Ciska Raaijmakers

Ciska Raaijmakers

Research assistant
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Visiting Address

Droevendaalsesteeg 10
6708 PB Wageningen

+31 (0) 317 47 34 00

The Netherlands

About

Research assistant at the TE department.
Chemical analyses
Field and greenhouse experiments

Biography

Ciska started at NIOO in 2001 as a research assistant at the TE department. Since then she has worked within the department for various projects.
Being part of the chemical lab staff, her work consists of several chromatography method developments and analyzes, lab management and supervision of students.

Experienced in the following analysis techniques
HPLC-DAD Plant exudates - Organic Acids - Phenolics – flavonoids - Glucosinolates
HPLC-ECD Mono- di- and tri-saccharides – Iridoide glycosides – Glucosamine
GC-C-IRMS Analysis of 13C/12C ratio of PLFA’s (fatty acids)
UHPLC-MSMS ergosterol - Amino acids - metabolite screening - glucosamine - plant hormones
GC-FID PLFA’s and NLFA’s (Fatty Acids Methyl Esters)

In addition to chemical analyses, she also provides practical support in the field and greenhouse to the TE department.

"think like a proton and stay positive"

CV

Publications

Peer-reviewed publications

  • Environmental microbiome
    19-07-2023

    Pioneer Arabidopsis thaliana spans the succession gradient revealing a diverse root-associated microbiome

    Vera Hesen, Yvet Boele, Tanja Bakx-Schotman, Femke van Beersum, Ciska Raaijmakers, Ben Scheres, Viola Willemsen, Wim H. van der Putten

    BACKGROUND: Soil microbiomes are increasingly acknowledged to affect plant functioning. Research in molecular model species Arabidopsis thaliana has given detailed insights of such plant-microbiome interactions. However, the circumstances under which natural A. thaliana plants have been studied so far might represent only a subset of A. thaliana's full ecological context and potential biotic diversity of its root-associated microbiome.

    RESULTS: We collected A. thaliana root-associated soils from a secondary succession gradient covering 40 years of land abandonment. All field sites were situated on the same parent soil material and in the same climatic region. By sequencing the bacterial and fungal communities and soil abiotic analysis we discovered differences in both the biotic and abiotic composition of the root-associated soil of A. thaliana and these differences are in accordance with the successional class of the field sites. As the studied sites all have been under (former) agricultural use, and a climatic cline is absent, we were able to reveal a more complete variety of ecological contexts A. thaliana can appear and sustain in.

    CONCLUSIONS: Our findings lead to the conclusion that although A. thaliana is considered a pioneer plant species and previously almost exclusively studied in early succession and disturbed sites, plants can successfully establish in soils which have experienced years of ecological development. Thereby, A. thaliana can be exposed to a much wider variation in soil ecological context than is currently presumed. This knowledge opens up new opportunities to enhance our understanding of causal plant-microbiome interactions as A. thaliana cannot only grow in contrasting soil biotic and abiotic conditions along a latitudinal gradient, but also when those conditions vary along a secondary succession gradient. Future research could give insights in important plant factors to grow in more ecologically complex later-secondary succession soils, which is an impending direction of our current agricultural systems.

    https://doi.org/10.1186/s40793-023-00511-y
  • 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
  • Frontiers in Microbiology
    2022

    Methane-Derived Carbon As A Driver For Cyanobacterial Growth

    Slawek Cerbin, German Perez, Michal Rybak, Łukasz Wejnerowski, Adam Konowalczyk, Nico Helmsing, Suzanne M.H. Naus-Wiezer, Marion Meima-Franke, Łukasz Pytlak, Ciska Raaijmakers, Witold Nowak, Paul Bodelier
    Methane, a potent greenhouse gas produced in freshwater ecosystems, can be used by methane-oxidizing bacteria (MOB) and can therefore subsidize the pelagic food web with energy and carbon. Consortia of MOB and photoautotrophs have been described in aquatic ecosystems and MOB can benefit from photoautotrophs which produce oxygen, thereby enhancing CH4 oxidation. Methane oxidation can account for accumulation of inorganic carbon (i.e., CO2) and the release of exometabolites that may both be important factors influencing the structure of phytoplankton communities. The consortium of MOB and phototroph has been mainly studied for methane-removing biotechnologies, but there is still little information on the role of these interactions in freshwater ecosystems especially in the context of cyanobacterial growth and bloom development. We hypothesized that MOB could be an alternative C source to support cyanobacterial growth in freshwater systems. We detected low δ13C values in cyanobacterial blooms (the lowest detected value −59.97‰ for Planktothrix rubescens) what could be the result of the use of methane-derived carbon by cyanobacteria and/or MOB attached to their cells. We further proved the presence of metabolically active MOB on cyanobacterial filaments using the fluorescein isothiocyanate (FITC) based activity assay. The PCR results also proved the presence of the pmoA gene in several non-axenic cultures of cyanobacteria. Finally, experiments comprising the co-culture of the cyanobacterium Aphanizomenon gracile with the methanotroph Methylosinus sporium proved that cyanobacterial growth was significantly improved in the presence of MOB, presumably through utilizing CO2 released by MOB. On the other hand, 13C-CH4 labeled incubations showed the uptake and assimilation of MOB-derived metabolites by the cyanobacterium. We also observed a higher growth of MOB in the presence of cyanobacteria under a higher irradiance regime, then when grown alone, underpinning the bidirectional influence with as of yet unknown environmental consequences.
    https://doi.org/10.3389/fmicb.2022.837198
  • Proceedings of the Royal Society B-Biological Sciences
    26-02-2020

    Adapted dandelions trade dispersal for germination upon root herbivore attack

    Zoe Bont, Marc Pfander, Christelle A. M. Robert, Meret Huber, Erik H. Poelman, Ciska Raaijmakers, Matthias Erb
    https://doi.org/10.1098/rspb.2019.2930
  • Soil Biology & Biochemistry
    2019

    Unexpected role of canonical aerobic methanotrophs in upland agricultural soils.

