Search

Among African great apes, play is virtually absent between adult lowland gorillas (Gorilla gorilla gorilla). Here, we report an extremely rare case of adult–adult play observed in the lowland gorilla group housed at La Vallée de Singes (France). We recorded three playful interactions between the silverback and an adult lactating female. Given the diverse causal and functional nature of play, different factors may join in promoting this behaviour. In our group, contrary to what has been shown by previous studies in wild and captive gorillas, adult females spent more time in spatial proximity with the silverback than with other females. Hence, the probability of social interaction (including play) between silverback and adult females was enhanced. Moreover, the motivation of the lactating female to play might be an effect of oxytocin, a hormone that reaches high concentration levels during lactation and that promotes social affiliation. The fact that play invitations were always performed by the female might support this hypothesis. Certainly, we cannot exclude the possibility that the play event is a group idiosyncrasy or an artefact of captivity, even though the subjects never showed abnormal behaviour. Structurally, play sessions showed a suitable degree of pattern variability and switching frequency from one pattern to another. The proportion of offensive patterns was higher in the female during play and in the male during aggression, which conforms to the role reversal play phenomenon. In conclusion, this report confirms that the absence of evidence is not the evidence of absence. It is likely that under particular physiological or socio-ecological conditions, adult–adult play may be manifested as an “unconventional” part of gorilla social behaviour.

In primates, yawn contagion (the yawning response elicited by others' yawn) is variably influenced by individual (e.g., sex, age) and social factors (e.g., familiarity) and possibly linked to interindividual synchronization, coordination, and emotional contagion. Two out of three studies on yawn contagion in bonobos (Pan paniscus), found the presence of the phenomenon with mixed results concerning the effect of familiarity and no replication on its modulating factors. To address this puzzling issue, we recorded all occurrences data on yawn contagion in a captive bonobo group (March-June 2021; 18 individuals; La Vallée des Singes, France). Contrary to chimpanzees and humans, the number of triggering yawns increased contagion, possibly owing to a higher stimulus threshold. This aspect may explain the interindividual variability observed in yawn contagion rates. In subjects under weaning, we did not detect yawn contagion and, as it occurs in certain human cohorts, yawn contagion declined with age, possibly due to reduced sensitivity to others. Females responded more than males and elicited more responses from females when showing sexual swelling. As reproductive females are central in bonobo society, our results support the hypothesis that-as in other Hominini-the most influential sex can influence yawn contagion. The relationship quality (measured via grooming/play) did not affect yawn contagion, possibly due to bonobos' xenophilic nature. Overall, this study confirms the presence of yawn contagion in bonobos and introduces new elements on its modulating factors, pointing toward the necessity of cross-group studies.

We assessed the occurrence, genetic diversity, and zoonotic potential of four protozoan (Cryptosporidium spp., Entamoeba histolytica, Entamoeba dispar, Giardia duodenalis), one stramenopile (Blastocystis sp.), one microsporidia (Enterocytozoon bieneusi), and two ciliate (Balantioides coli, Troglodytella abrassarti) intestinal parasite or commensal protist species in captive non-human primates (NHP) and their zookeepers from six European zoological gardens in France (n = 1), Germany (n = 1), and Spain (n = 4). Faecal samples from NHP (n = 454) belonging to 63 species within 35 genera and humans (n = 70) were collected at two sampling periods in each participating institution between October 2018-August 2021. Detection and species identification was accomplished by PCR and Sanger sequencing of the ssu rRNA and/or ITS genes. Sub-genotyping analyses using specific markers were conducted on isolates positive for G. duodenalis (gdh, bg, tpi) and Cryptosporidium spp. (gp60). Overall, 41.0% (186/454) and 30.0% (21/70) of the faecal samples of NHP and human origin tested positive for at least one intestinal protist species, respectively. In NHP, Blastocystis sp. was the most prevalent protist species found (20.3%), followed by G. duodenalis (18.1%), E. dispar (7.9%), B. coli and T. abrassarti (1.5% each), and Cryptosporidium spp. and E. bieneusi (0.9% each). Occurrence rates varied largely among NHP host species, sampling periods, and zoological institutions. The predominant protist species found in humans was Blastocystis sp. (25.7%), followed by Cryptosporidium spp. (2.9%), E. dispar (1.4%), and G. duodenalis (1.4%). Sequencing of PCR-positive amplicons in human and/or NHP confirmed the presence of Cryptosporidium in six isolates (C. hominis: 66.7%, C. parvum: 33.3%), G. duodenalis in 18 isolates (assemblage A: 16.7%, assemblage B: 83.3%), Blastocystis in 110 isolates (ST1:38.2%, ST2:11.8%, ST3: 18.2%, ST4: 9.1%, ST5: 17.3%, ST8: 2.7%, ST13: 0.9%), and E. bieneusi in four isolates (CM18: 75.0%, Type IV: 25.0%). Zoonotic transmission events involving Blastocystis ST1–ST4 were identified in four zoological institutions. Zoonotic transmission of C. hominis was highly suspected, but not fully demonstrated, in one of them. Monitoring of intestinal protist species might be useful for assessing health status of captive NHP and their zookeepers, and to identify transmission pathways of faecal-orally transmitted pathogens.

