Publications by authors named "Wim H Van Der Putten"

120 Publications

Global data on earthworm abundance, biomass, diversity and corresponding environmental properties.

Sci Data 2021 05 21;8(1):136. Epub 2021 May 21.

Forest Sciences and Forest Ecology, University of Göttingen, Büsgenweg 1, Göttingen, Germany.

Earthworms are an important soil taxon as ecosystem engineers, providing a variety of crucial ecosystem functions and services. Little is known about their diversity and distribution at large spatial scales, despite the availability of considerable amounts of local-scale data. Earthworm diversity data, obtained from the primary literature or provided directly by authors, were collated with information on site locations, including coordinates, habitat cover, and soil properties. Datasets were required, at a minimum, to include abundance or biomass of earthworms at a site. Where possible, site-level species lists were included, as well as the abundance and biomass of individual species and ecological groups. This global dataset contains 10,840 sites, with 184 species, from 60 countries and all continents except Antarctica. The data were obtained from 182 published articles, published between 1973 and 2017, and 17 unpublished datasets. Amalgamating data into a single global database will assist researchers in investigating and answering a wide variety of pressing questions, for example, jointly assessing aboveground and belowground biodiversity distributions and drivers of biodiversity change.
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http://dx.doi.org/10.1038/s41597-021-00912-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8140120PMC
May 2021

Plant-Soil Feedbacks and Temporal Dynamics of Plant Diversity-Productivity Relationships.

Trends Ecol Evol 2021 Jul 20;36(7):651-661. Epub 2021 Apr 20.

Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO- KNAW), Wageningen, The Netherlands; Institute of Biology, Section Plant Ecology and Phytochemistry, Leiden University, 2300, RA, Leiden, The Netherlands.

Plant-soil feedback (PSF) and diversity-productivity relationships are important research fields to study drivers and consequences of changes in plant biodiversity. While studies suggest that positive plant diversity-productivity relationships can be explained by variation in PSF in diverse plant communities, key questions on their temporal relationships remain. Here, we discuss three processes that change PSF over time in diverse plant communities, and their effects on temporal dynamics of diversity-productivity relationships: spatial redistribution and changes in dominance of plant species; phenotypic shifts in plant traits; and dilution of soil pathogens and increase in soil mutualists. Disentangling these processes in plant diversity experiments will yield new insights into how plant diversity-productivity relationships change over time.
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http://dx.doi.org/10.1016/j.tree.2021.03.011DOI Listing
July 2021

Evaluating long-term success in grassland restoration: an ecosystem multifunctionality approach.

Ecol Appl 2021 04 23;31(3):e02271. Epub 2021 Feb 23.

Community Ecology, Swiss Federal Institute for Forest, Snow and Landscape Research (WSL), Birmensdorf, 8903, Switzerland.

It is generally assumed that restoring biodiversity will enhance diversity and ecosystem functioning. However, to date, it has rarely been evaluated whether and how restoration efforts manage to rebuild biodiversity and multiple ecosystem functions (ecosystem multifunctionality) simultaneously. Here, we quantified how three restoration methods of increasing intervention intensity (harvest only < topsoil removal < topsoil removal + propagule addition) affected grassland ecosystem multifunctionality 22 yr after the restoration event. We compared restored with intensively managed and targeted seminatural grasslands based on 13 biotic and abiotic, above- and belowground properties. We found that all three restoration methods improved ecosystem multifunctionality compared to intensively managed grasslands and developed toward the targeted seminatural grasslands. However, whereas higher levels of intervention intensity reached ecosystem multifunctionality of targeted seminatural grasslands after 22 yr, lower intervention missed this target. Moreover, we found that topsoil removal with and without seed addition accelerated the recovery of biotic and aboveground properties, and we found no negative long-term effects on abiotic or belowground properties despite removing the top layer of the soil. We also evaluated which ecosystem properties were the best indicators for restoration success in terms of accuracy and cost efficiency. Overall, we demonstrated that low-cost measures explained relatively more variation of ecosystem multifunctionality compared to high-cost measures. Plant species richness was the most accurate individual property in describing ecosystem multifunctionality, as it accounted for 54% of ecosystem multifunctionality at only 4% of the costs of our comprehensive multifunctionality approach. Plant species richness is the property that typically is used in restoration monitoring by conservation agencies. Vegetation structure, soil carbon storage and water-holding capacity together explained 70% of ecosystem multifunctionality at only twice the costs (8%) of plant species richness, which is, in our opinion, worth considering in future restoration monitoring projects. Hence, our findings provide a guideline for land managers how they could obtain an accurate estimate of aboveground-belowground ecosystem multifunctionality and restoration success in a highly cost-efficient way.
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http://dx.doi.org/10.1002/eap.2271DOI Listing
April 2021

Globally, plant-soil feedbacks are weak predictors of plant abundance.

Ecol Evol 2021 Feb 27;11(4):1756-1768. Epub 2021 Jan 27.

Department of Biology University of British Columbia Kelowna BC Canada.

