The influence of behavioral context and social characteristics on the physical aspects of social grooming in rhesus monkeys

The extent to which dominance status and sex can influence the physical act of grooming was examined in two groups of rhesus monkeys. Both the sex and the dominance status of the groomee, but not of the groomer, were found to affect the body sites groomed and the positions assumed by the animals during the grooming bout. Females were groomed more on the back and head and less on the tail, rump, upper leg, and lower arm than males. Females with infants tended to face away from the groomer. Higher-ranking groomees were groomed more on the tail and rump and less on the upper leg and back than lower-ranking groomees. Higher-ranking groomees spent more time lying down during grooming than lower-ranking groomees, while lower-ranking groomees faced away from the groomer more then higher-ranking groomees. The behavioral interactions just prior to and immediately after grooming were also recorded. Although the onset of grooming was preceded by social interactions between the partners, the end of grooming was followed by a complete break in interactions. Particular types of social signals displayed by the groomee just prior to grooming were highly correlated with the grooming of specific body sites. These results suggest that the groomee controls the behavior of the groomer by the social signals it displays and the positions it maintains during the grooming bout. Thus, the grooming act itself may play an important role in the social relationships between group members.     

Time-matched grooming in female primates? New analyses from two species

The parcelling model of reciprocity predicts that grooming partners will alternate between giving and receiving grooming within grooming bouts, and that each partner will perform approximately as much grooming as it receives within each bout (‘time matching’). Models of allogrooming based on biological markets theory predict that individuals of lower dominance rank will exchange grooming for tolerance from high-rankers, and therefore an inverse relation will be found between grooming partners' dominance rank distance and how closely they match each other's grooming contributions within each bout. We used weighted logistic regression and weighted least-squares regression to test these predictions using data from female white-faced capuchins, Cebus capucinus, and bonnet macaques, Macaca radiata. Only 5-7% of macaque grooming bouts, and 12-27% of capuchin grooming bouts, were reciprocated. However, (1) the duration of grooming by the first groomer significantly predicted whether the groomee would reciprocate at all, and (2) when bouts were reciprocated, the duration of grooming by the first groomer significantly predicted the duration of grooming by the second groomer. Grooming was most balanced among females of similar dominance ranks. Both the time-matching and rank-related effects were weak, although significant. These results indicate that although some form of time matching may be a general characteristic of grooming in female-bonded primate species, time matching accounts for relatively little of the variation in the distribution of grooming within bouts. We also draw attention to weighted regression as a technique that avoids pseudoreplication while using all available data.     

Grooming site preferences in female langurs (Presbytis entellus)

Factors influencing grooming site preferences in adult female Hanuman langurs (Presbytis entellus) were investigated. The females belonged to a free-ranging harem troop (Jodhpur, India) and were observed for 569 hr by focal-female sampling. Decisive factors for grooming site preferences were the following: autogrooming was determined mostly by site accessiblity. Allogrooming was significantly concentrated on parts that are inaccessible to the groomee. Close female kin groomed significantly longer, more frequently, and more precisely at inaccessible body parts. Lower-ranking females were groomed significantly less often and more briefly but also more precisely at inaccessible parts. However, the latter might be due to a lower-ranking subjects desire to face away from the higher-ranking groomer in order to avoid eye contact. The data suggest that the groomee determines the sites being groomed.     

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.     

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.     

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 influences on grooming site preferences among captive long-tailed macaques

Data on grooming in a colony of 38 captive Macaca fascicularis were collected over a period of 6 months. The goal was to investigate how five social parameters (age, kinship, sex, grooming frequency, and relative rank) influenced the choice of body part being groomed. Age and kinship did not have systematic effects of grooming site preferences. The sex composition of individual dyads and the frequency at which grooming occurred were the factors with the greatest effect on body sites groomed among adults. Relative to other dyad types, male-male dyads almost never groomed on the face, avoided the front side of the trunk, and preferred the tail and back. Dyads that groomed relatively infrequently also favored the tail and avoided the face, chest, and belly. Relative rank had an effect on the body sites groomed among adult females: a groomer ranking lower than her partner groomed more often on the face, chest, and belly than a groomer ranking higher than her partner. Several hypotheses are discussed in the context of these results. The only one that explains most of the major results is that recipients of grooming expose relatively invulnerable parts of their bodies (i.e., back and tail) to and avoid eye contact with groomers that are relatively dangerous.     

