Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-15T17:15:23.620Z Has data issue: false hasContentIssue false

Influence of oil exposure on the physiology and ecologyof the common sole Solea solea: Experimental and field approaches

Published online by Cambridge University Press:  15 October 2004

Guy Claireaux
Affiliation:
Centre de Recherche sur les Écosystèmes marins et aquacoles (CNRS-IFREMER), 17137 L'Houmeau, France
Yves Désaunay
Affiliation:
IFREMER, Laboratoire d'Écologie halieutique, rue de l'Ile d'Yeu, 44311 Nantes Cedex 03, France
Farida Akcha
Affiliation:
IFREMER, Laboratoire d'Écologie halieutique, rue de l'Ile d'Yeu, 44311 Nantes Cedex 03, France
Benoît Aupérin
Affiliation:
INRA, Station commune de recherches en ichtyophysiologie, Biodiversité et Environnement, Équipe physiologie de l'adaptation et du stress, Campus de Beaulieu, 35042 Rennes Cedex, France
Gilles Bocquené
Affiliation:
IFREMER, Laboratoire d'Écologie halieutique, rue de l'Ile d'Yeu, 44311 Nantes Cedex 03, France
Hélène Budzinski
Affiliation:
Laboratoire de physico-toxicochimie des systèmes naturels, Université de Bordeaux, 351 cours de la Libération, 33405 Talence Cedex, France
Jean-Pierre Cravedi
Affiliation:
INRA, Laboratoire des xénobiotiques, UMR 1089, Toulouse, France
Fariba Davoodi
Affiliation:
Centre de Recherche sur les Écosystèmes marins et aquacoles (CNRS-IFREMER), 17137 L'Houmeau, France
Robert Galois
Affiliation:
Centre de Recherche sur les Écosystèmes marins et aquacoles (CNRS-IFREMER), 17137 L'Houmeau, France
Camille Gilliers
Affiliation:
IFREMER, Laboratoire d'Écologie halieutique, rue de l'Ile d'Yeu, 44311 Nantes Cedex 03, France
Christelle Goanvec
Affiliation:
Laboratoire de biologie et de physiologie cellulaire, Université de Bretagne Occidentale, UFR Sciences et Techniques, 6 avenue Le Gorgeu, BP 809, 29285 Brest Cedex, France
Daniel Guérault
Affiliation:
IFREMER, Laboratoire d'Écologie halieutique, rue de l'Ile d'Yeu, 44311 Nantes Cedex 03, France
Nathalie Imbert
Affiliation:
Université de La Rochelle, Laboratoire de biologie et environnement marins, avenue M. Crépeau, La Rochelle, 17042 Cedex 1, France
Olivier Mazéas
Affiliation:
Laboratoire de physico-toxicochimie des systèmes naturels, Université de Bordeaux, 351 cours de la Libération, 33405 Talence Cedex, France
Guy Nonnotte
Affiliation:
Laboratoire de biologie et de physiologie cellulaire, Université de Bretagne Occidentale, UFR Sciences et Techniques, 6 avenue Le Gorgeu, BP 809, 29285 Brest Cedex, France
Liliane Nonnotte
Affiliation:
Laboratoire de biologie et de physiologie cellulaire, Université de Bretagne Occidentale, UFR Sciences et Techniques, 6 avenue Le Gorgeu, BP 809, 29285 Brest Cedex, France
Patrick Prunet
Affiliation:
INRA, Station commune de recherches en ichtyophysiologie, Biodiversité et Environnement, Équipe physiologie de l'adaptation et du stress, Campus de Beaulieu, 35042 Rennes Cedex, France
Philippe Sébert
Affiliation:
Université de Bretagne Occidentale, Laboratoire de physiologie, Unité haute pression et métabolisme EA 3879, UFR Médecine, CS 93837, Brest 29238 Cedex 03, France
Aurélie Vettier
Affiliation:
Université de Bretagne Occidentale, Laboratoire de physiologie, Unité haute pression et métabolisme EA 3879, UFR Médecine, CS 93837, Brest 29238 Cedex 03, France
Get access

Abstract

Evaluating the ecological impact of an oil spill is a complex issue requiring coherently articulated examination of the sequence of interactions that link the cell, where contaminants exert their effects, to the ecosystem, where interactions with human activities arise. This sequence of interactions traverses the frontiers between scientific disciplines (chemistry, toxicology, physiology, and fisheries ecology). Using the common sole (Solea solea L.) as a model species for the coastal habitats polluted by the “Erika” oil spill, our research project attempted to define indices of functional integrity that characterised the consequences of fuel exposure at the different biological levels. The coupling of field observations with experimental laboratory work revealed how functional alterations which are readily observable within individuals and their organs are progressively obscured as investigation progresses towards more complex organisational levels. Some of the approaches and indices are proposed as instruments for evaluating the impact of contamination by hydrocarbons.

