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      {707} Chapter 5. Not for Breeding Only: Reproduction on the Periphery of Life

      1
Hutchinson, G. E. (1959) "A Speculative Consideration of Certain Possible Forms of Sexual Selection in Man," American Naturalist 93:81-91.

      2
According to sociobiologist James Weinrich, biological "mistakes" such as genetically transmitted diseases occur at very low rates, roughly 1 in 10,000 or less (Weinrich, J. D. [1987] Sexual Landscapes, p. 334 [New York: Charles Scribner's Sons]). Moreover, such genetic "defects," rather than being uniformly detrimental, sometimes confer unique abilities on their carriers. People with the genetic "disorder" of William's syndrome, for example — which occurs in about 1 in 20,000 people — often display extraordinary musical abilities, remarkable verbal skills, and exceptionally empathetic personalities, although they typically also have low IQs and some medical complications (Lenhoff, H. M., P. P. Wang, F. Greenberg, and U. Bellugi [1997] "William's Syndrome and the Brain," Scientific American 277[6]:68-73).

      3
As in most other "explanations" of homosexuality, these include both "proximate" and "ultimate" factors (a distinction widely employed in evolutionary biology). "Proximate" explanations focus on the immediate behavioral, social, physiological, demographic, environmental, and other factors that supposedly "trigger" or lead to homosexual activity, while "ultimate" explanations focus on the wider reproductive and evolutionary benefits that supposedly accrue from such activity.

      4
Weinrich, Sexual Landscapes; Ruse, M. (1982) "Are There Gay Genes? Sociobiology and Homosexuality," Journal of Homosexuality 6:5-34; Kirsch, J. A. W., and J. E. Rodman (1982) "Selection and Sexuality: The Darwinian View of Homosexuality," in W. Paul, J. D. Weinrich, J. C. Gonsiorek, and M. E. Hotveldt, eds., Homosexuality: Social, Psychological, and Biological Issues, pp. 183-95 (Beverly Hills, Calif.: SAGE Publications); Wilson, E. O. (1978) On Human Nature, pp. 142-47 (Cambridge, Mass.: Harvard University Press); Trivers, R. L. (1974) "Parent-Offspring Conflict," pp. 260-62, American Zoologist 14:249-64. For a critique of these theories as applied to humans, see Futuyama, D. J., and S. J. Risch (1984) "Sexual Orientation, Sociobiology, and Evolution," Journal of Homosexuality 9:157-68. For specific examples of homosexuality cited as a possible population-regulation mechanism — including nonreproductive sexuality as a stress-induced response to overpopulation in some species, and homosexuality as a form of "birth control" in humans — see Calhoun, J. B. (1962) "Population Density and Social Pathology," Scientific American 206(2):139-48; von Holst, D. (1974) "Social Stress in the Tree-Shrew: Its Causes and Physiological and Ethological Consequences," in R. D. Martin, G. A. Doyle, and A. C. Walker, eds., Prosimian Biology, pp. 389-411 (Pittsburgh: University of Pittsburgh Press); Denniston 1980:38 (Squirrel Monkey); Harris, M. (1980) Culture, People, and Nature, p. 208 (New York: Harper and Row). For more on the special "role" of homosexual and transgendered humans in some indigenous cultures, see chapter 6.

      5
See the discussion of same-sex parenting in chapter 1.

      6
See pp. 206-207 for further discussion of these and other alternate parenting arrangements.

      7
For a complete list of bird species with helpers, see Brown, J. L. (1987) Helping and Communal Breeding in Birds, pp. 18-24 (table 2.2) (Princeton: Princeton University Press). Three other species in which homosexual behavior occurs (Ostriches, House Sparrows, and Sociable Weavers) are classified by Brown as having helpers, but it is not clear that these represent genuine cases of helping. Even if they did, however, they would still not support the "helper" theory of homosexuality because homosexuality is either not limited to helpers in these species, or else not all helpers engage in homosexual behavior. In Ostriches "helping" behavior actually consists of foster-parenting by breeding pairs of males and females (ibid., p. 161); homosexuality only occurs in males in this species, and probably nonbreeders at that. In House Sparrows helping occurs occasionally among juveniles, probably of both sexes, and in only some populations (p. 31), while homosexual behavior only occurs in (a few) adult males. And in Sociable Weavers, breeding pairs are assisted in building communal nests, probably by birds of both sexes, but such birds do not help feed their young (see Maclean 1973); homosexuality occurs in both breeders and nonbreeders, but only males. Recently, helping behavior by adolescent males has also been discovered in Greater Rheas; however, this phenomenon is distinct from same-sex coparenting (and sexual activity) in this species, which involves adult males'(Codenotti and Alvarez 1997:570). For other surveys of the phenomena of communal breeding and helpers in birds, see Skutch, A. F. (1987) Helpers at Birds' Nests: A Worldwide Survey of Cooperative Breeding and Related Behavior (Iowa City: University of Iowa Press); Stacey, P. B., and W. D. Koenig, eds. (1990) Cooperative Breeding in Birds (Cambridge: Cambridge University Press).

      8
See chapters 1 and 4 for discussion of the fact that many cases of homosexuality in animals have probably been missed, overlooked, or remain to be discovered.

      9
Moynihan (1990:19) states that homosexual pairing and/or mounting is found among nonbreeding Pied Kingfisher males, but does not further specify which categories of nonbreeders known to exist in this species (primary helpers, secondary helpers, or nonhelpers) are involved. However, the likelihood that they are nonhelpers can be deduced from independent descriptions of the behavior of each of these categories. Homosexuality probably does not take place between breeding males and secondary helpers, since the former are antagonistic to the latter, engaging in "intense and prolonged fights" with them (Reyer 1986:288). Likewise for primary and secondary helpers: the former often attack and fight the latter (Reyer 1986:291). Thus, homosexuality probably occurs largely among nonhelping nonbreeders, or among secondary helpers — the latter is less likely, though, since their attentions are usually focused on feeding females, often as potential mates for the next season (Reyer 1984:1170; Reyer 1980:222). Patterns of helping, breeding, and homosexual participation analogous to the bird examples also occur among mammals. In Red Foxes, for example, same-sex mounting occurs both among younger females (nonbreeders and/or helpers) and between them and older breeding females, but only a subset of each; in Bush Dogs, nonbreeders of both sexes act as helpers (Macdonald 1996:535), yet only males occasionally participate in same-sex mounting.

      10
In fact, the only possible cases of adoption by homosexual pairs are in Hooded Warblers (where some male pairs may take over nests abandoned by females after they have been parasitized or robbed by predators), Black-headed Gulls (in which adoption of eggs by male pairs has been suggested [van Rhijn and Groothuis 1985:165-66] but not yet documented), and Cheetahs (in which paired males have occasionally been observed temporarily looking after lost cubs [Caro 1994:45, 91]). Coparenting of adopted pups by two females also occurs in Northern Elephant Seals, Gray Seals, and Spotted Seals, although the two females do not appear to have a "pair-bonded" or sexual relationship with each other.
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      11
For additional examples, see Squirrel Monkey, Common Murre, and Herring Gull. Another type of "helper" arrangement involves hierarchical societies in which only a small fraction of animals breed and the remainder assist them, often in a complex "caste" system in which each class of nonbreeders has its own specialized duties. This is typical of many social insects such as ants or honeybees, but is also found in some mammals such as naked mole-rats. Again, there is no particular association of homosexuality with these systems: homosexual behavior has been reported for perhaps only a handful of insect species with this type of social organization and is not specifically associated with helpers in these species. In fact, in most social insects helpers are asexual (and genetically sterile), and homosexual behavior is actually found among breeders, for example among fertile males participating in mating swarms (cf. O'Neill 1994 on Red Ants).

      12
Hanuman Langur (Srivastava et al. 1991:506). For specific evidence or argumentation against the idea that homosexual relations are a form of "kin selection" (i.e., an association between indivduals who interact with or help one another primarily because they are related and will therefore potentially be "benefiting" their own genes, albeit indirectly), see Fernandez and Reboreda 1995:323 (Greater Rhea), Afton 1993:232 (Lesser Scaup Duck), Rose 1992:104, 112 (Killer Whale), Hashimoto et al. 1996:316 (Bonobo), Ens 1998:635h (Oystercatcher), as well as the numerous species with nonincestuous homosexual relations and/or incest taboos.

      13
The general concept of a "population control" mechanism in animals would also be rejected by most biologists on theoretical grounds because it relies on the generally discredited notion of "group selection," which maintains that an animal's behavior sometimes benefits the population as a whole rather than the individual. This contradicts one of the most fundamental principles of evolutionary biology, that organisms act only in their self-interest. Some scientists, however, have strongly advocated the concept of group selection, and it remains an intriguing and controversial proposal. See, for example, Wynne-Edwards, V. C. (1986) Evolution through Group Selection (Oxford: Blackwell Scientific). For an overall critique of the notion of population regulation in humans, see Bates, D.G., and S. H. Lees (1979) "The Myth of Population Regulation," in N. A. Chagnon and W. Irons, eds., Evolutionary Biology and Human Social Behavior: An Anthropological Perspective, pp. 273-89 (North Scituate, Mass.: Duxbury Press).

      14
Damaraland mole-rat (Bennett, N.C. [1994] "Reproductive Suppression in Social Cryptomys damarensis Colonies — a Lifetime of Socially-Induced Sterility in Males and Females," Journal of Zoology, London 234:25-39); Killer Whale (Olesiuk et al. 1990:209). Long-term study of a stable Silver Gull population revealed that 93 percent of all eggs fail to produce birds that survive to breed, only 3 percent of the birds produce half of all surviving offspring, and 84-86 percent of the birds never produce any offspring who go on to breed themselves. In a number of other bird species, the proportion of "noncontributing" individuals is similarly high, ranging from 62-87 percent (Mills 1991:1525-26). Species with more than 50 percent nonbreeders in at least one sex, at any given time, include Bison (54 percent; based on figures in Lott 1981:98), Regent Bowerbirds (67 percent; based on figures in Lenz 1994:264, 267), Pronghorns (75 percent; based on figures in Kitchen 1974:11, 48, 50), and Grant's Gazelles (92 percent; based on figures in table 2, Walther 1972:358). See pp. 196-199 for further examples.

      15
Mammals (Macdonald, D. W., ed. [1993] The Encyclopedia of Mammals, pp. 633, 646, 654, 656-57, 722-23 [New York: Facts on File]); Birds (Piersma, T. [1996] "Scolopacidae [Snipes, Sandpipers, and Phalaropes]," p. 476, in J. del Hoyo, A. Elliott, and J. Sargatal, eds., Handbook of the Birds of the World, vol. 3: Hoatzin to Auks, pp. 444-533 [Barcelona: Lynx Editions]); Grouse (Bergerud, A. T. [1988] "Population Ecology of North American Grouse," in A. T. Bergerud and M. W. Gratson, eds., Adaptive Strategies and Population Ecology of Northern Grouse, pp. 578-685. [Minneapolis: University of Minnesota Press]).

