Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-8448b6f56d-xtgtn Total loading time: 0 Render date: 2024-04-23T10:40:01.856Z Has data issue: false hasContentIssue false

9 - Cytochrome P450 1A (CYP1A) as a biomarker in oil spill assessments

Published online by Cambridge University Press:  05 July 2013

By
James T. Oris  and
Aaron P. Roberts
Edited by
John A. Wiens
John A. Wiens
Affiliation:
PRBO Conservation Science, California and University of Western Australia, Perth
Get access

Summary

Introduction

More than 30 years ago, scientists began measuring biochemical and molecular responses in organisms as a way to understand pathways of exposure to chemicals in the environment. These responses, termed biomarkers, help screen for the presence or absence of classes of chemicals (e.g., aromatic hydrocarbons, metals) and other stressors (e.g., temperature, oxidative stress). They can also indicate possible mechanisms or pathways of potential toxic outcomes and provide direction for additional, more detailed analysis of the effects of exposures.

Biomarkers have been used extensively in studies of oil spills (Anderson and Lee, 2006). Investigations following the Exxon Valdez spill considered biomarkers for many species, including sea otters (Enhydra lutris), river otters (Lontra canadensis), harlequin ducks (Histrionicus histrionicus), Barrow’s goldeneye (Bucephala islandica), black oystercatchers (Haematopus bachmani), pigeon guillemots (Cepphus columba), intertidal fish, rockfish (Sebastes spp.), bottom fish, pink salmon embryos (Oncorhynchus gorbuscha), and mussels (Mytilus spp.).

No biomarker has received more attention than the Cytochrome P450 1A (CYP1A) enzyme system. Tens of thousands of papers have been published on using the CYP1A system as evidence of exposure to aromatic hydrocarbons found in fossil fuels and industrial chemicals. However, there are conflicting opinions in the literature on using the CYP1A system as a measure of low-level oil exposure when multiple sources of aromatic hydrocarbons are present. There are also conflicting opinions on whether the CYP1A system can be used as an indicator of both exposure and of effect or injury.

Type
Chapter
Information
Oil in the Environment
Legacies and Lessons of the Exxon Valdez Oil Spill
 , pp. 201 - 219
Publisher: Cambridge University Press
Print publication year: 2013

