International Journal of Primatology

, Volume 28, Issue 1, pp 159–182 | Cite as

Bimorphism in Male Verreaux’s Sifaka in the Kirindy Forest of Madagascar

  • Rebecca J. Lewis
  • Carel P. van Schaik

Male primates in species with pronounced secondary sexual adornments can exhibit reversible or irreversible bimorphism, i.e., striking variation in the degree to which males express the adornments. Verreaux’s sifaka (Propithecus verreauxi verreauxi) use scent marking as a form of communication and exhibit sex differences in scent glands. Some males exhibit a pronounced brown staining around their sternal gland, whereas others do not. We studied morphological and behavioral characteristics of males in 6 social groups in Kirindy Forest, Madagascar, from November 2000 to March 2002 to evaluate the hypotheses that the bimorphism in male sifaka chest status represents alternative mating tactics and is a badge of status. Males are clearly divided into 2 categories: clean and stained chests, with rare, but informative, intermediate males. The chest staining probably results from the males scent marking with their sternal glands, because stained-chested males scent marked significantly more often than clean-chested males. Though sample sizes are small, chest status did not appear to depend on body size. Chest status is reversible and related to dominance rank. In each group, only 1 male, the dominant, was stained-chested, whereas all other (subordinate) males were clean-chested. These findings suggest that stained chests are visual and olfactory signals of dominance rank and that clean chests signal lack of competitive intent. Thus, this bimorphism may reflect alternative mating tactics used by males to maximize their reproductive success based upon their social environment.


alternative mating strategies Propithecus Sexual selection signal 



We thank D. Brockman, M. Gerald, K. Glander, P. Kappeler, C. Kirk, K. Smith, M. Munger, D. Overdorff, and J. Mitani for valuable discussion and comments on the manuscript as well as 4 anonymous reviewers. Discussion in a departmental seminar at Duke University greatly improved the research. We thanks P. Kappeler, DPZ, the Malagasy Government, Eaux et Fôrets, CFPF, MICET, D. Rakotondavony, Enafa, J. Ratsirarson, and the Kirindy sifaka team for assistance in captures. Research methods were in compliance with the requirements of Madagascar. The Wenner-Gren and Leakey Foundations funded the research. The material is based on work supported by the National Science Foundation Dissertation Improvement Grant to RJL under grant no. 0002570.


