Monitoring hormones in urine and feces of captive bonobos (Pan paniscus)

Urinary and fecal hormones were analyzed on average every other day in 17 female bonobos kept at four US zoos (San Diego Zoo and Wild Animal Park, Milwaukee, Columbus, and Cincinnati). Ovarian cycle activity was monitored throughout the 15-month study period using estrogen and progesterone profiles and swelling charts. Behavioral data on sexual activity were also collected on a daily basis. Fecal and urinary samples were analyzed using high pressure liquid chromatography (HPLC), gas chromatography-mass spectrometry (CG-MS), and nanoelectrospray. Preliminary results indicate that in urine, both conjugated progestin and estrogen metabolites were abundant, while in fecal samples, free progestin metabolites from the 5a-pregnane series were found. Although traces of estrogen metabolites were detected in fecal samples, long-term monitoring of ovarian activity in our study yielded no meaningful estrogen profiles. In contrast, fecal progestin profiles, after adjusting for a one-day delay in excretion, closely matched the corresponding urinary progestin profiles. Using the identical antibody and tracer for both, fecal and urinary progestins, fecal samples yielded approximately ten times the relative amount of progestins compared to urinary progestins. Thus, when converted using a regression formula, fecal progestins may complete the picture obtained from urinary progestins, particularly in cases where the urine sample record is unavailable or incomplete. Evidence of the usefulness of urinary cortisol as a measure of stress is presented.     

Function and distribution of coalitions in captive bonobos (Pan paniscus)

We examined the distribution of support behaviour within a captive group of bonobos. Most support was evoked by inter-sexual conflicts with the two highest ranking females. Within a dyad, the usual winner was most often supported. Individuals that challenged the rank order by aggressions and pestering were aggressed more often by their targets in the company of an ally. The two lowest ranking males served as scapegoats, receiving 80% of the contra-support. In coalitions, inviduals did not aggress victims they would not dare to attack without supporters. However, the victims of coalitions reacted more strongly with fear and rarely counteraggressed than when being attacked alone, indicative of the high impact of aggression in support. The alpha female showed some control behaviour when intervening in conflicts. The data fitted with several functional hypotheses: coalitions functioned to maintain existing ranks, to acquire ranks, to reduce tension, and to test or strengthen the bond. We suggest that support behaviour fulfilled a crucial role in the maintenance of the power of the two highest ranking females over the males. Among the females themselves the dominance relationships were not based on coalitions, but on individual attributes.     

Peering in mature, captive bonobos (Pan paniscus)

“Peering”—close-proximity staring at the mouth of another—was observed in ten (three males and seven females) mature (at least 7 years old) bonobos (Pan paniscus) living in three social groups at the San Diego Zoo and Wild Animal Park. Instantaneous scan samples, taken at 2-min intervals, over a three-and-a-half year period, yielded 617 observations of peering (1.4 per observation hour). Food was exchanged in only 15 of these scans. Peering was most often performed by younger animals and was primarily directed toward older females (“matrons”). In a given dyad, the animal more likely to peer at the other was also more like to both peer and be peered at if they frequently groomed and infrequently displayed aggression at a given female. An adolescent male showed the highest frequency of peering when living with two older females, but dropped to adult male levels when later housed with two younger (albeit mature) females. A reversal in which animal was more likely to peer, follow, and groom occurred in one female dyad, after the birth of the younger animal's first infant. After a similar birth in the other group, no such changes were observed. We discuss how these and related findings, in conjunction with what is known of the social structure of this species, suggest that one possible function of peering in bonobos may be as a signal acknowledging female status.     