      16
Nor does the occurrence of homosexual bonding in Oystercatchers fluctuate along with the environmentally induced population fluctuations that occur in this species (Heg and van Treuren 1998:689-90). On the other hand, the incidence of velvet-horn (transgendered) White-tailed Deer might be associated with overpopulation or drought cycles. Anecdotal reports from ranchers and longtime residents of some regions suggest that the occurrence of such Deer (who are infertile) is cyclic and related to the ending of drought periods (Thomas et al. 1970:3). Scientists studying one population found that, overall, the reproductive rate was not reduced by the presence of so many nonbreeding bucks (ibid., p. 19) — in fact, their data show that such populations actually had elevated reproductive rates. However, this skew might accord with a population regulation /fluctuation hypothesis. In populations with significant numbers of velvet-horns, there were higher ovulation rates, pregnancy rates, and numbers of does with fawns among both adult and yearling females (at least one of which — the ovulation rate for adult females in 1960 — was statistically significant). Scientists were in fact puzzled over this apparently "opposite" finding: "the results are contrary to that expected if reproduction ... was adversely affected" by the presence of velvet-horns in the herd (ibid., p. 17). In fact, we might expect a slightly delayed, rather than immediate, effect on the number of velvet-horns if their prevalence is a response to population pressure. In 1959-61 the population in this region was significantly elevated, and velvet-horn numbers actually peaked several years later in 1962 (at 9.4 percent). Taylor et al. do report periods of drought and overpopulation in the Deer herds of this region during this time (ibid., p. 25). In addition, if the overall reproductive rate is the same between populations with and without velvet-horns, the effect of the velvet-horns could still be to reduce population growth during times when the population is in fact increasing at a faster rate. Of course, much more systematic long-term investigation is required before any conclusions can be drawn about these possible connections.
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      17
Tallies and designations of threatened species are based on the official roster of the World Conservation Union. The three categories (critically endangered, endangered, and vulnerable) represent points along a continuum, based on a set of five quantitative criteria that encompass the species' rate of population decline, restricted geographic distribution, extent of population fluctuation, age distribution, effects of human disturbances (pollutants, introduced species, exploitation), and so on. See Baillie, J., and B. Groombridge, eds. (1996) 1996 IUCN Red List of Threatened Animals (Gland, Switzerland, and Cambridge, UK: IUCN-World Conservation Union).

      18
Needless to say, the near extinction of this New Zealand bird is not a result of homosexuality in this species, but rather is due to the destructive effects of human activities — habitat loss because of drainage and hydroelectric development, as well as severe depletion by nonnative species introduced to the islands (Reed 1993:771).

      19
For a review of some of these strategies, and information on other possible mechanisms, see the discussion in the following section "Nonreproductive and Alternative Heterosexualities in Animals," as well as the following references: Cohen, M. N., R. S. Malpass, and H. G. Klein, eds. (1980) Biosocial Mechanisms of Population Regulation (New Haven: Yale University Press); Wilson, E. O. (1975) Sociobiology: The New Synthesis, pp. 82-90 (Cambridge, Mass.: Belknap Press); Wynne-Edwards, V. C. (1965) "Social Organization as a Population Regulator," in P. Ellis, ed., Social Organization of Animal Communities, pp. 173-80, Symposia of the Zoological Society of London no. 14 (London: Academic Press); Wynne-Edwards, V. C. (1959) "The Control of Population-Density Through Social Behavior: A Hypothesis," Ibis 101:436-41.

      20
For various statements of this hypothesis, see Hutchinson, "A Speculative Consideration of Certain Possible Forms of Sexual Selection in Man"; Kirsch and Rodman, "Selection and Sexuality: The Darwinian View of Homosexuality"; for a refutation, see Futuyama and Risch, "Sexual Orientation, Sociobiology, and Evolution." It is also possible that the homosexual gene would be recessive, i.e., not expressed when combined with the heterosexual gene — such individuals would therefore not be bisexual, but could still have a reproductive advantage. However, in the absence of any actual genetic information, there is no way to evaluate this version of the hypothesis, since individuals with a recessive homosexual gene would presumably be (superficially) indistinguishable from those with two heterosexual genes (for an alternate view and several other versions of this hypothesis, see McKnight, J. [1997] Straight Science? Homosexuality, Evolution, and Adaptation [London: Routledge]). Therefore, the following discussion is confined to assessing the version in which such individuals are actually behaviorally bisexual (e.g., Weinrich's 1987 version). In the spirit of the "bisexual superiority" hypothesis, see also Caldwell and Caldwell's (1967:15) suggestion that bisexuality in Bottlenose Dolphins represents a "more evolved" state because their sexuality is neither limited to reproductive activity nor confined to partners of only one sex. These scientists suggest that Dolphins may be more advanced than humans in this regard, based on the (erroneous) belief that Dolphins do not exhibit exclusive homosexuality, or (in their words) are not "fixated on a biologically inappropriate stimulus to the exclusion of the biologically appropriate one." For more on the myth of human uniqueness with regard to exclusive homosexuality, see chapter 2.

      21
Based on data in fig. 2, Braithwaite 1981:140; on heterosexual partitioning of incubation duties, and the possible advantages of greater male participation, see O'Brien 1990:1186 and Brugger and Taborsky 1994. Another possible case of bisexual pairs being more successful at reproduction concerns the Snow Goose. Diamond (1989:101) had speculated that female pairs (in this and other species) that fertilize their eggs by mating with males might be able to produce more offspring than heterosexual pairs. However, this does not appear to be a genuine case: the initial suggestion was entirely conjectural and not based on actual long-term studies of the reproductive output of same-sex versus opposite-sex pairs. Furthermore, this idea was later shown to be based on faulty reasoning, since the critical factor for comparing reproductive advantage is the number of goslings produced by each female in the pair, not by the pair as a whole (as the females are usually not related to one another). See Conover (1989) and Grether and Weaver (1990) for further discussion.

      22
Ruff (Hogan-Warburg 1966:179; van Rhijn 1973:197, 1991:76; Hugie and Lank 1997:220); Greylag Goose (Lorenz 1979:59-60); Pukeko (Jamieson and Craig 1987a:1251); Guianan Cock-of-the-Rock (Trail and Koutnik 1986:211, 215); Oystercatcher (Heg and van Treuren 1998:690; Ens 1998:635).

      23
Sociable Weaver (based on data in Collias and Collias 1980:248[table 5] Bonnet Macaque (based on data in Sugiyama 1971:252, 259-60 [tables 2, 8, 9]); Asiatic Elephant (based on data in Poole et al. 1997:306-7 [fig.5]); Japanese Macaque (Hanby 1974:838; Vasey 1996 and personal communication).

      24
Some "exclusively lesbian" females copulate with males to fertilize their eggs and thus are technically bisexual in their sexual behavior. However, in terms of pair-bonding these females only choose other females as partners, and therefore I follow Mills in not classifying these individuals as bisexual for the purpose of assessing their reproductive output. However, since exclusively homosexual females produce even fewer offspring than bisexual ones, including them in the bisexual category would not alter the overall conclusion that bisexual females are less prolific breeders.

      25
Silver Gull (Mills 1991:1525).

      26
Silver Gull (Mills 1989:397-98 [table 23.5]).

      27
Kirsch and Rodman (1982:189) state that "it would be difficult to construct a crucial experiment" to test this hypothesis, while Futuyama and Risch (1984:158) note that "it is hard to see how some of these theories could ever be subjected to proper scientific testing." They are primarily considering investigations on human homosexuality and bisexuality, yet (as we have seen) studies of homosexuality in wild animals can often provide exactly the type of information needed to evaluate these ideas.

      28
Kirsch and Rodman, "Selection and Sexuality," p. 189.
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      29
The few studies that have been conducted on bisexuality and reproductive output in humans also tend to agree with the Silver Gull (and other animal) findings. Two surveys of bisexual women (in Los Angeles and the UK) found that they had either less or statistically equivalent numbers of children over their lifetime than did exclusively heterosexual women (one study did find that before the age of 25, bisexual women generally have more children than heterosexual women, but this difference evens out once lifetime reproductive rates are considered). (Baker, R. R., and M. A. Bellis [1995] Human Sperm Competition: Copulation, Masturbation, and Infidelity, pp. 117-18 [London: Chapman and Hall]; Essock-Vitale, S. M., and M. T. McGuire [1985] "Women's Lives Viewed from an Evolutionary Perspective: I. Sexual Histories, Reproductive Success, and Demographic Characteristics of a Random Subsample of American Women," Ethology and Sociobiology 6:137-54.) This is one of the few examples of the relevant quantitative data in humans being available for testing the "bisexual superiority" hypothesis. Although Baker and Bellis (1995) address the question of how homosexuality affects reproductive output, their primary concern is in evaluating the hypothesis that bisexuality reduces rather than improves reproductive output, i.e., they are not specifically addressing the "bisexual superiority" hypothesis.

      30
Jackdaw (Lorenz 1970:202-3); Canada Goose (Allen 1934:187-88); Oystercatcher (Heg and van Treuren 1998: 688-89; Ens 1998:635); Calfbird (Snow 1972:156; Snow 1976:108); Buff-breasted Sandpiper (Myers 1989:44-45); Cheetah (Caro and Collins 1987:59, 62; Caro 1993:25, 1994:252, 304).

      31
Silver Gull (Mills 1991:1525 [table 1]); Black-headed Gull (based on table 3, van Rhijn and Groothuis 1985:161); Galah (based on figures in Rogers and McCulloch 1981:83-85). See also the discussion of sexual orientation profiles in chapter 2.

      32
Kob (Buechner and Schloeth 1965:219 [based on table 2]); Bonobo (Idani 1991:90-91 [based on tables 5-6]); Japanese Macaque (Chapais and Mignault 1991:175 [based on table II]); Pig-tailed Macaque (Tokuda et al. 1968:288, 290 [based on tables 3 and 5]).

      33
For example, an animal could participate in a large number of heterosexual copulations, only a few of which would actually lead to fertilization (not to mention successful birth or rearing of offspring), while an animal with fewer heterosexual encounters could have a higher proportion of fertilizations or successful pregnancies or could be a better parent. Moreover, females who mate repeatedly during one breeding season can only get pregnant or be fertilized once, effectively equalizing the difference between greater and lesser participation in heterosexual mating (unless promiscuity is positively correlated with parenting success). For further discussion of how copulation frequency does not necessarily reflect reproductive output, see Eberhard, W. G. (1996) Female Control: Sexual Selection by Cryptic Female Choice, especially pp. 418ff (Princeton: Princeton University Press).

