Hematological and histological parameters of Nile tilapia in response to the challenge of different salinity levels
DOI:
https://doi.org/10.20950/1678-2305.2016v42n3p635Keywords:
gills, chloride cells, electrophoresis, globulins, toleranceAbstract
This research aimed to evaluate the influence of different levels of salinity on growth performance, haematological parameters and the cells of Nile tilapia chloride. 144 fish were used during a 97 day trial period, submitted to four experimental treatments of 0 ‰, 10 ‰, 20 ‰ and 25 ‰ salinity. Sampling were collected for monitoring of performance parameters, blood samples to determine the erythrocyte count, packed cell volume, hemoglobin concentration, the erythrocyte indices, the count of thrombocytes and leukocytes and the electrophoretic profile of serum proteins. Gill samples were also collected for counting the number of cells chloride. Significant differences were found in hemoglobin concentration, the total plasma proteins and the number of erythrocytes (p <0.05). There was no difference in the number of white blood cells and thrombocytes. Serum proteins showed differences (p <0.05) from pre-albunima fractions, α1-globulin, α2-globulin, βglobulin, and γ-globulin. There was a direct relationship between the number of chloride cells and increase in salinity levels (p <0.05). The CBC constituents, the electrophoretic profile of proteins as well as quantitative analysis of gill chloride cells can serve as indicares mechanism of adaptation and tolerance to salinity in Nile tilapia.
References
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AKINROTIMI, O.A.; UEDEME-NAA, B.; AGOKEI, E.O. 2010 Effects of acclimation on haematological parameters of Tilapia guineensis (Bleeker, 1862). Science World Journal, 5: 1-4.
AL-AHMED, A.A. 2001 A review of tilapia culture in Kuwait. Word Aquaculture, 32: 47-48. AL-AMOUNDI, M.M. 1987 Acclimation of commercially cultured Oreochromis species to seawater na experimental study. Aquaculture, 65: 333-342.
ALTUN, T.; SARIHAN, E. 2008 Effects of freshwater and seawater on growth, total testosterone levels and testis development of tilapias. Journal of Animal and Veterinary Advances, 5: 657-662.
ARANA, L. V. 2004 Princípios químicos de qualidade de água em aquicultura: uma revisão para peixes e camarões. 2a ed. Florianópolis. UFSC, 331p.
AVELLA, M.; BERHAUT, J.; BORNANCIN, M. 1993 Salinity tolerance of two tropical fishes, Oreochromis aureus and O. niloticus. I. Biochemical and morphological changes in the gill epithelium. Journal of Fish Biology, 42: 243í 254.
BALDISSEROTO, B. 2009 Fisiologia de peixes aplicada í piscicultura. 2a ed. Santa Maria. UFSM, p. 349.
BARBIERI, E.; BONDIOLI, A. C. V. 2013 Acute toxicity of ammonia in Pacu fish ( Piaractus mesopotamicus , Holmberg, 1887) at different temperatures levels. Aquaculture Research, 46(3):565-571.
BARTON, B.A.; IWAMA, G.K. 1991 Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annual Review of Fish Diseases, 1: 3-26.
BRAUNER, C.J.; WANG, T.; JENSEN, F.B. 2002 Influence of hyperosmotic shrinkage and βadrenergic stimulation on red blood cell volume regulation and oxygen binding properties in rainbow trout and carp. Journal of Comparative Physiology, 172: 251í 262.
CAZENAVE, J.; BACCHETTA, C.; PARMA, M.J.; SCARABOTTI, P.A.; WUNDERLIN, D.A. 2009 Multiple biomarkers responses in Prochilodus lineatus allowed assessing changes in the walter quality of Salado River basin (Santa Fe,
Argentina). Environmental Pollution, 157: 3025- 3033.
CHEESBROUGH, M. 2005 Distinct Laboratory Practice in Tropical Countries. 2a ed. United Kingdom, Cambridge University Press. 434p.
CHERVINSKI, J.; HERING, E. 1973 Tilapia zillii (Gervais) (Pices, Cichlidae) and it’s adaptability to various saline conditions. Aquaculture, 2: 23-29.
