The document summarizes a study that analyzed the carbon isotope ratios in tooth enamel from 10 specimens of Australopithecus africanus from Sterkfontein in South Africa, dating to between 2.5-2.0 million years ago. The results show that A. africanus had a varied diet incorporating both C3 forest foods and C4 savanna foods to a greater degree than other early hominins. This suggests A. africanus was a highly adaptable and opportunistic feeder. The isotope data also indicates the individuals exhibited more dietary variation than other early hominin species, arguing against suggestions that multiple species are represented in the A. africanus taxon.

1. Journal of Human Evolution 44 (2003) 581–597
The carbon isotope ecology and diet of Australopithecus
africanus at Sterkfontein, South Africa
Nikolaas J. van der Merwe a,b*, J. Francis Thackeray c, Julia A. Lee-Thorp a,
Julie Luyt a
a
Archaeometry Research Unit, Department of Archaeology, University of Cape Town, 7701 Rondebosch, South Africa
b
Departments of Anthropology and Earth and Planetary Sciences, Harvard University, Cambridge, MA, USA
c
Department of Palaeontology, Transvaal Museum, Pretoria, South Africa
Received 23 October 2001; accepted 10 March 2003
Abstract
The stable carbon isotope ratio of fossil tooth enamel carbonate is determined by the photosynthetic systems of
plants at the base of the animal’s foodweb. In subtropical Africa, grasses and many sedges have C4 photosynthesis and
transmit their characteristically enriched 13C/12C ratios (more positive 13C values) along the foodchain to consumers.
We report here a carbon isotope study of ten specimens of Australopithecus africanus from Member 4, Sterkfontein
(ca. 2.5 to 2.0 Ma), compared with other fossil mammals from the same deposit. This is the most extensive isotopic
study of an early hominin species that has been achieved so far. The results show that this hominin was intensively
engaged with the savanna foodweb and that the dietary variation between individuals was more pronounced than for
any other early hominin or non-human primate species on record. Suggestions that more than one species have been
incuded in this taxon are not supported by the isotopic evidence. We conclude that Australopithecus africanus was
highly opportunistic and adaptable in its feeding habits.
2003 Elsevier Science Ltd. All rights reserved.
Keywords: Australopithecines; South Africa; Carbon isotopes; Diet; C4 plants
Introduction How and why did tree-climbing apes with diets of
forest plants evolve into bipedal savanna foragers
Hypotheses about the behavioural ecology of with omnivorous diets?
early hominins play a critical role in scenarios that Since the description of the Taung specimen by
seek to explain the evolution of humans from apes. Raymond Dart (1925), hypotheses about the
dietary behaviour of Australopithecus africanus
* Corresponding author. University of Cape Town, have been varied and contradictory. Dart (1925,
Archaeometry Research Unit, Department of Archaeology,
Rondebosch, 7701 South Africa
1926) suggested that the australopithecine diet
E-mail address: nikolaas@science.uct.ac.za (N.J. van der included various insects, rodents, eggs, and
Merwe). small antelopes. He based his suggestion on
0047-2484/03/$ - see front matter 2003 Elsevier Science Ltd. All rights reserved.
doi:10.1016/S0047-2484(03)00050-2

2. 582 N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597
environmental reconstructions available at the in Ethiopia (White et al., 1994, 2000), Kenya
time, to the effect that the climate of South Africa (Leakey et al., 2001; Pickford and Senut, 2001),
had not changed significantly during the Plio- Chad (Brunet et al., 1995), and at Sterkfontein
Pleistocene. In later years, of course, Dart (1957) (Stw 573, “Little Foot”) (Clarke, 1998, 2002b).
described A. africanus as a homicidal hunter with The East African and Sahelian hominins are said
an osteodontokeratic culture. This idea was laid to have lived in forested environments and Little
to rest by Brain (1981), who demonstrated that Foot has been described as a tree-climber who
the australopithecines were victims rather than lived in an environment that included (sub)tropical
aggressors. vines (Bamford, 1999). The latest turn in the story,
Nearly fifty years ago, John Robinson (1954) then, seems to be “back to the forest” and it has
presented a “dietary hypothesis”, in terms of which been suggested that the “savanna hypothesis”
he described A. africanus from Sterkfontein as an should be discarded.
omnivore and A. (Paranthropus) robustus from What do we actually know about the diets of
nearby Swartkrans (which he thought to be co- early hominins at about 2 Ma? Direct evidence is
eval) as a specialised herbivore. A. robustus was exceedingly scarce. Cutmarks on bones have been
subsequently shown to post-date A. africanus and recorded at a number of sites and recent evidence
to have co-existed with Homo sp. at Swartkrans suggests that one or more hominins at Swartkrans
(Brain, 1958, 1981). The designation of A. robustus and Drimolen in South Africa used bone tools to
as a specialised herbivore has persisted, however, crack open termite mounds (Backwell and
and a common perception has emerged that the d’Errico, 2000). The preponderence of A. robustus
omnivory of A. africanus was continued into the fossils at both these sites provides a basis for
Homo lineage. On the other hand, dental micros- suggesting that the robust australopithecine was
copy studies have suggested that A. africanus the termite-forager, but Homo sp. was also present
might have been largely a fruit and leaf eater here. The idea that A. robustus was a generalised
(Grine, 1981; Grine and Kay, 1988). feeder and perhaps an omnivore is given further
The publication of Robinson’s dietary hypoth- credence by the evidence from stable carbon iso-
esis nearly coincided with Mary Leakey’s 1959 topes (Lee-Thorp et al., 1994, 2000). Both A.
