Susanne Wurst

Choosing and using diversity indices: Insights for ecological applications from the German Biodiversity Exploratories

Biodiversity, a multidimensional property of natural systems, is difficult to quantify partly because of the multitude of indices proposed for this purpose. Indices aim to describe general properties of communities that allow us to compare different regions, taxa, and trophic levels. Therefore, they are of fundamental importance for environmental monitoring and conservation, although there is no consensus about which indices are more appropriate and informative. We tested several common diversity indices in a range of simple to complex statistical analyses in order to determine whether some were better suited for certain analyses than others. We used data collected around the focal plant Plantago lanceolata on 60 temperate grassland plots embedded in an agricultural landscape to explore relationships between the common diversity indices of species richness (S), Shannon’s diversity (H’), Simpson’s diversity (D1), Simpson’s dominance (D2), Simpson’s evenness (E), and Berger–Parker dominance (BP). We calculated each of these indices for herbaceous plants, arbuscular mycorrhizal fungi, aboveground arthropods, belowground insect larvae, and P. lanceolata molecular and chemical diversity. Including these trait-based measures of diversity allowed us to test whether or not they behaved similarly to the better studied species diversity. We used path analysis to determine whether compound indices detected more relationships between diversities of different organisms and traits than more basic indices. In the path models, more paths were significant when using H’, even though all models except that with E were equally reliable. This demonstrates that while common diversity indices may appear interchangeable in simple analyses, when considering complex interactions, the choice of index can profoundly alter the interpretation of results. Data mining in order to identify the index producing the most significant results should be avoided, but simultaneously considering analyses using multiple indices can provide greater insight into the interactions in a system.

Biodiversity at multiple trophic levels is needed for ecosystem multifunctionality

Many experiments have shown that loss of biodiversity reduces the capacity of ecosystems to provide the multiple services on which humans depend. However, experiments necessarily simplify the complexity of natural ecosystems and will normally control for other important drivers of ecosystem functioning, such as the environment or land use. In addition, existing studies typically focus on the diversity of single trophic groups, neglecting the fact that biodiversity loss occurs across many taxa and that the functional effects of any trophic group may depend on the abundance and diversity of others. Here we report analysis of the relationships between the species richness and abundance of nine trophic groups, including 4,600 above- and below-ground taxa, and 14 ecosystem services and functions and with their simultaneous provision (or multifunctionality) in 150 grasslands. We show that high species richness in multiple trophic groups (multitrophic richness) had stronger positive effects on ecosystem services than richness in any individual trophic group; this includes plant species richness, the most widely used measure of biodiversity. On average, three trophic groups influenced each ecosystem service, with each trophic group influencing at least one service. Multitrophic richness was particularly beneficial for ‘regulating’ and ‘cultural’ services, and for multifunctionality, whereas a change in the total abundance of species or biomass in multiple trophic groups (the multitrophic abundance) positively affected supporting services. Multitrophic richness and abundance drove ecosystem functioning as strongly as abiotic conditions and land-use intensity, extending previous experimental results to real-world ecosystems. Primary producers, herbivorous insects and microbial decomposers seem to be particularly important drivers of ecosystem functioning, as shown by the strong and frequent positive associations of their richness or abundance with multiple ecosystem services. Our results show that multitrophic richness and abundance support ecosystem functioning, and demonstrate that a focus on single groups has led to researchers to greatly underestimate the functional importance of biodiversity.

Priming and memory of stress responses in organisms lacking a nervous system.

Experience and memory of environmental stimuli that indicate future stress can prepare (prime) organismic stress responses even in species lacking a nervous system. The process through which such organisms prepare their phenotype for an improved response to future stress has been termed ‘priming’. However, other terms are also used for this phenomenon, especially when considering priming in different types of organisms and when referring to different stressors. Here we propose a conceptual framework for priming of stress responses in bacteria, fungi and plants which allows comparison of priming with other terms, e.g. adaptation, acclimation, induction, acquired resistance and cross protection. We address spatial and temporal aspects of priming and highlight current knowledge about the mechanisms necessary for information storage which range from epigenetic marks to the accumulation of (dormant) signalling molecules. Furthermore, we outline possible patterns of primed stress responses. Finally, we link the ability of organisms to become primed for stress responses (their ‘primability’) with evolutionary ecology aspects and discuss which properties of an organism and its environment may favour the evolution of priming of stress responses.

