, Volume 12, Issue 1–4, pp 183–197 | Cite as

Biological Effects of Marine PCB Contamination on Black Guillemot Nestlings at Saglek, Labrador: Liver Biomarkers

  • Zou Zou A. Kuzyk
  • Neil M. BurgessEmail author
  • Jason P. Stow
  • Glen A. Fox


Black guillemots (Cepphus grylle) in Saglek Bay, Labrador have elevated polychlorinated biphenyl (PCB) concentrations due to marine sediment contamination around a former military site. We measured liver biomarkers and ΣPCB concentrations in 31 nestlings from three PCB-exposure groups: Reference group (range: 15–46 ng/g liver, wet wt.), moderately exposed Islands group (24–150 ng/g), and highly exposed Beach group (170–6200 ng/g). Biomarker responses were dose-dependent and in some cases sex-dependent. Livers of female Beach nestlings were enlarged 36% relative to Reference females. In both sexes, Beach nestlings had liver ethoxyresorufin-O-deethylase (EROD) activities elevated 79% and liver retinol concentrations reduced 47%. Retinyl palmitate concentrations were reduced 50% but only among female nestlings. Island nestlings also exhibited EROD induction (57%) and reductions in retinol and retinyl palmitate concentrations (28 and 58%, respectively). Liver lipid content increased with ΣPCBs in both sexes, and correlated with liver mass in males. Malic enzyme activity and porphyrin concentrations showed little association with ΣPCBs. Although similar associations between liver biomarkers and organochlorine exposure in fish-eating birds are well documented, typically exposures involve multiple contaminants and there is uncertainty about specific PCB effects. Our findings indicate that liver biomarkers respond to relatively low PCB exposures (∼73 ng/g liver) in guillemots.

polychlorinated biphenyls black guillemot cepphus grylle liver biomarkers Saglek Labrador 


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  1. Agency for Toxic Substances and Disease Registry (ATSDR) (2000). Toxicological Profile for Polychlorinated Biphenyls (PCBs). Atlanta: US Dept. of Health and Human Services, Public Health Service.Google Scholar
  2. Bishop, C.A., Mahony, N.A., Trudeau, S. and Pettit, K.E. (1999). Reproductive success and biochemical effects in tree swallows (Tachycineta bicolor) exposed to chlorinated hydrocarbon contaminants in wetlands of the Great Lakes and St. Lawrence river basin, USA and Canada. Environ. Toxicol. Chem. 18, 263-71.Google Scholar
  3. Bradstreet, M.S.W. and Brown, R.G.B. (1985). Feeding ecology of the Atlantic Alcidae. In D.N. Nettleship and T.R. Birkhead (eds) The Atlantic Alcidae, pp. 263-318. London and New York: Academic Press.Google Scholar
  4. Bright, D.A., Dushenko, D.W., Grundy, S.L. and Reimer, K.J. (1995a). Effects of local and distant contaminant sources: polychlorinated biphenyls and other organochlorines in bottom-dwelling animals from an Arctic estuary. Sci. Tot. Environ. 160/161, 265-83.Google Scholar
  5. Bright, D.A., Grundy, S.L. and Reimer, K.J. (1995b). Diffential bioaccumulation of non-ortho-substituted and other PCB congeners in coastal arctic invertebrates and fish. Environ. Sci. Tech. 29, 2504-12.Google Scholar
  6. Cairns, D.K. (1980). Nesting density, habitat structure and human disturbance as factors in Black Guillemot reproduction. Wilson Bull. 92, 352-61.Google Scholar
  7. Cecil, H.C., Harris, S.J., Bitman, J. and Fries, F.F. (1973). Polychlorinated biphenyl-induced decrease in liver vitamin A in Japanese quail and rats. Bull. Environ. Contam. Toxicol. 9, 179-85.Google Scholar
  8. Custer, T.W., Custer, C.M., Hines, R.K., Gutreuter, S., Stronborg, K.L., Allen, P.D. and Melancon, M.L. (1999). Organochlorine contaminants and reproductive success of double-crested cormorants from Green Bay, Wisconsin, USA. Environ. Toxicol. Chem. 18, 1209-17.Google Scholar
  9. Custer, T.W., Hines, R.K., Melancon, M.J., Hoffman, D.J., Wickliffe, J.K., Bickham, J.W., Martin, J.W. and Henshel, D.S. (1997). Contaminant concentrations and biomarker response in great blue heron eggs from 10 colonies on the upper Mississippi river, USA. Environ. Toxicol. Chem. 16, 260-71.Google Scholar
