Research Article Received: 30 March 2015
Revised: 5 May 2015
Accepted article published: 29 June 2015
Published online in Wiley Online Library: 23 July 2015
(wileyonlinelibrary.com) DOI 10.1002/ps.4068
Cross-resistance and baseline susceptibility of Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) to cyantraniliprole in the south of China Song Sang, Benshui Shu, Xin Yi, Jie Liu, Meiying Hu and Guohua Zhong* Abstract BACKGROUND: The oriental leafworm moth, Spodoptera litura Fab. (Lepidoptera: Noctuidae), is a widely distributed polyphagous insect pest in Asia that has been shown to be resistant to various types of insecticide. The newly registered anthranilic diamide cyantraniliprole provided novel insight and great opportunities to control S. litura. RESULTS: In this study, the susceptibilities of S. litura collected from South China to cyantraniliprole were measured by standard leaf-disc bioassay, and obvious variation in susceptibility was observed among the 17 field populations, with LC50 values varying from 0.206 to 1.336 mg AI L−1 . Significant correlations were detected between the LC50 values of cyantraniliprole and chlorantraniliprole (P < 0.05). However, no significant correlation (P > 0.05) was observed between the two anthranilic diamides and other insecticides with different action mechanisms (delcamethrin, chlorpyrifos, indoxacarb and emamectin benzoate). Piperonyl butoxide showed obvious synergism in Lab-Sus, ZC14 and cyantraniliprole-resistant strains, while diethyl maleate and S,S,S-tributylphorotrithioate had no obvious synergistic effects in any of the strains tested. CONCLUSION: These results revealed obvious regional variation in cyantraniliprole susceptibilities among populations of S. litura from different areas, and potential cross-resistance to chlorantraniliprole, which suggested that S. litura could develop resistance to cyantraniliprole. Detoxification enzymes might not be involved in the observed tolerance in field-collected populations and the cyantraniliprole-resistant strain. © 2015 Society of Chemical Industry Keywords: Spodoptera litura; cyantraniliprole; baseline susceptibility; cross-resistance; detoxification mechanisms
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INTRODUCTION
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The oriental leafworm moth, Spodoptera litura Fab. (Lepidoptera: Noctuidae), is a widely distributed polyphagous pest with an extensive host range of economically important crops such as cotton (Gossypium hirsutum L.), groundnut (Arachis villosulicarpa L.), soybean [Glycine max (L.) Merr.], tobacco (Nicotiana tabacum L.), vegetables and others.1,2 In recent years, frequent outbreaks of this pest and crop failures have been more common in the middle and lower reaches of the Yangtze River and southern region of China.3,4 Chemical insecticide control is the most practical way to prevent its damage. However, the extensive and frequent application of insecticide has led to the rapid development of insecticide resistance, which has been confirmed as the major reason for field control failures. High levels of resistance to conventional insecticides, including organophosphates, carbamates and pyrethroids, have been reported in China5,6 and other countries.7 – 10 Recently, resistance to some novel insecticides such as abamectin, emamectin benzoate, fipronil, indoxacarb, spinosad and chlorantraniliprole has also been documented.6,11 – 14 In order to delay the development of resistance, new insecticides with different action mechanisms could be rotated with existing insecticides. Therefore, a novel insecticide cyantraniliprole was registered and commercialised in Pest Manag Sci 2016; 72: 922–928
China 2014, expected to provide a new option for the field control of this insect pest.15 Cyantraniliprole is a second-generation ryanodine receptor insecticide discovered after chlorantraniliprole by DuPont Crop Protection and belonging to the diamide family, group 28 (IRAC, 2012). This new insecticide group acts on binding and activating the ryanodine receptors in insect striate muscle cells, provoking calcium release from internal stores and causing muscular continuous contraction, paralysis and death.16 – 18 Cyantraniliprole has been reported to be effective against a broad spectrum of insect pests, including Lepidoptera, dipteran leafminers, aphids, leafhoppers, psyllids, beetles, whiteflies, thrips and weevils.16 Owing to their structural specificity to insect ryanodine receptors over mammalian counterparts, it has also been shown to be safe for non-target vertebrates.19 In addition, some research evidence
∗
Correspondence to: Guohua Zhong, Key Laboratory of Pesticide and Chemical Biology, College of Natural Resources and Environment, South China Agricultural University, Guangzhou 510642, China. E-mail: [email protected] Laboratory of Insect Toxicology, Key Laboratory of Pesticide and Chemical Biology, South China Agricultural University, Guangzhou, China
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Susceptibility of the oriental leafworm moth to cyantraniliprole
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Table 1. Locations, sampling sites, dates, host plants and developmental stages of S. litura collected from fields
Strains
Locations
Map reference number
Collection date
Sites
GZ13 HZ13 WY13 DG13 HZ14 YF14 FS14 GZ14 ZC14
Guangzhou, Guangdong Huizhou, Guangdong Wengyuan, Guangdong Dongguan, Guangdong Huizhou, Guangdong Yunfu, Guangdong Foshan, Guangdong Guangzhou, Guangdong Zengcheng, Guangdong
25 May 2013 26 June 2013 2 July 2013 12 September 2013 2 May 2014 27 May 2014 7 June 2014 3 May 2014 22 July 2014
1 2 3 4 2 5 6 1 7
23.21∘ N, 113.25∘ E 23.43∘ N, 114.48∘ E 24.44∘ N, 113.83∘ E 23.83∘ N, 113.74∘ E 23.28∘ N, 113.94∘ E 22.76∘ N, 111.84∘ E 23.04∘ N, 113.19∘ E 23.21∘ N, 113.25∘ E 23.23∘ N, 113.64∘ E
NX14 ZH14 NC14 ND14 FZ14 HK14
Nanxiong, Guangdong Zhuhai, Guangdong Nanchang, Jiangxi Ningde, Fujian Fuzhou, Fujian Haikou, Hainan
26 July 2014 16 August 2014 4 September 2014 15 September 2014 16 September 2014 21 August 2014
8 9 10 11 12 13
25.06∘ N, 114.27∘ E 22.03∘ N, 113.33∘ E 28.76∘ N, 115.84∘ E 27.21∘ N, 119.59∘ E 25.94∘ N, 119.27∘ E 20.00∘ N, 110.51∘ E
GL14 CS14
Guilin, Guangxi Changsha, Hunan
21 September 2014 25 September 2014
14 15
25.93∘ N, 111.09∘ E 28.18∘ N, 113.08∘ E
has indicated that cyantraniliprole presents no cross-resistance with other insecticides used frequently for the control of Bemisia tabaci.20,21 It is crucially important to establish the susceptibility levels of various field populations to newly developed insecticides at the outset, even before their widespread use. The objective of this research was to investigate the susceptibilities of field populations of S. litura to cyantraniliprole in the south of China, and to examine potential cross-resistance patterns to other insecticides used frequently against this pest. In addition, in order to explain the possible mechanisms involved in the resistance to cyantraniliprole, the synergistic effects of synergists were determined.
2
Colocasia esculenta Colocasia esculenta Colocasia esculenta Brassica chinensis L. Asparagus officinalis Arachis hypogaea L. Colocasia esculenta Colocasia esculenta Colocasia esculenta, Solanum melongena L. Colocasia esculenta Colocasia esculenta Colocasia esculenta Colocasia esculenta Colocasia esculenta Nelumbo nucifera Gaerth Colocasia esculenta Colocasia esculenta
Egg mass Egg mass Egg mass Egg mass Second to fifth instars Second to fourth instars Third to fifth instars Second to fourth instars Second to fourth instars
Third to fifth instars Second to fourth instars Third to fifth instars Third to fifth instars Third to fourth instars Third to fourth instars Third to fifth instars Second to fourth instars
10 15 11 12 14
5
MATERIALS AND METHODS
8 3 1 7 6 9
4
2
13
Figure 1. Sampling sites of S. litura field populations in the south of China.
