Direct and indirect effects of herbivores on nitrogen dynamics: voles in riparian areas

Herbivores can directly increase nitrogen mobility by increasing the quality of organic matter entering the decomposition cycle, but they also may decrease nitrogen mobility by decreasing the biomass of high-nitrogen species in the plant community. We assessed effects of voles (Microtus) on nitrogen dynamics using exclosures in two riparian meadows (Crystal Bench and Blacktail Deer Creek) in Yellowstone National Park (USA). At both sites, the quantity of plant litter was decreased by herbivory following a vole population peak in 1992. At Crystal Bench, removal of voles caused a decrease in the nitrogen concentration and an increase in the C:N ratio of plant litter over the four years of the study. The higher quality litter produced in the presence of voles at Crystal resulted in a larger pool of potentially mineralizable nitrogen in soil from control plots relative to soils from plots that had not been accessible to voles. At Crystal, vole removal did not cause a change in plant community composition. However, at Blacktail, after several years of vole exclusion, legumes became more common in exclosures than in control plots that were accessible to voles. Selective herbivory on high-nitrogen legumes kept the litter quality outside exclosures low, whereas higher legume biomass caused a decrease in C:N ratio of plant litter inside exclosures. The removal of voles at Blacktail caused a 15% increase in the fraction of the soil nitrogen that was rapidly mineralizable. Our results show that voles increased nitrogen mobility, especially during and after population peaks. However, that increase was offset by decreases in nitrogen mineralization over longer periods when voles caused a decrease in high-quality plant litter produced by preferred forage plants, especially legumes. Thus, both the mechanisms by which voles affected nitrogen dynamics and the net effects of voles varied over time and space. The balance of direct and indirect effects may provide a general mechanistic explanation of whether herbivores increase or decrease the rate of nitrogen cycling