Grooming Partners Research Articles

Group unity of chimpanzees elucidated by comparison of sex differences in short-range interactions in Mahale Mountains National Park, Tanzania

Chimpanzees (Pan troglodytes) form multi-male and multi-female unit groups with fission-fusion grouping patterns. Short-range interaction (SRI) plays an important role in the unity of these groups and in maintaining social bonds among members. This study evaluated three models of chimpanzee social structure that differed according to the emphasis each placed on social bonds between the sexes, i.e., the male-only, the bisexual, and the male-bonded unit-group model. I investigated differences in SRI between the sexes among group members in well-habituated wild chimpanzees in Mahale Mountains National Park, Tanzania. I followed six focal adult males and six females, and quantified their respective SRI with other chimpanzees. Except between subordinate males and adult females, adults in general engaged in SRI with about 60-90% of the individuals with whom they made visual contact each day, whether in large or small parties. Although the number of social grooming (SGR) partners was limited, male-male SGR networks were wider than were either male-female or female-female SGR networks among adults. The number of contact-seeking behavior (CSB) partners was also limited, but dominant males had more CSB partners. Adult females mainly interacted by pant-grunt greeting (PGG) with adult males, but tended to do so mainly with the highest-ranking male(s) within visual contact. These results indicated that the social bonds among adult males were essential to group unity. Because of clear male dominance, adult females established peaceful coexistence with all group members despite less frequent SRI with subordinate males by maintaining affiliative social bonds with dominant males, thereby supporting the male-bonded unit-group model. Adult females had many female SRI partners, but these interactions did not involve performing conspicuous behaviors, suggesting that females maintain social bonds with other females in ways that differ from how such bonds are maintained with and between adult males.

Analysing the effects of group size and food competition on Japanese macaque social relationships

Socio-ecological models predict group size to be one major factor affecting the level of food competition. The aims of this study were to analyse how grooming distribution and reconciliation were affected by differences in group size and food competition in a habitat where predation risk is absent. Data were collected on two groups of different size of wild Japanese macaques (Macaca fuscata yakui), living on Yakushima Island, Japan. The large group faced a greater level of intra-group scramble and a lower level of inter-group food competition. However, intra-group food competition appeared to be greater in the small group as evidenced by the stronger rank-related effects on diet composition in the small group. Grooming and reconciliation were more matrilineally kin-biased and more directed toward close-ranking monkeys in the small group than in the large group. Reconciliation was more frequent in the small group, but monkeys in the large group spent more time grooming and had a greater number of grooming partners. These results indicate that social relationships within the two groups were the result of the combination of group size differences and of the balance between the benefits and costs of a lower/greater level of inter- and intra-group food competition.

Grooming, rank, and agonistic support in tufted capuchin monkeys

Studies investigating the relation between allogrooming and social rank in capuchin monkeys (genus Cebus) have yielded inconsistent results. In this study, we investigated the relation between grooming, agonistic support, aggression and social rank in a captive group of tufted capuchin monkeys (C. apella). Differently from most previous studies, we based our analyses on a relatively large database and studied a group with known genealogical relationships. Tufted capuchin females did not exchange grooming for rank-related benefits such as agonistic support or reduced aggression. Coherently with this picture, they did not groom up the hierarchy and did not compete for accessing high-ranking grooming partners. It is suggested that a small group size, coupled with a strong kin bias, may make the exchange of grooming for rank-related benefits impossible or unprofitable, thus eliminating the advantages of grooming up the hierarchy. We provide several possible explanations for the heterogeneity of results across capuchin studies that have addressed similar questions.

Sexual Differences in Chimpanzee Sociality

Scientists usually attribute sexual differences in sociality to sex-specific dispersal patterns and the availability of kin within the social group. In most primates, the dispersing sex, which has fewer kin around, is the less social sex. Chimpanzees fit well into the pattern, with highly social philopatric males and generally solitary dispersing females. However, researchers in West Africa have long suggested that female chimpanzees can be highly social. We investigated whether chimpanzees in the Taï Forest (Côte d’Ivoire) exhibit the expected sexual differences in 3 social parameters: dyadic association, party composition, and grooming interactions. Though we found a significant sexual difference in each of the 3 parameters, with males being more social than females, the actual values do not reveal striking differences between the sexes and do not support the notion of female chimpanzees as asocial: females had dyadic association indices comparable to mixed-sex dyads, spent ca. 82% of their time together with other adult chimpanzees, and had a comparable number of grooming partners. Further, female associations can be among the strongest bonds within the community, indicating that both sexes can have strongly favored association partners. The findings are in contrast to reports on East African chimpanzees, the females of which are mainly solitary and rarely interact with other females. Our results suggest that researchers cannot generally regard chimpanzee females as asocial and need to redefine models deriving patterns of sociality from dispersal patterns to integrate the possibility of high female sociality in male philopatric systems.

