Biological Exuberance: Animal Homosexuality and Natural Diversity

Biological Exuberance: Animal Homosexuality and Natural Diversity

by Bruce Bagemihl

Paperback(First Edition)

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A Publishers Weekly Best Book

One of the New York Public Library's "25 Books to Remember" for 1999

Homosexuality in its myriad forms has been scientifically documented in more than 450 species of mammals, birds, reptiles, insects, and other animals worldwide. Biological Exuberance is the first comprehensive account of the subject, bringing together accurate, accessible, and nonsensationalized information. Drawing upon a rich body of zoological research spanning more than two centuries, Bruce Bagemihl shows that animals engage in all types of nonreproductive sexual behavior. Sexual and gender expression in the animal world displays exuberant variety, including same-sex courtship, pair-bonding, sex, and co-parenting—even instances of lifelong homosexual bonding in species that do not have lifelong heterosexual bonding.

Part 1, "A Polysexual, Polygendered World," begins with a survey of homosexuality, transgender, and nonreproductive heterosexuality in animals and then delves into the broader implications of these findings, including a valuable perspective on human diversity. Bagemihl also examines the hidden assumptions behind the way biologists look at natural systems and suggests a fresh perspective based on the synthesis of contemporary scientific insights with traditional knowledge from indigenous cultures.

Part 2, "A Wondrous Bestiary," profiles more than 190 species in which scientific observers have noted homosexual or transgender behavior. Each profile is a verbal and visual "snapshot" of one or more closely related bird or mammal species, containing all the documentation required to support the author's often controversial conclusions.

Lavishly illustrated and meticulously researched, filled with fascinating facts and astonishing descriptions of animal behavior, Biological Exuberance is a landmark book that will change forever how we look at nature.

Product Details

ISBN-13: 9780312253776
Publisher: St. Martin's Press
Publication date: 04/10/2000
Series: Stonewall Inn Editions (Paperback)
Edition description: First Edition
Pages: 768
Product dimensions: 6.00(w) x 9.00(h) x 1.70(d)

About the Author

Bruce Bagemihl, Ph.D., is a biologist and researcher who has served on the faculty of the University of British Columbia, where he taught linguistics and cognitive science. He has published diverse essays and scientific articles on issues pertaining to language, biology, gender, and sexuality. He lives in Seattle, Washington.

Read an Excerpt

Biological Exuberance

Part 1

A Polysexual, Polygendered World

Chapter 1

The Birds and the Bees

The universe is not only queerer than we suppose, it is queerer than we can suppose.

—evolutionary biologist J. B. s. HALDANE1


In the dimly lit undergrowth of a Central American rain forest, jewel-like male hummingbirds flit through the vegetation, pausing briefly to mate now with a male, now with a female. A whale glides through the dark and icy waters of the Arctic, then surges toward the surface in a playful frenzy of churning water and splashing, her fins and tail caressing another female. Drifting off to sleep, two male monkeys lie gently in each other's arms, cradled by one of the ancient jungles of Asia. A herd of deer picks its way cautiously through a semidesert scrub of Texas, each animal simultaneously male but not-quite-male, with half-developed, velvety antlers and diminutive, fine-boned proportions. In a protected New Zealand inlet, a pair of female gulls—mated for life—tend their chicks together. Tiny midges swarm above a bleak tundra of northern Europe, a whirlwind of mating activity as males couple with each other in midair. Circling and prancing around her partner, a female antelope courts another female in an ageless, elegant ritual staged on the African savanna.

Although biologist J. B. S. Haldane was not (necessarily) referring to homosexuality when he spoke of the "queerness" of the natural world, little did he know how accurate his statement would turn out to be. The world is, indeed, teeming with homosexual, bisexual, and transgendered creatures of every stripe and feather. From the Southeastern Blueberry Bee of the United States to more than 130 different bird species worldwide, the "birds and the bees," literally, are queer.2

On every continent, animals of the same sex seek each other out and have probably been doing so for millions of years.3 They court each other, using intricate and beautiful mating dances that are the result of eons of evolution. Males caress and kiss each other, showing tenderness and affection toward one another rather than just hostility and aggression. Females form long-lasting pair-bonds—or maybe just meet briefly for sex, rolling in passionate embraces or mounting one another. Animals of the same sex build nests and homes together, and many homosexual pairs raise young without members of the opposite sex. Other animals regularly have partners of both sexes, and some even live in communal groups where sexual activity is common among all members, male and female. Many creatures are "transgendered," crossing or combining characteristics of both males and females in their appearance or behavior. Amid this incredible variety of different patterns, one thing is certain: the animal kingdom is most definitely not just heterosexual.

Homosexual behavior occurs in more than 450 different kinds of animals worldwide, and is found in every major geographic region and every major animal group.4 It should come as no surprise, then, that animal homosexuality is not a single, uniform phenomenon. Whether one is discussing the forms it takes, its frequency, or its relationship to heterosexual activity, same-sex behavior in animals exhibits every conceivable variation. This chapter presents a broad overview of animal homosexuality and places it in the context of a number of other phenomena involving alternative genders and sexualities.

The Many Forms of Animal Homosexuality

For most people, "homosexuality" means one thing: sex. While it's true that animals of the same gender often interact sexually with each other, this is only one aspect of same-sex expression. Animal homosexuality represents a vast and diverse range of activities: it is neither a monolithic nor an exclusively sexual phenomenon. This section offers a survey of the full range of homosexual activity found in the animal world, organized around five major behavioral categories: courtship, affection, sex, pair-bonding, and parenting. While these categories are not mutually exclusive and often blend imperceptibly into one another, they offer a useful introduction to the multiplicity of homosexual expression in the animal kingdom.

A word on terminology is in order. In this book, heterosexuality is defined as courtship, affectionate, sexual, pair-bonding, and/or parenting behaviors between animals of the opposite sex, while homosexuality is defined as these same activities when they occur between animals of the same sex. When applied to people, the terms homosexual, gay, or lesbian can refer either to a particular behavior when it occurs between two men or two women, or to an individual whose primary "identity" involves any or all of these activities. Since the notion of identity is inappropriate to ascribe to animals, these terms will be reserved for the behaviors that animals engage in and, where relevant, to describe individuals whose primary "orientation" is toward animals of the same sex where courtship, sexual, and/or pair-bonding activities are concerned. In addition, because the terms gay and lesbian have particularly human connotations, these will generally be avoided in favor of homosexual(ity) or same-sex (although it must be remembered that each of these words can have specific meanings independent of their human connotations when used in relation to animals, and they are employed as cover terms for widely divergent activities even among humans). When a particular individual engages in both homosexual and heterosexual activity, these words are limited to describing the animal'sspecific behaviors (depending on the gender of the animal's partner), while the animal itself is described as bisexual.5

Pirouette Dances, Ecstatic Displays, and Triumph Ceremonies: Courtship Patterns

To attract the attention and interest of a potential partner, animals often perform a series of stylized movements and behaviors prior to mating, sometimes in the form of a complex visual or vocal display. This is known as courtship behavior, and it usually indicates that one animal is advertising his or her presence to prospective mates or is sexually interested in another individual. If the interest is mutual, this may lead to mating or other sexual activity and possibly pair-bonding (for example, in birds). Some animals also use special courtship behaviors to conclude, as well as initiate, sexual activity, or to reinforce their pair-bonds. Courtship behavior is a common feature of homosexual interactions, occurring in nearly 40 percent of the mammals and birds in which same-sex activity has been observed.

Same-sex courtship assumes a dizzying array of forms, and zoologists often use evocative or colorful names as the technical terms to designate these most striking of animal behaviors (which are usually part of heterosexual interactions as well). Many species perform elaborate dances or kinetic displays, such as the "strutting" of female Sage Grouse, who spread their fanlike tails; or the spectacular acrobatics and plumage displays of Birds of Paradise and Superb Lyrebirds; or the courtship encounters of Cavies, who "rumba," "rumble," "rump," and "rear" each other in an alliterative panoply of choreographed behaviors. In other cases, subtler poses, stylized postures, or movements are used, such as the foreleg kicking found in the courtship displays of many hoofed mammals; "rear-end flirtation" in male Nilgiri Langurs and Crested Black Macaques; ritual preening and bowing during courtship interactions in Penguins; "tilting" and "begging" postures in Black-billed Magpies; "jerking" by female Koalas; and "courtship feeding"—a ritual exchange of food gifts seen in same-sex (and opposite-sex) interactions among Antbirds, Black-headed and Laughing Gulls, Pukeko, and Eastern Bluebirds. Sometimes two courting individuals perform mutual or synchronized displays, such as the "triumph ceremonies" of male Greylag Geese and Black Swans; the "mutual ecstatic" and "dabbling" displays of Humboldt and King Penguins, respectively; synchronous aquatic spiraling in male Harbor Seals and Orcas; the elaborate "leapfrogging" and "Catherine wheel" courtship displays by groups of Manakins; and synchronized wing-stretching and head-bobbing in homosexual pairs of Galahs. Many birds have breathtaking aerial displays, including tandem flying in Griffon Vultures, shuttle displays and "dive-bombing" in Anna's Hummingbirds, "hover-flying" in Black-billed Magpies, "song-dancing" in Greenshanks, and the "bumblebee flight" of Red Bishop Birds.

