The influence of kinship and dominance hierarchy on grooming partner choice in free-ranging <Emphasis Type="Italic">Macaca mulatta brevicaudus</Emphasis>

In group-living animals, individuals do not interact uniformly with their conspecifics. Among primates, such heterogeneity in partner choice can be discerned from affiliative grooming patterns. While the preference for selecting close kin as grooming partners is ubiquitous across the primate order, the selection of higher-ranking non-kin individuals as grooming partners is less common. We studied a group of provisioned rhesus macaques (Macaca mulatta brevicaudus) on Hainan Island, China, to examine rank-related benefits of grooming exchanges and the influence of kin relationships. We tested four hypotheses based on Seyfarth’s model: (1) there will be kin preference in grooming relationships; (2) grooming between non-kin individuals will be directed up the dominance rank; (3) grooming between non-kin individuals will reduce aggression from higher-ranking ones; and (4) non-kin individuals will spend more time grooming with adjacent ranked ones. We found that grooming relationships between kin individuals were stronger than those between non-kin individuals. For non-kin relationships, lower-ranking individuals received less aggression from higher-ranking ones through grooming; a benefit they could not derive through grooming exchanges with individuals related by kinship. Individuals spent more time grooming adjacent higher-ranking non-kin individuals and higher-ranking individuals also received more grooming from non-kin individuals. Our results supported Seyfarth’s model for predicting partner choice between non-kin individuals. For relationships between kin individuals, we found results that were not consistent with prediction for the exchanges of aggression and grooming, indicating the importance to control for the influence of kinship in future studies.     

Homosexual incest avoidance among females in captive Japanese macaques

This paper reports a systematic pattern of homosexual incest avoidance among females in a captive group of Japanese macaques (Macaca fuscata) culled from the Arashiyama-West troop known for its high rates of female homosexuality. The study group included three matrilines and two generations. Between eight and 11 females were sexually active over four consecutive mating seasons, and all engaged in both heterosexual and homosexual activity. While all females performed homosexual acts with almost all possible non-kin partners, they systematically avoided homosexual interactions with their mother, daughters, and sisters. This pattern could not be explained either in terms of kin not being simultaneously in estrus, kin avoiding affiliative interactions in general, or non-kin utilizing the tension-reducing effect of estrus to affiliate exclusively with each other. In contrast to homosexual females, heterosexual pairs of relatives (brother-sister, mother-son) were sometimes incestuous. Assuming that female homosexuality expresses the reproductive strategy of females unconstrained by male influence, the present results point to the strong tendency of females to avoid incest and suggest that males are primarily responsible for the reported exceptions to incest avoidance.     

Social behavior of infant and mother Japanese Macaques (Macaca fuscata): Effects of kinship,partner sex,and infant sex

The behavioral interactions of 22 infant and mother Japanese macaques with other group members were studied. Focal-animal observations were made from the time of each infant’s birth until 1 year of age. Infants and mothers both displayed exceedingly strong preferences for associating with matrilineal kin and, specifically, for female kin. The degree of genetic relatedness was positively correlated with levels of spatial proximity, contact, grooming, aggression, and play. Overall frequencies of interactions with nonkin were very low, and partner sex was not an important factor in interactions with nonkin. There were no significant differences between male and female infants in interactions with kin versus nonkin. There was only one significant difference between male and female infants in interactions with males versus females: female infants showed stronger preferences for initiating proximity with females over males than did male infants. Because mothers provide the focal point for infant interactions during the first year of life, we compared the behavior of infants and mothers. Mothers were the recipients of more social interactions than were infants, mothers engaged in more grooming than did infants, and infants engaged in more social play than did mothers. These findings are only partially consistent with kin-selection theory, and the inadequacies of studying matrilineal kin discrimination to test kin selection are reviewed. The near-absence of infant sex differences in associations with social partners suggests that although maternal kin other than the mother are important to infant socialization, they probably do not contribute to the development of behavioral sex differences until after the first year of life.     

