Time-dependent hematological responses of Nile tilapia Oreochromis niloticus exposed to an estuarine contaminated water
DOI:
https://doi.org/10.33448/rsd-v10i6.15715Keywords:
Biomarkers; Blood; Environmental monitoring; Fish; Hematimetric indices.Abstract
We aimed to study hematological responses of Oreochromis niloticus experimentally exposed to the contaminated water of the Santos-São Vicente Estuary, testing hypotheses that exposure time to estuarine water promotes deleterious effects on hematological parameters and evaluating the use of erythrocytes and leukocytes alterations as environmental biomarkers. Estuarine water was collected from Largo da Pompeba. For the biological assay, 28 juveniles of O. niloticus (red strain) of both genders were randomly selected from commercial pisciculture. For the biological assay, 28 juveniles of O. niloticus of both sexes were randomly selected from commercial fish farms. The juveniles were kept in estuarine water for 72 and 120 hours and, after exposure, blood was collected by puncture of the caudal vein to determine total erythrocytes, hemoglobin concentration, hematocrit, hematimetric indices and total leukocytes, as lymphocyte, neutrophils, monocytes, eosinophils, and basophils were quantified by blood extensions. To test exposure overtime on hematological variables, we performed a two-factor Multivariate Analysis of Variance. Exposure for 72 hours resulted in immunosuppression as seen by the reduced counts of neutrophils, monocytes, and lymphocytes in the bloodstream, whereas after 120 hours the immune system was stimulated with the increase of all leukocyte cell types. Exposure to estuarine water resulted in marked changes in the leukocyte count of O. niloticus, demonstrating that alterations in white blood cells might be more sensitive biomarkers than red blood parameters.
References
Albergaria-Barbosa, A. C. R., Patire, V. F., Taniguchi, S., Fernandez, W. S., Dias, J. F., & Bícego, M. C. (2017). Mugil curema as a PAH bioavailability monitor for Atlantic west sub-tropical estuaries. Marine Pollution Bulletin, 114(1), 609-614. https://doi.org/10.1016/j.marpolbul.2016.09.039
Albergaria-Barbosa, A. C. R., Silva, D. A. M., Rocha, A. J. S., Taniguchi, S., Patire, V. F., Dias, J. F., & Bícego, M. C. (2018). Evaluation of polycyclic aromatic hydrocarbons bioavailability on Santos Bay (Brazil) through levels of biliary metabolites. Marine Pollution Bulletin, 129(2), 822-828. https://doi.org/10.1016/j.marpolbul.2017.10.006
Alishahi, M., Mohammadi, A., Mesbah, M., & Razi J. M. (2016). Haemato-immunological responses to diazinon chronic toxicity in Barbus sharpeyi. Iranian Journal of Fisheries Sciences, 15(2), 870-885.
Alwan, S. F., Hadi, A. A., & Shokr A. E. (2009). Alterations in hematological parameters of freshwater fish, Tilapia zillii, exposed to aluminum. Journal of Science and its Applications, 3(1), 12-19.
Arkoosh, M. R., Casillas, E., Clemons, E., Kagley, A. N., Olson, R., Reno, P., & Stein, J.E. (1998). Effect of pollution on fish diseases: potential impacts on salmonid populations. Journal of Aquatic Animal Health, 10(2), 182-190. https://doi.org/10.1577/1548-8667(1998)010<0182:eopofd>2.0.co;2
Authman, M. M. N., Zaki, M. S., Khallaf, E. A., & Abbas, H. H. (2015). Use of fish as bio-indicator of the effects of heavy metals pollution. Journal of Aquaculture Research & Development, 6(4), 1-13. https://doi.org/10.4172/2155-9546.1000328
Azevedo, J. S., Lopes, B., Katsumiti, A., Braga, E. S., Roche, H., Ribeiro, C. A. O., & Bebianno, M.J. (2012). Evidence of contamination by oil and oil products in the Santos-São Vicente estuary, São Paulo, Brazil. Brazilian Journal of Oceanography, 60(2), 117–126. https://doi.org/10.1590/S1679-87592012000200002
Azevedo, J. S., Serafim, A., Company, R., Braga, E. S., Fávaro, D. I., & Bebianno, M. J. (2009). Biomarkers of exposure to metal contamination and lipid peroxidation in the benthic fish Cathorops spixii from two estuaries in South America. Brazil. Ecotoxicology, 18, 1001-1010. https://doi.org/10.1007/s10646-009-0370-x
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
Burnett, K.G. (2005). Impacts of environmental toxicants and natural variables on the immune system of fishes. Biochemistry and Molecular Biology of Fishes, 6, 231-253. https://doi.org/10.1016/S1873-0140(05)80011-6
Burns-Naas, L. A., Meade, B. J., & Munson, A. E. (1996). Toxic responses of the immune system. In: C. D. Klaasen (Ed.), The Basic Science of Poisons, Casarett and Doull's Toxicology (p. 419-470). McGraw-Hill.
