Incorporation of probiotics in the diet for juvenile nile tilapias: hematological, immunological and microbiological parameters

Authors

  • Ivan Bernardoni NAKANDAKARE Pós-graduação do Instituto de Pesca, APTA/SAA/SP
  • Marina Keiko Pieroni IWASHITA Pós-graduação do Centro de Aquicultura da UNESP - CAUNESP
  • Danielle de Carla DIAS Pós-doutoranda do Instituto de Pesca, APTA/SAA/SP http://orcid.org/0000-0002-8375-5948
  • Leonardo TACHIBANA Pesquisadores Cientí­­ficos do Instituto de Pesca, APTA/SAA/SP
  • Maria José Tavares RANZANI-PAIVA Pesquisadores Cientí­­ficos do Instituto de Pesca, APTA/SAA/SP
  • Elizabeth ROMAGOSA Pesquisadores Cientí­­ficos do Instituto de Pesca, APTA/SAA/SP http://orcid.org/0000-0001-5363-4128

Keywords:

Bacillus subtilis, Bacillus toyoi, cichlid, macrophage migration

Abstract

Probiotics are generally considered as live micro-organisms which, when administered in adequate amounts, confer a health benefit to the host. The processing method of diet and the form of inclusion of probiotic can interfere in hematological, immunological and microbiological parameters in fish. The aim was to estimate the hematological, immunological and microbiological parameters in juveniles of Nile tilapia fed probiotic included before and after the process of pelletization and extrusion. The experimental design was completely randomized, with five treatments: pelleted diet without probiotic, pelleted diet with inclusion of probiotic before and after processing, extruded feed without probiotic and extruded feed with inclusion of probiotic after processing, and five replications. Two hundred and fifty fish were distributed in 25 aquaria (20 L) and fed for 63 days. The blood composition (red and white) showed no significant differences, except mean corpuscular hemoglobin concentration of control when compared to that of other treatments. The phagocytic capacity of the animals that had received the extruded diet supplemented with probiotic was significantly higher when compared to that of the other treatments. However, there were no differences between the treatments regarding to the phagocytic index. Fish fed the extruded diet exhibited significant improvement in the nonspecific immunity. The probiotic bacteria colonized the intestine, since it was possible to recover them. It can be stated that these fishes remained healthy, because the hematological parameters were not altered during the experimental period. The study shows that any form of inclusion in the feed tested (before or after and after pelletizing extrusion) may be easily used by the fish farmer.

References

ADEPARUSI, E.O. e ATAYI, A.D. 2000 Hematological characteristics of Nile tilapia
Oreochromis niloticus fed differently processed Lima beam (Phaseolus lunatus L.) diets. In: INTERNATIONAL SYMPOSIUM ON TILAPIA AQUACULTURE, 5., Rio de Janeiro, 3-7/set./2000. Anais… Rio de Janeiro: ISTA. p.131-137.

AL-DOHAIL, M.A.; HASHIM, R.; ALUYU-PAIKO, M. 2011 Evaluation the use Lactobacillus acidophilus as a biocontrol agent against common pathogenic bactéria and the effects on the haematology parameters and histopathology in African catfish, Clarias gariepinus, juveniles.Aquaculture Research, 42: 196-209.

ALKAHEM, H.F. 1994 The toxicity of nickel and the effects of sublethal levels on hematological parameters and behaviour of the fish,Oreochromis niloticus. Journal University Kuwait Science, 21: 243-252.

AOAC - ASSOCIATION OF OFFICIAL ANALYTICAL CHEMISTS 1990 Official methods
of analysis. 15th ed. Arlington: AOAC. 1298p.

BALCÁZAR, J.L.; DE BLAS, I.; RUIZ-ZARZUELA, I.;CUNNINGHAM, D.; VENDRELL, D.;
Mí­Å¡ZQUIZ, J.L. 2006 The role of probiotics in aquaculture. Veterinary Microbiology, 114: 173-186.

BARROS, M.M.; RANZANI-PAIVA, M.J.T.; PEZZATO, L.E.; FALCON, D.R.; GUIMARíES,
I.G. 2009 Hematological response and growth performance of Nile Tilapia fed diets containing folic acid. Aquaculture Research, 40: 895-903.

