Interactions between above‐ and belowground insect herbivores as mediated by the plant defense system

Abstract

Plants are frequently attacked by both above‐ and belowground arthropod herbivores. Nevertheless, studies rarely consider root and shoot herbivory in conjunction. Here we provide evidence that the root‐feeding insect Agriotes lineatus reduces the performance of the foliage feeding insect Spodoptera exigua on cotton plants. In a bioassay, S. exigua larvae were allowed to feed on either undamaged plants, or on plants that had previously been exposed to root herbivory, foliar herbivory, or a combination of both. Previous root herbivory reduced the relative growth rates as well as the food consumption of S. exigua by more than 50% in comparison to larvae feeding on the undamaged controls. We found no effects in the opposite direction, as aboveground herbivory by S. exigua did not affect the relative growth rates of root‐feeding A. lineatus. Remarkably, neither did the treatment with foliar herbivory affect the food consumption and relative growth rate of S. exigua in the bioassay. However, this treatment did result in a significant change in the distribution of S. exigua feeding. Plants that had been pre‐exposed to foliar herbivory suffered significantly less damage on their young terminal leaves. While plant growth and foliar nitrogen levels were not affected by any of the treatments, we did find significant differences between treatments with respect to the level and distribution of plant defensive chemicals (terpenoids). Exposure to root herbivores resulted in an increase in terpenoid levels in both roots as well as in mature and immature foliage. Foliar damage, on the other hand, resulted in high terpenoid levels in young, terminal leaves only. Our results show that root‐feeding herbivores may change the level and distribution of plant defenses aboveground. Our data suggest that the reported interactions between below‐ and aboveground insect herbivores are mediated by induced changes in plant secondary chemistry.

Intraspecific Variation in Plant Defense Alters Effects of Root Herbivores on Leaf Chemistry and Aboveground Herbivore Damage

“…Induction of secondary metabolites in roots due to root feeding by insect larvae has been reported for a number of plant and herbivore combinations (Birch et al 1992;Bezemer et al 2003Bezemer et al , 2004Borowicz et al 2003;Van Dam and Raaijmakers 2006) and might be a general plant response similar to aboveground induction due to shoot herbivores (Karban and Baldwin 1997). Irrespective of plant line, wireworms had no significant effect on root biomass, but led to an increase in leaf biomass, pointing to compensatory shoot growth (Wurst and Van der Putten 2007).…”

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

“…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. 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].…”

Effects of Soil Organisms on Aboveground Plant-Insect Interactions in the Field: Patterns, Mechanisms and the Role of Methodology

“…It should be noted that other nematodes (e.g., fungal feeders, bacterial feeders) may, however, also indirectly affect plant-insect interactions by interacting with other soil organisms. Plantparasitic nematodes, by feeding on the roots of shared host plants, can influence the defense status and nutritional quality of host plants, potentially leading to effects on herbivores (Bezemer et al, 2003;Bezemer and van Dam, 2005;Wondafrash et al, 2013;Biere and Goverse, 2016). Results from laboratory studies of the effects of plant-parasitic nematodes on aboveground insects are often variable for chewing insects, but generally show negative effects on either the performance or preference of sap sucking insects (Johnson et al, 2012;Wondafrash et al, 2013).…”