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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.

    Publications authored by the staff of the Research Institutes are available from 1995 onwards.

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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: Aboveground mammal and invertebrate exclusions cause consistent changes in soil food webs of two subalpine grassland types, but mechanisms are system-specific
Vandegehuchte, Martijn L. ; Putten, W.H. van der; Duyts, H. ; Schütz, Martin ; Risch, Anita C. - \ 2016
soil ecology - above-belowground interactions - herbivory
Data_OIK-03341.R2.csv contains the data on nematode feeding type abundances and community indices, as well as the data used in the Structural Equation Models of the progressive aboveground mammal and invertebrate exclusion effects on the abundance of bacterivorous, fungivorous, plant-feeding and omni-carnivorous nematode abundance via pathways of plants, soil nutrients, soil microbial biomass, and soil environment in both short- and tall-grass vegetation
Plant-mediated insect interactions on a perennial plant : consequences for community dynamics
Stam, J.M. - \ 2016
University. Promotor(en): Marcel Dicke, co-promotor(en): Erik Poelman. - Wageningen : Wageningen University - ISBN 9789462578647 - 254 p.
016-3976 - perennials - brassica oleracea - defence mechanisms - glucosinolates - insect pests - herbivory - plutella xylostella - mamestra brassicae - pieris rapae - herbivore induced plant volatiles - animal communities - population dynamics - overblijvende planten - verdedigingsmechanismen - glucosinolaten - insectenplagen - herbivorie - herbivoor-geinduceerde plantengeuren - diergemeenschappen - populatiedynamica

Plants interact with many organisms around them, and one of the most important groups that a plant has to deal with, are the herbivores. Insects represent the most diverse group of herbivores and have many different ways of using the plant as a food source. Plants can, however, defend themselves against those herbivores, either by constitutive defences, or by traits that are induced upon herbivory. These traits, such as the formation of more trichomes or the production of secondary metabolites, can deter an insect herbivore in its decision to eat from the plant, can be toxic, or otherwise hamper the insect to feed, grow or reproduce. The way a plant responds to herbivory is very specific, depending on the feeding mode or the species of the attacking insect. Furthermore, plant responses to dual herbivory differ from the sum of responses to each herbivore alone. Also the time and order at which multiple insects arrive on a plant, influence the plant’s response. Finally, plant species or populations can show different responses to herbivory. Altogether these factors result in a plant phenotype that the attacking herbivore has to deal with. In addition to the attacker, also subsequently arriving insects will be affected by a change in plant phenotype. Because plants and insects can respond to each other in a continuous chain of interactions, an herbivore early in the season can indirectly affect the later-season community composition through the induced plant response. However, we know only little about the consequences of a dual-herbivore induced plant phenotype for subsequent feeders, and ultimately, the effects on the assembly and dynamics of an insect community as a whole.

The aim of this thesis project was to study the consequences of feeding by multiple insects from the same plant, not only to a subsequent herbivore, but also to the dynamics of a whole insect community over the course of a growing season, and beyond. Furthermore, I studied how the order of herbivore arrival and timing of arrival affected both a next herbivore’s choice and performance in a greenhouse setting, as well as the development of the whole insect community in the field. In addition, I studied how plant populations vary in induced responses, have specific plant-mediated interactions among insect herbivores, and how long these induced responses influence the insect community and plant fitness. Finally, I identified non-additive effects of the history of insect attacks and plant ontogeny to the future insect community.

In the first chapter of this thesis, I introduce the study system. For this project I used several populations of the wild cabbage plant, Brassica oleracea. This is an herbaceous perennial plant that flowers from the second growing season onwards, and supports a large and diverse above-ground arthropod community of more than thirty different species. The plant belongs to the family of Brassicaceae, which is known for the biosynthesis of a group of secondary metabolites, the glucosinolates. These metabolites may deter insects, although some insect species use it as a feeding cue. Two specialist insect herbivores from different feeding guilds, the caterpillar of the diamondback moth Plutella xylostella and the cabbage aphid Brevicoryne brassicae, were used to study their effect as early-season inducer of plant responses either alone or in combination. The caterpillar of the generalist cabbage moth, Mamestra brassicae, was used in bioassays to assess the effects of the induced plant phenotype by single or dual herbivory. Furthermore, in three chapters (Chapters 4, 6 and 7) I have closely studied the composition of the naturally occurring insect community throughout the season for one or two years in a common-garden field setting. In the last of these three chapters, I used the caterpillars of the specialist cabbage white, Pieris rapae, to induce plants at different moments of their ontogeny, while excluding the insect community for varying periods of time by a net or exposing plants to their natural insect community.

In an elaborate literature review, I and my collaborators concluded in chapter 2 that plant responses to dual herbivory evoke different plant responses than the sum of each herbivore alone. This has consequences at all levels from arthropod community assembly to the choice and performance of individual insects. The mechanisms of plant responses to dual herbivory are found in gene expression, hormone production and other molecular processes within the plant. All these aspects of interactions between insects and plants occur and are connected at different time scales.

