W. H. Gera Hol

Soil food web properties explain ecosystem services across European land use systems

Intensive land use reduces the diversity and abundance of many soil biota, with consequences for the processes that they govern and the ecosystem services that these processes underpin. Relationships between soil biota and ecosystem processes have mostly been found in laboratory experiments and rarely are found in the field. Here, we quantified, across four countries of contrasting climatic and soil conditions in Europe, how differences in soil food web composition resulting from land use systems (intensive wheat rotation, extensive rotation, and permanent grassland) influence the functioning of soils and the ecosystem services that they deliver. Intensive wheat rotation consistently reduced the biomass of all components of the soil food web across all countries. Soil food web properties strongly and consistently predicted processes of C and N cycling across land use systems and geographic locations, and they were a better predictor of these processes than land use. Processes of carbon loss increased with soil food web properties that correlated with soil C content, such as earthworm biomass and fungal/bacterial energy channel ratio, and were greatest in permanent grassland. In contrast, processes of N cycling were explained by soil food web properties independent of land use, such as arbuscular mycorrhizal fungi and bacterial channel biomass. Our quantification of the contribution of soil organisms to processes of C and N cycling across land use systems and geographic locations shows that soil biota need to be included in C and N cycling models and highlights the need to map and conserve soil biodiversity across the world.

Intensive agriculture reduces soil biodiversity across Europe

Soil biodiversity plays a key role in regulating the processes that underpin the delivery of ecosystem goods and services in terrestrial ecosystems. Agricultural intensification is known to change the diversity of individual groups of soil biota, but less is known about how intensification affects biodiversity of the soil food web as a whole, and whether or not these effects may be generalized across regions. We examined biodiversity in soil food webs from grasslands, extensive, and intensive rotations in four agricultural regions across Europe: in Sweden, the UK, the Czech Republic and Greece. Effects of land-use intensity were quantified based on structure and diversity among functional groups in the soil food web, as well as on community-weighted mean body mass of soil fauna. We also elucidate land-use intensity effects on diversity of taxonomic units within taxonomic groups of soil fauna. We found that between regions soil food web diversity measures were variable, but that increasing land-use intensity caused highly consistent responses. In particular, land-use intensification reduced the complexity in the soil food webs, as well as the community-weighted mean body mass of soil fauna. In all regions across Europe, species richness of earthworms, Collembolans, and oribatid mites was negatively affected by increased land-use intensity. The taxonomic distinctness, which is a measure of taxonomic relatedness of species in a community that is independent of species richness, was also reduced by land-use intensification. We conclude that intensive agriculture reduces soil biodiversity, making soil food webs less diverse and composed of smaller bodied organisms. Land-use intensification results in fewer functional groups of soil biota with fewer and taxonomically more closely related species. We discuss how these changes in soil biodiversity due to land-use intensification may threaten the functioning of soil in agricultural production systems.

Where less may be more: how the rare biosphere pulls ecosystems strings

Rare species are increasingly recognized as crucial, yet vulnerable components of Earth’s ecosystems. This is also true for microbial communities, which are typically composed of a high number of relatively rare species. Recent studies have demonstrated that rare species can have an over-proportional role in biogeochemical cycles and may be a hidden driver of microbiome function. In this review, we provide an ecological overview of the rare microbial biosphere, including causes of rarity and the impacts of rare species on ecosystem functioning. We discuss how rare species can have a preponderant role for local biodiversity and species turnover with rarity potentially bound to phylogenetically conserved features. Rare microbes may therefore be overlooked keystone species regulating the functioning of host-associated, terrestrial and aquatic environments. We conclude this review with recommendations to guide scientists interested in investigating this rapidly emerging research area.

