Urinary oxytocin and social bonding in related and unrelated wild chimpanzees

Animals that maintain cooperative relationships show gains in longevity and offspring survival. However, little is known about the cognitive or hormonal mechanisms involved in cooperation. Indeed, there is little support for a main hypothesis that non-human animals have the cognitive capacities required for bookkeeping of cooperative exchanges. We tested an alternative hypothesis that cooperative relationships are facilitated by an endocrinological mechanism involving oxytocin, a hormone required for bonding in parental and sexual relationships across mammals. We measured urinary oxytocin after single bouts of grooming in wild chimpanzees. Oxytocin levels were higher after grooming with bond partners compared with non-bond partners or after no grooming, regardless of genetic relatedness or sexual interest. We ruled out other possible confounds, such as grooming duration, grooming direction or sampling regime issues, indicating that changes in oxytocin levels were mediated by social bond strength. Oxytocin, which is thought to act directly on neural reward and social memory systems, is likely to play a key role in keeping track of social interactions with multiple individuals over time. The evolutionary linkage of an ancestral hormonal system with complex social cognition may be the primary mechanism through which long-term cooperative relationships develop between both kin and non-kin in mammals.     

Social grooming among wild bonobos (Pan paniscus) at Wamba in the Luo Scientific Reserve, DR Congo, with special reference to the formation of grooming gatherings

Chimpanzees (Pan troglodytes) groom in gatherings in which many individuals may be connected via multiple chains of grooming and they often exchange partners with each other. They sometimes groom another while receiving grooming; that is, one animal can play two roles (i.e., groomer and groomee) simultaneously. Although this feature of chimpanzees is notable from the viewpoint of the evolution of human sociality, information on our other closest living relative, the bonobo (Pan paniscus), is still lacking. In this study, I describe grooming interactions of bonobos at Wamba in the Luo Scientific Reserve, Democratic Republic of the Congo (DR Congo), with a particular focus on the formation of grooming gatherings. Like chimpanzees, the bonobos also performed mutual grooming (two individuals grooming each other simultaneously) and polyadic grooming (three or more individuals). However, unlike chimpanzees, these sessions lasted for only a short time. Bonobos rarely groomed another while receiving grooming. Because social grooming occurred not only in trees but also in open spaces, including treefall gaps, the conditions did not necessarily limit the opportunity to make multiple chains of grooming. However, bonobos also engaged in social grooming in different ways from chimpanzees; That is, many individuals were involved simultaneously at a site, in which they separated for dyadic grooming. Some cases clearly showed that bonobos preferred a third party not to join while grooming in a dyad, suggesting that bonobos have a preference for grooming in dyads and that immature individuals formed the preference that was shared among adults while growing up. Most members of the study group ranged together during the majority of the study period. Although bonobos show a fission–fusion grouping pattern, when group members frequently encounter one another on a daily basis, they may not be motivated to form multiple grooming chains at this site, as do chimpanzees.     

Social relationship and hair cortisol level in captive male chimpanzees (<Emphasis Type="Italic">Pan troglodytes</Emphasis>)

Understanding how social relationships affect long-term stress is important because stress has a profound impact on the welfare of animals and social relationships often exert a strong influence on their stress responses. The purpose of this study was to investigate the relationship between social behaviors and long-term stress levels as assessed by hair cortisol (HC) concentration. The subjects were 11 chimpanzees living in an all-male group (divided into two sub-groups) in Kumamoto Sanctuary, Kyoto University, Japan. Behavioral data were collected between December 2014 and March 2015. The total observation time was 129 h. Hair samples were collected in late March and early April 2015, and cortisol was extracted from the hair and measured with enzyme immunoassay. The hair growth rate was estimated to be 1.33 ± 0.06 cm/month. The results revealed that there was a positive correlation between the rate of receiving aggression and HC levels. We also found a significant negative correlation between the balance between giving and receiving grooming (grooming balance index: GBI), which was calculated by subtracting the rate with which grooming is given from that with which it is received, and the rate of receiving aggression and between the GBI and HC levels. Thus, individuals receiving higher levels of aggression also tended to give grooming for relatively long periods compared to the time they were being groomed. In contrast, the rate of initiating aggression did not have a relationship with either HC levels or any measure of social grooming. We did not find social buffering effects, as there was no correlation between mutual social grooming and HC levels. These results show that not only aggressive interactions but also overall social situations in which animals do not have balanced relationships with others might result in the long-term elevation of cortisol levels in captive male chimpanzees.     