discovery at Olduvai of A. (Zinjanthropus) boisei, robustus and Homo sp. from Swartkrans had diets
a robust australopithecine (Leakey, 1959). For a of which about 25%, on average, was derived from
while, “Zinj” disrupted the hominin story line, C4 plants (savanna grasses or C4 sedges) and/or
because it was thought to be older than all of the their consumers (insects, reptiles, mammals). This
South African hominins and to have been the does not mean that they had identical diets, but the
producer of Oldowan stone tools. When “pre- carbon isotope data constrain the range of possi-
Zinj” was discovered at Olduvai in due course bilities of what their diets could have been. The C4
(Leakey et al., 1964), interest shifted to Homo component specifically excludes plants from
habilis as the meat-eating, toolmaking omnivore canopy forests, i.e., foods from open environments
and A. boisei was relegated to the same specialised are implied by the isotopic data. Carbon isotope
herbivorous niche as its South African counter- data are also available for four specimens of A.
part, A. robustus. The story regained its symmetry africanus from Makapansgat. This hominin had
with the discovery of A. afarensis (Johanson and C4-based foods in its diet as well, but the amounts
White, 1979), a possible East African precursor of varied from near 0 to 50% among the four
both H. habilis and A. boisei. The “forest to individuals (Sponheimer and Lee-Thorp, 1999a).
savanna” theme for the critical juncture in human These data are considered in detail below.
evolution endured as a result and was given an Obviously, at some point, hominins came to
environmental backdrop by Yves Coppens (1983, consume a greater component of food from the
1994) with his “East Side Story”. savannas, specifically animal food. The “expensive
Hominins older than A. africanus and A. afa- tissue hypothesis” of Aiello and Wheeler (1995)
rensis have been discovered during the last decade holds that increases in brain size would have

3. N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597 583
Fig. 1. 13C values of tooth enamel of Australopithecus africanus and associated fauna from Sterkfontein, Member 4. In the
box-and-whisker plots, the vertical centre line depicts the mean, the black box depicts 25%–75% of the range and the whiskers denote
10%–90% of the range.
required an increasing amount of high-nutrient ago (Broom and Schepers, 1946; Broom et al.,
animal foods, since the gut became smaller as the 1950; Vrba, 1976, 1982, 1995; Partridge 2000;
brain became larger. This progression of omnivory Partridge et al., 2000a,b); these have yielded more
in the course of encephalisation can be investigated than 500 fossil specimens of hominins, ranging
by means of isotopic dietary chemistry. from individual teeth and small skeletal elements
We have studied in some detail the carbon to complete crania (Kuman, 1994; Kuman and
isotope ecology of A. africanus at Sterkfontein and Clarke, 2000; Clarke and Kuman, 1998, 2000). A
have obtained carbon isotope ratios for the tooth recent discovery (Clarke, 1998) is a nearly com-
enamel of ten hominin specimens from Member 4. plete skeleton of an australopithecine (Stw 573)
This is the largest number of specimens of an early that lived more than 3 million years ago, but
hominin species that has been isotopically ana- excavation of this find is still in progress (Clarke,
lysed so far. The results reported here (Table 2, 2002b).
Fig. 2) show that A. africanus was an unusual Most of the hominin discoveries at Sterkfontein
generalised feeder. have come from Member 4, which consists of a
fossiliferous breccia that formed as a talus infill
inside a dolomite solution cavity. The infill was
Background to Sterkfontein hominins subsequently cemented by carbonates from the
percolating ground water. The ages of Member 4
Sterkfontein has hominin-bearing deposits that and other deposits at Sterkfontein are notably dif-
span the period of about 3.5 to 1.5 million years ficult to establish, due to the complex stratigraphy

4. 584 N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597
Fig. 2. 13C values for tooth enamel of hominid and other primate fossils from Sterkfontein Member 4. Specimens of Australopithecus
africanus with asterisks * have been designated by R. Clarke as possible members of a large-toothed, “pre-robust” species different
from A. africanus.
and the absence of volcanic materials that are The faunal assemblage from Sterkfontein
amenable to radiometric dating. Member 4 has Member 4 has been interpreted to suggest that the
been variously estimated by different authors (e.g., environment in the vicinity of the cave was “a
Johanson and Edey, 1981; Partridge and Watt, forested riverine habitat fringed by grassland”
1991; Partridge et al., 2002a,b; Kuman and Clarke, (Clarke and Kuman, 1998). On a wider timescale,
2000) to date between 3 and 2 Ma. A recent debate Clarke and Kuman, (2000) suggest that the
about the chronology (Berger et al., 2002; Clarke, environment changed between 3.0 and 2.6 Ma
2002a; Partridge, 2002) demonstrates that the issue from a moist habitat, which included tropical
remains unsettled; dates between 2.5 and 2.0 Ma elements like lianas (Bamford, 1999), to a drier
are probably reasonable estimates for our purpose. regime that was dominated by open grassland.
It is well beyond the scope of our study to Sterkfontein has attracted scientific interest
comment on the chronology of the hominins at since 1936, when Broom discovered the first fossil
Sterkfontein. We draw attention, however, to the cranium of a hominin at the site (Broom and
published isotopic data for four specimens of A. Schepers, 1946; Broom et al., 1950). Most hominin
africanus found at Makapansgat (Sponheimer and specimens found at Sterkfontein since then have
Lee-Thorp, 1999a), from a time (ca. 3 Ma) and come from Member 4. These are now classified by
geographic location different from Sterkfontein many palaeoanthropologists as Australopithecus
Member 4. africanus: a small-brained, bipedal, early hominin

5. N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597 585
that may be the ancestor of Australopithecus collagen, but carbon and oxygen isotope ratios
(Paranthropus) robustus and early Homo sp. In can be measured in the mineral phase of their
South Africa, the latter two taxa are represented at fossilised skeletons.
