Matt Sponheimer, Julia A. Lee-Thorp

Science Jan 15 1999: 368-370.

Current consensus holds that the 3-million-year-old hominid Australopithecus africanus subsisted on fruits and leaves, much as the modern chimpanzee does. Stable carbon isotope analysis of A. africanus from Makapansgat Limeworks, South Africa, demonstrates that this early hominid ate not only fruits and leaves but also large quantities of carbon-13-enriched foods such as grasses and sedges or animals that ate these plants, or both. The results suggest that early hominids regularly exploited relatively open environments such as woodlands or grasslands for food. They may also suggest that hominids consumed high-quality animal foods before the development of stone tools and the origin of the genus Homo.

M. Sponheimer, Department of Anthropology, Rutgers University, New Brunswick NJ 08901-1414, USA, and Department of Archaeology, University of Cape Town, Private Bag, Rondebosch 7701, Republic of South Africa. J. A. Lee-Thorp, Department of Archaeology, University of Cape Town, Private Bag, Rondebosch 7701, Republic of South Africa.

Little is known about the diets of hominids that predate the genus Homo, because they did not leave archaeological traces such as "kitchen middens" and stone tools. Consequently, researchers have made dietary inferences based on craniodental morphology (1-4), gross dental wear (1, 2, 5), and dental microwear (6, 7). Some researchers have stressed the importance of animal foods in the diets of these hominids (1, 8, 9); others have suggested that they were primarily adapted for the consumption of plant foods such as grass seeds and roots (3, 4). The current consensus, however, is that these early hominids ate fleshy fruits and leaves (6, 7, 10, 11). This agrees with evidence that they occupied relatively heavily wooded habitats, not open savannas (12-16). In contrast, there is evidence suggesting that the later hominids (~2.5 million years ago) Homo and Paranthropus inhabited more open environments (13, 16) and were omnivorous (17-20). Here we provide direct isotopic evidence of the diet of an early hominid, the 3-million-year-old Australopithecus africanus from Makapansgat Limeworks in Northern Province, South Africa (13, 16, 21).

Previous studies have shown that the ratio of ¹³C to ¹²C in tooth enamel can be used to provide dietary information about extinct fauna (19, 22). The foundation of this approach is our knowledge of photosynthesis in plants. Trees, bushes, shrubs, and forbs (C₃ plants) discriminate more markedly against the heavy ¹³C isotope during fixation of CO₂ than do tropical grasses and sedges (C₄ plants). As a result, C₃ plants have ¹³C values of -22 per mil () to -30, with an average of about -26.5 (23), whereas C₄ plants have ¹³C values of -10 to -14, with an average of about -12.5 (24, 25). Animals incorporate their food's carbon into their tooth enamel with some additional fractionation (26). Hence, the relative proportions of C₃ and C₄ vegetation in an animal's diet can be determined by analyzing its tooth enamel with stable isotope mass spectrometry. Animals that eat C₃ vegetation (including fruits, leaves, and the roots of trees, bushes, and forbs) have ¹³C values between about -10 and -16; animals that eat C₄ tropical grasses (including blades, seeds, and roots) have ¹³C values between 2 and -2; and mixed feeders that eat both fall somewhere in between these two extremes. Carnivores have tooth enamel ¹³C values similar to those of their prey (26).

We sampled molar tooth enamel from 4 of the 14 A. africanus individuals (MLD 12, MLD 28, MLD 30, and MLD 41) that have been unearthed at Makapansgat. We also analyzed the enamel of associated 3-million-year-old fauna (65 individuals from 19 mammalian taxa) in order to place A. africanus within a broader ecological context (Table 1) (27). Makapansgat's C₄ consumers (grazing taxa) include the equid Hipparion lybicum; the suid Notochoerus capensis; and the bovids Parmularius braini, Parmularius sp. nov., and Redunca darti. The C₃ consumers (browsers and browser/frugivores) include the giraffid Giraffa jumae; the rhinocerotid Diceros bicornis; the chalicothere Ancylotherium hennigi; and the bovids Tragelaphus sp. aff. angasi, T. pricei, Oreotragus cf. oreotragus, and Cephalophus sp. The bovids Makapania broomi and Simatherium cf. kohllarseni are the only mixed feeders that we analyzed. Aepyceros sp., Gazella gracilior, and G. vanhoepeni were all C₃ consumers (28), despite the fact that their extant kin are generally mixed feeders. This demonstrates the danger of assuming that fossil taxa had the same diets as their closest extant relatives.

