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.     

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     

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.     

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.     

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.     

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.     

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.     

Foraging strategies of yakushima macaques (Macaca fuscata yakui )

I investigated the activity budget and diet of Yakushima macaques (Macaca fuscata yakui,)in warm temperate broad- leaved forest of Yakushima, Japan. Both time spent feeding and time spent moving varied considerably between half- months. However, total time spent in active behaviors— feeding time plus moving time— was stable. The composition of the diet also showed considerable variation between half- months. The macaques fed mainly on fruits, seeds,mature leaves, fallen seeds, flowers, and young leaves, each of which accounted for more than 30% of feeding time in at least 1 half- month. They also ate insects and fungi, but each of them comprised ≤ 25 and ≤ 8% of feeding time in any half- month, respectively. Time spent feeding on mature leaves, young leaves, flowers, or fallen seeds is positively correlated with total time feeding and is negatively correlated with time moving. In contrast, time feeding on fruits, seeds, insects or fungi is negatively correlated with time feeding and is positively correlated with time moving. Foraging on foods that have a low energy content, a high density, and a relatively even distribution— mature leaves— or that need much manipulation to be processed— flowers and fallen seeds— increased feeding time, while foraging on foods for which monkeys must search intensively in the forest— fruits, seeds, insects, and fungi— led to increased moving time. I examined foraging strategies of Yakushima macaques in terms of moving costs and the quality of food items. Regarding time feeding on fruits, which have more energy and may need less manipulation than other foods, as a benefit, and moving time as a cost, they seemed to employ a strategy that balanced the costs and benefits of foraging.     

Rapid shifting of foraging pattern by Yakushima macaques ( Macaca fuscata yakui ) in response to heavy fruiting of Myrica rubra

We describe short-term changes in foraging behavior by wild Yakushima macaques (Macaca fuscata yakui),which inhabit a warm-temperate broad—leaved forest on Yakushima Island (30°N, 131°E), Japan. Rapid changes of dietary composition, activity budget, and range use by the monkeys occurred from May to June, apparently associated with changes in the availability of the fruit of Myrica rubraBefore the fruit ripened, monkeys spent less time moving and more time feeding on many species of leaves, which accounted for 40% of feeding time. However, when M. rubrabegan to ripen, they fed intensively on the fruit, which accounted for three-fourths of feeding time,though the activity budget remained unaffected As fiuit of M. rubradecreased,the monkeys fed more on the fruit of other species and on insects, and spent more time moving at higher speeds. There marked shifts in foraging pattern occurred within only two months. In terms of moving cost and dietary quality,Yakushima macaques shifted their foraging pattern according to the availability of M. rubrafrom a “low-cost, low-yield” strategy to a “low-cost, high-yield” strategy, and then to a more costly strategy. The ability to make such rapid shifts in foraging pattern may allow the macaques to effectively use the highly variable food supply within their small range.     

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.     

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.     

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.     

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.     

Summer dietary compositions of sika deer on Yakushima Island,southern Japan

Summer food habits of Sika deer (Cervus nippon yakushimae) on Yakushima Island, southern Japan, were studied focusing in particular onPseudosasa owatarii, a dwarf bamboo native to the island. Fecal analyses showed that the food habit of the Sika deer on Yakushima island was plastic: the dietary composition was dominated by graminoids (ca. 90%), particularlyP. owatarii (50%–60%) in the bamboo grassland of theP. owatarii zone above the timber line, whereas leaves and non-leafy parts of woody plants were important in the crytomeria forest and evergreen broad-leaved forest below the timber line. The maximum culm age ofP. owatarii was 8.5 yr, but the majority of leaves (97.8%) were younger than 2.5 yr. Since the weight contribution of the leaves is great (27.7%) and the turnover rate is high, theP. owatarii grassland affords a good foraging place for the Sika deer on Yakushima Island.     

Dietary selection by yakushima macaques ( Macaca fuscata yakui ): The influence of food availability and temperature

I examined dietary selection by Yakushima macaques (Macaca fuscata yakui)in relation to food availability and air temperature. Multiple regression analysis indicates that both food availability and temperature influenced the selection of foods. Feeding on young leaves, seeds, and flowers was affected more by availability, while feeding on fruits, mature leaves, and fallen seeds was affected more by temperature. Feeding on insects is strongly correlated with temperature,perhaps because availability of insects increased with temperature. These results suggest that temperature influences dietary selection of Yakushima macaques by changing the energy expenditure required for thermoregulation and through its influence on the accessibility to insects, which are an important protein source for the monkeys.     

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.     

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.     

Fecal testosterone immunoreactivity as a non-invasive index of functional testosterone dynamics in male Japanese macaques (Macaca fuscata)

Validation of a simple method for the extraction and quantification of testosterone (T) from the excreta of male Japanese macaques (Macaca fuscata) is presented. Radioimmunoassay of paired fecal and serum samples collected from four intact sexually mature males during the breeding season provided profiles that were significantly correlated when samples were offset by approximately 48 hr. Additionally, no significant differences were observed in the pattern of temporal variation of T levels in serum and feces. Two castrated males were injected with radioinert T, and the patterns of excretion were observed by analysis of serial fecal and urine samples. Approximately 48 hr after the steroid was administered, a significant peak in the average fecal T levels was apparent. The injection event was also registered in the urine of both males, although qualitative differences were observed. These data suggest that measures of fecal T provide a reliable and non-invasive means of assessing gonadal function in this species. As the analysis of hormone levels in feces allows for frequent, stress-free sampling with minimal disruption, this method should be preferred in long-term orin situ applications requiring endocrine monitoring.     

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.