Comparative effectiveness of Metarhizium rileyi, novaluron, and glyphosate on immune system, development, and redox metabolism of Anticarsia gemmatalis

Authors

DOI:

https://doi.org/10.33448/rsd-v10i6.15611

Keywords:

Agrochemical; Pest control; Entomopathogenic fungus; Oxidative stress; Soybean; Hemocytes.

Abstract

Anticarsia gemmatalis is one of the most important pests in world soybean crop. The most common intervention is the application of agrochemicals, such as novaluron and glyphosate. Among biological control agents, much attention has been drawn to entomopathogenic fungi, as Metarhizium rileyi. Here, we examined the changes that occur in the immune system (total and differential hemocyte count), secondary effects (caterpillar morphology), and oxidative metabolism after the caterpillars were exposed to M. rileyi, novaluron or glyphosate. M. rileyi was able to induce changes in the width, length, and weight of A. gemmatalis pupae, along with an increased in the number of defense cells. Novaluron prompt changes the insect’s immunity, and glyphosate caused milder immunological effects. However, it caused significant secondary effects including malformations in pupae and adults, and an increase in nitric oxide (NO) levels. Mortality observed when treating insects with novaluron and malformations due to glyphosate treatments did not occur due to oxidative stress. However, when insects were exposed to M. rileyi, we verified significantly increased levels of NO and concluded that these insects died due to oxidative stress. Our data provide evidence that contributes to better understanding the mechanism of herbicide-fungus interaction in the management of Anticarsia gemmatalis.

Author Biographies

Ana Paula Vargas Visentin, Universidade de Caxias do Sul

Biotechnology Institute, Pest Control Laboratory and Oxidative Stress and Antioxidants Laboratory

Lúcia Rosane Bertholdo, University of Caxias do Sul

Biotechnology Institute, Pest Control Laboratory

Rahyssa Chagas Hahn, University of Caxias do Sul

Biotechnology Institute, Pest Control Laboratory

Rafaela Andressa Thomazoni, University of Caxias do Sul

Biotechnology Institute, Pest Control Laboratory

Luciana Bavaresco Andrade Touguinha, University of Caxias do Sul

Institute of Biotechnology, Laboratory of Oxidative Stress and Antioxidants

Catia Santos Branco, University of Caxias do Sul

Institute of Biotechnology, Laboratory of Oxidative Stress and Antioxidants

Mirian Salvador, University of Caxias do Sul

Institute of Biotechnology, Laboratory of Oxidative Stress and Antioxidants

Neiva Monteiro de Barros, University of Caxias do Sul

Biotechnology Institute, Pest Control Laboratory

References

Agência Nacional de Vigilância Sanitária - ANVISA (2018). Nota Técnica No 23/2018/Sei/Creav /Gemar/Ggtox/Dire3/Anvisa http://antigo.anvisa.gov.br/documents/33836/349757/Nota+t%C3%A9cnica+23+2018+GGMED+-+Intercambialidade/a42bd2fa-0136-4bb1-b7dc-a8d5243197a7

Alves, S. B (1998). Fungos Entomopatogênicos. In: Controle Microbiano de Insetos, Fundação d. ed. Piracicaba/SP.

Branco, C. dos S., de Lima, É. D., Pavão, E., Bertholdo-Vargas, L. R., de Barros, N. M. & Salvador, M. (2014). Araucaria angustifolia (Bert.) O. Kuntze induces oxidative and genotoxic damage in larvae of Anticarsia gemmatalis Hübner (Lepidoptera: Erebidae). International Journal of Pest Management, 60 (2), 114-120.

Branco, C. dos S., Rodrigues, T. S., de Lima, É. D, Bertholdo-Vargas, L. R., Barros, N. M. & Salvador, M. (2016). Redox imbalance mediates entomotoxic effects of the conifer Araucaria angustifolia in Anticarsia gemmatalis velvetbean caterpillar. Cogent Food & Agriculture, 2(1), 1174973.

