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International audience; Cet article présente notre étude sur la reconnaissance vocale à long terme des partenaires sociaux chez les bonobos Pan paniscus. Ces résultats ont été publiés en 2016 dans la revue Scientific Reports 6 : 22046 | https://doi.org/10.1038/srep22046 et, avec l'accord de tous les co-auteurs, nous proposons ici une version française de cette étude pour la Revue de Primatologie. La reconnaissance sociale à long terme est vitale pour les espèces vivant dans des réseaux sociaux complexes et dans lesquels des individus familiers peuvent se rencontrer à nouveau après de longues périodes de séparation. Chez les primates non humains qui vivent dans des environnements forestiers denses, la visibilité est souvent limitée ; et, la reconnaissance des partenaires sociaux à longue distance dépend de la communication vocale. Etonnamment, la reconnaissance vocale de partenaires après des années de séparation n'a jamais été testée chez aucune espèce de grand singe, malgré l’organisation complexe de leur société et leur intelligence sociale. Nous montrons ici que les bonobos, Pan paniscus, sont capables d’une reconnaissance vocale fiable de leurs partenaires sociaux, et cela même s'ils ont été séparés pendant cinq ans. Nous avons testé expérimentalement les réponses de bonobos aux vocalisations d’anciens membres de leur groupe qui avaient été transférés entre parcs zoologiques. Malgré de longues périodes de séparation, les sujets ont répondu plus intensément aux voix familières qu'aux voix d'individus étrangers. Cette observation démontre expérimentalement que les bonobos peuvent discriminer des individus sur la seule base d’indice acoustique même des années après leur dernière rencontre. Notre étude suggère également que les bonobos peuvent cesser de faire la distinction entre des individus familiers et non familiers après une période de huit ans, indiquant que les représentations vocales ou l'intérêt pourraient être limités dans le temps chez cette espèce.

International audience; Human languages are deeply associated with the capacities to be engaged in social actions and cooperative communication. Despite their diversity, they all share the respect of conversational rules such as speech overlap avoidance, turn-taking and socially-based interlocutor preferences. Among primate species, such orderly vocal exchanges have been found in a diversity of monkey species, though surprisingly, not in great apes. Social functions of vocal exchanges have been largely evidenced and thus the absence of antiphony in great apes is puzzling regarding their complex social life and their evolutionary proximity with humans. The present study investigates whether bonobos – a highly social and cooperative species – present spontaneous coordinated vocal turn-taking and whether social factors affect these vocal productions. We monitored the vocal output of a captive group at La Vallée des Singes (France). Nearly 200 exchanged calls have been analyzed for which the caller identity and context of emission were known. We found the existence of temporally- and socially- ruled vocal exchanges, such as call overlap avoidance. Call repertoire sharing between exchanging partners was explained by social factors and not by their age, sex or kinship. Bonobos were also capable of immediate acoustic matching during interactions. These findings allowed testing whether the conversational rule-respect is significant for listeners or not. We played back four types of stimuli of vocal exchanges creating call overlap and/or modifying the caller identities. In total 10 bonobos have been tested. We found that the audience were sensitive to temporal rule-breaking of antiphony. This study demonstrates for the first time that great apes, like monkeys, apply some simple conversational turn-taking rules and that the audience pay attention to third-party vocal exchanges. Finding these shared traits between monkeys, apes and humans fills a significant gap and will be of high interest in the discussions of speech evolution.

We would like to thank the French Ministère de l’Enseignement Supérieur et de la Recherche (PhD grant to SK), the Université de Saint-Etienne (research sabbaticals to FL and NM, visiting professorship to KZ and research funding) and the European Research Council (KZ grant PRILANG 283871). Long-term social recognition is vital for species with complex social networks, where familiar individuals can encounter one another after long periods of separation. For non-human primates who live in dense forest environments, visual access to one another is often limited, and recognition of social partners over distances largely depends on vocal communication. Vocal recognition after years of separation has never been reported in any great ape species, despite their complex societies and advanced social intelligence. Here we show that bonobos, Pan paniscus, demonstrate reliable vocal recognition of social partners, even if they have been separated for five years. We experimentally tested bonobos' responses to the calls of previous group members that had been transferred between captive groups. Despite long separations, subjects responded more intensely to familiar voices than to calls from unknown individuals - the first experimental evidence that bonobos can identify individuals utilising vocalisations even years after their last encounter. Our study also suggests that bonobos may cease to discriminate between familiar and unfamiliar individuals after a period of eight years, indicating that voice representations or interest could be limited in time in this species. Publisher PDF

