Dominance, Coloration, and Social and Sexual Behavior in Male Drills Mandrillus leucophaeus

  • Jill S. Marty
  • James P. Higham
  • Elizabeth L. Gadsby
  • Caroline Ross
Article

Abstract

Sexual selection has driven the evolution and elaboration of a wide variety of displays and ornaments in male nonhuman primates, including capes, cheek flanges, and sexual coloration. Among the most sexually dimorphic of all primates is the drill (Mandrillus leucophaeus), the males of which can be 3 times the mass of females, possess large canines, and exhibit extremely bright sexual skin coloration. However, the function of male coloration in this species has never been examined. Here, we present data on male color (measured objectively using digital photography), dominance rank, measures of male-female association, and key sexual behaviors, of adult male drills (n = 17) living in four semi free-ranging enclosures at the Drill Rehabilitation and Breeding Center in Nigeria. We test the hypothesis that male coloration is a badge of status, indicating dominance rank, and the hypothesis that male coloration attracts females. We found that male coloration did indicate rank, and that high ranking, strongly colored males were more likely to associate with adult females, and more specifically with fully tumescent females. These males also engaged in more sexual activity. However, measures of male-female association and sexual behaviors were not related to male color once rank had been taken into consideration; i.e., for males of a given rank, females did not prefer those that were more colorful. We discuss the results in light of what is known about the wild drill social system, in which unfamiliar individuals may come together in “supergroups,” and in which quality indicators of competitive ability may be particularly important.

