Being facially expressive is socially advantageous.

Individuals vary in how they move their faces in everyday social interactions. In a first large-scale study, we measured variation in dynamic facial behaviour during social interaction and examined dyadic outcomes and impression formation. In Study 1, we recorded semi-structured video calls with 52 participants interacting with a confederate across various everyday contexts. Video clips were rated by 176 independent participants. In Study 2, we examined video calls of 1315 participants engaging in unstructured video-call interactions. Facial expressivity indices were extracted using automated Facial Action Coding Scheme analysis and measures of personality and partner impressions were obtained by self-report. Facial expressivity varied considerably across participants, but little across contexts, social partners or time. In Study 1, more facially expressive participants were more well-liked, agreeable, and successful at negotiating (if also more agreeable). Participants who were more facially competent, readable, and perceived as readable were also more well-liked. In Study 2, we replicated the findings that facial expressivity was associated with agreeableness and liking by their social partner, and additionally found it to be associated with extraversion and neuroticism. Findings suggest that facial behaviour is a stable individual difference that proffers social advantages, pointing towards an affiliative, adaptive function.

Revisiting Darwin's comparisons between human and non-human primate facial signals.

Darwin and other pioneering scholars made comparisons between human facial signals and those of non-human primates, suggesting they share evolutionary history. We now have tools available (Facial Action Coding System: FACS) to make these comparisons anatomically based and standardised, as well as analytical methods to facilitate comparative studies. Here we review the evidence establishing a shared anatomical basis between the facial behaviour of human and non-human primate species, concluding which signals are likely related, and which are not. We then review the evidence for shared function and discuss the implications for understanding human communication. Where differences between humans and other species exist, we explore possible explanations and future directions for enquiry.

Assessing the reliability of an automated method for measuring dominance hierarchy in non-human primates.

Among animal societies, dominance is an important social factor that influences inter-individual relationships. However, assessing dominance hierarchy can be a time-consuming activity which is potentially impeded by environmental factors, difficulties in the recognition of animals, or disturbance of animals during data collection. Here we took advantage of novel devices, machines for automated learning and testing (MALT), designed primarily to study non-human primate cognition, to additionally measure the dominance hierarchy of a semi-free-ranging primate group. When working on a MALT, an animal can be replaced by another, which could reflect an asymmetric dominance relationship. To assess the reliability of our method, we analysed a sample of the automated conflicts with video scoring and found that 74% of these replacements included genuine forms of social displacements. In 10% of the cases, we did not identify social interactions and in the remaining 16% we observed affiliative contacts between the monkeys. We analysed months of daily use of MALT by up to 26 semi-free-ranging Tonkean macaques (Macaca tonkeana) and found that dominance relationships inferred from these interactions strongly correlated with the ones derived from observations of spontaneous agonistic interactions collected during the same time period. An optional filtering procedure designed to exclude chance-driven displacements or affiliative contacts suggests that the presence of 26% of these interactions in data sets did not impair the reliability of this new method. We demonstrate that this method can be used to assess the dynamics of both individual social status, and group-wide hierarchical stability longitudinally with minimal research labour. Further, it facilitates a continuous assessment of dominance hierarchies in captive groups, even during unpredictable environmental or challenging social events, which underlines the usefulness of this method for group management purposes. Altogether, this study supports the use of MALT as a reliable tool to automatically and dynamically assess dominance hierarchy within captive groups of non-human primates, including juveniles, under conditions in which such technology can be used.

An understanding of third-party friendships in a tolerant macaque.

Complex societies are shaped by social relationships between multiple individuals. The pressure to track these relationships has driven the evolution of social cognition in primates. Importantly, it can be adaptive to track not only personal relationships, but also those established between third-parties. Primates have knowledge about others' dominance hierarchies and kinship, but we do not know to what extent they also understand friendships. In a playback experiment, Tonkean macaques were presented with simulated conflicts involving third-party female dyads who were established friends or non-friends. Hearing a conflict between friends elicited a stronger behavioural response in listeners (i.e. an increase in looking time) compared to hearing a conflict between non-friends. Conflicts between friends are likely to represent a greater disruption of the social group and structure of the network, and therefore this difference in response may represent an adaptive strategy employed by the macaques to selectively monitor important social interactions in the group. These findings provide evidence that Tonkean macaques (and potentially other primates) can classify the relationships of others based on their degree of friendship and additionally, confirms the important role friendships have within the societies of social primates.

Are there non-verbal signals of guilt?

Guilt is a complex emotion with a potentially important social function of stimulating cooperative behaviours towards and from others, but whether the feeling of guilt is associated with a recognisable pattern of nonverbal behaviour is unknown. We examined the production and perception of guilt in two different studies, with a total of 238 participants with various places of origin. Guilt was induced experimentally, eliciting patterns of movement that were associated with both the participants' self-reported feelings of guilt and judges' impressions of their guilt. Guilt was most closely associated with frowning and neck touching. While there were differences between self-reported guilt and perception of guilt the findings suggest that there are consistent patterns that could be considered a non-verbal signal of guilt in humans.