No Short‐Term Contingency Between Grooming and Food Tolerance in Barbary Macaques (Macaca sylvanus)

The exchange of services such as allo‐grooming, allo‐preening, food tolerance and agonistic support has been observed in a range of species. Two proximate mechanisms have been proposed to explain the exchanges of services in animals. First, an animal can give a service to a partner depending on how the partner behaved towards it in the recent past. This mechanism is usually tested by examining the within‐dyad temporal relation between events given and received over short time periods. Second, the partner choice mechanism assumes that animals give favours towards specific partners but not others, by comparing how each partner behaved towards them over longer time frames. As such, the partner choice mechanism does not make specific predictions on a temporal contingency between services received and given over short time frames. While there is evidence for a long‐term positive correlation between services exchanged in animals, results for short‐term contingencies between services given and received are mixed. Our study investigated the exchange of grooming for food tolerance in a partially provisioned group of Barbary macaques, by analysing the short‐term contingency between these events. Tolerance over food was compared immediately after grooming and in control condition, using food of different shareability. We found no evidence that grooming increases food tolerance or decrease aggression around food in the short term. Food tolerance was affected by the shareability of the food and the sex of the partners. The exchanges of grooming and food tolerance in non‐human primates may be little affected by recent single events. We suggest that long‐term exchanges between services given and received and social partner choice may play a more important role in explaining social interactions than short‐term contingent events.     

What Does Mutual Grooming Tell Us About Why Chimpanzees Groom?

Grooming might be a resource that is offered in exchange for some benefit (e.g. access to a feeding site or coalitionary support) or it might be a mechanism for building and servicing social relationships, whose function, in turn, is to facilitate the exchange of resources and services. Bi-directional (or simultaneous mutual) grooming is unusually common among chimpanzees (though rare in other primates) and we suggest that this might be because it is an especially strong indicator of social bonding. Because the bonding role of bi-directional grooming offers substantially different predictions from the interpretation offered by the models based on reciprocal altruism (RA), we use a critical tests methodology (i.e. tests that unequivocally support one hypothesis at the expense of the other) to differentiate between the bonding and RA hypotheses. We use data on the dynamics of grooming interactions from a captive group of chimpanzees ( Pan troglodytes ) to show that dominant individuals tolerated the individuals with whom they performed bi-directional grooming more than they did those who typically provided them unidirectional grooming. Dominants rejected and terminated grooming sessions more often with the individuals who provided them with mostly unidirectional grooming than with those with whom they groomed bi-directionally. In addition, animals engaged in bi-directional grooming more often with both relatives and those with whom they were often in proximity. These results support the bonding model of mutually reciprocated grooming at the expense of the RA model, and suggest that, at least in chimpanzees, simultaneous mutual grooming may play a particularly important role in social bonding.     

Interchange of Grooming and Agonistic Support in Chimpanzees

We investigated the temporal relationship between grooming given and agonistic support received in a group of chimpanzees at Chester Zoo, U.K. We compared grooming levels the day before a conflict-with-support to those the day before a conflict-without-support and to baseline to investigate whether individuals groom potential supporters in anticipation of the need for support. We also compared grooming and aggression levels the day after conflicts-with-support to levels the day after conflicts-without-support and to baseline levels to determine whether chimpanzees reward individuals that support them or punish those that do not. Finally, we compared grooming and aggression levels the day after conflicts-with-unsuccessful-solicitations-for-support to those the day after conflicts-with-support and to baseline to examine the behavioral consequences of not providing support when an individual had solicited but did not receive it. Future recipients of support groomed future supporters more the day before receiving support, compared to the day before conflicts-without-support, indicating that grooming increased the likelihood of support. The relationship between prior grooming and support held true only for aggressor and not victim support and is consistent with behavior expected if chimpanzees anticipated the need for agonistic support and groomed their supporter the day before to increase the likelihood of support. We found evidence of a system of reward and punishment. Individuals experienced significantly lower rates of aggression after conflicts in which they provided support than at baseline and after conflicts in which they did not provide support. The finding was true only for aggressor support. We found no evidence that chimpanzees punished individuals whom or that they unsuccessfully solicited with aggression or a reduction in grooming. However, solicitors groomed individuals that they solicited for support significantly more after unsuccessful solicitations than after individuals provided support (but with no difference from baseline), indicating that individuals may attempt to recement their relationship after an unsuccessful solicitation. The findings are consistent with a mechanism of calculated interchange in chimpanzees.     

