Buccal dental microwear variability in extant African Hominoidea: taxonomy versus ecology

Abstract

Buccal microwear patterns on teeth are good indicators of the abrasiveness of foodstuffs and have been used to trace the dietary habits of fossil species, including primates and hominids. However, few studies have addressed the variability of this microwear. The abrasiveness of dietary components depends not only on the hardness of the particles ingested, but also on the presence of dust and other exogenous elements introduced during food processing. These elements are responsible for the microwear typology observed on the enamel surfaces of primate teeth. Here we analyzed the variability of buccal microwear patterns in African Great Apes (Gorilla gorilla and Pan troglodytes), using tooth molds obtained from the original specimens held in several osteological collections. Our results suggest that ecological adaptations at subspecies or population level account for differences in microwear patterns, which are attributed to habitat and ecological conditions within populations rather than differences between species. The findings from studies on the variability of buccal dental microwear in extant species will contribute to a better understanding of extinct hominids’ diet and ecology.

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References

  1. Alberts SC, Hollister-Smith J, Mututua RS, Sayialel SN, Muruthi PM, Warutere JK, Altmann J (2005) Seasonality and long term change in a savannah environment. In: Brockman DK, Van Schaik CP (eds) Primate seasonality: implications for human evolution. Cambridge University Press, London, pp 157–196

    Google Scholar 

  2. Altmann SA, Altmann J (1970) Baboon ecology: African field research (Bibliotheca Primatologica, vol 12). University of Chicago Press/Karger, Chicago/Basel, pp 144–169

  3. Altmann J, Alberts SC, Altmann SA, Roy SB (2002) Dramatic change in local climate patterns in the Amboseli basin. African J Ecol 40:248–251

    Article  Google Scholar 

  4. Andritsakis DP, Vlamis KF (1986) A new generation of the elastomeric impression materials. Odontostomatol Proodos 40(3):133–142

    PubMed  CAS  Google Scholar 

  5. Basabose AK (2002) Diet composition of chimpanzees inhabiting the Montane forest of Kahuzi, Democratic Republic of Congo. Am J Primatol 58:1–21

    PubMed  Article  Google Scholar 

  6. Bermejo M (1997) Study of western lowland gorillas in the Lossi forest of North Congo and a pilot gorilla tourism plan. Gorilla Conserv News 11:6–7

    Google Scholar 

  7. Boesch C (2001) Hunting strategies of Gombe and Taï chimpanzees. In: Wrangham RW, McGrew WC, de Waal FBM, Heltne PG (eds) Chimpanzee cultures. Harvard University Press, Cambridge, pp 77–91

    Google Scholar 

  8. Bonnefille R, Vincens A, Buchet G (1987) Palynology, stratigraphy and palaeoenvironment of a Pliocene hominid site (2.9–3.3 m.y.) at Hadar, Ethiopia. Palaeogeogr Palaeoclimatol Palaeoecol 60:249–281

    Article  Google Scholar 

  9. Deblauwe I, Dupain J, Nguenang GM, Werdenich D, Van Elsaker L (2003) Insectivory by Gorilla gorilla gorilla in southest Cameroon. Int J Primatol 24(3):493–502

    Article  Google Scholar 

  10. Doran D, McNeilage A (1998) Gorilla ecology and behaviour. Evol Anthropol 6:120–131

    Article  Google Scholar 

  11. Doran D, Mc Neilage A, Greer D, Bocian C, Mehlman P, Shah N (2002) Western lowland gorilla diet, resource availability: new evidence, cross-site comparisons, reflections on indirect sampling methods. Am J Primatol 58:91–116

    PubMed  Article  Google Scholar 

  12. Estebaranz F, Galbany J, Martínez LM, Pérez-Pérez A (2007) 3-D Interferometric microscopy applied to the study of buccal enamel microwear. In: Bailey SE, Hublin JJ (eds) Dental perspectives on human evolution. Springer, Berlin, pp 389–401

