Wim H. van der Putten

Prof. dr. ir. Wim H. van der Putten

Head of department
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Visiting Address

Droevendaalsesteeg 10
6708 PB Wageningen

+31 (0) 317 47 34 00

The Netherlands


I am interested in unraveling how ecological systems respond to changes in biodiversity, climate, and land use. From thereon, my research contributes to the restoration, conservation, and maintenance of biodiversity under climate and land use change.


Wim van der Putten is Head of the Department of Terrestrial Ecology at the Netherlands Institute of Ecology. He graduated at Wageningen University in 1984 and defended his research on 'establishment, growth and degeneration of Ammophila arenaria in coastal foredunes' (performed at the Institute for Ecological Research in Oostvoorne) at Wageningen University in 1989. From 1988 onwards, he was appointed as a Postdoc the institute of Ecology at Heteren. In 1994 he became senior scientist at the department of Plant-Microorganism Interactions and acted as interim head in 1997. In 2000, he became head of the newly established department of Multitrophic Interactions at the Netherlands institute of Ecology (NIOO-KNAW). In September 2003, he was appointed extraordinary professor in Functional Biodiversity at Wageningen University. In 2005, he was awarded a VICI-grant from NWO-ALW (the Dutch research council), and in 2012 he obtained an ERC-Advanced grant from the European Research Council. Currently.

Wim has been associate editor of the Journal of Coastal Research, Plant and Soil, Plant Biology, the Journal of Applied Ecology, Oikos and Oecologia. Currently, he is associate editor of Ecology Letters and Board Reviewing Editor at Science. Since 1992, he has been coordinator of a number of European research projects (EUREED, CLUE, INVASS, EcoTrain), as well as PI in others (TLinks, Biorhiz, Consider, Soilservice, EcoFinders, and Liberation). He has been co-editor of a book on Soil Ecology, as well as on the European Atlas of Soil Biodiversity.

In 2010 he initiated the Wageningen Centre for Soil Ecology (CSE; http://www.soilecology.eu/) and since then he is chairman of the daily board. Aims of this centre are to stimulate utilization of knowledge from fundamental research and to attract and support young researchers in soil ecology. In 2011, he was one of the founders of the Global Soil Biodiversity Initiative (GSBI; http://www.globalsoilbiodiversity.org/) that integrates and disseminates information on the biological status of soils world-wide, a.o. serving as an expert centre for FAO, CBD and other global organizations.

Awards and distinctions

2021 Elected member of Academia Europaea
2020 Marie Curie award to Lilia Serrano
2019 Marie Curie individual grants to Safaa Wasof and Elizabeth Wandrag
2013 Co-author on paper by O. Kostenko et al. Ecology Letters 2012: NERN-prize and PE&RC prize of best paper 2012
2012 ERC-Advanced grant on 'aboveground-belowground community re-assemblages under global warming'
2012 Co-author on paper by T.F.J. van de Voorde et al.: runner-up for John Harper prize from Journal of Ecology
2009 Visiting scientist at Centre for Population Biology, Imperial College at Silwood Park, UK
2008 Co-author on paper by T. Engelkes et al. receiving the NERN-prize 2008
2007 Teachers award Wageningen University
2006 Co-author of paper by R. Soler et al. receiving Charles Elton award from the Journal of Animal Ecology
2005 Co-author of paper by G.B. De Deyn et al. receiving John Harper award from the Journal of Ecology
2004 VICI-award Dutch Research Council for personal innovation
2003/4 Visiting scientist at Landcare Research institute New Zealand
Main research areas

The research of Wim van der Putten has shown how soil-borne pathogens and parasites can drive compositional change in natural vegetation (Nature, 1993). Before that time, the traditional view in ecology was that symbiotic soil biota (mycorrhizal fungi and nitrogen-fixing microbes) and abiotic soil conditions (nutrients, pH, porosity, structure, and water availability) were the main belowground drivers of species composition and productivity of natural vegetation. His breakthrough on the role of soil-borne pathogens has stimulated numerous studies that advance understanding the role of plant-soil feedback interactions in functioning of natural ecosystems. He and coworkers have demonstrated that these feedback interactions promote diversity in plant communities (De Deyn et al. Nature, 2003), which is important information for ecological restoration, and that plant species that successfully shift range under current climate warming have similar properties as invasive species because of escape from aboveground and belowground enemies (Engelkes and Morrien et al. Nature, 2008). He and co-workers showed that extreme weather events may remain as legacy effects in the soil biota thus influencing plant invasiveness (PNAS, 2013). Future breakthroughs are expected to come from his ERC advanced grant (awarded in 2012), which enables him to gain insights in belowground-aboveground community re-assemblage process following climate warming-induced range shifts. These insights will provide fundamental understanding of ecological-evolutionary dynamics in terrestrial communities, which may lead to novel ways of ecosystem management by enhancing adaptation in natural communities to global environmental changes. Wim is also known for his contributions to many conceptual papers, such as on aboveground-belowground interactions (Van der Putten et al. TREE, 2001, Wardle et al. Science, 2004), species range shifts under climate warming (Van der Putten AREES 2012), species gain and loss (Wardle et al. Science, 2011), and belowground biodiversity and ecosystem functioning (Bardgett and Van der Putten Nature, 2014).
Recent books & reports

Jeffery S, Gardi C, Jones A, Montanarella L, Marmo L, Miko L, Ritz K, Peres G, Römbke J. and Van der Putten WH (eds.), 2010, European Atlas of Soil Biodiversity. European Commission, Publications Office of the European Union, Luxembourg. ISBN 978-92-79-15806-3, ISSN 1018-5593, doi 10.2788/94222, 128 pp.

Wall, D.H., Bardgett, R.D., Behan-Pelletier, V., Herrick, J.E., Jones, T.H., Ritz, K., Six, J., Strong, D.R., and van der Putten, W.H. (eds.) 2012. Soil Ecology and Ecosystem Services. Oxford: Oxford University Press.

Turbé, A, De Toni, A, Benito, P, Lavelle, P, Lavelle, P, Ruiz, N, Van der Putten, W.H., Labouze, E, and Mudgal, S. 2010 Soil biodiversity: functions, threats and tools for policy makers. Bio Intelligence Service, IRD, and NIOO, Report for European Commission (DG Environment), Brussels.
Rhizosphere 4 Conference (June 21-25, 2015, Maastricht, The Netherlands)

Management and organization

2017- Member of the RNWT of the KNAW

2016- Review panel KNAW Fund Ecology

2016-2017 Advisory board 2nd Global Soil Biodiversity Conference, Nanjing, China

2016-2018 Chair EASAC Committee on Soils at Risk

2016 Onderwijsprijs (Education prize) 2016 committee KNAW

2016 Evaluation committee environment panel Strategic Alliances Netherlands-China

2014-2017 Technical Chairman VICI committee of Dutch Research Council Life Sciences
2013- Chairman Althof Foundation
2012- Member of Editors group of Global Soil Biodiversity Atlas
2012- Organization committee of Soil Biodiversity symposium (Dijon, 2014)
2012- Member of organization of Rhizosphere 4 conference (Maastricht, 2015)
2012- Chairman De Levende Natuur Foundation
2012- Management team BE-Basic project
2012- Scientific Advisory Committee Gegevensautoriteit (Dutch Authority for Ecological Data)
2011- Member daily board Global Soil Biodiversity Initiative (GSBI)
2011- PI-Management Team Jena Experiment
2010- Chairman daily board Centre for Soil Ecology NIOO-WUR
2010- Scientific Advisory Board Centre for Functional Ecology, University of Coimbra, Portugal
2010- Steering Committee Ecotron CEFE-CNRS Montpellier
2010-2011 Member Knowledge Table SKB
2008-2012 Functional Agro Biodiversity Steering Committee
2006-2008 NWO-ALW VIDI committee
2006-2008 NWO Mozaiek committee (chairman in 2008)
2006-2007 Year Planet Earth Steering Committee
2002-2006 Coordinator EU-Ecotrain
2002-2005 Daily Board EU-TLinks
2002-2011 Replacing Director of Centre for Terrestrial Ecology
1997- NWO-ALW ad hoc selection committees
1997-1999 Coordinator EC-INVASS project
1996-1998 Coordinator EC-CLUE project
1996-1999 Board of the Dutch-Flemish Ecological Society (Secretary)
1994-1995 Coordinator EC-EUREED project
1992 Interim management Bird Ring Department at the Institute for Ecological Research
1989-1991 Coordinator Applied Ecology projects at the Institute for Ecological Research

Research groups


Ancillary activities


Peer-reviewed publications

  • Ecology Letters

    Soil legacy effects of plants and drought on aboveground insects in native and range-expanding plant communities

    Soils contain biotic and abiotic legacies of previous conditions that may influence plant community biomass and associated aboveground biodiversity. However, little is known about the relative strengths and interactions of the various belowground legacies on aboveground plant–insect interactions. We used an outdoor mesocosm experiment to investigate the belowground legacy effects of range-expanding versus native plants, extreme drought and their interactions on plants, aphids and pollinators. We show that plant biomass was influenced more strongly by the previous plant community than by the previous summer drought. Plant communities consisted of four congeneric pairs of natives and range expanders, and their responses were not unanimous. Legacy effects affected the abundance of aphids more strongly than pollinators. We conclude that legacies can be contained as soil ‘memories’ that influence aboveground plant community interactions in the next growing season. These soil-borne ‘memories’ can be altered by climate warming-induced plant range shifts and extreme drought.

  • Science

    Soil biodiversity needs policy without borders

    Wim H. van der Putten, Richard D. Bardgett, Monica Farfan, Luca Montanarella, Johan Six, Diana H. Wall
  • Ecological Monographs

    Temporal dynamics of range-expander and congeneric native plant responses during and after extreme drought events

    Qiang Yang, Ciska Veen, Roel Wagenaar, Marta Manrubia-Freixa, Freddy ten Hooven, Wim H. van der Putten

    Climate change is causing range shifts of many species to higher latitudes and altitudes and increasing their exposure to extreme weather events. It has been shown that range-shifting plant species may perform differently in new soil than related natives; however, little is known about how extreme weather events affect range-expanding plants compared to related natives. In this study we used outdoor mesocosms to study how range-expanding plant species responded to extreme drought in live soil from a habitat in a new range with and without live soil from a habitat in the original range (Hungary). During summer drought, the shoot biomass of the range-expanding plant community declined. In spite of this, in the mixed community, range expanders produced more shoot biomass than congeneric natives. In mesocosms with a history of range expanders in the previous year, native plants produced less biomass. Plant legacy or soil origin effects did not change the response of natives or range expanders to summer drought. During rewetting, range expanders had less biomass than congeneric natives but higher drought resilience (survival) in soils from the new range where in the previous year native plant species had grown. The biomass patterns of the mixed plant communities were dominated by Centaurea spp.; however, not all plant species within the groups of natives and of range expanders showed the general pattern. Drought reduced the litter decomposition, microbial biomass, and abundances of bacterivorous, fungivorous, and carnivorous nematodes. Their abundances recovered during rewetting. There was less microbial and fungal biomass, and there were fewer fungivorous nematodes in soils from the original range where range expanders had grown in the previous year. We concluded that in mixed plant communities of range expanders and congeneric natives, range expanders performed better, under both ambient and drought conditions, than congeneric natives. However, when considering the responses of individual species, we observed variations among pairs of congenerics, so that under the present mixed-community conditions there was no uniformity in responses to drought of range expanders versus congeneric natives. Range-expanding plant species reduced soil fungal biomass and the numbers of soil fungivorous nematodes, suggesting that the effects of range-expanding plant species can trickle up in the soil food web.

  • Plants

    Effects of Light Quality on Colonization of Tomato Roots by AMF and Implications for Growth and Defense

    Haymanti Saha, Nikolaos Kaloterakis, Jeff A. Harvey, Wim H. van der Putten, Arjen Biere

    Beneficial soil microbes can enhance plant growth and defense, but the extent to which this occurs depends on the availability of resources, such as water and nutrients. However, relatively little is known about the role of light quality, which is altered during shading, resulting a low red: far-red ratio (R:FR) of light. We examined how low R:FR light influences arbuscular mycorrhizal fungus (AMF)-mediated changes in plant growth and defense using Solanum lycopersicum (tomato) and the insect herbivore Chrysodeixis chalcites. We also examined effects on third trophic level interactions with the parasitoid Cotesia marginiventris. Under low R:FR light, non-mycorrhizal plants activated the shade avoidance syndrome (SAS), resulting in enhanced biomass production. However, mycorrhizal inoculation decreased stem elongation in shaded plants, thus counteracting the plant’s SAS response to shading. Unexpectedly, activation of SAS under low R:FR light did not increase plant susceptibility to the herbivore in either non-mycorrhizal or mycorrhizal plants. AMF did not significantly affect survival or growth of caterpillars and parasitoids but suppressed herbivore-induced expression of jasmonic acid-signaled defenses genes under low R:FR light. These results highlight the context-dependency of AMF effects on plant growth and defense and the potentially adverse effects of AMF under shading.

  • Biology and Fertility of Soils

    Greenhouse gas (CO2, CH4, and N2O) emissions after abandonment of agriculture, and insights on the response of the (de)nitrifier

    Alaa H.M. El-Hawwary, Kristof Brenzinger, Hyo Jung Lee, Annelies Veraart, Elly Morrien, Michael Schloter, Wim H. van der Putten, Paul Bodelier, Adrian Ho
    The GHG (CO2, CH4, N2O) emission potential along a chronosequence of former agricultural soils abandoned for 9 to 32 years were compared to an actively managed (on-going) agricultural soil (reference). The soils were incubated in mesocosms with and without manure amendment, and microbial functional groups involved in nitrous oxide emission were quantitatively assessed. Carbon dioxide emission significantly increased after agriculture abandonment (< 24 years) consistent with higher decomposition rate, but total emission decreased in the long term (> 29 years). With the cessation of agriculture, the abandoned sites generally became a net methane sink. Notably, total nitrous oxide emission showed a significant monotonic decrease over years of abandonment in response to manure amendment, possibly reflecting an altered capacity for (de)nitrification as indicated in the response of the (de)nitrifier abundance. Overall, our findings suggest that the GHG legacy of agriculture diminishes over time (> 29 years), with lowered GHG emissions and global warming potential (GWP) after abandonment of agriculture.
  • Journal of Applied Ecology

    Long-term recovery of above- and below-ground interactions in restored grasslands after topsoil removal and seed addition

    Monika Carol Resch, Martin Schütz, Raul Ochoa-Hueso, Nina Buchmann, Beat Frey, Ulrich Graf, Wim H. van der Putten, Stephan Zimmermann, Anita C. Risch

    Evaluation of restoration activities is indispensable to assess the extent to which targets have been reached. Usually, the main goal of ecological restoration is to restore biodiversity and ecosystem functioning, but validation is often based on a single indicator, which may or may not cope with whole-ecosystem dynamics. Network analyses are, however, powerful tools, allowing to examine both the recovery of various biotic and abiotic properties and the integrated response at community and ecosystem level. We used restoration sites where topsoil was removed from former intensively managed grassland and seeds were added. These sites were between 3 and 32 years old. We assessed how plants, soil biota, soil properties and correlation-based interactions between biotic communities and their abiotic environment developed over time and compared the results with (i) intensively managed (not restored), and (ii) well-preserved targeted semi-natural grasslands. Plant, nematode, fungal and prokaryotic diversity and community structures of the restored grasslands revealed clear successional patterns and followed similar trajectories towards targeted semi-natural grasslands. All biotic communities reached targeted diversity levels no later than 18 years post-restoration. Ecological networks of intensively managed and short-term (~4 years) restored grasslands were less tightly connected compared to those found in mid- and long-term (~18–30 years) restored and target grasslands. Restoration specifically enhanced interactions among biotic communities, but reduced interactions between biotic communities and their abiotic environment as well as interactions among abiotic properties in the short- and mid-term. Synthesis and applications: Overall, our study demonstrated that topsoil removal and seed addition were successful in restoring diverse, tightly coupled and well-connected biotic communities above- and below-ground similar to those found in the semi-natural grasslands that were restoration targets. Network analyses proved to be powerful in examining the long-term re-establishment of functionally connected biotic communities in restored ecosystems. Thus, we provide an approach to holistically assess restoration activities by notably considering the complexity of ecosystems, much in contrast to most traditional approaches.

  • 2022

    Sustainability tensions and opportunities for aviation biofuel production in Brazil

    Mar Palmeros Parada, Wim H. van der Putten, Luuk A.M. van der Wielen, Patricia Osseweijer, Mark van Loosdrecht, Farahnaz Pashaei Kamali, John A. Posada

    Aviation biofuels are promising to reduce carbon emissions in the aviation sector. However, emerging concerns over biofuels indicate a need for sustainability analyses that take into consideration the context around biofuel production. Here, we present a novel ex-ante sustainability analysis of production alternatives for aviation biofuel in Southeast Brazil. Considering local stakeholders’ concerns, the analysis is focused on climate change, commercial acceptability, efficiency, energy security, investment security, profitability, social development, and soil sustainability. By identifying tensions between production alternatives and these sustainability aspects, we discuss opportunities for further developments, such as sugarcane ethanol-to-jet production in the short term, and in-house production of hydrogen and power with renewable energy. Additionally, producer–operator partnerships and opening the decision-making to stakeholder participation are suggested to stimulate social cohesion, and reconcile diverging interests with biobased production. Analyzing sustainability with consideration of the local context can contribute to identify opportunities for more sustainable decarbonization alternatives.

  • Journal of Environmental Management

    Soil aggregate microbiomes steer plant community overyielding in ungrazed and intensively grazed grassland soils

    Xiliang Li, Zhen Zhang, Xiaotao Lü, Yuanheng Li, Ke Jin, Wim H. van der Putten

    Plant and soil microbial community composition play a central role in maintaining ecosystem functioning. Most studies have focused on soil microbes in the bulk soil, the rhizosphere and inside plant roots, however, less is known about the soil community that exists within soil aggregates, and how these soil communities influence plant biomass production. Here, using field-conditioned soil collected from experimental ungrazed and grazed grasslands in Inner Mongolia, China, we examined the composition of microbiomes inside soil aggregates of various size classes, and determined their roles in plant-soil feedbacks (PSFs), diversity-productivity relationships, and diversity-dependent overyielding. We found that grazing induced significantly positive PSF effects, which appeared to be mediated by mycorrhizal fungi, particularly under plant monocultures. Despite this, non-additive effects of microbiomes within different soil aggregates enhanced the strength of PSF under ungrazed grassland, but decreased PSF strength under intensively grazed grassland. Plant mixture-related increases in PSF effects markedly enhanced diversity-dependent overyielding, primarily due to complementary effects. Selection effects played far less of a role. Our work suggests that PSF contributes to diversity-dependent overyielding in grasslands via non-additive effects of microbiomes within different soil aggregates. The implication of our work is that assessing the effectiveness of sustainable grassland restoration and management on soil properties requires inspection of soil aggregate size-specific microbiomes, as these are relevant determinants of the feedback interactions between soil and plant performance.

  • Molecular Ecology

    Soil microbial diversity and community composition during conversion from conventional to organic agriculture

    Sophie van Rijssel, Ciska Veen, Guusje Koorneef, Tanja Bakx-Schotman, Freddy ten Hooven, Stefan Geisen, Wim H. van der Putten
    It is generally assumed that the dependence of conventional agriculture on artificial fertilizers and pesticides strongly impacts the environment, while organic agriculture relying more on microbial functioning may mitigate these impacts. However, it is not well known how microbial diversity and community composition change in conventionally managed farmers' fields that are converted to organic management. Here, we sequenced bacterial and fungal communities of 34 organic fields on sand and marine clay soils in a time series (chronosequence) covering 25 years of conversion. Nearby conventional fields were used as references. We found that community composition of bacteria and fungi differed between organic and conventionally managed fields. In the organic fields, fungal diversity increased with time since conversion. However, this effect disappeared when the conventional paired fields were included. There was a relationship between pH and soil organic matter content and the diversity and community composition of bacteria and fungi. In marine clay soils, when time since organic management increased, fungal communities in organic fields became more dissimilar to those in conventional fields. We conclude that conversion to organic management in these Dutch farmers' fields did not increase microbial community diversity. Instead, we observed that in organic fields in marine clay when time since conversion increased soil fungal community composition became progressively dissimilar from that in conventional fields. Our results also showed that the paired sampling approach of organic and conventional fields was essential in order to control for environmental variation that was otherwise unaccounted for.
  • Ecological Monographs

    Scientists' warning on climate change and insects

    Jeff A. Harvey, Kévin Tougeron, Rieta Gols, Robin Heinen, Mariana Abarca, Paul K. Abram, Yves Basset, Matty P. Berg, Carol Boggs, Jacques Brodeur, Pedro Cardoso, Jetske G. de Boer, Geert de Snoo, Charl Deacon, Jane E. Dell, Nicolas Desneux, Michael E. Dillon, Grant A. Duffy, Lee A. Dyer, Jacintha Ellers, Anahí Espíndola, James Fordyce, Matthew L. Forister, Caroline Fukushima, Matthew J. G. Gage, Carlos García‐Robledo, Claire Gely, Mauro Gobbi, Caspar A Hallmann, Thierry Hance, John Harte, Axel Hochkirch, Christian Hof, Ary A. Hoffmann, Joel G. Kingsolver, Greg P. A. Lamarre, William F Laurance, Blas Lavandero, Simon R Leather, Philipp Lehmann, Cécile Le Lann, Margarita M. López‐Uribe, Chun‐Sen Ma, Gang Ma, Joffrey Moiroux, Lucie Monticelli, Chris Nice, Paul J. Ode, Sylvain Pincebourde, William J. Ripple, Melissah Rowe, Michael J Samways, Arnaud Sentis, Alisha A. Shah, Nigel Stork, John S. Terblanche, Maddy Thakur, Matthew B. Thomas, Jason M. Tylianakis, Joan Van Baaren, Martijn van de Pol, Wim H. van der Putten, Hans Van Dyck, Wilco C. E. P. Verberk, David L Wagner, Wolfgang W. Weisser, William C. Wetzel, H. Arthur Woods, Kris A G Wyckhuys, Steven L Chown
    Climate warming is considered to be among the most serious of anthropogenicstresses to the environment, because it not only has direct effects on biodiver-sity, but it also exacerbates the harmful effects of other human-mediated threats. The associated consequences are potentially severe, particularly interms of threats to species preservation, as well as in the preservation of anarray of ecosystem services provided by biodiversity. Among the most affectedgroups of animals are insects—central components of many ecosystems—forwhich climate change has pervasive effects from individuals to communities.In this contribution to the scientists’warning series, we summarize the effectof the gradual global surface temperature increase on insects, in terms ofphysiology, behavior, phenology, distribution, and species interactions, as wellas the effect of increased frequency and duration of extreme events such as hotand cold spells, fires, droughts, and floods on these parameters. We warn that,if no action is taken to better understand and reduce the action of climatechange on insects, we will drastically reduce our ability to build a sustainablefuture based on healthy, functional ecosystems. We discuss perspectives onrelevant ways to conserve insects in the face of climate change, and we offerseveral key recommendations on management approaches that can beadopted, on policies that should be pursued, and on the involvement of thegeneral public in the protection effort.
  • ISME Journal

    Microbial storage and its implications for soil ecology

    Kyle Mason-Jones, Serina L. Robinson, Ciska Veen, S. Manzoni, Wim H. van der Putten
    Organisms throughout the tree of life accumulate chemical resources, in particular forms or compartments, to secure their availability for future use. Here we review microbial storage and its ecological significance by assembling several rich but disconnected lines of research in microbiology, biogeochemistry, and the ecology of macroscopic organisms. Evidence is drawn from various systems, but we pay particular attention to soils, where microorganisms play crucial roles in global element cycles. An assembly of genus-level data demonstrates the likely prevalence of storage traits in soil. We provide a theoretical basis for microbial storage ecology by distinguishing a spectrum of storage strategies ranging from surplus storage (storage of abundant resources that are not immediately required) to reserve storage (storage of limited resources at the cost of other metabolic functions). This distinction highlights that microorganisms can invest in storage at times of surplus and under conditions of scarcity. We then align storage with trait-based microbial life-history strategies, leading to the hypothesis that ruderal species, which are adapted to disturbance, rely less on storage than microorganisms adapted to stress or high competition. We explore the implications of storage for soil biogeochemistry, microbial biomass, and element transformations and present a process-based model of intracellular carbon storage. Our model indicates that storage can mitigate against stoichiometric imbalances, thereby enhancing biomass growth and resource-use efficiency in the face of unbalanced resources. Given the central roles of microbes in biogeochemical cycles, we propose that microbial storage may be influential on macroscopic scales, from carbon cycling to ecosystem stability.
  • One Earth

    Ecosystem coupling

    Raul Ochoa-Hueso, Manuel Delgado-Baquerizo, Anita C. Risch, Maarten Schrama, Elly Morrien, S. Henrik Barmentlo, Stefan Geisen, Emilia Hannula, Monika Carol Resch, Basten Snoek, Wim H. van der Putten

    Global change frequently disrupts the connections among species, as well as among species and their environment, before the most obvious impacts can be detected. Therefore, we need to develop a unified conceptual framework that allows us to predict early ecological impacts under changing environments. The concept of coupling, defined as the multiple ways in which the biotic and abiotic components of ecosystems are orderly connected across space and/or time, may provide such a framework. Here, we operationally define the coupling of ecosystems based on a combination of correlational matrices and a null modeling approach. Compared with null models, ecosystems can be (1) coupled; (2) decoupled; and (3) anticoupled. Given that more tightly coupled ecosystems displaying higher levels of internal order may be characterized by a more efficient capture, transfer, and storage of energy and matter (i.e., of functioning), understanding the links between coupling and functioning may help us to accelerate the transition to planetary-scale sustainability. This may be achieved by promoting self-organized order.

  • Journal of Thermal Biology

    Within-patch and edge microclimates vary over a growing season and are amplified during a heatwave: Consequences for ectothermic insects

    R. Gols, L.M. Ojeda-Prieto, Keli Li, Wim H. van der Putten, Jeff A. Harvey

    Embedded in longer term warming are extreme climatic events such as heatwaves and droughts that are increasing in frequency, duration and intensity. Changes in climate attributes such as temperature are often measured over larger spatial scales, whereas environmental conditions to which many small ectothermic arthropods are exposed are largely determined by small-scale local conditions. Exposed edges of plant patches often exhibit significant short-term (daily) variation to abiotic factors due to wind exposure and sun radiation. By contrast, within plant patches, abiotic conditions are generally much more stable and thus less variable. Over an eight-week period in the summer of 2020, including an actual heatwave, we measured small-scale (1 m2) temperature variation in patches of forbs in experimental mesocosms. We found that soil surface temperatures at the edge of the mesocosms were more variable than those within mesocosms. Drought treatment two years earlier, amplified this effect but only at the edges of the mesocosms. Within a plant patch both at the soil surface and within the canopy, the temperature was always lower than the ambient air temperature. The temperature of the soil surface at the edge of a patch may exceed the ambient air temperature when ambient air temperatures rise above 23 °C. This effect progressively increased with ambient temperature. We discuss how microscale-variation in temperature may affect small ectotherms such as insects that have limited ability to thermoregulate, in particular under conditions of extreme heat.

  • Functional Ecology

    Resilience of rhizosphere microbial predators and their prey communities after an extreme heat event

    Maddy Thakur, Wim H. van der Putten, Fariha Apon, Ezio Angelini, Branko Vreš, Stefan Geisen

    1. Climate change is known to disrupt above-ground food chains when the various trophic layers respond differently to warming. However, little is known about below-ground food chains involving microbial preys and their predators. Here, we study how climate warming-induced heat shocks influence resistance (change immediately after a disturbance) and resilience (ability to recover back to pre-disturbance levels) in rhizosphere microbial communities.

    2. We used three species of rhizosphere protists as microbial predators and six different rhizosphere bacterial communities as their prey. Protist species and bacterial communities were extracted from Centaurea stoebe—a range-expanding plant species in the Northern Europe. We then examined the temporal dynamics of protists and bacterial communities after an extreme heat event for several generations with sufficient recovery periods. We hypothesized that bacterial community resistance and resilience after the extreme heat event would be higher particularly when extreme heat effects would negatively affect their predators.

    3. Our results show that prey community biomass was strongly reduced after the extreme heat event and persisted with lower biomass throughout the recovery period. Opposite to what was expected, predators showed negligible changes in their active density after the same heat event. However, abundances of the three predators varied markedly in their temporal dynamics independent of the extreme heat event. Extreme heat event further increased the inactive density of predators, whereas one of the predators showed a decline in its body size owing to extreme heat event. Bacterial community resistance and resilience after the extreme heat event were independent of predator presence, although species-specific effects of predators on bacterial community resilience were different in the last week of recovery. Predator resilience (based on active predator density) also varied among the three predators but converged over time.

    4. Our results highlight that extreme heat events can be more detrimental to microbial prey communities than microbial predators when microbial predators can exhibit thermal acclimation (e.g. change in body size or become inactive) to overcome heat stress. Such thermal acclimation may promote predator resilience after extreme heat events.

  • Ecological Indicators

    Effects of bioavailable phosphorus and soil biota on typical Nardus grassland species in competition with fast-growing plant species

    Stephanie Schelfhout, Safaa Wasof, Jan Mertens, Margot Vanhellemont, Andreas Demey, Annelies Haegeman, Eva DeCock, Iris Moeneclaey, Pieter Vangansbeke, Nicole Viaene, Steve Baeyen, Nancy De Sutter, Martine Maes, Wim H. van der Putten, Kris Verheyen, An De Schrijver

    The restoration of Nardus grasslands is often hampered by high bioavailability of soil phosphorus and disturbed soil communities. In order to better understand these bottlenecks, we studied Nardus grassland species grown together in communities with fast-growing species in 50-liter pots along a gradient of bioavailable phosphorus with or without inoculated soil biota. These mesocosms allowed the plants to freely interact, including competition for light and nutrients. We investigated changes in the plant community composition along the phosphorus gradient using Threshold Indicator Taxa Analysis (TITAN). We found a negative threshold of 11.5 mg POlsen kg−1 with six significant indicator plant species. Above the threshold, a small increase in phosphorus resulted in a disproportionally large drop in biomass for the indicator species, including four typical Nardus grassland species. The decline in these ‘oligotrophic indicator species’ was also linked to increasing plant community biomass, so we suggest the oligotrophic indicator species to be outcompeted for light by fast-growing plant species. We did not find an effect of the soil biota treatment on the biomass of the oligotrophic indicator species, but did observe a positive effect of inoculation with soil biota on the total biomass of the plant community. Interestingly, the threshold for the plant communities in the mesocosm experiment was comparable to the upper bioavailable phosphorus concentrations in remnant Nardus grasslands in northern Belgium. For the restoration of Nardus grasslands, such phosphorus-poor soil conditions appear to be essential, because the plant species that typically occur in these grasslands are able to handle nutrient limitation, but not light limitation.

  • Ecology and Evolution

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

    Kurt O. Reinhart, Jonathan T. Bauer, Sarah McCarthy-Neumann, Andrew S. MacDougall, José L. Hierro, Mariana C. Chiuffo, Scott A. Mangan, Johannes Heinze, Joana Bergmann, Jasmin Joshi, Richard P. Duncan, Jeff M. Diez, Paul Kardol, Gemma Rutten, Markus Fischer, Wim H. van der Putten, T. Martijn Bezemer, John Klironomos

    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 ≤ (Formula presented.) ≤ 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.

  • Soil Biology and Biochemistry

    Optimizing stand density for climate-smart forestry: a way forward towards resilient forests with enhanced carbon storage under extreme climate events

    Frank Sterck, Marleen Vos, Emilia Hannula, Steven de Goede, Wim de Vries, Jan den Ouden, Gert-Jan Nabuurs, Wim H. van der Putten, Ciska Veen
    As a response to the increased pressure of global climate change on most ecosystems, national and international agreements aim at creating forests that are productive, resilient to climate change, and that store carbon to mitigate global warming. However, these aims are being challenged by increased tree mortality rates and decreased tree growth rates in response to increased incidence of extreme drought events. These phenomena make us aware of a lack of crucial insights into the effects of forest management on the growth and survival of trees, and on carbon storage in both trees and forest soils under increased incidence of drought. Here we compile current knowledge on how forest management and drought impact on tree growth and survival, and above- and belowground carbon storage in forest ecosystems. Based on this, we propose that climate-smart forestry may benefit from controlling stand density at intermediate levels (>60%, e.g.∼80%) by applying low levels of tree harvest intensity on a regular base. Furthermore, we propose that the actual optimal density will depend on the tree species, site conditions and management history. As a next step, studies are needed that take an above- and belowground approach and combine forest experiments with mechanistic models on water, carbon and nutrient flows in trees and soils within forests in order to transform current results, which focus on either soil or trees and are often highly-context dependent, to a more generic forest framework. Such a generic framework would be needed to enhance understanding across forest ecosystems on how forest management may promote forest resilience, productivity and carbon storage with increasing drought.
  • New Phytologist

    Severance of arbuscular mycorrhizal fungal mycelial networks in restoration grasslands enhances seedling biomass

    Sigrid Dassen, Wim H. van der Putten, Gerlinde De Deyn

    Establishment and growth of grassland plant species is generally promoted by arbuscular mycorrhizal fungi (AMF) when grown in isolation. However, in grassland communities AMF form networks that may connect individual plants of different ages within and between species. Here, we use an ingrowth core approach to examine how mycorrhizal networks influences performance of seedlings in grasslands. We selected four grass and four forb species with known negative or neutral-positive plant–soil feedback and grew them individually in steel mesh cores filled with living field soil. Cores were placed in six restored grasslands, three grasslands were of relatively young and three were of older successional age. Ingrowing mycorrhizal fungal hyphae were severed twice a week in half of all cores, which resulted into reduced AMF colonization and increased seedling biomass, irrespective of the fields' succession stage, and the plants' grass/forb group, or plant–soil feedback type. In the control cores, root colonization by AMF was negatively correlated to seedling biomass, whereas there was no such relationships in the cores that had been lifted. We conclude that connections to arbuscular mycorrhizal networks of surrounding plants had a negative impact on biomass of establishing forb and grass seedlings.

  • Trends in Ecology and Evolution

    Plant–Soil Feedbacks and Temporal Dynamics of Plant Diversity–Productivity Relationships

    Maddy Thakur, Wim H. van der Putten, Rutger Wilschut, Ciska Veen, Paul Kardol, Jasper van Ruijven, Eric Allan, Christiane Roscher, Mark van Kleunen, T. Martijn Bezemer

    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.

  • Journal of Ecology

    Fungal root endophytes influence plants in a species-specific manner that depends on plant's growth stage

    Stefan Geisen, Freddy ten Hooven, Olga Kostenko, Basten Snoek, Wim H. van der Putten

    The mycobiome (fungal microbiome) influences plants—from seed germination to full maturation. While many studies on fungal-plant interaction studies have focused on known mutualistic and pathogenic fungi, the functional role of ubiquitous endophytic fungi remains little explored. We examined how root-inhabiting fungi (endophytes) influence range-expanding plant species. We isolated endophytes from three European intra-continental range-expanders and three congenerics that are native both in the range expander's original (southern Europe) and new (northern Europe) range. To standardize our collection, endophytes were obtained from all six plant species growing under controlled conditions in northern (new range of the range expander) and southern (native range of the range expander) soils. We cultivated, molecularly identified and tested the effects of all isolates on seed germination, and growth of seedlings and older plants. Most of the 34 isolates could not be functionally characterized based on their taxonomic identity and literature information on functions. Endophytes affected plant growth in a plant species–endophyte-specific manner, but overall differed between range-expanders and natives. While endophytes reduced germination and growth of range-expanders compared to natives, they reduced seedling growth of natives more than of range-expanders. Synthesis. We conclude that endophytic fungi have a direct effect on plant growth in a plant growth stage-dependent manner. While these effects differed between range expanders and natives, the effect strength and significance varied among the plant genera included in the present study. Nevertheless, endophytes likely influence the establishment of newly arriving plants and influence vegetation dynamics.

  • Ecological Applications

    Evaluating long-term success in grassland restoration

    Monika Carol Resch, Martin Schütz, Nina Buchmann, Beat Frey, Ulrich Graf, Wim H. van der Putten, Stephan Zimmermann, Anita C. Risch

    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.

  • Plant and Soil

    Disentangling nematode and arbuscular mycorrhizal fungal community effect on the growth of range-expanding Centaurea stoebe in original and new range soil

    Kadri Koorem, Rutger Wilschut, Carolin Weser, Wim H. van der Putten
    Aims Numerous organisms show range expansions in response to current climate change. Differences in expansion rates, such as between plants and soil biota, may lead to altered interactions in the new compared to the original range. While plant-soil interactions influence plant performance and stress tolerance, the roles of specific soil organisms driving these responses remain unknown.

    Methods We manipulated the abundances of nematodes and arbuscular mycorrhizal fungi (AMF), collected from original and new range soils, and examined their effects on the biomass of range-expanding Centaurea stoebe and native Centaurea jacea. In the first approach, nematode and AMF communities were extracted from field soils, and inoculated to sterilized soil. In the second approach, the abundance of soil organisms in soil inocula was reduced by wet sieving; at first, plants were grown to condition the soil, and then plant-soil feedback was determined under ambient and drought conditions.

    Results The origin of soil communities did not influence the biomass production of range-expanding or native plant species, neither by addition nor by (partial) removal. However, after conditioning and under drought, range expanding C. stoebe produced more biomass with soil communities from the original range while C. jacea, native to both ranges, produced more biomass with new range soil communities.

    Conclusions We show that nematode and AMF communities from original and new range have similar effect on the growth of range expanding C. stoebe. Our results highlight that the effect of soil communities on plant growth increases after soil conditioning and under drought stress.
  • Biofuels, Bioproducts and Biorefining


    Mar Palmeros Parada, Wim H. van der Putten, Luuk A.M. van der Wielen, Patricia Osseweijer, Mark van Loosdrecht, Farahnaz Pashaei Kamali, John A. Posada

    Biobased production has been promoted as an alternative to fossil-based production to mitigate climate change. However, emerging concerns over the sustainability of biobased products have shown that tensions can emerge between different objectives and concerns, like emission reduction targets and food security, and that these are dependent on local contexts. Here we present the Open Sustainability-in-Design (OSiD) framework, the aim of which is to integrate a context-sensitive sustainability analysis in the conceptual design of biobased processes. The framework is illustrated, taking as an example the production of sustainable aviation fuel in southeast Brazil. The OSiD framework is a novel concept that brings the perspectives of stakeholders and considerations of the regional context to an ex ante sustainability analysis of biobased production. This work also illustrates a way to integrate methods from different scientific disciplines supporting the analysis of sustainability and the identification of tensions between different sustainability aspects. Making these tensions explicit early in the development of biobased production can make them more responsive to emerging sustainability concerns. Considering the global pressure to reduce carbon emissions, situating sustainability analyses in their socio-technical contexts as presented here can help to explain and improve the impacts of biobased production in the transition away from fossil resources.

  • Scientific data

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

    Helen R. P. Phillips, Elizabeth M. Bach, Marie L. C. Bartz, Joanne M. Bennett, Rémy Beugnon, Maria J.I. Briones, George Brown, Olga Ferlian, Konstantin B Gongalsky, Carlos A Guerra, Birgitta König-Ries, Julia Krebs, Alberto Orgiazzi, Kelly Ramirez, David J. Russell, Benjamin Schwarz, Diana H. Wall, Ulrich Brose, Thibaud Decaëns, Patrick Lavelle, Michel Loreau, Jérôme Mathieu, Christian Mulder, Wim H. van der Putten, Matthias C Rillig, Maddy Thakur, Franciska T. De Vries, David A. Wardle, Christian Ammer, Sabine Ammer, Miwa Arai, Fredrick O Ayuke, Geoff H Baker, Dilmar Baretta, Dietmar Barkusky, Robin Beauséjour, Jose C. Bedano, Klaus Birkhofer, Eric Blanchart, Bernd Blossey, Thomas Bolger, Robert L Bradley, Michel Brossard, James C. Burtis, Yvan Capowiez, Timothy R. Cavagnaro, Amy Choi, Julia Clause, Daniel Cluzeau, Anja Coors, Felicity V Crotty, Jasmine M. Crumsey, Andrea Dávalos, Darío J.Díaz Cosín, Annise M. Dobson, Anahí Domínguez, Andrés Esteban Duhour, Nick van Eekeren, Christoph Emmerling, Liliana B Falco, Rosa Fernández, Steven J. Fonte, Carlos Fragoso, André L C Franco, Abegail T Fusilero, Anna P. Geraskina, Shaieste Gholami, Grizelle González, Michael J. Gundale, Mónica Gutiérrez López, Branimir K. Hackenberger, Davorka K Hackenberger, Luis M Hernández, Jeff R. Hirth, Takuo Hishi, Andrew R Holdsworth, Martin Holmstrup, Kristine N Hopfensperger, Esperanza Huerta Lwanga, Veikko Huhta, Tunsisa T Hurisso, Basil V Iannone, Madalina Iordache, Ulrich Irmler, Mari Ivask, Juan B. Jesús, Jodi L. Johnson-Maynard, Monika Joschko, Nobuhiro Kaneko, Radoslava Kanianska, Aidan M. Keith, Maria L Kernecker, Armand W Koné, Yahya Kooch, Sanna T Kukkonen, H Lalthanzara, Daniel R Lammel, Iurii M Lebedev, Edith Le Cadre, Noa K Lincoln, Danilo López-Hernández, Scott R Loss, Raphael Marichal, Radim Matula, Yukio Minamiya, Jan Hendrik Moos, Gerardo Moreno, Alejandro Morón-Ríos, Hasegawa Motohiro, Bart Muys, Johan Neirynck, Lindsey Norgrove, Marta Novo, Visa Nuutinen, Victoria Nuzzo, P. Mujeeb Rahman, Johan Pansu, Shishir Paudel, Guénola Pérès, Lorenzo Pérez-Camacho, Jean-François Ponge, Jörg Prietzel, Irina B. Rapoport, Muhammad Imtiaz Rashid, Salvador Rebollo, Miguel Á Rodríguez, Alexander M Roth, Guillaume X Rousseau, Anna Rozen, Ehsan Sayad, Loes van Schaik, Bryant C Scharenbroch, Michael Schirrmann, Olaf Schmidt, Boris Schröder, Julia Seeber, Maxim P Shashkov, Jaswinder Singh, Sandy M Smith, Michael Steinwandter, Katalin Szlavecz, José Antonio Talavera, Dolores Trigo, Jiro Tsukamoto, Sheila Uribe-López, Anne W de Valença, Iñigo Virto, Adrian A Wackett, Matthew W Warren, Emily R. Webster, Nathaniel H Wehr, Joann K Whalen, Michael B Wironen, Volkmar Wolters, Pengfei Wu, Irina V Zenkova, Weixin Zhang, Erin K. Cameron, Nico Eisenhauer

    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.

