Adult human perception of distress in the cries of bonobo, chimpanzee, and human infants

Understanding the extent to which humans perceive the emotional state of animals has both theoretical and practical implications. While recent studies indicate that natural selection has led to some convergence of emotion coding among vertebrate species (including humans), highlighting the interspecific value of emotional signals, it has also been argued that interspecific communication of emotions can fail due to species-specific signalling traits impairing information decoding and/or absence of familiarity with heterospecific communication systems. In this article, we show that human listeners pay attention to the mean pitch of vocalizations when asked to rate the distress level expressed by human baby cries, and that they use a similar pitch scale to rate the emotional level of baby non-human ape (bonobo and chimpanzee) distress calls. As a consequence, the very high-pitched bonobo infant calls were systematically rated as expressing overall high distress levels despite being recorded in contexts eliciting various stress intensity. Conversely, chimpanzee infant calls – which are characterized by a relatively lower pitch – were systematically rated as expressing relatively lower distress levels. These results indicate that, in the absence of exposure/familiarity, our spontaneous ability to range the emotional content of vocalizations in closely related ape species remains biased by basic frequency differences, suggesting that the absolute interspecific value of emotional signals should not be overestimated

Enduring voice recognition in bonobos

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 PDFPeer reviewe

How Ebola Impacts Genetics of Western Lowland Gorilla Populations

12 pagesInternational audienceBackground: Emerging infectious diseases in wildlife are major threats for both human health and biodiversity conservation. Infectious diseases can have serious consequences for the genetic diversity of populations, which could enhance the species' extinction probability. The Ebola epizootic in western and central Africa induced more than 90% mortality in Western lowland gorilla population. Although mortality rates are very high, the impacts of Ebola on genetic diversity of Western lowland gorilla have never been assessed. Methodology/Principal Findings: We carried out long term studies of three populations of Western lowland gorilla in the Republic of the Congo (Odzala-Kokoua National Park, Lossi gorilla sanctuary both affected by Ebola and Lossi's periphery not affected). Using 17 microsatellite loci, we compared genetic diversity and structure of the populations and estimate their effective size before and after Ebola outbreaks. Despite the effective size decline in both populations, we did not detect loss in genetic diversity after the epizootic. We revealed temporal changes in allele frequencies in the smallest population. Conclusions/Significance: Immigration and short time elapsed since outbreaks could explain the conservation of genetic diversity after the demographic crash. Temporal changes in allele frequencies could not be explained by genetic drift or random sampling. Immigration from genetically differentiated populations and a non random mortality induced by Ebola, i.e., selective pressure and cost of sociality, are alternative hypotheses. Understanding the influence of Ebola on gorilla genetic dynamics is of paramount importance for human health, primate evolution and conservation biology

Communication vocale sous influence des liens sociaux chez les bonobos

National audienceLes 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 sociale comparables à celles des conversations humaines, comme le fait d’éviter de se couper la parole ou de respecter des tours de paroles entre interlocuteurs. 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 social 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 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’âges 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

Bases sociales des interactions vocales chez les gorilles

National audienceL’existence de possibles précurseurs aux conversations humaines chez les primates fait actuellement débat. Des règles dites conversationnelles (évitement de la coupure de parole, respect d’un tour de parole, base sociale du choix de l’interlocuteur) ont été décrites chez les singes non-anthropoïdes, mais les patterns temporels des interactions vocales étudiés chez nos plus proches cousins montrent des résultats controversés : duo chez les gibbons, chorus chez les chimpanzés, chorus et antiphonie chez les bonobos… Ici, nous proposons de contribuer à ce débat en étudiant une autre espèce de grand singe, le gorille. Nous avons découvert trois patterns d’émissions fréquents : les cris isolés, les séquences de cris répétés et les interactions vocales. Si les émissions isolées et répétées concernent plus particulièrement les types de cris avec des fonctions de jeu, de détresse et d’agression, les interactions vocales sont le propre des cris de contact et sont notamment plus fréquentes chez les adultes que chez les jeunes. De plus, les interactions vocales sont composées d’échanges antiphoniques de cris émis par des individus qui évitent clairement la superposition et entretiennent un lien social privilégié (fréquents échanges de regards, importante proximité spatiale). Par contre, si on se focalise sur les initiations de ces échanges, le nombre d’occurrences est positivement corrélé au rang de l’émetteur

Social basis of vocal interactions in western lowland gorillas (Gorilla g. gorilla).

International audienceAuthors have raised the possibility of identifying primitive forms of conversational rules in monkeys: temporally ruled vocal interactions, call overlap avoidance, and socially based calling partner preferences. The question as to how these abilities have evolved in the primate lineage remains open to debate, particularly because studies based on apes are scarce and controversial. We studied a captive group of western lowland gorillas and tested the influence of caller characteristics and the type of bond between calling partners on vocal behavior based on the following: age, dominance, spatial proximity, sociopositive contact, and gaze. Four calling patterns that are call type dependent were identified: vocal interaction with and (more frequently) without call overlap, isolated calling, and repeated calling. Adult calls and grunts (contact calls) were predominant during vocal interactions, and the "response" delay was most often around half a second. The frequency of grunt dyadic exchanges was found to be linked to spatial proximity, gaze exchanges, and age proximity between calling partners. The dominance rank of callers determined the rate of contribution to these exchanges. These results show that some apes use rule-governed call exchanges and that these socially guided vocal interactions are more widespread than previously believed

Response to begging calls by Zebra Finch parents : "first come, first served" rule may overcome a parental preference between chicks.

