Short-Term Benefits of Play Behavior and Conflict Prevention in Pan paniscus

Most theories on the function of play have focused on ultimate rather than proximate benefits. Play peaks during juvenility but, in some species, it is present in adulthood as well. In primates, social play and grooming often show a matched pattern because they bring individuals into close contact and favor social cohesion. In Pan, researchers have widely documented anticipation of competition at feeding time. Chimpanzees limit aggression over food by grooming (celebration), whereas bonobos use sociosexuality as a reassurance mechanism. We examined the function of play in the context of conflict prevention in the Apenheul bonobo colony. We analyzed the distribution of social play, grooming, and sexual contacts in periods around feeding and in a control condition. Adult-adult and adult-immature play frequencies were significantly higher during prefeeding than in any other condition, thus not supporting the commonly held view that social stress suppresses play. Further, there is a significant positive correlation between adult-adult play and rates of cofeeding. During feeding, adults engaged in their highest levels of sociosexual behaviors, whereas an increase in grooming rates occurred in prefeeding, though not significantly compared to the control rates. In conclusion, bonobos apparently cope with competition and social tension via 2 different mechanisms of conflict management: play to prevent tension, e.g., prefeeding, and sociosexual behaviors as appeasement and reassurance mechanisms once a tense situation emerges.     

Social structures in Pan paniscus: testing the female bonding hypothesis

Based on previous research in captivity, bonobos, Pan paniscus, have been called a female-bonded species. However, genetic and behavioural data indicate that wild females migrate. Bonding between these unrelated females would then be in contradiction with socio-ecological models. It has been argued that female bonding has been overemphasized in captive bonobos. We examine patterns of proximity, grooming and support behaviour in six well established captive groups of bonobos. We find that female bonding was not a typical characteristic of all captive bonobo groups. In only two groups there was a trend for females to prefer proximity with other females over association with males. We found no evidence that following or grooming between females was more frequent than between males and unrelated females or between males. Only in coalitions, females supported each other more than male–female or male–male dyads. We also investigated five mother–son pairs. Grooming was more frequent among mothers and sons than in any other dyad, but sons did not groom their mothers more than males groomed unrelated females. Mothers groomed their sons, or provided more support to them than females groomed or supported unrelated males. Thus, while bonds between females were clearly present, intersexual relations between males and either unrelated females or their mothers are of more, or equal importance.     

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.     

Context and Development of Sexual Behavior of Wild Bonobos (Pan paniscus) at Wamba, Zaire

I studied sexual behavior of immature bonobos (Pan paniscus) in a wild group living at Wamba, Zaire, with special reference to its development. Even immature individuals under 1 year old performed sexual behavior. Sexual behavior occurred in almost all age–sex combinations, except between immature and mature females. Based on analyses of behavioral pattern and context, I classified sexual behavior involving immature individuals into three categories. (1) Genital contact between immature individuals was observed during play, and was performed by males more frequently than by females. This sexual behavior shared many traits with that of other great apes. (2) Copulation-like genital contact was observed between immature males and mature females. Its frequency increased with the immature male's age; it developed into copulation in adulthood. (3) Genital contact used to regulate interindividual relationships. This behavior, which is unique to bonobos, was absent among infants. It developed between late juvenile and early adolescent periods in association with changes in social circumstances.     

Reproductive Parameters of Female<Emphasis Type="Italic">Pan paniscus</Emphasis> and <Emphasis Type="Italic">P. troglodytes</Emphasis>: Quality versus Quantity

We investigated intra- and interspecific differences in life history and reproductive parameters in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). We compare the parameters of wild and captive females in order to shed light on the influence of habitat or specific differences or both on reproduction. We present new and additional information on reproductive parameters from captive bonobos and chimpanzees. Captive chimpanzees birth more live offspring and have a shorter interbirth interval, but experience higher infant mortality than captive bonobos. Although captive bonobo females tend to start reproduction at a younger age than chimpanzees, this is effectively only so for wild-born females of both species. Ultimately both species reach the same rate of production of offspring surviving to 5 yr. These results contrast with data from the wild. Wild bonobos tend to have higher reproductive success, a higher fertility rate and a shorter interbirth interval than wild chimpanzees. Reproduction is similar for wild and captive bonobos, which suggests that they are producing at their maximum under both conditions. Overall captive chimpanzees perform better than their wild conspecifics, probably because of lower feeding competition. Infant survival is the only specific difference not affected by captivity. Bonobo infants survive better, which suggests that chimpanzee infants are more at risk. We argue that the interspecific variation in reproductive parameters in captivity is related to the different influence of captivity on reproduction and different pressures of external sources of infant and juvenile mortality.     