Aggressive interventions and matrilineal dominance relations in semifree-ranging barbary macaques (Macaca sylvanus)

Female Barbary macaques (Macaca sylvanus) form matrilineal hierarchies, i.e. they come to rank below their mother in relation to non-kin females in the course of maturation. The stability of such hierarchies and the acquisition of the matrilineal rank are achieved through dyadic aggressions and third party interventions in conflicts. This study examines the dynamics of interventions in non-kin conflicts in a semifree-ranging group of 109 Barbary macaques at “La Montagne des Singes,” Kintzheim, France. Focal sampling on 13 females aged 3 and 4 years not yet dominant over all older females from lower ranking kin groups (lower born females) was carried out during 16 months in 1987 and 1988. Results on the direction of support in non-kin female conflicts (all samples pooled) show that interventions were generally provided on behalf of the female from the higher ranking kin group (higher born female). Rates of interventions (derived from focal samples) given and received were correlated with the hierarchy; higher born females received more support and intervened more often than lower born females. A subset of interventions (based on the age of the females involved) was analyzed according to the rank distance between the opponents and the type of support provided (spontaneous or solicited). On the basis of their representation, intermediate-ranking supporters (i.e. females ranking between the opponents) intervened more often than above-ranking supporters (i.e. females dominant to both opponents), and they intervened more often spontaneously than following a solicitation. The results on interventions are discussed in the perspective of benefits to supporters. Twenty-one instances of outranking of older females (matrilineal rank acquisition) were observed. By the end of the study, the number of older lower born females not yet outranked by the focal females was negatively correlated to the rank distance between the two sets of females. However no such correlation was found between these two groups when compared according to their age difference in years.     

Differential effects of kinship,dominance, and the mating season on female allogrooming in a captive group ofMacaca fuscata

An analysis of allogrooming (total times spent grooming individual partners) of 8 sexually mature females (3–12 years of age) in a captive group of 17 Japanese macaques, shows that during the nonmating season, grooming distributions were characterized by high proportions of grooming given to family members and/or higher ranking nonkin. During the mating season, all eight females showed significant shifts in their grooming distributions, and four females showed significant shifts in grooming between their nonestrous and estrous periods (defined behaviorally). Fox six of eight females, mating season grooming was characterized by either high proportions of grooming given to family members and/or heterosexual and homosexual partners. It was found that within dyadic sexual relationships, dominants gave more grooming to subordinates than the former received, in contrast to a reversal of this pattern in the majority of these same dyads during the nonmating season. This is interpreted as one short-term function of grooming: a dominant asymmetrically grooms a subordinate sexual partner to maintain proximity with (or reduce tension in) the latter. The two remaining focal females (middle ranking, nulliparous) differed from the other females in that they shifted their mating season grooming to subordinate nonkin, despite the lack of evidence that this was a result of sexual interactions, patterns of partner availability, competition, patterns of grooming reciprocity, or agonistic alliance support. From these results, it is suggested that in some contexts, grooming of subordinate nonkin may function to reduce tension in thegroomer. In the Japanese macaque, this latter possibility and the asymmetric grooming of subordinate homosexual partners may prove to be exceptions to the general rule that female cercopithecine grooming of nonkin flows up the dominance hierarchy.     

Behavioural and hormonal responses to predation in female chacma baboons (Papio hamadryas ursinus)

In humans, bereavement is associated with an increase in glucocorticoid (GC) levels, though this increase can be mitigated by social support. We examined faecal GC levels and grooming behaviour of free-ranging female baboons to determine whether similar effects were also evident in a non-human species. Females who lost a close relative experienced a significant increase in GC levels in the weeks following their relative's death compared with the weeks before, whereas control females showed no such increase. Despite the fact that females concentrate much of their grooming on close kin, females who lost a close female relative did not experience a decrease in grooming rate and number of grooming partners; instead, both grooming rate and number of grooming partners increased after a relative's death. While the death of a close relative was clearly stressful over the short term, females appeared to compensate for this loss by broadening and strengthening their grooming networks. Perhaps as a result, females' GC levels soon returned to baseline. Even in the presence of familiar troop-mates and other relatives, females experienced a stress response when they lost specific companions, and they apparently sought to alleviate it by broadening and strengthening their social relationships.     

