Gestural communication in wild spider monkeys (Ateles geoffroyi).

Gestures play a central role in the communication systems of several animal families, including primates. In this study, we provide a first assessment of the gestural systems of a Platyrrhine species, Geoffroy's spider monkeys (Ateles geoffroyi). We observed a wild group of 52 spider monkeys and assessed the distribution of visual and tactile gestures in the group, the size of individual repertoires and the intentionality and effectiveness of individuals' gestural production. Our results showed that younger spider monkeys were more likely than older ones to use tactile gestures. In contrast, we found no inter-individual differences in the probability of producing visual gestures. Repertoire size did not vary with age, but the probability of accounting for recipients' attentional state was higher for older monkeys than for younger ones, especially for gestures in the visual modality. Using vocalizations right before the gesture increased the probability of gesturing towards attentive recipients and of receiving a response, although age had no effect on the probability of gestures being responded. Overall, our study provides first evidence of gestural production in a Platyrrhine species, and confirms this taxon as a valid candidate for research on animal communication.

Vigilance has mainly a social function in a wild group of spider monkeys (Ateles geoffroyi).

Vigilance is a widespread behavior that allows individuals to socially acquire information and/or effectively detect potential risks posed by predators and conspecifics. In this study, we aimed to investigate how social factors (i.e., subgroup size, number of males and immatures in the subgroup, presence of fission and fusion events, subgroup activity), individual characteristics (i.e., sex, presence of dependent offspring) and possible vulnerability to predation (i.e., being in smaller subgroups or lower in the canopy) explain variation in vigilance behavior in a wild group of spider monkeys (Ateles geoffroyi). We collected vigilance data during focal samples of all adults, subadults and juveniles of the group (N = 38), and ran generalized linear mixed models with a Bayesian approach. We found that the proportion of time both sexes spent in vigilance increased with subgroup size and during fusion events. Individuals also spent more time in vigilance when the subgroup was resting or socializing compared to other activities. Moreover, the proportion of time spent in vigilance increased in subgroups with more immatures. An alternative model with similar fit suggested that the proportion of time spent in vigilance increased in females when subgroups included more adult and subadult males. Overall, these results suggest that our study group mainly directed vigilance toward conspecifics (i.e., social vigilance), probably as a result of the relatively low predation pressure experienced, and contribute to the understanding of the multiple social factors affecting vigilance in group-living primates.

The effect of individual and food characteristics on food retrieval and food sharing in captive Guinea baboons (Papio papio).

Access to food is of major importance to the fitness and survival of every individual, particularly in group-living animals, in which individual characteristics and food distribution can affect food intake. Additionally, several species of primates are known to share food under certain conditions. Such unresisted transfer of food from one individual to another appears to be adaptive, for instance as a tool to maintain and reinforce social bonds. In this study, we aimed to test how food retrieval and food sharing varies depending on the social relationship between individuals, and on the characteristics of the food. In six different test conditions, we provided a captive group of Guinea baboons (Papio papio, N = 23) with multiple food items, differing in quality, quantity, density, monopolizability, and effort required to obtain it. We further used behavioral observations to assess individual relationships and possible variations in grooming exchanges linked to food sharing events. Out of 424 events in which food items were retrieved by the subjects, we detected no instances of active food sharing and only 17 of passive food sharing. The way food was retrieved was affected by individual and food characteristics (i.e., quantity, quality, and monopolizability of food): Males and central individuals (i.e., those connected to many partners, and/or having partners with many connections in the social network) were more likely to retrieve food during test conditions. In particular, events of passive food sharing mostly happened when the quality of food was low, and between individuals belonging to the same community (i.e., having close relationships). No other food characteristics affected the probability to share food, and the occurrence of food sharing had no immediate effect on grooming exchanges. Overall, our findings suggest that food sharing is relatively rare in Guinea baboons unless the food has a low quality and individuals form close social bonds.

Play behavior in immature moor macaques (Macaca maura) and Japanese macaques (Macaca fuscata).

