Skip to main content
SpringerLink
Log in

Life-stage-dependent side effects of selected insecticides on Trichogramma cacoeciae (Marchal) (hymenoptera: Trichogrammatidae) under laboratory conditions

  • Published:
Phytoparasitica Aims and scope Submit manuscript

Abstract

Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) is classified as one of the most harmful pest of tomato crops. Many species of predators and parasitoids including Trichogramma cacoeciae (Marchal) (Hymenoptera: Trichogrammatidae) are noted as potential candidates used for biological control of this pest. Therefore, the use of selective insecticides is critical to conserve and protect natural enemies in the field. This study assessed the side effects of insecticides on different development stages of T. cacoeciae under laboratory conditions. For this, eleven pesticides such as: Indoxacarb, spiromesifen, cyromazin, chlorfenapyr, cypermethrin, diafenthiuron, chlorantraniliprole, spinosad, azadirachtin, Bacillus thuringiensis (Bt) and virus HaNPV were tested. This study shows that indoxacarb, spiromesifen, chlorfenapyr, cypermethrin, diafenthiuron and spinosad had a negative effect on immature stages of Trichogramma. All insecticides residues on tomato leaves were found to be toxic to Trichogramma adults except azadirachtin, Bt and virus HaNPV. Therefore, the use of the tested natural products (azadirachtin, Bt and HaNPV) at the recommended doses is viable, having no negative impact on T. cacoeciae in tomato crops.

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

  • Abbes, K., Biondi, A., Zappala’, L., & Chermiti, B. (2014). Fortuitous parasitoids of the invasive tomato leafminer Tuta absoluta in Tunisia. Phytoparasitica, 42, 85–92.

    Article  Google Scholar 

  • Abreu Costa, M., Moscardini, V. F., da Costa Gontijo, P., Carvalho, G. A., de Oliveira, R. L., & de Oliveira, H. N. (2014). Sublethal and transgenerational effects of insecticides in developing Trichogramma galloi (hymenoptera: Trichogrammatidae). Ecotoxicology. https://doi.org/10.1007/s10646-014-1282-y

  • AVFA (2012) Tunisian Ministry of Agriculture (http://avfa.agrinet.tn/upload/manifestation/liste%20des%20produits%20pesticides%20homologu%C3%A9s.docx). Cited 19 July 2012.

  • Bai, B., Luck, R. F., Forster, L., Stephens, B., & Janssen, J. A. M. (1992). The effect of host size on quality attributes of the egg parasitoid, Trichogramma pretiosum. Journal of Entomologia Experimentalis and Applicata, 64, 37–48.

    Article  Google Scholar 

  • Biondi, A., Zappalà, L., Di Mauro, A., Tropea Garzia, G., Russo, A., Desneux, N., & Siscaro, G. (2016). Can alternative host plant and prey affect phytophagy and biological control by the zoophytophagous mirid Nesidiocoris tenuis? BioControl, 61, 79–90. https://doi.org/10.1007/s10526-015-9700-5

    Article  Google Scholar 

  • Blibech, I., Chaieb, I., & Ksantini, M. (2011). Quality assessment of local Trichogramma species (hymenoptera, Trichogrammatidae) to control the olive moth Prays oleae Bern. (Lepidoptera, Yponomeutidae). Journal of Environmental Entomology, 33(4), 429–435.

    Google Scholar 

  • Boller, E.F., Vogt, H., Ternes, P., & Malavolta, C. (2005). Working document on selectivity of pesticides. IOBC/wprs, 1-9. Available in http://www.iobc-wprs.org/ip_ipm/03021_IOBC_WorkingDocumentPesticides_Explanations.pdf.

  • Braga Maia, J., Andrade Carvalho, G., De Oliveira, R.L., Lasmar, O. and Santo Leite, M.I. (2013). Effects of insecticides used in corn on immature stages of Trichogramma atopovirilia (Hymenoptera: Trichogrammatidae). Revista Colombiana de Entomologia, 39(2), 2015–210.

  • Brar, K. S., Varma, G. C., & Shenhmar, M. (1991). Effect of insecticides on Trichogramma chilonis Ishii (hymenoptera: Trichogrammatidae), an egg parasitoid of sugarcane borers and cotton bollworms. Journal of Entomon, 16, 43–48.

    CAS  Google Scholar 

  • Brust G. & IPM Vegetable Specialist. (2008). Insect Pests of Tomato. Maryland Cooperative Extension, University of Maryland.13p.

