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Neonicotinoid insecticide resistance in the field populations of Sogatella furcifera (Horváth) in Central China from 2011 to 2015
Journal of Asia-Pacific Entomology 20 (2017) 955–958
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Short Communication
Neonicotinoid insecticide resistance in the field populations of Sogatella furcifera (Horváth) in Central China from 2011 to 2015
MARK
Xiaolei Zhang1, Xun Liao1, Kaikai Mao, Peng Yang, Dongyang Li, Ehsan Ali, Hu Wan, Jianhong Li⁎ Hubei Insect Resources Utilization and Sustainable Pest Management Key Laboratory, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, PR China
A R T I C L E I N F O
A B S T R A C T
Keywords: Sogatella furcifera Resistance monitoring Imidacloprid Thiamethoxam Acetamiprid Nitenpyram Clothianidin Dinotefuran
The whitebacked planthopper Sogatella furcifera (Horváth) is an important pest of rice throughout Asia. Application of chemical insecticide is the main approach to suppress the field populations of S. furcifera. In this study, neonicotinoid insecticide resistance in field populations of S. furcifera were evaluated. The results showed that some field populations of S. furcifera had developed moderate level of resistance to imidacloprid (RR = 1.1–16.4), thiamethoxam (RR = 0.8–14.9), dinotefuran (RR = 1.2–16.6) and acetamiprid (RR = 3.3–12.2), low level of resistance to nitenpyram (RR = 1.1–9.5) and clothianidin (RR = 1.3–8.7) in Central China. Moreover, there were an increasing trend in neonicotinoid insecticide resistance in the period 2011–2015. The results of current study may form the basis to identify and evaluate the resistance tendency of S. furcifera against neonicotinoid insecticides, which could make effective management recommendations to avoid further development of insecticide resistance in S. furcifera.
Introduction The white-back planthopper (WBPH), Sogatella furcifera (Horváth) (Homoptera: Delphacidae) is a serious insect pest in rice-growing countries of Asia (Catindig et al., 2009; Yadav and Chander, 2010; Zhang et al., 2011; Selvaraj et al., 2012; Cheng, 2015; Horgan et al., 2016). Chemical insecticide spraying was the main approach for efficiently controlling S. furcifera in the paddy field (Catindig et al., 2009; Liu et al., 2015). To date, S. furcifera has developed different levels of resistance to organophosphorus, carbamate, phenylpyrazole, neonicotinoid, pyrethroid, and insect growth regulator insecticides (Endo et al., 1988; Matsumura et al., 2008; Tang et al., 2010; Su et al., 2013; Matsumura et al., 2014; Zhang et al., 2014; Liu et al., 2015; Mu et al., 2016; Zhang et al., 2016a). At present, neonicotinoid insecticides including imidacloprid, thiamethoxam, nitenpyram are the most frequently used insecticides for managing rice planthopper in China for > 10 years (Su et al., 2013; Zhang et al., 2014), specifically, imidacloprid was used for rice planthopper control in the early 1990s, and thiamethoxam and nitenpyram become primary alternative insecticides to control rice planthopper since 2006. And clothianidin, dinotefuran and acetamiprid have been registered for planthoppers control in recent years. Thus, it is crucial point to understand the current susceptibility levels of S. furcifera to these insecticides in the field. The purpose of the
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1
present study was to assess the current status of resistance in S. furcifera to neonicotinoid insecticides, such as imidacloprid, thiamethoxam, nitenpyram, acetamiprid, clothianidin, and dinotefuran. Materials and methods Insect populations Twenty-seven field populations of S. furcifera were collected from rice paddy field of Gongan, Tongcheng, Wuxue, Xiaogan, Zaoyang, Xinyang, and Changsha in Central China from 2011 to 2015 (Table 1). The field collected S. furcifera were reared on rice seedlings (TN1) and mated, the third-instar nymphs of the first (F1) generation and the second (F2) generation were used for bioassay. Insecticides and bioassay The insecticides used in this study were technical grade compounds. Imidacloprid (96%) were supplied by Hebei VeYong Bio-Chemical Co., Ltd. Thiamethoxam (95%), dinotefuran (91%), nitenpyram (96%) and clothianidin (96%) were supplied by Hubei Kangbaotai Fine-Chemicals Co., Ltd. Acetamiprid (98.5%) was supplied by Shandong Sino-Agri United Biotechnology Co., Ltd. The technical compounds were
Corresponding author. E-mail address: [email protected] (J. Li). These authors contributed equally to this paper.
http://dx.doi.org/10.1016/j.aspen.2017.07.004 Received 23 February 2017; Received in revised form 3 July 2017; Accepted 11 July 2017 Available online 12 July 2017 1226-8615/ © 2017 Published by Elsevier B.V. on behalf of Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society.
