Skip to main content

Advertisement

Log in

A four-year survey on insecticide resistance and likelihood of chemical control failure for tomato leaf miner Tuta absoluta in the European/Asian region

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

Abstract

Tuta absoluta is an invasive destructive pest that is currently posing a major threat for tomato production worldwide. Insecticides are a key component of typical pest management schemes. Resistance to diamides, the most recently introduced class of insecticides, was recently reported in Italy. Monitoring of insecticide efficacy is the basic tool for proactive evidence-based resistance management. Here, we report the findings of a 4-year survey performed at the Euro-Asian region. A total of 35 populations were collected between 2012 and 2016 from Greece, Italy, Spain, Israel and UK. The response of these populations was evaluated through laboratory bioassays with the main insecticides used for T. absoluta control: chlorantraniliprole, indoxacarb, emamectin benzoate and spinosad. Analysis of the results indicated six cases of low/moderate resistance to the emamectin benzoate (resistance ratio (RR) > 15-fold), a single case of resistance to spinosad (RR: 33-fold) and five cases of resistance to indoxacarb (RR: 13- to 91-fold). Likelihood of control failure was detected for indoxacarb, but reports of poor field performance were absent. Resistance to chlorantraniliprole, after 2015, was widespread in Italy and Greece with high RR (>64-fold) and significant likelihood of control failure in most cases. Chlorantraniliprole resistance was also detected in Israel (RR: 22,573-fold) but not in Spain and UK (RR < twofold). The absence of diamide resistance in tomato leaf miner populations in Spain is most likely linked to a recently established integrated pest management program including non-chemical measures and the rotational use of insecticides of different mode of action classes.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abbes K, Harbi A, Chermiti B (2012) The tomato leafminer Tuta absoluta (Meyrick) in Tunisia: current status and management strategies. EPPO Bull 42:226–233

    Article  Google Scholar 

  • Abbot WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267

    Article  Google Scholar 

  • Abd El-Ghany NM, Abdel-Razek AS, Ebadah IMA, Mahmoud YA (2016) Evaluation of some microbial agents, natural and chemical compounds for controlling tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). J Plant Prot Res 56:372–379

    Article  Google Scholar 

  • AHDB (2015) PE 028—Tuta absoluta: investigating resistance to key insecticides and seeking alternative IPM compatible products. Jacobson R, Bass C (eds) Agriculture and Horticulture Development Board, https://horticulture.ahdb.org.uk/project/tuta-absoluta-investigating-resistance-key-insecticides-and-seeking-alternative-ipm. Accessed 17 Feb 2017

  • Aksoy E, Kovanci OB (2016) Mass trapping low-density populations of Tuta absoluta with various types of traps in field-grown tomatoes. J Plant Dis Prot 123:51–57

    Article  Google Scholar 

  • Alili D, Doumandji A, Benrima A, Doumandji S, Doumandji B (2014) Pheromone trapping and control by insect-proof nets of Tuta absoluta (Meyrick, 1917) in greenhouses and in the field at Fouka Marine. Bull Soc Zool Fr 139:71–81

    Google Scholar 

  • Armes NJ, Jadhav DR, DeSouza KR (1996) A survey of insecticide resistance in Helicoverpa armiger a in the Indian subcontinent. Bull Entomol Res 86:499–514

    Article  CAS  Google Scholar 

  • Benvenga SR, Fernandes OA, Gravena S (2007) Decision making for integrated pest management of the South American tomato pinworm based on sexual pheromone traps. Horticultura Brasileira 25:164–169

    Article  Google Scholar 

  • Berger M, Puinean AM, Randall E, Zimmer CT, Silva WM, Bielza P, Field LM, Hughes D, Mellor I, Hassani-Pak K, Siqueira HAA, Williamson MS, Bass C (2016) Insecticide resistance mediated by an exon skipping event. Mol Ecol 25:5692–5704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bielza P, García-Vidal L, Martínez-Aguirre MR (2016) Tuta absoluta—insecticide resistance management of this invasive species. In: XXV international congress of entomology, 25–30 September, Orlando, FL, USA

  • Biondi A, Desneux N, Amiens-Desneux E, Siscaro G, Zappalà L (2013) Biology and developmental strategies of the palaearctic parasitoid Bracon nigricans (Hymenoptera: Braconidae) on the neotropical moth Tuta absoluta (Lepidoptera: Gelechiidae). J Econ Entomol 106:1638–1647

