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
Hypotheses about the behavioural ecology of
early hominins play a critical role in scenarios that
seek to explain the evolution of humans from apes.
* Corresponding author. University of Cape Town,
Archaeometry Research Unit, Department of Archaeology,
Rondebosch, 7701 South Africa
E-mail address: [email protected] (N.J. van der
Merwe).
How and why did tree-climbing apes with diets of
forest plants evolve into bipedal savanna foragers
with omnivorous diets?
Since the description of the Taung specimen by
Raymond Dart (1925), hypotheses about the
dietary behaviour of Australopithecus africanus
have been varied and contradictory. Dart (1925,
1926) suggested that the australopithecine diet
included various insects, rodents, eggs, and
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
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environmental reconstructions available at the
time, to the effect that the climate of South Africa
had not changed significantly during the PlioPleistocene. In later years, of course, Dart (1957)
described A. africanus as a homicidal hunter with
an osteodontokeratic culture. This idea was laid
to rest by Brain (1981), who demonstrated that
the australopithecines were victims rather than
aggressors.
Nearly fifty years ago, John Robinson (1954)
presented a “dietary hypothesis”, in terms of which
he described A. africanus from Sterkfontein as an
omnivore and A. (Paranthropus) robustus from
nearby Swartkrans (which he thought to be coeval) as a specialised herbivore. A. robustus was
subsequently shown to post-date A. africanus and
to have co-existed with Homo sp. at Swartkrans
(Brain, 1958, 1981). The designation of A. robustus
as a specialised herbivore has persisted, however,
and a common perception has emerged that the
omnivory of A. africanus was continued into the
Homo lineage. On the other hand, dental microscopy studies have suggested that A. africanus
might have been largely a fruit and leaf eater
(Grine, 1981; Grine and Kay, 1988).
The publication of Robinson’s dietary hypothesis nearly coincided with Mary Leakey’s 1959
discovery at Olduvai of A. (Zinjanthropus) boisei,
a robust australopithecine (Leakey, 1959). For a
while, “Zinj” disrupted the hominin story line,
because it was thought to be older than all of the
South African hominins and to have been the
producer of Oldowan stone tools. When “preZinj” was discovered at Olduvai in due course
(Leakey et al., 1964), interest shifted to Homo
habilis as the meat-eating, toolmaking omnivore
and A. boisei was relegated to the same specialised
herbivorous niche as its South African counterpart, A. robustus. The story regained its symmetry
with the discovery of A. afarensis (Johanson and
White, 1979), a possible East African precursor of
both H. habilis and A. boisei. The “forest to
savanna” theme for the critical juncture in human
evolution endured as a result and was given an
environmental backdrop by Yves Coppens (1983,
1994) with his “East Side Story”.
Hominins older than A. africanus and A. afarensis have been discovered during the last decade
in Ethiopia (White et al., 1994, 2000), Kenya
(Leakey et al., 2001; Pickford and Senut, 2001),
Chad (Brunet et al., 1995), and at Sterkfontein
(Stw 573, “Little Foot”) (Clarke, 1998, 2002b).
The East African and Sahelian hominins are said
to have lived in forested environments and Little
Foot has been described as a tree-climber who
lived in an environment that included (sub)tropical
vines (Bamford, 1999). The latest turn in the story,
then, seems to be “back to the forest” and it has
been suggested that the “savanna hypothesis”
should be discarded.
What do we actually know about the diets of
early hominins at about 2 Ma? Direct evidence is
exceedingly scarce. Cutmarks on bones have been
recorded at a number of sites and recent evidence
suggests that one or more hominins at Swartkrans
and Drimolen in South Africa used bone tools to
crack open termite mounds (Backwell and
d’Errico, 2000). The preponderence of A. robustus
fossils at both these sites provides a basis for
suggesting that the robust australopithecine was
the termite-forager, but Homo sp. was also present
here. The idea that A. robustus was a generalised
feeder and perhaps an omnivore is given further
credence by the evidence from stable carbon isotopes (Lee-Thorp et al., 1994, 2000). Both A.
robustus and Homo sp. from Swartkrans had diets
of which about 25%, on average, was derived from
C4 plants (savanna grasses or C4 sedges) and/or
their consumers (insects, reptiles, mammals). This
does not mean that they had identical diets, but the
carbon isotope data constrain the range of possibilities of what their diets could have been. The C4
component specifically excludes plants from
canopy forests, i.e., foods from open environments
are implied by the isotopic data. Carbon isotope
data are also available for four specimens of A.
africanus from Makapansgat. This hominin had
C4-based foods in its diet as well, but the amounts
varied from near 0 to 50% among the four
individuals (Sponheimer and Lee-Thorp, 1999a).
These data are considered in detail below.
Obviously, at some point, hominins came to
consume a greater component of food from the
savannas, specifically animal food. The “expensive
tissue hypothesis” of Aiello and Wheeler (1995)
holds that increases in brain size would have
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
animal foods, since the gut became smaller as the
brain became larger. This progression of omnivory
in the course of encephalisation can be investigated
by means of isotopic dietary chemistry.