Compared to other animals, humans appear to have a special motivation to share experiences and mental states with others (Clark, 2006; Grice, 1975), which enables them to enter a condition of ‘we’ or shared intentionality (Tomasello & Carpenter, 2005). Shared intentionality has been suggested to be an evolutionary response to unique problems faced in complex joint action coordination (Levinson, 2006; Tomasello, Carpenter, Call, Behne, & Moll, 2005) and to be unique to humans (Tomasello, 2014). The theoretical and empirical bases for this claim, however, present several issues and inconsistencies. Here, we suggest that shared intentionality can be approached as an interactional achievement, and that by studying how our closest relatives, the great apes, coordinate joint action with conspecifics, we might demonstrate some correlate abilities of shared intentionality, such as the appreciation of joint commitment. We provide seven examples from bonobo joint activities to illustrate our framework.

Funding: Research was funded by the Swiss National Science Foundation (grant no. CR31I3_166331 awarded to A.B. and K.Z.). Joint action is central to human nature, enabling collectives to achieve goals otherwise unreachable by individuals. It is enabled by humans’ capacity to understand and engage in joint commitments. Joint commitments are evidenced when partners in interrupted joint actions reengage one another. To date, there is no clear evidence whether nonhuman animals understand joint commitment, suggesting that only humans experience it. Here, we revisit this claim by interrupting bonobos engaged in social activities. Bonobos reliably resumed the activity, and the likelihood of resumption was higher for social compared to solitary activities. Furthermore, communicative efforts deployed to suspend and resume social activities varied depending on partners’ social relationships and interactive roles. Our results suggest that bonobos, like humans, engage in joint commitment and have some awareness of the social consequences of breaking it. Publisher PDF

Funding: We thank the French Ministère de l’Enseignement Supérieur et de la Recherche (Ph.D. grant to S.K.), the Université de Saint-Etienne (research sabbaticals to F.L. and N.M., visiting professorship to K.Z. and research funding), the European Research Council (K.Z. grant PRILANG 283871), Institut universitaire de France (NM) and the Labex CeLyA. Vocalizations often contain both ‘dynamic’ information, related to short-term fluctuations in the individual's emotional states, and ‘static’ information, related to long-term attributes such as age, sex, weight and body size which define an ‘individual vocal signature’. While both types of information may be of functional value to receivers, dynamic information requires acoustic versatility, while static information depends on acoustic stability. Here we investigated whether an individual vocal signature is present across the vocal repertoire of the bonobo, Pan paniscus. First, the analysis of the acoustic structure of its five most common tonal vocalizations emphasized the highly graded structure of its repertoire. We then evaluated the reliability of identity information across these call types. The results show that, while all call types supported information related to identity, the reliability of these vocal signatures was not consistent along the graded vocal continuum. Caller identity was strongly encoded at one end of the acoustic gradation (high-hoot) and decreased from bark, soft bark, peep-yelp to peep calls. Strikingly, the reliability of the individual signature thus decreased from calls used in high-arousal contexts to those used in low-arousal contexts. To the best of our knowledge, this is the first demonstration that an acoustic gradation that codes for ‘dynamic’ information can be accompanied by variation in the ‘static’ information that supports vocal individuality. Postprint

