J. Pestic. Sci. 39(1), 7–13 (2014) DOI: 10.1584/jpestics.D13-053

Original Article

Resistant levels of Spodoptera exigua to eight various insecticides in ,

Peng Zhang, Ming Gao, Wei Mu,* Chao Zhou and Xiu-Huan Li

College of Plant Protection, Shandong Agricultural University, Tai’an, Shandong 271018, P. R. China (Received July 18, 2013; Accepted November 7, 2013)

Spodoptera exigua is a major insect pest of vegetables in Shandong, China, and has been reported to develop resistance to many insecticides. The present study was carried out in 2011–2012 to evaluate the resistance ratios (RRs) to eight insecticides in S. ex- igua populations from five regions in Shandong. A standard leaf-dip method showed no resistance to chlorfenapyr (RR< 2). RRs to emamectin benzoate, indoxacarb, and spinosyn were in the ranges of 3.00 to 37.4-fold, 8.63 to 84.1-fold, and 9.27 to 86.2-fold, respectively. S. exigua showed high resistance to the insect growth regulators (IGR) tebufenozide and methoxyfenozide. No re- sistance to the diamide insecticides chlorantraniliprole and flubendiamide was found. The insecticides chlorfenapyr, emamectin benzoate, indoxacarb, spinosyn, chlorantraniliprole, and flubendiamide had no, very low, low, and moderate resistance levels for most of the tested populations. Due to these characteristics they could be used in pest management programs supplemented with physical and biological control measures. © Pesticide Science Society of Japan Keywords: Spodoptera exigua, insecticide resistance, insecticides, China.

tance. For a more effective application of new insecticides, mon- Introduction itoring of resistance in S. exigua to these compounds is crucial. The beet armyworm, Spodoptera exigua (Hübner), is a polypha- The present study was initiated to determine the resistance of S. gous insect pest that infests a wide range of crops in tropical and exigua to chlorantraniliprole, flubendiamide, emamectin benzo- subtropical regions of the world.1) Under favorable conditions, ate, chlorfenapyr, spinosyn, indoxacarb, tebufenozide and me- its populations can expand rapidly and move across fields like an thoxyfenozid in Shandong, China. army, leading to its name “armyworm”.2) In China, the damage Materials and Methods caused by S. exigua has continually increased and S. exigua has attacked numerous economically important crops, causing great 1. Insects losses in agriculture since the 1980s.3) In recent years, mainly Field populations of S. exigua were collected from five vegeta- due to its development of insecticide resistance and subsequent ble production bases in Shandong, including Tai’an, , control failures, its outbreaks have become more common in the , Anqiu, and Zhangqiu (Fig. 1 and Table 1) between province of Shandong, especially in vegetable-growing areas. Al- July 2011 and October 2012. Third- to fifth-instar larvae were though physical control and natural predators may reduce field collected by walking through a 3-ha block of a particular crop populations of S. exigua,4) the current level of control is often in a zigzag manner in order to obtain a mixed population. To insufficient to avoid economic damage, especially for high-value get sufficient numbers of larvae, in some areas moths were col- crops. This makes insecticide control indispensable for insect lected using light traps and butterfly nets. The moths were kept pest management (IPM) programs of S. exigua. Due to resis- in cages with meshed sides to maintain ventilation. The adults tance, many conventional insecticides, such as pyrethroids and were fed on a solution containing sucrose (100 g/L) and a vita- organophosphorus insecticides, have failed to provide adequate min solution (20 mL/L) in a soaked cotton wool ball. All larvae control in recent years.4–6) Some new insecticides have been rap- were fed with a semi-synthetic diet, slightly modified from Mu idly introduced into S. exigua control, which feature low toxicity, et al.9) Third-instar larvae of the next generation, which repre- high activity, new modes of action, and environmental safety.7,8) sented the progeny of the field-collected insects, were used for No pesticides can avoid the development of pesticide resis- the resistance studies. All instars of the insects were reared in the laboratory at 27±​1°C and 50–75% relative humidity (RH) * To whom correspondence should be addressed. with a 14 hr : 10 hr L : D photoperiod. An insecticide-susceptible E-mail: [email protected] colony as a negative control was obtained from the Insti- Published online January 22, 2014 tute of Vegetable Science, China, where it had been maintained © Pesticide Science Society of Japan in a mass-rearing environment for 30 years. 8 P. Zhang et al. Journal of Pesticide Science

