Martijn Bezemer

Prof. Martijn Bezemer

Guest researcher
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Visiting Address

Droevendaalsesteeg 10
6708 PB Wageningen

+31 (0) 317 47 34 00

The Netherlands

About

I am at Leiden University now, but still connected to NIOO as a guest researcher.

CV

Ancillary activities

Publications

Peer-reviewed publications

  • Basic and Applied Ecology
    23-02-2024

    Distance- and density-dependent recruitment of common ragwort is not driven by plant-soil feedbacks

    Xiangyu Liu, Dong He, Klaas Vrieling, Suzanne T. E. Lommen, Chenguang Gao, T. Martijn Bezemer

    Janzen-Connell effects state that the accumulation of host-specific natural enemies near parent plants can negatively affect their offspring. Negative plant-soil feedbacks can produce patterns of seedling performance predicted by Janzen-Connell effects and influence plant populations, but their relevance in field conditions remains unclear. Here, using spatial point-pattern analysis, we examine the spatial distribution of Jacobaea vulgaris to assess whether distance- and density-dependent predictions of Janzen-Connell effects are evident in the field. We established 27 replicated 64 m2 plots at two grassland sites and mapped positions of rosette-bearing and flowering J. vulgaris plants within each plot. To investigate temporal distribution patterns, we tracked plant positions repeatedly in three plots during a single season. Additionally, we tested whether these patterns are soil-mediated. Soil samples were collected underneath flowering plants and at a distance of 0.5 meter, and used to compare seed germination, seedling survival, and growth under controlled conditions. Furthermore, we measured J. vulgaris growth in soil from patches with high J. vulgaris densities and in soil from areas outside these patches. The density of rosette-bearing plants was lower at close distances from flowering plants than expected from null models, suggesting negative distance-dependent plant recruitment. The degree of clustering decreased over time from rosette-bearing to flowering plants, indicating density-dependent self-thinning. Seed germination was higher in soil further away from flowering J. vulgaris plants than in soil underneath plants at one site, but soil distance was not an overall significant factor in explaining seed germination. However, seedling mortality and biomass did not differ between soils collected at the two distances, and plants produced similar biomass in soil collected from inside and outside J. vulgaris patches. Our study demonstrates conspecific distance- and density-dependent plant recruitment in J. vulgaris in the field, but we found no evidence this depends on belowground natural enemies.

    https://doi.org/10.1016/j.baae.2024.02.003
  • Applied Soil Ecology
    01-12-2023

    Combined effects of aboveground herbivores and belowground microorganisms on dynamics of soil nematode communities in grassland mesocosms

    Yuting Ji, Gerlinde De Deyn, Naili Zhang, Hongwei Xu, Minggang Wang, T. Martijn Bezemer
    Nematodes are the most abundant animals in soil. They are active in all trophic levels and functionally important for plant growth and plant diversity. Nematode community structure not only can be directly influenced by other belowground organisms such as soil microbes via trophic interactions, but also indirectly by aboveground organisms like herbivores through plant-mediated aboveground-belowground linkages. In the current study, by introducing foliar-feeding aphids (Rhopalosiphum padi) and soil microbial suspensions to mesocosms planted with 12 grassland plant species and where an identical nematode community was introduced in all mesocosms, we aimed to investigate the individual and combined effects of soil microbes and foliar herbivores on the dynamics of plant and the soil nematode community. Introduction of aphids reduced shoot and root biomass of the plant community, and in particular decreased the proportional biomass of the dominant plant species Anthoxanthum odoratum, resulting in a higher diversity of the plant community but without affecting the nematode communities. In contrast, the inoculation of soil microbes did not significantly alter plant composition structure, but it reduced the total nematode abundance and enhanced nematode diversity by increasing the abundance of carnivorous nematodes and decreasing the abundance of plant-feeding nematodes. There were no significant aboveground-belowground interactions in the current study via effects of aphids on the soil nematode communities or via soil microbes and nematodes on the plant communities. Collectively, our study indicates that soil nematode communities in grasslands can be strongly steered by soil microbial inoculations but weakly influenced by aboveground herbivory despite its resulting changes in plant communities, notwithstanding that these effects appeared to be largely independent.
    https://doi.org/10.1016/j.apsoil.2023.105097
  • Agriculture, Ecosystems and Environment
    01-10-2023

    Interspecific interactions between crops influence soil functional groups and networks in a maize/soybean intercropping system

    Guizong Zhang, Hao Yang, Weiping Zhang, T. Martijn Bezemer, Wenju Liang, Qi Li, Long Li

    Despite increasing evidence that intercropping systems may increase crop productivity, little is known about whether and how soil biota change under interspecific competition among plants. A field experiment with maize/soybean intercropping and the corresponding monoculture systems was conducted under four nitrogen fertilization regimes to investigate the effects of interspecific plant interactions on grain yield, soil properties (β-glucosidase and water-soluble carbohydrates), and biotic communities (bacteria, fungi, and nematodes). The soils under maize and soybean in the intercropping system were sampled separately to represent intercropped maize and intercropped soybean, respectively. Compared to monocultures, the complexity and robustness of soil networks comprising bacterial, fungal, and nematode communities increased in intercropped maize soils, but densities of plant parasitic nematodes and β-glucosidase activity were reduced. Intercropped soybean soils had lower C availability due to chronic shading by maize, but a significant increase was found in saprophytic fungi, and plant parasitic nematodes compared to soybean monoculture soils. Although intercropped soybean suffered from interspecific competition with maize, the interactions within the fungal community increased for both crop species in the intercropping system. Our study demonstrates that increased carbon uptake in maize due to increased light capture in the intercropping system can facilitate nutrient cycling by altering the abundance of functional groups of soil organisms, such as saprophytic fungi, and enhancing network complexity and stability. We detected a trade-off between productivity and soil nematode diversity in the intercropping system under nitrogen fertilization, the yield of maize increased but soil nematode richness decreased at low nitrogen level, while the yield of soybean decreased but the nematode richness increased at high nitrogen level. These findings show that both trade-offs and benefits occur in intercropping systems and highlight the role of plant-soil biota interactions in such systems.

    https://doi.org/10.1016/j.agee.2023.108595
  • Environmental Research
    01-09-2023

    Effect of organic amendments obtained from different pretreatment technologies on soil microbial community

    Yujia Luo, Vania Scarlet Chavez-Rico, Valentina Sechi, T. Martijn Bezemer, Cees N.J. Buisman, Annemiek ter Heijne

    The application of organic amendments (OAs) obtained from biological treatment technologies is a common agricultural practice to increase soil functionality and fertility. OAs and their respective pretreatment processes have been extensively studied. However, comparing the properties of OAs obtained from different pretreatment processes remains challenging. In most cases, the organic residues used to produce OAs exhibit intrinsic variability and differ in origin and composition. In addition, few studies have focused on comparing OAs from different pretreatment processes in the soil microbiome, and the extent to which OAs affect the soil microbial community remains unclear. This limits the design and implementation of effective pretreatments aimed at reusing organic residues and facilitating sustainable agricultural practices. In this study, we used the same model residues to produce OAs to enable meaningful comparisons among compost, digestate, and ferment. These three OAs contained different microbial communities. Compost had higher bacterial but lower fungal alpha diversity than ferment and digestate. Compost-associated microbes were more prevalent in the soil than ferment- and digestate-associated microbes. More than 80% of the bacterial ASVs and fungal OTUs from the compost were detected 3 months after incorporation into the soil. However, the addition of compost had less influence on the resulting soil microbial biomass and community composition than the addition of ferment or digestate. Specific native soil microbes, members from Chloroflexi, Acidobacteria, and Mortierellomycota, were absent after ferment and digestate application. The addition of OAs increased the soil pH, particularly in the compost-amended soil, whereas the addition of digestate enhanced the concentrations of dissolved organic carbon (DOC) and available nutrients (such as ammonium and potassium). These physicochemical variables were key factors that influenced soil microbial communities. This study furthers our understanding of the effective recycling of organic resources for the development of sustainable soils.

    https://doi.org/10.1016/j.envres.2023.116346
  • Geoderma
    09-2023

    Soil addition improves multifunctionality of degraded grasslands through increasing fungal richness and network complexity

    Yuhui Li, Xu Han, Bing Li, Yingbin Li, Xiaofang Du, Yixin Sun, Qi Li, T. Martijn Bezemer

    Soil addition is now widely used in the restoration of degraded ecosystems, but how soil addition influences multiple ecological functions of degraded grasslands, and whether these effects depend on the amount and type of soil inoculum, are still not clear. We performed two parallel experiments to examine how two different donor soil types and two amounts of donor soil addition affect the restoration of degraded grassland. In a field experiment at a degraded grassland site where the top layer of the soil was removed (5 cm), we assessed the effect of addition of soil collected from two different ecosystems (upland meadow and meadow steppe) and addition of different amounts of soil (0 cm, 1 cm and 3 cm) on ecosystem multifunctionality. In a microcosm experiment, we examined the effects of soil biotic and abiotic factors on ecosystem functions by inoculating sterilized and non-sterilized soil. Soil addition promoted the restoration of degraded grassland, particularly when higher amounts of soil were added. Both biotic and abiotic factors increased ecosystem multifunctionality. Biotic factors, especially fungal richness and network complexity, had the strongest positive effects on ecosystem multifunctionality. Our study reveals the importance of fungal communities in soil for improving ecosystem multifunctionality in restoration of degraded grassland. Future studies should explore the effects of joint addition of arbuscular mycorrhizal fungi and saprophytic fungi on the ecosystem functions of degraded grasslands.

    https://doi.org/10.1016/j.geoderma.2023.116607
  • Plant and Soil
    05-2023

    Local-scale soil nematode diversity in a subtropical forest depends on the phylogenetic and functional diversity of neighbor trees

    Yingbin Li, Xiaofang Du, Xiaolin Su, Xu Han, Wenju Liang, Zhengwen Wang, Helge Bruelheide, T. Martijn Bezemer, Qi Li
    Purpose

    Understanding the impact of neighbor tree diversity on soil biodiversity at the individual tree scale and clarifying which facets of neighbor tree diversity have a decisive impact on soil biodiversity.
    Methods

    We collected and identified soil nematodes underneath 256 individual trees of 16 species at four species-richness levels (1, 2, 4, 8 species) in a large tree diversity experiment in southeast China. We analyzed how the taxonomic, phylogenetic, and functional diversity of the nematode community were influenced by neighbor tree diversity.
    Results

    Our analyses showed that nematode alpha diversity at the individual tree scale decreased with increasing neighbor tree richness while beta diversity increased at taxonomic, phylogenetic, and functional levels. Nematode alpha diversity at the plot scale increased with increasing neighbor tree richness. Secondly, we found that reducing redundant species and increasing distinct species led to the differentiation of nematode communities under different individual trees in high-richness plots. Finally, our data revealed that the functional diversity of the neighbor tree community had the largest effects on the diversity of the local nematode community.
    Conclusion

    Our study emphasizes that there is a significant influence from neighboring trees, mainly the functional traits of the trees, even though they are spaced at distances multitudes greater than the distance over which soil nematodes can move. Hence it is important to consider these broader spatial aspects when examining the plant and soil biotic interactions.
    https://doi.org/10.1007/s11104-023-05882-2
  • Plant, Cell and Environment
    27-02-2023

    Root exudates and rhizosphere microbiomes jointly determine temporal shifts in plant‐soil feedbacks

    Katja Steinauer, Maddy Thakur, Alexander Weinhold, Henriette Uthe, Nicole M. van Dam, T. Martijn Bezemer
    Plants influence numerous soil biotic factors that can alter the performance of later growing plants—defined as plant-soil feedback (PSF). Here, we investigate whether PSF effects are linked with the temporal changes in root exudate diversity and the rhizosphere microbiome of two common grassland species (Holcus lanatus and Jacobaea vulgaris). Both plant species were grown separately establishing conspecific and heterospecific soils. In the feedback phase, we determined plant biomass, measured root exudate composition, and characterised rhizosphere microbial communities weekly (eight time points). Over time, we found a strong negative conspecific PSF on J. vulgaris in its early growth phase which changed into a neutral PSF, whereas H. lanatus exhibited a more persistent negative PSF. Root exudate diversity increased considerably over time for both plant species. Rhizosphere microbial communities were distinct in conspecific and heterospecific soils and showed strong temporal patterns. Bacterial communities converged over time. Using path models, PSF effects could be linked to the temporal dynamics of root exudate diversity, whereby shifts in rhizosphere microbial diversity contributed to temporal variation in PSF to a lesser extent. Our results highlight the importance of root exudates and rhizosphere microbial communities in driving temporal changes in the strength of PSF effects.
    https://doi.org/10.1111/pce.14570
  • Basic and Applied Ecology
    02-2023

    Current and legacy effects of neighborhood communities on plant growth and aboveground herbivory

    Xiangyu Liu, T. Martijn Bezemer

    Current and legacy effects can greatly affect the growth of a focal plant and its interactions with herbivores and such effects can be mediated by above- and belowground effects. However, determining the relative importance of current and legacy above- and belowground effects in natural conditions is a major challenge. In a long-term grassland experiment, we examined the relative importance of the current and legacy above- and belowground effects of plant communities on the growth and aboveground herbivore damage on a focal plant, Leucanthemum vulgare. Focal plants were planted into tubes with soil collected from different plant communities and placed back into the plant communities. Weekly, plant growth and damage were recorded and after 12 weeks plant biomass was measured. We analyzed how well aboveground and belowground characteristics of the current and legacy plots explained plant growth and herbivory. We found both current plant communities and legacy plant communities significantly affected plant growth (shoot biomass and the number of leaves) and herbivory. Root biomass of the focal plants was influenced by current plant communities only. Current and legacy above- and belowground characteristics explained 12% and 11% of the variation in shoot biomass. Root biomass was mainly explained by current above- and belowground characteristics with a total explained variation of 10%, while legacy effects explained 3%. Legacy effects explained most variation in the number of leaves during the first two weeks of measurements, and the effect remained present during the growth season. In contrast, characteristics of the current community explained most of the variation in herbivory throughout the growth period, with on average 6% explained variance aboveground vs. 5% belowground. Our grassland field study highlights that both current and legacy effects influence plant growth, but herbivory on focal plants is caused by current neighborhood effects only and not by legacy effects.

    https://doi.org/10.1016/j.baae.2022.12.007
  • Journal of Ecology
    31-01-2023

    Plant community responses to alterations in soil abiotic and biotic conditions are decoupled for above‐ and below‐ground traits

    Chenguang Gao, T. Martijn Bezemer, Peter M. van Bodegom, Johannes H. C. Cornelissen, Richard S.P. van Logtestijn, Xiangyu Liu, Riccardo Mancinelli, Harrie van der Hagen, Meng Zhou, Nadejda A. Soudzilovskaia

    Plant functional traits are increasingly recognised as being impacted by soil abiotic and biotic factors. Yet, the question to what extent the coupling between community-level above- and below-ground traits is affected by soil conditions remains open.
    In a field experiment in dune grassland, we quantified the responses of both community-level leaf and root traits to changes in soil abiotic and biotic conditions using soil inoculation by living and sterile soil inocula originated from different dune ecosystems.
    Altered soil conditions resulted in a strong decoupling in responses of community-level leaf and root traits. Changes in soil abiotic conditions imposed by soil inoculation were more important in determining the decoupling of the leaf vs root relationships than additions of soil biota. Altered soil abiotic factors influenced both leaf and root traits at the community level and caused the entire community-level trait spectrum to shift, while experimental additions of living soil inocula only significantly influenced root traits towards longer and thinner roots.
    Synthesis. Our results bring direct evidence that, at a plant community level, the dynamics of plant above-ground traits are not informative of below-ground traits. Particularly, below-ground abiotic processes are a major driver of commonly observed trait spectra. We suggest that future study is required to test the general pattern of leaf and root correlations across different ecosystems under field conditions.
    https://doi.org/10.1111/1365-2745.14070
  • Ecological Engineering
    2023

    Substrate composition impacts long-term vegetation development on blue-green roofs

    Henk-Jan van der Kolk, Petra van den Berg, Thijs van Veen, T. Martijn Bezemer

    Green roofs provide ecosystem services and can promote biodiversity in urban areas. Blue-green roofs have an additional water storage compartment under the substrate to reduce roof water runoff, thereby also reducing drought stress which is beneficial for green roof vegetation. In order to study which blue-green roof design supports the highest plant diversity, we assessed the effect of different substrates and seed mixtures on vegetation development in a short-term greenhouse experiment and long-term blue-green roof experiment. A ten-week full-factorial greenhouse experiment was performed for six substrate composition and four seed mixture treatments. On an experimental blue-green roof, we annually surveyed plants from 2013 to 2021 in nine different treatments (five replicates each), that varied in substrate composition, substrate depth and seed mixture that was initially applied. Two treatments resembled conventional non-green roofs (100% gravel) and conventional extensive Sedum green roofs. The results of the greenhouse experiment showed that seed mixture is more important than substrate composition in shaping the initial species richness and species composition. However, on the experimental roof the substrate composition was an important determinant of species richness and species composition long-term. Plant species richness on the experimental roof was lowest in the gravel treatment (resembling conventional non-green roofs), and highest in treatments where locally collected soil was used, likely due to additional species that appeared from the seed bank present in the transplanted soil. Soil was never completely covered with vegetation on unfertilized substrates that contained 20% or less dense and organic materials. Plant species richness on conventional Sedum roof substrate was higher on the experimental blue-green roof compared to an adjacent non-blue roof, highlighting that blue-green roofs can promote biodiversity more than conventional green roofs. For future construction of blue-green roofs in our region, we recommend the addition of 30% locally collected soil to a 6 cm deep lightweight substrate to maximize long-term plant cover and plant species richness.

    https://doi.org/10.1016/j.ecoleng.2022.106847
  • Science China Life Sciences
    2023

    Growth substrates alter aboveground plant microbial and metabolic properties thereby influencing insect herbivore performance

    Jun Yuan, Tao Wen, Shengdie Yang, Chao Zhang, Mengli Zhao, Guoqing Niu, Penghao Xie, Xiaoyu Liu, Xinyuan Zhao, Qirong Shen, T. Martijn Bezemer

    The gut microbiome of plant-eaters is affected by the food they eat, but it is currently unclear how the plant metabolome and microbiome are influenced by the substrate the plant grows in and how this subsequently impacts the feeding behavior and gut microbiomes of insect herbivores. Here, we use Plutella xylostella caterpillars and show that the larvae prefer leaves of cabbage plants growing in a vermiculite substrate to those from plants growing in conventional soil systems. From a plant metabolomics analysis, we identified 20 plant metabolites that were related to caterpillar feeding performance. In a bioassay, the effects of these plant metabolites on insects’ feeding were tested. Nitrate and compounds enriched with leaves of soilless cultivation promoted the feeding of insects, while compounds enriched with leaves of plants growing in natural soil decreased feeding. Several microbial groups (e.g., Sporolactobacillus, Haliangium) detected inside the plant correlated with caterpillar feeding performance and other microbial groups, such as Ramlibacter and Methylophilus, correlated with the gut microbiome. Our results highlight the role of growth substrates on the food metabolome and microbiome and on the feeding performance and the gut microbiome of plant feeders. It illustrates how belowground factors can influence the aboveground properties of plant-animal systems, which has important implications for plant growth and pest control.

    https://doi.org/10.1007/s11427-022-2279-5
  • Soil Biology and Biochemistry
    11-2022

    Biochar application differentially affects soil micro-, meso-macro-fauna and plant productivity within a nature restoration grassland

    Simon Jeffery, Tess Van de Voorde, W. Edwin Harris, Liesje Mommer, Jan Willem van Groenigen, Gerlinde De Deyn, Flemming Ekelund, Maria J.I. Briones, T. Martijn Bezemer

    Biochar is proposed as an option to sequester carbon (C) in soils and promote other soil-based ecosystem services. However, its impact on soil biota from micro to macroscale remains poorly understood. We investigated biochar effects on the soil biota across the soil food web, on plant community composition and on biomass production. We conducted a field experiment in a nature restoration grassland testing four treatments: two biochar types (herbaceous feedstock pyrolyzed at 400 °C or 600 °C – hereafter B400 and B600), and a positive (i.e. unpyrolysed biochar feedstock, hereafter Hay) and negative (no addition) control. Responses of plants and soil biota were evaluated one and three years after establishing the treatments. Soil pH and K concentrations increased significantly in the B600 treatment. Mite abundances were significantly higher in B400 whereas nematode abundances were highest in Hay (1st year) and lowest in B400 (3rd year). Other soil fauna groups (enchytraeids and earthworms) varied more between years than between treatments. Legume cover increased significantly in the biochar treatments but this effect was transient. Legumes, grasses and primary productivity also showed a statistically significant Treatment x Year interaction due to transitory effects that were no longer present by the 3rd year. Our results suggest that biochar produced from meadow cuttings and applied at the 10 t/ha rate cause transitory impacts on soil biota abundance and plant communities over the 3-year timeframe used for this experiment. Therefore, this type of biochar could potentially be used for soil carbon sequestration, with minimal impacts on soil biota abundance or diversity, within the groups studied here, or plant biodiversity and productivity. Further research is required to investigate the longer-term impacts of this potential soil C storage sink.

    https://doi.org/10.1016/j.soilbio.2022.108789
  • Functional Ecology
    10-2022

    Light condition experienced by parent plants influences the response of offspring to light via both parental effects and soil legacy effects

    Wei Xue, Lin Huang, Fei Hai Yu, T. Martijn Bezemer

    Environmental conditions experienced by parent plants can influence offspring performance through parental effects induced by DNA methylation. The offspring can also be influenced by environmental conditions experienced by their parents via soil legacy effects due to plant-mediated changes in the composition of soil microbes. These two effects are likely to act simultaneously, but empirical evidence for combined effects is limited. We conducted a two-phase experiment with five genotypes of a clonal plant Hydrocotyle vulgaris. In the first phase, we grew parent plants of each genotype under two light conditions (ambient vs. shade) and two DNA demethylation treatments [treated with water vs. 5-azacytidine (5-azaC)]. We then collected soils and clonal offspring for each genotype from each of these four treatments and measured soil (a)biotic properties. In the second phase, we grew the offspring from each of the four treatments in the four different soils, under the two light conditions. When grown under ambient light condition and in soil from ambient parents, offspring produced by ambient parents grew larger than offspring produced by shaded parents when the parents were treated with water. This difference was smaller when the parents were treated with 5-azaC, and disappeared when the offspring were grown in soil from shaded parents. The growth difference was also observed when the offspring were grown under shaded condition and in soil from shaded parents. However, this difference was greater when the parents were treated with 5-azaC, and disappeared when the offspring were grown in soil from ambient parents. Moreover, offspring growth was associated with fungal composition and total phosphorus of the soil in which the parents had grown. Our results show, for the first time, that light condition experienced by parents can influence offspring responses to light through both parental effects and soil legacies. The parental effects were mediated by changes in DNA methylation and the soil legacies were due to plant-mediated changes in a combination of soil biotic and abiotic properties. These impacts may eventually influence the ecological and evolutionary trajectories of clonal plant populations. Read the free Plain Language Summary for this article on the Journal blog.

    https://doi.org/10.1111/1365-2435.14136
  • ISME Communications
    26-07-2022

    Soil inoculum identity and rate jointly steer microbiomes and plant communities in the field

    Xu Han, Yingbin Li, Yuhui Li, Xiaofang Du, Bing Li, Qi Li, T. Martijn Bezemer
    Inoculation with soil from different ecosystems can induce changes in plant and soil communities and promote the restoration of degraded ecosystems. However, it is unknown how such inoculations influence the plant and soil communities, how much inoculum is needed, and whether inocula collected from similar ecosystems will steer soil and plant communities in different directions. We conducted a three-year soil inoculation experiment at a degraded grassland and used two different soil inocula both from grasslands with three inoculation rates. We measured the development of the soil and plant communities over a period of three years. Our results show that soil inoculation steers the soil microbiome and plant communities at the inoculated site into different directions and these effects were stronger with higher amount of soil used to inoculate. Network analyses showed that inoculation with upland meadow soil introduced more genera occupying the central position in the biotic network and resulted in more complex networks in the soil than inoculation with meadow steppe soil. Our findings emphasize that there are specific effects of donor soil on soil microbiomes as well as plant communities and that the direction and speed of development depend on the origin and the amount of soil inoculum used. Our findings have important implications for the restoration of biodiversity and ecosystem functioning in degraded grassland ecosystems.
    https://doi.org/10.1038/s43705-022-00144-1
  • Geoderma
    2022

    Effects of sterilization and maturity of compost on soil bacterial and fungal communities and wheat growth

    Yujia Luo, Siyu Chen, H. Pieter J. van Veelen, Valentina Sechi, Annemiek ter Heijne, Annegreet Veeken, Cees N.J. Buisman, T. Martijn Bezemer
    Composts are commonly used as soil amendments to sustain and improve the functionality of agricultural soil. Compost has abiotic (organic matter [OM], nutrients) and biotic characteristics (microorganisms) and both can influence the soil microbiome. The abiotic and biotic characteristics of compost, in turn, depend on properties of the compost such as maturity. Few studies have investigated the relative effects of abiotic and biotic components of compost on the soil microbial community and crop growth. To bridge this gap, we used a full-factorial design with sterile and live composts that differed in maturity (fresh, intermediate, mature) that were added to sterile and live soil to investigate the separate role of abiotic and biotic characteristics of composts on the resulting soil microbial community and on wheat growth. We found that the changes in the soil microbial community were mainly due to the input of compost with the presence of microorganisms rather than due to the abiotic properties of compost. The majority of the compost-associated microorganisms (more than 70% for bacteria and 90% for fungi) were detected in the soil in the presence of native soil microorganisms. Elimination of native soil microorganisms by sterilization enhanced the prevalence and abundance of compost-associated microorganisms. Adding fresh compost increased wheat biomass production, but the positive effects of compost on plant growth were strongest when sterile composts were used. Hence, our study reports that compost-associated microorganisms are essential to modify soil microbial community but may not benefit crop growth. This highlights the importance of understanding the role of abiotic and biotic properties of composts as common soil amendments on improving the functioning of agricultural soil.
    https://doi.org/10.1016/j.geoderma.2021.115598
  • Functional Ecology
    2022

    Foliar herbivory on plants creates soil legacy effects that impact future insect herbivore growth via changes in plant community biomass allocation

    Robin Heinen, Maddy Thakur, Jetske R. Hiddes de Fries, Katja Steinauer, Simon Vandenbrande, R. Jongen, T. Martijn Bezemer

    Plants leave legacy effects in the soil they grow in, which can drive important vegetation processes, including productivity, community dynamics and species turnover. Plants at the same time also face continuous pressure posed by insect herbivores. Given the intimate interactions between plants and herbivores in ecosystems, plant identity and herbivory are likely to interactively shape soil legacies. However, the mechanisms that drive such legacy effects on future generations of plants and associated herbivores are little known. In a greenhouse study, we exposed 10 common grasses and non-leguminous forbs individually to insect herbivory by two closely related noctuid caterpillars, Mamestra brassicae and Trichoplusia ni (Lepidoptera: Noctuidae) or kept them free of herbivores. We then used the soil legacies created by these plant individuals to grow a plant community composed of all 10 plant species in each soil and exposed these plant communities to M. brassicae. We measured conditioning plant biomass, soil respiration and chemistry of the conditioned soils, as well as individual plant, plant community and herbivore biomass responses. At the end of the conditioning phase, soils with herbivore legacies had higher soil respiration, but only significantly so for M. brassicae. Herbivore legacies had minimal impacts on community productivity. However, path models reveal that herbivore-induced soil legacies affected responding herbivores through changes in plant community shoot: root ratios. Soil legacy effect patterns differed between functional groups. We found strong plant species and functional group-specific effects on soil respiration parameters, which in turn led to plant community shifts in grass: forb biomass ratios. Soil legacies were negative for the growth of plants of the same functional group. Synthesis. We show that insect herbivory, plant species and their functional groups, all incur soil microbial responses that lead to subtle (herbivory) or strong (plants and their functional group) effects in response plant communities and associated polyphagous herbivores. Hence, even though typically ignored, our study emphasizes that legacies of previous insect herbivory in the soil can influence current soil–plant–insect community interactions. A free Plain Language Summary can be found within the Supporting Information of this article.

    https://doi.org/10.1111/1365-2435.14006
  • Plant and Soil
    2022

    Microbial soil legacies of crops under different water and nitrogen levels determine succeeding crop performance

    M. Kuerban, Wen-Feng Cong, Jingying Jing, T. Martijn Bezemer
    Background and aims
    Soil legacies mediated by abiotic and biotic factors can greatly influence succeeding plants, a phenomenon called plant-soil feedback (PSF). To date, the patterns and mechanisms of PSF remain largely unexplored in agroecosystems, especially how soil microbial legacies of crop species and management practices interact is poorly understood.