Animals sometimes exploit specific spatial and environmental elements in their courtship activities as well. Special display courts are used in same-sex (and opposite-sex) interactions in many species, including the "drumming logs" of male Ruffed Grouse, the elaborate architectural creations of Regent Bowerbirds, and the traditional group or communal display areas known as leks found in animals as diverse as Kob antelopes, Long-tailed Hermit Hummingbirds, and Ruffs. In other species, dramatic chases that may cover great distances are part of same-sex interactions: aerial pursuits occur in Greenshanks, Golden Plovers, Bank Swallows, and Chaffinches; ground chases take place during courtships in Mule Deer, Cheetahs, Whiptail Wallabies, and Redshanks; aquatic pursuits occur in Australian Shelducks; while Black-billed Magpies combine both ground and aerial pursuit in their courtship behavior known as chase-hopping. Perhaps most amazing of all are the light-related displays of a number of bird species, which are designed to utilize specific properties of sunlight or other luminosity in the bird's environment. Guianan Cock-of-the-Rock, for example, position their leks and courtship displays in special "light environments" that maximize the visibility of the birds through a sophisticated interaction of the ambient light, the reflectance and coloration of the bird's own (brilliant orange) plumage, and the forest geometry in which they are located. Anna's Hummingbirds precisely orient the trajectory of their stunning aerial climbs and dives to face into the sun, thereby showing off their iridescent plumage to its best. As a male swoops toward the object of his attentions (either male or female), he resembles a brilliant glowing ember that grows in intensity as he gets closer. To advertise their presence on the lek, male Buff-breasted Sandpipers perform a wing-raising display that exploits the midnight sun of their arctic habitat. Seen from a distance, the brilliant white underwings of each bird flash momentarily against the dull tundra background, reflecting the weak late-night sunlight and thereby creating a luminous semaphore that attracts other birds, both male and female, to their territories.6

In addition to spectacular visual displays, homosexual courtship—like the corresponding heterosexual behaviors—can involve a veritable cacophony of different sounds. Female Kob antelopes whistle, male Gorillas pant, female Rufous Rat Kangaroosgrowl, male Blackbuck antelopes bark, female Koalas bellow, male Ocellated Antbirds carol, female Squirrel Monkeys purr, and male Lions moan and hum. The "snap-hiss" ceremonial calls of Black-crowned Night Herons, the croaking of male Moose, "geckering" and "snirking" of female Red Foxes, the chirp-squeaks of male West Indian Manatees, "yip-purr" calls of Hammerheads, the yelping and babble-singing of Black-billed Magpies, "lip-smacking" in several Macaque species, the humming call of Pukeko, "stutters" and "chirps" of male Cheetahs, the "vacuum-slurping" of male Caribou, and pulsive scream-calls in Bowhead Whales are just some of the vocalizations heard during same-sex courtship and related interactions. Sometimes pairs of birds execute synchronized vocal displays, as in the duets of rolling calls performed by Greylag gander pairs, or the precisely syncopated "moo" calling of pairs of male Calfbirds. In a few cases, courtship activities involve nonvocal sounds or sounds produced in unusual ways. Male Guianan Cock-of-the-Rock, Ruffed Grouse, Victoria's Riflebirds, and Red Bishop Birds, for example, make distinctive whistling, drumming, or clapping sounds by beating or fanning their wings (which in some cases have specially modified, sound-producing feathers), while male Anna's Hummingbirds produce a shrill popping sound as a result of air passing through their tail feathers during display flights. Some of the most extraordinary sounds during same-sex courtship are made by aquatic animals: Walruses generate eerily metallic "bell" sounds by striking special throat pouches with their flippers and castanet-like "knocks" by chattering their teeth, while Musk Ducks have an entire repertoire of courtship splashing sounds made by kicking their feet during displays variously named the paddle-kick, plonk-kick, and whistle-kick. Finally, some Dolphins appear to engage in a sort of sonic "foreplay": male Atlantic Spotted Dolphins have been observed stimulating their partner's genitals with pulsed sound waves, using a type of vocalization known as a genital buzz.

In most species the same courtship behaviors are used in both homosexual and heterosexual interactions. Sometimes, however, same-sex courtship involves only a subset of the movements and behaviors found in opposite-sex displays. For example, when Canada Geese court each other homosexually, they perform a neckdipping ritual also found in heterosexual courtships, but do not adopt the special posture that males and females use after mating. In animals like the Western Gull or Kob antelope, individuals vary as to how many courtship behaviors they use in same-sex interactions. Some exhibit only one or two of the typical courtship postures and movements, while others go through the entire elaborate courtship sequence. Perhaps most interesting are those creatures that have a special courtship pattern found only in homosexual interactions. Male Ostriches, for example, perform a unique "pirouette dance" only when courting other males, while female Rhesus Macaques engage in courtship games such as "hide-and-seek" that are unique to lesbian interactions.

Kisses, Wuzzles, and Necking: Affectionate Behaviors

Many animals of the same sex touch each other in ways that are not overtly sexual (they do not involve direct contact of the genitals) but that do nevertheless haveclear sexual or erotic overtones. These are referred to as affectionate activities and are found in nearly a quarter of the animals in which some form of homosexual activity occurs. Although many of these behaviors (grooming, embracing, play-fighting) can occur in other contexts, their erotic nature in a same-sex context is usually obvious: the two animals may be visibly sexually aroused, the behavior may directly precede or follow homosexual copulation or courtship, or the affectionate activity may occur in a same-sex pair-bond.

One type of affectionate activity is simple grooming or rubbing. Male Lions "head-rub" and roll around with each other before having sex together; Bats such as Gray-headed Flying Foxes and Vampire Bats engage in erotic same-sex grooming and licking; male Mountain Sheep rub their horns and faces on other males, sometimes becoming sexually aroused; Whales and Dolphins stroke and rub each other with their flippers or tail flukes, as well as rub bodies together; while numerous primates such as Apes, Macaques, and Baboons frequently caress and groom each other in both sexual and nonsexual contexts. A few birds such as Humboldt Penguins, Pukeko, Black-billed Magpies, and Parrots also indulge in preening—the avian equivalent of grooming—in their homosexual interactions or pair-bonds.

Some animals also "kiss" each other: male African Elephants, female Rhesus Macaques, male West Indian Manatees and Walruses, female Hoary Marmots, and male Mountain Zebras (among others) all touch mouths, noses, or muzzles during their homosexual encounters. Even some birds, such as Black-billed Magpies, engage in mutual beak-nibbling or "billing" as part of same-sex courtship. In primates, kissing (in both homosexual and heterosexual contexts) can bear a startling resemblance to the corresponding human activity: a number of species such as Squirrel Monkeys and Common Chimpanzees engage in full mouth-to-mouth contact, while male Bonobos kiss each other with "passionate" openmouthed kisses with considerable mutual tongue stimulation.

Numerous species of Monkeys and Apes also "hug" or embrace same-sex partners in homosexual contexts (usually face-to-face, although male Bonobos and Vervets also embrace while standing in a front-to-back position). Among non-primates, female Bottlenose Dolphins clasp each other during homosexual activity, male West Indian Manatees embrace one another underwater, while Gray-headed Flying Foxes wrap their wing-membranes around same-sex partners while stimulating each other. A striking form of same-sex embracing is the "sleeping huddle" found in Stumptail and Bonnet Macaques: a pair of males often sleep together in a front-to-back position, one male wrapping his arms around the other and sometimes even holding on to his partner's penis. A similar sleeping arrangement occurs, surprisingly, among male Walruses, who often sleep in same-sex pairs or extended "chains" of males, all clasping each other in a front-to-back position as they float at the water's surface.

A number of mammals also engage in mock battles or "play-fights" that have erotic overtones. Although they superficially resemble aggressive behavior, these "battles" or "contests" do not involve any physical violence and are clearly distinguished from actual cases of aggressive or territorial behavior in these species. Male African Elephants, for example, frequently become sexually aroused and develop erections when they perform ritualized erotic jousting matches, while numerous hoofed mammals such as male Giraffes, Bison, Blackbuck antelopes, and Mule Deer mount each other during play-fights or ritualistic jousting. Among primates such as Orang-utans, Gibbons, and Proboscis Monkeys, males sometimes engage in playful wrestling matches that can develop into sexual encounters, while male Australian and New Zealand Sea Lions also indulge in play-fighting combined with same-sex mounting. Although play-fighting is most common among male mammals, female Cheetahs sometimes engage in "mock fighting" with each other as part of same-sex courtship sequences, while female (and male) Galahs and Orange-fronted Parakeets in same-sex pairs have playful "fencing bouts" with their bills.7

Many other types of affectionate and contactual behaviors occur between animals of the same sex. Sometimes animals gently bite, nibble, or chew on each other's ears (female Hoary Marmots), or wings and chests (Gray-headed Flying Foxes), or rumps (male Dwarf Cavies), or necks (male Savanna Baboons). Male African Elephants intertwine their trunks, while female Japanese Macaques sometimes suck each other's nipples, and male Crested Black Macaques and Savanna Baboons affectionately pat or grab other males' rear ends. Pairs of animals may sit, huddle, or lie together in close proximity, sometimes touching hands or putting an arm around the shoulder (female Gorillas, Squirrel Monkeys, and Japanese Macaques, male Siamangs), while male Hanuman Langurs "cuddle" together by sitting back-to-front, one male between the other's legs with his partner's hands resting on his loins. Male Lions and female Long-eared Hedgehogs slide the lengths of their bodies along their partner's, while male Bowhead Whales, Killer Whales, and Gray Seals roll their bodies over each other, and same-sex companions in Gray Whales and Botos swim side by side while gently touching each other with their fins.

Some animals have developed unique forms of touching that combine several different types of affectionate activities along with courtship and sexual behaviors. Male Giraffes engage in "necking", a multifaceted activity that incorporates elements of play-fighting, courtship, and sexuality, in which they rub their necks along each other's body while also licking, sniffing, and becoming sexually aroused by one another. In Giraffes and other species, these types of activities sometimes involvemultiple animals interacting simultaneously in near "orgies" of bodily contact. Spinner Dolphins, for example, participate in "wuzzles"—group sessions of mutual caressing and sexual activity (both same-sex and opposite-sex)—while West Indian Manatees have a similar sort of "free-for-all" group activity known as cavorting, which can involve rubbing, chasing, and sexual interactions, among many other activities. Among birds, Hammerheads, Acorn Woodpeckers, and Blue-bellied Rollers have ritualized bouts of courtship and mounting activity that may involve groups of individuals and both same-sex and opposite-sex partners. The distinctive and, in many cases, unabashedly sensual and playful aspects of some of these activities are aptly reflected in the descriptive names given to them by zoologists. In fact, the term wuzzle—though used as a technical designation for this behavior in the scientific literature—is actually a nonsense word coined by a marine biologist, whose whimsical "etymology" for the name could be right out of Lewis Carroll: "The term comes from W. E. Schevill of Woods Hole Oceanographic Institution, who, when asked what the behavior was, replied without hesitation, 'Why, it looks like a wuzzle to me.'"8

Mounting, Diddling, and Bump-Rumping: Sexual Techniques

Affectionate activity often leads to, or is inseparable from, overtly sexual behavior—defined here as any contact between two or more animals involving genital stimulation. Stumptail and Crab-eating Macaques, for example, kiss their same-sex partners during sexual mounting. In fact, mounting is the most common type of sexual behavior found in homosexual contexts: one animal climbs on top of the other in a position similar to heterosexual intercourse, usually from behind in a front-to-back position (that is, one animal mounted on the back of the other). More than 95 percent of mammal and bird species use this position, for both male and female homosexual interactions. On the other hand, some animals—particularly primates such as Gorillas, Bonobos, and White-handed Gibbons—use a face-to-face position (in addition to, or instead of), and in some cases this is more common in homosexual encounters than in heterosexual ones. Belly-to-belly copulation is also the norm for both homosexual and heterosexual interactions in Dolphins. Occasionally more unusual or "creative" mounting positions are used, particularly by female animals. In Bonobos, Stumptail Macaques, and Japanese Macaques, for instance, females sometimes interact in a supine or semirecumbent position, one individual behind the other with her partner between her legs or sitting "in her lap" (which may also be done in a face-to-face position). Occasionally female Warthogs, Rhesus and Japanese Macaques, Koalas, and Takhi mount their female partner from the side rather than from behind; lateral mounts also sometimes occur during heterosexual interactions in these (and other) species. And in some animals a "backward," head-to-tail mounting position is occasionally used, e.g., in Botos, Hammerheads, Ruffs, and Western Gulls. Most same-sex interactions involve only two individuals at a time, but group sexual (and courtship) activity—involving anywhere from three or four (Giraffes, Lions) to six or more (Bowhead Whales, Mountain Sheep) partners—occurs in over 25 different species.