Swartkrans (Vrba 1973, 1995; Brain, 1981, 1993); Isotopic analysis of fossils is a phenomenon of
at Sterkfontein itself (Hughes and Tobias, 1977; the past two decades, but it is already well-
Kuman and Clarke, 2000) they occur in deposits established in palaeontology. It was tried first on
younger than 2 Ma. Clarke has also suggested fossil bone (Sullivan and Krueger, 1981, 1983), but
that among the hominin fossils of Sterkfontein tooth enamel has proved to be the most reliable
Member 4 there is a “pre-robust” form with large sample material (Lee-Thorp and van der Merwe,
teeth, which is ancestral to A. robustus (Clarke, 1987, 1991; Lee-Thorp et al., 2000). Tooth enamel
1988). is a biological apatite (calcium phosphate), which
The taxonomy of hominin fossils is based on includes various impurities. Carbonates make up
anatomy. Some behavioural characteristics are about 3% by weight of bioapatite. These carbon-
inferred from anatomical details and associated ates are precipitated from dissolved CO2 in the
artefacts. An important behavioural argument blood plasma of the animal, which is derived from
involves diet, inferred from tooth morphology, the metabolism of food. The dietary information
dental scarring, and technological capability. encoded in the stable carbon isotope ratio ( 13C
Stable isotope analysis can provide significant value) of tooth enamel carbonate is an average of
information about the dietary behaviour of the the distinctive carbon isotope ratios of plants at
Sterkfontein hominins, while the isotopic data for the base of the foodweb of an individual. This
associated fauna contribute to an assessment of the isotopic signature can be acquired by eating the
environment they lived in. plants, eating animals or insects that eat the plants,
or both. C3 plants include essentially all trees and
shrubs (woody plants) and the grasses of temper-
Isotopes and tooth enamel
ate environments and shaded forests. C4 plants
The reconstruction of prehistoric diets and include most of the grasses and many of the sedges
environments by means of isotopic analysis of of subtropical regions. During the late Miocene
bone (Vogel and van der Merwe, 1977; van der (ca. 7 Ma), C4 grasslands expanded rapidly in
Merwe and Vogel, 1978) has been developed over many parts of the world, including the interior
more than thirty years and is by now routine in of East Africa (Cerling et al., 1993, 1997). The
archaeology (for reviews see van der Merwe, 1982; exact timing of the expansion of C4 grasses
Schoeninger and Moore, 1992; Katzenberg, 2000). in the South African interior remains to be docu-
Skeletal material of relatively recent vintage mented by means of isotopic analysis of the tooth
contains protein (bone collagen), which can be enamel of grazing animals, but it is clear from
analysed for its stable carbon and nitrogen iso- our data that the grasses in the vicinity of
tope ratios. Carbon isotopes provide a measure Sterkfontein during Member 4 times were of the
of the relative contributions of C3 and C4 plants C4 type.
to the foodweb of humans and other animals, At present, browsing herbivores (consumers of
and can also indicate whether the environment C3 foliage) of the South African interior have
was forested or open. Nitrogen isotopes give an mean enamel 13C values of about 14.5‰
indication of trophic level, especially relevant (per mil), while grazing animals (consumers of
when the diet includes meat, and may also pro- C4 grasses) have mean values of about 0.5‰
vide evidence of arid environments. The oldest (Lee-Thorp and van der Merwe, 1987). Carnivores
specimens of hominin collagen that have been have 13C values closely similar to that of their
successfully analysed came from Neanderthal prey. The 13C values of dedicated browsers (e.g.,
remains that were preserved in cold, dry cave giraffe, tragelaphines like bushbuck and kudu in
deposits (Bocherens et al., 1999; Richards et al., well-wooded regions) and of pure grazers (e.g.,
2000). Australopithecine remains do not contain alcelaphines like wildebeest) are regarded as the

6. 586 N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597
C3 and C4 end members. These values are not Isotopic analysis of hominins
static, but can be altered slightly by climatic or
atmospheric conditions. Increased humidity, for During the past fifteen years, the Archaeometry
example, may make the 13C values of C3 plants Research Unit of the University of Cape Town has
(but not C4) more negative by as much as 2‰ been intensively involved in the study of early
(for review, see Tieszen, 1991). Dense forests are hominin diets, utilising both stable isotope and
an extreme example, with C3 plants more nega- elemental chemistry. These studies have involved
tive by 10‰ than the average for C3 plants considerable refinement of the laboratory tech-
growing in the open. This is the result of high niques over time. The refinements have included
humidity, low light, and the recycling of CO2 changes in the chemical pre-treatment of sample
that is produced by rotting leaf litter and trapped material and, in particular, a reduction of the
under the canopy (van der Merwe and Medina, amount of tooth enamel required for isotopic
1989). On the other hand, increased aridity and analysis from 1 gram to 1 mg. The work reported
solar radiation make the 13C values of C3 plants in this article has spanned these fifteen years and,
slightly more positive (Ehleringer et al., 1986; therefore, records this history.
Ehleringer and Cooper, 1988), while C4 plants Analyses by the Cape Town laboratory have
may respond by the increased prevalence of included isotopic analysis of the tooth enamel of
enzymatic sub-types that have slightly more Australopithecus robustus and Homo sp. from
negative 13C values (Hattersley, 1982, 1992). Swartkrans (Lee-Thorp, 1989; Lee Thorp and van
Measurements by Cerling and Harris (1999) in der Merwe, 1989, 1993; Lee-Thorp et al., 1994;
Kenya show a difference of about 1‰ between Lee-Thorp et al., 2000). The Swartkrans results
these subtypes. Finally, changes in the atmos- demonstrated that both A. robustus and Homo sp.
phere may alter the 13C values of all plants by were generalised feeders with near-identical iso-
the same amount: burning of fossil fuel during topic signatures (mean 13C values about 8.5‰).
the industrial era raised the CO2 content of the A comparative study of closely related hominins
atmosphere substantially and made the 13C from Tanzania, A. boisei and Homo sp., has been
values of all terrestrial plants more negative by concluded and a report is forthcoming (van der
1.5‰ (Friedli et al., 1986; Marino and McElroy, Merwe et al., in preparation). Four specimens of A.