    Methods
    We subjected four common arable crop species (wheat, maize, soybean and rapeseed) to water (sufficient or drought) and nitrogen (high or low) treatments to condition living soil. We analyzed soil nutrient properties and microbiome composition, and then grew the four crops in conspecific and heterospecific soils to examine intra- and inter-specific PSFs.

    Results
    We found that crop species, nitrogen and water treatments created differential effects on soil bacteria and fungi diversity and community composition. Wheat grew better in conspecific-conditioned soil than in heterospecific-conditioned soil, whereas maize and soybean performed better in heterospecific-conditioned soils regardless of water and nitrogen treatments. The PSFs of rapeseed depended on the water and nitrogen treatments. The dissimilarity of both soil bacterial and fungal communities showed a consistently positive correlation with the feedback effect for wheat, while it negatively correlated for maize, rapeseed and soybean. Path analysis showed that soil abiotic, bacterial and fungal legacies all impacted the corresponding crop growth.

    Conclusions
    We show that via selecting crop species and by changing management practices we can create positive legacies that can enhance the growth of the succeeding crop. Hence, this work proposed a new way to capitalize on soil legacies for enhancing agricultural productivity.
    https://doi.org/10.1007/s11104-022-05412-6
  • Journal of Plant Ecology
    2022

    The negative effects of soil microorganisms on plant growth only extend to the first weeks.

    Jianfeng Zhang, P.G.L. Klinkhamer, Klaas Vrieling, T. Martijn Bezemer
    Soil biotic communities can strongly impact plant performance. In this paper, we ask the question: how long-lasting the effect of the soil microbial community on plant growth is. We examined the plant growth rates at three stages: early, mid and late growth. We performed two growth experiments with Jacobaea vulgaris, which lasted 49 and 63 days in sterilized soil or live soil. In a third experiment, we examined the effect of the timing of soil inoculation prior to planting on the relative growth rate of J. vulgaris with four different timing treatments. In all experiments, differences in biomass of plants grown in sterilized soil and live soil increased throughout the experiment. Also, the relative growth rate of plants in the sterilized soil was only significantly higher than that of plants in the live soil in the first two to three weeks. In the third experiment, plant biomass decreased with increasing time between inoculation and planting. Overall, our results showed that plants of J. vulgaris grew less well in live soil than in sterilized soil. The negative effects of soil inoculation on plant mass appeared to extend over the whole growth period but arise from the negative effects on relative growth rates that occurred in the first weeks.
    https://doi.org/10.1093/jpe/rtac022
  • Soil Biology and Biochemistry
    2022

    Bacterial and fungal co-occurrence patterns in agricultural soils amended with compost and bokashi

    Yujia Luo, Juan Bautista Gonzalez Lopez, H. Pieter J. van Veelen, Valentina Sechi, Annemiek ter Heijne, T. Martijn Bezemer, Cees N.J. Buisman

    The living soil harbors a significant number and diversity of bacteria and fungi, which are essential in sustaining soil ecosystem functions. Most studies focus on soil bacteria or fungi, ignoring potential interrelationships between kingdoms that coevolve and synergistically provide ecosystem functions. In a seven-year agricultural field, we explored the effects of organic amendments (OAs; i.e., compost and bokashi) on intra- and inter-kingdom co-occurrence networks of soil bacterial and fungal communities. We observed that OAs changed the co-occurrence patterns of bacteria and fungi. Distinct network modules were observed in the unamended and amended soils, and the physicochemical properties of the soil could partially explain the formation of these modules. We also found that compost and bokashi increased the proportion of positive correlations, and this could reduce competition among microorganisms for soil resources. Our study reveals that soil management with OAs affects relationships between bacterial and fungal subpopulations that physically co-exist, cooperate, and compete in non-random structured networks. It highlights that ecosystem functions may depend on inter-kingdom interactions shaped by different amendments and their applied dose.

    https://doi.org/10.1016/j.soilbio.2022.108831
  • Plant and Soil
    2022

    Belowground responses of bacterial communities to foliar SA application over four plant generations

    Jing Zhang, Peter G.L. Klinkhamer, Klaas Vrieling, T. Martijn Bezemer

    Background and aims: Jacobaea vulgaris plants grow better in sterilized than in live soil. Foliar application of SA mitigates this negative effect of live soil on plant growth. To examine what causes the positive effect of SA application on plant growth in live soils, we analyzed the effects of SA application on the composition of active rhizosphere bacteria in the soil.

    Methods: We studied the composition of the microbial community over four consecutive plant cycles (generations), using mRNA sequencing of the microbial communities in the rhizosphere of J. vulgaris. We initiated the experiment with an inoculum of live soil collected from the field, and at the start of each subsequent plant cycle, we inoculated a small part of the soil from the previous plant cycle into sterile bulk soil.

    Results: Application of SA did not significantly increase or decrease the Shannon diversity at genus level within each generation, but several specific genera were enriched or depleted after foliar SA application. The composition of bacterial communities in the rhizosphere significantly differed between plant cycles (generations), but application of SA did not alter this pattern. In the first generation no genera were significantly affected by the SA treatment, but in the second, third and fourth generations, specific genera were significantly affected. 89 species out of the total 270 (32.4%) were present as the “core” microbiome in all treatments over four plant cycles.

    Conclusions: Overall, our study shows that the composition of bacterial genera in the rhizosphere significantly differed between plant cycles, but that it was not strongly affected by foliar application of SA on J. vulgaris leaves. Further studies should examine how activation of the SA signaling pathway in the plant changes the functional genes of the rhizosphere bacterial community.

    https://doi.org/10.1007/s11104-021-05158-7
  • Ecosystems
    2022

    Soil Biota Adversely Affect the Resistance and Recovery of Plant Communities Subjected to Drought

    Chenguang Gao, Peter M. van Bodegom, T. Martijn Bezemer, Michiel P. Veldhuis, Riccardo Mancinelli, Nadejda A. Soudzilovskaia

    Climate change predictions indicate that summer droughts will become more severe and frequent. Yet, the impact of soil communities on the response of plant communities to drought remains unclear. Here, we report the results of a novel field experiment, in which we manipulated soil communities by adding soil inocula originating from different successional stages of coastal dune ecosystems to a plant community established from seeds on bare dune sand. We tested if and how the added soil biota from later-successional ecosystems influenced the sensitivity (resistance and recovery) of plant communities to drought. In contrast to our expectations, soil biota from later-successional soil inocula did not improve the resistance and recovery of plant communities subjected to drought. Instead, inoculation with soil biota from later successional stages reduced the post-drought recovery of plant communities, suggesting that competition for limited nutrients between plant community and soil biota may exacerbate the post-drought recovery of plant communities. Moreover, soil pathogens present in later-successional soil inocula may have impeded plant growth after drought. Soil inocula had differential impacts on the drought sensitivity of specific plant functional groups and individual species. However, the sensitivity of individual species and functional groups to drought was idiosyncratic and did not explain the overall composition of the plant community. Based on the field experimental evidence, our results highlight the adverse role soil biota can play on plant community responses to environmental stresses. These outcomes indicate that impacts of soil biota on the stability of plant communities subjected to drought are highly context-dependent and suggest that in some cases the soil biota activity can even destabilize plant community biomass responses to drought.

    https://doi.org/10.1007/s10021-022-00785-2
  • Journal of Ecology
    2022

    Temporal changes in plant soil feedback effects on microbial networks, leaf metabolomics and plant-insect interactions

    Martine Huberty, Katja Steinauer, Robin Heinen, R. Jongen, Young Hae Choi, T. Martijn Bezemer
    The importance of plant soil feedbacks (PSF) for above- and belowground multitrophic interactions is well recognized. However, most studies only condition soil for a short time before testing the feedback response. Here we investigate the influence of time of conditioning on soil microbiome composition, plant growth and metabolomics, and plant-insect interactions. We used soil collected from large outdoor mesocosms with monocultures of six species and investigated the temporal changes in the soil over a full year.
    Every two months we assessed the legacy effects of the soils on plant growth of one of the species (Jacobaea vulgaris) in a climate-controlled chamber. Each time we used tissue culture plants that were genetically identical. We also measured leaf herbivore performance and leaf metabolomes, as well as the abiotic and biotic soil properties.
    We show that the monoculture soils harboured different microbiomes, but that these varied over time. Growth of the test plants also varied over time and plants grew consistently less well in their own soil. The soil legacy effects on the leaf metabolome were less consistent and varied strongly over time. Networking analysis showed that soil bacteria had stronger effects on the leaf metabolome than fungi early on. However, after twelve months of conditioning only soil fungal community composition explained the metabolomic profiles of the leaves. Insect herbivory was not affected by soil conditioning, but decreased with increasing time of conditioning.
    Synthesis: Our results show that the biomass response of the test plants to soil conditioning remained consistent throughout the year, even though both the soil microbiome and leaf metabolomic responses to conditioned soil varied greatly over time. These soil-induced changes in the metabolome of plants over time can be an important driver of above-ground multitrophic interactions in nature. Our study demonstrates that the duration of conditioning has a strong impact on plant and soil properties, which highlights that temporal variation is an important aspect to consider in future studies investigating plant-soil interactions.
    https://doi.org/10.1111/1365-2745.13872
  • Plant and Soil
    2022

    Plant-litter-soil feedbacks in common grass species are slightly negative and only marginally modified by litter exposed to insect herbivory

    Jon De Long, Robin Heinen, Renske Jongen, Katja Steinauer, T. Martijn Bezemer

    Purpose: Insect herbivory affects plant growth, nutrient and secondary metabolite concentrations and litter quality. Changes to litter quality due to insect herbivory can alter decomposition, with knock on effects for plant growth mediated through the plant-litter-soil feedback pathway. Methods: Using a multi-phase glasshouse experiment, we tested how changes in shoot and root litter quality of fast- and slow-growing grass caused by insect herbivores affect the performance of response plants in the soil in which the litter decomposed. Results: We found that insect herbivory resulted in marginal changes to litter quality and did not affect growth when plants were grown with fast- versus slow-growing litter. Overall, presence of litter resulted in reduced root and shoot growth and this effect was significantly more negative in shoots versus roots. However, this effect was minimal, with a loss of c. 1.4% and 3.1% dry weight biomass in roots versus shoots, respectively. Further, shoot litter exposed to insect herbivory interacted with response plant identity to affect root growth. Conclusions: Our results suggest that whether litter originates from plant tissues exposed to insect herbivory or not and its interaction with fast- versus slow-growing grasses is of little importance, but species-specific responses to herbivory-conditioned litter can occur. Taken collectively, the overall role of the plant-litter-soil feedback pathway, as well as its interaction with insect herbivory, is unlikely to affect broader ecosystem processes in this system.

    https://doi.org/10.1007/s11104-022-05590-3
  • Plant and Soil
    2022

    Associational resistance to nematodes and its effects on interspecific interactions among grassland plants.

    Xiangyu Liu, Ciska Raaijmakers, Klaas Vrieling, Suzanne T. E. Lommen, T. Martijn Bezemer
    Aims
    Plants can influence the level of herbivory experienced by neighboring plants. The importance of such belowground associational effects are poorly understood. In this study we examine whether Jacobaea vulgaris provides associational resistance against nematodes to neighboring plants.

    Methods
    Thirteen species (6 forbs, 3 grasses and 4 legumes) were each grown in mixtures with J. vulgaris and in monocultures. A nematode community was introduced to half of the pots. After 12 weeks, plant dry mass was assessed for each individual plant in each pot, and the number of nematodes in the soil and roots were identified. We then examined for each plant species its performance in mixtures and in monocultures, in presence and absence of nematodes and analyzed the abundance and composition of nematodes.

    Results
    Forbs produced more, grasses similar, and legumes less biomass in mixtures with J. vulgaris than in monocultures. Nematode addition did not influence biomass. There were fewer root-feeding nematodes in the soil in mixtures than in monocultures, but this was only true for plants that were good hosts for nematodes. The community composition of soil nematodes was different in monocultures and mixtures. Densities of migratory endoparasitic nematodes in the roots of neighboring plants were lower in mixtures than in monocultures. Moreover, the presence of nematodes changed the outcome of plant-plant interactions, often in favor of J. vulgaris.

    Conclusions
    Jacobaea vulgaris provides belowground associational resistance to other plants against migratory endoparasitic nematodes, and the presence of nematodes can change the outcome of plant-plant interactions.
    https://doi.org/10.1007/s11104-021-05238-8
  • Trends in Plant Science
    2022

    Legacies at work: plant–soil–microbiome interactions underpinning agricultural sustainability

    Jiayi Jing, Wen-Feng Cong, T. Martijn Bezemer
    Agricultural intensification has had long-lasting negative legacies largely because of excessive inputs of agrochemicals (e.g., fertilizers) and simplification of cropping systems (e.g., continuous monocropping). Conventional agricultural management focuses on suppressing these negative legacies. However, there is now increasing attention for creating positive above- and belowground legacies through selecting crop species/genotypes, optimizing temporal and spatial crop combinations, improving nutrient inputs, developing intelligent fertilizers, and applying soil or microbiome inoculations. This can lead to enhanced yields and reduced pest and disease pressure in cropping systems, and can also mitigate greenhouse gas emissions and enhance carbon sequestration in soils. Strengthening positive legacies requires a deeper understanding of plant–soil–microbiome interactions and innovative crop, input, and soil management which can help to achieve agricultural sustainability.
    https://doi.org/10.1016/j.tplants.2022.05.007
  • Soil Biology & Biochemistry
    12-2021

    Plant community legacy effects on nutrient cycling, fungal decomposer communities and decomposition in a temperate grassland

    R. Jongen, Jon De Long, Robin Heinen, Martine Huberty, Katja Steinauer, T. Martijn Bezemer
    Soil legacies mediated by plant species-specific microbial communities are major drivers of plant community dynamics. Most soil legacy studies focus on the role of pathogens and mutualists in driving these processes, while much less is known about plant litter-mediated changes to the soil microbial community. Here, we used an existing plant-soil feedback field experiment in which plant communities with different growth strategies (i.e., fast versus slow) and different proportions of functional groups (i.e., grasses versus forbs) were allowed to condition the soil over contrasting temporal scales (i.e., one versus two years) in a natural grassland. In the feedback phase, we removed the existent plant community, and replaced it with a standardized response plant community. We then tested the legacy effects of these different soil conditioning treatments on decomposition processes, nutrient cycling and soil decomposer community composition. Soil legacy effects on decomposition and the soil decomposer community composition were most evident right after the start of the feedback phase, but disappeared soon after the new community established. The soil conditioning time and years since disturbance affected most of the soil functions consistently, while no strong effects of plant functional group and plant growth strategy were found. We conclude that after disturbance, it is recovery time, not soil legacy effects, that is the most important factor driving soil functions.
    https://doi.org/10.1016/j.soilbio.2021.108450
  • Ecological Research
    01-2021

    How plant-soil feedbacks influence the next generation of plants

    Jon De Long, Robin Heinen, R. Jongen, Martine Huberty, Anna Kielak, Katja Steinauer, T. Martijn Bezemer
    In response to environmental conditions, plants can alter the performance of the next generation through maternal effects. Since plant–soil feedbacks (PSFs) influence soil conditions, PSFs likely create such intergenerational effects. We grew monocultures of three grass and three forb species in outdoor mesocosms. We then grew one of the six species, Hypochaeris radicata, in the conditioned soils and collected their seeds. We measured seed weight, carbon and nitrogen concentration, germination and seedling performance when grown on a common soil. We did not detect functional group intergenerational effects, but soils conditioned by different plant species affected H. radicata seed C to N ratios. There was a relationship between parent biomass in the differently conditioned soils and the germination rates of the offspring. However, these effects did not change offspring performance on a common soil. Our findings show that PSF effects changed seed quality and initial performance in a common grassland forb. We discuss the implications of our findings for multi‐generational plant–soil interactions, and highlight the need to further explore how PSF effects shape plant community dynamics over different generations and across a broad range of species and functional groups.
    https://doi.org/10.1111/1440-1703.12165
  • Nature Communications
    2021

    Persistence of plant-mediated microbial soil legacy effects in soil and inside roots

    Robin Heinen, Martine Huberty, Katja Steinauer, Jon De Long, R. Jongen, T. Martijn Bezemer
    Plant-soil feedbacks are shaped by microbial legacies that plants leave in the soil. We tested the persistence of these legacies after subsequent colonization by the same or other plant species using 6 typical grassland plant species. Soil fungal legacies were detectable for months, but the current plant effect on fungi amplified in time. By contrast, in bacterial communities, legacies faded away rapidly and bacteria communities were influenced strongly by the current plant. However, both fungal and bacterial legacies were conserved inside the roots of the current plant species and their composition significantly correlated with plant growth. Hence, microbial soil legacies present at the time of plant establishment play a vital role in shaping plant growth even when these legacies have faded away in the soil due the growth of the current plant species. We conclude that soil microbiome legacies are reversible and versatile, but that they can create plant-soil feedbacks via altering the endophytic community acquired during early ontogeny.
    https://doi.org/10.1038/s41467-021-25971-z
  • Diversity and Distributions
    2021

    A matter of time: Recovery of plant species diversity in wild plant communities at declining nitrogen deposition

    Frank Berendse, R.H.E.M. Geerts, Wim Th. Elberse, T. Martijn Bezemer, P.W. Goedhart, Wei Xue, Erik Noordijk, Cajo J. F. ter Braak, H Korevaar
    Aim
    High levels of nitrogen deposition have been responsible for important losses of plant species diversity. It is often assumed that reduction of ammonia and nitrogen oxide emissions will result in the recovery of the former biodiversity. In Western Europe, N deposition peaked between 1980 and 1988 and declined thereafter. In a 60-year experiment in hay meadows, we tested the hypothesis that increasing and declining nitrogen deposition had negative, respectively, positive effects on plant species diversity.

    Location
    Wageningen, the Netherlands.

    Method
    Duplicated plots received different fertilization treatments from 1958 onwards (control, Ca, K, P, PK, N, NPK). Productivity, soil pH and species composition were measured at regular intervals. In the control plots, the correlations between N deposition, diversity, production and soil acidification were analysed. Subsequently, we tested whether the treatment effects (e.g. N addition and liming) confirmed the hypothesized interactions.

    Results
    In the control plots, soil pH, species diversity and the abundance of legumes and short forbs declined between 1958 and 1987 when atmospheric N deposition was high but recovered after 1987 when N deposition decreased. However, also in the N addition plots species diversity recovered partly after 1987, although the soil pH of the acidified soils in these plots did not. In addition, also in the limed plots diversity decreased rapidly during the first 30 years while in this treatment soil acidification was more than compensated.

    Main conclusions
    We conclude that declining N deposition resulted in the recovery of plant species diversity, but not in recovery of the former species composition. Time appears to be an additional, but crucial factor for the recovery of diverse, flowering meadows. Species not adapted to the new management conditions created at the start of the experiment disappeared during the first decades, while species fit for the new environment needed many years to establish.
    https://doi.org/10.1111/ddi.13266
  • Ecology and Evolution
    2021

    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.

    https://doi.org/10.1002/ece3.7167
  • Trends in Ecology and Evolution
    2021

    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.

    https://doi.org/10.1016/j.tree.2021.03.011
  • Journal of Animal Ecology
    2021

    Spatial patterns and ecological drivers of soil nematode β-diversity in natural grasslands vary among vegetation types and trophic position

    Dan Xiong, Cunzheng Wei, Xugao Wang, Xiaotao Lü, Shuai Fang, Yingbin Li, Xiao-Bo Wang, Wenju Liang, Xingguo Han, T. Martijn Bezemer, Qi Li
    Understanding biogeographic patterns of community assemblages is a core objective in ecology, but for soil communities these patterns are poorly understood. To understand the spatial patterns and underlying mechanisms of β-diversity in soil communities, we investigated the β-diversity of soil nematode communities along a 3,200-km transect across semi-arid and arid grasslands.
    Spatial turnover and nested-resultant are the two fundamental components of β-diversity, which have been attributed to various processes of community assembly. We calculated the spatial turnover and nested-resultant components of soil nematode β-diversity based on the β-partitioning framework. Distance matrices for the dissimilarity of soil nematode communities were computed using the ‘Sørensen’ method. We fitted negative exponential models to compare the distance decay patterns in nematode community similarity with geographic distance and plant community distance in three vegetation types (desert, desert steppe and typical steppe) and along the whole transect. Variation partitioning was used to distinguish the contribution of geographic distance and environmental variables to β-diversity and the partitioned components.
    Geographic distance and environmental filtering jointly drove the β-diversity patterns of nematode community, but environmental filtering explained more of the variation in β-diversity in the desert and typical steppe, whereas geographic distance was important in the desert steppe. Nematode community assembly was explained more by the spatial turnover component than by the nested-resultant component. For nematode feeding groups, the β-diversity in different vegetation types increased with geographic distance and plant community distance, but the nested-resultant component of bacterial feeders in the desert ecosystem decreased with geographic distance and plant community distance.
    Our findings show that spatial variation in soil nematode communities is regulated by environmental processes at the vegetation type scale, while spatial processes mainly work on the regional scale, and emphasize that the spatial patterns and drivers of nematode β-diversity differ among trophic levels. Our study provides insight into the ecological processes that maintain soil biodiversity and biogeographic patterns of soil community assemblage at large spatial scales.
    https://doi.org/10.1111/1365-2656.13461
  • Basic and Applied Ecology
    2021

    Exogenous application of plant defense hormones alters the effects of live soils on plant performance

    Jing Zhang, Klaas Vrieling, Peter G.L. Klinkhamer, T. Martijn Bezemer
    The overall effect of a live soil inoculum collected from nature on plant biomass is often negative. One hypothesis to explain this phenomenon is that the overall net pathogenic effect of soil microbial communities reduces plant performance. Induced plant defenses triggered by the application of the plant hormones jasmonic acid (JA) and salicylic acid (SA) may help to mitigate this pathogenic effect of live soil. However, little is known about how such hormonal application to the plant affects the soil and how this, in turn, impacts plant growth. We grew four plant species in sterilized and inoculated live soil and exposed their leaves to two hormonal treatments (JA and SA). Two species (Jacobaea vulgaris and Cirsium vulgare) were negatively affected by soil inoculation. In these two species foliar application of SA increased biomass in live soil but not in sterilized soil. Two other species (Trifolium repens and Daucus carota) were not affected by soil inoculum and for these two species foliar application of SA reduced plant biomass in both the sterilized and live soil. Application of JA reduced plant biomass in both soils for all species. We subsequently carried out a multiple generation experiment for one of the plant species, J. vulgaris. In each generation, the live soil was a mixture of 10% soil from the previous generation and 90% sterilized soil and the same hormonal treatments were applied. The negative effects of live soil on plant biomass were similar in all four generations, and this negative effect was mitigated by the application of SA. Our research suggests that the application of SA can mitigate the negative effects of live soil on plant growth. Although the inoculum of soil containing a natural live soil microbial community had a strong negative effect on the growth of J. vulgaris, we found no evidence for an increase or decrease in negative plant-soil feedback in either the control or the SA treated plants. Also plant performance did not decrease consistently with succeeding generations.
    https://doi.org/10.1016/j.baae.2021.07.011
  • New Phytologist
    2021

    Novel chemicals engender myriad invasion mechanisms

    [No Value] Inderjit, D. Simberloff, Harleen Kaur, Susan Kalisz, T. Martijn Bezemer
    Non-native invasive species (NIS) release chemicals into the environment that are unique to the invaded communities, defined as novel chemicals. Novel chemicals impact competitors, soil microbial communities, mutualists, plant enemies, and soil nutrients differently than in the species’ native range. Ecological functions of novel chemicals and differences in functions between the native and non-native ranges of NIS are of immense interest to ecologists. Novel chemicals can mediate different ecological, physiological, and evolutionary mechanisms underlying invasion hypotheses. Interactions amongst the NIS and resident species including competitors, soil microbes, and plant enemies, as well as abiotic factors in the invaded community are linked to novel chemicals. However, we poorly understand how these interactions might enhance NIS performance. New empirical data and analyses of how novel chemicals act in the invaded community will fill major gaps in our understanding of the chemistry of biological invasions. A novel chemical-invasion mechanism framework shows how novel chemicals engender invasion mechanisms beyond plant–plant or plant–microorganism interactions.
    https://doi.org/10.1111/nph.17685
  • Animal Microbiome
    07-10-2020

    Microbiomes of a specialist caterpillar are consistent across different habitats but also resemble the local soil microbial communities

    Sofia I. Fernandes Gomes, Anna Kielak, Robin Heinen, R. Jongen, Ivor Keesmaat, Jon De Long, T. Martijn Bezemer
    Background
    Insect-associated microorganisms can provide a wide range of benefits to their host, but insect dependency on these microbes varies greatly. The origin and functionality of insect microbiomes is not well understood. Many caterpillars can harbor symbionts in their gut that impact host metabolism, nutrient uptake and pathogen protection. Despite our lack of knowledge on the ecological factors driving microbiome assemblages of wild caterpillars, they seem to be highly variable and influenced by diet and environment. Several recent studies have shown that shoot-feeding caterpillars acquire part of their microbiome from the soil. Here, we examine microbiomes of a monophagous caterpillar (Tyria jacobaeae) collected from their natural host plant (Jacobaea vulgaris) growing in three different environments: coastal dunes, natural inland grasslands and riverine grasslands, and compare the bacterial communities of the wild caterpillars to those of soil samples collected from underneath each of the host plants from which the caterpillars were collected.

