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This thesis explores whether aphid-infestation interferes with the plant response to chewing herbivores and whether this impacts performance and behaviour of individual chewing insect herbivores and their natural enemies, as well as the entire insect community. I investigated this using three wild cabbage populations (Brassica oleracea) that are known to differ in inducible secondary chemistry, to reveal whether patterns were consistent.
A literature review on recent developments in the field of plant interactions with multiple herbivores (Chapter 2) addressed how plant traits mediate interactions with various species of the associated insect community and their dynamics. In addition, the mechanisms underlying phenotypic changes in response to different herbivores were discussed from the expression of defence-related genes, phytohormones and secondary metabolites in plants to their effects on the performance and behaviour of individual insects as well as the entire insect community. In Chapter 3, I investigated the effects of early-season infestation by the aphid Brevicoryne brassicae on the composition and dynamics of the entire insect community throughout the season in a garden experiment replicated in two consecutive years. Aphid infestation in the early season only affected a subset of the community, i.e. the natural enemies of aphids, but not the chewing herbivores and their natural enemies. Moreover, the effects were only significant in the first half (June & July), but waned in the second half of the season (August & September). The effect of aphid infestation on the community of natural enemies also varied among the cabbage populations. Chapter 4 investigated the effects of aphid infestation on plant direct defences against chewing herbivores in laboratory experiments by comparing the performance of chewing herbivores and their parasitoids on aphid-infested and aphid-free plants. The performance of the specialist herbivore Plutella xylostella and its parasitoid Diadegma semiclausum was better on plants infested with aphids than on aphid-free plants, whereas the performance of the generalist herbivore Mamestra brassicae and its parasitoid Microplitis mediator was not affected by aphid infestation. These results suggest that aphid induced changes in plant traits may differentially affect the performance of leaf-chewing herbivore species attacking the same host plant, and also varied among the cabbage populations. Chapter 5 examined the effects of B. brassicae aphid infestation on plant indirect defences against chewing herbivores. In a two-choice olfactometer bioassay, preference behaviour for volatiles emitted by plants infested with hosts alone and those emitted by plants infested with aphids and hosts was compared for D. semiclausum and M mediator, larval endoparasitoids of caterpillars of P. xylostella and M. brassicae, respectively. In addition, the headspace volatiles emitted by host-infested and dually-infested plants were collected and analyzed. Co-infestation with aphids differentially affected volatile-mediated foraging behaviour of the two parasitoid species in an infestation period-dependent manner. Diadegma semiclausum preferred dually infested plants over host-infested plants when aphids infested the plants for a short time period, i.e. 7 days, but the volatile preference of D. semiclausum was reversed when aphid infestation was extended to 14 days. In contrast, M. mediator consistently preferred volatiles emitted by the dually-infested plants over those emitted by host-infested plants. The patterns of preference behaviour of the two wasp species were consistent across the three cabbage populations. Interestingly, the emission rate of most volatile compounds was reduced in plants dually-infested with caterpillars and aphids compared to singly-infested with caterpillars. This study showed that aphid infestation increased plant indirect defences against caterpillars, but depended on the aphid infestation period and specific caterpillar-parasitoid association. We hypothesized a negative interference of aphid infestation on plant defences against chewing herbivores based on previously reported SA-JA antagonism. In Chapter 6, we assessed the activation of SA and JA signaling pathways in plants infested by both aphids (B. brassicae) and various caterpillar species (P. xylostella, M. brassicae and Pieris brassicae) in different time sequences by quantifying transcription levels of the SA- and JA-responsive marker genes, PR-1 and LOX respectively. The results did not provide support for SA-JA antagonism. Compared to single infestation with each of the herbivore species, dual infestation with aphid and caterpillars had no interactive effects on the transcription levels of the SA- and JA-responsive maker genes, regardless of the temporal sequence of aphid and caterpillar attack, or the identity of the attacking caterpillar species.
The findings of this thesis contribute to our understanding of plant responses to herbivory by insect species belonging to different feeding guilds and their ecological effects on other associated community members. Aphid infestation may interfere with plant direct and indirect defences against leaf-chewing herbivores at the individual species level, but the effects are species-specific and also depend on the infestation period of aphids. Early-season aphid infestation may further affect the composition of the insect community, but the effect is smaller influencing only a subset of the community compared to early infestation by chewing herbivores. The molecular mechanism underlying plant responses to both phloem-feeding and leaf-chewing herbivores are complex and require the investigation of a range of genes involved in JA- and SA-mediated defence signal transduction. Plant interact with multiple herbivores at different levels of biological organization ranging from the subcellular level to the individual and the community level, and an integrated multidisciplinary approach is required to investigate plant-insect interactions.
|Qualification||Doctor of Philosophy|
|Award date||1 Sep 2016|
|Place of Publication||Wageningen|
|Publication status||Published - 2016|
- brassica oleracea
- brevicoryne brassicae
- insect pests
- pest resistance
- defence mechanisms
- insect plant relations
- natural enemies
- herbivore induced plant volatiles
- plant-herbivore interactions
- genetic variation
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