Parasite infection alters nitrogen cycling at the ecosystem scale

Despite growing evidence that parasites often alter nutrient flows through their hosts and can comprise a substantial amount of biomass in many systems, whether endemic parasites influence ecosystem nutrient cycling, and which nutrient pathways may be important, remains conjectural. A framework to evaluate how endemic parasites alter nutrient cycling across varied ecosystems requires an understanding of the following: (i) parasite effects on host nutrient excretion; (ii) ecosystem nutrient limitation; (iii) effects of parasite abundance, host density, host functional role and host excretion rate on nutrient flows; and (iv) how this infection-induced nutrient flux compares to other pools and fluxes. Pathogens that significantly increase the availability of a limiting nutrient within an ecosystem should produce a measurable ecosystem-scale response. Here, we combined field-derived estimates of trematode parasite infections in aquatic snails with measurements of snail excretion and tissue stoichiometry to show that parasites are capable of altering nutrient excretion in their intermediate host snails (dominant grazers). We integrated laboratory measurements of host nitrogen excretion with field-based estimates of infection in an ecosystem model and compared these fluxes to other pools and fluxes of nitrogen as measured in the field. Eighteen nitrogen-limited ponds were examined to determine whether infection had a measurable effect on ecosystem-scale nitrogen cycling. Because of their low nitrogen content and high demand for host carbon, parasites accelerated the rate at which infected hosts excreted nitrogen to the water column in a dose-response manner, thereby shifting nutrient stoichiometry and availability at the ecosystem scale. Infection-enhanced fluxes of dissolved inorganic nitrogen were similar to other commonly important environmental sources of bioavailable nitrogen to the system. Additional field measurements within nitrogen-limited ponds indicated that nitrogen flux rates from the periphyton to the water column in high-snail density/high-infection ponds were up to 50% higher than low-infection ponds. By altering host nutrient assimilation/excretion flexibility, parasites could play a widespread, but currently unrecognized, role in ecosystem nutrient cycling, especially when parasite and host abundances are high and hosts play a central role in ecosystem nutrient cycling.