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.     

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.     

Parity-related differences in suckling behavior and nipple preference among free-ranging Japanese macaques

Suckling behavior of primiparae in free-ranging Japanese macaques (Macaca fuscata) was compared with that of multiparae at Jigokudani Monkey Park, the Shiga Heights, Nagano Prefecture, Japan, from April 1984 to June 1994. The estimated rates of milk secretion in a single preferred nipple among primiparae were lower than those among multiparae from birth to 5 months of age. Milk secretion capabilities of primiparous mothers, hence, appear to be inferior to those of multiparous mothers. In nutritive sucking, although Japanese macaque infants preferred one single nipple, nipple preferences in primiparae were weaker than those in multiparae. With supplementary two-nipple use during sucking, however, the infants of primiparae appear to overcome a suckling flaw of their primiparous mothers. After infants were 5 months of age and after a drop (from approximately 10% to approximately 5%) in the rates of milk secretion, however, milk secretion rates in a single preferred nipple among primiparae were similar to those in multiparae and the supplementary two-nipple use in primiparous mother-infant dyads disappeared. Am. J. Primatol. 42:331–339, 1997. © 1997 Wiley-Liss, Inc.     

The development of behavioural sex differences in infant rhesus macaques (Macaca mulatta)

Studies of infant rhesus macaques have generally reported sex differences in the frequency of expression of some behaviour patterns, such as rough-and-tumble play and socio-sexual mounting. In contrast, sex differences in other behaviour patterns, such as proximity to the mother, have been less consistantly reported. Using data on the behavioural development of infant rhesus macaques living in captive social groups, we have attempted to provide further evidence for, or against, sex differences in behaviour and to investigate the possible influence of maternal rank and parity on sex differences in infant behaviour and mother-infant interactions. The behaviour of 14 male and 20 female infants and their mothers was studied during the first six months of life, including measures of play behaviour socio-sexual mounting, and mother-infant interactions. Our data reveal that, on average, male infants exhibited more rough-and-tumble play and mounting than female infants, and also exhibited stationary play, chasing play, and initiated play more frequently than females. Such sex differences appear to be robust in macaques and have been reported in a variety of housing conditions. male and female infants did not differ in the amount of time spent at particular distances from their mothers, and mothers were not found to behave differently towards sons and daughters, using measures of restraint, rejection, and grooming. These results are in contrast to previous studies on singly-housed mother-infant pairs but similar to those on free-ranging populations. Mothers did behave differently towards their infants depending upon the mother's rank and previous number of offspring. These maternal characteristics may have significant consequences for the behavioural development of both male and female infant primates.     

Population genetical study of Japanese macaques,Macaca fuscata,in the shimokita A1 troop,with special reference to genetic variability and relationships to Japanese macaques in other troops

The genetic variations of 35 individuals of the Shimokita A1 troop of mainland Japanese macaques,Macaca fuscata fuscata, which live at the northern end of the habitat of the species, were investigated using 33 electrophoretically detectable blood protein loci. Among the loci examined, six were polymorphic. The average heterozygosity per individual was calculated as 0.0442. This was the highest value among all troops of Japanese macaques so far investigated. The mainland macaques of the Shimokita A1 troop were more differentiated genetically from other mainland macaque troops than were Yaku macaques, the subspeciesM. f. yakui.     

Female-male mounting in Japanese macaques: the proximate role of sexual reward

Female Japanese macaques (Macaca fuscata), in certain populations, routinely engage in female-male mounting. In this study, we documented patterns of vulvar, perineal and anal (VPA) stimulation during female-male mounting in Japanese macaques. During approximately 45% of the female-male mounts analyzed, two thirds of female mounters engaged in VPA stimulation. Given the VPA region's primary role in mediating sexual response, the results of this research provide direct evidence bearing on the sexual nature of a substantial proportion of female-male mounts in Japanese macaques.     

