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DNA Strand Length and EROD Activity in Relation to Two Screening Measures of Genotoxic Exposure in Great Lakes Herring Gulls

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Abstract

We collected tissues from herring gulls (Larus argentatus) nesting within and outside of the Great Lakes basin. Genotoxin exposure was assessed as fluorescent aromatic compounds (FACs) in bile and SOS Chromotest-inducing activity in muscle extracts. We determined whether these exposures were associated with decreased erythrocyte DNA strand length and/or induction of hepatic ethoxyresorufin-O-deethylase (EROD) activity. FACs were detected in all bile samples. Most muscle extracts produced a positive or marginal SOS response in the presence of S9. SOS induction potentials were strongly associated with dietary trophic level. The median molecular length of DNA isolated from erythrocytes for 14 of 17 adult and 10 of 11 prefledgling collections was reduced compared to the modal class for their respective age group suggesting widespread DNA damage. DNA damage was greatest in gulls from Saginaw Bay, Lake Huron. Median EROD activity in both adults and prefledglings from remote locations was significantly lower than that of gulls from the lower Great Lakes and was not associated with concentrations of benzo[a]pyrene (B[a]P)-like FACs. Our results indicate Great Lakes herring gulls were exposed to genotoxins and Ah-receptor activating agents in biologically significant concentrations in the early 1990s. These agents appear to be persistent bioaccumulative compounds and/or their metabolites.

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References

  • Ali, F., Lazar, R., Haffner, D. and Adeli, K. (1993). Development of a rapid and simple genotoxicity assay using a brown bullhead fish cell-line: application to toxicological surveys of sediments in the Huron-Erie corridor. J. Great Lakes Res. 19, 342–51

    Article  CAS  Google Scholar 

  • Anderson, S., Sadinski, W., Shugart, L., Brussard, P., Depledge, M., Ford, T., Hose, J., Stegeman, J., Suk, W., Wirgin, I. and Wogan G. (1994). Genetic and molecular toxicology: a research framework. Environ. Health Perspect. 102(Suppl. 12), 3–8

    Google Scholar 

  • Arcand-Hoy, L.D. and Metcalfe, C.D. (1999). Biomarkers of exposure of brown bullheads (Ameiurus nebulosus) to contaminants in the lower Great Lakes, North America. Environ. Toxicol. Chem. 18, 740–49

    Article  CAS  Google Scholar 

  • Avery, E.L., Dunstan, R.H. and Nell, J.A. (1996). The detection of pollutant impact in marine environments: condition index, oxidative DNA damage, and their associations with metal bioaccumulation in the Sydney rock oyster Saccostrea commercialis. Arch. Environ. Contamin. Toxicol. 31, 192–98

    Article  CAS  Google Scholar 

  • Black, M.C., Ferrell, J.R., Horning, R.C. and Martin, L.K. Jr. (1996). DNA strand breakage in freshwater mussels (Anodonta grandis) exposed to lead in the laboratory and field Environ. Toxicol. Chem. 15, 802–8

    Article  CAS  Google Scholar 

  • Borlak, J., Hock, A., Hansen, T. and Richter, E. (2003). DNA adducts in cultures of polychlorinated biphenyl-treated human hepatocytes. Toxicol. Appl. Pharmacol. 188, 81–91

    Article  PubMed  CAS  Google Scholar 

  • Broman, D., Naf, C., Lundbergh, I. and Zebuhr, Y., (1990). An in situ study on the distribution, biotransformation and flux of polycyclic aromatic hydrocarbons (PAHs) in an aquatic food chain (Seston-Mytilus edulis L.-Somateria mollissima L.) from the Baltic: an ecotoxicological perspective. Environ. Toxicol. Chem. 9, 429–42

    Article  CAS  Google Scholar 

  • Butterworth, F.M., Pandey, P., McGowen, R.M., Ali-Sadat, S. and Walia, S. (1995). Genotoxicity of polychlorinated biphenyls (PCBs): recombinogenesis by biotransformation products. Mut. Res. 342, 61–69

    Article  CAS  Google Scholar 

  • Campbell, L.M., Muir, D.C.G., Whittle, D.M., Backus, S., Norstrom, R.J. and Fisk, A.T. (2003). Hydroxylated PCBs and other chlorinated phenolic compounds in lake trout (Salvelinus namaycush) blood plasma from the Great Lakes region Environ. Sci. Technol. 37, 1720–5

    Article  CAS  Google Scholar 

  • Custer, T.W., Bickham, J.W., Lyne, T.B., Lewis, T., Ruedas, L.A., Custer, C.M. and Melancon, M.J. (1994). Flow cytometry for monitoring contaminant exposure in black-crowned night-herons. Arch. Environ. Contamin. Toxicol. 27, 176–9