on the results of bioassays from the previous generation. The number of larvae used for each generation ranged from 1000 to 1600, depending on availability. After 3 days of exposure, surviving larvae were transferred to fresh artificial diet and reared in the laboratory under the conditions described above. After 13 generations of resistance selection, there was a 24.10-fold increase in LC50 , which was then taken as the cyantraniliprole-resistant (CR) strain. 2.2 Chemicals Six insecticides were used in the present study: 94% cyantraniliprole, 95% chlorantraniliprole and 90% indoxacarb (DuPont Agricultural Chemicals Ltd, Shanghai, China), 97% chlorpyrifos (Zhejiang Xinnong Chemicals Co., Ltd, Hangzhou, China), 98% deltamethrin (Nanjing Redsun Co., Ltd, Nanjing, China) and 95%
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2.1 Insects Seventeen field populations of S. litura were collected from 15 different regions in the south of China. Approximately 15–20 egg masses and 150–300 individuals of second to fifth instars of S. litura were collected from each site (Fig. 1 and Table 1). Larvae of all populations were reared on an artificial diet,15 and adults were fed with 10% sugar solution. All stages were kept under the same standard conditions of 25 ± 1 ∘ C and 60–70% RH with a photoperiod of 16:8 h light:dark (L:D). Larvae of the first generation (F1 ) and second generation (F2 ) were used for susceptibility bioassays. The laboratory population (Lab-Sus) of S. litura was used as the reference population. This strain was obtained by single pair crosses of a field-collected population and reared on artificial diet in the laboratory without exposure to any insecticide for more than 6 years. This laboratory strain was used as the susceptible colony for the first generation of resistance selection. Newly third-instar larvae were used for the toxicity assays and the establishment of resistant lines. The concentration of cyantraniliprole used to select each subsequent generation was the LC50 , which was based Pest Manag Sci 2016; 72: 922–928
Developmental stage
Host plants
www.soci.org emamectin benzoate (Xianzhengda Nantong Crop Preservation Co., Ltd, Nantong, China). The 98% diethyl maleate (DEM), 96% piperonyl butoxide (PBO) and 98% S,S,S-tributylphorotrithioate (DEF) were supplied by Guangzhou Haoma Biotechnology Co., Ltd, Guangzhou, China. 2.3 Bioassay Bioassays were conducted with newly third-instar larvae of S. litura by a standard leaf-disc bioassay.22 A total of 5–6 serial dilutions of insecticide were prepared using distilled water containing 0.1% Triton X-100, and each disc (6.0 cm diameter) from arum leaves was immersed in a test solution for 10 s and allowed to dry at ambient temperature for 1–1.5 h. Control discs were treated with 0.1% Triton X-100 solution only. The leaf discs were placed in individual petri dishes (9 cm in diameter) containing moistened filter paper. Each treatment (concentration) was replicated 3 times, including controls. Ten newly third instars were placed on each leaf disc, and thus the total number of tested larvae per concentration was 30. The bioassays were kept at a temperature of 25 ± 2 ∘ C and 60–70% RH with a photoperiod of 16:8 h L:D. Mortality was assessed after exposure to delcamethrin, chlorpyrifos and emamectin benzoate for 48 h, and to indoxacarb, chlorantraniliprole and cyantraniliprole for 72 h. Larvae were considered to be dead if they failed to make a coordinated movement when prodded with a clean hair brush. 2.4 Synergist bioassays The standard leaf disc bioassay was also used to test the effect of synergists PBO, DEM and DEF on the toxicity of cyantraniliprole to two field strains, Lab-Sus strain and CR strain. Arum leaves treated with 100 mg L−1 of each synergist were fed to third instars for 12 h, and then larvae were assayed for toxicity against cyantraniliprole as described above.
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2.5 Statistical analysis Concentration–mortality responses, lethal concentrations (LC50 , LC90 ), confidence intervals and slopes were calculated by probit analysis with the POLOPlus program.23 In the comparisons of mortality responses between populations, two LC50 values were taken to be significantly different if there was no overlap between their corresponding 95% fiducial limits (FLs).24 Resistance factors (RFs) with 95% confidence limits were calculated using Lab-Sus strain as the factor divisor.25 The insecticide resistance level was described using RFs as reported by Lai et al.:26 susceptibility (RF = 1–3), decreased susceptibility (RF = 3–5), low resistance (RF = 5–10), moderate resistance (RF = 10–40), high resistance (RF = 40–160) and very high resistance (RF > 160). The synergistic ratio was calculated by dividing the LC50 values without synergist by the corresponding LC50 value with synergist, and the synergistic ratios were regarded as significant if their 95% FLs did not include 1.0.27 Correlation between variables was calculated by the Pearson method using the IBM SPSS Statistics software package, and a P-value of less than 0.05 was thought to be statistically significant.
3
RESULTS
3.1 Variation in cyantraniliprole susceptibilities among field populations Seventeen S. litura field populations collected from six Chinese provinces during 2013–2014 (Fig. 1 and Table 1) and a susceptible strain (Lab-Sus) were subjected to bioassays to examine the susceptibility to cyantraniliprole. Obtained results indicated that the Lab-Sus strain exhibited the most significant susceptibility to cyantraniliprole. The LC50 values of cyantraniliprole ranged from 0.206 to 1.336 mg AI L−1 across these field populations, and there was a 6.5-fold difference in LC50 values between the YF14 and GL14 strains (Table 2). The GL14 field strain displayed a 16.1-fold
Table 2. Susceptibility to cyantraniliprole of S. litura collected from fields in the south of China
Strains
na
Slope (SE)b
𝜒2
SS GZ13 HZ13 WY13 DG13 HZ14 YF14 FS14 GZ14 ZC14 NX14 NC14 ND14 FZ14 HK14 GL14 ZH14 CS14
210 210 210 180 180 180 210 210 210 180 180 180 180 210 210 180 180 180
2.239 (0.274) 1.291 (0.222) 2.128 (0.265) 2.066 (0.310) 1.842 (0.293) 1.503 (0.275) 1.365 (0.247) 1.615 (0.226) 1.578 (0.230) 1.735 (0.286) 1.650 (0.324) 1.743 (0.287) 2.161 (0.334) 1.168 (0.182) 1.267 (0.213) 1.488 (0.222) 1.767 (0.286) 1.743 (0.286)
1.597 (4) 0.161 (4) 3.162 (4) 0.633 (3) 0.880 (3) 0.676 (3) 0.062 (4) 5.897 (4) 1.294 (4) 0.407 (3) 0.508 (3) 0.882 (3) 2.090 (3) 0.667 (4) 0.894 (4) 1.582 (3) 0.290 (3) 0.229 (3)
(df )c
LC50 (mg AI L−1 ) (95% FL)
0.083 (0.066–0.106) 0.311 (0.223–0.509) 0.334 (0.191–0.490) 3.286 (1.961–8.273) 0.831 (0.649–1.064) 3.325 (2.345–5.622) 0.483 (0.363–0.625) 2.015 (1.390–3.723) 0.531 (0.390–0.705) 2.634 (1.706–5.621) 0.503 (0.343–0.705) 3.581 (2.052–10.650) 0.206 (0.102–0.315) 1.794 (1.143–3.946) 0.466 (0.274–0.887) 2.899 (1.333–20.078) 0.514 (0.358–0.697) 3.335 (2.155–6.775) 1.250 (0.918–1.702) 6.846 (4.201–16.573) 0.355 (0.188–0.517) 2.123 (1.390–4.668) 0.574 (0.425–0.791) 3.120 (1.881–7.841) 0.905 (0.702–1.242) 3.546 (2.262–7.796) 0.299 (0.142–0.343) 2.870 (1.549–8.287) 1.204 (0.838–1.894) 12.356 (5.897–49.811) 1.336 (0.931–1.937) 9.715 (5.566–24.865) 0.249 (0.184–0.338) 1.324 (0.822–3.099) 0.411 (0.296–0.554) 2.236 (1.412–5.072)
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a Number of insects bioassayed. b Standard error. c Chi-square (P > 0.05); df: degree of freedom. d Resistance factor (RF): LC , LC of the field-collected population/LC , LC 50 90 50 90
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LC90 (mg AI L−1 ) (95% FL)
RF50 (95% FL)d
RF90 (95% FL)d
– 4.0 (2.4–6.6) 10.0 (7.1–14.0) 5.8 (4.1–8.3) 6.4 (4.4–9.2) 6.0 (4.0–9.2) 2.5 (1.4–4.4) 5.6 (3.8–8.2) 6.2 (4.1–9.2) 15.0 (10.2–22.0) 4.3 (2.5–7.2) 6.9 (4.7–10.1) 10.9 (7.6–15.6) 2.8 (1.7–4.5) 14.5 (9.2–22.8) 16.1 (10.5–24.7) 3.0 (2.1–4.4) 4.9 (3.4–7.3)
– 10.6 (4.9–22.9) 10.7 (6.0–19.2) 6.5 (3.5–12.0) 8.4 (4.6–18.2) 11.5 (5.0–26.8) 5.8 (2.9–11.6) 9.3 (4.4–19.9) 10.7 (5.5–21.1) 22.0 (10.4–46.6) 6.8 (3.5–13.4) 10.0 (4.6–21.7) 11.4 (5.6–23.1) 9.2 (3.8–22.3) 39.7 (13.8–114.4) 31.3 (13.9–70.4) 4.2 (2.0–8.9) 7.2 (3.5–14.8)
of the Lab-sus strain.