  13. Estes RD (1997) The behaviour guide to African mammals. Russel Friedman, Halfway House

  14. Fleagle J (1999) Primate adaptation and evolution. Academic, London

  15. Galbany J (2006) El patró de microestriació dental de primats Catarrhini: un model ecològic per primats fòssils i homínids. Ph.D. dissertation, Universitat de Barcelona

  16. Galbany J, Pérez-Pérez A (2004) Buccal enamel microwear variability in Cercopithecoidea primates as a reflection of dietary habits in forested and open savannah environments. Anthropologie 42(1):13–19

    Google Scholar 

  17. Galbany J, Pérez-Pérez A (2006) Tamaño dental, desgaste oclusal y microestriación dentaria en primates Hominoidea. Rev Esp Antropol Biol 26:9–15

    Google Scholar 

  18. Galbany J, Martínez LM, Pérez-Pérez A (2002) Variabilidad del patrón de microestriación dentaria en primates Hominoideos: ¿una cuestión de especie o de entorno ecológico? Rev Esp Antropol Biol 23:77–83

    Google Scholar 

  19. Galbany J, Martínez LM, Pérez-Pérez A (2004a) Tooth replication tecniques, SEM imaging and microwear analysis in primates: methodological obstacles. Anthropologie 42(1):5–12

    Google Scholar 

  20. Galbany J, Martínez LM, Hiraldo O, Espurz V, Estebaranz F, Sousa M, Martínez López-Amor H, Medina AM, Farrés M, Bonnin A, Bernis C, Turbón D, Pérez-Pérez A (2004b) Teeth: Catálogo de los moldes de dientes de homínidos de la Universitat de Barcelona. Universitat de Barcelona, Barcelona

    Google Scholar 

  21. Galbany J, Moyà-Solà S, Pérez-Pérez A (2005a) Dental microwear variability on buccal tooth enamel surfaces of extant Catarrhini and the Miocene fossil Dryopithecus laietanus (Hominoidea). Folia Primatol 76(6):325–341

    PubMed  Article  CAS  Google Scholar 

  22. Galbany J, Martínez LM, López-Amor HM, Espurz V, Hiraldo O, Romero A, De Juan J, Pérez-Pérez A (2005b) Error rates in buccal-dental microwear quantification using scanning electron microscopy. Scanning 27:23–29

    PubMed  CAS  Google Scholar 

  23. Galbany J, Estebaranz F, Martínez LM, Romero A, De Juan J, Turbón D, Pérez-Pérez A (2006) Comparative analysis of dental enamel polyvinylsiloxane impression and polyurethane casting methods for SEM research. Microsc Res Tec 69(4):246–252

    Article  Google Scholar 

  24. Galbany J, Altmann J, Pérez-Pérez A, Alberts SC (2008) Abstract: buccal dental microwear in a living population of baboons from Amboseli (Kenya). Am J Phys Anthropol 135(S46):100

    Google Scholar 

  25. Grine FE (1986) Dental evidence for dietary differences in Australopithecus and Paranthropus. J Hum Evol 15:783–822

    Article  Google Scholar 

  26. Grine FE (1987) Quantitative analysis of occlusal microwear in Australopithecus and Paranthropus. Scan Microsc 1:647–656

    CAS  Google Scholar 

  27. Grine FE, Ungar PS, Teaford MF (2002) Error rates in dental microwear quantification using scanning electron microscopy. Scanning 24(3):144–153

    PubMed  CAS  Article  Google Scholar 

  28. Hernández-Aguilar A, Moore J, Pickering T (2007) Savanna chimpanzees use tools to harvest the underground storage organs of plants. Proc Natl Acad Sci USA 104:19210–19213

    Google Scholar 

  29. Hill DA, Lucas PW (1996) Toughness and fiber content of major leaf foods of Japanese macaques (Macaca fuscata yakui) in Yakushima. Am J Primatol 38:221–231