    Results
    The microbiomes of the caterpillars were dominated by Proteobacteria, Actinobacteria, Firmicutes and Bacteroidetes. Only 5% of the total bacterial diversity represented 86.2% of the total caterpillar’s microbiome. Interestingly, we found a high consistency of dominant bacteria within the family Burkholderiaceae in all caterpillar samples across the three habitats. There was one amplicon sequence variant belonging to the genus Ralstonia that represented on average 53% of total community composition across all caterpillars. On average, one quarter of the caterpillar microbiome was shared with the soil.

    Conclusions
    We found that the monophagous caterpillars collected from fields located more than 100 km apart were all dominated by a single Ralstonia. The remainder of the bacterial communities that were present resembled the local microbial communities in the soil in which the host plant was growing. Our findings provide an example of a caterpillar that has just a few key associated bacteria, but that also contains a community of low abundant bacteria characteristic of soil communities.
    https://doi.org/10.1186/s42523-020-00055-3
  • Journal of Chemical Ecology
    08-2020

    Soil inoculation alters leaf metabolic profiles in genetically identical plants

    Martine Huberty, B. Martis, J. van Kampen, Young Hae Choi, Klaas Vrieling, Peter G.L. Klinkhamer, T. Martijn Bezemer
    Abiotic and biotic properties of soil can influence growth and chemical composition of plants. Although it is well-known that soil microbial composition can vary greatly spatially, how this variation affects plant chemical composition is poorly understood. We grew genetically identical Jacobaea vulgaris in sterilized soil inoculated with live soil collected from four natural grasslands and in 100% sterilized soil. Within each grassland we sampled eight plots, totalling 32 different inocula. Two samples per plot were collected, leading to three levels of spatial variation: within plot, between and within grasslands. The leaf metabolome was analysed with 1H Nuclear magnetic resonance spectroscopy (NMR) to investigate if inoculation altered the metabolome of plants and how this varied between and within grasslands. Inoculation led to changes in metabolomics profiles of J. vulgaris in two out of four sites. Plants grown in sterilized and inoculated soils differed in concentrations of malic acid, tyrosine, trehalose and two pyrrolizidine alkaloids (PA). Metabolomes of plants grown in inoculated soils from different sites varied in glucose, malic acid, trehalose, tyrosine and in one PA. The metabolome of plants grown in soils with inocula from the same site was more similar than with inocula from distant sites. We show that soil influences leaf metabolomes. Performance of aboveground insects often depends on chemical composition of plants. Hence our results imply that soil microbial communities, via affecting aboveground plant metabolomes, can impact aboveground plant-insect food chains but that it is difficult to make general predictions due to spatial variation in soil microbiomes.
    https://doi.org/10.1007/s10886-020-01156-8
  • Nature Ecology and Evolution
    01-02-2020

    International scientists formulate a roadmap for insect conservation and recovery

    Jeff A. Harvey, Robin Heinen, Inge Armbrecht, Yves Basset, James H Baxter-Gilbert, T. Martijn Bezemer, Monika Böhm, Riccardo Bommarco, Paulo A V Borges, Pedro Cardoso, Viola Clausnitzer, Tara Cornelisse, Elizabeth E Crone, Marcel Dicke, Klaas-Douwe B Dijkstra, Lee A. Dyer, Jacintha Ellers, Thomas Fartmann, Matthew L. Forister, Michael J Furlong, Andres Garcia-Aguayo, Justin Gerlach, Rieta Gols, Dave Goulson, Jan-Christian Habel, Nick M Haddad, Caspar A Hallmann, Sérgio Henriques, Marie E Herberstein, Axel Hochkirch, Alice C Hughes, Sarina Jepsen, T Hefin Jones, Bora M Kaydan, David Kleijn, Alexandra-Maria Klein, Tanya Latty, Simon R Leather, Sara M Lewis, Bradford C Lister, John E Losey, Elizabeth C Lowe, Craig R Macadam, James Montoya-Lerma, Christopher D Nagano, Sophie Ogan, Michael C Orr, Christina J Painting, Thai-Hong Pham, Simon G. Potts, Aunu Rauf, Tomas L. Roslin, Michael J Samways, Francisco Sanchez-Bayo, Sim A Sar, Cheryl B Schultz, António O Soares, Anchana Thancharoen, Teja Tscharntke, Jason M. Tylianakis, Kate D L Umbers, Louise E.M. Vet, Marcel E. Visser, Ante Vujic, David L Wagner, Michiel F. WallisDeVries, Catrin Westphal, Thomas E White, Vicky L Wilkins, Paul H Williams, Kris A G Wyckhuys, Zeng-Rong Zhu, Hans de Kroon
    https://doi.org/10.1038/s41559-019-1079-8
  • New Phytologist
    2020

    Conditioning the soil microbiome through plant-soil feedbacks suppresses an aboveground insect pest

    Ana Pineda, Ian Kaplan, Wadih Ghanem, T. Martijn Bezemer
    •Soils and their microbiomes are now recognized as key components of plant health, but how to steer those microbiomes to obtain their beneficial functions is still unknown. Here, we assess whether plant‐soil feedbacks can be applied in a crop system to shape soil microbiomes that suppress herbivorous insects in aboveground tissues.

    •We used four grass and four forb species to condition living soil. Then we inoculated those soil microbiomes into sterilized soil and grew chrysanthemum as a focal plant. We evaluated the soil microbiome in the inocula and after chrysanthemum growth, as well as plant and herbivore parameters.

    •We show that inocula and inoculated soil in which a focal plant had grown harbor remarkably different microbiomes, with the focal plant exerting a strong negative effect on fungi, especially arbuscular mycorrhizal fungi. Soil inoculation consistently induced resistance against the thrips Frankliniella occidentalis, but not against the mite Tetranychus urticae, when compared with sterilized soil. Additionally, plant species shaped distinct microbiomes that had different effects on thrips, chlorogenic acid levels in leaves and plant growth.

    •This study provides a proof‐of‐concept that the plant‐soil feedback concept can be applied to steer soil microbiomes with the goal of inducing resistance aboveground against herbivorous insects.
    https://doi.org/10.1111/nph.16385
  • Frontiers in Ecology and Evolution
    2020

    Editorial: The Next Step: Disentangling the Role of Plant-Soil Feedbacks in Plant Performance and Species Coexistence Under Natural Conditions

    Johannes Heinze, T. Martijn Bezemer, Jasmin Joshi
    Effects of plant-induced changes in soil properties, which impact subsequent plant growth, have received increasing attention in plant ecology (e.g., Smith-Ramesh & Reynolds 2017). These plant-soil feedbacks (PSFs) are considered to be important for plant performance and plant-community composition in many terrestrial ecosystems (e.g., van der Putten et al. 2013). However, so far most conclusions on the importance of PSFs in natural systems have been drawn from experiments performed under highly controlled and artificial conditions. Under natural conditions, the growth and development of plants as well as that of soil organisms is influenced by many more abiotic and biotic interactions than in the greenhouse. Hence, there is an urgent need to investigate PSFs under more natural conditions and to better understand the interactions between PSFs and environmental drivers (De Long et al. 2019). This Research Topic comprises 14 articles - ranging from Original research articles, meta-analytical Reviews and Perspectives - that aim to advance our understanding of the contribution of PSFs to plant growth and plant community composition in different environmental contexts.
    https://doi.org/10.3389/fevo.2020.00231
  • Ecology Letters
    2020

    Plant community composition steers grassland vegetation via soil legacy effects

    Robin Heinen, Jon De Long, Martine Huberty, R. Jongen, Anna Kielak, Katja Steinauer, Feng Zhu, T. Martijn Bezemer
    Soil legacy effects are commonly highlighted as drivers of plant community dynamics and species co‐existence. However, experimental evidence for soil legacy effects of conditioning plant communities on responding plant communities under natural conditions is lacking. We conditioned 192 grassland plots using six different plant communities with different ratios of grasses and forbs and for different durations. Soil microbial legacies were evident for soil fungi, but not for soil bacteria, while soil abiotic parameters did not significantly change in response to conditioning. The soil legacies affected the composition of the succeeding vegetation. Plant communities with different ratios of grasses and forbs left soil legacies that negatively affected succeeding plants of the same functional type. We conclude that fungal‐mediated soil legacy effects play a significant role in vegetation assembly of natural plant communities.
    https://doi.org/10.1111/ele.13497
  • Environmental Microbiology
    2020

    Structure and ecological function of the soil microbiome affecting plant-soil feedbacks in the presence of a soil-borne pathogen

    Haikun Ma, Juan Esteban Perez Jaramillo, Ana Pineda, T. Martijn Bezemer
    Interactions between plants and soil microbes are important for plant growth and resistance. Through plant–soil‐feedbacks, growth of a plant is influenced by the previous plant that was growing in the same soil. We performed a plant–soil feedback study with 37 grass, forb and legume species, to condition the soil and then tested the effects of plant‐induced changes in soil microbiomes on the growth of the commercially important cut‐flower Chrysanthemum in presence and absence of a pathogen. We analysed the fungal and bacterial communities in these soils using next‐generation sequencing and examined their relationship with plant growth in inoculated soils with or without the root pathogen, Pythium ultimum. We show that a large part of the soil microbiome is plant species‐specific while a smaller part is conserved at the plant family level. We further identified clusters of plant species creating plant growth promoting microbiomes that suppress concomitantly plant pathogens. Especially soil inocula with higher relative abundances of arbuscular mycorrhizal fungi caused positive effects on the Chrysanthemum growth when exposed to the pathogen. We conclude that plants differ greatly in how they influence the soil microbiome and that plant growth and protection against pathogens is associated with a complex soil microbial community.
    https://doi.org/10.1111/1462-2920.14882
  • Plant and Soil
    2020

    Soil inoculation alters the endosphere microbiome of chrysanthemum roots and leaves

    Nurmi Pangesti, Ana Pineda, T. Martijn Bezemer
    Aims
    This study examines how inoculation with live soil influences the assembly of the endosphere microbiome of leaves and roots of chrysanthemum.

    Methods
    Sterilized soil was inoculated with 10% soil in which grasses had grown. Chrysanthemum was planted in these soils and control plants were grown in 100% sterilized soil. All plants were exposed to thrips, and leaves and roots were collected from inoculated and control plants that experienced high and low thrips damage. DNA was extracted and the bacterial and fungal community inside roots and leaves was determined using Illumina sequencing.

    Results
    Inoculation increased bacterial diversity in root but not in leaf tissues. The endosphere of both roots and leaves was dominated by Pseudomonadaceae. In leaves, the relative abundance of Pseudomonadaceae was higher in inoculated than in control plants, whereas this was opposite in roots. Leaves contained more rare bacterial families than roots. The number of fungal reads was very low and the endopshere did not differ between plants with high or low thrips damage.

    Conclusions
    Bacterial communities inside chrysanthemum root and leaf tissues differ considerably. Soil inoculation with entire microbiomes can be used to change root and foliar bacterial microbiomes and this is particularly effective in root tissues.
    https://doi.org/10.1007/s11104-020-04655-5
  • ISME Journal
    2020

    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.
    https://doi.org/10.1038/s41396-020-0695-2
  • Ecosphere
    2020

    Above-belowground linkages of functionally dissimilar plant communities and soil properties in a grassland experiment

    Katja Steinauer, Robin Heinen, Jon De Long, Martine Huberty, R. Jongen, Minggang Wang, T. Martijn Bezemer
    Changes in plant community composition can have long‐lasting consequences for ecosystem functioning. However, how the duration of plant growth of functionally distinct grassland plant communities influences abiotic and biotic soil properties and thus ecosystem functions is poorly known. In a field experiment, we established identical experimental subplots in two successive years comprising of fast‐ or slow‐growing grass and forb community mixtures with different forb:grass ratios. After one and two years of plant growth, we measured above‐ and belowground biomass, soil abiotic characteristics (pH, organic matter, soil nutrients), soil microbial properties (respiration, biomass, community composition), and nematode abundance. Fast‐ and slow‐growing plant communities did not differ in above‐ and belowground biomass. However, fast‐ and slow‐growing plant communities created distinct soil bacterial communities, whereas soil fungal communities differed most in 100% forb communities compared to other forb:grass ratio mixtures. Moreover, soil nitrate availability was higher after two years of plant growth, whereas the opposite was true for soil ammonium concentrations. Furthermore, total nematodes and especially bacterial‐feeding nematodes were more abundant after two years of plant growth. Our results show that plant community composition is a driving factor in soil microbial community assembly and that the duration of plant growth plays a crucial role in the establishment of plant community and functional group composition effects on abiotic and biotic soil ecosystem functioning under natural field conditions.
    https://doi.org/10.1002/ecs2.3246
  • Urban Ecosystems
    2020

    Shading enhances plant species richness and diversity on an extensive green roof

    Henk-Jan van der Kolk, Petra van den Berg, Gerard Korthals, T. Martijn Bezemer
    Green roofs can promote biodiversity in urban areas. The extent to which green roofs stimulate plant diversity can depend on roof characteristics such as roof age, substrate depth and shading. We exploratively studied the vegetation on a Dutch green roof in 50 permanent plots (1 m2) over eight years (2012–2019) following roof construction. Plots were situated either on low substrate depth (6 cm light-weight extensive substrate) or high substrate depth (6 cm light-weight extensive substrate topped with 14 cm native soil) and differed in the amount of shading received from a higher building floor. Increased substrate depth and shading additively increased plant species richness and plant diversity, with high shaded plots supporting on average 6.4 more plant species than low unshaded plots. Shading likely acts via reducing drought stress, whereas increasing substrate depth with native soil may also enhance plant diversity via addition of nutrients and native seeds. The vegetation composition on the roof was dynamic and changed over the years. Sedum acre was initially dominant but disappeared within the first years, whereas Sedum kamtschaticum increased and became dominant in the last years. Trifolium arvense was the most abundant forb species and was especially dominant three years after roof construction. We conclude that increased substrate depth and shading can promote plant species richness and diversity and recommend that both aspects are considered when green roofs are designed. Shading can be achieved by a stepped building architecture and by placing structures on the roof itself, such as solar panels on standards.
    https://doi.org/10.1007/s11252-020-00980-w
  • Applied Soil Ecology
    2020

    Steering root microbiomes of a commercial horticultural crop with plant-soil feedbacks

    Haikun Ma, Ana Pineda, Anna Kielak, Syahida Nindya Setyarini, T. Martijn Bezemer
    Plant-soil feedbacks (PSFs) can influence plant performance in natural and agricultural systems but how PSF principles can be applied in agriculture is not well-studied.

    In a two-phase PSF experiment, we tested how inoculating soil conditioned by plants into live and sterilized commercial glasshouse soil influences the root-associated microbiome (bacteria and fungi) and biomass of the cut flower chrysanthemum. The conditioned soil inocula were obtained by growing eight grassland species and chrysanthemum individually in soil collected from a commercial chrysanthemum glasshouse, or in soil from a natural grassland.

    Inoculation of conditioned grassland soil into sterilized glasshouse soil led to higher plant biomass, to more complex and connected microbial networks and to a lower abundance of the pathogenic fungi Olpidium in chrysanthemum roots, than inoculation into live glasshouse soil or inoculation with conditioned live glasshouse soil. Biomass of chrysanthemum was highest in 100% sterilized soil, but in this soil the root-associated microbiome also contained the highest relative abundance of Olpidium.

    Glasshouse soils are frequently steam-sterilized and our results show that inoculating these soils with desired soil microbiomes can steer the root microbiome in this crop. However, our study also highlights that steering live glasshouse soil with a disease-related microbiome into a healthy state remains challenging.
    https://doi.org/10.1016/j.apsoil.2019.103468
  • Journal of Ecology
    2020

    Aboveground plant metabolomic responses to plant-soil feedbacks and herbivory

    Martine Huberty, Young Hae Choi, Robin Heinen, T. Martijn Bezemer
    Understanding the causes of variation in foliar plant metabolomes is essential for
    our understanding of ecological interactions between plants and other organisms.
    It is well-accepted that foliar herbivory alters metabolites in leaves. However, soil
    (micro)organisms can also induce such changes.
    2. We generated plant-specific soil legacies by growing 12 plant species individually
    in a common starting soil. Then we planted all plant species in all soils and exposed
    a subset to foliar herbivory. We then used 1
    H nuclear magnetic resonance to analyse the shoot metabolomes of all responding plants.
    3. Above-ground herbivory and soil legacies altered shoot metabolomes. In most
    plant species, soil legacy more strongly affected shoot metabolomes than foliar
    herbivory.
    4. Synthesis. Our results show that plant-induced changes in soil alter metabolomes
    of plants that grow later in those soils. Such below-ground legacy effects can have
    far-stretching consequences for above-ground multitrophic interactions as these
    often depend on the plant chemical composition. Recently, plant–soil feedbacks
    have received considerable attention in ecological studies, and our study now
    highlights that these feedbacks can be an important determinant of the often unexplained intraspecific variation in chemical composition among plants.
    https://doi.org/10.1111/1365-2745.13394
  • Soil Biology & Biochemistry
    2020

    ‘Home’ and ‘away’ litter decomposition depends on the size fractions of the soil biotic community

    Yingbin Li, Ciska Veen, (Gera) W.H.G. Hol, Simon Vandenbrande, Freddy ten Hooven, Qi Li, Wenju Liang, T. Martijn Bezemer
    The ‘home-field advantage’ (HFA) hypothesis predicts that litter decomposition is accelerated in its home environment (i.e. in conspecific soil). Soil organisms play a key role in driving such HFA effects. Soil biota have a large range of body sizes, referred to as size fractions, which may influence their roles in the decomposition process and in the generation of HFA effects. However, how HFA effects depend on the different size fractions of the soil biotic community is unknown. We conducted a microcosm decomposition experiment to examine how size fractions of the soil biotic community affected litter decomposition and HFA effects. In a semi-natural grassland in the Netherlands, we collected leaf litter and soil from two abundant forbs: Tanacetum vulgare and Jacobaea vulgaris. Watery extracts of the soils were sieved through differently-meshed sieves (ranging from 850 μm to 6 μm) to obtain soil communities of different size fractions. Microcosms were inoculated with these different size fractions of the soil biotic community and we examined their effects on microbial composition, litter mass loss and HFA effects. Three months after inoculation, the diversity of the fungal community in the inoculated pots decreased with decreasing size fractions of the soil biotic community. Similarly, litter mass loss also decreased with decreasing soil biotic community size. In contrast, the HFA effect increased with decreasing size fractions of the soil biotic community, but these differences disappeared after six months of decomposition. Our results indicate that soil microorganisms, mainly the smallest size fractions, are specialized to decompose specific resources and thus promote HFA effects, but that their effect is only apparent during specific stages of litter decomposition.
    https://doi.org/10.1016/j.soilbio.2020.107783
  • Arthropod-Plant Interactions
    2020

    Exogenous application of plant hormones in the field alters aboveground plant–insect responses and belowground nutrient availability, but does not lead to differences in plant–soil feedbacks

    Robin Heinen, Katja Steinauer, Jon De Long, R. Jongen, Arjen Biere, Jeff A. Harvey, T. Martijn Bezemer
    Plant–soil feedbacks of plants that are exposed to herbivory have been shown to differ from those of plants that are not exposed to herbivores. Likely, this process is mediated by jasmonic acid (JA) and salicylic acid (SA) defense pathways, which are induced by aboveground herbivory. Furthermore, exogenous application of these phytohormones to plants alters belowground communities, but whether this changes plant–soil feedbacks in natural systems is unknown. We applied exogenous sprays of JA and SA individually and in combination to field plots in a restored grassland. Control plots were sprayed with demineralized water. After three repeated application rounds, we transplanted seedlings of the plant–soil feedback model plant Jacobaea vulgaris as phytometer plants to test the effects of potential phytohormone-mediated changes in the soil, on plant performance during the response phase. We further measured how exogenous application of phytohormones altered plant-related ecosystem characteristics (plot-level); soil chemistry, plot productivity, insect communities and predation. Biomass of the phytometer plants only co-varied with plot productivity, but was not influenced by phytohormone applications. However, we did observe compound-specific effects of SA application on insect communities, most notably on parasitoid attraction, and of JA application on soil nitrogen levels. Although we did not find effects on plant–soil feedbacks, the effects of exogenous application of phytohormones did alter other ecosystem-level processes related to soil nutrient cycling, which may lead to legacy effects in the longer term. Furthermore, exogenous application of phytohormones led to altered attraction of specific insect groups.
    https://doi.org/10.1007/s11829-020-09775-4
  • Soil Biology & Biochemistry
    2019

    Changes in litter quality induced by N deposition alter soil microbial communities

    Yingbin Li, T. Martijn Bezemer, Junjie Yang, Xiaotao Lü, Xinyu Li, Wenju Liang, Xingguo Han, Qi Li
    Soil microbial community composition and litter quality are important drivers of litter decomposition, but how litter quality influences the soil microbial composition largely remains unknown. We conducted a microcosm experiment to examine the effects of changes in litter quality induced by long-term N deposition on soil microbial community composition. Mixed-species litter and single-species litter were collected from a field experiment with replicate plots exposed to long-term N-addition in a semiarid grassland in northern China. The litters were decomposed in a standard live soil after which the composition of the microbial community was determined by Illumina MiSeq Sequencing. Changes in litter stoichiometry induced by N-addition increased the diversity of the fungal community. The alpha-diversity of the fungal community was more sensitive to the type of litter (mixed- or single-species) than to the N-addition effects, with higher abundance of fungal OTUs and Shannon-diversity observed in soil with mixed-species litter. Moreover, the relative abundance of saprophytic fungi increased with increasing N-addition rates, which suggests that fungi play an important role in the initial stages of the decomposition process. Litter type and N addition did not significantly change the diversity of bacterial community. The relative abundance of ammonia-oxidizing bacteria was lower in high N-addition treatments than in those with lower N input, indicating that changes in litter stoichiometry could change ecosystem functioning via its effects on bacteria. Our results presented robust evidence for the plant-mediated pathways through which N-deposition affects the soil microbial community and biogeochemical cycling.
    https://doi.org/10.1016/j.soilbio.2018.11.025
  • Oecologia
    2019

    The relative importance of plant-soil feedbacks for plant-species performance increases with decreasing intensity of herbivory

    Johannes Heinze, N.K. Simons, S. Seibold, A Wacker, G Weithoff, M.M. Gossner, Daniel Prati, T. Martijn Bezemer, Jasmin Joshi
    Under natural conditions, aboveground herbivory and plant-soil feedbacks (PSFs) are omnipresent interactions strongly affecting individual plant performance. While recent research revealed that aboveground insect herbivory generally impacts the outcome of PSFs, no study tested to what extent the intensity of herbivory affects the outcome. This, however, is essential to estimate the contribution of PSFs to plant performance under natural conditions in the field. Here, we tested PSF effects both with and without exposure to aboveground herbivory for four common grass species in nine grasslands that formed a gradient of aboveground invertebrate herbivory. Without aboveground herbivores, PSFs for each of the four grass species were similar in each of the nine grasslands—both in direction and in magnitude. In the presence of herbivores, however, the PSFs differed from those measured under herbivory exclusion, and depended on the intensity of herbivory. At low levels of herbivory, PSFs were similar in the presence and absence of herbivores, but differed at high herbivory levels. While PSFs without herbivores remained similar along the gradient of herbivory intensity, increasing herbivory intensity mostly resulted in neutral PSFs in the presence of herbivores. This suggests that the relative importance of PSFs for plant-species performance in grassland communities decreases with increasing intensity of herbivory. Hence, PSFs might be more important for plant performance in ecosystems with low herbivore pressure than in ecosystems with large impacts of insect herbivores.
    https://doi.org/10.1007/s00442-019-04442-9
  • mBio
    2019

    Time after time: Temporal variation in the effects of grass and forb species on soil bacterial and fungal communities

    Anna Kielak, Katja Steinauer, Martine Huberty, R. Jongen, Jon De Long, Robin Heinen, T. Martijn Bezemer
    Microorganisms are found everywhere and have critical roles in most ecosystems, but compared to plants and animals, little is known about their temporal dynamics. Here, we investigated the temporal stability of bacterial and fungal communities in the soil and how their temporal variation varies between grasses and forb species. We established 30 outdoor mesocosms consisting of six plant monocultures and followed microbial communities for an entire year in these soils. We demonstrate that bacterial communities vary greatly over time and that turnover plays an important role in shaping microbial communities. We further show that bacterial communities rapidly shift from one state to another and that this is related to changes in the relative contribution of certain taxa rather than to extinction. Fungal soil communities are more stable over time, and a large part of the variation can be explained by plant species and by whether they are grasses or forbs. Our findings show that the soil bacterial community is shaped by time, while plant group and plant species-specific effects drive soil fungal communities. This has important implications for plant-soil research and highlights that temporal dynamics of soil communities cannot be ignored in studies on plant-soil feedback and microbial community composition and function.

