The consistency of individual centrality across time and networks in wild vervet monkeys.

Previous primate social network studies largely limited their focus to grooming and/or aggression networks, particularly among adult females. In addition, the consistency of individuals' network centrality across time and/or different networks has received little attention, despite this being critical for a global understanding of dynamic social structure. Here, we analyzed the grooming, aggression, and play social networks of a group of 26-28 wild vervet monkeys (Chlorocebus pygerythrus), including adults and juveniles, over two periods of 6 months. We collected data on grooming, play, and aggression using focal animal sampling with instantaneous recording and ad libitum sampling. We examined whether individuals' network centralities were consistent over the two periods and across networks, as well as the effect of age, sex, and dominance rank on three individual centrality metrics in each network and within each study period. We found that individuals were quite consistent in their network position from 1 year to the next despite changes in group composition. However, their network centralities were not correlated across networks, except for Strength and weighted Eigenvector centrality between grooming and aggression networks. We also found that in the aggression network, high-rankers showed the highest centrality in most network metrics (e.g., Degree, Strength, and Eigenvector centrality) and compared to males, females were most central in 2017 but not in 2018. In the grooming network, high-ranking females had the highest Eigenvector centrality, whereas in the play network, juvenile males had the highest Eigenvector centrality. Our findings corroborate previous findings on vervet monkeys. In addition, they show that individuals' network centralities may vary among networks and over time; thus highlighting the effect of sociodemographics and behaviors' functions on the group level dynamics of social behavior.

The effects of data collection and observation methods on uncertainty of social networks in wild primates.

In social species, network centralities of group members shape social transmission and other social phenomena. Different factors have been found to influence the measurement of social networks, such as data collection and observation methods. In this study, we collected data on adults and juveniles and examined the effect of data collection method (ad libitum sampling vs. focal animal sampling) and observation method (interaction-grooming; play-vs. association-arm-length; 2 m; 5 m proximities-) on social networks in wild vervet monkeys. First, we showed using a bootstrapping method, that uncertainty of ad libitum grooming and play matrices were lesser than uncertainty of focal matrices. Nevertheless, grooming and play networks constructed from ad libitum and focal animal sampling were very similar and highly correlated. We improved the certainty of both grooming and play networks by pooling focal and ad libitum matrices. Second, we reported a high correlation between the proximity arm-length network and the focal grooming one making an arm-length proximity network a reasonable proxy for a grooming one in vervet monkeys. However, we did not find such a correlation between proximity networks and the play one. Studying the effects of methodological issues as data collection and observation methods can help improve understanding of what shapes social networks and which data collection method to choose to study sociality.

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.

Training experience in gestures affects the display of social gaze in baboons' communication with a human.

Gaze behaviour, notably the alternation of gaze between distal objects and social partners that accompanies primates' gestural communication is considered a standard indicator of intentionality. However, the developmental precursors of gaze behaviour in primates' communication are not well understood. Here, we capitalized on the training in gestures dispensed to olive baboons (Papio anubis) as a way of manipulating individual communicative experience with humans. We aimed to delineate the effects of such a training experience on gaze behaviour displayed by the monkeys in relation with gestural requests. Using a food-requesting paradigm, we compared subjects trained in requesting gestures (i.e. trained subjects) to naïve subjects (i.e. control subjects) for their occurrences of (1) gaze behaviour, (2) requesting gestures and (3) temporal combination of gaze alternation with gestures. We found that training did not affect the frequencies of looking at the human's face, looking at food or alternating gaze. Hence, social gaze behaviour occurs independently from the amount of communicative experience with humans. However, trained baboons-gesturing more than control subjects-exhibited most gaze alternation combined with gestures, whereas control baboons did not. By reinforcing the display of gaze alternation along with gestures, we suggest that training may have served to enhance the communicative function of hand gestures. Finally, this study brings the first quantitative report of monkeys producing requesting gestures without explicit training by humans (controls). These results may open a window on the developmental mechanisms (i.e. incidental learning vs. training) underpinning gestural intentional communication in primates.

Social dynamics of vervet monkeys are dependent upon group identity.

Traditions are widespread across the animal realm. Here, we investigated inter-group variability of social dynamics in wild vervet monkeys (Chlorocebus pygerythrus). We analyzed 84,704 social interactions involving 247 individuals collected over nine years in three neighboring groups of wild vervet monkeys. We found that in one group - Ankhase - individuals had a higher propensity to be affiliative (i.e., sociality) and grooming interactions were more reciprocal. Despite yearly fluctuations in sociality, differences between groups remained stable over time. Moreover, our statistical model predictions confirmed that these findings were maintained for similar sex ratios, age distributions, and group sizes. Strikingly, our results suggested that dispersing males adapted their sociality to the sociality of the group they integrated with. As a whole, our study sheds light on the existence of stable social dynamics dependent upon group identity in wild vervet monkeys and suggests that at least part of this variability is socially mediated.

Role of immigrant males and muzzle contacts in the uptake of a novel food by wild vervet monkeys.

