Zanna Clay

A comparison of bonobo and chimpanzee tool use: evidence for a female bias in the Pan lineage

Chimpanzees, Pan troglodytes, are the most sophisticated tool-users among all nonhuman primates. From an evolutionary perspective, it is therefore puzzling that the tool use behaviour of their closest living primate relative, the bonobo, Pan paniscus, has been described as particularly poor. However, only a small number of bonobo groups have been studied in the wild and only over comparably short periods. Here, we show that captive bonobos and chimpanzees are equally diverse tool-users in most contexts. Our observations illustrate that tool use in bonobos can be highly complex and no different from what has been described for chimpanzees. The only major difference in the chimpanzee and bonobo data was that bonobos of all age–sex classes used tools in a play context, a possible manifestation of their neotenous nature. We also found that female bonobos displayed a larger range of tool use behaviours than males, a pattern previously described for chimpanzees but not for other great apes. Our results are consistent with the hypothesis that the female-biased tool use evolved prior to the split between bonobos and chimpanzees.

Bonobos Respond to Distress in Others: Consolation across the Age Spectrum

How animals respond to conflict provides key insights into the evolution of socio-cognitive and emotional capacities. Evidence from apes has shown that, after social conflicts, bystanders approach victims of aggression to offer stress-alleviating contact behavior, a phenomenon known as consolation. This other-orientated behavior depends on sensitivity to the others emotional state, whereby the consoler acts to ameliorate the others situation. We examined post-conflict interactions in bonobos (Pan paniscus) to identify the determinants of consolation and reconciliation. Thirty-six semi-free bonobos of all ages were observed at the Lola ya Bonobo Sanctuary, DR Congo, using standardized Post-conflict/Matched Control methods. Across age and sex classes, bonobos consoled victims and reconciled after conflicts using a suite of affiliative and socio-sexual behaviors including embracing, touching, and mounting. Juveniles were more likely to console than adults, challenging the assumption that comfort-giving rests on advanced cognitive mechanisms that emerge only with age. Mother-reared individuals were more likely to console than orphans, highlighting the role of rearing in emotional development. Consistent with previous studies, bystanders were more likely to console relatives or closely bonded partners. Effects of kinship, affiliation and rearing were similarly indicated in patterns of reconciliation. Nearby bystanders were significantly more likely to contact victims than more distal ones, and consolation was more likely in non-food contexts than during feeding. The results did not provide convincing evidence that bystander contacts served for self-protection or as substitutes for reconciliation. Overall, results indicate that a suite of social, developmental and contextual factors underlie consolation and reconciliation in bonobos and that a sensitivity to the emotions of others and the ability to provide appropriate consolatory behaviors emerges early in development.

Food-associated vocalizations in mammals and birds: what do these calls really mean?

Alarm calls and food-associated calls from a diverse range of species are said to be functionally referential, in that receivers can use these sounds to predict environmental events in the absence of other contextual cues. The evolutionary driver for referential alarm calls has been hypothesized to be the mutually incompatible escape behaviours required to avoid different predators. However, some species produce acoustically distinctive and referential alarm calls but do not show highly referential abilities in other domains. We examined whether food-associated calls in many species are likely to be functionally referential and whether they specifically communicate about characteristic features of food. Foodassociated calls are given in both feeding and nonfeeding contexts, and the types of information contained vary greatly. Most species do not produce unique calls for different foods; more common is variation in the call rate, which suggests that call structure reflects the callers’ internal state rather than the food type. We also examined the ultimate function of food-associated calls to evaluate whether there is a unifying explanation for the evolution of functionally referential food calls. Based on the literature, there does not appear to be a unifying function. In conclusion, while functionally referential foodassociated calls have been convincingly demonstrated in a few species, it is more common for these vocalizations to reflect arousal rather than additionally providing specific referential information about the feeding event. At this point, there is no compelling hypothesis to explain the evolution of functionally referential food-associated calls. Given the multiple functions of food-associated signals, we should not expect a unitary explanation.

Bonobos Extract Meaning from Call Sequences

Studies on language-trained bonobos have revealed their remarkable abilities in representational and communication tasks. Surprisingly, however, corresponding research into their natural communication has largely been neglected. We address this issue with a first playback study on the natural vocal behaviour of bonobos. Bonobos produce five acoustically distinct call types when finding food, which they regularly mix together into longer call sequences. We found that individual call types were relatively poor indicators of food quality, while context specificity was much greater at the call sequence level. We therefore investigated whether receivers could extract meaning about the quality of food encountered by the caller by integrating across different call sequences. We first trained four captive individuals to find two types of foods, kiwi (preferred) and apples (less preferred) at two different locations. We then conducted naturalistic playback experiments during which we broadcasted sequences of four calls, originally produced by a familiar individual responding to either kiwi or apples. All sequences contained the same number of calls but varied in the composition of call types. Following playbacks, we found that subjects devoted significantly more search effort to the field indicated by the call sequence. Rather than attending to individual calls, bonobos attended to the entire sequences to make inferences about the food encountered by a caller. These results provide the first empirical evidence that bonobos are able to extract information about external events by attending to vocal sequences of other individuals and highlight the importance of call combinations in their natural communication system.

