Is birth attendance a uniquely human feature? New evidence suggests that Bonobo females protect and support the parturient

Birth attendance has been proposed as a distinguishing feature of humans (Homo sapiens) and it has been linked to the difficulty of the delivery process in our species. Here, we provide the first quantitative study based on video-recordings of the social dynamics around three births in captive bonobos (Pan paniscus), human closest living relative along with the chimpanzee. We show that the general features defining traditional birth attendance in humans can also be identified in bonobos. As in humans, birth in bonobos was a social event, where female attendants provided protection and support to the parturient until the infant was born. Moreover, bystander females helped the parturient during the expulsive phase by performing manual gestures aimed at holding the infant. Our results on bonobos question the traditional view that the “obligatory” need for assistance was the main driving force leading to sociality around birth in our species. Indeed, birth in bonobos is not hindered by physical constraints and the mother is self-sufficient in accomplishing the delivery. Although further studies are needed both in captivity and in the wild, we suggest that the similarities observed between birth attendance in bonobos and humans might be related to the high level of female gregariousness in these species. In our view, the capacity of unrelated females to form strong social bonds and cooperate could have represented the evolutionary pre-requisite for the emergence of human midwifery.     

Chimpanzees and bonobos distinguish between risk and ambiguity

Although recent research has investigated animal decision-making under risk, little is known about how animals choose under conditions of ambiguity when they lack information about the available alternatives. Many models of choice behaviour assume that ambiguity does not impact decision-makers, but studies of humans suggest that people tend to be more averse to choosing ambiguous options than risky options with known probabilities. To illuminate the evolutionary roots of human economic behaviour, we examined whether our closest living relatives, chimpanzees (Pan troglodytes) and bonobos (Pan paniscus), share this bias against ambiguity. Apes chose between a certain option that reliably provided an intermediately preferred food type, and a variable option that could vary in the probability that it provided a highly preferred food type. To examine the impact of ambiguity on ape decision-making, we interspersed trials in which chimpanzees and bonobos had no knowledge about the probabilities. Both species avoided the ambiguous option compared with their choices for a risky option, indicating that ambiguity aversion is shared by humans, bonobos and chimpanzees.     

Observations on the meat-eating behavior of wild bonobos (Pan paniscus) at Wamba,Republic of Zaire

Meat-eating behavior of wild bonobos (Pan paniscus) was witnessed on two occasions at Wamba, Republic of Zaire. Only flying squirrels were observed to be eaten by the bonobos. Several bonobos gathered around the possessor of the meat and showed interest in the meat on all occasions. Begging behavior was noted on one of the two occasions, but the possessor of the meat ignored it. No sharing of meat was seen on either occasion. The exclusive targets of hunting by bonobos are apparently small mammals, such as flying squirrels and infant duikers, since evidence of meat eating by wild bonobos, which have been studied for more than fifteen years, has been restricted to these mammals. The bonobos at Wamba may have a specialized “prey image”, as in the case of the chimpanzees (Pan troglodytes) of the Tai forest, and certain medium-sized or small mammals may not conform to this image.     

The Right Time to Happen: Play Developmental Divergence in the Two Pan Species

Bonobos, compared to chimpanzees, are highly motivated to play as adults. Therefore, it is interesting to compare the two species at earlier developmental stages to determine how and when these differences arise. We measured and compared some play parameters between the two species including frequency, number of partners (solitary, dyadic, and polyadic play), session length, and escalation into overt aggression. Since solitary play has a role in developing cognitive and physical skills, it is not surprising that chimpanzees and bonobos share similar developmental trajectories in the motivation to engage in this activity. The striking divergence in play developmental pathways emerged for social play. Infants of the two species showed comparable social play levels, which began to diverge during the juvenile period, a ‘timing hotspot’ for play development. Compared to chimpanzees, social play sessions in juvenile bonobos escalated less frequently into overt aggression, lasted longer, and frequently involved more than two partners concurrently (polyadic play). In this view, play fighting in juvenile bonobos seems to maintain a cooperative mood, whereas in juvenile chimpanzees it acquires more competitive elements. The retention of juvenile traits into adulthood typical of bonobos can be due to a developmental delay in social inhibition. Our findings show that the divergence of play ontogenetic pathways between the two Pan species and the relative emergence of play neotenic traits in bonobos can be detected before individuals reach sexual maturity. The high play motivation showed by adult bonobos compared to chimpanzees is probably the result of a long developmental process, rooted in the delicate transitional phase, which leads subjects from infancy to juvenility.     

