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Chapter 4. Explaining (Away) Animal Homosexuality
1
M. Grober, opening remarks to the plenary session on Sexual Orientation, 24th International Ethological Conference, Honolulu, Hawaii, August 12, 1995.
2
Among the attendees who had previously documented or written extensively on animal homosexual behavior, but who were not speaking on this topic, were B. Le Boeuf (Northern Elephant Seals), C. Clark (Right Whales), W. D. Koenig (Acorn Woodpeckers), M. Moynihan (Rufous-naped Tamarins, Pied Kingfishers, Blue-bellied Rollers), A. Srivastava (Hanuman Langurs), F. B. M. de Waal (Bonobos, other primates), and J. C. Wingfield (Gulls). A number of other disconcerting trends were also in evidence among the papers presented during this symposium: for example, many were based on studies of laboratory or captive animals to the exclusion of information on homosexuality/transgender in wild animals. One presenter (Ulibarri) actually went so far as to state that no information was available in English on any behavior of wild Mongolian gerbils, when in fact at least one such study had been published several years earlier in a prominent zoology journal (Ulibarri, C. [1995] "Gonadal Steroid Regulation of Differentiation of Neuroanatomical Structures Underlying Sexual Dimorphic Behavior in Gerbils," paper presented at the 24th International Ethological Conference, Honolulu, Hawaii; Agren, G., Q. Zhou, and W. Zhong [1989] "Ecology and Social Behavior of Mongolian Gerbils, Meriones unguiculatus, at Xilinhot, Inner Mongolia, China," Animal Behavior 37:11-27).
3
Caprio, F. S. (1954) Female Homosexuality, pp. 19, 76 (New York: Grove); Northern Fur Seal (Bartholomew 1959:168).
4
This idea appears in the descriptions of homosexuality in more than 40 different species of mammals and birds.
5
Homosexuality and related phenomena in animals have even been labeled "heterotypical behavior" (cf. Haug, M., P. F. Brain, and C. Aron, eds., [1991] Heterotypical Behavior in Man and Animals [New York: Chapman and Hall]). The intended meaning of this term is that the behavior of at least one of the partners during same-sex interactions is supposedly "typical" of participants in heterosexual activity, but transposed onto a same-sex context — in other words homosexuality is simply recast as a modified version of heterosexuality.
6
Orange-fronted/Aztec Parakeets (Hardy 1966:77, 1963:171). In a related vein, the vocal and sexual responses of female Stumptail Macaques during orgasm were studied primarily in homosexual, rather than heterosexual, interactions; this information was then generalized or extrapolated to opposite-sex contexts (cf. Goldfoot et al. 1980; Leinonen et al. 1991:245). Likewise, the synchronization of pair-bonding activities in Galahs was typified in one study with quantitative information from same-sex rather than opposite-sex pairs (Rogers and McCulloch 1981:87).
7
Freud, S. (1905/1961) Drei Abhandlungen zur Sexualtheorie (Frankfurt: Fischer); see also Ellis, H. (1936) Sexual Inversion: Studies in the Psychology of Sex (New York: Random House).
8
Morris 1954 (Zebra Finch); Morris 1952 (Ten-spined Stickleback). For a more recent article, see Schlupp et al. 1992 (Amazon Molly). See also Lorenz 1972:21 (Raven) for an early (errroneous) statement to the effect that during same-sex interactions animals only exhibit "purely" masculine or feminine behaviors (as defined by a heterosexual context) rather than any intermediate forms.
9
Takhi (Boyd 1986:661); Mallard Duck (Ramsay 1956:277); Snow Goose (Starkey 1972). Another notable example of the conflation of "inverted" gender traits (and other "deviant" characteristics) with playing the "opposite-sex" role in homosexual interactions involves the Common Chimpanzee. A female Chimp that was apparently exclusively lesbian for many years (and consorted with otherwise "heterosexual" females) was described by a scientist — in addition to being sexually "aberrant" — as having a "burly manner," being "masculine-looking," "two-faced and mean," "malevolent," and "deceitful." Comments from untrained observers that compared her to a witch were also repeated without qualification (de Waal 1982:64-65). While some of these traits may have reflected genuine aspects of her physical appearance, behavior, and personality, it is striking how loaded and anthropomorphic these descriptions are, and how many of the characteristics singled out for mention correspond precisely to the negative and distorted stereotypes of "butch" lesbians among humans. Moreover, in many animals, (heterosexual) females may display greater levels of aggression when they are in "heat" — one scientist even described female Chimpanzees as being "masculinized" by the onset of their estrus (Nishida 1979:103). Aside from being inappropriate in specific cases, then, it is inaccurate to ascribe greater aggression solely to "malelike" females in homosexual contexts when this may in fact be an independent feature of female sexual arousal. In addition, a recent comprehensive survey of over 700 mammal species found no correlation between the occurrence of "masculinized" female genitalia {697}
and female aggression or dominance (Teltscher, C., H. Hofer, and M. L. East [1997] "Virilized Genitalia are Not Required for the Evolution of Female Dominance," in M. Taborsky and B. Taborsky, eds., Contributions to the XXV International Ethological Conference, p. 281, Advances in Ethology no. 32. [Berlin: Blackwell Wissenschafts-Verlag]). Incidentally, the female Chimpanzee referred to above was also nicknamed "the Madam" because of her apparent regulation of the sexual activity of other females, echoing an earlier nicknaming of an intersexual Savanna Baboon as "the Prostitute" (Marais 1922/1969:205-6). These examples offer striking parallels to the association, among humans, of female homosexuality/gender variance with prostitution. Both are seen as "deviant" activities and are linked not only in the mythic and popular imagination, but also sometimes in actual historical and social realities (cf. Nestle, J. [1987] "Lesbians and Prostitutes: A Historical Sisterhood," in A Restricted Country, pp. 157-77 [Ithaca: Firebrand Books]; Salessi, J. [1997] "Medics, Crooks, and Tango Queens: The National Appropriation of a Gay Tango," pp. 151, 161-62, in C. F. Delgado and J. E. Munoz, eds., Everynight Life: Culture and Dance in Latin/o America, pp. 141-74 [Durham: Duke University Press]).
10
Although many zoologists have uncritically advocated such an "explanation" or interpretation of homosexuality, a few scientists have presented explicit arguments against such an analysis: Wolfe 1979:532, Lunardini 1989:183 (Japanese Macaque); Srivastava et al. 1991:506-7 (Hanuman Langur); Huber and Martys 1993:160 (Greylag Goose); Hunt et al. 1984 (Western Gull); Rogers and McCulloch 1981:90 (Galah).
11
This is especially true for "penis fencing" between male Bonobos, less so for mutual genital rubbing between females in this species. The latter usually involves one female "mounting" or embracing the other in a face-to-face position, hence it could be analogized with positions used in heterosexual interactions.
12
Even in some of these cases, however, a "pseudoheterosexual" framework has been imposed on the behavior. Mutual rump rubbing, in which two animals back up toward each other and rub their anal and genital regions together, has been interpreted as both animals adopting a "female" heterosexual invitation-to-mate posture in some species (e.g., Bonobos [Kitamura 1989:56-57]; Stumptail Macaques [Chevalier-Skolnikoff 1976:518]). This ignores the fact that both participants often actively rub their rumps together and make pelvic thrusts rather than simply passively presenting their hindquarters, and the two animals may also simultaneously fondle and stimulate each other's genitals with their hands — clearly making this a distinct sexual activity rather than simply a version of a heterosexual practice or posture.
13
Bottlenose Dolphin (Ostman 1991). For more on reverse heterosexual mounting, see chapter 5 and the species profiles in part 2.
14
See, for example, Huber and Martys (1993:160) for explicit refutation of the idea that one member of a Greylag gander pair adopts a "pseudofemale" role.
15
This is true, for example, in Mallard Ducks, Black-crowned Night Herons, Black-headed Gulls, Emus, and Jackdaws.
16
Red Deer (based on table 2, Hall 1983:278).
17
Byne, W. (1994) "The Biological Evidence Challenged," p. 53, Scientific American 270(5):50-55.
18
Northern jacana (del Hoyo, J., A. Elliott, and J. Sargatal, eds. [1996] Handbook of the Birds of the World, vol. 3, Hoatzin to Auks, p. 282 [Barcelona: Lynx Edicions]); arctic tern and other species (Weldon, P. J., and G. M. Burghardt [1984] "Deception Divergence and Sexual Selection," Zeitschrift fur Tierpsychologie 65:89-102, especially table 1).