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

Anderson, J.W. and Lee, R.F. (2006). Use of biomarkers in oil spill risk assessment in the marine environment. Human and Ecological Risk Assessment 12(6): 1192–1222.CrossRefGoogle Scholar
Ankley, G.T., Miracle, A.L., Perkins, E.J., and Daston, G.P., eds (2007). Genomics in Regulatory Ecotoxicology: Applications and Challenges. Boca Raton, FL, USA: CRC Press; ISBN-10: 142006682X; ISBN-13: 9781420066821.Google Scholar
Assunção, M.G.L., Miller, K.A., Dangerfield, N.J., Bandiera, S.M., and Ross, P.S. (2007). Cytochrome P450 1A expression and organochlorine contaminants in harbour seals (Phoca vitulina): evaluating a biopsy approach. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 145(2): 256–264.Google ScholarPubMed
Balk, L., Hylland, K., Hansson, T., Berntssen, M.H.G., Beyer, J., Jonsson, G., Melbye, A., Grung, M., Torstensen, B.E., Børseth, J.F., Skarphedinsdottir, H., and Klungsøyr, J. (2011). Biomarkers in natural fish populations indicate adverse biological effects of offshore oil production. PLoS ONE 6(5): e19735; DOI:10.1371/journal.pone.0019735.CrossRefGoogle ScholarPubMed
Ballachey, B.E., Stegeman, J.J., Snyder, P.W., Blundell, G.M., Bodkin, J.L., Dean, T.A., Duffy, L., Esler, D., Golet, G., Jewett, S., Holland-Bartels, L., Rebar, A.H., Seiser, P.E., and Trust, K.A. (2002). Oil exposure and health of nearshore vertebrate predators in Prince William Sound following the 1989 Exxon Valdez oil spill. In Mechanisms of Impact and Potential Recovery of Nearshore Vertebrate Predators following the 1989 Exxon Valdez Oil Spill. Holland-Bartels, L.E., ed. Anchorage, AK, USA: USGeological Survey, Alaska Biological Science Center; Exxon Valdez Oil Spill Restoration Project 99025 Final Report; Volume 1, 2.1–2.35.Google Scholar
Ben-David, M., Kondratyuk, T., Woodin, B.R., Snyder, P.W., and Stegeman, J.J. (2001). Induction of cytochrome P450 1A1 expression in captive river otters fed Prudhoe Bay crude oil: Evaluation by immunohistochemistry and quantitative RT-PCR. Biomarkers 6(3): 218–235.CrossRefGoogle ScholarPubMed
Bilbao, E., Raingeard, D., Diaz de Cerio, O., Ortiz-Zarragoitia, M., Ruiz, P., Izagirre, U., Orbea, A., Marigómez, I., Cajaraville, M.P., and Cancio, I. (2010). Effects of exposure to Prestige-like heavy fuel oil and to perfluorooctanesulfonate on conventional biomarkers and target gene transcription in the thicklip grey mullet Chelon labrosus. Aquatic Toxicology 98(3): 282–296.CrossRefGoogle ScholarPubMed
Binelli, A., Cogni, D., Parolini, M., and Provini, A. (2010). Multi-biomarker approach to investigate the state of contamination of the R. Lambro/R. Po confluence (Italy) by zebra mussel (Dreissena polymorpha). Chemosphere 79(5): 518–528.CrossRefGoogle Scholar
Bodkin, J.L., Ballachey, B.E., Dean, T.A., Fukuyama, A.K., Jewett, S.C., McDonald, L., Monson, D.H., O’Clair, C.E., and VanBlaricom, G.R. (2002). Sea otter population status and the process of recovery from the 1989 “Exxon Valdez” oil spill. Marine Ecology Progress Series 241: 237–253.CrossRefGoogle Scholar
Bowen, L., Miles, A.K., Murray, M., Haulena, M., Tuttle, J., Van Bonn, W., Adams, L., Bodkin, J.L., Ballachey, B., Estes, J., Tinker, M.T., Keister, R., and Stott, J.L. (2012). Gene transcription in sea otters (Enhydra lutris); development of a diagnostic tool for sea otter and ecosystem health. Molecular Ecology Resources 12(1): 67–74.CrossRefGoogle ScholarPubMed
Bowen, L., Riva, F., Mohr, C., Aldridge, B., Schwartz, J., Miles, A.K., and Stott, J.L. (2007). Differential gene expression induced by exposure of captive mink to fuel oil: a model for the sea otter. EcoHealth 4(3):298–309.CrossRefGoogle Scholar