Effects of earthworms and organic litter distribution on plant performance and aphid reproduction

Human management practices and large detritivores such as earthworms incorporate plant litter into the soil, thereby forming a heterogeneous soil environment from which plant roots extract nutrients. In a greenhouse experiment we investigated effects of earthworms and spatial distribution of 15N-labelled grass litter on plants of different functional groups [Lolium perenne (grass), Plantago lanceolata (forb), Trifolium repens (legume)]. Earthworms enhanced shoot and root growth in L. perenne and P. lanceolata and N uptake from organic litter and soil in all plant species. Litter concentrated in a patch (compared with litter mixed homogeneously into the soil) increased shoot biomass and 15N uptake from the litter in L. perenne and enhanced root proliferation in P. lanceolata when earthworms were present. Growth of clover (T. repens) was rather independent of the presence of earthworms and organic litter distribution: nevertheless, clover took up more nitrogen in the presence of earthworms and exploited more 15N from the added litter than the other plant species. The magnitude of the effects of earthworms and organic litter distribution differed between the plant species, indicating different responses of plants with contrasting root morphology. Aphid (Myzus persicae) reproduction was reduced on P. lanceolata in the presence of earthworms. We suggest that earthworm activity may indirectly alter plant chemistry and hence defence mechanisms against herbivores.

Land-use intensification causes multitrophic homogenization of grassland communities.

Land-use intensification is a major driver of biodiversity loss. Alongside reductions in local species diversity, biotic homogenization at larger spatial scales is of great concern for conservation. Biotic homogenization means a decrease in β-diversity (the compositional dissimilarity between sites). Most studies have investigated losses in local (α)-diversity and neglected biodiversity loss at larger spatial scales. Studies addressing β-diversity have focused on single or a few organism groups (for example, ref. 4), and it is thus unknown whether land-use intensification homogenizes communities at different trophic levels, above- and belowground. Here we show that even moderate increases in local land-use intensity (LUI) cause biotic homogenization across microbial, plant and animal groups, both above- and belowground, and that this is largely independent of changes in α-diversity. We analysed a unique grassland biodiversity dataset, with abundances of more than 4,000 species belonging to 12 trophic groups. LUI, and, in particular, high mowing intensity, had consistent effects on β-diversity across groups, causing a homogenization of soil microbial, fungal pathogen, plant and arthropod communities. These effects were nonlinear and the strongest declines in β-diversity occurred in the transition from extensively managed to intermediate intensity grassland. LUI tended to reduce local α-diversity in aboveground groups, whereas the α-diversity increased in belowground groups. Correlations between the β-diversity of different groups, particularly between plants and their consumers, became weaker at high LUI. This suggests a loss of specialist species and is further evidence for biotic homogenization. The consistently negative effects of LUI on landscape-scale biodiversity underscore the high value of extensively managed grasslands for conserving multitrophic biodiversity and ecosystem service provision. Indeed, biotic homogenization rather than local diversity loss could prove to be the most substantial consequence of land-use intensification.

Do endogeic earthworms change plant competition? A microcosm study

Plants compete for limited resources. Although nutrient availability for plants is affected by resource distribution and soil organisms, surprisingly few studies investigate their combined effects on plant growth and competition. Effects of endogeic earthworms (Aporrectodea jassyensis), root-knot nematodes (Meloidogyne incognita) and the spatial distribution of 15N labelled grass litter on the competition between a grass (Lolium perenne), a forb (Plantago lanceolata) and a legume (Trifolium repens) were investigated in the greenhouse. Earthworms promoted N uptake and growth of L. perenne. Contrastingly, shoot biomass and N uptake of T. repens decreased in the presence of earthworms. P. lanceolata was not affected by the earthworms. We suggest that earthworms enhanced the competitive ability of L. perenne against T. repens. Nematodes increased the proportion of litter N in each of the plant species. Litter distribution (homogeneous vs. patch) did not affect the biomass of any plant species. However, P. lanceolata took up more 15N, when the litter was homogeneously mixed into the soil. The results suggest that endogeic earthworms may affect plant competition by promoting individual plant species. More studies including decomposers are necessary to understand their role in determining plant community structure.

