Social Organization
Rhesus Macaques live in troops numbering up to 80–100 individuals. These are composed of several cosexual subgroups (averaging around 18 members) organized along matrilineal kinship. Males typically leave their subgroup during adolescence and establish themselves elsewhere—sometimes in all-male groups—leaving the female line of descent intact.
Description
Behavioral Expression: In female Rhesus Macaques, homosexual behavior usually takes place in a CONSORTSHIP, a type of pair-bond between two females that can last anywhere from a few days to many months (consortships are also characteristic of heterosexual relations). Two consorts follow and spend a great deal of time with each other, and participate in a wide variety of courtship, affectionate, and sexual activities; consort partners also sometimes cooperate in attacking other individuals. Females might consort with several other females, although most have only one partner. Lesbian courtship is highly distinctive, and involves five different playful pursuit games: “hide-and-seek,” in which two females peek at each other from around a tree trunk; “kiss and run,” in which one female rushes up to another and briefly kisses or nuzzles her before running off, the other in pursuit; “follow the leader,” in which the females alternate positions following one another; “lipsmack and circle,” where one female circles closer and closer to the other while making lip-smacking noises; and “present and run,” where one female invites the other to mount her and then teasingly runs off.
Courtship between two female Rhesus Macaques: a game of “hide-and-seek”
Sexual activity usually involves one female mounting the other, either in the position used for heterosexual mounting (with the mounter’s feet on the mountee’s legs), or in a position unique to homosexual mounting, in which one female climbs directly on the back of the other female and rubs her genitals on the mountee’s rump. Mounting from the side also occurs. The mounter sometimes stimulates her clitoris or has her partner do it for her, during a mount. Both females show signs of orgasm: the mounter often “pauses” the way a male does at the moment of ejaculation, while the mountee often reaches back and clutches her partner. In some consortships the two females mount each other reciprocally, although in many cases one female is consistently the mounter and her partner always the mountee. Sometimes two females also participate in sexual hugging, in which they wrap their arms and legs around each other while one or both of them engage in clitoral stimulation (including rubbing their genitals on the ground). Combined with sexual stimulation, females also kiss (touching lips or tongues), caress each other’s face, gently bite one another’s ears, and groom each other. Pregnant females sometimes participate in homosexual mounting and consortships as well. Occasionally, females behave aggressively toward a female sexual partner, as also seen in heterosexual interactions (see below).
Male Rhesus Macaques also mount each other, sometimes within a consortship as well. Mounting can include full anal penetration and ejaculation, or else simple thrusting against the partner. Sometimes the mounted male masturbates himself or his partner, and reciprocal mounting is also common (in which the two males take turns mounting each other). In some cases, one male performs a series of mounts one after the other on his partner, as in heterosexual mating. Homosexual activity may be accompanied by grooming or play-wrestling, and the two partners in a consortship can be highly affectionate toward each other, with extended periods of touching, holding, and embracing. Mounting between brothers has also been observed, as well as with males of other species such as Crab-eating Macaques (in captivity).
Several types of intersexuality occur spontaneously in Rhesus Macaques, including hermaphrodite monkeys whose internal gonads are a combination of ovaries and testes, as well as individuals that have female external genitalia but are missing a female sex chromosome and have no ovaries.
Frequency: In wild and semiwild populations of Rhesus Macaques, anywhere from 16 percent to 47 percent of mounting is between animals of the same sex; the majority of homosexual mounting (84 percent) is between males. Within a lesbian consortship, two females may mount each other more than 200 times over six months, and one couple participated in homosexual mounting more than 1,000 times during that time.
Orientation: Depending on the population, 20–90 percent of females participate in homosexual mounting and/or consortships. The majority of these females are bisexual, since they also engage in heterosexual activity (either concurrently or during other periods of their lives), and some even alternate between same-sex and opposite-sex activities in the same day. At least some females that are bisexual nevertheless do seem to prefer homosexual activity, since they return to their female consorts even after having mated with males; a female consort may also try to “win” her female partner back whenever she is temporarily with a male. In addition, some individuals participate in lesbian consortships more frequently than others and generally have much less contact with the opposite sex. Females may also be generally more receptive to same-sex advances: in one population, for example, only 6 percent of attempted homosexual mounts were rejected, compared to 29 percent of heterosexual attempts. Many male Rhesus Macaques are bisexual as well, and individuals vary in their participation in homosexual versus heterosexual activity. As with females, though, some individuals do seem to show a “preference” for homosexuality, since males may mount each other while ignoring available females. Moreover, in a detailed study of one male homosexual consortship or sexual “friendship” in captivity, both males preferred each other’s company to that of a female and chose each other as sexual partners when given a preference test (even though both were able to perform heterosexually with a female).
Nonreproductive and Alternative Heterosexualities
Rhesus Macaques are noted for their nonprocreative heterosexual behaviors. Half or more of all pregnant females engage in sexual behavior (including mating), and 12 percent of all copulations involve pregnant females. Some individual males even seem to prefer mating with females after they conceive, since nearly half of their copulations are with pregnant females. In fact, parturition itself sometimes stimulates sexual activity in attendants and onlookers, who may masturbate themselves or even mount the mother shortly after she gives birth. More than 40 percent of menstruating females also engage in sexual activity. The typical pattern for heterosexual copulation includes a large number of nonreproductive mounts, since the male may mount the female up to 100 or more times as part of each “copulation.” Although penetration may occur during each mount, usually only the final mount in the series involves ejaculation. Females often initiate sexual behavior with males and commonly experience orgasm during heterosexual mating. They may also copulate with several different males—in fact, females typically mate with more consort partners than do males, to such an extent that they experience a phenomenon known as VAGINAL OVERFLOW because of the amount of sperm they receive from such multiple matings. Rhesus Macaque females also sometimes mount males—such REVERSE mountings can account for 2–6 percent of all heterosexual mountings. Males may become sexually stimulated while a female is mounting them, masturbating or ejaculating spontaneously, and she may also achieve orgasm from rubbing during the mount. Males often masturbate to ejaculation on their own, while females have been observed fondling and sucking their own nipples. Sexual activity with nonoptimal partners also occurs: males occasionally mount their mothers or sisters (incestuous activity accounts for 12–15 percent of all sexual interactions in some populations), and adult-juvenile sexuality (primarily mounting but also fellatio, including with infants) may account for more than 15 percent of all sexual activity. A wide range of interspecies sexual interactions in captivity have also been observed (including a female Rhesus soliciting copulations from a Dog).
Male Rhesus Macaques have a yearly hormonal cycle with a distinct nonbreeding period. Females also commonly experience a postreproductive or “menopausal” stage later in their lives, in which they no longer breed but may still be sexually active. They may also continue to be valued members of the troop, even contributing to the care and raising of infants and juvenile monkeys. In addition, females of all ages participate in a type of “baby-sitting,” in which individuals—in—cluding nonbreeding monkeys—look after infants belonging to other females (and also act as “attendants” during their births). These “aunts,” as they are sometimes called (though they need not be genetically related to the mother), often protect and take care of the infants. Males (who generally do not participate in parenting) also occasionally engage in similar behavior and may even adopt orphaned infants. In some cases, though, “aunts” engage in aggressive or sexual interactions with the infants as well and may even try to “kidnap” another female’s baby. Mothers are also sometimes abusive toward their own infants—shoving, biting, and stepping on the baby’s head have all been observed, and one study showed that about 11 percent of infants are abused in their first two years of life. In addition, heterosexual relations are often characterized by aggression: males frequently attack and may severely wound females that they mate or consort with.
Sources
*asterisked references discuss homosexuality/transgender
*Akers, J. S., and C. H. Conaway (1979) “Female Homosexual Behavior in Macaca mulatta.” Archives of Sexual Behavior 8:63–80.
*Altmann, S. A. (1962) “A Field Study of the Sociobiology of Rhesus Monkeys, Macaca mulatta.” Annals of the New York Academy of Sciences 102:338-435.
*Carpenter, C. R. (1942) “Sexual Behavior of Free Ranging Rhesus Monkeys (Macaca mulatta). I. Specimens, Procedures, and Behavioral Characteristics of Estrus. II. Periodicity of Estrus, Homosexual, Autoerotic, and Non-Conformist Behavior.” Journal of Comparative Psychology 33:113–62.
Conaway, C. H., and C. B. Koford (1964) “Estrous Cycles and Mating Behavior in a Free-ranging Band of Rhesus Monkeys.” Journal of Mammalogy 45:577–88.
*Erwin, J., and T. Maple (1976) “Ambisexual Behavior with Male-Male Anal Penetration in Male Rhesus Monkeys.” Archives of Sexual Behavior 5:9–14.
*Fairbanks, L. A., M. T. McGuire, and W. Kerber (1977) “Sex and Aggression During Rhesus Monkey Group Formation.” Aggressive Behavior 3:241–49.
*Gordon, T. P., and I. S. Bernstein (1973) “Seasonal Variation in Sexual Behavior of All-Male Rhesus Troops.” American Journal of Physical Anthropology 38:221–26. *
Hamilton, G. V. (1914) “A Study of Sexual Tendencies in Monkeys and Baboons.” Journal of Animal Behavior 4:295–318.
*Huynen, M. C. (1997) “Homosexual Interactions in Female Rhesus Monkeys, Macaca mulatta.” In M. Taborsky and B. Taborsky, eds., Contributions to the XXV International Ethological Conference, p. 211. Advances in Ethology no. 32. Berlin: Blackwell Wissenschafts-Verlag.
Kaufmann, J. H. (1965) “A Three-Year Study of Mating Behavior in a Free-Ranging Band of Rhesus Monkeys.” Ecology 46:500–12.
*Kempf, E. J. (1917) “The Social and Sexual Behavior of Infrahuman Primates With Some Comparable Facts in Human Behavior.” Psychoanalytic Review 4:127–54.
*Lindburg, D. G. (1971) “The Rhesus Monkey in North India: An Ecological and Behavioral Study.” In L. A. Rosenblum, ed., Primate Behavior: Developments in Field and Laboratory Research, vol. 2, pp. 1–106. New York: Academic Press.
Loy, J. D. (1971) “Estrous Behavior of Free-Ranging Rhesus Monkeys (Macaca mulatta).” Primates 12:1-31.
———(1970) “Peri-Menstrual Sexual Behavior Among Rhesus Monkeys.” Folia Primatologica 13:286-97.
Michael, R. P., M. I. Wilson, and D. Zumpe (1974) “The Bisexual Behavior of Female Rhesus Monkeys.” In R. C. Friedman, ed., Sex Differences in Behavior, pp. 399–412. New York: John Wiley & Sons.
Missakian, E. A. (1973) “Genealogical Mating Activity in Free-Ranging Groups of Rhesus Monkeys (Macaca mulatta) on Cayo Santiago.” Behavior 45:225–41.
Partch, J. (1978) “The Socializing Role of Postreproductive Rhesus Macaque Females.” American Journal of Physical Anthropology 48:425.
*Reinhardt, V., A. Reinhardt, F. B. Bercovitch, and R. W. Goy (1986) “Does Intermale Mounting Function as a Dominance Demonstration in Rhesus Monkeys?” Folia Primatologica 47:55–60.
Rowell, T. E., R. A. Hinde, and Y. Spencer-Booth (1964) “‘Aunt’-Infant Interaction in Captive Rhesus Monkeys.” Animal Behavior 12:219–26.
*Sade, D. S. (1968) “Inhibition of Son-Mother Mating Among Free-Ranging Rhesus Monkeys.” In J. H. Masserman, ed., Animal and Human, pp. 18–38. Science and Psychoanalysis, vol. 12. New York: Grune & Stratton.