CIONI, C.; MERCH, C.; CATALDI, E.; CATAUDELLA, S. 1991 Fine structure of chloride cells in freswater and seawater
adapted Oreochromis mossambicus (Peters). Journal of Fish Biology, 39: 197-209.
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: 760-772.
EMELIKE, F.O.; ODEYENUMA, C.; JEREMIAH, Z.A.; OBIGWE, B.U. 2008 The use of anti-coogulated and defribinated blood samplesfor the evaluation of red cell osmotic fragility. International Journal of Natural and Applied Sciences, 4: 204-208.
FAGHALY, A.M.; EZZAT. A. A.; SHABANA, M. B. 1973 Effects of temperature and salinity changes on the blood characteristics of Tilapia zilli G. in Egyptian littoral lakes. Comparative Biochemistry and Physiology, 46: 183-193.
FAZIO, F.; MARAFIOTI, S.; TORRE, A.; SANFILIPPO, M.; PANZERA, M.; FAGGIO, C. 2013 Haematological and serum protein profiles of Mugil cephalus: effect of two different habitats. Ichthyological Research, 60: 36-42.
FOSKETT, J.K.; LOSGDON, C.D.; TURNER, T.; MACHEN, T.E; BERN, H.A. 1981 Differentiation of chloride extrusion
mechanism during seawater adaptation of a teleost fish, the cichlid Sarotherodon mossambicus. The Journal of Experimental Biology, 93: 209-224.
GARCÍA-ULLOA,M.; VILLA, R.L.; MARTÍNEZ, T.M. 2001 Growth and feed utilization of the tilápia hydrid Oreochromis mossambicus x O. niloticus cultured at different salinities under controlled laboratory conditions. Journal of the
World Aquaculture Society, 32: 117-121.
GICKING, J.C.; FOLEY, A.M.; HARR, K.E.; RASKIN, R.E.; JACOBSON, E. 2004 Plasma protein electrophoresis of the atantic loggerhead sea turtle, Caretta caretta. Journal of Herpetological Medicine and Surgary, 14: 13-18.
GUNER, Y.; OZDEN, O.; CAGIRGAN, H.; ALTUNOK, M.; KIZAK, V. 2004 Effects of salinity on the osmoregulatory functions of the gills in nile tilapia (Oreochromis niloticus). Turkish Journal of Veterinary & Animal Sciences, 29: 1259-1266.
HESSER, E. F. 1960 Methods for routine on fish haematology. The Progressive Fish Culturist, 22: 164-171.
HRUBEC, T.C.; SMITH, S.A. 1998 Hematology of fishes. In: WEISS,D.J.;WARDROP,K,J. Schalm´s Veterinary Hematology. 5a ed. Blackburg. Wiley-Blackwell. p. 1120-1125.
IQBAL, K. J.; QURESHI, N. A.; ASHRAF , M.; REHMAN, M. H. U.; KHAN, N.; JAVID, A.; ABBAS, F.; MUSHTAQ, M. M. H.; RASOOL, F.; MAJEED, H. 2012 Effect of different salinity levels on growth and survival of nile tilapia (Oreochromis niloticus). The Journal of Animal and Plant Sciences, 22: 919-922.
JAMIL, K.; SHOAIB, M.; AMEER, F.; HONG, L. 2004 Salinity tolerance and growth response of juvenile Oreochromis mossambicus. Journal of Ocean University of China, 3: 53-55.
JENSEN, F.B.; LECKLIN, T.; BUSK, M.; BURY, N.R.; WILSON, R.W.; WOOD, C.M.; GROSELL, M. 2002 Physiological impact of salinity increase at organism and red blood cell levels in the European flounder (Platichthys flesus). Journal
of Experimental Marine Biology and Ecology, 274: 159í 174.
KARSI, A.; YILDIZ, H.Y. 2005 Secondary stress response of nile tilapia, Oreochromis niloticus, after direct transfer to different salinities. Tarim Bilimleri Dergisi, 11: 39-141.