    Article  PubMed  Google Scholar 

  • Biondi A, Zappalà L, Desneux N, Aparo A, Siscaro G, Rapisarda C, Martin T, Garzia GT (2015) Potential toxicity of α-cypermethrin-treated nets on Tuta absoluta (Lepidoptera: Gelechiidae). J Econ Entomol 108:1191–1197

    Article  CAS  PubMed  Google Scholar 

  • Brunherotto R, Vendramim JD (2001) Bioactivity of aqueous extracts of Melia azedarach L. on tomato pinworm Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotrop Entomol 30:455–459

    Article  Google Scholar 

  • Calvo FJ, Lorente MJ, Stansly PA, Belda JE (2012) Preplant release of Nesidiocoris tenuis and supplementary tactics for control of Tuta absoluta and Bemisa tabaci in greenhouse tomato. Entomol Exp Appl 143:111–119

    Article  Google Scholar 

  • Campos M, Silva TM, Silva W, Silva J, Siqueira HA (2014a) Spinosyn resistance in the tomato borer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). J Pest Sci 88:405–412

    Article  Google Scholar 

  • Campos MR, Rodrigues ARS, Silva WM, Silva TBM, Silva VRF, Guedes RNC, Siqueira HAA (2014b) Spinosad and the tomato borer Tuta absoluta: a bioinsecticide, an invasive pest threat, and high insecticide resistance. PLoS ONE 9:e103235

    Article  PubMed  PubMed Central  Google Scholar 

  • Campos MR, Silva TB, Silva WM, Silva JE, Siqueira HA (2015) Susceptibility of Tuta absoluta (Lepidoptera: Gelechiidae) Brazilian populations to ryanodine receptor modulators. Pest Manag Sci 71:537–544

    Article  CAS  PubMed  Google Scholar 

  • Campos MR, Biondi A, Adiga A, Guedes RNC, Desneux N (2017) From the Western Palaearctic region to beyond: Tuta absoluta 10 years after invading Europe. J Pest Sci 90:787–796

    Article  Google Scholar 

  • Caparros Megido R, Haubruge E, Verheggen FJ (2013) Pheromone-based management strategies to control the tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae). A review. Biotechnol Agron Soc Environ 17:475–482

    Google Scholar 

  • Ceparano G, Iovine G, Hirsch J, Neufert B (2015) Assessment of economic and environmental effects of using DuPont™ Evalio® AgroSystems for growing of processing tomatoes in Italy. In: Acta horticulturae, pp 215–218

  • Chailleux A, Bearez P, Pizzol J, Amiens-Desneux E, Ramirez-Romero R, Desneux N (2013) Potential for combined use of parasitoids and generalist predators for biological control of the key invasive tomato pest Tuta absoluta. J Pest Sci 86:533–541

    Article  Google Scholar 

  • Cocco A, Deliperi S, Delrio G (2013) Control of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in greenhouse tomato crops using the mating disruption technique. J Appl Entomol 137:16–28

    Article  CAS  Google Scholar 

  • Cordova D, Benner EA, Sacher MD, Rauh JJ, Sopa JS, Lahm GP, Selby TP, Stevenson TM, Flexner L, Gutteridge S, Rhoades DF, Wu L, Smith RM, Tao Y (2006) Anthranilic diamides: a new class of insecticides with a novel mode of action, ryanodine receptor activation. Pestic Biochem Physiol 84:196–214

    Article  CAS  Google Scholar 

  • Cordova D, Benner EA, Sacher MD, Rauh JJ, Sopa JS, Lahm GP, Selby TP, Stevenson TM, Flexner L, Gutteridge S, Rhoades DF, Wu L, Smith RM, Tao Y (2007) The novel mode of action of anthranilic diamide insecticides: Ryanodine receptor activation. In: Synthesis and chemistry of agrochemicals VII, pp 223–234

  • Deguine JP, Ferron P, Russell D (2008) Sustainable pest management for cotton production. A review. Agron Sustain Dev 28:113–137

    Article  Google Scholar 

  • Dermauw W, Ilias A, Riga M, Tsagkarakou A, Grbić M, Tirry L, Van Leeuwen T, Vontas J (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 Biochem Mol Biol 42:455–465

