Baseline susceptibility and assessment of resistance risk to flubendiamide and chlorantraniliprole in Tuta absoluta (Lepidoptera: Gelechiidae) populations from Kuwait

  • Mustapha F. A. JallowEmail author
  • Abdelhafiz A. Dahab
  • Mohammed S. Albaho
  • Vimala Y. Devi
  • Dawood G. Awadh
  • Binson M. Thomas
Original Research Paper


The tomato leafminer, Tuta absoluta (Meyrick), is one of the most destructive pests of tomato worldwide. T. absoluta has developed resistance to a wide range of insecticides in the field. This study aimed to assess the baseline toxicity of field populations of T. absoluta to flubendiamide and chlorantraniliprole, diamide insecticides recently registered to control the pest in Kuwait. Subsequently, the risk of resistance evolving as well as inheritance of resistance to the insecticides was investigated. The susceptibility variation among the populations tested was low (threefold for flubendiamide and fourfold chlorantraniliprole). The LC50 values for flubendiamide ranged from 0.04 to 0.11 mg L−1, whereas the LC50 values for chlorantraniliprole ranged from 0.29 to 1.13 mg L−1. After 34 generations of selection, 750- and 860-fold increases in resistance were recorded for flubendiamide and chlorantraniliprole, respectively. The realized heritability (h2) of resistance was estimated as 0.21 for flubendiamide and 0.29 for chlorantraniliprole, using threshold trait analysis. The values of the response quotient (Q) for resistance against flubendiamide and chlorantraniliprole were 0.11 and 0.13, respectively. We discussed our results with regard to the development of diamide resistance in T. absoluta, the potential spread of resistance, and strategies to mitigate the evolution of resistance.


Tomato leafminer · Diamide insecticides · Baseline toxicity · Resistance · Resistance management 



The authors are grateful to the Kuwait Institute for Scientific Research and the Kuwait Foundation for the Advancement of Sciences for the financial support in carrying out this study (Grant Agreement No. FA116C-P215-42WE-03). The contribution of the farmers and the staff of the Kuwait Public Authority for Agriculture and Fish Resources to this study is gratefully acknowledged.


