Does allogrooming serve a hygienic function in Cercocebus torquatus lunulatus?

To test the hygienic functional hypothesis of allogrooming in the white-crowned mangabey (Cercocebus torquatus lunulatus), we analyzed the distribution of such behavior over the body surface in the individuals of two captive groups of this species (N = 9 and N = 8). To sample the data, we used focal animal sampling and continuous recording. Before analyzing the data, we measured a representative subject in order to calculate the body surface area occupied by each site, defined accessibility rigorously (distinguishing among three categories of sites: easy to reach, difficult to reach, and inaccessible), and tested empirically the classification proposed. To determine whether allogrooming was likely to concentrate on the body sites with accessibility problems, we ran three successive analyses, each of with was increasingly specific: grouping types of sites, analyzing each site separately, and analyzing each subject's reception profile. The results obtained show that in both groups inaccessible sites received more allogrooming than predicted by their actual surface area; sites that were difficult to reach received an amount of allogrooming proportional to the body surface area they occupied, and those easy to reach received less allogrooming than expected. This complementarity between the distribution of auto- and allogrooming is consistent with the hygienic functional hypothesis of allogrooming. However, not all inaccessible sides nor those difficult-to-reach were allogroomed equally: Allogrooming concentrated primarily on dorsal and caudal regions, whose care is incompatible with a ventral/ventral orientation between groomer and groomee. The strong distributional selectivity of allogrooming and the interindividual variability in preferred allogrooming sites suggest that the hygienic functional hypothesis cannot fully account for all the aspects of the corporal distribution of such behavior. Thus, in support of the multifunctional nature of allogrooming, we conclude that there must be more than cleaning involved in Cercocebus torquatus lunulatus' allogrooming.     

Grooming site preferences in wild white-handed gibbons (Hylobates lar)

During a four-month study of wild white-handed gibbons in Thailand one group was observed for 131 hr. The individuals spent 5.2% of their activity period allogrooming. Several body sites received more respectively less allogrooming than expected. Surface areas easy to clean by autogrooming such as the belly received significantly less allogrooming than expected. Upper body areas which are likely to be infested by parasites and other matter received significantly more allogrooming than lower body parts. Thus, grooming in gibbons seems to reflect a primarily hygienic function.     

Grooming site preferences in female langurs (Presbytis entellus)

Factors influencing grooming site preferences in adult female Hanuman langurs (Presbytis entellus) were investigated. The females belonged to a free-ranging harem troop (Jodhpur, India) and were observed for 569 hr by focal-female sampling. Decisive factors for grooming site preferences were the following: autogrooming was determined mostly by site accessiblity. Allogrooming was significantly concentrated on parts that are inaccessible to the groomee. Close female kin groomed significantly longer, more frequently, and more precisely at inaccessible body parts. Lower-ranking females were groomed significantly less often and more briefly but also more precisely at inaccessible parts. However, the latter might be due to a lower-ranking subjects desire to face away from the higher-ranking groomer in order to avoid eye contact. The data suggest that the groomee determines the sites being groomed.     

Functional Implications of Allogrooming in Cercocebus torquatus

We examined the hygienic functional hypothesis of allogrooming in two captive groups (N = 9 and N = 8) of white-crowned mangabeys (Cercocebus torquatus lunulatus) by analyzing the corporeal distribution of allogrooming solicitations according to the variable degree of accessibility of the various body sites. We used focal-animal sampling and continuous recording and nonparametric statistics (sing test and ²). The fact that in both groups more allogrooming was solicited to sites associated with accessibility problems is consistent with the hygienic functional hypothesis of allogrooming. In any case, there are two facts that suggest that this hypothesis cannot account for all the characteristics of such behavior: 1) the strong distributional selectivity shown by allogrooming solicitations—they concentrated primarily on dorsal and caudal regions instead of those difficult to reach or inaccessible on the whole—and 2) the significant role played by sex in the intragroup distribution of anogenital solicitations. Supporting the multifunctional nature of allogrooming, we find very appealing the ritualization hypothesis, according to which the allogrooming performed on certain body sites would have acquired a sociocommunicative meaning.     