The actual type of genital contact varies widely. Full penetration in male anal intercourse occurs in some species (for example, Orang-utans, Rhesus Macaques, Bison, and Bighorn rams), while female penetration of various types occurs during lesbian interactions in Orang-utans (insertion of the finger into the vagina), Bonobos (insertion of the erect clitoris into the vulva), and Bottlenose and Spinner Dolphins (insertion of a fin or tail fluke into the female's genital slit). Simple pelvic thrusting and rubbing of the genitals on the rump of the other animal is widespread in both male and female homosexual mounts (occurring in the Northern Fur Seal, Lion, and Proboscis Monkey, among others), and simple genital-to-genital touching is the form of homosexual (and heterosexual) contact in species where males do not have a penis (as in most birds, such as the Pukeko and Tree Swallow). A more unusual type of male homosexual contact involves various forms of non-anal penetration. In Whales and Dolphins, both males and females have a genital slit or opening; when not aroused, the male's penis is contained in the cavity leading to this slit. Homosexual activity in Bowhead Whales, Bottlenose Dolphins, and Botos sometimes involves insertion of the penis of one male into the genital slit of the other. Other more unusual forms of penetration have also been documented: male Botos occasionally insert the penis into a male partner's blowhole (on the top of his head!), while male Orang-utans have even been observed retracting their penis to form a sort of "hollow" or concavity that another male can penetrate. Clitoral rubbing or other types of genital tribadism are found in female Bonobos, Gorillas, and Rhesus Macaques (among others), while males in several species (e.g., White-handed Gibbons, West Indian Manatees, and Gray Whales) rub their penises together or on each other's body. In male Bonobos, mutual genital rubbing sometimes takes the form of an activity with the colorful name of "penis fencing," in which the males hang suspended by their arms and rub their erect organs against each other.

Oral sex of various kinds also occurs in a number of species. This may involve actual sucking of genitals (fellatio between males in Bonobos, Orang-utans, Siamangs, and Stumptail Macaques); licking of genitals (cunnilingus in Common Chimpanzees, Long-eared Hedgehogs, and Kob antelopes; penis-licking in Thinhorn Sheep and Vampire Bats; genital licking in female Spotted Hyenas and male Cheetahs); mouthing, nuzzling, or "kissing" of genitals (female Gorillas, male Savanna Baboons, Crab-eating Macaques, and West Indian Manatees); and genital sniffing in female Pronghorns and Marmots as well as scrotal sniffing in Whiptail and Red-necked Wallabies. Male Stumptail Macaques even perform mutual fellatio in a sixty-nine position, while males of a number of primate species (including Gibbons, Bonnet and Crested Black Macaques, and Nilgiri Langurs) sometimes actually eat or swallow their partner's (or their own) semen—though usually after mutual genital rubbing or manual stimulation rather than oral sex.9 Dwarf Cavies and Rufous Bettongs occasionally indulge in anal licking, nuzzling, and sniffing with same-sex (and opposite-sex) partners. Another sort of "oral" sexual activity is called beak-genital propulsion and occurs among both male and female Bottlenose and Spinner Dolphins: one animal inserts its snout or "beak" into the genital slit of another, simultaneously stimulating and propelling its partner forward while swimming (a similar behavior in Orcas, involving simple nuzzling or touching of the genitals with the snout, is known as beak-genital orientation).

Another type of activity found during homosexual interactions is masturbation, in which one animal stimulates its own or its partner's genitals with a finger, hand, foot, flipper, or some other appendage. For example, male Savanna Baboons often touch, grab, or fondle the genitals of another male—this behavior is known aptly as diddling—while male Bottlenose Dolphins and West Indian Manatees sometimes rub another male's penis with their flippers. Male Rhesus and Crested Black Macaques, female Gorillas, male Vampire Bats, female Proboscis Monkeys, and male Walruses sometimes masturbate themselves when mounting, courting, or interacting sexually with another animal of the same sex. Mutual masturbation in a side-by-side sixty-nine position occurs in female Crested Black Macaques, while male Bonnet and Stumptail Macaques masturbate each other and even fondle one another's scrotums. Another form of mutual masturbation in these species involves two males backing up toward each other and fondling each other's genitals between their legs. In Bonobos and Common Chimpanzees, individuals often rub their anal and genital regions together while in this rump-to-rump position, prompting zoologists to give these behaviors names like "rump-rubbing" and "bump-rump." Other more unusual forms of "manual" stimulation include mutual genital stimulation using trunks in female Elephants, and anal stimulation and penetration with fingers by male Common Chimpanzees, Siamangs, and Crab-eating Macaques.

Consorts, Satellites, and Triumvirates: Same-Sex Mates and Pair-Bonding

Wild animals often form significant pair-bonds with animals of the same sex. Homosexual pair-bonding takes many different forms, but two broad categories can be recognized: "partners," who engage in sexual or courtship activities with each other, and "companions," who are bonded to each other but do not necessarily engage in overt sexual activity with one another. More than a third of the mammalsand birds in which homosexual activity occurs have at least one of these types of same-sex bonding. The archetypal example of a "partnership" is the mated pair: two individuals who are strongly bonded to one another in a way that is equivalent to heterosexually paired animals of the same species. Partners engage directly in courtship, sexual, and/or parenting behaviors; they usually spend a significant amount of time with each other; and they do similar activities together. This is found primarily in birds (more than 70 different species)—not surprisingly, since heterosexual pairing is typical of feathered creatures (but generally rare in other animal groups). Examples of homosexual mates are found in male Black Swans and Black-headed Gulls, and female Black-winged Stilts and Silver Gulls (among many others). In mammals, partnerships take many different forms, including "consortships" in female Rhesus and Japanese Macaques, "sexual friendships" in Stumptail and Crab-eating Macaques, "tending bonds" between male Bison, and "coalitions" between male Bonnet Macaques, Savanna Baboons, and Cheetahs. Some animals, while not necessarily forming same-sex bonds, do have "preferred" or "favorite" sexual and affectionate partners with whom they tend to interact more often than with others: this is true for Bonobos, Gorillas, Killer Whales, and Dwarf Cavies, among others.

Many forms of same-sex partnership are exclusive or monogamous, and partners may even actively defend their pair-bond against the intrusion of outside individuals (for instance in male Gorillas, female Japanese Macaques, and male Lions). Animals of the same sex sometimes also compete with each other for the attentions of homosexual partners, as in male Gorillas and Blue-winged Teals; female Orang-utans, Japanese Macaques, and Orange-fronted Parakeets may even compete with males for "preferred" female partners. Some partnerships, however, are "open" or nonmonogamous: female Bonobos and Rhesus Macaques, for instance, may have sexual relations with several different "favorite" partners or consorts (of both sexes). Males in homosexual pairs of Greylag Geese, Laughing Gulls, Humboldt Penguins, and Flamingos sometimes engage in "promiscuous" copulations with birds (male or female) other than their mate (heterosexual pairs in these species are also sometimes nonmonogamous). Another form of nonmonogamy occurs among lesbian pairs in a number of Gulls and other birds: one or both females sometimesmate with a male (while still maintaining their same-sex bond) and are thereby able to fertilize their eggs and become parents.

The second main type of homosexual pairing is the "companionship." Two animals of the same sex may bond with each other, often spending most of their time together exclusive of the opposite sex, but they do not necessarily engage in recognizable courtship or sexual activities with each other. For example, older African Elephant bulls sometimes form long-lasting associations with a younger "attendant" male: these animals are loners, spending all their time with each other rather than with other Elephants, helping each other, and never engaging in heterosexual activity. Male Calfbird companions display and travel together and also sometimes share a "home" with one another (a special perch known as a retreat where they spend time away from the display court). Similar same-sex associations are found in many other species, including Orang-utans, Gray Whales, Grizzly Bears, Vampire Bats, and Superb Lyrebirds. Younger same-sex attendants are known as satellites in male Moose and shadows in male Walruses, while companions are called duos in male Hanuman Langurs and spinsters in female Warthogs—the latter is something of a misnomer, though, since Warthog companions do occasionally participate in sexual activity with males or females, but not necessarily with their companions.

Sometimes more than two animals bond together, forming a "trio" (in either partnership or companionship form). This arrangement can consist of three animals all of the same sex who are bonded with each other, as occasionally happens among female Ring-billed Gulls and male African Elephants, White-tailed Deer, and Black-headed Gulls. Trios can also be bisexual, consisting of two females and one male (e.g., Canada Geese, Common Gulls, and Jackdaws) or two males and one female (Greylag Geese, Black Swans, Sociable Weavers); in Oystercatchers, both types occur. In either form of a bisexual trio, there is significant bonding, courtship, and/or sexual behavior between the two animals of the same sex. This distinguishes such associations from heterosexual trios, in which two animals of the same sex are bonded with an opposite-sexed individual but not to each other. Same-sex trios of closely bonded male Greylag Geese or female Grizzly Bears are also sometimes known as triumvirates, while bisexual (and heterosexual) trios in Flamingos are called triads. In a few species, "quartets" involving simultaneous homosexual and heterosexual bonds between four individuals sometimes occur: in Greylag Geese and Black-headed Gulls, for instance, three males and a female sometimes bond with each other, while in Galahs, two males and two females may associate in a quartet with various bonding arrangements between them.

