Predictability of plant-soil feedback

ABSTRACT In my thesis project I studied the role of soil biota as possible drivers of linkages between plant community diversity and plant productivity. My study was carried out in the framework of a large grassland biodiversity experiment in Jena, the so-called Jena Experiment. In chapter 1 I explain how soil biota may exert control over plant community productivity by recycling organic material and by intimately interacting with plant roots, either acting as antagonists to plants or as plant growth-promoting symbionts. Reciprocal interactions between plant and soil communities are an important component of so-called ‘plant-soil feedbacks’ (PSFs). In the PSF loop, plant community composition drives changes in belowground communities and abiotic conditions, which can subsequently alter plant community composition and productivity. Such PSF interactions have been proposed to play a major role in plant community composition and functioning. In the second chapter I review studies that use an experimental approach of inoculating live soils into sterilized background soils to study the effects of root symbionts on plant growth. I demonstrate that we make many assumptions when translating results of controlled studies to natural systems. I propose that we should continuously and carefully consider these assumptions and aim for rigid hypothesis testing by cross-talking between different levels of ecological realism. In chapter 3 I test how plant traits relate to PSF using a 49 grassland plant species of the Jena Experiment. First, I grew individuals of all species for two months in sterilized soil inoculated with field soil. In the subsequent feedback phase, I grew all plant species for 6 weeks in sterilized soil inoculated with (I) species-specific inoculum (conspecific conditioned soil), (II) sterilized species-specific inoculum, or (III) a mixture of all 49 species-specific inoculums (mixed conditioned soil). Subsequently I compared biomass production in conspecific conditioned soil to biomass production in sterilized soil (PSFsterilized) and in mixed conditioned soil (PSFmixed). Species with increasing specific root length (SRL) were increasingly susceptible to antagonistic interactions in conspecific conditioned soil (i.e. they had strong negative PSFsterilized), while thick-rooted plants had both positive PSFsterilized and high colonization rates of arbuscular mycorrhizal fungi (AMF). Finally, I showed that species ranking of PSFmixed was similar to species ranking of PSFsterilized, indicating that plants with increasingly negative net interactions in conspecific conditioned soil increasingly benefit from growing in mixed conditioned soil. With these findings, I made a first important step in placing PSFs in plant ecological strategy frameworks: high SRL is typical for plants that adopt a ‘fast’ growth strategy, characterized by fast resource acquisition but poor defense against antagonists and little reliance on AMF. In chapter 4, I test the relation between phylogenetic relatedness and the feedback effect of one (soil conditioning) plant species to another (responding) plant species. This is named indirect PSF. I grew eleven focal plant species, chosen to represent plants that had negative, neutral and positive PSFsterilized, in soils that were conditioned by conspecifics and soils conditioned by three to four other species with a varying degree of phylogenetic relatedness to the focal plant species. I found that plant species with negative PSF had no different or slightly better growth when growing in soil conditioned by plant species with larger phylogenetic distance to the focal plant. In contrast, plant species with neutral PSF grew less well, and species with positive PSF even worse, in soil conditioned by plant species with increasing phylogenetic distance to the focal plant. I conclude that the effect of phylogenetic relatedness on PSF interactions between plant species may depend on the tendency of the focal plant species to develop detrimental or beneficial interactions with soil microbes. In chapter 5, I use the PSFmixed values of chapter 3 in a correlational analysis to test how short-term PSFs relate to longer-term species’ performances in the field, using established monocultures and species-rich (60 species) plant communities of the Jena Experiment. Based on some recently published studies I expected that plants with more negative PSFmixed would benefit most from growing in mixtures; these plant species were expected to overyield most in mixed plant communities. However, opposite to the expectation, plant species with the most negative PSF produced least biomass in the 60-species plant communities, whereas plant performance in monoculture was not related to its short-term PSF. I conclude that species-specific overyielding was positively related to species-specific PSF, and that community overyielding was mostly driven by plant species with a neutral to positive PSF. Finally, in chapter 6 I examine the role of quality and quantity of plant biomass in driving nematode feeding group abundance and diversity. I found strong positive effects of both plant species- and plant functional group-richness on abundances of plant feeding, bacterial feeding and fungal feeding nematodes, as well as omnivores, but not for predators. Structural equation modeling (SEM) analysis showed that the positive effect of plant diversity on the abundance of microbial feeding nematodes (fungal plus bacterial feeders) could not be explained by increased microbial biomass. Similarly, the abundance of plant feeding nematodes was not driven by the higher plant biomass in species rich plant communities. Instead, increased plant biomass explained the positive relation between plant species richness and the abundance of microbial feeding nematodes, while for plant feeding nematodes, increased C to N ratio of aboveground plant biomass appeared to explain the positive relation between the abundance of plant feeding nematodes and plant species and functional group richness. Importantly, the density of plant feeding nematodes per unit root biomass decreased with increasing plant diversity, indicating a root feeder dilution effect. I conclude that plant diversity does not explain nematode community composition primarily by simple bottom-up relations, but that other aspects, such as quality of resource and microhabitats quality, may play a role as well.</p

