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.     

Fecal testosterone immunoreactivity as a non-invasive index of functional testosterone dynamics in male Japanese macaques (Macaca fuscata)

Validation of a simple method for the extraction and quantification of testosterone (T) from the excreta of male Japanese macaques (Macaca fuscata) is presented. Radioimmunoassay of paired fecal and serum samples collected from four intact sexually mature males during the breeding season provided profiles that were significantly correlated when samples were offset by approximately 48 hr. Additionally, no significant differences were observed in the pattern of temporal variation of T levels in serum and feces. Two castrated males were injected with radioinert T, and the patterns of excretion were observed by analysis of serial fecal and urine samples. Approximately 48 hr after the steroid was administered, a significant peak in the average fecal T levels was apparent. The injection event was also registered in the urine of both males, although qualitative differences were observed. These data suggest that measures of fecal T provide a reliable and non-invasive means of assessing gonadal function in this species. As the analysis of hormone levels in feces allows for frequent, stress-free sampling with minimal disruption, this method should be preferred in long-term orin situ applications requiring endocrine monitoring.     

Environmental temperature and reproductive seasonality in Japanese macaques (Macaca fuscata)

This study demonstrates that the reproductive seasonality ofMacaca fuscata seems to be more affected by environmental temperature than by photoperiod. Mean conception dates for 25 groups of Japanese macaques species did not correlate with latitude. Instead, they were positively related to mean fall and winter temperatures and negatively related to the magnitude of the decrease in the mean temperature from summer to fall. Evidence from transplanted groups supports the hypothesis that environmental temperature is a decisive factor in determining the timing of mating activities of Japanese macaques. These results are also consistent with the concept that, in temperate zones, environmental temperature is probably the best indicator of local climatic characteristics.     

Relationship between sexual interactions and the timing of the fertile phase in captive female Japanese macaques (Macaca fuscata)

Japanese macaques live in multi‐male/multi‐female social groups in which competition between males, female mate choice, and alternative male mating strategies are important determinants of mating and reproductive success. However, the extent to which adult males rely on female behavior to make their mating decisions as well as the effect of social rank on mating success are not clear as results are inconclusive, varying from study to study. In this study, we combined behavioral and endocrine data of 14 female Japanese macaques to examine the relationship between ovarian cycle phase and frequency of sexual behaviors, and to investigate how social rank influences sexual behavior in this species. We found that there was no increase in female proceptive behaviors during the fertile phase of the ovarian cycle, suggesting that female behaviors did not clearly signal the probability of conception. In spite of that, the frequencies of ejaculatory copulations were highest during this phase, indicating that the attractivity of females increased significantly during the period with higher probability of conception. Males, and especially the highest ranking male, were able to discriminate females nearing ovulation and to concentrate their mating effort, implying that the timing of ovulation was not concealed from them. The α male seemed able to monopolize most female matings, which is probably due in part to the low number of females simultaneously ovulating and to the limited number of inconspicuous places that the lower ranking males have to mate with females and avoid α male aggression. All together, these results suggest that different males may have access to different signals of ovulation and/or are differentially restrained as to how they can act on that information. The exact nature of the estrogen‐related cues males use to recognize female reproductive status, and to what extent males use them warrants further investigation. Am. J. Primatol. 71:868–879, 2009. © 2009 Wiley‐Liss, Inc.     

Seasonal changes in the spermatogenic epithelium of adult Japanese macaques (Macaca fuscata fuscata)

A histological study was undertaken to clarify seasonal changes in the spermatogenic epithelium of Japanese macaques. Testicular tissue samples were excised by biopsies from five adult laboratory-maintained males in mating and non-mating seasons. The samples were fixed with Bouin's solution, embedded in paraffin, and stained with PAS and hematoxylin. Microscopic observations on cross-sections of seminiferous tubules revealed that the seminiferous epithelium in the mating season was thicker than in the non-mating season. PAS-stained granules were found in some of the dark A-type spermatogonia, which significantly increased in the non-mating season. Spermatids of the steps preceding the appearance of the acrosomic cap in stages I to III were observed significantly more often than those in the step coinciding with the formation of the acrosomic cap in stage IV. In stage I, the ratio of mature spermatids or spermatozoa to immature spermatids in the mating season was higher than that in the non-mating season. These findings suggest that spermiogenesis, as well as spermatocytogenesis, is inhibited in the non-mating season.     