Schapiro, S. J., and G. Mitchell (1983) “Infant-Directed Abuse in a Seminatural Environment: Precipitating Factors.” In M. Reite and N. G. Caine, eds., Child Abuse: The Nonhuman Primate Data, pp. 29–48. Monographs in Primatology, vol.1. New York: Alan R. Liss.
*Sullivan, D. J., and H. P. Drobeck (1966) “True Hermaphrodism in a Rhesus Monkey.” Folia Primatologica 4:309–17.
Tilford, B. (1981) “Nondesertion of a Postreproductive Rhesus Female by Adult Male Kin.” Journal of Mammalogy 62:638–39.
Vessey, S. H., and D. B. Meikle (1984) “Free-Living Rhesus Monkeys: Adult Male Interactions with Infants and Juveniles.” In D. M. Taub, ed., Primate Paternalism, pp. 113–26. New York: Van Nostrand Reinhold.
*Weiss, G., R. F. Weick, E. Knobil, S. R. Wolman, and F. Gorstein (1973) “An X-O Anomaly and Ovarian Dysgenesis in a Rhesus Monkey.” Folia Primatologica 19:24–7.
IDENTIFICATION: A medium-sized (2-foot-long) monkey with dark or reddish brown fur, a short, almost hairless tail, and mottled black-and-red skin on the face. DISTRIBUTION: Southeast Asia and south-central China; vulnerable. HABITAT: Dense forests, including mountainous regions. STUDY AREAS: Semiwild: island of Toto-gochillo, Lake Catemaco, Mexico; captivity: Stanford University; University of Helsinki; the Netherlands Primate Center; Yerkes and Wisconsin Regional Primate Research Centers; Calcutta and Paris Zoos.
Social Organization
Few field studies of Stumptail Macaques have been conducted, so little is known of their social organization in the wild. They generally appear to live in cosexual groups of 20–50 individuals with a matrilineal organization. The mating system is probably polygamous or promiscuous, involving copulations with multiple partners and little male parental involvement.
Description
Behavioral Expression: Male Stumptails form intense sexual “friendships” with each other, within which an extraordinary variety of homosexual activities are expressed. One male may develop strong affectionate bonds with another male, as shown by their embracing, gently nibbling at each other’s mouth, and huddling together. The two partners may even sleep together, one closely hugging the other from behind while holding his partner’s penis. The affection between these males is also expressed through sexual activity, ranging from mounting to oral sex to mutual masturbation. Mounting occurs in the typical front-to-back position found in heterosexual mating; pelvic thrusting, anal penetration, and occasionally ejaculation can all be components of this activity. Fellatio or oral-genital activity involves one male licking or sucking on the penis of the other for up to two minutes at a time. This is done in a variety of positions, for example with one male behind the other or mounted on him, sucking his genitals between his legs. The males may even perform mutual fellatio in a 69 position. Males also fondle one another’s scrotum and penis, rubbing the hand up and down the shaft; again, a number of positions are used—one male may stand sideways in front of another who is sitting down, spreading his thighs to allow the seated male to masturbate him, or they may engage in mutual masturbation by backing up toward each other and fondling each other’s genitals between their legs. Sometimes male Stumptails also sit together and masturbate themselves, stimulated by the sight of one another or of a nearby heterosexual mating. The partners in a sexual friendship may be of the same age, or one may be considerably younger than the other, perhaps even an infant.
Two male Stumptail Macaques in mutual fellatio
Female Stumptails also form sexual friendships with one another. These relationships, which involve a considerable amount of affectionate behavior as well, may be a stable association between just two females, or they may be more fluid, involving a network of three females, for example, or more short-lived pairings. Sexual behavior involves mounting with intense genital stimulation and orgasm. One female will climb onto the back of her favorite partner, using a position slightly different from heterosexual mating that allows her to rub her genitals against the rump of the other female. This may also be accomplished in a front-to-back sitting position, one female pulling the other up against her belly, and the two may even end up lying or leaning back together in this configuration. Lesbian interactions are prolonged, lasting up to two minutes (a duration similar to heterosexual mating), and the females usually make numerous pelvic thrusts comparable to the amount performed by a male in a heterosexual mounting. Orgasm is striking: the mounting female tenses up, first pausing and then showing a number of body spasms; her fur stands on end, and this is combined with a characteristic frowning and round-mouthed facial expression (also found in ejaculating males) and rapid breathing sounds. She also experiences a number of intense uterine contractions lasting for nearly a minute. The female being mounted does not, apparently, have the same sort of orgasmic response, although she is in a state of high sexual arousal, and will often reach back to clutch the mounting female and even kiss her during the climax. Following orgasm, the females usually hug one another and make teeth-chattering or squeaking sounds. In some cases females can apparently reach orgasm without direct genital stimulation, particularly when they are hugging their favorite female partner in great excitement after being reunited.
A female Stumptail Macaque kissing her female partner at the climax of mounting
Frequency: Homosexual activity is common in Stumptail Macaques, accounting for as much as 25–40 percent of all sexual encounters in some captive and semi-wild groups. In one study, nearly two-thirds of this same-sex activity was between females, while in another population, all same-sex mounting was between males.
Orientation: Most Stumptail females are probably simultaneously bisexual, interspersing heterosexual activity with homosexual activity. In fact, females have been known to participate in lesbian activities when they are lactating (and possibly even during pregnancy), indicating an easy compatibility between motherhood and homosexuality in this species. Some males show a decrease in the intensity of their same-sex friendships as they get older and may begin engaging in a larger proportion of heterosexual activity as they mature. Nevertheless, most males probably continue to have some homosexual contact throughout their lives.
Nonreproductive and Alternative Heterosexualities
Male Stumptails engage in both masturbation and nonreproductive heterosexual mating. In the latter case, males have been observed mounting females without full penetration, mating with menstruating females, rubbing their genitals on the female (sometimes to ejaculation), and even stimulating the penis with their own foot while mounted on the female. Both male and female orgasm can be a component of heterosexual mating. Sometimes, however, mating is distinctly less pleasurable—especially for the female, who may collapse under the weight of the male during copulation (he may be up to twice as heavy as she is). Females are also sometimes bitten by males during mounting, resulting in shallow cuts on her shoulders and upper arms (this occurs in about 15–18 percent of copulations). More than half of all matings involve male aggression (including chasing the female, pushing or pulling her, and fighting or biting her) and/or female resistance (including running away from the male, screaming, trying to dislodge him, and fighting with him). In addition, heterosexual copulations are often harassed by other individuals (of both sexes), sometimes in spectacular outbursts of activity that involve an entire social group. This often occurs following ejaculation while the two mating animals remain attached in a “copulatory tie,” similar to that of mating Dogs.
Sources
*asterisked references discuss homosexuality/transgender
*Bernstein, I. S. (1980) “Activity Patterns in a Stumptail Macaque Group (Macaca arctoides).” Folia Primatologica 33:20–45.
*Bertrand, M. (1969) The Behavioral Repertoire of the Stumptail Macaque: A Descriptive and Comparative Study. Bibliotheca Primatologica 11. Basel: S. Karger.
*Chevalier-Skolnikoff, S. (1976) “Homosexual Behavior in a Laboratory Group of Stumptail Monkeys (Macaca arctoides): Forms, Contexts, and Possible Social Functions.” Archives of Sexual Behavior 5:511–27.
*———(1974) “Male-Female, Female-Female, and Male-Male Sexual Behavior in the Stumptail Monkey, with Special Attention to the Female Orgasm.” Archives of Sexual Behavior 3:95–116.
*Estrada, A., and R. Estrada (1978) “Changes in Social Structure and Interactions After the Introduction of a Second Group in a Free-ranging Troop of Stumptail Macaques (Macaca arctoides): Social Relations II.” Primates 19:665–80.
*Estrada, A., R. Estrada, and F. Ervin (1977) “Establishment of a Free-ranging Colony of Stumptail Macaques (Macaca arctoides): Social Relations I.” Primates 18:647–76.
*Goldfoot, D. A., H. Westerborg-van Loon, W. Groeneveld, and A. K. Slob (1980) “Behavioral and Physiological Evidence of Sexual Climax in the Female Stump-tailed Macaque (Macaca arctoides).” Science 208:1477–79.
Gouzoules, H. (1974) “Harassment of Sexual Behavior in the Stumptail Macaque, Macaca arctoides.” Folia Primatologica 22:208–17.
*Leinonen, L., I. Linnankoski, M.-L. Laakso, and R. Aulanko (1991) “Vocal Communication Between Species: Man and Macaque.” Language and Communication 11:241–62.
*Linnankoski, I., and L. M. Leinonen (1985) “Compatibility of Male and Female Sexual Behavior in Macaca arctoides.” Zeitschrift für Tierpsychologie 70:115–22.
Niemeyer, C. L., and A. S. Chamove (1983) “Motivation of Harassment of Matings in Stumptailed Macaques.” Behavior 87:298–323.
*O’Keefe, R. T., and K. Lifshitz (1985) “A Behavioral Profile for Stumptail Macaques (Macaca arctoides).” Primates 26:143–60.
*Slob, A. K., and P. E. Schenk (1986) “Heterosexual Experience and Isosexual Behavior in Laboratory-Housed Male Stump-tailed Macaques (M. arctoides).” Archives of Sexual Behavior 15:261–68.
*de Waal, F. B. M. (1989) Peacemaking Among Primates. Cambridge, Mass.: Harvard University Press.
de Waal, F. B. M., and R. Ren (1988) “Comparison of the Reconciliation Behavior of Stumptail and Rhesus Macaques.” Ethology 78:129–42.
BONNET MACAQUE
IDENTIFICATION: A grayish brown monkey with a circular “cap” of hair on the head, a prominent wrinkled brow and forehead, and a long tail (over 2 feet in males). DISTRIBUTION: Southern India. HABITAT: Forests, scrub, open areas. STUDY AREAS: Near Somanathapur Sandal Reserve and Byrankuppe (Mysore State), Dharwar, Karnataka (Tamil Nadu), and Lal Bagh (Bangalore), India; California Primate Research Center; State University of New York; subspecies M.r. diluta.
CRAB-EATING MACAQUE
IDENTIFICATION: A gray-green to reddish brown monkey with a slight pointed crest, pinkish face, and long tail. DISTRIBUTION: Southeast Asia including Indonesia, Philippines, Nicobar Islands, and introduced to Palau. HABITAT: Forests, swamps. STUDY AREAS: Angaur Island, Palau, Micronesia; Yerkes Regional Primate Research Center; University of California—Berkeley.
Social Organization
Both Bonnet and Crab-eating Macaques live in fairly large matriarchal groups containing numerous adult males and females as well as youngsters; males typically emigrate from their home group on becoming adults. Bonnet groups can be as large as 50–60 monkeys, but most average around 18–20 individuals, with four or five each of adult males and females. Male Bonnets demonstrate a strong tendency to interact and cooperate with one another, often forming supportive COALITIONS together. Crab-eating Macaques live in troops containing 40–50 individuals on average; smaller groups each contain 2–9 adult males. Large subgroups of youngsters, as well as some peripheral or solitary animals, also occur.
