Skip to main content
SpringerLink
Log in

Mechanisms and management of acaricide resistance for Tetranychus urticae in agroecosystems

  • Review
  • Published:
Journal of Pest Science Aims and scope Submit manuscript

Abstract

The two-spotted spider mite, Tetranychus urticae Koch, is a constant threat to sustainable production of numerous economically important crops globally. Management of T. urticae is heavily reliant on the application of synthetic acaricides. However, T. urticae has rapidly developed resistance to most of the acaricides available for its control due to its very broad host plant range, extremely short lifecycle, high fecundity, arrhenotokous parthenogenesis, and overwintering strategy. Despite the recent progress in identifying genetic changes/markers associated with resistance toward some commonly used acaricides for T. urticae, there is still limited studies that select and apply these markers in field populations to guide sustainable pest management strategy design. Temporal and spatial characterization of acaricide-resistant phenotypes and their underlying mechanisms are crucial for the design and implementation of successful and sustainable integrated mite management programs. This review highlights the current acaricide resistance status of field-collected T. urticae populations and the underlying molecular mechanisms of resistance. Our review found that some genetic mutations in target sites and/or overexpression of metabolic genes confer resistance in geographically exclusive populations, while some resistance markers appear to be specific to populations at biogeographical areas. Thus, there is a need for locally based coordinated efforts to understand the mechanisms of resistance present in endemic T. urticae populations. Moreover, we discuss a prospective template for designing an effective acaricide resistance management program within various agroecosystems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

adopted from Piraneo et al. (2015). b Timeline of published studies on field-evolved resistance of T. urticae to MET complex III inhibitors

Fig. 12
Fig. 13

adopted from our previous studies Piraneo et al. 2015 (a) and Wu et al. 2019 (b)

Fig. 14

Similar content being viewed by others

References

  • Adesanya A, Morales M, Walsh D, Lavine L, Lavine M, Zhu F (2018a) Mechanisms of resistance to three mite growth inhibitors of Tetranychus urticae in hops. Bull Entomol Res 108:23–34

    Article  CAS  PubMed  Google Scholar 

  • Adesanya AW, Franco E, Walsh DB, Lavine M, Lavine L, Zhu F (2018b) Phenotypic and genotypic plasticity of acaricide resistance in populations of Tetranychus urticae (Acari: Tetranychidae) on peppermint and silage corn in the Pacific Northwest. J Econ Entomol 111:2831–2843

    CAS  PubMed  Google Scholar 

  • Adesanya AW, Beauchamp MJ, Lavine MD, Lavine LC, Zhu F, Walsh DB (2019) Physiological resistance alters behavioral response of Tetranychus urticae to acaricides. Sci Rep 9:1–12

    Article  Google Scholar 

  • Adesanya AW, Cardenas A, Lavine MD, Walsh DB, Lavine LC, Zhu F (2020) RNA interference of NADPH-Cytochrome P450 reductase increases susceptibilities to multiple acaricides in Tetranychus urticae. Pest Biochem Physiol 165:104550

    Article  CAS  Google Scholar 

  • Aguilar-Fenollosa E, Ibáñez-Gual MV, Pascual-Ruiz S, Hurtado M, Jacas J (2011) Effect of ground-cover management on spider mites and their phytoseiid natural enemies in clementine mandarin orchards: bottom-up regulation mechanisms. Biol Conserv 59:158–170

    Google Scholar 

  • Aiki Y, Kozaki T, Mizuno H, Kono Y (2005) Amino acid substitution in Ace paralogous acetylcholinesterase accompanied by organophosphate resistance in the spider mite Tetranychus kanzawai. Pest Biochem Physiol 82:154–161

    Article  CAS  Google Scholar 

  • Anazawa Y, Tomita T, Aiki Y, Kozaki T, Kono Y (2003) Sequence of a cDNA encoding acetylcholinesterase from susceptible and resistant two-spotted spider mite, Tetranychus urticae. Insect Biochem Mol Biol 33:509–514

    Article  CAS  PubMed  Google Scholar 

  • Ay R, Gürkan MO (2005) Resistance to bifenthrin and resistance mechanisms of different strains of the two-spotted spider mite (Tetranychus urticae) from Turkey. Phytoparasitica 33:237–244

    Article  CAS  Google Scholar 

  • Ay R, Kara FE (2011) Toxicity, inheritance of fenpyroximate resistance, and detoxiication-enzyme levels in a laboratory-selected fenpyroximate-resistant strain of Tetranychus urticae Koch (Acari: Tetranychidae). Crop Prot 30:605–610

  • Azadi Dana E, Sadeghi A, Güncan A, Khanjani M, Babolhavaeji H, Maroufpoor M (2018) Demographic comparison of the Tetranychus urticae Koch (Acari: Tetranychidae) reared on different cultivars of strawberry. J Econ Entomol 6:2927–2935