Experimental analysis of causal relationships between grooming behavior and inter-individual proximity in the stumptailed macaque (Macaca arctoides): a preliminary report

Some causal relationships between allogrooming, autogrooming, locomotion and close proximity in the behavior of one (adult female) Macaca arctoides while in the presence of another (adult male) monkey of the same species are reported. Allogrooming reduces the probability of walking away in the groomer, and thus increases the time spent close to the other monkey; autogrooming seems to have a similar effect. The duration of autogrooming is increased in a non-proportional manner by reduction of locomotion, but the duration of autogrooming seems to directly reduce the amount of locomotion. Up to a certain optimal value, the duration of autogrooming increases accordingly as the time spent close to the other monkey increases. The duration of allogrooming may be influenced in the same way as the duration of autogrooming.     

Allogrooming Behavior and Grooming Site Preferences in Captive Bonobos (Pan paniscus): Association with Female Dominance

I tested the utility of Seyfarth's (1977) model of rank-related attractiveness to explain the distribution of allogrooming behavior among captive bonobos (Pan paniscus). Adult female bonobos generally have high social status and may be dominant over males. As predicted by the model, I found that high-ranking adult females received most allogrooming within each of the four investigated groups. Among adult female-adult female dyads, however, allogrooming was not clearly associated with dominance rank. Contradictory to predictions of the model, the highest-ranking females were responsible for most displacements over allogrooming, and grooming competition is positively correlated with dominance rank. In the second part of this study, I investigated the social significance of allogrooming body site preferences. Bonobos direct significantly most allogrooming to the face of conspecifics, and high- and low-ranking individuals, as well as males and females, differ significantly in their preferences for certain allogrooming sites. Subordinates and males tended to avoid facial grooming and preferred the back and anogenital region, while high-ranking individuals and females directed most allogrooming to the face and head of grooming partners. Data from this study support the hypothesis that high-ranking females are the most attractive grooming partners within a female-centered bonobo society. Many other aspects of allogrooming behavior, however, are not consistent with the model of rank-related attractiveness.     

Scratching,dominance, tension,and displacement in male baboons

This paper reports a study designed to test the hypothesis that a relationship exists among dominance rank, tension, and scratch behaviors in anubis baboons (Papio cynocephalus anubis). Our study was conducted on two groups of male baboons, each containing eight unrelated individuals who were approximately 6 years of age and who shared common rearing histories. Focal animal sampling was used to collect behavioral data. Hand scratching, foot scratching, avoid, tension, allogrooming, autogrooming, and manipulation were measured as acts performed per hour of sampling. Dominance matrices were constructed based on net difference of avoid behavior performed and received (adjusted for time sampled). Individual status ranks were grouped into two status classes, high and low. Analysis of variance models demonstrated significant differences in the performance rate of scratching behaviors by dominance rank class, as well as differences in scratching performance by tension class. Individuals in the high status class had significantly higher rates of total scratching, hand scratching, foot scratching, and tension behavior performance than their counterparts in the low status class. No significant difference was found between status classes or tension classes for performance rate of allogrooming, autogrooming, or manipulation behavior. The frequency of scratching and general level of activity were not significantly correlated. The results are interpreted to indicate the possibility that scratching may function as a displacement behavior, which subjectively appears to communicate heightened frustration, anxiety, or arousal.     

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

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

Social interactions among wild female Bechstein's bats (<Emphasis Type="Italic">Myotis bechsteinii</Emphasis>) living in a maternity colony

