Lisa Bjørnlund

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.

Legacy effects of drought on plant growth and the soil food web.

Soils deliver important ecosystem services, such as nutrient provision for plants and the storage of carbon (C) and nitrogen (N), which are greatly impacted by drought. Both plants and soil biota affect soil C and N availability, which might in turn affect their response to drought, offering the potential to feed back on each other’s performance. In a greenhouse experiment, we compared legacy effects of repeated drought on plant growth and the soil food web in two contrasting land-use systems: extensively managed grassland, rich in C and with a fungal-based food web, and intensively managed wheat lower in C and with a bacterial-based food web. Moreover, we assessed the effect of plant presence on the recovery of the soil food web after drought. Drought legacy effects increased plant growth in both systems, and a plant strongly reduced N leaching. Fungi, bacteria, and their predators were more resilient after drought in the grassland soil than in the wheat soil. The presence of a plant strongly affected the composition of the soil food web, and alleviated the effects of drought for most trophic groups, regardless of the system. This effect was stronger for the bottom trophic levels, whose resilience was positively correlated to soil available C. Our results show that plant belowground inputs have the potential to affect the recovery of belowground communities after drought, with implications for the functions they perform, such as C and N cycling.

Interactions between saprotrophic fungi, bacteria and protozoa on decomposing wheat roots in soil influenced by the fungicide fenpropimorph (Corbel®): a field study.

Abstract Litterbags containing freshly harvested wheat roots with adhering rhizosphere soil were placed in their native soil. Four levels of the fungicide fenpropimorph were applied: 0, 1, 10 and 100 mg kg −1 soil. The experimental set-up was a randomised block design with five replicates. Litterbags were sampled six times over a 4-month period and microbial numbers determined. Bacteria (colony forming units, CFUs) and protozoa (most probable number) followed a similar pattern: a sudden decrease at the onset of the study period was followed by a fast recovery and increase. This ended at maximum mean values of ≈7.5 × 10 7 bacteria g −1 root litter by day 7 and 3 × 10 6 protozoa g −1 root litter by day 20, respectively. Fenpropimorph had no significant effect on either of these two groups, for which mean population sizes seemed to interact in a prey–predator manner. The fungi (stained by calcofluor white and fluorescein diacetate) were unaffected by the pesticide until day 20. Hereafter, fluorescein diacetate-active (FDA-active) hyphae were significantly inhibited in all fungicide treated plots, compared to the untreated plots 50 and 114 days after the application of fenpropimorph. Fungal colony forming units (fungal CFUs) on fenpropimorph-containing agar demonstrated a selection towards more fenpropimorph tolerant fungi in the 100 mg kg −1 fenpropimorph treated plots. The delayed effect of fenpropimorph on FDA-activity could be explained as a combined effect of the pesticide and the degradation product itself, and the fluctuating water stressing field conditions of this year. Our results, thus, demonstrated long term effects of fenpropimorph on the activity of saprotrophic fungi at recommended field dose, and that high dose fenpropimorph can select for fenpropimorph tolerant fungal populations.

Bacterial feeders, the nematode Caenorhabditis elegans and the flagellate Cercomonas longicauda, have different effects on outcome of competition among the Pseudomonas biocontrol strains CHA0 and DSS73.

How bacterial feeding fauna affects colonization and survival of bacteria in soil is not well understood, which constrains the applicability of bacterial inoculants in agriculture. This study aimed to unravel how food quality of bacteria and bacterial feeders with different feeding habits (the selective feeding flagellate Cercomonas longicauda versus the non-selective feeding nematode Caenorhabditis elegans) influence the abundance of two bacteria that compete for resources in simple model communities. Microcosms consisted of either one gfp-tagged bacterial strain (Pseudomonas fluorescens DSM50090 or one of two biocontrol strains P. fluorescens CHA0 or Pseudomonas sp. DSS73) or combinations of two bacterial strains. DSM50090 is a suitable food bacterium, DSS73 is of intermediate food quality, and CHA0 is inedible to the bacterial feeders. Bacterial and protozoan cell numbers were measured by flow cytometry. In the presence of flagellates, CHA0 increased its abundance as compared to the other biocontrol strain DSS73 or to DSM50090, which were both eaten by the flagellates. In contrast, the number of CHA0 declined as compared to DSS73 when the model community was subjected to nematode predation pressure. Hence, the results suggested that the outcome of competition among bacteria depended on their ability to cope with the prevailing bacterial predator.