    Article  Google Scholar 

  30. Jones C, Sabater Pi J (1971) Comparative ecology of Gorilla gorilla (Savage and Wyman) and Pan troglodytes (Blumenbach) in Rio Muni, West Africa. Bibliogr Primatol 13:1–96

    Google Scholar 

  31. Kingdon J (2001) The Kingdon field guide to African mammals. Academic, London

  32. Kuroda S, Nishihara T, Suzuki S, Oko RA (1996) Sympatric chimpanzees and gorillas in the Ndoki forest, Congo. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 58–70

    Google Scholar 

  33. Lalueza C, Pérez-Pérez A (1993) The diet of the Neanderthal child Gibraltar 2 (Devil’s Tower) through the study of the buccal striation pattern. J Hum Evol 24:29–41

    Article  Google Scholar 

  34. Lalueza C, Pérez-Pérez A, Turbón D (1993) Microscopic study of the Banyoles mandible (Girona, Spain) diet, cultural activity and toothpick use. J Hum Evol 24:281–300

    Article  Google Scholar 

  35. Lalueza C, Pérez-Pérez A, Turbón D (1996) Dietary inferences through buccal microwear analysis of middle and upper Pleistocene human fossils. Am J Phys Anthropol 100:367–387

    PubMed  Article  CAS  Google Scholar 

  36. Mahoney P (2006) Dental microwear from Natufian hunter-gatherers and early Neolithic farmers: comparisons within and between samples. Am J Phys Anthropol 130:308–319

    PubMed  Article  Google Scholar 

  37. Martínez LM, Pérez-Pérez A (2004) Post-mortem wear as indicator of taphonomic processes affecting enamel surfaces of hominin teeth from Laetoli and Olduvai (Tanzania): implications to dietary interpretations. Anthropologie 42(1):37–42

    Google Scholar 

  38. Martínez LM, López-Amor HM, Pérez-Pérez A (2001) Microestriación dentaria y alteraciones del esmalte dentario en homínidos Plio-Pleistocénicos de Laetoli I Olduvai (Tanzania). Rev Esp Antrop Biol 22:61–72

    Google Scholar 

  39. McGrew WC, Baldwin PJ, Tutin CEG (1988) Diet of wild chimpanzees (Pan troglodytes verus) at Mt. Assirik, Senegal: I. Composition. Am J Phys Anthropol 16:213–226

    Google Scholar 

  40. Merceron G, Taylor S, Scott R, Chaimanee Y, Jaeger JJ (2006) Dietary characterization of the hominoid Khoratpithecus (miocene of Thailand): evidence from dental topographic and microwear texture analyses. Naturwissenschaften 93:329–333

    PubMed  Article  CAS  Google Scholar 

  41. Newton-Fisher NE (1999) The diet of chimpanzees in the Budongo forest reserve, Uganda. Afr J Ecol 37:344–354

    Article  Google Scholar 

  42. Nishida T, Ohigashi H, Koshimizu K (2000) Tastes of chimpanzee plant foods. Current Anthropol 41(3):431–438

    Article  Google Scholar 

  43. Nishihara T (1995) Feeding ecology of western lowland gorillas in the Nouabalé-Ndoki National Park, northern Congo. Primates 35:151–168

    Article  Google Scholar 

  44. Organ JM, Teaford MF, Larsen CS (2005) Dietary inferences from dental occlusal microwear at Mission San Luis de Apalachee. Am J Phys Anthropol 128:801–811

    PubMed  Article  Google Scholar 

  45. Pérez-Pérez A, Lalueza C, Turbón D (1994) Intraindividual and intragroup variability of buccal tooth striation pattern. Am J Phys Anthropol 94:175–187

    PubMed  Article  Google Scholar 

  46. Pérez-Pérez A, Bermúdez de Castro JM, Arsuaga JL (1999) Non-occlusal dental microwear analysis of 300.000 year-old Homo heilderbergensis teeth from Sima de los Huesos (Sierra de Atapuerca, Spain): implications of intrapopulation variability for dietary analysis of hominid fossil remains. Am J Phys Anthropol 108(4):433–457

