Segment and joint angles of hind limb during bipedal and quadrupedal walking of the bonobo (Pan paniscus)

We describe segment angles (trunk, thigh, shank, and foot) and joint angles (hip, knee, and ankle) for the hind limbs of bonobos walking bipedally ("bent-hip bent-knee walking," 17 sequences) and quadrupedally (33 sequences). Data were based on video recordings (50 Hz) of nine subjects in a lateral view, walking at voluntary speed. The major differences between bipedal and quadrupedal walking are found in the trunk, thigh, and hip angles. During bipedal walking, the trunk is approximately 33-41 degrees more erect than during quadrupedal locomotion, although it is considerably more bent forward than in normal human locomotion. Moreover, during bipedal walking, the hip has a smaller range of motion (by 12 degrees ) and is more extended (by 20-35 degrees ) than during quadrupedal walking. In general, angle profiles in bonobos are much more variable than in humans. Intralimb phase relationships of subsequent joint angles show that hip-knee coordination is similar for bipedal and quadrupedal walking, and resembles the human pattern. The coordination between knee and ankle differs much more from the human pattern. Based on joint angles observed throughout stance phase and on the estimation of functional leg length, an efficient inverted pendulum mechanism is not expected in bonobos.     

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.     

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.     

Reconciliation and consolation in captive bonobos (Pan paniscus)

Although reconciliation in bonobos (Pan paniscus) has previously been described, it has not been analyzed heretofore by the postconflict (PC) match-control (MC) method. Furthermore, although reconciliation has been investigated before in this species, consolation has not. In this study we analyzed agonistic and affiliative contacts in all sex-class combinations to clarify and reevaluate the occurrence of reconciliation in bonobos via the PC-MC method. We also investigated the occurrence of consolation by analyzing the victims' triadic contact tendency (TCT), the influence of the sex of victims, and the relative occurrence of consolation and reconciliation. We collected 167 pairs of PC-MC observations in a captive group of bonobos (in Apeldoorn, The Netherlands). The conciliatory tendency (CCT) we obtained was tendentially lower than the mean value previously found for Yerkes captive chimpanzees. Close relationships, which were present in all female-female (FF) and some male-female (MF) dyads, positively affected reconciliation rates. When only adult PC-MC pairs (157) were considered, the mean TCTs and CCTs did not differ significantly. When we focused on types of PC affiliative contact, in the case of consolation we found a striking preference for sociosexual patterns. As to the relative occurrence of consolation and reconciliation, the highest level of the former was found in the absence of the latter. When reconciliation took place, consolation generally preceded it, suggesting that consolation may be a substitutive behavior. Our findings suggest that even if reconciliation remains the best option, consolation may be an alternative substitute for reconciliation that is used to buffer the tension originating from an unresolved conflict. Reconciliation and consolation are complex phenomena that are probably related to the life history of a group. Given that few studies have been conducted on this subject, we can not at this time make any generalizations regarding conflict resolution in certain species by comparing results among studies.     

Reevaluation of dominance hierarchy in bonobos (Pan paniscus)

While dominance relationships have been widely studied in chimpanzees, in bonobos, dominance style and linearity of hierarchy are still under debate. In fact, some authors stated that bonobo hierarchy is nonlinear/ill-defined, while others claimed that it is fairly linear. In this paper, we test the hypothesis that a shift in group composition determines changes in linearity of hierarchy. To test this hypothesis, we collected data on one of the largest captive groups in the world, in the Apenheul Primate Park (The Netherlands). We investigated the linearity of the hierarchy in two different periods, with a shifting group composition. We used the corrected Landau's index and David's scores to estimate which animals were most dominant. The major overall result of our study is that hierarchy is fairly nonlinear in this group: during the first study period (eight adults), the hierarchy was nonlinear, whereas during the second one (six adults), it failed to reach statistical linearity. We argue that the reduction of the number of adults is the principal factor affecting linearity. We also found that dominance interactions were evenly distributed across sex classes in both study periods. Furthermore, no correlation was observed between age/body weight and rank. As for the overall dominance relationship between males and females, our results suggest that there is no exclusive female dominance in the Apenheul group. The dominance style of bonobos may be loose and differentially expressed in diverse groups or in the same group, along with shifting conditions.     

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.     

Comparing maternal styles in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes)

