Toxicity of soybean-registered agrochemicals to Telenomus podisi and Trissolcus basalis immature stages

  • Ronaldo Zantedeschi
  • Matheus Rakes
  • Rafael Antonio Pasini
  • Mikael Bolke Araújo
  • Flávio Amaral Bueno
  • Anderson Dionei Grützmacher
Article
  • 21 Downloads

Abstract

Biological control of phytophagous bugs in soybean crops is efficiently performed by egg parasitoids, such as Telenomus podisi and Trissolcus basalis. Based on this, the use of agrochemicals in these crops must be managed consciously, making use of pesticides that are selective to the egg of these parasitoids, in order to ensure a balanced ecosystem. The aim of this study was to assess the selectivity of 15 registered pesticides to the immature stages (pre and post-parasitism) of T. podisi and T. basalis, following the method proposed by the “International Organization for Biological and Integrated Control” (IOBC). Pesticides were classified as class 1 – harmless (RP < 30%); class 2 – slightly harmful (30% ≤ RP ≤ 79%); class 3 – moderately harmful (80% ≤ RP ≤ 99%); and class 4 – harmful (RP > 99%). During pre-parasitism, the insecticides imidacloprid+beta-cyfluthrin, deltamethrin, lambda-cyhalothrin+thiamethoxam, acephate, and fenitrothion reduced parasitism of both parasitoids. The others: flubendiamide, diflubenzuron, Bacillus thuringiensis, lufenuron, and the herbicide isopropylamine were selective, i.e. harmless (class 1), to both parasitoids, except for pyraclostrobin+metconazole, which significantly reduced T. basalis parasitism, being considered slightly harmful (class 2). In post parasitism, all the aforementioned pesticides were harmless to T. podisi and T. basalis. Moreover, in pre-parasitism, T. basalis was found to be more sensitive to the tested pesticides when compared to T. podisi. Still, more studies must be conducted to provide a better understanding of the impact of agrochemicals on these parasitoid species in semi-field conditions.

Keywords

Glycine max Biological control Chemical control Integrated management of pests Natural enemies 

Notes

Acknowledgments

The authors would like to thank CAPES (Coordination for the Improvement of Higher Education Personnel) and CNPq (Brazilian National Council for Scientific and Technological Development).

Compliance with ethical standards

Conflict of interests

The authors declare the lack of conflict of interests in the present study.