    Article  CAS  PubMed  Google Scholar 

  • Desneux N, Wajnberg E, Wyckhuys K, Burgio G, Arpaia S, Narvaez-Vasquez C, Gonzalez-Cabrera J, Catalan Ruescas D, Tabone E, Frandon J, Pizzol J, Poncet C, Cabello T, Urbaneja A (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci 83:197–215

    Article  Google Scholar 

  • Desneux N, Luna MG, Guillemaud T, Urbaneja A (2011) The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: the new threat to tomato world production. J Pest Sci 84:403–408

    Article  Google Scholar 

  • Ebbinghaus-Kintscher U, Lümmen P, Raming K, Masaki T, Yasokawa N (2007) Flubendiamide, the first insecticide with a novel mode of action on insect ryanodine receptors. Pflanzenschutz-Nachrichten Bayer 60:117–139

    CAS  Google Scholar 

  • Elias J, Stain W (2016) Diamide resistance management in the diamondback moth, Plutella xylostella. In: XXV international congress of entomology, 25–30 September, Orlando, FL, USA

  • Ellsworth PC, Li X, Dennehy TJ, Palumbo JC, Castle S, Prabhaker N, Nichols RL (2013) Is monitoring susceptibility of Bemisia tabaci to insecticides useful to management? In: First international whitefly symposium, 20–24 May, Kolymbari, Crete, Greece

  • ffrench-Constant RH, Roush RT (1990) Resistance detection and documentation: the relative roles of pesticidal and biochemical assays. In: Roush RT, Tabashnik BE (eds) Pesticide resistance in arthropods. Springer, Boston, pp 4–38

    Chapter  Google Scholar 

  • Finney DJ (1964) Probit analysis. Cambridge University Press, Cambridge

    Google Scholar 

  • Fisher MH, Mrozik H (1992) The chemistry and pharmacology of avermectins. Annu Rev Pharmacol Toxicol 32:537–553

    Article  CAS  PubMed  Google Scholar 

  • Gao C, Yao R, Zhang Z, Wu M, Zhang S, Su J (2013) Susceptibility baseline and chlorantraniliprole resistance monitoring in Chilo suppressalis (Lepidoptera: Pyralidae). J Econ Entomol 106:2190–2194

    Article  CAS  PubMed  Google Scholar 

  • Gong W, Yan HH, Gao L, Guo YY, Xue CB (2014) Chlorantraniliprole resistance in the diamondback moth (Lepidoptera: Plutellidae). J Econ Entomol 107:806–814

    Article  CAS  PubMed  Google Scholar 

  • Gontijo PC, Picanço MC, Pereira EJG, Martins JC, Chediak M, Guedes RNC (2013) Spatial and temporal variation in the control failure likelihood of the tomato leaf miner, Tuta absoluta. Ann Appl Biol 162:50–59

    Article  Google Scholar 

  • González-Cabrera J, Mollá O, Montón H, Urbaneja A (2011) Efficacy of Bacillus thuringiensis (Berliner) in controlling the tomato borer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Biocontrol 56:71–80

    Article  Google Scholar 

  • Guedes RNC (2017) Insecticide resistance, control failure likelihood and the First Law of Geography. Pest Manag Sci 73:479–484

    Article  CAS  PubMed  Google Scholar 

  • Guedes RNC, Picanço MC (2012) The tomato borer Tuta absoluta in South America: pest status, management and insecticide resistance. EPPO Bull 42:211–216

    Article  Google Scholar 

  • Guillemaud T, Blin A, Le Goff I, Desneux N, Reyes M, Tabone E, Tsagkarakou A, Niño L, Lombaert E (2015) The tomato borer, Tuta absoluta, invading the Mediterranean Basin, originates from a single introduction from Central Chile. Sci Rep 5:8371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo L, Liang P, Zhou X, Gao X (2014) Novel mutations and mutation combinations of ryanodine receptor in a chlorantraniliprole resistant population of Plutella xylostella (L.). Sci Rep 4:6924

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haddi K, Berger M, Bielza P, Cifuentes D, Field LM, Gorman K, Rapisarda C, Williamson MS, Bass C (2012) Identification of mutations associated with pyrethroid resistance in the voltage-gated sodium channel of the tomato leaf miner (Tuta absoluta). Insect Biochem Mol Biol 42:506–513