Capparelli, M. V., Gusso-Choueri, P. K., Abessa, D. M. S., & Mcnamara, J. C. (2019). Seasonal environmental parameters influence biochemical responses of the fiddler crab Minuca rapax to contamination in situ. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 216, 93-100. https://doi.org/10.1016/j.cbpc.2018.11.012
Carmo, C. A., Abessa, D. M. S., & Machado-Neto, J. G. (2012). Metals in muscles of mullet (Mugil curema) from a contaminated estuary: evidences of potential risks to public health. Natural Resources, 2(2), 81–94. https://doi.org/10.6008/ESS2237-9290.2012.002.0007
Cazenave, J., Bacchetta, C., Rossi, A., Ale, A., Campana, M., & Parma, M. J. (2014). Deleterious effects of wastewater on the health status of fish: a field caging study. Ecological Indicators, 38, 104-112. https://doi.org/10.1016/j.ecolind.2013.10.029
Cicero, L. H., Souza, U. P., Rotundo, M. M., Pereira, C. D. S., & Sadauskas-Henrique, H. (2020). Biometric and hematological indices of Mugil curema inhabiting two Neotropical estuaries. Regional Studies in Marine Science, 38, 1-8. https://doi.org/10.1016/j.rsma.2020.101377
Clauss, T. M., Dove, A. D. M., & Arnold, J. E. (2008). Hematologic disorders of fish. Veterinary Clinics of North America: Exotic Animal Practice, 11(3), 445-462. https://doi.org/10.1016/j.cvex.2008.03.007
Companhia Ambiental do Estado de São Paulo. (2015). Qualidade das águas superficiais no Estado de São Paulo. CETESB
Companhia Ambiental do Estado de São Paulo. (2017). Qualidade de águas costeiras no Estado de São Paulo. CETESB
CONAMA. Conselho Nacional do Meio Ambiente. (2005). Dispõe sobre a classificação dos corpos de água e diretrizes ambientais para o seu enquadramento, bem como estabelece as condições e padrões de lançamento de efluentes, e dá outras providências.
Corrêa, S. A. S., Abessa, D. M. S., Santos, L. G., Silva, E. B., & Seriani, R. (2016). Differential blood counting in fish as a non-destructive biomarker of water contamination exposure. Toxicological & Environmental Chemistry, 99(3), 482-491. https://doi.org/10.1080/02772248.2016.1189554
Cruz, A. L., Prado, T. M., Maciel, L. A. S., & Couto, R. D. (2015). Environmental effects on the gills and blood of Oreochromis niloticus exposed to rivers of Bahia, Brazil. Ecotoxicology and Environmental Safety, 111, 23-31.
Davis, A. K., Maney, D. L., & Maerz, J. C. (2008). The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists. Functional Ecology, 22(5), 760-772. https://doi.org/10.1111/j.1365-2435.2008.01467.x
Dunier, M., & Siwicki, A. K. (1993). Effects of pesticides and other organic pollutants in the aquatic environment on immunity of fish: a review. Fish & Shellfish Immunology, 3(6), 423-438. https://doi.org/10.1006/fsim.1993.1042
Fánge, R. (1992). Fish Blood Cells. Fish Physiology, 12(B), 1-54. https://doi.org/10.1016/S1546-5098(08)60008-4
Fernandino, G., Elliff, C. I., Frutuoso, G. A., Silva, E. V. N. M., Gama, G. S., Sousa, J. H. O., & Silva, I.R. (2016). Considerations on the effects of tidal regimes in the movement of floating litter in an estuarine environment: Case study of the estuarine system of Santos-São Vicente, Brazil. Marine Pollution Bulletin, 110(1), 591-595. https://doi.org/10.1016/j.marpolbul.2016.05.080
Gaber, H. S., El-Kasheif, M. A., Ibrahim, S. A., & Authman, M. M. N. (2013). Effect of water pollution in El-Rahawy drainage canal on hematology and organs of freshwater fish. World Applied Sciences Journal, 21(3), 329-341. https://doi.org/10.5829/idosi.wasj.2013.21.3.71192
