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Temporal variation in oxidative stress indicators in liver of totoaba (Totoaba macdonaldi) Perciformes: Sciaenidae

Published online by Cambridge University Press:  31 January 2017

Sandra Berenice Hernández-Aguilar ,
Tania Zenteno-Savin ,
Juan Antonio De-Anda-Montañez  and
Lia Celina Méndez-Rodríguez
Sandra Berenice Hernández-Aguilar
Affiliation:
Centro de Investigaciones Biológicas del Noroeste, S.C., Instituto Politécnico Nacional 195, Col. Playa Palo de Santa Rita Sur, La Paz, Baja California Sur, 23096, Mexico
Tania Zenteno-Savin*
Affiliation:
Centro de Investigaciones Biológicas del Noroeste, S.C., Instituto Politécnico Nacional 195, Col. Playa Palo de Santa Rita Sur, La Paz, Baja California Sur, 23096, Mexico
Juan Antonio De-Anda-Montañez
Affiliation:
Centro de Investigaciones Biológicas del Noroeste, S.C., Instituto Politécnico Nacional 195, Col. Playa Palo de Santa Rita Sur, La Paz, Baja California Sur, 23096, Mexico
Lia Celina Méndez-Rodríguez
Affiliation:
Centro de Investigaciones Biológicas del Noroeste, S.C., Instituto Politécnico Nacional 195, Col. Playa Palo de Santa Rita Sur, La Paz, Baja California Sur, 23096, Mexico
*
Correspondence should be addressed to: T. Zenteno-Savin, Centro de Investigaciones Biológicas del Noroeste, S.C., Instituto Politécnico Nacional 195, Col. Playa Palo de Santa Rita Sur, La Paz, Baja California Sur, 23096, Mexico email: tzenteno04@cibnor.mx
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Abstract

Several characteristics of Totoaba macdonaldi Perciformes: Sciaenidae, including migratory movements along temperature gradients make it vulnerable to oxidative stress. Oxidative stress can also be associated with reproduction. The objectives of the present study were to examine oxidative stress indicators in liver of totoaba throughout the seasons (spring, autumn and winter), and the associated fluctuations in superficial sea temperature (SST, °C), as well as to evaluate possible variations between sexes and reproductive maturity stages. A total of 173 liver samples from totoaba captured in the Gulf of California, Mexico, were obtained from April 2010 to February 2013. Superoxide radical production (O2•−), lipid peroxidation (TBARS) levels, and activity of antioxidant enzymes; superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPx), glutathione reductase (GR) and glutathione S-transferase (GST) were quantified spectrophotometrically. Generalized linear models (GLM) were used to determine which factors contribute to explain O2•− production and TBARS levels. The significant predictive variables were the seasons, which were significant in all applied models, as well as SOD and CAT activities. In general, enzyme activity was higher in immature totoaba; this was not seasonally modified. Low temperatures in winter were associated with high O2•− production and TBARS levels, particularly in totoaba that are not yet reproductively mature. Seasonal changes in sea surface temperature did not affect the oxidative stress indicators in mature totoaba (both males and females); this suggests that mature totoaba are less sensitive to temperature changes from an oxidative stress perspective.