    Article  CAS  PubMed  Google Scholar 

  • IRAC (2016) IRAC MoA classification scheme (version 8.1) http://www.irac-online.org. Accessed Jan 2017

  • Ishtiaq M, Saleem MA, Razaq M (2011) Monitoring of resistance in Spodoptera exigua (Lepidoptera: Noctuidae) from four districts of the Southern Punjab, Pakistan to four conventional and six new chemistry insecticides. Crop Protect 33:13–20

    Article  Google Scholar 

  • Jeanguenat A (2013) The story of a new insecticidal chemistry class: the diamides. Pest Manag Sci 69:7–14

    Article  CAS  PubMed  Google Scholar 

  • Jiang D, Du Y, Nomura Y, Wang X, Wu Y, Zhorov BS, Dong K (2015) Mutations in the transmembrane helix S6 of domain IV confer cockroach sodium channel resistance to sodium channel blocker insecticides and local anesthetics. Insect Biochem Mol Biol 66:88–95

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kane NS, Hirschberg B, Qian S, Hunt D, Thomas B, Brochu R, Ludmerer SW, Zheng Y, Smith M, Arena JP, Cohen CJ, Schmatz D, Warmke J, Cully DF (2000) Drug-resistant Drosophila indicate glutamate-gated chloride channels are targets for the antiparasitics nodulisporic acid and ivermectin. Proc Natl Acad Sci USA 97:13949–13954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwon DH, Yoon KS, Clark JM, Lee SH (2010) 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

    Article  CAS  PubMed  Google Scholar 

  • Lahm GP, Selby TP, Freudenberger JH, Stevenson TM, Myers BJ, Seburyamo G, Smith BK, Flexner L, Clark CE, Cordova D (2005) Insecticidal anthranilic diamides: a new class of potent ryanodine receptor activators. Bioorg Med Chem Lett 15:4898–4906

    Article  CAS  PubMed  Google Scholar 

  • Lasota JA, Dybas RA (1991) Avermectins, a novel class of compounds: implications for use in arthropod pest control. Annu Rev Entomol 36:91–117

    Article  CAS  PubMed  Google Scholar 

  • Lietti MMM, Botto E, Alzogaray RA (2005) Insecticide resistance in Argentine populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotrop Entomol 34:113–119

    Article  Google Scholar 

  • Liu F, Shi X, Liang Y, Wu Q, Xu B, Xie W, Wang S, Zhang Y, Liu N (2014) A 36-bp deletion in the alpha subunit of glutamate-gated chloride channel contributes to abamectin resistance in Plutella xylostella. Entomol Exp Appl 153:85–92

    Article  CAS  Google Scholar 

  • Lümmen P (2013) Calcium channels as molecular target sites of novel insecticides. In: Advances in insect physiology. Elsevier, pp 287–347

  • Michereff Filho M, Vilela EF, Jham GN, Attygalle A, Svatoš A, Meinwald J (2000) Initial studies of mating disruption of the tomato moth, Tuta absoluta (Lepidoptera: Gelechiidae) using synthetic sex pheromone. J Braz Chem Soc 11:621–628

    Article  CAS  Google Scholar 

  • Moreno SC, Carvalho GA, Picanço MC, Morais EG, Pereira RM (2012) Bioactivity of compounds from Acmella oleracea against Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) and selectivity to two non-target species. Pest Manag Sci 68:386–393

    Article  CAS  PubMed  Google Scholar 

  • Naranjo SE, Ellsworth PC (2009) Fifty years of the integrated control concept: moving the model and implementation forward in Arizona. Pest Manag Sci 65:1267–1286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nauen R, Steinbach D (2016) Resistance to diamide insecticides in lepidopteran pests. In: Horowitz A, Ishaaya I (eds) Advances in insect control and resistance management. Springer, Cham, pp 219–240

  • Perry AS, Yamamoto I, Ishaaya I, Perry RY (1997) Insect resistance. In: Insecticides in agriculture and environment: retrospects and prospects. Springer, pp 208–220

  • Pires LM, Marques EJ, de Oliveira JV, Alves SB (2010) Selection of isolates of entomopathogenic fungi for controlling Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) and their compatibility with insecticides used in tomato crop. Neotrop Entomol 39:977–984

