Inter-Mount Social Interactions During Heterosexual and Homosexual Consortships in Japanese Macaques

In this study, we examined whether female Japanese macaques ( Macaca fuscata ) exhibited male-typical patterns of inter-mount social behaviour during homosexual consortships. Data were collected on heterosexual and homosexual consortships from a population of free-ranging Japanese macaques in Arashiyama, Japan. Inter-mount intervals were defined as the period between two consecutive mounts. A total of 3374 heterosexual inter-mount intervals and 1412 homosexual inter-mount intervals were analysed. We examined nine different categories of inter-mount behaviour. Sex differences between heterosexually consorting males and females existed for three of the inter-mount behaviours we examined (i.e. ventral-to-dorsal orientation, aggression directed toward third party individuals, tree-shaking displays). The subordinate female partners in homosexually consorting pairs exhibited some sex-atypical inter-mount behaviours. This sex-atypicality did not appear to reflect generalized developmental canalization in the direction of a male-typical suite of behaviours. Rather, the observed behavioural sex-atypicality could be best explained in terms of the unique alliance-related dynamics that characterized homosexual consortships in Japanese macaques.     

Sex differences in sexual partner acquisition, retention, and harassment during female homosexual consortships in Japanese macaques

Female Japanese macaques (Macaca fuscata) in certain populations are unusual in that they exhibit male-typical patterns of mounting behavior and sexual-partner preference. The goal of this study was to determine whether female Japanese macaques, from one such population, employ male-typical behavioral tactics to disrupt existing homosexual consortships, as well as to acquire and retain same-sex sexual partners. "Harassment" of homosexual consortships occurred when a sexually motivated, third-party male or female interrupted a consorting female couple by displacing or aggressing them. Sexual harassment was a male-typical strategy for disrupting existing homosexual consortships, but was rarely performed by females. "Intrusions" occurred when a male or female competitor attempted to acquire exclusive access to a female engaged in a homosexual consortship by targeting that female as the focus of competition and her partner as his/her competitor. "Sexual coercion" occurred when one individual alternately sexually solicited and aggressed another individual as part of the same behavioral sequence during an intrusion. Males employed consortship intrusions and sexual coercion when they attempted to acquire female sexual partners that were already engaged in homosexual consortships, but females rarely did so. However, females did employ male-typical patterns of aggressive competition and sexual coercion to retain same-sex sexual partners when confronted with male competitors' attempts to usurp those partners. These results indicate that female sexual activity during homosexual consortships is not uniformly "masculine" in expression, but rather is a mixture of male- and female-typical behaviors.     

Skewed sex ratios and female homosexual activity in Japanese macaques: An experimental analysis

In this paper we present the results of a behavioral experiment conducted to test whether homosexual consortships and sexual solicitations among female Japanese macaques (Macaca fuscata) increase in the context of operational sex ratios that are heavily skewed towards females. The study involved a baseline period of observation on an intact social group which had a female-biased sex ratio typical of this species. During the experimental period which followed, we created a sub-group with an operational sex ratio that was heavily skewed towards females. Compared to the baseline period, females solicited significantly more same-sex individuals for sex and formed significantly more homosexual consortships during the experimental period of the study. Females did not appear to engage in homosexual activity during the study's experimental period simply because they lacked heterosexual alternatives. Instead, we suggest that an abundance of certain types of preferred, same-sex sexual partners and/or a scarcity of opposite-sex sexual competitors best account for the increased levels of female homosexual behavior observed at this time.     