19
Mountain Zebra (Penzhorn 1984:119); Chaffinch (Marler 1956:69, 96-97, 119) (Marler misleadingly labels some cases of opposite-sex mimicry as "homosexual behavior" while noting explicitly that no same-sex mounting occurs in these contexts); Rufous-naped Tamarin (Moynihan 1970:48, 50); Black-crowned Night Heron (Noble and Wurm 1942:216); Kittiwake (Paludan 1955:16-17); Koala (Smith 1980:49). Two species in which opposite-sex mimicry does appear to be a component of at least some homosexual interactions are Buff-breasted Sandpipers and Ocher-bellied Flycatchers.
20
Northern Elephant Seal (Le Boeuf 1974:173); Black-headed Gull (van Rhijn 1985:87, 100); Red Deer (Darling 1937:170); Common Garter Snake (Mason and Crews 1985:59). Researchers have also found that transvestite paketi (a fish species) have huge testes that are about five times larger than that of nontransvestite males and are thus able to fertilize more eggs (Ayling, T. [1982] Sea Fishes of New Zealand, p. 255 [Auckland: Collins]; Jones, G. P. [1980] "Growth and Reproduction in the Protogynous Hermaphrodite Pseudolabrus celidotus [Pisces: Labridae] in New Zealand," Copeia 1980:660-75).
21
Tasmanian Native Hen (Ridpath 1972:30); Rhesus Macaque (Akers and Conaway 1979:76). On a related point, male Laysan Albatrosses may be stimulated to mount birds of either sex when the latter happen to assume a posture that resembles a female's invitation to mate (typically involving drooping and spread wings) — to the extent that if only a bird's right wing is drooping, for example, males on the bird's right side will attempt to mount while those on the left will not. However, this "triggering" effect can only be a partial explanation, since males do not generally try to mount females who are sitting on a nest, even though the posture and drooping wings of such birds greatly resemble the mating invitation. Researchers studying this species (e.g., Fisher 1971:45-46) have expressed puzzlement over the apparent failure of the triggering effect in this context, suggesting that perhaps the height of the incubating females (nests in this species are six to eight inches high) is an inhibiting factor. This is not consistent, however, with the fact that males sometimes mount even taller "stacks" of up to three other males that are simultaneously mounting one another. Similarly, scientists once observed a Red Deer stag mount another male whose posture, as it was beginning to undergo the effects of a tranquilizer, supposedly "resembled" a female's (Lincoln et al. 1970:101; cf. Klingel [1990:578] for a similar observation concerning anesthetized Plains Zebra stallions). Consequently, they attributed the homosexual behavior to the "triggering" effect of the supposedly femalelike visual cues presented by the other animal. Aside from the fact that the resemblance between a female Red Deer ready to mate and a drugged male is questionable, same-sex mounting in this species occurs commonly in contexts that have nothing to do with opposite-sex "resemblance" (cf. Hall 1983, Guiness et al. 1971; the same holds for Zebras).
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22
Bighorn Sheep (Berger 1985:334; Geist 1971:161-63, 185, 219). Another possible case of heterosexual interactions being modeled on homosexual ones occurs in Atlantic Spotted Dolphins: during heterosexual copulations some individuals have been observed apparently "mimicking" the sideways mounting position used during interspecies homosexual copulations with Bottlenose Dolphins (Herzing and Johnson 1997:96). Interestingly, the patterning of heterosexual relations after homosexual ones is also found in some human cultures. In medieval Baghdad and Andalusia, for example, the preeminence of (largely intergenerational) homosexual relations was such that heterosexual women often cross-dressed as male youths — sometimes even with painted mustaches — in order to compete with boys for the attentions of men (Murray and Roscoe, Islamic Homosexualities, pp. 99, 151). In contemporary North America, some men cross-dress as women when having sex with their wives/girlfriends because they enjoy imagining themselves as a lesbian couple, or they become transsexual/transgendered women and live with their female partners in a lesbian relationship (see, for example, Money, J. [1988] Gay, Straight, and In-Between: The Sexology of Erotic Orientation, pp. 105-6 [New York: Oxford University Press]; Bolin, A. [1994] "Transcending and Transgendering: Male-to-Female Transsexuals, Dichotomy and Diversity," p. 484, in G. Herdt, ed., Third Sex, Third Gender: Beyond Sexual Dimorphism in Culture and History, pp. 447-85 [New York: Zone Books]; Rothblatt, M. [1995] The Apartheid of Sex: A Manifesto on the Freedom of Gender, pp. 159-60 [New York: Crown]).
23
This is to some extent an arbitrary classification, since these three "types" may overlap with each other or even co-occur to varying degrees within the same species or individual. Nevertheless, they represent broad patterns that are a useful point of departure for discussion.
24
In the words of the scientists studing this species, "Female sexual displays formed a continuum from male-behaving females to normal females" (Buechner and Schloeth 1965:219).
25
Gorilla (Yamagiwa 1987a:13 [table 7], 1987b:36-37 [table 4]); Hanuman Langur (Srivastava et al. 1991:492 — 93 [table II]); Bonnet Macaque (Sugiyama 1971:260 [table 9]); Pig-tailed Macaque (Tokuda et al. 1968:291 [table 7]).
26
Western Gull (Hunt et al. 1984).
27
On the rarity of incubation feeding in male-female pairs, see Evans Ogden and Stutchbury 1994:8.
28
Some cases of apparently role-differentiated behavior are not so clearly gendered when examined in more detail. Kitagawa (1988a:65-66) suggests that females in homosexual pairs of Black-winged Stilts can be divided into "malelike" and "femalelike" partners. However, many of the courtship and pair-bonding behaviors that are used to make this distinction, such as "splashing water" or "irrelevant preening," are described by other sources (e.g., Goriup 1982; Hamilton 1975) as being performed by both sexes in heterosexual pairs. Even if we accept Kitagawa's classification of some behaviors as more typical of males or females, though, in at least one of the homosexual pairs described, it is difficult to see how this translates into gendered behavior. Both partners in this case performed putatively female activities such as "extending neck" and egg laying, putatively male behaviors such as "half-circling round," and putatively nongendered activities such as "showing nest spot" and incubation.
29
This behavior is exhibited by females when initiating pair-directed courtships, and by males when pursuing promiscuous matings (cf. Coddington and Cockburn 1995).
30
Swallow-tailed Manakin (Foster 1987:555; Sick 1967:17, 1959:286).
31
On the role differentiation of these parental duties in heterosexual pairs, see Martin et al. 1985:258.
32
Black-headed Gull (based on figs. 3-6, van Rhijn 1985:92-94). These comparisons are drawn from studies of captive birds; however, the behavior of wild Gulls appears to be similar — in a homosexual pair observed in the wild by Kharitonov and Zubakin (1984:103), for example, at least one partner exhibited a combination of both "male" and "female" behaviors.
33
For more extensive discussion of the full complexity and diversity of lesbian butch-femme, see Nestle, J. (1981) "Butch-Fem Relationships: Sexual Courage in the 1950's," Heresies No. 12, 3(4):21-24; Nestle, J., ed. (1992) The Persistent Desire: A Femme-Butch Reader (Boston: Alyson); Burana, L., Roxxie, and L. Due, eds. (1994) Dagger: On Butch Women (Pittsburgh and San Francisco: Cleis Press); Newman, L. (1995) The Femme Mystique (Boston: Alyson); Pratt, M. B. (1995) S/HE (Ithaca: Firebrand Books); Harris, L., and E. Crocker, eds. (1997) Femme: Feminists, Lesbians, and Bad Girls (New York: Routledge).
34
Australian Shelduck (Riggert 1977:60-61); Ring-billed Gull (Conover and Hunt 1984a); Mute Swan (Kear 1972:85-86); Mountain Sheep (Geist 1971:162); Bottlenose Dolphin (Tavolga 1966:729-30); Killer Whale (Rose 1992:112); White-handed Gibbon (Edwards and Todd 1991:234); West Indian Manatee (Hartman 1979:107-8); Hanuman Langur (Srivastava et al. 1991:508-9); Asiatic Elephant (Ramachandran 1984); Lion (Chavan 1981); Sage Grouse (Scott 1942:488).
35
For explicit rejection of (and evidence against) the shortage hypothesis by various zoologists studying animal homosexuality, see Gorilla (Harcourt et al. 1981:276); Japanese Macaque (Fedigan and Gouzoules 1978:494; Vasey 1996:550, 1998:17); Rhesus Macaque (Akers and Conaway 1979:77); Flamingo (King 1994:107); Common Gull (Riddiford 1995:112); Jackdaw (Roell 1978:103); Galah (Rogers and McCulloch 1981:90; Rowley 1990:59-60).
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36
Orang-utan (Rijksen 1978:259); Japanese Macaque (Vasey 1996 and personal communication; Corradino 1990:360; Wolfe 1984); Stumptail Macaque (Chevalier-Skolikoff 1976:520); Rhesus Macaque (Akers and Conaway 1979:76-77); Common Gull (Riddiford 1995:112); Black-headed Gull (van Rhijn 1985:91-93); King Penguin (Murphy 1936:340-41); Galah (Rogers and McCulloch 1981:90; Rowley 1990:59-60).