    IMPORTANCE Our findings highlight how soil fungal and bacterial communities respond to time, season, and plant species identity. We found that succession shapes the soil bacterial community, while plant species and the type of plant species that grows in the soil drive the assembly of soil fungal communities. Future research on the effects of plants on soil microbes should take into consideration the relative roles of both time and plant growth on creating soil legacies that impact future plants growing in the soil. Understanding the temporal (in)stability of microbial communities in soils will be crucial for predicting soil microbial composition and functioning, especially as plant species compositions will shift with global climatic changes and land-use alterations. As fungal and bacterial communities respond to different environmental cues, our study also highlights that the selection of study organisms to answer specific ecological questions is not trivial and that the timing of sampling can greatly affect the conclusions made from these studies.
    https://doi.org/10.1128/mBio.02635-19
  • Ecology Letters
    2019

    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.
    https://doi.org/10.1111/ele.13271
  • New Phytologist
    2019

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

    Minggang Wang, Weibin Ruan, Olga Kostenko, Sabrina Almeida de Carvalho, 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.
    https://doi.org/10.1111/nph.15485
  • Basic and Applied Ecology
    2019

    Taking plant-soil feedbacks to the field in a temperate grassland

    Jon De Long, Robin Heinen, Katja Steinauer, Martine Huberty, R. Jongen, Simon Vandenbrande, Minggang Wang, Feng Zhu, T. Martijn Bezemer
    Plant–soil feedbacks (PSFs) involve changes to the soil wrought by plants, which change biotic and abiotic properties of the soil, affecting plants that grow in the soil at a later time. The importance of PSFs for understanding ecosystem functioning has been the focus of much recent research, for example, in predicting the consequences for agricultural production, biodiversity conservation, and plant population dynamics. Here, we describe an experiment designed to test PSFs left by plants with contrasting traits under field conditions. This is one of the first, large-scale field experiments of its kind. We removed the existent plant community and replaced it with target plant communities that conditioned the soil. These communities consisted of contrasting proportions of grass and forb cover and consisted of either fast- or slow-growing plants, in accordance with the plant economics spectrum. We chose this well-established paradigm because plants on opposite ends of this spectrum have developed contrasting strategies to cope with environmental conditions. This means they differ in their feedbacks with soil abiotic and biotic factors. The experimental procedure was repeated in two successive years in two different subplots in order to investigate temporal effects on soils that were conditioned by the same plant community. Our treatments were successful in creating plant communities that differed in their total percentage cover based on temporal conditioning, percentage of grasses versus forbs, and percentage of fast- versus slow-growing plants. As a result, we expect that the influence of these different plant communities will lead to different PSFs. The unique and novel design of this experiment allows us to simultaneously test for the impacts of temporal effects, plant community composition and plant growth strategy on PSFs. Here, we describe the experimental design and demonstrate why this effective design is ideal to advance our understanding of PSFs in the field.
    https://doi.org/10.1016/j.baae.2019.08.001
  • Nature Communications
    2019

    Foliar-feeding insects acquire microbiomes from the soil rather than the host plant

    Feng Zhu, Robin Heinen, T. Martijn Bezemer
    Microbiomes of soils and plants are linked, but how this affects microbiomes of aboveground herbivorous insects is unknown. We first generated plant-conditioned soils in field plots, then reared leaf-feeding caterpillars on dandelion grown in these soils, and then assessed whether the microbiomes of the caterpillars were attributed to the conditioned soil microbiomes or the dandelion microbiome. Microbiomes of caterpillars kept on intact plants differed from those of caterpillars fed detached leaves collected from plants growing in the same soil. Microbiomes of caterpillars reared on detached leaves were relatively simple and resembled leaf microbiomes, while those of caterpillars from intact plants were more diverse and resembled soil microbiomes. Plant-mediated changes in soil microbiomes were not reflected in the phytobiome but were detected in caterpillar microbiomes, however, only when kept on intact plants. Our results imply that insect microbiomes depend on soil microbiomes, and that effects of plants on soil microbiomes can be transmitted to aboveground insects feeding later on other plants.
    https://doi.org/10.1038/s41467-019-09284-w
  • Trends in Ecology and Evolution
    2018

    Plant-Soil Feedback: Bridging Natural and Agricultural Sciences

    P. Mariotte, Z. Mehrabi, T. Martijn Bezemer, Gerlinde De Deyn, A. Kulmatiski, Barbara Drigo, Marcel G. A. van der Heijden, Ciska Veen, Paul Kardol
    PSF has been extensively studied in both agricultural and natural systems, with increased activity in recent years, but a framework for integrating the concepts and principles developed in these systems is lacking.

    Interactions between soil biota and plant leaf and root traits have become an important tool in understanding PSF in wild plants, but this understanding has not yet been utilized in agricultural crop rotations.

    Soil inoculations with microbial strains are increasingly being used for steering the soil microbiome in agriculture but might also offer a promising method of restoration of degraded systems, and for controlling the spread of invasive species.

    Increasing evidence shows that PSF can play important roles in mediating ecosystem responses to forecasted climate change and extreme weather events.

    In agricultural and natural systems researchers have demonstrated large effects of plant–soil feedback (PSF) on plant growth. However, the concepts and approaches used in these two types of systems have developed, for the most part, independently. Here, we present a conceptual framework that integrates knowledge and approaches from these two contrasting systems. We use this integrated framework to demonstrate (i) how knowledge from complex natural systems can be used to increase agricultural resource-use efficiency and productivity and (ii) how research in agricultural systems can be used to test hypotheses and approaches developed in natural systems. Using this framework, we discuss avenues for new research toward an ecologically sustainable and climate-smart future.
    https://doi.org/10.1016/j.tree.2017.11.005
  • Journal of Plant Ecology
    2018

    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
    Aims
    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.
    Methods
    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.
    https://doi.org/10.1093/jpe/rtx043
  • Functional Ecology
    2018

    Plant community evenness responds to spatial plant-soil feedback heterogeneity primarily through the diversity of soil conditioning

    1.Plant-soil feedback (PSF) has been identified as a key driver of local plant diversity and evenness in competitive communities. However, while it has been shown that spatial PSF heterogeneity can alter plant performance and competitive interactions, there is no proof of principle that spatial PSF heterogeneity enhances community diversity.

    2.Using a grassland model system we separated two aspects of spatial heterogeneity: the number of species conditioning the soil and spatial distribution of the PSFs.

    3.Our data show that PSFs promoted a higher plant evenness when the soil was conditioned by multiple species (mixed-conditioned), then when the soil was conditioned by a single species (mono-conditioned). On mono-conditioned soils, heterospecifics typically outperformed the focal species. In addition, there was a trend for increasing community evenness from uniform, via fine-grained to coarse-grained mixed-conditioned soils, but this was not significant.

    4.On mixed-conditioned soils, performance of all competing species was intermediate to the best and the worst mono-conditioned soils, leading to higher community evenness.

    5.Our data demonstrate that PSFs play a role in promoting plant evenness. Across mono-conditioned soils, PSF led to altered competitive hierarchies. However, on soils conditioned by multiple species, competitive ability among species was more similar and this led to higher plant evenness. The spatial distribution of the heterogeneity, on the other hand, did not significantly affect plant evenness. Our data therefore show that community evenness was more strongly related to the number of plant species that conditioned the soil than the spatial distribution of the PSF heterogeneity. Future studies need to investigate the importance of PSFs in the field across plant life-stages and multiple generations.
    https://doi.org/10.1111/1365-2435.13017
  • Plant and Soil
    2018

    Synergistic and antagonistic effects of mixing monospecific soils on plant-soil feedbacks

    Haikun Ma, Ana Pineda, Andre W. G. van der Wurff, T. Martijn Bezemer
    Background and aims
    Plants influence the soil they grow in, and this can alter the performance of other, later growing plants in the same soil. This is called plant-soil feedback and is usually tested with monospecific soils, i.e. soils that are conditioned by one plant species. Here, we test if plant-soil feedbacks of inocula consisting of mixtures of monospecific soils can be predicted from the effects of the component inocula.

    Methods
    Chrysanthemum plants were grown in sterile soil inoculated with eight monospecific conditioned soils and with mixtures consisting of all pairwise combinations. Plant biomass and leaf yellowness were measured and the additivity was calculated.

    Results
    On average, plant biomass in the mixed inocula was slightly but significantly (6%) lower than predicted. In contrast, when growing in mixed inocula, plants showed 38% less disease symptoms than predicted. Moreover, the larger the difference between the effects of the two monospecific soils on plant growth, the higher the observed effect in the mixture exceeded the predicted effects.

    Conclusions
    We show that mixed monospecific soils interact antagonistically in terms of plant growth, but synergistically for disease symptoms. Our study further advances our understanding of plant-soil feedbacks, and suggests that mixing soils can be a powerful tool to steer soil microbiomes to improve plant-soil feedback effects.
    https://doi.org/10.1007/s11104-018-3694-6
  • Journal of Ecology
    2018

    Plant competition alters the temporal dynamics of plant-soil feedbacks

    T. Martijn Bezemer, Jingying Jing, Tanja Bakx-Schotman, Erik-Jan Bijleveld
    Most studies on plant‐soil feedback (PSF) and plant competition measure the feedback response at one moment only. However, PSFs and competition may both change over time, and how PSF and competition interact over time is unclear.
    We tested the temporal dynamics of PSF and interspecific competition for the forb Jacobaea vulgaris and the grass Holcus lanatus. We grew both species individually and in interspecific competition in soil that was first conditioned in the greenhouse by J. vulgaris, by H. lanatus or without plant growth. For a period of 11 weeks, we harvested plants twice a week and analysed the fungal and chemical composition of the different soils at the end of the first and second growth phase.
    During the second growth phase, when grown in isolation, both species produced more biomass in heterospecific conditioned soil than in conspecific conditioned soil. Young J. vulgaris exhibited a strong negative conspecific feedback, but this effect diminished over time and became neutral in older plants. In contrast, when grown in competition, the negative conspecific feedback of J. vulgaris exacerbated over time. Older H. lanatus plants benefited more from heterospecific conditioning when competing with J. vulgaris, then when grown isolated.
    Fungal community composition and soil chemistry differed significantly between soils but this was mainly driven by differences between plant‐conditioned and unconditioned soils. Remarkably, at the end of the second growth phase, fungal community composition was not explained by the legacy of the species that had been grown in the soil most recently, but still reflected the legacy of the first growth phase. We reexamined plant growth during a third growth phase. Biomass of J. vulgaris was still influenced by the treatments imposed during the first phase, while H. lanatus responded only to the plant growth treatments imposed during the second phase.
    Synthesis. Our study shows that the direction and magnitude of PSF depends on plant age and competition, and also on soil legacy effects of earlier plant growth. These results highlight the need to incorporate dynamic PSFs in research on plant populations and communities.
    https://doi.org/10.1111/1365-2745.12999
  • 2018

    Application and Theory of Plant–Soil Feedbacks on Aboveground Herbivores

    Ian Kaplan, Ana Pineda, T. Martijn Bezemer
    Plant–soil feedbacks are legacy effects created by an initial plant on the growth of subsequent plants using the same soil. These indirect soil-mediated interactions are primarily studied in the context of changes in the belowground biotic community. Here, we review current evidence surrounding plant–soil feedbacks, focusing on how these interactions are studied from an experimental standpoint and expand this discussion into new directions surrounding the influence of feedbacks on interactions with aboveground herbivorous insects. The taxon-specific impact of individual soil groups on foliar-feeding insects is well-described, but expanding this framework to plant–soil feedbacks is challenging because different plant species cause simultaneous and dramatic shifts in the composition of all soil life, sometimes in contradictory directions (i.e., certain fungi may increase, while nematodes decrease). Thus, expanding simple pair-wise root herbivore–plant–insect relationships to more holistic approaches that account for the full spectrum of changes in soil biota represents both a mechanistic and analytical challenge. These community-wide shifts, however, are representative of true legacy effects encountered by plants and insects in nature. We end our chapter on a discussion of how plant–soil feedbacks can be functionally used to steer the microbiome for enhanced crop protection in applied agricultural systems.
    https://doi.org/10.1007/978-3-319-91614-9_14
  • Plant and Soil
    2018

    Intraspecific aggregation and soil heterogeneity: competitive interactions of two clonal plants with contrasting spatial architecture

    Wei Xue, Lin Huang, Fei Hai Yu, T. Martijn Bezemer
    Background and aims
    Intraspecific aggregation of plant individuals can promote species coexistence by delaying competitive exclusions. However, such impacts may differ among species with contrasting spatial architecture and rely on the spatial distribution of resources.

    Methods
    We grew a phalanx clonal plant Carex neurocarpa (with aggregated ramets) and a guerilla one Bolboschoenus planiculmis (with diffused ramets) in monocultures or in 1:1 mixtures with an even or a clustered distribution pattern of the two species in homogeneous or heterogeneous soils.

    Results
    After 16 months, shoot biomass and ramet number were greater in mixtures than in monocultures in C. neurocarpa, but smaller in B. planiculmis. However, the growth of neither C. neurocarpa nor B. planiculmis differed between even and clustered mixtures. Soil nutrient heterogeneity did not significantly affect the growth of either species, but increased relative yield of B. planiculmis and decreased that of C. neurocarpa.

    Conclusions
    The relative importance of intra- vs. interspecific competition depends on the spatial architecture of plants, and soil nutrient heterogeneity slows down competitive exclusion by decreasing differences in competitive ability between plants. However, our results do not support the idea that intraspecific aggregation of individuals alters competitive interactions between species.
    https://doi.org/10.1007/s11104-018-3578-9
  • Plant and Soil
    2018

    Density-dependency and plant-soil feedback: former plant abundance influences competitive interactions between two grassland plant species through plant-soil feedbacks

    Wei Xue, T. Martijn Bezemer, Frank Berendse
    Backgrounds and aims
    Negative plant-soil feedbacks (PSFs) are thought to promote species coexistence, but most evidence is derived from theoretical models and data from plant monoculture experiments.

    Methods
    We grew Anthoxanthum odoratum and Centaurea jacea in field plots in monocultures and in mixtures with three ratios (3:1, 2:2 and 1:3) for three years. We then tested in a greenhouse experiment the performance of A. odoratum and C. jacea in pots planted with monocultures and 1:1 mixtures and filled with live and sterile soils collected from the field plots.

    Results
    In the greenhouse experiment, C. jacea produced less aboveground biomass in soil conditioned by C. jacea monocultures than in soil conditioned by A. odoratum monocultures, while the aboveground biomass of A. odoratum in general did not differ between the two monospecific soils. The negative PSF effect was greater in the 1:1 plant mixture than in plant monocultures for A. odoratum but did not differ for C. jacea. In the greenhouse experiment, the performance of C. jacea relative to A. odoratum in the 1:1 plant mixture was negatively correlated to the abundance of C. jacea in the field plot where the soil was collected from. This relationship was significant both in live and sterile soils. However, there was no relationship between the performance of A. odoratum relative to C. jacea in the 1:1 plant mixture in the greenhouse experiment and the abundance of A. odoratum in the field plots.

    Conclusions
    The response of a plant to PSF depends on whether the focal species grows in monocultures or in mixtures and on the identity of the species. Interspecific competition can exacerbate the negative plant-soil feedbacks compared to intraspecific competition when a plant competes with a stronger interspecific competitor. Moreover, the abundance of a species in mixed plant communities, via plant-soil feedback, negatively influences the relative competitiveness of that species when it grows later in interspecific competition, but this effect varies between species. This phenomenon may contribute to the coexistence of competing plants under natural conditions through preventing the dominance of a particular plant species.
    https://doi.org/10.1007/s11104-018-3690-x
  • Oecologia
    2018

    Species-specific plant soil feedbacks affect herbivore-induced gene expression and defense chemistry in Plantago lanceolata.

    Plants actively interact with antagonists and beneficial organisms occurring in the above- and belowground domains of terrestrial ecosystems. In the past decade, studies have focused on the role of plant–soil feedbacks (PSF) in a broad range of ecological processes. However, PSF and its legacy effects on plant defense traits, such as induction of defense-related genes and production of defensive secondary metabolites, have not received much attention. Here, we study soil legacy effects created by twelve common grassland plant species on the induction of four defense-related genes, involved in jasmonic acid signaling, related to chewing herbivore defense (LOX2, PPO7), and in salicylic acid signaling, related to pathogen defense (PR1 and PR2) in Plantago lanceolata in response to aboveground herbivory by Mamestra brassicae. We also assessed soil legacy and herbivory effects on the production of terpenoid defense compounds (the iridoid glycosides aucubin and catalpol) in P. lanceolata. Our results show that both soil legacy and herbivory influence phenotypes of P. lanceolata in terms of induction of Pl PPO7 and Pl LOX2, whereas the expression of Pl PR1 and Pl PR2-1 is not affected by soil legacies, nor by herbivory. We also find species-specific soil legacy effects on the production of aucubin. Moreover, P. lanceolata accumulates more catalpol when they are grown in soils conditioned by grass species. Our study highlights that PSF can influence aboveground plant–insect interactions through the impacts on plant defense traits and suggests that aboveground plant defense responses can be determined, at least partly, by plant-specific legacy effects induced by belowground organisms.
    https://doi.org/10.1007/s00442-018-4245-9
  • Plant and Soil
    2018

    Potential for synergy in soil inoculation for nature restoration by mixing inocula from different successional stages.

    Jasper Wubs, Pauline D. Melchers, T. Martijn Bezemer
    Background and aims
    Soil inoculation is a powerful tool for the restoration of terrestrial ecosystems. However, the origin of the donor material may differentially influence early- and late-successional plant species. Donor soil from late-succession stages may benefit target plant species due to a higher abundance of soil-borne mutualists. Arable soils, on the other hand, may suppress ruderals as they support more root herbivores that preferentially attack ruderal plant species, while mid-succession soils may be intermediate in their effects on ruderals and target species performance. We hypothesized that a mixture of arable and late-succession inocula may outperform pure late-successional inocula for restoration, by promoting late-successional target plants, while simultaneously reducing ruderal species’ performance.

    Methods
    We conducted a glasshouse experiment and tested the growth of ruderal and target plant species on pure and mixed inocula. The inocula were derived from arable fields, mid-succession grasslands and late-succession heathlands and we created a replacement series testing different pairwise mixitures for each of these inocula types (ratios: 100:0, 75:25, 50:50, 25:75, 0:100 of inoculum A and B respectively).

    Results
    In general, we found that a higher proportion of heathland material led to a higher aboveground biomass of target plant species, while responses of ruderal species were variable. We found synergistic effects when specific inocula were mixed. In particular, a 50:50 mixture of heathland and arable soil in the inoculum led to a significant reduction in ruderal species biomass relative to the two respective pure inocula. The overall response was driven by Myosotis arvensis, since the other two ruderal species were not significantly affected.

    Conclusions
    Mixing inocula from different successional stages can lead to synergistic effects on restoration, but this highly depends on the specific combination of inocula, the mixing ratio and plant species. This suggest that specific inocula may need to be developed in order to rapidly restore different plant communities.
    https://doi.org//10.1007/s11104-018-3825-0
  • Plant and Soil
    2018

    Long-term fertilization management affects the C utilization from crop residues by the soil micro-food web

    Shuyan Cui, Siwei Liang, Xiaoke Zhang, Yingbin Li, Wenju Liang, Liangjie Sun, Jingkuan Wang, T. Martijn Bezemer, Qi Li
    Crop residue decomposition is a major component of carbon (C) cycling and provides energy and nutrients to the soil micro-food web. An in-situ field experiment was conducted to examine how exogenous organic C is incorporated into the soil micro-food web and how this is influenced by four different fertilization treatments: organic manure (M), urea fertilizer (U), the combined application of organic and urea fertilizer (MU) and unfertilized control.
    https://doi.org/10.1007/s11104-018-3688-4
  • Oikos
    2018

    Temporal carry-over effects in sequential plant-soil feedbacks

    Plant–soil feedbacks (PSF) strongly influence plant performance. However, to what extent these PSF effects are persistent in the soil and how they are altered by species that subsequently condition the soil is unclear. Here we test how conspecific and heterospecific soil-conditioning effects interact across different soil-conditioning phases. We conducted a fully factorial glasshouse experiment where six plant species conditioned soils in two consecutive phases and measured the performance of Jacobaea vulgaris. The species that conditioned the soil during the second conditioning phase strongly determined the performance of J. vulgaris, but also the order and combination of species that conditioned the soil in the two phases accounted for a large part of the variance. For shoot biomass this interaction was the dominant variance component. We show that soil conditioning legacies carry-over and interact with the conditioning effects of succeeding plants. In the field, species replacements at the patch level often appear to be unpredictable and we suggest that sequential feedbacks may explain these apparently unpredictable transitions.
    https://doi.org/10.1111/oik.04526
  • Plant and Soil
    2018

    Carry-over effects of soil inoculation on plant growth and health under sequential exposure to soil-borne diseases

    Haikun Ma, Ana Pineda, Andre W. G. van der Wurff, T. Martijn Bezemer
    Background and aims
    Most plant-soil feedback and inoculation studies are limited to one growth cycle. We examined the effects of inoculation with eight plant-conditioned soils on chrysanthemum during two sequential growth cycles. The plants were also exposed sequentially to soil diseases.

    Methods
    In cycle 1, plants were grown in sterile soil inoculated or not with plant-conditioned soils, and exposed or not to Pythium or root feeding nematodes. In cycle 2, new plants were grown in soil from cycle 1 or in new 100% sterile soil. Plants were exposed again to Pythium, or to soil with pathogens and nematodes collected from a commercial chrysanthemum greenhouse.

    Results
    After two cycles, effects of soil inoculation on plant growth were still present. Chrysanthemum exhibited a negative conspecific feedback response, but this was less strong in inoculated soils. Pythium or nematode addition did not affect plant growth. However, addition of pathogen-containing soil from the commercial greenhouse reduced plant growth in sterile soil but increased growth in plant-conditioned soils.

    Conclusions
    Inoculation with plant-conditioned soil can reduce the negative conspecific plant-soil feedback of chrysanthemum. Our study further advances our understanding of the temporal dynamics of conspecific and heterospecific plant-soil feedbacks, and how they interact with soil-borne diseases.
    https://doi.org/10.1007/s11104-018-3837-9
  • Ecology
    2018

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

    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.
    https://doi.org/10.1002/ecy.2400
  • Journal of Ecology
    2018

    Plant community composition but not plant traits determine the outcome of soil legacy effects on plants and insects

    1.Plants leave species-specific legacies in the soil they grow in that can represent changes in abiotic or biotic soil properties. It has been shown that such legacies can affect future plants that grow in the same soil (plant-soil feedback, PSF). Such processes have been studied in detail, but mostly on individual plants. Here we study PSF effects at the community level and use a trait-based approach both in the conditioning phase and in the feedback phase to study how twelve individual soil legacies influence six plant communities that differ in root size.

    2.We tested if (I) grassland perennial species with large root systems would leave a stronger legacy than those with small root systems, (II) grass species would leave a more positive soil legacy than forbs and (III) communities with large root systems would be more responsive than small-rooted communities. We also tested (IV) whether a leaf chewing herbivore and a phloem feeder were affected by soil legacy effects in a community framework.

    3.Our study shows that the six different plant communities that we used respond differently to soil legacies of twelve different plant species and their functional groups. Species with large root systems did not leave stronger legacies than species with small root systems, nor were communities with large root systems more responsive than communities with root systems.

    4.Moreover, we show that when communities are affected by soil legacies, these effects carry over to the chewing herbivore Mamestra brassicae (Lepidoptera: Noctuidae) through induced behavioral changes resulting in better performance of a chewing herbivore on forb-conditioned soils than on grass-conditioned soils, whereas performance of the phloem feeder Rhopalosiphum padi (Hemiptera: Aphididae) remained unaffected.

    5.Synthesis: The results of this study shed light on the variability of soil effects found in previous work on feedbacks in communities. Our study suggests that the composition of plant communities determines to a large part the response to soil legacies. Furthermore, the responses to soil legacies of herbivores feeding on the plant communities that we observed, suggests that in natural ecosystems, the vegetation history may also have an influence on contemporary herbivore assemblages. This opens up exciting new areas in plant-insect research and can have important implications for insect pest management.
    https://doi.org/10.1111/1365-2745.12907
  • Frontiers in Ecology and Evolution
    2018

    Effects of soil organisms on aboveground plant-insect interactions in the field: patterns, mechanisms and the role of methodology

    Soil biota-plant interactions play a dominant role in terrestrial ecosystems. Through nutrient mineralization and mutualistic or antagonistic interactions with plants soil biota can affect plant performance and physiology and via this affect plant-associated aboveground insects. There is a large body of work in this field that has already been synthesized in various review papers. However, most of the studies have been carried out under highly controlled laboratory or greenhouse conditions.
    Here, we review studies that manipulate soil organisms of four dominant taxa (i.e. bacteria, fungi, nematodes and soil arthropods) in the field and assess the effects on the growth of plants and interactions with associated aboveground insects.
    We show that soil organisms play an important role in shaping plant-insect interactions in the field and that general patterns can be found for some taxa. Plant growth-promoting rhizobacteria generally have negative effects on herbivore performance or abundance, most likely through priming of defenses in the host plant. Addition of arbuscular mycorrhizal fungi (AMF) has positive effects on sap sucking herbivores, which is likely due to positive effects of AMF on nutrient levels in the phloem. The majority of AMF effects on chewers were neutral but when present, AMF effects were positive for specialist and negative for generalist chewing herbivores. AMF addition has negative effects on natural enemies in the field, suggesting that AMF may affect plant attractiveness for natural enemies, e.g. through volatile profiles. Alternatively, AMF may affect the quality of prey or host insects mediated by plant quality, which may in turn affect the performance and density of natural enemies. Nematodes negatively affect the performance of sap sucking herbivores (generally through phloem quality) but have no effect on chewing herbivores. For soil arthropods there are no clear patterns yet. We further show that the methodology used plays an important role in influencing the outcomes of field studies. Studies using potted plants in the field and studies that remove target soil taxa by means of pesticides are most likely to detect significant results. Lastly, we discuss suggestions for future research that could increase our understanding of soil biota-plant-insect interactions in the field.
    https://doi.org/10.3389/fevo.2018.00106
  • Functional Ecology
    2018

    Spatial heterogeneity in plant-soil feedbacks alters competitive interactions between two grassland plant species

    Wei Xue, Frank Berendse, T. Martijn Bezemer
    The effects of plants on soil vary greatly between plant species and in mixed plant communities this can lead to spatial variation in plant‐soil feedback (PSF) effects. Such spatial effects are thought to influence plant species coexistence, but the empirical evidence for this hypothesis is limited.
    Here, we investigate how spatial heterogeneity in PSFs influences plant growth and competition. The experiment was carried out with high and low nutrient soils to examine how these effects depend on soil fertility. We collected soil from field plots planted for three years with monocultures of Anthoxanthum odoratum and Centaurea jacea and tested the performance of the two species in a greenhouse experiment in heterogeneous soils consisting of patches of “own” and “foreign” soils and in soils where the “own” and “foreign” soils were mixed homogeneously. In the test phase, plants were grown in monocultures and in 1:1 mixtures in live or sterilized soils.
    Overall, A. odoratum in monocultures produced less aboveground biomass in heterogeneous soils than in homogeneous soils. Centaurea jacea produced less belowground biomass in live heterogeneous soils than in live homogeneous soils, but there was no difference between sterile heterogeneous and homogeneous soils. The belowground biomass per patch varied more in pots with live heterogeneous soils than in pots with live homogeneous soils for both plant species, but there was no difference between pots with sterile heterogeneous and homogeneous soils. In pots with plant mixtures, the difference in aboveground biomass between the two competing species tended to be smaller in heterogeneous than in homogeneous soils. In pots with heterogeneous soils, both plant species grown in mixtures produced more aboveground biomass in “foreign” soil patches than in “own” soil patches. The responses of plants to heterogeneous PSFs were not different between low and high nutrient soils.
    Our results show that spatially heterogeneous PSFs can influence plant performance and competition via reducing the growth inequality between the two competing species by allowing selective growth in foreign soil patches, independent of initial soil nutrient availability. Such effect may slow down exclusion processes and thus promote the coexistence of competing species at the local scale in mixed plant communities.
    https://doi.org/10.1111/1365-2435.13124
  • Oikos
    06-2017

    After-life effects: living and dead invertebrates differentially affect plants and their associated above- and belowground multitrophic communities

    Martine Kos, Jingying Jing, Ivor Keesmaat, Steven A.J. Declerck, Roel Wagenaar, T. Martijn Bezemer
    Above-belowground (AG-BG) studies typically focus on plant-mediated effects inflicted by living organisms. However, animal cadavers may also play an important role in AG-BG interactions. Here, we explore whether living and dead foliar-feeding and soil-dwelling invertebrates differentially affect plants and their associated AG and BG multitrophic communities.