Carls, M.G., Heintz, R.A., Marty, C.D., and Rice, S.D. (2005). Cytochrome P450 1A induction in oil-exposed pink salmon Oncorhynchus gorbuscha embryos predicts reduced survival potential. Marine Ecology Progress Series 301: 253–265.CrossRefGoogle Scholar
Carvalho, R.N. and Lettieri, T. (2011). Proteomic analysis of the marine diatom Thalassiosira pseudonana upon exposure to benzo(a)pyrene. BMC Genomics 12: 159.CrossRefGoogle ScholarPubMed
Curtis, L., Garzon, C.B., Arkoosh, M., Collier, T., Myers, M.S., Buzitis, J., and Hahn, M.E. (2011). Reduced cytochrome P450 1A activity and recovery from oxidative stress during subchronic benzo[a]pyrene and benzo[e]pyrene treatment of rainbow trout. Toxicology and Applied Pharmacology 254(1): 1–7.CrossRefGoogle Scholar
Emlen, J.M. and Springman, K.R. (2007). Developing methods to assess and predict the population level effects of environmental contaminants. Integrated Environmental Assessment and Management 3(2): 157–165.CrossRefGoogle ScholarPubMed
Esler, D., Ballachey, B.E., Trust, K.A., Iverson, S.A., Reed, J.A., Miles, A.K., Henderson, J.D., Woodin, B.R., Stegeman, J.J., McAdie, M., Mulcahy, D.M., and Wilson, B.W. (2011). Cytochrome P450 1A biomarker indication of the timeline of chronic exposure of Barrow’s goldeneyes to residual Exxon Valdez oil. Marine Pollution Bulletin 62(3): 609–614.CrossRefGoogle Scholar
Esler, D., Trust, K.A., Ballachey, B.E., Iverson, S.A., Lewis, T.L., Rizzolo, D.J., Mulcahy, D.M., Miles, A.K., Woodin, B.R., Stegeman, J.J., Henderson, J.D., and Wilson, B.W. (2010). Cytochrome P450 1A biomarker indication of oil exposure in harlequin ducks up to 20 years after the Exxon Valdez oil spill. Environmental Toxicology and Chemistry 29(5): 1138–1145.Google Scholar
Esler, D. and Iverson, S.A. (2010). Female harlequin duck winter survival 11 to 14 years after the Exxon Valdez oil spill. Journal of Wildlife Management 74(3): 471–478.CrossRefGoogle Scholar
Forbes, V.E., Calow, P., and Sibly, R.M. (2008). The extrapolation problem and how population modeling can help. Environmental Toxicology and Chemistry 27(10): 1987–1994.CrossRefGoogle ScholarPubMed
Forbes, V.E., Palmqvist, A., and Bach, L. (2006). The use and misuse of biomarkers in ecotoxicology. Environmental Toxicology and Chemistry 25(1): 272–280.CrossRefGoogle ScholarPubMed
Godard-Codding, C.A.J., Clark, R., Fossi, M.C., Marsili, L., Maltese, S., West, A.G., Valenzuela, L., Rowntree, V., Polyak, I., Cannon, J.C., Pinkerton, K., Rubio-Cisneros, N., Mesnick, S.L., Cox, S.B., Kerr, I., Payne, R., and Stegeman, J.J. (2011). Pacific Ocean-wide profile of CYP1A1 expression, stable carbon and nitrogen isotope ratios, and organic contaminant burden in sperm whale skin biopsies. Environmental Health Perspectives 119(3): 337–343.CrossRefGoogle ScholarPubMed
Goldstone, J.V., Jönsson, M.E., Behrendt, L., Woodin, B.R., Jenny, M.J., Nelson, D.R., and Stegeman, J.J. (2009). Cytochrome P450 1D1: A novel CYP1A-related gene that is not transcriptionally activated by PCB126 or TCDD. Archives of Biochemistry and Biophysics 482(1–2): 7–16.CrossRefGoogle ScholarPubMed
Golet, G.H., Seiser, P.E., McGuire, A.D., Roby, D.D., Fischer, J.B., Kuletz, K.J., Irons, D.B., Dean, T.A., Jewett, S.C., and Newman, S.H. (2002). Long-term direct and indirect effects of the ‘Exxon Valdez’ oil spill on pigeon guillemots in Prince William Sound, Alaska. Marine Ecology Progress Series 241: 287–304.CrossRefGoogle Scholar
Handy, R.D., Galloway, T.S., and Depledge, M.H. (2003). A proposal for the use of biomarkers for the assessment of chronic pollution and in regulatory toxicology. Ecotoxicology 12(1–4): 331–343.CrossRefGoogle ScholarPubMed
Hicken, C.E., Linbo, T.L., Baldwin, D.H., Willis, M.L., Myers, M.S., Holland, L., Larsen, M., Stekoll, M.S., Rice, S.D., Collier, T.K., Scholz, N.L., and Incardona, J.P. (2011). Sublethal exposure to crude oil during embryonic development alters cardiac morphology and reduces aerobic capacity in adult fish. Proceedings of the National Academy of Sciences 108(17): 7086–7090.CrossRefGoogle ScholarPubMed
