Evaluating the Effect of Temperature on a Human Parasite and Its Intermediate Snail Host: Implications for a Changing Climate

Global climate change is impacting the emergence, re-emergence, prevalence, and incidence of infectious diseases worldwide, including parasitic diseases of humans (Blum and Hotez 2018). Neglected tropical diseases, defined as a group of parasitic diseases affecting developing countries in the tropics (Hotez et al. 2007), are of particular concern because these diseases occur in areas that are also expected to experience rapid population growth and agricultural development in the coming decades. As human population and food demand increase, the greater the likelihood of humans encountering intermediate hosts that either inhabit agricultural areas or are impacted by agricultural development, which will influence disease transmission (Rohr et al. 2019). Schistosomiasis, caused by trematodes of the genus Schistosoma, is one example. More than 200 million people are infected and nearly 800 million are at risk of contracting the disease worldwide (CDC 2019, WHO 2019). Most cases of schistosomiasis occur in sub-Saharan Africa (Gryseels et al. 2006, Hotez and Kamath 2009) and the life cycle circulates between humans and Biomphalaria spp., an intermediate snail host that inhabits freshwater habitats. Global climate change is expected to influence schistosomiasis, but predictions of future prevalence and incidence are highly variable and often have contradicting conclusions (Stensgaard et al. 2019). To improve model formulation and predictions, the response of the parasite and intermediate snail host to key climatic factors should be quantified. This doctoral dissertation aims to synthesize current work and address knowledge gaps on Biomphalaria spp. and Schistosoma mansoni, one of the major species causing human schistosomiasis. Specifically, the research presented here will examine the effect of temperature, an abiotic factor expected to fluctuate with global climate change, on life-history traits of the parasite and intermediate snail host. Because temperature will affect life-history traits differently, combining these data into mathematical models could help clarify and possibly improve predictions on whether global climate change will have net positive, net negative, or neutral changes on the prevalence and incidence of schistosomiasis. Chapter 1 introduces schistosomiasis, summarizes current studies that have examined the effect of temperature on this host-parasite system, and presents a modeling framework that could scale data from individual life-history traits to predict population-level host-parasite dynamics. In Chapter 2, a laboratory study was conducted to quantify hatching success and parasite emergence (from snails) of S. mansoni. We then combined these data to related life-history traits of S. mansoni and Biomphalaria spp. into a model to generate predictions of how R0, an estimate of the number of secondary cases given an infected individual, would change when temperature-dependent parameters were included (in the process of submitting for publication at PLoS Neglected Tropical Diseases). Chapter 3 examined the effect of temperature and viscosity on the movement of miracidia and cercariae, the two larval stages of S. mansoni (manuscript under review at International Journal of Parasitology). In Chapter 4, a four month mesocosm experiment was conducted to measure the effect of temperature on host-parasite disease dynamics at the population level across a temperature gradient. Measurements of snail egg production, population growth, parasite production, and total biomass were then compared to predictions of the same factors from a model where temperature-dependent rates of ingestion and mortality were included (manuscript in prep). There is a critical need to examine the effect of global climate change on infectious disease dynamics, and the work presented here provides insights into how temperature influences multiple life-history traits of parasites and intermediate hosts, and that these traits have downstream effects on host-parasite dynamics. Data from these experiments may be used to constrain future models, which will generate more biologically grounded predictions of disease spread. These data could also be used to produce more targeted management or intervention programs in regions where individuals are most at risk of contracting schistosomiasis or other parasitic diseases