Exploring the components, asymmetry and distribution of relationship quality in wild Barbary macaques (Macaca sylvanus)

Social relationships between group members are a key feature of many animal societies. The quality of social relationships has been described by three main components: value, compatibility and security, based on the benefits, tenure and stability of social exchanges. We aimed to analyse whether this three component structure could be used to describe the quality of social relationships in wild Barbary macaques (Macaca sylvanus). Moreover, we examined whether relationship quality was affected by the sex, age and rank differences between social partners, and investigated the asymmetric nature of social relationships. We collected over 1,900 hours of focal data on seven behavioural variables measuring relationship quality, and used principal component analysis to investigate how these variables clustered together. We found that relationship quality in wild Barbary macaques can be described by a three component structure that represents the value, compatibility and security of a relationship. Female-female dyads had more valuable relationships and same-age dyads more compatible relationships than any other dyad. Rank difference had no effect on the quality of a social relationship. Finally, we found a high degree of asymmetry in how members of a dyad exchange social behaviour. We argue that the asymmetry of social relationships should be taken into account when exploring the pattern and function of social behaviour in animal societies.     

Male–Female Association Patterns Among Free-ranging Chimpanzees (Pan troglodytes schweinfurthii)

Although male–female relationships can offer a number of advantages such as protection or social support, they are poorly studied among primates compared to same-sex relationships. We used 12 yr of data from the Kanyawara chimpanzee community to compare three independent measures of association (party association, 5m association, and grooming) among all adult dyads. Party association exhibited by male–female dyads was of intermediate strength between strong male–male and weak female–female association. Male–female dyads were less likely to be within 5m of one another and to groom as male–male dyads, but equally likely to be within 5m and more likely to groom as female–female dyads. Variation in male–female association strength was not related to male rank but was affected by female ranging patterns and female reproductive states. Females with core areas in the center of the home range were more likely to be in parties with males but did not show higher spatial proximity or grooming indices compared to females ranging in the periphery. Party association and 5m indices were higher for dyads of males and estrous females compared to those with anestrous females. These results indicate that male–female dyads are likely to associate with one another more often than female–female dyads because of overlapping ranging patterns and short-term changes in female reproductive state. We conclude that male and female chimpanzees do not exhibit proximity and grooming patterns indicative of strong affiliative bonds. This study also highlights the importance of using multiple independent measures of bond strength in studies of primate social dynamics.     

Complementarity and symmetry in social relationships of nonhuman primates

The paper examinesBateson’s idea that social relationships can be described according to the degree that behavior is symmetric (mutual) or complementary (non-mutual). It was suggested that in primates complementary relationships are most typical and stable.Bateson’s definitions were quantified and applied to observations of paired rhesus females, showing that familiar dyads had complementary relationships, probably reflecting social status, while unfamiliar dyads had symmetric relationships. Phases of this project were supported by U. S. P. H. S. grants, MH-17052 (toE. W. Hansen) and MH-00322 (Postdoctoral Fellowship).     

Risk is a Component of Social Relationships in Spider Monkeys

In group‐living animals, social relationships are the result of the interactions between two individuals over time and can provide fitness benefits to both the participants. Recently, components of social relationships were identified in Old World primates and ravens through the use of principal component analysis (PCA). We employed PCA to identify components that define the social relationships in two communities of wild spider monkeys in the Yucatán Peninsula, Mexico and investigated whether characteristics of the dyads, such as age combination, sex combination and kinship, had an effect on the components obtained. We found two components. Component 1 had high positive loadings of proximity, grooming and subgroup index, which may reflect value or compatibility. Embrace and aggression rates loaded highly on Component 2, which was labelled risk. Component 1 was affected by kinship: kin had higher scores than non‐kin. Both the components were affected by sex combination of the dyad. Male–male dyads had higher scores than female–male and female–female dyads. The results are in accordance with what is currently known about spider monkeys’ social relationships, but provide an additional perspective with the novel component of risk. In this respect, the two components are effective in capturing the ambiguous nature of male–male relationships in spider monkeys. Overall, this study offers further insight into the social patterns underlying the relationship quality in group‐living animals and the usefulness of PCA in providing an objective assessment that reflects the animals′ perspective of their social interactions.     

