Attraction of Three Mirid Predators to Tomato Infested by Both the Tomato Leaf Mining Moth Tuta absoluta and the Whitefly Bemisia tabaci

Abstract

Plants emit volatile compounds in response to insect herbivory, which may play multiple roles as defensive compounds and mediators of interactions with other plants, microorganisms and animals. Herbivore-induced plant volatiles (HIPVs) may act as indirect plant defenses by attracting natural enemies of the attacking herbivore. We report here the first evidence of the attraction of three Neotropical mirid predators (Macrolophus basicornis, Engytatus varians and Campyloneuropsis infumatus) toward plants emitting volatiles induced upon feeding by two tomato pests, the leaf miner Tuta absoluta and the phloem feeder Bemisia tabaci, in olfactometer bioassays. Subsequently, we compared the composition of volatile blends emitted by insect-infested tomato plants by collecting headspace samples and analyzing them with GC-FID and GC-MS. Egg deposition by T. absoluta did not make tomato plants more attractive to the mirid predators than uninfested tomato plants. Macrolophus basicornis is attracted to tomato plants infested with either T. absoluta larvae or by a mixture of B. tabaci eggs, nymphs and adults. Engytatus varians and C. infumatus responded to volatile blends released by tomato plants infested with T. absoluta larvae over uninfested plants. Also, multiple herbivory by T. absoluta and B. tabaci did not increase the attraction of the mirids compared to infestation with T. absoluta alone. Terpenoids represented the most important class of compounds in the volatile blends and there were significant differences between the volatile blends emitted by tomato plants in response to attack by T. absoluta, B. tabaci, or by both insects. We, therefore, conclude that all three mirids use tomato plant volatiles to find T. absoluta larvae. Multiple herbivory did neither increase, nor decrease attraction of C. infumatus, E. varians and M. basicornis. By breeding for higher rates of emission of selected terpenes, increased attractiveness of tomato plants to natural enemies may improve the effectiveness of biological control.

Attractiveness of uninfested vegetables to the omnivorous predators Dicyphus bolivari and D. errans (Hemiptera: Miridae) and their relative suitability for oviposition

“…However, a preference for uninfested crop plants over clean air has also been found with Y-tube olfactometry for M. pygmaeus (Ingegno et al, 2011;Lins et al, 2014) and N. tenuis (Naselli et al, 2017;Rim et al, 2015) on tomato and eggplant (Solanum melongena L.). Similar results were found for three neotropical predatory mirids on tomato (Silva et al, 2018), by Abbas et al (2014) on tomato and D. maroccanus (today synonymized to D. bolivari according to Sánchez and Cassis, 2018), and by Pérez-Hedo and Urbaneja (2015) on sweet pepper for N. tenuis, M. pygmaeus, and D. maroccanus. Other authors have emphasized the importance of plant genotypes in explaining variability of results regarding the attractiveness of uninfested plants to natural enemies (Rapusas et al, 1996).…”

“…Although predatory bugs have been tested for preferences among odor sources (e.g. Ingegno et al, 2011;Silva et al, 2018), it remains unknown how well these experiments reflect actual behavior in the field (Ballhorn and Kautz, 2013). In this study, we found that orientation to volatile cues does not always reflect oviposition free choice under short-distance cues, as D. bolivari showed contradictory results for tomato and calendula between the olfactometer and oviposition assays.…”

Response of mirid predators to synthetic herbivore‐induced plant volatiles

“…Besides their attraction to the GLVs (Z)-3-hexenyl acetate and (Z)-3-hexenyl propanoate, this study provided evidence that N. tenuis, M. pygmaeus, and D. bolivari are attracted to synthetic MeSA. Interestingly, previous studies showed that mirid species are attracted to whitefly-and T. absoluta-infested plants (Lins et al, 2014;Silva et al, 2018), which frequently emit these three compounds ( Angeles-L opez et al, 2012;Silva et al, 2017). Application of these compounds in the field could possibly serve to guide these predators to tomato crop areas.…”

From Evolutionary Aspects of Zoophytophagy to Biological Control

“…These predators use various cues related to plant quality and prey availability to discriminate and select their host (Coll, 1996;Eubanks and Denno, 2000a,b;Grosman et al, 2005;Lins et al, 2014;Ingegno et al, 2016). For instance, zoophytophagous predators are attracted to volatiles from prey-infested plants (herbivore-induced plant volatiles; HIPVs) (Lins et al, 2014;De Backer et al, 2015;Silva et al, 2018). Lins et al (2014) observed that both M. pygmaeus and N. tenuis responded positively to plants infested by their prey [whitefly Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae) and the tomato borer Tuta absoluta Meyrick (Lepidoptera: Gelechiidae)].…”