We have studied in some detail the carbon
isotope ecology of A. africanus at Sterkfontein and
have obtained carbon isotope ratios for the tooth
enamel of ten hominin specimens from Member 4.
This is the largest number of specimens of an early
hominin species that has been isotopically analysed so far. The results reported here (Table 2,
Fig. 2) show that A. africanus was an unusual
generalised feeder.
Background to Sterkfontein hominins
Sterkfontein has hominin-bearing deposits that
span the period of about 3.5 to 1.5 million years
ago (Broom and Schepers, 1946; Broom et al.,
1950; Vrba, 1976, 1982, 1995; Partridge 2000;
Partridge et al., 2000a,b); these have yielded more
than 500 fossil specimens of hominins, ranging
from individual teeth and small skeletal elements
to complete crania (Kuman, 1994; Kuman and
Clarke, 2000; Clarke and Kuman, 1998, 2000). A
recent discovery (Clarke, 1998) is a nearly complete skeleton of an australopithecine (Stw 573)
that lived more than 3 million years ago, but
excavation of this find is still in progress (Clarke,
2002b).
Most of the hominin discoveries at Sterkfontein
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
subsequently cemented by carbonates from the
percolating ground water. The ages of Member 4
and other deposits at Sterkfontein are notably difficult to establish, due to the complex stratigraphy
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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
amenable to radiometric dating. Member 4 has
been variously estimated by different authors (e.g.,
Johanson and Edey, 1981; Partridge and Watt,
1991; Partridge et al., 2002a,b; Kuman and Clarke,
2000) to date between 3 and 2 Ma. A recent debate
about the chronology (Berger et al., 2002; Clarke,
2002a; Partridge, 2002) demonstrates that the issue
remains unsettled; dates between 2.5 and 2.0 Ma
are probably reasonable estimates for our purpose.
It is well beyond the scope of our study to
comment on the chronology of the hominins at
Sterkfontein. We draw attention, however, to the
published isotopic data for four specimens of A.
africanus found at Makapansgat (Sponheimer and
Lee-Thorp, 1999a), from a time (ca. 3 Ma) and
geographic location different from Sterkfontein
Member 4.
The faunal assemblage from Sterkfontein
Member 4 has been interpreted to suggest that the
environment in the vicinity of the cave was “a
forested riverine habitat fringed by grassland”
(Clarke and Kuman, 1998). On a wider timescale,
Clarke and Kuman, (2000) suggest that the
environment changed between 3.0 and 2.6 Ma
from a moist habitat, which included tropical
elements like lianas (Bamford, 1999), to a drier
regime that was dominated by open grassland.
Sterkfontein has attracted scientific interest
since 1936, when Broom discovered the first fossil
cranium of a hominin at the site (Broom and
Schepers, 1946; Broom et al., 1950). Most hominin
specimens found at Sterkfontein since then have
come from Member 4. These are now classified by
many palaeoanthropologists as Australopithecus
africanus: a small-brained, bipedal, early hominin
N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597
that may be the ancestor of Australopithecus
(Paranthropus) robustus and early Homo sp. In
South Africa, the latter two taxa are represented at
Swartkrans (Vrba 1973, 1995; Brain, 1981, 1993);
at Sterkfontein itself (Hughes and Tobias, 1977;
Kuman and Clarke, 2000) they occur in deposits
younger than 2 Ma. Clarke has also suggested
that among the hominin fossils of Sterkfontein
Member 4 there is a “pre-robust” form with large
teeth, which is ancestral to A. robustus (Clarke,
1988).
The taxonomy of hominin fossils is based on
anatomy. Some behavioural characteristics are
inferred from anatomical details and associated
artefacts. An important behavioural argument
involves diet, inferred from tooth morphology,
dental scarring, and technological capability.
Stable isotope analysis can provide significant
information about the dietary behaviour of the
Sterkfontein hominins, while the isotopic data for
associated fauna contribute to an assessment of the
environment they lived in.
Isotopes and tooth enamel
The reconstruction of prehistoric diets and
environments by means of isotopic analysis of
bone (Vogel and van der Merwe, 1977; van der
Merwe and Vogel, 1978) has been developed over
more than thirty years and is by now routine in
archaeology (for reviews see van der Merwe, 1982;
Schoeninger and Moore, 1992; Katzenberg, 2000).
Skeletal material of relatively recent vintage
contains protein (bone collagen), which can be
analysed for its stable carbon and nitrogen isotope ratios. Carbon isotopes provide a measure
of the relative contributions of C3 and C4 plants
to the foodweb of humans and other animals,
and can also indicate whether the environment
was forested or open. Nitrogen isotopes give an
indication of trophic level, especially relevant
when the diet includes meat, and may also provide evidence of arid environments. The oldest
specimens of hominin collagen that have been
successfully analysed came from Neanderthal
remains that were preserved in cold, dry cave
deposits (Bocherens et al., 1999; Richards et al.,
2000). Australopithecine remains do not contain
585
collagen, but carbon and oxygen isotope ratios
can be measured in the mineral phase of their
fossilised skeletons.
