Abstract
Lead is a metal capable of affecting physiology and metabolism in fish, including Nile tilapia (Oreochromis niloticus). However, few studies have evaluated the effects of lead on digestive enzyme activities in fry. At that stage, independent feeding begins, and there is increased demand and consumption of food, so chronic exposure to metal during this stage of development would cause null or minimal growth in organisms. In this study, fry from Nile tilapia was used to evaluate the effects of lead acetate by chronic exposure on the growth and the activities of the digestive enzymes after 30 and 60 days exposures. Four treatment groups 0.025, 0.050, 0.075 and 0.100 mg/L of lead acetate and a lead-free control were established. The activity of enzymes decreased, in the case of acidic proteases after 30 days and lipases after 60 days of exposure, from 0.025 and 0.050 mg/L of lead acetate, respectively. The amylase activity increased in metal-treated, while the chymotrypsin decreased partially at 60 days. Lipases decreasing activity might be causing an increase of triglycerides (lipids) and body mass observed during the first 30 days of exposure. Concentrations, equal to or above 0.075 mg Pb/L, cause significant effects on size and weight of fry, with nearly 54% lower than controls. At chronic exposure and early stage of development, the enzymatic activity is partially reduced along with body weight gain, which would affect subsequent growing and aquaculture production. The digestive enzyme response is discussed as a possible limited biomarker of exposure, to be used in biomonitoring.
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Abdel-Tawwab, M., & Wafe, M. (2010). Efecto de la suplementación con Sel-Plex® sobre la respuesta de la Tilapia del Nilo, Oreochromis niloticus (L.) a la toxicidad por cadmio en el ambiente. Journal of World Aquaculture, 106–114.
Abdel-Tawwab, M., El-Sayed, G. O., & Shady, S. H. (2016). Growth, biochemical variables, and zinc bioaccumulation in Nile tilapia, Oreochromis niloticus (L.) as affected by water-born zinc toxicity and exposure period. International Aquatic Research, 8(3), 197–206. https://doi.org/10.1007/s40071-016-0135-0.
Abdel-Tawwab, M., El-Sayed, G. O., Monier, M. N., & Shady, S. H. (2017a). Dietary EDTA supplementation improved growth performance, biochemical variables, antioxidant response, and resistance of Nile tilapia, Oreochromis niloticus (L.) to environmental heavy metals exposure. Aquaculture, 473(2017), 478–486. https://doi.org/10.1016/j.aquaculture.2017.03.006.
Abdel-Tawwab, M., El-Sayed, G. O., & Shady, S. H. (2017b). Effect of dietary active charcoal supplementation on growth performance, biochemical and antioxidant responses, and resistance of Nile tilapia, Oreochromis niloticus (L.) to environmental heavy metals exposure. Aquaculture, 479(May), 17–24. https://doi.org/10.1016/j.aquaculture.2017.05.016.
Abedi, Z., Hasantabar, F., Khalesi, M. K., & Babaei, S. (2013). Enzymatic activities in common carp; Cyprinus carpio influenced by sublethal concentrations of cadmium, lead, chromium. World Journal of Fish and Marine Sciences, 5(2), 144–151. https://doi.org/10.5829/idosi.wjfms.2013.05.02.7143.
AILAD. (2010). Manual para el manejo de animales con fines de experimentación y de enseñanza. Villahermosa: UJAT.
Aldoghachi, M. A., Azirun, M. S., Yusoff, I., & Ashraf, M. A. (2016). Ultrastructural effects on gill tissues induced in red tilapia Oreochromis sp. by a waterborne lead exposure. Saudi Journal of Biological Sciences, 23(5), 634–641. https://doi.org/10.1016/j.sjbs.2015.08.004.
Alm-Eldeen, A. A., Donia, T., & Alzahaby, S. (2018). Comparative study on the toxic effects of some heavy metals on the Nile Tilapia, Oreochromis niloticus, in the Middle Delta, Egypt. Environmental Science and Pollution Research, 25(15), 14636–14646. https://doi.org/10.1007/s11356-018-1677-z.
Alvarado-Flores, J. (2010). Efectos de la bioacumulación de plomo sobre la tasa intrínseca de crecimiento (r) y otros parámetros poblacionales, localizacióncelular del plomo, y determinación de factor de bioconcentración en una especie de rotífero dulceacuícola. Universidad Autónoma de Aguascalientes. Retrieved from https://search.ebscohost.com/login.aspx?direct=true&db=cat04898a&AN=ua.000146105&site=eds-live.
