Soil legacy effects on aboveground plant-insect interactions

R. Heinen

Onderzoeksoutput: PhD Thesis (Proefschrift)PhD thesis (Proefschrift)

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Soils are highly diverse environments that contain many organisms that interact with the plants that grow in the soil. These organisms can have effects on plants that range from beneficial (e.g., mutualists) to detrimental (e.g., pathogens). Furthermore, a large group of organisms does not directly interact with plants, but are still essential parts of the soil, by breaking down organic matter and making nutrients available to the plant. In recent decades, it has also become very clear that soil organisms can affect organisms that interact with the plant aboveground. The field of above-belowground interactions has since become well-studied for many individual groups of soil taxa and aboveground insects. The implications of entire soil communities for aboveground plant-insect interactions has only recently received more attention.
Plants also have a strong effect on the organisms around their roots. Via the exudation of carbon and other compounds from their roots, they may repel some organisms and attract others. As a result, the soil microbiome often reveals plant species-specific patterns. These patterns in soil communities may persist in the soil for a long time, as soil legacies. It has been shown that these specific soil legacies can alter the growth of plants that grow later in the same soil (a process better known as plant-soil feedback). Pioneering work published before this PhD thesis, revealed that the effects of entire soil communities, in the form of plant-specific soil legacies, can also have strong effects on chewing and phloem-feeding insect herbivores.
In this thesis, we set out to explore how general these soil legacy effects occur in a broad range of plant species and a common polyphagous chewing herbivore, the cabbage moth (Mamestra brassicae). Furthermore, I assessed whether these species-specific legacy effects on plant-insect interactions could be predicted using plant growth rate (fast/slow) and plant functional type (grass/forb). Using twelve plants consisting of combinations of fast- and slow-growing grasses and forbs, I created soils with different legacies and grew all twelve plant species on all these soils, either individually (Chapter 3), or in communities (Chapter 4). In the response phase, cabbage moth caterpillars were introduced, after which I measured their growth and leaf consumption, as well as individual plant biomass responses. These two experiments revealed that soil legacy effects on plant-insect interactions are common in individual plants, as well as in plant communities, and can, in part, be explained by plant functional type and interactions between plant functional type and plant growth rate.
Most previous above-belowground research has focused on mechanisms that are mediated via the shared host plant. In Chapter 5, we investigated whether soil legacy effects could alter herbivore-induced plant defenses in a focal plant species, Plantago lanceolata. Here, it was shown that levels of secondary metabolites (iridoid glycosides) can differ considerably between soils. Furthermore, using gene expression assays of marker genes for the jasmonic acid and salicylic acid pathways - two important herbivore-induced phytohormonal defense pathways – we show that the ability of a plant to defend itself against aboveground herbivory, depends largely on the legacy present in the soils it grows in.
Lastly, in Chapter 6, the role of the biotic component of the soil legacy itself, in aboveground plant-insect interactions, was studied. Previous work indicates that subsets of the soil microbiome can end up in the shoot microbiome. Through consumption, these microbes could end up in the insect herbivore gut. Indeed, some of the caterpillar microbiome was ingested via its diet, although this turned out to be a rather minimal source of microbes. Interestingly, caterpillars appeared to take up the majority of their microbiome from soil. Through this direct but previously overlooked pathway, soil legacy effects may play an important role in influencing aboveground insects.
In conclusion, I have shown in this thesis that soil communities can play an important role in mediating aboveground plant-insect interactions. Soil matters! Now, there are plenty of ways that soils may build up microbial legacy effects. Plant-specific legacies are just the beginning. Future studies should unravel how other legacy effects (e.g., agricultural land use, urbanization, biodiversity, historical abiotic differences or biogeographical differences) may affect plant-insect interactions consequently.
Originele taal-2Engels
KwalificatieDoctor (dr.)
Toekennende instantie
  • Leiden University
  • Bezemer, T. Martijn, Promotor
  • Biere, Arjen, Co-promotor
  • Harvey, Jeff A., Co-promotor
Datum van toekenning04 dec 2019
Gedrukte ISBN's978-94-6332-578-3
StatusGepubliceerd - 14 okt 2019

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