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.     

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.     

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.     

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.     

Development of social grooming between mother and offspring in wild chimpanzees

Grooming between female chimpanzees and their offspring was studied in the Mahale Mountains, Tanzania. Infants under 2 years of age rarely groomed their mothers, and mostly groomed accessible parts of their mother's bodies, if they did so. Most older adolescents reciprocated grooming with their mothers almost equally. Daughters appeared to mature socially earlier than sons, judging from the earlier ages at which a female infant began to groom her mother, groom mutually with her, and groom others. Weaning infants groomed their mothers more when they were in oestrus than when they were not. Development of the use of grooming as a means of social manoeuvring is discussed.     

Age-related differences in social grooming among adult female Japanese monkeys ( Macaca fuscata)

The present study investigated the influence of dominance rank in combination with kinship on age-related differences in social grooming among adult females in a free-ranging group of Japanese monkeys (Macaca fuscata). Eighty-three adult females were divided into six sub-groups according to age-class (younger: 5–9 years old; middle: 10–14 years old; older: 15–22 years old) and dominance rank (high and low rank). The ratio of the number of unrelated females that each female groomed to the total number of available unrelated females and grooming bouts which she gave to unrelated females decreased with increasing age for both high- and low-ranking females, whereas age did not appear to affect corresponding values for related females. On the other hand, compared with low-ranking females, high-ranking females of all age-classes received grooming more often from a larger number of unrelated females. Moreover, older females of low rank received grooming less often from a smaller number of unrelated females than younger females of low rank. These results indicate that with increasing age females are more likely to concentrate on related females when they have grooming interactions with other females. This tendency seems to be more apparent for low-ranking females. Moreover, the present findings also indicate that older high-ranking females could maintain their social attractiveness as high as younger high-ranking females.     

Grooming reciprocity in female tibetan macaques macaca thibetana

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

Grooming Partners of Immature Blue Monkeys (Cercopithecus mitis) in the Kakamega

I report results of a 4-year study, which profiles grooming partners of immature blue monkeys in a Kenyan rain forest. The analysis focuses on the degree to which mothers and offspring were preferred grooming partners and on sex differences in grooming partners. Subjects ranged in age from 0 to 6 years and were members of one study group in which kinship relations were known from long-term study. Immatures often had their mothers as the top-ranked partner. Even more reliably, however, adult females had their offspring as top-ranked immature partners. As offspring grew older, they tended to fall in the rank ordering of their mothers' immature grooming partners, especially when younger siblings were born. Immature males had fewer grooming partners overall than female peers did. Thus, immature females diversified their partners more than males did, especially by establishing grooming relations with immature female partners. Immatures of both sexes had more female partners than expected by chance. Observed sex differences suggest that immature female blue monkeys may use grooming to cultivate relationships with long-term future benefits. It is less clear that the grooming of immature males functions in this way. Immatures of both sexes may also use grooming to maintain relationships of current value, to practice for future social exchange, and to keep clean, and some of their grooming may be in the primary interest of their partners, rather than themselves. In general, immature blue monkeys resemble the immatures of other catarrhine taxa in the way in which grooming is distributed among various partners.     

Social behaviour and infant carrying in a group of moustached tamarins,Saguinus mystax (primates: Platyrrhini: Callitrichidae), on Padre Isla,Peruvian Amazonia

The social behaviour of a group of eight moustached tamarins,Saguinus mystax, (five males, three females) was studied on Padre Isla in northeastern Peru. About 60% of all allogrooming was done by the two adult males in the group, and about 11% by a young adult female. All other group members groomed very little. The adult breeding female received more grooming than any other group member. After the death of the adult female (preyed upon by an anaconda) the amount of active allogrooming remained constant for all group members except for the young adult female, who increased her contribution to about 30%. Her preferred grooming partner was the subadult female, which generally screamed when being groomed by the young adult female and terminated grooming by going away. This kind of grooming relation is termed “forced grooming” and is interpreted as a possible social control mechanism. The young adult female groomed the adult males more often after the death of the adult female than before. This might have had the function of strengthening the social bond with the adult males and in obtaining the breeding position in the group. After the death of the adult female, the vulva of the young adult female grew to full adult size. Agonistic behaviour was less frequent than allogrooming. Most aggressive interactions (50%) originated from the subadult male of the group. The young adult female was the target of most of these aggressions. Extremely little aggression occurred between the three females. The young adult female was the only individual who tried to emigrate from the group during the study period. Her attempt to join a neighbour group failed due to rejection by all four members of this group. All group members participated in carrying an infant, but the adult males and the young adult female carried most frequently. Contribution to infant carrying varied with the infant's age.     

滇金丝猴雌性个体间的理毛行为

相互理毛行为广泛存在于社会性群居灵长类动物中,通常具有清洁卫生和社会交往功能。2012 年10 月至2013 年6 月,我们在云南白马雪山国家级自然保护区对一人工辅助投食滇金丝猴群,采用全事件取样法和焦点动物取样法收集了雌性个体间相互理毛的行为数据,包括理毛的部位、理毛的姿势、理毛的时间和回合数。研究结果表明:滇金丝猴雌性个体之间每次相互理毛的平均时间为5. 7 min。相互理毛部位较多的发生在自我理毛不能进行(达到)的部位(61.1% );在不能自我理毛部位的相互理毛行为持续时间长,平均9.7 min;在个体能够进行自我理毛部位的相互理毛持续时间短,平均为3. 2 min。相互理毛的姿势以对坐为主(48. 4% ),不同理毛姿势的理毛时间差异显著。新迁入家庭单元的雌性个体为理毛的首先发起者,但其获得被理毛的时间却并不多。滇金丝猴雌性个体相互理毛部位、理毛姿势和理毛时间的差异表明,它们之间的相互理毛行为符合卫生功能假说和社会功能假说。     

