Behavioural and hormonal responses to predation in female chacma baboons (Papio hamadryas ursinus)

In humans, bereavement is associated with an increase in glucocorticoid (GC) levels, though this increase can be mitigated by social support. We examined faecal GC levels and grooming behaviour of free-ranging female baboons to determine whether similar effects were also evident in a non-human species. Females who lost a close relative experienced a significant increase in GC levels in the weeks following their relative's death compared with the weeks before, whereas control females showed no such increase. Despite the fact that females concentrate much of their grooming on close kin, females who lost a close female relative did not experience a decrease in grooming rate and number of grooming partners; instead, both grooming rate and number of grooming partners increased after a relative's death. While the death of a close relative was clearly stressful over the short term, females appeared to compensate for this loss by broadening and strengthening their grooming networks. Perhaps as a result, females' GC levels soon returned to baseline. Even in the presence of familiar troop-mates and other relatives, females experienced a stress response when they lost specific companions, and they apparently sought to alleviate it by broadening and strengthening their social relationships.     

Social stressors and coping mechanisms in wild female baboons (Papio hamadryas ursinus)

We examined the social correlates of fecal glucocorticoid (GC) levels in wild female baboons during a period of social and demographic stability. Females' GC levels were not affected by individual attributes such as number of kin or dominance rank, nor could we detect any significant seasonal effects. Instead, GC levels were influenced by behavioral attributes that varied between individuals and within individuals across time. Pregnant and cycling females who received high rates of aggression had higher GC levels than others. In contrast, pregnant and cycling females who received grunts - vocal signals of benign intent - at high frequencies from dominant females had lower GC levels than females who received grunts at lower frequencies. Lactating females showed the opposite trend, apparently as a consequence of the high rate of grunting and intense, unsolicited attention that their infants received from others. All females experienced lower GC levels in months when they concentrated their grooming among a small number of partners than when their grooming was more evenly distributed among many partners. Although GC levels in female baboons are most strongly influenced by events that directly affect their reproductive success, subtle social factors associated with the loss of predictability and control also seem to exert an effect. Loss of control may be mitigated if a female is able to predict others' intentions - for example, if others grunt to her to signal their intentions - and if she is able to express some preference over the timing and identities of her grooming partners.     

Female dominance and female social relationships among yellow baboons (Papio hamadryas cynocephalus)

Adult females in a female-bonded, cercopithecine species such as baboons are characterized by hierarchically ranked matrilines, i.e., female offspring assume rankings just beneath those of their mothers. In this system of closely ranked matrilines, a female should engage in significantly more affiliative interactions with those individuals who are closely ranked to herself than with those individuals who are more distantly ranked. We examine the hypothesis that females in this troop of feral yellow baboons (Papio hamadryas cynocephalus) who are closely ranked will also show close social affiliation. We collected focal data on 23 feral, adult female subjects (253 possible dyads) over approximately 1 year at the Tana River National Primate Reserve, Kenya. Following Bramblett's [Behav Brain Sci 4: 435, 1981] method of dominance tabulation and utilizing a modified version of Smuts' [Sex and friendship in baboons, Hawthorne: Aldine Publishing Co., 1985] preferred partner index, we describe and compare the dominance matrix and hierarchy, preferred proximity partner and grooming partner sociograms, and the social networks of these 23 focal females. Over 1,400 interactions were utilized in the dominance tabulations, 41 statistically significant proximity partner preferences were documented, and 100 grooming dyads were recorded. We examine both partners' ranks and the presence of an infant as possible factors influencing proximity and grooming partner preferences. We find that in this population there is no direct correspondence between females' ranks and their affiliation partners. Neither proximity nor grooming preferences are consistently predictable from partners' ranks. While proximity preferences were not significantly influenced by the presence of an infant, grooming partner preferences were. Females with infants had more grooming partners and were more often involved in unidirectional grooming relationships as the recipients than were females without infants. We conclude that females' dominance rankings are not good predictors of either proximity partner or grooming partner preferences and that the presence of an infant does have a significant impact on grooming partner preferences in this population.     

Grooming and group structure in hamadryas baboons

The results of 3-year observation on coral living hamadryas baboons transported from natural habitat in Tuapse reservation have been presented. Despite of the fact that grooming between males and females accounted for 73% of total cases of grooming in adult individual pairs, only the relationships of males with high-ranked females of their harems fully corresponded to a star-shaped sociogram. The high-ranked females were not different from all the other females either according to a total number of grooming cases with their female partners or according to a proportion of a performed and received grooming. Grooming between the related females was noted predominantly in the cases when they belonged to the same harem. Grooming between the related males accounted for 59% of all the cases of grooming between the male partners.     