KATALOG, S.; PARLAK, H. 2004 The effects of pollution on haematological parameters of Black goby in foca and aliaga boys. E.U. Journal of Fisheries and Aquatic Sciences. 21: 113-117.
KUBITZA, F. 2003 Qualidade da água no cultivo de peixes e camarões. 1a ed. Jundiaí: Acqua Supre. 229p.
LABARRERE, C.R. 2011 Perfil sanguíneo de híbridos de surubim (Pseudoplatystoma reticulatum X P. coruscans) criados em diferentes densidades de estocagem. Belo Horizonte. 62p. Dissertação de Mestrado. Universidade Federal de Minas Gerais). <http://www.bibliotecadigital.ufmg.br/dspace/handle/1843/106> Acesso em 04 jun. 2013.
LARSON, P.H. 1974 Serum proteins diagnostic significance of electrophoretic patterns. Human Pathology, 5: 629-640.
LEAMASTER, B.R.; BROCK, J.A.; FUJIOKA, R.S.; NAKAMURA, R.M. 1990 Hematologic and blood chemistry values for Sarotherodon melanotheron and a red hybrid tilapia in freshwater and seawater. Comparative Biochemistry and Physiology, 97: 525-529.
MARTINS, M.L.; MORAES, F.R.; FUJIMOTO, R.Y.; NOMURA, D.T.; FENERICK, J. 2002 Respostas do híbrido tambacu (Piaractus mesopotamicusHolmberg, 1887 macho x Colossoma macropomum Cuvier,1818 fêmea) a estímulos
simples ou consecutivos de captura. Boletim Instituto de Pesca, 28: 195-204.
MARTINS, M.L.; PILARSKY, F.; ONAKA, E.M.; NOMURA, D.T.; FENERICK, JR. J.; RIBEIRO, K.; YIAZAKI, D.M.Y.; CASTRO, M.P; MALHEIROS, E.B. 2004 Hematologia e resposta inflamatória aguda em Oreochromis niloticus (Osteichthyes: Cichlidae) submetida aos estímulos único e consecutivo de estresse de captura. Boletim Instituto de Pesca, 30: 71-80.
MARUYAMAL, K.R.; VAL, A.L. 1998 Efeito da salinidade sobre a homeostase iônica e parí¢metros hematológicos de Colossoma macropomum (Cuvier, 1818). In: CONGRESSO DA SOCIEDADE BRASILEIRA DE ZOOLOGIA, 22., CBZ 1998, Recife. Anais... Recife: SBZ.
McCORNICK, S.D. Endocrine cortrol of osmoregulation in teleost fish. 2001 American Zoologist, 41: 781-794.
MORGADO, I.; SANTOS, C.R.A.; JACINTO, R.; POWER, D.M. 2007 Regulation of transthyretin by thyroid hormones in fish. General and Comparative Endocrinology, 152: 189í 197.
MUSA, S. O.; OMOREGIE, E. 1999 Haematological changes in the mud fish Clarias gariepinus exposed to malachite green. Journal of Aquatic Sciences, 14: 37 í 47.
NAOUM, P.C. 1990 Eletroforese í técnicas e diagnóstico. 2ª ed. São Paulo. Santos. 154p. OKECHUKWU, E. O.; ANSA, J.; BALOGUN, J. K. 2007 Effects of acute nominal doses of chlorpyrifos-ethyl on some haematological indices of African catfish Clarias gariepinus Journal of Fisheries International, 2: 190 í 194.
PITOMBEIRA, M.S.; MARTINS, J.M. 1966 A direct method for while blood cell count in fishes. Arquivos da Estação de Biologia Marinha da Universidade Federal do Ceará, 6: 605.
POWELL, M.D.; PARSONS, H.J.; NOWAY, B.F. 2001 Physiological effects of freshwater bathing of Atlantic salmon (Salmo salar) as a treatment for amoebic gill disease. Aquaculture, 199: 259-266.
