Staff Publications

Staff Publications

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    'Staff publications' is the digital repository of Wageningen University & Research

    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

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Data from: Responses of insect herbivores and their food plants to wind exposure and the importance of predation risk
Chen, C. ; Biere, Arjen ; Gols, R. ; Halfwerk, Wouter ; Oers, C.H.J. ; Harvey, J.A. - \ 2018
development - abiotic factors - plant-herbivore interactions - predator - plutella xylostella - Pieris brassicae - Parus major
1. Wind is an important abiotic factor that influences an array of biological processes, but it is rarely considered in studies on plant-herbivore interactions. 2. Here, we tested whether wind exposure could directly or indirectly affect the performance of two insect herbivores, Plutella xylostella and Pieris brassicae, feeding on Brassica nigra plants. 3. In a greenhouse study using a factorial design, B. nigra plants were exposed to different wind regimes generated by fans before and after caterpillars were introduced on plants in an attempt to separate the effects of direct and indirect wind exposure on herbivores. 4. Wind exposure delayed flowering, decreased plant height and increased leaf concentrations of amino acids and glucosinolates. 5. Plant-mediated effects of wind on herbivores, i.e., effects of exposure of plants to wind prior to herbivore feeding, were generally small. However, development time of both herbivores was extended and adult body mass of P. xylostella was reduced when they were directly exposed to wind. By contrast, wind-exposed adult P. brassicae butterflies were significantly larger, revealing a trade-off between development time and adult size. 6. Based on these results, we conducted a behavioral experiment to study preference by an avian predator, the Great Tit (Parus major) for last instar P. brassicae caterpillars on plants that were exposed to either control (no wind) or wind (fan-exposed) treatments. Tits captured significantly more caterpillars on still than on wind-exposed plants. 7. Our results suggest that P. brassicae caterpillars are able to perceive the abiotic environment and to trade off the costs of extended development time against the benefits of increased size depending on the perceived risk of predation mediated by wind exposure. Such adaptive phenotypic plasticity in insects has not yet been described in response to wind exposure.
Megaherbivores may impact expansion of invasive seagrass in the Caribbean
Christianen, M.J.A. - \ 2018
alien invasive species - Chelonia mydas - exotic - foundation species - Halophila stipulacea - landscape modification - non-native - plant-herbivore interactions - Thalassia testudinum
1. Our knowledge of the functional role of large herbivores is rapidly expanding, and the impact of grazing on species co-existence and non-native species expansion has been studied across ecosystems. However, experimental data on large grazer impacts on plant invasion in aquatic ecosystems are lacking. 2. Since its introduction in 2002, the seagrass species Halophila stipulacea has rapidly expanded across the Eastern Caribbean, forming dense meadows in green turtle (Chelonia mydas) foraging areas. We investigate the changes in seagrass species co-existence and the impacts of leaf grazing by green turtles on non-native seagrass expansion in Lac Bay (Bonaire, Caribbean Netherlands). 3. Green turtle grazing behavior changed after the introduction of non-native seagrass to Lac Bay in 2010. Field observations, together with time-lapse satellite images over the last four decades, showed initiation of new grazing patches (65 ha, an increase of 72%). The sharp border between grazed and ungrazed seagrass patches moved in the direction of shallower areas with native seagrass species that had previously (1970-2010) been ungrazed. Green turtles deployed with Fastloc-GPS transmitters confirmed high site fidelity to these newly cropped patches. In addition, cafeteria experiments indicated selective grazing by green turtles on native species. These native seagrass species had significantly higher nutritional values compared to the non native species. In parallel, exclosure-experiments showed that non-native seagrass expanded more rapidly in grazed canopies compared to ungrazed canopies. Finally, in six years from 2011-2017, H. stipulacea underwent a significant expansion, invading 20 of 49 fixed monitoring locations in Lac Bay, increasing from 6% to 20% in total occurrence. During the same period, native seagrass Thalassia testudinum occurrence decreased by 33%. 4. Synthesis. Our results provide first-time evidence that H. stipulacea can rapidly colonize and replace native seagrasses in the Caribbean and add a mechanistic explanation for this invasiveness. We conclude that green turtle leaf grazing may modify the rate and spatial extent of this invasive species’ expansion, due to grazing preferences, and increased space for settlement. This work shows how large herbivores play an important but unrecognized role in species co-existence and plant invasions of aquatic ecosystems.
Elucidating the interaction between light competition and herbivore feeding patterns using functional-structural plant modelling
Vries, Jorad De; Poelman, Erik H. ; Anten, Niels ; Evers, Jochem B. - \ 2018
Annals of Botany 121 (2018)5. - ISSN 0305-7364 - p. 1019 - 1031.
Brassica - competition - functional-structural plant modelling - growth-defence trade-off - herbivore specialization - herbivory - nigra - plant-herbivore interactions - red far-red ratio
Background and Aims Plants usually compete with neighbouring plants for resources such as light as well as defend themselves against herbivorous insects. This requires investment of limiting resources, resulting in optimal resource distribution patterns and trade-offs between growth- and defence-related traits. A plant's competitive success is determined by the spatial distribution of its resources in the canopy. The spatial distribution of herbivory in the canopy in turn differs between herbivore species as the level of herbivore specialization determines their response to the distribution of resources and defences in the canopy. Here, we investigated to what extent competition for light affects plant susceptibility to herbivores with different feeding preferences. Methods To quantify interactions between herbivory and competition, we developed and evaluated a 3-D spatially explicit functional-structural plant model for Brassica nigra that mechanistically simulates competition in a dynamic light environment, and also explicitly models leaf area removal by herbivores with different feeding preferences. With this novel approach, we can quantitatively explore the extent to which herbivore feeding location and light competition interact in their effect on plant performance. Key Results Our results indicate that there is indeed a strong interaction between levels of plant-plant competition and herbivore feeding preference. When plants did not compete, herbivory had relatively small effects irrespective of feeding preference. Conversely, when plants competed, herbivores with a preference for young leaves had a strong negative effect on the competitiveness and subsequent performance of the plant, whereas herbivores with a preference for old leaves did not. Conclusions Our study predicts how plant susceptibility to herbivory depends on the composition of the herbivore community and the level of plant competition, and highlights the importance of considering the full range of dynamics in plant-plant-herbivore interactions.
Data from: Effects of plant diversity on the concentration of secondary plant metabolites and the density of arthropods on focal plants in the field
Kostenko, O. ; Mulder, P.P.J. ; Courbois, Matthijs ; Bezemer, T.M. - \ 2016
plant-herbivore interactions - biodiversity - insect community - phytochemistry - plant quality - plant species richness - Jacobaea vulgaris
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.
Plant responses to multiple herbivory : phenotypic changes and their ecological consequences
Li, Yehua - \ 2016
Wageningen University. Promotor(en): Marcel Dicke, co-promotor(en): Rieta Gols. - Wageningen : Wageningen University - ISBN 9789462578043 - 165
brassica oleracea - brevicoryne brassicae - aphidoidea - caterpillars - insect pests - pest resistance - defence mechanisms - phenotypes - insect plant relations - parasitoids - natural enemies - herbivore induced plant volatiles - plant-herbivore interactions - genetic variation - rupsen - insectenplagen - plaagresistentie - verdedigingsmechanismen - fenotypen - insect-plant relaties - parasitoïden - natuurlijke vijanden - herbivoor-geinduceerde plantengeuren - plant-herbivoor relaties - genetische variatie

