Flavonoid‐producing tomato plants have a direct negative effect on the zoophytophagous biological control agent Orius sauteri

Abstract

Orius sauteri (Poppius) (Hemiptera: Anthocoridae) is often used for biological control of small arthropod pests in greenhouse vegetable production systems in Asia. In addition to feeding on arthropod prey, O. sauteri consumes small quantities of plant material. Previous studies demonstrated that tomato plant chemistry confers antixenosis resistance to phloem-feeding whiteflies, but the potential nontarget effects of phytochemicals on the beneficial predator O. sauteri are unknown. Comparison of O. sauteri confined to near-isogenic lines (NILs) of tomatoes producing high levels of flavonoids (NIL-purple hypocotyl; resistant to whiteflies) and low levels of flavonoids (NIL-green hypocotyl; susceptible to whiteflies) revealed that O. sauteri had reduced oviposition, nymphal survival, and development on resistant plants, even if they were also provided with prey that did not feed on the host plant. Moreover, O. sauteri showed a significant ovipositional preference in choice assays, laying significantly more eggs on susceptible than on resistant plants. Molecular gut content analysis using the specific chloroplast trnL gene from tomato confirmed that adult and immature O. sauteri feed on both resistant and susceptible genotypes, and feeding behavior assays revealed that resistance did not affect plant feeding or prey acceptance by O. sauteri adults. These results demonstrate a direct negative effect of phytochemicals on a nontarget beneficial species and indicate that resistance mediated by phytochemicals can affect organisms that do not solely feed on phloem sap. The results also indicate that the mode of action and the potential ecological effects of phytochemicalmediated resistance are broader than previously recognized.

Negative Effects of Phthorimaea absoluta-Resistant Tomato Genotypes on the Zoophytophagous Biocontrol Agent, Orius laevigatus (Fieber) (Hemiptera: Anthocoridae)

“…In addition, female bugs deposited significantly fewer eggs on P. absoluta -resistant genotypes than on susceptible plants. Yang et al (2022) [ 34 ] reported similar results for O. sauteri on whitefly-resistant genotypes, suggesting that phytochemicals have a direct adverse effect on a beneficial species and phytochemical-mediated resistance can affect non-target insects. Additionally, they suggested that phytochemical-mediated resistance has a potential ecological impact.…”

“…Plant chemical composition may be particularly important to the performance of omnivorous consumers that feed on both prey and plant materials. Such omnivores may exhibit retarded development and impaired survival and fecundity when they feed on defended plants [ 34 , 43 ]. In addition, the efficacy of biological control agents may be inferior on crop plants that are defended by glandular trichomes [ 34 , 44 ].…”

“…Such omnivores may exhibit retarded development and impaired survival and fecundity when they feed on defended plants [ 34 , 43 ]. In addition, the efficacy of biological control agents may be inferior on crop plants that are defended by glandular trichomes [ 34 , 44 ]. It was therefore important to assess the direct effect of resistant crop genotypes on omnivorous predators of major pests in the system [ 2 ].…”

“…In the present study, therefore, we tested the compatibility of P. absoluta -resistant tomato genotypes to O. laevigatus. For the following reasons, we decided to use O. laevigatus for the present study even though Orius performance on tomato plants is inferior compared to that on other crop plants (e.g., [ 31 ]) and compared to that of mirid bugs on tomato [ 32 , 33 ]: (i) Orius bugs are readily found in tomato fields, with more than 1700 published studies; (ii) the performance of mirid bugs, such as Macrolophus and Nesidiocoris species, on tomato has been studied extensively, with more than 5000 published papers; and (iii) we are aware of only two studies of the effect of tomato resistance on Orius bugs [ 27 , 34 ]. Yet, these studies explored the response of O. insidiosus and O. sauteri , respectively, to aphid- and whitefly-resistant tomato, and it is well established that plant resistance to sucking insects differs from that to chewing pests ( P. absoluta in our study).…”

Flavonoids Are Intra- and Inter-Kingdom Modulator Signals

“…In this context, an interesting perspective relies on the use of agricultural wastes as flavonoids' source material under the frame of a circular economy approach, once field experiments and evaluations on features such as environmental fate and target specificity would have ensured their safe use [229]. Flavonoids can have indeed a harmful effect on nontarget beneficial species, as observed on the zoophytophagous generalist predator Orius sauteri, a biological control agent of whiteflies, which showed a reduced oviposition, nymphal survival, and development on flavonoids-producing tomatoes [233]. Several studies also reported the phagostimulant or neutral activity of flavonoids in dependence of the insect species considered and of the molecule and dosage selected [228,234].…”