Reconstructing the detailed dietary behaviour of extinct hominins is challenging1—particularly for a species such as Australopithecus africanus, which has a highly variable dental morphology that suggests a broad diet2,3. The dietary responses of extinct hominins to seasonal fluctuations in food availability are poorly understood, and nursing behaviours even less so; most of the direct information currently available has been obtained from high-resolution trace-element geochemical analysis of Homo sapiens (both modern and fossil), Homo neanderthalensis4 and living apes5. Here we apply high-resolution trace-element analysis to two A. africanus specimens from Sterkfontein Member 4 (South Africa), dated to 2.6–2.1 million years ago. Elemental signals indicate that A. africanus infants predominantly consumed breast milk for the first year after birth. A cyclical elemental pattern observed following the nursing sequence—comparable to the seasonal dietary signal that is seen in contemporary wild primates and other mammals—indicates irregular food availability. These results are supported by isotopic evidence for a geographical range that was dominated by nutritionally depauperate areas. Cyclical accumulation of lithium in A. africanus teeth also corroborates the idea that their range was characterized by fluctuating resources, and that they possessed physiological adaptations to this instability. This study provides insights into the dietary cycles and ecological behaviours of A. africanus in response to food availability, including the potential cyclical resurgence of milk intake during times of nutritional challenge (as observed in modern wild orangutans5). The geochemical findings for these teeth reinforce the unique place of A. africanus in the fossil record, and indicate dietary stress in specimens that date to shortly before the extinction of Australopithecus in South Africa about two million years ago.
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
Balter, V., Braga, J., Télouk, P. & Thackeray, J. F. Evidence for dietary change but not landscape use in South African early hominins. Nature 489, 558–560 (2012).
Ungar, P. S. & Sponheimer, M. The diets of early hominins. Science 334, 190–193 (2011).
Copeland, S. R. et al. Strontium isotope evidence for landscape use by early hominins. Nature 474, 76–78 (2011).
Austin, C. et al. Barium distributions in teeth reveal early-life dietary transitions in primates. Nature 498, 216–219 (2013).
Smith, T. M., Austin, C., Hinde, K., Vogel, E. R. & Arora, M. Cyclical nursing patterns in wild orangutans. Sci. Adv. 3, e1601517 (2017).
Herries, A. I. R. et al. in The Paleobiology of Australopithecus (Vertebrate Paleobiology and Paleoanthropology Series) (eds Reed, K. E. et al.) 21–40 (Springer, Dordrecht, 2013).
Peterson, A., Abella, E. F., Grine, F. E., Teaford, M. F. & Ungar, P. S. Microwear textures of Australopithecus africanus and Paranthropus robustus molars in relation to paleoenvironment and diet. J. Hum. Evol. 119, 42–63 (2018).
Sponheimer, M. & Lee-Thorp, J. A. Isotopic evidence for the diet of an early hominid, Australopithecus africanus. Science 283, 368–370 (1999).
Strait, D. S. et al. The feeding biomechanics and dietary ecology of Australopithecus africanus. Proc. Natl Acad. Sci. USA 106, 2124–2129 (2009).
Dupont, L. M., Donner, B., Vidal, L., Pérez, E. M. & Wefer, G. Linking desert evolution and coastal upwelling: Pliocene climate change in Namibia. Geology 33, 461–464 (2005).
Pickering, R. & Herries, A. I. R. in Hominin Postcranial Remains from Sterkfontein, South Africa (eds Ward, C. V. & Zipfel, B.) (Oxford Univ. Press, Oxford, in the press).
Clarke, R. in The Paleobiology of Australopithecus (Vertebrate Paleobiology and Paleoanthropology Series) (eds Reed, K. et al.) 105–123 (Springer, Dordrecht, 2013).
Ecker, M., Brink, J., Kolska-Horwitz, L., Scott, L. & Lee-Thorp, J. A. A. 12,000 years record of changes in herbivore niche separation and palaeoclimate (Wonderwerk Cave, South Africa). Quat. Sci. Rev. 180, 132–144 (2018).
Caley, T. et al. A two-million-year-long hydroclimatic context for hominin evolution in southeastern Africa. Nature 560, 76–79 (2018).
Shorrocks, B. The Biology of African Savannas (Oxford Univ. Press, New York, 2007).
