Presence of organochlorine pesticides and characterization of biomarkers in wild mice living in crop fields
Palabras clave:
Acetylcholineterase, catalase, glutathione-S-transferase, biomarkers, Mus musculus, organochlorine pesticides, wildlifeResumen
The use of pesticides in crops bordering conservation areas poses risks for wildlife incidentally exposed; its effects in the Yucatan Peninsula, Mexico, are still unknown. Wild mice that inhabit farming land play a key ecological role, and can also be used as bioindicators of wildlife exposure to pollutants. The objectives of this work were to determine the presence of organochlorine pesticides (OC) in liver and evaluate the seasonal response of enzymatic biomarkers (BM) such as acetylcholinesterase (AChE), glutathione-S-transferase (GST), and catalase (CAT). Wild mice (Mus musculus) were captured between June 2015 and April 2016 in a watermelon crop of a rural community in Quintana Roo, Mexico. Individual mice were sacrificed in situ, followed by tissue dissection (liver, brain and skeletal muscle). Pesticides were determined by gas chromatography; BM activity was estimated by spectrophotometry. We captured 35 individuals, with a capture success of 2.33%. The prevailing OCs detected were drines in both climatic seasons. The rainy season influenced the activity of biomarkers to a greater extent, since AChE showed a lower activity (16 % and 40 % in brain and liver, respectively). GST was activated during the same season (77 % higher), while CAT did not show significant differences between seasons. There was no significant correlation between OC concentrations and biomarker activity, except for drines and AChE in the brain. OC concentrations recorded in the present work are below (2- and 20-fold lower) those reported in other works on rodents under controlled conditions. BM activity suggests that rainfall seem to exacerbate the effects of pesticides on mice; however, it seemingly does not pose a risk for their survival. The use of wild mice as bioindicators is a valuable and practical tool to detect disturbances derived from the use of pesticides in agricultural areas. Further research is recommended using a broader BM battery to identify those pollutants with the most severe effect on the physiology of wild animals incidentally exposed to pesticides.Citas
Aebi, H. 1984. Catalase in vitro. Methods in Enzymology 105:121–126.
Alcérreca Aguirre, C., R. Robles de Benito, L. Pereira Lara, and D. Amtochew Alonzo. 2009. Mamíferos de la Península de Yucatán, Guía completa. Ed. Dante. Mérida Yucatán, México.
Andrade-Herrera, M. 2011. Evaluación del efecto de la contaminación atmosférica en dos especies del género Peromyscus (Rodentia: Muridae) que cohabitan en el Parque Nacional Desierto de los Leones. Tesis de Maestría. Universidad Autónoma Metropolitana. México, D.F.
Andrade Herrera, M., G. Escalona Segura, M. González Jáuregui, R. Reyna Hurtado, J. A. Vargas Contreras, and J. Rendón von Osten. 2018. Presence of pesticides and toxicity assessment of agricultural soils in the Quintana Roo Mayan zone, Mexico using biomarkers in earthworms (Eisenia fetida). Artículo enviado para su publicación.
Ayed-Boussema, I., K. Rjiba, A. Moussa, N. Mnasri, and H. Bacha. 2012. Genotoxicity associated with oxidative damage in the liver and kidney of mice exposed to dimethoate subchronic intoxication. Environmental Science and Pollution Research 19:458–466.
Barrett, G. W., and R. M. Darnell. 1967. Effects of Dimethoate on Small Mammal Populations. American Midland Naturalist 77:164-175.
Bhaskar, R., and B. Mohanty. 2014. Pesticides in mixture disrupt metabolic regulation: In silico and in vivo analysis of cumulative toxicity of mancozeb and imidacloprid on body weight of mice. General and Comparative Endocrinology 205:226–234.
Block, E. K., T. E. Lacher, L. W. Brewer, G. P. Cobb, and R. J. Kendall. 1999. Population Responses of Peromyscus Resident in Iowa Cornfields Treated with the Organophosphorus Pesticide COUNTER®. Ecotoxicology 8:189–200.