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

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

Male chimpanzees' grooming rates vary by female age, parity, and fertility status

Copulation preferences in our closest living relative, the chimpanzee, suggest that males prefer older females who have had previous offspring. However, this finding is counter to some behavioral models, which predict that chimpanzee males, as promiscuous breeders with minimal costs to mating, should show little or no preference when choosing mating partners (e.g. should mate indiscriminately). To determine if the preferences indicated by copulations appear in other contexts as well as how they interact, we examined how male chimpanzees' grooming patterns varied amongst females. We found that males' preferences were based on interactions among females' fertility status, age, and parity. First, grooming increased with increasing female parity. We further found an effect of the estrous cycle on grooming; when females were at the lowest point of their cycle, males preferentially groomed parous females at peak reproductive age, but during maximal tumescence, males preferred the oldest multiparous females. Nulliparous females received relatively little grooming regardless of age or fertility. Thus, male chimpanzees apparently chose grooming partners based on both female's experience and fertility, possibly indicating a two-pronged social investment strategy. Male selectivity seems to have evolved to effectively distribute costly social resources in a pattern which may increase their overall reproductive success.     

Long-term grooming partnerships between unrelated adult females in a free-ranging group of Japanese monkeys (Macaca fuscata)

In order to examine the presence of long-term grooming relationships among unrelated females, grooming interactions of 18 adult females (range: 16-32 years) in a free-ranging group of Japanese monkeys (Macaca fuscata) were recorded in 2003 and compared with those recorded 10 years earlier, i.e., in 1993. In 2003, on average, each female who had survived the 10 years had grooming interactions with 2.2 surviving old partners with whom she was recorded to have grooming interactions in 1993, 3.5 females related to the surviving old partners, and 4.5 unrelated females who were other than the surviving old partners or their related females. By calculating the ratio of actual grooming partners to available females in 2003, we concluded that females had a greater possibility of selecting surviving old partners as their grooming partners than other unrelated partners, and that they also had a greater possibility of selecting females related to surviving old partners than females other than surviving old partners and their related females. These findings indicate that with regard to grooming relationships, female Japanese monkeys are basically conservative, showing a tendency to concentrate their grooming interactions on closely related females and certain familiar unrelated females such as surviving old partners and some females closely related to these partners. At the same time, however, female Japanese monkeys also showed a progressive trait for grooming since they formed grooming relationships with new partners. The necessity of long-term psychological bonding for long-term grooming relationships between unrelated females is discussed in this work.     

A dynamic interaction between aggression and grooming reciprocity among female chacma baboons

We used data from a natural experiment on adult female chacma baboons, Papio cynocephalus ursinus, to test the hypothesis that variation in aggression through time influences patterns of grooming reciprocity within a social group. Owing to a change in the baboons' competitive regime, we were able to compare data from periods when aggression was high (period 1) and low (period 2). During period 2, the slope of the relationship between aggression and rank was significantly shallower than during period 1 and less aggression was directed at the lowest-ranking females suggesting there had been a reduction in the dominance gradient. We attributed this to reduced effectiveness of dominance as a means of excluding other females from feeding resources. The reduction in aggression during period 2 was accompanied by an increase in grooming reciprocity between dyads suggesting that high-ranking females no longer attracted grooming by subordinates in exchange for tolerance, and that grooming in period 2 was exchanged for its intrinsic benefits. The loss of rank-related effects on grooming reciprocity in period 2 compared with period 1 further confirmed this. These findings show that female baboons are able to respond flexibly and swiftly to changes in their social circumstances and that a dynamic approach to primate social interactions is worth pursuing. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

A case report of a male rank reversal in a group of wild white-faced capuchins (Cebus capucinus)

During the course of a study of social relationships in wild, white-faced capuchins at Lomas Barbudal, Costa Rice (May 1990–May 1993), the alpha male was deposed by a subordinate male. The rank reversal was preceded by a decline in proximity maintenance by females to the alpha male, and an increase, in the amount of aggression directed toward the alpha male by the beta female and her female coalition partners. At the time of the rank reversal, females switched from giving thegargle vocalization exclusively to the old alpha male to gargling to the new alpha male; however, juveniles were less consistent with regard to which male they gargled to. At the time of the rank reversal, most adult females reduced the time spent in proximity and grooming with the old alpha male, and increased the time spent in proximity and grooming with the new alpha male. In contrast, juveniles' patterns of affiliation with males did not change in a predictable way following the reversal. The social strategies employed by capuchin monkeys during this rank reversal are compared with those of chimpanzees.     