Homosexual pair-bonds vary not only in their type, but also in their duration. Same-sex bonding often follows the species-typical pattern for heterosexual pairing in terms of how long it lasts. In species such as the Greylag Goose, for example, which remain mated for life (or else for many consecutive years), male pairs are also generally long-lasting or lifelong, while in Bison, tending bonds usually last only a few days or hours in both heterosexual and homosexual situations. In some cases, long-term pair bonding involves continuous association throughout the year, as among male Ocellated Antbirds. This contrasts with seasonal association, for example among several species of Gulls, in which females re-pair with the same femaleonly during the mating season. Homosexual pairs may also be of shorter duration than heterosexual ones in some species: Black-headed Gull male couples, for example, appear to be more prone to divorce than heterosexual ones. However, in many cases homosexual pairings, particularly companionships, actually exceed heterosexual ones in their stability and duration. Among Lions and Elephants, for example, the bond between male companions is closer and longer-lasting than any heterosexual bonds (which, in these and many other species, are virtually nonexistent beyond mating), while mated gander pairs in Greylag Geese are often more strongly bonded than heterosexual pairs. Consortships between Japanese Macaque females sometimes develop into yearlong friendships, unlike the majority of heterosexual associations in this species. In fact, in a number of animals the only pair-bonds that occur are homosexual, not heterosexual. Male Bottlenose Dolphins, for example, form lifelong partnerships with each other, while males and females in this species do not generally pair-bond with one another at all. Other animals with same-sex but not opposite-sex pairings (often in the form of companionships) include Musk-oxen, Wapiti, White-tailed Deer, Warthogs, Cheetahs, Eastern Gray Kangaroos, Red Squirrels, and Calfbirds.

Formidable Fathers and Supernormal Mothers: Homosexual Parenting

Same-sex pairs in many species (especially birds) raise young together. Not only are they competent parents, homosexual pairs sometimes actually exceed heterosexual ones in the number of eggs they lay, the size of their nests, or the skill and extent of their parenting. How are such animals able to have offspring in the first place if they are in homosexual associations? Many different strategies are used, including several in which one or both partners are the biological parent(s) of the young they raise together. The most common parenting arrangement of this type is found in lesbian pairs of several Gull, Tern, and Goose species: one or both female partners copulate with a male to fertilize her eggs. No bonding or long-term association develops between the female and the male (who is essentially a "sperm donor" to the homosexual pair), and the youngsters are then jointly raised by both females without any assistance from a male parent. Because female birds can lay eggs regardless of whether they are fertilized, however, each partner in a lesbian pair usually contributes a full clutch of eggs to their nest even if she hasn't mated with a male. As a result, female homosexual pairs often lay what are called supernormal clutches, that is, double the number of eggs usually found in nests of heterosexual pairs.10

Sometimes two female animals who already have offspring join forces, bonding together and raising their young as a same-sex family unit (among mammals, female coparents may even suckle each other's young): this occurs in Grizzly Bears, Red Foxes, Warthogs, Dwarf Cavies, Lesser Scaup Ducks, and Sage Grouse. Notably, heterosexual pairs do not occur in these species, and most offspring are otherwise raised by single females.11 In some species, a nonbreeding animal bonds with a (single) breeding animal and helps parent its young: this occurs in Squirrel Monkeys, Northern Elephant Seals, Jackdaws (where a widowed female with young may pairwith a single female), and Greater Rheas (where one male may help another incubate his eggs and then raise the young together). In most such joint parenting arrangements (as opposed to homosexual mated pairs), there is not necessarily any overt courtship or sexual activity between the bonded coparents, although in some species (e.g., Squirrel Monkeys, Northern Elephant Seals, Emus, Sage Grouse), homosexual activity does occur in contexts other than between coparents. Still other birds (e.g., Greylag Geese, Common Gulls, Oystercatchers) may form bisexual parenting trios, mating with the opposite-sexed partner(s) in their association while maintaining homosexual and heterosexual bonds simultaneously, with all three birds then raising the resulting offspring together. A variation on this arrangement in Black Swans involves a sort of "surrogate motherhood": established male homosexual pairs sometimes associate temporarily with a female, mating with her to father their own offspring. Once the eggs are laid, however, they chase her away and raise the cygnets on their own as a homosexual couple.

In a number of cases, homosexual pairs raise young without being the biological parents of the offspring they care for. Some same-sex pairs adopt young: two female Northern Elephant Seals occasionally adopt and coparent an orphaned pup, while male Hooded Warblers and Black-headed Gulls may adopt eggs or entire nests that have been abandoned by females, and pairs of male Cheetahs occasionally look after lost cubs. Sometimes female birds "donate" eggs to homosexual couples through a process known as parasitism: in many birds, females lay eggs in nests other than their own, leaving the parenting duties to the "host" couple. This occurs both within the same species, and (more commonly) across species, and usually involves heterosexual hosts. Male pairs of Hooded Warblers, however, sometimes receive eggs from Brown-headed Cowbirds (and possibly also from females of their own species) in this way; within-species parasitism may also provide eggs for male pairs of Black-headed Gulls and female pairs in Roseate and Caspian Terns. The opposite situation is thought to occur in Ring-billed Gulls: researchers believe that some homosexually paired females actually lay eggs in nests belonging to heterosexual pairs. Finally, some birds in same-sex pairs take over or "kidnap" nests from heterosexual pairs (e.g., in Black Swans, Flamingos) or occasionally "steal" individual eggs (e.g., in Caspian and Roseate Terns, Black-headed Gulls); homosexual pairs in captivity also raise foster young provided to them.

In a detailed study of parental behavior by female pairs of Ring-billed Gulls, scientists found no significant differences in quality of care provided by homosexual as opposed to heterosexual parents. They concluded that there was not anything that male Ring-billed Gull parents provided that two females could not offer equally well.12 This case is not exceptional: homosexual parents are generally as good at parenting as heterosexual ones. Examples of same-sex pairs successfully raising young have been documented in at least 20 species, and in a few cases, homosexual couples actually appear to have an advantage over heterosexual ones.13 Pairs of male Black Swans, for example, are often able to acquire the largest and best-quality territories for raising young because of their combined strength. Such fathers—dubbed "formidable" adversaries by one scientist—consequently tend to be more successful at raising offspring than most heterosexual pairs.14 And in many species in which single parenting is the rule (because there is no heterosexual pair-bonding), same-sex pairs provide a unique opportunity for young to be raised by two parents (e.g., Squirrel Monkeys, Grizzly Bears, Lesser Scaup Ducks). Moreover, in some Gulls, female pairs are consigned (for a variety of reasons) to less than optimal territories, yet they still successfully raise young: in many cases they compensate by investing more parental effort—and are more dutiful in caring for their chicks—than male-female pairs.15 There are exceptions, of course: some female pairs of Gulls, for instance, tend to lay smaller eggs and raise fewer chicks (although this is also true of heterosexual trios attending supernormal clutches), while same-sex parents in Jackdaws, Canada Geese, and Oystercatchers may experience parenting difficulties such as egg breakage or nonsynchronization of incubation duties. By and large, though, same-sex couples are competent and occasionally even superior parents.

Birds in homosexual pairs often build a nest together. Usually they construct a single nest the way most heterosexual pairs do, but other variations also occur: female Common Gulls and Jackdaws sometimes make "twin" or "joint" nests containing two cups in the same bowl, while male Greater Rheas and female Canada Geese may use "double" nests consisting of two adjacent or touching nests. Female Mute Swans occasionally construct two separate nests in which both birds lay eggs. Nests belonging to male couples in some species (e.g., Flamingos and Great Cormorants) are often impressive structures, exceeding the size of heterosexual nests because both males contribute equally to their construction (in heterosexual pairs of these species, usually only one sex builds the nest, or males and females make unequal contributions). Many same-sex pairs construct nests regardless of whether they lay fertile eggs. Male pairs of Mute Swans, Flamingos, Black-crowned Night Herons, and Great Cormorants, for example, usually build nests even though they never acquire eggs, and the male "parents" may even sit on the nests as if they containedeggs, while female pairs frequently build nests in which they lay supernormal clutches that are entirely infertile. Same-sex parents often share incubation duties, either taking turns sitting on their nest (the most common arrangement), or else incubating simultaneously on a single nest (female Red-backed Shrikes, male Emus) or side by side on a twin or double nest (female Jackdaws, male Greater Rheas).

In addition to parenting by homosexual couples, some animals raise young in alternative family arrangements, usually a group of several males or females living together. Gorilla babies, for example, grow up in mixed-sex, polygamous groups where their mothers may have lesbian interactions with each other, while Pukeko and Acorn Woodpeckers live and raise their young in communal breeding groups where many, if not all, group members engage in courtship and sexual activities with one another (both same-sex and opposite-sex). In such situations, individuals that engage in homosexual courtship or copulation activities may either reproduce directly because they also mate heterosexually (Pukeko), or they may assist members of their group in raising young without reproducing themselves (Acorn Woodpeckers).16 Other alternative family constellations include bisexual trios (mentioned above), homosexual trios (as in Grizzly Bears, Dwarf Cavies, Lesser Scaup Ducks, and Ring-billed Gulls) where three mothers jointly parent their offspring, and even quartets, in which four animals of the same (Grizzlies) or both sexes (Greylag Geese) are bonded to each other and all raise their young together.17

Finally, some animals that have homosexual interactions are "single parents." Many female mammals, for example, that court or mate with other females also mate heterosexually and raise the resulting young on their own or in female-only groups (as is typical for exclusively heterosexual females in the same species as well). This is especially prevalent among mammals with polygamous or promiscuous heterosexual mating systems, such as Kob and Pronghorn antelopes and Northern Fur Seals (where males, and sometimes females, usually mate with more than one partner). Males in many polygamous species are often bisexual as well, fathering offspring in addition to courting or mating with other males; typically, however, they do not actively parent their offspring regardless of whether they are bisexual or exclusively heterosexual.18

What's Good for the Goose ... : Comparisons of Male and Female Homosexuality

Is homosexuality more characteristic of male animals or female animals? And does it assume different forms in the two sexes—or, to paraphrase a popular saying, is the behavior of the "goose" essentially similar to that of the "gander"? As it so happens, homosexuality in three species of Geese—Canada, Snow, and Greylag—exemplifies some of the major patterns of male and female homosexuality and the range of variation found throughout the rest of the animal world. In Canada Geese, both males and females participate in the same basic type of homosexual activity, forming same-sex pairs and engaging in some courtship activities. Within these same-sex bonds, however, there are gender differences in some less common behaviors: sexual activity is more characteristic of females (especially if they are partof a bisexual trio), as is nest-building and parenting activity. There are also differences in the frequency of participation of the two sexes: although same-sex pairs are relatively common, accounting for more than 10 percent of pairs in some populations, a greater proportion of the male population participates in same-sex pairing. In contrast, homosexual activity in Snow Geese is vastly different in males than in females, although it is relatively infrequent in both sexes. Females form long-lasting pair-bonds with other females in which sexual activity is not necessarily very prominent, although parenting activity is: both partners lay eggs in a joint nest and raise their young together (they fertilize their eggs by mating with males). Ganders, on the other hand, limit their homosexual activity to same-sex mounting of other males during heterosexual group rape attempts and do not form same-sex pairs (although interspecies gander pairs with Canada Geese sometimes do occur). Finally, in Greylag Geese homosexual activity is found exclusively in males, who form gander pairs that engage in a variety of courtship, sexual, pair-bonding, and parenting activities.

