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Environ Sci Pollut Res Int. 2021 Sep 21; doi: 10.1007/s11356-021-16352-6. Epub 2021 Sep 21.

Bioconcentration and toxicological impacts of fipronil and 2,4-D commercial formulations (single and in mixture) in the tropical fish, Danio rerio.

Environmental science and pollution research international

Natália Prudêncio Viana, Laís Conceição Menezes da Silva, Natália Portruneli, Michelly Pereira Soares, Israel Luz Cardoso, Rocío Inés Bonansea, Bianca Veloso Goulart, Cassiana Carolina Montagner, Evaldo Luiz Gaeta Espíndola, Daniel Alberto Wunderlin, Marisa Narciso Fernandes

Affiliations

  1. Programa de Pós-graduação em Ecologia e Recursos Naturais, Universidade Federal de São Carlos, Rodovia Washington Luiz, km 235, São Carlos, São Paulo, 13565-905, Brazil.
  2. Departamento de Ciências Fisiológicas, Universidade Federal de São Carlos (UFSCar), Rodovia Washington Luiz, km 235, São Carlos, SP, 13565-905, Brazil.
  3. Programa de Pós-graduação em Ciências da Engenharia Ambiental, Escola de Engenharia de São Carlos (NEEA/CRHEA/SHS), Universidade de São Paulo, Av. Trabalhador São-Carlense, 400, São Carlos, SP, 13566-590, Brazil.
  4. Programa Interinstitucional de Pós-graduação em Ciências Fisiológicas, Universidade Federal de São Carlos/Universidade Estadual de São Paulo, Rodovia Washington Luiz, km 235, São Carlos, São Paulo, 13565-905, Brazil.
  5. Faculdade de Ciências Químicas, Universidade Nacional de Córdoba, Córdoba, Argentina.
  6. Instituto de Química, Universidade de Campinas (UNICAMP), Cidade Universitária Zeferino Vaz, Campinas, SP, 13083-970, Brazil.
  7. Instituto de Ciências e Tecnologia de Alimentos de Córdoba, CONICET, Córdoba, Argentina.
  8. Programa de Pós-graduação em Ecologia e Recursos Naturais, Universidade Federal de São Carlos, Rodovia Washington Luiz, km 235, São Carlos, São Paulo, 13565-905, Brazil. [email protected].
  9. Departamento de Ciências Fisiológicas, Universidade Federal de São Carlos (UFSCar), Rodovia Washington Luiz, km 235, São Carlos, SP, 13565-905, Brazil. [email protected].

PMID: 34546525 DOI: 10.1007/s11356-021-16352-6

Abstract

The insecticide fipronil and the herbicide 2,4-D are the most applied pesticides in sugarcane crops leading to aquatic contamination. The whole-body bioconcentration of fipronil and 2,4-D, single and in mixture, was evaluated in Danio rerio after 96-h exposure. The activities of catalase (CAT) and glutathione S-transferase(GST) in whole body and in the gills and the acetylcholinesterase (AChE) in muscle were determined. The gill histopathology and the morphology of the pavement (PVC) and the mitochondria-rich(MRC) cells at gill surface were analyzed. Bioconcentration occurred after exposure to fipronil (2.69 L kg

© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Keywords: Acetylcholinesterase; Bioconcentration; Catalase; Glutathione S-transferase; Histopathology; Mitochondria-rich cells