Keywords

Antioxidant enzymesuperficial sea temperatureTotoaba macdonaldi
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Issue 4 , June 2018 , pp. 833 - 844
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

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References

REFERENCES

Abele, D., Heise, K., Pörtner, H.O. and Puntarulo, S. (2002) Temperature dependence of mitochondrial function and production of reactive oxygen species in the intertidal mud clam Mya arenaria. Journal of Experimental Biology 205, 1831–1841.CrossRefGoogle ScholarPubMed
Abele, D. and Puntarulo, S. (2004) Formation of reactive species and induction of antioxidant defense systems in polar and temperate marine invertebrates and fish. Comparative Biochemistry and Physiology Part A 138, 405–415.Google Scholar
Akaike, H. (1973) Information theory and an extension of the maximum likelihood principle. In Petrov, B.N. and Csaki, F. (eds) Second international symposium on information theory. Budapest: Academiai Kiado, pp. 267–281.Google Scholar
Allen, J.R. and Wootton, R.J. (1982) Effect of food on the growth of carcase, liver and ovary in female Gasterosteus aculeatus L. Journal of Fish Biology 21, 537–547.CrossRefGoogle Scholar
Amado, L.L., Berteaux, R., Geracitano, L., Monserrat, J. and Bianchini, A. (2006b) Biomarkers of exposure and effect in the Brazilian flounder Paralichthys orbignyanus (Teleostei: Paralichthyidae) from the Patos Lagoon estuary (Southern Brazil). Marine Pollution Bulletin 52, 207–213.CrossRefGoogle ScholarPubMed
Amado, L.L., da Rosa, C.E., Meirelles, A., Moraes, L., Vaz Pires, W., Leães, G., Martinez, C., Berteaux, R., Maia, L., Monserrat, J., Bianchini, A., Martinez, P. and Garacitano, L. (2006a) Biomarkers in croakers Micropogonias furnieri (Teleostei, Sciaenidae) from polluted and non-polluted areas from the Patos Lagoon estuary (Southern Brazil): evidences of genotoxic and immunological effects. Marine Pollution Bulletin 52, 199–206.CrossRefGoogle ScholarPubMed
Aten, R.F., Duarte, K.M. and Behrman, H.R. (1992) Regulation of ovarian antioxidant vitamins, reduced glutathione, and lipid peroxidation by luteinizing hormone and prostaglandin F2α. Biology of Reproduction 46, 401–407.CrossRefGoogle Scholar
Bagnyukova, T.V., Luzhna, L.I., Pogribny, I.P. and Lushchak, V.I. (2007) Oxidative stress and antioxidant defenses in goldfish liver in response to short-term exposure to arsenite. Environmental and Molecular Mutagenesis 48, 658–665.Google Scholar
Bañuelos-Vargas, I., López, L.M., Pérez-Jiménez, A. and Peres, H. (2014) Effect of fishmeal replacement by soy protein concentrate with taurine supplementation on hepatic intermediary metabolism and antioxidant status of totoaba juveniles (Totoaba macdonaldi). Comparative Biochemistry and Physiology Part B 170, 18–25.CrossRefGoogle ScholarPubMed
Berdegué, A.J. (1955) La pesquería de Totoaba (Cynoscion macdonaldi) en San Felipe, Baja California. Revista de la Sociedad Mexicana de Historia Natural 16, 45–78.Google Scholar
Bradford, M. (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–253.CrossRefGoogle Scholar
Brett, J.R. (1965) The relation of size to rate of oxygen consumption and sustained swimming speed of sockeye salmon (Oncorhynchus nerka). Journal of the Fisheries Research Board of Canada 6, 1491–1501.CrossRefGoogle Scholar
Buchner, T., Abele-Oeschger, D. and Theede, H. (1996) Aspects of antioxidant status in the polychaete Arenicola marina: tissue and subcellular distribution, and reaction to environmental hydrogen peroxide and elevated temperatures. Marine Ecology Progress Series 143, 141–150.CrossRefGoogle Scholar
Buege, J.A. and Aust, S.D. (1978) Microsomal lipid peroxidation. In Packer, L. (ed.) Methods in enzymology, Vol. 52: Biomembranes. Part C. Biological oxidation microsomal, cytochrome p 450, and other hemoprotein systems. New York, NY: Academic Press, pp. 302–310.Google Scholar
Cassini, A., Favero, M. and Albergoni, V. (1993) Comparative studies of antioxidant enzymes in red-blooded and white-blooded Antarctic teleost fish, Pagothenia bernacchii and Chionodraco hamatus. Comparative Biochemistry and Physiology Part C 106, 333–336.Google Scholar
