Skip to main content
SpringerLink
Log in

Efficiency of spinosad, Bacillus thuringiensis and Trichogramma brassicae against the tomato leafminer in greenhouse

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

The objective of this study was to evaluate the efficacy of three eco-friendly control agents, either singly or in a pairwise combination, for the control of the tomato leafminer, Tuta absoluta (Meyrick) (Lep: Gelechiidae). They include the naturally derived pesticide spinosad, a commercially available formulation of Bacillus thuringiensis var. Kurstaki (Bt), and a native population of Trichogramma brassicae Bezdenko (Hym: Trichogrammatidae). Tomato plants containing the T. absoluta were treated with one of the seven following treatments in a greenhouse: (1) a single release of T. brassicae against the eggs; (2) two applications of Bt (2 kg ha−1); (3) and (4) one application of spinosad at two rates (60 and 120 g a.i. ha−1); (5) T. brassicae release + Bt spray; (6) T. brassicae release + spinosad spray; and (7) spinosad spray + Bt spray. The highest mortality rate was recorded for the spinosad + Bt (88.33 ± 1.43%) and T. brassicae + spinosad (78.33 ± 3.74%) combinations, respectively; while the lowest mortality rate was obtained through the single application of T. brassicae (31.67 ± 4.84%). Based on our results, the Bt and spinosad seem to be suitable candidates for combination with other biological and cultural techniques towards an integrated management of the tomato leafminer.

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
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ahmadipour R, Shakarami J, Farrokhi S, Jafari S (2016) Evaluation of Trichogramma brassicae native populations as egg parasitoid of tomato leafminer, Tuta absoluta (Meyrick) in the laboratory conditions. Biocontrol Plant Prot 3:109–122

    Google Scholar 

  • Arno J, Gabarra R (2011) Side effects of selected insecticides on the Tuta absoluta (Lepidoptera: Gelechiidae) predators Macrolophus pygmaeus and Nesidiocoris tenuis (Hemiptera: Miridae). J Pest Sci 84:513–520

    Article  Google Scholar 

  • Barbosa WF, Smagghe G, Guedes RNC (2015) Pesticides and reduced-risk insecticides, native bees and pantropical stingless bees: pitfalls and perspectives. Pest Manag Sci 71:1049–1053

    Article  PubMed  CAS  Google Scholar 

  • Biondi A, Desneux N, Siscaro G, Zappalà L (2012a) 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  PubMed  CAS  Google Scholar 

  • Biondi A, Mommaerts V, Smagghe G, Vinuela E, Zappal L, Desneux N (2012b) The non-target impact of spinosyns on beneficial arthropods. Pest Manag Sci 68:1523–1536

    Article  PubMed  CAS  Google Scholar 

  • 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(9):e76548

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cabello T, Gallego JR, Vila E, Soler A, Pino M, Camero A, Hernández-Suárez E, Polaszek A (2009) Biological control of the South American Tomato Pinworm, Tuta absoluta (Lep.: Gelechiidae), with releases of Trichogramma achaeae (Hym.: Trichogrammatidae) in tomato greenhouses of Spain. IOBC/WPRS Bull 49:225–230

    Google Scholar 

  • 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(8):e103235

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cascone P, Carpenito C, Slotsbo S, Iodice L, Sorensen JG, Holmstrup M, Guerrieri E (2015) Improving the efficiency of Trichogramma achaeae to control Tuta absoluta. BioControl 60:761–771

    Article  Google Scholar 

  • Chailleux A, Desneux N, Seguret J, Maignet P, Khanh HDT, Tabone E (2012) Assessing European egg parasitoids as a mean of controlling the invasive South American tomato pinworm Tuta absoluta. PLoS ONE 7(10):e48068

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chailleux A, Biondi A, Han P, Tabone E, Desneux N (2013) Suitability of the pest–plant system Tuta absoluta (Lepidoptera: Gelechiidae)—tomato for Trichogramma (Hymenoptera: Trichogrammatidae) parasitoids and insights for biological control. J Econ Entomol 106:2310–2321

    Article  PubMed  Google Scholar 

  • Cherif A, Kaouthar LG (2013) Trichogramma cacoeciae as a biological control agent of the tomato pinworm Tuta absoluta in Northeastern Tunisia. Entomol Hell 22:35–42

