Acute effect of carbofuran in Chirostoma humboldtianum juveniles (Atheriniformes: Atherinopsidae)
Keywords:
Carbofuran, lipoperoxidation, neurotoxicity, stress oxidativeAbstract
Background: Chirostoma populations have diminished because of loss of their habitat, introduction of exotic species and pollution. Chirostoma humboldtianum (Valenciennes, 1835) was recorded in Mexico basin, for last time in 1957. Carbofuran is a carbamic inseticide, broad spectrum systemic; its use is prohibited in many countries. However, in Mexico, it is widely used and its effects has not been evaluated in endemic fish. Goals: Evaluate acute effect of Carbofuran® in juveniles of Chirostoma humboldtianum (Valenciennes, 1835) through neurotoxicity biomarkersf and oxidative stress on brain, liver, gills and muscles. Methods: Effect Carbofuran (0.0, 0.025, 0.05, 0.1, 0.2, 0.4 mg/L) was evaluated in a static essay during 96 h without renewal water on seven-months old juveniles. Fish were obtained by in vitro fertilization, from breeders in captivity, morphologically and genetically certified. Results: CL50 was 0.077 mg/L at 96 h (0.028 – 0.118 mg/L -1, α = 0.05). Acetylcholinesterase activity (AChE) is inhibited in gills and liver. Lipoperoxidation level (LPO) was significantly higher in gills than liver and muscles (p < 0.05). Superoxide dismutase (SOD) and glutathione peroxidase (GPx) enzymes present a similar pattern in gills and liver. Conclusions: carbofuran causes neurotoxic and oxidative damage even at lower concentrations than those reported in other fish species.
Downloads
References
Addinsoft. 2014. XLSTAT. Statistical Software. BroNY, USA: Addinsoft, Inc.
Ahmad, I., T. Hamid, M. Fatima, H. S. Chand, S. K. Jain, M. Athar & S. Raisuddin. 2000. Induction of hepatic antioxidants in freshwater catfish (Channa punctatus Bloch) is a biomarker of paper mill effluent exposure. Biochemica et Biophysica Acta 1523 (1):37-48. DOI: 10.1016/S0304-4165(00)00098-2
Altamirano-Lozano, M. A., D. Toledo-Herrera, A. Rodríguez C. & G. Figueroa-Lucero. 2005. Chirostoma humboldtianum como modelo in Vitro para el estudio de embriotoxicidad de metales pesados. I. Cloruro de Cadmio. Revista Internacional de Contaminación Ambiental (21): 71-77. DOI:10.20937/RIC.2018.34.04.13
Amoatey, P. & M. S. Baawain. 2019. Effects of pollution on freshwater aquatic organisms. Water environment Reserch 91: 1272-1287. DOI:10.1002/wer.1221
Arcagni, M., A. Rizzo, R. Juncos, M. Pvlin, L. M. Campbell, M. A. Arribére, M. Horvat & S. Ribeiro-Guevara. 2017. Mercury and selenium in the food web of Lake Nahuel Huapi, Patagonia, Argentina. Chemosphere 166: 163-173.
Atli, G.& M. Canli. 2010. Response of antioxidant system of freshwater fish Oreochromis niloticus to acute and chronic metal (Cd, Cu, Cr, Zn, Fe) exposures. Ecotoxicology and Environmental Safety 73 (8): 1884-1889. DOI: 10.1016/j.ecoenv.2010.09.005
Avci, A., M. Kaçmaz & I. Durak. 2005. Peroxidation in muscle and liver tissues from fish in a contaminated river due to a petroleum refinery industry. Ecotoxicology and Environmental Safety 60 (1): 101-105. DOI: 10.1016/j.ecoenv.2003.10.003
Barbieri, E., K. Ruíz-Hidalgo, K. F. O. Rezende, A. F. G. Leonardo. & F. P. Sabino. 2017. Efectos del carbofuran en juveniles de Oreochromis niloticus en la toxicidad, metabolismo de rutina y los parámetros hematológicos. Boletim do Instituto de Pesca 43(4): 513-526. DOI: 10.20950/1678-2305.2017v43n4p513
Barbour, C. D. 1973. The Systematics and evolution of the genus Chirostoma Swaison (Pisces: Atherinidae). Tulane Studies in Zoology and Botany 18 (3), 97-141.