Description
Behavioral Expression: Male Bonnet Macaques frequently mount one another, using the same front-to-back position found in heterosexual copulation. A male may have anywhere from two to five different partners that he mounts; each male also varies in the proportion of times he mounts or is mounted. One male acted as the mountee in only 9 percent of his homosexual mountings, another did so in all of his mountings, though the average is a roughly equal proportion of mounter-mountee behavior, and reciprocal mounting occurs as well. In addition, male Bonnets engage in a wide variety of other same-sex behaviors, both affectionate and sexual, often within a coalition “bond” between them. Masturbation of another male is common in all age groups, especially younger males—one male holds or fondles the other’s penis and may even eat the semen from the resulting ejaculation (mutual masturbation also occurs). Males also sometimes grip and gently tug on each other’s scrotum; often, this is accompanied by embracing, nuzzling, grasping of the rump, tongue-clicking, and mouthing of the other’s neck or shoulders, all combined into a sort of ritualized “greeting” interaction. Another behavior, unique to homosexual interactions, involves two males rhythmically rubbing their rumps and genital areas together, often reaching back between their legs to fondle each other’s genitals. This behavior also occurs between females, as does mounting.
Homosexual mounting also occurs in male Crab-eating Macaques. In addition, male Crab-eaters may mouth and fondle the genitals and anal region of another male, including using their index finger to investigate the area. Males can also develop intense sexual friendships with one another, especially between older and younger males. In one such pair observed in captivity, affectionate embraces frequently led to sexual arousal and homosexual mounting, often accompanied by excited lip-smacking or crooning sounds; the male being mounted sometimes even turned his head to kiss his partner during a mount. Both consensual and nonconsensual mounting occurs in Crab-eating Macaques—in the former (54 percent of mounts between males), the mounted animal fully cooperates by standing still and helps support the weight of the other male (and perhaps even initiates the encounter). In nonconsensual mounts (46 percent of mounts between males), the mounting animal may corner his partner and hold him down (this also occurs in heterosexual mounting). Male Crab-eaters also occasionally engage in homosexual contact with other species. Wild Crab-eating Macaques sometimes allow male Orang-utans to perform fellatio on them, while in captivity they have been known to attempt copulation with males of a number of nonprimate species, including foxes.
An older male Bonnet Macaque in India mounting a younger male
Frequency: Homosexual mounting is very common in male Bonnet Macaques. In some populations, same-sex mounts exceed the number of heterosexual mounts by as much as four to one, and mounting between males can comprise 31 percent to 79 percent of all mounting. Sexual and affectionate behaviors between males occur in about a quarter of their interactions with one another. Female homosexual activity is somewhat less common: one study found that mounting between females occurred at rates that were two to seven times less than male-female or male-male mounting, although the rates of mutual rump rubbing with genital stimulation between females were only slightly less than between males. In Crab-eating Macaques, homosexual mounting accounts for 17–30 percent of mountings, and 10 percent of all interactions between males involve mounting (compared to nearly 50 percent of all interactions between males and females).
Orientation: Nearly all male Bonnet Macaques participate in both homosexual and heterosexual mounting, but it appears that they generally have more different male partners than female ones. Some males participate very little in homosexual activity (accounting for about 10 percent of the same-sex mountings in a population), while others may be involved in more than half of all homosexual mounts. A similar variation occurs with respect to their heterosexual participation. However, males that are the least active heterosexually are not necessarily the most active homosexually: in many cases, those males that participate in a large number of homosexual mountings also have a large number of heterosexual mountings. No quantitative information on sexual orientation is available for Crab-eaters; however, observations in captivity indicate that males engage in both homosexual and heterosexual copulation, sometimes alternating relatively frequently between the two. Furthermore, males that are “bonded” to one another show a preference for their partner that even survives separation and intervening heterosexual activity. If such males are separated from one another, they rush to embrace each other on being reunited, resuming their sexual relationship where they left off.
Nonreproductive and Alternative Heterosexualities
As noted above, heterosexual matings in Crab-eating Macaques are not always consensual: about 19 percent of such mounts are forced by the male on the female. Furthermore, male Crab-eaters sometimes severely attack females with small babies and also occasionally kill those infants to gain sexual and breeding access to the female. Both Bonnets and Crab-eaters participate in a range of nonprocreative sexual behaviors. Among Crab-eaters, females copulate during pregnancy (though usually not during the first two to three weeks), while more than half of male-female copulations do not involve ejaculation. In both species, females have multiple male partners and copulations—during one six-month period, for example, each female Crab-eater mated an average of 45 times, with some copulating more than 110 times. Female Bonnets may mate with up to three different males in succession, and females also sometimes mount males (REVERSE mounting). Male Bonnet Macaques may also manually penetrate females, inserting a finger and then licking or smelling it. Unlike in a number of other primates, in Bonnets this behavior does not appear to be simply a way of testing the sexual receptivity of the female. Both male and female Bonnets also masturbate, females sometimes employing innovative techniques (such as using objects or pulling their tail between their legs and using it to rub their labia while making pelvic thrusting movements). Crab-eating Macaques engage in an interesting form of “infidelity”: heterosexual mating typically occurs within a short-term bond or consortship. However, nearly 20 percent of all copulations in some populations are nonmonogamous: half of all females and almost three-quarters of the males “steal” matings with other partners during a consortship, but return to their original partner afterward. The social system of Bonnet Macaques may entail considerable inbreeding, and incestuous mother-son matings that produce viable offspring do occur.
Sources
*asterisked references discuss homosexuality/transgender
*Bernstein, S. (1970) “Primate Status Hierarchies.” In L. A. Rosenblum, ed., Primate Behavior: Developments in Field and Laboratory Research, vol. 1, pp. 71–109. New York: Academic Press.
Emory, G. R., and S. J. Harris (1978) “On the Directional Orientation of Female Presents in Macaca fascicularis.” Primates 19:227–29.
*Hamilton, G. V. (1914) “A Study of Sexual Tendencies in Monkeys and Baboons.” Journal of Animal Behavior 4:295–318.
*Kaufman, I. C., and L. A. Rosenblum (1966) “A Behavioral Taxonomy for Macaca nemestrina and Macaca radiata: Based on Longitudinal Observation of Family Groups in the Laboratory.” Primates 7:205–58.
*Makwana, S. C. (1980) “Observations on Population and Behavior of the Bonnet Monkey, Macaca radiata.” Comparative Physiology and Ecology 5:9–12.
Moore, J., and R. Ali (1984) “Are Dispersal and Inbreeding Avoidance Related?” Animal Behavior 32:94–112.
*Nolte, A. (1955) “Field Observations on the Daily Routine and Social Behavior of Common Indian Monkeys, with Special Reference to the Bonnet Monkey (Macaca radiata Geoffroy).” Journal of the Bombay Natural History Society 53:177–84.
Noordwijk, M. A. van (1985) “Sexual Behavior of Sumatran Long-tailed Macaques (Macaca fascicularis).” Zeitschrift für Tierpsychologie 70:277–96.
*Poirier, F. E., and E. O. Smith (1974) “The Crab-Eating Macaques (Macaca fascicularis) of Angaur Island, Palau, Micronesia.” Folia Primatologica 22:258–306.
Rahaman, H., and M. D. Parthasarathy (1969) “Studies on the Social Behavior of Bonnet Monkeys.” Primates 10:149–62.
*———(1968) “The Expressive Movements of the Bonnet Macaque.” Primates 9:259–72.
*Rasmussen, D. R. (1984) “Functional Alterations in the Social Organization of Bonnet Macaques (Macaca radiata) Induced by Ovariectomy: An Experimental Analysis.” Psychoneuroendocrinology 9:343–74.
*Silk, J. B. (1994) “Social Relationships of Male Bonnet Macaques: Male Bonding in a Matrilineal Society.” Behavior 130:271–92.
———(1993) “Does Participation in Coalitions Influence Dominance Relationships Among Male Bonnet Macaques?” Behavior 126:171–89.
Sinha, A. (1997) “Complex Tool Manufacture by a Wild Bonnet Macaque, Macaca radiata.” Folia Primatologica 68:23–25.
*Simonds, P. E. (1996) Personal communication.
*———(1965) “The Bonnet Macaque in South India.” In I. DeVore, ed., Primate Behavior: Field Studies of Monkeys and Apes, pp. 175–96. New York: Holt, Rinehart, & Winston.
*Sugiyama, Y. (1971) “Characteristics of the Social Life of Bonnet Macaques (Macaca radiata).” Primates 12:247–66.
*Thompson, N. S. (1969) “The Motivations Underlying Social Structure in Macaca irus.” Animal Behavior 17:459–67.
*———(1967) “Some Variables Affecting the Behavior of Irus Macaques in Dyadic Encounters.” Animal Behavior 15:307–11.
PIG-TAILED MACAQUE
IDENTIFICATION: A medium-sized monkey (up to 30 pounds in males) with olive-brown fur and a short, curly, nearly naked tail. DISTRIBUTION: Southeast Asia from Burma to Sumatra; vulnerable. HABITAT: Forests. STUDY AREAS: Near Mt. Kerinci, West Sumatra, Indonesia, subspecies M.n. nemestrina; Bernam River, western Malaysia; Washington and Yerkes Regional Primate Research Centers; State University of New York; Turin Zoo.
CRESTED BLACK MACAQUE
IDENTIFICATION: An entirely black monkey with a striking crest, long muzzle, high cheek and brow ridges, and a short tail. DISTRIBUTION: Sulawesi, Indonesia; endangered. HABITAT: Tropical forest. STUDY AREAS: Tangkoko-DuaSudara Nature Reserve, North Sulawesi, Indonesia; Oregon and Yerkes Regional Primate Research Centers; Woodland Park Zoological Gardens, Seattle, Washington.
Social Organization
Both of these species live in cosexual groups, containing 15–40 individuals in Pigtails and up to 40–90 individuals in Crested Black Macaques. Pig-tailed groups are matrilineal clans, in which females remain in their home (natal) group while males emigrate on reaching maturity. The heterosexual mating system is promiscuous: both sexes mate with multiple partners. Smaller Crested Black Macaque groups (6–15 individuals) may contain only one adult male.
Description
Behavioral Expression: Pig-tailed Macaques engage in homosexual mounting as well as kissing. Male Pigtails mount each other using the posture found in heterosexual mating (one male behind the other, hands grasping the loins, and feet clasping the calves of the other), sometimes with erection of the penis and pelvic thrusting (though anal penetration does not occur). Females use the same position and also occasionally thrust against their female partner; the mounting female is usually in heat. Some Pigtails engage in same-sex mounting with only one partner, while other Pigtails have several partners (as many as seven for females, though the average is three). Individuals differ as to whether they prefer mounting or being mounted in homosexual encounters: a few animals engage in only one or the other, while most exhibit a range of mounter/mountee behavior. Males may even mount each other reciprocally, exchanging positions in different mounting sessions. Same-sex kissing (mouth-to-mouth contact) occurs more often than heterosexual kissing and is most common between females. However, many female homosexual mounts are “forced” in the sense that the animal being mounted does not solicit the mounting, and aggression may also be involved: 48 percent of mounts between females are nonconsensual, compared to 18 percent of heterosexual ones. No mounts between males are forced. Some same-sex mounting is incestuous, e.g., between mother and daughter or siblings of either sex.
Crested Black Macaques also participate in male and female homosexual mounting, similar in many ways to that found in Pigtails. Females often reach back to clasp the leg of a female mounting them, which is believed to be a sign of orgasm (it also occurs in heterosexual mounting), while males being mounted by other males frequently fondle their own penis. Mounting is sometimes preceded by a gesture of invitation known as REAR-END FLIRTATION, in which one male walks by another and presents his hindquarters. Younger males often mount older ones in this species. A number of other homosexual activities occur in Crested Black Macaques. Females engage in a form of mutual masturbation unique to homosexual interactions, in which they stand side by side facing in opposite directions (draping an arm over the other’s waist) and fondle and sniff each other’s vulva, sometimes with direct clitoral stimulation. Males often participate in a form of erotic grooming: one male uses his hands, lips, and tongue to groom the other, who usually has an erection and may masturbate himself by rolling his penis between his palms or licking it (he usually eats his own semen if he ejaculates). The grooming animal is often sexually aroused, too, as evidenced by his erection. Males (especially younger ones) also use a number of ritualized erotic “greeting” gestures with one another, including embracing, face-licking or kissing, fondling or grabbing of the erect penis, mounting, and rump fingering.
