Biological Exuberance: Animal Homosexuality and Natural Diversity

portion of the “surplus” individuals form same-sex bonds include Flamingos, Laughing Gulls, Humboldt Penguins, Gentoo Penguins, Pied Kingfishers, Peach-faced Lovebirds, Galahs, and Bicolored Antbirds.⁴⁷

Although homosexual involvements in such species may be the “result” of skewed sex ratios, any “explanation” of homosexuality that relies on this factor alone needs to address why only some individuals “choose” this strategy, and why this strategy rather than another. For in addition to remaining single or forming same-sex pair-bonds, a wide variety of other behavioral responses occur among animals in populations that have a surplus of one sex, or in situations where the opposite sex is “unavailable.” For example, in many otherwise monogamous species that have more females than males (or vice versa), some individuals form polygamous heterosexual trios (so-called “bigamy”) or even quartets (“trigamy”). These options occur alongside homosexual pairings in Flamingos and Humboldt Penguins, and instead of same-sex pairing in Cattle Egrets, emperor penguins, and dippers (among many others). Individuals in the same population may also adopt different strategies or combine these strategies, to varying degrees: in Oystercatcher communities, for instance, with large surpluses of nonbreeding birds unable to find heterosexual mates or breeding territories of their own, only a small fraction of these birds form polygamous trios (most remain unmated); and only a portion of these in turn go on to develop homosexual bonds within their trio. Australian noisy miners (a bird species with a heavily male-biased sex ratio) have developed a complex, specieswide system of communal breeding that involves, among other arrangements, polyandry (several males associating with each female, without any same-sex bonding). The reverse situation occurs in spotted sandpipers, in which “surplus” birds actually participate in monogamy rather than polygamy. In this species, females usually mate with several males and generally leave the parenting duties to them; females unable to find polygamous mates, however, often “revert” to monogamous (heterosexual) pairing and parenting, helping one male partner with incubation and brooding.⁴⁸

Polygamy is just the tip of the iceberg as far as alternate strategies are concerned. Surplus female Redshanks participate in promiscuous matings with already paired males rather than forming bonds involving other females; “extra” male mustached warblers help already established pairs raise their families; while surplus female Ostriches and Greater Rheas lay their eggs in other females’ nests or abandon them rather than forming bonds with either males or females. Female Tree Swallows, male tropical house wrens, and male barn swallows unable to find mates of their own often invade the nests of existing heterosexual pairs and forcibly acquire a partner (either through direct attack and eviction of the other mate, or by killing their young and causing the pair’s breakup). In some species of Penguins and Egrets, individuals form temporary or serial heterosexual pair-bonds or divorce their partners more often in response to a surplus of one sex. In Black Stilt populations with a surplus of one sex, birds regularly seek heterosexual partners outside their species (hybridizing with the closely related Black-winged Stilt), while female Silver and Herring Gulls in some colonies with a “shortage” of adult males often simply pair with much younger males. A common response of male African Elephants that are sexually aroused but unable to find receptive female partners is simply to roll in mud wallows or take dust baths (thereby perhaps “diffusing” their arousal), rather than engaging in any sexual behavior (with either males or females). In all of these species, homosexual activity (if it occurs at all) is simply one “option” that some individuals adopt alongside many other alternatives.⁴⁹