Play is widespread across mammalian taxa, but species strongly vary in the ways they play. In less despotic primate species (i.e., with less steep dominance hierarchies, less severe conflicts, and more reconciliation), play has been described as being more frequent, cooperative, and freely expressed. To study the link between social play and dominance style, we compared play behavior in free-ranging infants, juveniles and subadults of more despotic Japanese macaques (Macaca fuscata, N = 24) and less despotic moor macaques (Macaca maura, N = 17). We found interspecific differences in play behavior that corresponded with the contrasting dominance styles of the study species, largely confirming our predictions. In particular, moor macaques spent a larger proportion of time in solitary and social play than Japanese macaques, while Japanese macaques spent a larger proportion of time in grooming interactions. In moor macaques, play sessions included more players, a larger variety of play behaviors, greater play face rates, a greater proportion of time in contact play, and a higher rate of reciprocal play-biting than in Japanese macaques. Aggressive escalations were not common, but more frequent in Japanese macaques. Finally, a higher frequency of play faces during play sessions predicted the occurrence of more reciprocal play-bites, but not the proportion of time spent in contact play behaviors. Additional studies on other groups and species will allow a better understanding of the link between dominance style and social play.

Bushmeat trade consequences predict higher anxiety, restraint, and dominance in chimpanzees.

More data are needed for a better understanding of the long-term influence of wider and combined stressful events in chimpanzee personality development. We evaluated the effects of bushmeat trade outcomes on the personality development in 84 African sanctuary chimpanzees. The chimpanzees presented different backgrounds regarding maternal care, social exposure, and abuse. We evaluated personality traits in chimpanzees using the Cattell 16PF personality questionnaire, the first application of this questionnaire in this species. We found that chimpanzees were rated as higher in anxiety after long social deprivation during infancy and juvenility, and if high human exposure was experienced. Mother-reared chimpanzees were rated as lower in restraint than hand-reared chimpanzees. Finally, mother-reared chimpanzees were rated as less dominant than hand-reared chimpanzees and rated higher when they had experienced severe mistreatment. Results suggest a wide range of possible stressful events could be potentially shaping rescued chimpanzees' personality and demonstrating the detrimental outcomes and consequences of the bushmeat and pet trade.

Impacts of illegal trade on socio-emotional and behavioural skills in macaques.

Decades of research have illuminated the consequences of early adverse rearing experiences in laboratory macaque populations. However, limited knowledge exists about the impact of traumatic episodes in non-laboratory environments. This study delves into the repercussions of illegal trade on socio-emotional and behavioural skills in five macaque species, all victims of poaching. We categorised their past experiences into seven aspects, encompassing maternal care and interactions with conspecifics. We assessed social engagement and cooperation by analysing social behaviours and employing the Social Responsiveness Scale. Emotional resilience was evaluated by measuring anxiety levels and the occurrence of abnormal behaviours, supported by a welfare questionnaire. Additionally, the introduction of Cattell's 16PF questionnaire in macaques for the first time aimed to reveal the influence of traumatic experiences on their personality traits. Our findings emphasise the significance of early social exposure. The lack of juvenile social contact predicts reduced social behaviours and an inclination towards social avoidance in adulthood. Macaques raised by humans tend to exhibit more abnormal behaviours in social contexts, compromising their welfare. Deprivation of social exposure in infancy negatively impacts psychological stimulation and overall welfare. The duration of time spent in illegal trade correlates with heightened anxiety levels. Personality traits such as 'Calmness' and 'Unfriendliness' are influenced by rearing conditions, with macaques deprived of social interaction during their early years showing higher levels of introversion. In conclusion, the absence of social exposure during early life and hand-rearing due to illegal trade significantly shape macaques' personality traits and their social and emotional skills.

Variation in neophilia in seven primate species.