Chapelle, S., Meister, R., Brichon, G. and Zwingelstein, G. (1997) Influence of temperature on the phospholipid metabolism of various tissues from the crab Carcinus maenas. Comparative Biochemistry and Physiology Part B 58, 413–417.CrossRefGoogle Scholar
Chung, M.L., Galano, J.M., Oger, C., Durand, T. and Chung-Yung, J.L. (2015) Hyperoxia elevates adrenic acid peroxidation in marine fish and is associated with reproductive pheromone mediators. Marine Drugs 13, 2215–2232.CrossRefGoogle ScholarPubMed
Chung, M.L., Lee, K.Y. and Lee, C.Y.J. (2013) Profiling of oxidized lipid products of marine fish under acute oxidative stress. Food Chemical Toxicology 53, 205–213.CrossRefGoogle ScholarPubMed
Cisneros-Mata, M.A., Botsford, L.W. and Quinn, J.F. (1997) Projecting viability of Totoaba macdonaldi, a population with unknown age-dependent variability. Ecological Applications 7, 968–980.Google Scholar
Cisneros-Mata, M.A., Montemayor-López, G. and Román-Rodríguez, M.J. (1995) Life history and conservation of Totoaba macdonaldi. Conservation Biology 9, 806–814.CrossRefGoogle Scholar
Costantini, D., Dell'Ariccia, G. and Lipp, H.P. (2008) Long flights and age affect oxidative status of homing pigeons (Columba livia). Journal of Experimental Biology 211, 377–381.CrossRefGoogle ScholarPubMed
Dammann, P. and Burda, H. (2006) Sexual activity and reproduction delay aging in a mammal. Current Biology 16, 117–118.CrossRefGoogle Scholar
De-Anda-Montañez, J.A., García de León, F., Zenteno-Savín, T., Balart, E.F., Méndez-Rodríguez, L.C., Bocanegra-Castillo, N., Martínez-Aguilar, S., Campos-Dávila, L., Román-Rodríguez, M.J., Valenzuela-Quiñónez-Valenzuela, F., Rodríguez-Jaramillo, M.C., Meza-Chávez, M.E., Ramírez-Rosas, J.J., Saldaña-Hernández, I.J., Olguín-Monroy, N.O. and Martínez-Delgado, M.E. (2013) Estado de salud y estatus de conservación de la(s) poblacion(es) de totoaba (Totoaba macdonaldi) en el Golfo de California: una especie en peligro de extinción. La Paz: Comisión Nacional para el Conocimiento y Uso de la Biodiversidad.Google Scholar
De Zwart, L.L., Meerman, J.H., Commandeur, J.N. and Vermeulen, N.P. (1999) Biomarkers of free radical damage applications in experimental animals and in humans. Free Radical Biology and Medicine 26, 202–226.CrossRefGoogle ScholarPubMed
Drossos, G., Lazou, A., Panagopoulos, P. and Westaby, S. (1995) Deferoxamine cardioplegia reduces superoxide radical production in human myocardium. Annals of Thoracic Surgery 59, 169–172.Google Scholar
Encina, L. and Granado-Lorencio, C. (1997) Seasonal changes in condition, nutrition, gonad maturation and energy content in barbel, Barbus sclateri, inhabiting a fluctuating river. Environmental Biology. Fishes 50, 75–84.CrossRefGoogle Scholar
Ferreira, M., Moradas-Ferreira, P. and Reis-Henriques, 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, 39–48.CrossRefGoogle ScholarPubMed
Filho, D.W., Giulivi, C. and Boveris, A. (1993) Antioxidant defences in marine fish – I. Teleosts. Comparative Biochemistry and Physiology Part C 106, 409–413. doi: 10.1016/0742-8413(93)90154-D.CrossRefGoogle Scholar
Flanagan, C.A. and Hendrickson, R. (1976) Observations on the commercial fishery and reproductive biology of the totoaba Cynoscion macdonaldi in the northern Gulf of California. Fishery Bulletin 74, 531–544.Google Scholar
Folhé, L. and Günzler, W.A. (1984) Assays for glutathione peroxidase. In Packer, L. (ed.). Methods in enzymology. Oxygen radicals in biological systems. New York, NY: Academic Press, pp. 105, 114–120.CrossRefGoogle Scholar
Freire, C.A., Welker, A.F., Storey, J.M., Storey, K.B. and Hermes-Lima, M. (2011) Oxidative stress in estuarine and intertidal environments (temperate and tropical). In Abele, D., Vázquez-Medina, J.P. and Zenteno-Savín, T. (eds) Oxidative stress in aquatic ecosystems. Chichester: John Wiley & Sons. doi: 10.1002/9781444345988.ch3.Google Scholar
