The role of earthworms for plant performance and ecosystem functioning in a plant diversity gradient

The role of earthworms for plant performance and ecosystem functioning in a plant diversity gradient was investigated as part of the “Jena Biodiversity Experiment”. Concomitantly effects of the plant diversity on earthworms, springtails, microorganisms and decomposition were studied. Two greenhouse experiments and one field experiment were conducted. The first greenhouse experiment focused on the responses of three decomposer groups (earthworms, springtails and microorganisms) to manipulations in plant species diversity (1, 2, 4, 8), plant functional group diversity (1, 2, 3, 4) and functional group identity (grasses, legumes, small herbs, tall herbs) in a microcosm experiment. Also, the response of the plant community to the four decomposer treatments (control, earthworms, springtails and combined) was investigated. The use of 15N labelled litter allowed tracking of nutrient fluxes from dead organic matter into plants and animals. We hypothesised (1) that an increase in plant species and functional group diversity will beneficially affect earthworms and microorganisms, and accelerate decomposition processes, (2) that plant species and functional groups will differentially respond to earthworms and springtails in the rhizosphere. As hypothesised, earthworm performance (biomass and 15N incorporation) increased with increasing plant species and functional group diversity. Presence of legumes also beneficially affected earthworm performance. The mechanism of the beneficial effect of increasing plant species diversity differed between the earthworm functional groups. For anecic species (Lumbricus terrestris) the effect of plant diversity was mainly due to the presence of legumes; nitrogen rich legume litter being preferred by this species. The endogeic species also benefited from increased plant diversity, but via belowground effects of plant diversity based on rhizodeposits. Increasing plant species and functional group diversity also affected microorganisms in soil. Respiration rates decreased with increasing plant species and functional group diversity, but correlated with root biomass. Identity of plant functional groups was also important; legumes increased and grasses decreased microbial respiration. Microbial biomass, however, was little responsive to changes in plant diversity. Plant performance (biomass, N tissue concentration, 15N) was strongly affected by the decomposer treatments and plant diversity. Increasing plant species and plant functional group diversity increased total number and total weight of seeds. Shoot biomass increased with increasing plant species diversity and, even more pronounced, with plant functional group diversity. The increased shoot biomass with increasing plant species and functional group diversity remained significant when calculated without legume biomass. Increasing plant species diversity but not plant functional group diversity, decreased root biomass. Plant functional group diversity but not plant species diversity, increased total plant biomass. Plant functional group identity mattered; grasses benefited most from the presence of earthworms. Decomposers strongly increased shoot biomass, being at a maximum in the earthworm only treatment. Root biomass decreased in presence of collembolans, and even stronger in presence of earthworms; however, it increased when both animal groups were present. In treatments with decomposers, total N tissue concentration and 15N enrichment of three focal species was increased. In the second greenhouse experiment the effect of the anecic earthworm L. terrestris on plant seedling recruitment and aggregation was investigated by varying the number of plant functional groups (grass, legumes, herbs), seed size (small and large), plant species diversity (1, 3, 6) and plant functional group diversity (1, 3). L. terrestris strongly affected the recruitment of plant seedlings depending on seed size and plant functional group. Furthermore, earthworms increased microhabitat heterogeneity. Seed translocation, surface cast deposition and formation of burrows presumably act as intermediate disturbances favouring the formation of a more diverse plant community. In the field experiment similar hypothesis as in the first greenhouse experiment were investigated. Manipulations of the density of earthworms (reduced and increased) and springtails (reduced and natural) were established. In addition, decomposition of litter as affected by plant species (1, 4, 16) and functional group diversity (1, 2, 3), decomposers and litter functional group identity was investigated. Consistent with the microcosm experiment earthworm performance (biomass) was increased with increasing plant species diversity. Microbial respiration increased with increasing plant species diversity and was correlated with root biomass. Soil texture and presence of legumes but not plant diversity affected the community composition of earthworms. Decomposition of litter was primarily affected by local abiotic conditions (block effects) and less by the plant diversity gradient. As expected, litter decomposition was strongly affected by the identity of plant functional groups; legume litter decomposed faster than grass and herb litter. Earthworms and increasing plant functional group diversity increased the decomposition of legume litter. The increase in earthworm density with increasing plant diversity accelerated the decomposition and mineralization of nitrogen rich organic matter; therefore, earthworms may have contributed to higher plant productivity in particular in treatments with high plant species and functional group diversity. The effects of earthworms on plant performance were more distinct in the greenhouse experiments than in the field. After two years from the establishment of the plant communities in the field we did not find significant effects of earthworms on plant performance (biomass) or plant community composition (plant species diversity or cover). Overall, the results document that there is a strong interdependence between plant diversity and the functioning of the decomposers and vice versa. The results suggest that increasing plant diversity has beneficial effects on decomposer performance. Legumes represent a key plant functional group that strongly affects the decomposition processes at least in part via beneficial effects on soil decomposer invertebrates, such as earthworms. The results also show that plant performance is beneficially affected by decomposers and that some decomposers, such as anecic earthworms, are promoting plant diversity.