  • Journal of Ecology

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

    Kadri Koorem, Basten Snoek, Janneke Bloem, Stefan Geisen, Olga Kostenko, Marta Manrubia-Freixa, Kelly Ramirez, Carolin Weser, Rutger Wilschut, Wim H. van der Putten
    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.
    Synthesis. 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.
  • Soil Biology & Biochemistry

    Soil predator loss alters aboveground stoichiometry in a native but not in a related range-expanding plant when exposed to periodic heat waves

    Casper Quist, Wim H. van der Putten, Maddy Thakur
    Increasing frequency and magnitude of climatic extremes, such as heat waves are expected to enhance abiotic stresses on ecological communities. It has been proposed that ecological communities in disturbed habitats may be most sensitive to climatic extremes, as disturbance may reduce density and diversity of higher trophic level organisms like predators. However, there is little experimental evidence that climatic extremes indeed have stronger impact on functioning of such trophically downgraded ecosystems. Here, we experimentally examine how removal of predators from soil communities affects plant performance under periodic heat waves. We used a native plant species, and a congeneric native that is currently expanding its range because of climate change. We used soil nematode communities as the model system, as these are most abundant soil animals and their communities are trophically diverse. Predatory nematodes were manually removed from intact soil nematode communities (mainly the adults as some juveniles are impossible to manually remove) to create a trophically downgraded soil. Intact nematode communities and communities with reduced predatory nematodes were added separately to soils that were planted with either the native Centaurea jacea or the range-expanding congener Centaurea stoebe. Half the experimental units were exposed periodically to experimental heat waves of 10 °C above the control temperature. Our results show that the C: N and C: N: P ratio of plant shoots in predator-reduced soils became lower when exposed to periodic heat waves, however, only in the native plant C. jacea. The decrease in C: N ratio corresponded with increase of an herbivorous nematode in trophically intact soils of C. jacea independent of warming, whereas this relationships disappeared in warmed and predator-reduced soils. Our results accordingly highlight that periodic heat waves may affect stoichiometry of certain plant species by altering trophic interactions in predator-reduced soils.
  • Fungal Ecology

    Rhizosphere fungi actively assimilating plant-derived carbon in a grassland soil

    Emilia Hannula, Elly Morrien, Wim H. van der Putten, Wietse de Boer
    Despite the advantages of the next generation sequencing (NGS) techniques, one of their caveats is that they do not differentiate between microbes that are actively participating in carbon cycling in the rhizosphere and microbes performing other functions in the soils. Here we combined DNA-SIP with NGS to investigate which rhizosphere fungi actively assimilate plant-derived carbon. We provided 13CO2 to plants in intact soil cores collected from a grassland and sampled the rhizosphere in a time series to follow the fate of carbon in the rhizosphere mycobiome. We detected a difference between active rhizosphere fungi using plant-derived carbon and the total mycobiota: 58% of fungal species were using fresh rhizodeposits, and an additional 22% of fungal species received carbon several weeks later while 20% were not involved in cycling of freshly photosynthesized carbon. We show that members of Ascomycota, Mucoromycota, and basidiomycete yeasts were first users of freshly photosynthesized carbon, while fungi not using recently fixed carbon consisted mainly of mycelial (non-yeast) Basidiomycota. We conclude that a majority of fungi inhabiting the rhizosphere in this grassland ecosystem are actively using plant derived carbon either directly or via food-web interactions.
  • Oecologia

    Plant population and soil origin effects on rhizosphere nematode community composition of a range-expanding plant species and a native congener

    Rutger Wilschut, K.J.H. Magnée, Stefan Geisen, Wim H. van der Putten, Olga Kostenko
    Climate change causes species range expansions to higher latitudes and altitudes. It is expected that, due to differences in dispersal abilities between plants and soil biota, range-expanding plant species will become associated with a partly new belowground community in their expanded range. Theory on biological invasions predicts that outside their native range, range-expanding plant species may be released from specialist natural enemies, leading to the evolution of enhanced defence against generalist enemies. Here we tested the hypothesis that expanded range populations of the range-expanding plant species Centaurea stoebe accumulate fewer root-feeding nematodes than populations from the original range. Moreover, we examined whether Centaurea stoebe accumulates fewer root-feeding nematodes in expanded range soil than in original range soil. We grew plants from three expanded range and three original range populations of C. stoebe in soil from the original and from the new range. We compared nematode communities of C. stoebe with those of C. jacea, a congeneric species native to both ranges. Our results show that expanded range populations of C. stoebe did not accumulate fewer root-feeding nematodes than populations from the original range, but that C. stoebe, unlike C. jacea, accumulated fewest root-feeding nematodes in expanded range soil. Moreover, when we examined other nematode feeding groups, we found intra-specific plant population effects on all these groups. We conclude that range-expanding plant populations from the expanded range were not better defended against root-feeding nematodes than populations from the original range, but that C. stoebe might experience partial belowground enemy release.
  • New Phytologist

    Phylogenetic signals and predictability in plant–soil feedbacks

    Elizabeth M. Wandrag, Sarah E. Bates, Luke G. Barrett, Jane A. Catford, Peter H. Thrall, Wim H. van der Putten, Richard P. Duncan
    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.
  • Global Change Biology

    Soil fauna diversity increases CO2 but suppresses N2O emissions from soil

    Ingrid M. Lubbers, Matty P. Berg, Gerlinde De Deyn, Wim H. van der Putten, Jan Willem van Groenigen
    Abstract 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 (CO2, end product of decomposition of organic matter) and nitrous oxide (N2O, an intermediate product of N transformation processes, in particular denitrification). Here, we studied how CO2 and N2O 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 CO2 emission (up to 10%), but decreased N2O emission (up to 62%). Large ecosystem engineers such as earthworms were key drivers of both CO2 and N2O emissions. Interestingly, increased biodiversity of other soil fauna in the presence of earthworms decreased faunal-induced N2O 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 CO2 emission, but concurrently also resulting in more complete denitrification and reduced N2O emission. Our results suggest that increased soil fauna species diversity has the potential to mitigate emissions of N2O 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 N2O emissions from managed soils.
  • ISME Journal

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

    Martinus A. Schneijderberg, Xu Cheng, Carolien Franken, Mattias De Hollander, Robin van Velzen, Lucas Schmitz, Robin Heinen, Rene Geurts, Wim H. van der Putten, T. Martijn Bezemer, Ton Bisseling
    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.
  • Biological Reviews

    Towards an integrative understanding of soil biodiversity

    Maddy Thakur, Helen R. P. Phillips, Ulrich Brose, Franciska T. De Vries, Patrick Lavelle, M. Loreau, J. Mathieu, Christian Mulder, Wim H. van der Putten, Matthias C Rillig, David A. Wardle, Elizabeth M. Bach, Marie L. C. Bartz, Joanne M. Bennett, M.J.I. Briones, George Brown, T. Decaëns, Nico Eisenhauer, Olga Ferlian, Carlos Guerra, Birgitta König-Ries, Alberto Orgiazzi, Kelly Ramirez, David Russell, M. Rutgers, Diana H. Wall, Erin K. Cameron
    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.
  • Nature Ecology and Evolution

    The long-term restoration of ecosystem complexity

    David Moreno Mateos, Antton Alberdi, Elly Morrien, Wim H. van der Putten, Asun Rodríguez-Uña, Daniel Montoya
    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.
  • BioScience

    Distinct Biogeographic Phenomena Require a Specific Terminology: A Reply to Wilson and Sagoff

    Franz Essl, Stefan Dullinger, Piero Genovesi, Philip E. Hulme, Jonathan M Jeschke, Stelios Katsanevakis, Ingolf Kühn, Bernd Lenzner, Aníbal Pauchard, Petr Pyšek, Wolfgang Rabitsch, David M. Richardson, Hanno Seebens, Mark van Kleunen, Wim H. van der Putten, Montserrat Vilà, Sven Bacher
  • Soil Biology & Biochemistry

    Short-term temperature history affects mineralization of fresh litter and extant soil organic matter, irrespective of agricultural management

    Kyle Mason-Jones, Pim Vrehen, Kevin Koper, Jin Wang, Wim H. van der Putten, Ciska Veen
    The influence of temperature on mineralization of plant litter and pre-existing soil organic matter (SOM) involves not only the prevailing temperature, but also how it has changed through time. However, little is known about how temperature variability through time influences mineralization processes. Here, we investigated how short-term temperature history affects the mineralization of SOM and plant litter in soils from different agricultural management systems. We used soils from a long-term experiment with conventional and organic management treatments to set up microcosms. The microcosms were exposed to eight days of contrasting temperature regimes (different mean temperatures and constant versus fluctuating temperatures). Microcosms were then returned to a common temperature of 16 °C, 13C-labelled plant litter was added to half of them, and CO2 efflux was measured over the following week. We found that SOM and litter mineralization were both sensitive to the temperature history, with lower mean temperatures during preliminary treatment associated with higher mineralization during the subsequent common-temperature incubation. This effect persisted through the week after temperature differences were removed. Different patterns of temperature fluctuation and agricultural management did not significantly affect mineralization during common-temperature incubation. The history sensitivity of litter mineralization, despite litter being added after temperature differences had ended, indicates that the temperature history effects may be driven by short-term microbial acclimation. We conclude that organic matter and litter mineralization, which are key processes in the carbon cycle, are sensitive to short-term temperature history. This suggests that future investigations of soil CO2 efflux may need to take recent weather effects into account.
  • Science advances

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

    Francisco I. Pugnaire, Jose A. Morillo, Josep Penuelas, Peter B. Reich, Richard D. Bardgett, Aurora Gaxiola, David A. Wardle, Wim H. van der Putten
    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.
  • Science

    Global distribution of earthworm diversity

    Helen R. P. Phillips, Carlos A Guerra, Marie L. C. Bartz, Maria J.I. Briones, George Brown, Tom Crowther, Olga Ferlian, Konstantin B Gongalsky, Johan van den Hoogen, Julia Krebs, Alberto Orgiazzi, Devin Routh, Benjamin Schwarz, Elizabeth M. Bach, Joanne M. Bennett, Ulrich Brose, Thibaud Decaëns, Birgitta König-Ries, Michel Loreau, Jérôme Mathieu, Christian Mulder, Wim H. van der Putten, Kelly Ramirez, Matthias C Rillig, David Russell, Michiel Rutgers, Maddy Thakur, Franciska T. De Vries, Diana H. Wall, David A. Wardle, Miwa Arai, Fredrick O Ayuke, Geoff H Baker, Robin Beauséjour, José C Bedano, Klaus Birkhofer, Eric Blanchart, Bernd Blossey, Thomas Bolger, Robert L Bradley, Mac A Callaham, Yvan Capowiez, Mark E Caulfield, Amy Choi, Felicity V Crotty, Andrea Dávalos, Darío J Diaz Cosin, Anahí Dominguez, Andrés Esteban Duhour, Nick van Eekeren, Christoph Emmerling, Liliana B Falco, Rosa Fernández, Steven J. Fonte, Carlos Fragoso, André L C Franco, Martine Fugère, Abegail T Fusilero, Shaieste Gholami, Michael J. Gundale, Mónica Gutiérrez López, Davorka K Hackenberger, Luis M Hernández, Takuo Hishi, Andrew R Holdsworth, Martin Holmstrup, Kristine N Hopfensperger, Esperanza Huerta Lwanga, Veikko Huhta, Tunsisa T Hurisso, Basil V Iannone, Madalina Iordache, Monika Joschko, Nobuhiro Kaneko, Radoslava Kanianska, Aidan M. Keith, Courtland A Kelly, Maria L Kernecker, Jonatan Klaminder, Armand W Koné, Yahya Kooch, Sanna T Kukkonen, H Lalthanzara, Daniel R Lammel, Iurii M Lebedev, Yiqing Li, Juan B Jesus Lidon, Noa K Lincoln, Scott R Loss, Raphael Marichal, Radim Matula, Jan Hendrik Moos, Gerardo Moreno, Alejandro Morón-Ríos, Bart Muys, Johan Neirynck, Lindsey Norgrove, Marta Novo, Visa Nuutinen, Victoria Nuzzo, Mujeeb Rahman P, Johan Pansu, Shishir Paudel, Guénola Pérès, Lorenzo Pérez-Camacho, Raúl Piñeiro, Jean-François Ponge, Muhammad Imtiaz Rashid, Salvador Rebollo, Javier Rodeiro-Iglesias, Miguel Á Rodríguez, Alexander M Roth, Guillaume X Rousseau, Anna Rozen, Ehsan Sayad, Loes van Schaik, Bryant C Scharenbroch, Michael Schirrmann, Olaf Schmidt, Boris Schröder, Julia Seeber, Maxim P Shashkov, Jaswinder Singh, Sandy M Smith, Michael Steinwandter, José A Talavera, Dolores Trigo, Jiro Tsukamoto, Anne W de Valença, Steven J Vanek, Iñigo Virto, Adrian A Wackett, Matthew W Warren, Nathaniel H Wehr, Joann K Whalen, Michael B Wironen, Volkmar Wolters, Irina V Zenkova, Weixin Zhang, Erin K. Cameron, Nico Eisenhauer

    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.

  • Nature

    Soil nematode abundance and functional group composition at a global scale

    Johan van den Hoogen, Stefan Geisen, Devin Routh, Howard Ferris, Walter Traunspurger, David A. Wardle, Ron G M de Goede, Byron J Adams, Wasim Ahmad, Walter S. Andriuzzi, Richard D. Bardgett, Michael Bonkowski, Raquel Campos-Herrera, Juvenil E Cares, Tancredi Caruso, Larissa de Brito Caixeta, Xiaoyun Chen, Sofia R Costa, Rachel Creamer, José Mauro da Cunha Castro, Anne Marie Van Dam, Djibril Djigal, Miguel Escuer, Bryan S. Griffiths, Carmen Gutiérrez, Karin Hohberg, Daria Kalinkina, Paul Kardol, Alan Kergunteuil, Gerard Korthals, Valentyna Krashevska, Alexey A Kudrin, Qi Li, Wenju Liang, Matthew Magilton, Mariette Marais, José Antonio Rodríguez Martín, Elizaveta Matveeva, El Hassan Mayad, Christian Mulder, Peter Mullin, Roy Neilson, T A Duong Nguyen, Uffe N Nielsen, Hiroaki Okada, Juan Emilio Palomares Rius, Kaiwen Pan, Vlada Peneva, Loïc Pellissier, Julio Carlos Pereira da Silva, Camille Pitteloud, Thomas O Powers, Kirsten Powers, Casper Quist, Sergio Rasmann, Sara Sánchez Moreno, Stefan Scheu, Heikki Setälä, Anna Sushchuk, Alexei V. Tiunov, Jean Trap, Wim H. van der Putten, Mette Vestergård, Cecile Villenave, Lieven Waeyenberge, Diana H. Wall, Rutger Wilschut, Daniel G Wright, Jiue-In Yang, Thomas Ward Crowther

    Soil organisms are a crucial part of the terrestrial biosphere. Despite their importance for ecosystem functioning, few quantitative, spatially explicit models of the active belowground community currently exist. In particular, nematodes are the most abundant animals on Earth, filling all trophic levels in the soil food web. Here we use 6,759 georeferenced samples to generate a mechanistic understanding of the patterns of the global abundance of nematodes in the soil and the composition of their functional groups. The resulting maps show that 4.4 ± 0.64 × 1020 nematodes (with a total biomass of approximately 0.3 gigatonnes) inhabit surface soils across the world, with higher abundances in sub-Arctic regions (38% of total) than in temperate (24%) or tropical (21%) regions. Regional variations in these global trends also provide insights into local patterns of soil fertility and functioning. These high-resolution models provide the first steps towards representing soil ecological processes in global biogeochemical models and will enable the prediction of elemental cycling under current and future climate scenarios.

  • Journal of Applied Ecology

    Does topsoil removal in grassland restoration benefit both soil nematode and plant communities?

    Monika Carol Resch, Martin Schütz, Ulrich Graf, Roel Wagenaar, Wim H. van der Putten, Anita C. Risch
    Abstract Successful restoration of semi-natural grasslands on grasslands previously subject to intensive management needs to overcome manifold barriers. These include high soil fertility, the dominance of a few fast-growing plant species, degraded soil faunal communities and missing propagules of the targeted above- and below-ground flora and fauna. A combination of removing the topsoil and introducing propagules of target plants has become one of the major tools for nature conservation agencies and practitioners to reduce soil fertility and restore former species-rich grasslands in various European countries. Using topsoil removal as a restoration measure has provoked an ongoing debate between supporting nature conservation and rejecting soil protection agencies. Although it favours species-rich plant communities, it strongly disturbs soil communities and affects physical and chemical soil properties and processes. Currently, there is a lack of long-term data to assess how restored grassland ecosystems develop and recover after topsoil removal. Here, we used two well-established bioindicators, soil nematodes and plants, to quantify restoration success of topsoil removal in comparison with alternative restoration measures and target communities 22 years after intervention. The nematode community composition indicated reduced nutrient availability in the restored systems, as was aimed at by topsoil removal. Nevertheless, after this 22-year period following topsoil removal, nematode composition and structure revealed successful recovery. Plant communities benefitted from the reduction of soil nutrients after topsoil removal as indicated by higher numbers of plant species and higher Shannon diversity. Furthermore, topsoil removal strongly promoted the re-establishment of plant species of the target plant community. Synthesis and applications. Overall, our study demonstrates how a massive intervention by topsoil removal proved successful in converting intensively managed into species-rich grasslands. This contrasts with the mild intervention of repeated mowing and removing of the harvested plant material. We show that, in the long run, potential negative effects of topsoil removal on the soil fauna can be successfully overcome and plant communities can develop into targeted species-rich grassland.
  • Trends in Ecology & Evolution

    Ecological Intensification: Bridging the Gap between Science and Practice

    David Kleijn, Riccardo Bommarco, Thijs P.M. Fijen, Lucas A. Garibaldi, Simon G. Potts, Wim H. van der Putten
    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.
  • PLoS One

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

    Viola Kurm, Wim H. van der Putten, (Gera) W.H.G. Hol
    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) 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.
  • Nature Communications

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

    Rutger Wilschut, Wim H. van der Putten, Paolina Garbeva, Paula Harkes, Wouter Konings, Purva Kulkarni, Henk Martens, Stefan Geisen
    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.
  • Functional Ecology

    Relationships between fungal community composition in decomposing leaf litter and home-field advantage effects

    Ciska Veen, Basten Snoek, Tanja Bakx-Schotman, David A. Wardle, Wim H. van der Putten
    Increasing evidence suggests that specific interactions between microbial decomposers and plant litter, named home field advantage (HFA), influence litter breakdown. However, we still have limited understanding of whether HFA relates to specific microbiota, and whether specialized microbes originate from the soil or from the leaf microbiome. Here, we disentangle the roles of soil origin, litter types, and the microbial community already present on the leaf litter in determining fungal community composition on decomposing leaf litter and HFA.

    We collected litters and associated soil samples from a secondary succession gradient ranging from herbaceous vegetation on recently abandoned ex‐arable fields to forest representing the end stage of succession. In a greenhouse, sterilized and unsterilized leaf litters were decomposed for 12 months in soils from early to late successional stages according to a full factorial design. At the end, we examined fungal community composition on the decomposing litter.

    Fungal communities on decomposed late‐successional litter in late‐successional soil differed from those in early‐ and mid‐successional stage litter and soil combinations. Soil source had the strongest impact on litter fungal composition when using sterilized litter, while the impact of litter type was strongest when using unsterilized litter. Overall, we observed HFA, as litter decomposition was accelerated in home soils. Increasing HFA did not relate to the dissimilarity in overall fungal composition, but there was increasing dissimilarity in the relative abundance of the most dominant fungal taxon between decomposing litter in home and away soils.

    We conclude that early, mid and late succession litter types did not exert strong selection effects on colonization by microorganisms from the soil species pool. Instead, fungal community composition on decomposing litter differed substantially between litter types for unsterilized litter, suggesting that the leaf microbiome, either directly or indirectly, is an important determinant of fungal community composition on decomposing leaves. HFA related most strongly to the abundance of the most dominant fungal taxa on the decomposing litter, suggesting that HFA may be attributed to some specific dominant fungi rather than to responses of the whole fungal community.
  • Global Change Biology

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

    Rutger Wilschut, Stefan Geisen, Henk Martens, Olga Kostenko, Mattias De Hollander, Freddy ten Hooven, Carolin Weser, Basten Snoek, Janneke Bloem, Danka Caković, Tatjana Čelik, Kadri Koorem, Nikos Krigas, Marta Manrubia-Freixa, Kelly Ramirez, M.A. Tsiafouli, Branko Vreš, Wim H. van der Putten
    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.
  • New Phytologist

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

    Minggang Wang, Weibin Ruan, Olga Kostenko, Sabrina Almeida de Carvalho, Emilia Hannula, P.P.J. Mulder, F. Bu, Wim H. van der Putten, T. Martijn Bezemer
    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.
  • Environmental Microbiology

    Competition and predation as possible causes of bacterial rarity

    Viola Kurm, Wim H. van der Putten, Simone Weidner, Stefan Geisen, Basten Snoek, Tanja Bakx-Schotman, (Gera) W.H.G. Hol

    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. This article is protected by copyright. All rights reserved.

  • Frontiers in Ecology and Evolution

    Applying the aboveground-belowground interaction concept in agriculture

    Ciska Veen, Jasper Wubs, Richard D. Bardgett, Edmundo Barrios, Mark Bradford, Sabrina Almeida de Carvalho, Gerlinde De Deyn, Franciska T. De Vries, Ken E. Giller, David Kleijn, Douglas A. Landis, Walter A.H. Rossing, Maarten Schrama, Johan Six, Paul C. Struik, Stijn van Gils, Johannes S.C. Wiskerke, Wim H. van der Putten, Louise E.M. Vet

    Interactions between aboveground and belowground organisms are important drivers of plant growth and performance in natural ecosystems. Making practical use of such above-belowground biotic interactions offers important opportunities for enhancing the sustainability of agriculture, as it could favor crop growth, nutrient supply, and defense against biotic and abiotic stresses. However, the operation of above-and belowground organisms at different spatial and temporal scales provides important challenges for application in agriculture. Aboveground organisms, such as herbivores and pollinators, operate at spatial scales that exceed individual fields and are highly variable in abundance within growing seasons. In contrast, pathogenic, symbiotic, and decomposer soil biota operate at more localized spatial scales from individual plants to patches of square meters, however, they generate legacy effects on plant performance that may last from single to multiple years. The challenge is to promote pollinators and suppress pests at the landscape and field scale, while creating positive legacy effects of local plant-soil interactions for next generations of plants. Here, we explore the possibilities to improve utilization of above-belowground interactions in agro-ecosystems by considering spatio-temporal scales at which aboveground and belowground organisms operate. We identified that successful integration of above-belowground biotic interactions initially requires developing crop rotations and intercropping systems that create positive local soil legacy effects for neighboring as well subsequent crops. These configurations may then be used as building blocks to design landscapes that accommodate beneficial aboveground communities with respect to their required resources. For successful adoption of above-belowground interactions in agriculture there is a need for context-specific solutions, as well as sound socio-economic embedding.

  • Current Biology

    Challenges and Opportunities for Soil Biodiversity in the Anthropocene

    Stefan Geisen, Diana H. Wall, Wim H. van der Putten
    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.
  • Agriculture, Ecosystems and Environment

    Pollination contribution to crop yield is often context-dependent: A review of experimental evidence

    Giovanni Tamburini, Riccardo Bommarco, David Kleijn, Wim H. van der Putten, Lorenzo Marini
    Insect pollination is a well-studied ecosystem service that supports production in 75% of globally important crops. Although yield is known to be sustained and regulated by a bundle of ecosystem services and management factors, the contribution of pollination to yield has been mostly studied in isolation. Here, we compiled and reviewed research on the contribution of pollination to crop yield under different environmental conditions, where the potential interaction between pollination and other factors contributing to yield, such as nutrient availability and control of pests, was tested. Specifically, we explored whether pollination displayed synergistic, compensatory or additive effects with concomitant factors. The literature search resulted in 24 peer-reviewed studies for a total of 39 individual tests of interactions. Studies examined responses in 13 crops testing interactions both at the local and the landscape scale. Interactions between pollination and other factors influencing yield were observed for several crops and mostly displayed positive-synergistic relationships. Crop life-history traits such as pollination dependency were found to affect the plant response to variations in resource and pollen availability. Soil properties and crop pests might affect contribution of pollination to yield by altering the amount of resources a plant can allocate to reproduction, independently of the amount of pollen provided. Current management strategies to enhance pollinators might fail to increase pollination benefits in landscapes characterized by poor soil resources or ineffective pest control. We propose that our understanding of the effects of crop-pollinator interactions will benefit by focusing on plant traits and physiological responses. Combining knowledge from plant physiology and ecology with technological advances in agriculture is needed to design novel management strategies to maximize pollination benefits and support yields and reduce environmental impacts of food production.
  • BioScience

    A Conceptual Framework for Range-Expanding Species that Track Human-Induced Environmental Change

    Franz Essl, Stefan Dullinger, Piero Genovesi, Philip E. Hulme, Jonathan M Jeschke, Stelios Katsanevakis, Ingolf Kühn, Bernd Lenzner, Aníbal Pauchard, Petr Pyšek, Wolfgang Rabitsch, David M. Richardson, Hanno Seebens, Mark van Kleunen, Wim H. van der Putten, Montserrat Vilà, Sven Bacher
    For many species, human-induced environmental changes are important indirect drivers of range expansion into new regions. We argue that it is important to distinguish the range dynamics of such species from those that occur without, or with less clear, involvement of human-induced environmental changes. We elucidate the salient features of the rapid increase in the number of species whose range dynamics are human induced, and review the relationships and differences to both natural range expansion and biological invasions. We discuss the consequences for science, policy and management in an era of rapid global change and highlight four key challenges relating to basic gaps in knowledge, and the transfer of scientific understanding to biodiversity management and policy. We conclude that range-expanding species responding to human-induced environmental change will become an essential feature for biodiversity management and science in the Anthropocene. Finally, we propose the term neonative for these taxa.
  • Ecology Letters

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

    Jasper Wubs, Wim H. van der Putten, S.R. Mortimer, Gerard Korthals, Henk Duyts, Roel Wagenaar, T. Martijn Bezemer
    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.
  • Nature Ecology and Evolution

    Range-expansion effects on the belowground plant microbiome

    Kelly Ramirez, Basten Snoek, Kadri Koorem, Stefan Geisen, L. Janneke Bloem, Freddy ten Hooven, Olga Kostenko, Nikos Krigas, Marta Manrubia-Freixa, Danka Caković, Debbie van Raaij, Maria A. Tsiafouli, Branko Vreš, Tatjana Čelik, Carolin Weser, Rutger Wilschut, Wim H. van der Putten
    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.
  • Soil Biology & Biochemistry

    Unexpected role of canonical aerobic methanotrophs in upland agricultural soils.

    Adrian Ho, Hyo Jung Lee, Max Reumer, M. Meima-Franke, Ciska Raaijmakers, Hans Zweers, Wietse de Boer, Wim H. van der Putten, Paul Bodelier
    Aerobic oxidation of methane at (circum-)atmospheric concentrations (<40 ppmv) has long been assumed to be catalyzed by the as-yet-uncultured high-affinity methanotrophs in well-aerated, non-wetland (upland) soils, the only known biological methane sink globally. Although the low-affinity canonical methanotrophs with cultured representatives have been detected along with the high-affinity ones, their role as a methane sink in upland soils remains enigmatic. Here, we show that canonical methanotrophs can contribute to (circum-)atmospheric methane uptake in agricultural soils. We performed a stable-isotope 13CCH4 labelling incubation in the presence and absence of bio-based residues that were added to the soil to track the flow of methane. Residue amendment transiently stimulated methane uptake rate (<50 days). Soil methane uptake was sustained throughout the incubation (130 days), concomitant to the enrichment of 13CCO2. The 13C-enriched phospholipid fatty acids (PLFAs) were distinct in both soils, irrespective of amendments, and were unambiguously assigned almost exclusively to canonical alphaproteobacterial methanotrophs with cultured representatives. 16S rRNA and pmoA gene sequence analyses revealed that the as-yet-uncultured high-affinity methanotrophs were virtually absent in these soils. The stable-isotope labelling approach allowed to attribute soil methane uptake to canonical methanotrophs, whereas these were not expected to consume (circum-)atmospheric methane. Our findings thus revealed an overlooked reservoir of high-affinity methane-oxidizers represented by the canonical methanotrophs in agriculture-impacted upland soils. Given that upland agricultural soils have been thought to marginally or do not contribute to atmospheric methane consumption due to the vulnerability of the high-affinity methanotrophs, our findings suggest a thorough revisiting of the contribution of agricultural soils, and the role of agricultural management to mitigation of climate change.
  • Frontiers in Microbiology

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

    Marta Manrubia-Freixa, Basten Snoek, Carolin Weser, Ciska Veen, Wim H. van der Putten
    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.
  • Functional Ecology

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

    Marta Manrubia-Freixa, Wim H. van der Putten, Carolin Weser, Freddy ten Hooven, Henk Martens, Pella Brinkman, Stefan Geisen, Kelly Ramirez, Ciska Veen
    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.
  • Nature Reviews Microbiology

    Microbial invasions in terrestrial ecosystems

    Maddy Thakur, Wim H. van der Putten, Marleen Cobben, M. Van Kleunen, Stefan Geisen
    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.
  • Soil Biology & Biochemistry

    Spatial distribution of soil nematodes relates to soil organic matter and life strategy

    Casper Quist, Gerrit Gort, Paul J.W. Mooijman, Dick J. Brus, Sven J.J. van den Elsen, Olga Kostenko, Mariette Vervoort, Jaap Bakker, Wim H. van der Putten, Johannes Helder
    Soils are among the most biodiverse and densely inhabited environments on our planet. However, there is little understanding of spatial distribution patterns of belowground biota, and this hampers progress in understanding species interactions in belowground communities. We investigated the spatial distribution of nematodes, which are highly abundant and diverse metazoans in most soil ecosystems. To gain insight into nematode patchiness, we mapped distribution patterns in twelve apparently homogeneous agricultural fields (100 m × 100 m each) with equal representation of three soil textures (marine clay, river clay and sandy soil). Quantitative PCRs were used to measure the abundances of 48 distinct nematode taxa in ≈1200 plots. Multivariate analysis showed that within this selection of sites, soil texture more strongly affected soil nematode communities than land management. Geostatistical analysis of nematode distributions revealed both taxon-specific and field-specific patchiness. The average geostatistical range (indicating patch diameter) of 48 nematode taxa in these fields was 36 m, and related to soil organic matter. Soil organic matter content affected the spatial variance (indicating within-field variation of densities) in a life-strategy dependent manner. The r-strategists (fast-growing bacterivores and fungivores) showed a positive correlation between organic matter content and spatial variance, whereas most K-strategists (slow-growing omnivores and carnivores) showed a negative correlation. Hence, the combination of two parameters, soil organic matter content and a general life-strategy characterisation, can be used to explain the spatial distribution of nematodes at field scale.
  • Nature Communications

    Size-dependent loss of aboveground animals differentially affects grassland ecosystem coupling and functions

    Anita C. Risch, R Ochoa-Hueso, Wim H. van der Putten, J K Bump, Matt D. Busse, B Frey, Dariusz J. Gwiazdowicz, Deborah S. Page-Dumroese, Martijn L. Vandegehuchte, Susan Zimmermann, Martin Schütz
    Increasing evidence suggests that community-level responses to human-induced biodiversity loss start with a decrease of interactions among communities and between them and their abiotic environment. The structural and functional consequences of such interaction losses are poorly understood and have rarely been tested in real-world systems. Here, we analysed how 5 years of progressive, size-selective exclusion of large, medium, and small vertebrates and invertebrates-a realistic scenario of human-induced defaunation-impacts the strength of relationships between above- and belowground communities and their abiotic environment (hereafter ecosystem coupling) and how this relates to ecosystem functionality in grasslands. Exclusion of all vertebrates results in the greatest level of ecosystem coupling, while the additional loss of invertebrates leads to poorly coupled ecosystems. Consumer-driven changes in ecosystem functionality are positively related to changes in ecosystem coupling. Our results highlight the importance of invertebrate communities for maintaining ecological coupling and functioning in an increasingly defaunated world.
  • Ecology Letters

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

    Lekberg Ylva, Bever James D., Rebecca A. Bunn, Callaway Ragan M., Hart Miranda M., Kivlin Stephanie N., Klironomos John, Larkin Beau G., Maron John L., Reinhart Kurt O., Remke Michael, Wim H. van der Putten
    Abstract 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.
  • Basic and Applied Ecology

    Drought and soil fertility modify fertilization effects on aphid performance in wheat

    Giovanni Tamburini, Stijn van Gils, Martine Kos, Wim H. van der Putten, Lorenzo Marini
    Agricultural intensification and climate change are expected to affect pest performance through excessive inputs of chemical fertilizers and increased probability of extreme drought events. Potential interactive effects of fertilization and water availability on aboveground pest performance may depend on soil fertility because of its effect on nutrient availability. In a greenhouse experiment, we examined the effects of inorganic fertilization on the performance of the grain aphid (Sitobion avenae, F.), an important pest of wheat, under different conditions of soil fertility and water availability. We found soil fertility and water availability to influence the positive effects of inorganic fertilizers on aphid growth, i.e. fertilization promoted faster aphid development time and higher fecundity and biomass under low fertility and under well-watered conditions. Moreover, although increased soil fertility favored aphid growth under well-watered conditions, it simultaneously sustained plant development. The current practices promoting soil fertility do not have direct negative consequence on crop protection under conventional cropping systems.
  • Agriculture, Ecosystems and Environment

    Crop yield gap and stability in organic and conventional farming systems

    Maarten Schrama, J. De Haan, M. Kroonen, H. Verstegen, Wim H. van der Putten
    Abstract A key challenge for sustainable intensification of agriculture is to produce increasing amounts of food and feed with minimal biodiversity loss, nutrient leaching, and greenhouse gas emissions. Organic farming is considered more sustainable, however, less productive than conventional farming. We analysed results from an experiment started under identical soil conditions comparing one organic and two conventional farming systems. Initially, yields in the organic farming system were lower, but approached those of both conventional systems after 10–13 years, while requiring lower nitrogen inputs. Unexpectedly, organic farming resulted in lower coefficient of variation, indicating enhanced spatial stability, of pH, nutrient mineralization, nutrient availability, and abundance of soil biota. Organic farming also resulted in improved soil structure with higher organic matter concentrations and higher soil aggregation, a profound reduction in groundwater nitrate concentrations, and fewer plant-parasitic nematodes. Temporal stability between the three farming systems was similar, but when excluding years of Phytophthora outbreaks in potato, temporal stability was higher in the organic farming system. There are two non-mutually exclusive mechanistic explanations for these results. First, the enhanced spatial stability in the organic farming system could result from changes in resource-based (i.e. bottom-up) processes, which coincides with the observed higher nutrient provisioning throughout the season in soils with more organic matter. Second, enhanced resource inputs may also affect stability via increased predator-based (i.e. top-down) control. According to this explanation, predators stabilize population dynamics of soil organisms, which is supported by the observed higher soil food web biomass in the organic farming system.We conclude that closure of the yield gap between organic and conventional farming can be a matter of time and that organic farming may result in greater spatial stability of soil biotic and abiotic properties and soil processes. This is likely due to the time required to fundamentally alter soil properties.
  • Ecology and Evolution

    Increased transgenerational epigenetic variation, but not predictable epigenetic variants, after environmental exposure in two apomictic dandelion lineages

    Veronica Preite, Carla Oplaat, Arjen Biere, Jan Kirschner, Wim H. van der Putten, Koen Verhoeven

    DNA methylation is one of the mechanisms underlying epigenetic modifications. DNA methylations can be environmentally induced and such induced modifications can at times be transmitted to successive generations. However, it remains speculative how common such environmentally induced transgenerational DNA methylation changes are and if they persist for more than one offspring generation. We exposed multiple accessions of two different apomictic dandelion lineages of the Taraxacum officinale group (Taraxacum alatum and T. hemicyclum) to drought and salicylic acid (SA) treatment. Using methylation-sensitive amplified fragment length polymorphism markers (MS-AFLPs) we screened anonymous methylation changes at CCGG restriction sites throughout the genome after stress treatments and assessed the heritability of induced changes for two subsequent unexposed offspring generations. Irrespective of the initial stress treatment, a clear buildup of heritable DNA methylation variation was observed across three generations, indicating a considerable background rate of heritable epimutations. Less evidence was detected for environmental effects. Drought stress showed some evidence for accession-specific methylation changes, but only in the exposed generation and not in their offspring. By contrast, SA treatment caused an increased rate of methylation change in offspring of treated plants. These changes were seemingly undirected resulting in increased transgenerational epigenetic variation between offspring individuals, but not in predictable epigenetic variants. While the functional consequences of these MS-AFLP-detected DNA methylation changes remain to be demonstrated, our study shows that (1) stress-induced transgenerational DNA methylation modification in dandelions is genotype and context-specific; and (2) inherited environmental DNA methylation effects are mostly undirected and not targeted to specific loci.

  • Journal of Plant Ecology

    Plant responses to variable timing of aboveground clipping and belowground herbivory depend on plant age

    Minggang Wang, T. Martijn Bezemer, Wim H. van der Putten, Pella Brinkman, Arjen Biere
    Plants use different types of responses such as tolerance and induced defense to mitigate the effects of herbivores. The direction and magnitude of both these plant responses can vary with plant age. However, most studies have focused on aboveground herbivory, whereas important feeding occurs belowground. Here we tested the hypothesis that plant tolerance and defense following shoot damage or root herbivory depends on plant age.
    In order to test our hypothesis, we exposed the perennial grass species Holcus lanatus to defoliation and root nematode inoculation at three growth stages (young, intermediate and old plants), and examined responses of plant traits related to tolerance (regrowth following defoliation) and defense (leaf and root nitrogen and phenolics).
    Important findings
    Defoliation overall reduced plant shoot and root biomass as well as foliar concentrations of phenolics regardless of plant age at defoliation. In contrast, defoliation increased foliar N concentrations, but only when defoliation occurred at intermediate and old plant age. Inoculation with root feeding nematodes reduced root N concentrations after a prolonged period of growth, but only when nematodes had been inoculated when plants were young. The relative shoot regrowth rate of plants increased immediately after defoliation but this was independent of the plant age at which defoliation occurred, i.e., was not stronger in plants that were defoliated at a more advanced age, as hypothesized. Similarly, relative root growth rates increased shortly after defoliation, but this was only observed for plants defoliated when they were young. We conclude that plant responses to above- and belowground herbivory in traits related to both defense and tolerance are affected by plant age, but do not generally change with plant age.
  • Ecology

    Biodiversity-ecosystem functioning relationships in a long-term non-weeded field experiment

    Ciska Veen, Wim H. van der Putten, T. Martijn Bezemer
    Many grassland biodiversity experiments show a positive relationship between biodiversity and ecosystem functioning, however, in most of these experiments plant communities are established by sowing and natural colonization is prevented by selective weeding of non‐sown species. During ecosystem restoration, for example on abandoned fields, plant communities start on bare soil, and diversity is often manipulated in a single sowing event. How such initial plant diversity manipulations influence plant biodiversity development and ecosystem functioning is not well understood. We examined how relationships between taxonomic and functional diversity, biomass production and stability develop over 16 yr in non‐weeded plots sown with 15 species, four species, or that were not sown. We found that sown plant communities become functionally similar to unsown, naturally colonized plant communities. However, initial sowing treatments had long‐lasting effects on species composition and taxonomic diversity. We found only few relationships between biomass production, or stability in biomass production, and functional or taxonomic diversity, and the ones we observed were negative. In addition, the cover of dominant plant species was positively related to biomass production and stability. We conclude that effects of introducing plant species at the start of secondary succession can persist for a long time, and that in secondary succession communities with natural plant species dynamics diversity–functioning relationships can be weak or negative. Moreover, our findings indicate that in systems where natural colonization of species is allowed effects of plant dominance may underlie diversity–functioning relationships.
  • Annals of Botany

    Soil microbial species loss affects plant biomass and survival of an introduced bacterial strain, but not inducible plant defences

    Viola Kurm, Wim H. van der Putten, Ana Pineda, (Gera) W.H.G. Hol
    • Background and Aims Plant growth-promoting rhizobacteria (PGPR) strains can influence plant–insect
    interactions. However, little is known about the effect of changes in the soil bacterial community in general and
    especially the loss of rare soil microbes on these interactions. Here, the influence of rare soil microbe reduction
    on induced systemic resistance (ISR) in a wild ecotype of Arabidopsis thaliana against the aphid Myzus persicae
    was investigated.
    • Methods To create a gradient of microbial abundances, soil was inoculated with a serial dilution of a microbial
    community and responses of Arabidopsis plants that originated from the same site as the soil microbes were
    tested. Plant biomass, transcription of genes involved in plant defences, and insect performance were measured.
    In addition, the effects of the PGPR strain Pseudomonas fluorescens SS101 on plant and insect performance were
    tested under the influence of the various soil dilution treatments.
    • Key Results Plant biomass showed a hump-shaped relationship with soil microbial community dilution,
    independent of aphid or Pseudomonas treatments. Both aphid infestation and inoculation with Pseudomonas
    reduced plant biomass, and led to downregulation of PR1 (salicylic acid-responsive gene) and CYP79B3 (involved
    in synthesis of glucosinolates). Aphid performance and gene transcription were unaffected by soil dilution.
    • Conclusions Neither the loss of rare microbial species, as caused by soil dilution, nor Pseudomonas affect the
    resistance of A. thaliana against M. persicae. However, both Pseudomonas survival and plant biomass respond to
    rare species loss. Thus, loss of rare soil microbial species can have a significant impact on both above- and belowground
  • Functional Ecology

    Variation in home-field advantage and ability in leaf litter decomposition across successional gradients

    Ciska Veen, A.D. Keiser, Wim H. van der Putten, David A. Wardle
    It is increasingly recognized that interactions between plants and soil (a)biotic conditions can influence local decomposition processes. For example, decomposer communities may become specialized in breaking down litter of plant species that they are associated with, resulting in accelerated decomposition, known as “home‐field advantage” (HFA). Also, soils can vary inherently in their capacity to degrade organic compounds, known as “ability.” However, we have a poor understanding how environmental conditions drive the occurrence of HFA and ability.
    Here, we studied how HFA and ability change across three types of successional gradients: coastal sand dunes (primary succession), inland drift sands (primary succession) and ex‐arable fields (secondary succession). Across these gradients, litter quality (i.e. nutrient, carbon and lignin contents) increases with successional time for coastal dunes and decreases for the other two gradients.
    We performed a 12‐months reciprocal litter transplant experiment under greenhouse conditions using soils and litters collected from early‐, mid‐ and late‐successional stages of each gradient.
    We found that HFA and ability did not consistently shift with successional stage for all gradients, but were instead specific for each type of successional gradient. In coastal dunes, HFA was positive for early‐successional litter, in drift, sands it was negative for mid‐successional litter, and for ex‐arable fields, HFA increased with successional time. Ability of decomposer communities was highest in mid‐successional stages for coastal dunes and drift sands, but for ex‐arable fields, ability decreased throughout with successional time. High HFA was related to high litter C content and soil and organic matter content in soils and to low litter and soil nutrient concentrations. Ability did not consistently occur in successional stages with high or low litter quality.
    Synthesis. Our findings show that specific environmental conditions, such as changes in litter or soil quality, along environmental gradients can shape the influence of HFA and ability on decomposition. In sites with strong HFA or ability, interactions between plants, litter and decomposer communities will be important drivers of nutrient cycling and hence have the potential to feedback to plant growth.
  • Journal of Ecology

    The influence of residence time and geographic extent on the strength of plant–soil feedbacks for naturalised Trifolium

    Kevin J. McGinn, Wim H. van der Putten, Philip E. Hulme, Natasha Shelby, Carolin Weser, Richard P. Duncan
    Release from natural enemies is considered an important mechanism underlying the success of plants introduced to new regions, but the degree to which alien plant species benefit from enemy release appears highly variable and context-dependent. Such variation could arise if enemy release is a transient phenomenon, whereby alien plant species initially escape but subsequently accumulate enemies in their new regions.
    To evaluate this hypothesis in terms of soil biota, we used 11 Trifolium (clover) species introduced to New Zealand from Europe to test whether species resident for longer or with a larger geographic extent in New Zealand were more adversely affected by soil communities in the introduced range, as expected if species have accumulated inhibitory soil biota over time. We used plant–soil feedback (PSF) experiments to compare the effect of soil biota on the growth of the Trifolium species in soil from their introduced (New Zealand) and native (Spain and the United Kingdom) ranges. We applied a novel statistical approach aimed at isolating the impact of antagonistic soil biota by accounting for variation in plant growth due to mutualistic rhizobia bacteria.
    The between-range differences in PSF varied considerably among the Trifolium species: some species were released from inhibitory PSF in the introduced range, but the majority experienced similar PSF in both ranges. Averaged over all 11 Trifolium species, PSF was less inhibitory in the introduced than in the native range, implying some release from soil-borne enemies. However, neither residence time nor geographic extent in the introduced range was significantly correlated with the strength of release from inhibitory PSF.
    Synthesis. Our multispecies study provides some evidence that alien plants can escape antagonistic soil biota in their introduced range, but highlights how plant–soil feedback responses can be highly variable among congeneric plant species in the same region. Our results do not support the hypothesis that the release from inhibitory plant–soil feedback is transient, questioning the generality of this phenomenon.
  • Planta

