International Journal of Primatology

, Volume 29, Issue 4, pp 885–905 | Cite as

Male Mating Interest Varies with Female Fecundity in Pan troglodytes schweinfurthii of Kanyawara, Kibale National Park

  • Melissa Emery ThompsonEmail author
  • Richard W. Wrangham


Female chimpanzees mate promiscuously during a period of extended receptivity marked by prominent sexual swelling. Recent studies of wild chimpanzees indicate that subtle variations in swelling size could act as a reliable cue of female fertilization potential both within and between cycles (Emery and Whitten Behavioral Ecology and Sociobiology, 54, 340–351, 2003; Deschner et al. Hormones and Behavior, 46, 204–215, 2004). Copulation rates increase during the periovulatory period and during conception cycles (Deschner et al. Hormones and Behavior, 46, 204–215, 2004; Emery Thompson American Journal of Primatology, 67, 137–158, 2005a), suggesting that males may be able to assess female fertilization potential. We asked whether facultative timing of copulation in Kanyawara chimpanzees was due to increased male mating interest or to increased female proceptivity during the most fecund days. We assessed multiple measures of male mating effort in cycles aligned relative to the day of detumescence and compared periovulatory days to other days of maximal swelling, and conception cycles to nonconception cycles. The rate and proportion of male initiative in soliciting sexual behavior increased during periods of highest fertilization potential. Males were also more likely to interrupt copulations, associate with estrous females, and compete with other males when females were most likely to conceive. Females initiated copulations more frequently during conception cycles but did not visibly shift mating behavior within cycles. Our results support the hypothesis that male chimpanzees have the ability to assess the profitability of mating attempts, a trait that may act as a counter-adaptation to female strategies to obscure paternity. We discuss potential cues and the implications for female reproductive strategies.


attractiveness chimpanzees fecundity sexual behavior sexual swellings 



Funding from NSF Grant 0416126, Harvard University, the L.S.B. Leakey Foundation, and the Wenner-Gren Foundation for Anthropological Research supported research at Kanyawara. The Uganda National Council for Science and Technology, the Uganda Wildlife Authority, and the Makerere University Biological Field Station provided local research support and permissions. Francis Mugurusi, the late Christopher Muruuli, Peter Tuhairwe, the late John Barwogeza, Christopher Katongole, and the late Donor Muhangyi performed daily data collection, with field management by Michael Wilson, Martin Muller, Katherine Pieta, Carole Hooven, and Kimberly Duffy. We thank Anne Pusey, Rebecca Stumpf, and Ian Gilby for suggestions on the manuscript.


  1. Andersson, M. (1994). Sexual selection. Princeton, NJ: Princeton University Press.Google Scholar
  2. Boesch, C., Kohou, G., Nene, H., & Vigilant, L. (2006). Male competition and paternity in wild chimpanzees of the Tai Forest. American Journal of Physical Anthropology, 130, 103–115. doi: 10.1002/ajpa.20341.PubMedCrossRefGoogle Scholar
  3. Bonsall, R., & Michael, R. (1980). The externalization of vaginal fatty acids by the female rhesus monkey. Journal of Chemical Ecology, 6, 499–509. doi: 10.1007/BF01402926.CrossRefGoogle Scholar
  4. Chapman, C. A., & Wrangham, R. W. (1993). Range use of the forest chimpanzees of Kibale: Implications for the understanding of chimpanzee social organization. American Journal of Physical Anthropology, 31, 263–273.Google Scholar
  5. Constable, J. L., Ashley, M. V., Goodall, J., & Pusey, A. E. (2001). Noninvasive paternity assignment in Gombe chimpanzees. Molecular Ecology, 10, 1279–1300. doi: 10.1046/j.1365-294X.2001.01262.x.PubMedCrossRefGoogle Scholar