  • Bull, D. L., & Coleman, R. J. (1985). Effects of pesticides on Trichogramma spp. Journal of Southwestern Entomologists, 8, 156–168.

    CAS  Google Scholar 

  • Bull, D. L., & House, V. S. (1983). Effects of different insecticides on parasitism of host eggs by Trichogramma pretiosum Riley. Journal of Southwestern Entomologists, 8, 46–53.

    CAS  Google Scholar 

  • Campos, M. R., Silva, T. B. M., Silva, W. M., Silva, J. E., & Siqueira, H. A. A. (2015). Spinosyn resistance in the tomato borer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Journal of Pest Science, 88, 405–412.

    Article  Google Scholar 

  • Caparros Megido, R., Haubruge, E., & Verheggen, F. J. (2012). First evidence of deuterotokous parthenogenesis in the tomato leafminer, Tuta absoluta (Meyrick) (Lep., Gelechiidae). Journal of Pest Science, 85(4), 409–412.

    Article  Google Scholar 

  • Carvalho, G. A., Reis, P. R., Rocha, L. C. D., Moraes, J. C., Fuini, L. C., & Ecole, C. C. (2003). Side-effects of insecticides used in tomato fields on Trichogramma pretiosum (hymenoptera, Trichogrammatidae). Maringá, 25(2), 275–279.

    CAS  Google Scholar 

  • Carvalho, G. A., Godoy, M. S., Parreira, D. S., & Rezende, D. T. (2010). Effect of chemical insecticides used in tomato crops on immature Trichogramma pretiosum (hymenoptera: Trichogrammatidae). Revista Colombiana de Entomología, 36(1), 10–15.

    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. Journal of Economic Entomology, 106(6), 2310–2321.

    Article  PubMed  Google Scholar 

  • Chen, X., Song, M., Qi, S., & Wang, C. (2013). Safety evaluation of eleven insecticides to Trichogramma nubilale (hymenoptera: Trichogrammatidae). Journal of Economic Entomology, 106(1), 136–141.

    Article  CAS  PubMed  Google Scholar 

  • Cherif, A., & Lebdi-Grissa, K. (2013). Trichogramma cacoeciae as a biological control agent of the tomato pinworm Tuta absoluta in northeastern Tunisia. Entomologia Hellenica, 22, 35–42.

    Article  Google Scholar 

  • Cherif, A., & Lebdi-Grissa, K. (2014). Control of the tomato leafminer Tuta absoluta (Lepidoptera; Gelechiidae) using the mass trapping tool in tomato open field plot and greenhouses in Tunisia. Agricultural Science Research Journal, 4(10), 161–173.

    Google Scholar 

  • Cherif, A., & Lebdi-Grissa, K. (2015). Control of the cotton bollworm Helicoverpa armigera in Tunisian tomato open field plots by the application of some insecticides. Tunisian Journal of Plant Protection, 10, 45–54.

    Google Scholar 

  • Chermiti, B., & Abbes, K. (2012). Comparison of pheromone lures used in mass trapping to control the tomato leafminer Tuta absoluta (Meyrick, 1917) in industrial tomato crops in Kairouan (Tunisia). Bulletin OEPP/EPPO Bulletin, 42(2), 241–248.

    Article  Google Scholar 

  • Cocco, A., Deliperi, S., & Delrio, G. (2012). Potential of mass trapping for Tuta absoluta management in greenhouse tomato crops using light and pheromone traps. IOBCWPRS Bulletin, 80, 319–324.

    Google Scholar 

  • Cocco, A., Deliperi, S., & Delrio, G. (2013). Control of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in greenhouse tomato crops using the mating disruption technique. Journal of Applied Entomology, 137, 16–28.

    Article  CAS  Google Scholar 

  • Cônsoli, F. L., Parra, J. R. P., & Hassan, S. A. (1998). Side effects of insecticides used in tomato fields on the egg parasitoid Trichogramma pretiosum Riley (Hym., Trichogrammatidae), a natural enemy of Tuta absoluta (Meyrick) (Lep., Gelechiidae). Journal of Applied Entomology, 122, 43–47.

    Article  Google Scholar 

  • Cônsoli, F. L., Botelho, P. S. M., & Parra, J. R. P. (2001). Selectivity of insecticides to the egg parasitoid Trichogramma galloi Zucchi, 1988, (Hym., Trichogrammatidae). Journal of Applied Entomology, 125, 37–43.

