Infant Handling and Maternal Response in Japanese Macaques

We focused on the social interactions of infant Japanese macaques (Macaca fuscata) and on the protective response of their mothers to such interactions. Infant social interactions included: received allomaternal behavior (positive infant handling), hand touch and inspection (neutral handling), and aggression (negative handling) as well as social play. Maternal protective responses included aggression to the infant's interactant and restraining or retrieving the infant. All types of social interactions as well as the maternal response to such interactions showed clear developmental variations. Frequency of infant social interactions and maternal protective responses also showed large interindividual variability. Juvenile and subadult females without maternal experience were the most frequent infant handlers. Infants received positive handling primarily from their kin, while mothers were equally protective in response to positive handling received by kin and by non-kin. Conversely, kin showed higher levels of neutral handling and their interest was more easily tolerated by mothers compared to that of non-kin.     

Grooming and aggression in captive Japanese macaques

This study investigated the relations between allogrooming and aggression in a captive group of Japanese macaques (Macaca fuscata). Our aim was to test whether evidence of an interchange between allogrooming and a reduction in aggression could be identified at a group level. Female Japanese macaques did not direct less aggression to those group mates that groomed them most. Although generally they did not direct more grooming to those group mates that attacked them most, they did show increased grooming towards those nonkin group mates that showed the most aggression. These results are interpreted in light of the conflicting processes that are likely to underlie macaque social choices.     

NRAMP1 polymorphism in a hybrid population between Japanese and Taiwanese macaques in Wakayama, Japan

A macaque population produced by the hybridization of native Japanese macaques (Macaca fuscata) and introduced Taiwanese macaques (M. cyclopis) in Wakayama Prefecture was shown to possess three DNA haplotypes of the natural resistance-associated macrophage protein 1 (NRAMP1). Based on genotyping and comparison with M. fuscata populations, it was revealed that the introduced M. cyclopis population was polymorphic for the NRAMP1 locus. Extensive crossbreeding of the introduced species with the native species was confirmed using this genetic marker and the proportion of M. cyclopis genes was 57.4%. Results of statistical tests suggested non-random mating in the hybrid population.     

Standing and climbing a pole by members of a captive group of Japanese monkeys

In a captive group of Japanese monkeys, a juvenile female spontaneously began standing poles against a concrete wall and climbing up them in 1983. By 1987, 3 juvenile females out of 39 monkeys had acquired the behavior. They stood rather heavy poles, weighing 2.6 kg, against the wall and climbed up them without training. At the top of the poles, they often explored the smooth wall by licking or touching it.     

Development of epiphyseal union in Japanese macaques of known chronological age

Forty epiphyseal unions were studied in the two subspecies of the Japanese macaque at known chronological ages. The age standards of the beginning and completion of epiphyseal union were estimated. The total score of the ratings of the unions revealed significant correlations with chronological age before 9 years of age. The linear regressions were calculated in each group of different sex and different subspecies in order to enable predictions to be made of the chronological age from the total score. Although males and females generally showed the same pattern of sequences, the unions of the females united earlier than those of the males in both subspecies before 9 years of age. The Yaku subspecies demonstrated an earlier union than the common Japanese macaque in both sexes before the age of 9 years old. The epiphyseal union of the Japanese macaque usually developed earlier than the reported union in the rhesus macaque. A large number of epiphyseal unions united at least partially and the total score deviated widely during the range from around 4 to 6 years of age. This period was in accordance with the adolescent growth period, especially in males, with rapid growth of body size as observed based on by somatometrical measurements. The skeletal growth of the trunk was generally late compared with that of the limbs. During the range after 8 years of age, some unions of the trunk united earlier in males than in females. The epiphyseal union could allow a more precise age estimation than the body mass or dental eruption during a certain range of ages. However, developmental estimations obtained from animals fed artificially, as the present samples were, must be applied with caution to wild animals.     