    Adrian Ho, Hyo Jung Lee, Max Reumer, Marion Meima-Franke, Ciska Raaijmakers, Hans Zweers, Wietse de Boer, Wim H. van der Putten, Paul Bodelier
    Aerobic oxidation of methane at (circum-)atmospheric concentrations (<40 ppmv) has long been assumed to be catalyzed by the as-yet-uncultured high-affinity methanotrophs in well-aerated, non-wetland (upland) soils, the only known biological methane sink globally. Although the low-affinity canonical methanotrophs with cultured representatives have been detected along with the high-affinity ones, their role as a methane sink in upland soils remains enigmatic. Here, we show that canonical methanotrophs can contribute to (circum-)atmospheric methane uptake in agricultural soils. We performed a stable-isotope 13CCH4 labelling incubation in the presence and absence of bio-based residues that were added to the soil to track the flow of methane. Residue amendment transiently stimulated methane uptake rate (<50 days). Soil methane uptake was sustained throughout the incubation (130 days), concomitant to the enrichment of 13CCO2. The 13C-enriched phospholipid fatty acids (PLFAs) were distinct in both soils, irrespective of amendments, and were unambiguously assigned almost exclusively to canonical alphaproteobacterial methanotrophs with cultured representatives. 16S rRNA and pmoA gene sequence analyses revealed that the as-yet-uncultured high-affinity methanotrophs were virtually absent in these soils. The stable-isotope labelling approach allowed to attribute soil methane uptake to canonical methanotrophs, whereas these were not expected to consume (circum-)atmospheric methane. Our findings thus revealed an overlooked reservoir of high-affinity methane-oxidizers represented by the canonical methanotrophs in agriculture-impacted upland soils. Given that upland agricultural soils have been thought to marginally or do not contribute to atmospheric methane consumption due to the vulnerability of the high-affinity methanotrophs, our findings suggest a thorough revisiting of the contribution of agricultural soils, and the role of agricultural management to mitigation of climate change.
    https://doi.org/10.1016/j.soilbio.2018.12.020
  • Chemoecology
    2018

    Seasonal and herbivore-induced dynamics of foliar glucosinolates in wild cabbage (Brassica oleracea)

    Rieta Gols, Nicole M. van Dam, Michael Reichelt, Jonathan Gershenzon, Ciska Raaijmakers, James M. Bullock, Jeff A. Harvey
    Levels of plant secondary metabolites are not static and often change in relation to plant ontogeny. They also respond to abiotic and biotic changes in the environment, e.g., they often increase in response to biotic stress, such as herbivory. In contrast with short-lived annual plant species, especially those with growing periods of less than 2–3 months, investment in defensive compounds of vegetative tissues in biennial and perennial species may also vary over the course of an entire growing season. In garden experiments, we investigated the dynamics of secondary metabolites, i.e. glucosinolates (GSLs) in the perennial wild cabbage (Brassica oleracea), which was grown from seeds originating from three populations that differ in GSL chemistry. We compared temporal long-term dynamics of GSLs over the course of two growing seasons and short-term dynamics in response to herbivory by Pieris rapae caterpillars in a more controlled greenhouse experiment. Long-term dynamics differed for aliphatic GSLs (gradual increase from May to December) and indole GSLs (rapid increase until mid-summer after which concentrations decreased or stabilized). In spring, GSL levels in new shoots were similar to those found in the previous year. Short-term dynamics in response to herbivory primarily affected indole GSLs, which increased during the 2-week feeding period by P. rapae. Herbivore-induced changes in the concentrations of aliphatic GSLs were population-specific and their concentrations were found to increase in primarily one population only. We discuss our results considering the biology and ecology of wild cabbage.
    https://doi.org/10.1007/s00049-018-0258-4
  • Oecologia
    2018

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

    Feng Zhu, Robin Heinen, Martijn van der Sluijs, Ciska Raaijmakers, Arjen Biere, T. Martijn Bezemer
    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
  • 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
  • AoB PLANTS
    2017

    Changing soil legacies to direct restoration of plant communities

    It is increasingly acknowledged that soil biota may influence interactions among plant species, however, little is known about how to change historical influences of previous land management on soil biota, the so-called ‘biotic soil legacy effect’. We used a two-phase plant community-soil feedback approach to study how plant species typical to original (i.e. undisturbed) and degraded fen meadows may influence effects of the soil community on Carex species that are dominant in fen meadows. In phase one, soil from original, degraded, successfully and unsuccessfully restored fen meadows was conditioned by growing plants typical to original or to degraded fen meadows. In phase two, interactions between Carex and neighbouring plant species were studied to quantify plant community-soil feedback effects in different neighbour plant mixtures. Soil conditioning with plants typical to original fen meadows resulted in significantly more Carex biomass than with plants typical to degraded fen meadows. These effects were strongest when the soil originated from unsuccessfully restored fen meadows. However, biomass of plants typical of degraded fen meadows was also higher in soil conditioned by typical fen meadow plants. We conclude that soil legacy effects of plants from degraded fen meadows can be altered by growing typical fen meadow plant species in that soil, as this enhances priority effects that favour growth of other typical fen meadow plants. As also plant species from degraded fen meadows benefitted from soil conditioning, further studies are needed to reveal if plant species can be chosen that change negative soil legacy effects for rare and endangered fen meadow plant species, but not for plant species that are typical to degraded fen meadows.
    https://doi.org/10.1093/aobpla/plx038
  • Chemoecology
    06-10-2016

    Effects of population-related variation in plant primary and secondary metabolites on aboveground and belowground multitrophic interactions

