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.     

Supply and Demand Determine the Market Value of Access to Infants in the Golden Snub-Nosed Monkey (Rhinopithecus roxellana)

According to a biological market paradigm, trading decisions between partners will be influenced by the current ‘exchange rate’ of commodities (good and services), which is affected by supply and demand, and the trader’s ability to outbid competitors. In several species of nonhuman primates, newborn infants are attractive to female group members and may become a desired commodity that can be traded for grooming within a biological market place. We investigated whether grooming was interchanged for infant handling in female golden snub-nosed monkeys (Rhinopithecus roxellana) inhabiting the Qinling Mountains of central China. R. roxellana exhibit a multilevel social organization characterized by over 100 troop members organized into 6–11 one-male units each composed one adult male and several adult females and their offspring. Behavioral data were collected over the course of 28 months on grooming patterns between mothers with infants less than 6 months old (N = 36) and other adult female troop members. Our results provide strong evidence for the interchange of grooming for access to infants. Grooming for infant access was more likely to be initiated by potential handlers (nonmothers) and less likely reciprocated by mothers. Moreover, grooming bout duration was inversely related to the number of infants per female present in each one-male unit indicating the possibility of a supply and demand market effect. The rank difference between mothers and handlers was negatively correlated with grooming duration. With increasing infant age, the duration of grooming provided by handlers was shorter suggesting that the ‘value’ of older infants had decreased. Finally, frequent grooming partners were allowed to handle and maintain access to infants longer than infrequent groomers. These results support the contention that grooming and infant handling may be traded in R. roxellana and that the price individuals paid for access to infants fluctuated with supply and demand.     

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.     

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.     

Mother-infant interactions of wild-born,individually-caged cynomolgus monkeys (Macaca fascicularis) during the first 14 weeks of infant life

This study documents age-related changes in the interactions of wild-born cynomolgus macaque mothers and their infants living in individual cages during the first 14 weeks of infant life. Body contact between mother and infant, maternal holding, and infant sucking were found to decrease, and the mothers showed an increased frequency of aggression toward their infants with age. These results were broadly similar to those reported for mother-infant interactions in other macaques living in social groups. Nevertheless, a clear difference between the present cynomolgus macaques and other macaques in social groups was apparent. The cynomolgus macaque mothers tended to permit their infants to move about freely without displaying maternal protectiveness such as restraint or retrieval, unlike other macaque mothers in social groups. Such maternal behaviors might derive from the experience of living in individual cages for many years and the relative safety of living in individual cages. The lack of maternal restraint and retrieval could be responsible for the observed sex differences in behavior: male infants moved more actively, and broke, and made contact with their mothers more frequently than did female infants. Moreover, mothers of female infants held and groomed them more frequently and were less aggressive toward them.     

Decision making in grooming by Japanese macaques (Macaca fuscata)

I analyzed the temporal organization of individual Japanese macaques’ (Macaca fuscata) grooming sequences in 14 mothers and 13 offspring of different age/sex classes and 4 nonkin females. I hypothesized that preceding grooming affects subsequent grooming by the same individual. Grooming bouts were likely to be terminated as the bouts became longer when females groomed nonrelatives. Moreover, the duration of first bouts was longer than that of following bouts. These effects were also seen in grooming of mothers by their offspring > 1 year old and that of adult and adolescent female offspring by their mothers. In contrast, neither the duration of first bouts nor the number of preceding bouts had much effect on the occurrence or duration of subsequent bouts in any subject.     

Social behavior of infant and mother Japanese Macaques (Macaca fuscata): Effects of kinship,partner sex,and infant sex

The behavioral interactions of 22 infant and mother Japanese macaques with other group members were studied. Focal-animal observations were made from the time of each infant’s birth until 1 year of age. Infants and mothers both displayed exceedingly strong preferences for associating with matrilineal kin and, specifically, for female kin. The degree of genetic relatedness was positively correlated with levels of spatial proximity, contact, grooming, aggression, and play. Overall frequencies of interactions with nonkin were very low, and partner sex was not an important factor in interactions with nonkin. There were no significant differences between male and female infants in interactions with kin versus nonkin. There was only one significant difference between male and female infants in interactions with males versus females: female infants showed stronger preferences for initiating proximity with females over males than did male infants. Because mothers provide the focal point for infant interactions during the first year of life, we compared the behavior of infants and mothers. Mothers were the recipients of more social interactions than were infants, mothers engaged in more grooming than did infants, and infants engaged in more social play than did mothers. These findings are only partially consistent with kin-selection theory, and the inadequacies of studying matrilineal kin discrimination to test kin selection are reviewed. The near-absence of infant sex differences in associations with social partners suggests that although maternal kin other than the mother are important to infant socialization, they probably do not contribute to the development of behavioral sex differences until after the first year of life.     

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.     

