Resistance Risk, Cross Resistance and Sublethal Effects of Methoxyfenozide on Rice Stemborers (Chilo suppressalis)

doi:10.16819/j.1001-7216.2023.220804

Abstract

Abstract:

【Objective】 We aim to investigate the resistance risk, cross resistance, and sublethal effects of methoxyfenozide on Chilo suppressalis.【Method】 We established the susceptibility baseline of the rice stem borer to methoxyfenozide using rice seedling dipping method and diet incorporation method, respectively. We assessed its resistance risk using diet incorporation method and determined the cross resistance of methoxyfenozide-resistant C. suppressalis population to RH-5849, tebufenozide and fufenozide. Then, we evaluated the effects of sublethal concentration of RH-5849 and methoxyfenozide on the development and reproduction of C. suppressalis using rice seedling dipping method. 【Results】 The results showed that it took 7.7, 6.3, 5.2, 4.4, and 3.5 generations for C. suppressalis to acquire ten-fold resistance to methoxyfenozide when the realized heritability (h²) was 0.402, the slope was 2.451 and the average selective pressure was 50%, 60%, 70%, 80%, and 90%. The bioassay results showed that Yuyao-19 (YY-19) population with a moderate level of resistance to methoxyfenozide (RR=73.4) exhibited moderate cross resistance to fufenozide (RR=24.7) and tebufenozide (RR=26.1), and lower cross-resistance to RH-5849 (RR=2.9). The larval development duration significantly increased but the pupation rate and the pupal weight remarkably decreased after the treatment of sublethal dose of RH-5849 and methoxyfenozide to 2^nd instar larvae of C. suppressalis. Moreover, the eclosion rate and the egg laying number per female of F₀ and F₁ generations decreased significantly after the treatment of sublethal dose of methoxyfenozide. 【Conclusion】 C. suppressalis has a high resistance risk to methoxyfenozide. The field population which exhibits a moderate level of resistance to methoxyfenozide has cross-resistance with other diacylhydrazines. A significant fitness cost is present in rice stem borers treated with a sublethal dose of methoxyfenozide.

Key words: Chilo suppressalis, methoxyfenozide, resistance risk assessment, cross resistance, fitness cost

摘要：

【目的】 明确二化螟对甲氧虫酰肼的抗性风险、交互抗性及亚致死效应。【方法】 分别采用饲料混药法和稻苗浸渍法建立了二化螟初孵和2龄幼虫对甲氧虫酰肼的敏感基线，采用饲料混药法评估了二化螟对甲氧虫酰肼的抗性风险；采用稻苗浸渍法测定了抗甲氧虫酰肼二化螟田间种群2龄幼虫对抑食肼、虫酰肼和呋喃虫酰肼的交互抗性以及亚致死浓度抑食肼和甲氧虫酰肼对二化螟生长发育与繁殖的影响。【结果】 当抗性现实遗传力(h²)为0.402，斜率为2.451，平均选择压力分别为50%、60%、70%、80%和90%时，二化螟对甲氧虫酰肼的抗性上升10倍分别需要7.7、6.3、5.2、4.4和3.5代；2019年采自余姚的二化螟田间种群(YY-19)对甲氧虫酰肼处于中等水平抗性(RR = 73.4倍)，对呋喃虫酰肼(RR = 24.7倍)和虫酰肼(RR = 26.1倍)同样存在中等水平的交互抗性，对抑食肼(RR=2.9倍)有低水平交互抗性；采用亚致死浓度(LC₂₅)抑食肼和甲氧虫酰肼处理二化螟2龄幼虫后，幼虫历期显著增加，化蛹率和F₀代雌蛹重均显著降低。此外，F₀和F₁代的羽化率和单雌产卵量在经亚致死浓度甲氧虫酰肼处理后显著降低。【结论】 二化螟对甲氧虫酰肼具有较高的抗性风险。对甲氧虫酰肼产生抗性的田间二化螟种群与其他双酰肼类杀虫剂之间存在交互抗性。亚致死剂量甲氧虫酰肼处理二化螟具有显著的适合度代价。

关键词: 二化螟, 甲氧虫酰肼, 抗性风险评估, 交互抗性, 适合度代价

LIU Yan, HE Linfeng, WANG Shuchao, YANG Fengxia, GAO Congfen, WU Shunfan. Resistance Risk, Cross Resistance and Sublethal Effects of Methoxyfenozide on Rice Stemborers (Chilo suppressalis)[J]. Chinese Journal OF Rice Science, 2023, 37(4): 427-435.

