Indicators of stress in tilapia subjected to different stunning methods
Keywords:
adenosine triphosphate, animal welfare, cortisol, Oreochromis niloticus, oxidative stress, slaughterAbstract
Nile tilapia is one of the main fish species cultivated in the world. However, there are few studies evaluating the effects of stunning methods on the stress of this fish. The aim of this study was to evaluate the effect of electrical stunning (ES), CO2 narcosis (CN), and iced water (IW) on indicators of stress in tilapia, e.g., muscle adenosine triphosphate (ATP), enzymatic antioxidants (catalase, lactate dehydrogenase and glutathione reductase) and plasma cortisol. The muscle ATP was highest (P<0.05) in fish stunned by CN. However, the cortisol level was higher (P<0.05) in tilapia stunned by IW and CN. The levels of catalase in the white muscles were higher (P<0.05) in fish stunned by ES than in fish stunned by CN and IW. For the red muscles, the highest levels (P<0.05) of catalase were observed in tilapia stunned by ES and IW. Lactate dehydrogenase levels in the white muscles were higher (P<0.05) in fish stunned by ES and lower (P<0.05) in fish stunned by CN. In the red muscles, lactate dehydrogenase levels were higher (P<0.05) in fish stunned by IW in comparison to ES and CN. Therefore, in tilapia stunned by CN, the stress is lesser when compared to that caused by ES or IW and is in accordance with good practices of animal welfare.
References
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bass (Dicentrarchus labrax). Aquaculture, 287(1-2):139-144.
ALMEIDA, J.D.; DINIZ, Y.S.; MARQUES, S.F.;FAINE, L.A.; RIBAS, B.O.; BURNEIKO, R.C.; NOVELLI, E.L. 2002 The use of the oxidative stress responses as biomarkers in Nile tilapia (Oreochromis niloticus) exposed to in vivo cadmium contamination. Environment International, 27(8):
673-679.
ATENCIO, L.; MORENO, I.; JOS, A.; PRIETO, A.;MOYANO, R.; BLANCO, A.; CAMEAN, A.M.2009 Effects of dietary selenium on the oxidative stress and pathological changes in tilapia (Oreochromis niloticus) exposed to a microcystinproducing cyanobacterial water bloom. Toxicon,53(2): 269í 282.
BARRETO, R.E. e VOLPATO, G.L. 2004 Caution for using ventilatory frequency as an indicator of
stress in fish. Behavioural Processes, 66(1): 43í 51.
BARTON, B.A. 2002 Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integrative and Comparative Biology, 42(3): 517-525.
BEERS, R.F. e SIZER, I.W.A. 1952 Spectophotometric method for measuring the breakdown of
hydrogen peroxide by catalase. The Journal of Biological Chemistry, 195: 133-140.
BERNAL, D.; SMITH, D.; LOPEZ, G.; WEITZ, D.; GRIMMINGER, T.; DICKSON, K.; GRAHAM, J.B. 2003 Comparative studies of high performance swimming in sharks II. Metabolic biochemistry of locomotor and myocardial muscle in endothermic and ectothermic sharks. The Journal of Experimental Biology, 206: 2845-2857.
BERNT, E. e BERGMEYER, H.U. 1974 Lactate desydrogenase assay. In: BERGMEYER, H.U. Methods of enzymatic analysis. London: Academic Press. p.1196-1201.
BERTOTTO, D.; POLTRONIERI, C.; NEGRATO, E.; MAJOLINI, D.; RADAELLI, G.; SIMONTACCHI,
C. 2010 Alternative matrices for cortisol measurement in fish. Aquaculture Research, 41(8):1261-1267.
BRADFORD, M.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(1-2): 248-254.
BRAITHWAITE, V.A. e BOULCOTT, P. 2007 Pain perception, aversion and fear in fish. Diseases of
Aquatic Organisms, 75(2): 131í 138.
