Biological Exuberance: Animal Homosexuality and Natural Diversity

season). Although marginal males rarely participate in sexual activity (with either males or females), they have occasionally been seen mounting other males.

A “marginal” male Ruff approaches a crouching “satellite” male (above) and then mounts him

Female Ruffs—also known as Reeves—engage in homosexual behavior as well. They often arrive on a lek in groups, and females sometimes mount one another as they begin simultaneously crouching near a resident male during courtship activities. Genital contact may occur, although this is difficult to verify, even for heterosexual (or male homosexual) copulations. Females also occasionally court each other, using some of the same stylized movements such as wing quivering that are seen in heterosexual courtship.

Male Buff-breasted Sandpipers attract other birds to their lek territories with a dramatic WING-UP DISPLAY that can be seen from miles away, in which they raise one wing vertically and flash its brilliant satiny-white underlining. Usually females are attracted to this courtship display, and sometimes up to six of them gather around a displaying male. Often, however, a male from a neighboring territory is drawn to the display as well (or he may “camouflage” himself in a group of females). He may interrupt the courtship when he arrives by mounting the displaying male and trying to copulate with him. He may also aggressively peck the other male on his head and neck while mounted on him, then fly back to his own territory. Sometimes the females follow him, and then the pattern of interruption and mounting is repeated, only this time the other male arrives to disrupt the courtship. This sequence of heterosexual courtship and homosexual mounting may be repeated many times, back and forth for an hour or more. Sometimes, instead of flying back to his own territory with the females, a male simply returns repeatedly to his neighbor’s territory, continuously interrupting the male’s courtship by mounting him. Homosexual mounting also occurs in other contexts: when not as many females are present on the leks (especially later in the mating season), one or more males may enter a neighbor’s territory and simply mount him. As many as four males at a time may participate in such activity.

Frequency: Homosexual mounting occurs regularly in Ruffs, especially at the beginning of the mating season. During one informal three-and-a-half-hour observation period, for example, 3 out of 12 mountings (25 percent) were between males. In Buff-breasted Sandpipers, courtship interruptions by other males are common. Nearly a third of all courtships are disrupted by another male’s arrival, although homosexual mounting does not necessarily take place every time—but then neither does heterosexual mounting, since females usually leave without having copulated (even if there has been no interruption).

Orientation: In Ruffs, homosexual behavior is seen primarily in resident males, who constitute about 40 percent of the male population, and satellite males, who make up roughly 15 percent to one-third of all males (on average). Not all of these individuals engage in same-sex mounting—but neither do they all participate in heterosexual mounting. On some leks, just over half the resident males mate with females—and some only copulate once each season—while 40—90 percent of satellites never mate with females (although they may court them). Of those birds that do participate in homosexual behavior, many alternate between same-sex and opposite-sex interactions and are therefore bisexual. This is also true of females, although some Reeves seem to “prefer” homosexual interactions since they ignore males in favor of mounting other females. Naked-nape males—who probably constitute no more than 10 percent of the male population—rarely, if ever, mate with females. Thus, when naked-napes and nonmating residents and satellites are all taken into account, significant portions of the male Ruff population—perhaps more than half—are involved predominantly, if not exclusively, in sexual activity with other males. This homosexuality may be long-term—satellites, for example, almost never become residents during their entire lives (since these two classes differ genetically). Most male Buff-breasted Sandpipers that mount other males are probably functionally bisexual (if not predominantly heterosexual), since they also court and mate with females.

Nonreproductive and Alternative Heterosexualities

Birds who do not mate or breed are a notable feature of both Ruff and Buff-breasted Sandpiper populations (as noted above). More than 60 percent of male Ruffs, on average, do not copulate with females (this includes males of all categories), while more than half of all territorial Buff-breasted males do not mate (and many males in this species are not territorial and hence probably do not reproduce either). In many cases, males are unable to breed because females select which males they want to mate with and often refuse to allow certain males to copulate with them. However, females of both species occasionally choose more than one male to mate with: almost a quarter of all Buff-breasted nests contain eggs fathered by more than one male, while Reeves have been known to copulate with several different males in a row. Sometimes, more than one male will even try to copulate simultaneously with the same female—usually a resident and a satellite together. Cross-species sexual activity has also been observed: male Ruffs occasionally court and try to mount other sandpipers such as red knots (Calidris canutus).

Courtship and mating are virtually the only times during the entire breeding season when the two sexes are together: in both species, there is significant separation (both physical and temporal) between males and females. After copulating, female Ruffs often leave the lek and migrate farther north to lay their eggs—sometimes more than 1,800 miles away, and two to three weeks after they last mated. It is thought that females are able to do this because they store sperm in special glands in their reproductive tracts, effectively separating fertilization from insemination. Male Buff-breasts take no part in parenting, and in fact depart from the leks well before the eggs hatch. Male Ruffs also generally leave parenting entirely to the females, who occasionally cooperate amongst themselves in tending and defending their young. In fact, chicks may be killed by males if the two sexes ever interact following the hatching of eggs. Infanticide has not been observed in Buff-breasts, although about 10 percent of nests are abandoned by females if a predator takes some of the eggs. Sex segregation also occurs in Ruffs after the breeding season because males and females have different migratory patterns. Females tend to travel farther south to spend the winter, and at some wintering sites in Africa they may outnumber males 15 to 1.

Sources

*asterisked references discuss homosexuality/transgender

Cant, R. G. H. (1961) “Ruff Displaying to Knot.” British Birds 54:205.

*Cramp, S., and K. E. L. Simmons (eds.) (1983) “Ruff (Philomachus pugnax).” In Handbook of the Birds of Europe, the Middle East, and North Africa, vol. 3, pp. 385—402. Oxford: Oxford University Press.

*Hogan-Warburg, A.J. (1993) “Female Choice and the Evolution of Mating Strategies in the Ruff Philomachus pugnax (L.).” Ardea 80:395—403.

*———(1966) “Social Behavior of the Ruff, Philomachus pugnax (L.).” Ardea 54:109—229.

Hugie, D. M., and D. B. Lank (1997) “The Resident’s Dilemma: A Female Choice Model for the Evolution of Alternative Mating Strategies in Lekking Male Ruffs (Philomachus pugnax).” Behavioral Ecology 8:218—25.

*Lanctot, R. B. (1995) “A Closer Look: Buff-breasted Sandpiper.” Birding 27:384- 90.

*Lanctot, R. B., and C. D. Laredo (1994) “Buff-breasted Sandpiper (Tryngites subruficollis).” In A. Poole and F. Gill, eds., The Birds of North America: Life Histories for the 21 st Century, no. 91. Philadelphia: Academy of Natural Sciences; Washington, D.C.: American Ornithologists’ Union.

Lank, D. B., C. M. Smith, O. Hanotte, T. Burke, and F. Cooke (1995) “Genetic Polymorphism for Alternative Mating Behavior in Lekking Male Ruff Philomachus pugnax.” Nature 378:59—62.

*Myers, J. P. (1989) “Making Sense of Sexual Nonsense.” Audubon 91:40—45.

———(1980) “Territoriality and Flocking by Buff-breasted Sandpipers: Variations in Non-breeding Dispersion.”