Herbivore intoxication as a potential primary function of an inducible volatile plant signal

Abstract

1. Plants release herbivore-induced volatiles (HIPVs), which can be used as cues by plants, herbivores and natural enemies. Theory predicts that HIPVs may initially have evolved because of their direct benefits for the emitter and were subsequently adopted as infochemicals.2. Here, we investigated the potential direct benefits of indole, a major HIPV constituent of many plant species and a key defence priming signal in maize. We used indole-deficient maize mutants and synthetic indole at physiologically relevant doses to document the impact of the volatile on the generalist herbivore Spodoptera littoralis. 3. Our experiments demonstrate that indole directly decreases food consumption, plant damage and survival of S. littoralis caterpillars. Surprisingly, exposure to volatile indole increased caterpillar growth. Furthermore, we show that S. littoralis caterpillars and adults consistently avoid indole-producing plants in olfactometer experiments, feeding assays and oviposition trials. 4. Synthesis. Together, these results provide a potential evolutionary trajectory by which the release of a HIPV as a direct defence precedes its use as a cue by herbivores and an alert signal by plants. Furthermore, our experiments show that the effects of a plant secondary metabolite on weight gain and food consumption can diverge in a counterintuitive manner, which implies that larval growth can be a poor proxy for herbivore fitness and plant resistance.

Root volatiles in plant–plant interactions II: Root volatiles alter root chemistry and plant–herbivore interactions of neighbouring plants

“…First, many herbivores are mobile, and increasing herbivore growth on neighbouring plants may lead to accelerated migration to the sender plant. Second, herbivore growth, as measured here, is not synonymous with plant damage and may be the result of an increase in performance of the receiver plant, in which case their competitiveness would not be reduced, and the benefit for the emitter would be less evident (Erb, ; Veyrat et al, ). Third, the benefits of inducing susceptibility in neighbouring plants may be offset in the absence of herbivores.…”

“…Plant VOCs can influence herbivore performance directly or indirectly by changing the chemistry of receiver plants (Engelberth et al, ; Erb et al, ; Huang et al, ; Sugimoto et al, ; Veyrat, Robert, Turlings, & Erb, ; Ye et al, ). In our earlier work, we excluded the possibility that M .…”

Manipulating two olfactory cues causes a biological control beetle to shift to non‐target plant species

“…; Veyrat et al . ). For example, Manduca sexta larvae‐induced emission of ( Z )‐3‐hexenol, linalool and trans ‐α‐bergamotene from tobacco plants functions as an indirect defence leading to more than 90% herbivore mortality by predators in the field (Kessler & Baldwin ; Schuman et al .…”

Covariation and phenotypic integration in chemical communication displays: biosynthetic constraints and eco‐evolutionary implications

“…However, in cases where a number of compounds in fixed ratios is required for a given function, these compounds may be organized in modules with a tight covariation pattern whereas the other compounds of the bouquet may still vary independently from the compounds within the functional module, again resulting in a CCD with low integration values. The reduction in integration values in plants that experienced herbivory and thus emit herbivore‐induced volatiles may also be explained by the finding that a small number of volatiles within the blends have multiple functions, such as in the attraction of the herbivores’ enemies or the repellence of the herbivores independent of the other compounds (Kessler & Baldwin, ; Gols et al ., ; Veyrat et al ., ).…”