Table 1. Mean 13C values, ranges, standard deviations, and number of individuals we sampled for each taxon from Makapansgat Member 3. Modern cercopithecids are also included for comparison. Permanent molars were sampled, except for larger species such as Diceros bicornis, from which mostly juvenile dentition was available (23). Species Mean () Range SD n C4 plant consumers Hipparion lybicum -0.8 0.2  to  -2.0 0.9 5 Notochoerus capensis -0.8 -0.6  to  -1.0 0.3 2 Parmularius braini 0.7 1.2  to  -0.2 0.7 4 Parmularius sp. nov. 0.7 1.3  to  -0.2 0.8 3 Redunca darti -1.3 1.3  to  -4.5 2.4 4 C3 plant consumers Aepyceros sp. -12.2 -11.0  to  -13.0 1.1 3 Ancylotherium hennigi -10.3 -10.1  to  -10.6 0.3 3 Cephalophus sp. -11.5 -11.4  to  -11.6 0.1 2 Diceros bicomis -11.6 -10.8  to  -13.1 1.3 3 Gazella gracilior -11.6 -10.7  to  -12.4 1.2 2 Gazella vanhoepeni -11.9 -10.9  to  -12.8 0.9 4 Giraffa jumae -11.3 -10.5  to  -12.6 0.8 7 Neotragini sp. -11.6 -11.2  to  -12.4 0.5 4 Oreotragus cf. oreotragus -11.6 -11.4  to  -11.7 0.2 2 Tragelaphus sp. aff. angasi -11.7 -9.5  to  -12.7 1.5 4 Tragelaphus pricei -11.8 -10.9  to  -12.5 0.8 3 Mixed C3 and C4 consumers Makapania broomi -3.4 -1.0  to  -5.3 1.8 4 Simatherium cf. kohllarseni -4.0 -3.4  to  -4.4 0.5 4 Carnivores Hyaena makapani -8.7 -8.1  to  -9.3 0.8 2 Primates A. africanus -8.2 -5.6  to  -11.3 2.4 4 Modern primates Papio cynocephalus ursinus -12.3 -10.3  to  -14.2 1.1 17 Cercopithecus aethiops -12.1 -7.8  to  -14.3 3.7 3

Analysis of variance shows that the ¹³C values for A. africanus are significantly different from the values for grazers, browsers, and mixed feeders from Makapansgat (P < 0.01) (Table 1). The only taxon from which they are not significantly different is the carnivore Hyaena makapani. Three of the four hominid specimens (MLD 12, MLD 28, and MLD 30) fall outside the range of C₃ (fruit, herb, or leaf) feeders at Makapansgat. MLD 30 is so enriched in ¹³C (-5.6) that it falls closer to the mean of the grazers than of the browsers. The ¹³C values for these specimens are inconsistent with a diet of fruits and leaves (C₃ plants). One specimen (MLD 41), however, does fall within the range of C₃ eaters. These data show that (i) A. africanus had a highly variable diet (its range of ¹³C values is greater than 18 of the 19 other taxa analyzed), and (ii) the majority of the Makapansgat hominids habitually obtained dietary carbon from C₄ plants such as grasses and sedges or from animals that ate C₄ foods, or both.

Modern South African cercopithecids that range into open woodland and grassland (Cercopithecus aethiops and Papio cynocephalus ursinus) can become similarly enriched in ¹³C, though they usually have nearly 100% C₃ diets (Table 1). Ecological studies of Papio have shown that grasses can be a dominant component of its diet, particularly in areas with little tree cover and during the dry season (9, 29). Field studies suggest that the only modern primates that consistently consume as much or more C₄ foods than A. africanus are Theropithecus gelada (9, 30), Erythrocebus patas (31), and P. hamadryas (32), all of which inhabit areas with few trees. In contrast, the majority of the Makapansgat hominids consumed somewhere between 25 and 50% C₄ foods despite a relatively high density of trees in the ancient Makapansgat Valley (12, 13, 16).