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Pest Manag Sci 2016; 72: 922–928
Susceptibility of the oriental leafworm moth to cyantraniliprole
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Table 3. The resistance levels of S. litura field populations to frequently used insecticides Delcamethrin Strains SS GZ13 HZ13 WY13 DG13 FS14 ZC14 NX14 NC14 ND14 GL14
LC50
(mg L−1 )
3.602 424.949 105.096 171.425 125.000 39.708 42.300 62.278 89.654 61.692 34.525
Chlorpyrifos RF
1.0 118.0 29.2 47.6 34.7 11.0 11.7 17.3 24.9 17.1 9.6
LC50
(mg L−1 )
2.434 154.198 50.845 276.709 143.601 37.829 34.192 28.053 99.524 71.811 23.264
Indoxacarb RF 1.0 63.4 20.9 113.7 59.0 15.54 14.0 11.5 40.9 29.5 9.6
Emamectin benzoate
(mg L−1 )
RF
3.521 72.336 54.018 88.886 7.739 35.243 14.322 22.583 36.280 40.817 11.011
1.0 20.5 15.3 25.2 2.2 10.0 4.1 6.4 10.3 11.6 3.1
LC50
LC50
(mg L−1 )
RF
0.051 0.216 0.500 1.350 1.564 1.096 0.808 0.411 0.438 0.890 0.862
– 4.2 9.8 26.7 30.6 21.5 15.8 8.1 8.6 17.5 16.9
Chlorantraniliprole LC50 (mg L−1 ) 0.111 0.563 0.856 0.555 0.582 0.240 1.266 0.494 1.349 1.710 1.291
RF – 5.1 7.7 5.0 5.2 2.2 11.4 4.4 12.1 15.3 11.6
Table 4. Pairwise correlation coefficient comparison between log LC50 values of tested insecticides on field populations of S. litura Cyantraniliprole Chlorantraniliprole Delcamethrin Chlorpyrifos Indoxacarb Emamectin benzoate a
0.716a −0.610 −0.466 −0.418 −0.042
Chlorantraniliprole
Delcamethrin
−0.195 −0.111 −0.174 −0.285
0.817a 0.546 −0.478
Chlorpyrifos
0.477 −0.277
Indoxacarb
−0.432
Positive correlation between LC50 values of insecticides at 95% significance level.
resistance to this insecticide, reaching a moderate resistance level, when compared with the Lab-Sus strain. The HZ13, ZC14, ND14 and HK14 strains also showed moderate resistance, and six populations had a low resistance level. Decreased susceptibility was observed in GZ13, NX14, ZH14 and CS14 strains. However, only two populations, YF14 and FZ14, exhibited similar susceptibility to that of Lab-Sus to this compound. No difference was detected in the years 2013 and 2014 from strains collected in Huizhou and Guangzhou. The results of the regression analysis of the slopes obtained for the field-collected populations varied from 1.168 ± 0.182 (FZ14) to 2.161 ± 0.334 (ND14), suggesting a fairly heterogeneous response to cyantraniliprole in the collected populations (Table 2). The LC90 values for cyantraniliprole ranged from 1.324 mg AI L−1 (ZH14) to 12.356 mg AI L−1 (HK14) (Table 2), which provided similar resistance ratios (RF90 = 4.2–39.7-fold) to RF50 values.
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3.3 Synergism tests To analyse the biochemical mechanisms to cyantraniliprole in S. litura, the mixed-function oxidase (MFO) inhibitor PBO, the esterase (EST) inhibitor DEF and the glutathione S-transferase (GST) inhibitor DEM were used for synergism assays in the Lab-Sus strain, the cyantraniliprole-resistant strain (CR) and the two field populations (ZC14 and GL14) with moderate resistance (Table 5). PBO showed obvious synergistic effects in ZC14 and cyantraniliprole-resistant strains, with synergistic ratios (SRs) of 1.8 and 2.1 respectively; however, an obvious and similar synergistic ratio was also observed in the Lab-Sus strain (SR = 1.7). The results indicated that MFO might be implicated in detoxification in the Lab-Sus, ZC14 and cyantraniliprole-resistant strains, but this occurs irrespective of the tolerance of S. litura to cyantraniliprole, which also indicated that rational applications of PBO may increase the efficacy of this product. DEM and DEF had no obvious effect on the toxicities of cyantraniliprole on any of the four strains tested. These results suggested that detoxification metabolism mediated by MFO, GST and EST might not be involved in the observed tolerance to cyantraniliprole in the feld populations ZC14 and GL14 and the cyantraniliprole-resistant strain of S. litura.
4
DISCUSSION AND CONCLUSION
S. litura has become a major insect pest in various vegetables and field crops in China. Multiple classes of insecticides, including
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3.2 Pairwise correlations between toxicities of cyantraniliprole and other insecticides Other than the concentration–mortality responses to cyantraniliprole, the dose–response of ten S. litura field populations to frequently used insecticides, including delcamethrin, chlorpyrifos, indoxacarb, emamectin benzoate and chlorantraniliprole, were also measured using the leaf-dip bioassay (Table 3). The pairwise correlations between the values of log LC50 of cyantraniliprole and log LC50 of the five frequently used insecticides were analysed. The results showed that significant correlation was observed between S. litura susceptibility to cyantraniliprole and chlorantraniliprole (R = 0.716, P < 0.05), which are both members of the anthranilic diamide class. However, no significant correlation was observed between the two
anthranilic diamides and the other four conventional insecticides (delcamethrin, chlorpyrifos, indoxacarb and emamectin benzoate). Moreover, significant correlation between delcamethrin and chlorpyrifos (R = 0.817, P < 0.05) was also determined (Table 4).
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Table 5. Insecticide synergism in the Lab-Sus strain and two field populations of S. litura
Strains
na
Lab-Sus Lab-Sus Lab-Sus Lab-Sus ZC14 ZC14 ZC14 ZC14 GL14 GL14 GL14 GL14 CRe CRe CRe CRe
210 210 180 180 180 210 180 180 180 180 180 180 180 180 180 180
LC50 (mg AI L−1 ) (95% FL)
Pesticides Cyantraniliprole only Cyantraniliprole + PBO Cyantraniliprole + DEF Cyantraniliprole + DEM Cyantraniliprole only Cyantraniliprole + PBO Cyantraniliprole + DEF Cyantraniliprole + DEM Cyantraniliprole only Cyantraniliprole + PBO Cyantraniliprole + DEF Cyantraniliprole + DEM Cyantraniliprole only Cyantraniliprole + PBO Cyantraniliprole + DEF Cyantraniliprole + DEM
0.083 (0.066–0.106) 0.049 (0.038–0.063) 0.068 (0.049–0.095) 0.059 (0.045–0.077) 1.250 (0.918–1.702) 0.709 (0.521–0. 950) 0.878 (0.608–1.194) 1.115 (0.818–1.497) 1.336 (0.931–1.937) 0.941 (0.672–1.304) 1.196 (0.840–1.704) 1.027 (0.777–1.360) 2.001 (1.294–3.093) 0.938 (0.631–1.370) 1.612 (1.125–2.226) 1.267 (0.891–1.692)
Slope (SE)b
𝜒 2 (df )c
Synergistic ratio (95% FL)d
2.239 (0.274) 2.064 (0.260) 1.647 (0.281) 2.020 (0.304) 1.735 (0.286) 1.660 (0.229) 1.655 (0.284) 1.785 (0.289) 1.488 (0.222) 1.610 (0.279) 1.552 (0.228) 1.947 (0.296) 1.225 (0.261) 1.371 (0.267) 1.585 (0.279) 1.795 (0.296)
1.597 (4) 0.219 (4) 0.878 (3) 0.848 (3) 0.407 (3) 0.543 (4) 0.024 (3) 0.325 (2) 1.582 (3) 0.531 (3) 1.135 (3) 0.392 (3) 0.219 (3) 0.118 (3) 0.675 (3) 0.277 (3)
– 1.7 (1.2–2.4)* 1.2 (0.8–1.8) 1.4 (1.0–2.0) – 1.8 (1.2–2.7)* 1.4 (0.9–2.2) 1.1 (0.7–1.7) – 1.4 (0.9–2.3) 1.1 (0.7–1.8) 1.3 (0.8–2.0) – 2.1 (1.2–3.7)* 1.2 (0.7–2.1) 1.5 (1.0–2.6)
a Number of larvae tested. b Standard error.
c Chi-square (P > 0.05); df: degree of freedom. d Synergistic ratio = LC (without synergist)/LC 50 50
(with synergist).
*The synergistic ratio is significant. e CR: cyantraniliprole-resistant strain.