    Google Scholar 

  • Bajda S et al (2017) A mutation in the PSST homologue of complex I (NADH: ubiquinone oxidoreductase) from Tetranychus urticae is associated with resistance to METI acaricides. Insect Biochem Mol Biol 80:79–90

    Article  PubMed  Google Scholar 

  • Balabanidou V, Grigoraki L, Vontas J (2018) Insect cuticle: a critical determinant of insecticide resistance. Curr Opin Insect Sci 27:68–74

    Article  PubMed  Google Scholar 

  • Beers E, Riedl H, Dunley J (1998) Resistance to abamectin and reversion to susceptibility to fenbutatin oxide in spider mite (Acari: Tetranychidae) populations in the Pacific Northwest. J Econ Entomol 91:352–360

    Article  Google Scholar 

  • Bi JL, Niu ZM, Yu L, Toscano NC (2016) Resistance status of the carmine spider mite, Tetranychus cinnabarinus and the twospotted spider mite, Tetranychus urticae to selected acaricides on strawberries. Insect Sci 23:88–93

    Article  CAS  PubMed  Google Scholar 

  • Campos F, Dybas RA, Krupa DA (1995) Susceptibility of Twospotted spider site (Acari: Tetranychidae) populations in California to abamectin. J Econ Entomol 88:225–231

    Article  CAS  Google Scholar 

  • Carrière Y et al (2012) Large-scale, spatially-explicit test of the refuge strategy for delaying insecticide resistance. Proc Natl Acad Sci 109:775–780

    Article  PubMed  Google Scholar 

  • Carvalho R, Yang Y, Field LM, Gorman K, Moores G, Williamson MS, Bass C (2012) Chlorpyrifos resistance is associated with mutation and amplification of the acetylcholinesterase-1 gene in the tomato red spider mite, Tetranychus evansi. Pest Biochem Physiol 104:143–149

    Article  CAS  Google Scholar 

  • Chen J-C, Gong Y-J, Shi P, Wang Z-H, Cao L-J, Wang P, Wei S-J (2019) 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

    Article  CAS  PubMed  Google Scholar 

  • Costello MJ, Daane KM (1998) Influence of ground cover on spider populations in a table grape vineyard. Ecol Entomol 23:33–40

    Article  Google Scholar 

  • Croft B, McGroarty D (1973) A model study of acaricide resistance, spider mite outbreaks, and biological control patterns in Michigan apple orchards. Environ Entomol 2:633–638

    Article  CAS  Google Scholar 

  • Demaeght P et al (2013) Molecular analysis of resistance to acaricidal spirocyclic tetronic acids in Tetranychus urticae: CYP392E10 metabolizes spirodiclofen, but not its corresponding enol. Insect Biochem Mol Biol 43:544–554

    Article  CAS  PubMed  Google Scholar 

  • Demaeght P et al (2014) High resolution genetic mapping uncovers chitin synthase-1 as the target-site of the structurally diverse mite growth inhibitors clofentezine, hexythiazox and etoxazole in Tetranychus urticae. Insect Biochem Mol Biol 51:52–61

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dermauw W et al (2012) The cys-loop ligand-gated ion channel gene family of Tetranychus urticae: implications for acaricide toxicology and a novel mutation associated with abamectin resistance Insect Biochand. Mol Biol 42:455–465

    CAS  Google Scholar 

  • Devine GJ, Barber M, Denholm I (2001) Incidence and inheritance of resistance to METI-acaricides in European strains of the two-spotted spider mite (Tetranychus urticae)(Acari: Tetranychidae). Pest Manag Sci Formerly Pest Sci 57:443–448

    Article  CAS  Google Scholar 

  • Dobis EA, Reid N, Schmidt C, Goetz SJ (2019) The role of craft breweries in expanding (local) hop production. J Wine Econ 14:374–382

    Article  Google Scholar 

  • Dong K (2007) Insect sodium channels and insecticide resistance. Invertebr Neurosci 7:17

    Article  CAS  Google Scholar 

  • Duso C, Chiarini F, Conte L, Bonora V, Dalla Montà L, Otto S (2004) Fogging can control Tetranychus urticae on greenhouse cucumbers. J Pest Sci 77:105–111

    Article  Google Scholar 

  • EPA (2017) Pesticides industry sales and usage 2008–2012 market estimates. https://www.epa.gov/pesticides/pesticides-industry-sales-and-usage-2008-2012-market-estimates. Accessed 22 June 2020

  • Esteca FdCN, Rodrigues LR, de Moraes GJ, Júnior ID, Klingen I (2018) Mulching with coffee husk and pulp in strawberry affects edaphic predatory mite and spider mite densities. Entomol Exp Appl 76:161–183

    Google Scholar 

  • Farnham A, Dennehy T, Denholm I, White J (1992) The microimmersion bioassay: a novel method for measuring acaricidal activity and for characterising pesticide resistance in spider mites. In: Proceedings Brighton crop protection conference-pests and diseases, vol 1, pp 257–262. Wiley