Isotopic analysis of fossils is a phenomenon of
the past two decades, but it is already wellestablished in palaeontology. It was tried first on
fossil bone (Sullivan and Krueger, 1981, 1983), but
tooth enamel has proved to be the most reliable
sample material (Lee-Thorp and van der Merwe,
1987, 1991; Lee-Thorp et al., 2000). Tooth enamel
is a biological apatite (calcium phosphate), which
includes various impurities. Carbonates make up
about 3% by weight of bioapatite. These carbonates are precipitated from dissolved CO2 in the
blood plasma of the animal, which is derived from
the metabolism of food. The dietary information
encoded in the stable carbon isotope ratio (13C
value) of tooth enamel carbonate is an average of
the distinctive carbon isotope ratios of plants at
the base of the foodweb of an individual. This
isotopic signature can be acquired by eating the
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 temperate environments and shaded forests. C4 plants
include most of the grasses and many of the sedges
of subtropical regions. During the late Miocene
(ca. 7 Ma), C4 grasslands expanded rapidly in
many parts of the world, including the interior
of East Africa (Cerling et al., 1993, 1997). The
exact timing of the expansion of C4 grasses
in the South African interior remains to be documented by means of isotopic analysis of the tooth
enamel of grazing animals, but it is clear from
our data that the grasses in the vicinity of
Sterkfontein during Member 4 times were of the
C4 type.
At present, browsing herbivores (consumers of
C3 foliage) of the South African interior have
mean enamel 13C values of about 14.5‰
(per mil), while grazing animals (consumers of
C4 grasses) have mean values of about 0.5‰
(Lee-Thorp and van der Merwe, 1987). Carnivores
have 13C values closely similar to that of their
prey. The 13C values of dedicated browsers (e.g.,
giraffe, tragelaphines like bushbuck and kudu in
well-wooded regions) and of pure grazers (e.g.,
alcelaphines like wildebeest) are regarded as the
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C3 and C4 end members. These values are not
static, but can be altered slightly by climatic or
atmospheric conditions. Increased humidity, for
example, may make the 13C values of C3 plants
(but not C4) more negative by as much as 2‰
(for review, see Tieszen, 1991). Dense forests are
an extreme example, with C3 plants more negative by 10‰ than the average for C3 plants
growing in the open. This is the result of high
humidity, low light, and the recycling of CO2
that is produced by rotting leaf litter and trapped
under the canopy (van der Merwe and Medina,
1989). On the other hand, increased aridity and
solar radiation make the 13C values of C3 plants
slightly more positive (Ehleringer et al., 1986;
Ehleringer and Cooper, 1988), while C4 plants
may respond by the increased prevalence of
enzymatic sub-types that have slightly more
negative 13C values (Hattersley, 1982, 1992).
Measurements by Cerling and Harris (1999) in
Kenya show a difference of about 1‰ between
these subtypes. Finally, changes in the atmosphere may alter the 13C values of all plants by
the same amount: burning of fossil fuel during
the industrial era raised the CO2 content of the
atmosphere substantially and made the 13C
values of all terrestrial plants more negative by
1.5‰ (Friedli et al., 1986; Marino and McElroy,
1991). To calculate the proportions of C3 and C4
plants in the foodweb of an individual at a given
time and place, therefore, it is necessary to establish the C3 and C4 end members (the 13C values
of reliable browsers and grazers) in the same
context.
When the 13C value of tooth enamel carbonate
is determined, the ratio of the stable oxygen
isotopes 18O and 16O (18O value) is routinely
measured in the mass spectrometer. It is now
known that oxygen isotopes are related to the
body water of an individual, which is acquired
from water or food in the local environment, and
which is altered by the thermophysiology of the
animal. These values may contribute to dietary
and behavioural interpretations (Quade et al.,
1992; Bocherens et al., 1996; Cerling et al., 1997;
Sponheimer and LeeThorp, 1999b), but are not yet
well understood. Oxygen isotope data are not
reported in this article.
Isotopic analysis of hominins
During the past fifteen years, the Archaeometry
Research Unit of the University of Cape Town has
been intensively involved in the study of early
hominin diets, utilising both stable isotope and
elemental chemistry. These studies have involved
considerable refinement of the laboratory techniques over time. The refinements have included
changes in the chemical pre-treatment of sample
material and, in particular, a reduction of the
amount of tooth enamel required for isotopic
analysis from 1 gram to 1 mg. The work reported
in this article has spanned these fifteen years and,
therefore, records this history.
Analyses by the Cape Town laboratory have
included isotopic analysis of the tooth enamel of
Australopithecus robustus and Homo sp. from
Swartkrans (Lee-Thorp, 1989; Lee Thorp and van
der Merwe, 1989, 1993; Lee-Thorp et al., 1994;
Lee-Thorp et al., 2000). The Swartkrans results
demonstrated that both A. robustus and Homo sp.
were generalised feeders with near-identical isotopic signatures (mean 13C values about 8.5‰).