Frequency: Same-sex mounting occurs frequently in Pig-tailed Macaques, accounting for 7—23 percent of all mounting activity. More than three-quarters of all kissing occurs between females. In Crested Black Macaques, about 5—8 percent of all mounting activity occurs between males. Ritualized penis-grabbing or fondling between males takes place regularly in this species and can be observed weekly, and perhaps even daily, in some wild populations.
Two female Crested Black Macaques masturbating each other
Orientation: Most Pig-tailed Macaques are probably bisexual, engaging in both same- and opposite-sex mounting. However, individuals vary along a continuum of what percentage of their activity is homosexual: for some males, it is as little as 8 percent, while for others, nearly two-thirds of their mounting activity is same-sex. Although less specific information is available for Crested Black Macaques, they appear to have a similar orientation profile: in one wild troop, for example, all males participated in both heterosexual and homosexual mounting (as well as penis-grabbing) to varying degrees.
Nonreproductive and Alternative Heterosexualities
As noted above, some heterosexual copulations in Pig-tailed Macaques are forced, in that the female is an unwilling participant. Furthermore, more than a third of aggressive interactions in Pigtails are between males and females (73 percent are directed by the male against the female). Infanticide has also been seen among captive Pigtails—in some cases, infants as young as one day old have died from head and neck injuries inflicted by adult males. In addition, a 33—year study of this species (spanning seven generations and nearly 400 individuals) found that one in eight infants is physically abused or neglected by its mother. This includes being dragged across the ground, having its fingers or tail chewed, suffering severe eye damage or blindness as a result of compulsive grooming around the eyes, having its head or body crushed on the ground, and/or being rejected, abandoned, or starved by its mother. Physical abuse accounts for about a third of all Pigtail infant injuries or deaths; it appears to run in families and is usually repeated with successive offspring. Infants can also be injured when they are kidnapped, which occurs only occasionally and is typically carried out by a nonbreeding female.
A number of nonreproductive sexual behaviors occur in these two species as well. In Pigtails, males mount nonovulating females 8—15 percent of the time, and 1—2 percent of heterosexual behavior involves females mounting males (REVERSE mounts). In addition, female Pigtails may mate with up to five different males during a single period of heat. Mother-son mountings occur as well. In both of these species, heterosexual mounting sometimes does not involve penetration: nearly a fifth of Crested Black male-female mounts, for example, are “ritualized” or non-copulatory. Male Pigtails and Crested Black Macaques also masturbate, occasionally eating their own semen, while female Crested Black Macaques sometimes masturbate by inserting a finger into the vagina and simultaneously slapping their rump with one hand. Infant and very young male Crested Blacks often mount adult females, performing pelvic thrusts and even achieving penetration. Finally, spontaneous abortions occur among Pigtails, often associated with a number of physiological changes in the female’s blood chemistry: one study in captivity found that 14 percent of pregnancies terminated in abortions (among females not otherwise at high risk for miscarriages).
Other Species
Homosexual mounting occurs in three other species of Macaques: Lion-tailed (Macaca silenus), Tonkean (Macaca tonkeana), and Moor (Macaca maurus) Macaques. In the latter two species, 11—13 percent of mounting activity is same-sex.
Sources
*asterisked references discuss homosexuality/transgender
*Bernstein, I. S. (1972) “Daily Activity Cycles and Weather Influences on a Pigtail Monkey Group.” Folia Primatologica 18:390-415.
*———(1970) “Primate Status Hierarchies.” In L. A. Rosenblum, ed., Primate Behavior: Developments in Field and Laboratory Research, vol.1, pp. 71—109. New York: Academic Press.
*———(1967) “A Field Study of the Pigtail Macaque (Macaca nemestrina).” Primates 8:217-28.
Bernstein, I. S., and S. C. Baker (1988) “Activity Patterns in a Captive Group of Celebes BlackApes (Macaca nigra).” Folia Primatologica 51:61-75.
*Bound, V., H. Shewman, and J. Sievert (1988) “The Successful Introduction of Five Male Lion-tailed Macaques (Macaca silenus) at Woodland Park Zoo.” In AAZPA Regional Conference Proceedings, pp. 122-31. Wheeling, W.Va.: American Association of Zoological Parks and Aquariums.
*Caldecott, J. 0. (1986) An Ecological and Behavioral Study of the Pig-Tailed Macaque. Basel: Karger.
*Dixson, A. F. (1977) “Observations of the Displays, Menstrual Cycles, and Sexual Behavior of the ‘Black Ape’ of Celebes (Macaca nigra).” Journal of Zoology, London 182:63-84.
*Giacoma, C., and P. Messeri (1992) “Attributes and Validity of Dominance Hierarchy in the Female Pigtail Macaque.” Primates 33:181-89.
*Kaufman, I. C., and L. A. Rosenblum (1966) “A Behavioral Taxonomy for Macaca nemestrina and Macaca radiata: Based on Longitudinal Observation of Family Groups in the Laboratory.” Primates 7:205—58.
Kyes, R. C., R. E. Rumawas, E. Sulistiawati, and N. Budiarsa (1995) “Infanticide in a Captive Group of Pigtailed Macaques (Macaca nemestrina):” American Journal of Primatology 36:135-36.
Maestripieri, D., K. Wallen, and K. A. Carroll (1997) “Infant Abuse Runs in Families of Group-Living Pigtail Macaques.” Child Abuse e’r Neglect 21:465—71.
*Matsumura, S., and K. Okamoto (1998) “Frequent Harassment of Mounting After a Takeover of a Group of Moor Macaques (Macaca maurus).” Primates 39:225—30.
*Nickelson, S. A., and J. S. Lockard (1978) “Ethogram of Celebes Monkeys (Macaca nigra) in Two Captive Habitats.” Primates 19:437—47.
Oi, T. (1996) “Sexual Behavior and Mating System of the Wild Pig-tailed Macaque in West Sumatra.” In J. E. Fa and D. G. Lindburg, eds., Evolution and Ecology of Macaque Societies, pp. 342—68. Cambridge: Cambridge University Press.
*———(1991) “Non-copulatory Mounting of Wild Pig-tailed Macaques (Macaca nemestrina nemestrina) in West Sumatra, Indonesia.” In A. Ehara, T. Kimura, O. Takenaka, and M. Iwamoto, eds., Primatology Today, pp. 147—50. Amsterdam: Elsevier Science Publishers.
*———(1990a) “Patterns of Dominance and Affiliation in Wild Pig-tailed Macaques (Macaca nemestrina nemestrina) in West Sumatra.” International Journal of Primatology 11:339—55.
———(1990b) “Population Organization of Wild Pig-tailed Macaques (Macaca nemestrina nemestrina) in West Sumatra.” Primates 31:15—31.
*Poirier, F. E. (1964) “The Communicative Matrix of the Celebes Ape (Cynopithecus niger): A Study of Sixteen Male Laboratory Animals.” Master’s thesis, University of Oregon.
*Reed, C. (1997) Personal communication.
*Reed, C., T. G. O’Brien, and M. F. Kinnaird (1997) “Male Social Behavior and Dominance Hierarchy in the Sulawesi Crested Black Macaque (Macaca nigra).” International Journal of Primatology 18:247—60.
Schiller, H. S., G. P. Sackett, W. T. Frederickson, and L. J. Risler (1983) “Maintenance of High-density Lipoprotein Blood Levels Prior to Spontaneous Abortion in Pig-tailed Macaques (Macaca nemestrina).” American Journal of Primatology 4:127—33.
*Skinner, S. W, and J. S. Lochard (1979) “An Ethogram of the Liontail Macaque (Macaca silenus) in Captivity.” Applied Animal Ethology 5:241-53.
*Thierry, B. (1986) “Affiliative Interference in Mounts in a Group of Tonkean Macaques (Macaca tonkeana).” American Journal of Primatology 11:89—97.
*Tokuda, K., R. C. Simons, and G. D. Jensen (1968) “Sexual Behavior in a Captive Group of Pigtailed Monkeys (Macaca nemestrina).” Primates 9:283—94.
OTHER PRIMATES
SAVANNA BABOON
IDENTIFICATION: The familiar baboon, with variable coat color (greenish to yellowish brown to grayish black), doglike head with a black face, and long tail (over 2 feet in males). DISTRIBUTION: Equatorial, eastern, and southern Africa. HABITAT: Scrub, savanna, woodland. STUDY AREAS: Gombe Stream National Park, Tanzania; Ishasha Forest and Queen Elizabeth National Park, Uganda; Amboseli National Park, and near Gilgil and the Athi River, Kenya; Cape of Good Hope Nature Reserve, South Africa; Namibia; subspecies P.c. anubis, the Olive Baboon; P.c. ursinus, the Chacma Baboon; and P.c. cynocephalus, the Yellow Baboon.
HAMADRYAS BABOON
IDENTIFICATION: A gray baboon with a striking silver-gray “cape” or shoulder mane in adult males. DISTRIBUTION: Somalia, Ethiopia, southern Saudi Arabia, Yemen. HABITAT: Semidesert, steppe, savanna woodlands, rocky terrain. STUDY AREAS: Erer-Gota region, eastern Ethiopia; Brookfield (Illinois) and London Zoos.
GELADA BABOON
identification: A brown baboon with a thick “cape” of fur in adult males; both sexes have an hourglass-shaped patch of bare skin on the chest, encircled by fleshy “beads” in estrous females. DISTRIBUTION: Northern and central Ethiopia. HABITAT: Mountain grasslands, rocky gorges. STUDY AREAS: Simien Mountain National Park, Ethiopia; Yerkes Regional Primate Research Center, Georgia; San Antonio Zoo, Texas.
Social Organization
Savanna Baboons live in groups of 30—100 containing both adult males and females. Females form the matriarchal core of each group since they remain for life, whereas males often emigrate to a new group on reaching adulthood. However, some troops are strongly inbred because individuals rarely leave. In contrast, both Gelada and Hamadryas Baboons live in large troops that include so-called HAREM groups—bands that have a single male and several females. In Geladas, the primary social bonds are between the females in such groups (most of whom are related to each other, as in Savanna Baboons), whereas in Hamadryas Baboons the primary bonds are between the male and the females. Unlike many other primates, Hamadryas females emigrate from the group while males remain (hence, most of the females in a group are not related to each other). Geladas also have “bachelor” troops of nonbreeding males, and “bachelor” Hamadryas or Gelada males sometimes associate with a harem group and may develop a close relationship with its male leader.
Description
Behavioral Expression: Homosexual mounting among both males and females occurs in all three of these Baboon species. The position used is similar to that for heterosexual copulation: the mounting animal places its hands on the mountee’s lower back and clasps the mountee’s ankles or thighs with its feet. Both sexes often make pelvic thrusts during homosexual mounts; males usually have an erection, and ejaculation does occur in at least some Savanna Baboon mounts between males. Male Savanna Baboons also sometimes fondle their own or their partner’s genitals during a same-sex mount, and male mounters may gently bite or nuzzle their partner’s neck after a homosexual mount. Male Geladas have also been observed masturbating other males. Females of these species mount each other both during “heat” and outside of their sexual cycle; about 9 percent of lesbian mounts in Savanna Baboons involve a pregnant female mounting another female. Because most Savanna and Gelada females are related to the other females in a troop, at least some homosexual activity is incestuous.