Intraspecific Variation in Plant Defense Alters Effects of Root Herbivores on Leaf Chemistry and Aboveground Herbivore Damage

Root herbivores can indirectly affect aboveground herbivores by altering the food quality of the plant. However, it is largely unknown whether plant genotypes differ in their response to root herbivores, leading to variable defensive phenotypes. In this study, we investigated whether root-feeding insect larvae (Agriotes sp. larvae, wireworms) induce different responses in Plantago lanceolata plants from lines selected for low and high levels of iridoid glycosides (IG). In the absence of wireworms, plants of the “high-IG line” contained approximately twofold higher levels of total IG and threefold higher levels of catalpol (one of the IG) in leaves than plants from the “low-IG line,” whereas both lines had similar levels of IG in roots. In response to wireworms, roots of plants from both lines showed increased concentrations of catalpol. Leaves of “low-IG line” plants increased catalpol concentrations in response to wireworms, whereas catalpol concentrations of leaves of “high-IG line” plants decreased. In contrast, glucose concentrations in roots of “low-IG” plants decreased, while they increased in “high-IG” plants after feeding by wireworms. The leaf volatile profile differed between the lines, but was not affected by root herbivores. In the field, leaf damage by herbivores was higher in wireworm-induced compared to noninduced “low-IG” plants and lower in wireworm-induced compared to noninduced “high-IG” plants, despite induction of catalpol in leaves of the “low-IG” plants and reduction in “high-IG” plants. This pattern might arise if damage is caused mainly by specialist herbivores for which catalpol may act as feeding stimulant rather than as deterrent. The present study documents for the first time that intraspecific variation in plant defense affects the outcome of plant-mediated interactions between root and shoot herbivores.

Earthworms and Litter Distribution Affect Plant-Defensive Chemistry

Studies on plant-defensive chemistry have mainly focused on plants in direct interaction with aboveground and occasionally belowground herbivores and pathogens. Here we investigate whether decomposers and the spatial distribution of organic residues in soil affect plant-defensive chemistry. Litter concentrated in a patch (vs. homogeneously mixed into the soil) led to an increase in the aucubin content in shoots of Plantago lanceolata. Earthworms increased total phytosterol content of shoots, but only when the litter was mixed homogeneously into the soil. The phytosterol content increased and aphid reproduction decreased with increasing N concentration of the shoots. This study documents for the first time that earthworms and the spatial distribution of litter may change plant-defensive chemistry against herbivores.

Locally rare species influence grassland ecosystem multifunctionality

Species diversity promotes the delivery of multiple ecosystem functions (multifunctionality). However, the relative functional importance of rare and common species in driving the biodiversity–multifunctionality relationship remains unknown. We studied the relationship between the diversity of rare and common species (according to their local abundances and across nine different trophic groups), and multifunctionality indices derived from 14 ecosystem functions on 150 grasslands across a land-use intensity (LUI) gradient. The diversity of above- and below-ground rare species had opposite effects, with rare above-ground species being associated with high levels of multifunctionality, probably because their effects on different functions did not trade off against each other. Conversely, common species were only related to average, not high, levels of multifunctionality, and their functional effects declined with LUI. Apart from the community-level effects of diversity, we found significant positive associations between the abundance of individual species and multifunctionality in 6% of the species tested. Species-specific functional effects were best predicted by their response to LUI: species that declined in abundance with land use intensification were those associated with higher levels of multifunctionality. Our results highlight the importance of rare species for ecosystem multifunctionality and help guiding future conservation priorities.

Effects of belowground biota on primary and secondary metabolites in Brassica oleracea

Summary.Soil organisms in direct and indirect interaction with plant roots affect aboveground herbivores, likely by inducing different plant responses. We investigated the combined effects of the root-knot nematode Meloidogyne incognita (in direct interaction with roots) and the endogeic earthworm Octolasion tyrtaeum (in indirect interaction with roots) on the performance of Brassica oleracea. Both earthworms and nematodes increased N uptake and shoot biomass of B. oleracea. Earthworm activity mobilized more soil N than litter N, and herbivory by nematodes tended to increase the microbial biomass in soil. Only the structural class of sulphur containing glucosinolates was affected by the soil organisms. Earthworms decreased glucoiberin concentrations in B. oleracea shoots. Glucoraphanin was affected by an interaction between earthworms and nematodes.