When we look at the full range of species and behaviors, we find that male homosexuality is slightly more prevalent, overall, than female homosexuality, although the two are fairly close. Same-sex activity (of all forms) occurs in male mammals and birds in about 80 percent of the species in which homosexuality has been observed, and between females in just over 55 percent of these (the figures add up to more than 100 percent because both male and female homosexuality are found in some species). It must also be kept in mind that the prevalence of female homosexuality may actually be greater than these figures indicate, but has simply not been documented as systematically owing to the general male bias of many biological studies.19 There is also variation between different animal subgroupings: in carnivores, marsupials, waterfowl, and shorebirds, for example, male and female homosexuality are almost equally common (in terms of the number of species in which each is found), while in marine mammals and perching birds male homosexuality is more prevalent. And in many species same-sex activity occurs only among males (e.g., Boto, a freshwater dolphin) or only among females (e.g., Puku, an African antelope).

The frequency of same-sex behavior in males versus females can also be assessed within a given species, and once again, many different patterns are found: in Rhesus Macaques, Hamadryas and Gelada Baboons, and Tasmanian Native Hens, for example, 80—90 percent of all same-sex mounting is between males, while homosexual activity is also more prevalent among male Gray-headed Flying Foxes.20 In other species, female homosexual activity assumes prominence: more than 70 percent of same-sex copulations in Pukeko are between females, and 70—80 percent of homosexual activity in Bonobos is lesbian. Females account for almost two-thirds of same-sex behaviors in Stumptail Macaques and Red Deer, while homosexual activity is also more typical of females in Red-necked Wallabies and Northern Quolls.21 In some species, however, male homosexuality is so predominant that same-sex activity in females is often missed by scientific observers or rarely mentioned (e.g., Giraffes, Blackbuck, Bighorn Sheep), while the reverse is true in other species (e.g., Hanuman Langurs, Herring Gulls, SilverGulls). In contrast, Pig-tailed Macaque same-sex mounting, Galah pair-bonds, and Pronghorn homosexual interactions are fairly equally distributed between the two sexes (although actual same-sex mounting is more common in male Pronghorns).22

As with the species of Geese mentioned above, gender differences are also apparent in various behavior types. Of those mammal and bird species in which some form of homosexual behavior occurs, each of the activities of courtship, affectionate, sexual, or pair-bonding are generally more prevalent in male animals. They occur among males in 75—95 percent of the species in which they are found, while among females these activities occur in 50—70 percent of the species (again, however, the possible gender bias of the studies these figures are based on must be kept in mind). The one exception is same-sex parenting, which is performed by females in more than 80 percent of the species where this behavior occurs, but by males in just over half of the species that have some form of such parenting. Of course, not all these forms of same-sex interaction always co-occur in the same species, and animals sometimes differ as to which activities males as opposed to females of the same species tend to participate in (as in the Geese). In Silver and Herring Gulls, for example, females form same-sex pairs that undertake parenting duties while males engage in homosexual mounting; in Cheetahs and Lions, both sexes engage in sexual activity, but males in each species also develop same-sex pair-bonds while female Cheetahs participate in same-sex courtship activities. In Ruffs, males engage in sexual, courtship, and (occasional) pairing activity with each other, while Reeves (the name for females of this sandpiper species) participate primarily in sexual activity with one another.

Within each of the categories of courtship, sexual, pairing, and parenting behaviors, further gender distinctions can be drawn. Consider various types of sexual behavior. Mounting as a same-sex activity is ubiquitous and occurs fairly regularly in both males and females (although there are exceptions—in African Elephants, for example, sexual activity between males assumes the form of mounting while female same-sex interactions consist of mutual masturbation). Oral sex (which includes activities as diverse as fellatio, cunnilingus, genital nuzzling and sniffing, and beak-genital propulsion) is about equally prevalent in both sexes. Group sexual activity is more common in males (only occurring among females in 6 species, including Bonobos and Sage Grouse), as are interactions between adults and adolescents (only occurring among females in 9 species, including Hanuman Langurs, Japanese Macaques, Ring-billed Gulls, and Jackdaws, but among males in more than 70 species). Although penetration is also more typical of male homosexual interactions, there are notable exceptions (e.g., Bonobos, Orang-utans, and Dolphins, as mentioned previously). Gender differences sometimes also manifest themselves in the minutiae of various sexual acts. Same-sex mounting in Gorillas, for instance, is performed in both face-to-face and front-to-back positions, but the two sexes differ in the frequency with which these two positions are used: females prefer the face-to-face position, adopting it in the majority of their sexual interactions, while males use it less often, in only about 17 percent of their homosexual mounting episodes.23 In contrast, the frequency of full genital contact during homosexualcopulations is nearly identical for both sexes of Pukeko: females achieve cloacal contact in about 23 percent of their same-sex mounts while males do so in about 25 percent of theirs (in comparison, genital contact occurs in a third to half of all heterosexual mounts). Among Flamingos, though, genital contact is more characteristic of copulations between females than between males.24

Or consider pair-bonding and parenting. Stable, long-lasting pair-bonds are generally not more characteristic of females (contrary to what one might initially expect); mated pairs or partnerships are almost equally common in both sexes (in terms of number of species in which homosexual pair-bonding occurs), while same-sex companionships are more prevalent between males. Likewise, long-term pair-bonds are just as likely to be found between males as females, while nonmonogamy and divorce occur in male and female couples in roughly equal numbers of species. Nor are male couples less successful parents: male coparents or partners are not overrepresented among the few species in which same-sex parents occasionally experience parenting difficulties. One area where a gender difference in same-sex parenting does manifest itself is in the way that homosexual pairs "acquire" offspring. Particularly among birds, female couples can raise their own offspring by simply having one or both partners mate with males without interrupting their homosexual pair-bond. This option is not as widely available for male couples, who usually father their own offspring by forming a longer-lasting (prior or simultaneous) association with a female (as in Black Swans, Greylag Geese, and Greater Rheas).

Japanese Macaques offer a particularly compelling example of the multiple ways that homosexual activity can differ between males and females. Although homosexual mounting occurs in both sexes in this species, males and females differ in the specific details of their sexual interactions. Homosexual mounts are usually initiated by the mounter between males but by the mountee between females, make use of a wider variety of mounting positions between females, are accompanied by a unique vocalization only between males, and involve pelvic thrusting and multiple mounts more often between females than between males.25 The two sexes also differ in their partner selection and pair-bonding activities: females generally form strongly bonded consortships and have fewer partners than males, while the latter tend to interact sexually with more individuals and develop less intense bonds (although some do have "preferred" male partners). Finally, there is a seasonal difference in male as opposed to female same-sex interactions: homosexual mounting is more common outside the breeding season in males but during the breeding season in females, while same-sex bonds in females, but not males, may extend into yearlong associations that transcend the breeding season.

Whether we're talking about ganders and geese or Ruffs and Reeves, whether it's Botos and Bonobos or Pukus and Pukeko, male and female homosexuality can be either surprisingly similar to each other or decidedly distinctive from one another. In any case, a complex intersection of factors is involved in the expression of homosexuality in each gender. As with other aspects of animal homosexuality, preconceived ideas about how males and females act must be reassessed and refined when considering the full range of animal behaviors. In some species such as SilverGulls, male and female homosexualities conform to stereotypes commonly held about similar human behaviors: females form stable, long-lasting lesbian pair-bonds and raise families while males participate in promiscuous homosexual activity. In other species these gender stereotypes are turned completely on their heads, as in Black Swans, where only males form long-term same-sex couples and raise offspring, and Sage Grouse, where only females engage in group "orgies" of homosexual activity.26 And in the majority of cases, male and female homosexualities present their own unique blends of behaviors and characteristics that defy any simplistic categorization—such as Bonobos, where sexual penetration occurs in female rather than male same-sex activity, where sexual interactions between adults and adolescents are a prominent feature of female interactions, and where males do not form strongly bonded relationships with each other the way females do, but engage in less homosexual activity overall and more affectionate activity such as openmouthed kissing. Once again, the diversity of animal homosexuality reveals itself down to the very last detail of expression.

A Hundred and One Lesbian Acts: Calculating the Frequency of Homosexual Behavior

where a, b, C, D, and E represent the number of nests with 2-6 eggs respectively

—formulas used in estimating the number of female homosexual pairs in Gull populations27


While studying Kob antelopes in Uganda, scientists recorded exactly 101 homosexual mounts between females. In Costa Rica, 2 copulations between males were observed during a study of Long-tailed Hermit Hummingbirds. In which species is homosexuality more frequent? The answer would appear to be obvious: Kob. However, simply knowing the total number of homosexual acts observed in each species is not sufficient to evaluate the prevalence of homosexuality. For example, it could be that the Kob were observed for a much longer period of time than the Hummingbirds, in which case the greater number of same-sex mounts would not necessarily reflect any actual difference between the two species. What we really need is a measure of the rate of homosexual activity—that is, the number of homosexual "acts" performed during a given period of time. To determine this, we have to know the duration of the study period for each species and how many animals were being observed. In this case, 8 female Kob antelopes were studied for a total of 67 hours, whereas 36 male Long-tailed Hermit Hummingbirds were observed over several hundred hours—so indeed the Kob have a much higher rate of same-sex activity (both in general and per individual), on the order of many hundreds of times higher than the Hummingbirds.

Rate of occurrence is only one measure of frequency, however. It could be that sexual activity in general is much rarer in Hummingbirds than in Kobs, in whichcase comparing absolute numbers or rates gives a distorted or incomplete picture. A more meaningful comparison would be to look at how many heterosexual acts are performed during the same time period and express the frequency of homosexual activity as a proportion of all sexual activity. In fact, sexual activity is incredibly common among Kob and much rarer in Long-tailed Hermits: during the same study period, 1,032 heterosexual mounts among Kob were tabulated while only 6 heterosexual matings in Hummingbirds were observed. Thus, homosexual mounts constitute only 9 percent of all sexual activity among the Kob, whereas one-fourth of all copulations in Long-tailed Hermits are between males. This is diametrically opposed to the frequency rate or absolute count of homosexual activity in the same species.28

These two cases offer a good example of the many complications that arise when attempting to answer the question "How common or frequent is homosexuality in animals?" The most valid answer—clichés aside—is, "It depends." It depends not only on the measure of frequency being used, but also on the species, the behaviors being tabulated, the observation techniques that are employed, and many other factors. In this section we'll explore some of these factors and try to arrive at some meaningful generalizations about the prevalence of homosexuality in the animal kingdom.