Although sociality is common in bats, few studies have investigated individual social behaviour in free-ranging colonies. This study quantifies social interactions among wild female Bechstein's bats (Myotis bechsteinii) belonging to one maternity colony. Our main goal was to analyse allogrooming and nose rubbing, which are both regularly displayed by adult females. Based on data of individually marked bats with known degrees of pairwise relatedness, we suggest that allogrooming has both a social and a hygienic function. Females groomed colony mates mainly on parts of the body that are difficult to reach by a bat itself. Thus, allogrooming may function to remove ectoparasites from inaccessible body parts. Allogrooming was rare compared to self-grooming (on average 0.7% vs 37.7% of a female's total observation time), and there was no significant correlation between the rate at which a bat groomed itself and the frequency with which it was groomed by conspecifics. Therefore, we assume that allogrooming also has a social purpose in addition to its assumed hygienic function. We suggest that allogrooming could strengthen social bonds among colony members that live together for many years. Mothers and adult daughters groomed each other preferentially. Thus, allogrooming may reflect special mother–daughter bonds. Nose rubbing occurred mainly within minutes (median: 80 s) after the arrival of a female in a night roost, and there was no correlation with relatedness. Therefore, it probably allows recognition of colony mates and may also be a greeting behaviour. Communicated by M.E. dos Santos     

Allogrooming behavior inCercocebus torquatus: The case for the hygienic functional hypothesis

The hygienic functional hypothesis of allogrooming behavior was examined in two captive groups (N=9 andN=8) of white-crowned mangabeys (Cercocebus torquatus lunulatus) by analyzing: (1) the corporal distribution of manipulation type according to hair density, and (2) the corporal distribution of allogrooming according to presence of wounds. In both groups the sites with higher hair density received more bouts of Superficial Grooming, which implies a tactile screening of a fragment of the body surface. Only one group tended to emit more allogrooming on the body sites when they were wounded. In the other group, however, the number of wounds was very small and the wounds concentrated predominantly on those sites which were accessible to the subject itself. Thus, our results may be consistent with the hygienic functional hypothesis of allogrooming behavior in general and with the sanitary one in particular.     

笼养川金丝猴理毛行为功能

<正>理毛行为(Grooming behavior)的定义是动物个体对自身或其同类个体体表(皮肤、毛发或羽毛等)进行的多种形式护理,包括对体表进行有规律的梳理,以及用舌头或嘴唇舔皮肤和毛发等(Veà et al., 1999)。在灵长类动物中,理毛行为大多表现为个体接触和探查自身或另一个体体表被毛,将毛发分开后从中拣出盐粒或皮肤寄生物放入口中咀嚼或直接用嘴咬食被毛下的盐粒或皮肤寄生物(李银华和李保国, 2002)。依据理毛接收对象的不同,可将     

Effects of Relatedness,Dominance, Age,and Association on Reciprocal Allogrooming by Captive Impala

Wild impala display a highly reciprocal allogrooming system that, by virtue of its frequency and high degree of reciprocity, is unique among ungulates. A herd of 35 free-ranging captive impala provided opportunity to examine the degree of reciprocity of allogrooming exchanges and the influence of relatedness, dominance, age and association on partner preferences and distribution of grooming between allogrooming partners. As in wild impala, the exchange of allogrooming bouts in the captive impala was highly reciprocal regardless of partners. Kinship and dominance had no influence on partner preference or distribution of grooming between partners. Although mothers showed a significant preference to allogroom with their unweaned offspring, this preference practically disappeared with older offspring. Age-mates (no greater than 6 mo apart) tended to associate with one another and spatial proximity was positively correlated with grooming partner preference. It was not clear whether impala actively sought out age-mates for grooming, or randomly chose grooming partners from nearby age-mates. The failure to find a role for kinship and dominance is counter to what has generally been found in most Old World terrestrial primate studies. The absence of pronounced social influences, coupled with the known effectiveness of grooming in removing ectoparasites, suggest that a utilitarian role, especially removal of ticks, is an important function of the impala reciprocal allogrooming system.     

灵长类相互理毛的影响因素、功能及其利益分析

理毛行为是动物行为学研究的主要内容之一,根据理毛的对象可分为自我理毛(Autogrooming)和相互理毛(Allogrooming),其中相互理毛是灵长类重要的社会行为。现在认为相互理毛可能与社会参量(亲缘关系、性别、年龄、等级制度、繁殖状况等)有联系,并且有一定的社会功能。本文论述了理毛行为的分类、影响相互理毛的因素、相互理毛功能假说及其相互理毛的投入-收益分析,以便人们对相互理毛的行为进行更深入的研究。     

