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Linking Variation in Plant Defence to Biodiversity at Higher Trophic Levels: a Multidisciplinary Approach

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Linking Variation in Plant Defence to Biodiversity at Higher Trophic Levels: a Multidisciplinary Approach Linking variation in plant defence to biodiversity at higher trophic levels: a multidisciplinary approach Erik H. Poelman Promotoren: Prof. dr. Marcel Dicke Hoogleraar Entomologie Wageningen Universiteit Prof. dr. Louise E.M. Vet Hoogleraar Evolutionaire Ecologie Wageningen Universiteit Co-promotoren: Dr. ir. Joop J.A. van Loon Universitair hoofddocent Entomologie Wageningen Universiteit Dr. ir. Nicole M. van Dam Senior onderzoeker Nederlands Instituut voor Ecologie, Heteren Promotiecommissie: Prof. dr. Anne-Marie Cortesero University of Rennes, France Prof. dr. ir. Harro J. Bouwmeester Wageningen Universiteit Prof. dr. ir. Corné M.J. Pieterse Universiteit Utrecht Prof. dr. Jan M. van Groenendael Radboud Universiteit Nijmegen Dit onderzoek is uitgevoerd binnen de onderzoeksschool Experimental Plant Sciences. Erik H. Poelman Linking variation in plant defence to biodiversity at higher trophic levels: a multidisciplinary approach Proefschrift Ter verkrijging van de graad van doctor op gezag van de rector magnificus van Wageningen Universiteit Prof. dr. M. J. Kropff in het openbaar te verdedigen op woensdag 1 oktober 2008 des namiddags te vier uur in de Aula Erik H. Poelman (2008) Linking variation in plant defence to biodiversity at higher trophic levels: a multidisciplinary approach PhD-thesis, Wageningen University - with references - with summary in Dutch ISBN 978-90-8504-962-3 Abstract Central issue in ecology are to identify the driving forces behind community diversity and the ways in which this biodiversity is maintained. Plant-insect associations form a signifi- cant part of the earth‟s biodiversity and are widely studied for their reciprocal interactions. The aim of this thesis was to identify the role of intraspecific variation in plant traits in affecting the diversity and composition of the plant-associated insect community. Cultivars of White Cabbage, Brassica oleracea, that differ in a set of defensive traits were used as a model system in conjunction with their insect community. The system was studied using a multidisciplinary approach that included targeted gene expression and chemical analyses of plant responses to insects as well as an ecological approach on the effect of plant defen- sive characteristics on insect communities. This project includes laboratory and field ex- periments. The investigated B. oleracea cultivars differed widely in resistance to herbivorous insects, although the concentration of glucosinolates, secondary metabolites characteristic for Brassicaceae, did not correlate with cultivar resistance to herbivores. Herbivore- susceptible cultivars harboured higher abundance and diversity of herbivores compared to herbivore-resistant cultivars in the field. Both specialist and generalist herbivores of differ- ent feeding guilds covaried in higher abundance on herbivore-susceptible cultivars that characteristically had low concentrations of glucosinolates with a shorter side chain in their molecule structure. Induction of the B. oleracea cultivars by Pieris rapae herbivory resulted in differ- ential induction of chemical plant defences such as indolyl-glucosinolates and volatile or- ganic compounds such as methyl salicylate. The different composition of the volatile blend emitted by the cultivars resulted in differential attraction of parasitoids to cultivars in an olfactometer assay. Cultivars showing higher attraction in this assay harboured a higher proportion of parasitized caterpillars in the field. The differences in indirect resistance among accessions had a two-fold effect on abundance and diversity of hyperparasitoids that parasitize on cocoons of the primary parasitoids. First, the larger number of cocoons sustained a larger number of hyperparasitoids and second the hyperparasitoids were also attracted to the plant accession that was most attractive to primary parasitoids. The full set of P. rapae-induced plant responses also affected the herbivore community. Plants that were previously damaged by P. rapae had different gene transcription responses to secon- dary herbivory than when these herbivore species were feeding as primary herbivore on a plant. The subsequently feeding herbivore species were all impeded in their performance, but had contrasting host plant preference for induced plants. Generalist herbivores avoided plants that were previously damaged by P. rapae, whereas specialist herbivores preferred induced plants. Thereby, early-season herbivory by P. rapae resulted in higher herbivore abundance and species richness compared to plants that had not experienced early-season herbivory in the field. Plant