Problem Solving in the Presence of Others: How Rank and Relationship Quality Impact Resource Acquisition in Chimpanzees (Pan troglodytes)

In the wild, chimpanzees (Pan troglodytes) are often faced with clumped food resources that they may know how to access but abstain from doing so due to social pressures. To better understand how social settings influence resource acquisition, we tested fifteen semi-wild chimpanzees from two social groups alone and in the presence of others. We investigated how resource acquisition was affected by relative social dominance, whether collaborative problem solving or (active or passive) sharing occurred amongst any of the dyads, and whether these outcomes were related to relationship quality as determined from six months of observational data. Results indicated that chimpanzees obtained fewer rewards when tested in the presence of others compared to when they were tested alone, and this loss tended to be greater when paired with a higher ranked individual. Individuals demonstrated behavioral inhibition; chimpanzees who showed proficient skill when alone often abstained from solving the task when in the presence of others. Finally, individuals with close social relationships spent more time together in the problem solving space, but collaboration and sharing were infrequent and sessions in which collaboration or sharing did occur contained more instances of aggression. Group living provides benefits and imposes costs, and these findings highlight that one cost of group living may be diminishing productive individual behaviors.     

Chimpanzees empathize with group mates and humans,but not with baboons or unfamiliar chimpanzees

Human empathy can extend to strangers and even other species, but it is unknown whether non-humans are similarly broad in their empathic responses. We explored the breadth and flexibility of empathy in chimpanzees, a close relative of humans. We used contagious yawning to measure involuntary empathy and showed chimpanzees videos of familiar humans, unfamiliar humans and gelada baboons (an unfamiliar species). We tested whether each class of stimuli elicited contagion by comparing the effect of yawn and control videos. After including previous data on the response to ingroup and outgroup chimpanzees, we found that familiar and unfamiliar humans elicited contagion equal to that of ingroup chimpanzees. Gelada baboons did not elicit contagion, and the response to them was equal to that of outgroup chimpanzees. However, the chimpanzees watched the outgroup chimpanzee videos more than any other. The combination of high interest and low contagion may stem from hostility towards unfamiliar chimpanzees, which may interfere with an empathic response. Overall, chimpanzees showed flexibility in that they formed an empathic connection with a different species, including unknown members of that species. These results imply that human empathic flexibility is shared with related species.     

Dynamics of the temporal structures of playing clusters and cliques among wild chimpanzees in Mahale Mountains National Park

The overall structure and temporally changing configuration of members of social play among the wild chimpanzees (Pan troglodytes schweinfurthii) of Mahale Mountains National Park, Tanzania, were described on both the microscopic ‘clique’ levels, conceptualized as directly connected configurations through social play behavior, and macroscopic ‘cluster’ levels, conceptualized as indirectly connected gatherings of members of adjacent multiple cliques at the same time and space. Most playing clusters started as dyads. Although the cumulative number of participants increased, each clique size remained at 2 for most of the observational units. Dyadic cliques were more stable and lasted longer than larger cliques. Of all clusters’ playing fields, 64.7 % had maximum diameters of 3 m. In summary, chimpanzees played stably in dyadic pairs in most of the time. As time passed, other chimpanzees often joined in the playing groups to form large polyadic clusters. Even when all chimpanzees in a cluster played socially at the same time, they normally did so in separate dyadic pairs, forming multiple dyadic cliques simultaneously in a small space. These social play dynamics may be explained assuming a hypothesis based on a balance model among socially playing chimpanzees, as the balanced cliques are limited only to those in which all the existing pairs form the mutual dyads, and they tend to avoid unbalanced and maintain balanced relationships during social play. As a result, larger cliques were difficult to maintain for long periods and tended to transition into dyadic mutual cliques. Thus, Heider’s balance theory can be one of the possible theories to explain not only human social phenomena, but also the proximate mechanism of the structure and the temporal change of social play among wild chimpanzees. Although both mutual and transitive relationships are known to be balanced in various human networks, only mutual relationships among socially playing chimpanzees were balanced.     