BURNS, G.B. e KEE, P.J. 1985 Liquid chromatographic determination of hypoxanthine
content in fish tissue. Journal of the Association Official Analytical Chemists, 68(3): 444-448.
CADENAS, S. e DAVIES, K.J.A. 2000 Mitochondrial free radical generation, oxidative stress and
aging. Free Radical Biology and Medicine, 29(3-4):222-230.
CALBERG, I. e MANNERVICK, B. 1985 Glutathione reductase In: CALBERG, I. e MANNERVICK B.
Methods in enzymology. New York: Academic Press. p.484-490.
CLUTTERHAM, S.; GAMPERL, A.K.; WALLACE,H.L.; CRAWSHAW, L.I.; FARRELL, A.P. 2004
Exhaustive exercise does not affect the preferred temperature for recovery in juvenile rainbow
trout (Oncorhynchus mykiss). Physiological and Biochemical Zoology, 77(4): 611-618.
DALZIEL, A.C.; MOORE, S.E.; MOYES, C.D. 2005 Mitochondrial enzyme content in the muscle of
high-performance fish: evolution and variation among fiber types. American Journal of Physiology
Regulatory Integrative and Comparative Physiology,288: 163-172.
ERIKSON, U. 2011 Assessment of different stunning methods and recovery of farmed Atlantic
salmon (Salmo salar): isoeugenol, nitrogen and three levels of carbon dioxide. Animal Welfare,
20: 365-375.
ERIKSON, U.; HULTMANN, L.; STEEN, J.E. 2006 Live chilling of Atlantic salmon (Salmo salar)
combined with mild carbon dioxide anaesthesia I. Establishing a method for large-scale
processing of farmed fish. Aquaculture, 252(2-4):183-198.
FERREIRA, M.; MORADAS-FERREIRA, P.; REISHENRIQUE, M.A. 2005 Oxidative stress biomarkers in two resident species, mullet (Mugil cephalus) and flounder (Platichthys flesus),from a polluted site in river Douro estuary, Portugal. Aquatic Toxicology, 71(1): 39-48.
FIGUEIREDO-FERNANDES, A.; FONTAINHASFERNANDES, A.; PEIXOTO, F.; ROCHA, E.; REIS-HENRIQUES, M.A. 2006 Effects of gender and temperature on oxidative stress enzymes in
Nile tilapia Oreochromis niloticus exposed to paraquat. Pesticide Biochemistry and Physiology,
85(2): 97í 103.
FOSS, A.; GRIMSBO, E.; VIKINGSTAD, E.; NORTVEDT, R.; SLINDE, E.; ROTH, B. 2012 Live chilling of Atlantic salmon: physiological response to handling and temperature decrease on welfare. Fish Physiology Biochemistry, 38(2):565-571.
GIUFFRIDA, A.; PENNISI, L.; ZIINO, G.; FORTINO,L.; VALVO, G.; MARINO, S.; PANEBIANCO, A.
2007 Influence of slaughtering method on some aspects of quality of gilthead sea bream and
smoked rainbow trout. Veterinary Research Comunications, 31(4): 437-446.
HALLIWELL, B. 1994 Free radicals and antioxidants: a personal view. Nutrition Reviews, 52(8): 253-265.
HALLIWELL, B. e GUTTERIDGE, J.M.C. 2007 Free radicals in biology and medicine. 4a ed. Oxford:
Oxford University Press. 888p.
IWAMA, G.K.; AFONSO, L.O.B.; TODGHAM, A.; ACKERMAN, P.; NAKANO, K. 2004 Are HSPS
suitable for indicating stressed states in fish? The Journal of Experimental Biology, 207: 15-19.
JOS, A.; PICHARDO, S.; PRIETO, A.I.; REPETTO, G.;VÁZQUEZ, C.M.; MORENO, I.; CAMEÁN,
A.M. 2005 Toxic cyanobacterial cells containing microcystins induce oxidative stress in exposed
tilapia fish (Oreochromis sp.) under laboratory conditions. Aquatic Toxicology, 72(3): 261í 271.
