Characterization of pyridalyl resistance in a laboratory-selected strain of Frankliniella occidentalis

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Highlights

  • Field-collected F. occidentalis showed high susceptibility to pyridalyl in China.

  • No cross-resistance was detected in the PY-R strain to all tested insecticides.

  • Synergism effects of DEM and PBO were observed in the PY-R strain.

  • Pyridalyl-resistance conferred significant fitness costs in the PY-R strain.

Abstract

Frankliniella occidentalis, the western flower thrips, is one of most notorious pests on a variety of crops worldwide and many populations have high resistance to different types of insecticides. In order to determine the susceptibility of F. occidentalis to the insecticide pyridalyl in the field and to understand the potential mechanism of resistance, we conducted field monitoring of resistance and investigated cross-resistance, fitness cost, and synergism for the 75.8-fold pyridalyl-resistant strain (PY-R) established with a long-term successive laboratory selection. The results showed that all field populations of F. occidentalis had high susceptibility to pyridalyl from 2016 to 2017. The PY-R strain showed no cross-resistance to spinosad, spinetoram, abamectin, imidacloprid, or pyriproxyfen. Tests of synergism demonstrated that piperonyl butoxide (PBO) and diethyl maleate (DEM) significantly inhibited pyridalyl resistance in the PY-R strain. Moreover, PY-R showed lower pupation and emergence rates than the susceptible strain (XY-S), and female fecundity was also significantly lower in PY-R than in XY-S. By calculating the net replacement rate (R0) of XY-S, the fitness of PY-R was established as 0.52. In conclusion, the susceptibility of F. occidentalis to pyridalyl is still high in China, but resistance could be developed by successive-generation selections. Enhanced metabolic detoxification is possibly involved in resistance in PY-R, which caused significant fitness costs. Thus, pyridalyl will likely prove useful in the field for controlling F. occidentalis in China, and development of resistance could be delayed by rotating pyridalyl with other chemical agents lacking cross-resistance.

Introduction

Frankliniella occidentalis, the western flower thrips is one of the most notorious insect pests on agricultural crops around the world. It causes considerable damage and losses not merely via direct feeding, but by transmitting viruses as well (Whitfield et al., 2005; Morse and Hoddle, 2006). Relevant biological traits include tiny body size, high fecundity, short lifespan, and extensive geographical distribution, and thus application of insecticides has been proved as principal measure for management (Gao et al., 2012; Reitz et al., 2020). This heavy reliance on pesticides caused and accelerated the development of resistance to various types of insecticides in F. occidentalis such as organophosphates (Zhao et al., 1994), carbamates (Zhao et al., 1995; Jensen, 2000; Espinosa et al., 2005;), pyrethroids (Bielza et al., 2007, Bielza et al., 2008; Thalavaisundaram et al., 2008;), neonicotinoids (Zhao et al., 1995; Gao et al., 2014), avermectins (Kontsedalov et al., 1998; Chen et al., 2011) and spinosyns (Bielza et al., 2007; Zhang et al., 2008; Wang et al., 2016). Continued use of these insecticides is therefore not conducive for the production of agricultural crops with low chemical residues, and rotation among insecticides with diverse mechanisms of action is required to maintain high efficacy.