Development of socio-emotional competence in bonobos

Significance Across human development, individuals better able to manage their own emotions show greater social competence and more empathic concern for others. To test this interplay between social and emotional skills in one of our closest relatives, we collected behavioral measures on bonobos (Pan paniscus) with different rearing backgrounds at a forested sanctuary in Africa. Young bonobos showed the same connection between the ability to regulate their own emotions and social competence, such as developing friendships and concern for others. Mother-reared juveniles performed far better in this regard than juveniles orphaned at a young age, thus highlighting the importance of the mother–offspring bond. Our results support a shared socio-emotional framework for human and nonhuman primate behavior. Social and emotional skills are tightly interlinked in human development, and both are negatively impacted by disrupted social development. The same interplay between social and emotional skills, including expressions of empathy, has received scant attention in other primates however, despite the growing interest in caring, friendships, and the fitness benefits of social skills. Here we examine the development of socio-emotional competence in juvenile bonobos (Pan paniscus) at a sanctuary in the Democratic Republic of the Congo, focusing on the interplay between various skills, including empathy-related responding. Most subjects were rehabilitated orphans, but some were born at the sanctuary and mother-reared there. We observed how juveniles with different rearing backgrounds responded to stressful events, both when the stress affected themselves (e.g., a lost fight) or others (e.g., witnessing the distress of others). The main dependent variable was the consolation of distressed parties by means of calming body contact. As in children, consolation was predicted by overall social competence and effective emotion regulation, as reflected in the speed of recovery from self-distress and behavioral measures of anxiety. Juveniles more effective at self-regulation were more likely to console others in distress, and such behavior was more typical of mother-reared juveniles than orphans. These results highlight the interplay between the development of social and emotional skills in our ape relatives and the importance of the mother–offspring bond in shaping socio-emotional competence.

Contextually variable signals can be functionally referential

• We offer a new definition of functional reference that highlights the role of contextual cues.

Female bonobos use copulation calls as social signals

During mating events, females of many primate species produce loud and distinct vocalizations known as ‘copulation calls’. The adaptive significance of these signals is considered to be in promoting the callers direct reproductive success. Here, we investigated copulation calling in bonobos (Pan paniscus), a species in which females produce these vocalizations during sexual interactions with partners of both sexes. Females were more likely to call when mating with males than with females. We also observed a positive relationship between the likelihood of calling and partner rank, regardless of partner sex. Sexual activity generally increased with swelling size (an indicator of reproductive state) and, during their peak swelling, females called more with male than with female partners. Female bonobos are unusual among the non-human primates in terms of their heightened socio-sexuality. Our results suggest that in this species, copulation calls have undergone an evolutionary transition from a purely reproductive to a more general social function, reflecting the intrinsic evolutionary links between vocal behaviour and social cognition.

Functional flexibility in wild bonobo vocal behaviour

A shared principle in the evolution of language and the development of speech is the emergence of functional flexibility, the capacity of vocal signals to express a range of emotional states independently of context and biological function. Functional flexibility has recently been demonstrated in the vocalisations of pre-linguistic human infants, which has been contrasted to the functionally fixed vocal behaviour of non-human primates. Here, we revisited the presumed chasm in functional flexibility between human and non-human primate vocal behaviour, with a study on our closest living primate relatives, the bonobo (Pan paniscus). We found that wild bonobos use a specific call type (the “peep”) across a range of contexts that cover the full valence range (positive-neutral-negative) in much of their daily activities, including feeding, travel, rest, aggression, alarm, nesting and grooming. Peeps were produced in functionally flexible ways in some contexts, but not others. Crucially, calls did not vary acoustically between neutral and positive contexts, suggesting that recipients take pragmatic information into account to make inferences about call meaning. In comparison, peeps during negative contexts were acoustically distinct. Our data suggest that the capacity for functional flexibility has evolutionary roots that predate the evolution of human speech. We interpret this evidence as an example of an evolutionary early transition away from fixed vocal signalling towards functional flexibility.

A Comparison Between Bonobos and Chimpanzees: A Review and Update

Chimpanzees (Pan troglodytes) and bonobos (P. paniscus) are our closest living relatives, with the human lineage diverging from the Pan lineage only around five to seven Mya, but possibly as early as eight Mya.1–2 Chimpanzees and bonobos even share genetic similarities with humans that they do not share with each other.2 Given their close genetic relationship to humans, both Pan species represent crucial living models for reconstructing our last common ancestor (LCA) and identifying uniquely human features. Comparing the similarities and differences of the two Pan is thus essential for constructing balanced models of human evolution.3

Communication during sex among female bonobos: effects of dominance, solicitation and audience.

Bonobo females frequently form close bonds, which give them social power over other group members. One potential mechanism to facilitate female bonding is the performance of sexual interactions. Using naturalistic observations and experiments, we found various patterns that determined female-female sexual interactions. First, while low-ranked females interacted with all females, sexual interactions between high-ranked females were rare. Second, during genital contacts, females sometimes produced ‘copulation calls’, which were significantly affected by the rank of the caller and partner, as well as the solicitation direction. Third, there was a significant effect of the alpha female as a bystander, while variables relating to physical experience had no effects. Overall, results highlight the importance of sexual interactions for bonobo female social relations. Copulation calls are an important tool during this process, suggesting that they have become ritualised, beyond their reproductive function, to serve as broader social signals in flexible and potentially strategic ways.