Tolerant macaque species are less impulsive and reactive.

Inhibitory control, the inhibition of impulsive behaviours, is believed to be key in navigating a complex social environment. Species characterised by higher social tolerance, living in more complex groups, with more diverse relationships, face higher uncertainty regarding the outcome of social interactions and, therefore, would benefit from employing more inhibitory strategies. To date, little is known about the selective forces that favour the evolution of inhibitory control. In this study, we compared inhibitory control skills in three closely related macaque species which differ in their social tolerance style. We tested 66 macaques from two institutions (Macaca mulatta, low tolerance; M. fascicularis, medium tolerance; and M. tonkeana, high tolerance) using a battery of validated inhibitory control touchscreen tasks. Higher social tolerance was associated with enhanced inhibitory control performances. More tolerant species were less impulsive and less distracted by pictures of unknown conspecifics. Interestingly, we did not find evidence that social tolerance degree was associated with performance in reversal learning. Overall, our results support the hypothesis that evolution has promoted the development of socio-cognitive skills to cope with the demands related to the complexity of the social environment.

Spot the odd one out: do snake pictures capture macaques' attention more than other predators?

Detecting and identifying predators quickly is key to survival. According to the Snake Detection Theory (SDT), snakes have been a substantive threat to primates for millions of years, so that dedicated visual skills were tuned to detect snakes in early primates. Past experiments confronted the SDT by measuring how fast primate subjects detected snake pictures among non-dangerous distractors (e.g., flowers), but did not include pictures of primates' other predators, such as carnivorans, raptors, and crocodilians. Here, we examined the detection abilities of N = 19 Tonkean macaques (Macaca tonkeana) and N = 6 rhesus macaques (Macaca mulatta) to spot different predators. By implementing an oddity task protocol, we recorded success rates and reaction times to locate a deviant picture among four pictures over more than 400,000 test trials. Pictures depicted a predator, a non-predator animal, or a simple geometric shape. The first task consisted of detecting a deviant picture among identical distractor pictures (discrimination) and the second task was designed to evaluate detection abilities of a deviant picture among different distractor pictures (categorization). The macaques detected pictures of geometric shapes better and faster than pictures of animals, and were better and faster at discriminating than categorizing. The macaques did not detect snakes better or faster than other animal categories. Overall, these results suggest that pictures of snakes do not capture visual attention more than other predators, questioning previous findings in favor of the SDT.

Individual differences in co-representation in three monkey species (Callithrix jacchus, Sapajus apella and Macaca tonkeana) in the joint Simon task: the role of social factors and inhibitory control.

Behavioral coordination is involved in many forms of primate interactions. Co-representation is the simultaneous mental representation of one's own and the partner's task and actions. It often underlies behavioral coordination and cooperation success. In humans, the dyadic social context can modulate co-representation. Here, we first investigated whether individual differences in co-representation in the joint Simon task in capuchin monkeys and Tonkean macaques can be explained by social factors, namely dyadic grooming and sociality index, rank difference and eigenvector centrality. These factors did not predict variation in co-representation. However, in this specific task, co-representation reduces rather than facilitates joint performance. Automatic co-representation therefore needs to be inhibited or suppressed to maximize cooperation success. We therefore also investigated whether general inhibitory control (detour-reaching) would predict co-representation in the joint Simon task in Tonkean macaques, brown capuchin and marmoset monkeys. Inhibitory control did neither explain individual differences nor species differences, since marmosets were most successful in their joint performance despite scoring lowest on inhibitory control. These results suggest that the animals' ability to resolve conflicts between self and other representation to increase cooperation success in this task is gradually learned due to frequent exposure during shared infant care, rather than determined by strong general inhibitory control. Further, we conclude that the joint Simon task, while useful to detect co-representation non-invasively, is less suitable for identifying the factors explaining individual differences and thus a more fruitful approach to identify these factors is to design tasks in which co-representation favors, rather than hinders cooperation success.

Development and validation of a new method for visual acuity assesment on tablet in pediatric population: eMOVA test.