1991). To calculate the proportions of C3 and C4 africanus from Makapansgat (ca. 3 Ma) have been
plants in the foodweb of an individual at a given analysed isotopically (Sponheimer and Lee-Thorp,
time and place, therefore, it is necessary to estab- 1999a). The results indicate that A. africanus was
lish the C3 and C4 end members (the 13C values also a generalist in its feeding behaviour, but the
of reliable browsers and grazers) in the same carbon isotope ratios are much more variable than
context. those for any given species of hominin from
When the 13C value of tooth enamel carbonate Swartkrans and Tanzania. The results for ten
is determined, the ratio of the stable oxygen specimens of A. africanus from Sterkfontein
isotopes 18O and 16O ( 18O value) is routinely Member 4 reported here are also highly variable,
measured in the mass spectrometer. It is now showing that the dietary adaptation of this species
known that oxygen isotopes are related to the was considerably more varied than those of other
body water of an individual, which is acquired hominin species that have been analysed.
from water or food in the local environment, and The first isotopic analyses of Sterkfontein
which is altered by the thermophysiology of the hominins were done as early as 1989, when Phillip
animal. These values may contribute to dietary Tobias provided us with seven individual teeth that
and behavioural interpretations (Quade et al., were identified as hominin. Since these were frag-
1992; Bocherens et al., 1996; Cerling et al., 1997; mentary, identification was difficult and some of
Sponheimer and LeeThorp, 1999b), but are not yet the specimens had isotopic characteristics that
well understood. Oxygen isotope data are not resembled those of grazing animals, i.e., with very
reported in this article. high C4 components in their diets. This was in stark

7. N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597 587
contrast to the results from Swartkrans, where the The specimens from Sterkfontein
13
C values of A. robustus and Homo sp. showed
that both hominins had about 25% carbon derived The tooth enamel samples from Sterkfontein
from C4 plants in their diets. Another primate from that we have analysed were obtained from
Swartkrans, however, did have the 13C value of a the collections of the Anatomy Department,
grazer: this was Theropithecus oswaldi (previously University of the Witwatersrand (prefix Stw); the
identified as T. darti), a distant relative of the storage shed at Sterkfontein itself (SF); and the
graminivorous gelada baboon of modern Ethiopia. Transvaal Museum (STS). These catalogue pre-
In 1989, no specimens of T. oswaldi had yet been fixes represent a 53-year history of the excavations
identified at Sterkfontein and it was assumed at Sterkfontein and the involvement of investiga-
that this primate was not present in South Africa at tors from the Transvaal Museum (Robert Broom,
the time of Member 4 deposition. We observed, John Robinson, Bob Brain, Elisabeth Vrba) and
however, that those hominin specimens from the University of the Witwatersrand (Phillip
Sterkfontein with very positive 13C values had Tobias, Alun Hughes, Ron Clarke, among others).
significantly thinner tooth enamel than the others Taxonomic identifications of Sterkfontein fossil
(Table 1). The same was true for T. oswaldi from specimens were done by a number of analysts,
Swartkrans; indeed, all the non-hominin primates re-done by others, and we found it necessary to
(e.g., Papio sp. and Parapapio sp.) have thinner question some of the identifications on the basis of
tooth enamel than hominins. isotopic dietary information.
Two developments served to revive our dor- Of the faunal assemblage from Member 4, 70
mant study of Sterkfontein hominins. In late specimens have been isotopically analysed. Some
1994 the Cape Town laboratory acquired a of these results have been published (van der
Finnegan MAT252 mass spectrometer with an Merwe and Thackeray 1997), while a complete
on-line Kiel II carbonate autosampler. This made report is available in a thesis (Luyt 2001) that will
it possible to reduce the minimum sample re- be published in due course. In Table 2 we report a
quirements for pre-treated tooth enamel from 1 g selection of carbon isotope values for browsing
to 1 mg. The procedure we developed was to and grazing ungulates (to establish the C3 and C4
remove about 3 mg of enamel from a tooth (for end members) as well as for Parapapio sp., a genus
two separate measurements), using a diamond- that includes three extinct species of baboons (to
tipped dental drill of about 1 mm diameter. The compare with the hominin results).
sample size is the equivalent of one or two sugar To establish the C3 and C4 end members, we
grains and allows for the sampling of specimens have selected specimens for which the identifica-
more valuable than broken teeth. Secondly, a tion is secure at least to the genus level. At the C3
nearly complete mandible of Theropithecus end of the dietary spectrum, these include Anti-
oswaldi from Sterkfontein Member 4 was found dorcas recki, an extinct browsing springbok, and
in 1996, which brought up the question of Tragelaphus strepsiceros, the extant greater kudu.
whether the hominin attribution of all seven teeth For the C4 end member, we have selected Anti-
we had analysed was correct. Accordingly, we dorcas bondi, an extinct grazing springbok; Conno-
were allowed to sample more hominin teeth from chaetes sp., similar to the extant blue wildebeest,
Sterkfontein and finally to sample two specimens C. taurinus; Damaliscus sp., similar to the extant
from Member 4 that were more complete and blesbok; and Hippotragus equinus, the extant roan
were attributed to Australopithecus africanus: a antelope.
palate (Stw 73) and cranial fragments plus a The specimens from Sterkfontein Member 4
maxilla with good dentition (Stw 252). At the that were assigned as hominin are described in
same time, we invited several palaeoanthropolo- Table 1. Comments about their taxonomic affilia-
gists to have a close look at casts of the teeth we tions are included, provided at various times over
had analysed in 1989 and to comment on their the past decade by Phillip Tobias (PVT), Fred
attribution (Table 1). Grine (FG), and Ron Clarke (RC).