Components of Relationship Quality in Chimpanzees

A novel approach to studying social relationships in captive adult chimpanzees ( Pan troglodytes ) was taken by using principal components analysis (PCA) to extract three key components of relationship quality from nine behavioural variables. Based on the loadings of the behavioural variables, the components appeared to match previously hypothesized critical aspects of social relationships and were therefore labelled Value, Compatibility and Security. The effects of kinship, sex combination, age difference and time spent together on each of the relationship quality components were analysed. As expected, kin were found to have more valuable, compatible and secure relationships than non-kin. Female–female dyads were found to be more compatible than male–male or mixed-sex dyads, whereas the latter were found to be most secure. Partners of a similar age were found to have more secure and more valuable relationships than those with a larger age gap. Individuals that were together in the group for longer were more valuable and more compatible, but their relationships were found to be less secure than individuals that were together in the group for a shorter time. Although some of the results may be unexpected based on chimpanzee socio-ecology, they fit well overall with the history and social dynamics of the study group. The methods used confer a significant advantage in producing quantitative composite measures of each component of relationship quality, obtained in an objective manner. These findings therefore promote the use of such measures in future studies requiring an assessment of the qualities of dyadic social relationships.     

Reproductive Parameters of Female<Emphasis Type="Italic">Pan paniscus</Emphasis> and <Emphasis Type="Italic">P. troglodytes</Emphasis>: Quality versus Quantity

We investigated intra- and interspecific differences in life history and reproductive parameters in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). We compare the parameters of wild and captive females in order to shed light on the influence of habitat or specific differences or both on reproduction. We present new and additional information on reproductive parameters from captive bonobos and chimpanzees. Captive chimpanzees birth more live offspring and have a shorter interbirth interval, but experience higher infant mortality than captive bonobos. Although captive bonobo females tend to start reproduction at a younger age than chimpanzees, this is effectively only so for wild-born females of both species. Ultimately both species reach the same rate of production of offspring surviving to 5 yr. These results contrast with data from the wild. Wild bonobos tend to have higher reproductive success, a higher fertility rate and a shorter interbirth interval than wild chimpanzees. Reproduction is similar for wild and captive bonobos, which suggests that they are producing at their maximum under both conditions. Overall captive chimpanzees perform better than their wild conspecifics, probably because of lower feeding competition. Infant survival is the only specific difference not affected by captivity. Bonobo infants survive better, which suggests that chimpanzee infants are more at risk. We argue that the interspecific variation in reproductive parameters in captivity is related to the different influence of captivity on reproduction and different pressures of external sources of infant and juvenile mortality.     

Social relationships and ritualized greetings in adult male baboons (Papio cynocephalus anubis)

Greetings involving exchanges of ritualized sexual gestures are a common form of interaction among adult male baboons, although relatively little attention has been paid to them. In this study, we investigate how greetings reflect important aspects of the male's social relationships, including dominance rank, age/residence status, and cooperative tendencies. The results are based on over 600 greetings among 12 adult males recorded during a 4-month study of a troop of wild olive baboons near Gilgil, Kenya. Four of the adult males were older, lower-ranking, long-term residents, which frequently formed coalitions to take estrous females away from the eight young, higher-ranking males. Virtually all dyads greeted: greetings occurred more than twice as often as other types of male-male interactions; and nearly all greetings occurred in a neutral context, in which there was no resource at stake. The percentage of greetings completed, the frequency with which different gestures were employed, and the roles adopted by each male varied significantly across old-old, old-young, and young-young dyads. Greetings between young adult males were often interrupted or actively resisted, consistent with their unstable and ambiguous dominance relationships. Greetings between old-old dyads were usually completed and appeared consistent with their cooperative relationships. One pair of old males formed a stable, reciprocal coalition against young males, and this pair's greetings showed remarkable symmetry of roles. Greetings, we hypothesize, function to allow males to negotiate important aspects of their relationships, including cooperation.     