Studies on Cercopithecine primate maternal styles, using factor analysis on a set of maternal behaviors, commonly render two factors that describe separate dimensions of maternal behavior: protectiveness and rejection. The aims of this study were to 1) investigate whether this method for determining maternal styles in Cercopithecine species can be applied to bonobos (Pan paniscus) and chimpanzees (Pan troglodytes), 2) determine whether they follow the same pattern, and 3) assess whether species differences in maternal style are apparent. We performed a factor analysis on nine maternal behaviors using data on eight mother-infant pairs of each species. This resulted in three factors: protectiveness, distance, and refusal. Protectiveness is positively correlated with time spent in ventral contact, making contact, approaching, and restraining. Distance is positively related with breaking contact and leaving. Refusal is positively correlated with rejecting and nipple-rejecting. The pattern of protectiveness corresponds with the pattern found in Cercopithecine species, suggesting a high consistency of this dimension across species and higher taxa. The retention of the other two factors indicates that in the Pan species, breaking contact and leaving represent another dimension, apart from rejecting and nipple-rejecting, which usually fall under one dimension in Cercopithecine species. An interspecific comparison of the factor scores for each dimension of maternal behavior reveals that, on average, bonobos and chimpanzees score equally on protectiveness. Scores on distance increase positively with infant age in chimpanzees, and negatively in bonobos, and on average bonobos have higher scores on refusal. These interspecies differences in maternal style are discussed in the light of interspecies differences in infant development, infant vulnerability to aggression, interbirth intervals, and female sociality.     

Dynamic plantar pressure distribution during terrestrial locomotion of bonobos (Pan paniscus)

We collected high-resolution plantar pressure distributions of seven bonobos during terrestrial bipedal and quadrupedal locomotion (N = 146). Functional foot length, degree of hallux abduction, and total contact time were determined, and plots, showing pressure as a function of time for six different foot regions, were generated. We also studied five adult humans for comparison (N = 13). Both locomotion types of the bonobo show a large variation in plantar pressure distributions, which could be due to the interference of instantaneous behavior with locomotion and differences in walking speed and body dimensions. The heel and the lateral midfoot typically touch down simultaneously at initial ground contact in bipedal and quadrupedal walking of bonobos, in contrast with the typical heel-strike of human bipedalism. The center of pressure follows a curved course during quadrupedalism, as a consequence of the medial weight transfer during mid-stance. Bipedal locomotion of bonobos is characterized by a more plantar positioning of the feet and by a shorter contact time than during quadrupedal walking, according to a smaller stride and step length at a higher frequency. We observed a varus position of the foot with an abducted hallux, which likely possesses an important sustaining and stabilizing function during terrestrial locomotion.     

Evidence of leopard predation on bonobos (Pan paniscus)

Current models of social organization assume that predation is one of the major forces that promotes group living in diurnal primates. As large body size renders some protection against predators, gregariousness of great apes and other large primate species is usually related to other parameters. The low frequency of observed cases of nonhuman predation on great apes seems to support this assumption. However, recent efforts to study potential predator species have increasingly accumulated direct and indirect evidence of predation by leopards (Panthera pardus) on chimpanzees and gorillas. The following report provides the first evidence of predation by a leopard on bonobos (Pan paniscus).     

Cannibalism in wild bonobos (Pan paniscus) at Lui Kotale

We describe the cannibalization of an infant bonobo (circa 2.5 years old) at Lui Kotale, in the Democratic Republic of Congo. The infant died of unknown causes and was consumed by several community members including its mother and an older sibling one day after death. Certain features concerning the pattern of consumption fit in with previously observed episodes of cannibalism in Pan, whereas others, such as the mother's participation in consuming the body, are notable. The incident suggests that filial cannibalism among apes need not be the result of nutritional or social stress and does not support the idea that filial cannibalism is a behavioral aberration. Am. J. Primatol. 72:509–514, 2010. © 2010 Wiley‐Liss, Inc.     

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.     

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.     

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.     

Rivers influence the population genetic structure of bonobos (Pan paniscus)

Bonobos are large, highly mobile primates living in the relatively undisturbed, contiguous forest south of the Congo River. Accordingly, gene flow among populations is assumed to be extensive, but may be impeded by large, impassable rivers. We examined mitochondrial DNA control region sequence variation in individuals from five distinct localities separated by rivers in order to estimate relative levels of genetic diversity and assess the extent and pattern of population genetic structure in the bonobo. Diversity estimates for the bonobo exceed those for humans, but are less than those found for the chimpanzee. All regions sampled are significantly differentiated from one another, according to genetic distances estimated as pairwise FSTs, with the greatest differentiation existing between region East and each of the two Northern populations (N and NE) and the least differentiation between regions Central and South. The distribution of nucleotide diversity shows a clear signal of population structure, with some 30% of the variance occurring among geographical regions. However, a geographical patterning of the population structure is not obvious. Namely, mitochondrial haplotypes were shared among all regions excepting the most eastern locality and the phylogenetic analysis revealed a tree in which haplotypes were intermixed with little regard to geographical origin, with the notable exception of the close relationships among the haplotypes found in the east. Nonetheless, genetic distances correlated with geographical distances when the intervening distances were measured around rivers presenting effective current-day barriers, but not when straight-line distances were used, suggesting that rivers are indeed a hindrance to gene flow in this species.     

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.     

Problems and experiences in performing artificial insemination in bonobos (Pan paniscus)

A report is given on the problems and the procedure of artificial insemination in the bonobo (Pan paniscus). In addition, the different possibilities and methods of the process of collecting sperm, its conservation, and determining the time of ovulation are discussed, as well as the various insemination techniques and their usage under practical conditions in zoological gardens.     

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.