Skip to main content
SpringerLink
Log in

Impact of dispersed fuel oil on cardiac mitochondrial function in polar cod Boreogadus saida

  • PAHs and fish – Exposure monitoring and adverse effects – from molecular to individual level
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

In this study, impact of dispersed oil on cardiac mitochondrial function was assessed in a key species of Arctic marine ecosystem, the polar cod Boreogadus saida. Mature polar cod were exposed during 48 h to dispersed oil (mechanically and chemically) and dispersants alone. The increase observed in ethoxyresorufin-O-deethylase activity and polycyclic aromatic hydrocarbon metabolites in bile indicated no difference in contamination level between fish exposed to chemical or mechanical dispersion of oil. Oil induced alterations of O2 consumption of permeabilised cardiac fibres showing inhibitions of complexes I and IV of the respiratory chain. Oil did not induce any modification of mitochondrial proton leak. Dispersants did not induce alteration of mitochondrial activity and did not increase oil toxicity. These data suggest that oil exposure may limit the fitness of polar cod and consequently could lead to major disruption in the energy flow of polar ecosystem.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aas E, Beyer J, Goksøyr A (2000) Fixed wavelength fluorescence (FF) of bile as a monitoring tool for polyaromatic hydrocarbon exposure in fish: an evaluation of compound specificity, inner filter effect and signal interpretation. Biomarkers 5:9–23

    Article  CAS  Google Scholar 

  • Bains OS, Kennedy CJ (2004) Energetic costs of pyrene metabolism in isolated hepatocytes of rainbow trout, Oncorhynchus mykiss. Aquat Toxicol 67:217–226

    Article  CAS  Google Scholar 

  • Bradstreet MSW, Finley KJ, Sekerak AD, Griffiths WB, Evans CR, Fabjan MF (1986) Aspects of biology of Arctic cod (Boreogadus saida) and its importance in Arctic marine food chains. Can Tech Rep Fischeries Aquat Sci 1491

  • Cameron JA, Smith RL (1980) Ultrastructure effects of crude oil on early life stages of Pacific herring. Trans Am Fish Soc 109:224–228

    Article  Google Scholar 

  • Chapman H, Purnell K, Law RJ, Kirby MF (2007) The use of chemical dispersants to combat oil spills at sea: a review of practice and research needs in Europe. Mar Pollut Bull 54:827–838

    Article  CAS  Google Scholar 

  • Christiansen JS, Karamushko LI, Nahrgang J (2010) Sub-lethal levels of waterborne petroleum may depress routine metabolism in polar cod Boreogadus saida (Lepechin, 1774). Polar Biol 33:1049–1055

    Article  Google Scholar 

  • Claireaux G, Théron M, Prineau M, Dussauze M, Merlin FX, Le Floch S (2013) Effects of oil exposure and dispersant use upon environmental adaptation performance and fitness in the European sea bass, Dicentrarchus labrax. Aquat Toxicol 130–131:160–170

    Article  Google Scholar 

  • Comiso JC, Parkinson CL, Gersten R, Stock L (2008) Accelerated decline in the Arctic sea ice cover. Geophys. Res. Lett 35

  • Correa M, Garcia HI (1990) Physiological responses of juvenile white mugil, Mugil curema, exposed to benzene. Bull Environ Contam Toxicol 44:428–434

    Article  CAS  Google Scholar 

  • Danion M, Le Floch S, Kanan R, Lamour F, Quentel C (2011) Effects of in vivo chronic hydrocarbons pollution on sanitary status and immune system in sea bass (Dicentrarchus labrax L.). Aquat Toxicol 105:300–311

    Article  CAS  Google Scholar 

  • Davoodi F, Claireaux G (2007) Effects of exposure to petroleum hydrocarbons upon the metabolism of the common sole Solea solea. Mar Pollut Bull 54:928–934

    Article  CAS  Google Scholar 

  • Eggens ML, Galgani F (1992) Ethoxyresorufin-O-deethylase (EROD) activity in flatfish: fast determination with a fluorescence plate-reader. Mar Environ Res 33:213–221

    Article  CAS  Google Scholar 

  • Fusey P, Oudot J (1976) Comparaison de deux méthodes d’évaluation de la biodégradation des hydrocarbures in vitro. Mater Organismen (Berlin) 4:241–251

    Google Scholar 

  • Gardiner WW, Word JQ, Word JD, Perkins RA, McFarlin KM, Hester BW, Word LS, Ray CM (2013) The acute toxicity of chemically and physically dispersed crude oil to key arctic species under arctic conditions during the open water season. Environ Toxicol Chem 32(10):2284–2300