Type
Research Article
Copyright
© EDP Sciences, IFREMER, IRD, 2004

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Akcha, F., Vincent-Hubert, F., Pfhol-Leszkowicz, A., 2003, Potential value of the comet assay and DNA adduct measurement in dab (Limanda limanda) for assessment of in situ exposure to genotoxic compounds. Mutat. Res. Genet. Toxicol. Environ. Mutagen. 534, 21-32. CrossRef
Amara, R., Lagardère, F., Désaunay, Y., 1993, Seasonal distribution and duration of the planktonic stage of Dover sole, Solea solea, larvae in the Bay of Biscay: an hypothesis. J. Fish Biol. 43, 17-30. CrossRef
Amara, R., Lagardère, F., Désaunay, Y., Marchand, J., 2000, Metamorphosis and estuarine colonisation in the common sole, Solea solea (L.): implications for recruitment regulation. Oceanol. Acta 23, 469-484. CrossRef
Anonymous, 2003, Report of the Working Group on the Assessment of Southern Shelf Demersal Stocks. ICES CM 2003/ACFM 03.
Barillé-Boyer, A.L., Gruet, Y., Barillé, L., Harin, N., 2004, Temporal changes in community structure of tide pools following the “Erika” oil spill. Aquat. Living Resour. 17, 323. CrossRef
Baumard, P., Budzinski, H., 1997, Internal standard quantification method and gas chromatography-mass spectrometry (GC/MS): a reliable tool for PAH quantification in natural matrices. Analusis 25, 246-252.
Berdugo, V. Harris, R.P. O'Hara S.C., 1977, The effect of petroleum hydrocarbons on reproduction of an estuarine planktonic copepod in laboratory cultures. Mar. Pollut. Bull. 8, 138-143. CrossRef
Bretagnolle, V., Certain, G., Houte, S., Métais, M., 2004, Distribution maps and minimum abundance estimates for wintering auks in the Bay of Biscay, based on aerial surveys. Aquat. Living Resour. 17, 353. CrossRef
Budzinski, H., Mazéas, O., Tronczynsky, J., Désaunay, Y., Bocquené, G., Claireaux, G., 2004, Link between exposure of fish (Solea solea) to PAHs and metabolites: application to the “Erika” oil spill. Aquat. Living Resour. 17, 329. CrossRef
Budzinski H., Papineau A., Baumard P., Garrigues P., 1995, Extraction assistée par chauffage microondes focalisées (MOF) à pression ambiante des composés organiques dans les matrices naturelles : application à l'analyse des composés aromatiques. C. R. Acad. Sci. Paris 321, sér. IIb, 69-76.
