Interactions Between Digenean Trematodes and Human Land Use, Nutrient Cycling, and Climate in Colorado

John Anthony Mischler, University of Colorado at Boulder

Abstract

Human actions have changed the face of the planet and have modified how ecosystems develop and function. These changes affect multiple aspects of ecosystems which can in turn have deleterious effects on human well-being. Human-caused change has led to the collapse of fisheries, massive erosion of soils, loss of fertility, increased disease risk from complex life cycle parasites, and the endangerment of clean drinking water (among others). Specifically, anthropogenic activities have fundamentally changed how carbon (C), nitrogen (N), and phosphorus (P) cycle through and among ecosystems, both locally and globally. Altering the fluxes and pools of these elements, fundamental to all life on Earth, produces cascading effects that completely alter species interactions within ecosystems. In this thesis I used a series of vernal ponds on the eastern plains of Colorado to investigate interactions between nutrient cycling and parasites. First I demonstrated the likely N limitation of these ponds using both lab-based nutrient addition bioassays as well as field-based stoichiometric inference over the better part of a growing season. Both approaches yielded results consistent with widespread N limitation in these ponds. N limitation likely arises due to large inflows of anthropogenic P (manure, sewage, fertilizer) without correspondingly large N inflows, coupled with intrinsically low water column N fixation rates. Now, with the establishment of N limitation in these ponds, I determined the manner and degree of interaction between parasitic infection and nutrient cycling. The digenean trematode parasite Cotylurus abelliformis commonly infects aquatic snails in these ponds and can reach high prevalences and abundances. Lab-based excretion trials using field-caught snails indicated that infection led to increased N fluxes from snail hosts via excretion. This N came both from the snails themselves (lower snail N content due to infection) as well as the periphyton (lower periphyton N content in higher infection ponds). This infection-induced N excretion increased the flux of N from organic-bound reservoirs to the water column (where it is available to the rest of the ecosystem). Using a basic empirical modeling approach, I determined that this infection-induced N flux was on par with water column N fixation in these systems, with the potential to be much larger with depending on infection prevalences/abundances and snail densities. The N limited conditions present in these ponds due to anthropogenic P loading allow for parasite-mediated N to be significant at the ecosystem level. Anthropogenic change may also affect the prevalence and abundance of trematode parasites directly. Changes in molluscan-trematode communities were evaluated in freshwater habitats close to Crested Butte, CO over the last 50+ years. The first survey of snail infection was conducted over the summers of 1957, 1958, and 1959. I revisited two of these sites during the summers of 2011 and 2012 to evaluate the effects of environmental change on molluscan-trematode communities at two sites: Lake Grant (high disturbance) and the Kettles (low disturbance). Human disturbance led to changes in snail communities in Lake Grant, which decreased the resilience of parasite communities to year-to-year fluctuations in mean weather conditions. Conversely, an increase in snail biodiversity at the Kettles, possibly facilitated by cattle-derived nutrients or warmer springs, led to enhanced stability in trematode communities. Additionally, exceptionally high schistosome diversity was uncovered at this site, a first for high elevation ponds. Therefore, interaction between anthropogenic activities and infection can alter the role of parasites in ecosystems through both direct changes in prevalence and abundance as well as cascading effects involving nutrient cycling and species interactions.