    Article  CAS  Google Scholar 

  • Goksøyr A, Förlin L (1992) The cytochrome P450 system in fish, aquatic toxicology and environmental monitoring. Aquat Toxicol 22:287–312

    Article  Google Scholar 

  • Hicken CE, Linbo TL, Baldwin DH, Willis ML, Myers MS, Holland L, Larsen M, Stekoll MS, Rice SD, Collier TK, Scholz NL, Incardona JP (2011) Sublethal exposure to crude oil during embryonic development alters cardiac morphology and reduces aerobic capacity in adult fish. Proc Natl Acad Sci 108:7086–7090

    Article  CAS  Google Scholar 

  • Hop H, Gjøsæter H (2013) Polar cod (Boreogadus saida) and capelin (Mallotus villosus) as key species in marine food webs of the Arctic and the Barents Sea. Mar Biol Res 9:878–894

    Article  Google Scholar 

  • Hose JE, Puffer HW (1984) Oxygen consumption of grunion (Leuresthes tenuis) embryos exposed to the petroleum hydrocarbon, benzo[a]pyrene. Environ Res 35:413–420

    Article  CAS  Google Scholar 

  • Jonsson H, Sundt RC, Aas E, Sanni S (2010) The Arctic is no longer put on ice: evaluation of polar cod (Boreogadus saida) as a monitoring species of oil pollution in cold waters. Mar Pollut Bull 60:390–395

    Article  CAS  Google Scholar 

  • Jung D, Di Giulio RT (2010) Identification of mitochondrial cytochrome P450 induced in response to polycyclic aromatic hydrocarbons in the mummichog (Fundulus heteroclitus). Comp Biochem Physiol Part C: Toxicol Pharmacol 151:107–112

    Google Scholar 

  • Knecht AL, Goodale BC, Truong L, Simonich MT, Swanson AJ, Matzke MM, Waters KA, Waters KM, Tanguay RL (2013) Comparative developmental toxicity of environmentally relevant oxygenated PAHs. Toxicol Appl Pharmacol 271:266–275

    Article  CAS  Google Scholar 

  • Kuznetsov AV, Veksler V, Gellerich FN, Saks V, Margreiter R, Kunz WS (2008) Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells. Nat Protoc 3:965–976

    Article  CAS  Google Scholar 

  • Lessard RR, Demarco G (2000) The significance of oil spill dispersants. Spill Sci Technol Bull 6:59–68

    Article  CAS  Google Scholar 

  • Lewis A, Crosbie A, Davies L, Lunel T (1998) Large scale field experiments into oil weathering at sea and aerial application of dispersants. In Proceedings of the 21st Arctic and Marine Oil Spill Program (AMOP), Edmonton, Canada

  • Lin ELC, Cormier SM, Torsella JA (1996) Fish biliary polycyclic aromatic hydro-carbon metabolites estimated by fixed-wavelength fluorescence: comparison with HPLC-fluorescent detection. Ecotoxicol Environ Saf 35:16–23

    Article  CAS  Google Scholar 

  • Luna-Acosta A, Kanan R, Le Floch S, Huet V, Pineau P, Bustamante P, Thomas-Guyon H (2011) Enhanced immunological and detoxification responses in Pacific oysters, Crassostrea gigas, exposed to chemically dispersed oil. Water Res 45:4103–4118

    CAS  Google Scholar 

  • Lunel T, Rusin J, Bailey N, Halliwell C, Davies L (1997) The net environmental benefit of a successful dispersant operation at the Sea Empress incident. In: Proceedings of the 1997 International oil Spill Conference API Washington, DC, 184–194

  • Mackey AP, Atkinson A, Hill SL, Ward P, Cunningham NJ, Johnston NM, Murphy EJ (2012) Antarctic macrozooplankton of the southwest Atlantic sector and Bellingshausen Sea: baseline historical distributions (Discovery Investigations, 1928–1935) related to temperature and food, with projections for subsequent ocean warming. Deep-Sea Res II 59–60:130–146

    Article  Google Scholar 

  • Milinkovitch T, Kanan R, Thomas-Guyon H, Le Floch S (2011a) Effects of dispersed oil exposure on the bioaccumulation of polycyclic aromatic hydrocarbons and mortality of juvenile Liza ramada. Sci Total Environ 409:1643–1650

    Article  CAS  Google Scholar 

  • Milinkovitch T, Ndiaye A, Sanchez W, Le Floch S, Thomas-Guyon H (2011b) Liver antioxidant and plasma immune responses in juvenile golden grey mullet (Liza aurata) exposed to dispersed crude oil. Aquat Toxicol 101:155–164