Neophilia is a measure of individuals' attraction to novelty and is thought to provide important fitness benefits related to the acquisition of information and the ability to solve novel problems. Although neophilia is thought to vary across individuals and species, few studies have made direct comparisons to assess the factors that predict this variation. Here we operationalized neophilia as the probability of interacting with novel objects and compared the response to familiar and novel objects in 53 captive individuals belonging to seven different primate species: chimpanzees (Pan troglodytes), bonobos (Pan paniscus), Sumatran orangutans (Pongo abelii), gorillas (Gorilla gorilla), long-tailed macaques (Macaca fascicularis), tufted capuchin monkeys (Sapajus apella), and Geoffroy's spider monkeys (Ateles geoffroyi). Our results showed that individuals were overall more likely to interact with novel than familiar objects. Moreover, we found no evidence that neophilia varied across individuals depending on their sex, age, and dominance rank. However, macaques were overall less likely to interact with objects (regardless of their novelty), as compared to bonobos, orangutans, gorillas, and capuchin monkeys. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Assessing Eysenck's PEN model to describe personality in chimpanzees.

Questionnaires based on human models can be used to reliably assess personality also in non-human primates. In this study, we used an adapted version of Eysenck's Psychoticism-Extraversion-Neuroticism (PEN) model that focuses on three higher-order personality traits. Extending previous work on a small group of chimpanzees (Pan troglodytes), we tested 37 chimpanzees housed at Fundació Mona (Girona, Spain) and the Leipzig Zoo (Germany). We assessed personality with a 12-item questionnaire, which raters scored using a 7-point Likert scale. To identify the personality traits, we conducted data reduction with Principal Components Analysis and Robust Unweighted Least Squares. The ICCs for the single (3, 1) and average (3, k) ratings indicated substantial agreement between raters. Parallel analyses identified two factors to retain, whereas the scree plot inspection and eigenvalues larger than one rule identified three factors. Factor 1 and 2 in our study were identical to the ones previously described for this species (labelled Extraversion and Neuropsychoticism, respectively) and we also obtained a third factor that could be related to Dominance (Fearless Dominance). Thus, our results confirm the potential of the PEN model to describe chimpanzee personality structure.

Yawning and scratching contagion in wild spider monkeys (Ateles geoffroyi).

Behavioural contagion is a widespread phenomenon in animal species, which is thought to promote coordination and group cohesion. Among non-human primates, however, there is no evidence of behavioural contagion in Platyrrhines (i.e. primates from South and Central America) yet. Here, we investigated whether behavioural contagion is also present in this taxon, by assessing yawning and scratching contagion in a wild group (N = 49) of Geoffroy's spider monkeys (Ateles geoffroyi). We conducted focal samples to examine whether individuals observing the triggering event (i.e. a naturally occurring yawning or scratching event in the group) would be more likely to yawn or scratch in the following 3 min, as compared to individuals who did not observe the triggering event. We ran generalized linear mixed models using a Bayesian approach, and found that the probability of yawning and scratching was higher for individuals observing others yawning and scratching, respectively, as compared to individuals who did not observe such an event. Behavioural contagion did not vary depending on the observer's sex, kinship or relationship quality with the individual performing the triggering event. These findings provide the first evidence for yawning and scratching contagion in a wild group of spider monkeys, and importantly contribute to the debate about the evolutionary origins of behavioural contagion in primates.

Maternal Investment Fosters Male but Not Female Social Interactions with Other Group Members in Immature Wild Spider Monkeys (Ateles geoffroyi).

In several species, individuals form long-lasting social relationships with other group members, which provide them with important fitness benefits. In primates, patterns of social relationships are known to differ between sexes, but little is known about how these differences emerge through development or the role that mothers might have in this process. Here, we investigated how sex differences in social behaviour emerge during the first six years of primate life and how sex-biased maternal investment can foster immatures' social development and social interaction with other group members. For this purpose, we observed 20 males and females aged between zero and six years in a wild group of spider monkeys (Ateles geoffroyi) that was male-philopatric and, therefore, expected to show sex-biased maternal investment. Our results showed no sex difference in the social development of offspring with regards to body contact and grooming, but the probability of play was rather constant throughout age for females, whereas, for males, it became higher than females around two years of age, peaking between three and four years of age. Moreover, we found differences between female and male immatures in the importance of maternal investment (which included the time mothers spent nursing, carrying, grooming, touching and playing with their offspring) for their social integration in the natal group. In particular, maternal investment increased the probability of playing with other group members for sons, but not for daughters. Our findings suggest that mothers, through sex-biased maternal investment, might have a crucial function in the social development of spider monkeys, fostering the abilities that young offspring need to thrive as adults. By shedding light on maternal investment and social development in a still understudied primate species, these findings contribute to understanding the evolutionary roots of human maternal care and social development.