  • Ferreira CB, Andrade FH, Rodrigues AR, Siqueira HA, Gondim MG Jr (2015) Resistance in field populations of Tetranychus urticae to acaricides and characterization of the inheritance of abamectin resistance. Crop Prot 67:77–83

    Article  CAS  Google Scholar 

  • Feyereisen R, Dermauw W, Van Leeuwen T (2015) Genotype to phenotype, the molecular and physiological dimensions of resistance in arthropods. Pest Biochem Physiol 121:61–77

    Article  CAS  Google Scholar 

  • Ffrench-Constant RH (2013) The molecular genetics of insecticide resistance. Genetics 194:807–815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fleschner CA (1952) Host-plant resistance as a factor influencing population density of citrus red mites on orchard trees. J Econ Entomol 45:687–695

    Article  CAS  Google Scholar 

  • Fonseca MM, Pallini A, Marques PH, Lima E, Janssen A (2020) Compatibility of two predator species for biological control of the two-spotted spider mite. Entomol Exp Appl 80:409–422

    Google Scholar 

  • Fotoukkiaii SM, Mermans C, Wybouw N, Van Leeuwen T (2020a) Resistance risk assessment of the novel complex II inhibitor pyflubumide in the polyphagous pest Tetranychus urticae. J Pest Sci 93:1085–1096

    Article  Google Scholar 

  • Fotoukkiaii SM, Tan Z, Xue W, Wybouw N, Van Leeuwen T (2020b) Identification and characterization of new mutations in mitochondrial cytochrome b that confer resistance to bifenazate and acequinocyl in the spider mite Tetranychus urticae. Pest Manag Sci 76:1154–1163

    Article  CAS  PubMed  Google Scholar 

  • Gent DH, Barbour JD, Dreves AJ, James DG, Parker R, Walsh DB, O’Neal S (2009) Field guide for integrated pest management in Hops Oregon State University. University of Idaho, USDA Agricultural Research Service, Washington State University, USA

  • Goddard TD, Huang CC, Meng EC, Pettersen EF, Couch GS, Morris JH, Ferrin TE (2018) UCSF ChimeraX: meeting modern challenges in visualization and analysis. Protein Sci 27:14–25

    Article  CAS  PubMed  Google Scholar 

  • Grafton-Cardwell EE, Granett J, Normington SM (1991) Influence of dispersal from almonds on the population dynamics and acaricide resistance frequencies of spider mites infesting neighboring cotton. Exp Appl Acarol 10:187–212

    Article  Google Scholar 

  • Grbić M et al (2011) The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 479:487

    Article  PubMed  PubMed Central  Google Scholar 

  • Helle W, Sabelis MW (1985) Spider mites: their biology, natural enemies and control. Elsevier, Amsterdam

    Google Scholar 

  • Herron G, Rophail J (1998) Tebufenpyrad (Pyranica®) resistance detected in two-spotted spider mite Tetranychus urticae Koch (Acari: Tetranychidae) from apples in Western Australia. Entomol Exp Appl 22:633–641

    CAS  Google Scholar 

  • Herron G, Edge V, Rophail J (1993) Clofentezine and hexythiazox resistance in Tetranychus urticae Koch in Australia. Entomol Exp Appl 17:433–440

    CAS  Google Scholar 

  • Herron GA, Langfield BJ, Tomlinson TM, Mo J (2011) Dose-response testing of Australian populations of onion thrips Thrips tabaci Lindeman (Thysanoptera: Thripidae) further refines baseline data and detects methidathion and likely imidacloprid resistance. Aust J Entomol 50:418–423

    Article  Google Scholar 

  • Herron GA, Woolley LK, Langfield KL, Chen Y (2018) First detection of etoxazole resistance in Australian two-spotted mite Tetranychus urticae Koch (Acarina: Tetranychidae) via bioassay and DNA methods. Austral Entomoly 57:365–368

    Article  Google Scholar 

  • Holtzer T, Norman J, Perring T, Berry J, Heintz J (1988) Effects of microenvironment on the dynamics of spider-mite populations. Exp Appl Acarol 4:247–264

    Article  Google Scholar 

  • Hoy MA (2012) Agricultural acarology: introduction to integrated mite management, CRC Press, Taylor & Francis Group, Boca Raton, Florida, 2011, ISBN: 978-1-4398-1751-3. J Asia Pac Entomol 15:200–200

  • Hoy MA (2016) Agricultural acarology: introduction to integrated mite management. CRC Press, Boca Raton

    Book  Google Scholar 

  • Hunkeler M, Hagmann A, Stuttfeld E, Chami M, Guri Y, Stahlberg H, Maier T (2018) Structural basis for regulation of human acetyl-CoA carboxylase. Nature 558:470–474

