Effect of copper exposure on growth, condition indices and biomarker response in juvenile sole <i>Solea senegalensis</i>

Vanessa Fonseca; Ângela Serafim; Rui Company; Maria João Bebianno; Henrique Cabral

doi:10.3989/scimar.2009.73n1051

Authors

Vanessa Fonseca Instituto de Oceanografia, Faculdade de Ciências, Universidade de Lisboa
Ângela Serafim CIMA, Faculdade de Ciências do Mar e do Ambiente, Universidade do Algarve
Rui Company CIMA, Faculdade de Ciências do Mar e do Ambiente, Universidade do Algarve
Maria João Bebianno CIMA, Faculdade de Ciências do Mar e do Ambiente, Universidade do Algarve
Henrique Cabral Instituto de Oceanografia, Faculdade de Ciências, Universidade de Lisboa

DOI:

https://doi.org/10.3989/scimar.2009.73n1051

Keywords:

fish growth, fish condition, metallothioneins, lipid peroxidation, juvenile sole, biomarkers

Abstract

Juvenile Solea senegalensis were exposed to different concentrations of waterborne copper (Cu) for 15 days in static conditions with continuous aerated artificial salt water at 20°C (± 0.8°C) with a normal photoperiod (10 h/14 h light/dark) and daily feeding. Several measures of exposure and effects were determined: 1) biomarkers - metallothioneins and lipid peroxidation level; 2) mass indices - growth rate and morphometric condition indices; and 3) biochemical condition indices - RNA:DNA ratio and lipid and protein content in fish tissues. Copper exposure triggered the response of the biomarkers and resulted in reduced growth and condition (RNA:DNA and lipid content), but the morphometric indices did not vary. The physiological costs of Cu contamination on condition suggested that lipid reserves were allocated as an energy source to enable exposed fish to respond to Cu toxicity as well as to maintain positive growth rates and protein synthesis throughout the experiment, although with lower growth rates than the control fish. This study showed the importance of selecting suitable biomarkers according to contaminant source, fish species and their life-history stage. In addition, the use of several biomarkers of exposure, growth and specific condition indices can improve fish health determination and should be considered in evaluations of the effects of environmental contaminants on fish.

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Author Biography

Henrique Cabral, Instituto de Oceanografia, Faculdade de Ciências, Universidade de Lisboa

Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa

References

Adams, S.M. – 2002. Biological Indicators of Aquatic Ecosystem Stress: Introduction and Overview. In: S.M. Adams (eds.), Biological indicators of aquatic ecosystem stress, American Fisheries Society, pp. 1-11. Bethesda, Maryland.

Adams, S.M. – 2005. Assessing cause and effect of multiple stressors on marine systems. Mar. Pollut. Bull., 51: 649-657. doi:10.1016/j.marpolbul.2004.11.040

Bebianno, M.J. and W.J. Langston. – 1989. Quantification of metallothioneins in marine invertebrates using differential pulse polarography. Port. Electrochimica Acta, 7: 511-524.

Beyers, D.W., A.J. Rice, W.H. Clements and C.J. Henry. – 1999. Estimating physiological cost of chemical exposure: Integrating energetics and stress to quantify toxic effects in fish. Can. J. Fish. Aquat. Sci., 56: 814-822. doi:10.1139/cjfas-56-5-814

Blanchard, J. and M. Grosell. – 2006. Copper toxicity across salinities from freshwater to seawater in the euryhaline fish Fundulus heteroclitus: Is copper an ionoregulatory toxicant in high salinities? Aquat. Toxicol., 80: 131-139. doi:10.1016/j.aquatox.2006.08.001

Broeg, K. and K.K. Lehtonen. – 2006. Indices for the assessment of environmental pollution of the Baltic Sea coasts: Integrated assessment of a multi-biomarker approach. Mar. Pollut. Bull., 53: 508-522. doi:10.1016/j.marpolbul.2006.02.004

Buckley, L.J., E. Caldarone, and T.L. Ong. – 1999. RNA-DNA ratio and other nucleic acid-based indicators for growth and condition of marine fishes. Hydrobiologia, 401: 265-277. doi:10.1023/A:1003798613241

Bullow, F.J. – 1970. RNA-DNA ratios as indicators of recent growth rates of a fish. J. Fish. Res. Board Can., 27: 2343-2349.