Bonobos Share with Strangers

Humans are thought to possess a unique proclivity to share with others – including strangers. This puzzling phenomenon has led many to suggest that sharing with strangers originates from human-unique language, social norms, warfare and/or cooperative breeding. However, bonobos, our closest living relative, are highly tolerant and, in the wild, are capable of having affiliative interactions with strangers. In four experiments, we therefore examined whether bonobos will voluntarily donate food to strangers. We show that bonobos will forego their own food for the benefit of interacting with a stranger. Their prosociality is in part driven by unselfish motivation, because bonobos will even help strangers acquire out-of-reach food when no desirable social interaction is possible. However, this prosociality has its limitations because bonobos will not donate food in their possession when a social interaction is not possible. These results indicate that other-regarding preferences toward strangers are not uniquely human. Moreover, language, social norms, warfare and cooperative breeding are unnecessary for the evolution of xenophilic sharing. Instead, we propose that prosociality toward strangers initially evolves due to selection for social tolerance, allowing the expansion of individual social networks. Human social norms and language may subsequently extend this ape-like social preference to the most costly contexts.     

Oxytocin and Vasopressin Receptor Gene Variation as a Proximate Base for Inter- and Intraspecific Behavioral Differences in Bonobos and Chimpanzees

Recent literature has revealed the importance of variation in neuropeptide receptor gene sequences in the regulation of behavioral phenotypic variation. Here we focus on polymorphisms in the oxytocin receptor gene (OXTR) and vasopressin receptor gene 1a (Avpr1a) in chimpanzees and bonobos. In humans, a single nucleotide polymorphism (SNP) in the third intron of OXTR (rs53576 SNP (A/G)) is linked with social behavior, with the risk allele (A) carriers showing reduced levels of empathy and prosociality. Bonobos and chimpanzees differ in these same traits, therefore we hypothesized that these differences might be reflected in variation at the rs53576 position. We sequenced a 320 bp region surrounding rs53576 but found no indications of this SNP in the genus Pan. However, we identified previously unreported SNP variation in the chimpanzee OXTR sequence that differs from both humans and bonobos. Humans and bonobos have previously been shown to have a more similar 5′ promoter region of Avpr1a when compared to chimpanzees, who are polymorphic for the deletion of ∼360 bp in this region (+/− DupB) which includes a microsatellite (RS3). RS3 has been linked with variation in levels of social bonding, potentially explaining part of the interspecies behavioral differences found in bonobos, chimpanzees and humans. To date, results for bonobos have been based on small sample sizes. Our results confirmed that there is no DupB deletion in bonobos with a sample size comprising approximately 90% of the captive founder population, whereas in chimpanzees the deletion of DupB had the highest frequency. Because of the higher frequency of DupB alleles in our bonobo population, we suggest that the presence of this microsatellite may partly reflect documented differences in levels of sociability found in bonobos and chimpanzees.     

Distribution of terrestrial herbaceous vegetation and its consumption by Pan paniscus in the Lomako Forest,Zaire

Data available on behavior and morphology of Pan paniscus (bonobos) suggest that terrestrial herbaceous vegetation (THV) is an important component of their diet and that it may be preferred by bonobos to a greater extent than by chimpanzees (Pan troglodytes). It has also been reported that THV is ubiquitously distributed in the lowland rain forests inhabited by bonobos. These data suggest that THV exploitation may be causally related to the evolution of the more cohesive social system found in bonobos compared to that of chimpanzees. Here, we present data that quantify the spatial distribution of THV in the Lomako Forest, an analysis of the nutrient content of the plant parts commonly consumed, and patterns of THV consumption in relation to its distribution. The data clearly demonstrate that THV, and particularly Haumania liebrechtsiana (Marantaceae), is ubiquitously distributed as previously suggested. However, THV feeding patches are rare because of distinct feeding preferences. Bonobos preferentially choose H. liebrechtsiana over other species of THV, choose patches with larger stems, and, within patches, choose larger stems over smaller stems. The plant parts chosen are high in proteins and relatively low in carbohydrates. Given the selectivity of the study population and the patchy distribution of THV, it is unlikely that THV has been responsible for the evolution of the unique social system reported for bonobos. Data presented on party size are consistent with this conclusion.     