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traditional and some novel selective chemistry pesticides, have been reported as failing to control this species. The recent commercialisation of cyantraniliprole provided an excellent strategy for the management of S. litura. Our previous experiment demonstrated that sublethal concentrations of cyantraniliprole could significantly affect the growth and development of S. litura.15 The present study established the baseline susceptibility of S. litura to cyantraniliprole in the south of China, before large-scale application of this insecticide. To the best of our knowledge, this is the first study to report the regional differences in susceptibility of S. litura to cyantraniliprole and obvious variation in tolerance in field populations (Fig. 1 and Tables 1 and 2). The present results clearly illustrated that several regional populations of S. litura had developed moderate resistance to this compound. Thus, this study provided valuable data for resistance monitoring and management in the future. The detection of regional differences in susceptibility to an insecticide before its widespread use in the field has been reported for metaflumizone,28 spinosad29 and chlorantraniliprole.14,26,30 – 33 Susceptibility variation in field populations of four insect species to cyantraniliprole has been reported recently. Caballero et al.34 observed that seven field populations of Bemisia tabaci biotype B (Gennadius) collected from southern Florida showed similar susceptibilities to cyantraniliprole. However, Grávalos et al.21 tested the same insecticide for Mediterranean strains of Bemisia tabaci and found that the LC50 values for nymphs from 14 field populations varied from 0.011 to 0.116 mg L−1 , a 10.5-fold natural variability. Other variations in cyantraniliprole susceptibility were observed in populations of Tuta absoluta (Lepidoptera: Gelechiidae),35 Bactrocera dorsalis (Diptera: Tephritidae)36 and Frankliniella occidentalis (Pergande)37 respectively. The present study found a wide range of variation (6.5-fold) in the susceptibility of S. litura from different areas where this compound had been
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introduced only for a short time (Table 2). Resistance selection experiments showed that S. litura might develop resistance to cyantraniliprole under continuous exposure (unpublished data). Therefore, more attention should be paid to the resistance risk of cyantraniliprole. The 17 S. litura strains tested were considered to be representatives of field populations causing widespread damage in the south of China (Fig. 1 and Table 1). The obversed 6.5-fold variation in susceptibility to cyantraniliprole from different areas implied that resistance might be caused by natural variation, different insecticide application history or other factors. To analyse the relationship between cyantraniliprole tolerance and past insecticide applications, pairwise correlations between LC50 values of cyantraniliprole and five frequently used insecticides were examined. No significant correlation (P > 0.05) was found between S. litura susceptibility to cyantraniliprole tolerance and the resistance to insecticides with other mechanisms of action (delcamethrin, chlorpyrifos, indoxacarb and emamectin benzoate) that were usually applied to control S. litura field populations in China, suggesting that the existing resistance mechanisms do not affect the performance of such anthranilic diamides. Lack of cross-resistance between cyantraniliprole and conventional insecticides has also been reported in B. tabaci from Arizona and Mediterranean strains.20,21 However, significant correlations (P < 0.05) were observed between cyantraniliprole and chlorantraniliprole, suggesting that a high risk of cross-resistance might be developed. Owing to the fact that both insecticides belong to group 28 (IRAC, 2012) and have the same mode of action, when resistance occurs, this situation will increase the risk of cross-resistance. However, only one resistant field strain has been identified. Recently, high levels of resistance to chlorantraniliprole and middle levels of resistance to cyantraniliprole have been reported for Plutella xylostella (L.) (Lepidoptera: Plutellidae) populations collected
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Susceptibility of the oriental leafworm moth to cyantraniliprole from South China.38 – 40 P. xylostella and S. litura could seriously mix-injure brassicaceous vegetables in the south of China all the year around, where the same insecticides are usually applied for controlling these two insect pests. Collectively, although the field-collected populations did not show a high resistance level to cyantraniliprole, a diamide should be used cautiously for controlling brassicaceous vegetable insect pests (e.g. P. xylostella and S. litura) in this region before the susceptibility of these pests to this class of compounds is restored. Understanding the detoxification metabolism mechanisms conferring insecticide resistance in field populations is necessary for resistance management and integrated pest management tactics. One of the most important factors of insect resistance is the increase in metabolic detoxification processes of the insecticide by MFO, EST and GST.41 In the present study, PBO showed obvious synergism in ZC14 and cyantraniliprole-resistant strains; however, an obvious synergistic ratio was also observed in the Lab-Sus strain. DEM and DEF had no obvious synergistic effects in any of the four strains. These results suggested that the detoxification enzymes MFO, EST and GST may not be involved in the observed tolerance of S. litura to cyantraniliprole. Similarly, a synergism assay in P. xylostella31 and Spodoptera exigua (Leidoptera: Noctuidae)26 demonstrated that MFO, EST and GST were not the main contributors to chlorantraniliprole resistance. Therefore, there might be some other mechanisms involved in the resistance to this class of insecticides in the tested insects. Owing to its broad spectrum, high efficiency and novel action mechanism, the environmental friendly insecticide cyantraniliprole has been well received by crop growers in China. The use of this compound will be more widespread in future. The bioassay results showed that cyantraniliprole is still effective in controlling S. litura in the south of China, but a wide range of variation in the susceptibility of field populations exists, and cross-resistance to chlorantraniliprole is possible. Therefore, susceptibility of S. litura to cyantraniliprole may be retained by rotating insecticides with different mechanisms of action. Simultaneously, an effective resistance management strategy should be put in place as early as possible to avoid/retard the further development of insect pest resistance to cyantraniliprole.
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ACKNOWLEDGEMENTS We thank Prof. Xiaomao Zhou (Hunan Agricultural University), Zhonghua Xiong (Jiangxi Agricultural University) and Gang Feng (Chinese Academy of Tropical Agricultural Sciences) for assistance in insect collection. This study was supported by a grant from the Guangdong Province Science and Technology Plan project (2012A020100009).
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REFERENCES
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1 Matsuura H and Naito A, Studies on the cold-hardiness and overwintering of Spodoptera litura F. (Lepidoptera: Noctuidae): VI. Possible overwintering areas predicted from meteorological data in Japan. Appl Entomol Zool 32:167–177 (1997). 2 Qin H, Ye Z, Huang S, Ding J and Luo R, The correlations of the different host plants with preference level, life duration and survival rate of Spodoptera litura Fabricius. Chin J Ecol Agric 12:40–42 (2004). 3 Huang S, Progress of the research on the control of Prodenia Litura Fabricius. Chin Acta Agric Jiangxi 10:65–69 (1998). 4 Zhou Z, A review on control of tobacco caterpillar, Spodoptera litura. Chin Bull Entomol 46:354–361 (2009). 5 Huang S, Xu J and Han Z, Baseline toxicity data of insecticides against the common cutworm Spodoptera litura (Fabricius) and a
comparison of resistance monitoring methods. Int J Pest Manag 52:209–213 (2006). Tong H, Su Q, Zhou X and Bai L, Field resistance of Spodoptera litura (Lepidoptera: Noctuidae) to organophosphates, pyrethroids, carbamates and four newer chemistry insecticides in Hunan, China. J Pest Sci 86:599–609 (2013). Armes NJ, Wightman JA, Jadhav DR and Rao R, Status of insecticide resistance in Spodoptera litura in Andhra Pradesh, India. Pestic Sci 50:240–248 (1999). Kim YG, Cho JR, Lee JN, Kang SY, Han SC, Hong KJ et al., Insecticide resistance in the tobacco cutworm, Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae). J Asia Pacif Entomol 1:115–122 (1998). Kranthi KR, Jadhav DR, Kranthi S, Wanjari RR, Ali SS and Russell DA, Insecticide resistance in five major insect pests of cotton in India. Crop Prot 21:449–460 (2002). Saleem MA, Ahmad M, Ahmad M, Aslam M and Sayyed AH, Resistance to selected organochlorine, organophosphate, carbamate and pyrethroid in Spodoptera litura (Lepidoptera: Noctuidae) from Pakistan. J Econ Entomol 101:1667–1675 (2008). Ahmad M, Sayyed AH, Saleem MA and Ahmad M, Evidence for field evolved resistance to newer insecticides in Spodoptera litura (Lepidoptera: Noctuidae) from Pakistan. Crop Prot 27:1367–1372 (2008). Shad SA, Sayyed AH and Saleema MA, Cross-resistance, mode of inheritance and stability of resistance to emamectin in Spodoptera litura (Lepidoptera: Noctuidae). Pest Manag Sci 66:839–846 (2010). Shad SA, Sayyed AH, Fazal S, Saleem MA and Zaka SM, Field evolved resistance to carbamates, organophosphates, pyrethroids, and new chemistry insecticides in Spodoptera litura Fab. (Lepidoptera: Noctuidae). J Pest Sci 85:153–162 (2012). Su J, Lai T and Li J, Susceptibility of field populations of Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) in China to chlorantraniliprole and the activities of detoxification enzymes. Crop Prot 42:217–222 (2012). Sang S, Shu B, Hu M, Wang Z and Zhong G, Sublethal effects of cyantraniliprole on the development and reproduction of the cabbage cutworm, Spodoptera litura. J South China Agric Univ (Nat Sci) 35:64–68 (2014). Lahm GP, Cordova D and Barry JD, New and selective ryanodine receptor activators for insect control. Bioorg Med Chem 17:4127–4133 (2009). Satelle DB, Cordova D and Cheek TR, Insect ryanodine receptors: molecular targets for novel control chemicals. Invert Neurosci 8:107–119 (2008). Lahm GP, Selby TP, Freudenberger JH, Stevenson TM, Myers BJ, Seburyamo G et al., Insecticidal anthranilic diamides: a new class of potent ryanodine receptor activators. Bioorg Med Chem Lett 15:4898–4906 (2005). Selby TP, Lahm GP, Stevenson TM, Hughes KA, Cordova D, Annan IB et al., Discovery of cyantraniliprole, a potent and selective anthranilic diamide ryanodine receptor activator with cross-spectrum insecticidal activity. Bioorg Med Chem Lett 23:6341–6345 (2013). Li X, Degain BA, Harpold VS, Marn PG, Nichols RL, Fournier AJ et al., Baseline susceptibilities of B- and Q-biotype Bemisia tabaci to anthranilic diamides in Arizona. Pest Manag Sci 68:83–91 (2012). Grávalos C, Fernández E, Belando A, Moreno I, Ros C and Bielza P, Cross-resistance and baseline susceptibility of Mediterranean strains of Bemisia tabaci to cyantraniliprole. Pest Manag Sci DOI: 10.1002/ps.388522 (2014). Sayyed AH, Ahmad M and Saleem MA, Cross-resistance and genetics of resistance to indoxacarb in Spodoptera litura (Lepidoptera: Noctuidae). J Econ Entomol 101:472–479 (2008). Roberson JL, Preisler HK and Russell RM, POLO-Plus – a User’s Guide to Probit and Logit Analysis. LeOra Software, Berkeley, CA (2002). Shelton AM, Robertson JL, Tang JD, Perez C, Eigenbrode SD, Preisler HK et al., Resistance of diamondback moth (Lepidoptera: Plutellidae) to Bacillus thuringiensis subspecies in the field. J Econ Entomol 86:697–705 (1993). Robertson JL, Russell RM, Preiseler HK and Savin NE, Bioassays with Arthropods, 2nd edition. CRC Press, Boca Raton, FL (2007). Lai T, Li J and Su J, Monitoring of beet armyworm Spodoptera exigua (Lepidoptera: Noctuidae) resistance to chlorantraniliprole in China. Pest Biochem Physiol 101:198–205 (2011). Sial AA and Brunner JF, Selection for resistance, reversion towards susceptibility and synergism of chlorantraniliprole and spinetoram