This thesis explores whether aphid-infestation interferes with the plant response to chewing herbivores and whether this impacts performance and behaviour of individual chewing insect herbivores and their natural enemies, as well as the entire insect community. I investigated this using three wild cabbage populations (Brassica oleracea) that are known to differ in inducible secondary chemistry, to reveal whether patterns were consistent.

A literature review on recent developments in the field of plant interactions with multiple herbivores (Chapter 2) addressed how plant traits mediate interactions with various species of the associated insect community and their dynamics. In addition, the mechanisms underlying phenotypic changes in response to different herbivores were discussed from the expression of defence-related genes, phytohormones and secondary metabolites in plants to their effects on the performance and behaviour of individual insects as well as the entire insect community. In Chapter 3, I investigated the effects of early-season infestation by the aphid Brevicoryne brassicae on the composition and dynamics of the entire insect community throughout the season in a garden experiment replicated in two consecutive years. Aphid infestation in the early season only affected a subset of the community, i.e. the natural enemies of aphids, but not the chewing herbivores and their natural enemies. Moreover, the effects were only significant in the first half (June & July), but waned in the second half of the season (August & September). The effect of aphid infestation on the community of natural enemies also varied among the cabbage populations. Chapter 4 investigated the effects of aphid infestation on plant direct defences against chewing herbivores in laboratory experiments by comparing the performance of chewing herbivores and their parasitoids on aphid-infested and aphid-free plants. The performance of the specialist herbivore Plutella xylostella and its parasitoid Diadegma semiclausum was better on plants infested with aphids than on aphid-free plants, whereas the performance of the generalist herbivore Mamestra brassicae and its parasitoid Microplitis mediator was not affected by aphid infestation. These results suggest that aphid induced changes in plant traits may differentially affect the performance of leaf-chewing herbivore species attacking the same host plant, and also varied among the cabbage populations. Chapter 5 examined the effects of B. brassicae aphid infestation on plant indirect defences against chewing herbivores. In a two-choice olfactometer bioassay, preference behaviour for volatiles emitted by plants infested with hosts alone and those emitted by plants infested with aphids and hosts was compared for D. semiclausum and M mediator, larval endoparasitoids of caterpillars of P. xylostella and M. brassicae, respectively. In addition, the headspace volatiles emitted by host-infested and dually-infested plants were collected and analyzed. Co-infestation with aphids differentially affected volatile-mediated foraging behaviour of the two parasitoid species in an infestation period-dependent manner. Diadegma semiclausum preferred dually infested plants over host-infested plants when aphids infested the plants for a short time period, i.e. 7 days, but the volatile preference of D. semiclausum was reversed when aphid infestation was extended to 14 days. In contrast, M. mediator consistently preferred volatiles emitted by the dually-infested plants over those emitted by host-infested plants. The patterns of preference behaviour of the two wasp species were consistent across the three cabbage populations. Interestingly, the emission rate of most volatile compounds was reduced in plants dually-infested with caterpillars and aphids compared to singly-infested with caterpillars. This study showed that aphid infestation increased plant indirect defences against caterpillars, but depended on the aphid infestation period and specific caterpillar-parasitoid association. We hypothesized a negative interference of aphid infestation on plant defences against chewing herbivores based on previously reported SA-JA antagonism. In Chapter 6, we assessed the activation of SA and JA signaling pathways in plants infested by both aphids (B. brassicae) and various caterpillar species (P. xylostella, M. brassicae and Pieris brassicae) in different time sequences by quantifying transcription levels of the SA- and JA-responsive marker genes, PR-1 and LOX respectively. The results did not provide support for SA-JA antagonism. Compared to single infestation with each of the herbivore species, dual infestation with aphid and caterpillars had no interactive effects on the transcription levels of the SA- and JA-responsive maker genes, regardless of the temporal sequence of aphid and caterpillar attack, or the identity of the attacking caterpillar species.