37
Bottlenose Dolphin (Ostman 1991:310); Squirrel Monkey (Mendoza and Mason 1991:476-77; Travis and Holmes 1974:55, 63); Bonobo (Kano 1992:149; Savage-Rumbaugh and Wilkerson 1979:338); Stumptail Macaque (Chevalier-Skolikoff 1976:524); Savanna (Yellow) Baboon (Maxim and Buettner-Janusch 1963:176); West Indian Manatee (Hartman 1979:101, 106); Pukeko (Jamieson and Craig 1987a:1251); Common Murre (Birkhead et al. 1985:614); Sociable Weaver (Collias and Collias 1980b:248); Bonnet Macaque (Sugiyama 1971:252, 259-60); Japanese Macaque (Vasey 1996:543 and personal communication). Homosexual mounting rates can also be independent of the presence of animals of the opposite sex: in an all-female group of Pig-tailed Macaques, for example, the rate of same-sex mounting was virtually identical both before and after introduction of a male into the group (Giacoma and Messeri 1992:183 [table I]). The finding of a positive correlation between homosexual and heterosexual rates is paralleled by some data on humans in sex-segregated environments. Researchers found that married men in prisons who receive conjugal visits with their wives are actually more likely to have sex with other male prisoners than men without conjugal visits (Wooden, W. S., and J. Parker [1982] Men Behind Bars: Sexual Exploitation in Prison, pp. 55-56 [New York: Plenum]).
38
For species with skewed sex ratios but no homosexuality, see Welty, J. C., and L. Baptista (1988) The Life of Birds, 4th ed., p. 154 (New York: W. B. Saunders); Newton, I. (1986) The Sparrowhawk, pp. 37, 151 (Calton, England: T. and A. D. Poyser); Taborsky, B., and M. Taborsky (1991) "Social Organization of North Island Brown Kiwi: Long-Term Pairs and Three Types of Male Spacing Behavior," Ethology 89:47-62. For verification of balanced sex ratios in populations exhibiting homosexuality, see Bonobo (Thompson-Handler et al. 1984:349); Bonnet Macaque (Simonds 1965); West Indian Manatee (Hartman 1979:139); Snow Goose (Quinn et al. 1989:184); California Gull (Conover et al. 1979); Pukeko (Craig 1980:594).
39
For sex ratios of various Seals and Sea Lions, see Fay 1982:256 (Walrus); for lunulated and salvin's antbirds, see Willis, E. O. (1968) "Studies of the Behavior of Lunulated and Salvin's Antbirds," Condor 70:128-48; for other antbird species with a "surplus" of unmated males but no homosexual pairs, see Willis, E. O. (1969) "On the Behavior of Five Species of Rhegmatorhina, Ant-Following Antbirds of the Amazon Basin," Wilson Bulletin 81:363-95.
40
Crab-eating Macaque (Poirier and Smith 1974); Pukeko (Craig 1980:594); Rhesus Macaque (Lindburg 1971:14, 69); Tree Swallow (Stutchbury and Robertson 1985, 1987b); Galah (Rogers and McCulloch 1981:90); Scarlet Ibis (Elbin and Lyles 1994:90-91); Flamingo (King 1994:104-5); Nilgiri Langur (Hohmann 1989:449); Little Egret (M. Fujioka, personal communication); Little Blue Heron (Werschkul 1982:382).
41
Black Stilt (Reed 1993:772); Humboldt Penguin (Scholten 1992:6 and personal communication); Savanna (Yellow) Baboon (Rowell 1967a:16, 22-23 [tables 2, 3]); Mallard Duck (Lebret 1961:108 [table I]).
42
Pig-tailed Macaque (Oi 1990a:340); Bottlenose Dolphin (Wells 1991:222); Cheetah (Eaton and Craig 1973:252); Koala (Smith 1980:184); Canada Goose (Collias and Jahn 1959:484); Flamingo (C. E. King, personal communication); Lesser Flamingo (Alraun and Hewston 1997:175-76).
43
Japanese Macaque (Chapais and Mignault 1991:172; Wolfe 1984:155); Giraffe (Dagg and Foster 1976:28, 124, 144); Greylag Goose (Huber and Martys 1993:160). Likewise, in Northern Fur Seal populations with up to 40 or more females for every male, a number of behavioral and other factors insure that nearly every female is still able to mate heterosexually (Gentry 1998:167, 192-93). For Macaques, some researchers have suggested that females resort to homosexuality when deprived of "novel" male partners rather than of males per se (i.e., when they "run out" of new partners or become overly familiar with them) (Wolfe 1984:155, 1986:274 [Japanese Macaque]; Huynen 1997 [Rhesus Macaque]). As Vasey (1996:550) points out, however, this explanation is flawed because the females they turn to are no more "novel" than the males are (and probably even less so, owing to the high levels of female bonding and familiarity in these species). In addition, some females continue to choose other females as partners even in populations that have novel males.
44
Gorilla (Robbins 1996; Fossey 1983, 1984; Harcourt et al. 1981); Hanuman Langur (Weber and Vogel 1970) Crested Black Macaque (Reed et al. 1997; Dixson 1977); Squirrel Monkey (DuMond 1968; Travis and Holmes 1974; Akers and Conaway 1979; Denniston 1980; Mendoza and Mason 1991); Walrus (Miller and Boness 1983; Sjare and Stirling 1996); Lion (Schaller 1972; Chavan 1981); Mallard Duck (Bossema and Roemers 1985; Schutz 1965:457-59); Black-headed Gull (Kharitonov and Zubakin 1984); West Indian Manatee (Hartman 1971, 1979); Cheetah (Eaton and Craig 1973; Eaton 1974a). In some of these cases (e.g., Gorillas, Hanuman Langurs) homosexual activity among males is much more common in same-sex groups although it still occurs sporadically or "residually" in mixed groups; in other cases (e.g., Squirrel Monkeys, Crested Black Macaques) homosexual activity is equally if not more common in at least some mixed-sex groups.
45
Squirrel Monkey (Talmage-Riggs and Anschel 1973:68, 71); Long-eared Hedgehog (Poduschka 1981:81).
46
Silver Gull (Mills 1991:1523, 1526); Mallard Duck (Schutz 1965:442); Canada Goose (Collias and Jahn 1959:500); Jackdaw (Roell 1979:126, table 1); Lesser Scaup Duck (Bellrose 1976:344); Caribou (Bergerud 1974:432).
47
Flamingo (Wilkinson 1989:53-54; King 1994:105; C. E. King, personal communication); Laughing Gull (Hand 1981:138-39); Humboldt Penguin (Scholten 1992:5); Gentoo Penguin (Stevenson 1983:192); Pied Kingfisher (Moynihan 1990:19; Reyer 80:220); Peach-faced Lovebird (Fischdick et al 1984:314); Galah (Rogers and McCulloch 1981:90); Bicolored Antbird (Willis 1967:112).
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48
Cattle Egret (Fujioka 1986b:421-22); emperor and other penguins (Williams, T. D. [1995] The Penguins: Spheniscidae, pp. 80, 160 [Oxford: Oxford University Press]); dipper (Wilson, J. D. [1996] "The Breeding Biology and Population History of the Dipper Cinclus cinclus on a Scottish River System," Bird Study 43:108-18); Oystercatcher (Heg and van Treuren 1998); Australian noisy miner (Dow, D. D., and M. J. Whitmore [1990] "Noisy Miners: Variations on the Theme of Communality," in P. B. Stacey and W. D. Koenig, eds., Cooperative Breeding in Birds: Long-Term Studies in Behavior, pp. 559-92 [Cambridge: Cambridge University Press]); spotted sandpiper (Oring, L. W., J. M. Reed, and S. J. Maxson [1994] "Copulation Patterns and Mate Guarding in the Sex-Role Reversed, Polyandrous Spotted Sandpiper, Actitis macularia," Animal Behavior 47:1065-72).
49
Redshank (Nethersole-Thompson and Nethersole-Thompson 1986:228); mustached warbler (Fessl, B., S. Kleindorfer, and H. Hoi [1996] "Extra Male Parental Behavior: Evidence for an Alternative Mating Strategy in the Moustached Warbler Acrocephalus melanopogon," Journal of Avian Biology 27:88-91); Ostrich (Bertram 1992:125-26, 178); Greater Rhea (Navarro et al. 1998:117-18); Tree Swallow (Leffelaar and Robertson 1985); tropical house wren (Freed, L. A. [1986] "Territory Takeover and Sexually Selected Infanticide in Tropical House Wrens," Behavioral Ecology and Sociobiology 19:197-206); barn swallow (Crook, J. R., and W. M. Shields [1985] "Sexually Selected Infanticide by Adult Male Barn Swallows," Animal Behavior 33:754-61); Black Stilt (Pierce 1996:85); Silver Gull (Mills 1989:388); Herring Gull (Burger and Gochfeld 1981:128); African Elephant (Buss and Smith 1966:385-86; Kuhme 1963:117).
