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Side effects of insecticides used in wheat crop on eggs and pupae of Chrysoperla externa and Eriopis connexa

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Abstract

In Brazil, chemical control is one of the main tools to manage insect pests in wheat. However, this kind of management can impair the biological control provided by the predators Chrysoperla externa and Eriopis connexa. The present study evaluated the side effects on C. externa and E. connexa of 15 insecticides registered for wheat. Insecticides were sprayed on eggs and pupae via Potter tower at the maximum recommended dose. We evaluated the viability of eggs and pupae as well as the sub-lethal effects on fecundity and fertility of the adults emerged from treated pupae. The insecticides were classified according to the scale of toxicity proposed by IOBC. Regarding the eggs, the insecticide etofenprox was classified as slightly harmful (class 2) to C. externa. Imidacloprid + beta-cyfluthrin, diflubenzuron WG, thiamethoxam + lambda-cyhalothrin A and B, gamma-cyhalothrin, and etofenprox were also classified as slightly harmful (class 2) to E. connexa, while methomyl was classified as moderately harmful (class 3) for the eggs of the predator. The insecticide imidacloprid + beta-cyfluthrin was considered slightly harmful (class 2) to pupae of C. externa, while imidacloprid + beta-cyfluthrin, thiamethoxam + lambda-cyhalothrin A and B, and lufenuron were classified as slightly harmful (class 2) to the pupae of E. connexa. The insecticides beta-cyfluthrin, diflubenzuron SC, lambda-cyhalothrin, permethrin, thiamethoxam, triflumuron, and zeta-cypermethrin were harmless to eggs and pupae of both predators and should therefore be prioritized in the control of insect pests in wheat, thus preserving the natural biological control provided by C. externa and E. connexa.

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References

  • AGROFIT (2017). Sistema de inseticidas fitossanitários. Retrieved from http://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons.

  • Bueno, A. F., & Freitas, S. (2004). Effect of the insecticides abamectin and lufenuron on eggs and larvae of Chrysoperla externa under laboratory conditions. Biological Control. https://doi.org/10.1023/B:BICO.0000025375.07428.0b

  • Carvalho, C. F., & Souza, B. (2000). Métodos de criação e produção de crisopídeos. In V. H. P. Bueno (Ed.), Controle biológico de pragas: produção massal e controle de qualidade (pp. 91–109). UFLA: Lavras.

    Google Scholar 

  • Carvalho, G. A., Carvalho, C. F., Souza, B., & Ulhôa, J. L. R. (2002). Seletividade de inseticidas a Chrysoperla externa (Hagen) (Neuroptera: Chrysopidae). Neotropical Entomology. https://doi.org/10.1590/S1519-566X2002000400015

  • Castilhos, R.V., Grützmacher, A.D., Nava, D.E., Zotti, M.J., Siqueira, P.R.B., & Spagnol, D. (2013). Selectivity of pesticides used in peach orchards on the larval stage of the predator Chrysoperla externa (Hagen). Semina: Ciências Agrárias. https://doi.org/10.5433/1679-0359.2013v34n6Supl1p3585.

  • Castilhos, R. V., Grützmacher, A. D., Siqueira, P. R. B., Moraes, I. L., & Gauer, C. J. (2014). Seletividade de inseticidas utilizados em pessegueiro sobre ovos e pupas do predador Chrysoperla externa. Ciência Rural. https://doi.org/10.1590/0103-8478cr20140248.

  • Cosme, L. V., Carvalho, G. A., Moura, A. P., & Parreira, D. S. (2009). Toxicidade de óleo de nim para pupas e adultos de Chrysoperla externa (Hagen) (Neuroptera: Chrysopidae). Arquivos do Instituto Biológico, 76, 233–238.

    Google Scholar 

  • Dacosta, R. R., Carvalho, G. A., Carvalho, C. F., & Costa, R. R. (2008). Ação de fungicidas utilizados na cultura do pepino sobre larvas de primeiro ínstar de Chrysoperla externa (Hagen, 1861) (Neuroptera: Chrysopidae) e os efeitos sobre suas fases subsequentes. Arquivos do Instituto Biológico, 75, 243–350.

    Google Scholar 

  • Desneux, N., Decourtye, A., & Delpuech, J. M. (2007). Sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology. https://doi.org/10.1146/annurev.ento.52.110405.091440

  • Eichler, M.R., & Reis, E.M. (1976). Seletividade fisiológica de inseticidas aos predadores de afídios: Cycloneda sanguinea L., 1763) e Eriopis connexa (Germ., 1824) (Coleoptera - Coccinellidae ). Passo Fundo, Embrapa Trigo (CNPT).