Demographic and Female Life History Parameters of Free-Ranging Chimpanzees at the Chimpanzee Rehabilitation Project, River Gambia National Park

We analyzed fertility and mortality records for 113 provisioned, free-ranging chimpanzees at the River Gambia National Park, The Gambia. The chimpanzees are rehabilitated orphans released by the Chimpanzee Rehabilitation Project (CRP), and their descendants born in a natural environment. Females experienced their 1st births at an average age of 14.3 yr, with average interbirth intervals of 68 mo. Despite limited provisioning, reproductive parameters in both released and 1st-generation females resembled those of wild chimpanzees and showed seasonal fluctuations. Mortality rates were low compared to those for wild chimpanzees, particularly for infants and juveniles; life expectancy at birth was 23.6 yr for females and 18 yr for males. The results have implications for our understanding of variation in reproductive parameters between captive and wild chimpanzees. We also discuss issues related to chimpanzee conservation and captive rearing.     

Social familiarity relaxes the constraints of limited attention and enhances reproduction of group‐living predatory mites

In many group‐living animals, within‐group associations are determined by familiarity, i.e. familiar individuals, independent of genetic relatedness, preferentially associate with each other. The ultimate causes of this behaviour are poorly understood and rigorous documentation of its adaptive significance is scarce. Limited attention theory states that focusing on a given task has interrelated cognitive, behavioural and physiological costs with respect to the attention paid to other tasks. In multiple signal environments attention has thus to be shared among signals. Assuming that familiar neighbours require less attention than unfamiliar ones, associating with familiar individuals should increase the efficiency in other tasks and ultimately increase fitness. We tested this prediction in adult females of the group‐living, plant‐inhabiting predatory mite Phytoseiulus persimilis. We evaluated the influence of social familiarity on within‐group association behaviour, activity, predation and reproduction. In mixed groups (familiar and unfamiliar), familiar predator females preferentially associated with each other. In pure groups (either familiar or unfamiliar), familiar predator females produced more eggs than unfamiliar females at similar predation rates. Higher egg production was correlated with lower activity levels, indicating decreased restlessness. In light of limited attention theory, we argue that the ability to discriminate between familiar and unfamiliar individuals and preferential association with familiar individuals confers a selective advantage because familiar social environments are cognitively and physiologically less taxing than unfamiliar social environments.     

Aggression with mixed age-sex groups of bolivian squirrel monkeys following single animal introductions and new group formations

The social organization of the Bolivian squirrel monkey (Saimiri boliviensis boliviensis) is thought to be sexually segregated, with males and females forming separate social groups during the nonbreeding season. To investigate the influence of this social order on patterns of aggression, controlled single animal introductions within established groups and establishment of new groups were studied in a systematic manner. Behavioral observations were made using an all-occurrences technique to sample all agonistic interactions. In study I, 4 animals of each age-sex class (adult males and females, juvenile males and females) were introduced one at a time into 4 different social groups composed of 1 adult male and 8 to 10 adult females. Behavioral observations were made prior to and after the introductions. Newly introduced adult males received significantly more contact aggression than other age classes. Only the adult females increased aggression after the introduction of new animals. In study II, new social groups were formed and behavioral observations were made following formation. One group was formed from 7 pairs of familiar females and an unfamiliar adult male. This group had a high frequency of aggression during the first half hour, with contact aggression rising to peaks at 3 and 5 h. The second group consisted of 10 familiar females, 2 pairs of familiar females and an unfamiliar male. There was a significant peak in contact aggression 3 h into the observation.     

