Grooming in Barbary macaques: better to give than to receive?

It is well established that grooming underpins sociality in group-living primates, and a number of studies have documented the stress-reducing effects of being groomed. In this study, we quantified grooming behaviour and physiological stress (assessed by faecal glucocorticoid analysis) in free-ranging Barbary macaques, Macaca sylvanus. Our results indicate that it is the giving rather than the receiving of grooming that is associated with lower stress levels. These findings shed important new light on the benefits of this key behaviour in primate social life.     

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.     

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.     

Female ovarian cycle phase affects the timing of male sexual activity in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar

Although all macaques have a multimale multifemale mating system, the degree of promiscuity shown by the Barbary macaque is considered to be extreme in terms of both mating frequency and number of mating partners. How mating activity is distributed throughout the female menstrual cycle and whether or not copulations are concentrated around the fertile phase as in other members of the genus is, however, not known. To examine this, we collected data on rates of copulation throughout 29 ovarian cycles from 13 free-ranging females of the Gibraltar Barbary macaque population and related them to the time of ovulation and the female fertile phase as determined from fecal hormone analysis. In addition, patterns of male inspection of females and time spent in consortship, both indicators of female attractivity, were also analyzed. The results indicate that both mating behavior and female attractivity vary predictably with ovarian cycle stage. Rates of copulation were found to increase toward the time of ovulation, with a distinct peak of ejaculatory (but not non-ejaculatory) copulations occurring in the fertile phase. Additionally, we show that frequency of inspection of females by males and time spent in consortship were also highest during the fertile phase and that ejaculatory copulations and male pericopulatory behaviors were significantly correlated with levels of female sex hormones. Our findings indicate that the Barbary macaque shows a mating pattern during the cycle similar to that described for other members of the genus. More importantly, however, our study provides clear evidence that despite an extreme degree of promiscuity Barbary macaque males concentrate their reproductive effort to the fertile phase, implying that they are able to discern this period and that thus timing of ovulation is not concealed from them. Estrogen-related cues appear to be involved in the process of recognition of female reproductive status by males, but the exact nature of these cues and how male Barbary macaques use them remains to be clarified.     

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.     

Play behavior in immature moor macaques (Macaca maura) and Japanese macaques (Macaca fuscata)

Play is widespread across mammalian taxa, but species strongly vary in the ways they play. In less despotic primate species (i.e., with less steep dominance hierarchies, less severe conflicts, and more reconciliation), play has been described as being more frequent, cooperative, and freely expressed. To study the link between social play and dominance style, we compared play behavior in free-ranging infants, juveniles and subadults of more despotic Japanese macaques (Macaca fuscata, N = 24) and less despotic moor macaques (Macaca maura, N = 17). We found interspecific differences in play behavior that corresponded with the contrasting dominance styles of the study species, largely confirming our predictions. In particular, moor macaques spent a larger proportion of time in solitary and social play than Japanese macaques, while Japanese macaques spent a larger proportion of time in grooming interactions. In moor macaques, play sessions included more players, a larger variety of play behaviors, greater play face rates, a greater proportion of time in contact play, and a higher rate of reciprocal play-biting than in Japanese macaques. Aggressive escalations were not common, but more frequent in Japanese macaques. Finally, a higher frequency of play faces during play sessions predicted the occurrence of more reciprocal play-bites, but not the proportion of time spent in contact play behaviors. Additional studies on other groups and species will allow a better understanding of the link between dominance style and social play.     

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.     

Whom to Groom and for What? Patterns of Grooming in Female Barbary Macaques (Macaca sylvanus)

Grooming is one of the most conspicuous social interactions among nonhuman primates. The selection of grooming partners can provide important clues about factors relevant for the distribution of grooming within a social group. We analyzed grooming behavior among 17 semi-free ranging female Barbary macaques (Macaca sylvanus). We tested whether grooming is related to kinship, rank and friendship. Furthermore, we tested whether grooming is reciprocated or exchanged for rank related benefits (i.e. lower aggression and increased tolerance whilst feeding). We found that in general grooming was reciprocally exchanged, directed up the hierarchy and at the same time affected by friendship and kinship. Grooming was more frequent among individuals with higher friendship values as well as amongst related individuals. We also divided our data set on the basis of rank difference and tested if different power asymmetries between individuals affected the tendency to exchange grooming for rank related benefits and grooming reciprocation. In support of our initial hypothesis our results show that the reciprocation of grooming was a significant predictor of grooming interactions between individuals of similar rank, but not between those individuals more distantly separated in the social hierarchy. However, we did not find any evidence for grooming being exchanged for rank related benefits in either data set. Our results, together with previously published studies, illustrate the behavioral flexibility of macaques. It is clear that multiple studies of the same species are necessary to gather the data required for the solid comparative studies needed to shed light on patterns of grooming behavior in primates.     