References

  1. AGROFIT. (2016). Sistema de agrotóxicos fitossanitários. Available at: <http://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons>. Accessed 14 Jun 2016.
  2. Alencar, J. R. D. C. C., Polanczyk, R. A., Fraga, D. F., Funichello, M., De Bortoli, S. A., Viana, M. A., Vacari, A. M., & Agostini, T. T. (2011). Seletividade de Bacillus thuringiensis para Telenomus remus no manejo de Spodoptera frugiperda. Horticultura Brasileira, 29, 552–558.Google Scholar
  3. Bacci, L., Picanço, M. C., Barros, E. C., Rosado, J. F., Silva, G. A., Silva, V. F., & Silva, N. R. (2009). Physiological selectivity of insecticides to wasps (Hymenoptera: Vespidae) preying on the diamondback moth. Sociobiology, 53, 151–167.Google Scholar
  4. Bayram, A., Salerno, G., Onofri, A., & Conti, E. (2010). Sub-lethal effects of two pyrethroids on biological parameters and behavioral responses to host cues in the egg parasitoid Telenomus busseolae. Biological Control, 53, 153–160.  https://doi.org/10.1016/j.biocontrol.2009.09.012.CrossRefGoogle Scholar
  5. Brunner, J. F., Dunley, J. E., Doerr, M. D., & Beers, E. H. (2001). Effect of pesticides on Colpoclypeus florus (Walker) (Hymenoptera: Eulophidae) and Trichogramma platneri, potential parasitoids of leafrollers in Washington. Journal of Economic Entomology, 94, 1075–1084.CrossRefPubMedGoogle Scholar
  6. Bueno, A. F., Bueno, R. C. O. F., Parra, J. R. P., & Vieira, S. S. (2008). Effects of pesticides used in soybean crops to the egg parasitoid Trichogramma pretiosum. Ciência Rural, 38, 1495–1503.  https://doi.org/10.1590/S0103-84782008000600001.CrossRefGoogle Scholar
  7. Bueno, R. C. O. F., Carneiro, T. R., Bueno, A. F., Pratissoli, D., Fernandes, O. A., & Vieira, S. S. (2010). Parasitism capacity of Telenomus remus Nixon (Hymenoptera: Scelionidae) on Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae) eggs. Brazilian Archives of Biology and Technology.  https://doi.org/10.1590/S1516-89132010000100017.
  8. Carmo, E. L., Bueno, A. F., Bueno, R. C. O. F., Vieira, S. S., Gobbi, A. L., & Vasco, F. R. (2009). Seletividade de diferentes agrotóxicos usados na cultura da soja ao parasitoide de ovos Telenomus remus. Ciência Rural.  https://doi.org/10.1590/S0103-84782009005000188.
  9. Carmo, E. L., Bueno, A. F., & Bueno, R. C. O. F. (2010a). Pesticide selectivity for the insect egg parasitoid Telenomus remus. Biological Control.  https://doi.org/10.1590/S0103-84782009005000188.
  10. Carmo, E. L., Bueno, A. F., Bueno, R. C. O. F., Vieira, S. S., Goulart, M. M. P., & Carneiro, T. R. (2010b). Seletividade de produtos fitossanitários utilizados na cultura da soja para pupas de Trichogramma pretiosum Riley, 1879 (Hymenoptera: Trichogrammatidae). Arquivos do Instituto Biológico, 77, 283–290.Google Scholar
  11. Carneiro, T. R., Fernandes, O. A., Cruz, I., & Bueno, R. C. O. F. (2010). Functional response of Telenomus remus Nixon (Hymenoptera, Scelionidae) to Spodoptera frugiperda (J. E. Smith) (Lepidoptera, Noctuidae) eggs: effect of female age. Revista Brasileira de Entomologia.  https://doi.org/10.1590/S0085-56262010000400023.
  12. Carvalho, G. A., Parra, J. R. P., & Baptista, G. C. (2001). Seletividade de alguns produtos fitossanitários a duas linhagens de Trichogramma pretiosum Riley, 1879 (Hymenoptera: Trichogrammatidae). Ciência e Agrotecnolgia, 25, 583–591.Google Scholar
  13. Carvalho, G. A., Parra, J. R. P., & Baptista, G. C. (2003). Bioatividade de produtos fitossanitários utilizados na cultura do tomateiro (Lycopersicon esculentum Mill.) a Trichogramma pretiosum Riley, 1879 (Hymenoptera: Trichogrammatidae) nas gerações F1 e F2. Ciência e Agrotecnolgia, 27, 261–270.CrossRefGoogle Scholar
  14. Castilhos, R. V., Grützmacher, A. D., Siqueira, P. R. B., Moraes, I. L., & Gauer, C. J. (2014). Seletividade de agrotóxicos utilizados em pessegueiro sobre ovos e pupas do predador Chrysoperla externa. Ciência Rural.  https://doi.org/10.1590/0103-8478cr20140248.
