Probability of paternity exclusion and the number of loci needed to determine the fathers in a troop of macaques

We calculated the probability of paternity exclusion (P) in 6 troops of rhesus and Japanese macaques housed in open enclosures and 68 wild troops of Japanese, crab-eating, and toque macaques using 33 genetic loci which encoded the blood protein variations detected by electrophoretic techniques. In the open enclosures, especially of rhesus troops, we obtained a fairly high probability of paternity exclusion and succeeded in determining the fathers of offspring. However, we found significant differences between the observed and calculated probabilities in most of the troops. These differences were ascribed to a situation whereby the Hardy-Weinberg equilibrium had not been attained in the troops and/or the numbers of variable loci were too small. In the wild troops of Japanese, crab-eating, and toque macaques, the means ofP were 0.2274 (0.0192–0.5017), 0.4635 (0.1676–0.7151), and 0.7382 (0.6266–0.7954), respectively. We also estimated the number of loci needed to determine the fathers of offspring with a probability of 0.8 assuming that ten males were present in the troop. The estimated number was about 13.5 times, 5 times and 1.8 times the number of loci examined on average in the troops of Japanese, crab-eating and toque macaques, respectively. This means that determination of most of the fathers of offspring in wild troops of these macaques, even of toque macaques which have a rather high probability of paternity exclusion, is difficult so long as we employ only electrophoretic techniques.     

Mass mortality of Japanese macaques in a western coastal forest of Yakushima

The mass mortality of wild Japanese macaques (Macaca fuscata Blyth) was observed in a warm temperate forest of Yakushima, southern Japan. Demographic changes of eight troops between August 1998 and August 1999 were studied and 56% of macaques disappeared from the five intensively studied troops. Mortality varied among troops: two troops became extinct, while another troop did not decrease in size. The rate of mortality of the other troops was between 33 and 80%. The variation in mortality among the troops was either the outcome of local concentrations of mortality or of intertroop competition. The rate of mortality decreased with increasing distance from the two extinct troops and with increasing troop size; these two factors could not be separated statistically. The direct cause of death was diagnosed as pneumonia for four out of five fresh carcasses. The fleshy fruit production in autumn 1998 was the lowest in 14years, and macaques had relied on leaves earlier than in usual years. It was exceptionally hot and dry in the summer of 1998. The exceptionally poor fruit production and hot summer of this year, with the resulting shortage of high-quality foods, was consistent with the scenario that mass mortality was due to the poor nutritional conditions. However, the possibility that epidemics caused the mass mortality cannot be ruled out. Our findings proved that primates in a seemingly stable habitat experience fluctuations in demographic parameters under natural conditions.     

Symmetrical patterns in non-agonistic social interactions found in unprovisioned Japanese macaques

Non-agonistic social interactions in an unprovisioned troop of Japanese macaques (Macaca fuscata yakui) were analyzed with the spacing between individuals, leading-following interactions, and exchange of social grooming. The most frequent interactions were found between kin-related females. Unrelated females stayed with one another rather frequently, but rarely exchanged social behaviors. Interactions between males and females were infrequent though they were occasionaly observed between high-ranking males and high-ranking females. Very frequent exchange of grooming was observed between males, and even high-ranking males exchanged grooming more frequently with males than with females. Most non-agonistic social interactions in the study troop were based on bidirectional exchange of social behaviors, in which no clear tendency relevant to dominance or sex was found; while in provisioned Japanese macaque troops, associations between males and females, between unrelated females, and between males were formed mainly be subordinates' active roles in associative behaviors. This seems relevant to the idea that dominance grealty influence social life in provisioned troops. The present study provides guidelines for interspecific comparison of social interaction patterns of macaque species.     

Hb Izu (Macaca)β83 (EF 7) Gly→Cys: The major hemoglobin of the Japanese monkey (Macaca fuscata) in a troop at Shimokita,the northernmost limit of its habitat

A hemoglobin variant was discovered in Japanese monkeys (Macaca fuscata) of the Wakinosawa A-1 troop of the Shimokita peninsula, the northernmost limit of this species' habitat. The variant was characterized by slow migration on starch gel electrophoresis due to its polymerizing nature. Structural analysis revealed that Gly at the 83rd amino acid residue of theβ chain was substituted by Cys, and the variant was identified as Hb Izu (Macaca). The gene frequency of the variant was extremely high, at 85.7%, and much higher than the 21.3% obtained for the troops of the Izu peninsula. The genotypic frequencies in the troops of both the Izu and Shimokita peninsulas agreed with expectations as calculated from the Hardy-Weinberg equilibrium.     