Japanese monkey group translocation: Effects on seasonal breeding

A 150-member troop of Japanese monkeys (Macaca fuscata)was translocated from its temperate native habitat, near Kyoto, Japan, to a 42-ha enclosure near Laredo, Texas, in February 1972. The seasonal timing and distribution of 430 births recorded over the period 1954–1971 were compared to those of 186 births recorded in Texas from 1973 to 1979. Despite striking climatological and environmental differences between the pre- and the postranslocation sites, the timing of the birth season remaines unchanged, although the distribution of births was altered. These findings, considered in light of other published data on the seasonality of mating in macaques, suggest that a phenomenon akin to social drift may account for much of the intertroop variation that occurs.     

Vocal individual discrimination in Japanese monkeys

The present study determines which features of the coo call are used by Japanese monkeys Macaca fuscata for vocal individual discrimination. First, two female Japanese monkeys were trained to discriminate conspecific individuals vocally, using an operant conditioning. Using as stimuli three unknown individuals with 30 calls per individual, the two monkeys succeeded in discriminating new call exemplars from the three stimulus individuals. A discriminant analysis performed on calls used as stimuli indicated that start frequency of the fundamental and call duration were variables that can differentiate individuals efficiently. Then, playbacks of acoustically modified signals were used to indicate which vocal features are used by monkeys for the individual discrimination. Stimuli signals containing modified pitch or duration, or filtered so as to keep only the fundamental component, were tested. Results indicated that Japanese monkeys use multiple acoustical cues to perform vocal individual discrimination, including at least pitch, call duration, and harmonics. However, harmonics seem to be less important for discrimination than pitch and call duration.     

Birth-season interactions of adult female Japanese Macaques(Macaca fuscata) without newborn infants

The affiliative interactions of 11 adult female Japanese macaques that did not deliver an infant during the 1981 birth season of the Arashiyama West troop were examined. Consideration was given to the effects of kinship as a structuring element in these birth-season interactions and to the degree of association with various categories of troop members based on age, sex, and (in the case of adult females) whether or not the females were new mothers. Females without infants interacted predominantly with their yearling off-spring, although it was the behavior of the offspring that precipitated the interaction. These females were active in soliciting affiliation with nonkin new mothers, whereas female matrilineal relatives with new infants approached and remained in proximity to them more than did nonrelated new mothers. Females without newborns groomed and approached nonkin infants more than infants within their own matriline, and these infants were predominantly those of females in the highest-ranking matriline of the troop. Adult males were responsible for 40% of all grooming received from nonkin by the females without newborns, and these males approached them significantly more than did other adult females without infants. These patterns demonstrate that the structure of social relationships is influenced by the particular dynamics of troop contexts such as birth seasons, as well as by enduring, broad-based affinities which are less affected by cyclic changes in troop context.     

Discrimination of mother by infant among Japanese Macaques (Macaca fuscata)

Experiments on five mother-infant pairs of Japanese monkeys (Macaca fuscata)living together in a captive group were conducted during the first 12 weeks after birth in order to assess the time at which infants begin to discriminate their own mothers from other adult females. After removal from their social group, infants exposed to their mothers and three unfamiliar adult females at a distance of 150 cm failed to orient visually toward their mothers. However, when the infants were allowed to approach the four females, they responded preferentially to their mothers during the third month of life. We concluded that by 8–12 weeks of age, infant Japanese macaques are able to discriminate between their mothers and other adult females.     

Population dynamics of Arashiyama west Japanese macaques

Demographic data have been collected on the Arashiyama Japanese macaque population from 1954 until the present, through the fissioning of the original group into two parts in 1966, and through the translocation of one of the two groups to Texas in 1972. Population dynamics are reported for the Arashiyama West group in Texas during 1972 to 1979 and then compared to data from Japan. After a short period of adjustment for the translocated group, during which time natality rates were relatively low and mortality rates were relatively high, many aspects of population structure, birth rates, and survivorship showed trends similar to those observed in Japan. This suggests that both long-term homeostatic processes and shorter-term responses to environmental fluctuations are significant to the study of nonhuman primate demography.     

