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Responses of juvenile European flounder (Platichthys flesus) to multistress in the Vilaine estuary, during a 6-month survey

  • Ecotoxicology of estuaries in France and Québec, Canada
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Abstract

Physiological and genetic responses of age 0+ Platichthys flesus were investigated in the eutrophicated and moderately contaminated Vilaine estuary, during a 6-month survey. The main objective of this study was to explore the biological responses of fishes during their juvenile period in an estuarine system in order to detect a possible selective pressure induced by the environmental stress. Our results showed a general convergence in physiological responses along the survey: an increase in genotoxicity was associated with an increase in mRNA expression of ATPase and betaine homocysteine methyltransferase. These results could suggest an increase of cellular damage, energetic request, and detoxification rate related to the growing exposure time to stress. Considering the aging of the cohort, the genetic characteristics of the Vilaine flounder cohort came closer to the one observed in a highly stressed system, the Seine estuary, suggesting a potential selective pressure mainly induced by the chemical stress.

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References

  • Amara R, Meziane T, Gilliers C, Hermel G, Laffargue P (2007) Growth and condition indices in juvenile sole Solea solea measured to assess the quality of essential fish habitat. Mar Ecol Prog Ser 351:201–208

    Article  Google Scholar 

  • Antunes P, Santos R (1999) Integrated environmental management of the oceans. Ecol Econ 31:215–226

    Article  Google Scholar 

  • Beck MW, Heck KL Jr, Able KW, Childers DL, Eggleston DB, Gillanders BM, Halpern B, Hays CG, Hoshino K, Minello TJ (2001) The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates. BioScience 51:633–641

    Article  Google Scholar 

  • Belkhir K, Borsa P, Goudet P, Bonhomme F (1996) GENETIX, logiciel sous Windows pour la génétique des populations. Laboratoire Génome et Populations, CNRS UPR 9060, Université de Montpellier II, Montpellier

  • Berrebi P (1988) Génétique des populations marines: le modèle “flet” (Platichthys flesus L. 1758), Téléostéen, Pleuronectidé. PhD thesis, Université des Sciences et Techniques du Languedoc, Montpellier

  • Bony S, Gillet C, Bouchez A, Margoum C, Devaux A (2008) Genotoxic pressure of vineyard pesticides in fish: field and mesocosm surveys. Aquat Toxicol 89:197–203

    Article  CAS  Google Scholar 

  • Borsa P, Blanquer A, Berrebi P (1997) Genetic structure of the flounder Platichthys flesus and P. stellatus at different geographic scales. Mar Biol 129:233–246

    Article  CAS  Google Scholar 

  • Cabral H, Costa MJ (1999) Differential use of nursery areas within the Tagus estuary by sympatric Soles, Solea solea and Solea senegalensis. Environ Biol Fish 56:389–397

    Article  Google Scholar 

  • Cabral HN, Vasconcelos R, Vinagre C, França S, Fonseca V, Maia A, Reis-Santos P, Lopes M, Ruano M, Campos J (2007) Relative importance of estuarine flatfish nurseries along the Portuguese coast. J Sea Res 57:209–217

    Article  Google Scholar 

  • Cachot J, Galgani F, Vincent F (1998) cDNA cloning and expression analysis of flounder p53 tumour suppressor gene. Comp Biochem Physiol Part B Biochem Mol Biol 121:235–242

    Article  CAS  Google Scholar 

  • Cachot J, Geffard O, Augagneur S, Lacroix S, Le Menach K, Peluhet L, Couteau J, Denier X, Devier MH, Pottier D, Budzinski H (2006) Evidence of genotoxicity related to high PAH content of sediments in the upper part of the Seine estuary (Normandy, France). Aquat Toxicol 79:257–267

    Article  CAS  Google Scholar 

  • Cailleaud K, Forget-Leray J, Souissi S, Hilde D, LeMenach K, Budzinski H (2007) Seasonal variations of hydrophobic organic contaminant concentrations in the water-column of the Seine Estuary and their transfer to a planktonic species Eurytemora affinis (Calanoïda, copepoda). Part 1: PCBs and PAHs. Chemosphere 70:270–280

    Article  CAS  Google Scholar 

  • Clark DR, Bickham JW, Baker DL, Cowman F (2000) Environmental contaminants in Texas, USA, wetland reptiles: evaluation using blood samples. Environ Toxicol Chem 19:2259–2265

    CAS  Google Scholar 

  • Costanza R (1999) The ecological, economic, and social importance of the oceans. Ecol Econ 31:199–213

    Article  Google Scholar 

  • Courrat A, Lobry J, Nicolas D, Laffargue P, Amara R, Lepage M, Girardin M, Le Pape O (2009) Anthropogenic disturbance on nursery function of estuarine areas for marine species. Est Coast Shelf Sci 81(2):179–190

