Earthworms Coordinate Soil Biota to Improve Multiple Ecosystem Functions

Abstract

Earthworms have been perceived as benevolent soil engineers since the time of Charles Darwin, but several recent syntheses link earthworm activities to higher greenhouse gas emissions, less soil biodiversity, and inferior plant defense against pests. Our study provides new field-based evidence of the multiple direct and indirect impacts of earthworms on ecosystem functions within an ecological multifunctionality framework (i.e., aggregated measures of the ability of ecosystems to simultaneously provide multiple ecosystem functions). Data from a 13-year field experiment describing 21 ecosystem functions showed that earthworm presence generally enhanced multifunctionality by indirect rather than direct effects. Specifically, earthworms enhanced multifunctionality by shifting the functional composition toward a soil community favoring the bacterial energy channel and strengthening the biotic associations of soil microbial and microfaunal communities. However, earthworm-mediated changes in soil physical structure, pH, and taxonomic diversity were not related to multifunctionality. We conclude that the coordinated actions of earthworms and their associated soil biota were responsible for the maintenance of multifunctionality at high levels in this rice-wheat cropping system. Management of crop residue inputs and reduction of soil physicochemical disturbances should encourage beneficial earthworm effects and support multiple ecosystem services that are vital to sustainable agriculture.

Keywords: bacterial-dominated channel; earthworm; ecosystem engineer; ecosystem service; soil fauna; soil microbe; sustainable agriculture.