Krachler, M., Rossipal, E. & Micetic-Turk, D. Concentrations of trace elements in sera of newborns, young infants, and adults. Biol. Trace Elem. Res. 68, 121–135 (1999).
Bouhallab, S. & Bouglé, D. Biopeptides of milk: caseinophosphopeptides and mineral bioavailability. Reprod. Nutr. Dev. 44, 493–498 (2004).
Smith, T. M. et al. Dental ontogeny in Pliocene and Early Pleistocene hominins. PLoS ONE 10, e0118118 (2015).
Lacruz, R. S., Dean, M. C., Ramirez-Rozzi, F. & Bromage, T. G. Megadontia, striae periodicity and patterns of enamel secretion in Plio-Pleistocene fossil hominins. J. Anat. 213, 148–158 (2008).
Pontzer, H., Raichlen, D. A., Shumaker, R. W., Ocobock, C. & Wich, S. A. Metabolic adaptation for low energy throughput in orangutans. Proc. Natl Acad. Sci. USA 107, 14048–14052 (2010).
van Noordwijk, M. A., Willems, E. P., Utami Atmoko, S. S., Kuzawa, C. W. & van Schaik, C. P. Multi-year lactation and its consequences in Bornean orangutans (Pongo pygmaeus). Behav. Ecol. Sociobiol. 67, 805–814 (2013).
Vogel, E. R. et al. Bornean orangutans on the brink of protein bankruptcy. Biol. Lett. 8, 333–336 (2012).
Harrison, M. E., Morrogh-Bernard, H. C. & Chivers, D. J. Orangutan energetics and the influence of fruit availability in the nonmasting peat-swamp forest of Sabangau, Indonesian Borneo. Int. J. Primatol. 31, 585–607 (2010).
Austin, C. et al. Uncovering system-specific stress signatures in primate teeth with multimodal imaging. Sci. Rep. 6, 18802 (2016).
Gitlin, M. Lithium side effects and toxicity: prevalence and management strategies. Int. J. Bipolar Disord. 4, 27 (2016).
Tandon, A., Bhalla, P., Nagpaul, J. P. & Dhawan, D. K. Effect of lithium on rat cerebrum under different dietary protein regimens. Drug Chem. Toxicol. 29, 333–344 (2006).
Wood, B. & Schroer, K. Reconstructing the diet of an extinct hominin taxon: the role of extant primate models. Int. J. Primatol. 33, 716–742 (2012).
Potts, R. Paleoenvironmental basis of cognitive evolution in great apes. Am. J. Primatol. 62, 209–228 (2004).
Guatelli-Steinberg, D. Macroscopic and microscopic analyses of linear enamel hypoplasia in Plio-Pleistocene South African hominins with respect to aspects of enamel development and morphology. Am. J. Phys. Anthropol. 120, 309–322 (2003).
Kennedy, G. E. From the ape’s dilemma to the weanling’s dilemma: early weaning and its evolutionary context. J. Hum. Evol. 48, 123–145 (2005).
Paton, C., Hellstrom, J., Paul, B., Woodhead, J. & Hergt, J. Iolite: Freeware for the visualisation and processing of mass spectrometric data. J. Anal. Atom. Spectrom. 26, 2508 (2011).
Woodhead, J. D., Swearer, S., Hergt, J. & Maas, R. In situ Sr-isotope analysis of carbonates by LA-MC-ICP-MS: interference corrections, high spatial resolution and an example from otolith studies. J. Anal. Atom. Spectrom. 20, 22 (2005).
Veizer, J. Strontium isotopes in seawater through time. Annu. Rev. Earth Planet. Sci. 17, 141–167 (1989).
Kuman, K. & Clark, R. J. Stratigraphy, artefact industries and hominid associations for Sterkfontein, Member 5. J. Hum. Evol. 38, 827–847 (2000).
