Skip to main content
SpringerLink
Log in

First report of Tuta absoluta resistance to diamide insecticides

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

Abstract

The tomato borer Tuta absoluta (Lepidoptera: Gelechiidae) is an invasive pest of tomato crops that is rapidly expanding around the world. It is considered a devastating pest and its control heavily relies on application of insecticides. Diamides are a novel class of insecticides acting on insect ryanodine receptors and are highly effective against lepidopteran pests. To date, chlorantraniliprole and flubendiamide have been registered in the market and they have been extensively used to manage T. absoluta. In this study, a survey was conducted in Greece and Italy monitoring diamide resistance. The populations originating from Sicily (Italy) exhibited LC50s that ranged between 47.6–435 for chlorantraniliprole and 993–1.376 for flubendiamide, while for Crete (Greece) LC50s ranged between 0.14–2.45 for chlorantraniliprole and 1.7–8.4 for flubendiamide (LC50s in mg L−1). Comparing this result to the susceptible reference strain, high resistance levels for the Italian populations were detected, i.e., up to 2,414- and 1,742-fold for chlorantraniliprole and flubendiamide, respectively. Resistance ratios for Greek populations were found up to 14-fold for chlorantraniliprole and 11-fold for flubendiamide, suggesting that diamide resistance is low but increasing considering monitoring data over time. Hereby, we report for the first time, cases of resistance development to diamide insecticides in T. absoluta. These findings underline the importance of committing to the resistance management strategies for diamide insecticides.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

References

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

    Article  Google Scholar 

  • Biondi A, Desneux N, Siscaro G, Zappalà 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 87:803–812

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • Campos MR, Silva TBM, Silva WM, Silva JE, Siqueira HAA (2014b) Susceptibility of Tuta absoluta (Lepidoptera: Gelechiidae) Brazilian populations to ryanodine receptor modulators. Pest Manag Sci (in press)

  • 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 

  • Che W, Shi T, Wu Y, Yang Y (2013) Insecticide resistance status of field populations of Spodoptera exigua (Lepidoptera: Noctuidae) from China. J Econ Entomol 106:1855–1862

    Article  CAS  PubMed  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, Luemmen P, Lobitz N, Schulte T, Funke C, Fischer R, Masaki T, Yasokawa N, Tohnishi M (2006) Phthalic acid diamides activate ryanodine-sensitive Ca2+ release channels in insects. Cell Calcium 39:21–33

    Article  CAS  PubMed  Google Scholar 

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

    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 

  • 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 

  • 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 

  • He Y, Zhang J, Chen J (2014) Effect of synergists on susceptibility to chlorantraniliprole in field populations of chilo suppressalis (Lepidoptera: Pyralidae). J Econ Entomol 107:791–796

    Article  CAS  PubMed  Google Scholar 

  • IRAC (2011) Tuta absoluta-The Tomato Leafminer or Tomato Borer: Recommendations for sustainable and effective resistance management. http://www.irac-online.org/documents/tuta-absoluta-irm-booklet/. Accessed Oct 2014)

  • IRAC (2014) IRAC MoA Classification Scheme (Version 7.3.1). http://www.irac-online.org. Accessed Oct 2014

  • Lahm GP, Stevenson TM, Selby TP, Freudenberger JH, Cordova D, Flexner L, Bellin CA, Dubas CM, Smith BK, Hughes KA, Hollingshaus JG, Clark CE, Benner EA (2007) Rynaxypyr™: a new insecticidal anthranilic diamide that acts as a potent and selective ryanodine receptor activator. Bioorg Med Chem Lett 17:6274–6279

    Article  CAS  PubMed  Google Scholar 

  • Larson J, Redmond C, Potter D (2014) Impacts of a neonicotinoid, neonicotinoid–pyrethroid premix, and anthranilic diamide insecticide on four species of turf-inhabiting beneficial insects. Ecotoxicology 23:252–259

    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 

  • Mollá O, Biondi A, Alonso-Valiente M, Urbaneja A (2014) A comparative life history study of two mirid bugs preying on Tuta absoluta and Ephestia kuehniella eggs on tomato crops: implications for biological control. Biocontrol 59:175–183

    Article  Google Scholar 

  • Ribeiro LMS, Wanderley-Teixeira V, Ferreira HN, Teixeira ÁAC, Siqueira HAA (2014) Fitness costs associated with field-evolved resistance to chlorantraniliprole in Plutella xylostella (Lepidoptera: Plutellidae). Bull Entomol Res 104:88–96