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.     

The Long-Term Effects of Reconciliation in Japanese Macaques Macaca fuscata

With one exception, all previous studies of reconciliation in non-human primates (friendly reunion between former opponents) have focused on demonstrating the immediate, short-term effects despite the widely held view that reconciliation has a long-term function of repairing social relationships following aggression. To investigate this long-term function I compared mean interaction rates between opponents during the 10 d following reconciled and non-reconciled conflicts to baseline levels of interaction. Aggression rates during the 10 d after non-reconciled conflicts were significantly higher than the baseline rate, whereas after reconciled conflicts aggression was minimal. Similarly, grooming, proximity and approach rates during the 10 d after non-reconciled conflicts were significantly lower than the baseline rate whereas grooming, proximity and approach rates in the 10 d after reconciled conflicts were restored to baseline levels. These results indicate that there are consequences to not reconciling with a former opponent and highlight the fact that these may be costly in terms of increased risk of long-term aggression and reduced affiliation. The data support predictions from the Relationship-Repair Hypothesis suggesting that reconciliation functions as a mechanism for the repair of social relationships damaged by aggression.     

Signals found in the grooming interactions of wild Japanese monkeys of the koshima troop

Signaling behaviors appearing in grooming interactions of wild Japanese monkeys were analysed. Vocal signals found in the grooming interactions had the content of asking the objective animal “if the vocal signaler may groom the recipient animal.” They could be divided into two categories of vocal sounds, VG-1 and VG-2. The former was uttered in common by all the troop members. The latter was uttered just before grooming by the groomer and is considered to have deeper connection with grooming. Each individual uttered mainly one kind of vocal sound out of VG-2, and the preferred vocal sounds for each individual differed. Furthermore, VG-2 differed in different troops. Behavioral signals had the content of showing “the acceptance of grooming” or showing “the request to be groomed.” The appearance of these signaling behaviors was closely related to the inter-individual relationships of grooming partners, especially as to whether or not they had blood relationships. Basically the monkeys have a system in which they must avoid each other, except in the case of mothers and their offspring, and if they had to approach too closely against this basic system, as in grooming interactions, there appeared signaling behaviors as mentioned above.     

Observations of a daytime birthing event in wild titi monkeys (Callicebus oenanthe): implications of the male parental role

Behaviors displayed during birth events, including prenatal, parturition, and postpartum periods, can give insight into caretaking roles in species in which the offspring is cared for by individuals other than the mother. Titi monkeys, genus Callicebus, exhibit a pair-bonded social system along with intense male care of offspring. Here, I report the first case of a birth seen in the wild in a group of Callicebus oenanthe, a little-known species in northern Peru, and describe infant care and development during the first few months after birth. Detailed behavior during the birth sequence as well as ad libitum data postpartum were recorded on nursing and infant care behaviors, including infant carrying, infant grooming, anogenital cleaning, protection, playing, and food sharing. In the 3 h preceding and during parturition, the male remained in contact with or in close proximity to the female (<1 m). The male licked and examined the newborn 3 min after parturition, carried the infant within 24 h after birth, was the main carrier of the infant, and was the predominant manual groomer of the infant during the first 4 months after birth. I argue that the male plays an integral role during the birth in order to establish his bond with the infant as well as reinforce infant care duties to the female and in predator vigilance. In light of various explanations for the exhibition of intense paternal care, I suggest that the male titi monkey provides infant care to release the female of these duties in order that she may spend more time foraging, thus potentially increasing the pair’s overall reproductive output.     