PROPHET, E.B.; MILLS, B.; ARRINGTON, J.B.; SOBIN, L.H. 1992 Laboratory Methods in Histotechnology. 3a ed. Washington, DC. Armed Force Registry of Pathology, 279p.
RAZANI-PAIVA, M.J.T.; ISHIKAWA, C.M.; EIRAS, A.C.; SILVEIRA, V.R. 2004 Effects of an experimental challenge with Mycobacterium marinum on the blood parameters of Nile tilapia, Oreochromis niloticus (Linnaeus, 1757).
Brazilian Archives of Biology and Technology, 47: 945-953.
ROSENFELD, G. 1947 Método rápido de coloração de esfregaços de sangue. Noções práticas sobre corantes pancrônicos e estudos de diversos fatores. Memórias de Instituto Butantã, 20: 315-328.
SCHUTT, D.A.; LEHMANN, J.; GUERLICH, R.; HAMERS, R. 1997 Haemotology of swondtail xiphiphorus helleri 1: Blood parameters and light microscopy of blood cells. Journal Applied Icthyology, 13: 83-89.
STICKNEY, R.R. Tilapia tolerance of saline waters: a review. 1986 Progressive Fish Culturist, 48: 161-167.
SURESH, A.V.; LIN, C.K. 1992 Tilapia culture in saline waters: a review. Aquaculture, 106: 201-226.
THRALL, M.A. 2006. Hematologia e Bioquímica Clínica Veterinária. 1ª ed. São Paulo. Roca, 582p.
UTIDA, S.; KAMIYA, M.; SHIRAI, N. 1971 Relationship between the activity of Na/K activated adenosinetriphosphatase and the number of chloride cells in eel gills with special reference to seawater adaptation. Comparative Biochemistry and Physiology, 38: 443-448.
VERDEGEM, M.C.J.; HILBRANDS, A.D.; BOON, J.H. 1997 Influence of salinity and dietary composition on blood parameter values of hybrid red tilapia, Oreochromis niloticus (Linnaeus) x O. mossambicus (Peters). Aquaculture Research, 28: 453-459.
WATANABE, W.O.; KUO, C.; HUANG, M. 1985 Salinity tolerance of Nile tilapia fry (Oreochromis niloticus), spawned and hatched at various salinities. Aquaculture, 48: 159-176.
YADA, T.; NAKANISHI, T. 2002 Interaction between endocrime and immune system in fish. International Journal of Review in Cytology, 220: 35-92.
ZOWAIL, M.E.M.; El í DEEB, S.I.; El í SERAFY, S.S.; RIZKALLA, E.H.; El-SAIED, H. 1994 Biochemical genetic studies of serum properties of family Mugillidae in two different habitats of Egyptian water. Bulletin National Institute Oceanography Fish Egypt, 20: 175-190.
AKINROTIMI, O.A.; UEDEME-NAA, B.; AGOKEI, E.O. 2010 Effects of acclimation on haematological parameters of Tilapia guineensis (Bleeker, 1862). Science World Journal, 5: 1-4.
AL-AHMED, A.A. 2001 A review of tilapia culture in Kuwait. Word Aquaculture, 32: 47-48. AL-AMOUNDI, M.M. 1987 Acclimation of commercially cultured Oreochromis species to seawater na experimental study. Aquaculture, 65: 333-342.
ALTUN, T.; SARIHAN, E. 2008 Effects of freshwater and seawater on growth, total testosterone levels and testis development of tilapias. Journal of Animal and Veterinary Advances, 5: 657-662.
ARANA, L. V. 2004 Princípios químicos de qualidade de água em aquicultura: uma revisão para peixes e camarões. 2a ed. Florianópolis. UFSC, 331p.
AVELLA, M.; BERHAUT, J.; BORNANCIN, M. 1993 Salinity tolerance of two tropical fishes, Oreochromis aureus and O. niloticus. I. Biochemical and morphological changes in the gill epithelium. Journal of Fish Biology, 42: 243í 254.
BALDISSEROTO, B. 2009 Fisiologia de peixes aplicada í piscicultura. 2a ed. Santa Maria. UFSM, p. 349.
