Species identities, not functional groups, explain the effects of earthworms on litter carbon-derived soil respiration

Authors: CHANG, CHIH-HAN - Johns Hopkins University; SLAVECZ, KATALIN - Johns Hopkins University; Buyer, Jeffrey

Submitted to: Soil Biology and Biochemistry
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/6/2016
Publication Date: 6/17/2016
Publication URL: http://handle.nal.usda.gov/10113/62681
Citation: Chang, C., Slavecz, K., Buyer, J.S. 2016. Species identities, not functional groups, explain the effects of earthworms on litter carbon-derived soil respiration. Soil Biology and Biochemistry. 100:129-139.

Interpretive Summary: Earthworms play important roles in soil ecology, decomposing surface litter, moving organic matter from the surface down into the soil, digesting and decomposing soil organic matter, and creating tunnels that alter soil porosity. They are often divided into functional groups based on their feeding and burrowing behaviors, and it is assumed that all species within each functional group will have similar effects on soil organic matter. We found that certain earthworm species affected soil microbiological activity, the incorporation of surface litter into soil organic matter, and the abundance of soil bacteria and fungi. These effects varied according to the specific earthworm species rather than the earthworm functional group, highlighting the need to incorporate species information into studies on earthworms and soil organic matter. These results will be useful to soil ecologists and may lead to strategies for managing earthworms and other soil biota in improving sustainability of agroecosystems.

Technical Abstract: Soil respiration is frequently measured as a surrogate for biological activities and is important in soil carbon cycling. The heterotrophic component of soil respiration is primarily driven by microbial decomposition of leaf litter and soil organic matter, and is partially controlled by resource availability. In North American temperate deciduous forests, invasive European and Asian earthworms of different functional groups are known to variously affect soil properties and resource availability through their distinct feeding, burrowing, and casting behaviors, and may affect different components of soil respiration through modulating the microbial communities. By tracing litter-derived C from 13C and 15N double-enriched leaf litter into soil and CO2 efflux in a mesocosm experiment, we tested the hypothesis that earthworms of different functional groups inhibit different components of soil respiration by reducing resource availability to soil microbes, and further examined how species-specific effects of earthworms on soil respiration are mediated by soil microbial community. We showed that while earthworms generally had no effect on total soil respiration, interspecific interactions between Octolasion lacteum (endogeic) and Lumbricus rubellus (epi-endogeic) had significant negative effects, presumably through affecting anaerobic microsites in the soil. Moreover, litter C-derived soil respiration was reduced by the Asian Amynthas hilgendorfi (epi-endogeic), the European L. rubellus, and the North American native species Eisenoides lonnbergi (endogeic), but not by the European species O. lacteum. Phospholipid fatty acid (PLFA) analysis and structural equation modeling indicated that while soil bacteria and fungi abundance was affected by earthworm species identities, the observed reduction of litter C-derived soil respiration could not be attributed to changes in microbial biomass. Direct paths with strong negative effects between earthworms and litter C-derived soil respiration in the structural equation model indicated the presence of important processes that were not explicitly identified in the final model. We attributed these direct paths to earthworm-induced aggregate formation, reduction of microbial transformation of labile carbon, and antimicrobial peptide activities. We concluded that the mechanisms through which the four earthworm species affect the fate of litter-derived C and its mineralization are species-specific and cannot be reasonably predicted by the functional group identities or feeding behaviors of the involved species. This study highlighted the importance of explicitly incorporating species identity and species-specific ecology in studying C biogeochemistry in earthworm invaded soils.