    Article  CAS  PubMed  Google Scholar 

  • Ilias A, Vontas J, Tsagkarakou A (2014) Global distribution and origin of target site insecticide resistance mutations in Tetranychus urticae. Insect Biochem Mol Biol 48:17–28

    Article  CAS  PubMed  Google Scholar 

  • İnak E, Alpkent YN, Çobanoğlu S, Dermauw W, Van Leeuwen T (2019) Resistance incidence and presence of resistance mutations in populations of Tetranychus urticae from vegetable crops in Turkey. Entomol Exp Appl 78:343–360

    Google Scholar 

  • Iskra A, Woods J, Gent D (2019) Stability and resiliency of biological control of the twospotted spider mite (Acari: Tetranychidae) in hop. Environ Entomol 48:894–902

    Article  CAS  PubMed  Google Scholar 

  • James DG, Price TS (2002) Fecundity in twospotted spider mite (Acari: Tetranychidae) is increased by direct and systemic exposure to imidacloprid. J Econ Entomol 95:729–732

    Article  CAS  PubMed  Google Scholar 

  • James DG, Price TS (2004) Field-testing of methyl salicylate for recruitment and retention of beneficial insects in grapes and hops. J Chem Ecol 30:1613–1628

    Article  CAS  PubMed  Google Scholar 

  • James DG, Price T, Wright LC, Coyle J, Perez J (2001) Mite abundance and phenology on commercial and escaped hops in Washington State, USA. Int J Acarol 27:151–156

    Article  Google Scholar 

  • Keena MA, Granett J (1987) Cyhexatin and propargite resistance in populations of spider mites (Acari: Tetranychidae) from California almonds. J Econ Entomol 80:560–564

    Article  CAS  Google Scholar 

  • Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJE (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845–858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khajehali J et al (2010) Acetylcholinesterase point mutations in European strains of Tetranychus urticae (Acari: Tetranychidae) resistant to organophosphates. Pest Manag Sci 66:220–228

    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 (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 

  • Kim SI, Koo H-N, Choi Y, Park B, Kim HK, Kim G-H (2019) Acequinocyl resistance associated with I256V and N321S mutations in the two-spotted spider mite (Acari: Tetranychidae). J Econ Entomol 112:835–841

    Article  CAS  PubMed  Google Scholar 

  • Kishimoto H (2002) Species composition and seasonal occurrence of spider mites (Acari: Tetranychidae) and their predators in Japanese pear orchards with different agrochemical spraying programs. Appl Entomol Zool 37:603–615

    Article  Google Scholar 

  • Krips O, Witul A, Willems P, Dicke M (1998) Intrinsic rate of population increase of the spider mite Tetranychus urticae on the ornamental crop gerbera: intraspecific variation in host plant and herbivore. Entomol Exp Appl 89:159–168

    Article  Google Scholar 

  • Kwon D, Clark J, Lee S (2010a) Extensive gene duplication of acetylcholinesterase associated with organophosphate resistance in the two-spotted spider mite. Insect Mol Biol 19:195–204

    Article  CAS  PubMed  Google Scholar 

  • Kwon DH, Im JS, Ahn JJ, Lee J-H, Clark JM, Lee SH (2010b) Acetylcholinesterase point mutations putatively associated with monocrotophos resistance in the two-spotted spider mite. Pest Biochem Physiol 96:36–42

    Article  CAS  Google Scholar 

  • Kwon DH et al (2010c) Residual contact vial bioassay for the on-site detection of acaricide resistance in the two-spotted spider mite. J Asia Pac Entomol 13:333–337

    Article  CAS  Google Scholar 

  • Kwon DH, Yoon KS, Clark JM, Lee SH (2010d) A point mutation in a glutamate-gated chloride channel confers abamectin resistance in the two-spotted spider mite, Tetranychus urticae Koch. Insect Mol Biol 19:583–591

    CAS  PubMed  Google Scholar 

  • Kwon DH, Lee SW, Ahn JJ, Lee SH (2014) Determination of acaricide resistance allele frequencies in field populations of Tetranychus urticae using quantitative sequencing. J Asia Pac Entomol 17:99–103

    Article  CAS  Google Scholar 

  • Kwon DH, Clark JM, Lee SH (2015a) Toxicodynamic mechanisms and monitoring of acaricide resistance in the two-spotted spider mite. Pest Biochem Physiol 121:97–101

    Article  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee S-Y, Kim G, Ahn K, Kim C, Shin S (2004) Inheritance and stability of etoxazole resistance in twospotted spider mite, Tetranychus urticae, and its cross resistance. Korean J Appl Entomol 43:43–48

    Google Scholar 

  • Lee K-R, Koo H-N, Yoon C-M, Kim G-H (2010) Cross resistance and point mutation of the mitochondrial cytochrome b of bifenazate resistant two-spotted spider mite, Tetranychus urticae. Korean J Pest Sci 14:247–254