A shortage explanation cannot adequately account for the occurrence of such multiple strategies, or for the choice of one over the other. By claiming that animals “resort” to homosexuality in times of need, scientists often overlook other more plausible (heterosexual) alternatives—unintentionally providing support for the idea that homosexuality may actually be the most appealing option for some individuals in these circumstances. For example, homosexual activity in White-handed Gibbons has been attributed to the unavailability (or unwillingness) of a male’s female partner to have sex with him. But why don’t such males seek heterosexual matings outside of their pair- bond or simply masturbate (strategies that both occur in other contexts for this species)? Likewise, homosexual courtships in Ostriches are claimed—in a particularly convoluted sequence of logic—to result from a balanced sex ratio in some populations. Because Ostriches often mate polygamously— one male with several females—a population that has equal numbers of males and females would supposedly be unable to support such multiple matings. One scientist suggested that in this case males turn to their own sex—but why would this occur instead of males simply remaining in monogamous heterosexual pairings (as do spotted sandpipers)? Some same-sex mountings in Buff-breasted Sandpipers are said to result from the scarcity of females late in the breeding season. But once females stop visiting the breeding territories at this time, males often move their courtship displays to where the females are (at their nests) and may even copulate with them during the egg- laying period. Why would some males “resort” to relocating their heterosexual activities, while others would “abandon” them for homosexual activities?⁵⁰ Even if same-sex activity in these species could be attributed to the unavailability of the opposite sex, important questions such as these remain unaddressed under a shortage explanation. On the other hand, if participation in homosexuality is seen as the expression of individual variability and plasticity in sexual orientation—rather than as being “caused” or “determined” by a shortage of the opposite sex—then the variety of sexual responses and capacities actually seen in such circumstances is no longer incongruous.

Deprived of Heterosexuality?

One particularly common version of the shortage explanation is that males turn to homosexuality after being prevented from mating with females, due to the active interference or inhibiting presence of higher-ranking males. This is often suggested for mammals with polygamous or promiscuous mating systems in which only relatively few males ever get to mate heterosexually. While this may contribute to same-sex activity in some species (e.g., Mountain Sheep, Northern Elephant Seals), there is considerable evidence that this explanation is overly simplistic. Homosexual mounting in American Bison, for instance, is especially common among younger males that do not breed (ages one to six), but this cannot be attributed solely to their being “denied” access to females by older, higher-ranking males. Same-sex activity is much less common among bulls four to six years old than it is in males one to three years old, even though both groups are “prevented” (or abstain) from engaging in breeding activities. Also, studies of populations in which older bulls have been removed (in order to give younger males more “access” to females) show that although heterosexual activity increases among the younger bulls in the absence of the higher-ranking males, so does homosexual activity. In fact, more than 55 percent of mounts in such groups are still between males even though there are no older bulls to “prevent” the males from mating heterosexually (and even though females outnumbered males in such populations). Likewise, as they are growing up, male Bonobos experience a sharp drop in their access to heterosexual partners that is not reflected in a corresponding increase in their homosexual activity. As infants and juveniles they are very sexually active with mature females, but once they reach adolescence, they are generally prevented by older males from interacting sexually with females. However, their participation in same-sex activity increases steadily throughout this period rather than rising sharply when female partners become “unavailable” (or dropping when they are once again available). In fact, homosexual activity reaches its maximum level during adulthood when heterosexual activity also peaks.⁵¹

Although younger male Musk-oxen may be excluded from heterosexual mating opportunities by older males, this does not “cause” the homosexual activity that occurs in this species. Courtship and mounting activity between males generally takes place in the breeding (harem) herds and is initiated by adult bulls toward yearlings—in other words, by the males who do have access to females. Most other adult males are excluded from breeding as well, yet homosexual behavior is not characteristic of the all-male herds where such bulls often spend much of their time. Additionally, in captive groups lacking older males to “prevent” heterosexual mating, homosexual mounting still occurs at a fairly high rate alongside opposite-sex mounting. Likewise, homosexual behaviors in male Asiatic Elephants occur in both breeding and nonbreeding individuals. When older or higher- ranking males (who usually monopolize female partners) are prevented from mating heterosexually in captive groups, younger or lower-ranking males are then able to copulate with females. However, same-sex activities continue in both age/rank groups regardless of whether they have access to female partners or not. In fact, males who are heterosexually active may exhibit higher levels of homosexual activity than those who do not mate with females. In New Zealand Sea Lions, most younger males are excluded from breeding, but homosexual activity also occurs among adult breeding males. Lower-ranking male Wolves are prevented from mating with the highest- ranking female in the pack, but rather than mating with the available lower-ranking females, such males often mount each other. Finally, although homosexual activity in adolescent Killer Whales is attributed to their exclusion from heterosexual mating opportunities, adult males who have access to females also sometimes participate in same-sex activity. In addition, adolescents spend roughly the same proportion of their time as do adults engaging in