BITTENCOURT, N.L.R.; MOLINARI, L.M.; SCOARIS, D.O.; PEDROSO, R.B.; NAKAMURA,
C.V.; NAKAMURA, T.U.; ABREU FILHO, B.A.; DIAS FILHO, B.P. 2003 Haematological and biochemical values for Nile tilapia Oreochromis niloticus cultured in semi-intensive system. Acta Scientiarum, 25: 385-389.

BUCIO, A.; HARTEMINK, R.; SCHRAMA, J.W.; VERRETH, J.; ROMBOUTS, F.M. 2005
Survival of Lactobacillus plantarum 44a after spraying and drying in feed and during
exposure to gastrointestinal tract fluids in vitro.The Journal of General and Applied Microbiology, 51(4): 221í 227.

BURR, G.; GATLIN, D.; RICKE, S. 2005 Microbial ecology of the gastrointestinal tract of fish and the potential application of prebiotics and probiotics in finfish aquaculture. Journal of World Aquaculture Society, 36: 425-436.

CASILLAS, E. and SMITH, L.S. 1977 Effect of stress on blood coagulation and haematology in rainbow trout (Salmo gairdneri). Journal of Fish Biology, 10: 481-491.

CHANG, C.-I., and LIU, W.-Y. 2002 An Evaluation of two probiotic bacterial strains, Enterococcus faecium SF68 and Bacillus toyoi, for Reducing Edwardsiellosis in Cultured European Eel, Anguilla anguilla L. Journal of Fish Diseases, 25(5):311í 315.

CHEN, C.Y.; WOOSTER, G.A.; BOWSER, P.R. 2004 Comparative blood chemistry and
histopathology of tilapia infected with Vibrio vulnificus or Streptococcus iniae or exposed to carbon tetrachloride, gentamicin, or copper sulphate. Aquaculture, 239: 421-443.

CROSS, M.L. 2002 Microbes versus microbes: immune signals generated by probiotic
lactobacilli and their role in protection against microbial pathogens. FEMS Immunology and Medical Microbiology, 34: 245-253.

DA SILVA, B.C.; MOURIí­"˜O, J.L.P.; VIEIRA, F.N.;JATOBÁ, A.; SEIFFERT, W.Q.; MARTINS, M.L. 2012 Haemorrhagic septicaemia in the hybrid surubim (Pseudoplatystoma corruscans and Pseudoplatystoma fasciatum) caused by Aeromonas hydrophila. Aquaculture Research, 43(6): 908í 916.

DIAS, D.C. 2010 Probióticos no desempenho produtivo, hematologia e migração de macrófagos do matrinxã, Bricon amazonicus. Jaboticabal. 112p. (Tese de Doutorado em Aquicultura. Universidade Estadual Paulista Júlio de Mesquita Filho).Disponí­­vel em: http://www.caunesp.unesp.br/Publicacoes/Dissertacoes_Teses/Dissertacoes.
pdf Acesso em: 20 abr. 2010.

DIAS, D.C.; STÉFANI, M.V.; FERREIRA, C.M.;FRANí­"¡A, F.M. 2008 Uso de probiótico em ração de rã-touro, Rana catesbeiana: desempenho produtivo. Archivos de Zootecnia, 57: 449-455.

DIAS, D.C.; LEONARDO, A.F.G.; TACHIBANA, L., CORREA, C.F.; BORDON, I.C.A.C.;
ROMAGOSA, E.; RANZANI-PAIVA, M.J.T. 2012 Effect of incorporating probiotics into the diet of matrinxã (Brycon amazonicus) breeders. Journal of Applied Ichthyology, 28(1): 40-45. Disponí­­vel em: http://onlinelibrary.wiley.com/doi/10.1111/j.1439-0426.2011.01892.x/full.Acesso em 15 fev. 2013.

DOGGETT, T.A. e HARRIS, J.E. 1989 Ultrastructure of the peripheral blood leucocytes of Oreochromis mossambicus. Journal of Fish Biology, 33: 747-756.

ELLIS, A.E. 1977 The leucocytes of fish: A review.Journal of Fish Biology, 11: 453-491.

EZZAT, A.A.; SHABANA, M.B.; FARGHALY, A.M. 1974 Studies on the blood characteristics of Tilapia zillii (Gervais). I. Blood cells. Journal of Fish Biology, 6: 1-12.