Butt, T.M & Shields, K.S. (1996). The structure and behavior of gypsy moth (Lymantria dispar) hemocytes. Journal of Invertebrate Pathology, 68(1), 1-14.

Cáceres, L., Necakov, A. A. S., Schwartz, C., Kimber, S., Roberts, I.J.H. & Krause, H.M. (2011). Nitric oxide coordinates metabolism, growth, and development via the nuclear receptor E75. Genes & development, 25 (14), 1476-1485.

Castro, J.M., Rozemberg, B., Gomide, M., Filho, P.A. & Silva, C.G. (2019). Desigualdades Sociais Nas Práticas De Uso De Inseticidas Domésticos No Município De Niterói – Rj. Revista Brasileira Ciências da Saúde 23, 263–272.

Cattani, D., de Liz Oliveira Cavalli, V.L., Heinz Rieg, C.E., Domingues, J.T., Dal-Cim, T., Tasca, C.I., Mena Barreto Silva, F.R. & Zamoner, A. (2014). Mechanisms underlying the neurotoxicity induced by glyphosate-based herbicide in immature rat hippocampus: Involvement of glutamate excitotoxicity. Toxicology 320, 34–45.

Cobb, C. A. & Cole, M. P. (2015). Oxidative and Nitrative Stress in Neurodegeneration. Neurobiology of disease, 84, 4-21.

Costa, A. M. & Martins, P. C. C. (2009). Análise da contagem total de hemócitos e capacidade coagulante da hemolinfa do camarão Litopenaeus Vannamei (BOONE, 1931) em cultivos analysis of total hemocytes counting and capacity of hemolymph coagulation of shrimp Litopenaeus vannamei . Boletim do Instituto de Pesca, 35(4), 545-551.

Departamento do Agronegócio da Fiesp- Deagro (2016). Safra Mundial de Soja 2015 / 16 - 10o Levantamento do USDA. Dep. do Agronegócio-DEAGRO/FIESP 10, 1.

Paulo, J. F., Camargo, M. G., Coutinho-Rodrigues, C. J. B., Marciano, A. F., de Freitas, M. C., da Silva, E. M., Gôlo, P. S., Morena, D. D. S., da Costa Angelo, I. & Bittencourt, V. R. E. P. (2018). Rhipicephalus microplus infected by Metarhizium: unveiling hemocyte quantification, GFP-fungi virulence, and ovary infection. Parasitology research, 117(6), 1847-1856.

Dubovskiy, I. M., Whitten, M. M. A., Yaroslavtseva, O. N., Greig, C., Kryukov, V. Y., Grizanova, E. V., Mukherjee, K., Vilcinskas, A., Glupov, V. V. & Butt, T. M. (2013). Can Insects Develop Resistance to Insect Pathogenic Fungi? PloS one, 8(4), e60248

El-Aziz, N. M. A. & Awad, H. H. (2010). Changes in the haemocytes of Agrotis ipsilon larvae (Lepidoptera: Noctuidae) in relation to dimilin and Bacillus thuringiensis infections. Micron, 41(3), 203-209.

Falleiros, Â. M. F., Bombonato, M. T. S. & Gregório, E. A. (2003). Ultrastructural and quantitative studies of hemocytes in the sugarcane borer, Diatraea saccharalis (Lepidoptera: Pyralidae). Brazilian Archives of Biology and Technology, 46, 287-294.

Faraldo, A. C., Sá-Nunes, A., Del Bel, E. A., Faccioli, L. H. & Lello, E. (2005). Nitric oxide production in blowfly hemolymph after yeast inoculation. Nitric Oxide, 13(4), 240-246.

Federação das Indústrias do Estado de São Paulo- Fiesp (2020). Informativo Safra Mundial de Soja 2019 / 20 - 3o Levantamento do USDA 20, 1.

Fiorotti, J., Menna-Barreto, R. F. S., Gôlo, P. S., Coutinho-Rodrigues, C. J. B., Bitencourt, R. O. B., Spadacci-Morena, D. D., Da Costa Angelo, I. & Bittencourt, V. R. E. P. (2019). Ultrastructural and Cytotoxic Effects of Metarhizium robertsii Infection on Rhipicephalus microplus Hemocytes. Frontiers in physiology, 10, 654.