Garcia, G. G., Miguel, E. J., Gabriel, M. A., & Mingala, C. N. (2016). The corollary effect of heavy metal accumulation in freshwater ponds on the hematological profile of Nile Tilapia (Oreochromis niloticus). Environmental and Experimental Biology, 14, 69–73. https://doi.org/10.22364/eeb.14.10
Ghiraldelli, L., Martins, M. L., Yamashita, M. M., & Jerônimo, G. T. (2006). Hematologia de Oreochromis niloticus (Cichlidae) e Cyprinus carpio (Cyprinidae) mantidos em diferentes condições de manejo e alimentação no Estado de Santa Catarina, Brasil. Acta Scientiarum. Biological Sciences, 28(4), 319-325. https://doi.org/10.4025/actascibiolsci.v28i4.162
Hamza-Chaffai, A. (2014). Usefulness of bioindicators and biomarkers in pollution biomonitoring. International Journal of Biotechnology for Wellness Industries, 3, 19-26. https://doi.org/10.6000/1927-3037.2014.03.01.4
Harabawy, A. S. A., & Ibrahim, A. Th. A. (2014). Sublethal toxicity of carbofuran pesticide on the African catfish Clarias gariepinus (Burchell, 1822): Hematological, biochemical and cytogenetic response. Ecotoxicology and Environmental Safety, 103, 61-67. https://doi.org/10.1016/j.ecoenv.2013.09.022
Hrubec, T. C., & Smith, S.A. (1998). Hematology of fishes. In: B. F. Feldman, J. G. Zinkl, & M. C. Jain (Eds.), Schalm’s Veterinary Hematology (p.1120-1125). Blackburg: Willey-Blackwell.
Ishikawa, N. M., Ranzani-Paiva, M. J. T., Lombardi, J. V., & Ferreira, C. M. (2007). Hematological parameters in Nile Tilápia, Oreochromis niloticus exposed to sub-letal concentrations of mercury. Brazilian Archives of Biology and Technology, 50(4), 619-626. https://doi.org/10.1590/S1516-89132007000400007
Javed, M., & Usmani, N. (2014). Impact of heavy metal toxicity on hematology and glycogen status of fish: a review. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences. B, 85, 889-900. https://doi.org/10.1007/s40011-014-0404-x
Kumar, R., Clermont, G., Vodovotz, Y., & Chow, C. C. (2004). The dynamics of acute inflammation. Journal of Theoretical Biology, 230(2), 145-155. https://doi.org/10.1016/j.jtbi.2004.04.044
Lamparelli, M., Costa, M. P., Prosperi, V., Bevilacqua, J. E., Araujo, R. P. A., Eysink, G. G. J., & Pompeia, S. (2001). Sistema Estuarino de Santos e São Vicente. São Paulo: CETESB. https://doi.org/10.13140/RG.2.1.3288.9764
Lataretu, A., Furnaris, F., & Mitrãnescu, E. (2013). Hematologic profile as stress indicator in fish. Scientific Works. Series C. Veterinary Medicine, 59(1), 102-104.
Li, Z. H., Velisek, J., Grabic, R., Li, P., Kolarova, J., & Randak, T. (2011). Use of hematological and plasma biochemical parameters to assess the chronic effects of a fungicide propiconazole on a freshwater teleost. Chemosphere, 83(4), 572-578. https://doi.org/10.1016/j.chemosphere.2010.12.024
Magalhães, C. A., Taniguchi, S., Lourenço, R. A., & Montone, R. C. (2017). Organochlorine pesticides, PCBs, and PBDEs in liver and muscle tissues of Paralonchurus brasiliensis, Trichiurus lepturus and Cathorops spixii in Santos Bay and surrounding area, São Paulo, Brazil. Regional Studies in Marine Science, 16, 42–48. https://doi.org/10.1016/j.rsma.2017.08.010
Naqvi, G. E. Z., Shoaib, N., & Ali, A. M. (2016). Genotoxic Potential of Pesticides in the Peripheral Blood Erythrocytes of Fish (Oreochromis mossambicus). Pakistan Journal of Zoology, 48(6), 1643-1648.