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

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

Grooming behavior of spider monkeys (Ateles geoffroyi) on barro colorado Island,Panama

Quantitative grooming data are presented for free-ranging black-handed spider monkeys (Ateles geoffroyi) on Barro Colorado Island, Republic of Panama. A total of 126 grooming sessions was recorded, with an average session length of 2.0 min (range, 0.1 to 10.0 min). Grooming was an infrequent behavior; on average, individuals allocated only 2.5% of their daily activity to grooming. Two daily peaks of grooming activity were observed, one near midday and another in the late aftermoon between 1600 and 1700. Adult females groomed most frequently, followed by males and then juveniles. Juveniles were the most frequent recipients of grooming, followed by females and then males. Individual preferences were observed primarily between mother-offspring, male-male, and juvenile-male grooming partners in this male-bonded fission-fusion, species. Grooming interactions reflect many of the social characteristics of spider monkey societies: intraclass grouping preferences, long period of juvenile dependence, male philopatry, and female dispersal.     

Infants as a commodity in a baboon market

We used data from adult female chacma baboons, Papio cynocephalus ursinus, to provide the first test of hypotheses on interchange trading and the structure of a biological market (Noë & Hammerstein 1994, Behavioral Ecology and Sociobiology,35, 1-11) within a primate group. The interchange commodities selected were grooming and handling of infants less than 3 months of age. Patterns of grooming in relation to infant handling showed strong evidence for interchange. Grooming for infant access was initiated by potential handlers and was significantly likely to be nonreciprocated. More critically, the data show that infant ‘supply’ created a market effect: grooming bout duration (the price ‘paid’ for handling) was inversely related to the number of infants present in the group. In addition, there was an inverse relationship between grooming bout duration and the rank distance between mothers and handlers, suggesting that higher-ranking mothers could demand a higher price for infant handling. Where rank distance was high, females were able to handle infants without grooming. Dominance could thus be used to disrupt the infant market effect. If biological markets models are to be fully applicable to primate groups (and those of other social mammals) then the potentially distorting effect of dominance needs to be incorporated into the framework. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Complex patterns of grooming and sexual activity in Barbary macaques (Macaca sylvanus)

Grooming in primates is often considered a “currency” that can be exchanged for other “services” or “commodities” such as reciprocal grooming, coalitionary support, infant handling, tolerance around food sources, active food sharing, or mating opportunities. Previous studies on primate grooming‐for‐sex exchange viewed the males as the demanding class, with the females as suppliers of mating opportunities. In this study, we examine the broader context of grooming‐for‐mating exchange in Barbary macaques in Gibraltar. Our data show that Barbary macaque males groom females with whom they are mating more frequently and for longer periods than other females, and the relationship between grooming and mating remains significant in both sexual and nonsexual contexts. In addition, females groomed males with whom they were mating more frequently and for longer periods than other males. In both sexes, grooming was observed to be far more frequent and to occur for longer durations in sexual compared to nonsexual contexts. We did not find any difference in grooming behavior between presexual and postsexual contexts. Our data suggest that there is no simple model to describe Barbary macaque grooming patterns in sexual contexts. Although our results are partly consistent with male use of grooming as payment for mating, broadly assessed grooming‐mating patterns cannot be solely explained by a male‐driven grooming‐for‐mating exchange.     

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.     

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.     

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.     

Infant handling in wild Cebus capucinus: testing bonds between females?

The evolved functions, if any, of infant handling (IH) by female primates remain unclear for many species. I tested a new hypothesis, that IH tests social bonds between adult females, using data on a group of wild white-faced capuchins. I also tested the nonadaptive, learning-to-mother, reciprocity, harassment and alliance-formation hypotheses. Focal subjects were the mothers of 10 infants that ranged in age from 0 to 90 days. The behaviours comprising IH (inspecting, nuzzling, sniffing, and a distinctive vocalization) differed from typical maternal behaviour. Nulliparous females engaged in no more IH than did parous females. The median frequency of rough handling was zero, kidnapping was not observed, and maternal restraint of infants was extremely rare. Infant handling rate was unrelated to the relative dominance ranks of the mother and the handler. Females tended to handle the infants of females with which they groomed and formed aggressive coalitions more frequently. Dyadic IH rates were not correlated with rates of allonursing when the infants were older than 90 days of age. There was no evidence for reciprocal exchanges of IH between females. Mother-terminated IH bouts were longer when the mother had groomed the handler more frequently before the infant's birth. Based on these findings, the learning-to-mother, reciprocity and harassment hypotheses are unsupported for this species. Some support exists for the nonadaptive hypothesis. Contrasting predictions of the bond-testing and alliance-formation hypothesis are presented for future testing. Copyright 1999 The Association for the Study of Animal Behaviour.     

Social structures in Pan paniscus: testing the female bonding hypothesis

Based on previous research in captivity, bonobos, Pan paniscus, have been called a female-bonded species. However, genetic and behavioural data indicate that wild females migrate. Bonding between these unrelated females would then be in contradiction with socio-ecological models. It has been argued that female bonding has been overemphasized in captive bonobos. We examine patterns of proximity, grooming and support behaviour in six well established captive groups of bonobos. We find that female bonding was not a typical characteristic of all captive bonobo groups. In only two groups there was a trend for females to prefer proximity with other females over association with males. We found no evidence that following or grooming between females was more frequent than between males and unrelated females or between males. Only in coalitions, females supported each other more than male–female or male–male dyads. We also investigated five mother–son pairs. Grooming was more frequent among mothers and sons than in any other dyad, but sons did not groom their mothers more than males groomed unrelated females. Mothers groomed their sons, or provided more support to them than females groomed or supported unrelated males. Thus, while bonds between females were clearly present, intersexual relations between males and either unrelated females or their mothers are of more, or equal importance.     

