Journal of Pest Science

, Volume 91, Issue 1, pp 421–435 | Cite as

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

  • Emmanouil RoditakisEmail author
  • Emmanouil Vasakis
  • Lidia García-Vidal
  • María del Rosario Martínez-Aguirre
  • Jean Luc Rison
  • Marie Odile Haxaire-Lutun
  • Ralf Nauen
  • Anastasia Tsagkarakou
  • Pablo Bielza
Original Paper


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.


Chlorantraniliprole Indoxacarb Spinosad Emamectin benzoate Resistance Tuta absoluta Leaf miner Borer Tomato 



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.

Compliance with ethical standards

Conflict of interest

We declare that there is no conflict of interest.


  1. Abbes K, Harbi A, Chermiti B (2012) The tomato leafminer Tuta absoluta (Meyrick) in Tunisia: current status and management strategies. EPPO Bull 42:226–233CrossRefGoogle Scholar
  2. Abbot WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267CrossRefGoogle Scholar
  3. 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 56:372–379CrossRefGoogle Scholar
  4. 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, Accessed 17 Feb 2017
  5. 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 123:51–57CrossRefGoogle Scholar
  6. 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 139:71–81Google Scholar
  7. Armes NJ, Jadhav DR, DeSouza KR (1996) A survey of insecticide resistance in Helicoverpa armiger a in the Indian subcontinent. Bull Entomol Res 86:499–514CrossRefGoogle Scholar
  8. 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 25:164–169CrossRefGoogle Scholar
  9. 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 25:5692–5704CrossRefPubMedPubMedCentralGoogle Scholar
  10. 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, USAGoogle Scholar
  11. 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 106:1638–1647CrossRefPubMedGoogle Scholar
  12. 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 108:1191–1197CrossRefPubMedGoogle Scholar
  13. Brunherotto R, Vendramim JD (2001) Bioactivity of aqueous extracts of Melia azedarach L. on tomato pinworm Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotrop Entomol 30:455–459CrossRefGoogle Scholar
  14. 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 143:111–119CrossRefGoogle Scholar
  15. 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 88:405–412CrossRefGoogle Scholar
  16. 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:e103235CrossRefPubMedPubMedCentralGoogle Scholar
  17. 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 71:537–544CrossRefPubMedGoogle Scholar
  18. 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 90:787–796CrossRefGoogle Scholar
  19. 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 17:475–482Google Scholar
  20. 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 215–218Google Scholar
  21. 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 86:533–541CrossRefGoogle Scholar
  22. 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 137:16–28CrossRefGoogle Scholar
  23. 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 84:196–214CrossRefGoogle Scholar
  24. 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 223–234Google Scholar
  25. Deguine JP, Ferron P, Russell D (2008) Sustainable pest management for cotton production. A review. Agron Sustain Dev 28:113–137CrossRefGoogle Scholar
  26. 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 42:455–465CrossRefPubMedGoogle Scholar
  27. 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 83:197–215CrossRefGoogle Scholar
  28. 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 84:403–408CrossRefGoogle Scholar
  29. 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 60:117–139Google Scholar
  30. 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, USAGoogle Scholar
  31. 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, GreeceGoogle Scholar
  32. 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 4–38CrossRefGoogle Scholar
  33. Finney DJ (1964) Probit analysis. Cambridge University Press, CambridgeGoogle Scholar
  34. Fisher MH, Mrozik H (1992) The chemistry and pharmacology of avermectins. Annu Rev Pharmacol Toxicol 32:537–553CrossRefPubMedGoogle Scholar