Ndimele, P. E., Pedro, M. O., Agboola, J. I., Chukwuka, K. S., & Ekwu, A. O. (2017). Heavy metal accumulation in organs of Oreochromis niloticus (Linnaeus, 1758) from industrial effluent-polluted aquatic ecosystem in Lagos, Nigeria. Environmental Monitoring and Assessment, 189, 255. https://doi.org/10.1007/s10661-017-5944-0
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O’hara, R. B., & Wagner, H. (2016). Vegan: Community Ecology Package. R package version 2.3-3. Recovered from: https://CRAN.R-project.org/package=vegan/ (accessed 21 July 2019).
Osman, A. G. M. (2012). Biomarkers in Nile tilapia Oreochromis niloticus niloticus (Linnaeus, 1758) to assess the impacts of river Nile pollution: bioaccumulation, biochemical and tissues biomarkers. Journal of Environmental Protection, 3(8A), 966-977. https://doi.org/10.4236/jep.2012.328112
Osman, A. G. M., Abouelfadl, K. Y., Abd El Reheem, A. E. B. M., Mahmoud, U. M., Kloas, W., & Moustafa, M. A. (2018). Blood Biomarkers in Nile tilapia Oreochromis niloticus niloticus and African Catfish Clarias gariepinus to Evaluate Water Quality of the River Nile. Journal of Fisheries Sciences.com, 12(1), 1-15. https://doi.org/10.21767/1307-234x.1000141
Parekh, H. M., & Tank, S. K. (2015). Studies of hematological parameters of Oreochromis niloticus exposed to Cadmium Chloride (CdCl2, 2H2O). International Journal of Environment, 4(2), 116-127. https://doi.org/10.3126/ije.v4i2.12631
Pereira, D. S. P., Guerra-Santos, B., Moreira, E. L. T., Albinati, R. C. B., & Ayres, M. C. C. (2016). Parâmetros hematológicos e histológicos de Tilápia do Nilo em resposta ao desafio de diferentes níveis de salinidade. Boletim do Instituto de Pesca, 42(3), 635-647.
Prado, L. R. G. B., Felix, C., Abessa, D. M. S., Buruaem, L. M., Abujamara, L. D., Kirschbaum, A. A., & Seriani, R. (2015). Hematological parameters and nuclear abnormalities in peripheral erythrocytes of Achirus lineatus (Pleuronectiformes: Achiridae). Comparative Clinical Pathology, 24, 169-175. https://doi.org/10.1007/s00580-014-1880-3
Ranzani-Paiva, M. J. T., Lombardi, J. V, Maiorino, F. M., Gonçalves, A., & Dias, D. C. (2014). Hematologia e Histologia de tilápia-do-Nilo exposta a concentrações sub-letais de selenito de sódio (Na2SeO3 Se4+). Boletim do Instituto de Pesca, 40, 23-33.
Ranzani-Paiva, M. J. T., Pádua, S. B., Tavares-Dias, M., & Egami, M. I. (2013). Métodos para análise hematológica em peixes. Editora da Universidade Estadual de Maringá-EDUEM.
Roversi, F., Rosman, P. C. C., Harari, J. (2016). Análise da renovação das águas do Sistema Estuarino de Santos usando modelagem computacional. Revista Ambiente & Água, 11(3), 566-585. https://doi.org/10.4136/ambi-agua.1770
Rowley, A. F. (1996). The evolution of inflammatory mediators. Mediators of Inflammation, 5(1), 3-13. https://doi.org/10.1155/S0962935196000014
Saleh, Y. S., & Marie, M. A. S. (2016). Use of Arius thalassinus fish in a pollution biomonitoring study, applying combined oxidative stress, hematology, biochemical and histopathological biomarkers: a baseline field study. Marine Pollution Bulletin, 106(1-2), 308-322. https://doi.org/10.1016/j.marpolbul.2016.03.030.