Behavioral patterns of estrous females of the Arashiyama West troop of Japanese macaques (Macaca fuscata)

This report contains detailed data on the sexual behavior of the 60 sexually mature females of the Arashiyama West troop of Japanese macaques. The study group was a natural troop transported intact in 1972 to a ranch in South Texas. Since transplantation, the monkeys have been free to roam and feed within a 42.2 ha enclosure. Analysis of data collected on the 140 monkeys that composed the troop during the 1973–74 and 1974–75 breeding seasons revealed: (1) Female-male mounting is an important aspect of Japanese macaque sexual behavior; (2) All females had preferred partners and most avoided both heterosexual and homosexual interactions with close kin; (3) Pubescent and adult females exhibit different patterns of sexual behavior; (4) Pubescent and adult females were affected somewhat differently by the transportation from Japan to their current home in South Texas. These behavioral patterns and their implications are discussed. The study was partially supported by PHS Biomedical Science Grant 50-262-1112.     

Sexual strategies of female Japanese macaques (Macaca fuscata)

Evidence is reviewed that female Japanese macaques have multiple male mating partners when they are available and show a preference for mating with sexually unfamiliar males. Several lines of evidence suggest that this aspect of female sexual behavior results in the offspring of an individual female being sired by more than one male thereby maintaining the genetic diversity of the troop. Evidence is presented in this paper that a decrease in the number of adult troop males and a lack of extra-troop migrant males in the Arashiyama West troop of Japanese macaques following transplantation to a ranch in south Texas had consequences for the sexual behavior of the females.     

Sexual Behaviour of Sumatran Long-tailed Macaques (Macaca fascicularis)

The sexual behaviour of wild long-tailed macaques (Macaca fascicularis) was studied in the Gunung Leuser National Park, Sumatra, Indonesia. All females showed some swelling of the sexual skin, but the frequency and maximum size of the swelling decreased with age. The frequency of copulations and consortships for a given female increased with increasing degree of swelling or coloration. No regular cycles could be found in the occurrence of swellings, copulations and consortships. Periods for which a female had consortships tended to be long (up to 5–6 weeks on end). These two results suggest that in the wild the predictability of the moment of ovulation is very low. The consortships were not exclusive: both the male and the female occasionally copulated with others. All females had many different male partners and, as ovulation signalling was not clear, none of these males could have any certainty about paternity of a female's offspring. Yet, the highest-ranking males probably had the best chances to father children because they were more often involved in sexual interaction (both copulations and consortships), especially around the estimated date of conception. This does not hold for the nulliparous females who were virtually ignored by the higher-ranking males. Consortships were occasionally actively maintained by the female, for whom a direct advantage of consorting might be an increased safety against conspecifics and predators. One advantage of mating with many different males might be a reduced risk of infanticide.     

Mounting Interactions between Female Japanese Macaques: Testing the Influence of Dominance and Aggression

The goal of the work reported here was to determine whether female Japanese macaques (Macaca fuscata) participated in same-sex mounting interactions during homosexual consortships to communicate about asymmetries in their dominance relationships and to reduce aggression. Focal data were collected during 21 homosexual consortships involving 14 females living in a captive, mixed-sex group of 37 individuals. We identified eight types of mounts, one solicitation used specifically to request to mount (hands-on-hindquarters solicitation), two solicitations used specifically to request to be mounted (hindquarter and back presentations), and one behavior employed to facilitate mounts-in-progress (clasping). We tested whether dominant consort partners (1) mounted more and (2) requested to mount more than their subordinate partners and whether subordinate consort partners (1) requested to be mounted more and (2) facilitated mounts-in-progress more than their dominant partners. Finally, we examined whether mounting was temporally linked to the onset of aggressive interactions between consort partners and whether it functioned to defuse incipient aggression. None of these predictions was supported. All types of mounts, mount solicitations, and clasping occurred bi-directionally within consort dyads. Mutual sexual attraction and gratification provided the proximate motivation for these mounting interactions and, in turn, for the formation and maintenance of their homosexual consortships.     