    Article  CAS  PubMed  Google Scholar 

  • Pu X, Yang Y, Wu S, Wu Y (2010) Characterisation of abamectin resistance in a field-evolved multiresistant population of Plutella xylostella. Pest Manag Sci 66:371–378

    CAS  PubMed  Google Scholar 

  • Reyes M, Rocha K, Alarcón L, Siegwart M, Sauphanor B (2012) Metabolic mechanisms involved in the resistance of field populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) to spinosad. Pestic Biochem Physiol 102:45–50

    Article  CAS  Google Scholar 

  • Riga M, Tsakireli D, Ilias A, Morou E, Myridakis A, Stephanou EG, Nauen R, Dermauw W, Van Leeuwen T, Paine M, Vontas J (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 

  • Roditakis E, Grispou M, Morou E, Kristoffersen JB, Roditakis NE, Nauen R, Vontas J, Tsagkarakou A (2009) Current status of insecticide resistance in Q biotype Bemisia tabaci populations from Crete. Pest Manag Sci 65:313–322

    Article  CAS  PubMed  Google Scholar 

  • Roditakis E, Papachristos D, Roditakis NE (2010) Current status of tomato leafminer Tuta absoluta in Greece. EPPO Bull 40:163–166

    Article  Google Scholar 

  • Roditakis E, Skarmoutsou C, Staurakaki M (2013a) Toxicity of insecticides to populations of tomato borer Tuta absoluta (Meyrick) from Greece. Pest Manag Sci 69:834–840

    Article  CAS  PubMed  Google Scholar 

  • Roditakis E, Skarmoutsou C, Staurakaki M, del Rosario Martínez-Aguirre M, García-Vidal L, Bielza P, Haddi K, Rapisarda C, Rison J-L, Bassi A, Teixeira LA (2013b) Determination of baseline susceptibility of European populations of Tuta absoluta (Meyrick) to indoxacarb and chlorantraniliprole using a novel dip bioassay method. Pest Manag Sci 69:217–227

    Article  CAS  PubMed  Google Scholar 

  • Roditakis E, Vasakis E, Grispou M, Stavrakaki M, Nauen R, Gravouil M, Bassi A (2015) First report of Tuta absoluta resistance to diamide insecticides. J Pest Sci 88:9–16

    Article  Google Scholar 

  • Roditakis E, Vasakis E, Stavrakaki M, Ilias A, Morou E, Steinbach D, Bielza P, Bass C, Bassi A, Nauen R, Vontas J, Tsagkarakou A (2016) The global importance of the tomato borer Tuta absoluta, its control and the current state of insecticide resistance. In: XXV international congress of entomology, p 3783, 25–30 September, Orlando, FL, USA

  • Roditakis E, Mavridis K, Riga M, Vasakis E, Morou E, Luc Rison J, Vontas J (2017a) Identification and detection of indoxacarb resistance mutations in the para sodium channel of the tomato leafminer, Tuta absoluta. Pest Manage Sci 73:1679–1688

    Article  CAS  Google Scholar 

  • Roditakis E, Steinbach D, Moritz G, Vasakis E, Stavrakaki M, Ilias A, García-Vidal L, Martínez-Aguirre MDR, Bielza P, Morou E, Silva JE, Silva WM, Siqueira ΗAA, Iqbal S, Troczka BJ, Williamson MS, Bass C, Tsagkarakou A, Vontas J, Nauen R (2017b) Ryanodine receptor point mutations confer diamide insecticide resistance in tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae). Insect Biochem Mol Biol 80:11–20

    Article  CAS  PubMed  Google Scholar 

  • Rugg D, Buckingham SD, Sattelle DB, Jansson RK (2005) The insecticidal macrocyclic lactones. Compr Mol Insect Sci 5:25–52

    Article  CAS  Google Scholar 

  • Sakuma M (1998) Probit analysis of preference data. Appl Entomol Zool 33:339–347

    Article  Google Scholar 

  • Salgado VL (1998) Studies on the mode of action of spinosad: insect symptoms and physiological correlates. Pestic Biochem Physiol 60:91–102

    Article  CAS  Google Scholar 

  • Silva GA, Picanço MC, Bacci L, Crespo ALB, Rosado JF, Guedes RNC (2011) Control failure likelihood and spatial dependence of insecticide resistance in the tomato pinworm, Tuta absoluta. Pest Manag Sci 67:913–920