Grooming and Anxiety in Barbary Macaques

Grooming is a fundamental component of sociality in many gregarious animal species, and elucidating the costs and benefits of this behaviour is crucial for understanding its function. There is evidence that animals giving grooming pay a cost in terms of the time and energy they invest, while recipients benefit not just from the removal of dirt and parasites, but also from the relaxing effects of being groomed. Recently, however, studies of primates have indicated that giving grooming may also provide such hedonic benefits, reducing levels of stress or anxiety in the groomer. In this study of free‐ranging adult female Barbary macaques at Trentham Monkey Forest (Stoke‐on‐Trent, UK), we tested the hypothesis that grooming reduces anxiety in the donor and/or the recipient. During focal follows, we quantified females' rates of self‐scratching as a behavioural index of their anxiety levels. Self‐scratching rates in the 2‐min periods after bouts of grooming (given, received and reciprocated) were compared to overall mean self‐scratching rates; we predicted that if grooming reduces anxiety, self‐scratching rates would be significantly lower after grooming bouts than mean levels. We first analysed all grooming bouts and then analysed separately grooming bouts with adult males, with all adult females, with subordinate adult females and with dominant adult females. Contrary to our prediction, self‐scratching rates were never seen to be lower after grooming than mean levels. In fact, for the majority of grooming partner–direction combinations, we found significantly higher rates of self‐scratching after grooming compared to mean levels. The hypothesis that grooming reduces anxiety was therefore not supported. Grooming seems in some cases to increase, not alleviate, anxiety. We explore possible explanations for these unexpected results.     

Quantitative observations of grooming behavior in free-rangingMacaca mulatta

Quantitative methods of observation and analysis were used in a 12-month study of grooming behavior of free-rangingMacaca mulatta on La Cueva Island at La Parguera, Puerto Rico. Observations lasting 30–120 minutes were made from eight positions on the island at a standard time of day when monkeys were either feeding or resting. Two dependent variables were obtained: (1) the number of monkeys present in the observation area were noted by age and sex class at five-minute intervals throughout each observation, and (2) the frequency of grooming encounters was tabulated by the age and sex class(es) of groomer and recipient. These data were computed as grooms/hour/possible interacting combination of monkeys. Grooming frequencies were higher in non-feeding situations than when monkeys were feeding. The largest social group had the lowest mean grooming rates, while the smallest group had the highest grooming frequencies. More grooming occurred during the November-to-February mating season than at other periods of the year. Adult females were involved in over 60% of all grooming behavior, juveniles participated in 25% of the grooming, while adult males groomed females, primarily during the mating season, and rarely groomed other males or juveniles. Genealogical relationships, levels of group aggression and the feeding or resting context all influenced the frequency of grooming. This study provides support for the hypothesis that the basic social unit for rhesus macaques consists of a core of adult females with their juvenile and infant progeny.     

A functional analysis of social grooming patterns through direct comparison with self-grooming in rhesus monkeys

Social grooming in primates is a complex behavior in which monkeys stroke, pick, or otherwise manipulate a companion’s body surface. While grooming has been associated with important social functions, researchers who have examined its physical characteristics, such as body site preferences, have focused on its role in skin care and ectoparasite removal. Whether the form of social grooming is constrained primarily by utilitarian or social functions was empirically tested by directly comparing this behavior with self-grooming, which was assumed to have primarily utilitarian functions. Predictions made concerning social grooming, based on a comparison with self-grooming, were tested by examining site preferences, duration of grooming (overall and to specific body sites), and method of grooming (stroking, picking, or a combination of the two) in rhesus monkeys. None of these predictions was verified. The physical characteristics of social grooming could not be predicted from the way an animal groomed itself. There was no relationship between site preferences in these two types of grooming. Animals groomed others for longer periods of time than they groomed themselves, both overall and when grooming specific sites. The methods these animals used differed markedly in self-and social grooming: they primarily picked at their own hair or skin but, when grooming others, varied their technique across sites, stroking the hair where it was thickest and picking where the hair was sparse. These results suggest that utilitarian functions are not the most important factors constraining the form of social grooming.     

Grooming in Barbary macaques: better to give than to receive?

It is well established that grooming underpins sociality in group-living primates, and a number of studies have documented the stress-reducing effects of being groomed. In this study, we quantified grooming behaviour and physiological stress (assessed by faecal glucocorticoid analysis) in free-ranging Barbary macaques, Macaca sylvanus. Our results indicate that it is the giving rather than the receiving of grooming that is associated with lower stress levels. These findings shed important new light on the benefits of this key behaviour in primate social life.     