      34
It should also be reiterated that detailed longitudinal studies of breeding success and sexual orientation (comparble to that done on Silver Gulls) have not been conducted on any of these species to verify possible connections between bisexuality and reproduction. Moreover, all of these cases involve homosexuality among members of only one gender, which again is inconsistent with a "bisexual superiority" hypothesis.

      35
Bonobo (Hashimoto 1997:12-13); Gorilla (Fossey 1990:460, 1983:74, 188-89); Squirrel Monkey (Mendoza and Mason 1991:476-77); Wolf (Zimen 1976:311, 1981:140); Common Tree Shrew (Kaufmann 1965:72); Bottlenose Dolphin (Ostman 1991:310). For arguments that this is not merely "displaced," "redirected," or "vicarious" heterosexuality (as Fossey [1990:460] and others have labeled it), see the discussion of the "shortage" hypothesis in chapter 4.

      36
Guianan Cock-of-the-Rock (Trail and Koutnik 1986:215); Oystercatcher (Heg and van Treuren 1998:690; D. Heg, personal communication).

      37
Kob (Buechner and Schloeth 1965:219 [table 2]).

      38
Cattle Egret (Fujioka and Yamagishi 1981:136, 139 [including tables 1, 3, 4]).

      39
See the profile of the Ruff for further details and illustrations.

      40
Ruff (Van Rhijn 1991:87; Hogan-Warburg 1966:176).

      41
Ruff (Lank et al. 1995). Nearly 30 years previously, Hogan-Warburg (1966) and van Rhijn (1973) had suggested that there might be genetic differences between various categories of males, based on the indirect evidence of their plumage and behavioral distinctions as well as the constancy of their category status. This hypothesis was subsequently confirmed by DNA and heredity studies.

      42
Red Flour Beetle (Castro et al. 1994; Serrano et al. 1991); Fruit Flies (numerous references, summarized in Finley et al. 1997). See also Hamer and Copeland (1994) on the role of genetics in human homosexuality.

      43
This has been suggested for species such as Stumptail Macaques, White-faced Capuchins, Killer Whales, Northern Elephant Seals, West Indian Manatees, Giraffes, Gray-headed Flying Foxes, Ring-billed Gulls, Black-headed Gulls, Ocher-bellied Flycatchers, Guianan Cock-of-the-Rock, Calfbirds, Superb Lyrebirds, and Adelie Penguins. In addition, in some species where homosexual behavior is classified as "play," the implication is also that it functions as practice for "real" (i.e., heterosexual) activity.

      44
Rhesus Macaque (Akers and Conaway 1979:76-77); Tree Swallow (Lombardo et al. 1994:556).

      45
In a number of species, though, homosexual activity is restricted to juvenile or younger animals (see Dagg, "Homosexual Behavior and Female-Male Mounting in Mammals," for a survey of such cases).

      46
See Baker and Bellis, Human Sperm Competition, pp. 118-19, where this "explanation" is proposed for both humans and nonhumans.
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      47
Guianan Cock-of-the-Rock (Trail and Koutnik 1986:209, 215). These scientists admit that they have no specific data to support the conjecture that courtship interactions between males actually improve the subsequent heterosexual performance of younger males.

      48
See below for discussion and refutation of the (related) idea that homosexuality is a form of courtship "disruption" in this species.

      49
See Rose et al. (1991:188) for a statement to this effect concerning Northern Elephant Seals. The Ocher-bellied Flycatcher is another species where the relative infrequency of this behavior is curiously at odds with its putative "practice" function (see Westcott and Smith [1994:681] for the suggestion that courtship interactions between males in this species may allow younger birds to gain courtship experience).

      50
Sage Grouse (Patterson 1952:153-54); Pandolfi, M. (1996) "Play Activity in Young Montagu's Harriers (Circus pygargus)," Auk 113:935-38.

      51
For a similar conclusion regarding this "explanation" for primates, see Vasey, "Homosexual Behavior in Primates," p. 192. See also Wagner (1996:212) on Razorbills.

      52
The only example specifically involving females is the Ring-billed Gull, and notably in this case it is experience with parenting or pair-bonding, not sexual behavior, that females are claimed to acquire through homosexual partnerships (Fox and Boersma 1983:555).

      53
On the myth of female passivity in sexual interactions, as well as the generally sexist interpretations of female behavior and physiology in this regard, see Eberhard, Female Control, pp. 34-41, 238, 420-21; Batten, M. (1992) Sexual Strategies (New York: Putnam's); Gowaty, P. A. (1997) "Principles of Females' Perspectives in Avian Behavioral Ecology," Journal of Avian Biology 28:95-102; and the numerous other references in note 10, chapter 3.

      54
For examples of scientists who have argued (or suggested) that homosexuality promotes or strengthens social bonds or general social cohesion and stability, see Kano 1992:192 (Bonobo); Yamagiwa 1987a:1, 23, 1987b:37, Robbins 1996:944 (Gorilla); Weber and Vogel 1970:79 (Hanuman Langur); Reinhardt et al. 1986:55 (Rhesus Macaque); Rose 1992:97-98, 116-17 (Killer Whale); Coe 1967:319 (Giraffe); Nelson 1965:552 (Gray-headed Flying Fox); Heg and van Treuren 1998:688, Ens 1998:635 (Oystercatcher); Sauer 1972:735 (Ostrich); Rogers and McCulloch 1981:90 (Galah). One scientist suggests that homosexual activity in Bonobos, although promoting bonding between same-sex individuals, actually serves a more important role in heterosexual relations: "Homosexual activity became a way of tying males and females together in larger aggregations" (de Waal 1997:138); for a refutation of this type of heterocentric interpretation, see Parish (1996:65). For examples of homosexuality claimed to be a strategy of alliance or coalition building, including for the purpose of acquiring heterosexual mates, see Kano 1992, Idani 1991 (Bonobo); Vasey 1996 (Japanese Macaque, other species); Bernstein 1980:40 (Stumptail Macaque); Smuts and Watanabe 1990 (Savanna Baboon); Colmenares 1991 (Hamadryas Baboon); R. Wrangham and S. B. Hrdy, in Weinrich 1980:291 (Gelada Baboon, Hanuman Langur); Wells 1991:218-20 (Bottlenose Dolphin).

      55
See chapter 4 for further discussion and refutation of the idea that this is the motivation (or adaptive function) for homosexual associations.

      56
Rhesus Macaque (Carpenter 1942:149); Bottlenose Dolphin (Wells 1991:220); both of these cases are highly speculative. The Rhesus example is based on an isolated observation of a single consortship and is a questionable interpretation, while the Bottlenose case is considerably more complex than it initially appears (see discussion below).

      57
Parker, G. A., and R. G. Pearson (1976) "A Possible Origin and Adaptive Significance of the Mounting Behavior Shown by Some Female Mammals in Oestrus," Journal of Natural History 10:241-45; Thompson-Handler et al. 1984:355-57 (Bonobo); African Elephant (Buss 1990); Greenshank, Golden Plover (Nethersole-Thompson 1975:55).

      58
Species in which homosexual activity among females has only been reported outside the breeding season (or when females are not in heat) include Wapiti, Barasingha, Waterbuck, and Gray-headed Flying Foxes.

      59
Japanese Macaque (Gouzoules and Goy 1983:47); Hanuman Langur (Srivastava et al. 1991:508).

      60
Hanuman Langur (Srivastava et al. 1991:508); Calfbird (Trail 1990:1849-50); Cheetah (Caro and Collins 1987:59, 62; Caro 1993:25, 1994:252, 304); Savanna Baboon (Noe 1992:295). For specific descriptions of animals of the opposite sex being "disinterested" or not attracted by homosexual activity, see Gorilla (Harcourt et al. 1981:276); White-handed Gibbon (Edwards and Todd 1991:232-33); Japanese Macaque (Wolfe 1984, Vasey 1995:190; Corradino 1990:360); Killer Whale (Jacobsen 1986:152); Gray Whale (Darling 1978:51-52); Northern Fur Seal (Bartholomew 1959:168); African Buffalo (Mloszewski 1983:186); Rufous Rat Kangaroo (Johnson 1980:356); Dwarf Cavy (Rood 1970:442); Laughing Gull (Noble and Wurm 1943:205); Sage Grouse (Scott 1942:495).

      61
Bottlenose Dolphin (Florida — Wells 1991:219-20, Wells 1995; Ecuador — Felix 1997:14; Australia — Connor et al. 1992:419, 426; Bahamas — Herzing and Johnson 1997).

      62
Squirrel Monkey (Travis and Holmes 1974:55); Stumptail Macaque (Chevalier-Skolnikoff 1976:524); Wolf (Zimen 1981:140); Savanna (Yellow) Baboon (Maxim and Buettner-Janusch 1963:176); Mountain Sheep (Geist 1971:162). For arguments against this being simple "displacement" or "redirected" (hetero)sexual activity, see chapter 4. On a related point, scientists have observed that male Oystercatchers in trios are unable to influence or "promote" homosexual activity among their female partners, yet males may suffer reproductive losses without the cooperation between females entailed by such same-sex activity (Heg and van Treuren 1998:690). Thus, males are essentially powerless to cultivate homosexual activity in females even when this activity may benefit them.
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      63
Dagg, "Homosexual Behavior and Female-Male Mounting in Mammals," p. 179.

      64
The one exception is R. Wrangham (quoted in Weinrich 1980:291), who suggests that male Gelada Baboons may essentially "perform" homosexual mounts in front of, and for the benefit of, females to demonstrate their mating "prowess." This activity is not, however, claimed to be sexually stimulating for females in the same way that female homosexuality is claimed to be for males.

      65
See discussion in chapter 4.

      66
Kittiwake (Coulson and Thomas 1985); Western Gull (Hunt and Hunt 1977); Herring Gull (Shugart et al. 1988); Silver Gull (Mills 1991); Ring-billed Gull (Ryder and Somppi 1979; Kovacs and Ryder 1983). See also chapter 4 for further evidence against the claim that female pairs in Gulls form primarily as a breeding strategy.

      67
Western Gull (Hunt et al. 1984); Black-winged Stilt (Kitagawa 1988); Lesser Scaup Duck (Afton 1993; Munro 1941); Acorn Woodpecker (W. D. Koenig, personal communication); Squirrel Monkey (Ploog 1967:159-60); Greylag Goose (Lorenz 1979, 1991); Oystercatcher (Heg and van Treuren 1998). Although female coparents in Acorn Woodpeckers are "platonic" in that they do not specifically engage in courtship or sexual behavior with one another, they still participate in the group mounting displays characteristic of this species (which usually include homosexual mounting and may actually involve mounting of their coparent).

