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.     

Reciprocal Allogrooming in Dam-reared and Hand-reared Impala Fawns

Among adult females and males of African antelope impala are unique in their performance of reciprocal allogrooming. The occurrence of this behaviour in neonatal impala fawns was explored in a free-ranging impala herd at the San Diego Wild Animal Park where 5 dam-reared fawns were observed from birth through 10 weeks of age. One-way maternal grooming and reciprocal allogrooming with the dam and non dam partners emerged as distinct behavioural systems. Maternal grooming, directed mostly to the anogenital area, was typical of that seen in other ungulates, and sharply declined over the first two weeks. Reciprocal allogrooming, characterized by alternate exchanges of grooming bouts with a partner in the same manner as in adults, was seen as early as 3–8 d after birth. All fawns were grooming with unrelated adult females by the end of the second week. By week 2 virtually every measure of reciprocal allogrooming by fawns (grooming delivered per hour, reciprocity, and percent of encounters initiated) was as high as for adults. The appearance of this reciprocal allogrooming pattern, especially at such an early age, appears to be unique among ungulates, and possibly mammals in general. Three hand-reared impala fawns, deprived of the opportunity to interact with older herdmates, but having access to impala fawns and heterospecific fawns, were observed from 1–3 mo of age. The hand-reared impala showed no alteration in the occurrence of reciprocal allogrooming behaviour compared with the dam-reared control fawns, indicating that allogrooming experience with older animals was not required for the appearance of reciprocal allogrooming at an early age. Interestingly, hand-reared fawns persisted in grooming heterospecific fawns despite the fact that heterospecifics rarely reciprocated grooming. We postulate that the strong predisposition for impala young to groom others may be related to the threat of tick infestation in the impala's ecotone habitat.     

Allogrooming by adult Callithrix jacchus in relation to postpartum oestrus

The allogrooming behaviour of the parents (= α-animals) of three family groups of Callithrix jacchus has been studied during 25 days following birth. A total of 22 postpartum periods has been analysed. We recorded significant increase of grooming activity beginning with the 5th day postpartum. Allogrooming initiated by invitation gesture dropped to one-tenth of the total allogrooming frequency within one week, starting from day 5 postpartum. As a rule, allogrooming activity increased abruptly, whereas the decrease was mostly continuous, lasting several days. The maximum of postpartum allogrooming frequency preceded to some extent the maximum of copulatory activity and sexual willingness of the ♀. The ♂ made more attempts to groom the ♀ than vice versa. Up to the 18th day postpartum the ♀ ♀ ended more grooming sessions than the ♂ and than during anoestrus. The ♀ ♀ refused more invitations to grooming than did the ♂ ♂. The analysis of postpartum grooming behaviour in C. jacchus does not allow for accurate determination of the first and last day of the postpartum oestrus.     

Handedness and Grooming in Pan troglodytes: Comparative Analysis Between Findings in Captive and Wild Individuals

Grooming is a complex set of motor actions, common in highly social primates. We tested for asymmetries in hand use during unimanual and bimanual allogrooming in 215 captive chimpanzees. In addition to hand use, we coded in the ethogram whether the manual grooming action co-occurred with the use of the mouth. Overall, grooming did not elicit strong handedness at the individual level, but there is a small yet significant population-level right-hand bias for bimanual grooming. Mouth use during grooming had no influence on hand use. A comparison of the findings with previously published data on handedness for grooming in wild chimpanzees suggests that wild apes are more right-handed than captive individuals are for allogrooming. Collectively, the results suggest that role differentiation of the hands is an important factor in the assessment of handedness for grooming, and perhaps additional manual actions of chimpanzees and other primates.     

Reciprocity in play,grooming, and proximity in sibling and nonsibling young rhesus monkeys

Play, grooming, and proximity, and the degree to which these were reciprocated between pairs, were studied in immature sibling and nonsibling rhesus monkeys (Macaca mulatta)in four established captive groups over two seasons. “Interaction reciprocity” and “partner reciprocity” were assessed for each dyad for each of the three behaviors. In play, interaction reciprocity was based on the ratio between the play initiations by each dyad member,in grooming on the ratio between the grooming durations by each dyad member, and in proximity on the relative responsibility for proximity maintenance. Two or three most frequent (top) partners for each behavior were found for each individual. If two monkeys were among each other’s top partners, they were said to be reciprocal partners. Monkeys played with nonsiblings as much as with siblings but spent more time grooming and in proximity with siblings than with nonsiblings. Same-age nonsiblings (peers) were more frequent partners than other nonsiblings for each behavior. Siblings’ grooming interactions were more reciprocal than those of nonsiblings. There was no such effect for play and proximity. All-male dyads tended to be more reciprocal in play interactions, and all-female dyads tended to be more reciprocal in grooming interactions. In play, but not in grooming or proximity, the interaction reciprocity of reciprocal partners was higher than that of nonreciprocal dyads. It is argued that the three behaviors have similar roles in infant’s social development but they differ in the expression of this role. Hence the reciprocity patterns vary with the behavior.     