Hand preferences in coordinated bimanual tasks in non-human primates: A systematic review and meta-analysis.

The evolutionary significance of hand preferences among non-human primates and humans has been studied for decades with the aim of determining the origins of the population-level tendency. In this study, a meta-analysis was conducted to statistically integrate data on hand preferences in non-human primates performing the tube task and other bimanual tasks to determine the presence and direction of manual laterality. Significant individual-level lateralization was obtained for these bimanual tasks. In nonhuman primates, 82% of the animals analysed showed right or left-hand preference performing the tube task, this figure being 90% for other bimanual tasks. In contrast with humans, no asymmetry was found at the population level. Additionally, population-level preferences were not found in either of the tasks, although a strong manual preference was found when performing the tube task and other bimanual tasks. Species was studied as a variable moderator throughout the meta-analysis. These results highlight the importance of standardized testing methodologies across species and institutions to obtain comparable data and fill the gaps in the taxonomy.

Cognitive enrichment in a social setting: assessing the use of a novel food maze in sanctuary-housed chimpanzees.

Foraging devices are effective enrichment tools for non-human primates, as they provide both cognitive and manipulative stimulation that may enhance these animals' welfare. We assessed the behavioral effects of a novel tool-based enrichment on 14 chimpanzees (Pan troglodytes) housed at Fundació Mona (Girona, Spain). The device consisted of a vertical maze filled with food rewards, which chimpanzees could extract by using tools. We conducted behavioral observations in two conditions over an approximately 2.5-month period: when the food maze was loaded (12 enrichment days), and when it was empty (12 baseline days). Data were collected using 2-min scan sampling and untimed-event focal sampling during two daily sessions of 80 min each. We expected that the chimpanzees' interest in the enrichment would decrease over time, but that its use would be linked to an increase in the occurrence of species-typical behaviors, a reduction in negative indicators of welfare, and changes in social behaviors. We found that participation widely varied among subjects, being higher in females and decreasing through time. Furthermore, participation was linked to an increase in tool use and a decrease in inactivity, but also to an increase in aggression-related behaviors. In contrast, participation had no effect on the occurrence of abnormal behaviors, social proximity or affiliation-related behaviors. Finally, we detected an increase in self-directed behaviors only when subjects actively interacted with the device. We conclude that, in future studies, these types of devices should be evaluated for longer periods of time and more attention should be paid to individuals' preferences and abilities.

Mechanisms of expression of object play: A comparative study of stone handling in two captive groups of long-tailed macaques (Macaca fascicularis fascicularis).

Stone handling (SH) is a form of solitary object play that is socially learned and culturally maintained. We studied two captive groups (Modena, N = 20; Padova, N = 20) of common long-tailed macaques housed in a sanctuary in Italy. Our research goal was two-fold: (1) establish the first SH repertoire in captive-raised long-tailed macaques, and (2) explain major differences in the expression of SH between the two study groups. Despite being of identical size and sharing similar environmental conditions, we found that SH was performed by most group members in Modena, whereas SH was absent in Padova. We aimed to explain this inter-group variation by exploring the role of proximate factors that are known to affect the occurrence of SH: demography, dominance, stone availability, activity budget, and food provisioning. The atypical age structure of Padova (i.e., no immature individuals) may have impaired the emergence of SH in this group. In Modena, we found no significant effect of hierarchical rank on SH frequency and duration and no temporal relationship between SH and feeding. Regarding the activity budget, SH filled in for a portion of affiliative and resting behaviours in Modena. Our findings lend support to the cultural nature of SH.