    Moniek Van Geem, Rieta Gols, Ciska Raaijmakers, Jeff A. Harvey
    Insects feeding on aboveground and belowground tissues can influence each other through their shared plant and this is often mediated by changes in plant chemistry. We examined the effects of belowground root fly (Delia radicum) herbivory on the performance of an aboveground herbivore (Plutella xylostella) and its endoparasitoid wasp (Cotesia vestalis). Insects were reared on three populations of wild cabbage (Brassica oleracea) plants, exhibiting qualitative and quantitative differences in root and shoot defense chemistry, that had or had not been exposed to root herbivory. In addition, we measured primary (amino acids and sugars) and secondary [glucosinolate (GS)] chemistry in plants exposed to the various plant population-treatment combinations to determine to what extent plant chemistry could explain variation in insect performance variables using multivariate statistics. In general, insect performance was more strongly affected by plant population than by herbivory in the opposite compartment, suggesting that population-related differences in plant quality are larger than those induced by herbivory. Sugar profiles were similar in the three populations and concentrations only changed in damaged tissues. In addition to population-related differences, amino acid concentrations primarily changed locally in response to herbivory. Whether GS concentrations changed in response to herbivory (indole GS) or whether there were only population-related differences (aliphatic GS) depended on GS class. Poor correlations between performance and chemical attributes made biological interpretation of these results difficult. Moreover, trade-offs between life history traits suggest that factors other than food nutritional quality contribute to the expression of life history traits.
    https://doi.org/10.1007/s00049-016-0222-0
  • Journal of Ecology
    2016

    Modification of plant-induced responses by an insect ecosystem engineer influences the colonization behaviour of subsequent shelter-users

    Akane Uesugi, Kimberly Morrell, Erik H. Poelman, Ciska Raaijmakers, André Kessler
    * Herbivores that modify plant morphology, such as gall-forming insects, can disproportionately impact arthropod community on their host plants by providing novel habitats and shelters from biotic and abiotic stresses. These ecosystem engineers could also modify plant chemical properties, but how such changes in plant quality affect the behaviour of subsequent colonizers has rarely been investigated. * We explored how an initial infestation of the tall goldenrod (Solidago altissima) by an ecosystem engineer, the rosette gall-midge (Rhopalomyia solidaginis), affects colonization behaviour of a shelter-using beetle (Microrhopala vittata) through plant-induced responses in the field. * Beetles preferentially colonized plants with galls and exhibited a clumped distribution on those plants, which suggested a possible advantage for aggregating on galled plants. Accordingly, we found that beetles remained longer on galled plants with previous beetle damage than those without beetle damage. No such effect of beetle damage was found on plants without a gall. Similar interactions between galler infestation and beetle damage were found in beetle's feeding choice, leaf diterpene and serine protease inhibitor production, and volatile organic compound (VOC) emission. These plant metabolic induction and herbivore response patterns indicated that the gall-midge can alter how plants respond to the beetle damage and that gall presence coupled with beetle damage improves leaf palatability for the beetle. Finally, we found reciprocal effects of beetles on gall-midge performance to be neutral to slightly positive, suggesting that the observed field association of the two herbivores could be formed by plant-mediated facilitation. * Synthesis. Our study suggests that an ecosystem engineer could have significant impact on herbivore community not only by changing plant morphology, but also by altering host quality and modifying plant-induced responses to subsequent herbivory. As such, R. solidaginis also functions as a keystone herbivore that has disproportionate effects on community dynamics and composition meditated by induced plant growth and metabolic responses.
    https://doi.org/10.1111/1365-2745.12587
  • Frontiers in Plant Science
    2016

    Root-lesion nematodes suppress cabbage aphid population development by reducing aphid daily reproduction

    (Gera) W.H.G. Hol, Ciska Raaijmakers, Ilse Mons, Katrin M. Meyer, Nicole M. van Dam
    Empirical studies have shown that belowground feeding herbivores can affect the performance of aboveground herbivores in different ways. Often the critical life-history parameters underlying the observed performance effects remain unexplored. In order to better understand the cause for the observed effects on aboveground herbivores, these ecological mechanisms must be better understood. In this study we combined empirical experiments with a modeling approach to analyze the effect of two root feeding endoparasitic nematodes with different feeding strategies on the population growth of the aboveground feeding specialist aphid Brevicoryne brassicae on Brassica nigra. The aim was to test whether emerging differences in life history characteristics (days until reproduction, daily reproduction) would be sufficient to explain observed differences in aphid population development on plants with and without two species of nematodes. Aphid numbers were lower on plants with Pratylenchus penetrans in comparison to aphid numbers on plants with Meloidogyne spp. A dedicated experiment showed that aphid daily reproduction was lower on plants with P. penetrans (3.08 offspring female–1 day–1) in comparison to both uninfested plants and plants with Meloidogyne spp. (3.50 offspring female–1 day–1). The species-specific reduction of aphid reproduction appeared independent of changes in amino acids, soluble sugars or the glucosinolate sinigrin in the phloem. An individual-based model revealed that relatively small differences in reproduction rate per female were sufficient to yield a similar difference in aphid populations as was found in the empirical experiments.
    https://doi.org/10.3389/fpls.2016.00111
  • Journal of Chemical Ecology
    2015

    Interactions between a belowground herbivore and primary and secondary root metabolites in wild cabbage