A comparative study of closely related hominins
from Tanzania, A. boisei and Homo sp., has been
concluded and a report is forthcoming (van der
Merwe et al., in preparation). Four specimens of A.
africanus from Makapansgat (ca. 3 Ma) have been
analysed isotopically (Sponheimer and Lee-Thorp,
1999a). The results indicate that A. africanus was
also a generalist in its feeding behaviour, but the
carbon isotope ratios are much more variable than
those for any given species of hominin from
Swartkrans and Tanzania. The results for ten
specimens of A. africanus from Sterkfontein
Member 4 reported here are also highly variable,
showing that the dietary adaptation of this species
was considerably more varied than those of other
hominin species that have been analysed.
The first isotopic analyses of Sterkfontein
hominins were done as early as 1989, when Phillip
Tobias provided us with seven individual teeth that
were identified as hominin. Since these were fragmentary, identification was difficult and some of
the specimens had isotopic characteristics that
resembled those of grazing animals, i.e., with very
high C4 components in their diets. This was in stark
N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597
contrast to the results from Swartkrans, where the
13C values of A. robustus and Homo sp. showed
that both hominins had about 25% carbon derived
from C4 plants in their diets. Another primate from
Swartkrans, however, did have the 13C value of a
grazer: this was Theropithecus oswaldi (previously
identified as T. darti), a distant relative of the
graminivorous gelada baboon of modern Ethiopia.
In 1989, no specimens of T. oswaldi had yet been
identified at Sterkfontein and it was assumed
that this primate was not present in South Africa at
the time of Member 4 deposition. We observed,
however, that those hominin specimens from
Sterkfontein with very positive 13C values had
significantly thinner tooth enamel than the others
(Table 1). The same was true for T. oswaldi from
Swartkrans; indeed, all the non-hominin primates
(e.g., Papio sp. and Parapapio sp.) have thinner
tooth enamel than hominins.
Two developments served to revive our dormant study of Sterkfontein hominins. In late
1994 the Cape Town laboratory acquired a
Finnegan MAT252 mass spectrometer with an
on-line Kiel II carbonate autosampler. This made
it possible to reduce the minimum sample requirements for pre-treated tooth enamel from 1 g
to 1 mg. The procedure we developed was to
remove about 3 mg of enamel from a tooth (for
two separate measurements), using a diamondtipped dental drill of about 1 mm diameter. The
sample size is the equivalent of one or two sugar
grains and allows for the sampling of specimens
more valuable than broken teeth. Secondly, a
nearly complete mandible of Theropithecus
oswaldi from Sterkfontein Member 4 was found
in 1996, which brought up the question of
whether the hominin attribution of all seven teeth
we had analysed was correct. Accordingly, we
were allowed to sample more hominin teeth from
Sterkfontein and finally to sample two specimens
from Member 4 that were more complete and
were attributed to Australopithecus africanus: a
palate (Stw 73) and cranial fragments plus a
maxilla with good dentition (Stw 252). At the
same time, we invited several palaeoanthropologists to have a close look at casts of the teeth we
had analysed in 1989 and to comment on their
attribution (Table 1).
587
The specimens from Sterkfontein
The tooth enamel samples from Sterkfontein
that we have analysed were obtained from
the collections of the Anatomy Department,
University of the Witwatersrand (prefix Stw); the
storage shed at Sterkfontein itself (SF); and the
Transvaal Museum (STS). These catalogue prefixes represent a 53-year history of the excavations
at Sterkfontein and the involvement of investigators from the Transvaal Museum (Robert Broom,
John Robinson, Bob Brain, Elisabeth Vrba) and
the University of the Witwatersrand (Phillip
Tobias, Alun Hughes, Ron Clarke, among others).
Taxonomic identifications of Sterkfontein fossil
specimens were done by a number of analysts,
re-done by others, and we found it necessary to
question some of the identifications on the basis of
isotopic dietary information.
Of the faunal assemblage from Member 4, 70
specimens have been isotopically analysed. Some
of these results have been published (van der
Merwe and Thackeray 1997), while a complete
report is available in a thesis (Luyt 2001) that will
be published in due course. In Table 2 we report a
selection of carbon isotope values for browsing
and grazing ungulates (to establish the C3 and C4
end members) as well as for Parapapio sp., a genus
that includes three extinct species of baboons (to
compare with the hominin results).
To establish the C3 and C4 end members, we
have selected specimens for which the identification is secure at least to the genus level. At the C3
end of the dietary spectrum, these include Antidorcas recki, an extinct browsing springbok, and
Tragelaphus strepsiceros, the extant greater kudu.
For the C4 end member, we have selected Antidorcas bondi, an extinct grazing springbok; Connochaetes sp., similar to the extant blue wildebeest,
C. taurinus; Damaliscus sp., similar to the extant
blesbok; and Hippotragus equinus, the extant roan
antelope.