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Derbalah AS, Morsey SZ, El-Samahy M (2012) Some recent approaches to control Tuta absoluta in tomato under greenhouse conditions. Afr Entomol 20:27–34

    Article  Google Scholar 

  • Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106

    Article  PubMed  CAS  Google Scholar 

  • Desneux N, Wajnberg E, Wyckhuys KAG, Burgio G, Arpaia S, Narváez-Vasquez CA, González-Cabrera J, Ruescas DC, Tabone E, Frandon J (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 

  • Ebrahimi E, Pintureau B, Shojai M (1998) Morphological and enzymatic study of the genus Trichogramma in Iran (Hym. Trichogrammatidae). Appl Entomol Phytopathol 66:39–42

    Google Scholar 

  • El-Arnaouty A, Pizzol J, Galal HH, Kortam MN, Afifi AI, Beyssat V, Desneux N, Biondi A, Heikal IH (2014) Assessment of the efficacy of two Trichogramma species in controlling Tuta absoluta in North African tomato greenhouses. Afr Entomol 22:801–809

    Article  Google Scholar 

  • Faria CA, Torres JB, Farias AMI (2000) Resposta funcional de Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) parasitando ovos de Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae): efeito da idade do hospedeiro. An Soc Entomol Bras 29:85–93

    Article  Google Scholar 

  • Gentz MC, Murdoch G, King GF (2010) Tandem use of selective insecticides and natural enemies for effective, reduced-risk pest management. Biol Control 52:208–215

    Article  Google Scholar 

  • Ghoneim K (2014) Parasitic insects and mites as potential biocontrol agents for a devastative pest of tomato, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) in the world: a review. Int J Adv Res 2:81–115

    Google Scholar 

  • Giustolin TA, Vendramim JD, Alves SB, Vieira SA, Pereira RM (2001) Susceptibility of Tuta absoluta (Meyrick) (Lep., Gelechiidae) reared on two species of Lycopersicon to Bacillus thuringiensis var. kurstaki. J Appl Entomol 125:551–556

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Hashemitassuji A, Safaralizadeh MH, Aramideh S, Hashemitassuji Z (2014) Effects of Bacillus thuringiensis var. kurstaki and Spinosad on three larval stages 1st, 2nd and 3rd of tomato borer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in laboratory conditions. Arch Phytopathol Plant Protect 48:1–8

    Google Scholar 

  • Kennedy GG (2003) Tomato, pests, parasitoids, and predators: tritrophic interactions involving the genus Lycopersicon. Annu Rev Entomol 48:51–72

    Article  PubMed  CAS  Google Scholar 

  • Kogan M (1998) Integrated pest management: historical perspectives and contemporary developments. Annu Rev Entomol 43:243–270

    Article  PubMed  CAS  Google Scholar 

  • Korycinska A, Moran H (2009) Plant Pest Notice: South American tomato moth, Tuta absoluta. Food Environ Res Agency 56:1–4

    Google Scholar 

  • Ksentini I, Jardak T, Zeghal N (2010) Bacillus thuringiensis, deltamethrin and spinosad side-effects on three Trichogramma species. B Insectol 63:31–37

    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 

  • Martinou AF, Seraphides N, Stavrinides MC (2014) Lethal and behavioral effects of pesticides on the insect predator Macrolophus pygmaeus. Chemosphere 96:167–173

    Article  PubMed  CAS  Google Scholar 

  • Medeiros MA, Vilela NJ, França FH (2006) Technical and economic efficiency of biological control of the South American tomato pinworm in protected environment. Hortic Bras 24:180–184

    Article  Google Scholar 

  • 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 17:475–482

    Google Scholar 

  • Molla O, Monton H, Vanaclocha P, Beitia F, Urbaneja A (2009) Predation by the mirids Nesidiocoris tenuis and Macrolophus pygmaeus on the tomato borer Tuta absoluta. IOBC/WPRS Bull 49:209–214

    Google Scholar 

  • Molla O, Gonzalez-Cabrera J, Urbaneja A (2011) The combined use of Bacillus thuringiensis and Nesidiocoris tenuis against the tomato borer Tuta absoluta. BioControl 56:71–80

    Article  Google Scholar 

  • Nazarpour L, Yarahmadi F, Saber M, Rajabpour A (2016) Short and long term effects of some bio-insecticides on Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) and its coexisting generalist predators in tomato fields. J Crop Prot 5:331–342