Group Composition Affects Seasonal Birth Timing in Captive Japanese Macaques

We analyzed birth dates recorded during an 18-year period in a group of Japanese macaques housed in the Rome zoo to assess the influence of environmental, physiological, and social factors on birth seasonality. Birth timing differed significantly among years. Birth timing was affected by reproductive condition of females—ones that had given birth in the previous year delivered significantly later than those that had not—but not by their age or dominance rank. We conducted further analyses separately on females that had or had not given birth in the previous year. In both subgroups of females mean birth date was not influenced either by environmental temperature and rainfall during the previous mating season or by group size. On the contrary, among females that had not given birth in the previous year, socionomic sex ratio—ratio of sexually mature males to sexually mature females—is positively correlated with both mean birth date and date of the first birth, but not with date of the last birth. Contrarily, among females that had given birth in the previous year, there is no significant relationship between these variables. We hypothesize that the effects of socionomic sex ratio on birth timing might depend on competition among males for access to fertile females. When the number of males per female was higher, mutual disruption of consort pairs may have led to a delay in the onset of mating.     

Measuring male-female relationships during the mating season in wild Japanese macaques (Macaca fuscata yakui)

Heterosexual relationships during one mating season were examined in a wild troop of Japanese macaques (Macaca fuscata yakui) on Yakushima Island, Japan. Validation tests of putative mate choice behaviors demonstrated that female initiation and maintenance of proximity, female lookback at the male, and sexual presents to the male, were associated with increased mating. Male grooming the female was also associated with increased mating. Ten dyadic social behaviors were subject to principal components analysis to empirically define behavioral dimensions of male-female relationships. The analysis yielded four relationship dimensions: ‘Mutual Choice and Male Coercion,’ ‘Female Choice’ (two types), and ‘Mutual Choice’ Dyads tended to be characterized by more than one dimension. The results suggested that females sought matings with multiple males of various dominance ranks. Female relationships with high ranking males contained elements of male coercion and mate guarding, however, because these males attempted to inhibit females from mating with lower ranking males. The correlation between each relationship dimension and mating success depended, in part, on the dominance rank of males. Relationships involving high ranking males, which were most likely to contain elements of male coercion and mate guarding, were associated with mating success. Relationships involving low ranking males, which usually lacked such coercive elements. were less strongly correlated with mating success. These results, obtained from a wild troop, are compared to those previously obtained in captive and provisioned groups of Japanese macaques.     

Development of co-feeding relationships in immature free-ranging Japanese monkeys (Macaca fuscata fuscata)

The co-feeding relationships of immature Japanese monkeys in the provisioned situation were studied. The most frequent co-feeders for immature females were diversified as compared to those for immature males. The number of immature females who showed strong co-feeding relationships with their mothers gradually decreased with age in both high- and middle/low-ranking matrilines, but the percent decrease was greater for middle/low-ranking immatures. Almost all immature females who displayed strong co-feeding relationships with adult males were from middle/low-ranking matrilines. Strong co-feeding relationships with mothers among immature males from high-ranking matrilines remained until 4 years of age. In contrast, strong co-feeding relationships with mothers among middle/low-ranking immature males decreased rapidly in the first year of life, and most 1- to 4-year-olds showed no strong co-feeding relationships with other group members. It is considered that middle/low-ranking mothers may not provide their immatures with a secure base for obtaining food in the provisioned situation.     

Hierarchy,kinship and social interaction among Japanese monkeys (Macaca fuscata)

The study reports the relationship between hierarchy, genetic relatedness and social interaction in captive Japanese macaques. Grooming and proximity were found to be positively related to both dominance rank and degrees of relatedness. Ranks also positively correlated with threats while no relationship was observed between genetic relationships and agonistic interactions. The removal of a-male tightened the male hierarchy while the female hierarchy became relatively loose. Affiliative behaviour became more correlated with ranks than degrees of genetic relatedness. In the absence of α-male, the next dominant male avoided involvement in either agonistic or afliliative interactions with reintroduced animals and group females.     

Spontaneous establishment of a novel Japanese macaque cell line with epithelial cell phenotypes

A novel macaque cell line (J3K) with epithelial phenotypes was spontaneously established from a kidney specimen of a Japanese macaque (Macaca fuscata). Its population doubling level reached more than 500, and it was regarded as an established permanent cell line. J3K cells have transformed cell phenotypes such as loss of contact inhibition and anchorage-independent cell growth. Unlike other monkey adherent cell lines, J3K had no SV40 large T antigen. After establishment, cells have constantly expressed telomerase activity, whereas telomere length has been maintained. No mutations in the coding regions of the p53 complementary deoxyribonucleic acid were detected in the late-passaged cells. J3K, a novel transformed epithelial cell line, will be useful material for the comparative study of human and other primate cellular aging as well as cancer cell biology.     