The Habituation Process in Two Groups of Wild Moor Macaques (Macaca maura).

When studying animal behavior in the wild, some behaviors may require observation from a relatively short distance. In these cases, habituation is commonly used to ensure that animals do not perceive researchers as a direct threat and do not alter their behavior in their presence. However, habituation can have significant effects on the welfare and conservation of the animals. Studying how nonhuman primates react to the process of habituation can help to identify the factors that affect habituation and implement habituation protocols that allow other researchers to speed up the process while maintaining high standards of health and safety for both animals and researchers. In this study, we systematically described the habituation of two groups of wild moor macaques (Macaca maura), an Endangered endemic species of Sulawesi Island (Indonesia), to assess the factors that facilitate habituation and reduce impact on animal behavior during this process. During 7 months, we conducted behavioral observations for more than 7,872 encounters and an average of 120 days to monitor how macaque behavior toward researchers changed through time in the two groups under different conditions. We found that both study groups (N = 56, N = 41) became more tolerant to the presence of researchers during the course of the habituation, with occurrence of neutral group responses increasing, and minimum distance to researchers and occurrence of fearful group responses decreasing through time. These changes in behavior were predominant when macaques were in trees, with better visibility conditions, when researchers maintained a longer minimum distance to macaques and, unexpectedly, by the presence of more than one researcher. By identifying these factors, we contribute to designing habituation protocols that decrease the likelihood of fearful responses and might reduce the stress experienced during this process.

Population dynamics and genetic connectivity in recent chimpanzee history.

Knowledge on the population history of endangered species is critical for conservation, but whole-genome data on chimpanzees (Pan troglodytes) is geographically sparse. Here, we produced the first non-invasive geolocalized catalog of genomic diversity by capturing chromosome 21 from 828 non-invasive samples collected at 48 sampling sites across Africa. The four recognized subspecies show clear genetic differentiation correlating with known barriers, while previously undescribed genetic exchange suggests that these have been permeable on a local scale. We obtained a detailed reconstruction of population stratification and fine-scale patterns of isolation, migration, and connectivity, including a comprehensive picture of admixture with bonobos (Pan paniscus). Unlike humans, chimpanzees did not experience extended episodes of long-distance migrations, which might have limited cultural transmission. Finally, based on local rare variation, we implement a fine-grained geolocalization approach demonstrating improved precision in determining the origin of confiscated chimpanzees.

Population-level right-handedness for a coordinated bimanual task in naturalistic housed chimpanzees: replication and extension in 114 animals from Zambia and Spain.

Recently, many studies have been conducted on manual laterality in chimpanzees. Nevertheless, whether nonhuman primates exhibit population-level handedness remains a topic of considerable debate. One of the behaviors studied has been bimanual coordinated actions. Although recent studies have highlighted that captive chimpanzees show handedness at population level for these tasks, some authors have questioned the validity and consistency of these results. The first reason has been the humanization of the samples. The second one has been that the results refer to animals in American biomedical centers and the studies were conducted by the same team [WD Hopkins et al.]. This article aims to assess the laterality in bimanual coordination (tube task) activities in animals housed in an intermediate environment (Chimfunshi, Zambia). This has been conducted by replicating previous studies on similar samples (Mona Foundation, Spain), and then by extending the results to chimpanzees housed in intermediate settings. Individuals were evaluated through four experimental sessions (tests). Results indicated that 86% of the Chimfunshi sample was lateralized (48% RH, 38% LH). Furthermore, the sample showed population-level right-handedness in the mean handedness index, in Test 1, Test 2, and the first half of the study (Test 112). Rearing experience did not have an influence on handpreference. Taken together, the two sample (intermediate settings: Chimfunshi and Mona) results indicate a clear right-handedness. In conclusion, this replication and extension shows that (1) the Mona and Chimfunshi chimpanzees are right-handed in certain conditions, (2) the results are consistent with those obtained by Hopkins in captive settings, (3) the humanization of the samples does not affect manual laterality, (4) females are right-handed at population-level, but not males, and (5) these results reinforce the fact that the complexity of the task plays a dominant role in the expression of hand laterality among chimpanzees.