    Article  Google Scholar 

  • Dauvin JC, Ruellet T (2008) Macrozoobenthic biomass in the Bay od Seine (Eastern English Channel). J Sea Res 59:320–326

    Article  Google Scholar 

  • de Andrade VM, de Freitas TRO, da Silva J (2004) Comet assay using mullet (Mugil sp.) and sea catfish (Netuma sp.) erythrocytes for the detection of genotoxic pollutants in aquatic environment. Mut Res Genet Toxicol Environ Mutagen 560:57–67

    Article  Google Scholar 

  • de Campos Ventura B, de Angelis DF, Marin-Morales MA (2008) Mutagenic and genotoxic effects of the Atrazine herbicide in Oreochromis niloticus (Perciformes, Cichlidae) detected by the micronuclei test and the comet assay. Pest Biochem Physiol 90:42–51

    Article  Google Scholar 

  • Durou C, Poirier L, Amiard JC et al (2007) Biomonitoring in a clean and a multi-contaminated estuary based on biomarkers and chemical analyses in the endobenthic worm Nereis diversicolor. Eviron Poll 148:445–458

    Article  CAS  Google Scholar 

  • Emmert JL, Webel DM, Biehl RR, Griffiths MA, Garrow LS, Garrow TA, Baker DH (1998) Hepatic and renal betaine homocysteine methyltransferase activity in pigs as affected by dietary intakes of sulphur amino acids, choline and betaine. J Anim Sci 76:606–610

    CAS  Google Scholar 

  • Evrard E, Devaux A, Bony S, Burgeot T, Riso R, Budzinski H, Le Du M, Quiniou L, Laroche J (2010a) Responses of the European flounder Platichthys flesus to the chemical stress in estuaries: load of contaminants, gene expression, cellular damage and growth rate. Biomarkers 15(2):111–127

    Article  CAS  Google Scholar 

  • Evrard E, Marchand J, Théron M, Pichavant-Rafini K, Durand G, Quiniou L, Laroche J (2010b) Impact of mixtures of herbicides on molecular and physiological responses of the European flounder Platichthys flesus. Comp Biochem Physiol C 153:321–331

    Google Scholar 

  • Fairbairn DW, Olive PL, O’Neill KL (1995) The comet assay: a comprehensive review. Mutat Res 339:37–59

    Article  CAS  Google Scholar 

  • Feder ME, Walser JC (2005) The biological limitations of transcriptomics in elucidating stress and stress responses. J Evol Biol 18:901–910

    Article  CAS  Google Scholar 

  • Fodrie FJ, Levin LA (2008) Linking juvenile habitat utilization to population dynamics of California halibut. Limnol Oceanogr 53(2):799–812

    Article  Google Scholar 

  • Fonseca V, Cabral HN (2007) Are fish early growth and condition patterns related to life-history patterns? Rev Fish Biol Fish 17(4):545–564

    Article  Google Scholar 

  • Fonseca VF, Vinagre C, Cabral HN (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(5):1551–1562

    Article  CAS  Google Scholar 

  • Fujimori K, Inui T, Uodome N, Kadoyama K, Aritake K, Urade Y (2006) Zebrafish and chicken lipocalin-type prostaglandin D synthase homologues: conservation of mammalian gene structure and binding ability for lipophilic molecules, and difference in expression profile and enzyme activity. Gene 375:14–25

    Article  CAS  Google Scholar 

  • Gibson RN (1994) Impact of habitat quality and quantity on the recruitment of juvenile fishes. Neth J Sea Res 32(2):191–206

    Article  Google Scholar 

  • Guinand B, Rolland JL, Bonhomme F (2008) Genetic structure of the common sole (Solae solea) in the Bay of Biscay: nurseries as units of selection? Est Coast Shelf Sci 78:316–326

    Article  Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportions for multiple alleles. Biometrics 48:361–372

    Article  CAS  Google Scholar 

  • Horst MN, Walker AN, Bush P, Wilson T, Chang ES, Miller T, Larkin P (2007) Pesticide induced alterations in gene expression in the lobster, Homarus americanus. Comp Biochem Physiol 2D:44–52

    CAS  Google Scholar 

  • Hunt von Herbing I, White L (2002) The effects of body mass and feeding on metabolic rate in small juvenile Atlantic cod. J Fish Biol 61:945–958

    Article  Google Scholar 

  • 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. Sci Mar 53:567–575

    Google Scholar 

  • Laroche J, Quiniou L, Juhel G, Auffret M, Moraga D (2002) Genetic and physiologic responses of flounder (Platichthys flesus) populations to chemical contamination in estuaries. Environ Toxicol Chem 21(12):2705–2712

