Archives of Sexual Behavior

, Volume 35, Issue 2, pp 116–128 | Cite as

Male–Female and Female–Female Mounting in Japanese Macaques: A Comparative Study of Posture and Movement

  • Paul L. Vasey
  • Afra Foroud
  • Nadine Duckworth
  • Stefani D. Kovacovsky
Article

Mounting is generally considered to be a male-typical behavior. Female Japanese macaques, in certain populations, are unusual, in that they routinely mount other females. In this study, we examined to what extent female Japanese macaques mount same-sex partners in a male-typical manner. We compared the mount postures males and females adopt and their rate of pelvic thrusting. In addition, we employed a modified form of Laban Movement Analysis (LMA) to compare patterns of pelvic movement during mounts. LMA is a universal language for movement that describes quantitative features of movement, such as changes in the relation of the body segments, as well as qualitative features, such as the style of movements. Our results indicate that female Japanese macaques do not mount in a male-typical manner. Females exhibited a much greater variety of mount postures than did males. Some of the most common types of mount postures employed by females were never exhibited by males. Females performed fewer pelvic thrusts per mount than males, but they executed more pelvic movements per mount, as well as, greater variety and complexity of movement. In addition, the qualitative style of pelvic mounting that females employed differed, in general, from that of males. We argue that these sex differences in mounting can be explained by the fact that both sexes sought sexual reward via genital stimulation during mounting, but they did so in different ways owing to the constraints imposed by their genital architecture. This study raises the larger question as to what constitutes a male-typical or female-typical behavior.

KEY WORDS

macaques mounting sex differences homosexual behavior movement analysis 

Notes

ACKNOWLEDGMENTS

We are extremely thankful to the following individuals, without whom, this research would not have been possible: Shigeru Suzuki, Shinsuke Asaba, Michael Huffman, Juichi Yamagiwa, Mr. Kowbatake, Mr. Inoue, the Enomoto family of Arashiyama, and the Sakami family of Tokyo. We also thank theKenneth Zuckerand three anonymous referees. This research was funded by grants to P.L.V. by the University of Lethbridge, the L.S.B. Leakey Foundation, the Natural Science and Engineering Research Council (NSERC) of Canada, by a NSERC Undergraduate Award to N.D., and by a Mount Holyoke College Bardwell Fellowship and Biology Post-Graduate Fellowship to S.D.K.