    Article  CAS  PubMed  Google Scholar 

  • Silva WM, Berger M, Bass C, Balbino VQ, Amaral MHP, Campos MR, Siqueira HAA (2015) Status of pyrethroid resistance and mechanisms in Brazilian populations of Tuta absoluta. Pestic Biochem Physiol 122:8–14

    Article  CAS  PubMed  Google Scholar 

  • Silva JE, Assis CP, Ribeiro LM, Siqueira HA (2016a) Field-evolved resistance and cross-resistance of Brazilian Tuta absoluta (Lepidoptera: Gelechiidae) populations to diamide insecticides. J Econ Entomol 109:2190–2195

    Article  Google Scholar 

  • Silva TBM, Silva WM, Campos MR, Silva JE, Ribeiro LMS, Siqueira HAA (2016b) Susceptibility levels of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) to minor classes of insecticides in Brazil. Crop Protect 79:80–86

    Article  CAS  Google Scholar 

  • Silva WM, Berger M, Bass C, Williamson M, Moura DMN, Ribeiro LMS, Siqueira HAA (2016c) Mutation (G275E) of the nicotinic acetylcholine receptor α6 subunit is associated with high levels of resistance to spinosyns in Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Pestic Biochem Physiol 131:1–8

    Article  CAS  PubMed  Google Scholar 

  • Silver KS, Song W, Nomura Y, Salgado VL, Dong K (2010) Mechanism of action of sodium channel blocker insecticides (SCBIs) on insect sodium channels. Pestic Biochem Physiol 97:87–92

    Article  CAS  PubMed  Google Scholar 

  • Siqueira HAA, Guedes RNC, Picanco MC (2000a) Cartap resistance and synergism in populations of Tuta absoluta (Lep., Gelechiidae). J Appl Entomol 124:233–238

    Article  CAS  Google Scholar 

  • Siqueira HAA, Guedes RNC, Picanco MC (2000b) Insecticide resistance in populations of Tula absoluta (Lepidoptera: Gelechiidae). Agric For Entomol 2:147–153

    Article  Google Scholar 

  • Siqueira HAA, Guedes RNC, Fragoso DB, Magalhaes LC (2001) Abamectin resistance and synergism in Brazilian populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Int J Pest Manag 47:247–251

    Article  Google Scholar 

  • Slater R, Stratonovitch P, Elias J, Semenov MA, Denholm I (2017) Use of an individual-based simulation model to explore and evaluate potential insecticide resistance management strategies. Pest Manag Sci 73:1364–1372

    Article  CAS  PubMed  Google Scholar 

  • Sparks TC, Nauen R (2015) IRAC: Mode of action classification and insecticide resistance management. Pestic Biochem Physiol 121:122–128

    Article  CAS  PubMed  Google Scholar 

  • Steinbach D, Gutbrod O, Lümmen P, Matthiesen S, Schorn C, Nauen R (2015) Geographic spread, genetics and functional characteristics of ryanodine receptor based target-site resistance to diamide insecticides in diamondback moth, Plutella xylostella. Insect Biochem Mol Biol 63:14–22

    Article  CAS  PubMed  Google Scholar 

  • Thompson GD, Dutton R, Sparks TC (2000) Spinosad—a case study: an example from a natural products discovery programme. Pest Manage Sci 56:696–702

    Article  CAS  Google Scholar 

  • Tonnang HEZ, Mohamed SF, Khamis F, Ekesi S (2015) Identification and risk assessment for worldwide invasion and spread of Tuta absoluta with a focus on Sub-Saharan Africa: implications for phytosanitary measures and management. PLoS ONE 10:e0135283

    Article  PubMed  PubMed Central  Google Scholar 

  • Troczka B, Zimmer CT, Elias J, Schorn C, Bass C, Davies TGE, Field LM, Williamson MS, Slater R, Nauen R (2012) Resistance to diamide insecticides in diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae) is associated with a mutation in the membrane-spanning domain of the ryanodine receptor. Insect Biochem Mol Biol 42:873–880

    Article  CAS  PubMed  Google Scholar 

  • Urbaneja A, Vercher R, Navarro V, Porcuna JL, Garcia- Marí F (2007) La polilla del tomate, Tuta absoluta. Phytoma España 194:16–24