      68
Greater Rhea (Fernandez and Reboreda 1995:323, 1998:340-46); Lesser Scaup Duck (Afton 1993). The supposed "benefits" of having male nest helpers in Greater Rheas are also not readily apparent: researchers were able to demonstrate few, if any, statistically significant differences in breeding success between solitary males and those with helpers (these results are still preliminary, though, as the phenomenon has only recently been discovered; cf. Codenotti and Alvarez 1997).

      69
Snow Goose (Martin et al. 1985:262-63); Black-billed Magpie (Dunn and Hannon 1989; Buitron 1988).

      70
Superb Lyrebird (Lill 1979b, 1986). For a survey of mate and offspring desertion by one parent in a wide variety of bird species, see Szekely, T., J. N. Webb, A. I. Houston, and J. M. McNamara (1996) "An Evolutionary Approach to Offspring Desertion in Birds," especially pp. 275-76, 310, in V. Nolan Jr., and E.D. Ketterson, eds., Current Ornithology, vol. 13, pp. 271-330 (New York: Plenum Press). For a summary of the effects of mate removal in more than 15 bird species, see Bart, J., and A. Tornes (1989) "Importance of Monogamous Male Birds in Determining Reproductive Success: Evidence for House Wrens and a Review of Male-Removal Studies," Behavioral Ecology and Sociobiology 24:109-16.

      71
Calfbird (Snow 1972:156, 1976:108); Japanese Macaque (Vasey 1998:13-14, 16); Oystercatcher (Heg and van Treuren 1998:688-89; Ens 1998:635); Jackdaw (Lorenz 1970:202-3); Lesser Scaup Duck (Munro 1941:130 — 31); Canada Goose (Allen 1934:187-88).

      72
See, for example, Srivastava et al. (1991:508-9) on female Hanuman Langurs, Huynen (1997:211) on female Rhesus Macaques, Gibson and Bradbury (1986:396) on female Sage Grouse, Jamieson and Craig (1987a:1252) on male Pukeko, and Wagner (1996:213) on male Razorbills.

      73
See Gouzoules and Goy (1983:47) for an explicit refutation of this hypothesis in Japanese Macaques, and Vasey, "Homosexual Behavior in Primates," for a more general refutation for primates. See also the discussion of mountee facilitation or initiation of homosexual interactions in chapters 3 and 4.

      74
Pukeko (Jamieson and Craig 1987a:1252, 1987b:321-23; Jamieson et al. 1994:275-76); Ocher-bellied Flycatcher: only 4 out of 12 courtship interactions between males occurred when a female was present (Westcott and Smith 1994:680); Guianan Cock-of-the-Rock (Trail and Koutnik 1986).

      75
Buff-breasted Sandpiper (Myers 1989:44-45; Pruett-Jones 1988:1745-47; Lanctot and Laredo 1994:9).

      76
A. P. Moller, in Lombardo et al. 1994:556 (Tree Swallow).

      77
As pointed out by Lombardo et al. (1994:556). In Tree Swallows, there are further arguments that reproductively oriented "sperm-swapping" is probably not involved. In one observation of homosexual mating in this species, the bird that other males were copulating with was already tending chicks, i.e., his mate could no longer be fertilized (the homosexual copulations occurred fairly late in the breeding season). Although some females may still have been fertile at that point because they had not yet laid eggs (M. P. Lombardo, personal communication), and reproductive copulations can occur fairly late in the season in this species (Robertson et al. 1992:11), it seems unlikely that homosexual matings are generally timed to take advantage of reproductive opportunities. In particular, they do not appear to be more prevalent earlier in the breeding season when putative "sperm-swapping" would be more likely to result in fertilizations (Lombardo, personal communication).

      78
Pukeko: See Craig (1980:593, 601-2) for speculation on the "possible swapping of sperm during female homosexual cloacal contacts" as well as synchronization of egg laying. On the mechanisms that independently insure obscured paternity and shared parenting, see Jamieson et al. 1994:274-76; Jamieson and Craig 1987b:323-25.

      79
Best, R. L<., and M. A. O'Brien (1967) The Book of Leinster, vol. 5, lines 35670-35710. (Dublin: Dublin Institute for Advanced Studies); Greene, D. (1976) "The 'Act of Truth' in a Middle-Irish Story," Saga och Sed (Kungliga Gustav Adolfs Akademiens Arsbok) 1976:30-37.

      80
Boswell, J. (1994) Same-Sex Unions in Premodern Europe, pp. xxviii — xxix (New York: Villard Books). In discussing this story, Greene (1976:33-34) cites several "extremely rare" examples from the late 1800s, of questionable validity, in which women supposedly became pregnant from homosexual activity in this way. Regardless of whether conception by this means has been "documented" or is even biologically possible, what stands out in these descriptions of both human and animal homosexuality is their concern with heterosexuality. Namely, the putative role of same-sex activity in facilitating insemination is emphasized, and there is an insistence on ascribing a reproductive function to homosexual activity.
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      81
For a good summary and survey of some current strains of thought in this area, see Abramson, P. A., and S. D. Pinkerton, eds. (1995) Sexual Nature, Sexual Culture (Chicago: University of Chicago Press).

      82
African Elephant (Sikes 1971:266).

      83
Cordero, A. (1995) "Correlates of Male Mating Success in Two Natural Populations of the Damselfly Ischnura graellsii (Odonata: Coenagrionidae)," Ecological Entomology 20:213-22.

      84
See the profiles for more information and references. Among those 48 species in which homosexuality has been documented and quantitative information on nonbreeders is available, an average of half of the population (or of one sex) does not participate in reproduction (independent of homosexuality).

      85
Squirrel Monkey (Baldwin and Baldwin 1981:295; Baldwin 1968:296, 311); Grizzly Bear (Craighead et al. 1995:139).

      86
Chalmers, N. R. (1968) "Group Composition, Ecology, and Daily Activities of Free-Living Mangabeys in Uganda," Folia Primatologica 8:247-62; Musk-ox (Gray 1973:170-71).

      87
Searcy, W. A., and K. Yasukawa (1995) Polygyny and Sexual Selection in Red-winged Blackbirds, pp. 6, 169 (Princeton: Princeton University Press). For the other species, see the profiles and the discussion of sexual orientation in chapter 2.

      88
Bennett, N. C. (1994) "Reproductive Suppression in Social Cryptomys damarensis Colonies — a Lifetime of Socially-Induced Sterility in Males and Females," Journal of Zoology, London 234:25-39; Northern Elephant Seal (Le Boeuf and Reiter 1988:351). In mole-rats, large numbers of adults are "permanently" nonbreeding, while in Northern Elephant Seals, many males simply do not survive to the relatively advanced age when breeding typically begins, and of those that do, less than half actually breed.

      89
Waser, P. M. (1978) "Postreproductive Survival and Behavior in a Free-Ranging Female Mangabey," Folia Primatologica 29:142-60; Ratnayeke, S. (1994) "The Behavior of Postreproductive Females in a Wild Population of Toque Macaques (Macaca sinica) in Sri Lanka," International Journal of Primatology 15:445-69; Bester, M. N. (1995) "Reproduction in the Female Subantarctic Fur Seal, Arctocephalus tropicalis," Marine Mammal Science 11:362-75. For further examples, see profiles of species indexed under "postreproductive individuals."

      90
Marsh, H., and T. Kasuya (1991) "An Overview of the Changes in the Role of a Female Pilot Whale With Age," in K. Pryor and K. S. Norris, eds., Dolphin Societies: Discoveries and Puzzles, pp. 281-85 (Berkeley: University of California Press).

      91
Canada Goose (Collias and Jahn 1959:505). It is not the case that these birds were simply "trying harder" to reproduce, since some of these pairs produced eggs but failed to incubate them. Rather, it appears that as nonparents, they were able to "indulge" in more sexual behavior.

      92
Birkhead, T. R., and A. P. Moller (1993) "Why Do Male Birds Stop Copulating While Their Partners Are Still Fertile?" Animal Behavior 45:105-18; Eberhard, Female Control, p. 395.

      93
Wasser, S. K., and D. P. Barash (1983) "Reproductive Suppression Among Female Mammals: Implications for Biomedecine and Sexual Selection Theory," Quarterly Review of Biology 58:513-38; Abbott, D. H. (1987) "Behaviorally Mediated Suppression of Reproduction in Female Primates," Journal of Zoology, London 213:455-70; Reyer et al. 1986 (Pied Kingfisher); Macdonald and Moehlman 1982 (Wild Dogs); Jennions, M. D., and D. W. Macdonald (1994) "Cooperative Breeding in Mammals," Trends in Ecology and Evolution 9:89-93; Creel and Macdonald 1995 (Wild Dogs); Solomon, N. G., and J.A. French, eds. (1997) Cooperative Breeding in Mammals, pp. 304-5 (Cambridge: Cambridge University Press).

      94
American Bison (Komers et al. 1994:324 [see also discussion in chapter 4]); Pied Kingfisher (Reyer et al. 1986:216); tamarins and marmosets (Snowdon, C. T. [1996] "Infant Care in Cooperatively Breeding Species," Advances in the Study of Behavior 25:643-89, especially pp. 677-80); other species (Solomon and French, Cooperative Breeding in Mammals, p. 5).

      95
Rohrbach, C. (1982) "Investigation of the Bruce Effect in the Mongolian Gerbil (Meriones unguiculatus)," Journal of Reproduction and Fertility 65:411-17.

      96
Bighorn Sheep (Geist 1971:181, 295); Red Deer (Clutton-Brock et al. 1983:371-72); Northern Quoll and other carnivorous marsupials (Dickman and Braithwaite 1992); Ruffed Grouse (Gullion 1981:379-80); Western Gull (Pyle et al. 1997:140,145); Spotted Hyena (Frank and Glickman 1994). For further discussion of the avoidance of reproduction because of its stressful and potentially injurious effects on the individual, see Hand 1981:140-42 (Laughing Gull).

      97
Wagner, R. H. (1991) "The Use of Extrapair Copulations for Mate Appraisal by Razorbills, Alca torda," Behavioral Ecology 2:198-203; Sheldon, B. C. (1993) "Sexually Transmitted Disease in Birds: Occurrence and Evolutionary Significance," Philosophical Transactions of the Royal Society of London, Series B 339:491-97; Hamilton, W. D. (1990) "Mate Choice Near or Far," American Zoologist 30:341-52; Freeland, W. J. (1976) "Pathogens and the Evolution of Primate Sociality," Biotropica 8:12-24. See also Birkhead, T. R., and A. P. Moller (1992) Sperm Competition in Birds: Evolutionary Causes and Consequences, p. 194 (London: Academic Press); Eberhard, Female Control, p. 111.