8. 588
Table 1
Fossil specimens from Sterkfontein Member 4 that were assigned as hominin or Theropithecus. Comments about their taxonomic affiliation were provided by
Phillip Tobias (PVT), Fred Grine (FG), and Ron Clarke (RC). Enamel thicknesses on the occlusal surfaces were measured by Thackeray (JFT); the results appear
to cluster into two groups of about 2 mm and 1.3 mm
N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597
Stw 73. Palate of Australopithecus africanus (PVT, RC); belongs with molars STS22 in the Transvaal Museum. Member 4. RM2 sampled by drilling (Method 2).
Stw 276. Unerupted crown of permanent molar. Location: S46 22#7$, Member 4. Identification: LM3 of A. africanus or H. habilis (PVT 1988); LM1 or LM2 of
A africanus (FG 1998); LM3, possible female of large-toothed, A. africanus/robustus or “pre-robust” form (RC 1996). Thick enamel, ca. 2 mm (JFT). Enamel
removed manually (Method 1) and subsequently drilled (Method 2).
Stw 252. Cranium with good dentition, illustrated by Johanson and Edgar (1996:146). Identification: A. africanus (PVT); large-toothed, “pre-robust” type (RC
1996). Member 4. RM1 (Stw 252f) sampled by drilling (Method 2).
Stw 211. Molar fragment of hominin (RC 1996). Location: V46 15#11$, Member 4. Stratigraphically high in the site, compared to other specimens. Thick enamel,
ca. 2 mm (JFT). Enamel removed manually (Method 1) and subsequently by drilling (Method 2).
Stw 304. Hominin molar fragment (RC 1998). Location: T48 26#9$, Member 4. Thick enamel, 2 mm (JFT). Enamel removed manually (Method 1) and by drilling
(Method 2).
Stw 14. Hominin LM1. Member 4. Identification: Australopithecus sp. (Wits catalogue); “pre-robust” form (RC 1996). Sampled by drilling (Method 2).
Stw 315. Lower left deciduous molar (Ldm2) of hominin (RC 1996). Location: R48 24#1$, Member 4. Enamel removed manually (Method 1) and by drilling
(Method 2).
Stw 309b. (formerly 409). Isolated LM1 (or 2 or 3) of hominin. Member 4. Identification: Australopithecus sp. (Wits catalogue); possible female of “pre-robust”
form (RC 1996). Sampled by drilling (Method 2).
Stw 229. Upper premolar crown fragment of hominin (RC 1996). Location: V47 20#7$, Member 4. Thick enamel, 2.1 0.2 mm (n = 7) (JFT). Enamel removed
manually (method 1) and by drilling (Method 2).
Stw 303. Right upper molar with broken edge. Member 4. Identification: RM2, possibly RM1, of A. africanus (PVT); RM1 of A .africanus (FG 1998); RM2 (?) of
australopithecine, most probably A. africanus, possibly “pre-robust” form (RC 1996). Enamel removed manually (Method 1) and by drilling (Method 2). Note:
this specimen has a 13C value of 4.4‰, the most positive of ten specimens firmly identified as hominin.
Stw 236. Premolar fragment. Location T45 19#6$, Member 4. Thin enamel, 1.3 0.6 mm (n = 3). Identification: listed as a hominin in Wits catalogue; status
uncertain (RC 1996). Enamel removed manually (method 1) and by drilling (method 2).
Stw 213i. LM1 fragment. Location T46 21#5$, Member 4. Identification: definitely a hominin (RC 1996). Thin enamel, 1.3 0.3 mm (n = 5) (JFT). Enamel
removed manually (Method 1) and by drilling (Method 2). Note: The very positive 13C value ( 1.8‰) and the thin enamel raise concerns about its hominin
status.
Stw 207. Tooth fragment. Member 4. Identification: listed as hominin in Wits catalogue; hominin status uncertain, could be Theropithecus (RC 1996). Sampled by
drilling (Method 2).
Stw uncatalogued. Nearly complete mandible, partially reconstructed by Alun Hughes. Location: X53 7#8$ 8#2$, from the same stratigraphic position as Stw 53,
hence Member 5 (PVT) or Member 4 (RC). Identification: Theropithecus oswaldi (RC 1996). RM3 sampled by drilling (Method 2).

9. N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597 589
Methods low-power, slow-turning hand drill. Where poss-
ible, broken enamel surfaces are used to grind off
Two different laboratory procedures were used the powder, instead of drilling a visible hole. Care
to analyse the tooth enamel; they represent, in is taken not to drill into dentine, or to heat the
effect, the history of development of isotopic enamel. Since 3 mg enamel is equal to about one or
studies on fossil teeth in our laboratory. Method 1 two sugar grains, damage to the tooth is minimal
was used in 1989 and Method 2 since 1995. and frequently invisible to the naked eye. The
fine powder is collected on smooth weighing paper
Method 1 and poured into a small centrifuge vial, in which
all subsequent pretreatment is carried out. The
This procedure has been described in more powder is pretreated with 1.5–2.0% sodium hypo-
detail elsewhere (Lee-Thorp and van der Merwe chlorite for 30 minutes, rinsed, and then reacted
1987, 1991; Lee-Thorp, 1989; Lee-Thorp et al., with 0.1 M acetic acid for 15 minutes. After wash-
1989). Enamel was separated manually from the ing and drying, 0.8–1.0 mg of powder is weighed
dentine using a jeweller’s sidecutter and a scalpel into individual reaction vessels of a Kiel II auto-
to obtain a sample of 0.5 to 1.0 g. The enamel was carbonate device. Each sample is reacted with
ground to powder in a Spex Freezer mill. An 100% phosphoric acid at 70(C, cryogenically dis-
aliquot of the powder was allowed to react over- tilled, and the isotope ratios of the resulting CO2
night with a weak solution (w2%) of sodium gas are measured in a Finnegan MAT252 mass
hypochlorite to eliminate bacterial proteins and spectrometer. The 13C and 18O values are cali-
humates, following which it was centrifuged and brated against PDB using a calibration curve
thoroughly rinsed. The anorganic powder was established from NBS standards 18 and 19, and by
pretreated with 1 M acetic acid for several days, inserting samples of secondary standards ‘Carrara
until effervescence ceased, then washed and freeze- Z marble’ and ‘Lincoln Limestone’ at regular
dried. This pretreatment dissolves carbonates that intervals in the sample run. Precision of replicate
may have precipitated from ground water and also analyses is better than 0.1‰.