References

  1. ABNT. Associação Brasileira de Normas Técnicas (2016) Toxicidade aguda – Método de ensaio com peixes (Cyprinidae). - PubMed
  2. Álvarez-Muñoz D, Al-Salhi R, Abdul-Sada A, González-Mazo E, Hill EM (2014) Global metabolite profiling reveals transformation pathways and novel metabolomic responses in Solea senegalensis after exposure to a non-ionic surfactant. Environ Sci Technol 48:5203–5210. https://doi.org/10.1021/es501276g - PubMed
  3. ANVISA. Consulta pública n° 164, de 03 de fevereiro de 2016, publicada no D.O.U de 12/04/2016. Disponível em: < http://portal.anvisa.gov.br/documents/10181/2719308/Relat%C3%B3rio+de+An%C3%A1lise+de+Contribui%C3%A7%C3%B5es+-+CP+164.pdf/41a725b5-37af-4a39-b809-f9f74807062c?version=1.0 > - PubMed
  4. ANVISA. Consulta pública n° 692, de 23 de agosto de 2019, publicada no D.O.U de 28/08/2019. < http://portal.anvisa.gov.br/documents/10181/5612748/CONSULTA+P%C3%9ABLICA+N+692+GGTOX.pdf/332022d9-cb9b-4ddf-bcd7-197e629636ae > - PubMed
  5. Arcaute CR, Soloneski S, Larramendy ML (2016) Toxic and genotoxic effects of the 2,4-dichlorophenoxyacetic acid (2,4-D)-based herbicide on the Neotropical fish Cnesterodon decemmaculatus. Ecotoxicol Environ Safe 128:222–229. https://doi.org/10.1016/j.ecoenv.2016.02.027 - PubMed
  6. Atamaniuk TM, Kubrak OI, Storey KB, Lushchak VI (2013) Oxidative stress as a mechanism for toxicity of 2,4-dichlorophenoxyacetic acid (2,4-D): studies with goldfish gills. Ecotoxicology 22:1498–1508. https://doi.org/10.1007/s10646-013-1136-z - PubMed
  7. Barreiros ALBS, David JM, David JP (2006) Estresse oxidativo: relação entre geração de espécies reativas e defesa do organismo. Quím Nova 29:113–123. https://doi.org/10.1590/S0100-40422006000100021 - PubMed
  8. Behmer AO, Tolosa EMC, Feritas-Neto AG (1976) Manual de técnicas para histologia normal e patológica. 1ª edição. São Paulo: EDART/USP. - PubMed
  9. Bernet D, Schmidt N, Meier W, Burkhardt-Holm P, Wahli T (1999) Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 22:25–34. https://doi.org/10.1046/j.1365-2761.1999.00134.x - PubMed
  10. Beutler E (1975) Red cell metabolism: manual of biochemical methods, 2nd edn. Grune & Stratton, New York - PubMed
  11. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram of protein utilizing the principal of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3 - PubMed
  12. Call DJ, Brooke LT, Kent RJ, Knuth ML, Anderson C, Moriarity C (1983) Toxicity, bioconcentration, and metabolism of the herbicide propanil (3',4'- Dichloropropionanilide) in freshwater fish. Arch Environ Contam Toxicol 12:352–358. https://doi.org/10.1007/bf01059578 - PubMed
  13. CETESB (2018) Qualidade das águas interiores no estado de São Paulo, 2017. - PubMed
  14. Clasen B, Loro VL, Cattaneo R, Moraes B, Lópes T, Avila LA, Zanella R, Reimche GB, Baldisserotto B (2012) Effects of the commercial formulation containing fipronil on the non-target organism Cyprinus carpio: implications for rice-fish cultivation. Ecotoxicol Environ Safe 77:45–51. https://doi.org/10.1016/j.ecoenv.2011.10.001 - PubMed
  15. Coelho S, Oliveira R, Pereira S, Musso C, Domingues I, Bhujel RC, Soares AMVM, Nogueira AJA (2011) Assessing lethal and sub-lethal effects of trichlorfon on different trophic levels. Aquat Toxicol 103:191–198. https://doi.org/10.1016/j.aquatox.2011.03.003 - PubMed
