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.

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

    Full text documents are added when available. The database is updated daily and currently holds about 240,000 items, of which 72,000 in open access.

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    Supplementary material from "How to escape from insect egg parasitoids: a review of potential factors explaining parasitoid absence across the Insecta"
    Fatouros, N.E. ; Cusumano, A. ; Bin, F. ; Polaszek, A. ; Lenteren, J.C. van - \ 2020
    Wageningen University & Research
    egg deposition - oviposition site - egg protection - parental care - herbivory - hymenoptera
    The egg is the first life stage directly exposed to the environment in oviparous animals, including many vertebrates and most arthropods. Eggs are vulnerable and prone to mortality risks. In arthropods, one of the most common egg mortality factors is attack from parasitoids. Yet, parasitoids that attack the egg stage are absent in more than half of all insect (sub)orders. In this review, we explore possible causes explaining why eggs of some insect taxa are not parasitized. Many insect (sub)orders that are not attacked by egg parasitoids lack herbivorous species, with some notable exceptions. Factors we consider to have led to escape from egg parasitism are parental egg care, rapid egg development, small egg size, hiding eggs, by e.g. placing them into the soil, applying egg coatings or having thick chorions preventing egg penetration, ‘eusociality, and egg cannibalism.’ A quantitative network analysis of host–parasitoid associations shows that the five most-speciose genera of egg parasitoids display patterns of specificity with respect to certain insect orders, especially Lepidoptera and Hemiptera, largely including herbivorous species that deposit their eggs on plants. Finally, we discuss the many counteradaptations that particularly herbivorous species have developed to lower the risk of attack by egg parasitoids.
    Determinants of tree seedling establishment in alpine tundra
    Marsman, Floor ; Nystuen, Kristin O. ; Opedal, Øystein H. ; Foest, Jessie J. ; Sørensen, Mia Vedel ; Frenne, Pieter De; Graae, Bente Jessen ; Limpens, Juul - \ 2020
    Journal of Vegetation Science (2020). - ISSN 1100-9233
    above-ground competition - alpine tundra - exclosure - herbivory - invasibility - microclimate - Pinus sylvestris - shrub encroachment

    Questions: Changes in climate and herbivory pressure affect northern alpine ecosystems through woody plant encroachment, altering their composition, structure and functioning. The encroachment often occurs at unequal rates across heterogeneous landscapes, hinting at the importance of habitat-specific drivers that either hamper or facilitate woody plant establishment. Here, we assess: (1) the invasibility of three distinct alpine plant community types (heath, meadow and Salix shrubland) by Pinus sylvestris (Scots pine); and (2) the relative importance of biotic (above-ground interactions with current vegetation, herbivory and shrub encroachment) and microclimate-related abiotic (soil temperature, moisture and light availability) drivers of pine seedling establishment success. Location: Dovrefjell, Central Norway. Methods: We conducted a pine seed sowing experiment, testing how factorial combinations of above-ground removal of co-occurring vegetation, herbivore exclusion and willow transplantation (simulated shrub encroachment) affect pine emergence, survival and performance (new stem growth, stem height and fraction of healthy needles) in three plant communities, characteristic of alpine tundra, over a period of five years. Results: Pine seedling emergence and survival were similar across plant community types. Herbivore exclusion and vegetation removal generally increased pine seedling establishment and seedling performance. Within our study, microclimate had minimal effects on pine seedling establishment and performance. These results illustrate the importance of biotic resistance to seedling establishment. Conclusion: Pine seedlings can easily establish in alpine tundra, and biotic factors (above-ground plant interactions and herbivory) are more important drivers of pine establishment in alpine tundra than abiotic, microclimate-related, factors. Studies aiming to predict future vegetation changes should thus consider local-scale biotic interactions in addition to abiotic factors.