2. Insecticides using a standard leaf-dip bioassay method.10) Serial dilutions as The following commercial formulations of the insecticides were mg/L of the active ingredient of the test compounds were pre- used in bioassays: chlorantraniliprole (200 g/L SC [suspending pared using tap water. Cabbage leaf discs (1-cm diameter) were agent]; DuPont Agriculture Co., ), flubendiamide (20% cut and dipped into the test solutions for 10 sec with gentle ag- WDG [water dispersible granule]; Janpen Pesticide Co.), chlorf- itation, and then allowed to dry between two pieces of paper enapyr (100 g/L, SC, BASF AG, Germany), indoxacarb (200 g/L, towel. At least six concentrations and four replications (20 larvae SC, DuPont Agriculture Co., Shanghai, China), spinosyn per replication) were used to estimate each concentration’s mor- (200 g/L, SC, Dow Agro Sci., USA), emamectin benzoate (10 g/L, tality line. Controls for each insecticide were treated with water. EC [emulsifiable concentrate], Lvba Chemistry Co., Shandong, Before and after treatment, larvae were maintained at a constant China), tebufenozide (200 g/L, SC, Dow Agro Sci., USA), and temperature of 27±​1°C and an RH of 50–75% with a photope- methoxyfenozide (200 g/L, SC, Dow Agro Sci., USA). riod of 14 hr : 10 hr L : D. Mortality was assessed after 48 hr for general insecticides and after 72 hr for insect growth regulator 3. Bioassays (IGR) insecticides. Larvae were considered dead if they were un- Bioassays were conducted on newly emerged third-instar larvae able to move in a coordinated manner when disturbed with the of S. exigua from the first filial generation of laboratory cultures tip of a pencil.11)

4. Statistical analysis Data were corrected for control mortality using Abbott’s formula12) before analysis, and data were analyzed using the SAS/STAT® version 6.12 (SAS Institute Inc., 1997). Statistical

differences between LC50 values were determined using the pres- ence or absence of overlap in the 95% confidence limits. Resis-

tance ratios (RRs) were calculated by dividing the LC50 of a field population by that of the susceptible population. The resistance level was considered as: none at RR <2-fold, very low at RR=​ 2–10-fold, low at RR=​11–20-fold, moderate at RR=​21–50-fold, high at RR=​51–100-fold, and very high at RR >100-fold.10) Results 1. Toxicity of insecticides to the laboratory strain Fig. 1. Location of collections of S. exigua in China. We tested the toxicity of eight various insecticides to the labora-

Table 1. Locations, sampling dates, and host plants of S. exigua collected from fields

Location Collection date No. collected Sites Host plants Tai’an July. 2011 Aug. 2012 600 500 36.18°N, 117.13°E Cabbage Zhangqiu Sep. 2011 Sep. 2012 460 700 36.72°N, 117.53°E Scallion Anqiu Aug. 2011 Sep. 2012 520 400 35.09°N, 117.17°E Scallion Tengzhou Sep. 2011 Oct. 2012 500 600 34.86°N, 117.57°E Ginger Binzhou Oct. 2011 Oct. 2012 600 850 37.36°N, 118.03°E Ginger

Table 2. Susceptible toxicity baseline of S. exigua to eight various insecticides