Keywords

color dichromatism female choice male-male competition Mandrillus sexual signals 

References

  1. Abernethy, K. A., White, L. J. T., & Wickings, E. J. (2002). Hordes of mandrills (Mandrillius sphinx): Extreme group size and seasonal male presence. Journal of Zoology, 258, 131–137.CrossRefGoogle Scholar
  2. Altmann, J. (1974). Observational study of behavior: Sampling methods. Behavior, 49, 227–267.CrossRefGoogle Scholar
  3. Astaras, C., Mulenberg, M., & Walter, M. (2008). Note on drill (Mandrillus leucophaeus) ecology and conservation status in Korup National Park, Southwest Cameroon. American Journal of Primatology, 70, 306–310.CrossRefPubMedGoogle Scholar
  4. Bercovitch, F. B. (1996). Testicular function and scrotal color in patas monkeys. Journal of Zoology, 239, 93–100.CrossRefGoogle Scholar
  5. Bergman, T. J., & Beehner, J. C. (2008). A simple method for measuring color variation in wild animals: Validation and use in geladas (Theropithecus gelada). Biological Journal of the Linnean Society, 94, 231–240.CrossRefGoogle Scholar
  6. Bergman, T. J., Ho, L., & Beehner, J. C. (2009). Chest color and social status in male geladas (Theropithecus gelada). International Journal of Primatology, 30. doi:10.1007/s10764-009-9374-x.
  7. Boer, M. (1987). Recent advances in drill research and conservation. Primate Conservation, 8, 55–57.Google Scholar
  8. Charpentier, M., Peignot, P., Hossaert-McKey, M., Gimenez, O., Setchell, J. M., & Wickings, E. J. (2005). Constraints on control: Factors influencing reproductive success in male mandrills (Mandrillus sphinx). Behavioral Ecology, 16, 614–623.CrossRefGoogle Scholar
  9. Cowlishaw, G., & Dunbar, R. I. M. (1991). Dominance rank and mating success in male primates. Animal Behaviour, 41, 1045–1056.CrossRefGoogle Scholar
  10. Cox, C. R. (1997). Drills (Mandrillus leucophaeus): Research and conservation initiatives, 1986–1996. In J. Wallis (Ed.), Primate conservation: The role of zoological parks (pp. 151–175). Norman, OK: American Society of Primatologists.Google Scholar
  11. Darwin, C. (1871). The descent of man and selection in relation to sex. London: John Murray.Google Scholar
  12. Darwin, C. (1876). Sexual selection in relation to monkeys. Nature, 15, 18–19.CrossRefGoogle Scholar
  13. de Ruiter, J. R., & van Hoof, J. A. R. A. M. (1993). Male dominance rank and reproductive success in primate groups. Primates, 34, 513–523.CrossRefGoogle Scholar
  14. Dixson, A. F. (1998). Primate sexuality: Comparative studies of the prosimians, monkeys, apes, and human beings. Oxford: Oxford University Press.Google Scholar
  15. Dixson, A. F., Bossi, T., & Wickings, E. J. (1993). Male dominance and genetically determined reproductive status in the mandrill (Mandrillus sphinx). Primates, 34, 525–532.CrossRefGoogle Scholar
  16. Dunbar, R. I. M. (1984). Reproductive decisions: An economic analysis of gelada baboon social strategies. Princeton, NJ: Princeton University Press.Google Scholar
  17. Elton, S., Bethan, J., & Morgan, B. J. (2006). Muzzle size, paranasal swelling size and body mass in Mandrillus leucophaeus. Primates, 47, 151–157.CrossRefPubMedGoogle Scholar
  18. Gartlan, J. S. (1970). Preliminary notes on the ecology and behaviour of the Drill Mandrillus leucophaeus Ritgen, 1824. In J. R. Napier & P. H. Napier (Eds.), Old World monkeys (pp. 445–480). New York: Academic Press.Google Scholar
  19. Gerald, M. S. (2001). Primate color reveals social status and predicts aggressive outcome. Animal Behaviour, 61, 559–566.CrossRefGoogle Scholar
  20. Gerald, M. S., Bernstein, J., Hinkson, R., & Fosbury, R. A. E. (2001). Formal method for objective assessment of primate color. American Journal of Primatology, 53, 79–85.CrossRefPubMedGoogle Scholar
  21. Higham, J. P. (2006). The reproductive ecology of female olive baboons (Papio hamadryas anubis) at Gashaka-Gumti National Park, Nigeria. Ph.D. Thesis, Roehampton University, London.Google Scholar
  22. Higham, J. P., MacLarnon, A. M., Ross, C., Heistermann, M., & Semple, S. (2008). Baboon sexual swellings: Information content of size and color. Hormones and Behavior, 53, 452–462.CrossRefPubMedGoogle Scholar
  23. Hill, W. C. O. (1955). A note on integumental colours with special reference to the genus Mandrillus. Saeugetierkündliche Mitteilungen, 3, 145–155.Google Scholar
  24. Hill, W. C. O. (1970). Primates: Comparative anatomy, and taxonomy, vol 8: Cynopithecinae. Edinburgh: Edinburgh University Press.Google Scholar
  25. IUCN. (2008). IUCN Red List of Threatened Species. www.iucnredlist.org (Accessed February 20, 2009).
  26. Jarvi, T., & Bakken, M. (1984). The function of the variation in the breast stripe of the great tit (Parus major). Animal Behaviour, 32, 590–596.CrossRefGoogle Scholar
  27. Kummer, H. (1968). Social organization of hamadryas baboons. Chicago: The University of Chicago Press.Google Scholar
  28. Maynard-Smith, J., & Harper, D. (2003). Animal signals. Oxford: Oxford University Press.Google Scholar
  29. Møller, A. P. (1992). Female swallow preference for symmetrical male sexual ornaments. Nature, 357, 238–240.CrossRefPubMedGoogle Scholar
  30. Nagel, L., & Schluter, D. (1998). Body size, natural selection, and speciation in sticklebacks. Evolution, 52, 209–218.CrossRefGoogle Scholar
  31. Packer, C. (1983). Sexual dimorphism: The horns of African antelopes. Science, 221, 1191–1193.CrossRefPubMedGoogle Scholar
  32. Paul, A., Kuester, J., Timme, A., & Arnemann, J. (1993). The association between rank, mating effort, and reproductive success in male Barbary macaques (Macaca sylvanus). Primates, 34, 491–502.CrossRefGoogle Scholar