The strength of negative plant–soil feedback increases from the intraspecific to the interspecific and the functional group level

One of the processes that may play a key role in plant species coexistence and ecosystem functioning is plant–soil feedback, the effect of plants on associated soil communities and the resulting feedback on plant performance. Plant–soil feedback at the interspecific level (comparing growth on own soil with growth on soil from different species) has been studied extensively, while plant–soil feedback at the intraspecific level (comparing growth on own soil with growth on soil from different accessions within a species) has only recently gained attention. Very few studies have investigated the direction and strength of feedback among different taxonomic levels, and initial results have been inconclusive, discussing phylogeny, and morphology as possible determinants. To test our hypotheses that the strength of negative feedback on plant performance increases with increasing taxonomic level and that this relationship is explained by morphological similarities, we conducted a greenhouse experiment using species assigned to three taxonomic levels (intraspecific, interspecific, and functional group level). We measured certain fitness‐related aboveground traits and used them along literature‐derived traits to determine the influence of morphological similarities on the strength and direction of the feedback. We found that the average strength of negative feedback increased from the intraspecific over the interspecific to the functional group level. However, individual accessions and species differed in the direction and strength of the feedback. None of our results could be explained by morphological dissimilarities or individual traits. Synthesis. Our results indicate that negative plant–soil feedback is stronger if the involved plants belong to more distantly related species. We conclude that the taxonomic level is an important factor in the maintenance of plant coexistence with plant–soil feedback as a potential stabilizing mechanism and should be addressed explicitly in coexistence research, while the traits considered here seem to play a minor role

The curse of the black box

Background Soil is a foremost provider of (agro-) ecosystem services, making plant-soil interactions pivotal in agriculture research. The functioning of soils entails complex interactions between soil biota and the abiotic soil environment and is therefore often considered as a ‘black box’. The study of Verbruggen et al. (this volume) tries to crack the black box open by examining the role of soil microbial communities from conventional and organic farming fields for the growth of Zea mays and phosphorous retention in the soil. Scope In this commentary on the paper of Verbruggen et al. (2011) we use the study to illustrate that investigating soils, and specifically the role of soil biota in ecosystem functioning, is not straightforward, given the overwhelming soil biodiversity and the complexity of soil as a habitat. We discuss the key elements that need to be considered in order to translate results of highly controlled experiments with inoculated soil biota to their functioning in the field. Conclusions Verbruggen et al. contribute to our understanding of the functional role of AMF in agro-ecosystems. Yet the results only allow us to merely speculate about the realized functional role of AMF communities in the field, a very interesting avenue for future research

