Effect of behavioural sampling methods on local and global social network metrics: a case-study of three macaque species.

Social network analysis (SNA) is a powerful, quantitative tool to measure animals' direct and indirect social connectedness in the context of social groups. However, the extent to which behavioural sampling methods influence SNA metrics remains unclear. To fill this gap, here we compare network indices of grooming, huddling, and aggression calculated from data collected from three macaque species through two sampling methods: focal animal sampling (FAS) and all-occurrences behaviour sampling (ABS). We found that measures of direct connectedness (degree centrality, and network density) were correlated between FAS and ABS for all social behaviours. Eigenvector and betweenness centralities were correlated for grooming and aggression networks across all species. By contrast, for huddling, we found a correlation only for betweenness centrality while eigenvector centralities were correlated only for the tolerant bonnet macaque but not so for the despotic rhesus macaque. Grooming and huddling network modularity and centralization were correlated between FAS and ABS for all but three of the eight groups. By contrast, for aggression network, we found a correlation for network centralization but not modularity between the sampling methodologies. We discuss how our findings provide researchers with new guidelines regarding choosing the appropriate sampling method to estimate social network metrics.

Impact of joint interactions with humans and social interactions with conspecifics on the risk of zooanthroponotic outbreaks among wildlife populations.

Pandemics caused by pathogens that originate in wildlife highlight the importance of understanding the behavioral ecology of disease outbreaks at human-wildlife interfaces. Specifically, the relative effects of human-wildlife and wildlife-wildlife interactions on disease outbreaks among wildlife populations in urban and peri-urban environments remain unclear. We used social network analysis and epidemiological Susceptible-Infected-Recovered models to simulate zooanthroponotic outbreaks, through wild animals' joint propensities to co-interact with humans, and their social grooming of conspecifics. On 10 groups of macaques (Macaca spp.) in peri-urban environments in Asia, we collected behavioral data using event sampling of human-macaque interactions within the same time and space, and focal sampling of macaques' social interactions with conspecifics and overall anthropogenic exposure. Model-predicted outbreak sizes were related to structural features of macaques' networks. For all three species, and for both anthropogenic (co-interactions) and social (grooming) contexts, outbreak sizes were positively correlated to the network centrality of first-infected macaques. Across host species and contexts, the above effects were stronger through macaques' human co-interaction networks than through their grooming networks, particularly for rhesus and bonnet macaques. Long-tailed macaques appeared to show intraspecific variation in these effects. Our findings suggest that among wildlife in anthropogenically-impacted environments, the structure of their aggregations around anthropogenic factors makes them more vulnerable to zooanthroponotic outbreaks than their social structure. The global features of these networks that influence disease outbreaks, and their underlying socio-ecological covariates, need further investigation. Animals that consistently interact with both humans and their conspecifics are important targets for disease control.

Implementing social network analysis to understand the socioecology of wildlife co-occurrence and joint interactions with humans in anthropogenic environments.

Human population expansion into wildlife habitats has increased interest in the behavioural ecology of human-wildlife interactions. To date, however, the socioecological factors that determine whether, when or where wild animals take risks by interacting with humans and anthropogenic factors still remains unclear. We adopt a comparative approach to address this gap, using social network analysis (SNA). SNA, increasingly implemented to determine human impact on wildlife ecology, can be a powerful tool to understand how animal socioecology influences the spatiotemporal distribution of human-wildlife interactions. For 10 groups of rhesus, long-tailed and bonnet macaques (Macaca spp.) living in anthropogenically impacted environments in Asia, we collected data on human-macaque interactions, animal demographics, and macaque-macaque agonistic and affiliative social interactions. We constructed 'human co-interaction networks' based on associations between macaques that interacted with humans within the same time and spatial locations, and social networks based on macaque-macaque allogrooming behaviour, affiliative behaviours of short duration (agonistic support, lip-smacking, silent bare-teeth displays and non-sexual mounting) and proximity. Pre-network permutation tests revealed that, within all macaque groups, specific individuals jointly took risks by repeatedly, consistently co-interacting with humans within and across time and space. GLMMs revealed that macaques' tendencies to co-interact with humans was positively predicted by their tendencies to engage in short-duration affiliative interactions and tolerance of conspecifics, although the latter varied across species (bonnets>rhesus>long-tailed). Male macaques were more likely to co-interact with humans than females. Neither macaques' grooming relationships nor their dominance ranks predicted their tendencies to co-interact with humans. Our findings suggest that, in challenging anthropogenic environments, less (compared to more) time-consuming forms of affiliation, and additionally greater social tolerance in less ecologically flexible species with a shorter history of exposure to humans, may be key to animals' joint propensities to take risks to gain access to resources. For males, greater exploratory tendencies and less energetically demanding long-term life-history strategies (compared to females) may also influence such joint risk-taking. From conservation and public health perspectives, wildlife connectedness within such co-interaction networks may inform interventions to mitigate zoonosis, and move human-wildlife interactions from conflict towards coexistence.