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.     

Interactions between zoo‐housed great apes and local wildlife

Although there are published reports of wild chimpanzees, bonobos, and orangutans hunting and consuming vertebrate prey, data pertaining to captive apes remain sparse. In this survey‐based study, we evaluate the prevalence and nature of interactions between captive great apes and various indigenous wildlife species that range into their enclosures in North America. Our hypotheses were threefold: (a) facilities housing chimpanzees will report the most frequent and most aggressive interactions with local wildlife; (b) facilities housing orangutans and bonobos will report intermediate frequencies of these interactions with low levels of aggression and killing; and (c) facilities housing gorillas will report the lowest frequency of interactions and no reports of killing local wildlife. Chimpanzees and bonobos demonstrated the most aggressive behavior toward wildlife, which matched our predictions for chimpanzees, but not bonobos. This fits well with expectations for chimpanzees based on their natural history of hunting and consuming prey in wild settings, and also supports new field data on bonobos. Captive gorillas and orangutans were reported to be much less likely to chase, catch and kill wildlife than chimpanzees and bonobos. Gorillas were the least likely to engage in aggressive interactions with local wildlife, matching our predictions based on natural history. However unlike wild gorillas, captive gorillas were reported to kill (and in one case, eat) local wildlife. These results suggest that some behavioral patterns seen in captive groups of apes may be useful for modeling corresponding activities in the wild that may not be as easily observed and quantified. Furthermore, the data highlight the potential for disease transmission in some captive settings, and we outline the associated implications for ape health and safety. Am. J. Primatol. 71:458–465, 2009. © 2009 Wiley‐Liss, Inc.     

Hand Preferences for Bimanual Coordination in 77 Bonobos (<Emphasis Type="Italic">Pan paniscus</Emphasis>): Replication and Extension

The literature on manual laterality in nonhuman primates provides inconsistent and inconclusive findings and is plagued by methodological issues (e.g., small samples, inconsistency in methods, inappropriate measures) and gaps. Few data are available on bonobos and these are only from small samples and for relatively simple tasks. We examined laterality in a large sample of bonobos for a complex task. We tested 48 bonobos from Lola Ya Bonobo sanctuary (DR Congo) in an extension of our previous study of 29 bonobos from 3 European zoos. We assessed hand preferences using the tube task, which involves bimanual coordination: one hand extracts food from a tube that is held by the other hand. This task is a good measure of laterality and it has been used in other studies. We recorded events (frequency) and independent bouts of food extraction. We found significant manual laterality, which was not influenced by the settings or rearing history. We observed little effect of sex and found an influence of age, with greater right hand use in adults. The laterality was marked, with strong preferences and most individuals being lateralized (when analyzing frequency). We found individual preferences, with no group-level bias, even when we combined the data from the sanctuary and the zoos to enlarge the sample to 77. These first data, for a complex task and based on a large sample, are consistent with previous findings in bonobos and in other nonhuman primate species for a variety of tasks. They suggest that, despite particular features in terms of proximity to humans, language and bipedalism, bonobos do not display a laterality that is more marked or more similar to human handedness compared to that of other nonhuman primate species.     

Evidence for Divergence in Populations of Bonobos (Pan paniscus) in the Lomami-Lualaba and Kasai-Sankuru Regions Based on Preliminary Analysis of Craniodental Variation

Historical climatic events and riverine barriers influence the distribution of primates. The River Congo exerts the most significant influence on primate distribution in equatorial Africa, but the extent to which the inner basin of the Congo provided a refuge against Plio-Pleistocene climatic fluctuation is poorly understood. In this study we use cranial and dental morphometrics to examine how riverine barriers affect population patterns in bonobos (Pan paniscus). Bonobos and chimpanzees (Pan troglodytes) are sister species and share the distinction of being the closest evolutionary relatives of humans, yet comparatively little is known about bonobo morphological diversity. We selected 55 adult bonobo crania with well-preserved postcanine dentitions and divided them into regions separated by the rivers Lukenie, Kasai, Lomami, and Lualaba. We found good discrimination among these regions in cranial and dental metrics, but whereas the discriminant functions from cranial metrics were statistically significant, the discriminant functions from dental metrics were not. Mean classification accuracy was 89% for craniometrics, and ranged between 72% and 93% for dental metrics. On average 84–97% of phenetic variation was encountered within regions. Our results mirror molecular studies in suggesting that bonobos are characterized by a long-term stable demographic history allowing strong gene flow between regions and precluding drift and population differentiation. There are some indications that the bonobos from the Lomami-Lualaba and the Kasai-Sankuru regions are divergent, but modest sample sizes do not allow us to be conclusive. We would welcome the opportunity to work with field researchers to augment our sample sizes and reanalyze our data.     