  16. Dallarés S, Dourado P, Sanahuja I, Solovyev M, Gisbert E, Montemurro N, Torreblanca A, Blázquez M, Solé M (2020) Multibiomarker approach to fipronil exposure in the fish Dicentrarchus labrax under two temperature regimes. Aquat Toxicol 219:105378. https://doi.org/10.1016/j.aquatox.2019.105378   - PubMed
  17. Deiú AS, Miglioranza KSB, Ondarza PM, Torre FR (2021) Exposure to environmental concentrations of fipronil induces biochemical changes on a neotropical freshwater fish. Environ Sci Pollut Res. 28:43872–43884. https://doi.org/10.1007/s11356-021-13786-w - PubMed
  18. Dutta HM, Munshi JSD, Roy PK, Singh NK, Motz L, Adhikari S (1997) Effects of diazinon on bluegill sunfish, Lepomis macrochirus, gills: scanning electron microscope observations. Exp Biol Online 2:1–11. https://doi.org/10.1007/s00898-997-0017-4 - PubMed
  19. Ellman GL, Courtney D, Andres VJ, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol. 7:88–95. https://doi.org/10.1016/0006-2952(61)90145-9 - PubMed
  20. El-Murr A, Imam TS, Hakim Y, Ghonimi WAM (2015) Histopathological, immunological, hematological and biochemical effects of fipronil on Nile tilapia (Oreochromis niloticus). J Veterinar Sci Technol 6(5):1000252. https://doi.org/10.4172/2157-7579.1000252 - PubMed
  21. European Food Safety Authority (2014) Conclusion on the peer review of the pesticide risk assessment of the active substance 2,4-D. EFSA 12(9):3812 - PubMed
  22. Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gills: dominant site for gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogen wastes. Physiol Rev 85:97–177 - PubMed
  23. Fernandes MN (2019) Gills. Respiration and ionic osmoregulation. In: Kirschbaum F, Formicki K (eds) The Histology of Fish. CRC Press, Boca Raton - PubMed
  24. Fernandes MN, Moron SE (2020) Breathing and respiratory adaptations. In: Baldisserotto B, Urbinati EC, Cyrino JEP (eds) Biology and Physiology of Freshwater Neotropical Fish. Academic Press, London, pp 217–250 - PubMed
  25. Fernandes MN, Moron SE, Sakuragui MM (2007) Gill morphological adjustments to environment and the gas exchange function. In: Fernandes MN, Glass ML, Rantin FT, Kapoor BG (eds) Fish respiration and environment. Science publishers, Enfield, pp 93–120 - PubMed
  26. Gaaied S, Oliveira M, Domingues I, Banni M (2019) 2,4-Dichlorophenoxyacetic acid herbicide effects on zebrafish larvae: development, neurotransmission, and behavior as sensitive endpoints. Environ Sci Pollut Res 27(4):3686–3696. https://doi.org/10.1007/s11356-019-04488-5 - PubMed
  27. Ghaffar A, Hussain R, Abbas G, Kalim M, Khan A, Ferrando S, Gallus L, Ahmed Z (2018) Fipronil (Phenylpyrazole) induces hemato-biochemical, histological and genetic damage at low doses in common carp, Cyprinus carpio (Linnaeus, 1758). Ecotoxicology 27:1261–1271. https://doi.org/10.1007/s10646-018-1979-4 - PubMed
  28. Gottardi M, Birch MR, Dalhoff K, Cedergreen N (2017) The effects of epoxiconazole and Α-cypermethrin on Daphnia magna growth, reproduction, and offspring size. Environ Toxicol Chem 36:2155–2166. https://doi.org/10.1002/etc.3752 - PubMed
  29. Gunasekara AS, Truong T, Goh KS, Spurlock F, Tjeerdema RS (2007) Environmental fate and toxicology of fipronil. J Pest Sci 32(3):189–199. https://doi.org/10.1584/jpestics.R07-02 - PubMed
  30. Gupta RC, Anandón A (2018) Fipronil. In: Gupta R (ed) Veterinary toxicology: basic and clinical principles. Academic Press, Cambridge, pp 533–538 - PubMed