The findings of this thesis contribute to our understanding of plant responses to herbivory by insect species belonging to different feeding guilds and their ecological effects on other associated community members. Aphid infestation may interfere with plant direct and indirect defences against leaf-chewing herbivores at the individual species level, but the effects are species-specific and also depend on the infestation period of aphids. Early-season aphid infestation may further affect the composition of the insect community, but the effect is smaller influencing only a subset of the community compared to early infestation by chewing herbivores. The molecular mechanism underlying plant responses to both phloem-feeding and leaf-chewing herbivores are complex and require the investigation of a range of genes involved in JA- and SA-mediated defence signal transduction. Plant interact with multiple herbivores at different levels of biological organization ranging from the subcellular level to the individual and the community level, and an integrated multidisciplinary approach is required to investigate plant-insect interactions.

The importance of phenology in studies of plant-herbivore-parasitoid interactions
Fei, Minghui - \ 2016
Wageningen University. Promotor(en): Louise Vet; J.A. Harvey; Rieta Gols. - Wageningen : Wageningen University - ISBN 9789462576551 - 170 p.
016-3952 - phenology - plant-herbivore interactions - parasitoids - interactions - annuals - insects - pieris brassicae - cotesia glomerata - brassicaceae - host plants - fenologie - plant-herbivoor relaties - parasitoïden - interacties - eenjarigen - insecten - waardplanten
Foraging behaviour of parasitoids in multi-herbivore communities
Rijk, M. de - \ 2016
Wageningen University. Promotor(en): Marcel Dicke, co-promotor(en): Erik Poelman. - Wageningen : Wageningen University - ISBN 9789462576377 - 217 p.
016-3931 - parasitoids - parasitoid wasps - feeding behaviour - plant-herbivore interactions - hosts - host parasite relationships - host preferences - host-seeking behaviour - cotesia glomerata - pieris brassicae - brassica oleracea - parasitoïden - sluipwespen - voedingsgedrag - plant-herbivoor relaties - gastheren (dieren, mensen, planten) - gastheer parasiet relaties - gastheerpreferenties - gedrag bij zoeken van een gastheer

Foraging behaviour of parasitoids in multi-herbivore communities

Parasitic wasps, or parasitoids, use herbivore-induced plant volatiles and infochemicals produced directly by the herbivore to locate their herbivorous hosts. This process could be interrupted by the presence of herbivores that are not suitable for the development of parasitoid offspring. These non-host herbivores could affect the behaviour of parasitoids both when parasitoids are foraging for host-infested plants by using plant volatiles and when parasitoids are foraging for hosts on the plant by using herbivore infochemicals.

The aim of this thesis was to study the impact of non-host presence on the parasitoid-host-food plant complex of the parasitoid Cotesia glomerata with its host caterpillar Pieris brassicae and a monoculture of the cultivated plant Brassica oleracea. To study the influence of non-hosts on the plant-volatile-based searching behaviour of the parasitoid, a wind-tunnel set-up in the laboratory was used. In this set-up, the parasitoids were given a choice between two plants or between the leaves of one plant. The plant/leaf on which the parasitoid landed was considered the preferred plant/leaf. A second laboratory set-up was used to study the influence of non-host herbivores on the host-infochemical-based searching behaviour of the parasitoid. In this on-plant experiment, the behaviour of the parasitoid was observed after landing on the plant. The influence of non-hosts on the combination of plant-volatile-based and host-infochemical-based searching, i.e. the total foraging efficiency of the parasitoid, was investigated using an outdoor tent set-up in an agricultural field. In this semi-field experiment, parasitoids were allowed to parasitize their hosts in a non-host environment for one to three days.

This thesis firstly shows that the feeding guild of non-host herbivores influenced the foraging behaviour of C. glomerata. Leaf-chewing non-hosts negatively impacted the plant-volatile-based searching behaviour of the parasitoid, whereas phloem-feeding non-hosts positively impacted the host-infochemical-based searching. The resulting host-finding efficiency was in general positively affected by phloem-feeding non-hosts. Secondly, the position of host and non-host herbivores on the plant affected the plant-volatile-based and the host-infochemical-based foraging behaviour of the parasitoid, but not the host-finding efficiency. An unnatural distribution of herbivores over the plant (host feeding on old leaf, non-host feeding on young leaf), negatively affected the choice of the parasitoid for a leaf to land on, i.e. the parasitoid more often landed on the non-host infested leaf. Combined feeding by the host and non-host on one leaf positively affected the number of hosts parasitized on that plant compared with the number of hosts parasitized when herbivores were separated. However, the parasitoid was able to compensate for these effects as a result of which the foraging efficiency was unaltered. Thirdly, the density of non-hosts did influence the plant-volatile-based searching of the parasitoid. A high non-host density negatively affected parasitoid preference for host-infested plants. However, the host-infochemical-based foraging and the total foraging efficiency remained unaffected. Fourthly, rather than the species diversity, the species identity of non-host herbivores had an influence on parasitoid host-infochemical-based searching. One of the tested non-host species negatively affected the behaviour of the parasitoid when searching on the plant. However, neither non-host species identity nor diversity affected plant-volatile-based searching of the parasitoid. Fifthly, this thesis investigated if a parasitoid could learn to associate non-host cues with the presence of hosts and if the parasitoid changed the parasitization preference accordingly. After receiving a learning experience, the parasitoid showed an altered landing preference for infested plants according to the learned cues. However, in an outdoor tent set-up, the parasitoid did not show an altered parasitization preference.