Female behavioral strategies during consortship in Tibetan macaques (Macaca thibetana)

Consortship has been defined as a temporary association between an adult male and an estrous/receptive female. It has been considered as male mating strategies to improve male mating success and potential reproductive success. However, the female roles have been more or less neglected, and thus, less is known about female behavioral strategies during the consortship periods. In this study, during the two consecutive mating seasons, we collected behavioral data of free‐ranging Tibetan macaques (Macaca thibetana) habituated in Mt. Huangshan, China, to investigate female behaviors when she was consorted by an adult male. The results showed that (a) females were more likely to approach and exhibit sexual solicitation to their consorting males during the consorted period, and females also exhibited less approach to their nonconsorting males; (b) females exhibited strong responses (either departed distantly or formed affiliative relationships with their consorting male partner) when their consorting males mated with rival females or showed sexual motivation toward rival females; (c) female preferences were positively correlated to the duration of consortships and the frequencies of ejaculation copulations, independent of the social ranks of their consorting male partners. Our results suggested that female strategies played much more important roles in forming and maintaining consortship than previously assumed. It provides new insight into understanding female adaptive strategies to male strategies by forming consortships in multimale–multifemale primate species when males could not identify female''s fertile phase accurately.     

Reproductive biology of rhesus and Japanese macaques

This paper offers a comparison of the reproductive biology of the Japanese macaques of Arashiyama, Japan and the free-ranging rhesus macaques of Silver Springs, Florida, U.S.A. The data indicate that rhesus macaques of Silver Springs have a higher reproductive rate than the Japanese macaques of Arashiyama. The reproducive rate of the rhesus monkeys over three birth seasons is 82% and that for the Japanese macaque is 53%. The higher reproductive rate of rhesus monkeys is accomplished through an earlier onset of sexual maturation (4 and 5 years for the rhesus and 5 and 6 years for the Japanese monkeys) and a shorter interbirth interval (14.27±5.54 months for rhesus and 18.00±6.57 months for Japanese monkeys). It is suggested that, because of the relatively harsh winters experienced by Japanese macaques, the slower reproductive rate of the Japanese monkeys has been selected for in order to enable females to lengthen the time in which maternal care is extended to their offspring.     

Altered pairing behaviour and reproductive success in white ibises exposed to environmentally relevant concentrations of methylmercury

Methylmercury (MeHg) is the most biologically available and toxic form of mercury, and can act as a powerful teratogen, neurotoxin and endocrine disruptor in vertebrates. However, mechanisms of endocrine impairment and net effects on demography of biota are poorly understood. Here, we report that experimental exposure of an aquatic bird over 3 years to environmentally relevant dietary MeHg concentrations (0.05-0.3 ppm wet weight) resulted in dose-related increases in male-male pairing behaviour (to 55% of males), and decreases in egg productivity (to 30%). Dosed males showed decreased rates of key courtship behaviours, and were approached less by courting females in comparison to control males. Within dosed groups, homosexual males showed a similar reduction when compared with dosed heterosexual males. We found an average 35 per cent decrease in fledgling production in high-dose birds over the study duration. These results are of interest because (i) MeHg exposure is experimentally tied to demographically important reproductive deficits, (ii) these effects were found at low, chronic exposure levels commonly experienced by wildlife, and (iii) effects on reproductive behaviour and sexual preference mediated by endocrine disruption represent a novel and probably under-reported mechanism by which contaminants may influence wild populations of birds.     

The effects of sex steroids and vasotocin on behavioral responses to visual and olfactory sexual stimuli in ovariectomized female roughskin newts

Previous studies have found that vasotocin (AVT) administration to male roughskin newts (Taricha granulosa) enhances courtship clasping as well as appetitive responses to specific sexual stimuli and that treating female newts with androgens plus AVT induces the expression of male-typical courtship clasping (the selective clasping of females). However, the unique and/or interactive effects of sex steroids and AVT on appetitive responses to specific sexual stimuli have not yet been determined. To first identify male-typical, sexually dimorphic appetitive responses to female sexual stimuli, we tested intact newts during the breeding season and found that males, but not females, are attracted to female visual and pheromonal sexual stimuli. We then used ovariectomized (ovx) females implanted with empty silastic capsules (Blk) or with capsules containing testosterone (T), dihydrotestosterone (DHT), or estradiol (E2) and then injected with either saline or AVT to determine the effects of steroids and AVT, alone or in combination with each other, on male-typical behavioral responses to those stimuli. E2 treatment depressed responses toward female visual stimuli independently of AVT. On the other hand, only T-implanted, AVT-injected females displayed male-typical behavioral responses toward female olfactory stimuli, preferring to spend more time in proximity to female-scented than unscented newt models and selectively clasping the female-scented models. Together, these results support the conclusion that sex steroids and AVT influence behavioral responses to sexual stimuli via sensory-specific mechanisms. Furthermore, they suggest that T and AVT interact within the brain to influence sensorimotor processing in the pathways that integrate olfactory sexual stimuli into male-typical courtship behaviors.     

