Trophic ecology of earthworms: the relative role of litter- and root-derived resources investigated with compound-specific stable isotope analysis of amino acids
by Linlin Zhong
Date of Examination:2024-03-01
Date of issue:2024-07-23
Advisor:Dr. Melanie Maraun
Referee:Prof. Dr. Stefan Scheu
Referee:Prof. Dr. Christoph Bleidorn
Persistent Address:
http://dx.doi.org/10.53846/goediss-10410
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Abstract
English
Earthworms, known as ecosystem engineers, shape the structure and functioning of ecosystems by altering nutrient cycling, habitat architecture and plant growth due to feeding interactions or physiological activities. They play a central role in soil food webs due to their high biomass. However, despite their ecological importance, the trophic niches of earthworms to date remain controversial. This largely limits the reconstruction of soil food web topology and the understanding of belowground processes. Earthworms are typically assumed to be fuelled by brown energy, i.e., dead plant litter. However, there is growing evidence that root-derived resources as the ‘green’ energy channel in soil food webs are of significant importance. Using resource manipulation experiments, this dissertation investigated the role of root- and litter-derived resources of different quality to earthworm nutrition and how earthworms in turn affect the plant performance. Further, the effect of different cropping systems on the incorporation of root-derived C and mineral N by earthworms and centipedes was explored based on a labelling experiment. In addition, I tested if the variation of trophic niches of earthworms further propagates to higher trophic levels using centipedes as representatives of major macrofauna predators. Chapter two investigates the dietary contribution of root-derived resources of differing quality (grasses, legumes) to the nutrition of earthworms by combining bulk and compound-specific amino acid stable isotope analysis. The results suggest that root-derived resources contribute to earthworm nutrition primarily via the bacterial channel. Direct contribution of plants to earthworm nutrition averaged 30% and was enhanced by legume monoculture and mixed cultures. The results provide novel insights into interactions between plant roots and detritivore soil animals and shed light on the contribution of ‘green’ energy to the nutrition of soil macro-detritivores. This study also challenges the view that the fungal energy channel dominates in soil food webs. Chapter three tests the effects of earthworm species (epigeic, anecic and endogeic) on plant performance of differing functional groups in monoculture and mixture. Plant mixture promoted the growth of both legumes and grasses, likely via complementary nitrogen use and alleviated intraspecific competition. Additionally, grass fuelled the activity of soil microorganisms by root exudation, likely benefiting legume nitrogen fixation. Earthworm species differentially affected nitrogen uptake by grasses, with epigeic and endogeic species facilitating nitrogen uptake of grasses more than anecic species, especially in grass monocultures. While underlining the potential of legume-grass mixture in improving plant nitrogen uptake and productivity, the results also highlight the role of earthworms in altering and improving the uptake of nitrogen by grass from different pools in soil. These findings suggest that epigeic and endogeic earthworms may be able to improve performance of grass monocultures, with potential implications for future agricultural management strategies. Chapter four uncovers the dietary contribution of litter-derived resources of differing quality to earthworm species of different ecological groups (epigeic, anecic and endogeic) using bulk and compound-specific amino acid stable isotope analysis. Litter resources contributed to earthworm nutrition mainly via the bacterial channel, but that this varied with earthworm ecological groups. Direct contribution of plant-derived resources to earthworm nutrition averaged 30%, but higher litter quality shifted the channelling of resources from the bacterial to the plant energy channel, suggesting important functional shifts in soil food webs in response to higher litter quality. Chapter five explores the effects of cropping system (rape, grass, willow) on the incorporation of root-derived C and mineral N by earthworms (epigeic, anecic and endogeic) and centipedes based on a combination of 13C pulse-labelling of plants and 15N labelling of soil and using analyses of bulk stable isotopes and compound-specific stable isotopes of amino acids. Across all cropping systems, anecic and epigeic earthworms incorporated more root-derived C than endogeic earthworms, supporting the notion that endogeic earthworms mainly rely on older soil organic matter. Compared to willow, the grass and rape only allowed faster root-derived C flux to anecic earthworms and centipedes, while coupling between root-derived C and mineral N incorporation by all soil animals was stronger in grass and rape either due to the direct use of plant root-derived resources or of root-associated microorganisms. In willow, the use of plant root-derived resources also facilitated the coupling of root-derived C and mineral N assimilation by anecic earthworms. Supporting the ‘trophic whales’ notion, earthworms were not the intermediate link in transferring the root-derived C and mineral N to centipedes as higher trophic level predators. Rather, soil mesofauna collembolans appeared to be the main mediator in simultaneously conveying root-derived C and mineral N to centipedes. Together, this study demonstrates joint effects of cropping system and ecological group of soil animals in modulating the fluxes of root-derived C and mineral N to the soil food web. Overall, this dissertation highlights that soil decomposer animals play key functional roles in linking green and brown energy via multiple energy channels, and that plant-based resources of different quality/identity alter the coupling of these energy channels. In turn, soil decomposer animals also enhance the nutrient uptake by plants via different nitrogen pools in soil, and thus improve the performance of plant monocultures, suggesting potential implications for sustainable agricultural management strategies.
Keywords: Soil food web; resources availability; litter; root; earthworms; CSIA of amino acids
