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.     

Courtship behaviour in Japanese macaques during heterosexual and homosexual consortships

Female Japanese macaques (Macaca fuscata) in the Arashiyama population near Kyoto, Japan, are unusual, in that they exhibit what many would consider to be male-typical sexual characteristics. Specifically, they mount other females within the context of temporary, but exclusive, sexual relationships (i.e., homosexual consortships) and they sometimes exhibit a preference for female sexual partners, even when given the choice of a sexually motivated male alternative. In this study, we examined whether female Japanese macaques also exhibited male-typical patterns of courtship behaviour during homosexual consortships. Data were collected on courtship behaviour during heterosexual and homosexual consortships in free-ranging Japanese macaques from the Arashiyama (Japan) population. We analyzed the occurrence of 12 different courtship behaviours during 3374 heterosexual inter-mount intervals and 1412 homosexual inter-mount intervals. Sex differences between heterosexually consorting males and females existed for only two of the 12 courtship behaviours we investigated: inclined-back presentations and sexual vocalizations. Dominant and subordinate homosexually consorting females were sex-typical in their expression of inclined-back presentations and sexual vocalizations. Consequently, facultative same-sex sexual partner preference, mounting and consortships do not co-occur with male-typical patterns of courtship behaviour in female Japanese macaques.     

Ovarian cycle phase and same-sex mating behavior in Japanese macaque females

The relationship of the ovarian cycle phase to same-sex mounting activity in adult female Japanese macaques (Macaca fuscata) was studied during the 1997/1998 mating season. Fecal samples were collected from eight female subjects two to three times per week and analyzed by enzyme immunoassay for fecal hormone levels. Hormone profiles of estrone (E1) and pregnanediol (PdG) were used to separate ovarian cycles into three phases: follicular, periovulatory, and luteal. Patterns of same-sex and heterosexual mounting behavior in the females were analyzed for phase variation during conceptive cycles. Same-sex mounting among female Japanese macaques occurred most frequently during the follicular and periovulatory phases of the cycle, and not at all during the luteal phase, paralleling the pattern found in heterosexual mounting behavior. These findings suggest a link between hormonal fluctuations and patterns of sexual mounting, regardless of whether the partner is of the same or opposite sex.     

Homosexual behaviour and female-male mounting in mammals—a first survey

Information from the literature is given on the presence or absence of homosexual behaviour and female-male mounting in 125 species of mammals, both captive and wild. Such behaviour occurs in the male and often female young of many species soon after their birth. It is more common in young, often in play, than in adults. Adult homosexual behaviour is widespread in male and female mammals (recorded in 63 and 71 species respectively), but common in few species. In males it is most likely to be correlated with dominance and thus to occur in species with hierarchies such as terrestrial monkeys and members of the sheep and goat tribe. In females it is often correlated with sexual condition; a female in heat most often mounted another female, and one in heat was next most likely to be mounted by another female. Anoestral females rarely mounted other anoestral females. Females of 43 species mounted males, which often excited them sexually. Captive mammals tended to mount animals of the same sex more often than did wild ones when comparative data were available. Domestic animals also mounted more man did wild ones, with several exceptions. Some phylogenetic groups of animals displayed similar degrees of homosexual mounting, but there was often considerable variation between closely related species. Nor could homosexual mounting be always correlated with the social structure of a group. The four reasons for, or contexts of, homosexual and female-male mountings were social play (in 34 species), aggression (19 species), sexual excitement (36 species), and physical contact—non-play (30 species). This last category included a state of tension, getting attention, greeting, grooming, caressing, reassurance and appeasement. There was some overlap between categories. Homosexual pair-bonds occur in captive mammals and have been observed throughout the year in non-captive female Japanese monkeys.     

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.     

Sexual performance of twin ram lambs and the effect of number and sex of contemporary siblings

The objectives of this investigation were to determine the degree of correspondence in the sexual performance of twin male sheep and to compare the sexual performance of ram lambs born co-twin to another male (M-M), co-twin to a female (M-F) and as single (S) offspring. Individual ram lambs (N=117), including 13 M-M twin sets, were exposed to four estrous ewes for 30 min at 7-day intervals over a 4-week period at 8 to 9 months of age.Frequencies of ejaculation (serving capacity) and mounts without ejaculation were recorded. M-M males averaged 2.9 ejaculations and 13.1 mounts per test. Individuals within 9 of the 13 M-M twin sets (69%) differed by an average of 0.5 or fewer ejaculations per test. Although variability within M-M twin sets was very low, variability between the 13 M-M twin sets was also low (coefficient of variation=10.6%). Consequently, frequencies of both ejaculation and mounting (without ejaculation) within the 13 twin sets were not correlated (P=0.50 and P=0.10, respectively). When the progeny of individual sires were compared, mounting frequencies were correlated (P<0.02) but not ejaculation rates (P=0.72). M-M, M-F and S ram lambs did not differ for either ejaculation frequency (P=0.26) or mounts without ejaculation (P=0.98). It was concluded that the sexual performance of related individuals is likely to be very similar and that the number and sex of contemporary siblings does not necessarily influence rates of mounting and ejaculation.     

