Grooming and the Expectation of Reciprocation in Mandrills (<Emphasis Type="Italic">Mandrillus sphinx</Emphasis>)

It is often (implicitly) assumed that the expectation of reciprocation motivates animal altruism, and thus that animals “plan” their social interactions. We tested this hypothesis by studying a captive group of mandrills (Mandrillus sphinx). In our focal group, the alpha male was more likely to provide agonistic support in the minutes after the receipt of grooming than in the absence of previous grooming. This offered other group members the possibility of manipulating the male’s support by grooming him before engaging in an aggression. We used survival analysis to test the hypothesis that the other group members systematically groomed the alpha male just before engaging in aggression, which would suggest that the expectation of reciprocation motivated their grooming. Contrary to the prediction of our hypothesis, we found that other group members did not groom the alpha male just before engaging in aggression, and thus did not benefit from increased support from the most effective ally. These results suggest that mandrills do not plan their social interactions and that the expectation of reciprocation does not motivate them to groom.     

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.     

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

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

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.     

'Friendship' for fitness in chimpanzees?

It has been repeatedly suggested that primates trade social services for fitness benefits in their relationships with the opposite sex. We tested this proposal in a colony of captive chimpanzees, Pan troglodytes, by examining behavioural data on grooming, agonistic support and food sharing in relation to genetically established paternity. We found no support for the notion of trade. First, males did not sire more offspring with females that they actively groomed more frequently, that they supported more often or with which they shared food more frequently. Correspondingly, females did not give birth to more offspring sired by males from which they received more services. Second, males that showed more affiliative behaviour towards females in general did not sire more progeny. Furthermore, females did not bear more offspring sired by males to which they themselves directed more sociopositive behaviour. Results from this captive colony are compatible with those reported for chimpanzees under natural conditions. Copyright 1999 The Association for the Study of Animal Behaviour.     

Reciprocation and interchange in wild Japanese macaques: grooming, cofeeding, and agonistic support

Social primates spend a significant proportion of their time exchanging grooming with their group companions. Although grooming is mainly exchanged in kind, given its hygienic and tension-reducing functions, it is still debated whether grooming also provides some social benefits, such as preferential access to resources (e.g., food or mating partners). In this study we analyzed grooming distribution among wild female Japanese macaques living in two groups on Yakushima. We tested the tendency of monkeys to reciprocate the amount of grooming received, and to direct their grooming up the hierarchy. Then we analyzed the relation of grooming to three of its possible benefits: reduced aggression, increased tolerance over food, and agonistic support against a male aggressor. The data were analyzed by means of row-wise matrix correlations. Grooming was highly reciprocated (i.e., exchanged in kind) and directed up the hierarchy in both the study groups. No significant relationship was found between grooming and aggression. Conversely, grooming favored tolerance over food, since it was positively correlated with presence on the same food patch, close proximity, and close approaches (both within 1 m) during feeding. Grooming was also positively related to agonistic support against adult males, although this relationship became nonsignificant when we controlled for kinship. Although these results are not definitive, they suggest that monkeys may derive various social benefits from grooming. This conclusion is supported by the fact that in various primate species animals tend to prefer high-ranking individuals as grooming partners.     

Alpha male chimpanzee grooming patterns: implications for dominance “style”

In social primates, individuals use various tactics to compete for dominance rank. Grooming, displays and contact aggression are common components of a male chimpanzee's dominance repertoire. The optimal combination of these behaviors is likely to differ among males with individuals exhibiting a dominance “style” that reflects their tendency to use cooperative and/or agonistic dominance tactics. Here, we examine the grooming behavior of three alpha male chimpanzees at Gombe National Park, Tanzania. We found that (1) these males differed significantly in their tendency to groom with other males; (2) each male's grooming patterns remained consistent before, during and after his tenure as alpha, and (3) the three males tended to groom with high‐ middle‐ and low‐ranking partners equally. We suggest that body mass may be one possible determinant of differences in grooming behavior. The largest male exhibited the lowest overall grooming rates, whereas the smallest male spent the most time grooming others. This is probably because large males are more effective at physically intimidating subordinates. To achieve alpha status, a small male may need to compensate for reduced size by investing more time and energy in grooming, thereby ensuring coalitionary support from others. Rates of contact aggression and charging displays conformed to this prediction, suggesting that each male exhibited a different dominance “style.” Am. J. Primatol. 71:136–144, 2009. © 2008 Wiley‐Liss, Inc.     

The trade balance of grooming and its coordination of reciprocation and tolerance in Indonesian long-tailed macaques (<Emphasis Type="Italic">Macaca fascicularis</Emphasis>)

We collected data on grooming, proximity, and aggression in long-tailed macaques (Macaca fascicularis) in Kalimantan, Indonesia. We used this data to study how grooming influenced a receiver's (B) behavior towards the bout's initiator (A). In our first analysis, post-grooming samples were collected after A groomed B. These were compared to matched-control samples of similar conditions but A had not previously groomed B. This comparison was performed on 26 individuals (16 female, 3 male, 7 immature) and tested whether A's initial act of grooming increased the pair's time in proximity and the amount of time B groomed A. We also tested if A's grooming decreased B's aggression towards A per time in proximity. Rates of B-->A aggression per time in proximity with A for 39 individuals (18 female, 5 male, 16 immature) were compared between post-grooming and focal sample data. Finally, we studied 248 grooming bouts to test if the first two grooming episodes were time matched. We assessed the influence of age, sex, rank and inferred kinship on time matching, and controlled for individual variation and tendency to groom using a general linear mixed model. Our results showed that A-->B grooming acted to increase B-->A grooming and the pair's proximity, while lowering B-->A aggression. Despite these effects, episodes in grooming bouts were generally not matched, except weakly among similar partners (i.e., female pairs and immature pairs). Grooming imbalance was greatest across age-sex class (i.e., male-female and adult-immature pairs). In similar pairs, grooming duration was skewed in favor of high-ranking individuals. We conclude grooming established tolerance and increased the likelihood that grooming reciprocation would occur, but grooming durations were not typically matched within bouts. Lack of time matching may be the result of grooming that is performed to coordinate interchanges of other social services.     