刘艳, 何林凤, 汪书超, 杨凤霞, 高聪芬, 吴顺凡. 二化螟对甲氧虫酰肼的抗性风险、交互抗性及亚致死效应研究[J]. 中国水稻科学, 2023, 37(4): 427-435.

Figures/Tables 6

References 41

[1]	张帅, 李永平, 邵振润, 郭井泉. 水稻二化螟抗药性监测及防控对策[J]. 植物保护, 2011, 37(2): 141-144.
	Zhang S, Li Y P, Shao Z R, Guo J Q. Monitoring and management of insecticide resistance of Chilo suppressalis in China[J]. Plant Protection, 2011, 37(2): 141-144. (in Chinese with English abstract)
[2]	李大喜. 水稻二化螟综合防治技术[J]. 现代农业科技, 2018(6): 110+115.
	Li D X. Integrated control technology of rice borer Chilo supressalis[J]. Modern Agricultural Science and Technology, 2018(6): 110+115. (in Chinese with English abstract)
[3]	冯建设. 水稻二化螟发生规律及防治对策[J]. 福建农业科技, 2012(Z1): 83-84.
	Feng J S. Occurrence regularity of Chilo Suppressalis and its controlling measure[J]. Fujian Agricultural Science and Technology, 2012(Z1): 83-84. (in Chinese with English abstract)
[4]	Li Y, Hallerman E M, Wu K, Peng Y. Insect-resistant genetically engineered crops in China: Development, application, and prospects for use[J]. Annual Review of Entomology, 2020, 65: 273-292.
[5]	韩招久, 韩召军, 陈长琨, 王荫长, 胡仕孟. 二化螟对杀虫单和甲胺磷抗性监测及田间抗性动态[J]. 植物保护学报, 2002(1): 93-94.
	Han Z J, Han Z J, Chen C K, Wang Y C, Hu S M. Monitoring of rice stem borer, Chilo suppressalis, resistance to monosultap and methamidophos, and dynamics[J]. Journal of Plant Protection, 2002(1): 93-94. (in Chinese with English abstract)
[6]	曹明章, 沈晋良, 张金振, 吕梅, 刘晓宇, 周威君. 二化螟抗药性监测和对三唑磷抗性的遗传分析[J]. 中国水稻科学, 2004(1): 75-81.
	Cao M Z, Shen J L, Zhang J Z, Lü M, Liu X Y, Zhou W J. Monitoring of insecticide resistance and inheritance analysis of triazophos resistance in the striped stem borer (Lepidoptera: Pyralidae)[J]. Chinese Journal of Rice Science, 2004(1): 75-81. (in Chinese with English abstract)
[7]	陆玉荣, 徐广和, 苏建坤, 刘琴, 吉春明, 张春梅, 刘怀阿. 扬州地区二化螟抗药性监测[J]. 安徽农业科学, 2003(1): 123-124.
	Lu Y R, Xu G H, Su J K, Liu Q, Ji C M, Zhang C M, Liu H A. Resistance monitoring of Chilo supressalis in Yangzhou area[J]. Journal of Anhui Agricultural Sciences, 2003(1): 123-124. (in Chinese with English abstract)
[8]	吕亮, 陈其志, 张舒, 杨小林, 常向前. 湖北省水稻二化螟和三化螟的抗药性监测[J]. 华中农业大学学报, 2008(2): 213-216.
	Lü L, Chen Q Z, Zhang S, Yang X L, Chang X Q. Mensuration and analysis of insecticide resistance of Chilo suppressalis Walker and Tryporyza incertulas Walker[J]. Journal of Huazhong Agricultural University, 2008(2): 213-216. (in Chinese with English abstract)
[9]	卢鹏, 李建洪, 覃春华, 张智科, 张凯雄, 彭传华, 罗汉刚. 湖北省水稻二化螟的抗药性监测[J]. 湖北农业科学, 2009, 48(9): 2160-2162.
	Lu P, Li J H, Qin C H, Zhang Z K, Zhang K X, Peng C H, Luo H G. Monitoring on resistance of rice stem borer to triazophos and fipronil in Hubei[J]. Hubei Agricultural Sciences, 2009, 48(9): 2160-2162. (in Chinese with English abstract)
[10]	Huang J M, Rao C, Wang S, He L F, Zhao S Q, Zhou L Q, Zhao Y X, Yang F X, Gao C F, Wu S F. Multiple target-site mutations occurring in lepidopterans confer resistance to diamide insecticides[J]. Insect Biochemistry and Molecular Biology, 2020, 121: 103367.
[11]	Huang J M, Sun H, He L F, Liu C, Ge WC, Ni H, Gao CF, Wu SF. Double ryanodine receptor mutations confer higher diamide resistance in rice stem borer, Chilo suppressalis[J]. Pest Management Science, 2021, 77(11): 4971-4979.
[12]	郭映花, 杨惠芳. 我国禁(限)用农药的管理与控制现状[J]. 现代预防医学, 2013, 40(12): 2198-2202.
	Guo Y H, Yang H F. The management and control status of banned (restricted) pesticides in China[J]. Modern Preventive Medicine, 2013, 40(12): 2198-2202. (in Chinese with English abstract)
[13]	郑永权, 孙海滨, 董丰收, 刘艳萍, 蒋红云, 刘新刚. 高效低风险是农药发展的必由之路[J]. 植物保护, 2012, 38(2): 1-3+11.