Bloom, D. D., J. T. Weir, K. R. Piller & N. R. Lovejoy. 2013. Do freshwater fishes diversify faster than marine fishes? A test using state-dependent diversification analyses and molecular phylogenetics of new world silversides (Atherinopsidae). Evolution 67: 2040–2057. DOI: 10.1111/evo.12074
Bradford, M. M. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72 (1-2): 248-254. DOI: 10.1016/0003-2697(76)90527-3
Bretaud, S., J. P. Toutant & P. Saglio. 2000. Effects of carbofuran, diuron, and nicosulfuron on acetylcholinesterase activity in goldfish (Carassius auratus). Ecotoxicology and Environmental Safety 47 (2): 117–124. DOI: 10.1006/eesa.2000.1954
Buege, J. A. & S. D. Aust. 1978. Microsomal lipid peroxidation. Method Enzymology 52: 302-310. DOI: 10.1016/S0076-6879(78)52032-6
Campanella D., L. C. Hughes, P. J. Unmack, D. D. Bloom, K. R. Piller & G. Ortí. 2015. Multi-locus fossil- calibrated phylogeny of Atheriniformes (Teleostei, Ovalentaria). Molecular Phylogenetics and Evolution 86: 8-23. DOI: 10.1016/j.ympev.2015.03.001
Casida, J. E. 1963. Mode of action of carbamates. Annual Review of Entomology 8: 39-58. DOI: 10.1146/annurev.en.08.010163.000351
Efecto agudo del carbofuran en C. humboldtianum
Casida, J.E. & G. B. Quistad. 2004. Organophosphate toxicology: safety aspects of nonacetylcholinesterase secondary targets. Chemical Research in Toxicology 17 (8), 983-998. DOI: 10.1021/tx0499259x
Clasen, B., J. Leitemperger, C. Murussi, A. Pretto, C. Menezes, F. Dalabona, E. Marchezan, M. Bohrer Adaime, R. Zanella & V. L. Loro. 2014. Carbofuran promotes biochemical changes in carp exposed to rice field and laboratory conditions. Ecotoxicology and environmental safety 101: 77-82. DOI: 10.1016/j.ecoenv.2013.12.012
Collective of authors SPA (State Phytosanitary Administration). 2002. List of the registered plant protection products. Agrospoj, SPA.
Dembelé, K., E. Haubruge & C. Gaspar. 2000. Concentration effects of selected insecticides on brain acetylcholinesterases in the common carp (Cyprinus carpio L.). Ecotoxicology and Environmental Safety 45 (1): 49-54. DOI: 10.1006/eesa.1999.1829
Dobšíková, R. 2003. Acute toxicity of carbofuran to selected species of aquatic and terrestrial organisms. Plant Protection Science 39, 103–108. DOI: 10.17221/3865-PPS.
Dutta, H. M. & D. A. Arends. 2003. Effects of endosulfan on brain acetylcholinesterase activity in juvenile bluegill sunfish. Environmental Research 91 (3): 157-162. DOI: 10.1016/S0013-9351(02)00062-2.
Dzul-Caamal, R., M. L. Domínguez-López, H. F. Olivares-Rubio, E. García-Latorre & A. Vega-López. 2014. The relationship between the bioactivation and detoxification of diazinon and chlorpyrifos, and the inhibition of acetylcholinesterase activity in Chirostoma jordani from three lakes with low to high organophosphate pesticides contamination. Ecotoxicology 23: 779-790. DOI: 10.1007/s10646-014-1216-8
Echelle, A. A. & A. F. Echelle. 1984. Evolutionary genetics of a “species flock”: atherinid fishes of the Mesa Central Mexico. In: A. A. Echelle y I. Konfield (Eds.), Evolution of fish species flocks. Orono, ME (USA) University of Maine. pp. 93-110.
Ensibi, C., D. Hernández Moreno, F. Soler Rodríguez, M.N. Daly Yahya, M.P. Míguez-Santiyán & M. Pérez-López. 2012. Effects of subchronic exposure to carbofuran on antioxidant defence system and malondialdehyde levels in common carp (Cyprinus carpio L.), Toxicological & Environmental Chemistry, 94 (4): 748-759, DOI:10.1080/02772248.2 012.672821
EPA (Environmental Protection Agency). 1993. Methods for measuring the acute toxicity of effluents and receiving water to freshwater and marine organisms, 4th end, 243 p.
