Female-female social relationships in wild white-faced capuchin monkeys,Cebus capucinus

A single social group of wild white-faced capuchin monkeys was studied for a period of 26 months at Lomas Barbudal Biological Reserve, Costa Rica. A total of 604 hr of focal animal data was collected on six adult females in a group of 21 monkeys. Females could be ranked in a stable, linear dominance hierarchy. Adult females spent much more time in proximity to other adult females than to adult males. Females groomed other females twice as often as they groomed males, and about 55 times more often than males groomed males. Females tended to groom up the dominance hierarchy, and dyads with smaller rank distances groomed more often. Higher-ranking females nursed infants other than their own at lower rates than did lower-ranking females; however, females nursed infants of females ranked both above and below them. Although lower-ranking females were more likely than higher-ranking females to be the victims of aggression, higher-ranking females were not necessarily more aggressive than lower-ranking females. In 96% of female-female coalitions vs. a female, the victim was lower-ranking than both coalition partners; in the remaining 4%, the victim was intermediate in rank between the two coalition partners. Higher-ranking female-female dyads formed coalitions more often than did lower-ranking dyads. Those female-female dyads that groomed more frequently also formed coalitions more frequently. The patterning of social interactions indicates that Cebus capucinus at Lomas Barbudal are female bonded. © 1996 Wiley-Liss, Inc.     

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.     

Relation of Intergroup Variation in Allogrooming to Group Social Structure and Ectoparasite Loads in Red Howlers (Alouatta seniculus)

We compare the allogrooming behavior of 5 troops (average size = 8.2) of red howlers (Alouatta seniculus) from the Venezuelan Llanos with that of other A. seniculus and Alouatta spp. of the genus. In 126.9 observation hr, we recorded 118 allogrooming events, with an average bout length of 109 sec. Females groomed more frequently than males did, but as groomees there is no significant differences between sexes. Adult males groomed adult females mostly in a sexual context (before copulation). Allogrooming rates differ significantly among groups. There are also significant differences among members of the same troop both as groomers and groomees, which we explain in the context of the social behavior and history of each troop. There is no significant correlation between weight of the groomee and duration of the grooming bout. However, the examination of grooming rates and ectoparasite load suggests that allogrooming may have hygienic consequences. Differences in allogrooming rates among species of Alouatta are related to differences in group kin structure and patterns of female competition, in particular, coalition formation. We conclude that the social structure and the degree of relatedness among individuals within a group (or among individuals in a population in interpopulation comparisons) is a more important determinant of allogrooming rate than body size or group size. Our results emphasize the importance of considering intergroup and interpopulational variation in behavior.     

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.     

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.     

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.     

Distress prevention by grooming others in crested black macaques

Allogrooming is probably one of the most common and most studied social behaviours in a variety of animals. Whereas the short-term benefits for the groomee have often been investigated, little is known about the effects for the groomer. Our study focused on the short-term effects of grooming another group member in seven adult female crested black macaques (Macaca nigra). We found reductions in self-directed behaviour, an indicator of anxiety, and aggressive tendencies soon after grooming, when compared to matched-control periods. These findings can be interpreted as evidence of distress prevention, possibly mediated by an increase in tolerance. Indeed, a former groomee was more likely to be the nearest neighbour of the former groomer in the 10 min after grooming ended. Thus, the role of grooming in short-term distress alleviation can be applicable to the groomer as well as the groomee. These short-term effects, together with the longer-term effects of large and/or strong grooming networks confirm that grooming, as well as receiving grooming, has great importance for social dynamics.     