    Google Scholar 

  • Lee SH, Kim YH, Kwon DH, Cha DJ, Kim JH (2015) Mutation and duplication of arthropod acetylcholinesterase: implications for pesticide resistance and tolerance. Pest Biochem Physiol 120:118–124

    Article  CAS  Google Scholar 

  • Lümmen P (2007) Mitochondrial electron transport complexes as biochemical target sites for insecticides and acaricides. In: Ishaaya I, Nauen R, Horowitz AR (eds) Insecticides design using advanced technologies. Springer, Berlin, pp 197–215

    Chapter  Google Scholar 

  • Lümmen P, Khajehali J, Luther K, Van Leeuwen T (2014) The cyclic keto-enol insecticide spirotetramat inhibits insect and spider mite acetyl-CoA carboxylases by interfering with the carboxyltransferase partial reaction. Insect Biochem Mol Biol 55:1–8

    Article  PubMed  Google Scholar 

  • Luo Y-J et al (2014) Molecular cloning and expression of glutathione S-transferases involved in propargite resistance of the carmine spider mite, Tetranychus cinnabarinus (Boisduval). Pest Biochem Physiol 114:44–51

    Article  CAS  Google Scholar 

  • Luo Y et al (2018) Cloning and different expression of ATP synthase genes between propargite resistant and susceptible strains of Tetranychus cinnabarinus (Acarina: Tetranychidae). J Asia Pac Entomol 21:402–407

    Article  Google Scholar 

  • Maeoka A et al (2020) Diagnostic prediction of acaricide resistance gene frequency using quantitative real-time PCR with resistance allele-specific primers in the two-spotted spider mite Tetranychus urticae population (Acari: Tetranychidae). Appl Entomol Zool 55:329–335

    Article  CAS  Google Scholar 

  • Marinosci C, Magalhaes S, Macke E, Navajas M, Carbonell D, Devaux C, Olivieri I (2015) Effects of host plant on life-history traits in the polyphagous spider mite Tetranychus urticae. Ecol Evol 5:3151–3158

    Article  PubMed  PubMed Central  Google Scholar 

  • Marrone PG (2014) The market and potential for biopesticides. Biopesticides: state of the art and future opportunities. ACS Publications, Washington, DC, pp 245–258

    Chapter  Google Scholar 

  • Marrone PG (2019) Pesticidal natural products—status and future potential. Pest Manag Sci 75:2325–2340

    CAS  PubMed  Google Scholar 

  • Martins J et al (2012) Analysis of six fungicides and one acaricide in still and fortified wines using solid-phase microextraction-gas chromatography/tandem mass spectrometry. Food Chem 132:630–636

    Article  CAS  PubMed  Google Scholar 

  • Meck ED, Kennedy GG, Walgenbach JF (2013) Effect of Tetranychus urticae (Acari: Tetranychidae) on yield, quality, and economics of tomato production. Crop Prot 52:84–90

    Article  Google Scholar 

  • Migeon A, Nouguier E, Dorkeld F (2010) Spider Mites Web: a comprehensive database for the Tetranychidae. Trends in acarology. Springer, Berlin, pp 557–560

    Chapter  Google Scholar 

  • Mohammadzadeh M, Bandani AR, Sabahi Q (2014) Comparison of susceptibility of two populations of Tetranychus urticae Koch to two acaricides, abamectin and propargite. Arch Phytopathol Plant Prot 47:2112–2123

  • Monteiro VB, Gondim MG Jr, Oliveira JEdM, Siqueira HA, Sousa JM (2015) Monitoring Tetranychus urticae koch (acari: tetranychidae) resistance to abamectin in vineyards in the lower middle São Francisco Valley. Crop Prot 69:90–96

    Article  CAS  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 

  • Nauen R (2005) Spirodiclofen: mode of action and resistance risk assessment in tetranychid pest mites. J Pest Sci 30:272–274

    Article  CAS  Google Scholar 

  • Nauen R, Stumpf N, Elbert A, Zebitz CPW, Kraus W (2001) Acaricide toxicity and resistance in larvae of different strains of Tetranychus urticae and Panonychus ulmi (Acari: Tetranychidae). Pest Manag Sci 57:253–261

    Article  CAS  PubMed  Google Scholar 

  • Nauen R, Wölfel K, Lueke B, Myridakis A, Tsakireli D, Roditakis E, Tsagkarakou A, Stephanou E, Vontas J (2015) Development of a lateral flow test to detect metabolic resistance in Bemisia tabaci mediated by CYP6CM1, a cytochrome P450 with broad spectrum catalytic efficiency. Pest Biochem Physiol 121:3–11