  1. Abernathy, K. A., White, L. J. T., and Wickings, E. J. (2002). Hordes of mandrills (Mandrillus sphinx): Extreme group size and seasonal male presence. J. Zool. Lond. 258: 131–137.Google Scholar
  2. Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour 48: 227–265.Google Scholar
  3. Brockman, D. K. (1994). Reproduction and Mating System of Verreaux’s Sifaka, Propithecus verreauxi, at Beza Mahafaly, Madagascar. Doctoral thesis. Yale University, New Haven, CT.Google Scholar
  4. Brockman, D. K. (1999). Reproductive behavior of female Propithecus verreauxi at Beza-Mahafaly, Madagascar. Int. J. Primatol. 20: 375–398.CrossRefGoogle Scholar
  5. Brockman, D. K., Whitten, P. L., Richard, A. F., and Schneider, A. (1998). Reproduction in free-ranging male Propithecus verreauxi: The hormonal correlates of mating and aggression. Am. J. Phys. Anthropol. 105: 137–151.PubMedCrossRefGoogle Scholar
  6. Brockman, D. K., Whitten, P. L., Richard, A. F., and Benander, B. (2001). Birth season testosterone levels in male Verreaux’s sifaka, Propithecus verreauxi: Insights into socio-demographic factors mediating seasonal testicular function. Behav. Ecol. Sociobiol. 49: 117–127.CrossRefGoogle Scholar
  7. Cohen J. (1988). Statistical Power Analysis for the Behavioral Sciences, 2nd ed. Lawrence Earlbaum, Hillsdale, NJ.Google Scholar
  8. Dawkins, R. (1980). Good strategy or evolutionary stable strategy? In Barlow, G. W., and Silverberg, J. (eds.), Sociobiology: Beyond Nature/Nurture? Westview, Boulder, CO, pp. 331–367.Google Scholar
  9. Dill, A. (2000). Aspekte der Jungenaufzucht bei Larvensifakas (Propithecus verreauxi verreauxi, Grandidier 1867, Primates: Indriidae). Msc-thesis. University of Würzburg, Würzburg, Germany.Google Scholar
  10. Dixson, A. F. (1976). Effects of testosterone on the sternal cutaneous glands and genitalia of the male greater galago (Galago crassicaudatus crassicaudatus). Folia Primatol. 26: 207–213.PubMedCrossRefGoogle Scholar
  11. Dixson, A. F. (1998). Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes, and Human Beings. Oxford University Press, Oxford.Google Scholar
  12. Ganzhorn, J. U. (2002). Distribution of a folivorous lemur in relation to seasonally varying food resources: Integrating quantitative and qualitative aspects of food characteristics. Oecologia 131: 427–435.CrossRefGoogle Scholar
  13. Ganzhorn, J. U., and Sorg, J.-P., eds. (1996). Ecology and economy of a tropical dry forest in Madagascar. Primate Report 46–1.Google Scholar
  14. Gerald, M. S. (2001). Primate colour predicts social status and aggressive outcome. Anim. Behav. 61: 559–566.CrossRefGoogle Scholar
  15. Gerald, M. S. (2003). How color may guide the primate world: Possible relationships between sexual selection and sexual dichromatism. In Jones, C. B. (ed), Sexual Selection and Reproductive Competition in Primates: New Perspectives and Directions. American Society of Primatologists, Norman, OK, pp. 141–171.Google Scholar
  16. Gerald, M. S., and Raleigh, M. J. (1997). A potential proximate mechanism for scrotal colour variation in captive vervet monkeys (Cercopithecus aethiops sabaeus). Am. J. Primatol. 42: 111–112.Google Scholar
  17. Glander, K. E., Wright, P. C., Daniels, P. S., and Merenlender, A. M. (1992). Mophometrics and testicle size of rain forest lemur species from southeastern Madagascar. J. Hum. Evol. 22: 1–17.CrossRefGoogle Scholar
  18. Grieser, B. (1992). Infant development ad parental care in two species of sifakas. Primates 33: 305–314.CrossRefGoogle Scholar
  19. Jolly, A. (1966). Lemur Behavior: A Madagascar Field Study. University of Chicago Press: Chicago, IL.Google Scholar
  20. Katsir, Z., and Crewe, R. M. (1980). Chemical communication in Galago crassicaudatus: investigation of the chest gland secretion. S. Afr. J. Zool. 15: 249–254.Google Scholar
  21. Kraus, C., Heistermann, M., and Kappeler, P. M. (1999). Physiological suppression of sexual function of subordinate males: A subtle form of intrasexual competition among male sifakas (Propithecus verreauxi)? Physiol. Behav. 66: 855–861.PubMedCrossRefGoogle Scholar
