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.     

Rank and grooming reciprocity among females in a mixed-sex group of captive hamadryas baboons

In a mixed-sex, captive group of hamadryas baboons (Papio hamadryas hamadryas) we investigated whether female grooming relationships are affected by their dominance ranks. Seyfarth's [1977] grooming for support model and Barrett et al.'s [1999] biological market model both predict that in primate groups where competition for monopolizable resources is high, grooming among females is based, at least partly, on the interchange of grooming for rank-related benefits, and that rank thus influences the distribution of grooming in females. Contrary to this prediction, our results show that despite the existence of a linear dominance hierarchy, rather strict dominance relationships, and high food-related aggression rates, grooming among female hamadryas baboons is not affected by rank and is only exchanged for itself. This is understandable since rank differences in our study group only result in differential access to limited, preferred food items that are not actively shared. Although some females are more likely to tolerate one another at the food pile, this tolerance is not determined by their grooming efforts and interchange of grooming for rank-related benefits does not occur. We conclude that female hamadryas baboons groom others in order to be groomed by them, which is supported by our observation that grooming reciprocity within a dyad increases when more grooming occurs in this dyad. Our results indicate that grooming is indeed a valuable commodity in itself, probably because of its stress- and tension-reducing effect. Based on our findings, the existing groom trade model is extended to include circumstances in which monopolizable resources are available but are not traded for grooming.     

Grooming up the hierarchy: the exchange of grooming and rank-related benefits in a new world primate

Seyfarth's model assumes that female primates derive rank-related benefits from higher-ranking females in exchange for grooming. As a consequence, the model predicts females prefer high-ranking females as grooming partners and compete for the opportunity to groom them. Therefore, allogrooming is expected to be directed up the dominance hierarchy and to occur more often between females with adjacent ranks. Although data from Old World primates generally support the model, studies on the relation between grooming and dominance rank in the New World genus Cebus have found conflicting results, showing considerable variability across groups and species. In this study, we investigated the pattern of grooming in wild tufted capuchin females (Cebus apella nigritus) in Iguazú National Park, Argentina by testing both the assumption (i.e., that females gain rank-related return benefits from grooming) and predictions (i.e., that females direct grooming up the dominance hierarchy and the majority of grooming occurs between females with adjacent ranks) of Seyfarth's model. Study subjects were 9 adult females belonging to a single group. Results showed that grooming was given in return for tolerance during naturally occurring feeding, a benefit that higher-ranking females can more easily grant. Female grooming was directed up the hierarchy and was given more often to partners with similar rank. These findings provide supporting evidence for both the assumption and predictions of Seyfarth's model and represent, more generally, the first evidence of reciprocal behavioural interchanges driven by rank-related benefits in New World female primates.     

三种笼养灵长类活动时间分配的比较研究

采用焦点动物法和连续记录法对3种笼养灵长类活动时间分配进行比较研究。结果表明,川金丝猴Rhi-nopithecus roxellanae和熊猴Macaca assamensis用于休息的时间多于猕猴Macaca mulatta,移动时间则相反;川金丝猴和猕猴用于理毛的时间多于熊猴。不同性别年龄组之间的活动时间分配有差异,主要表现在川金丝猴母亲用于理毛的时间明显多于成年儿子,用于玩耍的时间则相反;猕猴成年雄性的移动时间和理毛时间多于成年雌性,玩耍时间则少于成年雌性;熊猴成年雌性的移动时间多于成年雄性,与成年个体相比,幼体花更多的时间用于玩耍,而相应的减少了其休息时间。     

Female macaques compete for ‘power’ and ‘commitment’ in their male partners

The formation of male-female social bonds and the resulting competition among females for male partners is a core element of human societies. While female competition for a male partner outside the mating context is well studied in humans, evidence from non-human primates is scarce, and its evolutionary roots remain to be explored. We studied two multi male – multi female groups of wild Assamese macaques (Macaca assamensis), a species where females gain benefits from selectively affiliating with particular males. Using a behavioral data set collected over several years, we tested whether females competed over access to male social partners, whether success in competition was driven by female dominance rank, and which male traits were most attractive for females. We found assortative bonding by dominance rank between females and males, which together with females initiating and maintaining contact suggests direct female competition over males. Two male traits independently predicted male attractiveness to females: (1) current dominance rank, a measure of 'power' or a male's ability to provide access to resources, and (2) prior male affiliation with immatures, a measure of a male's potential paternal proclivity or 'commitment' to infant care. Both traits have been consistently identified as drivers of female partner choice in humans. Our study adds to the evidence that female competition for valuable male partners is not unique to humans, suggesting deep evolutionary origins of women's mate choice tendencies for ‘power’ and ‘commitment’.     

