Nutrient deposition in bullfrogs during the fattening phase
Keywords:
Lithobates catesbeianus, fat deposition, Logistic, protein depositionAbstract
Descriptions of nutrient deposition are important to determine the nutritional requirements of animals. The objective of this study was to describe nutrient deposition in the body and legs and the dietary intake of protein and fat of bullfrogs during the fattening phase using Gompertz and Logistic models, and to evaluate feed efficiency. A total of 2,375 froglets with an initial weight of 7.03 ± 0.16 g were housed in five fattening pens. The animals were fed a commercial diet containing 40% crude protein. Frogs and their legs were weighed and sampled at intervals of 14 days for the determination of nutrient composition. On the basis of the model selection criteria, the Logistic model was the most adequate to describe nutrient deposition in the body and legs of bullfrogs and the dietary intake of protein and fat. With respect to nutrient deposition in the body, the estimated values for nutrient weight at maturity (Wm) and the time when the maximum rate of deposition was attained (t*) were 244.3 g and 106 days, 55.2 g and 113 days, 30.9 g and 124 days, and 8.6 g and 99 days for water, protein, fat and ashes, respectively. For nutrient deposition in the legs, these values were 77.6 g and 111 days, 14.5 g and 104 days, 1.4 g and 86 days, and 3.7 g and 119 days, respectively. The protein efficiency of the bullfrog diet was low (36.76%), whereas the efficiency of fat utilization was high (140.9%), indicating the need to develop an ideal diet for bullfrogs.
References
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AMRKOLAIE, A.K. 2011 Reduction in the environmental impact of waste discharged by
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23(2): 349-358.
DUMAS, A.; FRANCE, J.; BUREAU, D. 2010 Modelling growth and body composition in fish
nutrition: Where have we been and where are we going? Aquaculture Research, 41(2): 161-181.
ETHERIDGE, R.D.; PESTI, G.M.; FOSTER, E.H. 1998 A comparison of nitrogen values obtained
utilizing the Kjeldahl nitrogen and Dumas combustion methodologies (Leco CNS 2000) on
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LUGO, M.G.; ALVAREZ, I.G.; NOVOA, M.A.O.;CÓRDOVA, G.M. 2003 Comparison of growth,
fillet yield and proximate composition between Stirling Nile tilapia (wild type) (Oreochromis
niloticus, Linnaeus) and red hybrid tilapia (Florida red tilapia x Stirling red O. niloticus)
males. Aquaculture Research, 34(2): 1023-1028.
MANSANO, C.F.M. 2015 Digestibilidade e exigência de aminoácidos para rã-touro. Jaboticabal. 115f. (Tese de Doutorado. Centro de Aquicultura (CAUNESP), Universidade Estadual Paulista -
UNESP).
MANSANO, C.F.M.; DE STÉFANI, M.V.; PEREIRA,M.M.; MACENTE, B.I. 2013 Deposição de nutrientes na carcaça de girinos de rãâ€"˜touro. Pesquisa Agropecuária Brasileira, 48(8): 885-891.
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MELLO, S.C.R.P.; SILVA, L.E.; MANO, S.; FRANCO,R.M. 2006 Avaliação bacteriológica e físicoquímica das carnes do dorso e coxa de rã (Rana catesbeiana) processadas em matadouro comercial. Revista Brasileira de Ciências Veterinárias, 13(1): 151-154.
MURUYAMA, K.; VINYARD, B.; AKBAR, M.K.; SHAFER, D.J.; TURK, C.M. 2001 Growth curve analyses in selected duck lines. British Poultry Science, 42(1): 574-582.
NEME, R.; SAKOMURA, N.K.; FUKAYAMA, E.H.; FREITAS, E.R.; FIALHO, F.B.; RESENDE, K.T.; FERNANDES, J.B.K. 2006 Curvas de crescimento e de deposição dos componentes corporais em aves de postura de diferentes linhagens. Revista Brasileira de Zootecnia, 35(6):1091-1100.
NEVEU, A. 2009 Suitability of European Green frogs for intensive culture: comparison between different phenotypes of the esculenta hybridogenetic complex. Aquaculture, 295(5): 30-37.
NÓBREGA, I.C.C.; ATAÍDE, C.S.; MOURA, O.M.;LIVERA, A.V.; MENEZES, P.H. 2007 Volatile
constituents of cooked bullfrog (Rana catesbeiana)legs. Food Chemistry, 102(3): 186-191
OLVERA-NOVOA, M.A.; ONTIVEROS-ESCUTIA,
V.M.; FLORES-NAVA, A. 2007 Optimum
protein level for growth in juvenile bullfrog
(Rana catesbeiana, Shaw, 1802). Aquaculture,
266(10): 191-199.
