Aggressive intergroup encounters in two populations of Japanese macaques (Macaca fuscata)

It is predicted that variation in intergroup relationships in group living primates reflects the cost and benefit of resource defense. We tested the applicability of the model by examining population difference, group difference, and seasonal difference in behaviors during intergroup encounters in two populations of Japanese macaques (Macaca fuscata), one of six groups from Yakushima Island, and the other of three groups from Kinkazan Island. We found that the nature of intergroup encounter varied with group identity, reproductive seasonality, and population. Yakushima groups showed aggressive behaviors more frequently than did Kinkazan groups and the difference was consistent with the food competition model, both because of the involvement of females, and because home ranges were smaller on Yakushima than on Kinkazan, and thus more defensive. Both sexes of animals participated in aggressive interactions, but males were more aggressive than females. Furthermore, Yakushima population showed more agonistic intergroup behaviors during the mating season than the non-mating season. Also during the encounters, intergroup mating was observed, but only in Yakushima. It is concluded that intergroup relationships reflect the mate guarding behavior by group males. However, the agonistic relationship during non-mating season, especially that of among females, is also consistent with the food competition model. It is also noted that males' behavior toward other groups can also be interpreted as a form of investigative behavior before possible transfer into a new group.     

Effects of habitat differences on feeding behaviors of Japanese monkeys: Comparison between Yakushima and Kinkazan

Feeding behaviors of Japanese monkeys (Macaca fuscata) were compared between a warm temperate habitat (Yakushima Island: 30°N, 131°E) and a cool temperate habitat (Kinkazan Island: 38°N, 141°E). The composition of diet and the activity budget in the two habitats were very different. Time spent feeding on Kinkazan Island was 1.7 times that on Yakushima Island. Two factors seem to be responsible for these: (1) the energy required for thermoregulation of monkeys on Kinkazan Island is greater than that on Yakushima Island; and (2) the food quality, which affects the intake speed of available energy, is lower on Kinkazan Island. However, monkeys in both habitats increased their moving time and decreased their feeding time when they fed on foods of relatively high quality. Such foraging strategies are predicted by optimal foraging models. Time spent social grooming on Yakushima Island was 1.9 times that on Kinkazan Island, although there were slight seasonal changes in both areas. The difference in time spent social grooming might be explained by the overall difference in feeding time and day length between the two habitats.     

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.     

Variation in Intergroup Encounters in Two Populations of Japanese Macaques

The nature of intergroup encounters differed between two populations of wild Japanese macaques (Macaca fuscata): the Yakushima and Kinkazan populations. In the Yakushima population, intergroup encounters were more likely to result in the displacement of one group, intergroup agonistic interaction was common, and intergroup dominance was usually distinct. When displacement occurred at Yakushima, larger groups tended to dominate smaller ones. Conversely, in the Kinkazan population, intergroup encounters rarely resulted in displacement, intergroup agonistic interaction was rare, and intergroup dominance was usually unclear. Thus, monkeys in Yakushima appear to defend resources actively during encounters, while those in Kinkazan usually did not defend resources. The frequency of encounters was significantly higher in Yakushima than in Kinkazan. The two populations had very different group densities and traveling speeds, both of which directly influence the chance of encounters. Taking these differences into account, we compared the observed frequency with those predicted by the ideal gas model. The observed frequencies in both populations were about one-third of the number expected with the model, which suggests that the differences in encounter frequency were caused by differences in group density and traveling speed. We discuss this intraspecific variation in light of economic defendability in connection to habitat differences and the evolutionary significance of resource defense behavior.     

Reproduction of wild Japanese macaque females of Yakushima and Kinkazan Islands: A preliminary report