      98
Watson, L. (1981) Sea Guide to Whales of the World, p. 174 (New York: E.P. Dutton).

      99
For further discussion, see Peterson 1968, Gentry 1981 (Northern Fur Seal); Smith 1976:71 (Musk-ox).

      100
Lee and Cockburn 1985:87-90, 163-70 (Carnivorous Marsupials).
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      101
Birkhead, T. R., and A. P. Moller (1993) "Sexual Selection and the Temporal Separation of Reproductive Events: Sperm Storage Data from Reptiles, Birds, and Mammals," Biological Journal of the Linnaean Society 50:295-311; Birkhead and Moller, Sperm Competition in Birds; Shugart, G. W. (1988) "Uterovaginal Sperm-storage Glands in Sixteen Species with Comments on Morphological Differences," Auk 105:379-84; Stewart, G. R. (1972) "An Unusual Record of Sperm Storage in a Female Garter Snake (Genus Thamnophis)," Herpetologica 28:346-47; Racey, P. A. (1979) "The Prolonged Storage and Survival of Spermatozoa in Chiroptera," Journal of Reproduction and Fertility 56:391-96; Baker and Bellis, Human Sperm Competition, pp. 42-43; Eberhard, Female Control, pp. 50-61, 167-69.

      102
Sandell, M. (1990) "The Evolution of Seasonal Delayed Implantation," Quarterly Review of Biology 65:23-42; York and Scheffer 1997:680 (Northern Fur Seal); Renfree, M. B., and J. H. Calaby (1981) "Background to Delayed Implantation and Embryonic Diapause," in A. P. F. Flint, M. B. Renfree, and B. J. Weir, eds., Embryonic Diapause in Mammals, Journal of Reproduction and Fertility, supplement no. 29:1-9; Riedman, M. (1990) The Pinnipeds: Seals, Sea Lions, and Walruses, pp. 224-25 (Berkeley: University of California Press).

      103
Greylag Goose (Lorenz 1979:74).

      104
Francis, C. M., E. L. P. Anthony, J. A. Brunton, and T. H. Kunz (1994) "Lactation in Male Fruit Bats," Nature 367:691-92.

      105
McVean, G., and L. D. Hurst (1996) "Genetic Conflicts and the Paradox of Sex Determination: Three Paths to the Evolution of Female Intersexuality in a Mammal," Journal of Theoretical Biology 179:199-211; King, A. S. (1981) "Phallus," in A. S. King and J. McLelland, eds., Form and Function in Birds, vol. 2, pp. 107-47 (London: Academic Press).

      106
Walrus (Fay 1982:39-40); Layne, J.N. (1954) "The Os Clitoridis of Some North American Sciuridae," Journal of Mammalogy 35:357-66; Bray, K. (1996) "Size Is Nothing at All: Female Fish Has Novel Way to Adapt to Mate's Lack of Penis," BBC Wildlife 14(11):15.

      107
Chaffinch (Marler 1956:113-14, 163 [table XI]); African jacana (Jenni, D. A. [1996] "Jacanidae [jacanas]," p. 282, in J. del Hoyo, A. Elliott, and J. Sargatal, eds., Handbook of the Birds of the World, vol. 3: Hoatzin to Auks, pp. 276-91 [Barcelona: Lynx Edicions]). For further examples and statistics on the widespread occurrence of matings that "fail" to result in insemination, see Eberhard, Female Control, pp. 399-403.

      108
For a general survey of mating harassment in primates, see Niemeyer, C. L., and J.R. Anderson (1983) "Primate Harassment of Matings," Ethology and Sociobiology 4:205-20.

      109
Asiatic Elephant (Eisenberg et al. 1971:205). For specific examples of male and female genitalia that do not "fit," see Eberhard, W. G. (1985) Sexual Selection and Animal Genitalia (Cambridge, Mass.: Harvard University Press). On the hostility of the female's reproductive tract to sperm, see Birkhead, T. R., A. P. Moller, and W. J. Sutherland (1993) "Why Do Females Make It So Difficult for Males to Fertilize Their Eggs?" Journal of Theoretical Biology 161:51-60; Birkhead, T., and A. Moller (1993) "Female Control of Paternity," Trends in Ecology and Evolution 8:100-104; Eberhard, Female Control, pp. 331-49.

      110
Musk-ox (Smith 1976:54-55).

      111
Clutton-Brock, T. H., and G. A. Parker (1995) "Sexual Coercion in Animal Societies," Animal Behavior 49:1345-65; Smuts, B. B., and R. W. Smuts (1993) "Male Aggression and Sexual Coercion of Females in Nonhuman Primates and Other Mammals: Evidence and Theoretical Implications," Advances in the Study of Behavior 22:1-63; Palmer, C. T. (1989) "Rape in Nonhuman Animal Species: Definitions, Evidence, and Implications," Journal of Sex Research 26:355-74; McKinney et al. 1983 (Ducks).

      112
For further examples and references, see Le Boeuf and Mesnick 1991 (Northern Elephant Seal); Miller et al. 1996 (Northern Fur Seal).

      113
Pronghorn (Geist 1990:283).

      114
Besides mating during the nonbreeding season or during menstruation or pregnancy, many female mammals also copulate during anovulatory cycles, that is, menstrual cycles during which ovulation has not taken place (Baker and Bellis, Human Sperm Competition, pp. 69-70; Eberhard, Female Control, pp. 133-39).

      115
Eberhard, Female Control, pp. 3-5, 202.

      116
Birkhead et al., "Why Do Females Make It So Difficult for Males to Fertilize Their Eggs?" p. 52; Birkhead and Moller, "Female Control of Paternity," p. 101; Ginsberg, J. R., and U. W. Huck (1989) "Sperm Competition in Mammals," Trends in Ecology and Evolution 4:74-79; Eberhard, Female Control, pp. 81-94.

      117
Rodents (Voss, R. S. [1979] "Male Accessory Glands and the Evolution of Copulatory Plugs in Rodents," Occasional Papers of the Museum of Zoology, University of Michigan 689:1-27; Baumgardner, D. J., T. G. Hartung, D. K. Sawrey, D. G. Webster, and D. A. Dewsbury [1982] "Muroid Copulatory Plugs and Female Reproductive Tracts: A Comparative Investigation," Journal of Mammalogy 63:110-17); Squirrel Monkey (Srivastava et al. 1970:129-30); Hedgehogs (Reeve 1994:178; Deansley, R. [1934] "The Reproductive Processes of Certain Mammals. VI. The Reproductive Cycle of the Female Hedgehog," especially p. 267, Philosophical Transactions of the Royal Society of London, Series B 223:239-76); lemurs and other prosimians (Dixson, A. E. [1995] "Sexual Selection and the Evolution of Copulatory Behavior in Nocturnal Prosimians," in L. Alterman, G. A. Doyle, and M. K. Izard, eds., Creatures of the Dark: The Nocturnal Prosimians, pp. 93-118 [New York: Plenum Press]); Dolphins (Harrison, R. J. [1969] "Reproduction and Reproductive Organs, p. 272, in H. T. Andersen, ed., The Biology of Marine Mammals, pp. 253-348 [New York and London: Academic Press]); on "chastity plugs" in Bats, see Fenton, M. B. (1984) "Sperm Competition? The Case of Vespertilionid and Rhinolophid Bats," in Smith, R. L. (1984) Sperm Competition and the Evolution of Animal Mating Systems, pp. 573-87 (Orlando: Academic Press); Squirrels (Koprowski 1992). For additional species, as well as other examples of females removing plugs, see Eberhard, Female Control, pp. 146-55.

      118
Common Chimpanzee (Dahl et al. 1996).
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      119
Bruce, H. M. (1960) "A Block to Pregnancy in the Mouse Caused by Proximity of Strange Males," Journal of Reproduction and Fertility 1:96-103; Schwagmeyer, P. L. (1979) "The Bruce Effect: An Evaluation of Male/ Female Advantages," American Naturalist 114:932-38; Labov, J. B. (1981) "Pregnancy Blocking in Rodents: Adaptive Advantages for Females," American Naturalist 118:361-71. See also Eberhard, Female Control, pp. 162-66.

      120
Springer, S. (1948) "Oviphagous Embryos of the Sand Shark, Carcharias taurus," Copeia 1948:153-57; Gilmore, R. G., J. W. Dodrill, and P. A. Linley (1983) "Reproduction and Embryonic Development of the Sand Tiger Shark, Odontaspis taurus (Rafinesque)," Fishery Bulletin U.S. 81:201-25; Gilmore, R. G. (1991) "The Reproductive Biology of Lamnoid Sharks," Underwater Naturalist 19:64-67; Kuzmin, S. L. (1994) "Feeding Ecology of Salamandra and Mertensiella: A Review of Data and Ontogenetic Evolutionary Trends," Mertensiella 4:271-86.

      121
Geist, V. (1971) "A Behavioral Approach to the Management of Wild Ungulates," in E. Duffey and A. S. Watt, eds., The Scientific Management of Animal and Plant Communities for Conservation, pp. 413-24 (London: Blackwell).

      122
California sea lion (Le Boeuf, B. J., R. J. Whiting, and R. F. Gantt [1972] "Perinatal Behavior of Northern Elephant Seal Females and Their Young," p. 129, Behavior 43:121-56; Odell, D. K. [1970] "Premature Pupping in the California Sea Lion," in Proceedings of the Seventh Annual Conference on Biological Sonar and Diving Mammals, pp. 185-90 [Menlo Park, Calif.: Stanford Research Institute]). On selective abortion as a mechanism females use to control paternity, see Birkhead and Moller, "Female Control of Paternity," p. 102. On possible deliberate ingestion of abortifacient plants by primates, see Bewley, D. (1997) "Healing Meals?" BBC Wildlife 15(9):63; Garey, J. D. (1997) "The Consumption of Human Medicinal Plants, Including Abortifacients, by Wild Primates," American Journal of Primatology 42:111. On abortion in other species not profiled in part 2, see Stehn, R.A., and 1. J. Jannett, Jr. (1981) "Male-induced Abortion in Various Microtine Rodents," Journal of Mammalogy 62:369-72; Gosling, L. M. (1986) "Selective Abortion of Entire Litters in the Coypu: Adaptive Control of Offspring Production in Relation to Quality and Sex," American Naturalist 127:772-95; Berger, J. (1983) "Induced Abortion and Social Factors in Wild Horses," Nature 303:59-61; Kozlowski, J., and S. C. Stearns (1989) "Hypotheses for the Production of Excess Zygotes: Models of Bet-Hedging and Selective Abortion," Evolution 43:1369-77; Schadker, M. H. (1981) "Postimplantation Abortion in Pine Voles (Microtus pinetorum) Induced by Strange Males and Pheromones of Strange Males," Biology of Reproduction 25:295-97.