    PubMed  Article  Google Scholar 

  47. Pérez-Pérez A, Espurz V, Bermúdez de Castro JM, de Lumley MA, Turbón D (2003a) Non-occlusal dental microwear variability in a sample of middle and upper Pleistocene human populations from Europe and the near east. J Hum Evol 44:497–513

    PubMed  Article  Google Scholar 

  48. Pérez-Pérez A, Farrés M, Martínez LM, Martínez López-Amor H, Galbany J (2003b) Correlación entre tamaño dentario y microestriación vestibular en homínidos Pli-Pleistocénicos de Kenia y Tanzania. In: Aluja MP, Malgosa A, Nogués R (eds) Antropología y biodiversidad. Edicions Bellaterra, Barcelona, pp 407–413

  49. Puech PF (1982) L’usure dentaire de l’homme de Tautavel. In: L’Homo erectus et la place de l’homme de Tautavel parmi les hominides fossiles. In: CNRS (ed) Nice Colloque Internacional du CNRS. CNRS, Paris, pp 249–275

  50. Puech PF (1984) Acidic food choice in Homo habilis at Olduvai. Curr Anthropol 25:349–350

    Article  Google Scholar 

  51. Puech PF (1986a) Australopithecus afarensis Garusi 1, diversite et specialization des primers hominides d’apres les caracteres maxillo-dentaires. C R Acad Sci Paris Ser II 303:1819–1824

  52. Puech PF (1986b) Tooth microwear in Homo habilis at Olduvai. Mem Mus Hist Natur Paris Ser C 53:399–414

  53. Remis MJ (1997) Western lowland Gorillas (Gorilla gorilla gorilla) as seasonal frugivores: use of variable resources. Am J Phys Anthropol 43:87–109

    CAS  Google Scholar 

  54. Remis MJ (2003) Are gorillas vacuum cleaners of the forest floor? The roles of gorilla body size, habitat and food preferences on dietary flexibility and nutrition. In: Taylor AB, Goldsmith ML (eds) Gorilla biology: a multidisciplinary perspective. Cambridge University Press, Cambridge, pp 385–404

    Google Scholar 

  55. Remis MJ, Dierenfeld ES, Carroll RW (2001) Nutritional aspects of western lowland gorilla (Gorilla gorilla gorilla). Diet during seasons of scarcity at Bai Hokou, Central Africa Republic. Int J Primatol 22(5):807–836

    Article  Google Scholar 

  56. Rogers ME, Maisels F, Williamson EA, Fernández M, Tutin CEG (1990) Gorilla diet in Lope Reserve, Gabon: a nutritional analysis. Oecologia 84:326–339

    Google Scholar 

  57. Rogers ME, Tutin CEG, Williamson EA, Parnell RJ, Voysey BC, Fernández M (1994) Seasonal feeding on bark by gorillas: an unexpected keystone food? In: Thierry B, Anderson JR, Roeder JJ, Herrenschmidt N (eds) Ecology and evolution. Universite Louis Pasteur, Strasbourg, pp 37–43

    Google Scholar 

  58. Rogers ME, Abernethy K, Bermejo M, Cipolletta C, Doran D, McFarland K, Nishihara T, Remis M, Tutin CEG (2004) Western Gorilla diet: a synthesis from six sites. Am J Phys Anthropol 64:173–192

    Google Scholar 

  59. Romero A, Juan De (2006) Análisis de microdesgaste dentario vestibular bajo dieta ad libitum. Rev Esp Antrop Fís 26:103–108

    Google Scholar 

  60. Romero A, Martínez-Ruiz N, Amorós A, De Juan J (2003/2004) Microdesgaste dental in vivo: modelo preliminar para interpretar su formación y variabilidad en grupos humanos antiguos. Rev Esp Antrop Fís 24:5–18

