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Journal of Asia-Pacific Entomology 18 (2015) 311–314

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Short Communication

Establishment of an insecticide resistance monitoring protocol based on the residual contact vial bioassay for Frankliniella occidentalis Deok Ho Kwon a, Kyungmun Kim b, Taek-Jun Kang c, Se-Jin Kim c, Byeong-Ryeol Choi d, Ju Il Kim e, Si Hyeock Lee a,b,⁎ a

Research Institute for Agriculture and Life Sciences, Seoul National University, Seoul 151-921, Republic of Korea Department of Agricultural Biotechnology, Seoul National University, Seoul 151-921, Republic of Korea Department of Horticultural Crop Research, National Institute of Horticultural and Herbal Science, RDA, Seoul 151-921, Republic of Korea d Division of Crop Protection, National Academy of Agricultural Science, Rural Development Administration, Suweon 440-707, Republic of Korea e Highland Agriculture Research Center, NICS, RDA, Pyeong-chang 232-955, Republic of Korea b c

a r t i c l e

i n f o

Article history: Received 14 January 2015 Revised 1 April 2015 Accepted 2 April 2015 Available online 11 April 2015 Keywords: Resistance Monitoring Frankliniella occidentalis Residual contact vial bioassay Insecticide Western flower thrips

a b s t r a c t A modified residual contact vial bioassay (RCV) in which a small aliquot (1 μl) of water was supplemented to minimize control mortality was established as a rapid insecticide resistance monitoring tool for the western flower thrips, Frankliniella occidentalis. Based on the RCV scheme, diagnostic doses for seven insecticides that are widely used for F. occidentalis control were determined at 8 h post-treatment using a susceptible RDA strain. The diagnostic doses for five insecticides (chlorfenapyr, acrinathrin, spinosad, emamectin benzoate and thiamethoxam) were in the range of 0.03 to 0.42 μg−1 cm2 and were readily applicable for the detection of resistance levels. In the case of the remaining two insecticides (omethoate and imidacloprid), however, the estimated diagnostic doses were too high (3.28 and 12.4 μg−1 cm2, respectively) to form a viscous film over the inner wall of the treated vial, thereby limiting their use for resistance detection. Thus, the performance of RCV in detecting resistance to the five insecticides was evaluated for five local populations of F. occidentalis. The RDA strain exhibited 100% mortality to all insecticides tested, whereas field populations collected from horticultural glass houses generally showed remarkably reduced mortality (b50%) to acrinathrin, thiamethoxam, spinosad, and emamectin benzoate, suggesting varying degrees of resistance to these insecticides. Chlorfenapyr resulted in relatively higher mortalities, indicating that it is a better option compared with the other insecticides for the control of these field populations. In summary, the RCV should facilitate the on-site resistance monitoring and the selection of appropriate insecticides against F. occidentalis. © 2015 Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society. Published by Elsevier B.V. All rights reserved.

Introduction The western flower thrips, Frankliniella occidentalis Pergande, are a serious cosmopolitan and polyphagous pests that feed on the flowers and leaves of horticultural and agricultural crops (Lewis, 1998). In addition to the direct damage by sucking, it causes indirect damage to plants by transmitting plant viruses, such as tospoviruses (Sakimura, 1962; Whitfield et al., 2005). Its endemic region is known to be western North America, but it has become a major crop pest worldwide after its spread to Europe, the Middle East and Asia since the late 1970s (Kirk and Terry, 2003). In Korea, F. occidentalis was first reported in a mandarin orange cultivation area of Jeju Province in 1994 (Woo et al., 1994), and currently it is widely spread all over the peninsula.

⁎ Corresponding author at: Department of Agricultural Biotechnology, Seoul National University, Seoul 151-921, Republic of Korea. Tel.: +82 2 880 4704; fax: +82 2 873 2319. E-mail address: [email protected] (S.H. Lee).