Mounting between two male Savanna Baboons in Tanzania
In Savanna Baboons, homosexual mounting occurs in a variety of contexts, including during good-natured play-fighting. However, in this species (and to some extent also in the other species) same-sex mounting is most prominent as part of a unique form of male “greeting” interaction. Whenever two males meet each other, they exchange a series of ritualized sexual behaviors that may include homosexual mounting and invitations to mount, as well as a wide variety of other sexual and affectionate contacts. One such behavior is known as DIDDLING, in which the males fondle each other’s genitals, including touching or pulling on the penis and fondling the scrotum. Males also embrace and kiss each other on the head or mouth, and may even bend down to kiss, lick, or nibble on another male’s penis or nuzzle his groin and thighs. Sometimes a male will also nuzzle another male’s back with his nose, especially during a mount. Another “greeting” behavior involves one male patting, grabbing, and sometimes even nuzzling or fingering another male’s rear end. Although most “greeting” interactions are relatively brief and one-sided, occasionally two males develop a closer, bonded relationship sometimes known as a COALITION, in which the “greeting” interactions are more extensive, frequent, and reciprocated. Partners in such an alliance take turns exchanging sexual behaviors with each other (especially diddling), and they often protect and help one another. Such coalitions between males may become stable, long-lasting associations that persist for many years.
A male Savanna Baboon in southern Africa nuzzling the genitals of another male
Several different kinds of intersexual or hermaphrodite individuals occur spontaneously in Savanna Baboons. In South African populations, gender-mixing individuals sometimes become high-ranking and powerful members of their troops. Such animals have female genitalia and internal organs, yet their mammary glands are not developed. Genetically, they are male (having XY chromosomes), physically they are large—exceeding the proportions of nonintersexed females and sometimes even males—and sexually, they often interact with males. Another type of intersexuality found in Baboons involves animals that have male external genitals (including testes) combined with some female internal reproductive organs (such as a uterus and fallopian tubes).
Frequency: Among Savanna Baboons, homosexual activity is common: 13—24 percent of all mounting behavior is between males and up to 9 percent is between females. “Greetings” interactions—which include ritualized homosexual activities—occur more than twice as often as any other form of interaction between males and take place roughly once every 50 minutes in some troops. Approximately 10 percent of males in some areas develop closely bonded coalitions, which comprise about 2 percent of all dyads between males. In Hamadryas Baboons, sexual behavior (homosexual or heterosexual) is overall less frequent, but approximately one-third to two-thirds of sexual activity may occur between animals of the same sex (mostly between males). In a study of wild Geladas, homosexual interactions between males were observed about once every two hours; in captivity, 14—25 percent of mounts are between males and 2—3 percent are between females.
Orientation: In Savanna Baboons, the entire male population participates in homosexual “greetings” interactions; all adult males (including those in bonded coalitions with other males) are sexually active with females as well, indicating a high degree of bisexuality. This is probably true to a lesser extent for females, not all of whom engage in homosexual mounting. In Hamadryas Baboons, harem-holding males may be bisexual, mounting both males and females, while Gelada harem males are usually exclusively heterosexual (although they may engage in same-sex genital handling if there is another male in the troop). Some “bachelor” males in both species may engage solely in homosexual activity, especially adolescents and younger adults. In Geladas, for example, an average of 12 percent of the population lives in all-male groups (where same-sex activity usually occurs). In some areas this proportion is as high as 40 percent or more, although most such males do eventually breed.
Nonreproductive and Alternative Heterosexualities
A large proportion of Baboon heterosexual behavior involves nonprocreative activities. Savanna and Hamadryas Baboons commonly mate when the female cannot get pregnant. In some Savanna populations, up to 18 percent of heterosexual copulations occur during the nonfertilizable stages of her ovulatory cycle (including during menstruation) and 2—12 percent of matings happen when the female is already pregnant. Most females, however, remain abstinent while pregnant or lactating and in fact are (hetero)sexually active for less than 10 percent of their adult lives. Heterosexual mountings do not always involve penetration and/or ejaculation, either—in fact, one study found that less than 40 percent of opposite-sex matings in Savanna Baboons involved “full” copulation. Moreover, a variety of sexual behaviors besides vaginal intercourse occur, including fondling of genitals and females mounting males (REVERSE mounts). Masturbation is also a component of Baboon sexual expression, with several innovative techniques employed: Savanna males stimulate the penis with their hand, lick their own penis, rub their genitals against the ground, or stroke the penis with the tip of the tail, while females stimulate the clitoris and perineal area with the tail or fingers. Both males and females show evidence of sexual arousal during grooming, in the form of rhythmic erection of the genitals—“penis flicking” in males, and labial and clitoral swelling and “pulsation” in females. Sexual activity in Baboons also sometimes includes copulation with partners that are not optimal for breeding: adult male Savanna Baboons and adult female Hamadryas Baboons may mate with juvenile animals, incestuous matings are common in inbred troops, while “friendships” and sexual behavior between Baboons and Common Chimpanzees have been observed in the wild (and between female Savanna Baboons and male Macaques in captivity). In addition, infertile females are occasionally found in Savanna Baboons—in one troop they constituted 10 percent of all the adult females—and these individuals continue to engage in sexual behavior.
Several other forms of nonbreeding are found among Baboons. Geladas and Hamadryas Baboons, for example, have significant “bachelor” populations that do not generally participate in reproduction (constituting 20 percent of the male Hamadryas population). Older female Savanna Baboons sometimes experience a postreproductive period, while breeding-age males and females in this species often form platonic “friendships” with each other. Sexual relations in Baboons, however, are sometimes characterized by significant antagonism and even violence between the sexes. Hamadryas harem males often threaten and attack females, biting them on the neck to prevent them from leaving the group. Adult male Savanna Baboons sometimes rape younger females, often seriously injuring them, and adult females avoid or refuse a third of all mating attempts by males. In some populations, abortions and infanticide result when an outside male takes over a troop. He viciously attacks both mothers and infants to maximize his breeding opportunities; as a result of this brutality, females may suffer severe injuries as well as miscarriages, and infants may be killed. There is also evidence that females attack other females in order to suppress their reproduction. Infanticide was recently discovered among Geladas as well. Many male Baboons act as “baby-sitters” for infants, although occasionally the youngsters become injured during fights between their “baby-sitter” (or “kidnapper”) and other males.
Other Species
Homosexual activity occurs in several other species of African monkeys. Same-sex mounting (in both males and females) is found in Vervets (Cercopithecus aethiops) (comprising about 11 percent of all mounting), Sooty Mangabeys (cercocebus torquatus) (about 18 percent of mounting), and Talapoins (Miopithecus talapoin). Mounting between male Vervets is often accompanied by grooming, embracing from behind, fondling and displaying of the genitals, and nuzzling of the perineum and scrotum. Same-sex mounting in Talapoins may also include embracing or play-wrestling. Among Patas Monkeys (Erythrocebus patas), adolescent and younger males often fondle and nuzzle the scrotum and genitals of adult males.
Sources
*asterisked references discuss homosexualityltransgender
*Abegglen, J.-J. (1984) On Socialization in Hamadryas Baboons: A Field Study. Lewisburg, Pa.: Bucknell University Press.
*Bernstein, I. S. (1975) “Activity Patterns in a Gelada Monkey Group.” Folia Primatologica 23:50—71.
*———(1970) “Primate Status Hierarchies.” In L. A. Rosenblum, ed., Primate Behavior: Developments in Field and Laboratory Research, vol.l, pp. 71—109. New York: Academic Press.
*Bielert, C. (1985) “Testosterone Propionate Treatment of an XY Gonadal Dysgenetic Chacma Baboon.” Hormones and Behavior 19:372—85.
*———(1984a) “The Social Interactions of Adult Conspecifics with an Adult XY Gonadal Dysgenetic Chacma Baboon (Papio ursinus).” Hormones and Behavior 18:42-55.
*———(1984b) “Estradiol Benzoate Treatment of an XY Gonadal Dysgenetic Chacma Baboon.” Hormones and Behavior 18:191—205.
*Bielert, C., R. Bernstein, G. B. Simon, and L. A. van der Walt (1980) “XY Gonadal Dysgenesis in a Chacma Baboon (Papio ursinus).” International Journal of Primatology 1:3—14.
*Dixson, A. F., D. M. Scruton, and J. Herbert (1975) “Behavior of the Talapoin Monkey (Miopithecus talapoin) Studied in Groups, in the Laboratory.” Journal of Zoology, London 176:177—210.
Dunbar, R. (1984) Reproductive Decisions: An Economic Analysis of Gelada Baboon Social Strategies. Princeton: Princeton University Press.
*Dunbar, R., and P. Dunbar (1975) Social Dynamics of Gelada Baboons. Basel: S. Karger.
*Fedigan, L. M. (1972) “Roles and Activities of Male Geladas (Theropithecus gelada).” Behavior 41:82-90.
*Gartlan, J. S. (1974) “Adaptive Aspects of Social Structure in Eryhthrocebus patas.” In S. Kondo, M. Kawai, A. Ehara, and S. Kawamura, eds., Proceedings from the Symposia of the Fifth Congress of the International Primatological Society, pp. 161-71. Tokyo: Japan Science Press.
*———(1969) “Sexual and Maternal Behavior of the Vervet Monkey, Cercopithecus aethiops.” Journal of Reproduction and Fertility, supplement 6:137—50.
*Hall, K. R. L. (1962) “The Sexual, Agonistic, and Derived Social Behavior Patterns of the Wild Chacma Baboon, Papio ursinus.” Proceedings of the Zoological Society of London 139:283—327.
*Hausfater, G., and D. Takacs (1987) “Structure and Function of Hindquarter Presentations in Yellow Ba boons (Papio cynocephalus).” Ethology 74:297—319.
*Kummer, H. (1968) Social Organization of Hamadryas Baboons. Chicago: University of Chicago Press.
*Kummer, H., and F. Kurt (1965) “A Comparison of Social Behavior in Captive and Wild Hamadryas Baboons.” In H. Vagtborg, ed., The Baboon in Medical Research, pp. 65—80. Austin: University of Texas Press.
*Leresche, L. A. (1976) “Dyadic Play in Hamadryas Baboons.” Behavior 57:190—205.
*Marais, E. N. (1926) “Baboons, Hypnosis, and Insanity.” Psyche 7:104—10.
*———(1922/1969) The Soul of the Ape. New York: Atheneum.
*Maxim, P. E., and J. Buettner-Janusch (1963) “A Field Study of the Kenya Baboon.” American Journal of Physical Anthropology 21:165—80.
Mori, A., T. Iwamoto, and A. Bekele (1997) “A Case of Infanticide in a Recently Found Gelada Population in Arsi, Ethiopia.” Primates 38:79-88.
*Mori, U. (1979) “Individual Relationships within a Unit; Development of Sociability and Social Status.” In M. Kawai (ed.) Ecological and Sociological Studies of Gelada Baboons, pp. 93-154. Basel: S. Karger.
*Noë, R. (1992) “Alliance Formation Among Male Baboons: Shopping for Profitable Partners.” In A. H. Harcourt and F. B. M. de Waal, eds., Coalitions and Alliances in Humans and Other Animals, pp. 284-321. Oxford: Oxford University Press.
*Owens, N. W. (1976) “The Development of Sociosexual Behaviour in Free-Living Baboons, Papio anubis.” Behavior 57:241—59.
Packer, C. (1980) “Male Care and Exploitation of Infants in Papio anubis.” Animal Behavior 28:512—20.
Pereira, M. E. (1983) “Abortion Following the Immigration of an Adult Male Baboon (Papio cynocephalus).” American Journal of Primatology 4:93—98.
*Ransom, T. W. (1981) Beach Troop of the Gombe. Lewisburg, Pa.: Bucknell University Press; London and Toronto: Associated University Presses.