To follow up on the question how timing plays a role in dual herbivory, we varied the time between, as well as the order of arrival of aphids and/or caterpillars on a plant. We observed that both affected the preference and performance of a subsequently feeding caterpillar (Chapter 3). Mamestra brassicae performed better on plants with a longer time interval between the first and second feeder. Also in a field setting (Chapter 4), the order of herbivore arrival early in the season affected the insect community composition later in the season in two different years, likely through a chain of indirect insect interactions. In this field study, the plant population influenced the outcome of early-season herbivory to later community dynamics. In chapter 5 we found that three plant populations in response to simultaneous aphid and caterpillar attack differed in the expression of two genes that are important for the regulation of herbivore-induced responses. Also, the production of one of two important plant hormones, salicylic acid, responded differently to single or dual herbivory in a unique pattern for each of the plant populations. These different plant responses subsequently negatively affected a next caterpillar on the same plant; M. brassicae growth was impaired on plants which had been fed upon by both aphids and caterpillars, in comparison to control plants. These field and greenhouse studies thus show the implications of dual herbivory beyond effects in the plant; it affects subsequent herbivory, and through a chain of plant-mediated insect interactions, the dynamics of a whole insect community.

In the sixth chapter we show that variation in insect community dynamics can last beyond the moment that the insects were present, even across years. In this field study, the naturally occurring carnivore community influenced the carnivore community composition a year later. Importantly, the herbivore community affected plant fitness across years (but not within years). We propose that such legacy effects are mediated by plant traits, which vary upon insect induction in the first year, and affect the insect community in the next year.

Finally, the history of all insect attacks to a plant up until that moment shape the future insect community by influencing the colonisation of insect species on the plant. Moreover, also plant ontogeny plays a role in shaping the insect community; plant-mediated responses to herbivory at different plant ages resulted in different insect colonisation rates. The most important conclusion from this last data chapter (Chapter 7) is that the two processes, insect community history and plant ontogeny, are non-additive and affect the colonisation of insect species in the same (synergistic) or opposite (antagonistic) direction.

By framing my study results in a time line from minutes to months to years, I show in the general discussion (Chapter 8) that the consequences of dual herbivory for subsequently arriving insects are connected at different time scales. Plant responses to herbivory can occur within hours to days, which affect herbivore choices and performance in the following days and weeks. In their turn, variation of a few days in arrival time of insects may change how plants respond and prioritize their responses to insects throughout the rest of the season. The insects that subsequently arrive on a dual-herbivore induced plant may change the plant phenotype even further and through a chain of insect-plant interactions, the effects on the insects and the plant can last throughout the season, and even across seasons. Furthermore, various factors such as the species of the attacking insect and its feeding guild, the timing after previous attack and the plant age at which herbivory occurs, as well as the genotypic background of the plant, all affect the outcomes of dynamic insect-plant interactions.

The results presented in this thesis thus contribute to the knowledge and interpretation of plant interactions with multiple herbivores. As plants are seldom attacked by a single herbivore, this implies that we have to take into account that multiple herbivory is not the same as the additive effects of single herbivores, and that this has long-lasting consequences for the insect community and the plant. To further understand how plants and insects have adapted to such a dynamic environment, I suggest future research to focus even more on the kinetics of plant physiological responses to dual attack, and to aim at answering the question of how predictable insect communities on a plant really are.

Unraveling molecular mechanisms underlying plant defense in response to dual insect attack : studying density-dependent effects
Kroes, A. - \ 2016
University. Promotor(en): Marcel Dicke; Joop van Loon. - Wageningen : Wageningen University - ISBN 9789462577756 - 265 p.
016-3953 - arabidopsis thaliana - insect pests - herbivory - pest resistance - defence mechanisms - insect plant relations - molecular plant pathology - density - insectenplagen - herbivorie - plaagresistentie - verdedigingsmechanismen - insect-plant relaties - moleculaire plantenziektekunde - dichtheid

In the field, plants suffer from attack by herbivorous insects. Plants have numerous adaptations to defend against herbivory. Not only do these defense responses reduce performance of the feeding herbivore, they also result in the attraction of natural enemies of herbivores.

The majority of studies investigating plant-insect interactions addressed mainly the effects of attack by a single herbivore species on induced plant defenses. However, because plants are members of complex communities, plants are exposed to different insect attackers at the same time. Moreover, attacks by different herbivores interact at different levels of biological organization, ranging from the level of gene expression, phytohormone production and biochemical changes up to the individual level. Effects of plant responses to feeding by two or more herbivore species simultaneously might cascade through the community and thereby affect insect community composition.

The induction of plant defense responses is regulated by a network of signaling pathways that mainly involve the phytohormones jasmonic acid (JA), salicylic acid (SA) and ethylene (ET). The signaling pathways of the two phytohormones SA and JA interact antagonistically, whereas JA and ET signaling pathways can interact both synergistically and antagonistically in regulating plant defense responses. In general, JA-mediated signaling underlies defense responses against leaf-chewing herbivores, such as caterpillars, whereas phloem-feeding insects, such as aphids, mainly induce SA-regulated defenses.

When caterpillars and aphids simultaneously feed on the same host plant, crosstalk between phytohormonal signaling pathways may affect the regulation of plant defenses. Consequently, multiple insect herbivores feeding on plants interact indirectly through plant-mediated effects. Studies investigating molecular mechanisms underlying interference by multiple attacking insects with induced plant defenses will benefit studies on the ecological consequences of induced plant responses.

The aim of this thesis was to elucidate molecular mechanisms that underlie plant-mediated interactions between attacking herbivores from different feeding guilds, namely Brevicoryne brassicae aphids and Plutella xylostella caterpillars.

