Earthworm and belowground competition effects on plant productivity in a plant diversity gradient

Diversity is one major factor driving plant productivity in temperate grasslands. Although decomposers like earthworms are known to affect plant productivity, interacting effects of plant diversity and earthworms on plant productivity have been neglected in field studies. We investigated in the field the effects of earthworms on plant productivity, their interaction with plant species and functional group richness, and their effects on belowground plant competition. In the framework of the Jena Experiment we determined plant community productivity (in 2004 and 2007) and performance of two phytometer plant species [Centaurea jacea (herb) and Lolium perenne (grass); in 2007 and 2008] in a plant species (from one to 16) and functional group richness gradient (from one to four). We sampled earthworm subplots and subplots with decreased earthworm density and reduced aboveground competition of phytometer plants by removing the shoot biomass of the resident plant community. Earthworms increased total plant community productivity (+11%), legume shoot biomass (+35%) and shoot biomass of the phytometer C. jacea (+21%). Further, phytometer performance decreased, i.e. belowground competition increased, with increasing plant species and functional group richness. Although single plant functional groups benefited from higher earthworm numbers, the effects did not vary with plant species and functional group richness. The present study indicates that earthworms indeed affect the productivity of semi-natural grasslands irrespective of the diversity of the plant community. Belowground competition increased with increasing plant species diversity. However, belowground competition was modified by earthworms as reflected by increased productivity of the phytometer C. jacea. Moreover, particularly legumes benefited from earthworm presence. Considering also previous studies, we suggest that earthworms and legumes form a loose mutualistic relationship affecting essential ecosystem functions in temperate grasslands, in particular decomposition and plant productivity. Further, earthworms likely alter competitive interactions among plants and the structure of plant communities by beneficially affecting certain plant functional groups

Animal Ecosystem Engineers Modulate the Diversity-Invasibility Relationship

Invasions of natural communities by non-indigenous species are currently rated as one of the most important global-scale threats to biodiversity. Biodiversity itself is known to reduce invasions and increase stability. Disturbances by ecosystem engineers affect the distribution, establishment, and abundance of species but this has been ignored in studies on diversity-invasibility relationships.We determined natural plant invasion into 46 plots varying in the number of plant species (1, 4, and 16) and plant functional groups (1, 2, 3, and 4) for three years beginning two years after the establishment of the Jena Experiment. We sampled subplots where earthworms were artificially added and others where earthworm abundance was reduced. We also performed a seed-dummy experiment to investigate the role of earthworms as secondary seed dispersers along a plant diversity gradient. Horizontal dispersal and burial of seed dummies were significantly reduced in subplots where earthworms were reduced in abundance. Seed dispersal by earthworms decreased with increasing plant species richness and presence of grasses but increased in presence of small herbs. These results suggest that dense vegetation inhibits the surface activity of earthworms. Further, there was a positive relationship between the number of earthworms and the number and diversity of invasive plants. Hence, earthworms decreased the stability of grassland communities against plant invasion.Invasibility decreased and stability increased with increasing plant diversity and, most remarkably, earthworms modulated the diversity-invasibility relationship. While the impacts of earthworms were unimportant in low diverse (low earthworm densities) and high diverse (high floral structural complexity) plant communities, earthworms decreased the stability of intermediate diverse plant communities against plant invasion. Overall, the results document that fundamental processes in plant communities like plant seed burial and invader establishment are modulated by soil fauna calling for closer cooperation between soil animal and plant ecologists

Plant Diversity Surpasses Plant Functional Groups and Plant Productivity as Driver of Soil Biota in the Long Term

One of the most significant consequences of contemporary global change is the rapid decline of biodiversity in many ecosystems. Knowledge of the consequences of biodiversity loss in terrestrial ecosystems is largely restricted to single ecosystem functions. Impacts of key plant functional groups on soil biota are considered to be more important than those of plant diversity; however, current knowledge mainly relies on short-term experiments.We studied changes in the impacts of plant diversity and presence of key functional groups on soil biota by investigating the performance of soil microorganisms and soil fauna two, four and six years after the establishment of model grasslands. The results indicate that temporal changes of plant community effects depend on the trophic affiliation of soil animals: plant diversity effects on decomposers only occurred after six years, changed little in herbivores, but occurred in predators after two years. The results suggest that plant diversity, in terms of species and functional group richness, is the most important plant community property affecting soil biota, exceeding the relevance of plant above- and belowground productivity and the presence of key plant functional groups, i.e. grasses and legumes, with the relevance of the latter decreasing in time.Plant diversity effects on biota are not only due to the presence of key plant functional groups or plant productivity highlighting the importance of diverse and high-quality plant derived resources, and supporting the validity of the singular hypothesis for soil biota. Our results demonstrate that in the long term plant diversity essentially drives the performance of soil biota questioning the paradigm that belowground communities are not affected by plant diversity and reinforcing the importance of biodiversity for ecosystem functioning

Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment

Biodiversity is rapidly declining1, and this may negatively affect ecosystem processes, including economically important ecosystem services. Previous studies have shown that biodiversity has positive effects on organisms and processes4 across trophic levels. However, only a few studies have so far incorporated an explicit food-web perspective. In an eight-year biodiversity experiment, we studied an unprecedented range of above- and below-ground organisms and multitrophic interactions. A multitrophic data set originating from a single long-term experiment allows mechanistic insights that would not be gained from meta-analysis of different experiments. Here we show that plant diversity effects dampen with increasing trophic level and degree of omnivory. This was true both for abundance and species richness of organisms. Furthermore, we present comprehensive above-ground/below-ground biodiversity food webs. Both above ground and below ground, herbivores responded more strongly to changes in plant diversity than did carnivores or omnivores. Density and richness of carnivorous taxa was independent of vegetation structure. Below-ground responses to plant diversity were consistently weaker than above-ground responses. Responses to increasing plant diversity were generally positive, but were negative for biological invasion, pathogen infestation and hyperparasitism. Our results suggest that plant diversity has strong bottom-up effects on multitrophic interaction networks, with particularly strong effects on lower trophic levels. Effects on higher trophic levels are indirectly mediated through bottom-up trophic cascades

Diversity Promotes Temporal Stability across Levels of Ecosystem Organization in Experimental Grasslands

The diversity–stability hypothesis states that current losses of biodiversity can impair the ability of an ecosystem to dampen the effect of environmental perturbations on its functioning. Using data from a long-term and comprehensive biodiversity experiment, we quantified the temporal stability of 42 variables characterizing twelve ecological functions in managed grassland plots varying in plant species richness. We demonstrate that diversity increases stability i) across trophic levels (producer, consumer), ii) at both the system (community, ecosystem) and the component levels (population, functional group, phylogenetic clade), and iii) primarily for aboveground rather than belowground processes. Temporal synchronization across studied variables was mostly unaffected with increasing species richness. This study provides the strongest empirical support so far that diversity promotes stability across different ecological functions and levels of ecosystem organization in grasslands

A comparison of the strength of biodiversity effects across multiple functions

In order to predict which ecosystem functions are most at risk from biodiversity loss, meta-analyses have generalised results from biodiversity experiments over different sites and ecosystem types. In contrast, comparing the strength of biodiversity effects across a large number of ecosystem processes measured in a single experiment permits more direct comparisons. Here, we present an analysis of 418 separate measures of 38 ecosystem processes. Overall, 45% of processes were significantly affected by plant species richness, suggesting that, while diversity affects a large number of processes not all respond to biodiversity. We therefore compared the strength of plant diversity effects between different categories of ecosystem processes, grouping processes according to the year of measurement, their biogeochemical cycle, trophic level and compartment (above- or belowground) and according to whether they were measures of biodiversity or other ecosystem processes, biotic or abiotic and static or dynamic. Overall, and for several individual processes, we found that biodiversity effects became stronger over time. Measures of the carbon cycle were also affected more strongly by plant species richness than were the measures associated with the nitrogen cycle. Further, we found greater plant species richness effects on measures of biodiversity than on other processes. The differential effects of plant diversity on the various types of ecosystem processes indicate that future research and political effort should shift from a general debate about whether biodiversity loss impairs ecosystem functions to focussing on the specific functions of interest and ways to preserve them individually or in combinatio

Collembola in a plant diversity gradient: Interactions between the aboveground and belowground system

