Trade‐offs in primate grooming reciprocation: testing behavioural flexibility and correlated evolution

Primates may trade altruistic behaviours, such as grooming, either for itself or for different rank‐related benefits, such as tolerance or agonistic support. Ecological conditions are expected to affect competition and thus the steepness of dominance hierarchies. This, in turn, may influence the value of the different currencies that primates exchange. Thus, it can be hypothesized that, as the dominance hierarchy becomes steeper, more grooming is directed up the hierarchy (in exchange for tolerance or agonistic support) and less grooming is exchanged for other grooming. We assembled a large database of within‐group grooming distribution in primates (38 social groups belonging to 16 species and eight genera) and tested these hypotheses both within species (i.e. comparing different groups of the same species) and between species (using comparative methods that control for phylogenetic relatedness). We found within‐species evidence that steeper dominance hierarchies were associated with more grooming being directed up the hierarchy, and that a trade‐off occurred between the tendency to groom up the hierarchy and the degree of grooming reciprocation (although, in some analyses, only a nonsignificant trend was observed). By contrast, phylogenetically controlled comparisons between species did not reveal evidence of correlated evolution between the steepness of the dominance hierarchy, the tendency to direct grooming up the hierarchy, and the degree of grooming reciprocation. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 439–446.     

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

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

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.     

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

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

Grooming reciprocity in female tibetan macaques macaca thibetana

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

The relative roles of kinship and reciprocity in explaining primate altruism

Several hypotheses have been proposed to explain the evolution of altruistic behaviours. Their relative roles in explaining actual cases of animal altruism are, however, unclear. In particular, while kin selection is widely believed to have a pervasive influence on animal behaviour, reciprocity is generally thought to be rare. Despite this general agreement, there has been no direct test comparing the relative roles of kinship and reciprocity in explaining animal altruism. In this paper, we report on the results of such a test based on a meta-analysis of allogrooming in primates, grooming being probably the most common altruistic behaviour among mammals. In direct contrast to the prevailing view, reciprocity played a much larger role than kinship in explaining primate allogrooming. These results point to a more significant role of reciprocity in the evolution of animal altruism than is generally acknowledged.
Ecology Letters (2010) 13: 45–50     

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.     

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.     

The Absence of Grooming for Rank-Related Benefits in Female Assamese Macaques (Macaca assamensis)

Seyfarth’s model of social grooming proposes that by grooming females higher ranking than themselves, females can gain access to important rank-related benefits, such as agonistic support. This, in turn, produces a distinctive pattern of grooming in which females direct their grooming up the female dominance hierarchy and compete for access to the highest ranking individuals. We aimed to test to what extent the grooming behavior of female Assamese macaques (Macaca assamensis) fits the assumptions and predictions of Seyfarth’s model. During two 1-yr sampling periods (October 2007–September 2008, May 2010–April 2011) we collected >2100 focal hours of data from a single wild group in their natural habitat at Phu Khieo Wildlife Sanctuary, Thailand. Subjects included all adult female group members (N?=?12 in 2007/8; N?=?15 in 2010/11). We collected detailed data on grooming interactions, approaches, and departures as well as all aggressive and submissive behaviors between all subjects. We found no evidence that grooming was exchanged for rank-related benefits. In line with this we found no evidence that the grooming of female Assamese macaques fits the pattern predicted by Seyfarth’s model. These results are surprising given that such deviations from Seyfarth’s model are relatively rare among macaques. We propose that our findings are best explained as a lack of a need for rank-related benefits by females in this group.     