Many types of insecticides have been intensively used to control F. occidentalis, but resistant populations have rapidly emerged due to its short life cycle, high fecundity and haplotype genetic manners (Lewis, 1998; Jensen, 2000). Currently, approximately 163 cases of resistance have been reported for more than 26 active ingredients (Whalon et al., 2008) in Denmark (Brødsgaard, 1994), the USA (Immaraju et al., 1990), Spain (Espinosa et al., 2002a,b, 2005; Bielza et al., 2007), Turkey (Dağlı and Tunç, 2007), New Zealand (Martin et al., 2005), Australia (Herron et al., 1996; Herron and James, 2005; Thalavaisundaram et al., 2008), Japan (Katayama, 1998) and China (Wang et al., 2011). In Korea, the first insecticide resistance monitoring was reported in the mid-1990s for three different populations collected in Jeju Province (Cho et al., 1999). When treated with the recommended concentrations of nine commercialized insecticides, including organophosphates, carbamates, pyrethroids, neonicotinoids and macrocyclic lactones, the field populations exhibited extremely low mortalities (Cho et al., 1999). In the resistance survey conducted in 2001 and 2003, field

http://dx.doi.org/10.1016/j.aspen.2015.04.003 1226-8615/© 2015 Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society. Published by Elsevier B.V. All rights reserved.

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populations showed a wide range of resistance (1.5- to 1428.6-fold) to chlorfenapyr, chlorpyrifos-methyl, emamectin benzoate, fenthion, phenthoate, furathiocarb and diflubenzuron (Yu et al., 2002; Choi et al., 2005). The frequent occurrence of insecticide-resistant populations of F. occidentalis has been the major problem in the cultivation area of agricultural and horticultural crops, particularly in glass houses (Choi et al., 2005). Resistance monitoring is the most crucial element in the efficient management of insecticide-resistant pest populations. Several resistance monitoring methods for F. occidentalis have been developed based on bioassays, such as topical application (Robb, 1989; Espinosa et al., 2002a,b; Espinosa et al., 2005; Bielza et al., 2007), indirect plant tissue (leaf, petal or pod) dipping (Cho et al., 1999; Jones et al., 2005; Martin et al., 2005; Guillén and Bielza, 2013; Guillén et al., 2014; Herron et al., 2014), direct spray (Herron et al., 1996; Herron and James, 2005; Kay and Herron, 2010) and glass-vial assay with food supplement (Zhao et al., 1995; Choi et al., 2005; Shan et al., 2012). Nevertheless, for a routine and large scale resistance monitoring, it is desirable to employ any bioassay method that is simpler to conduct and requires less time commitment. To develop a simple bioassay method that can be readily used in the field for the resistance monitoring of F. occidentalis, we have modified the residual contact vial (RCV) bioassay (Kwon et al., 2010). In the modified RCV, 1 μl of water was supplemented to minimize control mortality, and the mortality of F. occidentalis using predetermined diagnostic doses of test insecticides was evaluated at 8 h post-treatment. Based on the diagnostic doses of five insecticides, the resistance levels in five field populations were evaluated.

24 and the GW_GR strain from Pyeongchang, Gangwon Province (37°40′49.87″N, 128°43′49.10″E) on June 30, 2014. Preparation of vials for RCV and determination of diagnostic doses The insecticide-treated vials were prepared according to the method reported by Kwon et al. (Kwon et al., 2010) with slight modifications to reduce the mortality at 8 h post-treatment. Briefly, a 1-μl aliquot of water was dispensed into a small piece of filter paper (0.5 × 0.5 mm) (Whatman, GE Healthcare, UK) attached underneath the vial screw cap to increase the humidity inside the vial and thereby minimize the control mortality of F. occidentalis. An aliquot (100 μl) of insecticide solution dissolved in acetone with various concentrations (0.3–1000 ppm of stock solution) was coated over the inside wall of a 5-ml glass vial (Taeshin Bio Science, Seoul, Korea) using a rolling wave rotator (Eberbach, Ann Arbor, MI, USA) for 1 h under a fume hood until the acetone was completely evaporated. The coated dose of insecticide was estimated to be 1.8 × 10− 3 ~ 6.1 μg− 1 cm2 inner surface of the 5-ml glass vial. Female adult thrips (12–15) were transferred to each insecticide-coated vial. The vial was closed with the watersupplemented cap, and the mortality was determined in triplicate at 8 h post-treatment. The RCV supplemented with water was designated RCVpW (abbreviated from Residual Contact Vial Bioassay Plus Water). Thrips showing immobility for 2–3 s were considered dead. The LD50 and LD90 values were determined by probit analysis using IBM SPSS statistics ver. 20.0 (IBM Corp., NY, USA). A two-fold dose of LD90 for each insecticide was set as the diagnostic dose. Resistance monitoring of field populations

