Indirect and direct effects of exotic earthworms on soil nutrient and carbon pools in North American temperate forests

Abstract

Earthworm invasions in North American temperate forests cause considerable changes to soil and litter horizons, which can lead to changes in soil biogeochemistry and plant communities. These ecosystem changes have complex causal relationships, and the cascades of indirect effects from earthworm burrowing and feeding may have larger net effects on soil biogeochemistry than direct effects. In this study we partitioned the effects of earthworms on particular soil nutrient and carbon pools into direct and indirect effects. We defined direct effects as consisting of the association between the soil nutrient or carbon pool and earthworm biomass, whilst indirect effects included the impacts earthworms have on these soil pools through changing litter layer depth and soil chemical and biotic factors. We quantified these direct and indirect effects using a path analysis approach applied to data collected from 24 plots across an earthworm gradient in a northern hardwood forest stand in Ontario, Canada. As potential predictors, we measured earthworm functional group biomass, litter depth, microbial biomass, soil pH, texture, and organic matter. We related these predictors to extractable nutrient and carbon concentrations, including nitrate/nitrite, ammonium, orthophosphate, and dissolved organic nitrogen, phosphorus, and carbon. We found few direct effects and primarily indirect effects of earthworms on the soil nutrient and carbon pools we measured. Endogeic earthworms had the strongest indirect effects via changes to pH, microbial biomass carbon, and proportion of soil organic matter. Anecic earthworms only indirectly affected soil and nutrient pools through changes in pH, and epigeic earthworms did not have either direct or indirect effects. Because endogeic earthworms had indirect effects through changing multiple soil factors, for some soil and nutrient pools these indirect effects augmented each other (primarily yielding negative effects), although in some cases indirect positive effects mitigated negative effects. Overall, the net effects of exotic earthworms on soil and nutrient pools were mostly negative. Of particular concern was the potential exacerbation by endogeic earthworms of phosphorus limitation in N-saturated forest systems, as well as carbon loss from mineral soils in addition to losses from the forest floor.