    In a mesocosm study we separated effects of living and dead locusts (AG herbivores) and earthworms (BG detritivores) on experimental multitrophic communities consisting of eight plant species, an AG aphid and parasitoid community and a BG nematode community. We measured root and shoot biomass and determined plant community composition and densities of aphids, parasitoids and nematodes.

    Living locusts decreased total shoot and root biomass in the mesocosms, whereas living earthworms enhanced total root biomass. Cadavers of both invertebrates strongly increased total root and shoot biomass, and changed the plant community composition mainly via enhanced growth of grasses. Earthworm cadavers affected plant biomass and community composition more strongly than their living counterparts, while this was reversed for locusts. Structural equation models showed that aphids and parasitoids were influenced via changes in plant community composition. Nematode densities in the soil, especially those of bacterivorous and entomopathogenic nematodes, were strongly increased by dead invertebrates, but unaffected by living ones.

    We conclude that effects of invertebrates on plant growth and densities of AG and BG organisms strongly depend on whether the invertebrates are dead or alive. Remarkably, invertebrate cadavers may inflict even stronger effects than their living counterparts. Hence, our study reveals an important, but often neglected, role of animal cadavers in AG-BG studies.
    https://doi.org/10.1111/oik.03734
  • Journal of Ecology
    2017

    Effects of plant diversity on the concentration of secondary plant metabolites and the density of arthropods on focal plants in the field

    Olga Kostenko, Patrick P. J. Mulder, Matthijs Courbois, T. Martijn Bezemer
    1.The diversity of the surrounding plant community can directly affect the abundance of insects on a focal plant as well as the size and quality of that focal plant. However, to what extent the effects of plant diversity on the arthropod community on a focal plant are mediated by host plant quality or by the diversity of the surrounding plants remains unresolved.

    2.In the field, we sampled arthropod communities on focal Jacobaea vulgaris plants growing in experimental plant communities that were maintained at different levels of diversity (1, 2, 4 or 9 species) for three years. Focal plants were also planted in plots without surrounding vegetation. We recorded the structural characteristics of each of the surrounding plant communities as well as the growth, and primary and secondary chemistry (pyrrolizidine alkaloids, PAs) of the focal plants to disentangle the potential mechanisms causing the diversity effects.

    3.Two years after planting, the abundance of arthropods on focal plants that were still in the vegetative stage decreased with increasing plant diversity, while the abundance of arthropods on reproductive focal plants was not significantly affected by the diversity of the neighbouring community. The size of both vegetative and reproductive focal plants was not significantly affected by the diversity of the neighbouring community, but the levels of PAs and the foliar N concentration of vegetative focal plants decreased with increasing plant diversity. Structural equation modelling revealed that the effects of plant diversity on the arthropod communities on focal plants were not mediated by changes in plant quality.

    4.Synthesis. Plant quality can greatly influence insect preference and performance. However, under natural conditions the effects of the neighbouring plant community can overrule the plant quality effects of individual plants growing in those communities on the abundance of insects associated to this plant.
    https://doi.org/10.1111/1365-2745.12700
  • Plant and Soil
    2017

    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
    Aims

    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.

    Methods

    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.

    Results

    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.

    Conclusions

    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.
    https://doi.org/10.1007/s11104-016-3149-x
  • Trends in Plant Science
    2017

    Steering soil microbiomes to suppress aboveground insect pests

    Ana Pineda, Ian Kaplan, T. Martijn Bezemer
    Soil-borne microbes affect aboveground herbivorous insects through a cascade of molecular and chemical changes in the plant, but knowledge of these microbe?plant?insect interactions is mostly limited to one or a few microbial strains. Yet, the soil microbial community comprises thousands of unique taxa interacting in complex networks, the so-called 'microbiome', which provides plants with multiple beneficial functions. There has been little exploration of the role and management of whole microbiomes in plant-insect interactions, calling for the integration of this complexity in aboveground-belowground research. Here, we propose holistic approaches to select soil microbiomes that can be used to protect plants from aboveground attackers.
    https://doi.org/10.1016/j.tplants.2017.07.002
  • Frontiers in Plant Science
    2017

    Plant–Soil Feedback Effects on Growth, Defense and Susceptibility to a Soil-Borne Disease in a Cut Flower Crop: Species and Functional Group Effects

    Haikun Ma, Ana Pineda, Andre W. G. van der Wurff, Ciska Raaijmakers, T. Martijn Bezemer
    Plants can influence the soil they grow in, and via these changes in the soil they can positively or negatively influence other plants that grow later in this soil, a phenomenon called plant-soil feedback. A fascinating possibility is then to apply positive plant-soil feedback effects in sustainable agriculture to promote plant growth and resistance to pathogens. We grew the cut flower chrysanthemum (Dendranthema X grandiflora) in sterile soil inoculated with soil collected from a grassland that was subsequently conditioned by 37 plant species of three functional groups (grass, forb, legume), and compared it to growth in 100% sterile soil (control). We tested the performance of chrysanthemum by measuring plant growth, and defense (leaf chlorogenic acid concentration) and susceptibility to the oomycete pathogen Pythium ultimum. In presence of Pythium, belowground biomass of chrysanthemum declined but aboveground biomass was not affected compared to non-Pythium inoculated plants. We observed strong differences among species and among functional groups in their plant-soil feedback effects on chrysanthemum. Soil inocula that were conditioned by grasses produced higher chrysanthemum above- and belowground biomass, less yellowness than inocula conditioned by legumes or forbs. Chrysanthemum showed lower root/shoot ratio in response to Pythium in soil conditioned by forb than by grass. Leaf chlorogenic acid concentrations increased in presence of Pythium and correlated positively with chrysanthemum aboveground biomass. Although chlorogenic acid differed between soil inocula, it did not differ between functional groups. There was no relationship between the phylogenetic distance of conditioning plant species to chrysanthemum and their plant-soil feedback effects on chrysanthemum. Our study provides novel evidence that plant-soil feedback effects can influence crop health, and shows that plant-soil feedbacks, plant disease susceptibility, and plant aboveground defense compounds are tightly linked. Moreover, we highlight the relevance of considering plant-soil feedbacks in sustainable horticulture, and the larger role of grasses compared to legumes or forbs in this.
    https://doi.org/10.3389/fpls.2017.02127
  • Soil Biology & Biochemistry
    2017

    Transient negative biochar effects on plant growth are strongest after microbial species loss

    (Gera) W.H.G. Hol, M. Vestergård, Freddy ten Hooven, Henk Duyts, Tess Van de Voorde, T. Martijn Bezemer
    Biochar has been explored as an organic amendment to improve soil quality and benefit plant growth. The overall positive effects of biochar on crop yields are generally attributed to abiotic changes, while the alternative causal pathway via changes in soil biota is unexplored. We compared plant growth effects of legumes in sterile soil inoculated with dilutions of soil and soil microbial suspensions to determine the direct effects of biochar-induced changes in soil biota on plant growth. Suspensions and soil were from soil amended with biochar and soil without biochar. By comparing consecutive plant growth phases on the same inoculated soils, we also determined the temporal effects of soil biota from biochar-amended and control soils. Biota from biochar-amended soil was less beneficial for Medicago sativa growth, especially with small amounts of inocula. Flowering was delayed in the presence of biota from biochar plots. Inoculum with either soil or soil suspension gave similar results for plant biomass, indicating that microorganisms play a major role. Vicia villosa growth did not respond to the various inocula, even though the inoculum quantity strongly affected nematode community composition and protozoan abundance. In a later growing phase the negative effect of biochar-associated biota on Medicago growth mostly disappeared, which leads to the conclusion that the benefits of biochar application via abiotic changes may outweigh the negative effects of biochar on soil biota.
    https://doi.org/10.1016/j.soilbio.2017.09.016
  • Functional Ecology
    2017

    Home-field advantages of litter decomposition increase with increasing N deposition rates: a litter and soil perspective

    Y. Li, Qi Li, J. Yang, L. Xiaotao, W. Liang, Xingguo Han, T. Martijn Bezemer

    1.Differences in litter quality and in soil microbial community composition can influence the litter decomposition and “home-field advantage” (HFA). However, our knowledge about the relative role of litter and soil characteristics on litter decomposition and HFA effects is still limited, especially under long-term N deposition.

    2.We collected soil and two types of litter (monospecific and mixed species litter) from five replicate plots from a long-term N-deposition field experiment with seven N-addition treatments (0, 2, 5, 10, 15, 20, 50 g N m−2 yr−1). We examined the effects of N-addition on litter quality and soil characteristics. We then carried out a three-pronged microcosm decomposition experiment with (i) litter from different N-addition treatments decomposed on a standard field soil; (ii) standard litter decomposed on soils from the different N-addition treatments; and (iii) litter decomposed on soil from the same N-addition treatment plot.

    3.Decomposition of litter on standard soil was influenced strongly by the N-addition treatment, but did not consistently decrease or increase with increasing N-addition rates. Instead, decomposition of standard litter on soils collected from different N-addition treatments decreased with increasing rates of N-addition. Decomposition of litter on soil collected from the same plot increased with increasing N-addition rates. Soil characteristics explained more of the variation in litter decomposition than litter characteristics.

    4.There was a clear HFA effect for litter decomposition; both from a litter and from a soil perspective. HFA effects increased when the dissimilarity in litter quality (N content and C: N ratio) increase among the different N-addition treatments and the soil effect was strongest at high N-addition rates.

    5.N-addition influenced litter decomposition by changing both litter and soil characteristics. Importantly, N-addition decreased the capability of soils to decompose litter and it increased the home-field advantage effect indicating that soils decomposed local litter better than other litter, due to specialization in soil communities. Nitrogen deposition is an important threat to ecosystems worldwide and our study emphasizes that ecosystem functions such as decomposition can be greatly influenced by these global changes.
    https://doi.org/10.1111/1365-2435.12863
  • Plant and Soil
    2017

    Initial biochar effects on plant productivity derive from N fertilization

    Simon Jeffery, Ilse Memelink, Edward Hodgson, Sian Jones, Tess Van de Voorde, T. Martijn Bezemer, Liesje Mommer, Jan Willem van Groenigen
    Biochar application to soil is widely claimed to increase plant productivity. However, the underlying mechanisms are still not conclusively described. Here, we aim to elucidate these mechanisms using stable isotope probing.
    https://doi.org/10.1007/s11104-016-3171-z
  • Journal of Ecology
    2016

    Effects of spatial plant-soil feedback heterogeneity on plant performance in monocultures

    1. Plant-soil feedback (PSF) effects have almost exclusively been quantified on homogeneous soils, but as different plant species will influence their local soil differently in reality PSF effects will be spatially heterogeneous. Whether plant performance in soils with spatially heterogeneous PSF can be predicted from pot experiments with homogeneous soils is unclear. 2. In a greenhouse experiment we tested the response of monocultures of six grassland species (two grasses, two legumes, and two forbs) to three spatially explicit treatments (fine-grain heterogeneity, coarse-grain heterogeneity, and homogeneous). Sixteen patches of conditioned soil (~6x6 cm) were placed within each container. For homogeneous treatments all patches contained the same conditioned soil within a container. The fine-grained heterogeneous treatment contained four differently conditioned soils that were applied following a Latin square design, while for the coarse-grained heterogeneous treatment four contiguous square blocks of four cells each were created in each container. 3. In general species grew worse on soil conditioned by conspecifics. However, when the biomass production on all homogeneous soil treatments (own and foreign soils) was averaged and compared to the heterogeneous treatments, we found that biomass production was lower than expected in the heterogeneous soils. This effect of heterogeneity depended on both the conditioning and test species, but most heterogeneity effects were negative. The grain of the heterogeneity (coarse vs. fine: at the chosen spatial scale) did not affect plant performance. 4. We hypothesize that a more diverse soil community is present in spatially heterogeneous soils. This increases i) the chance of plants to encounter its antagonists, which may then rapidly increase in numbers; and ii) the scope for synergistic co-infections. Together this may lead to non-additive responses of plants to spatial heterogeneity in PSF. 5. Synthesis. Plant performance was lower in spatially heterogeneous soils than predicted by spatially homogeneous soils. In natural grasslands that have mixed plant communities conditioning the soil plant-soil feedback (PSF) effects on plant performance may therefore be more negative than what is predicted from pot experiments. Our results emphasise the need to incorporate the spatial dynamics of PSF both in empirical and modelling studies if we are to understand the role of PSF in plant-plant interactions and plant community dynamics. This article is protected by copyright. All rights reserved.
    https://doi.org/10.1111/1365-2745.12521
  • Agriculture, Ecosystems and Environment
    2016

    Cultivar specific plant-soil feedback overrules soil legacy effects of elevated ozone in a rice-wheat rotation system

    Qi Li, Yue Yang, Xuelian Bao, Jianguo Zhu, Wenju Liang, T. Martijn Bezemer
    Abstract Tropospheric ozone has been recognized as one of the most important air pollutants. Many studies have shown that elevated ozone negatively impacts yields of important crops such as wheat or rice, but how ozone influences soil ecosystems of these crops and plant growth in rotation systems is less well understood. Using soil collected from a free-air ozone enrichment experiment running for 5 years, we carried out a plant-soil feedback experiment under greenhouse conditions to evaluate the influence of wheat cultivars (Triticum aestivum L.) with different ozone-tolerance on rice (Oryza sativa L.) grown in soils with or without a history of ozone exposure. Our results indicate that there were interactive effects of wheat cultivar and history of ozone exposure on soil respiration and the abundance of fungivorous nematodes. Moreover, the soil microbial community and the abundance of omnivorours-predatory nematodes varied in different wheat cultivars. These differences in the soil, in turn, had feedback effects on the succeeding growth of rice. Rice grown in soil in which previously the ozone-sensitive wheat cultivars Yangmai 2 or Yangmai 19 had grown, had lower shoot biomass than rice grown in the ozone-tolerant wheat cultivars Yangmai 16 soil. However, these cultivar specific effects on rice growth were independent from the previous ozone exposure of the soil. Our results suggest that, in rice-wheat rotation systems, when selecting wheat cultivars to cope with changing climatic conditions, such as elevated ozone, growers should consider the soil-feedback effects of these cultivars on the succeeding crop.
    https://doi.org/10.1016/j.agee.2016.07.025
  • Applied Soil Ecology
    2016

    Opposing Effects of Nitrogen and Water addition on Soil Bacterial and Fungal Communities in the Inner Mongolia steppe: a field experiment

    Haikun Ma, Guang-ying Bai, Yang Sun, Olga Kostenko, Xiang Zhu, Shan Lin, W.B. Ruan, Nian-xi Zhao, T. Martijn Bezemer
    Grasslands are important ecosystems and make up 40% of the terrestrial ecosystems worldwide. The Inner Mongolia steppe is the main grassland region of China, and nitrogen (N) and water availability are two important factors that limit the productivity of these grasslands. We tested how N and water addition influence the composition of the microbial community in the soil using PLFA, and soil physical and chemical properties in two semiarid grassland sites in Inner Mongolia during two consecutive years. In both sites, a split-plot design was employed with two water treatments (natural precipitation, stimulated wet year precipitation) and three N treatments (0 kg N ha−1, 25 kg N ha−1, 50 kg N ha−1). Water addition greatly increased soil fungi and decreased bacteria while N had opposite effects. Water addition resulted in a significant increase in soil pH and electric conductivity. N addition did not lead to consistent changes in soil characteristics. Multivariate analysis showed that PLFA composition varied between all treatments but was mainly influenced by water addition. This study provides insight into how climatic changes such as alternations in rainfall and N deposition shape the soil microbial communities in Inner Mongolia steppes.
    https://doi.org/10.1016/j.apsoil.2016.08.008
  • Nature Plants
    2016

    Soil inoculation steers restoration of terrestrial ecosystems

    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.
    https://doi.org/10.1038/nplants.2016.107
  • Ecological Research
    2016

    Drivers of bacterial beta diversity in two temperate forests

    Xugao Wang, Hui Li, T. Martijn Bezemer, Zhanqing Hao
    Although the consequences of changes in microbial diversity have received increasing attention, our understanding of processes that drive spatial variation in microbial diversity remains limited. In this study, we sampled bacterial communities in early and late successional temperate forests in Northeast China, and used distance-based redundancy analysis to examine how different processes influence bacterial beta diversity and phylogeny-based beta diversity using the Bray–Curtis and UniFrac metrics, respectively. After controlling for sampling effects, bacterial beta diversity in both forests was higher than expected by chance, which indicates that the bacterial community showed strong intraspecific aggregation. Both environmental filtering and dispersal limitation contributed to bacterial beta diversity and phylogeny-based beta diversity in the two forests. However, the relative importance of these different processes varied between the two forests. In the early successional forest, dispersal limitation played a dominant role in structuring the bacterial community, whereas the effects of environmental filtering were more important in the late successional forest. Our study revealed that bacterial beta diversity and phylogeny-based beta diversity in forest communities from the same region are regulated by different forces and that the relative importance of different forces varies over succession.
    https://doi.org/10.1007/s11284-015-1313-z
  • Journal of Chemical Ecology
    11-2015

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

    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.
    https://doi.org/10.1007/s10886-015-0644-0
  • Scientific Reports
    2015

    Multi-trait mimicry of ants by a parasitoid wasp

    Mima Malčická, T. Martijn Bezemer, Bertanne Visser, Mark Bloemberg, Charles J. P. Snart, Ian C. W. Hardy, Jeff A. Harvey
    https://doi.org/10.1038/srep08043
  • Oikos
    2015

    Plant–soil feedback effects on plant quality and performance of an aboveground herbivore interact with fertilisation

    Martine Kos, Maarten A. B. Tuijl, Joris de Roo, Patrick P. J. Mulder, T. Martijn Bezemer
    Plant–soil feedback (PSF) effects on plant performance can be influenced by the availability of nutrients in the soil. Recent studies have shown that PSF effects can also change aboveground plant–insect interactions via soil-mediated changes in plant quality, but whether this is influenced by soil nutrient availability is unknown. We examined how fertilisation influences PSF effects on aboveground plant-aphid interactions in ragwort Jacobaea vulgaris. We grew J. vulgaris in soil conditioned by conspecific plants and in unconditioned soil at two levels of fertilisation and measured soil fungal communities, plant biomass, concentrations of primary (amino acids) and secondary (pyrrolizidine alkaloids; PAs) metabolites in phloem exudates, performance of the specialist aphid Aphis jacobaeae and sequestration of PAs by the aphid. We observed a strong interaction between soil conditioning and fertilisation on amino acid and PA concentrations in phloem exudates of J. vulgaris and on aphid performance, with opposite effects of soil conditioning at the two fertilisation levels. Plant biomass was reduced by soil conditioning and increased by fertilisation. Aphids contained high PA concentrations, converted N-oxides into tertiary amines and preferentially sequestered certain PA compounds, but PA sequestration was not affected by any of the treatments. We conclude that effects of PSF and fertilisation on plant chemistry and aphid performance are interdependent. Our study highlights the need to consider the importance of abiotic soil conditions on the outcome of PSF effects on aboveground plant–insect interactions.
    https://doi.org/10.1111/oik.01828
  • Nature
    2015

    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, Helge Bruelheide, E. De Luca, Anne Ebeling, John N. Griffin, Q. Guo, Yann Hautier, Andrew Hector, Anke Jentsch, Jürgen Kreyling, V. Lanta, P. Manning, Sebastian T. Meyer, Akira S. Mori, S. Naeem, P.A. Niklaus, H.W. Polley, P.B. Reich, Christiane Roscher, Eric W. Seabloom, Melinda D. Smith, Madhav Thakur, D. Tilman, B.F. Tracy, Wim H. van der Putten, Jasper van Ruijven, Alexandra Weigelt, Wolfgang 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.
    https://doi.org/10.1038/nature15374
  • Geoderma
    2015

    Biochar application does not improve the soil hydrological function of a sandy soil

    S. Jeffery, M.B.C. Meinders, C.R. Stoof, T. Martijn Bezemer, Tess Van de Voorde, Liesje Mommer, J.W. Van Groenigen
    Biochar application to soil is currently being widely posited as a means to improve soil quality and thereby increase crop yield. Next to beneficial effects on soil nutrient availability and retention, biochar is assumed to improve soil water retention. However, evidence for such an effect in the primary literature remains elusive. Therefore, we studied the effect of biochar on soil hydrological characteristics in two separate field experiments on a sandy soil in The Netherlands. In Experiment I, biochar produced through slow pyrolysis of herbaceous feedstock at two temperatures (400 °C and 600 °C) was applied to soil at a rate of 10 t ha− 1. In Experiment II, the 400 °C biochar was applied at rates of 1, 5, 20 and 50 t ha− 1. Soils were analysed for soil water retention, aggregate stability and other soil physical parameters after three growing seasons and one growing season for Experiment I and Experiment II, respectively. We characterised the pore structure of the biochar using X-ray computed micro-tomography (XRT) and hydrophobicity using contact angle measurements.

    We found no significant effects of biochar application on soil water retention in either experiment. Aggregate stability was also not significantly affected, nor was field saturated hydraulic conductivity. XRT analysis of the biochars showed that they were highly porous, with 48% and 57% porosity for the 400 °C and 600 °C biochar respectively. More than 99% of internal pores of the biochar particles were connected to the surface, suggesting a potential role for biochars in improving soil water retention. However, the biochars were highly hydrophobic. We postulate that this strong hydrophobicity prevented water from infiltrating into the biochar particles, prohibiting an effect on soil water retention. Our results suggest that, in addition to characterising pore space, biochars should be analysed for hydrophobicity when assessing their potential for improving soil physical properties.
    https://doi.org/10.1016/j.geoderma.2015.03.022
  • Ecology
    2015

    Disentangling above- and belowground neighbor effects on the growth, chemistry and arthropod community on a focal plant

    Martine Kos, Tibor Bukovinszky, P.P.J. Mulder, T. Martijn Bezemer
    Neighboring plants can influence arthropods on a focal plant and this can result in associational resistance or associational susceptibility. These effects can be mediated by above- and belowground interactions between the neighbor and focal plant, but determining the relative contribution of the above- and belowground effects remains an open challenge. We performed a common garden experiment with a design that enabled us to disentangle the above- and belowground effects of five different plant species on the growth and chemistry of the focal plant ragwort (Jacobaea vulgaris), and the arthropod community associated to this plant. Aboveground effects of different neighboring plant species were more important for the growth and quality of J. vulgaris and for the arthropod abundance on this plant than belowground effects of neighbors. This remained true when only indirect neighbor effects (via affecting the biomass or quality of the focal plant) were considered. The aboveground neighbor effects on arthropod abundance on the focal plant were strongly negative. However, the magnitude of the effect depended on the identity of the neighboring species, and herbivore abundance on the focal plant was higher when surrounded by conspecific than by heterospecific plants. We also observed interactions between above- and belowground neighbor effects, indicating that these effects may be non-additive. We conclude that above- and belowground associational effects are not equally strong, and that neighbor effects on plant-arthropod interactions occur predominantly aboveground. Read More: http://www.esajournals.org/doi/abs/10.1890/14-0563.1?af=R
    https://doi.org/10.1890/14-0563.1
  • Journal of Ecology
    2015

    Species-specific plant-soil feedback effects on above-ground plant-insect interactions

    Martine Kos, Maarten A. B. Tuijl, Joris de Roo, Patrick P. J. Mulder, T. Martijn Bezemer
    1.Plant-soil feedback (PSF) effects on plant performance strongly depend on the plant species that conditioned the soil. Recent studies have shown that PSF can change above-ground plant-insect interactions via soil-mediated changes in plant quality, but whether these effects depend on species-specific soil conditioning is unknown. We examined how PSF effects of several plant species influence above-ground plant-aphid interactions.

    2.We grew ragwort (Jacobaea vulgaris) in field soil conditioned specifically by 10 plant species, belonging to three functional groups (grasses, forbs and legumes), in a multispecies mixture of the conditioned soils and in control (unconditioned) field soil. We measured plant biomass, concentrations of primary (amino acids) and secondary (pyrrolizidine alkaloids) metabolites in phloem exudates, and performance of the generalist aphid Brachycaudus cardui and the specialist Aphis jacobaeae.

    3.We observed that plant species, via species-specific effects on soil fungal communities, exerted unique plant-soil effects on J. vulgaris biomass, amino acid concentrations in phloem exudates and aphid performance. The direction and magnitude of the species-specific PSF effects on aphid performance differed between both aphid species. PSF effects on soil fungal communities, plant biomass and A. jacobaeae performance also differed between grasses, forbs and legumes, with soil conditioning by forbs resulting in lowest plant biomass and aphid performance.

    4.Synthesis. Our study provides novel evidence that plant-soil feedback (PSF) effects on above-ground plant-insect interactions are highly species-specific. Our results add a new dimension to the rapidly developing research fields of PSF and above-below-ground interactions, and highlights that these fields are tightly linked.
    https://doi.org/10.1111/1365-2745.12402
  • Ecological Entomology
    2015

    Effects of plant diversity and structural complexity on parasitoid behaviour in a field experiment

    Olga Kostenko, Mark Lammers, Saskia S. Grootemaat, Thomas Kroon, Jeff A. Harvey, Moniek Van Geem, T. Martijn Bezemer
    1. In natural ecosystems, plants containing hosts for parasitoids are often embedded within heterogeneous plant communities. These plant communities surrounding host-infested plants may influence the host-finding ability of parasitoids.

    2. A release-recapture-approach was used to examine whether the diversity and structural complexity of the community surrounding a host-infested plant influences the aggregation behaviour of the leaf-miner parasitoid Dacnusa sibirica Telenga and naturally occurring local leaf-miner parasitoids. Released and locally present parasitoids were collected on potted Jacobaea vulgaris Gaertn.plants infested with the generalist leaf-miner Chromatomyia syngenesiae Hardy. The plants were placed in experimentally established plant communities differing in plant diversity (1–9 species) and habitat complexity (bare ground, mown vegetation, and tall vegetation). Additionally, parasitoids were reared out from host mines on the trap plants.

    3. Plant diversity did not influence the mean number of recaptured D. sibirica or captures of other locally present parasitoids but the number of recaptured parasitoids was influenced by habitat complexity. No D. sibirica parasitoids were recaptured in the bare ground plots or plots with mown vegetation. The mean number of recaptured D. sibirica generally increased with increasing complexity of the plant community, whereas locally present parasitoids were captured more frequently in communities with more bare ground. There was a unimodal relationship between the number of reared out parasitoids and diversity of the surrounding vegetation with the highest density of emerged parasitoids at intermediate diversity levels.