The results of this thesis show that non-host herbivore traits can affect the different phases of parasitoid foraging either positively, negatively or neutrally. The non-host effect on the total foraging efficiency is not necessarily a result of the sum of the effects on the first and the second foraging phase. In fact, the results of two out of three outdoor-tent experiments that investigated the foraging efficiency of the parasitoid showed no non-host effect, while the separate foraging phases were affected by non-host presence.

It is concluded that the foraging efficiency of the parasitoid C. glomerata when searching for its host P. brassicae is not strongly affected by non-host herbivore presence. The use of herbivore-induced plant volatiles by C. glomerata during this foraging process is not interrupted by non-host herbivores. It is advised to consider all phases of the foraging process in studies of parasitoid foraging behaviour, preferably in one experiment that covers the whole searching process. Altogether, this thesis gives a clear and comprehensive overview of the impact of non-host presence on a parasitoid-host-food plant complex and it thereby contributes to the fundamental knowledge of insect foraging in a multi-herbivore context.

Host location by hyperparasitoids: an ecogenomic approach
Zhu, F. - \ 2015
Wageningen University. Promotor(en): Marcel Dicke, co-promotor(en): Erik Poelman. - Wageningen : Wageningen University - ISBN 9789462574441 - 191
insect-plant relaties - insectenplagen - herbivorie - parasitoïden - planten - verdedigingsmechanismen - symbionten - plant-herbivoor relaties - herbivoor-geinduceerde plantengeuren - hyperparasitoïden - insect plant relations - insect pests - herbivory - parasitoids - plants - defence mechanisms - symbionts - plant-herbivore interactions - herbivore induced plant volatiles - hyperparasitoids

It is fascinating that our ecological systems are structured by both direct and indirect species interactions. In terrestrial ecosystems, plants interact with many species of insects that include both harmful herbivores and beneficial natural enemies of herbivores. During the last 30 years, substantial progress has been made in different plant-insect systems regarding plant trait-mediated species interactions in a tritrophic context. However, plant-based food webs generally consist of more than three trophic levels. For example, hyperparasitoids are parasitic wasps at the fourth trophic level within the plant-associated insect community. They parasitize larvae or pupae of primary parasitoids that are broadly used in biological pest control programmes. Surprisingly, the cues that hyperparasitoids use for host location have remained largely unknown.

The studies presented in this thesis aimed to investigate the cues that are used by hyperparasitoids in host location using an ecogenomic approach that combines metabolomic, transcriptomic and proteomic tools with behavioural studies and field experiments. In addition, we addressed the role of herbivore-associated organisms in plant-mediated indirect species interactions. A naturally existing study system of the Brassica oleracea plant-based food web, including four trophic levels was used. In this system, the two herbivorous insect species, Pieris brassicae and P. rapae, are specialists on Brassica plants. The plants emit herbivore-induced plant volatiles (HIPVs) in response to Pieris caterpillar feeding damage which results in attraction of natural enemies of the herbivores, i.e. Cotesia wasps. These parasitic wasps, in turn, are attacked by hyperparasitoids, such as Lysiba nana. The results presented in this thesis show that hyperparasitoids also use HIPVs for host searching. Interestingly, they are especially attracted by plant odours induced by parasitized caterpillars. Moreover, hyperparasitoids can also use caterpillar body odours to find their hosts at close distance. These findings indicate that infochemicals are the major cues that mediate host searching behaviour of hyperparastioids. Similar to other herbivore-associated organisms, parasitoid larvae feeding inside a herbivore host can induce both behavioral and physiological changes in the host. To further investigate how parasitoid larvae indirectly affect plant responses to herbivory and plant volatile-mediated multitrophic interactions, the role of caterpillar labial salivary glands in plant-hyperparasitoid interactions were investigated. The secretions of labial saliva were eliminated by using an ablation technique. Remarkably, the results show that when the labial salivary glands of the caterpillars were completely removed, plants induced by either unparasitized or Cotesia glomerata-parasitized caterpillars were equally attractive to the hyperparasitoid. Moreover, plants became less attractive to the hyperparasitoid when damaged by ablated caterpillars compared to plants damaged by mock-treated caterpillars and the hyperparasitoids were not able to distinguish between volatiles emitted by herbivore-damaged plants and undamaged control plants when caterpillar salivary glands had been removed. These results suggest that parasitism alters the composition of labial saliva of parasitized caterpillar, which thereby alters the plant phenotype and subsequently plant-hyperparasitoid interactions. The outcomes of this thesis contribute to our understanding of the role of infochemicals in foraging decisions of hyperparasitoids.

