International Journal of Primatology

, Volume 26, Issue 4, pp 825–854 | Cite as

New Insights into Old Lemurs: The Trophic Adaptations of the Archaeolemuridae

  • Laurie R. Godfrey
  • Gina M. Semprebon
  • Gary T. Schwartz
  • David A. Burney
  • William L. Jungers
  • Erin K. Flanagan
  • Frank P. Cuozzo
  • Stephen J. King
Article

Abstract

Modern tools of paleoecological and ecomorphological research have enabled researchers to reconstruct the lifeways of extinct species more thoroughly than ever before. We apply a variety of tools in an attempt to reconstruct the diets of the extinct archaeolemurids of Madagascar. Our data include dental use wear (examined across species and across ontogenetic series of single species), enamel microstructure, enamel thickness, and δ13C. The data are complemented by field data on the environmental contexts in which the species lived and 14C determinations that demonstrate the surprisingly late survival of archaeolemurids. Several lines of evidence converge to suggest that all archaeolemurid species were hard-object processors, but with different diets and different methods of food processing. Past reconstructions of the diet of Hadropithecus as a specialized grass consumer fail under the scrutiny of multiple lines of evidence.

Keywords

paleoecology ecomorphology diet microwear dental microstructure 13Archaeolemur Hadropithecus Madagascar 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ambrose, S. H., and DeNiro, M. J. (1989). Climate and habitat reconstruction using stable carbon and nitrogen isotope ratios of collagen in prehistoric herbivore teeth from Kenya. Quaternary Res. 31: 407–422.CrossRefGoogle Scholar
  2. Anthony, M. R. L., and Kay, R. F. (1993). Tooth form and diet in Ateline and Alouattine primates: Reflections on the comparative method. Am. J. Sci. 293A: 356–382.Google Scholar
  3. Barnett, A. A., and Brandon-Jones, D. (1997). The ecology, biogeography and conservation of the uakaris, Cacajao (Pitheciinae). Folia Primatol. 68: 223–235.Google Scholar
  4. Boinski, S., Quatrone, R. P., and Swartz, H. (2000). Substrate and tool use by brown capuchins in Suriname: Ecological contexts and cognitive bases. Am. Anthropol. 102: 741–761.CrossRefGoogle Scholar
  5. Boyde, A., and Fortelius, M. (1986). Development, structure and function of rhinoceros enamel. Zool. J. Linnean Soc. 87: 181–214.Google Scholar
  6. Burdick, R. K., Borror, C. M., and Montgomery, D. C. (2003). A review of methods for measurement systems capability analysis. J. Quality Technology 35: 342–354.Google Scholar
  7. Burney, D. A. (1997). Theories and facts regarding Holocene environmental change before and after human colonization. In Goodman, S. M., and Patterson, B. D. (eds.), Natural Change and Human Impact in Madagascar, Smithsonian Press, Washington, pp. 75–89.Google Scholar
  8. Burney, D. A. (1999). Rates, patterns, and processes of landscape transformation and extinction in Madagascar. In MacPhee, R. D. E. (ed.), Extinctions in Near Time: Causes, Contexts, and Consequences, Plenum, New York, pp. 145–164.Google Scholar
  9. Burney, D. A., James, H. F., Grady, F. V., Rafamantanantsoa, J.-G., Ramilisonina, Wright, H. T., and Cowart, J. B. (1997). “Environmental change”, extinction, and human activity: evidence from caves in NW Madagascar. J. Biogeography 24: 755–767.CrossRefGoogle Scholar
  10. Burney, D. A., and Ramilisonina, (1998). The kilopilopitsofy, kidoky, and bokyboky: Accounts of strange animals from Belo-sur-Mer, Madagascar, and the megafaunal “extinction window.” Am. Anthropol. 100: 1–10.CrossRefGoogle Scholar