Fit of probit line 95% Fiducial limits Insecticides LC50 (mg/L) Slop±S.E. χ2 df (Lower–Upper) Emamectin Benzoate 1.44±0.20 3.82 5 0.0305 0.0300–0.0402 Methoxyfenozide 1.65±0.34 4.33 4 0.201 0.184–0.232 Chlorantraniliprole 1.83±0.59 5.67 4 0.304 0.241–0.396 Indoxacarb 1.97±0.43 5.14 4 0.591 0.283–1.25 Flubendiamide 2.76±0.07 3.44 5 0.632 0.472–0.847 Spinosyn 1.95±0.26 5.32 4 1.23 0.862–1.74 Tebufenozide 1.96±0.35 2.45 5 1.67 1.61–1.74 Chlorfenapyr 2.55±0.24 3.42 5 12.3 7.18–21.2 Vol. 39, No. 1, 7–13 (2014) Resistant levels of Spodoptera exigua to eight various insecticides in Shandong, China 9

Table 3. Susceptibility of S. exigua larvae of different populations in Shandong China to chlorfenapyr and emamectin benzoate

Fit of probit line 95% Resistance Resistance Insecticides Year Poppulation LC50 (mg/L) Fiducial 2 ratios level Slop±S.E. χ df limits Chlorfenapyr 2011 Tai’an 3.18±0.46 4.23 5 12.0 10.1–14.5 0.976 None Zhangqiu 4.04±0.40 5.14 4 11.7 10.6–13.0 0.951 None Anqiu 1.67±0.24 3.38 4 15.9 11.5–23.6 1.29 None Tengzhou 4.00±0.40 4.86 5 11.9 10.8–13.2 0.967 None Binzhou 1.89±0.45 6.20 4 12.6 9.48–17.0 1.02 None 2012 Tai’an 2.50±0.32 4.02 6 18.0 15.3–21.7 1.46 None Zhangqiu 2.66±0.34 1.87 5 13.0 11.3–15.0 1.06 None Anqiu 1.58±0.25 3.76 5 7.90 5.54–11.2 0.642 None Tengzhou 3.90±0.39 1.20 4 8.80 7.18–10.4 0.715 None Binzhou 2.15±0.47 3.45 5 18.7 14.7–27.4 1.52 None Emamectin 2011 Tai’an 1.83±0.27 4.22 5 0.122 0.0814–0.149 4.00 Very low Benzoate Anqiu 1.83±0.27 3.80 4 0.220 0.162–0.303 7.21 Very low Zhangqiu 1.46±0.18 2.78 4 0.424 0.321–0.544 13.9 Low Tengzhou 1.54±0.16 5.40 4 0.683 0.502–0.971 22.4 Moderate Binzhou 2.63±0.38 2.21 6 0.902 0.724–1.00 29.6 Moderate 2012 Tai’an 2.57±0.26 1.90 5 0.0905 0.0721–0.103 3.00 Very low Anqiu 1.48±0.25 4.36 5 0.283 0.194–0.402 9.28 Very low Zhangqiu 1.53±0.18 6.75 4 0.331 0.251–0.420 10.9 Low Tengzhou 1.11±0.15 6.23 4 0.322 0.234–0.422 10.6 Low Binzhou 1.47±0.31 5.48 5 1.14 0.810–1.78 37.4 Moderate

a Resistance ratio (RR ) estimated as RR=LC50 of field strain /LC50 of the insecticide-susceptible strain.

Table 4. Susceptibility of S. exigua larvae of different populations in Shandong China to chlorantraniliprole and flubendiamide