One broad measure of frequency is the total number of species in which homosexuality occurs. Same-sex behavior (comprising courtship, sexual, pair-bonding, and parental activities) has been documented in over 450 species of animals worldwide.29 While this may seem like a lot of animals, it is in fact only a tiny fraction of the more than 1 million species that are known to exist.30 Even considering the two animal groups that are the focus of this book—mammals and birds—homosexual behavior is known to occur in roughly 300 out of a total of about 13,000 species, or just over 2 percent. However, comparing the number of species that exhibit homosexuality against all known species is probably an inaccurate measure, since only a fraction of existing species have been studied in any depth—and detailed study is usually required to uncover behaviors such as homosexuality. Scientists have estimated that at least a thousand hours of field observation are required before more unusual but important activities will become apparent in a species' behavior, and relatively few animals have received this level of scrutiny.31 Unfortunately, it is not known exactly how many species have been studied to this depth, although it has been estimated that perhaps only 1,000-2,000 have begun to be adequately described. Using these figures, the proportion of animal species exhibiting homosexual behavior comes in at 15-30 percent—a significant chunk.32

In fact, the percentage is probably even higher than this, when we consider how easy it is for common behaviors to be missed during even the most detailed of study. A caveat of any scientific endeavor, particularly biology, is that much remains to be learned and observed, and many secrets await discovery—and this is especially true where sexual behavior is concerned. Nocturnal or tree-dwelling habits, elusiveness, habitat inaccessibility, small size, and problems in identifying individual animals are just some of the factors that make field observations of sexuality inmany species exceedingly difficult.33 Consider heterosexual mating, a behavior that is known to occur in all mammals and birds (and most other animals), usually with great regularity.34 Yet in many species this activity has never been seen: "Despite literally thousands of hours of observations made by biologists over many years in the West Indies, Hawaii, and elsewhere, actual copulation in humpback whales has yet to be observed."35 Lucifer hummingbirds, northern rough-winged swallows, black-and-white warblers, red-tailed tropic birds, and several species of cranes (such as wattled and Siberian cranes) are just a handful of the birds in which heterosexual mating has never been recorded. In some cases, opposite-sex mating has been observed, but only a handful of times at most: in magnificent hummingbirds and black-headed grosbeaks, for example—the latter a common North American bird—copulation between males and females has only been seen once during the entire history of the scientific study of these species. Heterosexual copulation in Victoria's Riflebirds was not documented until the mid-1990s (and then only several times), even though the species has been known to Western science for nearly a century and a half. During a ten-year study of Cheetahs, no opposite-sex matings were seen over the course of 5,000 hours of observation, and copulation has only been observed a total of five times in the wild during the entire scientific study of this animal. Similar patterns are characteristic of other species: in the akepa (a Hawaiian finch), only five copulations were witnessed during five years of study, only five heterosexual matings were seen in a four-year study of Spotted Hyenas, and only three matings in a three-year study of Agile Wallabies. Nests and eggs of many birds such as swallows and birds of paradise have yet to be discovered, while the first nest of the marbled murrelet was found in 1959, more than 170 years after discovery of the species by Western science.

And of course new revelations about heterosexual behavior are being made all the time: female initiation of mating activity in Orang-utans, for example, was not documented until 1980 in spite of nearly 22,000 hours of observation over the preceding 20 years (and prior extensive field studies often failed to report any heterosexual copulations). As recently as 1996, the existence of polygamous trios in the tanga'eo or Mangaia kingfisher (of the Cook Islands near New Zealand) were uncovered for the first time, and the full extent of heterosexual mating by Common Chimpanzees with animals outside their group was not understood until 1997. Multiple heterosexual matings by female Harbor Seals were not verified until 1998; even then, the behavior was never directly observed during three years of study (including continuous, 24-hour videotape surveillance of captive animals over an entire breeding season), and had to be verified indirectly through DNA testing.36 If direct observation by scientists were used as the sole criterion for the existence of a behavior, we would have to conclude that many species never engage in heterosexuality (or in certain forms of heterosexuality)—yet we know this cannot be true. So the fact that homosexuality has not been seen in many animals does not necessarily mean that it is absent in those species—only that it has yet to be observed.

Ironically, many species in which heterosexuality has rarely or never been observed are ones in which homosexual activity has been recorded. No information on the heterosexual mating system of wild Emus was available prior to 1995, for example,although homosexual copulation in the same species had been observed in captivity more than 70 years earlier. Heterosexual mating has never been observed in Black-rumped Flameback Woodpeckers—although homosexual copulation has—while some studies of Nilgiri Langurs, Harbor Seals, Northern Quolls, and Gray-capped Social Weavers failed to record any instances of opposite-sex mounting, although same-sex mounting did occur. Similarly, documentation of sexual activity between male Walruses—including photographs—preceded by almost a decade comparable descriptions and photographic evidence of sexual activity between males and females. In Acorn Woodpeckers—a species that regularly engages in same-sex mounting—only 26 heterosexual copulations were recorded in over 1,400 hours of observation devoted specifically to recording opposite-sex mating. Likewise, heterosexual copulations in Australian Shelducks (a species in which females sometimes form homosexual pairs) were observed only nine times during nearly a decade of study, and on only three of these occasions was a complete behavioral sequence involved. Because of the difficulty of observing heterosexual copulation, the mating system of Killer Whales is still poorly understood and, according to one scientist, "may never be known with certainty." Homosexual activity in the same species has already been documented, although its study is also still in its infancy.37 Obviously, then, an activity can be part of the regular behavior of a species and still be completely missed by observers or documented only rarely, in spite of conscientious and in some cases exhaustive observational regimens (both in the wild and in captivity).

Scientists have often characterized homosexuality in animals as "extremely rare" or "quite common," for example, or as occuring "regularly" or "infrequently" —often without any numerical or contextual information. Yet such statements are virtually meaningless without a common standard of measurement and an agreed-upon point of reference. In an attempt to standardize the evaluation of homosexual behavior, therefore, many scientists have collected quantitative information—usually tallies of particular behaviors (sexual, courtship, pairing, etc.). In a few cases, the difficulty of field observations has precluded the direct observation of both heterosexual and homosexual activity, and several innovative techniques have been developed to calculate the frequency of same-sex activity based on indirect measures. The sex of Gulls, for example, is often difficult to determine under field conditions, and in colonies that may contain tens of thousands of breeding pairs, the task of determining which couples are homosexual and which are heterosexual is a daunting one. However, once researchers discovered that lesbian pairs typically lay supernormal clutches, the frequency of same-sex pairs could be much more easily tallied by counting the number of nests with double the usual number of eggs. One ornithologist even developed a mathematical formula (see the beginning of this section) for estimating the total number of lesbian pairs in a population based on a sample of clutch sizes, taking into account same-sex pairs that lay smaller than supernormal clutches (or heterosexual pairs that lay larger than average clutches).38 Likewise, determining the sex of mating Dragonflies can be extremely challenging while the animals are still alive, since they copulate in flight. Scientists discovered, though, that insects (both male and female) usuallysuffer head injuries from being clasped by a male during mating. These injuries can easily be recognized and counted once individual Dragonflies are collected—revealing that an average of nearly 20 percent of males in 11 different species (and more than 80 percent of males in some species) experience homosexual copulations.39

Even when quantitative information is available, assessments of frequency are often subjective and contradictory. For example, one scientist observed 24 homosexual copulations between Pukeko (7 percent of all sexual activity) and classified the behavior as "common," while another zoologist observed nearly identical numbers and proportions of same-sex mounts in Pronghorns (23 mounts, 10 percent of all mounting activity) yet classified the behavior as "rare."40 The problem is that there are many different ways of measuring and interpreting the frequency of same-sex behaviors. Besides tallying absolute numbers of particular activities or determining the proportion of all sexual activity that is homosexual, frequency rates and activity budgets can also be calculated, along with the percentage of the population that engages in same-sex activity. Frequency rate refers to the number of homosexual acts performed during a given time period, either by each individual or within a group of animals as a whole. For example, among Hanuman Langurs each female participates in a homosexual mounting, on average, once every five days, while in some populations of Ostriches courtship between males occurs at the rate of two to four times a day. An activity or time budget, on the other hand, refers to what proportion of an individual animal's activity or time is devoted to homosexual interactions. For instance, a male Killer Whale spends more than 10 percent of his time interacting socially and sexually with other males; about 15 percent of courtship display time in male Regent Bowerbirds involves displaying to other males; more than a third of some male White-handed Gibbons' time is devoted to homosexual interactions; while 10 percent of a male Crab-eating Macaque's interaction with other males involves mounting activity.41 The percentage of the population that engages in homosexual activity varies widely, from only one or two individuals in a flock of several thousand Gulls, to virtually the entire population of male Bighorn Sheep, and everything in between. Of course, some of these individuals also engage in heterosexual activity (exhibiting various degrees of bisexuality), while others are more or less exclusive in their homosexual relations; this will be discussed in more detail in chapter 2, where the question of sexual orientation is explored.

Because of the diversity and complexity of homosexual expression across a wide range of species, it is not always a straightforward matter to calculate various measures of frequency such as these. Three different species exemplify some of the issues that are involved in just one measure of frequency, the proportion of sexual activity that is homosexual. Observed versus actually occurring behaviors in Giraffes, seasonal variations in sexual activity in Mountain Sheep, and alternative standards of reference in Gray Herons complicate the calculation of homosexual frequency in each of these species. During an exhaustive study of Giraffes in the Arusha and Tarangire National Parks of Tanzania, researchers recorded 17 homosexual mounts and 1 heterosexual mount in more than a year (and 3,200 hours) ofobservation. Thus, 94 percent of all observed mounting activity was same-sex. Does this reflect the actual proportion of homosexual activity in Giraffes? Certainly more than one heterosexual mating occurred during that time, since over 20 calves were born that year in one population alone. However, these populations did have relatively low birth rates, and heterosexual mating appeared to be genuinely rare. In addition, if heterosexual matings were being missed by the observers, probably homosexual ones were as well (unless same-sex mountings consistently took place in a more visible setting than opposite-sex ones). This means that the same proportion of homosexual activity could have been involved regardless of whether some mountings were missed.42 In Mountain Sheep, there are sharp seasonal differences in the proportion of same-sex activity. During the rut (about two months out of the year), approximately a quarter of all mounts are between males; during the rest of the year, virtually all mounts are homosexual, although only a small fraction of rams' interactions with each other involves mounting.43 Thus, homosexual activity is more common during the rut if frequency rates, time budgets, or absolute numbers are tallied, but more prevalent outside the rut if proportions of sexual activity are calculated. Gray Herons, like many other birds, often engage in promiscuous copulations: males try to mate with birds, both male and female, other than their partner. One study revealed that about 8 percent of such promiscuous copulation attempts were homosexual. However, if the total number of copulations—both promiscuous and between bonded partners—is taken as the point of reference, the proportion of homosexual mounting drops to 1 percent.44 As these three examples show, differences between populations, seasons, and behaviors (among other factors) must be taken into consideration when assessing frequency.