International audience; Allogrooming in primates serves not only a hygienic function, but also plays a crucial role in maintaining strong affiliative bonds between group members, which in turn, underpin the emergence of cooperative behavior. In contrast, although allopreening occurs in many avian species, we know little about its social functions. Our study addresses this issue by investigating allopreening in a broad comparative data set including six corvid and nine parrot species. We assessed whether rates of allopreening initiations, proportion of time spent allopreening, and the number of grooming partners in captive group-housed birds were comparable to patterns observed in captive chimpanzees and bonobos. While parrots and corvids were found to have similar rates of social grooming to bonobos and chimpanzees, Pan species dedicated significantly more time to social grooming. Animals in larger groups had more grooming partners, but when controlling for the number of potential partners, birds tended to have fewer grooming interaction partners than Pan species. We then investigated whether allopreening in parrots and corvids was predicted by behavioral markers of affiliative social bonds (close physical proximity, active feeding, and low levels of agonistic behavior). Results revealed that providing allopreening to a partner was significantly predicted by often being in close proximity, but not engagement in active feeding or agonistic behavior. We examined the region allopreened in a subset of species and found that preening a partner's head was predicted by both close physical proximity and active feeding, while body allopreening was only predicted by close physical proximity. Head preening may confer more hygienic benefits to recipients, and thus, may be more selectively provided to valued partners. Results support the hypothesis that allopreening in corvids and parrots helps maintain social bonds with an individual's most important social partners, showing some similarities to allogrooming in primates.

Different primate species have developed extensive capacities for grasping and manipulating objects. However, the manual abilities of primates remain poorly known from a dynamic point of view. The aim of the present study was to quantify the functional and behavioral strategies used by captive bonobos (Pan paniscus) during tool use tasks. The study was conducted on eight captive bonobos which we observed during two tool use tasks: food extraction from a large piece of wood and food recovery from a maze. We focused on grasping postures, in-hand movements, the sequences of grasp postures used that have not been studied in bonobos, and the kind of tools selected. Bonobos used a great variety of grasping postures during both tool use tasks. They were capable of in-hand movement, demonstrated complex sequences of contacts, and showed more dynamic manipulation during the maze task than during the extraction task. They arrived on the location of the task with the tool already modified and used different kinds of tools according to the task. We also observed individual manual strategies. Bonobos were thus able to develop in-hand movements similar to humans and chimpanzees, demonstrated dynamic manipulation, and they responded to task constraints by selecting and modifying tools appropriately, usually before they started the tasks. These results show the necessity to quantify object manipulation in different species to better understand their real manual specificities, which is essential to reconstruct the evolution of primate manual abilities.

In the European captive population of western lowland gorillas (Gorilla gorilla gorilla), the harem social structure and an even sex ratio at birth result in a surplus of males and consequent management difficulties. This study seeks to assess the socialization differences between captive juvenile and adolescent male gorillas according to their fertility status (intact vs castrated) in different social compositions (familial vs bachelor groups), and to evaluate the suitability of castration as a management tool for the EEP gorilla population. We carried out social network analyses (SNA) to assess the “positive” proximity pattern of behaviour in 93 western lowland gorillas aged from 0 to 45 years old and housed in 11 social units (seven familial and four bachelor groups). We compared the data recorded for the 27 juvenile and adolescent (i.e. subadult and blackback) males included in our sample size. Although no differences were revealed between the intact juveniles and the castrated juveniles living in familial groups, our results showed that castrated adolescent individuals showed more cohesiveness within their familial group than their intact conspecifics in terms of their activity budget. They also displayed a “positive” proximity pattern of behaviour with all group members, including adults (silverback and females). Despite being significantly more isolated, the intact adolescent males living in bachelor groups do not differ from their castrated and intact counterparts of the same age class living in familial groups in terms of their strength of “positive” behaviour when close to group conspecifics. This effect highlights the social benefits of male-male interactions within gorilla species. Our results may be evidence that both of the management strategies compared here, i.e. bachelor groups and castration, could be appropriate socio-behavioural enrichments during juvenility and adolescence. These findings also highlight the need to continue investigations until the study subjects reach adulthood to validate and/or improve these tools for the welfare-compliant management of gorilla male surplus in captivity.

