International Journal of Primatology

, Volume 25, Issue 4, pp 901–917

Mating Tactics in Response to Costs Incurred by Mating with Multiple Males in Wild Female Japanese Macaques

  • Miki Matsubara
  • David S. Sprague
Article

Abstract

We investigated the costs of mating with multiple males in terms of feeding time, traveling distances, sexual proceptivity, and male aggression, for wild female (Macaca fuscata yakui) on Yakushima Island, Japan. We analyzed all-day focal sampling data from 7 females during the mating season (Sept.-Nov. 1996). On days when estrous females copulated with multiple males, they decreased their feeding time to half that of anestrous days, traveled longer distances, showed more proceptive sexual behaviors and received more aggression from subordinate males than on days when they copulated with only the 1st-ranking male. On days when females copulated with only the 1st-ranking male, they showed no difference in feeding time with that of anestrous days, and expended less effort than the above mating pattern because of short traveling distances, diminished sexual proceptivity and a lower frequency of aggression received. The results suggest that the costs of estrous vary according to female sexual proceptivity and the number and social status of mating partners. Female Japanese macaques exhibit a mixed mating strategy over prolonged estrous periods, which may provide females with opportunities to maximize the benefits of copulating with multiple males and to minimize the costs of estrus by mating with only the 1st-ranking male. During an estrous cycle, females may be adjusting efforts for reproduction and survival; i.e., mating vs. feeding.

mating with multiple males mating costs mating tactics activity budget traveling distance Japanese macaques 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