Garratt, M., Vasilaki, A., Stockley, P., McArdle, F., Jackson, M. and Hurst, J. (2010) Is oxidative stress a physiological cost of reproduction? An experimental test in house mice. Proceedings of the Royal Society of London B: Biological Science 278, 1098–1106. doi: 10.1098/rspb.2010.1818.Google ScholarPubMed
Goldberg, D.M. and Spooner, R.J. (1987) Glutathione reductase. In Bergmeyer, H.U. (ed.) Methods of enzymatic analysis, 3rd edition, Vol. III. Weinheim: Verlag Chemie, pp. 258–265.Google Scholar
Habig, W.H. and Jakoby, W.B. (1981) Glutathione S-transferases (rat and human). Methods in Enzymology 77, 218–235.CrossRefGoogle ScholarPubMed
Harshman, L.G. and Zera, A.J. (2007) The cost of reproduction – the devil in the details. Trends in Ecology and Evolution 22, 80–86.CrossRefGoogle ScholarPubMed
Heise, K., Puntarulo, S., Nikinmaa, M., Abele, D. and Pörtner, H.O. (2006) Oxidative stress during stressful heat exposure and recovery in the North Sea eelpout Zoarces viviparus L. Journal of Experimental Biology 209, 353–363.Google Scholar
Hermes-Lima, M. and Storey, K.B. (1993) Antioxidant defenses in the tolerance of freezing and anoxia by garter snakes. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 265, 646–652.Google Scholar
Jalabert, B. (2005) Particularities of reproduction and oogenesis in teleost fish compared to mammals. Reproduction Nutrition Development 45, 261–279.Google Scholar
Kregel, K.C. (2002) Invited review: heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. Journal of Applied Physiology 92, 2177–2186.CrossRefGoogle Scholar
Konigsberg, M. (2008) Radicales libres y estrés oxidativo. Aplicaciones médicas. Manual Moderno. Primera Edición. México D.F. 636 pp.Google Scholar
Kong, X., Wang, G. and Li, S. (2008) Seasonal variations of ATPase activity and antioxidant defenses in gills of the mud crab Scylla serrata (Crustacea, Decapoda). Marine Biology 154, 269–276.Google Scholar
Labrada-Martagon, V., Rodríguez, P.A.T., Méndez-Rodríguez, L.C. and Zenteno-Savin, T. (2011) Oxidative stress indicators and chemical contaminants in East Pacific green turtles (Chelonia mydas) inhabiting two foraging coastal lagoons in the Baja California peninsula. Comparative Biochemistry and Physiology Part C 154, 165–175.Google Scholar
Lesser, M.P. (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annual Review of Physiology 68, 253–278.Google Scholar
Liñán-Cabello, M.A., Flores-Ramírez, L.A., Zenteno-Savin, T., Olguín-Monroy, N.O., Sosa-Avalos, R., Patiño-Barragan, M. and Olivos-Ortiz, A. (2010) Seasonal changes of antioxidant and oxidative parameters in the coral Pocillopora capitata on the Pacific coast of Mexico. Marine Ecology Progress Series 31, 407–417.Google Scholar
López-Cruz, R.I., Zenteno-Savín, T. and Galván-Magaña, F. (2010) Superoxide production, oxidative damage and enzymatic antioxidant defenses in shark skeletal muscle. Comparative Biochemistry and Physiology 156, 50–56.Google Scholar
López, L.M., Durazo, E., Rodríguez-Gómez, A., True, C.D. and Viana, M.T. (2006) Proximate composition and fatty acid profile of wild and cultured juvenile Totoaba macdonaldi. Ciencias Marinas 32, 303–309.CrossRefGoogle Scholar
Love, R.M. (1970) The chemical biology of fishes. London: Academic Press.Google Scholar
Lowerre-Barbieri, S.K., Ganias, K., Saborido-Rey, F., Murua, H. and Hunter, J.R. (2011) Reproductive timing in marine fishes: variability, temporal scales, and methods. Marine and Coastal Fisheries 3, 71–91.CrossRefGoogle Scholar
Lushchak, V.I. (2011) Environmentally induced oxidative stress in aquatic animals. Aquatic Toxicology 101, 13–30.CrossRefGoogle ScholarPubMed
Lushchak, V.I. and Bagnyukova, T.V. (2006) Temperature increase results in oxidative stress in goldfish tissues. 1. Indices of oxidative stress. Comparative Biochemistry and Physiology Part C 143, 36–41.Google Scholar
Lyons, D.O. and Dunne, J.J. (2003) Reproductive cost to male and female worm pipefish. Journal of Fish Biology 58, 776–787.Google Scholar
Madeira, D., Narciso, L., Cabral, H.N., Vinagre, C. and Diniz, M.S. (2013) Influence of temperature in thermal and oxidative stress responses in estuarine fish. Comparative Biochemistry and Physiology Part A 166, 237–243.CrossRefGoogle ScholarPubMed
