Abstract
The effects of temperature on European seabass (Dicentrarchus labrax L.) juveniles were investigated using a 30-day bioassay carried out at 18 and 25 °C in laboratory conditions. A multiparameter approach was applied including fish swimming velocity and several biochemical parameters involved in important physiological functions. Fish exposed for four weeks to 25 °C showed a decreased swimming capacity, concomitant with increased oxidative stress (increased catalase and glutathione peroxidase activities) and damage (increased lipid peroxidation levels), increased activity of an enzyme involved in energy production through the aerobic pathway (isocitrate dehydrogenase) and increased activities of brain and muscle cholinesterases (neurotransmission) compared to fish kept at 18 °C. Globally, these findings indicate that basic functions, essential for juvenile seabass surviving and well performing in the wild, such as predation, predator avoidance, neurofunction and ability to face chemical stress may be compromised with increasing water temperature. This may be of particular concern if D. labrax recruitment phase in northwest European estuaries and coastal areas happens gradually in more warm environments as a consequence of global warming. Considering that the selected endpoints are generally applied in monitoring studies with different species, these findings also highlight the need of more research, including interdisciplinary and multiparameter approaches, on the impacts of temperature on marine species, and stress the importance of considering scenarios of temperature increase in environmental monitoring and in marine ecological risk assessment.
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References
Almeida, J.R., C. Oliveira, C. Gravato, and L. Guilhermino. 2010. Linking behavioural alterations with biomarkers responses in the European seabass Dicentrarchus labrax L. exposed to the organophosphate pesticide fenitrothion. Ecotoxicology (London, England) 19: 1369–1381.
Almeida, J.R., C. Gravato, and L. Guilhermino. 2012a. Biological parameters towards polycyclic aromatic hydrocarbons pollution: a study with Dicentrarchus labrax L. exposed to the model compound benzo(a)pyrene. Water Air Soil Poll 223: 4709–4722.
Almeida, J.R., C. Gravato, and L. Guilhermino. 2012b. Challenges in assessing the toxic effects of polycyclic aromatic hydrocarbons to marine organisms: a case study on the acute toxicity of pyrene to the European seabass (Dicentrarchus labrax L.). Chemosphere 86: 926–937.
An, M.I., and C.Y. Choi. 2010. Activity of antioxidant enzymes and physiological responses in ark shell, Scapharca broughtonii, exposed to thermal and osmotic stress: effects on hemolymph and biochemical parameters. Comparative Biochemistry and Physiology. Part B, Biochemistry and Molecular Biology 155: 34–42.
Angilletta, M.J.J. 2009. Thermal adaptation: a theoretical and empirical synthesis. Oxford: Oxford University Press.
Aslanidi, K.B., D.P. Kharakoz, and L.M. Chailakhyan. 2008. Temperature shock and adaptation in fish. Doklady 422: 302–303.
Barnabé, G. 1990. Rearing bass and gilthead bream. In Aquaculture, ed. G. Barnabé, 647–686. New York: Ellis Horwood Books in Aquaculture and Fisheries Support.
Beitinger, T.L., and L.C. Fitzpatrick. 1979. Physiological and ecological correlates of preferred temperature in fish. American Zoologist 19: 319–329.
Beitinger, T.L., W.A. Bennett, and R.W. McCauley. 2000. Temperature tolerances of North American freshwater fishes exposed to dynamic changes in temperature. Environmental Biology of Fishes 58: 237–275.
Bird, R.P., and A.H. Draper. 1984. Comparative studies on different methods of malondyhaldehyde determination. Methods in Enzymology 90: 105–110.
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: 248–254.
Breau, C., R.A. Cunjak, and S.J. Peake. 2011. Behaviour during elevated water temperatures: can physiology explain movement of juvenile Atlantic salmon to cool water? Journal of Animal Ecology 80: 844–853.
Cabral, H., and M.J. Costa. 2001. Abundance, feeding ecology and growth of 0-group sea bass, Dicentrarchus labrax, within the nursery areas of the Tagus estuary. Journal of the Marine Biological Association of the United Kingdom 81: 679–682.
Carlberg, I., and B. Mannervik. 1985. Glutathione reductase. Methods in Enzymology 113: 484–490.
Clairborne, A. 1985. Catalase activity. In CRC handbook of methods in oxygen radical research, ed. R.A. Greenwald, 283–284. Boca Raton: CRC.
Claireaux, G., C. Couturier, and A.L. Groison. 2006. Effect of temperature on maximum swimming speed and cost of transport in juvenile European sea bass (Dicentrarchus labrax). The Journal of Experimental Biology 209: 3420–3428.
