Biological Exuberance: Animal Homosexuality and Natural Diversity

Condor 82:426—29.

*Shugart, G. W., M. A. Fitch, and G. A. Fox (1988) “Female Pairing: A Reproductive Strategy for Herring Gulls?” Condor 90:933—35.

*———(1987) “Female Floaters and Nonbreeding Secondary Females in Herring Gulls.” Condor 89:902—6.

Tasker, C. R., and J. A. Mills (1981) “A Functional Analysis of Courtship Feeding in the Red-billed Gull, Larus novaehollandiae scopulinus.” Behavior 77:221—41.

Wheeler, W. R., and 1. Watson (1963) “The Silver Gull Larus novaehollandiae Stephens.” Emu 63:99—173.

IDENTIFICATION: A medium-sized gull (to 17 inches) with a distinctive black or chocolate brown “hood,” red legs, and a gray back and wings. DISTRIBUTION: Throughout most of Eurasia; winters south to Africa and southern Asia. HABITAT: Variable, including lakes, swamps, rivers, grassland, coasts, bays. STUDY AREAS: Kiyovo Lake near Moscow, Russia; University of Groningen, the Netherlands.

Social Organization

Black-headed Gulls are gregarious, gathering in large flocks throughout most of the year. They form pair- bonds and nest in dense colonies containing up to several thousand pairs.

Description

Behavioral Expression: Male homosexual pairs are found in Black-headed Gulls, and they are usually initiated with the same courtship behaviors seen in heterosexual pairs. At the beginning of the mating season, one male lands on the territory of another male who is performing an ADVERTISEMENT DISPLAY, consisting of a series of loud, rasping screams sounding like kreeeee kreeeee … (the LONG CALL). This is made while the bird assumes an OBLIQUE-POSTURE (head extended forward and upward with the bill horizontal). The displaying male may also approach the other male in the FORWARD-POSTURE, in which the head is lowered and held level with the rest of the body, neck kinked, and tail spread. Over the next several weeks, as their pair-bond develops, the two males perform frequent MEETING CEREMONIES, stylized courtship interactions that include many of the same movements seen in the advertisement display, combined with HEAD-FLAGGING, in which the two birds alternately turn their heads toward and away from their partner. The two birds sometimes also perform COURTSHIP-FEEDING, in which one male ritually begs the other for food, who may respond by regurgitating a ceremonial food “offering” for his mate. Males in homosexual pairs generally perform meeting ceremonies more frequently than birds in heterosexual pairs; their long-calling and head-flagging rates are intermediate between those of males and females in heterosexual pairs, while they generally beg and courtship-feed less than either males or females in opposite-sex pairs.

Once their pair-bond is established, male partners may also engage in sexual behavior. This can involve one male simply mounting the other, but in other cases it consists of full copulation with repeated genital contacts between the two males. In some homosexual couples, both males take turns mounting each other, although in most instances only one partner is the mounter and the other is the mountee. Male couples usually build a nest together, with both birds contributing to its construction. Occasionally the nest is built entirely by one partner (as in heterosexual pairs, where usually only the male builds the nest). Most homosexual pairs are unable to obtain eggs, although it is possible that some may “adopt” eggs abandoned by heterosexual pairs. In addition, females in this species occasionally lay eggs in other birds’ nests, so male pairs could acquire eggs in this way as well. When provided with “foster eggs” in captivity, homosexual pairs faithfully incubate and hatch them and in some cases even successfully raise the chicks together.

In addition to monogamous homosexual pairs, several other variations of same-sex bonding occur. About 25 percent of males in homosexual associations are polygamous (comparable to rates for males in heterosexual associations). Such males form trios, bonding either with two males, or with one male and one female (in one case, a same-sex trio later developed into a bisexual “quartet” when a female joined them). Some male couples are nonmonogamous, in that one or both partners court and even copulate with outside partners of either sex. Homosexual pairings are generally not as long-lasting as heterosexual ones: an average of 15 percent of same-sex bonds last for at least two consecutive seasons, compared to 56 percent of heterosexual bonds. Nevertheless, many homosexual bonds are strong, and partners will maintain their attachment to their mate even if they are forcibly separated from one another, resuming their partnership once reunited. Males also frequently engage in serial pairing, forming bonds with three to four different partners over time (both males and females). Sometimes, the permutations of all these different possibilities can be dizzying—in one case, a male who had been in a homosexual couple later paired with a female, during which time he engaged in promiscuous, “incestuous” courtship and mating with a heterosexually paired female that he had previously foster-parented with his male partner!

In addition to a pattern of homosexual pair-bonding, male Black-headed Gulls in heterosexual pairs sometimes copulate with birds other than their mate, including other males. These nonmonogamous copulations are usually “forced” in the sense that the mounted bird does not solicit the sexual activity and usually vigorously pecks at the male and drives him away. Often a promiscuous male will hover over another male, trying unsuccessfully to mount, although in some cases a male may be able to mount and remain on the other male for as long as five minutes (albeit without any genital contact taking place). Sometimes a promiscuous mounting leads to a same-sex pair-bond: one heterosexually paired bird who mounted both partners of a heterosexual couple, for example, formed a homosexual bond the next year with the male partner of that couple.

Frequency: Male couples that court, mate, and nest together have been documented in wild populations, although their overall incidence is not known. In captivity, homosexual pairs can account for 16—18 percent of all bonds, while two out of 9 promiscuous mountings (22 percent) in one study were homosexual. At the height of courtship, individual males in homosexual pairs may perform displays such as ceremonial encounters or long-calling as often as 40—60 or more times an hour.

Orientation: In a study of Black-headed Gulls in captivity, 22 percent of the males formed bonds only with other males, 15 percent formed bonds with both males and females, while 63 percent bonded only with members of the opposite sex. In addition, layered on top of these patterns of pair-bonding are instances of nonmonogamous, bisexual courtship and sexual activity—often same-sex for heterosexually paired birds, and opposite-sex for homosexually paired birds. Furthermore, younger males appear to have a preference for homosexual pairing that declines somewhat as the birds get older: 55—60 percent of bonds are same-sex among one-to-two-year-olds, compared to 30—45 percent in two-to-five-year-olds, and 20 percent in five-to-eight-year-olds. In addition, many males may have a “latent” capacity for bisexuality, being able to form same-sex bonds when females are not available.

Nonreproductive and Alternative Heterosexualities

Most of the variations on long-term, monogamous pair-bonds seen in homosexual contexts also occur in heterosexual associations among Black-headed Gulls. Promiscuous courtships and copulations can be entirely heterosexual: some females court males other than their mate, while males may try to rape females they aren’t paired with (within-pair copulations are also sometimes accompanied by aggression or unwillingness between partners). As noted above, divorce (changing of partners between breeding seasons) occurs fairly frequently in opposite-sex pairs. In addition, mate-switching within the breeding season is quite common—more than half of all males form brief liaisons with females that last a few days, mating with up to seven different partners. Polygamous trios also occur in this species: occasionally, a female will join a mated pair, bond with the male, and help them raise their young, although she herself does not breed. Some females lay eggs in the territories of other heterosexual couples, who may then adopt those eggs as their own; adoption of chicks also occurs. A number of nonreproductive sexual behaviors are also characteristic of this species. Heterosexual mounting often does not involve mutual genital contact, females sometimes mount males (REVERSE mounts), and heterosexual pairs