Wild Japanese macaque females of the Yakushima and Kinkazan populations exhibited similar reproductive features. (1) Births/female/year (BR: 0.27–0.35) was lower than those of provisioned troops, but (2) infant mortality (IM: 0.23–0.25) was higher than those of provisioned troops. (3) The interbirth interval (IBI) following the death of infants was 1.5–1.6 years, shorter than that following surviving infants (2.2–2.4 yrs). (4) Birth sex ratio (BSR) did not differ from 1∶1. There was no consistent correlation between (5) female age and IM, (6) maternal rank and offspring BSR, or (7) maternal rank and reproductive success. On the other hand, (8) BR of Yakushima females was significantly lower than that of Kinkazan females. In particular, (9) Yakushima females stopped reproduction earlier than Kinkazan females, although (10) the first birth of Yakushima females was about one year earlier than Kinkazan females. (11) BR exhibited a humped curve against female age in Yakushima, but it was uncertain whether old-aged females of Kinkazan exhibited a post-reproductive life span (PRLS). (12) The survivorship for female juveniles was lower than that for male juveniles in Yakushima, whereas the survivorship for male juveniles was lower than that for female juveniles in Kinkazan. These data may indicate that Yakushima females more severely compete for resources than Kinkazan females, because of high population density, whereas the population density of Kinkazan might be limited by climate (e.g. heavy snow) rather than density dependent ecological effects.     

Home range structure and inter-group competition for land of Japanese macaques in evergreen and deciduous forests

The per capita home range area of Japanese macaques,Macaca fuscata, is significantly smaller in evergreen forest than in deciduous forest, though a corresponding difference in food resource utilization patterns has never been described. The present study compared the home range utilization pattern of Japanese macaques living in two habitats: the Yakushima population inhabits an evergreen forest, while the Kinkazan population inhabits a deciduous forest. We found that in the Yakushima population, (1) food density was higher; (2) inter-feeding bout sites distance was shorter; (3) daily travel distance was shorter; (4) home range size was smaller; and (5) the unit value of the main home range was higher, than in the Kinkazan population. Yakushima groups utilized a small home range area intensively, compared to Kinkazan groups. We also found that a Yakushima group shared 24% of its main home range with neighboring groups, though a Kinkazan group shared only 10% with other groups. It is supposed that food distribution affects daily ranging pattern, and ultimately the social relationships between groups in Japanese macaques.     

Does troop size of wild Japanese macaques influence birth rate and infant mortality in the absence of predators?

For the wild Japanese macaques of Yakushima and Kinkazan Islands, we analyzed the relationship between the troop size or the number of adult females of each troop, infant/adult female ratio (IFR; crude birth rate), and infant mortality (IM) in habitats with no predators. In Yakushima, IFR was positively correlated to troop size and the number of adult females. In Kinkazan, however, IFR tended to decrease with the number of adult females. This difference may be due to the difference in troop size; i.e. in Yakushima, where troop size was small, IFR may increase with that of troop size, because a relatively larger troop is likely to the advantage in intertroop competition. In Kinkazan, where troop size was large, however, IFR is likely to decrease with troop size, because intratroop competition may increase. Thus, the present data roughly supportWrangham's model of the social structure of female-bonded primates, and suggests that there is an optimal troop size for birth rate (BR). On the other hand, there was no clear correlation between IM and the troop size or number of adult females of each troop.     

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.     

Inter-annual variation of reproductive parameters and fruit availability in two populations of Japanese macaques

Among wild Japanese macaques, which have clear reproductive seasonality, correspondence between fruit-food production in the mating season and birth rate in the following year was confirmed in two different habitats. One of the study areas was evergreen broad leaved forest on Yakushima Island, for which demographic and fruiting data for seven years were used. The other was a deciduous-coniferous mixed forest on Kinkazan Island in the cool temperate zone, for which 11 years of data were used. From the fruit-crop data, each year was classified as a good or bad fruiting year for each population. At both habitats, female macaques had fewer babies after bad fruiting years than after good fruiting years. In Yakushima, small troops had a lower birth rate than large troops and this tendency was clear after bad fruiting but not after good fruiting. On the other hand, in Kinkazan such differences due to troop size were not found. These findings were consistent with the observation that intertroop encounters occur more often and are more agonistic in Yakushima than in Kinkazan and large troops tend to be dominant to small troops in the Yakushima population. Thus annual fluctuations in fruit production appear to increase the difference in birth rates between troops of different sizes through intertroop competition in Yakushima, but not in Kinkazan.     