Diamantino, T.C., E. Almeida, A.M. Soares, and L. Guilhermino. 2001. Lactate dehydrogenase activity as an effect criterion in toxicity tests with Daphnia magna straus. Chemosphere 45: 553–560.
Durrieu de Madron, X., C. Guieu, R. Sempéré, P. Conan, D. Cossa, F. D’Ortenzio, C. Estournel, F. Gazeau, C. Rabouille, L. Stemmann, et al. 2011. Marine ecosystems’s responses to climatic and anthropogenic forcings in the Mediterranean. Progress in Oceanography 91: 97–166.
Ellis, G., and D.M. Goldberg. 1971. An improved manual and semi-automatic assay for NADP-dependent isocitrate dehydrogenase activity, with a description of some kinetic properties of human liver and serum enzyme. Clinical Biochemistry 4: 175–185.
Ellman, G.L., A. Burkhalter, and J. Ladou. 1961. A fluorometric method for the determination of hippuric acid. Journal of Laboratory and Clinical Medicine 57: 813–818.
European Commission. 2000. Directive 2000/60/EC of the European Parliament and of the Council of 23 October 2000, establishing a framework for community action in the field of water policy. Official Journal of the European Union L327: 1–72.
European Commission. 2008. Directive 2008/56/EC of the European Parliament and of the Council of 17 June 2008, establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive). Official Journal of the European Union L164: 19–40.
Flohe, L., and W.A. Gunzler. 1984. Assays of glutathione peroxidase. Methods in Enzymology 105: 114–121.
Flohe, L., and F. Otting. 1984. Superoxide dismutase assays. Methods in Enzymology 105: 93–104.
Fossi, M.C., S. Casini, I. Caliani, C. Panti, L. Marsili, A. Viarengo, R. Giangreco, G.N. di Sciara, F. Serena, A. Ouerghi, et al. 2012. The role of large marine vertebrates in the assessment of the quality of pelagic marine ecosystems. Marine Environmental Research 77: 156–158.
Frasco, M.F., and L. Guilhermino. 2002. Effects of dimethoate and beta-naphthoflavone on selected biomarkers of Poecilia reticulata. Fish Physiology and Biochemistry 26: 149–156.
Fry, F.E.J. 1971. The Effect of environmental factors on the physiology of fish. In Hoar, W.S, ed. D.J. Randall, 1–98. Academic: Fish physiology.
Godin, J.-G.J., 1997. Behavioural ecology of teleost fishes. Oxford University Press New York.
Golovanov, V. 2006. The ecological and evolutionary aspects of thermoregulation behavior on fish. Journal of Ichthyology 46: S180–S187.
Gravato, C., and L. Guilhermino. 2009. Effects of benzo(a)pyrene on seabass (Dicentrarchus labrax L.): biomarkers, growth and behavior. Human Ecol Risk Assess 15: 121–137.
Guilhermino, L., M.C. Lopes, A.P. Carvalho, and A. Soares. 1996. Inhibition of acetylcholinesterase activity as effect criterion in acute tests with juvenile Daphnia Magna. Chemosphere 32: 727–738.
Hussein, M.F., M.I. Mohamed, M.F. Selim, and M.A. El Din. 1983. Ambient temperature effects on brain and spinal cord acetylcholinesterase activity of two poikilotherms. Comparative Biochemistry and Physiology. C 75: 357–359.
IPCC, 2007. Climate Change 2007: Synthesis Report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. in: Core Writing Team, P., R.K and Reisinger, A. (Ed.). IPCC, Geneva, Switzerland, p. 104 pp.
Jo, S.H., M.K. Son, H.J. Koh, S.M. Lee, I.H. Song, Y.O. Kim, Y.S. Lee, K.S. Jeong, W.B. Kim, J.W. Park, et al. 2001. Control of mitochondrial redox balance and cellular defense against oxidative damage by mitochondrial NADP+ -dependent isocitrate dehydrogenase. The Journal of biological chemistry 276: 16168–16176.
Koumoundouros, G., D.G. Sfakianakis, P. Divanach, and M. Kentouri. 2002. Effect of temperature on swimming performance of sea bass juveniles. Journal of Fish Biology 60: 923–932.
Koumoundouros, G., C. Ashton, D.G. Sfakianakis, P. Divanach, M. Kentouri, N. Anthwal, and N.C. Stickland. 2009. Thermally induced phenotypic plasticity of swimming performance in European sea bass Dicentrarchus labrax juveniles. Journal of Fish Biology 74: 1309–1322.
Lee, S.M., H.J. Koh, D.C. Park, B.J. Song, T.L. Huh, and J.W. Park. 2002. Cytosolic NADP(+)-dependent isocitrate dehydrogenase status modulates oxidative damage to cells. Free Radical Biology and Medicine 32: 1185–1196.