PEREIRA, M.M.; RIBEIRO FILHO, O.P.; TRONI,A.R.; TAKAMURA, A.E.; MANSANO, C.F.M.;NASCIMENTO, F.B.; CAMARGO FILHO, C.B.2011 Tecido hepático e corpo adiposo de rãtouro (Lithobates catesbeianus) submetido a diferentes fotoperíodos. Acta Veterinaria Brasilica,
5(1): 76-80.
PETERSEN, A.M. and GLEESON, T.T. 2011 Acclimation temperature affects the metabolic response of amphibians skeletal muscle to insulin. Comparative Biochemistry and Phisiology, 160(3): 72-80.
REED, L.J. and PEARL, R. 1927 On the summation of logistic curves. Journal of the Royal Statistical
Society, 90(1): 729-746.
RODRIGUES, M.L.; LIMA, S.L.; MOURA, O.M.; AGOSTINHO. C.A.; SILVA. J.H.V.; CRUZ, G.R.B.;
CAMPOS, V.M.; CASALI, A.P.; MENDES, R.R.B.; ALBUQUERQUE, A.G. 2007 Curva de crescimento
em rã-touro na fase de recria. Archivos de Zootecnia, 56(1): 125-136.
SARMENTO, J.LR.; REGAZZI, A.J.; SOUZA, W.H.;TORRES, R.A.; BREDA, F.C.; MENEZES, G.R.O.
2006 Analysis of the growth curve of Santa Ines sheep. Revista Brasileira de Zootecnia, 35(3): 435-442.
SAS Institute. 2008 SAS/STAT 9.2. User’s guide. SASInstitute Inc, Cary, NC. p.4264-4286.
SEIXAS FILHO, J.T.; HIPOLITO, M.; MARTINS,A.M.C.R.P.F.; RODRIGUES, E.; CASTAGNA, A.A.; MELLO, S.C.R.P. 2009 Histopathological alterations in bullfrog juveniles fed commercial rations of different crude protein levels. Revista Brasileira de Zootecnia, 39(6): 2306-2310.
SILVA, D.J. and QUEIROZ, A.C. 2006 Análise de alimentos métodos químicos e biológicos. 3rd ed.
Viçosa, MG: Editora UFV. 235p.
TOKUR, B.; GíÅ“RBíÅ“Z, D.; í–ZYURT, G. 2008 Nutricional composition of frog (Rana esculanta) waste meal. Bioresource Technology, 99(6): 1332-1338.
TRUNG, D.V.; DIU, N.T.; HAO, N.T.; GLENCROSS B. 2011 Development of a nutritional model to
define the energy and protein requirements of tilapia, Oreochromis niloticus. Aquaculture,
320(1): 69-75.
TURNIPSEED, S.B.; CLARK, S.B.; STOREY, J.M.; CARR, J.R. 2012 Analysis of veterinary drug
residues in frog legs and other aquacultured species using liquid chromatography quadrupole time-of-flight mass spectrometry. Journal of Agricultural and Food Chemistry, 60(2):4430-4439.
WINSOR, C.P. 1932 The Gompertz curve as a growth curve. Proceedings of the National Academy of Sciences of the United States of America, 18(1): 1-8.
Control, 19(1): 716-723.
AMRKOLAIE, A.K. 2011 Reduction in the environmental impact of waste discharged by
fish farms through feed and feeding. Reviews in Aquaculture, 3(1): 19-26.
AMRKOLAIE, A.K.; YANSARI, A.T.; KHALESI, M.K. 2012 Calculation of protein and energy requirements in beluga sturgeon (Huso huso) using a factorial approach. Journal Animal Physiology and Animal Nutrition, 96(1): 1-10.
ASSIS, M.F.; FRANCO, M.L.R.S.; STÉFANI, M.V.;FRANCO, N.P.; GODOY, L.C.; OLIVEIRA, A.C.;
VISENTAINER, J.V.; SILVA, A.F.; HOCH, A.L.V. 2009 Efeito do alecrim na defumação da carne de rã (Rana catesbeiana): características sensoriais, composição e rendimento. Ciência e Tecnologia dos Alimentos, 29(3): 553-556.
BORGES, F.F.; AMARAL, L.A.; STEFANI, M.V. 2012 Characterization of effluents from bullfrog
(Lithobates catesbeianus, Shaw, 1802) grow-out ponds. Acta Limnologica Brasiliensia, 24(1): 160-166.
CASALI, A.P.; MOURA, O.M.; LIMA, S.L.; SILVA,J.H.V. 2005 Avaliação de rações comerciais nas
fases de crescimento e terminação da recria de rã-touro. Boletim do Instituto de Pesca, 31(1): 37-46.
