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.     

How social relationships influence a monkey's choice of feeding sites in the troop of Japanese macaques (Macaca fuscata fuscata) on Koshima islet

When the individual Japanese macaques of the Koshima troop feed on natural food, they usually feed alone. In situations where animals usually feed without other animals, there is a possibility that subordinate animals may avoid feeding sites at which dominant animals are feeding. This paper examines whether social relationships such as kinship or dominance exert any influence on an animal's choice of feeding sites, by analyzing episodes in which an animal approached and climbed into a tree where other animals were. As a result, it was found that social relationships did not influence whether an animal climbed into a tree where other animals were feeding, and that no particular age-sex pair co-fed. Agonistic interactions frequently occurred when the inter-individual distance was less than 1 m. From these findings, the feeding sites were divided into two spaces: (1) a tolerance feeding space, and (2) an intolerance feeding space. It is presumed that animals can feed without entering others' intolerance feeding spaces when food is abundant, as it was in the present study period. Thus social relationships do not influence an animal's choice of feeding sites in such a situation.     

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.     

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.     

Bioenergetics of Japanese monkeys (Macaca fuscata) on Kinkazan Island during winter

An adult female Japanese monkey was chosen as a focal animal in order to assess the nutritional condition of the species during winter on Kinkazan Island, which is covered by deciduous forest of the cool temperate zone. Five whole-day-long observations were performed at the end of November (late autumn) and also at the end of February (late winter). In November, the daily energy intake and protein intake were estimated to be 1,449 kcal and 36 g, respectively: both satisfied the intake requirement even in view of a digestibility of 55%. These findings suggest that the focal animal could accumulate body fat in November. In contrast, in February, the daily energy intake and protein intake were estimated to be 556 kcal and 12 g, respectively: both did not satisfy the intake requirement in view of a digestibility of 55%. These findings suggest that the focal animal consumed accumulated body fat in February. Various data for food intake, nutritional content, etc. on Kinkazan were compared with those on Koshima, which is covered by evergreen forest of the warm temperate zone. The nutritional intake in February on Kinkazan was much smaller than that in November on Kinkazan as well as those in November and February on Koshima. The small intake of the former appeared to be strongly influenced by the sign ficantly lower speed of dry weight intake, which derived partly from the significantly lighter unit weight of the food items (e.g., buds ofZanthoxylum piperitum, Castanea crenata, andCornus macrophylla; leaves and stems ofOplismenus uadulatifolius andZoysia japonica). The monkeys on Kinkazan Island increased their food diversity, shortened their daily travel distance, and avoided repeated use of sites within their home range to offset the deterioration of the food quality in February.     

Comparison between the diameter of hair cross-sections and the thickness of the enclosed hairs in Japanese monkeys (Macaca fuscata fuscata)

The thickness of hairs from Japanese monkeys was measured by enclosing the hairs on slide glasses with balsam. Nine monkeys were used for the study. Forty to 69 hairs from the back were examined per head. High correlations between the thickness of the enclosed hairs and the diameter of cross-sections were obtained in all monkeys. In the Japanese monkey, therefore, it is considered possible to utilize enclosed hairs for measuring the thickness without preparing cross-sections. Moreover, the medullae of which the air layers are strongly related to thermoregulation, were readily observed in the enclosed hairs.     

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.     

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.     

A further food-washing tradition in Japanese macaques (Macaca fuscata)

A case of food-washing tradition is reported in a captive group of Japanese macaques. Two techniques are employed, with one or both hands being used to wash food under water flowing from watering spouts. Processes of diffusion of the behaviour in the group follow the patterns previously described by Japanese scientists observing this species. It is suggested that development of such a behaviour could be related to particular environmental conditions.     