Costs of Mate Guarding and Opportunistic Mating Among Wild Male Japanese Macaques

A trade-off relationship between mating and feeding effort is important when considering reproductive strategies of long-lived species. I compared the influence of male sexual activities, female mate-choice behaviors and the daily activity budget on male mating success among males in a group of wild Japanese macaques (Macaca fuscata yakui) on Yakushima Island. The 1st-ranking male, which had immigrated into the troop at this rank, more frequently approached peri-ovulatory females, spent more time grooming peri-ovulatory females and in mounting series and spent less time feeding than subordinate males did. The 1st-ranking male attained the highest mating success as a result of his high expenditure of time and energy in sexual behaviors directed toward peri-ovulatory females. Mating success of subordinate males did not relate to the amount of sexual effort, but instead to the frequency of female approaches, female rush toward males and the number of peri-ovulatory females within the group. The pattern of intermale competition shifted from nearly contest competition to scramble competition as the number of peri-ovulatory females in the group increased. Feeding time of subordinate males did not vary between the days when they copulated and the days when they did not. The findings demonstrate that mate guarding in the 1st-ranking male is a high-cost mating tactic, while opportunistic mating in subordinate males is a low-cost mating tactic. The differences in male mating tactics are probably related to male life history and to the formation of groups with a high socionomic sex ratio.     

The Association of Intergroup Encounters,Dominance Status,and Fecal Androgen and Glucocorticoid Profiles in Wild Male White‐Faced Capuchins (Cebus capucinus)

Androgens play a role in male reproductive competition, frequently via aggression, while glucocorticoids are associated with the stress response. However, the relationships of these hormones with different sources of competition (intra‐ vs. intergroup) and dominance status are highly variable. Here, we consider the fecal androgen (fA) and glucocorticoid (fGC) profiles of alpha and subordinate male Cebus capucinus in the context of intergroup competition during a rare period of low intragroup competition (i.e. all females were either pregnant or lactating). Intergroup encounters (IGEs) are a long‐term reproductive strategy in male white‐faced capuchins, enabling them to assess the composition of neighboring groups. IGEs pose a threat to resident males as these can result in injury or death, loss of dominance rank, group eviction, and group takeovers that are frequently associated with infanticide. From February to July 2007, fecal samples were collected from eight males in three groups of white‐faced capuchins in the Santa Rosa Sector of the Área de Conservación Guanacaste, Costa Rica. IGE rate was positively associated with both fA and fGC levels, indicating that IGEs are perceived as reproductive challenges by resident males, and may be associated with elevated metabolic costs. Alpha males sire the majority of group offspring and, accordingly, the threat of IGEs to both future (via rank loss or eviction) and current (via infanticide) reproductive success is greater than for subordinate males. Consistent with this observation, alpha males had higher fA and fGC levels than subordinate males. Given that all females were either pregnant or lactating and pronounced overt intragroup competition was absent, we interpret the difference in hormone profiles of alpha and subordinate males as being primarily associated with variation in the perceived threats of IGEs according to dominance status. Future studies should focus on the interaction of intra‐ and intergroup competition by examining hormone levels in the presence of periovulatory females. Am. J. Primatol. 75:107‐115, 2013. © 2012 Wiley Periodicals, Inc.     

Effects of caller activity and habitat visibility on contact call rate of wild Japanese macaques (Macaca fuscata)

A major function of contact calls in nonhuman primates is to maintain spatial cohesion among individuals in a group. The risks of spatial/visual separation from the group are likely to affect auditory contact behavior, in particular by increasing the call rate. We tested whether the risk of separation influences coo call emission by investigating the variation in call rate among behavioral contexts in two wild populations of Japanese macaques (Macaca fuscata). We focused on caller activity and the degree of visibility within the habitat as primary potential factors mediating call rate. We first estimated the habitat visibility of the two research sites at Yakushima Island (YK) and Kinkazan Island (KZ), Japan. The habitat visibility of YK was significantly more restricted than that of KZ. We then compared the call rate of 20 adult and 12 juvenile female macaques between the two wild populations to examine the potential effects of environmental differences. Both populations had a lower call rate during grooming than during feeding and moving, which are behaviors associated to higher interindividual distances. The call rate of YK adult females was significantly greater than that of both juveniles and KZ adult females, independently of activity. The call rate increased as macaques matured in the YK population, but not in the KZ population, suggesting that different developmental processes involved in contact calling of the two populations. Our findings suggest that separation risk influences call rate, and also imply a possibility of social influence that social structure change effects on the call rates.     