Female Genito-genital Rubbing in a Group of Captive Chimpanzees

Wild and captive female bonobos exhibit a form of noncopulatory sexual behavior—genito-genital (GG) rubbing—in which 2 individuals rub their genital regions together. GG-rubbing in bonobos occurs in several contexts and may serve several functions, including tension reduction and reconciliation. It has not been reported for chimpanzees. In a study of captive, adolescent chimpanzees at the New Iberia Research Center, I observed that females rubbed genital regions at rates equivalent to those of bonobos, though the form of the behavior differed in significant ways from classic bonobo GG-rubbing. I describe the pattern of GG-rubbing in the chimpanzees and provide preliminary tests of 5 hypotheses for why the behavior occurs. All 4 females in the study group participated in GG-rubbing, though the frequency with which they initiated and participated varied. Females that GG-rubbed the most also groomed each other the most, supporting the hypothesis that GG-rubbing reinforces or at least reflects social bonds. The data do not support the hypothesis that females GG-rub to reconcile conflicts, to reduce tension during feeding, to signal social status, or to attract mates.     

Comparing infant and juvenile behavior in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes): a preliminary study

The dichotomy between the two Pan species, the bonobo (Pan paniscus) and chimpanzee (Pan troglodytes) has been strongly emphasized until very recently. Given that most studies were primarily based on adult individuals, we shifted the “continuity versus discontinuity” discussion to the infant and juvenile stage. Our aim was to test quantitatively, some conflicting statements made in literature considering species differences between immature bonobos and chimpanzees. On one hand it is suggested that infant bonobos show retardation in motor and social development when compared with chimpanzees. Additionally it is expected that the weaning process is more traumatic to chimpanzee than bonobo infants. But on the other hand the development of behaviors is expected to be very similar in both species. We observed eight mother–infant pairs of each species in several European zoos. Our preliminary research partially confirms that immature chimpanzees seem spatially more independent, spending more time at a larger distance from their mother than immature bonobos. However, the other data do not seem to support the hypothesis that bonobo infants show retardation of motor or social development. The development of solitary play, environmental exploration, social play, non-copulatory mounts and aggressive interactions do not differ between the species. Bonobo infants in general even groom other group members more than chimpanzee infants. We also found that older bonobo infants have more nipple contact than same aged chimpanzees and that the weaning process seems to end later for bonobos than for immature chimpanzee. Additionally, although immature bonobos show in general more signs of distress, our data suggest that the weaning period itself is more traumatic for chimpanzees.     

Food calling by captive bonobos (Pan paniscus): An experiment

We examined (i) whether bonobos display a specific food-calling behavior when discovering a hidden food resource, (ii) whether the presence of competitors affects this behavior, and (iii) whether food quantity or gender influences its appearance. We carried out experiments (n = 108) within a captive group of eight bonobos at the Animal Park Planckendael (Mechelen,Belgium). We hid highly preferred food items (n = 7 or 25) in their enclosure and recorded vocal behavior and interactions between discoverer and group members. As a control, we gave the same number of items to the individuals when isolated from the group, a situation without potential food competition (n = 38). The only vocalization frequently uttered by the discoverer was the food peep. They uttered food peeps significantly more often when no food competition was possible. The amount of food had no significant influence on whether food peeps were uttered. The same applies to the individuals’ identity or gender. Although the costs of food calling behavior seemed much higher for males, both sexes uttered food calls to the same extent. We hypothesize thai males signal food presence in order to attract potential mates and are willing to give up the discovered food resource in return for sex: sex for food exchange. In contrast, females may vocalize to attract coalition partners. Through these coalitions, they can monopolize food resources vis-à-vis males. It is also possible that females have less reason to suppress food calk, since they are dominant to males. This study suggests that bonobos are able to give shaded signals about their environment and have the potential to communicate this information in order to promote their sexual strategy.     

Sex differences in play behavior in juvenile tufted capuchin monkeys (Cebus apella)

According to the motor training hypothesis, play behavior in juvenile primates improves motor skills that are required in later adult life. Sex differences in juvenile play behavior can therefore be expected when adult animals assume distinct sexually dimorphic roles. Tufted capuchin monkeys show sexually dimorphic levels of physical antagonism in both inter- and intra-group encounters. Accordingly, it can be predicted that juvenile capuchins also show sex differences in social play behavior. To test this hypothesis, the play behavior of nine juvenile and two infant capuchins was examined. As predicted, juvenile males showed significantly higher levels of social play (wrestle, chase) than juvenile females, but no differences were found in nonsocial play (arboreal, object). Levels of infant play behavior were comparable to that of juveniles. These results lend support to the motor training hypothesis and highlight the need for more detailed investigations of individual differences in play behavior. An erratum to this article can be found at     

Carrying and hand-use patterns in Panamanian white-faced capuchins (Cebus capucinus)