    Moniek Van Geem, Jeff A. Harvey, A.M. Cortesero, Ciska Raaijmakers, R. Gols
    Plants are attacked by both above- and belowground herbivores. Toxic secondary compounds are part of the chemical defense arsenal of plants against a range of antagonists, and are subject to genetic variation. Plants also produce primary metabolites (amino acids, nutrients, sugars) that function as essential compounds for growth and survival. Wild cabbage populations growing on the Dorset coast of the UK exhibit genetically different chemical defense profiles, even though they are located within a few kilometers of each other. As in other Brassicaceae, the defensive chemicals in wild cabbages constitute, among others, secondary metabolites called glucosinolates. Here, we used five Dorset populations of wild cabbage to study the effect of belowground herbivory by the cabbage root fly on primary and secondary chemistry, and whether differences in chemistry affected the performance of the belowground herbivore. There were significant differences in total root concentrations and chemical profiles of glucosinolates, amino acids, and sugars among the five wild cabbage populations. Glucosinolate concentrations not only differed among the populations, but also were affected by root fly herbivory. Amino acid and sugar concentrations also differed among the populations, but were not affected by root fly herbivory. Overall, population-related differences in plant chemistry were more pronounced for the glucosinolates than for amino acids and sugars. The performance of the root herbivore did not differ among the populations tested. Survival of the root fly was low (<40 %), suggesting that other belowground factors may override potential differences in effects related to primary and secondary chemistry.
    https://doi.org/10.1007/s10886-015-0605-7
  • 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
  • PLoS One
    2013

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

    T. Tytgat, Koen Verhoeven, Jeroen Jansen, Ciska Raaijmakers, Tanja Bakx-Schotman, L.M. McIntyre, Wim H. van der Putten, Arjen Biere, Nicole M. van Dam
    Plants respond to herbivore attack by rapidly inducing defenses that are mainly regulated by jasmonic acid (JA). Due to the systemic nature of induced defenses, attack by root herbivores can also result in a shoot response and vice versa, causing interactions between above- and belowground herbivores. However, little is known about the molecular mechanisms underlying these interactions. We investigated whether plants respond differently when roots or shoots are induced. We mimicked herbivore attack by applying JA to the roots or shoots of Brassica oleracea and analyzed molecular and chemical responses in both organs. In shoots, an immediate and massive change in primary and secondary metabolism was observed. In roots, the JA-induced response was less extensive and qualitatively different from that in the shoots. Strikingly, in both roots and shoots we also observed differential responses in primary metabolism, development as well as defense specific traits depending on whether the JA induction had been below- or aboveground. We conclude that the JA response is not only tissue-specific but also dependent on the organ that was induced. Already very early in the JA signaling pathway the differential response was observed. This indicates that both organs have a different JA signaling cascade, and that the signal eliciting systemic responses contains information about the site of induction, thus providing plants with a mechanism to tailor their responses specifically to the organ that is damaged.
    https://doi.org/10.1371/journal.pone.0065502
  • 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
  • Phytochemistry
    2012

    Broccoli and turnip plants display contrasting responses to belowground induction by Delia radicum infestation and phytohormone applications

    P.S. Pierre, S. Dugravot, A.M. Cortesero, D. Poinsot, Ciska Raaijmakers, H.M. Hassan, Nicole M. van Dam
    Induced responses to insect herbivory are a common phenomenon in the plant kingdom. So far, induced responses have mostly investigated in aerial plant parts. Recently it was found that root herbivore may also elicit both local and systemic responses affecting aboveground herbivores and their natural enemies. Using broccoli (Brassica oleracea subsp. italica L.) and turnip (Brassica rapa subsp. rapa L.), two cultivated brassicaceaous plants differing in their chemistry and morphology, we analysed the local and systemic induced responses triggered by Delia radicum L. damage, JA and SA application. We also assessed whether the root induction treatments affected D. radicum larval performance. Both D. radicum damage and JA induced changes in glucosinolate and sugar content as well as affected D. radicum performance, while SA application did not. Despite the uniform chemical responses, the effect on larval performance on broccoli and turnip plantswas very different. On broccoli, JA root treatment reduced herbivore performance, whereas in turnips the same treatment enhanced it. JA- and D. radicum-induced responses followed similar patterns, which suggests that the JA signalling pathway is involved in rootinduced responses to larval feeding. Glucosinolate induction cannot fully explain the differences found in the performance of D. radicum on the different species. Changes in other resistance factors might significantly contribute to the induced resistance in these brassicaceaeous species as well.
    https://doi.org/10.1016/j.phytochem.2011.09.009
  • Applied Soil Ecology
    2012

    Matgrass sward plant species benefit from soil organisms

    Soilorganisms are important in the structuring of plant communities. However, little is known about how to apply this knowledge to vegetation management. Here, we examined if soilorganisms may promote plantspecies of characteristic habitats, and suppress plantspecies of disturbed habitats. We classified nineteen fields into four types: characteristic and disturbed matgrass swards and successfully and unsuccessfully restored fields. We recorded the vegetation composition and measured biotic and abiotic soil characteristics of the sites. In a pot experiment, we mixed non-sterilized (with soilorganisms) or sterilized (without soilorganisms) soil inoculum from each field with a common sterilized background soil. We planted seedlings of characteristic matgrass speciesAntennaria dioica and Nardus stricta, of disturbance indicators Deschampsia flexuosa and Agrostis capillaris, or a combination of the four species. At harvest, we measured root and shoot dry mass of all plants. The vegetation composition of characteristic matgrass swards differed from the disturbed and unsuccessfully restored fields. The successfully restored fields were intermediate. The composition of the nematode community tended to follow the same pattern. In the pot experiment, addition of soilorganisms increased the biomass of A. dioica, N. stricta and D. flexuosa, but decreased the biomass of A. capillaris. However, the effect of soilorganisms on plant biomass was not related to field type. A. dioica showed a large variation in biomass in non-sterilized, but not in sterilized soil. Soilorganisms from some sites increased plant biomass, whereas soilorganisms from other sites did not. The biomass of characteristic matgrass plants was lower in the presence of plants from disturbed swards, irrespective of the presence of soilorganisms. Probably A. capillaris was so much larger than the other species, that this overruled effects of added soilorganisms. Soilorganisms promoted growth of plantspecies characteristic of matgrass swards, whereas they reduced growth of a plantspecies characteristic of disturbed fields. Soilorganisms did not change the outcome of plant interactions, which was won by a disturbance indicator. Nevertheless, measurement of the growth stimulating capacity of a soil may be used to assess opportunities for reintroduction of characteristic plantspecies.
    https://doi.org/10.1016/j.apsoil.2012.07.012
  • Entomologia Experimentalis et Applicata
    2011