  22. Kubzdela, K. S. (1997). Sociodemography in Diurnal Primates: The Effects of Group Size and Female Dominance Rank on Intra-group Spatial Distribution, Feeding Competition, Female Reproductive Success, and Female Dispersal Patterns in White Sifaka, Propithecus verreauxi verreauxi. Doctoral thesis. University of Chicago, Chicago.Google Scholar
  23. Lawler, R. R. (2003). Causes and Consequences of Differential Reproductive Success in Male White Sifaka (Propithecus verreauxi verreauxi). Doctoral thesis. Yale University, New Haven, CT.Google Scholar
  24. Lawler, R. R., Richard, A. F., and Riley, M. A. (2005). Intrasexual selection in Verreaux’s sifaka (Propithecus verreauxi verreauxi). J. Hum. Evol. 48: 259–277.PubMedCrossRefGoogle Scholar
  25. Lewis, R. J. (2004). Male-Female Relationships in Sifaka (Propithecus verreauxi verreauxi): Power, Conflict, and Cooperation. Doctoral thesis. Duke University, Durham, NC.Google Scholar
  26. Lewis, R. J. (2005). Sex differences in scent-marking in sifaka: Mating conflict or male services? Am. J. Phys. Anthropol. 128: 389–398.PubMedCrossRefGoogle Scholar
  27. Lewis, R. J. (2006). Scent-marking in sifaka: No one function explains it all. Am. J. Primatol. 68(6): 622–636.Google Scholar
  28. Lewis, R. J., Razafindrasamba, S. M., and Tolojanahary, J. P. (2003). Observed infanticide in a seasonal breeding prosimian (Propithecus verreauxi verreauxi) in Kirindy Forest, Madagascar. Folia Primatol. 74(2): 101–103.Google Scholar
  29. Lewis, R. J., and Kappeler, P. M. (2005). Seasonality, Body Condition, and the Timing of Reproduction in Propithecus verreauxi verreauxi in the Kirindy Forest. Am. J. Primatol. 67(3): 347–364.Google Scholar
  30. Maggioncalda, A. N., Sapolsky, R. M., and Czekala, N. M. (1999). Reproductive hormone profiles in captive male orangutans: Implications for understanding developmental arrest. Am. J. Phys. Anthropol. 109: 19–32.PubMedCrossRefGoogle Scholar
  31. Maggioncalda, A. N., Czekala, N. M., and Sapolsky, R. M. (2000). Growth hormone and thyroid stimulating hormone concentrations in captive male orangutans: Implications for understanding developmental arrest. Am. J. Primatol. 50: 67–76.PubMedCrossRefGoogle Scholar
  32. McGraw, K. J., Dale, J., and Mackillop, E. A. (2003). Social environment during molt and the expression of melanin-based plumage pigmentation in male house sparrows (Passer domesticus). Behav. Ecol. Sociobiol. 53: 116–122.Google Scholar
  33. Mertl, A. S. (1976). Olfactory and visual cues in social interactions of Lemur catta. Folia Primatol. 26: 151–161.Google Scholar
  34. Petter, J.-J. (1962). Recherches sur l’ecologie et l’ethologie des lemuriens Malagaches. Mém. Mus. Nat. Hist. Nat. 27: 1–146.Google Scholar
  35. Preuschoft, S., and van Schaik, C. P. (2000). Dominance and communication: Conflict management in various social settings. In Aureli, F., and de Waal, F. B. M. (eds), Natural Conflict Resolution. University of California Press, Berkeley, pp. 77–105.Google Scholar
  36. Rensing, S. (1999). Immobilization and anesthesia of nonhuman primates. Primate Report 55: 33–38.Google Scholar
  37. Richard, A. F. (1978). Behavioral Variation: Case Study of a Malagasy Lemur. Bucknell University: Lewisburg, PA.Google Scholar
  38. Richard, A. F. (1985). Social boundaries in a Malagasy prosimian, the sifaka (Propithecus verreauxi). Int. J. Primatol. 6: 553–568.Google Scholar
  39. Richard, A. F. (1992). Aggressive competition between males, female-controlled polygyny and sexual monomorphism in a Malagasy primate, Propithecus verreauxi. J. Hum. Evol. 22: 395–406.CrossRefGoogle Scholar
  40. Richard, A. F., Rakotomanga, P., and Schwartz, M. (1993). Dispersal by Propithecus verreauxi at Beza Mahafaly, Madagascar: 1984–1991. Am. J. Primatol. 30: 1–20.CrossRefGoogle Scholar
  41. Richard, A. F., Dewar, R. E., Schwartz, M., and Ratsirarson, J. (2000). Mass change, environmental variability and female fertility in wild Propithecus verreauxi. J. Hum. Evol. 39: 381–391.PubMedCrossRefGoogle Scholar
