At the edge of zoonotic spillover : land use, human-primate contact, and social networks in western Uganda

Forest loss related to human expansion of agricultural and urbanized landscapes is expected to increase in future decades. Fragmentation - or the changing mosaic of forested and non-forested lands - has cascading effects on landscape structure, species' ranges, ecological assemblages, and utilization of ecosystem services of these forests by species. Deforestation often occurs in areas with the highest biodiversity and abundance of large-bodied mammal populations. Landscape modification often occurs at the boundary between human and wild animal habitats; at the intersection of protected lands and economically vulnerable populations. The overlap of wild animals and people at the edges of tropical forests causes concern due to the risk of the spillover of zoonotic infections (i.e., pathogens transmitted from nonhuman animals to humans). Zoonotic diseases account for the majority of emerging infectious disease events in humans. Due to genetic similarities, infections from wild nonhuman primates pose particular risks to people. In particular, retroviral infections from wild nonhuman primates have lead to devastating epidemics, most notably human immunodeficiency virus. Previous research has linked retroviral spillover with repeated physical contact between people and nonhuman primates that often includes the sharing of bodily fluids. Recent work has pointed to increased habitat overlap between people and wild nonhuman primates and associated behavioral changes as a stimulus for cross-species infection exposure. Alongside the changes to nonhuman primate population sizes, geographic ranges, and behaviors created by land use change in tropical forests, certain human behaviors also have consequence in these environments. The creation of protected lands aims to quell biodiversity losses and create barriers between people and wild animals, but people living beside them are vulnerable to ecological, economic, and health consequences, such as the spillover of novel retroviruses. The coincidence of conservation and development objectives poses a challenge to resource managers, land use planners, and public health officials since many people sustain their livelihoods and native wild animal populations depend upon forests as well. Without interdisciplinary understanding of the ways in which land use change affects people's behaviors and how behaviors influence the risk of zoonotic exposure, we are unlikely to build adequate solutions that benefit people and the planet. To understand the fine-scale, human-environment interactions that shape how macroscopic changes influence microbiological transmission, this dissertation argues that we need to understand the context in which rare spillover events occur in order to prevent and adequately respond to the next emerging infectious disease epidemic. In this dissertation, I investigate: (1) the ways in which forest fragmentation and human behaviors contribute to human-nonhuman primate contact, (2) the demographic and behavioral characteristics that increase the likelihood for repeated and risky nonhuman primate contact, (3) blood samples for evidence of nonhuman primate retroviral spillover, and (4) features of relationships in rural communities that generate social structures that can influence disease transmission. Studying communities adjacent to the northwestern edge of Kibale National Park in western Uganda, this project brings together behavioral, spatial, serological, and relational data from surveys, remote sensing, diagnostic testing, and egocentric network techniques to better understand the conditions under which zoonotic spillover can occur. This work contributes to our understanding of how land use influences human-primate interactions, how human behavior affects the risk of pathogenic exposure, and assesses the potential for a single spillover event to transmit across sparsely populated areas near animal reservoirs of infection. In light of increased human mobility and continued encroachment on animal habitats, understanding the relationships between ecological, social, and epidemiological factors influencing opportunities for cross-species infection transmission is of substantial importance. The first chapter outlines the theory, the causal framework, and background for this case study. The second chapter focuses on understanding how forests affected by fragmentation influence behaviors leading to human-nonhuman primate contact. The third chapter focuses on understanding the characteristics of individuals who have repeated risky contact with nonhuman primates. The fourth chapter focuses on examining serological data for evidence of cross-species transmission of nonhuman primate retroviruses into a population where bushmeat hunting is not customary. The fifth chapter focuses on understanding the factors that induce social aggregation and thus opportunities for infection sharing in rural locations. In sum, this dissertation provides an interdisciplinary lens for examining the interactions between environmental and social systems that can result in infectious disease emergence

Advisor: Jones James Holland
Dirzo Rodolfo
Luby Stephen