Exposição crônica ao inseticida Piretróide Deltametrina: Implicações hepáticas e energéticas em morcego frugívoro artibeus lituratus

Autores

  • Renata Maria Pereira de Freitas Universidade Federal de Goiás
  • Ariane Maria Rizzoli Moreno Universidade Federal de Viçosa
  • Ana Carolina Neves Universidade Federal de Viçosa
  • Mariana Moraes de Castro Universidade Federal de Viçosa https://orcid.org/0000-0002-7416-3529
  • Mariella Bontempo Freita Universidade Federal de Viçosa
  • Jerusa Maria de Oliveira Universidade Federal de Alagoas

DOI:

https://doi.org/10.37002/biodiversidadebrasileira.v13i2.2370

Palavras-chave:

Metabolismo Energético, Glicose, Estresse oxidativo

Resumo

Inseticidas piretroides foram incorporados no mercado como alternativa menos tóxica para animais não alvo. No entanto, a deltametrina, um inseticida dessa classe, é conhecida por causar toxicidade em exposição aguda e crônica em diferentes animais. Os morcegos são animais não alvo que estão constantemente expostos a pesticidas durante o forrageio e isso pode impactar sua sobrevivência. Objetivou-se avaliar o efeito da exposição crônica à deltametrina no estado redox e metabolismo energético de morcegos frugívoros da espécie Artibeus lituratus. Para isso os morcegos foram coletados (n=12) e separados em: grupo controle (Controle; n=6), alimentado com frutos não tratados; grupo deltametrina (DM; n = 6), alimentado com frutos tratados com deltametrina na concentração 1.00 mL/L mais espalhante adesivo (0,015 g/L). Após um período de exposição crônica (35 dias), o estado redox do fígado e rim, as alterações histológicas no fígado, a concentração de glicose e as reservas energéticas foram analisados. A exposição a doses comerciais de deltamentrina induziu estresse oxidativo e alterações morfológicas no fígado, além de causar hipoglicemia e reduzir as reservas energéticas dos morcegos. Considerando que os morcegos estão expostos naturalmente aos pesticidas durante o forrageio, o impacto dessa exposição pode alterar as reservas energéticas e induzir alterações no funcionamento normal do fígado, prejudicando a sobrevivência desses animais e, consequentemente, os serviços ecossistêmicos prestados por eles.

Referências

Aebi, H. (1984). [13] Catalase in vitro. In Methods in enzymology (Vol. 105, pp. 121-126). Academic press.

Agrawal, A. N. J. U., & Sharma, B. (2010). Pesticides induced oxidative stress in mammalian systems. Int J Biol Med Res, 1(3), 90-104.

Amaral, T. S., Carvalho, T. F., Silva, M. C., Barros, M. S., Picanço, M. C., Neves, C. A., & Freitas, M. B. (2012). Short-term effects of a spinosyn's family insecticide on energy metabolism and liver morphology in frugivorous bats Artibeus lituratus (Olfers, 1818). Brazilian Journal of Biology, 72, 299-304.

Amin, K. A., & Hashem, K. S. (2012). Deltamethrin-induced oxidative stress and biochemical changes in tissues and blood of catfish (Clarias gariepinus): antioxidant defense and role of alpha-tocopherol. BMC veterinary research, 8(1), 1-8.

Barbosa, K. B. F., Costa, N. M. B., Alfenas, R. D. C. G., De Paula, S. O., Minim, V. P. R., & Bressan, J. (2010). Estresse oxidativo: conceito, implicações e fatores modulatórios. Revista de nutrição, 23, 629-643.

Ben-Hamo, M., Muñoz-Garcia, A., & Pinshow, B. (2012). Respostas fisiológicas ao jejum em morcegos. Em Fisiologia comparativa do jejum, fome e limitação alimentar (pp. 257-275). Springer, Berlim, Heidelberg.

Bennett, B. S., & Thies, M. L. (2007). Organochlorine pesticide residues in guano of Brazilian free-tailed bats, Tadarida brasiliensis Saint-Hilaire, from East Texas. Bulletin of environmental contamination and toxicology, 78(3), 191-194.

Bianconi, G. V., Mikich, S. B., Teixeira, S. D., & Maia, B. H. L. (2007). Attraction of fruit‐eating bats with essential oils of fruits: A potential tool for forest restoration. Biotropica, 39(1), 136-140.