An individual-oriented model on the emergence of support in fights, its reciprocation and exchange

Complex social behaviour of primates has usually been attributed to the operation of complex cognition. Recently, models have shown that constraints imposed by the socio-spatial structuring of individuals in a group may result in an unexpectedly high number of patterns of complex social behaviour, resembling the dominance styles of egalitarian and despotic species of macaques and the differences between them. This includes affiliative patterns, such as reciprocation of grooming, grooming up the hierarchy, and reconciliation. In the present study, we show that the distribution of support in fights, which is the social behaviour that is potentially most sophisticated in terms of cognitive processes, may emerge in the same way. The model represents the spatial grouping of individuals and their social behaviour, such as their avoidance of risks during attacks, the self-reinforcing effects of winning and losing their fights, their tendency to join in fights of others that are close by (social facilitation), their tendency to groom when they are anxious, the reduction of their anxiety by grooming, and the increase of anxiety when involved in aggression. Further, we represent the difference in intensity of aggression apparent in egalitarian and despotic macaques. The model reproduces many aspects of support in fights, such as its different types, namely, conservative, bridging and revolutionary, patterns of choice of coalition partners attributed to triadic awareness, those of reciprocation of support and 'spiteful acts' and of exchange between support and grooming. This work is important because it suggests that behaviour that seems to result from sophisticated cognition may be a side-effect of spatial structure and dominance interactions and it shows that partial correlations fail to completely omit these effects of spatial structure. Further, the model is falsifiable, since it results in many patterns that can easily be tested in real primates by means of existing data.     

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.     

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.     

Prosocial primates: selfish and unselfish motivations

Non-human primates are marked by well-developed prosocial and cooperative tendencies as reflected in the way they support each other in fights, hunt together, share food and console victims of aggression. The proximate motivation behind such behaviour is not to be confused with the ultimate reasons for its evolution. Even if a behaviour is ultimately self-serving, the motivation behind it may be genuinely unselfish. A sharp distinction needs to be drawn, therefore, between (i) altruistic and cooperative behaviour with knowable benefits to the actor, which may lead actors aware of these benefits to seek them by acting cooperatively or altruistically and (ii) altruistic behaviour that offers the actor no knowable rewards. The latter is the case if return benefits occur too unpredictably, too distantly in time or are of an indirect nature, such as increased inclusive fitness. The second category of behaviour can be explained only by assuming an altruistic impulse, which—as in humans—may be born from empathy with the recipient''s need, pain or distress. Empathy, a proximate mechanism for prosocial behaviour that makes one individual share another''s emotional state, is biased the way one would predict from evolutionary theories of cooperation (i.e. by kinship, social closeness and reciprocation). There is increasing evidence in non-human primates (and other mammals) for this proximate mechanism as well as for the unselfish, spontaneous nature of the resulting prosocial tendencies. This paper further reviews observational and experimental evidence for the reciprocity mechanisms that underlie cooperation among non-relatives, for inequity aversion as a constraint on cooperation and on the way defection is dealt with.     

Sex differences in nonhuman primate grooming

In this article, sex differences in nonhuman primate social grooming are reviewed. In general, female nonhuman primates groom more than do males. This conclusion is tempered somewhat by acknowledgements of exceptions and qualifications, and by evidence for experiential control of grooming.     

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

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

Grooming, social bonding, and agonistic aiding in rhesus monkeys

An analysis of simultaneous grooming bouts in a captive group of rhesus monkeys (Macaca mulatta) failed to provide evidence of competition to groom high ranking partners. Not only were grooming supplantations rare, but the highest ranking individuals performing grooming did not groom the highest ranking animals receiving grooming. Lower ranking partners, however, did more grooming in nonkin dyads. Grooming partners aided one another in agonistic episodes, but the individual receiving the aid did not groom the individual providing the aid more than vice versa. Kin dyads did aid and groom one another at greater than expected rates, but the aider did not receive the greater proportion of grooming in the dyad. Males participated in more grooming than expected, but their grooming was not related to aiding either with regard to one another or female partners. Animals that were targeted in joint aggression, or aided against, received significantly less grooming from their opponents. A general social relationship expressed in partner preferences, social grooming, and agonistic aiding better explained the observed pattern than any model based on the exchange of services for favors in different currencies.     

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.     