Hoffmann, J.L. and Oris, J.T. (2006). Altered gene expression: A mechanism for reproductive toxicity in zebrafish exposed to benzo[a]pyrene. Aquatic Toxicology 78(4): 332–340.CrossRefGoogle Scholar
Hoffmann, J.L., Torontali, S.P., Thomason, R.G., Lee, D.M., Brill, J.L., Price, B.B., Carr, G.J., and Versteeg, D.J. (2006). Hepatic gene expression profiling using genechips in zebrafish exposed to 17 alpha-ethynylestradiol. Aquatic Toxicology 79(3): 233–246.CrossRefGoogle Scholar
Hook, S.E., Cobb, M., Oris, J., and Anderson, J. (2008). Gene sequences for Cytochrome P450 1A1 and 1A2: The need for biomarker development in sea otters (Enhydra lutris). Comparative Biochemistry and Physiology – Part B: Biochemistry and Molecular Biology 151(3): 336–348.CrossRefGoogle Scholar
Hook, S.E., Lampi, M.A., Febbo, E.J., Ward, J.A., and Parkerton, T.F. (2010). Temporal patterns in the transcriptomic response of rainbow trout, Oncorhynchus mykiss, to crude oil. Aquatic Toxicology 99(3): 320–329.CrossRefGoogle ScholarPubMed
Huggett, R.J., Neff, J.M., Stegeman, J.J., Woodin, B., Parker, K.R., and Brown, J.S. (2006). Biomarkers of PAH exposure in an intertidal fish species from Prince William Sound, Alaska: 2004–2005. Environmental Science & Technology 40(20): 6513–6517.CrossRefGoogle Scholar
Huggett, R.J., Stegeman, J.J., Page, D.S., Parker, K.R., Woodin, B., and Brown, J.S.(2003). Biomarkers in fish from Prince William Sound and the Gulf of Alaska: 1999–2000. Environmental Science & Technology 37(18): 4043–4051.CrossRefGoogle Scholar
Incardona, J.P., Carls, M.G., Day, H.L., Sloan, C.A., Bolton, J.J., Collier, T.K., and Scholz, N.L. (2009). Cardiac arrhythmia is the primary response of embryonic Pacific herring (Clupea pallasi) exposed to crude oil during weathering. Environmental Science & Technology 43(1): 201–207.CrossRefGoogle ScholarPubMed
Incardona, J.P., Carls, M.G., Teraoka, H., Sloan, C.A., Collier, T.K., and Scholz, N.L. (2005). Aryl hydrocarbon receptor-independent toxicity of weathered crude oil during fish development. Environmental Health Perspectives 113(12): 1755–1762.CrossRefGoogle ScholarPubMed
Kannan, K. and Perrotta, E. (2008). Polycyclic aromatic hydrocarbons (PAHs) in livers of California sea otters. Chemosphere 71(4): 649–655.CrossRefGoogle ScholarPubMed
McClain, J.S., Oris, J.T., Burton, G.A., and Lattier, D. (2003). Laboratory and field validation of multiple molecular biomarkers of contaminant exposure in rainbow trout (Oncorhynchus mykiss). Environmental Toxicology and Chemistry 22(2): 361–370.CrossRefGoogle Scholar
Meyer, J.N., Wassenberg, D.M., Karchner, S.I., Hahn, M.E., and Di Giulio, R.T. (2003). Expression and inducibility of aryl hydrocarbon receptor pathway genes in wild-caught killifish (Fundulus heteroclitus) with different contaminant-exposure histories. Environmental Toxicology and Chemistry 22(10): 2337–2343.CrossRefGoogle ScholarPubMed
Miles, A.K., Flint, P.L., Trust, K.A., Ricca, M.A., Spring, S.E., Arrieta, D.E., Hollmen, T., and Wilson, B.W. (2007). Polycyclic aromatic hydrocarbon exposure in Steller’s eiders (Polysticta stelleri) and harlequin ducks (Histrionicus histrionicus) in the eastern Aleutian Islands, Alaska, USA. Environmental Toxicology and Chemistry 26(12): 2694–2703.CrossRefGoogle Scholar
Miller, K.A., Assunção, M.G.L., Dangerfield, N.J., Bandiera, S.M., and Ross, P.S. (2005). Assessment of cytochrome P450 1A in harbour seals (Phoca vitulina) using a minimally-invasive biopsy approach. Marine Environmental Research 60(2): 153–169.CrossRefGoogle ScholarPubMed