Mating patterns,mate choice,and birth season heterosexual relationships in free-ranging rhesus macaques

Birth season adult heterosexual nonkin relationships of 50 free-ranging female rhesus macaques (Macaca mulatta) in two social groups at Cayo Santiago, Puerto Rico were examined using focal follow (289 hr) and ad lib data. Eighty-eight percent of subjects had at least one relationship characterized by particularly high frequencies of spatial proximity, grooming, or both. These were designated “friendships.” Males intervened in aggressive interactions more frequently on behalf of Friends than non-Friends. Female aggressive support of males was extremely rare. Higher-ranking males experienced more friendships than lower-ranking males. High-ranking females had higher-ranking Friends than low-ranking females. Older females had higher-ranking Friends than younger females. Females groomed high-ranking Friends more than they were groomed by them, whereas they groomed low-ranking Friends less than they were groomed by them. In one social group, high-ranking females were more likely than low-ranking females to groom their Friends more than they were groomed by them. Males were more responsible than females for spatial proximity maintenance in 9 of 14 Friend dyads for which sufficient data were available. Neither male nor female dominance rank affected responsibility for proximity maintenance in Friend dyads. Eight of 24 females had friendships with males with whom they had completed copulations during their conception peri-ovulatory period of the preceding mating season. Two of 19 females completed peri-ovulatory copulations with Friends during the following mating season. Friendship was not correlated with either of two demonstrated female mate choice indicators: (1) proximity maintenance during estrus; or (2) cooperation with male “hip-grasp” courtship attempts. Males directed “muzzle-up” courtship signals at lower rates toward Friends than toward non-Friends. These and other investigators' results indicate that (1) protection from aggression is the primary benefit to female rhesus macaques of birth season heterosexual relationships; (2) the most effective protectors are in greatest demand as Friends; and (3) friendship has no effect or an inhibitory effect on mate choice in this species. Benefits to males of friendships were not apparent from this study but may include coalitional support against lower-ranking males.     

Affiliative relationships and reciprocity among adult male bonnet macaques (Macaca radiata) at Arunachala Hill, India

In captivity, male bonnet macaques (Macaca radiata) frequently express "friendship" toward one another, including affiliative behavior such as huddling, grooming, coalitionary support, and sitting in close proximity. The purpose of this study was to determine whether wild adult male bonnet macaques also express "friendship" by investigating whether or not (1) adult male bonnet macaques have affiliative social relationships with other males, (2) the strength of social relationships varies among dyads, (3) there is time-matched reciprocity in allogrooming among dyads, and if so, whether the level of reciprocity occurs within a bout of grooming, a day, or over 2 months (the limit of this study), and (4) a correlation exists between the strength of social relationships and dominance ranks among adult males. Focal samples totaling 150 hr on all seven adult males in one study group were conducted to record both agonistic and affiliative interactions. Agonistic interactions were used to construct a dominance hierarchy, whereas affiliative interactions (sitting in proximity to within 1 m with and without grooming) were used to quantify the existence and strength of social bonds within dyads. Results show that adult male bonnet macaques had differentiated affiliative relationships with other males in their group. There was little reciprocity of grooming within a bout of grooming or within a day, but greater reciprocity over the study period of 2 months. There was no correlation between dominance ranking distance and the strength of affiliative relationship within dyads; however, within dyads lower-ranking males groomed higher-ranking males more than vice versa. This study suggests that friendships in male bonnet macaques are characterized not by immediate tit-for-tat reciprocal altruism, but by reciprocity over a longer time span, and that affiliative social relationships may be less constrained by agonistic relationships than is the case in more despotic species of macaques.     

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.     

Social relationships among adult female baboons

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

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.     

Weaving a tight social net: Allogrooming in free-ranging female langurs (Presbytis entellus)

We studied grooming among adults of a one-male multifemale troop of free-ranging Hanuman langurs (Presbytis entellus)living near Jodhpur, India, for 9 years. The 11–13 females devoted about 6% of their day to allogrooming. Adult males, whose tenures averaged 2.2 years, were transient figures in the troop's history, as reflected by their rather peripheral role in the grooming network. Females groomed males 4–40 times more frequently (1006 episodes) than vice versa- (176 episodes). Adult females received 97% of all grooming from other adult females (6655 episodes). Although females exhibited an age- inversed dominance hierarchy, they did not compete for grooming access to particular troop mates. Dyads of all possible rank differences occurred as frequently as expected: 51% of grooming was directed up the hierarchy and 49% down it. Young, high- ranking individuals gave and received significantly more grooming than the oldest, low- ranking females did. The pattern seemed to be influenced by kin selection because of the presumably high degree of female relatedness. They invested most in troopmates with the highest reproductive value, i.e., the youngest individuals. This trend was coupled with a preference of closest kin (mothers and daughters). Reciprocity was the outstanding feature since all adult females groomed and were groomed by all others. Such a tight social net might establish the necessary cohesion during frequent territorial disputes with neighboring troops.     