Inhibin B is the major form of inhibin secreted from testes in male Japanese macaques ( Macaca fuscata)

In order to clarify the cellular source and forms of bioactive inhibin in male Japanese macaques (Macaca fuscata), circulating concentrations of inhibin A and B, and immunohistochemical localization of inhibin subunits in testis were studied. Plasma concentrations of testosterone were also measured. The present study showed that inhibin B was clearly detected in the plasma of male Japanese macaques. Moreover, concentrations of both inhibin B and testosterone during the breeding (mating) season were significantly higher than those of the non-breeding season. On the other hand, plasma inhibin A was detected neither during the breeding seasons nor during the non-breeding seasons. Positive stainings with α and βB subunit antibodies were observed in the Sertoli cells, however staining with βA subunit antibody was not observed in the testicular samples. These results indicate that inhibin B is the major circulating inhibin and probably secreting from Sertoli cells in male Japanese macaques.     

Affiliative relations among male Japanese macaques (Macaca fuscata yakui) within and outside a troop on Yakushima Island

Male Japanese macaques (Macaca fuscata yakui) in a troop on Yakushima Island frequently groom other males. However, previous studies have not compared the social relations of troop males to those of non-troop males. I followed all troop males and non-troop males in and near a troop during a mating season and during the following non-mating season and recorded their neighbors, grooming, and agonistic interactions. Comparisons of the social relations of troop males and non-troop males with other troop members revealed that grooming and agonistic interactions with females during the mating season were similar between troop and non-troop males. However, troop males groomed each other more often and had fewer agonistic interactions among themselves than did non-troop males. Compared to what occurred in the mating season, troop males groomed females less often and exchanged grooming bouts more often with other troop males during the non-mating season. One non-troop male groomed females more frequently than did any troop male in both seasons, and this male groomed troop males more frequently than did any troop male in the non-mating season. This male immigrated into the troop during the following mating season. Regardless of their competition with respect to reproduction, male Japanese macaques on Yakushima Island maintain affiliative relations, probably to cooperatively defend fertile females from non-troop males.     

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.     

Age-related differences in social grooming among adult female Japanese monkeys ( Macaca fuscata)

The present study investigated the influence of dominance rank in combination with kinship on age-related differences in social grooming among adult females in a free-ranging group of Japanese monkeys (Macaca fuscata). Eighty-three adult females were divided into six sub-groups according to age-class (younger: 5–9 years old; middle: 10–14 years old; older: 15–22 years old) and dominance rank (high and low rank). The ratio of the number of unrelated females that each female groomed to the total number of available unrelated females and grooming bouts which she gave to unrelated females decreased with increasing age for both high- and low-ranking females, whereas age did not appear to affect corresponding values for related females. On the other hand, compared with low-ranking females, high-ranking females of all age-classes received grooming more often from a larger number of unrelated females. Moreover, older females of low rank received grooming less often from a smaller number of unrelated females than younger females of low rank. These results indicate that with increasing age females are more likely to concentrate on related females when they have grooming interactions with other females. This tendency seems to be more apparent for low-ranking females. Moreover, the present findings also indicate that older high-ranking females could maintain their social attractiveness as high as younger high-ranking females.     

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.     

