The forgotten adaptive social benefits of social learning in animals.

Theoretical and empirical scholars of cultural evolution have traditionally studied social learning strategies, such as conformity, as adaptive strategies to obtain accurate information about the environment, whereas within social psychology there has been a greater focus upon the social consequences of such strategies. Although these two approaches are often used in concert when studying human social learning, we believe the potential social benefits of conformity, and of social learning more broadly, have been overlooked in studies of non-humans. We review evidence from studies of homophily, imitation, and rapid facial mimicry that suggests that behaving like others affords social benefits to non-human animals and that behaviour matching may be deployed strategically to increase affiliation. Furthermore, we review studies of conformity in dispersers, and suggest that forgoing personal information or preferences in favour of those of the new group during immigration may be a strategy to facilitate social integration. We therefore propose that the informational and social functions of conformity apply to humans and animals alike. We use this perspective to generate several interesting research questions to inspire work in this field. For example, under what conditions do animals use informational or social conformity and what role does uncertainty play in social learning in immigrant individuals?

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.

Juvenile vervet monkeys rely on others when responding to danger.

Primate alarm calls are mainly hardwired but individuals need to adapt their calling behaviours according to the situation. Such learning necessitates recognising locally relevant dangers and may take place via their own experience or by observing others. To investigate monkeys alarm calling behaviour, we carried out a field experiment in which we exposed juvenile vervet monkeys to unfamiliar raptor models in the presence of audiences that differed in experience and reliability. We used audience age as a proxy for experience and relatedness as a proxy for reliability, while quantifying audience reactions to the models. We found a negative correlation between alarm call production and callers' age. Adults never alarm called, compared to juveniles. We found no overall effect of audience composition and size, with juveniles calling more when with siblings than mothers or unrelated individuals. Finally, concerning audience reactions to the models, we observed juveniles remained silent with vigilant mothers and only alarm called with ignoring mothers, whereas we observed the opposite for siblings: juveniles remained silent with ignoring siblings and called with vigilant siblings. Despite the small sample size, juvenile vervet monkeys, confronted with unfamiliar and potentially dangerous raptors, seem to rely on others to decide whether to alarm call, demonstrating that the choice of the model may play an important key role in the ontogeny of primate alarm call behaviour.

Context-dependent alarm responses in wild vervet monkeys.

The alarm calls of nonhuman primates are occasionally cited as functionally equivalent to lexical word meaning in human language. Recently, however, it has become increasingly unlikely that one-to-one relations between alarm call structures and predator categories are the default, mainly because many call types are produced in multiple contexts, requiring more complex notions of meaning. For example, male vervet monkeys produce the same alarm calls during encounters with terrestrial predators and neighbouring groups, suggesting that recipients require additional information to attribute meaning to the calls. We empirically tested the hypothesis that vervet monkeys take contextual information into account when responding to each other's alarm calls. In playback experiments, we exposed subjects to recordings of male alarm barks during actual intergroup encounters (predator unlikely) or when there was no intergroup encounter (predator likely). Subjects responded more strongly in the no intergroup encounter situations, typically associated with discovering a hiding predator, measured in terms of startle responses, vigilance behaviour and gazing towards the presumed caller. We discuss the significance of using contextual information for meaning attribution in nonhuman primate communication.

Lab cognition going wild: Implementing a new portable touchscreen system in vervet monkeys.

