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Palaeobiodiversity and Palaeoenvironments

, Volume 92, Issue 4, pp 573–583 | Cite as

Understanding Eocene primate palaeobiology using a comprehensive analysis of living primate ecology, biology and behaviour

  • Michelle L. SautherEmail author
  • Frank P. Cuozzo
Original Paper

Abstract

The comparative method is central to interpretations of Eocene primate palaeobiology. This method rests upon a thorough study of analogous living forms. With a rapidly increasing knowledge of such forms, most notably the Malagasy lemurs, our ability to advance the study of Eocene primate ecology, biology and behaviour far exceeds that of even just a few years ago. Here we present such a comparison. Based on our data collected from both living lemurs and extant lemur skeletal specimens, we are able to make a number of comparisons that provide insight into middle Eocene primate ecology and palaeobiology. At the Beza Mahafaly Special Reserve, Madagascar, omnivorous living ring-tailed lemurs that feed on large, hard and tough fruits display a pattern of frequent post-canine tooth wear laterality (62 %) when compared to sympatric, folivorous Verreaux’s sifaka (4 %). Our results indicate that Notharctus does not display a high frequency of tooth wear laterality (7 %), indicating folivory without processing large, hard fruits with its postcanines. Our data on Notharctus tooth wear also indicate, similar to living ring-tailed lemurs at Beza Mahafaly, that numerous individuals (21 %) survived long enough to experience heavy tooth wear, contrary to the assumption that heavy tooth wear leads to the rapid death of the individual. Finally, our data on trauma and injury from a living lemur population suggest that the reported wrist injury in Darwinius masillae (i.e. “Ida”) did not necessarily lead to her death, as numerous ring-tailed lemurs at Beza Mahafaly survive with similar or even more traumatic injuries and maintain the ability to climb. Thus, our data from living primates provide a broad comparative framework for interpreting the ecology, biology and behaviour of Eocene forms.

Keywords

Lemur Dental ecology Notharctus Darwinius Laterality 

Notes

Acknowledgements

We thank the organisers of the 22nd Annual Senckenberg Conference, most specifically Dr. Thomas Lehmann and Dr. Virgine Volpato, for organising a wonderful conference, and for their help with our abstract submission and registration. We are also grateful to Dr. Wighart von Koenigswald for his assistance with coordinating our attending the meeting in Frankfurt. We thank the many field and laboratory assistants, veterinary personnel and Malagasy colleagues who have aided our work in Madagascar from 2003 to 2011, and whom we have acknowledged in our previous publications. We thank the curatorial staffs at the American Museum of Natural History, the Denver Museum of Nature and Science and the United States National Museum of Natural History for access to the Eocene primate specimens we discuss herein. We also thank the curatorial staffs at the American Museum of Natural History, the United States National Museum of Natural History, the Natural History Museum (London), Harvard’s Museum of Comparative Zoology and the Museum für Naturkunde (Berlin) for access to the extant lemur specimens used in our analyses. We especially thank Greg Gunnell and Chris Beard for their thoughtful and helpful comments on our paper. Our work in Madagascar and the collection of museum data from 2003 to 2012 have been supported by the University of North Dakota (SSAC; Faculty Seed Money Award; Arts, Sciences and Humanities Award), ND EPSCoR, Primate Conservation Inc., The International Primatological Society, The St. Louis Zoo (FRC 06-1), The University of Colorado–Boulder (IGP and CRCW), The National Geographic Society, the American Society of Primatologists, The Lindbergh Fund and the United States National Science Foundation (BCS 0922465). All work with living lemurs in Madagascar was conducted with IACUC approval from the University of North Dakota and/or the University of Colorado–Boulder, with approval by Madagascar's governing authorities (ANGAP and/or MNP) and with CITES authorization.