Anson, M. L. (1938). The estimation of pepsin, trypsin, papain, and cathepsin with hemoglobin. Journal of General Physiology, 22(1), 79–89. https://doi.org/10.1085/jgp.22.1.79.
Anukoolpra, T., Srinuansom, K., Rukdontri, T., Nonkhukhet, S., & Petkam, R. (2019). Postprandial in vitro protease-specific activity of Nile tilapia (Oreochromis niloticus L.) digestive organs. Pakistan Journal of Nutrition, 18(2), 125–133. https://doi.org/10.3923/pjn.2019.125.133.
Araújo, F. G., Morado, C. N., Parente, T. T. E., Paumgartten, F. J. R., & Gomes, I. D. (2018). Biomarkers and bioindicators of the environmental condition using a fish species (Pimelodus maculatus Lacepède, 1803) in a tropical reservoir in Southeastern Brazil. Brazilian Journal of Biology, 78(2), 351–359. https://doi.org/10.1590/1519-6984.167209.
Baiomy, A. A. (2016). Histopathological biomarkers and genotoxicity in gill and liver tissues of Nile tilapia Oreochromis niloticus from a polluted part of the Nile River, Egypt. African Journal of Aquatic Science, 41(2), 181–191. https://doi.org/10.2989/16085914.2016.1168734.
Barbieri, E., Campos-Garcia, J., Martinez, D. S. T., Da Silva, J. R. M. C., Alves, O. L., & Rezende, K. F. O. (2016). Histopathological effects on gills of Nile tilapia (Oreochromis niloticus, Linnaeus, 1758) exposed to Pb and carbon nanotubes. Microscopy and Microanalysis, 22(6), 1162–1169. https://doi.org/10.1017/S1431927616012009.
Bartram, J., & Ballance, R. (1996). Water quality monitoring: a practical guide to the design of freshwater quality studies and monitoring programmes. Londres: Chapman and Hill.
Bergmeyer, H. V. (1974). Phosphatases. Methods of enzymatic analysis (Vol. 2). Academic Press.
Bolton, J. L., Stehr, C. M., Boyd, D. T., Burrows, D. G., Tkalin, A. V., & Lishavskaya, T. S. (2004). Organic and trace metal contaminants in sediments and English sole tissues from Vancouver Harbour, Canada. Marine Environmental Research, 57(1–2), 19–36. https://doi.org/10.1016/S0141-1136(03)00058-8.
Bradford, M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254. https://doi.org/10.1006/abio.1976.9999.
Cabral, H. N., Costa, M. J., & Salgado, J. P. (2001). Does the Tagus estuary fish community reflect environmental changes? Climate Research, 18(1–2), 119–126. https://doi.org/10.3354/cr018119.
Campos, S. A. B., Dal-Magro, J., & de Souza-Franco, G. M. (2018). Metals in fish of different trophic levels in the area of influence of the AHE Foz do Chapecó reservoir, Brazil. Environmental Science and Pollution Research, 25(26), 26330–26340. https://doi.org/10.1007/s11356-018-2522-0.
Chua, E. M., Flint, N., Wilson, S. P., & Vink, S. (2018). Potential for biomonitoring metals and metalloids using fish condition and tissue analysis in an agricultural and coal mining region. Chemosphere, 202, 598–608. https://doi.org/10.1016/j.chemosphere.2018.03.080.
CONAPESCA. (2017). La Acuacultura en Mexico, retos y oportunidades. XII Foro Internacional de Acuicultura (FIACUI) 2017. https://fiacui.com/2017/Tilapia/Jueves28sep/Copiade05SituaciónactualdelaacuiculturaenMéxico.ComisionadoMarioAguilarSanchez.pdf.
Daiwile, A. P., Naoghare, P. K., Giripunje, M. D., Rao, P. D. P., Ghosh, T. K., Krishnamurthi, K., et al. (2015). Correlation of melanophore index with a battery of functional genomic stress indicators for measurement of environmental stress in aquatic ecosystem. Environmental Toxicology and Pharmacology, 39(2), 489–495. https://doi.org/10.1016/j.etap.2014.12.006.
DelMar, E. G., Largman, C., Brodrick, J. W., & Geokas, M. C. (1979). A sensitive new substrate for chymotrypsin. Analytical Biochemistry, 99(2), 316–320. https://doi.org/10.1016/S0003-2697(79)80013-5.
Dixon, M., & Webb, E. (1979). Enzymes (3rd ed.). New York: Academic Press.
Dos Santos, C. R., Cavalcante, A. L. M., Hauser-Davis, R. A., Lopes, R. M., & Da Costa Mattos, R. D. C. O. (2016). Effects of sub-lethal and chronic lead concentrations on blood and liver ALA-D activity and hematological parameters in Nile tilapia. Ecotoxicology and Environmental Safety, 129, 250–256. https://doi.org/10.1016/j.ecoenv.2016.03.028.
