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Weeds should be controlled with low impact methods and selective agrochemicals that have little or no effect on non-target organisms. This study aimed to evaluate the effect of the herbicide atrazine (triazine class) on 10 Trichogrammatidae (Hymenoptera) species. A female of 10 species of these natural enemies was individually placed in a glass test tube (free-choice test) with two paper cards containing 45 Anagasta (Ephestia) kuehniella (Lepidoptera: Pyralidae) eggs (treatment and control), with 10 replications. The cards were sprayed with the herbicide atrazine at 8.07 L/ha; the control was sprayed with distilled water. Parasitism by these natural enemies was allowed for 48 h. Atrazine changes the behavior of female parasitoids, reducing the parasitism (≈ 71 %) and emergence (≈ 74 %) rates and sex ratio (≈ 74 %) of the Trichogrammatidae species, except for Trichogramma galloi and T. bennetti. No females emerged from eggs parasitized by T. acacioi, Trichogrammatoidea annulata, T. atopovirilia, T. bruni, T. brasiliensis, T. demoraesi, and T. soaresi with atrazine. The results revealed that atrazine herbicide is harmless to T. bennetti and T. galloi, but it was moderately harmful (80 – 99 % reduction) to the other Trichogrammatidae species based on the parasitism and emergence rates.

Demolin Leite, G. L. ., Rodrigues Bispo, E. P. ., Costa Alvarenga, . A. ., de Paulo, P. D. ., Soares, M. A., & Lemes, P. G. . (2021). Toxicological and behavioral impacts of atrazine on Trichogrammatidae (Hymenoptera) in choice tests. Revista Colombiana De Entomología, 47(1). https://doi.org/10.25100/socolen.v47i1.8445

ANTIGO, M. R.; OLIVEIRA, H. N.; CARVALHO, G. A.; PEREIRA, F. F. 2013. Repellence of pesticides used in sugarcane and their effects on the emergence of Trichogramma galloi. Revista

Ciência Agronômica 44 (4): 910-916. https://doi.org/10.1590/S1806-66902013000400030

BARA, J. J.; MONTGOMERY, A.; MUTURI, E. J. 2014. Sublethal effects of atrazine and glyphosate on life history traits of Aedes aegypti and Aedes albopictus (Diptera: Culicidae). Parasitology

Research 113: 2879-2886. https://doi.org/10.1007/s00436-014-3949-y

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. http://www.scielo.org.co/pdf/rcen/v36n1/v36n1a03.pdf

CHEN, L.; ZHU, X.; WANG, Y.; CHEN, L.; DUAN, Y. 2014. Proteomic analysis of the bacterial induction of resistance to atrazine in soybean leaves. Acta Physiologiae Plantarum 36: 2229-

https://doi.org/10.1007/s11738-014-1601-1

DAS, T. K.; SAKHUJA, P. K.; ZELLEKE, H. 2010. Herbicide efficacy and non-target toxicity in highland rainfed maize of Eastern Ethiopia. International Journal of Pest Management 56 (4): 315- 325. https://doi.org/10.1080/09670874.2010.497872

FICKETT, N. D.; BOERBOOM, C. M.; STOLTENBERG, D. E. 2013. Predicted corn yield loss due to weed competition prior to postemergence herbicide application on Wisconsin farms. Weed

Technology 27 (1): 54-62. https://doi.org/10.1614/WT-D-12-00097.1

GARDNER, J.; HOFFMANN, M. P.; PITCHER, S. A.; HARPER, J. K. 2011. Integrating insecticides and Trichogramma ostriniae to control European corn borer in sweet corn: Economic analysis.

Biological Control 56 (1): 9-16. https://doi.org/10.1016/j.biocontrol.2010.08.010

KHAN, M. A.; KHAN, H.; RUBERSON, J. R. 2015. Lethal and behavioral effects of selected novel pesticides on adults of Trichogramma pretiosum (Hymenoptera: Trichogrammatidae).