  10. Dahlgren, R.B., Bury, R.J., Linder, R.L. and Reideinger, F.R. Jr (1972a). Residue levels and histopathology in pheasants given polychlorinated biphenyls. J. Wildl. Manag. 36, 524-33.Google Scholar
  11. Dahlgren, R.B., Linder, R.L. and Carlson, C.W. (1972b). Polychlorinated biphenyls: their effects on penned pheasants. Environ. Health Perspect. 1, 89-101.Google Scholar
  12. Dahlgren, R.B., Linder, R.L. and Tucker, W.L. (1972c). Effects of stress on pheasants previously given polychlorinated biphenyls. J. Wildl. Manag. 36, 974-8.Google Scholar
  13. de March, B.G.E., de Wit, C.A. and Muir, D.C.G. (1998). Persistent organic pollutants. In S.J. Wilson, J.L. Murray and H.P. Huntington (eds), AMAP Assessment Report: Arctic Pollution Issues, pp. 183-371. Oslo: Arctic Montoring and Assessment Programme.Google Scholar
  14. Elliott, J.E., Kennedy, S.W., Jeffrey, D. and Shutt, L. (1991). Polychlorinated biphenyl (PCB) effects on hepatic mixed function oxidases and porphyria in birds: II. American kestrels. Comp. Biochem. Physiol. C99, 141-5.Google Scholar
  15. Elliott, J.E., Kennedy, S.W., Peakall, D.B. and Won, H. (1990). Polychlorinated biphenyl (PCB) effects on hepatic mixed function oxidases and porphyria in birds: I. Japanese quail. Comp. Biochem. Physiol. 1, 205-10.Google Scholar
  16. Elliott, J.E., Norstrom, R.J., Lorenzen, A., Hart, L.E., Pilibert, H., Kennedy, S.W., Stegeman, J.J., Bellward, G.D. and Cheng, K.M. (1996). Biological effects of polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls in bald eagle (Haliaetetus leucocephalis) chicks. Environ. Toxicol. Chem. 15, 782-93.Google Scholar
  17. Environmental Sciences Group (ESG) (1999). Saglek Food Chain Study Results Update. Kingston: Royal Military College of Canada.Google Scholar
  18. Fletcher, N., Hanberg, A. and Hakansson, H. (2001). Hepatic vitamin A depletion is a sensitive marker of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) exposure in four rodent species. Toxicol. Sci. 62, 166-75.Google Scholar
  19. Fox, G.A. (1993). What have biomarkers told us about the effects of contaminants of the health of fish-eating birds in the Great Lakes? The theory and a literature review. J. Gt. Lakes Res. 19, 722-36.Google Scholar
  20. Fox, G.A. (2001). Wildlife as sentinels of human health effects in the Great Lakes-St. Lawrence basin. Environ. Health Perspect. 109, 853-61.Google Scholar
  21. Fox, G.A., Grasman, K.A., Hobson, K.A., Williams, K., Jeffrey, D. and Hanbidge, B. (2002). Contaminant residues in tissues of adult and prefledged herring gulls from the Great Lakes in relation to diet in the early 1990s. J. Gt. Lakes Res. (in press) 28, 643-63.Google Scholar
  22. Fox, G.A., Kennedy, S.W., Norstrom, R.J. and Wigfield, D.C. (1988). Porphyria in herring gulls: a biochemical response to chemical contamination of Great Lakes food chains. Environ. Toxicol. Chem. 7, 831-9.Google Scholar
  23. Fox, G.A., Trudeau, S., Won, H. and Grasman, K.A. (1998). Monitoring the elimination of persistent toxic substances from the Great Lakes: chemical and physiological evidence from adult herring gulls. Environ. Monitor Assess. 53, 147-68.Google Scholar
  24. Gilbertson, M. and Fox, G.A. (1977). Pollutant-associated embryonic mortality of Great Lakes herring gulls. Environ. Pollut. 12, 211-16.Google Scholar
  25. Gilbertson, M., Kubiak, T., Ludwig, J. and Fox, G. (1991). Great Lakes embryo mortality, edema, and deformities syndrome (GLEMEDS) in colonial fish-eating birds: similarity to chick-edema disease. J. Toxicol. Environ. Health. 33, 455-520.Google Scholar
  26. Grasman, K.A. and Scanlon, P.F. (1995). Effects of acute lead ingestion and diet on antibody and T-cell-mediated immunity in Japanese quail. Arch. Environ. Contam. Toxicol. 28, 161-7.Google Scholar
  27. Grasman, K.A., Scalon, 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 Assess. 53, 117-45.Google Scholar