    Temporal dynamics of herbivore-induced responses in Brassica juncea and their effect on generalist and specialist herbivores

    Vartika Mathur, S. Ganta, Ciska Raaijmakers, A.S. Reddy, Louise E.M. Vet, Nicole M. van Dam
    Herbivore feeding may induce an array of responses in plants, and each response may have its own temporal dynamics. Precise timing of these plant responses is vital for them to have optimal effect on the herbivores feeding on the plant. This study measured the temporal dynamics of various systemically induced responses occurring in Brassica juncea (L.) Czern. (Brassicaceae) leaves after insect herbivory in India and The Netherlands. Morphological (trichomes, leaf size) and chemical (glucosinolates, amino acids, sugars) responses were analysed. The effects of systemic responses were assessed using a specialist [Plutella xylostella L. (Lepidoptera: Plutellidae)] and a generalist [Spodoptera litura Fabricius (Lepidoptera: Noctuidae)] herbivore. We tested the hypotheses that morphological responses were slower than chemical responses and that generalist herbivores would be more affected by induced responses than specialists. Glucosinolates and trichomes were found to increase systemically as quickly as 4 and 7 days after herbivore damage, respectively. Amino acids, sugars, and leaf size remained unaffected during this period. The generalist S. litura showed a significant feeding preference for undamaged leaves, whereas the specialist herbivore P. xylostella preferred leaves that were damaged 9 days before. Performance bioassays on generalist S. litura revealed that larvae gained half the weight on leaves from damaged plants as compared to larvae feeding on leaves from undamaged plants. These studies show that although morphological responses are somewhat slower than chemical responses, they also contribute to induced plant resistance in a relatively short time span. We argue that before considering induced responses as resistance factors, their effect should be assessed at various points in time with both generalist and specialist herbivores.
    https://doi.org/10.1111/j.1570-7458.2011.01122.x
  • Functional Ecology
    2009

    Nonlinear effects of plant root and shoot jasmonic acid application on the performance of Pieris brassicae and its parasitoid Cotesia glomerata

    B. Qiu, Jeff A. Harvey, Ciska Raaijmakers, Louise E.M. Vet, Nicole M. van Dam
    1. Plant species employ several direct and indirect defence strategies to protect themselves against insect herbivores. Most studies, however, have focused on shoot-induced responses. Much less is known about interactions between below- and above-ground herbivores and how these may affect their respective parasitoids. 2. Here, we quantify the impact of below-ground induced responses vs. that of above-ground induced responses in a feral Brassica on the performance of Pieris brassicae and its endoparasitoid Cotesia glomerata. Jasmonic acid (JA) was applied to induce the plants above- or below-ground. The glucosinolate, sugar and amino acid levels of the leaves were analysed. 3. Pieris brassicae larvae grew significantly slower on shoot JA-induced (SJA) plants than on root JA-induced (RJA) and control plants, which were treated with acidic water. On RJA and control plants they showed similar developmental trajectories. Pupal masses, survival till eclosion and egg load, however, were similar on all plants. 4. The development of C. glomerata larvae on SJA plants was significantly longer than that on RJA and control plants. In contrast, the parasitoid's pupal stage lasted longer in hosts feeding on control plants. The total developmental times eventually were similar in all groups. However, the masses of male and female C. glomerata adults that developed hosts on control and RJA plants were significantly larger than those from hosts on SJA plants. JA application increased total glucosinolate conten 5. These results show that the differential effects of above- and below-ground-induced responses on herbivores also affect higher trophic levels in a nonlinear fashion via differential changes in host plant quality. In particular, the indirect effects that below-ground herbivores have on the performance of above-ground parasitoids may exceed the direct effects of plant chemistry on herbivore performance. Consequently, above-ground and below-ground interactions mediated by induced plant response
    https://doi.org/10.1111/j.1365-2435.2008.01516.x
  • Oikos
    2009

    Are population differences in plant quality reflected in the preference and performance of two endoparasitoid wasps?

    R. Gols, Nicole M. van Dam, Ciska Raaijmakers, Marcel Dicke, Jeff A. Harvey
    In recent years, increasing attention has been paid in exploring the role of direct plant defence, through the production of allelochemicals, on the performance of parasitoid wasps and their hosts. However, few studies have determined if parasitoids can detect differences in plant quality and thus preferentially attack hosts on which their progeny develop most successfully. In this study we examined the development and preference of two endoparasitoids, Diadegmasemiclausum and Cotesia glomerata, developing in larvae of their respective hosts, Plutella xylostella and Pieris brassicae. In turn, these were reared on different wild populations of black mustard Brassica nigra originating in the Netherlands and Sicily (Italy), as well as single cultivated strains of B. nigra and brown mustard, B. juncea. Chemical analyses of foliar glucosinolates and volatile emissions by P. xylostella-damaged plants revealed large differences between B. nigra and B. juncea plants, with smaller differences among the B. nigra populations. The four mustard populations differentially affected development time and body mass of the herbivores and parasitoids. Contrasts among the means revealed significant differences mainly between B. nigra and B. juncea. Both parasitoids, however, preferred to alight on plants in which their progeny developed most successfully. In behavioural bioassays, D. semiclausum did not discriminate among the B. nigra populations and preferred to alight on B. juncea, which was the best plant population for parasitoid development. By contrast, C. glomerata females exhibited the lowest preference for Italian B. nigra populations, on which adult parasitoid size was the smallest. These results reveal that parasitoids can detect even small differences in plant quality presumably through their volatile blends and that plant preference and offspring performance in the two species are 'optimally synchronized'.
    https://doi.org/10.1111/j.1600-0706.2008.17231.x
  • Entomologia Experimentalis et Applicata
    2008