  6. Curtis, R., Ballantine, J., Keverne, E., Bonsall, R., & Michael, R. (1971). Identification of primate sexual pheromones and the properties of synthetic attractants. Nature, 232, 396–398. doi: 10.1038/232396a0.PubMedCrossRefGoogle Scholar
  7. Deschner, T., Heistermann, M., Hodges, K., & Boesch, C. (2003). Timing and probability of ovulation in relation to sex skin swelling in wild West African chimpanzees, Pan troglodytes verus. Animal Behaviour, 66, 551–560. doi: 10.1006/anbe.2003.2210.CrossRefGoogle Scholar
  8. Deschner, T., Heistermann, M., Hodges, K., & Boesch, C. (2004). Female sexual swelling size, timing of ovulation, and male behavior in wild West African chimpanzees. Hormones and Behavior, 46, 204–215. doi: 10.1016/j.yhbeh.2004.03.013.PubMedCrossRefGoogle Scholar
  9. Dixson, A. F. (1983). Observations on the evolution and behavioral significance of “sexual skin” in female primates. Advances in the Study of Behavior, 13, 63–106. doi: 10.1016/S0065-3454(08)60286-7.CrossRefGoogle Scholar
  10. Domb, L. G., & Pagel, M. D. (2001). Sexual swellings advertise female quality in wild baboons. Nature, 410, 204–206. doi: 10.1038/35065597.PubMedCrossRefGoogle Scholar
  11. Doran, D. M. (1997). Influence of seasonality on activity patterns, feeding behavior, ranging, and grouping patterns in Taï chimpanzees. International Journal of Primatology, 18, 183–206. doi: 10.1023/A:1026368518431.CrossRefGoogle Scholar
  12. Eberhard, W. G. (1996). Female control: Sexual selection by cryptic female choice. Princeton, NJ: Princeton University Press.Google Scholar
  13. Emery, M. A., & Whitten, P. L. (2003). Size of sexual swellings reflects ovarian function in chimpanzees (Pan troglodytes). Behavioral Ecology and Sociobiology, 54, 340–351. doi: 10.1007/s00265-003-0648-6.CrossRefGoogle Scholar
  14. Emery Thompson, M. (2005a). Reproductive endocrinology of wild female chimpanzees (Pan troglodytes schweinfurthii): Methodological considerations and the role of hormones in sex and conception. American Journal of Primatology, 67, 137–158. doi: 10.1002/ajp.20174.PubMedCrossRefGoogle Scholar
  15. Emery Thompson, M. (2005b). Endocrinology and ecology of wild female chimpanzee reproduction. PhD dissertation, Harvard University, Cambridge, MA.Google Scholar
  16. Emery Thompson, M., Kahlenberg, S. M., Gilby, I. C., & Wrangham, R. W. (2007). Core area quality is associated with variance in reproductive success among female chimpanzees at Kanyawara, Kibale National Park. Animal Behaviour, 73, 501–512. doi: 10.1016/j.anbehav.2006.09.007.CrossRefGoogle Scholar
  17. Emery Thompson, M., & Wrangham, R. W. (2006). Comparison of sex differences in gregariousness in fission-fusion species: Reducing bias by standardizing for party size. In N. E. Newton-Fisher, H. Notman, V. Reynolds, & J. Paterson (Eds.), Primates of Western Uganda (pp. 209–226). New York: Springer.CrossRefGoogle Scholar
  18. Emlen, S. T., & Oring, L. W. (1977). Ecology, sexual selection, and the evolution of mating systems. Science, 197, 215–223. doi: 10.1126/science.327542.PubMedCrossRefGoogle Scholar
  19. Engelhardt, A., Hodges, J. K., Niemitz, C., & Heistermann, M. (2005). Female sexual behavior, but not sex skin swelling, reliably indicates the timing of the fertile phase in wild long-tailed macaques (Macaca fascicularis). Hormones and Behavior, 47, 195–204. doi: 10.1016/j.yhbeh.2004.09.007.PubMedCrossRefGoogle Scholar
  20. Engelhardt, A., Pfiefer, J., Heistermann, M., Niemitz, C., van Hooff, J. A., & Hodges, J. K. (2004). Assessment of female reproductive status by male longtailed macaques, Macaca fascicularis, under natural conditions. Animal Behaviour, 67, 915–924. doi: 10.1016/j.anbehav.2003.09.006.CrossRefGoogle Scholar