  33. Reed, C., O’Brien, T. G., & Kinnaird, M. F. (1997). Male social behavior and dominance hierarchy in the Sulawesi crested black macaque (Macaca nigra). International Journal of Primatology, 18, 247–260.CrossRefGoogle Scholar
  34. Rhodes, L., Argersinger, M. E., Gantert, L. T., Friscino, B. H., Hom, G., Pikounis, B., et al. (1997). Effects of administration of testosterone, dihydrotestosterone, oestrogen and fadrozole, an aromatase inhibitor, on sex skin colour in intact male rhesus macaques. Reproduction, 111, 51–57.CrossRefGoogle Scholar
  35. Schürmann, C. L. (1982). Mating behavior of wild orangutans. In L. de Boer, L. (Ed.), The Orang-Utan: Its biology and conservation (pp. 271–286). The Hague: Junk Publishers.Google Scholar
  36. Setchell, J. M. (2005). Do female mandrills prefer brightly colored males? International Journal of Primatology, 26, 715–734.CrossRefGoogle Scholar
  37. Setchell, J. M., Charpentier, M. J. E., Abbott, K. M., Wickings, E. J., & Knapp, L. A. (2009). Is brightest best? Testing the Hamilton-Zuk hypothesis in Mandrills. International Journal of Primatology, 30. doi:10.1007/s10764-009-9371-0.
  38. Setchell, J. M., Charpentier, M., & Wickings, E. J. (2005). Mate guarding and paternity in mandrills: Factors influencing alpha male monopoly. Animal Behaviour, 70, 1105–1120.CrossRefGoogle Scholar
  39. Setchell, J. M., & Dixson, A. F. (2001a). Arrested development of secondary sexual adornments in subordinate adult male mandrills (Mandrillus sphinx). American Journal of Physical Anthropology, 115, 245–252.CrossRefPubMedGoogle Scholar
  40. Setchell, J. M., & Dixson, A. F. (2001b). Changes in the secondary sexual adornments of male mandrills (Mandrillus sphinx) are associated with gain and loss of alpha status. Hormones and Behaviour, 39, 177–184.CrossRefGoogle Scholar
  41. Setchell, J. M., & Dixson, A. F. (2001c). Circannual changes in the secondary sexual adornments of semifree-ranging male and female mandrills (Mandrillus sphinx). American Journal of Primatology, 53, 109–121.CrossRefPubMedGoogle Scholar
  42. Setchell, J. M., & Kappeler, P. M. (2003). Selection in relation to sex in primates. Advances in the Study of Behavior, 33, 87–173.CrossRefGoogle Scholar
  43. Setchell, J. M., Lee, P. C., Wickings, J. E., & Dixson, A. F. (2001). Growth and ontogeny of sexual size dimorphism in the mandrill (Mandrillus sphinx). American Journal of Physical Anthropology, 115, 349–360.CrossRefPubMedGoogle Scholar
  44. Setchell, J. M., & Wickings, J. E. (2005). Dominance, status signals and coloration in male mandrills (Mandrillus sphinx). Ethology, 111, 25–50.CrossRefGoogle Scholar
  45. Setchell, J. M., Wickings, E. J., & Knapp, L. A. (2006). Life history in male mandrills (Mandrillus sphinx): Physical development, dominance rank, and group association. American Journal of Physical Anthropology, 131, 498–510.CrossRefPubMedGoogle Scholar
  46. Stevens, M., Párraga, A., Cuthill, I. C., Partridge, J. C., & Troscianko, T. (2007). Using digital photography to study animal coloration. Biological Journal of the Linnean Society, 90, 211–237.CrossRefGoogle Scholar
  47. Stevens, M., Stoddard, M. C., & Higham, J. P. (2009). Studying primate color: Towards visual system-dependent methods. International Journal of Primatology, 30. doi:10.1007/s10764-009-9356-z.
  48. Thompson, C. W., & Moore, M. C. (1991). Throat color reliably signals status in male tree lizards, Urosaurus ornatus. Animal Behaviour, 42, 745–753.CrossRefGoogle Scholar
  49. van Schaik, C. P., & van Hooff, J. A. R. A. M. (1996). Towards an understanding of the orangutan’s social system. In W. C. McGrew, L. F. Marchant & T. Nishida (Eds.), Great ape societies (pp. 3–15). Chicago: The University of Chicago Press.Google Scholar
  50. Waitt, C., Little, A. C., Wolfensohn, S., Honess, P., Brown, A. P., Buchanan-Smith, H. M. F., et al. (2003). Evidence from rhesus macaques suggests male coloration plays a role in female primate mate choice. Proceedings Royal Society London Series B (Suppl.), 270, S144–146.CrossRefGoogle Scholar
  51. Wickings, E. J., Bossi, T., & Dixson, A. F. (1993). Reproductive success in the mandrill (Mandrillus sphinx): Correlations of male dominance and mating success with paternity as determined by DNA fingerprinting. Journal of Zoology (London), 231, 563–574.CrossRefGoogle Scholar
  52. Wickings, E. J., & Dixson, A. F. (1992). Testicular function, secondary sexual development and social status in male mandrills (Mandrillus sphinx). Physiology & Behavior, 52, 909–916.CrossRefGoogle Scholar
  53. Wickler, W. (1967). Socio-sexual signals and their intra-specific imitation among primates. In D. Morris (Ed.), Primate ethology (pp. 69–147). London: Weidenfeld & Nicolson.Google Scholar
  54. Wickler, W. (1968). Mimicry in plants and animals. New York: McGraw-Hill.Google Scholar
  55. Wild, C., Morgan, B. J., & Dixson, A. F. (2005). Conservation of drill populations in Bakossiland, Cameroon: Historical trends and current status. International Journal of Primatology, 26, 759–773.CrossRefGoogle Scholar
  56. Wood, K. L. (2007). Life history and behavioral characteristics of a semi-wild population of drills (Mandrillus leucophaeus) in Nigeria. Ph.D. thesis, University of Massachusetts, Boston.Google Scholar
  57. Zuckerman, S., & Parkes, A. S. (1939). Observations on the secondary sexual characters in monkeys. Journal of Endocrinology, 1, 430–439.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Jill S. Marty
    • 1
  • James P. Higham
    • 2
  • Elizabeth L. Gadsby
    • 4
  • Caroline Ross
    • 1
  1. 1.School of Human & Life SciencesRoehampton UniversityLondonUK
  2. 2.School of Human & Life SciencesRoehampton UniversityLondonUK
  3. 3.Institute for Mind and BiologyUniversity of ChicagoChicagoUSA
  4. 4.PandrillusCalabarNigeria

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