Vertical distribution of wild Yakushima macaques (Macaca fuscata yakui) in the western area of Yakushima Island, Japan: Preliminary report

A census of wild Yakushima macaques (Macaca fuscata yakui) was carried out in a 23-km² area of the western coast of Yakushima Island, Japan. We analyzed the census data to investigate changes in monkey distribution associated with the vertical distribution of vegetation. In the lowland coastal zone of 0–300 m above sea level (a.s.l.), 4.8 troops and 62.4–99.8 monkeys are estimated to have existed per km². In the mountainside zones of 300–900 m a.s.l., the troop density decreased to 1.3–1.6 troops/km². Since there was no difference in size between the coastal and mountainside troops, population density should decrease with altitude to about 30–36 monkeys per km². On the other hand, 2.4 troops and about 36 monkeys were estimated to have inhabited per km² in the mountain summit zone of 900–1,323 m a.s.l. Nature Conservation College     

Cheek-pouch dispersal of seeds by Japanese monkeys (Macaca fuscata yakui) on Yakushima Island, Japan

Seed dispersal by Japanese monkeys (Macaca fuscata yakui) via cheek-pouch was studied in a warm temperate evergreen forest on Yakushima Island. Plant list was compiled based on a study during 1986–1995, of which troops of monkeys have been habituated without artificial feeding. We followed the well-habituated monkeys in 1993 and 1994 to observe the feeding behavior and their treatments of fruits and seeds, and collected seeds dispersed by monkeys to record the distance carried from the mother trees. We checked the difference of germination ratio between seeds dispersed via cheek-pouch and seeds taken from mother trees by sowing experiments. Seeds and acorns of 22 species were observed to be dispersed via cheek-pouch of monkeys. Among them, three species with acorns were never dispersed via feces, and 15 species with drupes were seldom dispersed via feces. Plant species of which seeds are dispersed only via cheek-pouch had larger seeds than those of dispersed both via cheek-pouch and via feces, and typically had only one or two seeds in a fruit. As for one of cheek-pouch dispersal species,Persea thunbergii, the mean distance when seeds were carried from the mother trees via cheek-pouch was 19.7 m, and the maximum distance was as long as 105 m although more than 80% of seeds were dispersed within 30 m from mother trees. And 82% of seeds dispersed via cheek-pouch germinated. The easy separation of seeds from other parts of the fruit seems to facilitate cheek-pouch dispersal more than dispersal via feces. Cheek-pouch dispersal by monkeys has possibly enhanced the natural selection for larger seeds which bring forth larger seedlings with high shade-tolerance. In conclusion, cheek-pouch dispersal by monkeys is quite an important mode for trees in the mature stand in a warm temperate evergreen forest on Yakushima Island.     

Low genetic diversity and biased distribution of mitochondrial DNA haplotypes in the Japanese macaque (Macaca fuscata yakui) on Yakushima Island

The Japanese macaques (Macaca fuscata yakui) on Yakushima Island are an endemic subspecies and are closely related to the population of Kyushu, one of the main islands of Japan. Using feces collected throughout Yakushima Island, we examined mitochondrial DNA (mtDNA) to investigate the phylogeography of Japanese macaques. Six haplotypes were observed for a 203-bp fragment of the mtDNA control region. The nucleotide diversity () was low (0.0021). The genetic divergence within the Yakushima population was lower (0.009) than that among four haplotypes of the Kyushu population (0.015), calculated using Kimuras two-parameter method. The mismatch distribution analysis of the six haplotypes of the Yakushima population suggested that the Yakushima population had experienced a sudden expansion in population size, which could be related to the bottleneck effect. The geographic distribution of the mtDNA haplotypes was not uniform. One haplotype was distributed widely, whereas the other five haplotypes were distributed only in the lowlands. The low genetic diversity and biased distribution are discussed in relation to an environmental crash caused by ancient volcanic activity near this island, which is postulated to have happened about 7,300 years ago, and the delayed recovery of highland vegetation.     

Monthly and diurnal variations in food choice byMacaca fuscata yakui during the major fruiting season at Yakushima Island, Japan

An ecological survey was conducted on two groups of wild Japanese macaques (Macaca fuscata yakui) inhabiting the warm-temperate, broad-leaved forest of Yakushima Island. The survey was designed to determine and explain monthly and diurnal variations in both duration of feeding and food choice, and to explain these variations from a nutritional perspective. Feeding activity increased during the hour before sunset, while leaf eating in particular tended to be observed later in the day throughout the study period. A diverse and unstable diet promoted monthly differences in fat and protein consumption. The mean lipid and calorific content of the food and the rate of protein intake were high in early autumn.Ficus fruits were not selected when unripeArdisia sieboldii fruits were available, but were an important food resource in a general context. Differences in nutritional intake at different times of the day were determined by the combination of species eaten although no single species was preferred at a particular time. Similarities with experimental results in laboratory animals suggest that a physiological, rather than a behavioural, response was regulating nutritional intake. A high consumption of proteins before rest might produce satiety in the macaques and give them the opportunity to digest and absorb complicated or toxic metabolites slowly during the night.     