	Zheng Y Q, Sun H B, Dong F S, Liu Y P, Jiang H Y, Liu X G. High-efficiency and low-risk is the only way for pesticide development[J]. Plant Protection, 2012, 38(2): 1-3+11. (in Chinese with English abstract)
[14]	Moulton J K, Pepper D A, Jansson R K, Dennehy TJ. Pro-active management of Beet armyworm (Lepidoptera: Noctuidae) resistance to tebufenozide and methoxyfenozide: Baseline monitoring, risk assessment, and isolation of resistance[J]. Journal of Economic Entomology, 2002, 95(2): 414-424.
[15]	Osorio A, Martinez A M, Schneider M I, Diaz O, Corrales J L, Aviles M C, Smagghe G, Pineda S. Monitoring of Beet armyworm resistance to spinosad and methoxyfenozide in Mexico[J]. Pest Management Science, 2008, 64(10): 1001-1007.
[16]	Ahmad M, Sayyed A H, Saleem M A, Ahmad M,. Evidence for field evolved resistance to newer insecticides in Spodoptera litura (Lepidoptera: Noctuidae) from Pakistan[J]. Crop Protection, 2008, 27(10): 1367-1372.
[17]	Lu Y, Wang G, Zhong L, Zhang F, Bai Q, Zheng X, Lu Z. Resistance monitoring of Chilo suppressalis (Walker) (Lepidoptera: Crambidae) to chlorantraniliprole in eight field populations from east and central China[J]. Crop Protection, 2017, 100: 196-202.
[18]	Cao G, Han Z. Tebufenozide resistance selected in Plutella xylostella and its cross-resistance and fitness cost[J]. Pest Management Science, 2006, 62(8): 746-751.
[19]	刘娟, 董利霞, 谭晓伟, 范贤林, 芮昌辉. 棉铃虫抗甲氧虫酰肼种群对12种杀虫剂的交互抗性[J]. 植物保护, 2011, 37(3): 117-119+123.
	Liu J, Dong L X, Tan X W, Fan X L, Rui C H. Cross resistance to 12 insecticides in methoxyfenozide-resistant populations of Helicoverpa armigera[J]. Plant Protection, 2011, 37(3): 117-119+123. (in Chinese with English abstract)
[20]	Biddinger D, Hull L, Huang H, McPheron B, Loyer M. Sublethal effects of chronic exposure to tebufenozide on the development, survival, and reproduction of the tufted apple bud moth (Lepidoptera: Tortricidae)[J]. Journal of Economic Entomology, 2006, 99(3): 834-842.
[21]	Zarate N, Díaz O, Martínez A, Figueroa J I, Schneider M I, Smagghe G, Vinuela E, Budia F, Pineda S. Lethal and sublethal effects of methoxyfenozide on the development, survival and reproduction of the fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae)[J]. Neotrop Entomology, 2011, 40(1): 129-137.
[22]	Chen J, Jiang W, Hu H, Ma X, Ma Y. Joint toxicity of methoxyfenozide and lufenuron on larvae of Spodoptera exigua Hübner (Lepidoptera: Noctuidae)[J]. Journal of Asia-Pacific Entomology, 2019, 22(3): 795-801.
[23]	Seth R K, Kaur J J, Rao D K, Reynolds S E. Effects of larval exposure to sublethal concentrations of the ecdysteroid agonists RH-5849 and tebufenozide (RH-5992) on male reproductive physiology in Spodoptera litura[J]. Journal of Insect Physiology, 2004, 50(6): 505-517.
[24]	Sun X, Barrett B A. Fecundity and fertility changes in adult Codling moth (Lepidoptera: Tortricidae) exposed to surfaces treated with tebufenozide and methoxyfenozide[J]. Journal of Economic Entomology, 1999(5): 1039-1044.
[25]	Brown F, Paton D G, Catteruccia F, Ranson H, Ingham V A. A steroid hormone agonist reduces female fitness in insecticide-resistant Anopheles populations[J]. Insect Biochemistry and Molecular Biology, 2020, 121: 103372.
[26]	Desneux N, Decourtye A, Delpuech J M. The sublethal effects of pesticides on beneficial arthropods[J]. Annual Review of Entomology, 2007, 52(1): 81-106.
[27]	李波, 韩兰芝, 彭于发. 二化螟人工饲养技术[J]. 应用昆虫学报, 2015, 52(2): 498-503.
	Li B, Han L Z, Peng Y F. Development of a standardized artificial diet and rearing technique for the striped stem borer, Chilo suppressalis Walker (Lepidoptera: Crambidae)[J]. Chinese Journal of Applied Entomology, 2015, 52(2): 498-503. (in Chinese with English abstract)
