Biological Exuberance: Animal Homosexuality and Natural Diversity

between males, and sitting or lying on the partner’s back is rarely if ever used. Young males often make a distinctive purring or churring sound deep in the throat while mounting each other; this vocalization is not heard in heterosexual contexts. Sexual activity between males differs from male-female behavior in a number of other ways: homosexual mounting is more common outside or toward the end of the breeding season, while heterosexual mounts are more frequently interrupted by other individuals than mounts between males.

Frequency: The prevalence of homosexual activity in Japanese Macaques varies greatly between different troops, although it can be found to some degree in virtually every population. In some cases, more than a quarter of all consortships are between females and up to a third or more of all mounting episodes are homosexual; five to ten mounts between males may occur each morning in some troops. In other troops, same-sex behavior is much less frequent.

Orientation: Again, the proportion of the female population participating in homosexual activity is highly variable, ranging from 12–78 percent, averaging 43 percent (in semiwild troops). In some troops, all females that participate in same-sex consortships are bisexual, also consorting with males; however, while paired with a female they remain faithful to their partner, ignoring or rebuffing any advances made by males toward them. In other troops, though, some females are exclusively lesbian, engaging in sexual interactions only with females: in these cases, an average of 9 percent of females are homosexual, 56 percent bisexual, and 35 percent exclusively heterosexual. Among males, there is a similar variation in the proportion of individuals participating in homosexual mounting, from as low as 0–15 percent, to virtually all the males in a troop. Generally, though, males that engage in same-sex activity also participate in opposite-sex mounting. Interestingly, some of the most intense homosexual activity, involving complete mounts with ejaculation, is exhibited by males who are also the most active heterosexually.

Nonreproductive and Alternative Heterosexualities

Nonprocreative heterosexual activities are a prominent feature of Japanese Macaque life. In some populations, as many as three-quarters of all females actively seek sexual interactions while they are pregnant, half do so while menstruating, and individual females may copulate with an average of ten different males during the mating season. Most heterosexual mounts (nearly two-thirds) do not lead to ejaculation. In addition, REVERSE mounting is common, in which a female climbs on top of a male and rubs her genitals on his back. In some troops, about 40 percent of all females engage in this behavior and it occurs in about a third of all heterosexual interactions. Masturbation is also common in both males and females. Females in some troops frequently form consortships with sexually immature (preadolescent) males; as noted above, incestuous pairings also sometimes occur, and up to 15 percent of heterosexual mountings may be between related individuals.

Heterosexual mating occurs year round, but rarely leads to pregnancy when it takes place outside of the breeding season. Nor are females unique in experiencing a sexual cycle with distinct nonreproductive periods: males undergo a yearly seasonal fluctuation in their hormone levels that results in retraction of their testicles, cessation of ejaculation, and loss of color in their sexual skin during the nonmating season. In addition, approximately 10 percent of Japanese Macaques in some troops form nonbreeding or celibate heterosexual pairs: the partners specifically avoid sexual activities with each other, although they may interact sexually with other individuals. Many females also experience a long postreproductive period later in their lives, generally lasting four to five years and constituting about 16 percent of the average life span. Such individuals continue to be sexually active, copulating with males at rates comparable to those of breeding females and also interacting with the same number of female sexual partners as do younger females.

In some troops, a unique form of “baby-sitting” has developed. Although males in this species do not typically participate in parenting, high-ranking males in some populations take care of infants that are not their own for short periods. They groom, carry, embrace, and protect the infants, usually with the consent of their mothers. A few females also act as baby-sitters; however, nonbreeding females have also been known to kidnap infants, sometimes keeping them permanently. In addition, a few male caretakers interact sexually with infants (usually females), masturbating themselves while carrying them or even thrusting against them.

Sources

*asterisked references discuss homosexuality/transgender

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*Chapais, B., and C. Mignault (1991) “Homosexual Incest Avoidance Among Females in Captive Japanese Macaques.” American Journal of Primatology 23:171–83.

*Corradino, C. (1990) “Proximity Structure in a Captive Colony of Japanese Monkeys (Macaca fuscata fuscata): An Application of Multidimensional Scaling.” Primates 31:351–62.

*Eaton, G. G. (1978) “Longitudinal Studies of Sexual Behavior in the Oregon Troop of Japanese Macaques.” In T. E. McGill, D. A. Dewsbury, and B. D. Sachs, eds., Sex and Behavior: Status and Prospectus, pp. 35–59. New York: Plenum Press.

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*Fedigan, L. M., and H. Gouzoules (1978) “The Consort Relationship in a Troop of Japanese Monkeys.” In D. Chivers, ed., Recent Advances in Primatology, vol. 1: pp. 493–95. London: Academic Press.

*Gouzoules, H., and R. W. Goy (1983) “Physiological and Social Influences on Mounting Behavior of Troop- Living Female Monkeys (Macaca fuscata).” American Journal of Primatology 5:39–49.

*Green, S. (1975) “Variation of Vocal Pattern with Social Situation in the Japanese Monkey (Macaca fuscata): A Field Study.” In L. A. Rosenblum, ed., Primate Behavior: Developments in Field and Laboratory Research, vol. 4, pp. 1–102. New York: Academic Press.

*Hanby, J. P. (1974) “Male-Male Mounting in Japanese Monkeys (Macaca fuscata).” Animal Behavior 22:836–49.

*Hanby, J. P., and C. E. Brown (1974) “The Development of Sociosexual Behaviors in Japanese Macaques Macaca fuscata.” Behavior 49:152–96.

*Hanby, J. P., L. T. Robertson, and C. H. Phoenix (1971) “The Sexual Behavior of a Confined Troop of Japanese Macaques.” Folia Primatologica 16:123–43.

Itani, J. (1959) “Paternal Care in the Wild Japanese Monkey, Macaca fuscata fuscata.” Primates 2:61–93.

*Lunardini, A. (1989) “Social Organization in a Confined Group of Japanese Macaques (Macaca fuscata). An Application of Correspondence Analysis.” Primates 30:175–85.

*Rendall, D., and L. L. Taylor (1991) “Female Sexual Behavior in the Absence of Male-Male Competition in Captive Japanese Macaques (Macaca fuscata).” Zoo Biology 10:319–28.

*Sugiyama, Y. (1960) “On the Division of a Natural Troop of Japanese Monkeys at Takasakiyama.” Primates 2:109–48.

*Takahata, Y. (1982) “The Socio-sexual Behavior of Japanese Monkeys.” Zeitschrift fur Tierpsychologie 59:89–108.

*———(1980) “The Reproductive Biology of a Free-Ranging Troop of Japanese Monkeys.” Primates 21:303–29.

Takahata, Y., N. Koyama, and S. Suzuki (1995) “Do the Old Aged Females Experience a Long Postreproductive Life Span?: The Cases of Japanese Macaques and Chimpanzees.” Primates 36:169–80.