Unpeeling the layers of language: Bonobos and chimpanzees engage in cooperative turn-taking sequences

Human language is a fundamentally cooperative enterprise, embodying fast-paced and extended social interactions. It has been suggested that it evolved as part of a larger adaptation of humans’ species-unique forms of cooperation. Although our closest living relatives, bonobos and chimpanzees, show general cooperative abilities, their communicative interactions seem to lack the cooperative nature of human conversation. Here, we revisited this claim by conducting the first systematic comparison of communicative interactions in mother-infant dyads living in two different communities of bonobos (LuiKotale, DRC; Wamba, DRC) and chimpanzees (Taï South, Côte d’Ivoire; Kanyawara, Uganda) in the wild. Focusing on the communicative function of joint-travel-initiation, we applied parameters of conversation analysis to gestural exchanges between mothers and infants. Results showed that communicative exchanges in both species resemble cooperative turn-taking sequences in human conversation. While bonobos consistently addressed the recipient via gaze before signal initiation and used so-called overlapping responses, chimpanzees engaged in more extended negotiations, involving frequent response waiting and gestural sequences. Our results thus strengthen the hypothesis that interactional intelligence paved the way to the cooperative endeavour of human language and suggest that social matrices highly impact upon communication styles

Variable use of polyadic grooming and its effect on access to social partners in wild chimpanzees and bonobos

In mammals, allogrooming is prominent in forming and maintaining social and cooperative relationships. Yet an animal's social time is constrained, which may limit its access to a large number of partners. Dunbar (1993, Behavioral and Brain Sciences, 16 (4), 681–694) proposed that human polyadic conversations, which allow access to several social partners simultaneously, evolved as a form of social grooming to circumvent this time constraint. In nonhuman primates, polyadic grooming (PG), in contrast to dyadic grooming, may similarly be a time-efficient way to maintain weak social relationships with many partners which can be important for group level cooperation. It remains unknown whether PG is used to fulfil specific cooperative needs by accessing numerous weakly bonded partners and increasing the number of partners accessed per unit of time. We compared the use and effect of PG between chimpanzees, Pan troglodytes, which are highly territorial and collaborative (especially males), and bonobos, Pan paniscus, which are less territorial and collaborative and in which females are the main co-operators. We carried out focal grooming observations in one bonobo and two chimpanzee communities in the wild. As predicted, chimpanzees engaged in more PG than bonobos. Surprisingly, males engaged in PG more than females in both species. While chimpanzees accessed more partners per minute of grooming than bonobos via dyadic grooming, PG increased the number of partners accessed per minute only in bonobos. Finally, chimpanzees primarily used PG with individuals who were close in rank and frequent grooming partners, whereas bonobos used PG with individuals who were distant in rank, close party associates and frequent grooming partners. We suggest that bonobo males use PG to enhance conspecific social tolerance and mate choice. The overall higher rate of PG in chimpanzees suggests that between-group competition may promote polyadic affiliation, which possibly reinforces group cohesion and coordination. © 2020 The Author

Distance-decay effect in stone tool transport by wild chimpanzees

Stone tool transport leaves long-lasting behavioural evidence in the landscape. However, it remains unknown how large-scale patterns of stone distribution emerge through undirected, short-term transport behaviours. One of the longest studied groups of stone-tool-using primates are the chimpanzees of the Taï National Park in Ivory Coast, West Africa. Using hammerstones left behind at chimpanzee Panda nut-cracking sites, we tested for a distance-decay effect, in which the weight of material decreases with increasing distance from raw material sources. We found that this effect exists over a range of more than 2 km, despite the fact that observed, short-term tool transport does not appear to involve deliberate movements away from raw material sources. Tools from the millennia-old Noulo site in the Taï forest fit the same pattern. The fact that chimpanzees show both complex short-term behavioural planning, and yet produce a landscape-wide pattern over the long term, raises the question of whether similar processes operate within other stone-tool-using primates, including hominins. Where hominin landscapes have discrete material sources, a distance-decay effect, and increasing use of stone materials away from sources, the Taï chimpanzees provide a relevant analogy for understanding the formation of those landscapes

