The carbon isotope ecology and diet of australopithecus africanus at sterkfontein, south africa (van der merwe et al.)


Published on

Published in: Technology, Business
  • Be the first to comment

  • Be the first to like this

No Downloads
Total views
On SlideShare
From Embeds
Number of Embeds
Embeds 0
No embeds

No notes for slide

The carbon isotope ecology and diet of australopithecus africanus at sterkfontein, south africa (van der merwe et al.)

  1. 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: (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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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 wider than that observed for any other species of References early hominin, or indeed for any non-human primate, fossil or modern. It indicates that A. Backwell, L.R., d’Errico, F., 2000. First evidence for termite foraging by Swartkrans early hominids. Proceedings of the africanus was an exceptionally opportunistic National Academy of Science 98, 1358–1363. feeder: the ultimate in hominin adaptability. Such Bamford, M., 1999. Pliocene fossil wood from an early hominid adaptability would have contributed greatly to its cave deposit, Sterkfontein, South Africa. South African survival skills in the changing environments during Journal of Science 95, 231–237. this crucial stage of human evolution. Berger, L.R., Lacruz, R.S., de Ruiter, D.J., 2002. Revised estimates of Australopithecus bearing deposits at These results show that hominins had become Sterkfontein, South Africa. American Journal of Physical savanna foragers for a significant part of their diet Anthropology 119, 192–197. by ca. 3 Ma. The critical point when they emerged Brunet, M., Beauvilain, A., Coppens, Y., Heintz, E., Montaye, from the forest to sample savanna foods can only A.H.E., Pilbeam, D., 1995. The first australopithecine 2,500 be established if the newly-discovered “forest kilometers west of the Rift Valley (Chad). Nature 378, 273–275. hominins” of South and East Africa are subjected Bocherens, H., Billiou, D., Mariotti, A., Pathou-Mathis, M., to the same isotopic analysis. Otte, M., Bonjean, D., Toussaint, M., 1999. Palaeoenviron- mental and palaeodietary implications of isotopic bio- geochemistry of last interglacial Neanderthal and mammal bones in Scladina Cave (Belgium). Journal of Acknowledgements Archaeological Science 26, 599–607. Bocherens, H., Koch, P., Mariotti, A., Geraads, D., Jaeger, J., 1996. Isotopic biogeochemistry (13C, 18O) of mammalian The work reported here was done in the course enamel from African Pleistocene hominid sites. Palaios 11, of fifteen years as members of the Archaeometry 306–318. Research Unit at the University of Cape Town Brain, C.K., 1958. The Transvaal Ape-man Bearing Cave developed the methodology for measuring stable Deposits, Transvaal Museum Memoir No. 11. Transvaal Museum, Pretoria. carbon and oxygen isotope ratios in fossil tooth Brain, C.K., 1981. The Hunters or the Hunted? An Introduc- enamel, particularly that of hominins. Many col- tion to African Cave Taphonomy. University of Chicago leagues contributed to these developments, with Press, Chicago. John Lanham playing a leading role: he set up Brain, C.K., 1993. Swartkrans: a Cave’s Chronicle of Early mass spectrometers and vacuum lines and kept Man, Transvaal Museum Monographs. Transvaal Museum, Pretoria. them running. For our study of Sterkfontein fos- Broom, R., Schepers, G.W.H., 1946. The South African sils, Alun Hughes and Ron Clarke helped to select fossil ape-men, the Australopithecinae, Transvaal Museum specimens for analysis, while Matt Sponheimer Memoir No. 2. Transvaal Museum, Pretoria. and Ian Newton provided technical laboratory Broom, R., Robinson, J.T., Schepers, G.W.H., 1950. assistance. Corli Coetsee produced the figures. Sterkfontein Ape-man, Plesianthropus, Transvaal Museum Memoir No. 4. Transvaal Museum, Pretoria. Funds were provided by the National Research Cerling, T.E., Harris, J.M., 1999. Carbon isotope fractionation Foundation of South Africa and the American between diet and bioapatite in ungulate mammals and School of Prehistoric Research, Harvard Peabody implications for ecological and paleoecologtical studies. Museum. Oecologia 120, 347–363.