Pest Management Science 71 (12): 1640-1648. https://doi.org/10.1002/ps.3972

LEITE, G. L. D.; PAULO, P. D.; ZANUNCIO, J. C.; ALVARENGA, A. C.; SOARES, M. A.; TAVARES, W. S.; TUFFI-SANTOS, L. D.; SPÍNOLA-FILHO, P. R. C. 2015. Effects of atrazine-based herbicide on emergence and sex ratio of Trichogrammatidae (Hymenoptera). Florida Entomologist 98 (3): 899-902. https://doi.org/10.1653/024.098.0313

LINS, V. L.; SANTOS, H. R.; GONÇALVES, M. C. 2007. The effect of the glyphosate, 2,4-D, atrazinee nicosulfuron herbicides upon the edaphic Collembola (Arthropoda: Ellipura) in a no tillage system. Neotropical Entomology 36 (2): 261-267. https://doi.org/10.1590/S1519-566X2007000200013

MENEZES, C. W. G.; SOARES, M. A. 2016. Impacts of the control of weeds and herbicides applied to natural enemies. Revista Brasileira de Herbicidas 15 (1): 2-13. https://doi.org/10.7824/rbh.v1i1.407

MENEZES, C. W. G.; SANTOS, J. B.; ASSIS JÚNIOR, S. L.; FONSECA, A. J.; FRANÇA, A. C.; SOARES, M. A.; FERNANDES, A. F. 2012. Seletividade de atrazine e nicosulfuron a Podisus nigrispinus (Heteroptera: Pentatomidae). Planta Daninha 30 (2): 327-334. https://doi.org/10.1590/S0100-83582012000200011

MENEZES, C. W. G.; TAVARES, W. S.; SOUZA, E. G.; SOARES, M. A.; SERRÃO, J. E.; ZANUNCIO, J. C. 2014. Effects of crude extract fractions of Adenocalymma nodosum (Bignoniaceae) on duration of pupa stage emergence of Tenebrio molitor (Coleoptera: Tenebrionidae) and phytotoxicity on vegetable crops. Allelopathy Journal 33 (1): 141-149.

OLIVEIRA, H. N.; ANTIGO, M. R.; CARVALHO, G. A.; GLAESER, D. F. 2014. Effect of selectivity of herbicides and plant growth regulators used in sugarcane crops on immature stages of Trichogramma galloi (Hymenoptera: Trichogrammatidae). Planta Daninha 32 (1): 125-131. https://doi.org/10.1590/S0100-83582014000100014

PASCOALOTO, I. M.; ANDREOTTI, M.; CRUZ, S. S.; SABBAG, O. J.; BORGHI, E.; LIMA, G, C.; MODESTO, V. C. 2017. Economic analysis of sorghum consortia with forages or with dwarf pigeon pea succeeded by soybean or corn. Pesquisa Agropecuária Brasileira 52 (10): 833-840. https://doi.org/10.1590/s0100-204x2017001000002

PEREIRA, J. L.; SILVA, A. A.; PICANÇO, M. C.; BARROS, E. C.; JAKELAITIS, A. 2005. Effects of herbicide and insecticide interaction on soil entomofauna under maize crop. Journal of

Environmental Science and Health, Part B 40 (1): 45-54. https://doi.org/10.1081/PFC-200034212

PRATISSOLI, D.; OLIVEIRA, H. N.; GONÇALVES, J. R.; ZANUNCIO, J. C.; HOLTZ, A. M. 2004. Changes in biological characteristics of Trichogramma pretiosum (Hym.: Trichogrammatidae)

reared on eggs of Anagasta kuehniella (Lep.: Pyralidae) for 23 generations. Biocontrol Science and Technology 14 (3): 313-319. https://doi.org/10.1080/09583150310001639196

PRATISSOLI, D.; MILANEZ, A. M.; BARBOSA, W. F.; CELESTINO, F. N.; ANDRADE, G. S.; POLANCZYK. R. A. 2010. Side effects of fungicides used in cucurbitaceous crop on Trichogramma atopovirilia Oatman & Platner (Hymenoptera: Trichogramatidae). Chilean Journal of Agricultural Research 70 (2): 323-327. https://doi.org/10.4067/S0718-58392010000200016

PREZOTTI, L.; PARRA, J. R. P.; VENCOVSKY, R.; COELHO, A. S. G.; CRUZ, I. 2004. Effect of the size of the founder population on the quality of sexual populations of Trichogramma

pretiosum, in laboratory. Biological Control 30 (2): 174-180. https://doi.org/10.1016/j.biocontrol.2004.01.011