BACKGROUND: Amblyopia is a major public health concern. Its screening and management require reliable methods of visual acuity assessment. New technologies offer nowadays many tests available on different app stores for smartphone or tablet but most of them often lack of scientific validation for a medical use. The aim of our study was to attempt validating a tablet-based near visual acuity test adapted to the pediatric population: the eMOVA test (electronic Measurement Of Visual Acuity) by comparing visual acuity measured with more conventional test. METHODS: A cohort of 100 children aged 3 to 8 attending the ophthalmic-pediatric for eye examination between September 2016 and June 2017 were included in the study. Near visual acuity was assessed on participants using both the eMOVA test and a Standard test (Rossano-Weiss test). Duration of each test, its comprehension, its acceptability and the attention of the child during the test was also investigated. RESULTS: The eMOVA test overestimated near visual acuity by 0.06 logMAR. This difference, statistically significant, was not clinically relevant. The duration of the eMOVA test was longer than the reference test, but less discomfort and preferred by children and their parents compared to standard tests. CONCLUSION: The eMOVA test appears as a reliable test to assess near visual acuity in children. By its portability and efficiency, this application proved to be a relevant tool to be used for children eye examination in daily routine at the hospital.

Effects of social tolerance on stress: hair cortisol concentrations in the tolerant Tonkean macaques (Macaca tonkeana) and the despotic long-tailed macaques (Macaca fascicularis).

Group living is a source of stress and an individuals' social environment has been shown to have a significant effect on its health and well-being. However, little is known about how different social organizations affect the stress levels of their members. Is living in a hierarchical society more or less stressful than living in a more tolerant structure? Here, we assess cortisol concentrations in the hair of two macaque species with radically different dominance styles: the egalitarian Tonkean macaque (Macaca Tonkeana) and the despotic long-tailed macaques (Macaca fascicularis). Hair was sampled in winter and again in late spring in two mixed-sex groups of 22 Tonkean macaques and 9 long-tailed macaques; Hair cortisol concentrations were significantly higher in the egalitarian Tonkean macaques than in the despotic long-tailed macaques, ranging from 161.13 to 938.8 pg/mg (mean ± SD 349.67 ± 126.22) and from 134.46 to 339.86 pg/mg (mean ± SD 231.2 ± 44.24), respectively. There was no difference between male and female cortisol concentrations, but hair cortisol increased with age in males. Dominance rank certainty was lower among female Tonkean macaques compared to long-tailed macaques. Our results suggest that species differences in dominance styles may translate into differences in long-term cortisol concentrations. We suggest that the higher cortisol concentrations in Tonkean macaques could be linked to the instability and lack of predictability and control around social relationships.

LAY SUMMARYBeing part of a social group can be very stressful, depending on the social structure of this group. We found that the more socially tolerant Tonkean macaques exhibited on average higher hair cortisol concentrations than more despotic long-tailed macaques. Males and females exhibited similar concentrations of hair cortisol in both species, but in male Tonkean macaques concentrations increased with age. The finding that overall cortisol levels were higher in the more tolerant species suggests that psychological arousal due to unpredictable social relations and mating competition may be an important driver of cortisol release in this species despite its overall tolerant social organization.

An autonomous, automated and mobile device to concurrently assess several cognitive functions in group-living non-human primates.

Research methods in cognitive neuroscience using non-human primates have undergone notable changes over the last decades. Recently, several research groups have described freely accessible devices equipped with a touchscreen interface. Two characteristics of such systems are of particular interest: some apparatuses include automated identification of subjects, while others are mobile. Here, we designed, tested and validated an experimental system that, for the first time, combine automatization and mobility. Moreover, our system allows autonomous learning and testing of cognitive performance in group-living subjects, including follow-up assessments. The mobile apparatus is designed to be available 24h a day, 7days a week, in a typical confined primate breeding and housing facility. Here we present as proof of concept, the results of two pilot studies. We report that rhesus macaques (Macaca mulatta) learned the tasks rapidly and achieved high-level of stable performance. Approaches of this kind should be developed for future pharmacological and biomedical studies in non-human primates.

Behavioral and functional strategies during tool use tasks in bonobos.

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.

Do bimanual coordination, tool use, and body posture contribute equally to hand preferences in bonobos?

