, Volume 50, Issue 3, pp 221–230 | Cite as

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

  • Jordi GalbanyEmail author
  • Ferran Estebaranz
  • Laura M. Martínez
  • Alejandro Pérez-Pérez
Original Article


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.


Dental microwear SEM Pan troglodytes Gorilla gorilla 



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.


  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 157–196Google Scholar
  2. Altmann SA, Altmann J (1970) Baboon ecology: African field research (Bibliotheca Primatologica, vol 12). University of Chicago Press/Karger, Chicago/Basel, pp 144–169Google Scholar
  3. Altmann J, Alberts SC, Altmann SA, Roy SB (2002) Dramatic change in local climate patterns in the Amboseli basin. African J Ecol 40:248–251CrossRefGoogle Scholar
  4. Andritsakis DP, Vlamis KF (1986) A new generation of the elastomeric impression materials. Odontostomatol Proodos 40(3):133–142PubMedGoogle Scholar
  5. Basabose AK (2002) Diet composition of chimpanzees inhabiting the Montane forest of Kahuzi, Democratic Republic of Congo. Am J Primatol 58:1–21PubMedCrossRefGoogle 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 11:6–7Google 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 77–91Google 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 60:249–281CrossRefGoogle 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):493–502CrossRefGoogle Scholar
  10. Doran D, McNeilage A (1998) Gorilla ecology and behaviour. Evol Anthropol 6:120–131CrossRefGoogle 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 58:91–116PubMedCrossRefGoogle 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 389–401Google Scholar
  13. Estes RD (1997) The behaviour guide to African mammals. Russel Friedman, Halfway HouseGoogle Scholar
  14. Fleagle J (1999) Primate adaptation and evolution. Academic, LondonGoogle Scholar
  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 BarcelonaGoogle Scholar
  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):13–19Google Scholar
  17. Galbany J, Pérez-Pérez A (2006) Tamaño dental, desgaste oclusal y microestriación dentaria en primates Hominoidea. Rev Esp Antropol Biol 26:9–15Google 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 23:77–83Google 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):5–12Google 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, BarcelonaGoogle 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):325–341PubMedCrossRefGoogle 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 27:23–29PubMedGoogle 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):246–252CrossRefGoogle 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):100Google Scholar
  25. Grine FE (1986) Dental evidence for dietary differences in Australopithecus and Paranthropus. J Hum Evol 15:783–822CrossRefGoogle Scholar
  26. Grine FE (1987) Quantitative analysis of occlusal microwear in Australopithecus and Paranthropus. Scan Microsc 1:647–656Google Scholar
  27. Grine FE, Ungar PS, Teaford MF (2002) Error rates in dental microwear quantification using scanning electron microscopy. Scanning 24(3):144–153PubMedCrossRefGoogle 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 104:19210–19213Google 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 38:221–231CrossRefGoogle 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 13:1–96Google Scholar
  31. Kingdon J (2001) The Kingdon field guide to African mammals. Academic, LondonGoogle Scholar
  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 58–70Google 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 24:29–41CrossRefGoogle 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 24:281–300CrossRefGoogle 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 100:367–387PubMedCrossRefGoogle Scholar
  36. Mahoney P (2006) Dental microwear from Natufian hunter-gatherers and early Neolithic farmers: comparisons within and between samples. Am J Phys Anthropol 130:308–319PubMedCrossRefGoogle 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):37–42Google 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 22:61–72Google 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 16:213–226Google 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 93:329–333PubMedCrossRefGoogle Scholar
  41. Newton-Fisher NE (1999) The diet of chimpanzees in the Budongo forest reserve, Uganda. Afr J Ecol 37:344–354CrossRefGoogle Scholar
  42. Nishida T, Ohigashi H, Koshimizu K (2000) Tastes of chimpanzee plant foods. Current Anthropol 41(3):431–438CrossRefGoogle Scholar
  43. Nishihara T (1995) Feeding ecology of western lowland gorillas in the Nouabalé-Ndoki National Park, northern Congo. Primates 35:151–168CrossRefGoogle 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 128:801–811PubMedCrossRefGoogle Scholar
