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Field-evolved resistance and cross-resistance of the two-spotted spider mite, Tetranychus urticae, to bifenazate, cyenopyrafen and SYP-9625

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Abstract

The acaricide bifenazate acts as complex III inhibitor whereas cyenopyrafen and SYP-9625 act as complex II inhibitors. All these acaricides are commonly used to control two-spotted spider mite (TSSM), Tetranychus urticae Koch. We examined field-evolved and laboratory-selected resistance of TSSM to these three acaricides and determined cross-resistance among them. Six field populations of TSSM showed low levels of resistance to bifenazate with resistance ratios ranging from 2.20 to 10.65 compared to a susceptible strain. SYP-9625, structurally similar to cyenopyrafen, showed slightly higher activity to TSSMs but significant cross-resistance in both field populations and a laboratory-selected strain by SYP-9625. However, low levels of resistance to these two chemicals were found in field populations even when used for short time periods. Cross-resistance was not found between bifenazate and Complex II inhibitors, cyenopyrafen and SYP-9625, in both field populations and the laboratory-selected strain. Field-evolved resistance of TSSM to the tested acaricides is still low and should be delayed by the implementation of resistance management practices. Cross-resistance between cyenopyrafen and SYP-9625 is obvious, so they should not be used together in resistance management strategies based on mode of action rotation.

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References

  • Abraham CM, Braman SK, Oetting RD, Hinkle NC (2013) Pesticide compatibility with natural enemies for pest management in greenhouse gerbera daisies. J Econ Entomol 106:1590–1601

    Article  CAS  PubMed  Google Scholar 

  • Bernardi D, Botton M, da Cunha US, Bernardi O, Malausa T, Garcia MS, Nava DE (2013) Effects of azadirachtin on Tetranychus urticae (Acari: Tetranychidae) and its compatibility with predatory mites (Acari: Phytoseiidae) on strawberry. Pest Manag Sci 69:75–80

    Article  CAS  PubMed  Google Scholar 

  • Brandenburg R, Kennedy G (1982) Intercrop relationships and spider mite dispersal in a corn/peanut agro-ecosystem. Entomol Exp Appl 32:269–276

    Article  Google Scholar 

  • Castilho RC, Duarte VS, de Moraes GJ, Westrum K, Trandem N, Rocha LC, Delalibera I Jr, Klingen I (2015) Two-spotted spider mite and its natural enemies on strawberry grown as protected and unprotected crops in Norway and Brazil. Exp Appl Acarol 66:509–528

    Article  PubMed  Google Scholar 

  • Costa AF, Teodoro PE, Bhering LL, Fornazier MJ, Andrade JS, Martins DS, Zanuncio Junior JS (2017) Selection of strawberry cultivars with tolerance to Tetranychus urticae (Acari: Tetranychidae) and high yield under different managements. Genet Mol Res 16:gmr16029599

    Google Scholar 

  • Dittrich V, Cranham J, Jepson L, Helle W (1980) Revised method for spider mites and their eggs (eg Tetranychus spp. and Panonychus ulmi Koch), FAO method no. 10a. FAO Plant Prod Prot Pap 21:49–53

    Google Scholar 

  • Fernandez Ferrari MC, Schausberger P (2013) From repulsion to attraction: species- and spatial context-dependent threat sensitive response of the spider mite Tetranychus urticae to predatory mite cues. Die Naturwissenschaften 100:541–549

    Article  CAS  PubMed  Google Scholar 

  • Ferrero M, Tixier MS, Kreiter S (2014) Different feeding behaviours in a single predatory mite species. 2. Responses of two populations of Phytoseiulus longipes (Acari: Phytoseiidae) to various prey species, prey stages and plant substrates. Exp Appl Acarol 62:325–335

    Article  CAS  PubMed  Google Scholar 

  • Gerson U, Weintraub PG (2012) Mites (Acari) as a factor in greenhouse management. Annu Rev Entomol 57:229–247

    Article  CAS  PubMed  Google Scholar 

  • Gigon V, Camps C, Le Corff J (2016) Biological control of Tetranychus urticae by Phytoseiulus macropilis and Macrolophus pygmaeus in tomato greenhouses. Exp Appl Acarol 68:55–70