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.     

Persistence of sexual behavior in ovariectomized stumptail macaques following dexamethasone treatment or adrenalectomy

Daily administration over a period of 6 weeks of increasing doses of dexamethasone sodium phosphate (DEX) to seven long-term ovariectomized female stumptail monkeys significantly lowered circulating levels of testosterone without reducing any aspect of the females' sexual behavior or that of their male partners. Since treatment with DEX failed to suppress serum testosterone levels completely an additional experiment was performed in which the sexual behavior of five ovariectomized stumptails was compared before and after bilateral adrenalectomy, combined with chronic administration of both gluco- and mineralocorticoids. Serum levels of both testosterone and estradiol were reduced to very low levels in females after ovariectomy and adrenalectomy, yet no significant depression of females' sexual performance or that of their male partners occurred. Subsequent sc administration of estradiol or estradiol + testosterone in Silastic capsules to ovariectomized, adrenalectomized stumptails had little effect on sexual interaction. In a third experiment five ovariectomized stumptails which initially were relatively unreceptive and unattractive to males were given first testosterone and then testosterone + estradiol sc in Silastic capsules. One of the three indexes of females' receptivity increased significantly after testosterone; however, no other essential aspect of sexual interaction was affected. These findings suggest that sex steroids are normally not required in the female stumptail macaque for activation of preceptive and receptive sexual behaviors or for maintenance of sexual attractivity.     

The effect of solicitations on grooming exchanges among female Japanese macaques at Katsuyama

In group-living primates, individuals often exchange grooming with not only kin but also non-kin. We investigated the effect of soliciting behaviors on grooming exchanges in a free-ranging Japanese macaque (Macaca fuscata) group at Katsuyama. In this study, we used a focal animal sampling method, targeting 14 females. Data were collected for 15.75 ± 2.67 (mean ± SD) hours per focal female. We classified female–female pairs into three pair types: kin pairs, affiliated non-kin pairs, and unaffiliated non-kin pairs. Females received grooming more frequently when they solicited after grooming their partners than when they did not solicit in all pair types. In addition, females received grooming less frequently when they did not groom their unaffiliated non-kin partners before soliciting; prior grooming was not needed to receive grooming from kin or affiliated non-kin partners. The degree of grooming reciprocity did not differ according to the frequency with which females in kin or affiliated non-kin pairs solicited after grooming. On the other hand, grooming reciprocity between unaffiliated non-kin females was more balanced when they solicited frequently after grooming, as compared with when they did not. In conclusion, our study suggests that soliciting behaviors promote grooming exchanges in female Japanese 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.     

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.     

Rank and grooming reciprocity among females in a mixed-sex group of captive hamadryas baboons

In a mixed-sex, captive group of hamadryas baboons (Papio hamadryas hamadryas) we investigated whether female grooming relationships are affected by their dominance ranks. Seyfarth's [1977] grooming for support model and Barrett et al.'s [1999] biological market model both predict that in primate groups where competition for monopolizable resources is high, grooming among females is based, at least partly, on the interchange of grooming for rank-related benefits, and that rank thus influences the distribution of grooming in females. Contrary to this prediction, our results show that despite the existence of a linear dominance hierarchy, rather strict dominance relationships, and high food-related aggression rates, grooming among female hamadryas baboons is not affected by rank and is only exchanged for itself. This is understandable since rank differences in our study group only result in differential access to limited, preferred food items that are not actively shared. Although some females are more likely to tolerate one another at the food pile, this tolerance is not determined by their grooming efforts and interchange of grooming for rank-related benefits does not occur. We conclude that female hamadryas baboons groom others in order to be groomed by them, which is supported by our observation that grooming reciprocity within a dyad increases when more grooming occurs in this dyad. Our results indicate that grooming is indeed a valuable commodity in itself, probably because of its stress- and tension-reducing effect. Based on our findings, the existing groom trade model is extended to include circumstances in which monopolizable resources are available but are not traded for grooming.     