Materials and methods Insecticides Eight test insecticides (acrinathrin, chlorfenapyr, emamectin, benzoate, imidacloprid, omethoate, spinosad, and thiamethoxam) were selected as they have been widely used for thrip control in Korea. All of the insecticides were of technical grade and purchased from either Sigma-Aldrich (Saint Louis, MO, USA) or Chem Service Inc. (West Chester, PA, USA). Their purities were as follows: acrinathrin (99.8%), chlorfenapyr (99.6%), emamectin benzoate (99.4%), imidacloprid (99.9%), omethoate (97.0%), spinosad (98.0%), and thiamethoxam (99.6%).

The vial coated with the diagnostic dose of insecticide was used for the evaluation of the insecticide resistance levels in field-collected populations of F. occidentalis. Field-collected adults (12–18 females) were directly transferred to the vials coated with the diagnostic dose of each insecticide, and the mortality was determined after 8 h. Statistical analysis The significance of mortality difference between field populations was determined by ANOVA (Analysis of variance) in conjunction with Turkey's honest significant difference (HSD) test using SPSS 2.0. Results

Strains and rearing

Establishment of RCVpW

The RDA strain of F. occidentalis was reared using cotyledon of kidney beans (Phaseolus vulgaris) according to the method reported by Baek (2005) with slight modifications. Briefly, bean seeds were planted in sterilized soil for six days at 28 ± 1 °C and 55 ± 5% relative humidity (RH), and the sprouted cotyledon was used as a food source. An insect breeding dish (91.4 ø × 40-mm height, SPL Life Sciences, Korea) was based with water (4 ml)-soaked thin-layered cotton. Twenty to thirty cotyledons were supplied as food to maintain 100–200 female adults at each breeding dish under the conditions of 25 ± 1 °C, 55 ± 5% relative humidity (RH) and a photoperiod of 16:8 (L:D) h. The RDA strain was originally collected from a field and has been reared under laboratory conditions for more than 10 years without any treatment with insecticide. The RDA strain was presumed to be relatively susceptible to insecticides and used as a reference strain for the determination of diagnostic doses. The five field populations of F. occidentalis were collected from several regions as follows: the RDAHR and RDAHC strains from Suwon, Gyeonggi Province (37°15′44.39″N, 126°58′34.20″E) on July 19 and July 29, respectively; the JB_JJ strain from Jeonju, Jeonbuk Province (35°53′9.8″N, 127°0′27.9″E) on May 16; the GG_GY strain from Goyang, Gyeonggi Province (37°45′35.79″N, 126°49′20.07″E) on June