EPA. 2002. Public Health Goal for Carbofuran in drink water. United States Environmental Protection Agency. Manual Office of Environmental Health Hazard Assessment Washington. EUA, 15 pp.
Favari Perozzi, L., M. Madrigal Ortiz & E. López López. 2003. Efecto del agua del embalse de la Vega en la lipoperoxidación y los niveles de la acetilcolinesterasa en el hígado y el músculo de Xiphophorus helleri. Revista Internacional De Contaminación Ambiental 19(3): 145–155. Recuperado a partir de https://www.revistascca.unam. mx/rica/index.php/rica/article/view/23755
Fukuto, T. R. 1990. Mechanism of action of organophosphorus and carbamate insecticides. Environmental Health Perspectives 87: 245– 254. DOI: 10. 1289/ehp.9087245
Ghazala, S. M., L. Ahmad, S. Sultana, K. Al-Ghanim, F. Al-Misned & Z. Ahmad. 2014. Fish cholinesterases as biomarkers of sublethal effects of organophosphorus and carbamates in tissues of Labeo rohita. Journal of Biochemical and Molecular Toxicology 28 (3): 137-142. DOI: 10.1002/jbt.21545
Glusczak, L., D. Dos Santos Miron, B. S. Moraes, S. R. Rodríguez, S. M. R. Chitolina, V. M. Morsch & V. L. Loro. 2007. Acute effects of glyphosate herbicide on metabolic and enzymatic parameters of silver catfish (Rhamdia quelen). Comparative Biochemistry and Physiology part C: Toxicology & Pharmacology 146: 519-24. DOI: 10.1016/j. cbpc.2007.06.004
Güll, S., E. Belge-Kurutas, E. Yildiz, A. Sahan & F. Doran. 2004. Pollution correlated modifications of liver antioxidant systems and histopathology of fish (Cyprinidae) living in Seyhan Dam Lake, Turkey. Environment International 30: 605-609. DOI: 10.1016/s0160- 4120(03)00059-X
Gupta, R. C. (2009). Carbofuran toxicity. Journal of toxicology and environmental health. Vol.43-4. DOI: 10.1080/15287399409531931 Halliwell, B. & S. Chirico. 1993. Lipid peroxidation: its mechanism, measurement, and significance. The American Journal of Clinical Nutrition 57 (5): 7155-7255. DOI: 10.1093/ajcn/57.5.715S
Heath, A.G. 1995. Water Pollution and Fish Physiology. CRC Press. Boca Raton, Florida. DOI: 10.1201/9780203718896.
Hernández-Rubio, M. C., G. Figueroa-Lucero, I. A. Barriga-Sosa, J. L. Arredondo- Figueroa & T. Castro-Barrera. 2006. Early development of the shortfin silverside Chirostoma humboldtianum (Valenciennes, 1835) (Atheriniformes: Atherinopsidae). Aquaculture 261:1440- 1446. DOI: 10.1016/j.aquaculture.2006.0848
Hestrin, S. 1949. The reaction of acetylcholine and other carboxylic acid derivatives with hydroxylamine and its analytic applications. Journal of Biological Chemestry 180: 249-261. DOI: 10.1016/S0021- 9258(18)56740-5
Iannacone, J., L. AlvarIño & N. MamanI. 2011. Estimación de la Toxicidad Combinada de Mezclas de Furadán 4F® y Monofos® sobre Oncorhynchus mykiss (Walbaum, 1792). Journal of the Brazilian Society of Ecotoxicology 6 (1): 23-29. DOI:10.5132/jbse.2011.01.004
ISO 8692. 2004. Water quality freshwater algal growth inhibition test with unicellular green algae. International Organization for Standardization. Geneve, Switzerland.