  42. Richard, A. F., Dewar, R. E., Schwartz, M., and Ratsirarson, J. (2002). Life in the slow lane? Demography and life histories of male and female sifaka (Propithecus verreauxi verreauxi). J. Zool. Lond. 256: 421–436.Google Scholar
  43. Rohwer, S., and Ewald, P. W. (1981). The cost of dominance and advantage of subordination in a badge signaling system. Evolution 35: 441–454.CrossRefGoogle Scholar
  44. Rohwer, S., Fretwell, S. D., and Niles, D. M. (1980). Delayed maturation in passirine plumages and the deceptive acquisition of resources. Am. Nat. 115: 400–437.CrossRefGoogle Scholar
  45. Ronow R. L., and Rosenthal R. (1996). Computing contrasts, effect sizes, and countermills on other people’s published data: General procedures for research consumers. Psychol. Methods 1: 331–340.CrossRefGoogle Scholar
  46. Schilling, A. (1979). Olfactory communication in prosimians. In Doyle, G. A., and Martin, R. D. (eds), The Study of Prosimian Behavior. Academic Press, New York, pp. 461–542.Google Scholar
  47. Setchell, J. M. (2003). The evolution of alternative reproductive morphs in male primates. In Jones, C. B. (ed), Sexual Selection and Reproductive Competition in Primates: New Perspectives and Directions. American Society of Primatologists: Norman, OK, pp. 271–281.Google Scholar
  48. Setchell, J. M., and Dixson, A. F. (2001a). Arrested development of secondary sexual adornments in subordinate adult male mandrills (Mandrillus sphynx). Am. J. Phys. Anthropol. 115: 245–252.PubMedCrossRefGoogle Scholar
  49. Setchell, J. M., and Dixson, A. F. (2001b). Changes in secondary sexual adornments of male mandrills (Mandrillus sphynx) are associated with gain and loss of alpha status. Horm. Behav. 39: 177–184.PubMedCrossRefGoogle Scholar
  50. Setchell, J. M., and Dixson, A. F. (2002). Developmental variables and dominance rank in adolescent male mandrills (Mandrillus sphynx). Am. J. Primatol. 56: 9–25.PubMedCrossRefGoogle Scholar
  51. Setchell, J. M., and Wickings, J. (2005). Dominance, status signals, and coloration in male mandrills (Mandrillus sphinx). Ethology 111: 25–50.CrossRefGoogle Scholar
  52. Siegel, S., and Castellan, N. J. (1988). Nonparametric Statistics for the Behavioral Sciences. McGraw-Hill, New York.Google Scholar
  53. Shuster, S. M., and Wade, M. J. (2003). Mating Systems and Strategies. Princeton University Press, Princeton, NJ.Google Scholar
  54. Slagsvold, T., and Sætre, G.-P. (1991). Evolution of plumage colour in male pied flycatchers (Ficedula hypoleuca): Evidence for female mimicry. Evolution 45: 910–917.CrossRefGoogle Scholar
  55. Utami, S. S., Goossens, B., Bruford, M. W., de Ruiter, J. R., and van Hooff, J. A. R. A. M. (2002). Male bimaturism and reproductive success in Sumatran orang-utans. Behav. Ecol. 13: 643–652.CrossRefGoogle Scholar
  56. Utami Atmoko, S., and van Hooff, J. A. R. A. M. (2004). Alternative male reproductive strategies: male bimaturism in orangutans. In Kappeler, P. M., and van Schaik C. P. (eds), Sexual Selection in Primates: New and Comparative Perspectives. Cambridge University Press, Cambridge, pp. 196–207.Google Scholar
  57. van Noordwijk, M. A., and van Schaik, C. P. (1985). Male migration and rank acquisition in wild long-tailed macaques (Macaca fascicularis). Anim. Behav. 33: 849–861.CrossRefGoogle Scholar
  58. van Schaik, C. P. (2004). Among Orangutans: Red Apes and the Rise of Human Culture. Harvard University Press, Cambridge, MA.Google Scholar
  59. van Schaik, C. P., Pradhan, G. R., and van Noordwijk, M. A. (2004). Mating conflict in primates: infanticide, sexual harassment and female sexuality. In Kappeler, P. M., and van Schaik, C. P. (eds), Sexual Selection in Primates: New and Comparative Perspectives. Cambridge University: Cambridge, pp. 131–150.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  1. 1.Department of AnthropologyUniversity of Texas at AustinAustinUSA
  2. 2.Anthropological Institute and MuseumUniversity of Zürich8057 ZürichSwitzerland

Personalised recommendations