Part of this study was funded by Monash University seed grant to L.F., J.W.A., A.R.E., A.I.R.H., S.W., S.B., O.K. and R.J.-B. A.I.R.H., J.W.A. and R.J.-B. received funding from the Australian Research Council Discovery Grant DP170100056. C.A. is supported by NICHD award R00HD087523. I.M. is supported by an Australian Research Council DECRA Fellowship (DE160100703), a Commonwealth Rutherford Fellowship from the Commonwealth Scholarship Commission and a Research Associate position from Homerton College. M.A. is supported by the US National Institutes of Environmental Health Sciences Grants U2CES026561 and DP2ES025453. We thank the South African Heritage Resources Agency (SAHRA), B. Zipfel from the Evolutionary Studies Institute of the University of Witwatersrand and M. Tawane from the Ditsong National Museum of Natural History for granting the export permit for the samples for analyses; C. Lawrence and K. Simon-Menasse from Perth Zoo, who provided access to modern orangutan dental material; and K. Schultz for comments on this manuscript.
The authors declare no competing interests.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended data figures and tables
a, Plan view of the Sterkfontein surface excavation (adapted from ref. 34) showing the association between the type site excavation and Member 4 deposits. b, Photograph of fossil teeth of specimen StS 28. c, Upper first molar (M1) StS 28B. d, Permanent lower first molar (M1) StS 28C, after being sectioned in two with a diamond low-speed high-precision rotary saw. e, Photograph of fossil teeth of specimen StS 51. f, Permanent premolar (P3) StS 51A. g, Permanent canine (LC) StS 51B, after being sectioned in two with a diamond low-speed high-precision rotary saw. The two teeth that are still embedded in the breccia were not sectioned.
a, Sketch of second molar tooth dentine and enamel section (with indication of biogenic accentuated lines in green) of a fossil Pongo sp. b, c, Elemental mapping of both dental tissues using LA-ICP-MS shows strontium distribution following the incremental growth pattern of the tooth (b), typical of biogenic signals, contrary to post-mortem diagenetic processes (c) (uranium diffusion during burial).
a–o, Elemental mapping of upper first molar cusp (StS 28B) (a–e); and lower first molar (StS 28C) (f–o), showing records of cyclical banding between zero and seven years at crown completion. The broad repeated banding pattern is attributed to seasonal dietary shifts, and potentially to cyclical nursing during long weaning periods. The identical elemental banding pattern that is found in both the StS 28B and StS 28C first permanent molars confirm the biogenic nature of the signal observed (compare b, c and d with g, h and i, respectively). The typical patchy and spreading diffusion pathways of uranium in the dentine and the enamel can be observed (e, j and o) with characteristic accumulation or depletion in cracks and at the enamel–dentine junction, which is very different to the biogenic lithium, strontium and barium banding.
a–e, Photograph (a) and elemental mapping of permanent premolar StS 51A Li/Ca banding (b), Sr/Ca banding (c), Ba/Ca banding (d) and U/Ca diffusion (e). f–j, Photograph (f) and elemental mapping of permanent canine (StS 51B) Li/Ca banding (g), Sr/Ca banding (h), Ba/Ca banding (i) and U/Ca diffusion (j). The strontium signal shows additional discrete lines (that are most likely to be associated with episodes of stress) compared to Li/Ca and Ba/Ca. Uranium distribution shows a typical and rather uniform diffusion pattern with enrichment close to the enamel–dentine junction and in fractures and cracks.
a–f, All teeth specimens are from the grassland-dominated ecosystem of South Africa (frequently referred as savannah) and were recovered from wild, modern animals. a, M2 molar of springbok (Antidorcas marsupialis; herbivore). b, P4 premolar of caracal (Caracal caracal; carnivore). c, Third molar (M3) of chacma baboon (Papio ursinus; omnivore). d, First premolar (P3) of red river hog (Potamochoerus porcus; omnivore). e, Second molar (M2) of bat-eared fox (Otocyon megalotis; insectivore/carnivore). f, P. ursinus first molar (M1). All mammals exhibit Ba/Ca and Sr/Ca banding (except for e, in which no strontium lines can be observed). Li/Ca banding is absent from animal teeth except from the two P. ursinus teeth (c, f) and—perhaps—the P. porcus tooth (d). The Ba/Ca banding pattern in Papio is very similar to that observed in A. africanus: apart from the lack of clear periodicity, the baboon teeth are comparable to those of A. africanus. Baboons have a unique nursing cycle and an opportunistic seasonal feeding habit.