The specimens from Sterkfontein Member 4
that were assigned as hominin are described in
Table 1. Comments about their taxonomic affiliations are included, provided at various times over
the past decade by Phillip Tobias (PVT), Fred
Grine (FG), and Ron Clarke (RC).
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$, Member 4. Thick enamel, 2.10.2 mm (n = 7) (JFT). Enamel removed
manually (method 1) and by drilling (Method 2).
Stw 303. Right upper molar with broken edge. Member 4. Identification: RM2, possibly RM1, of A. africanus (PVT); RM1 of A .africanus (FG 1998); RM2 (?) of
australopithecine, most probably A. africanus, possibly “pre-robust” form (RC 1996). Enamel removed manually (Method 1) and by drilling (Method 2). Note:
this specimen has a 13C value of 4.4‰, the most positive of ten specimens firmly identified as hominin.
Stw 236. Premolar fragment. Location T45 19#6$, Member 4. Thin enamel, 1.30.6 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, 1.30.3 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).
N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597
Methods
Two different laboratory procedures were used
to analyse the tooth enamel; they represent, in
effect, the history of development of isotopic
studies on fossil teeth in our laboratory. Method 1
was used in 1989 and Method 2 since 1995.
Method 1
This procedure has been described in more
detail elsewhere (Lee-Thorp and van der Merwe
1987, 1991; Lee-Thorp, 1989; Lee-Thorp et al.,
1989). Enamel was separated manually from the
dentine using a jeweller’s sidecutter and a scalpel
to obtain a sample of 0.5 to 1.0 g. The enamel was
ground to powder in a Spex Freezer mill. An
aliquot of the powder was allowed to react overnight with a weak solution (w2%) of sodium
hypochlorite to eliminate bacterial proteins and
humates, following which it was centrifuged and
thoroughly rinsed. The anorganic powder was
pretreated with 1 M acetic acid for several days,
until effervescence ceased, then washed and freezedried. This pretreatment dissolves carbonates that
may have precipitated from ground water and also
some of the enamel. CO2 was produced by reacting
the freeze-dried powder with 100% phosphoric
acid. The CO2 was collected by cryogenic distillation in a vacuum line, the yield measured manometrically, and the gas was flame-sealed in Pyrex
for injection in the mass spectrometer. The 13C
and 18O values were measured on a VG602E
Micromass spectrometer, using a reference gas
calibrated against five NBS standards. The results
are reported relative to PeeDee Belemnite (PDB);
precision for repeat measurements is better than
0.1‰ (per mil).
Method 2
The procedure we have recently developed
(Lee-Thorp et al., 1997; Sponheimer, 1999; Luyt,
2001) requires only 1 mg of pretreated enamel
powder. To allow for replicate measurements,
about 3 mg of powder is drilled from the tooth
enamel under magnification, using a diamondtipped dental burr of 1 mm diameter, fitted into a
589
low-power, slow-turning hand drill. Where possible, broken enamel surfaces are used to grind off
the powder, instead of drilling a visible hole. Care
is taken not to drill into dentine, or to heat the
enamel. Since 3 mg enamel is equal to about one or
two sugar grains, damage to the tooth is minimal
and frequently invisible to the naked eye. The
fine powder is collected on smooth weighing paper
and poured into a small centrifuge vial, in which
all subsequent pretreatment is carried out. The
powder is pretreated with 1.5–2.0% sodium hypochlorite for 30 minutes, rinsed, and then reacted
with 0.1 M acetic acid for 15 minutes. After washing and drying, 0.8–1.0 mg of powder is weighed
into individual reaction vessels of a Kiel II autocarbonate device. Each sample is reacted with
100% phosphoric acid at 70(C, cryogenically distilled, and the isotope ratios of the resulting CO2
gas are measured in a Finnegan MAT252 mass
spectrometer. The 13C and 18O values are calibrated against PDB using a calibration curve
established from NBS standards 18 and 19, and by
inserting samples of secondary standards ‘Carrara
Z marble’ and ‘Lincoln Limestone’ at regular
intervals in the sample run. Precision of replicate
analyses is better than 0.1‰.
Comparison of methods 1 and 2
Comparison of more than 100 pairs of results
obtained by Methods 1 and 2 show that 13C
values differ by less than 0.1‰, on average. This
does not mean that each pair of results is always
the same, because Method 1 averages as much as
1 g of enamel, while Method 2 provides a spot
value for less than 3 mg. The average difference is
less that the analytical precision, however. In
Table 2, the results obtained by both methods
(where available) are reported, averaged and
rounded to the nearest 0.1‰. Previously published
13C values for grazing and browsing ungulates
from Sterkfontein (van der Merwe and Thackeray
1997) were obtained by Method 1.
Results
Results are listed in Table 2 and portrayed in
two Figures (Figs. 1 and 2).
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‰
13C (‰)
Taxon and specimen
Member
Method 1
Method 2
Primates
Australopithecus africanus
Stw 73
Stw 276*
Stw 252*
Stw 211
Stw 304
Stw 14*
Stw 315
Stw 309b (was 409)*
Stw 229
Stw 303*
M4
M4
M4
M4
M4
M4
M4
M4
M4
M4
n.a.