Trophic interactions between rhizosphere bacteria and bacterial feeders influenced by phosphate and aphids in barley

The aim was to study the effects of P fertilization and leaf aphid attack on the trophic interactions of bacteria and bacterial feeders in the rhizospheres of barley plants. The density of protozoa peaked in the rhizospheres of plants fertilized with N and P, whereas nematodes peaked in the rhizospheres of plants to which only N had been added. Fingerprinting of bacterial communities by length heterogeneity polymerase chain reaction revealed differences in community structure between NP rhizospheres and N rhizospheres as well as aphid-related differences within N rhizospheres. Specifically, α-proteobacteria increased with P addition. To evaluate if differences in bacteria in terms of their quality as food could partly explain the observed differences in protozoan and nematode abundances, growth of the flagellate Cercomonas sp. was assessed with 935 bacteria isolated from the different treatments. This assay indicated that bacterial isolates were of higher food quality to Cercomonas sp. in NP than in N rhizospheres when plants were subjected to aphid attack. Bacteria of high and low food quality for Cercomonas sp., respectively, were fed to the nematode Caenorhabditis elegans and larval production examined. α-Proteobacteria supported the growth of Cercomonas sp. well, whereas Actinobacteria did not. In contrast, C. elegans reproduced poorly on most α-proteobacteria but were able to reproduce well on some Actinobacteria. These results suggest that the different response of protozoa and nematodes to P addition could be mediated through a food quality-related change in community composition of bacteria and that leaf aphid attack may interfere with nutrient effects on bacterial assemblages of rhizospheres.

Disturbance Promotes Non-Indigenous Bacterial Invasion in Soil Microcosms: Analysis of the Roles of Resource Availability and Community Structure

Background Invasion-biology is largely based on non-experimental observation of larger organisms. Here, we apply an experimental approach to the subject. By using microbial-based microcosm-experiments, invasion-biology can be placed on firmer experimental, and hence, less anecdotal ground. A better understanding of the mechanisms that govern invasion-success of bacteria in soil communities will provide knowledge on the factors that hinder successful establishment of bacteria artificially inoculated into soil, e.g. for remediation purposes. Further, it will yield valuable information on general principles of invasion biology in other domains of life. Methodology/Principal Findings Here, we studied invasion and establishment success of GFP-tagged Pseudomonas fluorescens DSM 50090 in laboratory microcosms during a 42-day period. We used soil heating to create a disturbance gradient, and hypothesized that increased disturbance would facilitate invasion; our experiments confirmed this hypothesis. We suggest that the key factors associated with the heating disturbance that explain the enhanced invasion success are increased carbon substrate availability and reduced diversity, and thus, competition- and predation-release. In a second experiment we therefore separated the effects of increased carbon availability and decreased diversity. Here, we demonstrated that the effect of the indigenous soil community on bacterial invasion was stronger than that of resource availability. In particular, introduced bacteria established better in a long term perspective at lower diversity and predation pressure. Conclusion We propose increased use of microbial systems, for experimental study of invasion scenarios. They offer a simple and cost-efficient way to study and understand biological invasion. Consequently such systems can help us to better predict the mechanisms controlling changes in stability of communities and ecosystems. This is becoming increasingly relevant since anthropogenic disturbance causes increasing global change, which promotes invasion. Moreover, a thorough understanding of factors controlling invasion and establishment of artificially amended micro-organisms will mean a major step forward for soil-remediation microbiology.

Functional GacS in Pseudomonas DSS73 prevents digestion by Caenorhabditis elegans and protects the nematode from killer flagellates.

