Development of intervention behavior in Japanese macaques: Testing the targeting hypothesis

Matrilineal dominance systems, which characterize several species of cercopithecines, are determined largely by the patterning of third-party aggressive interventions in conflicts. Although the role of interventions in structuring rank relations has received much attention, very few studies have dealt specifically with the development of intervention behavior. In other words,most studies have focused on the interventions received and their effect on the recipients rather than on the interventions performed and the goals of the interveners. We analyzed the intervention behavior of 10 juvenile females in a colony of 40 Japanese macaques (Macaca fuscata)housed at the University of Montreal Laboratory of Behavioral Primatology. The analysis of 749 interventions performed by the juveniles over their first 4 years and 2425 interventions received over the same period reveals that (1) juvenile females intervened selectively against females ranking below their mother, (2) they began to intervene at about the same time that they began to challenge the latter females in dyadic contests, (3) they sided with females as well as with males against these females, (4) juvenile interveners incurred little risks in terms of aggressive retaliation from their targets, (5) they derived immediate benefits in terms of conflicts won over stronger targets, (6) interventions often did not take place when the possible recipients needed support, and (7) interveners did not conform to a pattern of mutually preferential support. These results support the view that interventions by juveniles are selfish (vs altruistic) and constitute a low-cost and effective means to target and to outrank prospectively subordinate females.     

Skewed sex ratios and female homosexual activity in Japanese macaques: An experimental analysis

In this paper we present the results of a behavioral experiment conducted to test whether homosexual consortships and sexual solicitations among female Japanese macaques (Macaca fuscata) increase in the context of operational sex ratios that are heavily skewed towards females. The study involved a baseline period of observation on an intact social group which had a female-biased sex ratio typical of this species. During the experimental period which followed, we created a sub-group with an operational sex ratio that was heavily skewed towards females. Compared to the baseline period, females solicited significantly more same-sex individuals for sex and formed significantly more homosexual consortships during the experimental period of the study. Females did not appear to engage in homosexual activity during the study's experimental period simply because they lacked heterosexual alternatives. Instead, we suggest that an abundance of certain types of preferred, same-sex sexual partners and/or a scarcity of opposite-sex sexual competitors best account for the increased levels of female homosexual behavior observed at this time.     

Patterns of dominance and affiliation in wild pig-tailed macaques (Macaca nemestrina nemestrina) in West Sumatra

Patterns of agonistic and nonagonistic behaviors were studied in a troop of wild pig-tailed macaques in West Sumatra, Indonesia. The animals were provisioned and the identities of all adult and adolescent individuals were known. The females could be divided into high-, mid-, and low-ranking subsets of individuals. Most grooming occurred within, instead of between members of these subsets. The members of each subset also tended to feed together at the baiting sites, and they probably represented groups of close kin. Among females, grooming appeared to be a conciliatory behavior and was generally performed by the subordinate partner, while mounting was performed by the dominant partner and appeared to be a reassertion of dominance. High-ranking males tended to form agonistic alliances with females and to exchange grooming with estrous females. Low-ranking males did not have such associations with females and were frequently the targets of agonistic alliances of females and juveniles. Mounting between males appeared to be a conciliatory behavior. It seemed effective since severe aggression between males was not observed. The subordinate partner mounted more frequently than the dominant one, but the direction of mounting was apparently controlled by the latter. This suggests that, among pig-tailed macaques, the dominant male plays an important role in the coexistence of males in the troop.     

Dominance in assamese macaques (Macaca assamensis)

A field study of 64 assamese macaques (Macaca assamensis) was conducted at a temple site in Assam, India. Focal and all occurrence scan techniques were used to collect data on agonistic, grooming, and sexual behavior. More than 1,000 hr of data were summarized into agonistic dominance, grooming, and mounting matrices. Rank hierarchies were constructed for all three and compared. We also directly compared each cell in each matrix with the corresponding cells in the other matrices. A nearly linear agonistic dominance hierarchy was found, but it did not correlate with the directionality of mounting or grooming. Adult males mounted females, generally were dominant to females and groomed females more often than they were groomed by females. Younger males groomed older males and were also generally subordinate to older males. These age and sex effects produced some inter‐correlations among grooming, mounting, and dominance but only for specific age‐sex classes. Theoretical models of social exchange were not considered useful in predicting the complex patterns of grooming, mounting, and dominance seen in the present group. Whereas such models may "explain" existing data for some groups and have gained widespread acceptance, they must be empirically tested. Am. J. Primatol. 48:283–289, 1999. © 1999 Wiley‐Liss, Inc.     

