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Insecticide resistance in the tomato pinworm Tuta absoluta: patterns, spread, mechanisms, management and outlook

  • R. N. C. GuedesEmail author
  • E. RoditakisEmail author
  • M. R. Campos
  • K. Haddi
  • P. Bielza
  • H. A. A. Siqueira
  • A. Tsagkarakou
  • J. Vontas
  • R. NauenEmail author
Review
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Abstract

The South American tomato pinworm, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae), is an invasive pest difficult to control. Insecticide application is quite common and remains the prevalent control method particularly in open-field cultivation systems. As a result, insecticide resistance to many chemical classes of insecticides has been described both in South America and in Europe. The development of insecticide resistance is relatively fast in this species, and the main mechanisms involved are altered target-site sensitivity and/or enhanced detoxification, depending on the chemical class. However, insecticide resistance mechanisms do not differ between South America and Europe and are mainly due to simple genotype variations leading to high levels of resistance. The presence of resistance alleles at low frequency, especially against newer chemistry, is of major concern, as they tend to spread with the invasions making tomato pinworm particularly difficult to control. The monitoring methods and management programmes developed for the species benefited from the pro-activity of the Insecticide Resistance Action Committee and its country groups, particularly in Brazil and Spain. Bioassay methods were developed, resistance monitoring activities initiated and resistance management guidance was provided. The implementation of integrated control programmes and appropriate resistance management strategies as part of such programs is of utmost importance to keep tomato pinworm infestations under economic damage thresholds, thus guaranteeing sustainable yields.

Keywords

Invasive species Insecticide resistance patterns Control failure Resistance management Target-site alteration Insecticide detoxification 
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Notes

Acknowledgements

We thank Drs. A. Biondi and N. Desneux for the invitation to prepare the present review and to the several funding agencies that have been providing financial support for the authors’ research on insecticide resistance in the tomato pinworm.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national and institutional guidelines for the care and use of animals were considered in the present study.

Informed consent

The authors of this manuscript accept that the paper is submitted for publication in the Journal of Pest Science, and report that this paper has not been published or accepted for publication in another journal, nor is under consideration at another journal.

