Skip to main content
SpringerLink
Log in

Compatibility of insecticides and Elachertus inunctus Nees (Hymenoptera: Eulophidae) for controlling Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) in greenhouse condition

  • Original Article
  • Published:
Journal of Plant Diseases and Protection Aims and scope Submit manuscript

Abstract

South American Tomato Pinworm (SATP), Tuta absoluta Meyrick (Lepidoptera: Gelechiidae), is one of the most devastating pests in tomato greenhouses. Efficacy of some chemical and biorational insecticides, namely chlorfenapyr, thiocyclam, azadirachtin and Bacillus thuringiensis (Bt), in controlling SATP and their compatibility with Elachertus inunctus, a new SATP larval ectoparasitoid, were studied under greenhouse conditions. For this purpose, larval mortality, leaf and fruit damage and parasitism following the different insecticide treatments and after various days from the treatment (DAT) were recorded and compared to untreated control. Results showed that chlorfenapyr had suitable effects on SATP larvae. Although the experiments indicated that the short-term effects of azadirachtin, thiocyclam and Bt were not detrimental to SATP larvae, but their residual effects were significant in the long term. Among the tested insecticides, Bt was more compatible with E. innunctus release. Overall, the results suggest that the integration application of Bt with early inundate release of E. innunctus can be recommended for suitable and environmentally safe control of SATP in greenhouse tomato.

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

Similar content being viewed by others

References

  • Abou-Fakhr Hammad EM, McAuslane HJ (2010) Effect of Melia azedarach L. extract on Liriomyza sativae (Diptera: Agromyzidae) and its biocontrol agent Diglyphus isaea (Hymenoptera: Eulophidae). J Food Agric Environ 8(34):1247–1252

    Google Scholar 

  • Akol AM, Sithanatham S, Varela AM, Mueke JM, Okelo RO (2001) Evaluation of two neem insecticides for non-target effects on the larval parasitoids of the diamondback moth, Plutella xylostella (L.). In: Proceeding of the 41th international workshop; Melbourne, Australia, November 26–29

  • Arnò 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(4):513–520. https://doi.org/10.1007/s10340-011-0384-z

    Article  Google Scholar 

  • Baniameri V, Cheraghian A (2012) The current status of Tuta absoluta in Iran and initial control strategies. In: EPPO/IOBC/FAO/NEPPO joint international symposium on management of Tuta absoluta (tomato borer). Agadir, Morocco, November 16–18

  • Biondi A, Desneux N, Siscaro G, Zappala 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. https://doi.org/10.1016/j.chemosphere.2011.12.082

    Article  PubMed  CAS  Google Scholar 

  • Biondi A, Mommaerts V, Smagghe G, Viñuela E, Zappalá L, Desneux N (2012b) The non-target impact of spinosyns on beneficial arthropods. Pest Manag Sci 68(12):1523–1536

    Article  PubMed  CAS  Google Scholar 

  • Biondi A, Zappalá L, 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. https://doi.org/10.1371/journal.pone.0076548.eCollection

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Biondi A, Guedes RNC, Wan FH, Desneux N (2018) Ecology, worldwide spread and management of the invasive South American Tomato Pinworm, Tuta absoluta: past, present, and future. Ann Rev Entomol 63:239–258. https://doi.org/10.1146/annurev-ento-031616-034933

    Article  CAS  Google Scholar 

  • Braham M, Hajji L (2012) Management of Tuta absoluta (Lepidoptera, Gelechiidae) with insecticides on tomatoes. In: Perveen F (ed) Insecticides pest engineering. In Tech, Rijeka, pp 333–354

    Google Scholar 

  • Braham M, Glida-Gnidez H, Hajji L (2012) Management of the tomato borer, Tuta absoluta in Tunisia with novel insecticides and plant extracts. OEPP/EPPO Bull 42(2):291–296. https://doi.org/10.1111/epp.2572

    Article  Google Scholar 

  • Brunner JF, Dunley JE, Doerr MD, Beers EH (2001) Effect of pesticides on Coloclypeus florus (Hymenoptera: Eulophidae) and Trichogramma platneri (Hymenoptera: Trichogrammatidae) parasitoids of leafrollers in Washington. J Econ Entomol 94(5):1072–1084. https://doi.org/10.1603/0022-0493-94.5.1075