      123
On ovicide, see Heinsohn, R. G. (1988) "Inter-group Ovicide and Nest Destruction in Cooperatively Breeding White-winged Choughs," Animal Behavior 36:1856-58. On egg ejection, see St. Clair, C. C., J. R. Waas, R. C. St. Clair, and P. T. Boag (1995) "Unfit Mothers? Maternal Infanticide in Royal Penguins," Animal Behavior 50:1177-85.

      124
Hausfater, G., and S. B. Hrdy, eds. (1984) Infanticide: Comparative and Evolutionary Perspective (New York: Aldine Press).

      125
This strategy is also sometimes employed by females: see Acorn Woodpecker, Little Egret; and Ichikawa, N. (1995) "Male Counterstrategy Against Infanticide of the Female Giant Water Bug Lethocerus deyrollei (Hemiptera: Belostomatidae)," Journal of Insect Behavior 8:181-88; Stephens, M. L. (1982) "Mate Takeover and Possible Infanticide by a Female Northern Jacana (Jacana spinosa)" Animal Behavior 30:1253-54.

      126
Hoagland, J. L. (1995) The Black-tailed Prairie Dog: Social Life of a Burrowing Mammal (Chicago: University of Chicago Press). For further discussion of the often neglected topic of female infanticide, see Digby, L. (1995) "Infant Care, Infanticide, and Female Reproductive Strategies in Polygynous Groups of Common Marmosets (Callithrix jacchus)," Behavioral Ecology and Sociobiology 37:51-61; Digby, L., M. Y. Merrill, and E. T. Davis (1997) "Infanticide by Female Mammals. Part I: Primates," American Journal of Primatology 42:105.

      127
For general surveys of cannibalism among animals, see Elgar, M. A., and B. J. Crespi, eds. (1992) Cannibalism: Ecology and Evolution Among Diverse Taxa (Oxford: Oxford University Press); Jones, J. S. (1982) "Of Cannibals and Kin," Nature 299:202-3; Polis, G. (1981) "The Evolution and Dynamics of Intraspecific Predation," Annual Review of Ecology and Systematics 12:225-51; Fox, L. R. (1975) Cannibalism in Natural Populations," Annual Review of Ecology and Systematics 6:87-106.

      128
Daly, M., and M. I. Wilson (1981) "Abuse and Neglect of Children in Evolutionary Perspective," in R. D. Alexander and D. W. Tinkle, eds., Natural Selection and Social Behavior: Recent Research and New Theory, pp. 405-16 (New York: Chiron Press); Reite, M., and N.G. Caine, eds., (1983) Child Abuse: The Nonhuman Primate Data. Monographs in Primatology, vol.1 (New York: Alan R. Liss); Szekely et al., "An Evolutionary Approach to Offspring Desertion in Birds."

      129
Stoleson, S. H., and S. R. Beissinger (1995) "Hatching Asynchrony and the Onset of Incubation in Birds, Revisited: When Is the Critical Period?" in D. M. Power, ed., Current Ornithology, vol. 12, pp. 191-270 (New York: Plenum Press); Evans, R. M., and S. C. Lee (1991) "Terminal-Egg Neglect: Brood Reduction Strategy or Cost of Asynchronous Hatching?" Acta XX Congressus Internationalis Ornithologici (Proceedings of the 20th International Ornithological Congress, Christchurch, New Zealand), vol. 3, pp. 1734-40 (Wellington, NZ: New Zealand Ornithological Trust Board); Mock, D. W. (1984) "Siblicidal Aggression and Resource Monopolization in Birds," Science 225:731-32; O'Connor, R. J. (1978) "Brood Reduction in Birds: Selection for Fratricide, Infanticide, or Suicide?" Animal Behavior 26:79-96.
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      130
Skeel and Mallory (1996) "Whimbrel (Numenius phaerops)" in A. Poole and F. Gill, eds., The Birds of North America: Life Histories for the 21st Century, no. 219, p. 17 (Philadelphia: Academy of Natural Sciences; Washington, D.C.: American Ornithologists' Union); Skutch, A. F. (1976) Parent Birds and Their Young, pp. 349-50 (Austin: University of Texas Press); Anthonisen, K., C. Krokene, and J. T. Lifjeld (1997) "Brood Division Is Associated with Fledgling Dispersion in the Bluethroat (Luscinia s. svecica)," Auk 114:553-61; Szekely et al., "An Evolutionary Approach to Offspring Desertion in Birds," pp. 275-76.

      131
See discussion on p. 171 and the references in note 7 (this chapter).

      132
Pierotti and Murphy 1987 (Western Gull/Kittiwake); Redondo, T., E. S. Tortosa, and L. A. de Reyna (1995) "Nest Switching and Alloparental Care in Colonial White Storks," Animal Behavior 49:1097-110; Tella, J. L., M. G. Forero, J. A. Donazar, J. J. Negro, and F. Hiraldo (1997) "Non-Adaptive Adoptions of Nestlings in the Colonial Lesser Kestrel: Proximate Causes and Fitness Consequences," Behavioral Ecology and Sociobiology 40:253-60. For egg transfer with adoption, see Black-billed Magpie, Caspian Tern, Cliff Swallow; for egg transfer through swallowing and regurgitation, see Vermeer, K. (1967) "Foreign Eggs in Nests of California Gulls," Wilson Bulletin 79:341; for a case of egg transfer that does not necessarily involve adoption, see Truslow, F. K. (1967) "Egg-Carrying by the Pileated Woodpecker," Living Bird 6:227-36.

      133
For further examples of animals caring for offspring other than their own, see the index and the following articles: Riedman, M. L. (1982) "The Evolution of Alloparental Care and Adoption in Mammals and Birds," Quarterly Review of Biology 57:405-35; Lank, D. B., M. A. Bousfield, F. Cooke, and R. F. Rockwell (1991) "Why Do Snow Geese Adopt Eggs?" Behavioral Ecology and Sociobiology 2:181-87; Andersson, M. (1984) "Brood Parasitism Within Species," in C. J. Barnard, ed., Producers and Scroungers: Strategies of Exploitation and Parasitism, pp. 195-228 (London: Croom Helm); Yom-Tov, Y. (1980) "Intraspecific Nest Parasitism in Birds," Biological Reviews 55:93-108; Quiatt, D. (1979) "Aunts and Mothers: Adaptive Implications of Allo-maternal Behavior of Nonhuman Primates," American Anthropologist 81:310-19; Packer, C., S. Lewis, and A. Pusey (1992) "A Comparative Analysis of Non-Offspring Nursing," Animal Behavior 43:265-81; Solomon and French, Cooperative Breeding in Mammals, especially pp. 335-63.

      134
For surveys of various types of mating systems, see Rowland, R. (1966) Comparative Biology of Reproduction in Mammals (Orlando: Academic Press); Slater, P. J. B., and T. R. Halliday, eds. (1994) Behavior and Evolution (Cambridge: Cambridge University Press); Clutton-Brock, T. G. (1989) "Mammalian Mating Systems," Proceedings of the Royal Society of London, Series B 235:339-72.

      135
See, for example, Palombit (1994a,b, 1996), especially with regard to reevaluating the nature and diversity of pair-bonding, fidelity, and monogamy in Gibbons. It should also be pointed out that because the occurrence of infidelity between pair-bonded partners has only been appreciated relatively recently, the term monogamy is often used in the zoological literature simply as a synonym for pair-bonding.

      136
Monogamy (absolute, or near absolute): Gyllensten, U. B., S. Jakobsson, and H. Temrin (1990) "No Evidence for Illegitimate Young in Monogamous and Polygynous Warblers," Nature 343:168-70; Holthuijzen, A. M. A. (1992) "Frequency and Timing of Copulations in the Prairie Falcon," Wilson Bulletin 104:333-38; Decker, M. D., P. G. Parker, D. J. Minchella, and K. N. Rabenold (1993) "Monogamy in Black Vultures: Genetic Evidence from DNA Fingerprinting," Behavioral Ecology 4:29-35; Vincent, A. C. J., and L. M. Sadler (1995) "Faithful Pair Bonds in Wild Seahorses, Hippocampus whitei," Animal Behavior 50:1557-69; Mauck, R. A., T. A. Waite, and P. G. Parker (1995) "Monogamy in Leach's Storm-Petrel: DNA-Fingerprinting Evidence," Auk 112:473 — 82; Haydock, J., P. G. Parker, and K. N. Rabenold (1996) "Extra-Pair Paternity Uncommon in the Cooperatively Breeding Bicolored Wren," Behavioral Ecology and Sociobiology 38:1-16; Fleischer, R. C., C. L. Tarr, E. S. Morton, A. Sangmeister, and K. C. Derrickson (1997) "Mating System of the Dusky Antbird, a Tropical Passerine, as Assessed by DNA Fingerprinting," Condor 99:512-14; Piper, W. H., D. C. Evers, M.W. Meyer, K. B. Tischler, J. D. Kaplan, and R. C. Fleischer (1997) "Genetic Monogamy in the Common Loon (Gavia immer )," Behavioral Ecology and Sociobiology 41:25-31; Kleiman, D. G. (1977) "Monogamy in Mammals," Quarterly Review of Biology 52:39-69; Foltz, D.W (1981) "Genetic Evidence for Long-Term Monogamy in a Small Rodent, Peromyscus polionotus," American Naturalist 117:665-75; Ribble, D. O. (1991) "The Monogamous Mating System of Peromyscus californicus As Revealed by DNA Fingerprinting," Behavioral Ecology and Sociobiology 29:161-66; Brotherton, P. N. M., J. M. Pemberton, P. E. Komers, and G. Malarky (1997) "Genetic and Behavioral Evidence of Monogamy in a Mammal, Kirk's Dik-dik (Madoqua kirkii)," Proceedings of the Royal Society of London, Series B 264:675-81. Infidelity or nonmonogamy: Gladstone, D. E. (1979) "Promiscuity in Monogamous Colonial Birds," American Naturalist 114:545-57; Gowaty, P. A., and D. W. Mock, eds., (1985) Avian Monogamy (Washington, D.C.: American Ornithologists' Union); Birkhead, T. R., L. Atkin, and A. P. Moller (1986) "Copulation Behavior of Birds," Behavior 101:101-38; Westneat, D. E., P. W. Sherman, and M. L. Morton (1990) "The Ecology and Evolution of Extra-pair Copulations in Birds," Current Ornithology 7:331-69; Black, J. M., ed. (1996) Partnerships in Birds: The Study of Monogamy (Oxford: Oxford University Press); Richardson, P. R. K. (1987) "Aardwolf Mating System: Overt Cuckoldry in an Apparently Monogamous Mammal," South African Journal of Science 83:405-10; Palombit 1994a,b (Gibbons); Sillero-Zubiri, C., D. Gottelli, and D. W. Macdonald (1996) "Male Philopatry, Extra-Pack Copulations, and Inbreeding Avoidance in Ethiopian Wolves (Canis simensis)," Behavioral Ecology and Sociobiology 38:331-40.