Rhizobacterial modification of plant defenses against insect herbivores: from molecular mechanisms to tritrophic interactions
Pangesti, N.P.D. - \ 2015
Wageningen University. Promotor(en): Marcel Dicke; Joop van Loon. - Wageningen : Wageningen University - ISBN 9789462572836 - 224
planten - rizosfeerbacteriën - insecten - multitrofe interacties - verdedigingsmechanismen - pseudomonas fluorescens - mamestra brassicae - pieris brassicae - plant-microbe interacties - insect-plant relaties - plant-herbivoor relaties - plants - rhizosphere bacteria - insects - multitrophic interactions - defence mechanisms - plant-microbe interactions - insect plant relations - plant-herbivore interactions


Plants as primary producers in terrestrial ecosystems are under constant threat from a multitude of attackers, which include insect herbivores. In addition to interactions with detrimental organisms, plants host a diversity of beneficial organisms, which include microbes in the rhizosphere. Furthermore, the interactions between plants and several groups of root-associated microbes such as mycorrhizae, plant growth promoting rhizobacteria (PGPR) and plant growth promoting fungi (PGPF) can affect plant interactions with foliar insect herbivores. The beneficial root-associated microbes are able to modify plant physiology by promoting plant growth and induced systemic resistance (ISR), in which the balance between both effects will determine the final impact on the insect herbivores. Using Arabidopsis thaliana Col-0, this thesis explores the molecular mechanisms on how plants integrate responses when simultaneously interacting with the rhizobacterium Pseudomonas fluorescens and the generalist and the specialist leaf-chewing insects Mamestra brassicae and Pieris brassicae respectively.

A literature review on the state-of-the-art in the field of microbe-plant-insect interactions (Chapter 2) explores how root-associated microbes and insect folivores can influence each other via a shared host plant. For more than a decade, both ecological and mechanistic studies mostly focused on exploring these belowground and aboveground interactions using single microbe and single herbivore species. The importance of increasing the complexity of the study system in order to understand the interactions in more natural situations is being emphasized. Furthermore, this review discusses the role of plant hormones in regulating plant growth and defense against folivores, while simultaneously being involved in associations with root-associated microbes.

Experimental evidence has shown patterns on the effects of mycorrhizal colonization on plant interactions with insect herbivores, and raises the question whether plant colonization by different groups of root-associated microbes has similar effects on particular categories of insect herbivores. In Chapter 3, plant-mediated effects of a non-pathogenic rhizobacterium on the performance of leaf-chewing insects, and the underlying mechanisms modulating the interactions, have been examined. Colonization of A. thaliana Col-0 roots by the bacterium P. fluorescens strain WCS417r resulted in decreased larval weight of the generalist leaf-chewing M. brassicae, and had no effect on larval weight of the specialist leaf-chewing P. brassicae. The crucial role of jasmonic acid (JA) in regulating rhizobacteria-mediated induced systemic resistance (ISR) against M. brassicae is confirmed by including plant mutants in the study. Interestingly, I also observed that rhizobacteria can induce systemic susceptibility to M. brassicae caterpillars. Comparison of M. brassicae performance and gene transcription in A. thaliana plants, grown in potting soil or a mixture of potting soil and sand in a 1:1 ratio, shows that in a mixture of potting soil and sand, rhizobacterial treatment had a consistently negative effect on M. brassicae, whereas the effect is more variable in potting soil. Rhizobacterial treatment primed plants grown in potting soil and sand for stronger expression of JA- and ethylene-regulated genes PDF1.2 and HEL, supporting stronger resistance to M. brassicae. Taken together, the results show that soil composition can be one of the factors modulating the outcome of microbe-plant-insect interactions.

Chapter 4 further addresses the mechanisms underlying rhizobacteria-mediated ISR against the generalist leaf-chewing M. brassicae by integrating plant gene transcription, chemistry and performance of M. brassicae in wild type A. thaliana Col-0 plants and mutants defective in the JA-pathway, i.e. dde2-2 and myc2, in the ET pathway, i.e. ein2-1, and in the JA-/ET-pathway, i.e. ora59. Results of this study show that rhizobacterial colonization alone or in combination with herbivore infestation induced the expression of the defense-associated genes ORA59 and PDF1.2 at higher levels than activation by herbivore feeding alone, and the expression of both genes is suppressed in the knock-out mutant ora59. Interestingly, the colonization of plant roots by rhizobacteria alters the levels of plant defense compounds, i.e. camalexin and glucosinolates (GLS), by enhancing the synthesis of constitutive and induced levels of camalexin and aliphatic GLS while suppressing the induced levels of indole GLS. The changes are associated with modulation of the JA-/ET-signaling pathways as shown by investigating mutants. Furthermore, the herbivore performance results show that functional JA- and ET-signaling pathways are required for rhizobacteria-mediated ISR against leaf-chewing insects as observed in the knock-out mutants dde2-2 and ein2-1. The results indicate that colonization of plant roots by rhizobacteria modulates plant-insect interactions by prioritizing the ORA59-branch over the MYC2-branch, although the transcription factor ORA59 is not the only one responsible for the observed effects of rhizobacteria-mediated ISR against leaf-chewing insects.