Plant-soil feedbacks (PSFs) have been shown to strongly affect plant performance under controlled conditions, and PSFs are thought to have far reaching consequences for plant population dynamics and the structuring of plant communities. However, thus far the relationship between PSF and plant species abundance in the field is not consistent. Here, we synthesize PSF experiments from tropical forests to semiarid grasslands, and test for a positive relationship between plant abundance in the field and PSFs estimated from controlled bioassays. We meta-analyzed results from 22 PSF experiments and found an overall positive correlation (0.12 ≤   ≤ 0.32) between plant abundance in the field and PSFs across plant functional types (herbaceous and woody plants) but also variation by plant functional type. Thus, our analysis provides quantitative support that plant abundance has a general albeit weak positive relationship with PSFs across ecosystems. Overall, our results suggest that harmful soil biota tend to accumulate around and disproportionately impact species that are rare. However, data for the herbaceous species, which are most common in the literature, had no significant abundance-PSFs relationship. Therefore, we conclude that further work is needed within and across biomes, succession stages and plant types, both under controlled and field conditions, while separating PSF effects from other drivers (e.g., herbivory, competition, disturbance) of plant abundance to tease apart the role of soil biota in causing patterns of plant rarity versus commonness.
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http://dx.doi.org/10.1002/ece3.7167DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7882948PMC
February 2021

Community-level interactions between plants and soil biota during range expansion.

J Ecol 2020 Sep 12;108(5):1860-1873. Epub 2020 Jun 12.

Netherlands Institute of Ecology Wageningen The Netherlands.

Plant species that expand their range in response to current climate change will encounter soil communities that may hinder, allow or even facilitate plant performance. It has been shown repeatedly for plant species originating from other continents that these plants are less hampered by soil communities from the new than from the original range. However, information about the interactions between intra-continental range expanders and soil communities is sparse, especially at community level.Here we used a plant-soil feedback experiment approach to examine if the interactions between range expanders and soil communities change during range expansion. We grew communities of range-expanding and native plant species with soil communities originating from the original and new range of range expanders. In these conditioned soils, we determined the composition of fungi and bacteria by high-throughput amplicon sequencing of the ITS region and the 16S rRNA gene respectively. Nematode community composition was determined by microscopy-based morphological identification. Then we tested how these soil communities influence the growth of subsequent communities of range expanders and natives.We found that after the conditioning phase soil bacterial, fungal and nematode communities differed by origin and by conditioning plant communities. Despite differences in bacterial, fungal and nematode communities between original and new range, soil origin did not influence the biomass production of plant communities. Both native and range expanding plant communities produced most above-ground biomass in soils that were conditioned by plant communities distantly related to them. . Communities of range-expanding plant species shape specific soil communities in both original and new range soil. Plant-soil interactions of range expanders in communities can be similar to the ones of their closely related native plant species.
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http://dx.doi.org/10.1111/1365-2745.13409DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7508040PMC
September 2020

Rhizosphere and litter feedbacks to range-expanding plant species and related natives.

J Ecol 2020 Jan 16;108(1):353-365. Epub 2019 Oct 16.

Department of Terrestrial Ecology Netherlands Institute of Ecology (NIOO-KNAW) Wageningen The Netherlands.

Plant-soil feedback (PSF) results from the net legacy effect that plants leave in the composition of soil communities and abiotic soil properties. PSF is induced by the rhizosphere and by litter inputs into the soil, however, we have little understanding of their individual contributions. Here, we examine feedback effects from the rhizosphere of living plants, decomposing litter and their combination.We used four pairs of climate warming-induced range-expanding plant species and congeneric natives, and examined PSF effects on plant biomass production, as well as on decomposition in their new range.We tested the hypothesis that the plant rhizosphere provides less negative feedback to range-expanders than to the congeneric natives, and that feedback mediated by litter decomposition does not provide such a difference because decomposers might be less specialized than pathogens. To determine PSF, we used soil from the congener species within each pair as an 'away' soil to indicate whether range-expanders may have lost their specialized soil biota upon arrival in the novel range.Our results show that although range-expanding plant species and their congeneric natives developed neutral PSF in both rhizosphere- and litter-conditioned soils, two of the four range-expanders produced more biomass than natives in soils conditioned by litter, that is, soils with high nutrient content. Shoot litter from two out of four range-expanding species decomposed more than that of natives, but decomposition was unaffected by soil conditioning. . We compared PSF effects of range-expanders and congeneric natives mediated via both the rhizosphere and litter using the congeneric species as a control. Under those conditions, PSF effects were neutral and not affected by plant origin. Therefore, we conclude that studies not comparing within plant genera may overestimate the impact of plant origin on PSF. Still, even under those conditions range-expanders appeared to benefit more from high soil nutrient availability than natives, thus providing a possible advantage over congeneric natives.
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http://dx.doi.org/10.1111/1365-2745.13299DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7363160PMC
January 2020

Quantitative comparison between the rhizosphere effect of Arabidopsis thaliana and co-occurring plant species with a longer life history.

ISME J 2020 10 8;14(10):2433-2448. Epub 2020 Jul 8.

Department of Plant Sciences, Laboratory of Molecular Biology, Wageningen University, Droevendaalsesteeg 1, 6708 PB, Wageningen, The Netherlands.

