An Apparent Trade-Off between Direct and Signal-Based Induced Indirect Defence against Herbivores in Willow Trees

Kinuyo Yoneya,Masayoshi Uefune,Junji Takabayashi,Jane Catherine Stout

doi:10.1371/journal.pone.0051505

Abstract

Signal-based induced indirect defence refers to herbivore-induced production of plant volatiles that attract carnivorous natural enemies of herbivores. Relationships between direct and indirect defence strategies were studied using tritrophic systems consisting of six sympatric willow species, willow leaf beetles (Plagiodera versicolora), and their natural predators, ladybeetles (Aiolocaria hexaspilota). Relative preferences of ladybeetles for prey-infested willow plant volatiles, indicating levels of signal-based induced indirect defence, were positively correlated with the vulnerability of willow species to leaf beetles, assigned as relative levels of direct defence. This correlation suggested a possible trade-off among the species, in terms of resource limitation between direct defence and signal-based induced indirect defence. However, analyses of volatiles from infested and uninfested plants showed that the specificity of infested volatile blends (an important factor determining the costs of signal-based induced indirect defence) did not affect the attractiveness of infested plant volatiles. Thus, the suggested trade-off in resource limitation was unlikely. Rather, principal coordinates analysis showed that this ‘apparent trade-off’ between direct and signal-based induced indirect defence was partially explained by differential preferences of ladybeetles to infested plant volatiles of the six willow species. We also showed that relative preferences of ladybeetles for prey-infested willow plant volatiles were positively correlated with oviposition preferences of leaf beetles and with the distributions of leaf beetles in the field. These correlations suggest that ladybeetles use the specificity of infested willow plant volatiles to find suitable prey patches.

Highlights

Besides the well-known direct defence mechanisms of plants against herbivores, many plants defend themselves indirectly by increasing the effectiveness of carnivorous natural enemies of these herbivores [1,2]
The leaf areas damaged by leaf beetle larvae in six willow species, which were considered to reflect relative levels of direct defence, were positively correlated with the relative preference of ladybeetles for infested willow leaf volatiles, which were considered an indicator of relative levels of signal-based induced indirect defence
These parameters were not correlated with the relative preferences of ladybeetles for uninfested willow leaf volatiles, which were considered to reflect relative levels of constitutive indirect defence

Summary

Introduction

Besides the well-known direct defence mechanisms of plants against herbivores, many plants defend themselves indirectly by increasing the effectiveness of carnivorous natural enemies of these herbivores [1,2]. It is important to note that, in this kind of defence, the plants themselves do not produce a specific reward for the carnivores. Rather, it is the herbivores on a plant that are the rewards to the attracted carnivores. Important factors for the carnivores taking part in a signal-based induced indirect defence response are whether the number and species of herbivores on the plant constitute a sufficient reward. The goal of direct defence is to minimize the number of herbivores, while signal-based indirect defence aims to maintain a sufficient number of herbivores to reward the carnivores. It is evident that there is a conflict between direct defence and signal-based induced indirect defence in terms of the number of herbivores

Methods

Results

Conclusion