Evaluating Dominance Styles in Assamese and Rhesus Macaques

Researchers have suggested that several types of agonistic and affiliative behavior covary as a set of species-specific traits, and have used the term dominance style to describe the covariation. We compared measures of dominance style between a group of Assamese macaques (Macaca assamensis) and a group of rhesus macaques (M. mulatta), though kinship information was unknown. Assamese and rhesus female-female dyads each showed a low proportion of counter aggression and a low conciliatory tendency, suggesting that they have despotic social relationships. They also showed a despotic pattern on several other types of agonistic and affiliative behavior, such as approach outcomes and grooming distributions, which is consistent with the covariation of dominance style traits. Assamese male-male dyads showed relatively high levels of reconciliation and counter aggression versus other macaque males portrayed in the literature, suggesting that Assamese males have a tolerant dominance style. Insofar as macaque dominance style depends on the behavior of females, we suggest that Assamese macaques, like rhesus macaques, have despotic social relationships, which contrasts with evidence of a strong correlation between phylogeny and dominance style in macaques. Further, our results indicate that strong male bonding and tolerant dominance relationships among males are independent of female dominance style. Lastly, some measures of agonistic behavior, such as rate of aggression or proportion of bites, are likely altered in competitive environments and thus are not useful indicators of dominance style.     

Male competition and its hormonal correlates in Assamese macaques (Macaca assamensis)

In polygynous mammals, where males compete over access to females, the potential of males to monopolize reproductive females largely depends on the spatio-temporal distribution of reproductive females. We investigated mechanisms of male reproductive competition and its hormonal basis in a cercopithecine species with reduced contest potential owing to female reproductive synchrony and concealed ovulation. Over 16 months including two mating seasons we collected 1218 h of observational focal animal data and 1254 fecal samples of 11-12 adult and large subadult male Assamese macaques (Macaca assamensis) living in their natural habitat in Thailand. Androgen output along with aggressive behavior showed a seasonal pattern, with highest values being obtained by all males during the mating season and by those males experiencing acute social challenges, e.g. rank change and dispersal. Individual androgen levels and rates of attacks were linked across the study period, suggesting a promoting function of androgens for aggressive behavior. Dominance rank predicted neither mating success nor androgen levels consistently, indicating a reduced selective advantage of high social status for general mating access. However, high ranking males engaged in extended consortships with reproductive females. Distribution of consortships across males followed a priority of access distribution, with the two top ranking males accounting for 75% of consort activity, suggesting that high social status also carries fitness benefits in a species characterized by low contest potential.     

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.     

A dynamic interaction between aggression and grooming reciprocity among female chacma baboons

We used data from a natural experiment on adult female chacma baboons, Papio cynocephalus ursinus, to test the hypothesis that variation in aggression through time influences patterns of grooming reciprocity within a social group. Owing to a change in the baboons' competitive regime, we were able to compare data from periods when aggression was high (period 1) and low (period 2). During period 2, the slope of the relationship between aggression and rank was significantly shallower than during period 1 and less aggression was directed at the lowest-ranking females suggesting there had been a reduction in the dominance gradient. We attributed this to reduced effectiveness of dominance as a means of excluding other females from feeding resources. The reduction in aggression during period 2 was accompanied by an increase in grooming reciprocity between dyads suggesting that high-ranking females no longer attracted grooming by subordinates in exchange for tolerance, and that grooming in period 2 was exchanged for its intrinsic benefits. The loss of rank-related effects on grooming reciprocity in period 2 compared with period 1 further confirmed this. These findings show that female baboons are able to respond flexibly and swiftly to changes in their social circumstances and that a dynamic approach to primate social interactions is worth pursuing. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Competition for grooming partners and interference in affiliation among female mandrills

Grooming is the most common primate affiliative behaviour, and primates compete for accessing grooming partners. We studied a captive group of mandrills (Mandrillus sphinx) to evaluate the role of different types of competitive interactions in shaping the distribution of grooming among females. Mandrill females preferentially groomed high‐ranking individuals, but low‐ranking females were less able to do so. Interference in others’ grooming and a (consequent) reluctance of low‐ranking females to access dominant group mates occurred frequently and contributed to the observed pattern of grooming distribution, while takeovers of grooming partners was relatively rare. Interference in others’ affiliation was possibly used to prevent the formation of revolutionary alliances. Difficulties in accessing individuals already engaged in grooming exerted a strong but rank‐independent effect on grooming interactions. These results highlight the role of competition in determining access to preferred social partners.     

