Invasive insect herbivores as disrupters of chemically-mediated tritrophic interactions: effects of herbivore density and parasitoid learning

Authors: DESURMONT, GAYLORD - European Biological Control Laboratory (EBCL); GUIGUET, ANTOINE - Neuchatel University - Switzerland; TURLINGS, TED - Neuchatel University - Switzerland

Submitted to: Biological Invasions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/21/2017
Publication Date: 7/28/2017
Citation: Desurmont, G., Guiguet, A., Turlings, T.C. 2017. Invasive insect herbivores as disrupters of chemically-mediated tritrophic interactions: effects of herbivore density and parasitoid learning. Biological Invasions. DOI:10.1007/s10530-017-1526-x.

Interpretive Summary: Invasive species of insects can impact ecosystem functions in many ways. However, little is known about the factors that affect their impact on native plants, native insect herbivores, and the native beneficial insects (parasitoids) that attack them. Here we focused on the exotic caterpillar S. littoralis as a model of invader and studied how different densities of these caterpillars on a native plant Brassica rapa have a different impact on 1) the odors emitted by the plant, 2) its attractiveness to native parasitoids. Our results show that low and medium densities of the exotic caterpillar have a relatively minor impact on plant odors and parasitoid attraction, but that at high densities plants emit a different bouquet of volatiles that is unattractive to native parasitoids. However, parasitoids were shown to be able to learn the odors of plants infested by high densities of exotic herbivores and overcome their innate deterrence toward these plants. This study illustrates the complexity of the ecological effects of invaders on native communities can be, but it also illustrate some biological mechanisms (i.e. learning in native parasitoids) through which native organisms can attenuate the detrimental effects of invaders.

Technical Abstract: Invasive species of insect herbivores have the potential to interfere with native multitrophic interactions when they invade new environments. For instance, exotic herbivores can affect the chemical cues emitted by plants and disrupt attraction of natural enemies mediated by herbivore-induced plant volatiles (HIPVs). In a previous study, we found that the presence of the exotic herbivore Spodoptera littoralis on Brassica rapa plants infested by the native herbivore Pieris brassicae makes dually infested plants (S. littoralis + P. brassicae) unattractive to the main parasitoid of P. brassicae, the braconid wasp Cotesia glomerata. Here, we tested whether or not this effect is herbivore density-dependent, and whether or not parasitoids can overcome their innate avoidance of dually infested plants through associative learning. Herbivore density was found to play a critical role in S. littoralis interference. Parasitoids were only deterred by dually infested plants when the density of S. littoralis on the plant exceeded the density of P. brassicae. At the chemical level, the blend of HIPVs emitted by dually infested plants differed the most from HIPVs emitted by Pieris-infested plants when S. littoralis density exceeded P. brassicae density, supporting the behavioral data. Associative learning also played a role in parasitoid preferences: attraction to dually infested plants increased when parasitoids were presented a P. brassicae caterpillar (rewarding experience) in presence of the odor of a dually infested plant, but not when presented a S. littoralis caterpillar (non-rewarding experience). A non-rewarding experience prior to the bioassays resulted in decreased parasitoid motivation to respond to plant odors. In summary, our study shows that herbivore density and parasitoid learning mediate the impact of S. littoralis on the interactions between B. rapa, P. brassicae, and C. glomerata. These two factors likely play an important role in the foraging behavior of natural enemies in multi-herbivore communities and should not be overlooked when investigating the ecological impact of exotic species on native foodwebs.