Montie, E.W., Fair, P.A., Bossart, G.D., Mitchum, G.B., Houde, M., Muir, D.C.G., Letcher, R.J., McFee, W.E., Starczak, V.R., Stegeman, J.J., and Hahn, M.E. (2008). Cytochrome P450 1A1 expression, polychlorinated biphenyls and hydroxylated metabolites, and adipocyte size of bottlenose dolphins from the Southeast United States. Aquatic Toxicology 86(3): 397–412.CrossRefGoogle Scholar
Mulligan, C.J., Goldfarb, L.G., Robin, R.W., Sambuughin, N., Osier, M.V., Kittles, R.A., Goldman, D., Hesselbrock, D., and Long, J.C. (2003). Allelic variation at alcohol metabolism genes (ADH1b, ADH1c, ALDH2) and alcohol dependence in an American Indian population. Human Genetics 113(4): 325–336.CrossRefGoogle Scholar
Nebert, D.W (2005). Role of host susceptibility to toxicity and cancer caused by pesticides: cytochromes P450. Journal of Biochemical and Molecular Toxicology 19(3): 184–186.CrossRefGoogle ScholarPubMed
Nebert, D.W. and Karp, C.L. (2008). Endogenous functions of the aryl hydrocarbon receptor (AHR): Intersection of cytochrome P450 1 (CYP1)-metabolized eicosanoids and AHR biology. Journal of Biological Chemistry 283(52): 36061–36065.CrossRefGoogle ScholarPubMed
Nebert, D.W., Dalton, T.P., Okey, A.B., and Gonzalez, F.J. (2004). Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. Journal of Biological Chemistry 279(23): 23847–23850.CrossRefGoogle ScholarPubMed
Nelson, D.R (1998). Metazoan cytochrome P450 evolution. Comparative Biochemistry and Physiology – Part C: Toxicology and Pharmacology 121(1–3): 15–22.Google ScholarPubMed
Nyman, M., Raunio, H., and Pelkonen, O. (2000). Expression and inducibility of members in the cytochrome P4501 (CYP1) family in ringed and grey seals from polluted and less polluted waters. Environmental Toxicology and Pharmacology 8(4): 217–225.CrossRefGoogle ScholarPubMed
Oris, J.T. and Roberts, A.P. (2007). Statistical analysis of cytochrome P450 1A biomarker measurements in fish. Environmental Toxicology and Chemistry 26(8): 1742–1750.CrossRefGoogle Scholar
Page, D.S., Boehm, P.D., Douglas, G.S., Bence, A.E., Burns, W.A., and Mankiewicz, P.J. (1996). The natural petroleum hydrocarbon background in subtidal sediments of Prince William Sound, Alaska. Environmental Toxicology and Chemistry 15(8): 1266–1281.CrossRefGoogle Scholar
Page, D.S., Boehm, P.D., Douglas, G.S., Bence, A.E., Burns, W.A., and Mankiewicz, P.J. (1999). Pyrogenic polycyclic aromatic hydrocarbons in sediments record past human activity: A case study in Prince William Sound Alaska. Marine Pollution Bulletin 38(4): 247–260.CrossRefGoogle Scholar
Pašková, V., Adamovský, O., Pikula, J., Skočovská, B., Band, H.’ouchová, J. Horáková, P. Babica, B. Maršálek, and K. Hilscherová (2008). Detoxification and oxidative stress responses along with microcystins accumulation in Japanese quail exposed to cyanobacterial biomass. Science of the Total Environment 398(1–3): 34–47.CrossRefGoogle ScholarPubMed
Puga, A., Tomlinson, C.R., and Xia, Y. (2005). Ah receptor signals cross-talk with multiple developmental pathways. Biochemical Pharmacology 69(2): 199–207.CrossRefGoogle ScholarPubMed
Ramos-Gómez, J., Martin-Diaz, M.L., Rodríguez, A., Riba, I., and DelValls, T.Á. (2008). In situ evaluation of sediment toxicity in Guadalete Estuary (SW Spain) after exposure of caged Arenicola marina. Environmental Toxicology 23(5): 643–651.CrossRefGoogle ScholarPubMed
Ricca, M.A., Miles, A.K., Ballachey, B.E., Bodkin, J.L., Esler, D., and Trust, K.A. (2010). PCB exposure in sea otters and harlequin ducks in relation to history of contamination by the Exxon Valdez oil spill. Marine Pollution Bulletin 60(6): 861–872.CrossRefGoogle ScholarPubMed
Roberts, A.P., Oris, J.T., and Stubblefield, W.A. (2006). Gene expression in caged juvenile coho salmon (Oncorhynchys kisutch) exposed to the waters of Prince William Sound, Alaska. Marine Pollution Bulletin 52(11): 1527–1532.CrossRefGoogle Scholar