Budzinski, H., Letellier, M., Garrigues, P., Le Menach, K., 1999, Optimisation of teh microwave-assisted extraction in open cell of PAHs from soils and sediments – Study of moisture effect. J. Chromatogr. A. 837, 187-200. CrossRef
Burgeot, T., Bocquené, G., Pingray, G., Godefroy, D., Legrand, J., Dimeet, J., Marco, F., Vincent, F., Henocque, Y., Oger Jeanneret, H., Galgani, F., 1994, Monitoring biological effects of contamination in marine fish along French coasts by measurement of ethoxyresorufin-O-deethylase activity. Ecotoxicol. Environ. Saf. 29, 131-147. CrossRef
Byrne, C.J., Calder, J.A., 1977, Effect of the water-soluble fractions of crude, refined and waste oils on the embryonic and larval stages of the quahog clam Mercenaria sp. Mar. Biol. 40, 225-231 CrossRef
Cann-Moisan, C., Caroff, J., Sebert, P., Barthelemy, L., 1989, Determination of nucleotide concentrations with high performance liquid chromatography (HPLC): application to fish. Aquaculture 76, 135-143. CrossRef
Capuzzo, J.M., 1980, Biological effect of petroleum hydrocarbons on marine organisms: integration of experimental results and predictions of impacts. Mar. Environ. Res. 17, 272-276. CrossRef
Claireaux, G., Lagardère, J.-P., 1999, Influence of temperature, oxygen and salinity on the metabolism of European sea bass. J. Sea Res. 42, 157-168. CrossRef
Claireaux, G., Webber, D.M., Lagardère, J.-P., Kerr, S.R., 2000, Influence of water temperature and oxygenation on the aerobic metabolic scope of Atlantic cod (Gadus morhua). J. Sea Res. 44, 257-265. CrossRef
Chantereau S., Chiffoleau J.-F., Dufour A., Jeanneret H., 2002, Utilisation des données du RNO dans le cadre du naufrage de l'Erika. In: Travaux du RNO 2002. Surveillance du milieu marin. Ifremer & Ministère de l'Écologie et du Développement Durable, pp. 25-43.
Connolly, J.P., 1991, Application of a food chain model to polychlorinated biphenyl contamination of the lobster and winter flounder food chains in New Bedford harbor. Environ. Sci. Technol. 25, 760-770. CrossRef
Cravedi, J.P., 2001, Métabolisme et bioaccumulation des xénobiotiques chez le poisson. C.R. Acad. Agric. Fr. 87, 199-208.
Daan, N., Richardson, K., Pope, J.G., 1996, Changes in the North Sea ecosystem and their causes: Aarhus 1975 revisited. ICES J. Mar. Sci. 53, 87-883.
Dale, V.H., Beyeler, S.C., 2001, Challenges in development and use of ecological indicators. Ecol. Indic. 1, 3-10. CrossRef
Désaunay, Y., Pérodou, J.B., Beillois, P., 1981, Etude des nurseries de poissons du littoral de la Loire Atlantique. Science et Pêche, Bull. Inst. Scient. Techn. Pêches Marit. 319, 1-23.
Désaunay Y., Guérault D., 2002, Manuel des protocoles de campagne halieutique, campagnes Nourriceries Gascogne. IFREMER, Système d'Informations halieutiques, DRV/RH/DT/2002-005, 31.
Dorel, D., Koutsikopoulos, C., Désaunay, Y., Marchand, J., 1991, Seasonal distribution of young sole Solea solea (L.) in the nursery ground of the Bay of Vilaine (northern Bay of Biscay). Neth. J. Sea Res. 27, 297-306. CrossRef
Fletcher, G.L., Kiceniuk, J.W., Williams, U.P., 1981, Effects of oiled sediments on mortality, feeding and growth of winter flounders Pseudopleuronectes americanus. Mar. Ecol. Prog. Ser. 4, 91-96. CrossRef
Frid, C., Rogers, S., Nicholson, M., Ellis, J., Freeman, S., 2000, Using biological characteristics to develop new indices of ecosystem health. Mini-symposium on Defining the role of ICES in supporting biodiversity conservation. ICES CM 2000/Mini: 02, 23 p.
Galgani, F., Payne, J.F., 1991, Biological effects of contaminants: microplate method for measurement of EROD activity in fish. ICES Techniques in Marine Environmental Sciences 13, 12.
Galois, R., Lagardère, F., Richard, P., 1990, Changes in biochemical composition and otolith microstructure of larval common solea, Solea solea (L.). La Mer 28, 273-285.