Eisler, R. (2000). Lead. In Handbook of chemical risk assessment (Vol. 1, pp. 201–311). Boca Raton: Lewis Publishers.
Erlanger, B. F., Kokowsky, N., & Cohen, W. (1961). The preparation and properties of two new chromogenic substrates of trypsin. Archives of Biochemistry and Biophysics, 95(2), 271–278. https://doi.org/10.1016/0003-9861(61)90145-X
Escobar, L., Olvera, M., & Puerto, C. (2006). Avances sobre la ecología microbiana del tracto digestivo de la tilapia y sus potenciales implicaciones. In VIII Simposium Internacional de Nutrición Acuícola. Monterrey: Universidad Autónoma de Nuevo León.
FAO. (2006). Identidad Perfil. Programa de información de especies acuáticas Oreochromis. http://www.revistaaquatic.com/aquatic/pdf/34_3.pdf.
FAO. (2018). Globefish highlights. FAO. https://issuu.com/globefish/docs/globefish_highlights-_issue_4_2018.
Flora, S. J. S., Saxena, G., Gautam, P., Kaur, P., & Gill, K. D. (2007). Response of lead-induced oxidative stress and alterations in biogenic amines in different rat brain regions to combined administration of DMSA and MiADMSA. Chemico-Biological Interactions, 170(3), 209–220. https://doi.org/10.1016/j.cbi.2007.08.003.
Flores, J., & Albert, L. A. (2004). Environmental lead in Mexico, 1990-2002. Reviews of Environmental Contamination and Toxicology, 181, 37–109. https://doi.org/10.1007/0-387-21733-9_2
Folk, J. E., & Schirmer, E. W. (1965). Isolation of the zymogen. The Journal of Biological Chemistry, 240(1), 181–192.
Fouz, B., Alcaide, E., Barrera, R., & Amaro, C. (2002). Susceptibility of Nile tilapia (Oreochromis niloticus) to vibriosis due to Vibrio vulnificus biotype 2 (serovar E). Aquaculture, 212(1–4), 21–30. https://doi.org/10.1016/S0044-8486(02)00002-9.
Fowler, J., Cohen, L., & Jarvis, P. (1998). Practical statistics for field biology. New York: John Wiley & Sons.
Frías-Espericueta, M. G., Voltolina, D., & Osuna-López, J. I. (2003). Acute toxicity of copper, zinc, iron, and manganese and of the mixtures copper-zinc and iron-manganese to white leg shrimp Litopenaeus vannamei postlarvae. Bulletin of Environmental Contamination and Toxicology, 71(1), 68–74. https://doi.org/10.1007/s00128-003-0132-z.
Garza, A., Chávez, H., Vega, R., & Soto, E. (2005). Mecanismos celulares y moleculares de la neurotoxicidad por plomo. Salud Mental, 28(2), 48–58. https://www.redalyc.org/articulo.oa?id=58222805.
Halver, J. E., & Handy, R. W. (2002). Fish nutrition (3rd ed.). San Diego: Academic Press.
Hashish, E. A., Elgaml, S. A., El-Murr, A., & Khalil, R. (2015). Nephroprotective and antioxidant significance of selenium and α-tocopherol on lead acetate-induced toxicity of Nile tilapia (Oreochromis niloticus). Fish Physiology and Biochemistry, 41(3), 651–660. https://doi.org/10.1007/s10695-015-0035-z.
Hsien-Tsang, S., & Quintanilla, M. (2008). Manual de reproducción y cultivo de tilapia. CENDEPESCA. Centro de Desarrollo de la Pesca y la Acuicultura. https://doi.org/10.1017/CBO9781107415324.004.
Klahan, R., Areechon, N., Yoonpundh, R., & Engkagul, A. (2009). Characterization and activity of digestive enzymes in different sizes of Nile tilapia (Oreochromis niloticus L.). Kasetsart Journal - Natural Science, 43(1), 143–153.
Kotorman, M., Laszlo, K., Nemcsok, J., & Simon, L. M. (2000). Effects of Cd2+, Cu2+, Pb2+ and Zn2+ on activities of some digestive enzymes in carp (Cyprinus carpio L.). Journal of Environmental Science and Health - Part A Toxic/Hazardous Substances and Environmental Engineering, 35(9), 1517–1526. https://doi.org/10.1080/10934520009377052.