    Article  CAS  Google Scholar 

  • Custer, T.W., Custer, C.M., Hines, R.K., Sparks, D.W., Melancon, M.J., Hoffman, D.J., Bickham, J.W. and Wickliffe, J.K. (2000). Mixed-function oxygenases, oxidative stress, and chromosomal damage measured in lesser scaup wintering on the Indiana Harbor Canal. Arch. Environ. Contamin. Toxicol. 38, 522–9

    Article  CAS  Google Scholar 

  • DeVault, D.S., Hesselberg, R., Rodgers, P.W. and Feist, T.J. (1996). Contaminant trends in lake trout and walleye from the Laurentian Great Lakes. J. Great Lakes Res. 22, 884–95

    CAS  Google Scholar 

  • Ellenton, J.A. and McPherson, M.F. (1983). Mutagenicity studies on herring gulls from different locations in the Great Lakes. I. Sister chromatid exchange rates in herring gull embryos. J. Toxicol. Environ. Health 12, 317–24

    CAS  Google Scholar 

  • Ellenton, J.A., McPherson, M.F. and Maus, K.L. (1983). Mutagenicity studies on herring gulls from different locations on the Great Lakes. II. Mutagenic evaluations of extracts of herring gull eggs in a battery of in vitro mammalian and microbial assays. J. Toxicol. Environ. Health. 12, 325–36

    PubMed  CAS  Google Scholar 

  • Fox, G.A., Grasman, K.A., Hobson, K.A., Williams, K., Jeffrey, D. and Hanbidge, B. (2002). Contaminant residues in tissues of adult and prefledfled herring gulls from the Great Lakes in relation to diet in the early 1990s. J. Great Lakes Res. 28, 643–63

    CAS  Google Scholar 

  • Gorsline, J. and Holmes, W.N. (1981) Effects of petroleum on adrenocortical activity and on hepatic naphthalene metabolizing activity in mallard ducks (Anas platyrhynchos). Arch. Environ. Contamin. Toxicol. 10, 765–77

    Article  CAS  Google Scholar 

  • Grasman, K.A. Scanlon, P.F. and Fox, G.A. (1998). Reproductive and physiological effects of environmental contaminants in fish-eating birds of the Great Lakes: A review of historical trends. Environ. Monitor. Assessment 53, 117–45

    Article  CAS  Google Scholar 

  • Honey, S., O’Keefe, P., Drahushuk, A.T., Olson, J.R., Kumar, S. and Sikka, H.C. (2000). Metabolism of benzo(a)pyrene by duck liver microsomes. Compar. Biochem. Physiol. 126C, 285–92

    CAS  Google Scholar 

  • International Air Quality Advisory Board (2003). Report of the IAQAB to the International Joint Commission. 2001–2003 Priorities and Progress Under the Great Lakes Water Quality Agreement. Windsor, ON and Washington, DC: International Joint Commission

  • Johnston, E.P. and Baumann, P.C. (1989). Analysis of fish bile by HPLC – fluorescence to determine environmental exposure to benzo(a)pyrene. Hydrobiologia 188/189, 561–6

    Google Scholar 

  • Jones, D.R. and Johanson, K. (1972). The blood vascular system of birds. In D.S. Farner, J.R. King (eds). Avian Biology, (II), pp. 158–285. New York, NY: Academic Press

    Google Scholar 

  • Kannan, K., Hilscherova, K., Imagawa, T., Yamashita, N., Williams, L.L. and Giesy, J.P. (2001). Polychlorinated naphthalenes, -biphenyls, -dibenzo-p-dioxins, and –dibenzofurans in double-crested cormorants and herring gulls from Michigan waters of the Great Lakes. Environ. Sci. Technol. 35, 441–7

    Article  PubMed  CAS  Google Scholar 

  • Kannan, K., Yamashita, N., Decoen, W., Khim, J.S., Day, R.M., Summer, C.L. and Giesy, J.P., (2000). Polychlorinated naphthalenes and polychlorinated biphenyls in fishes from Michigan waters including the Great Lakes. Environ. Sci. Technol. 34, 566–72

    Article  CAS  Google Scholar 

  • Kennedy, S.W., Fox, G.A., Jones, S.P. and Trudeau, S. (2003). Hepatic EROD activity is not a useful biomarker of polychlorinated biphenyl exposure in the adult herring gull (Larus argentatus). Ecotoxicology 12, 153–61