    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, 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 

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

    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 

  • 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 

  • Sparks TC (2013) Insecticide discovery: an evaluation and analysis. Pestic Biochem Physiol 107:8–17

    Article  CAS  PubMed  Google Scholar 

  • Steinbach D, Moritz G, Schorn C, Nauen R (2014) Genetics and toxicology of diamide insecticide resistance in diamondback moth, with special reference to fitness cost. In: Xth European Congress of Entomology, pp. P319, 3–8 August, University of York, York

  • Su J, Lai T, Li J (2012) Susceptibility of field populations of Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) in China to chlorantraniliprole and the activities of detoxification enzymes. Crop Protect 42:217–222

    Article  CAS  Google Scholar 

  • Teixeira LA, Andaloro JT (2013) Diamide insecticides: global efforts to address insect resistance stewardship challenges. Pestic Biochem Physiol 106:76–78

    Article  CAS  Google Scholar 

  • Tohnishi M, Nakao H, Furuya T, Seo A, Kodama H, Tsubata K, Fujioka S, Hirooka T, Nishimatsu T (2005) Flubendiamide, a novel insecticide highly active against lepidopterous insect pests. J Pestic Sci 30:354–360

    Article  CAS  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 

  • Tsagkarakou A, Nikou D, Roditakis E, Sharvit M, Morin S, Vontas J (2009) Molecular diagnostics for detecting pyrethroid and organophosphate resistance mutations in the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae). Pestic Biochem Physiol 94:49–54

    Article  CAS  Google Scholar 

  • Uchiyama T, Ozawa A (2014) Rapid development of resistance to diamide insecticides in the smaller tea tortrix, Adoxophyes honmai (Lepidoptera: Tortricidae), in the tea fields of Shizuoka Prefecture, Japan. Appl Entomol Zool 49:1–6

    Article  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, Khakame SK, Ye C, Yang Y, Wu Y (2013) Characterisation of field-evolved resistance to chlorantraniliprole in the diamondback moth, Plutella xylostella, from China. Pest Manag Sci 69:661–665

    Article  CAS  PubMed  Google Scholar 

  • Wu M, Zhang S, Yao R, Wu S, Su J, Gao C (2014) Susceptibility of the rice stem borer, Chilo suppressalis (Lepidoptera: Crambidae), to flubendiamide in China. J Econ Entomol 107:1250–1255

    Article  PubMed  Google Scholar 

  • Zappalà L, Siscaro G, Biondi A, Mollá O, González-Cabrera J, Urbaneja A (2012) Efficacy of sulphur on Tuta absoluta and its side effects on the predator Nesidiocoris tenuis. J Appl Entomol 136:401–409

    Article  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 

Download references

Acknowledgments

This work was partially funded by DuPont de Nemours France S.A.S and Bayer CropScience AG, Germany. The authors would like to thank, DuPont for providing the Tuta absoluta populations from Sicily, the local agronomists for their support during sampling and Mr M. Kechagiadakis (Fytochem S.A., Neo Mirtos, lerapetra) for supplies of plant material.

Author information

Authors and Affiliations

  1. Plant Protection Institute of Heraklion, Hellenic Agricultural Organization ‘Demeter’ (former NAGREF), P.O. Box 2228, 71003, Heraklion, Crete, Greece

    Emmanouil Roditakis, Emmanouil Vasakis, Maria Grispou & Marianna Stavrakaki

  2. Bayer Crop Science, R&D, Pest Control Biology, Alfred Nobel Str. 50, 40789, Monheim, Germany

    Ralf Nauen

  3. DuPont de Nemours ERDC, 24 rue du Moulin, 68740, Nambsheim, France

    Magali Gravouil

  4. Du Pont de Nemours Italiana Srl, Via Pietro Gobetti 2/C, 20063, Cernusco sul Naviglio, MI, Italy

    Andrea Bassi

Authors
  1. Emmanouil Roditakis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emmanouil Vasakis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maria Grispou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marianna Stavrakaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ralf Nauen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Magali Gravouil
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Andrea Bassi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Emmanouil Roditakis.

Additional information

Communicated by N. Desneux.

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., Grispou, M. et al. First report of Tuta absoluta resistance to diamide insecticides. J Pest Sci 88, 9–16 (2015). https://doi.org/10.1007/s10340-015-0643-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-015-0643-5

Keywords

Search

Navigation