Santos, C. R., Cavalcante, A. L. M., Hauser-Davis, R. A., Lopes, R. M., & Mattos, R. C. O. C. (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
Santos, M. A., & Hall, A. (1990). Influence of inorganic lead on the biochemical blood composition of the eel, Anguilla anguilla L. Ecotoxicology and Environmental Safety, 20(1), 7-9. https://doi.org/10.1016/0147-6513(90)90040-C
Saravanan, M., Kim, J. Y., Kim, H. N., Kim, S. B., Ko, D. H., & Hur, J. H. (2015). Ecotoxicological impacts of isoprothiolane on freshwater fish Cyprinus carpio fingerlings: a multi-biomarker assessment. Journal of the Korean Society for Applied Biological Chemistry, 58, 491-499. https://doi.org/10.1007/s13765-015-0066-2
Saravanan, M., Kumar, K. P., & Ramesh, M. (2011). Hematological and biochemical responses of freshwater teleost fish Cyprinus carpio (Actinopterygii: Cypriniformes) during acute and chronic sublethal exposure to lindane. Pesticide Biochemistry and Physiology, 100(3), 206-211. https://doi.org/10.1016/j.pestbp.2011.04.002
Schreck, C. B. (2010). Stress and fish reproduction: the roles of allostasis and hormesis. General and Comparative Endocrinology, 165(3), 549-556. https://doi.org/10.1016/j.ygcen.2009.07.004
Schreck, C. B., & Tort, L. (2016). The concept of stress in fish. Fish Physiology, 35, 1-34. https://doi.org/10.1016/B978-0-12-802728-8.00001-1
Seriani, R., Abessa, D. M. S., Kirschbaum, A. A., Pereira, C. D. S., Romano, P., & Ranzani-Paiva, M. J. T. (2011). Relationship between water toxicity and hematological changes in Oreochromis niloticus. Brazilian Journal of Aquatic Science and Technology, 15(2), 47-53. https://doi.org/10.14210/bjast.v15n2.p47-53
Seriani, R., Abessa, D. M. S., Pereira, C. D. S., Kirschbaum, A. A., Assunção, A., & Ranzani-Paiva, M. J. T. (2013). Influence of seasonality and pollution on the hematological parameters of the estuarine fish Centropomus parallelus. Brazilian Journal of Oceanography, 61(2), 105-111. https://doi.org/10.1590/S1679-87592013000200003
Seriani, R., Moreira, L. B., Abessa, D. M. S., Abujamara, L. D., Carvalho, N. S. B., Maranho, L. A., & Ranzani-Paiva, M. J. T. (2010). Hematological analysis of Micropogonias furnieri, Desmarest, 1823, Sciaenidae, from two estuaries of Baixada Santista, São Paulo Brazil. Brazilian Journal of Oceanography, 58(3), 87-92. https://doi.org/10.1590/S1679-87592010000700011
Seriani, R., Ranzani-Paiva, M. J. T., Gonçalves, A., Siqueira, S. R., & Lombardi, J. V. (2012). Determination of selenium toxicity to Oreochromis niloticus based on hematological parameters. Acta Scientiarum. Biological Sciences, 34(2), 125-131. https://doi.org/10.4025/actascibiolsci.v34i2.8755
Shah, N., Khan, A., Ali, R., Marimuthu, K., Uddin, M. N., Rizwan, M., & Khisroon, M. (2020). Monitoring Bioaccumulation (in Gills and Muscle Tissues), Hematology, and Genotoxic Alteration in Ctenopharyngodon idella Exposed to Selected Heavy Metals. BioMed Research International, 2020,1-16. https://doi.org/10.1155/2020/6185231
Shahjahan, M., Uddin, M. H., Bain, V., & Haque, M. M. (2018). Increased water temperature altered hemato-biochemical parameters and structure of peripheral erythrocytes in striped catfish Pangasianodon hypophthalmus. Fish Physiology and Biochemistry, 44, 1309-1318. https://doi.org/10.1007/s10695-018-0522-0
Sharma, M., Chadha, P., & Borah, M. K. (2015). Fish behaviour and immune response as a potential indicator of stress caused by 4-nonylphenol. American Journal of BioScience, 3(6), 278-83. https://doi.org/10.11648/j.ajbio.20150306.21
Shen, Y., Wang, D., Zhao, J., & Chen, X. (2018). Fish red blood cells express immune genes and responses. Aquaculture and Fisheries, 3(1), 14-21. https://doi.org/10.1016/j.aaf.2018.01.001
Silva, E. B., Corrêa, S. A. S., Abessa, D. M. S., Silva, B. F. X., Rivero, D. H. R. F., & Seriani, R. (2018). Mucociliary transport, differential white blood cells, and cyto-genotoxicity in peripheral erythrocytes in fish from a polluted urban pond. Environmental Science and Pollution Research, 25, 2683-2690. https://doi.org/10.1007/s11356-017-0729-0
Silva, R. D., Rocha, L. O., Fortes, B. D. A., Vieira, D., & Fioravanti, M. C. S. (2012). Parâmetros hematológicos e bioquímicos da tilápia-do-Nilo (Oreochromis niloticus L.) sob estresse por exposição ao ar. Pesquisa Veterinária Brasileira, 32(1), 99-107. https://doi.org/10.1590/S0100-736X2012001300017