    Article  Google Scholar 

  • Da Silva, D. M., & Bueno, A. D. F. (2015). Organic products selectivity for Trichogramma pretiosum (hymenoptera: Trichogrammatidae). Arquivos do Instituto Biologico, 82, 1–8.

    Google Scholar 

  • Desneux, N., Wajnberg, E., Wyckhuys, K., Burgio, G., Arpaia, S., Narváez-Vasquez, C., 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. Journal of Pest Science, 83, 197–215.

    Article  Google Scholar 

  • El-Wakeil, N. E., & Vidal, S. (2005). Using of Chrysoperla carnea in combination with Trichogramma species for controlling Helicoverpa armigera. Egyptian Journal of Agriculture Research, 83, 891–905.

    Google Scholar 

  • El-Wakeil, N. E., Gaafar, N., & Vidal, S. (2006). Side effect of some neem products on natural enemies of Helicoverpa Trichogramma spp. and Chrysoperla carnea. Archives of Phytopathology and Plant Protection, 39, 445–455.

    Article  Google Scholar 

  • Fernandes, O.D. (2003). Efeito do milho geneticamente modificado (MON810) em Spodoptera frugiperda (Smith, J.E., 1797) e no parasitoide de ovos Trichogramma spp. Thesis (Doctor in Science/Entomology) - Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, Piracicaba, Estado de São Paulo - Brazil. 182 p.

  • Gassen, D. (1996). Manejo de pragas associadas à cultura do milho. Passo Fundo: Aldeia Norte. 127 p.

  • GIL (2016). Available from internet (http://www.gil.com.tn/fr/).

  • Gomes, S. M., & Parra, J. R. P. (1998). The parasitization as a tool for factitious host selection for Trichogramma galloi Zucchi and T. pretiosum Riley. Mitteilungen aus der Biologischen Bundesanstalt für Landund Forstwirtschaft, Heft, 356, 13–23.

    Google Scholar 

  • Gomez, K. A., & Gomez, A. A. (1984). Statistical procedures for agricultural research (2nd ed.). New York: Wiley.

    Google Scholar 

  • Guedes, R. N. C., Lima, J. O. G., & Zanuncio, J. C. (1992). Seletividade dos inseticidas deltametrina, fenvalerato e fenitrotiom para Podisus connexivus (Heteroptera: Pentatomidae). Anais da Sociedade Entomológica do Brasil, 21(3), 339–346.

    CAS  Google Scholar 

  • Haddi, K., Berger, M., Bielza, P., Cifuentes, D., Field, L. M., Gorman, K., Rapisarda, C., Williamson, M. S., & Bass, C. (2012). Identification of mutations associated with pyrethroid resistance in the voltage-gated sodium channel of the tomato leaf miner (Tuta absoluta). Insect Biochemistry and Molecular Biology, 42, 506–513.

    Article  CAS  PubMed  Google Scholar 

  • Hassan, S. A. (1998). Guidelines for the evaluation of side effects of plant protection products on Trichogramma cacoeciae Marchal (Hym., Trichogrammatida). IOBC/WPRS Bulletin, 21, 119–128.

    Google Scholar 

  • Hassan, S. A., & Abdellgader, H. (2001). A sequential testing program to assess the side effects of pesticides on Trichogramma cacoeciae Marchal (hymenoptera: Trichogrammatidae). IOBC/WPRS Bulletin, 24(4), 71–81.

    Google Scholar 

  • Hewa-Kapuge, S., Mcdougall, S., & Hoffmann, A. A. (2003). Effects of Methoxyfenozide, Indoxacarb, and other insecticides on the beneficial egg parasitoid Trichogramma Nr. brassicae (hymenoptera: Trichogrammatidae) under laboratory and field conditions. Biological and Microbial Control, 96(4), 1083–1090.

    CAS  Google Scholar 

  • Hoffmann, E. J., Middleton, S. M., & Wise, J. C. (2008). Ovicidal activity of organophosphate, oxadiazine, neonicotinoid and insect growth regulator chemistries on northern strain plum curculio, Conotrachelus nenuphar. Journal of Insect Science, 8, 1–6.

    Article  Google Scholar 

  • Hussain, D., Ali, A., Ul-Hassan, M. M., Ali, S., Saleem, M., & Nadeem, S. (2012). Evaluation of toxicity of some new insecticides against egg parasitoid Trichogramma chilonis (Ishii) (hymenoptera: Trichogrammitidae). Pakistan Journal of Zoology, 44(4), 1123–1127.