Taking a step further in increasing the complexity of the study system, Chapter 5 investigates how co-cultivation of P. fluorescens strains WCS417r and SS101 affects direct plant defense to the caterpillar M. brassicae. Inoculation of either P. fluorescens WCS417r or SS101 singly at root tips or simultaneously at two different positions along the roots resulted in a similar level of rhizobacterial colonization by each strain, whereas co-cultivation of both strains at either the root tips or at two different positions along the roots resulted in a higher colonization level of strain WCS417r compared to colonization by SS101. The results suggest that the site of inoculation influences the direct interactions between the two strains in the rhizosphere, as also confirmed by in vitro antagonism assays in the absence of plants. Both upon single inoculation and co-cultivation of both strains at the same or different sites along the roots, the two rhizobacterial strains induced the same strength of ISR against the caterpillar M. brassicae and the same degree of plant growth promotion. In the roots, colonization by the two strains as single or mixed culture resulted in a similar gene expression pattern of up-regulation of MYC2, down-regulation of WRKY70 and no effect on NPR1 expression, genes representing JA-signaling, SA-signaling and the node of crosstalk between the two pathways, respectively. We hypothesize that both rhizobacterial strains use negative crosstalk between JA- and SA-pathways as mechanism to suppress plant immunity and establish colonization. This study shows that competitive interactions between rhizobacterial strains known to induce plant defense in systemic tissue via different signaling pathways, may interfere with synergistic effects on ISR and plant growth promotion.

While the effect of root-associated microbes on direct plant defense against insect herbivores has been studied previously, the effect of these microbes on indirect plant defense to herbivores is much less known. Chapter 6 explores how colonization by the rhizobacterium P. fluorescens strain WCS417r affects indirect plant defense against the generalist herbivore M. brassicae by combining behavioral, chemical and gene transcriptional approaches. The results show that rhizobacterial colonization of A. thaliana roots results in an increased attraction of the parasitoid Microplitis mediator to caterpillar-infested plants. Volatile analysis revealed that rhizobacterial colonization suppressed emission of the terpene (E)-α-bergamotene, and the aromatics methyl salicylate and lilial in response to caterpillar feeding. Rhizobacterial colonization decreased the caterpillar-induced transcription of the terpene synthase genes TPS03 and TPS04. Rhizobacteria enhanced both growth and indirect defense of plants under caterpillar attack. This study shows that rhizobacteria have a high potential to enhance the biocontrol of leaf-chewing herbivores based on enhanced attraction of parasitoids.

Taken together, the research presented in this thesis has shown how single or combined applications of rhizobacteria affect interactions of plants with leaf-chewing insects in terms of direct and indirect resistance. Furthermore, results presented in this thesis have revealed some of the molecular mechanisms underlying plant-mediated interactions between rhizobacteria and leaf-chewing insects that can be used in developing practical approaches by applying beneficial root-associated microbes for improving plant resistance.