The social function of the feeling and expression of guilt.

Humans are uniquely cooperative and form crucial short- and long-term social bonds between individuals that ultimately shape human societies. The need for such intense cooperation may have provided a particularly powerful selection pressure on the emotional and communicative behaviours regulating cooperative processes, such as guilt. Guilt is a social, other-oriented moral emotion that promotes relationship repair and pro-sociality. For example, people can be more lenient towards wrongdoers who display guilt than towards those who do not. Here, we examined the social consequences of guilt in a novel experimental setting with pairs of friends differing in relationship quality. Pairs of participants took part in a cooperative game with a mutual goal. We then induced guilt in one of the participants and informed the other participant of their partner's wrongdoing. We examined the outcome using a dictator game to see how they split a joint reward. We found that guilty people were motivated to repair wrongdoing regardless of friendship. Observing guilt in others led to a punishment effect and a victim of wrongdoing punished close friends who appeared guilty more so than acquaintances. We suggest, therefore, that guilt has a stronger function between close friends as the costs of relationship breakdown are greater. Relationship context, therefore, is crucial to the functional relevance of moral emotions.

Stress behaviours buffer macaques from aggression.

Primates (including humans) scratch when stressed. So far, such scratching has been seen as a by-product of physiological processes associated with stress, and attributed proximate, regulatory function. However, it is possible that others could use this relationship between scratching and stress as an indication of the animal's stress state, and thus scratching could potentially have social function. As a test of this theory, we measured the production of, and social responses to scratching in a group of free-ranging rhesus macaques (Macaca mulatta). Firstly, we found that the likelihood of scratching was greater around periods of heightened social stress, such as being in proximity to high-ranking individuals, or non-friends. Secondly, when macaques scratched, subsequent interactions were less likely to be aggressive and more likely to be affiliative. Potential attackers may avoid attacking stressed individuals as stressed individuals could behave unpredictably or be weakened by their state of stress (rendering aggression risky and/or unnecessary). Observable stress behaviour could therefore have additional adaptive value by reducing the potential for escalated aggression, benefiting both senders and receivers by facilitating social cohesion. This basic ability to recognise stress in others could also be an important component in the evolution of social cognition such as empathy.

Rethinking primate facial expression: A predictive framework.

Primate facial expression has long been studied within a framework of emotion that has heavily influenced both theoretical approaches and scientific methods. For example, our understanding of the adaptive function and cognition of facial expression is tied to the assumption that facial expression is accompanied by an emotional internal state, which is decipherable by others. Here, we challenge this view and instead support the alternative that facial expression should also be conceptualised as an indicator of future behaviour as opposed to current emotional state alone (Behavioural Ecology View, Fridlund, 1994). We also advocate the use of standardised, objective methodology Facial Action Coding System, to avoid making assumptions about the underlying emotional state of animals producing facial expressions. We argue that broadening our approach to facial expression in this way will open new avenues to explore the underlying neurobiology, cognition and evolution of facial communication in both human and non-human primates.

Macaques can predict social outcomes from facial expressions.

There is widespread acceptance that facial expressions are useful in social interactions, but empirical demonstration of their adaptive function has remained elusive. Here, we investigated whether macaques can use the facial expressions of others to predict the future outcomes of social interaction. Crested macaques (Macaca nigra) were shown an approach between two unknown individuals on a touchscreen and were required to choose between one of two potential social outcomes. The facial expressions of the actors were manipulated in the last frame of the video. One subject reached the experimental stage and accurately predicted different social outcomes depending on which facial expressions the actors displayed. The bared-teeth display (homologue of the human smile) was most strongly associated with predicted friendly outcomes. Contrary to our predictions, screams and threat faces were not associated more with conflict outcomes. Overall, therefore, the presence of any facial expression (compared to neutral) caused the subject to choose friendly outcomes more than negative outcomes. Facial expression in general, therefore, indicated a reduced likelihood of social conflict. The findings dispute traditional theories that view expressions only as indicators of present emotion and instead suggest that expressions form part of complex social interactions where individuals think beyond the present.

MaqFACS (Macaque Facial Action Coding System) can be used to document facial movements in Barbary macaques (Macaca sylvanus).

Human and non-human primates exhibit facial movements or displays to communicate with one another. The evolution of form and function of those displays could be better understood through multispecies comparisons. Anatomically based coding systems (Facial Action Coding Systems: FACS) are developed to enable such comparisons because they are standardized and systematic and aid identification of homologous expressions underpinned by similar muscle contractions. To date, FACS has been developed for humans, and subsequently modified for chimpanzees, rhesus macaques, orangutans, hylobatids, dogs, and cats. Here, we wanted to test whether the MaqFACS system developed in rhesus macaques (Macaca mulatta) could be used to code facial movements in Barbary macaques (M. sylvanus), a species phylogenetically close to the rhesus macaques. The findings show that the facial movement capacity of Barbary macaques can be reliably coded using the MaqFACS. We found differences in use and form of some movements, most likely due to specializations in the communicative repertoire of each species, rather than morphological differences.