Because herbivore density affects the regulation of plant defense responses, it may also influence the outcome of multiple insect-plant interactions. To study if modulation of induced plant defenses in response to dual insect attack depends on insect density, plants were infested with two densities of aphids.

Responses of Arabidopsis thaliana plants to simultaneous feeding by aphids and caterpillars were investigated by combining analyses of phytohormone levels, defense gene expression, volatile emission, insect performance and behavioral responses of parasitoids. To better predict consequences of interactions between plants and multiple insect attackers for herbivore communities, the regulation of defense responses against aphids and caterpillars was also studied in the ecological model plant wild Brassica oleracea.

Transcriptomic changes of plants during multiple insect attack and their consequences for the plant’s interactions with members of the associated insect community take place at different time scales. Direct correlation of transcriptomic responses with community development is, therefore, challenging. However, detailed knowledge of subcellular mechanisms can provide tools to address this challenge.

One of the objectives of this thesis, therefore, was to investigate the involvement of phytohormonal signaling pathways and their interactions during defense responses against caterpillars or aphids at different densities, when feeding alone or simultaneously on the model plant A. thaliana. The studies show that aphids at different densities interfere in contrasting ways with caterpillar-induced defenses, which required both SA- and JA-signal-transduction pathways. Transcriptional analysis revealed that expression of the SA transcription factor gene WRKY70 was differentially affected upon infestation by aphids at low or high densities. Interestingly, the expression data indicated that a lower expression level of WRKY70 led to significantly higher MYC2 expression through SA-JA crosstalk. Based on these findings, it is proposed that by down-regulating WRKY70 expression, the plant activates JA-dependent defenses which could lead to a higher resistance against aphids and caterpillars.

Plutella xylostella caterpillars also influenced plant defense responses when feeding simultaneously with aphids. Caterpillar feeding affected aphid-induced defenses which had negative consequences for aphid performance. Induction of both ET- and JA-mediated defense responses is required for this interference. Moreover, aphid density also played an important role in the modulation by P. xylostella of aphid-induced defenses: P. xylostella caterpillars induced changes in levels of JA and its biologically active from, JA-Ile, only when feeding simultaneously with aphids at a high density.

To study the overall effect of dual herbivory on induced plant defenses, not only interference with induced direct defense, but also with induced indirect defenses was addressed in A. thaliana. We found a significant preference of the aphid parasitoid Diaeretiella rapae for volatiles from aphid-infested A. thaliana wild-type plants and ein2-1 (ET-insensitive) mutants. Interestingly, simultaneous feeding by P. xylostella caterpillars on wild-type plants increased D. rapae’s preference for odors from aphid-infested plants. However, upon disruption of the ET-signaling pathway, D. rapae did not distinguish between ein2-1 mutants infested by aphids or by both aphids and caterpillars. This showed that intact ET signaling is needed for caterpillar modulation of the attraction of D. rapae parasitoids.

On the other hand, attraction of the caterpillar parasitoid Diadegma semiclausum to volatiles emitted by A. thaliana plants simultaneously infested by caterpillars and aphids was influenced by the density of the feeding aphids. Biosynthesis and emission of the terpene (E,E)-α-farnesene could be linked to the observed preference of D. semiclausum parasitoids for the HIPV blend emitted by plants dually infested by caterpillars and aphids at a high density, compared to dually infested plants with a low aphid density.

Transcriptomic changes in the response of A. thaliana wild-type plants to simultaneous feeding by P. xylostella caterpillars and B. brassicae aphids compared to plants infested by P. xylostella caterpillars alone were assessed using a microarray analysis. I particularly addressed the question whether the transcriptomic response to simultaneously attacking aphids and caterpillars was dependent on aphid density and time since initiation of herbivory. The data show that in response to simultaneous feeding by P. xylostella caterpillars and B. brassicae aphids the number of differentially expressed genes was higher compared to plants on which caterpillars had been feeding alone. Additionally, specific genes were differentially expressed in response to aphids feeding at low or high density. Cluster analysis showed that the pattern of gene expression over the different time points in response to dual infestation was also affected by the density of the attacking aphids. These results suggest that insects attacking at a high density cause an acceleration in plant responses compared to insects attacking at low density.

As a next step in the study of multiple interacting herbivores, I studied whether plant responses to dual herbivory have consequences for the performance of a subsequently arriving herbivore, Mamestra brassicae caterpillars. The ecological consequences of plant responses to dual herbivory cascading into a chain of interactions affecting other community members have remained unstudied so far. We used wild B. oleracea plants to evaluate dual herbivore-induced plant adaptations for subsequent herbivory. We found that simultaneous feeding by P. xylostella and B. brassicae resulted in different plant defense-related gene expression and differences in plant hormone levels compared to single herbivory, and this had a negative effect on subsequently arriving M. brassicae caterpillars. Differential induction of JA-regulated transcriptional responses to dual insect attack was observed which could have mediated a decrease in M. brassicae performance. The induction of plant defense signaling also affected both P. xylostella and B. brassicae performance. This study further helps to understand herbivore community build-up in the context of plant-mediated species interactions.

Altogether, findings from this thesis reveal a molecular basis underlying plant responses against multiple herbivory and provide insight in plant-mediated interactions between aphids and caterpillars feeding on plants growing in the field or used in agriculture.