    Climate change-mediated temperature extremes and insects: From outbreaks to breakdowns
    Harvey, Jeffrey A. ; Heinen, Robin ; Gols, Rieta ; Thakur, Madhav P. - \ 2020
    Global Change Biology 26 (2020)12. - ISSN 1354-1013 - p. 6685 - 6701.
    anthropogenic climate change - biodiversity - climatic extremes - heatwaves - herbivory - insect physiology - multitrophic interactions - parasitoids - predators
    Insects are among the most diverse and widespread animals across the biosphere and are well-known for their contributions to ecosystem functioning and services. Recent increases in the frequency and magnitude of climatic extremes (CE), in particular temperature extremes (TE) owing to anthropogenic climate change, are exposing insect populations and communities to unprecedented stresses. However, a major problem in understanding insect responses to TE is that they are still highly unpredictable both spatially and temporally, which reduces frequency- or direction-dependent selective responses by insects. Moreover, how species interactions and community structure may change in response to stresses imposed by TE is still poorly understood. Here we provide an overview of how terrestrial insects respond to TE by integrating their organismal physiology, multitrophic, and community-level interactions, and building that up to explore scenarios for population explosions and crashes that have ecosystem-level consequences. We argue that TE can push insect herbivores and their natural enemies to and even beyond their adaptive limits, which may differ among species intimately involved in trophic interactions, leading to phenological disruptions and the structural reorganization of food webs. TE may ultimately lead to outbreak–breakdown cycles in insect communities with detrimental consequences for ecosystem functioning and resilience. Lastly, we suggest new research lines that will help achieve a better understanding of insect and community responses to a wide range of CE.
    How to escape from insect egg parasitoids : a review of potential factors explaining parasitoid absence across the Insecta
    Fatouros, N.E. ; Cusumano, A. ; Bin, F. ; Polaszek, A. ; Lenteren, J.C. van - \ 2020
    Proceedings of the Royal Society. B: Biological Sciences 287 (2020)1931. - ISSN 0962-8452 - 1 p.
    egg deposition - egg protection - herbivory - hymenoptera - oviposition site - parental care

    The egg is the first life stage directly exposed to the environment in oviparous animals, including many vertebrates and most arthropods. Eggs are vulnerable and prone to mortality risks. In arthropods, one of the most common egg mortality factors is attack from parasitoids. Yet, parasitoids that attack the egg stage are absent in more than half of all insect (sub)orders. In this review, we explore possible causes explaining why eggs of some insect taxa are not parasitized. Many insect (sub)orders that are not attacked by egg parasitoids lack herbivorous species, with some notable exceptions. Factors we consider to have led to escape from egg parasitism are parental egg care, rapid egg development, small egg size, hiding eggs, by e.g. placing them into the soil, applying egg coatings or having thick chorions preventing egg penetration, eusociality, and egg cannibalism. A quantitative network analysis of host-parasitoid associations shows that the five most-speciose genera of egg parasitoids display patterns of specificity with respect to certain insect orders, especially Lepidoptera and Hemiptera, largely including herbivorous species that deposit their eggs on plants. Finally, we discuss the many counteradaptations that particularly herbivorous species have developed to lower the risk of attack by egg parasitoids.

    Soil eutrophication shaped the composition of pollinator assemblages during the past century
    Carvalheiro, Luísa G. ; Biesmeijer, Jacobus C. ; Franzén, Markus ; Aguirre-Gutiérrez, Jesús ; Garibaldi, Lucas A. ; Helm, Aveliina ; Michez, Denis ; Pöyry, Juha ; Reemer, Menno ; Schweiger, Oliver ; Leon van den, Berg ; WallisDeVries, Michiel F. ; Kunin, William E. - \ 2020
    Ecography 43 (2020)2. - ISSN 0906-7590 - p. 209 - 221.
    extinction debt - herbivory - historical biodiversity changes - nitrogen deposition - nitrophily - pollinator communities

    Atmospheric nitrogen deposition and other sources of environmental eutrophication have increased substantially over the past century worldwide, notwithstanding the recent declining trends in Europe. Despite the recognized susceptibility of plants to eutrophication, few studies evaluated how impacts propagate to consumers, such as pollinators. Here we aim to test if soil eutrophication contributes to the temporal dynamics of pollinators and their larval resources. We used a temporally and spatially explicit historical dataset with information on species occurrences to test if soil eutrophication, and more specifically nitrogen deposition, contributes to the patterns of change of plant and pollinator richness in the Netherlands over an 80 yr period. We focus on bees and butterflies, two groups for which we have good knowledge of larval resources that allowed us to define groups of species with different nitrogen related diet preferences. For each group we estimated richness changes between different 20-yr periods at local, regional and national scale, using analytical methods developed for analyzing richness changes based on collection data. Our findings suggest that the impacts of soil eutrophication on plant communities propagate to higher trophic levels, but with a time-lag. Pollinators with nitrogen-related diet preferences were particularly affected, in turn potentially impairing the performance of pollinator-dependent plants. Pollinator declines continued even after their focal plants started to recover. In addition, our results suggest that current levels of nitrogen deposition still have a negative impact on most groups here analyzed, constraining richness recoveries and accentuating declines. Our results indicate that the global increase in nitrogen availability plays an important role in the ongoing pollinator decline. Consequently, species tolerances to soil nitrogen levels should be considered across all trophic levels in management plans that aim to halt biodiversity loss and enhance ecosystems services worldwide.