      137
As noted earlier, females also avoid STDs by refraining from genital contact during such mountings. For both Razorbills and spotted sandpipers, see Wagner, R. H. (1991) "The Use of Extrapair Copulations for Mate Appraisal by Razorbills, Alca torda" Behavioral Ecology 2:198-203. See also Koala for an example of a species with high rates of STDs in wild populations (Brown et al. 1987; Weigler et al. 1988). For other species in which significant portions of nonmonogamous matings are nonprocreative, see the profiles of Snow Goose, Lesser Scaup Duck, Common Murre, Oystercatcher, Silver Gull, and Swallows.
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      138
In addition to pair-bonding species in which nonmonogamous or alternate parenting arrangements are adopted by some individuals, the opposite situation also occurs. In some species in which the mating arrangement is typically polygamous or in which males do not usually participate in parenting, some individuals deviate from this pattern. Monogamous pair-bonding occurs in some Gray Seals (Amos et al. 1995) and Ruffs (Cramp and Simmons 1983:391), for example, even though most individuals are polygamous in these species, while some male Mallards (Losito and Baldassarre 1996:692) and Lyrebirds (Smith 1988:37 — 38) occasionally parent their offspring even though males of these species generally do not contribute to parental duties.

      139
Based on data from 140 populations of 76 different bird species, the average divorce rate is about 20 percent; only about 11 percent of these populations have no heterosexual divorce at all or rates of less than 1 percent. See appendix 19.1 in Ens, B. J., S. Choudhury, and J. M. Black (1996) "Mate Fidelity and Divorce in Monogamous Birds," in J. M. Black, ed., Partnerships in Birds: The Study of Monogamy, pp. 344-401 (Oxford: Oxford University Press). For further discussion of divorce, see Choudhury, S. (1995) "Divorce in Birds: A Review of the Hypotheses," Animal Behavior 50:413-29; Rowley, I. (1983) "Re-Mating in Birds," in P. Bateson, ed., Mate Choice, pp. 331-60 (Cambridge: Cambridge University Press).

      140
Oystercatcher (Harris et al. 1987:47, 55); Ocellated Antbird (Willis 1973:35-36); Warthog (Cumming 1975:89-90); White-tailed Deer (Gerlach, D., S. Atwater, and J. Schnell, eds. [1994] Deer, pp. 145, 150 [Mechanicsburg, Pa.: Stackpole Books]); Snow Goose (Prevett and MacInnes 1980:25, 43).

      141
Siamang (Fox 1977:409, 413-14).

      142
Common Murre (based on figures in Hatchwell 1988:161, 164, 168); Kleiman, D. G., and D. S. Mack (1977) "A Peak in Sexual Activity During Mid-Pregnancy in the Golden Lion Tamarin, Leontopithecus rosalia (Primates: Callitrichidae)," Journal of Mammalogy 58:657-60; Proboscis Monkey (Gorzitze 1996:77).

      143
Rhesus Macaque (Rowell et al. 1964:219); Mountain Goat (Hutchins 1984:45); addax antelope (Manski, D.A. [1982] "Herding of and Sexual Advances Toward Females in Late Stages of Pregnancy in Addax Antelope, Addax nasomaculatus," Zoologische Garten 52:106-12; wildebeest (Watson, R. M. (1969) "Reproduction of Wildebeest, Connochaetes taurinus albojubatus Thomas, in the Serengeti Region, and Its Significance to Conservation," p. 292, Journal of Reproduction and Fertility, supp. 6:287-310. One scientist (Loy 1970:294) goes so far as to suggest that the term estrus (meaning, roughly, the period when the female is "in heat") should be redefined for Rhesus Macaques so as to make no reference to ovulation, since nonreproductive heterosexual behaviors are so prevalent in this species (traditionally, estrus is defined strictly in relation to the "reproductive" event of ovulation).

      144
See the index for examples of profiled species that engage in these activities. For cross-species surveys and additional examples, see also Rose et al. 1991 (Northern Elephant Seal); Robinson, S. K. (1988) "Anti-Social and Social Behavior of Adolescent Yellow-rumped Caciques (Icterinae: Cacicus cela)," Animal Behavior 36:1482-95; Thornhill, N. W. (1992) The Natural History of Inbreeding and Outbreeding: Theoretical and Empirical Perspectives (Chicago: University of Chicago Press); Krizek, G. O. (1992) "Unusual Interaction Between a Butterfly and a Beetle: 'Sexual Paraphilia' in Insects?" Tropical Lepidoptera 3(2):118; Ishikawa, H. (1985) "An Abnormal Connection Between Indolestes peregrinus and Cercion hieroglyphicum," Tombo (Tokyo) 28(1-4):39; Matsui, M., and T. Satow (1975) "Abnormal Amplexus Found in the Breeding Japanese Toad," Niigata Herpetological Journal 2:4-5; Riedman, M. (1990) The Pinnipeds: Seals, Sea Lions, and Walruses, pp. 216-17 (Berkeley: University of California Press).

      145
Lion (Eaton 1978; Bertram 1975:479); Raptors (Korpimaki et al. 1996).

      146
Oystercatcher (Heg et al. 1993:256); Kob (Buechner and Schloeth 1965:218-19).

      147
Such mounts are often described as "incomplete" or are viewed as nothing more than a component or prelude to "full" copulations. This implies that the "goal" of all sexual mounting is penetration, ejaculation, and ultimately, fertilization — certainly true for a great deal of mounting behavior, but by no means a uniform characterization of all sexual activity. For further discussion of what one biologist has aptly termed "fertilization myopia" — i.e., the narrowness and bias of most scientific descriptions of animal copulation, which focus only on "successful" matings (those that lead to fertilization) — see Eberhard, Female Control, pp. 28-34. For an example of "display" copulations in a bird species not profiled in part 2, as well as examples from other species, see Eberhard, Female Control, pp. 94-102; Strahl, S. D., and A. Schmitz (1990) "Hoatzins: Cooperative Breeding in a Folivorous Neotropical Bird," p. 145, in P. B. Stacey and W. D. Koenig, eds., Cooperative Breeding in Birds: Long-term Studies of Ecology and Behavior, pp. 131-56 (Cambridge: Cambridge University Press).

      148
For a survey of mammal species where reverse mounting occurs, see Dagg (1984). Reverse mounting usually involves the female climbing on top of the male (and rarely includes penetration [in mammals] or cloacal contact [in birds]). Because heterosexual mating in Dolphins typically occurs with the male in an upside-down position underneath the female, however, "reverse" mounting in these species involves the female assuming a position underneath the male.

      149
In addition to the references for species profiled in part 2, descriptions and discussion of masturbation in a wide variety of other animals can be found in the following articles: Shadle, A. R. (1946) "Copulation in the Porcupine," Journal of Wildlife Management 10:159-62; Ficken, M. S., and W. C. Dilger (1960) "Comments on Redirection with Examples of Avian Copulations with Substitute Objects," Animal Behavior 8:219-22; Snow, B. K. (1977) "Comparison of the Leks of Guy's Hermit Hummingbird Phaethornis guy in Costa Rica and Trinidad," Ibis 119:211-14; Buechner, H. K., and S. F. Mackler (1978) "Breeding Behavior in Captive Indian Rhinoceros," Zoologische Garten 48:305-22; Harger, M., and D. Lyon (1980) "Further Observations of Lek Behavior of the Green Hermit Hummingbird Phaethornis guy at Monteverde, Costa Rica," Ibis 122:525-30; {718} Wallis, S. J. (1983) "Sexual Behavior and Reproduction of Cercocebus albigena johnstonii in Kibale Forest, Western Uganda," International Journal of Primatology 4:153-66; Poglayen-Neuwall, I., and I. Poglayen-Neuwall (1985) "Observations of Masturbation in Two Carnivora," Zoologische Garten 1985 55:347-348; Frith, C. B., and D. W. Frith (1993) "Courtship Display of the Tooth-billed Bowerbird Scenopoeetes dentirostris and Its Behavioral and Systematic Significance," Emu 93:129-36; Post, W. (1994) "Redirected Copulation by Male Boat-tailed Grackles," Wilson Bulletin 106:770-71; Frith, C. B., and D. W. Frith (1997) "Courtship and Mating of the King of Saxony Bird of Paradise Pteridophora alberti in New Guinea with Comment on their Taxonomic Significance," Emu 97:185-93.

      150
As a rough measure of the overwhelming attention devoted to male as opposed to female genitalia, for example, the Zoological Record for 1978-97 lists 539 articles that deal with the penis, compared to only 7 for the clitoris (the Zoological Record is a comprehensive electronic database that indexes more than a million zoological source documents, including articles from over 6,000 journals worldwide; the following keywords/search terms were used in compiling this estimate: penis/penile/penial/penes, phallus/phallic, baculum, hemipenes, clitorislclitorallclitorides, (os) clitoridis).

      151
Stumptail Macaque (Goldfoot et al. 1980); Rhesus Macaque (Zumpe, D., and R. P. Michael [1968] "The Clutching Reaction and Orgasm in the Female Rhesus Monkey [Macaca mulatta]," Journal of Endocrinology 40:117-23). In what is perhaps the most extreme "experiment" of this type, female Rhesus Macaques were strapped to an apparatus made of iron and wood and forced to undergo stimulation with a dildo or "penis substitute" while their responses were monitored with electrodes (Burton, F. D. [1971] "Sexual Climax in Female Macaca mulatta," in J. Biegert and W. Leutenegger, eds., Proceedings of the 3rd International Congress of Primatology, vol. 3, pp. 180-91 [Basel: S. Karger]).