Approximately 90% of the human population is right-handed. The emergence of this hand preference in humans is thought to be linked to the ability to execute complex tasks and habitual bipedalism. In order to test these hypotheses, the present study explored, for the first time, hand preference in relation to both body posture (seated and bipedal) and task complexity (bimanual coordination and two tool use tasks of different complexity) in bonobos (Pan paniscus). Few studies have explored the effects of both posture and task complexity on handedness, and investigations with bonobos are scarce, particularly studies on tool use. Our study aims to overcome such a gap by addressing two main questions: 1) Does a bipedal posture increase the strength of hand preference and/or create a directional bias to the use of the right hand? 2) Independent of body posture, does task complexity increase the strength of the hand preference and/or create a directional bias to the use of the right hand? Our results show that independent of body posture, the more complex the task, the more lateralization occurred. Moreover, subjects tended to be right-handed for tasks involving tool use. However, posture had no significant effect on hand preference in the tasks tested here. Therefore, for a given task, bonobos were not more lateralized in a bipedal posture than in a seated one. Task complexity might thus have contributed more than bipedal posture to the emergence of human lateralization and the preponderance of right-handedness, although a larger sample size and more data are needed to be conclusive.

Intentional gestural communication and discrimination of human attentional states in rhesus macaques (Macaca mulatta).

The present study tested intentionality of a learned begging gesture and attention-reading abilities in rhesus macaques (Macaca mulatta). Subjects were trained to produce a begging gesture towards a hidden food reward that could be delivered by a human experimenter. More specifically, we investigated which attentional cues--body, face and/or eyes orientation of a human partner--were taken into account by the macaques in order to communicate with her. Our results provide strong evidence of intentional communication: the monkeys adjusted their behaviour to that of the partner. The latter's attentional state influenced the monkeys' likelihood of performing begging gestures and showing gaze alternation between the partner and the hidden food. By contrast, we found no evidence of attention-getting behaviours, persistence or elaboration of new communicative behaviours. Our results also showed that rhesus macaques discriminated gross cues including the presence, body and face orientation of the human experimenter but not her eyes. However, the monkeys emitted more gaze alternation and monitored the human's attentional state more closely when she also displayed gaze alternation, suggesting an important role of joint attention in gestural communication.

Do Tonkean macaques (Macaca tonkeana) tailor their gestural and visual signals to fit the attentional states of a human partner?

We tested here whether Tonkean macaques (Macaca tonkeana), trained to produce a pointing gesture, modify their behaviour in response to different human's attentional states. More specifically, we investigated the macaque's ability to communicate intentionally about the location of an unreachable hidden food reward in several contexts which differ by the human partner's attentional state. The experimenter displayed seven attentional states differing on the basis of body, head and gaze orientation. Our study validates several criteria of an intentional communication. We showed that macaques produce more pointing gestures when an audience, i.e. the human partner, is present than absent. We also revealed an adjustment of gaze alternation between the face of the experimenter and the hidden food reward according to several experimental conditions. However, in our study, macaques did not produce auditory attention-getting behaviours when the human partner was inattentive. Finally, only rough cues, i.e. presence, body and face orientation of the observer, seem to be taken into account by macaques. However, our results also supposed the importance of joint attention for macaques since they display more gaze alternation when the head and/or eyes of the human partner are mobile.

Tufted capuchins (Cebus apella) adapt their communicative behaviour to human's attentional states.

Animal communication has become a widely studied field of research, especially because of the associated debates on the origin of human language. Due to their phylogenetic proximity with humans, non-human primates represent a suitable model to investigate the precursors of language. This study focuses on the perception of the attentional states of others, an important prerequisite to intentional communication. We investigated whether capuchins (Cebus apella) produce a learnt pointing gesture towards a hidden and unreachable food reward as a function of the attentional status of the human experimenter. For that purpose, we tested five subjects that we first trained to indicate by a pointing gesture towards the human partner the position of a reward hidden by an assistant. Then, capuchins were tested in two experimental conditions randomly ordered. In the first condition-motivation trial-the experimenter was attentive to the subject gestures and rewarded him immediately when it pointed towards the baited cylinder. During the second condition-test trial-the experimenter adopted one of the following attention states and the subject was rewarded after 10 s has elapsed, regardless of the subject's behaviour. Five attentional states were tested: (1) experimenter absent, (2) experimenter back to the monkey, (3) experimenter's head away, (4) experimenter watching above the monkey, and (5) experimenter watching the monkey face. Our results reveal a variation in our subjects' communicative behaviours with a discrimination of the different postural clues (body and head orientation) available in our experimental conditions. This study suggests that capuchins can flexibly use a communicative gesture to adapt to the attentional state of their partner and provides evidence that acquired communicative gestures of monkeys might be used intentionally.