  15. Cordero, R. J., Bloomquist, J. R., & Kuhar, T. P. (2007). Susceptibility of two diamondback moth parasitoids, Diadegma insulare (Cresson) (Hymenoptera: Ichneumonidae) and Oomyzus sokolowskii (Kurdjumov) (Hymenoptera: Eulophidae), to selected commercial insecticides. Biological Control.  https://doi.org/10.1016/j.biocontrol.2007.04.005.
  16. Fernández, M. M., Medina, P., Fereres, A., Smagghe, G., & Viñuela, E. (2015). Are mummies and adults of Eretmocerus mundus (Hymenoptera: Aphelinidae) compatible with modern insecticides? Journal of Economic Entomology, 108, 2268–2277.  https://doi.org/10.1093/jee/tov181.CrossRefGoogle Scholar
  17. Freitas, R. M. F., Lima, L. E., Silva, R. S., Campos, H. D., & Perin, A. (2016). Fluxapyroxad in the Asian soybean rust control in the Cerrado biome. Revista Caatinga.  https://doi.org/10.1590/1983-21252016v29n312rc.
  18. Giolo, F. P., Grützmacher, A. D., Manzoni, C. G., Härter, W. R., Müller, C., & Castilhos, R. V. (2006). Toxicidade de pesticidas utilizados na cultura do pessegueiro para estágios imaturos de Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae). BioAssay.  https://doi.org/10.14295/BA.v1.0.35.
  19. Giolo, F. P., Grützmacher, A. D., Manzoni, C. G., Härter, W. R., Castilhos, R. V., & Müller, C. (2007). Toxicidade de agrotóxicos utilizados na cultura do pessegueiro sobre o parasitóide de ovos Trichogramma atopovirilia Oatman & Platner, 1983 (Hymenoptera: Trichogrammatidae). Ciência Rural, 37, 308–314.CrossRefGoogle Scholar
  20. Graff, J. F. (1993). The role of insect growth regulators in arthropod control. Parasitology Today.  https://doi.org/10.1016/0169-4758(93)90106-P.
  21. Hassan, S. A. (1998). Guideline for the evaluation of side effects of plant protection products on Trichogramma cacoeciae Marchal (Hym.: Trichogrammatidae). IOBC/WPRS Bulletin., 21, 119–128.Google Scholar
  22. Hassan, S. A., Halsall, N., Gray, A. P., Kuehner, C., Moll, M., Bakker, F. M., et al. (2000). A laboratory method to evaluate the side effects of plant protection products on Trichogramma cacoeciae Marchal (Hymenoptera: Trichogrammatidae). In M.P. Candolfi, S. Blümel, R. Forster, F.M. Bakker, C. Grimm, S.A. Hassan, U. Heimbach, M.A. Mead-Briggs, B. Reber, R. Schmuck, & Vogt, H. (eds), Guidelines to evaluate side-effects of plant protection products to non-target arthropods (pp. 107–119). Reinheim: IOBC/WPRS.Google Scholar
  23. Leite, G. L. D., Picanço, M., Guedes, R. N. C., & Gusmão, M. R. (1998). Selectivity of insecticides with and without mineral oil to Brachygastra lecheguana (Hymenoptera: Vespidae), a predator of Tuta absoluta (Lepidoptera: Gelechiidae). Ceiba, 39, 191–194.Google Scholar
  24. Magano, D. A., Grützmacher, A. D., De Armas, F. S., Paulus, L. F., Panozzo, L. E., Mentnech, K. J., & Zotti, M. J. (2015). Evaluating the selectivity of registered fungicides for soybean against Trichogramma pretiosum Riley, 1879 (Hymenoptera: Trichogrammatidae). African Journal of Agricultural Research, 10, 3825–3831.  https://doi.org/10.5897/AJAR2014.9083.CrossRefGoogle Scholar
  25. Manzoni, C. G., Grützmacher, A. D., Giolo, F. P., Härter, W. R., Castilhos, R. V., & Paschoal, M. (2007). Seletividade de agroquímicos utilizados na produção integrada de maçã aos parasitóides Trichogramma pretiosum Riley e Trichogramma atopovirilia Oatman & Platner (Hymenoptera: Trichogrammatidae). BioAssay.  https://doi.org/10.14295/BA.v2.0.50.
  26. Morais, M. R., Zanardi, O. Z., Rugno, G. R., & Yamamoto, P. T. (2016). Impact of five insecticides used to control citrus pests on the parasitoid Ageniaspis citricola Longvinovskaya (Hymenoptera: Encyrtidae). Ecotoxicology, 25, 1011–1020.  https://doi.org/10.1007/s10646-016-1658-2.CrossRefPubMedGoogle Scholar
  27. Moura, A. P., & Rocha, L. C. D. (2006). Seletivos e eficientes. Cultivar Hortaliças e Frutas, 6, 6–8.Google Scholar
  28. Oliveira, H. N., Antigo, M. R., Carvalho, G. A., Glaeser, D. F., & Pereira, F. F. (2013). Selectivity of inseticides used in the sugar-cane on adults of Trichogramma galloi Zucchi (Hymenoptera: Trichogrammatidae). Bioscience Journal, 29, 1267–1274.Google Scholar
