Identity Matters: Multiple Herbivory Induces Less Attractive or Repellent Coffee Plant Volatile Emission to Different Natural Enemies

Co-infestations by herbivores, a common situation found in natural settings, can distinctly affect induced plant defenses compared to single infestations. Related tritrophic interactions might be affected through the emission of changed blends of herbivore-induced plant volatiles (HIPVs). In a previous study, we observed that the infestation by red spider mite (Oligonychus ilicis) on coffee plants facilitated the infestation by white mealybug (Planococcus minor), whereas the reverse sequence of infestation did not occur. Here, we examined the involvement of the jasmonate and salicylate pathways in the plant-mediated asymmetrical facilitation between red spider mites and white mealybugs as well as the effect of multiple herbivory on attractiveness to the predatory mite Euseius concordis and the ladybug Cryptolaemus montrouzieri. Both mite and mealybug herbivory led to the accumulation of JA-Ile, JA, and cis-OPDA in plants, although the catabolic reactions of JA-Ile were specifically regulated by each herbivore. Infestation by mites or mealybugs induced the release of novel volatiles by coffee plants, which selectively attracted their respective predators. Even though the co-infestation by mites and mealybugs resulted in a stronger accumulation of JA-Ile, JA and SA than the single infestation treatments, the volatile emission was similar to that of mite-infested or mealybug-infested plants. However, multiple infestation had a negative impact on the attractiveness of HIPVs to the predators, making them less attractive to the predatory mite and a repellent to the ladybug. We discuss the potential underlying mechanisms of the susceptibility induced by mites, and the effect of multiple infestation on each predator.