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

Abstract

Summary 1.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. 2. 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. 3. 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. 4. 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. 5. 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%. 6. 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. 7. The significance of these findings is discussed in the context of current hypotheses of aboveground × below-ground herbivore interactions. In particular, examining specific plant nutrients could be critical to understanding conditional outcomes of insect × plant interactions.

Facilitation and inhibition: changes in plant nitrogen and secondary metabolites mediate interactions between above-ground and below-ground herbivores

“…In cotton, root-feeding wireworms decreased foliar caterpillar performance by increasing foliar terpenoid levels, but caterpillars had no effect on wireworm performance [16]. In barley, root-feeding wireworms increased foliar aphid reproduction by increasing essential amino acids in leaves, but aphids increased wireworm mass by increasing root mineral content [13]. To date, however, there is no general framework to illustrate how herbivore-induced changes in plant primary and secondary metabolites impact aboveground and below-ground herbivore interactions.…”

“…For example, tannins are considered especially important in defence against specialist insects as digestibility-reducing compounds [9,10]. Damage by above-ground and/or below-ground herbivores may affect the levels of primary and secondary metabolites in plants, and changes in these chemicals can mediate the interactions of above-ground and below-ground herbivores [11][12][13][14][15]. For instance, Kaplan et al [11] found in tobacco that root-feeding nematodes increased the performance of folivorous caterpillars by blocking synthesis of alkaloids that are transported to leaves, but caterpillars increased nematode performance by increasing nitrogen transport to roots.…”

Characterization of Volatile Organic Compounds Emitted by Barley (Hordeum vulgare L.) Roots and Their Attractiveness to Wireworms

“…aboveground plant insect interactions (Effmert et al 2012;Johnson et al 2009;Soler et al 2012;Wenke et al 2010); however, the belowground VOCs potentially responsible for such interactions have to date been partially neglected, due to technical limitations. The release of root VOCs can mediate various interactions: direct or indirect defense of roots against herbivores (Ali et al 2011;Rasmann et al 2005Rasmann et al , 2012a, plant -plant competition (Ens et al 2009;Jassbi et al 2010;Viles and Reese 1996), resistance of roots against pathogens (Cobb et al 1968;Kalemba et al 2002;Vilela et al 2009), and symbiotic interactions (Asensio et al 2012;Paavolainen et al 1998).…”

“…Larvae of Agriotes are polyphagous wireworms that feed on the roots of a variety of crops, including cereals (Johnson et al 2009;van Herk and Vernon 2013). Baits based on germinating wheat and barley seeds have been proven to be efficient (Parker 1996).…”

Arriving at the right time : a temporal perspective on above-belowground herbivore interactions

“…The deficiency of water could in turn lead to the elevation of concentrations of amino acids and carbohydrates in the foliage and ultimately enhance performance of foliar aphids. However, a later study reported higher aphid performance in foliage of root-damaged plants but without any increase of soluble N in root herbivore-damaged plants (Johnson et al 2009). The failure of several studies linking aphid performance to water or nutrient stress of the host plant has further challenged this hypothesis (Koricheva et al 1998;Huberty and Denno 2004).…”