KESTIN, S.C.; VAN DE VIS, J.W.; ROBB, D.H.F. 2002 Protocol for assessing brain function in fish and
the effectiveness of methods used to stun and kill them. Veterinary Records, 150(10): 302-307.
KNOWLES, T.G.; BROWN, S.N.; WARRISS, P.D.; LINES, J.; TINARWO, A.; BRAVO, A.;CARVALHO, H.; GONí"¡ALVES, A. 2007 Effect of electrical stunning at slaughter on the carcass,flesh and eating of farmed sea bass (Dicentrarchus labrax). Aquaculture Research,38(16): 1732-1741.
LAMBOOIJ, E.; GERRITZEN, M.A.; REIMERT, H.;BURGGRAAF, D.; VAN DE VIS, J.W. 2008 A humane protocol for electro-stunning and killing of Nile tilapia in fresh water. Aquaculture, 275(1-4): 88-95.
LEFíˆVRE, F.; BUGEON, J.; AUPÉRIN, B.; AUBIN, J. 2008 Rearing oxygen level and slaughter stress
effects on rainbow trout flesh quality. Aquaculture, 284(1-4): 81-89.
LINES, J.A. e SPENCE, J. 2011 Safeguarding the welfare of farmed fish at harvest. Fish Physiology
Biochemistry, 38(1): 153-162.
MCKENZIE, D.J.; WONG, S.; RANDALL, D.J.;EGGINTON, S.; TAYLOR, E.W.; FARRELL, A.P.2004 The effects of sustained exercise and hypoxia upon oxygen tensions in the red muscle of rainbow trout. The Journal of Experimental Biology, 207(21): 3629-3637.
MARX, H.; BRUNNER, B.; WEINZIERL, W.; HOLFMANN, R.; STOLLE, A. 1997 Methods of stunning freshwater fish: Impact on meat quality and aspects of animal welfare. Zeitschrift für
Lebensmittel-Untersuchung und -Forschung, 204(4): 282-286.
OZOGUL, Y. e OZOGUL, F. 2004 Effects of slaughtering methods on sensory, chemical and microbiological quality of rainbow trout (Onchorynchus mykiss) stored in ice and map.European Food Research Technology, 219(3): 211-213.
PANDEY, S.; PARVEZ, S.; SAYEED, I.; HAQUE, R.;BIN-HAFEEZ, B.; RAISUDDIN, S. 2003 Biomarkers
of oxidative stress: a comparative study of river Yamuna fish wallago Attu (bl. & schn.). Science
of the Total Environment, 309(1-3): 105í 115.
PEIXOTO, F.; ALVES-FERNANDES, D.; SANTOS,D.; FONTAÍNHAS-FERNANDES, A. 2006
Toxicological efects of oxyxuorfen on oxidative stress enzymes in tilapia Oreochromis niloticus.
Pesticide Biochemistry and Physiology, 85(2): 91í 96.
POLI, B.M.; PARISI, G.; SCAPPINI, F.; ZAMPACAVALLO, G. 2005 Fish welfare and quality as affected by pre-slaughter and slaughter management. Aquaculture International,13(1-2): 29í 49.
POPMA, T.J. e LOVSHIN, L.L. 1995 Worldwide prospects for commercial production of tilapia.
Commercial Tilapia Production. 42p. Availableat: <http://www.aces.edu/dept/fisheries/aqua
culture/docs/worldtilapia.pdf> Acesso em: 23 abr. 2014.
RIBAS, L.; FLOS, R.; REIG, L.; MACKENZIE, S.; BARTON, B.A.; TORT, L. 2007 Comparison of methods for anaesthetizing Senegal sole (Solea senegalensis) before slaughter: Stress responses and final product quality. Aquaculture, 269(1-4):250-258.