SOARES, M. A.; LEITE, G. L. D.; ZANUNCIO, J. C.; SÁ, V. G. M.; FERREIRA, C. S.; ROCHA, S. L.; PIRES, E. M.; SERRÃO, J.E. 2012. Quality control of Trichogramma atopovilia and Trichogramma

pretiosum (Hym.: Trichogrammatidae) adults reared under laboratory conditions. Brazilian Archives of Biology and Technology 55 (2): 305-311. https://doi.org/10.1590/S1516-

SOARES, M. A.; LEITE, G. L. D.; ZANUNCIO, J. C.; FERREIRA, C. S.; ROCHA, S. L.; SÁ, V. G. M. 2014. Assessment of Trichogramma species (Hymenoptera: Trichogrammatidae) for biological control in cassava (Manihot esculenta Crantz). Acta Scientiarum. Agronomy 36 (4): 403-408. https://doi.org/10.4025/actasciagron.v36i4.17744

SPÍNOLA-FILHO, P. R. C.; LEITE, G. L. D.; SOARES, M. A.; ALVARENGA, A. C.; PAULO, P. D.; TUFFI-SANTOS, L. D.; ZANUNCIO, J. C. 2014. Effects of duration of cold storage of host eggs on percent parasitism and adult emergence of each of ten Trichogrammatidae (Hymenoptera) species. Florida Entomologist 97 (1): 14-21. https://doi.org/10.1653/024.097.0102

STEFANELLO JÚNIOR, G. J.; GRÜTZMACHER, A. D.; GRÜTZMACHER, D. D.; LIMA, C. A. B.; DALMOZO, D. O.; PASCHOAL, M. D. F. 2008. Seletividade de herbicidas registrados para a cultura do milho a adultos de Trichogramma pretiosum (Hymenoptera: Trichogrammatidae). Planta Daninha 26 (2): 343-351. https://doi.org/10.1590/S0100-83582008000200010

STEFANELLO JÚNIOR, G. J.; GRÜTZMACHER, A. D.; PASINI, R. A.; BONEZ, C.; MOREIRA, D. C.; SPAGNOL, D. 2011. Seletividade de herbicidas registrados para a cultura do milho aos estádios imaturos de Trichogramma pretiosum (Hymenoptera: Trichogrammatidae). Planta Daninha 29 (special issue): 1069-1077. https://doi.org/10.1590/S0100-83582011000500014

STERK, G.; HASSAN, S. A.; BAILLOD, M.; BAKKER, F.; BIGLER, F.; BLÜMEL, S.; BOGENSCHÜTZ, 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.; ROVESTI, L.; SAMSOE-PETERSON, L.; SAUPHANOR, B.; SCHAUB, L.; STÄUBLI, A.;

TUSET, J.J.; VAINIO, A.; VAN DE VEIRE, M.; VIGGIANI, G.; VIÑUELA, 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 44: 99-117. https://doi.org/10.1023/A:1009959009802

TAVARES, W. S. 2010. Custos de uma Biofábrica de Trichogramma pretiosum Riley para o Controle da Lagarta-do-Cartucho no Milho. EntomoBrasilis 3 (2): 49-54. https://doi.org/10.12741/ebrasilis.v3i2.76

ZANUNCIO, J. C.; MATOS NETO, F. C.; TAVARES, W. S.; CRUZ, I.; LEITE, G. L. D.; SERRÃO, J. E. 2013. Functional and numerical responses and reproduction of Campoletis flavicincta

parasitizing Spodoptera frugiperda caterpillars. Acta Scientiarum. Agronomy 35 (4): 419-426. https://doi.org/10.4025/actasciagron.v35i4.15871

ZUIM, V.; RODRIGUES, H. S.; PRATISSOLI, D.; TORRES, J. B. 2017. Thermal requirements and performance of the parasitoid Trichogramma pretiosum (Hymenoptera: Trichogrammatidae)

on Helicoverpa armigera (Lepidoptera: Noctuidae) eggs undervariable temperatures. Environmental Entomology 46 (5): 1156-1164. https://doi.org/10.1093/ee/nvx132

Received 2019-08-26
Accepted 2021-01-12
Published 2021-06-10