[28]	尚稚珍, 王银淑, 邹永华. 二化螟饲养方法的研究[J]. 昆虫学报, 1979(2): 164-168+239.
	Shang Z Z, Wang Y S, Zou Y H. Researches on how to rear Chilo Suppressalis[J]. Acta Entomologica Sinica, 1979(2): 164-168+239. (in Chinese with English abstract)
[29]	Tabashnik B E, Mcgaughey W H. Resistance risk assessment for single and multiple Insecticides: Responses of Indianmeal moth (Lepidoptera: Pyralidae) to Bacillus thuringiensis[J]. Journal of Economic Entomology, 1994, 87(4): 834-841.
[30]	Shah R M, Shad S A, Abbas N. Methoxyfenozide resistance of the housefly, Musca domestica L. (Diptera: Muscidae): Cross-resistance patterns, stability and associated fitness costs[J]. Pest Management Science, 2017, 73(1): 254-261.
[31]	Rehan A, Freed S. Resistance selection, mechanism and stability of Spodoptera litura (Lepidoptera: Noctuidae) to methoxyfenozide[J]. Pesticide Biochemistry & Physiology, 2014, 110: 7-12.
[32]	赵琪, 闫乾, 郑宇, 王少丽, 张友军, 邱立红. 甜菜夜蛾对甲氧虫酰肼抗药性选育及其抗性生化机理初探[J]. 应用昆虫学报, 2012, 49(6): 1448-1453.
	Zhao Q, Yan Q, Zheng Y, Wang S L, Zhang Y J, Qiu L H. Selection for resistance of Spodoptera exigua to methoxyfenozide and preliminary study on the mechanisms of resistance[J]. Chinese Journal of Applied Entomology, 2012, 49(6): 1448-1453. (in Chinese with English abstract)
[33]	Keiding J. Prediction or resistance risk assessment[J]. Pesticide Resistance: Strategies and tactics for management, 1986: 279-297.
[34]	胡君. 二化螟抗药性监测及对呋喃虫酰肼的抗性风险评估[D]. 南京: 南京农业大学, 2010.
	Hu J. Monitoring of insecticide resistance and resistance risk assessment for js118in the rice stem borer, Chilo Suppressalis[D]. Nanjing: Nanjing Agricultural University, 2010. (in Chinese with English abstract)
[35]	方勇. 甜菜夜蛾对甲氧虫酰肼抗药性风险评估[D]. 南宁: 广西大学, 2011.
	Fang Y. Resistance risk assessment of methoxyfenozide in Exigua Hubner[D]. Nanning: Guangxi University, 2011. (in Chinese with English abstract)
[36]	刘娟, 芮昌辉, 范贤林, 董利霞. 棉铃虫对甲氧虫酰肼的抗性遗传力[J]. 植物保护学报, 2009, 36(4): 349-353.
	Liu J, Rui C H, Fan X L, Dong L X. Realized heritability of resistance to methoxyfenozide in Helicoverpa armigera(Hübner)[J]. Journal of Plant Protection, 2009, 36(4): 349-353. (in Chinese with English abstract)
[37]	王建军, 田大军, 庄静. 斜纹夜蛾对甲氧虫酰肼的抗性选育及抗性风险评估[J]. 江苏农业学报, 2009, 25(1): 79-83.
	Wang J J, Tian D J, Zhuang J. Selection and risk assessment of Spodoptera litura(Fabricius)resistance to methoxyfenozide[J]. Jiangsu Journal of Agricultural Sciences, 2009, 25(1): 79-83. (in Chinese with English abstract)
[38]	贾变桃, 沈晋良, 刘叙杆. 甜菜夜蛾对虫酰肼的抗性选育、风险评估及交互抗性[J]. 昆虫学报, 2007(11): 1116-1121.
	Jia B T, Shen J L, Liu X G. Selection risk assessment and cross-resistance of resistance to tebufenozide in the beet armyworm Spodoptera exigua (Hübner)(Lepidoptera: Noctuidae)[J]. Acta Entomologica Sinica, 2007(11): 1116-1121. (in Chinese with English abstract)
[39]	殷茜, 钱路, 曹广春, 韩召军. 小菜蛾阿维菌素和虫酰肼抗性品系对几种新型药剂的交互抗性研究[J]. 南京农业大学学报, 2010, 33(5): 60-64.
	Yin Q, Qian L, Cao G C, Han Z J. Cross-resistance to several new pesticedes exhibited by abamectin-and tebufenozide-resistant Plutella xylostella[J]. Journal of Nanjing Agricultural University, 2010, 33(5): 60-64. (in Chinese with English abstract)
[40]	Adel M M, Sehnal F. Azadirachtin potentiates the action of ecdysteroid agonist RH-2485 in Spodoptera littoralis[J]. Journal of Insect Physiology, 2000, 46(3): 267-274.
[41]	Enriquez, C L R, Pineda F J I, Schneider M I, Martinez A M. Toxicity and sublethal effects of methoxyfenozide on Spodoptera exigua (Lepidoptera: Noctuidae)[J]. Journal of Economic Entomology, 2010, 103(3): 662-667.