The aim of this project was to examine the potential influence of postural regulation on capuchin hand-use patterns by focusing on tasks that involved the carrying of objects. Two months were spent on Barro Colorado Island, Panama, collecting data on ten white-faced capuchins (Cebus capucicus) (four adult males/six adult females). Over 215 contact hours were spent with the monkeys, and a total of 213 carries were recorded. No hand preference bias at the population level was found for the carry task; and no detectable hand-use patterns for carry were correlated with the weight of the object carried (except a right-hand bias for carrying medium-sized objects), the plane of the monkey's movement, its locomotor pattern, or its height above the ground. Therefore, the results of this study do not support the hypothesis that the need for postural regulation while carrying an object influences hand-use patterns in free-ranging capuchins. Our results are especially important because they are contrary to the results of the only other free-ranging capuchin laterality study conducted to date (Panger, 1998).     

Sexual competition in a group of captive bonobos (Pan paniscus)

We describe the occurrence of sexual competition, expressed as harassment of sexual interactions in a captive group of bonobos. We monitored all aggressive and pestering interventions during sexual interactions of three captive adult females, one adolescent, and three adult males. The study period covered two complete menstrual cycles for each female, with continuous daily observations. There was relatively little overt sexual competition by the males, in analogy with other studies. Most male interventions occurred towards interactions with the alfa female. The alfa female performed the most intense and the highest number of interventions towards the sexual interactions of the other females. The data provide evidence for female intra-sexual competition in this female dominant species.     

Bonobo but not chimpanzee infants use socio-sexual contact with peers

Bonobos have been observed to use socio-sexual behavior at higher frequency than chimpanzees. Little is known about the developmental influences that shape this behavior in bonobos. We compared the social sexual behavior of wild-born bonobo (n = 8) and chimpanzee (n = 16) infants in an experimental feeding test. Subjects of both species were orphans of the bushmeat trade living at sanctuaries in peer groups. During the experiment, chimpanzee infants never had socio-sexual interactions with one another. In contrast, bonobo infants had socio-sexual interactions significantly more than the chimpanzee infants and more often when food was presented. During these socio-sexual interactions, bonobo infants did not show a preference for heterosexual partners or genital–genital positioning that is reproductive in adults (e.g. a dorso–ventral posture). These findings suggest that the socio-sexual behavior previously observed in various captive and wild bonobos is species-typical. Wild-born bonobos originating from a large geographical range develop this behavior long before puberty and without the need for adults initiating such behavior or acting as models for observational learning. Meanwhile, chimpanzee infants of the same age with similar rearing history show no signs of the same socio-sexual behavior. Results are interpreted regarding hypotheses for the evolution of bonobo psychology.     

Sex Differences in the Steepness of Dominance Hierarchies in Captive Bonobo Groups

Bonobos have a reputation as a female-dominated and egalitarian species. We examined the 2 aspects of dominance in 6 captive bonobo groups. Females do not consistently evoke submission from all males in all contexts. Though females occupy the highest-ranking positions in the dominance hierarchy, there are in each group males that obtain rather high ranks and are able to dominate ≥1 female. Thus female dominance is not complete and hierarchies can be better described as nonexclusive female dominance. We studied egalitarianism by measuring linearity and steepness of dominance hierarchies. The hierarchies of all groups are highly linear. Hierarchies among males are steeper than among females. On average, male bonobos are more despotic than females, but females too can have despotic relations, both with other females and with males. Hence one can call bonobos in captivity semidespotic rather than egalitarian.     

Co–Residence between Males and Their Mothers and Grandmothers Is More Frequent in Bonobos Than Chimpanzees

In long–lived social mammals such as primates, individuals can benefit from social bonds with close kin, including their mothers. In the patrilocal chimpanzee (Pan troglodytes spp.) and bonobo (Pan paniscus), sexually mature males reside and reproduce in their natal groups and can retain post-dependency bonds with their mothers, while immatures of both sexes might also have their paternal grandmothers available. However, quantitative information on the proportion of males and immatures that co-reside with both types of these close female relatives is limited for both species. Combining genetic parentage determination and group composition data from five communities of wild chimpanzees and three communities of wild bonobos, we estimated the frequency of co-residence between (1) mature males and their mothers, and (2) immature males and females and their paternal grandmothers. We found that adult males resided twice as frequently with their mothers in bonobos than in chimpanzees, and that immature bonobos were three times more likely to possess a living paternal grandmother than were immature chimpanzees. Patterns of female and male survivorship from studbook records of captive individuals of both species suggest that mature bonobo females survive longer than their chimpanzee counterparts, possibly contributing to the differences observed in mother–son and grandmother–immature co-residency levels. Taking into account reports of bonobo mothers supporting their sons'' mating efforts and females sharing food with immatures other than their own offspring, our findings suggest that life history traits may facilitate maternal and grandmaternal support more in bonobos than in chimpanzees.     

