Dietary proclivities of Paranthropus robustus from Swartkrans, South Africa
DOI:
https://doi.org/10.1515/anre-2015-0001Keywords:
Australopithecus, underground storage organs, dental microwear, grit, PleistoceneAbstract
Pleistocene Paranthropus robustus fossils from Swartkrans have yielded stable isotope values suggesting some foraging on C4 plants possibly including underground storage organs. Dental microwear texture analysis on P. robustus (SK 6, SK 34 and SK 47) from Swartkrans Member 1 is performed to examine whether tooth surface damage from mastication agrees with prior dietary inferences from carbon isotopes. There is considerable variation in textural characteristics among the P. robustus specimens. Specifically, adult SK 34 stands apart from the two subadult specimens, SK 6 and SK 47, suggesting life history could be reflected in patterns of dental microwear texture characteristics, although seasonality and availability of fallback foods may also explain the variation observed in P. robustus. The fossils all exhibit elevated surface texture complexity, resembling the values for Lophocebus albigena and Cebus apella, and to a lesser extent, Pan troglodytes. Paranthropus robustus is dissimilar to primary folivores, such as Trachypithecus cristatus or folivore-frugivores such as Alouatta palliata suggesting leaves comprised very little of its diet. The textural fill volume of P. robustus differs from that observed in extant primates from tropical forests indicating extreme durophagy, perhaps a function of differences in habitat. Ingestion of extraneous grit on the underground parts of plants and from terrestrial resources, perhaps as fallback foods or as dietary staples, may account for these enamel textural properties and may help explain the mixed C3/C4 isotopic signal in P. robustus.
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References
Aiello LC, Montgomery C, Dean C. 1991. The natural history of deciduous tooth attrition in hominoids. J Hum Evol 21:397–412.
View in Google Scholar
Avery DM. 2001. The Plio-Pleistocene vegetation and climate of Sterkfontein and Swartkrans, South Africa, based on micromammals. J Hum Evol 41:113–32.
View in Google Scholar
Backwell LR, d’Errico F. 2001. Evidence of termite foraging by Swartkrans early hominids. Proc Natl Acad Sci USA 98:1358–63.
View in Google Scholar
Brain CK. 1981. The Hunter or the Hunted? An Introduction to African Cave Taphonomy. Chicago: University of Chicago Press.
View in Google Scholar
Brain CK. 1985. Cultural and taxonomic comparisons of hominids from Sterkfontein and Swartkrans. In: E Delson, editor. Ancestors: The Hard Evidence. New York: Alan R. Liss. 72–78.
View in Google Scholar
Brain CK. 2004. Structure and stratigraphy of the Swartkrans Cave in light of the new excavations. In: CK Brain, editor. Swartkrans: A Cave’s Chronicle of Early Man, 2nd Edition. Pretoria: Transvaal Museum Monograph, No. 8. 7–22.
View in Google Scholar
Brotoisworo E, Dirgayusa IWA. 1991. Ranging and feeding behavior of Presbytis cristata in the Pangandaran nature reserve, West Java, Indonesia. In: A Ehara, T Kimura, O Takenaka and M Iwamonto, editors. Primatology Today. Amsterdam: Elsevier Science. 115–18.
View in Google Scholar
Chamberlain J, Nelson G, Milton K. 1993. Fatty acid profiles of major food sources of howler monkeys (Alouatta palliata) in the neotropics. Experientia 49:820–24.
View in Google Scholar
Conklin-Brittain NL, Wrangham RW, Smith CC. 2002. A two-stage model of increased dietary quality in early hominid evolution: the role of fiber. In: PS Ungar and MF Teaford, editors. Human Diet: Its Origin and Evolution. London: Bergin and Garvey. 61–76.
View in Google Scholar
Conover WJ, Inman RL. 1981. Rank transformation as a bridge between parametric and nonparametric statistics. Am Statistician 35:124–29.
View in Google Scholar
Constantino PJ, Lee JJW, Chai H, Zipfel B, Ziscovici C, Lawon BR, Lucas PW. 2010. Tooth chipping can reveal the diet and bite forces of fossil hominins. Biol Lett 6:826–29.
View in Google Scholar
Curnoe D, Grun G, Taylor L, Thackeray JF. 2001. Direct ESR dating of a Pliocene hominin from Swartkrans. J Hum Evol 40:379–91.
View in Google Scholar
Daegling DJ, Grine FE. 1999. Terrestrial foraging and dental microwear in Papio ursinus. Primates 40:559–72.
View in Google Scholar
Delson E. 1984. Cercopithecid biochronology of the African Plio-Pleistocene: correlations among eastern and southern hominid-bearing localities. Cour Forsch-Inst Senckenberg 69:199–218.