  21. Gesquiere, L. R., Wango, E. O., Alberts, S. C., & Altmann, J. (2007). Mechanisms of sexual selection: Sexual swellings and estrogen concentrations as fertility indicators and cues for male consort decisions in wild baboons. Hormones and Behavior, 51, 114–125. doi: 10.1016/j.yhbeh.2006.08.010.PubMedCrossRefGoogle Scholar
  22. Goodall, J. (1986). The chimpanzees of Gombe: Patterns of behavior. Cambridge, MA: Belknap Press.Google Scholar
  23. Graham, C. E. (1970). Reproductive physiology of the chimpanzee. In G. H. Bourne (Ed.), The chimpanzee (pp. 183–220). New York: Karger.Google Scholar
  24. Graham, C. E. (1973). Chimpanzee endometrium and sexual swelling during menstrual cycle or hormone administration. Folia Primatologica, 19, 458–468.Google Scholar
  25. Harvey, N., & Harcourt, A. H. (1984). Sperm competition, testes size, and breeding systems in primates. In R. Smith (Ed.), Sperm competition and the evolution of animal mating systems (pp. 589–600). New York: Academic Press.Google Scholar
  26. Hashimoto, C., Furuichi, T., & Tashiro, Y. (2001). What factors affect the size of chimpanzee parties in the Kalinzu Forest, Uganda? Examination of fruit abundance and number of estrous females. International Journal of Primatology, 22, 947–959. doi: 10.1023/A:1012061504420.CrossRefGoogle Scholar
  27. Hrdy, S. B. (1981). The woman that never evolved. Cambridge, UK: Harvard University Press.Google Scholar
  28. Johnson, M. H., & Everitt, B. J. (1988). Essential reproduction. Oxford: Blackwell.Google Scholar
  29. Keverne, E. (1976). Sexual receptivity and attractiveness in the female rhesus monkey. Advances in the Study of Behavior, 7, 155–200. doi: 10.1016/S0065-3454(08)60167-9.CrossRefGoogle Scholar
  30. Martin, D., Graham, C. E., & Gould, K. G. (1978). Successful artificial insemination in the chimpanzee. Symposia of the Zoological Society of London, 43, 249–260.Google Scholar
  31. Matsumoto-Oda, A. (1999). Female choice in the opportunistic mating of wild chimpanzees (Pan troglodytes schweinfurthii) at Mahale. Behavioral Ecology and Sociobiology, 46, 258–266. doi: 10.1007/s002650050618.CrossRefGoogle Scholar
  32. Matsumoto-Oda, A., Oda, R., Hayashi, Y., Murakami, H., Maeda, N., Kumazaki, K., et al. (2002). Vaginal fatty acids produced by chimpanzees during menstrual cycles. Folia Primatologica, 74, 75–79. doi: 10.1159/000070000.CrossRefGoogle Scholar
  33. McArthur, J. W., Beitins, I., Gorman, A., Collins, D. C., Preedy, J., & Graham, C. E. (1981). The interrelationship between sex skin swelling and the urinary excretion of LH, estrone, and pregnanediol by the cycling female chimpanzee. American Journal of Primatology, 1, 265–270. doi: 10.1002/ajp.1350010303.CrossRefGoogle Scholar
  34. Michael, R. P., Bonsall, R., & Warner, P. (1974). Human vaginal secretions: Volatile fatty acid content. Science, 186, 1217–1219. doi: 10.1126/science.186.4170.1217.PubMedCrossRefGoogle Scholar
  35. Michael, R., Bonsall, R., & Zumpe, D. (1976). Chemical communication among primates. Vitamins and Hormones, 34, 137–186. doi: 10.1016/S0083-6729(08)60075-8.PubMedCrossRefGoogle Scholar
  36. Michael, R., Keverne, E., & Bonsall, R. (1971). Pheromones: Isolation of male sex attractants from a female primate. Science, 172, 964–966. doi: 10.1126/science.172.3986.964.PubMedCrossRefGoogle Scholar
  37. Michael, R., & Zumpe, D. (1982). Influence of olfactory signals on the reproductive behaviour of social groups of rhesus monkeys (Macaca mulatta). The Journal of Endocrinology, 95, 189–205.PubMedGoogle Scholar
  38. Mitani, J. C., Watts, D. P., & Lwanga, J. S. (2002). Ecological and social correlates of chimpanzee party size and composition. In C. Boesch, G. Hohmann, & L. F Marchant (Eds.), Behavioural diversity in chimpanzees and bonobos (pp. 102–111). Cambridge, UK: Cambridge University Press.Google Scholar