    Article  PubMed  CAS  Google Scholar 

  • Krahn, M.M., Burrows, D.G., MacLeod, Jr. W.D. and Malins, D.C. (1987). Determination of individual metabolites of aromatic compounds in hydrolyzed bile of English sole (Parophrys vetulus) from polluted sites in Puget Sound, Washington. Arch. Environ. Contamin. Toxicol. 16, 511–22

    Article  CAS  Google Scholar 

  • Krahn, M.M., Kittle, L.J. Jr. and MacLeod, W.D. Jr. (1986a). Evidence for exposure of fish to oil spilled into the Columbia River. Mar. Environ. Res. 20, 291–8

    Article  CAS  Google Scholar 

  • Krahn, M.M., Myers, M.S., Burrows, D.G. and Malins, D.C. (1984). Determination of metabolites of xenobiotics in the bile of fish from polluted waterways. Xenobiotica 14, 633–46

    Article  PubMed  CAS  Google Scholar 

  • Krahn, M.M., Rhodes, L.D., Myers, M.S., Moore, L.K., MacLeod, W.D. Jr. and Malins, D.C. (1986b). Associations between metabolites of aromatic compounds in bile and the occurrence of hepatic lesions in English sole (Parophrys vetulus) from Puget Sound, Washington. Arch. Environ. Contamin. Toxicol. 15, 61–7

    Article  CAS  Google Scholar 

  • Landahl, J.T., McCain, B.B., Myers, M.S., Rhodes, L.D. and Brown, D.W. (1990). Consistent associations between hepatic lesions in English sole (Parophrys vetulus) and polycyclic aromatic hydrocarbons in bottom sediment. Environ. Health Perspect 89, 195–203

    Article  PubMed  CAS  Google Scholar 

  • Leadley, T.A., Arcand-Hoy, L.D., Haffner, G.D. and Metcalfe, C.D. (1999). Fluorescent aromatic hydrocarbons in bile as a biomarker of exposure of brown bullheads (Ameiurus nebulosus) to contaminated sediments. Environ. Toxicol. Chem. 18, 750–5

    Article  Google Scholar 

  • Li, H., Drouillard, K.G., Bennett, E., Haffner, G.D. and Letcher, R.J. (2003). Plasma-associated halogenated phenolic contaminants in benthic and pelagic fish species from the Detroit River. Environ. Sci. Technol. 37, 832–9

    Article  CAS  Google Scholar 

  • Maccubbin, A.E., Chidambaram, S. and Black, J.J. (1988). Metabolites of aromatic hydrocarbons in the bile of brown bullheads (Ictalurus nebulosus). J. Great Lakes Res. 14, 101–8

    CAS  Google Scholar 

  • Maness, T.J. and Emslie, S.D. (2001). An analysis of possible genotoxic exposure in adult and juvenile royal terns in North Carolina, USA. Waterbirds 24, 352–60

    Google Scholar 

  • Metcalfe, C.D., Balch, G.C., Cairns, V.W., Fitzsimons, J.D. and Dunn, B.P. (1990). Carcinogenic and genotoxic activity of extracts from contaminated sediments in western Lake Ontario. Sci. Total Environ. 94, 125–41

    Article  CAS  Google Scholar 

  • Meyer, J.N., Nacci, D.E. and Di Giulio, R.T. (2002). Cytochrome P4501A (CYP1A) in killifish (Fundulus heteroclitus): heritability of altered expression and relationship to survival in contaminated sediments. Toxicol. Sci. 68, 69–81

    Article  PubMed  CAS  Google Scholar 

  • Nacci, D.E., Kohan, M., Pelletier, M. and George, E. (2002). Effects of benzo[a]pyrene exposure on a fish population resistant to the toxic effects of dioxin-like compounds. Aqua. Toxicol. 57, 203–15

    Article  CAS  Google Scholar 

  • Pastor, N., López-Lázaro, M., Tella, J.L., Baos, R., Hiraldo, F. and Cortés, F. (2001). Assessment of genotoxic damage by the comet assay in white storks (Ciconia ciconia) after the Donana. Ecol. Disaster Mutagen. 16, 219–24

    Article  PubMed  CAS  Google Scholar 

  • Peakall, D.B., Jeffrey, D.A. and Boersma, D. (1987). Mixed-function oxidase activity in seabirds and its relationship to oil pollution. Compar. Biochem. Physiol. 88C, 151–4

    Article  CAS  Google Scholar 

  • Peakall, D.B., Norstrom, R.J., Jeffery, D.A. and Leighton, F.A. (1989). Induction of hepatic mixed function oxidases in the herring gull (Larus argentatus) by Prudhoe Bay crude oil and its fractions. Compar. Biochem. Physiol. 94C, 461–4