Dominance competition through affiliation and support in Japanese macaques: An experimental study

It has been proposed that monkeys direct grooming to high-ranking individuals in an attempt to obtain agonistic support in return. But whether these two categories of interactions are causally related has proven difficult to establish. Part of the problem stems from the fact that in stable groups social relationships reflect an equilibrium state and that behaviors need only be performed at low rates and long intervals to maintain the current social structure. In theory, however, if affiliative and supportive interactions are indeed causally related, it should be possible to accentuate their temporal relation, hence their causal dynamics. For example, destabilizing dominance relations can be expected to induce competition for status and force individuals to deploy behavioral tactics for settling new rank relations. We experimentally induced rank reversals in a captive group of Japanese macaques (Macaca fuscata) composed of three matrilines (A-B-C rank order). A reversed C-A-B order composed of three individuals per matriline was maintained for 2 weeks. The results show the close temporal relation among (i) asserting one’s rank, (ii) competing for access to dominants through affiliation and interferences in affiliation, (iii) receiving support from dominants against lower-ranking individuals, and (iv) supporting dominants against subordinates. These findings are compatible with one version of the affiliation-for-support hypothesis, namely that monkeys affiliate with dominants as a way to assert their position in the hierarchy. In a functional perspective, mutual selfishness provides a better explanation than reciprocal altruism because the possibility that both groomers and supporters derive immediate net benefits cannot be excluded.     

A Juvenile Hormone analogue enhances homosexual behaviour in female‐deprived males of the migratory locust

In laboratory colonies of crowded migratory locusts Locusta migratoria (L.), homosexual behaviour (i.e. males mounting other males) is commonly observed. Female‐deprived males of Locusta migratoria migratorioides R. & F. mount each other in a characteristic mating position, often forming a group of several insects. When allatectomized males are placed together with intact, female‐deprived males, the former are usually mounted by the latter, demonstrating some degree of control involving the corpora allata over homosexual behaviour. This may be related to the positive effects of Juvenile Hormone (JH) or Juvenile Hormone analogues (JHAs) in enhancing male sexual behaviour, as is shown in some other insects. In the present study, a potent JHA (i.e. pyriproxyfen) is injected into a group of young, crowded L. m. migratorioides males, and an equivalent group of control males is maintained in a separate cage. Both groups are deprived of females. Three times a week, during 2‐h observation periods, JHA‐injected and control males are placed together in the absence of females, and homosexual mountings, per group and per individual, are recorded every 10 min. Observations are performed for 10 weeks. Analysis of these data, including the time spent in mounting behaviour, the percentage of individuals within a group involved in the behaviour during the observation periods and the identity of both partners, reveals that the JHA‐treated males show a more intense homosexual mating behaviour than control males in all quantified parameters. This is the first report of the enhancement of homosexual behaviour by an endocrine factor in insects.     

Development of intervention behavior in Japanese macaques: Testing the targeting hypothesis

Matrilineal dominance systems, which characterize several species of cercopithecines, are determined largely by the patterning of third-party aggressive interventions in conflicts. Although the role of interventions in structuring rank relations has received much attention, very few studies have dealt specifically with the development of intervention behavior. In other words,most studies have focused on the interventions received and their effect on the recipients rather than on the interventions performed and the goals of the interveners. We analyzed the intervention behavior of 10 juvenile females in a colony of 40 Japanese macaques (Macaca fuscata)housed at the University of Montreal Laboratory of Behavioral Primatology. The analysis of 749 interventions performed by the juveniles over their first 4 years and 2425 interventions received over the same period reveals that (1) juvenile females intervened selectively against females ranking below their mother, (2) they began to intervene at about the same time that they began to challenge the latter females in dyadic contests, (3) they sided with females as well as with males against these females, (4) juvenile interveners incurred little risks in terms of aggressive retaliation from their targets, (5) they derived immediate benefits in terms of conflicts won over stronger targets, (6) interventions often did not take place when the possible recipients needed support, and (7) interveners did not conform to a pattern of mutually preferential support. These results support the view that interventions by juveniles are selfish (vs altruistic) and constitute a low-cost and effective means to target and to outrank prospectively subordinate females.     

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.     

Toughness and fiber content of major leaf foods of Japanese macaques (Macaca fuscata yakui) in Yakushima

During the spring, Japanese macaques in Yakushima feed predominantly on mature leaves of trees, vines, and ferns. They are selective in which parts of leaves they eat, and this study examines potential cues and consequences of typical patterns of selection. Toughness and fiber content (NDF) were assessed for 13 of the major leaf-food species from samples collected in the spring of 1994. The toughness of the petiole, the midrib, and two parts of the lamina were tested separately. Petioles were generally the toughest part of the leaf, followed by the midribs. For both midrib and lamina, there was a positive correlation between toughness and fiber content, but the toughness of midribs was at least three times that of laminae at similar fiber contents. A clear relationship was found between the toughness of plant parts and whether or not they were eaten: no plant parts with a toughness greater than 2,300 J m⁻² were consumed even at low fiber levels. Toughness therefore explained food selection patterns much better than did fiber content. Toughness is likely to be assessed at the front of the mouth or during mastication. However, the macaques rarely reject leaves after placing them in the mouth. We suggest, therefore, that toughness may be used to select between feeding sites, rather than between individual leaves. © 1996 Wiley-Liss, Inc.     