Social grooming among wild bonobos (Pan paniscus) at Wamba in the Luo Scientific Reserve, DR Congo, with special reference to the formation of grooming gatherings

Chimpanzees (Pan troglodytes) groom in gatherings in which many individuals may be connected via multiple chains of grooming and they often exchange partners with each other. They sometimes groom another while receiving grooming; that is, one animal can play two roles (i.e., groomer and groomee) simultaneously. Although this feature of chimpanzees is notable from the viewpoint of the evolution of human sociality, information on our other closest living relative, the bonobo (Pan paniscus), is still lacking. In this study, I describe grooming interactions of bonobos at Wamba in the Luo Scientific Reserve, Democratic Republic of the Congo (DR Congo), with a particular focus on the formation of grooming gatherings. Like chimpanzees, the bonobos also performed mutual grooming (two individuals grooming each other simultaneously) and polyadic grooming (three or more individuals). However, unlike chimpanzees, these sessions lasted for only a short time. Bonobos rarely groomed another while receiving grooming. Because social grooming occurred not only in trees but also in open spaces, including treefall gaps, the conditions did not necessarily limit the opportunity to make multiple chains of grooming. However, bonobos also engaged in social grooming in different ways from chimpanzees; That is, many individuals were involved simultaneously at a site, in which they separated for dyadic grooming. Some cases clearly showed that bonobos preferred a third party not to join while grooming in a dyad, suggesting that bonobos have a preference for grooming in dyads and that immature individuals formed the preference that was shared among adults while growing up. Most members of the study group ranged together during the majority of the study period. Although bonobos show a fission–fusion grouping pattern, when group members frequently encounter one another on a daily basis, they may not be motivated to form multiple grooming chains at this site, as do chimpanzees.     

Coprophagy in wild bonobos (<Emphasis Type="Italic">Pan paniscus</Emphasis>) at Wamba in the Democratic Republic of the Congo: a possibly adaptive strategy?

Four cases of coprophagy and two cases of fecal inspection were identified during the 1142 h of observing wild bonobos at Wamba in the Luo Scientific Reserve in the Democratic Republic of the Congo. At least 5 females in the study group practiced coprophagy and/or fecal inspection. According to our daily behavioral observations, boredom and stress, insufficient roughage, and the search for essential nutrients could not explain the coprophagy. Several episodes observed in this study indicated that bonobos might have sought and ingested certain valuable food items, such as hard Dialium seeds, in feces during relatively lean seasons. Although coprophagy occurred only rarely among wild bonobos, this practice appeared to represent a possibly adaptive feeding strategy during periods of food scarcity rather than a behavioral abnormality.     

Do bonobos copulate more frequently and promiscuously than chimpanzees?

The copulatory activities of bonobos (Pan paniscus) of Wamba, Zaire, were compared with those of chimpanzees (P. troglodytes schweinfurthii) of Mahale, Tanzania. The copulation rates of adult male bonobos were equal to or lower than those of adult male chimpanzees. The copulation rates of adult female bonobos were approximately equal to those of adult female chimpanzees who were in maximal genital swelling, but it should be much higher than those of the adult female chimpanzees throughout the birth interval. The copulation rates of adolescent male bonobos were lower than those of adolescent male chimpanzees, whereas the copulation rates of adolescent female bonobos were much higher than those of adolescent female chimpanzees. It was suggested that the bonobos of Wamba did not copulate more promiscuously than did the chimpanzees of Mahale. The female bonobos may show “receptivity”, whereas female chimpanzees may show rather “proceptivity”.     

