Ecological consequences of plant defense induction by biocontrol agents

Background/Question/Methods

Natural enemies of herbivorous arthropods such as predatory insects are known mainly for their ability to impact prey directly, via consumption. Nevertheless, certain zoophytophagous predatory insects are known to also affect herbivores indirectly, via their phytophagy and the elicitation of plant defense responses. Hence, zoophytophagous predators can play a conflicting role for the plant because they prey on herbivores but also feed with the plant. To unravel the role of zoophytophagous predators in shaping plant-herbivore interactions which is a field largely unexplored, we study the mechanisms and underlying ecological consequences of this behaviour. We conducted performance experiments where we exposed plants to mirid predators (Macrolophus pygmaeus) for four days and then challenged these plants with herbivorous arthropods (spider mites). Gene expression and phytohormones analyses were performed for leaf tissue harvested from exposed and control plants to assess any defense-related effects that could be explained by predator phytophagy. Furthermore, as we are interested in the ways zoophytophagous predators may be affected by the presence of other biocontrol agents such as beneficial soil microbes found belowground, we performed performance and olfactometer experiments where we inoculated plants with soil microbes (Trichoderma sp.,) and then recorded their plant-mediated effects on predator performance and behaviour.

Results/Conclusions

We show that the phytophagy of zoophytophagous predators may lead to the induction of plant responses that affect the performance of herbivores arriving later on the plants. Specifically, we found that spider mites can be negatively affected on plants exposed to the predators; this negative effect was shown in parallel to the increased expression of JA-related marker genes in these plants. Furthermore, the predators themselves can be affected by the inoculation of plants with certain microbial agents via the plant. In particular, we show that predator nymph emergence may not be affected in the presence of prey (i.e., whiteflies) but zoophytophagous predators (M. pygmaeus) are attracted by volatiles released from plants inoculated with Trichoderma sp. as compared to non-inoculated plants, either these were infested with prey or not. We conclude that plants respond to the phytophagy of zoophytophagous predators in ways similar to herbivores and this ability can be impacted by the presence of other biocontrol agents, via the plant. Studying the role of predators in affecting herbivores via their phytophagy, also the importance of soil microbes in shaping beneficial plant-predator interactions may help in the identification of sustainable pest control tools.