Martin Schädler

Empirical and theoretical challenges in aboveground–belowground ecology

A growing body of evidence shows that aboveground and belowground communities and processes are intrinsically linked, and that feedbacks between these subsystems have important implications for community structure and ecosystem functioning. Almost all studies on this topic have been carried out from an empirical perspective and in specific ecological settings or contexts. Belowground interactions operate at different spatial and temporal scales. Due to the relatively low mobility and high survival of organisms in the soil, plants have longer lasting legacy effects belowground than aboveground. Our current challenge is to understand how aboveground–belowground biotic interactions operate across spatial and temporal scales, and how they depend on, as well as influence, the abiotic environment. Because empirical capacities are too limited to explore all possible combinations of interactions and environmental settings, we explore where and how they can be supported by theoretical approaches to develop testable predictions and to generalise empirical results. We review four key areas where a combined aboveground–belowground approach offers perspectives for enhancing ecological understanding, namely succession, agro-ecosystems, biological invasions and global change impacts on ecosystems. In plant succession, differences in scales between aboveground and belowground biota, as well as between species interactions and ecosystem processes, have important implications for the rate and direction of community change. Aboveground as well as belowground interactions either enhance or reduce rates of plant species replacement. Moreover, the outcomes of the interactions depend on abiotic conditions and plant life history characteristics, which may vary with successional position. We exemplify where translation of the current conceptual succession models into more predictive models can help targeting empirical studies and generalising their results. Then, we discuss how understanding succession may help to enhance managing arable crops, grasslands and invasive plants, as well as provide insights into the effects of global change on community re-organisation and ecosystem processes.

Tradeoffs associated with constitutive and induced plant resistance against herbivory

Several prominent hypotheses have been posed to explain the immense variability among plant species in defense against herbivores. A major concept in the evolutionary ecology of plant defenses is that tradeoffs of defense strategies are likely to generate and maintain species diversity. In particular, tradeoffs between constitutive and induced resistance and tradeoffs relating these strategies to growth and competitive ability have been predicted. We performed three independent experiments on 58 plant species from 15 different plant families to address these hypotheses in a phylogenetic framework. Because evolutionary tradeoffs may be altered by human-imposed artificial selection, we used 18 wild plant species and 40 cultivated garden-plant species. Across all 58 plant species, we demonstrate a tradeoff between constitutive and induced resistance, which was robust to accounting for phylogenetic history of the species. Moreover, the tradeoff was driven by wild species and was not evident for cultivated species. In addition, we demonstrate that more competitive species—but not fast growing ones—had lower constitutive but higher induced resistance. Thus, our multispecies experiments indicate that the competition–defense tradeoff holds for constitutive resistance and is complemented by a positive relationship of competitive ability with induced resistance. We conclude that the studied genetically determined tradeoffs are indeed likely to play an important role in shaping the high diversity observed among plant species in resistance against herbivores and in life history traits.

OakContigDF159.1, a reference library for studying differential gene expression in Quercus robur during controlled biotic interactions: use for quantitative transcriptomic profiling of oak roots in ectomycorrhizal symbiosis

Oaks (Quercus spp.), which are major forest trees in the northern hemisphere, host many biotic interactions, but molecular investigation of these interactions is limited by fragmentary genome data. To date, only 75 oak expressed sequence tags (ESTs) have been characterized in ectomycorrhizal (EM) symbioses. We synthesized seven beneficial and detrimental biotic interactions between microorganisms and animals and a clone (DF159) of Quercus robur. Sixteen 454 and eight Illumina cDNA libraries from leaves and roots were prepared and merged to establish a reference for RNA-Seq transcriptomic analysis of oak EMs with Piloderma croceum. Using the Mimicking Intelligent Read Assembly (MIRA) and Trinity assembler, the OakContigDF159.1 hybrid assembly, containing 65 712 contigs with a mean length of 1003 bp, was constructed, giving broad coverage of metabolic pathways. This allowed us to identify 3018 oak contigs that were differentially expressed in EMs, with genes encoding proline-rich cell wall proteins and ethylene signalling-related transcription factors showing up-regulation while auxin and defence-related genes were down-regulated. In addition to the first report of remorin expression in EMs, the extensive coverage provided by the study permitted detection of differential regulation within large gene families (nitrogen, phosphorus and sugar transporters, aquaporins). This might indicate specific mechanisms of genome regulation in oak EMs compared with other trees.

