Earthworms impact on soil organic matter mineralization sheds new light on their ecological groups 

Abstract

Earthworms contribute to numerous ecological functions by impacting the soil biogeochemistry. Through their bioturbation activity, they modify the soil structure and the distribution of its components. By ingesting soil and secreting mucus, earthworms bring microorganisms and organic matter into contact under conditions that favor microbial activity, thus stimulating the mineralization of carbon and nutrients by soil microorganisms. While these effects are relatively well known for the dominant agricultural species, the diversity of earthworm habitats and functional traits suggests that not all would have the same impact. Recently, Capowiez et al. (2024) proposed a classification of earthworms into functional groups (sensu Hedde et al. 2022) in relation to bioturbation (reorganization of soil particles). The aim of our work was to study the linkages between the organic matter mineralization and soil bioturbation functions performed by earthworms. We aimed to assess the different impacts on biogeochemical cycles of earthworm species belonging to different bioturbation functional groups. Six earthworm taxa were incubated in soil columns in the presence of alfalfa litter: Octodrilus complanatus (intense tunneler or anecic), Lumbricus terrestris and Aporrectodea caliginosa meridionalis (burrower or epi-anecic), Alollobophora chlorotica (shallow biotubator or epi-endogeic), Octolasion cyaneum (deep bioturbator or hypo-endogeic), Microscolex dubius (intermediate). After 6 weeks of incubation, the gallery networks were scanned, and pictures were analyzed. The columns were then opened, and soil samples were taken to quantify carbon and nitrogen mineralization, as well as the abundance and diversity of microorganisms in different soil compartments: casts (earthworms surface excrement), drilosphere (soil around the galleries) and surrounding bulk (soil not directly altered by earthworms). The results on earthworm bioturbation activity were consistent with those obtained by Capowiez et al. (2024) and made it possible to distinguish five functional groups (A. c. merdionalis and O. cyaneum being indistinguishable from each other). The presence of earthworms increased carbon and nitrogen content and stimulated mineralization in the casts but had low impact on the drilosphere. Biogeochemical and microbiological measurements tended to separate the taxa studied into two groups: species that stimulated carbon and nitrogen mineralization in the casts, by selecting bacteria (during passage through the digestive tract) and maintaining high humidity, and those that had little effect on microbial communities and their activity. Furthermore, the results showed that L. terrestris, often used as a "model" worm, had a higher impact on soil structure and on the mineralization of organic matter than most of the other taxa studied, and is therefore not representative of the role of earthworms in soils.