Arriving at the right time : a temporal perspective on above-belowground herbivore interactions
Wang, Minggang - \ 2016
University. Promotor(en): Wim van der Putten, co-promotor(en): T.M. Bezemer; A. Biere. - Wageningen : Wageningen University - ISBN 9789462578142 - 174 p.
herbivores - aboveground belowground interactions - herbivory - defence mechanisms - roots - leaves - mycorrhizas - population dynamics - soil biology - herbivoren - boven- en ondergrondse interacties - herbivorie - verdedigingsmechanismen - wortels - bladeren - mycorrhizae - populatiedynamica - bodembiologie
Regulation of cucumber (Cucumis sativus) induced defence against the two-spotted spider mite (Tetranychus urticae
He, J. - \ 2016
University. Promotor(en): Harro Bouwmeester; Marcel Dicke, co-promotor(en): Iris Kappers. - Wageningen : Wageningen University - ISBN 9789462576810 - 211 p.
cucumis sativus - cucumbers - induced resistance - plant pests - tetranychus urticae - mites - defence mechanisms - herbivore induced plant volatiles - herbivory - metabolomics - terpenoids - genomics - komkommers - geïnduceerde resistentie - plantenplagen - mijten - verdedigingsmechanismen - herbivoor-geinduceerde plantengeuren - herbivorie - metabolomica - terpenen - genomica

Plants have evolved mechanisms to combat herbivory. These mechanisms can be classified as direct defences which have a negative influence on the herbivores and indirect defence that attracts natural enemies of the attacking herbivores. Both direct and indirect defences can be constantly present or induced upon attack. This study, using cucumber (Cucumis sativus) and the two-spotted spider mite (Tetranychus urticae) as model, aimed to reveal the molecular mechanisms underlying the induced defence during herbivory, with emphasis on transcriptional changes and the involved TFs, the enzymatic function of the genes associated with volatile biosynthesis, and their promoters which regulate their expression.

Fitness consequences of indirect plant defence in the annual weed, Sinapis arvensis
Gols, R. ; Wagenaar, R. ; Poelman, E.H. ; Kruidhof, M. ; Loon, J.J.A. van; Harvey, J.A. - \ 2015
herbivory - plant defence - insect-plant interactions - multitrophic interactions - natural enemies - parasitoid - plant fitness
1. Plant traits that enhance the attraction of the natural enemies of their herbivores have been postulated to function as an ‘indirect defence’. An important underlying assumption is that this enhanced attraction results in increased plant fitness due to reduced herbivory. This assumption has been rarely tested. 2. We investigated whether there are fitness consequences for the charlock mustard Sinapis arvensis, a short-lived outcrossing annual weedy plant, when exposed to groups of large cabbage white (Pieris brassicae) caterpillars parasitized by either one of two wasp species, Hyposoter ebeninus and Cotesia glomerata, that allow the host to grow during parasitism. Hyposoter ebeninus is solitary and greatly reduces host growth compared with healthy caterpillars, whereas C. glomerata is gregarious and allows the host to grow approximately as large as unparasitized caterpillars. Both healthy and parasitized P. brassicae caterpillars initially feed on the foliage, but later stages preferentially consume the flowers. 3. In a garden experiment, plants damaged by parasitized caterpillars produced more seeds than conspecific plants damaged by unparasitized caterpillars. Reproductive potential (germination success multiplied by total seed number) was similar for plants that were not exposed to herbivory and those that were damaged by parasitized caterpillars and lower for plants that were damaged by healthy unparasitized caterpillars. However, these quantitative seed traits negatively correlated with the qualitative seed traits, individual seed size and germination success, suggesting a trade-off between these two types of traits. 4. We show that parasitism of insect herbivores that feed on reproductive plant tissues may have positive fitness consequences for S. arvensis. The extent to which plant fitness may benefit depends on parasitoid lifestyle (solitary or gregarious), which is correlated with the amount of damage inflicted on these tissues by the parasitized host.
Host location by hyperparasitoids: an ecogenomic approach
Zhu, F. - \ 2015
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.

Getting prepared for future attack : induction of plant defences by herbivore egg deposition and consequences for the insect community
Pashalidou, F.G. - \ 2015
University. Promotor(en): Marcel Dicke; Joop van Loon, co-promotor(en): Nina Fatouros. - Wageningen : Wageningen University - ISBN 9789462574120 - 168
insect-plant relaties - planten - insectenplagen - herbivorie - verdedigingsmechanismen - geïnduceerde resistentie - herbivoor-geinduceerde plantengeuren - ovipositie - natuurlijke vijanden - brassica - pieris brassicae - trofische graden - sluipwespen - hyperparasitoïden - insectengemeenschappen - insect plant relations - plants - insect pests - herbivory - defence mechanisms - induced resistance - herbivore induced plant volatiles - oviposition - natural enemies - trophic levels - parasitoid wasps - hyperparasitoids - insect communities