Fifty years of chimpanzee demography at Taronga Park Zoo

There has been a captive Pan troglodytes colony at Taronga Park Zoo in Sydney, Australia, since the mid-1930s. Demographic data on these animals were first analyzed in 1986; however, further information collected for 15 years since then is now available. The reproductive histories of 33 females in the colony have been recorded, and these data form the largest collection of captive chimpanzee data from a setting that has involved natural breeding conditions since the mid-1960s. These data were analyzed in conjunction with data from wild populations to establish the degree of variability present within chimpanzee reproductive parameters, and to identify which distinctive life history characteristics persist in well-provisioned, natural-fertility populations. The age at first birth for the chimpanzee females is 9.8 yr on average (n=16), which is 1-4.8 yr earlier than the average for wild populations. In line with this accelerated reproduction, birth intervals are also significantly shorter than those in noncaptive chimpanzee populations. The median birth interval for all surviving infants (based on a Kaplan-Meier survival analysis) is 49 months (n=43) compared to 62+ months for wild groups. At the same time, infant mortality remains high. The data confirm distinctive features of the life history of common chimpanzees, including later maturation, long birth intervals, a relatively invariant fertility schedule, and high juvenile mortality. However, aspects of both fertility and mortality are significantly related to social circumstances, indicating that in common chimpanzees, as in humans, life history characters may represent ecological and social adaptations rather than species-fixed characteristics.     

Kinship and social bonds in female chimpanzees (Pan troglodytes)

A large body of theoretical and empirical research suggests that kinship influences the development and maintenance of social bonds among group‐living female mammals, and that human females may be unusual in the extent to which individuals form differentiated social relationships with nonrelatives. Here we combine behavioral observations of party association, spatial proximity, grooming, and space use with extensive molecular genetic analyses to determine whether female chimpanzees form strong social bonds with unrelated individuals of the same sex. We compare our results with those obtained from male chimpanzees who live in the same community and have been shown to form strong social bonds with each other. We demonstrate that party association is as good a predictor of spatial proximity and grooming in females as it is in males, that the highest party association indices are consistently found between female dyads, that the sexes do not differ in the long‐term stability of their party association patterns, and that these results cannot be explained as a by‐product of the tendency of females to selectively range in particular areas of the territory. We also show that close kin (i.e. mother–daughter and sibling dyads) are very rare, indicating that the vast majority of female dyads that form strong social bonds are not closely related. Additional analyses reveal that “subgroups” of females, consisting of individuals who frequently associate with one another in similar areas of the territory, do not consist of relatives. This suggests that a passive form of kin‐biased dispersal, involving the differential migration of females from neighboring communities into subgroups, was also unlikely to be occurring. These results show that, as in males, kinship plays a limited role in structuring the intrasexual social relationships of female chimpanzees. Am. J. Primatol. 71:840–851, 2009. © 2009 Wiley‐Liss, Inc.     

Familiarity and partner preferences in female common voles, <Emphasis Type="Italic">Microtus arvalis</Emphasis>

Captive female common voles (Microtus arvalis) had a clear social preference for familiar males in a standard preference test. Cohabitation for a short period resulted in preferences for familiar partners, and females spent eight times more time in body contact with a familiar male than with an unfamiliar male. Females also displayed stranger-directed aggression. Our results suggest that the common vole is a species with selective partner preferences and a tendency to form tight social relationships and stable male–female associations.     

Spatial Association in a Highly Inbred Ungulate Population: Evidence of Fine-Scale Kin Recognition

We present the first evidence of fine-scale kin recognition, based on a continuous measure of relatedness, in ungulates. The spatial association between herdmates of a captive population of aoudad ( Ammotragus lervia ), where all the individuals are related, is analysed during resting time. Our goal was to estimate which factors influence individuals' associations. The study population is highly inbred, although it does not show serious deleterious effects caused by consanguinity. It comprises a single captive herd, reproducing freely and in good conditions for more than 10 yr. It emerges that kin, measured as the coefficient of relationship between two given herdmates, is the main factor determining the spatial association (e.g. average distance) of male–male and female–female dyads, as more-related individuals tend to rest closer to each other than less-related ones. As for male–female dyads, individuals of a similar age tend to stay closer. To rule out any familiarity confounding effects, individuals' cohabitation time in the herd was added as a random factor in the analyses. Concerning the type of dyad, mother–calf dyads are characterized by higher proximity than others, particularly during the suckling period, whereas males tend to stay closer to each other than females or male–female dyads, being also more kin-related. Female social rank does not influence spatial association between herdmates. These results are related to group composition of the species in the wild, which are characterized by intense mother–calf bonds and all-male groups that are probably kin-related. It is seen that adult male–female associations are not related to kinship, but to age similarity, which is in accord with the assumption that main family groups in the wild are formed by matrilineal lines, whereas males are the dispersing sex.     