ROTH, B, SLINDE, E.; ROBB, DHF. 2006 Field evaluation of live chilling with CO2 on stunning
Atlantic salmon (Salmo salar) and the subsequent effect on quality. Aquaculture Research, 37(8):
799-804.
ROTH, B.; MOELLER, D.; VELAND, J.O.;IMSLAND, A.; SLINDE, E. 2002 The effect of stunning methods on rigor mortis and texture properties of Atlantic salmon (Salmo salar).Journal of Food Science, 67(4): 1462-1466.
ROTH, B.; IMSLAND, A.; GUNNARSSON, S.; FOSS, A.; SCHELVIS-SMIT, R. 2007 Slaughter quality and
rigor contraction in farmed turbot (Scophthalmusmaximus): a comparison between different
stunning methods. Aquaculture, 272(1-4): 754-761.
SCHERER, R.; AUGUSTI, P.R.; STEFFENS, C.; BOCHI, V.C.; HECKTHEURER, L.H.; LAZZARI, R.; RADUNZ-NETO, J.; POMBLUM, S.C.G.; EMANUELLI, T. 2005 Effect of slaughter method on postmortem changes of grass carp (Ctenopharyngodon idella) stored in ice. Journal of Food Science, 70(5): 348-353.
SKJERVOLD, P.O.; FJAERA, S.O.; OSTBY, P.B.; EINEN, O. 2001 Live-chilling and crowding stress before slaughter of Atlantic salmon. Aquaculture, 192(2-4): 265-280.
VAN DE VIS, H.; KESTIN, S.; ROBB, D.; OEHLENSCHLAGER, J.; LAMBOOIJ, B.; MUNKNER, W.; KUHLMANN, H.; KLOOSTERBOER, K.; TEJADA, M.; HUIDOBRO,A.; OTTERA, H.; ROTH, B.; SORENSEN, N.K.;AKSE, L.; BYRNE, H.; NESVADBA, P. 2003 Is humane slaughter of fish possible for industry?
Aquaculture Research, 34(3): 211-220.
VIEGAS, E.M.M.; PIMENTA, F.A.; PREVIERO, T.C.; GONí"¡ALVES, L.U.; DURíES, J.P.; RIBEIRO,M.A.R.; OLIVEIRA FILHO, P.R.C. 2012 Métodos de abate e qualidade da carne de peixe. Archivos de Zootecnia, 61(R): 41-50.
WENDELAAR BONGA, S.E. 1997 The stress response in fish. Physiological Reviews, 77(3): 591-625.
WINSTON, G.W. and DI GIULIO, R.T. 1991 Prooxidant and antioxidant mechanisms in aquatic organism. Aquatic Toxicology, 19(2):137-161.
bass (Dicentrarchus labrax). Aquaculture, 287(1-2):139-144.
ALMEIDA, J.D.; DINIZ, Y.S.; MARQUES, S.F.;FAINE, L.A.; RIBAS, B.O.; BURNEIKO, R.C.; NOVELLI, E.L. 2002 The use of the oxidative stress responses as biomarkers in Nile tilapia (Oreochromis niloticus) exposed to in vivo cadmium contamination. Environment International, 27(8):
673-679.
ATENCIO, L.; MORENO, I.; JOS, A.; PRIETO, A.;MOYANO, R.; BLANCO, A.; CAMEAN, A.M.2009 Effects of dietary selenium on the oxidative stress and pathological changes in tilapia (Oreochromis niloticus) exposed to a microcystinproducing cyanobacterial water bloom. Toxicon,53(2): 269í 282.
BARRETO, R.E. e VOLPATO, G.L. 2004 Caution for using ventilatory frequency as an indicator of
stress in fish. Behavioural Processes, 66(1): 43í 51.
BARTON, B.A. 2002 Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integrative and Comparative Biology, 42(3): 517-525.
BEERS, R.F. e SIZER, I.W.A. 1952 Spectophotometric method for measuring the breakdown of
hydrogen peroxide by catalase. The Journal of Biological Chemistry, 195: 133-140.