Postconflict Behavior Among Male Japanese Macaques

Reconciliation was first described more than 20 years ago. Since then, it has been observed in many mammals (mainly primates) but data on postconflict behavior among males are still scarce because they usually aggressively compete for mating partners, rarely maintain amicable relationships with one another. Accordingly, reconciliation is expected to occur at low rates. Although this is true for Japanese macaque males, the subspecies on Yakushima Island (Macaca fuscata yakui) seems to represent an exception as grooming among males occurs often. We analyzed postconflict behavior among them and discuss the possible factors that may favor the occurrence of grooming and reconciliation. Selective attraction between former opponents—reconciliation—occurred soon after conflicts. Consolation—affiliative interactions between a focal animal and group members other than the former opponents occurring earlier in PCs than in MCs—was absent among males. Conciliatory tendency is higher for Yakushima macaque males (0.31) versus that in studies on the other subspecies Macaca fuscata. We discuss differences in the behavioral ecology of the 2 subspecies, the ecological and social factors that may favor the occurrence of reconciliation, and the possible benefits that males gain from grooming exchange and reconciliation.     

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.     

Even adult sex ratios in lemurs: Potential costs and benefits of subordinate males in Verreaux's sifaka (Propithecus verreauxi) in the Kirindy Forest CFPF,Madagascar

Optimal group size and composition are determined by both the costs and benefits of group living for the group's members. Verreaux's sifakas (Propithecus verreauxi), a diurnal lemur, form multimale multifemale groups with the tendency toward even adult sex ratios despite a small average number of females per group. The unexpected presence of multiple adult males may be explained by tolerance of other group members if subordinate males provide benefits to the group that outweigh the costs associated with their presence. Results based on both demographic data collected over a 13‐year period and behavioral observations suggest that subordinate males provide no benefits in terms of infant survival and defense against group takeover by outside males. Although groups with more males are more likely to win intergroup encounters, subordinate males do not participate in these encounters more often than expected. Subordinate males are not costly to other group members in terms of direct intragroup feeding competition, but aggression rates between dominant and immigrated subordinate males increase in the mating season. Even though subordinate males provide very few benefits to the group, they are not very costly either and thus may be tolerated by resident females and dominant males. This tolerance may help to partially explain the tendency towards their unusual adult sex ratio. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

Grooming Between Male Chimpanzees at Ngogo,Kibale National Park. II. Influence of Male Rank and Possible Competition for Partners

Allogrooming contributes to the development and maintenance of social relationships, including those that involve alliances, in many primate species. Variation in relatedness, dominance rank, and other factors can produce variation in the value of others as grooming partners. Several models have been developed to account for variation in the distribution of grooming in relation to dominance ranks. These start from the premise that individuals are attracted to high-ranking partners, but time limits, direct competition, and prior grooming engagement between high-ranking individuals can constrain access to them. Sambrook et al. (1995) formalized some of these models and showed the importance of taking group size variation into account when assessing them. Chimpanzees form multimale communities in which males are the philopatric sex. Males commonly associate and groom with each other; they also form dominance hierarchies and form alliances that influence dominance ranks and mating success. Both male rank and the rank distance between partners are significantly correlated with the distribution of grooming between males in an extremely large chimpanzee community at Ngogo, Kibale National Park, Uganda, that has more males than any other known community. High-ranking males had more grooming partners than mid- or low-ranking males. Grooming predominantly went up the dominance hierarchy, but was also concentrated among males that were close in rank. Rank and rank distance apparently both affected grooming independently of reciprocity in grooming and independently of the frequency with which males associated in temporary parties. However, the data do not clearly indicate how constraints on access to partners might have operated. Published data from a smaller chimpanzee community at Mahale show no rank or rank distance effect on male grooming. These results and earlier, conflicting findings on the association between dominance rank and grooming in male chimpanzees indicate that variation in group size, i.e., the number of males per community, probably influences the strength of any such effects, as happens for grooming between females in several cercopithecine species. Data on coalitions at Ngogo support the argument that high-ranking males are valuable social partners, and similarity in strategies of alliance formation may influence the distribution of grooming.     