FAO/WHO 2001 Report on Joint FAO/WHO Expert consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. 1-4/out./2001, Córdoba, Argentina.Disponí­­vel em: ftp://ftp.fao.org/es/esn/food/probio_report_en.pdf Acesso em:23 ago. 2009.

FULLER, R. 1989 Probiotics in man and animals: A review. Journal of Applied Bacteriology, 66: 365-378.

FURUYA, W.M.; PEZZATO, L.E.; BARROS, M.M.;CYRINO, J.E.P. 2012 Exigências nutricionais e alimentação em tilápia. In: FRACALOSSI, D.M. e CYRINO, J.E.P. Nutrição e alimentação de espécies de interesse para a aqüicultura brasileira NUTRIAQUA. Florianópolis: Sociedade Brasileira de Aquicultura e Biologia aquática, 2012.Gráfica e Editora Copiart Ltda. p. 255-268.

GATESOUPE, F.J. 2008 Updating the importance of lactic acid bacteria in fish farming: natural occurrence and probiotic treatments. Journal Molecular Microbiology Biotechnology, 14: 107-114.

GHIRALDELLI, L.; MARTINS, M.L.; YAMASHITA,M.M.; JERÔNIMO, G.T. 2006 Ectoparasites influence on the haematological parameters of Nile tilapia and carp cultured in the State of Santa Catarina, South Brazil. Journal of Fish and Aquatic Science, 1: 270-276.

GILL, H.S.; RUTHERFURD, K J.; PRASAD, J.; GOPAL, P.K. 2000 Enhancement of natural and acquired immunity by Lactobacillus rhamnosus (HN001), Lactobacillus acidophilus (HN017) and Bifidobacterium lactis (HN019). British Journal of Nutrition, 83: 167-176.

GULLIAN, M.; THOMPSON F.; RODRIGUEZ J. 2004 Selection of probiotic bacteria and study of their immunoestimulatory effect in Penaeus vannamei. Aquaculture, 233: 1-14.

HARIKRISHNAN. R.; BALASUNDARAM, C.; HEO,M.S. 2010 Supplementation diet containing probiotics, herbal and azadirachtin on hematological and biochemical changes in Cirrhina mrigala against Aphanomyces invadans. Fisheries and Aquaculture Journal, Volume 2010:FAJ-4: 1-11.

HILL, D.J. e ROWLEY, A.F. 1996 The thromboxane mimetic, U-46619, induces the aggregation of fish thrombocytes. Britany Journal of Haematology,92: 200-211.

HISANO, H.; PEZZATO, L.E.; BARROS, M.M.; KLEEMANN, G.K.; FREIRE, E.S.; GONí­"¡ALVES, G.S.; ZUANON, J.A.S.; SÁ, M.V.C. 2003 Yeast and zinc on hematological parameters of nile tilapia fingerlings, Oreochromis niloticus. In:WORLD AQUACULTURE 2003, Salvador, BA,19-23/mai./2003. Anais... Salvador: WAS. p.575.

HRUBEC, T.C. e SMITH, S.A. 1998 Hematology of fish. In: FELDMAN, B.F.; ZINKL, J.G.; JAIN, N.C. (Ed.). Schalm’s veterinary hematology. 5th ed.Sydney: W. W. Lippincott. p.1120-1125.

HRUBEC, T.C.; CARDINALE, J.L.; SMITH, S.A. 2000 Hematology and chemistry reference intervals for cultured tilapia (Oreochromis hybrid).Veterinary Clinical Pathology, 29: 7-12.

IMAGAWA, T.; HASHIMOTO, Y.; KITAGAWA, H.; KON, Y.; KUDO, N.; SUGIMURA, M. 1989 Morphology of blood cells in carp (Cyprinus carpio L.). Japan Jourmal of Veterinary Science, 51: 1163-1172.

IRIANTO, A. e AUSTIN, B. 2002 Use of probiotics to control furunculosis in rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases, 25: 333í 342.

ISHIKAWA, C.M. 1998 Quantificação bacteriana e avaliação das lesões em peixes da espécie Oreochromis niloticus (tilápia do Nilo) inoculadas experimentalmente com Mycobacterium marinum ATCC 927. São Paulo. 58p. (Dissertação de Mestrado. Universidade de São Paulo í  USP).Disponí­­vel em. http://www.fmvz.usp.br Acesso em: 18 jun. 2010.

