Intertroop Transfer and Dominance Rank Structure of Nonnatal Male Japanese Macaques in Yakushima, Japan

We examined the interaction between intertroop transfer and male dominance ranks in a wild population of Japanese macaques (Macaca fuscata yakui) in Yakushima using data collected over 15 years. Intertroop transfer tended to maintain a linear, stable, and age-graded dominance rank order among nonnatal males irrespective of variation in troop size or composition. All males that joined a troop at the top of the rank order were prime adults. Among males joining at lower ranks, entry at the most subordinate position in the hierarchy was common. Males joining at lower ranks tended to join troops in which all other resident males were the same age or older. Adult males tended to join troops with few or no males. Young males tended to join troops with many resident males, and in which a relatively large proportion of males was other young ones. Intertroop transfer was responsible for most rank changes of resident males. The most common cause of males rising in rank was the emigration or death of a higher-ranking male. Males fell in rank most frequently as a result of a new male joining the troop at the top of the hierarchy. Rank reversals among resident males were rare. The cumulative effects of male transfers produce sociodemographic variation within a troop over time and sociodemographic diversity among troops in a local population. A key feature of intertroop diversity is that larger troops have a significantly greater proportion of young males than smaller troops. This diversity also creates the potential for intertroop variation in the severity of male competition and provides a range of options for transferring males.     

Troop Extinction and Female Fusion in Wild Japanese Macaques in Yakushima

We observed three cases of troop extinction and two cases of female fusion in the wild population of Japanese macaques on Yakushima Island, Japan. Troops P and T decreased in size relatively slowly over a few years until each troop consisted of only three monkeys. Several months later, the remaining adult female of P merged with the adjacent troop S, followed by the remaining female of T. S subsequently also decreased in size and disappeared about 2 years later. In the early stage of troop decline, the mortality rate of adult females was as low as in a growing troop, but the birthrate was quite low. In the late stage of troop decline, the mortality rate increased and the birthrate remained low. An important factor leading to troop extinction may be an increase in population density and the resulting increase in intergroup competition. During the period when P and T declined and ceased to exist, the range of the adopted troop shifted to cover their previous ranges. In the fused troop, there was no severe aggression directed towards the immigrant females or harassment from residents of the adopted troop and there was affiliative social interaction between the immigrant females and resident members. These results agree with previous reports on female fusion: it occurs when the shrinking group consists of one or no adult member, and the immigrant females are not at a severe disadvantage in their adoptive group. A possible benefit for immigrant females is to avoid disadvantage of one-adult group in conflict with conspecifics. A possible cost for immigrant females is transfer to the other troop or to unfamiliar area or both. The cost to transfer to another group may not be high because the members of the adoptive troop are relatively tolerant to immigrants. The cost to transfer to unfamiliar range may be minimized by immigration to the troop whose range shifted to the immigrants' former range.     

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.     

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.     

Radio tracking of a male Japanese macaque emigrated from its group

A male Japanese macaque's ranging behavior before and after emigration from its group was investigated by using radiotelemetry techniques. The male's locations before leaving the troop were regarded as those of the troop, while those after leaving were regarded as those of a solitary male. Monthly home range sizes of the male with the troop were larger than those of the male moving alone, while the whole home range of the male with the troop for three months was much smaller than that of the male moving alone for five months. Overlaps between the male's home ranges with the troop between months were much greater than those between the ranges of the male moving alone. One neighboring troop's home range overlapped the male's range in August and September, and another neighboring troop's range overlapped the male's in October. The mean travel distance and speed of the male with the troop per day did not differ significantly from those of the male moving alone. The results suggest that emigrated males of Japanese macaques may visit home ranges of some troops and stay for a while without interacting troop monkeys before they decide to visit or join the troops.     

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.     

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.     

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.     

Changes of dominance rank,age, and tenure of wild Japanese macaque males in the Kinkazan a troop during seven years

Male age-rank and tenure-rank relationships were studied for seven years in unprovisioned Japanese macaque (Macaca fuscata fuscata) troop on Kinkazan Island, Japan. Males whose estimated ages were between 15 and 19 yr old monopolized the highest ranks, while older males whose estimated ages were ≥ 20 yr old tended to decline in rank, resulting in a humped age-rank curve. The ranks of males tended to rise as their tenure in the troop increased. The departure of higher-ranking males was the social mechanism for changes in rank, suggesting that the disappearance of higher-ranking males plays an important role in determining rank dominance.     

Suppressed copulatory behavior and ovarian function in lactating Japanese monkeys (Macaca fuscata fuscata) during the mating season

The influence of lactation on copulatory behaviors and ovarian functions was studied in Japanese monkeys (Macaca fuscata fuscata) during the mating season. Three lactating females were housed in an outdoor group cage with their infants, and three nonlactating females were housed in an adjacent outdoor cage. They were mated by introduction of one of four rotationally chosen males into the females' cage, for two hours three times a week; the occurrence of ejaculatory copulations was recorded. Blood samples were collected on each observation day, and plasma levels of estradiol, progesterone, and luteinizing hormone (LH) were measured by specific radioimmunoassays. In nonlactating females, plasma estradiol increased during the transition into the mating season, and rose to levels over 90 pg/ml for the first time on about 50 days before the first ovulation. Shortly after plasma estradiol exceeded 90 pg/ml in the nonlactating females, the onset of ejaculatory copulations occurred. They received ejaculations continuously up to the early ovarian luteal phase. On the other hand, in lactating females, there were lower levels of plasma estradiol (below 90 pg/ml) during the transition into the mating season, and they received no ejaculation during that period. Two of the three lactating females ovulated only once, and they received ejaculations only during the periovulatory period, coinciding with the rise of their plasma estradiol levels over 90 pg/ml. The remaining lactating female remained anovulatory and received no ejaculation throughout the entire mating season. These results have demonstrated that the low sexual activity of lactating females is clearly correlated with low levels of plasma estradiol due to suppressed ovarian function.     