Social behavior of infant and mother Japanese Macaques (Macaca fuscata): Effects of kinship,partner sex,and infant sex

The behavioral interactions of 22 infant and mother Japanese macaques with other group members were studied. Focal-animal observations were made from the time of each infant’s birth until 1 year of age. Infants and mothers both displayed exceedingly strong preferences for associating with matrilineal kin and, specifically, for female kin. The degree of genetic relatedness was positively correlated with levels of spatial proximity, contact, grooming, aggression, and play. Overall frequencies of interactions with nonkin were very low, and partner sex was not an important factor in interactions with nonkin. There were no significant differences between male and female infants in interactions with kin versus nonkin. There was only one significant difference between male and female infants in interactions with males versus females: female infants showed stronger preferences for initiating proximity with females over males than did male infants. Because mothers provide the focal point for infant interactions during the first year of life, we compared the behavior of infants and mothers. Mothers were the recipients of more social interactions than were infants, mothers engaged in more grooming than did infants, and infants engaged in more social play than did mothers. These findings are only partially consistent with kin-selection theory, and the inadequacies of studying matrilineal kin discrimination to test kin selection are reviewed. The near-absence of infant sex differences in associations with social partners suggests that although maternal kin other than the mother are important to infant socialization, they probably do not contribute to the development of behavioral sex differences until after the first year of life.     

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.     

Decision making in grooming by Japanese macaques (Macaca fuscata)

I analyzed the temporal organization of individual Japanese macaques’ (Macaca fuscata) grooming sequences in 14 mothers and 13 offspring of different age/sex classes and 4 nonkin females. I hypothesized that preceding grooming affects subsequent grooming by the same individual. Grooming bouts were likely to be terminated as the bouts became longer when females groomed nonrelatives. Moreover, the duration of first bouts was longer than that of following bouts. These effects were also seen in grooming of mothers by their offspring > 1 year old and that of adult and adolescent female offspring by their mothers. In contrast, neither the duration of first bouts nor the number of preceding bouts had much effect on the occurrence or duration of subsequent bouts in any subject.     

Adolescent growth and development in Japanese macaques (Macaca fuscata): Punctuated adolescent growth spurt by season

Adolescent growth of Japanese macaques (Macaca fuscata) was studied. Their growth is composed both of a seasonal cycle of acceleration and deceleration and of linear increases. There is a major growth spurt in linear dimension and body weight at the beginning of the breeding season of the third and fourth year of life in females and males respectively, when they mature reproductively. They show additional accelerated growth in the following year(s). These growth spurts, in total, are considered to correspond with the adolescent growth spurt in humans. Adolescent growth of Japanese macaques is characterized by a punctuation by slower growth and a later start, which is considered to be the product of adaptation to a strongly seasonal environment.     

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.     

Decisions on time allocation to different food patches by Japanese monkeys (Macaca fuscata)

From the standpoint of the possible development of an optimal foraging strategy, the time allocation to different food patches and the decision as to when to leave any given patch were examined in wild Japanese monkeys (Macaca fuscata). The investigations yielded the following results: (1) There was no tendency for feeding bouts to be of longer duration in higher-quality patches, i.e. the monkeys did not employ an energy-maximizing strategy during their feeding bouts. (2) The speed of feeding barely decreased with passage of time during a bout. In most cases, therefore, a decrease in feeding speed was not considered relevant to the decision to leave a patch. These findings are evaluated in terms of social factors, and it appears that following a monkey's own family group or the troop usually contributes to the timing of leaving a food patch.     

Lactation in the Japanese monkey (Macaca fuscata): Yield and composition of milk and nipple preference of young