Reciprocal Allogrooming in Wild Impala Lambs

Adult impala engage in a form of reciprocal allogrooming distinguished by a high degree of reciprocity and ***lack of influence of dominance or relatedness on partner preference or distribution of grooming between partners. A previous study on reciprocal allogrooming of captive newborn impala lambs in a zoological park found that the allogrooming emerged as early as the first week after birth and was identical in structure and reciprocity to allogrooming in adults. Because these findings of apparently unique allogrooming behavior of newborn impala could have been a reflection of the effects of being born and raised in a small, stable captive herd, it was necessary to investigate reciprocal allogrooming in newborn impala in the wild. The emergence, reciprocity, rate, and partner distribution of reciprocal allogrooming in wild newborn impala were observed at two study sites: a national park in Zimbabwe and a game farm in South Africa. Maternal one-way grooming between mother and newborn emerged as distinct from reciprocal allogrooming and rapidly declined after week 1 postpartum. Reciprocal allogrooming by lambs was first seen between 5 and 8 d postpartum, and as soon as the behavior occurred it was the same basic pattern as seen in adult impala. The reciprocity index for lambs was near 0.5, indicating that lambs delivered as much grooming during an encounter as the partner. Lambs were grooming frequently with non-mother adults and other lambs by week 1 or 2; by week 3 and onward the allogrooming rate of lambs was more than twice that of their mothers, as predicted by the body size principle of the programmed grooming model. The strong predisposition of neonatal impala lambs to deliver reciprocal allogrooming as early as the first or second week postpartum would appear to reflect a genetically acquired adaptation to the threat of tick infestation in their natural habitat.     

The first weeks of cohabitation of newly-formed heterosexual pairs of common marmosets (Callithrix jacchus)

16 pairs of common marmosets were formed, six of which were observed for 7 weeks, and ten for 4 weeks. A variety of behaviours was recorded, including sexual mounting, male tongue-smacking, female slit-eyed tongue-flicking, scent marks, huddling, allogrooming and autogrooming. Behaviours associated with sexual encounters occurred initially at high levels but declined during the study period. The incidence of sexual mounting was closely related to that of male tongue-smacking and female slit-eyed tongue-flicking. Other social behaviours including scent-marking and allogrooming did not show a consistent pattern of occurrence with respect to time or sexual activity.     

Relation of Intergroup Variation in Allogrooming to Group Social Structure and Ectoparasite Loads in Red Howlers (Alouatta seniculus)

We compare the allogrooming behavior of 5 troops (average size = 8.2) of red howlers (Alouatta seniculus) from the Venezuelan Llanos with that of other A. seniculus and Alouatta spp. of the genus. In 126.9 observation hr, we recorded 118 allogrooming events, with an average bout length of 109 sec. Females groomed more frequently than males did, but as groomees there is no significant differences between sexes. Adult males groomed adult females mostly in a sexual context (before copulation). Allogrooming rates differ significantly among groups. There are also significant differences among members of the same troop both as groomers and groomees, which we explain in the context of the social behavior and history of each troop. There is no significant correlation between weight of the groomee and duration of the grooming bout. However, the examination of grooming rates and ectoparasite load suggests that allogrooming may have hygienic consequences. Differences in allogrooming rates among species of Alouatta are related to differences in group kin structure and patterns of female competition, in particular, coalition formation. We conclude that the social structure and the degree of relatedness among individuals within a group (or among individuals in a population in interpopulation comparisons) is a more important determinant of allogrooming rate than body size or group size. Our results emphasize the importance of considering intergroup and interpopulational variation in behavior.     