Oil palm cultivation critically affects sociality in a threatened Malaysian primate.

Human-induced habitat alterations globally threaten animal populations, often evoking complex behavioural responses in wildlife. This may be particularly dramatic when negatively affecting social behaviour, which fundamentally determines individual fitness and offspring survival in group-living animals. Here, we provide first evidence for significant behavioural modifications in sociality of southern pig-tailed macaques visiting Malaysian oil palm plantations in search of food despite elevated predation risk. Specifically, we found critical reductions of key positive social interactions but higher rates of aggression in the plantation interior compared to the plantation edge (i.e. plantation areas bordering the forest) and the forest. At the plantation edge, affiliation even increased compared to the forest, while central positions in the macaques' social network structure shifted from high-ranking adult females and immatures to low-ranking individuals. Further, plantations also affected mother-infant relationships, with macaque mothers being more protective in the open plantation environment. We suggest that although primates can temporarily persist in human-altered habitats, their ability to permanently adapt requires the presence of close-by forest and comes with a trade-off in sociality, potentially hampering individual fitness and infant survival. Studies like ours remain critical for understanding species' adaptability to anthropogenic landscapes, which may ultimately contribute to facilitating their coexistence with humans and preserving biodiversity.

Female social structure influences, and is influenced by, male introduction and integration success among captive rhesus macaques (Macaca mulatta).

Animal social structure is influenced by multiple socioecological factors. Of these, the links between changes to group demography through the arrival of new individuals and residents' social structure remain unclear. Across seven groups of captive rhesus macaques (Macaca mulatta), we examine how male introductions may be influenced by, and in-turn influence, aspects of female social structure. GLMMs revealed that males integrated more successfully into groups in which females showed more 'despotic' social structures, i.e., higher aggression rates, steeper dominance hierarchies, and greater rank-skew in allogrooming network connectedness. Yet during periods that followed males' social integration, females increased their social tolerance (decreased aggression and shallower hierarchies) and group cohesivity (less clustered allogrooming networks), but retained their tendencies to groom dominants. Our findings, independent of group size and matrilineal relatedness, help better understand how dispersal/immigration may influence social structure, and how assessing changes to social structure may inform macaque welfare and management.

Impact of individual demographic and social factors on human-wildlife interactions: a comparative study of three macaque species.

Despite increasing conflict at human-wildlife interfaces, there exists little research on how the attributes and behavior of individual wild animals may influence human-wildlife interactions. Adopting a comparative approach, we examined the impact of animals' life-history and social attributes on interactions between humans and (peri)urban macaques in Asia. For 10 groups of rhesus, long-tailed, and bonnet macaques, we collected social behavior, spatial data, and human-interaction data for 11-20 months on pre-identified individuals. Mixed-model analysis revealed that, across all species, males and spatially peripheral individuals interacted with humans the most, and that high-ranking individuals initiated more interactions with humans than low-rankers. Among bonnet macaques, but not rhesus or long-tailed macaques, individuals who were more well-connected in their grooming network interacted more frequently with humans than less well-connected individuals. From an evolutionary perspective, our results suggest that individuals incurring lower costs related to their life-history (males) and resource-access (high rank; strong social connections within a socially tolerant macaque species), but also higher costs on account of compromising the advantages of being in the core of their group (spatial periphery), are the most likely to take risks by interacting with humans in anthropogenic environments. From a conservation perspective, evaluating individual behavior will better inform efforts to minimize conflict-related costs and zoonotic-risk.