    Article  CAS  Google Scholar 

  • Milinkovitch T, Lucas J, Le Floch S, Thomas-Guyon H, Lefrançois C (2012) Effect of dispersed crude oil exposure upon the aerobic metabolic scope in juvenile golden grey mullet (Liza aurata). Mar Pollut Bull 64:865–871

    Article  CAS  Google Scholar 

  • Milinkovitch T, Imbert N, Sanchez W, Le Floch S, Thomas-Guyon H (2013) Toxicological effects of crude oil and oil dispersant: Biomarkers in the heart of the juvenile golden grey mullet (Liza aurata). Ecotoxicol Environ Saf 88:1–8

    Article  CAS  Google Scholar 

  • Musatov A, Robinson NC (2012) Susceptibility of mitochondrial electron-transport complexes to oxidative damage. Focus on cytochrome c oxidase. Free Radic Res 46(11):1313–1326

    Article  CAS  Google Scholar 

  • Nahrgang J, Camus L, Carls MG, Gonzalez P, Jönsson M, Taban IC, Bechmann, RK, Christiansen JS, Hop H, (2009). Biomarker responses in polar cod (Boreogadus saida) exposed to the water soluble fraction of crude oil. Aquat. Toxicol.11.003

  • Nahrgang J, Camus L, Broms F, Christiansen JS, Hop H (2010) Seasonal baseline levels of physiological and biochemical parameters in polar cod (Boreogadus saida): implications for environmental monitoring. Mar Pollut Bull 60:1336–1345

    Article  CAS  Google Scholar 

  • Norton WN, Maitie DR, Kearns CL (1985) The cytopathologic effects of specific aromatic hydrocarbons. AJP 387–397

  • Orlova EL, Dolgov AV, Rudneva GB, Oganin IA, Konstantinova LL (2009) Trophic relations of capelin Mallotus villosus and polar cod Boreogadus saida in the Barents Sea as a factor of impact on the ecosystem. Deep-Sea Res II 56:2054–2067

    Article  Google Scholar 

  • Perovich DK, Ritcher-Menge JA, Jones KF, Light B (2008) Sunlight, water, and ice: extreme Arctic sea ice melt during the summer of 2007. Geophys Res Lett 35, L11501

    Article  Google Scholar 

  • Pietri D, Soule A, Kershner J, Soles P, Sullivan M (2008) The Arctic shipping and environmental management agreement: a regime for marine pollution. Coast Manag 36(5):508–523

    Article  Google Scholar 

  • Ramachandran SD, Hodson PV, Khan CW, Lee K (2004) Oil dispersant increases PAH uptake by fish exposed to crude oil. Ecotoxicol Environ Saf 59:300–308

    Article  CAS  Google Scholar 

  • Rowe C, Mitchelmore C, Baker J (2009) Lack of biological effects of water accommodated fractions of chemically- and physically-dispersed oil on molecular, physiological, and behavioral traits of juvenile snapping turtles following embryonic exposure. Sci Total Environ 407:5344–5355

    Article  CAS  Google Scholar 

  • Salazar I, Pavani M, Aranda W, Maya JD, Morello A, Ferreira J (2004) Alterations of rat liver mitochondrial oxidative phosphorylation and calcium uptake by benzo[a]pyrene. Toxicol Appl Pharmacol 1981–10

  • Serigstad B, Adoff GR (1985) Effects of oil exposure on oxygen consumption of cod eggs and larvae. Mar Environ Res 17:266–268

    Article  CAS  Google Scholar 

  • Sharp JR, Fucik KW, Neff JM (1979) Physiological basis of differential sensitivity of fish embryonic stages to oil pollution. In: Vernberg WB, Calabrese A, Thurberg FP, Vernberg FJ (eds) Marine pollution: functional responses. Academic, New York, pp 85–108

    Chapter  Google Scholar 

  • Spooner MF (1970) Oil spill in Tarut Bay. Saudi Arab Mar Pollut Bull 1:166–167

    Article  Google Scholar 

  • Stabenau EK, Sasser A, Schulte C (2008) The effects of pyrene exposure on exercise performance, muscle contraction, and mitochondrial O2 consumption in the leopard frog (Rana pipiens). J Environ Sci Health A Tox Hazard Subst Environ Eng 43(6):576–583

    Article  CAS  Google Scholar 

  • Stange K, Klungsøyr J (1997) Organochlorine contaminants in fish and polycyclic aromatic hydrocarbons in sediments from the Barents Sea. ICES J Mar Sci 54(3):318–332

    Article  Google Scholar 

  • Toleikis A, Majiene D, Trumbeckaite S, Dagys A (1997) The effects of ischemia and experimental conditions on the respiration rate of cardiac fibers. Moll Cell Biochem 174:87–90