    4. The present study adds to the thus far limited body of literature examining the aggregation behaviour of parasitoids in the field and suggests that the preference of parasitoids to aggregate in complex versus simple vegetation is association specific and thus depends on the parasitoid species as well as the identity of the plant community.
    https://doi.org/10.1111/een.12251
  • Basic and Applied Ecology
    2015

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

    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.
    https://doi.org/10.1016/j.baae.2015.01.001
  • Soil Biology & Biochemistry
    2015

    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.
    https://doi.org/10.1016/j.soilbio.2015.08.029
  • Basic and Applied Ecology
    2015

    Interactive effects of above- and belowground herbivory and plant competition on plant growth and defence

    Jingying Jing, Ciska Raaijmakers, Olga Kostenko, Martine Kos, P.P.J. Mulder, T. Martijn Bezemer
    Competition and herbivory are two major factors that can influence plant growth and plant defence. Although these two factors are often studied separately, they do not operate independently. We examined how aboveground herbivory by beet armyworm larvae (Spodoptera exigua) and belowground herbivory by wireworms (Agriotes lineatus) influenced competition between the plant species Jacobaea vulgaris and Leucanthemum vulgare exposed to three competition levels (no, intra-, and interspecific competition). In addition, we studied the effects of herbivory and competition on pyrrolizidine alkaloid (PA) concentrations in leaves of J. vulgaris. For J. vulgaris, aboveground herbivory significantly reduced shoot biomass while belowground herbivory increased root biomass. Biomass of L. vulgare was not affected by herbivory. Competition caused a reduction in biomass for both plant species, but herbivory did not affect the outcome of the competition. However, competition significantly influenced the amount of leaf damage experienced by the plants. A L. vulgare plant had significantly less damage from aboveground herbivores when grown together with J. vulgaris than when grown alone or in intraspecific competition, while a J. vulgaris plant experienced lowest damage in conditions of intraspecific competition. The total PA concentration in J. vulgaris leaves was highest for plants exposed to interspecific competition. Root herbivory caused an increase in the relative concentration of N-oxides, the less toxic form of PAs, in leaves of plants that were grown without competition, but a decrease in plants exposed to competition. Our study shows that competition and herbivory but also the type of competition and whether herbivory occurs above- or belowground, all influence plant performance. However, overall, there was no evidence that herbivory affects plant–plant competition.
    https://doi.org/10.1016/j.baae.2015.04.009
  • Soil Biology & Biochemistry
    2015

    Community composition, diversity and metabolic footprints of soil nematodes in differently-aged temperate forests

    Xiaoke Zhang, Pingting Guan, Yaolei Wang, Qi Li, Shixiu Zhang, Zhiyong Zhang, T. Martijn Bezemer, Wenju Liang
    Abstract Soil nematode communities can provide important information about soil food web structure and function. However, how soil nematode communities and their metabolic footprints change over time in temperate forests is not well known. We examined the changes in the composition, diversity and metabolic footprints of soil nematode communities in three differently-aged (young, mid and old) forests of the Changbai Mountains, China. Carbon flows through different nematode trophic groups were also quantified based on nematode biomasses. The results showed that the highest abundance and diversity of total nematodes was found in the mid forest. Nematode communities were characterized by the replenishment in abundance but not the replacement of dominant genera. A low enrichment footprint in the young forest suggests a decline in available prey, while a high enrichment footprint in the mid forest indicates an increase in resource entry into soil food web. The relationship between the carbon flows of omnivores-predators and fungivores was stronger than that among other trophic groups. Our study shows that bottom-up effects of the vegetation, the soil environment and the connectedness of nematode trophic groups are all important driving forces for nematode community structure in temperate forests.
    https://doi.org/10.1016/j.soilbio.2014.10.003
  • Journal of Ecology
    2015

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


    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.
    https://doi.org/10.1111/1365-2745.12388
  • Ecology and Evolution
    2015

    Plant diversity and identity effects on predatory nematodes and their prey

    Olga Kostenko, Henk Duyts, Saskia S. Grootemaat, Gerlinde De Deyn, T. Martijn Bezemer
    There is considerable evidence that both plant diversity and plant identity can influence the level of predation and predator abundance aboveground. However, how the level of predation in the soil and the abundance of predatory soil fauna are related to plant diversity and identity remains largely unknown. In a biodiversity field experiment, we examined the effects of plant diversity and identity on the infectivity of entomopathogenic nematodes (EPNs, Heterorhabditis and Steinernema spp.), which prey on soil arthropods, and abundance of carnivorous non-EPNs, which are predators of other nematode groups. To obtain a comprehensive view of the potential prey/food availability, we also quantified the abundance of soil insects and nonpredatory nematodes and the root biomass in the experimental plots. We used structural equation modeling (SEM) to investigate possible pathways by which plant diversity and identity may affect EPN infectivity and the abundance of carnivorous non-EPNs. Heterorhabditis spp. infectivity and the abundance of carnivorous non-EPNs were not directly related to plant diversity or the proportion of legumes, grasses and forbs in the plant community. However, Steinernema spp. infectivity was higher in monocultures of Festuca rubra and Trifolium pratense than in monocultures of the other six plant species. SEM revealed that legumes positively affected Steinernema infectivity, whereas plant diversity indirectly affected the infectivity of Heterorhabditis EPNs via effects on the abundance of soil insects. The abundance of prey (soil insects and root-feeding, bacterivorous, and fungivorous nematodes) increased with higher plant diversity. The abundance of prey nematodes was also positively affected by legumes. These plant community effects could not be explained by changes in root biomass. Our results show that plant diversity and identity effects on belowground biota (particularly soil nematode community) can differ between organisms that belong to the same feeding guild and that generalizations about plant diversity effects on soil organisms should be made with great caution.
    https://doi.org/10.1002/ece3.1337
  • Global Change Biology Bioenergy
    2015

    The way forward in biochar research: targeting trade-offs between the potential wins

    S. Jeffery, T. Martijn Bezemer, Gerard Cornelissen, T.W. Kuyper, J. Lehmann, Liesje Mommer, S. Sohi, Tess Van de Voorde, David A. Wardle, J.W. Van Groenigen
    Biochar application to soil is currently widely advocated for a variety of reasons related to sustainability. Typically, soil amelioration with biochar is presented as a multiple-‘win’ strategy, although it is also associated with potential risks such as environmental contamination. The most often claimed benefits of biochar (i.e. the ‘wins’) include (i) carbon sequestration; (ii) soil fertility enhancement; (iii) biofuel/bioenergy production; (iv) pollutant immobilization; and (v) waste disposal. However, the vast majority of studies ignore possible trade-offs between them. For example, there is an obvious trade-off between maximizing biofuel production and maximizing biochar production. Also, relatively little attention has been paid to mechanisms, as opposed to systems impacts, behind observed biochar effects, often leaving open the question as to whether they reflect truly unique properties of biochar as opposed to being simply the short-term consequences of a fertilization or liming effect. Here, we provide an outline for the future of soil biochar research. We first identify possible trade-offs between the potential benefits. Second, to be able to better understand and quantify these trade-offs, we propose guidelines for robust experimental design and selection of appropriate controls that allow both mechanistic and systems assessment of biochar effects and trade-offs between the wins. Third, we offer a conceptual framework to guide future experiments and suggest guidelines for the standardized reporting of biochar experiments to allow effective between-site comparisons to quantify trade-offs. Such a mechanistic and systems framework is required to allow effective comparisons between experiments, across scales and locations, to guide policy and recommendations concerning biochar application to soil.
    https://doi.org/10.1111/gcbb.12132
  • Arthropod Plant Interactions
    2014

    Small-scale spatial resource partitioning in a hyperparasitoid community

    Jeff A. Harvey, Helen Snaas, Mima Malčická, Bertanne Visser, T. Martijn Bezemer
    Plant-herbivore-natural enemy associations underpin ecological communities, and such interactions may go up to four (or even more) trophic levels. Here, over the course of a growing season, we compared the diversity of secondary hyperparasitoids associated with a common host, Cotesia glomerata, a specialized larval endoparasitoid of cabbage butterfly caterpillars that in turn feed on brassicaceous plants. Cocoon clusters of C. glomerata were pinned to similar to 30 Brassica nigra plants by pinning them either to branches in the canopy (similar to 1.5 m high) or to the base of the stem near the ground. The cocoons were collected a week later and reared to determine which hyper-parasitoid species emerged from them. This was done in four consecutive months (June-September). Cocoons placed in the canopy were primarily attacked by specialized winged hyperparasitoids (Lysibia nana, Acrolyta nens), whereas cocoons on the ground were attacked by both winged and generalist wingless hyperparasitoids Gelis acarorum, G. agilis), although this changed with season. There was much more temporal variation in the diversity and number of species attacking cocoons in the canopy than on the ground; the abundance of L. nana and A. nens varied from month to month, whereas P. semotus was only prevalent in August. By contrast, G. acarorum was abundant in all of the samples placed near the ground. Our results show that hyperparasitoids partition host resources at remarkably small vertical spatial scales. We argue that spatial differences in the distribution of natural enemies can contribute to the diversity patterns observed in the field.
    https://doi.org/10.1007/s11829-014-9319-y
  • Annual Review of Entomology
    2014

    Response of native insect communities to invasive plants

    Invasive plants can disrupt a range of trophic interactions in native communities. As novel resource they can affect the performance of native insect herbivores and their natural enemies such as parasitoids and predators, and this can lead to host shifts of these herbivores and natural enemies. Through the release of volatile compounds, and by changing the chemical complexity of the habitat, invasive plants can also affect the behavior of native insects such as herbivores, parasitoids and pollinators. Studies that compare insects on related native and invasive plants in invaded habitats show that the abundance of insect herbivores is often lower on invasive plants, but that damage levels are similar. The impact of invasive plants on the population dynamics of resident insect species has been rarely examined, but invasive plants can influence the spatial and temporal dynamics of native insect (meta)populations and communities, ultimately leading to changes at the landscape level.
    https://doi.org/10.1146/annurev-ento-011613-162104
  • Agriculture, Ecosystems and Environment
    2014

    Soil amendment with biochar increases the competitive ability of legumes via increased potassium availability

    N.J. Oram, Tess Van de Voorde, G.J. Ouwehand, T. Martijn Bezemer, Liesje Mommer, S. Jeffery, J.W. van Groeningen
    Soil amendment with biochar is currently proposed as a management strategy to improve soil quality and enhance plant productivity. Relatively little is known about how biochar affects plant competition, although it has been suggested that it can increase the competitive ability of legumes. This study tested the impact of a biochar on the competitive ability of legumes through alterations to soil pH and/or nutrient availability. Biochar was produced from aboveground plant biomass from a species-rich semi-natural grassland pyrolysed at 400 °C. In a greenhouse experiment, a legume (red clover, Trifolium pratense L.); a grass (red fescue, Festuca rubra L.); and a forb (plantain, Plantago lanceolata L.) were grown in (1) monocultures, (2) in a mixed culture of red fescue and red clover, and (3) in a mixture of all three species. Soil treatments included fertilisation with nitrogen (N), potassium (K), phosphorus (P), or micronutrient fertiliser in the presence or absence of biochar; a pH-adjusted control soil; and a control (i.e. with no amendment). The competitive ability of red clover was quantified as the proportion of aboveground biomass of this species within the mixtures. Both biochar amendment and K fertilisation significantly (P <0.001) increased red clover biomass, and increased the competitive ability of red clover when grown with red fescue and plantain. Application of N fertiliser, irrespective of biochar amendment, resulted in significantly (P <0.001) greater red fescue and plantain biomass and eliminated the competitive advantage of red clover. The biochar-mediated pH increase did not affect red clover biomass or its competitive ability. We conclude that biochar has a beneficial effect on red clover under N limiting conditions due to an increase in K availability. Our results suggest a potential role for biochar to maintain the proportion of forage legumes in agricultural pastures or semi-natural grasslands.
    https://doi.org/10.1016/j.agee.2014.03.031
  • Ecological Applications
    2014

    Soil biochar amendment in a nature restoration area: effects on plant productivity and community composition

    Tess Van de Voorde, T. Martijn Bezemer, J.W. Van Groenigen, S. Jeffery, Liesje Mommer
    Biochar (pyrolyzed biomass) amendment to soils has been shown to have a multitude of positive effects, e.g., on crop yield, soil quality, nutrient cycling, and carbon sequestration. So far the majority of studies have focused on agricultural systems, typically with relatively low species diversity and annual cropping schemes. How biochar amendment affects plant communities in more complex and diverse ecosystems that can evolve over time is largely unknown. We investigated such effects in a field experiment at a Dutch nature restoration area. In April 2011, we set up an experiment using biochar produced from cuttings collected from a local natural grassland. The material was pyrolyzed at 400 degrees C or at 600 degrees C. After biochar or residue (non-pyrolyzed cuttings) application (10 Mg/ha), all plots, including control (0 Mg/ha) plots, were sown with an 18-species grassland mixture. In August 2011, we determined characteristics of the developed plant community, as well as soil nutrient status. Biochar amendment did not alter total plant productivity, but it had a strong and significant effect on plant community composition. Legumes were three times as abundant and individual legume plants increased four times in biomass in plots that received biochar as compared to the control treatment. Biomass of the most abundant forb (Plantago lanceolata) was not affected by biochar addition. Available phosphorous, potassium, and pH were significantly higher in soils that received biochar than in Control soils. The rate of biological nitrogen fixation and seed germination were not altered by biochar amendment, but the total amount of biological N fixed per Trifolium pratense (red clover) plant was more than four times greater in biochar-amended soil. This study demonstrates that biochar amendment has a strong and rapid effect on plant communities and soil nutrients. Over time these changes may cascade up to other trophic groups, including above-and belowground organisms. Our results emphasize the need for long-term studies that examine not only the short-term effects of biochar amendment, but also follow how these effects evolve over time and affect ecosystem functioning.
    https://doi.org/10.1890/13-0578.1
  • Agriculture, Ecosystems and Environment
    2014

    Biochar application rate affects biological nitrogen fixation in red clover conditional on potassium availability

    S. Mia, J.W. van Groeningen, Tess Van de Voorde, N.J. Oram, T. Martijn Bezemer, Liesje Mommer, S. Jeffery
    Increased biological nitrogen fixation (BNF) by legumes has been reported following biochar application to soils, but the mechanisms behind this phenomenon remain poorly elucidated. We investigated the effects of different biochar application rates on BNF in red clover (Trifolium pratense L.). Red clover was grown in mono or mixed cultures with red fescue grass (Festuca rubra L.) and plantain (Plantago lanceolata L.) at a range of different biochar application rates (0, 10, 50 and 120 t ha−1). In a separate experiment, nutrient effects of biochar on BNF were investigated using nitrogen, phosphorous and potassium (N, P and K) and micronutrient fertilization using the same plant species. Biochar addition increased BNF and biochar applied at a rate of 10 t ha−1 led to the highest rate of BNF. Total biomass also showed the greatest increase at this application rate. An application rate of 120 t ha−1 significantly decreased biomass production in both single and mixed cultures when compared to the control, with the greatest reduction occurring in red clover. Furthermore, BNF was significantly higher in pots in which red clover was grown in mixed cultures compared to monocultures. In the absence of biochar, K fertilization caused a significant increase in BNF. For N, P, and micronutrient fertilization, BNF did not significantly differ between treatments with and without biochar addition. We conclude that different biochar application rates lead to different effects in terms of BNF and biomass production. However, due to the high variety of biochar properties, different application rates should be investigated on a case specific basis to determine the optimum biochar application strategies.
    https://doi.org/10.1016/j.agee.2014.03.011
  • Basic and Applied Ecology
    2014

    Reciprocal interactions between native and introduced populations of common milkweed, Asclepias syriaca, and the specialist aphid, Aphis nerii

    Tibor Bukovinszky, R. Gols, A.A. Agrawal, C. Roge, T. Martijn Bezemer, Arjen Biere, Jeff A. Harvey
    Following its introduction into Europe (EU), the common milkweed (Asclepias syriaca) has been free of most specialist herbivores that are present in its native North American (NA) range, except for the oleander aphid Aphis nerii. We compared EU and NA populations of A. nerii on EU and NA milkweed populations to test the hypothesis that plant–insect interactions differ on the two continents. First, we tested if herbivore performance is higher on EU plants than on NA plants, because the former have escaped most of their herbivores and have perhaps been selected for lower defence levels following introduction. Second, we compared two A. nerii lines (one from each continent) to test whether genotypic differences in the herbivore may influence species interactions in plant–herbivore communities in the context of species introductions. The NA population of A. nerii developed faster, had higher fecundity and attained higher population growth rates than the EU population. There was no overall significant continental difference in aphid resistance between the plants. However, milkweed plants from EU supported higher population growth rates and faster development of the NA line of A. nerii than plants from NA. In contrast, EU aphids showed similar (low) performance across plant populations from both continents. In a second experiment, we examined how chewing herbivores indirectly mediate interactions between milkweeds and aphids, and induced A. syriaca plants from each continent by monarch caterpillars (Danaus plexippus) to compare the resulting changes in plant quality on EU aphid performance. As specialist chewing herbivores of A. syriaca are only present in NA, we expected that plants from the two continents may affect aphid growth in different ways when they are challenged by a specialist chewing herbivore. Caterpillar induction decreased aphid developmental times on NA plants, but not on EU plants, whereas fecundity and population growth rates were unaffected by induction on both plant populations. The results show that genetic variation in the plants as well as in the herbivores can determine the outcome of plant–herbivore interactions.
    https://doi.org/10.1016/j.baae.2014.07.004
  • Oecologia
    2014

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

    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
    https://doi.org/10.1007/s00442-014-2885-y
  • Basic and Applied Ecology
    2014

    Biochars produced from individual grassland species differ in their effect on plant growth

    Tess Van de Voorde, F. Van Noppen, R.W. Nacheniusc, W.P. Prins, Liesje Mommer, J.W. Van Groenigen, T. Martijn Bezemer
    Biochar, pyrolyzed biomass, has been shown to be a promising way to improve plant productivity and soil quality. Biochar characteristics and its effect on plant performance depend strongly on the type of feedstock from which it is made. However, whether biochars produced from individual grassland species differ in their characteristics and effects on plant growth when applied to soil is poorly understood. The aim of this study was to examine how soil application of pyrolyzed and non-pyrolyzed biomass originating from different grassland species influences plant performance. We measured the growth of the forb Jacobaea vulgaris in soil amended with pyrolyzed or non-pyrolyzed biomass of seven different plant species, and in control soil without amendments. The characteristics (nutrient content, C:N) and effects on plant growth of both pyrolyzed and non-pyrolyzed biomass differed significantly between species from which the biomass originated (‘feedstock species’). For most feedstock species there was no relationship between the effects that the pyrolyzed and the non-pyrolyzed biomass had on plant performance. Our results show that pyrolyzed grassland species differ in their characteristics and their effect on plant growth when amended to soil. This shows that it is important to test what the effect of pyrolysing a chosen feedstock is on a species before applying it on a larger scale and that potentially biochar with predefined effects could be designed for specific purposes.
    https://doi.org/10.1016/j.baae.2013.12.005
  • Journal of Applied Ecology
    2013

    Sustaining ecosystem functions in a changing world: a call for an integrated approach

    H. Tomimatsu, T. Sasaki, J.R. Bridle, C. Fontaine, J. Kitano, D.B. Stouffer, M. Vellend, T. Martijn Bezemer, T. Fukami, E.A. Hadly, Marcel G. A. van der Heijden, M. Kawata, S. Kéfi, N.J.B. Kraft, K.S. McCann, P.J. Mumby, T. Nakashizuka, O.L. Petchey, T.N. Romanuk, K.N. Suding, G. Takimoto, J. Urabe, S. Yachi
    With ever-increasing human pressure on ecosystems, it is critically important to predict how ecosystem functions will respond to such human-induced perturbations. We define perturbations as either changes to abiotic environment (e.g. eutrophication, climate change) that indirectly affects biota, or direct changes to biota (e.g. species introductions). While two lines of research in ecology, biodiversity–ecosystem function (BDEF) and ecological resilience (ER) research, have addressed this issue, both fields of research have nontrivial shortcomings in their abilities to address a wide range of realistic scenarios. We outline how an integrated research framework may foster a deeper understanding of the functional consequences of perturbations via simultaneous application of (i) process-based mechanistic predictions using trait-based approaches and (ii) detection of empirical patterns of functional changes along real perturbation gradients. In this context, the complexities of ecological interactions and evolutionary perspectives should be integrated into future research. Synthesis and applications. Management of human-impacted ecosystems can be guided most directly by understanding the response of ecosystem functions to controllable perturbations. In particular, we need to characterize the form of a wide range of perturbation–function relationships and to draw connections between those patterns and the underlying ecological processes. We anticipate that the integrated perspectives will also be helpful for managers to derive practical implications for management from academic literature.
    https://doi.org/10.1111/1365-2664.12116
  • BioScience
    2013

    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.
    https://doi.org/10.1525/bio.2013.63.1.8
  • Frontiers in Plant Science
    2013

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

    (Gera) W.H.G. Hol, T. Martijn Bezemer, Arjen Biere
    Plant growth-promoting rhizobacteria (PGPR) are increasingly appreciated for their contributions to primary productivity through promotion of growth and triggering of induced systemic resistance in plants. Here we focus on the beneficial effects of one particular species of PGPR (Pseudomonas fluorescens) on plants through induced plant defense. This model organism has provided much understanding of the underlying molecular mechanisms of PGPR-induced plant defense. However, this knowledge can only be appreciated at full value once we know to what extent these mechanisms also occur under more realistic, species-diverse conditions as are occurring in the plant rhizosphere. To provide the necessary ecological context, we review the literature to compare the effect of P. fluorescens on induced plant defense when it is present as a single species or in combination with other soil dwelling species. Specifically, we discuss combinations with other plant mutualists (bacterial or fungal), plant pathogens (bacterial or fungal), bacterivores (nematode or protozoa), and decomposers. Synergistic interactions between P. fluorescens and other plant mutualists are much more commonly reported than antagonistic interactions. Recent developments have enabled screenings of P. fluorescens genomes for defense traits and this could help with selection of strains with likely positive interactions on biocontrol. However, studies that examine the effects of multiple herbivores, pathogens, or herbivores and pathogens together on the effectiveness of PGPR to induce plant defenses are underrepresented and we are not aware of any study that has examined interactions between P. fluorescens and bacterivores or decomposers. As co-occurring soil organisms can enhance but also reduce the effectiveness of PGPR, a better understanding of the biotic factors modulating P. fluorescens–plant interactions will improve the effectiveness of introducing P. fluorescens to enhance plant production and defense.
    https://doi.org/10.3389/fpls.2013.00081
  • Journal of Ecology
    2013

    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.
    https://doi.org/10.1111/1365-2745.12045
  • Basic and Applied Ecology
    2013

    Intraspecific variation in plant size, secondary plant compounds, herbivory and parasitoid assemblages during secondary succession

    Olga Kostenko, T. Martijn Bezemer
    During secondary succession on abandoned agricultural fields the diversity and abundance of insect communities often increases, whereas the performance and nutritional quality of early successional plants often declines. As the diversity and abundance of insects on a single plant are determined by characteristics of the environment as well as of the host plant, it is difficult to predict how insects associated with a single plant species will change during succession. We examined how plant characteristics of the early successional plant species ragwort (Jacobaea vulgaris), and the herbivores and parasitoids associated with these plants change during secondary succession. In ten grasslands that differed in time since abandonment (3–26 years), we measured the size and primary and secondary chemistry of individual ragwort plants. For each plant we also recorded the presence of herbivores in flowers, leaves and stems, and reared parasitoids from these plant parts. Ragwort plants were significantly larger but had lower nitrogen concentrations in recently abandoned sites than in older sites. Pyrrolizidine alkaloid (PA) composition varied among plants within sites but also differed significantly among sites. However, there was no relationship between the age of a site and PA composition. Even though plant size decreased with time since abandonment, the abundance of stem-boring insects and parasitoids emerging from stems significantly increased with site age. The proportion of plants with flower and leaf herbivory and the number of parasitoids emerging from flowers and leaves was not related to site age. Parasitoid diversity significantly increased with site age. The results of our study show that ragwort and insect characteristics both change during secondary succession, but that insect herbivore and parasitoid abundances are not directly related to plant size or nutritional quality.
    https://doi.org/10.1016/j.baae.2013.02.006
  • Journal of Ecology
    2013

    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.
    https://doi.org/10.1111/1365-2745.12054
  • Journal of Chemical Ecology
    2013

    Effects of root herbivory on pyrrolizidine alkaloid content and aboveground plant-herbivore-parasitoid interactions in Jacobaea vulgaris

    Olga Kostenko, P.P.J. Mulder, T. Martijn Bezemer
    The importance of root herbivory is increasingly recognized in ecological studies, and the effects of root herbivory on plant growth, chemistry, and performance of aboveground herbivores have been relatively well studied. However, how belowground herbivory by root feeding insects affects aboveground parasitoid development is largely unknown. In this study, we examined the effects of root herbivory by wireworms (Agriotes lineatus) on the expression of primary and secondary compounds in the leaves and roots of ragwort (Jacobaea vulgaris). We also studied the effects of root herbivory on the performance of a generalist aboveground herbivore, Mamestra brassicae and its parasitoid Microplitis mediator. In contrast to what most other studies have reported, root herbivory in J. vulgaris had a strong negative effect on the total concentration of pyrrolizidine alkaloids (PAs) in shoot tissues. The composition of PAs in the shoots also changed after root herbivory. In particular, the concentration of less toxic N-oxide PAs decreased. There was no significant effect of root herbivory on PA composition and concentration in the roots. Although the concentration of PA in the leaves decreased, M. brassicae tended to grow slower on the plants exposed to root herbivory. Parasitoid performance was not affected by root herbivory, but parasitoids developed faster when the concentration of jacobine-type PAs in the foliage was higher. These results point at a putative role of individual PAs in multitrophic interactions and emphasize that generalizations about aboveground-belowground effects should be made with great caution.
    https://doi.org/10.1007/s10886-012-0234-3
  • Journal of Insect Behavior
    2013

    A device to study the behavioral responses of zooplankton to food quality and quantity