Impact of anthropogenic factors on affiliative behaviors among bonnet macaques.

OBJECTIVES: In primates, allogrooming and other affiliative behaviors confer many benefits and may be influenced by many socioecological factors. Of these, the impact of anthropogenic factors remain relatively understudied. Here we ask whether interactions with humans decreased macaques' affiliative behaviors by imposing time-constraints, or increased these behaviors on account of more free-/available-time due to macaques' consumption of high-energy human foods. MATERIALS AND METHODS: In Southern India, we collected data on human-macaque and macaque-macaque interactions using focal-animal sampling on two groups of semi-urban bonnet macaques for 11 months. For each macaque within each climatic season, we calculated frequencies of human-macaque interactions, rates of monitoring human activity and foraging on anthropogenic food, dominance ranks, grooming duration, number of unique grooming partners, and frequencies of other affiliative interactions. RESULTS: We found strong evidence for time-constraints on grooming. Macaques that monitored humans more groomed for shorter durations and groomed fewer partners, independent of their group membership, sex, dominance rank, and season. However, monitoring humans had no impact on other affiliative interactions. We found no evidence for the free-time hypothesis: foraging on anthropogenic food was unrelated to grooming and other affiliation. DISCUSSION: Our results are consistent with recent findings on other urban-dwelling species/populations. Macaques in such environments may be especially reliant on other forms of affiliation that are of short duration (e.g., coalitionary support, lip-smacking) and unaffected by time-constraints. We stress on the importance of evaluating human impact on inter-individual differences in primate/wildlife behavior for conservation efforts.

Individuals in urban dwelling primate species face unequal benefits associated with living in an anthropogenic environment.

In primates, living in an anthropogenic environment can significantly improve an individual's fitness, which is likely attributed to access to anthropogenic food resources. However, in non-professionally provisioned groups, few studies have examined whether individual attributes, such as dominance rank and sex, affect primates' ability to access anthropogenic food. Here, we investigated whether rank and sex explain individual differences in the proportion of anthropogenic food consumed by macaques. We observed 319 individuals living in nine urban groups across three macaque species. We used proportion of anthropogenic food in the diet as a proxy of access to those food resources. Males and high-ranking individuals in both sexes had significantly higher proportions of anthropogenic food in their diets than other individuals. We speculate that unequal access to anthropogenic food resources further increases within-group competition, and may limit fitness benefits in an anthropogenic environment to certain individuals.

Time matching between grooming partners: Do methodological distinctions between short versus long-term reciprocation matter?

Primatologists have long focused on grooming exchanges to examine aspects of social relationships, co-operation, and social cognition. One particular interest is the extent to which reciprocating grooming partners time match, and the time frame over which they do so. Conclusions about time matching vary across species. Generally, researchers focus on the duration of pauses between grooming episodes that involve a switch in partner roles and choose a cut-off point to distinguish short from longer-term reciprocation. Problematically, researchers have made inconsistent choices about cut-offs. Such methodological variations are potentially concerning, as it is unclear whether inconsistent conclusions about short-term time matching are attributable to species/ecological differences, or are due in part to methodological inconsistency. We ask whether various criteria for separating short versus long-term reciprocation influence conclusions about short-term time matching using data from free-ranging rhesus ( Macaca mulatta) and captive-crested macaques ( Macaca nigra). We compare several commonly used cut-offs to ones generated by the currently preferred approach-survival analysis. Crested macaques displayed a mild degree of time matching regardless of the cutoff used. For rhesus macaques, whereas most cut-offs yielded similar degrees of time matching as the one derived from survival analysis, very short ones significantly underestimated both the degree of time matching and the influence of rank distance on time matching. Although researchers may have some flexibility in their choice of cut-offs, we suggest that they employ caution by using survival analysis when possible, and when not possible, by avoiding very short time windows.

