Arch Sex Behav (2014) 43:853–861 DOI 10.1007/s10508-014-0310-6
ORIGINAL PAPER
Male Homosexual Behavior in a Free-Ranging All-Male Group of Japanese Macaques at Minoo, Japan Jean-Baptiste Leca • Noe¨lle Gunst • Paul L. Vasey
Received: 27 February 2013 / Revised: 1 May 2013 / Accepted: 19 April 2014 / Published online: 28 May 2014 Ó Springer Science+Business Media New York 2014
Abstract We documented nine male homosexual consortships within three different male–male dyads in a free-ranging all-male group of Japanese macaques (Macaca fuscata), at Minoo, Japan. A total of 63 male–male mounts were observed during these consortships. Male homosexual interactions shared most of the behavioral components that have been reported to characterize heterosexual and female homosexual consortships in this species. Convergent behavioral data, including analysis of male–male solicitations, mounting postures, body orientations, inter-mount activities, and third-party male intrusions supported the conclusion that male–male consortships are a sexual phenomenon. We discussed a series of proximate and ultimate hypotheses that purport to account for the occurrence of male homosexual behavior in all-male groups of primates, including humans. This first report of male homosexual interactions in an all-male group of Japanese macaques contributes to the growing database used to provide insights into the developmental processes, causal mechanisms, adaptive significance, and phylogenetic pathways of same-sex sexual behavior. Keywords Male–male consortship Ventro-ventral mounts Sociosexual behavior Macaca fuscata
Introduction Homosexual behavior is typically defined as an interaction involving courtship displays (or sexual solicitations), mounting, and genital contact and/or stimulation between same-sex J.-B. Leca (&) N. Gunst P. L. Vasey Department of Psychology, University of Lethbridge, 4401 University Drive, Lethbridge, AB T1K 3M4, Canada e-mail: [email protected]
individuals (Vasey & Sommer, 2006). Although widespread in the animal kingdom, such behavioral patterns represent an evolutionary conundrum because they do not directly contribute to reproduction (Bagemihl, 1999; Poiani, 2010; Sommer & Vasey, 2006; Wallen & Parsons, 1997). In an attempt to address this apparent paradox, homosexual behaviors are often viewed as sociosexual, that is, behaviors that are sexual in their structure, but underlain by little or no sexual motivation and instead performed for their adaptive social functions (Wickler, 1967). Sociosexual behavioral patterns are common in several species of Old World monkeys and great apes (Dixson, 2012; Wallen & Parsons, 1997). However, there is no a priori reason why samesex mounts could not be also sexually motivated (Vasey & VanderLaan, 2012). As Dixson (2012) noted, ‘‘There is not a rigid dichotomy between the ‘sexual’ and ‘sociosexual’ functions of isosexual behavior’’(pp. 218–220).1 Several other proximate and ultimate hypotheses have been proposed to account for same-sex sexual behaviors in animals, including humans (reviewed in Poiani, 2010). For example, sex ratio bias is one of the main life history traits invoked to explain same-sex sexual behaviors in male and female birds and mammals. A lack of opposite-sex sexual partners and the availability of same-sex mates during mating periods may create a demographic constraint that leads to the expression of homosexual behavior. This is alternatively referred to as the ‘‘heterosexual deprivation hypothesis’’ (Vasey & Gauthier, 2000), the ‘‘bestof-a-bad-job hypothesis’’(Poiani, 2010), or a‘‘Hobson’s choice’’ (sensu Fedigan, 1982). It seems intuitive to predict that individuals living in unisexual groups will exhibit more homosexual interactions than those living in mixed-sex groups (i.e., 1
Isosexual behavior includes same-sex mounting and presentation and is considered a neutral term (rather than sociosexual, homosexual, or bisexual behavior) that does not involve any assumptions about the motivation of the participants (Dixson, 2012).
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groups including members of both sexes). For example, in a captive setting and during the mating season, an all-male group of rhesus macaques (Macaca mulatta), with visual access to a mixed-sex group, engaged in series of male–male mounts, some terminating with ejaculation(Gordon & Bernstein, 1973). Interestingly, unisexual male groups commonly occur in natural settings in species that form polygynous or multi-male/ multi-female breeding groups. In many gregarious primate species, dispersing individuals transfer directly from one mixedsex group to another, but, in others, including several colobine and cercopithecine species, individuals may join non-breeding (usually all-male) groups for variable periods (Pusey & Packer, 1987). All-male groups of primates are typically subordinate to mixed-sex groups, either travelling independently or occupying suboptimal ranges around mixed-sex groups (e.g., rhesus macaques: Drickamer & Vessey, 1973; Tana River red colobus, Colobus badius rufomitratus: Marsh, 1979; geladas, Theropithecus gelada: Kawai, Dunbar, & Ohsawa, 1983; Thomas’s leaf monkeys, Presbytis thomasi: Gurmaya, 1986; patas monkeys, Erythrocebus patas: Ohsawa, Inoue, & Takenaka, 1993; proboscis monkeys, Nasalis larvatus: Yeager, 1995; ursine colobus, Colobus vellerosus: Sicotte & MacIntosh, 2004). Despite the fact that they are common in many primate species, all-male groups have rarely been the focus of any detailed studies. Male–male sexual activity has been reported in some allmale groups of non-human primates. For example, in wild mountain gorillas (Gorilla gorilla beringei), male homosexual behavior occurred frequently in all-male groups, but was rarely observed in mixed-sex groups (Yamagiwa, 1987). Genital stimulation during male–male mounts in all-male groups of mountain gorillas did not seem to serve any sociosexual functions, but instead occurred in purely sexual contexts, with intensive sexual competition between adult males for access to sub-adult male partners (Yamagiwa, 1987, 2006). Although detailed studies are extremely rare (for notable exceptions, see mona monkeys, Cercopithecus mona: Glenn, Matsuda, & Bensen, 2002; Hanuman langurs, Presbytis entellus: Sommer, Schauer, & Kyriazis, 2006; mountain gorillas: Yamagiwa, 2006), research on male homosexual behavior in all-male groups of primates under natural settings may provide insights into the developmental processes, causal mechanisms, adaptive significance, and phylogenetic pathways that characterize male same-sex sexual behavior in humans. There are three reasons why the Japanese macaque (Macaca fuscata) is an ideal non-human primate model for research on male homosexual behavior. First, immature male Japanese macaques display a large repertoire of sociosexual behavioral patterns, such as male–male mounts in playful or tension-reduction contexts (Gunst, Leca, & Vasey, 2013; Hanby & Brown, 1974; VanderLaan, Pellis, & Vasey, 2012). Second, certain populations on the island of Honshu in central Japan (e.g., at Arashiyama, near Kyoto city) have been reported to exhibit male homosexual behavior (Takenoshita, 1998, 2012). Patterns
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of courtship, mounting, and inter-mount behavior are very similar across male–male and male–female sexual interactions (Takenoshita, 2012). Third, long-term studies of life history of Japanese macaques showed that almost all males eventually leave their natal group between the ages of 3–8 years, mainly during the mating season. Such males may either transfer directly into another mixed-sex group, temporarily join an allmale group or remain solitary for a period of time (Sprague, Suzuki, Takahashi, & Sato, 1998; Sugiyama, 1976). All-male groups of Japanesemacaques have been reported at several field sites, including Arashiyama, Kinkazan, Koshima, Minoo, Ryozenyama, and Shodoshima (Kawamura & Kawai, 1956; Koyama, 1970; Matsumura, 1993; Mori & Watanabe, 2003; Sprague et al., 1998; Sugiyama & Ohsawa, 1982; Yamada, 1966), but detailed studies of these naturally occurring groups are needed. To our knowledge, there are no reports of male homosexual behavior in free-ranging all-male groups of Japanese macaques. Our objectives were: (1) to document and describe male–male consortship activity, (2) to assess the sexual nature of such interactions, and (3) to discuss a series of proximate and ultimate hypotheses about the occurrence of male homosexual behavior in all-male groups of Japanese macaques and other primate species, including humans.