    Google Scholar 

  • Urbaneja A, Montón H, Mollá O (2009) Suitability of the tomato borer Tuta absoluta as prey for Macrolophus pygmaeus and Nesidiocoris tenuis. J Appl Entomol 133:292–296

    Article  Google Scholar 

  • Viggiani G, Filella F, Delrio G, Ramassini W, Foxi C (2009) Tuta absoluta, nuovo lepidottero segnalato anche in Italia. L’Informatore Agrario 2:66–68

    Google Scholar 

  • Wang X, Wu Y (2012) High levels of resistance to chlorantraniliprole evolved in field populations of Plutella xylostella. J Econ Entomol 105:1019–1023

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Wang R, Yang Y, Wu S, O’Reilly AO, Wu Y (2016a) A point mutation in the glutamate-gated chloride channel of Plutella xylostella is associated with resistance to abamectin. Insect Mol Biol 25:116–125

    Article  CAS  PubMed  Google Scholar 

  • Wang XL, Su W, Zhang JH, Yang YH, Dong K, Wu YD (2016b) Two novel sodium channel mutations associated with resistance to indoxacarb and metaflumizone in the diamondback moth, Plutella xylostella. Insect Sci 23:50–58

    Article  CAS  PubMed  Google Scholar 

  • Wing KD, Andaloro JT, McCann SF (2010) Indoxacarb and the sodium channel blocker insecticides: chemistry, physiology and biology in insects. In: Gilbert LI, Gill SS (eds) Insect control biological and synthetic agents. Elsevier, Oxford, pp 35–57

    Google Scholar 

  • Zappalà L, Biondi A, Alma A, Al-Jboory IJ, Arnò J, Bayram A, Chailleux A, El-Arnaouty A, Gerling D, Guenaoui Y, Shaltiel-Harpaz L, Siscaro G, Stavrinides M, Tavella L, Vercher Aznar R, Urbaneja A, Desneux N (2013) Natural enemies of the South American moth, Tuta absoluta, in Europe, North Africa and Middle East, and their potential use in pest control strategies. J Pest Sci 86:635–647

    Article  Google Scholar 

  • Zhao JZ, Collins HL, Li YX, Mau RFL, Thompson GD, Hertlein M, Andaloro JT, Boykin R, Shelton AM (2006) Monitoring of diamondback moth (Lepidoptera: Plutellidae) resistance to spinosad, indoxacarb, and emamectin benzoate. J Econ Entomol 99:176–181

    Article  CAS  PubMed  Google Scholar 

  • Zimmer CT, Panini M, Singh KS, Randall EL, Field LM, Roditakis E, Mazzoni E, Bass C (2017) Use of the synergist piperonyl butoxide can slow the development of alpha-cypermethrin resistance in the whitefly Bemisia tabaci. Insect Mol Biol 26:152–163

    Google Scholar 

Download references

Acknowledgements

Hellenic Agricultural Organisation—‘Demeter’ was partially supported by an ARIMnet2 StomP grant to A. Tsagkarakou and E. Roditakis. Emmanouil Vasakis was supported by a scholarship provided by the Hellenic Entomological Society. The Universidad Politécnica de Cartagena would like to thank for partial financial support the Ministerio de Economía y Competitividad of Spain and FEDER (AGL2011-25164). Lidia García-Vidal holds a grant from the MECD (FPU13/01528). Also, the work was partially supported by grants provided by DuPont De Nemours to E. Roditakis and P. Bielza and by Bayer AG to E. Roditakis. Finally, the Hellenic Agricultural Organisation—‘Demeter’ would like to thank Fytochem S.A., Neo Mirtos, Ierapetra for supplies of plant material, as well as agronomists in Greece, Italy, Israel, Spain and UK for their support in sample collection.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Emmanouil Roditakis.

Ethics declarations

Conflict of interest

We declare that there is no conflict of interest.

Additional information

Communicated by M. Traugott.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Roditakis, E., Vasakis, E., García-Vidal, L. et al. A four-year survey on insecticide resistance and likelihood of chemical control failure for tomato leaf miner Tuta absoluta in the European/Asian region. J Pest Sci 91, 421–435 (2018). https://doi.org/10.1007/s10340-017-0900-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-017-0900-x

Keywords

Navigation