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 patterns in Verreaux's sifaka

Lemur grooming has received very little attention in the literature. Nevertheless, allogrooming in lemurs has been suggested to be fundamentally different from the grooming of anthropoids. One reason is that lemurs generally rely on oral rather than manual grooming. Lemur allogrooming has also been suggested to serve less of a social function than has been attributed to anthropoid grooming. I analyzed the allogrooming behaviors of 29 Verreaux's sifaka (Propithecus verreauxi) living in five social groups in the Kirindy Forest of Madagascar. Based upon 1,586 observation hours, I found that sifaka, like anthropoids, spend very little time mutual grooming (2±3%). Half of all allogrooming involved parts of the body that could have been easily groomed by the recipient, such as the limbs. Even though ectoparasite loads are expected to be greater during the rainy season, allogrooming did not increase during the rainy season. Allogrooming rates were influenced by both rank and sex, and increased by 50–100% during the mating season. The results of this study suggest that allogrooming in Verreaux's sifaka plays an important social function, even though it is performed with a toothcomb. Am. J. Primatol. 72:254–261, 2010. © 2009 Wiley‐Liss, Inc.     

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.     

Group harmony in gibbons: Comparison between white-handed gibbon (Hylobates lar) and siamang (H. syndactylus)

The siamang (Hylobates syndactylus) is exceptional among gibbons in that its area of distribution almost completely overlaps those of other gibbons, namely the white-handed gibbon (H. lar) and the agile gibbon (H. agilis) of the lar group. The siamang has almost twice the body weight of the gibbons of the lar group (ca. 11 kg vs. 5–6 kg), and it has been suggested that distinct ecological and behavioural differences exist between the siamang and its two sympatric species. The siamang has been claimed to differ from the white-handed gibbon “in the closer integration and greater harmony of group life” (Chivers, 1976, p. 132). However, few quantitative data exist to support this hypothesis. In the present study, intra-group interactions in captive family groups of white-handed gibbons and siamangs (two groups of each species) were recorded by focal-animal sampling. These data failed to show a consistent association between species and most of the behavioural patterns recorded, such as frequency of aggression, percentage of successful food transfer, frequency of social grooming bouts, and duration of social grooming/animal/hr. A significant difference was found for only two of the variables: Individual siamangs in this study showed longer grooming bout durations, and made fewer food transfer attempts than lar individuals. Only the first of these two differences is consistent with the hypothesis mentioned above, whereas the lower frequency of food transfer attempts in siamangs is the opposite of what should be expected under the hypothesis. On the other hand, two of these behavioural patterns showed a significant correlation with the parameters group size and individual age: Both individuals in larger groups and younger individuals tended to show shorter grooming bouts and a smaller proportion of successful food transfers. Our findings indicate that social cohesion within these gibbon groups may be much more flexible according to and depending on social or ecological influences and less rigidly linked to specific gibbon taxa than previously assumed. A considerably larger number of gibbon groups would have to be compared to provide reliable evidence for or against species-specific differences in group cohesion. Another finding of this study—a positive correlation between the frequency of aggression and grooming—is discussed in the light of the functional interpretations commonly attributed to allogrooming behaviour in primates.     

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.     

Allogrooming in two species of macaque (Macaca nemestrina andMacaca radiata)

This paper analyzes allogrooming (social grooming) data collected from two large, fully integrated and long established social groups of macaques (one of pigtail macaques and one of bonnet macaques). The data demonstrates a species and sex difference for total allogrooming given with females of both species giving more grooming than the males and with pigtails as a species giving more grooming than bonnets. Also, pigtail females gave more allogrooming to clan members than to nonclan members, but this was not true for pigtail males, bonnet males, and bonnet females. Allogrooming given and allogrooming received by age class for both species showed development of a sexual dichotomy at three to four years. The analysis characterized some of the social structures extant in two closely related species of macaque, particularly the somewhat different use of allogrooming in pigtail females as opposed to the other three categories of animals. Social implications with relation to macaque societies are discussed.     