  39. Muller, M. N. (2002). Agonistic relations among Kanyawara chimpanzees. In C. Boesch, G. Hohmann, & L. F. Marchant (Eds.), Behavioural diversity in chimpanzees and bonobos (pp. 112–124). Cambridge, UK: Cambridge University Press.Google Scholar
  40. Muller, M. N., Emery Thompson, M., & Wrangham, R. W. (2006). Male chimpanzees prefer mating with old females. Current Biology, 16, 2234–2238. doi: 10.1016/j.cub.2006.09.042.PubMedCrossRefGoogle Scholar
  41. Muller, M. N., Kahlenberg, S. M., Emery Thompson, M., & Wrangham, R. W. (2007). Male coercion and the costs of promiscuous mating for female chimpanzees. Proceedings of the Royal Society Series B: Biological Science, 274, 1009–1014. doi: 10.1098/rspb.2006.0206.CrossRefGoogle Scholar
  42. Muller, M. N., & Wrangham, R. W. (2004). Dominance, aggression and testosterone in wild chimpanzees: A test of the ‘challenge hypothesis’. Animal Behaviour, 67, 113–123. doi: 10.1016/j.anbehav.2003.03.013.CrossRefGoogle Scholar
  43. Nadler, R. D., Graham, C. E., Gosselin, R. E., & Collins, D. C. (1985). Serum levels of gonadotropins and gonadal steroids, including testosterone, during the menstrual cycles of the chimpanzee (Pan troglodytes). American Journal of Primatology, 9, 273–284. doi: 10.1002/ajp.1350090404.CrossRefGoogle Scholar
  44. Nishida, T. (1968). The social group of wild chimpanzees in the Mahale mountains. Primates, 19, 167–224. doi: 10.1007/BF01730971.CrossRefGoogle Scholar
  45. Nunn, C. L. (1999). The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Animal Behaviour, 58, 229–246. doi: 10.1006/anbe.1999.1159.PubMedCrossRefGoogle Scholar
  46. Nunn, C. L., van Schaik, C. P., & Zinner, D. (2001). Do exaggerated sexual swellings function in female mating competition in primates? A comparative test of the reliable indicator hypothesis. Behavioral Ecology, 12, 646–654. doi: 10.1093/beheco/12.5.646.CrossRefGoogle Scholar
  47. Ostner, J., Chalise, M. K., Koenig, A., Launhardt, K., Nikolei, J., Podzuweit, D., et al. (2006). What hanuman langur males know about female reproductive status. American Journal of Primatology, 68, 701–712. doi: 10.1002/ajp.20260.PubMedCrossRefGoogle Scholar
  48. Ozasa, H., & Gould, K. G. (1982). Demonstration and characterization of estrogen receptor in chimpanzee sex skin: correlation between nuclear receptor levels and degree of swelling. Endocrinology, 111, 125–131.PubMedGoogle Scholar
  49. Pieta, K. (2008). Female mate preferences among Pan troglodytes schweinfurthii of Kanyawara, Kibale National Park. International Journal of Primatology 29.Google Scholar
  50. Royston, J. (1982). Basal body temperature, ovulation, and the risk of conception, with special reference to the lifetimes of sperm and egg. Biometrics, 38, 397–406.PubMedCrossRefGoogle Scholar
  51. Shimizu, K., Douke, C., Fujita, S., Matsuzawa, T., Tomonaga, M., Tanaka, M., et al. (2003). Urinary steroids, FSH and CG measurements for monitoring the ovarian cycle and pregnancy in the chimpanzee. Journal of Medical Primatology, 32, 15–22. doi: 10.1034/j.1600-0684.2003.01039.x.PubMedCrossRefGoogle Scholar
  52. Steinetz, B. G., Ducrot, C., Randolph, C., & Mahoney, C. (1992). Determination of the time of ovulation in chimpanzees by measurement of LH, estrone sulfate, and pregnanediol 3alpha-glucuronide in urine: comparison with serum hormone patterns. Journal of Medical Primatology, 21, 239–245.PubMedGoogle Scholar
  53. Stumpf, R. M., & Boesch, C. (2005). Does promiscuous mating preclude female choice? Female sexual strategies in chimpanzees (Pan troglodytes verus) of the Tai National Park, Côte d’Ivoire. Behavioral Ecology and Sociobiology, 57, 511–524. doi: 10.1007/s00265-004-0868-4.CrossRefGoogle Scholar