Matoo, O.B., Ivanina, A.V., Ullstad, C., Beniash, E. and Sokolova, I.M. (2013) Interactive effects of elevated temperature and CO2 levels on metabolism and oxidative stress in two common marine bivalves (Crassostrea virginica and Mercenaria mercenaria). Comparative Biochemistry and Physiology Part A 164, 545–553.Google Scholar
Metcalfe, N.B. and Monaghan, P. (2013) Does reproduction cause oxidative stress? An open question. Trends in Ecology and Evolution 28, 347–350. doi: 10.1016/j.tree.2013.01.015.Google Scholar
Miller, K.M, Schulze, A.D, Ginther, N., Li, S. Patterson, D.A., Farrell, A.P. and Hinch, S.G. (2009) Salmon spawning migration: metabolic shifts and environmental triggers. Comparative Biochemistry and Physiology Part D 4, 75–89.Google ScholarPubMed
Mommsen, T.P. (1998) Growth and metabolism. In Evans, D.H. (ed.) The physiology of fishes, 2nd edition. Boca Raton, FL: CRC Press, pp. 65–97.Google Scholar
Mommsen, T.P., French, C.J. and Hochachka, P.W. (1980) Sites and patterns of protein and amino acid utilization during the spawning migration of salmon. Canadian Journal of Zoology 10, 1785–1799.CrossRefGoogle Scholar
Monaghan, P., Metcalfe, N. and Torres, R. (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecology Letters 12, 75–92.Google Scholar
Oakes, K.D. and Van Der Kraak, G. (2003) Utility of the TBARS assay in detecting oxidative stress in white sucker (Catostomus commersoni) populations exposed to pulp mill effluent. Aquatic Toxicology 63, 447–463.CrossRefGoogle ScholarPubMed
Parihar, M.S., Dubey, A.K., Javeri, T. and Prakash, P. (1996) Changes in lipid peroxidation, superoxide dismutase activity, ascorbic acid and phospholipid content in liver of freshwater catfish Heteropneustes fossilis exposed to elevated temperature. Journal of Thermal Biology 21, 323–330.Google Scholar
Patiño, R. and Sullivan, C.V. (2002) Ovarian follicle growth, maturation, and ovulation in teleost fish. Fish Physiology Biochemistry 26, 57–70.Google Scholar
Pike, T., Blount, J., Bjerkeng, B., Lindström, J. and Metcalfe, N. (2007) Carotenoids, oxidative stress and female mating preference for longer lived males. Proceedings of the Royal Society of London B: Biological Science 274, 1591–1596.Google Scholar
Pörtner, H.O. (2002) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comparative Biochemistry and Physiology Part A 132, 739–761.Google Scholar
Pörtner, H.O. (2010) Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. Journal of Experimental Biology 213, 881–893.Google Scholar
Román-Rodríguez, M. and Hammann, G.M. (1997) Age and growth of totoaba, Totoaba macdonaldi (Sciaenidae), in the upper Gulf of California. Fishery Bulletin 95, 620–628.Google Scholar
Rudneva, I.I. (1995) The ratio of processes of lipid peroxidation and antioxidant activity in gonads of Elasmobranchia and teleost fishes of the Black Sea. Ukrainskii Biokhimicheskii Zhurnal 67, 72–79.Google Scholar
Rudneva, I.I., Skuratovskaya, E.N., Kuzminova, N.S. and Kovyrshina, T.B. (2010) Age composition and antioxidant enzyme activities in blood of Black Sea teleosts. Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology 151, 229–239.Google Scholar
Sies, H. (1997) Oxidative stress: oxidants and antioxidants. Experimental Physiology 82, 291–295.Google Scholar
Schmidt, C., Blount, J.D. and Bennett, N. (2014) Reproduction is associated with a tissue-dependent reduction of oxidative stress in eusocial female Damaraland mole-rats (Fukomys damarensis). PLoS ONE 9, e103286. doi: 10.1371/journal.pone.0103286.Google Scholar
Speakman, J.R. and Garratt, M. (2010) Oxidative stress as a cost of reproduction: beyond the simplistic trade-off model. Bioessays 36, 93–106.Google Scholar
Suzuki, K. (2000) Measurement of Mn-SOD and Cu, Zn-SOD. In Taniguchi, N. and Gutteridge, J. (eds) Experimental protocols for reactive oxygen and nitrogen species. Oxford: Oxford University Press, pp. 91–95.Google Scholar