Differential effects of kinship,dominance, and the mating season on female allogrooming in a captive group ofMacaca fuscata

An analysis of allogrooming (total times spent grooming individual partners) of 8 sexually mature females (3–12 years of age) in a captive group of 17 Japanese macaques, shows that during the nonmating season, grooming distributions were characterized by high proportions of grooming given to family members and/or higher ranking nonkin. During the mating season, all eight females showed significant shifts in their grooming distributions, and four females showed significant shifts in grooming between their nonestrous and estrous periods (defined behaviorally). Fox six of eight females, mating season grooming was characterized by either high proportions of grooming given to family members and/or heterosexual and homosexual partners. It was found that within dyadic sexual relationships, dominants gave more grooming to subordinates than the former received, in contrast to a reversal of this pattern in the majority of these same dyads during the nonmating season. This is interpreted as one short-term function of grooming: a dominant asymmetrically grooms a subordinate sexual partner to maintain proximity with (or reduce tension in) the latter. The two remaining focal females (middle ranking, nulliparous) differed from the other females in that they shifted their mating season grooming to subordinate nonkin, despite the lack of evidence that this was a result of sexual interactions, patterns of partner availability, competition, patterns of grooming reciprocity, or agonistic alliance support. From these results, it is suggested that in some contexts, grooming of subordinate nonkin may function to reduce tension in thegroomer. In the Japanese macaque, this latter possibility and the asymmetric grooming of subordinate homosexual partners may prove to be exceptions to the general rule that female cercopithecine grooming of nonkin flows up the dominance hierarchy.     

Affiliative relationships and reciprocity among adult male bonnet macaques (Macaca radiata) at Arunachala Hill, India

In captivity, male bonnet macaques (Macaca radiata) frequently express "friendship" toward one another, including affiliative behavior such as huddling, grooming, coalitionary support, and sitting in close proximity. The purpose of this study was to determine whether wild adult male bonnet macaques also express "friendship" by investigating whether or not (1) adult male bonnet macaques have affiliative social relationships with other males, (2) the strength of social relationships varies among dyads, (3) there is time-matched reciprocity in allogrooming among dyads, and if so, whether the level of reciprocity occurs within a bout of grooming, a day, or over 2 months (the limit of this study), and (4) a correlation exists between the strength of social relationships and dominance ranks among adult males. Focal samples totaling 150 hr on all seven adult males in one study group were conducted to record both agonistic and affiliative interactions. Agonistic interactions were used to construct a dominance hierarchy, whereas affiliative interactions (sitting in proximity to within 1 m with and without grooming) were used to quantify the existence and strength of social bonds within dyads. Results show that adult male bonnet macaques had differentiated affiliative relationships with other males in their group. There was little reciprocity of grooming within a bout of grooming or within a day, but greater reciprocity over the study period of 2 months. There was no correlation between dominance ranking distance and the strength of affiliative relationship within dyads; however, within dyads lower-ranking males groomed higher-ranking males more than vice versa. This study suggests that friendships in male bonnet macaques are characterized not by immediate tit-for-tat reciprocal altruism, but by reciprocity over a longer time span, and that affiliative social relationships may be less constrained by agonistic relationships than is the case in more despotic species of macaques.     

Nursing behavior and early development of impala at San Diego Wild Animal Park

Because impala are commonly exhibited and handreared in zoos and their natural nursing behavior had not previously been studied, we examined nursing and early development in five impala calves housed in a large, naturalistic enclosure. Calves were observed for the first 5 weeks of life during 12-hr continuous watches and 20-min focal animal samples. Total daily suckling time decreased while time grazing and feeding on concentrates increased from 1–5 weeks of age. An increasing proportion of nursing bouts were terminated by the dam as calves matured, with dams terminating almost 70% of bouts during the first week. Suckling success and maternal grooming also decreased after week I, suggesting that impala mothers cut back early on nursing and grooming of offspring. Rapid decline in mother-young spatial proximity and a concomitant increase in calf association with age-mates over time suggests that the mother-young bond is weak and ephemeral in impala. An example of the implications of our results for improving handrearing programs would be that newborn calves should be started on a daylight feeding schedule of one bottle-feeding every three hours, and that they not be allowed to gorge themselves at any one of these feedings.     