50
White-handed Gibbon (Edwards and Todd 1991:234; Reichard 1995 a,b; Mootnick and Baker 1994); Ostrich (Sauer 1972:737); Buff-breasted Sandpiper (Lanctot and Laredo 1994:8; Pruett-Jones 1988:1748).
51
American Bison (Komers et al. 1994:324; D. F. Lott, personal communication); Bonobo (Hashimoto 1997:12 — 13).
52
Musk-ox (Smith 1976:37, 56, 75-77; Gray 1979; Reinhardt 1985); Asiatic Elephant (Poole et al. 1997:304, 306-7 [fig. 5]); New Zealand Sea Lion (Marlow 1975:186, 203); Wolf (Zimen 1981:140); Killer Whale (Rose 1992:73, 83-84, 112, 116).
53
Ruff (Hogan-Warburg 1966:178-79, 199-200; van Rhijn 1991:69); Pukeko (Jamieson et al. 1994:271; Jamieson and Craig 1987a); Ocher-bellied Flycatcher (Westcott 1993:450); Ruffed Grouse (Gullion 1981:377, 379-80); Oystercatcher (Heg and van Treueren 1998: 689-90); Brown-headed Cowbird (Rothstein et al. 1986:150, 154-55, 167; Darley 1978); Guianan Cock-of-the-Rock (Trail and Koutnik 1986:209).
54
Giraffe (Dagg and Foster 1976:123; Innis 1958:258-60); Japanese Macaque (Vasey 1996 and personal communication; Corradino 1990:360; Wolfe 1984); Hanuman Langur (Srivastava et al. 1991); Gray Seal (Backhouse 1960:310); Killer Whale (Jacobsen 1990:75-78); Zebras (Rasa and Lloyd 1994:186); Great Cormorant (Kortlandt 1949); Orange-fronted Parakeet (Hardy 1965:152-53); Wapiti (Lieb 1973:61; Graf 1955:73; Harper et al. 1967:37); Ducks (McKinney et al. 1983). Most of these cases are also examples of a "preference" for homosexual activity in the participating individuals.
55
White-fronted Amazon Parrot (Clarke 1982:71); Long-eared Hedgehog (Poduschka 1981:81); Steller's Sea Eagle (Pringle 1987:104); Barn Owl (Jones 1981:54); Rhesus Macaque (Erwin and Maple 1976:12-13); Crab-eating Macaque (Hamilton 1914:307-8); Bottlenose Dolphin (McBride and Hebb 1948:121); Cheetah (Ruiz-Miranda et al. 1998:7, 12); Black-headed Gull (van Rhijn and Groothuis 1987:142-43; van Rhijn 1985:91-93); Mallard Duck (Schutz 1965:442, 449-50, 460).
56
Ring-billed Gull (Conover and Hunt 1984a); Greylag Goose (Huber and Martys 1993:157[fig.1]).
57
Willson, M. F., and E. R. Pianka (1963) "Sexual Selection, Sex Ratio, and Mating Systems," American Naturalist 97:405-7; Verner, J. (1964) "Evolution of Polygamy in the Long-billed Marsh Wren," Evolution 18:252 — 61; Verner, J., and M. F. Willson (1966) "The Influence of Habitats on Mating Systems of North American Passerine Birds," Ecology 47:143-47; Wittenberger, J. E. (1976) "The Ecological Factors Selecting for Polygyny in Altricial Birds," American Naturalist 109:779-99; Wittenberger, J. E. (1979) "The Evolution of Vertebrate Mating Systems," in P. Marler and J. Vandenbergh, eds., Handbook of Neurobiology: Social Behavior and Communication, pp. 271-349 (New York: Plenum Press); Goldizen et al 1998 (Tasmanian Native Hen). For examples of (heterosexual) mating systems actually determining the sex ratio rather than vice versa, see Hamilton, W. D. (1967) "Extraordinary Sex Ratios," Science 156:477-88; Wilson, D. S., and R. K. Colwell (1981) "Evolution of Sex Ratio in Structured Demes," Evolution 35:882-97.
58
In Roseate Terns, for example, homosexual pairs were initially taken as evidence of skewed sex ratios, even though the sex ratio in this species had not yet been reliably determined (owing to the difficulty, until recently, of accurately determining the sex of individuals) (Sabo et al. 1994:1023, 1026).
59
Western Gull (Hunt and Hunt 1977; Hunt et al. 1980; Wingfield et al. 1980; Fry and Toone 1981; Fry et al. 1987; Hayward and Fry 1993); Herring Gull (Fitch 1979; Shugart et al. 1987, 1988; Pierotti and Good 1994).
60
For explicit refutation of an association between female homosexual pairs and environmental toxins, see Hunt 1980 (Western Gull); Lagrenade and Mousseau 1983; and Conover 1984c (Ring-billed Gull).
61
Fry et al. 1987; Fry, D. M., and C. K. Toone (1981) "DDT-induced Feminization of Gull Embryos," Science 213:922-24.
62
Fry et al. 1987:37, 39; Fry and Toone 1981:923. Behavioral changes that could potentially be relevant have only been observed in other bird species, and only as a result of direct injection with estrogen, a female hormone, and not as a result of exposure to toxins (which mimic some of the effects of estrogen).
63
Indeed, if toxin-induced "feminization" resulted in behavioral changes, one might even expect this to be manifested directly as male homosexuality (especially under a "pseudoheterosexual" interpretation, or one in which homosexuality is equated with intersexuality), yet this has not been reported for these populations either. Even if such homosexuality were to occur, however, it would not necessarily argue for reduced numbers of breeding males: homosexually paired males in several bird species (including Black-headed and Laughing Gulls) sometimes continue to copulate with females (i.e., they are functionally bisexual and their same-sex pair bonds are nonmonogamous).
{701}
64
Herring Gull and other species (Fitch and Shugart 1983:6).
65
Western Gull (Fry et al. 1987); Herring Gull (Burger and Gochfeld 1981; Nisbet and Drury 1984:88). In these populations scientists have suggested that perhaps a cofactor is involved: availability of nest sites (Fry et al. 1987:40). The hypothesis is that homosexual pairs will only form in sex-skewed populations if there are vacant nest sites, since female pairs presumably are less able to compete for territories in dense colonies. However, Hand (1980:471) argues that homosexual pairs can effectively obtain (and defend) territories even in dense colonies. In addition, Fetterolf et al. (1984) show that female pairs of Ring-billed Gulls in crowded colonies are simply relegated to less optimal nest sites, rather than failing to form in the first place (or disbanding) because of competition or crowding. This "cofactor" is also of limited applicability to other bird species. In Orange-fronted Parakeets, for example, female pairs compete successfully against heterosexual pairs for possession of nest sites (Hardy 1963:187), while in many species female pairs form regardless of whether they acquire nesting sites (i.e., homosexual pair-formation is independent of nesting).
66
Herring Gull (Shugart et al. 1987, 1988); Ring-billed Gull (Conover and Hunt 1984a,b).
67
Watson, A., and D. Jenkins (1968) "Experiments on Population Control by Territorial Behavior in Red Grouse," Journal of Animal Ecology 37:595-614; Weatherhead, P. J. (1979) "Ecological Correlates of Monogamy in Tundra-Breeding Savannah Sparrows," Auk 96:391-401; Smith, J. N. M., Y. Yom-Tov, and R. Moses (1982) "Polygyny, Male Parental Care, and Sex Ratio in Song Sparrows: An Experimental Study," Auk 99:555-64; Hannon, S. J. (1984) "Factors Limiting Polygyny in the Willow Ptarmigan," Animal Behavior 32:153-61; Greenlaw, J. S., and W. Post (1985) "Evolution of Monogamy in Seaside Sparrows, Ammodramus maritimus: Tests of Hypotheses," Animal Behavior 33:373-83; Gauthier, G. (1986) "Experimentally-Induced Polygyny in Buffleheads: Evidence for a Mixed Reproductive Strategy?" Animal Behavior 34:300-302; Bjork-lund, M., and B. Westman (1986) "Adaptive Advantages of Monogamy in the Great Tit (Parus major): An Experimental Test of the Polygyny Threshold Model," Animal Behavior 34:1436-40; Stenmark, G., T. Slagsvold, and J. T. Lifjeld (1988) "Polygyny in the Pied Flycatcher, Ficedula hypoleuca: A Test of the Deception Hypothesis," Animal Behavior 36:1646-57; Brown-headed Cowbird (Yokel and Rothstein 1991).