三种笼养灵长类活动时间分配的比较研究

采用焦点动物法和连续记录法对3种笼养灵长类活动时间分配进行比较研究。结果表明,川金丝猴Rhi-nopithecus roxellanae和熊猴Macaca assamensis用于休息的时间多于猕猴Macaca mulatta,移动时间则相反;川金丝猴和猕猴用于理毛的时间多于熊猴。不同性别年龄组之间的活动时间分配有差异,主要表现在川金丝猴母亲用于理毛的时间明显多于成年儿子,用于玩耍的时间则相反;猕猴成年雄性的移动时间和理毛时间多于成年雌性,玩耍时间则少于成年雌性;熊猴成年雌性的移动时间多于成年雄性,与成年个体相比,幼体花更多的时间用于玩耍,而相应的减少了其休息时间。     

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.     

Sex differences in vocal communication among adult rhesus macaques

In female-bonded primate species, females invest more time in grooming than males, and the majority of this grooming occurs in intra- rather than intersexual interactions. These clear sex differences in sociability reflect females' need to forge and maintain complex networks of social relationships with other females in the group. Increasing evidence indicates that vocal signals can have a similar function to grooming in mediating social interactions and relationships, and sex differences in patterns of use of vocal communication comparable to those seen for grooming might therefore be expected to occur. In this study of free-ranging adult rhesus macaques, we tested for such patterns, focusing on the frequency of utterance of three types of vocalisations given during close-range social interactions: coos, grunts, and girneys. As predicted, we found that females gave such calls significantly more frequently than males and also directed more of these vocalisations towards other females than to males; males' rate of vocalising towards the two sexes was not significantly different. To our knowledge, these results provide the first evidence for a sex difference in the rate of production of social vocalisations among adult nonhuman primates. The finding that increased sociability is associated with increased reliance on vocal communication may have important implications for theories of language evolution.     

Activities and feeding behavior of free-ranging pregnant baboons

The activities and feeding behavior of pregnant baboons, Papio cynocephalus,were studied in two free-ranging groups in Amboseli National Park, Kenya. Both the environmental conditions and the age of their fetuses influenced females’ activity budgets and feeding behavior. Females fed more and rested less during the dry season than during the wet season, and most females spent progressively more time feeding and less time grooming than expected (based upon the amount of recent rainfall) as their fetuses matured. During the wet season, females also devoted significantly greater proportions of feeding time to consumption of grass blades, leaves, and flowers and significantly smaller proportions of their feeding time to feeding upon seeds, corms, and fruit. As their fetuses became older, the proportion of time spent feeding upon seeds increased, and the proportion of time spent feeding upon grass blades and fruit declined.     

Differences in Activity Budgets and Diet Between Semiprovisioned and Wild‐Feeding Groups of the Endangered Barbary Macaque (Macaca sylvanus) in the Central High Atlas Mountains,Morocco

The Barbary macaque, Macaca sylvanus is a very adaptable primate species occupying a wide range of habitats in Morocco and Algeria. Several groups of this endangered macaque can be found in tourist sites, where they are affected by the presence of visitors providing food to them. We compare the activity budgets and the diet of semiprovisioned and wild‐feeding groups of Barbary macaques in the central High Atlas Mountains of Morocco from February to August 2008. We used instantaneous scan sampling at 15‐min intervals. The behaviors included in the activity budget were feeding, moving, foraging, resting, and aggressive display. Food items were grouped into seven categories. We found no differences between the two groups in the daily percentages of records attributed to feeding. The semiprovisioned group spent significantly more time engaged in resting and aggressive behavior, and foraged and moved significantly less than the wild‐feeding group. There was no significant difference between the two groups in time spent eating leaves, fruits, or roots and bark. The semiprovisioned group, however, spent significantly less time per day feeding on herbs, seeds, and acorns than the wild‐feeding group. Human food accounted for 26% of the daily feeding records for the semiprovisioned group and 1% for the wild‐feeding group. Our findings agree with previous studies and indicate that in the tourist site, where food is highly clumped, macaques decreased foraging time yet showed higher levels of contest competition. Our results support the common claim that the diet of the Barbary macaque is highly flexible, differing among its varied habitats. Conservation efforts for the Barbary macaques should take into account the changes in behavior that human‐modified environments may cause.     

The Effect of Climatic Factors on the Activity Budgets of Barbary Macaques (Macaca sylvanus)

Climatic conditions can significantly affect the behavior of animals and constrain their activity or geographic distribution. Barbary macaques (Macaca sylvanus) are one of the few primates that live outside the tropics. Here we analyze if and how the activity budgets of Barbary macaques are affected by climatic variables, i.e., air temperature, relative humidity, rainfall, and snow coverage. We collected scan sampling data on the activity budgets of four groups of macaques living in the Middle Atlas Mountains of Morocco from June 2008 to January 2011. This habitat is characterized by extreme seasonal changes, from cold and snowy winters to hot and dry summers. The activity budgets of the macaques differed across months but not across the time of day (with the exception of time spent feeding). The monkeys spent significantly more time feeding or foraging when there was no snow than when snow coverage was moderate or major. Daily rainfall was positively related to resting time and negatively to time spent moving or in social behavior. Air temperature was negatively related to time spent feeding or foraging. Finally, time spent on social behavior was significantly lower when relative humidity was high. These data indicate that environmental factors significantly affect the time budgets of endangered Barbary macaques, a species that has been little studied in the wild. Our findings support previous studies on temperate primates in showing that snow coverage can have negative consequences on the feeding ecology and survival of these species.     