Method Study Site and Groups We studied three free-ranging groups of Japanese macaques, living in the Meiji Memorial Forest of Minoo Park located on the outskirts of Minoo city, Osaka Prefecture, central Japan. The first two groups, namely Minoo F and Minoo L, were mixed-sex multimale–multifemale groups, derived from an original group that fissioned into two stable social units in 1955 (S. Suzuki, personal communication). The third group was an all-male group. Although there are no recent reports on the all-male Minoo group, its origins may be traced back to the main group fission (Kawamura & Kawai, 1956). Group sizes and compositions are shown in Table 1. The three groups foraged extensively on natural foods occurring within their respective home ranges. In order to prevent the monkeys from roaming around Minoo city, the park staff provided groups F and L with wheat grains and soy beans twice a day, along a 500-m stretch of mountain trail (Y. Iwanaga, personal communication). Groups F and L generally spent from 2 to 4 h each day around the food provisioning site. These two groups were separated by a 50 to 100-m buffer zone, within which aggressive inter-group encounters occurred. The all-male group was not directly fed by the park staff. However, members of the all-male group typically arrived at the feeding site early in the morning (before groups F and L)
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Table 1 Size and composition of the three study groups during the study period Old adult ([15 years)
Middle-aged adult (11–15 years)
Young adult (7–10 years)
Subadult (4–6 years)
Juvenile (1–3 years)
Group
Male
Female
Male
Female
Male
Female
Male
Female
Male
Female
F
7±1
18 ± 2
8±1
18 ± 3
9±1
11 ± 2
4±1
12 ± 2
9±1
6±1
10 ± 1
111 ± 7
L
2±1
5±1
6±1
19 ± 2
4±1
11 ± 1
1±1
7±1
5±1
4±1
6±1
71 ± 5
–
2±1
6±2
–
3±1
–
–
15 ± 3
All-male 1 ± 1
–
4±1
–
Infant (\1 year) Total
The mean values ± SD indicate differences in survey counts: Group F and the all-male group were surveyed six times and group L was surveyed five times (cf. Leca, Gunst, & Huffman, 2007 for criteria of age classification in Japanese macaques)
and scavenged food remains left behind by groups F and L the day before. Inter-individual arrival times and positions at the feeding site suggested that spatio-temporal coordination was looser in the all-male group than in the two neighboring mixed-sex groups. However, three types of data supported the persistent existence of the all-male group (as opposed to an occasional aggregation of solitary males). First, most members of the all-male group tended to arrive at, and leave from, the feeding site within a short period of time (generally around 15 min). Second, these males were often involved in allo-grooming activity around the feeding site. Third, our repeated survey counts of the all-male group provided consistent data pertaining to group size and composition (Table 1). Although the three groups of monkeys might have occasional contact with visitors in other parts of the forest, the food provisioning area was somewhat isolated and entry was restricted to a few researchers and park staff.
Procedure and Measures From November 14, 2012 to January 6, 2013, between 9:00 am and 4:00 pm, we conducted daily observations on the three groups. Observation times on Group F, Group L, and the allmale group were 79.4, 77.0, and 21.3 h, respectively. Most observations were made in the vicinity of the food provisioning site. Like most other surveys on rare and somewhat unpredictable animal behaviors, this study of male homosexual behavior was based on opportunistic observations and alloccurrence sampling (cf. Martin & Bateson, 1993). Whenever male homosexual behavior was observed, we focused on both consortship partners and continuously video-recorded behavioral data with a HDR-XR350 Sony digital camera. The six males involved in homosexual behavior could be identified individually. When collecting observational data on male– male consortships, we recorded the following behaviors and interactions: (1) same-sex solicitations, including grabbing, pushing, and crouching on the ground while emitting repeated shrieking vocalizations, (2) mounting behaviors, and (3) nonsexual inter-mount activities such as allo-grooming, resting, huddling, feeding, locomotion, and vigilance (cf. Hanby &
Brown, 1974; Vasey, VanderLaan, Rains, Duckworth, & Kovacovsky, 2008). For future comparative purposes, we used the same behavioral definitions and measures as those used in previous studies of heterosexual and female homosexual consortships in Japanese macaques (cf. Vasey, 2006). A male homosexual consortship was defined as a temporary, but exclusive, sexual association between two males and occurred when two partners engaged in a mount series (i.e., three or more mounts within a 10-min period). A consortship was deemed to have terminated if the two partners were not in proximity (separated by a distance of more than 1 m) and exhibited no mounting for 10 min. We also distinguished between two mounting postures: (1) dorso-ventral double foot-clasp mounts involved the mounter grasping with his feet between the mountee’s ankles and hips and with his hands on the mountee’s back (cf. Hanby & Brown, 1974; Vasey, Foroud, Duckworth, & Kovacovsky, 2006) and (2) ventro-ventral mounts occurred when the two participants embraced each other with their arms and legs, with chest-to-chest and belly-to-belly contact, facing each other in a standing, sitting or lying position. For each of these six mounting postures, we recorded whether or not the mounter performed pelvic thrusting (i.e., rhythmic movements of the mounter’s pelvic girdle toward the mountee’s perineum; cf. Vasey et al., 2006). Statistical analyses were performed using the SPSS 13.0 analytical program. Significance levels were set at a = .05.
Results Individuals Involved in Male Homosexual Consortships We observed male homosexual behaviors in three different male–male dyads, involving a total of six different individuals. Within each of the three dyads, the younger individual was a juvenile male (aged 3 years) and the older individual was either a young adult (between 7 and 10 years old for dyads A and B) or a middle-aged adult male (between 11 and 15 years old for dyad C). None of the three dyads was
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involved in homosexual behavior for more than one observation day. The three adult males and two of the three juvenile males (from dyads A and B) were members of the all-male group. The juvenile male of dyad C was probably in the process of migrating from group L to the all-male group, as he was observed interacting with members of both groups within the same day. However, all the male homosexual consortships occurred within the all-male group. We did not observe male homosexual behavior in groups F and L, despite longer observation times on these two mixed-sex groups. Male Homosexual Solicitations, Consortships, and Mounting Behaviors We recorded a total of 63 male–male mounts within nine consortships. The average duration of male homosexual consortships was 8.4 ± 4.8 min, range, 1.9–17.1 (Table 2). There was no significant difference in the duration of male homosexual consortships observed in the all-male group at Minoo and between subadult central males and adult solitary males at Arashiyama (M ± SD: 8.4 ± 4.8 min and 14.0 ± 15.4 min, respectively; Mann–Whitney U test, z = -.04, NMinoo = NArashiyama = 9; cf. Takenoshita, 2012 for data on male homosexual behavior at Arashiyama). We found that 49 mounts (77.8 %) were solicited by the juvenile males who grabbed (59.2 %) or pushed (22.4 %) their adult male partners or crouched on the ground while screaming (18.4 %) within a few seconds before mounting occurred. In dyad A, mounts were almost exclusively unidirectional, with 97.3 % of mounts (36 out of 37 mounts) being performed by the adult male. In the other two dyads, mounts were more bidirectional, with the juvenile and the adult male performing similar number of mounts within a given mount series (56.2 and
60.0 % of mounts performed by the adult male in dyads B and C, respectively) (Table 2). All mounts performed in dyad A were ventro-ventral (N = 37). Ventro-ventral mounting was characterized by the two participants embracing each other with their arms and legs, with chest-to-chest and belly-to-belly contact, facing each other in a standing, sitting or lying position and with the juvenile male hanging below the body of the adult male (Fig. 1a). In contrast, all mounts performed in dyads B and C were dorso-ventral double foot-clasp mounts (N = 26). We compared the duration of male homosexual mounts with respect to two types of posture, namely ventro-ventral and dorso-ventral double foot-clasp. We found that the former were significantly longer than the latter (M ± SD: 10.5 ± 2.9 s and 6.9 ± 1.2 s, respectively), Mann–Whitney U test, z = -4.64, Nventro-ventral = 37, Ndorso-ventral = 26, p\.001.