Roberts, A.P., Oris, J.T., Burton, G.A., and Clements, W.H. (2005). Gene expression in caged fish as a first-tier indicator of contaminant exposure in streams. Environmental Toxicology and Chemistry 24(12): 3092–3098.CrossRefGoogle ScholarPubMed
Schlenk, D. (1999). Necessity of defining biomarkers for use in ecological risk assessments. Marine Pollution Bulletin 39(1–12): 48–53.CrossRefGoogle Scholar
Schlenk, D., Benson, W.H., Steinert, S., Handy, R., and Depledge, M. (2008). Biomarkers. In The Toxicology of Fishes. DiGiulio, R.T. and Hinton, D.E., eds. Boca Raton, FL, USA: CRC; ISBN-10: 041524868X; ISBN-13: 9780415248686; pp. 683–723.CrossRefGoogle Scholar
Schwartz, J.A., Aldridge, B.M., Lasley, B.L., Snyder, P.W., Stott, J.L., and Mohr, F.C.(2004). Chronic fuel oil toxicity in American mink (Mustela vison): Systemic and hematological effects of ingestion of a low concentration of bunker C fuel oil. Toxicology and Applied Pharmacology 200(2): 146–158.CrossRefGoogle ScholarPubMed
Short, J.W., Springman, K.R., Lindeberg, M.R., Holland, L.G., Larsen, M.L., Sloan, C.A., Khan, C., Hodson, P.V., and Rice, S.D. (2008). Semipermeable membrane devices link site-specific contaminants to effects: Part II – A comparison of lingering Exxon Valdez oil with other potential sources of CYP1A inducers in Prince William Sound, Alaska. Marine Environmental Research 66(5): 487–498.CrossRefGoogle Scholar
Springman, K.R., Short, J.W., Lindeberg, M.R., Maselko, J.M., Khan, C., Hodson, P.V., and Rice, S.D. (2008a). Semipermeable membrane devices link site-specific contaminants to effects: Part I – Induction of CYP1A in rainbow trout from contaminants in Prince William Sound, Alaska. Marine Environmental Research 66(5): 477–486.CrossRefGoogle Scholar
Springman, K.R., Short, J.W., Lindeberg, M.R., and Rice, S.D. (2008b). Evaluation of bioavailable hydrocarbon sources and their induction potential in Prince William Sound, Alaska. Marine Environmental Research 66(1): 218–220.CrossRefGoogle Scholar
Trust, K.A., Esler, D., Woodin, B.R., and Stegeman, J.J. (2000). Cytochrome P450 1A induction in sea ducks inhabiting nearshore areas of Prince William Sound, Alaska. Marine Pollution Bulletin 40(5): 397–403.CrossRefGoogle Scholar
Walraven, J.M., Trent, J.O., and Hein, D.W. (2008). Structure-function analyses of single nucleotide polymorphisms in human N-acetyltransferase 1. Drug Metabolism Reviews 40(1): 169–184.CrossRefGoogle ScholarPubMed
Wang, Z. and Stout, S.A., eds (2007). Oil Spill Environmental Forensics: Fingerprinting and Source Identification. Burlington, MA, USA: Academic Press; ISBN-13: 9780123695239; ISBN-10: 0123695236.Google Scholar
Whyte, J.J., Jung, R.E., Schmitt, C.J., and Tillitt, D.E. (2000). Ethoxyresorufin-O-deethylase (EROD) activity in fish as a biomarker of chemical exposure. Critical Reviews in Toxicology 30(4): 347–570.CrossRefGoogle ScholarPubMed
Wilson, J.Y., Cooke, S.R., Moore, M.J., Martineau, D., Mikaelian, I., Metner, D.A., Lockhart, W.L., and Stegeman, J.J. (2005). Systemic effects of arctic pollutants in beluga whales indicated by CYP1A1 expression. Environmental Health Perspectives 113(11): 1594–1599.CrossRefGoogle ScholarPubMed
Wolkers, J., Witkamp, R.F., Nijmeijer, S.M., Burkow, I.C., de Groene, E.M., Lydersen, C., Dahle, S., and Monshouwer, M. (1998). Phase I and phase II enzyme activities in ringed seals (Phoca hispida): Characterization of hepatic cytochrome P450 by activity patterns, inhibition studies, mRNA analyses, and western blotting. Aquatic Toxicology 44(1–2): 103–115.CrossRefGoogle Scholar
Wooley, C. (2002). The myth of the “pristine environment”: Past human impacts in Prince William Sound and the Gulf of Alaska. Spill Science and Technology Bulletin, 7(1–2): 89–104.CrossRefGoogle Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×