Female relationships in bonobos(Pan paniscus)

The popular belief that women are not naturally able to bond with each other is often supported by theoretical and empirical evidence that unrelated females do not bond in nonhuman primate species. Bonobos (rare and endangered African apes, also known as pygmy chimpanzees) are (with their congener, chimpanzees) the closest living relatives of humans and appear to be an exception to this characterization. Data collected on individuals representing half of the world’s captive population reveal that bonobo females are remarkably skillful in establishing and maintaining strong affiliative bonds with each other despite being unrelated. Moreover, they control access to highly desirable food, share it with each other more often than with males, engage in same-sex sexual interactions in order to reduce tension, and form alliances in which they cooperatively attack males and inflict injuries. Their power does not stem from a size equality with or advantage over males (in fact, females average 82.5% of male size), but rather from cooperation and coalition formation. The immediate advantage to female alliances is increased control over food, the main resource on which their reproductive success depends, as well as a reduction in other costs typically associated with a female-biased dispersal system, such as male agonism in the contexts of feeding competition and sexual coercion. The ultimate advantage of friendly relationships among females is an earlier age at first reproduction, which results in a large increase in lifetime reproductive success. Analysis of this bonding phenomenon sheds light on when, where, and how we should expect unrelated human females to bond with one another by demonstrating that bonding is not dependent on access to one’s relatives but rather on an environmental situation in which female aggregation is possible, coupled with an incentive for cooperation.     

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.     

Evidence for the consumption of arboreal,diurnal primates by bonobos (Pan paniscus)

We present evidence for the consumption of a diurnal, arboreal, group living primate by bonobos. The digit of an immature black mangabey (Lophocebus aterrimus) was found in the fresh feces of a bonobo (Pan paniscus) at the Lui Kotale study site, Democratic Republic of Congo. In close proximity to the fecal sample containing the remains of the digit, we also found a large part of the pelt of a black mangabey. Evidence suggests that the Lui Kotale bonobos consume more meat than other bonobo populations and have greater variation in the mammalian species exploited than previously thought [Hohmann & Fruth, Folia primatologica 79:103–110]. The current finding supports Stanford's argument [Current Anthropology 39:399–420] that some differences in the diet and behavior between chimpanzees (P. troglodytes) and bonobos are an artefact of the limited number of bonobo study populations. If bonobos did obtain the monkey by active hunting, this would challenge current evolutionary models relating the intra‐specific aggression and violence seen in chimpanzees and humans to hunting and meat consumption [Wrangham, Yearbook of Physical Anthropology 42:1–30]. Am. J. Primatol. 71:171–174, 2009. © 2008 Wiley‐Liss, Inc.     

Possible roles of consolation in captive chimpanzees (Pan troglodytes)

Empathy is a necessary prerequisite for the occurrence of consolation. The term "consolation" contains a hypothesis about function, which is distress alleviation. The present study aims to confirm the occurrence of consolation in captive chimpanzees via the post-conflict/matched-control method (PC-MC) and to suggest its possible roles. We collected 273 PC-MC pairs in the group of Pan troglodytes housed in the ZooParc de Beauval (France). We confirmed the presence of consolatory contacts (mean level of consolation, 49.5% +/- 22.3% SEM) in the colony. Consolation rates were significantly higher than reconciliation levels (mean level of reconciliation, 28.9% +/- 16.8% SEM). The level of consolation was greater in the absence of reconciliation than in the presence of it, suggesting that consolation might be an alternative behavior. As friendship and relatedness did not influence the occurrence of consolation, they did not seem to be the best prerequisites for this behavioral mechanism, at least in this chimpanzee colony. Affinitive contacts with third parties were significantly more frequent when the victim called attention to itself during severe aggressions by screaming. These high-pitched sounds seem to be useful in eliciting aid from conspecifics, as occurs in young humans. The occurrence of consolation reduced the likelihood of further attacks among group-members. From this perspective, both victims and consolers most likely gain potential advantages by interacting with each other when aggression is particularly severe, reconciliation is not immediate, and consequently social stress reaches high levels.     

Handedness in captive bonobos (Pan paniscus)

Species level right-handedness is often considered to be unique to humans. Handedness is held to be interrelated to our language ability and has been used as a means of tracing the evolution of language. Here we examine handedness in 3 captive groups of bonobos (Pan paniscus) comprising 22 individuals. We found no evidence for species level handedness. Conclusions that can be drawn from these findings are: (1) species level handedness evolved after the divergence of the Pan and Homo lineages; (2) inconsistent preferences may represent precursors to human handedness, and (3) Pan may have language abilities but these cannot be measured using handedness.     