    Article  CAS  Google Scholar 

  • US Geological Survey (2000) World Petroleum Assessment 2000—description and results. US Geological Survey, Reston

    Google Scholar 

  • van der Oost R, Beyer J, Vermeulen N (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149

    Article  Google Scholar 

  • Veksler V, Kuznetsov AV, Sharov VG, Kapelko VI, Saks VA (1987) Mitochondrial respiratory parameters in cardiac tissue: a novel method of assessment by using saponin-skinned fibers. Biochim Biophys Acta 892:191–196

    Article  CAS  Google Scholar 

  • Vuontisjärvie H, Keinänen M, Vuorinen P, Peltonen K (2004) A comparison of HPLC with fluorescence detection and fixed wavelength fluorescence methods for the determination of polycyclic aromatic hydrocarbon metabolites in fish. Polycyc Aromat Comp 24:333–342

    Article  Google Scholar 

  • Vuorinen P, Keinänen M, Vuotisjärvie H, Barsiene J, Broeg K, Förlin L, Gercken J, Kopecka J, Köhler A, Pkkonen J, Pempkowiak J, Schiedek D (2006) Use of PAH metabolites as a biomarker of pollution in fish from the Baltic sea. Mar Pollut Bull 55:479–487

    Article  Google Scholar 

  • Welch HE, Bergmann MA, Siferd TD, Martin KA, Curtis MF, Crawford RE (1992) Energy flow through the marine ecosystem of the Lancaster Sound region, Arctic Canada. Arctic 45:342–357

    Article  Google Scholar 

  • Westman O, Nordén M, Larsson M, Johansson J, Venizelos N, Hollert H, Engwall M (2013) Polycyclic aromatic hydrocarbons (PAHs) reduce hepatic β-oxidation of fatty acids in chick embryos. Environ Sci Pollut Res Int Mar 20(3):1881–1888

    Article  CAS  Google Scholar 

  • Whyte JJ, Jung RE, Schmitt CJ, Tillitt DE (2000) Ethoxyresorufin-O-deethylase (EROD) activity in fish as a biomarker of chemical exposure. Crit rev Toxicol 30:347–550

    Article  CAS  Google Scholar 

  • Xia T, Korge P, Weiss JN, Li N, Venkatesen MI, Sioutas C, Nel A (2004) Quinones and aromatic chemical compounds in particulate matter induce mitochondrial dysfunction: implications for ultrafine particle toxicity. Environ Healt Perspect 112:1347–1358

    Article  CAS  Google Scholar 

  • Zhu H, Li YB, Trush MA (1995) Characterization of benzo[a]pyrene quinone-induced toxicity to primary cultured bone marrow stromal cells from DBA/2 mice: Potential role of mitochondrial dysfunction. Toxicol Appl Pharmacol 130:108–120

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by a Ph.D. grant from Total Fluides, a mobility grant from the Université de Bretagne Occidentale and the FearIce project financed by the Ministry of Environment Norway through the Fram Centre. The authors thank Sally Fergusson (Alba Traduction) for improving the English of the manuscript.

Author information

Authors and Affiliations

  1. Laboratoire ORPHY EA4324, Université de Bretagne Occidentale, 6 Avenue le Gorgeu, CS 93 837, 29 238, Brest Cedex 3, France

    Matthieu Dussauze, Karine Pichavant-Rafini, Aline Amérand & Michael Theron

  2. Cedre, Centre de Documentation, de Recherche et d’Expérimentations sur les Pollutions Accidentelles des Eaux, 715 rue Alain Colas, CS 41 836, Brest Cedex 2, France

    Matthieu Dussauze, Stéphane Le Floch & Nathalie Coquillé

  3. Akvaplan-niva, High North Research Centre for Climate and the Environment, 9296, Tromsø, Norway

    Lionel Camus & Perrine Geraudie

  4. Engineering and Safety Department, University of Tromsø, Tromsø, Norway

    Lionel Camus

  5. Total Fluides Total Fluides, S.A. 92907, Paris la Défense, France

    Philippe Lemaire

Authors
  1. Matthieu Dussauze
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lionel Camus
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stéphane Le Floch
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Karine Pichavant-Rafini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Perrine Geraudie
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nathalie Coquillé
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Aline Amérand
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Philippe Lemaire
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Michael Theron
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matthieu Dussauze.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dussauze, M., Camus, L., Le Floch, S. et al. Impact of dispersed fuel oil on cardiac mitochondrial function in polar cod Boreogadus saida . Environ Sci Pollut Res 21, 13779–13788 (2014). https://doi.org/10.1007/s11356-014-2618-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-2618-0

Keywords

Search

Navigation