Kunitz, M. (1946). Crystalline soybean trypsin inhibitor. The Journal of General Physiology, 29(3), 291–310.
Li, J. S., Li, J. L., & Wu, T. T. (2007). The effects of copper, iron and zinc on digestive enzyme activity in the hybrid tilapia Oreochromis niloticus (L.) x Oreochromis aureus (Steindachner). Journal of Fish Biology, 71(6), 1788–1798. https://doi.org/10.1111/j.1095-8649.2007.01643.x.
Lorenzo - Manzanarez, J. L. (2011). Efecto de tres métodos de cocción sobre el contenido nutricional de la mojarra Tilapia (Oreochromis sp.). Universidad del Papaloapan.
Lu, H., Guizzetti, M., & Costa, L. G. (2001). Inorganic lead stimulates DNA synthesis in human astrocytoma cells: role of protein kinase Cα. Journal of Neurochemistry, 78(3), 590–599. https://doi.org/10.1046/j.1471-4159.2001.00434.x.
Maroux, S., Louvard, D., & Baratti, J. (1973). The aminopeptidase from hog intestinal brush border. Biochimica et Biophysica Acta, 321, 282–295.
Martinez, D. S. T., Alves, O. L., & Barbieri, E. (2013). Carbon nanotubes enhanced the lead toxicity on the freshwater fish. Journal of Physics: Conference Series, 429(1). https://doi.org/10.1088/1742-6596/429/1/012043.
Matos, L. A., Cunha, A. C. S., Sousa, A. A., Maranhão, J. P. R., Santos, N. R. S., de Gonçalves, M. M. C., et al. (2017). The influence of heavy metals on toxicogenetic damage in a Brazilian tropical river. Chemosphere, 185, 852–859. https://doi.org/10.1016/j.chemosphere.2017.07.103.
Montoya-Mejía, M., García-Ulloa, M., Hernández-Llamas, A., Nolasco-Soria, H., & Rodríguez-González, H. (2017). Digestibility, growth, blood chemistry, and enzyme activity of juvenile Oreochromis niloticus fed isocaloric diets containing animal and plant byproducts. Revista Brasileira de Zootecnia, 46(12), 873–882. https://doi.org/10.1590/S1806-92902017001200001.
OCDE. (2012). Fish toxicity testing framework.
Pérez-López, A., Núñez-Nogueira, G., Álvarez-González, C. A., De la Rosa-García, S., Uribe-López, M., Quintana, P., & Peña-Marín, E. S. (2020). Effect of salinity on zinc toxicity (ZnCl2 and ZnO nanomaterials) in the mosquitofish (Gambusia sexradiata). Environmental Science and Pollution Research, 1–10. https://doi.org/10.1007/s11356-020-08851-9.
Pezo, D., Paredes, A., & Bedayán, A. (1992). Determinación de metales pesados bioacumulables en especies icticas de consumo humano en la. Amazonia Peruana, 4(2), 171–181.
Rani, S., Gupta, R. K., & Kanikatehri. (2015). Zinc and cadmium induced changes in the proteolytic and amylolytic enzyme activity in Indian major carps. The Bioscan, 10(2), 613–616.
Rathore, R. M., Kumar, S., & Chakrabarti, R. (2005). Digestive enzyme profile of Cyprinus carpio during ontogenic development. World Aquaculture, 36(2), 37–41.
Raz-Guzmán, M. A. (2000). Moluscos. In E. G. De la Lanza, P. S. Hernández, & P. J. L. Carbajal (Eds.), Organismos Indicadores de la Calidad del Agua y de la Contaminación (Bioindicadores) (pp. 265–307). Mexico: Plaza y Valdés.
Robyt, J. F., & Whelan, W. J. (1968). Starch and its derivates. In J. A. Radley (Ed.). London: Chapman and Hall.
Rungruangsak-Torrissen, K., Moss, R., Andresen, L. H., Berg, A., & Waagbø, R. (2006). Different expressions of trypsin and chymotrypsin in relation to growth in Atlantic salmon (Salmo salar L.). Fish Physiology and Biochemistry, 32(1), 7–23. https://doi.org/10.1007/s10695-005-0630-5.
Salazar-Lugo, R. (2009). The current state of knowledge of the concentrations of cadmium, mercury and lead from aquatic organisms of Venezuela. REDVET. Revista Electrónica de Veterinaria, 10(11), 0–15.
SEMARNAT. (1996). Límites máximos permisibles de contaminantes en las descargas de aguas residuales en aguas y bienes nacionales. Norma Oficial Mexicana, NOM-001-SEMARNAT-1996 33. Mexico.