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.     

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.     

Population genetical study of Japanese macaques,Macaca fuscata,in the shimokita A1 troop,with special reference to genetic variability and relationships to Japanese macaques in other troops

The genetic variations of 35 individuals of the Shimokita A1 troop of mainland Japanese macaques,Macaca fuscata fuscata, which live at the northern end of the habitat of the species, were investigated using 33 electrophoretically detectable blood protein loci. Among the loci examined, six were polymorphic. The average heterozygosity per individual was calculated as 0.0442. This was the highest value among all troops of Japanese macaques so far investigated. The mainland macaques of the Shimokita A1 troop were more differentiated genetically from other mainland macaque troops than were Yaku macaques, the subspeciesM. f. yakui.     

Parity-related differences in suckling behavior and nipple preference among free-ranging Japanese macaques

Suckling behavior of primiparae in free-ranging Japanese macaques (Macaca fuscata) was compared with that of multiparae at Jigokudani Monkey Park, the Shiga Heights, Nagano Prefecture, Japan, from April 1984 to June 1994. The estimated rates of milk secretion in a single preferred nipple among primiparae were lower than those among multiparae from birth to 5 months of age. Milk secretion capabilities of primiparous mothers, hence, appear to be inferior to those of multiparous mothers. In nutritive sucking, although Japanese macaque infants preferred one single nipple, nipple preferences in primiparae were weaker than those in multiparae. With supplementary two-nipple use during sucking, however, the infants of primiparae appear to overcome a suckling flaw of their primiparous mothers. After infants were 5 months of age and after a drop (from approximately 10% to approximately 5%) in the rates of milk secretion, however, milk secretion rates in a single preferred nipple among primiparae were similar to those in multiparae and the supplementary two-nipple use in primiparous mother-infant dyads disappeared. Am. J. Primatol. 42:331–339, 1997. © 1997 Wiley-Liss, Inc.     

Courtship behaviour in Japanese macaques during heterosexual and homosexual consortships

Female Japanese macaques (Macaca fuscata) in the Arashiyama population near Kyoto, Japan, are unusual, in that they exhibit what many would consider to be male-typical sexual characteristics. Specifically, they mount other females within the context of temporary, but exclusive, sexual relationships (i.e., homosexual consortships) and they sometimes exhibit a preference for female sexual partners, even when given the choice of a sexually motivated male alternative. In this study, we examined whether female Japanese macaques also exhibited male-typical patterns of courtship behaviour during homosexual consortships. Data were collected on courtship behaviour during heterosexual and homosexual consortships in free-ranging Japanese macaques from the Arashiyama (Japan) population. We analyzed the occurrence of 12 different courtship behaviours during 3374 heterosexual inter-mount intervals and 1412 homosexual inter-mount intervals. Sex differences between heterosexually consorting males and females existed for only two of the 12 courtship behaviours we investigated: inclined-back presentations and sexual vocalizations. Dominant and subordinate homosexually consorting females were sex-typical in their expression of inclined-back presentations and sexual vocalizations. Consequently, facultative same-sex sexual partner preference, mounting and consortships do not co-occur with male-typical patterns of courtship behaviour in female Japanese macaques.     

Female-male mounting in Japanese macaques: the proximate role of sexual reward

Female Japanese macaques (Macaca fuscata), in certain populations, routinely engage in female-male mounting. In this study, we documented patterns of vulvar, perineal and anal (VPA) stimulation during female-male mounting in Japanese macaques. During approximately 45% of the female-male mounts analyzed, two thirds of female mounters engaged in VPA stimulation. Given the VPA region's primary role in mediating sexual response, the results of this research provide direct evidence bearing on the sexual nature of a substantial proportion of female-male mounts in Japanese macaques.     