some of the enamel. CO2 was produced by reacting
the freeze-dried powder with 100% phosphoric Comparison of methods 1 and 2
acid. The CO2 was collected by cryogenic distilla-
tion in a vacuum line, the yield measured mano- Comparison of more than 100 pairs of results
metrically, and the gas was flame-sealed in Pyrex obtained by Methods 1 and 2 show that 13C
for injection in the mass spectrometer. The 13C values differ by less than 0.1‰, on average. This
and 18O values were measured on a VG602E does not mean that each pair of results is always
Micromass spectrometer, using a reference gas the same, because Method 1 averages as much as
calibrated against five NBS standards. The results 1 g of enamel, while Method 2 provides a spot
are reported relative to PeeDee Belemnite (PDB); value for less than 3 mg. The average difference is
precision for repeat measurements is better than less that the analytical precision, however. In
0.1‰ (per mil). Table 2, the results obtained by both methods
(where available) are reported, averaged and
Method 2 rounded to the nearest 0.1‰. Previously published
13
C values for grazing and browsing ungulates
The procedure we have recently developed from Sterkfontein (van der Merwe and Thackeray
(Lee-Thorp et al., 1997; Sponheimer, 1999; Luyt, 1997) were obtained by Method 1.
2001) requires only 1 mg of pretreated enamel
powder. To allow for replicate measurements, Results
about 3 mg of powder is drilled from the tooth
enamel under magnification, using a diamond- Results are listed in Table 2 and portrayed in
tipped dental burr of 1 mm diameter, fitted into a two Figures (Figs. 1 and 2).

10. 590 N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597
Table 2
Stable carbon isotope ratios ( 13C values) for tooth enamel of Sterkfontein hominins and other fauna, relative to PDB. Methods 1
and 2 involved different chemical pre-treatment and sampling procedures (see text). Precision of repeated measurements were
better than 0.1‰
13
C (‰)
Taxon and specimen Member Method 1 Method 2 Ave.
Primates
Australopithecus africanus
Stw 73 M4 n.a. 8.8 8.8
Stw 276* M4 n.a. 8.0 8.0
Stw 252* M4 7.9 7.4 7.7
Stw 211 M4 7.8 7.3 7.5
Stw 304 M4 7.4 7.4 7.4
Stw 14* M4 n.a. 6.7 6.7
Stw 315 M4 7.0 5.7 6.4
Stw 309b (was 409)* M4 n.a. 6.1 6.1
Stw 229 M4 5.8 5.8 5.8
Stw 303* M4 4.4 4.3 4.4
Mean(n = 10) = 6.9 1.3
Australopithecus?
Stw 236 M4 3.8 3.6 3.7
Stw 213i M4 1.8 n.a. 1.8
Stw 207 M4 1.9 2.0
2.0
Theropithecus oswaldi
Stw uncatalogued M4/5 n.a. 2.9
2.9
Parapapio sp.
STS 422 M4 n.a. 8.8 8.8
STS 519 M4 n.a. 10.8 10.8
STS 526 M4 n.a. 9.8 9.8
STS 379A (P. broomi) M4 8.6 n.a. 8.6
STS 302 (P. jonesi) M4 8.1 n.a. 8.1
STS 348 (P. jonesi) M4 8.5 n.a. 8.5
Mean(n = 6) = 9.1 1.0
Browsers
Antidorcas recki
STS 2379 M4 n.a. 10.5 10.5
STS 1944 M4 n.a. 14.0 14.0
STS 1325A M4 n.a. 13.3 13.3
STS 1435 M4 n.a. 13.7 13.7
Mean (n = 4) = 12.9 1.6
Tragelaphus strepsiceros
SF 046 D13 M4 8.0 8.9 8.5
SF 1300 P46 8#2$–9#2$ M4 8.1 n.a. 8.1
STS 1573 M4 10.6 10.0 10.3
STS 2121 M4 8.7 8.2 8.5
Mean (n = 4) = 8.9 1.0
Grazers
Antidorcas bondi
STS 1125 M4 n.a. 1.3 1.3
Connochaetes sp.
SF 114 H2 C. cf. taurinus M4 1.2 2.0 1.6
SF 112 H2 C. cf. taurinus M4 0.2 0.7 0.5
SF 334 D13 C. cf. taurinus M4 0.0 1.1 0.6
Mean (n = 3) = 0.9 0.6

11. N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597 591
Table 2 (continued)
13
C (‰)
Taxon and specimen Member Method 1 Method 2 Ave.
Damaliscus sp.