The research leading to these results has received funding from the European Research Council under the European Union’s Seventh Framework Programme (FP7/2007-2013) / ERC grant agreement n°283871 and the Swiss National Science Foundation (Social learning in primate communication: 31003A_166458 / Coordinating joint action in apes: Testing the boundaries of the human interaction engine: CR31I3_159655). A fruitful approach to investigate social learning in animals is based on paradigms involving the manipulation of artefacts. However, tool use and elaborate object manipulations are rare in natural conditions, suggesting that social learning evolved in other contexts where fitness consequences are higher, such as discriminating palatable from noxious foods, recognising predators or understanding social hierarchies. We focussed on one such context by investigating whether bonobos socially learned others’ arbitrary food preferences through mere observation. To this end, we trained two demonstrators to prefer or avoid distinctly coloured food items, treated with either a sweet or bitter agent. Demonstrators then displayed their newly acquired preferences in front of naïve subjects. In subsequent choice tests, subjects generally matched their choices to the demonstrators’ preferred food colours, despite having already tasted the equally palatable colour alternative. Both age and exposure to demonstrator preference had a significant positive effect on the proportion of matched choices. Moreover, in a context where errors can be costly, social learning was instant insofar as six of seven subjects used socially learned information to influence their very first food choice. We discuss these findings in light of the current debate on the evolution of social learning in animals. Postprint

The research leading to these results has received funding from the European Research Council under the European Union's Seventh Framework Programme (FP7/2007-2013)/ERC grant agreement no. 283871 and the Swiss National Science Foundation (Social learning in primate communication: 31003A_166458 / Coordinating joint action in apes: Testing the boundaries of the human interaction engine: CR31I3_159655). The question of whether animals have some sort ofself-awareness is a topic of continued debate. A necessary precondition forself-awareness is the ability to visually discriminate the self from others,which has traditionally been investigated through mirror self-recognition experiments.Although great apes generally pass such experiments, interpretations of resultshave remained controversial. The aim of this study was to investigate howbonobos (Pan paniscus) respond todifferent types of images of themselves and others, both before and afterprolonged mirror exposure. We first presented presumably mirror-naive subjectswith representations of themselves in three different ways (mirror image,contingent and non-contingent video footage) as well as representations ofothers (video footage of known and unknown conspecifics). We found thatsubjects paid significantly less attention to contingent images of themselves(mirror image, video footage) than to non-contingent images of themselves andunfamiliar individuals, suggesting they perceived the non-contingent self-imageas novel. We then provided subjects with three months of access to a largemirror centrally positioned in the enclosure. Following this manipulation,subjects showed significantly reduced interest in the non-contingentself-images, while interest in unknown individuals remained unchanged,suggesting that the mirror experience has led to a fuller understanding oftheir own self. We discuss implications of this preliminary investigation forthe on-going debate on self-awareness in animals. Publisher PDF

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

Different primate species have developed extensive capacities for grasping and manipulating objects. However, the manual abilities of primates remain poorly known from a dynamic point of view. The aim of the present study was to quantify the functional and behavioral strategies used by captive bonobos (Pan paniscus) during tool use tasks. The study was conducted on eight captive bonobos which we observed during two tool use tasks: food extraction from a large piece of wood and food recovery from a maze. We focused on grasping postures, in-hand movements, the sequences of grasp postures used that have not been studied in bonobos, and the kind of tools selected. Bonobos used a great variety of grasping postures during both tool use tasks. They were capable of in-hand movement, demonstrated complex sequences of contacts, and showed more dynamic manipulation during the maze task than during the extraction task. They arrived on the location of the task with the tool already modified and used different kinds of tools according to the task. We also observed individual manual strategies. Bonobos were thus able to develop in-hand movements similar to humans and chimpanzees, demonstrated dynamic manipulation, and they responded to task constraints by selecting and modifying tools appropriately, usually before they started the tasks. These results show the necessity to quantify object manipulation in different species to better understand their real manual specificities, which is essential to reconstruct the evolution of primate manual abilities.

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. Etonnamment, 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. 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’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.

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.