  11. Burney, D. A., Burney, L. P., Godfrey, L. R., Jungers, W. L., Goodman, S. M., Wright, H.T., and Jull, A. J. T. (2004). A chronology for late prehistoric Madagascar. J. Hum. Evol. 47: 25–63.PubMedGoogle Scholar
  12. Daegling, D. J. (1989). Biomechanics of cross-sectional size and shape in the hominoid mandibular corpus. Am. J. Phys. Anthropol. 80: 91–106.PubMedGoogle Scholar
  13. Daegling, D. J., and Grine, F. E. (1991). Compact bone distribution and biomechanics of early hominid mandibles. Am. J. Phys. Anthropol. 86: 321–339.PubMedGoogle Scholar
  14. Decary, R. (1926). Une mission scientifique dans le sud-est de Madagascar. Bull. Acad. Malgache 9 (N.S.): 79–86.Google Scholar
  15. Dirks, W., Reid, D. J., Jolly, C. J., Phillips-Conroy, J. E., and Brett, F. L. (2002). Out of the mouths of baboons: Stress, life history, and dental development in the Awash National Park hybird zone, Ethiopia. Am. J. Phys. Anthropol. 118: 239–252.CrossRefPubMedGoogle Scholar
  16. Dumont, E. R. (1995). Enamel thickness and dietary adaptation among extant primates and chiropterans. J. Mammal. 76: 1127–1136.Google Scholar
  17. Flanagan, E. K. (2004). The ontogeny of dental use wear in Archaeolemur spp. and Macaca fascicularis. Master’s Thesis, University of Massachusetts, Amherst.Google Scholar
  18. Fortelius, M. (1985). Ungulate cheek teeth: developmental, functional, and evolutionary interrelations. Acta Zoologica Fennica 180: 1–76.Google Scholar
  19. Garbutt, N. (1999). Mammals of Madagascar. New Haven: Yale University Press.Google Scholar
  20. Godfrey, L. R., and Jungers, W. L. (2002). Quaternary fossil lemurs. In Hartwig, W. C. (ed.), The Primate Fossil Record, Cambridge University Press, Cambridge, pp. 97–121.Google Scholar
  21. Godfrey, L. R., Jungers, W. L., Reed, K. E., Simons, E. L., and Chatrath, P. S. (1997a). Subfossil lemurs: Inferences about past and present primate communities in Madagascar. In Goodman, S. M., and Patterson, B. D. (eds.), Natural Change and Human Impact in Madagascar, pp. 218–256. Washington D.C.: Smithsonian Institution Press.Google Scholar
  22. Godfrey, L. R., Jungers, W. L, Wunderlich, R. E., and Richmond, B. G. (1997b). Reappraisal of the postcranium of Hadropithecus (Primates, Indroidea). Am. J. Phys. Anthropol. 103: 529–556.CrossRefGoogle Scholar
  23. Godfrey, L. R., Jungers, W. L., Simons, E. L., Chatrath, P. S., and Rakotosamimanana, B. (1999). Past and present distributions of lemurs in Madagascar. In Rakotosamimanana, B., Rasamimanana, H., Ganzhorn, J. U., and Goodman, S. M. (eds.), New Directions in Lemur Studies, Kluwer Academic/Plenum Publishers, New York, pp. 19–53.Google Scholar
  24. Godfrey, L. R., Petto, A. J., and Sutherland, M. R. (2002). Dental ontogeny and life-history strategies: The case of the giant extinct indroids of Madagascar. In Plavcan, J. M., Kay, R. F., Jungers, W. L., and van Schaik, C. P. (eds.), Reconstructing Behavior in the Primate Fossil Record, Kluwer Academic/Plenum Publishers, New York, pp. 113–157.Google Scholar
  25. Godfrey, L. R., Semprebon, G. M., Jungers, W. L., Sutherland, M. R., Simons, E. L., and Solounias, N. (2004). Dental use wear in extinct lemurs: evidence of diet and niche differentiation. J. Hum. Evol. 47: 145–169.CrossRefPubMedGoogle Scholar
  26. Gommery, D., Ziegle, P., Ramanivosoa, B., and Cauvin, J. (1998). Discovery of a new sub-fossil lemur site in Madagascar karsts. Comptes Rendus de l’Académie des Sciences, Ser. II Fasc. A. 326: 823–826.Google Scholar
  27. Grine, F. E. (1981). Trophic differences between “gracile” and “robust” australopithecines: A scanning electron analysis of occlusal events. S. Afr. J. Sci. 77: 203–230.Google Scholar
  28. Grine, F. E. (1986). Dental evidence for dietary differences in Australopithecus and Paranthropus: a quantitative analysis of permanent molar microwear. J. Hum. Evol. 15: 783–822.Google Scholar