The success of biocontrol bacteria in soil depends in part on their ability to escape predation. We explored the interactions between Pseudomonas strain DSS73 and two predators, the nematode Caenorhabditis elegans and the flagellate Cercomonas sp. Growth of the nematode in liquid culture was arrested when it was feeding on DSS73 or a DSS73 mutant (DSS73-15C2) unable to produce the biosurfactant amphisin, whereas a regulatory gacS mutant (DSS73-12H8) that produces no exoproducts supported fast growth of the nematode. The flagellate Cercomonas sp. was able to grow on all three strains. The biosurfactant-deficient DSS73 mutant caused severe dilation of the nematode gut. In three-species systems (DSS73, Cercomonas and C. elegans), the nematodes fed on the flagellates, which in turn grazed the bacteria and the number of C. elegans increased. The flagellates Cercomonas sp. usually kill C. elegans. However, DSS73 protected the nematodes from flagellate killing. Soil microcosms inoculated with six rhizobacteria and grazed by nematodes were colonized more efficiently by DSS73 than similar systems grazed by flagellates or without grazers. In conclusion, our results suggest that C. elegans and DSS73 mutually increase the survival of one another in complex multispecies systems and that this interaction depends on the GacS regulator.

Simulated herbivory effects on rhizosphere organisms in pea (Pisum sativum) depended on phosphate

The effects of simulated aboveground herbivory and phosphate addition to soil on rhizosphere organisms (arbuscular mychorrhiza (AM), Rhizobium spp., bacteria, protozoa and nematodes) were studied in a 2 by 2 factorial designed pot experiment with Pea plants (Pisum sativum). Measurements were performed on 24 day old plants that were still in the nutrient acquisition phase before flowering. AM colonization and bacterial feeding nematodes were stimulated by high simulated her- bivory especially when plants were phosphate deficient. Total number of nematodes was higher with phosphate deficiency. Furthermore, non-significant peak values in soil respiration, total number of nematodes, and bacterial number were observed in phosphate deficient plants with high simulated herbivory. In phosphate amended plants, fast-growing protozoa and bacterial feeding nematodes decreased at high simulated herbivory. These results support the hypothesis that the plant regulates abundances of both AM and free-living rhizosphere organisms and thereby the amount of plant-available nutrients, according to demand via root exudation. Rhizobium spp. was significantly stimulated by phosphate addition but not affected by simulated herbivory. Metabolites produced by rhizosphere bacteria from plants exposed to high simulated herbivory in phosphate amended soil stimulated seed performance. Possible interactions between protozoa and nematodes in relation to production and composition of bacteria in the rhizosphere are discussed.

Nematode communities of natural and managed beech forests – a pilot survey

Summary The soil nematode communities of natural beech forests and managed beech forests were surveyed in order to examine which community parameters, if any, would be suited to differentiate between the two management regimes. Nematodes were collected from mineral soil at three sites, each including managed and adjacent natural beech forests. Following enumeration and identification of nematodes to family level, relative abundance of trophic groups, adult/juvenile ratio, Shannon-index, Plant Parasitic Index (PPI) and Maturity Index (MI) were determined. A clear separation of samples according to site was found in a Canonical Community Ordination (CANOCO) that related nematode data and various soil parameters in each sample. Beech forests of Mid-Zealand (Suserup) had significantly lower sand content, higher pH, higher PPI and higher nematode diversity according to the Shannon-index than the forests of North Zealand (Farum and Rankeskov). A distinct difference in the distribution of families was observed between sites, which could be governed by differences in texture and pH. The MI of the two old natural forest sites (Farum and Suserup) was significantly higher than the comparable managed sites, while this was not the case for Rankeskov, which is in a less mature state. There was a significantly higher adult/juvenile ratio and higher relative abundance of bacterial feeders in the natural forests compared to the managed forests. The apparent relation between pH and Maturity Index in beech forests is discussed. We suggest dead wood input to be the driving variable leading to the observed differences in the nematode community between managed and natural forests of Zealand, Denmark. The marked site differences found in this study emphasizes the need to carefully choose reference areas where soil conditions etc. are very similar to the managed forest in question when reference schemes for nature-based forestry are being developed.