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

    Purva Kulkarni, Rutger Wilschut, Koen Verhoeven, Wim H. van der Putten, Paolina Garbeva
    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-assisted 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 was acquired in a mass range of m/z 50-1200 with a spatial resolution of 100 μm. The acquired data was 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.
  • Methods in Ecology and Evolution

    Integrating quantitative morphological and qualitative molecular methods to analyse soil nematode community responses to plant range expansion

    Stefan Geisen, Basten Snoek, Freddy ten Hooven, Henk Duyts, Olga Kostenko, Janneke Bloem, Henk Martens, Casper Quist, Johannes Helder, Wim H. van der Putten
    Below‐ground nematodes are important for soil functioning, as they are ubiquitous and operate at various trophic levels in the soil food web. However, morphological nematode community analysis is time consuming and requires ample training. qPCR‐based nematode identification techniques are well available, but high‐throughput sequencing (HTS) might be more suitable for non‐targeted nematode community analyses.
    We compared effectiveness of qPCR‐ and HTS‐based approaches with morphological nematode identification while examining how climate warming‐induced plant range expansion may influence below‐ground nematode assemblages. We extracted nematodes from soil of Centaurea stoebe and C. jacea populations in Slovenia, where both plant species are native, and Germany, where C. stoebe is a range expander and C. jacea is native. Half of each nematode sample was identified morphologically and the other half was analysed using targeted qPCR and a novel HTS approach.
    HTS produced the highest taxonomic resolution of the nematode community. Nematode taxa abundances correlated between the methods. Therefore, especially relative HTS and relative morphological data revealed nearly identical ecological patterns. All methods showed lower numbers of plant‐feeding nematodes in rhizosphere soils of C. stoebe compared to C. jacea. However, a profound difference was observed between absolute and relative abundance data; both sampling origin and plant species affected relative abundances of bacterivorous nematodes, whereas there was no effect on absolute abundances.
    Taken together, as HTS correlates with relative analyses of soil nematode communities, while providing highest taxonomic resolution and sample throughput, we propose a combination of HTS with microscopic counting to supplement important quantitative data on soil nematode communities. This provides the most cost‐effective, in‐depth methodology to study soil nematode community responses to changes in the environment. This methodology will also be applicable to nematode analyses in aquatic systems.
  • Ecology and Evolution

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

    Rutger Wilschut, Olga Kostenko, Kadri Koorem, Wim H. van der Putten
    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 rootfeeding
    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 rangeexpanding
    plant species do not accumulate fewer root-feeding nematodes in their
    new than in their original range.
  • Oikos

    Relatedness with plant species in native community influences ecological consequences of range expansions

    Kadri Koorem, Olga Kostenko, Basten Snoek, Carolin Weser, Kelly Ramirez, Rutger Wilschut, Wim H. van der Putten
    Global warming is enabling many plant species to expand their range to higher latitudes and altitudes, where they may suffer less from natural aboveground and belowground enemies. Reduced control by natural enemies can enable climate warming-induced range expanders to get an advantage in competition with natives and become disproportionally abundant in their new range. However, so far studies have examined individual growth of range expanders, which have common congeneric plant species in their new range. Thus it is not known how general is this reduced effect of above- and belowground enemies and how it operates in communities, where multiple plant species also interact with each other. Here we show that range-expanding plant species with and without congenerics in the invaded habitats differ in their ecological interactions in the new range. In a community-level experiment, range-expanding plant species, both with and without congenerics, suppressed the growth of a herbivore. However, only range expanders without congenerics reduced biomass production of the native plant species. In the present study, range expanders without congenerics allocated more biomass aboveground compared to native plant species, which can explain their competitive advantage. Competitive interaction and also biomass allocation of native plants and their congeneric range expanders were similar. Our results highlight that information about species phylogenetic relatedness with native flora can be crucial for improving predictions about the consequences of climate warming-induced range expansions.
  • Nature Microbiology

    Detecting macroecological patterns in bacterial communities across independent studies of global soils

    Kelly Ramirez, Christopher G. Knight, Mattias De Hollander, Francis Q. Brearley, Bede Constantinides, Anne Cotton, Si Creer, Tom Crowther, John Davison, Manuel Delgado-Baquerizo, Ellen Dorrepaal, David R. Elliott, Graeme Fox, Robert I. Griffiths, Chris Hale, Kyle Hartman, Ashley Houlden, David L. Jones, Eveline J. Krab, Fernando T. Maestre, Krista L. McGuire, Sylvain Monteux, Caroline H. Orr, Wim H. van der Putten, Ian S. Roberts, David A. Robinson, Jennifer D. Rocca, Jennifer Rowntree, Klaus Schlaeppi, Matthew Shepherd, Brajesh K. Singh, Angie Straathof, Jennifer M. Bhatnagar, Cécile Thion, Marcel G. A. van der Heijden, Franciska T. De Vries
    The emergence of high-throughput DNA sequencing methods provides unprecedented opportunities to further unravel bacterial biodiversity and its worldwide role from human health to ecosystem functioning. However, despite the abundance of sequencing studies, combining data from multiple individual studies to address macroecological questions of bacterial diversity remains methodically challenging and plagued with biases. Here, using a machine-learning approach that accounts for differences among studies and complex interactions among taxa, we merge 30 independent bacterial data sets comprising 1,998 soil samples from 21 countries. Whereas previous meta-analysis efforts have focused on bacterial diversity measures or abundances of major taxa, we show that disparate amplicon sequence data can be combined at the taxonomy-based level to assess bacterial community structure. We find that rarer taxa are more important for structuring soil communities than abundant taxa, and that these rarer taxa are better predictors of community structure than environmental factors, which are often confounded across studies. We conclude that combining data from independent studies can be used to explore bacterial community dynamics, identify potential ‘indicator’ taxa with an important role in structuring communities, and propose hypotheses on the factors that shape bacterial biogeography that have been overlooked in the past.
  • Trends in Plant Science

    Network Analyses Can Advance Above-Belowground Ecology

    Kelly Ramirez, Stefan Geisen, Elly Morrien, Basten Snoek, Wim H. van der Putten
    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.
  • Ecosystems

    Enhancing Soil Organic Matter as a Route to the Ecological Intensification of European Arable Systems

    Michael P. D. Garratt, Riccardo Bommarco, David Kleijn, E. Martin, S.R. Mortimer, Sarah Redlich, Deepa Senapathi, I. Steffan-Dewenter, Stanisław Świtek, Viktória Takács, Stijn van Gils, Wim H. van der Putten, Simon G. Potts
    Soil organic matter (SOM) is declining in most agricultural ecosystems, impacting multiple ecosystem services including erosion and flood prevention, climate and greenhouse gas regulation as well as other services that underpin crop production, such as nutrient cycling and pest control. Ecological intensification aims to enhance crop productivity by including regulating and supporting ecosystem service management into agricultural practices. We investigate the potential for increased SOM to support the ecological intensification of arable systems by reducing the need for nitrogen fertiliser application and pest control. Using a large-scale European field trial implemented across 84 fields in 5 countries, we tested whether increased SOM (using soil organic carbon as a proxy) helps recover yield in the absence of conventional nitrogen fertiliser and whether this also supports crops less favourable to key aphid pests. Greater SOM increased yield by 10%, but did not offset nitrogen fertiliser application entirely, which improved yield by 30%. Crop pest responses depended on species: Metopolophium dirhodum were more abundant in fertilised plots with high crop biomass, and although population growth rates of Sitobion avenae were enhanced by nitrogen fertiliser application in a cage trial, field populations were not affected. We conclude that under increased SOM and reduced fertiliser application, pest pressure can be reduced, while partially compensating for yield deficits linked to fertiliser reduction. If the benefits of reduced fertiliser application and increased SOM are considered in a wider environmental context, then a yield cost may become acceptable. Maintaining or increasing SOM is critical for achieving ecological intensification of European cereal production.
  • Global Change Biology

    Rapid evolution of phenology during range expansion with recent climate change

    Nicky Lustenhouwer, Rutger Wilschut, J.L. Williams, Wim H. van der Putten, J.M. Levine
    Although climate warming is expected to make habitat beyond species’ current cold range edge suitable for future colonization, this new habitat may present an array of biotic or abiotic conditions not experienced within the current range. Species’ ability to shift their range with climate change may therefore depend on how populations evolve in response to such novel environmental conditions. However, due to the recent nature of thus far observed range expansions, the role of rapid adaptation during climate change migration is only beginning to be understood. Here, we evaluated evolution during the recent native range expansion of the annual plant Dittrichia graveolens, which is spreading northward in Europe from the Mediterranean region. We examined genetically based differentiation between core and edge populations in their phenology, a trait that is likely under selection with shorter growing seasons and greater seasonality at northern latitudes. In parallel common garden experiments at range edges in Switzerland and the Netherlands, we grew plants from Dutch, Swiss, and central and southern French populations. Population genetic analysis following RAD-sequencing of these populations supported the hypothesized central France origins of the Swiss and Dutch range edge populations. We found that in both common gardens, northern plants flowered up to four weeks earlier than southern plants. This differentiation in phenology extended from the core of the range to the Netherlands, a region only reached from central France over approximately the last 50 years. Fitness decreased as plants flowered later, supporting the hypothesized benefits of earlier flowering at the range edge. Our results suggest that native range expanding populations can rapidly adapt to novel environmental conditions in the expanded range, potentially promoting their ability to spread.
  • Frontiers in Microbiology

    Drought legacy effects on the composition of soil fungal and prokaryote communities

    Annelein Meisner, Jacquiod Samuel, Basten Snoek, Freddy ten Hooven, Wim H. van der Putten
    It is increasingly acknowledged that climate change is influencing terrestrial ecosystems by increased drought and rainfall intensities. Soil microbes are key drivers of many processes in terrestrial systems and rely on water in soil pores to fulfill their life cycles and functions. However, little is known on how drought and rainfall fluctuations, which affect the composition and structure of microbial communities, persist once original moisture conditions have been restored. Here, we study how simulated short-term drying and re-wetting events shape the community composition of soil fungi and prokaryotes. In a mesocosm experiment, soil was exposed to an extreme drought, then re-wetted to optimal moisture (50% WHC, water holding capacity) or to saturation level (100% WHC). Composition, community structure and diversity of microbes were measured by sequencing ITS and 16S rRNA gene amplicons 3 weeks after original moisture content had been restored. Drying and extreme re-wetting decreased richness of microbial communities, but not evenness. Abundance changes were observed in only 8% of prokaryote OTUs, and 25% of fungal OTUs, whereas all other OTUs did not differ between drying and re-wetting treatments. Two specific legacy response groups (LRGs) were observed for both prokaryotes and fungi. OTUs belonging to the first LRG decreased in relative abundance in soil with a history of drought, whereas OTUs that increased in soil with a history of drought formed a second LRG. These microbial responses were spread among different phyla. Drought appeared to be more important for the microbial community composition than the following extreme re-wetting. 16S profiles were correlated with both inorganic N concentration and basal respiration and ITS profiles correlated with fungal biomass. We conclude that a drying and/or an extreme re-wetting history can persist in soil microbial communities via specific response groups composed of members with broad phylogenetic origins, with possible functional consequences on soil processes and plant species. As a large fraction of OTUs responding to drying and re-wetting belonged to the rare biosphere, our results suggest that low abundant microbial species are potentially important for ecosystem responses to extreme weather events.
  • Ecology Letters

    Combined effects of agrochemicals and ecosystem services on crop yield across Europe

    Vesna Gagic, David Kleijn, András Báldi, Gergely Boros, Helene Bracht Jørgensen, Zoltán Elek, Michael P. D. Garratt, G. Arjen de Groot, Katarina Hedlund, Anikó Kovács- Hostyánszki, Lorenzo Marini, Emily Martin, Ines Pevere, Simon G. Potts, Sarah Redlich, Deepa Senapathi, Ingolf Steffan-Dewenter, Stanislaw Świtek, Henrik G. Smith, Viktória Takács, Piotr Tryjanowski, Wim H. van der Putten, Stijn van Gils, Riccardo Bommarco
    Simultaneously enhancing ecosystem services provided by biodiversity below and above ground is recommended to reduce dependence on chemical pesticides and mineral fertilisers in agriculture. However, consequences for crop yield have been poorly evaluated. Above ground, increased landscape complexity is assumed to enhance biological pest control, whereas below ground, soil organic carbon is a proxy for several yield-supporting services. In a field experiment replicated in 114 fields across Europe, we found that fertilisation had the strongest positive effect on yield, but hindered simultaneous harnessing of below- and above-ground ecosystem services. We furthermore show that enhancing natural enemies and pest control through increasing landscape complexity can prove disappointing in fields with low soil services or in intensively cropped regions. Thus, understanding ecological interdependences between land use, ecosystem services and yield is necessary to promote more environmentally friendly farming by identifying situations where ecosystem services are maximised and agrochemical inputs can be reduced.
  • Nature

    The plant perceptron connects environment to development

    Ben Scheres, Wim H. van der Putten
    Plants cope with the environment in a variety of ways, and ecological analyses attempt to capture this through life-history strategies or trait-based categorization. These approaches are limited because they treat the trade-off mechanisms that underlie plant responses as a black box. Approaches that involve the molecular or physiological analysis of plant responses to the environment have elucidated intricate connections between developmental and environmental signals, but in only a few well-studied model species. By considering diversity in the plant response to the environment as the adaptation of an information-processing network, new directions can be found for the study of life-history strategies, trade-offs and evolution in plants.
  • Oikos

    Aboveground mammal and invertebrate exclusions cause consistent changes in soil food webs of two subalpine grassland types, but mechanisms are system-specific

    Martijn L. Vandegehuchte, Wim H. van der Putten, Henk Duyts, Martin Schütz, Anita C. Risch

    Ungulates, smaller mammals, and invertebrates can each affect soil biota through their influence on vegetation and soil characteristics. However, direct and indirect effects of the aboveground biota on soil food webs remain to be unraveled. We assessed effects of progressively excluding aboveground large-, medium- and small-sized mammals as well as invertebrates on soil nematode diversity and feeding type abundances in two subalpine grassland types: short- and tall-grass vegetation. We explored pathways that link exclusions of aboveground biota to nematode feeding type abundances via changes in plants, soil environment, soil microbial biomass, and soil nutrients.

    In both vegetation types, exclusions caused a similar shift toward higher abundance of all nematode feeding types, except plant feeders, lower Shannon diversity, and lower evenness. These effects were strongest when small mammals, or both small mammals and invertebrates were excluded in addition to excluding larger mammals. Exclusions resulted in a changed abiotic soil environment that only affected nematodes in the short-grass vegetation. In each vegetation type, exclusion effects on nematode abundances were mediated by different drivers related to plant quantity and quality. In the short-grass vegetation, not all exclusion effects on omni–carnivorous nematodes were mediated by the abundance of lower trophic level nematodes, suggesting that omni–carnivores also depended on other prey than nematodes.

    We conclude that small aboveground herbivores have major impacts on the soil food web of subalpine short- and tall-grass ecosystems. Excluding aboveground animals caused similar shifts in soil nematode assemblages in both subalpine vegetation types, however, mechanisms turned out to be system-specific.
  • Aquatic Botany

    Effects of temperature, moisture and soil type on seedling emergence and mortality of riparian plant species

    Gerard N.J. Ter Heerdt, Ciska Veen, Wim H. van der Putten, Jan P. Bakker
    Abstract Restoration of riparian plant communities on bare soil requires germination of seeds and establishment of seedlings. However, species that are present in the soil seed bank do not always establish in the vegetation. Temperature, moisture conditions and soil type could play a major role in the establishment of riparian plant communities, through impacting seedling emergence. We studied the effects of temperature, combinations of temperature and moisture conditions, and soil type on seedling emergence and mortality of perennial reeds (Typha latifolia and Phragmites australis) and annual or biannual pioneer species (Senecio congestus, Rumex maritimus and Chenopodium rubrum). The responses to the environmental conditions were species-specific and resulted in context-dependent differences in proportions of species emerging from the soil seed bank. Typha latifolia and S. congestus preferred wet or very wet conditions, C. rubrum and R. maritimus preferred dry to very dry conditions. Phragmites australis was able to establish under all conditions. Both cold and very dry conditions resulted in low emergence and survival, which was not fully compensated for when conditions became favorable again. Senecio congestus, R. maritimus and C. rubrum benefitted from secondary seedling emergence when, after a very dry period, the weather became very wet again, while T. latifolia and P. australis remained absent. When the conditions remained wet, more seedlings emerged from sand than from clay. However, when the soil was drying out, fewer seedlings emerged from sand than from clay. We propose that using information on plant species-specific responses to abiotic environmental conditions during germination, emergence and establishment can help to restore different target riparian plant communities.
  • Frontiers in Plant Science

    Belowground plant-herbivore interactions vary among climate-driven range-expanding plant species with different degrees of novel chemistry

    Rutger Wilschut, J.C. Pereira da Silva, Paolina Garbeva, Wim H. van der Putten
    An increasing number of studies reports plant range expansions to higher latitudes and altitudes in response to global warming. However, consequences for interactions with other species in the novel ranges are poorly understood. Here, we examine how range-expanding plant species interact with root-feeding nematodes from the new range. Root-feeding nematodes are ubiquitous belowground herbivores that may impact the structure and composition of natural vegetation. Because of their ecological novelty, we hypothesized that range-expanding plant species will be less suitable hosts for root-feeding nematodes than native congeneric plant species. In greenhouse and lab trials we compared nematode preference and performance of two root-feeding nematode species between range-expanding plant species and their congeneric natives. In order to understand differences in nematode preferences, we compared root volatile profiles of all range expanders and congeneric natives. Nematode preferences and performances differed substantially among the pairs of range-expanders and natives. The range-expander that had the most unique volatile profile compared to its related native was unattractive and a poor host for nematodes. Other range-expanding plant species that differed less in root chemistry from native congeners, also differed less in nematode attraction and performance. We conclude that the three climate-driven range-expanding plant species studied varied considerably in their chemical novelty compared to their congeneric natives, and therefore affected native root-feeding nematodes in species-specific ways. Our data suggest that through variation in chemical novelty, range-expanding plant species may vary in their impacts on belowground herbivores in the new range.
  • Ecology

    Low abundant soil bacteria can be metabolically versatile and fast growing

    Viola Kurm, Wim H. van der Putten, Wietse de Boer, Suzanne M.H. Naus-Wiezer, (Gera) W.H.G. Hol
    The abundance of species is assumed to depend on their life history traits, such as growth rate and resource specialization. However, this assumption has not been tested for bacteria. Here we investigate how abundance of soil bacteria relates to slow growth and substrate specialization (oligotrophy) versus fast growth and substrate generalization (copiotrophy). We collected 47 saprotrophic soil bacterial isolates of differing abundances and measured their growth rate and the ability to use a variety of single carbon sources. Opposite to our expectation, there was no relationship between abundance in soil and the measured growth rate or substrate utilization profile (SUP). However, isolates with lower growth rates used fewer substrates than faster growing ones supporting the assumption that growth rate may relate to substrate specialization. Interestingly, growth rate and SUP were correlated with phylogeny, rather than with abundance in soil. Most markedly, Gammaproteobacteria on average grew significantly faster and were able to use more substrates than other bacterial classes, whereas Alphaproteobacteria were growing relatively slowly and used fewer substrates. This finding suggests that growth and substrate utilization are phylogenetically deeply conserved.

    We conclude that growth rate and substrate utilization of soil bacteria are not general determinants of their abundance. Future studies on explaining bacterial abundance need to determine how other factors, such as competition, predation and abiotic factors may contribute to rarity or abundance in soil bacteria.
  • Ecosphere

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

    Roeland Cortois, Ciska Veen, Henk Duyts, M. Abbas, T Strecker, Olga Kostenko, Nico Eisenhauer, S. Scheu, G. Gleixner, Gerlinde De Deyn, Wim H. van der Putten
    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 microbial-feeding 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.
  • Molecular Ecology

    Differential responses of soil bacteria, fungi, archaea and protists to plant species richness and plant functional group identity

    Sigrid Dassen, Roeland Cortois, Henk Martens, Mattias De Hollander, George Kowalchuk, Wim H. van der Putten, Gerlinde De Deyn
    Plants are known to influence belowground microbial community structure along their roots, but the impacts of plant species richness and plant functional group (FG) identity on microbial communities in the bulk soil are still not well understood. Here, we used 454-pyrosequencing to analyse the soil microbial community composition in a long-term biodiversity experiment at Jena, Germany. We examined responses of bacteria, fungi, archaea, and protists to plant species richness (communities varying from 1-60 sown species) and plant FG identity (grasses, legumes, small herbs, tall herbs) in bulk soil. We hypothesised that plant species richness and FG identity would alter microbial community composition and have a positive impact on microbial species richness. Plant species richness had a marginal positive effect on the richness of fungi, but we observed no such effect on bacteria, archaea, and protists. Plant species richness also did not have a large impact on microbial community composition. Rather, abiotic soil properties partially explained the community composition of bacteria, fungi, arbuscular mycorrhizal fungi (AMF), archaea, and protists. Plant FG richness did not impact microbial community composition, however plant FG identity was more effective. Bacterial richness was highest in legume plots and lowest in small herb plots, and AMF and archaeal community composition in legume plant communities was distinct from that in communities composed of other plant FGs. We conclude that soil microbial community composition in bulk soil is influenced more by changes in plant FG composition and abiotic soil properties, than by changes in plant species richness per se.
  • Nature Ecology and Evolution

    A test of the hierarchical model of litter decomposition

    Mark Bradford, Ciska Veen, A. Bonis, E.M. Bradford, A. T. Classen, J.H.C. Cornelissen, Tom Crowther, J.R. De Long, G.T. Freschet, Paul Kardol, Marta Manrubia-Freixa, Daniel S. Maynard, G.S. Newman, R. Van Logtestijn, Maria Viketoft, David A. Wardle, W.R. Wieder, S.A. Wood, Wim H. van der Putten
    Our basic understanding of plant litter decomposition informs the assumptions underlying widely applied soil biogeochemical models, including those embedded in Earth system models. Confidence in projected carbon cycle–climate feedbacks therefore depends on accurate knowledge about the controls regulating the rate at which plant biomass is decomposed into products such as CO2. Here we test underlying assumptions of the dominant conceptual model of litter decomposition. The model posits that a primary control on the rate of decomposition at regional to global scales is climate (temperature and moisture), with the controlling effects of decomposers negligible at such broad spatial scales. Using a regional-scale litter decomposition experiment at six sites spanning from northern Sweden to southern France—and capturing both within and among site variation in putative controls—we find that contrary to predictions from the hierarchical model, decomposer (microbial) biomass strongly regulates decomposition at regional scales. Furthermore, the size of the microbial biomass dictates the absolute change in decomposition rates with changing climate variables. Our findings suggest the need for revision of the hierarchical model, with decomposers acting as both local- and broad-scale controls on litter decomposition rates, necessitating their explicit consideration in global biogeochemical models.
  • 2017

    Soil Biodiversity and Ecosystem Functioning

    Richard D. Bardgett, Franciska T. De Vries, Wim H. van der Putten

    Changing soil legacies to direct restoration of plant communities

    Pella Brinkman, Ciska Raaijmakers, Wietse de Boer, Wim H. van der Putten
    It is increasingly acknowledged that soil biota may influence interactions among plant species, however, little is known about how to change historical influences of previous land management on soil biota, the so-called ‘biotic soil legacy effect’. We used a two-phase plant community-soil feedback approach to study how plant species typical to original (i.e. undisturbed) and degraded fen meadows may influence effects of the soil community on Carex species that are dominant in fen meadows. In phase one, soil from original, degraded, successfully and unsuccessfully restored fen meadows was conditioned by growing plants typical to original or to degraded fen meadows. In phase two, interactions between Carex and neighbouring plant species were studied to quantify plant community-soil feedback effects in different neighbour plant mixtures. Soil conditioning with plants typical to original fen meadows resulted in significantly more Carex biomass than with plants typical to degraded fen meadows. These effects were strongest when the soil originated from unsuccessfully restored fen meadows. However, biomass of plants typical of degraded fen meadows was also higher in soil conditioned by typical fen meadow plants. We conclude that soil legacy effects of plants from degraded fen meadows can be altered by growing typical fen meadow plant species in that soil, as this enhances priority effects that favour growth of other typical fen meadow plants. As also plant species from degraded fen meadows benefitted from soil conditioning, further studies are needed to reveal if plant species can be chosen that change negative soil legacy effects for rare and endangered fen meadow plant species, but not for plant species that are typical to degraded fen meadows.
  • PLoS One

    Soil pathogen-aphid interactions under differences in soil organic matter and mineral fertilizer

    Stijn van Gils, Giovanni Tamburini, Marini Lorenzo, Arjen Biere, Maaike Van Agtmaal, Olaf Tyc, Martine Kos, David Kleijn, Wim H. van der Putten
    There is increasing evidence showing that microbes can influence plant-insect interactions. In addition, various studies have shown that aboveground pathogens can alter the interactions between plants and insects. However, little is known about the role of soil-borne pathogens in plant-insect interactions. It is also not known how environmental conditions, that steer the performance of soil-borne pathogens, might influence these microbe-plant-insect interactions. Here, we studied effects of the soil-borne pathogen Rhizoctonia solani on aphids (Sitobion avenae) using wheat (Triticum aestivum) as a host.

    In a greenhouse experiment, we tested how different levels of soil organic matter (SOM) and fertilizer addition influence the interactions between plants and aphids. To examine the influence of the existing soil microbiome on the pathogen effects, we used both unsterilized field soil and sterilized field soil.

    In unsterilized soil with low SOM content, R. solani addition had a negative effect on aphid biomass, whereas it enhanced aphid biomass in soil with high SOM content. In sterilized soil, however, aphid biomass was enhanced by R. solani addition and by high SOM content. Plant biomass was enhanced by fertilizer addition, but only when SOM content was low, or in the absence of R. solani.

    We conclude that belowground pathogens influence aphid performance and that the effect of soil pathogens on aphids can be more positive in the absence of a soil microbiome. This implies that experiments studying the effect of pathogens under sterile conditions might not represent realistic interactions. Moreover, pathogen-plant-aphid interactions can be more positive for aphids under high SOM conditions. We recommend that soil conditions should be taken into account in the study of microbe-plant-insect interaction
  • New Phytologist

    Soil handling methods should be selected based on research questions and goals

    Michael J. Gundale, David A. Wardle, Paul Kardol, Wim H. van der Putten, Richard W. Lucas
  • Nature Communications

    Soil networks become more connected and take up more carbon as nature restoration progresses

    Elly Morrien, Emilia Hannula, Basten Snoek, Nico Helmsing, Hans Zweers, Mattias De Hollander, Raquel Lujan Soto, M.L. Bouffaud, M. Buée, Wim Dimmers, Henk Duyts, Stefan Geisen, M. Girlanda, R.I. Griffiths, H-B. Jørgensen, J. Jensen, Pierre Plassart, Dirk Redecker, R.M. Schmelz, O. Schmidt, B.C. Thomson, Emilie Tisserant, S. Uroz, A. Winding, M.J. Bailey, M. Bonkowski, Jack H. Faber, F. Martin, P. Lemanceau, Wietse de Boer, Hans van Veen, Wim H. van der Putten
    Soil organisms have an important role in aboveground community dynamics and ecosystem functioning in terrestrial ecosystems. However, most studies have considered soil biota as a black box or focussed on specific groups, whereas little is known about entire soil networks. Here we show that during the course of nature restoration on abandoned arable land a compositional shift in soil biota, preceded by tightening of the belowground networks, corresponds with enhanced efficiency of carbon uptake. In mid- and long-term abandoned field soil, carbon uptake by fungi increases without an increase in fungal biomass or shift in bacterial-to-fungal ratio. The implication of our findings is that during nature restoration the efficiency of nutrient cycling and carbon uptake can increase by a shift in fungal composition and/or fungal activity. Therefore, we propose that relationships between soil food web structure and carbon cycling in soils need to be reconsidered
  • Plant and Soil

    Timing of simulated aboveground herbivory influences population dynamics of root-feeding nematodes

    Minggang Wang, Arjen Biere, Wim H. van der Putten, T. Martijn Bezemer, Pella Brinkman

    Plant damage inflicted by aboveground herbivores can occur at different stages of plant development and can induce plant responses that affect the growth of belowground herbivores. This study explores impacts of aboveground herbivory at different plant development stages on the population dynamics of root-feeding nematodes.


    We simulated aboveground herbivory by clipping the foliage of the grass species Holcus lanatus, and tested how plant defoliation at different times (1, 4 or 7 weeks after nematode inoculation) influenced the population of two root-feeding nematode species: the endoparasitic Pratylenchus penetrans and the ectoparasitic Tylenchorhynchus dubius.


    Defoliation increased the total abundance of P. penetrans and the number per unit root mass (density) of both P. penetrans and T. dubius. Defoliation enhanced the density of P. penetrans, however, only when plants were defoliated early. Timing did not influence the density of T. dubius, although both abundance and density increased over time. Defoliation increased the nitrogen concentration of plant roots, but reduced root biomass. The strongest reduction of root biomass occurred after early defoliation.


    Our study indicates that plant responses to aboveground herbivory and their effects on belowground herbivores can be influenced by the time when plants are defoliated, as well as by the belowground herbivore species and their interactions.
  • Global Change Biology Bioenergy

    Effects of bio-based residue amendments on greenhouse gas emission from agricultural soil are stronger than effects of soil type with different microbial community composition.

    Adrian Ho, Umer Zeeshan Ijaz, Thierry Janssens, Rienke Ruijs, Sang Yoon Kim, Wietse de Boer, Aad J Termorshuizen, Wim H. van der Putten, Paul Bodelier
    With the projected rise in the global human population, agriculture intensification and land-use conversion to arable fields is anticipated to meet the food and bio-energy demand to sustain a growing population. Moving towards a circular economy, agricultural intensification results in the increased re-investment of bio-based residues in agricultural soils, with consequences for microbially-mediated greenhouse gas (GHG) emission, as well as other aspects of soil functioning. To date, systematic studies to address the impact of bio-based residue amendment on the GHG balance, including the soil microorganisms, and nutrient transformation in agricultural soils are scarce. Here, we assess the Global Warming Potential (GWP) of in-situ GHG (i.e. CO2, CH4, and N2O) fluxes after application of six bio-based residues with broad C:N ratios (5-521) in two agricultural soils (sandy loam and clay; representative of vast production areas in north-western Europe). We relate the GHG emission to the decomposability of the residues in a litter bag assay, and determined the effects of residue input on crop (common wheat) growth after incubation. The shift in the bacterial community composition and abundance was monitored using IonTorrentTM sequencing and qPCR, respectively by targeting the 16S rRNA gene. The decomposability of the residues, independent of C:N ratio, was proportional to the GWP derived from the GHG emitted. The soils harbored distinct bacterial communities, but responded similarly to the residue amendments, because both soils exhibited the highest mean GWP after addition of the same residues (sewage sludge, aquatic plant material, and compressed beet leaves). Our results question the extent of using the C:N ratio alone to predict residue-induced response in GHG emission. Taken together, we show that although soil properties strongly affect the bacterial community composition, microbially-mediated GHG emission is residue-dependent.
  • Frontiers in Microbiology

    Seed and root endophytic fungi in a range expanding and a related plant species

    Stefan Geisen, Olga Kostenko, Mark C. Cnossen, Freddy ten Hooven, Branko Vreš, Wim H. van der Putten
    Climate change is accelerating the spread of plants and their associated species to new ranges. The differences in range shift capacity of the various types of species may disrupt long-term co-evolved relationships especially those belowground, however, this may be less so for seed-borne endophytic microbes. We collected seeds and soil of the range-expanding Centaurea stoebe and the congeneric C. jacea from three populations growing in Slovenia (native range of both Centaurea species) and the Netherlands (expanded range of C. stoebe, native range of C. jacea). We isolated and identified endophytic fungi directly from seeds, as well as from roots of the plants grown in Slovenian, Dutch or sterilized soil to compare fungal endophyte composition. Furthermore, we investigated whether C. stoebe hosts a reduced community composition of endophytes in the expanded range due to release from plant-species specific fungi while endophyte communities in C. jacea in both ranges are similar.We cultivated 46 unique and phylogenetically diverse endophytes. A majority of the seed endophytes resembled potential pathogens, while most root endophytes were not likely to be pathogenic. Only one endophyte was found in both roots and seeds, but was isolated from different plant species. Unexpectedly, seed endophyte diversity of southern C. stoebe populations was lower than of populations from the north, while the seed endophyte community composition of northern C. stoebe populations was significan...
  • ISME Journal

    Shifts in rhizosphere fungal community during secondary succession following abandonment from agriculture

    Emilia Hannula, Elly Morrien, Mattias De Hollander, Wim H. van der Putten, Hans van Veen, Wietse de Boer
    Activities of rhizosphere microbes are key to the functioning of terrestrial ecosystems. It is commonly believed that bacteria are the major consumers of root exudates and that the role of fungi in the rhizosphere is mostly limited to plant-associated taxa, such as mycorrhizal fungi, pathogens and endophytes, whereas less is known about the role of saprotrophs. In order to test the hypothesis that the role of saprotrophic fungi in rhizosphere processes increases with increased time after abandonment from agriculture, we determined the composition of fungi that are active in the rhizosphere along a chronosequence of ex-arable fields in the Netherlands. Intact soil cores were collected from nine fields that represent three stages of land abandonment and pulse labeled with 13CO2. The fungal contribution to metabolization of plant-derived carbon was evaluated using phospholipid analysis combined with stable isotope probing (SIP), whereas fungal diversity was analyzed using DNA-SIP combined with 454-sequencing. We show that in recently abandoned fields most of the root-derived 13C was taken up by bacteria but that in long-term abandoned fields most of the root-derived 13C was found in fungal biomass. Furthermore, the composition of the active functional fungal community changed from one composed of fast-growing and pathogenic fungal species to one consisting of beneficial and slower-growing fungal species, which may have essential consequences for the carbon flow through the soil food web and consequently nutrient cycling and plant succession.
  • Journal of Ecology

    Plant-soil feedbacks: role of plant functional group and plant traits

    Roeland Cortois, T. Schröder-Georgi, A. Weigelt, Wim H. van der Putten, Gerlinde De Deyn
    Plant-soil feedback (PSF), plant trait and functional group concepts advanced our understanding of plant community dynamics, but how they are interlinked is poorly known. To test how plant functional groups (FGs: graminoids, small herbs, tall herbs, legumes) and plant traits relate to PSF, we grew 48 grassland species in sterilized soil, sterilized soil with own species soil inoculum and sterilized soil with soil inoculum from all species, and quantified relative growth rate (RGR), specific leaf area (SLA), specific root length (SRL) and per cent arbuscular mycorrhizal fungi colonization (%AMF). Plant growth response to the plant species' own soil biota relative to sterilized soil (PSFsterilized) reflects net effects of all (generalist+specialized) soil biota. Growth response to the plant species' own soil biota relative to soil biota of all plant species (PSFaway) reveals effects of more specialized soil organisms. PSFsterilized showed that graminoids and small herbs have a negative and tall herbs a positive response to their own soil biota, whereas legumes responded neutrally. However, PSFaway showed that on average, all plant FGs benefitted from growing with other species' soil biota, suggesting that pathogens are more specialized than plant growth-promoting soil biota. Feedback to plant growth from all soil biota (PSFsterilized) was stronger than from more specialized soil biota (PSFaway) and could be predicted by SRL and especially by %AMF colonization. Species with high SRL and low %AMF colonization when grown in away soil experienced most negative soil feedback.Synthesis. Plant species from all plant FGs grow better in soil from other species because of less net negative effects of soil biota (in graminoids), or because of more net positive soil biota effects (in tall herbs). Explorative plant species (high SRL, low %AMF colonization) suffer most from negative feedback of all soil biota, whereas more resource conservative species (low SRL, high %AMF colonization) benefit from soil feedback of all soil biota. These findings help to understand replacement of explorative species during succession. Moreover, we suggest a potentially larger role for species with positive feedback than for species with negative feedback to contribute to maintain plant community productivity of diverse communities over time.
  • Journal of Biogeography

    Trifolium species associate with a similar richness of soil-borne mutualists in their introduced and native ranges

    Kevin J. McGinn, Wim H. van der Putten, Richard P. Duncan, Natasha Shelby, Carolin Weser, Philip E. Hulme
  • Nature Plants

    Soil inoculation steers restoration of terrestrial ecosystems

    Jasper Wubs, Wim H. van der Putten, M. Bosch, T. Martijn Bezemer
    Many natural ecosystems have been degraded because of human activities1,2 and need to be restored so that biodiversity is protected. However, restoration can take decades and restoration activities are often unsuccessful3 because of abiotic constraints (for example, eutrophication, acidification) and unfavourable biotic conditions (for example, competition or adverse soil community composition). A key question is what manageable factors prevent transition from degraded to restored ecosystems and what interventions are required for successful restoration2,4. Experiments have shown that the soil community is an important driver of plant community development5,​6,​7,​8, suggesting that manipulation of the soil community is key to successful restoration of terrestrial ecosystems3,9. Here we examine a large-scale, six-year-old field experiment on ex-arable land and show that application of soil inocula not only promotes ecosystem restoration, but that different origins of soil inocula can steer the plant community development towards different target communities, varying from grassland to heathland vegetation. The impact of soil inoculation on plant and soil community composition was most pronounced when the topsoil layer was removed, whereas effects were less strong, but still significant, when the soil inocula were introduced into intact topsoil. Therefore, soil inoculation is a powerful tool to both restore disturbed terrestrial ecosystems and steer plant community development.
  • Functional Ecology

    Where, when and how plant-soil feedback matters in a changing world

    Wim H. van der Putten, Mark Bradford, Pella Brinkman, Tess Van de Voorde, Ciska Veen
    It is increasingly acknowledged that plant-soil feedbacks may play an important role in driving the composition of plant communities and functioning of terrestrial ecosystems. However, the mechanistic understanding of plant-soil feedbacks, as well as their roles in natural ecosystems in proportion to other possible drivers, is still in its infancy. Such knowledge will enhance our capacity to determine the contribution of plant-soil feedback to community and ecosystem responses under global environmental change. Here, we review how plant-soil feedbacks may develop under extreme drought and precipitation events, CO2 and nitrogen enrichment, temperature increase, land use change and plant species loss vs. gain. We present a framework for opening the black box of soil' considering the responses of the various biotic components (enemies, symbionts and decomposers) of plant-soil feedback to the global environmental changes, and we discuss how to integrate these components to understand and predict the net effects of plant-soil feedbacks under the various scenarios of change. To gain an understanding of how plant-soil feedback plays out in realistic settings, we also use the framework to discuss its interaction with other drivers of plant community composition, including competition, facilitation, herbivory, and soil physical and chemical properties. We conclude that understanding the role that plant-soil feedback plays in shaping the responses of plant community composition and ecosystem processes to global environmental changes requires unravelling the individual contributions of enemies, symbionts and decomposers. These biotic factors may show different response rates and strengths, thereby resulting in different net magnitudes and directions of plant-soil feedbacks under various scenarios of global change. We also need tests of plant-soil feedback under more realistic conditions to determine its contribution to changes in patterns and processes in the field, both at ecologically and evolutionary relevant time-scales.
  • Journal of Ecology

    Plant mutualisms with rhizosphere microbiota in introduced versus native ranges

    Natasha Shelby, Richard P. Duncan, Wim H. van der Putten, Kevin J. McGinn, Carolin Weser, Philip E. Hulme
    * The performance of introduced plants can be limited by the availability of soil mutualists outside their native range, but how interactions with mutualists differ between ranges is largely unknown. If mutualists are absent, incompatible or parasitic, plants may compensate by investing more in root biomass, adapting to be more selective or by maximizing the benefits associated with the mutualists available. * We tested these hypotheses using seven non-agricultural species of Trifolium naturalized in New Zealand (NZ). We grew seeds from two native (Spain, UK) and one introduced (NZ) provenance of each species in glasshouse pots inoculated with rhizosphere microbiota collected from conspecifics in each region. * We compared how plant biomass, degree of colonization by rhizobia and arbuscular mycorrhizal fungi (AMF), and the growth benefit associated with each mutualist differed between provenances (native and introduced populations) when grown with soil microbiota from each region. We also tested whether the growth benefit of colonization by mutualists was correlated with the extent to which alien plants were distributed in the introduced range. * Rhizobia colonization was generally lower among introduced relative to native provenances. In NZ soils, 9% of all plants lacked rhizobia and 16% hosted parasitic nodules, whereas in native-range soils, there was no evidence of parasitism and all but one plant hosted rhizobia. Growth rates as a factor of rhizobia colonization were always highest when plants were grown in soil from their home range. Colonization by AMF was similar for all provenances in all soils but for four out of seven species grown in NZ soils, the level of AMF colonization was negatively correlated with growth rate. In general, introduced provenances did not compensate for lower growth rates or lower mutualist associations by decreasing shoot–root ratios. * Synthesis. Despite differences between introduced and native provenances in their associations with soil mutualists and substantial evidence of parasitism in the introduced range, neither level of colonization by mutualists nor the growth benefit associated with colonization was correlated with the extent of species’ distributions in the introduced range, suggesting mutualist associations are not predictive of invasion success for these species.
  • Oecologia

    Herbivory and dominance shifts among exotic and congeneric native plant species during plant community establishment

    T. Engelkes, Annelein Meisner, Elly Morrien, Olga Kostenko, Wim H. van der Putten, Mirka Macel
    Invasive exotic plant species often have fewer natural enemies and suffer less damage from herbivores in their new range than genetically or functionally related species that are native to that area. Although we might expect that having fewer enemies would promote the invasiveness of the introduced exotic plant species due to reduced enemy exposure, few studies have actually analyzed the ecological consequences of this situation in the field. Here, we examined how exposure to aboveground herbivores influences shifts in dominance among exotic and phylogenetically related native plant species in a riparian ecosystem during early establishment of invaded communities. We planted ten plant communities each consisting of three individuals of each of six exotic plant species as well as six phylogenetically related natives. Exotic plant species were selected based on a rapid recent increase in regional abundance, the presence of a congeneric native species, and their co-occurrence in the riparian ecosystem. All plant communities were covered by tents with insect mesh. Five tents were open on the leeward side to allow herbivory. The other five tents were completely closed in order to exclude insects and vertebrates. Herbivory reduced aboveground biomass by half and influenced which of the plant species dominated the establishing communities. Exposure to herbivory did not reduce the total biomass of natives more than that of exotics, so aboveground herbivory did not selectively enhance exotics during this early stage of plant community development. Effects of herbivores on plant biomass depended on plant species or genus but not on plant status (i.e., exotic vs native). Thus, aboveground herbivory did not promote the dominance of exotic plant species during early establishment of the phylogenetically balanced plant communities.
  • Global Change Biology Bioenergy

    Effects of first- and second-generation bioenergy crops on soil processes and legacy effects on a subsequent crop

    Maarten Schrama, Bart Vandecasteele, Sabrina Almeida de Carvalho, Hilde Muylle, Wim H. van der Putten
    To develop a more sustainable bio-based economy, an increasing amount of carbon for industrial applications and biofuel will be obtained from bioenergy crops. This may result in intensified land use and potential conflicts with other ecosystem services provided by soil, such as control of greenhouse gas emissions, carbon sequestration, and nutrient dynamics. A growing number of studies examine how bioenergy crops influence carbon and nitrogen cycling. Few studies, however, have combined such assessments with analysing both the immediate effects on the provisioning of soil ecosystem services as well as the legacy effects for subsequent crops in the rotation. Here, we present results from field and laboratory experiments on effects of a standard first-generation bioenergy crop (maize) and three different second-generation bioenergy crops (willow short rotation coppice (SRC), Miscanthus × giganteus, switchgrass) on key soil quality parameters: soil structure, organic matter, biodiversity and growth and disease susceptibility of a major follow-up crop, wheat (Triticum aestivum). We analysed a 6-year field experiment and show that willow SRC, Miscanthus, and maize maintained a high yield over this period. Soil quality parameters and legacy effects of Miscanthus and switchgrass were similar or performed worse than maize. In contrast, willow SRC enhanced soil organic carbon concentration (0–5 cm), soil fertility, and soil biodiversity in the upper soil layer when compared to maize. In a greenhouse experiment, wheat grown in willow soil had higher biomass production than when grown in maize or Miscanthus soil and exhibited no growth reduction in response to introduction of a soil-borne (Rhizoctonia solani) or a leaf pathogen (Mycosphaerella graminicola). We conclude that the choice of bioenergy crops can greatly influence provisioning of soil ecosystem services and legacy effects in soil. Our results imply that bioenergy crops with specific traits might even enhance ecosystem properties through positive legacy effects.
  • SOIL Discussions

    FORUM paper: The significance of soils and soil science towards realization of the UN sustainable development goals (SDGs)

    S. D. Keesstra, J. Bouma, J. Wallinga, P. Tittonell, Pete Smith, A. Cerdà, L. Montanarella, J. Quinton, Y. Pachepsky, Wim H. van der Putten, Richard D. Bardgett, S. Moolenaar, G. Mol, L. O Fresco
  • Applied Soil Ecology

    Organic farming practices result in compositional shifts in nematode communities that exceed crop-related changes

    Casper W. Quist, Maarten Schrama, Janjo J. de Haan, Geert Smant, Jaap Bakker, Wim H. van der Putten, Johannes Helder
    Intensification of conventional agriculture has resulted in a decline of soil ecosystem functioning. Organic agriculture intends to manage soil biota in a manner that is more geared towards adequate cycling of nutrients with minimal losses. Ecological interpretation of agricultural practices-induced shifts in primary decomposers, bacteria and fungi, is non-trivial due to their enormous biodiversity. Bacterivorous and fungivorous nematodes feed selectively on these microorganisms, and we intended to test whether farming system effects are mirrored in compositional changes in nematode communities. Therefore, we analysed the impact of three farming systems, conventional (ConMin), integrated (ConSlu) and organic (Organic), on nematode communities in the southeastern part of The Netherlands on a sandy soil with 3–5% organic matter. Effects of each farming system were assessed for four different crops (barley, maize, pea or potato) by a series of taxon-specific quantitative PCRs (qPCR). Changes in community structure analysed by nonmetric multidimensional scaling (NMDS) showed that organic farming resulted in specific shifts in nematode community composition exceeding crop-related assemblage shifts. Three out of thirteen quantified nematode taxa showed significant farming system effects. Strongest effects were observed for the (putative) bacterivore Prismatolaimus, which was relatively common in Organic fields and nearly absent in ConMin and ConSlu fields. A reverse effect was observed for Pristionchus; this necromenic bacterivore and facultative predator made up about 21% and 7% of the total nematode community in respectively ConMin and ConSlu fields, whereas it was nearly absent from Organic fields. The observed farming system effects suggest that specific nematode taxa might be indicative for the impact of farming practices on soil biota.
  • Journal of Applied Ecology

    Can above-ground ecosystem services compensate for reduced fertilizer input and soil organic matter in annual crops?