View in Google Scholar
de Ruiter DJ. 2003. Revised faunal lists for Members 1–3 of Swartkrans, South Africa. Ann Transvaal Mus 40:29–41.
View in Google Scholar
de Ruiter DJ, Sponheimer M, Lee-Thorp JA. 2008. Indications of habitat association of Australopithecus robustus in the Bloubank Valley, South Africa. J Hum Evol 55:1015–20.
View in Google Scholar
Dirks JH, Taylor D. 2012. Fracture toughness of locust cuticle. J Experimental Biol 215:1502–08.
View in Google Scholar
Doran-Sheehy D, Mongo P, Lodwick J, Conklin-Brittain NL. 2009. Male and female western gorilla diet: preferred foods, use of fallback resources, and implications for ape versus Old World monkey foraging strategies. Am J Phys Anthropol 140:727–38.
View in Google Scholar
Dumont ER, Ryan TM, Godfrey LR. 2011. The Hadropithecus conundrum reconsidered, with implications for interpreting diet in fossil hominins. P Roy Soc B-Biol Sci 278:3654–61.
View in Google Scholar
Elton E. 2007. Environmental correlates of the cercopithecoid radiations. Folia Primatol 78:244–364.
View in Google Scholar
Elton E. 2008. The environmental context of human evolutionary history in Eurasia and Africa. J Anat 212:377–93.
View in Google Scholar
Estrada A. 1984. Resource use by howler monkeys (Alouatta palliata) in the rain forest of Los Tuxtlas, Veracruz, Mexico. Intl J Primatol 5:105–31.
View in Google Scholar
Galbany J, Estebaranz F, Martínez LM, Pérez-Pérez A. 2009. Buccal dental microwear variability in extant African Hominoidea: taxonomy versus ecology. Primates 50:221–30.
View in Google Scholar
Galbany J, Estebaranz F, Martínez LM, Romero A, De Juan J, Turbo D, Pérez-Pérez A. 2006. Comparative analysis of dental enamel polyvinylsiloxane impression and polyurethane casting methods for SEM research. Microscopy Res Tech 69:246–52.
View in Google Scholar
Galbany J, Martínez LM, Pérez-Pérez A. 2004. Tooth replication techniques, SEM imaging and microwear analysis in primates: methodological obstacles. Anthropologie 42:5–12.
View in Google Scholar
Galbany J, Romero A, Mayo-Alesón M, Itsoma F, Gamarra B, Pérez-Pérez A, Willaume E, Kappeler PM, Charpentier MJE. 2014. Age-related tooth wear differs between forest and savanna primates. PLoS ONE 9:e94938. doi:10.1371/journal.pone.0094938
View in Google Scholar
Grine FE. 1981. Trophic differences between gracile and robust Australopithecus: a scanning electron microscope analysis of occlusal events. S Afr J Sci 77:203–30.
View in Google Scholar
Grine FE. 1986. Dental evidence for dietary differences in Australopithecus and Paranthropus: a quantitative analysis of permanent molar microwear. J Hum Evol 15:783–822.
View in Google Scholar
Grine FE. 1989. New hominid fossils from the Swartkrans formation (1979–1986 excavations): cranio-dental specimens. Am J Phys Anthropol 79:409–49.
View in Google Scholar
Gordon KD. 1982. A study of microwear on chimpanzee molars: implications for dental microwear analysis. Am J Phys Anthropol 59:195–215.
View in Google Scholar
Hatley T, Kappelman J. 1980. Bears, pigs, and Plio-Pleistocene hominids: a case for the exploitation of belowground food resources. Hum Ecol 8:371–87.
View in Google Scholar
Head JS, Boesch C, Makaga L, Robbins MM. 2011. Sympatric chimpanzees (Pan troglodytes troglodytes) and gorillas (Gorilla gorilla gorilla) in Loango National Park, Gabon: dietary composition, seasonality, and intersite comparisons. Intl J Primatol 32:755–75.
View in Google Scholar
Herries AIR, Curnoe D, Adams JW. 2009. A multi-disciplinary seriation of early Homo and Paranthropus bearing palaeocaves in southern Africa. Quat Intl 202:14–28.
View in Google Scholar
Jack KM. 2011. The cebines: toward an explanation of variable social structure. In: CJ Campbell, A Fuentes, KC MacKinnon, SK Bearder and RM Stumpf, editors. Primates in Perspective, 2nd Edition. New York: Oxford University Press. 108–21.
View in Google Scholar
Jolly CJ. 1970. The seed-eaters: a new model of hominid evolution based on a baboon analogy. Man 5:5–26.
View in Google Scholar
Kay RF. 1985. Dental evidence for the diet of Australopithecus. Ann Rev Anthropol 14:315–41.