The origin of human speech is still a hotly debated topic in science. Evidence of socially-guided acoustic flexibility and proto-conversational rules has been found in several monkey species, but is lacking in social and cooperative great apes. Here we investigated spontaneous vocal interactions within a peaceful context in captive bonobos to reveal that vocal interactions obey temporally and social rules. Dyadic vocal interactions were characterized by call overlap avoidance and short inter-call intervals. Bonobos preferentially responded to conspecifics with whom they maintained close bonds. We also found that vocal sharing rate (production rate of shared acoustic variants within each given dyad) was mostly explained by the age difference of callers, as other individual characteristics (sex, kinship) and social parameters (affinity in spatial proximity and in vocal interactions) were not. Our results show that great apes spontaneously display primitive conversation rules guided by social bonds. The demonstration that such coordinated vocal interactions are shared between monkeys, apes and humans fills a significant gap in our knowledge of vocal communication within the primate phylogeny and highlights the universal feature of social influence in vocal interactions.

International audience; Bonobos live in dense forest habitats where visual communication is often limited rendering vocal signals important to regulate their social interactions. Moreover their fluid fission-fusion society requires contact over long distances, suggesting that vocal signals of group members are recognised individually. To this end, individual signatures should be reliably encoded in vocal interactions and memorised by recipients over long periods. In this study we investigated individual vocal recognition of group members that had been separated for long periods of time (two to nine years) with varying relationships. In the wild, long-term separation happens regularly, usually in relation to female migration. In captivity, the same process takes place during the transfer of individuals between zoos, mimicking wild migration. We simulated bonobo transfers by broadcasting contact calls of familiar or unfamiliar individuals to our subjects, thus imitating the arrival of new group members. In total, we tested 15 bonobos (> 10 years old) from three European zoos and compared their behavioural responses. We found that bonobos responded differently to familiar voices than to stranger voices, even after prolonged separation. However, the recognition of past partners appears to diminish after being separated for 6-8 years. This interesting result will be discussed regarding to the social needs in bonobos.

International audience; Les productions vocales des primates non humains sont encore décrites comme innées et peu flexibles, pourtant, de plus en plus d'études montrent qu'ils sont capables d'apprentissage et d'ajustement vocal. Étonnamment, peu d'études ont traité la question de la plasticité vocale chez les grands singes, nos plus proches parents et à l'organisation sociale complexe. Outre la plasticité vocale, des 'conversations' simples ont été décrites chez quatre espèces de primates. Elles échangent des vocalisations en respectant des règles d'organisation temporelle et sociales comparables à celles des conversations humaines. Chez les chimpanzés (grands singes), deux études mentionnent plutôt l'existence de chorus et des manifestations vocales désorganisées. Nous proposons ici d'étudier l'organisation des interactions vocales chez une autre espèce de grand singe, le bonobo (Pan paniscus). Les bonobos vivent dans un système sociale de type fission-fusion où chaque membre de la communauté occupe une position sociale unique et développe des relations d'affinités avec certains membres du groupe indépendamment des relations d'apparentées. Au contraire, chez les chimpanzés la majorité des affinités sociales sont dictées par les apparentements. Notre étude qui porte sur un groupe captif de neuf individus au parc Zoologique de la Vallée des Singes (France) montre qu'il existe un partage vocal important entre individus qui présentent une forte affinité sociale (définie par leur proximité spatiale). En revanche les relations d'apparentement, la différence d'âge et le sexe des individus ne semblent pas influencer le degré de partage vocal. Enfin, au sein des échanges vocaux, il y a convergence acoustique dans le domaine temporel et fréquentiel. Ainsi les cris émis en réponse tendent à ressembler au cri entendu précédemment. Cette étude montre pour la première fois, à l'instar des autres primates, des comportements vocaux qui répondent à des règles sociales de conversation et une capacité d'ajustement vocal immédiat chez une espèce de grand singe.