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.     

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.     

The relationship of male-male mounting to mate choice and sexual performance in male dairy goats

Rearing of male farm animals in unisexual groups has been implicated as a factor contributing to the failure of many males to breed as adults. The present study examines the relationship of male-male mounting in yearling dairy goats to subsequent mate preferences and sexual performance.Twenty-four sexually inexperienced male dairy goats, representing the Alpine, LaMancha, Saanen and Toggenburg breeds, were observed for male-male mounting in their home enclosure and then tested for mate choice and sexual performance when exposed to male and female (estrous and diestrous) stimulus animals. Their sexual behavior was compared with 7 adult goats with previous breeding experience.In the mate choice-sexual performance tests, 4 sexually inexperienced goats (17%) were sexually inactive, 6 (25%) mounted both male and female stimulus animals and 14 (58%) mounted only the female stimuli. Mate choice and sexual performance of the 20 sexually active males was not related to the number of male-male mounts initiated or the number of different males mounted in their home enclosure. However, the goats that received the greatest number of mounts in their home pen tended to be bisexual (would mount both male and female stimulus animals) in the mate choice tests. Males that were sexually inactive in mate choice-sexual performance tests repeatedly mounted the same male during home pen observations. Except for ejaculation frequency, the sexual performance of the sexually naive and experienced goats was similar. Goats of the Saanen breed were favored recipients of mounts from other males. There was no relationship between the number of male-male mounts performed and received.It was hypothesized that the reproductive failure of many male farm animals reared in all-male groups may be more closely related to the formation of specific sexual attachments to other males rather than the frequency with which they exhibit homosexual behaviors.     

Relationship between male-male and male-female sexual behavior in 5-6-month-old male lambs

To characterize male–male sexual behavior during lamb development, to relate it with lamb body and testicular growth, and with sexual behavior toward estrual ewes, 40 Milchschaf male lambs, weaned at 45 days of age, were kept with ewes that were nursing younger lambs. Experimental lambs were weighed and scrotal circumference was measured every 2 weeks. Male–male sexual behavior was observed during 1–2 h every 2 weeks after birth until 7 months of age. Observations were recorded more intensively (3–4 h on five different days) for 2 weeks (5–6 months of age) as male–male sexual behavior increased during that period. Both mounting and mounted lambs were identified. An individual mounting index (MI) was calculated. To study male–female sexual behavior, lambs were individually located with two estrual ewes, and during 5 min the number of ano-genital sniffing, lateral approaches, mounts, and mounts with ejaculation were recorded. From those data, a libido index was also calculated. Male–male mounts (n = 308) were observed. Courtship behavior was displayed in 25% of interactions; mounts were accepted in 72.1% of attempted mounts. Mounts without previous courtship were accepted more frequently than mounts with previous courtship (P = 0.002). Lamb weight and scrotal circumference were not different according to MI groups. Lambs that mounted more times estrual ewes (first tertile) had greater (P = 0.04) MI (0.61 ± 0.10) than lambs with medium (0.27 ± 0.09) and less (0.30 ± 0.10) MI. The regression between MI and heterosexual libido index was r = 0.33 (P < 0.05). In summary, intensive male–male sexual activity during a short period of male lamb development was observed. There was a positive relationship between sexual behavior of male lambs towards other male lambs and towards estrual ewes.     

Sociosexual behavior of captive sichuan golden monkeys (Rhinopithecus roxellana)

The Sichuan golden snub-nosed monkey, Rhinopithecus roxellana, is an endangered Colobine endemic to China. The social and reproductive behavior of this species are little known, and it has rarely been kept in captivity outside China. Results from observations of a captive golden monkey pair revealed some unusual details of sociosexual behavior. Both members of the pair mounted one other, and female mounting of the male occurred nearly as often as the reverse. Male mounts were always preceded by a stereotyped behavioral sequence that included distinct facial and vocal displays. Female mounts occurred in response to male solicitation (presenting). No evidence of ejaculation was observed in association with mounts, although mounts were only observed in a distinctly sexual context. Sexual behavior was associated with aggressive displays by one or both animals and with apparently proceptive behavior by the female. All sexual behaviors showed a peak near the end of the study, although the female was continually receptive throughout the 2-month study period.     

