Grooming and group cohesion in primates: implications for the evolution of language

It is well established that allogrooming, which evolved for a hygienic function, has acquired an important derived social function in many primates. In particular, it has been postulated that grooming may play an essential role in group cohesion and that human language, as verbal grooming or gossip, evolved to maintain group cohesion in the hominin lineage with its unusually large group sizes. Here, we examine this group cohesion hypothesis and test it against the alternative grooming-need hypothesis which posits that rates of grooming are higher in species where grooming need (i.e. the motivation to groom for hygiene and its associated psychological reward) is more pronounced. This alternative predicts that the derived social function of grooming evolved mostly in those lineages that had the highest exposure to ectoparasites and dirt, i.e. terrestrial species. A detailed comparative analysis of 74 species of wild primates, controlling for phylogenetic non-independence, showed that terrestriality was a highly significant predictor of allogrooming time, consistent with the prediction. The predictions of the group cohesion hypothesis were not supported, however. Group size did not predict grooming time across primates, nor did it do so in separate intra-population analyses in 17 species. Thus, there is no comparative support for the group-cohesion function of allogrooming, which questions the role of grooming in the evolution of human language.     

Network cohesion,group size and neocortex size in female-bonded Old World primates

Most primates are intensely social and spend a large amount of time servicing social relationships. In this study, we use social network analysis to examine the relationship between primate group size, total brain size, neocortex ratio and several social network metrics concerned with network cohesion. Using female grooming networks from a number of Old World monkey species, we found that neocortex size was a better predictor of network characteristics than endocranial volumes. We further found that when we controlled for group size, neocortex ratio was negatively correlated with network density, connectivity, relative clan size and proportional clan membership, while there was no effect of neocortex ratio on change in connectivity following the removal of the most central female in the network. Thus, in species with larger neocortex ratios, females generally live in more fragmented networks, belong to smaller grooming clans and are members of relatively fewer clans despite living in a closely bonded group. However, even though groups are more fragmented to begin with among species with larger neocortices, the removal of the most central individual does cause groups to fall apart, suggesting that social complexity may ultimately involve the management of highly fragmented social groups while at the same time maintaining overall social cohesion. These results emphasize a need for more detailed brain data on a wider sample of primate species.     

Grooming Between Male Chimpanzees at Ngogo,Kibale National Park. I. Partner Number and Diversity and Grooming Reciprocity

Allogrooming serves many social functions in primates. Grooming can help individuals to service social relationships generally, sometimes reciprocally, and may be particularly important in the development and maintenance of alliances. However, time constraints limit the number of partners with whom one individual can groom enough to maintain cooperative relationships. As a result, the size of its grooming network may reach an asymptote as the size of its group increases, and it may distribute its grooming less equally among potential partners. Chimpanzees live in multimale, fission-fusion communities; males are philopatric, and commonly associate and groom with each other. Males form within-community alliances that influence dominance rank and access to mates, and allies groom with each other regularly; males also cooperate in aggression between communities. The chimpanzee community at Ngogo, in Kibale National Park, Uganda, is unusually large and has more males than any other known community. Field data show that adult Ngogo males groomed far more with other adult males than with females or with adolescent males, in contrast to a previous report (Ghiglieri, 1984). Adolescent males groomed adults much more than the reverse; males groomed and were groomed by females about equally. Individual males groomed mostly with a small number of other males. On average, males at Ngogo had only slightly more male grooming partners overall and had the same number of important partners as those of males in a much smaller community in the Mahale National Park, Tanzania, and they distributed their grooming less equitably. These results fit those expected if limits on available grooming time cause males to have a loyalty problem as the number of potential grooming and alliance partners increases. Despite differences in the extent and equitability of their grooming networks, males at both Ngogo and Mahale showed reciprocity in grooming. Grooming reciprocity has been demonstrated for captive chimpanzee males, but the Ngogo findings are the first demonstrations of reciprocity in wild communities.     