    Article  Google Scholar 

  • Oliveira L, Durao AC, Fontes J, Roja IS, Tavares J (2017) Potential of Trichogramma achaeae (Hymenoptera: Trichogrammatidae) in biological control of Tuta absoluta (Lepidoptera: Gelechiidae) in Azorean greenhouse tomato crops. J Econ Entomol 110:2010–2015

    Article  PubMed  Google Scholar 

  • Parra JRP, Zucchi RA (2004) Trichogramma in Brazil: feasibility of use after twenty years of research. Neotrop Entomol 33:271–281

    Article  Google Scholar 

  • Picanco M, Leite GLD, Guedes RNC, Silva EA (1998) Yield loss in trellised tomato affected by insecticidal sprays and plant spacing. Crop Prot 17:447–452

    Article  Google Scholar 

  • Pratissoli D, Thuler RT, Andrade GS, Zanotti LCM, da Silva AF (2005) Estimate of Trichogramma pretiosum to control Tuta absoluta in stalked tomato. Pesqu Agropecu Bras 40:715–718

    Article  Google Scholar 

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

    Article  CAS  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 

  • Salehi Z, Yarahmadi F, Rasekh A, Sohani NZ (2016) Functional responses of Orius albidipennis Reuter (Hemiptera, Anthocoridae) to Tuta absoluta Meyrick (Lepidoptera, Gelechiidae) on two tomato cultivars with different leaf morphological characteristics. Entomol Gen 36:127–136

    Article  Google Scholar 

  • SAS Institute (2011) SAS/STAT user’s guide, version 9.3. SAS Institute, Cary

    Google Scholar 

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

    Article  Google Scholar 

  • Sithanantham S, Ballal CR, Jalali SK, Bakthavatsalam N (2013) Biological control of insect pests using egg parasitoids. Springer, India

    Book  Google Scholar 

  • Sohrabi F, Nooryazdan H, Gharati B, Saeidi Z (2016) Evaluation of ten tomato cultivars for resistance against tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) under field infestation conditions. Entomol Gen 36:163–175

    Article  Google Scholar 

  • Tomé HVV, Barbosa WF, Martins GF, Guedes RNC (2015) Spinosad in the native stingless bee Melipona quadrifasciata: Regrettable non-target toxicity of a bioinsecticide. Chemosphere 124:103–109

    Article  PubMed  CAS  Google Scholar 

  • Urbaneja A, Sanchez E, Stansly PA (2007) Life history of Eretmocerus mundus, a parasitoid of Bemisia tabaci, on tomato and sweet pepper. BioControl 52:25–39

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Wajnberg E, Hassan SA (1994) Biological control with egg parasitoids. CABI Publishing, Wallingford

    Google Scholar 

  • Williams T, Valle J, Vinuela E (2003) Is the naturally derived insecticide spinosad compatible with natural enemies? Biocontrol Sci Technol 13:459–475

    Article  Google Scholar 

  • Youssef NA, Hassan GM (2013) Bioinsecticide activity of Bacillus thuringiensis isolates on tomato borer, Tuta absoluta (Meyrick) and their molecular identification. Afr J Biotech 12:3699–3709

    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

Acknowledgements

The authors would like to thank the Iranian Research Institute of Plant Protection (IRIPP) for providing biological agents and experimental materials. This study was financially supported by the University of Tehran. We thank two anonymous reviewers for helpful comments on an earlier version of the manuscript.

Author information

Authors and Affiliations

  1. Department of Entomology and Plant Pathology, College of Abouraihan, University of Tehran, Tehran, Iran

    Arsalan Jamshidnia, Saba Abdoli & Reza Sadeghi

  2. Biological Control Research Department, Iranian Research Institute of Plant Protection, Agricultural Research, Education and Extension Organization (AREEO), Tehran, Iran

    Shahram Farrokhi

Authors
  1. Arsalan Jamshidnia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Saba Abdoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shahram Farrokhi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Reza Sadeghi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Arsalan Jamshidnia.

Additional information

Handling Editor: Dirk Babendreier.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jamshidnia, A., Abdoli, S., Farrokhi, S. et al. Efficiency of spinosad, Bacillus thuringiensis and Trichogramma brassicae against the tomato leafminer in greenhouse. BioControl 63, 619–627 (2018). https://doi.org/10.1007/s10526-018-9893-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-018-9893-5

Keywords

Search

Navigation