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

  • Jin-Cui Chen
  • Ya-Jun Gong
  • Pan Shi
  • Ze-Hua Wang
  • Li-Jun Cao
  • Peng Wang
  • Shu-Jun WeiEmail author
Article
  • 6 Downloads

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.

Keywords

Tetranychus urticae Field population Cross-resistance Bioassay 

Notes

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).

References

  1. Abraham CM, Braman SK, Oetting RD, Hinkle NC (2013) Pesticide compatibility with natural enemies for pest management in greenhouse gerbera daisies. J Econ Entomol 106:1590–1601CrossRefGoogle Scholar
  2. 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 69:75–80CrossRefGoogle Scholar
  3. Brandenburg R, Kennedy G (1982) Intercrop relationships and spider mite dispersal in a corn/peanut agro-ecosystem. Entomol Exp Appl 32:269–276CrossRefGoogle Scholar
  4. 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 66:509–528CrossRefGoogle Scholar
  5. 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:gmr16029599Google Scholar
  6. 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 21:49–53Google Scholar
  7. 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 100:541–549CrossRefGoogle Scholar
  8. 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 62:325–335CrossRefGoogle Scholar
  9. Gerson U, Weintraub PG (2012) Mites (Acari) as a factor in greenhouse management. Annu Rev Entomol 57:229–247CrossRefGoogle Scholar
  10. 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 68:55–70CrossRefGoogle Scholar
  11. 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 52:225–227Google Scholar
  12. 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 47:2990–2997Google Scholar
  13. 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 69:311–321CrossRefGoogle Scholar
  14. 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 106:80–85CrossRefGoogle Scholar
  15. 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 42:305–311CrossRefGoogle Scholar
  16. 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 59:328–336Google Scholar
  17. 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 67:1424–1433CrossRefGoogle Scholar
  18. 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 70:365–368CrossRefGoogle Scholar
  19. 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 7:103–112Google Scholar
  20. 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 72:103–112CrossRefGoogle Scholar
  21. 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:e0139934CrossRefGoogle Scholar
  22. Li B, Yu HB, Luo YM, Wu HF (2016) The synthesis and acaricidal activity of SYP-9625. Mod Agrochem 15:15–17Google Scholar
  23. Liu N, Yue X (2000) Insecticide resistance and cross-resistance in the house fly (Diptera: Muscidae). J Econ Entomol 93:1269–1275CrossRefGoogle Scholar
  24. 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 56:113–122CrossRefGoogle Scholar
  25. Nakahira K (2011) Strategy for discovery of a novel miticide Cyenopyrafen which is one of electron transport chain inhibitors. J Pest Sci 36:511–515CrossRefGoogle Scholar
  26. 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 50:231–241CrossRefGoogle Scholar
  27. 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 Google Scholar
  28. 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 12:98CrossRefGoogle Scholar
  29. 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 5:17090CrossRefGoogle Scholar
  30. 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 65:91–99CrossRefGoogle Scholar
  31. 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 42:10–20CrossRefGoogle Scholar
  32. Sparks TC, Dripps JE, Watson GB, Paroonagian D (2012) Resistance and cross-resistance to the spinosyns—a review and analysis. Pestic Biochem Phys 102:1–10CrossRefGoogle Scholar
  33. Sugimoto N, Osakabe M (2014) Cross-resistance between cyenopyrafen and pyridaben in the twospotted spider mite Tetranychus urticae (Acari: Tetranychidae). Pest Manag Sci 70:1090–1096CrossRefGoogle Scholar
  34. 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 58:101–110CrossRefGoogle Scholar
  35. 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 109:1758–1765CrossRefGoogle Scholar
  36. Tang Q, Feng M (2002) DPS data processing system for practical statistics. Science Press, BeijingGoogle Scholar
  37. Ubara M, Osakabe M (2015) Suspension of egg gatching caused by high humidity and submergence in spider mites. Environ Entomol 44:1210–1219CrossRefGoogle Scholar
  38. 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 95:1267–1274CrossRefGoogle Scholar
  39. Van Leeuwen T, Dermauw W (2016) The molecular evolution of xenobiotic metabolism and resistance in chelicerate mites. Annu Rev Entomol 61:475–498CrossRefGoogle Scholar
  40. 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 61:499–507CrossRefGoogle Scholar
  41. 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 36:869–877CrossRefGoogle Scholar
  42. 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 105:5980–5985CrossRefGoogle Scholar
  43. 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 40:563–572CrossRefGoogle Scholar
  44. 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 20:135–140CrossRefGoogle Scholar
  45. 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 121:12–21CrossRefGoogle Scholar
  46. 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 65:404–412CrossRefGoogle Scholar
  47. Vassiliou VA, Kitsis P (2013) Acaricide resistance in Tetranychus urticae (Acari: Tetranychidae) populations from Cyprus. J Econ Entomol 106:1848–1854CrossRefGoogle Scholar
  48. Wei T, Simko V (2017) Package “corrplot”: visualization of a correlation matrix (version 0.84). https://github.com/taiyun/corrplot

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Institute of Plant and Environmental ProtectionBeijing Academy of Agriculture and Forestry SciencesBeijingChina
  2. 2.Dow AgroSciences (China) Co., Ltd.ShanghaiChina

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