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: 619-626

JATOBÁ, A.; VIEIRA, F.N.; BUGLIONE, C.; SILVA, B.C.; MOURIí­"˜O, J.L.P.; JERÔNIMO, G.T.;
DOTTA, G.; MARTINS, M.L. 2008 Utilização de bactérias ácido-lácticas isoladas do trato intestinal de tilápia-do-nilo como probiótico.Pesquisa Agropecuária Brasileira, 43: 1201-1207.

JATOBÁ, A.; VIEIRA, F. N.; BUGLIONE, C.; SILVA,B.C.; MOURIí­"˜O, J.L.P.; SILVA, B.C.; SEIFTTER, W.Q.; ANDREATTA, E.R. 2011 Diet supplemented with probiotic for Nile tilapia in polyculture system with marine shrimp. Fish Physiology and Biochemistry, 37: 725-732.

KESARCODI-WATSON, A.; KASPAR, H.; LATEGAN, M.J.; GIBSON, L. 2008 Probiotics in
aquaculture: the need, principles and mechanisms of action and screening processes.Aquaculture, 274: 1-14.

KUBITZA, F. 1999 Nutrição e alimentação dos peixes cultivados. 3ªed. Jundiaí­­: Kubitza, F. 123p.

LARA-FLORES, M.L.; BRIONES, L.E.; NOVOA,M.A.O. 2002 Avances en utilización de
probiotico como promotores de crecimiento em tilapia nilótica (Oreochromis niloticus). In: CRUZSUÁREZ, L.E.; RICQUE-MARIE, D.; TAPIASALAZAR, M.; GAXIOLA-CORTÉS, M.G.;SIMOES, N. (Eds) Avances en nutrición acuí­­cola.Memórias del Simposium International de Nutrición Acuí­­cola, 6, 2002, Cancún. Anais...Cancún: CICESE, 2002. p.314-335.

MARTINS, M.L.; PILARSKY, F.; ONAKA, E.M.;NOMURA, D.T.; FENERICK, J.; RIBEIRO, K.;
MIYAZAKI, 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 do Instituto de Pesca, 30: 71-80.

MATUSHIMA, E.R. e MARIANO, M. 1996 Kinetics of the inflammatory reaction induced by carrageenin in the swinbladder of Oreochromis niloticus (Nile tilapia). Brazilian Journal of Veterinary Animal Science, 33(1): 5-10.

MERRIFIELD, D.L.; DIMITROGLOU, A.; FOEY, A.; DAVIES, S.J.; BAKER, R.T.M.; BOGWALD, J.; CASTEX, M.; RINGO, E. 2010 The current status and future focus of probiotic and prebiotic applications for salmonids. Aquaculture, 302: 1-18.

MEURER, F.; HAYASHI, C.; COSTA, M.M.; MAUERWERK, V.L.; MASCIOLI, A.S.;COLPINI, L.M.S.; FRECCIA, A. 2008 Levedura como probiótico na reversão sexual da tilápiado-Nilo. Revista Brasileira de Saúde e Produção Animal, 9: 804-812.

MOURIí­"˜O, J.L.P.; NASCIMENTO VIEIRA, F.; JATOBÁ, A.B.; DA SILVA, B.C.; JESUS, G.F.A.;
SEIFFERT, W.Q.; MARTINS, M.L. 2012 Effect of dietary supplementation of inulin and W. cibaria on haemato-immunological parametres of hybrid surubim (Pseudoplatystoma sp).Aquaculture Nutrition, 18: 73-80.

MOYLE, P.B. e CECH JR, J.J. 1982 Fishes: An Introduction to Ichthyology. Prentice-Hall, Inc.,New Jersey. 309p.

NAGESWARA, P.V. e BABU, D.E. 2006 Probiotics as an alternative therapy to minimize or avoid antibiotics use in aquaculture. Fishing Chimes,26(1): 112-114.

NAYAK, S.K. 2010 Probiotics and immunity: A fish perspective. Fish and Shellfish Immunology, 29: 2-14.

NRC - NATIONAL RESEARCH COUNCIL 1993 Nutrient Requirements of Warm water, Fishes and Shellfishes: Nutrient Requirements of Domestic Animals. Washington. 125p.