Plants have evolved intriguing defences against insect herbivores. Compared to constitutive Plants have evolved intriguing defences against insect herbivores. Compared to constitutive defences that are always present, plants can respond with inducible defences when they are attacked. Insect herbivores can induce phenotypic changes in plants and consequently these changes may differentially affect subsequent attackers and their associated insect communities. Many studies consider herbivore-feeding damage as the first interaction between plants and insects. The originality of this study was to start with the first phase of herbivore attack, egg deposition, to understand the consequences of plant responses to eggs on subsequently feeding caterpillars and their natural enemies. The main plant species used for most of the experiments was Brassica nigra (black mustard), which occurs naturally in The Netherlands. The main herbivore used was the lepidopteran Pieris brassicae, which lays eggs in clusters and feeds on plants belonging to the Brassicaceae family. This study investigated plant-mediated responses to oviposition and their effects on different developmental stages of the herbivore, such as larvae and pupae. Furthermore, the effects of oviposition were extended to four more plant species of the same family, and to higher trophic levels including parasitoids and hyperparasitoids. The experiments were conducted under laboratory, semi-field and field conditions. This study shows that B. nigra plants recognize the eggs of P. brassicae and initiate resistance against subsequent developmental stages of the herbivore. Interestingly, plant responses to oviposition were found to be species specific. Plants did not respond to egg deposition by another herbivore species, the generalist moth Mamestra brassicae. Moreover, most of the Brassicaceae species tested were found to respond to P. brassicae eggs, which indicates that plant responses against oviposition are more common among the family of Brassicaceae. To assess effects on other members of the food chain, the effects of oviposition on plant volatile emission and the attraction of parasitic wasps, such as the larval parasitoid Cotesia glomerata, were tested. It was shown that the wasps were able to use the blend of plant volatiles, altered by their hosts’ oviposition, to locate young caterpillars just after hatching from eggs. The observed behaviour of the wasps was associated with higher parasitism success and higher fitness in young hosts. Similar results were obtained in a field experiment, where plants infested with eggs and caterpillars attracted more larval parasitoids and hyperparasitoids and eventually produced more seeds compared to plants infested with caterpillars only. This study shows that an annual weed like B. nigra uses egg deposition as reliable information for upcoming herbivory and responds accordingly with induced defences. Egg deposition could influence plant-associated community members at different levels in the food chain and benefit seed production. As the importance of oviposition on plant-herbivore interactions is only recently discovered, more research is needed to elucidate the mechanisms that underlie such plant responses and how these interactions affect the structure of insect communities in nature.