Souza, A. C., Taniguchi, S., Figueira, C. L., Montone, R. C., Bícego, M. C., & Martins, C. C. (2018). Historical records and spatial distribution of high hazard PCBs levels in sediments around a large South American industrial coastal area (Santos Estuary, Brazil). Journal of Hazardous Materials, 360, 428–435. http://dx.doi.org/10.1016/j.jhazmat.2018.08.041
Sweilum, M. A. (2006). Effect of sublethal toxicity of some pesticides on growth parameters, haematological properties and total production of Nile tilapia (Oreochromis niloticus L.) and water quality of ponds. Aquaculture Research, 37(11), 1079-1089. https://doi.org/10.1111/j.1365-2109.2006.01531.x
Thummabancha, K., Onparn, N., & Srisapoome, P. (2016). Analysis of hematologic alterations, immune responses and metallothionein gene expression in Nile tilapia (Oreochromis niloticus) exposed to silver nanoparticles. Journal of Immunotoxicology, 13(6), 909-917. https://doi.org/10.1080/1547691X.2016.1242673
Tort, L. (2011). Stress and immune modulation in fish. Developmental & Comparative Immunology, 35(12), 1366-1375. https://doi.org/10.1016/j.dci.2011.07.002
Ueda, I. K., Egami, M. I., Sasso, W. S., & Matushima, E. R. (1997). Estudos hematológicos em Oreochromis niloticus (Linnaeus, 1758) (Cichlidae, Teleostei): part I. Brazilian Journal of Veterinary Research and Animal Science, 34(5), 270-275. https://doi.org/10.11606/issn.2318-3659.v34i5p270-275.
Ueda, I. K., Egami, M. I., Sasso, W. S., & Matushima, E. R. (2001). Cytochemical aspects of the peripheral blood cells of Oreochromis (Tilapia) niloticus. (Linnaeus, 1758) (Cichlidae, Teleostei): part II. Brazilian Journal of Veterinary Research and Animal Science, 38(6), 273-277. https://doi.org/10.1590/S1413-
Van Der Oost, R., Beyer, J., & Vermeulen, N. P. (2003). Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environmental Toxicology and Pharmacology, 13(2), 57-149. https://doi.org/10.1016/s1382-6689(02)00126-6
Vasseur, P., & Cossu-Leguile, C. (2003). Biomarkers and community indices as complementary tools for environmental safety. Environment International, 28(8), 711-717. https://doi.org/10.1016/S0160-4120(02)00116-2
Ventura, A. S., Corsini, F. E., & Gabriel, A. M. A. (2015). Hematologia como biomarcador de contaminação ambiental em peixe. Nutritime, 12(6), 4500-4507.
Wintrobe, M. M. (1934). Variations in the size and hemoglobin content of erythrocytes in the blood of various vertebrates. Folia Haematologica, 51, 32-49.
Witeska, M. (2005). Stress in fish-hematological and immunological effects of heavy metals. Electronic Journal of Ichthyology, 1, 35-41.
Witeska, M. (2015). Anemia in teleost fishes. Bulletin of the European Association of Fish Pathologists, 35(4), 148-160.
Xu, H., Zhang, X., Li, H., Li, C., Huo, X. J., Hou, L. P., & Gong, Z. (2018). Immune response induced by major environmental pollutants through altering neutrophils in zebrafish larvae. Aquatic Toxicology, 201, 99-108. https://doi.org/10.1016/j.aquatox.2018.06.002
Yacoub, A. M., Sabra, S. M. M., & Al-Kourashi, M. K. D. (2018). Meat quality and hematological indices of Oreochromis niloticus fish experimentally exposed to Escherichia coli toxins. International Journal of Biotechnology and Bioengineering, 4(7), 139-148.
Yada, T., & Tort, L. (2016). Stress and disease resistance: immune system and immunoendocrine interactions. Fish Physiology, 35, 365–403. https://doi.org/10.1016/b978-0-12-802728-8.00010-2
Yaghoobi, Z., Safahieh, A., Ronagh, M. T., Movahedinia, A., & Mousavi, S. M. (2017). Hematological changes in yellowfin seabream (Acanthopagrus latus) following chronic exposure to bisphenol A. Comparative Clinical Pathology, 26, 1305-1313. https://doi.org/10.1007/s00580-017-2530-3
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2021 Aline Raquel Gomes Guerra; Ursulla Pereira Souza; Rafael Mendonça Duarte; Fábio Cop Ferreira; José Reinaldo Oliveira Conceição; Olivia Menossi
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
1) Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
2) Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
3) Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.