Seed dispersal and predation by Yakushima macaques, Macaca fuscata yakui, in a warm temperate forest of Yakushima Island, southern Japan

The relationships between fruit morphology and the foraging behavior of the Yakushima macaque, Macaca fuscata yakui were studied during a 9-month field study and series of laboratory experiments on Yakushima Island, southern Japan. These relationships may affect seed germination traits through seed dispersal. The macaques foraging behavior was observed in order to obtain data concerning the treatment of pulp and seeds. Seeds in feces and spat seeds were collected and analyzed. A linear discriminant analysis of the data led to the following results: (i) an increase in the relative flesh volume of a fruit was one of the potential factors which increased the probability of seed dispersal by the macaques; and (ii) seed size was an important parameter in relation to the type of seed dispersal (by defecation or spitting out). The germination test was conducted in a laboratory, then the germination rates and delays of dispersed seeds were compared with those of seeds collected directly from trees. The germination of dispersed seeds of Ficus thunbergii, Eurya japonica, and Vaccinium bracteatum, was significantly enhanced by passage through the macaques gut. The enhanced germination behavior was not seen in larger seeds, such as those of Psychotria serpens, Myrsine seguinii, Diospyros morrisiana, and Neolitsea sericea. The germination enhancement in small-seeded plants could be due to a sorting effect from the passage through the gut, which selects seeds with a narrower range of germination traits.     

Activity patterns of a troop of Japanese monkeys (Macaca fuscata yakui) on Yakushima Island,Japan

Activity patterns of Japanese monkeys (Macaca fuscata) were observed for 240 hr from August to December 1976 on the western slope of Mt. Kuniwari, Yakushima Island, Japan. Activity patterns and the time budget of a habituated wild troop which consisted of 47 animals in August 1976, were studied quantitatively by using the scan-sampling method at 15-min intervals. Six thousand seven hundred and six animals were recorded in 959 scans during the study period and the mean number of animals seen per scan was 7.0. The time budget established for different categories of activity was as follows: inactive—20.9%; moving—22.8%; feeding—23.5%; social grooming—27.9%; self-grooming—1.2%; and other activities—3.7%. Adult males spent less time in feeding and more time in resting or being inactive than females or juveniles. The daily activity patterns were highly variable with respect to time. Intraspecific variations were examined between troops in several regions of Japan and it was noted that the percentages of time devoted to feeding were similar in all areas. Inter-species variations in the activity budgets of several species of primates were also examined. The percentage of time spent in social grooming by Japanese monkeys is exceptionally high compared to that recorded in other species.     

An ecological study of troop fissions of Japanese monkeys (Macaca fuscata yakui) on Yakushima Island,Japan

Wild, habituated, Japanese monkeys were observed from 1975 to 1979 on Yakushima Island, Southern Japan. The monkey troops had a continuous distribution in a warm temperate forest. Demographic data on local populations was collected. The population density was 33 animals/km². The growth rate of the studied troop was 3.0% per year. A significant correlation between home range areas (R) and troop size (P) was found (r=0.955,p<0.005), using anR-P equation,R=1.84P. One troop split into three troops through two successive fissions. Twenty-one intertroop encounters were observed. Five types of encounters were distinguished. The encounters were apparently territorial defence. Increases in birth rate and socionomic sex ratio after the fissions were prominent. The following four factors had a direct effect upon the dispersion of the troops after fission: (1) dominance relation between the fission troops; (2) social pressure of the neighbors; (3) troop's attachment to its home range; and (4) structure of the environment. The home range of Japanese monkeys is a territory, and territoriality is a population regulating mechanism which serves to reduce competition for food.     

Affiliative relations among male Japanese macaques (Macaca fuscata yakui) within and outside a troop on Yakushima Island

Male Japanese macaques (Macaca fuscata yakui) in a troop on Yakushima Island frequently groom other males. However, previous studies have not compared the social relations of troop males to those of non-troop males. I followed all troop males and non-troop males in and near a troop during a mating season and during the following non-mating season and recorded their neighbors, grooming, and agonistic interactions. Comparisons of the social relations of troop males and non-troop males with other troop members revealed that grooming and agonistic interactions with females during the mating season were similar between troop and non-troop males. However, troop males groomed each other more often and had fewer agonistic interactions among themselves than did non-troop males. Compared to what occurred in the mating season, troop males groomed females less often and exchanged grooming bouts more often with other troop males during the non-mating season. One non-troop male groomed females more frequently than did any troop male in both seasons, and this male groomed troop males more frequently than did any troop male in the non-mating season. This male immigrated into the troop during the following mating season. Regardless of their competition with respect to reproduction, male Japanese macaques on Yakushima Island maintain affiliative relations, probably to cooperatively defend fertile females from non-troop males.     