References

  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. Arias-Martín M, García M, José M et al (2016) Effects of three-year cultivation of Cry1Ab-expressing Bt maize on soil microarthropod communities. Agric Ecosyst Environ 220:125–134CrossRefGoogle Scholar
  3. Balzan MV, Moonen AC (2012) Management strategies for the control of Tuta absoluta (Lepidoptera: Gelechiidae) damage in open-field cultivations of processing tomato in Tuscany (Italy). EPPO Bull 42:217–225CrossRefGoogle Scholar
  4. Banks NC, Paini DR, Baylists KL, Hodda M (2015) The role of global trade and transport network topology in the human-mediated dispersal of alien species. Ecol Lett 18:188–199.  https://doi.org/10.1111/ele.12397 CrossRefGoogle Scholar
  5. Barati R, Hejazi MJ, Mohammadi SA (2018) Insecticide susceptibility in Tuta absoluta (Lepidoptera: Gelechiidae) and metabolic characterization of resistance to diazinon. J Econ Entomol 111:1555–1557CrossRefGoogle Scholar
  6. Berger M, Piunean AM, Randall E et al (2016a) Insecticide resistance mediated by an exon skipping event. Mol Ecol 25:5692–5704CrossRefGoogle Scholar
  7. Berger M, Puinean AM, Bielza P, Jacobson R, Field LM, Bass C, Williamson M (2016) Mechanisms of spinosad resistance in European populations of the tomato leafminer. In: XXV International Congress of Entomology, 25–30 September, Orlando, FL, USAGoogle Scholar
  8. Bielza P (2008) Insecticide resistance management strategies against the western flower thrips, Frankliniella occidentalis. Pest Manag Sci 64:1131–1138CrossRefGoogle Scholar
  9. Bielza P, Espinosa PJ, Quinto V, Abellán J, Contreras J (2007) Synergism studies with binary mixtures of pyrethroid, carbamate and organophosphate insecticides on Frankliniella occidentalis (Pergande). Pest Manag Sci 63:84–89CrossRefGoogle Scholar
  10. Bielza P, Garcíaa-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, Siscaro G, Zappala L (2012) Using organic certified rather than synthetic pesticides may not be safer for biological control agents: selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphere 87:803–812CrossRefGoogle Scholar
  12. Biondi A, Zappalà L, Stark JD, Desneux N (2013) Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS ONE 8:e76548CrossRefGoogle Scholar
  13. Biondi A, Guedes RNC, Wan F-H, Desneux N (2018) Ecology, worldwide spread, and management of the invasive South American tomato pinworm, Tuta absoluta: past, present, and future. Annu Rev Entomol 63:239–258CrossRefGoogle Scholar
  14. Bradshaw CJA, Leroy B, Bellard C et al (2016) Massive yet grossly underestimated global costs of invasive insects. Nat Commun 7:12986CrossRefGoogle Scholar
  15. Brévault T, Sylla S, Diatte M, Bernadas G, Diarra K (2014) Tuta absoluta Meyrick (Lepidoptera: Gelechiidae): a new threat to tomato production in Sub-Saharan Africa. Afr Entomol 22:441–444CrossRefGoogle Scholar
  16. Campos MR, Rodrigues ARS, Silva WM et al (2014) Spinosad and the tomato borer Tuta absoluta: a bioinsecticide, an invasive pest threat, and high insecticide resistance. PLoS ONE 9:e103235CrossRefGoogle Scholar
  17. Campos MR, Silva TB, Silva WM et al (2015) Susceptibility of Tuta absoluta (Lepidoptera: Gelechiidae) Brazilian populations to ryanodine receptor modulators. Pest Manag Sci 71:537–544CrossRefGoogle Scholar
  18. Campos MR, Biondi A, Adiga A, Guedes RN, 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. Cherif A, Harbaoui K, Zappalà L, Grissa-Lebdi K (2018) Efficacy of mass trapping and insecticides to control T. absoluta in Tunisia. J Plant Dis Prot 125:51–61CrossRefGoogle Scholar
  20. Crossthwaite AJ, Bigot A, Camblin P, Goodchild J, Lind RJ, Slater R, Maienfisch P (2017) The invertebrate pharmacology of insecticides acting at nicotinic acetylcholine receptors. J Pestic Sci 42:67–83CrossRefGoogle Scholar
  21. Cutler GC (2013) Insects, insecticides and hormesis: evidence and considerations for study. Dose-Response 11:154–177CrossRefGoogle Scholar
  22. Cutler GC, Guedes RNC (2017) Occurrence and significance of insecticide-induced hormesis in insects. In: Duke SO, Kudsk P, Solomon K (eds) Pesticide dose: effects on the environment and target and non-target organisms. American Chemical Society, Washington, pp 101–119CrossRefGoogle Scholar
