Understanding Environmental and Anthropogenic Drivers of Lemur Health in Madagascar: The Importance of a One Health Perspective

Abstract

<p>Anthropogenic effects on ecosystems have expanded in their scope and intensity, with significant consequences for global environmental, wildlife and human health. As human encroachment into wildlife habitat grows, habitat degradation and fragmentation intensify, leading to increased contact among wildlife, humans and domestic animals. Due to this increasing frequency of interaction, and the emergence of several high-profile diseases, global concern has grown over the risk of emerging infectious disease from zoonotic origins. </p><p>Due to Madagascar's rampant rate of human population growth and deforestation, its incredible species diversity, the widespread presence of domestic and invasive species, and its evolutionary isolation, it can be viewed as a high risk region for potential disease emergence. There is a need for assessment of the zoonotic and reverse zoonotic disease potential within this country. </p><p>To contribute to this assessment, consistent baseline health monitoring provides an effective tool for evaluating wildlife health and preparing for future disease occurrences. Limited, disconnected surveys of lemur health have occurred, yet there remained a need for more extensive, country-wide evaluations that also addresses invasive species, domestic animal and human health, as well shifting patterns of environmental and climatic change. </p><p>This research has investigated the connections among human, animal (both domestic and wildlife) and ecosystem health in Madagascar. I have examined current trends in anthropogenically-driven environmental change in Madagascar--including deforestation, illegal logging of precious hardwoods, mining, hunting, and agriculture--and evaluated how this change affects patterns of lemur, domestic animal and human health by evaluating a suite of health measures and parasite prevalence and richness. I have also examined how predicted global climate changes may influence the spatial patterns of lemur parasites and human infectious disease by assessing their shifts in distributions and geographic extent. </p><p>To assess the risk of disease transmission among lemur, domestic animal and human hosts, I have modeled the areas of geographic overlap among these parasites and their hosts and identified high-risk areas for disease emergence using geospatial analysis. This information can help to develop predictive statistical and spatial tools, which can inform both environmental management and public health planning. </p><p>Through this work, I have evaluated the severe loss of distribution that rosewood species have undergone, which highly qualifies them for international trade protection. We predicted areas of high risk for future logging, many of which occurred within protected areas in the biodiverse northeast. </p><p>Secondly, I have compiled the most comprehensive record of parasites of lemurs to date. Building upon the Prosimian Biomedical Survey Project data and the published literature, we have recorded 88 parasites that have been documented in lemurs. These are composed of helminths, bacteria, ectoparasites and protozoa. Of the 23 focal parasite species studied more in depth in this study, we noted high variability in prevalence measures for unique parasites at different sites. Parasite coinfection occurred quite commonly, with up to as many as 7 parasites concurrently. On average, lemur parasites tend to be less species-, genus-, or family-specific than other parasites across all primates. </p><p>Thirdly, I documented highly significant differences in health measures from two populations of Indri that exist under differing levels of anthropogenic pressure. Of note, the parasite richness, leukocyte count and differential, and nickel and cobalt levels were significantly higher in the more exposed population, while the total protein measures were significantly lower. These data suggest that the exposed population experiencing more anthropogenic pressure suffered from elevated health and nutritional stress. </p><p>Fourthly, I have documented strong correlations among environmental drivers (temperature, precipitation and landscape-scale features) and lemur parasite distributions. Striking shifts in their distributions are predicted to occur with projected climate change in Madagascar, including an expansion of helminth, virus and ectoparasite distributions, but a contraction of bacteria distributions due to warming and drying in the south. </p><p>Fifthly, I have examined 10 human and domestic animal parasites that hold great consequence for lemur, human and domestic animal health in Madagascar. I have similarly demonstrated strong correlations among environmental drivers (temperature, precipitation and landscape-scale features) and the distributions of these human parasites. Shifts in the distributions are also predicted to occur with projected climate change, including an expansion of helminth parasites, and a contraction of viruses and bacteria due to warming and drying in the south. I have identified areas of high risk for the transmission of parasites from human hosts to lemurs, as well as conversely from lemur hosts to humans. These risk indices will serve to highlight geographic areas at particular risk, and will also help to direct limited funds and staff to those areas most in need of attention. </p><p>Sixthly, I have demonstrated a need to train a growing cadre of One Health professionals from many different disciplines. I have offered several suggestions to integrate One Health training into graduate education, and have identified several geographic regions of potential to be a Center of One Health Excellence, of which the North Carolina Triangle area is one of great promise.</p>