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.     

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.     

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.     

Seasonal variation in the feeding behavior and diet of Japanese macaques (Macaca fuscata yakui) in lowland forest of Yakushima

The feeding behavior of the southern subspecies of Japanese macaque (Macaca fuscata yakui) was studied over a period of 18 months in warm temperate broad-leaved forest on the island of Yakushima, Japan. Focal animal data were collected for the eight adults in the troop. Over a full annual cycle, 35.0% of foraging on identified foods was on leaves and shoots, 30.2% on fleshy fruit, 13.2% on seeds, and 5.5% on flowers. Invertebrates and other animal matter accounted for 10.3% of foraging and fungi for 4.6%. There was marked seasonal variation in the use of different food categories, and seeds, leaves, fleshy fruit, and animal matter were each predominant at different times of year. There was also evidence of annual cyclicity in patterns of foraging on all major food types. The monkeys spent less time moving and ate a greater variety of foods when feeding on leaves than when feeding on fruit and seeds, or on insects. Time spent foraging was positively correlated with diversity of the diet, but there was no simple relationship between time spent foraging and the predominant food type. This suggests that a wide variety of foods takes longer to harvest and process, irrespective of the food type. The diet of the study troop was flexible and could not be assigned to a simple dietary category, such as frugivorous or folivorous. If these data are representative of the subspecies, the Yakushima macaque is much more of a dietary generalist than most primates for which there are adequate data. Am. J. Primatol. 43:305–322, 1997. © 1997 Wiley-Liss, Inc.     

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     

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.     

Bite forces used by Japanese macaques (Macaca fuscata yakui) on Yakushima Island, Japan to open aphid-induced galls on Distylium racemosum (Hamamelidaceae)

Japanese macaques on Yakushima Island have been seen attempting to open thick, woody plant galls in order to eat aphids contained within them. We analysed a sample of galls and gall fragments with toothmarks and found that 22% were still intact indicating a failure to open them. These marks were examined and measured. Ten pits had a mean indentational area of 1.44 mm² (S.D. 0.28 mm²), while 15 elongated scratches had a mean width of 1.26mm (S.D. 0.27 mm). The gall resembled a light wood in its mechanical properties and had a microhardness of 80.4MPa. Assuming that at least two marks were formed in any given bite, indentational analysis gave a mean estimate of bite forces of 232N (maximum 291 N) to produce pits and 255 N (maximum 487N) to produce scratches. These forces are consistent with, but at the high end of, limits predicted by anatomical analysis.     

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.     

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.     

Toughness and fiber content of major leaf foods of Japanese macaques (Macaca fuscata yakui) in Yakushima

During the spring, Japanese macaques in Yakushima feed predominantly on mature leaves of trees, vines, and ferns. They are selective in which parts of leaves they eat, and this study examines potential cues and consequences of typical patterns of selection. Toughness and fiber content (NDF) were assessed for 13 of the major leaf-food species from samples collected in the spring of 1994. The toughness of the petiole, the midrib, and two parts of the lamina were tested separately. Petioles were generally the toughest part of the leaf, followed by the midribs. For both midrib and lamina, there was a positive correlation between toughness and fiber content, but the toughness of midribs was at least three times that of laminae at similar fiber contents. A clear relationship was found between the toughness of plant parts and whether or not they were eaten: no plant parts with a toughness greater than 2,300 J m⁻² were consumed even at low fiber levels. Toughness therefore explained food selection patterns much better than did fiber content. Toughness is likely to be assessed at the front of the mouth or during mastication. However, the macaques rarely reject leaves after placing them in the mouth. We suggest, therefore, that toughness may be used to select between feeding sites, rather than between individual leaves. © 1996 Wiley-Liss, Inc.     

