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.     

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.     

The role of conformity in foraging when personal and social information conflict

There is currently considerable interest in the interplay betweenpersonal and social information in decision-making processes.Two experiments are presented exploring the relative use ofprior personal information and subsequent social informationin foraging decisions of guppies. Experiment 1 tested the assumptionthat when the use of information acquired through personal experienceis not costly, conflicting social information will be ignored.The assumption was confirmed because, when given a choice betweenfeeding at two food patches, at one of which they had previouslyseen conspecifics feed, individual fish with prior experienceof feeding at the alternative site chose the alternative, whereasfish with no prior experience chose the site at which theirconspecifics had fed. Experiment 2 tested theoretical predictionsthat when the use of information acquired through personal experienceis potentially costly, conflicting social information will beweighed more heavily than will personal information. The predictionwas confirmed because, when given a choice between feeding attwo food patches, one at which they had previously seen conspecificsfeed and one behind a visual barrier, individual fish with priorexperience of feeding behind the barrier chose the site at whichtheir conspecifics had fed. These findings suggest that conformitycan promote social learning in naïve individuals, but priorexperience can insulate individuals from conformity providedthe costs of relying on that experience are small. In addition,the experiments highlight the fact that personal and socialinformation are not always weighed equally.     

Differences in Diet Between Six Neighbouring Groups of Vervet Monkeys

The comparative approach provides a powerful tool to study evolutionary questions on both intra‐ and interspecific variation. It has been applied to a great variety of taxa, including primates. Primate studies differ from those on most other taxa in two ways: first, data from most study sites contain information about only one group. Second, primatologists have used the comparative approach also to identify local traditions, that is, behaviours that spread through social learning. Here, we evaluate the appropriateness of such data by comparing the diet composition of six neighbouring groups of vervet monkeys, Cercopithecus aethiops. We used scan samples to collect diet data, and abundance measures and phenology to assess the availability of the 14 most important tree species utilised during the study. We calculated indices of diet overlap, which were highly variable and could be remarkably low. Furthermore, we found significant differences between group diets with respect to the relative utilisation of 13 of the 14 tree species. For all 13 species, we found positive correlations between local abundance and appearance in the diet, consistent with the importance of local ecology for diet composition. Nevertheless, more detailed comparisons of pairs of groups often revealed significant mismatches between the relative importance of a tree species and its local abundance. In conclusion, local variation merits increased attention by primatologists. While our results are compatible with the possibility that traditions exist on a local (group) rather than population scale, alternative explanations have to be considered.     

Acute changes in social composition and agonistic behavior in male vervet monkeys (Cercopithecus aethiops sabaeus)

Among nonhuman primates the composition of social groups influences the interactions of group members. We assessed the effects of acute changes in social composition on behavior among 15 adult male vervet monkeys (Cercopithecus aethiops sabaeus). Subjects were observed in their basal social groups which comprised 3 adult males, 2–4 adult females, and offspring; and in two subgroups consisting of either two or three adult males. Agonism and vigilance increased in smaller groups relative to basal conditions, while subjects in two-male groups displayed more aggression than those in three-male groups. These findings suggest that, among male vervet monkeys, acute disruption of stable social groups increases aggressive behavior, and that the amount of agonism is influenced by the composition of the consequent subgroups. © 1992 Wiley-Liss, Inc.     

Role of spatial memory in primate foraging patterns: Saguinus mystax and Saguinus fuscicollis

From field data collected in the Amazon Basin of northeastern Peru, I present evidence that moustached (Saguinus mystax) and saddle-back (Saguinus fuscicollis) tamarins maintain detailed knowledge of the distribution and location of many tree species in their home range. During the wet season months of October through December 1984, fruits and exudates from 20 tree species and over 150 individual trees accounted for 75% of plant feeding time. These trees exhibited a patchy distribution; mean nearest-neighbor distances between trees of the same species averaged 148 meters. Moustached and saddle-back tamarins visited an average of 13 trees per day, concentrating their feeding efforts on 4–11 individual trees from a small number of target species. In 70% of all cases the nearest tree of a given species was selected as the next feeding site. Movement between these sites was characterized by relatively straight-line travel. It is argued that S. mystax and S. fuscicollis offset the patchiness component of the fruit and exudate part of their diet through goal-directed foraging and an ability to compare accurately the distances and directions from their present location to a large number of potential feeding trees.     