    Performance of specialist and generalist herbivores feeding on cabbage cultivars is not explained by glucosinolate profiles

    Erik H. Poelman, R.J.F.H. Galiart, Ciska Raaijmakers, Joop J.A. van Loon, Nicole M. van Dam
    Plants display a wide range of chemical defences that may differ in effectiveness against generalist and specialist insect herbivores. Host plant-specific secondary chemicals such as glucosinolates (GS) in Brassicaceae typically reduce the performance of generalist herbivores, whereas specialists have adaptations to detoxify these compounds. The concentration of glucosinolates may also alter upon herbivory, allowing the plant to tailor its response to specifically affect the performance of the attacking herbivore. We studied the performance of three Lepidoptera species, two specialists [Pieris rapae L. (Pieridae), Plutella xylostella L. (Yponomeutidae)] and one generalist [Mamestra brassicae L. (Noctuidae)], when feeding on eight cultivars of Brassica oleracea L. and a native congener (Brassica nigra L.) and related this to the GS content. We tested the hypotheses (i) that a generalist herbivore is more affected by high GS concentrations, and (ii) that generalist feeding has a stronger effect on GS levels. Although performance of the three herbivores was different on the B. oleracea cultivars, M. brassicae and P. xylostella had a similar ranking order of performance on the eight cultivars. In most of the cultivars, the concentration of indole GS was significantly higher after feeding by P. rapae or M. brassicae than after P. xylostella feeding. As a consequence, the total concentration of GS in the cultivars showed a different ranking order for each herbivore species. The generalist M. brassicae performed equally well as the specialist P. xylostella on cultivars with high concentrations of GS. Our findings suggest that secondary metabolites other than GSs or differences in nutrient levels affect performance of the species studied.
    https://doi.org/10.1111/j.1570-7458.2008.00700.x
  • Entomologia Experimentalis et Applicata
    2008

    Reciprocal interactions between the cabbage root fly (Delia radicum) and two glucosinolate phenotypes of Barbarea vulgaris

    H. Van Leur, Ciska Raaijmakers, Nicole M. van Dam
    The cabbage root fly, Delia radicum L. (Diptera: Anthomyiidae), has a life cycle with spatially separated components: adults live and oviposit above ground, whereas larvae feed and pupate below ground. Oviposition choice is affected by shoot glucosinolates. However, little is known about below-ground plant defence against D. radicum. Here, we investigate the effect of glucosinolates on oviposition preference and performance of D. radicum, using two naturally occurring heritable chemotypes of Barbarea vulgaris R. Br. (Brassicaceae) with different glucosinolate profiles: BAR-type plants (the most common and genetically dominant glucosinolate profile, dominated by glucobarbarin) and NAS-type plants (the recessive phenotype, dominated by gluconasturtiin). Performance was studied by applying 10 neonate D. radicum larvae per plant and measuring pupal biomass after 18 days. There was no difference in retrieval, but pupae had a higher biomass after development on BAR-type plants. On average, BAR-type plants received 1.8 times more eggs than NAS types, but this difference was not statistically significant. In a separate experiment, we compared the physiological response of both chemotypes to D. radicum feeding. Infestation reduced root and shoot biomass, root sugar and amino acid levels, and shoot sugar levels. Except for shoot sugar levels, these responses did not differ between the two chemotypes. Shoot or root glucosinolate profiles did not change on infestation. As glucosinolate profiles were the only consistent difference between the chemotypes, it is likely that this difference caused the reduced biomass of D. radicum pupae on NAS-type plants. In an experimental garden, plants were heavily infested by root flies, but we found no differences in the percentage of fallen-over flower stalks between the chemotypes. Overall, we found more pupae in the soil near BAR-type plants, but this was not statistically significant. The results of the performance experiment suggest that BAR-type plants may be more suitable hosts than NAS-type plants.
    https://doi.org/10.1111/j.1570-7458.2008.00722.x
  • Basic and Applied Ecology
    2007

    Temporal changes affect plant chemistry and tritrophic interactions

    R. Gols, Ciska Raaijmakers, Nicole M. van Dam, Marcel Dicke, Tibor Bukovinszky, Jeff A. Harvey
    In nature, individuals of short-lived plant species (e.g. annuals, biennials) may grow at different times during the growing season. These plants are therefore exposed to different season-related conditions such as light and temperature, which in turn may have consequences for primary and secondary chemistry of the plant. Despite this, many studies examining plant–consumer interactions are performed in single replicates, which may thus ignore temporal variation in the expression of phenotypic plant traits that affect multitrophic interactions. In the present study, we demonstrated that even under strictly controlled conditions in a greenhouse, secondary plant chemistry changes dramatically in plants growing at different times in a single year, i.e. July, August and November. Glucosinolate (GS) contents in herbivore-damaged leaves of two different crucifer species, Brassica oleracea and Sinapis alba were higher in the August and November replicates than in the July replicate and GS concentrations were 10–25 times higher in S. alba than in B. oleracea. The development of a specialist herbivore, Plutella xylostella, also varied significantly over the three replicates. Larvae of P. xylostella that had fed upon either S. alba or B. oleracea, attained the largest biomass and had the fastest development rate in the November replicate. Female P. xylostella moths grew larger on S. alba than on B. oleracea, whereas male biomass was not significantly affected by host-plant species. Plant species, but not season also affected performance of the endoparasitoid, Diadegma semiclausum. Similar to the performance of host females, parasitoid males developed faster and attained the highest biomass when attacking P. xylostella larvae feeding on S. alba. Most importantly, the performance of the herbivore and its parasitoid only appeared to partially conform to levels of GS in damaged leaves, indicating that there is a complex of factors involved in determining the effects of plant quality on higher trophic levels.
    https://doi.org/10.1016/j.baae.2006.09.005
  • Oikos
    2007