  31. Habig WH, Jakoby WB (1981) Assays for differentiation of glutathione-S-transferases. Method Enzymol. 77:398–405. https://doi.org/10.1016/S0076-6879(81)77053-8 - PubMed
  32. Huber PC, Almeida WP, Fátima ÂD (2008) Glutationa e enzimas relacionadas: papel biológico e importância em processos patológicos. Quím Nova 31:1170–1179. https://doi.org/10.1590/S0100-40422008000500046 - PubMed
  33. Hwang P-P, Lee T-H, Lin L-Y(2011) Ion regulation in fish gills: recent progress in the cellular and molecular mechanisms. Am J Physiol Regul Integr Comp Physiol 301:R28–R47. https://doi.org/10.1152/ajpregu.00047.2011 - PubMed
  34. Islam F, Wang J, Farooq MA, Khan MSS, Xu L, Zhu J, Zhao M, Muños S, Li QX, Weijun Z (2018) Potential impact of the herbicide 2,4-dichlorophenoxyacetic acid on human and ecosystems. Environ Int 111:332–351. https://doi.org/10.1016/j.envint.2017.10.020 - PubMed
  35. Jonsson CM, Moura MAM, Ferracini VL, Paraíba LC, Assalin MR, Queiroz SCN (2019) Bioconcentrations of herbicides used in sugarcane crops in tilapia (Oreochromis niloticus) and the risk for human consumption. Heliyon 5(8):e02237. https://doi.org/10.1016/j.heliyon.2019.e02237 - PubMed
  36. Konwick BJ, Garrison AW, Black MC, Avants JK, Fisk AT (2006) Bioaccumulation, biotransformation, and metabolite formation of fipronil and chiral legacy pesticides in rainbow trout. Environ Sci Technol 40:2930–2936. https://doi.org/10.1021/es0600678 - PubMed
  37. Lewis L, Kwong RWM (2018) Zebrafish as a model system for investigating the compensatory regulation of ionic balance during metabolic acidosis. Int J Mol Sci 19:1087. https://doi.org/10.3390/ijms19041087 - PubMed
  38. Li K, Wu J-Q, Jiang L-L, Shen L-Z, Li J-Y, He Z-H, Wei P, Lv Z, He M-F(2017) Developmental toxicity of 2,4-dichlorophenoxyacetic acid in zebrafish embryos. Chemosphere 171:40–48. https://doi.org/10.1016/j.chemosphere.2016.12.032 - PubMed
  39. Li H, You J, Wang W-X(2018)Multi-compartmental toxicokinetic modeling of fipronil in tilapia: accumulation, biotransformation and elimination. J Hazard Mater 360:420–427. https://doi.org/10.1016/j.jhazmat.2018.07.85 - PubMed
  40. Lins JAPN, Kirschnik PG, Queiroz VS, Cirio SM (2010) Use of fish as biomarkers for monitoring aquatic environment. Rev. Acad., Ciênc Agrár Ambient 8:469–484. https://doi.org/10.7213/cienciaanimal.v8i4.11018 - PubMed
  41. Lopes FM, Caldas SS, Primel EG, Rosa CE (2017) Glyphosate adversely affects Danio rerio males: acetylcholinesterase modulation and oxidative stress. Zebrafish 14:97–105. https://doi.org/10.1089/zeb.2016.1341 - PubMed
  42. Martinez-Sales M, Garcia-Ximenez F, Espinos FJ (2015) Zebrafish as a possible bioindicator of organic pollutants with effects on reproduction in drinking waters. J Environ Sci 33:254–260. https://doi.org/10.1016/j.jes.2014.11.012 - PubMed
  43. Mela M, Guiloski IC, Doria HB, Randi MAF, Ribeiro CAO, Pereira L, Maraschi AC, Prodocimo V, Freire CA, Assis HCS (2013) Effects of the herbicide atrazine in neotropical catfish (Rhamdia quelen). Ecotoxicol Environ Safe 93:13–21. https://doi.org/10.1016/j.ecoenv.2013.03.026 - PubMed
  44. Moreira RA, Daam MA, Vieir BH, Sanches ALM, Reghini MV, Mansano AS, Freitas EC, Espindola ELG, Rocha O (2017) Toxicity of abamectin and difenoconazole mixtures to a Neotropical cladoceran after simulated run-off and spray drift exposure. Aquat Toxicol 185:58–66. https://doi.org/10.1016/j.aquatox.2017.02.001 - PubMed