68
Western Gull (Hunt and Hunt 1977); Herring Gull (Shugart et al. 1988). Fertility rates for homosexual pairs in other Gull species (not associated with environmental toxins) vary considerably, from 0 percent fertile eggs in Kittiwake female pairs (Coulson and Thomas 1985), 33 percent for Silver Gulls (Mills 1991), and 8-94 percent for Ring-billed Gulls (Ryder and Somppi 1979; Kovacs and Ryder 1983). Incidentally, only some of the males that copulate with female Western Gulls in homosexual pairs are known to be already paired; the remainder may in fact be single males that females are bypassing for pair-bonding, while utilizing them to fertilize their eggs (see Pierotti 1981:538-39). Also, some Silver Gulls in homosexual pairs may be raped by males, i.e., their particiption in breeding may be "forced" rather than "consensual" (Mills 1989:397).
69
Herring Gull (Fitch and Shugart 1984:123); Ring-billed Gull (Conover 1984b:714-16; Fetterolf and Blokpoel 1984:1682); Western Gull (Pierotti 1980:292); Roseate Tern (Spendelow and Zingo 1997:553). In Roseate Terns, females with proven single-parenting abilities nevertheless sometimes still form homosexual pairs, indicating that their same-sex partnership is not due solely to the "necessity" of finding a coparent (e.g., one female formed a homosexual pair even though she had successfully raised a chick on her own when her male partner died the previous year).
70
For an extensive list of species in which supernormal clutches have been found — only a fraction of which involve verified female pairs — see Conover 1984c (Ring-billed Gull). For other sources of supernormal clutches (and the occurrence of female pairs with regular-sized clutches), see Western Gull and other species (Conover 1984); Ring-billed Gull and other species (Conover and Aylor 1985; Conover and Hunt 1984; Ryder and Somppi 1979); Common Gull (Trubridge 1980); Terns (Penland 1984; Shealer and Zurovchak 1995; Gochfeld and Burger 1996:631); loons (McNicholl, M. K. [1993] "Supernumerary Clutches of Common Loons, Gavia immer, in Ontario," Canadian Field-Naturalist 107:356-58); sandpipers and related species (Mundahl, J. T., O. L. Johnson, and M. L. Johnson [1981] "Observations at a Twenty-Egg Killdeer Nest," Condor 83:180-82; Sordahl, T. A. [1997] "Breeding Biology of the American Avocet and Black-necked Stilt in Northern Utah," pp. 350, 352, Southwestern Naturalist 41:348-54); Laysan Albatross (Fisher 1968). On the nonoccurrence of female pairs in certain species with supernormal clutches, see Narita, A. (1994) "Occurrence of Super Normal Clutches in the Black-tailed Gull Larus crassirostris," Journal of the Yamashina Institute of Ornithology 26:132-34; Chardine, J. W., and R. D. Morris (1996) "Brown Noddy (Anous stolidus)," in A. Poole and F. Gill, eds., The Birds of North America: Life Histories for the 21st Century no. 220, pp. 10, 18 (Philadelphia: Academy of Natural Sciences; Washington, D.C.: American Ornithologists' Union).
71
And sometimes the correlation between the two end points is itself suspect. For example, it has been claimed that supernormal clutches are more common in Great Lakes populations of Herring Gulls than they are in New England, a fact that is attributed to greater levels of DDT poisoning in the Great Lakes (Conover 1984c:254) and/or the absence of available nesting sites in New England (Fry et al. 1987:40; see note 65 above). However, Nisbet and Drury (1984:88) show that the "higher rate" of supernormal clutches in the Great Lakes can be traced to only one particular colony site; in three other Great Lakes areas censused, the prevalence of supernormal clutches was no greater than in New England. Moreover, even if such clutches are more common in the Great Lakes area, the fact that they still occur in New England indicates that their presence cannot be due entirely to pollutant-related (or nest-site availability) factors.
{702}
72
In Western Gulls, the correlation between toxins and supernormal clutches is claimed to be supported by chronological evidence: larger clutches were supposedly not common prior to the widespread use of pesticides in the 1950s-1970s in southern California, while female pairs are claimed to occur at a "much lower" rate (Hayward and Fry 1993:19) or to have all but disappeared (Pierotti and Annett 1995:11) now that pesticide use has stopped. However, no comprehensive survey of the affected areas has in fact been conducted to assess the actual incidence of female pairs today (even if such a study were to find consistently low levels, this would still be significant, since it would demonstrate a "residual" component of same-sex activity that is independent of toxin effects and of a "shortage" of the opposite sex, as is true for many other species). Nor have detailed longitudinal or geographic studies been conducted to track the putative correlations during this entire five-to-six-decade period. In fact, records of supernormal clutches in Ring-billed Gulls go back much earlier, to the early 1900s (and in other species back to the late 1800s), while in some Terns their frequency has actually decreased since the 1950s (Conover 1984c), so the chronological question is far from resolved. At least one researcher who has addressed the temporal issue rejects the DDT (or other pollutant) connection for the majority of cases: Conover (1984c:254) conducted an extensive survey of the occurrence of supernormal clutches in 34 species, including comparing pre- and post-1950 rates, and concluded that their frequency is not higher since the 1940s for most Gull and Tern species. Finally, no studies have yet determined the incidence of homosexual pairing/supernormal clutches in other regions of the world that have the highest levels of contamination from DDT and related pollutants, such as the Baltic Sea, the Waddensee, the Irish Sea, the Gulf of St. Lawrence, and the northern Gulf of Mexico (Nisbet, I. C. T. [1994] "Effects of Pollution on Marine Birds," p. 13, in D. N. Nettleship, J. Burger, and M. Gochfeld, eds. Seabirds on Islands: Threats, Case Studies, and Action Plans, pp. 8-25. [Cambridge: BirdLife International]).
73
Hayward and Fry 1993:19; Luoma, J. R. (1995) "Havoc in the Hormones," Audubon 97(4):60-67; Robson, B. (1997) "A Chemical Imbalance," Nature Canada 26(1):29-33; see also Coulson 1983 (Caspian Tern). The equating of homosexuality with environmental and physiological "havoc" has also entered the more popular discourse, as in a recent public radio broadcast that referred to lesbian pairs in Gulls as evidence of hormonal imbalances caused by environmental contamination ("Gator Envy," All Things Considered, National Public Radio, February 1, 1995). Some things not considered in this report were the broader context of same-sex pairing in other species and the intricacies of the specific cases. For more on the pathologizing of homosexuality, see the following section "Gross Abnormalities of Behavior."
74
See, for example, Aiken (1981) on Water Boatman Bugs. Even this case is somewhat less than definitive, however, since more than half of all mating attempts in this species are by males on other males.
75
Guianan Cock-of-the-Rock (Trail 1985a:238, 240); Giraffe (Spinage 1968:130); Black-billed Magpie (Baeyens 1979:39-40); Mountain Sheep (Geist 1968:208). For examples of homosexual interactions that are explicitly labeled "mistakes" or "errors" (including, but not limited to, cases of sex misrecognition), see Asiatic Mouflon (Schaller and Mirza 1974:318-20); Common Murre (Birkhead et al. 1985:610-11); Oystercatcher (Makkink 1942:60); Laughing Gull (Hand 1981:139-40); Greater Rhea (Fernandez and Reboreda 1995:323).
76
Redshank (Hale and Ashcroft 1982:471). Other species in which the occurrence of homosexuality is taken as the sole evidence of faulty sex recognition or "indiscriminate" mating or courtship include Cavies (Rood 1970:449), Little Brown Bats (Thomas et al. 1979:134), Shags (Snow 1963:93-94), Little Egrets (Fujioka 1988), Oystercatchers (Makkink 1942:67-68), Black-headed Gulls (van Rhijn 1985:87, 93), Superb Lyrebirds (Lill 1979a:496), and King Penguins (Murphy 1936:340). It should also be pointed out that the claim of "indiscriminate" sexual activity is often quite exaggerated: it is not uncommon for the mere existence of same-sex activity to be interpreted as evidence that the sex of the partner is immaterial, even when the animals show clear partner preferences, sometimes even favoring homosexual activity. For example, Trail and Koutnik (1986:210-11) claim that yearling Guianan Cock-of-the-Rock will mount any bird that sits still long enough; in fact, only one attempted heterosexual mount by a yearling was recorded during their study, compared to hundreds of homosexual mounts, and certain adult males were clearly mounted more often than others (ibid., 211-12, 215).
77
Yellow-eyed penguin (Richdale, L. E. [1951] Sexual Behavior in Penguins, p. 73 [Lawrence, Kans.: University of Kansas Press]); Silvery Grebe (Nuechterlein and Storer 1989:344); Red-faced Lovebird (Dilger 1960:667).