Recognizing that measures of frequency often obscure important behavioral distinctions between (and within) species and may reflect widely divergent observational methodologies, it is nevertheless still useful to compare the prevalence of various homosexual activities across a wide variety of animals. The following summaries focus on the proportion of three behavioral categories—courtship, sexual, and pair-bonding—that occur between animals of the same sex, as well as the percentage of the population that engages in homosexual activity. These measures are the most widely available for a large number of animals, and they lend themselves fairly well to cross-species comparisons. Interestingly, similar average proportions are obtained for a number of these measures, even though they represent many different species and behaviors.45

In those animals where homosexual activity occurs, an average of about a quarter of individuals in the population (or of a given sex) engage in same-sex activity—ranging from 2-3 percent of male Ostriches and female Sage Grouse, to nearly half of all male Giraffes and Killer Whales, to entire troops of Bonobos. Concerning specific behaviors, an average of about 25 percent of courtship activity occurs between animals of the same sex in those species that exhibit homosexual courtship interactions—ranging from less than 5 percent in Herring Gulls and Calfbirds, to more than 50 percent in Dwarf Cavies and Giraffes. A nearly identical proportion of sexual activity, just over one-quarter, occurs between animals of the same sex inthose species where homosexuality has been observed—from as little as .3 percent in Silvery Grebes and 1-2 percent in Dusky Moorhens and Tasmanian Native Hens, to more than half of all sexual activity in Bison and Bonnet Macaques, and a whopping 94 percent of observed mountings in some populations of Giraffes (as mentioned above). Finally, an average of 14 percent of all pairs are homosexual in those species that have some form of same-sex (and opposite-sex) pair-bonding: ranging from as few as .3-.5 percent in Herring Gulls and Snow Geese, to more than a quarter of all consortships (on average) in Japanese Macaques, to more than half of all pair-bonds among young Galahs.

Combining these three behavioral categories yields a figure of just over 20 percent: roughly one-fifth of all interactions, on average, are homosexual in mammal and bird species that have at least some form of same-sex courtship, sexual, and/or pair-bonding activities. If one figure could be said to represent the overall frequency of homosexual activity in animals, this would probably be the one—but it is virtually impossible to come up with a truly "representative" number. A figure such as this collapses a multiplicity of behaviors (both between and within species), it represents only a fraction of the animals in which homosexuality has been documented, it glosses over many observational and theoretical uncertainties (not the least of which is widely differing sample sizes), and it misleadingly equates often radically unlike phenomena (different forms of heterosexual and homosexual behaviors, disparate social contexts, and so on). A less satisfying, but ultimately more meaningful, "formula" for understanding frequency is to recognize that there is no one overall frequency, no single formula. As in all aspects of animal homosexuality, different species exhibit an extraordinary range of rates, quantities, periodicities, and proportions of same-sex behavior—a diversity that is equal to the variation in the behaviors themselves. We can make tallies for particular species, develop formulas for certain populations or behaviors, and calculate percentages, time budgets, and so on—thereby trying to gain some overall impressions regarding the prevalence of homosexuality in animals. In the end, though, we must acknowledge that our measures are at best imperfect—and what we are attempting to quantify is, in many senses, incalculable.

Within Genders, Without Genders, Across Genders

The traditional view of the animal kingdom—what one might call the Noah's ark view—is that biology revolves around two sexes, male and female, with one of each to a pair. The range of genders and sexualities actually found in the animal world, however, is considerably richer than this. Animals with females that become males, animals with no males at all, animals that are both male and female simultaneously, animals where males resemble females, animals where females court other females and males court other males—Noah's ark was never quite like this! Homosexuality represents but one of a wide variety of alternative sexualities and genders. Many people are familiar with transvestism or transsexuality only in humans, yet similar phenomena are also found in the animal kingdom. Although this book focuses primarily on homosexuality, it is helpful to compare this with relatedphenomena that are often confused with homosexuality, and to discuss some specific examples of each.

Many animals live without two distinct genders, or with multiple genders. In hermaphrodite species, for instance, all individuals are both male and female simultaneously, and hence there are not really two separate sexes; in parthenogenetic species, all individuals are female and they reproduce by virgin birth. A number of other phenomena in the animal kingdom—for which we will use the cover term transgender—involve the crossing or traversing of existing gender categories: for example, transvestism (imitating the opposite sex, either behaviorally, visually, or chemically), transsexuality (physically becoming the opposite sex), and intersexuality (combining physical characteristics of both sexes).46

Early descriptions of animal homosexuality often mistakenly called the animals "hermaphrodites," since any "transgression" of gender categories (such as sexual behavior) was usually equated with physical gender-mixing. True hermaphroditism, however, involves animals that have both male and female reproductive organs at the same time. This phenomenon is found in many invertebrate organisms, such as slugs and worms, as well as in a number of fish species (for example, lantern fishes and some species of hamlets and deep-sea fishes). Some hermaphrodites can fertilize themselves, but mating in many hermaphroditic species involves two individuals having sex with each other in order to mutually exchange both eggs and sperm.47 Since both such individuals have identical biologies, i.e., are of the same (dual) sex, technically such behavior could be classified as homosexual. However, such activity differs from actual homosexuality because it occurs in a species that does not have two separate sexes, and because it typically does result in procreation. In species that do have two distinct sexes, there are other types of hermaphroditism or intersexuality, in which individuals combine various physical features of both sexes. These differ from species-wide, true hermaphroditism because such animals are not able to reproduce as both males and females simultaneously, and they usually comprise only a fraction of the otherwise nonhermaphroditic population. Further examples of this type of transgender will be discussed in chapter 6.

Virgin birth, or parthenogenesis, is not just the stuff of religions: it is actually found in over a thousand species worldwide and is a "natural" form of cloning. Each member of a parthenogenetic species is biologically female (that is, capable of producing eggs). Rather than requiring sperm to fertilize these eggs, however, she simply makes an exact copy of her own genetic code. Virgin birth is found in a number of fishes, lizards, insects, and other invertebrates. In most parthenogenetic species, individuals do not have sex with each other, but in some species, such as the Amazon Molly and Whiptail Lizards, females actually court and mate with one another, even though no eggs (or sperm) are exchanged in such encounters.

Whereas homosexuality and bisexuality involve activity within the same gender, hermaphroditism and parthenogenesis involve courtship and sexual behavior without genders (at least, without one class of individuals that are male and another class that are female). In contrast, transvestism and transsexuality are a kind of "crossing over" from one gender or sexual category to another, or the combining of elements from each category. In transvestism, individuals of one biological sex takeon the characteristics of the other sex, either behaviorally or physically, without actually changing their own sex. In transsexuality, individuals actually become the opposite sex, so that a male turns into a female or vice versa (where male and female are used strictly in the reproductive sense to refer to animals that produce sperm or eggs, respectively).

Transvestism is widespread in the animal kingdom and takes a variety of forms.48 Both male-to-female and female-to-male transvestism occur: some female African swallowtail butterflies, for example, resemble males in their wing coloration and patterning, while in some species of squid, males imitate female arm postures during aggressive encounters.49 Physical transvestism can involve almost total physical resemblance between males and females, or mimicry of only certain primary or secondary sexual characteristics. For instance, in several species of North American perching birds, young males resemble adult females in their plumage—making them distinct from both adult males and juvenile females. In some birds, such as the painted bunting, the resemblance between adult females and juvenile males is nearly total, while in others, younger males are more intermediate between adult males and females in appearance.50 Several species of hoofed mammals show a different type of physical transvestism: female mimicry of the horns or tusks found in males.51 Female Chinese water deer, for example, grow special tufts of hairs on their jaws that resemble the tusks of the male, while female Musk-oxen have a patch of hair on their foreheads that mimics the males' horn shield. Physical transvestism can also be chemical or scent-based: some male Common Garter Snakes, for example, produce a scent that resembles the female pheromone, causing males to mistake them for females and attempt to court and mate with them.

In behavioral transvestism, an animal of one sex acts in a way that is characteristic of members of the opposite sex of that species—often fooling other members of their own species. For example, males of several species of terns imitate female food-begging gestures to steal food from other males. Behavioral transvestism does not mean animals behaving in ways that are thought to be "typically" male or female in other species. In sea horses and pipefishes, for instance, the male bears and gives birth to the young. Even though these are activities usually thought to be "female," this is not a genuine case of transvestism because it is part of the regular behavior patterns and biology of the species (i.e., it is true for all males and no females). Female sea horses never bear young, nor are they fooled into thinking that males aren't male because they do bear young. The same goes for initiation of courtship: in some species the female is more aggressive in initiating courtship and copulation (e.g., in greater painted-snipes), yet this could only be considered "transvestism" with reference to other species in which females do not initiate such activity.52

The question of transvestism is an important one for animal homosexuality because these two phenomena have often been confused. Many scientists have labeled all examples of animal homosexuality male or female "mimicry" since they consider any same-sex behavior to be nothing more than imitation of the opposite sex. True, many animals, when courting and mating homosexually, employ behavior patterns that the opposite sex also employs. In most cases, however, this simply involvesmaking use of the available behavioral repertoire of the species rather than being an attempt to mimic the opposite sex. Moreover, the resemblance to "heterosexual" patterns is often partial at best, while in some species entirely distinct courtship and copulation patterns are used for homosexual activity.53

A good example of the difference between behavioral transvestism and homosexuality is in the Bighorn Sheep. In this species, males and females lead almost entirely separate lives: they live in sex-segregated herds for most of the year and come together for only a few short months during the breeding season. Among males, homosexual mounting is common, while females do not generally permit themselves to be mounted by males except when they are in heat (estrus). A small percentage of males, however, are behavioral transvestites: they remain in the female herds year-round and also mimic female behavior patterns. Significantly, such males also generally refuse to allow other males to mount them, just the way females do. Thus, among Bighorn Sheep, being mounted by a male is a typically "masculine" activity, while refusal of such mounting is a typically "feminine" behavior. Males who mimic females specifically avoid homosexuality. This is the exact opposite of the stereotypical view of male homosexuality, which is often considered to be a case of males "imitating" females. It is also a striking reminder of how important it is not to be misled by our preconceptions about human homosexuality when looking at animals.54