Gamperl, A.K., Farrell, A.P., 2004, Cardiac plasticity in fishes: environmental influences and intraspecific differences. J. Exp. Biol. 207, 2539-2550. CrossRef
Gamperl, A.K., Vijayan, M.M., Boutilier, R.G., 1994, Experimental control of stress hormone levels in fishes: techniques and application. Rev. Fish Biol. Fish. 4, 215-255. CrossRef
Goksoyr, A., Beyer, J., Husoy, A.M., Larsen, H.E., Westrheim, K., Wilhelmsen, S., Klungsoyr, J., 1994, Accumulation and effects of aromatic and chlorinated hydrocarbons in juvenile Atlantic cod (Gadus morhua) cages in a polluted fjord (Sorfjorden, Norway). Aquat. Toxicol. 29, 21-35. CrossRef
Hilborn R., 1996, Detecting population impacts from oil spills: a comparison of methodologies. Am. Fish. Soc. Symp.18, 639-644.
Hontela, A., Dumont, P., Duclos, D., Fortin, R., 1995, Endocrine and metabolic dysfunction in yellow perch, Perca flavescens, exposed to organic contaminants and heavy metals in the St Lawrence river. Environ. Toxicol. Chem. 14, 725-731. CrossRef
Hose, J.E., McGurk, M.D., Marty, G.D., Hinton, D.E., Brown, E.D., Baker, T.T., 1996, Sublethal effects of the “Exxon Valdez” oil spill on herring embryos and larvae: morphological, cytogenetic and histopathological assessements, 1989-1991. Can. J. Fish. Aquat. Sci. 53, 2355-2365.
Karakiri, M., Berghahn, R., Von Westernhagen, H., 1989, Growth differences in 0-group plaice Pleuronectes platessa as revealed by otolith microstructure analysis. Mar. Ecol. Prog. Ser. 55, 15-22. CrossRef
Kiceniuk, J.W., Khan, R.A., 1987, Effect of petroleum hydrocarbons on Atlantic cod, Gadus morhua, following chronic exposure. Can. J. Zool. 65, 490-494. CrossRef
Kirby, M.F., Neall, P., Taylor, T., 1999, EROD activity measured in flatfish from the area of the Sea Empress oil spill. Chemosphere 38, 2929-2949. CrossRef
Kocan, R.M., Marty, G.D., Okihiro, M.S., Brown, E.D., Baker, T.T., 1996, Reproductive success and histopathology of individual Prince William Sound Pacific herring 3 years after the “Exxon Valdez” oil spill. Can. J. Fish. Aquat. Sci. 53, 2388-2393.
Köhler, A., Hölzel, F., 1980, Investigation on health conditions of flounder and smelt in the Elbe estuary. Helgol. Meers. 33, 401-414. CrossRef
Koutsikopoulos, C., Désaunay, Y., Dorel, D., Marchand, J., 1989, The role of coastal areas in the life history of sole (Solea solea L.) in the Bay of Biscay. In: Ros J.D. (Ed.), Topics in Marine Biology. Scient. Mar. 53, 567-575.
Koutsikopoulos, C., Lacroix, N., 1992, Distribution and abundance of sole (Solea solea L.) eggs and larvae in the Bay of Biscay between 1986 and 1989. Neth. J. Sea Res. 29, 81-91. CrossRef
Koutsikopoulos C., Dorel D., Désaunay Y., Le Cann B., Forest A., 1995, Interactions entre processus physiques et comportement individuel : conséquences sur l'organisation et le fonctionnement du stock de sole (Solea solea L.) du golfe de Gascogne. ORSTOM (Ed.) Colloques et Séminaires, 1er Forum Halieumétrique, pp. 49-74.
Lancaster, J.E., Pawson, M.G., Pickett, G.D., Jennings, S., 1998, The impact of the Sea Empress oil spill on seabass recruitment. Mar. Pollut. Bull. 36, 677-688. CrossRef
Léauté J.P., Caill-Milly N., 2003, Les petites pêches côtières et estuariennes françaises du sud du golfe de Gascogne. Extrait du rapport final du contrat PECOSUDE EC/DG Fish (DG XIV) No. 99/024, Ifremer, DRV/RH/DT/03-01.