Table 2 Number and duration of male homosexual consortships within three male–male dyads, including the percentage of time both partners spent in body contact and the number of mounts performed by each partner Dyad Consortship
Number of mounts performed
No. Duration % time in By adult (min) body contact male A
B
C
By juvenile male
1
7.9
96.4
10
0
2
17.1
90.4
13
0
3
1.9
100
2
1
4 5
14.8 5.1
97.5 100
11 2
0 2
6
7.7
100
3
2
7
8.3
100
4
3
8
8.2
100
4
2
9
4.8
100
2
2
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Fig. 1 Male homosexual consortship between a young adult and a juvenile (dyad A), engaged in a ventro-ventral mount (a), and embracing each other in a sitting position (b) (note the redness of the juvenile male’s face). Photo by N. Gunst
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We compared the duration of dorso-ventral double foot-clasp male–male mounts in two types of context: mount series in a homosexual context (this study) and single mounts in a sociosexual context (i.e., when a higher-ranking male mounted a lower-ranking male as part of a dominance display; Leca, unpublished data collected in the Arashiyama group of Japanese macaques). We found that the former were significantly longer than the latter (M ± SD: 6.9 ± 1.2 s and 4.4 ± 0.8 s, respectively), Mann–Whitney U test, z = -4.94, Nhomosexual = 26, Nsociosexual = 14, p\.001. In all male homosexual mounts, the mounter performed pelvic thrusting. When mounting their younger partners, the three adult males showed penile erection during all mounts. However, we did not observe anal intromission and ejaculation in any of these male–male mounts. Although we did not observe penile erection in the juvenile males during homosexual consortships, they showed bright red faces (Fig. 1b) and emitted repeated shrieks, both of which are indicative of sexual receptivity. Inter-Mount Activities and Body Orientations During Male Homosexual Consortships When not engaged in mounts, the main three activities exhibited by male consort partners were allo-grooming (48.2 ± 14.9 % of inter-mount time), resting (36.2 ± 11.0 %), and vigilance (13.2 ± 9.9 %) (Fig. 2). All allo-grooming bouts were directed to the male mate. In general, male mates did not separate between mounts (2.2 ± 0.3 % of inter-mount time)(Fig. 2). Rather, during inter-mount intervals, they typically stayed in body contact (97.8 ± 3.6 %) (Table 2) and huddled, i.e., faced each other in a ventro-ventral orientation (80.7 ± 5.2 %) (Fig. 1b). Vigilance activity occurred in all but one consortship. During the consortship in which vigilance did not occur, both partners were located at the periphery of the all-male group and hid themselves behind vegetation. We did not record
Fig. 2 Inter-mount activities during male homosexual consortships (mean percentage of time ± SD)
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any agonistic interactions between partners during male homosexual consortships. In six cases, male homosexual consortships terminated when one of the two partners left and no mounting was recorded for at least 10 min. In three cases, intrusions terminated the consortships. In each of these instances, a third-party male aggressed the consorting juvenile male. However, the male intruders did not attempt to acquire exclusive access to the juvenile males as sexual partners following the intrusions.
Discussion Ten types of convergent behavioral data supported the conclusion that the male–male consortship activity observed was sexual in character. First, as with all heterosexual and female homosexual sexual activity, male–male sexual interactions occurred during the fall-winter mating season. Second, most mounts were triggered by sexual solicitations performed by one partner and hence could be linked to sexual proceptivity on the part of the soliciting individual. Third, the sexual solicitations males performed were similar to those exhibited during heterosexual and female homosexual interactions (Vasey, Rains, VanderLaan, Duckworth, & Kovacovsky, 2008). Fourth, all of the male–male sexual solicitations and mounting we observed occurred with the context of temporary, but exclusive sexual relationships (i.e., consortships), as is the case with male– female and female–female sexual interactions. Fifth, all of the male–male mounts we observed occurred as part of a series of mounting episodes in which multiple mounts were performed, as opposed to single mounts. Series mounting is characteristic of both heterosexual and female homosexual consortships, whereas sociosexual mounts between males are typically single mounts and do not occur during consortships (VanderLaan et al., 2012). Sixth, the mounter performed pelvic thrusting during all of the male–male mounts that we observed. Pelvic thrusting occurs during almost all heterosexual mounts performed by males, but does not necessarily occur during male– male sociosexual mounts (Leca, unpublished data collected at Arashiyama; Vasey et al., 2006). Seventh, when engaging in same-sex mounts, the three adult males showed penile erection. Eighth, the dorso-ventral double foot-clasp male–male mounts observed during homosexual consortships were longer in duration than those observed in sociosexual contexts. This difference in mount duration may result from immediate sexual reward experienced by the mounter that possibly occurs during same-sex mounts with thrusting, as the erect penis of the mounter is thrust against the body of the mountee. Ninth, the three juvenile males who engaged in same-sex consortships exhibited physical and behavioral cues that are indicative of increased sexual receptivity during the estrus period in female Japanese macaques, namely a reddening of the face and shrieking vocalizations (reminiscent of female estrus calls) (cf. Hanby
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& Brown, 1974; Tokuda, 1961). These two cues were also reported in sub-adult central males engaged in homosexual consortships with young adult solitary males at Arashiyama (Takenoshita, 1998, 2012). The existence of female-typical sexual behaviors (i.e., shrieking vocalizations) in juvenile males underscores the fact that males in this species exhibit bisexual potential, which Dixson (2012) argued is characteristic of many non-human primate species. Although the gonadal condition of the juvenile males was not investigated, it is noteworthy that their scrotal sacks lacked the deep reddish hue that is typical of sexually active adult males. This suggests that although these juvenile males engaged in sexual behavior, they were not yet fully sexually mature in a physiological sense. Tenth, aggressive responses by third-party males toward male homosexual consortships that were not performed in the service of sexual partner acquisition were similar to third-party male ‘‘interference’’ behavior that is directed to both heterosexual and female homosexual consortships (cf. Huffman, 1991; Vasey, 2004). Although we did not observe anal intromission and ejaculation, neither should be considered the sine qua non of male– male sexual behavior in animals or humans for that matter (Bagemihl, 1999; Vasey, 1995, 2002). It is possible that some events of anal intromission and ejaculation remained unnoticed due to the difficulty of continuously video-recording close-up behavioral data in the field, in part due to the mountainous terrain at Minoo. Further, to obtain data on anal intromission, it is necessary that the animals be extremely habituated as the observer must be positioned beside the animals and then look directly downward to verify if anal intromission is occurring. Failing this, the mounter’s body blocks the observer’s view and anal intromission cannot be verified. Obviously, such conditions are extremely rare in the field and the macaques at Minoo were not habituated to the point where such close-up observations were possible. It is noteworthy, however, that anal intromission during male–male mounts among juveniles has been observed at Arashiyama where the Japanese macaques are much more habituated to the presence of human observer (Vasey, personal observations, 2000–2010). Further, it deserves mention that observations of ejaculate on the back of a male mountee cannot necessarily be taken as evidence that anal intromission has occurred. In light of the aforementioned ten lines of evidence, it seems parsimonious to conclude that the male–male consortship activity reported in this study was sexual in nature, given that it was characterized by numerous behavioral components that typify heterosexual and female homosexual interactions in Japanese macaques. Accordingly, we believe that the available evidence supports the conclusion that the male–male-mounting and sexual solicitations reported here can be accurately categorized as sexual behaviors. Our observations of ventro-ventral mounting in one male–male consortship dyad—a pattern which is unusual in Japanese macaques (but see Vasey & Reinhart,