雌性黄山短尾猴回避近亲交配

本研究分别在交配期(2006年9月-2006年12月)和产仔期(2007年1月-2007年4月)对黄山短尾猴鱼鳞坑YA1群中5只雄猴和5只雌猴成年个体采用目标动物法、随机取样法和连续记录法记录行为参数。研究期间记录交配行为336例:母子交配0例;母系兄妹交配7例(占2.1%),其中强行交配4例;非亲缘关系交配329例(占97.9%),非亲缘关系交配频次显著高于亲缘关系。在交配期,雄猴对亲缘雌猴跟随、性检查频次均低于非亲缘雌猴,接近指数(PMI)在亲缘和非亲缘雌猴间无显著性差异;雌猴对亲缘雄猴交配拒绝率显著高于非亲缘雄猴,接近指数在交配期显著低于非亲缘雄猴,产仔期接近指数在亲缘和非亲缘雄猴间无显著性差异。尽管雄猴在交配选择上趋于避免与亲缘雌猴交配,但某些雄猴仍会主动对有亲缘关系的雌猴邀配或强行交配,雌猴则主动回避。这些结果表明:黄山短尾猴母系亲属间可以通过行为倾向抑制近亲交配发生,且雌猴更主动回避交配,支持了近交回避的双亲投资理论。     

The social grooming of captive female rhesus monkeys: Effects of the births of their infants

We observed the grooming interactions of 13 female rhesus monkeys (Macaca mulatta)before and for 12 weeks after the births of their infants. Mothers groomed for similar amounts of time before and after the birth of their infants, but after the birth, the grooming they directed to their infants may have been at the expense of that directed to other partners. Lactating females did not receive more grooming from other females but were approached more often, suggesting that they were more attractive. Mothers that groomed their infants most groomed others least, as if grooming time was limited for each mother or as if she was trying to compensate for avoiding interactions with other partners. Mothers of male infants groomed others more than mothers with female infants did, which might be due to mothers with daughters receiving more aggression and therefore avoiding interaction. Experienced and high-ranking mothers groomed their newborn infants considerably more than primiparous mothers did in the 24 hr following birth. Grooming was preferentially directed at close kin before the births of the infants. Mothers tended to groom higher-ranked partners more than they were groomed by them, and they tended to receive more grooming from lower-ranked partners than they gave, as suggested in models of rank attractiveness.     

Grooming reciprocity in female tibetan macaques macaca thibetana

Grooming among nonhuman primates is widespread and may represent an important service commodity that is exchanged within a biological marketplace. In this study, using focal animal sampling methods, we recorded grooming relationships among 12 adult females in a free-ranging group of Tibetan macaques (Macaca thibetana) at Huangshan, China, to determine the influence of rank and kinship on grooming relationships, and whether females act as reciprocal traders (exchange grooming received for grooming given) or interchange traders (interchange grooming for social tolerance or other commodities). The results showed that: (1) grooming given was positively correlated with grooming received; (2) kinship did not exert a significant influence on grooming reciprocity; and (3) grooming reciprocity occurred principally between individuals of adjacent rank; however, when females of different rank groomed, females tended to groom up the hierarchy (lower ranking individuals groomed higher ranking individuals more than vice versa). Our results support the contention that both grooming reciprocity and the interchange of grooming for tolerance represent important social tactics used by female Tibetan macaques.     

Long-term reciprocation of grooming in wild West African chimpanzees

Humans are well known for their ability to keep track of social debts over extended periods of time, and for their tendency to preferentially cooperate with closely bonded partners. Non-human primates have been shown to cooperate with kin and non-kin, and reciprocate helpful acts. However, there is ongoing debate over whether they keep track of previous interactions and, if so, whether they can do it over extended periods of time, or are constrained to finalize exchanges within a single encounter. In this study, we used 3000 hours of all-day focal follows of wild chimpanzees (Pan troglodytes verus) to investigate whether both females and males reciprocate grooming within a single interaction, throughout the day, or over longer periods of time. We found that grooming was reciprocated more symmetrically when measured on a long-term, rather than on an immediate or short-term basis. Random giving, general allocation of grooming efforts, similarities among individuals and kinship do not appear to explain these highly reciprocal exchanges. Previously collected consecutive focal follows of single individuals revealed that dyads groomed an average of once every 7 days. Our findings strongly suggest that chimpanzees, similar to humans, are able to keep track of past social interactions, at least for a one-week period, and balance services over repeated encounters.     