Lee, W.Y., Winters, K., Nicol, J.A.C., 1978, The biological effects of the water-soluble fractions of a No. 2 fuel oil on the planktonic shrimp, Lucifer faxoni. Environ. Pollut. 153, 167-183. CrossRef
Lefrançois, C., Claireaux, G., 2003, Influence of ambient oxygenation and temperature on metabolic scope and scope for heart rate in the common sole (Solea solea). Mar. Ecol. Prog. Ser. 259, 273-284. CrossRef
Le Pape, O., Désaunay, Y., Guérault, D., 2003a, Relationship between fluvial discharge and sole (Solea solea L.) recruitment in the Bay of Biscay (France). ICES Mar. Sci. Symp. 219, 241-248.
Le Pape, O., Chauvet, F., Désaunay, Y., Guérault, D., 2003b, Relationship between interannual variations of the river plume and the extent of nursery grounds for the common sole (Solea solea L.) in Vilaine Bay. Effects on recruitment variability. J. Sea Res. 50, 177-185. CrossRef
Le Pape, O., Chauvet, F., Mahévas, S., Lazure, P., Guérault, D., Désaunay, Y., 2003c, Quantitative description of habitat suitability for the juveniles common sole (Solea solea L.) in the Bay of Biscay (France) and the contribution of different habitats to the adult population. J. Sea Res. 50, 139-149. CrossRef
Le Pape, O., Holley, J.-F., Guérault, D., Désaunay, Y., 2003d, Quality of coastal and estuarine essential fish habitats: Estimations based on the size of juvenile common sole (Solea solea L.). Estuar. Coast. Shelf Sci. 58, 793-803. CrossRef
Linden, O., 1978, Biological effects of oil on early development of the Baltic herring Clupea harengus membras. Mar. Biol. 45, 273-283. CrossRef
Mallatt J., 1985. Fish structural changes induced by toxicants and other irritants: a statistical review. Can. J. Fish. Aquat. Sci. 42, 630-648.
Martoja, R., Martoja-Pierson, M., 1967, Initiation aux techniques de l'histologie animale. Masson Paris, France.
Marty, G.D., Short, J.W., Dambach, D.M., Willits, N.H., Heintz, R.A., Rice, S.D., Stegeman, J.J., Hinton, D.E., 1996, Ascites, premature emergence, increased gonadal cell apoptosis and cytochrome P4501A induction in pink salmon larvae continuously exposed to oil-contaminated gravel during development. Can. J. Zool. 75, 989-1007. CrossRef
Mazéas, L., Budzinski, H., 2001, Improved accuracy of GC-MS quantification of aliphatic and aromatic hydrocarbons in marine sediments and petroleums. Validation on reference matrices and application to the Erika oil spill. Intern. J. Environ. Anal. Chem. 82, 157-173. CrossRef
Mercier, C., Axelsson, M., Imbert, N. Claireaux, G., Lefrançois, C., Altimiras, J., Farrell, A.P., 2002, In vitro cardiac performance in triploid brown trout (Salmo trutta) at two acclimation temperatures. J. Fish Biol. 60, 117-137. CrossRef
Moles, A., Rice, S., Norcross, B.L., 1994, Non-avoidance of hydrocarbon laden sediments by juvenile flatfishes. Neth. J. Sea Res. 32, 361-367. CrossRef
Moles, A., Norcross, B.L., 1998, Effects of oil-laden sediments on growth and health of juvenile flatfishes. Can. J. Fish. Aquat. Sci. 55, 605-610. CrossRef
Monod, G., Saucier, D., Perdu-Durand, E., Diallo, M., Cravedi, J.P., Astic, L., 1994, Biotransformation enzyme activities in the olfactory organ of rainbow trout (Oncorhynchus mykiss). Immunocytochemical localization of cytochrome P4501 A1 and its induction by ß-naphthoflavone. Fish Physiol. Biochem. 13, 433-444.