  45. Moreira RA, Araújo CVM, Pinto TJS, Silva LCM, Goulart BV, Viana NP, Montagner CC, Fernandes MN, Espindola ELG (2021) Fipronil and 2,4-D effects on tropical fish: could avoidance response be explained by changes in swimming behavior and neurotransmission impairments? Chemosphere 263:127972. https://doi.org/10.1016/j.chemosphere.2020.127972 - PubMed
  46. Moron SE, Oba ET, Andrade CA, Fernandes MN (2003) Chloride cell responses to ion challenge in two tropical freshwater fish, the erythrinids Hoplias malabaricus and Hoplerythrinus unitaeniatus. J Exp Zool A 298(2):93–104. https://doi.org/10.1002/jez.a.10259 - PubMed
  47. Nakagome FK, Noldin JA, Resgalla C Jr (2006) Toxicidade aguda de alguns herbicidas e inseticidas utilizados em lavouras de arroz irrigado sobre o peixe Danio rerio. Pesticidas: Rev. Ecoloxicol Meio Amb 16:93–100. https://doi.org/10.5380/pes.v17i0.9186 - PubMed
  48. Navarro CDC, Martinez CBR (2014) Effects of the surfactant polyoxyethylene amine (POEA) on genotoxic, biochemical, and physiological parameters of the freshwater teleost Prochilodus lineatus. Comp Biochem Physiol C Toxicol.Pharmacol 165:83–90. https://doi.org/10.1016/j.cbpc.2014.06.003 - PubMed
  49. Opperhuizen A (1991) Bioconcentration and bioaccumulation: is a distinction necessary. In: Naget R, Loskill R (eds) Bioaccumulation in aquatic systems. VCH Publishers, Weinheim, pp 67–80 - PubMed
  50. Oruc EÖ, Üner N (1999) Effects of 2,4-diamin on some parameters of protein and carbohydrate metabolisms in the serum, muscle and liver of Cyprinus carpio. Environ Pollut 105:267–272. https://doi.org/10.1016/S0269-7491(98)00206-1 - PubMed
  51. Paulino MG, Souza NES, Fernandes MN (2012) Subchronic exposure to atrazine induces biochemical and histopathological changes in the gills of a Neotropical freshwater fish, Prochilodus lineatus. Ecotoxicol Environ Safe 80:6–13. https://doi.org/10.1016/j.ecoenv.2012.02.001 - PubMed
  52. Perry SF, Goss GG, Laurent P (1992) The interrelationships between gill chloride cell morphology and ionic uptake in four freshwater teleosts. Can J Zool 70:1775–1786. https://doi.org/10.1139/z92-245 - PubMed
  53. Pinto TJS, Moreira RA, Silva LCM, Yoshii MPC, Goulart BV, Fraga PD, Rolim VLS, Montagner CC, Daam MA, Espindola ELG (2021) Toxicity of fipronil and 2,4-D formulations (alone and in a mixture) to the tropical amphipod Hyalella meinerti. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-021-13296-9 - PubMed
  54. Poleksic V, Mitrovic-Tutundzic V (1994) Fish gills as a monitor of sublethal and chronic effects of pollution. In: Müller R, Lloyd R (eds) Sublethal and Chronic effects of pollutants on freshwater fish. Fishing News Books, Oxford, pp 339–352 - PubMed
  55. Portruneli N (2020) Efeito da exposição aguda do inseticida Regent 800 WG (Fipronil), do herbicida DMA 806 BR (2,4-D) e mistura de ambos em curimbatá, Prochilodus lineatus (Teleósteo, Prochilodontidae). MSc Thesis. Universidade Federal de São Carlos, São Paulo, Brazil, 40 pp. - PubMed
  56. Pottel J, Armstrong D, Zou L, Fekete A, Huang X-P, Torosyan H, Bednarczyk D, Whitebread S, Bhhatarai B, Liang G, Jin H, Ghaemi SN, Slocum S, Lukacs CV, Irwin JJ, Berg EL, Giacomini KM, Roth BL, Shoichet BK, Urban L (2020) The activities of drug inactive ingredients on biological targets. Science 369:403–413. https://doi.org/10.1126/science.aaz9906 - PubMed