Time-matched grooming in female primates? New analyses from two species

The parcelling model of reciprocity predicts that grooming partners will alternate between giving and receiving grooming within grooming bouts, and that each partner will perform approximately as much grooming as it receives within each bout (‘time matching’). Models of allogrooming based on biological markets theory predict that individuals of lower dominance rank will exchange grooming for tolerance from high-rankers, and therefore an inverse relation will be found between grooming partners' dominance rank distance and how closely they match each other's grooming contributions within each bout. We used weighted logistic regression and weighted least-squares regression to test these predictions using data from female white-faced capuchins, Cebus capucinus, and bonnet macaques, Macaca radiata. Only 5-7% of macaque grooming bouts, and 12-27% of capuchin grooming bouts, were reciprocated. However, (1) the duration of grooming by the first groomer significantly predicted whether the groomee would reciprocate at all, and (2) when bouts were reciprocated, the duration of grooming by the first groomer significantly predicted the duration of grooming by the second groomer. Grooming was most balanced among females of similar dominance ranks. Both the time-matching and rank-related effects were weak, although significant. These results indicate that although some form of time matching may be a general characteristic of grooming in female-bonded primate species, time matching accounts for relatively little of the variation in the distribution of grooming within bouts. We also draw attention to weighted regression as a technique that avoids pseudoreplication while using all available data.     

The effect of solicitations on grooming exchanges among female Japanese macaques at Katsuyama

In group-living primates, individuals often exchange grooming with not only kin but also non-kin. We investigated the effect of soliciting behaviors on grooming exchanges in a free-ranging Japanese macaque (Macaca fuscata) group at Katsuyama. In this study, we used a focal animal sampling method, targeting 14 females. Data were collected for 15.75 ± 2.67 (mean ± SD) hours per focal female. We classified female–female pairs into three pair types: kin pairs, affiliated non-kin pairs, and unaffiliated non-kin pairs. Females received grooming more frequently when they solicited after grooming their partners than when they did not solicit in all pair types. In addition, females received grooming less frequently when they did not groom their unaffiliated non-kin partners before soliciting; prior grooming was not needed to receive grooming from kin or affiliated non-kin partners. The degree of grooming reciprocity did not differ according to the frequency with which females in kin or affiliated non-kin pairs solicited after grooming. On the other hand, grooming reciprocity between unaffiliated non-kin females was more balanced when they solicited frequently after grooming, as compared with when they did not. In conclusion, our study suggests that soliciting behaviors promote grooming exchanges in female Japanese macaques.     

Grooming reciprocation among female primates: a meta-analysis

The theory of reciprocal altruism offers an explanation for the evolution of altruistic behaviours among unrelated animals. Among primates, grooming is one of the most common altruistic behaviours. Primates have been suggested to exchange grooming both for itself and for rank-related benefits. While previous meta-analyses have shown that they direct their grooming up the hierarchy and exchange it for agonistic support, no comprehensive evaluation of grooming reciprocation has been made. Here we report on a meta-analysis of grooming reciprocation among female primates based on 48 social groups belonging to 22 different species and 12 genera. The results of this meta-analysis showed that female primates groom preferentially those group mates that groom them most. To the extent allowed by the availability of kinship data, this result holds true when controlling for maternal kinship. These results, together with previous findings, suggest that primates are indeed able to exchange grooming both for itself and for different rank-related benefits.     

Effect of resource competition on the long-term allocation of grooming by female baboons: evaluating Seyfarth's model

Seyfarth (1977, Journal of Theoretical Biology, 65, 671-698) proposed an influential model that explained the long-term patterning of grooming relationships between female primates in terms of an interaction between the idealized grooming objectives of females and competition for valuable grooming partners. A critical test of the model requires a demonstration not only that competition for partners exists, but also that females do have an underlying target for the amount of grooming that they would like to receive relative to the amount they need to give. As it is not possible to stipulate a priori what this target is, or to detect it directly, we assessed its applicability by making a set of predictions, within the framework of Seyfarth's model, as to how observed grooming patterns should change with changes in the intensity of resource competition. We tested these predictions with data from a troop of baboons, Papio hamadryas ursinus, for which the within-bout structure of grooming has already been shown to be sensitive to changes in resource competition (Barrett et al. 2002, Animal Behaviour, 63, 1047-1053). We found no evidence of competition for grooming partners and our results do not support the predictions of the modified model with respect to the existence of underlying grooming objectives. The findings that the grooming of female baboons is more diverse and that the mean rank distance separating partners increases when resource competition is greater, together with the absence of rank effects on long-term patterns, are, however, supportive of the recent biological market approach to social interactions. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Stability and Durability of Intra- and Intersex Social Bonds of Captive Rhesus Macaques (Macaca mulatta)