BARBIERI, E.; BONDIOLI, A. C. V. 2013 Acute toxicity of ammonia in Pacu fish ( Piaractus mesopotamicus , Holmberg, 1887) at different temperatures levels. Aquaculture Research, 46(3):565-571.
BARTON, B.A.; IWAMA, G.K. 1991 Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annual Review of Fish Diseases, 1: 3-26.
BRAUNER, C.J.; WANG, T.; JENSEN, F.B. 2002 Influence of hyperosmotic shrinkage and βadrenergic stimulation on red blood cell volume regulation and oxygen binding properties in rainbow trout and carp. Journal of Comparative Physiology, 172: 251í 262.
CAZENAVE, J.; BACCHETTA, C.; PARMA, M.J.; SCARABOTTI, P.A.; WUNDERLIN, D.A. 2009 Multiple biomarkers responses in Prochilodus lineatus allowed assessing changes in the walter quality of Salado River basin (Santa Fe,
Argentina). Environmental Pollution, 157: 3025- 3033.
CHEESBROUGH, M. 2005 Distinct Laboratory Practice in Tropical Countries. 2a ed. United Kingdom, Cambridge University Press. 434p.
CHERVINSKI, J.; HERING, E. 1973 Tilapia zillii (Gervais) (Pices, Cichlidae) and it’s adaptability to various saline conditions. Aquaculture, 2: 23-29.
CIONI, C.; MERCH, C.; CATALDI, E.; CATAUDELLA, S. 1991 Fine structure of chloride cells in freswater and seawater
adapted Oreochromis mossambicus (Peters). Journal of Fish Biology, 39: 197-209.
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: 760-772.
EMELIKE, F.O.; ODEYENUMA, C.; JEREMIAH, Z.A.; OBIGWE, B.U. 2008 The use of anti-coogulated and defribinated blood samplesfor the evaluation of red cell osmotic fragility. International Journal of Natural and Applied Sciences, 4: 204-208.
FAGHALY, A.M.; EZZAT. A. A.; SHABANA, M. B. 1973 Effects of temperature and salinity changes on the blood characteristics of Tilapia zilli G. in Egyptian littoral lakes. Comparative Biochemistry and Physiology, 46: 183-193.
FAZIO, F.; MARAFIOTI, S.; TORRE, A.; SANFILIPPO, M.; PANZERA, M.; FAGGIO, C. 2013 Haematological and serum protein profiles of Mugil cephalus: effect of two different habitats. Ichthyological Research, 60: 36-42.
FOSKETT, J.K.; LOSGDON, C.D.; TURNER, T.; MACHEN, T.E; BERN, H.A. 1981 Differentiation of chloride extrusion
mechanism during seawater adaptation of a teleost fish, the cichlid Sarotherodon mossambicus. The Journal of Experimental Biology, 93: 209-224.
GARCÍA-ULLOA,M.; VILLA, R.L.; MARTÍNEZ, T.M. 2001 Growth and feed utilization of the tilápia hydrid Oreochromis mossambicus x O. niloticus cultured at different salinities under controlled laboratory conditions. Journal of the
World Aquaculture Society, 32: 117-121.
GICKING, J.C.; FOLEY, A.M.; HARR, K.E.; RASKIN, R.E.; JACOBSON, E. 2004 Plasma protein electrophoresis of the atantic loggerhead sea turtle, Caretta caretta. Journal of Herpetological Medicine and Surgary, 14: 13-18.
GUNER, Y.; OZDEN, O.; CAGIRGAN, H.; ALTUNOK, M.; KIZAK, V. 2004 Effects of salinity on the osmoregulatory functions of the gills in nile tilapia (Oreochromis niloticus). Turkish Journal of Veterinary & Animal Sciences, 29: 1259-1266.
HESSER, E. F. 1960 Methods for routine on fish haematology. The Progressive Fish Culturist, 22: 164-171.
HRUBEC, T.C.; SMITH, S.A. 1998 Hematology of fishes. In: WEISS,D.J.;WARDROP,K,J. Schalm´s Veterinary Hematology. 5a ed. Blackburg. Wiley-Blackwell. p. 1120-1125.