REFERENCES

  1. Albert, S. C., Altmann, J., and Wilson, M. L. (1996). Mate guarding constrains foraging activity of male baboons. Anim. Behav. 51: 1269-1277.Google Scholar
  2. Altmann, J. (1974). Observational study of behaviour: Sampling methods. Behaviour 49: 227-265.Google Scholar
  3. Arnqvist, G. (1989). Multiple mating in a water strider: Mutual benefits or intersexual conflict? Anim. Behav. 38: 749-756.Google Scholar
  4. Aujard, F., Heistermann, M., Thierry, B., and Hodges, J. K. (1998). Functional significance of behavioral morphological and endocrine correlates across the ovarian cycle in semifree ranging female Tonkean macaques. Am. J. Primatol. 46: 285-309.Google Scholar
  5. Beach, F. A. (1976). Sexual attractivity proceptivity and receptivity in female mammals. Horm. and Behav. 7: 105-138.Google Scholar
  6. Bercovitch, F. B. (1983). Time budgets and consortships in olive baboons (Papio anubis).Folia Primatol. 41: 180-190.Google Scholar
  7. Bercovitch, F. B. (1987). Female weight and reproductive condition in a population of olive baboons (Papio anubis).Am. J. Primatol. 12: 189-195.Google Scholar
  8. Bercovitch, F. B., Lebron, M. R., Martinez, H. S., and Kessler, M. J. (1998). Primigravidity body weight and costs of rearing first offspring in rhesus macaques. Am. J. Primatol. 46: 135-144.Google Scholar
  9. Bielert, C., and Busse, C. (1983). Influences of ovarian hormones on the food intake and feeding of captive and wild female chacma baboons (Papio ursinus).Physiol. Behav. 30: 103-111.Google Scholar
  10. Brereton, A. R. (1992). Alternative reproductive tactics in stumptail macaques (Macaca arctoides).Folia Primatol. 59: 209-212.Google Scholar
  11. Brereton, A. R. (1994). Return-benefit spite hypothesis: An explanation for sexual interference in stumptail macaques (Macaca arctoides).Primates 35: 123-136.Google Scholar
  12. Bulger, J. B. (1993). Dominance rank and access to estrous females in male savanna baboons. Behaviour 127: 67-103.Google Scholar
  13. Chapman, T., Liddle, L. F., Kalb, J. M., Wolfner, M. F., and Partridge, L. (1995). Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373: 241-244.Google Scholar
  14. Czaja, J. A., and Goy, R. W. (1975). Ovarian hormones and food intake in female guinea pigs and rhesus monkeys. Horm. Behav. 6: 329-349.Google Scholar
  15. Daly, M. (1978). The cost of mating. Am. Nat. 112: 771-774.Google Scholar
  16. Dixson, A. F. (1997). Evolutionary perspectives on primate mating systems and behavior. Ann. N. Y. Acad. Sci. 807: 42-61.Google Scholar
  17. Dixson, A. F. (1998). Primate Sexuality, Oxford University Press, New York.Google Scholar
  18. Dwass, M. (1960). Some k-sample rank-order tests. In Olkin, I. (ed.), Contributions to Probability and Statistics Stanford University Press, California, pp. 198-202.Google Scholar
  19. Enomoto, T. (1974). The sexual behavior of Japanese monkeys. J. Hum. Evol. 3: 351-372.Google Scholar
  20. Enomoto, T. (1979). On the correlation between sexual behavior and ovarian hormone level during the menstrual cycle in captive Japanese monkeys. Primates 20: 563-570.Google Scholar
  21. Fedigan, L. M. (1983). Dominance and reproductive success in primates. Yrbk Phys. Anthropol. 26: 91-129.Google Scholar
  22. Furuichi, T. (1985). Inter-male associations in a wild Japanese macaque troop on Yakushima Island Japan. Primates 26: 219-237.Google Scholar
  23. Furuichi, T. (1987). Sexual swelling receptivity and grouping of wild pygmy chimpanzee females at Wamba Zaire. Primates 28: 309-318.Google Scholar
  24. Hasegawa, T. (1990). Sex differences in ranging patterns. In Nishida, T (ed.), The Chimpanzees of the Mahale Mountains, University of Tokyo Press, Tokyo, pp. 99-114.Google Scholar
  25. Hausfater, G. (1975). Dominance and Reproduction in Baboons (Papio cynocephalus): A Quantitative Analysis, S. Karger, Basel, Switzerland.Google Scholar
  26. Hogg, J. T. (1984). Mating in bighorn sheep: Multiple creative male strategies. Science 225: 526-528.Google Scholar
  27. Hrdy, S. B. (1977). Infanticide as a primate reproductive strategy. Am. Sci. 65: 40-49.Google Scholar
  28. Huffman, M. A. (1987). Consort intrusion and female male choice in Japanese macaques (Macaca fuscata).Ethology 75: 221-234.Google Scholar