Pre-reproductive alliance formation in female wild house mice (<Emphasis Type="Italic">Mus domesticus</Emphasis>): the effects of familiarity and age disparity

Female house mice (Mus domesticus) are known to perform communal breeding more often with kin than with non-kin partners. When mice are grouped in semi-natural enclosures, related females develop pre-reproductive alliances more frequently than unrelated ones. However, little is known about the behavioural mechanisms and the factors promoting kin preferential cooperative associations in female mice. Here we evaluate the relative importance of familiarity and age disparity on the pre-reproductive development of agonistic behaviour and spatial associations within groups of three related females, freely interacting in semi-natural indoor enclosures. We found that familiarity clearly promoted female alliance formation by reducing aggression and enhancing spatial cohabitation, while genetic relatedness per se did not alleviate the effects of unfamiliarity on female grouping. Older sisters clearly dominated younger ones, even if they had lower body weights, or if they had to confront two allied littermate sisters. Hence, our findings corroborate previous findings on familiarity as a proxy for kin-preferential alliance formation in female mice. Moreover, we observed a strong impact of age stratification on female aggression-mediated dominance development. We suggest that this age effect could be expected from a queuing-for-reproduction view of younger house mouse females.Communicated by I. Schlupp     

Long-term grooming partnerships between unrelated adult females in a free-ranging group of Japanese monkeys (Macaca fuscata)

In order to examine the presence of long-term grooming relationships among unrelated females, grooming interactions of 18 adult females (range: 16-32 years) in a free-ranging group of Japanese monkeys (Macaca fuscata) were recorded in 2003 and compared with those recorded 10 years earlier, i.e., in 1993. In 2003, on average, each female who had survived the 10 years had grooming interactions with 2.2 surviving old partners with whom she was recorded to have grooming interactions in 1993, 3.5 females related to the surviving old partners, and 4.5 unrelated females who were other than the surviving old partners or their related females. By calculating the ratio of actual grooming partners to available females in 2003, we concluded that females had a greater possibility of selecting surviving old partners as their grooming partners than other unrelated partners, and that they also had a greater possibility of selecting females related to surviving old partners than females other than surviving old partners and their related females. These findings indicate that with regard to grooming relationships, female Japanese monkeys are basically conservative, showing a tendency to concentrate their grooming interactions on closely related females and certain familiar unrelated females such as surviving old partners and some females closely related to these partners. At the same time, however, female Japanese monkeys also showed a progressive trait for grooming since they formed grooming relationships with new partners. The necessity of long-term psychological bonding for long-term grooming relationships between unrelated females is discussed in this work.     

Initiation and solicitation in male-female grooming in a wild Japanese macaque troop on yakushima island

Grooming initiation among adult males and females of a Japanese macaque troop was analyzed during the non-mating season. Some gestures (“solicitation”) elicited grooming from partners at a high rate. Grooming initiation patterns were divided into two main types: (1) a male often solicited a female to groom him immediately after approaching her and was groomed by her; and (2) a female approached an alpha male selectively, and immediately groomed him. After a female groomed a male, she rarely solicited him to groom her and instead often moved away from him. These results indicated that males were motivated to be groomed, while females were more highly motivated to groom. Sex differences in grooming motivation can be explained by sex differences in the benefit to be groomed.     

Huddling relationships in night sleeping groups among wild Japanese macaques in Kinkazan Island during winter