IQBAL, K. J.; QURESHI, N. A.; ASHRAF , M.; REHMAN, M. H. U.; KHAN, N.; JAVID, A.; ABBAS, F.; MUSHTAQ, M. M. H.; RASOOL, F.; MAJEED, H. 2012 Effect of different salinity levels on growth and survival of nile tilapia (Oreochromis niloticus). The Journal of Animal and Plant Sciences, 22: 919-922.
JAMIL, K.; SHOAIB, M.; AMEER, F.; HONG, L. 2004 Salinity tolerance and growth response of juvenile Oreochromis mossambicus. Journal of Ocean University of China, 3: 53-55.
JENSEN, F.B.; LECKLIN, T.; BUSK, M.; BURY, N.R.; WILSON, R.W.; WOOD, C.M.; GROSELL, M. 2002 Physiological impact of salinity increase at organism and red blood cell levels in the European flounder (Platichthys flesus). Journal
of Experimental Marine Biology and Ecology, 274: 159í 174.
KARSI, A.; YILDIZ, H.Y. 2005 Secondary stress response of nile tilapia, Oreochromis niloticus, after direct transfer to different salinities. Tarim Bilimleri Dergisi, 11: 39-141.
KATALOG, S.; PARLAK, H. 2004 The effects of pollution on haematological parameters of Black goby in foca and aliaga boys. E.U. Journal of Fisheries and Aquatic Sciences. 21: 113-117.
KUBITZA, F. 2003 Qualidade da água no cultivo de peixes e camarões. 1a ed. Jundiaí: Acqua Supre. 229p.
LABARRERE, C.R. 2011 Perfil sanguíneo de híbridos de surubim (Pseudoplatystoma reticulatum X P. coruscans) criados em diferentes densidades de estocagem. Belo Horizonte. 62p. Dissertação de Mestrado. Universidade Federal de Minas Gerais). <http://www.bibliotecadigital.ufmg.br/dspace/handle/1843/106> Acesso em 04 jun. 2013.
LARSON, P.H. 1974 Serum proteins diagnostic significance of electrophoretic patterns. Human Pathology, 5: 629-640.
LEAMASTER, B.R.; BROCK, J.A.; FUJIOKA, R.S.; NAKAMURA, R.M. 1990 Hematologic and blood chemistry values for Sarotherodon melanotheron and a red hybrid tilapia in freshwater and seawater. Comparative Biochemistry and Physiology, 97: 525-529.
MARTINS, M.L.; MORAES, F.R.; FUJIMOTO, R.Y.; NOMURA, D.T.; FENERICK, J. 2002 Respostas do híbrido tambacu (Piaractus mesopotamicusHolmberg, 1887 macho x Colossoma macropomum Cuvier,1818 fêmea) a estímulos
simples ou consecutivos de captura. Boletim Instituto de Pesca, 28: 195-204.
MARTINS, M.L.; PILARSKY, F.; ONAKA, E.M.; NOMURA, D.T.; FENERICK, JR. J.; RIBEIRO, K.; YIAZAKI, D.M.Y.; CASTRO, M.P; MALHEIROS, E.B. 2004 Hematologia e resposta inflamatória aguda em Oreochromis niloticus (Osteichthyes: Cichlidae) submetida aos estímulos único e consecutivo de estresse de captura. Boletim Instituto de Pesca, 30: 71-80.
MARUYAMAL, K.R.; VAL, A.L. 1998 Efeito da salinidade sobre a homeostase iônica e parí¢metros hematológicos de Colossoma macropomum (Cuvier, 1818). In: CONGRESSO DA SOCIEDADE BRASILEIRA DE ZOOLOGIA, 22., CBZ 1998, Recife. Anais... Recife: SBZ.
McCORNICK, S.D. Endocrine cortrol of osmoregulation in teleost fish. 2001 American Zoologist, 41: 781-794.