Extended Data Fig. 6 138Ba/43Ca and 88Sr/43Ca distribution in the enamel parallel to the enamel–dentine junction.
a, StS 51 canine. The comparison of Ba/Ca and Sr/Ca ratios shows an inverse correlation towards the end of exclusive breastfeeding (marked by a circled A). This pattern is repeated at the points marked by circled B and C; these are approximately six months apart, which may indicate cyclical milk intake. The concurrent increase in Sr/Ca with decreasing Ba/Ca at the position marked by the circled A indicates an increase in the predominance of solid food in the diet, and a food source with more bioavailable strontium than is present in milk. The timing for the tooth development was approximated using estimated values for the species A. africanus17,18, and assuming linear growth rate of the enamel. b, Modern baboon (P. ursinus) molars. The Ba/Ca and Sr/Ca ratios along the enamel–dentine junction of a first (left) (see also Extended Data Fig. 5f) and a third molar (right) (see also Extended Data Fig. 5c) of a modern baboon was compared, giving several years of record. Although both teeth had clear banding, the M1 molars display more intense fluctuations, compared to the pattern observed in the third molars. This is potentially attributable to an additional nursing signal in M1, with exclusive breastfeeding for the first 4–6 months, until being completely weaned at just after a year.
The 7Li/43Ca, 88Sr/43Ca and 138Ba/43Ca ratios for each of three modern human specimens (Homo sapiens), labelled HT01 (upper first molar), HT02 (lower first molar) and HT03 (upper first molar) (left to right, respectively). The distribution pattern of all three elements is notably different to the signal observed in A. africanus, with enrichment towards the pulp cavity for both 88Sr/43Ca and 138Ba/43Ca that is probably associated with blood flow. An important difference is the absence of a repeated pattern that is observable for all three elemental ratios. Although some features could be interpreted as banding (such as the 88Sr/43Ca root signal of HT03), these isolated patterns are not mirrored in the distributions of the other elements.
Extended Data Fig. 8 Comparison of temporal occurrence of lithium and barium banding in the StS 28C upper first molar.
a–c, The Li/Ca banding (a) when placed over the Ba/Ca bands (b) shows a slight offset of the lithium banding (b). The lighter element (red dotted line marks the start of the lithium deposition) appears to occur immediately before, and during, the deposition of barium (blue shaded lines). We hypothesize that the location of lithium in the hydrosphere of the bone means that this element is more rapidly reabsorbed and transported into the bloodstream than is barium.
a, b, Location of the laser-ablation spot (150 μm) along the enamel and dentine for StS 51A (a) and StS 28C (b). Circles with red filling correspond to the first point (1) and yellow filling to the final point (point 9 for enamel, and point 6 for dentine). The table below shows the 87Sr/86Sr isotopic ratio and associated errors for each laser-ablation spot measured above. All values measured in both teeth (including point 6 in the dentine of StS 28, with associated error) correspond to values of the Malmani dolomite that surrounds Sterkfontein (the 87Sr/86Sr ratio of the Malmani dolomite ranges between 0.723 and 0.734)3, which shows that both specimens had limited mobility.
The orangutan Hsing Hsing was born in captivity in 1975 in the Singapore Zoo, and was raised by its parents (although additional human feeding cannot definitively be excluded). The orangutan joined the Perth Zoo as an immature individual in 1983. There appears to be no Ba/Ca banding pattern that would indicate cyclical milk consumption during crown completion. The diet of this orangutan would have been substantially different to that of orangutans living in the wild, with limited seasonal influence and no periods of food scarcity. It is expected that the orangutan and its parents would have had abundant and guaranteed access to food, which would probably have led it to being prematurely weaned (compared to wild Pongo). On this basis, it is unlikely that this orangutan would have had recurrent breastfeeding cycles, and therefore the absence of barium banding in this specimen is expected. The discrete banding lines observed in the Sr/Ca and the two Ba/Ca ratios are probably stress-related accentuated lines. No clear banding was observed in the enamel of this specimen.
About this article
Cite this article
Joannes-Boyau, R., Adams, J.W., Austin, C. et al. Elemental signatures of Australopithecus africanus teeth reveal seasonal dietary stress. Nature 572, 112–115 (2019). https://doi.org/10.1038/s41586-019-1370-5
Journal of Internal Medicine (2020)
Patterns of urinary cortisol levels during ontogeny appear population specific rather than species specific in wild chimpanzees and bonobos
Journal of Human Evolution (2020)
Nature Communications (2020)
Frontiers in Endocrinology (2020)
American Journal of Physical Anthropology (2020)