Journal of Asia-Pacific Entomology 20 (2017) 955–958
X. Zhang et al.
Table 1 Sampling sites, collection dates and developmental stages of S. furcifera collected from rice paddy fields of Central China from 2011 to 2015. Populations
Locations
Collection date
Site
GA-2011 GA-2012 GA-2013 GA-2014 GA-2015 CS-2015 WX-2011 WX-2012 WX-2013 WX-2014 WX-2015 TC-2011 TC-2012 TC-2013 TC-2014 TC-2015 ZY-2011 ZY-2012 ZY-2013 ZY-2014 ZY-2015 XG-2011 XG-2012 XG-2013 XG-2014 XG-2015 XY-2015
Gongan, Hubei Gongan, Hubei Gongan, Hubei Gongan, Hubei Gongan, Hubei Changsha, Hunan Wuxue, Hubei Wuxue, Hubei Wuxue, Hubei Wuxue, Hubei Wuxue, Hubei Tongcheng, Hubei Tongcheng, Hubei Tongcheng, Hubei Tongcheng, Hubei Tongcheng, Hubei Zaoyang, Hubei Zaoyang, Hubei Zaoyang, Hubei Zaoyang, Hubei Zaoyang, Hubei Xiaogan, Hubei Xiaogan, Hubei Xiaogan, Bubei Xiaogan, Hubei Xiaogan, Hubei Xinyang, Henan
Jul 12, 2011 Jul 22, 2012 Aug 1, 2013 Aug 3, 2014 Aug 2, 2015 Jul 29, 2015 Aug 10, 2011 Aug 18, 2012 Jul 28, 2013 Aug 21, 2014 Aug 1, 2015 Aug 5, 2011 Aug 4, 2012 Jul 30, 2013 Aug 15, 2014 Aug 8, 2015 Jul 23, 2011 Aug 7, 2012 Aug 12, 2013 Aug 3, 2014 Jul 27, 2015 Jul 29, 2011 Aug 13, 2012 Aug 11, 2013 Aug 7, 2014 Aug 9, 2015 Aug 11, 2015
30.05° 30.05° 30.05° 30.05° 30.05° 20.18° 30.11° 30.11° 30.11° 30.11° 30.11° 29.26° 29.26° 29.26° 29.26° 29.26° 31.98° 31.98° 31.98° 31.98° 31.98° 31.27° 31.27° 31.27° 31.27° 31.27° 32.25°
Insect stage N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N,
112.19° 112.19° 112.19° 112.19° 112.19° 112.57° 115.59° 115.59° 115.59° 115.59° 115.59° 113.84° 113.84° 113.84° 113.84° 113.84° 112.76° 112.76° 112.76° 112.76° 112.76° 113.84° 113.84° 113.84° 113.84° 113.84° 113.88°
E E E E E E E E E E E E E E E E E E E E E E E E E E E
Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph
and and and and and and and and and and and and and and and and and and and and and and and and and and and
adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult
Table 2 The resistance levels of S. furcifera field populations to neonicotinoid insecticides. Populations
GA-2011 GA-2012 GA-2013 GA-2014 GA-2015 WX-2011 WX-2012 WX-2013 WX-2014 WX-2015 TC-2011 TC-2012 TC-2013 TC-2014 TC-2015 ZY-2011 ZY-2012 ZY-2013 ZY-2014 ZY-2015 XG-2011 XG-2012 XG-2013 XG-2014 XG-2015 XY-2015 CS-2015
Imidacloprid
Nitenpyram
Thiamethoxam
Dinotefuran
Clothianidin
Acetamiprid
LC50 (mg/L) (95% CI)
RR
LC50 (mg/L) (95% CI)
RR
LC50 (mg/L) (95% CI)
RR
LC50 (mg/L) (95% CI)
RR
LC50 (mg/L) (95% CI)
RR
LC50 (mg/L) (95% CI)
RR
0.22 0.25 0.39 0.73 0.33 0.27 0.33 0.51 1.10 0.51 0.12 0.19 0.40 0.88 0.81 0.14 0.22 0.67 0.65 1.79 0.24 0.35 0.99 0.45 1.25 1.51 0.54
2.0 2.3 3.6 6.7 3.0 2.5 3.0 4.7 10.1 4.7 1.1 1.7 3.7 8.1 7.4 1.3 2.0 6.2 6.0 16.4 2.2 3.2 9.1 4.1 11.5 13.9 5.0
0.57 0.41 0.22 0.48 0.40 0.24 0.21 0.14 0.68 0.51 0.24 0.17 0.50 0.66 0.58 0.31 0.26 0.25 0.30 0.88 0.28 0.19 0.51 0.73 1.05 0.67 1.23
4.4 3.2 1.7 3.7 3.1 1.9 1.6 1.1 5.2 3.9 1.9 1.3 3.9 5.1 4.5 2.4 2.0 1.9 2.3 6.8 2.2 1.5 3.9 5.6 8.1 5.2 9.5
0.36 0.18 0.39 0.35 1.23 0.25 0.20 0.22 0.53 1.38 0.20 0.22 0.49 0.51 1.10 0.13 0.15 0.29 0.70 0.60 0.08 0.20 0.36 0.80 1.43 0.87 1.04
3.8 1.9 4.1 3.7 12.8 2.6 2.1 2.3 5.5 14.4 2.1 2.3 5.1 5.3 11.5 1.4 1.6 3.0 7.3 6.3 0.8 2.1 3.8 8.3 14.9 9.1 10.8
0.63 0.54 0.20 0.64 1.17 0.42 0.50 0.14 0.57 0.86 0.60 0.29 0.24 0.34 1.99 0.48 0.59 0.17 1.20 1.54 0.55 0.67 0.30 0.82 1.17 0.93 1.37
5.3 4.5 1.7 5.3 9.8 3.5 4.2 1.2 4.8 7.2 5.0 2.4 2.0 2.8 16.6 4.0 4.9 1.4 10.0 12.8 4.6 5.6 2.5 6.8 9.8 7.8 11.4
0.79 0.57 0.38 0.80 0.64 0.34 0.26 0.69 0.38 0.44 0.30 0.37 0.41 0.34 0.79 0.48 0.39 0.20 0.41 0.79 0.72 0.62 0.31 0.76 0.83 0.74 1.31
5.3 3.8 2.5 5.3 4.3 2.3 1.7 4.6 2.5 2.9 2.0 2.5 2.7 2.3 5.3 3.2 2.6 1.3 2.7 5.3 4.8 4.1 2.1 5.1 5.5 4.9 8.7
5.58 2.11 4.46 6.34 – 5.42 1.71 2.09 4.15 – 4.29 5.70 3.22 4.25 – 2.90 4.40 2.96 5.66 – 2.93 4.35 3.40 3.59 – – –
(3.95–7.80) (1.36–3.32) (3.19–6.15) (4.31–9.22)
10.7 4.1 8.6 12.2
(4.47–6.57) (1.38–2.10) (1.30–3.04) (3.46–4.96)
10.4 3.3 4.0 8.0
(3.88–4.74) (4.81–6.74) (2.18–4.53) (3.63–4.98)
8.3 11.0 6.2 8.2
(2.45–3.40) (3.37–5.73) (1.95–4.22) (3.63–8.72)
5.6 8.5 5.7 10.9
(2.35–3.67) (3.25–5.77) (2.36–4.71) (2.06–5.97)
5.6 8.4 6.5 6.9
(0.16–0.29) (0.16–0.36) (0.28–0.55) (0.49–1.22) (0.16–0.52) (0.21–0.36) (0.22–0.57) (0.35–0.72) (0.67–2.23) (0.29–0.74) (0.09–0.17) (0.12–0.27) (0.26–0.57) (0.59–1.58) (0.55–1.13) (0.11–0.21) (0.15–0.32) (0.47–0.93) (0.42–1.10) (1.09–4.27) (0.18–0.31) (0.25–0.47) (0.68–1.50) (0.31–0.70) (0.76–2.00) (1.17–1.96) (0.21–0.93)
(0.46–0.70) (0.26–0.69 (0.15–0.31) (0.34–0.74) (0.28–0.56) (0.19–0.29) (0.14–0.33) (0.08–0.22) (0.43–1.37) (0.45–0.58) (0.17–0.33) (0.11–0.26) (0.35–0.72) (0.44–1.01) (0.35–0.88) (0.22–0.41) (0.18–0.39) (0.17–0.36) (0.21–0.45) (0.49–1.36) (0.20–0.36) (0.14–0.26) (0.32–0.79) (0.45–1.46) (0.47–1.82) (0.50–0.87) (0.59–2.57)
(0.26–0.49) (0.12–0.26) (0.29–0.52) (0.25–0.52) (0.59–2.57) (0.15–0.39) (0.15–0.27) (0.14–0.32) (0.37–0.77) (1.17–1.62) (0.13–0.29) (0.15–0.33) (0.35–0.69) (0.36–0.73) (0.66–1.69) (0.09–0.19) (0.10–0.21) (0.18–0.41) (0.50–1.02) (0.02–1.13) (0.05–0.13) (0.14–0.29) (0.25–0.51) (0.53–1.55) (1.07–1.88) (0.72–1.01) (0.92–1.17)
(0.54–0.74) (0.43–0.66) (0.14–0.28) (0.56–0.73) (0.50–2.25) (0.39–0.46) (0.35–0.69) (0.08–0.23) (0.48–0.66) (0.56–1.29) (0.30–0.95) (0.26–0.33) (0.16–0.34) (0.31–0.38) (0.69–6.42) (0.42–0.53) (0.48–0.72) (0.10–0.26) (0.99–1.43) (1.26–1.87) (0.43–0.72) (0.60–0.74) (0.21–0.42) (0.63–1.04) (0.72–1.70) (0.41–1.56) (1.15–1.61)
