Abstract
Summary Herbivore communities are shaped by indirect plant‐mediated interactions whose outcomes are strongly dependent on the sequence of herbivore arrival. However, the mechanisms underlying sequence specificity are poorly understood.We examined the mechanisms that govern sequence‐specific effects of the interaction between two specialist maize herbivores, the leaf feeder Spodoptera frugiperda and the root feeder Diabrotica virgifera virgifera. In the field, S. frugiperda reduces D. v. virgifera abundance, but only when it arrives on the plant first.In behavioral experiments, D. v. virgifera larvae continued feeding on plants that they had infested before leaf infestation, but refused to initiate feeding on plants that were infested by S. frugiperda before their arrival. Changes in root‐emitted volatiles were sufficient to elicit this sequence‐specific behavior. Root volatile and headspace mixing experiments showed that early‐arriving D. v. virgifera larvae suppressed S. frugiperda‐induced volatile repellents, which led to the maintenance of host attractiveness to D. v. virgifera.Our study provides a physiological and behavioral mechanism for sequence specificity in plant‐mediated interactions and suggests that physiological canalization of behaviorally active metabolites can drive sequence specificity and result in strongly diverging herbivore distribution patterns.
Highlights
Interspecific competition influences the structure, function and stability of natural and agricultural ecosystems (Loreau & de Mazancourt, 2013)
A growing number of studies show that plant-mediated, indirect effects are the most common form of interspecific competition between herbivores (Ohgushi, 2005; Kaplan & Denno, 2007; Xiao et al, 2012; Huang et al, 2013) and that they act as driving forces of herbivore community composition in nature (Kaplan & Denno, 2007; Poelman & Dicke, 2014; Stam et al, 2014)
D. v. virgifera decreases the performance of leaf-feeders on maize under water limiting conditions, which may lead to plant-mediated feedback loops (Erb et al, 2009; Erb et al, 2011b), we found no correlation between the amount of S. frugiperda leaf-damage and the reduction of D. v. virgifera performance in our previous work (Erb et al, 2011a)
Summary
Interspecific competition influences the structure, function and stability of natural and agricultural ecosystems (Loreau & de Mazancourt, 2013). Interspecific competition can occur through direct interference or through plant-mediated, indirect effects (Denno et al, 1995). A growing number of studies show that plant-mediated, indirect effects are the most common form of interspecific competition between herbivores (Ohgushi, 2005; Kaplan & Denno, 2007; Xiao et al., 2012; Huang et al, 2013) and that they act as driving forces of herbivore community composition in nature (Kaplan & Denno, 2007; Poelman & Dicke, 2014; Stam et al., 2014). A recent meta-analysis on interactions between leaf and root feeding herbivores identified the sequence of arrival as a strong predictor for the directionality of effects for this type of plant-mediated interactions (Johnson et al., 2012)
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