Affiliation and disease risk: social networks mediate gut microbial transmission among rhesus macaques.

In social animals, affiliative behaviours bring many benefits, but also costs such as disease risk. The ways in which affiliation may affect the risk of infectious agent transmission remain unclear. Moreover, studies linking variation in affiliative interactions to infectious agent incidence/diversity have speculated that disease transmission may have occurred, rather than revealing that transmission did occur. We address these gaps using the phylogenetics of commensal gut Escherichia coli to determine whether affiliative grooming and huddling social networks mediated microbial transmission among rhesus macaques. We collected behavioural and microbial data from adult macaques across a 12-week period that was split into two 6-week phases to better detect dyadic transmission. We reconstructed undirected social networks from affiliative interactions and reconstructed microbial transmission networks from the pairwise phylogenetic similarity of E. coli pulsotypes from macaques within and across adjacent sampling events. Macaque E. coli pulsotypes were more phylogenetically similar to each other than to environmental isolates, which established a premise for socially mediated transmission. Dyadic grooming and huddling frequencies strongly influenced the likelihood of E. coli transmission during the second data collection phase, but not the first. Macaques that were more central/well connected in both their grooming and huddling networks were also more central in the E. coli transmission networks. Our results confirmed that affiliative grooming and huddling behaviours mediate the transmission of gut microbes among rhesus macaques, particularly among females and high-ranking individuals. The detectability of socially mediated E. coli transmission maybe partially masked by environmental acquisition in males, or by high frequencies of interactions in captivity. Predicting the potential transmission pathways of gastrointestinal parasites and pathogens, our findings add to current knowledge of the coevolutionary relationships between affiliative behaviour and health and may be used to identify 'superspreader' individuals as potential targets for disease control strategies.

Rates of human-macaque interactions affect grooming behavior among urban-dwelling rhesus macaques (Macaca mulatta).

OBJECTIVES: The impact of anthropogenic environmental changes may impose strong pressures on the behavioral flexibility of free-ranging animals. Here, we examine whether rates of interactions with humans had both a direct and indirect influence on the duration and distribution of social grooming in commensal rhesus macaques (Macaca mulatta). MATERIALS AND METHODS: Data were collected in two locations in the city of Shimla in northern India: an urban setting and a temple area. We divided these two locations in a series of similar-sized physical blocks (N = 48) with varying rates of human-macaque interactions. We conducted focal observations on three free-ranging rhesus macaque groups, one in the urban area and two in the temple area. RESULTS: Our analysis shows that macaques engaged in shorter grooming bouts and were more vigilant while grooming in focal sessions during which they interacted with people more frequently, suggesting that humans directly affected grooming effort and vigilance behavior. Furthermore, we found that in blocks characterized by higher rates of human-macaque interactions grooming bouts were shorter, more frequently interrupted by vigilance behavior, and were less frequently reciprocated. DISCUSSION: Our work shows that the rates of human-macaque interaction had both a direct and indirect impact on grooming behavior and that macaques flexibly modified their grooming interactions in relation to the rates of human-macaque interaction to which they were exposed. Because grooming has important social and hygienic functions in nonhuman primates, our work suggests that human presence can have important implications for animal health, social relationships and, ultimately, fitness. Our results point to the need of areas away from people even for highly adaptable species where they can engage in social interactions without human disruption.

The influence of phylogeny, social style, and sociodemographic factors on macaque social network structure.

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.

Prevalence of enteric bacterial parasites with respect to anthropogenic factors among commensal rhesus macaques in Dehradun, India.