    Article  PubMed  Google Scholar 

  • Gong Y, Shi B, Wang Z, Kang Z, Jin G, Cui W, Wei S (2013) Toxicity and field control efficacy of the new acaricide bifenazate to the two-spotted mite Tetranychus urticae Koch. Agrochemicals 52:225–227

    CAS  Google Scholar 

  • Gong Y, Wang Z, Shi B, Cui W, Jin G, Sun Y, Wei S (2014) Sensitivity of different field populations of Tetranychus urticae Koch (Acari: Tetranychidae) to theacaricides in Beijing area. Sci Agric Sin 47:2990–2997

    CAS  Google Scholar 

  • Hata FT, Ventura MU, Carvalho MG, Miguel AL, Souza MS, Paula MT, Zawadneak MA (2016) Intercropping garlic plants reduces Tetranychus urticae in strawberry crop. Exp Appl Acarol 69:311–321

    Article  PubMed  Google Scholar 

  • Howell AD, Daugovish O (2013) Biological control of Eotetranychus lewisi and Tetranychus urticae (Acari: Tetranychidae) on strawberry by four phytoseiids (Acari: Phytoseiidae). J Econ Entomol 106:80–85

    Article  PubMed  Google Scholar 

  • Ilias A, Roditakis E, Grispou M, Nauen R, Vontas J, Tsagkarakou A (2012) Efficacy of ketoenols on insecticide resistant field populations of two-spotted spider mite Tetranychus urticae and sweet potato whitefly Bemisia tabaci from Greece. Crop Prot 42:305–311

    Article  CAS  Google Scholar 

  • Jin GH, Gong YJ, Qian ZW, Zhu L, Wang ZH, Chen JC, Wei SJ (2016) Selectivity and fitness of the two-spotted spider mite, Tetranychus urticae (Acarina: Tetranychidae) to different varieties of eggplant. Acta Entomol Sin 59:328–336

    Google Scholar 

  • Khajehali J, Van Nieuwenhuyse P, Demaeght P, Tirry L, Van Leeuwen T (2011) Acaricide resistance and resistance mechanisms in Tetranychus urticae populations from rose greenhouses in the Netherlands. Pest Manag Sci 67:1424–1433

    Article  CAS  PubMed  Google Scholar 

  • Khalighi M, Tirry L, Van Leeuwen T (2014) Cross-resistance risk of the novel complex II inhibitors cyenopyrafen and cyflumetofen in resistant strains of the two-spotted spider mite Tetranychus urticae. Pest Manag Sci 70:365–368

    Article  CAS  PubMed  Google Scholar 

  • Khalighi M, Dermauw W, Wybouw N, Bajda S, Osakabe M, Tirry L, Van Leeuwen T (2015) Molecular analysis of cyenopyrafen resistance in the two-spotted spider mite Tetranychus urticae. Pest Manag Sci 7:103–112

    Google Scholar 

  • Khalighi M, Dermauw W, Wybouw N, Bajda S, Osakabe M, Tirry L, Van Leeuwen T (2016) Molecular analysis of cyenopyrafen resistance in the two-spotted spider mite Tetranychus urticae. Pest Manag Sci 72:103–112

    Article  CAS  PubMed  Google Scholar 

  • Kwon DH, Kang TJ, Kim YH, Lee SH (2015) Phenotypic- and genotypic-resistance detection for adaptive resistance management in Tetranychus urticae Koch. PLoS ONE 10:e0139934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li B, Yu HB, Luo YM, Wu HF (2016) The synthesis and acaricidal activity of SYP-9625. Mod Agrochem 15:15–17

    Google Scholar 

  • Liu N, Yue X (2000) Insecticide resistance and cross-resistance in the house fly (Diptera: Muscidae). J Econ Entomol 93:1269–1275

    Article  CAS  Google Scholar 

  • Marcic D, Petronijevic S, Drobnjakovic T, Prijovic M, Peric P, Milenkovic S (2012) The effects of spirotetramat on life history traits and population growth of Tetranychus urticae (Acari: Tetranychidae). Exp Appl Acarol 56:113–122