Sexual Differences in Chimpanzee Sociality

Scientists usually attribute sexual differences in sociality to sex-specific dispersal patterns and the availability of kin within the social group. In most primates, the dispersing sex, which has fewer kin around, is the less social sex. Chimpanzees fit well into the pattern, with highly social philopatric males and generally solitary dispersing females. However, researchers in West Africa have long suggested that female chimpanzees can be highly social. We investigated whether chimpanzees in the Taï Forest (Côte d’Ivoire) exhibit the expected sexual differences in 3 social parameters: dyadic association, party composition, and grooming interactions. Though we found a significant sexual difference in each of the 3 parameters, with males being more social than females, the actual values do not reveal striking differences between the sexes and do not support the notion of female chimpanzees as asocial: females had dyadic association indices comparable to mixed-sex dyads, spent ca. 82% of their time together with other adult chimpanzees, and had a comparable number of grooming partners. Further, female associations can be among the strongest bonds within the community, indicating that both sexes can have strongly favored association partners. The findings are in contrast to reports on East African chimpanzees, the females of which are mainly solitary and rarely interact with other females. Our results suggest that researchers cannot generally regard chimpanzee females as asocial and need to redefine models deriving patterns of sociality from dispersal patterns to integrate the possibility of high female sociality in male philopatric systems.     

Grooming in mandrills and the time frame of reciprocal partner choice

In this study, we examined the time frame of reciprocal partner choice in the grooming interactions of captive mandrills (Mandrillus sphinx) in order to test the hypothesis that the cognitive limitations of primates constrain the occurrence of reciprocation to short time intervals. In contrast to this hypothesis, mandrills groomed preferentially those individuals that groomed them more even when cases of immediate reciprocation were excluded from the analysis. These results show that mandrills were not limited to reciprocating grooming over short time intervals. It is proposed that a system of emotional bookkeeping may support the ability of primates to reciprocate over long time frames. Am. J. Primatol. 71:884–888, 2009. © 2009 Wiley‐Liss, Inc.     

Handedness and Grooming in Pan troglodytes: Comparative Analysis Between Findings in Captive and Wild Individuals

Grooming is a complex set of motor actions, common in highly social primates. We tested for asymmetries in hand use during unimanual and bimanual allogrooming in 215 captive chimpanzees. In addition to hand use, we coded in the ethogram whether the manual grooming action co-occurred with the use of the mouth. Overall, grooming did not elicit strong handedness at the individual level, but there is a small yet significant population-level right-hand bias for bimanual grooming. Mouth use during grooming had no influence on hand use. A comparison of the findings with previously published data on handedness for grooming in wild chimpanzees suggests that wild apes are more right-handed than captive individuals are for allogrooming. Collectively, the results suggest that role differentiation of the hands is an important factor in the assessment of handedness for grooming, and perhaps additional manual actions of chimpanzees and other primates.     

Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees

Humans excel in cooperative exchanges between unrelated individuals. Although this trait is fundamental to the success of our species, its evolution and mechanisms are poorly understood. Other social mammals also build long-term cooperative relationships between non-kin, and recent evidence shows that oxytocin, a hormone involved in parent–offspring bonding, is likely to facilitate non-kin as well as kin bonds. In a population of wild chimpanzees, we measured urinary oxytocin levels following a rare cooperative event—food sharing. Subjects showed higher urinary oxytocin levels after single food-sharing events compared with other types of social feeding, irrespective of previous social bond levels. Also, urinary oxytocin levels following food sharing were higher than following grooming, another cooperative behaviour. Therefore, food sharing in chimpanzees may play a key role in social bonding under the influence of oxytocin. We propose that food-sharing events co-opt neurobiological mechanisms evolved to support mother–infant bonding during lactation bouts, and may act as facilitators of bonding and cooperation between unrelated individuals via the oxytocinergic system across social mammals.     

Grooming interactions among adult chimpanzees at Bossou,Guinea, with special reference to social structure

Grooming and proximity interactions among chimpanzees at Bossou, Republic of Guinea, were analyzed as an index of friendly and affinitive relationships among adult males, among adult females, and between the sexes. Data from the first (1976–1977) and the third (1982–1983) study period were used. The expected value of their interactions was calculated from the number of adult males and females in the group and also from the observed frequency of combinations of adult males and females in the parties (temporary foraging groups). In the pooled data from the two periods, there was little difference between grooming and proximity (without grooming). The frequency of male-female grooming and proximity interactions was lower than expected, and that of female-female interactions was higher than expected. The frequencies of male-male grooming and proximity were intermediate but fluctuated. Male-male grooming frequency was lower than that recorded in chimpanzees of East Africa. Characteristics of same-sex affinitive interactions, especially between Bossou chimpanzee females, clearly differ from those of East African chimpanzees and are more like those recorded for female-related groups of Japanese macaques (Macaca fuscata).These differences indicate the variability and flexibility of chimpanzee social structure.     