Hand preference for a bimanual coordinated task in captive hatinh langurs (Trachypithecus hatinhensis) and grey-shanked douc langurs (Pygathrix cinerea).

Right-handedness in humans reflects the functional brain specialisation of the left hemisphere. To better understand the origins of this population-level tendency, it is crucial to understand manual lateralisation in other non-human primate species. The aim of this article is to present a first approach to the hand preference of two primates from Vietnam, the endangered hatinh langur (Trachypithecus hatinhensis) and the critically endangered grey-shanked douc langur (Pygathrix cinerea). Eighteen individuals from each species (N = 36) were evaluated by means of the bimanual coordinated tube task and their responses were recorded in terms of manual events and bouts. Our results showed that subjects presented strong individual-level preferences but not lateralisation at the group-level. No sex differences were detected within species. The index finger was used in all of the extractions during this bimanual task, alone (86 %) or in combination with other fingers (14 %). In addition, hatinh langurs exhibited a greater strength of hand preferences than grey-shanked douc langurs, pointing to a possible higher manual specialisation during the leaf-eating process. These findings help to broaden our scarce knowledge of manual laterality in Asian colobine monkeys and confirm the bimanual tube task as a sensitive measure for assessing manual laterality in non-human primates.

Invasive Research on Non-Human Primates-Time to Turn the Page.

Invasive research on primates (i.e., laboratory research that implies body manipulations causing pain or distress that is not aimed to directly improve the individuals' well-being) has a long history. Although some invasive studies have allowed answering research questions that we could not have addressed with other methods (or at least not as quickly), the use of primates in invasive research also raises ethical concerns. In this review, we will discuss (i) recent advances in the study of primates that show evidence of complex behaviour and cognition, (ii) welfare issues that might arise when using primates in invasive research, (iii) the main ethical issues that have been raised about invasive research on primates, (iv) the legal protection that primates are granted in several countries, with a special focus on the principle of the 3Rs, and (v) previous and current attempts to ban the use of primates in invasive research. Based on this analysis, we suggest that the importance of a research question cannot justify the costs of invasive research on primates, and that non-invasive methods should be considered the only possible approach in the study of primates.

Is There a "Right" Side of Communicating Friendship? Lateralization of Social Interactions in Zoo Barbary macaques (Macaca sylvanus).

Social laterality in non-human primates has started to attract attention in recent years. The positioning of individuals during social interactions could possibly suggest the nature of a relationship and the social ranking of the subjects involved. The subjects of the present study were 12 adult Barbary macaques (Macaca sylvanus) housed in a zoological garden. We carried out fourteen 210-min video-recorded sessions and we used a focal animal sampling method to collect the position of the subjects during different social interactions. Data on the position of each macaque during three types of social interactions were collected (approach, proximity and affiliative contacts). Moreover, we focused on the outcomes of dyadic agonistic encounters to build the hierarchy of the colony. For each social interaction, two conditions were considered: the side preference (being kept on the left or on the right) and the sagittal preference (being kept in front or on the rear). Bouts of preference of different positions were collected for different social interactions (approach, proximity and contacts). No group-level side preferences were found for any social interaction, suggesting that both hemispheres might be complemental and balance each other during intraspecific communication. For the sagittal preference, we found a group-level bias for proximity, with macaques being kept in front rather than on the rear by close conspecifics. This might be due to the need to detect emotions and intentions of conspecifics. Moreover, high-ranking individuals are kept more frontally than on the rear when in proximity with other macaques. More studies are needed to better investigate social laterality, possibly distinguishing more categories of social interaction, and detecting other variables that might influence the positioning preferences.