    Tibor Bukovinszky, Nico Helmsing, R.A. Grau, (Liesbeth) E.S. Bakker, T. Martijn Bezemer, Matthijs Vos, H. Uittenhout, Anthony M. Verschoor
    In order to explore the behavioral mechanisms underlying aggregation of foragers on local resource patches, it is necessary to manipulate the location, quality and quantity of food patches. This requires careful control over the conditions in the foraging arena, which may be a challenging task in the case of aquatic resourceconsumer systems, like that of freshwater zooplankton feeding on suspended algal cells. We present an experimental tool designed to aid behavioral ecologists in exploring the consequences of resource characteristics for zooplankton aggregation behavior and movement decisions under conditions where the boundaries and characteristics (quantity and quality) of food patches can be standardized. The aggregation behavior of Daphnia magna and D. galeata x hyalina was tested in relation to i) the presence or absence of food or ii) food quality, where algae of high or low nutrient (phosphorus) content were offered in distinct patches. Individuals of both Daphnia species chose tubes containing food patches and D. galeata x hyalina also showed a preference towards food patches of high nutrient content. We discuss how the described equipment complements other behavioral approaches providing a useful tool to understand animal foraging decisions in environments with heterogeneous resource distributions.
    https://doi.org/10.1007/s10905-012-9366-0
  • Basic and Applied Ecology
    2013

    Local variation in conspecific plant density influences plant-soil feedback in a natural grassland

    Martine Kos, Johan Veendrick, T. Martijn Bezemer
    Several studies have argued that under field conditions plant–soil feedback may be related to the local density of a plant species, but plant–soil feedback is often studied by comparing conspecific and heterospecific soils or by using mixed soil samples collected from different locations and plant densities. We examined whether the growth of the early successional species Jacobaea vulgaris in soil collected from the field is related to the local variation in plant density of this species. In a grassland restoration site, we selected eight 8 m × 8 m plots, four with high and four with low densities of J. vulgaris plants. In 16 subplots in each plot we recorded the density and size of J. vulgaris, and characteristics of the vegetation and the soil chemistry. Soil collected from each subplot was used in a greenhouse pot-experiment to study the growth of J. vulgaris, both in pure field soil and in sterile soil inoculated with a small part of field soil. In the field, flowering J. vulgaris plants were taller, the percentage of rosette plants was higher and seed density was larger in High- than in Low-density plots. In the pot experiment, J. vulgaris had a negative plant–soil feedback, but biomass was also lower in soil collected from High- than from Low-density plots, although only when growing in inoculated soil. Regression analyses showed that J. vulgaris biomass of plants growing in pure soil was related to soil nutrients, but also to J. vulgaris density in the field. We conclude that in the field there is local variation in the negative plant–soil feedback of J. vulgaris and that this variation can be explained by the local density of J. vulgaris, but also by other factors such as nutrient availability.
    https://doi.org/10.1016/j.baae.2013.07.002
  • Basic and Applied Ecology
    2012

    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.
    https://doi.org/10.1016/j.baae.2012.08.012
  • Entomologia Experimentalis et Applicata
    2012

    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.
    https://doi.org/10.1111/j.1570-7458.2012.01251.x
  • Ecological Research
    2012

    The effects of CO2 and nutrient enrichment on photosynthesis and growth of Poa annua in two consecutive generations

    T. Martijn Bezemer, T.H. Jones
    We studied short- and long-term growth responses of Poa annua L. (Gramineae) at ambient and elevated (ambient +200 lmol mol 1) atmospheric CO2. In experiment 1 we compared plant growth during the early, vegetative and final, reproductive growth phases. Plant growth in elevated CO2 was significantly enhanced during the early phase, but this was reversed in the reproductive phase. Seed mass and percentage germination were significantly reduced in elevated CO2. Experiment 2 tested for the impact of transgenerational and nutrient effects on the response of Poa annua to elevated CO2. Plants were grown at ambient and elevated CO2 for one or two consecutive generations at three soil nutrient levels. Leaf photosynthesis was significantly higher at elevated CO2, but was also affected by both soil nutrient status and plant generation. Plants grown at elevated CO2 and under conditions of low nutrient availability showed photosynthetic acclimation after 12 weeks of growth but not after 6 weeks. Firstgeneration growth remained unaffected by elevated CO2, while second-generation plants produced significantly more tillers and flowers when grown in elevated CO2 compared to ambient conditions. This effect was strongest at low nutrient availability. Average above- and belowground biomass after 12 weeks of growth was enhanced in elevated CO2 during both generations, but more so during plant generation 2. This study demonstrates the importance of temporal/maternal effects in plant responses to elevated CO2.
    https://doi.org/10.1007/s11284-012-0961-5
  • Acta Oecologica
    2012

    Arbuscular mycorrhizal colonization, plant chemistry, and aboveground herbivory on Senecio jacobaea

    S. Reidinger, R. Eschen, A.C. Gange, P. Finch, T. Martijn Bezemer
    Arbuscular mycorrhizal fungi (AMF) can affect insect herbivores by changing plant growth and chemistry. However, many factors can influence the symbiotic relationship between plant and fungus, potentially obscuring experimental treatments and ecosystem impacts. In a field experiment, we assessed AMF colonization levels of individual ragwort (Senecio jacobaea) plants growing in grassland plots that were originally sown with 15 or 4 plant species, or were unsown. We measured the concentrations of carbon, nitrogen and pyrrolizidine alkaloids (PAs), and assessed the presence of aboveground insect herbivores on the sampled plants. Total AMF colonization and colonization by arbuscules was lower in plots sown with 15 species than in plots sown with 4 species and unsown plots. AMF colonization was positively related to the cover of oxeye daisy (Leucanthemum vulgare) and a positive relationship between colonization by arbuscules and the occurrence of a specialist seed-feeding fly (Pegohylemyia seneciella) was found. The occurrence of stem-boring, leaf-mining and sap-sucking insects was not affected by AMF colonization. Total PA concentrations were negatively related to colonization levels by vesicles, but did not differ among the sowing treatments. No single factor explained the observed differences in AMF colonization among the sowing treatments or insect herbivore occurrence on S. jacobaea. However, correlations across the treatments suggest that some of the variation was due to the abundance of one plant species, which is known to stimulate AMF colonization of neighbouring plants, while AMF colonization was related to the occurrence of a specialist insect herbivore. Our results thus illustrate that in natural systems, the ecosystem impact of AMF through their influence on the occurrence of specialist insects can be recognised, but they also highlight the confounding effect of neighbouring plant species identity. Hence, our results emphasise the importance of field studies to elucidate interactions between AMF and organisms of different trophic levels.
    https://doi.org/10.1016/j.actao.2011.08.003
  • PLoS One
    2012

    The Good, the Bad and the Plenty: Interactive Effects of Food Quality and Quantity on the Growth of Different Daphnia Species

    Tibor Bukovinszky, Anthony M. Verschoor, Nico Helmsing, T. Martijn Bezemer, (Liesbeth) E.S. Bakker, Matthijs Vos, Lisette de Senerpont Domis
    Effects of food quality and quantity on consumers are neither independent nor interchangeable. Although consumer growth and reproduction show strong variation in relation to both food quality and quantity, the effects of food quality or food quantity have usually been studied in isolation. In two experiments, we studied the growth and reproduction in three filter-feeding freshwater zooplankton species, i.e. Daphnia galeata x hyalina, D. pulicaria and D. magna, on their algal food (Scenedesmus obliquus), varying in carbon to phosphorus (C:P) ratios and quantities (concentrations). In the first experiment, we found a strong positive effect of the phosphorus content of food on growth of Daphnia, both in their early and late juvenile development. Variation in the relationship between the P-content of animals and their growth rate reflected interspecific differences in nutrient requirements. Although growth rates typically decreased as development neared maturation, this did not affect these species-specific couplings between growth rate and Daphnia P-content. In the second experiment, we examined the effects of food quality on Daphnia growth at different levels of food quantity. With the same decrease in P-content of food, species with higher estimated P-content at zero growth showed a larger increase in threshold food concentrations (i.e. food concentration sufficient to meet metabolic requirements but not growth). These results suggest that physiological processes such as maintenance and growth may in combination explain effects of food quality and quantity on consumers. Our study shows that differences in response to variation in food quality and quantity exist between species. As a consequence, species-specific effects of food quality on consumer growth will also determine how species deal with varying food levels, which has implications for resource-consumer interactions.
    https://doi.org/10.1371/journal.pone.0042966
  • Soil Biology & Biochemistry
    2012

    Soil inoculation method determines the strength of plant–soil interactions

    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.
    https://doi.org/10.1016/j.soilbio.2012.05.020
  • Basic and Applied Ecology
    2012

    Host location success of root-feeding nematodes in patches that differ in size and quality: A belowground release-recapture experiment

    Tibor Bukovinszky, (Liesbeth) E.S. Bakker, Ciska Raaijmakers, Anthony M. Verschoor, T. Martijn Bezemer
    Resource patchsize and patch nutritional quality are both important factors influencing local densities of herbivores. The responses of herbivores to resource patchsize have been mostly studied in aboveground plant–insect interactions, whereas belowground organisms have received little attention. We studied responses of different root-feedingnematode species associated with marram grass (Ammophila arenaria (L.) Link) to resource patchsize and quality. Different nematode species were released in experimental mesocosms filled with dune sand in which we established marram grass patches of varying sizes. Half of the patches of small, medium and large size were fertilized to test if immigration probabilities of nematodes depended on patch quality. We tested the hypotheses that (1) nematodes should aggregate on larger patches and (2) colonization of patches would also depend on patch nutritional quality, with higher nematoderecapture rates expected in fertilized patches. Two species (Helicotylenchus pseudorobustus, Hemicycliophora thornei) of the five released species were recaptured in the experiment. The fraction of nematodes immigrating into the rhizosphere of a plant patch increased with patchsize (i.e. root biomass), which was in line with predictions of the Resource Concentration Hypothesis. When fractions were recalculated to represent recapture rates per liter of soil, recapture rates of nematodes did not differ among patchsizes, indicating that the increase in recapture rates was directly proportional to the increase in patchsize. This suggests that the process through which nematodes located patches was not distinguishable from a random process where entering patches is based on random encounters with patch boundaries. In contrast to our expectation, fertilization had a strong negative effect on patch responses of both nematode species. Our study represents an approach that may be used to explore whether belowground biota behave in similar ways as aboveground biota, in order to determine how perceived differences in environments affect ecological interactions.
    https://doi.org/10.1016/j.baae.2012.03.002
  • Journal of Chemical Ecology
    2012

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

    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.
    https://doi.org/10.1007/s10886-012-0104-z
  • Soil Biology & Biochemistry
    2012

    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.
    https://doi.org/10.1016/j.soilbio.2011.10.006
  • Basic and Applied Ecology
    2012

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

    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.
    https://doi.org/10.1016/j.baae.2012.10.005
  • Ecology Letters
    2012

    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.
    https://doi.org/10.1111/j.1461-0248.2012.01801.x
  • Oikos
    2011

    Intrinsic competition between two secondary hyperparasitoids results in temporal trophic switch

    Jeff A. Harvey, F. Pashalidou, Roxina Soler , T. Martijn Bezemer
    Interspecific competition amongst parasitoids is important in shaping the evolution of life-history strategies in these insects as well as community structure. Competition for hosts may occur between adult female parasitoids (‘extrinsic’ competition) or their progeny (‘intrinsic’ competition). Here, we examined intrinsic competition between two solitary secondary hyperparasitoids, Lysibia nana and Gelis agilis in cocoons of a primary parasitoid, Cotesia glomerata. Each species was allowed to sting hosts previously parasitized by the other at 24 h time intervals over the course of 144 h (6 days). When hosts were attacked simultaneously, neither species was dominant although the species to attack first won most encounters when it had a 24–48 h head start. However, after this time there was dramatic shift in the outcome with G. agilis dominating in all hosts > 72-h old, regardless of which species had parasitized C. glomerata first. G. agilis larvae, which initially had competed with L. nana for control of C. glomerata resources, began attacking the larvae of L. nana, whereas L. nana rejected hosts with older G. agilis larvae or pupae. Effects of multiparasitism also affected the development time and adult mass of the winning parasitoid. Our results reveal a shift in the trophic status of G. agilis from C. glomerata (in younger hosts) to L. nana (in older hosts), the first time such a phenomenon has been reported in parasitoids.
    https://doi.org/10.1111/j.1600-0706.2010.18744.x
  • Journal of Ecology
    2011

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

    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.
    https://doi.org/10.1111/j.1365-2745.2011.01815.x
  • Ecology
    2011

    Recovery of plant species richness during long-term fertilization of a species-rich grassland

    M. Pierik, Jasper van Ruijven, T. Martijn Bezemer, R.H.E.M. Geerts, Frank Berendse
    Nutrient enrichment of habitats (eutrophication) is considered to be one of the main causes of plant diversity decline worldwide. Several experiments have shown a rapid loss of species in the first years after fertilization started. However, little is known about changes in species richness in the long term. Here, we use a 50-year-old field experiment with a range of fertilization treatments in grasslands that were mown twice each year in the center of The Netherlands. We show that species richness in all plots initially declined but started to recover after ;25 years of continued fertilization. This was also true for the heavily fertilized treatment (NPK). In NPK-fertilized plots, the decline was strongest and associated with a strong divergence of plant trait composition from the control, reflecting a shift to a plant community adapted to nutrient-rich conditions. During the subsequent period of increase in species richness, the trait composition remained stable. These results show that plant species richness can, at least partially, recover after an initial diversity decline caused by fertilization.
    https://doi.org/10.1890/10-0210.1
  • Entomologia Experimentalis et Applicata
    2010

    Impacts of belowground herbivory on oviposition decisions in two congeneric butterfly species

    Roxina Soler , Jeff A. Harvey, R. Rouchet, Sonja Schaper, T. Martijn Bezemer
    Root-feeding insects can affect the performance of aboveground insect herbivores when they are forced to feed on the same host plant. Here we explored whether the oviposition behaviour of two closely related herbivorous species (cabbage butterflies; Lepidoptera: Pieridae) is influenced by root-feeding insects, when they are given the chance to choose between host plants with and without root herbivores. Considering that egg load is an important physiological factor influencing the foraging behaviour of insects, we also examined whether root-feeding insects differentially influence oviposition preference in butterflies with low and high egg loads. Oviposition preference in both butterfly species with low and high egg loads was monitored using host plants with and without root herbivores. To ascertain the status of butterfly age with low and high egg loads, the oviducts of a separate group of butterflies was dissected to record the number of immature and mature eggs in butterflies of various ages. Pieris brassicae L. butterflies with low egg loads preferred plants without root herbivores over plants with root herbivores, and laid more egg clutches on the leaves of plants that were not attacked by root herbivores. Butterflies with comparatively high egg loads also selected a larger proportion of plants without root herbivores, but laid a similar number of egg clutches on the plant shoots independent of the presence or absence of root herbivores belowground. Independent of the age and egg load, Pieris rapae L. butterflies selected a larger proportion of plants not attacked by root herbivores to lay eggs, but the number of eggs laid was similar in plants with and without root herbivores. This study shows that belowground insects can influence behavioural decisions of aboveground insect herbivores. Interestingly, the strength of these interactions depends on the physiological state of the insects which is probably correlated with their perception of environmental quality.
    https://doi.org/10.1111/j.1570-7458.2010.01015.x
  • Environmental Microbiology
    2010

    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.
    https://doi.org/10.1111/j.1462-2920.2009.02053.x
  • Ecological Entomology
    2010

    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.
    https://doi.org/10.1111/j.1365-2311.2010.01184.x
  • Oecologia
    2010

    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.
    https://doi.org/10.1007/s00442-009-1526-3
  • New Phytologist
    2010

    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.
    https://doi.org/10.1111/j.1469-8137.2010.03216.x
  • Ecology
    2010

    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.
    https://doi.org/10.1890/09-2198.1
  • Global Change Biology
    2010

    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.
    https://doi.org/10.1111/j.1365-2486.2009.01996.x
  • Basic and Applied Ecology
    2010

    Combined effects of patch size and plant nutritional quality on local densities of insect herbivores

    Tibor Bukovinszky, R. Gols, A.F.D. Kamp, F. De Oliveira-Domingues, P.A. Hambäck, Y. Jongema, T. Martijn Bezemer, Marcel Dicke, Nicole M. van Dam, Jeff A. Harvey
    Plant–insect interactions occur in spatially heterogeneous habitats. Understanding how such interactions shape density distributions of herbivores requires knowledge on how variation in plant traits (e.g. nutritional quality) affects herbivore abundance through, for example, affecting movement rates and aggregation behaviour. We studied the effects of plant patch size and herbivore-induced differences in plant nutritional quality on local densities of insect herbivores for two Brassica oleracea cultivars, i.e. white cabbage and Brussels sprouts. Early season herbivory as a treatment resulted in measurable differences in glucosinolate concentrations in both cultivars throughout the season. Herbivore induction and patch size both influenced community composition of herbivores in both cultivars, but the effects differed between species. Flea beetles (Phyllotreta spp.) were more abundant in large than in small patches, and this patch response was more pronounced on white cabbage than on Brussels sprouts. Herbivore-induction increased densities in all patches. Thrips tabaci was also more abundant in large patches and densities of this species were higher on Brussels sprouts than on white cabbage. Thrips densities were lower on induced than on control plants of both cultivars and this negative effect of induction tended to be more pronounced in large than in small patches. Densities of the cabbage moth (Mamestra brassicae) were lower on Brussels sprouts than on white cabbage and lower on herbivore-induced than on uninduced plants, with no effect of patch size. No clear effects of patch size and induction were found for aphids. This study shows that constitutive and herbivore-induced differences in plant traits interact with patch responses of insect herbivores.
    https://doi.org/10.1016/j.baae.2010.04.005
  • Journal of Vegetation Science
    2010

    Travelling to a former sea floor: colonization of forests by understorey plant species on land recently reclaimed from the sea

    M. Pierik, Jasper van Ruijven, T. Martijn Bezemer, Frank Berendse
    Questions: What are important forest characteristics determining colonization of forest patches by forest understorey species? Location: Planted forests on land recently reclaimed from the sea, the Netherlands. Methods: We related the distribution of forest specialist species in the understorey of 55 forests in Dutch IJsselmeer polders to the following forest characteristics: age, area, connectivity, distance to mainland (as a proxy for distance to seed source) and path density. We used species of the Fraxino-Ulmetum association for the Netherlands as reference for species that could potentially occur in the study area. Results: Area and age of the surveyed forests explained a large part of the variation in overall species composition and species number of forest plant species. The importance of connectivity and distance to the mainland of forest habitats became apparent only at a more detailed level of dispersal groups and individual species. The importance of forest parameters differed between dispersal groups and also between individual species. After 60 years, 75% of the potential pool of wind-dispersed spe Conclusions: The data strongly suggest that the colonization process in polder forests is still in its initial phase, during which easily dispersed species dominate the vegetation. Colonization success of common species that lack adaptations to long-distance dispersal is affected by spatial configuration of the forests, and most rare species that could potentially occur in these forests are still absent. Implications for conservation of rare species in fragmented landscapes are discussed.
    https://doi.org/10.1111/j.1654-1103.2009.01134.x
  • Ecological Entomology
    2009

    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.
    https://doi.org/10.1111/j.1365-2311.2008.01082.x
  • Oecologia
    2009

    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.
    https://doi.org/10.1007/s00442-009-1351-8
  • Entomologia Experimentalis et Applicata
    2009

    Life-history traits in closely related secondary parasitoids sharing the same primary parasitoid host: evolutionary opportunities and constraints

    Thus far, few studies have compared life-history traits amongst secondary parasitoids attacking and developing in cocoons of their primary parasitoid hosts. This study examines development and reproduction in Lysibia nana Gravenhorst and Acrolyta nens Hartig (both Hymenoptera: Ichneumonidae), two related and morphologically similar secondary parasitoids that attack pupae of the gregarious endoparasitoid, Cotesia glomerata L. (Hymenoptera: Braconidae). On black mustard, Brassica nigra L. (Brassicaceae) plants in a field plot, adults of L. nana and A. nens frequently emerged from the same cocoon broods of C. glomerata. Based on similarities in their phylogeny and morphology, it was hypothesized that both species would exhibit considerable overlap in other life-history traits. In both L. nana and A. nens, adult wasp size increased with host cocoon mass at parasitism, although L. nana wasps were slightly larger than A. nens wasps, and completed their development earlier. Adult females of both species emerged with no eggs but matured eggs at similar rates over the following days. When provided with 20 host cocoons daily, fecundity in female L. nana was slightly more skewed towards early life than in A. nens, although lifetime fecundity did not differ between the two species. Longevity was significantly reduced in females of both species that were provided with hosts. Both parasitoids were found to exhibit strong similarities in life-history and development traits and in their ecological niche, thereby supporting our general hypothesis. Competition between L. nana and A. nens is presumably diffused because their preferred host (C. glomerata) is relatively abundant in open habitats.
    https://doi.org/10.1111/j.1570-7458.2009.00882.x
  • Acta Oecologica
    2009

    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.
    https://doi.org/10.1016/j.actao.2009.05.006
  • Journal of Animal Ecology
    2009

    Interactions to the fifth trophic level: secondary and tertiary parasitoid wasps show extraordinary efficiency in utilizing host resources

    1. Parasitoid wasps are highly efficient organisms at utilizing and assimilating limited resources from their hosts. This study explores interactions over three trophic levels, from the third (primary parasitoid) to the fourth (secondary parasitoid) and terminating in the fifth (tertiary parasitoid). 2. Host utilization and adult body mass of the secondary and tertiary parasitoid Gelis agilis was determined when developing on pre-pupae of its primary parasitoid host, Cotesia glomerata, and from pre-pupae of another secondary parasitoid, Lysibia nana that had developed initially on pre-pupae of C. glomerata. 3. In both C. glomerata and G. agilis, the body mass of emerging adult parasitoids was strongly positively correlated with initial cocoon mass. For a given cocoon mass at parasitism, emerging adult G. agilis wasps were almost 90% as large as C. glomerata adults developing in healthy cocoons of comparable mass. Furthermore, G. agilis adults were still 75% as large as C. glomerata adults even when developing on L. nana that in turn had developed on C. glomerata. Otherwise, in terms of adult body mass 4. Analyses of carbon and nitrogen in body tissues of the parasitoids over the third to the fifth trophic level revealed that percentage nitrogen was higher and carbon lower in G. agilis and L. nana than in C. glomerata. Furthermore, percentage carbon was lower in adult G. agilis wasps that had developed from L. nana than from C. glomerata. 5. We argue that the remarkable efficiency which characterizes the development of secondary and tertiary parasitoids is based on the very high nutritional quality of resources that increase in quality up the food chain and rigid selection optimizing allocation of limited host resources. Consequently, food webs involving secondary and tertiary parasitoids can go to levels hitherto unexplored thus far in empirical studies. The use of molecular markers in future studies may reveal just how long food c
    https://doi.org/10.1111/j.1365-2656.2008.01516.x
  • Restoration Ecology
    2009

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

    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.
    https://doi.org/10.1111/j.1526-100X.2007.00351.x
  • Physiological Entomology
    2008

    Comparing the physiological effects and function of larval feeding in closely-related endoparasitoids (Braconidae: Microgastrinae)

    Jeff A. Harvey, T. Martijn Bezemer, R. Gols, Nakamatsu Y., T. Tanaka
    The larvae of most endoparasitoid wasps consume virtually all host tissues before pupation. However, in some clades, the parasitoid larvae primarily consume haemolymph and fat body and emerge through the side of the host, which remains alive and active for up to several days. The evolutionary significance of this host-usage strategy has attracted attention in recent years. Recent empirical studies suggest that the surviving larva guards the parasitoid broods against natural enemies such as predators and hyperparasitoids. Known as the 'usurpation hypothesis', the surviving larvae bite, regurgitate fluids from the gut, and thrash the head capsule when disturbed. In the present study, the 'usurpation hypothesis' is tested in the association involving Manduca sexta, its parasitoid Cotesia congregata, and a secondary hyperparasitoid Lysibia nana. Percentage parasitoid survival is higher and hyperparasitism lower when cocoons of C. congregata are attached to the dorsum of M. sexta caterpillars. Fat body contents in several associations involving solitary and gregarious parasitoids feeding on haemolymph and fat body are also compared. The amount of fat body retained in parasitized caterpillars varies considerably from one association to another. In M. sexta and Pieris brassicae, considerable amounts of fat body remain after parasitoid emergence whereas, in Cotesia kariyai and Cotesia rufricus, virtually all of the fat body is consumed by the parsasitoid larvae. The length of post-egression survival of parasitized caterpillars differs considerably in several tested associations. In Pseudeletia separata, most larvae die within a few hours of parasitoid emergence whereas, in M. sexta, parasitized larvae live up to 2 weeks after parasitoid emergence. Larvae in other associations parasitized by gregarious and solitary endoparasitoids live for intermediate periods. The results are discussed in relation to the adaptive significance of different feeding strategies of immature parasitoids and of the costs and benefits of retaining the parasitized caterpillar in close proximity with the parasitoid cocoons.
    https://doi.org/10.1111/j.1365-3032.2008.00623.x
  • Plant Signaling & Behavior
    2008

    Plants as green as phones: Novel insights into plant-mediated communication between below- and above-ground insects

    Roxina Soler , Jeff A. Harvey, T. Martijn Bezemer, J.F. Stuefer
    can act as vertical communication channels or ‘green phones’ linking soil-dwelling insects and insects in the aboveground ecosystem. When root-feeding insects attack a plant, the direct defense system of the shoot is activated, leading to an accumulation of phytotoxins in the leaves. The protection of the plant shoot elicited by root damage can impair the survival, growth and development of aboveground insect herbivores, thereby creating plant-based functional links between soil-dwelling insects and insects that develop in the aboveground ecosystem. The interactions between spatially separated insects below- and aboveground are not restricted to root and foliar plant-feeding insects, but can be extended to higher trophic levels such as insect parasitoids. Here we discuss some implications of plants acting as communication channels or ‘green phones’ between root and foliar-feeding insects and their parasitoids, focusing on recent findings that plants attacked by root-feeding insects are significantly less attractive for the parasitoids of foliar-feeding insects.
    https://doi.org/10.4161/psb.3.8.6338
  • Soil Biology & Biochemistry
    2008

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

    K. Birkhofer, T. Martijn Bezemer, J. Bloem, Michael 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.
    https://doi.org/10.1016/j.soilbio.2008.05.007
  • Agriculture, Ecosystems and Environment
    2008

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

    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.
    https://doi.org/10.1016/j.agee.2008.03.006
  • Biological Conservation
    2008

    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.
    https://doi.org/10.1016/j.biocon.2008.06.011
  • Nature
    2008

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

    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.
    https://doi.org/10.1038/nature07474
  • Animal Behaviour
    2008

    Do parasitized caterpillars protect their parasitoids from hyperparasitoids? A test of the ‘usurpation hypothesis’