  • Fogel, M., Rimoldi, F., Pineda, S., Schneider, M., & Ronco, A. (2009). Side effects of teflubenzuron and chlorfenapyr in Eriopis connexa eggs (coleoptera: Coccinellidae). Communications in Agricultural and Applied Biological Sciences, 74, 419–423.

  • Fogel, M. N., Schneider, M. I., Desneux, N., González, B., & Ronco, A. E. (2013). Impact of the neonicotinoid acetamiprid on immature stages of the predator Eriopis connexa (Coleoptera: Coccinellidae). Ecotoxicology. https://doi.org/10.1007/s10646-013-1094-5

  • Galvan, T. L., Koch, R. L., & Hutchison, W. D. (2005). Toxicity of commonly used insecticides in sweet corn and soybean to multicolored Asian lady beetle (Coleoptera: Coccinellidae). Journal of Economic Entomology. https://doi.org/10.1603/0022-0493-98.3.780

  • Garzon, A., Medina, P., Amor, F., Vinuela, E., & Budia, F. (2015). Toxicity and sublethal effects of six insecticides to last instar larvae and adults of the biocontral agents Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) and Adalia bipunctata (L.) (Coleoptera: Coccinellidae). Chemosphere. https://doi.org/10.1016/j.chemosphere.2015.03.016

  • Gassen, D. N. (1988). Controle biológico de pulgões em trigo. Embrapa Trigo (CNPT): Passo Fundo.

    Google Scholar 

  • Gassen, D. N. (1999). Controle biológico de pulgões de trigo no Brasil. Embrapa Trigo (CNPT): Passo Fundo.

    Google Scholar 

  • Godoy, M. S., Carvalho, G. A., Moraes, J. C., Cosme, L. V., Goussain, M. M., Carvalho, C. F., & Morais, A. A. (2004). Seletividade de seis inseticidas utilizados em citros a pupas e adultos de Chrysoperla externa (Hagen) (Neuroptera: Chrysopidae). Neotropical Entomology. https://doi.org/10.1603/0022-0493-98.3.780

  • Gusmão, M. R., Picanço, M., Leite, G. L. D., & Moura, M. F. (2000). Seletividade de inseticidas a predadores de pulgões. Horticultura Brasileira. https://doi.org/10.1590/S0102-05362000000200011

  • Lavagnini, T. C., Morales, A. C., & Freitas, S. (2015). Population genetics of Chrysoperla externa (Neuroptera: Chrysopidae) and implications for biological control. Brazilian Journal of Biology. https://doi.org/10.1590/1519-6984.02014

  • Medina, P., Budia, F., Estal, E. P., Del Adán, A., & Viñuela, E. (2003). Side effects of six insecticides on different developmental stages of Chrysoperla carnea (Neuroptera: Chrysopidae). IOBC/WPRS Bulletin, 26, 33–40.

  • Moraes, J. C., Goussain, M. M., Basagli, M. A. B., Carvalho, G. A., Ecole, C. C., & Sampaio, M. V. (2004). Silicon influence on the tritrophic interaction: Wheat plants, the greenbug Schizaphis graminum (Rondani) (Hemiptera: Aphididae), and its natural enemies, Chrysoperla externa (Hagen) (Neuroptera: Chrysopidae) and Aphidius colemani Viereck (hymenoptera: Aphidiidae). Neotropical Entomology. https://doi.org/10.1590/S1519-566X2004000500012

  • Moura, A. P., Carvalho, G. A., Lasmar, O., Moscardini, V. F., & Rezende, D. T. (2009). Efeitos da aplicação de inseticidas utilizados na produção integrada de maçã sobre pupas de Chrysoperla externa. Ciência Rural. https://doi.org/10.1590/S0103-84782009005000182.

  • Moura, A. P., Carvalho, G. A., Moscardini, V. F., Lasmar, O., Rezende, D. T., & Marques, M. C. (2010). Selectivity of pesticides used in integrated apple production to the lacewing, Chrysoperla externa. Journal of Insect Science. https://doi.org/10.1673/031.010.12101

  • Nasreen, A., Ashfaq, M., Mustafa, G., & Khan, R. R. (2007). Mortality rates of five commercial insecticides on Chrysoperla carnea (Stephens, 1836) (Chrysopidae: Neuroptera). Pakistan Journal of Agricultural Sciences, 44, 266–271.