Fit of probit line 95% LC Resistance Resistance Insecticides Year Poppulation 50 Fiducial 2 (mg/L) ratios level Slop±S.E. χ df limits Chlorantraniliprole 2011 Anqiu 1.97±0.32 5.24 5 0.262 0.191–0.323 0.862 None Tai’an 1.66±0.20 5.86 5 1.67 1.30–2.18 5.49 Very low Tengzhou 1.06±0.11 5.33 5 1.80 1.30–2.44 5.92 Very low Zhangqiu 1.13±0.11 6.15 4 1.98 1.47–2.63 6.51 Very low Binzhou 2.95±0.49 2.46 4 6.03 4.99–7.23 19.8 Moderate 2012 Anqiu 2.35±0.47 3.42 4 0.633 0.502–0.801 2.08 Very low Tai’an 1.73±0.19 5.54 4 2.12 1.68–2.61 6.97 Very low Tengzhou 0.852±0.11 5.53 5 4.42 3.06–6.67 14.5 Low Zhangqiu 1.10±0.11 4.34 4 5.02 3.72–7.05 16.5 Low Binzhou 2.36±0.48 2.75 5 8.63 6.96–11.7 28.4 Moderate Flubendiamide 2011 Anqiu 1.22±0.28 6.44 4 0.771 0.510–1.11 1.22 None Binzhou 2.28±0.48 3.25 4 3.51 2.51–4.38 5.55 Very low Tengzhou 1.81±0.22 5.62 6 5.30 4.34–6.30 8.39 Very low Zhangqiu 2.02±0.23 2.67 4 6.53 5.34–7.85 10.3 Low Tai’an 1.71±0.32 4.53 4 11.6 8.62–17.0 18.4 Moderate 2012 Anqiu 1.22±0.28 3.44 4 1.03 0.82–1.24 1.63 None Binzhou 1.80±0.46 2.34 4 7.26 5.51–11.8 11.5 Low Tengzhou 1.79±0.22 2.65 4 9.73 8.16–11.9 15.4 Low Zhangqiu 1.87±0.24 5.36 4 10.7 8.77–13.2 16.9 Low Tai’an 2.00±0.28 4.59 5 13.7 11.1–17.6 21.7 Moderate 10 P. Zhang et al. Journal of Pesticide Science tory strain in 2011 (Table 2). The laboratory colony was suscep- <2.00-fold). The resistance ratio of flubendiamide changed in tible to all eight insecticides and was used for calculating the the other four regions in 2011–2012, increasing from 5.55-fold resistance ratios. Emamectin benzoate had the highest toxicity to 11.5-fold in Binzhou, from 10.3-fold to 16.9-fold in Zhangqiu, with an LC50 of 0.03 mg/L. Indoxacarb, spinosyn, tebufenozide, from 8.39-fold to 15.4-fold in Tengzhou, and from 18.4-fold to methoxyfenozide, chlorantraniliprole, and flubendiamide had 21.7-fold in Tai’an.

LC50 values between 0.20 and 0.63 mg/L. Spinosyn and tebufe- nozide showed moderate levels of toxicity (LC50=1.23 mg/L and 4. Indoxacarb and spinosyn 1.67 mg/L, respectively). Chlorfenapyr was the least toxic among Five populations from Shandong had moderate resistance levels, the tested insecticides (LC50=12.3 mg/L). two had high resistance levels, two showed low resistance levels, and two had very low resistance levels (Table 5). No significant 2. Chlorfenapyr and emamectin benzoate changes toward indoxacarb were found in the five regions in Toxicity results of the various chemistry insecticides against dif- 2011–2012. Tests with spinosyn (Table 5) revealed differences in ferent populations are shown in Table 3. In five regions, all pop- the five regions. S. exigua showed a high resistance to spinosyn ulations showed no resistance to chlorfenapyr (RR <2), suggest- in Tai’an and Binzhou, with 86.2-fold and 68.1-fold resistance ing that S. exigua was susceptible to chlorfenapyr. Chlorfena- ratios, respectively, in 2012. Moderate resistance levels were pyr has been used extensively in China, yet there are no reports found in Zhangqiu and Anqiu (20≤ RR <50). The populations of resistance against it. There were three regions in Tai’an and collected from Tengzhou showed low or very low resistance in Anqiu in which low to moderate resistance to emamectin ben- 2011–2012. zoate was observed, although at very low levels (2≤ RR <10). 5. Tebufenozide and methoxyfenozide 3. Chlorantraniliprole and flubendiamide Tebufenozide and methoxyfenozide are insect growth regu- In most tested populations, no resistance to chlorantraniliprole lators. They have been used widely in Shandong, especially in or flubendiamide was found (Table 4).S. exigua from Binzhou vegetable-growing areas. Our data (Table 6) revealed high and revealed moderate resistance to chlorantraniliprole, with resis- very high resistance ratios to tebufenozide. S. exigua from all tance levels ranging from 19.8-fold to 28.4-fold. Compared to ten populations tested between 2011 and 2012 showed very high chlorantraniliprole, flubendiamide, the second diamide insec- resistance to methoxyfenozide, especially in Zhangqiu and Teng- ticide had lower toxicity levels in most populations. In Anqiu, zhou (RR=672-​ and 612-fold in 2011 and 567- and 622-fold in the population showed no resistance to flubendiamide (RR 2012, respectively).