种群 Population	生测方法 Bioassay methods	龄期 Instar	斜率±标准误 Slope ± SE	卡方值(自由度) χ²(df)	致死中浓度(95%置信限) LC₅₀(95%FL)/(mg·L⁻¹)
WH-S	稻苗浸渍法	1龄1st larval instar^a	1.718±0.219	1.212(4)	5.175(3.892−6.804)
	Seedling dipping method	2龄2nd larval instar^b	2.285±0.305	6.091(3)	9.903(4.470−18.392)
	人工饲料混药法 Artificial diet incorporation method	1龄1st larval instar^a	3.255±0.476	2.600(3)	0.213(0.171−0.257)
	人工饲料混药法 Artificial diet incorporation method	2龄2nd larval instar^b	2.686±0.335	2.697(3)	0.880(0.711−1.073)

种群 Population	生测方法 Bioassay methods	龄期 Instar	斜率±标准误 Slope ± SE	卡方值(自由度) χ²(df)	致死中浓度(95%置信限) LC₅₀(95%FL)/(mg·L⁻¹)
WH-S	稻苗浸渍法	1龄1st larval instar^a	1.718±0.219	1.212(4)	5.175(3.892−6.804)
	Seedling dipping method	2龄2nd larval instar^b	2.285±0.305	6.091(3)	9.903(4.470−18.392)
	人工饲料混药法 Artificial diet incorporation method	1龄1st larval instar^a	3.255±0.476	2.600(3)	0.213(0.171−0.257)
	人工饲料混药法 Artificial diet incorporation method	2龄2nd larval instar^b	2.686±0.335	2.697(3)	0.880(0.711−1.073)