Variation in kin bias over time in a group of Tibetan macaques at Huangshan, China: contest competition, time constraints or risk response?

We examine variation in grooming kin bias intensity (KBI) among wild female Tibetan macaques ( Macaca thibetana huangshanensis ) in one group over time. We test three hypotheses based on socioecological theory, time constraints and risk-related responses. Only the time constraints hypothesis was supported. Grooming KBI was higher when the group was larger, but was unrelated to other indicators of within-group competition. Allies were not necessarily frequent grooming partners; thus, support did not depend on maintaining strong grooming relationships. Females groomed similar amounts, regardless of group size, but groomed smaller percentages of available partners when the group was larger, suggesting that they were unable to maintain grooming relationships with all females as the group expanded. Females with several close kin groomed each of them less than females with few. The lowest ranking females tended to groom close kin almost exclusively, as expected if they had less grooming time to spare than other females. Although grooming KBI was higher when stressful external risks (many humans) were present, the correlation was unsustained when group size was controlled. We suggest that kin-focused grooming networks are shaped at least in part by time constraints and may not be linked directly or indirectly to within-group competition.

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.

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.

Reciprocation and interchange in wild Japanese macaques: grooming, cofeeding, and agonistic support

Social primates spend a significant proportion of their time exchanging grooming with their group companions. Although grooming is mainly exchanged in kind, given its hygienic and tension-reducing functions, it is still debated whether grooming also provides some social benefits, such as preferential access to resources (e.g., food or mating partners). In this study we analyzed grooming distribution among wild female Japanese macaques living in two groups on Yakushima. We tested the tendency of monkeys to reciprocate the amount of grooming received, and to direct their grooming up the hierarchy. Then we analyzed the relation of grooming to three of its possible benefits: reduced aggression, increased tolerance over food, and agonistic support against a male aggressor. The data were analyzed by means of row-wise matrix correlations. Grooming was highly reciprocated (i.e., exchanged in kind) and directed up the hierarchy in both the study groups. No significant relationship was found between grooming and aggression. Conversely, grooming favored tolerance over food, since it was positively correlated with presence on the same food patch, close proximity, and close approaches (both within 1 m) during feeding. Grooming was also positively related to agonistic support against adult males, although this relationship became nonsignificant when we controlled for kinship. Although these results are not definitive, they suggest that monkeys may derive various social benefits from grooming. This conclusion is supported by the fact that in various primate species animals tend to prefer high-ranking individuals as grooming partners.

Meat sharing among the Gombe chimpanzees: harassment and reciprocal exchange

Sharing food with nonkin is detrimental to a food donor's fitness, unless it is matched by compensatory benefits. I evaluated two explanations for nonkin meat sharing among wild chimpanzees, Pan troglodytes schweinfurthii. Reciprocal exchange proposes that a possessor relinquishes food in exchange for past or future sharing or for items of a different currency (e.g. grooming, alliances or copulations). The second hypothesis is the sharing-under-pressure/harassment model, which proposes that an individual shares to avoid the costs of defending a food item against persistent beggars. At Gombe National Park, Tanzania, I collected dyadic grooming and association data during focal follows of adult male chimpanzees. I videotaped meat-eating bouts, subsequently extracting detailed begging and sharing data. There was mixed support for the reciprocal exchange hypothesis. Sharing with males was not influenced by overall association and grooming rates. Female sexual receptivity did not affect the probability of sharing, nor did sharing increase the probability of mating. Meat possessors shared larger amounts, and were more likely to share actively with frequent female grooming partners. However, this pattern may have resulted from increased harassment by these individuals. In contrast, the sharing-under-pressure hypothesis was consistently supported: the possessor's feeding rate decreased with the number of beggars, the probability of sharing increased with the occurrence and duration of harassment, and harassment decreased following sharing events. I conclude that the pattern of meat sharing among the Gombe chimpanzees is largely explained by the sharing-under-pressure hypothesis, while the significance of reciprocal exchange remains unclear.

