Monitoring Resistance of Euschistus heros (Fabricius) (Hemiptera: Pentatomidae) to Insecticides by Using Encapsulated Artificial Diet Bioassay

Abstract

The novel ingestion bioassay method was developed for detecting and monitoring resistance of Euschistus heros by encapsulating an artificial liquid diet using Parafilm®. This methodology was compared with the tarsal contact (vial test) and topical application methods for thiamethoxam, imidacloprid, and lambda-cyhalothrin. The best bioassay method for the neonicotinoid insecticides thiamethoxam and imidacloprid was ingestion. For pyrethroid insecticide lambda-cyhalothrin, the best result was obtained by topical application. Using the best bioassay method for each insecticide, the susceptibility to these insecticides was monitored in 30 populations of E. heros collected from soybean crops in Brazil from 2018 to 2020. High variations in susceptibility to thiamethoxam (resistance ratios, 1.6–22 times), imidacloprid (resistance ratios, 1.6–22 times), and lambda-cyhalothrin (resistance ratios, 5–40 times) were detected among the evaluated E. heros populations. In order to monitor the susceptibility of E. heros to insecticides, diagnostic concentrations were defined based on the LC99 of the susceptible reference population: 5.65 µL of a.i./mL for thiamethoxam, 12.45 µL of a.i./mL for imidacloprid, and 0.20 µg of a.i./insect for lambda-cyhalothrin. Subsequently, we select an E. heros strain resistant to neonicotinoid insecticides and another to lambda-cyhalothrin. The resistance ratios obtained after seven selection cycles were 66, 41 and 44 times for thiamethoxam, imidacloprid and lambda-cyhalothrin, respectively.

Sex‐dependent body mass and respiratory responses on Euschistus heros individuals resistant to imidacloprid

“…Our present efforts highlight the involvement of other resistance mechanisms in the ImiPBOSel strain, as the application of PBO (an inhibitor of the monooxygenase system) speeds up the selection of imidacloprid resistant individuals, leading ImiPBOSel individuals to resist exposure to imidacloprid concentrations as high as 40‐fold the field rate recommendation. The existence of multiple resistance mechanisms may contribute to the increasing number of reports indicating that imidacloprid‐containing commercial formulations do not adequately control E. heros populations (Somavilla, Reis, et al, 2020, Somavilla, da Gubiani, et al, 2020; Sosa‐Gómez et al, 2020; Steinhaus et al, 2022; Tibola et al, 2021; Tuelher et al, 2018).…”

“…The adoption of this control strategy has caused neonicotinoid substances to be integrated (alone or in combination with other molecules) into virtually all insecticide formulations registered for controlling stink bugs in the Neotropical region (MAPA, 2022), which threatens the efficacy of the strategy. Reductions on the strategy efficacy might derive from the indiscriminate use and overuse of neonicotinoids, as it has favoured the selection of resistant individuals (Castellanos et al, 2019; Somavilla, da Gubiani, et al, 2020; Somavilla, Reis, et al, 2020; Sosa‐Gómez et al, 2020; Steinhaus et al, 2022; Tibola et al, 2021; Tuelher et al, 2018), and led to hormetic (i.e., stimulatory) effects on the behavioural and physiological responses of sublethally exposed insects (Haddi et al, 2016; Rodrigues et al, 2021; Santos, Campos, et al, 2016; Tuelher et al, 2017). The selection of resistant individuals and the undesirable hormetic effects, that is, when mild stress protects and improves animal performance (Berry & López‐Martínez, 2020; Cutler et al, 2022; Guedes et al, 2016), may have contributed to E. heros population outbreaks in Neotropical regions.…”

“…Among neonicotinoids, imidacloprid is one of the largest marketable insecticides worldwide (Casida, 2018; Jeschke et al, 2011, 2013) and one of the most commonly used for the control of E. heros . However, an increasing number of reports of imidacloprid resistance have been demonstrated in Brazilian populations of E. heros (Somavilla, da Gubiani, et al, 2020; Somavilla, Reis, et al, 2020; Steinhaus et al, 2022; Tibola et al, 2021; Tuelher et al, 2018). Imidacloprid exerts its toxicity primarily by causing irreversible disruption of the functions of nicotinic acetylcholine receptor (nAChR) subtypes expressed in the insect nervous system (Jeschke & Nauen, 2008; Oliveira et al, 2010, 2011; Salgado, 2016; Salgado & Saar, 2004), although its actions at secondary targets also play pivotal roles in its efficacy (Castellanos et al, 2021; Perez Campos et al, 2021; Stamm et al, 2011; Yuan et al, 2021).…”

“…Reductions on the strategy efficacy might derive from the indiscriminate use and overuse of neonicotinoids, as it has favoured the selection of resistant individuals (Castellanos et al, 2019;Sosa-G omez et al, 2020;Steinhaus et al, 2022;Tibola et al, 2021;Tuelher et al, 2018), and led to hormetic (i.e., stimulatory) effects on the behavioural and physiological responses of sublethally exposed insects (Haddi et al, 2016;Rodrigues et al, 2021;Santos, Campos, et al, 2016;Tuelher et al, 2017). The selection of resistant individuals and the undesirable hormetic effects, that is, when mild stress protects and improves animal performance (Berry & L opez-Martínez, 2020;Cutler et al, 2022;Guedes et al, 2016), may have contributed to E. heros population outbreaks in Neotropical regions.…”

Transcriptomic investigation of the molecular mechanisms underlying resistance to the neonicotinoid thiamethoxam and the pyrethroid lambda‐cyhalothrin in Euschistus heros (Hemiptera: Pentatomidae)

“…Such decrease in the frequency of the susceptible phenotypes in field conditions has facilitated the selection of two strains of E. heros with resistance to the neonicotinoid thiamethoxam or to the pyrethroid lambda-cyhalothrin. 6,[9][10][11][12][13][14][15] The ease with which resistance can be selected in the laboratory serves as a warning of the high risk of field evolved resistance in E. heros to neonicotinoids and pyrethroids if integrated pest management and insect resistance management strategies are not employed.…”