Changes in the yield and chemical composition of milk, together with those in the nipple preferences and suckling behavior of infants, were followed in three lactating Japanese monkeys rearing single infants under laboratory conditions at monthly intervals for six months after their paturition. Milk accumulating in the mammary glands during a 4-hr separation of the infant was collected by milking under anesthesia with the aid of a physiological dose of oxytocin. The stage of full lactation appeared to last for about two or three months after parturition. The milk at this stage contained 14.0% of total solids, 4.2% of lipids, 1.6% of proteins, and 6.2% of lactose, and the concentrations of Na, Cl, and K in the milk water were 7.4, 15.1, and 5.9 mM, respectively. From the 9th or 13th week of lactation onwards, according to the individual, the milk composition changed appreciably and the time during which the young left hold of the mother's nipple also increased. The weaning of young in the Japanese monkey appears to begin during the 3rd or 4th month of age. The milk production then wanes and almost ceases by the end of the 6th month. The nipple preference of the young was generally established completely by the 3rd, or the 8th at latest, week of age. However, no difference in either the yield or composition of the milk secreted was found between the mammary glands of the preferred and non-preferred sides. Without regard to the apparent nipple preference, infants seem to ingest milk from the mother's breasts of both sides. Accurate estimation of the rate of milk production could not be achieved, but the rate was expected to be 150–200 g/day at the height of lactation based on the relation between the mother's body weight and the milk production rates of other primate species. A disparity was noted between the observed and estimated values for the milk yield, and a diurnal fluctuation in the milk secretion of the Japanese monkey was inferred. This study was conducted through the official system of the Primate Research Institute, Kyoto University, for cooperative research work with other institutions.     

Behavior of Japanese monkey (Macaca fuscata) mothers and neonates at parturition

Parturitional behavior in 12 caged Macaca fuscatawas analyzed. Wild-caught mothers showed adequate maternal behaviors immediately following the neonate’s expulsion. Parity differences existed in the behaviors; primiparae were more idiosyncratic than were multiparae. Among multiparae, those with two or more offspring were uniformly adequate, but those with a single birth experience varied in the adequacy of the maternal care they provided at parturition. Mothers embraced and licked their neonates and had ventroventral contact with them frequently immediately after parturition but decreased these behaviors after expulsion of the placenta. In contrast, mothers showed allogrooming after consuming the placenta. Placentophagy was correlated with the level of orality represented by maternal licking behaviors. An isolation-reared primipara reacted to her newborn in a basically negative manner, although she showed little actual aggression. She showed a rapid shift in her negative behavior during the immediate postpartum period. This mother’s newborn sought contact with her, indicating the neonate’s active role in establishing a stable mother-neonate bond.     

Socio-sexual factors of troop fission in wild Japanese monkeys (Macaca fuscata yakui) on Yakushima Island,Japan

The troop fissions which occurred in a wild population of Japanese monkeys (Macaca fuscata yakui) were observed from 1977 to 1979 on Yakushima Island. The fissions were initiated in the breeding season by non-troop males who established a consort relation with estrous females. In order to analyze the socio-sexual factors which accelerated the fissions, the male emigrations and immigrations before and after two successive fissions, and the copulation frequencies, competition among males and preferences of mating partners in both sexes in the 1977–78 breeding season after the first fission were examined. The results indicated that three factors (a large number of non-troop males, a shortage of troop males and the females' choice of mating partners) effectively influenced on the establishment of consort relationships between non-troop males and estrous females. It is suggested that these factors may exert different effects on the troop disorganization in relation to troop size. In small-sized troops, a large number of non-troop males and a shortage of troop males may lead to stronger competition between them, and the females' choice affected by prolonged intimate relations with the dominant TMs may reduce their priority of access to estrous females. This situation possibly stimulates fission or male emigration in small-sized troops under the natural conditions on Yakushima Island. In contrast, in large-sized troops under isolated conditions, a surplus rather than a shortage of troop males may contribute to troop disorganization, as most former studies have suggested. A higher socionomic sex ratio may decrease the mating activities of subordinate troop males and increase the competition among them. This situation possibly accelerates the fission of large-sized troops through prolonged interactions between females and subordinate or peripheral troop males. A lower ratio and the females' choice, however, raise the mating chances of subordinate troop males and may not promote the fission of large-sized troops under isolated conditions. This study was financed in part by a Grant-in-Aid for Special Project Research on Biological Aspects of Optimal Strategy and Social Structure from the Japan Ministry of Education, Science and Culture, and by the Cooperative Research Fund of the Primate Research Institute, Kyoto University.