  45. Pérez-Pérez A, Lalueza C, Turbón D (1994) Intraindividual and intragroup variability of buccal tooth striation pattern. Am J Phys Anthropol 94:175–187PubMedCrossRefGoogle 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):433–457PubMedCrossRefGoogle 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 44:497–513PubMedCrossRefGoogle 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 407–413Google Scholar
  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 249–275Google Scholar
  50. Puech PF (1984) Acidic food choice in Homo habilis at Olduvai. Curr Anthropol 25:349–350CrossRefGoogle 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 303:1819–1824Google Scholar
  52. Puech PF (1986b) Tooth microwear in Homo habilis at Olduvai. Mem Mus Hist Natur Paris Ser C 53:399–414Google Scholar
  53. Remis MJ (1997) Western lowland Gorillas (Gorilla gorilla gorilla) as seasonal frugivores: use of variable resources. Am J Phys Anthropol 43:87–109Google 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 385–404Google 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):807–836CrossRefGoogle Scholar
  56. Rogers ME, Maisels F, Williamson EA, Fernández M, Tutin CEG (1990) Gorilla diet in Lope Reserve, Gabon: a nutritional analysis. Oecologia 84:326–339Google 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 37–43Google 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 64:173–192Google Scholar
  59. Romero A, Juan De (2006) Análisis de microdesgaste dentario vestibular bajo dieta ad libitum. Rev Esp Antrop Fís 26:103–108Google 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 24:5–18Google Scholar
  61. Rose JJ (1983) A replication technique for scanning electron microscopy: applications for anthropologists. Am J Phys Anthropol 62:255–261CrossRefGoogle Scholar
  62. Sabater-Pi J (1960) Beitrag zür biologie del flachlandgorillas (Gorilla gorilla gorilla). Z Säugetierkd 25:133–141Google 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):183–204CrossRefGoogle 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 50:265–281PubMedGoogle 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 436:693–695PubMedCrossRefGoogle 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):901–918CrossRefGoogle 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 94:213–228PubMedCrossRefGoogle Scholar
  68. Sugiyama Y, Koman J (1992) The flora of Bossou: its utilization by chimpanzees and humans. Afr Study Monogr 13:127–169Google Scholar
  69. Teaford MF, Oyen OJ (1989) In vivo and in vitro turnover in dental microwear. Am J Phys Anthropol 80:447–460PubMedCrossRefGoogle Scholar
  70. Tutin CEG (1999) Fragmented living: behavioural ecology of primates in a forest fragment in the Lopé Reserve, Gabon. Primates 40(1):249–265CrossRefGoogle Scholar
  71. Tutin CEG, Fernandez M (1983) Gorillas feeding on termites in Gabon, West Africa. J Mammal 64:511–513CrossRefGoogle 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 28:29–40CrossRefGoogle 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 30:195–211CrossRefGoogle 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 29–35Google 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 34:1–24CrossRefGoogle Scholar
  76. Tweheyo M, Lye KA (2003) Phenology of figs in Budongo forest Unganda and its importance for the chimpanzee diet. Afr J Ecol 41:306–316CrossRefGoogle 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 39:133–139CrossRefGoogle 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 100:101–113PubMedCrossRefGoogle 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 97:93–99PubMedCrossRefGoogle 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 PubMedCrossRefGoogle 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 165–182Google Scholar
  82. Whiten A (2007) Pan African culture: memes and genes in wild chimpanzees. Proc Natl Acad Sci USA 104:17559–17560Google Scholar
  83. Wrahgham RW (1977) Feeding behaviour of chimpanzees in Gombe national park, Tanzania. In: Cluttin-Brock TH (ed) Primate ecology. Academic, LondonGoogle Scholar
  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, CambridgeGoogle Scholar
  85. Wrangham RW (1984) Chimpanzees. In: MacDonald DW (ed) The encyclopedia of mammals. Facts on File, Inc., New York, pp 422–427Google Scholar
  86. Wrangham RW, Riss VZB (1990) Rates of predation on mammals by Gombe chimpanzees, 1972–1975. Primates 31:157–170CrossRefGoogle 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 334:171–178CrossRefGoogle 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 106:283–295PubMedCrossRefGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer 2009

Authors and Affiliations

  • Jordi Galbany
    • 1
    • 2
    Email author
  • Ferran Estebaranz
    • 2
  • Laura M. Martínez
    • 2
  • Alejandro Pérez-Pérez
    • 2
  1. 1.Department of BiologyDuke UniversityDurhamUSA
  2. 2.Secc. Antropologia, Dept. Biologia Animal, Facultat de BiologiaUniversitat de BarcelonaBarcelonaSpain

Personalised recommendations