View in Google Scholar
Kay RF, Hiiemae KM. 1977. Jaw movement and tooth use in recent and fossil primates. Am J Phys Anthropol 40:227–56.
View in Google Scholar
Krueger KL, Scott JR, Kay RF, Ungar PS. 2008. Technical note: dental microwear textures of “Phase I” and “Phase II” facets. Am J Phys Anthropol 137:485–90.
View in Google Scholar
Lee-Thorp JA, Sponheimer M, Luyt J. 2007. Tracking changing environments using stable carbon isotopes in fossil tooth enamel: an example from the South African hominin sites. J Hum Evol 53:595–601.
View in Google Scholar
Lee-Thorp JA, van der Merwe NJ, Brain CK. 1994. Diet of Australopithecus robustus at Swartkrans from stable carbon isotopic analysis. J Hum Evol 27:361–72.
View in Google Scholar
Laden G, Wrangham R. 2005. The rise of the hominids as an adaptive shift in fallback foods: plant underground storage organs (USOs) and australopith origins. J Hum Evol 49:482–98.
View in Google Scholar
Lambert JE, Chapman CA, Wrangham RW, Conklin-Brittain NL. 2004. Hardness of cercopithecine foods: implications for the critical function of enamel thickness in exploiting fallback foods. Am J Phys Anthropol 125:363–68.
View in Google Scholar
Lucas PW, Omar R, Al-Fadhalah K, Almusallam AS, Henry AG, Michael S, et al. 2013. Mechanisms and causes of wear in tooth enamel: implications for hominin diets. JR Soc Interface 10:20120923 http://dx.doi.org/10.1098/rsif.2012.0923
View in Google Scholar
Merceron G, Scott JS, Scott RS, Geraads D, Spassov N, Ungar PS. 2009. Folivory or fruit/seed predation for Mesopithecus, an earliest colobine from the late Miocene of Eurasia? J Hum Evol 57:732–38.
View in Google Scholar
McGrew WC. 1992. Chimpanzee Material Culture: Implications for Human Evolution. Cambridge: Cambridge University Press.
View in Google Scholar
Nystrom P, Phillips-Conroy JE, Jolly CJ. 2004. Dental microwear in anubis and hybrid baboons (Papio hamadryas, sensu lato) living in Awash National Park, Ethiopia. Am J Phys Anthropol 125:279–91.
View in Google Scholar
Peters CR, Vogel JC. 2005. Africa’s wild C4 plant foods and possible early hominid diets. J Hum Evol 48:219–36.
View in Google Scholar
Pinilla Pérez B, Romero A, Pérez-Pérez A. 2011. Age-related variability in buccal dental-microwear in Middle and Upper Pleistocene human populations. Anthropol Rev 74:25–37.
View in Google Scholar
Reed K. 1997. Early hominid evolution and ecological change through the African Plio-Pleistocene. J Hum Evol 323:289–322.
View in Google Scholar
Reed KE, Rector AL. 2006. African Pliocene paleoecology: hominin habitats, resources, and diets. In: P Ungar, editor. Evolution of the Human Diet: The Known, the Unknown, and the Unknowable. New York: Oxford University Press. 262–88.
View in Google Scholar
Robinson JT. 1954. Prehominid dentition and hominid evolution. Evol 8:324–34.
View in Google Scholar
Rodrigues HG, Meceron G, Viriot L. 2009. Dental microwear patterns of extant and extinct Muridae (Rodentia, Mammalia): ecological implications. Naturwissenschaften 96:537–42.
View in Google Scholar
Romero A, Galbany J, De Juan J, Pérez-Pérez A. 2012. Short- and long-term in vivo human buccal-dental microwear turnover. Am J Phys Anthropol 148:467–72.
View in Google Scholar
Sanson GD, Kerr SA, Gross KA. 2007. Do silica phytoliths really wear mammalian teeth? J Archaeol Sci 34:526–31.
View in Google Scholar
Schmidt CW. 2010. On the relationship between dental microwear and dental macrowear. Am J Phys Anthropol 142:67–73.
View in Google Scholar
Schwartz GT, Thackeray JF, Reid C, van Reenan JF. 1998. Enamel thickness and the topography of the enamel-dentine junction in South African Plio-Pleistocene hominids with special reference to the Carabelli trait. J Hum Evol 35:523–42.
View in Google Scholar
Scott RS, Teaford MF, Ungar PS. 2012. Dental microwear texture and anthropoid diets. Am J Phys Anthropol 147:551–79.
View in Google Scholar
Scott RS, Ungar PS, Bergstrom TS, Brown CA, Childs BE, Teaford MF, Walker A. 2006. Dental microwear texture analysis: technical considerations. J Hum Evol 51:339–49.