As a model for genetic studies, Arabidopsis thaliana (Arabidopsis) offers great potential to unravel plant genome-related mechanisms that shape the root microbiome. However, the fugitive life history of this species might have evolved at the expense of investing in capacity to steer an extensive rhizosphere effect. To determine whether the rhizosphere effect of Arabidopsis is different from other plant species that have a less fugitive life history, we compared the root microbiome of Arabidopsis to eight other, later succession plant species from the same habitat. The study included molecular analysis of soil, rhizosphere, and endorhizosphere microbiome both from the field and from a laboratory experiment. Molecular analysis revealed that the rhizosphere effect (as quantified by the number of enriched and depleted bacterial taxa) was ~35% lower than the average of the other eight species. Nevertheless, there are numerous microbial taxa differentially abundant between soil and rhizosphere, and they represent for a large part the rhizosphere effects of the other plants. In the case of fungal taxa, the number of differentially abundant taxa in the Arabidopsis rhizosphere is 10% of the other species' average. In the plant endorhizosphere, which is generally more selective, the rhizosphere effect of Arabidopsis is comparable to other species, both for bacterial and fungal taxa. Taken together, our data imply that the rhizosphere effect of the Arabidopsis is smaller in the rhizosphere, but equal in the endorhizosphere when compared to plant species with a less fugitive life history.
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http://dx.doi.org/10.1038/s41396-020-0695-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7490400PMC
October 2020

Phylogenetic signals and predictability in plant-soil feedbacks.

New Phytol 2020 11 31;228(4):1440-1449. Epub 2020 Jul 31.

Institute for Applied Ecology, University of Canberra, Canberra, ACT, 2617, Australia.

There is strong evidence for a phylogenetic signal in the degree to which species share co-evolved biotic partners and in the outcomes of biotic interactions. This implies there should be a phylogenetic signal in the outcome of feedbacks between plants and the soil microbiota they cultivate. However, attempts to identify a phylogenetic signal in plant-soil feedbacks have produced mixed results. Here we clarify how phylogenetic signals could arise in plant-soil feedbacks and use a recent compilation of data from feedback experiments to identify: whether there is a phylogenetic signal in the outcome of plant-soil feedbacks; and whether any signal arises through directional or divergent changes in feedback outcomes with evolutionary time. We find strong evidence for a divergent phylogenetic signal in feedback outcomes. Distantly related plant species show more divergent responses to each other's soil microbiota compared with closely related plant species. The pattern of divergence implies occasional co-evolutionary shifts in how plants interact with soil microbiota, with strongly contrasting feedback responses among some plant lineages. Our results highlight that it is difficult to predict feedback outcomes from phylogeny alone, other than to say that more closely related species tend to have more similar responses.
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http://dx.doi.org/10.1111/nph.16768DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7689780PMC
November 2020

The long-term restoration of ecosystem complexity.

Nat Ecol Evol 2020 05 13;4(5):676-685. Epub 2020 Apr 13.

Centre for Biodiversity Theory and Modelling, Theoretical and Experimental Ecology Station, CNRS, 2 route du CNRS, Moulis, France.

Multiple large-scale restoration strategies are emerging globally to counteract ecosystem degradation and biodiversity loss. However, restoration often remains insufficient to offset that loss. To address this challenge, we propose to focus restoration science on the long-term (centuries to millennia) re-assembly of degraded ecosystem complexity integrating interaction network and evolutionary potential approaches. This approach provides insights into eco-evolutionary feedbacks determining the structure, functioning and stability of recovering ecosystems. Eco-evolutionary feedbacks may help to understand changes in the adaptive potential after disturbance of metacommunity hub species with core structural and functional roles for their use in restoration. Those changes can be studied combining a restoration genomics approach based on whole-genome sequencing with replicated space-for-time substitutions linking changes in genetic variation to functions or traits relevant to the establishment of evolutionarily resilient communities. This approach may set the knowledge basis for future tools to accelerate the restoration of ecosystems able to adapt to ongoing global changes.
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http://dx.doi.org/10.1038/s41559-020-1154-1DOI Listing
May 2020

A global database of soil nematode abundance and functional group composition.

Sci Data 2020 03 26;7(1):103. Epub 2020 Mar 26.

J. F. Blumenbach Institute of Zoology and Anthropology, University of Göttingen, Göttingen, Germany.

As the most abundant animals on earth, nematodes are a dominant component of the soil community. They play critical roles in regulating biogeochemical cycles and vegetation dynamics within and across landscapes and are an indicator of soil biological activity. Here, we present a comprehensive global dataset of soil nematode abundance and functional group composition. This dataset includes 6,825 georeferenced soil samples from all continents and biomes. For geospatial mapping purposes these samples are aggregated into 1,933 unique 1-km pixels, each of which is linked to 73 global environmental covariate data layers. Altogether, this dataset can help to gain insight into the spatial distribution patterns of soil nematode abundance and community composition, and the environmental drivers shaping these patterns.
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http://dx.doi.org/10.1038/s41597-020-0437-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7099023PMC
March 2020

Soil functional responses to drought under range-expanding and native plant communities.

Funct Ecol 2019 Dec 12;33(12):2402-2416. Epub 2019 Sep 12.

Department of Terrestrial Ecology Netherlands Institute of Ecology (NIOO-KNAW) Wageningen The Netherlands.