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

    Gerlinde De Deyn, Jasper van Ruijven, Ciska Raaijmakers, P.C. de Ruiter, Wim H. van der Putten
    Interactions between above- and belowground invertebrate herbivores alter plant diversity, however, little is known on how these effects may influence higher trophic level organisms belowground. Here we explore whether above- and belowground invertebrate herbivores which alter plant community diversity and biomass, in turn affect soil nematode communities. We test the hypotheses that insect herbivores 1) alter soil nematode diversity, 2) stimulate bacterial-feeding and 3) reduce plant-feeding nematode abundances. In a full factorial outdoor mesocosm experiment we introduced grasshoppers (aboveground herbivores), wireworms (belowground herbivores) and a diverse soil nematode community to species-rich model plant communities. After two years, insect herbivore effects on nematode diversity and on abundance of herbivorous, bacterivorous, fungivorous and omni-carnivorous nematodes were evaluated in relation to plant community composition. Wireworms did not affect nematode diversity despite enhanced plant diversity, while grasshoppers, which did not affect plant diversity, reduced nematode diversity. Although grasshoppers and wireworms caused contrasting shifts in plant species dominance, they did not affect abundances of decomposer nematodes at any trophic level. Primary consumer nematodes were, however, strongly promoted by wireworms, while community root biomass was not altered by the insect herbivores. Overall, interaction eff
    https://doi.org/10.1111/j.2007.0030-1299.15761x
  • Phytochemistry
    2006

    A heritable glucosinolate polymorphism within natural populations of Barbarea vulgaris

    H. Van Leur, Ciska Raaijmakers, Nicole M. van Dam
    In natural populations of Barbarea vulgaris we found two distinctly different glucosinolate profiles. The most common glucosinolate profile is dominated (94%) by the hydroxylated form, (S)-2-hydroxy-2-phenylethyl-glucosinolate (glucobarbarin, BAR-type), whereas in the other type 2-phenylethyl-glucosinolate (gluconasturtiin, NAS-type) was most prominent (82%). NAS-type plants have a 108-fold increase of gluconasturtiin concentration in rosette leaves compared to BAR-type plants. The glucosinolate composition of both chemotypes is consistent throughout all plant organs and after induction with jasmonic acid. Although the glucosinolate profile of the roots has a more diverse composition than other plant organs, it still matches the chemotype. In 12 natural populations that we sampled in Germany, Belgium, France and Switzerland solely BAR-type plants were found. However, eight out of the 15 Dutch populations that were sampled contained 2–22% NAS-type plants. Controlled crosses showed that the chemotype was heritable and determined by a single gene with two alleles. The allele coding for the BAR-type was dominant and the allele for the NAS-type was recessive. The different glucosinolate profiles will yield different hydrolysis products upon damage, and therefore we expect them to differentially affect the multitrophic interactions associated with B. vulgaris in their natural environment. [KEYWORDS: Barbarea vulgaris ; Brassicaceae ; Glucosinolates ; Glucobarbarin ; Gluconasturtiin ; Plant defence ; Polymorphism; Heritability]
    https://doi.org/10.1016/j.phytochem.2006.04.021
  • Chemoecology
    2006

    Local and systemic induced responses to cabbage root fly larvae (Delia radicum) in Brassica nigra and B. oleracea

    Nicole M. van Dam, Ciska Raaijmakers
    Feeding by belowground herbivores may induce systemic changes in shoot defence levels that affect the performance of above ground herbivores and higher trophic levels. In this paper two wild Brassica species, B. nigra and B. oleracea were experimentally infested with 10 larvae of the cabbage root fly, Delia radicum. Plant dry masses and glucosinolate levels in shoots, main roots, and fine roots were determined at 3, 7, 12 and 14 days after infestation and compared to those of control plants. The systemic response in the leaves differed between plant species. In B. nigra shoot glucosinolate levels in D. radicum infested plants steadily increased with time until they were almost twice those of controls 14 days after infestation. B. oleracea plants infested with D. radicum did not show significant changes in shoot glucosinolate levels within 14 days, which may be due to the unexpected poorer performance of D. radicum on this species. Both plant species showed a local increase in indole glucosinolates in the main roots, which are the preferred feeding site of D. radicum larvae. B. oleracea plants however showed a stronger (1.9 – 4.7 times) increase in indole glucosinolate levels than B. nigra (1.5 – 2.6 times). The increase in indole glucosinolates in B. nigra main roots, was counterbalanced by a significant decrease in aromatic glucosinolate levels. These differences in local responses to D. radicum feeding between the two s [KEYWORDS: Above-belowground interactions ;- root herbivores ; induced responses ; Brassica oleracea ; Brassica nigra ; Delia radicum]
    https://doi.org/10.1007/s00049-005-0323-7
  • Entomologia Experimentalis et Applicata
    2005

    Root herbivory reduces growth and survival of the shoot feeding specialist Pieris rapae on Brassica nigra