筛选世代Generation	筛选浓度 Selection concentration/(mg·L⁻¹)	处理虫数 Number	平均存活率 Survival rate/%	斜率±标准误 Slope±SE	卡方值(自由度) χ² (df)	致死中浓度(95%置信限) LC₅₀(95%FL)/(mg·L⁻¹)	RR
M₀	0.3	10 000	60	2.511±0.327	1.082(3)	0.424(0.336−0.517)	1.0
M₁	0.3	4 000	70	2.934±0.377	2.320(3)	0.761(0.636−0.929)	1.8
M₂	0.3	5 000	83	2.942±0.407	2.417(4)	0.470(0.369−0.584)	1.0
M₃	0.4	6 000	68	1.989±0.231	7.507(4)	0.596(0.332−0.924)	1.4
M₄	0.2	650	95	1.994±0.279	0.536(3)	1.598(1.258−2.163)	3.8
M₅	0.3	4 000	73	2.723±0.288	1.212(4)	1.393(1.162−1.674)	3.3
M₆	0.8	14 000	73	2.464±0.299	5.829(3)	0.711(0.417−1.182)	1.7
M₇	1.6	14 000	52	2.608±0.361	1.936(4)	1.510(1.170−1.876)	3.6
M₈	0.4	500	60	−	−	−	−
M₉	0.8	3 000	87	2.141±0.242	5.932(4)	1.428(0.935−2.067)	3.7
M₁₀	0.8	5 000	88	2.673±0.326	3.647(4)	2.253(1.793−2.770)	5.3

筛选世代Generation	筛选浓度 Selection concentration/(mg·L⁻¹)	处理虫数 Number	平均存活率 Survival rate/%	斜率±标准误 Slope±SE	卡方值(自由度) χ² (df)	致死中浓度(95%置信限) LC₅₀(95%FL)/(mg·L⁻¹)	RR
M₀	0.3	10 000	60	2.511±0.327	1.082(3)	0.424(0.336−0.517)	1.0
M₁	0.3	4 000	70	2.934±0.377	2.320(3)	0.761(0.636−0.929)	1.8
M₂	0.3	5 000	83	2.942±0.407	2.417(4)	0.470(0.369−0.584)	1.0
M₃	0.4	6 000	68	1.989±0.231	7.507(4)	0.596(0.332−0.924)	1.4
M₄	0.2	650	95	1.994±0.279	0.536(3)	1.598(1.258−2.163)	3.8
M₅	0.3	4 000	73	2.723±0.288	1.212(4)	1.393(1.162−1.674)	3.3
M₆	0.8	14 000	73	2.464±0.299	5.829(3)	0.711(0.417−1.182)	1.7
M₇	1.6	14 000	52	2.608±0.361	1.936(4)	1.510(1.170−1.876)	3.6
M₈	0.4	500	60	−	−	−	−
M₉	0.8	3 000	87	2.141±0.242	5.932(4)	1.428(0.935−2.067)	3.7
M₁₀	0.8	5 000	88	2.673±0.326	3.647(4)	2.253(1.793−2.770)	5.3

筛选代数 Selected generation	每代平均反应 Estimate of mean response per generation				每代平均选择差异 Estimate of mean selected differential per generation					现实遗传力h²
筛选代数 Selected generation	始LC₅₀对数值 Logarithm of initial LC₅₀	终LC₅₀对数值 Logarithm of final LC₅₀	选择反应 R		平均存活率 P	选择强度 i	平均斜率 Mean slope	表型标准差 σ_p	选择差异 S
10(M₁~M₁₀)	−0.373	0.353	0.073		73.55	0.442	2.451	0.408	0.180	0.402