Cooperation among Norway Rats: The Importance of Visual Cues for Reciprocal Cooperation,and the Role of Coercion

Some animals reciprocate help, but the underlying proximate mechanisms are largely unclear. Norway rats (Rattus norvegicus) have been shown to cooperate in a variant of the iterated prisoner's dilemma paradigm, yet it is unknown which sensory modalities they use. Visual information is often implicitly assumed to play a major role in social interactions, but primarily nocturnal species such as Norway rats may rely on different cues when deciding to reciprocate received help. We used an instrumental cooperative task to compare the test rats' propensity to reciprocate received help between two experimental conditions, with and without visual information exchange between social partners. Our results show that visual information is not required for reciprocal cooperation among social partners because even when it was lacking, test rats provided food significantly earlier to partners that had helped them to obtain food before than to those that had not done so. The mean decision speed did not differ between the two experimental conditions, with or without visual information. Social partners sometimes showed aggressive behaviour towards focal test individuals. When including this in the analyses to assess the possible role of aggression as a trigger of cooperation, aggression received from cooperators apparently reduced the cooperation propensity, whereas aggression received from defectors increased it. Hence, in addition to reciprocity, coercion seems to provide additional means to generate altruistic help in Norway rats.     

Female contributions to the peaceful nature of bonobo society

Although chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) are closely related, females of the two species show surprisingly large differences in many behavioral aspects. While female chimpanzees tend to range alone or in small parties during non-estrous periods, female bonobos aggregate even more often than do males. Female chimpanzees do not have frequent social interactions with other females, whereas female bonobos maintain close social associations with one another. Although the ranging patterns of chimpanzee parties are generally led by males, female bonobos often take the initiative in ranging behavior. While female chimpanzees usually do not exhibit estrus during postpartum amenorrhea or pregnancy, female bonobos exhibit a prolonged pseudo-estrus during such non-conceptive periods. Studies of these two species have also shown great differences in agonistic behaviors performed by males. Male chimpanzees frequently fight with other males to compete for estrous females, but male bonobos seldom do so. While there are many records of infanticide by male chimpanzees, there is no confirmed record of such an event among bonobos. Several cases of within-group killing among adult male chimpanzees have been reported, but there is no such record for bonobos. While intergroup conflicts among chimpanzees sometimes involve killing members of the other group, intergroup conflicts among bonobos are considerably more moderate. In some cases, bonobos from two different groups may even range together for several days while engaging in various peaceful interactions. I will address two important questions that arise from these comparisons, exploring why females of such closely related species show such clear differences in behavior and whether or not the behavioral characteristics of female bonobos contribute to the peaceful nature of bonobo society.     

Neighbor effect: evidence of affiliative and agonistic social contagion in captive chimpanzees (Pan troglodytes)

Previous studies of captive chimpanzees have demonstrated the "neighbor effect," or social contagion, with respect to agonistic vocalizations and behaviors. The present study considers whether there is a relationship between behavior patterns in focal animals and the auditory signals of neighboring social groups. Using focal-group sampling, we collected 172.5 hr of data on 51 subjects (25 females and 26 males) housed in 10 social groups. We performed two-tailed Wilcoxon matched-pairs signed-rank tests to determine whether the relative frequency of the vocalizations (high vs. low) affected the behaviors. In keeping with past research, we found that agonistic noises and vocalizations from neighboring social groups had a significant effect on the rates of focal-group bluff displays, pant-hoots, and aggression (P<0.05). In addition, we also found significant relationships between grooming behavior and vocalizations in focal groups, and grooming vocalizations from neighboring groups (P<0.05). The results suggest that social contagion is not limited to aggressive behaviors, but also occurs for affiliative behavior patterns.     

The Time Frame of Partner Choice in the Grooming Reciprocation of Cebus apella

Recent theoretical and experimental studies argued that reciprocity is constrained by the cognitive limitations of most animals and that, when reciprocation occurs, it should necessarily be short term. In this study, we examined the time frame of partner choice in the reciprocal grooming of captive female tufted capuchin monkeys ( Cebus apella ). Female capuchins groomed preferentially those individuals that overall groomed them most. Tufted capuchins did sometimes reciprocate grooming immediately. We quantified the time course and probability of immediate reciprocation, and excluded from the analysis cases of immediate reciprocation. We then showed that, even excluding immediate reciprocation, female capuchins still preferred to groom those individuals that groom them most. Our results show that partner choice is not necessarily based on immediate reciprocation and suggest that capuchins are able to reciprocate over longer time frames. These findings argue against the hypothesis that long-term reciprocation is absent in species lacking sophisticated cognitive abilities. We suggest that reciprocal altruism over long time frames relies on a system of emotional bookkeeping.     

