Abstract
BackgroundVolatiles emitted by herbivore-infested plants are highly attractive to parasitoids and therefore have been proposed to be part of an indirect plant defense strategy. However, this proposed function of the plant-provided signals remains controversial, and it is unclear how specific and reliable the signals are under natural conditions with simultaneous feeding by multiple herbivores. Phloem feeders in particular are assumed to interfere with plant defense responses. Therefore, we investigated how attack by the piercing-sucking cicadellid Euscelidius variegatus influences signaling by maize plants in response to the chewing herbivore Spodoptera littoralis.ResultsThe parasitoid Cotesia marginiventris strongly preferred volatiles of plants infested with its host S. littoralis. Overall, the volatile emissions induced by S. littoralis and E. variegatus were similar, but higher levels of certain wound-released compounds may have allowed the wasps to specifically recognize plants infested by hosts. Expression levels of defense marker genes and further behavioral bioassays with the parasitoid showed that neither the physiological defense responses nor the attractiveness of S. littoralis infested plants were altered by simultaneous E. variegatus attack.ConclusionsOur findings imply that plant defense responses to herbivory can be more robust than generally assumed and that ensuing volatiles convey specific information about the type of herbivore that is attacking a plant, even in complex situations with multiple herbivores. Hence, the results of this study support the notion that herbivore-induced plant volatiles may be part of a plant's indirect defense stratagem.
Highlights
Volatiles emitted by herbivore-infested plants are highly attractive to parasitoids and have been proposed to be part of an indirect plant defense strategy
Parasitoid attraction To test whether the parasitoid C. marginiventris is able to distinguish between volatile blends from plants infested with its host S. littoralis and volatiles emitted by plants infested with the non-host E. variegatus, we performed an olfactometer assay giving the wasps a choice between uninfested, S. littoralis, and E. variegatus-infested plants
Previous contact with E. variegatus over a period of 2 minutes drastically reduced the overall responsiveness of the wasps and the choice for the odor of host-infested plants: Compared to naïve and host-experienced wasps, wasp choice was reduced by 50% after they had contacted E. variegatus while being exposed to the odor of E. variegatus infested plants and by two thirds after they encountered E. variegatus in association with the odor of S. littoralis-infested plants (Figure 1b)
Summary
Volatiles emitted by herbivore-infested plants are highly attractive to parasitoids and have been proposed to be part of an indirect plant defense strategy. Parasitoids in particular can use herbivore-induced plant volatiles (HIPVs) as host-searching cues [1,2] Such volatile-mediated tritrophic interactions have a considerable potential to shape ecosystem dynamics [3], but it remains unclear to what extend the plant signals are emitted by the plant to attract natural enemies of herbivores [4]. If HIPVs are emitted by the plant to attract the third tropic level, specificity of the signals should be an important aspect of the interactions [5] This is relevant under natural conditions, where plants are often attacked by non-hosts or indicating host presence, even in a complex situation with multiple herbivore attacking the same plants. Little is known about this alleged robustness of volatile-mediated tritrophic interactions
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