      152
For a sample of some of this debate, see Allen, M. L., and W. B. Lemmon (1981) "Orgasm in Female Primates," American Journal of Primatology 1:15-34; Rancour- Laferriere, D. (1983) "Four Adaptive Aspects of the Female Orgasm," Journal of Social and Biological Structures 6:319-33; Baker, R., and M. A. Bellis (1995) Human Sperm Competition: Copulation, Masturbation, and Infidelity, pp. 234-49 (London: Chapman and Hall); Hrdy, S.B. (1996) "The Evolution of Female Orgasms: Logic Please but No Atavism," Animal Behavior 52:851-52; Thornhill, R., and S. W. Gangstead (1996) "Human Female Copulatory Orgasm: A Human Adaptation or Phylogenetic Holdover," Animal Behavior 52:853-55. For recent discussions that sidestep the question of sexual pleasure with regard to the "function" of the clitoris, as well as in relation to a variety of specific sexual behaviors (e.g., stimulatory movements such as thrusting during intercourse, multiple ejaculations, lengthy copulations, etc.), see Baker and Bellis, Human Sperm Competition, pp. 126-31; Eberhard, Female Control, pp. 142-46, 204-45, 248-54.

      153
A similar conundrum pertains to the "function" of the male copulatory organ in birds. Most male birds do not have a penis — insemination is achieved through simple contact of male and female genital apertures — and therefore its occurrence in some birds would appear to be, from a functional standpoint, "superfluous" (which could perhaps also be said about its occurrence in all other species). Moreover, in those species that do have a phallus (about 3 percent of all birds), its precise role in ejaculation and transporting semen remains unclear (see King, A. S. [1981] "Phallus," in A. S. King and J. McLelland, eds., Form and Function in Birds, vol. 2, pp. 107-47 [London: Academic Press]; Briskie, J. V., and R. Montgomerie [1997] "Sexual Selection and the Intromittent Organ of Birds," Journal of Avian Biology 28:73-86). In ratites such as Ostriches, Rheas, and Emus, as well as in Ducks and Geese, for example, the penis does not have an orifice connected to the male's internal reproductive organs, and he simply ejaculates through his cloaca (at the base of the penis) as do all other male birds without a phallus. Although it carries a groove on its outside surface that may help direct semen during penetration, the penis does not transport semen internally. Moreover, in some birds such as buffalo weavers, the phallus has no such groove whatsoever (nor any internal ducts) and its role in sperm transport is even less clear. Consequently, the phallus's reproductive "function" in these species is nearly as puzzling to biologists as that of the clitoris — the possibility that it could give sexual pleasure (to male and/or female) is rarely, if ever, even considered. Indeed, it is perhaps just as appropriate to speak of a male "clitoris" as it is of an actual "penis" in these cases, since the anatomy and function(s) of this organ may not be directly related to insemination (i.e., sperm transport). In addition, display of the phallus may also be an important element of courtship (as opposed to copulatory) activity in some species, as in the male Ostrich's "penis-swinging" ceremony (Sauer and Sauer 1966:56-57) and possible penile displays in the white-billed buffalo weaver (Birkhead, T. R., M. T. Stanback, and R. E. Simmons [1993] "The Phalloid Organ of Buffalo Weavers Bubalornis," p. 330, Ibis 135:326-31).

      154
Scientists who have recognized that sexual pleasure (or related aspects such as sexual arousal, gratification, or libido, and/or sexual, affectionate, or "erotic" attraction) may play a significant role in homosexual and /or heterosexual interactions include: primates (Wolfe, "Human Evolution and the Sexual Behavior of Female Primates," p. 144; Vasey, "Homosexual Behavior in Primates," p. 196); Bonobo (Kano 1992:195-96, 1990:66; Thompson-Handler et al. 1984; de Waal 1995:45-46, 1997:1,4,104, 111, 158); Orang-utan (Maple 1980: 158-59); Rhesus Macaque (Hamilton 1914:317-18; Akers and Conaway 1979:78-79; Erwin and Maple 1976:13); Japanese Macaque (Vasey 1996); Stumptail Macaque (Chevalier-Skolnikoff 1976:525); Killer Whale (Rose 1992:116-17); Gray Whale (Darling 1978:60; 1977:10); Northern Elephant Seal (Rose et al. 1991:186); African Elephant (Buss 1990:20); Silver Gull (Mills 1994:57-58); Laughing Gull (Hand 1981:139-40); Sage Grouse (Scott 1942:495). See also M. O'Neil's and J. D. Paterson's replies to Small (Small, M. F. (1988) "Female Primate Sexual Behavior and Conception: Are There Really Sperm to Spare?" pp. 91-92, Current Anthropology 29:81-100), and P. Vasey's recent comments in Adler, T. (1996) "Animals' Fancies: Why Members of Some Species Prefer Their Own Sex," Science News 151:8-9.
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      155
Birkhead, T. (1995) "The Birds in the Trees Do It," BBC Wildlife 13(2):46-50; Brown-headed Cowbird (Rothstein et al. 1986:127-28).

      156
For some specific examples, see Marais 1922/1969:196-97 (Savanna Baboon); Fradrich 1965:379 (Warthog); Greenhall 1965:450 (Vampire Bat); Kear 1972:85-86 (Swans); Kharitonov and Zubakin 1984:103 (Black-headed Gull), Coulson and Thomas 1985:20 (Kittiwake); Nuechterlein and Storer 1989:341 (Grebes); Szekely et al., "An Evolutionary Approach to Offspring Desertion in Birds," pp. 272-73.

      157
Common Murre (Birkhead and Nettleship 1984:2123-25).

      158
Virtually any of the references provided in the preceding notes will offer a sense of the ongoing debate and confusion about the "function" of each of these phenomena. For further examples, see: Adoption — Hansen, T. F. (1995) "Does Adoption Make Evolutionary Sense?" Animal Behavior 51: 474-75.
      Nonreproductive copulations — Hatchwell 1988 (Common Murre); Small, "Female Primate Sexual Behavior and Conception."
      Multiple copulations — Gowaty, P. A. (1996) "Battles of the Sexes and Origins of Monogamy," in J. M. Black, ed., Partnerships in Birds: The Study of Monogamy, pp. 21-52 (Oxford: Oxford University Press); Hunter, F. M., M. Petrie, M. Otronen, T. Birkhead, and A. P. Moller (1993) "Why Do Females Copulate Repeatedly With One Male?" Trends in Ecology and Evolution 8:21-26; Petrie, M. (1992) "Copulation Behavior in Birds: Why Do Females Copulate More Than Once with the Same Male?" Animal Behavior 44:790-92.
      Infanticide — Hrdy, S. B., C. Janson, and C. van Schaik (1994/1995) "Infanticide: Let's Not Throw Out the Baby with the Bath Water," Evolutionary Anthropology 3:151-54; Sussman, R. W., J. M. Cheverud, and T. Q. Bartlett (1984/1985) "Infant Killing as an Evolutionary Strategy: Reality or Myth?" Evolutionary Anthropology 3:149-51; Small, "Female Primate Sexual Behavior and Conception."
      Sex segregation (including migratory) — Miquelle et al. 1992 (Moose); Myers, J. P. (1981) "A Test of Three Hypotheses for Latitudinal Segregation of the Sexes in Wintering Birds," Canadian Journal of Zoology 59:1527-34; Stewart and DeLong 1995 (Northern Elephant Seal).
      Masturbation — Baker, R. R., and M. A. Bellis (1993) "Human Sperm Competition (Ejaculate Adjustment by Males and the Function of Masturbation," Animal Behavior 46:861-85; Wikelski, M., and S. Baurle (1996) "Pre-Copulatory Ejaculation Solves Time Constraints During Copulations in Marine Iguanas," Proceedings of the Royal Society of London, Series B 263:439-44.
      On a related point, a number of insightful analyses of otherwise puzzling aspects of sexual and reproductive behavior are now being offered by two relatively recent (and complementary) strains in biological thinking. One of these is the theory of "sperm competition," which contends that reproductive anatomy, physiology, and behavior are fundamentally shaped by the phenomenon of sperm from different males competing for fertilization by being present simultaneously in the female's reproductive tract. The other is the theory of "cryptic female choice," which argues that females themselves exert considerable influence on paternity after mating takes place by controlling whether and how sperm is utilized for fertilization. However, the complete absence of any discussion of sexual pleasure in these analyses (even where human beings are concerned) is notable. Not only is sexual pleasure as a "motivating force" compatible with many "sperm competition" and "cryptic female choice" analyses (and should therefore be considered as an important cofactor), it also offers significant insights into phenomena that continue to elude even these approaches (such as the extraordinarily high copulation rates of monogamous raptors, or mating far in advance of sperm storage periods in birds, or extrapair copulations with nonfertilizable females). For some discussion of these theories, see Baker and Bellis, Human Sperm Competition; Birkhead and Moller, Sperm Competition in Birds; Ginsberg and Huck, "Sperm Competition in Mammals"; Smith, ed., Sperm Competition and the Evolution of Animal Mating Systems; Eberhard, Female Control; Birkhead and Moller, "Female Control of Paternity." For a critique of the general male-centeredness of most sperm-competition studies, see Gowaty, P. A. (1997) "Principles of Females' Perspectives in Avian Behavioral Ecology," pp. 97-98, Journal of Avian Biology 28:95- 102. For additional observations on the limitations of sperm competition (and sexual selection) theory as applied to species such as Oystercatchers, see Ens (1998:637).

      159
On the "function" of kissing in various species, see Common Chimpanzee (Nishida 1970:51-52); Orang-utan (Rijksen 1978:204-6); Squirrel Monkey (Peters 1970); West Indian Manatee (Moore 1956; Hartman 1979:110). For similar analyses applied to human kissing in various cultures, see Eibl-Eibesfeldt, I. (1972) Love and Hate: The Natural History of Behavior Patterns, pp. 134-39 (New York: Holt, Rinehart, and Winston).

      160
cummings, e. e. (1963) Complete Poems 1913-1962, p. 556 (New York and London: Harcourt Brace Jovanovich).

      161
Dawson, W. L. (1923) The Birds of California, pp. 1090-91 (San Diego: South Moulton Co.); Jehl, J. R., Jr. (1987) "A Historical Explanation for Polyandry in Wilson's Phalarope," Auk 104:555-56. Likewise, an even more "innocuous" phenomenon — the existence of female choice in mating among a wide variety of organisms — was considered "controversial" less than 20 years ago (Eberhard, Female Control, pp. 420-21), owing to the widespread belief among biologists that females are merely passive participants or "receptacles" in mating activities. Unfortunately, this idea still persists among many biologists today (cf. Gowaty, "Principles of Females' Perspectives in Avian Behavioral Ecology"). Similarly, de Waal (1997:76) suggests that cultural biases and sexism may have contributed to scientists' denial, until 1992, of the occurrence of female dominance in Bonobos. Indeed, he points out that if any scientists had proposed this thirty years ago — along with the full set of traits now known to be a part of Bonobo life (including a richly elaborated nonreproductive sexuality) — they would simply have been "laughed out of the halls of academe" (ibid., p. 160).
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