    Stijn van Gils, Wim H. van der Putten, David Kleijn
    1.Above-ground and below-ground environmental conditions influence crop yield by pollination, pest pressure, and resource supply. However, little is known about how interactions between these factors contribute to yield. Here, we used oilseed rape Brassica napus to test their effects on crop yield.2.We exposed potted plants to all combinations of high and low levels of soil organic matter (SOM) and fertilizer supply, and placed all treatments at a variety of field sites representing a gradient in pollinator visitation rate and pest exposure. We determined the relative contribution of pollinators and pests, SOM and fertilizer supply to yield. We also tested whether SOM can moderate effects of fertilizer on yield and whether soil conditions influence the relationship between above-ground conditions and yield.3.Increases in pollinator visitation rate and decreases in pest pressure enhanced yield more than increase of fertilizer supply. Although higher SOM content resulted in plants with more biomass and flowers, under our experimental conditions SOM neither enhanced yield, nor influenced effects of fertilizer, pollinators or pests on yield.4.The relationships between yield, pollinator visitation rate and pest pressure did not depend on the level of fertilization suggesting that the effects of fertilizer application and above-ground (dis)services on yield were additive. In contrast, pollinator visitation rate was more strongly related to yield at low pest pressure than at high pest pressure indicating trade-offs between above-ground services and disservices.5.Synthesis and applications. Our results show that it is possible to increase oilseed rape yield by enhancing pollination, irrespective of supplying mineral fertilizer. Moreover, the fact that below-ground conditions did not alter the effect of above-ground conditions, suggests that farmers may obtain even higher yields by maximizing both above-ground ecosystem services and external inputs. Further studies are needed to understand at which point the positive relationships between pollinator visitation and yield, as well as between fertilizer and yield will level off. Considering above-ground and below-ground services and inputs in agro-ecosystems in conjunction is crucial in order to optimize external inputs for crop yield from an economic and ecological perspective.This article is protected by copyright. All rights reserved.
  • Soil Biology & Biochemistry

    Interspecific differences in nematode control between range-expanding plant species and their congeneric natives

    Rutger Wilschut, Stefan Geisen, Freddy ten Hooven, Wim H. van der Putten
    Climate change enables range expansions of plants, animals and microbes to higher altitudes and latitudes. Plants may benefit from range expansion when they escape from natural enemies. However, range expansion becomes a disadvantage when plants become disconnected from organisms that control enemies in the new range. Here, we examined nematode control in the root zone of range-expanding plant species and congeneric natives. In a greenhouse, we determined bottom-up (by the plants) and top-down (by natural enemies of the nematodes) control of two root-feeding nematode species (Helicotylenchus pseudorobustus and Meloidogyne hapla) in the rhizospheres of two range-expanding plant species, Centaurea stoebe and Geranium pyrenaicum, and two congeneric natives, Centaurea jacea and Geranium molle. Pots with plants growing in sterilized soil were inoculated with either a microbial soil community from the newly colonized natural habitat, a mixture of native microbial nematode antagonists, or a combination of these two communities. We tested the hypotheses that bottom-up control of root-feeding nematodes would be strongest in the root zone of range expanders and that top-down control would be strongest in the root zone of native plant species. We observed profound intra- and interspecific differences in bottom-up and top-down control among all four plant species. Bottom-up control by the range-expanding plant species was either strong or weak. Top-down control by microbes was strongest in native Centaurea. The addition of a mixture of both microbial communities reduced control of M. hapla in the root zones of the native plant species, and enhanced its control in the root zones of range-expanding plant species. We conclude that there was species-specific bottom-up and top-down control of root-feeding nematodes among the four plant species tested. Range-expanding plant species influenced their microbial rhizosphere community differently compared to native plant species, but top-down control in the root zone of natives was not systematically superior to that of range-shifting plant species.
  • New Phytologist

    Pampered inside, pestered outside? Differences and similarities between plants growing in controlled conditions and in the field.

    H. Poorter, F. Fiorani, R. Pieruschka, T. Wojciechowski, Wim H. van der Putten, Michael Kleyer, U. Schurr, J. Postma
    Plant biologists often grow plants in growth chambers or glasshouses with the ultimate aim to understand or improve plant performance in the field. What is often overlooked is how results from controlled conditions translate back to field situations. A meta-analysis showed that lab-grown plants had faster growth rates, higher nitrogen concentrations and different morphology. They remained smaller, however, because the lab plants had grown for a much shorter time. We compared glasshouse and growth chamber conditions with those in the field and found that the ratio between the daily amount of light and daily temperature (photothermal ratio) was consistently lower under controlled conditions. This may strongly affect a plant's source : sink ratio and hence its overall morphology and physiology. Plants in the field also grow at higher plant densities. A second meta-analysis showed that a doubling in density leads on average to 34% smaller plants with strong negative effects on tiller or side-shoot formation but little effect on plant height. We found the r2 between lab and field phenotypic data to be rather modest (0.26). Based on these insights, we discuss various alternatives to facilitate the translation from lab results to the field, including several options to apply growth regimes closer to field conditions.
  • Landschap

    Natuurherstel door grondtransplantatie

    Jasper Wubs, Wim H. van der Putten, Bosch M., T. Martijn Bezemer

    No difference in the competitive ability of introduced and native Trifolium provenances when grown with soil biota from their introduced and native ranges

    Natasha Shelby, Philip E. Hulme, Wim H. van der Putten, Kevin J. McGinn, Carolin Weser, Richard P. Duncan
    The evolution of increased competitive ability (EICA) hypothesis could explain why some introduced plant species perform better outside their native ranges. EICA proposes that introduced plants escape specialist pathogens or herbivores leading to selection for resources to be reallocated away from defence and toward greater competitive ability. We tested the hypothesis that escape from soil enemies has led to increased competitive ability in three non-agricultural Trifolium (Fabaceae) species native to Europe that were introduced to New Zealand in the 19th century. Trifolium performance is intimately tied to rhizosphere biota. Thus, we grew plants from one introduced (New Zealand) and two native (Spain and the UK) provenances for each of three species in pots inoculated with soil microbiota collected from the rhizosphere beneath conspecifics in the introduced and native ranges. Plants were grown singly and in competition with conspecifics from a different provenance in order to compare competitive ability in the presence of different microbial communities. In contrast to the predictions of the EICA hypothesis, we found no difference in the competitive ability of introduced and native provenances when grown with soil microbiota from either the native or introduced range. Although plants from introduced provenances of two species grew more slowly than native provenances in native-range soils, as predicted by the EICA hypothesis, plants from the introduced provenance were no less competitive than native conspecifics. Overall, the growth rates of plants grown singly was a poor predictor of their competitive ability, highlighting the importance of directly quantifying plant performance in competitive scenarios, rather than relying on surrogate measures such as growth rate.
  • New Phytologist

    Effects of root decomposition on plant–soil feedback of early– and mid–successional plant species.

    Plant–soil feedback (PSF) is an important driver of plant community dynamics. Many studies have emphasized the role of pathogens and symbiotic mutualists in PSFs; however, less is known about the contribution of decomposing litter, especially that of roots.
    We conducted a PSF experiment, where soils were conditioned by living early- and mid-successional grasses and forbs with and without decomposing roots of conspecific species (conditioning phase). These soils were used to test growth responses of conspecific and heterospecific plant species (feedback phase).
    The addition of the roots of conspecifics decreased the biomass of both early- and mid-successional plant species in the conditioning phase. In the feedback phase, root addition had positive effects on the biomass of early-successional species and neutral effects on mid-successional species, except when mid-successional grasses were grown in soils conditioned by conspecifics, where effects were negative. Biomass of early- and mid-successional forbs was generally reduced in soils conditioned by conspecifics.
    We conclude that root decomposition may increase short-term negative PSF effects, but that the effects can become neutral to positive over time, thereby counteracting negative components of PSF. This implies that root decomposition is a key element of PSF and needs to be included in future studies.
  • Journal of Chemical Ecology

    Effects of the Timing of Herbivory on Plant Defense Induction and Insect Performance in Ribwort Plantain (Plantago lanceolata L.) Depend on Plant Mycorrhizal Status

    Minggang Wang, T. Martijn Bezemer, Wim H. van der Putten, Arjen Biere
    Plants often are exposed to antagonistic and symbiotic organisms both aboveground and belowground. Interactions between above- and belowground organisms may occur either simultaneously or sequentially, and jointly can determine plant responses to future enemies. However, little is known about time-dependency of such aboveground-belowground interactions. We examined how the timing of a 24 h period of aboveground herbivory by Spodoptera exigua (1–8 d prior to later arriving conspecifics) influenced the response of Plantago lanceolata and the performance of later arriving conspecifics. We also examined whether these induced responses were modulated by the arbuscular mycorrhizal fungus (AMF) Funneliformis mosseae. The amount of leaf area consumed by later arriving herbivores decreased with time after induction by early herbivores. Mycorrhizal infection reduced the relative growth rate (RGR) of later arriving herbivores, associated with a reduction in efficiency of conversion of ingested food rather than a reduction in relative consumption rates. In non-mycorrhizal plants, leaf concentrations of the defense compound catalpol showed a linear two-fold increase during the eight days following early herbivory. By contrast, mycorrhizal plants already had elevated levels of leaf catalpol prior to their exposure to early herbivory and did not show any further increase following herbivory. These results indicate that AMF resulted in a systemic induction, rather than priming of these defenses. AMF infection significantly reduced shoot biomass of Plantago lanceolata. We conclude that plant responses to future herbivores are not only influenced by exposure to prior aboveground and belowground organisms, but also by when these prior organisms arrive and interact.
  • Ecology

    Aboveground vertebrate and invertebrate herbivore impact on net N mineralization in subalpine grasslands

    Anita C. Risch, Martin Schütz, Martijn L. Vandegehuchte, Wim H. van der Putten, Henk Duyts, Ursina Raschein, Dariusz J. Gwiazdowicz, Matt D. Busse, Deborah S. Page-Dumroese, Stephan Zimmermann
    Aboveground herbivores have strong effects on grassland nitrogen (N) cycling. They can accelerate or slow down soil net N mineralization depending on ecosystem productivity and grazing intensity. Yet, most studies only consider either ungulates or invertebrate herbivores, but not the combined effect of several functionally different vertebrate and invertebrate herbivore species or guilds. We assessed how a diverse herbivore community affects net N mineralization in subalpine grasslands. By using size-selective fences, we progressively excluded large, medium, and small mammals, as well as invertebrates from two vegetation types, and assessed how the exclosure types (ET) affected net N mineralization. The two vegetation types differed in long-term management (centuries), forage quality, and grazing history and intensity. To gain a more mechanistic understanding of how herbivores affect net N mineralization, we linked mineralization to soil abiotic (temperature; moisture; NO3?, NH4+, and total inorganic N concentrations/pools; C, N, P concentrations; pH; bulk density), soil biotic (microbial biomass; abundance of collembolans, mites, and nematodes) and plant (shoot and root biomass; consumption; plant C, N, and fiber content; plant N pool) properties. Net N mineralization differed between ET, but not between vegetation types. Thus, short-term changes in herbivore community composition and, therefore, in grazing intensity had a stronger effect on net N mineralization than long-term management and grazing history. We found highest N mineralization values when only invertebrates were present, suggesting that mammals had a negative effect on net N mineralization. Of the variables included in our analyses, only mite abundance and aboveground plant biomass explained variation in net N mineralization among ET. Abundances of both mites and leaf-sucking invertebrates were positively correlated with aboveground plant biomass, and biomass increased with progressive exclusion. The negative impact of mammals on net N mineralization may be related partially to (1) differences in the amount of plant material (litter) returned to the belowground subsystem, which induced a positive bottom-up effect on mite abundance, and (2) alterations in the amount and/or distribution of dung, urine, and food waste. Thus, our results clearly show that short-term alterations of the aboveground herbivore community can strongly impact nutrient cycling within ecosystems independent of long-term management and grazing history.
  • Soil Biology & Biochemistry

    Legacy effects of elevated ozone on soil biota and plant growth

    Qi Li, Yue Yang, Xuelian Bao, Fang Liu, Wenju Liang, Jianguo Zhu, T. Martijn Bezemer, Wim H. van der Putten
    Abstract Many studies have examined how human-induced atmospheric changes will influence ecosystems. The long-term consequences of human induced climate changes on terrestrial ecosystems may be determined to a large extend by how the belowground compartment will respond to these changes. In a free-air ozone enrichment experiment running for 5 years, we reciprocally transplanted soil cores from ambient and elevated ozone rings to test whether exposure to elevated ozone results in persistent changes in the soil biota when the plant and soil are no longer exposed to elevated ozone, and how these legacy effects of elevated ozone influenced plant growth as compared to current effects of elevated ozone. After one growing season, the current ozone treatment enhanced plant growth, but in soil with a historical legacy of elevated ozone the plant biomass in that soil was reduced compared to the cores originated from ambient rings. Current exposure to ozone increased the phospholipid fatty acids of actinomycetes and protozoa, however, it decreased dissolved organic carbon, bacterivorous and fungivorous nematodes. Interestingly, numbers of bacterivorous and fungivorous nematodes were enhanced when soils with a legacy of elevated ozone were placed under elevated ozone conditions. We conclude that exposure to elevated [O3] results in a legacy effect in soil. This legacy effect most likely influenced plant growth and soil characteristics via responses of bacteria and fungi, and nematodes that feed upon these microbes. These soil legacies induced by changes in soil biotic community after long-term exposure of elevated ozone can alter the responses of ecosystems to current climatic changes.
  • PLoS One

    Herbivory and Stoichiometric Feedbacks to Primary Production

    J.A. Krumins, Valdis Krumins, Eric Forgoston, Lora Billings, Wim H. van der Putten

    Established theory addresses the idea that herbivory can have positive feedbacks on nutrient flow to plants. Positive feedbacks likely emerge from a greater availability of organic carbon that primes the soil by supporting nutrient turnover through consumer and especially microbially-mediated metabolism in the detrital pool. We developed an entirely novel stoichiometric model that demonstrates the mechanism of a positive feedback. In particular, we show that sloppy or partial feeding by herbivores increases detrital carbon and nitrogen allowing for greater nitrogen mineralization and nutritive feedback to plants. The model consists of differential equations coupling flows among pools of: plants, herbivores, detrital carbon and nitrogen, and inorganic nitrogen. We test the effects of different levels of herbivore grazing completion and of the stoichiometric quality (carbon to nitrogen ratio, C:N) of the host plant. Our model analyses show that partial feeding and plant C:N interact because when herbivores are sloppy and plant biomass is diverted to the detrital pool, more mineral nitrogen is available to plants because of the stoichiometric difference between the organisms in the detrital pool and the herbivore. This model helps to identify how herbivory may feedback positively on primary production, and it mechanistically connects direct and indirect feedbacks from soil to plant production.

  • Global Change Biology

    Intensive agriculture reduces soil biodiversity across Europe

    Maria A. Tsiafouli, Elisa Thébault, Stefanos P. Sgardelis, Peter C. De Ruiter, Wim H. van der Putten, Klaus Birkhofer, Lia Hemerik, Franciska T. De Vries, Richard D. Bardgett, Mark Vincent Brady, Lisa Bjornlund, Helene Bracht Jørgensen, Sören Christensen, Tina D'Hertefeldt, Stefan Hotes, (Gera) W.H.G. Hol, Jan Frouz, Mira Liiri, Simon R. Mortimer, Heikki Setälä, Joseph Tzanopoulos, Karoline Uteseny, Václav Pižl, Josef Stary, Volkmar Wolters, Katarina Hedlund
    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. This article is protected by copyright. All rights reserved.
  • Basic and Applied Ecology

    Interspecific competition of early successional plant species in ex-arable fields as influenced by plant-soil feedback

    Jingying Jing, T. Martijn Bezemer, Wim H. van der Putten
    Plant–soil feedback can affect plants that belong to the same (intraspecific feedback) or different species (interspecific feedback). However, little is known about how intra- and interspecific plant–soil feedbacks influence interspecific plant competition. Here, we used plants and soil from early-stage ex-arable fields to examine how intra- and interspecific plant–soil feedbacks affect the performance of 10 conditioning species and the focal species, Jacobaea vulgaris. Plants were grown alone and in competition in both conditioned and control soils. Overall, plant–soil feedback of the 10 plant species influenced the competitiveness of J. vulgaris more strongly than their own competitiveness. However, effects depended on species combination: competitiveness of J. vulgaris was significantly enhanced by interspecific plant–soil feedback from Anthoxanthum odoratum, Agrostis capillaris, and Trifolium dubium, and significantly decreased by interspecific feedback from Achillea millefolium. Intraspecific feedback from Taraxacum officinale and A. odoratum decreased their competitiveness with J. vulgaris. There was a positive relationship between the strength of interspecific feedback and competitiveness of J. vulgaris in conditioned soil. Multiple linear regression showed that the competitiveness of J. vulgaris in conditioned soil was determined by interspecific feedback and competitiveness of neighbour plants. The positive relationship between interspecific feedback and competitiveness in control soil suggests that the soil feedback effect of the competing species on J. vulgaris can build up quickly during competition. We conclude that the effect of plant–soil feedback on interspecific competition may be due to either legacy effects of plant species previously colonizing the soil, or immediate interspecific feedback of the competing plant species via the soil. Therefore, our results suggest that plant–soil feedback can influence interspecific plant competition through a multitude of intra- and interspecific plant–soil interactions both from predecessors, and from the currently competing plant species.
  • 2015

    Towards an integration of biodiversity-ecosystem functioning and food web theory to evaluate relationships between multiple ecosystem services

    Jes Hines, Wim H. van der Putten, Gerlinde De Deyn, Cameron Wagg, Winfried Voigt, Christian Mulder, Wolfgang W. Weisser, Jan Engel, Carlos Melian, Stefan Scheu, Klaus Birkhofer, Anne Ebeling, Christoph Scherber, Nico Eisenhauer
    Ecosystem responses to changes in species diversity are often studied individually. However, changes in species diversity can simultaneously influence multiple interdependent ecosystem functions. Therefore, an important challenge is to determine when and how changes in species diversity that influence one function will also drive changes in other functions. By providing the underlying structure of species interactions, ecological networks can quantify connections between biodiversity and multiple ecosystem functions. Here, we review parallels in the conceptual development of biodiversity–ecosystem functioning (BEF) and food web theory (FWT) research. Subsequently, we evaluate three common principles that unite these two research areas by explaining the patterns, concentrations, and direction of the flux of nutrients and energy through the species in diverse interaction webs. We give examples of combined BEF–FWT approaches that can be used to identify vulnerable species and habitats and to evaluate links that drive trade-offs between multiple ecosystems functions. These combined approaches reflect promising trends towards better management of biodiversity in landscapes that provide essential ecosystem services supporting human well-being.
  • Global Change Biology

    Unexpected stimulation of soil methane uptake as emergent property of agricultural soils following bio-based residue application

    Adrian Ho, A. Reim, Sang Yun Kim, M. Meima-Franke, Aad J Termorshuizen, Wietse de Boer, Wim H. van der Putten, Paul Bodelier
    Intensification of agriculture to meet the global food, feed, and bioenergy demand entail increasing re-investment of carbon compounds (residues) into agro-systems to prevent decline of soil quality and fertility. However, agricultural intensification decreases soil methane uptake, reducing and even causing the loss of the methane sink function. In contrast to wetland agricultural soils (rice paddies), the methanotrophic potential in well-aerated agricultural soils have received little attention, presumably due to the anticipated low or negligible methane uptake capacity in these soils. Consequently, a detailed study verifying or refuting this assumption is still lacking. Exemplifying a typical agricultural practice, we determined the impact of bio-based residue application on soil methane flux, and determined the methanotrophic potential, including a qualitative (diagnostic microarray) and quantitative (group-specific qPCR assays) analysis of the methanotrophic community after residue amendments over two months. Unexpectedly, after amendments with specific residues we detected a significant transient stimulation of methane uptake confirmed by both the methane flux measurements and methane oxidation assay. This stimulation was apparently a result of induced cell-specific activity, rather than growth of the methanotroph population. Although transient, the heightened methane uptake offsets up to 16% of total gaseous CO2 emitted during the incubation. The methanotrophic community, predominantly comprised of Methylosinus may facilitate methane oxidation in the agricultural soils. While agricultural soils are generally regarded as a net methane source or a relatively weak methane sink, our results show that methane oxidation rate can be stimulated, leading to higher soil methane uptake. Hence, even if agriculture exerts an adverse impact on soil methane uptake, implementing carefully designed management strategies (e.g. repeated application of specific residues) may compensate for the loss of the methane sink function following land-use change.
  • Frontiers in Plant Science

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

    (Gera) W.H.G. Hol, Wietse de Boer, Mattias De Hollander, Eiko Kuramae, Annelein Meisner, Wim H. van der Putten
    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.
  • Functional Ecology

    Root responses of grassland species to spatial heterogeneity of plant-soil feedback

    Marloes Hendriks, Eric J. W. Visser, Isabella G. S. Visschers, Bart H. J. Aarts, Hannie de Caluwe, Annemiek E. Smit-Tiekstra, Wim H. van der Putten, Hans de Kroon, Liesje Mommer
    Plant roots selectively forage for soil nutrients when these are heterogeneously distributed. In turn, effects of plant roots on biotic and abiotic conditions in the soil, which result in so-called plant–soil feedback can be heterogeneously distributed as well, but it is unknown how this heterogeneity affects root distribution, nutrient uptake and plant biomass production. Here, we investigate plant root distribution patterns as influenced by spatial heterogeneity of plant–soil feedback in soil and quantify consequences for plant nitrogen uptake and biomass production.
    We conditioned soils by four grassland plant species to obtain ‘own’ and ‘foreign’ soils that differed in biotic conditions similar as is done by the first phase of plant–soil feedback experiments. We used these conditioned soils to create heterogeneous (one patch of own and three patches of foreign soils) or homogeneous substrates where own and foreign soils were mixed. We also included sterilized soil to study the effect of excluding soil biota, such as pathogens, symbionts and decomposers. We supplied 15N as tracer to measure nutrient uptake.
    In nonsterile conditions, most plant species produced more biomass in heterogeneous than in homogeneous soil. Root biomass and 15N uptake rates were higher in foreign than own soil patches. These differences between heterogeneous and homogeneous soil disappeared when soil was sterilized, suggesting that the effects in nonsterilized soils were due to species-specific soil biota that had responded to soil conditioning.
    We conclude that plants produce more biomass when own and foreign soils are patchily distributed than when mixed. We show that this enhanced productivity is due to nutrient uptake being overall most efficient when own and foreign soils are spatially separated. We propose that spatial heterogeneity of negative plant–soil feedback in species diverse plant communities may provide a better explanation of overyielding than assuming that plant–soil feedback effects are diluted.
  • New Phytologist

    Spatial heterogeneity of plant-soil feedback affects root interactions and interspecific competition

    Marloes Hendriks, Janneke M. Ravenek, Annemiek E. Smit-Tiekstra, Jan Willem van der Paauw, Hannie de Caluwe, Wim H. van der Putten, Hans de Kroon, Liesje Mommer
    Plant-soil feedback is receiving increasing interest as a factor influencing plant competition and species coexistence in grasslands. However, we do not know how spatial distribution of plant-soil feedback affects plant below-ground interactions. We investigated the way in which spatial heterogeneity of soil biota affects competitive interactions in grassland plant species. We performed a pairwise competition experiment combined with heterogeneous distribution of soil biota using four grassland plant species and their soil biota. Patches were applied as quadrants of own' and foreign' soils from all plant species in all pairwise combinations. To evaluate interspecific root responses, species-specific root biomass was quantified using real-time PCR. All plant species suffered negative soil feedback, but strength was species-specific, reflected by a decrease in root growth in own compared with foreign soil. Reduction in root growth in own patches by the superior plant competitor provided opportunities for inferior competitors to increase root biomass in these patches. These patterns did not cascade into above-ground effects during our experiment. We show that root distributions can be determined by spatial heterogeneity of soil biota, affecting plant below-ground competitive interactions. Thus, spatial heterogeneity of soil biota may contribute to plant species coexistence in species-rich grasslands.
  • Journal of Ecology

    Complementarity and selection effects in early and mid-successional plant communities are differentially affected by plant-soil feedback

    Jingying Jing, T. Martijn Bezemer, Wim H. van der Putten

    1.Many studies that provided evidence for a positive relationship between plant diversity and productivity have proposed that this effect may be explained by complementarity among species in resources utilization, or selection of particularly productive species in high-diversity plant communities. Recent studies have related the higher productivity in diverse plant communities to suppression of pathogenic soil biota. If soil biota play a role in diversity-productivity relationships, the question remains about how they may influence complementarity and selection effects.

    2.Here we examine how complementarity and selection effects may depend on soil biota using a plant-soil feedback approach. We used monocultures and mixtures of early successional plant species, which are known to have mostly negative plant-soil feedback effects, and mid-successional plant species, which generally have neutral plant-soil feedback.

    3.We found that plant-soil feedback effects differed between monocultures and mixed plant communities, as well as between early and mid-succession plants. This resulted in a significant interaction effect between diversity and successional stage. In monocultures, plant-soil feedback tended to be negative for early- and positive for mid-succession plant species. Interestingly, the community feedback responses of the mixed communities were opposite, being positive for early- and negative for mid-succession community.

    4.Plant-soil feedback differentially affected complementarity and selection effects of early and mid-succession plant communities: it enhanced complementarity effects of early- and decreased selection effects of mid-succession species.

    5.Synthesis. Soil biota that drive plant-soil feedback effects can influence the diversity-productivity relationship not only through decreased biomass production in monocultures compared to mixtures, but also through influencing complementarity and selection effects among species in mixed plant communities. Our results reveal that biodiversity-productivity relationships depend on plant-soil feedback interactions, which depend on the successional position of the plant. We propose that including successional position and trait-based analyses of plant-soil feedback in diversity-functioning studies will enhance understanding consequences of biodiversity loss for productivity and other ecosystem processes.
  • Frontiers in Ecology and Evolution

    Towards a global platform for linking soil biodiversity data

    Kelly Ramirez, Markus Döring, Nico Eisenhauer, Ciro Gardi, Josh Ladau, Jonathan W Leff, Guillaume Lentendu, Zoë Lindo, Matthias C Rillig, David Russell, Stefan Scheu, Mark G St. John, Franciska T. De Vries, Tesfaye Wubet, Wim H. van der Putten, Diana H. Wall
    BACKGROUND: Soil biodiversity is immense, with an estimated 10-100 million organisms belonging to over 5000 taxa in a handful of soil. In spite of the importance of soil biodiversity for ecosystem functions and services, information on soil species, from taxonomy to biogeographical patterns, is incomplete and there is no infrastructure to connect pre-existing or future data. Here, we propose a global platform to allow for greater access to soil biodiversity information by linking databases and repositories through a single open portal. The proposed platform would for the first time, link data on soil organisms from different global sites and biomes, and will be inclusive of all data types, from molecular sequences to morphology measurements and other supporting information. Access to soil biodiversity species records and information will be instrumental to progressing scientific research and education. Further, as demonstrated by previous biodiversity synthesis efforts, data availability is key for adapting to, and creating mitigation plans in response to global changes. With the rapid influx of soil biodiversity data, now is the time to take the first steps forward in establishing a global soil biodiversity information platform.
  • Ecology

    Separating the role of biotic interactions and climate in determining adaptive response of plants to climate change

    S. Tomiolo, Wim H. van der Putten, K. Tielborger

    Altered rainfall regimes will greatly affect the response of plant species to climate change. However, little is known about how direct effects of changing precipitation on plant performance may depend on other abiotic factors and biotic interactions. We used reciprocal transplants between climatically very different sites with simultaneous manipulation of soil, plant population origin, and neighbor conditions to evaluate local adaptation and possible adaptive response of four Eastern Mediterranean annual plant species to climate change. The effect of site on plant performance was negligible, but soil origin had a strong effect on fecundity, most likely due to differential water retaining ability. Competition by neighbors strongly reduced fitness.

    We separated the effects of the abiotic and biotic soil properties on plant performance by repeating the field experiment in a greenhouse under homogenous environmental conditions and including a soil biota manipulation treatment. As in the field, plant performance differed among soil origins and neighbor treatments. Moreover, we found plant species-specific responses to soil biota that may be best explained by the differential sensitivity to negative and positive soil biota effects. Overall, under the conditions of our experiment with two contrasting sites, biotic interactions had a strong effect on plant fitness that interacted with and eventually overrode climate. Because climate and biotic interactions covary, reciprocal transplants and climate gradient studies should consider soil biotic interactions and abiotic conditions when evaluating climate change effects on plant performance.

    Read More: http://www.esajournals.org/doi/10.1890/14-1445.1
  • Plant and Soil

    Plant-feeding nematodes in coastal sand dunes: occurrence, host specificity and effects on plant growth

    Pella Brinkman, Henk Duyts, G. Karssen, C.D. Van der Stoel, Wim H. van der Putten
    Coastal sand dunes have a well-established abiotic gradient from beach to land and a corresponding spatial gradient of plant species representing succession in time. Here, we relate the distribution of plant-feeding nematodes with dominant plant species in the field to host specialization and impacts on plant species under controlled greenhouse conditions.
    We assessed plant-feeding nematodes in soil and roots of six plant species that dominate the vegetation at successional positions along the gradient. In controlled conditions, we determined performance of all plant-feeding nematodes on each plant species and their effects on plant biomass.
    Specialist feeding type nematodes were confined to plant species in either foredunes or landward dunes. Generalist feeding type nematodes were found in highest numbers in the landward dunes. Most tested nematode species decreased root, but not shoot or rhizome biomass.
    Host plant suitability determined occurrence of some plant-feeding nematodes in dunes, but abiotic and biotic soil conditions may play a role as well. Generalist feeding type nematodes were able to reproduce on all plant species. Feeding specialists, which are more protected by plant roots, might prefer host plants in the foredunes for the same reason as their host plants: to escape from natural enemies.
  • Nature

    Biodiversity increases the resistance of ecosystem productivity to climate extremes

    F. Isbell, D. Craven, J. Connolly, M. Loreau, B. Schmid, C. Beierkuhnlein, T. Martijn Bezemer, C. Bonin, H. Bruelheide, E. De Luca, A. Ebeling, J.N. Griffin, Q. Guo, Y. Hautier, A. Hector, A. Jentsch, J. Kreyling, V. Lanta, P. Manning, S.T. Meyer, A.S. Mori, S. Naeem, P.A. Niklaus, H.W. Polley, P.B. Reich, C. Roscher, Eric W. Seabloom, M.D. Smith, M.P. Thakur, D. Tilman, B.F. Tracy, Wim H. van der Putten, Jasper van Ruijven, A. Weigelt, W.W. Weisser, B. Wilsey, Nico Eisenhauer
    It remains unclear whether biodiversity buffers ecosystems against climate extremes, which are becoming increasingly frequent worldwide1. Early results suggested that the ecosystem productivity of diverse grassland plant communities was more resistant, changing less during drought, and more resilient, recovering more quickly after drought, than that of depauperate communities2. However, subsequent experimental tests produced mixed results3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13. Here we use data from 46 experiments that manipulated grassland plant diversity to test whether biodiversity provides resistance during and resilience after climate events. We show that biodiversity increased ecosystem resistance for a broad range of climate events, including wet or dry, moderate or extreme, and brief or prolonged events. Across all studies and climate events, the productivity of low-diversity communities with one or two species changed by approximately 50% during climate events, whereas that of high-diversity communities with 16–32 species was more resistant, changing by only approximately 25%. By a year after each climate event, ecosystem productivity had often fully recovered, or overshot, normal levels of productivity in both high- and low-diversity communities, leading to no detectable dependence of ecosystem resilience on biodiversity. Our results suggest that biodiversity mainly stabilizes ecosystem productivity, and productivity-dependent ecosystem services, by increasing resistance to climate events. Anthropogenic environmental changes that drive biodiversity loss thus seem likely to decrease ecosystem stability14, and restoration of biodiversity to increase it, mainly by changing the resistance of ecosystem productivity to climate events.

    Local dominance of exotic plants declines with residence time: a role for plant–soil feedback?

    Tanja Speek, Joop H.J. Schaminée, Jeltje M. Stam, L.A.P. Lotz, Wim A. Ozinga, Wim H. van der Putten
    Recent studies have shown that introduced exotic plant species may be released from their native soil-borne pathogens, but that they become exposed to increased soil pathogen activity in the new range when time since introduction increases. Other studies have shown that introduced exotic plant species become less dominant when time since introduction increases, and that plant abundance may be controlled by soil-borne pathogens; however, no study yet has tested whether these soil effects might explain the decline in dominance of exotic plant species following their initial invasiveness. Here we determine plant–soil feedback of 20 plant species that have been introduced into The Netherlands. We tested the hypotheses that (i) exotic plant species with a longer residence time have a more negative soil feedback and (ii) greater local dominance of the introduced exotic plant species correlates with less negative, or more positive, plant–soil feedback. Although the local dominance of exotic plant species decreased with time since introduction, there was no relationship of local dominance with plant–soil feedback. Plant–soil feedback also did not become more negative with increasing time since introduction. We discuss why our results may deviate from some earlier published studies and why plant–soil feedback may not in all cases, or not in all comparisons, explain patterns of local dominance of introduced exotic plant species.
  • Basic and Applied Ecology

    Top-down control of root-feeding nematodes in range-expanding and congeneric native plant species

    Maria Viketoft, Wim H. van der Putten
    Abstract Climate warming may result in range expansion of species towards previously colder environments, and it has been demonstrated that in the new range successfully range-expanding plant species can be less attacked by aboveground and belowground enemies than congeneric natives. Plant enemies may be controlled naturally by complex bottom-up and top-down interactions with their hosts, however, little is known about how these interactions may operate in the new range. Here, we examine how root-feeding nematodes are controlled in the root zone of successfully range-expanding plant species in comparison with congeneric plant species native to the new range. As range-expanding plant species can have less negative soil feedback than congeneric natives, we tested the hypothesis that top-down control of root-feeding nematodes may be strongest on range-expanding plant species. To test this, we grew 4 pairs of range-expanding plant species and their native congeners in field soil, to which we added soil microbes, nematodes, or microarthropods from the new habitat. Addition of soil microorganisms and microarthropods reduced the numbers of root-feeding nematodes, being strongest when microorganisms were added. Opposite to our expectation, nematode control was not more effective in the root zone of range-expanding than native plant species. We conclude that top-down control of root-feeding nematodes is highly plant species-specific and that top-down control of these nematodes in the root zone of range-expanding plant species can be as effective as in the root zone of congeneric natives.
  • Soil Biology & Biochemistry

    Shifts in microbial diversity through land use intensity as drivers of carbon mineralization in soil

    Vincent Tardy, Aymé Spor, Olivier Mathieu, Jean Lévèque, Sébastien Terrat, Pierre Plassart, Tiffanie Regnier, Richard D. Bardgett, Wim H. van der Putten, Pier Paolo Roggero, Giovanna Seddaiu, Simonetta Bagella, Philippe Lemanceau, Lionel Ranjard, Pierre-Alain Maron
    Abstract Land use practices alter the biomass and structure of soil microbial communities. However, the impact of land management intensity on soil microbial diversity (i.e. richness and evenness) and consequences for functioning is still poorly understood. Here, we addressed this question by coupling molecular characterization of microbial diversity with measurements of carbon (C) mineralization in soils obtained from three locations across Europe, each representing a gradient of land management intensity under different soil and environmental conditions. Bacterial and fungal diversity were characterized by high throughput sequencing of ribosomal genes. Carbon cycling activities (i.e., mineralization of autochthonous soil organic matter, mineralization of allochthonous plant residues) were measured by quantifying 12C- and 13C-CO2 release after soils had been amended, or not, with 13C-labelled wheat residues. Variation partitioning analysis was used to rank biological and physicochemical soil parameters according to their relative contribution to these activities. Across all three locations, microbial diversity was greatest at intermediate levels of land use intensity, indicating that optimal management of soil microbial diversity might not be achieved under the least intensive agriculture. Microbial richness was the best predictor of the C-cycling activities, with bacterial and fungal richness explaining 32.2 and 17% of the intensity of autochthonous soil organic matter mineralization; and fungal richness explaining 77% of the intensity of wheat residues mineralization. Altogether, our results provide evidence that there is scope for improvement in soil management to enhance microbial biodiversity and optimize C transformations mediated by microbial communities in soil.
  • Molecular Ecology

    The epigenetic footprint of poleward range-expanding plants in apomictic dandelions

    Veronica Preite, Basten Snoek, Carla Oplaat, Arjen Biere, Wim H. van der Putten, Koen Verhoeven
    Epigenetic modifications, such as DNA methylation variation, can generate heritable phenotypic variation independent of the underlying genetic code. However, epigenetic variation in natural plant populations is poorly documented and little understood. Here, we test if northward range expansion of obligate apomicts of the common dandelion (Taraxacum officinale) is associated with DNA methylation variation. We characterized and compared patterns of genetic and DNA-methylation variation in greenhouse-reared offspring of T. officinale that were collected along a latitudinal transect of northward range expansion in Europe. Genetic AFLP and epigenetic MS-AFLP markers revealed high levels of local diversity and modest but significant heritable differentiation between sampling locations and between the Southern, Central and Northern regions of the transect. Patterns of genetic and epigenetic variation were significantly correlated, reflecting the genetic control over epigenetic variation and/or the accumulation of lineage-specific spontaneous epimutations, which may be selectively neutral. In addition, we identified a small component of DNA methylation differentiation along the transect that is independent of genetic variation. This epigenetic differentiation might reflect environment-specific induction or, in case the DNA methylation variation affects relevant traits and fitness, selection of heritable DNA methylation variants. Such generated epigenetic variants might contribute to the adaptive capacity of individual asexual lineages under changing environments. Our results highlight the potential of heritable DNA methylation variation to contribute to population differentiation along ecological gradients. Further studies are needed using higher-resolution methods to understand the functional significance of such natural occurring epigenetic differentiation.
  • Functional Ecology

    Are there evolutionary consequences of plant-soil feedbacks along soil gradients?