Female rank and reproductive success among arashiyama B Japanese macaques (Macaca fuscata)

Five hypotheses that related female rank and reproductive success were tested in an intact troop of free-ranging, provisioned, Japanese macaques. The hypotheses stated that high-ranking females (1) begin parturition earlier in life than low-ranking females; (2) produce more offspring than low-ranking females; (3) give birth during some optimal time during the birth season to a greater extent than low-ranking females; (4) experience less infant mortality than low-ranking females;and (5) more frequently produce male offspring, while low-ranking females more frequently produce female offspring. A statistical analysis of the data which included three birth seasons and 55 adult females and 34 pubescent females, all of known age, rank, and matrifocal membership in the Arashiyama B troop, revealed few significant results. An association was found between the rank of the matrifocal unit and the age of first birth. However, the relationship was the reverse of hypothesis 1, i.e., females of the lower-ranking matrifocal units began parturition earlier than females of higher-ranking matrifocal units. Therefore, in this troop of Japanese monkeys— where alternative feeding strategies existed— there was little association between female rank and reproductive success.     

Matrilineal rank Inheritance varies with absolute rank in Japanese macaques

In many cercopithecine primates, females form linear dominance hierarchies based on kinship. It is known that female rank follows the rules of matrilineal rank inheritance (MIR): (1) maternal rank inheritance, (2) maternal dominance, and (3) youngest ascendancy among sisters. Although, several determining such variation remain largely unknown. In this paper, I investigate the dominance relation-ships of 69 adult (>6 yr old) female Japanese macaques (Macaca fuscata fuscata) in a free-ranging provisioned troop living in Shiga-Heights (Nagano Prefecture, Japan) and report new evidence of intra-group variation. Dominance relationships among high-ranking females followed MRI within kin units, those among low-ranking females did not. Maternal rank inheritance and youngest ascendancy operated between mother/daughter dyads and sister dyads of high-rank, but not in the dyads of low-rank. The dominance ranks of females from low-ranking kin units were dispersed and less predictable. These findings suggest that MRI varies with absolute dominance rank, and are discussed in relation to other asymmetries between high-and low-rank     

A fatal attack on an unweaned infant by a non-resident male in a free-ranging group of Japanese macaques (Macaca fuscata) at Katsuyama

A non-resident male attacked a 4-month-old unweaned infant in a free-ranging group of Japanese macaques (Macaca fuscata) and it died 2 days later from a severe wound. When the infant was alone at the feeding site, the non-resident male rushed at it. The infant ran away as soon as it became aware of the male, but was captured. The male bit the infant on its hand, foot, and arm, while continuously scanning his surroundings. He did not kill the infant immediately and, after the infant escaped, he did not chase or attack it at all. Although the infants right arm was bleeding heavily, it survived until the following day. The infanticide occurred a few weeks before the mating season began, so the victims mother soon resumed estrus and the subsequent inter-birth interval was shortened. The first-, second-, and fourth-ranking adult males had died or disappeared a few months before this infanticide, and there were no other group members near the infant when the infanticidal male appeared. The infanticidal male had not been observed before this incident. Compared to one-male groups, the occurrence of infanticide in multi-male groups of Japanese macaques is extremely infrequent. However, in other reports of infanticide in Japanese macaques as well as in this case, it has been noted that infanticide is likely to occur in the pre- or early-mating season, when there are no resident males to defend the infant against attacks, and when a threatening male is least likely to be the infants father.Electronic Supplementary Material Supplementary material is available for this article at     

An experimental analysis of a mother-daughter rank reversal in Japanese macaques (Macaca fuscata)

This paper describes in detail how a 2.5-year-old female belonging to the second-ranking family in a captive group of three families managed to outrank her healthy, three-times heavier mother with the aid of the two immature daughters of the alpha female who was not herself directly involved. After the outranking was completed, the two active allies were removed. This had no effect on the rank relation between the female and her daughter. It is only after the mother of the two allies was removed (in addition to her daughters) that the mother recovered her rank above her daughter. This case study and the few other reported cases of changes in rank among females are discussed in relation to the issue of the stability of rank relations in hierarchical systems where rank is socially inherited rather than based solely on dyadic power contests. On the basis of this combined evidence, it appears that when attempting to rise in rank, females do not challenge dominants by allying with subordinates, but that they rather ally with an individual ranking above the target. This phenomenon, together with the fact that support is given to other females downwards the hierarchy, might explain the stability of female dominance relations and be the manifestation of an Evolutionarily Stable Strategy.     

