Herbivory affects subsequent herbivores, mainly regulated by the phytohormones jasmonic (JA) and salicylic acid (SA). Additionally, organisms such as soil microbes belowground or parasitoids that develop inside their herbivorous hosts aboveground, can change plant responses to herbivory. However, it is not yet well known how organisms of trophic levels other than herbivores, below- and above-ground, alter the interactions between insect species sharing a host plant. Here, we investigated whether the parasitoid Aphidius colemani and different soil microbial communities (created through plant-soil feedbacks) affect the JA and SA signalling pathways in response to the aphid Myzus persicae and the thrips Frankliniella occidentalis, as well as subsequent thrips performance. Our results show that the expression of the JA-responsive gene CaPINII in sweet pepper was more suppressed by aphids than by parasitised aphids. However, parasitism did not affect the expression of CaPAL1, a biosynthetic gene of SA. Furthermore, aphid feeding enhanced thrips performance compared with uninfested plants, but this was not observed when aphids were parasitised. Soils where different plant species were previously grown, did not affect plant responses or the interaction between herbivores. Our study shows that members of the third trophic level can modify herbivore interactions by altering plant physiology.

Herbivore natural enemies base their foraging decision on information cues from different trophic levels but mainly from plant odors. However, the second trophic level (i.e., the herbivorous prey) may also provide reliable infochemical cues for their natural enemies. We have evaluated the role of the aggregation pheromone from Frankliniella occidentalis (Pergande) as a potential kairomone for its natural enemy, the predatory bug Orius laevigatus (Fieber). For this purpose, we have analyzed the response of O. laevigatus to (R)-lavandulyl acetate and neryl (S)-2-methylbutanoate, the two major components of the thrips aggregation pheromone. These compounds have been offered to O. laevigatus adult females and nymphs of the predatory bugs both in separate and as specific (1:1 or 1:2.3) blends, in experiments involving a dual choice Y-tube olfactometer. None of the compounds attracted adults or nymphs when they were individually supplied. Conversely, they were significantly attracted to both adults and nymphs when offered as a blend. A 1:2.3 (R)-lavandulyl acetate:neryl (S)-2-methylbutanoate blend was attractive to both nymphs and adults, while a 1:1 blend elicited response only in nymphs. These results suggest that specific blends of these compounds from the aggregation pheromone may be used as an attractant to O. laevigatus. The results of this work highlight the importance of studying olfactory responses of natural enemies for a better understanding of their foraging behavior. Potential uses of these results in future studies are discussed.

In complex food webs, plants are commonly attacked by multiple herbivorous species, affecting the preference and performance of other herbivores and natural enemies. The role of omnivorous insects in ecosystems may be more complex because of the consumption of both plant and animal organisms. However, the effect of omnivorous insects on herbivores and natural enemies, has received little attention so far. The main goal of this study was to investigate whether the dual herbivore interaction between aphids and thrips, an omnivorous pest, on a sweet pepper system, may affect different trophic levels, from plant and aphid performance until the third trophic level, i.e., preference and performance of the predatory hoverfly Sphaerophoria rueppellii. Additionally, we tested whether the aggregation pheromone of the thrips Frankliniella occidentalis, could disturb the oviposition behavior of the predatory hoverfly. Our results show that the presence of thrips decreases host plant and aphid performance. Furthermore, despite not affecting syrphid larval performance, thrips presence reduces fecundity of the adults that emerge from those larvae. Additionally, we observed that syrphids avoid ovipositing on plants with either thrips or thrips aggregation pheromone. The present study reveals how the presence of thrips or a semiochemical compound related to thrips, can impact the behavior and performance of an aphidophagous predator.