78
For species with adult-female/younger-male resemblances, see Rohwer, S., S. D. Fretwell, and D. M. Niles (1980) "Delayed Maturation in Passerine Plumages and the Deceptive Acquistion of Resources," American Naturalist 115:400-437; for species with adult-female/adult-male resemblances, see Burley, N. (1981) "The Evolution of Sexual Indistinguishability," in R. D. Alexander and D. W. Tinkle, eds., Natural Selection and Social Behavior, pp. 121-37 (New York: Chiron Press). A caveat about these cases is that the absence of homosexuality in a species is not necessarily a reliable form of evidence, since (as discussed in chapters 1-3) homosexual behavior is often hard to observe, easy to overlook, or deliberately ignored in the field.
79
Blackbuck (Dubost and Feer 1981:74-75); Guianan Cock-of-the-Rock (Trail and Koutnik 1986:199; Trail 1983); Swallow-tailed Manakin (Foster 1987:549; Sick 1967:17; 1959:286); Blue-backed Manakin (Snow 1963:172); Raggiana's Bird of Paradise, Victoria's Riflebird (Gilliard 1969:113, 223); Regent Bowerbird (Gilliard 1969:337); Superb Lyrebird (Smith 1982 and personal communication).
80
Mountain Goat (Chadwick 1983:14, 189-91); Bishop Birds (Craig and Manson 1981:13); Galah (Rogers and McCulloch 1981:81; Rowley 1990:4); Humboldt Penguin (Scholten 1987:200); King Penguin (Stonehouse 1960:11); Superb Lyrebird (Smith 1982 and personal communication); Ocher-bellied Flycatcher (Westcott and Smith 1994:678, 681; Snow and Snow 1979:286); Tree Swallow (Stutchbury and Robertson 1987c); Anna's Hummingbird (Ortiz-Crespo 1972; Wells et al. 1996).
{703}
81
Andersson, S., J. Ornborg, and M. Andersson (1998) "Ultraviolet Sexual Dimorphism and Assortative Mating in Blue Tits," Proceedings of the Royal Society of London, Series B 265:445-50; Hunt, S., A. T. D. Bennett, I. C. Cuthill, and R. Griffiths (1998) "Blue Tits Are Ultraviolet Tits," Proceedings of the Royal Society of London, Series B 265:451-55; Witte, K., and M. J. Ryan (1997) "Ultraviolet Ornamentation and Mate Choice in Bluethroats," in M. Taborsky and B. Taborsky, eds., Contributions to the XXV International Ethological Conference, p. 201, Advances in Ethology no. 32 (Berlin: Blackwell Wissenschafts-Verlag); Roper, T. J. (1997) "How Birds Use Sight and Smell," Journal of Zoology, London 243:211-13; Bennett, A. T. D., I. C. Cuthill, J. C. Partridge, and E. J. Maier (1996) "Ultraviolet Vision and Mate Choice in Zebra Finches," Nature 380:433-35; Waldvogel, J. A. (1990) "The Bird's Eye View," American Scientist 78:342-53; Cabbage White Butterfly (Obara 1970 and personal communication; Obara, Y. [1995] "The Mating Behavior of the Cabbage White Butterfly," paper presented at the 24th International Ethological Conference, Honolulu, Hawaii); Superb Lyrebird (Reilly 1988:45).
82
Mountain Goat (Geist 1964:565); Musk-ox (Smith 1976:56); Cavies (Rood 1972:27, 54, 1970:443); Bighorn Sheep (Geist 1968:208); Common Murre (Birkhead et al. 1985:610-11); Flamingo (C. E. King, personal communication); Pronghorn (Kitchen 1974:44 [table 22]). In addition, some homosexual activity in Mountain Goats and Pronghorns also involves age-mates interacting with each other (adult males in Mountain Goats, younger males in Pronghorns). See also Wagner (1996) on Razorbills.
83
Swallow-tailed Manakin (Foster 1987:555); Laughing Gull (Noble and Wurm 1943:205); Black-headed Gull (van Rhijn and Groothuis 1985:163). Conversely, homosexuality has sometimes been attributed to behavioral identity between males and females. In Ruffed Grouse, for example, the nonaggressive or "submissive" posture of a male is similar to the behavior of a female during courtship, and that males court both sexes is attributed to their inability to distinguish "female-acting" males from actual females (Allen 1934:185; see also the discussion of "pseudoheterosexuality" earlier in this chapter). Aside from the fact that males and females are very different visually from each other in this species and therefore "there is no excuse for a male not recognizing a female" (as Allen [1934:180-81] observes), in the related red grouse there is a parallel identity between male "submissive" and female courtship behavior, yet males do not court other males in this species (Watson, A., and D. Jenkins [1964] "Notes on the Behavior of the Red Grouse," British Birds 57:157).
84
Tree Swallow (Stutchbury and Robertson 1987a:719-20, 1987b:418). It is also unlikely that homosexual activity between adult males results from their mistaking one another for (adult) females. As Lombardo et al. (1994) point out, although the two sexes in this species look similar, the sex of at least one male involved in homosexual activity was nevertheless identifiable from his cloacal (genital) protuberance, lack of brood patch, and wing length. Most adult females are also visually distinct from males owing to the presence of a brown patch on the forehead (shorter wings also distinguish subadult females from subadult males) (Stutchbury and Robertson 1987c). In addition, same-sex copulations appear to be fairly uncommon in this species (Lombardo, personal communication) — certainly they are not nearly as frequent as one would expect if "mistakes" in sex recognition were prevalent.
85
Black-headed Gull (van Rhijn 1985:87, 100).
86
Hooded Warbler (Niven 1993:191) (cf. Lynch et al. [1985:718] for mean dimensions of other males). Niven (1993 and personal communication) suggests that it was also the female behavior patterns of this male that "triggered" the homosexual pairing, yet this bird's behavior was actually a mixture of male and female patterns, involving, for example, incubation (female duties) as well as singing (male). Moreover, male Hooded Warblers are particularly attuned to differences in song pattern, using this information to recognize individual birds and then storing it in long-term memory for future use (Godard 1991). Because this male's singing was highly distinctive, it is improbable that other males simply "disregarded" this aspect of his behavior or were "unaware" of his male status (especially given his physical characteristics). Furthermore, all "female" behaviors recorded in this individual occurred after the formation of the pair-bond — since pairs were not observed early in the breeding season, we do not in fact know whether this individual exhibited any (or only) "femalelike" patterns during courtship and pair-formation.
87
Hooded Warbler: differential attacking of males (Stutchbury 1994:65-67); mating success of malelike females (as evidenced by the fact that nests are fairly equally distributed between dark and light females) (Stutchbury et al. 1994:389[fig.6]; Stutchbury and Howlett 1995:95); promiscuous mating attempts on hooded females (Stutchbury et al. 1994:388).
88
Common Garter Snake (Mason 1993:261, 264; Mason et al. 1989:292; Mason and Crews 1985; Noble 1937:710-11); other species (Muma, K., and P. J. Weatherhead [1989] "Male Traits Expressed in Females: Direct or Indirect Sexual Selection?" Behavioral Ecology and Sociobiology 25:23-31; Potti, J. [1993] "A Male Trait Expressed in Female Pied Flycatchers Ficedula hypoleuca: The White Forehead Patch," Animal Behavior 45:1245-47 [cf. also Saetre and Slagsvold 1992:295-96]; Tella, J.L., M. G. Forero, J.A. Donazar, and F. Hiraldo [1997] "Is the Expression of Male Traits in Female Lesser Kestrels Related to Sexual Selection?" Ethology 103:72-81; McDonald, D. B. [1993] "Delayed Plumage Maturation and Orderly Queues for Status: A Manakin Mannequin Experiment," p. 38, Ethology 94:31-45). Experimental "disguising" of individuals to look like the opposite sex does not automatically induce "homosexual" behavior either. Female Chaffinches whose plumage has been painted to resemble male patterns, for example, are not courted by (nor do they form pair-bonds with) other females that "mistake" them for males (Marler 1955). Homosexual pairing does {704}
occur in this species, but between females that do not look like males. Likewise, yellowthroats (a bird species) are able to recognize the "true" sex of both males and females whose facial coloration has been manipulated to make them resemble the opposite sex. Similar results have been found for damselflies (Lewis, D. M. [1972] "Importance of Face-Mask in Sexual Recognition and Territorial Behavior in the Yellowthroat," Jack-Pine Warbler 50:98-109; Gorb, S. N. [1997] "Directionality of Tandem Response by Males of a Damselfly, Coena-grion puella," in M. Taborsky and B. Taborsky, eds., Contributions to the XXV International Ethological Conference, p. 138. Advances in Ethology no. 32 [Berlin: Blackwell Wissenschafts-Verlag]). In addition, in species such as lazuli buntings where juvenile males resemble adult females, experimental studies have demonstrated that adult males are in fact consistently able to distinguish the two sexes (Muehter, V. R., E. Greene, and L. Ratcliffe [1997] "Delayed Plumage Maturation in Lazuli Buntings: Tests of the Female Mimicry and Status Signalling Hypotheses," Behavioral Ecology and Sociobiology 41:281-90).