(0.70–0.87) (0.42–0.76) (0.27–0.52) (0.69–0.93) (0.51–0.78) (0.28–0.40) (0.20–0.33) (0.46–1.05) (0.33–0.44) (0.22–0.76) (0.24–0.37) (0.27–0.48) (0.27–0.66) (0.30–0.38) (0.66–0.95) (0.42–0.55) (0.27–0.54) (0.13–0.29) (0.34–0.49) (0.55–1.24) (0.67–0.77) (0.51–0.74) (0.21–0.45) (0.54–1.04) (0.25–1.44) (0.67–0.81) (0.78–2.50)
appropriate insecticide solutions for 30 s and then air-dried at room temperature for about an hour and a half. The rice stems with roots were wrapped with water-impregnated cotton and put into 500-mL plastic cups. The third instar nymphs were collected with a homemade aspirating device, and twenty nymphs were transferred onto rice stems into a plastic cup for each replicate. There were three replicates for each dose (concentration). Control rice stems were treated with 0.1% Triton
dissolved in acetone as stock solution and then diluted in a series of 6–9 concentration gradients with water containing 0.1% of Triton X-100. Rice-stem dipping method (Zhang et al., 2016a) was used to monitor insecticide resistance of S. furcifera. Briefly, rice plants at the tillering to early booting stage were pulled out from the soil, washed thoroughly, cut into an approximately 10 cm long rice stem with roots and air-dried. Three rice stems were grouped together and dipped into 956
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thiamethoxam, nitenpyram and dinotefuran (Fig. 1, Table 2). Neonicotinoid insecticides have been used widely and intensively to control rice planthopper since the early 1990s in China, and also played an important role in chemical control of insect pest (Wang et al., 2008; Wang et al., 2009; Zhang et al., 2014; Zhang et al., 2016a, 2016b). The introduction of the first neonicotinoid insecticide imidacloprid in 1995 exhibited excellent efficacy for the control of rice hopper in China. Currently, it was only applied for controlling S. furcifera in the early stage of rice since 2005 in China. The recent report revealed that field populations of S. furcifera developed moderate level of resistance to imidacloprid in Guangxi, Fujian, Hunan, Jiangsu, Anhui and Sichuan provinces in China (Su et al., 2013; Zhang et al., 2014). The present survey of imidacloprid resistance in S. furcifera showed similar results to that reported by Su et al. (2013). And the field populations of S. furcifera from China only showed low level of resistance to thiamethoxam (Su et al., 2013), however, we found that some field populations have developed moderate level of resistance to the same insecticide in Central China during 2011 to 2015. In the study, low level of resistance to nitenpyram was also detected, which may be the results of increased application intensity of this insecticide in S. furcifera control in recent years. Similar situations of increased resistance due to intensive applications of imidacloprid and buprofezin have also been reported in the brown planthopper Nilaparvata lugens (Wang et al., 2008; Wang et al., 2009; Zhang et al., 2016b). Though acetamiprid, dinotefuran, and clothianidin have not been used for the control of rice planthopper, we found that some field populations of S. furcifera had developed moderate level of resistance to dinotefuran and acetamiprid, and low level of resistance to clothianidin, and dinotefuran resistance increased obviously in 2015 compared with that from 2011 to 2014. This may partially because of the cross-resistance between dinotefuran and other insecticide, and application of this insecticide in Southeast Asian countries (Wang et al., 2008; Mu et al., 2016). In addition, resistance to clothianidin in 2015 was obviously high than that from 2011 to 2014, but this increase may result from cross-resistance with other insecticide of different mode of action. Resistance to acetamiprid did not increase as obviously as other insecticides, the possible explanation for this is that these insecticides have not been used extensively for
X-100 water solution only. All treatments were maintained at a temperature of 27 ± 1 °C and 70%–80% relative humidity with a 16-h light/8-h dark photoperiod. Mortality was assessed after exposure to these insecticides for 96 h. The nymphs were considered dead if they were unable to move after a gentle prodding with a fine brush. Data analysis The LC50 values, 95% confidence interval were calculated by Probit analysis via DPS (3.01). The LC50 value of the susceptible baseline for imidacloprid, thiamethoxam, nitenpyram, dinotefuran, clothianidin and acetamiprid were 0.109 (0.057–0.172), 0.096 (0.040–0.169), 0.13 (0.10–0.18), 0.12 (0.08–0.17), 0.15 (0.09–0.21) and 0.52 (0.19–0.82) mg/L respectively (Zhang et al., 2013; Zhang et al., 2016a). Classification of resistance level was according to Shao et al. (2013), resistance with a RR ≤ 5-fold was classified as susceptible, RR = 5–10-fold as low resistance level, RR = 10–100-fold as medium resistance level and RR > 100-fold as high resistance level. Results and discussion The results showed that field populations of S. furcifera had developed different levels of resistance to all tested neonicotinoid insecticides. More specifically, approximately 85.0% of field populations of S. furcifera exhibited low to moderate levels of resistance to acetamiprid (Resistance Ratio, RR = 5.6–12.2), while other populations remained susceptible to this insecticide (RR = 3.3–4.1) (Table 2). Whereas, most field populations of S. furcifera (55.6% − 74.1%) still maintained susceptible (RR = 0.8–5.0) to thiamethoxam (55.6%), dinotefuran (55.6%), imidacloprid (63.0%), nitenpyram (74.1%), clothianidin (74.1%) respectively, only 11.1% − 25.0% of field populations exhibited moderate level of resistance to imidacloprid (14.8%), thiamethoxam (18.5%), dinotefuran (11.1%) and acetamiprid (25.0%) with RR ranging from 10.1 to 16.6, the other populations showed low level of resistance to these insecticides (RR = 5.1–10.0) (Table 2). Further, there were an increasing trend in neonicotinoid insecticide resistance in the period 2011–2015, including imidacloprid,