8.8
n.a.
8.0
7.9
7.4
7.8
7.3
7.4
7.4
n.a.
6.7
7.0
5.7
n.a.
6.1
5.8
5.8
4.4
4.3
Mean(n = 10) = 6.91.3
Ave.
8.8
8.0
7.7
7.5
7.4
6.7
6.4
6.1
5.8
4.4
Australopithecus?
Stw 236
Stw 213i
Stw 207
M4
M4
M4
Theropithecus oswaldi
Stw uncatalogued
M4/5
n.a.
Parapapio sp.
STS 422
STS 519
STS 526
STS 379A (P. broomi)
STS 302 (P. jonesi)
STS 348 (P. jonesi)
M4
M4
M4
M4
M4
M4
n.a.
8.8
n.a.
10.8
n.a.
9.8
8.6
n.a.
8.1
n.a.
8.5
n.a.
Mean(n = 6) = 9.11.0
8.8
10.8
9.8
8.6
8.1
8.5
M4
M4
M4
M4
n.a.
10.5
n.a.
14.0
n.a.
13.3
n.a.
13.7
Mean (n = 4) = 12.91.6
10.5
14.0
13.3
13.7
M4
M4
M4
M4
8.0
8.9
8.1
n.a.
10.6
10.0
8.7
8.2
Mean (n = 4) = 8.91.0
8.5
8.1
10.3
8.5
M4
n.a.
1.3
1.3
M4
M4
M4
1.2
2.0
0.2
0.7
0.0
1.1
Mean (n = 3) = 0.90.6
1.6
0.5
0.6
Browsers
Antidorcas recki
STS 2379
STS 1944
STS 1325A
STS 1435
Tragelaphus strepsiceros
SF 046 D13
SF 1300 P46 8#2$–9#2$
STS 1573
STS 2121
Grazers
Antidorcas bondi
STS 1125
Connochaetes sp.
SF 114 H2 C. cf. taurinus
SF 112 H2 C. cf. taurinus
SF 334 D13 C. cf. taurinus
3.8
1.8
1.9
3.6
n.a.
2.0
2.9
3.7
1.8
2.0
2.9
N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597
591
Table 2 (continued)
13C (‰)
Taxon and specimen
Damaliscus sp.
SF 327 D13
SF 328 D13
SF 329 D13
SF 330 D13
SF 332 D13
Member
Method 1
M4
M4
M4
M4
M4
0.3
0.9
+0.7
+1.4
+2.3
+1.4
n.a.
+3.7
+3.5
+3.1
Mean (n = 5) = +1.91.7
0.6
+1.1
+1.9
+3.7
+3.3
n.a.
n.a.
Mean (n = 2) = 1.1
+0.1
2.2
+0.1
2.2
n.a.
n.a.
Mean (n = 2) = 2.3
2.1
2.5
2.1
2.5
Hippotragus equinus
STS 2599
STS 1630
Matrix
UCT 1832 breccia D13
UCT 2768 calcite D13
*
M4
M4
Method 2
Ave.
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
negative 13C values are those obtained for one
specimen each of Antidorcas recki (14‰), Parapapio sp. (10.8‰) and Tragelaphus strepsiceros
(10.3‰). Of these, A. recki was clearly a dedicated browser (mean 12.8‰, n = 4), with a diet
that probably consisted of shrubs. T. strepsiceros,
which prefers browse in most environments,
included some C4 grass in its diet in this case.
At the C4 end of the spectrum, the most positive
13C values are those for individual specimens of
Damaliscus sp. (+3.7‰), Hippotragus equinus
(+0.5‰) and Connochaetes sp. (0.5‰). Wherever these taxa have been compared, whether in
fossil or modern assemblages, 13C values for
Damaliscus sp. have invariably been more positive
than those for other grazers (Cerling et al., 1997;
Smith 1997). The diet of Damaliscus sp. includes
no browse and is apparently concentrated on the
subtypes of C4 grasses with the most positive 13C
values.
Based on these 13C values, the C3 and C4 end
members for Sterkfontein Member 4 can be estimated to lie at about 13‰ and +1‰; the latter is
a weighted average for the grazer 13C values
available for this time and place. When the 13C
values for modern animals from South Africa are
adjusted for industrial changes in the atmosphere
(by adding 1.5‰ to the measured values), the end
members are identical to those of Sterkfontein
Member 4.
Given a spectrum between 13‰ and +1‰
for the 13C values of fossil tooth enamel at
Sterkfontein, we can assess the diets of hominins
from Member 4. The average 13C value for ten
specimens that are attributed to Australopithecus
africanus is 6.91.3‰. Three specimens are
excluded from this average: their taxonomic status
is uncertain, as they are fragmentary and characterised by thin enamel (about 1.3 mm). Their 13C
values are more positive than those of the
undoubted australopithecines and they may be
representatives of Theropithecus oswaldi, the grazing baboon, for which one well-identified specimen
with a 13C value of 2.9‰ is available. The
average 13C value of about 7‰ for ten australopithecines represents a foodweb with about
60% C3 plants and 40% C4 plants at its base. This
result is similar to those for Swartkrans hominins,
although the average Sterkfontein C4 component
is larger by about 10 to 15%. Of more importance,
however, is the range of 13C values of the
Sterkfontein hominins, between 8.8‰ (about
30% C4) and 4.4‰ (about 60% C4). To this
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N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597
range one can add four measurements for australopithecines (A. africanus) from Makapansgat (ca.