Curvature of the forelimb bones of anthropoid primates: Overall allometric patterns and specializations in suspensory species

It has previously been reported that brachiating primates, particularly gibbons, are characterized by distinctively straight forelimb long bones, yet no hypotheses have been proposed to explain why straight limb bones may be adaptive to suspensory locomotion. This study explores quantitatively the curvature of the long bones in 13 species of anthropoid primates and analyzes the functional consequences of curvature in biomechanical terms. These analyses demonstrate that, whereas the humeri of gibbons and spider monkeys are functionally less curved than those of other taxa, the ulnae of brachiators are neither more nor less curved than those of other anthropoids, and the gibbon radius is far more curved than would be predicted from body size alone. The humerus is likely significantly less curved in brachiators because of its torsion-dominated loading regime and the greatly increased stress magnitude developed in torsionally loaded curved beams. The large curvature of the radius is localized in the region of attachment of the supinator muscle. Analysis presented here of muscle mass allometry in catarrhines demonstrates that gibbons are characterized by an extremely massive supinator, and the large radial curvature is therefore most likely due to forearm muscle mechanics. This study also demonstrates that the overall pattern of limb bone curvature for anthropoids is distinct from the pattern reported for mammals as a whole. This distinctive scaling relationship may be related to the increased length of the limb bones of primates in comparison to other mammals.     

Female Songs of the Nonduetting Javan Gibbons (<Emphasis Type="Italic">Hylobates moloch</Emphasis>) Function for Territorial Defense

Duets in territorial, pair-living primates may function to maintain intragroup cohesion, promote intergroup avoidance, and assist in territorial and resource defense, as well as advertising and reinforcing pair bonds. Despite the absence of duetting in Javan gibbons (Hylobates moloch), recent playback experiments suggested that Javan gibbon songs also play a role in pair-bond advertisement as well as territorial and mate defense. However, playback experiments only assess motivations of the listener, which may not reflect the motivations of the caller. We conducted an observational study of naturally occurring female songs in two groups of Javan gibbons from July 2009 to March 2010 and from March to November 2011 in Gunung Halimun–Salak National Park, Indonesia. We investigated female singing rates in relation to singing location, daily path length, occurrence of intergroup encounters, feeding rate, allogrooming rate, and distance between pair mates. The two females produced 47 songs during 164 observation days. Females in the area of their home range that overlapped with neighboring groups sang more frequently than expected based on time spent in the area of overlap vs. the home range interior. Groups also had longer daily path lengths on days when females sang than on nonsinging days, and on days when they visited the area of overlap than on nonvisiting days. Our findings indicate that, like the duets of other pair-living territorial primates, female Javan gibbon songs function for territorial defense, but we found no support for other functions such as intergroup avoidance, resource defense, and pair-bond reinforcement.     

Allogrooming, partner choice, and dominance in male anubis baboons

This study was designed to test the hypothesis that among unrelated male baboons (Papio cynocephalus anubis) in single-gender social groups there is no significant association between dominance status and allogrooming performance. The hypothesis was tested using behavioral measures obtained by focal animal sampling techniques. The results indicate that unrelated male baboons established well-defined linear dominance hierarchies, formed allogrooming relationships with one another, and exhibited a nonrandom distribution of allogrooming; however, there were no significant relationships between dominance rank and the frequency of allogrooming. We further tested our results by grouping individuals into three dominance status classes (high, middle, and low) and comparing the classes. Analysis of variance demonstrated no significant differences in rates of allogrooming by dominance class. These results suggest that dominance did not account for the variation in observed allogrooming behavior: Dominance status did not appear to determine the frequency with which animals groomed others, the number of grooming partners, or frequency of grooming that any individual received in comparison to that performed. High-ranking animals did not have significantly more grooming partners than low-ranking animals, and there appeared to be little competition within the groups for subordinates to groom high-ranking animals. When age, kinship, and group tenure are controlled, performance and reception of allogrooming are not strongly associated with dominance in single-gender social groups of male anubis baboons.     