Observations of physical abnormalities among the wild bonobos (Pan paniscus) of Wamba,Zaire

The wild bonobos (Pan paniscus) of Wamba, Zaire have an extremely high frequency of external abnormal traits. Out of 96 animals in a sample comprising all age and sex classes from two different natural groups, 46 individuals had at least one limb defect. The frequency of abnormalities was greater in males than in females, and increased directly with age. Almost all infants and juveniles had completely normal limbs, but virtually all males and over half the females which had reached their prime were found to have one or more limb defects. These findings indicate that congenital factors contribute little to the frequency of abnormalities in this sample. Survival rate is the same in individuals with defects as in those without defects. It appears that individual social status is far more important in procuring foods than locomotor ability. Thus, the operation of such abnormalities as a selective factor in intraspecific competition is minimized in the network of their social relations.     

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.     

Reconciliation, consolation and postconflict behavioral specificity in chimpanzees

Conflicts of interest arise regularly in the lives of all group-living animals and may escalate into aggressive conflicts. The costs of aggressive escalation can be reduced through peaceful postconflict interactions. This study investigated the postconflict behavior of 22 adult chimpanzees at Chester Zoo. The occurrence of reconciliation, i.e. the postconflict affiliative reunion between conflict opponents, and consolation, i.e. a postconflict affiliative interaction directed from a third party to the recipient of aggression, were demonstrated. Consolation was more likely to occur in the absence of reconciliation than after reconciliation, and reconciliation was more likely to occur in the absence of consolation than after consolation, supporting the hypothesis that consolation acts as a substitute for reconciliation when the latter fails to occur. Evidence for behavioral specificity, i.e. context-specific use of certain behaviors, was found for both reconciliation and consolation, which, along with high conciliatory tendencies, suggests an explicit style of postconflict behavior in the study subjects.     

Pan paniscus and human evolution

Detailed comparisons of the postcranium, cranium, and dentition of Pan paniscus, Pan troglodytes, and Homo reveal that except for slight differences in fore- and hindlimb proportions and the morphology of the shoulder, the postcranium of the two species of Pan are allometrically scaled variants of the same animal and one does not resemble Homo more than the other. Nor does the postcranium of one species of Pan resemble Australopithecus more closely than the other when the effects of body size are controlled. The over all morphological pattern of the skull and teeth of the two chimpanzees is clearly different, however, but both are about equally distinct from the earliest known members of the family Hominidae.     

Postconflict behavior in captive western lowland gorillas (Gorilla gorilla gorilla)

Postconflict (PC) behaviors, including reconciliation and consolation, have been observed in many primate and several nonprimate species. Using the PC-matched control (MC) method, PC behavior was examined in two groups (n=13) of captive western lowland gorillas, a species for which no conflict resolution data have been published. Analyses of 223 conflicts showed significantly more affiliation between former opponents after a conflict when compared to control periods, indicating reconciliation. Results also showed significantly more affiliation between the victim and a third-party after a conflict, indicating consolation. Both solicited and unsolicited consolation were observed. The majority of the affiliative interactions observed for both reconciliation and consolation were social proximity, which suggests that unlike most nonhuman primates, proximity, rather than physical contact, may be the main mechanism for resolving conflicts in western lowland gorillas. PC behavior was not uniform throughout the groups, but rather varied according to dyad type.     

Behavioral and physiological response to inequity in bonobos (Pan paniscus)