Opposing effects of allogrooming on disease transmission in ant societies

To prevent epidemics, insect societies have evolved collective disease defences that are highly effective at curing exposed individuals and limiting disease transmission to healthy group members. Grooming is an important sanitary behaviour—either performed towards oneself (self-grooming) or towards others (allogrooming)—to remove infectious agents from the body surface of exposed individuals, but at the risk of disease contraction by the groomer. We use garden ants (Lasius neglectus) and the fungal pathogen Metarhizium as a model system to study how pathogen presence affects self-grooming and allogrooming between exposed and healthy individuals. We develop an epidemiological SIS model to explore how experimentally observed grooming patterns affect disease spread within the colony, thereby providing a direct link between the expression and direction of sanitary behaviours, and their effects on colony-level epidemiology. We find that fungus-exposed ants increase self-grooming, while simultaneously decreasing allogrooming. This behavioural modulation seems universally adaptive and is predicted to contain disease spread in a great variety of host–pathogen systems. In contrast, allogrooming directed towards pathogen-exposed individuals might both increase and decrease disease risk. Our model reveals that the effect of allogrooming depends on the balance between pathogen infectiousness and efficiency of social host defences, which are likely to vary across host–pathogen systems.     

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.     

Coping with social tension: Sex differences in the effect of food provision to small rhesus monkey groups

In previous research, male chimpanzees (Pan troglodytes) were found to be more ‘conciliatory’ than females, in that after aggressive incidents males more often engaged in socially positive contact with former opponents. The first part of the present paper presents similar results for a large breeding troop of rhesus monkeys (Macaca mulatta). To investigate further the possible sex difference in postconflict behaviour, a series of experiments was carried out on small isosexual groups of young rhesus monkeys, three male and three female groups. Food competition was created by providing either a single apple piece (Monopoly test) or a handful of small pieces (Equality test). Observations lasted for 30 min, and behaviour in tests without food provisioning was also recorded. The predicted response to food was an increase in aggression followed by restorative behaviour, such as grooming. In Equality tests both sexes showed similar responses, i.e. increased aggression and decreased grooming and cohesiveness. In Monopoly tests, however, their responses differed. After the aggression increase, which occurred in all groups, males showed a significant increase in grooming and cohesiveness, whereas females showed the (non-significant) opposite trend. Another sex difference was that changes in grooming and aggression frequencies were related to the rank order in female groups, but not in male groups. Since there was no evidence for a direct causal connection between grooming and aggression, a new model is introduced which links grooming behaviour to the type of food provision rather than to the social disturbance by aggression. According to this model inequality in food distribution causes social tensions. Males actively try to reduce these tensions, whereas females do not. Some alternative explanations are also discussed.     

Evidence for varying social strategies across the day in chacma baboons

Strong social bonds can make an important contribution to individual fitness, but we still have only a limited understanding of the temporal period relevant to the adjustment of social relationships. While there is growing recognition of the importance of strong bonds that persist for years, social relationships can also vary over weeks and months, suggesting that social strategies may be optimized over shorter timescales. Using biological market theory as a framework, we explore whether temporal variation in the benefits of social relationships might be sufficient to generate daily adjustments of social strategies in wild baboons. Data on grooming, one measure of social relationships, were collected from 60 chacma baboons (Papio ursinus) across two troops over a six month period. Our analyses suggest that social strategies can show diurnal variation, with subordinates preferentially grooming more dominant individuals earlier in the day compared with later in the day. These findings indicate that group-living animals may optimize certain elements of their social strategies over relatively short time periods.     

Social behavior of wild moustached tamarins,Saguinus mystax,at the Estación Biológica Quebrada Blanco,Peruvian Amazonia

The social behavior in two small, polyandrous groups of moustached tamarins, Saguinus mystax, was studied at the Estación Biológica Quebrada Blanco in northeastern Peru. Allogrooming was the most obvious type of social interaction. Grooming relations were characterized by a strong asymmetry. In both groups, one adult male contributed about 70% of all allogrooming given (in terms of time spent grooming) and allocated his allogrooming evenly to all other group members. Grooming relations between the second adult male and other group members were less intensive. Intragroup agonistic interactions were infrequent, and most of them occurred in the context of feeding on small food resources (fruit, exudate) and during intergroup encounters. Sexual behavior was rare, but at least in one group a tendency existed for the principal groomer to be somewhat more active than the other male. Results are compared with data from other field studies on callitrichid social behavior. Although the label polyandrous correctly describes the demographic structure of many groups, it is not clear whether it is sufficient for understanding the patterning of social relations and thus the social organization of tamarins. © 1996 Wiley-Liss, Inc.