SF 327 D13 M4 0.3 0.9 0.6
SF 328 D13 M4 +0.7 +1.4 +1.1
SF 329 D13 M4 +2.3 +1.4 +1.9
SF 330 D13 M4 n.a. +3.7 +3.7
SF 332 D13 M4 +3.5 +3.1 +3.3
Mean (n = 5) = +1.9 1.7
Hippotragus equinus
STS 2599 n.a. +0.1 +0.1
STS 1630 n.a. 2.2 2.2
Mean (n = 2) = 1.1
Matrix
UCT 1832 breccia D13 M4 n.a. 2.1 2.1
UCT 2768 calcite D13 M4 n.a. 2.5 2.5
Mean (n = 2) = 2.3
*
Hominin specimens with asterisks were identified by R.J. Clarke as possible “pre-robust” australopithecines.
At the C3 end of the dietary spectrum, the most adjusted for industrial changes in the atmosphere
negative 13C values are those obtained for one (by adding 1.5‰ to the measured values), the end
specimen each of Antidorcas recki ( 14‰), Para- members are identical to those of Sterkfontein
papio sp. ( 10.8‰) and Tragelaphus strepsiceros Member 4.
( 10.3‰). Of these, A. recki was clearly a dedi- Given a spectrum between 13‰ and +1‰
cated browser (mean 12.8‰, n = 4), with a diet for the 13C values of fossil tooth enamel at
that probably consisted of shrubs. T. strepsiceros, Sterkfontein, we can assess the diets of hominins
which prefers browse in most environments, from Member 4. The average 13C value for ten
included some C4 grass in its diet in this case. specimens that are attributed to Australopithecus
At the C4 end of the spectrum, the most positive africanus is 6.9 1.3‰. Three specimens are
13
C values are those for individual specimens of excluded from this average: their taxonomic status
Damaliscus sp. (+3.7‰), Hippotragus equinus is uncertain, as they are fragmentary and charac-
(+0.5‰) and Connochaetes sp. ( 0.5‰). Wher- terised by thin enamel (about 1.3 mm). Their 13C
ever these taxa have been compared, whether in values are more positive than those of the
fossil or modern assemblages, 13C values for undoubted australopithecines and they may be
Damaliscus sp. have invariably been more positive representatives of Theropithecus oswaldi, the graz-
than those for other grazers (Cerling et al., 1997; ing baboon, for which one well-identified specimen
Smith 1997). The diet of Damaliscus sp. includes with a 13C value of 2.9‰ is available. The
no browse and is apparently concentrated on the average 13C value of about 7‰ for ten austra-
subtypes of C4 grasses with the most positive 13C lopithecines represents a foodweb with about
values. 60% C3 plants and 40% C4 plants at its base. This
Based on these 13C values, the C3 and C4 end result is similar to those for Swartkrans hominins,
members for Sterkfontein Member 4 can be esti- although the average Sterkfontein C4 component
mated to lie at about 13‰ and +1‰; the latter is is larger by about 10 to 15%. Of more importance,
a weighted average for the grazer 13C values however, is the range of 13C values of the
available for this time and place. When the 13C Sterkfontein hominins, between 8.8‰ (about
values for modern animals from South Africa are 30% C4) and 4.4‰ (about 60% C4). To this

12. 592 N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597
range one can add four measurements for austra- animals. It is unlikely, for example, that a leopard
lopithecines (A. africanus) from Makapansgat (ca. could drag such prey into a tree. The scarcity of
3 Ma), which vary in 13C values from 10.7‰ to browsing ungulates at Sterkfontein is underscored
5.3‰ (Sponnheimer and Lee-Thorp 1999). The by the carbon isotope data for Tragelaphus strep-
C3 and C4 end members for fossil fauna from siceros, the greater kudu, which had 30% C4 plants
Sterkfontein Member 4 are slightly different from in its diet. Greater kudu occur in a variety of
those for Makapansgat ( 11‰ and +1‰); given modern African biomes and are usually browsers.
these end members, Makapansgat hominins had Significant exceptions in our database, with C4
diets with C4 components ranging from essentially dietary components as high as 50%, are from the
0 to 50%. Thus, two groups of hominin specimens Kalahari thornveld, where the browse is thorny,
that have been attributed to the species Australo- and the southern Namib desert, where it is scarce.
pithecus africanus, from two different locations and Making due allowance for the different accumula-
separated in time by perhaps as much as half a tion processes, the carbon isotope values for
million years, both had mixed diets with C4 com- the faunal assemblages from Makapansgat and
ponents that varied very widely between individ- Sterkfontein Member 4 show that the environment
uals. This is an extraordinary result and deserves at Makapansgat was slightly more wooded (Luyt,
close scrutiny. 2001).
The baboons of Sterkfontein Member 4 occu-
pied two distinct ecological niches. Three different
Discussion species may be represented among the results for
Parapapio sp.; they shared the C3 end of the
The carbon isotope data from Sterkfontein pro- spectrum with the browsers. The single specimen
vide several significant results. As expected, the of Theropithecus oswaldi ( 2.9‰) had a diet that
isotopic signatures of known grazers (Damaliscus included about 70% C4 plants. It is worth noting
sp., Connochaetes sp., Antidorcas bondi, and Hip- that the ecological niches occupied by Parapapio
potragus equinus) are at the positive (C4) end of the sp and T. oswaldi at Sterkfontein were still valid at
spectrum. The C3 end of the spectrum, however, is Swartkrans, half a million or more years later.
poorly represented. The only reliable browser in The most significant results from Sterkfontein
the assemblage was Antidorcas recki, an extinct are those for specimens that have been attributed
springbok (mean 13C value 12.8‰). Tragela- to Australopithecus africanus. These are highly
phus strepsiceros, the extant greater kudu variable, with 13C values for ten specimens vary-
( 8.9‰), included some 30% of C4 plants in its ing between 8.8‰ and 4.4‰, a range of 4.4‰.