International audienceIn birds, parents may provide differential food provisioning among offspring according to their sex. Here, we test the hypothesis that events linked to the fine dynamics of begging behaviour could modulate parental preferences. After evaluating the preference related to chick sex for each parent of six Zebra Finch Taeniopygia guttata pairs, we studied the possible modifications of this preference when offspring begging was asynchronous. Our observations show that male parents follow a "first come, first served" rule, whereas females keep their initial choice. Although this study remains preliminary due to the sample size, it underlines the potential importance of investigating fine temporal features of begging behaviour to fully understand parents' provisioning strategies

Importance du respect des "règles de conversation" chez les gorilles des plaines de l'Ouest

International audienc

Population and group structure of western lowland gorillas (Gorilla gorilla gorilla) at Lokoue, Republic of Congo

WOS:000223184100001International audienceDuring a 17-month study at the Lokoue clearing in Odzala National Park, Republic of Congo, we identified 377 western lowland gorillas. This population included 31 solitary males, 37 breeding groups, and eight nonbreeding groups. Its age- and sex-class structure was similar to those observed at two other clearings in the same forest block. However, the size of breeding groups varied with site (either clearing or forest sites). At Lokoue, breeding groups (mean size: 8.2 gorillas; range: 3-15) included a single silverback male and, on average, 3.2 adult females. Nonbreeding groups (mean size: 5.5; range: 2-15) were devoid of adult females. Five of the nonbreeding groups were composed predominantly of blackbacks, subadult males, and juveniles, and thus fit the definition of all-male groups previously observed in mountain gorillas. Our study confirms that 1) one-male breeding groups are the norm in western gorillas, and 2) all-male groups occur in this species. Despite frequent changes in members due to migrations of the males, the persistence of these all-male groups indicates that they may play an important role in the life of migrating males. Variations in population structure, and group composition and type among gorilla populations are discussed. However, a further understanding of the evolution of group-living in gorillas requires detailed ecological studies conducted in parallel with studies of the population structure and dynamics of these groups. (C) 2004 Wiley-Liss, Inc

Breaking conversational rules matters to captive gorillas: A playback experiment

International audienceAcross human cultures, conversations are regulated by temporal and social rules. The universality of conversational rules suggests possible biological bases and encourages comparisons with the communicative interactions of nonhuman animals. Unexpectedly, few studies have focused on other great apes despite evidence of proto-conversational rules in monkeys, thus preventing researchers from drawing conclusions on potential evolutionary origins of this behaviour. A previous study showed however that western lowland gorillas engage in soft call interactions that seem temporally-and socially-ruled. Indeed, interactions occurred mainly between individuals close in age who followed a preset response delay, thus preventing call overlap. Here, we experimentally investigated the presence of these rules in a captive gorilla group, using a violation-of-expectation paradigm. Head orientation responses suggest that the respect of response delay matters to subjects, but the importance of the interlocutors' age proximity appeared less clear. The intensity of the response varied with subjects' age in a context-dependent way, supporting a possible role of learning. Our findings support the growing number of studies highlighting the importance of vocal turn-taking in animals and a possible sociogenesis of this ability. The capacity to "converse" might have been a key step in the co-evolution of communication and complex sociality. Despite the diversity of human cultures, some basic conversational rules are respected in all societies and thus appear universal 1. These features are gathered in a so-called "contract of communication" that conversing interlocutors informally agree on 2. The contract takes into account "context relevance" (i.e. the evaluation of the context as pertinent or not to initiate a conversation), "reciprocity" (i.e. the evaluation of both partners as valid interlocutors), and "contract-based temporal rules" (i.e. the respect of a reciprocal exchange of alternating, short, and flexible turns between two or more interlocutors 3 , and speech overlap avoidance). Several authors have questioned the possible biological bases of these conversational rules and have, for several decades, conducted cross-species comparisons to understand their origin and role across animal communication systems 4-7. To facilitate cross species investigations, authors typically distinguish "conversation-like vocal exchanges" from other vocal patterns like isolated calling (one call emitted and no other calls can be heard around, e.g. in red-capped mangabeys Cercocebus torquatus 8), repeated calling (the same caller calls several times in a row, e.g. in Japanese macaques Macaca fuscata 9), disorganized phonoresponses (one individual produces a call, typically an alarm call that triggers calls in an apparent chaotic way from the other group members, e.g. in blue monkeys Cercopithecus mitis stuhlmanni 10), chorusing (two or more individuals overlap their emission of a given call type, e.g. in chimpanzees Pan troglodytes 11) and duetting (two individuals synchronise long series of calls or songs with stereotyped temporal association: e.g. in birds 12-14 , and gibbons Hylobates syndactylus 15). "Conversation-like vocal exchanges" are distinguished from the other types of vocal interactions because of their following specific features. First, they involve a diversity of recurrent vocal partners (which differs from duets). Second, interlocutors are typically familiar individuals belonging to a given social group and can be of any age or either sex (which differs from synchronized signalling 16-20). Third, "conversation-like vocal exchanges" are not restricted to a specific context, which differs from-usually long-distance-collective communication associated with mate attraction, territory protection and environmental disturbance 21 , and time of the day or year (excluding morning choruses and reproductive signals 22,23). Most commonly, these "conversation-like vocal exchanges" are observe