Dual benefit from a belowground symbiosis: nitrogen fixing rhizobia promote growth and defense against a specialist herbivore in a cyanogenic plant

Legume-associated nitrogen-fixing bacteria play a key role for plant performance and productivity in natural and agricultural ecosystems. Although this plant-microbe mutualism has been known for decades, studies on effects of rhizobia colonisation on legume-herbivore interactions are scarce. We hypothesized that additional nitrogen provided by rhizobia may increase plant resistance by nitrogen-based defense mechanisms. We studied this below-aboveground interaction using a system consisting of lima bean (Phaseolus lunatus L.), rhizobia, and the Mexican bean beetle (Epilachna varivestis Muls.) as an insect herbivore. We showed that the rhizobial symbiosis not only promotes plant growth but also improves plant defense and resistance against herbivores. Results of our study lead to the suggestion that nitrogen provided by rhizobia is allocated to the production of nitrogen-containing cyanogenic defense compounds, and thereby crucially determines the outcome of plant-herbivore interactions. Our study supports the view that the fitness benefit of root symbioses includes defence mechanisms and thus extends beyond the promotion of plant growth. Since the associations between legumes and nitrogen-fixing rhizobia are ubiquitous in terrestrial ecosystems, improved knowledge on rhizobia-mediated effects on plant traits―and the resulting effects on higher trophic levels―is important for better understanding of the role of these microbes for ecosystem functioning.

Induced plant defense via volatile production is dependent on rhizobial symbiosis

Nitrogen-fixing rhizobia can substantially influence plant–herbivore interactions by altering plant chemical composition and food quality. However, the effects of rhizobia on plant volatiles, which serve as indirect and direct defenses against arthropod herbivores and as signals in defense-associated plant–plant and within-plant signaling, are still unstudied. We measured the release of jasmonic acid (JA)-induced volatiles of rhizobia-colonized and rhizobia-free lima bean plants (Fabaceae: Phaseolus lunatus L.) and tested effects of their respective bouquets of volatile organic compounds (VOCs) on a specialist insect herbivore (Mexican bean beetle; Coccinellidae: Epilachna varivestis Mulsant) in olfactometer choice trials. In a further experiment, we showed that VOC induction by JA reflects the plant responses to mechanical wounding and insect herbivory. Following induction with JA, rhizobia-colonized plants released significantly higher amounts of the shikimic acid-derived compounds, whereas the emission of compounds produced via the octadecanoid, mevalonate and non-mevalonate pathways was reduced. These changes affected the choice behavior of beetles as the preference of non-induced plants was much more pronounced for plants that were colonized by rhizobia. We showed that indole likely represents the causing agent for the observed repellent effects of jasmonic acid-induced VOCs of rhizobia-colonized lima bean plants. Our study demonstrates a rhizobia-triggered efficacy of induced plant defense via volatiles. Due to these findings, we interpret rhizobia as an integral part of legume defenses against herbivores.

Host plant genotype determines bottom-up effects in an aphid-parasitoid-predator system.

Plant genotypes are known to affect performance of insect herbivores and the community structure of both herbivores and higher trophic levels. Still, only a limited number of studies demonstrate differences in the performance of predators and parasitoids because of plant genotypic effects and most of these focus on gall formers. We designed a greenhouse experiment to investigate the effects of host plant genotype on fitness components in a grass‐aphid‐carnivore system. We used clones of quackgrass [Elytrigia repens (L.) Desv. ex Nevski (Poaceae)], the aphid Rhopalosiphum padi (L.) (Hemiptera: Aphididae), the parasitoid wasp Aphidius colemani (Viereck) (Hymenoptera: Braconidae), and the predatory lacewing Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). The number of aphid offspring differed considerably among plant genotypes. These differences were only in part because of differences in the production of biomass among host genotypes. Therefore, genotypes may differ in their nutritional value for phytophages. The number of aphids attacked by the parasitoid also differed among genotypes and aphid numbers only partly accounted for this effect. Moreover, pupal development time of female parasitoids was affected by plant genotype. We found no differences in mortality, body size, or sex ratio of hatching wasps between genotypes of quackgrass. Development time of the larvae and larval weight of the predatory lacewings differed among genotypes, but not weight of pupae and adults. Generally, the proportion of the total variance explained by the plant genotype was smaller for parasitoids and predators than for aphids. Overall, our experiments indicated that the plant genotype affects tri‐trophic interactions, but also that the strength of these effects decreases along the food chain.

ANTAGONISTIC INTERACTIONS BETWEEN PLANT COMPETITION AND INSECT HERBIVORY

Interspecific competition between plants and herbivory by specialized insects can have synergistic effects on the growth and performance of the attacked host plant. We tested the hypothesis that competition between plants may also negatively affect the performance of herbivores as well as their top-down effect on the host plant. In such a case, the combined effects of competition and herbivory may be less than expected from a simple multiplicative response. In other words, competition and herbivory may interact antagonistically. In a greenhouse experiment, Poa annua was grown in the presence or absence of a competitor (either Plantago lanceolata or Trifolium repens), as well as with or without a Poa-specialist aphid herbivore. Both competition and herbivory negatively affected Poa growth. Competition also reduced aphid density on Poa. This effect could in part be explained by changes in the biomass and the nitrogen content of Poa shoots. In treatments with competitors, reduced aphid densities alleviated the negative effect of herbivory on above- and belowground Poa biomass. Hence, we were able to demonstrate an antagonistic interaction between plant-plant interspecific competition and herbivory. However, response indices suggested that antagonistic interactions between competition and herbivory were contingent on the identity of the competitor. We found the antagonistic effect only in treatments with T. repens as the competitor. We conclude that both competitor identity and the herbivores ability to respond with changes in its density or activity to plant competition affect the magnitude and direction (synergistic vs. antagonistic) of the interaction between competition and herbivory on plant growth.