    CAS  Google Scholar 

  • Laroche J, Gauthier O, Quiniou L, Devaux A, Bony S, Evrard E, Cachot J, Chérel Y, Riso R, Pichereau V, Le Du M, Budzinski H (2012) Variation patterns in individual fish responses to chemical stress among estuaries, seasons and genders: the case of the European flounder (Platichthys flesus) in the Bay of Biscay. Environ Sci Pollut R (Special Issue EXECO)

  • Le Pape O, Holley J, Guérault D, Désaunay Y (2003a) Quality of coastal and estuarine essential fish habitats: estimations based on the size of juvenile common sole (Solea solea, L.). Est Coast Shelf Sci 58:793–803

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Leberg PL (1992) Effects of population bottlenecks on genetic diversity as measured by allozyme electrophoresis. Evolution 46(2):477–494

    Article  Google Scholar 

  • Levine AJ (1997) p53, the cellular gatekeeper for growth and division. Cell 88(3):323–331

    Article  CAS  Google Scholar 

  • Liepelt A, Karbe L, Westendorf J (1995) Induction of DNA strand breaks in rainbow trout Oncorhynchus mykiss under hypoxic and hyperoxic conditions. Aquat Toxicol 33:177–181

    Article  CAS  Google Scholar 

  • Lin J, Chen J, Elenbaas B, Levine AJ (1994) Several hydrophobic amino acids in the p53 amino-terminal domain are required for transcriptional activation, binding to mdm-2 and the adenovirus 5 E1B 55-kD protein. Genes Dev 8:1235–1246

    Article  CAS  Google Scholar 

  • Lin-Lee YC, Kao FT, Cheung P, Chan L (1985) Apolipoprotein E gene mapping and expression: localization of the structural gene to human chromosome 19 and expression of ApoE mRNA in lipoprotein- and non-lipoprotein-producing tissues. Biochemistry 24:3751–3756

    Article  CAS  Google Scholar 

  • Livingstone DR (2003) Oxidative stress in aquatic organisms in relation to pollution and aquaculture. Rev Méd Vét 154:427–430

    CAS  Google Scholar 

  • Lockhart DJ, Winzeler EA (2000) Genomics, gene expression and DNA arrays. Nature 405:827–836

    Article  CAS  Google Scholar 

  • Marchand J, Tanguy A, Laroche J, Quiniou L, Moraga D (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

    Article  CAS  Google Scholar 

  • Marchand J, Quiniou L, Riso R, Thebaut M-T, Laroche J (2004) Physiological cost of tolerance to toxicants in the European flounder Platichthys flesus, along the French Atlantic Coast. Aquat Toxicol 70:327–343

    Article  CAS  Google Scholar 

  • Marchand J, Tanguy A, Charrier G, Quiniou L, Plee-Gauthier E, Laroche J (2006) Molecular identification and expression of differentially regulated genes of the European flounder, Platichthys flesus, submitted to pesticide exposure. Mar Biotechnol 8:275–294

    Article  CAS  Google Scholar 

  • Marchand J, Evrard E, Guinand B, Cachot J, Quiniou L, Laroche J (2010) Genetic polymorphism and its potential relation to environmental stress in five populations of the European flounder Platichthys flesus, along the French Atlantic coast. Mar Environ Res 70:201–209

    Article  CAS  Google Scholar 

  • Masson G (1987). Biologie et écologie d’un poisson plat amphihalin, le flet (Platichthys flesus flesus Linné, 1758) dans l’environnement ligérien : distribution, démographie, place au sein des réseaux trophiques. PhD thesis, Université de Bretagne Occidentale

  • Menesguen A, Aminot A, Belin C, Chapelle A, Guillaud J-F, Joanny M, Lefebvre A, Merceron M, Piriou J-Y, Souchu P (2001) L’eutrophisation des eaux marines et saumâtres en Europe, en particulier en France. Rapport IFREMER pour la Commission Européenne—DG.ENV.B1, 59p

  • Minier C, Abarnou A, Jaouen-Madoulet A, Le Guellec AM, Tutundjian R, Bocquené G, Leboulenger F (2006) A pollution-monitoring pilot study involving contaminant and biomarker measurements in the Seine Estuary, France, using zebra mussels (Dreissena polymorpha). Environ Toxicol Chem 25:112–119

    Article  CAS  Google Scholar 

  • Pellacani C, Buschini A, Furlini M, Poli P, Rossi C (2006) A battery of in vivo and in vitro tests useful for genotoxic pollutant detection in surface waters. Aquat Toxicol 77:1–10

    Article  CAS  Google Scholar 

  • Piry S (2000) Treemaker v1.0.1, INRA

  • Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GeneClass2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539