REFERENCES

  1. Adkins-Regan, E. (1988). Sex hormones and sexual orientation in animals. Psychobiology, 16, 335–347.Google Scholar
  2. Adkins-Regan, E. (1998). Hormonal mechanisms of mate choice. American Zoologist, 38, 166–178.Google Scholar
  3. Adkins-Regan, E., Mansukhani, V., Thompson, R., & Yang, S. (1997). Organizational actions of sex hormones on sexual partner preference. Brain Research Bulletin, 44, 497–502.PubMedCrossRefGoogle Scholar
  4. Altmann, J. (1974). Observational studies of behavior: Sampling methods. Behaviour, 49, 227–265.PubMedCrossRefGoogle Scholar
  5. Aou, S., Oomura, Y., & Yoshimatsu, H. (1988). Neuron activity of the ventromedial hypothalamus and the medial preoptic area of the female monkey during sexual behavior. Brain Research, 455, 65–71.PubMedCrossRefGoogle Scholar
  6. Bagemihl, B. (1999). Biological exuberance: Animal homosexual and natural diversity. New York: St. Martin's.Google Scholar
  7. Barternieff, I., & Lewis, D. (1980). Body movement: Coping with the environment. Langhorne, PA: Gordon & Breach Science.Google Scholar
  8. Baum, M. J. (1979). Differentiation of coital behavior in mammals. Neuroscience and Biobehavior Reviews, 3, 65–84.Google Scholar
  9. Beach, F. A. (1968). Factors involved in the control of mounting behavior by female mammals. In M. Diamond (Ed.), Perspectives in reproduction and sexual behavior (pp. 83–131). Bloomington: Indiana University Press.Google Scholar
  10. Chapais, B. (1992). The role of alliances in the social inheritance of rank among female primates. In A. Harcourt & F. M. B. de Waal (Eds.), Coalitions and alliances in humans and other animals (pp. 29–60). Oxford: Oxford University Press.Google Scholar
  11. Chapais, B., Gauthier, C., Prud'homme, J., & Vasey, P. L. (1997). Relatedness threshold for nepotism in Japanese macaques. Animal Behaviour, 53, 533–548.CrossRefGoogle Scholar
  12. Chapais, B., & Mignault, C. (1991). Homosexual incest avoidance among females in captive Japanese macaques. American Journal of Primatology, 23, 171–183.CrossRefGoogle Scholar
  13. Dixson, A. F. (1998). Primate sexuality: Comparative studies of prosimians, monkeys, apes and human beings. Oxford: Oxford University Press.Google Scholar
  14. Eaton, G. G., Glick, B. B., Worlein, J. M., & Martin, T. L. (1987). Sexual behavior at puberty in prenatally androgenized female Japanese macaques. American Journal of Primatology, 12, 340.Google Scholar
  15. Eaton, G. G., Goy, R. W., & Phoenix, C. H. (1973). Effects of testosterone treatment in adulthood on sexual behavior of female pseudohermaphrodite rhesus monkeys. Nature New Biology, 242, 119–120.PubMedCrossRefGoogle Scholar
  16. Eaton, G. G., Worlein, J. M., Martin, T. L., & Glick, B. B. (1988). Sexual behavior of prenatally androgenized female and estrogen treated male Japanese macaques (Macaca fuscata). American Journal of Primatology, 14, 419.Google Scholar
  17. Ellis, L., & Ames, M. A. (1987). Neurohormonal functioning and sexual orientation: A theory of homosexuality–heterosexuality. Psychological Bulletin, 101, 233–258.PubMedCrossRefGoogle Scholar
  18. Fagen, R., Conitz, J., & Kunibe, E. (2000). Observing behavioral qualities. International Journal of Comparative Psychology, 10, 167–179.Google Scholar
  19. Fedigan, L. M., & Gouzoules, H. (1978). The consort relationship in a troop of Japanese monkeys. In D. J. Chivers & J. Herbert (Eds.), Recent advances in primatology, Vol. 1: Behavior (pp. 493–495). New York: Academic.Google Scholar
  20. Fischer, R. B., & Nadler, R. D. (1978). Affiliative, playful, and homosexual interactions of adult female lowland gorillas. Primates, 19, 657–664.CrossRefGoogle Scholar
  21. Foroud, A., & Pellis, S. M. (2003). The development of “roughness” in the play fighting of rats: A Laban Movement Analysis perspective. Developmental Psychobiology, 42, 35–43.PubMedCrossRefGoogle Scholar
  22. Foroud, A., Whishaw, I. Q., & Pellis, S. M. (2004). Experience and cortical control over the pubertal transition to rougher play fighting in rats. Behavioral Brain Research, 149, 69–76.CrossRefGoogle Scholar
  23. Gouzoules, H., & Goy, R. W. (1983). Physiological and social influences on mounting behavior of troop-living female monkeys (Macaca fuscata). American Journal of Primatology, 5, 39–49.CrossRefGoogle Scholar
  24. Huffman, M. A. (1991). History of the Arashiyama Japanese macaques in Kyoto, Japan. In L. M. Fedigan & P. J. Asquith (Eds.), The monkeys of Arashiyama: Thirty-five years of research in Japan and the West (pp. 21–53). Albany: SUNY Press.Google Scholar
  25. Hunt, G. L., Newman, A. L., Warner, M. H., Wingfield, J. C., & Kaiwi, J. (1984). Comparative behavior of male–female and female–female pairs among western gulls prior to egg-laying. Condor, 86, 157–162.CrossRefGoogle Scholar
  26. Hutchins, M. (1984). The mother–offspring relationship in mountain goats (Oreamnos americanus). Unpublished doctoral dissertation, University of Washington.Google Scholar
  27. Hutchinson, A. (1977). Labanotation: The system of analyzing and recording movement (3rd ed.). New York: Theatre Arts Books.Google Scholar
  28. Kendrick, K. M., & Dixson, A. F. (1986). Anteromedial hypothalamic lesions block proceptivity but not receptivity in the female common marmoset (Callithrix jacchus). Brain Research, 375, 221–229.PubMedCrossRefGoogle Scholar
  29. Koyama, N. (1991). Grooming relationships in the Arashiyama group of Japanese monkeys. In L. M. Fedigan & P. J. Asquith (Eds.), The monkeys of Arashiyama: Thirty-five years of research in Japan and the West (pp. 211–226). Albany: SUNY Press.Google Scholar
  30. Koyama, Y., Fujita, I., Aou, S., & Oomura, Y. (1988). Proceptive presenting elicited by electrical stimulation of the female monkey hypothalamus. Brain Research, 446, 199–203.PubMedCrossRefGoogle Scholar