Fig. 1. Comparison of resistance levels of Sogatella furcifera field populations collected in Central China in the period 2011–2015 to 6 insecticides. The scatter diagram of the resistance ratios of different populations of S. furcifera to different insecticides. Red horizontal lines across the scatter diagram represent the mean value of the resistance ratio of the different populations. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
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controlling rice planthopper in China. Fast development of neonicotiniod insecticides resistance indicated that integrated pest management (IPM), including biological control, cultural practice (good irrigation practices, resistant rice varieties, reduction of nitrogen fertilizer and so on), should be implemented along with insecticide application in controlling this pest. However, the application of chemical insecticides remains a primary tool for WBPH control currently. Mode of action rotation is one of the corner stones of modern resistance management strategies and the IRAC mode of action classification helps to make correct decisions on how to alternate different chemical classes of insecticides (Sparks and Nauen, 2015), thus, chemical insecticides belonging to mode of action classes other than nicotinic acetylcholine receptor modulators should be used in a rational manner in order to safeguard their long term efficacy and utility in controlling this pest. Competing interests The authors have declared that no competing interests exist. Acknowledgements This work was supported by the Special Fund for Agro-Scientific Research in the Public Interest (201203038 and 201503107). References Catindig, J.L.A., Arida, G.S., Baehaki, S.E., Bentur, J.S., Cuong, L.Q., Norowi, M., Rattanakarn, W., Sriratanasak, W., Xia, J., Lu, Z., 2009. Situation of planthoppers in Asia. In: Heong, K.L., Hardy, B. (Eds.), Planthoppers: New Threats to the Sustainability of Intensive Rice Production Systems in Asia. International Rice Research Institute, Philippines, pp. 191–220. Cheng, J.A., 2015. Rice planthoppers in the past half century in China. In: Heong, K.L., Cheng, J.A., Escalada, M.M. (Eds.), Rice Planthopper: Ecology, Management. Socio Economics and Policy. Zhejiang University Press, Hangzhou and Springer Science Publisher, London, pp. 1–32. Endo, S., Nagata, T., Kawabe, S., Kazano, H., 1988. Changes of insecticide susceptibility of the white backed planthopper Sogatella furcifera Horváth (Homoptera: delphacidae) and the brown planthopper Nilaparvata lugens Stål (Homoptera: delphacidae). Appl. Entomol. Zool. 23, 417–421. Horgan, F.G., Srinivasan, T.S., Naik, B.S., Ramal, A.F., Bernal, C.C., Almazan, M.L.P., 2016. Effects of nitrogen on egg-laying inhibition and ovicidal response in planthopper-resistant rice varieties. Crop. Prot. 89, 223–230. Liu, Z.W., Wu, J.C., Zhang, Y.X., Liu, F., Xu, J.X., Bao, H.B., 2015. Mechanism of rice
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Journal of Asia-Pacific Entomology journal homepage: www.elsevier.com/locate/jape
Short Communication
Neonicotinoid insecticide resistance in the field populations of Sogatella furcifera (Horváth) in Central China from 2011 to 2015
MARK
Xiaolei Zhang1, Xun Liao1, Kaikai Mao, Peng Yang, Dongyang Li, Ehsan Ali, Hu Wan, Jianhong Li⁎ Hubei Insect Resources Utilization and Sustainable Pest Management Key Laboratory, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, PR China
A R T I C L E I N F O
A B S T R A C T
Keywords: Sogatella furcifera Resistance monitoring Imidacloprid Thiamethoxam Acetamiprid Nitenpyram Clothianidin Dinotefuran
The whitebacked planthopper Sogatella furcifera (Horváth) is an important pest of rice throughout Asia. Application of chemical insecticide is the main approach to suppress the field populations of S. furcifera. In this study, neonicotinoid insecticide resistance in field populations of S. furcifera were evaluated. The results showed that some field populations of S. furcifera had developed moderate level of resistance to imidacloprid (RR = 1.1–16.4), thiamethoxam (RR = 0.8–14.9), dinotefuran (RR = 1.2–16.6) and acetamiprid (RR = 3.3–12.2), low level of resistance to nitenpyram (RR = 1.1–9.5) and clothianidin (RR = 1.3–8.7) in Central China. Moreover, there were an increasing trend in neonicotinoid insecticide resistance in the period 2011–2015. The results of current study may form the basis to identify and evaluate the resistance tendency of S. furcifera against neonicotinoid insecticides, which could make effective management recommendations to avoid further development of insecticide resistance in S. furcifera.