The entry into and uptake of information in social groups is critical for behavioral adaptation by long-lived species in rapidly changing environments. We exposed five groups of wild vervet monkeys to a novel food to investigate the innovation of processing and consuming it. We report that immigrant males innovated in two groups, and an infant innovated in one group. In two other groups, immigrant males imported the innovation from their previous groups. We compared uptake between groups with respect to the initial innovator to examine the extent to which dispersing males could introduce an innovation into groups. Uptake of the novel food was faster in groups where immigrant males ate first rather than the infants. Younger individuals were more likely overall, and faster, to subsequently acquire the novel food. We also investigated the role of muzzle contact behavior in information seeking around the novel food. Muzzle contacts decreased in frequency over repeated exposures to the novel food. Muzzle contacts were initiated the most by naïve individuals, high rankers, and juveniles; and were targeted most towards knowledgeable individuals and high rankers, and the least towards infants. We highlight the potential importance of dispersers in rapidly exploiting novel resources among populations.

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.

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.

Processing of novel food reveals payoff and rank-biased social learning in a wild primate.

Social learning-learning from others-is the basis for behavioural traditions. Different social learning strategies (SLS), where individuals biasedly learn behaviours based on their content or who demonstrates them, may increase an individual's fitness and generate behavioural traditions. While SLS have been mostly studied in isolation, their interaction and the interplay between individual and social learning is less understood. We performed a field-based open diffusion experiment in a wild primate. We provided two groups of vervet monkeys with a novel food, unshelled peanuts, and documented how three different peanut opening techniques spread within the groups. We analysed data using hierarchical Bayesian dynamic learning models that explore the integration of multiple SLS with individual learning. We (1) report evidence of social learning compared to strictly individual learning, (2) show that vervets preferentially socially learn the technique that yields the highest observed payoff and (3) also bias attention toward individuals of higher rank. This shows that behavioural preferences can arise when individuals integrate social information about the efficiency of a behaviour alongside cues related to the rank of a demonstrator. When these preferences converge to the same behaviour in a group, they may result in stable behavioural traditions.

Wild primates copy higher-ranked individuals in a social transmission experiment.

Little is known about how multiple social learning strategies interact and how organisms integrate both individual and social information. Here we combine, in a wild primate, an open diffusion experiment with a modeling approach: Network-Based Diffusion Analysis using a dynamic observation network. The vervet monkeys we study were not provided with a trained model; instead they had access to eight foraging boxes that could be opened in either of two ways. We report that individuals socially learn the techniques they observe in others. After having learnt one option, individuals are 31x more likely to subsequently asocially learn the other option than individuals naïve to both options. We discover evidence of a rank transmission bias favoring learning from higher-ranked individuals, with no evidence for age, sex or kin bias. This fine-grained analysis highlights a rank transmission bias in a field experiment mimicking the diffusion of a behavioral innovation.

Correction: 'Unwilling' versus 'unable': Tonkean macaques' understanding of human goal-directed actions.

[This corrects the article DOI: 10.7717/peerj.3227.].

'Unwilling' versus 'unable': Tonkean macaques' understanding of human goal-directed actions.

The present study investigated the understanding of goal-directed actions in Tonkean macaques (Macaca tonkeana) using the unwilling versus unable paradigm, previously used in several species. Subjects were tested in three experimental conditions that varied according to the goal-directed actions of a human actor. In the "unwilling" condition, the actor was capable of giving the subject food but unwilling to do it; in the "unable" condition, she was willing to give food but was unable to do it because of a physical barrier; and in the "distracted" condition, she was occupied by manipulating a pebble instead of food. We report for the first time that Tonkean macaques, like capuchins, chimpanzees and human infants, behaved differently across these experimental conditions. They attempted to grasp food in the actor's hand significantly more and displayed more threats in the presence of an unwilling actor rather than an unable or a distracted one. Inversely, they begged significantly more and displayed more frustration behaviors facing a distracted and unable experimenter rather than an unwilling one. These results suggest that Tonkean macaques understand human goal-directed actions by predicting whether they were likely to obtain food merely based on movements, cue and motor intentions reading and understanding of physical constraints.

Do Tonkean macaques (Macaca tonkeana) perceive what conspecifics do and do not see?

The understanding of the visual perception of others, also named visual perspective taking, is a component of Theory of Mind. Although strong evidence of visual perspective taking has been reported in great apes, the issue is more open to discussion in monkeys. We investigated whether Tonkean macaques (Macaca tonkeana) know what conspecifics do and do not see, using a food competition paradigm originally developed in great apes. We tested individuals in pairs, after establishing the dominance relationship within each pair. Twenty-one pairs were tested in four different conditions. In one condition, the subordinate had the choice between two pieces of food, one that was visible only to it and another that was also visible to the dominant. It was predicted that if the subordinate understands that the dominant cannot see both pieces of food because one is hidden from its view, the subordinate should preferentially go for the food visible only to itself. In the three other conditions, we varied the temporal and visual access to food for both individuals, to control for alternative explanations based on dominance. We recorded the first movement direction chosen by subjects, i.e. towards a) visible food b) hidden food or c) elsewhere; and the outcome of the test, i.e. the quantity of food obtained. Results showed that subordinates moved preferentially for the hidden food when released simultaneously with the dominant and also with a head start on the dominant. By contrast, dominants' choices of the two pieces of food were random. We also describe and discuss some of the strategies used by subordinates in these tests. According to the whole of our results, Tonkean macaques seem capable of visual perspective taking despite the fact that a low-level explanation as behavior reading has not been totally excluded.