The curse of the black box

Background Soil is a foremost provider of (agro-) ecosystem services, making plant-soil interactions pivotal in agriculture research. The functioning of soils entails complex interactions between soil biota and the abiotic soil environment and is therefore often considered as a ‘black box’. The study of Verbruggen et al. (this volume) tries to crack the black box open by examining the role of soil microbial communities from conventional and organic farming fields for the growth of Zea mays and phosphorous retention in the soil. Scope In this commentary on the paper of Verbruggen et al. (2011) we use the study to illustrate that investigating soils, and specifically the role of soil biota in ecosystem functioning, is not straightforward, given the overwhelming soil biodiversity and the complexity of soil as a habitat. We discuss the key elements that need to be considered in order to translate results of highly controlled experiments with inoculated soil biota to their functioning in the field. Conclusions Verbruggen et al. contribute to our understanding of the functional role of AMF in agro-ecosystems. Yet the results only allow us to merely speculate about the realized functional role of AMF communities in the field, a very interesting avenue for future researc

Possible mechanisms underlying abundance and diversity responses of nematode communities to plant diversity

Plant diversity is known to influence the abundance and diversity of belowground biota; however, patterns are not well predictable and there is still much unknown about the driving mechanisms. We analyzed changes in soil nematode community composition as affected by long-term manipulations of plant species and functional group diversity in a field experiment with plant species diversity controlled by sowing a range of 1-60 species mixtures and controlling non-sown species by hand weeding. Nematode communities contain a variety of species feeding on bacteria, fungi, plants, invertebrates, while some are omnivorous. We analyzed responses of nematode abundance and diversity to plant species and functional diversity, and used structural equation modeling (SEM) to explore the possible mechanisms underlying the observed patterns. The abundance of individuals of all nematode feeding types, except for predatory nematodes, increased with both plant species and plant functional group diversity. The abundance of microbial-feeding nematodes was related positively to aboveground plant community biomass, whereas abundance of plant-feeding nematodes was related positively to shoot C:N ratio. The abundance of predatory nematodes, in turn, was positively related to numbers of plant-feeding nematodes, but not to the abundance of microbial feeders. Interestingly, the numbers of plant-feeding nematodes per unit root mass were lowest in the high-diversity plant communities, pointing at reduced exposure to belowground herbivores when plants grow in species-diverse communities. Taxon richness of plant-feeding and microbialfeeding nematodes increased with plant species and plant functional group diversity. Increasing plant functional group diversity also enhanced taxon richness of predatory nematodes. The SEM suggests that bottom-up control effects of plant species and plant functional group diversity on abundance of nematodes in the various feeding types predominantly involve mechanistic linkages related to plant quality instead of plant quantity; especially, C:N ratios of the shoot tissues, and/or effects of plants on the soil habitat, rather than shoot quantity explained nematode abundance. Although aboveground plant properties may only partly serve as a proxy for belowground resource quality and quantity, our results encourage further studies on nematode responses to variations in plant species and plant functional diversity in relation to both quantity and quality of the belowground resources.</p

Biodiversity increases multitrophic energy use efficiency, flow and storage in grasslands

The continuing loss of global biodiversity has raised questions about the risk that species extinctions pose for the functioning of natural ecosystems and the services that they provide for human wellbeing. There is consensus that, on single trophic levels, biodiversity sustains functions; however, to understand the full range of biodiversity effects, a holistic and multitrophic perspective is needed. Here, we apply methods from ecosystem ecology that quantify the structure and dynamics of the trophic network using ecosystem energetics to data from a large grassland biodiversity experiment. We show that higher plant diversity leads to more energy stored, greater energy flow and higher community-energy-use efficiency across the entire trophic network. These effects of biodiversity on energy dynamics were not restricted to only plants but were also expressed by other trophic groups and, to a similar degree, in aboveground and belowground parts of the ecosystem, even though plants are by far the dominating group in the system. The positive effects of biodiversity on one trophic level were not counteracted by the negative effects on adjacent levels. Trophic levels jointly increased the performance of the community, indicating ecosystem-wide multitrophic complementarity, which is potentially an important prerequisite for the provisioning of ecosystem services.</p