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.

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.

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.

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.

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.

Resilience of experimentally seeded dietary traditions in wild vervets: Evidence from group fissions.

Controlled laboratory experiments have delivered extensive and compelling evidence for the diffusion and maintenance of socially learned behavior in primates and other animals. Such evidence is rarer in the wild, but we show that a behavior seeded in a majority of individuals within vervet monkey (Chlorocebus pygerythus) groups may be sustained across several years. Here, we report results of two natural fission events in such groups that offer novel evidence of the resilience of socially transmitted group norms of behavior. Before fission, high ranked females exhibited an almost exclusive adherence to a group preference among two food options, originally introduced through a distasteful additive in one option, but no longer present in repeated later tests. Because of rank-dependent competition, low-ranked females ate more of the formerly distasteful food and so discovered it was now as palatable as the alternative. Despite this experience, low ranked females who formed the splinter groups then expressed a 100% bias for the preferred option of their original parent group, revealing these preferences to be resilient. We interpret this effect as conformity to either the preferences of high rankers or of a majority in the parent group, or both. However, given fissioned individuals' familiarity with their habitat and experimental options, we question the adequacy of the informational function usually ascribed to conformity and discuss alternatives under a concept of "social conformity".

Wild vervet monkeys copy alternative methods for opening an artificial fruit.

Experimental studies of animal social learning in the wild remain rare, especially those that employ the most discriminating tests in which alternative means to complete naturalistic tasks are seeded in different groups. We applied this approach to wild vervet monkeys (Chlorocebus aethiops) using an artificial fruit ('vervetable') opened by either lifting a door panel or sliding it left or right. In one group, a trained model lifted the door, and in two others, the model slid it either left or right. Members of each group then watched their model before being given access to multiple baited vervetables with all opening techniques possible. Thirteen of these monkeys opened vervetables, displaying a significant tendency to use the seeded technique on their first opening and over the course of the experiment. The option preferred in these monkeys' first successful manipulation session was also highly correlated with the proportional frequency of the option they had previously witnessed. The social learning effects thus documented go beyond mere stimulus enhancement insofar as the same door knob was grasped for either technique. Results thus suggest that through imitation, emulation or both, new foraging techniques will spread across groups of wild vervet monkeys to create incipient foraging traditions.

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.

Urbanization does not increase "object curiosity" in vervet monkeys, but semi-urban individuals selectively explore food-related anthropogenic items.

Urban environments expose animals to abundant anthropogenic materials and foods that facilitate foraging innovations in species with opportunistic diets and high behavioral flexibility. Neophilia and exploration tendency are believed to be important behavioral traits for animals thriving in urban environments. Vervet monkeys (Chlorocebus pygerythrus) are one of few primate species that have successfully adapted to urban environments, thus making them an ideal species to study these traits. Using a within-species cross-habitat approach, we compared neophilia and exploration of novel objects (jointly referred to as "object curiosity") between semi-urban, wild, and captive monkeys to shed light on the cognitive traits facilitating urban living. To measure "object curiosity," we exposed monkeys to various types of novel stimuli and compared their approaches and explorative behavior. Our results revealed differences in the number of approaches and explorative behavior toward novel stimuli between the habitat types considered. Captive vervet monkeys were significantly more explorative than both semi- urban and wild troops, suggesting that positive experiences with humans and lack of predation, rather than exposure to human materials per se, influence object curiosity. Across habitats, juvenile males were the most explorative age-sex class. This is likely due to males being the dispersing sex and juveniles being more motivated to learn about their environment. Additionally, we found that items potentially associated with human food, elicited stronger explorative responses in semi-urban monkeys than non-food related objects, suggesting that their motivation to explore might be driven by "anthrophilia", that is, their experience of rewarding foraging on similar anthropogenic food sources. We conclude that varying levels of exposure to humans, predation and pre-exposure to human food packaging explain variation in "object curiosity" in our sample of vervet monkeys.

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?

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'.

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.

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.

Selective attention to philopatric models causes directed social learning in wild vervet monkeys.

Human behaviour is often based on social learning, a mechanism that has been documented also in a variety of other vertebrates. However, social learning as a means of problem-solving may be optimal only under specific conditions, and both theoretical work and laboratory experiments highlight the importance of a potential model's identity. Here we present the results from a social learning experiment on six wild vervet monkey groups, where models were either a dominant female or a dominant male. We presented 'artificial fruit' boxes that had doors on opposite, differently coloured ends for access to food. One option was blocked during the demonstration phase, creating consistent demonstrations of one possible solution. Following demonstrations we found a significantly higher participation rate and same-door manipulation in groups with female models compared to groups with male models. These differences appeared to be owing to selective attention of bystanders to female model behaviour rather than owing to female tolerance. Our results demonstrate the favoured role of dominant females as a source for 'directed' social learning in a species with female philopatry. Our findings imply that migration does not necessarily lead to an exchange of socially acquired information within populations, potentially causing highly localized traditions.

Contact with human facilities appears to enhance technical skills in wild vervet monkeys (Chlorocebus aethiops).

Technical abilities of primates are typically tested in the laboratory. It has been argued that close contact between animals and humans may lead to an increase in skills due to an 'enculturation' of subjects. Here, we provide evidence that exposure to human facilities may improve wild vervet monkeys' technical skills in a social learning task using the 'artificial fruit' approach. Two of our 6 study groups had access to human facilities within their territories. Only members of these 2 groups were likely to open successfully 'artificial fruit' during their first attempt. Success appeared to be independent of individual sex or the type of task. Our results highlight the possibility that human enculturation may allow captive monkeys to acquire more technical skills than their wild counterparts, and we suggest that this possibility should be tested in further field experiments.

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.

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.

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

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