    Google Scholar 

  • Ndakidemi, B., Mtei, K., & Ndakidemi, P. A. (2016). Impacts of synthetic and botanical pesticides on beneficial insects. Agricultural Sciences. https://doi.org/10.4236/as.2016.76038

  • Pappas, M. L., Broufas, G. D., & Koveos, D. S. (2011). Chrysopid predators and their role in biological control. Journal of Entomology. https://doi.org/10.3923/je.2011.301.326

  • Pedroso, E. C., Carvalho, G. A., Leite, M. I. S., & Rezende, D. T. (2011). Seletividade de inseticidas utilizados no algodoeiro sobre pupas e adultos da joaninha Cycloneda sanguinea (Linnaeus, 1763). Arquivos do Instituto Biológico, 78, 573–584.

    Google Scholar 

  • Pedroso, E. C., Carvalho, G. A., Leite, M. I. S., Rezende, D. T., & Moura, A. P. (2012). Seletividade de inseticidas utilizados na cultura algodoeira a ovos e larvas de terceiro instar de Cycloneda sanguinea. Arquivos do Instituto Biológico. https://doi.org/10.1590/S1808-16572012000100009

  • Picanço, M. C., Bacci, L., Crespo, A. L. B., Miranda, M. M. M., & Martins, J. C. (2007). Effect of integrated pest management practices on tomato production and conservation of natural enemies. Agricultural and Forest Entomology. https://doi.org/10.1111/j.1461-9563.2007.00346.x

  • Püntener, W. (1981). Manual for field trials in plant protection. 2.ed. Ciba-Geigy, Basle.

  • Reddy, P. P. (2016). Selective pesticides in IPM. In P. P. Reddy (Ed.), Sustainable crop protection under protected cultivation (pp. 121–131). Singapore: Springer.

    Chapter  Google Scholar 

  • Resende, A. L. S., Ferreira, R. B., Silveira, L. C. P., Pereira, L. P. S., Landim, D. V., & Carvalho, C. F. (2015). Desenvolvimento e reprodução de Eriopis connexa (Germar, 1824) (Coleoptera: Coccinellidae) alimentada com recursos florais de coentro (Coriandrum sativum L.). Entomotropica, 30, 12–19.

  • Rodrigues, A. R. S., Torres, J. B., Siqueira, H. A. A., & Lacerda, D. P. (2013). Inheritance of lambda-cyhalothrin resistance in the predator lady beetle Eriopis connexa (Germar) (Coleoptera: Coccinellidae). Biological Control. https://doi.org/10.1016/j.biocontrol.2012.11.018

  • Rugno, G. R., Zanardi, O. Z., & Yamamoto, P. T. (2015). Are the pupae and eggs of the lacewing Ceraeochrysa cubana (Neuroptera: Chrysopidae) tolerant to insecticides? Journal of Economic Entomology. https://doi.org/10.1093/jee/tov263

  • Ruiz-Sánchez, E., Caamal-Eb, L., Cristóbal-Alejo, J., Munguía-Rosale, R., & Pérez-Gutiérrez, A. (2010). Survivorship and development of immature Harmonia axyridis Pallas (Coleoptera: Coccinellidae) exposed to diflubenzuron. Agrociencia, 44, 373–379.

    Google Scholar 

  • 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. https://doi.org/10.5897/AJAR2016.11522

  • Silva, R. A., Carvalho, G. A., Carvalho, C. F., Reis, P. R., Souza, B., & Pereira, A. M. A. R. (2006). Ação de produtos fitossanitários utilizados em cafeeiros sobre pupas e adultos de Chrysoperla externa (Hagen, 1861) (Neuroptera: Chrysopidae). Ciencia Rural. https://doi.org/10.1590/S0103-84782006000100002

  • Silva, R. B., Zanuncio, J. C., Serrao, J. E., Lima, E. R., Figueiredo, M. L. C., & Cruz, I. (2009). Suitability of different artificial diets for development and survival of stages of the predaceous ladybird beetle Eriopis connexa. Phytoparasitica. https://doi.org/10.1007/s12600-008-0015-2

  • Stark, J. D., Vargas, R., & Banks, J. E. (2007). Incorporating ecologically relevant measures of pesticide effect for estimating the compatibility of pesticides and biocontrol agents. Journal of Economic Entomology, 100(4), 1027-1032. https://doi.org/10.1093/jee/100.4.1027