Seasonal variation and sex differences in the nutritional status in two local populations of wild Japanese macaques

Seasonal variations and sex differences in the nutritional status in two local populations of wild Japanese macaques (Macaca fuscata fuscata) were examined. It was hypothesized that the ecological condition and/or reproductive strategies of each sex determine the nutritional condition and its seasonal fluctuation in each sex. Morphometric measures such as body mass, thoracic and femoris circumferences, skinfold thickness in four places (triceps, biceps femoris, subscapular, and abdomen), and wet mass of mesenteric and omental fat were used for comparisons between sexes, seasons, and populations. Animals of the Shimane population were larger than those of the Boso population in most morphometric measures, abdominal skinfold, and mesenteric and omental fat mass, suggesting environmental and/or genetic differences in the two populations. Females of both populations had larger skinfolds and mesenteric and omental fat mass than males, indicating that females had more fat than males. Females showed seasonality in most measures, having two peaks of body mass, thoracic and femoris circumferences, abdominal skinfold, and mesenteric and omental fat masses in early spring and late fall. In contrast, males exhibited no clear seasonal variations for most measurements, except for biceps femoris and subscapular skinfolds, which showed peaks in summer. Most morphometric measurements significantly correlated to each other, particularly in females, but most skinfolds had no correlation with other measurements. These findings suggest that sexual dimorphism in body composition and its fluctuation may be affected by the different reproductive strategies of males and females.     

Regional differences in the infection of wild Japanese macaques by gastrointestinal helminth parasites

A coprological survey of gastrointestinal parasites in wild Japanese macaques (Macaca fuscata), from 14 natural habitats was done. Ova of five nematode species (Trichuris trichiura, Strongyloides fuelleborni, Streptopharagus pigmentatus, Oesophagostomum aculeatum, andGongylonema species) and a worm of the cestode species,Bertiella studieri, were detected. Some differences found in rates of infection by sex were observed in the 14 areas. Differences based on age were found in only troops in which the infection rates ofStrongyloides fuelleborni, Streptopharagus pigmentatus, andTrichuris trichiura were higher in the juvenile monkeys. The number of parasite species was related to the geographical and climatic conditions of the habitat of the troop: troops living in areas cold in winter were infected by fewer parasite species than those in southern warmer areas.     

Threat calls in alliance formation by members of a captive group of Japanese monkeys

The vocal behavior of threat calls was investigated in a captive group of Japanese monkeys (Macaca fuscata fuscata). The vocalizations were heard most often when they undertook winner-support during triadic agonistic interactions. The likelihood of call emission in support of the winner was affected by the attributes of the participants, and not by the types of agonistic behavior. The calls were emitted by intermediate ranking animals frequently in support of high ranking animals and in support of females. The calling behavior of winner-supporters appears to advertise the partner and distant group members of their support for reciprocation in the near future.     

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.     

Mirror responses in a Japanese macaque troop (Arashiyama West)

Behavior toward two mirrors in the field was observed in the Arashiyama West troop ofMacaca fuscata. Counts of visits to the mirrors, plus scan and focal animal sampling were used. Some animals were marked with fluorescent paint to test informally for self-recognition. A relatively high mean frequency of visits to the reflecting side of both mirrors by all age classes, ranks, and sexes was recorded. There was no age difference in frequency of mirror visits per sample but adults spent more time per visit than subadults who in turn spent more time than juveniles. There was no indication of self-recognition by paint-marked animals. Mirrors appeared to be used to monitor the reflected scene and to look at the self-image. Social behavior in the mirror zone that was not directed toward the mirror was common to all age classes. Species-typical behavior directed toward the mirror was seen in younger animals but very seldom in adults. No threat displays by any animal were observed. We suggest that for adults the mirror image was not seen simply as another monkey.