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.     

Playmate relationships among individuals of the Japanese monkey troop in arashiyama

Observations of play behavior were made on a troop of Japanese monkeys for five months. The troop consisted of 125 animals during the study period. Only 104 animals were observed playing with the troop members while the other 21 animals were never observed playing with other individuals. Two-member play was the most frequent. On the average, a monkey played with 20.7 individuals. A total of 6,068 play bouts were observed. The frequency of play appeared to be affected by age, sex, and degree of relatedness. One-year-old infant males played most with other members and the frequency of play decreased with age. Between monkeys whose disparity of age was less than two years, 5,763 bouts (95.0% of the total) were observed. Moreover, among sameaged monkeys who comprised 10.6% of the possible pair combinations, 2,739 play bouts (45.1%) were observed. Juvenile males played with same-sexed peers more than with opposite-sexed peers, whereas older juvenile females appeared to play with infants of both sexes. Individuals who were related and similarly-ranked tended to play together. There was no apparent preference for animals to play with the offspring of the highest-ranking female. Dominance rank of infnats and juveniles was primarily affected by rank of their mothers and to a lesser extent by play partners. Dominance rank of older juvenile males is more likely to be affected by play partners than females. It may be a critical time for males when they leave their natal troop and join a new troop. The timing of troop shifting by males seemed to be affected by the presence or absence of play-mates. For male Japanese monkeys, play is very important in developing social bonds. Play may act to perpetuate social bonds, enhance the chance of survival, and may contribute to their future reproductive success.     

Variability in the development of mother-infant relationships among free-ranging Japanese macaques

Mother-infant relationships were studied during the infant's first year in free-ranging Japanese macaques (Macaca fuscata). Three possible factors controlling the mother-infant relationships were examined using multivariate analysis. Parity was determined to exert the strongest influence on mother-infant relationships. Specifically, during month 1, multiparous mothers showed greater maternal suckling rejection than primiparous mothers, and primparae and multiparae differed in their responses to suckling behavior. During month 6, multiparous mothers prompted independence of their offspring more than primiparous mothers. By month 8, however, parity differences in maternal behavior were substantially reduced. Maternal rank was a less important factor, although during month 1, high-ranking mothers showed greater maternal restriction than low-ranking ones. In the present study, infant gender appeared to have no effect on mother-infant relationships. That most differences were due to parity indicates that mother-infant relations were largely determined by the mothers. This observation conflicts with the “learning-to-mother” hypothesis. Allo-mothering of neonates by nulliparae is rare among Japanese macaques. Primiparous mothers learned appropriate suckling care from handling their own infants.     

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.     

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.     

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.     

The use of redirection in a captive group of Japanese monkeys

The present study was chiefly focused on nonadult animals of a captive group of Japanese monkeys housed at the Rome Zoo. Over a five month-period, during 1 hr daily observations, threats, chases, physical assaults, submissions, and flights showed by each participant to agonistic interactions were recorded. Sex differences in the behavioral responses to received aggression, in the distribution of threats or attacks in dyadic interactions and in the second dyads of redirections, in the dominance relationship between actor and target in dyadic interactions and in the second dyads of redirections, emerged. The results stressed the short term functional implications of redirection behavior and suggested more long term functional implications to be effective in the female redirection behavior.     

Male life history in natural populations of Japanese macaques: Migration, dominance rank, and troop participation of males in two habitats

This paper compares male life history parameters of two populations of Japanese macaques (Macaca fuscata Blyth, 1875), studied without provisioning: Yakushima (M. f. yakui), a subtropical forest habitat in southwestern Japan, and Kinkazan (M. f. fuscata), a temperate, deciduous forest habitat in northeastern Japan. The males of the two sites experienced similar life histories with respect to several traits. Age at natal dispersal was at about 5 years. Average troop residence was about three years. Most males joined troops at the bottom of the rank order, although a few males joined troops at the top rank. Dominance ranks of males tended to rise with the death or departure of higher ranking males. Visiting males accounted for about 41% of observed mating at both sites. However, the two sites differed in the sex ratio of troops, partly because a larger proportion of males apparently lived outside of troops in the Kinkazan site compared to Yakushima. In particular, non-natal young males were absent from the main study troop at Kinkazan. Large within-species variation may exist in the degree to which males associate with troops.     

