Effects of multiple herbivore infestation on chemically mediated interactions: from meta-analysis to case study

Abstract

The response of plants to herbivory are modulated by the level of infestation and identity of the herbivores, influencing plant defenses, herbivore performance, and their interactions with natural enemies (NEs). This study explores how multiple infestations by arthropods affect plant defense induction and herbivore-induced plant volatiles (HIPVs), with consequences for tritrophic interactions. Through a broader analysis of these interactions via meta-analysis, we found that while co-infestations alter volatiles composition, they do not necessarily impair the ability of NE to locate their host. Specialist NEs did not differentiate between HIPVs from their host alone or in co-infestation with non-host herbivores. This result suggests that chemical communication remains stable despite the complexity imposed by herbivory. Contrary to expectations, generalist NEs exhibit a preference for volatiles emitted by plants hosting a greater diversity of herbivores. However, a tendency was observed for generalists to prefer plants infested by herbivores from distinct feeding guilds (piercing sucking and chewing) over those infested by a single host species. In a specific case study with coffee plants (Coffea arabica) infested by Coccus viridis (green scales) and Planococcus citri (citrus mealybugs), we examined plant defense pathways, herbivore performance, and the response of the coccidophagous predator Cryptolaemus montrouzieri. Our results indicated that mealybugs induced an increase in jasmonic acid (JA) and salicylic acid (SA) levels, whereas herbivory by green scales triggered SA accumulation without altering the JA pathway, a pattern known as SA-JA negative crosstalk, commonly observed in phloem-feeding insect infestation. This hormonal modulation resulted in a secondary metabolite profile (alkaloids and phenolic compounds) in the leaves that differed from plants infested by Co. viridis and P. citri. Infestation

by one scale species did not influence the subsequent choice of the other species, but the co- infestation impacted P. citri performance. The ladybird beetle Cr. montrouzieri was able to

recognize plants infested by green scales or mealybugs through HIPVs, showing a preference for volatiles emitted by infested plants over non-infested ones. However, multiple infestations altered the volatile profile in a way that was not recognized by the ladybird as a cue for prey presence. These findings highlight the complexity of multitrophic interactions mediated by plant defenses, emphasizing species-specific defense induction and the resilience of tritrophic signaling. Understanding these dynamics provides valuable insights into plant resistance strategies, biological control, and their implications for pest management in agricultural systems.