The Time Frame of Partner Choice in the Grooming Reciprocation of Cebus apella

Recent theoretical and experimental studies argued that reciprocity is constrained by the cognitive limitations of most animals and that, when reciprocation occurs, it should necessarily be short term. In this study, we examined the time frame of partner choice in the reciprocal grooming of captive female tufted capuchin monkeys ( Cebus apella ). Female capuchins groomed preferentially those individuals that overall groomed them most. Tufted capuchins did sometimes reciprocate grooming immediately. We quantified the time course and probability of immediate reciprocation, and excluded from the analysis cases of immediate reciprocation. We then showed that, even excluding immediate reciprocation, female capuchins still preferred to groom those individuals that groom them most. Our results show that partner choice is not necessarily based on immediate reciprocation and suggest that capuchins are able to reciprocate over longer time frames. These findings argue against the hypothesis that long-term reciprocation is absent in species lacking sophisticated cognitive abilities. We suggest that reciprocal altruism over long time frames relies on a system of emotional bookkeeping.     

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     

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.     

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.     

Tolerant food sharing and reciprocity is precluded by despotism among bonobos but not chimpanzees

Tolerant food sharing among human foragers can largely be explained by reciprocity. In contrast, food sharing among chimpanzees and bonobos may not always reflect reciprocity, which could be explained by different dominance styles: in egalitarian societies reciprocity is expressed freely, while in more despotic groups dominants may hinder reciprocity. We tested the degree of reciprocity and the influence of dominance on food sharing among chimpanzees and bonobos in two captive groups. First, we found that chimpanzees shared more frequently, more tolerantly, and more actively than bonobos. Second, among chimpanzees, food received was the best predictor of food shared, indicating reciprocal exchange, whereas among bonobos transfers were mostly unidirectional. Third, chimpanzees had a shallower and less linear dominance hierarchy, indicating that they were less despotic than bonobos. This suggests that the tolerant and reciprocal sharing found in chimpanzees, but not bonobos, was made possible by the absence of despotism. To investigate this further, we tested the relationship between despotism and reciprocity in grooming using data from an additional five groups and five different study periods on the main groups. The results showed that i) all chimpanzee groups were less despotic and groomed more reciprocally than bonobo groups, and ii) there was a general negative correlation between despotism and grooming reciprocity across species. This indicates that an egalitarian hierarchy may be more common in chimpanzees, at least in captivity, thus fostering reciprocal exchange. We conclude that a shallow dominance hierarchy was a necessary precondition for the evolution of human‐like reciprocal food sharing. Am J Phys Anthropol 143:41–51, 2010. © 2010 Wiley‐Liss, Inc.     

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 and aggression in captive Japanese macaques

This study investigated the relations between allogrooming and aggression in a captive group of Japanese macaques (Macaca fuscata). Our aim was to test whether evidence of an interchange between allogrooming and a reduction in aggression could be identified at a group level. Female Japanese macaques did not direct less aggression to those group mates that groomed them most. Although generally they did not direct more grooming to those group mates that attacked them most, they did show increased grooming towards those nonkin group mates that showed the most aggression. These results are interpreted in light of the conflicting processes that are likely to underlie macaque social choices.     

The relative roles of kinship and reciprocity in explaining primate altruism

Several hypotheses have been proposed to explain the evolution of altruistic behaviours. Their relative roles in explaining actual cases of animal altruism are, however, unclear. In particular, while kin selection is widely believed to have a pervasive influence on animal behaviour, reciprocity is generally thought to be rare. Despite this general agreement, there has been no direct test comparing the relative roles of kinship and reciprocity in explaining animal altruism. In this paper, we report on the results of such a test based on a meta-analysis of allogrooming in primates, grooming being probably the most common altruistic behaviour among mammals. In direct contrast to the prevailing view, reciprocity played a much larger role than kinship in explaining primate allogrooming. These results point to a more significant role of reciprocity in the evolution of animal altruism than is generally acknowledged.
Ecology Letters (2010) 13: 45–50     

Grooming and group cohesion in primates: implications for the evolution of language