Regional differences in the infection of wild Japanese macaques by gastrointestinal helminth parasites

A coprological survey of gastrointestinal parasites in wild Japanese macaques (Macaca fuscata), from 14 natural habitats was done. Ova of five nematode species (Trichuris trichiura, Strongyloides fuelleborni, Streptopharagus pigmentatus, Oesophagostomum aculeatum, andGongylonema species) and a worm of the cestode species,Bertiella studieri, were detected. Some differences found in rates of infection by sex were observed in the 14 areas. Differences based on age were found in only troops in which the infection rates ofStrongyloides fuelleborni, Streptopharagus pigmentatus, andTrichuris trichiura were higher in the juvenile monkeys. The number of parasite species was related to the geographical and climatic conditions of the habitat of the troop: troops living in areas cold in winter were infected by fewer parasite species than those in southern warmer areas.     

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 distance mobility of male Japanese macaques evidenced by mitochondrial DNA

A 487-nucleotide sequence in the polymorphic D-loop region of matrilineally inherited mitochondrial DNA was compared in samples from 14 (9 adult males and 5 females or young) Japanese macaques (Macaca fuscata fuscata) of two troops at Gagyusan in Takahashi City, Okayama Prefecture, Japan. The majority (7 out of the sampled 9) of the adult males associated with the troops had nucleotide sequences of six distinct types, all of which were different from that of the Gagyusan troop females, whereas two young solitary males shared the same sequence. The present study exemplified a case in which the majority of adult males immigrated from outside the local population. Notably, two of the males were revealed to share the same sequence determined for a matriline 45 km away. Electronic Publication     

Habitual fission-fusion and social organization of the Hakone troop T of Japanese macaques in Kanagawa prefecture,Japan

To analyze the socioecological factors of habitual fission-fusion of troop members, which is an underreported phenomenon in Japanese macaques, the seasonal pattern of fission-fusion within the Hakone troop T in Kanagawa Prefecture, Japan, was examined. Although almost all the study troop members were included in a large-sized group in winter, a portion of its members of ten formed small subgroups from spring to autumn. The frequencies and age-sex composition of these subgroups changed seasonally. All troop members participated, more or less, in subgroup formation. Subgroups tended to be composed of animals of the same age-sex class. Troop members did not fission along matrilineal lines. Although the study troop members repeatedly joined with and parted from subgroups, the characteristic social structure of Japanese macaque troops was maintained. Habitual fission-fusion among troop members may be one of a number of foraging strategies that facilitate efficient food gathering when the population density exceeds and /or reaches the carrying capacity of the area. The seasonal variation of pattern and composition type of each subgroup could be attributed to alternation of attractive food plant species, as well as age, rank, and sexual activity of both sexes.     

Elemental hair analysis of Japanese macaques transplanted to the United States

One of the world’s best studied troops of Japanese macaques (Macaca fuscata) was captured intact at Arashiyama, Japan and transplanted to a brushland savannah area near Laredo, Texas, in 1972. The transplantation provided a unique opportunity to study the biological responses of this troop to a drastically different environment than the one in which it evolved. We investigated one biological response, the metabolism of nutrient, and non-nutrient elements, by neutron activation analysis (NAA) of hair from 88 of the transplanted monkeys nine months after transplantation. Many of the elements mammals metabolize are deposited in hair. Hair analysis is therefore a measure of these elements the mammal encounters in its environment. Hair concentration of S and Cl were found to increase with animal age at the 95% confidence level, and hair concentrations of Hg, Se, and I were found to decrease with animal age at the 95% confidence level. Male hair had more Zn and less Se than female hair at the 95% confidence level. Comparison of this information with similar information on the sister troop in Japan and on other troops will provide some indication of the homeostatic ability of this primate species to cope with different exposure regimes of certain elements. Such information is of general interest where pollution and other cultural activities are changing environmental levels of many elements.     

