Examination of snail-digenean trematode interactions, and the relationship between snail diversity, host range and infection

Human activities are negatively impacting the Earth’s biodiversity. Cataloguing and protecting biodiversity is more important than ever. Unfortunately, parasites are often excluded from biodiversity surveys even though they play essential roles in their communities, such as regulating host populations, impacting predator-prey dynamics, and acting as a nutritional source for other organisms. Digenean trematode parasites are of particular interest because of the complex life cycles connecting them to two or more host taxa in their environments. Most trematodes parasitize a gastropod as the first intermediate host in their life cycle. The snail-trematode relationship is often considered more specific than the relationship between trematodes and their second intermediate or definitive hosts. Trematodes can be host generalists, infecting many different species of host, or host specialists, infecting a single or few host species, i.e., the host range. Trematode host range is shaped by filters such as host encounter and trematode-host compatibility. Increasing our knowledge of the impact of changes in diversity on trematode infections is critical. Previous research has studied the effect of increasing biodiversity on trematode diversity, based on the dilution effect hypothesis, where the prevalence of tick-borne bacteria in the white-footed mouse could be decreased by increasing non-competent host diversity in the area. When applying this hypothesis to trematodes, non-competent hosts “dilute” larval stages within the environment, decreasing transmission success. The opposite relationship has also been observed, where increasing host diversity increases trematode diversity, known as the diversity-begets-diversity hypothesis. When evaluating the impact of changes in diversity on trematodes, previous research often compares definitive host richness to trematode richness, with fewer studies comparing first intermediate host diversity to trematode richness. Increases in host diversity can increase, decrease, or have no effect on trematode diversity depending on the ecological context, e.g., host composition, host range of the trematode, and spatial scale. Using data on host-trematode relationships from central Alberta, we examined the effect of snail diversity on trematode infection prevalence of generalist trematodes, specialist trematodes, and overall infections. We undertook a longitudinal snail-trematode survey at reclaimed wetlands in central Alberta to investigate the relationship between snail host diversity and trematode infections, emphasizing differences between host-generalist and host-specialist trematodes. While previous studies have explored biodiversity-disease dynamics in controlled settings or through meta-analyses, this work uses large-scale, field-based data from reclaimed wetlands in Alberta. We also capitalized on a unique research opportunity in Michigan, USA, where a resident, focal, definitive host was being removed from lakes in an effort to control the avian schistosome cercariae that cause swimmer’s itch. Additionally, we compared traditional trematode sampling methods to novel, minimally invasive environmental sampling techniques. The overarching aim of my doctoral research was to further our understanding of the relationship between snail host diversity and trematode infections, with a focus on how these dynamics may differ between trematodes that are host-specialists or host-generalists. To accomplish this, we undertook three specific aims: (1) elucidate the life cycle and ecological impact of a novel avian schistosome species and assess how host removal affects the parasite community; (2) examine how snail communities influence trematode infection patterns in natural wetlands over time, including how wetland age and host specificity shape trematode richness and infection prevalence; and (3) compare traditional snail-based methods with environmental DNA and cercariometry for detecting trematode diversity. We observed 74 trematode species across four years and discovered nine provisionally-named trematode lineages. A positive relationship was uncovered between snail richness and both overall and generalist infection prevalence, suggesting that increasing first-intermediate host diversity increases generalist trematode infections. Additionally, we confirmed that environmental sampling techniques can reliably identify trematode species when compared to traditional sampling methods. The research presented herein offers new insights into the relationship between snail diversity and trematode infections, highlighting the importance of snails in trematode life cycles.

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