Fitness consequences of indirect plant defence in the annual weed, Sinapis arvensis
Gols, R. ; Wagenaar, R. ; Poelman, E.H. ; Kruidhof, H.M. ; Loon, J.J.A. van; Harvey, J.A. - \ 2015
Functional Ecology 29 (2015)8. - ISSN 0269-8463 - p. 1019 - 1025.
pieris-brassicae - herbivory - tolerance - evolution - volatiles - insects - parasitoids - strategies - selection - ecology
Plant traits that enhance the attraction of the natural enemies of their herbivores have been postulated to function as an 'indirect defence'. An important underlying assumption is that this enhanced attraction results in increased plant fitness due to reduced herbivory. This assumption has been rarely tested. We investigated whether there are fitness consequences for the charlock mustard Sinapis arvensis, a short-lived outcrossing annual weedy plant, when exposed to groups of large cabbage white (Pieris brassicae) caterpillars parasitized by either one of two wasp species, Hyposoter ebeninus and Cotesia glomerata, that allow the host to grow during parasitism. Hyposoter ebeninus is solitary and greatly reduces host growth compared with healthy caterpillars, whereas C. glomerata is gregarious and allows the host to grow approximately as large as unparasitized caterpillars. Both healthy and parasitized P. brassicae caterpillars initially feed on the foliage, but later stages preferentially consume the flowers. In a garden experiment, plants damaged by parasitized caterpillars produced more seeds than conspecific plants damaged by unparasitized caterpillars. Reproductive potential (germination success multiplied by total seed number) was similar for plants that were not exposed to herbivory and those that were damaged by parasitized caterpillars and lower for plants that were damaged by healthy unparasitized caterpillars. However, these quantitative seed traits negatively correlated with the qualitative seed traits, individual seed size and germination success, suggesting a trade-off between these two types of traits. We show that parasitism of insect herbivores that feed on reproductive plant tissues may have positive fitness consequences for S. arvensis. The extent to which plant fitness may benefit depends on parasitoid lifestyle (solitary or gregarious), which is correlated with the amount of damage inflicted on these tissues by the parasitized host
Salt-marsh erosion and restoration in relation to flood protection on the Wadden Sea barrier island Terschelling
Loon-Steensma, J.M. van; Slim, P.A. ; Decuyper, M. ; Hu, Zhan - \ 2014
Journal of Coastal Conservation 18 (2014)4. - ISSN 1400-0350 - p. 415 - 430.
north norfolk - vegetation - succession - herbivory - estuary - defense - field
This paper explores the impact of erosion and restoration measures on habitat development and on wave damping by a small salt marsh nestled alongside a dike on the Wadden island of Terschelling. The aim is to advance knowledge about the benefits and possible side-effects of salt-marsh restoration. Analysis of a time series of aerial photographs from 1944 to 2010 indicates that the salt marsh decreased steadily in size after maintenance of accretion works was terminated. In the western part of the marsh, which is accessible to sheep, vegetation is low (5–15 cm) and dominated by Salicornia europaea and by Spartina anglica. In the most intensively grazed parts, vegetation is very scarce. The eastern, inaccessible part of the salt marsh is covered by dense patches of the shrubby perennial Atriplex portulacoides and Spartina anglica (15–25 cm in height). SWAN wave models show that wave height at this location is significantly affected by the areal extent of the salt marsh as well as by the vegetation. High or dense vegetation are in the models nearly as effective in damping waves (with an initial height of 0.15 and 0.5 m) as widening the salt-marsh area by 350 m. A low density of low plants, as observed in the grazed part of the marsh, has almost no wave-damping effect. Even under conditions of sea level rise, a broader salt marsh vegetated with high plants significantly affects modelled wave height. Therefore, salt-marsh restoration is an adaptation measure worth exploring, though an array of effect types must be considered.
Dendrochronology of Atriplex portulacoides and Artemisia maritima in Wadden Sea salt marshes
Decuyper, M. ; Slim, P.A. ; Loon-Steensma, J.M. van - \ 2014
Journal of Coastal Conservation 18 (2014)3. - ISSN 1400-0350 - p. 279 - 284.
wood anatomy - chenopodiaceae - competition - succession - herbivory - defense
The study uses a rather unusual method, dendrochronology, to investigate the growth and survival of Atriplex portulacoides L. and Artemisia maritima L. on salt marshes at two field sites on the Dutch North Sea barrier islands of Terschelling and Ameland. By providing information on longevity of these typical salt-marsh shrubs, dendrochronology offers an indirect way to investigate the influence of management regime – grazing in this case – on marsh quality and areal extent. Diminishment of salt marshes is a continuing concern in the northern Netherlands. The two shrub species studied here, A. portulacoides and A. maritima, are common to salt marshes. With their extensive roots and branches, they facilitate sedimentation and stabilize salt marshes. Using dendrochronology, this study found that annual growth rings could be identified to determine shrub age and growth. In A. portulacoides these rings took the form of a narrow band of terminal parenchyma. In A. maritima they were made up of unlignified marginal parenchyma together with higher vessel density at the beginning of the growing season. Growth rings indicated that intense grazing was clearly detrimental to the survival of A. portulacoides at the Terschelling site. However, grazing facilitated survival of A. maritima at the Ameland site by reducing light and nutrient competition from grasses. No growth trends could be found, however, as the lifespan for both species is short and many other influences on shrub growth could be identified.
Defoliation effects on seed dispersal and seedling recruitment in a tropical rain forest understorey palm
Lent, J. van; Hernandez-Barrios, J.C. ; Anten, N.P.R. ; Martinez-Ramos, M. - \ 2014
Journal of Ecology 102 (2014)3. - ISSN 0022-0477 - p. 709 - 720.
plant-population - herbaceous perennials - temperate forest - patch dynamics - olea-europaea - leaf harvest - vital-rates - source-sink - dry forest - herbivory