  54. Stumpf, R. M., & Boesch, C. (2006). The efficacy of female choice in chimpanzees of the Taï Forest, Côte d’Ivoire. Behavioral Ecology and Sociobiology, 60, 749–765. doi: 10.1007/s00265-006-0219-8.CrossRefGoogle Scholar
  55. Sugiyama, Y. (1968). Social organization of chimpanzees in the Budongo Forest, Uganda. Primates, 9, 225–258. doi: 10.1007/BF01730972.CrossRefGoogle Scholar
  56. Takasaki, H. (1985). Female life history and mating patterns among the M group chimpanzees of the Mahale National Park, Tanzania. Primates, 26, 121–129. doi: 10.1007/BF02382012.CrossRefGoogle Scholar
  57. Tutin, C. E. (1980). Reproductive behavior of wild chimpanzees in the Gombe National Park, Tanzania. Journal of Reproduction and Fertility. Supplement, 28, 43–57.PubMedGoogle Scholar
  58. Wallis, J. (1997). A survey of reproductive parameters in the free-ranging chimpanzees of Gombe National Park. Journal of Reproduction and Fertility, 109, 297–307. doi: 10.1530/jrf.0.1090297.PubMedCrossRefGoogle Scholar
  59. Watts, D. P. (2007). Effects of male group size, parity, and cycle stage on female chimpanzee copulation rates at Ngogo, Kibale National Park, Uganda. Primates, 48, 222–231. doi: 10.1007/s10329-007-0037-2.PubMedCrossRefGoogle Scholar
  60. Wilcox, A., Weinberg, C., & Baird, D. (1995). Timing of sexual intercourse in relation to ovulation. The New England Journal of Medicine, 333, 1517–1521. doi: 10.1056/NEJM199512073332301.PubMedCrossRefGoogle Scholar
  61. Wilson, M. L. (2001). Imbalances of power: how chimpanzees respond to the threat of intergroup aggression. PhD dissertation, Harvard University, Cambridge, MA.Google Scholar
  62. Wrangham, R. W. (1993). The evolution of sexuality in chimpanzees and bonobos. Human Nature (Hawthorne, N.Y.), 4, 47–79. doi: 10.1007/BF02734089.CrossRefGoogle Scholar
  63. Wrangham, R. W. (2000). Why are male chimpanzees more gregarious than mothers? A scramble competition hypothesis. In P. M. Kappeler (Ed.), Primate males: Causes and consequences of variation in group composition (pp. 248–258). Cambridge, UK: Cambridge University Press.Google Scholar
  64. Wrangham, R. W. (2002). The cost of sexual attraction: Is there a trade-off in female Pan between sex appeal and received coercion? In C. Boesch, G. Hohmann, & L. F. Marchant (Eds.), Behavioural diversity in chimpanzees and bonobos (pp. 204–215). Cambridge, UK: Cambridge University Press.Google Scholar
  65. Wrangham, R. W., Chapman, C. A., Clark-Arcadi, A. P., & Isabirye-Basuta, G. (1996). Social ecology of Kanyawara chimpanzees: Implications for understanding the costs of great ape groups. In W. C. McGrew, L. Marchant, & T. Nishida (Eds.), Great ape societies (pp. 45–57). Cambridge, UK: Cambridge University Press.Google Scholar
  66. Wrangham, R. W., Clark, A., & Isabirye-Basuta, G. (1992). Female social relationships and social organization of Kibale Forest chimpanzees. In T. Nishida, W. C. McGrew, P. Marler, M. Pickford, & F. B. de Waal (Eds.), Topics in primatology, vol I: Human origins (pp. 81–98Tokyo). University of Tokyo Press.Google Scholar
  67. Yerkes, R. M. (1943). Chimpanzees: A laboratory colony p. New Haven. Yale University Press.Google Scholar
  68. Yerkes, R. M., & Elder, J. H. (1937). Concerning reproduction in the chimpanzee. The Yale Journal of Biology and Medicine, 10, 41–48.Google Scholar
  69. Young, W. C., & Yerkes, R. M. (1943). Factors influencing the reproductive cycle in the chimpanzee; The period of adolescent sterility and related problems. Endocrinology, 33, 121–154.CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  1. 1.Department of AnthropologyHarvard UniversityCambridgeUSA
  2. 2.Department of AnthropologyUniversity of New MexicoAlbuquerqueUSA

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