  15. 15. N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597 595 Cerling, T.E., Harris, J.M., Ambrose, S.H., Leakey, M.G., Grine, F.E., 1981. Trophic differences between gracile and Solounias, N., 1997. Dietary and environmental reconstruc- robust australopithecines. South African Journal of Science tion with stable isotope analyses of herbivore tooth enamel 77, 203–230. from the Miocene locality of Fort Ternan, Kenya. Journal Grine, F.E., Kay, R.F., 1988. Early hominid diets from of Human Evolution 33, 635–650. quantitative image analysis of dental microwear. Nature Cerling, T.E., Harris, J.M., MacFadden, B.J., Leakey, M.G., 333, 765–768. Quade, J., Eisenmann, V., Ehleringer, J.R., 1997. Global Hattersley, P.W., 1982. 13C values of C4 types of grasses. vegetation change through the Miocene/Pliocene boundary. Australian Journal of Plant Physiology 9, 139–154. Nature 389, 153–158. Hattersley, P.W., 1992. C4 photosynthetic pathway variation in Cerling, T.E., Wang, Y., Quade, J., 1993. Expansion of C4 grasses (Poaceae): its significance for arid and semi-arid ecosystems as an indicator of global ecological change in the lands. In: Chapman, G.P. (Ed.), Desertified Grasslands: late Miocene. Nature 361, 344–345. Their Biology and Management. The Linnean Society, Clarke, R.J., 1988. A new Australopithecus cranium from London, pp. 181–212. Sterkfontein and its bearing on the ancestry of Hughes, A.R., Tobias, P.V., 1977. A fossil skull probably of the Paranthropus. In: Grine, F.E. (Ed.), Evolutionary History genus Homo from Sterkfontein, Transvaal. Nature 265, of the Robust Australopithecines. Aldine de Gruyter, New 310. York, pp. 285–292. Johanson, D.C., White, T.D., 1979. A systematic assessment of Clarke, R.J., 1998. First ever discovery of a well-preserved skull early African hominids. Science 202, 321–330. and associated skeleton of Australopithecus. South African Johanson, D.C., Edey, M.A., 1981. Lucy, the Beginning of Journal of Science 94, 463. Humankind. Granada, London. Clarke, R.J., 2002a. On the unrealistic “revised age estimates” Johanson, D., Edgar, B., 1996. From Lucy to Language. for Sterkfontein. South African Journal of Science 98, University of the Witwatersrand Press, Johannesburg. 415–418. Katzenberg, M.A., 2000. Stable isotope analysis: a tool for Clarke, R.J., 2002b. Newly revealed information on the studying past diet, demography, and life history. In: Sterkfontein Member 2 Australopithecus skeleton. South Katzenberg, M.A., Saunders, S.R. (Eds.), Biological African Journal of Science 98, 523–526. Anthropology of the Human Skeleton. Wiley-Liss, New Clarke, R.J., Kuman, K. 1998. The Sterkfontein caves: York, pp. 305–327. palaeontological and archaeological sites. In Clarke, R.J., Keyser, A., Menter, C.G., Moggi-Cecchi, J., Pickering, T.R., Kuman, K., Brain, C.K., Tobias, P.V., Thackeray, J.F., Berger, L.R., 2000. Drimolen: a new hominid-bearing site in (compilers). Mid-Congress Excursion Handbook, pp. 3–20. Gauteng, South Africa. South African Journal of Science Dual Congress ’98: International Associations of Human 96, 193–197. Palaeontologists and Human Biologists. Pretoria: Desktop Creations. Kuman, K., 1994. The archaeology of Sterkfontein – past and Clarke, R.J., Kuman, K. 2000. The Sterkfontein Caves present. Journal of Human Evolution 27, 471–495. palaeontological and archaeological site. University of the Kuman, K., Clarke, R.J., 2000. Stratigraphy, artefact industries Witwatersrand, pamphlet, 18pp. and hominid associations for Sterkfontein, Member 5. Coppens, Y., 1983. Le singe, l’Afrique et l’Homme. Fayard, Journal of Human Evolution 38, 827–847. Paris. Leakey, L.S.B., 1959. A new fossil skull from Olduvai. Nature Coppens, Y., 1994. East Side Story: the origin of humankind. 184, 491–493. Scientific American 270, 62–69. Leakey, L.S.B., Tobias, P.V., Napier, J., 1964. A new Dart, R.A., 1925. Australopithecus africanus: the man-ape of species of the genus Homo from Olduvai Gorge. Nature South Africa. Nature 115, 195–199. 