Why preen others? Predictors of allopreening in parrots and corvids and comparisons to grooming in great apes

Allogrooming in primates serves not only a hygienic function, but also plays a crucial role in maintaining strong affiliative bonds between group members, which in turn, underpin the emergence of cooperative behavior. In contrast, although allopreening occurs in many avian species, we know little about its social functions. Our study addresses this issue by investigating allopreening in a broad comparative data set including six corvid and nine parrot species. We assessed whether rates of allopreening initiations, proportion of time spent allopreening, and the number of grooming partners in captive group-housed birds were comparable to patterns observed in captive chimpanzees and bonobos. While parrots and corvids were found to have similar rates of social grooming to bonobos and chimpanzees, Pan species dedicated significantly more time to social grooming. Animals in larger groups had more grooming partners, but when controlling for the number of potential partners, birds tended to have fewer grooming interaction partners than Pan species. We then investigated whether allopreening in parrots and corvids was predicted by behavioral markers of affiliative social bonds (close physical proximity, active feeding, and low levels of agonistic behavior). Results revealed that providing allopreening to a partner was significantly predicted by often being in close proximity, but not engagement in active feeding or agonistic behavior. We examined the region allopreened in a subset of species and found that preening a partner's head was predicted by both close physical proximity and active feeding, while body allopreening was only predicted by close physical proximity. Head preening may confer more hygienic benefits to recipients, and thus, may be more selectively provided to valued partners. Results support the hypothesis that allopreening in corvids and parrots helps maintain social bonds with an individual's most important social partners, showing some similarities to allogrooming in primates.     

Activity Patterns, Intergroup Encounters, and Male Affiliation in Free-Ranging Bearded Sakis (Chiropotes sagulatus)

The assessment of how primates divide their daily activities is one of the foundations of primate behavioral ecology but the activity patterns and social behavior of the Pitheciines, including bearded sakis (genus Chiropotes), are poorly understood. During a 15-mo study, I collected 560 h of data on subgrouping, activity patterns, social behavior, and intergroup encounters of a group of free-ranging Guianan bearded sakis (Chiropotes sagulatus) in Guyana. The study group consisted of at least 65 individuals but showed a high degree of flexibility in grouping patterns (mean group size 39 ± 10). They were highly active, spending ca. 70% of their diurnal activity budget traveling and feeding. Activity patterns were relatively consistent throughout the year, although time spent feeding correlated significantly with fruit availability. The most common social behaviors were social resting and grooming. Agonism was rare (2.56% of social behavior) but did occur in the context of intergroup encounters, with males from the same group cooperating in intergroup agonism. Bearded sakis showed a high level of within group male affiliation, with male–male partners making up 65% of grooming dyads and males having another male as their nearest-neighbor 66% of the time. These results show that bearded sakis are characterized by egalitarian male–male and male–female relationships, highly fluid group sizes, and high levels of male affiliation. Similarities in the social behavior of bearded sakis and muriquis suggest several possible explanations for male–male bonding including cooperative defense of females from other groups, kinship, and maintenance of social cohesion after subgroup coalescence.     

Market forces predict grooming reciprocity in female baboons

We argue that grooming is a commodity that female primates can trade, either for itself or in exchange for other services (sensu biological markets theory) and that the decision to do either will depend on the degree of competition within a social group. We test this using data from four chacma baboon troops, living in two populations that differ markedly in the degree of contest competition. As predicted by the predominance of grooming dyads in which females are closely ranked there was, in all four troops, a positive correlation between the time invested by one partner and that by the other. In addition, as predicted, the allocation of time was more closely matched in troops where grooming could not be exchanged for anything else. In troops where resource competition was high, we found in one of two troops a positive relationship between rank distance and the discrepancy in time allocation, with the lower ranking of the partners contributing more grooming.     

Intragroup cohesion and intergroup hostility: the relation between grooming distributions and intergroup competition among female primates

In some primate species, females interact affinitively withmany related and unrelated females, whereas in other speciesfemales interact with only a small subset of available partners.One explanation for high rates of affinitive interactions amongfemale members of the same group is that they function to maintainthe group's cohesion in competition for resources against othergroups. Here, I attempt to determine if grooming is more "egalitarian"or diverse in groups that compete aggressively with their neighborsthan in groups in which females rarely take an active role inbetween-group competition. Three types of data are considered.The first concerns grooming and intergroup encounters in onepopulation of free-ranging vervet monkeys. The second concernsgrooming interactions in a captive population of vervets beforeand after females in adjacent cages began to respond aggressivelyto one another. The third involves a literature survey of avariety of species. When only female-bonded species are considered,there is no relation between the diversity of grooming withingroups and female participationin intergroup encounters. Therealso appears to be no clear relation between the strength ofthe female dominance hierarchy and the diversity of groomingamong females. Female-bonded groups are apparently composedof subgroups allied in a loose confederation against other groups.Female members of the same group may compete against other groupsas a cohesive unit, but their grooming relationships are oftensharply differentiated.     