    Jeff A. Harvey, Martine Kos, Y. Nakamatsu, T. Tanaka, Marcel Dicke, Louise E.M. Vet, J. Brodeur, T. Martijn Bezemer
    Caterpillars that are attacked by some species of parasitoid wasps are known to survive for several days after the parasitoid larvae emerge and pupate. It has been argued that the behaviour of the parasitized larva is ‘usurped’ by the parasitoid and that it ‘guards’ the parasitoid cocoons against their own natural enemies such as hyperparasitoids (the ‘usurpation hypothesis'). We tested this hypothesis in the association involving a gregarious endoparasitoid, the wasp Cotesia glomerata; caterpillars of its host, the large cabbage white butterfly Pieris brassicae; and a pupal hyperparasitoid, the wasp Lysibia nana. In laboratory experiments, we presented cocoon broods of C. glomerata to single females of L. nana in arenas for 6 h. We tested several treatments for rates of primary parasitoid survival, including variation in the position of the caterpillar and the presence or absence of an additional silk web spun by parasitized caterpillars. Parasitized P. brassicae larvae survived longer than the period necessary for C. glomerata adults to emerge. Rates of parasitoid survival were, however, unaffected by the presence of a P. brassicae larva on the cocoon brood, although significantly more parasitoids emerged when the silk web was present. Analyses of the foraging behaviour of individual L. nana females in arenas, performed using Observer software, revealed that the wasps showed a greater tendency to leave cocoons when caterpillars and silk were present. The laboratory experiments only partially support the usurpation hypothesis. In nature, usurpation of the host of the primary parasitoid may be a more effective strategy against generalist predators than against more specialized and better-adapted hyperparasitoids.
    https://doi.org/10.1016/j.anbehav.2008.03.016
  • Ecology
    2007

    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.
    https://doi.org/10.1890/0012-9658(2007)88[424:CVSFIL]2.0.CO;2
  • Oecologia
    2007

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

    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.
    https://doi.org/10.1007/s00442-006-0649-z
  • Oikos
    2007

    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.
    https://doi.org/10.1111/j.0030-1299.2007.15501.x
  • Nature
    2007

    Ecology: Diversity and stability in plant communities

    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.
    https://doi.org/10.1038/nature05749
  • Functional Ecology
    2007

    Foraging efficiency of a parasitoid of a leaf herbivore is influenced by root herbivory on neighbouring plants

    1. Root feeding insects can influence foliar quality of the host plant, which can affect the development and behaviour of leaf herbivores and parasitoids. Thus far, such interactions have been reported in situations where root and leaf associated organisms share a host-plant. We tested whether root herbivory influences searching behaviour of an above-ground parasitoid when the foliar feeding host of the parasitoid and the root herbivore are feeding on different plants. 2. We manipulated the proportion of 25 plants (ranging from 0 to 1) exposed to root herbivory by Delia radicum (neighbouring-plants). Five additional plants were infested above-ground with Pieris brassicae larvae (host-infested plants) and were placed in-between the neighbouring plants. We then released females of the parasitoid Cotesia glomerata which attacks P. brassicae and studied foraging efficiency of the parasitoid. 3. Overall, parasitoids located more host-infested plants during the maximum allowed searching time, and found their hosts about three times faster when neighbouring plants were exposed to root herbivory, than when neighbouring plants were not infested with D. radicum. Similar results were found when the host-infested plants were also exposed to root herbivory. 4. Our results show that the interaction between an above-ground foliar feeding insect and its parasitoid can be influenced by the presence of non-host herbivores feeding on the roots of neighbouring conspecific plants.
    https://doi.org/10.1111/j.1365-2435.2007.01309.x
  • Journal of Ecology
    2007

    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, Will 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.
    https://doi.org/10.1111/j.1365-2745.2007.01282.x
  • Journal of Chemical Ecology
    2007

    Development of an insect herbivore and its pupal parasitoid reflect differences in direct plant defense

    Jeff A. Harvey, R. Gols, Roel Wagenaar, T. Martijn Bezemer
    In nature, plants defend themselves by production of allelochemicals that are toxic to herbivores. There may be considerable genetic variation in the expression of chemical defenses because of various selection pressures. In this study, we examined the development of the small cabbage butterfly, Pieris rapae, and its gregarious pupal ectoparasitoid, Pteromalus puparum, when reared on three wild populations (Kimmeridge, Old Harry, Winspit) of cabbage, Brassica oleracea, and a Brussels sprout cultivar. Wild plant populations were obtained from seeds of plants that grow naturally along the south coast of Dorset, England. Significant differences in concentrations of allelochemicals (glucosinolates) were found in leaves of plants damaged by P. rapae. Total glucosinolate concentrations in Winspit plants, the population with the highest total glucosinolate concentration, were approximately four times higher than in the cultivar, the strain with the lowest total glucosinolate concentration. Pupal mass of P. rapae and adult body mass of Pt. puparum were highest when reared on the cultivar and lowest when developing on Kimmeridge plants, the wild strain with the lowest total glucosinolate concentration. Development of male parasitoids was also more negatively affected than female parasitoids. Our results reveal that plant quality, at least for the development of ‘adapted’ oligophagous herbivores, such as P. rapae, is not based on total glucosinolate content. The only glucosinolate compound that corresponded with the performance of P. rapae was the indole glucosinolate, neoglucobrassicin. Our results show that performance of ectoparasitoids may closely reflect constraints on the development of the host.
    https://doi.org/10.1007/s10886-007-9323-0
  • Applied Vegetation Science
    2007

    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, Helene Bracht 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
    https://doi.org/10.1658/1402-2001(2007)10[97:LEOSHA]2.0.CO;2
  • Ecology
    2006

    Interplay between Senecio jacobaea and plant, soil and aboveground insect herbivore community composition

    T. Martijn Bezemer, Jeff A. Harvey, George Kowalchuk, H. Korpershoek, Wim H. van der Putten
    To elucidate the factors that affect the performance of plants in their natural environment, it is essential to study interactions with other neighboring plants, as well as with above- and belowground higher trophic organisms. We used a long-term field experiment to study how local plant community diversity influenced colonization by the biennial composite Senecio jacobaea in its native range in The Netherlands in Europe. We tested the effect of sowing later-succession plant species (0, 4, or 15 species) on plant succession and S. jacobaea performance. Over a period of eight years, the percent cover of S. jacobaea was relatively low in communities sown with 15 or 4 later-succession plant species compared to plots that were not sown, but that were colonized naturally. However, after four years of high abundance, the density of S. jacobaea in unsown plots started to decline, and the size of the individual plants was smaller than in the plots sown with 15 or 4 plant species. In the unsown plots, densities of aboveground leaf-mining, flower-feedin In a greenhouse experiment, we grew S. jacobaea in sterilized soil inoculated with soil from the different sowing treatments of the field experiment. Biomass production was lower when S. jacobaea test plants were grown in soil from the unsown plots than in soil from the sown plots (4 or 15 species). Molecular analysis of the fungal and bacterial communities revealed that the composition of fungal communities in unsown plots differed significantly from those in sown plots, suggesting that soil fu
    https://doi.org/10.1890/0012-9658(2006)87[2002:IBSJAP]2.0.CO;2
  • Journal of Ecology
    2006

    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 ]
    https://doi.org/10.1111/j.1365-2745.2006.01158.x
  • Archives of Insect Biochemistry and Physiology
    2006

    Remarkable similarity in body mass of a secondary hyperparasitoid Lysibia nana and its primary parasitoid host Cotesia glomerata emerging from cocoons of a comparable size

    Lysibia nana is a solitary, secondary idiobiont hyperparasitoid that attacks newly cocooned pre-pupae and pupae of several closely related gregarious endoparasitoids in the genus Cotesia, including C. glomerata. Prior to oviposition, the female wasp injects paralysing venom into the host, thus preventing further development. Here, host fate, emerging hyperparasitoid mass, and egg-to-adult development time was compared in hosts parasitized at different ages over 24-h intervals. Cocoons of C. glomerata were parasitized by L. nana at 12, 36, 60, 84, and 108 h post-egression from the secondary host, Pieris brassicae. Hyperparasitoid survival exceeded 80% in hosts parasitized within the first 60 h after pupation, but dropped thereafter, with no hyperparasitoids emerging in hosts aged 108 h. The mass of hyperparasitoids was positively correlated with the mass of the host cocoon, and this relationship remained consistent in hosts up to 60 h old. Within each host age cohort, the mass of male and female wasps was not significantly different. Development time in L. nana was uniform in hosts up to 60 h old, but increased significantly in 84-h-old hosts, and male wasps completed their development earlier than female wasps. Regulation of host growth varied with the age of the host at parasitism, with the early growth of older hosts reduced much more dramatically than young hosts. Unlike most parasitoids, pupal hyperparasitoids do not make cocoons but instead pupate within the already prepared cocoon of the host parasitoid. Consequently, for a given mass of cocoon, newly emerged L. nana adults were remarkably similar in size with male and female adults of C. glomerata. This reveals that L. nana is extremely efficient at exploiting its primary parasitoid host. [KEYWORDS: Cotesia glomerata ; development ; host quality ; hyperparasitoid ; idiobiont ; Lysibia nana]
    https://doi.org/10.1002/arch.20080
  • Ecology Letters
    2006

    Temporal variation in plant-soil feedback controls succession

    Soil abiotic and biotic factors play key roles in plant community dynamics. However, little is known about how soil biota influence vegetation changes over time. Here, we show that the effects of soil organisms may depend on both the successional development of ecosystems and on the successional position of the plants involved. In model systems of plants and soils from different successional stages, we observed negative plant–soil feedback for early-successional plant species, neutral feedback for mid-successional species, and positive feedback for late-successional species. The negative feedback of early-successional plants was independent of soil origin, while late-successional plants performed best in late- and worst in early-successional soil. Increased performance of the subordinate, late-successional plants resulted in enhanced plant community diversity. Observed feedback effects were more related to soil biota than to abiotic conditions. Our results show that temporal variations in plant–soil interactions profoundly contribute to plant community assemblage and ecosystem development. [KEYWORDS: biodiversity ; ecosystem restoration ; plant community composition ; plant-specific effects ; secondary succession soil communities]
    https://doi.org/10.1111/j.1461-0248.2006.00953.x
  • Acta Oecologica
    2006

    Long-term effects of sowing high or low diverse seed mixtures on plant and gastropod diversity

    I. Dedov, I.L. Stoyanov, L. Penev, Jeff A. Harvey, Wim H. van der Putten, T. Martijn Bezemer
    A number of studies have reported that consumers affect a range of community-level processes, and in turn their diversity and abundance is influenced by the structure and diversity of the plant community. Although gastropods are important generalist herbivores in many environments, few studies have examined the effects of plant species richness and plant community structure on gastropods. This study investigated gastropod species richness and interactions with various above-ground parameters of the vegetation on an experimental field with four plant treatments: low and high diversity of sown later succession plant species, natural colonization at the start of the experiment and natural colonization after 3 years of continued agricultural practice. The investigated gastropod assemblage contained only seven species and was highly dominated by two of them. Both in pitfalls and with hand-sorting the number of species collected per plot was highest in plots with natural plant colonization. Multivariate analysis revealed that overall gastropod abundance was positively associated with plant height and percentage cover of plants, and negatively with percentage grass cover. The same pattern holds for one of the dominant species-complex (Cochlicopa lubrica/lubricella). The other dominant gastropod species (Deroceras reticulatum) was more abundant in samples with higher percentages of moss cover and higher plant diversity, while less abundant at samples with higher plant cover, indicating that the gastropod species preferences may matter more than just their response to plant diversity. Two plant–gastropod species-level associations were observed: Senecio jacobaea with D. reticulatum and Tanacetum vulgare with Cochlicopa spp. The present study also demonstrated that pitfall-traps are suitable for collecting terrestrial gastropods, at least for species-poor grassland habitats. [KEYWORDS: Cochlicopa spp. ; Deroceras reticulatum ; Plant diversity ; Plant–gastropod interactions ; Terrestrial gastropod diversity ; Vegetation structure]
    https://doi.org/10.1016/j.actao.2006.03.004
  • Ecology Letters
    2005

    Soil community composition drives aboveground plantherbivoreparasitoid interactions

    T. Martijn Bezemer, Gerlinde De Deyn, T.M. Bossinga, Nicole M. van Dam, Jeff A. Harvey, Wim H. van der Putten
    Soil organisms can influence higher trophic level aboveground organisms, but only very few studies have considered such effects. We manipulated soil community composition of model grassland ecosystems by introducing nematode communities, microorganisms, neither or both groups. Above ground, aphids (Rhopalosiphum padi) and parasitoids (Aphidius colemani) were introduced, and we measured individual performance and population dynamics of plants, aphids and parasitoids. In microcosms with nematode inoculations either with or without microorganism inoculation, aphids offspring production was significantly reduced by 31%. Aphid populations on both host plants Agrostis capillaris and Anthoxanthum odoratum were lowest in microcosms with combined nematode and microorganism inoculations. Opposite results were found for parasitoids. While the number of emerged parasitoids did not differ between treatments, parasitoid mortality and the proportion of males were significantly lower in microcosms with nematode and microorganism inoculations. Parasitized aphids were significantly larger in microcosms with nematodes inoculated. Plant biomass did not differ, but in the preferred host plant A. odoratum, foliar phenolic content was reduced in the presence of nematodes, and also the concentration of amino acids in the phloem. This study shows that the composition of the soil community matters for aboveground multitrophic interactions. [KEYWORDS: Abovegroundbelowground interactions ; aphid ; Aphidius colemani ; fitness ; herbivory ; microcosm ; nematode ; parasitoid ; Rhopalosiphum padi]
    https://doi.org/10.1111/j.1461-0248.2005.00762.x
  • Journal of Animal Ecology
    2005

    Root herbivore effects on aboveground herbivore, parasitoid and hyperparasitoid performance via changes in plant quality

    1. Plants and insects are part of a complex multitrophic environment, in which they closely interact. However, most of the studies have been focused mainly on bi-tritrophic above-ground subsystems, hindering our understanding of the processes that affect multitrophic interactions in a more realistic framework. 2. We studied whether root herbivory by the fly Delia radicum can influence the development of the leaf feeder Pieris brassicae, its parasitoid Cotesia glomerata and its hyperparasitoid Lysibia nana, through changes in primary and secondary plant compounds. 3. In the presence of root herbivory, the development time of the leaf herbivore and the parasitoid significantly increased, and the adult size of the parasitoid and the hyperparasitoid were significantly reduced. The effects were stronger at low root fly densities than at high densities. 4. Higher glucosinolate (sinigrin) levels were recorded in plants exposed to below-ground herbivory, suggesting that the reduced performance of the above-ground insects was via reduced plant quality. Sinigrin contents were highest in plants exposed to low root fly densities, intermediate in plants exposed to high root fly densities and lowest in plants that were not exposed to root herbivory. 5. Our results show, for the first time, that root herbivory via changes in plant quality can reduce the performance of an above-ground multitrophic level food chain. This underlines the importance of integrating a broader range of above- and below-ground organisms to facilitate a better understanding of complex multitrophic interactions and interrelationships. [KEYWORDS: above–below-ground interactions ; Cotesia glomerata ; Lysibia nana ; Pieris brassicae ; plant–insect interactions]
    https://doi.org/10.1111/j.1365-2656.2005.01006.x
  • Ecology Letters
    2005

    Species divergence and trait convergence in experimental plant community assembly

    T. Fukami, T. Martijn Bezemer, S.R. Mortimer, Wim H. van der Putten
    Despite decades of research, it remains controversial whether ecological communities converge towards a common structure determined by environmental conditions irrespective of assembly history. Here, we show experimentally that the answer depends on the level of community organization considered. In a 9-year grassland experiment, we manipulated initial plant composition on abandoned arable land and subsequently allowed natural colonization. Initial compositional variation caused plant communities to remain divergent in species identities, even though these same communities converged strongly in species traits. This contrast between species divergence and trait convergence could not be explained by dispersal limitation or community neutrality alone. Our results show that the simultaneous operation of trait-based assembly rules and species-level priority effects drives community assembly, making it both deterministic and historically contingent, but at different levels of community organization. [KEYWORDS: Alternative states ; assembly history ; assembly rules ; community convergence ; dispersal limitation ; ecological restoration ; historical contingency ; neutral theory ; priority effects ; succession]
    https://doi.org/10.1111/j.1461-0248.2005.00829.x
  • Ecological Entomology
    2005

    Influence of adult nutrition on the relationship between body size and reproductive parameters in a parasitoid wasp

    1. An important constraint upon life-history evolution in parasitoids is the limit imposed by body size on allocation of limited metabolic resources to different fitness-related physiological functions such as reproduction and survival. 2. The influence of adult nutrition on reproductive and maintenance variables was studied in the synovigenic ectoparasitoid Mastrus ridibundus, and it was determined whether resource allocation to these different functions depends on body size. 3. Over the course of adult life there was a positive relationship between body size and the number of mature eggs in adult females both in the presence and absence of food. However, only in the presence of food did egg maturation rates increase significantly with body size. Starved wasps produced significantly smaller eggs than fed ones, which has not been documented before. Moreover, starved wasps produced fewer offspring than fed wasps, and attacked fewer hosts. 4. The availability of food had a major effect on longevity, with fed females living about 10 times longer than starved ones. There was also a positive relationship between body size and longevity. In starved wasps, this relationship was the same both in the presence and absence of hosts, but in fed wasps there was a positive relationship between body size and longevity in the absence of hosts only. Allocation to initial eggs relative to lifetime progeny production did not decline with body size 5. The data reveal that in M. ridibundus the trade-off between maintenance and reproduction varies with life expectancy. [KEYWORDS: Egg maturation ; egg production ; egg size ; reproductive strategies ; resource allocation ; sizefitness relationship ; synovigeny]
    https://doi.org/10.1111/j.0307-6946.2005.00726.x
  • Journal of Chemical Ecology
    2004

    Above- and below-ground terpenoid aldehyde induction in cotton, Gossypium herbaceum, following root and leaf injury

    T. Martijn Bezemer, Roel Wagenaar, Nicole M. van Dam, Wim H. van der Putten, F.L. Wäckers
    Studies on induced defenses have predominantly focused on foliar induction by above-ground herbivores and pathogens. However, roots are attacked by as many if not more phytophages than shoots, so in reality plants are exposed to above- and below-ground attack. Here, we report effects of foliar and/or root damage on terpenoid aldehyde accumulation in cotton (Gossypium herbaceum). Using HPLC, we analyzed concentrations of individual terpenoid aldehydes in foliage and root tissue. In undamaged plants, terpenoid aldehydes were concentrated in young immature main leaves. Concentrations in side leaves, branching from the main leaves, did not differ among leaf position. Above-ground feeding by Spodoptera exigua larvae on a mature leaf enhanced terpenoid concentrations in immature leaves but not in the damaged leaf. In particular, concentrations of hemigossypolone and the heliocides 1 and 4 were enhanced following herbivory. Root herbivory by wireworms (Agriotes lineatus) also resulted in an increase in terpenoid levels in the foliage. In contrast with foliar herbivory, both immature and mature leaves were induced. However, the level of induction after root herbivory was much lower compared to foliar herbivory. Plants exposed to root herbivory also had significantly higher levels of terpenoid aldehydes in root tissue, while no such effect was found following foliar herbivory. Plants exposed to both root and foliar herbivory appeared to induce primarily above-ground at the cost of below-ground defense. The implications for above- and below-ground Mutitrophic interactions are discussed. [KEYWORDS: Agriotes lineatus ; allocation; gossypol; heliocide; hemigossypolone; induced defense; mechanical damage; spatial distribution; Spodoptera exigua; systemic induction]
    https://doi.org/10.1023/B:JOEC.0000013182.50662.2a
  • Plant Biology
    2004

    Above- and Belowground Trophic Interactions on Creeping Thistle (Cirsium arvense) in High- and Low-Diversity Plant Communities: Potential for Biotic Resistance?

    T. Martijn Bezemer, O. Graça, P. Rousseau, Wim H. van der Putten
    The capacity of local communities to control introduced plants is called biotic resistance. Biotic resistance has been almost exclusively tested for plant competition and aboveground herbivores and pathogens, while neglecting root herbivores and soil pathogens. Here, we present biotic resistance by above- and belowground herbivores in concert, and relate the abundance of the plant enemies to the species diversity of the local plant communities. The study was carried out in a 7-year-old biodiversity field experiment. We used creeping thistle (Cirsium arvense) as a model, and quantified sap-sucking herbivores: aboveground aphids, their antagonists, and root-feeding nematodes. As plant diversity treatments, we used field plots sown with high (15 plant species, HSD) or low (4 plant species, LSD) diverse seed mixtures in 1996 and that were not weeded. Creeping thistle became established spontaneously at the start of the experiment. In 2002, in HSD plots, 90 % of the plant community was made up by 11 species, compared to seven species in LSD plots. No differences were found for C. arvense abundance or biomass. Aboveground, three aphid species were found on C. arvense-Uroleucon cirsii, Aphis fabae, and Macrosiphum euphorbiae, but the latter was found only in low densities. Significantly more aphid species were found on individual plants in HSD plots. Moreover, in HSD plots, on average 10 % of aphids were parasitized, while no parasitism was observed in LSD plots. In the root zone of C. arvense, significantly more nematodes were found in HSD than in LSD plots, and a significantly higher proportion of those nematodes were plant parasites. The dominant plant parasitic nematode in both treatments was Paratylenchus. We conclude that biotic resistance by natural enemies may be enhanced by plant species diversity, but that above- and belowground sap-sucking herbivores do not necessarily have to respond similarly to the diversity of the surrounding plant community. [KEYWORDS: Aphis fabae ; Macrosiphum euphorbiae ; nematode ; Paratylenchus ; Uroleucon cirsii.]
    https://doi.org/10.1055/s-2004-817846
  • Ecological Entomology
    2004

    Development of the solitary endoparasitoid Microplitis demolitor: host quality does not increase with host age and size

    Jeff A. Harvey, T. Martijn Bezemer, Jelmer Elzinga, M.R. Strand
    1. Many studies examining the relationship between host size, an index of host quality, and parasitoid fitness use development time and/or adult parasitoid size as currencies of fitness, while ignoring pre-adult mortality. Because the physiological suitability of the host may vary in different stages, sizes, or ages of hosts, a misleading picture of host quality may therefore be obtained in cases where fitness is based on only one or two developmental traits. 2. The development of the solitary koinobiont endoparasitoid Microplitis demolitor is examined in different larval age-classes of its host the soybean looper Pseudoplusia includens. Hosts were parasitised on days 1-8 after hatching from the egg, and development time, adult body size, and mortality of the parasitoid were compared. 3. A comparison of larval growth trajectories (using dry body mass) of M. demolitor revealed that parasitoid larvae attained over twice as much body mass in old hosts than in younger hosts. Similarly, adult parasitoid size at eclosion generally increased with host size, although parasitoids developing in smaller hosts lost a much lower proportion of mass between pupation and eclosion. 4. Overall egg-to-adult development was most rapid in intermediate-aged hosts, and longer in hosts at opposite ends of the age continuum. Moreover, parasitoid mortality varied non-linearly with host stage, and was generally higher in very young and older hosts. 5. Based on these results and other empirical data for koinobionts, it is argued that fitness functions in this group of parasitoids are not simply a positive function of host size or age, but instead may be distinctly dome-shaped, both patterns reflecting the degree of physiological and nutritional compatibility between the two organisms. [KEYWORDS: Development time ; host quality ; koinobiont ; Microplitis ; demolitor ; parasitoid ; Pseudoplusia ; includens size]
    https://doi.org/10.1111/j.0307-6946.2004.00568.x
  • Basic and Applied Ecology
    2004

    Trophic interactions in a changing world

    Wim H. van der Putten, P.C. de Ruiter, T. Martijn Bezemer, Jeff A. Harvey, M.J. Wassen, V. Wolters
    Across the biosphere, rapid and accelerating changes in land use, climate and atmospheric composition driven primarily by anthropogenic forces are known to exert major influences on the productivity, biodiversity and sustainable provision of ecosystem goods and services. Thus far, many studies assessing the ecological consequences of global change have focussed on single trophic levels. However, understanding these changes and predicting their consequences may benefit from unravelling how interactions between primary producers, primary, and secondary consumers (plants, herbivores and carnivores) are being affected. Conservation and restoration may be improved when assessing species and their interactions on appropriate scales, while acknowledging that above- and belowground biota are ecologically linked. Selection pressures on one species may depend on others, so that species loss means more for diversity than just loss of a single taxon. It may also result in the loss of other species of the same or different trophic levels and in the dilution, or even loss, of various selection pressures. We review a number of discussions on trophic interactions in a changing world in relation to (i) the scale of ecosystem response to environmental change with emphasis on the soil subsystem, (ii) the linkage of above- and belowground subsystems and (iii) natural selection and the stability of community structure and ecosystem functioning. We discuss the need to bring together isolated sub-disciplines of ecology in order to understand the implications of global changes for ecosystem processes. [KEYWORDS: Biodiversity; Global human-induced changes; Trophic level communities; Foodweb; Stablility; Ecosystem services; Sustainable land use; Above–belowground interactions]
    https://doi.org/10.1016/j.baae.2004.09.003
  • Basic and Applied Ecology
    2003

    Interactions between aboveground and belowground induced responses against phytophages

    Since their discovery about thirty years ago, induced plant responses have mainly been studied in interactions of plants with aboveground (AG) pathogens, herbivores and their natural enemies. Many induced responses, however, are known to be systemic and thus it is likely that responses induced by AG phytophages affect belowground (BG) phytophages feeding on the same plant, and vice versa. The awareness that interactions between AG and BG phytophages may be an important aspect in the evolution of induced responses came only recently and little research has been done to date. In this review we first summarise ecological studies that show how AG phytophages may affect BG phytophages, and vice versa. Then we focus on mechanisms governing interactions between AG and BG induced responses, such as cross-talk between signals. We chose the genus Nicotiana and the family Brassicaceae as two examples of plant groups that have been well studied for their induced responses both AG and BG – but not in concert – and explore how interactions between AG and BG induced compounds may link multitrophic interactions associated with these plants. We propose that future research on AG and BG interactions should focus on: 1). Identification of compounds and signalling pathways involved in AG and BG induced responses and analysis of their interaction mechanisms, 2). Evaluation of how induced responses affect interactions between BG and AG phytophages and their natural enemies, 3). Evaluation of the effects of AG and BG phytophages -in combination with their natural enemies- on plant fitness to identify keystone interactions that are driving the natural selection for induced responses in plants. Seit ihrer Entdeckung vor ca. dreißig Jahren werden induzierte pflanzliche Antworten der Pflanzen zumeist mit solchen Pathogenen, Herbivoren und deren natürlichen Feinden untersucht, die an oberirdischen Pflanzenteilen zu finden sind. Viele induzierte Antworten der Pflanzen können aber systemisch sein. Daher ist es wahrscheinlich, dass pflanzliche Antworten, die durch oberirdische Organismen induziert werden, auch solche Phytophagen beeinflussen, die unterirdisch an der Pflanze fressen, und umge [KEYWORDS: ecological costs; induced volatiles; insect herbivores; multitrophic interactions; mycorrhizal fungi; nematodes; pathogens; parasitoids; signal cross-talk; trade-offs]
    https://doi.org/10.1078/1439-1791-00133

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