*Rowell, T. E. (1973) “Social Organization of Wild Talapoin Monkeys.” American Journal of Physical Anthropology 38:593—98.
*———(1967a) “Female Reproductive Cycles and the Behavior of Baboons and Rhesus Macaques.” In S. A. Altmann, ed., Social Communication Among Primates, pp. 15—32. Chicago: University of Chicago Press.
“———(1967b) “A Quantitative Comparison of the Behavior of a Wild and a Caged Baboon Group.” Animal Behavior 15:499—509.
Saayman, G. S. (1970) “The Menstrual Cycle and Sexual Behavior in a Troop of Free Ranging Chacma Baboons (Papio ursinus).” Folia Primatologica 12:81—110.
Smuts, B. B. (1987) “What Are Friends For?” Natural History 96(2):36-45.
———(1985) Sex and Friendship in Baboons. New York: Aldine.
*Smuts, B. B., and J. M. Watanabe (1990) “Social Relationships and Ritualized Greetings in Adult Male Baboons (Papio cynocephalus anubis).” International Journal of Primatology 11:147—72.
*Struhsaker, T. T. (1967) Behavior of Vervet Monkeys (Cercopithecus aethiops). University of California Publications in Zoology, vol. 82. Berkeley: University of California Press.
*Wadsworth, P. F., D. G. Allen, and D. E. Prentice (1978) “Pseudohermaphroditism in a Baboon (Papio anubis).” Toxicology Letters 1:261—66.
Wasser, S. K., and S. K. Starling (1988) “Proximate and Ultimate Causes of Reproductive Suppression Among Female Yellow Baboons at Mikumi National Park, Tanzania.” American Journal of Primatology 16:97—121.
*Weinrich, J. D. (1980) “Homosexual Behavior in Animals: A New Review of Observations From the Wild, and Their Relationship to Human Sexuality.” In R. Forleo and W. Pasini, eds., Medical Sexology: The Third International Congress, pp. 288—95. Littleton, Mass.: PSG Publishing.
*Wolfheim, J. H., and T. E. Rowell (1972) “Communication Among Captive Talapoin Monkeys (Miopithecus talapoin).” Folia Primatologica 18:224—55.
*Zuckerman, S. (1932) The Social Life of Monkeys and Apes. New York: Harcourt, Brace and Company.
SQUIRREL MONKEY
IDENTIFICATION: A small (9—14 inch) monkey with a long tail; a pinkish white, heart- or skull-shaped facial pattern; and dense, yellowish or gray-green fur. DISTRIBUTION: Throughout most of northeastern South America, including Brazil, Colombia. HABITAT: Forests, swamps. STUDY AREAS: Monkey Jungle, Miami, Florida; Washington and California Regional Primate Research Centers; University of California—Santa Barbara; Max-Planck Institute of Psychiatry, Munich, Germany.
RUFOUS-NAPED TAMARIN
IDENTIFICATION: A squirrel-sized monkey with a mottled black and golden coat, a reddish tail and head, and a white crown. DISTRIBUTION: Northwestern Colombia through central Panama and Costa Rica. HABITAT: Tropical forests. STUDY AREA: Barro Colorado Island, Panama.
Social Organization
Squirrel Monkeys live in troops of 20—70 animals containing a majority of females. Younger males leave their home troops and live for several years in all-male “bachelor” bands of 2—10 monkeys, after which they join the cosexual troops as peripheral members. Females generally remain in their home troops for life, where they develop strong bonds with each other. Rufous-naped Tamarins live in cosexual groups of 3—9 individuals in which usually only one male-female pair breeds; the remainder of the group consists of their offspring and unrelated adult nonbreeders.
Description
Behavioral Expression: Female Squirrel Monkeys court and mount each other. Homosexual courtship is initiated by one female facing the other, tilting her head, and making a “purring” noise (a series of soft, guttural clicklike sounds). This may be accompanied by a GENITAL DISPLAY, in which the soliciting female positions herself in front of the other, spreading her thighs to expose her vulva and engorged or erect clitoris. As an invitation to the other female to mount, she turns around and presents her hindquarters, looking over her shoulder with her feet spread apart. This may be repeated several times, the presenting female moving away each time as the other female approaches in a sort of courtship “chase.” Mounting is done in the same position used for heterosexual mating: one female grasps the other’s waist with her hands and her calves with her feet, making thrusting movements with her pelvis. The mounted female frequently purrs during the sexual interaction. Sometimes two females take turns mounting each other, but often one female is more typically a mounter and the other a mountee.
Female Squirrel Monkeys may develop a short, consortlike bond (also seen in heterosexual interactions) during which they interact sexually with one another. In addition, a number of other types of female bonding occur in this species. Females frequently have one close female “friend” with whom they travel and rest; often this relationship develops into a highly affectionate one and may even include coparenting. The two females frequently touch hands, kiss each other on the mouth, and huddle together. If one of them is a mother, the other helps her raise her infant; if both are mothers, they help each other with parenting, including nuzzling and carrying each other’s infant and protecting them from predators. Often the infant develops a strong bond with the comother, although some females act as coparents for infants belonging to several different mothers. The coparenting female is sometimes known as an “aunt,” although she need not be genetically related to the mother; her relationship with the mother often outlasts the duration of parenting.
A female Squirrel Monkey mounting another female
A male Squirrel Monkey (right) performing a “genital display” toward another male
Homosexual mounting sometimes occurs between male Squirrel Monkeys, especially younger individuals or between an older and a younger (adult) partner; adult males also perform the genital display to each other. During intense displays, one male will thrust his erect penis into the face of the other male while holding him down with his hands and may even climb onto the back of the other male (who also sometimes develops an erection). Several males can be drawn into the activity, forming a ball or “pileup” of three or four individuals all twisting and climbing on one another as they try to perform genital displays.
In Rufous-naped Tamarins, homosexual behavior takes the form of same-sex mounting, including pelvic thrusting (as in heterosexual copulation); both males and females participate in homosexual mounts.
Frequency: In captivity, homosexual mounting can occur quite frequently in both mixed-sex and single-sex groups of Squirrel Monkeys: one study recorded mounts between females roughly once every 40 minutes, with homosexual activity taking place over three to seven days each month. An average of about 40 percent of genital displays occur between animals of the same sex; more than one-quarter are between females. In Rufous-naped Tamarins, homosexual mounting occurs sporadically.
Orientation: Some female Squirrel Monkeys that bond with other females as coparents are themselves nonbreeders; to this extent, then, they are involved exclusively in same-sex activities. Most other Squirrel Monkeys, as well as Rufous-naped Tamarins, that participate in homosexual behavior are probably simultaneously bisexual. In a group of three Squirrel Monkeys (two females and one male) whose sexual activities were briefly sampled, for example, heterosexual and homosexual encounters alternated continuously for a half hour, and more than 25 percent of the courtship and sexual activities were between the females. However, no detailed long-term studies have been conducted to verify the extent of individuals’ same-sex versus opposite-sex activity throughout their entire lives.
Nonreproductive and Alternative Heterosexualities
In addition to the female coparenting arrangement described above, other alternative family configurations and nonbreeding individuals occur in Squirrel Monkeys. One female sometimes adopts another female’s infant, raising it along with her own baby, while some male Squirrel Monkeys never copulate at all during the mating season. Interestingly, these may be the highest-ranking males in the troop, who are often more aggressive and less patient than other males and therefore more likely to disturb females or fail to attract willing mates. Several other aspects of Squirrel Monkey heterosexual life reveal considerable antagonism and separation between the sexes. Females often form groups or COALITIONS during the mating season to chase off males who are pursuing unwilling females; females (and occasionally males) may also directly disrupt heterosexual copulations in progress. At other times, females persistently harass males so that they remain spatially segregated from the females, either on the periphery of the troop or closer to the ground. When a willing female is found and the sexual interaction is not disturbed, often several males will participate, all joining in by kissing the female on the mouth, displaying their genitals, and sniffing or nuzzling her genitalia. The mating system is promiscuous, as both males and females copulate with multiple partners.
A number of nonprocreative sexual activities are also found in these New World monkeys. Male Squirrel Monkeys masturbate by either sucking their own penis or rubbing it with one or both hands, while females may copulate when not in heat or during pregnancy (up to the fourth month). In addition, females sometimes produce a vulvar plug from sloughed vaginal cells when they are in heat, which may serve to limit inseminations. Rufous-naped Tamarin males on occasion mount females without thrusting or penetration. Male Squirrel Monkeys also have a pronounced sexual cycle: for three to four months out of the year, they are sexually active, more aggressive, and develop a characteriscic appearance—heavier, with more fluffed fur—during which time they are known as FATTED MALES. For the remainder of the year, however, their testes are essentially dormant; they lose their “fatted” appearance and live largely separate from the females. In Rufous-naped Tamarins, as in other tamarins and marmosets, all but the highest-ranking female in a group forgo reproduction, perhaps through a complex mechanism of “self-restraint” that is mediated by pheromones from the lead female. As a result, only about half of all mature females actually reproduce at one time; however, nonbreeding individuals often continue to copulate. In addition, most matings outside the breeding season do not result in offspring, and it is thought that many embryos may be reabsorbed, aborted, or the young die soon after birth.
Other Species
Same-sex activity occurs in several other species of Central and South American monkeys. Homosexual mounting (in both males and females), including pelvic thrusting and genital rubbing on the partner, has been observed in a variety of Tamarin species, including the Saddle-back Tamarin (Saguinus fuscicollis), the Mustached Tamarin (S. mystax), and the Cotton-top Tamarin (S. oedipus). Both male and female Lion Tamarins (Leontopithecus rosalia) sometimes mount their own offspring of both sexes, including adolescents and younger individuals. Approximately 1 percent of mounting activity in Common Marmosets (Callithrix jac-chus) occurs among adolescent and younger males (brothers living in the same family group). In White-fronted Capuchin Monkeys (Cebus albifrons), young males occasionally suck and fondle the scrotum of older males, while homosexual activity among females (including mounting) also occurs in Brown Capuchins (C. apella) and Weeper Capuchins (C. olivaceous). More than half of all mounting in White-faced Capuchins (C. capucinus) is between same-sex partners, often preceded by a type of courtship activity known as WHEEZE DANCING, involving contorted postures, wheezing vocalizations, and “slow-motion” chases.
Sources
*asterisked references discuss homosexualityltransgender
*Akers, J. S., and C. H. Conaway (1979) “Female Homosexual Behavior in Macaca mulatta.” Archives of Sexual Behavior 8:63—80.
*Anschel, S., and G. Talmage-Riggs (1978) “Social Structure Dynamics in Small Groups of Captive Squirrel Monkeys.” In D. J. Chivers and J. Herbert, eds., Recent Advances in Primatology, vol. 1, pp. 601—4. New York: Academic Press.
*Baldwin, J. D. (1969) “The Ontogeny of Social Behavior of Squirrel Monkeys (Saimiri sciureus) in a Seminatural Environment.” Folia Primatologica 11:35—79.
———(1968) “The Social Behavior of Adult Male Squirrel Monkeys (Saimiri sciureus) in a Seminatural Environment.” Folia Primatologica 9:281—314.
Baldwin, J. D., and J. I. Baldwin (1981) “The Squirrel Monkeys, Genus Saimiri.” In A. F. Coimbra-Filho and R. A. Mittermeier, eds., Ecology and Behavior of Neotropical Primates, vol. 1, pp. 277—330. Rio de Janeiro: Academia Brasileira de Ciencias.
*Castell, R., and B. Heinrich (1971) “Rank Order in a Captive Female Squirrel Monkey Colony.” Folia Primatologica 14:182—89.