89
Tree Swallow (Lombardo et al. 1994:555-56; Venier et al. 1993; Venier and Robertson 1991); Black-crowned Night Heron (Noble et al. 1938:29); Regent Bowcrbird (Marshall 1954:114-16); Greenshank (Nethersole-Thompson and Nethersole-Thompson 1979:114; Nethersole-Thompson 1951:104). In Tree Swallows, it is also unlikely that males cooperate during homosexual copulations in order to "appease" the birds mounting them and thereby avoid attack or injury (as suggested by Lonrbsrdo et al. 1994:556). Aggressive attacks in this species are characterized by a number of distinctive behavioral elements on the part of both the attacker (e.g., threat displays, grappling, pecking) and the bird being attacked (e.g., appeasement displays, submissive and distress calling) (cf. Robertson et al. 1992:6, 8) — and homosexual mountings exhibit none of these hallmarks.
90
Such cases contrast markedly with ones in which the pursued animal is clearly not a willing participant, such as Mountain Goats, Common Murres, or Anna's Hummingbirds. In these instances, however, there are other arguments against a sex misrecognition analysis (as mentioned previously).
91
Swans (Kear 1972:85-86).
92
Wattled Starling (Sontag 1991:6); Common Chimpanzee (Kollar et al. 1968:444, 458); Gorilla (Coffin 1978:67); Stumptail Macaque (Bernstein 1980:32); Musk-ox (Reinhardt 1985:298-99); Koala (Smith 1980:186); Long-eared Hedgehog (Poduschka 1981:81; Reeve 1994:189); Vampire Bat (Greenhall 1965:442); Black-crowned Night Heron (Noble et al. 1938:14, 28-29). Factors such as stress or crowding have also been invoked for wild animals, such as Blue-bellied Rollers (Moynihan 1990).
93
Dolphins (Pilleri, G. [1983] "Cetaceans in Captivity," Investigations on Cetacea 15:221-49); Barn Owl (Jones 1981); Rhesus Macaque (Strobel. I). [1979] "Behavior and Malnutrition in Primates," in D.A. Levitsky, ed., Malnutrition, Environment, and Behavior: New Perspectives, pp. 193-218 [Ithaca: Cornell University Press]). Many reports of animal homosexuality and transgender have appeared in medical journals and other publications dealing with pathology. See, for example, the descriptions of same-sex activity among Common Chimpanzees in Kollar et al. 1968 (characterized as "perverse sexual acts"), which appeared in the Journal of Nervous and Mental Disease.
94
Cheetah (Eaton 1974a:116); Zebra Finch (Immelmann et al. 1982:422). The assessment for Cheetahs is particularly inappropriate in light of the fact that heterosexual activity is extremely difficult to observe in this species in the wild. As mentioned in chapter 1, during one ten-year study of Cheetahs, no heterosexual matings were seen over 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 species (Caro 1994:42). It is hardly surprising, therefore, that homosexual courtship and mating activity has so far only been seen in captivity. It should also be pointed out that male "coalitions" (bonded pairs or trios) have been observed in both wild and captive Cheetahs (wild [Caro and Collins 1986, 1987; Caro 1994]; captive [Eaton and Craig 1973:223; Ruiz-Miranda et al. 1998]). The assumption that sex segregation is completely "artificial" for male Cheetahs living in captivity is also false (see discussion below).
95
Fedigan 1982:143 (Japanese Macaque). See also Crews et al. (1983:228-30) and Crews and Young (1991:514) for similar statements challenging the supposed "abnormalcy" of same-sex copulation among Whiptail Lizards in captivity versus the wild.
96
In a few cases, specific homosexual activities, rather than the occurrence of homosexuality itself, have been observed in only wild or captive conditions. In Bonobos, for example, penis-fencing (a form of genital rubbing) has only been seen in the wild, while fellatio has only been observed in captivity (de Waal 1997:103-4). In addition, the duration of sexual acts can vary contextually: for example, de Waal (1987:326) found that episodes of genital rubbing between female Bonobos were considerably shorter in captivity (averaging around 9 seconds) than in the wild (averaging around 15 seconds).
97
Orang-utan (Nadler 1988: 107); Hamadryas Baboon (Kummer and Kurt 1965:74); Mule Deer (Halford et al. 1987:107); Musk-ox (Reinhardt 1985:298).
98
Bonobo, wild (Kano 1992:187 [table 24], 140; Kitamura 1989:53, 55-57, 61); Bonobo, captive (de Waal 1995:41 [table 3.1]); Black Swan (Braithwaite 1981:141-42). Five other species for which the relevant quantitative information is available are Pig-tailed, Crested Black, and Stumptail Macaques, Common Chimpanzees, and Vervets. Although the wild (or semi-wild) and captive figures in these cases are more difficult to compare (due to differences in group size and composition, observed behaviors, length of study periods, etc.), they also generally show fairly comparable rates. For Pig-tailed Macaques in the wild, 7-23 percent of mounting is same-sex, compared to about 25 percent in captivity (rates in the wild based on information in Oi 1990a:350-1 [including table [V], Oi 1996:345, and Bernstein 1967:226-27; captivity — Tokuda et al. 1968:287, 291 [table 7]). Among captive Crested Black Macaques, about 5 percent of mounting is between males {705}
(Dixson 1977:74, 77), compared to an estimated 8 percent in the wild (C. Reed, personal communication; figures for both of these species combine "copulatory" with "noncopulatory" mounts). However, another study (Bernstein 1970:94 [table IV]) yielded a much higher rate of same-sex mountings in captivity for these species — 49 percent for Pigtails, 22 percent for Crested Blacks — demonstrating that there can be considerable differences between individual studies and/or populations (see also Bernstein [1967:228] for more on wild/captive comparisons in Pigtails). In Stumptail Macaques, 25 percent of sexual interactions (of all types) in captivity are homosexual (Chevalier-Skolnikoff 1974:100-101, 110), compared to 30-40 percent for mounting in a semi-wild troop (formerly captive animals that were transplanted and released) (Estrada et al. 1977:667 [fig.14]; Estrada and Estrada 1978:672 [table 4]). In Common Chimpanzees, same-sex mounting actually occurs more frequently in the wild: de Waal and van Hooff (1981:182 [table 2]) found that mounting between males in captivity constitutes only 1-2 percent of the behaviors involved in reassurance, enlistment of support, and other activities during conflicts, while Nishida and Hosaka (1996:120-21 [tables 9.5-9.6]) found that mounting accounts for one-third to one-half of such behaviors in wild Chimps. Likewise, Bernstein (1970:94 [table IV]) found that 9 percent of mounting activity in captive Vervets is same-sex, while Gartlan (1969:144, 146) and Struhsaker (1957:21, 27 [tables 8, 10]) both recorded 11 percent same-sex mounting in the wild. Rowell (1967b) also conducted a detailed quantitative comparison of behavioral frequency rates in the wild and captivity among Savanna (Olive) Baboons; unfortunately, mounting (and other sexual-behavior) rates between males in the wild could not be compared to rates in captivity because males were too aggressive to be kept together in captivity. On a related point, Rasa (1979b:321) found no substantial differences in Dwarf Mongoose same-sex (and opposite-sex) mounting rates when their behavior in crowded versus noncrowded captive conditions was compared (based on controlled observational regimes). Likewise, Heg and van Treuren (1998:689-90) did not find significantly higher rates of homosexual bonding (in the form of bisexual trios) when population densities increased among wild Oystercatchers.
99
Bottlenose Dolphin (McBride and Hebb 1948:114, 122; Wells et al. 1987; Wells 1991; Wells et al. 1998:65-67); Gorilla (Schaller 1963:278: Stewart 1977; Yamagiwa 1987a,b; Harcourt 1988; Porton and White 1996:723-24).
100
Jackdaw (Lorenz 1935/1970; Roell 1979); Elephants (Rosse 1892; Shelton 1965); Crested Black Macaque (Poirier 1964:147; Dixson 1977; Reed et al. 1997); Orange-fronted Parakeet (Buchanan 1966); Lion (Cooper 1942; Chavan 1981); Great Cormorant (Kortlandt 1949; Fukuda 1992); Regent Bowerbird (Phillipps 1905; Lenz 1994); Dolphins (Brown et al. 1966; Herzing and Johnson 1997). Similar erroneous assertions are sometimes made regarding transgender. Payne (1984:14), for example, claims that female-plumaged or transvestite male Ruffs occur only in captivity (citing Stonor 1937). In fact, female-plumaged males — generally referred to in this species as naked-nape males — are now known to be a regular feature of wild Ruff populations (cf. van Rhijn 1991) and have been discussed as such in the scientific literature since at least Hogan-Warburg (1966). Payne, R. B. (1984) Sexual Selection, Lek and Arcna Behavior, and Sexual Size Dimorphism in Birds, Ornithological Mongraphs no. 33 (Washington, D.C.: American Ornithologists' Union).