The influence of sex and relatedness on stress response in common marmosets (Callithrix jacchus)

Research in stress physiology has demonstrated the benefits of receiving social support during stressful conditions. However, recent data have shown that the efficacy of social support in buffering physiological and behavioral responses to stressor agents depends on species, sex, and relatedness among animals. This study investigated whether different kinds of social support (presence of same sex related or nonrelated conspecifics) have the same effect on hormonal (fecal cortisol levels) and behavioral responses (agonistic: scent-marking and individual piloerection; anxiety: locomotion; tension-reducing: autogrooming, allogrooming, and body contact). We used adult male and female isosexual dyads of Callithrix jacchus, a small Neotropical primate from the Callitrichidae family, widely used in the study of stress and related diseases. Following a 28-day baseline phase, dyads faced three challenging situations (phase 1: dyads were moved together from the baseline cage to a similar new cage; phase 2: each dyad member was moved alone to a new cage; and phase 3: dyad members were reunited in the same baseline cage). Type of social support was found to influence the response to stressors differently for each sex. Related male dyads did not change their hormonal or behavioral profile over the three experimental phases, when compared to the baseline phase. For nonrelated male dyads, social support buffered hormonal but not behavioral response. For females, the social support offered by a related and nonrelated animal, does not seem to buffer the stress response, as shown by correlations between agonistic behaviors versus cortisol and locomotion during all three experimental phases and a significant increase in fecal cortisol levels during phases 2 and 3, when compared with baseline levels. The results only partially support the buffering model theory and corroborate other studies reporting that the benefits of social support during a period of crisis arise only when it is adaptive for that species.     

Correlates of Self-Directed Behaviour in Wild White-Faced Capuchins

Elevated rates of self‐directed behaviour (SDB) such as self‐scratching and autogrooming have been widely used in recent years as an indicator of anxiety in catarrhine primates. This study presents the first examination of correlates of SDB rates in a platyrrhine primate. Subjects were 8 wild female white‐faced capuchins at Lomas Barbudal, Costa Rica, who were observed for 119 h of focal individual follows. The subjects performed significantly more self‐scratching and autogrooming while in close proximity to conspecifics than while alone, irrespective of whether the neighbour was dominant or subordinate to them. This result was attributable to elevated SDB rates during the 30 s preceding and following allogrooming bouts. Furthermore, subjects engaged in more SDB while in proximity to females (a) that were closer to them in dominance rank and (b) with whom they spent a larger proportion of their time in proximity. Self‐directed behaviour rates after conflicts did not differ from non‐postconflict rates. Nor were SDB rates above baseline levels during the 30 s before subjects descended to the ground. These results may provide support for the view that SDB rates index anxiety in this species, if grooming decisions signal individuals' current allegiances and are therefore a source of anxiety, even if being groomed is, itself, relaxing. Postconflict preparation for further aggression may mitigate against scratching and autogrooming in a fast‐moving arboreal species.     

Allogrooming as a tension-reduction mechanism: A behavioral approach

The hypothesis that allogrooming functions as a tension-reduction mechanism was tested. Tension was measured by the frequency of displacement activities by an animal. Two adult male and 11 adult female Java (or long-tailed) monkeys (Macaca fascicularis) that were relatively unfamiliar with each other were paired 1 hour per day for five consecutive days during the periovulatory portion of the menstrual cycle. Female allogrooming was found to reduce the frequency of male displacement activities both during the course of interaction and outside it, and this decrease was proportional to the amount of allogrooming received. Female allogrooming did not, however, exert long-lasting effects on the frequency of female displacement activities. An increase in the frequency of male displacement activities was recorded during the 10-second interval immediately after the end of the female allogrooming bouts. Neither postinhibitory rebound nor frustration owing to the cessation of a pleasant situation, i.e., the two advanced explanatory hypotheses, accounted for this increase. The results of the present study concur with physiological findings that support the tension-reduction hypothesis. The social function of allogrooming appears quite important and is entirely compatible with the functional hypothesis that emphasizes hygiene.     

Differential effects of ambient temperature and humidity on allogrooming, self-grooming, and scratching in wild Japanese macaques

This study presents data on the effects of variations in ambient temperature and humidity on behaviors related to the care of the pelage (allogrooming, self-grooming, and scratching) in wild Japanese macaques (Macaca fuscata yakui). The amount of time monkeys spent allogrooming was essentially unaffected by variations in ambient temperature and relative humidity. Frequency of scratching and, to a lesser extent, time spent self-grooming significantly increased when ambient temperature and/or relative humidity increased. These results are interpreted in relation to the differences in ultimate function that exist between allogrooming (with both hygienic and social functions) and self-grooming and scratching (with a solely hygienic function).