  1. Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267CrossRefGoogle Scholar
  2. Ayalew G (2015) Efficacy of selected insecticides against the South American tomato moth, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) on tomato in the Central Rift Valley of Ethiopia. Afr Entomol 23:410–417CrossRefGoogle Scholar
  3. Biondi A, Guedes RNC, Wan F, 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
  4. Brown A (1977) Resistance as a factor in pesticide management. XV International Congress of Entomology, 19–27 August 1976. DC, USA, Washington, pp 816–824Google Scholar
  5. CABI/EPPO. Tuta absoluta distribution map (2013) Wallingford, UK Center for Agriculture and Biosciences International, Map 723 (2nd revision)Google Scholar
  6. Campos MR, Rodrigues ARS, Silva WM, Silva TBM, Silva VRF, Guedes RNC, Siqueira HAA (2014) Spinosad and the tomato borer Tuta absoluta: a bioinsecticide, an invasive pest threat, and high insecticide resistance. PLoS ONE 9:e103235CrossRefGoogle Scholar
  7. Campos MR, Silva TB, Silva WM, Silva JE, Siqueira HA (2015a) Spinosyn resistance in the tomato borer Tuta absoluta (Meyrick)(Lepidoptera: Gelechiidae). J Pest Sci 88:405–412CrossRefGoogle Scholar
  8. Campos MR, Silva TBM, Silva WM, Silva JE, Siqueira HAA (2015b) Susceptibility of Tuta absoluta (Lepidoptera: Gelechiidae) Brazilian populations to ryanodine receptor modulators. Pest Manage Sci 71:537–544CrossRefGoogle Scholar
  9. Campos MR, Biondi A, Adiga A, Guedes RNC, Desneux N (2017) From the Western Palaearctic region to beyond: Tuta absoluta ten years after invading Europe. J Pest Sci 90:787–796CrossRefGoogle Scholar
  10. Cifuentes D, Chynoweth R, Bielza P (2011) Genetic study of Mediterranean and South American populations of tomato leafminer Tuta absoluta (Povolny, 1994)(Lepidoptera: Gelechiidae) using ribosomal and mitochondrial markers. Pest Manag Sci 67:1155–1162PubMedGoogle Scholar
  11. Cook DR, Leonard BR, Gore J, Temple JH (2005) Baseline responses of bollworm, Helicoverpa zea (Boddie), and tobacco budworm, Heliothis virescens (F.), to indoxacarb and pyridalyl. J Agric Urban Entomol 22:100–109Google Scholar
  12. 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. Pest Biochem Physiol 84:196–214CrossRefGoogle Scholar
  13. 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
  14. Desneux N, Wajnberg E, Wyckhuys KAG, Burgio G, Arpaia S, Narváez-Vasquez CA, González-Cabrera J, Catalán 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
  15. Falconer DS, Mackay TF, Frankham R (1996) Introduction to quantitative genetics, 4th edn. Longman, New YorkGoogle Scholar
  16. Finney D (1971) Probit Analysis, 3rd edn. Cambridge University Press, LondonGoogle Scholar
  17. French-Constant RH (2007) Which came first: insecticides or resistance? Trends Genet 23:1–4CrossRefGoogle Scholar
  18. Guedes RNC (2017) Insecticide resistance, control failure likelihood and the first law of geography. Pest Manag Sci 73:479–484CrossRefGoogle Scholar
  19. Guedes R, Siqueira H (2012) The tomato borer Tuta absoluta: insecticide resistance and control failure. CAB Rev Perspect Agric Vet Sci Nutr Nat Resour 7:1–7Google Scholar
  20. Guillemaud T et al (2015) The tomato borer, Tuta absoluta, invading the mediterranean basin, originates from a single introduction from Central Chile. Sci Rep 5:8371. CrossRefPubMedPubMedCentralGoogle Scholar
  21. IRAC (2015) IRAC susceptibility test methods series: Method 022. Insecticide Resistance Action Committee. Available online: Accessed 16 November, 2017
  22. Jallow MF, Awadh DG, Albaho MS, Devi VY, Thomas BM (2017a) Pesticide risk behaviors and factors influencing pesticide use among farmers in Kuwait. Sci Total Environ 574:490–498CrossRefGoogle Scholar
  23. Jallow MF, Awadh DG, Albaho MS, Devi VY, Thomas BM (2017b) Pesticide knowledge and safety practices among farm workers in Kuwait: results of a survey. Int J Environ Res Public Health 14:340. CrossRefPubMedCentralGoogle Scholar
  24. Jallow MF, Awadh DG, Albaho MS, Devi VY, Ahmad N (2017c) Monitoring of pesticide residues in commonly used fruits and vegetables in Kuwait. Int J Environ Res Public Health 14:833. CrossRefPubMedCentralGoogle Scholar
  25. Karaagac SU (2015) Enzyme activities and analysis of susceptibility levels in Turkish Tuta absoluta populations to chlorantraniliprole and metaflumizone insecticides. Phytoparasitica 43:693–700CrossRefGoogle Scholar
  26. 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
  27. LeOra Software, POLO-Plus, POLO for windows computer program, version 2.0. LeOra- software (2005), Petaluma, California, USAGoogle Scholar
  28. Megido RC, 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
  29. Naselli M, Biondi A, Tropea Garzia G, Desneux N, Russo A, Siscaro G, Zappala L (2017) Insights on food webs associated with the South American tomato pinworm. Pest Manag Sci 73:1352–1357CrossRefGoogle Scholar
  30. Nauen R, Steinbach D (2016) Resistance to diamide insecticides in lepidopteran pests. In: Horowitz AR, Ishaaya I (eds) Advances in insect control and resistance management. Springer, Switzerland, pp 219–240CrossRefGoogle Scholar
  31. Robertson J, Preisler H, Ng S, Hickle LA, Gelernter W (1995) Natural variation: a complicating factor in bioassays with chemical and microbial pesticides. J Econ Entomol 88:1–10CrossRefGoogle Scholar
  32. Robertson JL, Savin N, Russell RM, Preisler HK (2007) Bioassays with arthropods. CRC Press, Boca RatonGoogle Scholar
  33. Roditakis E, Skarmoutsou C, Staurakaki M (2013) Toxicity of insecticides to populations of tomato borer Tuta absoluta (Meyrick) from Greece. Pest Manag Sci 69:834–840CrossRefGoogle Scholar
  34. 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
  35. Roditakis E, Steinbach D, Moritz G et al (2017) Ryanodine receptor point mutations confer diamide insecticide resistance in tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae). Insect Biochem Mol Biol 80:11–20CrossRefGoogle Scholar
  36. Roditakis E, Vasakis E, Garcia-Vidal L et al (2018) 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 Science 91:421–435CrossRefGoogle Scholar
  37. 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 67:913–992CrossRefGoogle Scholar
  38. Silva JE, Assis CP, Ribeiro LM, Siqueira HA (2016) Field-evolved resistance and cross-resistance of Brazilian Tuta absoluta (Lepidoptera: Gelechiidae) populations to diamide insecticides. J Econ Entomol 109:2190–2195CrossRefGoogle Scholar
  39. 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 63:14–22CrossRefGoogle Scholar
  40. Tabashnik BE (1992) Resistance risk assessment: realized heritability of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae), tobacco budworm (Lepidoptera: Noctuidae), and Colorado potato beetle (Coleoptera: Chrysomelidae). J Econ Entomol 85:1551–1559CrossRefGoogle Scholar
  41. Tabashnik BE, McGaughey WH (1994) Resistance risk assessment for single and multiple insecticides: response of Indianmeal moth (Lepidoptera: Pyralidea) to Bacillus thuringiensis. J Econ Entomol 87:834–841CrossRefGoogle Scholar
  42. Terzidis AN, Wilcockson S, Leifert C (2014) The tomato leaf miner (Tuta absoluta): conventional pest problem, organic management solutions? Organ Agric 4:43–61CrossRefGoogle Scholar
  43. Tropea Garzia G, Siscaro G, Biondi A, Zappalà L (2012) Tuta absoluta, a South American pest of tomato now in the EPPO region: biology, distribution and damage. EPPO Bull 42:205–221CrossRefGoogle Scholar

Copyright information

© The Japanese Society of Applied Entomology and Zoology 2018

Authors and Affiliations

  • Mustapha F. A. Jallow
    • 1
    Email author
  • Abdelhafiz A. Dahab
    • 1
  • Mohammed S. Albaho
    • 1
  • Vimala Y. Devi
    • 1
  • Dawood G. Awadh
    • 1
  • Binson M. Thomas
    • 1
  1. 1.Environment and Life Sciences Research Center, Kuwait Institute for Scientific ResearchSafatKuwait

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