Jash, N. B. & S. Bhattacharya. 1983. Delayed toxicity of carbofuran in freshwater teleosts, Channa punctatus (Bloch) and Anabas testudineus (Bloch). Water, Air, and Soil Pollution 19: 209-213. DOI: 10.1007/ BF00599047
Lal, B., M. K. Sarang & P. Kumar. 2013. Malathion exposure induces the endocrine disruption and growth retardation in the catfish, Clarias batrachus (Linn.). General and Comparative Endocrinology 181: 139145. DOI: 10.1016/j.ygcen.2012.11.004
Lawrence, R. A. & R. Burk. 1976. Glutathione peroxidase activity in selenium-deficient rat liver. Biochemical Biophysical Research Communications 71: 952-958. DOI: 10.1016/0006-291x (76)90747-6
Li F., L. Ji, Y. Luo & K. Oh. 2007. Hydroxyl radical generation and oxidative stress in Carassius Auratus Liver as Affected by 2,4,6-trichlorophenol, Chemosphere 67 (1): 13-19. DOI:10.1016/j.chemosphere.2006.10.030
Livingstone, D. R. 2003. Oxidative stress in aquatic organisms in relation to pollution and aquaculture. Revue de Médicine Vétérinaire 154 (6): 427-30.
Lushchack, V.I. 2011. Environmentally induced oxidative stress in aquatic animals. Aquatic Toxicology 101: 13-30. DOI: 10.1016/j.aquatox.2010.10.006
Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms. 2002. Quinta edición. U.S. EPA Office of Water, Washington, D.C. EPA-821-R-02-012. 266 pp.
Modesto, K. A. & C. B. R. Martínez. 2010. Roundup® causes oxidative stress in liver and inhibits acetylcholinesterase in muscle and brain of the fish Prochilodus lineatus. Chemosphere 78 (1): 294-299. DOI: 10.1016/j.chemosphere.2009.10.047
Moreira, R.A., A. da Silva Mansano & O. Rocha. 2015. The toxicity of carbofuran to the freshwater rotifer, Philodina roseola. Ecotoxicology 24: 604–615. DOI: 10.1007/s10646-014-1408-2
Nemcsók, J., A. Németh, Z. Buzás & L. Boross. 1984. Efects of copper, zinc, and paraquat on acetylcholinesterase activity in carp (Cyprinus carpio L.). Aquatic Toxicology 5 (1): 23-31. DOI: 10.1016/0166- 445X(84)90029-8
Nikoloff, N., S. Soloneski & M. L. Larramendy. 2012. Genotoxic and cytotoxic evaluation of the herbicide flurochloridone on Chinese hamster ovary (CHO-K1) cells. Toxicology in Vitro 26 (1): 157-163. DOI: 10.1016/j.tiv.2011.10.015
Norma Oficial Mexicana NOM-062-ZOO-1999. Que determina las especificaciones técnicas para la producción, cuidado y uso de animales de laboratorio. Secretaria de Agricultura y Desarrollo Rural, Diario oficial de la Federación. 6 de diciembre de 1999. México.
O’Brien, R. D. 1967. Insecticides: Action and Metabolism. Academic Press, New York, EUA. DOI: 10.1016/C2013-0-11985-X
Ochoa D. M. & J. F. González. 2008. Estrés oxidativo en peces inducido por contaminantes ambientales. Revista Medicina Veterinaria y de Zootecnia. 55:115-126.
Organization for the Economical Cooperation and Development (OECD). 2012. Fish acute toxicity test. OECD Guideline for Testing of Chemicals No. 203.
Paulo-Maya, J., G. Figueroa-Lucero & M. Soria-Barreto. 2000. Peces dulceacuícolas mexicanos XIX. Chirostoma humboldtianum (Atheriniformes: Atherinopsidae). Zoología Informa 43: 59-74
Pelletier M. 1986. Mercury-Selenium interactions in aquatic organisms: a review. Marine Environmental Research 18 (2): 111-132. DOI: 0143-8174/86/503-50
Peixoto, F., D. Alves-Fernandes, D. Santos & A. Fontaínhas Fernandes. 2006. Toxicological effects of oxyfluorfen on oxidative stress enzymes in tilapia Oreochromis nilocticus. Pesticide Biochemistry and Physiology 85 (2): 91-96. DOI: 10.1016/j.pestbp.2005.10.007
Priego A., H. Cotler, A. Fregoso, N. Luna & C. Enriquez. 2004. La dinámica ambiental de la cuenca Lerma-Chapala. Gaceta Ecológica 71: 23-38.
Ranjbar A. 2014. Evidence of oxidative damage in paraquat toxicity. Zahedan Journal Research in Medical Sciences 16 (12): 1-8.
