Papers by Jean-Pascal Guéry
American journal of primatology, Mar 28, 2024
BMC ecology and evolution, Feb 14, 2024
Background Biological adaptation manifests itself at the interface of different biologically rele... more Background Biological adaptation manifests itself at the interface of different biologically relevant 'levels' , such as ecology, performance, and morphology. Integrated studies at this interface are scarce due to practical difficulties in study design. We present a multilevel analysis, in which we combine evidence from habitat utilization, leaping performance and limb bone morphology of four species of tamarins to elucidate correlations between these 'levels'. Results We conducted studies of leaping behavior in the field and in a naturalistic park and found significant differences in support use and leaping performance. Leontocebus nigrifrons leaps primarily on vertical, inflexible supports, with vertical body postures, and covers greater leaping distances on average. In contrast, Saguinus midas and S. imperator use vertical and horizontal supports for leaping with a relatively similar frequency. S. mystax is similar to S. midas and S. imperator in the use of supports, but covers greater leaping distances on average, which are nevertheless shorter than those of L. nigrifrons. We assumed these differences to be reflected in the locomotor morphology, too, and compared various morphological features of the long bones of the limbs. According to our performance and habitat utilization data, we expected the long bone morphology of L. nigrifrons to reflect the largest potential for joint torque generation and stress resistance, because we assume longer leaps on vertical supports to exert larger forces on the bones. For S. mystax, based on our performance data, we expected the potential for torque generation to be intermediate between L. nigrifrons and the other two Saguinus species. Surprisingly, we found S. midas and S. imperator having relatively more robust morphological structures as well as relatively larger muscle in-levers, and thus appearing better adapted to the stresses involved in leaping than the other two. Conclusion This study demonstrates the complex ways in which behavioral and morphological 'levels' map onto each other, cautioning against oversimplification of ecological profiles when using large interspecific eco-morphological studies to make adaptive evolutionary inferences.
Frontiers in Veterinary Science, Jan 4, 2022
E. bieneusi in four isolates (CM18: 75.0%, Type IV: 25.0%). Zoonotic transmission events involvin... more 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.
PeerJ, Aug 28, 2020
The question of whether animals have some sort of self-awareness is a topic of continued debate. ... more The question of whether animals have some sort of self-awareness is a topic of continued debate. A necessary precondition for self-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 results have remained controversial. The aim of this study was to investigate how bonobos (Pan paniscus) respond to different types of images of themselves and others, both before and after prolonged mirror exposure. We first presented presumably mirror-naive subjects with representations of themselves in three different ways (mirror image, contingent and non-contingent video footage) as well as representations of others (video footage of known and unknown conspecifics). We found that subjects paid significantly less attention to contingent images of themselves (mirror image, video footage) than to non-contingent images of themselves and unfamiliar individuals, suggesting they perceived the non-contingent self-images as novel. We then provided subjects with three months of access to a large mirror centrally positioned in the enclosure. Following this manipulation, subjects showed significantly reduced interest in the non-contingent self-images, while interest in unknown individuals remained unchanged, suggesting that the mirror experience has led to a fuller understanding of their own self. We discuss implications of this preliminary investigation for the ongoing debate on self-awareness in animals.
American Journal of Primatology, Jul 28, 2023
Applied Animal Behaviour Science, Apr 1, 2023
Animals, Jan 26, 2023
This article is an open access article distributed under the terms and conditions of the Creative... more This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY
Primates, Feb 22, 2022
Among African great apes, play is virtually absent between adult lowland gorillas (Gorilla gorill... more 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.
Ethology, Dec 16, 2019
Allogrooming in primates serves not only a hygienic function, but also plays a crucial role in ma... more 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.
Behavioural Processes, Oct 1, 2019
Bonobos socially learn and copy the arbitrary food preferences of others. Bonobos copied others... more Bonobos socially learn and copy the arbitrary food preferences of others. Bonobos copied others' arbitrary preferences of novel foods on first attempts. Subject age and exposure time have a positive effect on successful social learning. Copied food preferences can remain stable despite having better knowledge.
Revue de Primatologie, Jan 26, 2015
Bonobos live in dense forest habitats where visual communication is often limited rendering vocal... more 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.
Applied Animal Behaviour Science, 2021
Abstract In the European captive population of western lowland gorillas (Gorilla gorilla gorilla)... more Abstract 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.