Table 5. Susceptibility of S. exigua larvae of different populations in Shandong China to indoxacarb and spinosyn

Fit of probit line 95% LC Resistance Resistance Insecticides Year Poppulation 50 Fiducial 2 (mg/L) ratios level Slop±S.E. χ df limits Indoxacarb 2011 Zhangqiu 1.44±0.16 4.45 5 5.45 3.62–8.35 9.22 Very low Tengzhou 1.36±0.16 3,33 4 7.66 5.03–12.5 13.0 Low Tai’an 2.93±0.51 1.20 4 12.1 9.98–16.0 20.5 Moderate Anqiu 2.00±0.32 5.17 5 17.6 13.2–22.0 29.8 Moderate Binzhou 1.94±0.42 3.78 5 37.3 28.6–50.4 63.1 High 2012 Tengzhou 2.84±0.32 4.07 5 5.10 4.38–5.78 8.63 Very low Zhangqiu 1.51±0.17 1.98 4 6.20 4.20–9.69 10.5 Low Tai’an 3.43±0.42 4.20 6 19.7 17.4–22.7 33.3 Moderate Anqiu 1.66±0.30 3.67 4 28.9 22.1–38.6 48.9 Moderate Binzhou 2.14±0.43 6.45 4 49.7 39.1–70.3 84.1 High Spinosyn 2011 Tengzhou 1.77±0.22 4.48 5 11.4 8.93–14.0 9.27 Low Zhangqiu 2.30±0.47 1.88 4 25.4 19.2–31.7 20.7 Moderate Anqiu 2.49±0.34 5.63 4 27.0 22.9–31.2 22.0 Moderate Binzhou 1.84±0.30 4.47 5 48.0 37.5–62.0 39.0 Moderate Tai’an 2.44±0.50 3.77 6 93.0 75.1–128 75.6 High 2012 Tengzhou 1.86±0.24 5.12 5 18.8 15.4–23.3 15.3 Low Anqiu 3.25± 0.37 4.66 4 25.8 22.7–29.1 21.0 Moderate Zhangqiu 3.10±0.50 1.10 4 33.9 28.5–40.8 27.6 Moderate Binzhou 2.47±0.48 2.70 5 83.8 68.2–111 68.1 High Tai’an 2.53±0.39 2.50 6 106 89.1–137 86.2 High Vol. 39, No. 1, 7–13 (2014) Resistant levels of Spodoptera exigua to eight various insecticides in Shandong, China 11

Table 6. Susceptibility of S. exigua larvae of different populations in Shandong China to tebufenozide and methoxyfenozide