Pyridalyl is a new class of insecticide recognized by the Insecticide Resistance Action Committee (IRAC) with an unknown mode of action which has shown high insecticidal activity against Heliothis virescens, Plutella xylostella (Sakamoto et al., 2004) and F. occidentalis (Isayama et al., 2005), and it has been commercialized in many countries such as Korea, Japan, India, the Netherlands, the United States and so on (Jeschke et al., 2019). Compared with other popular chemical agents, pyridalyl has a unique chemical structure which gives it a particular insecticidal profile (Powell et al., 2011). Further, no cross-resistance was detected between pyridalyl and pyrethroids or organophosphates in H. virescens and P. xylostella (Moriya et al., 2008). Yin et al. (2018) also showed that there was no cross-resistance between pyridalyl and other insecticides such as abamectin, chlorfenapyr, and chlorantraniliprole, in P. xylostella. Moreover, it is noteworthy that pyridalyl showed minimal toxicity to beneficial insects and mammals (Sakamoto et al., 2004). Although pyridalyl has been demonstrated to be effective for controlling F. occidentalis in some countries (Isayama et al., 2005; Kay and Herron, 2010), the effects of pyridalyl on F. occidentalis have not yet been reported in China, and this agent has been registered in China recently and introduced into Chinese market in 2017. As with many commercially successful chemical agents, it is of great importance to assess the risk of resistance development, investigate the potential mechanism of resistance, and then design rational strategies of resistance management prior to the occurrence of resistance (Li et al., 2007). Thus, it is important to understand susceptibility of pests to pyridalyl in the field and to characterize resistance to pyridalyl in order to contribute to developing advanced pest control strategies.

It is well known that development of insecticide resistance results in fitness costs while no selection pressure of chemical agent was applied (Roush and McKenzie, 1987). Marked fitness costs in Frankliniella occidentalis including reduced survival rates, delayed growth, decreased fecundity have been demonstrated in the resistance to thiamethoxam and spinosad, respectively (Gao et al., 2014; Li et al., 2017). Study on fitness costs related with resistance to popular insecticides is essential for understanding and realizing how to delay the development of resistance (Georghiou and Taylor, 1977). Further, it is universally acknowledged that the strategy of rotation by using different classes of insecticides with no cross-resistance plays very important role in the field to delay the development of resistance, and fitness costs associated with resistance is one of prerequisites for the strategy (Kliot and Ghanim, 2012). So far, there are no reports about pyridalyl-associated resistance of the costs in F. occidentalis. Here, we first monitored the level of resistance to pyridalyl in F. occidentalis in the field in China to establish the baseline level of susceptibility. We conducted laboratory trials with successive-generation selection on a susceptible strain of F. occidentalis to generate a high level of resistance to pyridalyl. We then used both the susceptible and laboratory-selected pyridalyl-resistant strains to determine the cross-resistance pattern, synergism, and fitness costs of pyridalyl resistance in F. occidentalis.

Section snippets

Insects

One pyridalyl-susceptible (XY-S) and one pyridalyl-resistant strain (PY-R) of F. occidentalis were used. The susceptible XY-S strain was collected in a greenhouse in the city of Xiangyang, China in 2012, and then was reared on bean pods under controlled conditions without exposure to any pesticides over 4 years, following the method of Zhang et al. (2007). The resistant PY-R strain was derived from XY-S by exposing thrips to bean pods treated with formulated pyridalyl beginning in 2014, and the

Monitoring resistance to pyridalyl in China

From 2016 to 2017, monitoring of resistance to pyridalyl was conducted in several areas of China (Table 1). All field populations, which included 12 populations from 6 provinces of China, were susceptible to pyridalyl (LC50 values ranged from 1.16 to 5.21 mg L−1). Compared to the susceptible strain XY-S, the field populations showed no or very low-level resistance to pyridalyl (resistance ratios varied from 1.2 to 5.6-fold).

Pyridalyl resistance selection

Pyridalyl resistance in the susceptible F. occidentalis strain XY-S was

Discussion

In China, F. occidentalis has become a major pest of horticultural crops and has been widely distributed since 2003 (Zhang et al., 2003). A variety of chemical agents have been shown to fail to control it which means new chemical agent with different mode of action is needed for controlling of this pest (Gao et al., 2012). Our present work constructed a baseline susceptibility of F. occidentalis to pyridalyl in China and should be helpful for management of resistance development. These data are

Acknowledgments

This work was supported by the National Key Research Development Program of China (No. 2016YFD0200500), the National Key Technology R&D Program of China (No. 2014BAD23B01), the National Natural Science Foundation of China (21502061, 21332004), China Agriculture Research System (CARS-24-C-03).

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    These authors contributed equally to this study.

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