Tales on insect-flowering plant interactions : the ecological significance of plant responses to herbivores and pollinators
Lucas Gomes Marques Barbosa, D. - \ 2015
Wageningen University. Promotor(en): Marcel Dicke, co-promotor(en): Joop van Loon. - Wageningen : Wageningen University - ISBN 9789462572119 - 207
bloeiende planten - insecten - insect-plant relaties - plant-herbivoor relaties - herbivoren - bestuivers (dieren) - trofische graden - parasitoïden - herbivoor-geinduceerde plantengeuren - flowering plants - insects - insect plant relations - plant-herbivore interactions - herbivores - pollinators - trophic levels - parasitoids - herbivore induced plant volatiles - cum laude
cum laude graduation
Insects on individual plants : plant quality, plant diversity and aboveground-belowground effects
Kostenko, O. - \ 2014
Wageningen University. Promotor(en): Wim van der Putten, co-promotor(en): T.M. Bezemer. - Wageningen : Wageningen University - ISBN 9789461738639 - 231
insecten - planten - insect-plant relaties - boven- en ondergrondse interacties - soortendiversiteit - parasitoïden - plant-herbivoor relaties - senecio jacobaea - fauna - insects - plants - insect plant relations - aboveground belowground interactions - species diversity - parasitoids - plant-herbivore interactions
Planten en insecten vormen de basis van veel ecosystemen en ze zijn verantwoordelijk voor belangrijke ecologische functies. Gedurende de laatste drie decennia zijn ecologen en entomologen zich er steeds meer bewust van geworden dat het aantal insecten en de soortsamenstelling van die insecten op één plantensoort sterk kan variëren tussen individuen van die plantensoort. Het is echter nog steeds niet duidelijk welke factoren verantwoordelijk zijn voor deze variatie en op welke manier die variatie tot stand komt. Met meer kennis hierover kunnen we beter voorspellen hoe insectengemeenschappen er op een bepaalde plant uitzien en hoe ze zullen reageren op veranderingen in het milieu. Eerder onderzoek heeft aangetoond dat zowel de kwaliteit van de waardplant (zoals de hoeveelheid voedingsstoffen en plantverdedigingsstoffen) als haar omgeving insecten kunnen beïnvloeden. In dit promotieonderzoek heb ik met een combinatie van kas- en veldexperimenten onderzocht hoe intraspecifieke variatie in de waardplantkwaliteit en de omringende planten de insectengemeenschap op een individuele plant bepalen. Ik heb dit onderzoek gedaan met Jakobskruiskruid (Jacobaea vulgaris Gaertner ssp. vulgaris) en de bovengrondse en ondergrondse multitrofe gemeenschap waar deze plant mee geaffilieerd is.
Going back to the roots: the microbial ecology of the rhizosphere
Philippot, L. ; Raaijmakers, J. ; Lemanceau, P. ; Putten, W.H. van der - \ 2013
Nature Reviews Microbiology 11 (2013)11. - ISSN 1740-1526 - p. 789 - 799.
arbuscular mycorrhizal fungi - bacterial community structure - disease-suppressive bacteria - gradient gel-electrophoresis - plant-herbivore interactions - elevated atmospheric co2 - soil-borne pathogens - medicago-truncatula - food webs - arabidopsis-thaliana
The rhizosphere is the interface between plant roots and soil where interactions among a myriad of microorganisms and invertebrates affect biogeochemical cycling, plant growth and tolerance to biotic and abiotic stress. The rhizosphere is intriguingly complex and dynamic, and understanding its ecology and evolution is key to enhancing plant productivity and ecosystem functioning. Novel insights into key factors and evolutionary processes shaping the rhizosphere microbiome will greatly benefit from integrating reductionist and systems-based approaches in both agricultural and natural ecosystems. Here, we discuss recent developments in rhizosphere research in relation to assessing the contribution of the micro- and macroflora to sustainable agriculture, nature conservation, the development of bio-energy crops and the mitigation of climate change.
Kuiters, A.T. ; Casaer, J. - \ 2010
In: Bosecologie en Bosbeheer / Muys, B., den Ouden, J., Mohren, G.M.J., Verheyen, K., Leuven : ACCO - ISBN 9789033477829 - p. 417 - 424.
bossen - plantengemeenschappen - plant-herbivoor relaties - forests - plant communities - plant-herbivore interactions
Naast grote herbivoren kunnen ook kleinere zoogdieren een effect hebben op bosvegetatie, zij het over het algemeen op een beperktere schaal. In deze bijdrage met name aandacht voor het aanvreten van bosvegetatie door hoefdieren. De effecten op vegetatie en bodem, en populatiedynamiek bij hoefdieren. Tot slot de maatschappelijke aspecten van een duurzaam wildbeheer
Metabolomics: the chemistry between ecology and genetics
Macel, M. ; Dam, N.M. van; Keurentjes, J.J.B. - \ 2010
Molecular Ecology Resources 10 (2010). - ISSN 1755-098X - p. 583 - 593.
plant-herbivore interactions - arabidopsis-thaliana - pyrrolizidine alkaloids - mass-spectrometry - secondary metabolites - functional genomics - evolutionary significance - cynoglossum-officinale - generalist herbivores - quantitative trait
Metabolomics is a fast developing field of comprehensive untargeted chemical analyses. It has many applications and can in principle be used on any organism without prior knowledge of the metabolome or genome. The amount of functional information that is acquired with metabolomics largely depends on whether a metabolome database has been developed for the focal species. Metabolomics is a level downstream from transcriptomics and proteomics and has been widely advertised as a functional genomics and systems biology tool. Indeed, it has been successfully applied to link phenotypes to genotypes in the model plant Arabidopsis thaliana. Metabolomics is also increasingly being used in ecology (ecological metabolomics) and environmental sciences (environmental metabolomics). In ecology, the technique has led to novel insights into the mechanisms of plant resistance to herbivores. Some of the most commonly used analytical metabolomic platforms are briefly discussed in this review, as well as their limitations. We will mainly focus on the application of metabolomics in plant ecology and genetics
Plant-mediated multitrophic interactions between aboveground and belowground insects
Soler Gamborena, R. - \ 2009
Entomologische Berichten 69 (2009)6. - ISSN 0013-8827 - p. 202 - 210.
planten - insecten - bodeminsecten - herbivoren - trofische graden - brassicaceae - insect-plant relaties - multitrofe interacties - plant-herbivoor relaties - plants - insects - soil insects - herbivores - trophic levels - insect plant relations - multitrophic interactions - plant-herbivore interactions