    A native with a taste for the exotic: weeds and pasture provide year-round habitat for Nysius vinitor (Hemiptera: Orsillidae) across Australia, with implications for area-wide management
    Parry, Hazel R. ; Marcora, Anna ; Macfadyen, Sarina ; Hopkinson, Jamie ; Hulthen, Andrew D. ; Neave, Mick ; Bianchi, Felix J.J.A. ; Franzmann, Bernard A. ; Lloyd, Richard J. ; Miles, Melina ; Zalucki, Myron P. ; Schellhorn, Nancy A. - \ 2019
    Austral Entomology 58 (2019)2. - ISSN 2052-174X - p. 237 - 247.
    arthropod - habitat management - herbivory - pest management - Rutherglen bug - weed

    While pest management tends to focus on pests that are already present in crops, non-crop hosts may play a crucial role in supporting pest populations outside the crop growing season. Non-crop hosts may allow pest populations to persist throughout the year, build-up and colonise crops after emergence. Here, we assess the hosts of the Rutherglen bug, Nysius vinitor Bergroth, which is a polyphagous native insect pest of growing economic importance in Australia. We conducted a literature review on the occurrence of N. vinitor on crop and non-crop hosts and analysed field survey data on N. vinitor abundance from two independent field studies in three agricultural regions of Australia. We differentiated between juvenile (nymph) and adult stages to consider the function of plants as reproduction sites. The literature review resulted in reports of N. vinitor on 44 crop species from 18 plant families. Pigweed Portulaca oleracea and capeweed Arctotheca calendula were the most cited weed hosts. In the field study, N. vinitor was primarily found on exotic weeds and grasses within pastures, Lucerne and degraded native vegetation remnants. While N. vinitor was found on a total of 16 weed plant families, juvenile stages of N. vinitor were most often observed on fleabane (Conyza spp.), goosefoot Chenopodium pumilio (Amaranthaceae) and plants of the Asteraceae family, indicating that these are important host plants for N.

    Ecological significance of light quality in optimizing plant defence
    Douma, Jacob C. ; Vries, Jorad de; Poelman, Erik H. ; Dicke, Marcel ; Anten, Niels P.R. ; Evers, Jochem B. - \ 2019
    Plant, Cell & Environment 42 (2019)3. - ISSN 0140-7791 - p. 1065 - 1077.
    Brassica nigra - competition - functional–structural plant modelling - growth-defence trade-off - herbivory - plant defence - red to far-red ratio - shade avoidance

    Plants balance the allocation of resources between growth and defence to optimize fitness in a competitive environment. Perception of neighbour-detection cues, such as a low ratio of red to far-red (R:FR) radiation, activates a suite of shade-avoidance responses that include stem elongation and upward leaf movement, whilst simultaneously downregulating defence. This downregulation is hypothesized to benefit the plant either by mediating the growth-defence balance in favour of growth in high plant densities or, alternatively, by mediating defence of individual leaves such that those most photosynthetically productive are best protected. To test these hypotheses, we used a 3D functional–structural plant model of Brassica nigra that mechanistically simulates the interactions between plant architecture, herbivory, and the light environment. Our results show that plant-level defence expression is a strong determinant of plant fitness and that leaf-level defence mediation by R:FR can provide a fitness benefit in high densities. However, optimal plant-level defence expression does not decrease monotonically with plant density, indicating that R:FR mediation of defence alone is not enough to optimize defence between densities. Therefore, assessing the ecological significance of R:FR-mediated defence is paramount to better understand the evolution of this physiological linkage and its implications for crop breeding.

