Herbivore-specific, density-dependent induction of plant volatiles: honest or "cry wolf" signals?

Andy Hector,Kaori Shiojiri,Masayoshi Uefune,Michiel Van Wijk,Maurice W Sabelis,Soichi Kugimiya,Rika Ozawa,Junji Takabayashi

doi:10.1371/journal.pone.0012161

Andy Hector, Kaori Shiojiri + Show 6 more

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https://doi.org/10.1371/journal.pone.0012161

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Abstract

Plants release volatile chemicals upon attack by herbivorous arthropods. They do so commonly in a dose-dependent manner: the more herbivores, the more volatiles released. The volatiles attract predatory arthropods and the amount determines the probability of predator response. We show that seedlings of a cabbage variety (Brassica oleracea var. capitata, cv Shikidori) also show such a response to the density of cabbage white (Pieris rapae) larvae and attract more (naive) parasitoids (Cotesia glomerata) when there are more herbivores on the plant. However, when attacked by diamondback moth (Plutella xylostella) larvae, seedlings of the same variety (cv Shikidori) release volatiles, the total amount of which is high and constant and thus independent of caterpillar density, and naive parasitoids (Cotesia vestalis) of diamondback moth larvae fail to discriminate herbivore-rich from herbivore-poor plants. In contrast, seedlings of another cabbage variety of B. oleracea (var. acephala: kale) respond in a dose-dependent manner to the density of diamondback moth larvae and attract more parasitoids when there are more herbivores. Assuming these responses of the cabbage cultivars reflect behaviour of at least some genotypes of wild plants, we provide arguments why the behaviour of kale (B. oleracea var acephala) is best interpreted as an honest signaling strategy and that of cabbage cv Shikidori (B. oleracea var capitata) as a “cry wolf” signaling strategy, implying a conflict of interest between the plant and the enemies of its herbivores: the plant profits from being visited by the herbivore's enemies, but the latter would be better off by visiting other plants with more herbivores. If so, evolutionary theory on alarm signaling predicts consequences of major interest to students of plant protection, tritrophic systems and communication alike.

Highlights

Plants release specific blends of volatile chemicals in response to insect herbivory, thereby attracting the herbivore’s enemies [1,2,3]
C. vestalis did not or could not determine whether cabbage plants harbour few or many diamondback moths (DBM) larvae, whereas C. glomerata preferred cabbage plants with more cabbage white butterflies (CWB) larvae. To test whether the latter phenomenon was unique for the plant, the two-choice tests were repeated with the same population of C. vestalis parasitoids and the same population of DBM caterpillars, but a different variety of B. oleracea
Our experiments reveal that cabbage seedlings show such a positive response to the density of CWB caterpillars (Figure 4a): with an increase in CWB density, the total amount of all induced volatiles together increased significantly and the amounts of some induced volatiles increased, two significantly (Figure 4a) and one almost significantly

Summary

Introduction

Plants release specific blends of volatile chemicals in response to insect herbivory, thereby attracting the herbivore’s enemies [1,2,3]. At some point the predator may discover that the plant has little to offer and leave, but unwillingly it has given a benefit to the mutant plant in terms of protection against any herbivore already present or attempting to settle Such mutant plants overproducing the signal are further referred to as dishonest or ‘‘cry wolf’’ signalers, a term first used in the biological literature in relation to alarm calling behaviour of birds [8]. ‘‘Cry wolf’’ plants create a conflict of interests with the enemy of its enemies: the plant does not provide information to the herbivores’ enemies about the number of potential prey it harbours [9] Such conflicts are of paramount importance in driving the evolutionary dynamics of herbivore-induced plant signals: when plants sending honest signals are common, there is opportunity for mutants sending dishonest signals and once plants sending dishonest signals become too common, plants sending new-and-honest signals will be favoured by selection. Evolutionary models of the ‘‘cry wolf’’ game predict sustained waves of honest and dishonest signals under a broad range of conditions [10,11]

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