Social networks analysis in primates, a multilevel perspective

Accentuated lines in dental microstructure are hypothesized to correlate with potentially stressful life history events, but our understanding of when, how and why such accentuated lines form in relation to stressful events is limited. We examined accentuated line formation and life history events in the teeth of three naturally deceased mandrills (Mandrillus sphinx, Cercopithecidae), for whom we had detailed life history information. We determined the ages at formation of accentuated lines in histological tooth sections and used dates of birth and death to calibrate dental histology to calendar time and individual age. We found accentuated lines that matched their mother's resumption of sexual cycles in two individuals, and possibly in the third individual. The subjects also formed lines when their mothers were mate-guarded by males or wounded. Accentuated lines matched the birth of the next sibling in one of two cases. Both females formed accentuated lines when they experienced their own sexual swelling cycles, but lines did not match all sexual swelling cycles. Mate-guarding matched an accentuated line in one case, but not in another. Lines matched all three parturitions in the two females. Changes in alpha male and captures did not consistently coincide with accentuated line formation, but repeated captures were associated with lines. Using simulated data, we show that the observed number of matches between lines and events would be very unlikely under a null hypothesis of random line formation. Our results support the hypothesis that some life history events are physiologically stressful enough to cause accentuated line formation in teeth. They contribute to our understanding of how primate life histories are recorded during dental development and enhance our ability to use teeth to reconstruct life history in the absence of direct observation.

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.

How animals interact and develop social relationships in face of sociodemographic and ecological pressures is of great interest. New methodologies, in particular Social Network Analysis (SNA), allow us to elucidate these types of questions. However, the different methodologies developed to that end and the speed at which they emerge make their use difficult. Moreover, the lack of communication between the different software developed to provide an answer to the same/different research questions is a source of confusion. The R package ‘Animal Network Toolkit’ (ANT) was developed with the aim of implementing in one package the different social network analysis techniques currently used in the study of animal social networks. Hence, ANT is a toolkit for animal research allowing among other things to: 1) measure global, dyadic and nodal networks metrics; 2) perform data randomization: pre- and post-network (node and link permutations); 3) perform statistical permutation tests. The package is partially coded in C++ for an optimal computing speed. The package gives researchers a workflow from the raw data to the achievement of statistical analyses, allowing for a multilevel approach: from the individual's position and role within the network, to the identification of interactional patterns, and the study of the overall network properties. Furthermore, ANT also provides a guideline on the SNA techniques used: 1) from the appropriate randomization technique according to the data collected; 2) to the choice, the meaning, the limitations and advantages of the network metrics to apply, 3) and the type of statistical tests to run.

Group-living animals rely on efficient transmission of information for optimal exploitation of their habitat. How efficient and resilient a network is depend on its structure, which is a consequence of the social interactions of the individuals that comprise the network. In macaques, network structure differs according to dominance style. Networks of intolerant species are more modular, more centralized, and less connected than those of tolerant ones. Given these structural differences, networks of intolerant species are potentially more vulnerable to fragmentation and decreased information transmission when central individuals disappear. Here we studied network resilience and efficiency in artificial societies of macaques. The networks were produced with an individual-based model that has been shown to reproduce the structural features of networks of tolerant and intolerant macaques. To study network resilience, we deleted either central individuals or individuals at random and studied the effects of these deletions on network cohesiveness and efficiency. The deletion of central individuals had more negative effects than random deletions from the networks of both tolerant and intolerant artificial societies. Central individuals thus appeared to aid in the maintenance of network cohesiveness and efficiency. Further, the networks of both intolerant and tolerant societies appeared to be robust to the loss of individuals, as network fragmentation was never observed. Our results suggest that despite differences in network structure, networks of tolerant and intolerant macaques may be equally resilient.