3 Ma), which vary in 13C values from 10.7‰ to
5.3‰ (Sponnheimer and Lee-Thorp 1999). The
C3 and C4 end members for fossil fauna from
Sterkfontein Member 4 are slightly different from
those for Makapansgat (11‰ and +1‰); given
these end members, Makapansgat hominins had
diets with C4 components ranging from essentially
0 to 50%. Thus, two groups of hominin specimens
that have been attributed to the species Australopithecus africanus, from two different locations and
separated in time by perhaps as much as half a
million years, both had mixed diets with C4 components that varied very widely between individuals. This is an extraordinary result and deserves
close scrutiny.
Discussion
The carbon isotope data from Sterkfontein provide several significant results. As expected, the
isotopic signatures of known grazers (Damaliscus
sp., Connochaetes sp., Antidorcas bondi, and Hippotragus equinus) are at the positive (C4) end of the
spectrum. The C3 end of the spectrum, however, is
poorly represented. The only reliable browser in
the assemblage was Antidorcas recki, an extinct
springbok (mean 13C value 12.8‰). Tragelaphus strepsiceros, the extant greater kudu
(8.9‰), included some 30% of C4 plants in its
diet. In contrast, the published isotope data for
Makapansgat (Sponheimer and Lee-Thorp, 1999a)
include eleven species with 13C values at the C3
end of the spectrum.
It is necessary to consider the different bone
accumulation processes at Makapansgat and
Sterkfontein to interpret these isotope data
(Maguire et al., 1980). At Makapansgat, a variety
of carnivore species were able to drag their prey
into a large cave. The faunal remains in the talus
deposit of Sterkfontein member 4 were probably
washed into a narrow sinkhole, or were dropped
from trees overhead, e.g., by leopards. The
Makapansgat assemblage includes large browsing
species like giraffe and rhinoceros; although these
are juvenile specimens, they are nevertheless large
animals. It is unlikely, for example, that a leopard
could drag such prey into a tree. The scarcity of
browsing ungulates at Sterkfontein is underscored
by the carbon isotope data for Tragelaphus strepsiceros, the greater kudu, which had 30% C4 plants
in its diet. Greater kudu occur in a variety of
modern African biomes and are usually browsers.
Significant exceptions in our database, with C4
dietary components as high as 50%, are from the
Kalahari thornveld, where the browse is thorny,
and the southern Namib desert, where it is scarce.
Making due allowance for the different accumulation processes, the carbon isotope values for
the faunal assemblages from Makapansgat and
Sterkfontein Member 4 show that the environment
at Makapansgat was slightly more wooded (Luyt,
2001).
The baboons of Sterkfontein Member 4 occupied two distinct ecological niches. Three different
species may be represented among the results for
Parapapio sp.; they shared the C3 end of the
spectrum with the browsers. The single specimen
of Theropithecus oswaldi (2.9‰) had a diet that
included about 70% C4 plants. It is worth noting
that the ecological niches occupied by Parapapio
sp and T. oswaldi at Sterkfontein were still valid at
Swartkrans, half a million or more years later.
The most significant results from Sterkfontein
are those for specimens that have been attributed
to Australopithecus africanus. These are highly
variable, with 13C values for ten specimens varying between 8.8‰ and 4.4‰, a range of 4.4‰.
When the results for four Makapansgat specimens
(13C values between 10.7‰ and 5.3‰) are
added to those of Sterkfontein, this range is
extended to 6.3‰. (Also note that Stw 213i, of
which the hominin attribution is in contention, has
a 13C value of 1.8‰; its inclusion would extend
the range to 8.9‰). This is an extraordinary range
for any species.
An extensive isotope database for fossil and
modern African fauna is available by now, both
published and unpublished. The 13C values for a
single species at a given time and place are almost
invariably clustered more tightly than those for A.
africanus reported here. An exception is Aepyceros
melampus, the impala (Sponheimer et al., in
press), which is an unusual mixed feeder. Such
N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597
adaptability has made Aepyceros sp. an evolutionary success story in the Plio-Pleistocene and earned
modern impala the soubriquet of “the cockroaches
of Africa” in wildlife conservation circles.