Introduction The white-back planthopper (WBPH), Sogatella furcifera (Horváth) (Homoptera: Delphacidae) is a serious insect pest in rice-growing countries of Asia (Catindig et al., 2009; Yadav and Chander, 2010; Zhang et al., 2011; Selvaraj et al., 2012; Cheng, 2015; Horgan et al., 2016). Chemical insecticide spraying was the main approach for efficiently controlling S. furcifera in the paddy field (Catindig et al., 2009; Liu et al., 2015). To date, S. furcifera has developed different levels of resistance to organophosphorus, carbamate, phenylpyrazole, neonicotinoid, pyrethroid, and insect growth regulator insecticides (Endo et al., 1988; Matsumura et al., 2008; Tang et al., 2010; Su et al., 2013; Matsumura et al., 2014; Zhang et al., 2014; Liu et al., 2015; Mu et al., 2016; Zhang et al., 2016a). At present, neonicotinoid insecticides including imidacloprid, thiamethoxam, nitenpyram are the most frequently used insecticides for managing rice planthopper in China for > 10 years (Su et al., 2013; Zhang et al., 2014), specifically, imidacloprid was used for rice planthopper control in the early 1990s, and thiamethoxam and nitenpyram become primary alternative insecticides to control rice planthopper since 2006. And clothianidin, dinotefuran and acetamiprid have been registered for planthoppers control in recent years. Thus, it is crucial point to understand the current susceptibility levels of S. furcifera to these insecticides in the field. The purpose of the
⁎
1
present study was to assess the current status of resistance in S. furcifera to neonicotinoid insecticides, such as imidacloprid, thiamethoxam, nitenpyram, acetamiprid, clothianidin, and dinotefuran. Materials and methods Insect populations Twenty-seven field populations of S. furcifera were collected from rice paddy field of Gongan, Tongcheng, Wuxue, Xiaogan, Zaoyang, Xinyang, and Changsha in Central China from 2011 to 2015 (Table 1). The field collected S. furcifera were reared on rice seedlings (TN1) and mated, the third-instar nymphs of the first (F1) generation and the second (F2) generation were used for bioassay. Insecticides and bioassay The insecticides used in this study were technical grade compounds. Imidacloprid (96%) were supplied by Hebei VeYong Bio-Chemical Co., Ltd. Thiamethoxam (95%), dinotefuran (91%), nitenpyram (96%) and clothianidin (96%) were supplied by Hubei Kangbaotai Fine-Chemicals Co., Ltd. Acetamiprid (98.5%) was supplied by Shandong Sino-Agri United Biotechnology Co., Ltd. The technical compounds were
Corresponding author. E-mail address: [email protected] (J. Li). These authors contributed equally to this paper.
http://dx.doi.org/10.1016/j.aspen.2017.07.004 Received 23 February 2017; Received in revised form 3 July 2017; Accepted 11 July 2017 Available online 12 July 2017 1226-8615/ © 2017 Published by Elsevier B.V. on behalf of Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society.
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Table 1 Sampling sites, collection dates and developmental stages of S. furcifera collected from rice paddy fields of Central China from 2011 to 2015. Populations
Locations
Collection date
Site
GA-2011 GA-2012 GA-2013 GA-2014 GA-2015 CS-2015 WX-2011 WX-2012 WX-2013 WX-2014 WX-2015 TC-2011 TC-2012 TC-2013 TC-2014 TC-2015 ZY-2011 ZY-2012 ZY-2013 ZY-2014 ZY-2015 XG-2011 XG-2012 XG-2013 XG-2014 XG-2015 XY-2015
Gongan, Hubei Gongan, Hubei Gongan, Hubei Gongan, Hubei Gongan, Hubei Changsha, Hunan Wuxue, Hubei Wuxue, Hubei Wuxue, Hubei Wuxue, Hubei Wuxue, Hubei Tongcheng, Hubei Tongcheng, Hubei Tongcheng, Hubei Tongcheng, Hubei Tongcheng, Hubei Zaoyang, Hubei Zaoyang, Hubei Zaoyang, Hubei Zaoyang, Hubei Zaoyang, Hubei Xiaogan, Hubei Xiaogan, Hubei Xiaogan, Bubei Xiaogan, Hubei Xiaogan, Hubei Xinyang, Henan
Jul 12, 2011 Jul 22, 2012 Aug 1, 2013 Aug 3, 2014 Aug 2, 2015 Jul 29, 2015 Aug 10, 2011 Aug 18, 2012 Jul 28, 2013 Aug 21, 2014 Aug 1, 2015 Aug 5, 2011 Aug 4, 2012 Jul 30, 2013 Aug 15, 2014 Aug 8, 2015 Jul 23, 2011 Aug 7, 2012 Aug 12, 2013 Aug 3, 2014 Jul 27, 2015 Jul 29, 2011 Aug 13, 2012 Aug 11, 2013 Aug 7, 2014 Aug 9, 2015 Aug 11, 2015
30.05° 30.05° 30.05° 30.05° 30.05° 20.18° 30.11° 30.11° 30.11° 30.11° 30.11° 29.26° 29.26° 29.26° 29.26° 29.26° 31.98° 31.98° 31.98° 31.98° 31.98° 31.27° 31.27° 31.27° 31.27° 31.27° 32.25°
Insect stage N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N, N,
112.19° 112.19° 112.19° 112.19° 112.19° 112.57° 115.59° 115.59° 115.59° 115.59° 115.59° 113.84° 113.84° 113.84° 113.84° 113.84° 112.76° 112.76° 112.76° 112.76° 112.76° 113.84° 113.84° 113.84° 113.84° 113.84° 113.88°
E E E E E E E E E E E E E E E E E E E E E E E E E E E
Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph Nymph
and and and and and and and and and and and and and and and and and and and and and and and and and and and
adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult adult
Table 2 The resistance levels of S. furcifera field populations to neonicotinoid insecticides. Populations
GA-2011 GA-2012 GA-2013 GA-2014 GA-2015 WX-2011 WX-2012 WX-2013 WX-2014 WX-2015 TC-2011 TC-2012 TC-2013 TC-2014 TC-2015 ZY-2011 ZY-2012 ZY-2013 ZY-2014 ZY-2015 XG-2011 XG-2012 XG-2013 XG-2014 XG-2015 XY-2015 CS-2015
Imidacloprid
Nitenpyram
Thiamethoxam
Dinotefuran
Clothianidin
Acetamiprid
LC50 (mg/L) (95% CI)
RR
LC50 (mg/L) (95% CI)
RR