Group-living animals rely on efficient transmission of information for optimal exploitation of their habitat. How efficient and resilient a network is depend on its structure, which is a consequence of the social interactions of the individuals that comprise the network. In macaques, network structure differs according to dominance style. Networks of intolerant species are more modular, more centralized, and less connected than those of tolerant ones. Given these structural differences, networks of intolerant species are potentially more vulnerable to fragmentation and decreased information transmission when central individuals disappear. Here we studied network resilience and efficiency in artificial societies of macaques. The networks were produced with an individual-based model that has been shown to reproduce the structural features of networks of tolerant and intolerant macaques. To study network resilience, we deleted either central individuals or individuals at random and studied the effects of these deletions on network cohesiveness and efficiency. The deletion of central individuals had more negative effects than random deletions from the networks of both tolerant and intolerant artificial societies. Central individuals thus appeared to aid in the maintenance of network cohesiveness and efficiency. Further, the networks of both intolerant and tolerant societies appeared to be robust to the loss of individuals, as network fragmentation was never observed. Our results suggest that despite differences in network structure, networks of tolerant and intolerant macaques may be equally resilient.

Since group-living animals are embedded in a network of social interactions, socioecological factors may not only affect individual behavioural strategies but also the patterning of group-level social interactions, i.e. the network structure. These co-variations between socioecological factors, individual behaviour, and group-level structure are important to study since ecological factors may strongly influence animal health outcomes and reproductive success. Besides factors such as social information and/or infectious agents, with far-reaching individual fitness consequences, seem independent of individuals’ own social interactions but directly affected by the topology of the social network. This paper reviews how socio-ecological pressures, i.e., causal factors (food distribution, predation and infectious agent risk), via intermediary mechanisms (stress, information sharing and mating system), may affect individual social behaviour and consequently, social network topology. We also discuss how evolutionary driving forces, genetic (i.e. genes) and cultural (i.e. learned behaviour) selection, may result in a specific composition of individuals’ social strategies that produce network topologies that might be optimized to specific socio-ecological conditions. We conclude that studies focusing on whether and how well networks resist to changing conditions might provide a better understanding of the rules underlying individual behaviour, which in turn influences network topology - a process we have called network evolution. Evolutionary processes may favour a group phenotypic composition, thus a network topology. This has been referred to as a “collective social niche construction”.

In group-living animals, individuals do not interact uniformly with their conspecifics. Among primates, such heterogeneity in partner choice can be discerned from affiliative grooming patterns. While the preference for selecting close kin as grooming partners is ubiquitous across the primate order, the selection of higher-ranking non-kin individuals as grooming partners is less common. We studied a group of provisioned rhesus macaques (Macaca mulatta brevicaudus) on Hainan Island, China, to examine rank-related benefits of grooming exchanges and the influence of kin relationships. We tested four hypotheses based on Seyfarth’s model: (1) there will be kin preference in grooming relationships; (2) grooming between non-kin individuals will be directed up the dominance rank; (3) grooming between non-kin individuals will reduce aggression from higher-ranking ones; and (4) non-kin individuals will spend more time grooming with adjacent ranked ones. We found that grooming relationships between kin individuals were stronger than those between non-kin individuals. For non-kin relationships, lower-ranking individuals received less aggression from higher-ranking ones through grooming; a benefit they could not derive through grooming exchanges with individuals related by kinship. Individuals spent more time grooming adjacent higher-ranking non-kin individuals and higher-ranking individuals also received more grooming from non-kin individuals. Our results supported Seyfarth’s model for predicting partner choice between non-kin individuals. For relationships between kin individuals, we found results that were not consistent with prediction for the exchanges of aggression and grooming, indicating the importance to control for the influence of kinship in future studies.

Three mechanisms have been proposed to underlie reciprocation of social behaviors in gregarious animals: "calculated reciprocity," "emotional bookkeeping," and "symmetry-based reciprocity." Among these explanations, emotional book-keeping has received the broadest support from experimental and observational studies. On the other hand, 3 individual-based models have shown that reciprocation may emerge via "symmetry-based reciprocity," "emotional bookkeeping," or a combination of both mechanisms. Here, we use these 3 models to assess their relative fit with empirical data on reciprocation and social network structure across different groups and species of macaques. We collected grooming data from 14 groups and 8 macaque species and simulated each group in each model. We analyzed and quantitatively compared social network metrics of the empirical and the models' grooming networks. The 3 models captured fairly well the features of observed networks, and fitted data from wild groups better than captive ones. The emotional bookkeeping model seemed on average to fit slightly better the social networks metrics observed in empirical data, but failed to reproduce some grooming patterns. The symmetry-based models, on the other hand, fitted better other network parameters (e.g., modularity). No model generally fitted the data better than the others, and the fit with some metrics (e.g., modularity, centralization index) was low even after optimization. Thus, our analyses indicate that in the models social interactions may be simpler than in reality and models may miss social processes (e.g., third-party awareness).