References

  1. Anemone RL, Covert HH (2000) New skeletal remains of Omomys (Primates, Omomyidae): functional morphology of the hindlimb and locomotor behavior of a middle Eocene primate. J Hum Evol 38:607–633CrossRefGoogle Scholar
  2. Anthony MRL, Kay RF (1993) Tooth form and diet in ateline and alouattine primates: reflections on the comparative method. Am J Sci 293A:356–382CrossRefGoogle Scholar
  3. Beard KC, MacPhee RDE (1994) Cranial anatomy of Shoshonius and the antiquity of Anthropoidea. In: Fleagle JG, Kay RF (eds) Anthropoid origins. Plenum Press, New York, pp 55–97Google Scholar
  4. Beard KC, Krishtalka L, Stucky RK (1991) First skulls of the early Eocene primate Shoshonius cooperi and the anthropoid-tarsier dichotomy. Nature 349:64–67CrossRefGoogle Scholar
  5. Beard KC, Marivaux L, Chaimanee Y, Jaeger J-J, Marandat B, Tafforeau P, Soe AN, Tun ST, Kway AA (2009) A new primate from the Eocene Pondaung Formation of Myanmar and the monophyly of Burmese amphipithecids. Proc R Soc Lond Biol 276:3285–3294CrossRefGoogle Scholar
  6. Covert HH (1986) Biology of early Cenozoic primates. In: Swindler DR, Erwin J (eds) Comparative primate biology. Volume 1: systematics, evolution, and anatomy. Alan R. Liss, New York, pp 335–339Google Scholar
  7. Covert HH (1997) The early primate adaptive radiations and new evidence about anthropoid origins. In: Boaz NT, Wolfe LD (eds) Biological anthropology: the state of the science. Oregon State University Press IIHER Publications, International Institute for Human Evolutionary Research, Bend, pp 1–23Google Scholar
  8. Covert HH, Hamrick M (1993) Description of new skeletal remains of the early Eocene anaptomorphine primate Absarokius (Omomyidea) and a discussion of its adaptive profile. J Hum Evol 25:351–362CrossRefGoogle Scholar
  9. Cuozzo FP, Sauther ML (2004) Tooth loss, survival, and resource use in wild ring-tailed lemurs (Lemur catta): implications for inferring conspecific care in fossil hominids. J Hum Evol 46:625–633CrossRefGoogle Scholar
  10. Cuozzo FP, Sauther ML (2006) Severe wear and tooth loss in wild ring-tailed lemurs (Lemur catta): a function of feeding ecology, dental structure, and individual life history. J Hum Evol 51:490–505CrossRefGoogle Scholar
  11. Cuozzo FP, Sauther ML (2012) What is dental ecology? Am J Phys Anthropol 148:163–170CrossRefGoogle Scholar
  12. Cuozzo FP, Yamashita N (2006) Impact of ecology on dental adaptations of extant lemurs: a review of tooth function, variation, and life history. In: Gould L, Sauther ML (eds) Lemurs: ecology and adaptations. Springer, New York, pp 69–98Google Scholar
  13. Cuozzo FP, Sauther ML, Yamashita N, Lawler RR, Brockman DK, Godfrey LR, Gould L, Jacky Youssouf IA, Lent C, Ratsirarson J, Richard A, Scott JR, Sussman RW, Villers LM, Weber MA, Willis G (2008) A comparison of salivary pH in sympatric wild lemurs (Lemur catta and Propithecus verreauxi) at Beza Mahafaly Special Reserve, Madagascar. Am J Primatol 70:363–371CrossRefGoogle Scholar
  14. Cuozzo FP, Sauther ML, Gould L, Sussman RW, Villers LM, Lent C (2010) Variation in dental wear and tooth loss in known-aged, older ring-tailed lemurs (Lemur catta): a comparison between wild and captive individuals. Am J Primatol 72:1026–1037CrossRefGoogle Scholar