  23. Dângelo RAC, Campos MR, Silva PS, Guedes RNC (2018) Insecticide resistance and control failure likelihood of the whitefly Bemisia tabaci (MEAM1; B biotype): a Neotropical. Ann Appl Biol 172:88–99CrossRefGoogle Scholar
  24. Desneux N, Wajnberg E, Wyckhuys KAG et al (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
  25. Desneux N, Luna MG, Guillemaud T, Urbaneja A et al (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
  26. Douris V, Papapostolou KM, Ilias A, Roditakis E, Kounadi S, Riga M, Nauen E, Vontas J (2017) Investigation of the contribution of RyR target-site mutations in diamide resistance by CRISPR/Cas9 genome modification in Drosophila. Insect Biochem Mol Biol 87:127–135CrossRefGoogle Scholar
  27. Feyereisen R, Dermauw W, van Leeuwen T (2015) Genotype to phenotype, the molecular and physiological dimensions of resistance in arthropods. Pest Biochem Physiol 121:61–67CrossRefGoogle Scholar
  28. Galdino TVS, Picanço MC, de Morais EGF et al (2011) Metodologia de bioensaio para estudos de toxicidade de formulações comerciais de inseticidas a Tuta absoluta (Meyrick, 1917). Cienc Agrotecnol 35:869–877CrossRefGoogle Scholar
  29. Gontijo PC, Picanço MC, Pereira EJG et al (2013) Spatial and temporal variation in the control failure likelihood of the tomato leaf miner, Tuta absoluta. Ann Appl Biol 162:50–59CrossRefGoogle Scholar
  30. Guedes RNC (2017) Insecticide resistance, control failure likelihood and the First Law of Geography. Pest Manag Sci 73:479–484CrossRefGoogle Scholar
  31. Guedes RNC, Cutler GC (2014) Insecticide-induced hormesis and arthropod pest management. Pest Manag Sci 70:690–697CrossRefGoogle Scholar
  32. 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
  33. Guedes RNC, Siqueira HAA (2012) The tomato borer Tuta absoluta: insecticide resistance and control failure. CAB Rev Perspect Agric Vet Sci Nutr Nat Resour 7:1–7Google Scholar
  34. Guedes NMP, Tolledo J, Corrêa AS, Guedes RNC (2010) Insecticide-induced hormesis in an insecticide-resistant strain of the maize weevil, Sitophilus zeamais. J Appl Entomol 134:142–148CrossRefGoogle Scholar
  35. Guedes RNC, Smagghe G, Stark JD, Desneux N (2016) Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Annu Rev Entomol 61:43–62CrossRefGoogle Scholar
  36. Guedes RNC, Walse SS, Throne JE (2017) Sublethal exposure, insecticide resistance, and community stress. Curr Opin Insect Sci 21:47–53CrossRefGoogle Scholar
  37. Guillemaud T, Blin A, Legoff I et al (2015) The tomato borer, Tuta absoluta, invading the Mediterranean Basin, originates from a single introduction from Central Chile. Sci Rep 5:8371CrossRefGoogle Scholar
  38. 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 4:6924CrossRefGoogle Scholar
  39. 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 42:506–513CrossRefGoogle Scholar
  40. Haddi K, Berger M, Bielza P et al (2017) Mutation in the ace-1 gene of the tomato leaf miner (Tuta absoluta) associated with organophosphates resistance. J Appl Entomol 141:612–619CrossRefGoogle Scholar
  41. Han P, Zhang Y-N, Lu Z-Z, Wang S, Ma D-Y, Biondi A et al (2018) Are we ready for the invasion of Tuta absoluta? Unanswered key questions for elaborating an Integrated Pest Management package in Xinjiang, China. Entomol Gen 38:113–125CrossRefGoogle Scholar
  42. Han P, Bayram Y, Shaltiel-Harpaz L, Sohrabi F, Saji A, Esenali UT et al (2019) Tuta absoluta continues to disperse in Asia: damage, ongoing management and future challenges. J Pest Sci.  https://doi.org/10.1007/s10340-018-1062 Google Scholar
  43. Hill MP, Clusella-trullas S, Terblanche JS, Richardson DM (2016) Drivers, impacts, mechanisms and adaptation in insect invasions. Biol Invasions 18:883–891CrossRefGoogle Scholar
  44. IRAC (2014) Tuta absoluta—the tomato leafminer or tomato borer. Recommendations for Sustainable and Effective Resistance Management. http://www.irac-online.org/pests/tuta-absoluta/presentations/. Accessed 23 Oct 2018