Tkachenko, H., Kurhaluk, N., Grudniewska, J. and Andriichuk, A. (2014) Tissue-specific responses of oxidative stress biomarkers and antioxidant defenses in rainbow trout Oncorhynchus mykiss during a vaccination against furunculosis. Fish Physiology and Biochemistry 40, 1289–1300.Google Scholar
Tocher, D.R. (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Reviews in Fish Science 11, 107–184.CrossRefGoogle Scholar
Toyokuni, S. (1999) Reactive oxygen species-induced molecular damage and its application in pathology. Pathology International 49, 91–102.Google Scholar
Tremblay, N., Gómez-Gutiérrez, J., Zenteno-Savín, T., Robinson, C.J. and Sánchez-Velasco, L. (2010) Role of oxidative stress in seasonal and daily vertical migration of three species of krill in the Gulf of California. Limnology Oceanography 55, 2570–2584.CrossRefGoogle Scholar
Tyler, C.R. and Sumpter, J.P. (1996) Oocyte growth and development in teleost. Reviews in Fish Biology and Fisheries 6, 287–318.Google Scholar
Valenzuela-Quiñonez, F., Arreguín-Sánchez, F., Salas-Márquez, S., García-de-León, F.J., Garza, J.C., Román-Rodríguez, M. and de-Anda-Montañez, J.A. (2015) Critically endangered totoaba Totoaba macdonaldi: signs of recovery and potential threats after a population collapse. Endangered Species Research 29, 1–11. doi: 10.3354/esr00693.CrossRefGoogle Scholar
Valenzuela-Quiñonez, F., García-de-León, F., De Anda Montañez, J.A. and Balart, E.F. (2011) La totoaba del Golfo de California ¿Una especie en peligro de extinción? Interciencia 36, 664–671.Google Scholar
Valenzuela-Quiñonez, F., Garza, J.C., De-Anda-Montañez, J.A. and García-de-León, F.J. (2014) Inferring past demographic changes in a critically endangered marine fish after fishery collapse. ICES Journal of Marine Science 71, 1619–1628.Google Scholar
van Bohemen, Ch.G., Lambert, J.G. and Peute, J. (1981) Annual changes in plasma and liver in relation to vitellogenesis in the female rainbow trout, Salmo gairdneri. General and Comparative Endocrinology 44, 94–107.Google Scholar
Vasseur, P. and Cossu-Leguille, C. (2003) Biomarkers and community indices as complementary tools for environmental safety. Environment International 28, 711–717.Google Scholar
Vega-López, A., Galar-Martínez, M., Jimenez-Orozco, F.A., Garcia-Latorre, E. and Dominguez-López, M.L. (2007) Gender related differences in the oxidative stress response to PCB exposure in an endangered goodeid fish (Girardinichthys viviparus). Comparative Biochemistry and Physiology Part A 146, 672–678.Google Scholar
Vinagre, C., Madeira, D., Narciso, L.S., Cabral, H.N. and Diniz, M.S. (2012) Effect of temperature on oxidative stress in fish: lipid peroxidation and catalase activity in the muscle of juvenile seabass, Dicentrarchus labrax. Ecological Indicators 23, 274–279.CrossRefGoogle Scholar
Ware, D.M. (1975) Growth, metabolism, and optimal swimming speed of a pelagic fish. Journal of the Fisheries Research Board of Canada 1, 33–41.Google Scholar
Wolf, J.C. and Wolfe, M.J. (2005) A brief overview of non neoplastic hepatic toxicity in fish. Toxicologic Pathology 33, 75–85.Google Scholar
Wu, J. (1992) The involvement of lipid peroxidation in fatty liver haemorrhagic syndrome in laying hens. M.Sc. thesis. University of Guelph, Guelph, Canada.Google Scholar
Zanuy, S., Prat, F., Carrillo, M. and Bromage, N.R. (1995) Effects of constant photoperiod on spawning and plasma 17β-estradiol levels of sea bass (Dicentrarchus labrax). Aquatic Living Resources 8, 147–152.Google Scholar
Zar, J.H. (1999) Biostatistical analysis, 4th edition. Upper Saddle River, NJ: Prentice Hall.Google Scholar
Zenteno-Savín, T., Clayton-Hernández, E. and Elsner, R. (2002) Diving seals: are they a model for coping with oxidative stress? Comparative Biochemistry and Physiology Part C 133, 527–536.Google Scholar
Zenteno-Savín, T., Saldierna-Martínez, R. and Ahuejote-Sandoval, M. (2006) Superoxide radical production in response to environmental hypoxia in cultured shrimp. Comparative Biochemistry and Physiology Part C 142, 301–308.Google Scholar
Zenteno-Savín, T., St Leger, J. and Ponganis, P.J. (2010) Hypoxemic and ischemic tolerance in emperor penguins. Comparative Biochemistry and Physiology Part C 152, 18–23.Google Scholar