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.

Intracommunity Coalitionary Killing of an Adult Male Chimpanzee at Ngogo, Kibale National Park, Uganda

Intercommunity coalitionary killing of adult and adolescent males has been documented in two chimpanzee communities in the wild, and it was strongly suspected in a third. It may increase survivorship for the attackers, their mates, and their offspring by reducing the combined strength of hostile neighbors and/or by increasing territory size and food availability, and it may help the attackers to attract mates. Lethal coalitionary attacks by males on other male members of their own communities would not provide these benefits and are not expected, given the importance of cooperation among male community members in contests for dominance rank and in both defense and offense against neighboring males. Nevertheless, intracommunity coalitionary killings associated with struggles for alpha rank occur in the wild and in captivity, and observers have seen serious gang attacks on maturing adolescent and young adult males at Mahale and Budongo: the victim in the Budongo case was killed (Fawcett and Muhumuza, 2000). I describe a lethal attack on a young adult male by a large coalition of males from his community at Ngogo, Kibale National Park, Uganda. The Ngogo community is the largest known for chimpanzees and has an unusually large number of males. The attack was not related to a struggle for alpha rank: the victim was low-ranking and the community had a well-established alpha at the time. However, the victim had risen substantially in the male hierarchy over the past few years and might have appeared threatening to many higher-ranking males. Simultaneously, he associated relatively little with most other adult males, had relatively few grooming partners and was not well integrated into the male grooming network, and had no influential allies. The combination of these social factors with the unusual demographic circumstances – which presumably meant that mating competition was relatively high and the cost of losing one male relatively low – might have triggered the attack.

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.

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.

Grooming Interactions Among the Chimpanzees of the Budongo Forest, Uganda: Tests of Five Explanatory Models

AbstractPatterns of allogrooming among the Sonso community of chimpanzees of the Budongo Forest, Uganda, were examined and found to closely resemble those at other study sites. Strong affiliative bonds among males were reflected in high levels of grooming compared with other sex combinations. Adult males groomed, and received grooming most often from, other adult males and also adolescent females which were the only females with regular oestrous cycles during the study. Males had a wider diversity of grooming partners than females and groomed more equitably. However, males concentrated the majority of their effort on a very small number of partners compared with other sites. Grooming reciprocity was found among all age/sex combinations with the exception of adult male-female dyads once immediate reciprocation in the form of synchronous mutual grooming was removed from the analysis. Since grooming among males is thought to play a major role in servicing relationships and agonistic coalitions that can improve dominance status, competition for high-ranking grooming partners was predicted to influence the distribution of grooming among males. Grooming was indeed directed up the male hierarchy and closely ranked males groomed each other more often than those that were distantly ranked. However, when only adult males were considered, rank had little effect on grooming distributions. High rank appeared to influence access to females, but did not attract more female grooming partners. Grooming distributions in this average-sized community did not fit a number of alternative priority of access models which assume competition for high-ranking grooming partners that Watts (2000b) found to have some explanatory value in one very large community of chimpanzees, but not in a smaller, more representative one. Although rank is highly likely to influence coalition partner choice, whether such relationships depend upon strategic grooming partner choices in wild chimpanzees is presently unclear.

Matrilineal Cohesion and Social Networks in Macaca fuscata

In a provisioned troop of Japanese macaques (Macaca fuscata) in Arashiyama, Japan, greater adherence to Kawamura's rules of matrilineal rank inheritance and youngest ascendancy occurred among high-ranking females versus low-ranking females. Accordingly, high-ranking females formed more clustered hierarchies and low-ranking females had more dispersed hierarchies. A proximate explanation for this finding may be related to differences in how females maintain their social networks. To determine whether the clustering in the hierarchy was reflected in patterns of social cohesiveness, I compared network sizes of coalition and grooming partners for females in each third of the hierarchy. I calculated the proportion of available partners that were coalition and grooming partners within each category of relatedness (0.5 ≥ r ≤ 0.004 and r = 0). High-ranking females formed coalitions with a large proportion of their close relatives and a small proportion of their distant relatives; middle-ranking females supported an intermediate proportion of their close relatives and a small proportion of their distant relatives; and, low-ranking females formed coalitions with very few available close and distant relatives. High-ranking females groomed nearly all available close relatives and an intermediate proportion of distant relatives, whilst middle- and low-ranking females groomed a large proportion of available close relatives and a very small proportion of distant relatives. Thus, levels of clustering within the hierarchy appeared to reflect levels of social cohesion, in terms of grooming and coalition formation.