Foley, E. & O’Farrell, P. H. (2003). Nitric oxide contributes to induction of innate immune responses to gram-negative bacteria in Drosophila. Genes & development, 17(1), 115-125.

Fronza, E., Specht, A., Heinzen, H. & de Barros, N.M. (2017). Metarhizium (Nomuraea) rileyi as biological control agent. Biocontrol Science and Technology, 27(11), 1243-1264.

Gonzalez, E. A., Garg, A., Tang, J., Nazario-Toole, A. E. & Wu, L. P. (2013). A Glutamate Dependent Redox System in Blood Cells is Integral for Phagocytosis in Drosophila melanogaster. Current Biology, 23(22), 2319-2324.

Green, L. C., Ruiz de Luzuriaga, K., Wagner, D. A., Rand, W., Istfan, N., Young, V. R. & Tannenbaum, S. R. (1981). Nitrate biosynthesis in man. Proceedings of the National Academy of Sciences, 78 (12), 7764-7768.

Greenne, G. L., Leppla, N. & Dickerson, W. (1976). Velvetbean Caterpillar: a rearing produce and antificial médium. Journal of Economic Entomology, 69(4), 487-488.

Gupta, A. P. (1991). Insect immunocytes and other hemocytes: Roles in cellular and humoral immunity, in: Immunology of Insects and Other Arthropods. pp. 19-118.

Gupta, A. P. (1979). Insect hemocytes: development, forms, functions, and techniques, Cambridge. ed.

Haase, S., Sciocco-Cap, A. & Romanowski, V. (2015). Baculovirus insecticides in Latin America: Historical overview, current status and future perspectives. Viruses, 7 (5), 2230-2267.

Hermes-Lima, M. & Storey, K., (1995). Antioxidant defenses and metabolic depression in a pulmonate land snail. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 268(6), R1386-R1393.

Huang, Q., Zhang, L., Yang, C., Yun, X. & He, Y. (2016). The competence of hemocyte immunity in the armyworm Mythimna separata larvae to sublethal hexaflumuron exposure. Pesticide biochemistry and physiology, 130, 31-38.

Iummato, M. M., Sabatini, S. E., Cacciatore, L. C., Cochón, A. C., Cataldo, D., de Molina, M. del C.R. & Juárez, Á. B. (2018). Biochemical responses of the golden mussel Limnoperna fortunei under dietary glyphosate exposure. Ecotoxicology and environmental safety, 163, 69-75.

Kogan, M. & Turnipseed, S.G. (1987). Ecology and management of soybean arthropods. Annual Review of Entomology, 32(1), 507-538.

Kreutz, L. C., Gil Barcellos, L. J., de Faria Valle, S., de Oliveira Silva, T., Anziliero, D., Davi dos Santos, E., Pivato & M., Zanatta, R. (2011). Altered hematological and immunological parameters in silver catfish (Rhamdia quelen) following short term exposure to sublethal concentration of glyphosate. Fish & shellfish immunology, 30(1), 51-57.

Kreyci, P. F. & Menten, J.O. (2013). Limitadoras de produtividade. Cultiv. Cad. Técnico 167, 1–12.

Kwon, H., Bang, K. & Cho, S. (2014). Characterization of the hemocytes in larvae of Protaetia brevitarsis seulensis: Involvement of granulocyte-mediated phagocytosis. PLoS One, 9(8), e103620.

Lanctot, C., Navarro-Martín, L., Robertson, C., Park, B., Jackman, P., Pauli, B.D. & Trudeau, V.L. (2014). Effects of glyphosate-based herbicides on survival, development, growth and sex ratios of wood frog (Lithobates sylvaticus) tadpoles. II: Agriculturally relevant exposures to Roundup WeatherMax® and Vision® under laboratory conditions. Aquatic Toxicology, 154, 291-303.