Caldarone, E.M., M. Wagner, J. St Onge-Burns and L.J. Buckley. – 2001. Protocol and guide for estimating nucleic acids in larval fish using a fluorescence microplate reader. Northeast Fish. Sci. Cent. Ref. Doc. (01-11), pp.1-22.

Daskalakis, K.D. and T.P. O’Connor. – 1995. Distribution of chemical concentrations in US coastal and estuarine sediment. Mar. Environ. Res., 40: 381-398. doi:10.1016/0141-1136(94)00150-N

De Boeck, G., A. Vlaeminck and R. Blust. – 1997. Effects of sublethal copper exposure on copper accumulation, food consumption, growth, energy storages and nucleic acid content in common carp. Arch. Environ. Contam. Toxicol., 33: 415-422. doi:10.1007/s002449900271

Den Besten, P.J. – 1998. Concepts for the implementation of biomarkers in environmental monitoring. Mar. Environ. Res., 46: 253-256. doi:10.1016/S0141-1136(97)00049-4

Eastwood, S. and P. Couture. – 2002. Seasonal variation in condition and liver metal concentrations of yellow perch (Perca flavescens) from metal-contaminated environment. Aquat. Toxicol., 58: 43-56. doi:10.1016/S0166-445X(01)00218-1

Erdelmeier, I., D. Gerard-Monnier, J.C. Yadan and J. Acudiere. – 1998. Reactions of N-methyl-2-phenylindole with malondialdehyde and 4-hydroxyalkenals. Mechanistic aspects of the colorimetric assay of lipid peroxidation. Chem. Res. Toxicol., 11: 1184-1194. doi:10.1021/tx970180z

Ferron, A. and W.C. Leggett. – 1994. An appraisal of condition measures for marine fish larvae. Adv. Mar. Biol., 30: 217-303. doi:10.1016/S0065-2881(08)60064-4

Fonseca, V.F., C. Vinagre and H.N. Cabral. – 2006. Growth variability of juvenile soles Solea solea and Solea senegalensis, and comparison with RNA:DNA ratios in the Tagus estuary, Portugal. J. Fish Biol., 68: 1551-1562. doi:10.1111/j.0022-1112.2006.001042.x

Hall, L.W. and R.D. Anderson. – 1999. A deterministic risk assessment for copper in European saltwater environments. Mar. Pollut. Bull., 38(3): 207-208. doi:10.1016/S0025-326X(98)00164-7

Humphrey, C.A., S.C. King and D.W. Klumpp. – 2007. A multibiomarker approach in barramundi (Lates calcarifer) to measure exposure to contaminants in estuaries of tropical North Queensland. Mar. Pollut. Bull., 54: 1569-1581. doi:10.1016/j.marpolbul.2007.06.004

Knight, J.A., S. Anderson and J.M. Rawle. – 1972. Chemical basis of the sulfo-phospho-vanillin reaction for estimating total serum lipids. Clin. Chem., 18: 199-202.

Levesque, H.M., T.W. Moon, P.G.C. Campbell, and A. Hontela. – 2002. Seasonal variation in carbohydrate and lipid metabolism of yellow perch (Perca flavescens) chronically exposed to metals in the field. Aquat. Toxicol., 60: 257-267. doi:10.1016/S0166-445X(02)00012-7

Lloret, J. and S. Planes. – 2003. Condition, feeding and reproductive potential of white seabream Diplodus sargus as indicators of habitat quality and the effect of reserve protection in the Northwestern Mediterranean. Mar. Ecol. Prog. Ser., 248: 197-208. doi:10.3354/meps248197

Lowry, O.H., N.J. Rosebrough, A.L. Farr and R.J. Randal. – 1951. Protein measurement with folinphenol reagent. J. Biol. Chem., 193: 265-275.