Dawson, G. A. (1976) “Behavioral Ecology of the Panamanian Tamarin, Saguinus oedipus (Callitrichidae, Primates).” Ph.D. thesis, Michigan State University.
*Defler, T. R. (1979) “On the Ecology and Behavior of Cebus albifrons in Eastern Colombia: II. Behavior.” Primates 20:491—502.
*Denniston, R. H. (1980) “Ambisexuality in Animals.” In J. Marmor, ed., Homosexual Behavior: A Modern Reappraisal, pp. 25—40. New York: Basic Books.
*DuMond, F. V. (1968) “The Squirrel Monkey in a Seminatural Environment.” In L. A. Rosenblum and R. W. Cooper, eds., The Squirrel Monkey, pp. 87-145. New York: Academic Press.
DuMond, F. V., and T. C. Hutchinson (1967) “Squirrel Monkey Reproduction: The ‘Fatted’ Male Phenomenon and Seasonal Spermatogenesis.” Science 158:1067—70.
*Hoage, R. J. (1982) Social and Physical Maturation in Captive Lion Tamarins, Leontopithecus rosalia rosalia (Primates: Callitrichidae). Smithsonian Contributions to Zoology no. 354. Washington, D.C.: Smithsonian Institution Press.
Hopf, S., E. Hartmann-Wiesner, B. Kuhlmorgen, and S. Mayer (1974) “The Behavioral Repertoire of the Squirrel Monkey (Saimiri).” Folia Primatologica 21:225—49.
Latta, J., S. Hopf, and D. Ploog (1967) “Observation of Mating Behavior and Sexual Play in the Squirrel Monkey (Saimiri sciureus).” Primates 8:229—46.
*Linn, G. S., D. Mase, D. LaFrançois, R. T. O’Keeffe, and K. Lifshitz (1995) “Social and Menstrual Cycle Phase Influences on the Behavior of Group-Housed Cebus apella.” American Journal of Primatology 35:41—57.
*Manson, J. H., S. Perry, and A. R. Parish (1997) “Nonconceptive Sexual Behavior in Bonobos and Capuchins.” International Journal of Primatology 18:767-86.
*Mendoza, S. P., and W. A. Mason (1991) “Breeding Readiness in Squirrel Monkeys: Female-Primed Females are Triggered by Males.” Physiology & Behavior 49:471—79.
Mitchell, C. L. (1994) “Migration Alliances and Coalitions Among Adult Male South American Squirrel Monkeys (Saimiri sciureus).” Behavior 130:169—90.
*Moynihan, M. (1970) Some Behavior Patterns of Platyrrhine Monkeys. II. Saguinus geoffroyi and Some Other Tamarins. Smithsonian Contributions to Zoology no. 28. Washington, D.C.: Smithsonian Institution Press.
*Perry, S. (1998) “Male-Male Social Relationships in Wild White-faced Capuchins, Cebus capucinus.” Behavior 135:139—72.
Peters, M. (1970) “Mouth to Mouth Contact in Squirrel Monkeys (Saimiri sciureus).” Zeitschrift für Tierpsychologie 27:1009—10.
Ploog, D. W (1967) “The Behavior of Squirrel Monkeys (Saimiri sciureus) as Revealed by Sociometry, Bioa-coustics, and Brain Stimulation.” In S. Altmann, ed., Social Communication Among Primates, pp. 149— 84. Chicago: University of Chicago Press.
*Ploog, D. W., J. Blitz, and F. Ploog (1963) “Studies on the Social and Sexual Behavior of the Squirrel Monkey (Saimiri sciureus).” Folia Primatologica 1:29—66.
Ploog, D. W., and P. D. Maclean (1963) “Display of Penile Erection in Squirrel Monkey (Saimiri sciureus).” Animal Behavior 11:32—39.
Rosenblum, L.A. (1968) “Mother-Infant Relations and Early Behavioral Development in the Squirrel Monkey.” In L. A. Rosenblum and R. W. Cooper, eds., The Squirrel Monkey, pp. 207—33. New York: Academic Press.
*Rothe, H. (1975) “Some Aspects of Sexuality and Reproduction in Groups of Captive Marmosets (Callithrix jacchus).” Zeitschrift für Tierpsychologie 37:255-73.
*Shadle, A. R., E. A. Mirand, and J. T. Grace Jr. (1965) “Breeding Responses in Tamarins.” Laboratory Animal Care 15:1—10.
Skinner, C. (1985) “A Field Study of Geoffroy’s Tamarin (Saguinus geoffroyi) in Panama.” American Journal of Primatology 9:15—25.
Snowdon, C. T. (1996) “Infant Care in Cooperatively Breeding Species.” Advances in the Study of Behavior 25:643—89.
Srivastava, P. K., F. Cavazos, and F. V. Lucas (1970) “Biology of Reproduction in the Squirrel Monkey (Saimiri sciureus): I. The Estrus Cycle.” Primates 11:125—34.
*Talmage-Riggs, G., and S. Anschel (1973) “Homosexual Behavior and Dominance in a Group of Captive Squirrel Monkeys (Saimiri sciureus).” Folia Primatologica 19:61—72.
*Travis, J. C., and W. N. Holmes (1974) “Some Physiological and Behavioral Changes Associated with Oestrus and Pregnancy in the Squirrel Monkey (Saimiri sciureus).” Journal of Zoology, London 174:41— 66.
*Vasey, P. L.(1995) “Homosexual Behavior in Primates: A Review of Evidence and Theory.” International Journal of Primatology 16:173—204.
VERREAUX’S SIFAKA
IDENTIFICATION: A long-legged lemur with a plush white coat, black face, black or brown crown and underparts, and long tail (nearly 2 feet). DISTRIBUTION: Western and southern Madagascar; vulnerable. HABITAT: Forests. STUDY AREA: Near Hazafotsy, Madagascar; subspecies P.v. verreauxi.
LESSER BUSHBABY
IDENTIFICATION: A small, squirrel-like primate (7 inches, plus a foot-long tail) with silky, grayish-yellow fur, a broad face, and enormous eyes and ears. DISTRIBUTION: Sub-Saharan Africa. HABITAT: Woodland, savanna, scrub. STUDY AREA: Witwatersrand University, South Africa.
Social Organization
Verreaux’s Sifakas live in cosexual groups of up to 12 individuals and sometimes associate as male-female pairs. As in most Lemurs, females are generally dominant to males in this species. Females typically remain in their birth group for life, while males leave their group on maturing and transfer between groups several times throughout their lives. The mating system has elements of POLYGYNANDRY, that is, females generally mate with more than one male and vice versa. Lesser Bushbabies generally live in family groups consisting of females and their offspring along with peripheral males. They are often found singly or in pairs and may form sleeping groups of up to seven individuals.
Description
Behavioral Expression: Male Verreaux’s Sifakas sometimes mount other males during the mating season. The mounted animal—usually a younger adult or adolescent male—often snaps at the mounter and tries to wriggle free (as do females trying to escape from unwelcome heterosexual advances). In Lesser Bushbabies, females occasionally mount and thrust against each other when in heat. Like other species of Bushbabies, the genitals of female Lesser Bushbabies are unusual in several respects. The clitoris is long and pendulous, greatly resembling the male’s penis, and the urethra extends through to the tip of the organ, so that females urinate through the clitoris rather than through a urethral opening near the vagina. Females do not menstruate, and in fact the vagina remains closed at all times except during the mating season (which lasts no more than two to three weeks and occurs twice a year).
Frequency: Homosexual mounting probably occurs only occasionally in Ver-reaux’s Sifakas and Lesser Bushbabies. However, one study of wild Verreaux’s Sifakas found that 3 out of 21 mountings (14 percent) were between males.
Orientation: Lemurs and Bushbabies that participate in same-sex mounting probably also engage in heterosexual activity, although too little is known about individual life histories in these species to draw any firm conclusions.
Nonreproductive and Alternative Heterosexualities
Many heterosexual copulations in Verreaux’s Sifakas—more than two-thirds in some populations—do not involve penetration or ejaculation, often because the female resists the mating attempt and wriggles free. Females sometimes also mate when they are not in heat: for some individuals, 30–80 percent of their sexual activity is nonprocreative, taking place during times when they cannot conceive. In some populations females also delay reproducing for several years, and only slightly more than half of all adult females reproduce each year. Infanticide occurs occasionally in this species, and possibly also abortions. In Lesser Bushbabies, heterosexual copulations can be lengthy—more than nine minutes in some cases—and a female often bites the male, “boxes” him with her hands, and tries to push him off or get away from him during mating.
Sources
*asterisked references discuss homosexuality/transgender
*Andersson, A. B. (1969) “Communication in the Lesser Bushbaby (Galago senegalensis moholi).” Master’s thesis, Witwatersrand University.
Bearder, S. K., and G. A. Doyle (1974) “Field and Laboratory Studies of Social Organization in Bushbabies (Galago senegalensis).” Journal of Human Evolution 3:37-50.
Brockman, D. K., and P. L. Whitten (1996) “Reproduction in Free-Ranging Propithecus verreauxi: Estrus and the Relationship Between Multiple Partner Matings and Fertilization.” American Journal of Physical Anthropology 100:57–69.
Butler, H. (1967) “The Oestrus Cycle of the Senegal Bush Baby (Galago senegalensis senegalensis) in the Sudan.” Journal of Zoology, London 151:143–62.
Dixson, A. F. (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.
*Doyle, G. A. (1974a) “Behavior of Prosimians.” Behavior of Nonhuman Primates 5:154–353.
———(1974b) “The Behavior of the Lesser Bushbaby.” In R. D. Martin, G. A. Doyle, and A. C. Walker, eds., Prosimian Biology, pp. 213–31. Pittsburgh: University of Pittsburgh Press.
Doyle, G. A., A. Pelletier, and T. Bekker (1967) “Courtship, Mating, and Parturition in the Lesser Bushbaby (Galago senegalensis moholi) Under Semi-Natural Conditions.” Folia Primatologica 7:169-97.
Kubzdela, K. S., A. F. Richard, and M. E. Pereira (1992) “Social Relations in Semi-Free-Ranging Sifakas (Propithecus verreauxi verreauxi) and the Question of Female Dominance.” American Journal of Primatology 28:139–45.
Lipschitz, D. L. (1996) “Male Copulatory Patterns in the Lesser Bushbaby (Galago moholi) in Captivity.” International Journal of Primatology 17:987–1000.
Lowther, F. D. L. (1940) “A Study of the Activities of a Pair of Galago senegalensis moholi in Captivity, Including the Birth and Postnatal Development of Twins.” Zoologica 25:433-65.
Richard, A., (1992) “Aggressive Competition Between Males, Female-Controlled Polygyny, and Sexual Monomorphism in a Malagasy Primate, Propithecus verreauxi.” Journal of Human Evolution 22:395–406.
———(1978) Behavioral Variation: Case Study of a Malagasy Lemur. Lewisburg, Pa.: Bucknell University Press.
*————(1974a) “Intra-specific Variation in the Social Organization and Ecology of Propithecus verreauxi.” Folia Primatologica 22:178–207.
*———(1974b) “Patterns of Mating in Propithecus verreauxi verreauxi.” In R. D. Martin, G. A. Doyle, and A. C. Walker, eds., Prosimian Biology, pp. 49–74. London: Duckworth; Pittsburgh: University of Pittsburgh Press.
Richard, A., P. Rakotomanga, and M. Schwartz (1991) “Demography of Propithecus verreauxi at Beza Ma-hafaly, Madagascar: Sex Ratio, Survival, and Fertility, 1984–1988.” American Journal of Physical Anthropology 84:307–22.