  29. Pacheco, D. J. P., & Corrêa-Ferreira, B. S. (2000). Parasitismo de Telenomus podisi Ashmead (Hymenoptera: Scelionidae) em populações de percevejos pragas da soja. Anais da Sociedade Entomológica do Brasil.  https://doi.org/10.1590/S0301-80592000000200011.
  30. Pazini, J. B., Grützmacher, A. D., Martins, J. F. S., Pasini, R. A., & Rakes, M. (2016). Selectivity of pesticides used in rice crop on Telenomus podisi and Trichogramma pretiosum. Pesquisa Agropecuária Tropical.  https://doi.org/10.1590/1983-40632016v4640844.
  31. Pratissoli, D., Thuler, R. T., Pereira, F. F., Reis, E. F., & Ferreira, A. T. (2004). Ação transovariana de lufenuron (50 g/l) sobre adultos de Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) e seu efeito sobre o parasitóide de ovos Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae). Ciência e Agrotecnologia.  https://doi.org/10.1590/S1413-70542004000100001.
  32. Proque, A. L., Cassuce, F. C. C., & Silva, E. H. (2014). Interações de Estados Unidos e Brasil no mercado mundial de soja em grão: uma análise dinâmica baseada nas trajetórias estocásticas das exportações. Organizações Rurais & Agroindustriais, 16, 518–531.Google Scholar
  33. Saber, M., Hejazi, M. J., Kamali, K., & Moharramipour, S. (2005). Lethal and sublethal effects of fenitrothion and deltamethrin residues on the egg parasitoid Trissolcus grandis (Hymenoptera: Scelionidae). Journal of Economic Entomology.  https://doi.org/10.1603/0022-0493-98.1.35.
  34. Sattar, S., Farmanullah, Saljoqi, A. R., Arif, M., Sattar, H., & Qazi, J. I. (2011). Toxicity of some new insecticides against Trichogramma chilonis (Hymenoptera: Trichogrammatidae) under laboratory and extended laboratory conditions. Pakistan Journal of Zoology, 43, 1117–1125.Google Scholar
  35. Shea, K., Nisbet, R. M., Murdoch, W. W., & Yoo, H. J. S. (1996). The effect of egg limitation on stability in insect host-parasitoid population models. The Journal of Animal Ecology, 65(6), 743–755.CrossRefGoogle Scholar
  36. Silva, F. A. S., & Azevedo, C. A. V. (2016). The ASSISTAT software version 7.7 and its use in the analysis of experimental data. African Journal of Agricultural Research, 11, 3733–3740.  https://doi.org/10.5897/AJAR2016.11522.CrossRefGoogle Scholar
  37. Silva, A. F., Concenço, G., Aspiazú, I., Ferreira, E. A., Galon, L., Coelho, A. T. C. P., Silva, A. A., & Ferreira, F. A. (2009). Interferência de plantas daninhas em diferentes densidades no crescimento da soja. Planta Daninha.  https://doi.org/10.1590/S0100-83582009000100011.
  38. Smaniotto, L.F., Gouvea, A., Potrich, M., Silva, E.R.L., Silva, J. & Pegorini, C.S. (2013). Seletividade de produtos alternativos a Telenomus podisi Ashmead (Hymenoptera: Scelionidae). Semina: Ciênc. Agrár. doi: https://doi.org/10.5433/1679-0359.2013v34n6Supl1p3295.
  39. Souza, J. R., Carvalho, G. A., Moura, A. P., Couto, M. H. G., & Maia, J. B. (2014). Toxicity of some insecticides used in maize crop on Trichogramma pretiosum (Hymenoptera, Trichogrammatidae) immature stages. Chilean Journal of Agricultural Research.  https://doi.org/10.4067/S0718-58392014000200016.
  40. Stefanello, G. J., Grützmacher, A. D., Grützmacher, D. D., Dalmazo, G. O., Paschoal, M. D. F., & Härter, W. R. (2008). Efeito de inseticidas usados na cultura do milho sobre a capacidade de parasitismo de Trichogramma pretiosum Riley, 1879 (Hymenoptera: Trichogrammatidae). Arquivos do Instituto Biológico, 75, 187–194.Google Scholar
  41. Vianna, U. R., Pratissoli, D., Zanuncio, J. C., Lima, E. R., Brunner, J., Pereira, F. F., & Serrão, J. E. (2009). Insecticide toxicity to Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) females and effect on descendant generation. Ecotoxicology, 18, 180–186.  https://doi.org/10.1007/s10646-008-0270-5.CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Crop Protection, Faculty of Agricultural Sciences Eliseu Maciel (FAEM)Federal University of Pelotas (UFPel)PelotasBrazil

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