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.

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

I investigated the effect of the density of louse eggs (Pedicinus obtusus and P. 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.

Reconciliation in Captive Chimpanzees: A Reevaluation with Controlled Methods

Affiliative postconflict reunions—reconciliations—of former opponents were first demonstrated in the chimpanzees at the Arnhem Zoo. Since then methods have been considerably refined, and reconciliation has been demonstrated in a large number of primates and also some gregarious nonprimates. This study, conducted with a different captive group, is the first to use the revised methodology with chimpanzees. We analyzed a total of 297 agonistic conflicts with the PC–MC method: we observed focal individuals for 15 min after a conflict and during matched control observations the next day. The mean conciliatory tendency of the 16 chimpanzees was 41%, with a range in different age-sex classes of 58% (among adult females) to 19% (among adult vs. immature males). After conflicts, former opponents were selectively attracted to one another. Preferential contact with previous opponents persisted when activity level during matched controls was controlled for statistically. Opponents that were frequent grooming partners reconciled more frequently, but the frequency of agonistic support had no such effect. Our findings thus confirm the existence of reconciliation in chimpanzees, which show one of the highest conciliatory tendencies among primate species.

Grooming Circadian Rhythmicity, Progesterone Levels and Partner Preference of the Reproductive Pair of a Captive Common Marmoset (Callithrix jacchus) Family Group during Pregnancy and after Parturition

One family group of common marmosets (Callithrix jacchus) maintained in captivity under natural environmental conditions (Natal, Brazil, 05°46'S, 35°12'W) was observed by focal sampling at two non-consecutive days per week during two non-consecutive pregnancies (pregnancy 1: the last 8 fortnights before parturition; pregnancy 2: the last 5 ones) and after parturition (4 fortnights for both). The hourly percentiles of the duration of self-grooming and allogrooming interactions of the reproductive pair were submitted to Cosinor analysis for the 24-h period (p ≤ 0.05). The reproductive female's progesterone was monitored by fecal collection twice a week between 7:00 h to 9:00 h. Levels of progesterone were determined by ELISA method. During pregnancy 1, all interactions of the reproductive pair showed a 24-h statistically significant period. However, after parturition this periodicity is not present in some behaviors of the reproductive male. This animal presents the 24-h periodicity only toward to the reproductive female, the subadult son and to the newborns. Hormonal levels of the reproductive female showed isolated increases above 100 ng/g at the second and third fortnight after parturition, but did not characterize ovulation. Between pregnancy 1 and 2, the family was increased by the birth of four animals. During pregnancy 2, a statistically significant 24-h period was find only in self-grooming of the reproductive male and female, and in the interactions between the reproductive pair. Also, in the interactions of the reproductive male with only one of the juvenile son. After parturition the reproductive female ovulated at the second fortnight and became pregnant again. At this time, those interactions still have a 24-h period, except in grooming directed to the juvenile son by the reproductive male. As in the first post-partum, grooming directed to the newborns showed statistically significant 24-h period. These results suggest that the reproductive pair performs 24-h rhythmic grooming interactions only with some animals, supposed to be the preferential grooming partners. Furthermore, the temporal grooming expression in common marmosets may be affected by the reproductive condition (progesterone levels) of the reproductive female, by the care of newborn after parturition and the group size.

Vocalization before grooming interactions in Japanese macaques

Japanese macaques, Macaca fuscata, often utter girneys and 'short low' coos when they begin grooming interactions. In a captive group of Japanese macaques, instances of grooming of others by females were compared to cases in which they received grooming with regard to kinship and dominance relations. For unrelated females, dominant females vocalized more frequently when they received grooming than when they groomed subordinates. In contrast, subordinate females vocalized more frequently when they groomed a dominant female than when they received grooming. However, even when each case was examined individually, grooming was not consistently preceded by vocalizations. Generally, females uttered these vocalizations more frequently to unrelated females than to related females. On the other hand, solicitation of unrelated dominant females was infrequent. These results suggest that grooming partners and roles in grooming do not always determine the pattern of vocalization; instead, female monkeys may utter these vocalizations to reduce tension.