Lima, I., S.M. Moreira, J.R. Osten, A.M. Soares, and L. Guilhermino. 2007. Biochemical responses of the marine mussel Mytilus galloprovincialis to petrochemical environmental contamination along the North-western coast of Portugal. Chemosphere 66: 1230–1242.
Limon-Pacheco, J., and M.E. Gonsebatt. 2009. The role of antioxidants and antioxidant-related enzymes in protective responses to environmentally induced oxidative stress. Mutation Research 674: 137–147.
Livingstone, D.R. 2001. Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Marine Pollution Bulletin 42: 656–666.
Lushchak, V.I., and T.V. Bagnyukova. 2006a. Temperature increase results in oxidative stress in goldfish tissues. 1. Indices of oxidative stress. Comparative Biochemistry and Physiology C Toxicol Pharmacol 143: 30–35.
Lushchak, V.I., and T.V. Bagnyukova. 2006b. Temperature increase results in oxidative stress in goldfish tissues. 2. Antioxidant and associated enzymes. Comparative Biochemistry and Physiology C Toxicol Pharmacol 143: 36–41.
Madeira, D., L. Narciso, H.N. Cabral, and C. Vinagre. 2012. Thermal tolerance and potential impacts of climate change on coastal and estuarine organisms. Journal of Sea Research 70: 32–41.
Magnuson, J.J., L.B. Crowder, and P.A. Medvick. 1979. Temperature as an ecological resource. American Zoologist 19: 331–343.
Melo, J.B., P. Agostinho, and C.R. Oliveira. 2003. Involvement of oxidative stress in the enhancement of acetylcholinesterase activity induced by amyloid beta-peptide. Neuroscience Research 45: 117–127.
Montgomery, J.C., and J.A. Macdonald. 1990. Effects of temperature on nervous system: implications for behavioral performance. The American Journal of Physiology 259: R191–R196.
Moyle, P.B., and J.J. Cech. 2003. Fishes: an introduction to ichthyology, 5th ed. Upper Saddle River: Prentice Hall.
Mukhopadhyay, S., and M.K. Poddar. 1990. Higher environmental temperature-induced change in synaptosomal acetylcholinesterase activity of brain regions. Neurochemical Research 15: 231–236.
Noyes, P.D., M.K. McElwee, H.D. Miller, B.W. Clark, L.A. Van Tiem, K.C. Walcott, K.N. Erwin, and E.D. Levin. 2009. The toxicology of climate change: environmental contaminants in a warming world. Environment International 35: 971–986.
Nunes, B., F. Carvalho, and L. Guilhermino. 2004. Acute and chronic effects of clofibrate and clofibric acid on the enzymes acetylcholinesterase, lactate dehydrogenase and catalase of the mosquitofish, Gambusia holbrooki. Chemosphere 57: 1581–1589.
Ohkawa, H., N. Ohishi, and K. Yagi. 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry 95: 351–358.
Pickett, G.D., and M.G. Pawson. 1994. Sea bass: biology, exploitation and conservation. Lowestoft, UK: Chapman & Hall.
Pitcher, T.J., and J.K. Parrish. 1993. Functions of shoaling behaviour in teleosts. In Behaviour of teleost fishes, ed. T.J. Pitcher, 363–439. London, UK: Chapman & Hall.
Portner, H.O. 2001. Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88: 137–146.
Pörtner, H., A.F. Bennett, F. Bozinovic, A. Clarke, M.A. Lardies, M. Lucassen, B. Pelster, F. Schiemer, and J. Stillman. 2006. Trade-offs in thermal adaptation: the need for a molecular to ecological integration. Physiological and Biochemical Zoology 79: 295–313.
Prosser, C.L., and D.O. Nelson. 1981. The role of nervous systems in temperature adaptation of poikilotherms. Annual Review of Physiology 43: 281–300.
Roche, H., and G. Bogé. 1996. Fish blood parameters as a potential tool for identification of stress caused by environmental factors and chemical intoxication. Marine Environmental Research 41: 27–43.
Sanchez, W., and J.M. Porcher. 2009. Fish biomarkers for environmental monitoring within the Water Framework Directive of the European Union. Trac-Trend Analytical Chemistry 28: 150–158.
Schiedek, D., B. Sundelin, J.W. Readman, and R.W. Macdonald. 2007. Interactions between climate change and contaminants. Marine Pollution Bulletin 54: 1845–1856.
Schmidt-Nielsen, K., 1997. Animal physiology: adaptation and environment, 5th ed. Cambridge University Press.