    Article  Google Scholar 

  • 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 90:787–796. https://doi.org/10.1007/s10340-017-0867-7

    Article  Google Scholar 

  • Chilcutt CF, Tabashnik BE (1999) Effects of Bacillus thuringiensis on adults of Cotesia plutellae (Hymenoptera: Braconidae), a parasitoid of the Diamondback Moth, Plutella xylostella (Lepidoptera: Plutellidae). Biocontrol Sci Technol 9(3):435–440. https://doi.org/10.1080/09583159929695

    Article  Google Scholar 

  • Cloyd R (2005) Compatibility conflict: Is the use of biological control agents with pesticides a viable management strategy? In: Second international symposium on biological control of arthropods; Davos, Switzerland, September 12–16

  • Cloyd R (2005) Compatibility conflict: is the use of biological control agents with pesticides a viable management strategy? In: Second international symposium on biological control of arthropods, Compiler, University of California, Riverside, USA

  • Copping LG, Menn JJ (2000) Biopesticides: a review of their mode of action and efficacy. Pest Manag Sci 56:651–676. https://doi.org/10.1002/1526-4998(200008)56:8<651:AID-PS201>3.0.CO;2-U

  • Croft BA (1990) Arthropod biological control agents and pesticides. Wiley Interscience, New York

    Google Scholar 

  • Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106. https://doi.org/10.1146/annurev.ento.52.110405.091440

    Article  PubMed  CAS  Google Scholar 

  • Desneux N, Wajnberg E, Wyckhuys KAG, Burgio G, Arpaia S, Narvez-Vasquez CA, Gonalez-Cabrera J, Catalan Ruescas D, Frandon TE (2010) Biological invasion of European tomato crops by Tuta absoluta: Ecology, geographic expansion and prospects for biological control. J Pest Sci 83(3):197–215. https://doi.org/10.1007/s10340-010-0321-6

    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 

  • Glare T, Caradus J, Gelerner W, Jackson T, Keyhani N, Kohl J, Marrone P, Morin L, Stewart A (2012) Have biopesticides come of age? Trends Biotech 30(5):250–258. https://doi.org/10.1016/j.tibtech.2012.01.003

    Article  CAS  Google Scholar 

  • Gozalez-Caberera J, Mollá O, Monton H, Urbaneja A (2001) Efficacy of Bacillus thuringiensis (Berliner) in controlling the tomato borer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Biocontrol 56:71–80. https://doi.org/10.1007/s10526-010-9310-1

    Article  Google Scholar 

  • Greenberg SM, Showler AT, Liu TX (2005) Effects of neem-based insecticides on beet armyworm (Lepidoptera: Noctuidae). Insect Sci 12(1):17–23. https://doi.org/10.1111/j.1672-9609.2005.00003.x

    Article  CAS  Google Scholar 

  • Guedes RNC, Picanço MC (2012) The tomato borer Tuta absoluta in South America: pest status, management and insecticide resistance. EPPO Bull 42(2):211–216. https://doi.org/10.1111/epp.2557

    Article  Google Scholar 

  • Guedes RNC, Siqueira HAA (2012) The tomato borer Tuta absoluta: insecticide resistance and control failure. CAB Rev 7(55):1–7

    Article  CAS  Google Scholar 

  • Hamel DR (1977) The effects of Bacillus thuringiensis on parasitoids of the western spruce budworm, Choristoneura occidentals (Lepidoptera: Tortricidae), and the sprouce coneworm, Diorycteia reniculelloids (Lepidoptera: Pyralidae) in montana. Cana Entomol 109(11):1409–1415

    Article  Google Scholar 

  • Haseeb M, Amano H (2002) Effects of contact, oral and persistent toxicity of selected pesticides on Cotesia plutellae (Hym., Braconidae), a potential parasitoid of Plutella xylostella (Lep., Plutellidae). J App Entomol 126(1):8–13. https://doi.org/10.1046/j.1439-0418.2002.00596.x