Marine Mammals
DOLPHINS AND WHALES
IDENTIFICATION: An 8-foot-long dolphin with a long, toothed beak and light blue or even bright pink skin. DISTRIBUTION: The Amazon and Orinoco River systems; vulnerable. HABITAT: Slow-moving streams and tributaries, flooded forests, lakes. STUDY AREAS: Duisburg Zoo, Germany; Aquarium of Niagara Falls, New York; subspecies l.g. humboldtiana, the Orinoco Dolphin.
Social Organization
Although little is known about their social organization, it appears that Botos are largely solitary animals that occasionally associate in groupings of up to a dozen or more individuals. Larger aggregations generally occur at feeding areas, and Botos may even coordinate their fishing attempts with other species, such as the giant river otter (Pteronura brasiliensis). The Boto mating system is probably polygamous.
Description
Behavioral Expression: Male Botos participate in a wide variety of homosexual interactions, including mating with each other using fully three different types of penetration: one male may insert his erect penis into the genital slit of the other, into his anus, or into his blowhole. When engaging in anal or genital-slit intercourse, one male swims upside down beneath the other one as in heterosexual copulation; blowhole mating occurs with the inserting male above the other one. If there is an age difference between the males, typically the older one penetrates the younger one. Males also rub their genital openings or erect penises against each other; alternatively, one male might rub his head against the other’s genitals, stimulating an erection. Pairs of males who interact sexually also display a great deal of affection toward one another, caressing each other with their beak or flippers, brushing against one another, swimming side by side while touching each other’s body, flippers, or flukes, surfacing to breathe simultaneously, or playing and resting together. Male homosexual encounters can be quite lengthy—continuing for a whole afternoon, for example—although if mating occurs, the actual penetration lasts for only about one minute (in anal intercourse).
Male Botos also engage in homosexual activity with another species of Amazon River dolphin, the Tucuxi (Sotalia fluviatilis). In these interspecies encounters, genital slit intercourse between males involves the same belly-to-belly position described above, but sometimes the penetrating animal twists around so that his head faces in the opposite direction (while still remaining inserted in the other male). In addition to caresses and genital rubbing, homosexual activity sometimes includes more unusual behavior: a male Boto was once seen gently taking a Tucuxi’s entire head into his mouth, in an apparently affectionate gesture.
Frequency Homosexual activity is common in captive Botos; its prevalence among wild animals is not known. Similarly, sexual behavior between Botos and Tucuxis has only been seen in captivity, but these two species do occasionally interact with one another in the wild.
Orientation: Because homosexual behavior has been studied in detail only in captive male Botos without access to females, it is not known whether this behavior occurs in other contexts, or if it is simply an expression of a latent or “situational” bisexual potential. However, given the varied and generally plastic nature of dolphin sexuality, it is likely that homosexual or bisexual expression is a basic component of Boto social life for at least some individuals.
Nonreproductive and Alternative Heterosexualities
Male and female Botos sometimes engage in nonreproductive matings: heterosexual blowhole copulations have been observed, and a male will also sometimes rub his penis against the female’s fins or flukes, especially if she does not permit him to copulate vaginally. In addition, heterosexual matings can be remarkably frequent and prolonged affairs: one male and female were seen to mate once every four minutes for a virtually continuous period of over three hours. However, females are not always willing participants in such repeated copulations, often fleeing into shallow waters to avoid males that are harassing them. Females that cannot escape may be attacked and bitten around the genital area by males. Masturbation is also common in Botos: males rub the penis with one of their fins, females sometimes try to insert objects into the genital slit, while both sexes rub their genitals against underwater objects or surfaces. Botos have also developed an alternate parenting or “baby-sitting” arrangement of communal nursery groups. Young Botos gather together in shallow water, forming what are sometimes known as CRÈCHES that contain both calves and older juveniles; these groups offer them safety in numbers while their parents feed on their own.
Two forms of copulation between male Botos: genital-slit (or anal) penetration (above) and blowhole penetration
Two male Botos, a younger and an older individual who are sexually involved with one another, swimming side by side while touching
Sources
*asterisked references discuss homosexuality/transgender
*Best, R. C., and V. M. F. da Silva (1989) “Amazon River Dolphin, Boto, Inia geoffrensis (de Blainville, 1817).” In S. H. Ridgway and R. Harrison, eds., Handbook of Marine Mammals, vol. 4: River Dolphins and the Larger Toothed Whales, pp. 1–23. London: Academic Press.
*Caldwell, M. C., D. K. Caldwell, and R. L. Brill (1989) “Inia geoffrensis in Captivity in the United States.” In W. F. Perrin, R. L. Brownell, Jr., Z. Kaiya, and L. Jiankang, eds., Biology and Conservation of the River Dolphins, pp. 35–41. Occasional Papers of the IUCN Species Survival Commission no. 3. Gland, Switzerland: International Union for Conservation of Nature and Natural Resources.
*Caldwell, M. C., D. K. Caldwell, and W. E. Evans (1966) “Sounds and Behavior of Captive Amazon Freshwater Dolphins, Inia geoffrensis.” Los Angeles County Museum Contributions in Science 108:1–24.
Layne, J. N. (1958) “Observations on Freshwater Dolphins in the Upper Amazon.” Journal of Mammology 39:1–22.
*Layne, J. N, and D. K. Caldwell (1964) “Behavior of the Amazon Dolphin, Inia geoffrensis (Blainville), in Captivity.” Zoologica 49:81–108.
*Pilleri, G., M. Gihr, and C. Kraus (1980) “Play Behavior in the Indus and Orinoco Dolphin (Platanista indi and Inia geoffrensis).” Investigations on Cetacea 11:57–107.
*Renjun, L., W. Gewalt, B. Neurohr, and A. Winkler (1994) “Comparative Studies on the Behavior of Inia geoffrensis and Lipotes vexillifer in Artificial Environments.” Aquatic Mammals 20:39–45.
*Spotte, S. H. (1967) “Intergeneric Behavior Between Captive Amazon River Dolphins Inia and Sotalia.” Underwater Naturalist 4:9-13.
*Sylvestre, J.-P. (1985) “Some Observations on Behavior of Two Orinoco Dolphins (Inia geoffrensis humboldtiana [Pilleri and Gihr 1977]), in Captivity, at Duisburg Zoo.” Aquatic Mammals 11:58–65.
Trujillo, F. (1996) “Seeing Fins.” BBC Wildlife 14:22–28.
BOTTLENOSE DOLPHIN
IDENTIFICATION: The familiar gray, 10–13-foot-long dolphin. DISTRIBUTION: Worldwide oceans and seas. HABITAT: Coastal, temperate-to-tropical waters. STUDY AREAS: Near Sarasota, Florida; Grand Bahama Island, the Bahamas; Marineland, Florida; Marine World Africa, California; Marineland of the Pacific, California; Port Elizabeth Oceanarium, South Africa; Harderwijk Dolphinarium, the Netherlands; subspecies, T.t. truncatus, the Atlantic Bottlenose; T.t. gilli, the Pacific Bottlenose; and T.t. aduncus, the Indian Ocean Bottlenose.
SPINNER DOLPHIN
IDENTIFICATION: A 6-foot-long dolphin with a long, slender beak; steep, triangular dorsal fin; dark upperparts and light underparts. DISTRIBUTION: Tropical oceans worldwide. HABITAT: Often in deep, offshore waters. STUDY AREAS: Kealake’akua Bay, Hawaii; Sea Life Park Oceanarium, Hawaii; subspecies SJ. longirostris, the Hawaiian Spinner Dolphin.
Social Organization
Bottlenose Dolphins have a highly developed social system characterized by four basic social units: mother-calf pairs, groups of adolescents (often male-only, or with a preponderance of males), bands of up to a dozen adult females and their young, and adult males in pair-bonds (and less commonly, on their own). Spinner Dolphins may have a more fluid social organization, although coalitions of males can sometimes be recognized, as well as schools of a thousand or more individuals. The heterosexual mating system is poorly understood; however, there are no strong male-female bonds, and animals probably mate with multiple partners.
Description
Behavioral Expression: In both Bottlenose and Spinner Dolphins, animals of the same sex frequently engage in affectionate and sexual activities with each other that have many of the elements of heterosexual courtship and sexuality. For example, two males or two females often rub their bodies together, mouthing and nuzzling one another, and may caress and stroke each other—simultaneously or alternately—with their fins, flukes, snouts (or “beaks”), and heads. Sometimes this is accompanied by playful rolling, chasing, pushing, and leaping. During this activity—which can last anywhere from several minutes to several hours—males may display erect penises. More overt homosexual activity takes a variety of forms. One animal might stroke or gently probe the other’s genital area with the soft tips of its flukes or flippers. Female Spinner Dolphins sometimes even “ride” on each other’s dorsal fin—one inserts her fin into the other’s vulva or genital slit, then the two swim together in this position. Among Bottlenose females, direct stimulation of the clitoris is a prominent feature of homosexual interactions. Two females often take turns rubbing each other’s clitoris, using either the snout, flippers, or flukes, or else actively masturbate against their partner’s appendages. Females may also clasp one another in a belly-to-belly position (as in heterosexual mating) and thrust against each other.
Homosexual interactions also involve a form of “oral” sex in which one animal rubs and nuzzles the other’s genitals with its snout or beak; because both males and females have a genital slit or opening, penetration is also possible in this fashion for both sexes. One animal might insert the tip of its beak into the other’s genitals or perhaps just use its lower jaw to penetrate and stimulate his or her partner. Sometimes this develops into a sexual activity known as BEAK-GENITAL PROPULSION, in which one partner inserts its beak into the other’s genitals and gently propels the two of them forward, maintaining penetration while they swim together. The lower animal may also turn on its side or rotate belly up during this activity. Male Dolphins sometimes rub their erect penises on one another’s body or genital area. This may lead to copulation, in which one male swims upside down underneath the other, pressing his genitals against the other and even inserting his penis into the genital slit (or less commonly, anus) of the male above him (this same position is used in heterosexual intercourse). The two partners may switch positions, alternating during the same session, or perhaps exchanging “roles” over a longer period. If there is an age difference between male partners, either may penetrate the other, and Bottlenose adolescents have even been observed penetrating much older males. Groups of three or four males may engage in homosexual activity together, or one male may masturbate (by rubbing his penis on rocks or sand) while other males are coupling nearby. Homosexual activity is sometimes accompanied by aggressive behaviors, but these can also occur during heterosexual interactions (males and females have been observed diving forcefully at each other, for example, and violently ramming their foreheads together as a prelude to mating). In Spinner Dolphins, groups of a dozen or more dolphins of both sexes sometimes gather together in near “orgies” of caressing and sexual behavior (both same-sex and opposite-sex); these groups are known as WUZZLES.
“Beak-genital propulsion” between two female Spinner Dolphins
Homosexual copulation in Bottlenose Dolphins: the male in an upside-down position is penetrating the male above him
Male Bottlenose Dolphins often form life-long pair-bonds with each other. Adolescent and younger males typically live in all-male groups in which homosexual activity is common; within these groups, a male begins to develop a strong bond with a particular partner (usually of the same age) with whom he will spend the rest of his life. The two Dolphins become constant companions, often traveling widely; although sexual activity probably declines as they get older, it may continue to be a regular feature of such partnerships. Paired males sometimes take turns guarding or remaining vigilant while their partner rests. They also defend their mates against predators such as sharks and protect them while they are healing from wounds inflicted during predators’ attacks. Sometimes three males form a tightly bonded trio. On the death of his partner, a male may spend a long time searching for a new male companion—usually unsuccessfully, since most other males in the community are already paired and will not break their bonds. If, however, he can find another “widower” whose male partner has died, the two may become a couple.