Differential effects of kinship,dominance, and the mating season on female allogrooming in a captive group ofMacaca fuscata

An analysis of allogrooming (total times spent grooming individual partners) of 8 sexually mature females (3–12 years of age) in a captive group of 17 Japanese macaques, shows that during the nonmating season, grooming distributions were characterized by high proportions of grooming given to family members and/or higher ranking nonkin. During the mating season, all eight females showed significant shifts in their grooming distributions, and four females showed significant shifts in grooming between their nonestrous and estrous periods (defined behaviorally). Fox six of eight females, mating season grooming was characterized by either high proportions of grooming given to family members and/or heterosexual and homosexual partners. It was found that within dyadic sexual relationships, dominants gave more grooming to subordinates than the former received, in contrast to a reversal of this pattern in the majority of these same dyads during the nonmating season. This is interpreted as one short-term function of grooming: a dominant asymmetrically grooms a subordinate sexual partner to maintain proximity with (or reduce tension in) the latter. The two remaining focal females (middle ranking, nulliparous) differed from the other females in that they shifted their mating season grooming to subordinate nonkin, despite the lack of evidence that this was a result of sexual interactions, patterns of partner availability, competition, patterns of grooming reciprocity, or agonistic alliance support. From these results, it is suggested that in some contexts, grooming of subordinate nonkin may function to reduce tension in thegroomer. In the Japanese macaque, this latter possibility and the asymmetric grooming of subordinate homosexual partners may prove to be exceptions to the general rule that female cercopithecine grooming of nonkin flows up the dominance hierarchy.     

The dining etiquette of desert baboons: the roles of social bonds, kinship, and dominance in co-feeding networks

To better understand how individual relationships influence patterns of social foraging in primate groups, we explored networks of co-feeding in wild desert baboons (Papio ursinus). To minimize the risk of aggression and injury associated with contest competition, we expected that individual group members would choose to co-feed with those group-mates that are most likely to show tolerance and a willingness to share food patches. We tested two alternative hypotheses about who those group-mates might be: the "social bonds hypothesis" predicts that preferred foraging partners will be those with whom individuals share strong social bonds, indexed by grooming, whereas the "kinship hypothesis" predicts that preferred foraging partners will be relatives. We also investigated and controlled for the effects of dominance rank, given that competitive ability is known to shape foraging patterns. Social network analyses of over 5,000 foraging events for 14 adults in a single troop revealed that baboon co-feeding was significantly correlated with grooming relationships but not genetic relatedness, and this finding was also true of the female-only co-feeding network. Dominant individuals were also found to be central to the co-feeding network, frequently sharing food patches with multiple group-mates. This polyadic analysis of foraging associations between individuals underlines the importance of dominance and affiliation to patterns of primate social foraging.     

Competition for grooming partners and interference in affiliation among female mandrills

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

Serial agonistic attacks by greylag goose families, Anser anser, against the same opponent

It is known from primates that alliance partners may support each other's interests in competition with others, for example, through repeated agonistic attacks against a particular individual. We examined serial aggressive interactions between greylag goose families and other flock members. We found that repeated attacks towards the same individual were common and that up to five serial attacks by family members followed an initial attack. Family size did not affect the frequency of such serial attacks. Juvenile geese evidently benefited most from active social support through serial attacks. About 60% of the juveniles' lost primary interactions were subsequently reversed by another family member. This may be one of the reasons why juveniles rank higher in the social hierarchy than would be expected from their age and size alone. Losses in serial attacks predominantly occurred against other, presumably higher-ranking, family geese and ganders. We propose three major functions/consequences of serial attacks. Analogous to primates, serial attacks in greylag geese may serve to reinforce a losing experience of an opponent defeated in a preceding attack. On the side of the winning family, serial attacks may reinforce the experience of winning. Both winning and losing experiences are linked with physiological consequences in higher vertebrates, affecting the future social performance of winners or losers. Finally, serial attacks may signal the agonistic potential of a family to other flock members. This is supported by heart rate data, which indicate that greylags are competent to interpret third-party relationships.     