Testing multiple hypotheses for the maintenance of male homosexual copulatory behaviour in flour beetles

Diverse animal groups exhibit homosexual interactions, yet the evolutionary maintenance of such behaviours remains enigmatic as they do not directly increase reproductive success by generating progeny. Here, we use Tribolium castaneum flour beetles, which exhibit frequent male homosexual copulations, to empirically test several hypotheses for the maintenance of such behaviours: (1) establishing social dominance; (2) practice for future heterosexual encounters; and (3) indirect sperm translocation. We found no evidence that Tribolium males use homosexual copulations either to establish dominance or to practice behaviours that increase their subsequent heterosexual reproductive performance. Our results provide limited support for the hypothesis of indirect sperm translocation: when males from two genetic strains mated with females immediately following a homosexual copulation, females produced progeny sired not only by the directly mating male, but also by that male’s homosexual partner. However, this phenomenon was detected in only 7% of homosexual pairs, and in each case such indirectly sired progeny accounted for < 0.5% of females’ total progeny. Direct observations indicated that mounting males often released spermatophores during homosexual copulations. These observations suggest that homosexual copulations may be a behavioural mechanism that allows males to expel older, potentially low‐quality sperm. Additional work is needed to test this new hypothesis, and to determine whether sperm release during homosexual copulations occurs in other groups.     

Psycholinguistic analyses of alarm calls of Japanese monkeys (Macaca fuscata fuscata)

Alarm and estrous calls emitted by Japanese macaques were recorded and analyzed in the Arashiyama West and East groups. Their responses to natural calls as well as to synthesized versions varying in the acoustic parameters that defined the vocalizations were studied. The response patterns shown by Arashiyama West group members, which were subject to a distinct change with only a slight difference of a single parameter, appeared to reflect strict underlying perceptual boundaries. This was analogous to the categorical perception that humans show with speech sounds. In contrast, continuous perception was exhibited by Arashiyama East group individuals. When several sounds were played back in combination to the former group, following stimuli were recognized by quite different cues from those by which the first sound was perceived. The groups' differences in vocal perception are discussed in terms of the ecological differences of the environments they inhabit.     

Homosexual incest avoidance among females in captive Japanese macaques

This paper reports a systematic pattern of homosexual incest avoidance among females in a captive group of Japanese macaques (Macaca fuscata) culled from the Arashiyama-West troop known for its high rates of female homosexuality. The study group included three matrilines and two generations. Between eight and 11 females were sexually active over four consecutive mating seasons, and all engaged in both heterosexual and homosexual activity. While all females performed homosexual acts with almost all possible non-kin partners, they systematically avoided homosexual interactions with their mother, daughters, and sisters. This pattern could not be explained either in terms of kin not being simultaneously in estrus, kin avoiding affiliative interactions in general, or non-kin utilizing the tension-reducing effect of estrus to affiliate exclusively with each other. In contrast to homosexual females, heterosexual pairs of relatives (brother-sister, mother-son) were sometimes incestuous. Assuming that female homosexuality expresses the reproductive strategy of females unconstrained by male influence, the present results point to the strong tendency of females to avoid incest and suggest that males are primarily responsible for the reported exceptions to incest avoidance.     