Dominance Turnover Between an Alpha and a Beta Male and Dynamics of Social Relationships in Japanese Macaques

We report a case of turnover between an alpha (GN) and a beta male (R7) and its effects in a troop of provisioned Japanese macaques (Macaca fuscata fuscata) in Shiga-Heights, Nagano Prefecture, Japan. The aggression between the 2 males was caused by the intrusion of GN towards the consort of R7. R7 received support from his brother and mother, and consequently defeated GN. After the turnover, R7 attacked GN frequently, which may have functioned to stabilize the dominance relationship between them. Also, R7 selectively attacked females friendly to GN soon after the turnover. Although we never observed polyadic aggression among males during the stable dominance period, 20 cases of polyadic aggression occurred among the 6 highest-ranked males in the 2 days following the turnover, and one case occurred on the fourth day. R7 and GN formed stable conservative alliances for attacking subordinate males. Males that did not participate in the turnover began to form revolutionary coalitions to attack higher-ranking males, but they were thwarted by the conservative coalitions between the dominants. Mutualism was a plausible explanation for the patterns of coalition formation because most of them were conservative with little associated cost. Seven females had a high proximity index (C-score) to GN before the turnover, but a significantly lower proximity index after the turnover. On the day of the turnover, 6 non-lactating females suddenly became receptive, suggesting that the turnover induced immediate receptivity in the females.     

Distribution of Grooming Among Adult Females in a Large,Free-Ranging Group of Japanese Macaques

We analyzed grooming episodes recorded among adult females in a large, provisioned, free-ranging group of Japanese macaques (Macaca fuscata) at an individual level. Each female groomed on average 10 of the other 84 females, and 54% of them devoted 50% of their grooming to a single female grooming partner, which indicates that most females had grooming interactions with a relatively small subset of available females. Although 65% of the total grooming bouts were between related females, 25% of females disproportionately groomed unrelated females, 22% groomed related and unrelated females equally, and grooming was kin-biased for the remaining 53%. Moreover, 11 of 16 kin-groups included at least one female that groomed unrelated females significantly more often than related females. In 18% of unrelated dyads, grooming was directed down the hierarchy, in 58%, grooming was well-balanced between the two females, and in the remaining 25%, grooming was directed up the hierarchy. The results indicate that although Japanese macaques are considered a despotic species based on their dominance style, this group included some females that showed egalitarian tendencies, i.e., grooming was directed down the hierarchy or was well-balanced, and was directed toward unrelated females as often as or more often than toward related females. The presence of egalitarian individuals might be important to maintain a well-organized, female-bonded group.     

Grooming and agonistic support: a meta-analysis of primate reciprocal altruism

Grooming and agonistic support are 2 common primate behaviorsthat have been hypothesized to constitute examples of reciprocalaltruism. In particular, because primates often direct theirgrooming up the dominance hierarchy, it has been suggested thatthey may exchange grooming for agonistic support. Empiricaltests of this hypothesis have resulted in highly inconsistentfindings. I synthesized the published literature on the relationbetween grooming and agonistic support in primates using modernmeta-analytical techniques. A meta-analysis of 36 studies carriedout on 14 different species showed that a significant positiverelation exists between grooming and agonistic support (weightedaverage r = 0.154, corrected for publication bias). These findingssuggest that grooming and agonistic support may have evolvedas part of a system of low-cost reciprocal altruism. They alsohighlight the potential of meta-analysis in tackling the studyof behavioral phenomena characterized by low overall frequencyand small effect sizes.     

Kinship Bonds Are Not Necessary for Maintaining Matrilineal Rank in Captive Japanese Macaques

Although kinship is of central importance in matrilineal (nepotistic) dominance systems, various lines of evidence indicate that its role has probably been overestimated. For example, alliances among nonkin, patterned on the basis of dominance per se, contribute to the maintenance of rank and to the remarkable stability of matrilineal rank orders. But because kin and nonkin alliances exert their stabilizing effects on the rank order simultaneously, the effect of nonkin alliances per se is unknown. We tested whether nonkin alliances are sufficient to ensure the stability of matrilineal rank relations in a laboratory-housed group of Japanese macaques (Macaca fuscata). We first created a group composed of two female subgroups: (1) a subordinate subgroup of close kin known to constitute an effective revolutionary alliance and (2) a dominant subgroup composed mostly of nonkin and distant kin known to support each other against lower-ranking females. In the course of 12 consecutive experimental manipulations, we reduced progressively the relative power of the dominant subgroup by manipulating its size and age composition. The members of the dominant subgroup maintained their rank in all experimental situations except when alone. Thus, nonkin alliances remained effective up to extremely pronounced levels of power imbalance. These results suggest that the remarkable stability of matrilineal rank orders is not conditional upon the existence of nepotistic alliances and strong matrilines of close kin.     