Scientific Reports, Jan 24, 2019
the origin of human speech is still a hotly debated topic in science. evidence of socially-guided... more 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. The evolutionary origins of language and speech remains a fundamental question in science. In particular, whether clues to the origins of speech are present in nonhuman primate communication remains a hotly debated topic 1-4. Despite the diversity of social cultures and languages in humans, universal features in conversations are found across all languages, such as the avoidance of overlapping and a minimum gap between turns 5-8. Orderly vocal exchanges (antiphony between two or more animals or duets within male-female pairs 9) have been found across the primate order: from lemurs 10 , to New World monkeys 11-15 , Old World monkeys 16 and lesser apes 17,18. Vocal turn-taking appears to be associated with social life and cooperation capacities 1,2,5,9,19-21. It is thought to maintain and reinforce social bonds between individuals (e.g. in non-human primates 10,22), enable the extraction of information in the absence of overlap (e.g. 23 but see 24) and reduce stress as in the case of social grooming 25. Vocal exchange is "a characteristic communication style in which a sender produces a vocalization to address a receiver, and the receiver emits a call in response within a brief interval" (cited from 26). Vocal exchange patterns are influenced by social factors in non-human primates. 'Interlocutors' are not randomly selected, and preference is given to elders 11,27-29 , social allies 12,14,22 or dominant individuals 30,31. The attention of the audience also influences vocal outputs leading to persistence (repetition of calls) and elaboration (changes in the acoustic structure of calls) in situations where no response has been received 32,33. Shared primitive forms of vocal turn-taking within non-human primate species might suggest an ancient evolutionary origin 1,34. Surprisingly, however, studies based on great apes are scarce and controversial. No evidence of spontaneous vocal coordinated exchanges has been found in wild chimpanzees 35 , who display complex social interactions and cooperative abilities 36. Indeed, Arcadi 35 found that chimpanzees do not "respond" to the majority of calls they heard (within 5 sec), and that instead, bonded males tend to chorus together, matching each-other's pant hoots 37,38. Nevertheless, a recent study in great apes found for the first time that captive gorillas display some rule-governed call exchanges 31. Relying on our current knowledge, vocal turn-taking is thus reported across phylogenetically distant species (monkeys and more generally in some social mammals such as African elephants 39 , bottlenose dolphins 40 , bats 41,42 , naked mole-rats 43) but with some apparent discontinuities among great apes. More investigations among great ape species, our closest, highly social, relatives, are thus necessary in order to ascertain if vocal-turn taking behavior is as a result of convergent evolution (analogies as adaptations to similar social requirements) or is shared ancestry (homologies which are inheritance behaviours) 34 .
PLOS ONE, Apr 26, 2023
Individual variation in complex social behavioral traits, like primate grooming, can be influence... more Individual variation in complex social behavioral traits, like primate grooming, can be influenced by the characteristics of the individual and those of its social group. To better grasp this complexity, social network analysis can be used to quantify direct and indirect grooming relationships. However, multi-group social network studies remain rare, despite their importance to disentangle individual from group-level trait effects on grooming strategies. We applied social network analysis to grooming data of 22 groups of zoo-housed bonobos and investigated the impact of three individual (sex, age, and rearing-history) and two grouplevel traits (group size and sex ratio) on five social network measures (out-strength, instrength, disparity, affinity, and eigenvector centrality). Our results showed age-effects on all investigated measures: for females, all measures except for affinity showed quadratic relationships with age, while in males, the effects of age were more variable depending on the network measure. Bonobos with atypical rearing histories showed lower out-strength and eigenvector centrality, while in-strength was only impacted by rearing history in males. Group size showed a negative association with disparity and eigenvector centrality, while sex ratio did not influence any of the investigated measures. Standardization for group size did not impact the effects of sex and age, indicating the robustness of these findings. Our study provides comprehensive insights into the complexity of grooming behavior in zoohoused bonobos, and underlines the importance of multi-group analyses for the generalizability of social network analysis results for species as a whole.
PLOS ONE, Apr 26, 2023
Individual variation in complex social behavioral traits, like primate grooming, can be influence... more Individual variation in complex social behavioral traits, like primate grooming, can be influenced by the characteristics of the individual and those of its social group. To better grasp this complexity, social network analysis can be used to quantify direct and indirect grooming relationships. However, multi-group social network studies remain rare, despite their importance to disentangle individual from group-level trait effects on grooming strategies. We applied social network analysis to grooming data of 22 groups of zoo-housed bonobos and investigated the impact of three individual (sex, age, and rearing-history) and two grouplevel traits (group size and sex ratio) on five social network measures (out-strength, instrength, disparity, affinity, and eigenvector centrality). Our results showed age-effects on all investigated measures: for females, all measures except for affinity showed quadratic relationships with age, while in males, the effects of age were more variable depending on the network measure. Bonobos with atypical rearing histories showed lower out-strength and eigenvector centrality, while in-strength was only impacted by rearing history in males. Group size showed a negative association with disparity and eigenvector centrality, while sex ratio did not influence any of the investigated measures. Standardization for group size did not impact the effects of sex and age, indicating the robustness of these findings. Our study provides comprehensive insights into the complexity of grooming behavior in zoohoused bonobos, and underlines the importance of multi-group analyses for the generalizability of social network analysis results for species as a whole.