Touchscreen technology has provided researchers with opportunities to conduct well-controlled cognitive tests with captive animals, allowing researchers to isolate individuals, select participants based on specific traits, and control aspects of the environment. In this study, we aimed to investigate the potential utility of touchscreen technology for the study of cognition in wild vervet monkeys. We assessed the viability of touchscreen testing by comparing rates of participation between wild and sanctuary-housed vervets. Additionally, we compared performance on a simple associative learning task in order to verify that wild participants are able to engage meaningfully with a touchscreen task presented in their natural environment. We presented eight groups of vervet monkeys (four wild and four sanctuary groups, totalling 240 individuals) with a portable touchscreen device. The touchscreen displayed tasks in which food rewards could be gained by touching a stimulus displayed on the screen. We assessed individuals' likelihood of interacting with the touchscreen, their frequency of participation, and their performance on a simple associative learning task. We found that sanctuary-housed monkeys were more likely to interact with the touchscreen. Participation in wild vervet monkeys was influenced by sex and age. However, monkeys in the two contexts (sanctuary vs. wild) did not differ in their performance on a simple associative learning task. This study demonstrates that touchscreen technology can be successfully deployed in a population of wild primates. This gives us a starting point to test animal cognition under natural conditions that include varying group composition, environmental challenges and ongoing activities such as foraging, which are challenging to recreate in captivity. While rates of participation were lower than those found in captivity, reasonable sample sizes can be achieved, and wild primates can successfully learn touchscreen tasks in a manner comparable to their captive counterparts.

Drivers and outcomes of between-group conflict in vervet monkeys.

Neighbouring groups compete over access to resources and territories in between-group encounters, which can escalate into between-group conflicts (BGCs). Both the ecological characteristics of a territory and the rival's fighting ability shape the occurrence and outcome of such contests. What remains poorly understood, however, is how seasonal variability in the ecological value of a territory together with fighting ability related to the likelihood of between-group encounters and the extent to which these escalate into conflicts. To test this, we observed and followed four vervet monkey groups in the wild, and recorded the group structure (i.e. size, composition), the locations and the outcomes of 515 BGCs. We then assessed key ecological measures at these locations, such as vegetation availability (estimated from Copernicus Sentinel 2 satellite images) and the intensity of usage of these locations. We tested to what extent these factors together influenced the occurrence and outcomes of BGCs. We found that the occurrence of BGCs increased at locations with higher vegetation availability relative to the annual vegetation availability within the group's home territory. Also, groups engaging in a BGC at locations far away from their home territory were less likely to win a BGC. Regarding group structure, we found that smaller groups systematically won BGCs against larger groups, which can be explained by potentially higher rates of individual free-riding occurring in larger groups. This study sheds light on how the ecology of encounter locations in combination with a group's social characteristics can critically impact the dynamics of BGCs in a non-human primate species. This article is part of the theme issue 'Intergroup conflict across taxa'.

Captivity and habituation to humans raise curiosity in vervet monkeys.

The cognitive mechanisms causing intraspecific behavioural differences between wild and captive animals remain poorly understood. Although diminished neophobia, resulting from a safer environment and more "free" time, has been proposed to underlie these differences among settings, less is known about how captivity influences exploration tendency. Here, we refer to the combination of reduced neophobia and increased interest in exploring novelty as "curiosity", which we systematically compared across seven groups of captive and wild vervet monkeys (Chlorocebus pygerythrus) by exposing them to a test battery of eight novel stimuli. In the wild sample, we included both monkeys habituated to human presence and unhabituated individuals filmed using motion-triggered cameras. Results revealed clear differences in number of approaches to novel stimuli among captive, wild-habituated and wild-unhabituated monkeys. As foraging pressure and predation risks are assumed to be equal for all wild monkeys, our results do not support a relationship between curiosity and safety or free time. Instead, we propose "the habituation hypothesis" as an explanation of why well-habituated and captive monkeys both approached and explored novelty more than unhabituated individuals. We conclude that varying levels of human and/or human artefact habituation, rather than the risks present in natural environments, better explain variation in curiosity in our sample of vervet monkeys.

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.

Organized to learn: the influence of social structure on social learning opportunities in a group.

Social learning, which is a mechanism that allows an individual to acquire skills from other individuals, occurs in a social context. Therefore, factors that influence social context, like social structure, will impact social learning opportunities. This review explores how features of social structure affect social learning opportunities in primates, either through their relationship with social tolerance or through the number of social learning models. Features that are investigated in this review and that we hypothesize affect social learning opportunities are parental investment, dominance hierarchy, nepotism, social bonds, dispersal, group size, fission-fusion dynamics, and sex ratio. For most of these features we find evidence, but support varies. Of all primate species, only humans show all the requirements of an optimal social structure to promote social learning. Future research into social learning and culture should not overlook the social context in which it takes place.