Longitudinal changes of dominance rank among the females of the Koshima group of Japanese monkeys

The changes of dominance rank among female Japanese monkeys of the Koshima group over a period of 29 years from 1957 were studied. The dominance rank order was relatively stable in the early population growing phase, while large scale-changes of dominance rank order occurred successively in the phase of population decrease brought about by the severe control of artificial feeding after 1972. Nevertheless, the rank order of several females of the highest status was stable. Furthermore, the reproductive success of these highest status females was high (Mori, 1979a;Watanabe et al., in prep.). Divergence of the dominance rank order fromKawamura's rules (Kawamura, 1958) was observed in the following respects: (1) Some females significantly elevated their rank depending on the leader males. (2) If mothers died when their daughters were still juveniles or nulliparous, the dominance rank of some of these offspring females was significantly lower than the mother's one. However 55% of daughters which lost their mothers at a young age inherited the mother's rank. (3) Dominance among sisters whose mother had died when at least one of the daughters was under 6 years old followed the rule of youngest ascendancy in 60% (Kawamura, 1958), and in 80% when both of the daughters were nulliparous at the mother's death. The mean rate of aggressive interactions for each female with subordinates to her was calculated by dividing the total aggressive interactions between the female in question and her subordinates by the number of subordinate females to the female in question. A female which showed a high rate of aggressive interactions with her subordinates was categorized as an “Attacker”, and a female showing a lower rate was categorized as a “Non-attacker”. Similarly, categories of “Attacked”, and “Non-attacked” were distinguished by using the rate of aggressive interactions with dominant females. Several females which were once categorized in one category in a year were repeatedly categorized in the same category over different years. The “Attacked” tended to be females of higher rank, and “Non-attackers” tended to be females of lower rank. “The second-higher-status females”, were “Attacked”, and their rank was unstable. In particular, females of lower rank within the lineage of the highest rank suffered this kind of severe status. Most of the daughters of these females showed a sharp drop of rank, and died when they were still at a young age, i.e. “the second-higher-status females” displayed low fitness. “Non-attackers” were significantly “Non-attacked”; i.e. they were females which showed a non-social attitude. Females which underwent a drop of rank tended to be “Non-attackers”. The most important factor which determined the females' rank was the memory of their dominance relations under the influence of their mother [dependent rank (Kawai, 1958)] in their early life during development. This finding corresponds well with the results in baboons obtained byWalter (1980); the target females of aggressive interactions by adolescent females were determined by the rank of the mothers when these adolescent females were born.     

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.     

Huddling relationships in night sleeping groups among wild Japanese macaques in Kinkazan Island during winter

Huddling groups at sleeping sites, and allogrooming and proximity in the daytime during winter, were examined in a wild Japanese macaque (Macaca fuscata) troop on Kinkazan Island in the non-snowy district of northern Japan. All sleeping groups, defined as a cluster in which individuals huddle at sleeping sites, were formed on the ground. Their sizes tended to increase when the temperature was lower. The number of adults with mutual physical contact in sleeping groups increased when the size of sleeping groups increased. These results suggest that the physiological function of huddling is protection from low temperatures, and that macaques select the ground as sleeping sites to form large sized groups. Huddling was performed most frequently among kin dyads. Non-related dyads which appeared to be affiliative in the daytime also huddled frequently at sleeping sites. Even non-related dyads which showed affiliative behavior less frequently in the daytime exhibited huddling, at night, however, they did so less often than those of kin dyads and affiliated dyads. It appears that huddling at night by pairs that did not normally affiliate in the daytime was made possible by the increased tolerance of individuals responding to colder temperatures at night in winter. Furthermore, huddling, grooming, and proximity were exhibited at greater frequency between kin dyads, and between high-ranking males and specific females of kin groups, although the dyads of individuals older than 15 years often were involved only in huddling. These results suggest that two types of social bonds exist at sleeping sites in winter. One is the social bond common to both the daytime and nighttime, the other is peculiar to nighttime. Consequently, the social function of huddling is that, troop integration might increase at sleeping sites in winter as close social relationships among adults are extended more widely than those in daytime.     