Is self-awareness necessary to have a theory of mind?

Forty years ago, Gallup proposed that theory of mind presupposes self-awareness. Following Humphrey, his hypothesis was that individuals can infer the mental states of others thanks to the ability to monitor their own mental states in similar circumstances. Since then, advances in several disciplines, such as comparative and developmental psychology, have provided empirical evidence to test Gallup's hypothesis. Herein, we review and discuss this evidence.

Olive baboons communicate intentionally by pointing.

A pointing gesture creates a referential triangle that incorporates distant objects into the relationship between the signaller and the gesture's recipient. Pointing was long assumed to be specific to our species. However, recent reports have shown that pointing emerges spontaneously in captive chimpanzees and can be learned by monkeys. Studies have demonstrated that both human children and great apes use manual gestures (e.g. pointing), and visual and vocal signals, to communicate intentionally about out-of-reach objects. Our study looked at how monkeys understand and use their learned pointing behaviour, asking whether it is a conditioned, reinforcement-dependent response or whether monkeys understand it to be a mechanism for manipulating the attention of a partner (e.g. a human). We tested nine baboons that had been trained to exhibit pointing, using operant conditioning. More specifically, we investigated their ability to communicate intentionally about the location of an unreachable food reward in three contexts that differed according to the human partner's attentional state. In each context, we quantified the frequency of communicative behaviour (auditory and visual signals), including gestures and gaze alternations between the distal food and the human partner. We found that the baboons were able to modulate their manual and visual communicative signals as a function of the experimenter's attentional state. These findings indicate that monkeys can intentionally produce pointing gestures and understand that a human recipient must be looking at the pointing gesture for them to perform their attention-directing actions. The referential and intentional nature of baboons' communicative signalling is discussed.

Hand preferences on unimanual and bimanual tasks in Tonkean macaques (Macaca tonkeana).

This is the first study to examine hand preferences in Tonkean macaques on a bimanual task. One of our objectives was to continue the move toward greater task standardization, in order to facilitate comparisons between species and studies on handedness. The main aim was to test and determine task robustness, by varying intra-task complexity. To this end, we administered several different tasks to the subjects: two unimanual tasks (grasping task featuring items of different sizes) and three coordinated bimanual tasks (tube task involving different materials, weights, and diameters). Although we found no significant hand preference in either task at the group level, the macaques were more strongly lateralized for small items than for large ones in the unimanual grasping task. Moreover, the absence of a correlation between these two versions of the unimanual task confirmed the weakness of this grasping task for assessing handedness. Regarding the bimanual tube task, no difference was found between the three versions in either the direction or the strength of hand preference. Moreover, the highly correlated hand preferences between these three versions suggest that the tube task provides a more robust means of measuring manual preferences.

Baboons' hand preference resists to spatial factors for a communicative gesture but not for a simple manipulative action.

Olive baboons (Papio anubis) do acquire and use intentional requesting gestures in experimental contexts. Individual's hand preference for these gestures is consistent with that observed for typical communicative gestures, but not for manipulative actions. Here, we examine whether the strength of hand preference may also be a good marker of hemispheric specialization for communicative gestures, hence differing from the strength of hand preference for manipulative actions. We compared the consistency of individuals' hand preference with regard to the variation in space of either (i) a communicative partner or (ii) a food item to grasp using a controlled set-up. We report more consistent hand preference for communicative gestures than for grasping actions. Established hand preference in the midline was stronger for gesturing than for grasping and allowed to predict the consistency of hand preference across positions. We found no significant relation between the direction of hand preference and the task.

Patterns of hemispheric specialization for a communicative gesture in different primate species.

We review four studies investigating hand preferences for grasping versus pointing to objects at several spatial positions in human infants and three species of nonhuman primates using the same experimental setup. We expected that human infants and nonhuman primates present a comparable difference in their pattern of laterality according to tasks. We tested 6 capuchins, 6 macaques, 12 baboons, and 10 human infants. Those studies are the first of their kind to examine both human infants and nonhuman primate species with the same communicative task. Our results show remarkable convergence in the distribution of hand biases of human infants, baboons and macaques on the two kinds of tasks and an interesting divergence between capuchins' and other species' hand preferences in the pointing task. They support the hypothesis that left-lateralized language may be derived from a gestural communication system that was present in the common ancestor of macaques, baboons and humans.