Hand preference in capuchin monkeys varies with age

The purpose of this research was to examine the influence of age on hand preference in capuchin monkeys (Cebus apella). Twenty-two capuchins, aged 6 months to 30 years, were presented with a task that involved reaching for food and a task that involved using sponging tools to absorb juice. Adults exhibited a greater percentage of right-handed actions in each task than did immature subjects. Adults also exhibited a stronger lateral bias than did immature subjects in the sponging task. These results are consistent with hypotheses: a) adult capuchin monkeys are biased toward use of their right hand for reaching; b) adult capuchins exhibit a greater incidence of right-hand preference than do immature capuchins; and c) primates exhibit age-related differences in the strength and direction of hand preference in tasks that involve the use of tools.     

Urine Washing and Sniffing in Wild White-faced Capuchins (<Emphasis Type="Italic">Cebus capucinus</Emphasis>): Testing Functional Hypotheses

Urine washing (UW) is taxonomically widespread among strepsirhines and platyrrhines, yet its functional significance is still unclear. We used 2274 h of focal follows of 35 adult and subadult wild white-faced capuchins (Cebus capucinus) to test 1) the intergroup signaling, intragroup social signaling, and thermoregulatory hypotheses for UW and 2) the hypothesis that individuals sniff each other's urine and other traces to gather socially significant information. Males engaged in significantly more UW than females. All 5 α-males engaged in more UW than subordinate males did, including 4 α-males that increased their UW rate above that of their male groupmates after their rise to α rank. Males engaged in significantly less UW while in view of other males than at other times. Male-male sniffing rates do not correlate with either aggression rate or dominance rank distance. Urine washing rates did not increase while subjects were in parts of their home range where more intergroup encounters occurred. Urine washing rates were highest early in the morning and late in the afternoon, presumably when temperatures were coolest. The data do not support either the thermoregulatory or social signaling hypothesis. We suggest that experiments with captive capuchins are necessary to resolve the issue of the function of urine washing in the taxon.     

Coping with Acute Crowding by Cebus apella

Traditionally, scientists believed that crowded housing conditions increased aggression in animals. Recent research on captive primates fails to support a linear relationship between population density and aggressive behavior. Our study is the first to investigate the effects of acute crowding on a New World primate. We observed brown capuchins (Cebus apella) under 2 different spatial conditions: a control that offered the full indoor space in the enclosure and a short-term experimental condition that restricted the capuchins to approximately half the amount of space of the control condition. We compared rates of self-grooming, aggression, contact sitting, social grooming, and play between both conditions. We conducted a mixed factorial ANOVA at the individual level while taking subject sex and age class into account. Intense aggression, play, and social grooming decreased significantly in crowded conditions, suggesting that capuchins avoid social encounters if spatially confined. Their strategy for coping with acute crowding via a decrease in all forms of social behavior is intermediate between chimpanzee and macaque strategies in similar experiments. The only behavior to increase under crowding was a nonsocial, self-directed behavior with the potential of reducing arousal: self-grooming.     

Social integration of a bonobo mother and her dependent daughter into an unfamiliar group

In the present study, we obtained quantitative behavioral data on the integration process of an adult female with her dependent daughter into a resident zoo population of six bonobos (Pan paniscus). During the whole observation time of almost two months, the integration happened very peacefully without significant increases of aggressive or agonistic tendencies. The integration was mediated and actively supported mainly by two processes: contacts of resident infants and juveniles towards the immigrating animals and contacts of the immigrating adult female to a “specific senior female” of the resident group. Adult males and adolescent females seemed not to play a role in the social integration of new group members. The new adult female soon became a preferred partner for sexual interactions such as genito-genital rubbing. The social integration of the 18-month-old young was controlled by her mother and finished only after the adult female had reached a stable and safe position in the new group. According to our observations, the exchange of an adult female bonobo including her young between zoos has no negative effects on the animals involved.     

Multiple paternity and kinship in the gray fox (Urocyon cinereoargenteus)

Despite mounting evidence that extra-pair copulations (EPCs) are common in the Canidae, no studies have examined the most basal member of this family, the gray fox (Urocyon cinereoargenteus). In this study we explored the possibility that gray foxes may be socially, but not genetically, monogamous. Multiple paternity was confirmed in one litter and suspected in three others (n=7), thus 14.3–57.1% of all litters had more than one father. In this high-density population, multiple paternity may be one strategy to reduce inbreeding, although only one pair was significantly related to each other (r=0.36). Mother–daughter pairs were more common than father–son pairs. These results coupled with a previous study showing a female-biased sex ratio suggest male-biased dispersal and the potential for helper females.