The survival rate of F. occidentalis females transferred to the untreated control vial was determined (Fig. 1). The initial mortality was observed to be 3% at 4 h and reached 27.9% at 8 h after F. occidentalis was transferred to the test vials without any supplement of water. Supplementation of the vial with a 1-μl aliquot water resulted in no mortality up to 8 h post-treatment, and a low level of mortality was observed at 12 h (approx. 7.3%). This finding demonstrated that the addition of water minimized the control mortality of F. occidentalis and allowed evaluation of the pure insecticide toxicity with little influences by other factors at 8 h post-treatment. Determination of diagnostic dose Based on the established methods of RCVpW, the toxicity parameters for seven insecticides that are widely used for the control of F. occidentalis were determined using the reference RDA strain. The estimated LD50 values were in the range of 0.004 to 0.496 μg− 1 cm2. Spinosad exhibited the highest efficacy, followed by chlorfenapyr, emamectin benzoate, thiamethoxam and acrinathrin. Omethoate and imidacloprid were the least effective insecticides against F. occidentalis

D.H. Kwon et al. / Journal of Asia-Pacific Entomology 18 (2015) 311–314

Fig. 1. Comparison of the cumulative mortalities of Frankliniella occidentalis with or without water supplementation for 72 h in 5-ml glass vials. The data points represent the average mortality with the standard deviation.

as their LD50 values were determined to be 12.9- to 45.0-fold greater than those of the other insecticides examined. A two-fold amount of the LD90 dose was arbitrarily set as the diagnostic dose to ensure 100% mortality of the RDA strain (Table 1). With the exception of omethoate and imidacloprid, the diagnostic doses for the other insecticides were determined to be in the range of 0.03 to 0.42 μg−1 cm2. The diagnostic doses for omethoate and imidacloprid were too high (3.28 and 12.4 μg−1 cm2, respectively) to form a viscous film over the inner wall of the coated vial, causing non-selective physical damages to F. occidentalis and thereby limiting their use for resistance detection. Mortality of field populations determined by RCVpW The efficacy levels of the five insecticides, with the exception of omethoate and imidacloprid, were measured using the RCVpW method for five field populations. The four field populations (RDAHR, RDAHC, GG_GY and JB_JJ) collected from glass houses revealed relatively low susceptibilities (0–50% mortality) to acrinathrin, thiamethoxam, spinosad and emamectin benzoate (Table 2). However, the GW_GR population exhibited relatively higher susceptibilities (63.4–100% mortality) to all of the insecticides with the exception of acrinathrin. Chlorfenapyr resulted in relatively higher mortalities compared with the other insecticides, indicating that it is a better option for controlling field populations of F. occidentalis. Discussion Establishment of rapid and easy resistance detection methods is most important to manage insecticide-resistant populations of F. occidentalis.

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Various bioassay methods have been devised for the resistance monitoring of F. occidentalis. The dipping method (leaf, petal and pod) has been widely used for insecticide bioassay of thrips because it is easier to conduct than topical application and generally produces accurate and reliable results (Cho et al., 1999; Jones et al., 2005; Martin et al., 2005; Guillén and Bielza, 2013; Guillén et al., 2014; Herron et al., 2014). However, the preparation of dipping units before the infestation of thrips is a time-taking procedure and cannot be conducted in the field. The direct spraying method is similar to the dipping method in terms of the overall time commitment but produces relatively uneven data, perhaps due to the fact that controlling the exact amount of spray is not easy (Kwon et al., 2010). As a handier bioassay method, the glass-vial bioassay was developed (Zhao et al., 1995; Choi et al., 2005; Shan et al., 2012). However, this method was designed for evaluating mortality at 24 h post-treatment and uses a relatively large vial (20–22 ml) to hold the food source, thereby requiring large volumes of the test insecticides to completely coat the vial. In this study, as a less-technique-dependent bioassay method that can be easily used by practitioners who periodically monitor the resistance levels in the fields, a modified RCV protocol was established. In this method, the use of a smaller 5-ml vial facilitated insecticide coating with a smaller volume of the test insecticide and improved the overall practicability of the bioassay in terms of the easiness of mass production and handling and the simplicity of the procedure. The determination of mortality at 8 h post-treatment allowed completion of the whole procedures from thrip collection to bioassay within a day, thereby enabling a more prompt evaluation of the resistant level. The addition of 1 μl of water to the test vial was necessary to maintain optimum humidity inside the vial, thereby ensuring the control survivorship of thrips for at least 10 h without supplying food. The addition of more than 3 μl of water resulted in condensation of water around the inner surface of vials and increased mortality (data not shown), suggesting that the excess humidity level inside the vials is also detrimental. In addition, the procedures for thrip collection and transfer to the test vial can be simplified by employing an aspirator that can directly fit into the vial and be conducted on site (Kwon et al., 2010). Despite its several advantages, RCVpW was not applicable for some insecticides, such as omethoate and imidacloprid because the estimated diagnostic doses were too high. Since they have significantly lower octanol–water coefficients (Log Kow) (Table 1) compared with other insecticides, their penetration to the cuticle of thrips via contact was likely to be limited (Tomlin, 2000). However, thiamethoxam, which has a slightly higher but still negative Log Kow value, exhibited approximately 15-fold higher efficacy than imidacloprid, which belongs to the same neonicotinoid group. This finding suggests that, in addition to the low Log Kow values, any predisposed insecticide resistance traits in the reference RDA strain may contribute to the significantly reduced susceptibilities observed in the RCVpW bioassay. Because the RDA strain was initially collected from a field in 2005, when organophosphates and imidacloprid were extensively used for thrip control, the resistance traits to omethoate and imidacloprid may have predisposed. The scanning of known mutations associated with target site insensitivity in the transcriptome of the RDA strain identified an acetylcholinesterase

