Parasitic infection by Cotylurus flabelliformis alters aquatic nitrogen cycling at the ecosystem scale

Background/Question/Methods

The potential effects of altered nitrogen (N) and phosphorus (P) cycles on parasitic infection has received considerable attention. However, parasitic infection itself alters host metabolism in ways that may, in turn, affect the availability of key nutrients at the ecosystem scale. Here, we explored this potential in a series of 20 ponds in northeastern Colorado in which prevalence of the trematode parasite Cotylurus flabelliformis varies. These ponds, as with neighboring water bodies, display multiple indicators of nitrogen (N) limitation, as well as pond-to-pond variance in the N and P cycles. We assessed whether parasitic infection of Stagnicola elodes snails could contribute to such biogeochemical variation. All 20 ponds were surveyed for water chemistry and Cotylurus flabelliformis infection in August 2010 and 19 of these 20 ponds were resurveyed during the summer of 2011 for water chemistry, infection, and periphyton nutrients. In August 2012, 115 snails were collected from a single pond and sealed individually into centrifuge tubes for a 3 hour excretion experiment. Following the experiment, water and snail feces were collected from the centrifuge tubes for nutrient analyses. Snails were dissected to determine infection intensity and snail feet were collected for nutrient analyses.

Results/Conclusions

The number of metacercariae per snail in the excretion experiment ranged from 0 to 450. Data were pooled into high infection (300 to 450 metacercariae, N=23) and low infection (0 to 150 metacercariae, N=60) groups. While no significant effects on P cycling were found, highly infected snails excreted significantly less carbon (C) (p<0.05) and significantly more nitrogen (p<0.05) than their less infected counterparts, probably as a result of the use of protein catabolism to support infection. Highly infected snails had significantly less body nitrogen (p<0.05) than the low infection group. Parasite-mediated excretion rates led to decreases in the TDOC:TDN ratio (p<0.05, R²=0.43) and the accumulation of TDN (p<0.05, R²=0.17) in the water column of high infection ponds in the field. Additionally, periphyton nitrogen content was lower in ponds with high infection rates, presumably due to snail-mediated increases in the rate of nitrogen cycling to the water column. We show that parasitic infection can exert a top-down control (similar to predation) on the cycling and availability of a potentially limiting nutrient at an ecosystem scale. Our results demonstrate the importance of going beyond simple correlational assays of biogeochemistry and disease dynamics to understand the underlying mechanisms and chain of cause-and-effect.