Sequence of arrival determines plant‐mediated interactions between herbivores

Abstract

Summary1. Induced changes in plant quality can mediate indirect interactions between herbivores. Although the sequence of attack by different herbivores has been shown to influence plant responses, little is known about how this affects the herbivores themselves. 2. We therefore investigated how induction by the leaf herbivore Spodoptera frugiperda influences resistance of teosinte (Zea mays mexicana) and cultivated maize (Zea mays mays) against rootfeeding larvae of Diabrotica virgifera virgifera. The importance of the sequence of arrival was tested in the field and laboratory. 3. Spodoptera frugiperda infestation had a significant negative effect on colonization by D. virgifera larvae in the field and weight gain in the laboratory, but only when S. frugiperda arrived on the plant before the root herbivore. When S. frugiperda arrived after the root herbivore had established, no negative effects on larval performance were detected. Yet, adult emergence of D. virgifera was reduced even when the root feeder had established first, indicating that the negative effects were not entirely absent in this treatment. 4. The defoliation of the plants was not a decisive factor for the negative effects on root herbivore development, as both minor and major leaf damage resulted in an increase in root resistance and the extent of biomass removal was not correlated with root-herbivore growth. We propose that leaf-herbivore-induced increases in feeding-deterrent and ⁄ or toxic secondary metabolites may account for the sequence-specific reduction in root-herbivore performance. 5. Synthesis. Our results demonstrate that the sequence of arrival can be an important determinant of plant-mediated interactions between insect herbivores in both wild and cultivated plants. Arriving early on a plant may be an important strategy of insects to avoid competition with other herbivores. To fully understand plant-mediated interactions between insect herbivores, the sequence of arrival should be taken into account.

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

“…As soil communities are dynamic and species-specific soil communities accumulate over time (Diez et al, 2010;Flory and Clay, 2013;Van der Putten et al, 2013;Heinen et al, 2018), it is likely that these temporal dynamics will strongly influence the performance of aboveground insect communities over time. Various controlled studies have shown that the sequence of arrival of aboveground and belowground herbivores on the plant can greatly alter the outcome of soil biota-plant-insect interactions (e.g., Erb et al, 2011;Wang et al, 2014) and to some extent, this has also been shown in field studies (e.g., Gange et al, 2005a), although the link between temporally changing soil communities and temporal variation in aboveground insect communities has not been made. In the field, insect communities also change throughout the season.…”

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

“…For systems with differing aboveground and below-ground herbivore species, their interactions may be affected by the sequence of herbivory, herbivore types and host plant species [2]. For instance, Erb et al [42] found in maize that noctuid moth feeding had a significant negative effect on colonization by a root-feeding beetle, but only when above-ground herbivores attacked the plant first. Most previous studies used different above-ground and belowground herbivore species, while tests on herbivore species that have both above-ground and below-ground life stages are rare [43].…”

Plant diversity effects on insect herbivores and their natural enemies: current thinking, recent findings, and future directions

“…For instance, damage caused by one herbivore species may induce plant chemical defences which in turn influence attack by another herbivore guild [43] as well as arthropod community structure [44]. Such effects are particularly common in systems where early-season herbivores triggers plant induced responses that affect late-season herbivores [45,46]. Surprisingly, however, this area of research has developed independently of plant diversity studies, despite the fact that diversity effects on herbivory would be expected to influence plant induced responses and thus potentially lead to plant-mediated interactions among herbivores.…”