The Human Semicircular Canals Orientation Is More Similar to the Bonobos than to the Chimpanzees

For some traits, the human genome is more closely related to either the bonobo or the chimpanzee genome than they are to each other. Therefore, it becomes crucial to understand whether and how morphostructural differences between humans, chimpanzees and bonobos reflect the well known phylogeny. Here we comparatively investigated intra and extra labyrinthine semicircular canals orientation using 260 computed tomography scans of extant humans (Homo sapiens), bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Humans and bonobos proved more similarities between themselves than with chimpanzees. This finding did not fit with the well established chimpanzee – bonobo monophyly. One hypothesis was convergent evolution in which bonobos and humans produce independently similar phenotypes possibly in response to similar selective pressures that may be associated with postural adaptations. Another possibility was convergence following a “random walk” (Brownian motion) evolutionary model. A more parsimonious explanation was that the bonobo-human labyrinthine shared morphology more closely retained the ancestral condition with chimpanzees being subsequently derived. Finally, these results might be a consequence of genetic diversity and incomplete lineage sorting. The remarkable symmetry of the Semicircular Canals was the second major finding of this article with possible applications in taphonomy. It has the potential to investigate altered fossils, inferring the probability of post-mortem deformation which can lead to difficulties in understanding taxonomic variation, phylogenetic relationships, and functional morphology.     

Non-antagonistic relations between wild bonobos and two species of guenons

Interspecific relations between wild bonobos (Pan paniscus) and two species of guenons (Cercopithecus wolfi andC. ascanius) were studied at Wamba in the Central Zaire Basin from September 1989 to January 1990. Data on the guenons were collected while following parties of bonobos or when searching for them. The guenons were observed directly 59 times during the study period. In about half of these observations, the guenons were found within 20 m from the bonobo parties. The encounters between the bonobos and the guenons sometimes lasted over an hour. The guenons mainly initiated the encounters by approaching the bonobos. During the encounters, no aggressive interactions were observed between the bonobos and the guenons. Evidence of hunting by wild bonobos has been restricted to small mammals, and there has been no evidence of hunting of primates by wild bonobos. These findings and the results of the present study strongly suggest that wild bonobos do not hunt sympatric primates.     

Tool use behavior in three wild bonobo communities at Kokolopori

Comparative studies on tool technologies in extant primates, especially in our closest living relatives, offer a window into the evolutionary foundations of tool use in hominins. Whereas chimpanzee tool technology is well studied across populations, the scarcity of described tool technology in wild populations of our other closest living relative, the bonobo, is a mystery. Here we provide a first report of the tool use repertoire of the Kokolopori bonobos and describe in detail the use of leaf-umbrellas during rainfall, with the aim to improve our knowledge of bonobo tool use capacity in the wild. The tool use repertoire of the Kokolopori bonobos was most similar to that of the nearby population of Wamba and comprised eight behaviors, none in a foraging context. Further, over a 6-month period we documented 44 instances of leaf-umbrella use by 22 individuals from three communities, suggesting that this behavior is habitual. Most leaf-umbrella tool users were adult females, and we observed a nonadult using a leaf-umbrella on only a single occasion. While the study and theory of tool technologies is often based on the use of tools in foraging tasks, tool use in bonobos typically occurs in nonforaging contexts across populations. Therefore, incorporating both foraging and nonforaging contexts into our theoretical framework is essential if we wish to advance our understanding of the evolutionary trajectories of tool technology in humans.     

Testing the Effect of Medical Positive Reinforcement Training on Salivary Cortisol Levels in Bonobos and Orangutans

The management of captive animals has been improved by the establishment of positive reinforcement training as a tool to facilitate interactions between caretakers and animals. In great apes, positive reinforcement training has also been used to train individuals to participate in simple medical procedures to monitor physical health. One aim of positive reinforcement training is to establish a relaxed atmosphere for situations that, without training, might be very stressful. This is especially true for simple medical procedures that can require animals to engage in behaviours that are unusual or use unfamiliar medical devices that can be upsetting. Therefore, one cannot exclude the possibility that the training itself is a source of stress. In this study, we explored the effects of medical positive reinforcement training on salivary cortisol in two groups of captive ape species, orangutans and bonobos, which were familiar to this procedure. Furthermore, we successfully biologically validated the salivary cortisol assay, which had already been validated for bonobos, for orangutans. For the biological validation, we found that cortisol levels in orangutan saliva collected during baseline conditions were lower than in samples collected during three periods that were potentially stressful for the animals. However, we did not find significant changes in salivary cortisol during medical positive reinforcement training for either bonobos or orangutans. Therefore, for bonobos and orangutans with previous exposure to medical PRT, the procedure is not stressful. Thus, medical PRT provides a helpful tool for the captive management of the two species.     

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.