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.     

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.     

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.     

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.     

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.     

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.     

Endocrine correlates of rank,reproduction, and female-directed aggression in male Japanese macaques (Macaca fuscata)

Fecal testosterone and cortisol levels in six wild male Japanese macaques (Macaca fuscata), three of high rank and three of low, were analyzed to investigate the hormonal correlates of rank, reproduction, and female-directed aggression. The study encompassed the 6-month mating season, from October 1999 to March 2000, during which time 251 fecal samples and approximately 550 h of behavioral data were collected. Dominant males were not found to differ from subordinate males in overall rates of aggressive or copulatory behavior. Likewise, testosterone excretion, which peaked in the early part of the mating season and declined gradually thereafter, did not differ significantly by rank. High-ranking males, however, were observed to excrete significantly higher levels of cortisol than low-ranking males, suggesting that dominance may carry costs. The two hormones were found to be inversely correlated in the two most dominant males, but independent in all others. Rate of noncontact aggression was significantly correlated with testosterone, while no significant relationships were observed between testosterone and contact aggression nor any aspect of copulatory behavior. These data further support the contention that social subordinance and stress are not inexorably linked, as well as suggest that elevated glucocorticoid concentrations in high-ranking males may reflect increased metabolic costs associated with dominant male reproductive strategy.     

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.     

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.     

Birth rate and mortality rate of infants with congenital malformations of the limbs in the Awajishima free-ranging group of Japanese monkeys (Macaca fuscata)

The birth rate and mortality rate of infants with congenital malformations of the limbs were examined in the Awajishima free-ranging group of Japanese macaques (Macaca fuscata). Of the 606 infants born between 1978 and 1995, 86 (14.2%) were malformed. The male-female ratio did not differ between malformed and normal infants. Most kin-groups included females who gave birth to malformed infants at least once. The mortality rate within the first year after birth for malformed infants (28.2%) was significantly higher than that for normal infants (10.0%). However, this indicates that more than 70% of malformed infants were able to survive for the first year of life, even though they were unable to cling to their mothers ventrum due to their limb deformities. This finding indicates that maternal care-taking is sufficient to enable malformed infants to survive during the early stages of development and that clinging by the infant is not necessary for the display of maternal care. Am. J. Primatol. 42:225–234, 1997. © 1997 Wiley-Liss, Inc.     

Genotyping from semen of wild Japanese macaques (Macaca fuscata)

The noninvasive collection of animal cells is crucial for DNA analyses in wild populations that cannot be disturbed by capture. We describe the collection of 68 semen samples following copulation and masturbation events in wild habituated and nonhabituated troops of Japanese macaques on the protected island of Yakushima. We used this DNA to amplify 390 base pairs (bp) of the mitochondrial DNA control region in 16 individuals from eight troops, and found a monomorphic pattern in agreement with the low variability imposed by geographic isolation and female philopatry. We also amplified two microsatellite loci from samples collected after the resident males of a focal troop had copulated with different females. We found several different allele combinations in samples collected after the observed mating of a single male, indicating the presence of contaminant DNA, presumably from males that had previously mated with the same female. This discovery made it impossible to assign a given sample to a specific male except when the samples were recovered after masturbation events. Thus, it was not possible to test for kinship or estimate allele frequencies from the semen samples. The mixing of semen, and the pattern of sample collection observed in morphologically identified individuals support the notion that strong mating and sperm competition exists among resident and nonresident males.     

Development in the Usage and Comprehension of Greeting Calls in a Free‐Ranging Group of Japanese Macaques (Macaca fuscata)

The main objective of this study is to clarify the developmental process involved in both the usage of greeting calls and the response to greeting calls by Japanese macaques. These greeting calls facilitate affiliative interactions by communicating benign intent. Specifically, individuals frequently emit greeting calls when interacting with less‐predictable individuals. Here, we examined whether the targets at which greeting calls are directed, along with associated behavioral responses, differed among the age classes, by conducting a cross‐sectional observation of females aged 0–5 yr and their mothers. We found that infant females showed a weak tendency to emit greeting calls at no specific receivers, unlike that by older females. Adult females emitted greeting calls more frequently when approaching unrelated females than related females. In contrast, young adult or juvenile females exhibited no significant difference in the proportion of the calls with related and unrelated conspecifics. Adult and young adult females were more likely to respond affiliatively to other individuals that approached using greeting calls compared with silent approaches, whereas juveniles did not exhibit different responses to the two types of approaches. This study showed that the target‐specific usage and affiliative response to greeting calls emerge with changes in the developmental stage. Furthermore, the fact that even young adults did not use greeting calls as adults indicates that the usage of greeting calls is modified in conjunction with the expansion of social relationships.     

Effects of age, dominance, and seasonal changes on proximity relationships in female Japanese macaques (Macaca fuscata) in a free-ranging group at Katsuyama

The present study compares the behavior of old female Japanese macaques (Macaca fuscata) with that of their full adult daughters in a free-ranging group, with respect to dominance and seasonal changes. Old mothers (21 to 25 years old) spent more time resting and alone than did their middle-aged adult daughters (10 to 17 yr old). However, the number of skin-related animals in proximity to the subject females, did not differ between mothers and their adult daughters. Mothers maintained proximity to more non-kin-related immature animals in the mating season than did their adult daughters, perhaps to avoid sexual aggression from males and to reduce the loss of body temperature in the cold. Dominance rank clearly influenced the social interactions of old mothers: high-ranking mothers interacted with more non-related adult females and immature animals than did low-ranking mothers, indicating that old age does not decrease the attractiveness of high-ranking animals.     

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     

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.     

Borna disease virus RNA detected in Japanese macaques (Macaca fuscata)

We have examined the seroprevalence of BDV in wild Japanese macaques (Macaca fuscata) in the peninsula (Chiba prefecture), Japan. Serum samples from macaques were examined by the ELISA, Western blot and immunofluorescence assays to detect the presence of serum antibodies that react specifically to BDV antigens. Among 49 investigated individuals, 6 (12.2%) showed positive reaction to BDV antigens. RT-PCR studies detected BDV sequences in brain tissue of one case among four seropositive cases examined. Sequence analysis revealed a high degree of genetic conservation between BDV sequences derived from Japanese macaques and those documented for other animal species. Nevertheless, phylogenetic analysis revealed unique differences between macaque and other species derived BDV sequences.     

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.