    Article  CAS  Google Scholar 

  • Peterson, G.L. (1977). A simplification of the protein assay method of Lowry et al. Anal. Biochem. 83, 346–56

    Article  PubMed  CAS  Google Scholar 

  • Pohl, R.J. and Fouts, J.R. (1980). A rapid method for assaying the metabolism of 7-ethoxyresorufin by microsomal subscellular fractions. Anal. Biochem. 107, 150–5

    Article  PubMed  CAS  Google Scholar 

  • Pyykkö, K. (1983). Characterization and stability of rat liver microsomes isolated by a rapid gel filtration method. Acta Pharmacol. Toxicol. 52, 39–46

    Article  Google Scholar 

  • Quillardet, P., Huisman, O., D’Ari, R. and Horfnung, M., (1982). SOS Chromostest, a direct assay of induction of an SOS function in Escherichia coli K-12 to measure genotoxicity. Proc. Natl. Acad. Sci. USA 79, 5971–5

    Article  PubMed  CAS  Google Scholar 

  • Schmutz, J.A., and Hobson, K.A. (1998). Geographical, temporal, and age-specific variation in diets of glaucous gulls in western Alaska. Condor 100, 119–30

    Article  Google Scholar 

  • Schoen, D.J., Brownstein, J.S. and White, P.A. (2002). Mutation load in natural populations of the sensitive fern Onoclea sensibilis exposed to soil mutagens. Ecol. Appl. 12, 124–37

    Article  Google Scholar 

  • Shugart L.R., (2000). DNA damage as a biomarker of exposure Ecotoxicology 9:329–40

    Article  CAS  Google Scholar 

  • Shugart, L., Bickham, J., Jackim, G., McMahon, G., Ridley, W., Stein, J. and Steinert, S. (1992). DNA alterations. In R.J. Huggett, R.A. Kimerle, P.M. Mehrle Jr., H.L. Bergman (eds). Biomarkers. Biochemical, Physiological, and Histological Markers of Anthropogenic Stress, pp. 125–53. Chelsea, MI, USA: Lewis Publishers

    Google Scholar 

  • Sinkevicius, S., and Lekevicius, R. (1990). The analysis of the influence of DDT, DDE, DDD, DDA and Dicofol on marrow cells of the Black-headed gull. Acta Ornithol. Lituanica 2, 81–9

    Google Scholar 

  • Stapleton, H.M., Masterson, C., Skubinna, J., Ostrom, P., Ostrom, N.E. and Baker, J.E. (2001). Accumulation of atmospheric and sedimentary PCBs and toxaphene in a Lake Michigan food web. Environ. Sci. Technol. 35, 3287–93

    Article  PubMed  CAS  Google Scholar 

  • Stein, J.E., Hom, T., Collier, T.K., Brown, D.W. and Varanasi, U. (1995). Contaminant exposure and biochemical effects in outmigrant juvenile chinook salmon from urban and nonurban estuaries of Puget Sound, Washington. Environ. Toxicol. Chem. 14, 1019–29

    Article  CAS  Google Scholar 

  • Theodorakis, C.W., D’Surney, S.J. and Shugart, L.R. (1994). Detection of genotoxic insult as DNA strand breaks in fish blood cells by agarose gel electrophoresis. Environ. Toxicol. Chem. 13, 1023–31

    Article  CAS  Google Scholar 

  • Theodorakis, C.W., Elbl, T. and Shugart, L.R. (1999). Genetic ecotoxicology IV: Survival and DNA strand breakage is dependent on genotype in radionuclide-exposed mosquitofish. Aqua. Toxicol. 45, 279–91

    Article  CAS  Google Scholar 

  • Tice, R.R. (1995). Application of the single cell gel assay to environmental biomonitoring for genotoxic pollutants. In F.M. Butterworth et al., (eds). Biomonitors and Biomarkers as Indicators of Environmental Change, pp. 69–79. NY: Plenum Press

    Google Scholar 

  • Trust, K.A., Fairbrother, A. and Hooper, M.J. (1994). Effects of 7,12-dimethylbenz(a)anthracene on immune function and mixed-function oxygenase activity in the European starling. Environ. Toxicol. Chem. 13, 821–30

    Article  CAS  Google Scholar 

  • Wahba, Z.Z., Lawson, T.A. and Stohs, S.J. (1988). Induction of hepatic DNA single strand breaks in rats by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Cancer Lett. 29, 281–6

    Article  Google Scholar 

  • Walker, G.C. (1984). Mutagenesis and inducible responses to deoxyribonucleic acid damage in E. coli. Microbiol. Rev. 48, 60–93