  15. Eaglen RH (1985) Behavioral correlates of tooth eruption in Madagascar lemurs. Am J Phys Anthropol 66:307–315CrossRefGoogle Scholar
  16. Fleagle JG (1998) Primate adaptation and evolution, 2nd edn. Academic Press, New YorkGoogle Scholar
  17. Franzen JL, Habersetzer J, Schlosser-Sturm E, Franzen EL (2011) Paleopathology of Darwinius masillae (Mammalia, Primates). In: Lehmann T, Schaal SFK (eds) The world at the time of Messel: puzzles in the palaeobiology, palaeoenvironment, and the history of the early primates (22nd Int Senckenberg Conf, conference volume). Senckenberg Gesellschaft für Naturforschung, Frankfurt am Main, pp 61-62Google Scholar
  18. Gould L, Sauther ML (2006) Lemurs: ecology and adaptation. Springer, New YorkGoogle Scholar
  19. Gunnell GF (1995) Omomyid primates (Tarsiiformes) from the bridger formation, middle Eocene, southern Green River Basin, Wyoming. J Hum Evol 28:147–187CrossRefGoogle Scholar
  20. Gunnell GF (1997) Wasatchian-Briderian (Eocene) paleoecology of the western interior of North America: changing paleoenvironments and taxonomic composition of omomyid (Tarsiiformes) primates. J Hum Evol 32:105–132CrossRefGoogle Scholar
  21. Jablonski NG, Leakey MG, Ward CV, Mauricio A (2008) Systematic paleontology of the large colobines. In: Jablonksi NG, Leakey MG (eds) Koobi fora research project. Volume 6. The fossil monkeys. California Academy of Sciences, San Francisco, pp 31–102Google Scholar
  22. Jaeger JJ, Chaimanee Y, Tafforeau P, Ducrocq S, Soe AN, Marivaux L, Sudre J, Tun ST, Htoon W, Marandat B (2004) Systematics and paleobiology of the anthropoid primate Pondaungia from the late Middle Eocene of Myanmar. C R Palevol 3:243–255CrossRefGoogle Scholar
  23. Jolly A, Sussman RW, Rasamimanana H (2006) Ringtailed lemur biology: Lemur catta in Madagascar. Springer, New YorkCrossRefGoogle Scholar
  24. Kappeler PM, Ganzhorn JU (1993) Lemur social systems and their ecological basis. Springer, New YorkGoogle Scholar
  25. Larsen RS, Sauther ML, Cuozzo FP (2011a) Evaluation of modified techniques for immobilization of wild ring-tailed lemurs (Lemur catta). J Zoo Wildl Med 42(4):623–633CrossRefGoogle Scholar
  26. Larsen RS, Moresco A, Sauther ML, Cuozzo FP (2011b) Field anesthesia of wild ring-tailed lemurs (Lemur catta) using tiletamine-zolazepam, medetomidine, and butorphanol. J Zoo Wildl Med 42(1):75–87CrossRefGoogle Scholar
  27. Lucas PW (2004) Dental functional morphology: how teeth work. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  28. Martin LB, Olejniczak AJ, Maas MC (2003) Enamel thickness and microstructure in pitheciin primates, with comments on dietary adaptations of the middle Miocene hominoid Kenyapithecus. J Hum Evol 45:351–367CrossRefGoogle Scholar
  29. Miller DS, Sauther ML, Hunter-Ishikawa M, Fish KD, Culbertson H, Cuozzo FP, Campbell TW, Chavey S, Nachreiner R, Rumbeiha W, Stacewicz-Sapantzakis M, Lappin MR (2007) Biomedical evaluation of free-ranging ring-tailed lemurs (Lemur catta) in three habitats at the Beza Mahafaly Special Reserve, Madagascar. J Zoo Wildl Med 38:201–216CrossRefGoogle Scholar
  30. Murphey PC, Torick LL, Bray ES, Chandler R, Evanoff E (2001) Taphonomy, fauna, and depositional environment of the Omomys quarry, an unusual accumulation from the Bridger Formation (Middle Eocene) of southwestern Wyoming (USA). In: Gunnell GF (ed) Eocene biodiversity: unusual occurrences and rarely sampled habitats. Kluwer Academic/Plenum Press, New York, pp 361–401CrossRefGoogle Scholar