Revisiting the mark test for mirror self-recognition.

Despite half a century of research, few species have exhibited convincing evidence of mirror self-recognition. Several methodological objections to Gallup's mark test have been raised, but empirical studies have shown that methodology does not adequately explain why most species fail to recognize themselves in mirrors. However, a potential issue was constantly overlooked: mirror ecological relevance. Although reflective surfaces in nature are horizontal, previous studies indeed used vertical mirrors. The present study revisited the mark test to address this issue in an experiment with capuchin monkeys (Sapajus apella). Additionally, a new procedure based on sticker exchange was designed to maximize mark attractiveness. Subjects were first trained to exchange stickers, habituated to being head-touched, and exposed to a horizontal mirror. Then, their mirror self-recognition was tested by surreptitiously placing a sticker on their forehead before requesting them to exchange stickers. None of the monkeys removed the sticker from their forehead in the presence of the mirror. In line with previous studies, this result suggests that capuchin monkeys lack the ability to recognize themselves in mirrors. Nonetheless, this modified mark test could prove useful in future studies, including investigation of interindividual variability of mirror self-recognition in self-recognizing species.

Is this worth the trouble? Strategic conflict management in Tonkean macaques.

Conflict management entails preventing and repairing damages resulting from social conflicts. While previous research has emphasized post-conflict actions like reconciliation, the understanding of how primates weigh the costs and benefits of conflict remains limited. Uncovering this hidden but fundamental aspect of conflict management requires addressing actively avoided social conflicts. In a study involving semi-free ranging Tonkean macaques, individuals were presented with social dilemmas: displacing a peer to access a preferred juice reward or opting for a peer-free but less preferred one to avoid conflict. The results showed that subjects attributed a cost to the social conflict and did not demonstrate a systematic drive to dominate. Decision modeling revealed integration of peer hierarchy and reward subjective value, with subjects' own social rank impacting the balance between these social and economic dimensions. Overall, this research highlights how primates strategically address group cohesion and peacekeeping, sometimes at the expense of personal preferences.

Comparative genomics reveals the hybrid origin of a macaque group.

Although species can arise through hybridization, compelling evidence for hybrid speciation has been reported only rarely in animals. Here, we present phylogenomic analyses on genomes from 12 macaque species and show that the fascicularis group originated from an ancient hybridization between the sinica and silenus groups ~3.45 to 3.56 million years ago. The X chromosomes and low-recombination regions exhibited equal contributions from each parental lineage, suggesting that they were less affected by subsequent backcrossing and hence could have played an important role in maintaining hybrid integrity. We identified many reproduction-associated genes that could have contributed to the development of the mixed sexual phenotypes characteristic of the fascicularis group. The phylogeny within the silenus group was also resolved, and functional experimentation confirmed that all extant Western silenus species are susceptible to HIV-1 infection. Our study provides novel insights into macaque evolution and reveals a hybrid speciation event that has occurred only very rarely in primates.

Hand preference and its flexibility according to the position of the object: a study in cercopithecines examining spontaneous behaviour and an experimental task (the Bishop QHP task).

The extant literature on manual laterality in non-human primates is inconclusive, plagued by inconsistent or contradictory findings and by disturbing methodological issues (e.g. uncontrolled influential factors, comparability issues). The present study examined hand preference and its flexibility in 15 red-capped mangabeys (C. t. torquatus) and 13 Campbell's monkeys (C. c. campbelli), two species that differ in their degree of arboreality. We investigated the influence of the spatial position of the object on hand preference for reaching. We considered spontaneous behaviour (reaching for food during daily feeding) and an experimental task: the QHP task. The QHP is a task that is used in humans. This is a simple reaching task that involves high spatial constraints on hand use. In our study, the subject had to reach for items that were placed on a semi-circle in front of it on five positions, including in the centre position, in the ipsilateral space and in the contralateral space. We assessed hand preference for reaching in front (baseline condition), and we examined how this preference changed when reaching in lateral positions. For reaching in front, about half of the subjects were lateralized and no group-level bias occurred, for both spontaneous and experimental conditions. When considering reaching in the lateral positions, we observed that the position of the object influenced hand use: individuals used the hand that was closest to the object. The results are discussed in relation to previous findings in humans and in non-human primates and regarding theories on handedness and flexibility of hand preference.