Earthworms in a plant diversity gradient : direct and indirect effects on plant competition and establishment

The human-caused rapid loss of biodiversity is one of the most dramatic aspects which has generated concern over the consequences for ecosystem functioning. During the last two decades understanding biodiversity-ecosystem process relationships have become a major focus in ecological research, however, the majority of biodiversity experiments in temperate grasslands focussed on a limited number of ecosystem processes, e.g. aboveground plant productivity. Above- and belowground components of ecosystems have traditionally been considered in isolation from one another ignoring the fundamental role of aboveground-belowground feedbacks in controlling ecosystem processes in understanding of biodiversity loss. Although the decomposer subsystem drives essential ecosystem processes, it has received only limited consideration in previous biodiversity-experiments. The soil fauna is known to govern nutrient cycling, organic matter turnover, and maintenance of soil physical structure, processes that are key determinants of primary production and ecosystem carbon storage. In many terrestrial ecosystems earthworms dominate the invertebrate biomass and are the most important decomposer group by structuring the whole belowground system and by directly and indirectly affecting the aboveground subsystem. The design of The Jena Experiment offers the unique opportunity to investigate the relationship between biodiversity and ecosystem processes while simultaneously manipulating trophic interactions. Thereby, it is possible for the first time to explore the consequences of human-induced diversity loss while considering interrelationships between plant communities and important animal ecosystem engineers. In the present thesis I performed two field experiments and four greenhouse experiments in order to extract the main direct and indirect interacting mechanisms between earthworms and grassland plant communities varying in diversity. The objectives of the first greenhouse experiment were to quantify the effects of earthworms on grass-legume competition in model grassland systems in order to improve the understanding of ecological mechanisms structuring grass-legume associations. We established model grassland systems in microcosms that were harvested twice to simulate the widespread biannual mowing regime in Central European grasslands. The presence of Lumbricus terrestris L. increased the productivity of grasses and legumes after 6 weeks but only that of grasses after another 10 weeks. Analyses of 15N/14N ratios indicate that, compared to legumes, grasses more efficiently exploit soil mineral N and benefit from legume presence through reduced “intra-functional group” competition. Earthworms appeared to modulate the competition between grasses and legumes by mobilizing soil N and thereby fostering the competitive strength of grasses. Moreover, earthworms were shown to affect the aboveground system and to function as essential driving agents of grass-legume associations by increasing grass yield, the amount of N in grass hay, the infestation rate of grasses with aphids, and potentially by reducing the attractiveness (number of flowerheads) of grass-legume associations to pollinators. The second greenhouse experiment investigated the effects of three apparently anecic earthworm species on wheat seed burial, seedling establishment, wheat growth, and litter incorporation. In contrast to Aporrectodea longa Ude, L. terrestris and Lumbricus rubellus friendoides Bouché reduced the litter layer considerably and buried more wheat seeds. The results show that anecic earthworm species differentially affect wheat seed burial, litter incorporation and wheat establishment. The effects of L. terrestris and L. rubellus friendoides were conform to the characteristics of anecic earthworm species whereas those of A. longa rather resemble endogeic species. The aim of the third greenhouse experiment was to investigate the impact of L. terrestris, plant functional group identity and seed size of plant invader species and plant functional group of the established plant community on the number and biomass of plant invaders. Earthworm performance was influenced by an interaction between plant functional group identity of the established plant community and that of invader species. Since earthworm effects on the number and biomass of invader plants varied with seed size and plant functional group identity they probably play a key role in seedling establishment and plant community composition. Seeds and germinating seedlings in earthworm burrows may significantly contribute to earthworm nutrition. The first field survey aimed to explore modifications of the invasibility and stability of grassland communities varying in plant species und functional group diversity by L. terrestris. We weeded experimental subplots differing in L. terrestris densities) by removing, counting and weighing non-target plant species. The results show that increasing diversity enhances the stability of the plant community which was primarily due to the higher probability of grass presence in the resident community. Earthworm performance likely is not affected by plant diversity per se but by the presence of certain plant functional groups (legumes and grasses). By successfully manipulating earthworm densities in the field the present study for the first time documents that earthworms in fact modulate seed dispersal and invader establishment. Moreover, plant species invasion and community stability are driven by a complex interaction between the diversity, functional identity, and structural complexity of plant communities and by belowground ecosystem engineers such as anecic earthworms. The fourth greenhouse experiment investigated direct and indirect impacts of endogeic earthworms on grassland plant seeds. Seed ingestion and digestion and germination in presence of earthworm excreta appeared to be plant and earthworm species-specific. Ingestion of seeds by earthworms likely strongly impacts plant seed survival and germination by stimulating germination of some species while digesting seeds from others. Selective ingestion and digestion of plant seeds by endogeic earthworm species presumably alter the composition of the soil seed bank and, consequently, plant community assembly. A second field survey investigated the efficiency of the electrical octet method and the mustard extraction method for sampling of different ecological groups of earthworms (anecics, endogeics and epigeics) under dry soil conditions. The mustard method was shown to be more efficient for the extraction of anecic earthworms, whereas the octet method was inappropriate in reflecting the actual earthworm community structure under dry soil conditions. The efficiency of both methods could not be improved by beforehand water addition. Moreover, the present study highlights the differing ecology of earthworm groups by showing that anecic earthworms, in contrast to endogeics, remain active during dry periods. Overall, the present thesis indicates that earthworm performance is unresponsive to manipulations of plant community diversity. Rather earthworms are affected by the presence of nutrient rich resources provided by legumes. Earthworm effects on the aboveground system appeared to be manifold playing a decisive role via four different fundamental ecosystem processes. First, (anecic) earthworms act as decomposers by increasing nutrient availability for plants and driving the competition between plants. Second, (anecic) earthworms are important ecosystem engineers by creating structures of increased nutrient availability (middens) functioning as small scale disturbances and regeneration niches for plant seedlings. Thereby, earthworms were shown to promote plant diversity. Third, (anecic) earthworms function as important seed dispersers by seed burial and ingestion and egestion of plant seeds. Seed burial might be an essential mechanism increasing the survival of seeds from certain plant species since L. terrestris was shown to stay active even during dry periods, e.g. in late summer during seed set. Fourth, earthworms directly affect plant community assembly by functioning as seed predators whereas seed predation is earthworm and plant species-specific. The present combined approach of above- and belowground systems emphasizes their intimate interrelationships demanding for the consideration of both systems when interpreting, estimating and modelling human-induced global change phenomena