    Ecological interactions shape the adaptive value of plant defence : Herbivore attack versus competition for light
    Vries, Jorad de; Evers, Jochem B. ; Dicke, Marcel ; Poelman, Erik H. - \ 2019
    Functional Ecology 33 (2019)1. - ISSN 0269-8463 - p. 129 - 138.
    Brassica nigra - competition - ecological costs - functional-structural plant modelling - growth-defence trade-off - herbivore interactions - herbivory - plant - plant defence

    Plants defend themselves against diverse communities of herbivorous insects. This requires an investment of limited resources, for which plants also compete with neighbours. The consequences of an investment in defence are determined by the metabolic costs of defence as well as indirect or ecological costs through interactions with other organisms. These ecological costs have a potentially strong impact on the evolution of defensive traits, but have proven to be difficult to quantify. We aimed to quantify the relative impact of the direct and indirect or ecological costs and benefits of an investment in plant defence in relation to herbivory and intergenotypic competition for light. Additionally, we evaluated how the benefits of plant defence balance its costs in the context of herbivory and intergenotypic competition. To this end, we utilised a functional-structural plant (FSP) model of Brassica nigra that simulates plant growth and development, morphogenesis, herbivory and plant defence. In the model, a simulated investment in defences affected plant growth by competing with other plant organs for resources and affected the level and distribution of herbivore damage. Our results show that the ecological costs of intergenotypic competition for light are highly detrimental to the fitness of defended plants, as it amplifies the size difference between defended and undefended plants. This leads to herbivore damage counteracting the effects of intergenotypic competition under the assumption that herbivore damage scales with plant size. Additionally, we show that plant defence relies on reducing herbivore damage rather than the dispersion of herbivore damage, which is only beneficial under high levels of herbivore damage. We conclude that the adaptive value of plant defence is highly dependent on ecological interactions and is predominantly determined by the outcome of competition for light.

    Data from: Modulation of plant-mediated interactions between herbivores of different feeding guilds: effects of parasitism and belowground interactions
    Vaello, Teresa ; Sarde, Sandeep ; Marcos-García, Mª Ángeles ; Boer, J.G. de; Pineda, Ana - \ 2018
    Universidad de Alicante
    plant soil feedback - herbivory - plant defense - insect - parasitism - gene expression
    Herbivory affects subsequent herbivores, mainly regulated by the phytohormones jasmonic (JA) and salicylic acid (SA). Additionally, organisms such as soil microbes belowground or parasitoids that develop inside their herbivorous hosts aboveground, can change plant responses to herbivory. However, it is not yet well known how organisms of trophic levels other than herbivores, below- and above-ground, alter the interactions between insect species sharing a host plant. Here, we investigated whether the parasitoid Aphidius colemani and different soil microbial communities (created through plant-soil feedbacks) affect the JA and SA signalling pathways in response to the aphid Myzus persicae and the thrips Frankliniella occidentalis, as well as subsequent thrips performance. Our results show that the expression of the JA-responsive gene CaPINII in sweet pepper was more suppressed by aphids than by parasitised aphids. However, parasitism did not affect the expression of CaPAL1, a biosynthetic gene of SA. Furthermore, aphid feeding enhanced thrips performance compared with uninfested plants, but this was not observed when aphids were parasitised. Soils where different plant species were previously grown, did not affect plant responses or the interaction between herbivores. Our study shows that members of the third trophic level can modify herbivore interactions by altering plant physiology.
    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
    Wageningen University & Research
    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
    Wageningen University. Promotor(en): Marcel Dicke, co-promotor(en): Erik Poelman. - Wageningen : Wageningen University - ISBN 9789462578647 - 254
    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 - brassica oleracea - verdedigingsmechanismen - glucosinolaten - insectenplagen - herbivorie - plutella xylostella - mamestra brassicae - pieris rapae - 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
    Wageningen University. Promotor(en): Marcel Dicke; Joop van Loon. - Wageningen : Wageningen University - ISBN 9789462577756 - 265
    016-3953 - arabidopsis thaliana - insect pests - herbivory - pest resistance - defence mechanisms - insect plant relations - molecular plant pathology - density - arabidopsis thaliana - 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
    Wageningen University. Promotor(en): Wim van der Putten, co-promotor(en): T.M. Bezemer; A. Biere. - Wageningen : Wageningen University - ISBN 9789462578142 - 174
    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
    Wageningen University. Promotor(en): Harro Bouwmeester; Marcel Dicke, co-promotor(en): Iris Kappers. - Wageningen : Wageningen University - ISBN 9789462576810 - 211
    cucumis sativus - cucumbers - induced resistance - plant pests - tetranychus urticae - mites - defence mechanisms - herbivore induced plant volatiles - herbivory - metabolomics - terpenoids - genomics - cucumis sativus - komkommers - geïnduceerde resistentie - plantenplagen - tetranychus urticae - 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
    Wageningen UR
    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
    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.

    Getting prepared for future attack : induction of plant defences by herbivore egg deposition and consequences for the insect community
    Pashalidou, F.G. - \ 2015
    Wageningen 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 - brassica - pieris brassicae - 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.
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