Moore, M.J., Stegeman, J.J., 1994, Hepatic neoplasm in winter flounder Pleuronectes americanus from Boston harbor, Massachusett, USA. Dis. Aquat. Org. 20, 33-48. CrossRef
Peterson, C.H., 2001, The “Exxon Valdez” oil spill in Alaska: Acute, indirect and chronic effects on the ecosystem. Adv. Mar. Biol. 39, 1-103. CrossRef
Peterson, C.H., Rice, S.D., Short, J.W., Esler, D., Bodkin, J.L., Ballachey, B.E., Irons, D.B., 2003, Long-term ecosystem response to the “Exxon Valdez” oil spill. Science 302, 2082-2086. CrossRef
Priede, I.G., 1977, Natural selection for energetic efficiency and relationship between activity level and mortality. Nature 267, 610-612. CrossRef
Priede I.G., 1985, Metabolic scope in fish. In: Tyler P., Calow P. (Eds.), Fish energetics: new perspectives. Croom Helm, London, pp. 33-64.
Reid, SG., Bernier, NJ., Perry, SF., 1998, the adrenergic stress response in fish: control of catecholamine storage and release. Comp. Biochem. Physiol. C 120, 1-27
Shiels, H.S., Stevens, E.D., Farrell, A.P., 1998, Effect of temperature, adrenaline and ryanodine on power production in rainbow trout Oncorhynchus mykiss ventricular trabeculae. J. Exp. Biol. 201, 27102710.
Sogard, S., Able, K.W., 1992, Growth variation of newly settled winter flounder (Pseudopleurectes americanus) in New Jersey estuaries as determined by otolith microstructure. Neth. J. Sea Res. 29, 163-172. CrossRef
Soimasuo, R., Jokinen, I., Kukkonen, J., Petanen, T., Ristola, T., Oikari, A., 1995, Biomarker responses along a pollution gradient: effects of pulp and paper mill effluents on caged whitefish. Aquat. Toxicol. 31, 329-345. CrossRef
Solangi, M.A., Overstreet, R.M., 1982, Histopathological changes in two estuarine fishes, Menidia beryllina (Cope) and Trinectes maculatus (Bloch and Schneider) exposed to crude oil and its water-soluble fractions. J. Fish Dis. 5, 13-35. CrossRef
Stehr, C.M., Myers, M.S., Johnson, L.L., Spencer, S., Stein, J.E., 2003, Toxicopathic liver lesions in English sole and chemical contaminant exposure in Vancouver Harbour, Canada. Mar. Environ. Res. 57, 55.74. CrossRef
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. CrossRef
Tronczynski, J., Munschy, C., Moisan, K., Guiot, N., Truquet, I., Olivier, N., Men, S., Furaut, A., 2004, Contamination of the Bay of Biscay by polycyclic aromatic hydrocarbons (PAHs) following the T/V “Erika” oil spill. Aquat. Living Resour. 17, 243. CrossRef
Truscott, B., Idler, D.R., Fletcher, G.L., 1992, Alteration of reproductive steroids of male winter flounder (Pleuronectes americanus) chronically exposed to low levels of crude oil in sediments. Can. J. Fish. Aquat. Sci. 49, 2190-2195. CrossRef
Van Den Thillart, G., Dalla Via, J., Vitali, G., Cortesi, P., 1994, Influence of long-term hypoxia exposure on the energy metabolism of Solea solea. I. Critical O2 levels for aerobic and anaerobic metabolism. Mar. Ecol. Prog. Ser. 104, 109-117. CrossRef
Vethaak, A.D., Jol, J.G., Meijboom, A., Eggens, M.L., 1996, Skin and liver diseases in flounder (Platichthys flesus) after long-term exposure to contaminated sediments in large scale mesocosms. Environ. Health Perspect. 104, 1218-1229. CrossRef
Vethaak, A.D., Wester, P.W., 1996, Diseases in flounder Platichthys flesus in Dutch coastal and estuarine waters, with particular reference to environmental stress factors. II. Liver histopathology. Dis. Aquat. Org. 26, 99-116. CrossRef
Vettier, A., Sébert, P., 2004, Pressure resistance of aerobic metabolism in eels from different water environments. Mitochondrion 3, 347-354. CrossRef
Whitfield A.K., Elliott M., 2002, Fishes as indicators of environmental and ecological changes within estuaries: A review progress and some suggestions for the future. J. Fish Biol. 61 (suppl. A), 229-250.