Reappraising the role of plant nutrients as mediators of interactions between root- and foliar-feeding insects

Scott N. Johnson, Cathy Hawes, Alison J. Karley

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    Abstract

    There is increasing evidence that many above-ground and below-ground processes are tightly linked through plant-mediated mechanisms, including indirect interactions between foliar and root herbivores underpinned by changes in host plant chemistry (e.g. defensive or nutritional status). To date, studies addressing interactions involving nutritional mechanisms have relied on rudimentary chemical measurements (e.g. total/soluble nitrogen), overlooking other nutrients such as minerals and specific amino acids. This study investigated how the nutrient composition of barley (Hordeum vulgare) responded to separate and simultaneous attack by root-feeding wireworms (Agriotes spp.) and foliar-feeding aphids (Rhopalosiphum padi) after short and long exposures to herbivory, and determined whether the two insects indirectly interacted with each other. Wireworms significantly reduced total plant mass and leaf dry mass by up to 25%, but had little impact on nutritional chemistry compared with aphids. Aphids did not affect plant growth but caused significant reductions in most leaf minerals: nitrogen (N), sulphur (S), calcium (Ca) and phosphorus (P). In contrast, aphids increased root mineral concentrations: N, S, Ca and potassium (K). Aphid-induced changes occurred in both short and long exposure experiments, with the exception of leaf Ca, and root N and K which were only significantly affected in the short exposure experiment. Above-ground and below-ground herbivory had several interactive (often reversible) effects on plant nutrients. For example, wireworms strengthened the aphid-driven increases in root S by 35% after short exposure, but reduced aphid-induced increases by 10% after longer exposure. There was evidence for positive bi-directional interactions between above-ground and below-ground herbivores, with wireworms promoting aphid numbers by 30% and aphids increasing wireworm mass by 25%. Contrary to previous mechanistic explanations, below-ground herbivory had little impact on foliar amino acid concentrations, whereas aphids caused significant (approximately 50%) reductions in essential amino acids. However, after longer exposure to wireworm herbivory, aphid-driven reductions in essential amino acids were attenuated. Aphids caused significant increases in root mineral concentrations (especially root S) which potentially promoted wireworm performance. The significance of these findings is discussed in the context of current hypotheses of above-ground × below-ground herbivore interactions. In particular, examining specific plant nutrients could be critical to understanding conditional outcomes of insect × plant interactions.
    Original languageEnglish
    Number of pages8
    JournalFunctional Ecology
    Publication statusPublished - 2009

    Keywords

    • above and below ground
    • aphids
    • barley
    • foliar amino acids
    • mineral nutrients
    • wireworm

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