MORGADO, I.; SANTOS, C.R.A.; JACINTO, R.; POWER, D.M. 2007 Regulation of transthyretin by thyroid hormones in fish. General and Comparative Endocrinology, 152: 189í 197.
MUSA, S. O.; OMOREGIE, E. 1999 Haematological changes in the mud fish Clarias gariepinus exposed to malachite green. Journal of Aquatic Sciences, 14: 37 í 47.
NAOUM, P.C. 1990 Eletroforese í técnicas e diagnóstico. 2ª ed. São Paulo. Santos. 154p. OKECHUKWU, E. O.; ANSA, J.; BALOGUN, J. K. 2007 Effects of acute nominal doses of chlorpyrifos-ethyl on some haematological indices of African catfish Clarias gariepinus Journal of Fisheries International, 2: 190 í 194.
PITOMBEIRA, M.S.; MARTINS, J.M. 1966 A direct method for while blood cell count in fishes. Arquivos da Estação de Biologia Marinha da Universidade Federal do Ceará, 6: 605.
POWELL, M.D.; PARSONS, H.J.; NOWAY, B.F. 2001 Physiological effects of freshwater bathing of Atlantic salmon (Salmo salar) as a treatment for amoebic gill disease. Aquaculture, 199: 259-266.
PROPHET, E.B.; MILLS, B.; ARRINGTON, J.B.; SOBIN, L.H. 1992 Laboratory Methods in Histotechnology. 3a ed. Washington, DC. Armed Force Registry of Pathology, 279p.
RAZANI-PAIVA, M.J.T.; ISHIKAWA, C.M.; EIRAS, A.C.; SILVEIRA, V.R. 2004 Effects of an experimental challenge with Mycobacterium marinum on the blood parameters of Nile tilapia, Oreochromis niloticus (Linnaeus, 1757).
Brazilian Archives of Biology and Technology, 47: 945-953.
ROSENFELD, G. 1947 Método rápido de coloração de esfregaços de sangue. Noções práticas sobre corantes pancrônicos e estudos de diversos fatores. Memórias de Instituto Butantã, 20: 315-328.
SCHUTT, D.A.; LEHMANN, J.; GUERLICH, R.; HAMERS, R. 1997 Haemotology of swondtail xiphiphorus helleri 1: Blood parameters and light microscopy of blood cells. Journal Applied Icthyology, 13: 83-89.
STICKNEY, R.R. Tilapia tolerance of saline waters: a review. 1986 Progressive Fish Culturist, 48: 161-167.
SURESH, A.V.; LIN, C.K. 1992 Tilapia culture in saline waters: a review. Aquaculture, 106: 201-226.
THRALL, M.A. 2006. Hematologia e Bioquímica Clínica Veterinária. 1ª ed. São Paulo. Roca, 582p.
UTIDA, S.; KAMIYA, M.; SHIRAI, N. 1971 Relationship between the activity of Na/K activated adenosinetriphosphatase and the number of chloride cells in eel gills with special reference to seawater adaptation. Comparative Biochemistry and Physiology, 38: 443-448.
VERDEGEM, M.C.J.; HILBRANDS, A.D.; BOON, J.H. 1997 Influence of salinity and dietary composition on blood parameter values of hybrid red tilapia, Oreochromis niloticus (Linnaeus) x O. mossambicus (Peters). Aquaculture Research, 28: 453-459.
WATANABE, W.O.; KUO, C.; HUANG, M. 1985 Salinity tolerance of Nile tilapia fry (Oreochromis niloticus), spawned and hatched at various salinities. Aquaculture, 48: 159-176.
YADA, T.; NAKANISHI, T. 2002 Interaction between endocrime and immune system in fish. International Journal of Review in Cytology, 220: 35-92.
ZOWAIL, M.E.M.; El í DEEB, S.I.; El í SERAFY, S.S.; RIZKALLA, E.H.; El-SAIED, H. 1994 Biochemical genetic studies of serum properties of family Mugillidae in two different habitats of Egyptian water. Bulletin National Institute Oceanography Fish Egypt, 20: 175-190.
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