  29. Huffman, M. A. (1991). Mate selection and partner preference in female Japanese macaques. In Fedigan, L. M., and Asquith, P. (eds.), The Monkeys of Arashiyama. Thirty-Five Years of Study in the East and West, State University of New York Press, Albany, pp. 101-122.Google Scholar
  30. Huffman, M. A. (1992). Influences of female partner preference on potential reproductive outcome in Japanese macaques. Folia Primatol. 59: 77-88.Google Scholar
  31. Kurland, J. A. (1977). Kin selection in the Japanese monkey. In Szalay, E. S. (ed.), Contributions to Primatology, Vol. 12, S. Karger, New York, pp. 1-145.Google Scholar
  32. Manson, J. H. (1997). Primate consortships. Curr. Anthropol. 38: 353-374.Google Scholar
  33. Maruhashi, T. (1980). Feeding behavior and diet of the Japanese monkeys (Macaca fuscata yakui) on Yakushima Island Japan. Primates 21: 141-160.Google Scholar
  34. Maruhashi, T. (1982). An ecological study of troop fissions of Japanese monkeys (Macaca fuscata yakui) on Yakushima Island Japan. Primates 23: 317-337.Google Scholar
  35. Matsubara, M. (2003). Costs of mate guarding and opportunistic mating among wild male Japanese macaques. Int. J. Primatol. 24: 1057-1075.Google Scholar
  36. Matsumoto-Oda, A., and Oda, R. (1998). Changes in the activity budget of cycling female chimpanzees. Am. J. Primatol. 46: 157-166.Google Scholar
  37. Milton, K. (1985). Mating patterns of wooly spider monkeys Brachyteles arachnoides: Implications for female choice. Behav. Ecol. Sociobiol. 17: 53-59.Google Scholar
  38. Mitsunaga, F., Nozaki, M., Inoue, M., Takenaka, A., Takenaka, O., Sakura, O., Sugiyama, Y., and Ohsawa, H. (1992). Steroid hormones and sexual behavior of female Japanese monkeys in an enclosed group. In Itoigawa, N., Sugiyama, Y., Sackett, G. P., and Thompson, R. K. R. (eds.), Topics in Primatology 2, University of Tokyo Press, Tokyo, pp. 23-34.Google Scholar
  39. Mori, A., Yamaguchi, N., Watanabe, K., Shimizu, K. (1997). Japanese macaques under poor nutritional conditions and food-enhanced perineal swelling in the Koshima troop. Int. J. Primatol. 18: 553-579.Google Scholar
  40. Nunn, C. L. (1999). The evolution of exaggerated sexual swellings in primates and the graded-signal hypothesis. Anim. Behav. 58: 229-246.Google Scholar
  41. Okayasu, N. (1992). Prolonged estrus in female Japanese macaques (Macaca fuscata yakui) and the social influence on estrus: With special reference to male intertroop movement. In Itoigawa, N., Sugiyama, Y., Sackett, G. P., and Thompson, R. K. R. (eds.), Topics in Primatology 2, University of Tokyo Press, Tokyo, pp. 163-178.Google Scholar
  42. Parker, G. A. (1984). Human sperm competition. In Smith, R. L. (ed.), Sperm Competition and the Evolution of Animal Mating Systems, Academic Press, Orlando, Tokyo, pp. 601-659.Google Scholar
  43. Paul, A. (2002). Sexual selection and mate choice. Int. J. Primatol. 23: 877-904.Google Scholar
  44. Reynolds, J. D., and Gross, M. R. (1990). Costs and benefits of female mate choice: Is there a lek paradox? Am. Nat. 136: 230-243.Google Scholar
  45. Saayman, G. S. (1970). The menstrual cycle and sexual behavior in a troop of free ranging Chacma baboons (Papio ursinus).Folia. Primatol. 12: 81-110.Google Scholar
  46. Small, M. F. (1988). Female primate sexual behavior and conception: Are there really sperm to spare? Curr. Anthropol. 29: 81-100.Google Scholar
  47. Smuts, B. B. (1987). Sexual competition and mate choice. In Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W., and Struhsaker, T. T. (eds.), Primate Societies, University of Chicago Press, Chicago, pp. 385-399.Google Scholar
  48. Smuts, B. B., and Smuts, R. W. (1993). Male aggression and sexual coercion of females in nonhuman primates and other mammals: Evidence and theoretical implications. Adv. Stud. Behav. 22: 1-63.Google Scholar
  49. Soltis, J. (1999). Measuring male–female relationships during the mating season in wild Japanese macaques (Macaca fuscata yakui).Primates 40: 453-467.Google Scholar
  50. Soltis, J. (2002). Do primate female gain nonprocreative benefits by mating with multiple males? Theoretical and empirical considerations. Evol. Anthropol. 11: 187-197.Google Scholar
  51. Soltis, J., and McElreath, R. (2001). Can females gain extra paternal investment by mating with multiple males? A game theoretic approach. Am. Nat. 158: 519-529.Google Scholar
  52. Soltis, J., Mitsunaga, F., Shimizu, K., Nozaki, M., Yanagihara, Y., Domingo-Roura, X., and Takenaka, O. (1997a). Sexual selection in Japanese macaques I: Female mate choice and male–male competition. Anim. Behav. 54: 725-736.Google Scholar