It is well established that allogrooming, which evolved for a hygienic function, has acquired an important derived social function in many primates. In particular, it has been postulated that grooming may play an essential role in group cohesion and that human language, as verbal grooming or gossip, evolved to maintain group cohesion in the hominin lineage with its unusually large group sizes. Here, we examine this group cohesion hypothesis and test it against the alternative grooming-need hypothesis which posits that rates of grooming are higher in species where grooming need (i.e. the motivation to groom for hygiene and its associated psychological reward) is more pronounced. This alternative predicts that the derived social function of grooming evolved mostly in those lineages that had the highest exposure to ectoparasites and dirt, i.e. terrestrial species. A detailed comparative analysis of 74 species of wild primates, controlling for phylogenetic non-independence, showed that terrestriality was a highly significant predictor of allogrooming time, consistent with the prediction. The predictions of the group cohesion hypothesis were not supported, however. Group size did not predict grooming time across primates, nor did it do so in separate intra-population analyses in 17 species. Thus, there is no comparative support for the group-cohesion function of allogrooming, which questions the role of grooming in the evolution of human language.     

Grooming Between Male Chimpanzees at Ngogo,Kibale National Park. I. Partner Number and Diversity and Grooming Reciprocity

Allogrooming serves many social functions in primates. Grooming can help individuals to service social relationships generally, sometimes reciprocally, and may be particularly important in the development and maintenance of alliances. However, time constraints limit the number of partners with whom one individual can groom enough to maintain cooperative relationships. As a result, the size of its grooming network may reach an asymptote as the size of its group increases, and it may distribute its grooming less equally among potential partners. Chimpanzees live in multimale, fission-fusion communities; males are philopatric, and commonly associate and groom with each other. Males form within-community alliances that influence dominance rank and access to mates, and allies groom with each other regularly; males also cooperate in aggression between communities. The chimpanzee community at Ngogo, in Kibale National Park, Uganda, is unusually large and has more males than any other known community. Field data show that adult Ngogo males groomed far more with other adult males than with females or with adolescent males, in contrast to a previous report (Ghiglieri, 1984). Adolescent males groomed adults much more than the reverse; males groomed and were groomed by females about equally. Individual males groomed mostly with a small number of other males. On average, males at Ngogo had only slightly more male grooming partners overall and had the same number of important partners as those of males in a much smaller community in the Mahale National Park, Tanzania, and they distributed their grooming less equitably. These results fit those expected if limits on available grooming time cause males to have a loyalty problem as the number of potential grooming and alliance partners increases. Despite differences in the extent and equitability of their grooming networks, males at both Ngogo and Mahale showed reciprocity in grooming. Grooming reciprocity has been demonstrated for captive chimpanzee males, but the Ngogo findings are the first demonstrations of reciprocity in wild communities.     

Grooming up the hierarchy: the exchange of grooming and rank-related benefits in a new world primate

Seyfarth's model assumes that female primates derive rank-related benefits from higher-ranking females in exchange for grooming. As a consequence, the model predicts females prefer high-ranking females as grooming partners and compete for the opportunity to groom them. Therefore, allogrooming is expected to be directed up the dominance hierarchy and to occur more often between females with adjacent ranks. Although data from Old World primates generally support the model, studies on the relation between grooming and dominance rank in the New World genus Cebus have found conflicting results, showing considerable variability across groups and species. In this study, we investigated the pattern of grooming in wild tufted capuchin females (Cebus apella nigritus) in Iguazú National Park, Argentina by testing both the assumption (i.e., that females gain rank-related return benefits from grooming) and predictions (i.e., that females direct grooming up the dominance hierarchy and the majority of grooming occurs between females with adjacent ranks) of Seyfarth's model. Study subjects were 9 adult females belonging to a single group. Results showed that grooming was given in return for tolerance during naturally occurring feeding, a benefit that higher-ranking females can more easily grant. Female grooming was directed up the hierarchy and was given more often to partners with similar rank. These findings provide supporting evidence for both the assumption and predictions of Seyfarth's model and represent, more generally, the first evidence of reciprocal behavioural interchanges driven by rank-related benefits in New World female primates.     

Social behavior in a captive chimpanzee (Pan troglodytes) group

A group of captive chimpanzees, consisting of one adult male and three mother/infant pairs, was systematically observed over a 15-month period. Over 200 hr of data were collected, using both sequential and time sampling techniques, and compared to the available data on wild chimps. Unlike many captive groups, most behavior patterns were remarkably similar, both qualitatively and quantitatively, to that of wild chimpanzees including: play, grooming, infant sexual development, tool use, food sharing, prosocial partner preferences, and aggressive displays.