    J.A. Schweitzer, I. Juric, Tess Van de Voorde, K. Clay, Wim H. van der Putten, J.K. Bailey
    Both abiotic and biotic gradients exist in soils, and several of these gradients have been shown to select for plant traits. Moreover, plants possess a multitude of traits that can lead to strong niche construction (i.e. plant-induced changes to soils). Our objectives in this paper are to outline both empirical and theoretical evidence for the evolutionary consequences of plant-soil linkages and feedbacks on plants along soil heterogeneity gradients. We describe a simple mathematical model of plant evolution to explore the relationship between the sign and magnitude of feedback and the divergence of plant traits. We also constructed an individual-based simulation model to study the conditions under which plant-soil feedbacks occur, niche construction evolves, and plant traits diverge. This approach allows us to address specific hypotheses regarding relationships between positive and negative plant-soil feedback with variation in niche construction, the strength of selective gradients and the relative importance of local adaptation vs. feedbacks. The models suggest that feedbacks between soils and plants may commonly result in evolutionary interactions. The simulation model indicates that plant traits can diverge with niche construction and traits can be selected for in response to niche construction. However, the magnitude of feedbacks and how strongly they evolve depends on the amount of gene flow and the strength of selective gradients over time. These results suggest that plant-soil feedback can lead to evolution in plants and reveals new research directions for further inquiry. Questions addressing trade-offs and relationships between positive and negative feedbacks as well as adaptation and maladaptation of plant traits represent important frontiers in plant-soil feedback studies.
  • Urban Ecosystems

    Urban and agricultural soils: conflicts and trade-offs in the optimization of ecosystem services

    H. Setälä, Richard D. Bardgett, K. Birkhofer, M. Brady, L. Byrne, P.C. de Ruiter, F.T. De Vries, C. Gardi, K. Hedlund, L. Hemerik, S. Hotes, M. Liiri, S.R. Mortimer, M. Pavao-Zuckerman, R. Pouyat, M. Tsiafouli, Wim H. van der Putten
    [KEYWORDS: Agriculture Ecosystem services Land use Management optimization Soil Urban Trade-off] On-going human population growth and changing patterns of resource consumption are increasing global demand for ecosystem services, many of which are provided by soils. Some of these ecosystem services are linearly related to the surface area of pervious soil, whereas others show non-linear relationships, making ecosystem service optimization a complex task. As limited land availability creates conflicting demands among various types of land use, a central challenge is how to weigh these conflicting interests and how to achieve the best solutions possible from a perspective of sustainable societal development. These conflicting interests become most apparent in soils that are the most heavily used by humans for specific purposes: urban soils used for green spaces, housing, and other infrastructure and agricultural soils for producing food, fibres and biofuels. We argue that, despite their seemingly divergent uses of land, agricultural and urban soils share common features with regards to interactions between ecosystem services, and that the trade-offs associated with decision-making, while scale- and context-dependent, can be surprisingly similar between the two systems. We propose that the trade-offs within land use types and their soil-related ecosystems services are often disproportional, and quantifying these will enable ecologists and soil scientists to help policy makers optimizing management decisions when confronted with demands for multiple services under limited land availability.
  • Nature

    Belowground biodiversity and ecosystem functioning

    Richard D. Bardgett, Wim H. van der Putten
    Belowground biodiversity is largely out of sight and mind, but there is mounting evidence to show that the vast diversity of subterranean microorganisms and animals that live belowground contribute significantly to shaping the overall biodiversity and and terrestrial ecosystem function. In this review, Richard Bardgett and Wim van der Putten consider recent work on the ecological and evolutionary role of belowground biodiversity and outline areas or research that would improve our understanding of the influence of soil biodiversity on the ecological and evolutionary responses of terrestrial ecosystems to environmental change.
  • Phytochemistry

    Chemical variation in Jacobaea vulgaris is influenced by the interaction of season and vegetation successional stage

    Sabrina Almeida de Carvalho, Mirka Macel, P.P.J. Mulder, A. Skidmore, Wim H. van der Putten
    Knowledge on spatio-temporal dynamics of plant primary and secondary chemistry under natural conditions is important to assess how plarit defence varies in real field conditions. Plant primary and secondary chemistry is known to vary with both season and vegetation successional stage, however, in few studies these two sources of variation have been examined in combination. Here we examine variations in primary and secondary chemistry of Jacobaea vulgaris (Asteraceae) throughout the growing season in early, mid, and late stages of secondary succession following land abandonment using a well-established chronosequence in The Netherlands. We investigated primary and secondary chemistry of both leaves and flowers, in order to determine if patterns during seasonal (phenological) development may differ among successional stages. The chemical concentration of primary and secondary chemistry compounds in J. vulgaris varied throughout the season and was affected by vegetation succession stage. Concentrations of pyrrolizidine alkaloid (PA) tertiary-amines were highest in flowers during early Summer and in fields that had been abandoned ten to twenty years ago. PA N-oxide concentrations of both leaves and flowers, on the other hand increased with the progression of both season and succession. In Spring and early Summer chlorophyll concentrations were highest, especially in the oldest fields of the chronosequence. During phenological development, nitrogen concentration increased in flowers and decreased in leaves revealing allocation of nutrients from vegetative to reproductive plant parts throughout the growing season. The highest concentrations of N-oxides and chlorophylls were detected in older fields. Thus, our results suggest that variations in plant patterns of nutritional and defence compounds throughout the growing season are depending on successional context. (C) 2013 Elsevier Ltd. All rights reserved.
  • Ecology and Evolution

    Novel chemistry of invasive plants: exotic species have more unique metabolomic profiles than native congeners

    Mirka Macel, R.C.H. de Vos, Jeroen Jansen, Wim H. van der Putten, Nicole M. van Dam
    t is often assumed that exotic plants can become invasive when they possess novel secondary chemistry compared with native plants in the introduced range. Using untargeted metabolomic fingerprinting, we compared a broad range of metabolites of six successful exotic plant species and their native congeners of the family Asteraceae. Our results showed that plant chemistry is highly species-specific and diverse among both exotic and native species. Nonetheless, the exotic species had on average a higher total number of metabolites and more species-unique metabolites compared with their native congeners. Herbivory led to an overall increase in metabolites in all plant species. Generalist herbivore performance was lower on most of the exotic species compared with the native species. We conclude that high chemical diversity and large phytochemical uniqueness of the exotic species could be indicative of biological invasion potential.
  • Plant Ecology & Diversity

    The northward shifting neophyte Tragopogon dubius is just as effective in forming mycorrhizal associations as the native T. pratensis

    Roy H. A. van Grunsven, Tri-Wira Yuwati, George Kowalchuk, Wim H. van der Putten, Elmar M. Veenendaal
    Background: As a consequence of climate warming, many organisms are shifting their range towards higher latitudes and altitudes. As not all do so at the same speed, this may disrupt biotic interaction. Release from natural enemies through range expansion can result in invasiveness, whereas loss of mutualists can reduce plant vigour and fitness. One of the most important groups of plant symbiotic mutualists is the arbuscular mycorrhizal fungi (AMF).Aims: We used greenhouse experiments to test whether Tragopogon dubius, a species that has recently expanded its range northward and colonised the Netherlands, is able to associate with the same AMF as the native congener T. pratensis.Methods: In soils collected from four locations in the new range of T. dubius we compared the density of infective AMF propagules associating with both plant species, as well as AMF colonisation of the roots. The AMF community structure in the roots of these species was also analysed using polymerase chain reaction-denaturing gradient gel electrophoresis (PCR-DGGE).Results: Tragopogon dubius and T. pratensis did not differ in any of these characteristics.Conclusions: We therefore conclude that the range-shifting T. dubius is as effective in the formation of mycorrhiza as the native congener.
  • Oikos

    Selective alteration of soil food web components by invasive giant goldenrod Solidago gigantea in two distinct habitat types

    C.W. Quist, M.T.W. Vervoort, H. Van Megen, G. Gort, J. Bakker, Wim H. van der Putten, J. Helder
    Apart from relatively well-studied aboveground effects, invasive plant species will also impact the soil food web. So far, most research has been focusing on primary decomposers, while studies on effects at higher trophic levels are relatively scarce. Giant goldenrod Solidago gigantea, native to North America, is a widespread and common invasive species in most European countries. We investigated its impact on plant communities and on multiple trophic levels of the soil food web in two contrasting habitats: riparian zones and semi-natural grasslands. In 30 pairs of invaded and uninvaded plots, floristic composition, pH, fungal biomass and the densities of 11 nematode taxa were determined by using a quantitative PCR-based method. In the two habitats, the invader outcompeted both rare and dominant plant species. Belowground, S. gigantea invasion reduced pH, increased overall fungal biomass as well as the density of a single lineage of fungivorous nematodes, the family Aphelenchoididae. The densities of two other, phylogenetically distinct lineages of fungivorous nematodes, Aphelenchidae and Diphtherophoridae, were unaffected by the local increase in fungal biomass. Apparently this plant species induces a local asymmetric boost of the fungal community, and only Aphelenchoididae were able to benefit from this invader-induced change. The alternative explanation - the results are explained by a subtle, S. gigantea - induced 0.1-0.2 units decrease of pH - seems unlikely, as pH optima for nematode taxa are relatively broad. Thus, apart from readily observable aboveground effects, the invasive plant species S. gigantea affects fungal biomass as well as a specific part of the fungivorous nematode community in a soil type-independent manner. [KEYWORDS: EXOTIC PLANT INVASIONS NEMATODE COMMUNITIES ALIEN PLANTS ERGOSTEROL BIOTA DIVERSITY BIODIVERSITY EXTRACTION CANADENSIS FEEDBACKS]
  • Oikos

    Grazing-induced changes in plant–soil feedback alter plant biomass allocation

    Large vertebrate herbivores, as well as plant–soil feedback interactions are important drivers of plant performance, plant community composition and vegetation dynamics in terrestrial ecosystems. However, it is poorly understood whether and how large vertebrate herbivores and plant–soil feedback effects interact. Here, we study the response of grassland plant species to grazing-induced legacy effects in the soil and we explore whether these plant responses can help us to understand long-term vegetation dynamics in the field. In a greenhouse experiment we tested the response of four grassland plant species, Agrostis capillaris, Festuca rubra, Holcus lanatus and Rumex acetosa, to field-conditioned soils from grazed and ungrazed grassland. We relate these responses to long-term vegetation data from a grassland exclosure experiment in the field. In the greenhouse experiment, we found that total biomass production and biomass allocation to roots was higher in soils from grazed than from ungrazed plots. There were only few relationships between plant production in the greenhouse and the abundance of conspecifics in the field. Spatiotemporal patterns in plant community composition were more stable in grazed than ungrazed grassland plots, but were not related to plant–soil feedbacks effects and biomass allocation patterns. We conclude that grazing-induced soil legacy effects mainly influenced plant biomass allocation patterns, but could not explain altered vegetation dynamics in grazed grasslands. Consequently, the direct effects of grazing on plant community composition (e.g. through modifying light competition or differences in grazing tolerance) appear to overrule indirect effects through changes in plant–soil feedback
  • Biological Invasions

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

    Annelein Meisner, (Gera) W.H.G. Hol, Wietse de Boer, J.A. Krumins, David A. Wardle, Wim H. van der Putten
    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.
  • Oecologia

    Sequential effects of root and foliar herbivory on aboveground and belowground induced plant defense responses and insect performance

    Minggang Wang, Arjen Biere, Wim H. van der Putten, T. Martijn Bezemer
    Plants are often simultaneously or sequentially attacked by multiple herbivores and changes in host plants induced by one herbivore can influence the performance of other herbivores. We examined how sequential feeding on the plant Plantago lanceolata by the aboveground herbivore Spodoptera exigua and the belowground herbivore Agriotes lineatus influences plant defense and the performance of both insects. Belowground herbivory caused a reduction in the food consumption by the aboveground herbivore independent of whether it was initiated before, at the same time, or after that of the aboveground herbivore. By contrast, aboveground herbivory did not significantly affect belowground herbivore performance, but significantly reduced the performance of later arriving aboveground conspecifics. Interestingly, belowground herbivores negated negative effects of aboveground herbivores on consumption efficiency of their later arriving conspecifics, but only if the belowground herbivores were introduced simultaneously with the early arriving aboveground herbivores. Aboveground–belowground interactions could only partly be explained by induced changes in an important class of defense compounds, iridoid glycosides (IGs). Belowground herbivory caused a reduction in IGs in roots without affecting shoot levels, while aboveground herbivory increased IG levels in roots in the short term (4 days) but only in the shoots in the longer term (17 days). We conclude that the sequence of aboveground and belowground herbivory is important in interactions between aboveground and belowground herbivores and that knowledge on the timing of exposure is essential to predict outcomes of aboveground–belowground interactions
  • Journal of Chemical Ecology

    Heterodera schachtii nematodes interfere with aphid-plant relations on Brassica oleracea

    (Gera) W.H.G. Hol, Wietse de Boer, Aad J Termorshuizen, Katrin Meyer, J.H.M. Schneider, Wim H. van der Putten, Nicole M. van Dam
    Aboveground and belowground herbivore species modify plant defense responses differently. Simultaneous attack can lead to non-additive effects on primary and secondary metabolite composition in roots and shoots. We previously found that aphid (Brevicoryne brassicae) population growth on Brassica oleracea was reduced on plants that were infested with nematodes (Heterodera schachtii) prior (4 weeks) to aphid infestation. Here, we examined how infection with root-feeding nematodes affected primary and secondary metabolites in the host plant and whether this could explain the increase in aphid doubling time from 3.8 to 6.7 days. We hypothesized that the effects of herbivores on plant metabolites would depend on the presence of the other herbivore and that nematode-induced changes in primary metabolites would correlate with reduced aphid performance. Total glucosinolate concentration in the leaves was not affected by nematode presence, but the composition of glucosinolates shifted, as gluconapin concentrations were reduced, while gluconapoleiferin concentrations increased in plants exposed to nematodes. Aphid presence increased 4-methoxyglucobrassicin concentrations in leaves, which correlated positively with the number of aphids per plant. Nematodes decreased amino acid and sugar concentrations in the phloem. Aphid population doubling time correlated negatively with amino acids and glucosinolate levels in leaves, whereas these correlations were non-significant when nematodes were present. In conclusion, the effects of an herbivore on plant metabolites were independent of the presence of another herbivore. Nematode presence reduced aphid population growth and disturbed feeding relations between plants and aphids.
  • Journal of Ecology

    Consequences of plant–soil feedbacks in invasion

    K.N. Suding, W.S. Harpole, A. Kulmatiski, A.S. MacDougall, T. Fukami, Wim H. van der Putten
  • BioScience

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

    J.A. Krumins, D. Van Oevelen, T. Martijn Bezemer, Gerlinde De Deyn, (Gera) W.H.G. Hol, Ellen Van Donk, Wietse de Boer, P.C. de Ruiter, J.J. Middelburg, F. Monroy, K.E.R. Soetaert, E. Thebault, J. Van de Koppel, Hans van Veen, M. Viketoft, Wim H. van der Putten
    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.
  • Proceedings of the National Academy of Sciences of the United States of America

    Soil biotic legacy effects of extreme weather events influence plant invasiveness

    Annelein Meisner, Gerlinde De Deyn, Wietse de Boer, Wim H. van der Putten
    Climate change is expected to increase future abiotic stresses on ecosystems through extreme weather events leading to more extreme drought and rainfall incidences [Jentsch A, et al. (2007) Front Ecol Environ 5(7):365–374]. These fluctuations in precipitation may affect soil biota, soil processes [Evans ST, Wallenstein MD (2012) Biogeochemistry 109:101–116], and the proportion of exotics in invaded plant communities [Jiménez MA, et al. (2011) Ecol Lett 14:1277–1235]. However, little is known about legacy effects in soil on the performance of exotics and natives in invaded plant communities. Here we report that drought and rainfall effects on soil processes and biota affect the performance of exotics and natives in plant communities. We performed two mesocosm experiments. In the first experiment, soil without plants was exposed to drought and/or rainfall, which affected soil N availability. Then the initial soil moisture conditions were restored, and a mixed community of co-occurring natives and exotics was planted and exposed to drought during growth. A single stress before or during growth decreased the biomass of natives, but did not affect exotics. A second drought stress during plant growth resetted the exotic advantage, whereas native biomass was not further reduced. In the second experiment, soil inoculation revealed that drought and/or rainfall influenced soil biotic legacies, which promoted exotics but suppressed natives. Our results demonstrate that extreme weather events can cause legacy effects in soil biota, promoting exotics and suppressing natives in invaded plant communities, depending on the type, frequency, and timing of extreme events.
  • Journal of Ecology

    Soil microbial community structure of range-expanding plant species differs from co-occurring natives

    1. Due to global warming and other changes in the environment, many native and exotic plant species show range expansion from lower to higher latitudes. In the new range, the (in)ability of range-expanding plants to establish associations with local soil microbes can have important consequences for plant abundance; however, very little information exists on rhizosphere communities of range-expanding plant species. Here, we examine the rhizosphere microbial community composition of range-expanding plant species in comparison with phylogenetically related species that are native in the invaded range. 2. We tested the hypothesis that range-expanding plants species would promote fewer shifts in rhizosphere communities than congeneric natives would. In order to test this, soil was collected from the invaded habitat and six range-expanding and nine congeneric natives were planted individually in pots to condition soil microbial communities. 3. After harvesting, individuals of the same species were planted in conditioned own and control soils to test the legacy effects of soil conditioning on biomass production. The control soils were mixtures of soils conditioned by all other plant species, except congenerics. After 10 weeks of plant growth, we determined the rhizosphere community composition of bacteria, fungi, arbuscular mycorrhizal fungi (AMF) and Fusarium spp. 4. All groups of microbes were analysed qualitatively using denaturating gradient gel electrophoresis (DGGE). Ergosterol was determined as a quantitative measure of nonarbuscular mycorrhizal fungal biomass, and real-time PCR was applied to detect amounts of Fusarium spp. 5. Range-expanding plants had less fungal hyphal biomass and lower amounts of Fusarium spp. in the rhizosphere than congenerics. Bacterial community composition was influenced by a combination of soil conditioning and plant origin, whereas fungal communities, AMF and Fusarium spp. were less pronounced in their responses to the experimental treatments. 6. Synthesis. We conclude that the lack of legacy effects in range-expanding plant species compared with natives may be due to differences in bacterial rhizosphere community composition, or to different quantities of potential pathogenic fungi. If the range-expanding plant species were benefiting more from AMF, effects will not have been due to differences in community composition, but we cannot exclude other options, such as different effectiveness of AMF or other soil biota in the rhizosphere of range-expanding vs. native plant species. The greater accumulation of bacterial and fungal pathogens in the rhizosphere of natives in relation to range expanders might explain the successful establishment of range-expanding plants.
  • PLoS One

    Competition increases sensitivity of wheat (Triticum aestivum) to biotic plant-soil feedback

    (Gera) W.H.G. Hol, Wietse de Boer, Freddy ten Hooven, Wim H. van der Putten
    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.
  • Journal of Ecology

    Independent variations of plant and soil mixtures reveal soil feedback effects on plant community overyielding

    Marloes Hendriks, Liesje Mommer, H. De Caluwe, A.E. Smit-Tiekstra, Wim H. van der Putten, H. de Kroon
    * Recent studies have shown that the positive relationship between plant diversity and plant biomass (‘overyielding’) can be explained by soil pathogens depressing productivity more in low than in high diverse plant communities. However, tests of such soil effects in field studies were constrained by experimental limitations to manipulate soil community composition independent of plant community composition. Here, we report of an experiment where feedback effects to plants were tested for both plant and soil monocultures and mixtures. * Our results demonstrate that overyielding is the result of plant species in mixture being more growth-limited by ‘own’ soil biota than by soil biota of other plant species. This effect disappeared when the soils had been sterilized by gamma-irradiation. Mixing plants themselves did not result in overyielding except when grown in the soil of one of the species (Leucanthemum vulgare), where growth of one species disproportionally increased in mixture compared to monoculture. * Soil nutrient availability could not explain differences in growth between the non-sterilized soils. Therefore, our results suggest that plant species–specific soil biota rather than the plants have contributed to the plant community overyielding. * Species biomass ranking in mixtures highly differed between non-sterilized soils of different histories of soil conditioning, whilst the ranking was more consistent in sterilized soil. Sterilized soils of different origin differed significantly in nutrient availability. These results suggest that shifts in competitive hierarchies depend on plant species–specific interactions influenced by soil biota and cannot be induced by mineral nitrogen. * Synthesis. Our results show that overyielding in four plant species mixtures can be due to species-specific interactions between plants and their specific soil biota. Neither mixing the plant species alone nor the differential responses of species to mineral nitrogen influenced community productivity, but mixing soil biota did. [KEYWORDS: Anthoxanthum odoratum biodiversity experiment biodiversity–productivity relationship competitive hierarchy determinants of plant community diversity and structure grasslands Leucanthemum vulgare micro-organisms pathogens plant–soil feedback]
  • Frontiers in Plant Science

    The importance of aboveground-belowground interactions on the evolution and maintenance of variation in plant defence traits

    Moniek Van Geem, R. Gols, Nicole M. van Dam, Wim H. van der Putten, Taiadjana Fortuna, Jeff A. Harvey
    Over the past two decades a growing body of empirical research has shown that many ecological processes are mediated by a complex array of indirect interactions occurring between rhizosphere-inhabiting organisms and those found on aboveground plant parts. Aboveground - belowground studies have thus far focused on elucidating processes and underlying mechanisms that mediate the behavior and performance of invertebrates in opposite compartments. Less is known about genetic variation in plant traits as this applies to an above- belowground framework. For instance, although the field of genetic variation in aboveground plant traits on community-level interactions is well developed, most studies have ignored genetic variation in plant traits – such as defence - that may have evolved in response to pressures from the combined effects of above- and below ground interactions from antagonists and mutualists. Here, we discuss gaps in our understanding of genetic variation in plant- and consumer-related traits as they relate to aboveground and belowground multitrophic interactions. When metabolic resources are limiting, then multiple attack by antagonists in both domains may lead to trade-offs in where these resources are optimally invested. In nature, these trade-offs may critically depend upon their effects on plant fitness. Natural enemies of herbivores may also influence selection for different traits via top-down control. At larger scales these interactions may generate evolutionary ‘hotspots’ where the expression of various plant traits is the result of strong reciprocal selection via direct and indirect interactions. The role of abiotic factors in driving genetic variation in plant traits is also discussed.
  • Biological Invasions

    Testing the Australian Weed Risk Assessment with different proxies for invasiveness

    Tanja Speek, J.A.R. Davies, L.A.P. Lotz, Wim H. van der Putten
    The Weed Risk Assessment (WRA) has become an effective tool in predicting invasiveness of exotic plant species. In studies testing the WRA, exotic plant species are usually divided into major weeds, minor weeds and non-weeds. However, these divisions are qualitative, as the categories are assigned by experts. Many studies searching for plant traits that are indicative of plant invasiveness use quantitative estimates to measure invasiveness. We compared how quantitative and qualitative estimates of invasiveness may relate to WRA scores. As quantitative estimates we used regional frequency (spread), change in regional frequency and local dominance of naturalized exotic plant species in The Netherlands. To obtain a qualitative estimate we determined if the exotic plant species occurred on a black list in neighbouring regions. We related WRA scores of the exotic plant species to these qualitative and quantitative estimates of invasiveness. Our results reveal that the WRA predicted the qualitative (black list) estimate more accurately than the quantitative (dominance and spread) ones. The black list estimate matches with the overall impact of exotic species, which is assumed to incorporate regional spread, local dominance and noxiousness. Therefore, the WRA predicts the noxiousness component, but to a lesser extent the spatial components of impact of exotic species. On the other hand, studies that use regional spread and other quantitative estimates of invasiveness tend not to include the noxiousness component of impact. We propose that our analyses may also help to further solve the recent debate on whether or not performing research on exotic species.
  • Proceedings of the National Academy of Sciences of the United States of America

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

    F.T. De Vries, E. Thébault, M. Liiri, K. Birkhofer, M.A. Tsiafouli, L. Bjørnlund, H.B. Jørgensen, M.V. Brady, S. Christensen, P.C. de Ruiter, T. D'Hertefeldt, J. Frouz, K. Hedlund, L. Hemerik, (Gera) W.H.G. Hol, S. Hotes, S.R. Mortimer, H. Setälä, S.P. Sgardelis, K. Uteseny, Wim H. van der Putten, V. Wolters, R.D. Bardget
    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.
  • Nature Reviews Microbiology

    Going back to the roots: the microbial ecology of the rhizosphere

    L. Philippot, Jos M. Raaijmakers, P. Lemanceau, Wim H. van der Putten
    The rhizosphere is the interface between plant roots and soil where interactions among a myriad of microorganisms and invertebrates affect biogeochemical cycling, plant growth and tolerance to biotic and abiotic stress. The rhizosphere is intriguingly complex and dynamic, and understanding its ecology and evolution is key to enhancing plant productivity and ecosystem functioning. Novel insights into key factors and evolutionary processes shaping the rhizosphere microbiome will greatly benefit from integrating reductionist and systems-based approaches in both agricultural and natural ecosystems. Here, we discuss recent developments in rhizosphere research in relation to assessing the contribution of the micro- and macroflora to sustainable agriculture, nature conservation, the development of bio-energy crops and the mitigation of climate change.
  • Journal of Ecology

    Above- and below-ground herbivory effects on below-ground plant–fungus interactions and plant–soil feedback responses

    T. Martijn Bezemer, Wim H. van der Putten, Henk Martens, Tess Van de Voorde, P.P.J. Mulder, Olga Kostenko
    Summary Feeding by insect herbivores can affect plant growth and the concentration of defense compounds in plant tissues. Since plants provide resources for soil organisms, herbivory can also influence the composition of the soil community via its effects on the plant. Soil organisms, in turn, are important for plant growth. We tested whether insect herbivores, via their effects on the soil microbial community, can influence plant-soil feedbacks. We first examined the effects of above-ground (AG) and below-ground (B) insect herbivory on the composition of pyrrolizidine alkaloids (PAs) in roots and on soil fungi in roots and rhizosphere soil of ragwort (Jacobaea vulgaris). The composition of fungal communities in roots and rhizosphere soil was affected by both AG and BG herbivory, but fungal composition also differed considerably between roots and rhizosphere soil. The composition of PAs in roots was affected only by BG herbivory. Thirteen different fungal species were detected in roots and rhizosphere soil. The presence of the potentially pathogenic fungus Fusarium oxysporum decreased and that of Phoma exigua increased in presence of BG herbivory, but only in soil samples. We then grew new plants in the soils conditioned by plants exposed to the herbivore treatments and in unconditioned soil. A subset of the new plants was exposed to foliar insect herbivory. Plant-soil feedback was strongly negative, but the feedback effect was least negative in soil conditioned by plants that had been exposed to BG herbivory. There was a negative direct effect of foliar herbivory on plant biomass during the feedback phase, but this effect was far less strong when the soil was conditioned by plants exposed to AG herbivory. AG herbivory during the conditioning phase also caused a soil feedback effect on the PA concentration in the foliage of ragwort. Synthesis. Our results illustrate how insect herbivory can affect interactions between plants and soil organisms, and via these effects how herbivory can alter the performance of late-growing plants. Plant-soil feedback is emerging as an important theme in ecology and these results highlight that plant-soil feedback should be considered from a multitrophic AG and BG perspective.
  • Journal of Ecology

    Plant-soil feedback: the past, the present and future challenges

    Wim H. van der Putten, Richard D. Bardgett, J.D. Bever, T. Martijn Bezemer, B.B. Casper, T. Fukami, Paul Kardol, J.N. Klironomos, A. Kulmatiski, J.A. Schweitzer, K.N. Suding, Tess Van de Voorde, David A. Wardle
    Summary Plant–soil feedbacks is becoming an important concept for explaining vegetation dynamics, the invasiveness of introduced exotic species in new habitats and how terrestrial ecosystems respond to global land use and climate change. Using a new conceptual model, we show how critical alterations in plant–soil feedback interactions can change the assemblage of plant communities. We highlight recent advances, define terms and identify future challenges in this area of research and discuss how variations in strengths and directions of plant–soil feedbacks can explain succession, invasion, response to climate warming and diversity-productivity relationships. While there has been a rapid increase in understanding the biological, chemical and physical mechanisms and their interdependencies underlying plant–soil feedback interactions, further progress is to be expected from applying new experimental techniques and technologies, linking empirical studies to modelling and field-based studies that can include plant–soil feedback interactions on longer time scales that also include long-term processes such as litter decomposition and mineralization. Significant progress has also been made in analysing consequences of plant–soil feedbacks for biodiversity-functioning relationships, plant fitness and selection. To further integrate plant–soil feedbacks into ecological theory, it will be important to determine where and how observed patterns may be generalized, and how they may influence evolution. Synthesis. Gaining a greater understanding of plant–soil feedbacks and underlying mechanisms is improving our ability to predict consequences of these interactions for plant community composition and productivity under a variety of conditions. Future research will enable better prediction and mitigation of the consequences of human-induced global changes, improve efforts of restoration and conservation and promote sustainable provision of ecosystem services in a rapidly changing world.
  • PLoS One

    Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea

    T. Tytgat, Koen Verhoeven, Jeroen Jansen, Ciska Raaijmakers, Tanja Bakx-Schotman, L.M. McIntyre, Wim H. van der Putten, Arjen Biere, Nicole M. van Dam
    Plants respond to herbivore attack by rapidly inducing defenses that are mainly regulated by jasmonic acid (JA). Due to the systemic nature of induced defenses, attack by root herbivores can also result in a shoot response and vice versa, causing interactions between above- and belowground herbivores. However, little is known about the molecular mechanisms underlying these interactions. We investigated whether plants respond differently when roots or shoots are induced. We mimicked herbivore attack by applying JA to the roots or shoots of Brassica oleracea and analyzed molecular and chemical responses in both organs. In shoots, an immediate and massive change in primary and secondary metabolism was observed. In roots, the JA-induced response was less extensive and qualitatively different from that in the shoots. Strikingly, in both roots and shoots we also observed differential responses in primary metabolism, development as well as defense specific traits depending on whether the JA induction had been below- or aboveground. We conclude that the JA response is not only tissue-specific but also dependent on the organ that was induced. Already very early in the JA signaling pathway the differential response was observed. This indicates that both organs have a different JA signaling cascade, and that the signal eliciting systemic responses contains information about the site of induction, thus providing plants with a mechanism to tailor their responses specifically to the organ that is damaged.
  • ISPRS Journal of Photogrammetry and Remote Sensing

    Changes in plant defense chemistry (pyrrolizidine alkaloids) revealed through high-resolution spectroscopy

    Sabrina Almeida de Carvalho, Mirka Macel, M. Schlerf, F. Eghbali Moghaddam, P.P.J. Mulder, A.K. Skidmore, Wim H. van der Putten
    Plant toxic biochemicals play an important role in defense against natural enemies and often are toxic to humans and livestock. Hyperspectral reflectance is an established method for primary chemical detection and could be further used to determine plant toxicity in the field. In order to make a first step for pyrrolizidine alkaloids detection (toxic defense compound against mammals and many insects) we studied how such spectral data can estimate plant defense chemistry under controlled conditions. In a greenhouse, we grew three related plant species that defend against generalist herbivores through pyrrolizidine alkaloids: Jacobaea vulgaris, Jacobaea erucifolia and Senecio inaequidens, and analyzed the relation between spectral measurements and chemical concentrations using multivariate statistics. Nutrient addition enhanced tertiary-amine pyrrolizidine alkaloids contents of J. vulgaris and J. erucifolia and decreased N-oxide contents in S. inaequidens and J. vulgaris. Pyrrolizidine alkaloids could be predicted with a moderate accuracy. Pyrrolizidine alkaloid forms tertiary-amines and epoxides were predicted with 63% and 56% of the variation explained, respectively. The most relevant spectral regions selected for prediction were associated with electron transitions and CH, OH, and NH bonds in the 1530 and 2100 nm regions. Given the relatively low concentration in pyrrolizidine alkaloids concentration (in the order of mg g−1) and resultant predictions, it is promising that pyrrolizidine alkaloids interact with incident light. Further studies should be considered to determine if such a non-destructive method may predict changes in PA concentration in relation to plant natural enemies. Spectroscopy may be used to study plant defenses in intact plant tissues, and may provide managers of toxic plants, food industry and multitrophic-interaction researchers with faster and larger monitoring possibilities
  • Soil Biology & Biochemistry

    Community patterns of soil bacteria and nematodes in relation to geographic distance

    F. Monroy, Wim H. van der Putten, E. Yergeau, S.R. Mortimer, Henk Duyts, T. Martijn Bezemer
    Ecosystems consist of aboveground and belowground subsystems and the structure of their communities is known to change with distance. However, most of this knowledge originates from visible, aboveground components, whereas relatively little is known about how soil community structure varies with distance and if this variability depends on the group of organisms considered. In the present study, we analyzed 30 grasslands from three neighboring chalk hill ridges in southern UK to determine the effect of geographic distance (1–198 km) on the similarity of bacterial communities and of nematode communities in the soil. We found that for both groups, community similarity decayed with distance and that this spatial pattern was not related to changes either in plant community composition or soil chemistry. Site history may have contributed to the observed pattern in the case of nematodes, since the distance effect depended on the presence of different nematode taxa at one of the hill ridges. On the other hand, site-related differences in bacterial community composition alone could not explain the spatial turnover, suggesting that other factors, such as biotic gradients and local dispersal processes that we did not include in our analysis, may be involved in the observed pattern. We conclude that, independently of the variety of causal factors that may be involved, the decay in similarity with geographic distance is a characteristic feature of both communities of soil bacteria and nematodes.
  • Soil Biology & Biochemistry

    Soil inoculation method determines the strength of plant–soil interactions

    Tess Van de Voorde, Wim H. van der Putten, T. Martijn Bezemer
    There is increasing evidence that interactions between plants and biotic components of the soil influence plant productivity and plant community composition. Many plant–soil feedback experiments start from inoculating relatively small amounts of natural soil to sterilized bulk soil. These soil inocula may include a variety of size classes of soil biota, each having a different role in the observed soil feedback effects. In order to examine what may be the effect of various size classes of soil biota we compared inoculation with natural field soil sieved through a 1 mm mesh, a soil suspension also sieved through a 1 mm mesh, and a microbial suspension sieved through a 20 μm mesh. We tested these effects for different populations of the same plant species and for different soil origins. Plant biomass was greatest in pots inoculated with the microbial suspension and smallest in pots inoculated with sieved soil, both in the first and second growth phase, and there was no significant population or soil origin effect. Plant-feeding nematodes were almost exclusively found in the sieved soil treatment. We show that processing the soil to obtain a microbial suspension reduces the strength of the soil effect in both the first and second growth phase. We also show that the results obtained with inoculating sieved soil and with a soil suspension are not comparable. In conclusion, when designing plant–soil feedback experiments, it is crucial to consider that soil inoculum preparation can strongly influence the observed soil effect.
  • Journal of Chemical Ecology

    Root herbivore effects on aboveground multitrophic interactions: Patterns, processes and mechanisms

    Roxina Soler , Wim H. van der Putten, Jeff A. Harvey, Louise E.M. Vet, Marcel Dicke, T. Martijn Bezemer
    In terrestrial food webs, the study of multitrophic interactions traditionally has focused on organisms that share a common domain, mainly above ground. In the last two decades, it has become clear that to further understand multitrophic interactions, the barrier between the belowground and aboveground domains has to be crossed. Belowground organisms that are intimately associated with the roots of terrestrial plants can influence the levels of primary and secondary chemistry and biomass of aboveground plant parts. These changes, in turn, influence the growth, development, and survival of aboveground insect herbivores. The discovery that soil organisms, which are usually out of sight and out of mind, can affect plant-herbivore interactions aboveground raised the question if and how higher trophic level organisms, such as carnivores, could be influenced. At present, the study of above-belowground interactions is evolving from interactions between organisms directly associated with the plant roots and shoots (e.g., root feeders - plant - foliar herbivores) to interactions involving members of higher trophic levels (e.g., parasitoids), as well as non-herbivorous organisms (e.g., decomposers, symbiotic plant mutualists, and pollinators). This multitrophic approach linking above- and belowground food webs aims at addressing interactions between plants, herbivores, and carnivores in a more realistic community setting. The ultimate goal is to understand the ecology and evolution of species in communities and, ultimately how community interactions contribute to the functioning of terrestrial ecosystems. Here, we summarize studies on the effects of root feeders on aboveground insect herbivores and parasitoids and discuss if there are common trends.We discuss the mechanisms that have been reported to mediate these effects, from changes in concentrations of plant nutritional quality and secondary chemistry to defense signaling. Finally, we discuss how the traditional framework of fixed paired combinations of root- and shoot-related organisms feeding on a common plant can be transformed into a more dynamic and realistic framework that incorporates community variation in species, densities, space and time, in order to gain further insight in this exciting and rapidly developing field.
  • Journal of Experimental Botany

    How genetic modification of roots affects rhizosphere processes and plant performance

    Patrick Kabouw, Nicole M. van Dam, Wim H. van der Putten, Arjen Biere
    Genetic modification of plants has become common practice. However, root-specific genetic modifications have only recently been advocated. Here, a review is presented regarding how root-specific modifications can have both plant internal and rhizosphere-mediated effects on aboveground plant properties and plant performance. Plant internal effects refer to pleiotropic processes such as transportation of the modified gene product. Rhizosphere-mediated effects refer to altered plant–rhizosphere interactions, which subsequently feed back to the plant. Such plant–soil feedback mechanisms have been demonstrated both in natural systems and in crops. Here how plant internal and rhizosphere-mediated effects could enhance or counteract improvements in plant properties for which the genetic modification was intended is discussed. A literature survey revealed that rice is the most commonly studied crop species in the context of root-specific transgenesis, predominantly in relation to stress tolerance. Phytoremediation, a process in which plants are used to clean up pollutants, is also often an objective when transforming roots. These two examples are used to review potential effects of root genetic modifications on shoots. There are several examples in which root-specific genetic modifications only lead to better plant performance if the genes are specifically expressed in roots. Constitutive expression can even result in modified plants that perform worse than non-modified plants. Rhizosphere effects have rarely been examined, but clearly genetic modification of roots can influence rhizosphere interactions, which in turn can affect shoot properties. Indeed, field studies with root-transformed plants frequently show negative effects on shoots that are not seen in laboratory studies. This might be due to the simplified environments that are used in laboratories which lack the full range of plant–rhizosphere interactions that are present in the field.
  • Journal of Chemical Ecology

    Ecology and evolution of soil nematode chemotaxis

    S. Rasmann, J.G. Ali, J. Helder, Wim H. van der Putten
    Plants influence the behavior of and modify community composition of soil-dwelling organisms through the exudation of organic molecules. Given the chemical complexity of the soil matrix, soil-dwelling organisms have evolved the ability to detect and respond to these cues for successful foraging. A key question is how specific these responses are and how they may evolve. Here, we review and discuss the ecology and evolution of chemotaxis of soil nematodes. Soil nematodes are a group of diverse functional and taxonomic types, which may reveal a variety of responses. We predicted that nematodes of different feeding guilds use host-specific cues for chemotaxis. However, the examination of a comprehensive nematode phylogeny revealed that distantly related nematodes, and nematodes from different feeding guilds, can exploit the same signals for positive orientation. Carbon dioxide (CO2), which is ubiquitous in soil and indicates biological activity, is widely used as such a cue. The use of the same signals by a variety of species and species groups suggests that parts of the chemo-sensory machinery have remained highly conserved during the radiation of nematodes. However, besides CO2, many other chemical compounds, belonging to different chemical classes, have been shown to induce chemotaxis in nematodes. Plants surrounded by a complex nematode community, including beneficial entomopathogenic nematodes, plant-parasitic nematodes, as well as microbial feeders, are thus under diffuse selection for producing specific molecules in the rhizosphere that maximize their fitness. However, it is largely unknown how selection may operate and how belowground signaling may evolve. Given the paucity of data for certain groups of nematodes, future work is needed to better understand the evolutionary mechanisms of communication between plant roots and soil biota.
  • Annual Review of Ecology Evolution and Systematics

    Climate change, aboveground-belowground interactions, and species range shifts

    Changes in climate, land use, fire incidence, and ecological connections all may contribute to current species' range shifts. Species shift range individually, and not all species shift range at the same time and rate. This variation causes community reorganization in both the old and new ranges. In terrestrial ecosystems, range shifts alter aboveground-belowground interactions, influencing species abundance, community composition, ecosystem processes and services, and feedbacks within communities and ecosystems. Thus, range shifts may result in no-analog communities where foundation species and community genetics play unprecedented roles, possibly leading to novel ecosystems. Long-distance dispersal can enhance the disruption of aboveground-belowground interactions of plants, herbivores, pathogens, symbiotic mutualists, and decomposer organisms. These effects are most likely stronger for latitudinal than for altitudinal range shifts. Disrupted aboveground-belowground interactions may have influenced historical postglacial range shifts as well. Assisted migration without considering aboveground-belowground interactions could enhance risks of such range shift–induced invasions.
  • PLoS One

    Testing the paradox of enrichment along a land use gradient in a multitrophic aboveground and belowground community

    Katrin Meyer, Matthijs Vos, Wolf M. Mooij, (Gera) W.H.G. Hol, Aad J Termorshuizen, Wim H. van der Putten
    In the light of ongoing land use changes, it is important to understand how multitrophic communities perform at different land use intensities. The paradox of enrichment predicts that fertilization leads to destabilization and extinction of predator-prey systems. We tested this prediction for a land use intensity gradient from natural to highly fertilized agricultural ecosystems. We included multiple aboveground and belowground trophic levels and land use-dependent searching efficiencies of insects. To overcome logistic constraints of field experiments, we used a successfully validated simulation model to investigate plant responses to removal of herbivores and their enemies. Consistent with our predictions, instability measured by herbivore-induced plant mortality increased with increasing land use intensity. Simultaneously, the balance between herbivores and natural enemies turned increasingly towards herbivore dominance and natural enemy failure. Under natural conditions, there were more frequently significant effects of belowground herbivores and their natural enemies on plant performance, whereas there were more aboveground effects in agroecosystems. This result was partly due to the “boom-bust” behavior of the shoot herbivore population. Plant responses to herbivore or natural enemy removal were much more abrupt than the imposed smooth land use intensity gradient. This may be due to the presence of multiple trophic levels aboveground and belowground. Our model suggests that destabilization and extinction are more likely to occur in agroecosystems than in natural communities, but the shape of the relationship is nonlinear under the influence of multiple trophic interactions.
  • 2012

    Soil Ecology and Ecosystem Services

    D.H. Wall, Richard D. Bardgett, V. Behan-Pelletier, J.E. Herrick, T.H. Jones, K. Ritz, J. Six, D.R. Strong, Wim H. van der Putten
  • Ecology Letters

    Legacy effects of aboveground–belowground interactions

    Olga Kostenko, Tess Van de Voorde, P.P.J. Mulder, Wim H. van der Putten, T. Martijn Bezemer
    Root herbivory can greatly affect the performance of aboveground insects via changes in plant chemistry. These interactions have been studied extensively in experiments where aboveground and belowground insects were feeding on the same plant. However, little is known about how aboveground and belowground organisms interact when they feed on plant individuals that grow after each other in the same soil. We show that feeding by aboveground and belowground insect herbivores on ragwort (Jacobaea vulgaris) plants exert unique soil legacy effects, via herbivore-induced changes in the composition of soil fungi. These changes in the soil biota induced by aboveground and belowground herbivores of preceding plants greatly influenced the pyrrolizidine alkaloid content, biomass and aboveground multitrophic interactions of succeeding plants. We conclude that plant-mediated interactions between aboveground and belowground insects are also important when they do not feed simultaneously on the same plant.
  • Oikos

    Effects of native and exotic range-expanding plant species on taxonomic and functional composition of nematodes in the soil food web

    Due to climate warming, many plant species shift ranges towards higher latitudes. Plants can disperse faster than most soil biota, however, little is known about how range-expanding plants in the new range will establish interactions with the resident soil food web. In this paper we examine how the soil nematode community from the new range responds to range-expanding plant species compared to related natives. We focused on nematodes, because they are important components in various trophic levels of the soil food web, some feeding on plant roots, others on microbes or on invertebrates. We expected that range expanding plant species have fewer root-feeding nematodes, as predicted by enemy release hypothesis. We therefore expected that range expanders affect the taxonomic and functional composition of the nematode community, but that these effects would diminish with increasing trophic position of nematodes in the soil food web. We exposed six range expanders (including three intercontinental exotics) and nine related native plant species to soil from the invaded range and show that range expanders on average had fewer root-feeding nematodes per unit root biomass than related natives. The range expanders showed resistance against rather than tolerance for root-feeding nematodes from the new range. On the other hand, the overall taxonomic and functional nematode community composition was influenced by plant species rather than by plant origin. The plant identity effects declined with trophic position of nematodes in the soil food web, as plant feeders were influenced more than other feeding guilds. We conclude that range-expanding plant species can have fewer root-feeding nematodes per unit root biomass than related natives, but that the taxonomic and functional nematode community composition is determined more by plant identity than by plant origin. Plant species identity effects decreased with trophic position of nematodes in the soil food web.
  • Basic and Applied Ecology

    Contrasting patterns of herbivore and predator pressure on invasive and native plants

    T. Engelkes, B. Wouters, T. Martijn Bezemer, Jeff A. Harvey, Wim H. van der Putten
    Invasive non-nativeplant species often harbor fewer herbivorous insects than related nativeplant species. However, little is known about how herbivorous insects on non-nativeplants are exposed to carnivorous insects, and even less is known on plants that have recently expanded their ranges within continents due to climate warming. In this study we examine the herbivore load (herbivore biomass per plant biomass), predator load (predator biomass per plant biomass) and predatorpressure (predator biomass per herbivore biomass) on an inter-continental non-native and an intra-continental range-expanding plant species and two congeneric native species. All four plant species co-occur in riparian habitat in north-western Europe. Insects were collected in early, mid and late summer from three populations of all four species. Before counting and weighing the insects were classified to trophic guild as carnivores (predators), herbivores, and transients. Herbivores were further subdivided into leaf-miners, sap-feeders, chewers and gallers. Total herbivore loads were smaller on inter-continental non-native and intra-continental range-expanding plants than on the congeneric natives. However, the differences depended on time within growing season, as well as on the feeding guild of the herbivore. Although the predator load on non-nativeplants was not larger than on natives, both non-nativeplant species had greater predatorpressure on the herbivores than the natives. We conclude that both these non-nativeplant species have better bottom-up as well as top-down control of herbivores, but that effects depend on time within growing season and (for the herbivore load) on herbivore feeding guild. Therefore, when evaluating insects on non-nativeplants, variation within season and differences among feeding guilds need to be taken into account.
  • Applied Soil Ecology