101
In this regard, homosexual activity in some species is also claimed to be "caused" by unusual or abnormal environmental or climatic conditions, such as severe winter snowstorms that disrupt "normal" pairing in Golden Plovers (Nethersole-Thompson and Nethersole-Thompson 1961:207-8), or exceptionally rainy seasons that somehow "overstimulate" Ostriches (Sauer 1972:717) Assuming that ecological factors of this sort could be involved (which is debatable), an equally valid interpretation is that such species possess an inherent flexibility in their social and sexual systems that manifests itself during times of ecological flux or stress. Rather than being the "product" of "abnormal" conditions, then, such behavioral plasticity allows the species to respond "creatively" — in ways that, obviously, are not yet fully understood — to the vagaries of an ever-changing environment. See chapter 6 for further discussion.
102
Cheetah (Herdman 1972:112, 123;Caro 1993:27-28, 1994:362; Ruiz-Miranda et al. 1998:1, 13). For more on the false dichotomy of "wild" versus "captive" studies of animals, and the general compatibility and continuity between the two, see de Waal 1989a:27-33, 1997:11 (Bonobo).
103
Boto (Best and da Silva 1989:12-13); Orang-utan (van Schaik, C. P., E.A. Fox, and A. F. Sitompul [1996] "Manufacture and Use of Tools in Wild Sumatran Orangutans: Implications for Human Evolution," Naturwissenschaften 83:186-88); Savanna (Olive) Baboon (DeVore, 1. [1965] "Male Dominance and Mating Behavior in Baboons," p. 286, in F. A. Beach, ed., Sex and Behavior, pp. 266-89 [New York: John Wiley and Sons]); Thomson's Gazelle (Walther 1995:30-31); King Penguin (Gillespie 1932; Stonehouse 1960); Black-headed Gull (Kharitonov and Zubakin 1984:103; van Rhijn and Groothuis 1987:144); Flamingo (Cezilly and Johnson 1995).
104
Griffon Vulture (Blanco and Martinez 1996:247; Sarrazin et al. 1996:316); King Penguin (Weimerskirch et al. 1992:108); Gentoo Penguin (Williams and Rodwell 1992:637; Bost and Jouventin 1991:14); Flamingo (A. R. Johnson, personal communication); Dugong (Anderson 1997:440, 458; Preen 1989:384). See also chapter 3 for further discussion of heterosexual bias in the methods of sex determination employed during field studies of these and other species.
105
Canids (Macdonald 1980, 1996); Macaques (Oi 1990a; Reed et al. 1997); Gibbons (Fox 1977; Edwards and Todd 1991); Rose 1992:1-2 (Killer Whale); Aperea (Rood 1972:42); Rufous Bettong (Johnson 1980:347).
106
Orang-utan (Schurmann 1982:270-71, 282); Oystercatcher (Angier, N. [1998] "Birds' Design for Living Offers Clues to Polygamy," New York Times March 3, pp. B11-12).
107
van Lawick-Goodall, J. (1970) "Tool-Using in Primates and Other Vertebrates," p. 208, Advances in the Study of Behavior 3:195-249.
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108
Sage Grouse (Scott 1942:495); Rhesus Macaque (Carpenter 1942:150); Fat-tailed Dunnart (Ewer 1968:351); Long-eared Hedgehog (Poduschka 1981:84); Takhi (Boyd 1986:660).
109
Common Garter Snake (Noble 1937:710-11); Hooded Warbler (Niven 1993:192).
110
African Elephant (Sikes 1971:265-66); Snow/Canada Goose (Starkey 1972:456-57).
111
Western Gull (Wingfield et al. 1982); Ring-billed Gull (Kovacs and Ryder 1985). See also the examples of more "intense" nesting behavior in female pairs of Ring Doves and Budgerigars discussed in note 15, chapter 1, which might also be correlated with hormonal effects.
112
For a summary of these results, see Vasey, P. L. (1995) "Homosexual Behavior in Primates: A Review of Evidence and Theory," International Journal of Primatology 16:173-204. Some of the species in which hormone levels have been studied in association with homosexual behavior are Rhesus Macaques (Akers and Conaway 1979; Turner et al. 1989) and Hanuman Langurs (Srivastava et al. 1991). (Turner, J. J., J. G. Herndon, M.-C. Ruiz de Elvira, and D. C. Collins [1989] "A Ten-Month Study of Endogenous Testosterone Levels and Behavior in Outdoor-Living Female Rhesus Monkeys [Macaca mulatta]," Primates 30:523-30.) For a discussion of the problematic nature of studies on laboratory rats that purport to show an association between homosexual behavior and hormones, see Mondimore, F. M. (1996) A Natural History of Homosexuality, pp. 111-13, 129-30 (Baltimore: Johns Hopkins University Press); Byne, W. (1994) "The Biological Evidence Challenged," Scientific American 270(5):50-55.
113
Pied Kingfisher (Reyer et al. 1986:216); Orang-utan (Kingsley 1982:227); Spotted Hyena (Frank 1996; Frank et al. 1985, 1995 ; Glickman et al. 1993); Western Gull (Wingfield et al. 1982). See also Mloszewski (1983:186), who indicates that masculinized female African Buffalo — i.e., those with "pronounced male secondary sexual characteristics," likely due in part to a differing hormonal profile — do not participate in homosexual activity any more often than do nontransgendered females (and perhaps do so even less often). For other species in which a subset of individuals have different hormone profiles (not associated with homosexual activity), see Solomon, N. G., and J. A. French, eds. (1997) Cooperative Breeding in Mammals, pp. 241, 304-5, 370 (Cambridge: Cambridge University Press).
114
Takhi (Boyd 1986:660). Although detailed hormonal studies of Takhi during pregnancy have been conducted, they did not involve sampling of androgens or other male hormones; see Monfort et al. 1994; Monfort, S. L., N. P. Arthur, and D. E. Wildt (1991) "Monitoring Ovarian Function and Pregnancy by Evaluating Excretion of Urinary Oestrogen Conjugates in Semi-Free-Ranging Przewalski's Horses (Equus przewalskii)," Journal of Reproduction and Fertility 91:155-64.
115
Domestic Horses (McDonnell, S. [1986] "Reproductive Behavior of the Stallion," especially p. 550, in S. L. Crowell-Davis and K. A. Houpt, eds., Behavior, pp. 535-55. Veterinary Clinics of North America: Equine Practice 2[3] [Philadelphia: W. B. Saunders]).
116
Recent work on the sexual orientation of Domestic Sheep has begun to move away from this paradigm, to the extent that hormonal profiles are assessed for males who prefer mounting other males, rather than simply for the ("gender-atypical") males who are themselves mounted by other males. In this case, there do appear to be some differences between homosexual and heterosexual sheep (cf. Adler, T. [1996] "Animals' Fancies: Why Members of Some Species Prefer Their Own Sex," Science News 151:8-9; Resko et al. 1996; Perkins et al. 1992, 1995). However, rarely (if ever) is the two-way influence of biology and behavior discussed in these studies, i.e., biology (hormones, brain structure) is invariably assumed to determine sexual behavior, when in fact it is also possible for behavior (and other social factors) to alter or affect an animal's hormonal profile or brain structure. Moreover, the search for hormonal differences is little more than a continuation of the need to find a physiological "cause" for homosexuality. Within an overall framework in which any nonreproductive behavior is still seen as anomalous, this is only a few steps removed from the overt pathologizing of homosexuality so characteristic of earlier studies.
117
Savanna Baboon (Marais 1922/1969:205); Baker, J.R. (1929) Man and Animals in the New Hebrides, pp. 22, 117 (London: George Routledge and Sons).
118
Bighorn Sheep (Berger 1985:334-35); White-tailed Deer (Thomas et al. 1964:236; see also Taylor et al. 1964; Thomas et al. 1965, 1970); Savanna Baboon (Marais 1922/1969; Bielert 1984b, 1985).
119
For early descriptions of intersexual Savanna Baboons, see Marais 1922/1969, 1926. For a summary of early observations of velvet-horns and other gender-mixing Deer, see Thomas et al. 1970:3 (White-tailed Deer) and Anderson 1981:94-95 (Mule Deer).
120
Northern Elephant Seal (Le Boeuf 1974:173); Red Deer (Darling 1937:170); Black-headed Gull (van Rhijn 1985:87, 100); Common Garter Snake (Mason and Crews 1985:59).
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