    Article  CAS  Google Scholar 

  • Haseeb M, Liu TX, Jones WA (2004) Effects of selected insecticides on Cotesia plutellae, endoparasitoid of Plutella xylostella. BioContr 49(1):33–46. https://doi.org/10.1023/B:BICO.0000009377.75941.d7

    Article  CAS  Google Scholar 

  • Haseeb M, Amano H, Liu TX (2005) Effects of selected insecticides on Diadegma semiclausum (Hymenoptera: Ichneumonidae) and Oomyzus sokolowskii (Hymenoptera: Eulophidae), parasitoids of Plutella xylostella (Lepidoptera: Plutellidae). Insect Sci 12(3):163–170. https://doi.org/10.1111/j.1005-295X.2005.00020.x

    Article  CAS  Google Scholar 

  • Ibrahim AM, Kim Y (2008) Transient expression of protein tyrosine phosphatases encoded in Cotesia plutellae bracovirus inhibits insect cellular immune responses. Naturwissenschaften 95(1):25–32. https://doi.org/10.1007/s00114-007-0290-7

    Article  PubMed  CAS  Google Scholar 

  • Isman MB (2015) A renaissance for botanical insecticides? Pest Manag Sci 71(12):1587–1590. https://doi.org/10.1002/ps.4088

    Article  PubMed  CAS  Google Scholar 

  • Kapuge S, McDougall S, Hoffmann AA (2003) Effects of methoxyfenozide, indoxacarb, and other insecticides on the beneficial egg parasitoid Trichogramma nr. brassicae (Hymenoptera:Trichogrammatidae) under laboratory and field conditions. J Econ Entomol 96(4):1083–1090. https://doi.org/10.1603/0022-0493-96.4.1083

    Article  Google Scholar 

  • Kleeberg H (2001) NeemAzal-T/S a botanical product for efficient control of insect pests. In: Soares de Faria R, Kleeberg H (eds) Practice oriented results on use and production of plant extracts and pheromones in integrated and biological pest control. Proc. 2nd workshop “neem and pheromones”. Trifolio-GmbH, Lahnau, pp 28–35

  • Liang GM, Chen W, Liu TX (2003) Effects of three neem-based insecticides on diamondback moth (Lepidoptera: Plutellidae). Crop Protec 22(2):333–340. https://doi.org/10.1016/S0261-2194(02)00175-8

    Article  CAS  Google Scholar 

  • Lietti M, Botto E, Alzogaray RA (2005) Insecticide resistance in Argentine populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotrop Entomol 34:113–119. https://doi.org/10.1590/S1519-566X2005000100016

    Article  Google Scholar 

  • Lowerey DT, Isman MB (1994) Insect growth regulating effects of neem extract and azadirachtin on aphids. Entomol Exp Appl 72:77–84. https://doi.org/10.1111/j.1570-7458.1994.tb01804

    Article  Google Scholar 

  • Luna-Cruz A, Rodriguez-Leyva E, Lomeli-Flores JR, Ortega-Arenas DL, Bautista-Martinez N, Pineda S (2015) Toxicity and residual activity of insecticides against Tamarixia triozae (Hymenoptera: Eulophidae), a parasitoid of Bactericera cockerelli (Hemiptera: Triozidae). J Econ Entomol 108(5):2289–2295. https://doi.org/10.1093/jee/tov206

    Article  PubMed  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 Protec 5(3):331–342. https://doi.org/10.18869/modares.jcp.5.3.331

    Article  Google Scholar 

  • Pedigo LP (2002) Entomology and pest management. Iowa University Press, Iowa City

    Google Scholar 

  • Peralta C, Palma L (2017) Is the insect world overcoming the efficacy of Bacillus thuringiensis? Toxins 9:39. https://doi.org/10.3390/toxins9010039

    Article  PubMed Central  CAS  Google Scholar 

  • Pietrantonio PV, Benedict JH (1999) Effect of new cotton insecticide chemistries, tefenozide, spinosad and chlorfenapyr, on Orius insidiosus and two Cotesia species. Southwest Entomol 24(1):21–29