During the past few decades, there has been growing understanding that human well-being is fundamentally linked to the state of the environment. The rapid decline of global biodiversity and its consequences for ecosystem functioning therefore has become a focal point of scientific interest and prompted a multitude of biodiversity studies aiming to investigate the complex relationship between plant species richness and ecosystem functioning in terrestrial grassland ecosystems. However, the majority of these studies predominantly focused on the aboveground aspects of terrestrial ecosystems such as plant productivity, neglecting the role of the belowground decomposer community as an important driver of fundamental ecosystem processes. Soil microorganisms and decomposer animals control decomposition processes and nutrient mineralization in soil, processes that are key determinants for plant performance and ecosystem functioning. Collembola are among the most important microarthropods in terrestrial ecosystems as they are known to affect ecosystem processes and plant nutrition by a variety of direct and indirect mechanisms. The present thesis was conducted within the framework of the Jena Experiment, a large biodiversity experiment aiming to investigate the impacts of declining plant diversity on ecosystem processes and trophic interactions in grassland ecosystems. The overall objective of my thesis was to investigate the effects of plant species richness, plant functional group richness and particular plant functional groups on Collembola communities in temperate grassland and to explore the main mechanisms by which Collembola in turn affect plant communities. These questions were addressed in a field study and two greenhouse experiments. The intentions of the field study were to assess the effects of plant species richness, plant functional group richness and plant functional identity on the structure of Collembola communities in temperate grassland and if plant community effects on Collembola vary with season. Collembola density and diversity significantly increased with plant species and plant functional group richness, highlighting the importance of the singular hypothesis for soil invertebrates. Generally, grasses and legumes beneficially affected Collembola density and diversity, whereas effects of small herbs usually were detrimental. These impacts were largely consistent in spring and autumn. The results indicate a distinct time-lag of the response of Collembola to vegetation manipulations, suggesting that effects of plant functional group identity on the belowground system are more immediate whereas effects of plant species and plant functional group richness will become important in the long-term. The first greenhouse experiment investigated how plant productivity and decomposition processes are influenced by Collembola diversity and if effects of Collembola vary with plant functional group identity. Collembola decreased soil surface litter decomposition whereas root litter decomposition was enhanced. Furthermore, Collembola diversity changed root depth distribution in a plant functional group specific way, indicating distinct changes in plant competition due to changes in Collembola diversity and composition. However, effects of Collembola on plant performance appeared to be idiosyncratic and point to strong context-dependent interactions among Collembola species, such as facilitation or competition for nutrients and living space. The results therefore suggest that changes in Collembola diversity may have unpredictable consequences for ecosystem functioning. The aim of the second greenhouse experiment was to investigate effects of Collembola and arbuscular-mycorrhizal fungi (AMF) on plant competition and the performance of Lolium perenne, Plantago lanceolata and Trifolium pratense representing three dominant plant functional groups (grasses, herbs and legumes). Further, we investigated variations in Collembola performance and AMF colonization rates of plant roots as influenced by the different plant communities. Collembola did not affect total colonization of roots by AMF but increased the number of mycorrhizal vesicles in P. lanceolata. AMF and Collembola both enhanced the amount of N and P in plant shoot tissue, but impacts of Collembola were less pronounced in the presence of AMF. Overall, the results suggest that AMF and Collembola interact in affecting plant competition. Presence of AMF modulated plant specific effects on Collembola and increased the competitiveness of P. lanceolata and T. pratense against L. perenne, pointing to a loose inter-kingdom mutualistic relationship between plant, mycorrhiza and Collembola. The results demonstrate that Collembola and AMF interactively impact the competition between plant species by differentially but concordantly affecting nutrient acquisition of the plant. The insights of the present thesis corroborate the importance of the belowground community for ecosystem functioning and human well-being by highlighting the interactions within the different levels of soil biota

Interacting effects of plant diversity and earthworms.

<p>Effects of plant species richness (1, 4, and 16-species mixtures) and earthworm treatment (earthworm reduction [-ew] and earthworm addition [+ew]) on the coefficient of variation (CV; [%]) of (A) the number and (B) biomass of herb invaders in the years 2004 to 2006 and effects of plant functional group richness (1, 2, 3, and 4 plant functional groups) and earthworm treatment on the CV [%] on (C) the number and (B) biomass of herb invaders in the years 2004 to 2006. Means with standard errors.</p

Experimental setup and earthworm midden.

<p>(A) Photograph of the field site of the Jena Experiment taken in 2004 showing the main experimental plots (20×20 m) varying in plant species richness (1, 2, 4, 8, 16, and 60) and plant functional group richness (1, 2, 3, and 4) and the X- (horizontal axis; coordinates 0–4) and Y-coordinates (vertical axis; coordinates 0–6). Photo by J. Baade. (B) Photograph of one exemplary earthworm subplot (1×1 m), the enclosures for earthworm density manipulations (earthworm addition and earthworm reduction), and four octet devices used for earthworm extraction by electro-shocking. Photo by N. Eisenhauer. (C) Photograph of one exemplary <i>Lumbricus terrestris</i> midden with three invader seedlings on the field site of the Jena Experiment. Photo by N. Eisenhauer.</p

Diversity–stability relationships for the twelve ecological functions grouped by levels of organization.

<p>Each dot represents the mean of temporal stability values (vertical axes) obtained across experimental plots sowed with the same number of plant species (1, 2, 4, 8, 16 or 60 species). Error bars represent the 95% confidence interval around the mean. Each temporal stability measure was standardized with a mean of zero and variance of one to ease the comparison of diversity–stability relationships within and between organizational levels. The left panels (A–D) show the relationships between plant species richness and the variance CV, while the right panels (E–H) show the relationships to the co-variance CV. No measurements were available for species richness treatments 2 and 8 in Earthworm Biomass, Parasitic Hymenoptera, Below- and Aboveground Invertebrates, and Arthropod Diversity production functions. For each component of temporal stability we report Pearson's correlation coefficient r estimated by a linear fit between the logarithm of plant species richness and one component of temporal stability. The number of stars next to Pearson's r values gives the probability of accepting the null hypothesis following a distribution-free randomization test <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0013382#pone.0013382-Legendre1" target="_blank">[37]</a> (df are in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0013382#pone-0013382-t001" target="_blank">Table 1</a>): Blank (p>0.05), *(p<0.05), **(p<0.01), ***(p<0.001).</p