    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, Imamura T, Nakano R, Kamikawa S, Tadatsu M, Kunimoto Y, Doi M (2017) Combination of restriction endonuclease digestion with the ΔΔCt method in real-time PCR to monitor etoxazole resistance allele frequency in the two-spotted spider mite. Pest Biochem Physiol 139:1–8

    Article  CAS  Google Scholar 

  • Patil CM, Udikeri SS, Karabhantanal S (2020) Grape infesting mite Tetranychus urticae Koch. resistance to acaricides. Pak J Zool 52:1189–1192

    Article  Google Scholar 

  • Pavlidi N, Tseliou V, Riga M, Nauen R, Van Leeuwen T, Labrou NE, Vontas J (2015) Functional characterization of glutathione S-transferases associated with insecticide resistance in Tetranychus urticae. Pest Biochem Physiol 121:53–60

    Article  CAS  Google Scholar 

  • Pavlidi N et al (2017) A glutathione-S-transferase (TuGSTd05) associated with acaricide resistance in Tetranychus urticae directly metabolizes the complex II inhibitor cyflumetofen. Insect Biochem Mol Biol 80:101–115

    Article  CAS  PubMed  Google Scholar 

  • Penman D, Chapman R (1980) Woolly apple aphid outbreak following use of fenvalerate in apples in Canterbury, New Zealand. J Econ Entomol 73:49–51

    Article  CAS  Google Scholar 

  • Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF Chimera—a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612

    Article  CAS  PubMed  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 

  • Riahi E, Shishehbor P, Nemati A, Saeidi Z (2013) Temperature effects on development and life table parameters of Tetranychus urticae (Acari: Tetranychidae). J Agric Sci Technol 15:661–672

    Google Scholar 

  • Riga M et al (2014) Abamectin is metabolized by CYP392A16, a cytochrome P450 associated with high levels of acaricide resistance in Tetranychus urticae. Insect Biochem Mol Biol 46:43–53

    Article  CAS  PubMed  Google Scholar 

  • Riga M et al (2017) The relative contribution of target-site mutations in complex acaricide resistant phenotypes as assessed by marker assisted backcrossing in Tetranychus urticae. Sci Rep 7:9202

    Article  PubMed  PubMed Central  Google Scholar 

  • Roush R, Hoy MA (1978) Relative toxicity of permethrin to a predator, Metaseiulus occidentalis, and its prey, Tetranychus urticae. Environ Entomol 7:287–288

    Article  CAS  Google Scholar 

  • Roy A, Kucukural A, Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5:725–738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sabelis M, Van de Baan H (1983) Location of distant spider mite colonies by phytoseiid predators: demonstration of specific kairomones emitted by Tetranychus urticae and Panonychus ulmi. Entomol Exp Appl 33:303–314

    Article  Google Scholar 

  • Sato ME, Silva MZd, Raga A, Souza Filho MFd (2005) Abamectin resistance in Tetranychus urticae Koch (Acari: Tetranychidae): selection, cross-resistance and stability of resistance. Neotrop Entomol 34:991–998

    Article  CAS  Google Scholar 

  • Sato ME, Veronez B, Stocco RS, Queiroz MCV, Gallego R (2016) Spiromesifen resistance in Tetranychus urticae (Acari: Tetranychidae): selection, stability, and monitoring. Crop Prot 89:278–283

    Article  CAS  Google Scholar 

  • Schmidt-Jeffris RA, Beers EH (2018) Potential impacts of orchard pesticides on Tetranychus urticae: a predator–prey perspective. Crop Prot 103:56–64

    Article  CAS  Google Scholar 

  • Shi P et al (2019) Independently evolved and gene flow-accelerated pesticide resistance in two-spotted spider mites. Ecol Evol 9:2206–2219

    Article  PubMed  PubMed Central  Google Scholar 

  • Smissaert H (1964) Cholinesterase inhibition in spider mites susceptible and resistant to organophosphate. Science 143:129–131

    Article  CAS  PubMed  Google Scholar 

  • Snoeck S et al (2019) High-resolution QTL mapping in Tetranychus urticae reveals acaricide-specific responses and common target-site resistance after selection by different METI-I acaricides. Insect Biochem Mol Biol 110:19–33

    Article  CAS  PubMed  Google Scholar 

  • Song C, Kim GH, Ahn SJ, Park NJ, Cho KY (1995) Acaricide susceptibilities of field-collected populations of two-spotted spider mite, Tetranychus urticae (Acari: Tetranychidae) from apple orchards. Korean J Appl Entomol 34:328–333

  • Sparks TC et al (1989) The role of behavior in insecticide resistance. Pest Sci 26:383–399

    Article  CAS  Google Scholar 

  • Sparks TC et al (2020) Insecticides, biologics and nematicides: updates to IRAC’s mode of action classification-a tool for resistance management. Pest Biochem Physiol 167:104587

    Article  CAS  Google Scholar 

  • Strong W, Slone D, Croft B (1999) Hops as a metapopulation landscape for tetranychid-phytoseiid interactions: perspectives of intra-and interplant dispersal. Exp Appl Acarol 23:581–597