    Article  PubMed  Google Scholar 

  • Nakahira K (2011) Strategy for discovery of a novel miticide Cyenopyrafen which is one of electron transport chain inhibitors. J Pest Sci 36:511–515

    Article  CAS  Google Scholar 

  • Nicastro RL, Sato ME, Da Silva MZ (2010) Milbemectin resistance in Tetranychus urticae (Acari: Tetranychidae): selection, stability and cross-resistance to abamectin. Exp Appl Acarol 50:231–241

    Article  CAS  PubMed  Google Scholar 

  • Osakabe M, Uesugi R, Goka K (2009) Evolutionary aspects of acaricide-resistance development in spider mites. Psyche J Entomol. https://doi.org/10.1155/2009/947439

    Article  Google Scholar 

  • Pakyari H, Enkegaard A (2012) Effect of different temperatures on consumption of two spotted mite, Tetranychus urticae, eggs by the predatory thrips, Scolothrips longicornis. J Insect Sci 12:98

    Article  PubMed  PubMed Central  Google Scholar 

  • Piraneo TG, Bull J, Morales MA, Lavine LC, Walsh DB, Zhu F (2015) Molecular mechanisms of Tetranychus urticae chemical adaptation in hop fields. Sci Rep 5:17090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riga M, Myridakis A, Tsakireli D, Morou E, Stephanou EG, Nauen R, Van Leeuwen T, Douris V, Vontas J (2015) Functional characterization of the Tetranychus urticae CYP392A11, a cytochrome P450 that hydroxylates the METI acaricides cyenopyrafen and fenpyroximate. Insect Biochem Mol 65:91–99

    Article  CAS  Google Scholar 

  • Sarwar M (2014) Influence of host plant species on the development, fecundity and population density of pest Tetranychus urticae Koch (Acari: Tetranychidae) and predator Neoseiulus pseudolongispinosus (Xin, Liang and Ke) (Acari: Phytoseiidae). N Z J Crop Horticult 42:10–20

    Article  Google Scholar 

  • Sparks TC, Dripps JE, Watson GB, Paroonagian D (2012) Resistance and cross-resistance to the spinosyns—a review and analysis. Pestic Biochem Phys 102:1–10

    Article  CAS  Google Scholar 

  • Sugimoto N, Osakabe M (2014) Cross-resistance between cyenopyrafen and pyridaben in the twospotted spider mite Tetranychus urticae (Acari: Tetranychidae). Pest Manag Sci 70:1090–1096

    Article  CAS  PubMed  Google Scholar 

  • Suzuki T, Ghazy NA, Amano H, Ohyama K (2012) A high-performance humidity control system for tiny animals: demonstration of its usefulness in testing egg hatchability of the two-spotted spider mite, Tetranychus urticae. Exp Appl Acarol 58:101–110

    Article  PubMed  Google Scholar 

  • Tanaka M, Yase J, Aoki S, Sakurai T, Kanto T, Osakabe M (2016) Physical control of spider mites using ultraviolet-B with light reflection sheets in greenhouse strawberries. J Econ Entomol 109:1758–1765

    Article  PubMed  Google Scholar 

  • Tang Q, Feng M (2002) DPS data processing system for practical statistics. Science Press, Beijing

    Google Scholar 

  • Ubara M, Osakabe M (2015) Suspension of egg gatching caused by high humidity and submergence in spider mites. Environ Entomol 44:1210–1219

    Article  CAS  PubMed  Google Scholar 

  • Uesugi R, Goka K, Osakabe M (2002) Genetic basis of resistances to chlorfenapyr and etoxazole in the two-spotted spider mite (Acari: Tetranychidae). J Econ Entomol 95:1267–1274

    Article  CAS  PubMed  Google Scholar 

  • Van Leeuwen T, Dermauw W (2016) The molecular evolution of xenobiotic metabolism and resistance in chelicerate mites. Annu Rev Entomol 61:475–498