Huddling groups at sleeping sites, and allogrooming and proximity in the daytime during winter, were examined in a wild Japanese macaque (Macaca fuscata) troop on Kinkazan Island in the non-snowy district of northern Japan. All sleeping groups, defined as a cluster in which individuals huddle at sleeping sites, were formed on the ground. Their sizes tended to increase when the temperature was lower. The number of adults with mutual physical contact in sleeping groups increased when the size of sleeping groups increased. These results suggest that the physiological function of huddling is protection from low temperatures, and that macaques select the ground as sleeping sites to form large sized groups. Huddling was performed most frequently among kin dyads. Non-related dyads which appeared to be affiliative in the daytime also huddled frequently at sleeping sites. Even non-related dyads which showed affiliative behavior less frequently in the daytime exhibited huddling, at night, however, they did so less often than those of kin dyads and affiliated dyads. It appears that huddling at night by pairs that did not normally affiliate in the daytime was made possible by the increased tolerance of individuals responding to colder temperatures at night in winter. Furthermore, huddling, grooming, and proximity were exhibited at greater frequency between kin dyads, and between high-ranking males and specific females of kin groups, although the dyads of individuals older than 15 years often were involved only in huddling. These results suggest that two types of social bonds exist at sleeping sites in winter. One is the social bond common to both the daytime and nighttime, the other is peculiar to nighttime. Consequently, the social function of huddling is that, troop integration might increase at sleeping sites in winter as close social relationships among adults are extended more widely than those in daytime.     

Sex and age differences in juvenile social priorities in female philopatric,nondespotic blue monkeys

Juveniles should choose social partners on the basis of both current and future utility. Where one sex is philopatric, one expects members of that sex to develop greater and sex‐typical social integration with group‐mates over the juvenile period. Where a partner's position in a dominance hierarchy is not associated with services it can provide, one would not expect juveniles to choose partners based on rank, nor sex differences in rank‐based preferences. We tested these ideas on 39 wild juvenile (3.2–7.4 years) blue monkeys (Cercopithecus mitis stuhlmanni), cercopithecines with strict female philopatry and muted hierarchies. We made focal animal observations over 6 months, and computed observed:expected amounts of proximity time, approaches and grooming given to various social partners. Overall, our results agree with the hypothesis that juvenile blue monkeys target social partners strategically. Spatial proximity, approaches and active grooming showed similar patterns regarding juvenile social preferences. Females were far more sociable than males, groomed more partners, reciprocated grooming more frequently, and preferred—while males avoided—infants as partners. Older juveniles (5–7 years) spent more time than younger juveniles (3–4 years) near others, and older females were especially attracted to infants. Close kin, especially mothers and less consistently adult sisters, were attractive to both male and female juveniles, regardless of age. Both sexes also preferred same‐sex juveniles as social partners while avoiding opposite‐sex peers. Juveniles of both sexes and ages generally neither preferred nor avoided nonmaternal adult females, but all juveniles avoided adult males. Partner's rank had no consistent effect on juveniles' preference, as expected for a species in which dominance plays a weak role. Juveniles' social preferences likely reflect both future and current benefits, including having tolerant adult kin to protect them against predators and conspecifics, same‐sex play partners, and, for females, infants on which to practice mothering skills. Am. J. Primatol. 72:193–205, 2010. © 2009 Wiley‐Liss, Inc.     

Social relationships of nulliparous young adult females beyond the ordinary age of the first birth in a free-ranging troop of Japanese macaques (Macaca fuscata)

We describe the social relationships of young adult female Japanese macaques (Macaca fuscata) in a free-ranging troop in Arashiyama, Kyoto, Japan, who remained nulliparous beyond the ordinary age of first birth because of contraceptive administration. We observed 12 young nulliparous adult females (6–9 years old) for 270 h and 10 min from 2 February to 5 October 2010. The majority maintained close relationships with their mothers through proximity and grooming, whereas a few had very infrequent social interactions with their mothers. Most had asymmetrical grooming relationships; the grooming they received from unrelated adult females was less than the grooming they gave. Young adult females who had less frequent interactions with their mothers by either proximity or grooming received more grooming from a larger number of unrelated adult females than did those who had more frequent social interactions with their mothers. These results indicate that most young adult females who remained nulliparous beyond the ordinary age of first birth tended to maintain close relationships with their mothers, and their grooming relationships with unrelated adult females were inversely related to the degree of closeness with their mothers.     