Influence of food availability and climate on behavior patterns of western black crested gibbons (Nomascus concolor) at Mt. Wuliang,Yunnan, China

Food abundance and climatic factors can significantly affect the behavior of animals and constrain their activity budgets. The population of western black crested gibbons (Nomascus concolor) in Mt. Wuliang lives in montane forest and is close to the northern extreme of the distribution for gibbons (Hylobatidae). Their habitats show remarkable seasonal variation in terms of food availability, temperature, and rainfall. To understand behavioral adaptations of western black crested gibbons to different sets of ecological conditions, we examined relationships among food availability, mean temperature, rainfall, and behavior patterns by observing two groups for 1 year each. Our results revealed that activity budget was affected by food availability and mean temperature. The gibbons spent more time eating flowers when that resource was more available and spent less time moving when fruit was more available. The gibbons spent less time feeding and more time resting, and spent less feeding time on fruit and leaves when the mean temperature was lower. These results suggest that the gibbons displayed a pronounced preference for flowers as a food resource and adopted a time minimizer strategy when high‐nutrient food items (i.e., fruit) were more available. In addition, the gibbons adopted an energy‐conserving strategy during periods of low temperature. The flexibility of behavioral patterns in responding to food availability and temperature may potentially improve the gibbons’ prospects of surviving and reproducing in a northern montane forest.     

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.     

Grooming site preferences in primates and their functional implications

The hypothesis that skin care is an important function of allogrooming in primates was evaluated in the light of data on its physical distribution in a wide range of species. It was found that the distribution of autogrooming (assumed to be primarily utilitarian) and allogrooming over 17 body sites were complementary and that allogrooming was concentrated on areas which are inaccessible and/or invisible to an autogrooming animal. However, within accessible and inaccessible site categories, allogrooming was evenly distributed over the body surface, despite any special social or communicatory significance that particular sites may have. Intertaxonomic differences in the distributions of both types of grooming, notably between anthropoids and lemurs, lent further support to the notion of complementarity. It was concluded that the data support previous suggestions linking allogrooming site preferences with a utilitarian function, analytic and methodological differences being the probable explanation for discrepancies between these results and those obtained in another study.     

Group size and stability: Why do gibbons and spider monkeys differ?

Gibbons and spider monkeys have similar diets, body size, and locomotor patterns. They are therefore expected to be subject to similar socioecological rules. However their grouping patterns differ. Gibbons live in small stable groups, whereas spider monkey form unstable sub-groups that vary from small to large during different seasons. If similar principles apply to the two species, food abundance should vary more for spider monkeys than for gibbons; food density should be similar for the two species when spider monkey sub-groups are the same size as gibbon groups; and the highest level of food abundance should be higher for spider monkeys than for gibbons. These predictions are upheld for a comparison of particular populations ofHylobates muelleri andAteles geoffroyi.     

Selection of sleeping trees in pileated gibbons (Hylobates pileatus)

Selection and use patterns of sleeping sites in nonhuman primates are suggested to have multiple functions, such as predation avoidance, but they might be further affected by range defense as well as foraging constraints or other factors. Here, we investigate sleeping tree selection by the male and female members of one group of pileated gibbons (Hylobates pileatus) at Khao Ang Rue Nai Wildlife Sanctuary, Thailand. Data were collected on 113 nights, between September 2006 and January 2009, yielding data on 201 sleeping tree choices (107 by the female and 94 by the male) and on the characteristics of 71 individual sleeping trees. Each sleeping tree and all trees ≥40 cm diameter at breast height (DBH) in the home range were assessed (height, DBH, canopy structure, liana load) and mapped using a GPS. The gibbons preferentially selected tall (mean=38.5 m), emergent trees without lianas. The majority of the sleeping trees (53.5%) were used only once and consecutive reuse was rare (9.5%). Sleeping trees were closer to the last feeding tree of the evening than to the first feeding tree in the morning, and sleeping trees were located in the overlap areas with neighbors less often than expected based on time spent in these areas. These results suggest avoidance of predators as the main factor influencing sleeping tree selection in pileated gibbons. However, other non‐mutually exclusive factors may be involved as well. Am. J. Primatol. 72:617–625, 2010. © 2010 Wiley‐Liss, Inc.     

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.     