环境和社会因素对喀斯特石山猕猴日活动节律和活动时间分配的影响

2007年9月至2008年8月,以广西弄岗国家级自然保护区内的一大群野生猕猴为研究对象进行连续的跟踪观察,采用瞬时扫描取样法收集其食物组成、活动节律和活动时间分配的数据,旨在探讨影响石山猕猴活动节律及活动时间分配的环境和社会因素。结果表明：研究猴群的日活动节律表现为上午和下午的觅食高峰以及中午的休息高峰,这与白天温度和日照强度的变化有关。日活动时间分配中,休息42.1%,移动34.5%,觅食15.1%,玩耍2.0%,理毛5.2%,其他行为1.3%。猴群依据食物的变化调整活动时间分配,其中用于移动的时间与食物中果实的比例成显著的正相关性。不同性别年龄组个体的活动时间分配表现出显著差异,主要表现为成年雄性花费更多的时间休息,而成年雌性花费更多的时间觅食和社会性理毛,未成年个体则花费更多的时间玩耍。与同域分布的小群猕猴相比,本研究群花费更多的时间休息,较少的时间觅食。这些差异可能与盗食农作物有关。     

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.     

Rank relations among sisters in semi-free-ranging Barbary macaques (Macaca sylvanus)

Although semi-free-ranging Barbary macaque females are able to outrank older females from lower-ranking matrilines (matrilineal rank acquisition), they do not systematically outrank their older sisters, as is known to be the case for semi-free-ranging rhesus monkeys (Macaca mulatta) and Japanese macaques (Macaca fuscata). We test the hypothesis that differences in the support received by younger sisters against their older sisters and against older lower-ranking females might account for this interspecific difference. Thirty-one sister dyads, members of a group of 109 Barbary macaques living at La Montagne des Singes, France, were observed during 16 months. The results indicate that (1) all females were dominant to their younger sisters, and the latter were never observed to challenge their older sisters; (2) younger sisters received as much kin support against their older sisters as against older lower-ranking females; (3) only very young females received support from their kin against their older sisters; (4) younger sisters received much more support from nonkin females against lower-ranking females than against their older sisters; and (5) Barbary macaque females appear to be supported against their older sisters less frequently than rhesus macaque females are. We conclude that the lack of nonkin support is the main factor accounting for the failure of younger sisters to outrank their older sisters in Barbary macaques. Initially this might result from kin support not being sufficient to induce younger sisters to challenge and to solicit support against their older sisters.     

First occurrence of twins in provisioned free-ranging Tibetan macaques (Macaca thibetana) at Huangshan, China

A first case of newborn Tibetan macaque (Macaca thibetana) twins was observed in a free-ranging group at Huangshan, China. The female that gave birth to the twins was studied during their first 5 months post-partum, and her activity budget was compared to those of adult females with single or no offspring in order to assess her behavioral changes. Our report shows that female Tibetan macaques can produce twins, and that twins can successfully survive. The adult female with twins spent more time foraging and resting, but less time moving and engaged in other social behaviors than adult females with a single infant or no infant. Our report provides a case of successfully surviving twins in a wild environment and suggests that the mother modified her behavior patterns to adapt to the heavy burden. We conclude that both food provisioning and the mother’s behavioral strategies facilitated the survivorship of twins. This expands our understanding of the reproductive biology of Tibetan macaques.     

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.     

Maternal Infant Monitoring in a Free-ranging Group of Japanese Macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

In nonhuman primates, females with infants visually monitor their infants from a distance to detect and consequently avoid potential threats to their infants. We recorded maternal visual monitoring of infants (infant monitoring) ages 7–18 wk in a free-ranging, provisioned group of Japanese macaques (Macaca fuscata). The infant monitoring rate declined as a function of infants’ ages in weeks and increased when the infants were beyond their mother’s reach, indicating that infant monitoring reflects the vulnerability of infants. Females with infants increased infant monitoring when their infants were handled by other group members but not when their infants moved alone. This suggests that intragroup threats (harassment/mishandling or kidnapping) have a relatively stronger influence on infant monitoring than external threats (predation or infanticide) under the condition of this study. Infant monitoring of middle-/low-ranking females was more frequent than that of high-ranking females when their infants were handled by other individuals. This may reflect greater intragroup threats to infants of middle-/low-ranking females; however, further study is needed to confirm this. During important activities (feeding or grooming), the infant monitoring rate was lower than that during other activities (resting or self-directed behavior). However, even during important activities, females with infants increased infant monitoring when infants were handled. This indicates that females with infants face a trade-off between infant monitoring and other important activities, and even if females have to reduce the time spent on important activities, they increase infant monitoring when their infants face greater potential intragroup threats.