Caterpillar-induced rice volatiles provide enemy-free space for the offspring of the brown planthopper

Abstract

Plants typically release large quantities of volatiles in response to herbivory by insects. This benefits the plants by, for instance, attracting the natural enemies of the herbivores. We show that the brown planthopper (BPH) has cleverly turned this around by exploiting herbivore-induced plant volatiles (HIPVs) that provide safe havens for its offspring. BPH females preferentially oviposit on rice plants already infested by the rice striped stem borer (SSB), which are avoided by the egg parasitoid Anagrus nilaparvatae, the most important natural enemy of BPH. Using synthetic versions of volatiles identified from plants infested by BPH and/or SSB, we demonstrate the role of HIPVs in these interactions. Moreover, greenhouse and field cage experiments confirm the adaptiveness of the BPH oviposition strategy, resulting in 80% lower parasitism rates of its eggs. Besides revealing a novel exploitation of HIPVs, these findings may lead to novel control strategies against an exceedingly important rice pest.

Cooperative herbivory between two important pests of rice

“…This is also the case for our study system. We previously showed that BPH preferentially oviposits on SSB-infested rice plants, thereby avoiding the attraction of the egg parasitoid Anagrus nilaparvatae 25 . These various examples confirm that insect herbivores not only can evolve the ability to use volatiles to identify host plants of better nutritional quality, but also plants where their offspring can escape natural enemies 50 .…”

“…The copyright holder for this preprint this version posted March 11, 2021. ; https://doi.org/10.1101/2021.03.10.434708 doi: bioRxiv preprint BPH is a phloem-sucking insect that feeds at the surface on leaf blades and leaf sheaths 25,59 . Hence, there is usually no direct physical interaction between the two species.…”

“…(v) SSB→BPH-infested plants, each potted rice plant was artificially infested with one SSB larvae alone for the first 24 hr, then 15 BPH nymphs were additionally introduced for another 24 hr; vi) BPH→SSB-infested plants, namely each potted rice plant was artificially infested with 15 BPH nymphs for the first 24 hr, then one SSB larvae were additionally introduced for another 24 hr. Plant treatments were conducted as described in detail in our previous study 25 . During herbivory treatment, the uninfested plants were placed in a separate room to avoid possible volatile-mediated interference.…”

“…The copyright holder for this preprint this version posted March 11, 2021. ; https://doi.org/10.1101/2021.03.10.434708 doi: bioRxiv preprint that make these plants less toxic and/or more nutritious 16,17,[19][20][21][22] or by masking the (volatile) foraging cues used by natural enemies [23][24][25][26][27] . To our knowledge, however, there are no known examples of two species of herbivores both consistently benefitting from presence of each other on the same host plants.…”

“…Here we propose such a coevolved partnership between the brown planthopper (BPH), Nilaparvata lugens and the rice striped stem borer (SSB), Chilo suppressalis , two of the most devastating pests of rice 29 . Our hypothesis that both insects benefit from attacking the same plant was prompted by our recent finding that BPH can escape parasitism of its eggs by preferentially ovipositing on rice plants that are already infested by SSB 25 . The apparent reason for this oviposition strategy is that, Anagrus nilaparvatae , the most common egg parasitoid of BPH, uses volatiles emitted by BPH-infested plants to locate plants with eggs.…”