Table 1 Toxicity parameter and diagnostic doses. Groupa

Insecticide

Log Kowb

N

Slope ± SE

χ2

df

LD50c (μg−1 cm2, 95% CL)

LD90c

DDc,d

1B 3A 4A 4A 5 6 13

Omethoate Acrinathrin Imidacloprid Thiamethoxam Spinosad Emamectin benzoate Chlorfenapyr

−0.74 6.3 −0.24 −0.13 2.8 5.0 5.28

114 163 118 133 133 176 181

2.5 ± 0.3 3.1 ± 0.3 1.1 ± 0.2 1.5 ± 0.1 2.4 ± 0.2 1.4 ± 0.1 1.2 ± 0.1

0.6 2 0.4 10.1 14.3 3.3 20.4

1 2 1 2 2 2 3

0.496 (0.423–0.616) 0.034 (0.03–0.039) 0.438 (0.245–1.548) 0.029 (0.002–0.23) 0.004 (0.001–0.056) 0.020 (0.015–0.025) 0.011 (0.003–0.077)

1.64 0.089 6.18 0.21 0.014 0.15 0.132

3.28 0.18 12.4 0.42 0.03 0.30 0.26

a b c d

Group number classified by the mode of action according to the Insecticide Resistance Action Committee (IRAC). Log Kow represents the log octanol–water partition coefficient. The unit of LD50, LD90 and D/D is μg−1 cm2. DD represents the diagnostic dose (two-fold of LD90).

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Table 2 Mortality against five insecticides of five strains in F. occidentalis. Strains

RDA RDAHR RDAHC GG_GY JB_JJ⁎⁎ GW_GR

Host

– Rose Chrysanthemum Rose Rose Potato

Mortality (%, Average ± stdev) Acrinathrin

Thiamethoxam

Spinosad

Emamectin benzoate

Chlorfenapyr

100 ± 0 a⁎ 35.3 ± 13.1 b 7.5 ± 7.2 c 8.1 ± 8.3 c 50 17.2 ± 7.8 bc

100 ± 0 a 28.8 ± 5.2 b 15.0 ± 6.0 b 32.1 ± 10.2 b 8.3 ± 11.8 76.7 ± 15.1 a

100 ± 0 a 18.5 ± 23.1 b 0.0 ± 0.0 b 10.7 ± 5.2 b 0 100 ± 0 a

100 ± 0 a 5.3 ± 4.6 b 0.0 ± 0.0 b 14 ± 3.5 b 0±0 63.4 ± 33.1 b

100 ± 0 a 72.2 ± 26.8 a 64.4 ± 32.5 a 93.2 ± 6.7 a 92.3 ± 10.9 100 ± 0 a

⁎ Represents the significant difference by Tukey's HSD test. ⁎⁎ JB_JJ strain was excluded at the statistical analysis for the insufficient mortality data.