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in obliquebanded leafroller, Choristoneura rosaceana (Lepidoptera: Tortricidae). Pest Manag Sci 68:462–468 (2012). Khakame SK, Wang X and Wu Y, Baseline toxicity of metaflumizone and lack of cross resistance between indoxacarb and metaflumizone in diamondback moth (Lepidoptera: Plutellidae). J Econ Entomol 106:1423–1429 (2013). Osorio A, Martínez AM, Schneider MI, Díaz OJL, Corrales JL, Avilés MC et al., Monitoring of beet armyworm resistance to spinosad and methoxyfenozide in Mexico. Pest Manag Sci 64:1001–1007 (2008). Sial AA, Brunner JF and Doerr MD, Susceptibility of Choristoneura rosaceana (Lepidoptera: Tortricidae) to two new reduced-risk insecticides. J Econ Entomol 103:140–146 (2010). Wang X, Li X, Shen A and Wu Y, Baseline susceptibility of the diamondback moth (Lepidoptera: Plutellidae) to chlorantraniliprole in China. J Econ Entomol 103:843–848 (2010). Zheng X, Ren X and Su J, Insecticide susceptibility of Cnaphalocrocis medinalis (Lepidoptera: Pyralidae) in China. J Econ Entomol 104:653–658 (2011). da Silva JE, de Siqueira HAA, Silva TBM, de Campos MR and Barros R, Baseline susceptibility to chlorantraniliprole of Brazilian populations of Plutella xylostella. Crop Prot 35:97–101 (2012). Caballero R, Cyman S, Schuster DJ, Portillo HE and Slater R, Baseline susceptibility of Bemisia tabaci (Genn.) biotype B in southern Florida to cyantraniliprole. Crop Prot 44:104–108 (2013).
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35 Campos MR, Silva TBM, Silva WM, Silva JE and Siqueira HAA, Susceptibility of Tuta absoluta (Lepidoptera: Gelechiidae) Brazilian populations to ryanodine receptor modulators. Pest Manag Sci DOI: 10.1002/ps.3835 (2014). 36 Zhang R, He S and Chen J, Monitoring of Bactrocera dorsalis (Diptera: Tephritidae) resistance to cyantraniliprole in the south of China. J Econ Entomol 107:1233–1238 (2014). 37 Bielza P and Guillén J, Cyantraniliprole: a valuable tool for Frankliniella occidentalis (Pergande) management. Pest Manag Sci DOI: 10.1002/ps.3886 (2014). 38 Wang X and Wu Y, High levels of resistance to chlorantraniliprole evolved in field populations of Plutella xylostella. J Econ Entomol 105:1019–1023 (2012). 39 Wang X, Khakame SK, Ye C, Yang Y and Wu Y, Characterisation of field-evolved resistance to chlorantraniliprole in the diamondback moth, Plutella xylostella, from China. Pest Manag Sci 69:661–665 (2013). 40 Lin Q, Feng X, Hu Z, Yin F, Bao H, Li Z et al., The sensitivity baseline and current insecticide resistance of Plutella xylostella to cyantraniliprole. Chin Guangdong Agric Sci 15:76–78 (2014). 41 Mohan M and Gujar GT, Local variation in susceptibility of the diamondback moth, Plutella xylostella (Linnaeus), to insecticides and role of detoxification enzymes. Crop Prot 22:495–504 (2003).
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Revised: 5 May 2015
Accepted article published: 29 June 2015
Published online in Wiley Online Library: 23 July 2015
(wileyonlinelibrary.com) DOI 10.1002/ps.4068
Cross-resistance and baseline susceptibility of Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) to cyantraniliprole in the south of China Song Sang, Benshui Shu, Xin Yi, Jie Liu, Meiying Hu and Guohua Zhong* Abstract BACKGROUND: The oriental leafworm moth, Spodoptera litura Fab. (Lepidoptera: Noctuidae), is a widely distributed polyphagous insect pest in Asia that has been shown to be resistant to various types of insecticide. The newly registered anthranilic diamide cyantraniliprole provided novel insight and great opportunities to control S. litura. RESULTS: In this study, the susceptibilities of S. litura collected from South China to cyantraniliprole were measured by standard leaf-disc bioassay, and obvious variation in susceptibility was observed among the 17 field populations, with LC50 values varying from 0.206 to 1.336 mg AI L−1 . Significant correlations were detected between the LC50 values of cyantraniliprole and chlorantraniliprole (P < 0.05). However, no significant correlation (P > 0.05) was observed between the two anthranilic diamides and other insecticides with different action mechanisms (delcamethrin, chlorpyrifos, indoxacarb and emamectin benzoate). Piperonyl butoxide showed obvious synergism in Lab-Sus, ZC14 and cyantraniliprole-resistant strains, while diethyl maleate and S,S,S-tributylphorotrithioate had no obvious synergistic effects in any of the strains tested. CONCLUSION: These results revealed obvious regional variation in cyantraniliprole susceptibilities among populations of S. litura from different areas, and potential cross-resistance to chlorantraniliprole, which suggested that S. litura could develop resistance to cyantraniliprole. Detoxification enzymes might not be involved in the observed tolerance in field-collected populations and the cyantraniliprole-resistant strain. © 2015 Society of Chemical Industry Keywords: Spodoptera litura; cyantraniliprole; baseline susceptibility; cross-resistance; detoxification mechanisms
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INTRODUCTION
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The oriental leafworm moth, Spodoptera litura Fab. (Lepidoptera: Noctuidae), is a widely distributed polyphagous pest with an extensive host range of economically important crops such as cotton (Gossypium hirsutum L.), groundnut (Arachis villosulicarpa L.), soybean [Glycine max (L.) Merr.], tobacco (Nicotiana tabacum L.), vegetables and others.1,2 In recent years, frequent outbreaks of this pest and crop failures have been more common in the middle and lower reaches of the Yangtze River and southern region of China.3,4 Chemical insecticide control is the most practical way to prevent its damage. However, the extensive and frequent application of insecticide has led to the rapid development of insecticide resistance, which has been confirmed as the major reason for field control failures. High levels of resistance to conventional insecticides, including organophosphates, carbamates and pyrethroids, have been reported in China5,6 and other countries.7 – 10 Recently, resistance to some novel insecticides such as abamectin, emamectin benzoate, fipronil, indoxacarb, spinosad and chlorantraniliprole has also been documented.6,11 – 14 In order to delay the development of resistance, new insecticides with different action mechanisms could be rotated with existing insecticides. Therefore, a novel insecticide cyantraniliprole was registered and commercialised in Pest Manag Sci 2016; 72: 922–928
China 2014, expected to provide a new option for the field control of this insect pest.15 Cyantraniliprole is a second-generation ryanodine receptor insecticide discovered after chlorantraniliprole by DuPont Crop Protection and belonging to the diamide family, group 28 (IRAC, 2012). This new insecticide group acts on binding and activating the ryanodine receptors in insect striate muscle cells, provoking calcium release from internal stores and causing muscular continuous contraction, paralysis and death.16 – 18 Cyantraniliprole has been reported to be effective against a broad spectrum of insect pests, including Lepidoptera, dipteran leafminers, aphids, leafhoppers, psyllids, beetles, whiteflies, thrips and weevils.16 Owing to their structural specificity to insect ryanodine receptors over mammalian counterparts, it has also been shown to be safe for non-target vertebrates.19 In addition, some research evidence
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Correspondence to: Guohua Zhong, Key Laboratory of Pesticide and Chemical Biology, College of Natural Resources and Environment, South China Agricultural University, Guangzhou 510642, China. E-mail: [email protected] Laboratory of Insect Toxicology, Key Laboratory of Pesticide and Chemical Biology, South China Agricultural University, Guangzhou, China
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Susceptibility of the oriental leafworm moth to cyantraniliprole
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Table 1. Locations, sampling sites, dates, host plants and developmental stages of S. litura collected from fields
Strains
Locations
Map reference number
Collection date
Sites
GZ13 HZ13 WY13 DG13 HZ14 YF14 FS14 GZ14 ZC14
Guangzhou, Guangdong Huizhou, Guangdong Wengyuan, Guangdong Dongguan, Guangdong Huizhou, Guangdong Yunfu, Guangdong Foshan, Guangdong Guangzhou, Guangdong Zengcheng, Guangdong
25 May 2013 26 June 2013 2 July 2013 12 September 2013 2 May 2014 27 May 2014 7 June 2014 3 May 2014 22 July 2014
1 2 3 4 2 5 6 1 7
23.21∘ N, 113.25∘ E 23.43∘ N, 114.48∘ E 24.44∘ N, 113.83∘ E 23.83∘ N, 113.74∘ E 23.28∘ N, 113.94∘ E 22.76∘ N, 111.84∘ E 23.04∘ N, 113.19∘ E 23.21∘ N, 113.25∘ E 23.23∘ N, 113.64∘ E
NX14 ZH14 NC14 ND14 FZ14 HK14
Nanxiong, Guangdong Zhuhai, Guangdong Nanchang, Jiangxi Ningde, Fujian Fuzhou, Fujian Haikou, Hainan
26 July 2014 16 August 2014 4 September 2014 15 September 2014 16 September 2014 21 August 2014
8 9 10 11 12 13
25.06∘ N, 114.27∘ E 22.03∘ N, 113.33∘ E 28.76∘ N, 115.84∘ E 27.21∘ N, 119.59∘ E 25.94∘ N, 119.27∘ E 20.00∘ N, 110.51∘ E
GL14 CS14
Guilin, Guangxi Changsha, Hunan
21 September 2014 25 September 2014
14 15
25.93∘ N, 111.09∘ E 28.18∘ N, 113.08∘ E
has indicated that cyantraniliprole presents no cross-resistance with other insecticides used frequently for the control of Bemisia tabaci.20,21 It is crucially important to establish the susceptibility levels of various field populations to newly developed insecticides at the outset, even before their widespread use. The objective of this research was to investigate the susceptibilities of field populations of S. litura to cyantraniliprole in the south of China, and to examine potential cross-resistance patterns to other insecticides used frequently against this pest. In addition, in order to explain the possible mechanisms involved in the resistance to cyantraniliprole, the synergistic effects of synergists were determined.