Many social species maintain differentiated relationships with their group members. These social bonds may reflect short-term interactions satisfying immediate needs. Alternatively, individuals of some species may entertain stable and valuable bonds that last much longer than opportunistic interactions would predict. This claim is supported by recent research that revealed clear fitness benefits for long-lasting social bonds. Here, we investigated the stability and equitability of social relationships in captive rhesus macaques, measured using their proximity and grooming patterns over a 3-yr period. We show that, in general, proximity patterns of the whole group were stable over 3 yr. More specifically, each individual’s top two nonkin within and between sex relationships based on proximity were relatively stable and some of these relationships lasted the full 3 yr. Female grooming relationships within and between sex were also stable over 3 yr. Moreover, strong social bonds in females were not based on age similarity and were not sex specific, suggesting that a general underlying mechanism of social bonding in female rhesus macaques. In contrast, patterns of male grooming of other males and of females were relatively unstable and male social bonds were less equitable than those of females. The differences in stability of the relationships between the sexes may reflect the dispersal pattern of rhesus macaques, although we have limited data on non-natal males in our study. With these data we add to a growing body of literature describing the value and durability of relationships among primates and other species.     

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.     

Changes in the social structure of two groups of stumptail macaques (Macaca arctoides)

Two previously studied groups of stumptail macaques were restudied to investigate stabilities and instabilities within group structures. Frequency data for nonsocial and dyad behaviors were collected. While there was considerable group stability, several important changes occurred. The most noteworthy group changes were in grooming and playing. Individual changes centered upon females. The first and fourth ranking females of one group switched dominance positions. The roots of this reversal were minimally reflected by aggressive and submissive interactions, and more fully exposed by quiet association patterns such as grooming, huddling, and sitting together. Increased frequencies of huddling, touching, and approaching indicated that the lowest ranking female of each group moved closer to other group members. There was no hint of this change in agonistic interactions.     

Allogrooming Behavior and Grooming Site Preferences in Captive Bonobos (Pan paniscus): Association with Female Dominance

I tested the utility of Seyfarth's (1977) model of rank-related attractiveness to explain the distribution of allogrooming behavior among captive bonobos (Pan paniscus). Adult female bonobos generally have high social status and may be dominant over males. As predicted by the model, I found that high-ranking adult females received most allogrooming within each of the four investigated groups. Among adult female-adult female dyads, however, allogrooming was not clearly associated with dominance rank. Contradictory to predictions of the model, the highest-ranking females were responsible for most displacements over allogrooming, and grooming competition is positively correlated with dominance rank. In the second part of this study, I investigated the social significance of allogrooming body site preferences. Bonobos direct significantly most allogrooming to the face of conspecifics, and high- and low-ranking individuals, as well as males and females, differ significantly in their preferences for certain allogrooming sites. Subordinates and males tended to avoid facial grooming and preferred the back and anogenital region, while high-ranking individuals and females directed most allogrooming to the face and head of grooming partners. Data from this study support the hypothesis that high-ranking females are the most attractive grooming partners within a female-centered bonobo society. Many other aspects of allogrooming behavior, however, are not consistent with the model of rank-related attractiveness.     

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.     

Niche separation of sympatric macaques, Macaca assamensis and M. mulatta, in limestone habitats of Nonggang, China

Comparative studies of sympatric species are essential in understanding those species’ behavioral and ecological adaptations as well as the mechanisms that can reduce resource competition enough to allow coexistence. We collected data on diet, activity budget and habitat use from two sympatric macaque species, the Assamese macaque (Macaca assamensis) and the rhesus macaque (M. mulatta), in a limestone seasonal rainforest of Nonggang Nature Reserve, southwestern Guangxi, China. Our results show that the two sympatric macaques differ in diet, activity budget, and habitat use: (1) out of the 131 plant species that were used by both macaque species as food over the year, only 15 plant species (11 %) were shared. Rhesus macaques used more plant species as major foods, and had higher dietary diversity and evenness indexes than Assamese macaques. (2) Assamese macaques fed predominantly on leaves, whereas rhesus macaques fed more selectively on fruits. The rhesus macaques’ diet varied according to season, and was significantly correlated to season fluctuation in fruit availability. (3) Assamese macaques devoted more time to resting, and less time to feeding than rhesus macaques (4) Assamese macaques were present mostly on the cliff, and tended to stay on the ground, whereas rhesus macaques were present mostly on the hillside, and showed preference to lower and middle canopy. The observed differences in diet and habitat use between the two macaque species represent behavioral patterns enabling their coexistence.