Getting the ecology into interactions between plants and the plant growth-promoting bacterium Pseudomonas fluorescens

Plant growth-promoting rhizobacteria (PGPR) are increasingly appreciated for their contributions to primary productivity through promotion of growth and triggering of induced systemic resistance in plants. Here we focus on the beneficial effects of one particular species of PGPR (Pseudomonas fluorescens) on plants through induced plant defense. This model organism has provided much understanding of the underlying molecular mechanisms of PGPR-induced plant defense. However, this knowledge can only be appreciated at full value once we know to what extent these mechanisms also occur under more realistic, species-diverse conditions as are occurring in the plant rhizosphere. To provide the necessary ecological context, we review the literature to compare the effect of P. fluorescens on induced plant defense when it is present as a single species or in combination with other soil dwelling species. Specifically, we discuss combinations with other plant mutualists (bacterial or fungal), plant pathogens (bacterial or fungal), bacterivores (nematode or protozoa), and decomposers. Synergistic interactions between P. fluorescens and other plant mutualists are much more commonly reported than antagonistic interactions. Recent developments have enabled screenings of P. fluorescens genomes for defense traits and this could help with selection of strains with likely positive interactions on biocontrol. However, studies that examine the effects of multiple herbivores, pathogens, or herbivores and pathogens together on the effectiveness of PGPR to induce plant defenses are underrepresented and we are not aware of any study that has examined interactions between P. fluorescens and bacterivores or decomposers. As co-occurring soil organisms can enhance but also reduce the effectiveness of PGPR, a better understanding of the biotic factors modulating P. fluorescens–plant interactions will improve the effectiveness of introducing P. fluorescens to enhance plant production and defense.

Plant–soil feedbacks of exotic plant species across life forms: a meta-analysis

Invasive exotic plant species effects on soil biota and processes in their new range can promote or counteract invasions via changed plant–soil feedback interactions to themselves or to native plant species. Recent meta-analyses reveale that soil influenced by native and exotic plant species is affecting growth and performance of natives more strongly than exotics. However, the question is how uniform these responses are across contrasting life forms. Here, we test the hypothesis that life form matters for effects on soil and plant–soil feedback. In a meta-analysis we show that exotics enhanced C cycling, numbers of meso-invertebrates and nematodes, while having variable effects on other soil biota and processes. Plant effects on soil biota and processes were not dependent on life form, but patterns in feedback effects of natives and exotics were dependent on life form. Native grasses and forbs caused changes in soil that subsequently negatively affected their biomass, whereas native trees caused changes in soil that subsequently positively affected their biomass. Most exotics had neutral feedback effects, although exotic forbs had positive feedback effects. Effects of exotics on natives differed among plant life forms. Native trees were inhibited in soils conditioned by exotics, whereas native grasses were positively influenced in soil conditioned by exotics. We conclude that plant life form matters when comparing plant–soil feedback effects both within and between natives and exotics. We propose that impact analyses of exotic plant species on the performance of native plant species can be improved by comparing responses within plant life form.

Comparing arbuscular mycorrhizal communities of individual plants in a grassland biodiversity experiment

Plants differ greatly in the soil organisms colonizing their roots. However, how soil organism assemblages of individual plant roots can be influenced by plant community properties remains poorly understood. We determined the composition of arbuscular mycorrhizal fungi (AMF) in Jacobaea vulgaris plants, using terminal restriction fragment length polymorphism (T-RFLP). The plants were collected from an experimental field site with sown and unsown plant communities. Natural colonization was allowed for 10 yr in sown and unsown plots. Unsown plant communities were more diverse and spatially heterogeneous than sown ones. Arbuscular mycorrhizal fungi diversity did not differ between sown and unsown plant communities, but there was higher AMF assemblage dissimilarity between individual plants in the unsown plant communities. When we grew J. vulgaris in field soil that was homogenized after collection in order to rule out spatial variation, no differences in AMF dissimilarity between sown and unsown plots were found. Our study shows that experimental manipulation of plant communities in the field, and hence plant community assembly history, can influence the AMF communities of individual plants growing in those plant communities. This awareness is important when interpreting results from field surveys and experimental ecological studies in relation to plant-symbiont interactions.