2
Colocasia esculenta Colocasia esculenta Colocasia esculenta Brassica chinensis L. Asparagus officinalis Arachis hypogaea L. Colocasia esculenta Colocasia esculenta Colocasia esculenta, Solanum melongena L. Colocasia esculenta Colocasia esculenta Colocasia esculenta Colocasia esculenta Colocasia esculenta Nelumbo nucifera Gaerth Colocasia esculenta Colocasia esculenta
Egg mass Egg mass Egg mass Egg mass Second to fifth instars Second to fourth instars Third to fifth instars Second to fourth instars Second to fourth instars
Third to fifth instars Second to fourth instars Third to fifth instars Third to fifth instars Third to fourth instars Third to fourth instars Third to fifth instars Second to fourth instars
10 15 11 12 14
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MATERIALS AND METHODS
8 3 1 7 6 9
4
2
13
Figure 1. Sampling sites of S. litura field populations in the south of China.
on the results of bioassays from the previous generation. The number of larvae used for each generation ranged from 1000 to 1600, depending on availability. After 3 days of exposure, surviving larvae were transferred to fresh artificial diet and reared in the laboratory under the conditions described above. After 13 generations of resistance selection, there was a 24.10-fold increase in LC50 , which was then taken as the cyantraniliprole-resistant (CR) strain. 2.2 Chemicals Six insecticides were used in the present study: 94% cyantraniliprole, 95% chlorantraniliprole and 90% indoxacarb (DuPont Agricultural Chemicals Ltd, Shanghai, China), 97% chlorpyrifos (Zhejiang Xinnong Chemicals Co., Ltd, Hangzhou, China), 98% deltamethrin (Nanjing Redsun Co., Ltd, Nanjing, China) and 95%
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2.1 Insects Seventeen field populations of S. litura were collected from 15 different regions in the south of China. Approximately 15–20 egg masses and 150–300 individuals of second to fifth instars of S. litura were collected from each site (Fig. 1 and Table 1). Larvae of all populations were reared on an artificial diet,15 and adults were fed with 10% sugar solution. All stages were kept under the same standard conditions of 25 ± 1 ∘ C and 60–70% RH with a photoperiod of 16:8 h light:dark (L:D). Larvae of the first generation (F1 ) and second generation (F2 ) were used for susceptibility bioassays. The laboratory population (Lab-Sus) of S. litura was used as the reference population. This strain was obtained by single pair crosses of a field-collected population and reared on artificial diet in the laboratory without exposure to any insecticide for more than 6 years. This laboratory strain was used as the susceptible colony for the first generation of resistance selection. Newly third-instar larvae were used for the toxicity assays and the establishment of resistant lines. The concentration of cyantraniliprole used to select each subsequent generation was the LC50 , which was based Pest Manag Sci 2016; 72: 922–928
Developmental stage
Host plants
www.soci.org emamectin benzoate (Xianzhengda Nantong Crop Preservation Co., Ltd, Nantong, China). The 98% diethyl maleate (DEM), 96% piperonyl butoxide (PBO) and 98% S,S,S-tributylphorotrithioate (DEF) were supplied by Guangzhou Haoma Biotechnology Co., Ltd, Guangzhou, China. 2.3 Bioassay Bioassays were conducted with newly third-instar larvae of S. litura by a standard leaf-disc bioassay.22 A total of 5–6 serial dilutions of insecticide were prepared using distilled water containing 0.1% Triton X-100, and each disc (6.0 cm diameter) from arum leaves was immersed in a test solution for 10 s and allowed to dry at ambient temperature for 1–1.5 h. Control discs were treated with 0.1% Triton X-100 solution only. The leaf discs were placed in individual petri dishes (9 cm in diameter) containing moistened filter paper. Each treatment (concentration) was replicated 3 times, including controls. Ten newly third instars were placed on each leaf disc, and thus the total number of tested larvae per concentration was 30. The bioassays were kept at a temperature of 25 ± 2 ∘ C and 60–70% RH with a photoperiod of 16:8 h L:D. Mortality was assessed after exposure to delcamethrin, chlorpyrifos and emamectin benzoate for 48 h, and to indoxacarb, chlorantraniliprole and cyantraniliprole for 72 h. Larvae were considered to be dead if they failed to make a coordinated movement when prodded with a clean hair brush. 2.4 Synergist bioassays The standard leaf disc bioassay was also used to test the effect of synergists PBO, DEM and DEF on the toxicity of cyantraniliprole to two field strains, Lab-Sus strain and CR strain. Arum leaves treated with 100 mg L−1 of each synergist were fed to third instars for 12 h, and then larvae were assayed for toxicity against cyantraniliprole as described above.
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2.5 Statistical analysis Concentration–mortality responses, lethal concentrations (LC50 , LC90 ), confidence intervals and slopes were calculated by probit analysis with the POLOPlus program.23 In the comparisons of mortality responses between populations, two LC50 values were taken to be significantly different if there was no overlap between their corresponding 95% fiducial limits (FLs).24 Resistance factors (RFs) with 95% confidence limits were calculated using Lab-Sus strain as the factor divisor.25 The insecticide resistance level was described using RFs as reported by Lai et al.:26 susceptibility (RF = 1–3), decreased susceptibility (RF = 3–5), low resistance (RF = 5–10), moderate resistance (RF = 10–40), high resistance (RF = 40–160) and very high resistance (RF > 160). The synergistic ratio was calculated by dividing the LC50 values without synergist by the corresponding LC50 value with synergist, and the synergistic ratios were regarded as significant if their 95% FLs did not include 1.0.27 Correlation between variables was calculated by the Pearson method using the IBM SPSS Statistics software package, and a P-value of less than 0.05 was thought to be statistically significant.