The Influence of Age,Sex, and Rank on Yawning Behavior in Two Species of Macaques (Macaca fascicularis and M. fuscata)

Yawning behavior was studied in two species of macaques: the long-tailed macaque (Macaca fascicularis) and the Japanese macaque (M. fuscata). Japanese macaques yawned much more than long-tailed macaques. Age, sex, and dominance rank exerted different effects on yawning in the two species. In the long-tailed macaques, sex differences in frequency of yawning emerged only after sexual maturity; yawning rates increased significantly in both males and females as they reached sexual maturity; and, among males, dominance rank was positively correlated with frequency of yawning. Differently, in the Japanese macaques, males, both mature and immature, yawned more than same-aged females; sexual maturity was associated with an increase in yawning in males only; and male rank did not correlate with the frequency of yawning. Regardless of interspecific differences, the overall results supported only in part the finding that, in Old World monkeys, yawning is largely influenced by plasma concentrations of androgens. There was evidence that social factors were also important in influencing the age-sex class distribution of yawning.     

Male Post‐Ejaculatory Mounting in the Ring‐Tailed Lemur (Lemur catta): A Behavior Solicited by Females?

Male mate guarding can take many forms but often involves aggression toward male conspecifics and continued proximity with a female. This study describes a previously undocumented behavior in a promiscuous primate, the ring‐tailed lemur: post‐ejaculatory (PE) mounting. PE mounting was documented across eight mating seasons in a ring‐tailed lemur colony on St. Catherines Island (SCI), USA. During PE mounting, a male remounts a female following ejaculation and clasps her midsection as if to mate again, but copulation does not occur; males showing this behavior typically lack erections, and their mounts show an absence of penile intromission and rhythmic thrusting. Male PE mounting was more common among males mating earlier in the queue, and when PE mounting occurred, it accompanied mate guarding. Four non‐mutually exclusive hypotheses to explain PE mounting were evaluated as follows: (1) gaining additional copulations, (2) prevention of re‐mating, (3) lengthening sperm residence time, and (4) re‐mounting as a function of female proceptivity. Male PE mounting did not aid males in gaining additional copulations nor did PE mounting prevent females from mating with new males. Equivocal support was found for Hypothesis 3: although there was much overlap in copulatory plug residence times for males who did and did not show PE mounting, one‐third of males who practiced PE mounting had plug residence times of 2 h or more, much longer than that of males who did not show PE mounting. PE mounting may therefore be related to increased plug residence time, which may provide an advantage to males in sperm competition. Strong evidence was found in support of Hypothesis 4: males overwhelmingly performed PE mounts in response to continued female sexual presentations, suggesting that females can solicit this male behavior. Females consequently exercise an even greater degree of control over males than was previously realized in this ‘female dominant’ primate.     

Female reproductive cycles and the sexual behavior of moor macaques (Macaca maurus) in their natural habitat,South Sulawesi,Indonesia

The female reproductive cycles and sexual behavior of moor macaques (Macaca maurus) were studied in their natural habitat. Female moor macaques showed repeated perineal swelling. The average cycle length was 36.2 days and the mean duration of swelling was 11.9 days. The estimated duration of gestation in two observed cases was 175 and 176 days, respectively. Females did not exhibit post-conception sexual swelling. Males appeared to ejaculate in multi-mounts. Serial mounting by the alpha male was concentrated on swelling females, while second- and third-ranking males sometimes mounted non-swelling females in series.     

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.     

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.     

