skip to main content


Title: Rates of human–macaque interactions affect grooming behavior among urban‐dwelling rhesus macaques ( Macaca mulatta )
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 adirectandindirectinfluence 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.

 
more » « less
NSF-PAR ID:
10078324
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
American Journal of Physical Anthropology
Volume:
168
Issue:
1
ISSN:
0002-9483
Page Range / eLocation ID:
p. 92-103
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    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 (Macacaspp.) 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
  2. Abstract

    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.

     
    more » « less
  3. Abstract Objectives

    The use of dental metrics in phylogenetic reconstructions of fossil primates assumes variation in tooth size is highly heritable. Quantitative genetic studies in humans and baboons have estimated high heritabilities for dental traits, providing a preliminary view of the variability of dental trait heritability in nonhuman primate species. To expand upon this view, the heritabilities and evolvabilities of linear dental dimensions are estimated in brown‐mantled tamarins (Saguinus fuscicollis) and rhesus macaques (Macaca mulatta).

    Materials and methods

    Quantitative genetic analyses were performed on linear dental dimensions collected from 302 brown‐mantled tamarins and 364 rhesus macaques. Heritabilities were estimated in SOLAR using pedigrees from each population, and evolvabilities were calculated manually.

    Results

    Tamarin heritability estimates range from 0.19 to 0.99, and 25 of 26 tamarin estimates are significantly different from zero. Macaque heritability estimates range from 0.08 to 1.00, and 25 out of 28 estimates are significantly different from zero.

    Discussion

    Dental dimensions are highly heritable in captive brown‐mantled tamarins and free‐ranging rhesus macaques. The range of heritability estimates in these populations is broadly similar to those of baboons and humans. Evolvability tends to increase with heritability, although evolvability is high relative to heritability in some dimensions. Estimating evolvability helps to contextualize differences in heritability, and the observed relationship between evolvability and heritability in dental dimensions requires further investigation.

     
    more » « less
  4.  
    more » « less
  5. Abstract

    The genusMacacais 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.

     
    more » « less