Distribution of Grooming Among Adult Females in a Large,Free-Ranging Group of Japanese Macaques

We analyzed grooming episodes recorded among adult females in a large, provisioned, free-ranging group of Japanese macaques (Macaca fuscata) at an individual level. Each female groomed on average 10 of the other 84 females, and 54% of them devoted 50% of their grooming to a single female grooming partner, which indicates that most females had grooming interactions with a relatively small subset of available females. Although 65% of the total grooming bouts were between related females, 25% of females disproportionately groomed unrelated females, 22% groomed related and unrelated females equally, and grooming was kin-biased for the remaining 53%. Moreover, 11 of 16 kin-groups included at least one female that groomed unrelated females significantly more often than related females. In 18% of unrelated dyads, grooming was directed down the hierarchy, in 58%, grooming was well-balanced between the two females, and in the remaining 25%, grooming was directed up the hierarchy. The results indicate that although Japanese macaques are considered a despotic species based on their dominance style, this group included some females that showed egalitarian tendencies, i.e., grooming was directed down the hierarchy or was well-balanced, and was directed toward unrelated females as often as or more often than toward related females. The presence of egalitarian individuals might be important to maintain a well-organized, female-bonded group.     

Sex and age differences in juvenile social priorities in female philopatric,nondespotic blue monkeys

Juveniles should choose social partners on the basis of both current and future utility. Where one sex is philopatric, one expects members of that sex to develop greater and sex‐typical social integration with group‐mates over the juvenile period. Where a partner's position in a dominance hierarchy is not associated with services it can provide, one would not expect juveniles to choose partners based on rank, nor sex differences in rank‐based preferences. We tested these ideas on 39 wild juvenile (3.2–7.4 years) blue monkeys (Cercopithecus mitis stuhlmanni), cercopithecines with strict female philopatry and muted hierarchies. We made focal animal observations over 6 months, and computed observed:expected amounts of proximity time, approaches and grooming given to various social partners. Overall, our results agree with the hypothesis that juvenile blue monkeys target social partners strategically. Spatial proximity, approaches and active grooming showed similar patterns regarding juvenile social preferences. Females were far more sociable than males, groomed more partners, reciprocated grooming more frequently, and preferred—while males avoided—infants as partners. Older juveniles (5–7 years) spent more time than younger juveniles (3–4 years) near others, and older females were especially attracted to infants. Close kin, especially mothers and less consistently adult sisters, were attractive to both male and female juveniles, regardless of age. Both sexes also preferred same‐sex juveniles as social partners while avoiding opposite‐sex peers. Juveniles of both sexes and ages generally neither preferred nor avoided nonmaternal adult females, but all juveniles avoided adult males. Partner's rank had no consistent effect on juveniles' preference, as expected for a species in which dominance plays a weak role. Juveniles' social preferences likely reflect both future and current benefits, including having tolerant adult kin to protect them against predators and conspecifics, same‐sex play partners, and, for females, infants on which to practice mothering skills. Am. J. Primatol. 72:193–205, 2010. © 2009 Wiley‐Liss, Inc.     

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

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

Grooming site preferences determined by lice infection among Japanese macaques in Arashiyama

I investigated the effect of the density of louse eggs (Pedicinus obtusus andP. eurygaster) on grooming site preferences in Japanese macaques (Macaca fuscata). Louse eggs were more often found on the outer side of the body (upper back, lower back, outer arms, and outer legs) than on the inner side of the body (chest, belly, inner arms, and inner legs). Japanese macaques were more likely to be groomed on the outer side than the inner side of the body by allogrooming and autogrooming. Such grooming site preferences correlated with the distribution of louse eggs but not with the areas of body parts. Thus, the ecology of lice might affect grooming behavior of Japanese macaques. Five hundred and fifty louse eggs were estimated to parasitize an adult female Japanese macaque. Considering the intrinsic rate of natural increase of lice, monkeys need to be groomed almost every day. This suggests that Japanese macaques need grooming partners and form social bonds with others for everyday grooming.     

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

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

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.     

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.     

Social grooming and play behavior of a captive group of chimpanzees

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

Grooming in brown howler monkeys,Alouatta fusca

The grooming behavior of a group of brown howler monkeys was studied for one year in an Atlantic forest reserve of southeastern Brazil. A total of 290 grooming bouts were recorded and analyzed. The two adult females directed most of the grooming (91%), while the adult male was the major recipient (37%). Grooming between females, and between them and their siblings, also occurred quite often. On average, the group spent 2% of its daily time grooming, with a higher frequency around noon. There were significant differences, however, in time spent grooming between seasons; grooming was more abundant during the coldest seasons (autumn–winter) and rarer in hotter ones (spring–summer). A significant negative correlation was found between grooming time and temperature, but contrary to expectations, grooming time failed to correlate with both the group' diet and the demands of food-gathering, as measured by travelling time and day range length. A comparison of grooming behavior with other species of the genus suggests that brown, red (A. seniculus), and black howler monkeys (A. caraya) are more similar to each other than to mantled howlers (A. palliata), a result that probably is linked with the differing social structure and group size of the latter species. © 1995 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.