Brinati, A., Oliveira, J. M., Oliveira, V. S., Barros, M. S., Carvalho, B. M., Oliveira, L. S., ... & Freitas, M. B. (2016). Low, chronic exposure to endosulfan induces bioaccumulation and decreased carcass total fatty acids in neotropical fruit bats. Bulletin of Environmental Contamination and Toxicology, 97(5), 626-631.

Buege, J. A., & Aust, S. D. (1978). [30] Microsomal lipid peroxidation. In Methods in enzymology (Vol. 52, pp. 302-310). Academic press.

Chargui, I., Grissa, I., Bensassi, F., Hrira, M. Y., Haouem, S., Haouas, Z., & Bencheikh, H. (2012). Oxidative stress, biochemical and histopathological alterations in the liver and kidney of female rats exposed to low doses of deltamethrin (DM): a molecular assessment. Biomedical and Environmental Sciences, 25(6), 672-683.

Chauhan, L. K., Kumar, M., Paul, B. N., Goel, S. K., & Gupta, S. K. (2007). Cytogenetic effects of commercial formulations of deltamethrin and/or isoproturon on human peripheral lymphocytes and mouse bone marrow cells. Environmental and Molecular Mutagenesis, 48(8), 636-643.

Chionh, Y. T., Cui, J., Koh, J., Mendenhall, I. H., Ng, J. H., Low, D., ... & Wang, L. F. (2019). High basal heat-shock protein expression in bats confers resistance to cellular heat/oxidative stress. Cell Stress and Chaperones, 24(4), 835-849.

Cummins, I., Dixon, D. P., Freitag-Pohl, S., Skipsey, M., & Edwards, R. (2011). Multiple roles for plant glutathione transferases in xenobiotic detoxification. Drug metabolism reviews, 43(2), 266-280.

Cutler, R. G. (1985). Peroxide-producing potential of tissues: inverse correlation with longevity of mammalian species. Proceedings of the National Academy of Sciences, 82(14), 4798-4802.

Davies, T. G. E., Field, L. M., & Williamson, M. S. (2012). The re‐emergence of the bed bug as a nuisance pest: implications of resistance to the pyrethroid insecticides. Medical and veterinary entomology, 26(3), 241-254.

de Oliveira, J. M., de Almeida Lima, G. D., Destro, A. L. F., Condessa, S., Zuanon, J. A. S., Freitas, M. B., & de Oliveira, L. L. (2021). Short-term intake of deltamethrin-contaminated fruit, even at low concentrations, induces testicular damage in fruit-eating bats (Artibeus lituratus). Chemosphere, 278, 130423.

de Souza, M. B., de Souza Santos, L. R., Borges, R. E., Nunes, H. F., Vieira, T. B., Pacheco, S. M., & de Melo e Silva, D. (2020). Current status of ecotoxicological studies of bats in Brazil. Bulletin of environmental contamination and toxicology, 104(4), 393-399.

de Souza, T. C., da Silva, S. L. R., Marcon, J. L., & Waichman, A. V. (2020). Acute toxicity of deltamethrin to Amazonian freshwater fish. Toxicology and Environmental Health Sciences, 12(2), 149-155.

Desneux, N., Decourtye, A., & Delpuech, J. M. (2007). The sublethal effects of pesticides on beneficial arthropods. Annual review of entomology, 52(1), 81-106.

Dieterich, S., Bieligk, U., Beulich, K., Hasenfuss, G., & Prestle, J. (2000). Gene expression of antioxidative enzymes in the human heart: increased expression of catalase in the end-stage failing heart. Circulation, 101(1), 33-39.

Dietz, S., De Roman, M., Lauck-Birkel, S., Maus, C., Neumann, P., & Fischer, R. (2009). Ecotoxicological and environmental profile of the insecticide delta methrin. In Pyrethroid Scientific Forum 2009 (p. 211).

Dubey, N., Khan, A. M., & Raina, R. (2013). Sub-acute deltamethrin and fluoride toxicity induced hepatic oxidative stress and biochemical alterations in rats. Bulletin of environmental contamination and toxicology, 91(3), 334-338.

Folch, J., Lees, M., & Sloane Stanley, G. H. (1957). A simple method for the isolation and purification of total lipids from animal tissues. J biol Chem, 226(1), 497-509.

Freitas, M. B., Passos, C. B., Vasconcelos, R. B., & Pinheiro, E. C. (2005). Effects of short-term fasting on energy reserves of vampire bats (Desmodus rotundus). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 140(1), 59-62.