    CAS  Google Scholar 

  • Jader-Braga, M., Andrade-Carvalho, G., De-Oliveira, R. L., Lasmar, O., & Santos-Leite, M. I. (2013). Effects of insecticides used in corn on immature stages of Trichogramma atopovirilia (hymenoptera: Trichogrammatidae). Revista Colombiana de Entomología, 39(2), 205–210.

    Google Scholar 

  • James, D. G. (2002). Selectivity of the acaricide, bifenazate, and aphicide, pymetrozine, to spider mite predators in Washington hops. International Journal of Acarology, 28, 175–179.

    Article  Google Scholar 

  • Khan, M. A., Khan, H., & Farid, A. (2014a). Assessment of the lethal and parasitism effects of Heicoverpa armigera Nucleopolyhedrovirus (HaNPV) on Trichogramma chilonis (Ishii) (hymenoptera: Trichogrammatidae). Sarhad Journal of Agriculture, 30(4), 425–432.

    Google Scholar 

  • Khan, M. A., Khan, H., Farid, A., & Ali, A. (2014b). Evaluation of toxicity of some novel pesticides to parasitism by Trichogramma Chilonis (hymenoptera: Trichogrammatidae). Journal of Agriculture Research, 53(1), 63–73.

    Google Scholar 

  • Knutson, A. (1998). The Trichogramma manual. In Texas agriculture extension service, Texas a & M University system. College Station: Texas.

    Google Scholar 

  • Kölliker-Ott, U. M., Blows, M. W., & Hoffmann, A. A. (2003). Are wing size, wing shape and asymmetry related to the field fitness of Trichogramma egg parasitoids? Oikos, 100, 563–573.

    Article  Google Scholar 

  • Ksentini, I., Jardak, T., & Zeghal, N. (2010). Bacillus thuringiensis, deltamethrin and spinosad side-effects on three Trichogramma species. Bulletin of Insectology, 63(1), 31–37.

    Google Scholar 

  • Ksentini, I., Herz, A., Ksantini, M., Jardak, T., & Hassan, S. A. (2011). Temperature and strain effects on reproduction and survival of Trichogramma oleae and Trichogramma cacoeciae (hymenoptera: Trichogrammatidae). Biocontrol Science and Technology, 21(8), 903–916.

    Article  Google Scholar 

  • Li, K. H., Xu, X., Li, Y. F., Meng, Q. Z., & Zhou, L. C. (1986). Determination of toxicity of 29 chemicals to Trichogramma japonicum at various developmental stages. Journal of Natural Enemies of Insects, 8, 187–194.

    Google Scholar 

  • Lietti, M. M. M., Botto, E., & Alzogara, R. (2005). Insecticide resistance in argentine populations of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Neotropical Entomology, 34, 113–119.

    Article  Google Scholar 

  • Moreno, S. C., Carvalho, G. A., Picanço, M. C., Morais, E. G., & Pereira, R. M. (2012). Bioactivity of compounds from Acmellaoleracea against Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) and selectivity to two non-target species. Pest Management Science, 68, 386–393.

    Article  CAS  PubMed  Google Scholar 

  • Moura, A. P., Carvalho, G. A., & de -Oliveira Rigitano, R. L. (2005). Toxicity of insecticides used in tomato crop to Trichogramma pretiosum. Pesquisa Agropecuaria. Brasíliera, 40(3), 203–210.

    Google Scholar 

  • Naselli, M., Zappalà, L., Gugliuzzo, A., Tropea Garzia, G., Biondi, A., Rapisarda, C., Cincotta, F., Condurso, C., Verzera, A., & Siscaro, G. (2016). Olfactory response of the zoophytophagous mirid Nesidiocoris tenuis to tomato and alternative host plants. Arthropod-Plant Interactions. https://doi.org/10.1007/s11829-016-9481-5

  • Navarajan Paul, A. V., & Agarwal, R. A. (1989). Persistent toxicity of some insecticides to the egg parasitoid, Trichogramma brasiliensis Ashmead. Indian Journal of Entomology, 51, 273–277.

    Google Scholar 

  • Pavlik, J. (1993). Variability in the host acceptance of European corn borer, Ostrinia nubilalis Hb. (Lep., Pyralidae) in strains of the egg parasitoid Trichogramma spp. (Hym., Trichogrammatidae). Journal of Applied Entomology, 115, 77–84.

    Article  Google Scholar 

  • Plewka, T., Kot, J., & Krukierek, T. (1975). Effect of insecticides on the longevity and fecundity of Trichogramma evanescens (hymenoptera: Trichogrammatidae). Polish Journal of Ecological Studies, 1, 197–210.