Bradford, M. M. 1976. A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding. Analitical Biochemistry 72:248–254.
Buenfil-Rojas, A. M., T. Alvarez-Legorreta, and J. R. Cedeño-Vazquez. 2016. Metals and metallothioneins in Morelet’s crocodile (Crocodylus moreletii) from Rio Hondo. Toxicology Letters 259:S96.
Caldas, E. D., R. Coelho, L. C. K. R. Souza, and S. C. Siba. 1999. Organochlorine Pesticides in Water, Sediment, and Fish of Paranoá Lake of Brasilia, Brazil. Bulletin of Environmental Contamination and toxicology 62:199–206.
Cárdenas, S., and A. Márquez. 2015. Persistencia de plaguicidas organoclorados en suelos, agua y sedimentos de la cuenca del Tucutunemo, Municipio Zamora, Estado Aragua. In Memorias del XXI Congreso Venezolano de la ciencia del suelo.
Ceballos, G. 2005. Orden Rodentia. Pp. 530. in Los mamíferos silvestres de México (Ceballos G., and G. Oliva, Eds.). Fondo de Cultura Económica. Ciudad de México, México.
Charruau, P., Y. Hénaut, and T. Álvarez-Legorreta. 2013. Organochlorine pesticides in nest substratum and infertile eggs of American crocodiles (Reptilia, Crocodylidae) in a Mexican Caribbean atoll. Caribbean Journal of Science 47:1–12.
Chen, X. P., T. T. Wang, X. Z. Wu, D. W. Wang, and Y. S. Chao. 2016. An in vivo study in mice: mother’s gestational exposure to organophosphorus pesticide retards the division and migration process of neural progenitors in the fetal developing brain. Toxicology Research 5:1359–1370.
Chi Coyoc, T. E., G. Escalona Segura, A. Vallarino Moncada, J. A. Vargas Contreras, G. E. Castillo Vela, and J. Lara Reyna. 2016. Organochlorine and anticholinergic pesticides in wild mice from wetland ecosystems of the Gulf of Mexico. Therya 7:465–482.
Cobos, V., M. Mora, and G. Escalona. 2006. Inhibición de colinesterasa plasmática en el zorzal pardo (Turdus grayi), expuesto a diazinón en cultivos de papaya maradol en Yucatán, México. Revista de Toxicología 23:17–21.
Custer, T. W., E. F. Hill, and H. M. Ohlendorf. 1985. Effects of wildlife of ethyl and methyl parathion applied to California USA rice fields. California Fish and Game 71:220–224.
Dell’Omo, G., M. G. Pleskacheva, D. P. Wolfer, H. P. Lipp, and R. F. Shore. 2003. Comparative Effects of Exposure to an Organophosphate Pesticide on Locomotor Activity of Laboratory Mice and Five Species of Wild Rodents. Bulletin of Environmental Contamination and Toxicology 70:138–145.
Dell’Omo, G., and R. F. Shore. 1996. Behavioral and physiological effects of acute sublethal exposure to dimethoate on wood mice, Apodemus sylvaticus. Archives of Environmental Contamination and Toxicology 31:91–97.
Durda, J. L., R. A. Powell, and G. T. Barthalmus. 1989. Physiological and behavioral effects of guthion on pine voles,Microtus pinetorum. Bulletin of Environmental Contamination and Toxicology 43:80–86.
Edward Montz, W., P. F. Scanlon, and R. L. Kirkpatrick. 1983. Effects of field application of the anti-cholinesterase insecticide methomyl on brain acetylcholinesterase activities in wild Mus musculus. Bulletin of Environmental Contamination and Toxicology 31:158–163.
Ellman, G. L., K. D. Courtney, V. J. Andres, and R. M. Featherstone. 1961. A New and Rapid Colorimetric Determination of Acetilcholinesterase Activity. Biochemical Pharmacology 7:88–95.
Ghodrat, E. M., P. Kazem, H. Shapour, Y. Parichehr, and N. Golamreza. 2014. The effects of pyridaben pesticide on gonadotropic, gonadal hormonal alternations, oxidative and nitrosative stresses in Balb/C mice strain. Comparative Clinical Pathology 23:297–303.