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.     

Automatically detecting and tracking free‐ranging Japanese macaques in video recordings with deep learning and particle filters

Recently, automated observation systems for animals using artificial intelligence have been proposed. In the wild, animals are difficult to detect and track automatically because of lamination and occlusions. Our study proposes a new approach to automatically detect and track wild Japanese macaques (Macaca fuscata) using deep learning and a particle filter algorithm. Macaque likelihood is derived through deep learning and used as an observation model in a particle filter to predict the macaques’ position and size in an image. By using deep learning as an observation model, it is possible to simplify the observation model and improve the accuracy of the classifier. We investigated whether the algorithm could find body regions of macaques in video recordings of free‐ranging groups at Katsuyama, Japan to evaluate our model. Experimental results showed that our method with deep learning as an observation model had higher tracking accuracy than a method that uses a support vector machine. More generally, our study will help researchers to develop automatic observation systems for animals in the wild.     

Demography and reproductive parameters of a free-ranging group of Japanese macaques (Macaca fuscata) at Katsuyama

Demographic and reproductive data were analyzed for a period of 28 years in the females of a free-ranging group of Japanese macaques at Katsuyama, Okayama Prefecture, Japan. The overall mean, age-specific fecundity rates were 5.43% for 4-year-olds and 41.86% for 5-year-olds, increasing to a peak of 66.67% for 13-year-olds. Fecundity remained relatively high (52.31–54.24%) in 16–19-year-olds, but decreased sharply (45.45–17.86%) in 20–23-year-olds, and became very low in 24–26-year-olds. Females aged 27 years or more did not produce infants. The average age at first birth was 5.41 years. Births peaked in mid-May. The timing of the first births each year remained essentially unchanged during the study period, whereas the timing of the median and last births shifted towards the later part of the season. The mean interbirth interval for all females was 1.56 years. The value was 1.54 years for multiparous females and 1.29 years for females following infant loss. These intervals were significantly shorter than those for primiparous females, and females with surviving infants. The overall mean infant mortality within the first year of life was 10.2%. The value was 8.6% for 10–14-year-olds, and 7.5% for 15–19-year-olds. The timing of birth differed among the four female matrilineal dominance rank-classes. The female fecundity rates increased as a function of matrilineal dominance rank. It is suggested that all demographic and reproductive data should be analyzed in detail with respect to the group's history.     

Non-offspring nursing by a nulliparous pregnant female just before first parturition in free-ranging Japanese macaques

A nulliparous pregnant Japanese macaque, Macaca fuscata, suckled her 1-year-old sister 44 days before her own parturition. Other Japanese macaque yearlings did not hold the nipples of this nulliparous female in their mouths. Although this non-offspring nursing before first parturition did not improve the rate of milk secretion, the nulliparous female may have improved her indirect fitness and her suckling behavior.     

Induction of matrilineal rank instability by the alpha male in a group of Japanese macaques

Destabilizing alliances and ensuing rank changes occur infrequently in matrilineal dominance systems, and consequently very little is known about their dynamics. In one such type of alliance, called bridging, dominant individuals are ultimately responsible for subordinate monkeys out-ranking intermediate-ranking animals. Previously reported bridging alliances were based on sexual attraction, kinship ties, or special affinitive bonds between partners. In this paper we describe bridging alliances involving the alpha male in a group of Japanese macaques (Macaca fuscata) housed at the University of Montreal Laboratory of Behavioral Primatology. The comparison of rank relations in the presence and absence of the alpha male indicates that the latter was responsible for the destabilization of more than half of rank relations between members of the first and second matrilines. Another experiment revealed that the alpha male also induced extensive intermatriline reversals in priority of access to concentrated and highly prized food. These effects could be attributed to the male's consistent pattern of agonistic interventions in favor of the second matriline. However, the alpha male was not engaged in preferential affinitive relationships or reciprocally supportive interactions with the members of the second matriline. On the other hand, various lines of evidence indicate that the alpha male competed for dominance with the matriarch of the first matriline, suggesting that he might have consistently joined other individuals against that female and her kin in this context. The present data constitute further evidence for the nonaltruistic nature of aggressive interventions and the effectiveness of bridging alliances. © 1995 Wiley-Liss, Inc.