Effects of vegetation type on habitat use by crop-raiding Japanese macaques during a food-scarce season

Habitat use by crop-raiding Japanese macaques (Macaca fuscata) was studied in western Japan from December 2005 to February 2006, a food-scarce season. To examine how different vegetation types affect habitat use by monkeys, two crop-raiding troops were compared: the first troop inhabited a habitat involving more wild food resources; the second troop inhabited a habitat providing fewer wild food resources. It was hypothesized that monkeys living in the habitat with fewer wild food resources are more likely to utilize human settlements and areas around them (i.e. adjacent zones), with a dependence on crop foods. Comparisons of observed and expected habitat use frequencies showed that the first troop selected evergreen broad-leaved forests and conifer plantations, and avoided adjacent zones, rice fields, and golf courses. The second troop selected adjacent zones and avoided conifer plantations, pine forests, and deciduous broad-leaved forests. Both troops moved rapidly in avoided habitat types. These results suggest that monkeys living in the habitat with fewer wild food resources are more likely to utilize areas around human settlements during a food-scarce season.     

Birth-season variation in Japanese macaques,<Emphasis Type="Italic"> Macaca fuscata</Emphasis>

Japanese macaques, Macaca fuscata, exhibit an annual reproductive cycle that apparently is maintained intrinsically. Translocation of nine troops to new latitudes within the northern hemisphere has had minimal effect on the timing of birth seasonality in these troops; translocation of one troop to the southern hemisphere has resulted in a 6-month forward displacement of birth seasonality in this troop. Limited available evidence indicates that, in the latitudinal zone between Toimisaki (31°22′N) and Kinkazan (38°17′N), mean birth date in in-situ troops becomes earlier as latitude of troop localities increases; the same relationship between mean birth date and latitude apparently does not apply to in-situ troops south and north of the Toimisaki–Kinkazan latitudinal zone. Within the Toimisaki–Kinkazan latitudinal zone, earlier mean birth dates at higher latitudes may permit infants to achieve an adequate level of development before the earlier onset of poor winter food conditions. South of the Toimisaki–Kinkazan latitudinal zone, winters are relatively mild and may be less of a factor in infant survival; north of this zone, poor winter food conditions persist so long that earlier infant births may be maladaptive. Electronic Publication     

Genetic polymorphism of blood proteins in the troops of Japanese macaques,Macaca fuscata: II. Erythrocyte lactate dehydrogenase polymorphism inMacaca fuscata

In investigating the genetic marker for population genetics of Japanese macaques by electrophoresis, the author found the erythrocyte lacate dehydrogenase (LDH) polymorphism existing in some troops. There were four kinds of variations which seemed to be controlled by two loci, controlling A and B subunits of this enzyme. The variant phenotypes were named LDH-A_mac2-1 LDH-B_mac1-1, LDH-A_mac3-1 LDH-B_mac1-1, LDH-A_mac 1-1 LDH-B_mac2-1, and LDH-A_mac1-1 LDH-B_mac2-2. The two former types seemed to be heterozygote of a mutation controlling subunit A; the third was heterozygote, and the last homozygote, a mutation controlling subunit B. LDH-A_mac2-1 LDH-B_mac1-1 was found in Takasakiyama A, Takasakiyama B, Takasakiyama C, and Kamae troops; LDH-A_mac3-1 LDH-B_mac1-1 was in an individual of the unknown group. LDH-A_mac1-1 LDH-B_mac2-1 and LDH-A_mac1-1 LDH-B_mac2-2 were found in the Kohchi troop. All other troops were found to be monomorphic.     

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.     

Life history variables of wild troops of formosan macaques (Macaca cyclopis) in Kenting,Taiwan

A study on population dynamics of wild Formosan macaques (Macaca cyclopis) in Kenting, southern Taiwan, was conducted from March 1985 to August 1990. At first, only one monkey troop was studied. It fissioned in 1987 and both of the daughter troops have been observed since then. Total number of animals increased from 10 to 29 over the years, but the sizes of individual troops have never been more than 20. Seasonality in breeding has been detected: copulations were concentrated in the period from November to January and 75% of all the 28 births occurred between April and June. Time of birth by parous females without offspring from the preceding year was earlier than that of lactating females. Young females gave their first births at 4 or 5 years of age. Total birth rate over the study period was 0.8 infant per female per year. Hunting was the main cause of death while natural mortality rate was low for the animals. There was only one adult male in each troop for most of the time. Troop males in the two daughter troops have been replaced two or three times in the three years by some solitary males that moved around in the area. The reproductive parameters of Formosan macaques in Kenting were found to be more similar to that of rhesus monkeys than to Japanese macaques. And a case of higher reproductive success in a high-ranking matriline was reported.     