1. Assessing the demographic effects of leaf area losses in perennial plants is important to determine population resilience to natural and anthropogenic disturbances. Yet, while impacts of defoliation on vital rates of adult plants have been well documented, consequences for seed dispersal and seedling recruitment have been barely explored. 2. Here, we assessed the effects of defoliation on fruit production, fruit/seed size, seed dispersal and seedling recruitment in populations of Chamaedorea ernesti-augustii, a tropical rain forest, understorey palm from Mesoamerica, whose leaves are exploited as a highly valuable non-timber forest product (NTFP). 3. Fruit size and seed production were quantified in mature palms that were subjected to 0% (control), 25%, 50%, 75% and 100% experimental removal of standing leaves, applied every 6 months over 2 years. Seed dispersal by birds and gravity, and seed predation by small vertebrates on the ground were also quantified. Rates of seedling recruitment were recorded in non-defoliated and ‘sterile’ populations (75% sustained defoliation and periodical removal of all produced fruits). Finally, a stochastic model was used to quantify the overall effect of defoliation on seedlings recruited from locally (i.e. dispersed by gravity) and immigrant produced seeds (i.e. dispersed by birds). 4. Increasing defoliation strongly reduced seed production. The probability of bird dispersal was positively correlated with fruit/seed size. Isolated (i.e. bird-dispersed) seeds endured lower predation rates than grouped (i.e. gravity-dispersed) ones. Modelling showed that seedling recruitment rate is severely reduced in highly defoliated populations due to a strong decline in the number of seedlings coming from local seed sources. Surrounding non-defoliated populations could partly compensate for this effect via seedlings coming from immigrant seeds. 5. Synthesis. Chronic and intense defoliation negatively affects seed production and dispersal, which reduces the probability of seedling recruitment. Such effects may have a profound impact on the dynamics and genetic variability of populations, which should be taken into account when considering the effects of natural defoliation and sustainability of leaf-harvesting regimes.
Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea.
Tytgat, T. ; Verhoeven, K.J.F. ; Janssen, J.J. ; Raaijmakers, C.E. ; Bakx-Schotman, J.M.T. ; McIntyre, L.M. ; Putten, W.H. van der; Biere, A. ; Dam, N.M. van - \ 2013
PLoS One 8 (2013)6. - ISSN 1932-6203
gene-expression - arabidopsis-thaliana - jaz repressors - multitrophic interactions - 12-oxo-phytodienoic acid - stress responses - herbivory - dynamics - defenses - carbon
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.
Reproductive escape: annual plant responds to butterfly eggs by accelerating seed production
Lucas-Barbosa, D. ; Loon, J.J.A. van; Gols, R. ; Beek, T.A. van; Dicke, M. - \ 2013
Functional Ecology 27 (2013)1. - ISSN 0269-8463 - p. 245 - 254.
pieris-brassicae - raphanus-raphanistrum - solanum-carolinense - volatile emissions - flower visitation - insect eggs - herbivory - pollinators - ecology - defense
1.Plants respond to insect herbivores with changes in physical and chemical traits, both locally and systemically, in leaves and flowers. Such phenotypic changes may influence the behaviour of every community member that interacts with the plant. Here, we address effects of plant responses to eggs and subsequent herbivory by caterpillars on plant-mediated interactions with pollinators and consequences for plant fitness. 2.Using a common garden set-up, we have investigated responses of Brassica nigra plants to herbivore exposure from egg deposition onwards throughout larval development. We quantified effects of infestation by the specialist Pieris brassicae on: 1. behaviour of pollinators; 2. volatile emission and 3. timing and number of seeds produced. 3.Egg deposition and folivory did not influence visitation by pollinators to plots of infested or control plants. Effects of herbivore infestation on both pollinator visitation and volatile emission were observed only at a later stage, when caterpillars were feeding on the flowers. 4.Remarkably, before eggs had hatched, infested plants accelerated seed production. The caterpillars that developed from the eggs fed on flowers but not on seeds and thus seed production prior to herbivory on flowers safeguarded reproductive output. 5.The results of this study show that early plant investments in reproduction can successfully prevent consumption of expensive reproductive tissues. By accelerating seed production, plants prevented consumption of flowers and effectively defended themselves against the herbivores
A gain-of-function polymorphism controlling complex traits and fitness in nature
Prasad, K.V.S.K. ; Song, B. ; Olson-Manning, C. ; Anderson, J.T. ; Lee, C. ; Schranz, Eric ; Windsor, A.J. ; Clauss, M.J. ; Manzaneda, A.J. ; Naqvi, I. ; Reichelt, M. ; Gershenzon, J. ; Rupasinghe, S.G. ; Schuler, M.A. ; Mitchell-Olds, T. - \ 2012
glucosinolate - herbivory - ecological genomics - Boechera stricta
Identification of the causal genes that control complex trait variation remains challenging, limiting our appreciation of the evolutionary processes that influence polymorphisms in nature. We cloned a quantitative trait locus that controls plant defensive chemistry, damage by insect herbivores, survival, and reproduction in the natural environments where this polymorphism evolved. These ecological effects are driven by duplications in the BCMA (branched-chain methionine allocation) loci controlling this variation and by two selectively favored amino acid changes in the glucosinolate-biosynthetic cytochrome P450 proteins that they encode. These changes cause a gain of novel enzyme function, modulated by allelic differences in catalytic rate and gene copy number. Ecological interactions in diverse environments likely contribute to the widespread polymorphism of this biochemical function.
Cutting affects growth of Potamogeton lucens L. and Potamogeton compressus L
Zuidam, J.P. van; Peeters, E.T.H.M. - \ 2012
Aquatic Botany 100 (2012). - ISSN 0304-3770 - p. 51 - 55.
macrophyte communities - aquatic macrophytes - vegetation - habitat - impact - biodiversity - netherlands - diversity - herbivory - responses
Effects of cutting on the growth of Potamogeton lucens L and Potamogeton compressus L were studied indoor under experimental conditions. Plants were cut every time they reached the water surface, applying three depth treatments at which the plants were cut; halfway down the water column, at three-quarters down the water column and at the sediment-water interface. For both species short term negative effects of cutting on biomass production and survival were observed. P. lucens seemed to be the more tolerant species as only below-ground biomass was significantly lower when cutting biomass at the sediment-water interface together with a downward trend in shoot biomass at increasing cutting depth. The low below-ground biomass (less than 20% of that in the controls) was caused by the death of most plants in this treatment. P. compressus was more vulnerable with every treatment resulting in significantly lower below-ground and green shoot biomass production. The lowest biomass for P. compressus was observed when plants were cut at the sediment-water interface with values more than 80% lower compared to the controls, while cutting halfway and at three-quarters resulted in values 30-50% lower compared to the controls. Long term effects of cutting on P. lucens might occur through decreased development of the rhizome network. Long term effects on reproduction of P. compressus might be expected as flowering decreased when cut at the sediment-water interface, while turion formation only occurred in the uncut controls. Additionally, the decreased biomass production by P. compressus may lead to a competitive disadvantage in the field as fast-growing, disturbance tolerant species such as Elodea nuttallii St. John may outcompete the species. Creating patchiness in mowing height and frequency or applying a mowing regime that leads to reduced biomass development while species still survive might create opportunities to both maintain the water transporting function of drainage ditches while preserving the species in the system.
