
Eco-Epidemiology of Emerging Pox Viruses in Africa

Concomitant with the waning of vaccine-based and naturally-occurring immunity to variola virus, monkeypox virus (MPXV) has become an emerging pathogen that has resulted in up to 10% human mortality among infected individuals in parts of forested Central and West Africa, with the highest number of human cases reported in theDemocratic Republic of the Congo (DRC). Outbreaks of the human disease in Africa have been associated with animal contact including hunting, butchering, and consuming monkeypox-infected mammals such as rodents or primates. Interestingly, human monkeypox cases have not been reported in eastern Africa (East of the Ruwenzori Mountains). Whether this is due to lower levels of human contact with small mammals or the absence of a suitable MPXV mammalian reservoir in this geographic location is unknown. To test the later possibility, I have begun a collaboration with Joanna Shisler (Microbiology) and the CDC Poxvirus Program to collect and test small mammal species for evidence of exposure to MPXV in Uganda, a country that borders the eastern side of the DRC that has no reported human monkeypox cases. These data will contribute to a better understanding of the natural distribution, maintenance, and mechanisms of spread of MPXV in Africa and to other continents as occurred in the United States in 2003 from a country in West Africa (Ghana), which also has no reported human monkeypox cases.

In 2004, Thomas Gillespie and Tony Goldberg founded the Kibale EcoHealth Project. The overall goal of this project is to determine how and why anthropogenic changes to tropical forests place people and non-human primates living in such ecosystems at increased risk of pathogen exchange. The central hypothesis of this work is that key human behaviors, primate behaviors, ecological conditions, and landscape features increase the risks of interspecific disease transmission. We focus our efforts on nine communities near Kibale National Park in western Uganda. These communities vary in the nature and degree to which they use associated forest fragments, allowing us to examine how specific alterations to primate habitats affect the dynamics of primate-human interaction and the risks of zoonotic disease transmission. This effort entails a combination of epidemiology, molecular ecology, behavioral ecology, social and clinical survey, and spatially explicit modeling. The ultimate product will be an implementable plan for protecting human and non-human primate health, while simultaneously ensuring the sustainability of the ecosystems within which they live.
Regional-Scale and Comparative Approaches for Understanding Linkages between Anthropogenic Disturbance and Primate Infection Dynamics.

There is growing recognition of the importance of land-use change andhuman-wildlife linkages in disease emergence and ecosystem health. My doctoral work included a series of investigations demonstrating that certain disturbance-related features of degraded forests are excellent predictors of infection rates in primates and of the prevalence of parasites shared between primates and humans in and around Kibale National Park in Uganda. In this five-year study, I compared patterns of gastrointestinal parasite infection and infection risk among metapopulations of multiple monkey species inhabiting undisturbed forest, selectively logged forest, and a series of forest fragments. My results demonstrated that forest fragmentation and selective logging increased prevalence and infection risk and that certain forest fragment attributes were strongly associated with infection patterns. These results suggest that on a local scale, infection dynamics of gastrointestinal pathogens are significantly affected by the degree and nature of anthropogenic disturbance to forests. Do these same relationships hold when we scale up to the regional level? I propose to examine the generality of this relationship through a multi-site comparison of undisturbed and disturbed forest across equatorial Africa. This project compares patterns of parasite infection and infection risk in free-ranging western lowland gorillas (Gorilla gorilla), mountain gorillas (Gorilla beringei) and chimpanzees (Pan troglodytes) in Congo, Gabon, Rwanda, Senegal, Tanzania, and Uganda. These multi-site collaborations allow us to determine the generality of patterns observed at Kibale, observe transmission dynamics along a continuum of disturbance intensity, and examine pathogen-disturbance dynamics at both local and regional scales.
Primate Behavioral Responses to Parasitism.

Competition and predation have long been considered the primary factors shaping the behavioral ecology and evolutionof primates. However, recent studies of diverse taxa imply that parasite-hostdynamics may provide important insights into complex aspects of behavior such as sociality, habitat use, groupformation,and mate choice. Our work has examined the behavioral patterns of red colobus monkeys at Kibale National Park, Uganda, in relation to concurrent infection status at the individual, group, and population levels. This research has uncovered interesting relationships among infection prevalence, infection risk, ranging behavior, multi-species associations, and intra-group interactions (i.e., inter-individual spacing, grooming behavior). These results suggest that parasitic diseases are a selective force that must be considered if we are to improve our understanding of the proximate mechanisms underlying primate behavior. One interesting aspect of this work has been an investigation of the role of self-medication as a behavioral response to infection. This research integrates behavioral, in-vitro, and clinical aspects; providing some of the strongest quantitative support for self-medication by animals to date.