  29. Grine, F. E., and Martin, L. B. (1988). Enamel thickness and development in Australopithecus and Paranthropus. In Grine, F. E. (ed.), Evolutionary History of the “Robust” Australopithecines, Aldine de Gruyter, New York, pp. 3–42.Google Scholar
  30. Grine, F. E., Ungar, P., and Teaford, M. F. (2002). Error rates in dental microwear quantification using scanning electron microscopy. Scanning 24: 144–153.PubMedGoogle Scholar
  31. Hylander, W. L. (1975). Incisor size and diet in anthropoids with special reference to the Cercopithecidae. Science 189: 1095–1098.PubMedGoogle Scholar
  32. Hylander, W. L. (1979). The functional significance of primate mandibular form. J. Morphol. 160: 223–240.CrossRefPubMedGoogle Scholar
  33. Iwano, T., and Iwakawa, C. (1988). Feeding behavior of the aye-aye (Daubentonia madagascariensis) on nuts of ramy (Canarium madagascariensis). Folia Primatol. 50: 136–142.Google Scholar
  34. Iwano, T., Randalana, R., and Rakotoarisoa, G. (1991). Ecology of the aye-aye (Daubentonia madagascariensis) I. Distribution. In Ehara, A., Kimura, T., Takenaka, O., and Iwamoto, M. (eds.), Primatology today: Proceedings of the XIIIth Congress of the International Primatological Society, Nagoya and Nyoto, 18–24 July (1990), pp. 41–42. Amsterdam: Elsevier Science Publishers.Google Scholar
  35. Jolly, C. J. (1970a). Hadropithecus: A lemuroid small-object feeder. Man (N.S.) 5: 619–626.Google Scholar
  36. Jolly, C. J. (1970b). The seed-eaters: a new model of hominid differentiation based on a baboon analogy. Man (N.S.) 5: 5–26.Google Scholar
  37. Jungers, W. L., Godfrey, L. R., Simons, E. L., Wunderlich, R. E., Richmond, B. G. andChatrath, P. S. (2002). Ecomorphology and behavior of giant extinct lemurs from Madagascar. In, Plavcan, J. M., Kay, R. F., Jungers, W. L., and van Schaik, C. P. (eds.), Reconstructing Behavior in the Primate Fossil Record, Kluwer Academic/Plenum Publishers, New York, pp. 371–411.Google Scholar
  38. Kay, R. F. (1977). The evolution of molar occlusion in the Cercopithecidae and early catarrhines. Am. J. Phys. Anthropol. 46: 327–352.CrossRefPubMedGoogle Scholar
  39. Kay, R. F. (1981). The nut-crackers: A new theory of the adaptations of the Ramapithecinae. Am. J. Phys. Anthropol. 55: 141–151.Google Scholar
  40. King, S. J., Godfrey, L. R., and Simons, E.L. (2001). Adaptive and phylogenetic significance of ontogenetic sequences in Archaeolemur, subfossil lemur from Madagascar. J. Hum. Evol. 41: 545–576.CrossRefPubMedGoogle Scholar
  41. Kinzey, W. G. (1992). Dental and dietary adaptations in the Pitheciinae. Am. J. Phys. Anthropol. 88: 499–514.PubMedGoogle Scholar
  42. Lamberton, C. (1938, for the year 1937). Contribution ‘a la connaissance de la faune subfossile de Madagascar. Note III. Les Hadropith‘eques. Bull. Acad. Malgache (nouv. s’erie) 20: 127–170 plus plates.Google Scholar
  43. Macho, G. A., Reid, D. J., Leakey, M. G., Jablonski, N., and Beynon, A. D. (1996). Climatic effects on dental development of Theropithecus oswaldi from Koobi Fora and Olorgesailie. J. Hum. Evol. 30: 57–70.CrossRefGoogle Scholar
  44. Martin, L. B. (1985). Significance of enamel thickness in hominoid evolution. Nature 314: 260–263.CrossRefPubMedGoogle Scholar
  45. Martin, L. B., Olejniczak, A. J., and Maas, M. C. (2003). Enamel thickness and microstructure in pitheciin primates, with comments on dietary adaptations of the middle Miocene hominoid Kenyapithecus. J. Hum. Evol. 45: 351–367.CrossRefPubMedGoogle Scholar
  46. Meldrum, D. J., and Kay, R. F. (1997). Nucicruptor rubicae, a new pitheciin seed predator from the Miocene of Colombia. Am. J. Phys. Anthropol. 102: 407–428.CrossRefPubMedGoogle Scholar