Fit of probit line 95% LC Resistance Resistance Insecticides Year Poppulation 50 Fiducial 2 (mg/L) ratios level Slop±S.E. χ df limits Tebufenozide 2011 Anqiu 1.46±0.30 3.78 5 86.9 49.9–124 52.0 High Tai’an 3.33±0.57 4.50 4 96.3 79.4–113 57.7 High Zhangqiu 1.45±0.22 5.34 4 134 101–199 80.2 High Tengzhou 1.54±0.23 4.12 5 152 115–227 91.0 High Binzhou 1.10±0.30 5.32 5 203 128–375 122 Very high 2012 Tengzhou 1.88±0.20 6.44 4 28.2 23.4–33.7 16.9 Low Zhangqiu 1.50±0.22 5.57 4 97.5 76.2–133 58.4 High Tai’an 4.25±0.51 1.22 5 140 127–156 83.8 High Anqiu 1.56±0.31 3.50 4 199 143–292 119 Very high Binzhou 1.64±0.32 7.45 4 210 154–304 126 Very high Methoxy- 2011 Anqiu 2.08±0.33 3.93 5 21.0 16.3–27.8 104 Very high fenozide Binzhou 1.52±0.26 4.24 4 27.4 18.5–36.8 136 Very high Tai’an 2.26±0.30 2.40 4 39.8 31.9–49.5 198 Very high Tengzhou 2.54±0.35 5.31 6 123 107–144 612 Very high Zhangqiu 2.56±0.35 4.41 5 135 117–158 672 Very high 2012 Anqiu 1.52±0.30 2.34 4 26.3 18.8–40.5 131 Very high Tai’an 4.30±0.45 5.57 5 27.9 25.1–31.0 139 Very high Binzhou 1.57±0.24 2.27 4 52.5 39.3–71.4 261 Very high Zhangqiu 2.07±0.33 1.56 5 114 94.4–136 567 Very high Tengzhou 3.29±0.37 3.67 5 125 111–141 622 Very high