Het is bekend dat planten als verticale communicatiekanalen kunnen fungeren tussen onder-en bovengrondse plantetende insecten. Worteleters veroorzaken veranderingen in biomassa en de chemische samenstelling van de bovengrondse delen van een plant. Deze veranderingen kunnen de overleving, de groei en de ontwikkeling van bladeters beïnvloeden. In het promotieproject werd onderzocht of en hoe de wisselwerking tussen ruimtelijk gescheiden insecten beperkt is tot planteneters, dan wel uitgebreid kan worden naar hogere trofische niveaus zoals bijvoorbeeld parasitaire wespen, de natuurlijke vijanden van de plantenetende insecten. Tijdens de 20e Nederlandse Entomologendag (19 december 2008) is de eerste NEV dissertatieprijs uitgereikt aan dit proefschrift
On the risk of extinction of a wild plant species through spillover of a biological control agent: analysis of an ecosystem compartment model
Chalak-Haghighi, M. ; Hemerik, L. ; Werf, W. van der; Ierland, E.C. van - \ 2008
Wageningen : Mansholt Graduate School (Working paper / Mansholt Graduate School of Social Sciences : Discussion paper ) - 37
onkruidbestrijding - biologische bestrijding - wilde planten - uitsterven - verspreiding - ecosystemen - natuurlijke vijanden - gewas onkruid concurrentie - plant-herbivoor relaties - weed control - biological control - wild plants - extinction - dispersal - ecosystems - natural enemies - crop weed competition - plant-herbivore interactions
Invasive plant species can be controlled by introducing one or more of their natural enemies (herbivores) from their native range; however such introduction entails the risk that the introduced natural enemy will attack indigenous plant species in the area of introduction. The effect of spillover of a natural enemy from a managed ecosystem compartment (agriculture) in the area of introduction to a natural compartment (non-managed) in which an indigenous plant species is attacked by the introduced natural enemy, whereas another indigenous plant species, which competes with the first, is not attacked, has been studied. The combination of competition and herbivory may result in extinction of the attacked wild plant species. Using a modelling approach, the authors have determined model parameters that characterize the risk of extinction. The findings point to the importance of spillover and the relative attack rates (specificity) of introduced natural enemies with respect to target and non-target plant species
Dynamics of grazing lawn formation: An experimental test of the role of scale-dependent processes
Cromsigt, J.P.G.M. ; Olff, H. - \ 2008
Oikos 117 (2008)10. - ISSN 0030-1299 - p. 1444 - 1452.
plant-herbivore interactions - mixed-grass prairie - community structure - growth-responses - african savanna - salt-marsh - serengeti - vegetation - heterogeneity - grazers
Grazing lawns are characteristic for African savanna grasslands, standing out as intensely grazed patches of stoloniferous grazing-tolerant grass species. Grazing lawn development has been associated with grazing and increased nutrient input by large migratory herds. However, we argue that in systems without mass migrations disturbances, other than direct grazing, drive lawn development. Such disturbances, e.g. termite activity or megaherbivore middens, also increase nutrient input and keep the bunch vegetation down for a prolonged time period. However, field observations show that not all such disturbances lead to grazing lawns. We hypothesize that the initial disturbance has to be of a minimal threshold spatial scale, for grazing intensity to be high enough to induce lawn formation. We experimentally tested this idea in natural tall savanna grassland. We mowed different-sized plots to simulate initial disturbances of different scales (six times during one year) and applied fertilizer to half of the plots during two years to simulate increased nutrient input by herbivores or termite activity. Allowing grazing by naturally occurring herbivores, we followed the vegetation development over more than three years. Grazing kept bunch grass short in coarser, fertilized plots, while grasses grew out toward their initial height in fine-scale and unfertilized plots. Moreover, lawn grasses strongly increased in cover in plots with an increased nutrient input but only after coarser scale disturbance. These results support our hypothesis that an increased nutrient input in combination with grazing indeed induces grazing lawn formation, but only above a threshold scale of the initial disturbance. Our results provide an alternative mechanism for the development of grazing lawns in systems that lack mass migrating herds. Moreover, it gives a new spatial dimension to the processes behind grazing lawn development, and hence help to understand how herbivores might create and maintain spatial heterogeneity in grassland systems.
Linking variation in plant defence to biodiversity at higher trophic levels: a multidisciplinary approach
Poelman, E.H. - \ 2008
Wageningen University. Promotor(en): Marcel Dicke; Louise Vet, co-promotor(en): Joop van Loon; N.M. van Dam. - [S.l.] : s.n. - ISBN 9789085049623 - 163
brassica oleracea - cotesia - parasitoïden - verdedigingsmechanismen - hyperparasieten - trofische graden - gastheer parasiet relaties - pieris brassicae - insectenplagen - plant-herbivoor relaties - herbivoor-geinduceerde plantengeuren - parasitoids - defence mechanisms - hyperparasites - trophic levels - host parasite relationships - insect pests - plant-herbivore interactions - herbivore induced plant volatiles - cum laude
cum laude graduation (with distinction)
Gewasbescherming van opkomst tot oogst in de gesloten productie
Janssen, A. ; Maanen, R. van; Messelink, G.J. ; Sabelis, M.W. - \ 2008
Gewasbescherming 39 (2008)Suppl.. - ISSN 0166-6495 - p. 17 - 17.
biologische bestrijding - kassen - voedselwebben - voedselketens - interacties - analytische methoden - risicoschatting - glastuinbouw - agro-ecosystemen - plant-herbivoor relaties - insect-plant relaties - biological control - greenhouses - food webs - food chains - interactions - analytical methods - risk assessment - greenhouse horticulture - agroecosystems - plant-herbivore interactions - insect plant relations
Genetica, chemie en ecologie van een kwalitatief glucosinolaatpolymorfisme in barbarakruid (Barbarea vulgaris)
Leur, H. van - \ 2008
Gewasbescherming 39 (2008)3. - ISSN 0166-6495 - p. 108 - 110.
gewasbescherming - barbarea vulgaris - glucosinolaten - chemotypen - genetica - nematoda - plaagresistentie - experimenteel veldonderzoek - plant-herbivoor relaties - plant protection - glucosinolates - chemotypes - genetics - pest resistance - field experimentation - plant-herbivore interactions
Op 17 maart 2008 promoveerde Hanneke van Leur aan Wageningen Universiteit op het proefschrift getiteld 'Genetics, chemistry and ecology of a qualitative glucosinolate polymorphism in Barbarea vulgaris). Uit haar onderzoek kan op basis van de gehouden kas- en veldproeven geconcludeerd worden dat de structuur van de glucosinaten significante verschillen veroorzaakt in resistentie tegen verschillende herbivoren. Het is echter niet zo dat het ene chemotype in alle gevallen meer resistent is dan het andere chemotype.
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