This raises the following question: Why did the Makapansgat hominids exploit C₄ resources to such an extent, despite an abundance of C₃ resources as well as evidence that they may have been well adapted for foraging in trees (33, 34)? C₃ feeders are abundant at Makapansgat (16), so it is possible that A. africanus minimized competition by foraging for C₄ grasses and sedges, particularly during the dry season when a large portion of available nutrition is found in their roots (which cannot be readily accessed by most animals). An equally plausible explanation is that A. africanus had a preference for high-quality animal foods, which included C₄ plant-eating insects such as Trinervitermes trinervoides or the young of grazing mammals like R. darti, or both. There is limited evidence to help us decide whether one or both of these alternatives is correct. Researchers comparing the dental microwear of A. africanus and modern primates did not conclude that these hominids ate grasses (6, 7), but these studies included no grass-eating modern primates. A comparison of the dental microwear of A. africanus and modern Papio populations from open environments, whose diet is 25 to 50% grasses (9), would be ideal, but no such study has been undertaken. Recent research demonstrates, however, that the percentage of pitting versus scratching on the molars of modern T. gelada (~10%) (35) is different from the percentage previously reported for A. africanus (~30%) (7). Theropithecus gelada consumes grass blades, seeds, and roots nearly exclusively (9, 30), making it a less than ideal analog for a hominid eating 25 to 50% grass foods. Nonetheless, the large difference in microwear features between Theropithecus and A. africanus suggests that we must seriously consider the possibility that these hominids were ¹³C-enriched because they consumed animal foods.

Carbon isotope analysis of 1.8- to 1.0-million-year-old Paranthropus robustus from Swartkrans in South Africa demonstrates that it too is enriched in ¹³C as compared to pure C₃ consumers (19). The mean ¹³C value for A. africanus (-8.2) is very similar to the mean for P. robustus (-8.5), although the range for the Makapansgat hominids is greater (5.7, as compared to 3.2). This is surprising because P. robustus lived in an area with more abundant C₄ grasses (13, 16) and, concomitantly, animals that ate C₄ grasses. This similarity in ¹³C values, combined with the fact that the craniodental specialization of P. robustus may be in an incipient state in A. africanus (2, 36), might mean that these species ate similar food items but that the further specialized P. robustus ate them more efficiently. Thus, P. robustus may have included a higher proportion of tough, fibrous foods in its diet (6, 7) and may have orally processed foods (such as Sclerocarya nuts) that A. africanus could only access with hammerstones (like chimpanzees use today) (37). Presently there is no evidence that A. africanus used tools, although it is not unreasonable to assume that they could have used tools in the same manner as chimpanzees do today. Despite this, it is suggestive that the last appearance date of Australopithecus and the first appearance date of Paranthropus are close in time (~2.5 million years ago) (13, 16, 38). It is possible that P. robustus was better able to process foods that A. africanus also favored, contributing to the latter's eventual extinction.

It is believed that the encephalization of early Homo was made possible by the consumption of energy- and nutrient-rich animal foods to "pay" for its metabolically expensive brain (39, 40). Our results raise the possibility, however, that dietary quality improved (through the consumption of animal foods) before the development of Homo (41) and stone tools (42) about 2.5 million years ago. Moreover, trace element (Sr/Ca) (43) and stable carbon isotope analyses (44) do not seem to indicate that early Homo from Swartkrans consumed more animal foods than did A. africanus. Therefore, the primary dietary difference between A. africanus and Homo may not have been the quality of their food but their manner of procuring it. One key difference may have been that stone tools allowed Homo to disarticulate bones and exploit bone marrow from large carcasses (obtained through hunting or scavenging) that A. africanus could not (17, 18, 45).

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9 September 1998; accepted 18 November 1998

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