Giles Jr., R. H. 1970. The Ecology of a Small Forested Watershed Treated with the Insecticide Malathion: S35. Wildlife Monographs 3-81.
Givaudan, N., F. Binet, B. Le Bot, and C. Wiegand. 2014. Earthworm tolerance to residual agricultural pesticide contamination: Field and experimental assessment of detoxification capabilities. Environmental Pollution 192:9–18.
Gómez-Ugalde, R. M. 2003. Efectos de la contaminación atmosférica en poblaciones de pequeños roedores silvestres (Microtus mexicanus, Peromyscus melanotis y Peromyscus difficilis) en México, D. F. Tesis de Doctorado. Universitat de Barcelona. Barcelona, España.
González Váldez, L. S., R. Irigoyen Campuzano, V. Ortega Martínez, and S. V. Jáquez Matas. 2013. Comportamiento de plaguicidas persistentes en el medio ambiente. Centro Interdisciplinario de Investigación para el Desarrollo Integral Regionla Unidad Durango del Instituto Politécnico Nacional 1:1–17.
Guilhermino, L., M. C. Lopes, A. P. Carvalho, and A. M. V. M. Soares. 1996. Inhibition of acetylcholinesterase activity as effect criterion in acute tests with juvenile Daphnia Magna. Chemosphere 32:727–738.
Habig, W. H., M. J. Pabst, and W. B. Jakoby. 1974. Glutathione S-transferases: The first enzymatic step in mercapturic acid formation. The Journal of Biological Chemistry 249:7130–7139.
Helsel, D. R. 2012. Statistics for Censored Environmental Data Using Minitab and R. 2a ed. John Wiley and Sons.
Hirano, T., S. Yanai, T. Takada, N. Yoneda, T. Omotehara, N. Kubota, K. Minami, A. Yamamoto, Y. Mantani, T. Yokoyama, H. Kitagawa, and N. Hoshi. 2017. NOAEL-dose of a neonicotinoid pesticide, clothianidin, acutely induce anxiety-related behavior with human-audible vocalizations in male mice in a novel environment. Toxicology Letters 282:57-63.
Jefferies, D. J., B. Stainsby, and M. C. French. 1973. The ecology of small mammals in arable fields drilled with winter wheat and the increase in their dieldrin and mercury residues. Journal of Zoology 171:513–539.
Jett, D. A. 1986. Cholinesterase inhibition in meadow voles (Microtus Pennsylvanicus) following field applications of orthene®. Environmental Toxicology and Chemistry 5:255-259.
Jin, Y., J. Wang, X. Pan, L. Wang, and Z. Fu. 2013. cis-Bifenthrin enantioselectively induces hepatic oxidative stress in mice. Pesticide Biochemistry and Physiology 107:61–67.
Jin, Y., L. Wang, M. Ruan, J. Liu, Y. Yang, C. Zhou, B. Xu, and Z. Fu. 2011. Cypermethrin exposure during puberty induces oxidative stress and endocrine disruption in male mice. Chemosphere 84:124–130.
Johnston, J. J. 2000. Introduction to Pesticides and Wildlife. 771:1–5. in Pesticides and Wildlife (Johnston, J. J. Ed.). American Chemical Society. Washington, U. S. A.
Köhler, H. R., and R. Triebskorn. 2013. Wildlife Ecotoxicology of Pesticides: Can We Track Effects to the Population Level and Beyond? Science 341:759–765.
Latchoumycandane, C., and P. Mathur. 2002. Induction of oxidative stress in the rat testis after short-term exposure to the organochlorine pesticide methoxychlor. Archives of Toxicology 76:692–698.
Laubscher, J. A., G. R. Dutt, and C. C. Roan. 1971. Chlorinated insecticide residues in wildlife and soil as a function of distance from application. Pesticide Monitoring Journal 5:251-258.