Szabo, T.M., T. Brookings, T. Preuss, and D.S. Faber. 2008. Effects of temperature acclimation on a central neural circuit and its behavioral output. Journal of Neurophysiology 100: 2997–3008.
Taylor, E.W., G. Egginton, S.E. Taylor, and P.J. Butler. 1997. Factors which may limit swimming performance at different temperatures. In Global warming: implications for freshwater and marine fish, ed. C.M. Wood and D.G. McDonald, 105–134. UK pp: Cambridge University Press, Cambridge.
Thain, J., A.D. Vethaak, and K. Hylland. 2008. Contaminants in marine ecosystems: develo** an integrated indicator framework using biological-effect techniques. ICES Journal of Marine Science 65: 1508–1541.
Tierney, K.B. 2011. Behavioural assessments of neurotoxic effects and neurodegeneration in zebrafish. Biochimica et Biophysica Acta (BBA)—Molecular Basis of Disease 1812: 381–389.
Torres, M.A., C.P. Testa, C. Gaspari, M.B. Masutti, C.M. Panitz, R. Curi-Pedrosa, E.A. de Almeida, P. Di Mascio, and D.W. Filho. 2002. Oxidative stress in the mussel Mytella guyanensis from polluted mangroves on Santa Catarina Island, Brazil. Marine Pollution Bulletin 44: 923–932.
van der Oost, R., J. Beyer, and N.P.E. Vermeulen. 2003. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environmental Toxicology and Pharmacology 13: 57–149.
Varò, I., J.C. Navarro, F. Amat, and L. Guilhermino. 2003. Effect of dichlorvos on cholinesterase activity of the European sea bass (Dicentrarchus labrax). Pestic Biochemistry Physics 75: 61–72.
Vassault, A. 1983. Lactate dehydrogenase. In Methods of enzymatic analysis Vol III, enzymes: oxireductases, transferases, ed. H.O. Bergmeyer, 118–126. New York: Academic.
Vinagre, C., T. Ferreira, L. Matos, M.J. Costa, and H.N. Cabral. 2009. Latitudinal gradients in growth and spawning of sea bass, Dicentrarchus labrax, and their relationship with temperature and photoperiod. Estuarine, Coastal and Shelf Science 81: 375–380.
Vinagre, C., D. Madeira, L. Narciso, H.N. Cabral, and M. Diniz. 2012a. 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.
Vinagre, C., D. Madeira, L. Narciso, H.N. Cabral, and M.S. Diniz. 2012b. Impact of climate change on coastal versus estuarine nursery areas: cellular and whole-animal indicators in juvenile seabass Dicentrarchus labrax. Mar Ecol-Prog Ser 464: 237–243.
Vinagre, C., L. Narciso, H.N. Cabral, M.J. Costa, and R. Rosa. 2012c. Coastal versus estuarine nursery grounds: effect of differential temperature and heat waves on juvenile seabass, Dicentrarchus labrax. Estuar Coast Shelf S 109: 133–137.
Zar, J.H. 1999. Biostatistical analysis, 4th ed. Upper Saddle River, New Jersey, USA: Prentice Hall, Inc.
Zhang, H.J., L. Xu, V.J. Drake, L. **e, L.W. Oberley, and K.C. Kregel. 2003. Heat-induced liver injury in old rats is associated with exaggerated oxidative stress and altered transcription factor activation. Faseb Journal 17: 2293–2295.
Acknowledgments
This study was done in the scope of the project ‘RAMOCS—Implementation of Risk Assessment Methodologies for Oil and Chemical Spills in the European Marine Environment’, funded by the Portuguese Foundation for the Science and Technology (FCT) and FEDER funds (ERA-AMPERA/0001/2007), in the framework of the EU ERA-NET AMPERA (ERAC-CT2005-016165, 6th EU Framework Program). This research was partially supported by the European Regional Development Fund (ERDF) through the COMPETE—Operational Competitiveness Programme and national funds through FCT—Foundation for Science and Technology, under the project ‘PEst-C/MAR/LA0015/2013’. Joana R. Almeida had a PhD grant from FCT (SFRH/BD/40843/2007) supported with European social funds and funds of Portuguese MCTES (POPH-QREN-Tipology 4.2).
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Almeida, J.R., Gravato, C. & Guilhermino, L. Effects of Temperature in Juvenile Seabass (Dicentrarchus labrax L.) Biomarker Responses and Behaviour: Implications for Environmental Monitoring. Estuaries and Coasts 38, 45–55 (2015). https://doi.org/10.1007/s12237-014-9792-7
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DOI: https://doi.org/10.1007/s12237-014-9792-7