Transsexuality or sex change is a routine aspect of many animals' lives, especially in invertebrates: shrimp, oysters, and sow bugs, for example, all undergo complete reversals of their sex at some stage in their lives.55 It is among coral-reef fish, however, that the most remarkable examples of transsexuality are found. More than 50 species of parrot fishes, wrasses, groupers, angelfishes, and other species are transsexual. In all such cases, the reproductive organs of the fish undergo a complete reversal. What were once fully functional ovaries, for example, become fully functional testes, and the formerly female fish is able to mate and reproduce as a male.56

The types of sex change that are found, the number and fluidity of genders, and the overall social organization of these species are so complex that a detailed terminology has been developed by scientists to describe all the variations. In some species, females turn into males (this is called protogynous sex change), while in others males become females (called protandrous sex change). In some fish, sex change is maturational; that is, it happens automatically to all individuals when they reach a certain age or size or else occurs spontaneously at different times for each individual. In other species, sex change appears to be triggered by factors in the social environment of the fish, such as the size, sex, or number of neighboring fish. In female-to-male fish species, many different gender profiles are found. In some cases, all fish are born female, and males result only from sex change (such a system is called monandric). In other cases, both genetic males (born male) and sex-changed males are found (this arrangement is called diandric). In these fishes, genetic males are sometimes referred to as primary males while sex-changed males are called secondary males. Often these two types of males differ in their coloration, behavior, and social organization so that transsexual males form a distinct and clearly visible "gender" in the population.

Things get even more complicated in some species. Among secondary males, some change sex before they mature as females (prematurational secondary males), while others change sex only after they live part of their adult life as females (post-maturational secondary males). Many species also have two distinct color phases: fish often begin life with a dull color and drab patterning, then change into the more brilliant hues typically associated with tropical fish as they get older. Which individuals change color, when they change, and their gender at the time of the color change can yield further variations. Many species of parrot fishes, for example, have multiple "genders" or categories of individuals based on these distinctions. In fact, in some families of fishes, transsexuality is so much the norm that biologists have coined a term to refer to those "unusual" species that don't change sex—gonochoristic animals are those with two distinct sexes in which males always remain male and females always remain female.

As an example of how elaborate transsexuality can become in coral-reef fish, consider the striped parrot fish, a medium-sized species native to Caribbean and Atlantic waters from Bermuda to Brazil (the name refers to the fact that its teeth are fused together like a parrot's beak).57 Striped parrot fish, like many sex-changing fishes, have both males that were born as males and males that were born as females. In fact, more than half of all males in this species used to be females. Moreover, all female striped parrot fish eventually change their sex, becoming male once they reach a certain size; the sex change can take as little as ten days to be completed. Sex-changed males have fully functional testes that used to be fully functional ovaries when the fish was female; they are able to mate and fertilize eggs the same way that genetic males do. Striped parrot fish have one of the most complex polygendered societies in the animal kingdom. There are five distinct genders, distinguished by biological sex, genetic origin, and color phase. Biological sex refers to whether the fish has ovaries (= female) or testes (= male). Genetic origin refers to whether the fish was born that sex or has changed from another sex (= transsexual). Color phase refers to the two types of coloration that striped parrot fish exhibit: initial-phase fish (so named because all fish start out with this coloration) are a drabber brown or bluish gray, while terminal-phase fish are a brilliant blue-green and orange. These three categories intersect to create the following five genders(percentages refer to what proportion of the total population, at any given time, belongs to each gender): (1) genetic females: born female, each of these initial-phase fish will eventually become a male and change color (45 percent); (2) initial-phase transsexual males: born female, these fish become male before they change into their bright colors and are fairly rare (1 percent); (3) terminal-phase transsexual males: born female, these fish become male at the same time they changed color, usually at a later age than genetic males (27 percent); (4) initial-phase genetic males: born male, most of these will change color as they get older (but won't change sex) (14 percent); and (5) terminal-phase genetic males: born male, these fish start out as initial-phase males and change color (but not sex) at a younger age than transsexual males (13 percent).

Along with its numerous genders and fluid changes between them, striped parrot fish society is characterized by a number of intricate systems of social organization and mating patterns, each found in a particular geographic area. One system, known as group spawning or explosive breeding assemblages, is common in Jamaican striped parrot fish. Large groups of up to 20 initial-phase males and females gather to spawn together, swimming in dramatic formations that rapidly change direction. Often, terminal-phase males try to disrupt this mating activity. Another system is found in the waters off Panama and is known as haremic because the basic breeding group consists of one terminal-phase male and several females. These individuals are known as territorials since they live in permanent locations that they defend against intruders. Other fish in the same area, however, associate with each other in different kinds of groups: "stationaries" are celibate (nonbreeding) fish in both initial and terminal phases, while "foragers" gather together to feed in large groups of up to 500 fish. Some of these foraging groups are composed of females and initial-phase genetic males, while others are made up only of terminal-phase males; half of all the females, and all the males, in such groups are nonbreeders. Finally, striped parrot fish in the waters off Puerto Rico and the Virgin Islands associate together in "leks," clusters of small, temporary territories that both initial-phase and terminal-phase males defend and use to attract females for spawning.

Further variations in transsexuality are found in other species. The paketi or spotty, a New Zealand fish, combines transsexuality with transvestism (some females become males before changing color, thus "masquerading" as females), while the humbug damselfish combines transsexuality with same-sex pairings and associations. An even more complex gender system, involving hermaphroditism, transsexuality, transvestism, and apparent homosexual activities, exists in the lantern bass and other fishes. In addition to nontranssexual males and females, some individuals are hermaphrodites (both male and female at the same time) and others are secondary (transsexual) males, while in a few cases individuals exhibit courtship and mating patterns typical of the opposite sex (directed toward individuals of the same sex). All female Red Sea anemonefish start out as males; once they change sex, however, they become dominant to males and tend "harems" of up to nine males, all but one of whom are nonbreeders. Finally, although most transsexual fishes are one-way sex changers, in a few species sex change actually occurs in both directions. In the coral goby, for instance, some individuals go from male to female,others from female to male, and some even undergo multiple sequential changes, "back and forth" from male to female to male, or female to male to female.58


As these examples show, not only are transgendered and genderless biologies a fact of life for many animals, they have developed into incredibly sophisticated and complex systems of social organization and behavioral patterning in many species. For those of us used to thinking in terms of two unchanging and wholly separate sexes, this is extraordinary news indeed. Likewise, animal homosexuality itself is a rich and multifaceted phenomenon that is at least as complex and varied as heterosexuality Animals of the same sex court each other with an assortment of special—and in some cases, unique—behavior patterns. They are both affectionate and sexual toward one another, utilizing multiple forms of touch and sexual technique, ranging from kissing and grooming to cunnilingus and anal intercourse. And they form pair-bonds of several different types and durations and even raise young in an assortment of same-sex family configurations. If, as scientist J. B. S. Haldane stated, the natural world is queerer than we can ever know, then it is also true that the lives of "queer" animals are far more diverse than we could ever have imagined. In the next chapter, we'll take a look at how these different forms of sexual and gender expression in animals compare to similar phenomena in people.

BIOLOGICAL EXUBERANCE:ANIMAL HOMOSEXUALITY AND NATURAL DIVERSITY. Copyright © 1999 by Bruce Bagemihl. All rights reserved. No part of this book may be used or reproduced in any manner whatsoever without written permission except in the case of brief quotations embodied in critical articles or reviews. For information, address St. Martin's Press, 175 Fifth Avenue, New York, N.Y 10010.

Table of Contents

Acknowledgments xiii
Introduction 1(8)
Part I A Polysexual, Polygendered World
The Birds and the Bees
The Many Forms of Animal Homosexuality
What's Good for the Goose...: Comparisons of Male and Female Homosexuality
A Hundred and One Lesbian Acts: Calculating the Frequency of Homosexual Behavior
Within Genders, Without Genders, Across Genders
Humanistic Animals, Animalistic Humans
From Pederasty to Butch-Femme: Uniquely Human?
Primate (Homo) Sexuality and the Origins of Culture
Unnatural Nature
Two Hundred Years of Looking at Homosexual Wildlife
A Brief History of the Study of Animal Homosexuality
"A Lowering of Moral Standards Among Butterflies": Homophobia in Zoology
Anything but Sex
Explaining (Away) Animal Homosexuality
"Which One Plays the Female Role?"---Homosexuality as Pseudoheterosexuality
"The Lengths to Which Deprived Creatures Will Go"---Homosexuality as Substitute Heterosexuality
"The Errors of Their Ways"---Homosexuality as Mistaken Sex Identification
"Gross Abnormalities of Behavior"---Homosexuality as Pathology
Not for Breeding Only: Reproduction on the Periphery of Life
The Evolutionary "Value" of Homosexuality
Homosexuality in the Service of Heterosexuality
Nonreproductive and Alternative Heterosexualities in Animals
A New Paradigm: Biological Exuberance
Left-Handed Bears and Androgynous Cassowaries: Informing Biology with Indigenous Knowledge
A Revolution Under Way: Contemporary Scientific and Philosophical Perpectives
Returning to the Source: Indigenous Cosmologies and Fractal Sexualities
The Magnificent Overabundance of Reality
Part II A Wondrous Bestiary
Portraits of Homosexual, Bisexual, and Transgendered Wildlife
Langurs and Leaf Monkeys
Other Primates
Marine Mammals
Dolphins and Whales
Seals and Manatees
Hoofed Mammals
Giraffes, Antelopes, and Gazelles
Wild Sheep, Goats, and Buffalo
Other Hoofed Mammals
Other Mammals
Rodents, Insectivores, and Bats
Waterfowl and Other Aquatic Birds
Geese, Swans, and Ducks
Other Aquatic Birds
Wading Birds
Shore Birds
Sandpipers and Their Relatives
Gulls and Terns
Perching Birds and Songbirds
Cotingas, Manakins, and Others
Swallows, Warblers, Finches, and Others
Sparrows, Blackbirds, and Crows
Birds of Paradise, Bowerbirds, and Others
Other Birds
Flightless Birds
Birds of Prey and Game Birds
Hummingbirds, Woodpeckers, and Others
Appendix: Other Species 657(14)
Notes to Part I 671(62)
Credits and Permissions 733(4)
Animal Index 737(6)
Subject Index 743

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