Current climate warming enables plant species and soil organisms to expand their range to higher latitudes and altitudes. At the same time, climate change increases the incidence of extreme weather events such as drought. While it is expected that plants and soil organisms originating from the south are better able to cope with drought, little is known about the consequences of their range shifts on soil functioning under drought events.Here, we test how range-expanding plant species and soil communities may influence soil functioning under drought. We performed a full-factorial outdoor mesocosm experiment with plant communities of range expanders or related natives, with soil inocula from the novel or the original range, with or without summer drought. We measured litter decomposition, carbon mineralization and enzyme activities, substrate-induced respiration and the relative abundance of soil saprophytic fungi immediately after drought and at 6 and 12 weeks after rewetting.Drought decreased all soil functions regardless of plant and soil origin except one; soil respiration was less reduced in soils of range-expanding plant communities, suggesting stronger resistance to drought. After rewetting, soil functioning responses depended on plant and soil origin. Soils of native plant communities with a history of drought had more litter mass loss and higher relative abundance of saprophytic fungi than soils without drought and soils of range expanders. Functions of soil from range expanders recovered in a more conservative manner than soils of natives, as litter mass loss did not exceed the control rates. At the end of the experiment, after rewetting, most soil functions in mesocosms with drought history did not differ anymore from the control.We conclude that functional consequences of range-expanding plants and soil biota may interact with effects of drought and that these effects are most prominent during the first weeks after rewetting of the soil. A free http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13453/suppinfo can be found within the Supporting Information of this article.
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http://dx.doi.org/10.1111/1365-2435.13453DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6919305PMC
December 2019

Climate change effects on plant-soil feedbacks and consequences for biodiversity and functioning of terrestrial ecosystems.

Sci Adv 2019 11 27;5(11):eaaz1834. Epub 2019 Nov 27.

Department of Terrestrial Ecology, Netherlands Institute of Ecology, Post Office Box 50, 6700 AB Wageningen, Netherlands.

Plant-soil feedbacks (PSFs) are interactions among plants, soil organisms, and abiotic soil conditions that influence plant performance, plant species diversity, and community structure, ultimately driving ecosystem processes. We review how climate change will alter PSFs and their potential consequences for ecosystem functioning. Climate change influences PSFs through the performance of interacting species and altered community composition resulting from changes in species distributions. Climate change thus affects plant inputs into the soil subsystem via litter and rhizodeposits and alters the composition of the living plant roots with which mutualistic symbionts, decomposers, and their natural enemies interact. Many of these plant-soil interactions are species-specific and are greatly affected by temperature, moisture, and other climate-related factors. We make a number of predictions concerning climate change effects on PSFs and consequences for vegetation-soil-climate feedbacks while acknowledging that they may be context-dependent, spatially heterogeneous, and temporally variable.
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http://dx.doi.org/10.1126/sciadv.aaz1834DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6881159PMC
November 2019

Towards an integrative understanding of soil biodiversity.

Biol Rev Camb Philos Soc 2020 04 15;95(2):350-364. Epub 2019 Nov 15.

Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, Uusimaa, Finland.

Soil is one of the most biodiverse terrestrial habitats. Yet, we lack an integrative conceptual framework for understanding the patterns and mechanisms driving soil biodiversity. One of the underlying reasons for our poor understanding of soil biodiversity patterns relates to whether key biodiversity theories (historically developed for aboveground and aquatic organisms) are applicable to patterns of soil biodiversity. Here, we present a systematic literature review to investigate whether and how key biodiversity theories (species-energy relationship, theory of island biogeography, metacommunity theory, niche theory and neutral theory) can explain observed patterns of soil biodiversity. We then discuss two spatial compartments nested within soil at which biodiversity theories can be applied to acknowledge the scale-dependent nature of soil biodiversity.
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http://dx.doi.org/10.1111/brv.12567DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7078968PMC
April 2020

Global distribution of earthworm diversity.

Science 2019 10;366(6464):480-485

Asian School of the Environment, Nanyang Technological University, 639798 Singapore.

Soil organisms, including earthworms, are a key component of terrestrial ecosystems. However, little is known about their diversity, their distribution, and the threats affecting them. We compiled a global dataset of sampled earthworm communities from 6928 sites in 57 countries as a basis for predicting patterns in earthworm diversity, abundance, and biomass. We found that local species richness and abundance typically peaked at higher latitudes, displaying patterns opposite to those observed in aboveground organisms. However, high species dissimilarity across tropical locations may cause diversity across the entirety of the tropics to be higher than elsewhere. Climate variables were found to be more important in shaping earthworm communities than soil properties or habitat cover. These findings suggest that climate change may have serious implications for earthworm communities and for the functions they provide.
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http://dx.doi.org/10.1126/science.aax4851DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7335308PMC
October 2019

Challenges and Opportunities for Soil Biodiversity in the Anthropocene.

Curr Biol 2019 10;29(19):R1036-R1044

Department of Terrestrial Ecology, Netherlands Institute of Ecology, 6708 PB Wageningen, The Netherlands; Laboratory of Nematology, Wageningen University and Research, P.O. Box 8123, 6700 ES, Wageningen, The Netherlands.

Biodiversity on Earth is strongly affected by human alterations to the environment. The majority of studies have considered aboveground biodiversity, yet little is known about whether biodiversity changes belowground follow the same patterns as those observed aboveground. It is now established that communities of soil biota have been substantially altered by direct human activities such as soil sealing, agricultural land-use intensification, and biological invasions resulting from the introduction of non-native species. In addition, altered abiotic conditions resulting from climate change have also impacted soil biodiversity. These changes in soil biodiversity can alter ecosystem functions performed by the soil biota, and therefore, human-induced global changes have a feedback effect on ecosystem services via altered soil biodiversity. Here, we highlight the major phenomena that threaten soil biodiversity, and we propose options to reverse the decline in soil biodiversity. We argue that it is essential to protect soil biodiversity as a rich reservoir that provides insurance against the changes wrought by the Anthropocene. Overall, we need to better understand the determinants of soil biodiversity and how they function, plan to avoid further losses, and restore soil biodiversity where possible. Safeguarding this rich biotic reservoir is essential for soil sustainability and, ultimately, the sustainability of human society.
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http://dx.doi.org/10.1016/j.cub.2019.08.007DOI Listing
October 2019

Soil fauna diversity increases CO but suppresses N O emissions from soil.