The psychology of primate cooperation and competition: a call for realigning research agendas

Cooperation and competition are two key components of social life. Current research agendas investigating the psychological underpinnings of competition and cooperation in non-human primates are misaligned. The majority of work on competition has been done in the context of theory of mind and deception, while work on cooperation has mostly focused on collaboration and helping. The current impression that theory of mind is not necessarily implicated in cooperative activities and that helping could not be an integral part of competition might therefore be rather misleading. Furthermore, theory of mind research has mainly focused on cognitive aspects like the type of stimuli controlling responses, the nature of representation and how those representations are acquired, while collaboration and helping have focused primarily on motivational aspects like prosociality, common goals and a sense of justice and other-regarding concerns. We present the current state of these two bodies of research paying special attention to how they have developed and diverged over the years. We propose potential directions to realign the research agendas to investigate the psychological underpinnings of cooperation and competition in primates and other animals.     

Video demonstrations seed alternative problem-solving techniques in wild common marmosets

Studies of social learning and tradition formation under field conditions have recently gained momentum, but suffer from the limited control of socio-ecological factors thought to be responsible for transmission patterns. The use of artificial visual stimuli is a potentially powerful tool to overcome some of these problems. Here, in a field experiment, we used video images of unfamiliar conspecifics performing virtual demonstrations of foraging techniques. We tested 12 family groups of wild common marmosets. Six groups received video demonstrations (footage of conspecifics either pulling a drawer open or pushing a lid upwards, in an ‘artificial fruit’); the other six groups served as controls (exposed to a static image of a conspecific next to the fruit). Subjects in video groups were more manipulative and successful in opening the fruit than controls; they were also more likely to use the technique they had witnessed and thus could serve as live models for other family members. To our knowledge, this is the first study that used video demonstrations in the wild and demonstrated the potent force of social learning, even from unfamiliar conspecifics, under field conditions.     

Adaptations for social cognition in the primate brain

Studies of the factors affecting reproductive success in group-living monkeys have traditionally focused on competitive traits, like the acquisition of high dominance rank. Recent research, however, indicates that the ability to form cooperative social bonds has an equally strong effect on fitness. Two implications follow. First, strong social bonds make individuals'' fitness interdependent and the ‘free-rider’ problem disappears. Second, individuals must make adaptive choices that balance competition and cooperation—often with the same partners. The proximate mechanisms underlying these behaviours are only just beginning to be understood. Recent results from cognitive and systems neuroscience provide us some evidence that many social and non-social decisions are mediated ultimately by abstract, domain-general neural mechanisms. However, other populations of neurons in the orbitofrontal cortex, striatum, amygdala and parietal cortex specifically encode the type, importance and value of social information. Whether these specialized populations of neurons arise by selection or through developmental plasticity in response to the challenges of social life remains unknown. Many brain areas are homologous and show similar patterns of activity in human and non-human primates. In both groups, cortical activity is modulated by hormones like oxytocin and by the action of certain genes that may affect individual differences in behaviour. Taken together, results suggest that differences in cooperation between the two groups are a matter of degree rather than constituting a fundamental, qualitative distinction.     

Social structure of primate interaction networks facilitates the emergence of cooperation

Animal cooperation has puzzled biologists for a long time as its existence seems to contravene the basic notion of evolutionary biology that natural selection favours ‘selfish’ genes that promote only their own well-being. Evolutionary game theory has shown that cooperators can prosper in populations of selfish individuals if they occur in clusters, interacting more frequently with each other than with the selfish. Here we show that social networks of primates possess the necessary social structure to promote the emergence of cooperation. By simulating evolutionary dynamics of cooperative behaviour on interaction networks of 70 primate groups, we found that for most groups network reciprocity augmented the fixation probability for cooperation. The variation in the strength of this effect can be partly explained by the groups’ community modularity—a network measure for the groups’ heterogeneity. Thus, given selective update and partner choice mechanisms, network reciprocity has the potential to explain socially learned forms of cooperation in primate societies.     

Reducing the primate pet trade: Actions for primatologists

This commentary emerged from a panel presentation at the International Primatological Society Congress in Nairobi, Kenya, 2018. The goal was to provide regional updates on the status of primate removal from habitat countries, especially for the pet trade, and develop guidelines that could help primatologists address this critical problem. The trade in live primates includes those used as pets, in entertainment, and as subjects of biomedical experimentation, but here we focus on those primates destined for the pet trade. Such transactions are a hugely lucrative business, impacting hundreds of thousands of individuals annually and affecting the survival of wild populations. Being intimately familiar with primate social behavior, life history and biology, primatologists, whether they work with captive or wild primates, are in a unique position to understand the nature of the trade and attempt to counter its effects. In addition to updating the status of the primate pet trade, we provide recommendations that may help primatologists formulate a plan to deal, locally and regionally, with illegal trafficking in live primates. General guidelines include increasing awareness of local customs, policies and laws; developing collaborative research opportunities for local people; engaging in training/informational opportunities; and instructing on how to take action when encountering illegally-trafficked primates.     