  28. Grasman, K.A., Scalon, P.F. and Fox, G.A. (2000). Geographic variation in hematological variables in adult and prefledgling herring gulls (Larus argentatus) and possible associations. Arch. Environ. Contam. Toxicol. 38, 244-53.Google Scholar
  29. Grundy, S.L., Bright, D.A., Dushenko, W.T., Dodd, M., Englander, S., Johnston, K., Pier, D. and Reimer, K.J. (1997). Dioxin and furan signatures in northern Canadian soils: correlation to source signatures using multivariate unmixing techniques. Chemosphere 34, 1203-19.Google Scholar
  30. Hahn, M.E., Woodward, B.L., Stegeman, J.J. and Kennedy, S.W. (1996). Rapid assessment of induced cytochrome P4501A protein and catalytic activity in fish hepatoma cells grown in multiwell plates: response to TCDD, TCDF, and two planar PCBs. Environ. Toxicol. Chem. 15, 582-91.Google Scholar
  31. Hoffman, D.J., Rattner, B.A., Sileo, L., Docherty, D. and Kubiak, T.J. (1987). Embryotoxicity, teratogenicity, and aryl hydrocarbon hydroxylase activity in Forster's terns on Green Bay, Lake Michigan. Environ. Res. 42, 176-84.Google Scholar
  32. Hoffman, D.J., Rice, C.P. and Kubiak, T.J. (1996). PCBs and dioxins in birds. In W.N. Beyer, G.H. Heinz and A. Walters Redmon (eds) Environmental Contaminants in Wildlife: Interpreting Tissue Concentrations, pp. 165-207. Boca Raton: Lewis Publishers.Google Scholar
  33. Hoffman, D.J., Smith, G.J. and Rattner, A. (1993). Biomarkers of contaminant exposure in common terns and black-crowned night-herons in the Great Lakes. Environ. Toxicol. Chem. 12, 1095-103.Google Scholar
  34. Kakela, A., Kakela, R., Hyvarinen, H. and Asikainen, J. (2002). Vitamins A1 and A2 in hepatic tissue and subcellular fractions in mink feeding on fish-based diets and exposed to Aroclor 1242. Environ. Toxicol. Chem. 21, 397-403.Google Scholar
  35. Kennedy, S.W., Fox, G.A., Jones, S.P. and Trudeau, S. (2002). Ethoxyresorufin-O-deethylase activity is not a useful biomarker of total polychlorianted biphenyl exposure in the herring gull (Larus argentatus). Ecotoxicology this issue.Google Scholar
  36. Kennedy, S.W., Fox, G.A., Trudeau, S., Bastien, L.J. and Jones, S.P. (1998). Highly carboxylated porphyrin concentration: a biochemical marker of PCB exposure in herring gulls. Mar. Environ. Res. 46, 65-9.Google Scholar
  37. Kennedy, S.W. and James, C.A. (1993). Improved method to extract and concentrate porphyrins from liver tissue for analysis by high-performance liquid chromatography. J. Chromatog. Biomed. Appl. 619, 127-32.Google Scholar
  38. Kennedy, S.W. and Jones, S.P. (1994). Simultaneous measurement of cytochrome P4501A catalytic activity and total protein concentration with a fluorescence plate reader. Anal. Biochem. 222, 217-23.Google Scholar
  39. Kennedy, S.W., Lorenzen, A., Jones, S.P., Hahn, M.E. and Stegeman, J.S. (1996). Cytochrome P4501A induction in avian hepatocyte cultures: a promising approach for predicting the sensitivity of avian species to toxic effects of halogenated aromatic hydrocarbons. Toxicol. Appl. Pharmacol. 141, 214-30.Google Scholar
  40. Kimbrough, R.D., Linder, R.E. and Gaines, T.B. (1972). Morphological changes in livers of rats fed polychlorinated biphenyls. Light microscopy and ultrastructure. Arch. Environ. Health 25, 354-64.Google Scholar
  41. Kuzyk, Z.A. (2000). Bioaccumulation of PCBs from contaminated sediments in a coastal marine ecosystem of northern Labrador. M.Sc. Thesis, Queen's University, Kingston, ON.Google Scholar
  42. Lorenzen, A., Moon, T.W., Kennedy, S.W. and Fox, G.A. (1999). Relationships between environmental organochlorine contaminant residues, plasma corticosterone concentrations, and intermediary metabolic enzyme activities. Environ. Health Perspect. 107, 179-86.Google Scholar
  43. McKinney, J.D., Chae, K., Gupta, B.N., Moore, J.A. and Goldstein, J.A. (1976). Toxicological assessment of hexachlorobiphenyl isomers and 2,3,7,8-tetrachlorodibenzofuran in chicks: I. Relationship of chemical parameters. Toxicol. Appl. Pharmacol. 36, 65-80.Google Scholar