Intragroup cohesion and intergroup hostility: the relation between grooming distributions and intergroup competition among female primates

In some primate species, females interact affinitively withmany related and unrelated females, whereas in other speciesfemales interact with only a small subset of available partners.One explanation for high rates of affinitive interactions amongfemale members of the same group is that they function to maintainthe group's cohesion in competition for resources against othergroups. Here, I attempt to determine if grooming is more "egalitarian"or diverse in groups that compete aggressively with their neighborsthan in groups in which females rarely take an active role inbetween-group competition. Three types of data are considered.The first concerns grooming and intergroup encounters in onepopulation of free-ranging vervet monkeys. The second concernsgrooming interactions in a captive population of vervets beforeand after females in adjacent cages began to respond aggressivelyto one another. The third involves a literature survey of avariety of species. When only female-bonded species are considered,there is no relation between the diversity of grooming withingroups and female participationin intergroup encounters. Therealso appears to be no clear relation between the strength ofthe female dominance hierarchy and the diversity of groomingamong females. Female-bonded groups are apparently composedof subgroups allied in a loose confederation against other groups.Female members of the same group may compete against other groupsas a cohesive unit, but their grooming relationships are oftensharply differentiated.     

Comparison of energy balance between two different-sized groups of Japanese macaques (<Emphasis Type="Italic">Macaca fuscata yakui</Emphasis>)

Quantifying the energy balance is essential for testing socio-ecological models. To reveal costs and benefits of group living in Japanese macaques from the perspective of feeding competition, Kurihara and Hanya (Am J Primatol 77:986–1000, 2015) previously compared feeding behavior between two different-sized groups of macaques (larger group 30–35 individuals; smaller group 13–15 individuals) in the coastal forest of Yakushima, Japan. The results suggested that the larger group exhibited greater feeding effort because of intragroup scramble competition and that the smaller group suffered from higher travel costs, possibly owing to intergroup contest competition. However, it remained unclear whether the behavioral differences affected their energy budgets. The present study examined energetic consequences of the different feeding behaviors in the two groups. Using behavioral data from 10 to 13 adult females and nutritional composition of food items, we compared ingestion rates, energetic/nutritional content of diet, and energy budgets between the two groups. Ingestion rates and energetic/nutritional content of diet did not differ between the two groups. Despite the higher feeding effort of the larger group, energy intake did not differ between the two groups. Energy expenditure did not differ between the two groups because higher travel costs were negated by lower feeding effort in the smaller group. Consequently, the energy balance did not differ between the two groups. We demonstrated that the behavioral measures of feeding competition were not translated into their energetic condition; moreover, our findings re-emphasize the importance of quantifying behavioral and fitness measures for interpreting variation in feeding behavior properly.     

Time, gender, and seasonality in vervet activity: A chronobiological approach

A chronobiological approach has been used to highlight the issue of how climatic factors and breeding seasonality may affect male and female diurnal activity budget. We investigated gender differences for vervet monkeys in the diurnal distribution of feeding, locomotion, inactivity, and social grooming within and between birth, pre-mating, and mating seasons. The main climatic traits were that days were shorter, drier, and cooler in the mating season. Non-parametric statistics showed that female activities changed with time of day to a greater extent than did male activities. When the constraints imposed by climatic factors and mate competition increased, from the birth to the mating season, male maintenance activities were more independent of the time of day whereas females continued to vary. Gender differences in timing were therefore greater in the mating season, except for social grooming; males and females were more coordinated in diurnal timing of their grooming in the mating season. It is argued that these changes may result in reduced levels of male-female contest competition, and may be related to higher levels of male-female socialization in the mating season. Finally, it is inferred that an out-of-phase synchronization between inactivity and feeding for males in the birth season, and for females in the mating season, may result from each sex investing more time feeding at the expense of resting in those periods.     

Effect of Dominance,Reproductive State,and Group Size on Body Mass in Macaca radiata

Body mass can impact reproductive performance in males and females. In nonhuman primates the relationship is often mediated by dominance. We measured body mass monthly in a provisioned group of bonnet macaques (Macaca radiata) living at a Hindu temple. We also measured body mass on 3 occasions in a wild population of bonnet macaques. In the temple group, females that reproduced lost body mass, while females that did not reproduce gained body mass. Mass loss among females occurred primarily while they were nursing. Adult males from the temple group lost mass during the mating season and gained it during the non-mating season. Subadult males experienced less seasonal variation in body mass. Body mass and changes in mass were not related to dominance rank in either the temple or the forest group. Furthermore, maternal dominance rank did not affect infant mass. Females from the smallest forest group weighed significantly less than females from the two larger forest groups, which suggests intergroup competition in the population. Body mass was not related to dominance rank in a straightforward manner but may indirectly affect reproductive performance. The pattern of body mass change suggests that the period of lactation is critical for females and endurance rivalry is an important form of competition among males.