    Article  Google Scholar 

  • Stumpf N, Nauen R (2002) Biochemical markers linked to abamectin resistance in Tetranychus urticae (Acari: Tetranychidae). Pest Biochem Physiol 72:111–121

    Article  CAS  Google Scholar 

  • Sugimoto N, Takahashi A, Ihara R, Itoh Y, Jouraku A, Van Leeuwen T, Osakabe M (2020) QTL mapping using microsatellite linkage reveals target-site mutations associated with high levels of resistance against three mitochondrial complex II inhibitors in Tetranychus urticae. Insect Biochem Mol Biol 123:103410

    Article  CAS  PubMed  Google Scholar 

  • Suh E, Koh S-H, Lee J-H, Shin K-I, Cho K (2006) Evaluation of resistance pattern to fenpyroximate and pyridaben in Tetranychus urticae collected from ggreenhouses and apple orchards using lethal concentration-slope relationship. Exp Appl Acarol 38:151–165

    Article  PubMed  Google Scholar 

  • Tang X, Zhang Y, Wu Q, Xie W, Wang S (2014) Stage-specific expression of resistance to different acaricides in four field populations of Tetranychus urticae (Acari: Tetranychidae). J Econ Entomol 107:1900–1907

    Article  PubMed  Google Scholar 

  • Tong L (2005) Acetyl-coenzyme A carboxylase: crucial metabolic enzyme and attractive target for drug discovery. Cell Mol Life Sci 62:1784–1803

    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  PubMed  Google Scholar 

  • Van Leeuwen T, Tirry L (2007) Esterase-mediated bifenthrin resistance in a multiresistant strain of the two-spotted spider mite, Tetranychus urticae. Pest Manag Sci 63:150–156

    Article  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 Biol 36:869–877

    Article  PubMed  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 U S A 105:5980–5985

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Leeuwen T, Vontas J, Tsagkarakou A, Tirry L (2009) Mechanisms of acaricide resistance in the two-spotted spider mite Tetranychus urticae. Biorational control of arthropod pests. Springer, Berlin, pp 347–393

    Chapter  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 Biol 40:563–572

    Article  PubMed  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  PubMed  Google Scholar 

  • Van Leeuwen T et al (2012) Population bulk segregant mapping uncovers resistance mutations and the mode of action of a chitin synthesis inhibitor in arthropods. Proc Natl Acad Sci U S A 109:4407–4412

    Article  PubMed  PubMed Central  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. Pest Biochem Physiol 121:12–21

    Article  Google Scholar 

  • Van Leeuwen T, Dermauw W, Mavridis K, Vontas J (2020) Significance and interpretation of molecular diagnostics for insecticide resistance management of agricultural pests. Curr Opin Insect Sci 39:69–76

    Article  PubMed  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  PubMed  Google Scholar 

  • Van Pottelberge S, Van Leeuwen T, Khajehali J, Tirry L (2009a) Genetic and biochemical analysis of a laboratory-selected spirodiclofen-resistant strain of Tetranychus urticae Koch (Acari: Tetranychidae). Pest Manag Sci 65:358–366

    Article  PubMed  Google Scholar 

  • Van Pottelberge S, Van Leeuwen T, Nauen R, Tirry L (2009b) Resistance mechanisms to mitochondrial electron transport inhibitors in a field-collected strain of Tetranychus urticae Koch (Acari: Tetranychidae). Bull Entomol Res 99:23–31

    Article  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 

  • Vontas J, Mavridis K (2019) Vector population monitoring tools for insecticide resistance management: myth or fact? Pest Biochem Physiol 161:54–60

    Article  CAS  Google Scholar 

  • Voss G, Matsumura F (1964) Resistance to organophosphorus compounds in the two-spotted spider mite: two different mechanisms of resistance. Nature 202:319–320

    Article  CAS  PubMed  Google Scholar 

  • Walsh DB, Grove GG (2005) Repellency and repulsiveness of selected agrichemicals to the two-spotted spider mite (Tetranychus urticae) on grape foliage. Plant Health Prog 6:1

    Article  Google Scholar 

  • Wei P, Chen M, Nan C, Feng K, Shen G, Cheng J, He L (2019) Downregulation of carboxylesterase contributes to cyflumetofen resistance in Tetranychus cinnabarinus (Boisduval). Pest Manag Sci 75:2166–2173

    Article  CAS  PubMed  Google Scholar 

  • Wilkening S, Hemminki K, Kumar Thirumaran R, Lorenzo Bermejo J, Bonn S, Försti A, Kumar R (2005) Determination of allele frequency in pooled DNA: comparison of three PCR-based methods. Biotechniques 39:853–858