LC50 (mg/L) (95% CI)
RR
LC50 (mg/L) (95% CI)
RR
LC50 (mg/L) (95% CI)
RR
LC50 (mg/L) (95% CI)
RR
0.22 0.25 0.39 0.73 0.33 0.27 0.33 0.51 1.10 0.51 0.12 0.19 0.40 0.88 0.81 0.14 0.22 0.67 0.65 1.79 0.24 0.35 0.99 0.45 1.25 1.51 0.54
2.0 2.3 3.6 6.7 3.0 2.5 3.0 4.7 10.1 4.7 1.1 1.7 3.7 8.1 7.4 1.3 2.0 6.2 6.0 16.4 2.2 3.2 9.1 4.1 11.5 13.9 5.0
0.57 0.41 0.22 0.48 0.40 0.24 0.21 0.14 0.68 0.51 0.24 0.17 0.50 0.66 0.58 0.31 0.26 0.25 0.30 0.88 0.28 0.19 0.51 0.73 1.05 0.67 1.23
4.4 3.2 1.7 3.7 3.1 1.9 1.6 1.1 5.2 3.9 1.9 1.3 3.9 5.1 4.5 2.4 2.0 1.9 2.3 6.8 2.2 1.5 3.9 5.6 8.1 5.2 9.5
0.36 0.18 0.39 0.35 1.23 0.25 0.20 0.22 0.53 1.38 0.20 0.22 0.49 0.51 1.10 0.13 0.15 0.29 0.70 0.60 0.08 0.20 0.36 0.80 1.43 0.87 1.04
3.8 1.9 4.1 3.7 12.8 2.6 2.1 2.3 5.5 14.4 2.1 2.3 5.1 5.3 11.5 1.4 1.6 3.0 7.3 6.3 0.8 2.1 3.8 8.3 14.9 9.1 10.8
0.63 0.54 0.20 0.64 1.17 0.42 0.50 0.14 0.57 0.86 0.60 0.29 0.24 0.34 1.99 0.48 0.59 0.17 1.20 1.54 0.55 0.67 0.30 0.82 1.17 0.93 1.37
5.3 4.5 1.7 5.3 9.8 3.5 4.2 1.2 4.8 7.2 5.0 2.4 2.0 2.8 16.6 4.0 4.9 1.4 10.0 12.8 4.6 5.6 2.5 6.8 9.8 7.8 11.4
0.79 0.57 0.38 0.80 0.64 0.34 0.26 0.69 0.38 0.44 0.30 0.37 0.41 0.34 0.79 0.48 0.39 0.20 0.41 0.79 0.72 0.62 0.31 0.76 0.83 0.74 1.31
5.3 3.8 2.5 5.3 4.3 2.3 1.7 4.6 2.5 2.9 2.0 2.5 2.7 2.3 5.3 3.2 2.6 1.3 2.7 5.3 4.8 4.1 2.1 5.1 5.5 4.9 8.7
5.58 2.11 4.46 6.34 – 5.42 1.71 2.09 4.15 – 4.29 5.70 3.22 4.25 – 2.90 4.40 2.96 5.66 – 2.93 4.35 3.40 3.59 – – –
(3.95–7.80) (1.36–3.32) (3.19–6.15) (4.31–9.22)
10.7 4.1 8.6 12.2
(4.47–6.57) (1.38–2.10) (1.30–3.04) (3.46–4.96)
10.4 3.3 4.0 8.0
(3.88–4.74) (4.81–6.74) (2.18–4.53) (3.63–4.98)
8.3 11.0 6.2 8.2
(2.45–3.40) (3.37–5.73) (1.95–4.22) (3.63–8.72)
5.6 8.5 5.7 10.9
(2.35–3.67) (3.25–5.77) (2.36–4.71) (2.06–5.97)
5.6 8.4 6.5 6.9
(0.16–0.29) (0.16–0.36) (0.28–0.55) (0.49–1.22) (0.16–0.52) (0.21–0.36) (0.22–0.57) (0.35–0.72) (0.67–2.23) (0.29–0.74) (0.09–0.17) (0.12–0.27) (0.26–0.57) (0.59–1.58) (0.55–1.13) (0.11–0.21) (0.15–0.32) (0.47–0.93) (0.42–1.10) (1.09–4.27) (0.18–0.31) (0.25–0.47) (0.68–1.50) (0.31–0.70) (0.76–2.00) (1.17–1.96) (0.21–0.93)
(0.46–0.70) (0.26–0.69 (0.15–0.31) (0.34–0.74) (0.28–0.56) (0.19–0.29) (0.14–0.33) (0.08–0.22) (0.43–1.37) (0.45–0.58) (0.17–0.33) (0.11–0.26) (0.35–0.72) (0.44–1.01) (0.35–0.88) (0.22–0.41) (0.18–0.39) (0.17–0.36) (0.21–0.45) (0.49–1.36) (0.20–0.36) (0.14–0.26) (0.32–0.79) (0.45–1.46) (0.47–1.82) (0.50–0.87) (0.59–2.57)
(0.26–0.49) (0.12–0.26) (0.29–0.52) (0.25–0.52) (0.59–2.57) (0.15–0.39) (0.15–0.27) (0.14–0.32) (0.37–0.77) (1.17–1.62) (0.13–0.29) (0.15–0.33) (0.35–0.69) (0.36–0.73) (0.66–1.69) (0.09–0.19) (0.10–0.21) (0.18–0.41) (0.50–1.02) (0.02–1.13) (0.05–0.13) (0.14–0.29) (0.25–0.51) (0.53–1.55) (1.07–1.88) (0.72–1.01) (0.92–1.17)
(0.54–0.74) (0.43–0.66) (0.14–0.28) (0.56–0.73) (0.50–2.25) (0.39–0.46) (0.35–0.69) (0.08–0.23) (0.48–0.66) (0.56–1.29) (0.30–0.95) (0.26–0.33) (0.16–0.34) (0.31–0.38) (0.69–6.42) (0.42–0.53) (0.48–0.72) (0.10–0.26) (0.99–1.43) (1.26–1.87) (0.43–0.72) (0.60–0.74) (0.21–0.42) (0.63–1.04) (0.72–1.70) (0.41–1.56) (1.15–1.61)
(0.70–0.87) (0.42–0.76) (0.27–0.52) (0.69–0.93) (0.51–0.78) (0.28–0.40) (0.20–0.33) (0.46–1.05) (0.33–0.44) (0.22–0.76) (0.24–0.37) (0.27–0.48) (0.27–0.66) (0.30–0.38) (0.66–0.95) (0.42–0.55) (0.27–0.54) (0.13–0.29) (0.34–0.49) (0.55–1.24) (0.67–0.77) (0.51–0.74) (0.21–0.45) (0.54–1.04) (0.25–1.44) (0.67–0.81) (0.78–2.50)
appropriate insecticide solutions for 30 s and then air-dried at room temperature for about an hour and a half. The rice stems with roots were wrapped with water-impregnated cotton and put into 500-mL plastic cups. The third instar nymphs were collected with a homemade aspirating device, and twenty nymphs were transferred onto rice stems into a plastic cup for each replicate. There were three replicates for each dose (concentration). Control rice stems were treated with 0.1% Triton
dissolved in acetone as stock solution and then diluted in a series of 6–9 concentration gradients with water containing 0.1% of Triton X-100. Rice-stem dipping method (Zhang et al., 2016a) was used to monitor insecticide resistance of S. furcifera. Briefly, rice plants at the tillering to early booting stage were pulled out from the soil, washed thoroughly, cut into an approximately 10 cm long rice stem with roots and air-dried. Three rice stems were grouped together and dipped into 956
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thiamethoxam, nitenpyram and dinotefuran (Fig. 1, Table 2). Neonicotinoid insecticides have been used widely and intensively to control rice planthopper since the early 1990s in China, and also played an important role in chemical control of insect pest (Wang et al., 2008; Wang et al., 2009; Zhang et al., 2014; Zhang et al., 2016a, 2016b). The introduction of the first neonicotinoid insecticide imidacloprid in 1995 exhibited excellent efficacy for the control of rice hopper in China. Currently, it was only applied for controlling S. furcifera in the early stage of rice since 2005 in China. The recent report revealed that field populations of S. furcifera developed moderate level of resistance to imidacloprid in Guangxi, Fujian, Hunan, Jiangsu, Anhui and Sichuan provinces in China (Su et al., 2013; Zhang et al., 2014). The present survey of imidacloprid resistance in S. furcifera showed similar results to that reported