  31. Kurland, J. A. (1977). Kin selection in the Japanese monkey. Basel: Karger.Google Scholar
  32. Laban, R. (1971). In L. Ullman (Ed.), The mastery of movement (Rev. 3rd ed.). Boston: Plays.Google Scholar
  33. MacDonald, D. W. (1987). Running with the fox. New York: Facts on File.Google Scholar
  34. Maletic, V. (1987). Body, space, expression: The development of Rudolf Laban's movement and dance concepts. New York: Mouton de Gnoyter.Google Scholar
  35. Oomura, Y., Aou, S., Koyama, Y., Fujita, I., & Yoshimatsu, H. (1988). Central control of sexual behavior. Brain Research Bulletin, 20, 863–870.PubMedCrossRefGoogle Scholar
  36. Parker, G. A., & Pearson, R. G. (1976). A possible origin and adaptive significance of mounting behavior shown by some female mammals in oestrous. Journal of Natural History, 10, 241–245.CrossRefGoogle Scholar
  37. Phoenix, C. H., & Chambers, K. C. (1982). Sexual behavior in adult gonadectomized female pseudohermaphrodite, female, and male rhesus macaques (Macaca mulatta) treated with estradiol benzoate and testosterone propionate. Journal of Comparative Physiological Psychology, 96, 823–833.CrossRefGoogle Scholar
  38. Phoenix, C. H., Goy, R. W., Gerall, A. A., & Young, W. C. (1959). Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology, 65, 369–382.PubMedCrossRefGoogle Scholar
  39. Pomerantz, S. M., Goy, R. W., & Roy, M. M. (1986). Expression of male-typical behavior in adult female pseudohermaphroditic rhesus: Comparisons with normal males and neonatally gonadectomized males and females. Hormones and Behavior, 20, 483–500.PubMedCrossRefGoogle Scholar
  40. Takahata, Y. (1982). The sociosexual behavior of Japanese macaques. Zeitschrift für Tierpsychologie, 59, 89–108.PubMedCrossRefGoogle Scholar
  41. Vasey, P. L. (1995). Homosexual behavior in primates: A review of evidence and theory. International Journal of Primatology, 16, 173–204.CrossRefGoogle Scholar
  42. Vasey, P. L. (1996). Interventions and alliance formation between female Japanese macaques, Macaca fuscata, during homosexual consortships. Animal Behaviour, 52, 539–551.CrossRefGoogle Scholar
  43. Vasey, P. L. (1998). Female choice and inter-sexual competition for female sexual partners in Japanese macaques. Behaviour, 135, 579–597.Google Scholar
  44. Vasey, P. L. (2002a). Sexual partner preference in female Japanese macaques. Archives of Sexual Behavior, 31, 45–56.CrossRefGoogle Scholar
  45. Vasey, P. L. (2002b). Same-sex sexual partner preference in hormonally and neurologically unmanipulated animals. Annual Review of Sex Research, 13, 141–179.PubMedGoogle Scholar
  46. Vasey, P. L. (2004a). Homosexual behavior. In B. Thierry, M. Singh, & W. Kaumanns (Eds.), Macaque societies: A model for the study of social organization (pp. 151–154). Cambridge, UK: Cambridge University Press.Google Scholar
  47. Vasey, P. L. (2004b). Pre- and post-conflict interactions among female Japanese macaques during homosexual consortships. International Journal of Comparative Psychology, 17, 351–359.Google Scholar
  48. Vasey, P. L. (2004c). Sex differences in sexual partner acquisition, retention and harassment during female homosexual consortships in Japanese macaques. American Journal of Primatology, 64, 397–409.PubMedCrossRefGoogle Scholar
  49. Vasey, P. L., Chapais, B., & Gauthier, C. (1998). Mounting interactions between female Japanese macaques: Testing the influence of dominance and aggression. Ethology, 104, 387–398.CrossRefGoogle Scholar
  50. Vasey, P. L., & Duckworth, N. (in preparation). Sexual reward via vulvar and perineal stimulation as a proximate mechanism for female–female mounting in Japanese macaques.Google Scholar
  51. Vasey, P. L., & Gauthier, C. (2000). Skewed sex ratios and female homosexual activity in Japanese macaques: An experimental analysis. Primates, 41, 17–25.CrossRefGoogle Scholar
  52. Vasey, P. L., & Pfaus, J. G. (2005). A sexually dimorphic hypothalamic nucleus in a macaque species with frequent female–female mounting and same-sex sexual partner preference. Behavioral Brain Research, 157, 265–272.CrossRefGoogle Scholar
  53. Wallen, K., & Parson, W. A. (1997). Sexual behavior in same-sexed nonhuman primates: Is it relevant to understanding human homosexuality? Annual Review of Sex Research, 7, 195– 225.Google Scholar
  54. Whishaw, I. Q., Gorny, B., Foroud, A., & Kleim, J. (2003). Long–Evans and Sprague–Dawley rats have similar skilled reaching success and topographic limb representations in motor cortex but use different movements as assessed by EWMN and Laban Movement Analysis. Behavioral Brain Research, 145, 221–232.CrossRefGoogle Scholar
  55. Wickler, W. (1967). Socio-sexual signals and their intra-specific imitation among primates. In D. Morris (Ed.), Primate ethology (pp. 69–147). London: Weidenfield & Nicolson.Google Scholar
  56. Wolfe, L. D. (1979). Behavioral patterns of estrous females of the Arashiyama West troop of Japanese macaques (Macaca fuscata). Primates, 20, 525–534.CrossRefGoogle Scholar
  57. Wolfe, L. D. (1984). Japanese macaque female sexual behavior: A comparison of Arashiyama East and West. In M. F. Small (Ed.), Female primates: Studies by women primatologists (pp. 141–157). New York: Alan R. Liss.Google Scholar
  58. Yamagiwa, J., & Hill, D. A. (1998). Intraspecific variation in social organization of Japanese macaques: Past and present scope of field studies in natural habitats. Primates, 39, 257– 274.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Paul L. Vasey
    • 1
  • Afra Foroud
    • 1
  • Nadine Duckworth
    • 1
  • Stefani D. Kovacovsky
    • 2
  1. 1.Department of Psychology and NeuroscienceUniversity of LethbridgeLethbridgeCanada
  2. 2.Neuroscience and Behavior ProgramMount Holyoke CollegeSouth HadleyUSA

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