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2009)—may reflect a flexible behavioral response by two sexually motivated partners whose body size discrepancies do not allow for double-foot clasp mounting. A similar explanation for ventro-ventral mounting in male mountain gorillas has been proposed (Yamagiwa, 1987). Our data set was too small to formally test different explanatory hypotheses about the occurrence of male homosexual behavior in an all-male group of Japanese macaques. However, this preliminary report was also intended as a forum for proposing a series of explanations that may serve as a launching pad for future studies on this topic. First, same-sex mounting may allow immature male Japanese macaques to learn copulatory skills that are essential later in a heterosexual context. The ‘‘practice for heterosexual sex hypothesis’’has been proposed to account for same-sex mounts in immature individuals in a variety of animal taxa (Dagg, 1984; Vasey, 1995). Interestingly, all the male–male consortship dyads observed in our study were combinations of immature and mature males, which was consistent withprevious reports of male homosexual consortships in Japanese macaques (Takenoshita, 1998, 2012). As such, this hypothesis might explain why the sexually inexperienced males we observed would engage in homosexual behavior, but it cannot explain why the sexually experienced ones would. This underscores an important point, namely, that each partner in a sexual exchange may have different motivations for engaging in the sexual interaction. Second, male–male mounts in Japanese macaques may facilitate adaptive social goals in the context of all-male groups, such as dominance demonstration, alliance formation either during or after group transfer, tension regulation, or reconciliation. Longitudinal data on a captive multimale-multifemale group of Japanese macaques indicated that male–male mounting may be caused by such a multiplicity of factors (Hanby, 1974). Young male Japanese macaques are the most frequent participants in mounting interactions and most of these interactions are sociosexual in nature (Hanby & Brown, 1974; VanderLaan et al., 2012). The ‘‘sociosexual hypothesis’’ has been proposed to account for male homosexual behavior in a variety of other non-human primate species (stumptail macaques, Macaca arctoides: Chevalier-Skolnikoff, 1976; whitehandedgibbons,Hylobateslar:Edwards&Todd,1991;Sumatran orangutans, Pongo pygmaeus abelii: Fox, 2001; olive baboons, Papio anubis: Smuts & Watanabe, 1990; Hanuman langurs: Sommer et al., 2006; pigtailed macaques, Macaca nemestrina: Tokuda, Simons, & Jensen, 1968). Human males that belong to all-male groups sometimes engage in same-sex behaviors that appear superficially sexual, but which are formally enacted to facilitate some sort of social goal. For example, members of male-only support structures (e.g., fraternities, boarding schools, or military academies) often displayed a wide variety of behaviors that have been characterized as homosocial bonding and that may be used to recruit new members (Anderson, 2009; Connell & Messerschmidt,
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2005; Flood, 2008). Although some of these male–male interactions (e.g., extended kissing on the lips, genital exposure, and penis-grabbing games) may be defined as homosexual in other contexts, the participants themselves described these behaviors as non-sexual means of expressing platonic affection among heterosexual friends (Anderson, Adams, & Rivers, 2012; Prohaska & Gailey, 2010). Similarly, in traditional Melanesian societies, the performance of ritualized homosexual acts within all-male groups contributes to the establishment of male–male bonds (Kelly, 1993). Third, male homosexual behavior may be a developmental by-product of play mounting activity. In Japanese macaques, juvenile male–male mounting in a double foot-clasp posture is typically performed as a sociosexual signal to facilitate social play or reduce tension (Hanby & Brown, 1974; VanderLaan et al., 2012). Immature males may first experience same-sex genital stimulation during playful interactions with peer playmates; then, after leaving their natal group, they may continue to seek similar sexual reward with same-sex partners, particularly under the demographic conditions of an allmale group. The‘‘developmental by-product hypothesis’’has been proposed to account for male–male mounts between adult ‘‘silverbacks’’ and subadults in all-male groups of mountain gorillas (Yamagiwa, 2006). Fourth, male homosexual behavior in all-male groups of animals, like in the all-male group of Japanese macaques at Minoo, may be a substitute for heterosexual sex in the absence of opposite-sex partners. The ‘‘outlet for sexual frustration hypothesis’’ (or ‘‘heterosexual deprivation hypothesis’’: Vasey & Gauthier, 2000) has been invoked to explain male–male mounting in animals, such as feral cats (Yamane, 2006). Similarly‘‘situational’’homosexuality is expressed by human males under a variety of same-sex settings (Anderson, 2009; Burg, 1983; Flynt, 1902; Gear, 2005; Kirkham, 2000; Moodie, Ndatshe, & Sibuyi, 1989). Fifth, it might be argued that adult male Japanese macaques mounted immature males because they mistook them for females, owing to their relative small body sizes and estruslike cues. The‘‘mistaken sexual identity hypothesis’’has been invoked to explain cases of male–male mounting in sexually monomorphic species of birds (e.g., Birkhead, Johnson, & Nettleship, 1985). However, this hypothesis is implausible in our case because Japanese macaques are not monomorphic, males’ scrotums are conspicuous, and group-living monkeys know each other well (Seyfarth & Cheney, 2012). As this overview of possible explanatory hypotheses makes clear, further research is needed to ascertain whether male–male homosexual behavior in Japanese macaques is an adaptation that evolved due to direct selection or a neutral behavioral by-product that exists because it does not negatively impact reproduction and is linked to some possible adaptation, such as sociosexual male–male mounting among juveniles (VanderLaan et al., 2012). The‘‘neutral by-product
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hypothesis’’ has been proposed to explain the origin and maintenance of female homosexual behavior in Japanese macaques (Vasey, 2006; Vasey & VanderLaan, 2012). It is important to note that the hypotheses presented above, and particularly the‘‘sexual’’and‘‘sociosexual’’functions of same-sex mounting behavior, are not necessarily mutually exclusive. Variation between and within individuals (e.g., males versus females, immature versus sexually mature individuals), populations, and species in the form and function of homosexual behavior may reflect multiple motivations, different developmental pathways, and divergent evolutionary histories, which require different explanatory frameworks (Vasey & Sommer, 2006). To further assess the nature of male–male mounting in this all-male group of Japanese macaques, future observations should be conducted both during and outside the mating season. We conclude that the behaviors reported here were homosexual behaviors, based on the ten pieces of evidence previously mentioned. At present, there is no evidence that this homosexual behavior reflects homosexual orientation. Rather, it likely reflects Japanese macaque males’ potential for bisexual behavior, which exists in several other Old World monkeys and in great apes (Dixson, 2012). The expression of male homosexual behavior might be favored by the particular sociodemographic setting under study here, namely the occurrence of an all-male group. More research on male homosexual behavior in non-human primates is needed, particularly in all-male groups. When considering how our results may apply to the evolution of human sexuality, one should keep in mind that although reproductive behaviors in humans and Japanese macaques likely share homologous features, non-conceptive sexual behaviors in these two species may be analogous. Exclusive same-sex sexual orientation has not been documented in any free-ranging nonhuman primate species, including Japanese macaques. As such, the study of homosexual behavior in non-human primates may inform us about the evolution of homosexual behavior in humans, but may shed only limited light as to why exclusive male homosexuality evolved. Acknowledgments This study was funded by the following agen cies: Natural Sciences and Engineering Research Council of Canada (NSERC), Alberta Innovates Health Solutions (AIHS), Japan Society for the Promotion of Science (JSPS), American Institute of Bisexuality (AIB), the L.S.B. Leakey Foundation, as well as the Office of the Dean of Arts and Science and the Office of Research Services at the University of Lethbridge. We thank Lydia Ottenheimer Carrier for assistance with data collection. We thank Penny D’Agnone for help securing AIHS funding. We thank Y. Iwanaga for permission to work at Meiji Memorial Forest Minoo Park and S. Suzuki for valuable information in the field. We thank the Editor, Alan Dixson, and one anonymous reviewer for fruitful comments on a previous version of the article.