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 function of allogrooming in domestic cats (Felis silvestris catus); a study in a group of cats living in confinement

Grooming interactions (n=83) occurring in a group of non free-ranging adult neutered male (n=14) and female (n=11) domestic cats (Felis silvestris catus) were analysed. Grooming was not induced by the proximity (distance <=0.5 m) of another animal. Grooming was in general directed at the head-neck area. Higher ranking animals groomed lower ranking animals more often than the other way round. Groomers tended to adopt ‘higher’ (standing, sitting upright) postures than groomees (sitting, lying). Agonistic behaviour occurred in 35% of interactions. Groomers showed offensive behaviour more often than groomees, most often after grooming a partner. Furthermore groomers often groomed themselves after grooming a partner. The degree of relatedness of animals did not affect the frequencies or durations of grooming. These results are consistent with the hypothesis that allogrooming in domestic cats may be a way of redirecting (potential) aggression in situations in which overt aggression is too costly. The data were previously presented at the 29th International Congress of the International Society for Applied Ethology (van den Bos, R. (1995) Allogrooming in domestic cats in confinement, Proceedings of the 29th International Congress of the International Society for Applied Ethology, S.M. Rutter et al. (Eds.), pp. 109–110)     

Social grooming in assamese macaques (Macaca assamensis)

Reciprocity and social bonding hypotheses were evaluated as explanations for observed patterns of social grooming in assamese macaques (Macaca assamensis). In accordance with social bonding, females, as the long-term residents of this matrifocal group, groomed each other and juveniles more often than males groomed one another or juveniles. On the other hand, males groomed females more often and for longer durations than females groomed males and, whereas both males and females groomed juveniles more often than juveniles groomed them, juveniles groomed their elders for longer durations. Male grooming of females did not seem directly related to matings as males are single mount ejaculators and use coercive mating tactics. Male grooming of females could not be accounted for in terms of reciprocity; it was not a simple function of dominance. Although both sexes groomed subordinate females more than vice versa, males groomed dominant males more and females groomed subordinate males more than they received grooming from them. Grooming was concluded to function to establish and maintain affiliative social bonds rather than as a specific mechanism to obtain matings or any other specific reciprocation in terms of services or favors.     

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.     

Female social dominance in two Eulemur species with different social organizations

Female social dominance is rare in mammals, but common in lemurs. We investigated social dominance in two Eulemur species; the polygynous crowned lemur (E. coronatus) and the monogamous red‐bellied lemur (E. rubriventer), using four and two social groups, respectively. We collected data on agonistic interactions and two types of affiliative behavior (grooming and maintaining spatial proximity). We used a combination of focal watches of individuals, instantaneous scan‐sampling of groups, and all‐occurrence of some behaviors in groups. We found that overall rates of agonistic interactions were higher in E. coronatus, and they also had more decided intersexual agonistic interactions than E. rubriventer. However, in both species the females won the vast majority of these agonistic interactions. E. coronatus females were groomed more often by males than vice versa, whereas no sex differences in grooming were observed in E. rubriventer. We found that males were responsible for maintaining spatial proximity in E. coronatus whereas in E. rubriventer, females were responsible. In one group of E. coronatus, the male was overweight and dominant to the female and this is the first observation of male dominance in a lemur species typically described as female dominant. We suggest that body weights in captivity be monitored for maintaining normal dominance relationships. Overall, agonistic behaviors were consistent with clear female social dominance in both E. coronatus and E. rubriventer. The affiliative behaviors also provided clear evidence for female dominance E. coronatus, but not for E. rubriventer. Zoo Biol 0: 1–14, 2007. © 2007 Wiley‐Liss, Inc.     

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.     

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

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