  45. IRAC Spain (2009) Prevención de resistencias en Tuta absoluta. http://www.irac-online.org/countries/spain/publications/. Accessed 23 Oct 2018
  46. Karaagaç SU (2015) Enzyme activities and analysis of susceptibility levels in Turkish Tuta absoluta populations to chlorantraniliprole and metaflumizone insecticides. Phytoparasitica 43:693–700CrossRefGoogle Scholar
  47. Klieber J, Reineke A (2016) The entomopathogen Beauveria bassiana has epiphytic and endophytic activity against the tomato leaf miner Tuta absoluta. J Appl Entomol 140:580–589CrossRefGoogle Scholar
  48. Konuş M (2014) Analysing resistance of different T. absoluta (Meyrick) (Lepidoptera: Gelechiidae) strains to abamectin insecticide. Turkish J Biochem 39:291–297CrossRefGoogle Scholar
  49. Lee S-J, Caboni P, Tomizawa M, Casida JE (2004) Cartap hydrolysis relative to its action at the insect nicotinic channel. J Agric Food Chem 52:95–98CrossRefGoogle Scholar
  50. Li X, Schuler MA, Berenbaum MR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Ann Rev Entomol 52:231–253CrossRefGoogle Scholar
  51. Liebhold AM, Berec L, Brockerhoff EG et al (2016) Eradication of invading insect populations: from concepts to applications. Annu Rev Entomol 61:335–352CrossRefGoogle 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. Lockwood JL, Hoopes MF, Marchetti MP (2013) Invasion ecology, 2nd edn. Wiley, New YorkGoogle Scholar
  54. Lümmen P (2013) Calcium channels as molecular target sites of novel insecticides. Adv Insect Physiol 44:287–347CrossRefGoogle Scholar
  55. Mansour R, Brévault T, Chailleux A et al (2018) Occurrence, biology, natural enemies and management of Tuta absoluta in Africa. Entomol Gen 38:83–112CrossRefGoogle Scholar
  56. Martin EA, Reineking B, Seo B, Steffan-dewenter I (2013) Natural enemy interactions constrain pest control in complex agricultural landscapes. Proc Natl Acad Sci USA 110:5534–5539CrossRefGoogle Scholar
  57. Moulton JK, Pepper DA, Dennehy TJ (2000) Beet armyworm (Spodoptera exigua) resistance to spinosad. Pest Manag Sci 56:842–848CrossRefGoogle Scholar
  58. Nauen R (2006) Insecticide mode of action: return of the ryanodine receptor. Pest Manag Sci 62:690–692CrossRefGoogle Scholar
  59. Nauen R, Steinbach D (2016) Resistance to diamide insecticides in lepidopteran pests. In: Horowitz AR, Ishaaya I (eds) Advances in insect control and in resistance management. Springer, Dordrecht, pp 219–240CrossRefGoogle Scholar
  60. Pfeiffer DG, Muniappan R, Sall D et al (2013) First record of Tuta absoluta (Lepidoptera: Gelechiidae) in Senegal. Fla Entomol 96:661–662CrossRefGoogle Scholar
  61. Potting RP, Van Der Gaag DJ, Loomans A et al (2013) Pest risk analysis—Tuta absoluta, tomato leaf miner moth. Ministry of Agriculture, Nature and Food Quality. Plant Protection Service of the Netherlands, UtrechtGoogle Scholar
  62. Puinean AM, Lansdell SJ, Collins T et al (2013) A nicotinic acetylcholine receptor transmembrane point mutation (G275E) associated with resistance to spinosad in Frankliniella occidentalis. J Neurochem 124:590–601CrossRefGoogle Scholar
  63. Reyes M, Rocha K, Alarcón L et al (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
  64. Rinkevich FD, Du Y, Dong K (2013) Diversity and convergence of sodium channel mutations involved in resistance to pyrethroids. Pestic Biochem Physiol 106:93–100CrossRefGoogle Scholar
  65. Ripa SR, Rojas PS, Velasco G (1995) Releases of biological control agents of insect pests on Easter Island (Pacific Ocean). Entomophaga 40:427–440CrossRefGoogle Scholar
  66. Rix RR, Ayyanath MM (2004) Cutler GC (2016) Sublethal concentrations of imidacloprid increase reproduction, alter expression of detoxification genes, and prime Myzus persicae for subsequent stress. J Pest Sci 89:581–589CrossRefGoogle Scholar
  67. Roditakis E (2018) Insecticide mode of action and resistance management: lessons learned from the case of T. absoluta. In XI European Congress of Entomology, pp 56–57, Napoli 2–6 JulyGoogle Scholar
  68. Roditakis E, Skarmoutsou C, Staurakaki M (2013a) Toxicity of insecticides to populations of tomato borer Tuta absoluta (Meyrick) from Greece. Pest Manag Sci 69:834–840CrossRefGoogle Scholar