Systematic mapping of developmental milestones in wild chimpanzees

Postnatal development is protracted relative to lifespan in many primates, including modern humans (Homo sapiens), facilitating the acquisition of key motor, communication and social skills that can maximize fitness later in life. Nevertheless, it remains unclear what evolutionary drivers led to extended immature periods. While the developmental milestone literature is well established in humans, insight we can gain from one-species models is limited. By comparing the timing of relatable developmental milestones in a closely related species, the chimpanzee (Pan troglodytes), we can gain further understanding of the evolution of such an extended developmental phase. To date, few studies have specifically attempted to estimate developmental milestones in a manner comparable to the human literature, and existing studies lack sufficient sample sizes to estimate which milestones are more plastic with higher inter-individual variation in the timing of their emergence. Here, we describe the emergence of gross motor, fine motor, social interaction and communication traits from a longitudinal sample of 19 wild chimpanzee infants (8 females and 11 males), Taï National Park, Côte d’Ivoire. Gross motor traits emerged at a mean of 4 months, communication traits at 12 months, social interaction traits at 14 months and fine motor traits at 15 months, with later emerging milestones demonstrating greater inter-individual variation in the timing of the emergence. This pattern of milestone emergence is broadly comparable to observations in humans, suggesting selection for a prolonged infantile phase and that sustained skills development has a deep evolutionary history, with implications for theories on primate brain development

Long-term repeatability in social behaviour suggests stable social phenotypes in wild chimpanzees

Consistent individual differences in social phenotypes have been observed in many animal species. Changes in demographics, dominance hierarchies or ecological factors, such as food availability or disease prevalence, are expected to influence decision-making processes regarding social interactions. Therefore, it should be expected that individuals show flexibility rather than stability in social behaviour over time to maximize the fitness benefits of social living. Understanding the processes that create and maintain social phenotypes requires data encompassing a range of socioecological settings and variation in intrinsic state or life-history stage or strategy. Using observational data spanning up to 19 years for some individuals, we demonstrate that multiple types of social behaviour are repeatable over the long term in wild chimpanzees, a long-lived species with complex fission-fusion societies. We controlled for temporal, ecological and demographic changes, limiting pseudo-repeatability. We conclude that chimpanzees living in natural ecological settings have relatively stable long-term social phenotypes over years that may be independent of life-history or reproductive strategies. Our results add to the growing body of the literature suggesting consistent individual differences in social tendencies are more likely the rule rather than the exception in group-living animals

Maternal effects on offspring growth indicate post-weaning juvenile dependence in chimpanzees (Pan troglodytes verus)

Background: In animals with altricial offspring, most growth occurs after birth and may be optimized by post-natal maternal care. Maternal effects on growth may be influenced by individual characteristics of the mothers, such as social status, individual investment strategies and the length of association with offspring. The prolonged juvenile dependence seen in humans is a distinctive life history adaptation, which may have evolved to facilitate sustained somatic and brain growth. In chimpanzees, offspring are typically weaned at approximately 4 years old, yet immature individuals continue to associate with their mothers for up to 10 years beyond weaning. Whether this lengthy association or the individual characteristics of mothers influences growth patterns in this species is not clear. The relationship between urinary creatinine and specific gravity is an established non-invasive measure of muscle mass in humans and chimpanzees. We analysed the urinary creatinine and specific gravity of 1318 urine samples from 70 wild chimpanzees from the Taï Forest, Ivory Coast aged 4 to 15 years. Results: We showed a clear increase in urinary creatinine levels with age in both males and females, replicating established growth curves in this species and reaffirming this measure as a reliable proxy for lean body mass. Comparing those who experience maternal loss (orphans) with non-orphan chimpanzees, maternal presence beyond weaning age and into late juvenility positively influenced offspring muscle mass throughout ontogeny such that orphans had significantly less muscle mass than age-matched non-orphans. In age-matched offspring with mothers, those with high-ranking mothers had greater muscle mass. Accounting for variation in muscle mass attributable to maternal presence, we found no effect of maternal investment (length of inter birth interval, from own birth to birth of following sibling) on offspring muscle mass. Conclusion: Chimpanzee mothers have an extended and multi-faceted influence on offspring phenotypes. Our results suggest that maternal investment extends beyond lactation and into early adulthood and has clear benefits to offspring physical development. Therefore, prolonged juvenile dependence, although unique in its form in human societies, may be a trait with deeper evolutionary origins