obtained after selection for 12 generations in the laboratory. The Discussion spider mite Tetranychus urticae has been shown to reach 10-fold The present study was conducted between 2011 and 2012, and levels of resistance to chlorfenapyr after treatment for 12 genera- demonstrated that the Shandong populations of S. exigua have tions.15) Therefore, chlorfenapyr should be applied for popula- varying degrees of resistance to eight insecticides. However, no tion management of S. exigua. resistance to chlorfenapyr was found in Shandong. In China, S. Emamectin benzoate belongs to the avermectin group of pes- exigua populations resistant to conventional insecticides (beta- ticides, which act as chloride channel activators.16) Although cypermethrin, chlorpyrifos and methomyl),4) emamectin ben- moderate resistance to emamectin benzoate was found in 8) zoate, indoxacarb, spinosyn, tebufenozide, chlorantraniliprole, Binzhou, the LC50 value was very low (LC50 <1.20 mg/L). No and flubendiamide have been found.13) This suggests that popu- increase was observed from 2011 to 2012, indicating that ema- lations of this species in Shandong have the potential to develop mectin benzoate could also be used to manage S. exigua. Zhou resistance to a wide range of compounds. In recent years, con- et al.4) found that S. exigua showed low resistance to emamectin current outbreaks of this pest in Shandong have mostly been benzoate in Shandong between 2008 and 2010. Likewise, in Pak- associated with the development of resistance to various insec- istan, emamectin benzoate is considered an effective insecticide ticides. In Shandong, conventional insecticides, such as organo- for most populations, which exhibited very low to low levels of phosphorus compounds, pyrethroids, and carbamate insecti- resistance in nine populations and medium levels of resistance cides, have been widely used for pest control for more than 20 in three out of 15 populations.17) Emamectin benzoate is thus years. However, due to long-term usage, the control effect on S. considered an effective tool for the management of S. exigua. exigua in the field has decreased rapidly. Many new pesticides Indoxacarb acts as a voltage-dependent sodium channel with high toxicity to S. exigua have been favorably received by blocker, and it belongs to the group of oxadiazine insecticides.18) farmers. Many pests have the potential to develop resistance to indoxa- The development rate of resistance by insects relies on the fac- carb. After selection against indoxacarb for six generations, a tors of selection pressure by insecticides, initial frequency of re- field population of Plutella xylostella evolved a 2595-fold in- sistant genotypes, and the fitness of individual insects. No resis- creased resistance as compared to a susceptible population.19) tance to chlorfenapyr was found in Shandong populations, per- Musca domestica20) and S. exigua5) can also develop high levels haps because it is very difficult to develop resistance against this of resistance to indoxacarb in a relatively short period of time. compound. Zhang et al.14) indicated that an S. exigua strain with Indoxacarb resistance increased in Shandong, with moderate very low levels of resistance (RR=​4.72-fold) to chlorfenapyr was levels of resistance found in four populations and high resistance 12 P. Zhang et al. Journal of Pesticide Science levels found in two out of 10 populations tested. Therefore, it interesting because flubendiamide is rarely used in Shandong. should be applied only sparsely. Flubendiamide resistance in S. exigua might be a typical case Spinosad belongs to the spinosyn group and acts on nicotinic of cross-resistance acquired chlorantraniliprole. Flubendiamide acetylcholine and gamma-aminobutyric acid (GABA) recep- has the same target and mechanism as chlorantraniliprole,6) and tors.20,21) It has been found to be effective against pests of the cross-resistance between chlorantraniliprole and flubendiamide orders Lepidoptera, Diptera, Thysanoptera, and some species in P. xylostella has been reported previously.29) of Coleoptera and Orthoptera.22,23) In our study, eight out of 10 Chemical control plays an important role in the control of populations of S. exigua exhibited moderate to high resistance S. exigua in Shandong. Plant growers are already experiencing to spinosad, while only two populations showed low resistance failures in controlling S. exigua. Conventional insecticides have levels. Although spinosad has a novel action mechanism and no been replaced with new and more potent compounds that em- cross-resistance to many different insecticides, many pest spe- ploy novel modes of action. However, some S. exigua popula- cies have still generated different levels of resistance. In Mex- tions have developed resistance to some of the new insecticides ico, Osorio et al.22) demonstrated that S. exigua exhibited low on different levels. Using chemicals is insufficient for successful to moderate resistance to spinosad, increasing from 16-fold to control and pest management; biological and physical control 37-fold. Similarly, Liriomyza trifolii produced high to very high measures should be applied based on the occurrence, regularity, resistance to spinosad in greenhouse ornamental plants in the and ecology of S. exigua. Using radar, a simultaneously operated United States.24) searchlight trap, and a ground light trap at a site in Langfang Tebufenozide and methoxyfenozide are insect growth regula- in 2002, Feng et al.30) observed the migration of S. exigua and tors, which are highly effective against Lepidopteran pests and indicated that the insect was a high-altitude nocturnal wind- have an excellent environmental and mammalian toxicological borne migrant in northern China. Thus, trapping and killing the profile.25) In recent years, tebufenozide and methoxyfenozide adults in UV light traps is an effective control measure during have been widely used to control S. exigua in vegetable fields in the eclosion and migration period. The authors have observed Shandong. However, as they were overused to control insects, natural predators of S. exigua in the field, such as Harmonia axy- their effects on S. exigua decreased rapidly. Almost all popula- ridis, Chrysoperla sinica, Snelleniua manila and Telenomus remus tions in Shandong exhibited high to very high resistance ratios. Nixon, as they collected larvae and pupae from most of the areas Jia and Shen indicated that a tebufenozide-resistant strain of during the study period. Due to their high selectivity, new in- S. exigua had a high cross-resistance (RR=​77.4-fold) to me- secticides, such as chlorantraniliprole, flubendiamide, spinosyn, thoxyfenozide, and it has proved difficult to recover sensitivity tebufenozide and methoxyfenozide, should help to protect these to tebufenozide during a short period.7) The pesticide selection natural predators. pressure and cross-resistance were the main causes of resistance Acknowledgements to tebufenozide and methoxyfenozide. 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