Among extant non-human primates, the 13C
values for any given species in a single environment are tightly clustered around the mean (e.g.,
Schoeninger et al., 1997, 1999) and differences
between males and females are not particularly
noticeable. Thackeray et al., (1996) have measured
collagen 13C values of the modern baboon, Papio
cynocephalus ursinus in southern Africa. The specimens came from six different localities, with
environmental settings as varied as the Namib
desert, the Limpopo Valley, and the subtropical
savanna of Kwazulu-Natal. The total range for P.
cynocephalus ursinus across these six environments
is 5.7‰, but in any given environment the range is
less than 3‰. The range in 13C for this baboon
species across all of southern Africa, therefore,
is less than that for A. africanus at two sites
(Sterkfontein and Makapansgat) and only slightly
more than that for A. africanus at Sterkfontein
alone.
The variation in 13C values for P. cynocephalus
in any given area more closely resembles those for
the hominins A. robustus and Homo sp. at
Swartkrans. Recent measurements by van der
Merwe (unpublished) of carbon isotope ratios in
the tooth enamel of three specimens of A. robustus
from the nearby site of Drimolen (Keyser et al.,
2000), three specimens of Homo habilis from
Olduvai, Tanzania and two specimens of A. boisei
from Tanzania (Olduvai and Peninj) are similarly
constrained in their variability. All of these
hominins had significant (and different) C4 dietary
components, but A. africanus had much more
variation between individuals in the consumption
of C4-based foods.
C4-based foods can include C4 grasses and
sedges, the vertebrates and insects that eat these
plants, or the carnivores that eat the plant consumers. Carbon isotope ratios by themselves
cannot distinguish between these potential food
sources. Oxygen isotope ratios could be of some
help here, since they record the body water of
consumers. Early hominins from South and East
Africa have relatively low 18O values and show
593
similarities with suids, monkeys and carnivores,
but these similarities are as yet poorly understood
(Lee-Thorp et al., 2003). Oxygen isotope data for
Sterkfontein are reported elsewhere (Luyt, 2001
and in prep.)
Palaeoenvironmental changes could have contributed to the variability observed in the carbon
isotope ratios of Sterkfontein Member 4 hominins,
given that the assemblage accumulated over an
unknown period of time. The same degree of
variability is found, however, among the four
hominin specimens from Makapansgat, which are
from a different time and place.
We can conclude that Australopithecus africanus
at Sterkfontein had a well established C4 dietary
component, which may well have included all of
the available C4 food sources: grasses, particularly
seeds and rhizomes; C4 sedges (which have
starchy underground storage organs); invertebrates (including locusts and termites); grazing
mammals; and perhaps even insectivores and
carnivores. Whatever the sources were, different
individuals of this early hominin species differed
widely in their consumption of C4-based foods.
The range of 13C values for A. africanus is so wide
that it invites consideration of the idea that more
than one species of australopithecine is represented
in Sterkfontein Member 4. Clarke (1988) has
argued for the presence of a large-toothed, “prerobust” australopithecine and has identified five
potential specimens of this type among the ten
specimens we have analysed isotopically. These
five individuals are starred in Table 2 and Fig. 2
and can be seen to vary as much in 13C values as
the remaining five. It is our opinion that only one
species, A. africanus, was present; if so, it had the
most variable dietary behaviour of all the early
hominin species we have investigated. The alternative hypothesis would be that two hominin species
with equally unusual diets were present, which is
less plausible.
Conclusion
The stable carbon isotope ratios for ten specimens of A. africanus from Sterkfontein Member 4
show that this species of hominin had an unusually
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
foods. These could have included C4 grasses and
sedges and/or the insects and vertebrates that eat
these plants. The C4 dietary component varied
considerably from one individual to the next, with
a mean of about 40% and a range between about
30 and 60%. When the results for four specimens
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
wider than that observed for any other species of
early hominin, or indeed for any non-human
primate, fossil or modern. It indicates that A.
africanus was an exceptionally opportunistic
feeder: the ultimate in hominin adaptability. Such
adaptability would have contributed greatly to its
survival skills in the changing environments during
this crucial stage of human evolution.
These results show that hominins had become
savanna foragers for a significant part of their diet
by ca. 3 Ma. The critical point when they emerged
from the forest to sample savanna foods can only
be established if the newly-discovered “forest
hominins” of South and East Africa are subjected
to the same isotopic analysis.
Acknowledgements
The work reported here was done in the course
of fifteen years as members of the Archaeometry
Research Unit at the University of Cape Town
developed the methodology for measuring stable
carbon and oxygen isotope ratios in fossil tooth
enamel, particularly that of hominins. Many colleagues contributed to these developments, with
John Lanham playing a leading role: he set up
mass spectrometers and vacuum lines and kept
them running. For our study of Sterkfontein fossils, Alun Hughes and Ron Clarke helped to select
specimens for analysis, while Matt Sponheimer
and Ian Newton provided technical laboratory
assistance. Corli Coetsee produced the figures.
Funds were provided by the National Research
Foundation of South Africa and the American
School of Prehistoric Research, Harvard Peabody
Museum.
Two palaeoanthropologists supported our isotopic approach to dietary analysis from the start
and allowed us to analyse hominin teeth from
Swartkrans and Sterkfontein, even though the
sample requirement was relatively large in the
early days. They are Bob Brain and Phillip Tobias.
We dedicate this article to them, with appreciation.
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