202, 7–9. Dart, R.A., 1926. Taungs and its significance. Natural History Leakey, M.G., Spoor, F., Brown, F.H., Gathogo, P.N., Kiarie, 26, 315–327. C., Leakey, L.N., McDougall, I., 2001. New hominin genus Dart, R.A., 1957. The osteodontokeratic culture of Australo- from eastern Africa shows diverse middle Pliocene lineages. pithecus prometheus, Transvaal Museum Memoir No. 10. Nature 410, 433–440. Transvaal Museum, Pretoria. Lee-Thorp, J.A. 1989. Stable carbon isotopes in deep time. Ehleringer, J.R., Cooper, T.A., 1988. Correlations between University of Cape Town, unpublished doctoral carbon isotope ratio and microhabitat in desert plants. dissertation. Oecologia 76, 562–566. Lee-Thorp, J.A., van der Merwe, N.J., 1987. Carbon isotope Ehleringer, J.R., Field, C.B., Lin, Z.F., Kuo, C.Y., 1986. Leaf analysis of fossil bone apatite. South African Journal of carbon isotope and mineral composition in subtropical Science 83, 712–715. plants along an irradiance cline. Oecologia 70, 520–526. Lee-Thorp, J.A., van der Merwe, N.J., 1991. Aspects of the Friedli, H., Lotscher, H., Oeschger, H., Siegenthaler, U., chemistry of fossil and modern biological apatites. Journal Stauffer, B., 1986. Ice core record of the 13C/12C ratio of of Archaeological Science 18, 343–354. atmospheric CO2 in the past two centuries. Nature 324, Lee-Thorp, J.A., van der Merwe, N.J., 1993. Stable carbon 237–238. isotope studies of Swartkrans fossils. In: Brain, C.K. (Ed.),
  16. 16. 596 N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597 Swartkrans, A Cave’s Chronicle of Early Man, Transvaal Vindija and Neanderthal predation: the evidence from Museum Monographs. Transvaal Museum, Pretoria, pp. stable isotopes. Proceedings of the National Academy of 251–256. Science 97, 7663–7666. Lee-Thorp, J.A., Manning, L., Sponheimer, M., 1997. Explor- Robinson, J.T., 1954. Prehominid dentition and hominid ing problems and opportunities offered by down-scaling evolution. Evolution 8, 324–334. sample sizes for carbon isotope analyses of fossils. Bulletin Schoeninger, M., Moore, K., 1992. Bone stable isotope de la Societe Geologique de France 168, 767–773. ` studies in archaeology. Journal of World Prehistory 6, Lee-Thorp, J.A., Sealy, J.C., van der Merwe, N.J., 1989. Stable 247–296. carbon isotope ratio differences between bone collagen and Schoeninger, M., Iwaniec, U.T., Glander, K.E., 1997. Stable bone apatite, and their relationship to diet. Journal of isotope ratios indicate diet and habitat use of New World Archaeological Science 18, 585–599. monkeys. American Journal of Physical Anthropology 103, Lee-Thorp, J.A., Sponheimer, M., van der Merwe, N.J., 2003. 69–83. What do stable isotopes tell us about hominid dietary and Schoeninger, M., Moore, J., Sept, J.M., 1999. Subsistence ecological niches in the Pliocene? International Journal of strategies of two “savanna” chimpanzee populations: the Osteoarchaeology 13, 104–113. stable isotope evidence. American Journal of Primatology Lee-Thorp, J.A., Thackeray, J.F., van der Merwe, N.J., 2000. 49, 297–314. The hunters and the hunted revisited. Journal of Human Smith, J. 1997. Stable isotope analysis of fauna and soils from Evolution 39, 565–576. sites in the eastern Free State and western Lesotho, south- Lee-Thorp, J.A., van der Merwe, N.J., Brain, C.K., 1994. Diet ern Africa. University of Cape Town, unpublished master’s of Australopithecus robustus and associated fauna from thesis. Swartkrans. Journal of Human Evolution 27, 361–372. Sponheimer, M. 1999. Isotopic ecology of the Makapansgat Luyt, J. 2001. Revisiting palaeoenvironments from the Limeworks fauna. Rutgers University, doctoral disserta- hominid-bearing Plio-Pleistocene sites: New isotopic tion. Ann Arbor, MI: University Microfilms. evidence from Sterkfontein. University of Cape Town, Sponheimer, M., Lee-Thorp, J.A., 1999a. Isotopic evidence for unpublished master’s thesis. the diet of an early hominid, Australopithecus africanus. Maguire, J.M., Pemberton, D., Collett, M.H., 1980. The Science 283, 368–370. Makapansgat Limeworks grey breccia: hominids, hyenas, Sponheimer, M., Lee-Thorp, J.A., 1999b. Oxygen isotope hystricids or hillwash? Palaeontologia Africana 23, 75–98. ratios in enamel carbonate and their ecological