  35. 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 106:2190–2194CrossRefPubMedGoogle Scholar
  36. Gong W, Yan HH, Gao L, Guo YY, Xue CB (2014) Chlorantraniliprole resistance in the diamondback moth (Lepidoptera: Plutellidae). J Econ Entomol 107:806–814CrossRefPubMedGoogle Scholar
  37. 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 162:50–59CrossRefGoogle Scholar
  38. 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 56:71–80CrossRefGoogle Scholar
  39. Guedes RNC (2017) Insecticide resistance, control failure likelihood and the First Law of Geography. Pest Manag Sci 73:479–484CrossRefPubMedGoogle Scholar
  40. Guedes RNC, Picanço MC (2012) The tomato borer Tuta absoluta in South America: pest status, management and insecticide resistance. EPPO Bull 42:211–216CrossRefGoogle Scholar
  41. 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 5:8371CrossRefPubMedPubMedCentralGoogle Scholar
  42. 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 4:6924CrossRefPubMedPubMedCentralGoogle Scholar
  43. 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 42:506–513CrossRefPubMedGoogle Scholar
  44. IRAC (2016) IRAC MoA classification scheme (version 8.1) Accessed Jan 2017
  45. 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 33:13–20CrossRefGoogle Scholar
  46. Jeanguenat A (2013) The story of a new insecticidal chemistry class: the diamides. Pest Manag Sci 69:7–14CrossRefPubMedGoogle Scholar
  47. 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 66:88–95CrossRefPubMedPubMedCentralGoogle Scholar
  48. 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 97:13949–13954CrossRefPubMedPubMedCentralGoogle Scholar
  49. 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 19:583–591CrossRefPubMedGoogle Scholar
  50. 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 15:4898–4906CrossRefPubMedGoogle Scholar
  51. Lasota JA, Dybas RA (1991) Avermectins, a novel class of compounds: implications for use in arthropod pest control. Annu Rev Entomol 36:91–117CrossRefPubMedGoogle Scholar
  52. Lietti MMM, Botto E, Alzogaray RA (2005) Insecticide resistance in Argentine populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotrop Entomol 34:113–119CrossRefGoogle Scholar
  53. 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 153:85–92CrossRefGoogle Scholar
  54. Lümmen P (2013) Calcium channels as molecular target sites of novel insecticides. In: Advances in insect physiology. Elsevier, pp 287–347Google Scholar
  55. 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 11:621–628CrossRefGoogle Scholar
  56. 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 68:386–393CrossRefPubMedGoogle Scholar
  57. Naranjo SE, Ellsworth PC (2009) Fifty years of the integrated control concept: moving the model and implementation forward in Arizona. Pest Manag Sci 65:1267–1286CrossRefPubMedPubMedCentralGoogle Scholar
  58. 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 219–240Google Scholar
  59. Perry AS, Yamamoto I, Ishaaya I, Perry RY (1997) Insect resistance. In: Insecticides in agriculture and environment: retrospects and prospects. Springer, pp 208–220Google Scholar
  60. 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 39:977–984CrossRefPubMedGoogle Scholar
  61. 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 66:371–378PubMedGoogle Scholar
  62. 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 102:45–50CrossRefGoogle Scholar
  63. 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 46:43–53CrossRefPubMedGoogle Scholar
  64. 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 65:313–322CrossRefPubMedGoogle Scholar
  65. Roditakis E, Papachristos D, Roditakis NE (2010) Current status of tomato leafminer Tuta absoluta in Greece. EPPO Bull 40:163–166CrossRefGoogle Scholar
  66. Roditakis E, Skarmoutsou C, Staurakaki M (2013a) Toxicity of insecticides to populations of tomato borer Tuta absoluta (Meyrick) from Greece. Pest Manag Sci 69:834–840CrossRefPubMedGoogle Scholar
  67. 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 69:217–227CrossRefPubMedGoogle Scholar
  68. 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 88:9–16CrossRefGoogle Scholar
  69. 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, USAGoogle Scholar