Comparative study of grooming relationships among wild Japanese macaques in Kinkazan A troop and Yakushima M troop

The influences of socionomic sex ratio (SSR; adult males/adult female) and troop size upon male-male, female-female, and male-female grooming relationships were examined and compared between two wild Japanese macaque troops (Kinkazan A and Yakushima M troops) in Japan. The Yakushima M troop was smaller and had a higher-SSR than the Kinkazan A troop. Between the troops, (1) the male-male grooming frequency and number of partners were greater in the Yakushima M troop than in the Kinkazan A troop; (2) the female-female grooming frequency and number of partners were not different; and (3) the male-female grooming frequency and number of partners were not different. Based on these features, the patterns of female-female and male-female grooming relationships appear to be independent of SSR and troop size variations. In contrast, male-male grooming relationships are influenced by both factors, especially SSR. Frequent grooming interactions among males may be useful for the continued coexistence of relatively many males especially in a higher-SSR troop.     

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.     

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.     

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.     

The influence of snowfall,temperature and social relationships on sleeping clusters of Japanese monkeys during winter in Shiga Heights

We studied Japanese monkeys (Macaca fuscata) of the Shiga A₁ troop at their sleeping sites in Shiga Heights, Japan, for 41 nights during 3 winters. Monkeys chose their sleeping sites in Japanese cedars and in deciduous broad-leaved forests on non-snowing nights and in Japanese cedar forests on snowing nights. We counted 399 sleeping clusters in which 2 or more monkeys remained in physical contact through the night and 43 solitary sleeping monkeys, though monkeys did not maintain physical contact with others in the daytime. We found 397 clusters on tree branches and 2 clusters on rocks. The mean size of huddling clusters was 3.06±1.22 SD. The cluster size (3.17±1.26 SD) at lower ambient temperatures between −7 and −4°C was larger than that at higher temperatures between −2 and 4°C (cluster size 2.88±1.13 SD). Most clusters were composed of kin. Females kept close to related females in the daytime and huddled with them at night. The highest-ranking male mainly huddled with his kin and his familiar females. Other males kept farther apart from each other in the daytime, probably to avoid social conflicts. Through cold winter nights, however, such males reduced inter-individual distances and huddled with other males. Japanese monkeys appear to recognize three types of inter-individual distances: an intimate distance less than 1 m, a personal distance of 1–3 m and a social distance of 3–20 m; they change their inter-individual distances according to social and ecological circumstances.     

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.     

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.     

Are daughters more costly to produce for Japanese macaque mothers?: Sex of the offspring and subsequent interbirth intervals

Based on a sample of 237 live births recorded over a period of 30 years, a tendency for longer interbirth intervals following the birth of daughters than sons was recognized, in the provisioned Arashiyama troop of Japanese macaques. This may indicate that female infants were more costly to produce than male infants. This tendency seemed to be independent of a mother’s rank.     

Feeding strategies of Japanese monkeys against deterioration of habitat quality

Field observations of the feeding behaviour of Japanese monkeys were carried out from autumn to winter on Kinkazan Island which is covered with cool temperate forest. As a result, the following two points became clear: (1) the available food items were fixed for a long time; and (2) the habitat quality deteriorated monotonously because the monkeys themselves or their competitors, such as wild mice, utilized the food resources. Against the decrease in food intake caused by this deterioration of the habitat quality, the monkeys controlled the decrease in food intake by employing the following strategies: (1) they recovered their feeding speed by exploiting new food patches (patch-increase strategy); (2) they extended the time spent on feeding (time-extension strategy); and (3) they changed their food (food-change strategy). The former two strategies operated earlier than the third one.