significance. Marino, B.D., McElroy, M.B., 1991. Isotopic composition of Journal of Archaeological Science 26, 723–728. atmospheric CO2 inferred from carbon in plant cellulose. Sponheimer, M., Grant, C.C., de Ruiter, D., Lee-Thorp, J.A., Nature 349, 127–131. Codron, C., Codron, J. in press. Diets of impala from Partridge, T.C., 2002. Untitled comment in “News and Views”. Kruger National Park: evidence from stable carbon iso- South African Journal of Science 98, 418–419. topes. Koedoe. Partridge, T.C., Watt, I.B., 1991. The stratigraphy of the Sullivan, C.H., Krueger, H.W., 1981. Carbon isotope analysis Sterkfontein hominid deposit and its relationship to the of separate phases in modern and fossil bone. Nature 292, underground cave system. Palaeontologia Africana 28, 333–335. 35–40. Sullivan, C.H., Krueger, H.W., 1983. Carbon isotope ratios of Partridge, T.C., Shaw, J., Heslop, D., 2000a. Note on recent bone apatite and animal diet reconstruction. Nature 301, magnetostratigraphic analyses of Member 2 of the 177. Sterkfontein Formation. In: Partridge, T.C., Maud, R.R. Thackeray, J.F., Henzi, S.P., Brain, C., 1996. Stable carbon and (Eds.), The Cenozoic of southern Africa. Oxford University nitrogen isotope analysis of bone collagen in Papio cyno- Press, New York, pp. 129–130. cephalus ursinus: comparison with ungulates and Homo Partridge, T.C., Latham, A.G., Heslop, D., 2000b. Appendix sapiens from southern and East African environments. on magnetostratigraphy of Makapansgat, Sterkfontein, South African Journal of Science 92, 209–212. Taung and Swartkrans. In: Partridge, T.C., Maud, R.R. Tieszen, L.L., 1991. Natural variation in the carbon isotope (Eds.), The Cenozoic of southern Africa. Oxford University values of plants: implications for archaeology, ecology and Press, New York, pp. 126–129. paleoecology. Journal of Archaeological Science 18, Pickford, M., Senut, B., 2001. “Millennium Ancestor”, a 227–248. 6-million year old bipedal hominid from Kenya. South van der Merwe, N.J., 1982. Carbon isotopes, photosynthesis, African Journal of Science 97, 22. and archaeology. American Scientist 70, 596–606. Quade, J., Cerling, T.E., Barry, J.C., Morgan, M.E., Pilbeam, van der Merwe, N.J., Medina, E., 1989. Photosynthesis and 13 D.R., Chivas, A.R., Lee-Thorp, J.A., van der Merwe, N.J., C/12C ratios in Amazonian rain forests. Geochimica et 1992. A 16-Ma record of paleodiet using carbon and oxygen Cosmochimica Acta 53, 1091–1094. isotopes in fossil teeth from Pakistan. Chemical Geology van der Merwe, N.J., Thackeray, J.F., 1997. Stable carbon (Isotope Geoscience Section) 94, 183–192. isotope analysis of Plio-Pleistocene ungulate teeth from Richards, M.P., Pettitt, P.B., Trinkhaus, E., Smith, F.H., Sterkfontein, South Africa. South African Journal of Paunovic, M., Karavanic, I., 2000. Neanderthal diet at Science 93, 194.
  17. 17. N.J. van der Merwe et al. / Journal of Human Evolution 44 (2003) 581–597 597 van der Merwe, N.J., Vogel, J.C., 1978. 13C content of human Vrba, E.S., 1995. The fossil record of African antelopes collagen as a measure of prehistoric diet in woodland North (Mammalia, Bovidae) in relation to human evolution America. Nature 276, 815–816. and paleoclimate. In: Vrba, E.S. (Ed.), Paleoclimate Vogel, J.C., van der Merwe, N.J., 1977. Isotopic evidence for and Evolution, With Emphasis on Human Origins. Yale early maize cultivation in New York State. American University Press, New Haven, pp. 385–424. Antiquity 42, 238–242. White, T.D., Suwa, G., Asfaw, B., 1994. Australopithecus Vrba, E.S., 1976. The Fossil Bovidae of Sterkfontein, ramidus, a new species of early hominid from Aramis, Swartkrans and Kromdraai, Transvaal Museum Memoir Ethiopia. Nature 371, 306–312. No. 21. Transvaal Museum, Pretoria. White, T.D., Suwa, G., Simpson, S., Asfaw, B., 2000. Jaws and Vrba, E.S., 1982. Biostratigraphy and chronology based par- teeth of A. afarensis from Maka, Middle Awash, Ethiopia. ticularly on Bovidae of southern hominid associated American Journal of Physical Anthropology 111, 45–68. assemblages. In: de Lumley, H., de Lumley, M.-A. (Eds.), Proc. Congres International de Palaeontologie Humaine. Vol. 2. Nice, France, pp. 707–752.