diet. In contrast, the published isotope data for When the results for four Makapansgat specimens
Makapansgat (Sponheimer and Lee-Thorp, 1999a) ( 13C values between 10.7‰ and 5.3‰) are
include eleven species with 13C values at the C3 added to those of Sterkfontein, this range is
end of the spectrum. extended to 6.3‰. (Also note that Stw 213i, of
It is necessary to consider the different bone which the hominin attribution is in contention, has
accumulation processes at Makapansgat and a 13C value of 1.8‰; its inclusion would extend
Sterkfontein to interpret these isotope data the range to 8.9‰). This is an extraordinary range
(Maguire et al., 1980). At Makapansgat, a variety for any species.
of carnivore species were able to drag their prey An extensive isotope database for fossil and
into a large cave. The faunal remains in the talus modern African fauna is available by now, both
deposit of Sterkfontein member 4 were probably published and unpublished. The 13C values for a
washed into a narrow sinkhole, or were dropped single species at a given time and place are almost
from trees overhead, e.g., by leopards. The invariably clustered more tightly than those for A.
Makapansgat assemblage includes large browsing africanus reported here. An exception is Aepyceros
species like giraffe and rhinoceros; although these melampus, the impala (Sponheimer et al., in
are juvenile specimens, they are nevertheless large press), which is an unusual mixed feeder. Such

13. N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597 593
adaptability has made Aepyceros sp. an evolution- similarities with suids, monkeys and carnivores,
ary success story in the Plio-Pleistocene and earned but these similarities are as yet poorly understood
modern impala the soubriquet of “the cockroaches (Lee-Thorp et al., 2003). Oxygen isotope data for
of Africa” in wildlife conservation circles. Sterkfontein are reported elsewhere (Luyt, 2001
Among extant non-human primates, the 13C and in prep.)
values for any given species in a single environ- Palaeoenvironmental changes could have con-
ment are tightly clustered around the mean (e.g., tributed to the variability observed in the carbon
Schoeninger et al., 1997, 1999) and differences isotope ratios of Sterkfontein Member 4 hominins,
between males and females are not particularly given that the assemblage accumulated over an
noticeable. Thackeray et al., (1996) have measured unknown period of time. The same degree of
collagen 13C values of the modern baboon, Papio variability is found, however, among the four
cynocephalus ursinus in southern Africa. The speci- hominin specimens from Makapansgat, which are
mens came from six different localities, with from a different time and place.
environmental settings as varied as the Namib We can conclude that Australopithecus africanus
desert, the Limpopo Valley, and the subtropical at Sterkfontein had a well established C4 dietary
savanna of Kwazulu-Natal. The total range for P. component, which may well have included all of
cynocephalus ursinus across these six environments the available C4 food sources: grasses, particularly
is 5.7‰, but in any given environment the range is seeds and rhizomes; C4 sedges (which have
less than 3‰. The range in 13C for this baboon starchy underground storage organs); inverte-
species across all of southern Africa, therefore, brates (including locusts and termites); grazing
is less than that for A. africanus at two sites mammals; and perhaps even insectivores and
(Sterkfontein and Makapansgat) and only slightly carnivores. Whatever the sources were, different
more than that for A. africanus at Sterkfontein individuals of this early hominin species differed
alone. widely in their consumption of C4-based foods.
The variation in 13C values for P. cynocephalus The range of 13C values for A. africanus is so wide
in any given area more closely resembles those for that it invites consideration of the idea that more
the hominins A. robustus and Homo sp. at than one species of australopithecine is represented
Swartkrans. Recent measurements by van der in Sterkfontein Member 4. Clarke (1988) has
Merwe (unpublished) of carbon isotope ratios in argued for the presence of a large-toothed, “pre-
the tooth enamel of three specimens of A. robustus robust” australopithecine and has identified five
from the nearby site of Drimolen (Keyser et al., potential specimens of this type among the ten
2000), three specimens of Homo habilis from specimens we have analysed isotopically. These
Olduvai, Tanzania and two specimens of A. boisei five individuals are starred in Table 2 and Fig. 2
from Tanzania (Olduvai and Peninj) are similarly and can be seen to vary as much in 13C values as
constrained in their variability. All of these the remaining five. It is our opinion that only one
hominins had significant (and different) C4 dietary species, A. africanus, was present; if so, it had the
components, but A. africanus had much more most variable dietary behaviour of all the early
variation between individuals in the consumption hominin species we have investigated. The alterna-
of C4-based foods. tive hypothesis would be that two hominin species
C4-based foods can include C4 grasses and with equally unusual diets were present, which is
sedges, the vertebrates and insects that eat these less plausible.
plants, or the carnivores that eat the plant con-
sumers. Carbon isotope ratios by themselves
cannot distinguish between these potential food Conclusion
sources. Oxygen isotope ratios could be of some
help here, since they record the body water of The stable carbon isotope ratios for ten speci-
consumers. Early hominins from South and East mens of A. africanus from Sterkfontein Member 4
Africa have relatively low 18O values and show show that this species of hominin had an unusually

14. 594 N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597
varied diet with a sizeable component of C4-based Two palaeoanthropologists supported our iso-
foods. These could have included C4 grasses and topic approach to dietary analysis from the start
sedges and/or the insects and vertebrates that eat and allowed us to analyse hominin teeth from
these plants. The C4 dietary component varied Swartkrans and Sterkfontein, even though the
considerably from one individual to the next, with sample requirement was relatively large in the
a mean of about 40% and a range between about early days. They are Bob Brain and Phillip Tobias.
30 and 60%. When the results for four specimens We dedicate this article to them, with appreciation.
of A. africanus from Makapansgat are added to
those from Sterkfontein, the C4 component can be
seen to vary from nearly 0 to 60%. This range is
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