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ORIGINAL PAPER
Male Homosexual Behavior in a Free-Ranging All-Male Group of Japanese Macaques at Minoo, Japan Jean-Baptiste Leca • Noe¨lle Gunst • Paul L. Vasey
Received: 27 February 2013 / Revised: 1 May 2013 / Accepted: 19 April 2014 / Published online: 28 May 2014 Ó Springer Science+Business Media New York 2014
Abstract We documented nine male homosexual consortships within three different male–male dyads in a free-ranging all-male group of Japanese macaques (Macaca fuscata), at Minoo, Japan. A total of 63 male–male mounts were observed during these consortships. Male homosexual interactions shared most of the behavioral components that have been reported to characterize heterosexual and female homosexual consortships in this species. Convergent behavioral data, including analysis of male–male solicitations, mounting postures, body orientations, inter-mount activities, and third-party male intrusions supported the conclusion that male–male consortships are a sexual phenomenon. We discussed a series of proximate and ultimate hypotheses that purport to account for the occurrence of male homosexual behavior in all-male groups of primates, including humans. This first report of male homosexual interactions in an all-male group of Japanese macaques contributes to the growing database used to provide insights into the developmental processes, causal mechanisms, adaptive significance, and phylogenetic pathways of same-sex sexual behavior. Keywords Male–male consortship Ventro-ventral mounts Sociosexual behavior Macaca fuscata
Introduction Homosexual behavior is typically defined as an interaction involving courtship displays (or sexual solicitations), mounting, and genital contact and/or stimulation between same-sex J.-B. Leca (&) N. Gunst P. L. Vasey Department of Psychology, University of Lethbridge, 4401 University Drive, Lethbridge, AB T1K 3M4, Canada e-mail: [email protected]
individuals (Vasey & Sommer, 2006). Although widespread in the animal kingdom, such behavioral patterns represent an evolutionary conundrum because they do not directly contribute to reproduction (Bagemihl, 1999; Poiani, 2010; Sommer & Vasey, 2006; Wallen & Parsons, 1997). In an attempt to address this apparent paradox, homosexual behaviors are often viewed as sociosexual, that is, behaviors that are sexual in their structure, but underlain by little or no sexual motivation and instead performed for their adaptive social functions (Wickler, 1967). Sociosexual behavioral patterns are common in several species of Old World monkeys and great apes (Dixson, 2012; Wallen & Parsons, 1997). However, there is no a priori reason why samesex mounts could not be also sexually motivated (Vasey & VanderLaan, 2012). As Dixson (2012) noted, ‘‘There is not a rigid dichotomy between the ‘sexual’ and ‘sociosexual’ functions of isosexual behavior’’(pp. 218–220).1 Several other proximate and ultimate hypotheses have been proposed to account for same-sex sexual behaviors in animals, including humans (reviewed in Poiani, 2010). For example, sex ratio bias is one of the main life history traits invoked to explain same-sex sexual behaviors in male and female birds and mammals. A lack of opposite-sex sexual partners and the availability of same-sex mates during mating periods may create a demographic constraint that leads to the expression of homosexual behavior. This is alternatively referred to as the ‘‘heterosexual deprivation hypothesis’’ (Vasey & Gauthier, 2000), the ‘‘bestof-a-bad-job hypothesis’’(Poiani, 2010), or a‘‘Hobson’s choice’’ (sensu Fedigan, 1982). It seems intuitive to predict that individuals living in unisexual groups will exhibit more homosexual interactions than those living in mixed-sex groups (i.e., 1
Isosexual behavior includes same-sex mounting and presentation and is considered a neutral term (rather than sociosexual, homosexual, or bisexual behavior) that does not involve any assumptions about the motivation of the participants (Dixson, 2012).
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groups including members of both sexes). For example, in a captive setting and during the mating season, an all-male group of rhesus macaques (Macaca mulatta), with visual access to a mixed-sex group, engaged in series of male–male mounts, some terminating with ejaculation(Gordon & Bernstein, 1973). Interestingly, unisexual male groups commonly occur in natural settings in species that form polygynous or multi-male/ multi-female breeding groups. In many gregarious primate species, dispersing individuals transfer directly from one mixedsex group to another, but, in others, including several colobine and cercopithecine species, individuals may join non-breeding (usually all-male) groups for variable periods (Pusey & Packer, 1987). All-male groups of primates are typically subordinate to mixed-sex groups, either travelling independently or occupying suboptimal ranges around mixed-sex groups (e.g., rhesus macaques: Drickamer & Vessey, 1973; Tana River red colobus, Colobus badius rufomitratus: Marsh, 1979; geladas, Theropithecus gelada: Kawai, Dunbar, & Ohsawa, 1983; Thomas’s leaf monkeys, Presbytis thomasi: Gurmaya, 1986; patas monkeys, Erythrocebus patas: Ohsawa, Inoue, & Takenaka, 1993; proboscis monkeys, Nasalis larvatus: Yeager, 1995; ursine colobus, Colobus vellerosus: Sicotte & MacIntosh, 2004). Despite the fact that they are common in many primate species, all-male groups have rarely been the focus of any detailed studies. Male–male sexual activity has been reported in some allmale groups of non-human primates. For example, in wild mountain gorillas (Gorilla gorilla beringei), male homosexual behavior occurred frequently in all-male groups, but was rarely observed in mixed-sex groups (Yamagiwa, 1987). Genital stimulation during male–male mounts in all-male groups of mountain gorillas did not seem to serve any sociosexual functions, but instead occurred in purely sexual contexts, with intensive sexual competition between adult males for access to sub-adult male partners (Yamagiwa, 1987, 2006). Although detailed studies are extremely rare (for notable exceptions, see mona monkeys, Cercopithecus mona: Glenn, Matsuda, & Bensen, 2002; Hanuman langurs, Presbytis entellus: Sommer, Schauer, & Kyriazis, 2006; mountain gorillas: Yamagiwa, 2006), research on male homosexual behavior in all-male groups of primates under natural settings may provide insights into the developmental processes, causal mechanisms, adaptive significance, and phylogenetic pathways that characterize male same-sex sexual behavior in humans. There are three reasons why the Japanese macaque (Macaca fuscata) is an ideal non-human primate model for research on male homosexual behavior. First, immature male Japanese macaques display a large repertoire of sociosexual behavioral patterns, such as male–male mounts in playful or tension-reduction contexts (Gunst, Leca, & Vasey, 2013; Hanby & Brown, 1974; VanderLaan, Pellis, & Vasey, 2012). Second, certain populations on the island of Honshu in central Japan (e.g., at Arashiyama, near Kyoto city) have been reported to exhibit male homosexual behavior (Takenoshita, 1998, 2012). Patterns
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of courtship, mounting, and inter-mount behavior are very similar across male–male and male–female sexual interactions (Takenoshita, 2012). Third, long-term studies of life history of Japanese macaques showed that almost all males eventually leave their natal group between the ages of 3–8 years, mainly during the mating season. Such males may either transfer directly into another mixed-sex group, temporarily join an allmale group or remain solitary for a period of time (Sprague, Suzuki, Takahashi, & Sato, 1998; Sugiyama, 1976). All-male groups of Japanesemacaques have been reported at several field sites, including Arashiyama, Kinkazan, Koshima, Minoo, Ryozenyama, and Shodoshima (Kawamura & Kawai, 1956; Koyama, 1970; Matsumura, 1993; Mori & Watanabe, 2003; Sprague et al., 1998; Sugiyama & Ohsawa, 1982; Yamada, 1966), but detailed studies of these naturally occurring groups are needed. To our knowledge, there are no reports of male homosexual behavior in free-ranging all-male groups of Japanese macaques. Our objectives were: (1) to document and describe male–male consortship activity, (2) to assess the sexual nature of such interactions, and (3) to discuss a series of proximate and ultimate hypotheses about the occurrence of male homosexual behavior in all-male groups of Japanese macaques and other primate species, including humans.