Limón-Pacheco, J., and M. E. Gonsebatt. 2009. The role of antioxidants and antioxidant-related enzymes in protective responses to environmentally induced oxidative stress. Mutation Research/Genetic Toxicology and Environmental Mutagenesis 674:137–147.
Lincer, J. L., and J. A. Sherburne. 1974. Organochlorines in Kestrel Prey: A North-South Dichotomy. The Journal of Wildlife Management 38:427-434.
Linder, G., and G. Joermann. 2001. Assessing Hazard and Risk of Chemical Exposures to wild mammals: Food-chain analysis and its role in Ecological Risk Assessment. Pp. 635-670 in Ecotoxicology of Wild Mammals (Shore, R. F., and B. A. Rattner, eds.). 1a ed. John Wiley and Sons Ltd.
Lopaka, L. 2013. Nondetects and Data Analysis for Environmental Data. R package version.
Lukaszewicz-Hussain, A. 2010. Role of oxidative stress in organophosphate insecticide toxicity – Short review. Pesticide Biochemistry and Physiology 98:145–150.
Mackay, D., L. S. McCarty, and MacLeod, M. 2001. On the validity of classifying chemicals for persistence, bioaccumulation, toxicity, and potential for longâ€range transport. Environmental Toxicology and Chemistry 20:1491-1498.
Meyers, S. M., and J. O. Wolff. 1994. Comparative toxicity of azinphos-methyl to house mice, laboratory mice, deer mice, and gray-tailed voles. Archives of Environmental Contamination and Toxicology 26:478–482.
Morales-Prieto, N., and N. Abril. 2017. REDOX proteomics reveals energy metabolism alterations in the liver of M. spretus mice exposed to p, p′-DDE. Chemosphere 186:848–863.
Morris, R. D. 1968. Effects of endrin feeding on survival and reproduction in the deer mouse, Peromyscus maniculatus. Canadian Journal of Zoology 46:951–958.
Noreña-Barroso, E., R. Sima-Alvarez, G. Gold-Bouchot, and O. Zapata-Perez. 2004. Persistent organic pollutants and histological lesions in Mayan catfish Ariopsis assimilis from the Bay of Chetumal, Mexico. Marine Pollution Bulletin 48:263–269.
Oksanen, J., F. G. Blanchet, M. Friendly, R. Kindt, P. Legendre, D. McGlinn, P. R. Minchin, B. R. O’Hara, G. L. Simpson, P. Solymos, M. H. H. Stevens, E. Szoecs, and H. Wagner. 2017. Vegan: Community Ecology Package. R package.
Panemangalore, M., and F. N. Bebe, 2000. Dermal exposure to pesticides modifies antioxidant enzymes in tissues of rats. Journal of environmental science and health. Part. B, Pesticides, food contaminants, and agricultural wastes 35:399–416.
Peakall, D. B., and McBee, K. 2001. Biomarkers for Contaminant Exposure and Effects in mammals. Pp. 551–576 In Ecotoxicology of Wild Mammals (Shore, R. F., and B. A. Rattner, eds.). John Wiley and Sons Ltd. U. S. A.
Perez-Gonzalez, E., U. G. Osuna-Martinez, M. N. Herrera-Moreno, G. D. Rodriguez-Meza, H. A. Gonzalez-Ocampo, and M. Bucio-Pacheco. 2017. Organochlorine Pesticides in Gonad, Brain, and Blood of Mice in Two Agricultural Areas of Sinaloa. Bulletin of Environmental Contamination and Toxicology 98:454–459.
Peris-Sampedro, F., I. Reverte, P. Basaure, M. Cabré, J. L. Domingo, and M. T. Colomina. 2016. Apolipoprotein E (APOE) genotype and the pesticide chlorpyrifos modulate attention, motivation and impulsivity in female mice in the 5-choice serial reaction time task. Food and Chemical Toxicology 92:224–235.
R Core Team. 2016. R: A language and environment for statistical computing.
Ramírez, J. A., and M. Lacasaña. 2001. Plaguicidas: Clasificación, Uso, Toxicología Y Medición De La Exposición. Archivos de Prevención de Riesgos Laborales. 4:67–75.