Animals
The welfare of captive animals relies on numerous factors. Keepers can affect animals’ welfare an... more The welfare of captive animals relies on numerous factors. Keepers can affect animals’ welfare and this could especially apply to emotionally and cognitively complex species, such as great apes. We collected video data over three months on 17 bonobos (La Vallée des Singes, France) and extracted five behaviours (play, aggression, anxiety, gestures, sociosexual interactions) —during two-minute slots—under three conditions: keeper-present/food-unavailable; keeper-present/food-available; keeper-absent/food-unavailable. We ran generalized linear models to investigate whether behavioral frequencies were affected by food presence/quality and keeper familiarity. Anxiety-related behaviors increased when the keeper was present and in absence of food, due to food expectation. Sociosexual interactions increased in presence of more familiar keepers and in absence of food, maybe to decrease the tension around food. Gestures increased in presence of more familiar keepers and with low-quality food,...
Revue de primatologie, 2015
La main humaine est consideree comme unique au travers certaines specificites fonctionnelles comm... more La main humaine est consideree comme unique au travers certaines specificites fonctionnelles comme l’individualisation des doigts et la capacite de saisir avec puissance un outil entre le pouce et le cote lateral de l'index. Cependant, les primates non-humains presentent de grandes capacites de manipulations. Ainsi, peut-on reellement affirmer que ces caracteristiques fonctionnelles humaines ne sont pas partagees par d'autres primates ? L'etude preliminaire menee ici a pour objectif d'analyser les strategies de manipulation chez des humains, adultes (N = 10 hommes, âge = 28 ± 5,92 ans) comme enfants (N = 10 garcons, âge = 5,3 ± 0,48) et des bonobos ("Pan paniscus") captifs (N = 6 dont 4 femelles et 2 mâles, âge = 20,33 ± 5,31) au cours d’une meme tâche necessitant la manipulation d'un outil. Cette nouvelle tâche consiste a recuperer une noix placee dans un labyrinthe en bois et ceci a travers un grillage. Les deux especes disposaient d'un choix varie de branches (divers tailles et diametres). Trois sessions par individu, une session correspondant a 1 noix recuperee, ont ete menees chez les bonobos comme les humains. Differents parametres ont ete quantifies comme le type de saisie (uni-manuelle versus bi-manuelle), de postures manuelles (e.g. puissance, precision) et la performance (basee sur les nombres de mouvements et d'obstacles touches). Les resultats montrent des differences inter et intra-specifiques et un effet de l'âge chez les humains pour certains parametres. Tout d'abord, les bonobos ont utilise un seul outil avec une seule main alors que les humains (adultes et enfants) ont employe en majorite des strategies bi-manuelles (65 %) et les adultes se sont parfois servis de deux outils (30 %). Concernant les saisies uni-manuelles, les bonobos ont utilise 32 formes de postures manuelles contre 26 pour les humains adultes et 125 pour les enfants. Au cours des saisies bi-manuelles, 4 fois plus de postures ont ete quantifiees. Par ailleurs, les enfants ont davantage utilise des saisies de puissance que les adultes qui ont principalement employe une saisie de precision a 3 doigts (e.g. tenue du stylo) pendant que les bonobos ont presente des preferences differenciees au niveau individuel. Pour finir, les adultes humains se sont montres plus performants que les bonobos, eux-memes plus performants que les enfants. L'utilisation des deux mains chez les humains pourrait s'expliquer par une saisie plus stable et puissante de l'outil pendant que l'utilisation de deux outils chez les adultes, plus complexe sur le plan de la coordination, pourrait apporter a certains individus une optimisation du trajet de la noix par dissociation des actions de la main droite versus de la main gauche (pousser vs controler). La plus grande variabilite des types de saisies chez les enfants pourrait s'expliquer par le manque d'experience et d'apprentissage dans les strategies de manipulation. Les bonobos presentent quant a eux des specificites individuelles pouvant traduire la specialisation de leurs strategies de manipulations. L'ensemble des resultats montre qu’il est necessaire d'approfondir les manipulations d'objets afin de mieux comprendre les specificites de chaque espece, et pas seulement humaines, et les causes des convergences parfois partagees. Seule une approche detaillee et comparative (inter et intra-specifique) nous permettra de discuter sous un nouvel angle l'emergence des eventuelles specificites humaines.
Scientific Reports
Different Old World primates show conspicuous anogenital swelling, with the Maximum Swelling Phas... more Different Old World primates show conspicuous anogenital swelling, with the Maximum Swelling Phase (MSP) signaling the ovulatory phase. MSP synchronization between females has been linked to social dynamics. In bonobos, characterized by female dominance, MSP is not a fully reliable signal of fertility because it may cover anovulatory periods. We investigated whether bonobo females synchronized their MSP and whether this phenomenon was modulated by social factors. Data were collected at LaValléedesSinges (France). In the period 2009–2022, swelling cycles data were collected daily on bonobo females (N = 9). In the period 2018–2022, ethological data (aggression/affiliation/socio-sexual behaviors) were also collected. We found that: (i) females synchronized their MSP and most likely experienced MSP onset following the MSP onset in other females; (ii) synchronization increased as the years spent together by females increased; (iii) synchronization preferentially occurred between females ...
Uploads
Papers by Jean-Pascal Guéry