Grooming and group structure in hamadryas baboons

The results of 3-year observation on coral living hamadryas baboons transported from natural habitat in Tuapse reservation have been presented. Despite of the fact that grooming between males and females accounted for 73% of total cases of grooming in adult individual pairs, only the relationships of males with high-ranked females of their harems fully corresponded to a star-shaped sociogram. The high-ranked females were not different from all the other females either according to a total number of grooming cases with their female partners or according to a proportion of a performed and received grooming. Grooming between the related females was noted predominantly in the cases when they belonged to the same harem. Grooming between the related males accounted for 59% of all the cases of grooming between the male partners.     

Sex differences in sexual partner acquisition, retention, and harassment during female homosexual consortships in Japanese macaques

Female Japanese macaques (Macaca fuscata) in certain populations are unusual in that they exhibit male-typical patterns of mounting behavior and sexual-partner preference. The goal of this study was to determine whether female Japanese macaques, from one such population, employ male-typical behavioral tactics to disrupt existing homosexual consortships, as well as to acquire and retain same-sex sexual partners. "Harassment" of homosexual consortships occurred when a sexually motivated, third-party male or female interrupted a consorting female couple by displacing or aggressing them. Sexual harassment was a male-typical strategy for disrupting existing homosexual consortships, but was rarely performed by females. "Intrusions" occurred when a male or female competitor attempted to acquire exclusive access to a female engaged in a homosexual consortship by targeting that female as the focus of competition and her partner as his/her competitor. "Sexual coercion" occurred when one individual alternately sexually solicited and aggressed another individual as part of the same behavioral sequence during an intrusion. Males employed consortship intrusions and sexual coercion when they attempted to acquire female sexual partners that were already engaged in homosexual consortships, but females rarely did so. However, females did employ male-typical patterns of aggressive competition and sexual coercion to retain same-sex sexual partners when confronted with male competitors' attempts to usurp those partners. These results indicate that female sexual activity during homosexual consortships is not uniformly "masculine" in expression, but rather is a mixture of male- and female-typical behaviors.     

Weaving a tight social net: Allogrooming in free-ranging female langurs (Presbytis entellus)

We studied grooming among adults of a one-male multifemale troop of free-ranging Hanuman langurs (Presbytis entellus)living near Jodhpur, India, for 9 years. The 11–13 females devoted about 6% of their day to allogrooming. Adult males, whose tenures averaged 2.2 years, were transient figures in the troop's history, as reflected by their rather peripheral role in the grooming network. Females groomed males 4–40 times more frequently (1006 episodes) than vice versa- (176 episodes). Adult females received 97% of all grooming from other adult females (6655 episodes). Although females exhibited an age- inversed dominance hierarchy, they did not compete for grooming access to particular troop mates. Dyads of all possible rank differences occurred as frequently as expected: 51% of grooming was directed up the hierarchy and 49% down it. Young, high- ranking individuals gave and received significantly more grooming than the oldest, low- ranking females did. The pattern seemed to be influenced by kin selection because of the presumably high degree of female relatedness. They invested most in troopmates with the highest reproductive value, i.e., the youngest individuals. This trend was coupled with a preference of closest kin (mothers and daughters). Reciprocity was the outstanding feature since all adult females groomed and were groomed by all others. Such a tight social net might establish the necessary cohesion during frequent territorial disputes with neighboring troops.     

Social benefits of non-kin food sharing by female vampire bats

Regurgitations of blood among vampire bats appear to benefit both direct and indirect fitness. To maximize inclusive fitness, reciprocal food sharing should occur among close kin. Why then do females with kin roost-mates help non-kin? We tested the hypothesis that helping non-kin increases a bat''s success at obtaining future donations by expanding its network of potential donors. On six occasions, we individually fasted 14 adult females and measured donations from 28 possible donors. Each female was fasted before, during and after a treatment period, when we prevented donations from past donors (including 10 close relatives) by simultaneously fasting or removing them. This experiment was designed to detect partner switching and yielded three main results. First, females received less food when we prevented donations from a past donor versus a control bat. Donors within a group are therefore not interchangeable. Second, the treatment increased the variance in donors'' contributions to food received by subjects, suggesting the possibility of alternative responses to a partner''s inability to reciprocate. Finally, bats that fed more non-kin in previous years had more donors and received more food during the treatment. These results indicate that a bat can expand its network of possible donors by helping non-kin.