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.

Corrigendum: Dynamics of Intersexual Dominance and Adult Sex- Ratio in Wild Vervet Monkeys.

[This corrects the article DOI: 10.3389/fpsyg.2020.00839.].

Reactions to infant death by wild vervet monkeys (Chlorocebus pygerythrus) in KwaZulu-Natal, South Africa: prolonged carrying, non-mother carrying, and partial maternal cannibalism.

Observations of dead infant carrying have been reported for many primate species, and researchers have proposed several hypotheses to explain this behaviour. However, despite being a relatively well-studied species, reports of dead infant carrying in wild vervet monkeys (Chlorocebus pygerythrus) remain scarce. Here we report 14 observations of dead infant carrying by female vervet monkeys in a population at Mawana Game Reserve, KwaZulu-Natal, South Africa. Most of the females carried the dead infant for a day or less, but one female carried her infant for at least 14 days. In one case the maternal sister of a dead infant carried it after the death of their mother. We also report a case of mother-infant cannibalism: a female consumed part of her deceased infant's tail. Other post-mortem care-taking behaviours such as grooming, smelling and licking were also recorded. Of 97 recorded infant deaths in this study population since 2010, 14.4% are known to have elicited dead infant carrying, a proportion similar to that reported for other monkey species. We discuss our observations in relation to various hypotheses about this behaviour, including the post-parturition hormones hypothesis, learning to mother hypothesis, and unawareness of death hypothesis.

Dynamics of Intersexual Dominance and Adult Sex- Ratio in Wild Vervet Monkeys.

Intersexual dominance relations are important for female mammals, because of their consequences for accessing food and for the degree of sexual control females experience from males. Female mammals are usually considered to rank below males in the dominance hierarchy, because of their typical physical inferiority. Yet, in some groups or species, females are nonetheless dominant over some males (partial female dominance). Intersexual dominance, therefore, also depends on traits other than sexual dimorphism, such as social support, social exchange, group adult sex-ratio, and the widespread self-reinforcing effects of winning and losing fights, the "winner-loser effect." The importance of sex-ratio and the winner-loser effect remains poorly understood. A theoretical model, DomWorld, predicts that in groups with a higher proportion of males, females are dominant over more males when aggression is fierce (not mild). The model is based on a small number of general processes in mammals, such as grouping, aggression, the winner-loser effect, the initially greater fighting capacity of males than females, and sex ratio. We expect its predictions to be general and suggest they be examined in a great number of species and taxa. Here, we test these predictions in four groups of wild vervet monkeys (Chlorocebus pygerythrus) in Mawana game reserve in Africa, using 7 years of data. We confirm that a higher proportion of males in the group is associated with greater dominance of females over males; a result that remains when combining these data with those of two other sites (Amboseli and Samara). We additionally confirm that in groups with a higher fraction of males there is a relatively higher (a) proportion of fights of males with other males, and (b) proportion of fights won by females against males from the fights of females with any adults. We reject alternative hypotheses that more dominance of females over males could be attributed to females receiving more coalitions from males, or females receiving lowered male aggression in exchange for sexual access (the docile male hypothesis). We conclude that female dominance relative to males is dynamic and that future empirical studies of inter-sexual dominance will benefit by considering the adult sex-ratio of groups.

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.

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.

Correlates of social role and conflict severity in wild vervet monkey agonistic screams.

Screams are acoustically distinct, high-pitched and high-amplitude calls, produced by many social species. Despite a wide range of production contexts, screams are characterised by an acoustic structure that appears to serve in altering the behaviour of targeted receivers during agonistic encounters. In chimpanzees, this can be achieved by callers producing acoustic variants that correlate with their identity, social role, relationship with the targeted recipient, the composition of the audience and the nature of the event. Although vervet monkeys (Chlorocebus pygerythrus) have been studied for decades, not much is known about their agonistic screams. Here, we examined agonistic screams produced by wild vervet monkeys to investigate the degree to which caller identity, social role and conflict severity affected call structure. We found that screams were both individually distinctive and dependent of the agonistic events. In particular, victim screams were longer and higher-pitched than aggressor screams, while screams produced in severe conflicts (chases, physical contact) had higher entropy than those in mild conflicts. We discuss these findings in terms of their evolutionary significance and suggest that acoustic variation might serve to reduce the aggression level of opponents, while simultaneously attracting potential helpers.