Defoliation and gender effects on fitness components in three congeneric and sympatric understorey palms
Hernández-Barrios, J.C. ; Anten, N.P.R. ; Ackerly, D.D. - \ 2012
Journal of Ecology 100 (2012)6. - ISSN 0022-0477 - p. 1544 - 1556.
tropical rain-forest - neotropical dioecious palm - compensatory responses - chamaedorea-radicalis - resource availability - water availability - acer-negundo - leaf harvest - growth - herbivory
1.Rain forest understorey perennial plants can be frequently exposed to leaf area losses induced by herbivory or physical damage from falling canopy debris. In dioecious species, tolerance to defoliation may differ between genders (e.g. females may suffer more than males), but this topic has so far received little attention. 2.Here, we quantified gender-dependent effects of increased levels (0–100%) of sustained defoliation (applied bi-annually for 2 years) on vital rates in three economically important dioecious understorey palm species in the genus Chamaedorea (C. elegans, C. ernesti-augustii and C. oblongata). We also quantified gender differences in functional and life-history traits and assessed the direct reproductive costs in terms of biomass allocation to reproduction. 3.In the three species, non-defoliated (control) females were smaller and had three to seven times higher reproductive allocation than males. 4.Defoliation did not affect survivorship in any of the three species, except in the 100% defoliation treatment. Stem growth (RGR) and especially reproduction (probability of reproduction and reproductive output) were negatively affected by defoliation. Females of C. ernesti-augustii suffered higher mortality than males at 100% defoliation, but this was not the case for the other two species. Also, only in C. ernesti-augustii females exhibited lower RGR than males. In all species, the probability of reproduction did not differ between genders. The reproductive output (production rate of inflorescences) differed among genders only in C. ernesti-augustii, where males were more productive than females. 5.Interestingly, in most cases, defoliation effects on vital rates did not differ significantly between males and females, indicating that tolerance to defoliation was similar between genders. Such results were independent of plant size (stem length). 6.Synthesis. Our results do not support the prevailing theory that the greater reproductive costs of females will lead to reduced tolerance to stresses such as defoliation. The implications of these results and their importance for designing sustainable leaf harvesting regimes are discussed.
Transgenerational Effects of Stress Exposure on Offspring Phenotypes in Apomictic Dandelion
Verhoeven, K.J.F. ; Gurp, T.P. van - \ 2012
PLoS One 7 (2012)6. - ISSN 1932-6203
arabidopsis-thaliana - trichome density - mimulus-guttatus - plants - responses - methylation - plasticity - herbivory - consequences - inheritance
Heritable epigenetic modulation of gene expression is a candidate mechanism to explain parental environmental effects on offspring phenotypes, but current evidence for environment-induced epigenetic changes that persist in offspring generations is scarce. In apomictic dandelions, exposure to various stresses was previously shown to heritably alter DNA methylation patterns. In this study we explore whether these induced changes are accompanied by heritable effects on offspring phenotypes. We observed effects of parental jasmonic acid treatment on offspring specific leaf area and on offspring interaction with a generalist herbivore; and of parental nutrient stress on offspring root-shoot biomass ratio, tissue P-content and leaf morphology. Some of the effects appeared to enhance offspring ability to cope with the same stresses that their parents experienced. Effects differed between apomictic genotypes and were not always consistently observed between different experiments, especially in the case of parental nutrient stress. While this context-dependency of the effects remains to be further clarified, the total set of results provides evidence for the existence of transgenerational effects in apomictic dandelions. Zebularine treatment affected the within-generation response to nutrient stress, pointing at a role of DNA methylation in phenotypic plasticity to nutrient environments. This study shows that stress exposure in apomictic dandelions can cause transgenerational phenotypic effects, in addition to previously demonstrated transgenerational DNA methylation effects.
Resilience to chronic defoliation in a dioecious understorey tropical rain forest palm
Lopez-Toledo, L. ; Anten, N.P.R. ; Endress, B.A. ; Ackerly, D.D. ; Martínez-Ramos, M. - \ 2012
Journal of Ecology 100 (2012)5. - ISSN 0022-0477 - p. 1245 - 1256.
carbohydrate reserves - astrocaryum-mexicanum - seedling survival - leaf harvest - vital-rates - growth - reproduction - herbivory - plants - sustainability
1. Perennial plants often endure chronic loss of leaf area due to recurrent physical damage, herbivory and, for species used as non-timber forest products, due to leaf harvesting. However, little is known about functional and demographic resilience (extent and speed of recovery) of plants subjected to varying levels of chronic defoliation. 2. We used a dioecious, understorey palm (Chamaedorea elegans) to evaluate temporal trajectories and rates of recovery of leaf functional traits and vital rates (survival, growth and reproduction) after being subjected to experimental chronic defoliation regimes. 3. Pristine populations of mature C. elegans, categorized by gender (male and female), were subjected to five defoliation levels (0%, 33%, 50%, 66% or 100% of newly produced leaves) every 6 months over a period of 3 years (1997–2000). To evaluate recovery from defoliation, surviving palms were monitored for 3 years after the cessation of the defoliation treatment (2000–2003). We recorded leaf functional traits (leaf persistence, leaf production rate, leaf size and leaf area) and annual rates of mortality, growth and reproduction. 4. Cumulative effects of chronic defoliation concomitantly reduced leaf traits, survival, growth and reproduction, and this effect was stronger in female than in male palms, independent of plant size. Recovery from defoliation was faster in males than in females, but proceeded gradually overall. Survival increased first, followed by growth, while reproductive traits showed the slowest recovery rate. Recovery was independent of plant size. Notably, 3 years after defoliation treatment, the standing leaf area and probability of reproduction had not recovered to pre-defoliation levels. Additionally, we found that the occurrence of a severe drought in the first year (2000) after defoliation ceased led to decreased survival, growth and reproduction and the ability of plants to recover from defoliation. 5. Synthesis. Chronic defoliation reduces fitness components of C. elegans palms differentially between genders. Recovery is gradual and is slower and less complete in females compared with males. The lower level of resilience to chronic defoliation shown by female plants may have profound consequences for the dynamics and genetic variability of populations of tropical understorey plants undergoing prolonged defoliation. Such effects may be aggravated by severe drought episodes that are expected to increase in frequency according to global climate change predictions.
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