PASTORE, S.C.G.; GAIOTTO, J.R.; RIBEIRO, F.A.S.; NUNES, A.J.P. 2012 Formulação de rações e boas práticas de fabricação. In: FRACALOSSI, D.M. e CYRINO, J.E.P. Nutrição e alimentação de espécies de interesse para a aqüicultura brasileira. NUTRIAQUA. Florianópolis: Sociedade Brasileira de Aqüicultura e Biologia aquática,2012. Gráfica e Editora Copiart Ltda. p.293-346.

PIRARAT, N.; KOBAYASHI, T.; KATAGIRI, T.;MAITA, M.; ENDO, M. 2006 Protective effects and mechanisms of a probiotic bacterium Lactobacillus rhamnosus against experimental Edwardsiella tarda infection in tilapia (Oreochromis niloticus). Veterinary Immunology and Immunopathology, 113: 339-347.

PITOMBEIRA, M.S. e MARTINS, J.M. 1970 Haematology of the Spanish mackerel,
Scomberomorus maculatus. Copeia, 1: 182-186.

RANZANI-PAIVA, M.J.T. e GODINHO, H.M. 1983 Sobre células sangüí­­neas e contagem diferencial de leucócitos e eritroblastos em curimbatá, Prochilodus scrofa Steindacher, 1881 (Osteichthyes, Cypriniformes, Prochilodontidae). Revista Brasileira de Biologia, 43: 331-338.

RANZANI-PAIVA, M.J.T. e SILVA-SOUZA, A. 2004 Hematologia de peixes Brasileiros In:
RANZANI-PAIVA, M.J.T.; TAKEMOTO, R.M.; LIZAMA, M.A.P. Sanidade de Organismos
Aquáticos. Varela, São Paulo, p.89-120.

RANZANI-PAIVA, M.J.T.; FELIZARDO, N.N.;LUQUE, J.L. 2005 Parasitological and
hematological analysis in Nile tilapia Oreochromis niloticus Linnaeus, 1757, from
Guarapiranga Reservoir São Paulo State, Brazil.Acta Scientiarum, 27: 231-237.

RENGPIPAT, S.; RUKPRATANPON, S.; PIYATIRATITIVORAKUL, S.; MENASAVETA,
P. 2000 Inmunity enhancement in black tiger shirimp (Penaeus monodon) by a probiotic bacterium (Bacillus S11). Aquaculture, 191: 271-288.

RINGO, E. e GATESOUPE, F., 1998 Lactic acid bacteria in fish: a review. Aquaculture, 160:177í 203.

RINGO, E.; OLSEN, R.E.; MAYHEWC, T.M.; MYKLEBUSTD, R. 2003 Electron microscopy of the intestinal microflora of fish. Aquaculture, 227: 1-4.

ROBERTS, R.J. 1981 Patologia de los peces. Madrid: Mundií Prensa. 366p.

ROSENFELD, G. 1947 Corante pancrônico para hematologia e citologia clí­­nica. Nova
constituição dos componentes do May Grünwald e do Giemsa num só corante de
emprego rápido. Memórias do Instituto Butantã,20: 329-334.

SAHU, M.K.; SWARNAKUMAR, N.S.;SIVAKUMAR, K.; THANGARADJOU, T.; KANNAN, L. 2008 Probiotics in aquaculture:importance and future perspectives. Indian Journal of Microbiology, 48: 299-308.

SELVIN, J.; HUXLEY, A.J.; LIPTON, P. 2004 Immunomodulatory potential of marine
secondary metabolites against bacterial diseases of shrimp. Aquaculture, 230: 242-248.

SETLOW, P., 2006. Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals. Journal of Applied Microbiology, 101:514-525.

SILVA, J.R.M.C.; STAINES, N.A.; HERNANDEZBLAZQUEZ, F.J.; PORTO-NETO, L.R.; BORGES, J.C.S. 2002 Phagocytosis and giant cell formation at 0ºC by macrophage of Notothenia coriiceps. Journal Fish Biology, 60: 466-478.

SILVA, J.R.M.C.; PORTO-NETO, L.R.; BORGES J.C.S.; JENSCH-JUNIOR, B.E. 2005 Germicide capacity of macrophages in the Antartic fish Notothenia coriiceps (Richardson, 1844) at 0ºC. Polar Biology, 28(4): 326-328.

TACHIBANA, L.; DIAS, D.C.; ISHIKAWA, C.M.; CORREA, C.F.; LEONARDO, A.F.G.;
RANZANI-PAIVA, M.J.T. 2011 Probiótico na alimentação da tilápia-do-nilo (Oreochromis niloticus Lineu, 1758): desempenho zootécnico e recuperação da bactéria probiótica intestinal. Bioikos, 25(1): 25-31.

