzer, E.G., Brun, W.A., 1969. Carbon dioxide
compensation points in related plant species. Science 164,
187e188.
Nabil El Hadidi, M., 1985. Zygophyllaceae. Flora of Tropical
East Africa. A.A. Balkema, Rotterdam.
Peters, C.R., 1979. Toward an ecological model of African PlioPleistocene hominid adaptations. Am. Anthropol. 81,
261e278.
Peters, C.R., 1981. Robust vs. gracile early hominid masticatory
capabilities: the advantages of the megadonts. In: Mai, L.L.,
Shahklin, E., Sussman, R.W. (Eds.), The Perception of
Evolution: Essays Honoring Joseph B. Birdsell. Anthropology UCLA, vol. 7. Department of Anthropology,
University of California at Los Angeles, pp. 161e181.
Peters, C.R., 1987. Nut-like oil seeds: food for monkeys,
chimpanzees, humans, and probably ape-men. Am. J. Phys.
Anthropol. 73, 333e363.
Peters, C.R., 1993. Shell strength and primate seed predation of
nontoxic species in eastern and southern Africa. Int. J.
Primatol. 14, 315e344.
Peters, C.R., 1994. African wild plants with rootstocks reported
to be eaten raw: the monocotyledons, part III. In: Seyani,
J.H., Chikuni, A.C. (Eds.), Proceedings of the XIIIth
Plenary Meeting of AETFAT, Zomba, Malawi, 2-11 April
1991. National Herbarium and Botanic Gardens of Malawi,
Zomba, pp. 25e38.
Peters, C.R., 1999. African wild plants with rootstocks reported
to be eaten raw: the monocotyledons, part IV. In: Timberlake,
J., Kativu, S. (Eds.), African Plants: Biodiversity, Taxonomy
and Uses. Royal Botanic Gardens, Kew, pp. 483e503.
Peters, C.R., OBrien, E.M., 1981. The early hominid plantfood niche: insights from an analysis of plant exploitation
by Homo, Pan, and Papio in eastern and southern Africa.
Curr. Anthropol. 22, 127e140.
Peters, C.R., OBrien, E.M., 1994. Potential hominid plant foods
from woody species in semi-arid vs. sub-humid subtropical
Africa. In: Chivers, D.J., Langer, P. (Eds.), The Digestive
System in Mammals: Food, Form and Function. Cambridge
University Press, Cambridge, pp. 166e192.
Peters, C.R., OBrien, E.M., Box, E.O., 1984. Plant types and
seasonality of wild-plant foods, Tanzania to southwestern
Africa: resources for models of the natural environment.
J. Hum. Evol. 13, 397e414.
Peters, C.R., OBrien, E.M., Drummond, R.B., 1992. Edible Wild
Plants of Subsaharan Africa. Royal Botanic Gardens, Kew.
Pooley, E., 1998. A Field Guide to Wild Flowers of KwazuluNatal and the Eastern Region. Natal Flora Publication
Trust, Durban.
Raven, J.A., Spicer, R.A., 1996. The evolution of Crassulacean
Acid Metabolism. In: Winter, K., Smith, J.A.C. (Eds.),
Crassulacean Acid Metabolism: Biochemistry, Ecophysiology and Evolution. Springer-Verlag, Berlin, pp. 360e385.
Reed, K.E., 1997. Early hominid evolution and ecological
change through the African Plio-Pleistocene. J. Hum. Evol.
32, 289e322.