Primates are living links to our past: The contribution of comparative studies with wild vervet monkeys to the field of social cognition.

By studying the behavior of nonhuman primates, particularly in wild settings, researchers have been able to investigate a range of cognitive abilities, shedding light on the evolution of certain aspects of cognition and revealing potential evolutionary precursors of many capacities considered uniquely human. Vervet monkeys (Chlorocebus pygerythrus) have been widely investigated due to their prevalence and their suitability for experimental testing in the wild with an ecologically valid approach that is not possible with many other primates, especially apes. Here we review advances in the understanding of a number of cognitive and behavioral processes that have been gleaned from studies conducted with wild vervet monkeys over the past half century, primarily focusing on social cognitive abilities. We direct our attention to three major areas of study; communication, cooperation and trade, and social learning. We discuss how findings from this species have contributed (and continue to contribute) to our understanding of the evolution of human cognitive capacities and suggest future avenues of research with this species.

Social attention biases in juvenile wild vervet monkeys: implications for socialisation and social learning processes.

The concept of directed social learning predicts that social learning opportunities for an individual will depend on social dynamics, context and demonstrator identity. However, few empirical studies have examined social attention biases in animal groups. Sex-based and kinship-based biases in social learning and social attention towards females have been shown in a despotic and female philopatric primate: the vervet monkey (Chlorocebus pygerythrus). The present study examined social attention during the juvenile period. Social attention was recorded through 5-min focal observations during periods of natural foraging. Kin emerged as the most important focus of social attention in juveniles, intensified by biased spatial proximity towards matrilineal related members. The highest-ranking conspecifics were more frequently observed by juveniles than low-ranking ones. Additionally, younger and orphaned juveniles showed higher levels of social attention overall, compared to other age categories. No effect of the juvenile's hierarchical rank was detected, suggesting that the variation in social attention recorded reflects different biases and stages of social learning and socialisation, rather than social anxiety. Juvenile females tended to exhibit a dominance-based bias more strongly than did males. This might be explained by a greater emphasis on attaining social knowledge during juvenile socialisation in the philopatric sex. Moreover, despite a preferred association between juveniles, social attention was more often directed to adults, suggesting that adults may still be more often chosen as a target of attention independent of their dominance rank.

Celebrating the continued importance of "Machiavellian Intelligence" 30 years on.

The question of what has shaped primates' (and other species') cognitive capacities, whether technical or social demands, remains a hot topic of inquiry. Indeed, a key area of study within the field of comparative psychology in the last few decades has been the focus on social life as a driving force behind the evolution of cognition, studied from behavioral and neurological perspectives and from theoretical and empirical perspectives. Reflecting on contemporary studies of primate social cognition specifically, one cannot ignore the book, Machiavellian Intelligence, coedited by Richard Byrne and Andrew Whiten (Byrne & Whiten, 1988a). It is a keystone for the field: The volume as a whole has been cited over 3,000 times, without even including citations to individual chapters. This year, 2018, is the 30th anniversary of the first publication of Machiavellian Intelligence, and with this special issue of the Journal of Comparative Psychology, we mark that milestone. The key concept put forth in Machiavellian Intelligence was that primates' sociocognitive abilities were shaped by the complex social worlds that they inhabited, rather than the technical or foraging challenges that they faced, as had previously been posited. In this issue, we consider the strength of the Machiavellian intelligence hypothesis 30 years on to explain primate social cognition, and we consider its applicability to nonprimate species and to other cognitive domains. (PsycINFO Database Record (c) 2018 APA, all rights reserved).