    Matgrass sward plant species benefit from soil organisms

    Pella Brinkman, Ciska Raaijmakers, Tanja Bakx-Schotman, Emilia Hannula, R.H. Kemmers, Wietse de Boer, Wim H. van der Putten
    Soilorganisms are important in the structuring of plant communities. However, little is known about how to apply this knowledge to vegetation management. Here, we examined if soilorganisms may promote plantspecies of characteristic habitats, and suppress plantspecies of disturbed habitats. We classified nineteen fields into four types: characteristic and disturbed matgrass swards and successfully and unsuccessfully restored fields. We recorded the vegetation composition and measured biotic and abiotic soil characteristics of the sites. In a pot experiment, we mixed non-sterilized (with soilorganisms) or sterilized (without soilorganisms) soil inoculum from each field with a common sterilized background soil. We planted seedlings of characteristic matgrass speciesAntennaria dioica and Nardus stricta, of disturbance indicators Deschampsia flexuosa and Agrostis capillaris, or a combination of the four species. At harvest, we measured root and shoot dry mass of all plants. The vegetation composition of characteristic matgrass swards differed from the disturbed and unsuccessfully restored fields. The successfully restored fields were intermediate. The composition of the nematode community tended to follow the same pattern. In the pot experiment, addition of soilorganisms increased the biomass of A. dioica, N. stricta and D. flexuosa, but decreased the biomass of A. capillaris. However, the effect of soilorganisms on plant biomass was not related to field type. A. dioica showed a large variation in biomass in non-sterilized, but not in sterilized soil. Soilorganisms from some sites increased plant biomass, whereas soilorganisms from other sites did not. The biomass of characteristic matgrass plants was lower in the presence of plants from disturbed swards, irrespective of the presence of soilorganisms. Probably A. capillaris was so much larger than the other species, that this overruled effects of added soilorganisms. Soilorganisms promoted growth of plantspecies characteristic of matgrass swards, whereas they reduced growth of a plantspecies characteristic of disturbed fields. Soilorganisms did not change the outcome of plant interactions, which was won by a disturbance indicator. Nevertheless, measurement of the growth stimulating capacity of a soil may be used to assess opportunities for reintroduction of characteristic plantspecies.
  • PLoS One

    Reciprocal effects of litter from exotic and congeneric native plant species via soil nutrients

    Annelein Meisner, Wietse de Boer, J.H.C. Cornelissen, Wim H. van der Putten
    Invasive exotic plant species are often expected to benefit exclusively from legacy effects of their litter inputs on soil processes and nutrient availability. However, there are relatively few experimental tests determining how litter of exotic plants affects their own growth conditions compared to congeneric native plant species. Here, we test how the legacy of litter from three exotic plant species affects their own performance in comparison to their congeneric natives that co-occur in the invaded habitat. We also analyzed litter effects on soil processes. In all three comparisons, soil with litter from exotic plant species had the highest respiration rates. In two out of the three exotic-native species comparisons, soil with litter from exotic plant species had higher inorganic nitrogen concentrations than their native congener, which was likely due to higher initial litter quality of the exotics. When litter from an exotic plant species had a positive effect on itself, it also had a positive effect on its native congener. We conclude that exotic plant species develop a legacy effect in soil from the invaded range through their litter inputs. This litter legacy effect results in altered soil processes that can promote both the exotic plant species and their native congener.
  • Biological Reviews

    Landscape moderation of biodiversity patterns and processes - eight hypotheses

    T. Tscharntke, J.M. Tylianakis, T.A. Rand, R.K. Didham, L. Fahrig, P. Batáry, J. Bengtsson, Y. Clough, T.O. Crist, C.F. Dormann, R.M. Ewers, J. Fründ, R.D. Holt, A. Holzschuh, A.M. Klein, David Kleijn, C. Kremen, D.A. Landis, W. Laurance, D. Lindenmayer, C. Scherber, N. Sodhi, I. Steffan-Dewenter, C. Thies, Wim H. van der Putten, C. Westphal
    Understanding how landscape characteristics affect biodiversity patterns and ecological processes at local and landscape scales is critical for mitigating effects of global environmental change. In this review, we use knowledge gained from human-modified landscapes to suggest eight hypotheses, which we hope will encourage more systematic research on the role of landscape composition and configuration in determining the structure of ecological communities, ecosystem functioning and services. We organize the eight hypotheses under four overarching themes. Section A: ‘landscape moderation of biodiversity patterns’ includes (1) the landscape species pool hypothesis—the size of the landscape-wide species pool moderates local (alpha) biodiversity, and (2) the dominance of beta diversity hypothesis—landscapemoderated dissimilarity of local communities determines landscape-wide biodiversity and overrides negative local effects of habitat fragmentation on biodiversity. Section B: ‘landscape moderation of population dynamics’ includes (3) the cross-habitat spillover hypothesis—landscape-moderated spillover of energy, resources and organisms across habitats, including between managed and natural ecosystems, influences landscape-wide community structure and associated processes and (4) the landscape-moderated concentration and dilution hypothesis—spatial and temporal changes in landscape composition can cause transient concentration or dilution of populationswith functional consequences. Section C: ‘landscape moderation of functional trait selection’ includes (5) the landscape-moderated functional trait selection hypothesis—landscape moderation of species trait selection shapes the functional role and trajectory of community assembly, and (6) the landscape-moderated insurance hypothesis—landscape complexity provides spatial and temporal insurance, i.e. high resilience and stability of ecological processes in changing environments. Section D: ‘landscape constraints on conservation management’ includes (7) the intermediate landscape-complexity hypothesis—landscapemoderated effectiveness of local conservation management is highest in structurally simple, rather than in cleared (i.e. extremely simplified) or in complex landscapes, and (8) the landscape-moderated biodiversity versus ecosystem service management hypothesis—landscape-moderated biodiversity conservation to optimize functional diversity and related ecosystem services will not protect endangered species. Shifting our research focus from local to landscape-moderated effects on biodiversity will be critical to developing solutions for future biodiversity and ecosystem service management.
  • New Phytologist

    Soil biotic impact on plant species shoot chemistry and hyperspectral reflectance patterns

    Sabrina Almeida de Carvalho, Mirka Macel, M. Schlerf, A.K. Skidmore, Wim H. van der Putten
    Recent studies revealed that plant–soil biotic interactions may cause changes in above-ground plant chemistry. It would be a new step in below-ground–above-ground interaction research if such above-ground chemistry changes could be efficiently detected. Here we test how hyperspectral reflectance may be used to study such plant–soil biotic interactions in a nondestructive and rapid way. The native plant species Jacobaea vulgaris and Jacobaea erucifolius, and the exotic invader Senecio inaequidens were grown in different soil biotic conditions. Biomass, chemical content and shoot reflectance between 400 and 2500 nm wavelengths were determined. The data were analysed with multivariate statistics. Exposing the plants to soil biota enhanced the content of defence compounds. The highest increase (400%) was observed for the exotic invader S. inaequidens. Chemical and spectral data enabled plant species to be classified with an accuracy > 85%. Plants grown in different soil conditions were classified with 50–60% correctness. Our data suggest that soil microorganisms can affect plant chemistry and spectral reflectance. Further studies should test the potential to study plant–soil biotic interactions in the field. Such techniques could help to monitor, among other things, where invasive exotic plant species develop biotic resistance or the development of hotspots of crop soil diseases.
  • Entomologia Experimentalis et Applicata

    Effects of diversity and identity of the neighbouring plant community on the abundance of arthropods on individual ragwort (Jacobaea vulgaris) plants

    Olga Kostenko, Saskia S. Grootemaat, Wim H. van der Putten, T. Martijn Bezemer
    The diversity of plant community can greatly affect the abundance and diversity of arthropods associated to that community, but can also influence the composition or abundance of arthropods on individual plants growing in that community. We sampled arthropods and recorded plant size of individual ragwort, Jacobaea vulgaris Gaertner ssp. vulgaris [synonym Senecio jacobaea L. (Asteraceae)], plants transplanted into 70 experimental grassland plots that differed in plant diversity (1–9 species) or that were kept without vegetation. The arthropod fauna was dominated by the specialist aphid Aphis jacobaeae Schrank (Hemiptera: Aphididae). The abundance of aphids on ragwort plants decreased significantly with increasing plant diversity. The abundance of other arthropod species was not affected by the diversity of the surrounding plant community. Plant size was also not affected by the diversity of the surrounding plant community, but varied significantly among monocultures. Ragwort plants were largest in monocultures of legumes. Aphid abundance on ragwort plants, however, was not related to the size of the individual ragwort plants, but was high in monocultures consisting of Tanacetum vulgare L. (Asteraceae) plants. This plant is morphologically similar to ragwort. Even though we observed significant effects of plant diversity, ragwort plants were considerably larger – and the abundance of aphids and other arthropods on ragwort plants substantially higher – in plots without vegetation than in vegetated plots. Our results show that the presence and the diversity of neighbouring plants can provide associational resistance to focal plants growing in that community. We conclude that the surrounding plant community directly affects the abundance of arthropods on focal ragwort plants, and not via the effects of neighbouring plants on the performance of the focal plants.
  • Basic and Applied Ecology

    Can the negative plant-soil feedback of Jacobaea vulgaris be explained by autotoxicity?

    Tess Van de Voorde, M.B.C. Ruijten, Wim H. van der Putten, T. Martijn Bezemer
    Field and bioassay studies with Jacobaea vulgaris (ragwort) have shown that plants grow poorly in soil originating from the rhizosphere of this species and that this can influence the dynamics of ragwort populations during secondary succession. In the present study we examined whether the negative effect of ragwort on conspecifics may be due to autotoxicity. First, we experimentally established that ragwort exerts negative plant–soil feedback. We subsequently examined the inhibitory effects on germination and seedling performance of different strengths of aqueous extracts made from shoot and root tissues of ragwort, and from soil in which ragwort had been growing. The effects of the extracts were tested for seedlings growing in sterilised soil or in glass beads with water. Finally, the inhibitory effect of entire root fragments on seedling performance was tested. We observed that performance of seedlings growing in glass beads was significantly reduced by the high and medium strength root and shoot extracts. Extracts made from soil did not differ significantly from the control, and seedlings growing in sterilised soil were also not affected by ragwort extracts. Seed germination was significantly reduced by the high strength shoot extract only. The root length of seedlings growing in water with root fragments was reduced significantly. We conclude that under laboratory conditions ragwort can be autotoxic and discuss the role that autotoxicity may play in influencing the dynamics of ragwort populations during secondary succession.
  • Science Magazine

    Ecosystem rates of transformation matter response

    David A. Wardle, Richard D. Bardgett, R.M. Callaway, Wim H. van der Putten
    no abstract
  • Frontiers in Ecology and the Environment

    Idiosyncrasy in ecology - what's in a word?

    (Gera) W.H.G. Hol, Katrin Meyer, Wim H. van der Putten
    no abstract
  • Trends in Plant Science

    Redefining plant systems biology: from cell to ecosystem

    J.J.B. Keurentjes, G.C. Angenent, Marcel Dicke, V.A.P. Martins Dos Santos, J. Molenaar, Wim H. van der Putten, P.C. de Ruiter, P.C. Struik, B.P.H.J. Thomma
    Molecular biologists typically restrict systems biology to cellular levels. By contrast, ecologists define biological systems as communities of interacting individuals at different trophic levels that process energy, nutrient and information flows. Modern plant breeding needs to increase agricultural productivity while decreasing the ecological footprint. This requires a holistic systems biology approach that couples different aggregation levels while considering the variables that affect these biological systems from cell to community. The challenge is to generate accurate experimental data that can be used together with modelling concepts and techniques that allow experimentally verifying in silico predictions. The coupling of aggregation levels in plant sciences, termed Integral Quantification of Biological Organization (IQBiO), might enhance our abilities to generate new desired plant phenotypes
  • Ecology

    Additive effects of aboveground polyphagous herbivores and soil feedback in native and range-expanding exotic plants

    Plant biomass and plant abundance can be controlled by aboveground and belowground natural enemies. However, little is known about how the aboveground and belowground enemy effects may add up. We exposed 15 plant species to aboveground polyphagous insect herbivores and feedback effects from the soil community alone, as well as in combination. We envisaged three possibilities: additive, synergistic, or antagonistic effects of the aboveground and belowground enemies on plant biomass. In our analysis, we included native and phylogenetically related range-expanding exotic plant species, because exotic plants on average are less sensitive to aboveground herbivores and soil feedback than related natives. Thus, we examined if lower sensitivity of exotic plant species to enemies also alters aboveground-belowground interactions. In a greenhouse experiment, we exposed six exotic and nine native plant species to feedback from their own soil communities, aboveground herbivory by polyphagous insects, or a combination of soil feedback and aboveground insects and compared shoot and root biomass to control plants without aboveground and belowground enemies. We observed that for both native and range-expanding exotic plant species effects of insect herbivory aboveground and soil feedback added up linearly, instead of enforcing or counteracting each other. However, there was no correlation between the strength of aboveground herbivory and soil feedback. We conclude that effects of polyphagous aboveground herbivorous insects and soil feedback add up both in the case of native and related range-expanding exotic plant species, but that aboveground herbivory effects may not necessarily predict the strengths of soil feedback effects.
  • Journal of Plant Ecology

    Effects of plant–soil feedback on tree seedling growth under arid conditions

    S.S. Meijer, M. Holmgren, Wim H. van der Putten
    Aims Plants are able to influence their growing environment by changing biotic and abiotic soil conditions. These soil conditions in turn can influence plant growth conditions, which is called plant–soil feedback. Plant–soil feedback is known to be operative in a wide variety of ecosystems ranging from temperate grasslands to tropical rain forests. However, little is known about how it operates in arid environments. We examined the role of plant–soil feedbacks on tree seedling growth in relation to water availability as occurring in arid ecosystems along the west coast of South America. Methods In a two-phased greenhouse experiment, we compared plant–soil feedback effects under three water levels (no water, 10% gravimetric moisture and 15% gravimetric moisture). We used sterilized soil inoculated with soil collected from northwest Peru (Prosopis pallida forests) and from two sites in north-central Chile (Prosopis chilensis forest and scrublands without P. chilensis). Important Findings Plant–soil feedbacks differed between plant species and soil origins, but water availability did not influence the feedback effects. Plant–soil feedbacks differed in direction and strength in the three soil origins studied. Plant–soil feedbacks of plants grown in Peruvian forest soil were negative for leaf biomass and positive for root length. In contrast, feedbacks were neutral for plants growing in Chilean scrubland soil and positive for leaf biomass for those growing in Chilean forest soil. Our results show that under arid conditions, effects of plant–soil feedback depend upon context. Moreover, the results suggest that plant–soil feedback can influence trade-offs between root growth and leaf biomass investment and as such that feedback interactions between plants and soil biota can make plants either more tolerant or vulnerable to droughts. Based on dissecting plant–soil feedbacks into aboveground and belowground tissue responses, we conclude that plant–soil feedback can enhance plant colonization in some arid ecosystems by promoting root growth.
  • Science Magazine

    Terrestrial ecosystem responses to species gains and losses

    David A. Wardle, Richard D. Bardgett, R.M. Callaway, Wim H. van der Putten
    Ecosystems worldwide are losing some species and gaining others, resulting in an interchange of species that is having profound impacts on how these ecosystems function. However, research on the effects of species gains and losses has developed largely independently of one another. Recent conceptual advances regarding effects of species gain have arisen from studies that have unraveled the mechanistic basis of how invading species with novel traits alter biotic interactions and ecosystem processes. In contrast, studies on traits associated with species loss are fewer, and much remains unknown about how traits that predispose species to extinction affect ecological processes. Species gains and losses are both consequences and drivers of global change; thus, explicit integration of research on how both processes simultaneously affect ecosystem functioning is key to determining the response of the Earth system to current and future human activities.
  • Ecology Letters

    The ecological and evolutionary implications of merging different types of networks

    C. Fontaine, P.R. Guimaraes, S. Kefi, N. Loeuille, J. Memmott, Wim H. van der Putten, F.J.F. Van Veen, E. Thebault
    Interactions among species drive the ecological and evolutionary processes in ecological communities. These interactions are effectively key components of biodiversity. Studies that use a network approach to study the structure and dynamics of communities of interacting species have revealed many patterns and associated processes. Historically these studies were restricted to trophic interactions, although network approaches are now used to study a wide range of interactions, including for example the reproductive mutualisms. However, each interaction type remains studied largely in isolation from others. Merging the various interaction types within a single integrative framework is necessary if we want to further our understanding of the ecological and evolutionary dynamics of communities. Dividing the networks up is a methodological convenience as in the field the networks occur together in space and time and will be linked by shared species. Herein, we outline a conceptual framework for studying networks composed of more than one type of interaction, highlighting key questions and research areas that would benefit from their study.
  • Entomologia Experimentalis et Applicata

    Effects of soil organisms on aboveground multitrophic interactions are consistent between plant genotypes mediating the interaction

    Patrick Kabouw, Martine Kos, S. Kleine, E.A. Vockenhuber, Joop J.A. van Loon, Wim H. van der Putten, Nicole M. van Dam, Arjen Biere
    Belowground communities can affect interactions between plants and aboveground insect communities. Such belowground–aboveground interactions are known to depend on the composition of belowground communities, as well as on the plant species that mediates these interactions. However, it is largely unknown whether the effect of belowground communities on aboveground plant–insect interactions also depends on genotypic variation within the plant species that mediates the interaction. To assess whether the outcome of belowground–aboveground interactions can be affected by plant genotype, we selected two white cabbage cultivars [Brassica oleracea L. var. capitata (Brassicaceae)]. From previous studies, it is known that these cultivars differ in their chemistry and belowground and aboveground multitrophic interactions. Belowground, we inoculated soils of the cultivars with either nematodes or microorganisms and included a sterilized soil as a control treatment. Aboveground, we quantified aphid [Brevicoryne brassicae (L.) (Hemiptera: Aphididae)] population development and parasitoid [Diaeretiella rapae (McIntosh) (Hymenoptera: Braconidae)] fitness parameters. The cultivar that sustained highest aphid numbers also had the best parasitoid performance. Soil treatment affected aphid population sizes: microorganisms increased aphid population growth. Soil treatments did not affect parasitoid performance. Cultivars differed in their amino acid concentration, leaf relative growth rate, and root, shoot, and phloem glucosinolate composition but showed similar responses of these traits to soil treatments. Consistent with this observation, no interactions were found between cultivar and soil treatment for aphid population growth or parasitoid performance. Overall, the aboveground community was more affected by cultivar, which was associated with glucosinolate profiles, than by soil community.
  • Journal of Ecology

    Comparison of nutrient acquisition in exotic plant species and congeneric natives

    Annelein Meisner, Wietse de Boer, Koen Verhoeven, H.T.S. Boschker, Wim H. van der Putten
    1.The ability of exotic plant species to establish and expand in new areas may be enhanced by a relatively high ability to acquire soil nutrients. To test this hypothesis, we predicted that the capacity for nutrient acquisition would be higher in seedlings of exotic species than in seedlings of native congeners. 2.We selected the five exotic species that had recently increased in abundance in a riverine habitat in the Netherlands and that had a native congener that was common in the same habitat. We grew seedlings of each of these ten species singly in pots of soil from this habitat in a glasshouse. After two months, we measured the final dry mass and N and P content of each plant and components of microbial biomass and nutrient mineralization in the soil. We also measured these soil characteristics in pots that had been left unplanted. 3.Exotic and native congeners did not differ consistently in the uptake of N or P or in effects on components of soil mineralization. Within a genus, values of these measurements were sometimes higher, sometimes lower and sometimes similar to the exotic when compared with the native species. 4.Depending upon the statistical analysis used, biomarker-based biomass of arbuscular mycorrhizal fungi was generally higher in soil planted with exotic than with native species. Most measures of microbial biomass and soil mineralization were higher in pots that had been planted with plants than in pots with no plant. 5.Synthesis. Our results do not suggest that invasive, exotic plant species generally possess greater capacity for nutrient acquisition during the early establishment than native species do.
  • Diversity and Distributions

    Factors relating to regional and local success of exotic plant species in their new range

    Tanja Speek, L.A.P. Lotz, W.A. Ozinga, W.L.M. Tamis, J.H.J. Schaminee, Wim H. van der Putten
    Aim  To estimate invasiveness of exotic plant species, many studies have used the frequency of occurrence within a defined region. This measure is informative on how widespread exotics are, however, it does not inform on their local dominance, which is crucial for conservation of biodiversity and ecosystem functioning. The aim of the present study is to determine if regional frequency of occurrence of exotic plant species indeed is indicative of their local dominance. We also determined which plant traits and other factors predict regional and local frequencies best. Location  The Netherlands. Methods  We used information on exotic plant species established in The Netherlands and compared traits relating to their frequency of occurrence regionally (the entire country) and their frequency of dominance locally (in 1–100 m2 quadrats). We created minimal adequate models with factors explaining regional frequency and frequency of local dominance of 111 exotic plant species in The Netherlands. Results  The model that used plant traits to explain regional frequency of exotic plant species differed from the models that best explained their frequency of local dominance. Regionally, the factors that correlated with frequency were: life form, height, polyploidy, length of flowering season, residence time, human use and origin. The factors that correlated to frequency of local dominance were lateral vegetative spread and residence time. Main conclusions  We conclude that plant traits relating to the regional frequency of exotic plant species differ from those that relate to their frequency of local dominance. The implication of our results is that predictive studies on plant invasiveness based on regional frequencies may not be indicative of the local impacts. Since the prediction of local impacts is crucial for conservation and risk assessment, our study emphasized the need for better information on the local abundance of exotic invaders.
  • Journal of Ecology

    Intra- and interspecific plant-soil interactions, soil legacies and priority effects during old-field succession

    Tess Van de Voorde, Wim H. van der Putten, T. Martijn Bezemer
    1. Legacy effects of plant influences on abiotic and biotic soil properties can result in priority effects that influence the structure and composition of plant communities. To better understand the role of these plant–soil interactions, here we expand the concept of plant–soil feedbacks from a within-species approach (intraspecific plant–soil feedback) to a between-species approach (interspecific plant–soil interactions). 2. In a greenhouse experiment, we tested how the early successional Jacobaea vulgaris affects its own performance and the performance of 30 co-occurring plant species via changes in abiotic and biotic soil conditions. In addition, we examined the reciprocal effect of the co-occurring species on J. vulgaris. 3. Our study had three important results. First, J. vulgaris exhibits strong negative plant–soil feedback. Secondly, there were large differences among the co-occurring species in interspecific plant–soil effects on J. vulgaris growth. Approximately, half the species reduced J. vulgaris performance, whereas the other half had no effect. Thirdly, soil conditioned by J. vulgaris had a positive or neutral effect on the growth of the co-occurring species. 4. To test the soil effects of entire plant communities, in 10 old-fields that differed in time since abandonment we recorded the identity of all plants surrounding J. vulgaris individuals. We calculated the weighted soil effect of this community on J. vulgaris and the reciprocal effect of J. vulgaris on the community. There was a positive linear relationship between time since abandonment and the weighted feedback effect of J. vulgaris on the plant community. 5. We suggest three mechanisms how the legacy of plant–soil interactions may enhance the rate of succession through priority effects: early successional plant species exert negative plant–soil feedback; co-occurring plant species cause negative interspecific plant–soil effects to the early successional species; and the early successional species have overall positive interspecific plant–soil effects on the co-occurring plant species. 6.Synthesis. The performance of an early successional species can be reduced directly by the legacy effects of intraspecific plant–soil feedback, as well as indirectly by the legacy effects of both intra- and interspecific plant–soil interactions. These intra- and interspecific plant–soil interactions can prioritize transitions of plant species in plant communities.
  • Nature

    Non-natives: 141 scientists object

    D. Simberloff, Wim H. van der Putten
    Supplementary information to: Non-natives: 141 scientists object Full list of co-signatories to a Correspondence published in Nature 475, 36 (2011); doi: 10.1038/475036a. Daniel Simberloff University of Tennessee, Knoxville, Tennessee, USA. dsimberloff@utk.edu Jake Alexander Institute of Integrative Biology, Zurich, Switzerland. Fred Allendorf University of Montana, Missoula, Montana, USA. James Aronson CEFE/CNRS, Montpellier, France. Pedro M. Antunes Algoma University, Sault Ste. Marie, Ontario, Canada. Sven Bacher University of Fribourg, Fribourg, Switzerland. Richard Bardgett Lancaster University, Lancaster, UK. Sandro Bertolino University of Turin, Grugliasco, Italy. Melanie Bishop Macquarie University, Sydney, Australia. Tim M. Blackburn Zoological Society of London, London, UK. April Blakeslee Smithsonian Environmental Research Center, Edgewater, Maryland, USA. Dana Blumenthal USDA Agricultural Research Service, Fort Collins, Colorado, USA. Alejandro Bortolus Centro Nacional Patagónico-CONICET, Puerto Madryn, Argentina. Ralf Buckley Griffith University, Southport, Queensland, Australia. Yvonne Buckley CSIRO Ecosystem Sciences and The University of Queensland, ARC Centre of Excellence in Environmental Decisions, St Lucia, Queensland, Australia. Jeb Byers The University of Georgia, Athens, Georgia, USA. Ragan M. Callaway University of Montana, Missoula, Montana, USA. Faith Campbell The Nature Conservancy, Arlington, Virginia, USA. Karl Campbell Island Conservation, Santa Cruz, California, USA. Marnie Campbell Central Queensland University, Queensland, Australia. James T. CarltonWilliams College — Mystic Seaport, Mystic, Connecticut, USA. Phillip Cassey University of Adelaide, Adelaide, South Australia, Australia. Jane Catford The University of Melbourne, Melbourne, Victoria, Australia. Laura Celesti-Grapow Sapienza University of Rome, Rome, Italy. John Chapman Hatfield Marine Science Center, Oregon State University, Newport, Oregon, USA. Paul Clark Natural History Museum, London, UK. Andre Clewell Tall Timbers Research Station, Tallahassee, Florida USA. João Canning Clode Smithsonian Environmental Research Center, Edgewater, Maryland USA Andrew Chang Smithsonian Environmental Research Center, Edgewater, Maryland, USA. Milan Chytrý Masaryk University, Brno, Czech Republic. Mick Clout University of Auckland, Auckland, New Zealand. Andrew Cohen Center for Research on Aquatic Bioinvasions, Richmond, California, USA. Phil Cowan Landcare Research, Palmerston North, New Zealand. Robert H. Cowie University of Hawaii, Honolulu, Hawaii, USA. Alycia W. Crall Colorado State University, Fort Collins, Colorado, USA. Jeff Crooks Tijuana River National Estuarine Research Reserve, Imperial Beach, California, USA. Marty Deveney South Australian Aquatic Sciences Centre,West Beach, Australia. Kingsley Dixon Kings Park and Botanic Garden,West Perth, Australia. Fred C. Dobbs Old Dominion University, Norfolk, Virginia, USA. David Cameron Duffy University of Hawaii Manoa, Honolulu, Hawaii, USA. Richard Duncan Lincoln University, Lincoln, New Zealand. Paul R. Ehrlich Stanford University, Stanford, California, USA. Lucius Eldredge Bishop Museum, Honolulu, Hawaii, USA. Neal Evenhuis Bishop Museum, Honolulu, Hawaii, USA. Kurt D. Fausch Colorado State University, Fort Collins, Colorado, USA. Heike Feldhaar University of Osnabrück, Osnabrück, Germany. Jennifer Firn Queensland University of Technology, Brisbane, Queensland, Australia. Amy Fowler Smithsonian Environmental Research Center, Edgewater, Maryland, USA. Bella Galil National Institute of Oceanography, Haifa, Israel. Emili Garcia-Berthou Universitat de Girona, Girona, Spain. Jonathan Geller Moss Landing Marine Laboratories, Moss Landing, California, USA. Piero Genovesi Italian National Institute for Environmental Protection and Research, Rome, Italy. Esther Gerber CABI Europe, Delemont, Switzerland. Francesca Gherardi Universita’ di Firenze, Firenze, Italy. Stephan Gollasch Hamburg, Germany. Doria Gordon University of Florida, Gainesville, Florida, USA. Jim Graham Colorado State University, Fort Collins, Colorado, USA. Paul Gribben University of Technology, Sydney, Australia. Blaine Griffen Smithsonian Environmental Research Center, Edgewater, Maryland, USA. Edwin D. Grosholz University of California, Davis, California, USA. Chad Hewitt Central Queensland University, Queensland, Australia. José L. Hierro CONICET-Universidad Nacional de La Pampa, La Pampa, Argentina. Philip Hulme Lincoln University, Lincoln, New Zealand. Pat Hutchings Australian Museum, Sydney, Australia. Vojtěch Jarošík Charles University, Prague, Czech Republic. Jonathan M. Jeschke Technische Universität München, Freising- Weihenstephan, Germany. Chris Johnson University of Tasmania, Hobart, Tasmania, Australia. Ladd Johnson Université Laval, Ville de Québec, Quebec, Canada. Emma L. Johnston University of New South Wales, Sydney, Australia. Carl G. Jones Durrell Wildlife Conservation Trust, Jersey, Channel Islands, UK. Reuben Keller University of Chicago, Chicago, Illinois, USA. Carolyn M. King University of Waikato, Hamilton, New Zealand. Bart G. J. Knols Academic Medical Center, Amsterdam, The Netherlands; K&S Consulting, Dodewaard, the Netherlands. Johannes Kollmann Technische Universität München, Freising, Germany. Thomas Kompas The Australian National University, Canberra, Australia. Peter M. Kotanen University of Toronto at Mississauga, Mississauga, Ontario, Canada. Ingo Kowarik Technische Universität Berlin, Berlin, Germany. Ingolf Kühn Helmholtz-Zentrum für Umweltforschung, Halle, Germany. Sabrina Kumschick Colorado State University, Fort Collins, Colorado, USA. Brian Leung McGill University, Montreal, Quebec, Canada. Andrew Liebhold USDA Forest Service, Morgantown, West Virginia, USA. Hugh MacIsaac University of Windsor, Windsor, Ontario, Canada. Richard Mack Washington State University, Pullman, Washington, USA. Deborah G. McCullough Michigan State University, East Lansing, Michigan, USA. Robbie McDonald The Food and Environmental Research Agency, Department for Environment, Food, and Rural Affairs, Stonehouse, UK. David M. Merritt United States Forest Service, Fort Collins, Colorado, USA. Laura Meyerson University of Rhode Island, Kingston, Rhode Island, USA. Dan Minchin Marine Organism Investigations, Killaloe, Ireland. Harold A. Mooney Stanford University, Stanford, California, USA. Jeffrey T. Morisette United States Geological Survey, Fort Collins Science Center, Fort Collins, Colorado, USA. Peter Moyle University of California, Davis, California, USA. Heinz Müller-Schärer Université de Fribourg/Pérolles, Fribourg, Switzerland. Brad R. Murray University of Technology Sydney, Sydney, Australia. Stefan Nehring Bundesamt für Naturschutz, Bonn, Germany. Wendy Nelson National Institute of Water and Atmospheric Research, Wellington, New Zealand. Wolfgang Nentwig University of Bern, Bern, Switzerland. Stephen J. Novak Boise State University, Boise, Idaho, USA. Anna Occhipinti Universita di Pavia, Pavia, Italy. Henn Ojaveer University of Tartu, Pärnu, Estonia. Bruce Osborne University College Dublin, Dublin, Ireland. Richard S. Ostfeld Cary Institute of Ecosystem Studies, Millbrook, New York, USA. John Parker Smithsonian Environmental Research Center, Edgewater, Maryland, USA. Judith Pederson Worcester, Massachusetts, USA. Jan Pergl Academy of Sciences of the Czech Republic, Pruhonice, Czech Republic. Megan L. Phillips University of Technology Sydney, Sydney, Australia. Petr Pyšek Academy of Sciences, Průhonice, Czech Republic. Marcel Rejmánek University of California, Davis, California, USA. Anthony Ricciardi McGill University, Montreal, Quebec, Canada. Carlo Ricotta University of Rome ‘La Sapienza’, Rome, Italy. David Richardson Stellenbosch University, Matieland, South Africa. Gil Rilov National Institute of Oceanography, Haifa, Israel. Euan Ritchie Deakin University, Burwood, Victoria, Australia. Peter A. Robertson Food and Environment Research Agency, York, UK. Joe Roman University of Vermont, Burlington, Vermont, USA. Gregory Ruiz Smithsonian Environmental Research Center, Edgewater, Maryland, USA. Hanno Schaefer Harvard University, Cambridge, Massachusetts, USA. Britta Schaffelke Australian Institute of Marine Science, Townsville, Australia. Kristina A. Schierenbeck California State University, Chico, California, USA. Don C. Schmitz Florida Fish and Wildlife Conservation Commission, Tallahassee, Florida, USA. Evangelina Schwindt Centro Nacional Patagónico-CONICET, Puerto Madryn, Argentina. Jim Seeb University of Washington, Seattle, Washington, USA. L. David Smith Smith College, Northampton, Massachusetts, USA. Gideon F. Smith University of Pretoria, Pretoria, South Africa. Thomas Stohlgren Colorado State University, Fort Collins, Colorado, USA. David L. Strayer Cary Institute of Ecosystem Studies, Millbrook, New York, USA. Donald Strong University of California, Davis, California,USA. William J. Sutherland University of Cambridge , Cambridge, UK. Thomas Therriault Pacific Biological Station, Nanaimo, British Columbia, Canada. Wilfried Thuiller Université Joseph Fourier, Grenoble, France. Mark Torchin Smithsonian Tropical Research Institute, Balboa, Panama. Wim van der Putten Netherlands Institute of Ecology, Wageningen, the Netherlands. Montserrat Vilà Estación Biológica de Doñana, Sevilla, Spain. Betsy Von Holle University of Central Florida, Orlando, Florida, USA. Inger Wallentinus University of Gothenburg, Goteborg, Sweden. David Wardle Swedish University of Agricultural Sciences, Umeå, Sweden. Mark Williamson University of York, York, UK. John Wilson Stellenbosch University, Matieland, South Africa. Marten Winter Helmholtz-Zentrum für Umweltforschung, Halle, Germany. Lorne M. Wolfe Georgia Southern University, Statesboro, Georgia, USA. Jeff Wright The University of Tasmania, Launceston, Australia. Marjorie Wonham Quest University, Squamish, British Columbia, Canada. Chela Zabin Smithsonian Environmental Research Center, Edgewater, Maryland, USA.
  • PLoS One

    Enhancement of late successional plants on ex-arable land by soil inoculations

    Vanesa Carbajo, B. Den Braber, Wim H. van der Putten, Gerlinde De Deyn
    Restoration of species-rich grasslands on ex-arable land can help the conservation of biodiversity but faces three big challenges: absence of target plant propagules, high residual soil fertility and restoration of soil communities. Seed additions and top soil removal can solve some of these constraints, but restoring beneficial biotic soil conditions remains a challenge. Here we test the hypotheses that inoculation of soil from late secondary succession grasslands in arable receptor soil enhances performance of late successional plants, especially after top soil removal but pending on the added dose. To test this we grew mixtures of late successional plants in arable top (organic) soil or in underlying mineral soil mixed with donor soil in small or large proportions. Donor soils were collected from different grasslands that had been under restoration for 5 to 41 years, or from semi-natural grassland that has not been used intensively. Donor soil addition, especially when collected from older restoration sites, increased plant community biomass without altering its evenness. In contrast, addition of soil from semi-natural grassland promoted plant community evenness, and hence its diversity, but reduced community biomass. Effects of donor soil additions were stronger in mineral than in organic soil and larger with bigger proportions added. The variation in plant community composition was explained best by the abundances of nematodes, ergosterol concentration and soil pH. We show that in controlled conditions inoculation of soil from secondary succession grassland into ex-arable land can strongly promote target plant species, and that the role of soil biota in promoting target plant species is greatest when added after top soil removal. Together our results point out that transplantation of later secondary succession soil can promote grassland restoration on ex-arable land.
  • Soil Biology & Biochemistry

    Modelling C and N mineralisation in soil food webs during secondary succession on ex-arable land

    R. Holtkamp, Annemieke van der Wal, Paul Kardol, Wim H. van der Putten, P.C. de Ruiter, S.C. Dekker
    The rate of secondary succession after land abandonment depends on the interplay between aboveground and belowground processes. Changes in vegetation composition lead to altered amounts and composition of soil organic matter (SOM) with consequences for the abundance and functioning of the soil food web. In turn, soil food web structure determines the mineralisation rate of nutrients that can be taken up by plants. This study analyses changes in the C and N mineralisation rates along with soil food web structure during secondary succession after land abandonment. In a previous study, changes in soil food web structure and SOM quantity and quality were measured at different stages of secondary succession on abandoned arable fields (abandoned for 2, 9 and 22 years and a heathland, which is the assumed target of the secondary succession). Based on these measurements we expected the C and N mineralisation rates to increase during secondary succession. The key hypothesis is that with a description of the soil food webs in terms of quantified biomasses, natural death rates, energy conversion efficiencies and diets enables a calculation of C and N mineralisation rates in soils. The basic assumptions connected to this hypothesis are that on a time-scale of years the population sizes are in steady state. We also calculated mineralisation rates per trophic level and energy channel. Based on the same measurements we expected that the contributions by the lower trophic level groups will increase as well as the mineralisation rates by bacterial and fungal energy channels. Measured C and N mineralisation indeed increased during the 22-year period of abandonment. The calculated C and N mineralisation rates showed the same trend after land abandonment as the measured values. Calculated contributions to mineralisation of organisms at trophic level 1 increase during secondary succession following land abandonment. The fungal decomposition channel contributed more to N mineralisation than the bacterial decomposition channel, whereas both channels contributed equally to C mineralisation rates. Direct contributions by higher trophic levels to mineralisation decreased during secondary succession. However, higher trophic levels were direct important for N mineralisation and indirect for both C and N mineralisation due to their effect on biomass turnover rates of groups at lower trophic levels. The increasing total N mineralisation rate of the soil food web, however, does not benefit plants, as during succession plant species that mainly grow under high nutrient availability are replaced by species that can grow in nutrient poor condition.
  • 2011

    Microbial ecology and nematode control in natural ecosystems

    S.R. Costa, Wim H. van der Putten, B.R. Kerry
    Plant-parasitic nematodes have traditionally been studied in agricultural systems, where they can be pests of importance on a wide range of crops. Nevertheless, nematode ecology in natural ecosystems is receiving increasing interest because of the role of nematodes in soil food webs, nutrient cycling, influences on vegetation composition, and because of their indicator value. In natural ecosystems, plant-parasitic nematode populations can be controlled by bottom-up, horizontal and top-down mechanisms, with more than one mechanism acting upon a given population. Moreover, in natural ecosystems soil nematodes inhabit probably more heterogeneous environment than in agricultural soils. New breakthroughs are to be expected when new molecular-based methods can be used for nematode research in natural ecosystems. Thus far, nematode ecology has strongly relied on coupling conventional abundance and diversity measurements with conceptual population ecology. Biochemical and molecular methods are changing our understanding of naturally co-evolved multitrophic plant-nematode-antagonist interactions in nature, the inter-connections within the soil food web and the extent to which nematodes are involved in many, disparate, soil processes. We foresee that finer nematode interactions that lead to their management and control can only be fully understood through the joint effort of different research disciplines that investigate such interactions from the molecular to the ecosystem level.
  • Phytopathologia Mediterranea

    First record of Helicotylenchus varicaudatus Yuen, 1964 (Nematoda: Hoplolaimidae) parasitizing Ammophila arenaria (L.) Link in Portuguese coastal sand dunes

    C. Schreck Reis, M.C. Vieira dos Santos, M. Marais, M.S. N. de A. Santos, Henk Duyts, H. Freitas, Wim H. van der Putten, I.M. de O. Abrantes
    A spiral nematode, Helicotylenchus varicaudatus Yuen, 1964, parasitizing Ammophila arenaria (L.) Link, the dominant grass in the Portuguese coastal sand dunes, is reported from Portugal for the first time and raises to seven the number of Helicotylenchus species detected in Portugal. A redescription of the species, with illustrations, and light and scanning electron microscope images of both female and male specimens, is presented. The rDNA containing the internal transcribed spacer regions (ITS) of H. varicaudatus was analysed with ITS-RFLP using the restriction endonuclease Hinf I. Molecular data from the ribosomal small subunit (SSU) (18S) confirmed the identification
  • Journal of Ecology

    Plant-soil feedback: Experimental approaches, statistical analyses and biological interpretations

    Pella Brinkman, Wim H. van der Putten, E.J. Bakker, Koen Verhoeven
    1. Feedback between plants and soil organisms has become widely recognized as a driving force of community composition and ecosystem functioning. However, there is little uniformity in quantification and analysis of plant soil feedback effects. Meta-analysis suggested that the various experimental methods tend to result in different feedback values. Yet, a direct comparison of the different experimental approaches and their statistical analyses is lacking. 2. We used currently applied methods to calculate plant soil feedback value ranges and compared their statistical analyses to those based on actual biomass data. Then, we re-analysed a case study to compare plant soil feedback values obtained under the same environmental conditions, but using different experimental approaches: soil sterilization, addition of soil inoculum, and soil conditioning by own vs. foreign plant species. 3. Different measures to calculate plant soil feedback values were more variable in positive than in negative feedback values. Analysis of calculated feedback values that are based on treatment averages can lead to a serious inflation of type I errors. 4. In our case study, both the strength and the direction of the feedback effects depended on the experimental approach that was chosen, leading to diverging conclusions on whether feedback to a certain soil was positive or negative. Soil sterilization and addition of soil organisms yielded larger feedback than comparison of own and foreign soil. 5. Synthesis. The ecological interpretation of plant soil feedback effects strongly depends on the experimental procedure. When the research question focuses on the strength and the sign of plant soil feedback, soil sterilization (presumed that the side effect of increased nutrient availability can be controlled) or addition of soil inoculum is to be preferred. When the research question concerns the specificity of soil feedback effects, plant performance can be better compared between own and foreign soil. We recommend that when using calculated feedback values, the original data need to be presented as well in order to trace the cause of the effect.
  • Plant and Soil

    Effects of intraspecific variation in white cabbage (Brassica oleracea var. capitata) on soil organisms

    Patrick Kabouw, Wim H. van der Putten, Nicole M. van Dam, Arjen Biere
    Intraspecific variation in plants can affect soil organisms. However, little is known about whether the magnitude of the effect depends on the degree of interaction with the roots. We analyzed effects of plant intraspecific variation on root herbivores and other soil organisms that interact directly with living plant roots, as well as on decomposer organisms that interact more indirectly with roots. We used four different white cabbage (Brassica oleracea var. capitata) cultivars exhibiting a high degree of intraspecific variation in root lucosinolate profiles. Intraspecific variation affected root-feeding nematodes, whereas decomposer organisms such as earthworms and Collembola were not affected. Root-feeding nematodes were most abundant in one of the cultivars, Badger Shipper, which lacked the glucosinolate gluconasturtiin. The effect of the intraspecific variation in glucosinolate composition may have been restricted to root-feeding nematodes due to the rapid degradation of glucosinolates and their breakdown products in the soil. Additionally, the low biomass of root-feeding nematodes, relative to other soil organisms, limits the possibility to affect higher trophic level organisms. Our results show that variation in root chemistry predominantly affects belowground herbivores and that these effects do not extend into the soil food web.
  • 2010

    Applications of community ecology approaches in terrestrial ecosystems: local problems, remote causes

    Community ecology is the study of the interactions between populations of co-existing species. This book provides a survey of the state-of-the-art in theory and applications of community ecology, with special attention to topology, dynamics, the importance of spatial and temporal scale, as well as applications to emerging problems in human-dominated ecosystems (including the restoration and reconstruction of viable communities). It adopts a mainly theoretical approach and focuses on the use of network-based theory which remains little explored in standard community ecology textbooks. The book includes discussion of the effects of biotic invasions on natural communities, the linking of ecological network structure to empirically measured community properties and dynamics, the effects of evolution on community patterns and processes, and the integration of fundamental interactions into ecological networks. A final chapter indicates future research directions for the discipline. This book provides ideal graduate seminar course material.
  • Ecology Letters

    Reduction of rare soil microbes modifies plant-herbivore interactions

    (Gera) W.H.G. Hol, Wietse de Boer, Aad J Termorshuizen, Katrin Meyer, J.H.M. Schneider, Nicole M. van Dam, Hans van Veen, Wim H. van der Putten
    Rare species are assumed to have little impact on community interactions and ecosystem processes. However, very few studies have actually attempted to quantify the role of rare species in ecosystems. Here we compare effects of soil community assemblages on plant-herbivore interactions and show that reduction of rare soil microbes increases both plant biomass and plant nutritional quality. Two crop plant species growing in soil where rare microbes were reduced, had tissues of higher nutritional quality, which theoretically makes them more susceptible to pest organisms such as shoot-feeding aphids and root-feeding nematodes. Reduction of rare microbes increased aphid body size in the absence of nematodes; nematodes always reduced aphid body size independent of the soil microbial community. This study is the first to show that rare soil microbes are not redundant but may play a role in crop protection by enhancing aboveground and belowground plant defence. It remains to be tested whether these are direct effects of rare soil microbes on plants and herbivores, or indirect effects via shifts in the microbial soil community assemblages
  • Biological Conservation

