Susceptibility of Liriomyza sativae Blanchard (Diptera: Agromyzidae) populations to reduced risk insecticides

Highlights

• Susceptibility of Liriomyza sativae to novel insecticides was surveyed in Brazil.

• Large variation of response to chlorantraniliprole was observed among populations.

• Most populations were very susceptible to cyantraniliprole and spinetoram.

• Evidence of cross-resistance was observed among novel and classical insecticides.

• Other control measures than insecticides must be encouraged to delay resistance in L. sativae.

Abstract

Liriomyza sativae Blanchard is a major pest of melon and other crops in the Northeast of Brazil, where it has caused great losses despite the use of insecticides to reduce infestations. Previous studies showed that Liriomyza flies can develop resistance to several groups of insecticides, making difficult its control in the field. Bioassays to estimate the concentration-mortality curves were performed to investigate the response of L. sativae populations to abamectin, spinosad and chlorantraniliprole, as well as to establish a baseline for cyantraniliprole and spinetoram. The LC₅₀ values for abamectin varied from 2.8 (PB1 population) to 4.8 (MSR2 population) mg/L, for chlorantraniliprole from 0.5 (MSR2 population) to 15.8 (PB1 population) mg/L, for cyantraniliprole from 0.7 (MSR1 population) to 5.2 (CMSF population) mg/L, for spinosad from 1.0 (PB3 population) to 13.5 (MSR2 population) mg/L, and for spinetoram from 0.2 (PB3 population) to 0.6 (MSR2 population) mg/L. Resistance ratios higher than 10-fold were observed for the populations PB3 (12.5-fold), CMSF (12.8-fold), PB1 (34.53-fold) for chlorantraniliprole, and MSR2 population (13.1-fold) for spinosad. The highest resistance ratio for abamectin, cyantraniliprole and spinetoram was respectively 1.8-fold (MSR2 population), 7.2-fold (CMSF population) and 3.1-fold (MSR2 population). Recommended doses of abamectin and spinosad caused 100% mortality of assessed populations. Overall, enzyme activities showed no association between susceptibility and insecticides among populations but were variable among populations. Monitoring and product rotation for managing the evolution of L. sativae to resistance is recommended.

Introduction

The polyphagous and cosmopolitan serpentine leafminer, Liriomyza sativae Blanchard (Diptera: Agromyzidae), is among the major pests of many agricultural and ornamental crops (Reitz et al., 2013). It is one of the most economically important pests of horticultural crops in the Northeast region of Brazil, where it has inflicted yield losses up to 15% in melon (Cucumis melo L.) in the Rio Grande do Norte state (Araujo et al., 2007). Although cultural and behavior-based practices are used to manage it, chemicals sprays are an integral measure to reduce L. sativae population outbreaks in Brazil (Lima et al., 2012). Cyromazine, abamectin and cartap hydrochloride are the most used molecules to control L. sativae in melon crops (AGROFIT, 2019). This narrow portfolio of modes of action (MoA) has curtailed the proper rotation of active ingredients, increasing the risk of resistance evolution. Despite the frequent use of abamectin and cyromazine for several years against L. sativae in many countries, few resistance cases have been reported so far (Cox et al., 1995; Ferguson, 2004; Ferguson and Pineda, 2010; IRAC, 2019; Reitz et al., 2013). However, previous studies showed that Liriomyza spp. can develop resistance to various insecticides from distinct chemical groups compromising sustainable control in the future (Askari Saryazdi et al., 2014; Ferguson, 2004; Ferguson and Pineda, 2010).

The limited number of insecticides used to control L. sativae associated with its frequent outbreaks are potential factors to increase its tolerance to insecticides, rendering them ineffective in the future (Parrella, 1987). Registration of new active ingredients is important to delay the loss of insecticides already in use, allowing an adequate rotation of MoAs. In this context, a baseline of susceptibility of L. sativae in Brazil is needed for any potential new insecticide, because it is the first step of a successful resistance management program. With that baseline, the natural variability of the species’ response to a given insecticide prior to market release may be determined. Spinetoram (a spinosyn) and cyantraniliprole (an anthranilic diamide) were recently commercialized in Brazil against the larval stage, but no data have been published regarding susceptibility of populations to these two insecticides.

There are no reported instances of L. sativae resistance to insecticides to date in Brazil. However, there is a high risk of resistance evolution in this species in Brazil because of the previous use of spinosad and chlorantraniliprole. Resistance to insecticides is an inherent ability of an organism to survive insecticide doses that would be lethal under normal conditions to other individuals of its species (Croft and van De Baan, 1988; Whalon et al., 2008). Other than cases with abamectin and cyromazine (Ferguson, 2004), Askari Saryazdi et al. (2014) reported resistance in Iranian populations of L. sativae to fenpropathrin after selection pressure in greenhouses. Mechanisms involved in the development of insect resistance can include the reduction of penetration through the insect cuticle, target site insensitivity, and/or increased detoxification by metabolism (Hemingway, 2000). Major detoxification enzyme groups include esterase, glutathione S-transferases (GST) and oxidases, which have been observed at significant high titration in resistant populations (Askari-Saryazdi et al., 2015; Askari Saryazdi et al., 2014; Wei et al., 2015). High levels of activity of esterase and monooxygenase have been reported in populations of L. sativae resistant to fenpropathrin (Askari Saryazdi et al., 2014). Additionally, higher GST activities have been reported in L. sativae populations resistant to abamectin (Wei et al., 2015). Thus, these mechanisms of resistance may hinder the management of the leafminer in the field in view of the scarcity of products available for its control. The objectives of this study were to assess the susceptibility of L. sativae to several insecticides, and further investigate detoxification enzymes among populations for possible correlation with susceptibility.