Lundebye, A.K., M.H.G. Berntssen, S.E.W. Bonga and A. Maage. – 1999. Biochemical and physiological responses in Atlantic salmon (Salmo salar) following dietary exposure to copper and cadmium. Mar. Pollut. Bull., 39: 137-144. doi:10.1016/S0025-326X(98)00208-2

Marchand, J., A. Tanguy, J. Laroche, L. Quiniou and D. Moraga. – 2003. Responses of European flounder Platichthys flesus populations to contamination in different estuaries along the Atlantic coast of France. Mar. Ecol. Prog. Ser., 260: 273-284. doi:10.3354/meps260273

Marchand, J., L. Quiniou, R. Riso, M.T. Thebaut and J. Laroche. – 2004. Physiological cost of tolerance to toxicants in the European flounder Platichthys flesus, along the French Atlantic Coast. Aquat. Toxicol., 70: 327-343. doi:10.1016/j.aquatox.2004.10.001

Marr, J.C.A., J. Lipton, D. Cacela, J.A. Hansen, H.L. Bergman, J.S. Meyer and C. Hogtrand. – 1996. Relationship between copper exposure duration, tissue copper concentration, and rainbow trout growth. Aquat. Toxicol., 36: 17-30. doi:10.1016/S0166-445X(96)00801-6

Nye, J.A., D.D. Davis and T.J. Miller. – 2007. The effect of maternal exposure to contaminated sediment on the growth and condition of larval Fundulus heteroclitus. Aquat. Toxicol., 82: 242-250. doi:10.1016/j.aquatox.2007.02.011

Riba, I., M.C. Casado-Martínez, J. Blasco and T.A. DelValls. – 2004. Bioavailability of heavy metals bound to sediments affected by a mining spill using Solea senegalensis and Scrobicularia plana. Mar. Environ. Res., 58: 395-399. doi:10.1016/j.marenvres.2004.03.085

Ricker, W.E. – 1975. Computation and interpretation of biological statistics of fish populations. Bull. Fish. Res. Board Can., 191: 1-382.

Roesijadi, G. – 1996. Metallothionein and its role in toxic metal regulation. Comp. Biochem. Physiol. C, 113: 117-123.

Rowe, C.L. – 2003. Growth responses of an estuarine fish exposed to mixed trace elements in sediments over a full life cycle. Ecotoxicol. Environ. Safety, 54: 229-239. doi:10.1016/S0147-6513(02)00055-6

Rueda-Jasso, R., L.E.C. Conceição, J. Dias, W. De Coen, E. Gomes, J.F. Rees, F. Soares, M.T. Dinis and P. Sorgeloos. – 2004. Effect of dietary non-protein energy levels on condition and oxidative status of Senegalese sole (Solea senegalensis) juveniles. Aquaculture, 231: 417-433. doi:10.1016/S0044-8486(03)00537-4

Sanchez, W., O. Palluel, L. Meunier, M. Coquery, J.M. Porcher and S. Aït-Aïssa. – 2005. Copper-induced oxidative stress in three-spined stickleback: relationship with hepatic metal levels. Environ. Toxicol. Pharmacol., 19: 177-183. doi:10.1016/j.etap.2004.07.003

Seim, W.K., L.R. Curtis, S.W. Gleen and G.A. Chapman. – 1984. Growth and survival of developing steelhead trout (Salmo gairdneri) continuously or intermittently exposed to copper. Can. J. Fish. Aquat. Sci., 41: 433-438. doi:10.1139/f84-051

Shugart, L.R., J.F. McCarthy and S.H. Halbrook. – 1992. Biological markers of environmental and ecological contamination: an overview. Risk Anal., 12: 353-360. doi:10.1111/j.1539-6924.1992.tb00687.x

Suthers, I.M. – 1998. Bigger? Fatter? Or is faster growth better? Considerations on condition in larval and juvenile coral-reef fish. Aust. J. Ecol., 23: 265-273. doi:10.1111/j.1442-9993.1998.tb00730.x

Van der Oost, R., J. Beber and N.P.E. Vermeulen. – 2003. Fish bioaccumulation and biomarkers in environmental risks assessment: a review. Environ. Toxicol. Pharmacol., 13: 57-149. doi:10.1016/S1382-6689(02)00126-6

Wu, R.S.S., C.A. Pollino, D.W.T. Au, G.J. Zheng, B.H. Yuen and P.K.S. Lam. – 2003. Evaluation of biomarkers of exposure and effect in juvenile aerolated grouper (Epinephelus aerolatus) on foodborne exposure to Benzo[a]pyrene. Environ. Toxicol. Chem., 22: 1568-1573. doi:10.1897/1551-5028(2003)22<1568:EOBOEA>2.0.CO;2