    Interactions between invasive plants and insect herbivores: A plea for a multitrophic perspective

    Jeff A. Harvey, Tibor Bukovinszky, Wim H. van der Putten
    Invasive species represent one of the most important threats to biodiversity worldwide, with consequences for ecosystem functioning and the delivery of important ecological services to society. Several hypotheses have been generated to explain the success of exotic plants in their new ranges, with escape from their old natural enemies, such as pathogens and herbivores (the ‘enemy release hypothesis’) and novel defensive chemistry (the ‘novel weapons hypothesis’) receiving considerable attention. Thus far, virtually all studies of exotic plants and insects have been conducted in a strictly bi-trophic framework involving plants and herbivores. On the other hand, it has been argued that a better understanding of the forces regulating community structure and function should include natural enemies of the herbivores. Furthermore, indirect interactions between organisms in the plant roots (below-ground) and shoots (above-ground) are known to strongly effect the behaviour and performance of consumers in the opposite ‘compartment’. Here, we discuss a range of physiological, evolutionary and ecological aspects of plant–herbivore-natural enemy interactions involving exotic plants. Further, interactions between soil and above-ground organisms are explored with respect to studies with exotic plants. We argue that it is important to link population and community ecology to individual-level variation in the physiology and behaviour of insects across several trophic levels in studies with invasive plants. Future research with invaders should also aim to integrate physically separated compartments (e.g. plant roots and shoots). This will facilitate a more complete understanding of the factors underlying the success (or failure) of exotic plants to spread and become dominant in their new ranges. Moreover, these data will also help to unravel the relative importance of top-down and bottom-up processes in regulating communities in which exotic plants have become established. Lastly, we discuss consequences for conservation.
  • Annals of Botany

    Climate change and invasion by intracontinental range-expanding exotic plants: the role of biotic interactions

    Elly Morrien, T. Engelkes, Mirka Macel, Annelein Meisner, Wim H. van der Putten
    Background and Aims: In this Botanical Briefing we describe how the interactions between plants and their biotic environment can change during range-expansion within a continent and how this may influence plant invasiveness. Scope: We address how mechanisms explaining intercontinental plant invasions by exotics (such as release from enemies) may also apply to climate-warming-induced range-expanding exotics within the same continent. We focus on above-ground and below-ground interactions of plants, enemies and symbionts, on plant defences, and on nutrient cycling. Conclusions: Range-expansion by plants may result in above-ground and below-ground enemy release. This enemy release can be due to the higher dispersal capacity of plants than of natural enemies. Moreover, lower-latitudinal plants can have higher defence levels than plants from temperate regions, making them better defended against herbivory. In a world that contains fewer enemies, exotic plants will experience less selection pressure to maintain high levels of defensive secondary metabolites. Range-expanders potentially affect ecosystem processes, such as nutrient cycling. These features are quite comparable with what is known of intercontinental invasive exotic plants. However, intracontinental range-expanding plants will have ongoing gene-flow between the newly established populations and the populations in the native range. This is a major difference from intercontinental invasive exotic plants, which become more severely disconnected from their source populations.
  • Environmental Microbiology

    Influences of space, soil, nematodes and plants on microbial community composition of chalk grassland soils

    E. Yergeau, T. Martijn Bezemer, K. Hedlund, S.R. Mortimer, George Kowalchuk, Wim H. van der Putten
    Microbial communities respond to a variety of environmental factors related to resources (e.g. plant and soil organic matter), habitat (e.g. soil characteristics) and predation (e.g. nematodes, protozoa and viruses). However, the relative contribution of these factors on microbial community composition is poorly understood. Here, we sampled soils from 30 chalk grassland fields located in three different chalk hill ridges of Southern England, using a spatially explicit sampling scheme. We assessed microbial communities via phospholipid fatty acid (PLFA) analyses and PCR-denaturing gradient gel electrophoresis (DGGE) and measured soil characteristics, as well as nematode and plant community composition. The relative influences of space, soil, vegetation and nematodes on soil microorganisms were contrasted using variation partitioning and path analysis. Results indicate that soil characteristics and plant community composition, representing habitat and resources, shape soil microbial community composition, whereas the influence of nematodes, a potential predation factor, appears to be relatively small. Spatial variation in microbial community structure was detected at broad (between fields) and fine (within fields) scales, suggesting that microbial communities exhibit biogeographic patterns at different scales. Although our analysis included several relevant explanatory data sets, a large part of the variation in microbial communities remained unexplained (up to 92% in some analyses). However, in several analyses, significant parts of the variation in microbial community structure could be explained. The results of this study contribute to our understanding of the relative importance of different environmental and spatial factors in driving the composition of soil-borne microbial communities.
  • Journal of Agricultural and Food Chemistry

    Intra-specific differences in root and shoot glucosinolate profiles among white cabbage (Brassica oleracea var. capitata) cultivars

    Patrick Kabouw, Arjen Biere, Wim H. van der Putten, Nicole M. van Dam
    Shoot glucosinolate profiles of Brassicaceae are known to vary within species, across environmental conditions, and between developmental stages. Here we study whether root profiles follow the intra-specific, environmental, and developmental variation observed for aerial parts in white cabbage cultivars. We also assess whether greenhouse studies can be used to predict shoot and root glucosinolate concentrations and profiles in the field. Root glucosinolate profiles showed significant intra-specific variation; however, this variation was unrelated to that in shoot profiles. One of the strongest determinants of the diversity in the root profiles was 2-phenylethyl glucosinolate (gluconasturtiin). Root profiles were generally comparable between greenhouse studies and field trials, whereas shoot profiles were highly plastic. We conclude that among white cabbage cultivars, shoot glucosinolate profiles are not indicative of root profiles. We further conclude that greenhouse assessments of root glucosinolates can be reliable predictors of root glucosinolate profiles in the field due to their low plasticity.
  • Trends in Ecology & Evolution

    Impacts of soil microbial communities on exotic plant invasions

    [No Value] Inderjit, Wim H. van der Putten
    Soil communities can have profound effects on invasions of ecosystems by exotic plant species. We propose that there are three main pathways by which this can happen. First, plant–soil feedback interactions in the invaded range are neutral to positive, whereas native plants predominantly suffer from negative soil feedback effects. Second, exotic plants can manipulate local soil biota by enhancing pathogen levels or disrupting communities of root symbionts, while suffering less from this than native plants. Third, exotic plants produce allelochemicals toxic to native plants that cannot be detoxified by local soil communities, or that become more toxic following microbial conversion. We discuss the need for integrating these three pathways in order to further understand how soil communities influence exotic plant invasions.
  • New Phytologist

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

    Tess Van de Voorde, Wim H. van der Putten, H.A. Gamper, (Gera) W.H.G. Hol, T. Martijn Bezemer
    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.
  • Global Change Biology

    Plant–soil interactions in the expansion and native range of a poleward shifting plant species

    Roy H. A. van Grunsven, Wim H. van der Putten, T. Martijn Bezemer, Frank Berendse, E.M. Veenendaal
    Climate warming causes range shifts of many species toward higher latitudes and altitudes. However, range shifts of host species do not necessarily proceed at the same rates as those of their enemies and symbionts. Here, we examined how a range shifting plant species performs in soil from its original range in comparison with soil from the expansion range. Tragopogon dubius is currently expanding from southern into north-western Europe and we examined how this plant species responds to soil communities from its original and expansion ranges. We compared the performance of T. dubius with that of the closely related Tragopogon pratensis, which has a natural occurrence along the entire latitudinal gradient. Inoculation with the rhizosphere soil from T. dubius populations of the original range had a more negative effect on plant biomass production than inoculation with rhizosphere soil from the expansion range. Interestingly, the nonrange expander T. pratensis experienced a net negative soil effect throughout this entire range. The effects observed in this species pair may be due to release from soil born enemies or accumulation of beneficial soil born organisms. If this phenomenon applies broadly to other species, then range expansion may enable plants species to show enhanced performance.
  • Ecology

    Divergent composition but similar function of soil food webs beneath individual plants: plant species and community effects

    T. Martijn Bezemer, M.T. Fountain, J.M. Barea, S. Christensen, S.C. Dekker, Henk Duyts, R. van Hal, Jeff A. Harvey, K. Hedlund, M. Maraun, J. Mikola, A.G. Mladenov, Catherine Robin, P.C. de Ruiter, S. Scheu, H. Setälä, P. Milauer, Wim H. van der Putten
    Soils are extremely rich in biodiversity, and soil organisms play pivotal roles in supporting terrestrial life, but the role that individual plants and plant communities play in influencing the diversity and functioning of soil food webs remains highly debated. Plants, as primary producers and providers of resources to the soil food web, are of vital importance for the composition, structure, and functioning of soil communities. However, whether natural soil food webs that are completely open to immigration and emigration differ underneath individual plants remains unknown. In a biodiversity restoration experiment we first compared the soil nematode communities of 228 individual plants belonging to eight herbaceous species. We included grass, leguminous, and non-leguminous species. Each individual plant grew intermingled with other species, but all plant species had a different nematode community. Moreover, nematode communities were more similar when plant individuals were growing in the same as compared to different plant communities, and these effects were most apparent for the groups of bacterivorous, carnivorous, and omnivorous nematodes. Subsequently, we analyzed the composition, structure, and functioning of the complete soil food webs of 58 individual plants, belonging to two of the plant species, Lotus corniculatus (Fabaceae) and Plantago lanceolata (Plantaginaceae). We isolated and identified more than 150 taxa/groups of soil organisms. The soil community composition and structure of the entire food webs were influenced both by the species identity of the plant individual and the surrounding plant community. Unexpectedly, plant identity had the strongest effects on decomposing soil organisms, widely believed to be generalist feeders. In contrast, quantitative food web modeling showed that the composition of the plant community influenced nitrogen mineralization under individual plants, but that plant species identity did not affect nitrogen or carbon mineralization or food web stability. Hence, the composition and structure of entire soil food webs vary at the scale of individual plants and are strongly influenced by the species identity of the plant. However, the ecosystem functions these food webs provide are determined by the identity of the entire plant community.
  • Philosophical Transactions of the Royal Society B: Biological Sciences

    Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels

    Current predictions on species responses to climate change strongly rely on projecting altered environmental conditions on species distributions. However, it is increasingly acknowledged that climate change also influences species interactions. We review and synthesize literature information on biotic interactions and use it to argue that the abundance of species and the direction of selection during climate change vary depending on how their trophic interactions become disrupted. Plant abundance can be controlled by aboveground and belowground multitrophic level interactions with herbivores, pathogens, symbionts and their enemies. We discuss how these interactions may alter during climate change and the resulting species range shifts. We suggest conceptual analogies between species responses to climate warming and exotic species introduced in new ranges. There are also important differences: the herbivores, pathogens and mutualistic symbionts of range-expanding species and their enemies may co-migrate, and the continuous gene flow under climate warming can make adaptation in the expansion zone of range expanders different from that of cross-continental exotic species. We conclude that under climate change, results of altered species interactions may vary, ranging from species becoming rare to disproportionately abundant. Taking these possibilities into account will provide a new perspective on predicting species distribution under climate change.
  • Biological Invasions

    Ecological fits, mis-fits and lotteries involving insect herbivores on the invasive plant, Bunias orientalis

    Jeff A. Harvey, Arjen Biere, Taiadjana Fortuna, Louise E.M. Vet, T. Engelkes, Elly Morrien, R. Gols, Koen Verhoeven, H. Vogel, Mirka Macel, H. Heidel-Fischer, K. Schramm, Wim H. van der Putten
    Exotic plants bring with them traits that evolved elsewhere into their new ranges. These traits may make them unattractive or even toxic to native herbivores, or vice versa. Here, interactions between two species of specialist (Pieris rapae and P. brassicae) and two species of generalist (Spodoptera exigua and Mamestra brassicae) insect herbivores were examined on two native crucifer species in the Netherlands, Brassica nigra and Sinapis arvensis, and an exotic, Bunias orientalis. Bu. orientalis originates in eastern Europe and western Asia but is now an invasive pest in many countries in central Europe. P. rapae, P. brassicae and S. exigua performed very poorly on Bu. orientalis, with close to 100% of larvae failing to pupate, whereas survival was much higher on the native plants. In choice experiments, the pierid butterflies preferred to oviposit on the native plants. Alternatively, M. brassicae developed very poorly on the native plants but thrived on Bu. orientalis. Further assays with a German Bu. orientalis population also showed that several specialist and generalist herbivores performed very poorly on this plant, with the exception of Spodoptera littoralis and M. brassicae. Bu. orientalis produced higher levels of secondary plant compounds (glucosinolates) than B. nigra but not S. arvensis but these do not appear to be important factors for herbivore development. Our results suggest that Bu. orientalis is a potential demographic ‘trap’ for some herbivores, such as pierid butterflies. However, through the effects of an evolutionary ‘lottery’, M. brassicae has found its way through the plant’s chemical ‘minefield’.
  • Oecologia

    Plant-soil feedback of native and range-expanding plant species is insensitive to temperature

    Roy H. A. van Grunsven, Wim H. van der Putten, T. Martijn Bezemer, E.M. Veenendaal
    Temperature change affects many aboveground and belowground ecosystem processes. Here we investigate the effect of a 5°C temperature increase on plant–soil feedback. We compare plant species from a temperate climate region with immigrant plants that originate from warmer regions and have recently shifted their range polewards. We tested whether the magnitude of plant–soil feedback is affected by ambient temperature and whether the effect of temperature differs between these groups of plant species. Six European/Eurasian plant species that recently colonized the Netherlands (non-natives), and six related species (natives) from the Netherlands were selected. Plant–soil feedback of these species was determined by comparing performance in conspecific and heterospecific soils. In order to test the effect of temperature on these plant–soil feedback interactions, the experiments were performed at two greenhouse temperatures of 20/15°C and 25/20°C, respectively. Inoculation with unconditioned soil had the same effect on natives and non-natives. However, the effect of conspecific conditioned soil was negative compared to heterospecific soil for natives, but was positive for non-natives. In both cases, plant–soil interactions were not affected by temperature. Therefore, we conclude that the temperature component of climate change does not affect the direction, or strength of plant–soil feedback, neither for native nor for non-native plant species. However, as the non-natives have a more positive soil feedback than natives, climate warming may introduce new plant species in temperate regions that have less soil-borne control of abundance.
  • Ecological Entomology

    Behaviour of male and female parasitoids in the field: influence of patch size, host density and habitat complexity

    T. Martijn Bezemer, Jeff A. Harvey, A.F.D. Kamp, Roel Wagenaar, R. Gols, Olga Kostenko, Taiadjana Fortuna, T. Engelkes, Louise E.M. Vet, Wim H. van der Putten, Roxina Soler
    1. Two field experiments were carried out to examine the role of patch size, host density, and complexity of the surrounding habitat, on the foraging behaviour of the parasitoid wasp Cotesia glomerata in the field. 2. First, released parasitoids were recaptured on patches of one or four Brassica nigra plants, each containing 10 hosts that were placed in a mown grassland area. Recaptures of females were higher than males, and males and females aggregated at patches with four plants. 3. In experiment 2, plants containing 0, 5 or 10 hosts were placed in unmown grassland plots that differed in plant species composition, on bare soil, and on mown grassland. Very low numbers of parasitoids were recaptured in the vegetated plots, while high numbers of parasitoids were recaptured on plants placed on bare soil or in mown grassland. Recaptures were higher on plants on bare soil than on mown grassland, and highest on plants containing 10 hosts. The host density effect was significantly more apparent in mown grassland than on bare soil. 4. Cotesia glomerata responds in an aggregative way to host density in the field. However, host location success is determined mostly by habitat characteristics, and stronger host or host-plant cues are required when habitat complexity increases.
  • New Phytologist

    Virulence of soil-borne pathogens and invasion by Prunus serotina

    K.O. Reinhart, T.O.G. Tytgat, Wim H. van der Putten, Keith Clay
    Globally, exotic invaders threaten biodiversity and ecosystem function. Studies often report that invading plants are less affected by enemies in their invaded vs home ranges, but few studies have investigated the underlying mechanisms. Here, we investigated the variation in prevalence, species composition and virulence of soil-borne Pythium pathogens associated with the tree Prunus serotina in its native US and non-native European ranges by culturing, DNA sequencing and controlled pathogenicity trials. Two controlled pathogenicity experiments showed that Pythium pathogens from the native range caused 38 462% more root rot and 80 583% more seedling mortality, and 19 45% less biomass production than Pythium from the non-native range. DNA sequencing indicated that the most virulent Pythium taxa were sampled only from the native range. The greater virulence of Pythium sampled from the native range therefore corresponded to shifts in species composition across ranges rather than variation within a common Pythium species. Prunus serotina still encounters Pythium in its non-native range but encounters less virulent taxa. Elucidating patterns of enemy virulence in native and nonnative ranges adds to our understanding of how invasive plants escape disease. Moreover, this strategy may identify resident enemies in the non-native range that could be used to manage invasive plants.
  • Plant and Soil

    Microorganisms and nematodes increase levels of secondary metabolites in roots and root exudates of Plantago lanceolata

    S. Wurst, Roel Wagenaar, Arjen Biere, Wim H. van der Putten
    Plant secondary metabolites play an important role in constitutive and inducible direct defense of plants against their natural enemies. While induction of defense by aboveground pathogens and herbivores is well-studied, induction by belowground organisms is less explored. Here, we examine whether soil microorganisms and nematodes can induce changes in levels of the secondary metabolites aucubin and catalpol (iridoid glycosides, IG) in roots and root exudates of two full-sib families of Plantago lanceolata originating from lines selected for low and high constitutive levels of IG in leaves. Addition of soil microorganisms enhanced the shoot and root biomass, and the concentration of aucubin in roots of both Plantago lines without affecting IG levels in the rhizosphere. By contrast, nematode addition tended to reduce the root biomass and enhanced the stalk biomass, and increased the levels of aucubin and catalpol in root exudates of both Plantago lines, without affecting root IG concentrations. The Plantago lines did not differ in constitutive levels of aucubin and total IG in roots, while the concentration of catalpol was slightly higher in roots of plants originally selected for low constitutive levels of IG in leaves. Root exudates of “high IG line” plants contained significantly higher levels of aucubin, which might be explained by their higher root biomass. We conclude that soil microorganisms can induce an increase of aucubin concentrations in the roots, whereas nematodes (probably plant feeders) lead to an enhancement of aucubin and catalpol levels in root exudates of P. lanceolata. A potential involvement of secondary metabolites in belowground interactions between plants and soil organisms is discussed.
  • Ecology

    Vertebrate herbivores influence soil nematodes by modifying plant communities

    Ciska Veen, H. Olff, Henk Duyts, Wim H. van der Putten
    Abiotic soil properties, plant community composition, and herbivory all have been reported as important factors influencing the composition of soil communities. However, most studies thus far have considered these factors in isolation, whereas they strongly interact in the field. Here, we study how grazing by vertebrate herbivores influences the soil nematode community composition of a floodplain grassland while we account for effects of grazing on plant community composition and abiotic soil properties. Nematodes are the most ubiquitous invertebrates in the soil. They include a variety of feeding types, ranging from microbial feeders to herbivores and carnivores, and they perform key functions in soil food webs. Our hypothesis was that grazing affects nematode community structure and composition through altering plant community structure and composition. Alternatively, we tested whether the effects of grazing may, directly or indirectly, run via changes in soil abiotic properties. We used a long-term field experiment containing plots with and without vertebrate grazers (cattle and rabbits). We compared plant and nematode community structure and composition, as well as a number of key soil abiotic properties, and we applied structural equation modeling to investigate four possible pathways by which grazing may change nematode community composition. Aboveground grazing increased plant species richness and reduced both plant and nematode community heterogeneity. There was a positive relationship between plant and nematode diversity indices. Grazing decreased the number of bacterial-feeding nematodes, indicating that in these grasslands, top-down control of plant production by grazing leads to bottom-up control in the basal part of the bacterial channel of the soil food web. According to the structural equation model, grazing had a strong effect on soil abiotic properties and plant community composition, whereas plant community composition was the main determinant of nematode community composition. Other pathways, which assumed that grazing influenced nematode community composition by inducing changes in soil abiotic properties, did not significantly explain variation in nematode community composition. We conclude that grazing-induced changes in nematode community composition mainly operated via changes in plant community composition. Influences of vertebrate grazers on soil nematodes through modification of abiotic soil properties were of less importance.
  • 2010

    European atlas of soil biodiversity

    S. Jeffery, C. Gardi, A. Jones, L. Montanarella, L. Marmo, L. Miko, K. Ritz, G. Peres, J. Rombke, Wim H. van der Putten
  • Oecologia

    Chemical defense, mycorrhizal colonization and growth responses in Plantago lanceolata L.

    Gerlinde De Deyn, Arjen Biere, Wim H. van der Putten, Roel Wagenaar, J.N. Klironomos
    Allelochemicals defend plants against herbivore and pathogen attack aboveground and belowground. Whether such plant defenses incur ecological costs by reducing benefits from plant mutualistic symbionts is largely unknown. We explored a potential trade-off between inherent plant chemical defense and belowground mutualism with arbuscular mycorrhizal fungi (AMF) in Plantago lanceolata L., using plant genotypes from lines selected for low and high constitutive levels of the iridoid glycosides (IG) aucubin and catalpol. As selection was based on IG concentrations in leaves, we first examined whether IG concentrations covaried in roots. Root and leaf IG concentrations were strongly positively correlated among genotypes, indicating genetic interdependence of leaf and root defense. We then found that root AMF arbuscule colonization was negatively correlated with root aucubin concentration. This negative correlation was observed both in plants grown with monocultures of Glomus intraradices and in plants colonized from whole-field soil inoculum. Overall, AMF did not affect total biomass of plants; an enhancement of initial shoot biomass was offset by a lower root biomass and reduced regrowth after defoliation. Although the precise effects of AMF on plant biomass varied among genotypes, plants with high IG levels and low AMF arbuscule colonization in roots did not produce less biomass than plants with low IG and high AMF arbuscule colonization. Therefore, although an apparent trade-off was observed between high root chemical defense and AMF arbuscule colonization, this did not negatively affect the growth responses of the plants to AMF. Interestingly, AMF induced an increase in root aucubin concentration in the high root IG genotype of P. lanceolata. We conclude that AMF does not necessarily stimulate plant growth, that direct plant defense by secondary metabolites does not necessarily reduce potential benefits from AMF, and that AMF can enhance concentrations of root chemical defenses, but that these responses are plant genotype-dependent.
  • Ecology Letters

    Plant invaders and their novel natural enemies: who is naive?

    Koen Verhoeven, Arjen Biere, Jeff A. Harvey, Wim H. van der Putten
    Introduced exotic species encounter a wide range of non-coevolved enemies and competitors in their new range. Evolutionary novelty is a key aspect of these interactions, but who benefits from novelty: the exotic species or their new antagonists? Paradoxically, the novelty argument has been used to explain both the release from and the suppression by natural enemies. We argue that this paradox can be solved by considering underlying interaction mechanisms. Using plant defenses as a model, we argue that mismatches between plant and enemy interaction traits can enhance plant invasiveness in the case of toxin-based defenses, whereas invasiveness is counteracted by mismatches in recognition-based defenses and selective foraging of generalist herbivores on plants with rare toxins. We propose that a mechanistic understanding of ecological mismatches can help to explain and predict when evolutionary novelty will enhance or suppress exotic plant invasiveness. This knowledge may also enhance our understanding of plant abundance following range expansion, or during species replacements along successional stages.
  • Ecological Modelling

    The power of simulating experiments

    Katrin Meyer, Wolf M. Mooij, Matthijs Vos, (Gera) W.H.G. Hol, Wim H. van der Putten
    Addressing complex ecological research questions often requires complex empirical experiments. However, due to the logistic constraints of empirical studies there is a trade-off between the complexity of experimental designs and sample size. Here, we explore if the simulation of complex ecological experiments including stochasticity-induced variation can aid in alleviating the sample size limitation of empirical studies. One area where sample size limitations constrain empirical approaches is in studies of the above- and belowground controls of trophic structure. Based on a rule- and individual-based simulation model on the effect of above- and belowground herbivores and their enemies on plant biomass, we evaluate the reliability of biomass estimates, the probability of experimental failure in terms of missing values, and the statistical power of biomass comparisons for a range of sample sizes. As expected, we observed superior performance of setups with sample sizes typical of simulations (n = 1000) as compared to empirical experiments (n = 10). At low sample sizes, simulated standard errors were smaller than expected from statistical theory, indicating that stochastic simulation models may be required in those cases where it is not possible to perform pilot studies for determining sample sizes. To avoid experimental failure, a sample size of n = 30 was required. In conclusion, we propose that the standard tool box of any ecologist should comprise a combination of simulation and empirical approaches to benefit from the realism of empirical experiments as well as the statistical power of simulations.
  • Journal of Ecology

    A multitrophic perspective on functioning and evolution of facilitation in plant communities

    1. Plant facilitation has been studied mostly in the context of plant–plant interactions, whereas multitrophic interactions including those that occur below ground have not yet received much attention. Here, I will discuss how above-ground and below-ground natural enemies and their predators influence plant facilitation and its evolution. 2. Specific above-ground and below-ground plant enemies and their predators play a major role in structuring the composition and dynamics of plant communities. In successional sequences, above-ground and below-ground multitrophic level interactions may tip the balance from competitive to facilitative states and vice versa. 3. Little is known about how above-ground and below-ground multitrophic interactions develop along resource or stress gradients and how the outcomes of above-ground–below-ground interactions depend on variations in these environmental conditions. 4. Facilitated plants need to fit into the above-ground–below-ground multitrophic communities of their facilitators. 5. Little is known also about the evolution of plant facilitation. The observed distance in phylogeny between facilitators and facilitated plants suggests that host-specific enemies may very well co-determine which species become facilitated by which facilitators. 6. Further, very little attention has been given to how plant strategies (allelopathy, accumulation of enemies, monopolization of symbionts) may be the result of selection against being facilitative. 7. Synthesis. Plant facilitation cannot be understood without considering a plant's natural enemies and also its enemies' enemies. Plant enemies can turn competitive interactions into facilitative interactions, whereas the enemies' enemies can turn facilitation back into competition. Below-ground interactions will have longer-lasting effects on facilitation than those above ground, because many organisms can persist in the soil, even when the host plants have disappeared.
  • Ecological Entomology

    Influence of presence and spatial arrangement of belowground insects on host-plant selection of aboveground insects: a field study

    J.J. Soler, Sonja Schaper, T. Martijn Bezemer, A.M. Cortesero, T.S. Hoffmeister, Wim H. van der Putten, Louise E.M. Vet, Jeff A. Harvey
    1. Several studies have shown that above- and belowground insects can interact by influencing each others growth, development, and survival when they feed on the same host-plant. In natural systems, however, insects can make choices on which plants to oviposit and feed. A field experiment was carried out to determine if root-feeding insects can influence feeding and oviposition preferences and decisions of naturally colonising foliar-feeding insects. 2. Using the wild cruciferous plant Brassica nigra and larvae of the cabbage root fly Delia radicum as the belowground root-feeding insect, naturally colonising populations of foliar-feeding insects were monitored over the course of a summer season. 3. Groups of root-infested and root-uninfested B. nigra plants were placed in a meadow during June, July, and August of 2006 for periods of 3 days. The root-infested and the root-uninfested plants were either dispersed evenly or placed in clusters. Once daily, all leaves of each plant were carefully inspected and insects were removed and collected for identification. 4. The flea beetles Phyllotreta spp. and the aphid Brevicoryne brassicae were significantly more abundant on root-uninfested (control) than on root-infested plants. However, for B. brassicae this was only apparent when the plants were placed in clusters. Host-plant selection by the generalist aphid M. persicae and oviposition preference by the specialist butterfly P. rapae, however, were not significantly influenced by root herbivory. 5. The results of this study show that the presence of root-feeding insects can affect feeding and oviposition preferences of foliar-feeding insects, even under natural conditions where many other interactions occur simultaneously. The results suggest that root-feeding insects play a role in the structuring of aboveground communities of insects, but these effects depend on the insect species as well as on the spatial distribution of the root-feeding insects.
  • Basic and Applied Ecology

    Can root-feeders alter the composition of AMF communities? Experimental evidence from the dune grass Ammophila arenaria

    S. Rodríguez-Echeverría, E. De la Peña, M. Moens, H. Freitas, Wim H. van der Putten
    Root herbivores and plant mutualists, such as arbuscular mycorrhizal fungi (AMF), have a significant effect on the structure and dynamic of plant communities. Nevertheless, the interactions between the two groups of organisms in natural ecosystems are far from understood. We carried out an inoculation experiment to examine the effect of two root herbivores, Pratylenchus penetrans and P. dunensis (Nematoda), on the composition of the AMF communities associated with two populations of the dune grass Ammophila arenaria. The outcome of the interaction in terms of plant and nematode performance was also analyzed. The total percentage of AMF colonization was not affected by the presence of root-feeders, but they did alter the composition of the AMF communities inside the roots. These changes were dependent on the root-feeder species and the original AMF community: the most severe alterations were observed in the mycorrhizal plants from Wales attacked by P. penetrans. Plant growth was impaired in plants from Wales inoculated with AMF and P. dunensis, which suggests a highly species-specific synergistic interaction with negative consequences for the plant. Root infection by the nematodes was reduced in all mycorrhizal plants when compared to non-mycorrhizal plants. However, a significant reduction of the final number of nematodes was observed only in the mycorrhizal plants from one population.
  • Restoration Ecology

    Soil organism and plant introductions in restoration of species-rich grassland communities

    Paul Kardol, T. Martijn Bezemer, Wim H. van der Putten
    Soil organisms can strongly affect competitive interactions and successional replacements of grassland plant species. However, introduction of whole soil communities as management strategy in grassland restoration has received little experimental testing. In a 5-year field experiment at a topsoil-removed ex-arable site (receptor site), we tested effects of (1) spreading hay and soil, independently or combined, and (2) transplanting intact turfs on plant and soil nematode community development. Material for the treatments was obtained from later successional, species-rich grassland (donor site). Spreading hay affected plant community composition, whereas spreading soil did not have additional effects. Plant species composition of transplanted turfs became less similar to that in the donor site. Moreover, most plants did not expand into the receiving plots. Soil spreading and turf transplantation did not affect soil nematode community composition. Unfavorable soil conditions (e.g., low organic matter content and seasonal fluctuations in water level) at the receptor site may have limited plant and nematode survival in the turfs and may have precluded successful establishment outside the turfs. We conclude that introduction of later successional soil organisms into a topsoil-removed soil did not facilitate the establishment of later successional plants, probably because of the "mismatch" in abiotic soil conditions between the donor and the receptor site. Further research should focus on the required conditions for establishment of soil organisms at restoration sites in order to make use of their contribution to grassland restoration. We propose that introduction of organisms from "intermediate" stages will be more effective as management strategy than introduction of organisms from "target" stages.
  • Functional Ecology

    Soil microorganisms in coastal foredunes control the ectoparasitic root-feeding nematode Tylenchorhynchus ventralis by local interactions

    A.M. Piśkiewicz, Henk Duyts, Wim H. van der Putten
    1. In natural grassland ecosystems, root-feeding nematodes and insects are the dominant below-ground herbivores. In coastal foredunes, the ectoparasitic nematode Tylenchorhynchus ventralis would be a major root herbivore if not strongly controlled by soil microorganisms. Here, we examined if the suppressive effects of the microbial enemies of T. ventralis act by local interactions such as predation, parasitism or antagonism, or local induction of plant defence, or by non-local interactions, such as systemic effects when microorganisms in one section of the plant roots can affect nematode control in another section of the root system. We show that abundance of T. ventralis in the root zone of the grass Ammophila arenaria is suppressed by local interactions. 2. We compared local vs. non-local control of nematodes by a natural community of soil microorganisms in a split-root experiment, where nematodes and microbes were inoculated to the same, or to opposite root compartments. 3. The split-root experiment revealed that microorganisms affected T. ventralis numbers only when present in the same root compartment. Therefore, the effects of microorganisms on T. ventralis are due to local interactions and not due to induction of a systemic defence mechanism in the plant host. 4. When inoculated together with microorganisms, the nematodes were heavily infected with unknown bacteria and with fungi that resembled the genus Catenaria, suggesting that microorganisms control nematodes through parasitism. However, local defence induction cannot be completely excluded. 5. Besides microbial enemies of nematodes, the root zone of A. arenaria also contains plant pathogens. Root biomass was reduced by nematode infection, but also by the combination of nematodes and microorganisms, most likely because the soil pathogens overwhelmed the effects of nematode control on plant production. 6. We conclude that there may be a trade-off between beneficial effects of soil microorganisms on the plant host due to nematode control vs. pathogenic effects of soil microorganisms on the plant host. We propose that such trade-offs require more attention when studying below-ground multitrophic interactions.
  • Acta Oecologica

    Contrasting diversity patterns of soil mites and nematodes in secondary succession

    Paul Kardol, J.S. Newton, T. Martijn Bezemer, M. Maraun, Wim H. van der Putten
    Soil biodiversity has been recognized as a key feature of ecosystem functioning and stability. However, soil biodiversity is strongly impaired by agriculture and relatively little is known on how and at what spatial and temporal scales soil biodiversity is restored after the human disturbances have come to an end. Here, a multi-scale approach was used to compare diversity patterns of soil mites and nematodes at four stages (early, mid, late, reference site) along a secondary succession chronosequence from abandoned arable land to heath land. In each field four soil samples were taken during four successive seasons. We determined soil diversity within samples (α-diversity), between samples (β-diversity) and within field sites (γ-diversity). The patterns of α- and γ-diversity developed similarly along the chronosequence for oribatid mites, but not for nematodes. Nematode α-diversity was highest in mid- and late-successional sites, while γ-diversity was constant along the chronosequence. Oribatid mite β-diversity was initially high, but decreased thereafter, whereas nematode β-diversity increased when succession proceeded; indicating that patterns of within-site heterogeneity diverged for oribatid mites and nematodes. The spatio-temporal diversity patterns after land abandonment suggest that oribatid mite community development depends predominantly on colonization of new taxa, whereas nematode community development depends on shifts in dominance patterns. This would imply that at old fields diversity patterns of oribatid mites are mainly controlled by dispersal, whereas diversity patterns of nematodes are mainly controlled by changing abiotic or biotic soil conditions. Our study shows that the restoration of soil biodiversity along secondary successional gradients can be both scale- and phylum-dependent.
  • Oikos

    Quantifying the impact of above- and belowground higher trophic levels on plant and herbivore performance by modeling

    Katrin Meyer, Matthijs Vos, Wolf M. Mooij, (Gera) W.H.G. Hol, Aad J Termorshuizen, Louise E.M. Vet, Wim H. van der Putten
    Growing empirical evidence suggests that aboveground and belowground multitrophic communities interact. However, investigations that comprehensively explore the impacts of above- and belowground third and higher trophic level organisms on plant and herbivore performance are thus far lacking. We tested the hypotheses that above- and belowground higher trophic level organisms as well as decomposers affect plant and herbivore performance and that these effects cross the soil–surface boundary. We used a well-validated simulation model that is individual-based for aboveground trophic levels such as shoot herbivores, parasitoids, and hyperparasitoids while considering belowground herbivores and their antagonists at the population level. We simulated greenhouse experiments by removing trophic levels and decomposers from the simulations in a factorial design. Decomposers and above- and belowground third trophic levels affected plant and herbivore mortality, root biomass, and to a lesser extent shoot biomass. We also tested the effect of gradual modifications of the interactions between different trophic level organisms with a sensitivity analysis. Shoot and root biomass were highly sensitive to the impact of the fourth trophic level. We found effects that cross the soil surface, such as aboveground herbivores and parasitoids affecting root biomass and belowground herbivores influencing aboveground herbivore mortality. We conclude that higher trophic level organisms and decomposers can strongly influence plant and herbivore performance. We propose that our modelling framework can be used in future applications to quantitatively explore the possible outcomes of complex above- and belowground multitrophic interactions under a range of environmental conditions and species compositions.
  • Journal of Ecology

    Plant–soil feedback induces shifts in biomass allocation in the invasive plant Chromolaena odorata

    M. te Beest, N. Stevens, H. Olff, Wim H. van der Putten
    1. Soil communities and their interactions with plants may play a major role in determining the success of invasive species. However, rigorous investigations of this idea using cross-continental comparisons, including native and invasive plant populations, are still scarce. 2. We investigated if interactions with the soil community affect the growth and biomass allocation of the (sub)tropical invasive shrub Chromolaena odorata. We performed a cross-continental comparison with both native and non-native-range soil and native and non-native-range plant populations in two glasshouse experiments. 3. Results are interpreted in the light of three prominent hypotheses that explain the dominance of invasive plants in the non-native range: the enemy release hypothesis, the evolution of increased competitive ability hypothesis and the accumulation of local pathogens hypothesis. 4. Our results show that C. odorata performed significantly better when grown in soil pre-cultured by a plant species other than C. odorata. Soil communities from the native and non-native ranges did not differ in their effect on C. odorata performance. However, soil origin had a significant effect on plant allocation responses. 5. Non-native C. odorata plants increased relative allocation to stem biomass and height growth when confronted with soil communities from the non-native range. This is a plastic response that may allow species to be more successful when competing for light. This response differed between native and non-native-range populations, suggesting that selection may have taken place during the process of invasion. Whether this plastic response to soil organisms will indeed select for increased competiti 6. The native grass Panicum maximum did not perform worse when grown in soil pre-cultured by C. odorata. Therefore, our results did not support the accumulation of local pathogens hypothesis. 7. Synthesis. Non-native C. odorata did not show release from soil-borne enemies compared to its native range. However, non-native plants responded to soil biota from the non-native range by enhanced allocation in stem biomass and height growth. This response can affect the competitive balance between native and invasive species. The evolutionary potential of this soil biota-induced change in plant biomass allocation needs further study.
  • Functional Ecology

    Plant defence against nematodes is not mediated by changes in the soil microbial community

    S. Wurst, S. Van Beersum, Roel Wagenaar, Tanja Bakx-Schotman, Barbara Drigo, I. Janzik, A. Lanoue, Wim H. van der Putten
    1. Indirect plant defence, the recruitment of antagonists of herbivores, is well-known above the ground. In spite of various soil microorganisms acting as antagonists to root herbivores, it is still largely unknown whether plants can promote antagonistic microorganisms as an indirect defence mechanism. 2. In a greenhouse study we examined whether soil microorganisms could mediate plant defence against plant-feeding nematodes. Growth, nutrient contents and root exudation of three plant species (Plantago lanceolata, Holcus lanatus, Lotus corniculatus) and the performance of nematodes and fungal communities in the rhizospheres were measured. 3. The plant species differed in their effects on plant-feeding nematodes; however, the addition of soil microorganisms did not enhance nematode control. Nematode addition changed root exudation patterns and rhizosphere fungal community structure in a plant species-specific manner. Glucose levels in the root exudates of all three examined plant species were enhanced, and P. lanceolata root exudates contained higher levels of fumaric acid when nematodes had been added. 4. We conclude that nematodes have plant species-specific effects on root exudate chemistry and rhizosphere fungal community composition, but these effects do not necessarily enhance indirect control of nematodes by antagonistic microorganisms. More studies on below-ground plant defence are definitely needed.
  • Plant and Soil

    Plant ectoparasitic nematodes prefer roots without their microbial enemies

    A.M. Piśkiewicz, M.J.K. de Milliano, Henk Duyts, Wim H. van der Putten
    Root-feeding nematodes are major soil-borne pests in agriculture. In natural ecosystems, their abundance can be strongly controlled by natural enemies. In coastal foredune soil, the abundance of the ectoparasitic nematode Tylenchorhynchus ventralis is controlled by local interactions with soil microorganisms. If not controlled, T. ventralis reduces growth and performance of the host plant Ammophila arenaria. In the present study, we examine if the nematodes may sense the presence of soil microorganisms and, if so, they are able to actively avoid their enemies. First, using Petri dishes with agar medium we examined if T. ventralis can choose between A. arenaria seedlings inoculated with or without soil microorganisms. We observed that there was a trend (although non-significant) in nematode migration towards the non-inoculated plants. If the seedlings were not present, the nematodes did not make any choice and stayed in the centre of the Petri dish. Then, using Y-tubes filled with sterilized dune soil, we examined if T. ventralis could choose between A. arenaria roots with or without microorganisms. We also included treatments of microbial suspensions without plants and a microbe-free filtrate. We observed that the nematodes preferred roots without microorganisms. Microorganisms alone or roots with microbial filtrate did not influence nematode choice significantly. We conclude that the nematode T. ventralis is able to choose roots without soil microorganisms when having roots with them as alternative. Such avoidance could explain why biological control of nematodes in field is not always effective, especially when microbial antagonists accumulate in specific parts of the rhizosphere.
  • Soil Biology & Biochemistry

    Local variation in belowground multitrophic interactions

    A growing number of studies point at the involvement of root herbivores in influencing plant performance, community composition and succession. However, little is known about the factors that control root herbivore abundance and the role of local variation in the effectiveness of these factors. Here, we performed a full factorial experiment with plants, root-feeding nematodes and rhizosphere microbial communities from two dune sites, to test the hypothesis that the outcome of belowground multitrophic interactions depends on local differences between the interacting organisms. The organisms included the marram grass Ammophila arenaria, the cyst nematode Heterodera arenaria, microbial plant pathogens and natural enemies of the nematodes from two coastal foredune systems, one in The Netherlands and one in Wales. The two plant populations differed at the molecular and phenotypic level, and the microbial communities from the two dune sites differed in the composition of the dominant soil fungi but not of the dominant bacteria. Plants were negatively affected by the rhizosphere microorganisms from one of the sites. Nevertheless, nematode performance was not affected by the origin of both the host plants and the microbial communities. The reproductive output of the cyst nematode depended on the presence of microorganisms, as well as on inter-population variability in the response of the nematode to these natural enemies. In the absence of microorganisms, the two nematode populations differed in the number and size of the produced cysts, although maternal effects cannot be excluded. Inter-population differences in the host plant were a secondary factor in the nematode–microorganisms interactions, and did not influence bottom–up control of the cyst nematodes. Our results did not reveal strong signals of coevolution in belowground multitrophic interactions of plants, cyst nematodes and soil microbial communities. We conclude that the interactions between the studied organisms do not necessarily depend on their local vs. non-local origin. Nevertheless, we were able to show that local variation in soil organism community composition can be an important factor in determining the outcome of interactions in belowground multitrophic systems.
  • Metabolomics

    Metabolic analysis of the interaction between plants and herbivores

    J.M. Jansen, J.W. Allwood, E. Marsden-Edwards, Wim H. van der Putten, R. Goodacre, Nicole M. van Dam
    Insect herbivores by necessity have to deal with a large arsenal of plant defence metabolites. The levels of defence compounds may be increased by insect damage. These induced plant responses may also affect the metabolism and performance of successive insect herbivores. As the chemical nature of induced responses is largely unknown, global metabolomic analyses are a valuable tool to gain more insight into the metabolites possibly involved in such interactions. This study analyzed the interaction between feral cabbage (Brassica oleracea) and small cabbage white caterpillars (Pieris rapae) and how previous attacks to the plant affect the caterpillar metabolism. Because plants may be induced by shoot and root herbivory, we compared shoot and root induction by treating the plants on either plant part with jasmonic acid. Extracts of the plants and the caterpillars were chemically analysed using Ultra Performance Liquid Chromatography/Time of Flight Mass Spectrometry (UPLCT/MS). The study revealed that the levels of three structurally related coumaroylquinic acids were elevated in plants treated on the shoot. The levels of these compounds in plants and caterpillars were highly correlated: these compounds were defined as the ‘metabolic interface’. The role of these metabolites could only be discovered using simultaneous analysis of the plant and caterpillar metabolomes. We conclude that a metabolomics approach is useful in discovering unexpected bioactive compounds involved in ecological interactions between plants and their herbivores and higher trophic levels.
  • 2009