Ray, A. K. & M. C. Ghosh. 2006. Aquatic toxicity of carbamates and organophosphates. Toxicology of Organophosphate and Carbamate Compounds chapter 45: 657-672. DOI: 10.1016/B978-012088523- 7/50046-6
Straus, D. L. & J. E. Chambers. 1995. Inhibition of acetylcholinesterase and aliesterases of fingerling channel catfish by chlorpyrifos, parathion, and S S S-tributyl phosphorotrithioate (DEF). Aquatic Toxicology 33 (3-4): 311-324. DOI: 10.1016/0166-445X(95)00024-X
Sun, Y., L. W. Oberley & Y. Li. 1988. A simple method for clinical assay of superoxide dismutase. Clinical Chemistry 34 (3): 497-500. DOI: 10.1093/clinchem/34.3.497
Trotter, D. M., R. A. Kent & M. P. Wong. 1991: Aquatic fate and effect of carbofuran. Critical Reviews in Environmental Control 21 (2): 137- 176. DOI: 10.1080/10643389109388412
USFDA (U.S. Food and Drugs Administration). 2014. Pesticides residue monitoring program. Disponible en línea en http://w.w.w.fda.gov/food/ foodboinellnesscontaminants/pesticides/default.html (consultado 15 mayo 2021).
Van der Oost, R., J. Beyer & N. P. E. Vermeulen. 2003. Fish bioaccumulation and biomarkers in environmental risk assessment: A review. Environmental Toxicology and Pharmacology 13 (2): 57-149. DOI: 10.1016/s1382-6689(02)00126-6
Yi, M.Q., H. X. Liu, X. Y. Shi, P. Liang & X. W. Gao. 2006. Inhibitory effects of four carbamate insecticides on acetylcholinesterase of male and female Carassius auratus in vitro. Comparative Biochemistry and Physiology Part C: Toxicology & Phrmacology 143(1): 113–116. DOI: 10.1016/j.cbpc.2005.12.008
Young, G., P. M. Lokman, I. Nakamura & F. W. Goetz. 2005. Gonadal steroidogenesis in teleost fish. In: Melamed, P. & N. Sherwood (eds). Molecular aspects of fish and marine biology 4: Hormones and their receptors in fish reproduction. Hackensack: World Scientific Publishing Co, pp. 155-223.
Zar J. H. 1984, Biostatistical Analysis. Prentice Hall, Nueva Jersey, EUA, 718 p.
Downloads
Published
How to Cite
Issue
Section
License
Los autores/as que publiquen en esta revista aceptan las siguientes condiciones:
De acuerdo con la legislación de derechos de autor, HIDROBIOLÓGICA reconoce y respeta el derecho moral de los autores, así como la titularidad del derecho patrimonial, el cual será cedido a la revista para su difusión en acceso abierto.
Publicar en la revista HIDROBIOLÓGICA tiene un costo de recuperación de $500 pesos mexicanos por página en blanco y negro (aproximadamente 29 dólares americanos) y $1000 pesos por página a color (aproximadamente 58 dólares americanos).
Todos los textos publicados por HIDROBIOLÓGICA sin excepción se distribuyen amparados bajo la licencia Creative Commons 4.0Atribución-No Comercial (CC BY-NC 4.0 Internacional), que permite a terceros utilizar lo publicado siempre que mencionen la autoría del trabajo y a la primera publicación en esta revista.
Los autores/as pueden realizar otros acuerdos contractuales independientes y adicionales para la distribución no exclusiva de la versión del artículo publicado en HIDROBIOLÓGICA (por ejemplo incluirlo en un repositorio institucional o publicarlo en un libro) siempre que indiquen claramente que el trabajo se publicó por primera vez en HIDROBIOLÓGICA.
Para todo lo anterior, el o los autor(es) deben remitir el formato de Carta-Cesión de la Propiedad de los Derechos de la primera publicación debidamente requisitado y firmado por el autor(es). Este formato se puede enviar por correo electrónico en archivo pdf al correo: enlacerebvistahidrobiológica@gmail.com; rehb@xanum.uam.mx (Carta-Cesión de Propiedad de Derechos de Autor).
Esta obra está bajo una licencia de Creative Commons Reconocimiento-No Comercial 4.0 Internacional.