    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. Journal of Pest Science, 88(1), 9–16.

    Article  Google Scholar 

  • Santini, A. (2001). Tomate. Manejo de pragas e doenças. Correio Agrícola, 2(1), 8–11.

    Google Scholar 

  • Sechser, B., Reber, B., & Bourgeois, F. (2002). Pymetrozine: Selectivity spectrum to beneficial arthropods and fitness for integrated pest management. Journal of Pest Science, 75, 72–77.

    Google Scholar 

  • Singh, P. P., & Varma, G. C. (1986). Comparative toxicities of some insecticides to Chrysoperla carnea (Chrysopidae: Neuroptera) and Trichogramma brasiliensis (Trichogrammatidae: Hymenoptera), two arthropod natural enemies of cotton pests. Journal of Agriculture, Ecosystems and Environment, 15, 23–30.

    Article  CAS  Google Scholar 

  • Smilanick, J. M., Zalom, F. G., & Ehler, L. E. (1996). Effect of metamidophos residue on the pentatomid egg parasitoids Trissolcus basalis & T. utahensis. Biolgical Control, 6, 193–201.

    Article  Google Scholar 

  • SPSS (2012). SPSS 21.0 brief guide. SPSS incorporation, Chicago.

  • Sterk, G., Hassan, S. A., Baillod, M., Bakker, F., Bigler, F., Blumel, S., Bogenschutz, H., Boller, E., Bromand, B., Brun, J., et al. (1999). Results of the seventh joint pesticide testing programme carried out by the IOBC/ WPRSWorking group “pesticides and beneficial organisms”. BioControl, 44, 99–117.

    Article  CAS  Google Scholar 

  • Stock, D., & Holloway, P. J. (1993). Possible mechanisms for surfactant induced foliar uptake of agrochemicals. Journal of Pest Science, 38, 165–177.

    Article  CAS  Google Scholar 

  • Suh, C. P. C., Orr, D. B., & Van Duyn, J. W. (2000). Effect of insecticides on Trichogramma exiguum (Trichogrammatidae: Hymenoptera): Preimaginal development and adult survival. Journal of Economic Entomology, 93(3), 577–583.

    Article  CAS  PubMed  Google Scholar 

  • Volkmar, C., Schumacher, K., & Müller, J. (2008). Impact of low-input pesticides usage on spider communities with special regards to accumulated effects. Pesticides and Beneficial Organisms IOBC/ Wprs Bulletin, 35, 18–25.

    Google Scholar 

  • Youssef, A. I., Nasr, F. N., Stefanos, S. S., Elkhair, S. S. A., Shehata, W. A., Agamy, E., Herz, A., & Hassan, S. A. (2004). The side-effects of plant protection products used in olive cultivation on the hymenopterous egg parasitoid Trichogramma cacoeciae Marchal. Journal of Applied Entomology, 128, 593–599.

    Article  CAS  Google Scholar 

  • Zouba, A., Chermiti, B., Chraiet, R., & Mahjoubi, K. (2013). Effect of two indigenous Trichogramma species on the infestation level by tomato miner Tuta absoluta in tomato greenhouses in the south-west of Tunisia. Tunisian Journal of Plant Protection, 8, 87–106.

    Google Scholar 

Download references

Acknowledgements

We are grateful to Sonia Jendoubi (Laboratory of Entomology-Acarology, National Agronomic Institute of Tunisia) and Zaâra Guannouni (Laboratory of Entomology-Acarology, National Agronomic Institute of Tunisia) for their technical assistance in the laboratory.

Author information

Authors and Affiliations

  1. Department of Plant Protection and Post-harvest Diseases, Laboratory of Entomology-Acarology, National Agronomic Institute of Tunisia, 43 avenue Charles Nicolle, Cité Mahrajène, 1082, Tunis, Tunisia

    Cherif Asma, Ichaoui Ons, Barhoumi-Attia Sabrine & Lebdi-Grissa Kaouthar

Authors
  1. Cherif Asma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ichaoui Ons
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Barhoumi-Attia Sabrine
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lebdi-Grissa Kaouthar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cherif Asma.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Asma, C., Ons, I., Sabrine, BA. et al. Life-stage-dependent side effects of selected insecticides on Trichogramma cacoeciae (Marchal) (hymenoptera: Trichogrammatidae) under laboratory conditions. Phytoparasitica 46, 105–113 (2018). https://doi.org/10.1007/s12600-018-0638-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12600-018-0638-x

Keywords

Search

Navigation