mutation that is related with organophosphate resistance (data not shown), supporting this notion. RCVpW was employed for the monitoring of the insecticide resistance levels in five field populations of F. occidentalis. Moderate to high levels of resistance to acrinathrin, spinosad, emamectin benzoate and thiamethoxam were observed in most field populations. In particular, RDAHR and RDAHC populations revealed low susceptibility to spinosad and emamectin benzoate. Compared to the resistance monitoring results obtained in 2001 (Yu et al., 2002) and 2003 (Choi et al., 2005), the current resistance levels to these insecticides appear to have increased, suggesting that F. occidentalis populations have been constantly selected by these newer-generation insecticides (Table 2). Among the insecticides investigated, chlorfenapyr revealed relatively higher efficacy, indicating that it is a better option compared with other insecticides for controlling these field populations. With a larger-scale determination of the diagnostic doses for other insecticides, the RCVpW should facilitate systematic and routine resistance monitoring in both the laboratory and field. In addition, it should provide basic information regarding the selection of appropriate insecticides against insecticide-resistant populations of F. occidentalis. Acknowledgments This work was supported by a grant (No. PJ009365) from the Rural Development Administration. KM Kim was supported in part by the Brain Korea 21 plus program. We also want to thank JY Lee and SH Kim for their assistance in maintaining the laboratory populations of thrips. References Baek, C.-H., 2005. Frankliniella occidentalis. In: Seol, K.-Y., Choi, B.-R., Kim, H.S. (Eds.), Insect rearing methods. Hanrimwon, Seoul, pp. 151–161. Bielza, P., Quinto, V., Contreras, J., Torné, M., Martín, A., Espinosa, P.J., 2007. Resistance to spinosad in the western flower thrips, Frankliniella occidentalis (Pergande), in greenhouses of south-eastern Spain. Pest Manag. Sci. 63, 682–687. Brødsgaard, H.F., 1994. Insecticide resistance in European and African strains of western flower thrips (Thysanoptera: Thripidae) tested in a new residue-on-glass test. J. Econ. Entomol. 87, 1141–1146. Cho, K., Uhm, K.B., Lee, J.O., 1999. Effect of test leaf and temperature on mortality of Frankliniella occidentalis in leaf dip bioassay of insecticides. J. Asia Pac. Entomol. 2, 69–75. Choi, B.-R., Lee, S.-W., Park, H.-M., Yoo, J.-K., Kim, S.-G., Baik, C.-H., 2005. Monitoring on insecticide resistance of major insect pests in plastic house. J. Pestic. Sci. 9, 380–390. Dağlı, F., Tunç, İ., 2007. Insecticide resistance in Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) collected from horticulture and cotton in Turkey. Aust. J. Entomol. 46, 320–324. Espinosa, P.J., Bielza, P., Contreras, J., Lacasa, A., 2002a. Field and laboratory selection of Frankliniella occidentalis (Pergande) for resistance to insecticides. Pest Manag. Sci. 58, 920–927. Espinosa, P.J., Bielza, P., Contreras, J., Lacasa, A., 2002b. Insecticide resistance in field populations of Frankliniella occidentalis (Pergande) in Murcia (south-east Spain). Pest Manag. Sci. 58, 967–971. Espinosa, P.J., Contreras, J., Quinto, V., Grávalos, C., Fernández, E., Bielza, P., 2005. Metabolic mechanisms of insecticide resistance in the western flower thrips, Frankliniella occidentalis (Pergande). Pest Manag. Sci. 61, 1009–1015.

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