by Su et al. (2013). And the field populations of S. furcifera from China only showed low level of resistance to thiamethoxam (Su et al., 2013), however, we found that some field populations have developed moderate level of resistance to the same insecticide in Central China during 2011 to 2015. In the study, low level of resistance to nitenpyram was also detected, which may be the results of increased application intensity of this insecticide in S. furcifera control in recent years. Similar situations of increased resistance due to intensive applications of imidacloprid and buprofezin have also been reported in the brown planthopper Nilaparvata lugens (Wang et al., 2008; Wang et al., 2009; Zhang et al., 2016b). Though acetamiprid, dinotefuran, and clothianidin have not been used for the control of rice planthopper, we found that some field populations of S. furcifera had developed moderate level of resistance to dinotefuran and acetamiprid, and low level of resistance to clothianidin, and dinotefuran resistance increased obviously in 2015 compared with that from 2011 to 2014. This may partially because of the cross-resistance between dinotefuran and other insecticide, and application of this insecticide in Southeast Asian countries (Wang et al., 2008; Mu et al., 2016). In addition, resistance to clothianidin in 2015 was obviously high than that from 2011 to 2014, but this increase may result from cross-resistance with other insecticide of different mode of action. Resistance to acetamiprid did not increase as obviously as other insecticides, the possible explanation for this is that these insecticides have not been used extensively for
X-100 water solution only. All treatments were maintained at a temperature of 27 ± 1 °C and 70%–80% relative humidity with a 16-h light/8-h dark photoperiod. Mortality was assessed after exposure to these insecticides for 96 h. The nymphs were considered dead if they were unable to move after a gentle prodding with a fine brush. Data analysis The LC50 values, 95% confidence interval were calculated by Probit analysis via DPS (3.01). The LC50 value of the susceptible baseline for imidacloprid, thiamethoxam, nitenpyram, dinotefuran, clothianidin and acetamiprid were 0.109 (0.057–0.172), 0.096 (0.040–0.169), 0.13 (0.10–0.18), 0.12 (0.08–0.17), 0.15 (0.09–0.21) and 0.52 (0.19–0.82) mg/L respectively (Zhang et al., 2013; Zhang et al., 2016a). Classification of resistance level was according to Shao et al. (2013), resistance with a RR ≤ 5-fold was classified as susceptible, RR = 5–10-fold as low resistance level, RR = 10–100-fold as medium resistance level and RR > 100-fold as high resistance level. Results and discussion The results showed that field populations of S. furcifera had developed different levels of resistance to all tested neonicotinoid insecticides. More specifically, approximately 85.0% of field populations of S. furcifera exhibited low to moderate levels of resistance to acetamiprid (Resistance Ratio, RR = 5.6–12.2), while other populations remained susceptible to this insecticide (RR = 3.3–4.1) (Table 2). Whereas, most field populations of S. furcifera (55.6% − 74.1%) still maintained susceptible (RR = 0.8–5.0) to thiamethoxam (55.6%), dinotefuran (55.6%), imidacloprid (63.0%), nitenpyram (74.1%), clothianidin (74.1%) respectively, only 11.1% − 25.0% of field populations exhibited moderate level of resistance to imidacloprid (14.8%), thiamethoxam (18.5%), dinotefuran (11.1%) and acetamiprid (25.0%) with RR ranging from 10.1 to 16.6, the other populations showed low level of resistance to these insecticides (RR = 5.1–10.0) (Table 2). Further, there were an increasing trend in neonicotinoid insecticide resistance in the period 2011–2015, including imidacloprid,
Fig. 1. Comparison of resistance levels of Sogatella furcifera field populations collected in Central China in the period 2011–2015 to 6 insecticides. The scatter diagram of the resistance ratios of different populations of S. furcifera to different insecticides. Red horizontal lines across the scatter diagram represent the mean value of the resistance ratio of the different populations. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
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planthopper resistance to insecticides. In: Heong, K.L., Cheng, J.A., Escalada, M.M. (Eds.), Rice Planthopper: Ecology, Management, Socio Economics and Policy. Zhejiang Universty Press, Hangzhou and Springer Science Publisher, London, pp. 117–141. Matsumura, M., Takeuchi, H., Satoh, M., Sanada-Morimura, S., Otuka, A., Watanabe, T., Thanh, D.V., 2008. Species-specific insecticide resistance to imidacloprid and fipronil in the rice planthoppers Nilaparvata lugens and Sogatella furcifera in east and southeast Asia. Pest Manag. Sci. 64, 1115–1121. Matsumura, M., Sanada-Morimura, S., Otuka, A., Ohtsu, R., Sakumoto, S., Takeuchia, H., Satoha, M., 2014. Insecticide susceptibilities in populations of two rice planthoppers, Nilaparvata lugens and Sogatella furcifera, immigrating into Japan in the period 2005− 2012. Pest Manag. Sci. 70, 615–622. Mu, X.C., Zhang, W., Wang, L.X., Zhang, S., Zhang, K., Gao, C.F., Wu, S.F., 2016. Resistance monitoring and cross-resistance patterns of three rice planthoppers, Nilaparvata lugens, Sogatella furcifera and Laodelphax striatellus to dinotefuran in China. Pestic. Biochem. Physiol. 