Interplay between various aspects in social relationships of young rhesus monkeys: Dominance,agonistic help,and affiliation

Relationships between group-living primates depend strongly on their position in the group dominance hierarchy and on their relationships with other group members. The influence of various behaviours on social relationships of immature rhesus monkeys (Macaca mulatta) was investigated here. Dominance ranks were established and related to the degree of affiliation in a dyad. Older monkeys were mostly dominant to the younger ones, regardless of kinship. Subordinate monkeys left proximity of their dominant members more often than they were left by them both among siblings and non-siblings, but the effect of dominance rank on the amount of play initiation and grooming in a dyad differed between these two types of dyads. The amount of agonistic help two individuals provided for each other was low among immatures. Nevertheless, pairs of siblings gave help to each other in agonistic conflicts more often than non-siblings, and such help was more often reciprocated between siblings than between non-siblings. Help in agonistic conflicts was positively correlated with the amount of time monkeys spent playing, grooming, or in proximity. Adults tended to interfere less in conflicts of frequent sibling play partners or non-sibling grooming partners. No evidence was found for young monkeys to exchange reciprocally grooming for agonistic help. It is argued that the time monkeys spend interacting with each other in affiliative interactions increases their familiarity and thus promotes close relationships between them. On the whole, young monkeys' relationships, like those between adults, are influenced strongly by their kinship, and position in the dominance hierarchy.     

Grooming and Infant Handling Interchange in <Emphasis Type="Italic">Macaca fascicularis</Emphasis>: The Relationship Between Infant Supply and Grooming Payment

Female long-tailed macaques are attracted to infants and frequently groom mothers bearing them. Such grooming often involves the groomer contacting the infant and may be a trade of grooming for infant handling. To identify if grooming and infant handling are directly traded, I collected samples on times after female-to-mother grooming and on interactions in which a female groomed a mother and contacted her infant. I determined that grooming tended to promote an exchange with infant handling and that the supply of available infants was related to how long a female groomed a mother. Grooming interactions were longer when infants were scarce in the surrounding social environment than when they were abundant, indicating a possible supply-and-demand effect. This supports that grooming may be payment for infant handling. Grooming-infant handling interchanges tended to be unidirectional as mothers usually did not reciprocate grooming. Instead, infant contact occurred. A larger proportion of grooming-infant handling interchanges involved younger infants, but infant age did not seem to influence grooming durations. The length of female-to-mother grooming had no observable effect on handling time. Lower-ranked females groomed higher-ranked mothers and their infants longer than vice versa. Moreover, it was possible to predict up-rank grooming via supply and demand better than down-rank grooming. There was no observable influence of kinship on grooming-infant handling interchange. These results support the conclusion that grooming and infant handling may be traded. Grooming promoted infant handling, while supply and rank predicted the grooming payment a female would offer to access an infant.     

Negotiations over Grooming in Wild Vervet Monkeys (Chlorocebus pygerythrus)

Mutual grooming plays a central role in the establishment and maintenance of social relationships in primates. Allogrooming has two main functions: hygiene and bonding with partners. The duration of grooming bouts is commonly used in studies of the functional aspects of grooming, but few reflect on the proximate mechanisms that determine grooming bout lengths. As it is highly unlikely that groomer and groomee prefer exactly the same bout length, we are likely to observe the result of some form of negotiation. We currently lack information about the signals that primates employ to inform others about their intentions and desires concerning grooming interactions. From October 2006 until April 2007 we studied three behaviors shown in grooming interactions that could potentially have a signaling function in the negotiation process over the initiation and length of grooming bouts among adult females of two vervet groups freely ranging in the Loskop Dam Nature Reserve, South Africa: approaching another individual as far as that resulted in a grooming session, changing of the body position by the groomed individual, and lip smacking. We found that “approach” did not reliably predict which individual would receive grooming first, although approaching individuals groomed significantly more than those approached. Thus, in the context of grooming interactions, moving toward a group member may signal the willingness to invest. Body part presentations appeared to be the main signal used to demand a prolongation of the grooming by the partner. Finally, lip smacking was used under potentially stressful circumstances, notably shortly before using the mouth to groom the partner or an attempt to touch a mother’s infant. Our exploratory study hopefully inspires colleagues to start looking at the role of communication during cooperative interactions for a better appreciation of how animals manage cooperation and negotiate exchange rates.