Patterns of sexual behavior in male macaques

One large social group of each of three species of macaques (Macaca mulatta, M. fascicularis, M. radiata), housed in half-acre field cages at the California Primate Research Center, were observed for a total of 150 h. Data on sexual behavior and dominance interactions were recorded by pairs of experienced observers using a focal animal technique. Single or multiple mount-to-ejaculation sequences, number of thrusts per mount, number of mounts per sequence, duration of mounts per sequence, duration of sequences, social rank and frequency of sexual activity were recorded for each adult male. M. mulatta used a multiple mount-to-ejaculation (MME) pattern in 91% of their copulations. M. radiata used a single mount-to-ejaculation (SME) pattern in 91% of their copulations. M. fascicularis used both patterns—53% MME and 47% SME. A positive correlation was found between rank and sexual activity in fascicularis and mulatta males. A negative correlation between rank and sexual activity was found in radiata males and also a positive correlation between rank and age indicating that the youngest and most subordinate radiata males were the most sexually active males. In reviewing the literature, a relationship between degree of intermale competition, intermale tolerance and type of mounting pattern was revealed. Macaque species that primarily use an SME pattern also show sa high degree of intermale tolerance and little interrnale competition. Macaque species that primarily use an MME pattern typically show a high degree of intermale competition and a low degree of intermale tolerance. Possible events leading to such relationships are discussed.     

Sexual behavior of male New Zealand white rabbits in an intensive production unit

Sexual behavior in the male white New Zealand rabbit in intensive production units is not fully documented. Therefore, the objective of this work was to provide further information about the sexual behavior of this species in intensive production systems. Fourteen 6- to 12-month-old rabbits were studied for 6 months (July/December) when housed individually under natural photoperiod (19 degrees latitude north). They were mated once a week. When mated they were exposed at 6-min intervals to five oestrous females. The number of mounts, time between mounts, time and number of ejaculations, time between ejaculations, and also enuresis, grasping and kicking were recorded. Mounts (n=222) were observed and recorded. Males mated one to five times during each evaluative session. Enuresis was present only in one observation. Sexual aggressiveness such as grasping and kicking was present during 142 and 133 matings. Time for mounting and ejaculation in accumulated means (minutes, seconds, tenths) from the first to the fifth mount were noted and an accumulative average of 4.20 min for the fifth mounting was noted. Minimum times for ejaculation and next mating was 00:17:00 min and maximum was 05:33:03 min. It was concluded that sexual behavior in white New Zealand male rabbits remained unchanged through the duration of the period of study.     

Plasma cholesterol levels in free-ranging macaques compared with captive macaques and humans

Plasma total cholesterol in free-ranging Japanese macaques (Macaca fuscata) on Koshima islet and in free-ranging long-tailed macaques (Macaca fascicularis) at Pangandaran in Indonesia was found to occur at very low levels compared with captive macaques and humans. Although total cholesterol levels in captive macaques were lower than humans, differences in HDL cholesterol levels were only small. In both sexes of wild and captive Japanese macaques, total cholesterol levels decreased from birth through to young adulthood but then increased in adult females of the captive group. In contrast, the value for adult females of the wild troop remained at a low level. Low TCH levels in adult females of the wild Japanese macaque troop may be due to a low energy intake and may have caused a delay in the onset of sexual maturation. Plasma TCH levels increased with the addition of 0.1% dietary cholesterol over six weeks in captive long-tailed macaques. That the cholesterol value after six weeks was dependent on cholesterol levels prior to supplementation indicates that captive macaques are slightly saturated with cholesterol.     

Relationship between ovarian cycle phase and sexual behavior in female Japanese macaques (Macaca fuscata)

We conducted behavioral observations simultaneously with fecal sample collection on eight nonlactating females 2-3 times per week, October 1997-March 1998, to examine the relationship between ovarian hormones and the sexual behavior of female Japanese macaques (Macaca fuscata) during the mating season. We analyzed samples by enzyme immunoassay for fecal hormone levels. Hormone profiles of estrone-glucuronide (E1) and pregnanediol-glucuronide (PdG) were used to separate ovarian cycles into three phases (follicular, periovulatory, and luteal). Hormonal profiles indicate average cycle lengths of 27.6 +/- 4.2 days (+/- SD; n = 26). Average lengths of the luteal and follicular phases were 12.3 +/- 3.8 days (+/- SD) and 8.3 +/- 3.4 days (+/- SD), respectively. We observed female Japanese macaques engaging in sexual activity throughout the ovarian cycle, with the highest rates occurring during the follicular and periovulatory phases as compared to the luteal phase. The attractivity of female Japanese macaques increased significantly during the follicular and periovulatory phases of the ovarian cycle, when E1 levels are peaking and PdG levels drop to baseline. In addition, females displayed a significant increase in proceptive behavior during the follicular and periovulatory phases. Grooming bouts, as well as proximity between female and male macaques, also increased significantly during the follicular and periovulatory phases. We conclude that fluctuating levels of ovarian hormones in different phases of the cycle are significantly associated with variable rates of copulatory and pericopulatory behaviors in these Japanese macaque females.