Rattner, B. A., and D. J. Hoffman. 1984. Comparative toxicity of acephate in laboratory mice, white-footed mice, and meadow voles. Archives of Environmental Contamination and Toxicology 13:483–491.
Rendón von Osten, J., M. Memije-Canepa, and N. A. Ek-Moo. 2005. Plaguicidas Orgánicos Persistentes (POPs) en Sedimentos de la Costa Sur de Campeche, México. Pp. 249–260 in Golfo de México Contaminación e Impacto Ambiental: Diagnóstico y Tendencias (Botello, A. V., J. Rendón-von Osten, G. Gold-Bouchot, and C. Agraz-Hernández, Eds.). 2da. edición,). Universidad Autónoma de Campeche. Campeche, México.
Rodríguez-Castellanos, L., and J. C. Sanchez-Hernandez. 2007. Earthworm biomarkers of pesticide contamination: Current status and perspectives. Journal of Pesticides Sciences 32:360–371.
Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación. 2014. Norma Oficial Mexicana NOM-033-SAG/ZOO-2014, Que establece Métodos para dar muerte a los animales domésticos y silvestres. Mexico. 26 de agosto de 2015 .
SAGARPA. 2015. Avance e producción agrícola con tecnificación del riego en Quintana Roo. Secretaría de agricultura, ganadería, desarrollo rural, pesca y alimentación.
Sheffield, S. R., K. Sawicka-Kapusta, J. B. Cohen, and B. A. Rattner. 2001. Rodentia and lagomorpha. Pp. 215–314 In Ecotoxicology of Wild Mammals (Shore, F. R., and B. A. Rattner, Eds.). New York. John Wiley and Sons Ltd. U. S. A.
van der Oost, R., J. Beyer, and N. P. E. Vermeulen. 2003. Fish bioaccumulation and biomarkers in environmental risk assessment : A review. Environmental Toxicology and Pharmacology 13:57–149.
Westlake, G. E., A. D. Martin, P. I. Stanley, and C. H. Walker. 1983. Control enzyme levels in the plasma, brain and liver from wild birds and mammals in Britain. Comparative Biochemistry and Physiology Part C: Comparative Pharmacology 76:15–24.
Wolfe, J. L., and R. J. Esher. 1980. Toxicity of carbofuran and lindane to the old-field mouse (Peromyscus polionotus) and the cotton mouse (P. gossypinus). Bulletin of Environmental Contamination and Toxicology 24:894–902.
Yilmaz, H. R., E. Yüksel, and Y. Türköz. 2004. The effect of 2, 4-dichlorophenoxyacetic acid on some antioxidant enzymes in kidneys of the second cross offsprings mice. Arastirma 11:6-9.
Zar, J. H. 2010. Biostatistical Analysis (5th ed.). Pearson Prentice Hall. Upper Saddle River.
Zhang, H., Z. Wang, B. Lu, C. Zhu, G. Wu, and V. Walter. 2007. Occurrence of organochlorine pollutants in the eggs and dropping-amended soil of Antarctic large animals and its ecological significance. Science in China Series D: Earth Sciences 50:1086–1096.
Zhao, Y., Y. Zhang, G. Wang, R. Han, and X. Xie. 2016. Effects of chlorpyrifos on the gut microbiome and urine metabolome in mouse (Mus musculus). Chemosphere 153:287–293.
Descargas
Publicado
Número
Sección
Licencia
La revista THERYA, con base en su política de acceso abierto, permite descargar en forma gratuita el contenido completo de la revista en formato digital. También autoriza al autor a colocar el artículo en el formato publicado por la revista en su sitio web personal, o en un repositorio de acceso abierto, distribuir copias del artículo publicado en formato electrónico o impreso a quien él considere conveniente, y reutilizar parte o la totalidad del artículo en sus artículos o libros futuros, dando los créditos correspondientes. Se utiliza la licencia Creative Commons CC BY-NC-SD. La que se especifica en las publicaciones.