BERNAL, D.; SMITH, D.; LOPEZ, G.; WEITZ, D.; GRIMMINGER, T.; DICKSON, K.; GRAHAM, J.B. 2003 Comparative studies of high performance swimming in sharks II. Metabolic biochemistry of locomotor and myocardial muscle in endothermic and ectothermic sharks. The Journal of Experimental Biology, 206: 2845-2857.
BERNT, E. e BERGMEYER, H.U. 1974 Lactate desydrogenase assay. In: BERGMEYER, H.U. Methods of enzymatic analysis. London: Academic Press. p.1196-1201.
BERTOTTO, D.; POLTRONIERI, C.; NEGRATO, E.; MAJOLINI, D.; RADAELLI, G.; SIMONTACCHI,
C. 2010 Alternative matrices for cortisol measurement in fish. Aquaculture Research, 41(8):1261-1267.
BRADFORD, M.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(1-2): 248-254.
BRAITHWAITE, V.A. e BOULCOTT, P. 2007 Pain perception, aversion and fear in fish. Diseases of
Aquatic Organisms, 75(2): 131í 138.
BURNS, G.B. e KEE, P.J. 1985 Liquid chromatographic determination of hypoxanthine
content in fish tissue. Journal of the Association Official Analytical Chemists, 68(3): 444-448.
CADENAS, S. e DAVIES, K.J.A. 2000 Mitochondrial free radical generation, oxidative stress and
aging. Free Radical Biology and Medicine, 29(3-4):222-230.
CALBERG, I. e MANNERVICK, B. 1985 Glutathione reductase In: CALBERG, I. e MANNERVICK B.
Methods in enzymology. New York: Academic Press. p.484-490.
CLUTTERHAM, S.; GAMPERL, A.K.; WALLACE,H.L.; CRAWSHAW, L.I.; FARRELL, A.P. 2004
Exhaustive exercise does not affect the preferred temperature for recovery in juvenile rainbow
trout (Oncorhynchus mykiss). Physiological and Biochemical Zoology, 77(4): 611-618.
DALZIEL, A.C.; MOORE, S.E.; MOYES, C.D. 2005 Mitochondrial enzyme content in the muscle of
high-performance fish: evolution and variation among fiber types. American Journal of Physiology
Regulatory Integrative and Comparative Physiology,288: 163-172.
ERIKSON, U. 2011 Assessment of different stunning methods and recovery of farmed Atlantic
salmon (Salmo salar): isoeugenol, nitrogen and three levels of carbon dioxide. Animal Welfare,
20: 365-375.
ERIKSON, U.; HULTMANN, L.; STEEN, J.E. 2006 Live chilling of Atlantic salmon (Salmo salar)
combined with mild carbon dioxide anaesthesia I. Establishing a method for large-scale
processing of farmed fish. Aquaculture, 252(2-4):183-198.
FERREIRA, M.; MORADAS-FERREIRA, P.; REISHENRIQUE, M.A. 2005 Oxidative stress biomarkers in two resident species, mullet (Mugil cephalus) and flounder (Platichthys flesus),from a polluted site in river Douro estuary, Portugal. Aquatic Toxicology, 71(1): 39-48.
FIGUEIREDO-FERNANDES, A.; FONTAINHASFERNANDES, A.; PEIXOTO, F.; ROCHA, E.; REIS-HENRIQUES, M.A. 2006 Effects of gender and temperature on oxidative stress enzymes in
Nile tilapia Oreochromis niloticus exposed to paraquat. Pesticide Biochemistry and Physiology,
85(2): 97í 103.
FOSS, A.; GRIMSBO, E.; VIKINGSTAD, E.; NORTVEDT, R.; SLINDE, E.; ROTH, B. 2012 Live chilling of Atlantic salmon: physiological response to handling and temperature decrease on welfare. Fish Physiology Biochemistry, 38(2):565-571.