Information transfer efficiency differs in wild chimpanzees and bonobos, but not social cognition

Several theories have been generated to understand the socio-cognitive mechanisms underlying the unique cooperative abilities of humans. The ‘interdependence hypothesis' posits first, that the cognitive dimension of human cooperation evolved in contexts when several individuals needed to act together to achieve a common goal, like when hunting large prey. Second, the more interdependent individuals are, the more likely they are to provide services to conspecifics in other contexts. Alternatively, the ‘social tolerance hypothesis' proposes that higher social tolerance allows conspecifics to cooperate more efficiently and with a wider range of partners. We conducted the first field experimental evaluation of both hypotheses in our closest living relatives by contrasting chimpanzees to the less interdependent but more tolerant bonobos. We compared each species' performance during a cooperative task: informing conspecifics about a danger. We presented Gaboon viper models to 82 individuals from five wild communities. Chimpanzees arriving late at the snake were significantly more likely to have heard a call and less likely to startle, indicating that chimpanzees were better informed about the presence of the threat than bonobos. This stems from clear species differences in how individuals adjusted their calling decisions to the level of information already available. Chimpanzees were more likely to call and produced more alarm calls when they had not yet heard a call, whereas bonobos did so when they already heard a call. Our results confirm the link between interdependence and cooperation performance. These species differences were most likely driven by differences in motivation rather than in cognitive capacities because both species tended to consider audience knowledge in their decision to call. Our results inform theories on the evolution of human cooperation by linking inter-group competition pressure and in-group cooperative motivation and/or capability

Social uncertainty promotes signal complexity during approaches in wild chimpanzees (Pan troglodytes verus) and mangabeys (Cercocebus atys atys)

The social complexity hypothesis for the evolution of communication posits that complex social environments require greater communication complexity for individuals to effectively manage their relationships. We examined how different socially uncertain contexts, reflecting an increased level of social complexity, relate to variation in signalling within and between two species, which display varying levels of fission-fusion dynamics (sympatric-living chimpanzees and sooty mangabeys, Taï National Park, Ivory Coast). Combined signalling may improve message efficacy, notably when involving different perception channels, thus may increase in moments of high social uncertainty. We examined the probability of individuals to emit no signal, single or multisensory or combined (complex) signals, during social approaches which resulted in non-agonistic outcomes. In both species, individuals were more likely to use more combined and multisensory signals in post-conflict approaches with an opponent than in other contexts. The clearest impact of social uncertainty on signalling complexity was observed during chimpanzee fusions, where the likelihood of using complex signals tripled relative to other contexts. Overall, chimpanzees used more multisensory signals than mangabeys. Social uncertainty may shape detected species differences in variation in signalling complexity, thereby supporting the hypothesis that social complexity, particularly associated with high fission-fusion dynamics, promotes signalling complexity

Attractiveness of female sexual signaling predicts differences in female grouping patterns between bonobos and chimpanzees.

Here we show that sexual signaling affects patterns of female spatial association differently in chimpanzees and bonobos, indicating its relevance in shaping the respective social systems. Generally, spatial association between females often mirrors patterns and strength of social relationships and cooperation within groups. While testing for proposed differences in female-female associations underlying female coalition formation in the species of the genus Pan, we find only limited evidence for a higher female-female gregariousness in bonobos. While bonobo females exhibited a slightly higher average number of females in their parties, there is neither a species difference in the time females spent alone, nor in the number of female party members in the absence of sexually attractive females. We find that the more frequent presence of maximally tumescent females in bonobos is associated with a significantly stronger increase in the number of female party members, independent of variation in a behavioural proxy for food abundance. This indicates the need to look beyond ecology when explaining species differences in female sociality as it refutes the idea that the higher gregariousness among bonobo females is driven by ecological factors alone and highlights that the temporal distribution of female sexual receptivity is an important factor to consider when studying mammalian sociality