  69. Roditakis E, Skarmoutsou C, Staurakaki M et al (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 69:217–227CrossRefGoogle Scholar
  70. Roditakis E, Vasakis E, Grispou M et al (2015) First report of T. absoluta resistance to diamide insecticides. J Pest Sci 88:9–16CrossRefGoogle Scholar
  71. Roditakis E, Mavridis K, Riga M, Vasakis E, Morou E, Rison JL, Vontas J (2017a) Identification and detection of indoxacarb resistance mutations in the para sodium channel of the tomato leafminer, T. absoluta. Pest Manag Sci 73:1679–1688CrossRefGoogle Scholar
  72. Roditakis E, Steinbach D, Moritz G et al (2017b) Ryanodine receptor point mutations confer diamide insecticide resistance in tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae). Insect Biochem Mol Biol 80:11–20CrossRefGoogle Scholar
  73. Roditakis E, Vasakis E, García-Vidal L, del Rosario Martínez-Aguirre M, Rison JL, Haxaire-Lutun MO, Nauen R, Tsagkarakou A, Bielza P (2018) A four-year survey on insecticide resistance and likelihood of chemical control failure for tomato leaf miner T. absoluta in the European/Asian region. J Pest Sci 91:421–435CrossRefGoogle Scholar
  74. Salazar ER, Araya JE (1997) Deteccin de resistencia a insecticides en la polilla del tomate. Simiente 67:8–22Google Scholar
  75. Salazar ER, Araya JE (2001) Tomato moth, Tuta absoluta (Meyrick) response to insecticides in Arica, Chile. Agric Técnica 61:1–7Google Scholar
  76. Sankarganesh E, Firake DM, Sharma B et al (2017) Invasion of the South American Tomato Pinworm, Tuta absoluta, in northeastern India: a new challenge and biosecurity concerns. Entomol Gen 1:335–345CrossRefGoogle Scholar
  77. Santana PA Jr, Kumar L, Da Silva RS, Picanço MC (2019) Global geographic distribution of Tuta absoluta as affected by climate change. J Pest Sci.  https://doi.org/10.1007/s10340-018-1057-y Google Scholar
  78. Scott JG (2008) Unraveling the mystery of spinosad resistance in insects. J Pestic Sci 33:221–227CrossRefGoogle Scholar
  79. Sharma PL, Gavkare O (2017) New distributional record of invasive pest Tuta absoluta (Meyrick) in North-Western Himalayan Region of India. Natl Acad Sci Lett 40:217–220CrossRefGoogle Scholar
  80. Silva GA, Picanço MC, Bacci L et al (2011) Control failure likelihood and spatial dependence of insecticide resistance in the tomato pinworm, Tuta absoluta. Pest Manag Sci 67:913–920CrossRefGoogle Scholar
  81. Silva WM, Berger M, Bass C et al (2015) Status of pyrethroid resistance and mechanisms in Brazilian populations of Tuta absoluta. Pestic Biochem Physiol 122:8–14CrossRefGoogle Scholar
  82. Silva JE, Assis CPO, Ribeiro LMS, Siqueira HAA (2016a) Field-evolved resistance and cross-resistance of Brazilian Tuta absoluta (Lepidoptera: Gelechiidae) populations to diamide insecticides. J Econ Entomol 109:2190–2195CrossRefGoogle Scholar
  83. Silva TBM, Silva WM, Campos MR et al (2016b) Susceptibility levels of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) to minor classes of insecticides in Brazil. Crop Prot 79:80–86CrossRefGoogle Scholar
  84. Silva WM, Berger M, Bass C et al (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 131:1–8CrossRefGoogle Scholar
  85. Silva JE, Ribeiro LMS, Vinasco N et al (2019) Field-evolved resistance to chlorantraniliprole in the tomato pinworm Tuta absoluta: inheritance, cross-resistance profile, and metabolism. J Pest Sci.  https://doi.org/10.1007/s10340-018-1064-z Google Scholar
  86. Siqueira HAA, Guedes RNC, Picanço MC (2000a) Insecticide resistance in populations of Tuta absoluta (Lepidoptera: Gelechiidae). Agric For Entomol 2:147–153CrossRefGoogle Scholar
  87. Siqueira HAA, Guedes RNC, Picanço MC (2000b) Cartap resistance and synergism in populations of Tuta absoluta (Lep., Gelechiidae). J Appl Entomol 124:233–238CrossRefGoogle Scholar
  88. 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
  89. Soares MA, Campos MR, Passos LC, Carvalho GA (2019) Botanical insecticide and natural enemies: a potential combination for pest management against Tuta absoluta. J Pest Sci.  https://doi.org/10.1007/s10340-018-01074-5 Google Scholar