    The role of nematodes in ecosystems

    G.W. Yeates, H. Ferris, T. Moens, Wim H. van der Putten
  • 2009

    Microbial biodiversity and ecosystem functioning under controlled conditions and in the wild

    T. Bell, M.O. Gessner, R.I. Griffiths, J.R. McLaren, P.J. Morin, Marcel G. A. van der Heijden, Wim H. van der Putten
  • Science Magazine

    No Paradox for Invasive Plants

    Annelein Meisner, Wietse de Boer, (Gera) W.H.G. Hol, J.A. Krumins, Wim H. van der Putten
  • Oecologia

    Empirical and theoretical challenges in aboveground–belowground ecology

    Wim H. van der Putten, Richard D. Bardgett, P.C. de Ruiter, (Gera) W.H.G. Hol, Katrin Meyer, T. Martijn Bezemer, M.A. Bradford, S. Christensen, M.B. Eppinga, T. Fukami, L. Hemerik, J. Molofsky, M. Schädler, C. Scherber, S.Y. Strauss, Matthijs Vos, David A. Wardle
    A growing body of evidence shows that aboveground and belowground communities and processes are intrinsically linked, and that feedbacks between these subsystems have important implications for community structure and ecosystem functioning. Almost all studies on this topic have been carried out from an empirical perspective and in specific ecological settings or contexts. Belowground interactions operate at different spatial and temporal scales. Due to the relatively low mobility and high survival of organisms in the soil, plants have longer lasting legacy effects belowground than aboveground. Our current challenge is to understand how aboveground–belowground biotic interactions operate across spatial and temporal scales, and how they depend on, as well as influence, the abiotic environment. Because empirical capacities are too limited to explore all possible combinations of interactions and environmental settings, we explore where and how they can be supported by theoretical approaches to develop testable predictions and to generalise empirical results. We review four key areas where a combined aboveground–belowground approach offers perspectives for enhancing ecological understanding, namely succession, agro-ecosystems, biological invasions and global change impacts on ecosystems. In plant succession, differences in scales between aboveground and belowground biota, as well as between species interactions and ecosystem processes, have important implications for the rate and direction of community change. Aboveground as well as belowground interactions either enhance or reduce rates of plant species replacement. Moreover, the outcomes of the interactions depend on abiotic conditions and plant life history characteristics, which may vary with successional position. We exemplify where translation of the current conceptual succession models into more predictive models can help targeting empirical studies and generalising their results. Then, we discuss how understanding succession may help to enhance managing arable crops, grasslands and invasive plants, as well as provide insights into the effects of global change on community re-organisation and ecosystem processes.
  • Biological Conservation

    Restoration of species-rich grasslands on ex-arable land: Seed addition outweighs soil fertility reduction

    Paul Kardol, Annemieke van der Wal, T. Martijn Bezemer, Wietse de Boer, Henk Duyts, R. Holtkamp, Wim H. van der Putten
    A common practice in biodiversity conservation is restoration of former species-rich grassland on ex-arable land. Major constraints for grassland restoration are high soil fertility and limited dispersal ability of plant species to target sites. Usually, studies focus on soil fertility or on methods to introduce plant seeds. However, the question is whether soil fertility reduction is always necessary for getting plant species established on target sites. In a three-year field experiment with ex-arable soil with intensive farming history, we tested single and combined effects of soil fertility reduction and sowing mid-successional plant species on plant community development and soil biological properties. A controlled microcosm study was performed to test short-term effects of soil fertility reduction measures on biomass production of mid-successional species. Soil fertility was manipulated by adding carbon (wood or straw) to incorporate plant-available nutrients into organic matter, or by removing nutrients through top soil removal (TSR). The sown species established successfully and their establishment was independent of carbon amendments. TSR reduced plant biomass, and effectively suppressed arable weeds, however, created a desert-like environment, inhibiting the effectiveness of sowing mid-successional plant species. Adding straw or wood resulted in short-term reduction of plant biomass, suggesting a temporal decrease in plant-available nutrients by microbial immobilisation. Straw and wood addition had little effects on soil biological properties, whereas TSR profoundly reduced numbers of bacteria, fungal biomass and nematode abundance. In conclusion, in ex-arable soils, on a short-term sowing is more effective for grassland restoration than strategies aiming at soil fertility reduction.
  • Soil Biology & Biochemistry

    Interactions between root-feeding nematodes depend on plant species identity

    Pella Brinkman, Henk Duyts, Wim H. van der Putten
    Root-feeding nematodes play an important role in structuring the composition of natural plant communities. Little is known about the role of intra- and interspecific interactions in determining the abundance of root-feeding nematodes in natural ecosystems. We examined interactions between two ectoparasitic root-feeding nematodes on two plant species: a good host plant for both nematode species and a good host for only one of the nematodes. We tested the hypothesis that root herbivore competitiveness depends on host suitability and related the experimental results to field data. In a greenhouse, we added different densities of the nematodes Tylenchorhynchus microphasmis and Tylenchorhynchus ventralis to Ammophila arenaria (the good host for both) and Carex arenaria (a good host for T. microphasmis only). Addition of T. ventralis did not significantly affect multiplication of T. microphasmis on both plant species. In contrast, on A. arenaria, T. ventralis experienced interspecific competition. However, on C. arenaria, T. microphasmis facilitated multiplication of T. ventralis. To explain this effect, we studied systemic plant-mediated effects in a split-root experiment. Nematode addition to one root compartment did not significantly influence nematode multiplication in the other root compartment, irrespective of nematode species identity. Therefore, the observed nematode interactions were not related to induced changes in the roots. In a two-choice experiment we tested whether host suitability was related to root attractiveness. Both nematode species were attracted to seedlings of A. arenaria, but not to C. arenaria. The low multiplication of T. ventralis on C. arenaria could be related to poor attraction to the roots. However, the poor attraction of T. microphasmis cannot be related to poor host suitability. Adding T. ventralis reduced shoot biomass of A. arenaria more than T. microphasmis did, whereas for C. arenaria the effect was the reverse. The interaction of the two nematodes on A. arenaria and C. arenaria shoot biomass was insignificant. However, the effect on root biomass of A. arenaria was interactive; adding T. ventralis to plants with high inoculation densities of T. microphasmis further decreased root biomass. Adding T. microphasmis further decreased root biomass of plants inoculated with low levels of T. ventralis. Depending on host plant identity, interactions between root-feeding nematodes may lead to competition or facilitation. Our results suggest that facilitation by T. microphasmis contributes to persistence of T. ventralis on C. arenaria. Thus, the population dynamics of root-feeding nematodes is influenced both by host plant identity and the presence of other root-feeding nematodes.
  • Nature

    Successful range-expanding plants experience less above-ground and below-ground enemy impact

    T. Engelkes, Elly Morrien, Koen Verhoeven, T. Martijn Bezemer, Arjen Biere, Jeff A. Harvey, L.M. McIntyre, W.L.M. Tamis, Wim H. van der Putten
    Many species are currently moving to higher latitudes and altitudes1, 2, 3. However, little is known about the factors that influence the future performance of range-expanding species in their new habitats. Here we show that range-expanding plant species from a riverine area were better defended against shoot and root enemies than were related native plant species growing in the same area. We grew fifteen plant species with and without non-coevolved polyphagous locusts and cosmopolitan, polyphagous aphids. Contrary to our expectations, the locusts performed more poorly on the range-expanding plant species than on the congeneric native plant species, whereas the aphids showed no difference. The shoot herbivores reduced the biomass of the native plants more than they did that of the congeneric range expanders. Also, the range-expanding plants developed fewer pathogenic effects4, 5 in their root-zone soil than did the related native species. Current predictions forecast biodiversity loss due to limitations in the ability of species to adjust to climate warming conditions in their range6, 7, 8. Our results strongly suggest that the plants that shift ranges towards higher latitudes and altitudes may include potential invaders, as the successful range expanders may experience less control by above-ground or below-ground enemies than the natives.
  • Journal of Chemical Ecology

    Barbarea vulgaris glucosinolate phenotypes differentially affect performance and preference of two different species of lepidopteran herbivores

    H. Van Leur, Louise E.M. Vet, Wim H. van der Putten, Nicole M. van Dam
    The composition of secondary metabolites and the nutritional value of a plant both determine herbivore preference and performance. The genetically determined glucosinolate pattern of Barbarea vulgaris can be dominated by either glucobarbarin (BAR-type) or by gluconasturtiin (NAS-type). Because of the structural differences, these glucosinolates may have different effects on herbivores. We compared the two Barbarea chemotypes with regards to the preference and performance of two lepidopteran herbivores, using Mamestra brassicae as a generalist and Pieris rapae as a specialist. The generalist and specialist herbivores did not prefer either chemotype for oviposition. However, larvae of the generalist M. brassicae preferred to feed and performed best on NAS-type plants. On NAS-type plants, 100% of the M. brassicae larvae survived while growing exponentially, whereas on BAR-type plants, M. brassicae larvae showed little growth and a mortality of 37.5%. In contrast to M. brassicae, the larval preference and performance of the specialist P. rapae was unaffected by plant chemotype. Total levels of glucosinolates, water soluble sugars, and amino acids of B. vulgaris could not explain the poor preference and performance of M. brassicae on BAR-type plants. Our results suggest that difference in glucosinolate chemical structure is responsible for the differential effects of the B. vulgaris chemotypes on the generalist herbivore. Electronic supplementary material The online version of this article (doi:10.1007/s10886-007-9424-9) contains supplementary material, which is available to authorized users.
  • Applied Soil Ecology

    Soil food web structure during ecosystem development after land abandonment

    R. Holtkamp, Paul Kardol, Annemieke van der Wal, S.C. Dekker, Wim H. van der Putten, P.C. de Ruiter
    The re-establishment of natural species rich heathlands on abandoned agricultural land is a common land use change in North-West Europe. However, it can take several decades to re-establish natural species rich heathland vegetation. The development rate has found to depend both on soil food web composition and on soil processes. We measured the soil food web composition in three ex-arable fields abandoned 2, 9 and 22 years ago and in a heathland. To characterize food structure, we defined four trophic levels and a root, fungal and bacterial energy channel. We hypothesized that with increasing time since abandonment, i.e. field age, (1) the basic resource level biomass, i.e. soil organic matter (SOM) and roots, will increase and thereby also that of biomasses at higher trophic levels, (2a) the root energy channel biomass The results showed that biomasses at the basic resource level and at the first trophic level indeed increased with field age, but not the biomasses at higher trophic levels. It is not clear what the cause of the lack of increase in higher trophic levels was, possibly top-down or bottom-up forces played a role. The root energy channel biomass decreased and the fungal channel increased as hypothesized, but the bacterial channel biomass also increased with field age. The increase of the bacterial channel biomass contradicted the hypothesis, but agreed with the observed increase in SOM quantity and lack of decrease in SOM quality. On overall, results show that changes in belowground food webs lag behind changes of the aboveground vegetation. Such time lags may hamper secondary vegetation succession. Understanding those time lags may therefore help to develop management schemes improving land conversion processes.
  • Soil Biology & Biochemistry

    Multiple species-specific controls of root-feeding nematodes in natural soils

    A.M. Piśkiewicz, Henk Duyts, Wim H. van der Putten
    One of the major limitations to enhance sustainability of crop production systems is the inability to control root-feeding nematodes without using chemical biocides. In soils under wild vegetation, however, root-feeding nematodes affect plant performance and plant community composition varying from substantially to insignificantly. Previous studies in natural ecosystems have already shown that mutualistic symbionts, such as arbuscular mycorrhizal fungi and endophytes, may influence plant exposure to root-feeding nematodes. In order to learn more from natural systems, we examined nematode control in the root zone of a wild coastal foredune grass by microorganisms, other nematodes and microarthropods. We cultured all eight root-feeding nematode species that occur in the root zone of marram grass (Ammophila arenaria) in coastal foredunes of the Netherlands. Then, in an indoor growth experiment we exposed each nematode species to the potential natural antagonists collected from the same dune soil. Most of the eight dominant root-feeding nematode species could be controlled to some extent by more than one group of soil organisms added. The effectiveness of control varied among nematode species, which seemed to be controlled in a species-specific way. We conclude that in a natural soil the effectiveness of control by microorganisms, other nematodes or microarthropods varies among root-feeding nematode species. Most are controlled, at least to some extent, by soil microbes. However, some root-feeding nematode species are controlled only by microarthropods. Our results strongly suggest that sustainable agriculture will benefit from using a range of biological control mechanisms when controlling root-feeding nematodes, rather than relying on single control agents. Our suggestion also implies that conserving soil biodiversity is crucial in order to enhance the reliability of biological crop protection against soil-borne pests and diseases.
  • Agriculture, Ecosystems and Environment

    Effects of changes in plant species richness and community traits on carabid assemblages and feeding guilds

    Jeff A. Harvey, Wim H. van der Putten, H. Turin, Roel Wagenaar, T. Martijn Bezemer
    Experiments were conducted between 2001 and 2003 in constructed plant communities that were set up in 1996 on abandoned agricultural land. The primary aim of the experiment was to study how different secondary vegetation succession scenarios influence community development of invertebrates in different trophic levels. The succession scenarios were obtained by sowing high diversity or low diversity seed mixtures of mid-successional plant species in 1996 in comparison with unsown plots where agriculture ceased in 1996 or 1999. Carnivorous carabid species generally preferred plots characterized by open vegetation, whereas herbivorous carabids generally favored plots associated with high plant diversity. However, carabid community composition was affected most by sampling year and there was also a dramatic shift over the three years in the relative proportion of the different trophic groups. Irrespective of treatment, the proportion of carnivores in the community declined with time, whereas phytophages increased over the course of the three years. By contrast, the proportion of omnivores peaked during the second year. These long-term changes were, at least to some extent, related to short-term changes in the structure and composition of the plant communities. The importance of local variation and temporal changes in plant species richness on carabids and other insect fauna are discussed.
  • Applied Soil Ecology

    Responses of root-feeding nematodes (Helicotylenchus spp.) to local and non-local populations of the host plant Ammophila arenaria

    C. Schreck Reis, H. Freitas, Wim H. van der Putten
    The root-feeding nematode community of wild plants may vary throughout their natural range. Little is known about how the variation of wild plants along their range affects their relationship with root-feeding nematodes. In the present study, we examined local and non-local combinations of host plants and root-feeding nematodes to test the hypothesis that nematode reproduction is favoured by local hosts. In two indoor experiments, we exposed populations of the wild dune grass Ammophila arenaria from northern and southern European coastal sand dunes to plant parasitic nematode species (Helicotylenchus spp.) from those same geographical origins. First, we used the southern nematode species to determine whether the effect of a local versus a non-local host may depend on nematode density. Then, in a cross-inoculation experiment we investigated how both nematode species performed with their local, as compared to the non-local hosts. In both experiments, plant biomass and ontogenetic characteristics were not significantly different between the northern and southern populations. The applied nematode densities did not have a negative impact on plant performance. This allowed us to consider the response of the two different nematode species and their host plants without co-varying differences in plant responses. Reproduction of the nematode species differed according to host origin, but contrary to what we expected, nematode sp We concluded that ectoparasitic root-feeding nematodes Helicotylenchus spp. do not necessarily perform best on their local host population of the foredune grass A. arenaria. Our results imply that the natural distribution of Helicotylenchus spp. along the European coast is determined by other factors than host populations. These other factors that could be abiotic, e.g. water availability, or biotic, e.g. local natural enemies adapted to Helicotylenchus spp. Introducing plant genotypes from othe
  • Soil Biology & Biochemistry

    Long-term organic farming fosters below and aboveground biota: Implications for soil quality, biological control and productivity

    K. Birkhofer, T. Martijn Bezemer, J. Bloem, M. Bonkowski, S. Christensen, D. Dubois, F. Ekelund, A. Fließbach, L. Gunst, K. Hedlund, P. Mäder, J. Mikola, Catherine Robin, H. Setälä, F. Tatin-Froux, Wim H. van der Putten, S. Scheu
    Organic farming may contribute substantially to future agricultural production worldwide by improving soil quality and pest control, thereby reducing environmental impacts of conventional farming. We investigated in a comprehensive way soil chemical, as well as below and aboveground biological parameters of two organic and two conventional wheat farming systems that primarily differed in fertilization and weed management strategies. Contrast analyses identified management related differences between “herbicide-free” bioorganic (BIOORG) and biodynamic (BIODYN) systems and conventional systems with (CONFYM) or without manure (CONMIN) and herbicide application within a long-term agricultural experiment (DOK trial, Switzerland). Soil carbon content was significantly higher in systems receiving farmyard manure and concomitantly microbial biomass (fungi and bacteria) was increased. Microbial activity parameters, such as microbial basal respiration and nitrogen mineralization, showed an opposite pattern, suggesting that soil carbon in the conventional system (CONFYM) was more easily accessible to microorganisms than in organic systems. Bacterivorous nematodes and earthworms were most abundant in systems that received farmyard manure, which is in line with the responses of their potential food sources (microbes and organic matter). Mineral fertilizer application detrimentally affected enchytraeids and Diptera larvae, whereas aphids benefited. Spider abundance was favoured by organic management, most likely a response to increased prey availability from the belowground subsystem or increased weed coverage. In contrast to most soil-based, bottom-up controlled interactions, the twofold higher abundance of this generalist predator group in organic systems likely contributed to the significantly lower abundance of aboveground herbivore pests (aphids) in these systems. Long-term organic farming and the application of farmyard manure promoted soil quality, microbial biomass and fostered natural enemies and ecosystem engineers, suggesting enhanced nutrient cycling and pest control. Mineral fertilizers and herbicide application, in contrast, affected the potential for top-down control of aboveground pests negatively and reduced the organic carbon levels. Our study indicates that the use of synthetic fertilizers and herbicide application changes interactions within and between below and aboveground components, ultimately promoting negative environmental impacts of agriculture by reducing internal biological cycles and pest control. On the contrary, organic farming fosters microbial and faunal decomposers and this propagates into the aboveground system via generalist predators thereby increasing conservation biological control. However, grain and straw yields were 23% higher in systems receiving mineral fertilizers and herbicides reflecting the trade-off between productivity and environmental responsibility.
  • Journal of Chemical Ecology

    Intraspecific Variation in Plant Defense Alters Effects of Root Herbivores on Leaf Chemistry and Aboveground Herbivore Damage

    S. Wurst, Nicole M. van Dam, F. Monroy, Arjen Biere, Wim H. van der Putten
    Root herbivores can indirectly affect aboveground herbivores by altering the food quality of the plant. However, it is largely unknown whether plant genotypes differ in their response to root herbivores, leading to variable defensive phenotypes. In this study, we investigated whether root-feeding insect larvae (Agriotes sp. larvae, wireworms) induce different responses in Plantago lanceolata plants from lines selected for low and high levels of iridoid glycosides (IG). In the absence of wireworms, plants of the “high-IG line” contained approximately twofold higher levels of total IG and threefold higher levels of catalpol (one of the IG) in leaves than plants from the “low-IG line,” whereas both lines had similar levels of IG in roots. In response to wireworms, roots of plants from both lines showed increased concentrations of catalpol. Leaves of “low-IG line” plants increased catalpol concentrations in response to wireworms, whereas catalpol concentrations of leaves of “high-IG line” plants decreased. In contrast, glucose concentrations in roots of “low-IG” plants decreased, while they increased in “high-IG” plants after feeding by wireworms. The leaf volatile profile differed between the lines, but was not affected by root herbivores. In the field, leaf damage by herbivores was higher in wireworm-induced compared to noninduced “low-IG” plants and lower in wireworm-induced compared to noninduced “high-IG” plants, despite induction of catalpol in leaves of the “low-IG” plants and reduction in “high-IG” plants. This pattern might arise if damage is caused mainly by specialist herbivores for which catalpol may act as feeding stimulant rather than as deterrent. The present study documents for the first time that intraspecific variation in plant defense affects the outcome of plant-mediated interactions between root and shoot herbivores.
  • Oikos

    Earthworms counterbalance the negative effects of microorganisms on plant diversity and enhance the tolerance of grasses to nematodes

    S. Wurst, Bas Allema, Henk Duyts, Wim H. van der Putten
    Plant community composition is affected by a wide array of soil organisms with diverse feeding modes and functions. Former studies dealt with the high diversity and complexity of soil communities by focusing on particular functional groups in isolation, by grouping soil organisms into body size classes or by using whole communities from different origins. Our approach was to investigate both the individual and the interaction effects of highly abundant soil organisms (microorganisms, nematodes and earthworms) to evaluate their impacts on grassland plant communities. Earthworms increased total plant community biomass by stimulating root growth. Nematodes reduced the biomass of grasses, but this effect was alleviated by the presence of earthworms. Non-leguminous forb biomass increased in the presence of nematodes, probably due to an alleviation of the competitive strength of grasses by nematodes. Microorganisms reduced the diversity and evenness of the plant community, but only in the absence of earthworms. Legume biomass was not affected by soil organisms, but Lotus corniculatus flowered earlier in the presence of microorganisms and the number of flowers decreased in the presence of nematodes. The results indicate that earthworms have a profound impact on the structure of grassland plant communities by counterbalancing the negative effects of plant-feeding nematodes on grasses and by conserving the evenness of the plant community. We propose that interacting effects of functionally dissimilar soil organisms on plant community performance have to be taken into account in future studies, since individual effects of soil organism groups may cancel out each other in functionally diverse soil communities.
  • Oikos

    Root herbivores influence the behaviour of an aboveground parasitoid through changes in plant-volatile signals

    Roxina Soler , Jeff A. Harvey, A.F.D. Kamp, Louise E.M. Vet, Wim H. van der Putten, Nicole M. van Dam, J.F. Stuefer, R. Gols, Cees Hordijk, T. Martijn Bezemer
    It is widely reported that plants emit volatile compounds when they are attacked by herbivorous insects, which may be used by parasitoids and predators to locate their host or prey. The study of herbivore-induced plant volatiles and their role in mediating interactions between plants, herbivores and their natural enemies have been primarily based on aboveground systems, generally ignoring the potential interactions between above and belowground infochemical- and food webs. This study examines whether herbivory by Delia radicum feeding on roots of Brassica nigra (black mustard) affects the behaviour of Cotesia glomerata, a parasitoid of the leaf herbivore Pieris brassicae, mediated by changes in plant volatiles. In a semi-field experiment with root-damaged and root-undamaged plants C. glomerata prefers to oviposit in hosts feeding on root-undamaged plants. In addition, in a flight-cage experiment the parasitoid also prefers to search for hosts on plants without root herbivores. Plants exposed to root herbivory were shown to emit a volatile blend characterized by high levels of specific sulphur volatile compounds, which are reported to be highly toxic for insects, combined with low levels of several compounds, i.e. beta-farnesene, reported to act as attractants for herbivorous and carnivorous insects. Our results provide evidence that the foraging behaviour of a parasitoid of an aboveground herbivore can be influenced by belowground herbivores through changes in the plant volatile blend. Such indirect interactions may have profound consequences for the evolution of host selection behaviour in parasitoids, and may play an important role in the structuring and functioning of communities.
  • Oecologia

    Soil microorganisms control plant ectoparasitic nematodes in natural coastal foredunes

    A.M. Piśkiewicz, Henk Duyts, M.P. Berg, S.R. Costa, Wim H. van der Putten
    Belowground herbivores can exert important controls on the composition of natural plant communities. Until now, relatively few studies have investigated which factors may control the abundance of belowground herbivores. In Dutch coastal foredunes, the root-feeding nematode Tylenchorhynchus ventralis is capable of reducing the performance of the dominant grass Ammophila arenaria (Marram grass). However, field surveys show that populations of this nematode usually are controlled to nondamaging densities, but the control mechanism is unknown. In the present study, we first established that T. ventralis populations are top-down controlled by soil biota. Then, selective removal of soil fauna suggested that soil microorganisms play an important role in controlling T. ventralis. This result was confirmed by an experiment where selective inoculation of microarthropods, nematodes and microbes together with T. ventralis into sterilized dune soil resulted in nematode control when microbes were present. Adding nematodes had some effect, whereas microarthropods did not have a significant effect on T. ventralis. Our results have important implications for the appreciation of herbivore controls in natural soils. Soil food web models assume that herbivorous nematodes are controlled by predaceous invertebrates, whereas many biological control studies focus on managing nematode abundance by soil microorganisms. We propose that soil microorganisms play a more important role than do carnivorous soil invertebrates in the top-down control of herbivorous ectoparasitic nematodes in natural ecosystems. This is opposite to many studies on factors controlling root-feeding insects, which are supposed to be controlled by carnivorous invertebrates, parasitoids, or entomopathogenic nematodes. Our conclusion is that the ectoparasitic nematode T. ventralis is potentially able to limit productivity of the dune grass A. arenaria but that soil organisms, mostly microorganisms, usually prevent the development of growth-reducing population densities.
  • Basic and Applied Ecology

    Root herbivore identity matters in plant-mediated interactions between root and shoot herbivores

    Plants are simultaneously attacked by a multitude of herbivores that affect plant responses and plant-mediated interactions in a variety of ways. So far, studies on indirect interactions between below- and aboveground herbivores have almost exclusively focused on interactions between only one root and one shoot herbivore species at the same time. Since these studies show a variety of outcomes, we test the hypothesis that root herbivore identity matters in below-/aboveground interactions. We studied the combined effects root-feeding nematodes (Pratylenchus penetrans) and wireworms (Agriotes lineatus larvae) on Plantago lanceolata and on the performance of aboveground phloem-feeding aphids (Myzus persicae) and chewing caterpillars (Chrysodeixis chalcites larvae). Since root herbivores may also affect resource availability and the microbial community in the rhizosphere, we examined resource utilization by soil microorganisms using BIOLOG EcoPlates™. Wireworms decreased root biomass by 13%, but led to compensatory shoot growth. Nematodes and the aboveground herbivores did not affect the biomass of Plantago lanceolata. Feeding by C. chalcites larvae enhanced the concentration of aucubin in leaves, which might explain the high mortality of the caterpillars. Aphids and the belowground herbivores did not change iridoid glycoside levels in the leaves. However, the number of aphid offspring was reduced by 44% when nematodes had been added to the s
  • Ecology

    Climate vs. soil factors in local adaptation of two common plant species

    Mirka Macel, C.S. Lawson, S.R. Mortimer, M. Šmilauerova, A. Bischoff, L. Crémieux, J. Doleźal, A.R. Edwards, V. Lanta, T. Martijn Bezemer, Wim H. van der Putten, J.M. Igual, C. Rodriguez-Barrueco, H. Müller-Schärer, T. Steinger
    Evolutionary theory suggests that divergent natural selection in heterogeneous environments can result in locally adapted plant genotypes. To understand local adaptation it is important to study the ecological factors responsible for divergent selection. At a continental scale, variation in climate can be important while at a local scale soil properties could also play a role. We designed an experiment aimed to disentangle the role of climate and (abiotic and biotic) soil properties in local adaptation of two common plant species. A grass (Holcus lanatus) and a legume (Lotus corniculatus), as well as their local soils, were reciprocally transplanted between three sites across an Atlantic–Continental gradient in Europe and grown in common gardens in either their home soil or foreign soils. Growth and reproductive traits were measured over two growing seasons. In both species, we found significant environmental and genetic effects on most of the growth and reproductive traits and a significant interaction between the two environmental effects of soil and climate. The grass species showed significant home site advantage in most of the fitness components, which indicated adaptation to climate. We found no indication that the grass was adapted to local soil conditions. The legume showed a significant home soil advantage for number of fruits only and thus a weak indication of adaptation to soil and no adaptation to climate. Our results show that the importance of climate and soil factors as drivers of local adaptation is species-dependent. This could be related to differences in interactions between plant species and soil biota.
  • Oecologia

    Impact of foliar herbivory on the development of a root-feeding insect and its parasitoid

    Roxina Soler , T. Martijn Bezemer, A.M. Cortesero, Wim H. van der Putten, Louise E.M. Vet, Jeff A. Harvey
    The majority of studies exploring interactions between above- and below-ground biota have been focused on the effects of root-associated organisms on foliar herbivorous insects. This study examined the effects of foliar herbivory by Pieris brassicae L. (Lepidoptera: Pieridae) on the performance of the root herbivore Delia radicum L. (Diptera: Anthomyiidae) and its parasitoid Trybliographa rapae (Westwood) (Hymenoptera: Figitidae), mediated through a shared host plant Brassica nigra L. (Brassicaceae). In the presence of foliar herbivory, the survival of D. radicum and T. rapae decreased significantly by more than 50%. In addition, newly emerged adults of both root herbivores and parasitoids were significantly smaller on plants that had been exposed to foliar herbivory than on control plants. To determine what factor(s) may have accounted for the observed results, we examined the effects of foliar herbivory on root quantity and quality. No significant differences in root biomass were found between plants with and without shoot herbivore damage. Moreover, concentrations of nitrogen in root tissues were also unaffected by shoot damage by P. brassicae larvae. However, higher levels of indole glucosinolates were measured in roots of plants exposed to foliar herbivory, suggesting that the development of the root herbivore and its parasitoid may be, at least partly, negatively affected by increased levels of these allelochemicals in root tissues. Our results show that foliar herbivores can affect the development not only of root-feeding insects but also their natural enemies. We argue that such indirect interactions between above- and below-ground biota may play an important role in the structuring and functioning of communities.
  • Nature

    Ecology: Diversity and stability in plant communities

    T. Martijn Bezemer, Wim H. van der Putten
    The relationship between species diversity and ecosystem stability is controversial1, 2. Tilman et al.3 analyse biomass patterns over a decade in a grassland experiment with artificial plant communities, and provide evidence for a positive relationship between the number of plant species and the temporal stability of the ecosystem. Here we use data from a long-term biodiversity experiment with plant communities that were not controlled by weeding4 in order to show that diverse systems can be both stable and unstable.
  • ISME Journal

    Microbial ecology of biological invasions

    Wim H. van der Putten, J.N. Klironomos, David A. Wardle
    Invasive microbes, plants and animals are a major threat to the composition and functioning of ecosystems; however, the mechanistic basis of why exotic species can be so abundant and disruptive is not well understood. Most studies have focused on invasive plants and animals, although few have considered the effects of invasive microbes, or interactions of invasive plant and animal species with microbial communities. Here, we review effects of invasive plants on soil microbial communities and discuss consequences for plant performance, plant community structure and ecosystem processes. In addition, we briefly discuss effects of invasive soil microbes on plant communities, which has been less well studied, and effects of invasive animals on soil decomposers and ecosystem functioning. We do this by considering each of three important functional groups of microbes, namely soil microbial parasites and pathogens, mutualistic symbionts and decomposers. We conclude that invasive plants, pathogenic and symbiotic soil microbes will have strongest effects on the abundance of individual species, community diversity and ecosystem functioning. Invasive decomposer microbes probably have little impact, because of limited specificity and great functional redundancy. However, invasive plants and animals can have major effects on microbial decomposition in soil. We propose that understanding, predicting and counteracting consequences of enhanced global homogenization of natural communities through introducing exotic plants, animals and microbes will require future studies on how pathogenic, symbiotic and decomposer soil microbes interact, how they are influenced by higher trophic level organisms and how their combined effects are influencing the composition and functioning of ecosystems.
  • Ecology

    Soil feedback of exotic savannah grass relates to pathogen absense and mycorrhizal selectivity

    Wim H. van der Putten, George Kowalchuk, Pella Brinkman, G.T.A. Doodeman, R.M. van der Kaaij, A.F.D. Kamp, F.B.J. Menting, E.M. Veenendaal
    Enemy release of exotic plants from soil pathogens has been tested by examining plant–soil feedback effects in repetitive growth cycles. However, positive soil feedback may also be due to enhanced benefit from the local arbuscular mycorrhizal fungi (AMF). Few studies actually have tested pathogen effects, and none of them did so in arid savannas. In the Kalahari savanna in Botswana, we compared the soil feedback of the exotic grass Cenchrus biflorus with that of two dominant native grasses, Eragrostis lehmanniana and Aristida meridionalis. The exotic grass had neutral to positive soil feedback, whereas both native grasses showed neutral to negative feedback effects. Isolation and testing of root-inhabiting fungi of E. lehmanniana yielded two host-specific pathogens that did not influence the exotic C. biflorus or the other native grass, A. meridionalis. None of the grasses was affected by the fungi that were isolated from the roots of the exotic C. biflorus. We isolated and compared the AMF community of the native and exotic grasses by polymerase chain reaction-denaturing gradient gel elecrophoresis (PCR-DGGE), targeting AMF 18S rRNA. We used roots from mon In conclusion, our results support the hypothesis that release from soil-borne enemies may facilitate local abundance of exotic plants, and we provide the first evidence that these processes may occur in arid savanna ecosystems. Pathogenicity tests implicated the involvement of soil pathogens in the soil feedback responses, and further studies should reveal the functional consequences of the observed high infection with a low diversity of AMF in the roots of exotic plants.
  • Ecological Monographs

    Microbe-mediated plant-soil feedback causes historical contingency effects in plant community assembly

    Paul Kardol, N.J. Cornips, M.M.L. Van Kempen, Tanja Bakx-Schotman, Wim H. van der Putten
    Plant–soil feedback affects performance and competitive ability of individual plants. However, the importance of plant–soil feedback in historical contingency processes and plant community dynamics is largely unknown. In microcosms, we tested how six early-successional plant species of secondary succession on ex-arable land induced plant-specific changes in soil community composition. Following one growth cycle of conditioning the soil community, soil feedback effects were assessed as plant performance in soil of their own as compared to soil from a mixture of the other five early-successional species. Performance was tested in monocultures and in mixed communities with heterospecific competition from mid-successional species. The role of soil microorganisms was determined by isolating the microbial component from the soil community, re-inoculating microorganisms into sterilized substrate, and analyzing plant biomass responses of the early- and mid-successional species. Plant–soil feedback responses of the early-successional species were negative and significantly increased when the plants were grown in a competitive environment with heterospecifics. In monocultures, three early-successional species experienced negative feedback in soil with a history of conspecifics, while all early-successional species experienced negative feedback when grown with interspecific competition. Interestingly, the nonnative forb Conyza canadensis showed the weakest soil feedback e We conclude that feedback between early-successional plant species and soil microorganisms can play a crucial role in breaking dominance of early-successional plant communities. Moreover the influences on soil microorganism community composition influenced plant community dynamics in the mid-successional plant communities. These results shed new light on how feedback effects between plants and soil organisms in one successional stage result in a biotic legacy effect, which influences plant commu
  • Journal of Ecology

    Reduced plant–soil feedback of plant species expanding their range as compared to natives

    Roy H. A. van Grunsven, Wim H. van der Putten, T. Martijn Bezemer, W.L.M. Tamis, Frank Berendse, E.M. Veenendaal
    1. As a result of global warming, species may spread into previously cool regions. Species that disperse faster than their natural enemies may become released from top-down control. We investigated whether plants originating from southern Europe and recently established in north-western Europe experience less soil pathogen effects than native species. 2. We selected three plant species originating from southern Europe that have immigrated into the Netherlands and three similar native Dutch species. All six plant species were grown in sterilized soils with a soil inoculum collected from the rhizospheres of field populations. As a control we grew a series of all six plant species with a sterilized rhizosphere inoculum. 3. We harvested the plants, added the conditioned soil to sterilized soil and grew a second generation of all six plant species in order to test for each plant pair feedback effects from the conditioned soil communities to conspecifics and heterospecifics. 4. The effect of the soil community is dependent on plant species, and is dependent on soil fertility in only one of the three pairs. 5. Soil conditioning caused less biomass reduction to exotic plant species than to native species, suggesting that exotic immigrants are less exposed to soil pathogens than similar native plant species. 6. Our results suggest that plant species that expand their range as a result of climate change may become released from soil pathogenic activity. Whether the exotics are released from soil pathogens, or whether they experience enhanced benefit from mutualistic symbionts remains to be studied. We conclude that range expansion may result in enemy release patterns that are similar to artificially introduced invasive exotic plant species. 7. The escape from enemies through range shifts changes key biotic interactions and complicates predictions of future distribution and dominance.
  • Applied Vegetation Science

    Long-term effectiveness of sowing high and low diversity seed mixtures to enhance plant community development on ex-arable fields

    J. Lepš, J. Doležal, T. Martijn Bezemer, V.K. Brown, K. Hedlund, M. Igual Arroyo, H.B. Jørgensen, C.S. Lawson, S.R. Mortimer, A. Peix Geldart, C. Rodríguez Barrueco, I. Santa Regina, P. Smilauer, Wim H. van der Putten
    Questions: How is succession on ex-arable land affected by sowing high and low diversity mixtures of grassland species as compared to natural succession? How long do effects persist? Location: Experimental plots installed in the Czech Republic, The Netherlands, Spain, Sweden and the United Kingdom. Methods: The experiment was established on ex-arable land, with five blocks, each containing three 10 m × 10 m experimental plots: natural colonization, a low- (four species) and high-diversity (15 species) seed mixture. Species composition and biomass was followed for eight years. Results: The sown plants considerably affected the whole successional pathway and the effects persisted during the whole eight year period. Whilst the proportion of sown species (characterized by their cover) increased during the study period, the number of sown species started to decrease from the third season onwards. Sowing caused suppression of natural colonizing species, and the sown plots had more biomass. These effects were on average larger in the high diversity mixtures. However, the lo Conclusions: The effect of sowing demonstrated dispersal limitation as a factor controlling the rate of early secondary succession. Diversity was important primarily for its ‘insurance effect’: the high diversity mixtures were always able to compensate for the failure of some species. Abbreviations; ED = Euclidian distance; HD = High diversity; LD = Low diversity; NC = Natural colonization
  • Oikos

    Above- and belowground insect herbivores differentially affect soil nematode communities in species-rich plant communities

    Gerlinde De Deyn, Jasper van Ruijven, Ciska Raaijmakers, P.C. de Ruiter, Wim H. van der Putten
    Interactions between above- and belowground invertebrate herbivores alter plant diversity, however, little is known on how these effects may influence higher trophic level organisms belowground. Here we explore whether above- and belowground invertebrate herbivores which alter plant community diversity and biomass, in turn affect soil nematode communities. We test the hypotheses that insect herbivores 1) alter soil nematode diversity, 2) stimulate bacterial-feeding and 3) reduce plant-feeding nematode abundances. In a full factorial outdoor mesocosm experiment we introduced grasshoppers (aboveground herbivores), wireworms (belowground herbivores) and a diverse soil nematode community to species-rich model plant communities. After two years, insect herbivore effects on nematode diversity and on abundance of herbivorous, bacterivorous, fungivorous and omni-carnivorous nematodes were evaluated in relation to plant community composition. Wireworms did not affect nematode diversity despite enhanced plant diversity, while grasshoppers, which did not affect plant diversity, reduced nematode diversity. Although grasshoppers and wireworms caused contrasting shifts in plant species dominance, they did not affect abundances of decomposer nematodes at any trophic level. Primary consumer nematodes were, however, strongly promoted by wireworms, while community root biomass was not altered by the insect herbivores. Overall, interaction eff
  • New Phytologist

    Mechanism of control of root-feeding nematodes by mycorrhizal fungi in the dune grass Ammophila arenaria

    E. De la Peña, S. Rodriguez Echeverría, Wim H. van der Putten, H. Freitas, M. Moens
    Root-feeding herbivores can affect plant performance and the composition of natural plant communities, but there is little information about the mechanisms that control root herbivores in natural systems. This study explores the interactions between the pioneer dune grass Ammophila arenaria, arbuscular mycorrhizal fungi (AMF) and the root-feeding nematode Pratylenchus penetrans. Our objectives were to determine whether AMF can suppress nematode infection and reproduction and to explore the mechanisms of nematode control by AMF. A sequential inoculation experiment and a split-root experiment were designed to analyse the importance of plant tolerance and resistance and of direct competition between AMF and P. penetrans for the root herbivore and the plant. Root infection and multiplication of P. penetrans were significantly reduced by the native inoculum of AMF. Plant preinoculation with AMF further decreased nematode colonization and reproduction. Nematode suppression by AMF did not occur through a systemic plant response but through local mechanisms. Our results suggest that AMF are crucial for the control of root-feeding nematodes in natural systems and illustrate that locally operating mechanisms are involved in this process. [KEYWORDS: bottom-up control ; coastal dunes ; multitrophic interactions ; nematode control ; plant ; mutualists ; Pratylenchus sp. ; root-feeding nematodes]
  • Journal of Ecology

    Plant species and functional group effects on abiotic and microbial soil properties and plant-soil feedback responses in two grasslands

    T. Martijn Bezemer, C.S. Lawson, K. Hedlund, A.R. Edwards, A.J. Brook, J.M. Igual, S.R. Mortimer, Wim H. van der Putten
    1 Plant species differ in their capacity to influence soil organic matter, soil nutrient availability and the composition of soil microbial communities. Their influences on soil properties result in net positive or negative feedback effects, which influence plant performance and plant community composition. 2 For two grassland systems, one on a sandy soil in the Netherlands and one on a chalk soil in the United Kingdom, we investigated how individual plant species grown in monocultures changed abiotic and biotic soil conditions. Then, we determined feedback effects of these soils to plants of the same or different species. Feedback effects were analysed at the level of plant species and plant taxonomic groups (grasses vs. forbs). 3 In the sandy soils, plant species differed in their effects on soil chemical properties, in particular potassium levels, but PLFA (phospholipid fatty acid) signatures of the soil microbial community did not differ between plant species. The effects of soil chemical properties were even greater when grasses and forbs were compared, especially because potassium levels were lower in grass monocultures. 4 In the chalk soil, there were no effects of plant species on soil chemical properties, but PLFA profiles differed significantly between soils from different monocultures. PLFA profiles differed between species, rather than between grasses and forbs. 5 In the feedback experiment, all plant species in sandy soils grew less vigorously in soils conditioned by grasses than in soils conditioned by forbs. These effects correlated significantly with soil chemical properties. None of the seven plant species showed significant differences between performance in soil conditioned by the same vs. other plant species. 6 In the chalk soil, Sanguisorba minor and in particular Briza media performed best in soil collected from conspecifics, while Bromus erectus performed best in soil from heterospecifics. There was no distinctive pattern between soils collected from forb and grass monocultures, and plant performance could not be related to soil chemical properties or PLFA signatures. 7 Our study shows that mechanisms of plant–soil feedback can depend on plant species, plant taxonomic (or functional) groups and site-specific differences in abiotic and biotic soil properties. Understanding how plant species can influence their rhizosphere, and how other plant species respond to these changes, will greatly enhance our understanding of the functioning and stability of ecosystems. [KEYWORDS: chalk grassland ; ecosystem functioning ; mechanisms of plant–soil feedback ; PLFA ; soil biodiversity ; soil chemistry ; stability ; succession ; variance partitioning ]
  • Advances in Agronomy

    Nematode interactions in nature: models for sustainable control of nematode pests of crop plants?

    Wim H. van der Putten, R. Cook, S.R. Costa, K.G. Davies, M. Fargette, H. Freitas, (Gera) W.H.G. Hol, B.R. Kerry, N. Maher, T. Mateille, M. Moens, E. De la Peña, A. Piskiewicz, A. Raeymaekers, S. Rodríguez-Echeverría, A.W.G. Van der Wurff
    Plant-parasitic nematodes are major crop pests in agro-ecosystems while in nature their impact may range from substantial to no significant growth reduction. The aim of this review is to determine if nematode population control in natural ecosystems may provide us with a model for enhancing sustainable control of nematodes in crops. In agricultural systems, monocultures, narrow rotations, alteration of the soil habitat, and fertilization may alter plant-parasitic nematode dynamics and boost nematode numbers while reducing diversity and effectiveness of top–down control organisms and protective mutualisms (endophytes and arbuscular mycorrhizal fungi). Traditional agro-ecosystems (still applied in tropical regions) involve the development of complex practices such as a broad range of plant species of high genetic diversity gr In nature, plant-parasitic nematodes (and other root feeders and soil pathogens) drive plant community processes, such as succession and plant species diversity. Natural soils contain a wide variety of potential nematode control organisms, but the consequences of this diversity are not known. Wild plant populations also contain more genetic variability than crops, but consequences for coevolution and Red Queen processes for nematode populations have not been studied. We conclude that integrated crop pest control may benefit from studying plant-parasitic nematode—natural antagonist interactions in natural systems, which have been coevolved for longer than crop-nematode–antagonist systems. Understanding how wild plants co