ABOVE‐ AND BELOWGROUND INTERACTIONS ARE MEDIATED BY NUTRIENT AVAILABILITY

By influencing nutrient mineralization in the soil, decomposers may affect the performance of plants and their associated herbivores. The strength of above-belowground linkages may therefore depend on the availability of nutrients in ecosystems. We investigated the dependency of decomposer- and leaf-herbivore-mediated changes in plant performance on soil nutrient availability in microcosm systems. In separate treatments, Poa annua was used as host plant for the herbivore and was grown in combination with different herb species: Plantago lanceolata, Trifolium repens, and Sanguisorba minor. At three different levels of nutrient availability, the impact of Collembola (Folsomia candida) and aphids (Rhopalosiphum padi), as well as their interacting effects on plant performance, were investigated. We further assessed the effects of Collembola on the performance of aphids and vice versa, as well as the effects on element contents in P. annua and soil nutrients. Collembola increased total aboveground biomass and biomass of single plant species (except T. repens) only at low and moderate nutrient availability, whereas the negative effects of aphids on P. annua and total aboveground biomass were highest at high nutrient availability. Collembola decreased relative root allocation. The negative effect of aphids on plant biomass was more pronounced in the presence of Collembola. Nitrogen concentration in shoots of P. annua was increased by Collembola. Aphids decreased the nitrogen concentration in grass shoots only when Collembola were present. These interacting effects can be related to indirect effects of decomposers on herbivore performance. At low and moderate nutrient availability, aphid numbers strongly increased due to decomposers, whereas at high nutrient availability this effect was much weaker. In turn, aphid herbivory increased the number of Collembola only at high nutrient availability. We conclude that the role of both below- and aboveground food webs for the dynamics of vegetation depend on each other and the availability of nutrients in ecosystems. This suggests that nutrient enrichment of ecosystems may have important consequences for above-belowground linkages and their effects on natural communities.

How do extreme drought and plant community composition affect host plant metabolites and herbivore performance

Water availability and plant community composition alter plant nutrient availability and the accumulation of plant defence compounds therefore having an impact on herbivore performance. Combined effects of drought stress and plant community composition on leaf chemicals and herbivore performance are largely unexplored. The objective of our study was, therefore, to find out the impact of extreme drought and of plant community composition on plant–herbivore interactions. Larvae of the generalist butterfly Spodoptera littoralis were reared on leaves of the grass Holcus lanatus which was grown in experimental communities, differing in species- and functional group richness. These communities were either subjected to extreme drought or remained under ambient climatic conditions. Drought decreased relative water content, soluble protein content, nitrogen and total phenol content and increased the content of carbohydrates in the grass. As a consequence, the larvae feeding on drought-exposed plants revealed a longer larval stage, increased pupal weight and higher adult eclosion rates. Plant community composition mainly caused changes to the defensive compounds of the grass, but also marginally affected protein and carbohydrate content. Larvae feeding on species-richest communities without legumes showed the highest mortality. Our findings imply that climate change that is projected to increase the frequency of severe droughts, as well as alter plant community compositions, is likely to affect arthropod–plant interactions through an alteration of leaf chemicals.

Interaction between silicon cycling and straw decomposition in a silicon deficient rice production system

Background and aimsRice plants (Oryza sativa L.) contain large quantities of silicon (Si) in form of phytoliths, which increase their resistance to abiotic and biotic stresses. The Si cycle through rice fields is hardly studied. We tested how increasing Si availability affects rice growth and the decomposability of the straw. Secondly we tested the role of straw recycling for Si availability.MethodsIn a field experiment, we applied three levels of silica gel during one rice cropping season. In a follow-up laboratory experiment, we used straw produced in the field experiment, having different Si concentrations, and studied straw decomposition, straw Si release, and Si uptake by plants.ResultsSilicon fertilization increased Si contents, biomass production, and grain yield of rice plants. Increased Si uptake by rice decreased concentrations of C and some essential nutrients (N, P, K, Ca, and Mg) in the straw, and increased straw decomposability and Si release.ConclusionsFertilization with silica gel is an option to improve Si supply to rice plants growing on weathered soils with low levels of plant-available Si. Phytoliths from fresh rice straw dissolve fast in soil, thus, recycling of rice straw is an important source of plant-available Si.