Method Study Site and Groups We studied three free-ranging groups of Japanese macaques, living in the Meiji Memorial Forest of Minoo Park located on the outskirts of Minoo city, Osaka Prefecture, central Japan. The first two groups, namely Minoo F and Minoo L, were mixed-sex multimale–multifemale groups, derived from an original group that fissioned into two stable social units in 1955 (S. Suzuki, personal communication). The third group was an all-male group. Although there are no recent reports on the all-male Minoo group, its origins may be traced back to the main group fission (Kawamura & Kawai, 1956). Group sizes and compositions are shown in Table 1. The three groups foraged extensively on natural foods occurring within their respective home ranges. In order to prevent the monkeys from roaming around Minoo city, the park staff provided groups F and L with wheat grains and soy beans twice a day, along a 500-m stretch of mountain trail (Y. Iwanaga, personal communication). Groups F and L generally spent from 2 to 4 h each day around the food provisioning site. These two groups were separated by a 50 to 100-m buffer zone, within which aggressive inter-group encounters occurred. The all-male group was not directly fed by the park staff. However, members of the all-male group typically arrived at the feeding site early in the morning (before groups F and L)
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Table 1 Size and composition of the three study groups during the study period Old adult ([15 years)
Middle-aged adult (11–15 years)
Young adult (7–10 years)
Subadult (4–6 years)
Juvenile (1–3 years)
Group
Male
Female
Male
Female
Male
Female
Male
Female
Male
Female
F
7±1
18 ± 2
8±1
18 ± 3
9±1
11 ± 2
4±1
12 ± 2
9±1
6±1
10 ± 1
111 ± 7
L
2±1
5±1
6±1
19 ± 2
4±1
11 ± 1
1±1
7±1
5±1
4±1
6±1
71 ± 5
–
2±1
6±2
–
3±1
–
–
15 ± 3
All-male 1 ± 1
–
4±1
–
Infant (\1 year) Total
The mean values ± SD indicate differences in survey counts: Group F and the all-male group were surveyed six times and group L was surveyed five times (cf. Leca, Gunst, & Huffman, 2007 for criteria of age classification in Japanese macaques)
and scavenged food remains left behind by groups F and L the day before. Inter-individual arrival times and positions at the feeding site suggested that spatio-temporal coordination was looser in the all-male group than in the two neighboring mixed-sex groups. However, three types of data supported the persistent existence of the all-male group (as opposed to an occasional aggregation of solitary males). First, most members of the all-male group tended to arrive at, and leave from, the feeding site within a short period of time (generally around 15 min). Second, these males were often involved in allo-grooming activity around the feeding site. Third, our repeated survey counts of the all-male group provided consistent data pertaining to group size and composition (Table 1). Although the three groups of monkeys might have occasional contact with visitors in other parts of the forest, the food provisioning area was somewhat isolated and entry was restricted to a few researchers and park staff.
Procedure and Measures From November 14, 2012 to January 6, 2013, between 9:00 am and 4:00 pm, we conducted daily observations on the three groups. Observation times on Group F, Group L, and the allmale group were 79.4, 77.0, and 21.3 h, respectively. Most observations were made in the vicinity of the food provisioning site. Like most other surveys on rare and somewhat unpredictable animal behaviors, this study of male homosexual behavior was based on opportunistic observations and alloccurrence sampling (cf. Martin & Bateson, 1993). Whenever male homosexual behavior was observed, we focused on both consortship partners and continuously video-recorded behavioral data with a HDR-XR350 Sony digital camera. The six males involved in homosexual behavior could be identified individually. When collecting observational data on male– male consortships, we recorded the following behaviors and interactions: (1) same-sex solicitations, including grabbing, pushing, and crouching on the ground while emitting repeated shrieking vocalizations, (2) mounting behaviors, and (3) nonsexual inter-mount activities such as allo-grooming, resting, huddling, feeding, locomotion, and vigilance (cf. Hanby &
Brown, 1974; Vasey, VanderLaan, Rains, Duckworth, & Kovacovsky, 2008). For future comparative purposes, we used the same behavioral definitions and measures as those used in previous studies of heterosexual and female homosexual consortships in Japanese macaques (cf. Vasey, 2006). A male homosexual consortship was defined as a temporary, but exclusive, sexual association between two males and occurred when two partners engaged in a mount series (i.e., three or more mounts within a 10-min period). A consortship was deemed to have terminated if the two partners were not in proximity (separated by a distance of more than 1 m) and exhibited no mounting for 10 min. We also distinguished between two mounting postures: (1) dorso-ventral double foot-clasp mounts involved the mounter grasping with his feet between the mountee’s ankles and hips and with his hands on the mountee’s back (cf. Hanby & Brown, 1974; Vasey, Foroud, Duckworth, & Kovacovsky, 2006) and (2) ventro-ventral mounts occurred when the two participants embraced each other with their arms and legs, with chest-to-chest and belly-to-belly contact, facing each other in a standing, sitting or lying position. For each of these six mounting postures, we recorded whether or not the mounter performed pelvic thrusting (i.e., rhythmic movements of the mounter’s pelvic girdle toward the mountee’s perineum; cf. Vasey et al., 2006). Statistical analyses were performed using the SPSS 13.0 analytical program. Significance levels were set at a = .05.
Results Individuals Involved in Male Homosexual Consortships We observed male homosexual behaviors in three different male–male dyads, involving a total of six different individuals. Within each of the three dyads, the younger individual was a juvenile male (aged 3 years) and the older individual was either a young adult (between 7 and 10 years old for dyads A and B) or a middle-aged adult male (between 11 and 15 years old for dyad C). None of the three dyads was
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involved in homosexual behavior for more than one observation day. The three adult males and two of the three juvenile males (from dyads A and B) were members of the all-male group. The juvenile male of dyad C was probably in the process of migrating from group L to the all-male group, as he was observed interacting with members of both groups within the same day. However, all the male homosexual consortships occurred within the all-male group. We did not observe male homosexual behavior in groups F and L, despite longer observation times on these two mixed-sex groups. Male Homosexual Solicitations, Consortships, and Mounting Behaviors We recorded a total of 63 male–male mounts within nine consortships. The average duration of male homosexual consortships was 8.4 ± 4.8 min, range, 1.9–17.1 (Table 2). There was no significant difference in the duration of male homosexual consortships observed in the all-male group at Minoo and between subadult central males and adult solitary males at Arashiyama (M ± SD: 8.4 ± 4.8 min and 14.0 ± 15.4 min, respectively; Mann–Whitney U test, z = -.04, NMinoo = NArashiyama = 9; cf. Takenoshita, 2012 for data on male homosexual behavior at Arashiyama). We found that 49 mounts (77.8 %) were solicited by the juvenile males who grabbed (59.2 %) or pushed (22.4 %) their adult male partners or crouched on the ground while screaming (18.4 %) within a few seconds before mounting occurred. In dyad A, mounts were almost exclusively unidirectional, with 97.3 % of mounts (36 out of 37 mounts) being performed by the adult male. In the other two dyads, mounts were more bidirectional, with the juvenile and the adult male performing similar number of mounts within a given mount series (56.2 and
60.0 % of mounts performed by the adult male in dyads B and C, respectively) (Table 2). All mounts performed in dyad A were ventro-ventral (N = 37). Ventro-ventral mounting was characterized by the two participants embracing each other with their arms and legs, with chest-to-chest and belly-to-belly contact, facing each other in a standing, sitting or lying position and with the juvenile male hanging below the body of the adult male (Fig. 1a). In contrast, all mounts performed in dyads B and C were dorso-ventral double foot-clasp mounts (N = 26). We compared the duration of male homosexual mounts with respect to two types of posture, namely ventro-ventral and dorso-ventral double foot-clasp. We found that the former were significantly longer than the latter (M ± SD: 10.5 ± 2.9 s and 6.9 ± 1.2 s, respectively), Mann–Whitney U test, z = -4.64, Nventro-ventral = 37, Ndorso-ventral = 26, p\.001.