Non‐random species loss in bacterial communities reduces antifungal volatile production

The contribution of low-abundance microbial species to soil ecosystems is easily overlooked because there is considerable overlap between metabolic abilities (functional redundancy) of dominant and subordinate microbial species. Here we studied how loss of less abundant soil bacteria affected the production of antifungal volatiles, an important factor in the natural control of soil-borne pathogenic fungi. We provide novel empirical evidence that the loss of soil bacterial species leads to a decline in the production of volatiles that suppress root pathogens. By using dilution-to-extinction for seven different soils we created bacterial communities with a decreasing number of species and grew them under carbon-limited conditions. Communities with high bacterial species richness produced volatiles that strongly reduced the hyphal growth of the pathogen Fusarium oxysporum. For most soil origins loss of bacterial species resulted in loss of antifungal volatile production. Analysis of the volatiles revealed that several known antifungal compounds were only produced in the more diverse bacterial communities. Our results suggest that less abundant bacterial species play an important role in antifungal volatile production by soil bacterial communities and, consequently, in the natural suppression of soil-borne pathogens.

Competition Increases Sensitivity of Wheat (Triticum aestivum) to Biotic Plant-Soil Feedback

Plant-soil feedback (PSF) and plant competition play an important role in structuring vegetation composition, but their interaction remains unclear. Recent studies suggest that competing plants could dilute pathogenic effects, whereas the standing view is that competition may increase the sensitivity of the focal plant to PSF. In agro-ecosystems each of these two options would yield contrasting outcomes: reduced versus enhanced effects of weeds on crop biomass production. To test the effect of competition on sensitivity to PSF, we grew Triticum aestivum (Common wheat) with and without competition from a weed community composed of Vicia villosa, Chenopodium album and Myosotis arvensis. Plants were grown in sterilized soil, with or without living field inoculum from 4 farms in the UK. In the conditioning phase, field inocula had both positive and negative effects on T. aestivum shoot biomass, depending on farm. In the feedback phase the differences between shoot biomass in T. aestivum monoculture on non-inoculated and inoculated soils had mostly disappeared. However, T. aestivum plants growing in mixtures in the feedback phase were larger on non-inoculated soil than on inoculated soil. Hence, T. aestivum was more sensitive to competition when the field soil biota was present. This was supported by the statistically significant negative correlation between shoot biomass of weeds and T. aestivum, which was absent on sterilized soil. In conclusion, competition in cereal crop-weed systems appears to increase cereal crop sensitivity to soil biota.

Soil and Freshwater and Marine Sediment Food Webs: Their Structure and Function

The food webs of terrestrial soils and of freshwater and marine sediments depend on adjacent aboveground or pelagic ecosystems for organic matter input that provides nutrients and energy. There are important similarities in the flow of organic matter through these food webs and how this flow feeds back to primary production. In both soils and sediments, trophic interactions occur in a cycle in which consumers stimulate nutrient cycling such that mineralized resources are made available to the primary producers. However, aquatic sediments and terrestrial soils differ greatly in the connectivity between the production and the consumption of organic matter. Terrestrial soils and shallow aquatic sediments can receive organic matter within hours of photosynthesis when roots leak carbon, whereas deep oceanic sediments receive organic matter possibly months after carbon assimilation by phytoplankton. This comparison has implications for the capacity of soils and sediments to affect the global carbon balance.

Context dependency and saturating effects of loss of rare soil microbes on plant productivity

Land use intensification is associated with loss of biodiversity and altered ecosystem functioning. Until now most studies on the relationship between biodiversity and ecosystem functioning focused on random loss of species, while loss of rare species that usually are the first to disappear received less attention. Here we test if the effect of rare microbial species loss on plant productivity depends on the origin of the microbial soil community. Soils were sampled from three land use types at two farms. Microbial communities with increasing loss of rare species were created by inoculating sterilized soils with serially diluted soil suspensions. After 8 months of incubation, the effects of the different soil communities on abiotic soil properties, soil processes, microbial community composition, and plant productivity was measured. Dilution treatments resulted in increasing species loss, which was in relation to abundance of bacteria in the original field soil, without affecting most of the other soil parameters and processes. Microbial species loss affected plant biomass positively, negatively or not at all, depending on soil origin, but not on land use history. Even within fields the effects of dilution on plant biomass varied between replicates, suggesting heterogeneity in microbial community composition. The effects of medium and severe species loss on plant biomass were similar, pointing toward a saturating effect of species loss. We conclude that changes in the composition of the soil microbial community, including rare species loss, can affect plant productivity, depending on the composition of the initial microbial community. Future work on the relation between function and species loss effects should address this variation by including multiple sampling origins.