CASAS, G.A.; RODRÍGUEZ, D.; AFANADOR, G.2010 Propiedades matemáticas del modelo de Gompertz y su aplicación al crecimiento de los cerdos. Revista Colombiana de Ciencias Pecuarias,
23(2): 349-358.
DUMAS, A.; FRANCE, J.; BUREAU, D. 2010 Modelling growth and body composition in fish
nutrition: Where have we been and where are we going? Aquaculture Research, 41(2): 161-181.
ETHERIDGE, R.D.; PESTI, G.M.; FOSTER, E.H. 1998 A comparison of nitrogen values obtained
utilizing the Kjeldahl nitrogen and Dumas combustion methodologies (Leco CNS 2000) on
samples typical of an animal nutrition analytical laboratory. Animal Feed Science and Technology,
73(1): 21-28.
FARIAS, L.N.; VASCONCELOS, V.R.; CARVALHO,V.R.; SARMENTO, J.L.R. 2011 Avaliação dos modelos logístico bicompartimental e de Gompertz na estimativa da diní¢mica de fermentação ruminal in vitro do farelo e da torta de babaçu (Orbignya martiana). Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 63(1): 136-142.
FELISBINO, S.L. and CARVALHO, H.F. 2001 Growth cartilage calcification and formation of
bone trabeculae are late and dissociated events in the endochondral ossification of Rana
catesbeiana. Cell Tissue Research, 306(2): 319-323.
FENERICK JR, J. and STÉFANI, M.V. 2005 Desempenho e parí¢metros metabólicos de rãtouro, Rana catesbeiana, alimentada com diferentes rações comerciais. Acta Scientiarium.Animal Science, 27(2): 377-383.
FREITAS, A.R. 2005. Curvas de Crescimento na Produção Animal. Revista Brasileira de Zootecnia,
34(4): 786-795.
GONí"¡ALVES, L.U.; FERROLI, F.; VIEGAS, E.M.M. 2012 Effect of the inclusion of fish residue oils in
diets on the fatty acid profile of muscles of males and females lambari (Astyanax altiparanae).
Revista Brasileira de Zootecnia, 41(8): 1967-1974.
HAFS, A.W.; MAZIK, P.M.; KENNEY, P.B.;SILVERSTEIN, J.T. 2012 Impact of carbon dioxide level, water velocity, strain, and feeding regimen on growth and fillet attributes of cultured rainbow trout (Oncorhynchus mykiss). Aquaculture, 350(1): 46-53.
HARTLEY, H.O. 1961 The modified Gauss Newton method for the fitting of non linear regression
functions by least squares. Technometrics, 3(2):269-280.
HUA, K.; BIRKETT, S.; DE LANGE, C.F.M.;BUREAU, D.P. 2010 Adaptation of a nonruminant nutrient-based growth model to rainbow trout (Oncorhynchus mykiss Walbaum).Journal of Agricultural Science, 148(1): 19-27.
LIEBERT, F.; SíÅ“NDER, A.; MOHAMED, K. 2006 Assessment of nitrogen maintenance requirement and potential for protein deposition in juvenile Tilapia genotypes by application of an exponential nitrogen utilization model.Aquaculture, 78(4): 812-821.
LIMA, S.L. 1997 Criação de rãs (Sistema Anfrigranja).Viçosa: CPT, Manual técnico (08). 48p.
LUGO, M.G.; ALVAREZ, I.G.; NOVOA, M.A.O.;CÓRDOVA, G.M. 2003 Comparison of growth,
fillet yield and proximate composition between Stirling Nile tilapia (wild type) (Oreochromis
niloticus, Linnaeus) and red hybrid tilapia (Florida red tilapia x Stirling red O. niloticus)
males. Aquaculture Research, 34(2): 1023-1028.
MANSANO, C.F.M. 2015 Digestibilidade e exigência de aminoácidos para rã-touro. Jaboticabal. 115f. (Tese de Doutorado. Centro de Aquicultura (CAUNESP), Universidade Estadual Paulista -
UNESP).
MANSANO, C.F.M.; DE STÉFANI, M.V.; PEREIRA,M.M.; MACENTE, B.I. 2013 Deposição de nutrientes na carcaça de girinos de rãâ€"˜touro. Pesquisa Agropecuária Brasileira, 48(8): 885-891.
MARCATO, S.M.; SAKOMURA, N.K.; MUNARI,D.P.; FERNANDES, J.B.K.; KAWAUCHI, I.M.; BONATO, M.A. 2008 Growth and body nutrient deposition of two broiler commercial genetic lines. Brazilian Journal of Poultry Science, 10(3): 117-123.