  47. Nowak, R. M. (1999). Walker’s Primates of the World. Baltimore: The Johns Hopkins University Press.Google Scholar
  48. Rafferty, K., and Teaford, M. F. (1992). Diet and dental microwear in Malagasy subfossil lemurs. Am. J. Phys. Anthropol. Suppl. 14: 134.Google Scholar
  49. Rafferty, K. L., Teaford, M. F., and Jungers, W. L. (2002). Molar microwear of subfossil lemurs: improving the resolution of dietary inferences. J. Hum. Evol. 43: 645–657.CrossRefPubMedGoogle Scholar
  50. Rak, Y. (1983). The Australopithecine Face. New York: Academic Press.Google Scholar
  51. Rasoloharijaona, S. (1999). Contribution á l’étude du genre Archaeolemur sp. (Archaeolemuridae): Un L’emurien subfossil provenant de la r’egion de l’Ankarana. Essai de reconstitution du paleoenvironnement de la r’egion de l?Ankarana. Lemur News 4:7–10.Google Scholar
  52. Ravosa, M. J. (1991). Structural allometry of the prosimain mandibular corpus and symphysis. J. Hum. Evol. 20: 3–20.Google Scholar
  53. Ravosa, M. J., and Simons, E. L (1994). Mandibular growth and function in Archaeolemur. Am. J. Phys. Anthropol. 95: 63–76.PubMedGoogle Scholar
  54. Reid, D. J., Schwartz, G. T., Chandrasekera, M. S., and Dean, M. C. (1998). A histological reconstruction of dental development in the common chimpanzee, Pan troglodytes. J. Hum. Evol. 35: 427–448.CrossRefPubMedGoogle Scholar
  55. Rensberger, J. M., and von Koenigswald, W. (1980). Functional and phylogenetic interpretation of enamel microstructure in rhinoceroses. Paleobiology 6: 447–495.Google Scholar
  56. Rosenberger, A. L. (1992). Evolution of feeding niches in New World monkeys. Am. J. Phys. Anthropol. 88: 535–562.Google Scholar
  57. Schoeninger, M. J., Iwaniec, U. T., and Nash, L. T., (1998). Ecological attributes recorded in stable isotope ratios of arboreal prosimian hair. Oecologia 113: 222–230.CrossRefGoogle Scholar
  58. Schwartz, G. T., and Dean, M. C. (2000). Interpreting the hominid dentition: Ontogenetic and phylogenetic aspects. In O’Higgins, P., and Cohen, M., (eds.), Development, Growth and Evolution: Implications for the Study of the Hominid Skeleton. Academic Press, London, pp. 207–233.Google Scholar
  59. Schwartz G. T., Liu W., and Zheng, L. (2003). Preliminary investigation of dental microstructure in the Yuanmou hominoid (Lufengpithecus hudienensis), Yunnan Province, China. J. Hum. Evol. 44: 189–202.CrossRefPubMedGoogle Scholar
  60. Schwartz, G. T., Reid, D. J., and Dean, M. C. (2001). Developmental aspects of sexual dimorphism in hominoid canines. Int. J. Primatol. 22: 837–860.CrossRefGoogle Scholar
  61. Schwartz, G. T., Samonds, K. E., Jungers, W. L., and Godfrey, L. R. (2000). Dental microstructure and life history in subfossil lemurs. J. Vert. Paleontol. 20 Suppl.: 68A.Google Scholar
  62. Schwartz, G. T., Samonds, K. E., Godfrey, L. R., Jungers, W. L., and Simons, E. L. (2002). Dental microstructure and life history in subfossil Malagasy lemurs. Proc. Nat. Acad. Sci. USA. 99: 6124–6129.CrossRefPubMedGoogle Scholar
  63. Semprebon, G. M., Godfrey, L. R., Solounias, N., Sutherland, M. R., and Jungers, W. L. (2004). Can low-magnification stereomicroscopy reveal diet? J. Hum. Evol. 47: 115–144.CrossRefPubMedGoogle Scholar
  64. Semprebon, G. M., Janis, C. M., and Solounias, N. 2004. The diets of the Dromomerycidae (Mammalia: Artiodactyla) and their response to Miocene vegetational change. J. Vert. Paleontol. 24: 430–437.Google Scholar
  65. Shellis, R. P., Beynon, A. D., Reid, D. J. and Hiiemae, K. M. (1998). Variation in molar enamel thickness among primates. J. Hum. Evol. 35: 507–522.CrossRefPubMedGoogle Scholar