Lopez-Lastra, C. & Boucias, D. G. (1994). Studies on the Cellular Reactions of Spodoptera exigua Larvae Infected with the fungus Nomuraea rileyi. Journal of invertebrate pathology, 63(1), 101-102.

Lushchak, O. V., Kubrak, O. I., Storey, J. M., Storey, K. B. & Lushchak, V. I. (2009). Low toxic herbicide Roundup induces mild oxidative stress in goldfish tissues. Chemosphere, 76(7), 932-937.

Moncada, S. & Higgs, E. A. (2006). The discovery of nitric oxide and its role in vascular biology. British journal of pharmacology, 147(S1), S193-S201.

Monserrat, J. M., Martínez, P. E., Geracitano, L. A., Lund Amado, L., Martinez Gaspar Martins, C., Lopes Leães Pinho, G., Soares Chaves, I., Ferreira-Cravo, M., Ventura-Lima, J. & Bianchini, A. (2007). Pollution biomarkers in estuarine animals: Critical review and new perspectives. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 146(1-2), 221-234.

Monte, T. C. D. C., Chometon, T. Q., Bertho, A. L., de Moura, V. S., de Vasconcellos, M. C., Garcia, J., Ferraz-Nogueira, R., Maldonado Júnior, A. & Faro, M.J. (2019). Changes in hemocytes of Biomphalaria glabrata infected with Echinostoma paraensei and exposed to glyphosate-based herbicide. Journal of invertebrate pathology, 160, 67-75.

Moscardi, F., Bueno, A. D. F., Sosa-Gómez, D. R., Roggia, S., Hoffmann-Campo, C. B., Pomari, A. F., Corso, I. C. & Yano, S. A. C. (2012). Artrópodes que atacam as folhas da soja. Soja: manejo integrado de insetos e outros artrópodes-praga, 4, 859.

Nardi, J. B. (2004). Embryonic origins of the two main classes of hemocytes - Granular cells and plasmatocytes - In Manduca sexta. Development Genes and Evolution, 214(1), 19-28.

Navarro-Martín, L., Lanctôt, C., Jackman, P., Park, B. J., Doe, K., Pauli, B. D. & Trudeau, V. L. (2014). Effects of glyphosate-based herbicides on survival, development, growth and sex ratios of wood frogs (Lithobates sylvaticus) tadpoles. I: Chronic laboratory exposures to VisionMax®. Aquatic Toxicology, 154, 278-290.

Negreiro, C. de & Andrade, F. G. de (2004). Sistema imunológico de defesa em insetos: uma abordagem em lagartas da soja, Anticarsia gemmatalis Hübner (Lepidoptera: Noctuidae), resistentes ao AgMNPV Immunology defense system in insects : an approach in velvetbean catterpillar , Anticarsia gemmatalis. SEBRAE, Paraíba 25, 293–308.

Negreiro, M. C. C. de, Carvalho, R. B. R., Andrade, F. G. de, Levy, S. M., Moscardi, F. & Falleiros, Â. M. F. (2009). Caracterização citológica dos hemócitos de Anticarsia gemmatalis (Lepidoptera, Noctuidae) em larvas resistentes ao vírus AgMNPV. Iheringia. Série Zoologia, 99(1), 66-70.

O’Donnell, V. B., Eiserich, J. P., Chumley, P. H., Jablonsky, M. J., Krishna, N. R., Kirk, M., Barnes, S., Darley-Usmar, V. M. & Freeman, B. A. (1999). Nitration of unsaturated fatty acids by nitric oxide-derived reactive nitrogen species peroxynitrite, nitrous acid, nitrogen dioxide, and nitronium ion. Chemical research in toxicology, 12(1), 83-92.

Silva Júnior, N. R., Vital, C. E., de Almeida Barros, R., Faustino, V. A., Monteiro, L. P., Barros, E., de Oliveira, E. E., de Oliveira Ramos, H. J. & de Almeida Oliveira, M.G. (2020). Intestinal proteolytic profile changes during larval development of Anticarsia gemmatalis caterpillars. Archives of insect biochemistry and physiology, 103(1), e21631.