Formidable females redux: male social integration into female networks and the value of dynamic multilayer networks

The development of multilayer network techniques is a boon for researchers who wish to understand how different interaction layers might influence each other,and how these in turn might influence group dynamics.Here,we investigate how integration between male and female grooming and aggression interaction networks influences male power trajectories in vervet monkeys Chlorocebus pygerythrus.Our previous analyses of this phenomenon used a monolayer approach,and our aim here is to extend these analyses using a dynamic multilayer approach.To do so,we constructed a temporal series of male and female interaction layers.We then used a multivariate multilevel autoregression model to compare cross-lagged associations between a male's centrality in the female grooming layer and changes in male Elo ratings.Our results confirmed our original findings:changes in male centrality within the female grooming network were weakly but positively tied to changes in their Elo ratings.However,the multilayer network approach offered additional insights into this social process,identifying how changes in a male's centrality cascade through the other network layers.This dynamic view indicates that the changes in Elo ratings are likely to be short-lived,but that male centrality within the female network had a much stronger impact throughout the multilayer network as a whole,especially on reducing intermale aggression(i.e.,aggression directed by males toward other males).We suggest that multilayer social network approaches can take advantage of increased amounts of social data that are more commonly collected these days,using a variety of methods.Such data are inherently multilevel and multilayered,and thus offer the ability to quantify more precisely the dynamics of animal social behaviors.     

Social tolerance in a despotic primate: co-feeding between consortship partners in rhesus macaques

Food sharing among nonkin-one of the most fascinating cooperative behaviors in humans-is not widespread in nonhuman primates. Over the past few years, a large body of work has investigated the contexts in which primates cooperate and share food with unrelated individuals. This work has successfully demonstrated that species-specific differences in temperament constrain the extent to which food sharing emerges in experimental situations, with despotic species being less likely to share food than tolerant ones. However, little experimental work has examined the contexts that promote food sharing and cooperation within a species. Here, we examine whether one salient reproductive context-the consortship dyad-can allow the necessary social tolerance for co-feeding to emerge in an extremely despotic species, the rhesus macaque (Macaca mulatta). We gave naturally formed male-female rhesus macaque pairs access to a monopolizable food site in the free-ranging population at Cayo Santiago, Puerto Rico. Using this method, we were able to show that tolerated co-feeding between unrelated adults can take place in this despotic species. Specifically, our results show that consort pairs co-fed at the experimental food site more than nonconsort control pairs, leading females to obtain more food in this context. These results suggest that co-feeding is possible even in the most despotic of primate species, but perhaps only in contexts that specifically promote the necessary social tolerance. Researchers might profit from exploring whether other kinds of within-species contexts could also generate cooperative behaviors.     

Simian immunodeficiency viruses replication dynamics in African non-human primate hosts: common patterns and species-specific differences

METHODS: To define potential common features of simian immunodeficiency virus (SIV) infections in different naturally infected host species, we compared the dynamics of viral replication in 31 African green monkeys (10 sabeus, 15 vervets and seven Caribbean AGMs), 14 mandrills and three sooty mangabeys (SMs) that were experimentally infected with their species-specific viruses. RESULTS: After infection, these SIVs replicated rapidly reaching viral loads (VLs) of 10(5)-10(9) copies/ml of plasma between days 9-14 post-infection (p.i). Set point viremia was established between days 42 and 60 p.i., with levels of approximately 10(5)-10(6) copies/ml in SM and mandrills, and lower levels (10(3)-10(5) copies/ml) in AGMs. VL during the chronic phase did not correlate with viral genome structure: SIVmnd-2 (a vpx-containing virus) and SIVmnd-1 (which does not contain vpu or vpx) replicated to similar levels in mandrills. VL was dependent on virus strain: vervets infected with three different viral strains showed different patterns of viral replication. The pattern of viral replication of SIVagm.sab, which uses both CCR5 and CXCR4 co-receptors was similar to those of the other viruses. CONCLUSIONS: Our results show a common pattern of SIV replication in naturally and experimentally infected hosts. This is similar overall to that observed in pathogenic SIV infection of macaques. This result indicates that differences in clinical outcome between pathogenic and non-pathogenic infections rely on host responses rather than the characteristics of the virus itself.