GIUFFRIDA, A.; PENNISI, L.; ZIINO, G.; FORTINO,L.; VALVO, G.; MARINO, S.; PANEBIANCO, A.
2007 Influence of slaughtering method on some aspects of quality of gilthead sea bream and
smoked rainbow trout. Veterinary Research Comunications, 31(4): 437-446.
HALLIWELL, B. 1994 Free radicals and antioxidants: a personal view. Nutrition Reviews, 52(8): 253-265.
HALLIWELL, B. e GUTTERIDGE, J.M.C. 2007 Free radicals in biology and medicine. 4a ed. Oxford:
Oxford University Press. 888p.
IWAMA, G.K.; AFONSO, L.O.B.; TODGHAM, A.; ACKERMAN, P.; NAKANO, K. 2004 Are HSPS
suitable for indicating stressed states in fish? The Journal of Experimental Biology, 207: 15-19.
JOS, A.; PICHARDO, S.; PRIETO, A.I.; REPETTO, G.;VÁZQUEZ, C.M.; MORENO, I.; CAMEÁN,
A.M. 2005 Toxic cyanobacterial cells containing microcystins induce oxidative stress in exposed
tilapia fish (Oreochromis sp.) under laboratory conditions. Aquatic Toxicology, 72(3): 261í 271.
KESTIN, S.C.; VAN DE VIS, J.W.; ROBB, D.H.F. 2002 Protocol for assessing brain function in fish and
the effectiveness of methods used to stun and kill them. Veterinary Records, 150(10): 302-307.
KNOWLES, T.G.; BROWN, S.N.; WARRISS, P.D.; LINES, J.; TINARWO, A.; BRAVO, A.;CARVALHO, H.; GONí"¡ALVES, A. 2007 Effect of electrical stunning at slaughter on the carcass,flesh and eating of farmed sea bass (Dicentrarchus labrax). Aquaculture Research,38(16): 1732-1741.
LAMBOOIJ, E.; GERRITZEN, M.A.; REIMERT, H.;BURGGRAAF, D.; VAN DE VIS, J.W. 2008 A humane protocol for electro-stunning and killing of Nile tilapia in fresh water. Aquaculture, 275(1-4): 88-95.
LEFíˆVRE, F.; BUGEON, J.; AUPÉRIN, B.; AUBIN, J. 2008 Rearing oxygen level and slaughter stress
effects on rainbow trout flesh quality. Aquaculture, 284(1-4): 81-89.
LINES, J.A. e SPENCE, J. 2011 Safeguarding the welfare of farmed fish at harvest. Fish Physiology
Biochemistry, 38(1): 153-162.
MCKENZIE, D.J.; WONG, S.; RANDALL, D.J.;EGGINTON, S.; TAYLOR, E.W.; FARRELL, A.P.2004 The effects of sustained exercise and hypoxia upon oxygen tensions in the red muscle of rainbow trout. The Journal of Experimental Biology, 207(21): 3629-3637.
MARX, H.; BRUNNER, B.; WEINZIERL, W.; HOLFMANN, R.; STOLLE, A. 1997 Methods of stunning freshwater fish: Impact on meat quality and aspects of animal welfare. Zeitschrift für
Lebensmittel-Untersuchung und -Forschung, 204(4): 282-286.
OZOGUL, Y. e OZOGUL, F. 2004 Effects of slaughtering methods on sensory, chemical and microbiological quality of rainbow trout (Onchorynchus mykiss) stored in ice and map.European Food Research Technology, 219(3): 211-213.
PANDEY, S.; PARVEZ, S.; SAYEED, I.; HAQUE, R.;BIN-HAFEEZ, B.; RAISUDDIN, S. 2003 Biomarkers
of oxidative stress: a comparative study of river Yamuna fish wallago Attu (bl. & schn.). Science
of the Total Environment, 309(1-3): 105í 115.