Familiar and unfamiliar face recognition in crested macaques (Macaca nigra).

Many species use facial features to identify conspecifics, which is necessary to navigate a complex social environment. The fundamental mechanisms underlying face processing are starting to be well understood in a variety of primate species. However, most studies focus on a limited subset of species tested with unfamiliar faces. As well as limiting our understanding of how widely distributed across species these skills are, this also limits our understanding of how primates process faces of individuals they know, and whether social factors (e.g. dominance and social bonds) influence how readily they recognize others. In this study, socially housed crested macaques voluntarily participated in a series of computerized matching-to-sample tasks investigating their ability to discriminate (i) unfamiliar individuals and (ii) members of their own social group. The macaques performed above chance on all tasks. Familiar faces were not easier to discriminate than unfamiliar faces. However, the subjects were better at discriminating higher ranking familiar individuals, but not unfamiliar ones. This suggests that our subjects applied their knowledge of their dominance hierarchies to the pictorial representation of their group mates. Faces of high-ranking individuals garner more social attention, and therefore might be more deeply encoded than other individuals. Our results extend the study of face recognition to a novel species, and consequently provide valuable data for future comparative studies.

Facial expression recognition in crested macaques (Macaca nigra).

Facial expressions are a main communication channel used by many different species of primate. Despite this, we know relatively little about how primates discriminate between different facial expressions, and most of what we do know comes from a restricted number of well-studied species. In this study, three crested macaques (Macaca nigra) took part in matching-to-sample tasks where they had to discriminate different facial expressions. In a first experiment, the macaques had to match a photograph of a facial expression to another exemplar of the same expression produced by a different individual, against examples of one of three other types of expressions and neutral faces. In a second experiment, they had to match a dynamic video recording of a facial expression to a still photograph of another exemplar of the same facial expression produced by another individual, also against one of four other expressions. The macaques performed above chance in both tasks, identifying expressions as belonging to the same category regardless of individual identity. Using matrix correlations and multidimensional scaling, we analysed the pattern of errors to see whether overall similarity between facial expressions and/or specific morphological features caused the macaques to confuse facial expressions. Overall similarity, measured with the macaque facial action coding system (maqFACS), did not correlate with performances. Instead, functional similarities between facial expressions could be responsible for the observed pattern of error. These results expand previous findings to a novel primate species and highlight the potential of using video stimuli to investigate the perception and categorisation of visual signals in primates.

Evaluation of public engagement activities to promote science in a zoo environment.

Scientists are increasing their efforts to promote public engagement with their science, but the efficacy of the methods used is often not scientifically evaluated. Here, we designed, installed and evaluated the educational impact of interactive games on touchscreens at two primate research centres based in zoo environments. The games were designed to promote interest in and understanding of primates and comparative psychology, as a scaffold towards interest in science more generally and with the intention of targeting younger individuals (under 16's). We used systematic observational techniques and questionnaires to assess the impact of the games on zoo visitors. The games facilitated increased interest in psychology and science in zoo visitors, and changed the knowledge of visitors, through demonstration of learning about specific scientific findings nested within the games. The impact of such devices was greatest on younger individuals (under 16's) as they were significantly more likely to engage with the games. On the whole, therefore, this study demonstrates that interactive devices can be successful educational tools, and adds to the growing body of evidence that conducting research on public view in zoos can have a tangible impact on public engagement with science.

The impact of cognitive testing on the welfare of group housed primates.

Providing cognitive challenges to zoo-housed animals may provide enriching effects and subsequently enhance their welfare. Primates may benefit most from such challenges as they often face complex problems in their natural environment and can be observed to seek problem solving opportunities in captivity. However, the extent to which welfare benefits can be achieved through programmes developed primarily for cognitive research is unknown. We tested the impact of voluntary participation cognitive testing on the welfare of a socially housed group of crested macaques (Macaca nigra) at the Macaque Study Centre (Marwell Zoo). First, we compared the rate of self-directed and social behaviours on testing and non-testing days, and between conditions within testing days. Minimal differences in behaviour were found when comparing testing and non-testing days, suggesting that there was no negative impact on welfare as a result of cognitive testing. Lipsmacking behaviours were found to increase and aggressive interaction was found to decrease in the group as a result of testing. Second, social network analysis was used to assess the effect of testing on associations and interactions between individuals. The social networks showed that testing subjects increased their association with others during testing days. One interpretation of this finding could be that providing socially housed primates with an opportunity for individuals to separate from the group for short periods could help mimic natural patterns of sub-group formation and reunion in captivity. The findings suggest, therefore, that the welfare of captive primates can be improved through the use of cognitive testing in zoo environments.