Stable isotopes in fossil hominin tooth enamel suggest a fundamental dietary shift in the Pliocene

Abstract

Accumulating isotopic evidence from fossil hominin tooth enamel has provided unexpected insights into early hominin dietary ecology. Among the South African australopiths, these data demonstrate significant contributions to the diet of carbon originally fixed by C(4) photosynthesis, consisting of C(4) tropical/savannah grasses and certain sedges, and/or animals eating C(4) foods. Moreover, high-resolution analysis of tooth enamel reveals strong intra-tooth variability in many cases, suggesting seasonal-scale dietary shifts. This pattern is quite unlike that seen in any great apes, even 'savannah' chimpanzees. The overall proportions of C(4) input persisted for well over a million years, even while environments shifted from relatively closed (ca 3 Ma) to open conditions after ca 1.8 Ma. Data from East Africa suggest a more extreme scenario, where results for Paranthropus boisei indicate a diet dominated (approx. 80%) by C(4) plants, in spite of indications from their powerful 'nutcracker' morphology for diets of hard objects. We argue that such evidence for engagement with C(4) food resources may mark a fundamental transition in the evolution of hominin lineages, and that the pattern had antecedents prior to the emergence of Australopithecus africanus. Since new isotopic evidence from Aramis suggests that it was not present in Ardipithecus ramidus at 4.4 Ma, we suggest that the origins lie in the period between 3 and 4 Myr ago.

Figure 1.

Data for all the South African hominins are summarized as means δ¹³C (black boxes) and standard deviations compared with means and standard deviations for the browsing and grazing fauna. The sites are given in sequence from oldest (top) to youngest (bottom). Makapansgat Member 3 is about 2.7–3 Ma, Sterkfontein Member 4 is usually considered to be about 2.2–2.5 Ma and Swartkrans Member 1 is younger than 2 Ma. These ages based on biostratigraphy are imprecise, but sufficient for our purposes. More precise chronometric studies based on Pb/U isotopes have recently been completed (R. Pickering 2009, personal communication), but do not change the overall sequence. All the hominin data show significant C₄ contributions compared with C₃ feeders, in spite of large shifts, from closed to open, in the environments (Reed 1997). Adapted from Lee-Thorp & Sponheimer (2006).

Figure 2.

High-resolution laser ablation δ¹³C sequences for (a) A. africanus and (b) P. robustus plotted against sample (scan) number. Sample increments were approximately 0.3 mm. The Paranthropus data are from Sponheimer et al. (2006b), where the data were plotted according to a time-sequence model based on perikymata counts. In this case, we avoided the application of a time sequence based on perikymata because the lengthy maturation time introduces not only a longer time period but also more uncertainty. (a) Open diamonds, STS 2518 max RM3; filled circles, STS 31 max RM3; filled triangles, STS 2253 mand RM1. (b) Open diamonds, SKW 6427 M; filled circles, SKW 5939 M; filled triangles, SK 24606 RM2 or 3; squares with crosses, SK 24606 RM3.

Figure 3.

A summary comparison of the hominin data for Aramis (above), and Makapansgat (below), plotted as means (black boxes) and standard deviations with mean values for C₃ and C₄ feeders shown for comparison. Data for carnivores (hyaenids) are also shown (white boxes; n = 2 for Makapansgat), because they are effectively integrators for the values of all the fauna they consume. These data are shifted towards values more enriched in ¹³C in Aramis, suggesting more open, C₄ elements in the environment compared with Makapansgat, where the faunal assemblage consists largely of C₃ feeders. In spite of this difference, Ar. ramidus remains relatively depleted in ¹³C, quite unlike the patterns for A. africanus seen at Makapansgat. Data for Aramis are from White et al. (2009b), and for Makapansgat are from Sponheimer (1999).

Figure 4.

Bivariate δ¹³C and δ¹⁸O comparisons of similar taxa in (a) Aramis and (b) Makapansgat shown as means and standard deviations. Several significant differences are observed. On average, δ¹⁸O values for Makapansgat fauna are about 2‰ lower than at Aramis, which is consistent with their relative geographical positions and associated values for hydrology. However, the Aramis data are more variable, with some exceptional and unusually low values for Deinotherium in particular. Australopithecus africanus data are relatively enriched in ¹³C and depleted in ¹⁸O, and occupy the same isotopic ‘space’ as the hyaenids, quite unlike Ar. ramidus. The other primate species are also more enriched in ¹³C, unlike Aramis, but the impala (Aepyceros) has higher δ¹³C values at Aramis. Although impalas are generally considered to be mixed feeders, a recent study showed high δ¹³C and almost exclusive grazing habits for Aepyceros in the nutritious grasslands of Rwanda (Copeland et al. 2009). The data for Nyanzochoerus at Aramis are remarkably similar to those for the Suidae at Makapansgat, suggesting a similar ecological niche. Data for Aramis are from White et al. (2009b) and for Makapansgat from Sponheimer (1999).