    CAS  Google Scholar 

  • Raghavendra K, Barik TK, Sharma P, Bhatt RM, Srivastava HC, Sreehari U, Dash AP (2011) Chlorfenapyr: a new insecticide with novel mode of action can control pyrethroid resistant malaria vectors. Malar J 10:16. https://doi.org/10.1186/1475-2875-10-16

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Saad AS, Massoud MA, Abdel-Mageed AA, Hamid NA, Mourad AK, Barakat AS (2007) Abamectin, pymetrozine and azadirachtin sequence as a unique solution to control the leafminer Liriomyza trifolii (Burgess) (Diptera: Agromyzidae) infesting garden beans (Phaseolus vulgaris L.) in Egypt. Commun Agri Appl Biol Sci 72(3):583–593

    CAS  Google Scholar 

  • Sabbour MM, Soleiman N (2012) Evaluations of three Bacillus thuringiensis against Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in Egypt. Int J Sci Res 3(8):2067–2073. https://doi.org/10.13140/RG.2.1.3355.37652015-07-22T15:25:42UTC

    Article  Google Scholar 

  • Sankarganesh E, Firake DM, Sharma B, Verma VK, Behere GT (2017) Invasion of South American Tomato Pinworm, Tuta absoluta, in northeastern India: a new challenge and biosecurity concerns. Entomol Gen 36(4):335–345

    Article  Google Scholar 

  • Santos MS, Zanardi OZ, Pauli KS, Forim MR, Yamamoto PT, Vendramim JD (2015) Toxicity of an azadirachtin-based biopesticide on Diaphorina citri Kuwayama (Hemiptera: Liviidae) and its ectoparasitoid Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae). Crop Protec 74:116–123. https://doi.org/10.1016/j.cropro.2015.04.015

    Article  CAS  Google Scholar 

  • Schauff ME (1985) Taxonomic study of the Nearctic species of Elachertus Spinola (Hymenoptera: Eulophidae). Proc Entomol Soc Wash 87(4):843–858

    Google Scholar 

  • Silvério FO, de Alvarenga ES, Moreno SC, Picanço MC (2009) Synthesis and insecticidal activity of new pyrethroids. Pest Manage Sci 65:900–905. https://doi.org/10.1002/ps.1771

    Article  CAS  Google Scholar 

  • Singh G, Rup PJ, Koul O (2007) Acute, sublethal and combination effects of azadirachtin and Bacillus thuringiensis toxins on Helicoverpa armigera (Lepidoptera: Noctuidae) larvae. Bull Entomol Res 97(4):351–357. https://doi.org/10.1017/S0007485307005019

    Article  PubMed  CAS  Google Scholar 

  • Soleiman MMM, Abdel-Moniem ASH, Abdel-Rahim HA (2013) Impact of some insecticides and their mixtures on the population of tomato borers, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) and Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) in tomato crop at upper Egypt. Arch Phytopathol Plant Protect 47(14):1764–1776. https://doi.org/10.1080/03235408.2013.857226

    Article  CAS  Google Scholar 

  • Stark JD, Vargas R, Banks JE (2007) Incorporating ecologically relevant measures of pesticide effect for estimating the compatibility of pesticides and biocontrol agents. J Econ Entomol 100:1027–1032. https://doi.org/10.1603/0022-0493(2007)100[1027:IERMOP]2.0.CO;2

    Article  PubMed  Google Scholar 

  • Sylla S, Brévault T, Bal AB, Chailleux A, Diatte M, Desneux N, Diarra K (2017) Rapid spread of the tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae), an invasive pest in Sub-Saharan Africa. Entomol Gen 36(3):269–283

    Article  Google Scholar 

  • Urbaneja A, Desneux N, Gabarra R, Arno J, González-Cabrera J, Mafra-Neto A, Pinto ADS, Parra JRP (2013) Biology, ecology and management of the tomato borer, Tuta absoluta. In: Peña JE (ed) Potential invasive pests of agricultural crops. CABI Series, Wallingford, pp 98–125. https://doi.org/10.1079/9781845938291.0098