Among the stressors that can affect animal welfare in zoos, the immediate effect of relocation to a novel environment is one that has received little attention in the literature. Here, we compare the social network, daily activity and the expression of stress-related behavior in capuchins (Cebus apella) and squirrel monkeys (Saimiri sciureus) before and just after they were relocated to a new enriched enclosure. Results showed similar immediate responses to the move in the two species. Both showed a substantial increase in the time spent resting and spent more time in the highest and "safest" part of their enclosure after relocation. Both capuchins and squirrel monkeys spent significantly more time in close proximity to other group members after relocation, compared to before. In squirrel monkeys, the structure of the social network, which was initially correlated to affiliation, was no longer so after the move. In capuchins, the network analysis showed that individuals regrouped by age, with the youngsters who were potentially more affected by stress being in the center of the network. Social network analysis helped to achieve a more complete picture of how individuals were affected by relocation. We suggest that this type of analysis should be used alongside traditional methods of observation and analysis to encompass the most complex aspects of animal behavior in times of stress and to improve welfare.

Social network analysis offers new tools to study the social structure of primate groups. We used social network analysis to investigate the cohesiveness of a grooming network in a captive chimpanzee group (N = 17) and the role that individuals may play in it. Using data from a year-long observation, we constructed an unweighted social network of preferred grooming interactions by retaining only those dyads that groomed above the group mean. This choice of criterion was validated by the finding that the properties of the unweighted network correlated with the properties of a weighted network (i.e. a network representing the frequency of grooming interactions) constructed from the same data. To investigate group cohesion, we tested the resilience of the unweighted grooming network to the removal of central individuals (i.e. individuals with high betweenness centrality). The network fragmented more after the removal of individuals with high betweenness centrality than after the removal of random individuals. Central individuals played a pivotal role in maintaining the network's cohesiveness, and we suggest that this may be a typical property of affiliative networks like grooming networks. We found that the grooming network correlated with kinship and age, and that individuals with higher social status occupied more central positions in the network. Overall, the grooming network showed a heterogeneous structure, yet did not exhibit scale-free properties similar to many other primate networks. We discuss our results in light of recent findings on animal social networks and chimpanzee grooming.

Multilevel social systems have evolved in several species of cercopithecoid primates and appear to be an effective means of changing group size amid variation in environmental conditions. Larger groupings of these species fission and fuse, making intraunit relationships essential to maintain the integrity of the smallest social units. We examine these intraunit relationships in four primates with multilevel social systems: proboscis monkeys (Nasalis larvatus), snub-nosed monkeys (Rhinopithecus roxellana), hamadryas baboons (Papio hamadryas), and geladas (Theropithecus gelada), using social network analysis. The proboscis monkeys and hamadryas baboons were wild and unprovisioned, whereas the snub-nosed monkeys and geladas were partly provisioned. Comparison of eigenvector centrality coefficients revealed a phylogenetic difference in the key individuals maintaining social networks between the colobines and the cercopithecines: females were more central in proboscis and snub-nosed monkeys, with males generally peripheral to social interaction, whereas males were more central than females in geladas and hamadryas. A comparison of sex differences in clustering coefficients, however, revealed a significant difference only in geladas, suggesting that one-male–multifemale units in this species become more unstable when females, but not males, are removed from social networks. Taken together, our results reveal the strongest differences between geladas, characterized by female philopatry and male dispersal, and the three species with bisexual dispersal. These results demonstrate the potential for social network analysis to reveal the social bonds most important for maintaining cohesion of the smallest units of primate multilevel societies. This, in turn, can serve as a proxy, in the absence of long-term data, for underlying patterns of sex-biased dispersal and philopatry.