Glob Chang Biol 2020 03 4;26(3):1886-1898. Epub 2019 Nov 4.

Soil Biology Group, Wageningen University, Wageningen, The Netherlands.

Soil faunal activity can be a major control of greenhouse gas (GHG) emissions from soil. Effects of single faunal species, genera or families have been investigated, but it is unknown how soil fauna diversity may influence emissions of both carbon dioxide (CO , end product of decomposition of organic matter) and nitrous oxide (N O, an intermediate product of N transformation processes, in particular denitrification). Here, we studied how CO and N O emissions are affected by species and species mixtures of up to eight species of detritivorous/fungivorous soil fauna from four different taxonomic groups (earthworms, potworms, mites, springtails) using a microcosm set-up. We found that higher species richness and increased functional dissimilarity of species mixtures led to increased faunal-induced CO emission (up to 10%), but decreased N O emission (up to 62%). Large ecosystem engineers such as earthworms were key drivers of both CO and N O emissions. Interestingly, increased biodiversity of other soil fauna in the presence of earthworms decreased faunal-induced N O emission despite enhanced C cycling. We conclude that higher soil fauna functional diversity enhanced the intensity of belowground processes, leading to more complete litter decomposition and increased CO emission, but concurrently also resulting in more complete denitrification and reduced N O emission. Our results suggest that increased soil fauna species diversity has the potential to mitigate emissions of N O from soil ecosystems. Given the loss of soil biodiversity in managed soils, our findings call for adoption of management practices that enhance soil biodiversity and stimulate a functionally diverse faunal community to reduce N O emissions from managed soils.
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http://dx.doi.org/10.1111/gcb.14860DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7078878PMC
March 2020

Microbial invasions in terrestrial ecosystems.

Nat Rev Microbiol 2019 10 26;17(10):621-631. Epub 2019 Jul 26.

Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands.

Human travel and global trade have tremendously increased the spread of invasive microorganisms in new regions. Experimental and observational studies in terrestrial ecosystems are beginning to shed light on processes of microbial invasions, their ecological impacts and implications for ecosystem functioning. We provide examples of terrestrial invasive microorganisms, including bacteria, fungi, oomycetes and other protists, and viruses, and discuss the impacts of pathogenic and non-pathogenic invasive microorganisms at levels ranging from host species to ecosystems. This Review highlights that despite the recent progress in microbial invasion research, we are only beginning to understand how alien microorganisms interact with native microorganisms, and the implications of those interactions. Finally, we propose three research themes - microbial interactions, impacts and climate change - to make microbial invasion research a truly integrative discipline.
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http://dx.doi.org/10.1038/s41579-019-0236-zDOI Listing
October 2019

Single introductions of soil biota and plants generate long-term legacies in soil and plant community assembly.

Ecol Lett 2019 Jul 24;22(7):1145-1151. Epub 2019 Apr 24.

Netherlands Institute of Ecology (NIOO-KNAW), Department of Terrestrial Ecology, P.O. Box 50, 6700 AB, Wageningen, the Netherlands.

Recent demonstrations of the role of plant-soil biota interactions have challenged the conventional view that vegetation changes are mainly driven by changing abiotic conditions. However, while this concept has been validated under natural conditions, our understanding of the long-term consequences of plant-soil interactions for above-belowground community assembly is restricted to mathematical and conceptual model projections. Here, we demonstrate experimentally that one-time additions of soil biota and plant seeds alter soil-borne nematode and plant community composition in semi-natural grassland for 20 years. Over time, aboveground and belowground community composition became increasingly correlated, suggesting an increasing connectedness of soil biota and plants. We conclude that the initial composition of not only plant communities, but also soil communities has a long-lasting impact on the trajectory of community assembly.
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http://dx.doi.org/10.1111/ele.13271DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6850328PMC
July 2019

Latitudinal variation in soil nematode communities under climate warming-related range-expanding and native plants.

Glob Chang Biol 2019 08 20;25(8):2714-2726. Epub 2019 May 20.

Netherlands Institute of Ecology, Wageningen, The Netherlands.

Current climate change has led to latitudinal and altitudinal range expansions of numerous species. During such range expansions, plant species are expected to experience changes in interactions with other organisms, especially with belowground biota that have a limited dispersal capacity. Nematodes form a key component of the belowground food web as they include bacterivores, fungivores, omnivores and root herbivores. However, their community composition under climate change-driven intracontinental range-expanding plants has been studied almost exclusively under controlled conditions, whereas little is known about actual patterns in the field. Here, we use novel molecular sequencing techniques combined with morphological quantification in order to examine nematode communities in the rhizospheres of four range-expanding and four congeneric native species along a 2,000 km latitudinal transect from South-Eastern to North-Western Europe. We tested the hypotheses that latitudinal shifts in nematode community composition are stronger in range-expanding plant species than in congeneric natives and that in their new range, range-expanding plant species accumulate fewest root-feeding nematodes. Our results show latitudinal variation in nematode community composition of both range expanders and native plant species, while operational taxonomic unit richness remained the same across ranges. Therefore, range-expanding plant species face different nematode communities at higher latitudes, but this is also the case for widespread native plant species. Only one of the four range-expanding plant species showed a stronger shift in nematode community composition than its congeneric native and accumulated fewer root-feeding nematodes in its new range. We conclude that variation in nematode community composition with increasing latitude occurs for both range-expanding and native plant species and that some range-expanding plant species may become released from root-feeding nematodes in the new range.
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http://dx.doi.org/10.1111/gcb.14657DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6617783PMC
August 2019

Root traits and belowground herbivores relate to plant-soil feedback variation among congeners.