Materteral and Avuncular Tendencies in Samoa

Androphilia refers to sexual attraction and arousal to adult males, whereas gynephilia refers to sexual attraction and arousal to adult females. In Independent Samoa, androphilic males, most of whom are effeminate or transgendered, are referred to as fa’afafine, which means “in the manner of a woman.” Previous research has established that fa’afafine report significantly higher avuncular tendencies relative to gynephilic men. We hypothesized that Samoan fa’afafine might adopt feminine gender role orientations with respect to childcare activity. If so, then the fa’afafine’s femininity might be a proximate mechanism for promoting their elevated avuncular tendencies. Our analyses indicated that fa’afafine had significantly higher willingness to assist in the childcare of nieces and nephews than childless women, mothers, or men, none of whom differed from each other on this measure. Thus, femininity does not appear to explain the fa’afafine’s pattern of avuncular tendencies, nor the women’s pattern of materteral (i.e., aunt-like) tendencies, relative to gynephilic men. We discuss how the fa’afafine “third” gender status might influence the expression of their elevated avuncular tendencies.

Shape of,and body direction in,huddles of Japanese macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>) in Arashiyama,Japan

We studied huddles of Japanese macaques (Macaca fuscata) in the Arashiyama E troop at the “Arashiyama Monkey Park, Iwatayama” of Kyoto, central Japan. The macaques made physical contact with other individuals and formed huddles when the air was cold. The 99–101 adult females and 26–36 adult males in the study troop formed 345 huddles during 42 scan samples in the winter of 2001 and 376 huddles during 52 scan samples in the winter of 2002. The average size of huddles was 2.3 (range 2–7) individuals. Males huddled less frequently than females. Maternal kin-related dyads formed 2-female huddles more frequently than unrelated dyads. Choice of huddling partners might restrict the size of huddles. The most frequently observed 3 and 4-member huddles were triangular and diamond-shaped. Macaques usually huddled ventro–ventrally, ventro–laterally, and ventro–dorsally. A third individual frequently placed the ventral part of its body against the first individual and simultaneously put the lateral part of its body against the second individual, so that the 3 individuals formed a triangular huddle. This behaviour indicates that Japanese macaques choose their position and body direction in the huddle to reduce the area of body surface exposed to the air, thereby conserving body heat.     

Endocrine aspects of female-female pairing in the Western gull (Larus occidentalis wymani)

Investigations of the colonies of western gulls on Santa Barbara Island, California, have revealed a surplus of females and the occurrence of female-female pairs that produce clutches with as many as six eggs. Females are able to establish and defend breeding territories, behaviours generally thought to be under the control of androgens. There are very few significant differences in circulating levels of the luteinizing hormone and androgens among breeding males, breeding females in heterosexual pairs, and breeding females in homosexual pairs. In contrast, however, only females sampled in 1877, in both homo- and heterosexual pairs, have elevated plasma levels of oestrogens, in spring, coincident with the period in which they show courtship behaviours such as food begging and solicitation of copulation. Given a sex ratio skewed in favour of females, as is apparently the case with the colonies of this species on Santa Barbara Island, and the essentially equal plasma levels of androgens in males and females, it is not difficult to rationalize the formation of female-female pairs. Our findings do not support the hypothesis that female-female pairing involves hormonal masculinization of one member of the pair.     

Social relationships between adult male and female rhesus macaques: 1. Sexual consortships