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.     

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.     

Long-Term Trends in Matrilineal Inbreeding Among the Japanese Macaques of Arashiyama B Troop

In a long-term study of sexual behavior in Japanese macaques, we found that matrilineal inbreeding accounted for 2.9% of the copulations recorded for the Arashiyama B troop during 7 mating seasons between 1968 and 1984. Of the 906 copulatory dyads, 46 (5.1%) occurred among kin. Close matrilineal kin dyads (r = 1/2–1/8, 1.1% of the total of copulatory dyads) strongly avoided matrilineal inbreeding, but for remote kin dyads (r > 1/8, 4.0% of the total) the tendency was weaker in some years. Among the possible determinants of matrilineal inbreeding, we found that it tended to occur among younger and lower-ranking males as an effect of troop demographic changes. There is no significant association between female rank and matrilineal inbreeding. Our results are consistent with the hypothesis that different degrees of kin relatedness are discriminated by individuals with respect to mate choice.     

Sexual Maturation of Female Japanese Macaques Under Poor Nutritional Conditions and Food-Enhanced Perineal Swelling in the Koshima Troop

Provisioned food was severely restricted for 5 years, from 1972 until June 1977, in the insular Koshima troop of Japanese macaques. The monkeys experienced very poor nutritional conditions during this period. The feeding policy was changed in 1977 and food conditions improved, but only in summer. A remarkable consequence of intensive provisioning in summer was the occurrence of perineal swelling in many young females outside of the mating season. Females that matured during the period of poor food conditions showed an extraordinary delay in primiparity and exhibited conspicuous perineal swelling in the summer of 1977. Researchers studied the development of perineal swelling under standard conditions of constant provisioning from 1990 to 1995. First perineal swelling appeared at 5 years of age under standard conditions but appeared at 8 years of age under poor food conditions. The extraordinary delay in primiparity did not occur among females that were 6 years old when food conditions were improved in summer. We deduced that female Japanese macaques have a critical age of 5 to 6 years for sexual maturation. If the critical age is exceeded under poor food conditions, sexual maturation is hard to achieve even with improvements in food conditions. Seasonal changes in the incidence of perineal swelling were related to the period of high body weight. Rapid improvements in food conditions probably caused perineal swelling and activated sex hormones in female Koshima Japanese macaques.     

Social object play among young Japanese macaques (Macaca fuscata) in Arashiyama, Japan

Social object play (SOP), i.e., social play using portable object(s), among young Japanese macaques (Macaca fuscata; 0-4 years old) in the Arashiyama E troop was studied using a modified sequence sampling method from July to October 2000. SOP was a relatively common activity for most of the young macaques and often continued for long periods. Participants used many kinds of object, including edible natural objects and artificial objects, such as plastic bottles, but they never used provisioned food or wild fruit in SOP bouts. An analysis of long bouts (>/=0.5 min) revealed the following interactive SOP features: (1) at any given time, participants used only one object, and only one participant held the object; (2) during SOP play-chasing, the object holder was likely to be chased by others; (3) during long bouts, the object changed hands frequently; and (4) agonistic competition for an object among young macaques was rare. Combinations of sexes, ages, relative ranks, or matrilines of the object holder and non-holder did not affect the tendency that the holder was chased by non-holder(s) during play-chasing. Even when there was a change in object holders, the repetitiveness of this interactive pattern, i.e., that the holder would be chased during SOP bouts, distinguished the SOP structure from that of other types of social play without object(s). General proximate social play mechanisms, such as self-handicapping or role taking, were associated with SOP. Other mechanisms that affected SOP included the following: (1) young macaques treated an object as a target in play competition, and (2) 'being the holder of a target object' was associated with the 'role of the chasee.'     

Inter-male associations in a wild Japanese macaque troop on Yakushima Island,Japan

Adult male association and its annual change were studied in a wild population of Japanese macaques (Macaca fuscata yakui) on Yakushima Island, Japan. Unlike many other Japanese macaque troops, adult troop males frequently maintained proximity and exchanged grooming with one another in both the mating and non-mating seasons, and the dominance relationship rarely appeared in such inter-male associations. The few cases of agonistic interactions occurred mostly when estrous females or food resources were immediately concerned. Although troop males were very intolerant to newly appeared solitary males (new males) during the mating season, close associations were formed between troop males and new males as soon as the mating season terminated. The consort of new males and lower-ranking troop males with estrous females was frequently disturbed, but these males could copulate no less frequently than higher-ranking males. A comparison among macaque species suggests the existence of two forms of inter-male association: (1) the frequent association based on the symmetrical exchange of social behaviors; and (2) the infrequent and asymmetrical association related to the dominance relationship. The form of inter-male association seems to be influenced by whether or not males can keep close associations with females throughout the year.     

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.     

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.     

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.     

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.