西黑冠长臂猿隔离小种群栖息地植被特征与其食性及生境利用

由于长期的捕猎及森林破坏,许多西黑冠长臂猿群体生活于零散的小型生境片段中。在云南南部芭蕉河地区,利用55个样方测量了西黑冠长臂猿一个隔离小种群栖息地植被,共记录乔木28科57属85种,其中壳斗科、樟科及省沽油科占优势地位,植被组成与结构在不同的森林片段、地形及干扰程度区域中差异显著。利用瞬时扫描法在两个年周期中的系统观察发现,与连续森林中的群体相比,芭蕉河长臂猿更加依赖对桂北木姜子、大果山香圆等优势乔木树种的取食,在乔木果实缺乏的季节,其并未取食更多叶类,而是进入次生植被搜寻藤本果实。可能受人为干扰及植被结构的影响,长臂猿未取食无花果类植物。原始林中植被结构并未对长臂猿生境利用造成明显影响,但其在不同森林片段间表现出显著的选择性。通过对芭蕉河、大寨子、平河及新平茶马古道四地的比较发现,西黑冠长臂猿栖息地植被特征存在较大的地区差异,其生态与行为可能因此表现出较强的适应性,但这需要更大时空尺度的研究予以验证。     

Linear enamel hypoplasia in gibbons (Hylobates lar carpenteri)

This study describes the expression of linear enamel hypoplasia (LEH), a sensitive dental indicator of physiological stress, in Thailand gibbons (Hylobates lar carpenteri). Previous studies of enamel hypoplasia in hominoids have focused on great apes, with little attention given to the expression of this stress indicator in gibbons. In that gibbons differ from both monkeys and great apes in numerous life history features, LEH expression in gibbons might be expected to show significant differences from both. In this study, 92 gibbon specimens from two sites in Thailand were compared with several samples of monkeys and great apes in their expression of LEH. The intertooth distribution of LEH in gibbons was compared to that of chimpanzees and rhesus monkeys. Gibbon populations from both sites exhibit LEH frequencies intermediate between those of the monkey samples, in which LEH prevalence is usually low, and those of the great ape samples, in which LEH prevalence is high. Gibbons differ significantly from monkeys, but not great apes, in the number of individuals whose teeth record multiple stress events. Multiple episodes of stress are rarely recorded in the teeth of monkeys, while multiple stress events occur with higher frequency in gibbons and great apes. Taxonomic variation in the duration of crown formation, the prominence and spacing of perikymata on dental crowns, life history features, and/or experience of physiological stress may explain these patterns. The intertooth distribution of LEH in gibbons is, for different reasons, unlike that of either chimpanzees or rhesus monkeys. The mandibular canines of gibbons have significantly more LEH than any of their other teeth. Aspects of crown morphology, perikymata prominence/spacing, enamel thickness, and crown formation spans are potential causes of taxonomic variation in the intertooth distribution of LEH.     

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.     

滇金丝猴雌性个体间的理毛行为

相互理毛行为广泛存在于社会性群居灵长类动物中,通常具有清洁卫生和社会交往功能。2012 年10 月至2013 年6 月,我们在云南白马雪山国家级自然保护区对一人工辅助投食滇金丝猴群,采用全事件取样法和焦点动物取样法收集了雌性个体间相互理毛的行为数据,包括理毛的部位、理毛的姿势、理毛的时间和回合数。研究结果表明:滇金丝猴雌性个体之间每次相互理毛的平均时间为5. 7 min。相互理毛部位较多的发生在自我理毛不能进行(达到)的部位(61.1% );在不能自我理毛部位的相互理毛行为持续时间长,平均9.7 min;在个体能够进行自我理毛部位的相互理毛持续时间短,平均为3. 2 min。相互理毛的姿势以对坐为主(48. 4% ),不同理毛姿势的理毛时间差异显著。新迁入家庭单元的雌性个体为理毛的首先发起者,但其获得被理毛的时间却并不多。滇金丝猴雌性个体相互理毛部位、理毛姿势和理毛时间的差异表明,它们之间的相互理毛行为符合卫生功能假说和社会功能假说。     

Maternal behavior of the Eurasian lynx <Emphasis Type="Italic">Lynx lynx</Emphasis> L. during the early postnatal ontogeny of its cubs

The dynamics of the major elements of maternal behavior of Eurasian lynx females during the first month of life of their cubs and their association with litter parameters (number of kittens, sex, and mass) have been traced. By the end of the first month, the amount of time spent by the female outside of the den significantly increases. An association between the litter size and maternal behavior has been found. Females rearing small litters spend more time outside of their den; they also spend more time on allogrooming of each separate kitten than females with large litters. Concerning allogrooming duration, a preference for male kittens by lynx females has been noticed in the third week.