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 (
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 (
- NSF-PAR ID:
- 10089225
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- American Journal of Primatology
- Volume:
- 81
- Issue:
- 4
- ISSN:
- 0275-2565
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract 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. -
more » « less
Abstract 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 andindirect 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.
-
A comparison of cell density and serotonergic innervation of the amygdala among four macaque speciesmore » « less
Abstract The genus
Macaca is an ideal model for investigating the biological basis of primate social behavior from an evolutionary perspective. A significant amount of behavioral diversity has been reported among the macaque species, but little is known about the neural substrates that support this variation. The present study compared neural cell density and serotonergic innervation of the amygdala among four macaque species using histological and immunohistochemical methods. The species examined included rhesus (Macaca mulatta) , Japanese (M. fuscata) , pigtailed (M. nemestrina) , and moor macaques (M. maura) . We anticipated that the more aggressive rhesus and Japanese macaques would have lower serotonergic innervation within the amygdala compared to the more affiliative pigtailed and moor macaques. In contrast to our prediction, pigtailed macaques had higher serotonergic innervation than Japanese and moor macaques in the basal and central amygdala nuclei when controlling for neuron density. Our analysis of neural cell populations revealed that Japanese macaques possess significantly higher neuron and glia densities relative to the other three species, however we observed no glia‐to‐neuron ratio differences among species. The results of this study revealed serotonergic innervation and cell density differences among closely related macaque species, which may play a role in modulating subtle differences in emotional processing and species‐typical social styles. -
Endogenous and exogenous cannabinoids signal through the cannabinoid 1 receptor (CB1R) to modulate various aspects of social behavior, including aggression and anxiety. In rodents and primates, CB1R expression in the basolateral amygdala is dense and cannabinoid signaling in this region has been reported to influence social behavior. Little is known about how endocannabinoid signaling in the amygdala contributes to primate social diversity. The behaviorally diverse and species-rich cercopithecoid monkey genus Macaca is an ideal model for addressing this topic. Japanese (Macaca fuscata) and rhesus macaques (M. mulatta) display similar social styles in some respects; however, there is evidence to suggest they differ in their stress response, amygdala structure, and monoaminergic signaling. To further assess the molecular basis of social style in Japanese and rhesus macaques, we used immunohistochemistry and stereological methods to compare CB1R-immunoreactive (CB1R-ir) axon density in the basolateral amygdala, which is comprised of the lateral, basal, and accessory basal nuclei. Our study sample included 6 Japanese and 5 rhesus macaques. Repeated-measures ANOVAs were used to evaluate species differences, with amygdala region as the within-subjects measure and species as the between-subjects factor. This revealed significant main effects for species and area (p values < 0.05) with no interaction. Post hoc tests revealed higher CB1R-ir axon density in the basal and accessory basal nuclei of rhesus macaques compared to Japanese macaques. Our results suggest that CB1R-mediated signaling in the lateral nucleus of the amygdala is comparable between the two species, while the differences we observed in the basal and accessory basal nuclei may contribute to the nuanced behavioral differences observed between them.more » « less
-
more » « less
Abstract Species in the genus
Macaca typically live in multimale‐multifemale social groups with male macaques exhibiting some of the largest testis: body weight ratios among primates. Males are believed to experience intense levels of sperm competition. Several spermatogenesis genes are located on the Y‐chromosome and, interestingly, occasional hybridization between two species has led to the introgression of the rhesus macaque (Macaca mulatta ) Y‐chromosome deep into the range of the long‐tailed macaque (M .fascicularis ). These observations have led to the prediction that the successful introgression of the rhesus Y‐haplotype is due to functional differences in spermatogenesis genes compared to those of the native long‐tailed Y‐haplotype. We examine here four Y‐chromosomal loci—RBMY ,XKRY , and two nearly identical copies ofCDY —and their corresponding protein sequences. The genes were surveyed in representative animals from north of, south of, and within the rhesus x long‐tailed introgression zone. Our results show a series of non‐synonymous amino acid substitutions present between the two Y‐haplotypes. Protein structure modeling via I‐TASSER revealed different folding patterns between the two species' Y‐proteins, and functional predictions via TreeSAAP further reveal physicochemical differences as a result of non‐synonymous substitutions. These differences inform our understanding of the evolution of primate Y‐proteins involved in spermatogenesis and, in turn, have biomedical implications for human male fertility.