The Chimpanzee''s service economy: Food for grooming

Evidence is presented that the reciprocal exchange of social services among chimpanzees (Pan troglodytes) rests on cognitive abilities that allow current behavior to be contingent upon a history of interaction. Food sharing within a captive colony of chimpanzees was studied by means of 200 food trials, conducted on separate daus over a 3-year period, in which 6,972 approaches occurred among the nine adults in the colony. The success rate of each adult, A, to obtain food from another adult, B, was compared with grooming interactions between A and B in the 2 hours prior to each food trial. The tendency of B to share with A was higher if A had groomed B than if A had not done so. The exchange was partner-specific, i.e., the effect of previous grooming on the behavior of food possessors was limited to the grooming partner. Grooming did not affect subsequent sharing by the groomer, only by the groomee. The effect of grooming was greatest for pairs of adults who rarely groomed. Nevertheless, the effect was general: 31 dyadic directions showed an increase in sharing following grooming, and only 11 a decrease. Food possessors actively resisted approaches by individuals who had not groomed them. After food trials there was a significant reduction of grooming by previous possessors towards those individuals with whom they had shared.     

'Gatherings' of social grooming among wild chimpanzees: implications for evolution of sociality

Chimpanzees (Pan troglodytes) often groom in gatherings that cannot simply be divided into unilateral dyadic grooming interactions. This feature of grooming is studied at two different levels: grooming cliques and grooming clusters. Grooming cliques are defined as directly connected configurations of grooming interactions at any given moment, and when any member of a clique successively grooms any member of another clique within 5min and within a distance of 3m, all the members of both cliques are defined as being in the same grooming cluster. Twenty-seven types of cliques are observed, with the largest one consisting of seven individuals. Mutual and/or polyadic cliques account for more than 25% of all cliques. The size of grooming clusters varies from two to 23 individuals, and almost 70% of the grooming time is spent in polyadic clusters. Although adult males groom the longest in relatively smaller clusters (size=2-4), adult females groomed the longest in clusters of five or more individuals. A review of the literature implies that mutual and polyadic cliques occur less often in other primate species than in chimpanzees. The importance of overlapping interactions for these kinds of gatherings and its possible significance in the evolution of sociality is discussed in this article.     

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.     

Grooming-at-a-distance by exchanging calls in non-human primates

The ‘social bonding hypothesis'' predicts that, in large social groups, functions of gestural grooming should be partially transferred to vocal interactions. Hence, vocal exchanges would have evolved in primates to play the role of grooming-at-a-distance in order to facilitate the maintenance of social cohesion. However, there are few empirical studies testing this hypothesis. To address this point, we compared the rate of contact call exchanges between females in two captive groups of Japanese macaques as a function of female age, dominance rank, genetic relatedness and social affinity measured by spatial proximity and grooming interactions. We found a significant positive relationship between the time spent on grooming by two females and the frequency with which they exchanged calls. Our results conform to the predictions of the social bonding hypothesis, i.e. vocal exchanges can be interpreted as grooming-at-a-distance.     

Whom to Groom and for What? Patterns of Grooming in Female Barbary Macaques (Macaca sylvanus)

Grooming is one of the most conspicuous social interactions among nonhuman primates. The selection of grooming partners can provide important clues about factors relevant for the distribution of grooming within a social group. We analyzed grooming behavior among 17 semi-free ranging female Barbary macaques (Macaca sylvanus). We tested whether grooming is related to kinship, rank and friendship. Furthermore, we tested whether grooming is reciprocated or exchanged for rank related benefits (i.e. lower aggression and increased tolerance whilst feeding). We found that in general grooming was reciprocally exchanged, directed up the hierarchy and at the same time affected by friendship and kinship. Grooming was more frequent among individuals with higher friendship values as well as amongst related individuals. We also divided our data set on the basis of rank difference and tested if different power asymmetries between individuals affected the tendency to exchange grooming for rank related benefits and grooming reciprocation. In support of our initial hypothesis our results show that the reciprocation of grooming was a significant predictor of grooming interactions between individuals of similar rank, but not between those individuals more distantly separated in the social hierarchy. However, we did not find any evidence for grooming being exchanged for rank related benefits in either data set. Our results, together with previously published studies, illustrate the behavioral flexibility of macaques. It is clear that multiple studies of the same species are necessary to gather the data required for the solid comparative studies needed to shed light on patterns of grooming behavior in primates.