Freitas, M. B., Welker, A. F., & Pinheiro, E. C. (2006). Efeitos do jejum e da variação sazonal sobre as reservas lipídicas de morcegos hematófagos (Chiroptera: Phyllostomidae). Brazilian Journal of Biology, 66, 1051-1055.

Freitas, R. M., Linhares, B. S., Oliveira, J. M., Leite, J. P. V., da Matta, S. L. P., Gonçalves, R. V., & Freitas, M. B. (2021). Tebuconazole-induced toxicity and the protective effect of Ficus carica extract in Neotropical fruit-eating bats. Chemosphere, 275, 129985.

Frisard, M., & Ravussin, E. (2006). Energy metabolism and oxidative stress. endocrine, 29(1), 27-32.

Froese, J. M., Smits, J. E., Forsyth, D. J., & Wickstrom, M. L. (2009). Toxicity and immune system effects of dietary deltamethrin exposure in tiger salamanders (Ambystoma tigrinum). Journal of Toxicology and Environmental Health, Part A, 72(8), 518-526.

Guardiola, F. A., Gónzalez-Párraga, P., Meseguer, J., Cuesta, A., & Esteban, M. A. (2014). Modulatory effects of deltamethrin-exposure on the immune status, metabolism and oxidative stress in gilthead seabream (Sparus aurata L.). Fish & Shellfish Immunology, 36(1), 120-129.

Habig, W. H., Pabst, M. J., & Jakoby, W. B. (1974). Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. Journal of biological Chemistry, 249(22), 7130-7139.

Hayes, J. D., Flanagan, J. U., & Jowsey, I. R. (2005). Glutathione transferases. Annual review of pharmacology and toxicology, 45(1), 51-88.

Hermes-Lima, M. (2004). Oxygen in biology and biochemistry: role of free radicals. Functional metabolism: regulation and adaptation, 1, 319-66.

Jones, G., Jacobs, D. S., Kunz, T. H., Willig, M. R., & Racey, P. A. (2009). Carpe noctem: the importance of bats as bioindicators. Endangered species research, 8(1-2), 93-115.

Ku, H. H., Brunk, U. T., & Sohal, R. S. (1993). Relationship between mitochondrial superoxide and hydrogen peroxide production and longevity of mammalian species. Free Radical Biology and Medicine, 15(6), 621-627.

Li, M., Liu, X., & Feng, X. (2019). Cardiovascular toxicity and anxiety-like behavior induced by deltamethrin in zebrafish (Danio rerio) larvae. Chemosphere, 219, 155-164.

Liao, C. H., He, X. J., Wang, Z. L., Barron, A. B., Zhang, B., Zeng, Z. J., & Wu, X. B. (2018). Short-term exposure to lambda-cyhalothrin negatively affects the survival and memory-related characteristics of worker bees Apis mellifera. Archives of environmental contamination and toxicology, 75(1), 59-65.

Limón-Pacheco, J., & Gonsebatt, M. E. (2009). The role of antioxidants and antioxidant-related enzymes in protective responses to environmentally induced oxidative stress. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 674(1-2), 137-147.

Lowry, O. H. (1951). Protein measurement with the Folin phenol reagent. J biol Chem, 193, 265-275.

Lu, Q., Sun, Y., Ares, I., Anadón, A., Martínez, M., Martínez-Larrañaga, M. R., ... & Martínez, M. A. (2019). Deltamethrin toxicity: A review of oxidative stress and metabolism. Environmental research, 170, 260-281.

Lushchak, V. I., & Storey, K. B. (2021). Oxidative stress concept updated: Definitions, classifications, and regulatory pathways implicated. EXCLI journal, 20, 956.

Magalhães, J. P. D., Costa, J., & Church, G. M. (2007). An analysis of the relationship between metabolism, developmental schedules, and longevity using phylogenetic independent contrasts. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 62(2), 149-160.

Martins, M. P. V.; Torres, J. M.; Dos Anjos, E. A. C. (2014). Dieta de morcegos filostomídeos (Mammalia, Chiroptera, (Phyllostomidae) em fragmento urbano do Instituto São Vicente, Campo Grande, Mato Grosso do Sul. Papeis Avulsos de Zoologia, v. 54, n. 20, p. 665–670.

Melo, F. P., Rodriguez‐Herrera, B., Chazdon, R. L., Medellin, R. A., & Ceballos, G. G. (2009). Small tent‐roosting bats promote dispersal of large‐seeded plants in a Neotropical forest. Biotropica, 41(6), 737-743.