    Plants may respond to herbivore attacks by changing their chemical profile. Such induced responses occur both locally and systemically throughout the plant. In this paper we studied how Brassica nigra (L.) Koch (Brassicaceae) plants respond to two different root feeders, the endoparasitic nematode Pratylenchus penetrans Cobb (Tylenchida: Pratylenchidae) and the larvae of the cabbage root fly Delia radicum L. (Diptera: Anthomyiidae). We tested whether the activities of the root feeders affected the survival and development of the shoot feeding crucifer specialist Pieris rapae (L.) (Lepidoptera: Pieridae) via systemically induced changes in the shoots. Overall, P. rapae larvae grew slower and produced fewer pupae on plants that were infested with root feeders, especially on plants infested with P. penetrans. This effect could not be attributed to lower water or protein levels in these plants, as the percentage of water in the controls and root infested shoots was similar, and protein content was even higher in root infested plants. Both glucosinolate as well as phenolic levels were affected by root feeding. Initially, glucosinolate levels were the lowest in root infested plants, but on P. penetrans infested plants they increased more rapidly after P. rapae started feeding than in controls or D. radicum infested plants. Plants with D. radicum feeding on their roots had the highest phenolic levels at all harvest dates. Our results indicate that root feeding can significantly alter the nutritional quality of shoots by changes in secondary metabolite levels and hence the performance of a specialist shoot feeder. [KEYWORDS: above-ground ; below-ground interactions ; black mustard ; Brassicaceae ; cabbage ; cabbage root fly ; Delia radicum ; endoparasitic nematodes ; induced plant responses ; glucosinolates ; phenolics ; Pratylenchus penetrans ; proteins]
    https://doi.org/10.1111/j.1570-7458.2005.00241.x
  • Ecology Letters
    2005

    Interactions between spatially separated herbivores indirectly alter plant diversity

    Jasper van Ruijven, Gerlinde De Deyn, Ciska Raaijmakers, Frank Berendse, Wim H. van der Putten
    Above- and belowground herbivores promote plant diversity when selectively feeding on dominant plant species, but little is known about their combined effects. Using a model system, we show that neutral effects of an aboveground herbivore and positive effects of a belowground herbivore on plant diversity became profoundly negative when adding these herbivores in combination. The non-additive effects were explained by differences in plant preference between the aboveground- and the belowground herbivores and their consequences for indirect interactions among plant species. Simultaneous exposure to aboveground- and belowground herbivores led to plant communities being dominated by a few highly abundant species. As above- and belowground invertebrate herbivores generally differ in their mobility and local distribution patterns, our results strongly suggest that abovegroundbelowground interactions contribute to local spatial heterogeneity of diversity patterns within plant communities. [KEYWORDS: Abovebelowground interactions ; indirect effects ; insect herbivores ; nematodes ; plant diversity]
    https://doi.org/10.1111/j.1461-0248.2004.00688.x
  • Oikos
    2004

    Plant species identity and diversity effects on different trophic levels of nematodes in the soil food web

    Gerlinde De Deyn, Ciska Raaijmakers, Jasper van Ruijven, Frank Berendse, Wim H. van der Putten
    Previous studies on biodiversity and soil food web composition have mentioned plant species identity, as well as plant species diversity as the main factors affecting the abundance and diversity of soil organisms. However, most studies have been carried out under limitations of time, space, or appropriate controls. In order to further examine the relation between plant species diversity and the soil food web, we conducted a three-year semi-field experiment in which eight plant species (4 forb and 4 grass species) were grown in monocultures and mixtures of two, four and eight plant species. In addition there were communities with 16 plant species. We analyzed the abundance and identity of the nematodes in soil and roots, including feeding groups from various trophic levels (primary and secondary consumers, carnivores, and omnivores) in the soil food web. Plant species diversity and plant identity affected the diversity of nematodes. The effect of plant diversity was attributed to the complementarity in resource quality of the component plant species rather than to an increase in total resource quantity. The nematode diversity varied more between the different plant species than between different levels of plant species diversity, so that plant identity is more important than plant diversity. Nevertheless the nematode diversity in plant mixtures
    https://doi.org/10.1111/j.0030-1299.2004.13265.x
  • Journal of Ecology
    2004

    Plant community development is affected by nutrients and soil biota

    1 Plant community development depends to a great extent on the availability of soil nutrients, but recent studies underline the role of symbiotic, herbivorous and pathogenic soil biota. We tested for interactions between these biotic and abiotic factors by studying the effects of additional nutrients and the removal of soil biota on the replacement of grassland plant species typical of different successional stages. 2 Species representing each of the early, mid and target phases of secondary succession in a grassland community (four per phase) were grown in mid-successional grassland soil. The mixed plant communities were grown in sterilized and non-sterilized soil, at three nutrient supply levels. The distribution of shoot biomass over the different plant species, and the total root biomass, were determined, as well as the composition of nematode and microarthropod communities and soil decomposition rates 3 The effect of nutrient supply on plant community composition depended on soil sterilization. In sterilized soil, the plant community was initially dominated by grasses that increased in dominance even without fertilization. In non-sterilized soil, the plant community was more diverse and grass dominance decreased over time, except with high fertilization. Fertilization enhanced the productivity of the plant community in sterilized and, to a greater extent, in non-sterilized soil. 4 The abundance of root-feeding nematodes was positively related to increased root biomass, pointing to a strong bottom-up control. Increased levels of nutrient supply were associated with reduced abundance of omnivorous nematodes, the cause of this reduction being less clear. Increased soil fertility altered the functional diversity of the soil nematode community, which might, in the longer term, also affect their feedback effects on the plant community. 5 Increased nutrient supply reduced soil decomposition activity in the non-sterilized soil, but not in the sterilized soil. 6 Our results imply that soil biota may reduce the effects of nutrient supply on plant dominance. Incorporating the effects of soil biota on plant species interactions into studies on succession, plant species diversity and restoration may therefore considerably increase our understanding of the observed plant community patterns. [KEYWORDS: plant diversity ; plant-soil feedback ; soil fertility soil invertebrates ; succession]
    https://doi.org/10.1111/j.0022-0477.2004.00924.x

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