Table 2 Number and duration of male homosexual consortships within three male–male dyads, including the percentage of time both partners spent in body contact and the number of mounts performed by each partner Dyad Consortship
Number of mounts performed
No. Duration % time in By adult (min) body contact male A
B
C
By juvenile male
1
7.9
96.4
10
0
2
17.1
90.4
13
0
3
1.9
100
2
1
4 5
14.8 5.1
97.5 100
11 2
0 2
6
7.7
100
3
2
7
8.3
100
4
3
8
8.2
100
4
2
9
4.8
100
2
2
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Fig. 1 Male homosexual consortship between a young adult and a juvenile (dyad A), engaged in a ventro-ventral mount (a), and embracing each other in a sitting position (b) (note the redness of the juvenile male’s face). Photo by N. Gunst
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We compared the duration of dorso-ventral double foot-clasp male–male mounts in two types of context: mount series in a homosexual context (this study) and single mounts in a sociosexual context (i.e., when a higher-ranking male mounted a lower-ranking male as part of a dominance display; Leca, unpublished data collected in the Arashiyama group of Japanese macaques). We found that the former were significantly longer than the latter (M ± SD: 6.9 ± 1.2 s and 4.4 ± 0.8 s, respectively), Mann–Whitney U test, z = -4.94, Nhomosexual = 26, Nsociosexual = 14, p\.001. In all male homosexual mounts, the mounter performed pelvic thrusting. When mounting their younger partners, the three adult males showed penile erection during all mounts. However, we did not observe anal intromission and ejaculation in any of these male–male mounts. Although we did not observe penile erection in the juvenile males during homosexual consortships, they showed bright red faces (Fig. 1b) and emitted repeated shrieks, both of which are indicative of sexual receptivity. Inter-Mount Activities and Body Orientations During Male Homosexual Consortships When not engaged in mounts, the main three activities exhibited by male consort partners were allo-grooming (48.2 ± 14.9 % of inter-mount time), resting (36.2 ± 11.0 %), and vigilance (13.2 ± 9.9 %) (Fig. 2). All allo-grooming bouts were directed to the male mate. In general, male mates did not separate between mounts (2.2 ± 0.3 % of inter-mount time)(Fig. 2). Rather, during inter-mount intervals, they typically stayed in body contact (97.8 ± 3.6 %) (Table 2) and huddled, i.e., faced each other in a ventro-ventral orientation (80.7 ± 5.2 %) (Fig. 1b). Vigilance activity occurred in all but one consortship. During the consortship in which vigilance did not occur, both partners were located at the periphery of the all-male group and hid themselves behind vegetation. We did not record
Fig. 2 Inter-mount activities during male homosexual consortships (mean percentage of time ± SD)
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any agonistic interactions between partners during male homosexual consortships. In six cases, male homosexual consortships terminated when one of the two partners left and no mounting was recorded for at least 10 min. In three cases, intrusions terminated the consortships. In each of these instances, a third-party male aggressed the consorting juvenile male. However, the male intruders did not attempt to acquire exclusive access to the juvenile males as sexual partners following the intrusions.
Discussion Ten types of convergent behavioral data supported the conclusion that the male–male consortship activity observed was sexual in character. First, as with all heterosexual and female homosexual sexual activity, male–male sexual interactions occurred during the fall-winter mating season. Second, most mounts were triggered by sexual solicitations performed by one partner and hence could be linked to sexual proceptivity on the part of the soliciting individual. Third, the sexual solicitations males performed were similar to those exhibited during heterosexual and female homosexual interactions (Vasey, Rains, VanderLaan, Duckworth, & Kovacovsky, 2008). Fourth, all of the male–male sexual solicitations and mounting we observed occurred with the context of temporary, but exclusive sexual relationships (i.e., consortships), as is the case with male– female and female–female sexual interactions. Fifth, all of the male–male mounts we observed occurred as part of a series of mounting episodes in which multiple mounts were performed, as opposed to single mounts. Series mounting is characteristic of both heterosexual and female homosexual consortships, whereas sociosexual mounts between males are typically single mounts and do not occur during consortships (VanderLaan et al., 2012). Sixth, the mounter performed pelvic thrusting during all of the male–male mounts that we observed. Pelvic thrusting occurs during almost all heterosexual mounts performed by males, but does not necessarily occur during male– male sociosexual mounts (Leca, unpublished data collected at Arashiyama; Vasey et al., 2006). Seventh, when engaging in same-sex mounts, the three adult males showed penile erection. Eighth, the dorso-ventral double foot-clasp male–male mounts observed during homosexual consortships were longer in duration than those observed in sociosexual contexts. This difference in mount duration may result from immediate sexual reward experienced by the mounter that possibly occurs during same-sex mounts with thrusting, as the erect penis of the mounter is thrust against the body of the mountee. Ninth, the three juvenile males who engaged in same-sex consortships exhibited physical and behavioral cues that are indicative of increased sexual receptivity during the estrus period in female Japanese macaques, namely a reddening of the face and shrieking vocalizations (reminiscent of female estrus calls) (cf. Hanby
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& Brown, 1974; Tokuda, 1961). These two cues were also reported in sub-adult central males engaged in homosexual consortships with young adult solitary males at Arashiyama (Takenoshita, 1998, 2012). The existence of female-typical sexual behaviors (i.e., shrieking vocalizations) in juvenile males underscores the fact that males in this species exhibit bisexual potential, which Dixson (2012) argued is characteristic of many non-human primate species. Although the gonadal condition of the juvenile males was not investigated, it is noteworthy that their scrotal sacks lacked the deep reddish hue that is typical of sexually active adult males. This suggests that although these juvenile males engaged in sexual behavior, they were not yet fully sexually mature in a physiological sense. Tenth, aggressive responses by third-party males toward male homosexual consortships that were not performed in the service of sexual partner acquisition were similar to third-party male ‘‘interference’’ behavior that is directed to both heterosexual and female homosexual consortships (cf. Huffman, 1991; Vasey, 2004). Although we did not observe anal intromission and ejaculation, neither should be considered the sine qua non of male– male sexual behavior in animals or humans for that matter (Bagemihl, 1999; Vasey, 1995, 2002). It is possible that some events of anal intromission and ejaculation remained unnoticed due to the difficulty of continuously video-recording close-up behavioral data in the field, in part due to the mountainous terrain at Minoo. Further, to obtain data on anal intromission, it is necessary that the animals be extremely habituated as the observer must be positioned beside the animals and then look directly downward to verify if anal intromission is occurring. Failing this, the mounter’s body blocks the observer’s view and anal intromission cannot be verified. Obviously, such conditions are extremely rare in the field and the macaques at Minoo were not habituated to the point where such close-up observations were possible. It is noteworthy, however, that anal intromission during male–male mounts among juveniles has been observed at Arashiyama where the Japanese macaques are much more habituated to the presence of human observer (Vasey, personal observations, 2000–2010). Further, it deserves mention that observations of ejaculate on the back of a male mountee cannot necessarily be taken as evidence that anal intromission has occurred. In light of the aforementioned ten lines of evidence, it seems parsimonious to conclude that the male–male consortship activity reported in this study was sexual in nature, given that it was characterized by numerous behavioral components that typify heterosexual and female homosexual interactions in Japanese macaques. Accordingly, we believe that the available evidence supports the conclusion that the male–male-mounting and sexual solicitations reported here can be accurately categorized as sexual behaviors. Our observations of ventro-ventral mounting in one male–male consortship dyad—a pattern which is unusual in Japanese macaques (but see Vasey & Reinhart,