  44. Muir, D.C.G., Braune, B., DeMarch, B., Norstrom, R.J., Wagemann, R., Lockhart, L., Hargrave, B.T., Bright, D.A., Addison, R., Payne, J.F. and Reimer, K.J. (1999). Spatial and temporal trends and effects of contaminants in the Canadian Arctic marine ecosystem: a review. Sci. Tot. Environ. 230, 83-144.Google Scholar
  45. Niimi, A.J. (1996). PCBs in aquatic organisms. In W.N. Beyer, G.H. Heinz and A. Walters Redmon (eds) Environmental Contaminants in Wildlife: Interpreting Tissue Concentrations, pp. 117-52. Boca Raton: Lewis Publishers.Google Scholar
  46. Peakall, D.B., Hallett, D., Miller, D.S., Buter, R.G. and Kinter, W.B. (1980). Effects of ingested crude oil on black guillemots: a combined field and laboratory study. Ambio 9, 28-30.Google Scholar
  47. Prichard, A.K., Roby, D.D., Bowyer, R.T. and Duffy, L.K. (1997). Pigeon guillemots as a sentinel species: a dose-response experiment with weathered oil in the field. Chemosphere 35, 1531-48.Google Scholar
  48. Rattner, B.A., Melancon, M.J., Custer, T.W., Hothem, R.L., King, K.A., LeCaptain, L.J., Spann, J.W., Woodin, B.R. and Stegeman, J.J. (1993). Biomonitoring environmental contamination with pipping black-crowned night heron embryos: induction of cytochrome P450. Environ. Toxicol. Chem. 12, 1719-32.Google Scholar
  49. Rattner, B.A., Melancon, M.J., Custer, T.W. and Hothem, R.L. (1996). Cytochrome P450 and contaminant concentrations in nestling black-crowned night-herons and their interrelation with sibling embryos. Environ. Toxicol. Chem. 15, 715-21.Google Scholar
  50. Rousseeuw, P.J. and Leroy, A.M. (1987). Robust Regression and Outlier Detection. New York: J. Wiley and Sons.Google Scholar
  51. Sanderson, T.J., Kennedy, S.W. and Giesy, J.P. (1998). In vitro induction of ethoxyresorufin-O-deethylase and porphyrins by halogenated aromatic hydrocarbons in avian primary hepatocytes. Environ. Toxicol. Chem. 17, 2006-18.Google Scholar
  52. Scheuhammer, A.M. and Bond, D. (1991). Factors affecting the determination of total mercury in biological samples by continuous-flow cold vapor atomic absorption spectrophotometry. Biol. Trace Elem. Res. 31, 119-29.Google Scholar
  53. Spear, P.A., Moon, T.W. and Peakall, D.B. (1986). Liver retinoid concentrations in natural populations of herring gulls (Larus argentatus) contaminated by 2,3,7,8-tetrachlorodibenzo-p-dioxin and in ring doves (Streptopelia risoria) injected with a dioxin analogue. Can. J. Zool. 64, 204-8.Google Scholar
  54. Spear, P.A., Bourbonnais, D.H., Peakall, D.B. and Moon, T.W. (1989). Dove reproduction and retinoid (vitamin A) dynamics in adult females and their eggs following exposure to 3,3′,4,4′-tetrachlorobiphenyl. Can. J. Zool. 67, 908-13.Google Scholar
  55. Trudeau, S.F. and Maisonneuve, F.J. (2001). A method to determine cytochrome P4501A activity in wildlife microsomes. Can. Wildl. Serv. Technical Report Series No. 339E.Google Scholar
  56. van den Berg, M., Craane, B.L.H.J., Sinnige, T., van Mourik, S., Dirksen, S., Boudewijn, T.H. and van der Gaag, M. (1994). Biochemical and toxic effects of polychlorinated biphenyls (PCBs), dibenzo-p-dioxins (PCDDs) and dibenzofurans (PCDFs) in the cormorant (Phalacrocorax carbo) after in ovo exposure. Environ. Toxicol. Chem. 13, 803-16.Google Scholar
  57. van den Berg, M., Brunström, B. and Nolt, C. (1998). Toxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wildlife. Environ. Health Perspect. 106, 775-92.Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • Zou Zou A. Kuzyk
    • 1
  • Neil M. Burgess
    • 2
    Email author
  • Jason P. Stow
    • 1
  • Glen A. Fox
    • 3
  1. 1.Environmental Sciences GroupRoyal Military College of CanadaKingston, ONCanada
  2. 2.Canadian Wildlife ServiceEnvironment CanadaMount Pearl, NLCanada
  3. 3.Canadian Wildlife ServiceNational Wildlife Research CenterOttawa, ONCanada

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