  31. Powzyk JA, Mowry CB (2007) The feeding ecology and related adaptations of Indri indri. In: Gould L, Sauther ML (eds) Lemurs: ecology and adaptation. Springer, New York, pp 353–368Google Scholar
  32. Rakotosamimanana B, Rasamimanana H, Ganzhorn J, Goodman SM (1999) New directions in lemur studies. Springer, New YorkCrossRefGoogle Scholar
  33. Richard A (1977) The feeding behavior of Propithecus verreauxi. In: Clutton-Brock TH (ed) Primate ecology. Academic Press, London, pp 71–96Google Scholar
  34. Richard A (1978) Behavioral variation: a case study of a Malagasy lemur. Buckness University Press, LewisburgGoogle Scholar
  35. Rose KD, MacPhee RDE, Alexander JP (1999) Skull of early Eocene Cantius abditus (Primates: Adapiformes) and its phylogenetic implications, with a reevaluation of "Hesperolemur" actius. Am J Phys Anthropol 109:523–539CrossRefGoogle Scholar
  36. Ross C, Covert HH (2000) The petrosal of Omomys carteri and the evolution of the primate basicranium. J Hum Evol 39:225–251CrossRefGoogle Scholar
  37. Sauther ML, Cuozzo FP (2008) Somatic variation in living, wild ring-tailed lemurs (Lemur catta). Folia Primatol 79:55–78CrossRefGoogle Scholar
  38. Sauther ML, Cuozzo FP (2009) The impact of fallback foods on wild ring-tailed lemur biology: a comparison of intact and anthropogenically disturbed habitat. Am J Phys Anthropol 140:671–686CrossRefGoogle Scholar
  39. Sauther ML, Sussman RW, Cuozzo FP (2002) Dental and general health in a population of wild ring-tailed lemurs: a life history approach. Am J Phys Anthropol 117:122–132CrossRefGoogle Scholar
  40. Sussman RW, Richard RF, Ratsirarson J, Sauther ML, Brockman DK, Gould L, Lawler R, Cuozzo FP (2012) Beza Mahafaly Special Reserve: long-term research on lemurs in Southwestern Madagascar. In: Kappeler PM, Watts DP (eds) Long-term field studies of primates. Springer, Berlin, pp 45–66CrossRefGoogle Scholar
  41. Ungar PS (2002) Reconstructing the diets of fossil primates. In: Plavcan JM, Kay RF, Jungers WL, van Schaik CP (eds) Reconstructing behavior in the fossil record. Kluwer Academic/Plenum Press, Dordrecht/New York, pp 261–296CrossRefGoogle Scholar
  42. Ungar PS, M’Kirera F (2003) A solution to the worn tooth conundrum in primate functional anatomy. Proc Natl Acad Sci USA 100:3874–3877CrossRefGoogle Scholar
  43. Walker A, Hoeck HN, Perez L (1978) Microwear of mammalian teeth as an indicator of diet. Science 201:980–910CrossRefGoogle Scholar
  44. Williams BA, Covert HH (1994) New early Eocene anaptomorphine primate (Omomyidae) from the Washakie Basin, Wyoming, with comments on the phylogeny and paleobiology of anaptomorphines. Am J Phys Anthropol 93:323–340CrossRefGoogle Scholar
  45. Yamashita N, Cuozzo FP, Sauther ML (2012) Interpreting food processing through dietary mechanical properties: a Lemur catta case study. Am J Phys Anthropol 148:205–214CrossRefGoogle Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer 2012

Authors and Affiliations

  1. 1.Department of AnthropologyUniversity of ColoradoBoulderUSA
  2. 2.Department of AnthropologyUniversity of North DakotaGrand ForksUSA

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