Life history and male intertroop mobility among Japanese macaques (Macaca fuscata)

Male intertroop transfer among Japanese macaques (Macaca fuscata) often coincides with the mating season. However, no necessary connection exists between mating by newly arrived males and whether they join a troop—visitors often mate, and males that join troops may show little mating success. On the other hand, intertroop transfer often coincides with major events in the developmental and social life history of males, such as the attainment of sexual maturity and full adult body size or rise in dominance rank. Thus, intertroop transfer may reflect age-specific behavioral patterns in which males maintain a position in the age-rank structure of troops, where the rank acquired in a new troop is partially determined by age.     

Dominance style of Japanese macaques compared with rhesus and stumptail macaques

In the present study, we seek to relate dominance style with group cohesion in a captive group of Japanese macaques (Macaca fuscata). Social data were gathered on approach rate, result, and direction, aggression rate and intensity, grooming rate and direction, and conciliatory tendency. Data were collected using focal animal sampling and instantaneous scan sampling. Reconciliation data were collected using ad libitum observations of aggression with ten-minute post-conflict and matched-control focal observations. Data were compared to prior studies on rhesus (M. mulatta) and stumptail macaques (M. arctoides) living in similar environments. Each species demonstrated the presence of a formalized dominance hierarchy based on the teeth-baring display. The Japanese macaque group showed a lower rate of approach with a higher proportion of negative outcomes than either of the other species. Rates of aggression and reconciliation were also lower in the study troop, suggesting a strict hierarchy while maintaining an optimal nearest-neighbor distance. Overall, this group of Japanese macaques was less sociable than other groups of the same species, perhaps due to a history of individual removals. © 1995 Wiley-Liss, Inc.     

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.     

Plasma cholesterol levels in free-ranging macaques compared with captive macaques and humans

Plasma total cholesterol in free-ranging Japanese macaques (Macaca fuscata) on Koshima islet and in free-ranging long-tailed macaques (Macaca fascicularis) at Pangandaran in Indonesia was found to occur at very low levels compared with captive macaques and humans. Although total cholesterol levels in captive macaques were lower than humans, differences in HDL cholesterol levels were only small. In both sexes of wild and captive Japanese macaques, total cholesterol levels decreased from birth through to young adulthood but then increased in adult females of the captive group. In contrast, the value for adult females of the wild troop remained at a low level. Low TCH levels in adult females of the wild Japanese macaque troop may be due to a low energy intake and may have caused a delay in the onset of sexual maturation. Plasma TCH levels increased with the addition of 0.1% dietary cholesterol over six weeks in captive long-tailed macaques. That the cholesterol value after six weeks was dependent on cholesterol levels prior to supplementation indicates that captive macaques are slightly saturated with cholesterol.     

Frog- and lizard-eating behaviour of wild Japanese macaques in Yakushima,Japan

Frog- and lizard-eating and related behaviours were observed on eight occasions in two troops of wild Japanese macaques (Macaca fuscata yakui) in Yakushima, between March 1984 and April 1989. In each case, the first animal seen handling the prey was an adult. Juveniles showed interest in the prey, sniffed or mouthed it in three cases, and ate discarded parts of it in another. In the three cases where capture was observed, detection of the prey appeared to be fortuitous. Four monkeys ate leaves after eating meat. Those leaves identified were of species not commonly eaten. Though invertebrate-eating is common and widespread among Japanese macaques, the consumption of vertebrates is rare. The possibility that these behaviours represent a local tradition among the Yakushima macaques is discussed.     

Outcast males and social structure among bonnet macaques (Macaca radiata)

Outcast males are a regular feature of rhesus (Macaca mulatta) and Japanese (M. fuscata) macaque societies but are rare among bonnet macaques (M. radiata). Apparently bonnets have other solutions than ostracism for their social problems. For example, in many troops the male-female ratio ranges from 0.7?1.0+; and, as the young adult males grow to full social and physical maturity, they remain in the troop and participate actively in social relationships. A few troops of bonnet macaques, however, have a network of social relationships which prevents the young males from being integrated into the social system; in some of these cases, male isolation occurs. A comparison of the social relations between males in bonnet macaque societies of both types suggests that societies with strong male-male bonds accommodate their growing males better than those with highly individual males.