    Article  CAS  Google Scholar 

  • Pluquet O, Hainaut P (2001) Genotoxic and non-genotoxic pathways of p53 induction. Cancer Lett 174:1–15

    Article  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rogel A, Popliker M, Webb CG, Oren M (1985) p53 cellular tumor antigen: analysis of mRNA levels in normal adult tissues, embryos, and tumors. Mol Cell Biol 5:2851–2855

    CAS  Google Scholar 

  • Shugart LR (1998) Structural damage to DNA in response to toxicant exposure. In: Forbes VE (ed) Genetics and ecotoxicology. Taylor & Francis, New York, pp 151–167

    Google Scholar 

  • Singh N, McCoy M, Tice R, Schneider E (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res 175:184–191

    Article  CAS  Google Scholar 

  • Tennant AH, Peng B, Kligerman AD (2001) Genotoxicity studies of three triazine herbicides: in vivo studies using the alkaline single cell gel (SCG) assay. Mutat Res Genet Toxicol Environ Mutagen 493:1–10

    Article  CAS  Google Scholar 

  • van der Veer HW, Berghahn R, Miller JM, Rijnsdorp AD (2000) Recruitment in flatfish, with special emphasis on North Atlantic species: progress made by the flatfish symposia. ICES J Mar Sci 57:202–215

    Article  Google Scholar 

  • Vasconcelos RP, Reis-Santos P, Fonseca V, Maia A, Ruano M, França S, Vinagre C, Costa MJ, Cabral H (2007) Assessing anthropogenic pressures on estuarine fish nurseries along the Portuguese coast: a multi-metric index and conceptual approach. Sci Total Environ 374(2–3):199–215

    Article  CAS  Google Scholar 

  • Vasconcelos RP, Reis-Santos P, Tanner S, Maia A, Latkoczy C, Günther D, Costa MJ, Cabral H (2008) Evidence of estuarine nursery origin of five coastal fish species along the Portuguese coast through otolith elemental fingerprints. Est Coast Shelf Sci 79(2):317–327

    Article  Google Scholar 

  • Vindelov LL, Christensen IJ (1990) A review of techniques and results obtained in one laboratory by an integrated system on methods designed for routine clinical flow cytometric DNA analysis. Cytometry 11:753–770

    Article  CAS  Google Scholar 

  • Wickliffe JK, Bickham JW (1998) Flow cytometric analysis of haematocytes from Brown Pelicans (Pelecanus occidentalis) exposed to planar halogenated hydrocarbons and heavy metals. Bull Environ Contam Toxicol 61:239–246

    Article  CAS  Google Scholar 

  • Wright S (1969) Evolution and the genetics of populations, Vol. 2: The theory of gene frequencies. University of Chicago Press, Chicago

    Google Scholar 

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Acknowledgments

This study was supported by the INTERREG program: DIESE by the DEVIL-INERIS program and by the EVOLFISH project (ANR-VMCS). Authors also thank F. and R. Triballier (Vilaine) and C. Drouin (Seine) for field sampling. The authors also wish to thank Dr Henrique Cabral for his helpful comments on the manuscript.

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Authors and Affiliations

  1. CEDRE, rue Alain Colas, CS 41836, 29218, Brest Cedex 2, France

    Estérine Evrard

  2. USC INRA “Impact génotoxique sur les hydrosystèmes”, UMR LEHNA 5023, ENTPE, Rue Maurice Audin, 69518 Vaulx en Velin, Cedex, France

    Alain Devaux & Sylvie Bony

  3. Univ. Bordeaux, EPOC UMR 5805, LPTC group, avenue des Facultés, 33405, Talence, France

    Jérôme Cachot

  4. Department of Marine Ecology, Univ. Gothenburg, Tjärnö, SE-452 96, Strömstad, Sweden

    Grégory Charrier

  5. Université Européenne de Bretagne, Université de Brest, UMR 6539 CNRS/UBO/IRD/Ifremer, Laboratoire des Sciences de l’Environnement Marin LEMAR, Institut Universitaire Européen de la Mer, 29280, Plouzané, France

    Louis Quiniou & Jean Laroche

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  1. Estérine Evrard
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  2. Alain Devaux
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  3. Sylvie Bony
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  4. Jérôme Cachot
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  5. Grégory Charrier
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  6. Louis Quiniou
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  7. Jean Laroche
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Correspondence to Jean Laroche.

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Evrard, E., Devaux, A., Bony, S. et al. Responses of juvenile European flounder (Platichthys flesus) to multistress in the Vilaine estuary, during a 6-month survey. Environ Sci Pollut Res 20, 676–689 (2013). https://doi.org/10.1007/s11356-012-1138-z

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