Root-derived resources fuel earthworms predominantly via bacterial and plant energy channels – Insights from bulk and compound-specific isotope analyses

Abstract

Soil food webs rely on both brown and green energy, i.e., litter material and root-derived resources such as exudates. Earthworms have traditionally been viewed as macro-detritivores fuelled by brown energy and playing a central role in nutrient cycling and belowground energy flux. However, the role of root-derived resources for earthworm nutrition remains controversial. We studied the dietary contribution of root-derived resources from different plant functional groups to earthworms using bulk and compound-specific stable isotope analyses in a microcosm experiment with five earthworm species, grasses and legumes in monoculture and mixture, and an unplanted control by preventing leaf litter from entering the microcosms. The presence of plants consistently depleted bulk 13C values of the five earthworm species studied suggesting that root-derived carbon contributed to earthworm nutrition in each of the species. The response of bulk 15N values was less consistent, which is in line with the assumption that root-derived resources fuel soil food webs mainly via carbon-based root exudates. These observations were corroborated by 13C values of essential amino acids suggesting that most of the tissue carbon of earthworms was incorporated via bacterial- (∼60%) and plant-derived resources (∼30%), with the presence of legumes enhancing the incorporation via plant-derived resources. The high proportion of bacterial resources in the earthworms was consistent with the relative dominance of bacteria in the experimental soil and suggests that bacteria serve as important link in the acquisition of food resources. However, it remains an open question whether earthworms feed directly on soil bacteria, bacterial residues in soil or rely on nutritional supplementation by gut microorganisms. Overall, our results show that when root-derived resources are available, earthworms, as macro-detritivores, also incorporate green energy, with these resources being assimilated mainly via the bacterial energy channel, pointing to the importance of bacterial energy channelling in ecosystems with high earthworm biomass.