View in Google Scholar
Scott RS, Ungar PS, Bergstrom TS, Brown CA, Grine FE, Teaford MF, et al. 2005. Dental microwear texture analysis shows within-species diet variability in fossil hominins. Nature 436:693–95.
View in Google Scholar
Sillen A. 1992. Strontium–calcium ratios (Sr/Ca) of Australopithecus robustus and associated fauna from Swartkrans. J Hum Evol 23:495–516.
View in Google Scholar
Sillen A, Hall G, Armstrong R. 1995. Strontium–calcium ratios (Sr/Ca) and strontium isotope ratios (87Sr/86Sr) of Australopithecus robustus and Homo sp. from Swartkrans. J Hum Evol 28:277–85.
View in Google Scholar
Sponheimer M, Lee-Thorp JA. 2003. Differential resource utilization by extant great apes and australopithecines: towards solving the C4 conundrum. Comp Biochem Phys 136:27–34.
View in Google Scholar
Sponheimer M, Loudon JE, Codron D, Howells ME, Pruetz JD, Codron J, de Ruiter DJ, Lee-Thorp JA. 2006a. Do ‘‘savanna’’ chimpanzees consume C4 resources? J Hum Evol 51:128–33.
View in Google Scholar
Sponheimer M, Passey BH, de Ruiter DJ, Guatelli-Steinberg D, Cerling TE, Lee-Thorp JA. 2006b. Isotopic evidence for dietary variability in the early hominin Paranthropus robustus. Science 314:980–82.
View in Google Scholar
Strait SG. 1993. Molar microwear in extant small-bodied faunivorous mammals – an analysis of feature density and pit frequency. Am J Phys Anthropol 92:63–79.
View in Google Scholar
Teaford MF, Ungar PS. 2000. Diet and the evolution of the earliest human ancestors. Proc Natl Acad Sci USA 97:13506–11.
View in Google Scholar
Tobias PV, Copley K, Brain CK. 1977. South Africa. In: KP Oakley, BG Campbell and TI Molleson, editors. Catalogue of Fossil Hominids. Part I: Africa, 2nd Edition. London: Trustees of the British Museum (Natural History). 95–151.
View in Google Scholar
Ungar PS, Grine FE. 1991. Incisor size and wear in Australopithecus africanus and Paranthropus robustus. J Hum Evol 20:313–40.
View in Google Scholar
Ungar PS, Krueger KL, Blumenschine RJ, Njau J, Scott RS. 2012. Dental microwear texture analysis of hominins recovered by the Olduvai Landscape Paleoanthropology Project, 1995–2007. J Hum Evol 63:429–37.
View in Google Scholar
Ungar PS, Scott RS. 2009. Dental evidence for diets of Early Homo. In: FE Grine, RE Leakey and JG Fleagle, editors. The First Humans: Origins of the Genus Homo. New York: Springer-Verlag. 121–34.
View in Google Scholar
Ungar PS, Scott RS, Grine FE, Teaford MF. 2010. Molar microwear textures and the diets of Australopithecus afarensis and Australopithecus anamensis. Phil Trans R Soc B-Biol Sci 365:3345–54.
View in Google Scholar
Ungar PS, Scott RS, Scott JR, Teaford MF. 2008. Dental microwear analysis: historical perspectives and new approaches. In: JD Irish and GC Nelson, editors. Technique and Application in Dental Anthropology. Cambridge: Cambridge University Press. 389–425.
View in Google Scholar
Vincent JFV, Wegst UGK. 2004. Design and mechanical properties of insect cuticle. Arthrop Struc Dev 33:187–99.
View in Google Scholar
Vrba ES. 1985. Ecological and adaptive changes associated with early hominid evolution. In: E Delson, editor. Ancestors: The Hard Evidence. New York: Alan R. Liss. 63–71.
View in Google Scholar
Vrba ES. 1995. The fossil record of African antelopes (Mammalia, Bovidae) in relation to human evolution and paleoclimate. In: ES Vrba, GH Denton, TC Partridge and LH Burkle, editors. Paleoclimate and Evolution, with Emphasis on Human Origins. New Haven: Yale University Press. 385–424.
View in Google Scholar
Wallace JA. 1973. Tooth chipping in the australopithecines. Nature 244:117–18.
View in Google Scholar
Wood B, Strait D. 2004. Patterns of resource use in early Homo and Paranthropus. J Hum Evol 46:119–62.
View in Google Scholar
Wrangham RW, Jones JH, Laden G, Pilbeam D, Conklin-Brittain N. 1999. The raw and the stolen: cooking and the ecology of human origins. Curr Anthropol 40:567–94.
View in Google Scholar
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