    PubMed  CAS  Google Scholar 

  • White, P.A., Blaise, C. and Rasmussen, J.B. (1997). Detection of genotoxic substances in bivalve mollusks from the Saguenay Fjord (Canada), using the SOS chromotest Mutation Res. 392, 277–300

    PubMed  CAS  Google Scholar 

  • White, P.A. and Rasumussen, J.B. (1996). SOS chromotest results in a broader context Empirical relationships between genotoxic potency, mutagenic potency, and carcinogenic potency. Environ. Mol. Mutagenesis 27, 270–305

    Article  CAS  Google Scholar 

  • White, P.A., Rasmussen, J.B. and Blaise, C. (1996). A semi-automated, microplate version of the SOS Chromotest for the analysis of complex environmental extracts. Mut. Res. 360, 51–74

    CAS  Google Scholar 

  • White, P.A., Rasmussen, J.B. and Blaise C. (1998a). Genotoxic substances in the St. Lawrence system I: industrial genotoxins sorbed to particulate matter in the St. Lawrence, St. Maurice, and Saguenay Rivers (Canada). Environ. Toxicol. Chem. 17, 286–303

    Article  CAS  Google Scholar 

  • White, P.A., Rasmussen, J.B. and Blaise, C. (1998b). Genotoxic substances in the St. Lawrence River system II: extracts of fish and macroinvertebrates from the St. Lawrence and Saguenay Rivers (Canada). Environ. Toxicol. Chem. 17, 304–16

    Article  CAS  Google Scholar 

  • White, P.A., Robitaille, S. and Rasmussen, J.B. (1999). Heritable reproductive effects of benzo[a]pyrene on the fathead minnow (Pimephales promelas). Environ. Toxicol. Chem. 18, 1843–7

    Article  CAS  Google Scholar 

  • Wickliffe, J.K. and Bickham, J.W. (1998). Flow cytometric analysis of hematocytes from brown pelicans (Pelecanus occidentalis) exposed to planar halogenated hydrocarbons and heavy metals. Bull. Environ. Contamin. Toxicol. 61,239–46

    Article  CAS  Google Scholar 

  • Yang, X., Peterson, D.S., Baumann, P.C. and Lin, E.L.C. (2003). Fish biliary PAH metabolites estimated by fished-wavelength fluorescence as an indicator of environmental exposure and effects. J. Great Lakes Res. 29,116–23

    CAS  Google Scholar 

  • Yauk, C.L., Fox, G.A., McCarry, B.E. and Quinn, J.S. (2000). Induced microsatelite mutations in herring gulls (Larus argentatus) living near steel mills. Mut. Res. 452, 211–3

    CAS  Google Scholar 

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Acknowledgments

We thank K. and S. Grasman, D. Jeffrey, B. Hanbidge, K. Williams, J. Ludwig, T. Erdman, C. Hebert, P. Ewins, C. Weseloh, B. Iko, H. Auman, H. Morrison, and N. Mahony for assistance with collection of gull tissues. The Bowdoin College Field Station and BASF provided access to Kent and Fighting Islands, respectively. H. Won measured the organochlorine contaminants, J. Moisey the NOPCBs, PCDDs and PCDFs, and E. Neugebauer the metals. G. Perry conducted the stable isotope analyses. J. Stein of NOAA provided fish bile samples for validation of our FACs methodology. L. Beneditti prepared the map. This project received funding from the Great Lakes Action Plan. Paul White acknowledges financial support in the form of an NSERC postgraduate scholarship and postdoctoral fellowship.

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  1. Canadian Wildlife Service – National Wildlife Research Centre, Carleton University, K1A 0H3, Ottawa, ON, Canada

    Glen A. Fox, Suzanne Trudeau, Laird J. Shutt & Sean W. Kennedy

  2. Mutagenesis Section, Safe Environments Program, Health Canada, Tunney’s Pasture 0803a, K1A 0L2 , Ottawa, ON, Canada

    Paul A. White

  3. Aquatic Toxicology Section, The Institute of Environmental and Human Health, Department of Environmental Toxicology, Texas Tech University, Lubbock, TX , 79409-1163, USA

    Chris Theodorakis

  4. Canadian Wildlife Service – Ontario Region, Environment Canada, 867 Lakeshore Rd, L7R 4A6, Burlington, ON, Canada

    Kim J. Fernie

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  1. Glen A. Fox
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Fox, G.A., White, P.A., Trudeau, S. et al. DNA Strand Length and EROD Activity in Relation to Two Screening Measures of Genotoxic Exposure in Great Lakes Herring Gulls. Ecotoxicology 14, 527–544 (2005). https://doi.org/10.1007/s10646-005-0002-9

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