Grooming behaviors of black‐tailed prairie dogs are influenced by flea parasitism,conspecifics, and proximity to refuge

Grooming is a common animal behavior that aids in ectoparasite defense. Ectoparasites can stimulate grooming, and natural selection can also favor endogenous mechanisms that evoke periodic bouts of “programmed” grooming to dislodge or kill ectoparasites before they bite or feed. Moreover, grooming can function as a displacement or communication behavior. We compared the grooming behaviors of adult female black‐tailed prairie dogs (Cynomys ludovicianus) on colonies with or without flea control via pulicide dust. Roughly 91% of the prairie dogs sampled on the non‐dusted colony carried at least one flea, whereas we did not find fleas on two dusted colonies. During focal observations, prairie dogs on the non‐dusted colony groomed at higher frequencies and for longer durations than prairie dogs on the dusted colonies, lending support to the hypothesis that fleas stimulated grooming. However, the reduced amount of time spent grooming on the dusted colonies suggested that approximately 25% of grooming might be attributed to factors other than direct stimulation from ectoparasites. Non‐dusted colony prairie dogs rarely autogroomed when near each other. Dusted colony prairie dogs autogroomed for shorter durations when far from a burrow opening (refuge), suggesting a trade‐off between self‐grooming and antipredator defense. Allogrooming was detected only on the non‐dusted colony and was limited to adult females grooming young pups. Grooming appears to serve an antiparasitic function in C. ludovicianus. Antiparasitic grooming might aid in defense against fleas that transmit the plague bacterium Yersinia pestis. Plague was introduced to North America ca. 1900 and now has a strong influence on most prairie dog populations, suggesting a magnified effect of grooming on prairie dog fitness.     

The response of some prosimian primate mothers to their own anesthetized infants

Six lemur mothers of three different species and oneGalago crassicaudatus mother were observed in the presence of their own anesthetized infants. Two of the lemur mothers spent only very brief periods sitting near their infants and seldom groomed them; the other four spent over half of the infant immobility period in close proximity to their infants and groomed them frequently. Four lemur mothers groomed the ano-genital region of their infant at least once. None of the lemur mothers picked up or carried her immobilized infant, as has been reported for some higher primate mothers, although one lemur mother used her hands to pull the infant toward her ventrum while sitting on the floor. Five lemur mothers rejected their infants when the infants displayed disoriented behavior while emerging from anesthesia. The galago mother retrieved her anesthetized infant in her jaws but dropped the infant several times while attempting to groom it. These results suggest very tentatively that prosimian mothers lack the ability shown by mothers of some higher primate species to improvise protective ways of behaving toward helpless infants.     

Birth Timing and Behavioral Responsiveness Predict Individual Differences in the Mother–Infant Relationship and Infant Behavior During Weaning and Maternal Breeding

There is a great deal of variability in mother–infant interactions and infant behavior across the first year of life in rhesus monkeys. The current article has two specific aims: (1) to determine if birth timing predicts variability in the mother–infant relationship and infant behavior during weaning and maternal breeding, and (2) to identify predictors of infant behavior during a period of acute challenge, maternal breeding. Forty‐one mother–infant pairs were observed during weaning when infants were 4.5 months old, and 33 were followed through maternal breeding. Subjective ratings of 16 adjectives reflecting qualities of maternal attitude, mother–infant interactions, and infant attitude were factor analyzed to construct factors relating to the mother–infant relationship (Relaxed and Aggressive) and infant behavior (Positive Engagement and Distress). During weaning, late born infants were more Positively Engaged than peak born infants (ANOVA, P < 0.05); however, birth timing did not affect the mother–infant relationship factors Relaxed and Aggressive or the infant attitude factor Distress. During maternal breeding, early born infants had less Relaxed relationships with their mothers than peak or late born infants, higher Positive Engagement scores than peak or late born infants, and tended to have higher Distress scores than peak born infants (repeated‐measures ANOVA, P < 0.05). In addition, Distress scores were higher during maternal breeding than during the pre‐ and postbreeding phases. Finally, multiple regression (P < 0.05) indicated that while infant behavioral responsiveness predicted infant Positive Engagement during the acute challenge of maternal breeding, qualities of the mother–infant relationship predicted infant Distress. These data suggest that birth timing influences the patterns of mother–infant interactions during weaning and maternal breeding. Additionally, infant behavioral responsiveness and mother–infant relationship quality impact infant social engagement and affect expression, respectively. Am. J. Primatol. 74:734‐746, 2012. © 2012 Wiley Periodicals, Inc.