Socioecological Context of Parturition in Wild Japanese Macaques (Macaca fuscata) on Yakushima Island

Female primates may adopt special feeding, foraging, and social strategies around the time of giving birth. We observed 8 females during the prepartum period, the day of birth, and the postpartum period in a wild troop of Japanese macaques (Macaca fuscata yakui) on Yakushima Island, Japan. We collected data on their activity budgets, quantitative feeding and foraging behavior, and on female-male interactions. On the day of birth, females spent less time moving and feeding, and more time resting relative to other periods. Overall dietary diversity as well as arthropod foraging also decreased on the day of birth. Females fed mostly on mature leaves, new leaves and shoots during prepartum periods but mostly on fruit during postpartum periods. Decreased feeding on leaves and increased feeding on fruit probably changed as a result of seasonal availability, independently of parturition. Feeding on flowers, fungi and other items remained constant over all periparturitional periods. On the day of birth, new mothers had fewer social interactions with males and spent more time out of proximity with other adults than in other periods. Females rejected grooming presentations from males, groomed less with males, spent less time 3 m of males, and received less aggression from males on the day of birth. In the postpartum period, interactions with males returned to prepartum values. Grooming with females did not differ across the three periods. These results suggest that interactions with males may be costly for females on the day of birth.     

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.     

Copulatory behavior unaccompanied by ovulation in the Japanese monkey (Macaca fuscata)

Copulatory behavior unrelated to conception is sometimes observed in some non-human primates including the Japanese monkey. In the present study, the authors examined whether a mature follicle or a newly formed fresh corpus luteum was observed in the ovaries of female Japanese monkeys which displayed the copulatory behavior unrelated to conception. Post-conception copulatory behaviors were observed in three out of four females usually kept in individual cages in an air-conditioned room, and in two out of three females without infants kept in an outdoor group cage. However, neither a mature Graafian follicle nor a fresh corpus luteum formed newly after conception was observed in any of these females by laparoscopic examinations conducted immediately after termination of the copulatory behavior. In females with infants born in the preceding birth season, copulatory behaviors were observed in three out of four females kept in the outdoor group cage, and in two out of four females in a free-ranging troop. Ovulation was confirmed in one case out of the three kept in the outdoor group cage, but neither a mature follicle nor a newly formed corpus luteum was observed in the remaining four females. These findings suggest that copulatory behavior in the Japanese monkey is not always controlled by the development of a follicle or ovulation in the ovary.     

Hematological analyses of the Japanese monkey (Macaca fuscata)

Various hematological examinations were performed on a total of 208 Japanese monkeys (Macaca fuscata). One hundred and fifty-eight of the monkeys were originally from different habitats in the western part of Japan, where they existed as free-ranging animals. The remaining 50 monkeys were kept in an open-enclosure for about one year. Laboratory examinations on blood specimens included the following; the erythrocyte and leukocyte counts, hemoglobin concentration, hematocrit, the specific gravity of the blood and plasma, protein concentration of the plasma, SGO-T, SGP-T, A/G ratio and the erythrocyte sedimentation rate. Results were similar to those reported for otherMacaca species. When the data reported here was compared with the known values for man, the Japanese monkey showed lower values for the erythrocyte count, hemoglobin concentration, hematocrit, and the specific gravity of the blood. Higher values were shown for the leukocyte count and SGO-T activity, with a wider overall range of variation.     

Clinical examinations of the Japanese monkey (Macaca fuscata)

Since 1962 clinical examinations have been performed on all 466 Japanese monkeys from the troops of the western part of Japan.During the external inspection we found a few cases of malformation of the hand and foot in some troops, but except for these they were in good physical condition, negative in tuberculin test and in Shigella and Salmonella infection.In all troops a high rate of helminthic infection was detected and there was a difference in the rate of occurrence of certain helminths betweenMacaca fuscata fuscata andM. fuscata yakui. No single case with the antibody to the B Virus was encountered, and it seems that no infection of the B Virus is present among the Japanese monkey.The free-ranging condition under which the Japanese monkey inhabits in troops seems to be satisfactory and they seem to have no serious problem of any kind at present.     

Male-female mating tactics and paternity of wild Japanese Macaques (Macaca fuscata yakui)

For Japanese macaques, visits by nontroop males (NTMs) often diminish the immediate copulation success of high-ranking males, although few studies have conducted a genetic analysis to show their contribution to the gene pool. I used noninvasively collected samples of semen, blood, urine and feces for the analysis of paternity in nine offspring born in two troops living on the island of Yakushima, Japan. I found that five of the nine offspring were sired by NTMs. It is argued that social change, small troop size and the timing of conception are all factors contributing to the NTM's reproductive success.     

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.