  57. Qureshi IZ, Bibi A, Shahid S, Ghazanfar M (2016) Exposure to sub-acute doses of fipronil and buprofezin in combination or alone induces biochemical, hematological, histopathological and genotoxic damage in common carp (Cyprinus carpio L.). Aquat Toxicol 179:103–114. https://doi.org/10.1016/j.aquatox.2016.08.012 - PubMed
  58. R DEVELOPMENT CORE TEAM (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna - PubMed
  59. Rao JV (2006) Toxic effects of novel organophosphorus insecticide (RPR-V) on certain biochemical parameters of euryhaline fish, Oreochromis mossambicus. Pestic Biochem Physiol 86:8–84. https://doi.org/10.1016/j.pestbp.2006.01.008 - PubMed
  60. Reynaud S, Worms IAM, Veyrenc S, Portier J, Maitre A, Miaud C, Raveton M (2012) Toxicokinetic of benzo[a]pyrene and fipronil in female green frogs (Pelophylax kl. esculentus). Environ Pollut 161:206–214. https://doi.org/10.1016/j.envpol.2011.10.029 - PubMed
  61. Rosetto R, Santiago AD (2021). Plantio da cana-de-açúcar. Agência Embrapa de Informação Tecnológica - Plantio. https://www.agencia.cnptia.embrapa.br/gestor/cana-de-acucar/arvore/CONTAG01_33_711200516717.html . - PubMed
  62. Sanches ALM, Vieira BH, Reghini MV, Moreira RA, Freitas EC, Espindola ELG, Daam MA (2017) Single and mixture toxicity of abamectin and difenoconazole to adult zebrafish (Danio rerio). Chemosphere 188:582–587. https://doi.org/10.1016/j.chemosphere.2017.09.027 - PubMed
  63. Serra-Compte A, Álvarez-Muñoz D, Rodríguez-Mozaz S (2017)Multi-residue method for the determination of antibiotics and some of their metabolites in seafood. Food Chem Toxicol 104:3–13. https://doi.org/10.1016/j.fct.2016.11.031 - PubMed
  64. Simon-Delso N, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Chagnon M, Downs C, Furlan L, Gibbons DW, Giorio C, Girolami V, Goulson D, Kreutzweiser DP, Krupke CH, Liess M, Long E, McField M, Mineau P, Mitchell EAD, Morrissey CA et al (2015) Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites. Environ Sci Pollut Res 22:5–34. https://doi.org/10.1007/s11356-014-3470-y - PubMed
  65. Smejtek P, Paulis-Illangasekare M (1979) Modification of ion transport in lipid bilayer membranes in the presence of 2,4-dichlorophenoxyacetic acid. Biophys J 26:441–466. https://doi.org/10.1016/S0006-3495(79)85265-0 - PubMed
  66. Van Der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149. https://doi.org/10.1016/s1382-6689(02)00126-6 - PubMed
  67. Wang C, Qian Y, Zhang X, Chen F, Zhang Q, Li Z, Zhao MA (2016) Metabolomic study of fipronil for the anxiety-like behavior in zebrafish larvae at environmentally relevant levels. Environ Pollut 211:252–258. https://doi.org/10.1016/j.envpol.2016.01.016 - PubMed
  68. Wu H, Gao C, Guo Y, Zhang Y, Zhang J, Ma E (2014) Acute toxicity and sublethal effects of fipronil on detoxification enzymes in juvenile zebrafish (Danio rerio). Pestic Biochem Physiol 115:9–14. https://doi.org/10.1016/j.pestbp.2014.07.010 - PubMed
  69. Zhang J, Shen H, Wang X, Wu J, Xue Y (2004) Effects of chronic exposure of 2,4-dichlorophenol on the antioxidant system in liver of freshwater fish Carassius auratus. Chemosphere 55:167–174 - PubMed

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