There has been a recent surge in research on primate infectious disease ecology. Two major areas remain relatively unaddressed to date-the prevalence of enteric bacterial parasites and the role of anthropogenic environmental factors in parasite acquisition in commensally living primate populations. In this preliminary assessment, we address both these gaps by assessing the prevalence, and the role of anthropogenic factors in shaping this prevalence, of three enteric bacterial parasites-E . coli O157:H7, Salmonella sp., Shigella sp.-across populations of rhesus macaques (M. mulatta) that live commensally with humans in Dehradun, northern India. Across 10-week study period, we collected data on (1) human-macaque behavioral interactions, (2) macaque and human demographic and activity scans, and (3) macaque fecal samples from the environment at four different locations in Dehradun. Biochemical tests and morphology-based confirmations clearly established the presence of all three enteric bacterial parasites in rhesus macaques. Overall prevalence ranged from 2 to 5 %, with Shigella sp. being the most prevalent. Regression analyses linking anthropogenic factors to bacterial prevalence showed a positive association between rates of macaques eating human garbage and E. coli O157:H7 (ß = 0.23, p = 0.083), but a negative association with Salmonella sp. (ß = -0.17, p = 0.026). Rather, the prevalence of Salmonella sp. was positively linked to rates of macaque eating provisioned food (ß = 0.0012, p = 0.058). Finally, we found no relationship between anthropogenic factors and the prevalence of Shigella sp. Our findings establish the prevalence of enteric bacterial parasites in commensal populations of primates and suggest that although anthropogenic factors are linked to bacterial prevalence, the nature of the relationships may depend on the socioecological/foraging strategies of macaques and the food sources that facilitate the environmental survival of particular types of enteric bacteria over others.

Human-wildlife conflict: proximate predictors of aggression between humans and rhesus macaques in India.

Macaques live in close contact with humans across South and Southeast Asia, and direct interaction is frequent. Aggressive contact is a concern in many locations, particularly among populations of rhesus and longtail macaques that co-inhabit urbanized cities and towns with humans. We investigated the proximate factors influencing the occurrence of macaque aggression toward humans as well as human aggression toward macaques to determine the extent to which human behavior elicits macaque aggression and vice versa. We conducted a 3-month study of four free-ranging populations of rhesus macaques in Dehradun, India from October-December 2012, using event sampling to record all instances of human-macaque interaction (N = 3120). Our results show that while human aggression was predicted by the potential for economic losses or damage, macaque aggression was influenced by aggressive or intimidating behavior by humans as well as recent rates of conspecific aggression. Further, adult female macaques participated in aggression more frequently than expected, whereas adult and subadult males participated as frequently as expected. Our analyses demonstrate that neither human nor macaque aggression is unprovoked. Rather, both humans and macaques are responding to one another's behavior. Mitigation of human-primate conflict, and indeed other types of human-wildlife conflict in such coupled systems, will require a holistic investigation of the ways in which each participant is responding to, and consequently altering, the behavior of the other.

Hierarchical steepness, counter-aggression, and macaque social style scale.

Nonhuman primates show remarkable variation in several aspects of social structure. One way to characterize this variation in the genus Macaca is through the concept of social style, which is based on the observation that several social traits appear to covary with one another in a linear or at least continuous manner. In practice, macaques are more simply characterized as fitting a four-grade scale in which species range from extremely despotic (grade 1) to extremely tolerant (grade 4). Here, we examine the fit of three core measures of social style-two measures of dominance gradients (hierarchical steepness) and another closely related measure (counter-aggression)-to this scale, controlling for phylogenetic relationships. Although raw scores for both steepness and counter-aggression correlated with social scale in predicted directions, the distributions appeared to vary by measure. Counter-aggression appeared to vary dichotomously with scale, with grade 4 species being distinct from all other grades. Steepness measures appeared more continuous. Species in grades 1 and 4 were distinct from one another on all measures, but those in the intermediate grades varied inconsistently. This confirms previous indications that covariation is more readily observable when comparing species at the extreme ends of the scale than those in intermediate positions. When behavioral measures were mapped onto phylogenetic trees, independent contrasts showed no significant consistent directional changes at nodes below which there were evolutionary changes in scale. Further, contrasts were no greater at these nodes than at neutral nodes. This suggests that correlations with the scale can be attributed largely to species' phylogenetic relationships. This could be due in turn to a structural linkage of social traits based on adaptation to similar ecological conditions in the distant past, or simply to unlinked phylogenetic closeness.