Inequity aversion (IA), the affective, cognitive, and behavioral response to inequitable outcomes, allows individuals to avoid exploitation and therefore stabilizes cooperation. The presence of IA varies across animal species, which has stimulated research to investigate factors that might explain this variation, and to investigate underlying affective responses. Among great apes, IA is most often studied in chimpanzees. Here, we investigate IA in bonobos, a reputedly tolerant and cooperative species for which few IA studies are available. We describe how bonobos respond to receiving less preferred rewards than a partner in a token exchange task. We show that bonobos respond to receiving less preferred rewards by refusing tokens and rewards, and by leaving the experimental area. Bonobos never refused a trial when receiving preferred rewards, and thus showed no advantageous IA. We also investigate the variability in the disadvantageous IA response on a dyadic level, because the level of IA is expected to vary, depending on characteristics of the dyad. Like in humans and chimpanzees, we show that the tolerance towards inequity was higher in bonobo dyads with more valuable relationships. To study the affective component of IA, we included behavioral and physiological measures of arousal: a displacement behavior (rough self-scratching) and changes in salivary cortisol levels. Both measures of arousal showed large variability, and while analyses on rough self-scratching showed no significant effects, salivary cortisol levels seemed to be lower in subjects that received less than their partner, but higher in subjects that received more than their partner, albeit that both were not significantly different from the equity condition. This suggests that although overcompensated bonobos showed no behavioral response, they might be more aroused. Our data support the cooperation hypothesis on an interspecific and intraspecific level. They show inequity aversion in bonobos, a reputedly cooperative species, and suggest that the variability in IA in bonobos can be explained by their socioecology. Most successful cooperative interactions happen between mothers and their sons and among closely bonded females. The limited need to monitor the partners' investment within these dyads can result in a higher tolerance towards inequity. We therefore suggest future studies to consider relevant socioecological characteristics of the species when designing and analyzing IA studies.     

Locomotor behavior of Pan paniscus in Zaire

The locomotor behavior of Pan paniscus was studied over a four-week period in Equateur, Republic of Zaire. Bonobos were found to be both arboreal and terrestrial in their daily activities. In the trees adult bonobos are basically quadrupedal, but they also have significant components of armswinging, diving, leaping, and bipedalism in their locomotor repertoire.     

Behavioral laterality in captive bonobos (Pan paniscus): Replication and extension

We report observational data on behavioral laterality in 10 captive bonobos (Pan paniscus)at the San Diego Zoo. The unimanual measures include carrying, leading limb in locomotion, self-touching, face-touching, reaching, and gestures. We also recorded bimanual feeding in these subjects. A significant population level left-hand bias exists for carrying. Right-hand biases occur for leading limb in locomotion and gestures. During bimanual feeding, the bonobos hold food items with the left hand while feeding with the right hand. Overall, bonobos exhibit behavioral asymmetries that are similar to previous findings in other pongid ape species. The asymmetries in gestures and bimanual feeding represent novel findings with theoretical implications for the origins of tool use and language.     

Structure and use of distance calls in wild bonobos (Pan paniscus)

We report the physical structure and use of a distance call (high-hoot) by wild bonobos (Pan paniscus).Although spectrographic analyses reveal high structural variability, the total sample can be subdivided according to the composition of units—the presence or absence of an initial segment—and the range of the lowest harmonic. Analyses of samples from male—female pairs,vocalizing simultaneously and in close proximity, reveal that both animals utter calls in more or less precise temporal alternation but with different spectral ranges. Whether these differences are gender-specific or related to other factors, such as age or the social relations between particular individuals, is not clear. We suggest that (a) individuals of the same party may coordinate their vocal activity on both the temporal and the spectral level and (b) high hootings stimulate emission of equal vocalizations by members of other parties and may increase cohesion among community members. Comparison of a restricted number of spectrograms from known individuals indicates that bonobos may be able to adjust spectral parameters of one type of distance calls (high- hoot) according to corresponding calls of conspecifics.     

Association and social interactions between strangers and residents in bonobos (Pan paniscus)

This study reports on close spatial association and repeated behavioural interactions between two strange adult male bonobos with residents of another community. Over a period of 12 months one of the two males developed friendly social relations to some of the females and other residents, which were indistinguishable from those existing between co-residents. Aggression by resident males against the strangers decreased but the former remained intolerant. The strange males appeared at a time when the number of adult resident males was lower as in the years before and when the adult sex ratio (number of adult females per male) was higher as in the years before. Using definitions from studies on dispersal patterns of male gorillas (Harcourt, 1978) and female bonobos (Furuichi, 1989) the spatial association between the two strange males and residents could be described as male transfer.