Nat Commun 2019 04 5;10(1):1564. Epub 2019 Apr 5.

Laboratory of Nematology, Wageningen University, PO Box 8123, Droevendaalsesteeg, 16700 ES, Wageningen, The Netherlands.

Plant-soil feedbacks contribute to vegetation dynamics by species-specific interactions between plants and soil biota. Variation in plant-soil feedbacks can be predicted by root traits, successional position, and plant nativeness. However, it is unknown whether closely related plant species develop more similar plant-soil feedbacks than more distantly related species. Where previous comparisons included plant species from distant phylogenetic positions, we studied plant-soil feedbacks of congeneric species. Using eight intra-continentally range-expanding and native Geranium species, we tested relations between phylogenetic distances, chemical and structural root traits, root microbiomes, and plant-soil feedbacks. We show that root chemistry and specific root length better predict bacterial and fungal community composition than phylogenetic distance. Negative plant-soil feedback strength correlates with root-feeding nematode numbers, whereas microbiome dissimilarity, nativeness, or phylogeny does not predict plant-soil feedbacks. We conclude that root microbiome variation among congeners is best explained by root traits, and that root-feeding nematode abundances predict plant-soil feedbacks.
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http://dx.doi.org/10.1038/s41467-019-09615-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6450911PMC
April 2019

Belowground Consequences of Intracontinental Range-Expanding Plants and Related Natives in Novel Environments.

Front Microbiol 2019 18;10:505. Epub 2019 Mar 18.

Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, Netherlands.

Introduced exotic plant species that originate from other continents are known to alter soil microbial community composition and nutrient cycling. Plant species that expand range to higher latitudes and altitudes as a consequence of current climate warming might as well affect the composition and functioning of native soil communities in their new range. However, the functional consequences of plant origin have been poorly studied in the case of plant range shifts. Here, we determined rhizosphere bacterial communities of four intracontinental range-expanding plant species in comparison with their four congeneric natives grown in soils collected from underneath those plant species in the field and in soils that are novel to them. We show that, when controlling for both species relatedness and soil characteristics, range-expanding plant species in higher latitude ecosystems will influence soil bacterial community composition and nutrient cycling in a manner similar to congeneric related native species. Our results highlight the importance to include phylogenetically controlled comparisons to disentangle the effect of origin from the effect of contrasting plant traits in the context of exotic plant species.
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http://dx.doi.org/10.3389/fmicb.2019.00505DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6431654PMC
March 2019

Range-expansion effects on the belowground plant microbiome.

Nat Ecol Evol 2019 04 25;3(4):604-611. Epub 2019 Mar 25.

Netherlands Institute of Ecology, Wageningen, the Netherlands.

Plant range expansion is occurring at a rapid pace, largely in response to human-induced climate warming. Although the movement of plants along latitudinal and altitudinal gradients is well-documented, effects on belowground microbial communities remain largely unknown. Furthermore, for range expansion, not all plant species are equal: in a new range, the relatedness between range-expanding plant species and native flora can influence plant-microorganism interactions. Here we use a latitudinal gradient spanning 3,000 km across Europe to examine bacterial and fungal communities in the rhizosphere and surrounding soils of range-expanding plant species. We selected range-expanding plants with and without congeneric native species in the new range and, as a control, the congeneric native species, totalling 382 plant individuals collected across Europe. In general, the status of a plant as a range-expanding plant was a weak predictor of the composition of bacterial and fungal communities. However, microbial communities of range-expanding plant species became more similar to each other further from their original range. Range-expanding plants that were unrelated to the native community also experienced a decrease in the ratio of plant pathogens to symbionts, giving weak support to the enemy release hypothesis. Even at a continental scale, the effects of plant range expansion on the belowground microbiome are detectable, although changes to specific taxa remain difficult to decipher.
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http://dx.doi.org/10.1038/s41559-019-0828-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6443080PMC
April 2019

Competition and predation as possible causes of bacterial rarity.

Environ Microbiol 2019 04 18;21(4):1356-1368. Epub 2019 Mar 18.

Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), P.O. Box 50, 6700 AB, Wageningen, The Netherlands.

We assembled communities of bacteria and exposed them to different nutrient concentrations with or without predation by protists. Taxa that were rare in the field were less abundant at low nutrient concentrations than common taxa, independent of predation. However, some taxa that were rare in the field became highly abundant in the assembled communities, especially under ample nutrient availability. This high abundance points at a possible competitive advantage of some rare bacterial taxa under nutrient-rich conditions. In contrast, the abundance of most rare bacterial taxa decreased at low resource availability. Since low resource availability will be the prevailing situation in most soils, our data suggests that under those conditions poor competitiveness for limiting resources may contribute to bacterial rarity. Interestingly, taxa that were rare in the field and most successful under predator-free conditions in the lab also tended to be more reduced by predation than common taxa. This suggests that predation contributes to rarity of bacterial taxa in the field. We further discuss whether there may be a trade-off between competitiveness and predation resistance. The substantial variability among taxa in their responses to competition and predation suggests that other factors, for example abiotic conditions and dispersal ability, also influence the local abundance of soil bacteria.
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http://dx.doi.org/10.1111/1462-2920.14569DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6850713PMC
April 2019

Cultivation-success of rare soil bacteria is not influenced by incubation time and growth medium.