134, 8–13. Selvaraj, K., Chander, S., Sujithra, M., 2012. Determination of multiple-species economic injury levels for rice insect pests. Crop. Prot. 32, 150–160. Shao, Z.R., Feng, X., Zhang, S., Li, Z.Y., Huang, J.D., Cheng, H.Y., Hu, Z.D., 2013. Guideline for Insecticide Resistance Monitoring of Plutella xylostella (L.) on Cruciferous Vegetables. China Agriculture Press, Beijing. Sparks, T.C., Nauen, R., 2015. IRAC: mode of action classification and insecticide resistance management. Pestic. Biochem. Physiol. 121, 122–128. Su, J.Y., Wang, Z.W., Zhang, K., Tian, X.R., Yin, Y.Q., Zhao, X.Q., Sheng, A.D., Gao, C.F., 2013. Status of insecticide resistance of the whitebacked planthopper, Sogatella furcifera (Hemiptera: Delphacidae). Fla. Entomol. 96, 948–956. Tang, J., Li, J., Shao, Y., Yang, B.J., Liu, Z.W., 2010. Fipronil resistance in the whitebacked planthopper (Sogatella furcifera): possible resistance mechanisms and crossresistance. Pest Manag. Sci. 66, 121–125. Wang, Y.H., Chen, J., Zhu, Y.C., Ma, C.Y., Huang, Y., Shen, J.L., 2008. Susceptibility to neonicotinoids and risk of resistance development in the brown planthopper, Nilaparvata lugens (Stål) (Homoptera: Delphacidae). Pest Manag. Sci. 64, 1278–1284. Wang, Y.H., Wu, S.G., Zhu, Y.C., Chen, J., Liu, F.Y., Zhao, X.P., Wang, Q., Li, Z., Bo, X.P., Shen, J.L., 2009. Dynamics of imidacloprid resistance and cross-resistance in the brown planthopper, Nilaparvata lugens. Entomol. Exp. Appl. 131, 20–29. Yadav, D.S., Chander, S., 2010. Simulation of rice planthopper damage for developing pest management decision support tools. Crop. Prot. 29, 267–276. Zhang, X.F., Li, J.J., Qi, G.F., Wen, K., Lu, J.Z., Zhao, X.Y., 2011. Insecticidal effect of recombinant endophytic bacterium containing Pinellia ternata agglutinin against white backed planthopper, Sogatella furcifera. Crop. Prot. 30, 1478–1484. Zhang, K., Wang, Z.W., Gao, C.F., 2013. Methods for rice planthopper resistance monitoring. Chin. J. Appl. Entomol. 52, 542–547. Zhang, K., Zhang, W., Zhang, S., Wu, S.F., Ban, L.F., Su, J.Y., Gao, C.F., 2014. Susceptibility of Sogatella furcifera and Laodelphax striatellus (Hemiptera: Delphacidae) to six insecticides in China. J. Econ. Entomol. 107, 1916–1922. Zhang, X.L., Liao, X., Mao, K.K., Li, J.H., Wan, H., 2016a. Insecticide resistance monitoring in field populations of the white-back planthopper, Sogatella furcifera (Hemiptera: Delphacidae) in rice production areas of Hubei Province, Central China. Acta Entomol. Sin. 59, 1213–1221. Zhang, X.L., Liao, X., Miao, K.K., Zhang, K.X., Wan, H., Li, J.H., 2016b. Insecticide resistance monitoring and correlation analysis of insecticides in field populations of the brown planthopper Nilaparvata lugens (Stål). Pestic. Biochem. Physiol. 132, 13–20.
controlling rice planthopper in China. Fast development of neonicotiniod insecticides resistance indicated that integrated pest management (IPM), including biological control, cultural practice (good irrigation practices, resistant rice varieties, reduction of nitrogen fertilizer and so on), should be implemented along with insecticide application in controlling this pest. However, the application of chemical insecticides remains a primary tool for WBPH control currently. Mode of action rotation is one of the corner stones of modern resistance management strategies and the IRAC mode of action classification helps to make correct decisions on how to alternate different chemical classes of insecticides (Sparks and Nauen, 2015), thus, chemical insecticides belonging to mode of action classes other than nicotinic acetylcholine receptor modulators should be used in a rational manner in order to safeguard their long term efficacy and utility in controlling this pest. Competing interests The authors have declared that no competing interests exist. Acknowledgements This work was supported by the Special Fund for Agro-Scientific Research in the Public Interest (201203038 and 201503107). References Catindig, J.L.A., Arida, G.S., Baehaki, S.E., Bentur, J.S., Cuong, L.Q., Norowi, M., Rattanakarn, W., Sriratanasak, W., Xia, J., Lu, Z., 2009. Situation of planthoppers in Asia. In: Heong, K.L., Hardy, B. (Eds.), Planthoppers: New Threats to the Sustainability of Intensive Rice Production Systems in Asia. International Rice Research Institute, Philippines, pp. 191–220. Cheng, J.A., 2015. Rice planthoppers in the past half century in China. In: Heong, K.L., Cheng, J.A., Escalada, M.M. (Eds.), Rice Planthopper: Ecology, Management. Socio Economics and Policy. Zhejiang University Press, Hangzhou and Springer Science Publisher, London, pp. 1–32. Endo, S., Nagata, T., Kawabe, S., Kazano, H., 1988. Changes of insecticide susceptibility of the white backed planthopper Sogatella furcifera Horváth (Homoptera: delphacidae) and the brown planthopper Nilaparvata lugens Stål (Homoptera: delphacidae). Appl. Entomol. Zool. 23, 417–421. Horgan, F.G., Srinivasan, T.S., Naik, B.S., Ramal, A.F., Bernal, C.C., Almazan, M.L.P., 2016. Effects of nitrogen on egg-laying inhibition and ovicidal response in planthopper-resistant rice varieties. Crop. Prot. 89, 223–230. Liu, Z.W., Wu, J.C., Zhang, Y.X., Liu, F., Xu, J.X., Bao, H.B., 2015. Mechanism of rice
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