SEMARNAT. (1999). Especificaciones técnicas para la producción, cuidado y uso de animales de laboratorio. Norma Oficial Mexicana, NOM-062-ZOO-1999 58. Mexico.
Sharaf, S., Dighiesh, H., & Eldanasoury, M. A. (2011). Haematological, biochemical and histological alterations in Nile tilapia Oreochromis niloticus exposed to sublethal concentrations of lead. Egypt Journal of Aquatic Biology and Fish, 15(3), 425–439.
Tchounwou, P. B., Yedjou, C. G., Patlolla, A. K., & Sutton, D. J. (2014). Heavy metals toxicity and the environment, 101, 1–30. https://doi.org/10.1007/978-3-7643-8340-4.
Toledo-Pérez, J. S., & García-Capote, M. C. (2000). Nutrición y Alimentación de Tilapia Cultivada en América Latina y el Caribe. Avances en Nutrición Acuícola IV, 537, 83–137.
Utami, N. R., Widiyaningrum, P., & Iswari, R. S. (2018). Histologic structure of red Nile tilapia fish (Oreochromis niloticus Var.) gill which is exposed to lead acetate. Journal of Physics: Conference Series, 983(1). https://doi.org/10.1088/1742-6596/983/1/012181.
Vázquez, S., Pérez, R., Castro, M., González, M., & Velázquez, V. (2006). Macroinvertebrados bénticos bioindicadores de calidad del agua en 1os Ríos Apatlaco y Amacuzac en Morelos, México. Sociedad Mexicana Historia Natural 3a época, 3(1), 1.
Vázquez-Silva, G., Castro-Mejía, G., Castro-Barrera, T., Castro-Mejía, J., & De Lara, A. R. (2011). Peces indicadores de la calidad del agua registrados en los ríos. Revista Digital E-Bios, 1(27), 27–34.
Versaw, W. K., Cuppett, S. L., Winters, D. D., & Williams, L. E. (1989). An improved colorimetric assay for bacterial lipase in nonfat dry milk. Journal of Food Science, 54(6), 1557–1558. https://doi.org/10.1111/j.1365-2621.1989.tb05159.x.
Villarejo, A. L. (2006). Ecotoxicologico y acccion toxicológica del plomo. Anales de la Real Académia Nacional de Farmacia, 72, 409–422.
Walter, H. E. (1984). Proteinases: methods with hemoglobin, casein and azocoll as substrates. In H. J. Bergmeyer (Ed.), Methods of enzymatic. Analysis. Vol V (pp. 270–277). Verlang Chemie: Weinham.
Whiton, A. B. (1975). River ecology. Oxford: Blackwell Scientific Publications.
Zhai, Q., Wang, H., Tian, F., Zhao, J., Zhang, H., & Chen, W. (2017). Dietary Lactobacillus plantarum supplementation decreases tissue lead accumulation and alleviates lead toxicity in Nile tilapia (Oreochromis niloticus). Aquaculture Research, 48(9), 5094–5103. https://doi.org/10.1111/are.13326.
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The authors appreciate the support given by the biochemistry laboratory of the Academic Division of Biological Sciences of the Juarez Autonomous University of Tabasco (DACBIOL-UJAT) to make possible the realization of this research work. G.N-N recognizes the support provided by the PII SNI-UJAT program.
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Funding support was provided by the Biochemistry laboratory of the Academic Division of Biological Sciences of the Juarez Autonomous University of Tabasco (DACBIOL-UJAT) and the Programa Institucional de Ingreso al Sistema Nacional de Investigadores (PII SNI-UJAT) through G.N-N.
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All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Álvarez-González, C.A., Martínez-Sánchez, L., Peña-Marín. E.S., Guerrero-Zárate, R., Jesús-Ramírez, F., and Morales-García, V. The first draft of the manuscript was written by Uribe-López, M. and Núñez-Nogueira, G., and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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After metal exposure, the fish were sacrificed by induced hypothermia accordingly to the NOM-062-ZOO-1999 protocol, approved by The Ministry of Agriculture, Livestock, Rural Development, Fishing and Food (SEMARNAT 1999), and under the established guidelines for the management of experimental animals of the Juarez Autonomous University of Tabasco (AILAD 2010).
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Álvarez-González, C.A., Martínez-Sánchez, L., Peña-Marín, E.S. et al. Effects on the Growth and Digestive Enzyme Activity in Nile Tilapia Fry (Oreochromis niloticus) by Lead Exposure. Water Air Soil Pollut 231, 477 (2020). https://doi.org/10.1007/s11270-020-04810-9
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DOI: https://doi.org/10.1007/s11270-020-04810-9