PLoS One 2019 10;14(1):e0210073. Epub 2019 Jan 10.

Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands.

Rare bacterial species have recently attracted interest due to their many potential beneficial functions. However, only little is known about their cultivability. In this study we test the hypotheses that the use of flow cell-sorting for cultivation results in a high proportion of rare soil bacterial isolates relative to bacterial taxa that are abundant in soil. Moreover, we investigate whether different oligotrophic cultivation media and a prolonged incubation time increase the number of cultivated rare species. In a cultivation study we used flow cell sorting to select for small cells and to separate single cells, and grew bacteria on different oligotrophic media with prolonged incubation times. The abundance of the isolates in the field was assessed by comparing them to a 454-sequencing dataset from the same soil. Consequentially, all bacterial isolates were classified as either rare (<0.01% relative abundance) or abundant (>0.01% relative abundance) in the field soil. We found more bacterial taxa among the isolates that were abundant in soil than would be expected by the proportion of abundant species in the field. Neither incubation time nor growth medium had an influence on the recovery of rare species. However, we did find differences in time until visible growth on the plate between different phylogenetic classes of the isolates. These results indicate that rare cultivable species are active and not more likely to be dormant than abundant species, as has been suggested as a reason for their rarity. Moreover, future studies should be aware of the influence incubation time might have on the phylogenetic composition of the isolate collection.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0210073PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6328151PMC
September 2019

Ecological Intensification: Bridging the Gap between Science and Practice.

Trends Ecol Evol 2019 02 30;34(2):154-166. Epub 2018 Nov 30.

Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, The Netherlands; Laboratory of Nematology, Wageningen University and Research, Wageningen, The Netherlands.

There is worldwide concern about the environmental costs of conventional intensification of agriculture. Growing evidence suggests that ecological intensification of mainstream farming can safeguard food production, with accompanying environmental benefits; however, the approach is rarely adopted by farmers. Our review of the evidence for replacing external inputs with ecosystem services shows that scientists tend to focus on processes (e.g., pollination) rather than outcomes (e.g., profits), and express benefits at spatio-temporal scales that are not always relevant to farmers. This results in mismatches in perceived benefits of ecological intensification between scientists and farmers, which hinders its uptake. We provide recommendations for overcoming these mismatches and highlight important additional factors driving uptake of nature-based management practices, such as social acceptability of farming.
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http://dx.doi.org/10.1016/j.tree.2018.11.002DOI Listing
February 2019

Nematode community responses to range-expanding and native plant communities in original and new range soils.

Ecol Evol 2018 Oct 2;8(20):10288-10297. Epub 2018 Oct 2.

Department of Terrestrial Ecology Netherlands Institute of Ecology (NIOO-KNAW) Wageningen The Netherlands.

Many plant species expand their range to higher latitudes in response to climate change. However, it is poorly understood how biotic interactions in the new range differ from interactions in the original range. Here, in a mesocosm experiment, we analyze nematode community responses in original and new range soils to plant communities with either (a) species native in both the original and new range, (b) range-expanding species related to these natives (related range expanders), or (c) range expanders without native congeneric species in the new range (unrelated range expanders). We hypothesized that nematode community shifts between ranges are strongest for unrelated range expanders and minimal for plant species that are native in both ranges. As a part of these community shifts, we hypothesized that range expanders, but not natives, would accumulate fewer root-feeding nematodes in their new range compared to their original range. Analyses of responses of nematodes from both original and new ranges and comparison between range expanders with and without close relatives have not been made before. Our study reveals that none of the plant communities experienced evident nematode community shifts between the original and new range. However, in soils from the new range, root-feeding nematode communities of natives and related range expanders were more similar than in soils from the original range, whereas the nematode community of unrelated range expanders was distinct from the communities of natives and related range expanders in soils from both ranges. The abundances of root-feeding nematodes were comparable between the original and new range for all plant communities. Unexpectedly, unrelated range expanders overall accumulated most root-feeding nematodes, whereas related range expanders accumulated fewest. We conclude that nematode communities associated with native and range-expanding plant species differ between the original and the new range, but that range-expanding plant species do not accumulate fewer root-feeding nematodes in their new than in their original range.
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http://dx.doi.org/10.1002/ece3.4505DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6206179PMC
October 2018

Removal of soil biota alters soil feedback effects on plant growth and defense chemistry.

New Phytol 2019 02 17;221(3):1478-1491. Epub 2018 Oct 17.

Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), PO Box 50, 6700 AB, Wageningen, the Netherlands.