Home range structure and inter-group competition for land of Japanese macaques in evergreen and deciduous forests

The per capita home range area of Japanese macaques,Macaca fuscata, is significantly smaller in evergreen forest than in deciduous forest, though a corresponding difference in food resource utilization patterns has never been described. The present study compared the home range utilization pattern of Japanese macaques living in two habitats: the Yakushima population inhabits an evergreen forest, while the Kinkazan population inhabits a deciduous forest. We found that in the Yakushima population, (1) food density was higher; (2) inter-feeding bout sites distance was shorter; (3) daily travel distance was shorter; (4) home range size was smaller; and (5) the unit value of the main home range was higher, than in the Kinkazan population. Yakushima groups utilized a small home range area intensively, compared to Kinkazan groups. We also found that a Yakushima group shared 24% of its main home range with neighboring groups, though a Kinkazan group shared only 10% with other groups. It is supposed that food distribution affects daily ranging pattern, and ultimately the social relationships between groups in Japanese macaques.     

Automatically detecting and tracking free‐ranging Japanese macaques in video recordings with deep learning and particle filters

Recently, automated observation systems for animals using artificial intelligence have been proposed. In the wild, animals are difficult to detect and track automatically because of lamination and occlusions. Our study proposes a new approach to automatically detect and track wild Japanese macaques (Macaca fuscata) using deep learning and a particle filter algorithm. Macaque likelihood is derived through deep learning and used as an observation model in a particle filter to predict the macaques’ position and size in an image. By using deep learning as an observation model, it is possible to simplify the observation model and improve the accuracy of the classifier. We investigated whether the algorithm could find body regions of macaques in video recordings of free‐ranging groups at Katsuyama, Japan to evaluate our model. Experimental results showed that our method with deep learning as an observation model had higher tracking accuracy than a method that uses a support vector machine. More generally, our study will help researchers to develop automatic observation systems for animals in the wild.     

Demography and reproductive parameters of a free-ranging group of Japanese macaques (Macaca fuscata) at Katsuyama

Demographic and reproductive data were analyzed for a period of 28 years in the females of a free-ranging group of Japanese macaques at Katsuyama, Okayama Prefecture, Japan. The overall mean, age-specific fecundity rates were 5.43% for 4-year-olds and 41.86% for 5-year-olds, increasing to a peak of 66.67% for 13-year-olds. Fecundity remained relatively high (52.31–54.24%) in 16–19-year-olds, but decreased sharply (45.45–17.86%) in 20–23-year-olds, and became very low in 24–26-year-olds. Females aged 27 years or more did not produce infants. The average age at first birth was 5.41 years. Births peaked in mid-May. The timing of the first births each year remained essentially unchanged during the study period, whereas the timing of the median and last births shifted towards the later part of the season. The mean interbirth interval for all females was 1.56 years. The value was 1.54 years for multiparous females and 1.29 years for females following infant loss. These intervals were significantly shorter than those for primiparous females, and females with surviving infants. The overall mean infant mortality within the first year of life was 10.2%. The value was 8.6% for 10–14-year-olds, and 7.5% for 15–19-year-olds. The timing of birth differed among the four female matrilineal dominance rank-classes. The female fecundity rates increased as a function of matrilineal dominance rank. It is suggested that all demographic and reproductive data should be analyzed in detail with respect to the group's history.     

Auditory behavioral thresholds for Japanese macaques using insert earphones

The goal of this study was to measure behavioral auditory thresholds in four Japanese macaques. Animals were trained using food as a reward in an operant reinforcement paradigm. Stimuli were 1-s sinusoids with 10-ms rise/fall times delivered through insert earphones (Etymotic ER-1) having expandable foam eartips. The animals generally produced threshold contours similar in shape to those reported for other macaques species, except that the low-frequency thresholds may have been slightly higher in the present studies. At middle and high frequencies, thresholds fell at the lower extreme of the range previously reported in other macaque species. The possible difference in low-frequency thresholds may have been a result of either transducer and calibration differences between studies or true species variations, or both. Though somewhat limited at high frequencies, the insert earphones used in these studies offer more reliable calibrations, less susceptibility to changes in positioning with movement of the animal, and greater interaural attenuation. Am. J. Primatol. 41:323–329, 1997. © 1997 Wiley-Liss, Inc.     