responses to early-season herbivory resulted in induced resis- tance to generalists, but in induced susceptibility to specialist herbivores of different feed- ing guilds. In conclusion, the set of constitutive as well as inducible direct and indirect defensive traits of a plant affects the composition of the plant-associated insect community. The insect community as a whole should, therefore, be considered in studies of reciprocal selection between insects and defensive traits of plants. Abstract 7 Chapter 1 General introduction: Consequences of variation in plant defence for biodiversity at higher trophic levels 11 Chapter 2 Performance of specialist and generalist herbivores feeding on cabbage cultivars is not explained by glucosinolate profiles 25 Chapter 3 Chemical diversity in Brassica oleracea affects biodiversity of insect herbivores 39 Chapter 4 Laboratory assays on differential attraction of Cotesia parasitoids by cultivars of Brassica oleracea reliably predict 59 parasitism rates in the field Chapter 5 Plant variation in herbivore-induced volatiles affects hyperparasitoid attraction and hyperparasitoid community 79 composition Chapter 6 Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their 93 abundance in the field Chapter 7 Community-wide effects of induced plant responses: a trade-off between induced resistance to generalist and susceptibility to 111 specialist herbivores Chapter 8 General discussion 125 References 135 Summary 151 Samenvatting 155 Dankwoord 159 Curriculum vitae 161 Publications 163 Chapter 1 Chapter Consequences of variation in plant defence for biodiversity at higher trophic levels Erik H. Poelman, Joop J.A. van Loon & Marcel Dicke In press in: Trends in Plant Science Chapter 1 Abstract Plants are the basic food resource of complex communities. The organisms forming these communities in turn exert selection pressures on plant traits. Antagonistic spe- cies such as insect herbivores impose selection on plants to defend themselves against these attackers. Although selection on plant defence traits has typically been studied for pairwise plant-attacker interactions, other community members are unavoidably affected by these traits as well. A plant trait may e.g. affect parasitoids and predators feeding on the herbivore or other herbivores may be affected through induced changes in plant defence. Consequently, defensive plant traits structure the diversity and composition of the community associated with the plant and communities as a whole also feed back to selection on plant traits. Here, we review recent develop- ments in the understanding of plant defence traits structuring insect communities and discuss how molecular mechanisms may drive community-wide effects. Key words: plant defence, induced response, indirect defence, biodiversity 12 General introduction Chapter 1 Plant traits and biodiversity Central issues in ecology are to identify the driving forces behind community diversity Glossary and the ways in which this biodiversity is maintained. The ca. 300,000 different spe- Biodiversity: The number of species and cies of plants and 3 to 6 million species of their individual abundance in a given insects, half of which are herbivorous, are a environment significant part of the Earth‟s total recorded Constitutive plant defence: defence of a biodiversity. Among the most common in- plant that is expressed independent of teractions occurring in ecosystems are plant- attack insect interactions. Studies of plant-insect associations have played an important role Community: the assembly of species in in understanding ecological and evolution- a particular area ary processes that underlie community bio- diversity (Whitham et al. 2006). Community-wide effect: an effect on Recent studies have provided ample many individual species constituting a information on the molecular basis and community ecology of plant defences against insects Induced plant defence: the set of and pathogens. Constitutive defences of changes in a plant in response to an at- plants differentially affect various insect tack that impedes on plant fitness, which herbivores. These defences not only affect results in a reduced plant fitness loss the performance of an attacker but may also inflicted by the attacking organism influence the behaviour of the attacker, for example its host-plant selection behaviour Induced plant response: the set of (Schoonhoven et al. 2005). Upon damage changes, such as morphological and by pathogens or herbivores, plants also re- phytochemical, in a plant in response to an abiotic or biotic event impacting on spond to their attacker (Schaller 2008). In- the plant duced defence is observed as alterations in a set of traits that lead to a reduced effect of Trophic cascade: an organism at one the attacker on plant fitness. Many of these level of the food chain influences the induced plant defences
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