  90. Soliman T, Mourits MCM, Lansink AGJMO, Van Der Werf W (2015) Quantitative economic impact assessment of invasive plant pests: what does it require and when is it worth the effort? Crop Prot 69:9–17CrossRefGoogle Scholar
  91. Sparks TC, Nauen R (2015) IRAC: mode of action classification and insecticide resistance management. Pestic Biochem Physiol 121:122–128CrossRefGoogle Scholar
  92. Sparks TC, Dripps JE, Watson GB, Paroonagian D (2012) Resistance and cross-resistance to the spinosyns—a review and analysis. Pestic Biochem Physiol 102:1–10CrossRefGoogle Scholar
  93. Steinbach D, Gutbrod O, Lümmen P et al (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 63:14–22CrossRefGoogle Scholar
  94. Sylla S, Brevault T, Bal AB, Chailleux A, Diatte M, Desneux N et al (2017) Rapid spread of the tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae), an invasive pest in Sub-Saharan Africa. Entomol Gen 36:269–283CrossRefGoogle Scholar
  95. 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:e0135283CrossRefGoogle Scholar
  96. Troczka B, Zimmer CT, Elias J et al (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 42:873–880CrossRefGoogle Scholar
  97. Troczka BJ, Williams AJ, Williamson MS et al (2015) Stable expression and functional characterisation of the diamondback moth ryanodine receptor G4946E variant conferring resistance to diamide insecticides. Sci Rep 5:14680CrossRefGoogle Scholar
  98. Ugurlu Karaağaç S (2015) Enzyme activities and analysis of susceptibility levels in Turkish T. absoluta populations to chlorantraniliprole and metaflumizone insecticides. Phytoparasitica 43:693–700CrossRefGoogle Scholar
  99. Urbaneja A, Vercher R, Navarro V et al (2007) La polilla del tomate, Tuta absoluta. Phytoma Espana 194:16–23Google Scholar
  100. Visser D, Uys VM, Nieuwenhuis RJ, Pieterse W (2017) First records of the tomato leaf miner Tuta absoluta (Meyrick, 1917) (Lepidoptera: Gelechiidae) in South Africa. Bio Invasions Rec 6:301–305Google Scholar
  101. Vontas J et al (2018) Rapid selection of a pyrethroid metabolic enzyme CYP9K1 by operational malaria control activities. Proc Natl Acad Sci 115:4619–4624Google Scholar
  102. Wang X, Wu Y (2012) High levels of resistance to chlorantraniliprole evolved in field populations of Plutella xylostella. J Econ Entomol 105:1019–1023CrossRefGoogle Scholar
  103. Wang X-L, Su W, Zhang J-H et al (2016) Two novel sodium channel mutations associated with resistance to indoxacarb and metaflumizone in the diamondback moth, Plutella xylostella. Insect Sci 23:50–58CrossRefGoogle Scholar
  104. Yalçin M, Mermer S, Kozaci LD, Turgut C (2015) Insecticide resistance in two populations of T. absoluta (Meyrick, 1917) (Lepidoptera: Gelechiidae) from Turkey. Turkiye Entomoloji Dergisi 39:137–145Google Scholar
  105. Zibaee I, Mahmood K, Esmaeily M et al (2018) Organophosphate and pyrethroid resistances in the tomato leaf miner T. absoluta (Lepidoptera: Gelechiidae) from Iran. J Appl Entomol 142:181–191CrossRefGoogle Scholar
  106. Zimmer CT (2018) Characterization and monitoring of target-site resistance in the Ryanodine Receptor of the tomato leafminer, T. absoluta. In: XI European Congress of Entomology, pp 54–55, Napoli 2–6 JulyGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Departamento de EntomologiaUniversidade Federal de ViçosaViçosaBrazil
  2. 2.Hellenic Agricultural Organisation – ‘Demeter’Institute of Olive Tree, Subtropical Plants and VinicultureHeraklionGreece
  3. 3.INRA (French National Institute for Agricultural Research)Université Côte d´Azur, CNRS, UMA 1355–7254, Institut Sophia AgrobiotechSophia AntipolisFrance
  4. 4.Departamento de Producción VegetalUniversidad Politécnica de CartagenaCartagenaSpain
  5. 5.Departamento de Agronomia – EntomologiaUniversidade Federal Rural de PernambucoRecifeBrazil
  6. 6.Institute of Molecular Biology and BiotechnologyFoundation for Research and Technology-HellasHeraklionGreece
  7. 7.Department of Crop Science, Pesticide Science LabAgricultural University of AthensAthensGreece
  8. 8.Bayer AG, Crop Science DivisionR&D, Pest ControlMonheinGermany

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