果蝇求偶行为分子调控机制的研究进展

果蝇(Drosophila)的求偶行为受多个基因调控,例如fruitless(fru)、dissatisfaction(dsf)和retained(retn)等。它们通过不同的剪切方式产生特异性产物,利用这些产物来控制雌雄果蝇的求偶行为,它们的剪切方式是雌雄果蝇求偶行为和性别决定所必需的。主要阐述了这些基因在果蝇求偶行为方面的分子调控机制,为进一步研究果蝇的求偶行为和性别决定提供理论依据。     

Birth-season variation in Japanese macaques,<Emphasis Type="Italic"> Macaca fuscata</Emphasis>

Japanese macaques, Macaca fuscata, exhibit an annual reproductive cycle that apparently is maintained intrinsically. Translocation of nine troops to new latitudes within the northern hemisphere has had minimal effect on the timing of birth seasonality in these troops; translocation of one troop to the southern hemisphere has resulted in a 6-month forward displacement of birth seasonality in this troop. Limited available evidence indicates that, in the latitudinal zone between Toimisaki (31°22′N) and Kinkazan (38°17′N), mean birth date in in-situ troops becomes earlier as latitude of troop localities increases; the same relationship between mean birth date and latitude apparently does not apply to in-situ troops south and north of the Toimisaki–Kinkazan latitudinal zone. Within the Toimisaki–Kinkazan latitudinal zone, earlier mean birth dates at higher latitudes may permit infants to achieve an adequate level of development before the earlier onset of poor winter food conditions. South of the Toimisaki–Kinkazan latitudinal zone, winters are relatively mild and may be less of a factor in infant survival; north of this zone, poor winter food conditions persist so long that earlier infant births may be maladaptive. Electronic Publication     

Non-offspring nursing by a nulliparous pregnant female just before first parturition in free-ranging Japanese macaques

A nulliparous pregnant Japanese macaque, Macaca fuscata, suckled her 1-year-old sister 44 days before her own parturition. Other Japanese macaque yearlings did not hold the nipples of this nulliparous female in their mouths. Although this non-offspring nursing before first parturition did not improve the rate of milk secretion, the nulliparous female may have improved her indirect fitness and her suckling behavior.     

Changes in testicular and nipple volume related to age and seasonality in Japanese macaques (Macaca fuscata), especially in the pre- and post-pubertal periods

We investigated, longitudinally and cross-sectionally, age and seasonal change in both the testis and nipple volume of Japanese macaques (Macaca fuscata) in relation to concentration profiles of gonadal steroids: testosterone (T) in males and progesterone (P) in females. Testicular volume (TV) and nipple volume (NV) showed rapid growth at puberty, 4.5 and 3.5 years of age in males and females, respectively, but in both sexes there were precocious individuals. The testis as a whole matures at about 10 years of age. TV change is closely related to T concentration profile. The pattern of TV change is composed of maturation and seasonal effects, with individual variation evident mainly in the latter. Some individuals show a simple pattern consisting of one peak in the breeding season (from summer to winter) and one trough in the non-breeding season. Other individuals exhibit a more complicated pattern composed of two or more peaks and troughs before and during the breeding season. The nipple matures at about 7 years but it is difficult to determine the exact maturational age as there are many confounding factors relating to NV. NV shows seasonal fluctuations similar to that of TV. Many animals have periods of substantial growth whereas others do not. The NV in adults from 10 to 25 years does not appear to change much with age, but animals older than 25 years of age have significantly smaller nipples. Seasonal fluctuation in NV mirrors that of the P level. Considered to be controlled by estrogen and P, the NV is a good indicator of the physiological status of reproduction, with its peak about 2 weeks earlier than that of P, that is, at the mid-follicular phase. NV and P level show a similar pattern in pregnancy; from conception, indicated by a P peak, NV and P concentration first decrease, then they increase until peri-parturition and slowly decrease again until the next breeding season.This revised version was published online in April 2005 with corrections to the cover date of the issue.