  53. Soltis, J., Mitsunaga, F., Shimizu, K., Nozaki, M., Yanagihara, Y., Domingo-Roura, X., and Takenaka, O. (1997b). Sexual selection in Japanese macaques II: Female mate choice and male–male competition. Anim. Behav. 54: 737-746.Google Scholar
  54. Sprague, D. S. (1998). Topographic effects on measures of monkey habitat-use in a mountainous study site in Japan. Am. J. Phys. Anthropol. 26: 207.Google Scholar
  55. Sprague, D. S., Suzuki, S., Takahashi, H., and Sato, S. (1998). Male life history in natural populations of Japanese macaques: Migration, dominance rank, and troop participation of males in two habitats. Primates 39: 351-363.Google Scholar
  56. Steel, R. D. G. (1960). A rank sum test for comparing all pairs of treatments. Technometrics 2: 197-207.Google Scholar
  57. Sugiyama, Y. (1965). On the social charge of hanuman langurs (Presbytis entellus) in their natural condition. Primates 6: 213-247.Google Scholar
  58. Takahata, Y. (1980). The reproductive biology of a free-ranging troop of Japanese monkeys. Primates 21: 303-329.Google Scholar
  59. Takahata, Y., Huffman, M. A., Suzuki, S., Koyama, N., and Yamagiwa, J. (1999). Why dominants do not consistently attain high mating and reproductive success: A review of longitudinal Japanese macaque studies. Primates 40: 143-158.Google Scholar
  60. Tardif, S. D., and Jaquish, C. E. (1994). The common marmoset as a model for nutritional impacts upon reproduction. Ann. N. Y. Acad. Sci. 709: 214-215.Google Scholar
  61. Taub, D. M. (1980). Female choice and mating strategies among wild Barbary macaques (Macaca sylvanus).In Lindburg, D. G. (ed.), The Macaques: Studies in Ecology, Behavior and Evolution, Van Nostrand Reinhold, New York, pp. 287-344.Google Scholar
  62. Taylor, C. R., Schmidt-Nielsen, K., and Raab, J. L. (1970). Scaling of energetic cost of running to body size in mammals. Am. J. Physiol. 219: 1104-1107.Google Scholar
  63. Tutin, C. E. G. (1979). Mating patterns and reproductive strategies in a community of wild chimpanzees (Pan troglodytes schweinfurthii).Behav. Ecol. Sociobiol. 6: 29-38.Google Scholar
  64. van Noordwijk, M. A., and van Schaik, C. P. (2000). Reproductive patterns in eutherian mammals: Adaptations against infanticide? In Schaik, C. P., and Janson, C. H. (eds.), Infanticide by Males and its Consequences, Cambridge University Press, Cambridge, pp. 322-360.Google Scholar
  65. Wada, K., Moriya, K., Hara, K., and Ohsawa, W. (1975). On the body fat of Japanese monkeys inhabiting the Shiga Heights (in Japanese with English summary). Physiol. Ecol. Jpn. 16: 104-107.Google Scholar
  66. Walker, M. L., Gordon, T. P., and Wilson, M. E. (1983). Menstrual cycle characteristics of seasonally breeding rhesus monkeys. Biol. Reprod. 29: 841-848.Google Scholar
  67. Wrangham, R. W. (1979). Sex differences in chimpanzee dispersion. In Hamburg, D. A., and McCown, E. R. (eds.), The Great Apes, Benjamin/Cummings Publication, Menlo Park, CA, pp. 481-489.Google Scholar
  68. Yamagiwa, J. (1985). Socio-sexual factors of troop fission in wild Japanese monkeys (Macaca fuscata yakui) Yakushima Island Japan. Primates 26: 105-120.Google Scholar
  69. Yamagiwa, J., and Hill, D. A. (1998). Intraspecific variation in the social organization of Japanese macaques: Past and present scope of field studies in natural habitats. Primates 39: 257-273.Google Scholar
  70. Yasui, Y. (1998). The ‘genetic benefits’ of female multiple mating reconsidered. Trends Ecol. Evol. 13: 246-250.Google Scholar
  71. Yoshihiro, S., Ohtake, M., Matsubara, H., Zamma, K., Hanya, G., Tanimura, Y., Kubota, H., Kubo, R., Arakane, T., Hirata, T., Furukawa, M., Sato, A., and Takahata, Y. (1999). Vertical distribution of wild Yakushima macaques (Macaca fuscata yakui) in the western area of Yakushima Island Japan: Preliminary report. Primates 40: 409-415.Google Scholar

Copyright information

© Plenum Publishing Corporation 2004

Authors and Affiliations

  • Miki Matsubara
    • 1
  • David S. Sprague
    • 2
  1. 1.Laboratory of Human Evolution Studies, Department of Zoology, Graduate School of ScienceKyoto UniversitySakyo, KyotoJapan
  2. 2.Ecological Management Unit, Ecosystems Group, National Institute for Agro-Environmental SciencesJapan

Personalised recommendations