    Google Scholar 

  61. Rose JJ (1983) A replication technique for scanning electron microscopy: applications for anthropologists. Am J Phys Anthropol 62:255–261

    Article  Google Scholar 

  62. Sabater-Pi J (1960) Beitrag zür biologie del flachlandgorillas (Gorilla gorilla gorilla). Z Säugetierkd 25:133–141

    Google Scholar 

  63. Sabater-Pi J (1977) Contribution to the study of alimentation of lowland gorillas in natural state in Rio Muni, Rep. Equat. Guinea (West Africa). Primates 18(1):183–204

    Article  Google Scholar 

  64. Sabater-Pi J (1979) Feeding behaviour and diet of chimpanzees (Pan troglodytes troglodytes) in the Okorobikó mountains of Rio Muni, West Africa. Z Tierpsychol 50:265–281

    PubMed  CAS  Google Scholar 

  65. Scott RS, Ungar PS, Bergstrom TS, Brown CA, Grine FE, Teaford MF, Walker A (2005) Dental microwear texture analysis reflects diets of living primates and fossil hominins. Nature 436:693–695

    PubMed  Article  CAS  Google Scholar 

  66. Stanford CB, Nkurunungi JB (2003) Behavioral ecology of sympatric chimpanzees and gorillas in Bwindi impenetrable National Park, Uganda: diet. Int J Primatol 24(4):901–918

    Article  Google Scholar 

  67. Stanford CB, Wallis J, Matama H, Goodall J (1994) Patterns of predation by chimpanzees on red colobus monkeys in Gombe National Park, 1982–1991. Am J Phys Anthropol 94:213–228

    PubMed  Article  CAS  Google Scholar 

  68. Sugiyama Y, Koman J (1992) The flora of Bossou: its utilization by chimpanzees and humans. Afr Study Monogr 13:127–169

    Google Scholar 

  69. Teaford MF, Oyen OJ (1989) In vivo and in vitro turnover in dental microwear. Am J Phys Anthropol 80:447–460

    PubMed  Article  CAS  Google Scholar 

  70. Tutin CEG (1999) Fragmented living: behavioural ecology of primates in a forest fragment in the Lopé Reserve, Gabon. Primates 40(1):249–265

    Article  Google Scholar 

  71. Tutin CEG, Fernandez M (1983) Gorillas feeding on termites in Gabon, West Africa. J Mammal 64:511–513

    Article  Google Scholar 

  72. Tutin CEG, Fernandez M (1992) Insect-eating by sympatric lowland gorillas (Gorilla g. gorilla) and chimpanzees (Pan t. troglodytes) in the Lopé Reserve, Gabon. Am J Primatol 28:29–40

    Article  Google Scholar 

  73. Tutin CEG, Fernández M (1993) Composition of the diet of chimpanzees and comparisons with that of sympatric lowland gorillas in the Lopé Reserve, Gabon. Am J Primatol 30:195–211

    Article  Google Scholar 

  74. Tutin CEG, Fernández M (1994) Comparison of food processing by sympatric apes in the Lopé Reserve, Gabon. In: Thierry B, Anderson JR, Roeder JJ, Herrenschmidt N (eds) Ecology and evolution. Universite Louis Pasteur, Strasbourg, pp 29–35

    Google Scholar 

  75. Tutin CEG, Ham RM, White LJT, Harrison MJS (1997) The primate community of the Lopé Reserve, Gabon: diets, responses to fruit scarcity, and effects of biomass. Am J Primatol 34:1–24

    Article  Google Scholar 

  76. Tweheyo M, Lye KA (2003) Phenology of figs in Budongo forest Unganda and its importance for the chimpanzee diet. Afr J Ecol 41:306–316