Grooming relationships of adolescent orphans in a free-ranging group of Japanese macaques (Macaca fuscata) at Katsuyama: a comparison among orphans with sisters, orphans without sisters, and females with a surviving mother

The present study examined grooming relationships of adolescent females in a free-ranging group of Japanese macaques (Macaca fuscata) at Katsuyama. To assess whether the loss of the mother influenced the grooming relationships of adolescent females (5–7 years old), we compared the time spent in grooming interactions and the number of grooming partners among the following three groups: 6 adolescent orphans with sisters, 9 adolescent orphans without sisters, and 11 adolescent non-orphans with surviving mothers. In Japanese macaques, grooming most frequently occurs between mothers and their daughters. Therefore, it is expected that if the mother is lost, orphans will devote less time to grooming interactions than non-orphans. However, the time spent in overall grooming interactions did not differ among the three groups. While non-orphans maintained grooming relationships with their mothers, orphans acquired alternative grooming relationships with other group members. Orphans adopted two kinds of tactics to compensate for the loss of the mother. First, adolescent orphans with sisters developed more affiliative grooming relationships with their sisters than non-orphans with sisters. Secondly, adolescent orphans without sisters spent more time in grooming interactions with same-aged females and non-related adult females. Moreover, regarding grooming interactions with same-aged females and non-related adult females, orphans without sisters had a larger number of grooming partners than non-orphans. These results indicate that adolescent females have enough flexibility to develop their grooming network after the loss of their mothers, and that the lack of mother and sisters might accelerate socialization of adolescent females and enable them to be integrated in reciprocal adult grooming relationships.     

Grooming relationships between breeding females and adult group members in cooperatively breeding moustached tamarins (Saguinus mystax)

Grooming is the most common form of affiliative behavior in primates that apart from hygienic and hedonistic benefits offers important social benefits for the performing individuals. This study examined grooming behavior in a cooperatively breeding primate species, characterized by single female breeding per group, polyandrous matings, dizygotic twinning, delayed offspring dispersal, and intensive helping behavior. In this system, breeding females profit from the presence of helpers but also helpers profit from staying in a group and assisting in infant care due to the accumulation of direct and indirect fitness benefits. We examined grooming relationships of breeding females with three classes of partners (breeding males, potentially breeding males, (sub)adult non-breeding offspring) during three reproductive phases (post-partum ovarian inactivity, ovarian activity, pregnancy) in two groups of wild moustached tamarins (Saguinus mystax). We investigated whether grooming can be used to regulate group size by either "pay-for-help" or "pay-to-stay" mechanisms. Grooming of breeding females with breeding males and non-breeding offspring was more intense and more balanced than with potentially breeding males, and most grooming occurred during the breeding females' pregnancies. Grooming was skewed toward more investment by the breeding females with breeding males during the phases of ovarian activity, and with potentially breeding males during pregnancies. Our results suggest that grooming might be a mechanism used by female moustached tamarins to induce mate association with the breeding male, and to induce certain individuals to stay in the group and help with infant care.     

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.     

Social relationships of nulliparous young adult females beyond the ordinary age of the first birth in a free-ranging troop of Japanese macaques (Macaca fuscata)

We describe the social relationships of young adult female Japanese macaques (Macaca fuscata) in a free-ranging troop in Arashiyama, Kyoto, Japan, who remained nulliparous beyond the ordinary age of first birth because of contraceptive administration. We observed 12 young nulliparous adult females (6–9 years old) for 270 h and 10 min from 2 February to 5 October 2010. The majority maintained close relationships with their mothers through proximity and grooming, whereas a few had very infrequent social interactions with their mothers. Most had asymmetrical grooming relationships; the grooming they received from unrelated adult females was less than the grooming they gave. Young adult females who had less frequent interactions with their mothers by either proximity or grooming received more grooming from a larger number of unrelated adult females than did those who had more frequent social interactions with their mothers. These results indicate that most young adult females who remained nulliparous beyond the ordinary age of first birth tended to maintain close relationships with their mothers, and their grooming relationships with unrelated adult females were inversely related to the degree of closeness with their mothers.     

Individual contributions to a dyadic interaction: An analysis of baboon grooming

Grooming in dyads of six captive female hamadryas baboons (Papio hamadryas) was analysed. Each dyad was observed in isolation and as part of a group of three to six females. The isolated dyads differed from dyads in groups, as follows. (1) Grooming in isolated dyads mainly depended on the actor's general tendency to groom, whereas actors in groups were more responsive to who the recipient was. (2) In groups, grooming tended to be more frequent among females of high dominance rank and among females who preferred one another in choice tests. The opposites were true for isolated dyads. Females in isolated dyads seemed to use grooming to improve a poor relationship, whereas grooming in groups was used as if to maintain and defend a valuable relationship.