  70. 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 73:1679–1688CrossRefGoogle Scholar
  71. 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 80:11–20CrossRefPubMedGoogle Scholar
  72. Rugg D, Buckingham SD, Sattelle DB, Jansson RK (2005) The insecticidal macrocyclic lactones. Compr Mol Insect Sci 5:25–52CrossRefGoogle Scholar
  73. Sakuma M (1998) Probit analysis of preference data. Appl Entomol Zool 33:339–347CrossRefGoogle Scholar
  74. Salgado VL (1998) Studies on the mode of action of spinosad: insect symptoms and physiological correlates. Pestic Biochem Physiol 60:91–102CrossRefGoogle Scholar
  75. 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 67:913–920CrossRefPubMedGoogle Scholar
  76. 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 122:8–14CrossRefPubMedGoogle Scholar
  77. 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 109:2190–2195CrossRefGoogle Scholar
  78. 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 79:80–86CrossRefGoogle Scholar
  79. 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 131:1–8CrossRefPubMedGoogle Scholar
  80. 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 97:87–92CrossRefPubMedGoogle Scholar
  81. Siqueira HAA, Guedes RNC, Picanco MC (2000a) Cartap resistance and synergism in populations of Tuta absoluta (Lep., Gelechiidae). J Appl Entomol 124:233–238CrossRefGoogle Scholar
  82. Siqueira HAA, Guedes RNC, Picanco MC (2000b) Insecticide resistance in populations of Tula absoluta (Lepidoptera: Gelechiidae). Agric For Entomol 2:147–153CrossRefGoogle Scholar
  83. 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 47:247–251CrossRefGoogle Scholar
  84. 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 73:1364–1372CrossRefPubMedGoogle Scholar
  85. Sparks TC, Nauen R (2015) IRAC: Mode of action classification and insecticide resistance management. Pestic Biochem Physiol 121:122–128CrossRefPubMedGoogle Scholar
  86. 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 63:14–22CrossRefPubMedGoogle Scholar
  87. Thompson GD, Dutton R, Sparks TC (2000) Spinosad—a case study: an example from a natural products discovery programme. Pest Manage Sci 56:696–702CrossRefGoogle Scholar
  88. 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:e0135283CrossRefPubMedPubMedCentralGoogle Scholar
  89. 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 42:873–880CrossRefPubMedGoogle Scholar
  90. Urbaneja A, Vercher R, Navarro V, Porcuna JL, Garcia- Marí F (2007) La polilla del tomate, Tuta absoluta. Phytoma España 194:16–24Google Scholar
  91. 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 133:292–296CrossRefGoogle Scholar
  92. Viggiani G, Filella F, Delrio G, Ramassini W, Foxi C (2009) Tuta absoluta, nuovo lepidottero segnalato anche in Italia. L’Informatore Agrario 2:66–68Google Scholar
  93. Wang X, Wu Y (2012) High levels of resistance to chlorantraniliprole evolved in field populations of Plutella xylostella. J Econ Entomol 105:1019–1023CrossRefPubMedGoogle Scholar
  94. 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 25:116–125CrossRefPubMedGoogle Scholar
  95. 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 23:50–58CrossRefPubMedGoogle Scholar
  96. 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 35–57Google Scholar
  97. 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 86:635–647CrossRefGoogle Scholar
  98. 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 99:176–181CrossRefPubMedGoogle Scholar
  99. 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 26:152–163Google Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Emmanouil Roditakis
    • 1
    Email author
  • Emmanouil Vasakis
    • 1
  • Lidia García-Vidal
    • 2
  • María del Rosario Martínez-Aguirre
    • 2
  • Jean Luc Rison
    • 3
  • Marie Odile Haxaire-Lutun
    • 3
  • Ralf Nauen
    • 4
  • Anastasia Tsagkarakou
    • 1
  • Pablo Bielza
    • 2
  1. 1.Hellenic Agricultural Organisation - ‘Demeter’, Institute of Olive Tree, Subtropical Plants and VinicultureHeraklion, CreteGreece
  2. 2.Departamento de Producción VegetalUniversidad Politécnica de CartagenaCartagenaSpain
  3. 3.DuPont de Nemours ERDCNambsheimFrance
  4. 4.Bayer AG, Crop Science Division, R&D, Pest ControlMonheimGermany

Personalised recommendations