  66. Simmen, B., and Sabatier, D. (1996). Diets of some French Guianan primates: Food composition and food choices. Int. J. Primatol. 17: 661–693.Google Scholar
  67. Simons, E. L., Burney, D. A., Chatrath, P. S., Godfrey, L. R., Jungers, W. L. and Rakotosamimanana, B. (1995). AMS 14C dates on extinct lemurs from caves in the Ankarana Massif of northern Madagascar. Quaternary Res. 43: 249–254.CrossRefGoogle Scholar
  68. Shoukri, M. (2003). Measures of Interobserver Agreement. Chapman & Hall, CRC Press, Boca Raton, FL.Google Scholar
  69. Smith, B. H. (2000). ‘Schultz’s Rule’ and the evolution of tooth emergence and replacement patterns in primates and ungulates. In Teaford, M. F., Smith, M. M., and Ferguson, M.W.J. (eds.), Development, Function, and Evolution of Teeth, Cambridge University Press, Cambridge, pp. 212–227.Google Scholar
  70. Smith, B. H., Crummett, T. L., and Brandt K. L. (1994). Ages of eruption of primate teeth: A compendium for aging individuals and comparing life histories. Yearbook Phys. Anthropol. 37: 177–231.CrossRefGoogle Scholar
  71. Smith, T.M., Martin, L.B., and Leakey, M.G. (2003). Enamel thickness, microstructure and development in Afropithecus turkanensis. J. Hum. Evol. 44: 283–306.CrossRefPubMedGoogle Scholar
  72. Solounias, N., and Semprebon, G.M. (2002). Advances in the reconstruction of ungulate ecomorphology with application to early fossil equids. American Museum Novitates No. 3366: 1–49.CrossRefGoogle Scholar
  73. Sterling, E. J. (1994). Aye-ayes: specialists on structurally defended resources. Folia Primatol. 62: 142–154.PubMedGoogle Scholar
  74. Strait, S. G. (1997). Tooth use and the physical properties of food. Evol. Anthropol. 5: 199–211.CrossRefGoogle Scholar
  75. Stuiver, M., Reimer, P. J., Bard, E., Beck, J. W., Burr, G. S., Hughen, K. A., Kromer, B., McCormac, F. G., van der Plicht, J., and Spurk, M. (1998). INTCAL98. Radiocarbon 40(3): 1041–1083.Google Scholar
  76. Tattersall, I. (1973). Cranial anatomy of the Archaeolemurinae (Lemuroidea, Primates). Anthrop. Pap. Am. Mus. Nat. Hist. 52: 1–110.Google Scholar
  77. Tattersall, I. (1975). Notes on the cranial anatomy of the subfossil Malagasy lemurs. In Tattersall, I., and Sussman, R. W. (eds.), Lemur Biology. Plenum Press, New York, pp. 111–124.Google Scholar
  78. Tattersall, I. (1982). The Primates of Madagascar. New York: Columbia University Press.Google Scholar
  79. Ungar, P. S. (2002). Reconstructing the diets of fossil primates. In Plavcan, J. M., Kay, R. F., Jungers, W. L., and van Schaik, C. P. (eds.), Reconstructing Behavior in the Primate Fossil Record, Kluwer Academic/Plenum Publishers, New York, pp. 261–296.Google Scholar
  80. Ward, S. C. and Molnar, S. (1980). Experimental stress analysis and topographic diversity in early hominid gnathic morphology. Am. J. Phys. Anthropol. 53: 383–395.PubMedGoogle Scholar
  81. Wheeler, D. J. and Lyday, R. W. (1989). Evaluating the Measurement Process, 2nd edition. SPC Press, Inc. Knoxville, Tennessee.Google Scholar

Copyright information

© Springer Science + Business Media, Inc. 2005

Authors and Affiliations

  • Laurie R. Godfrey
    • 1
  • Gina M. Semprebon
    • 2
  • Gary T. Schwartz
    • 3
  • David A. Burney
    • 4
    • 5
  • William L. Jungers
    • 6
  • Erin K. Flanagan
    • 1
  • Frank P. Cuozzo
    • 7
  • Stephen J. King
    • 7
  1. 1.Anthropology, Univ. Mass. Amherst
  2. 2.Bay Path CollegeLongmeadow
  3. 3.Anthropology and Institute of Human Origins, Arizona State UniversityTempe
  4. 4.Biological Sciences, Fordham University, New YorkNew York
  5. 5.National Tropical Botanical GardenKalaheo
  6. 6.Anatomical Sciences, Stony Brook UniversityStony Brook
  7. 7.Anthropology, University of North DakotaGrand Forks

Personalised recommendations