PEIXOTO, F.; ALVES-FERNANDES, D.; SANTOS,D.; FONTAÍNHAS-FERNANDES, A. 2006
Toxicological efects of oxyxuorfen on oxidative stress enzymes in tilapia Oreochromis niloticus.
Pesticide Biochemistry and Physiology, 85(2): 91í 96.
POLI, B.M.; PARISI, G.; SCAPPINI, F.; ZAMPACAVALLO, G. 2005 Fish welfare and quality as affected by pre-slaughter and slaughter management. Aquaculture International,13(1-2): 29í 49.
POPMA, T.J. e LOVSHIN, L.L. 1995 Worldwide prospects for commercial production of tilapia.
Commercial Tilapia Production. 42p. Availableat: <http://www.aces.edu/dept/fisheries/aqua
culture/docs/worldtilapia.pdf> Acesso em: 23 abr. 2014.
RIBAS, L.; FLOS, R.; REIG, L.; MACKENZIE, S.; BARTON, B.A.; TORT, L. 2007 Comparison of methods for anaesthetizing Senegal sole (Solea senegalensis) before slaughter: Stress responses and final product quality. Aquaculture, 269(1-4):250-258.
ROTH, B, SLINDE, E.; ROBB, DHF. 2006 Field evaluation of live chilling with CO2 on stunning
Atlantic salmon (Salmo salar) and the subsequent effect on quality. Aquaculture Research, 37(8):
799-804.
ROTH, B.; MOELLER, D.; VELAND, J.O.;IMSLAND, A.; SLINDE, E. 2002 The effect of stunning methods on rigor mortis and texture properties of Atlantic salmon (Salmo salar).Journal of Food Science, 67(4): 1462-1466.
ROTH, B.; IMSLAND, A.; GUNNARSSON, S.; FOSS, A.; SCHELVIS-SMIT, R. 2007 Slaughter quality and
rigor contraction in farmed turbot (Scophthalmusmaximus): a comparison between different
stunning methods. Aquaculture, 272(1-4): 754-761.
SCHERER, R.; AUGUSTI, P.R.; STEFFENS, C.; BOCHI, V.C.; HECKTHEURER, L.H.; LAZZARI, R.; RADUNZ-NETO, J.; POMBLUM, S.C.G.; EMANUELLI, T. 2005 Effect of slaughter method on postmortem changes of grass carp (Ctenopharyngodon idella) stored in ice. Journal of Food Science, 70(5): 348-353.
SKJERVOLD, P.O.; FJAERA, S.O.; OSTBY, P.B.; EINEN, O. 2001 Live-chilling and crowding stress before slaughter of Atlantic salmon. Aquaculture, 192(2-4): 265-280.
VAN DE VIS, H.; KESTIN, S.; ROBB, D.; OEHLENSCHLAGER, J.; LAMBOOIJ, B.; MUNKNER, W.; KUHLMANN, H.; KLOOSTERBOER, K.; TEJADA, M.; HUIDOBRO,A.; OTTERA, H.; ROTH, B.; SORENSEN, N.K.;AKSE, L.; BYRNE, H.; NESVADBA, P. 2003 Is humane slaughter of fish possible for industry?
Aquaculture Research, 34(3): 211-220.
VIEGAS, E.M.M.; PIMENTA, F.A.; PREVIERO, T.C.; GONí"¡ALVES, L.U.; DURíES, J.P.; RIBEIRO,M.A.R.; OLIVEIRA FILHO, P.R.C. 2012 Métodos de abate e qualidade da carne de peixe. Archivos de Zootecnia, 61(R): 41-50.
WENDELAAR BONGA, S.E. 1997 The stress response in fish. Physiological Reviews, 77(3): 591-625.
WINSTON, G.W. and DI GIULIO, R.T. 1991 Prooxidant and antioxidant mechanisms in aquatic organism. Aquatic Toxicology, 19(2):137-161.
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