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.     

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.     

History and Present Scope of Field Studies on <Emphasis Type="Italic">Macaca fuscata yakui</Emphasis> at Yakushima Island,Japan

Field studies on Japanese macaques on Yakushima Island started in the mid-1970s, >25 yr after the emergence of Japanese primatology, in response to criticism of methods using provisioning and the desire to find the socioecological factors influencing the social life of macaques in natural habitats. We habituated macaques without provisioning mainly in the coastal warm-temperate forest and found that they lived in small troops with a high socionomic sex ratio. Observations of several troop fissions and troop takeovers by nontroop males suggest that Yakushima macaques have a different social organization from that of Japanese macaques in other habitats. For example, youngest ascendancy as the dominance relationhip among sisters, which usually occurs in provisioned troops, was absent in Yakushima macaques. We compared their ecological and social features with those of Japanese macaques at Kinkazan (cool-temperate forests) and found that abundance of high-quality foods may cause stronger intra- and intertroop competition at Yakushima. Female Yakushima macaques may more positively solicit nontroop males to associate with them during the mating season. Such a tendency may promote frequent male movement between troops and frequent troop fissions. Though ecological factors form social features of Japanese macaques, some features such as male association and movements between troops are not accounted for via socioecology. Recent field studies have focused on macaques living at higher altitudes in Yakushima and on individual survival strategies by taking diverse viewpoints and using new technologies. DNA analysis of fecal samples shows low genetic diversity and suggests the macaques’ recent expansion from lowland to highland forests in Yakushima. The population censuses conducted annually indicate that the higher-altitude macaques have a larger home range but a similar group size versus their counterparts at low elevations. The unsolved issues in socioecology will pose a challenge to the younger generation of primatologists. Conservation of macaques and their habitat is one of our major activities at Yakushima. The level of protection has gradually increased in the National Park at Yakushima and, via our various conservation efforts, its most important area was designated a World Heritage Site by UNESCO in 1993. However, large-scale logging in the 1960s and 1970s caused the loss of macaque habitats and led to increased crop damage by them in the 1980s. We have proposed effective methods to protect cultivated fields from macaques as well as several plans for sustainable use of forests, such as ecotourism and a fieldwork course for university students. Local residents and researchers have created several nongovernment organizations (NGOs) to promote conservation and nature study at Yakushima. The role of local NGOs is particularly important to mitigate conflicts between people and wildlife. Though hundreds of macaques are still captured as pests annually in Yakushima, we continue the conservation measures and spread awareness of conservation in cooperation with the local NGOs.     

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.     

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.     

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.     

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.     

Age-dependent patterns of intensive observation on elders by free-ranging juvenile Japanese macaques (Macaca fuscata yakui) within foraging context on Yakushima

Early learning about edible food in the environment is a critical survival task for young nonhuman primates. Social learning and social facilitation are often cited to explain how youngsters learn to select and find their food. In this framework, we observed eight mother-youngster pairs of free-ranging Japanese macaques divided into two sets according to the age of the young (infants aged between 7 and 12 months and juveniles aged between 1.5 and 2 years) during three winter months. We systematically investigated the intensive observation directed by the youngsters toward elders by recording the target's identity (e.g. mother, subadult), the items manipulated by the elder and those items closely observed by the youngster, along with the behavior of the youngster preceding and immediately following an intensive observation period. The diet of the mothers and juveniles was estimated from time records of each feeding occurrence for each food item (identified to species level) and from the quantity of fresh matter ingested. The results show that intensive observation by both infants and juveniles were directed toward those elders engaged in plant and invertebrate foraging. Such behavior was age-dependent, being more frequent in infants than in juveniles. The majority of the intensive observations were directed toward the mother. Intensive observations also shaped a change in the behavior of infants by significantly stimulating the investigation of food items and locations otherwise not investigated by juveniles. Moreover, infants showed a particular interest in rare food items and especially invertebrates. Age differences between the two sets of young and their interest in rare foods are discussed with reference to the occurrence of intensive observation within the framework of kin relationships, social organization, and social transmission of information about food type and food location and its survival values.     

Troop extinction and fusion in wild Japanese macaques of Yakushima Island,Japan

A wild Japanese macaque troop decreased in size because the birth rate dropped and infant mortality increased. In the 1989 mating season, the last male left the troop, and the remaining two females joined a neighboring troop. Thus, the troop ceased to exist as an independent troop. A lower limit to troop size may exist, below which a troop cannot effectively defend its range, forcing the females to join a larger troop. © 1994 Wiley-Liss, Inc.