The sexual relationships of 15 adult male rhesus macaques (Macaca mulatta), of one social group in the Cayo Santiago colony, Puerto Rico, were studied during the 1981 mating season. Two criteria were used to determine whether or not a focal male was in consort in a given 20-min observational sample. One hundred and thirty-two consortships were recorded. The distribution and duration of all consortships, and the distribution of those consortships that coincided with the estimated time of conception, were positively correlated with male dominance rank and length of tenure. Correlations with dominance were stronger than those with tenure. Older females had more consortships with focal males than younger females. There was no relationship between female rank and the distribution of consortships. Consortships did not give exclusive access to receptive females although they may do in feral situations. Males were primarily responsible for maintaining proximity in about two thirds of consortships. The four top-ranking males were primarily responsible in all but one of their consortships. Almost all of those in which the female was primarily responsible involved younger, slightly lower-ranking males. This pattern may have resulted from the females being attracted to the latter males although other interpretations are possible. The partner who was primarily responsible for maintaining proximity also tended to be the predominant groomer, supporting the view that grooming plays a role in the maintenance of sexual consortships. Almost a third of consortships were with females who had conceived, suggesting that males could not accurately assess female reproductive state. Consortships maintained by the male were longer than those maintained by the female. Males may try to increase their chances of fertilising a female by prolonging the consortship. High-ranking males may have been more successful at this, resulting in the positive correlation between male dominance rank and consortship duration.     

Differential effects of kinship,dominance, and the mating season on female allogrooming in a captive group ofMacaca fuscata

An analysis of allogrooming (total times spent grooming individual partners) of 8 sexually mature females (3–12 years of age) in a captive group of 17 Japanese macaques, shows that during the nonmating season, grooming distributions were characterized by high proportions of grooming given to family members and/or higher ranking nonkin. During the mating season, all eight females showed significant shifts in their grooming distributions, and four females showed significant shifts in grooming between their nonestrous and estrous periods (defined behaviorally). Fox six of eight females, mating season grooming was characterized by either high proportions of grooming given to family members and/or heterosexual and homosexual partners. It was found that within dyadic sexual relationships, dominants gave more grooming to subordinates than the former received, in contrast to a reversal of this pattern in the majority of these same dyads during the nonmating season. This is interpreted as one short-term function of grooming: a dominant asymmetrically grooms a subordinate sexual partner to maintain proximity with (or reduce tension in) the latter. The two remaining focal females (middle ranking, nulliparous) differed from the other females in that they shifted their mating season grooming to subordinate nonkin, despite the lack of evidence that this was a result of sexual interactions, patterns of partner availability, competition, patterns of grooming reciprocity, or agonistic alliance support. From these results, it is suggested that in some contexts, grooming of subordinate nonkin may function to reduce tension in thegroomer. In the Japanese macaque, this latter possibility and the asymmetric grooming of subordinate homosexual partners may prove to be exceptions to the general rule that female cercopithecine grooming of nonkin flows up the dominance hierarchy.     

Agonistic Behaviour and Sexual Conflict in Atypical Reproductive Groups: The Case of Bearded Vulture Gypaetus barbatus Polyandrous Trios

Social behaviour in species forced to form atypical breeding coalitions is poorly documented. The saturation of optimum territories in the Bearded vulture Gypaetus barbatus population in the Pyrenees has led floating males to settle in already occupied territories, thereby forming polyandrous trios. We examined the patterns of intrasexual aggression in five trios (nine reproductive events in total) during courtship. Alpha males initiated 82% of agonistic encounters that were mainly aimed at preventing or disrupting copulations. During the fertile period in recently formed groups, intrasexual aggression had a negative influence on the frequency of heterosexual copulations, which may be a contributing factor to the lower productivity of polyandrous trios. Females rejected a higher proportion of beta male- than alpha male-initiated copulations, and rejected copulations with both alpha and beta males more often when the other male was present close by. These results indicate that alpha males cannot effectively prevent all copulation attempts by beta males and that females avoid harassment by minimizing sexual activity when both males are present. Aggression between males decreased with time, occurring less often in established than in recent trios, despite the fact that the frequency of heterosexual copulations – the cause of conflicts – was similar. The frequency of homosexual interactions tended to increase in established trios, suggesting that this behaviour may help to regulate aggression within these groups, although no significant relationship between homosexual interactions and aggression was found. In summary, reproductive conflicts in trios seem to be unavoidable, although they tend to decrease if the group is maintained. This suggests that, for birds in these groups, the maintenance of a quality territory is more important than solving sexual conflicts.