235

Robinson, J.T., 1954. Prehominid dentition and human

evolution. Evolution 8, 324e334.
Sage, R.F., 2004. The evolution of C4 photosynthesis. New
Phytol. 161, 341e370.
Sage, R.F., Li, M., Monson, R.K., 1999. The taxonomic
distribution of C4 photosynthesis. In: Sage, R.F., Monson,
R.K. (Eds.), C4 Plant Biology. Academic Press, New York,
pp. 551e584.
Senzota, R.B.M., 1983. A case of rodent-ungulate resource
partitioning. J. Mammal. 64, 326e329.
Sillen, A., 1992. Strontium-calcium ratios (Sr/Ca) of Australopithecus robustus and associated fauna from Swartkrans.
J. Hum. Evol. 23, 495e516.
Sillen, A., Hall, G., Armstrong, R., 1995. Strontium calcium
ratios (Sr/Ca) and strontium isotope ratios (87Sr/86Sr) of
Australopithecus robustus and Homo sp. from Swartkrans.
J. Hum. Evol. 28, 277e285.
Sillen, A., Hall, G., Richardson, S., Armstrong, R., 1998.
87
Sr/86Sr in modern and fossil foodwebs of the Sterkfontein
Valley: implications for early hominid habitat preference.
Geochim. et Cosmochim. Acta 62, 2463e2473.
Smith, J.A.C., Winter, K., 1996. Taxonomic distribution of
Crassulacean Acid Metabolism. In: Winter, K., Smith,
J.A.C. (Eds.), Crassulacean Acid Metabolism: Biochemistry, Ecophysiology and Evolution. Springer-Verlag, Berlin,
pp. 427e436.
Sponheimer, M., Lee-Thorp, J.A., 1999. Isotopic evidence for
the diet of an early hominid, Australopithecus africanus.
Science 283, 368e370.
Sponheimer, M., Reed, K.E., Lee-Thorp, J.A., 1999. Combining isotope and ecomorphological data to rene bovid
paleodietary reconstruction: a case study from the Makapansgat Limeworks hominid locality. J. Hum. Evol. 36,
705e718.
Storrs, A.E.G., Piearce, G.D., 1982. Dont Eat These: A Guide
to Some Local Poisonous Plants. Forest Department,
Ndola, Zambia.
Townsend, C.C., 1985. Amaranthaceae. Flora of Tropical East
Africa. A.A. Balkema, Rotterdam.
Tregunna, E.B., Smith, B.N., Berry, J.A., Downton, W.J.S.,
1970. Some methods for studying the photosynthetic
taxonomy of the angiosperms. Canadian Journal of Botany
48, 1209e1214.
Van der Merwe, N.J., Tschauner, H., 1999. C4 plants and the
development of human societies. In: Sage, R.F., Monson,
R.K. (Eds.), C4 Plant Biology. Academic Press, London,
pp. 509e549.
Van Wyk, B., van Heerden, F., van Oudtshoorn, B., 2002.
Poisonous Plants of South Africa. Briza, Pretoria.
Verdcourt, B., 1961. Boraginaceae. Flora of Tropical East
Africa. A.A. Balkema, Rotterdam.
Verdcourt, B., Trump, E.C., 1969. Common Poisonus Plants of
East Africa. Collins, London.
Vogel, J.C., 1978. Isotopic assessment of the dietary habits of
ungulates. S. Afr. J. Sci. 74, 298e301.
Vogel, J.C., Fuls, A., Ellis, R.P., 1978. The distribution of
Kranz grasses in South Africa. S. Afr. J. Sci. 74, 209e215.

236

C.R. Peters, J.C. Vogel / Journal of Human Evolution 48 (2005) 219e236

Vogel, J.C., van der Merwe, N., 1977. Isotopic evidence for
early maize cultivation in New York State. Am. Antiq. 42,
237e241.
Ward, P., 1971. The migration patterns of Quelea quelea in
Africa. Ibis 113, 275e297.
Watson, V., 1993. Composition of the Swartkrans
bone accumulations, in terms of skeletal parts and
animals represented. In: Brain, C.K. (Ed.), Swartkrans:
A Caves Chronicle of Early Man. Transvaal Museum
Monograph No. 8. Transvaal Museum, Pretoria, pp.
35e73.

Watt, J.M., Breyer-Brandwijk, M.G., 1962. The Medicinal and

Poisonous Plants of Southern and Eastern Africa. E. &
S. Livingstone Ltd, Edinburgh.
Wehmeyer, A.S., 1986. Edible Wild Plants of Southern Africa:
Data on the Nutrient Contents of Over 300 Species.
National Food Research Institute, CSIR, Pretoria.
Whitehouse, C., 1996. Nyctaginaceae. Flora of Tropical East
Africa. A.A. Balkema, Rotterdam.
Winter, K., Smith, J.A.C. (Eds.), 1996. Crassulacean Acid
Metabolism: Biochemistry, Ecophysiology and Evolution.
Springer-Verlag, Berlin.