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

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

The evolution of the social brain: anthropoid primates contrast with other vertebrates

The social brain hypothesis argues that large brains have arisen over evolutionary time as a response to the social and ecological conflicts inherent in group living. We test predictions arising from the hypothesis using comparative data from birds and four mammalian orders (Carnivora, Artiodactyla, Chiroptera and Primates) and show that, across all non-primate taxa, relative brain size is principally related to pairbonding, but with enduring stable relationships in primates. We argue that this reflects the cognitive demands of the behavioural coordination and synchrony that is necessary to maintain stable pairbonded relationships. However, primates differ from the other taxa in that they also exhibit a strong effect of group size on brain size. We use data from two behavioural indices of social intensity (enduring bonds between group members and time devoted to social activities) to show that primate relationships differ significantly from those of other taxa. We suggest that, among vertebrates in general, pairbonding represents a qualitative shift from loose aggregations of individuals to complex negotiated relationships, and that these bonded relationships have been generalized to all social partners in only a few taxa (such as anthropoid primates).     

Bridging the bonding gap: the transition from primates to humans

Primate societies are characterized by bonded social relationships of a kind that are rare in other mammal taxa. These bonded relationships, which provide the basis for coalitions, are underpinned by an endorphin mechanism mediated by social grooming. However, bonded relationships of this kind impose constraints on the size of social groups that are possible. When ecological pressures have demanded larger groups, primates have had to evolve new mechanisms to facilitate bonding. This has involved increasing the size of vocal and visual communication repertoires, increasing the time devoted to social interaction and developing a capacity to manage two-tier social relationships (strong and weak ties). I consider the implications of these constraints for the evolution of human social communities and argue that laughter was an early evolutionary innovation that helped bridge the bonding gap between the group sizes characteristic of chimpanzees and australopithecines and those in later hominins.     

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.     

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

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

Social relationships of immigrant and resident female mountain gorillas. I. Male-female relationships

Adult males are important social partners for all females in mountain gorilla social groups, but male-female relationships can vary in association with variation in female residence status, male age and mating status, and relatedness. Such variation occurred in a large group observed over a 3-year period. All females associated and interacted affiliatively relatively often with a young silverback with whom all mated. Long-term resident females also did so with an old, non-breeding male to whom most were related, but recent immigrants spent little time near him and had few non-aggressive interactions with him. The old male made agonistic interventions to support relatives; interventions in female conflicts by the younger male tended to ameliorate competitive differentials that immigrants faced and may have helped him to retain them as mates. Males aggression toward females was common, most probably served as a mating tactic, and did not involve resource competition. Extensive grooming by an adolescent male suggests that males may also use affiliative behavior to develop mating relationships. Females may have competed for proximity with and social access to the younger silverback; competitive success could influence how well females and their offspring are protected by silver-backs, but the extent of such competition was not clear. Large group size may have heightened differentiation of male-female relationships and competition among females, but comparative data from smaller groups generally corroborate the findings from the large group. © 1992 Wiley-Liss, Inc.     

Increasing Group Size Alters Behavior of a Folivorous Primate

Group size influences many aspects of mammalian social life, including stress levels, disease transmission, reproductive rates, and behavior. However, much of what is known about the effects of group size on behavioral ecology has come from comparisons across multiple groups of different sizes. These findings may be biased because behavioral differences across groups may be more indicative of how environmental variation influences animal behavior, rather than group size itself. To partially circumvent this limitation, we used longitudinal data to examine how changes in group size across time affect the behavior of folivorous red colobus monkeys (Procolobus rufomitratus) of Kibale National Park, Uganda. Controlling for food availability, we demonstrated that increasing group size resulted in altered activity budgets, based on 6 yr of data on a group that increased from 57 to 98 members. Specifically, as group size increased, individuals spent less time feeding and socializing, more time traveling, and increased the diversity of their diet. These changes appear to allow the monkeys to compensate for greater scramble competition apparent at larger group sizes, as increasing group size did not show the predicted relationship with lower female fecundity. Our results support recent findings documenting feeding competition in folivorous primates. Our results also document behavioral flexibility, an important trait that allows many social mammals to maximize the benefits of sociality (e.g., increased vigilance), while minimizing the costs (e.g., increased feeding competition).     

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.     

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.