  • Sterk, G., Hassan, S. A., Baillod, M., Bakker, F., Bigler, F., Blümel, S., Bogenschutz, H., Boller, E., Bromand, B., Brun, J., Calis, J. N. M., Coremans-Pelseneer, J., Duso, C., Garrido, A., Grove, A., Heimbach, U., Hokkanen, H., Jacas, J., Lewis, G., Moreth, L., Polgar, L., Roversti, L., Samsoe-Peterson, L., Sauphanor, B., Schaub, L., Stäubli, A., Tuset, J. J., Vainio, A., Van de Veire, M., Viggiani, G., Vinuela, E., & Vogt, H. (1999). Results of the seventh joint pesticide testing programme carried out by the IOBC/WPRS-working group 'Pesticides and beneficial Organisms'. BioControl. https://doi.org/10.1023/A:1009959009802

  • Torres, A. F., Carvalho, G. A., Santa-Cecília, L. V. C. & Moscardini, V. F. (2013). Selectivity of seven insecticides against pupae and adults of Chrysoperla externa (Neuroptera: Chrysopidae). Revista Colombiana de Entomologia, 39, 34–39.

  • Venzon, M., Rosado, M. C., Pallini, A., Fialho, A., & Pereira, C. J. (2007). Lethal and sublethal toxicity of neem on green peach aphid and on its predator Eriopis connexa. Pesquisa Agropecuária Brasileira. https://doi.org/10.1590/S0100-204X2007000500003

  • Venzon, M., Lemos, F., Sarmento, R. A., & Pallini, A. (2009). Predation by coccinellids and chrysopid species influenced by Tetranychus evansi webbing. Pesquisa Agropecuária Brasileira. https://doi.org/10.1590/S0100-204X2009000900003

  • Vilela, M., Carvalho, G. A., Carvalho, C. F., Vilas boas, M. A., & Leite, M. I. S. (2010). Seletividade de acaricidas utilizados em cafeeiro para larvas de crisopídeos. Revista Ceres. https://doi.org/10.1590/S0034-737X2010000500009.

  • Vogt, H., Rumpf, S., Wetzel, C., & Hassan, S. A. (1992). A field method for testing effects of pesticides on the green lacewing Chrysoperla carnea Steph. IOBC/WPRS Bulletin, 15, 176–182.

    Google Scholar 

  • Vogt, H., Bigler, F., Brown, K., Candolfi, M. P., Kemmeter, F., Kühner, C., Moll, M., Travis, A., Ufer, A., Viñuela, E., Wladburger, M., & Waltersdorfer, A. (2000). Laboratory method to test effects of plant protection products on larvae of Chrysoperla carnea (Neuroptera: Chrysopidae). In M. P. Candolfi, S. Blumel, R. Forster, F. M. Bakker, C. Grimm, S. A. Hassan, U. Heimbach, M. A. Mead-Briggs, B. Reber, R. Schmuck, & H. Vogt (Eds.), Guidelines to evaluate side-effects of plant protection products to non-target arthropods (pp. 27–44). Germany: Reinheim.

    Google Scholar 

  • Youn, Y. N., Seo, M. J., Shin, J. G., Jang, C., & Yu, Y. M. (2003). Toxicity of greenhouse pesticides to multicolored Asian lady beetles, Harmonia axyridis (Coleoptera: Coccinellidae). Biological Control. https://doi.org/10.1016/S1049-9644(03)00098-7

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Acknowledgements

This research was supported by the Coordination for the Improvement of Higher Education Personnel (CAPES) and the National Council for Scientific and Technological Development (CNPq).

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  1. Department of Plant Protection, Federal University of Pelotas, Pelotas, Rio Grande do Sul, postcode 96010-900, Brazil

    Rafael Antonio Pasini, Anderson Dionei Grützmacher, Juliano de Bastos Pazini, Franciele Silva de Armas, Flávio Amaral Bueno & Stefânia Nunes Pires

  2. Faculdade de Agronomia Eliseu Maciel (FAEM), Universidade Federal de Pelotas (UFPel), Pelotas, Rio Grande do Sul, postcode 96010-900, Brazil

    Rafael Antonio Pasini

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  1. Rafael Antonio Pasini
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  2. Anderson Dionei Grützmacher
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Pasini, R.A., Grützmacher, A.D., de Bastos Pazini, J. et al. Side effects of insecticides used in wheat crop on eggs and pupae of Chrysoperla externa and Eriopis connexa. Phytoparasitica 46, 115–125 (2018). https://doi.org/10.1007/s12600-018-0639-9

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