TAPIA-PANIAGUA, S.T.; CHABRILLÓN, M.; DÍAZROSALES, P.; BANDA, I.G.; LOBO, C.;
BALEBONA, M.C.; MORIí­"˜IGO, M.A. 2010 Intestinal microbiota diversity of the flat fish
Solea senegalensis (Kaup, 1858) following probiotic administration. Microbial Ecology, 60(2):310í 319.

TAVARES-DIAS, M. 2003 Variáveis hematológicas de teleósteos brasileiros de importí­¢ncia zootécnica. Jaboticabal. 248p. (Tese de Doutorado em Aqüicultura. Universidade Estadual Paulista Júlio de Mesquita Filho). Disponí­­vel em:http://www.caunesp.unesp.br/Publicacoes/Dissertacoes_Teses/Dissertacoes.pdf Acesso em:13 abr. 2010.

TAVARES-DIAS, M. e FAUSTINO, C.D. 1998 Parí­¢metros hematológicos da tilápia-do-Nilo Oreochromis niloticus (Cichlidae) em cultivo extrensivo. Ars Veterinária, 14: 254-263.

TAVARES-DIAS, M. e MORAES, F.R. 2003 Caracterí­­sticas hematológicas da Tilapia rendalli Boulenger, 1896 (Osteichthyes: Cichlidae) capturadas em "pesque-pague” de Franca, São Paulo, Brasil. Bioscience Journal, 19: 107-114.

TAVARES-DIAS, M. e MORAES, F.R. 2004 Hematologia de Peixes Teleósteos. Ed. Eletrônica e Arte Final. Riberão Preto. SP. 144p.

TAVARES-DIAS, M.; FRASCÁ-SCORVO, C.M.D.;NOVATO, P.F.C.; MORAES, F.R. 2000
Hematological characteristics of hybrid Florida red tilapia, Oreochromis urolopis hornorum x O. mossambicus under intensive rearing. In: INTERNATIONAL SYMPOSIUM ON TILAPIA AQUACULTURE, 5., Rio de Janeiro, 3-7/set./2000.Anais… Rio de Janeiro: ISTA. p.533-541.

TAVARES-DIAS, M.; MORAES, F.R.; MARTINS, M.L.; SANTANA, A.E. 2002 Haematological changes in Oreochromis niloticus (Osteichthyes: Cichlidae) with gill ichthyophthiriasis and saprolegniosis. Boletim do Instituto de Pesca, 28: 1-9.

UEDA, I.K.; EGAMI, M.I.; SASSO, W.S.; MATUSHIMA, E.R. 1997 Estudos hematológicos em Oreochromis niloticus (Linnaeus, 1758) (Cichlidae, Teleostei) - Parte I. Brazilian Journal of Veterinary Research and Animal Science, 34: 270-275.

WELKER, T.L. e LIM, C. 2011 Use of probiotics in diets of tilapia. Journal of Aquaculture Research & Development (on-line), S1:014: 1-8. DOI:10.4172/2155-9546.S1-014

VEIGA, M.L.; EGAMI, M.I.; RANZANI-PAIVA,M.J.T.; RODRIGUES, E.L. 2000 ASPECTOS
morfológicos y citoquí­­micos de las células sanguí­­neas de Salminus maxillosus Valenciennes, 1840 (Characiformes, Characidae). Revista Chilena de Anatomia, 18: 245-250.

VERSCHUERE, L.; ROMBAUT, G.; SORGELOOS, P.;VERSTRAETE, W. 2000 Probiotic bacteria as biological control agents in aquaculture. Microbiology and Molecular Biology Reviews, 64:655-671.

VIEIRA, J.S.; LOGATO, P.V.R.; RIBEIRO, P.A.P.; FREITAS, R.; FIALHO, E.T. 2005 Efeito do
processamento do milho sobre o desempenho e composição de carcaça de piaba (Leporinus friderici) criada em tanques-rede. Ciência e Agrotecnologica, 29: 453-458.

ZAR, J.H. 2009 Biostatistical Analysis. 5th. Edition,Prentice-Hall, Inc., Upper Saddle River, New Jersey, USA. 576p

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2018-11-11

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