    Article  Google Scholar 

  77. Tweheyo M, Obua J (2001) Feeding habits of chipanzees (Pan troglodytes), red-tail monkeys (Cercopithecus ascanius schmidti) and blue monkeys (Cercopithecus mitis stuhlmanii) on figs in Budongo forest reserve, Uganda. Afr J Ecol 39:133–139

    Article  Google Scholar 

  78. Ungar PS, Teaford MF (1996) Preliminary examination of non-occlusal dental microwear in Anthropoids: implications for the study of fossils. Am J Phys Anthropol 100:101–113

    PubMed  Article  CAS  Google Scholar 

  79. Ungar PS, Teaford MF, Glander KE, Pastor RF (1995) Dust accumulation in the canopy: a potential cause of dental microwear in primates. Am J Phys Anthropol 97:93–99

    PubMed  Article  CAS  Google Scholar 

  80. Ungar PS, Grine FE, Teaford MF (2008) Dental microwear and diet of the Plio-Pleistocene Hominin Paranthropus boisei. PLoS ONE 3(4):e2044. doi:10.1371/journal.pone.0002044

    PubMed  Article  CAS  Google Scholar 

  81. White LJT (2001) Forest-savanna dynamics and the origins of Marantaceae forest in central Gabon. In: Weber W, White LJT, Vedder A, Naughton-Treves L (eds) African rain forest ecology, conservation. Yale University Press, New Haven, pp 165–182

    Google Scholar 

  82. Whiten A (2007) Pan African culture: memes and genes in wild chimpanzees. Proc Natl Acad Sci USA 104:17559–17560

    Google Scholar 

  83. Wrahgham RW (1977) Feeding behaviour of chimpanzees in Gombe national park, Tanzania. In: Cluttin-Brock TH (ed) Primate ecology. Academic, London

  84. Wrahgham RW, Chapman CA, Clark-Arcadi AP, Isabirye-Basuta G (1996) Social ecology of Kanyawara chimpanzees: implications for understanding the costs of great apes groups. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge

    Google Scholar 

  85. Wrangham RW (1984) Chimpanzees. In: MacDonald DW (ed) The encyclopedia of mammals. Facts on File, Inc., New York, pp 422–427

  86. Wrangham RW, Riss VZB (1990) Rates of predation on mammals by Gombe chimpanzees, 1972–1975. Primates 31:157–170

    Article  Google Scholar 

  87. Wrangham RW, Conklin NL, Chapman CA, Hunt KD (1991) The significance of fibrous foods for Kibale forest chimpanzees. Phil Trans R Soc Lond Ser B 334:171–178

    Article  CAS  Google Scholar 

  88. Yamakoshi G (1998) Dietary responses to fruit scarcity on wild chimpanzees at Bossou, Guinea: possible implications for ecological importance of tool use. Am J Phys Anthropol 106:283–295

    PubMed  Article  CAS  Google Scholar 

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Acknowledgments

This research was funded by the Spanish CGL2004-00775/BTE and CGL-200760802 projects and was supported by the “Departament d’Educació i Universitats de la Generalitat de Catalunya––Beatriu de Pinós 2006.” We thank the institutions that granted permission to study the extant primate specimens and Dr. Peter S. Ungar (University of Arkansas) for lending us his Hominoidea molds taken in the Royal Museum for Central Africa (MRAC) in Tervuren (Belgium). We also thank Núria Garriga (Universitat de Barcelona) and Dr. Alejandro Romero (Universidad de Alicante) for their help in plot generation. Furthermore, thanks go to the two anonymous referees for their reviews and useful comments. All SEM images were obtained at the “Serveis Cientificotècnics” of the Universitat de Barcelona.

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Correspondence to Jordi Galbany.

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Galbany, J., Estebaranz, F., Martínez, L.M. et al. Buccal dental microwear variability in extant African Hominoidea: taxonomy versus ecology. Primates 50, 221–230 (2009). https://doi.org/10.1007/s10329-009-0139-0

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Keywords

  • Dental microwear
  • SEM
  • Pan troglodytes
  • Gorilla gorilla