Munshi-South, J., & Wilkinson, G. S. (2010). Bats and birds: exceptional longevity despite high metabolic rates. Ageing research reviews, 9(1), 12-19.

Nunes, H., Rocha, F. L., & Cordeiro-Estrela, P. (2017). Bats in urban areas of Brazil: roosts, food resources and parasites in disturbed environments. Urban ecosystems, 20(4), 953-969.

Oliveira, J. M., Condessa, S. S., Destro, A. L. F., Lima, G. D. A., Cupertino, M. C., Cardoso, S. A., Freitas, M. B., & Oliveira, L. L. (2022). Morphophysiological alterations in fruit-eating bats after oral exposure to deltamethrin. International Journal of Experimental Pathology, 00:1–12.

Oliveira, J. M., Destro, A. L. F., Freitas, M. B., & Oliveira, L. L. (2020). How do pesticides affect bats?–A brief review of recent publications. Brazilian Journal of Biology, 81, 499-507.

Oliveira, J. M., Losano, N. F., Condessa, S. S., de Freitas, R. M. P., Cardoso, S. A., Freitas, M. B., & de Oliveira, L. L. (2018). Exposure to deltamethrin induces oxidative stress and decreases of energy reserve in tissues of the Neotropical fruit-eating bat Artibeus lituratus. Ecotoxicology and environmental safety, 148, 684-692.

Oliveira, J. M., Brinati, A., Miranda, L. D. L., Morais, D. B., Zanuncio, J. C., Gonçalves, R. V., ... & Freitas, M. B. (2017). Exposure to the insecticide endosulfan induces liver morphology alterations and oxidative stress in fruit‐eating bats (Artibeus lituratus). International Journal of Experimental Pathology, 98(1), 17-25.

Romero, A., Ares, I., Ramos, E., Castellano, V., Martinez, M., Martínez-Larrañaga, M. R., ... & Martínez, M. A. (2015). Evidence for dose-additive effects of a type II pyrethroid mixture. In vitro assessment. Environmental Research, 138, 58-66.

Royauté, R., Buddle, C. M., & Vincent, C. (2015). Under the influence: sublethal exposure to an insecticide affects personality expression in a jumping spider. Functional Ecology, 29(7), 962-970.

Santos, M. A., Rodrigues, M. V., Áreas, M. A., & Reyes, F. G. (2011). Deltamethrin and Permethrin in the liver and heart of Wistar rats submitted to oral subchronic exposure. Journal of the Brazilian Chemical Society, 22, 891-896.

Siwicki, A. K., Terech‐Majewska, E., Grudniewska, J., Malaczewska, J., Kazun, K., & Lepa, A. (2010). Influence of deltamethrin on nonspecific cellular and humoral defense mechanisms in rainbow trout (Oncorhynchus mykiss). Environmental Toxicology and Chemistry: An International Journal, 29(3), 489-491.

Sjörgren, B., Noerdenskjold, T., Holmgeen, H. And Mollerstrom, J., 1938. Beitrag zur kenntnis der leberrhythmik (glykogen, phosphor und calcium in der kaninchenleber). Pflügers Archiv, p. 240-247.

Stahlschmidt, P., Hahn, M., & Brühl, C. A. (2017). Nocturnal risks-high bat activity in the agricultural landscape indicates potential pesticide exposure. Frontiers in Environmental Science, 5, 62.

Tanikawa, K., & Torimura, T. (2006). Studies on oxidative stress in liver diseases: important future trends in liver research. Medical molecular morphology, 39(1), 22-27.

Torquetti, C. G., Guimarães, A. T. B., & Soto-Blanco, B. (2021). Exposure to pesticides in bats. Science of the Total Environment, 755, 142509.

Vizotto, L. D., & Taddei, V. A. (1973). Chave para determinação de quirópteros brasileiros.

Yang, C., Lim, W., & Song, G. (2020). Mediation of oxidative stress toxicity induced by pyrethroid pesticides in fish. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 234, 108758.

Yildirim, M. Z., Benlı, A. Ç. K., Selvı, M., Özkul, A., Erkoç, F., & Koçak, O. (2006). Acute toxicity, behavioral changes, and histopathological effects of deltamethrin on tissues (gills, liver, brain, spleen, kidney, muscle, skin) of Nile tilapia (Oreochromis niloticus L.) fingerlings. Environmental Toxicology: An International Journal, 21(6), 614-620.

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Publicado

02/08/2023