Acute effect of carbofuran in Chirostoma humboldtianum juveniles (Atheriniformes: Atherinopsidae)

Authors

  • Octavio Abeja-Pineda Universidad Autónoma Metropolitana-Iztapalapa
  • Gerardo Figueroa Lucero Universidad Autónoma Metropolitana-Iztapalapa
  • María Cecilia Hernández-Rubio Instituto Politécnico Nacional
  • Liliana Favari Perozz Instituto Politécnico Nacional

Keywords:

Carbofuran, lipoperoxidation, neurotoxicity, stress oxidative

Abstract

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

Download data is not yet available.

Author Biography

Gerardo Figueroa Lucero, Universidad Autónoma Metropolitana-Iztapalapa

Profesor Titular

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.

Published

2023-05-10

How to Cite

Abeja-Pineda, O., Figueroa Lucero, G., Hernández-Rubio, M. C., & Favari Perozz, L. . (2023). Acute effect of carbofuran in Chirostoma humboldtianum juveniles (Atheriniformes: Atherinopsidae). HIDROBIOLÓGICA, 33(3). Retrieved from https://hidrobiologica.izt.uam.mx/hidrobiologica/index.php/revHidro/article/view/1594

Issue

Section

Artículos