Schneider, M. I., Sanchez, N., Pineda, S., Chi, H. & Ronco, A. (2009). Impact of glyphosate on the development, fertility and demography of Chrysoperla externa (Neuroptera: Chrysopidae): Ecological approach. Chemosphere 76, 1451–1455.

Serviço Nacional de Aprendizagem Rural - Senar (2018). Grãos: Manejo Integrado de Pragas (MIP) em soja, milho e sorgo, 2 edição. ed. Brasília.

Sharma, P. R., Sharma, O. P. & Saxena, B. P. (2008). Effect of sweet flag rhizome oil (Acorus calamus) on hemogram and ultrastructure of hemocytes of the tobacco armyworm, Spodoptera litura (Lepidoptera: Noctuidae). Micron, 39(5), 544-551.

Sharma, P. R., Sharma, O. P. & Saxena, B. P. (2003). Effect of Neem gold on haemocytes of the tobacco armyworm, Spodoptera litura (Fabricius) (Lepidoptera; Noctuidae). Current Science, 84, 690-695.

Sies, H. (1993). Strategies of antioxidant defense. EJB Reviews 1993, 101-107.

Silva, W. C., Ribeiro, J. D., Souza, H. E. M. de & Corrêa, R. da S. (2007). Atividade inseticida de Piper aduncum L. (Piperaceae) sobre Aetalion sp. (Hemiptera: Aetalionidae), praga de importância econômica no Amazonas. Acta Amazonica, 37(2), 293-298.

Sistema de Agrotóxicos Fitossanitários (Agrofit) (2015). Consulta de produtos formulados.http://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons/

Song, Z., Lin, Y., Du, F., Yin, Y. & Wang, Z. (2017). Statistical optimisation of process variables and large-scale production of Metarhizium rileyi (Ascomycetes: Hypocreales) microsclerotia in submerged fermentation. Mycology, 8(1), 39-47.

Strand, M.R. (2008). The insect cellular immune response. Insect science, 15(1), 1-14.

Tanaka, H. & Yamakawa, M., (2011). Regulation of the innate immune responses in the silkworm, Bombyx mori. Invertebrate Survival Journal, 8(1), 59-69.

Tomás-Barberán, F.A., García-Villalba, R., González-Sarrías, A., Selma, M. V. & Espín, J.C. (2014). Ellagic acid metabolism by human gut microbiota: Consistent observation of three urolithin phenotypes in intervention trials, independent of food source, age, and health status. Journal of Agricultural and Food Chemistry, 62(28), 6535-6538.

Wang, C. & St. Leger, R.J. (2006). A collagenous protective coat enables Metarhizium anisopliae to evade insect immune responses. Proceedings of the National Academy of Sciences, 103(17), 6647-6652.

World Health Organization (2004). Who Specifications and Evaluations for Public Health Pesticides: Novaluron https://www.who.int/neglected_diseases/vector_ecology/pesticide-specifications/Novaluron_evaluation_Dec_2004.pdf.

Yamanaka, N. & O’Connor, M. (2011). Nitric oxide directly regulates gene expression during Drosophila development: need some gas to drive into metamorphosis? Genes & Development, 25(14), 1459-1463.

Downloads

Published

27/05/2021

How to Cite

VISENTIN, A. P. V.; BERTHOLDO, L. R.; HAHN, R. C.; THOMAZONI, R. A. .; TOUGUINHA, L. B. A.; BRANCO, C. S.; SALVADOR, M. .; BARROS, N. M. de . Comparative effectiveness of Metarhizium rileyi, novaluron, and glyphosate on immune system, development, and redox metabolism of Anticarsia gemmatalis . Research, Society and Development, [S. l.], v. 10, n. 6, p. e19810615611, 2021. DOI: 10.33448/rsd-v10i6.15611. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/15611. Acesso em: 25 jul. 2021.

Issue

Section

Agrarian and Biological Sciences