Conflict Resolution in Chimpanzees and the Valuable-relationships Hypothesis

Reconciliation, or peaceful postconflict interaction, can restore the usual pattern of interaction between social partners after open conflict has disrupted it—i.e., it can resolve conflicts. Researchers have documented reconciliation in >20 primate species, but the tendency to reconcile typically varies among dyads and dyad classes. The valuable-relationships hypothesis proposes that differences in the value of social relationships account for much of this variation. Value depends on how likely partners are to act in ways that benefit each other, where the benefits are ultimately direct or indirect increases in fitness. Researchers have responded to studies that have tested predictions of the hypothesis with extensive, if not universal, support. For example, kin show higher conciliatory tendencies than nonkin in many species, and conciliatory tendencies between unrelated females are high in several cercopithecines in which nonkin agonistic support is important for rank acquisition and maintenance. However, most of the support is indirect, because we lack direct evidence on the link between assays of relationship value and fitness. Also, some studies have methodological weaknesses, e.g., analyses based on pooled data and insufficient sample sizes. I review evidence in favor of the hypothesis with special attention to studies that come closest to providing evidence for predicted fitness effects. I also present new data on postconflict interactions between adult male chimpanzees at Ngogo that show how often pairs of males formed coalitions and how much time they spent grooming influenced the likelihood that they would reconcile after conflicts, and that allies were particularly likely to reconcile and to do so by grooming each other. The most important future research direction is to integrate detailed data on conflict management, analyzed at the level of dyads, with long-term data on reproductive success, such as that now available from several study sites, on the same populations.     

Food Competition and Linear Dominance Hierarchy Among Female Chimpanzees of the Taï National Park

Dominance rank in female chimpanzees correlates positively with reproductive success. Although a high rank obviously has an advantage for females, clear (linear) hierarchies in female chimpanzees have not been detected. Following the predictions of the socio-ecological model, the type of food competition should affect the dominance relationships among females. We investigated food competition and relationships among 11 adult female chimpanzees in the Taï National Park, Côte d'Ivoire (West Africa). We detected a formal linear dominance hierarchy among the females based on greeting behaviour directed from the subordinate to the dominant female. Females faced contest competition over food, and it increased when either the food was monopolizable or the number of competitors increased. Winning contests over food, but not age, was related to the dominance rank. Affiliative relationships among the females did not help to explain the absence of greetings in some dyads. However comparison post hoc among chimpanzee study sites made differences in the dominance relationships apparent. We discuss them based on social relationships among females, contest competition and predation. The cross-site comparison indicates that the differences in female dominance hierarchies among the chimpanzee study sites are affected by food competition, predation risk and observation time.     

Female Coalitions Against Male Aggression in Wild Chimpanzees of the Budongo Forest

In the wild, female chimpanzees (Pan troglodytes) are subject to male aggression that at times can be prolonged or particularly violent. There are no reports of cooperative retaliation to such aggression, a strategy observed in the congeneric Pan paniscus, from the wild despite >4 decades of detailed behavioral study across a number of populations and its occurrence among captive female chimpanzees. If the reports from captivity represent an inherent capacity, then the absence of similar reports from wild populations suggests that females may be able to form coalitions only under appropriate ecological and demographic conditions. During a study of male and female aggressive interactions among chimpanzees of the Budongo Forest, Uganda, wild adult female chimpanzees sometimes formed coalitions with one another to retaliate against male aggression. This may be possible because these females tend to be more gregarious than in other populations of East African chimpanzees, as other studies of the same population have suggested; the extent and variation of female chimpanzee social strategies may, therefore, need reconsideration. Further, my observations strengthen the argument that at least some of the differences between chimpanzees and bonobos may be more of degree than of kind.