Sex and season predict wounds in zoo-housed Japanese macaques (Macaca fuscata): A multi-institutional study

Japanese macaque societies are characterized by frequent intragroup conflict both in free-ranging and zoo-housed conditions. In zoos, understanding the factors that contribute to wounding is of interest because this knowledge can aid in proactive husbandry and management planning that can minimize the negative impacts wounding can have on individual welfare. This study sought to determine whether the variables sex, season and age predicted wounding rates. Data were collected for 24 months on 119 Japanese macaques living in 10 zoos, and we analyzed the contribution of variables using generalized linear mixed models. A total of 1,007 wounds were reported, and the best model included the interaction between sex and season. Follow-up analyses revealed that females incurred more wounds than males, and this sex difference was more pronounced during the breeding compared to the nonbreeding season. On average, individuals received 4.67 (±SEM: 0.55) wounds per year and 77.31% of the population incurred at least one wound in the study period. The majority of wounds were superficial and did not require veterinary intervention. Wound locations were not randomly distributed across body regions and were most often reported on the face. Finally, macaques living in larger social groups experienced more wounds, on average. This study represents the first quantification of wounding in this species and may provide insight to help inform husbandry and management strategies in zoos.     

Seasonal changes in spermatogenic cell degeneration in the seminiferous epithelium of adult Japanese macaques (Macaca fuscata fuscata)

The degenerating pattern of spermatogenic cells in the seminiferous tubule of Japanese macaques was studied to clarify a relationship between seasonal changes of reproductive performances and cytological findings in the Japanese macaque. For light microscopy, testis samples were obtained from five adult animals by biopsy in April (nonmating season) and October (mating season). For electron microscopy, specimens from four additional macaques were used. Degenerating cells were found in all steps of spermatogenesis. In stages I to V of the cycle of the seminiferous epithelium, morphologically atypical pachytene spermatocytes were observed in 14.7 and 10.0% of the cells in the nonmating and mating seasons, respectively, although the difference in percentage was not significant. Mature spermatids with atypical features in those stages occupied 59.6% of the cells in the nonmating season, which significantly decreased to 34.1% in the mating season. These results imply that the seasonal change of sperm production is related, at least in part, to the process of degeneration of the spermatogenic cells in this species.     

Social rank and cortisol among female rhesus macaques (Macaca mulatta)

In animal societies, some stressful events can lead to higher levels of physiological stress. Such stressors, like social rank, also predict an increased vulnerability to an array of diseases. However, the physiological relationship between social rank and stress varies between different species, as well as within groups of a single species. For example, dominant individuals are more socially stressed at times, while at other times it is the subordinate ones who experience this stress. Together, these variations make it difficult to assess disease vulnerability as connected to social interactions. In order to learn more about how physiological rank relationships vary between groups of a single species, cortisol measurements from hair samples were used to evaluate the effects of dominance rank on long-term stress levels in despotic and less stringent female rhesus macaque hierarchal groups. In despotic groups, cortisol levels were found not to be correlated with social rank, but a negative correlation was found between social rank and cortisol levels in less stringent hierarchies. Low ranking monkeys in less stringent groups secreted elevated levels of cortisol compared to higher ranking animals. These data suggest that variations in the strictness of the dominance hierarchy are determining factors in rank related stress physiology. The further consideration of nonhuman primate social system diversity and the linear degree of their hierarchies may allow for the development of valid rank-related stress models that will help increase our understanding and guide the development of new therapeutics for diseases related to human socioeconomic status.     

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.