    Chapter  Google Scholar 

  • Vasconcelos GR (2013) Strain selection and host effect on Trichogramma pretiosum Riley, 1879 (Hymenoptera: Trichogrammatidae) quality for Tuta absoluta (Meyrick, 1917(Lepidoptera: Gelechiidae) control in tomato crops. Dissertation, University of Moura Lacerda, Brazil

  • Wang SS, Guo ZL, Lio YL (2014) Acute toxicities and sublethal effects of some conventional insecticides on Trichogramma chilonis (Hymenoptera: Trichogrammatidae). J Econ Entomol 105(4):1157–1163. https://doi.org/10.1603/EC12042

    Article  CAS  Google Scholar 

  • Wilcox D, Shivakumar B, Melin MF, Miller TA, Benson CW, Shopp D, Casuto GJ, Gundling TJ, Bolling BB, Spear JL (1986) Genetic engineering of bio insecticides. In: Inouye M, Sarma R (eds) Protein engineering: applications in science, medicine, and industry. Academic, Orlando, pp 395–413

    Google Scholar 

  • Xian X, Han P, Wang S, Zhang G, Liu W, Desneux N, Wan F (2017) The potential invasion risk and preventive measures against the tomato leafminer Tuta absoluta in China. Entomol Gen 36(4):319–333

    Article  Google Scholar 

  • Yankova V (2012) Damage caused by tomato leaf miner (Tuta absoluta Meyrick) in tomato varieties grown in greenhouse. Plant Sci 49:92–97

    Google Scholar 

  • Yankova V, Valchev N, Markova D (2014) Effectiveness of phytopesticide Neem Azal T/S against tomato leaf miner (Tuta absoluta Meyrick) in greenhouse tomato. Bulg J Agric Sci 20:1116–1118

    Google Scholar 

  • Yarahmadi F, Salehi Z, Lotfalizadeh H (2016) Two species of the genus Elachertus Spinola (Hym.: Eulophidae) new larval ectoparasitoids of Tuta absoluta (Meyreck) (Lep.: Gelechidae). J Crop Protect 5(3):413–418

    Article  Google Scholar 

  • Yee WL, Toscano NC (2014) Laboratory evaluations of synthetic and natural insecticides on beet armyworm (Lepidoptera: Noctuidae) damage and survival on lettuce. J Econ Entomol 91(1):56–63. https://doi.org/10.1093/jee/91.1.56

    Article  Google Scholar 

  • Zabel A, Manojlovic B, Rajkovic S, Stankovic S, Kostic M (2002) Effect of Neem extract on Lymantria dispar L. (Lepidoptera: Lymantriidae) and Leptinotarsa decemlineata Say. (Coleoptera: Chrysomelidae). J Pest Sci 75(1):19–25. https://doi.org/10.1046/j.1439-0280.2002.02006.x

    Article  Google Scholar 

  • Zappalà L, Bernardo U, Biondi A, Cocco A, Deliperi S, Delrio G, Giorgini M, Pedata P, Rapisarda C, Garzia GT, Siscaro G (2012) Recruitment of native parasitoids by the exotic pest Tuta absoluta in Southern Italy. Bull Insectology 65(1):51–61

    Google Scholar 

Download references

Acknowledgements

This research was supported by research deputy of Khuzestan Agricultural Sciences and Natural Resources University [Grant Number 941/09].

Author information

Authors and Affiliations

  1. Department of Plant Protection, Faculty of Agriculture, Khuzestan Agricultural Sciences and Natural Resources University, Ahvaz (Mollasani), Iran

    Fatemeh Yarahmadi & Zohreh Salehi

  2. Department of Plant Protection, East-Azarbaijan Research Center for Agriculture and Natural Resources, Tabriz, Iran

    Hossein Lotfalizadeh

Authors
  1. Fatemeh Yarahmadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zohreh Salehi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hossein Lotfalizadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fatemeh Yarahmadi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yarahmadi, F., Salehi, Z. & Lotfalizadeh, H. Compatibility of insecticides and Elachertus inunctus Nees (Hymenoptera: Eulophidae) for controlling Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) in greenhouse condition. J Plant Dis Prot 125, 357–364 (2018). https://doi.org/10.1007/s41348-018-0164-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s41348-018-0164-6

Keywords

Search

Navigation