3
RESULTS
3.1 Variation in cyantraniliprole susceptibilities among field populations Seventeen S. litura field populations collected from six Chinese provinces during 2013–2014 (Fig. 1 and Table 1) and a susceptible strain (Lab-Sus) were subjected to bioassays to examine the susceptibility to cyantraniliprole. Obtained results indicated that the Lab-Sus strain exhibited the most significant susceptibility to cyantraniliprole. The LC50 values of cyantraniliprole ranged from 0.206 to 1.336 mg AI L−1 across these field populations, and there was a 6.5-fold difference in LC50 values between the YF14 and GL14 strains (Table 2). The GL14 field strain displayed a 16.1-fold
Table 2. Susceptibility to cyantraniliprole of S. litura collected from fields in the south of China
Strains
na
Slope (SE)b
𝜒2
SS GZ13 HZ13 WY13 DG13 HZ14 YF14 FS14 GZ14 ZC14 NX14 NC14 ND14 FZ14 HK14 GL14 ZH14 CS14
210 210 210 180 180 180 210 210 210 180 180 180 180 210 210 180 180 180
2.239 (0.274) 1.291 (0.222) 2.128 (0.265) 2.066 (0.310) 1.842 (0.293) 1.503 (0.275) 1.365 (0.247) 1.615 (0.226) 1.578 (0.230) 1.735 (0.286) 1.650 (0.324) 1.743 (0.287) 2.161 (0.334) 1.168 (0.182) 1.267 (0.213) 1.488 (0.222) 1.767 (0.286) 1.743 (0.286)
1.597 (4) 0.161 (4) 3.162 (4) 0.633 (3) 0.880 (3) 0.676 (3) 0.062 (4) 5.897 (4) 1.294 (4) 0.407 (3) 0.508 (3) 0.882 (3) 2.090 (3) 0.667 (4) 0.894 (4) 1.582 (3) 0.290 (3) 0.229 (3)
(df )c
LC50 (mg AI L−1 ) (95% FL)
0.083 (0.066–0.106) 0.311 (0.223–0.509) 0.334 (0.191–0.490) 3.286 (1.961–8.273) 0.831 (0.649–1.064) 3.325 (2.345–5.622) 0.483 (0.363–0.625) 2.015 (1.390–3.723) 0.531 (0.390–0.705) 2.634 (1.706–5.621) 0.503 (0.343–0.705) 3.581 (2.052–10.650) 0.206 (0.102–0.315) 1.794 (1.143–3.946) 0.466 (0.274–0.887) 2.899 (1.333–20.078) 0.514 (0.358–0.697) 3.335 (2.155–6.775) 1.250 (0.918–1.702) 6.846 (4.201–16.573) 0.355 (0.188–0.517) 2.123 (1.390–4.668) 0.574 (0.425–0.791) 3.120 (1.881–7.841) 0.905 (0.702–1.242) 3.546 (2.262–7.796) 0.299 (0.142–0.343) 2.870 (1.549–8.287) 1.204 (0.838–1.894) 12.356 (5.897–49.811) 1.336 (0.931–1.937) 9.715 (5.566–24.865) 0.249 (0.184–0.338) 1.324 (0.822–3.099) 0.411 (0.296–0.554) 2.236 (1.412–5.072)
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a Number of insects bioassayed. b Standard error. c Chi-square (P > 0.05); df: degree of freedom. d Resistance factor (RF): LC , LC of the field-collected population/LC , LC 50 90 50 90
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LC90 (mg AI L−1 ) (95% FL)
RF50 (95% FL)d
RF90 (95% FL)d
– 4.0 (2.4–6.6) 10.0 (7.1–14.0) 5.8 (4.1–8.3) 6.4 (4.4–9.2) 6.0 (4.0–9.2) 2.5 (1.4–4.4) 5.6 (3.8–8.2) 6.2 (4.1–9.2) 15.0 (10.2–22.0) 4.3 (2.5–7.2) 6.9 (4.7–10.1) 10.9 (7.6–15.6) 2.8 (1.7–4.5) 14.5 (9.2–22.8) 16.1 (10.5–24.7) 3.0 (2.1–4.4) 4.9 (3.4–7.3)
– 10.6 (4.9–22.9) 10.7 (6.0–19.2) 6.5 (3.5–12.0) 8.4 (4.6–18.2) 11.5 (5.0–26.8) 5.8 (2.9–11.6) 9.3 (4.4–19.9) 10.7 (5.5–21.1) 22.0 (10.4–46.6) 6.8 (3.5–13.4) 10.0 (4.6–21.7) 11.4 (5.6–23.1) 9.2 (3.8–22.3) 39.7 (13.8–114.4) 31.3 (13.9–70.4) 4.2 (2.0–8.9) 7.2 (3.5–14.8)
of the Lab-sus strain.
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Susceptibility of the oriental leafworm moth to cyantraniliprole
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Table 3. The resistance levels of S. litura field populations to frequently used insecticides Delcamethrin Strains SS GZ13 HZ13 WY13 DG13 FS14 ZC14 NX14 NC14 ND14 GL14
LC50
(mg L−1 )
3.602 424.949 105.096 171.425 125.000 39.708 42.300 62.278 89.654 61.692 34.525
Chlorpyrifos RF
1.0 118.0 29.2 47.6 34.7 11.0 11.7 17.3 24.9 17.1 9.6
LC50
(mg L−1 )
2.434 154.198 50.845 276.709 143.601 37.829 34.192 28.053 99.524 71.811 23.264
Indoxacarb RF 1.0 63.4 20.9 113.7 59.0 15.54 14.0 11.5 40.9 29.5 9.6
Emamectin benzoate
(mg L−1 )
RF
3.521 72.336 54.018 88.886 7.739 35.243 14.322 22.583 36.280 40.817 11.011
1.0 20.5 15.3 25.2 2.2 10.0 4.1 6.4 10.3 11.6 3.1
LC50
LC50
(mg L−1 )
RF
0.051 0.216 0.500 1.350 1.564 1.096 0.808 0.411 0.438 0.890 0.862
– 4.2 9.8 26.7 30.6 21.5 15.8 8.1 8.6 17.5 16.9
Chlorantraniliprole LC50 (mg L−1 ) 0.111 0.563 0.856 0.555 0.582 0.240 1.266 0.494 1.349 1.710 1.291
RF – 5.1 7.7 5.0 5.2 2.2 11.4 4.4 12.1 15.3 11.6
Table 4. Pairwise correlation coefficient comparison between log LC50 values of tested insecticides on field populations of S. litura Cyantraniliprole Chlorantraniliprole Delcamethrin Chlorpyrifos Indoxacarb Emamectin benzoate a
0.716a −0.610 −0.466 −0.418 −0.042
Chlorantraniliprole
Delcamethrin
−0.195 −0.111 −0.174 −0.285
0.817a 0.546 −0.478
Chlorpyrifos
0.477 −0.277
Indoxacarb
−0.432
Positive correlation between LC50 values of insecticides at 95% significance level.
resistance to this insecticide, reaching a moderate resistance level, when compared with the Lab-Sus strain. The HZ13, ZC14, ND14 and HK14 strains also showed moderate resistance, and six populations had a low resistance level. Decreased susceptibility was observed in GZ13, NX14, ZH14 and CS14 strains. However, only two populations, YF14 and FZ14, exhibited similar susceptibility to that of Lab-Sus to this compound. No difference was detected in the years 2013 and 2014 from strains collected in Huizhou and Guangzhou. The results of the regression analysis of the slopes obtained for the field-collected populations varied from 1.168 ± 0.182 (FZ14) to 2.161 ± 0.334 (ND14), suggesting a fairly heterogeneous response to cyantraniliprole in the collected populations (Table 2). The LC90 values for cyantraniliprole ranged from 1.324 mg AI L−1 (ZH14) to 12.356 mg AI L−1 (HK14) (Table 2), which provided similar resistance ratios (RF90 = 4.2–39.7-fold) to RF50 values.
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3.3 Synergism tests To analyse the biochemical mechanisms to cyantraniliprole in S. litura, the mixed-function oxidase (MFO) inhibitor PBO, the esterase (EST) inhibitor DEF and the glutathione S-transferase (GST) inhibitor DEM were used for synergism assays in the Lab-Sus strain, the cyantraniliprole-resistant strain (CR) and the two field populations (ZC14 and GL14) with moderate resistance (Table 5). PBO showed obvious synergistic effects in ZC14 and cyantraniliprole-resistant strains, with synergistic ratios (SRs) of 1.8 and 2.1 respectively; however, an obvious and similar synergistic ratio was also observed in the Lab-Sus strain (SR = 1.7). The results indicated that MFO might be implicated in detoxification in the Lab-Sus, ZC14 and cyantraniliprole-resistant strains, but this occurs irrespective of the tolerance of S. litura to cyantraniliprole, which also indicated that rational applications of PBO may increase the efficacy of this product. DEM and DEF had no obvious effect on the toxicities of cyantraniliprole on any of the four strains tested. These results suggested that detoxification metabolism mediated by MFO, GST and EST might not be involved in the observed tolerance to cyantraniliprole in the feld populations ZC14 and GL14 and the cyantraniliprole-resistant strain of S. litura.
4
DISCUSSION AND CONCLUSION
S. litura has become a major insect pest in various vegetables and field crops in China. Multiple classes of insecticides, including
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3.2 Pairwise correlations between toxicities of cyantraniliprole and other insecticides Other than the concentration–mortality responses to cyantraniliprole, the dose–response of ten S. litura field populations to frequently used insecticides, including delcamethrin, chlorpyrifos, indoxacarb, emamectin benzoate and chlorantraniliprole, were also measured using the leaf-dip bioassay (Table 3). The pairwise correlations between the values of log LC50 of cyantraniliprole and log LC50 of the five frequently used insecticides were analysed. The results showed that significant correlation was observed between S. litura susceptibility to cyantraniliprole and chlorantraniliprole (R = 0.716, P < 0.05), which are both members of the anthranilic diamide class. However, no significant correlation was observed between the two
anthranilic diamides and the other four conventional insecticides (delcamethrin, chlorpyrifos, indoxacarb and emamectin benzoate). Moreover, significant correlation between delcamethrin and chlorpyrifos (R = 0.817, P < 0.05) was also determined (Table 4).