    Article  CAS  PubMed  Google Scholar 

  • Van Leeuwen T, Van Pottelberge S, Tirry L (2005) Comparative acaricide susceptibility and detoxifying enzyme activities in field-collected resistant and susceptible strains of Tetranychus urticae. Pest Manag Sci 61:499–507

    Article  CAS  PubMed  Google Scholar 

  • Van Leeuwen T, Tirry L, Nauen R (2006) Complete maternal inheritance of bifenazate resistance in Tetranychus urticae Koch (Acari: Tetranychidae) and its implications in mode of action considerations. Insect Biochem Mol 36:869–877

    Article  CAS  Google Scholar 

  • Van Leeuwen T, Vanholme B, Van Pottelberge S, Van Nieuwenhuyse P, Nauen R, Tirry L, Denholm I (2008) Mitochondrial heteroplasmy and the evolution of insecticide resistance: non-Mendelian inheritance in action. Proc Natl Acad Sci USA 105:5980–5985

    Article  CAS  PubMed  Google Scholar 

  • Van Leeuwen T, Vontas J, Tsagkarakou A, Dermauw W, Tirry L (2010) Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: a review. Insect Biochem Mol 40:563–572

    Article  CAS  Google Scholar 

  • Van Leeuwen T, Van Nieuwenhuyse P, Vanholme B, Dermauw W, Nauen R, Tirry L (2011) Parallel evolution of cytochrome b mediated bifenazate resistance in the citrus red mite Panonychus citri. Insect Mol Biol 20:135–140

    Article  CAS  PubMed  Google Scholar 

  • Van Leeuwen T, Tirry L, Yamamoto A, Nauen R, Dermauw W (2015) The economic importance of acaricides in the control of phytophagous mites and an update on recent acaricide mode of action research. Pestic Biochem Phys 121:12–21

    Article  CAS  Google Scholar 

  • Van Nieuwenhuyse P, Van Leeuwen T, Khajehali J, Vanholme B, Tirry L (2009) Mutations in the mitochondrial cytochrome b of Tetranychus urticae Koch (Acari: Tetranychidae) confer cross-resistance between bifenazate and acequinocyl. Pest Manag Sci 65:404–412

    Article  CAS  PubMed  Google Scholar 

  • Vassiliou VA, Kitsis P (2013) Acaricide resistance in Tetranychus urticae (Acari: Tetranychidae) populations from Cyprus. J Econ Entomol 106:1848–1854

    Article  CAS  PubMed  Google Scholar 

  • Wei T, Simko V (2017) Package “corrplot”: visualization of a correlation matrix (version 0.84). https://github.com/taiyun/corrplot

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Acknowledgements

We thank Prof. Shao-Li Wang for providing the susceptible strain of the TSSM, Ting-Ting Cao, Ming-Liang Li for assistance of field collection. Funding for this study was provided jointly by the Promotion and Innovation of Beijing Academy of Agriculture and Forestry Sciences (KJCX20180113), the Innovative Team of Beijing Academy of Agriculture and Forestry Sciences (JNKYT201605), Beijing Municipal Science and Technology Project (D16110500550000) and Beijing Key Laboratory of Environmentally Friendly Pest Management on Northern Fruits (BZ0432).

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  1. Jin-Cui Chen and Ya-Jun Gong contributed equally to this study.

Authors and Affiliations

  1. Institute of Plant and Environmental Protection, Beijing Academy of Agriculture and Forestry Sciences, 9 Shuguanghuayuan Middle Road, Haidian District, Beijing, 100097, China

    Jin-Cui Chen, Ya-Jun Gong, Pan Shi, Ze-Hua Wang, Li-Jun Cao & Shu-Jun Wei

  2. Dow AgroSciences (China) Co., Ltd., Shanghai Branch, Shanghai, 201203, China

    Peng Wang

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  1. Jin-Cui Chen
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Chen, JC., Gong, YJ., Shi, P. et al. Field-evolved resistance and cross-resistance of the two-spotted spider mite, Tetranychus urticae, to bifenazate, cyenopyrafen and SYP-9625. Exp Appl Acarol 77, 545–554 (2019). https://doi.org/10.1007/s10493-019-00359-3

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