We examined how the removal of soil biota affects plant-soil feedback (PSF) and defense chemistry of Jacobaea vulgaris, an outbreak plant species in Europe containing the defense compounds pyrrolizidine alkaloids (PAs). Macrofauna and mesofauna, as well as fungi and bacteria, were removed size selectively from unplanted soil or soil planted with J. vulgaris exposed or not to above- or belowground insect herbivores. Wet-sieved fractions, using 1000-, 20-, 5- and 0.2-μm mesh sizes, were added to sterilized soil and new plants were grown. Sieving treatments were verified by molecular analysis of the inocula. In the feedback phase, plant biomass was lowest in soils with 1000- and 20-μm inocula, and soils conditioned with plants gave more negative feedback than without plants. Remarkably, part of this negative PSF effect remained present in the 0.2-μm inoculum where no bacteria were present. PA concentration and composition of plants with 1000- or 20-μm inocula differed from those with 5- or 0.2-μm inocula, but only if soils had been conditioned by undamaged plants or plants damaged by aboveground herbivores. These effects correlated with leaf hyperspectral reflectance. We conclude that size-selective removal of soil biota altered PSFs, but that these PSFs were also influenced by herbivory during the conditioning phase.
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http://dx.doi.org/10.1111/nph.15485DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6587519PMC
February 2019

LAESI mass spectrometry imaging as a tool to differentiate the root metabolome of native and range-expanding plant species.

Planta 2018 Dec 23;248(6):1515-1523. Epub 2018 Aug 23.

Netherlands Institute of Ecology (NIOO-KNAW), Droevendaalsesteeg 10, 6708 PB, Wageningen, The Netherlands.

Main Conclusion: LAESI-MSI, an innovative high-throughput technique holds a unique potential for untargeted detection, profiling and spatial localization of metabolites from intact plant samples without need for extraction or extensive sample preparation. Our understanding of chemical diversity in biological samples has greatly improved through recent advances in mass spectrometry (MS). MS-based-imaging (MSI) techniques have further enhanced this by providing spatial information on the distribution of metabolites and their relative abundance. This study aims to employ laser-ablation electrospray ionization (LAESI) MSI as a tool to profile and compare the root metabolome of two pairs of native and range-expanding plant species. It has been proposed that successful range-expanding plant species, like introduced exotic invaders, have a novel, or a more diverse secondary chemistry. Although some tests have been made using aboveground plant materials, tests using root materials are rare. We tested the hypothesis that range-expanding plants possess more diverse root chemistries than native plant species. To examine the root chemistry of the selected plant species, LAESI-MSI was performed in positive ion mode and data were acquired in a mass range of m/z 50-1200 with a spatial resolution of 100 µm. The acquired data were analyzed using in-house scripts, and differences in the spatial profiles were studied for discriminatory mass features. The results revealed clear differences in the metabolite profiles amongst and within both pairs of congeneric plant species, in the form of distinct metabolic fingerprints. The use of ambient conditions and the fact that no sample preparation was required, established LAESI-MSI as an ideal technique for untargeted metabolomics and for direct correlation of the acquired data to the underlying metabolomic complexity present in intact plant samples.
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http://dx.doi.org/10.1007/s00425-018-2989-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6244666PMC
December 2018

Network Analyses Can Advance Above-Belowground Ecology.

Trends Plant Sci 2018 09 30;23(9):759-768. Epub 2018 Jul 30.

Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), P.O. Box 50, 6700 AB, Wageningen, The Netherlands; Laboratory of Nematology, Wageningen University, P.O. Box 8123, 6700 ES, Wageningen, The Netherlands.

An understanding of above-belowground (AG-BG) ecology is important for evaluating how plant interactions with enemies, symbionts, and decomposers affect species diversity and will respond to global changes. However, research questions and experiments often focus on only a limited number of interactions, creating an incomplete picture of how entire communities may be involved in AG-BG community ecology. Therefore, a pressing challenge is to formulate hypotheses of AG-BG interactions when considering communities in their full complexity. Here we discuss how network analyses can be a powerful tool to progress AG-BG research, link across scales from individual to community and ecosystem, visualize community interactions between the two (AG and BG) subsystems, and develop testable hypotheses.
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http://dx.doi.org/10.1016/j.tplants.2018.06.009DOI Listing
September 2018

Relative importance of competition and plant-soil feedback, their synergy, context dependency and implications for coexistence.

Ecol Lett 2018 08 12;21(8):1268-1281. Epub 2018 Jun 12.

Department of Terrestrial Ecology (NIOO-KNAW), Netherlands Institute of Ecology, 6708 PB, Wageningen, the Netherlands.

Plants interact simultaneously with each other and with soil biota, yet the relative importance of competition vs. plant-soil feedback (PSF) on plant performance is poorly understood. Using a meta-analysis of 38 published studies and 150 plant species, we show that effects of interspecific competition (either growing plants with a competitor or singly, or comparing inter- vs. intraspecific competition) and PSF (comparing home vs. away soil, live vs. sterile soil, or control vs. fungicide-treated soil) depended on treatments but were predominantly negative, broadly comparable in magnitude, and additive or synergistic. Stronger competitors experienced more negative PSF than weaker competitors when controlling for density (inter- to intraspecific competition), suggesting that PSF could prevent competitive dominance and promote coexistence. When competition was measured against plants growing singly, the strength of competition overwhelmed PSF, indicating that the relative importance of PSF may depend not only on neighbour identity but also density. We evaluate how competition and PSFs might interact across resource gradients; PSF will likely strengthen competitive interactions in high resource environments and enhance facilitative interactions in low-resource environments. Finally, we provide a framework for filling key knowledge gaps and advancing our understanding of how these biotic interactions influence community structure.
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http://dx.doi.org/10.1111/ele.13093DOI Listing
August 2018