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Table 5. Insecticide synergism in the Lab-Sus strain and two field populations of S. litura
Strains
na
Lab-Sus Lab-Sus Lab-Sus Lab-Sus ZC14 ZC14 ZC14 ZC14 GL14 GL14 GL14 GL14 CRe CRe CRe CRe
210 210 180 180 180 210 180 180 180 180 180 180 180 180 180 180
LC50 (mg AI L−1 ) (95% FL)
Pesticides Cyantraniliprole only Cyantraniliprole + PBO Cyantraniliprole + DEF Cyantraniliprole + DEM Cyantraniliprole only Cyantraniliprole + PBO Cyantraniliprole + DEF Cyantraniliprole + DEM Cyantraniliprole only Cyantraniliprole + PBO Cyantraniliprole + DEF Cyantraniliprole + DEM Cyantraniliprole only Cyantraniliprole + PBO Cyantraniliprole + DEF Cyantraniliprole + DEM
0.083 (0.066–0.106) 0.049 (0.038–0.063) 0.068 (0.049–0.095) 0.059 (0.045–0.077) 1.250 (0.918–1.702) 0.709 (0.521–0. 950) 0.878 (0.608–1.194) 1.115 (0.818–1.497) 1.336 (0.931–1.937) 0.941 (0.672–1.304) 1.196 (0.840–1.704) 1.027 (0.777–1.360) 2.001 (1.294–3.093) 0.938 (0.631–1.370) 1.612 (1.125–2.226) 1.267 (0.891–1.692)
Slope (SE)b
𝜒 2 (df )c
Synergistic ratio (95% FL)d
2.239 (0.274) 2.064 (0.260) 1.647 (0.281) 2.020 (0.304) 1.735 (0.286) 1.660 (0.229) 1.655 (0.284) 1.785 (0.289) 1.488 (0.222) 1.610 (0.279) 1.552 (0.228) 1.947 (0.296) 1.225 (0.261) 1.371 (0.267) 1.585 (0.279) 1.795 (0.296)
1.597 (4) 0.219 (4) 0.878 (3) 0.848 (3) 0.407 (3) 0.543 (4) 0.024 (3) 0.325 (2) 1.582 (3) 0.531 (3) 1.135 (3) 0.392 (3) 0.219 (3) 0.118 (3) 0.675 (3) 0.277 (3)
– 1.7 (1.2–2.4)* 1.2 (0.8–1.8) 1.4 (1.0–2.0) – 1.8 (1.2–2.7)* 1.4 (0.9–2.2) 1.1 (0.7–1.7) – 1.4 (0.9–2.3) 1.1 (0.7–1.8) 1.3 (0.8–2.0) – 2.1 (1.2–3.7)* 1.2 (0.7–2.1) 1.5 (1.0–2.6)
a Number of larvae tested. b Standard error.
c Chi-square (P > 0.05); df: degree of freedom. d Synergistic ratio = LC (without synergist)/LC 50 50
(with synergist).
*The synergistic ratio is significant. e CR: cyantraniliprole-resistant strain.
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traditional and some novel selective chemistry pesticides, have been reported as failing to control this species. The recent commercialisation of cyantraniliprole provided an excellent strategy for the management of S. litura. Our previous experiment demonstrated that sublethal concentrations of cyantraniliprole could significantly affect the growth and development of S. litura.15 The present study established the baseline susceptibility of S. litura to cyantraniliprole in the south of China, before large-scale application of this insecticide. To the best of our knowledge, this is the first study to report the regional differences in susceptibility of S. litura to cyantraniliprole and obvious variation in tolerance in field populations (Fig. 1 and Tables 1 and 2). The present results clearly illustrated that several regional populations of S. litura had developed moderate resistance to this compound. Thus, this study provided valuable data for resistance monitoring and management in the future. The detection of regional differences in susceptibility to an insecticide before its widespread use in the field has been reported for metaflumizone,28 spinosad29 and chlorantraniliprole.14,26,30 – 33 Susceptibility variation in field populations of four insect species to cyantraniliprole has been reported recently. Caballero et al.34 observed that seven field populations of Bemisia tabaci biotype B (Gennadius) collected from southern Florida showed similar susceptibilities to cyantraniliprole. However, Grávalos et al.21 tested the same insecticide for Mediterranean strains of Bemisia tabaci and found that the LC50 values for nymphs from 14 field populations varied from 0.011 to 0.116 mg L−1 , a 10.5-fold natural variability. Other variations in cyantraniliprole susceptibility were observed in populations of Tuta absoluta (Lepidoptera: Gelechiidae),35 Bactrocera dorsalis (Diptera: Tephritidae)36 and Frankliniella occidentalis (Pergande)37 respectively. The present study found a wide range of variation (6.5-fold) in the susceptibility of S. litura from different areas where this compound had been
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introduced only for a short time (Table 2). Resistance selection experiments showed that S. litura might develop resistance to cyantraniliprole under continuous exposure (unpublished data). Therefore, more attention should be paid to the resistance risk of cyantraniliprole. The 17 S. litura strains tested were considered to be representatives of field populations causing widespread damage in the south of China (Fig. 1 and Table 1). The obversed 6.5-fold variation in susceptibility to cyantraniliprole from different areas implied that resistance might be caused by natural variation, different insecticide application history or other factors. To analyse the relationship between cyantraniliprole tolerance and past insecticide applications, pairwise correlations between LC50 values of cyantraniliprole and five frequently used insecticides were examined. No significant correlation (P > 0.05) was found between S. litura susceptibility to cyantraniliprole tolerance and the resistance to insecticides with other mechanisms of action (delcamethrin, chlorpyrifos, indoxacarb and emamectin benzoate) that were usually applied to control S. litura field populations in China, suggesting that the existing resistance mechanisms do not affect the performance of such anthranilic diamides. Lack of cross-resistance between cyantraniliprole and conventional insecticides has also been reported in B. tabaci from Arizona and Mediterranean strains.20,21 However, significant correlations (P < 0.05) were observed between cyantraniliprole and chlorantraniliprole, suggesting that a high risk of cross-resistance might be developed. Owing to the fact that both insecticides belong to group 28 (IRAC, 2012) and have the same mode of action, when resistance occurs, this situation will increase the risk of cross-resistance. However, only one resistant field strain has been identified. Recently, high levels of resistance to chlorantraniliprole and middle levels of resistance to cyantraniliprole have been reported for Plutella xylostella (L.) (Lepidoptera: Plutellidae) populations collected
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Susceptibility of the oriental leafworm moth to cyantraniliprole from South China.38 – 40 P. xylostella and S. litura could seriously mix-injure brassicaceous vegetables in the south of China all the year around, where the same insecticides are usually applied for controlling these two insect pests. Collectively, although the field-collected populations did not show a high resistance level to cyantraniliprole, a diamide should be used cautiously for controlling brassicaceous vegetable insect pests (e.g. P. xylostella and S. litura) in this region before the susceptibility of these pests to this class of compounds is restored. Understanding the detoxification metabolism mechanisms conferring insecticide resistance in field populations is necessary for resistance management and integrated pest management tactics. One of the most important factors of insect resistance is the increase in metabolic detoxification processes of the insecticide by MFO, EST and GST.41 In the present study, PBO showed obvious synergism in ZC14 and cyantraniliprole-resistant strains; however, an obvious synergistic ratio was also observed in the Lab-Sus strain. DEM and DEF had no obvious synergistic effects in any of the four strains. These results suggested that the detoxification enzymes MFO, EST and GST may not be involved in the observed tolerance of S. litura to cyantraniliprole. Similarly, a synergism assay in P. xylostella31 and Spodoptera exigua (Leidoptera: Noctuidae)26 demonstrated that MFO, EST and GST were not the main contributors to chlorantraniliprole resistance. Therefore, there might be some other mechanisms involved in the resistance to this class of insecticides in the tested insects. Owing to its broad spectrum, high efficiency and novel action mechanism, the environmental friendly insecticide cyantraniliprole has been well received by crop growers in China. The use of this compound will be more widespread in future. The bioassay results showed that cyantraniliprole is still effective in controlling S. litura in the south of China, but a wide range of variation in the susceptibility of field populations exists, and cross-resistance to chlorantraniliprole is possible. Therefore, susceptibility of S. litura to cyantraniliprole may be retained by rotating insecticides with different mechanisms of action. Simultaneously, an effective resistance management strategy should be put in place as early as possible to avoid/retard the further development of insect pest resistance to cyantraniliprole.
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ACKNOWLEDGEMENTS We thank Prof. Xiaomao Zhou (Hunan Agricultural University), Zhonghua Xiong (Jiangxi Agricultural University) and Gang Feng (Chinese Academy of Tropical Agricultural Sciences) for assistance in insect collection. This study was supported by a grant from the Guangdong Province Science and Technology Plan project (2012A020100009).
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