Early maternal loss may influence later social functioning in human and non-human primates. Previously, we found social grooming to be more strongly affected in chimpanzees that were maternally and socially deprived in their early infancy (ED) compared to later deprived (LD) and non-deprived ones. In these studies, all deprived chimpanzees were captured in the wild. In addition to the loss of the mother, these wild-caught individuals also witnessed the killing of their mother and experienced a radical change in living conditions. Therefore, we expected wildcaught EDs to be more strongly affected in their social grooming activity than captive-born EDs who were rejected by their mothers. In the present study, we evaluated the social grooming networks of two all-male groups. One group, housed at the primate house in Gaenserndorf, Austria, consisted of 7 ex-laboratory individuals (6 wild-caught EDs and 1 LD) and was studied during the first year of group life. The second group, housed at the Kumamoto Sanctuary in Japan, consisted of 15 mainly ex-laboratory individuals (6 wild-caught EDs, 6 captive-born EDs, and 3 LDs) and had been stable for two years, though individual males had been socially housed for up to 20 years. We compared two different network measures reflecting the individual grooming activity and the evenness in the distribution of grooming among group members between wild-caught ( n = 12) and captive-born ED males ( n = 6). Contrary to our expectation, we found no difference between wild-caught and captive-born EDs, neither in terms of their grooming activity nor in their distribution of grooming among group mates. Moreover, there was no association between grooming network measures and years spent socially housed. Even though we cannot draw a clear causal link due to the retrospective nature of this and previous studies, our findings show that early maternal loss affects not only wild-caught but also captive-born chimpanzees’ social grooming competence in the long-term.

Among nonhuman primates, the evolutionary underpinnings of variation in social structure remain debated, with both ancestral relationships and adaptation to current conditions hypothesized to play determining roles. Here we assess whether interspecific variation in higher-order aspects of female macaque (genus: Macaca) dominance and grooming social structure show phylogenetic signals, that is, greater similarity among more closely-related species. We use a social network approach to describe higher-order characteristics of social structure, based on both direct interactions and secondary pathways that connect group members. We also ask whether network traits covary with each other, with species-typical social style grades, and/or with sociodemographic characteristics, specifically group size, sex-ratio, and current living condition (captive vs. free-living). We assembled 34–38 datasets of female-female dyadic aggression and allogrooming among captive and free-living macaques representing 10 species. We calculated dominance (transitivity, certainty), and grooming (centrality coefficient, Newman's modularity, clustering coefficient) network traits as aspects of social structure. Computations of K statistics and randomization tests on multiple phylogenies revealed moderate-strong phylogenetic signals in dominance traits, but moderate-weak signals in grooming traits. GLMMs showed that grooming traits did not covary with dominance traits and/or social style grade. Rather, modularity and clustering coefficient, but not centrality coefficient, were strongly predicted by group size and current living condition. Specifically, larger groups showed more modular networks with sparsely-connected clusters than smaller groups. Further, this effect was independent of variation in living condition, and/or sampling effort. In summary, our results reveal that female dominance networks were more phylogenetically conserved across macaque species than grooming networks, which were more labile to sociodemographic factors. Such findings narrow down the processes that influence interspecific variation in two core aspects of macaque social structure. Future directions should include using phylogeographic approaches, and addressing challenges in examining the effects of socioecological factors on primate social structure.

Social play and grooming are typical affiliative interactions for many primate species, and are thought to have similar biological functions. However, grooming increases with age, whereas social play decreases. We proposed the hypothesis that both social grooming and social play in juveniles strengthen their social bonds in daily activities. We carried out field research on the social relationships among juvenile wild Japanese macaques in a troop in Kinkazan, Miyagi Prefecture, Japan, from fall 2007 to spring 2008 to investigate this hypothesis. We evaluated three relationships among juveniles, play indices (PI), grooming indices (GI), and 3-m-proximity indices (3mI) of each dyad (i.e., interacting pair), and compared these social networks based on the matrices of the indices. The play and grooming networks were correlated with the association network throughout the two research periods. The multiple network level measurements of the play network, but not the grooming network, resembled those of the association network. Using a causal step approach, we showed that social play and grooming interactions in fall seem to predict associations in the following spring, controlling for the PI and GI matrix in spring, respectively. Social play and grooming for each juvenile were negatively correlated. The results partially support our predictions; therefore, the hypothesis that the biological function of social play among immature Japanese macaques is to strengthen their social bonds in the near future and develop their social life appears to be correct. For juvenile macaques, social play, rather than grooming, functions as an important social mechanism to strengthen affiliative relationships.