Social grooming and play behavior of a captive group of chimpanzees

Aspects of the social grooming and play behavior of a group of six adolescent and young adult chimpanzees are contrasted and compared. Eleven months’ data indicate that older chimpanzees groomed more and played less than younger individuals. This transition period occurred earlier for females than males. Grooming behavior appeared to vary with reproductive state. A positive correlation was found between the estrous condition of cycling females and the amount of grooming that they received from the males. A mother of a young infant received particularly high levels of grooming from the other group members. Less variation among individuals was found for frequencies of play as compared to grooming. Play dropped following the death of one individual and was entirely inhibited for three weeks following the group’s transfer to a new environment and the reintroduction of a former group member. Comparison to a free-ranging population indicates important differences in both frequencies and general patterns of play and grooming.     

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.     

Grooming coercion and the post-conflict trading of social services in wild Barbary macaques

In animal and human societies, social services such as protection from predators are often exchanged between group members. The tactics that individuals display to obtain a service depend on its value and on differences between individuals in their capacity to aggressively obtain it. Here we analysed the exchange of valuable social services (i.e. grooming and relationship repair) in the aftermath of a conflict, in wild Barbary macaques (Macaca sylvanus). The relationship repair function of post-conflict affiliation (i.e. reconciliation) was apparent in the victim but not in the aggressor. Conversely, we found evidence for grooming coercion by the aggressor; when the victim failed to give grooming soon after a conflict they received renewed aggression from the aggressor. We argue that post-conflict affiliation between former opponents can be better described as a trading of social services rather than coercion alone, as both animals obtain some benefits (i.e. grooming for the aggressor and relationship repair for the victim). Our study is the first to test the importance of social coercion in the aftermath of a conflict. Differences in competitive abilities can affect the exchange of services and the occurrence of social coercion in animal societies. This may also help explain the variance between populations and species in their social behaviour and conflict management strategies.     

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

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

Long-term reciprocation of grooming in wild West African chimpanzees

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

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 relationships among adult female baboons

Adult female baboons were studied over a 15-month period which included sexual cycling, pregnancy, and lactation. Females could be ranked in a linear dominance hierarchy which accurately predicted the direction, but not the frequency, of agonistic interactions. Females were most attractive to others during lactation, receiving less aggression, more friendly gestures, more grooming, and grooming by more different individuals than females in other reproductive states. In all three reproductive states high-ranking females were more attractive than others. When differences in behaviour related to changes in reproductive state were factored out, individual females groomed animals next to themselves in the dominance hierarchy more than others. A model is presented showing how rank-relaed access and attractiveness may interact to perpetuate this distribution of grooming over time.     

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.     

Reconciliation in Captive Chimpanzees: A Reevaluation with Controlled Methods

Affiliative postconflict reunions—reconciliations—of former opponents were first demonstrated in the chimpanzees at the Arnhem Zoo. Since then methods have been considerably refined, and reconciliation has been demonstrated in a large number of primates and also some gregarious nonprimates. This study, conducted with a different captive group, is the first to use the revised methodology with chimpanzees. We analyzed a total of 297 agonistic conflicts with the PC–MC method: we observed focal individuals for 15 min after a conflict and during matched control observations the next day. The mean conciliatory tendency of the 16 chimpanzees was 41%, with a range in different age-sex classes of 58% (among adult females) to 19% (among adult vs. immature males). After conflicts, former opponents were selectively attracted to one another. Preferential contact with previous opponents persisted when activity level during matched controls was controlled for statistically. Opponents that were frequent grooming partners reconciled more frequently, but the frequency of agonistic support had no such effect. Our findings thus confirm the existence of reconciliation in chimpanzees, which show one of the highest conciliatory tendencies among primate species.     

Dominance in assamese macaques (Macaca assamensis)

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

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.     

Response of Rhesus Macaques (Macaca mulatta) to the Body of a Group Member That Died from a Fatal Attack

Among animals that form social bonds, the death of a conspecific may be a significant social event, representing the loss of an ally and resulting in disruptions to the dominance hierarchy. Despite this potential biological importance, we have only limited knowledge of animals’ reactions to the death of a group member. This is particularly true of responses to dead adults, as most reports describe the responses of mothers to dead infants. Here, we describe in detail and provide video evidence of the behavioral responses of a group of free-ranging rhesus macaques (Macaca mulatta) immediately after the death of a mid-ranking adult male as a result of a fatal attack. High-ranking male members of the group, suspected to have carried out the attack, dragged and bit the dead body, exhibiting a rate of aggression 20 times greater than baseline levels. Lower-ranking individuals approached and inspected the body by looking closely, smelling, and grooming the fur. There was inconclusive evidence that these rhesus macaques found the death of a conspecific stressful: Levels of grooming between group members after the fatal attack were significantly higher than baseline levels, and higher than levels of grooming after nonfatal attacks. However, when grooming levels were adjusted based on the assumption that individuals positioned close to the body, i.e., those visible to researchers, were more likely to be engaged in grooming than those positioned farther away, this difference from baseline was no longer significant. The rate of self-directed behaviors after the fatal attack was also not different from baseline. Many of the behaviors we observed directed toward the body (aggression, inspection) have been previously reported in chimpanzees and geladas, and are similar to reactions sometimes displayed by humans. As such, this report represents a potentially valuable contribution the nascent field of nonhuman primate thanatology.