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2009)—may reflect a flexible behavioral response by two sexually motivated partners whose body size discrepancies do not allow for double-foot clasp mounting. A similar explanation for ventro-ventral mounting in male mountain gorillas has been proposed (Yamagiwa, 1987). Our data set was too small to formally test different explanatory hypotheses about the occurrence of male homosexual behavior in an all-male group of Japanese macaques. However, this preliminary report was also intended as a forum for proposing a series of explanations that may serve as a launching pad for future studies on this topic. First, same-sex mounting may allow immature male Japanese macaques to learn copulatory skills that are essential later in a heterosexual context. The ‘‘practice for heterosexual sex hypothesis’’has been proposed to account for same-sex mounts in immature individuals in a variety of animal taxa (Dagg, 1984; Vasey, 1995). Interestingly, all the male–male consortship dyads observed in our study were combinations of immature and mature males, which was consistent withprevious reports of male homosexual consortships in Japanese macaques (Takenoshita, 1998, 2012). As such, this hypothesis might explain why the sexually inexperienced males we observed would engage in homosexual behavior, but it cannot explain why the sexually experienced ones would. This underscores an important point, namely, that each partner in a sexual exchange may have different motivations for engaging in the sexual interaction. Second, male–male mounts in Japanese macaques may facilitate adaptive social goals in the context of all-male groups, such as dominance demonstration, alliance formation either during or after group transfer, tension regulation, or reconciliation. Longitudinal data on a captive multimale-multifemale group of Japanese macaques indicated that male–male mounting may be caused by such a multiplicity of factors (Hanby, 1974). Young male Japanese macaques are the most frequent participants in mounting interactions and most of these interactions are sociosexual in nature (Hanby & Brown, 1974; VanderLaan et al., 2012). The ‘‘sociosexual hypothesis’’ has been proposed to account for male homosexual behavior in a variety of other non-human primate species (stumptail macaques, Macaca arctoides: Chevalier-Skolnikoff, 1976; whitehandedgibbons,Hylobateslar:Edwards&Todd,1991;Sumatran orangutans, Pongo pygmaeus abelii: Fox, 2001; olive baboons, Papio anubis: Smuts & Watanabe, 1990; Hanuman langurs: Sommer et al., 2006; pigtailed macaques, Macaca nemestrina: Tokuda, Simons, & Jensen, 1968). Human males that belong to all-male groups sometimes engage in same-sex behaviors that appear superficially sexual, but which are formally enacted to facilitate some sort of social goal. For example, members of male-only support structures (e.g., fraternities, boarding schools, or military academies) often displayed a wide variety of behaviors that have been characterized as homosocial bonding and that may be used to recruit new members (Anderson, 2009; Connell & Messerschmidt,
Arch Sex Behav (2014) 43:853–861
2005; Flood, 2008). Although some of these male–male interactions (e.g., extended kissing on the lips, genital exposure, and penis-grabbing games) may be defined as homosexual in other contexts, the participants themselves described these behaviors as non-sexual means of expressing platonic affection among heterosexual friends (Anderson, Adams, & Rivers, 2012; Prohaska & Gailey, 2010). Similarly, in traditional Melanesian societies, the performance of ritualized homosexual acts within all-male groups contributes to the establishment of male–male bonds (Kelly, 1993). Third, male homosexual behavior may be a developmental by-product of play mounting activity. In Japanese macaques, juvenile male–male mounting in a double foot-clasp posture is typically performed as a sociosexual signal to facilitate social play or reduce tension (Hanby & Brown, 1974; VanderLaan et al., 2012). Immature males may first experience same-sex genital stimulation during playful interactions with peer playmates; then, after leaving their natal group, they may continue to seek similar sexual reward with same-sex partners, particularly under the demographic conditions of an allmale group. The‘‘developmental by-product hypothesis’’has been proposed to account for male–male mounts between adult ‘‘silverbacks’’ and subadults in all-male groups of mountain gorillas (Yamagiwa, 2006). Fourth, male homosexual behavior in all-male groups of animals, like in the all-male group of Japanese macaques at Minoo, may be a substitute for heterosexual sex in the absence of opposite-sex partners. The ‘‘outlet for sexual frustration hypothesis’’ (or ‘‘heterosexual deprivation hypothesis’’: Vasey & Gauthier, 2000) has been invoked to explain male–male mounting in animals, such as feral cats (Yamane, 2006). Similarly‘‘situational’’homosexuality is expressed by human males under a variety of same-sex settings (Anderson, 2009; Burg, 1983; Flynt, 1902; Gear, 2005; Kirkham, 2000; Moodie, Ndatshe, & Sibuyi, 1989). Fifth, it might be argued that adult male Japanese macaques mounted immature males because they mistook them for females, owing to their relative small body sizes and estruslike cues. The‘‘mistaken sexual identity hypothesis’’has been invoked to explain cases of male–male mounting in sexually monomorphic species of birds (e.g., Birkhead, Johnson, & Nettleship, 1985). However, this hypothesis is implausible in our case because Japanese macaques are not monomorphic, males’ scrotums are conspicuous, and group-living monkeys know each other well (Seyfarth & Cheney, 2012). As this overview of possible explanatory hypotheses makes clear, further research is needed to ascertain whether male–male homosexual behavior in Japanese macaques is an adaptation that evolved due to direct selection or a neutral behavioral by-product that exists because it does not negatively impact reproduction and is linked to some possible adaptation, such as sociosexual male–male mounting among juveniles (VanderLaan et al., 2012). The‘‘neutral by-product
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hypothesis’’ has been proposed to explain the origin and maintenance of female homosexual behavior in Japanese macaques (Vasey, 2006; Vasey & VanderLaan, 2012). It is important to note that the hypotheses presented above, and particularly the‘‘sexual’’and‘‘sociosexual’’functions of same-sex mounting behavior, are not necessarily mutually exclusive. Variation between and within individuals (e.g., males versus females, immature versus sexually mature individuals), populations, and species in the form and function of homosexual behavior may reflect multiple motivations, different developmental pathways, and divergent evolutionary histories, which require different explanatory frameworks (Vasey & Sommer, 2006). To further assess the nature of male–male mounting in this all-male group of Japanese macaques, future observations should be conducted both during and outside the mating season. We conclude that the behaviors reported here were homosexual behaviors, based on the ten pieces of evidence previously mentioned. At present, there is no evidence that this homosexual behavior reflects homosexual orientation. Rather, it likely reflects Japanese macaque males’ potential for bisexual behavior, which exists in several other Old World monkeys and in great apes (Dixson, 2012). The expression of male homosexual behavior might be favored by the particular sociodemographic setting under study here, namely the occurrence of an all-male group. More research on male homosexual behavior in non-human primates is needed, particularly in all-male groups. When considering how our results may apply to the evolution of human sexuality, one should keep in mind that although reproductive behaviors in humans and Japanese macaques likely share homologous features, non-conceptive sexual behaviors in these two species may be analogous. Exclusive same-sex sexual orientation has not been documented in any free-ranging nonhuman primate species, including Japanese macaques. As such, the study of homosexual behavior in non-human primates may inform us about the evolution of homosexual behavior in humans, but may shed only limited light as to why exclusive male homosexuality evolved. Acknowledgments This study was funded by the following agen cies: Natural Sciences and Engineering Research Council of Canada (NSERC), Alberta Innovates Health Solutions (AIHS), Japan Society for the Promotion of Science (JSPS), American Institute of Bisexuality (AIB), the L.S.B. Leakey Foundation, as well as the Office of the Dean of Arts and Science and the Office of Research Services at the University of Lethbridge. We thank Lydia Ottenheimer Carrier for assistance with data collection. We thank Penny D’Agnone for help securing AIHS funding. We thank Y. Iwanaga for permission to work at Meiji Memorial Forest Minoo Park and S. Suzuki for valuable information in the field. We thank the Editor, Alan Dixson, and one anonymous reviewer for fruitful comments on a previous version of the article.
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