    Article  CAS  PubMed  Google Scholar 

  • Wilson L, Bauer L, Lally D (1998) Effect of early season insecticide use on predators and outbreaks of spider mites (Acari: Tetranychidae) in cotton. Bull Entomol Res 88:477–488

    Article  CAS  Google Scholar 

  • Woolley LK, Chen Y, Herron GA(2015) Investigation of target site resistance mechanisms in sixteen Australian cultures of Tetranychus urticae (Tetranychidae: Acari). In: Australian cotton research conference, Science Securing Cotton’s Future. University of Southern Queensland, Toowoomba, pp 8–10

  • Wu M, Adesanya AW, Morales MA, Walsh DB, Lavine LC, Lavine MD, Zhu F (2019) Multiple acaricide resistance and underlying mechanisms in Tetranychus urticae on hops. J Pest Sci 92:543–555

    Article  Google Scholar 

  • Wybouw N et al (2019) Long-term population studies uncover the genome structure and genetic basis of xenobiotic and host plant adaptation in the herbivore. Tetranychus urticae. Genetics 211:1409–1427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu D, He Y, Zhang Y, Xie W, Wu Q, Wang S (2018) Status of pesticide resistance and associated mutations in the two-spotted spider mite, Tetranychus urticae, in China. Pest Biochem Physiol 150:89–96

    Article  CAS  Google Scholar 

  • Xue W, Snoeck S, Njiru C, Inak E, Dermauw W, Van Leeuwen T (2020) Geographical distribution and molecular insights into abamectin and milbemectin cross-resistance in European field populations of Tetranychus urticae. Pest Manag Sci 76:2569–2581

    Article  CAS  PubMed  Google Scholar 

  • Yalçin K, Döker İ, Kazak C (2018) Acaricide resistance in Tetranychus urticae red form (Acari: Tetranychidae) collected from strawberry in southern Turkey: bioassay and biochemical studies. Syst Appl Acarol 23:2279–2287

    Google Scholar 

  • Yang X, Buschman LL, Zhu KY, Margolies DC (2002) Susceptibility and detoxifying enzyme activity in two spider mite species (Acari: Tetranychidae) after selection with three insecticides. J Econ Entomol 95:399–406

    Article  CAS  PubMed  Google Scholar 

  • Yorulmaz S, Ay R (2009) Multiple resistance, detoxifying enzyme activity, and inheritance of abamectin resistance in Tetranychus urticae Koch (Acarina: Tetranychidae). Turk J Agric For 33:393–402

    CAS  Google Scholar 

  • Yu H, Cheng Y, Xu M, Song Y, Luo Y, Li B (2016) Synthesis, acaricidal activity, and structure–activity relationships of pyrazolyl acrylonitrile derivatives. J Agric Food Chem 64:9586–9591

    Article  CAS  PubMed  Google Scholar 

  • Zhu F (2007) Molecular mechanisms of cytochrome P450 monooxygenase-mediated pyrethroid resistance in the house fly, Musca domestica (L). PhD, Auburn Univerisity

  • Zhu F, Gujar H, Gordon JR, Haynes KF, Potter MF, Palli SR (2013) Bed bugs evolved unique adaptive strategy to resist pyrethroid insecticides. Sci Rep 3:1456

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu S, Noviello CM, Teng J, Walsh RM Jr, Kim JJ, Hibbs RE (2018) Structure of a human synaptic GABA(A) receptor. Nature 559:67–72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was supported by the United States Department of Agriculture National Institute of Food and Agriculture Specialty Crop Research Initiative (SCRI) (Award number 2014-51181-22381), the Hop Research Council, the Washington Hop Commission, and the Washington State Commission on Pesticide Registration. Authors express sincere apologies to our colleagues whose works were not referenced in this article.

Author information

Authors and Affiliations

  1. Irrigated Agriculture Research and Extension Center, Washington State University, Prosser, WA, 99350, USA

    Adekunle W. Adesanya, Mark D. Lavine & Douglas B. Walsh

  2. Department of Entomology, Washington State University, Pullman, WA, 99164, USA

    Adekunle W. Adesanya, Mark D. Lavine, Laura C. Lavine & Douglas B. Walsh

  3. Department of Entomology, Pennsylvania State University, University Park, PA, 16802, USA

    Timothy W. Moural & Fang Zhu

Authors
  1. Adekunle W. Adesanya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mark D. Lavine
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Timothy W. Moural
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Laura C. Lavine
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fang Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Douglas B. Walsh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Adekunle W. Adesanya or Douglas B. Walsh.

Ethics declarations

Conflict of interest

The authors declare they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Communicated by N. Desneux .

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Adesanya, A.W., Lavine, M.D., Moural, T.W. et al. Mechanisms and management of acaricide resistance for Tetranychus urticae in agroecosystems. J Pest Sci 94, 639–663 (2021). https://doi.org/10.1007/s10340-021-01342-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-021-01342-x

Keywords

Search

Navigation