MELLO, S.C.R.P.; SILVA, L.E.; MANO, S.; FRANCO,R.M. 2006 Avaliação bacteriológica e físicoquímica das carnes do dorso e coxa de rã (Rana catesbeiana) processadas em matadouro comercial. Revista Brasileira de Ciências Veterinárias, 13(1): 151-154.
MURUYAMA, K.; VINYARD, B.; AKBAR, M.K.; SHAFER, D.J.; TURK, C.M. 2001 Growth curve analyses in selected duck lines. British Poultry Science, 42(1): 574-582.
NEME, R.; SAKOMURA, N.K.; FUKAYAMA, E.H.; FREITAS, E.R.; FIALHO, F.B.; RESENDE, K.T.; FERNANDES, J.B.K. 2006 Curvas de crescimento e de deposição dos componentes corporais em aves de postura de diferentes linhagens. Revista Brasileira de Zootecnia, 35(6):1091-1100.
NEVEU, A. 2009 Suitability of European Green frogs for intensive culture: comparison between different phenotypes of the esculenta hybridogenetic complex. Aquaculture, 295(5): 30-37.
NÓBREGA, I.C.C.; ATAÍDE, C.S.; MOURA, O.M.;LIVERA, A.V.; MENEZES, P.H. 2007 Volatile
constituents of cooked bullfrog (Rana catesbeiana)legs. Food Chemistry, 102(3): 186-191
OLVERA-NOVOA, M.A.; ONTIVEROS-ESCUTIA,
V.M.; FLORES-NAVA, A. 2007 Optimum
protein level for growth in juvenile bullfrog
(Rana catesbeiana, Shaw, 1802). Aquaculture,
266(10): 191-199.
PEREIRA, M.M.; RIBEIRO FILHO, O.P.; TRONI,A.R.; TAKAMURA, A.E.; MANSANO, C.F.M.;NASCIMENTO, F.B.; CAMARGO FILHO, C.B.2011 Tecido hepático e corpo adiposo de rãtouro (Lithobates catesbeianus) submetido a diferentes fotoperíodos. Acta Veterinaria Brasilica,
5(1): 76-80.
PETERSEN, A.M. and GLEESON, T.T. 2011 Acclimation temperature affects the metabolic response of amphibians skeletal muscle to insulin. Comparative Biochemistry and Phisiology, 160(3): 72-80.
REED, L.J. and PEARL, R. 1927 On the summation of logistic curves. Journal of the Royal Statistical
Society, 90(1): 729-746.
RODRIGUES, M.L.; LIMA, S.L.; MOURA, O.M.; AGOSTINHO. C.A.; SILVA. J.H.V.; CRUZ, G.R.B.;
CAMPOS, V.M.; CASALI, A.P.; MENDES, R.R.B.; ALBUQUERQUE, A.G. 2007 Curva de crescimento
em rã-touro na fase de recria. Archivos de Zootecnia, 56(1): 125-136.
SARMENTO, J.LR.; REGAZZI, A.J.; SOUZA, W.H.;TORRES, R.A.; BREDA, F.C.; MENEZES, G.R.O.
2006 Analysis of the growth curve of Santa Ines sheep. Revista Brasileira de Zootecnia, 35(3): 435-442.
SAS Institute. 2008 SAS/STAT 9.2. User’s guide. SASInstitute Inc, Cary, NC. p.4264-4286.
SEIXAS FILHO, J.T.; HIPOLITO, M.; MARTINS,A.M.C.R.P.F.; RODRIGUES, E.; CASTAGNA, A.A.; MELLO, S.C.R.P. 2009 Histopathological alterations in bullfrog juveniles fed commercial rations of different crude protein levels. Revista Brasileira de Zootecnia, 39(6): 2306-2310.
SILVA, D.J. and QUEIROZ, A.C. 2006 Análise de alimentos métodos químicos e biológicos. 3rd ed.
Viçosa, MG: Editora UFV. 235p.
TOKUR, B.; GíÅ“RBíÅ“Z, D.; í–ZYURT, G. 2008 Nutricional composition of frog (Rana esculanta) waste meal. Bioresource Technology, 99(6): 1332-1338.
TRUNG, D.V.; DIU, N.T.; HAO, N.T.; GLENCROSS B. 2011 Development of a nutritional model to
define the energy and protein requirements of tilapia, Oreochromis niloticus. Aquaculture,
320(1): 69-75.
TURNIPSEED, S.B.; CLARK, S.B.; STOREY, J.M.; CARR, J.R. 2012 Analysis of veterinary drug
residues in frog legs and other aquacultured species using liquid chromatography quadrupole time-of-flight mass spectrometry. Journal of Agricultural and Food Chemistry, 60(2):4430-4439.
WINSOR, C.P. 1932 The Gompertz curve as a growth curve. Proceedings of the National Academy of Sciences of the United States of America, 18(1): 1-8.
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