Plant-mediated multitrophic interactions between aboveground and belowground insects

R. Soler Gamborena

Research output: Thesisinternal PhD, WU


Herbivory can induce changes in plant growth, physiology, morphology, and phenology. Such herbivore-induced changes by insects are commonly observed in many plant species. Changes in the host plant can alter interaction linkages between plants, herbivores and higher trophic levels such as carnivores of the herbivores. These interaction linkages shape community organization and biodiversity in plant-based terrestrial communities. Considering that plants have both aboveground and belowground parts, systemic herbivore-induced changes within the plant could potentially link spatially separated herbivores associated with plants in the soil and in the aboveground (sub) system. Relatively recently, an increasing number of studies have shown that root herbivores, among other soil dwelling organisms, can indeed interact with foliar herbivores. Root herbivores change the quality and biomass of aboveground plant parts, which in turn influences the growth, development and survival of foliar herbivores. Similarly, foliar-feeding insects have been shown to influence root-feeding insects. This thesis explores whether, and mechanistically how, these feed-backs between root and foliar herbivores are transmitted through the soil and the aboveground food chains influencing the performance and behaviour of higher trophic levels. In Chapter 1, I introduce plant-insect interactions in a multitrophic context, briefly describing how the plant mediates these intricate interactions, and I describe the general aim and the outline of the thesis. In Chapter 2 I study the effects of root herbivores, at different densities, on the biomass and quality of the plant shoot, and on the performance of a foliar herbivore, its primary parasitoid and its secondary parasitoid (hyperparasitoid) sharing the host plant. In Chapter 3 I study the reverse effect; the effects of foliar herbivores on a root herbivore and its parasitoid mediated by the host plant. The results of these Chapters show that the spatially separated herbivores negatively affect each other's performances by increasing the levels of secondary plant compounds within the host plant. These     negative effects are not restricted to the herbivore level, but are transmitted to the parasitoids and the hyperparasitoids, reducing in particular the growth and size of the off-spring of the aboveground parasitoid. Based on the results of Chapter 2, where I observed a marked suboptimal performance of the off-spring of the aboveground parasitoid when sharing the host plant with root herbivores, I investigate in Chapter 4 whether female parasitoids of foliar herbivores can exploit root herbivore-related cues to select the most suitable hosts for their offspring. In this Chapter I show that female parasitoids avoid to parasitise hosts feeding on plants shared with root herbivores, when hosts feeding on root-undamaged plants are available. The mechanism points to changes in the volatile blend of the plant triggered by the root-feeding insects. After observing this strong interaction between root herbivores and aboveground parasitoids mediated by the host-infested plant, in Chapter 5, I investigate whether root herbivores influence the behaviour of female parasitoids also indirectly via changes in the surrounding habitat. I provide evidence that root-feeding insects can influence the behaviour and foraging efficiency of parasitoids of foliar herbivores, even when the foliar (parasitoid-host) and the root herbivores do not feed on the same plant, but on neighbouring conspecific plants within the same habitat. The above described results are based on experiments carried out under controlled conditions in the laboratory or semi-field experiments in large, enclosed cages. To test some of the lab-based results under more natural conditions, I conducted a field experiment in which several cohorts of mustard plants with and without root herbivores were placed in the field and were monitored aboveground for the presence of foliar herbivores over the course of a summer season. To investigate whether the spatial distribution of root-damaged plants influences the plant preference of the foliar-feeders, I arranged the plants in the field in plots either in clusters of root-undamaged and root-damaged plants, or root-undamaged and root-damaged plants homogeneously mixed. Specialised foliar herbivores were observed feeding and ovipositing preferentially on root- ____________________________________________________________ Summary uninfested plants over plants shared with root herbivores. Interestingly, one of the species only discriminates against root-damaged plants when the plants were grouped in clusters. This thesis shows that the strong feedbacks between root and shoot associated organisms can significantly influence the performance and behaviour of organisms of higher trophic levels. Therefore, interactive effects of aboveground and belowground organisms cannot be limited to organisms directly associated with the shared host plant because they occur throughout a complex multitrophic chain of organisms. Furthermore, this thesis underlines the importance of considering not only the mere presence or absence of the soil dwelling organisms, but show that the density and distribution of root herbivores can determine the outcome of the interactions with their aboveground counterparts. These interactions are mediated by the shared host plant, via induced changes in the secondary plant compounds within the plant and in the plant volatile blend. Consumers in one compartment can change the quality of the plant in the opposite compartment, as well as induce changes in the emission of the plant volatiles used by carnivores that forage for hosts. Moreover, I provide evidence that spatially separated insects can interact not only via changes in the shared host plant, but also more indirectly via changes in the quality of the surrounding habitat. This suggest that aboveground-belowground multitrophic interactions can occur and interact in much more complex ways than what has been reported so far. In the last experimental Chapter I provide evidence that behavioural decisions in naturally occurring populations of foliar-feeding insects can also be influenced by root-feeding insects, under field conditions where several complex interactions take place simultaneously. In the final Chapter, I summarise the results presented in this thesis and provide a general conclusion of the work. I identify a number of important areas and topics for future research to further gain insight into aboveground-belowground multitrophic interactions.
Original languageEnglish
QualificationDoctor of Philosophy
Awarding Institution
  • Wageningen University
  • Vet, Louise, Promotor
  • van der Putten, Wim, Promotor
  • Harvey, J.A., Co-promotor, External person
  • Bezemer, T.M., Co-promotor
Award date30 Oct 2007
Place of Publication[S.l.]
Print ISBNs9789085047384
Publication statusPublished - 2007


  • plants
  • insects
  • soil insects
  • herbivores
  • trophic levels
  • insect plant relations
  • multitrophic interactions
  • plant-herbivore interactions

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