Primate Infectious Disease Ecology: Insights and Future Directions at the Human-Macaque Interface

Abstract

Global population expansion has increased interactions and conflicts between humans and nonhuman primates over shared ecological space and resources. Such ecological overlap, along with our shared evolutionary histories, makes human-nonhuman primate interfaces hot spots for the acquisition and transmission of parasites. In this chapter, we bring to light the importance of human-macaque interfaces in particular as hot spots for infectious disease ecological and epidemiological assessments. We first outline the significance and broader objectives behind research related to the subfield of primate infectious disease ecology and epidemiology. We then reveal how members of the genus Macaca, being among the most socioecologically flexible and invasive of all primate taxa, live under varying degrees of overlap with humans in anthropogenic landscapes. Thus, human-macaque interfaces may favor the bidirectional exchange of parasites. We then review studies that have isolated various types of parasites at human-macaque interfaces, using information from the Global Mammal Parasite Database (GMPD: http://www.mammalparasites.org/). Finally, we elaborate on avenues through which the implementation of both novel conceptual frameworks (e.g., Coupled Systems, One Health) and quantitative network-based approaches (e.g., social and bipartite networks, agent-based modeling) may potentially address some of the critical gaps in our current knowledge of infectious disease ecology at human-primate interfaces.

Joint interactions with humans may pose a higher risk of zoonotic outbreaks than interactions with conspecifics among wildlife populations at human-wildlife interfaces

“…On the other hand, given the exploratory and increased risk-taking behavior of males resulting in their being more well-connected in co-interaction networks compared to females (Balasubramaniam et al 2020b(Balasubramaniam et al , 2021, we predicted that outbreak sizes through co-interaction networks would be higher when the first-infected individuals are males (versus females). Finally, we also explored whether the overall anthropogenic exposure of first-infected macaques, specifically their frequencies of interactions with humans, and time spent foraging on anthropogenic food, influenced zoonotic outbreak sizes through both network-types.…”

“…We observed 10 macaque groups representing three different species at human-primate interfaces across three locations in Asiafour groups of rhesus macaques in Shimla in Northern India (31.05 0 N, 77.1 0 E) between July 2016 and February 2018, four groups of long-tailed macaques in Kuala Lumpur in Malaysia (3.3 0 N, 101 0 E) between September 2016 and February 2018, and two groups of bonnet macaques in Thenmala in Southern India (8.90 0 N, 77.10 0 E) between July 2017 and May 2018 (Supplementary Figure 1). All macaque groups were observed in (peri)urban environments, and their home-ranges overlapped with humans and anthropogenic settlements -e.g., Hindu temples (Shimla and Kuala Lumpur), recreational parks (outskirts of Kuala Lumpur, Thenmala), roadside areas (Thenmala, Shimla)to varying extents (Balasubramaniam et al 2020b;Kaburu et al 2019;Marty et al 2019a). Subjects were adult male and female macaques which were pre-identified during a two-month preliminary phase prior to data collection at each location.…”

“…We also examined whether the magnitude of this effect was different across network-type for each host-species, and across hostspecies for each network-type. Rhesus and long-tailed macaques, compared to bonnet macaques, typically show greater ecological flexibility and overlap with anthropogenic environments (Balasubramaniam et al 2020b), as well as more nepotistic social systems characterized by greater tendencies for individuals to engage with specific subsets of group conspecifics than with others (Thierry 2007). Given these differences, across network-type for each host-species, we predicted that the co-interaction network centrality of first-infected macaques would have a stronger effect on outbreak sizes than grooming network centrality for rhesus macaques and long-tailed macaques, but that bonnet macaques would show the opposite effect.…”

“…48 ), others have more recently been exposed to anthropogenic factors through activities like tourism and habitat encroachment (e.g., chimpanzees, Pan troglodytes 49 ; mountain gorillas, Gorilla gorilla beringei 50 ). Unsurprisingly, human-primate interfaces are 'hotspots' for zoonosis and disease emergence 7,8,16,[51][52][53] meaning that these phenomena consistently and repeatedly occur in such places, and share many diseases with humans including malaria, measles, HIV/AIDS, Herpes B, and tuberculosis (reviewed in 8 ). For example, a recent study also revealed that all apes as well as African and Asian primates are vulnerable to infection from SARS-CoV-2 54 .…”

“…Influenced by both their evolutionary histories and their adaptive responses to socioecological 60,61 and anthropogenic factors 58 , macaques also show marked inter-and intra-specific variation in social behavior with their conspecifics and (consequently) social networks 12,58,61,62 . Many epidemiological studies have documented evidence of human-to-macaque disease transmission (and vice-versa), including vector-borne malaria parasites, respiratory viruses, and gastrointestinal enteric bacteria and protozoa (reviewed in 16,63 ). Yet there is little knowledge of the social-ecological pathways of zoonotic transmission at human-macaque, or indeed other human-primate, interfaces.…”