Abstract
Bald eagle (Haliaeetus leucocephalus) eggs were collected during incubation, 1990–1992, from 16 nests near three bleached-kraft pulp mills, from six nests in the Fraser River estuary and from seven nests at a reference site on the Pacific coast of Canada. Polychlorinated dibenzo-p-dioxins (PCDDs) and polychlorinated dibenzofurans (PCDFs) were present in all eggs in a qualitatively similar pattern among sites. Mean concentrations of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) were significantly higher in eggs collected from near three kraft pulp mill sites in the Strait of Georgia (44, 45, 84 ng/kg) than from the reference area in Johnstone Strait (15 ng/kg). There were few differences among sites in mean organochlorine pesticide levels, indicating the diffuse distribution of those chemicals and the domination of atmospheric inputs. Mean concentrations of total polychlorinated biphenyls (PCBs) were highest in eggs from the Strait of Georgia (4.86 mg/kg) and the PCB congener pattern was significantly different between that area and both the lower Fraser valley and Johnstone Strait. Mean mercury concentrations, which were mainly methyl-mercury, were significantly higher in eggs collected from the lower Fraser Valley (0.258 mg/kg) and Johnstone Strait (0.294 mg/kg) compared to the Strait of Georgia (0.188 mg/kg). Individual and regional variation in concentrations of organochlorine pesticides, PCBs and mercury in eagle eggs were thought to be influenced mainly by dietary differences. Toxicologically, in 1990, mean TCDD-toxic equivalents (TEQs) in bald eagle eggs were about two-fold greater than a lowest-observed-effect level, suggested elsewhere for this species, of 210 ng/kg TEQs. In the Strait of Georgia, PCCDs and PCDFs made a greater contribution to TEQs than non-ortho and mono-ortho PCBs, whereas the reverse was true for eggs outside the strait. Mean eggshell thickness was less than the pre-1947 value at all sites, although there was no significant relationship between eggshell thickness and DDE concentrations. Levels of other organochlorine pesticides and mercury were below those considered to be toxic.
Similar content being viewed by others
References
Ahlborg UG, Beckling GC, Birnbaum LS, Brouwer A, Derks HJ, Feeley M, Golor G, Hanberg A, Larsen JC, Liem AKD, Safe SH, Schlatter C, Waern F, Younes M, Yrjanheikki E (1994) Toxic equivalency factors for dioxin-like PCBs. Chemosphere 28:1049–1067
Allred PM, Strange JR (1977) The effects of 2,4,5-trichlorophenoxyacetic acid and 2,3,7,8-tetrachlorodebenzo-p-dioxin on developing chick embryos. Arch Environ Contam Toxicol 5:483–489
Anderson DW, Hickey JJ (1972) Eggshell changes in certain North American birds. Proc Int Ornithol Cong 15:514–540
Ankley GT, Niemi GJ, Lodge KB, Harris HJ, Beaver DL, Tillitt DE, Schwartz TR, Giesy JP, Jones PD, Hagley C (1993) Uptake of planar polychlorinated biphenyls and 2,3,7,8-substituted polychlorinated dibenzofurans and dibenzo-p-dioxins by birds nesting in the lower Fox River and Green Bay, Wisconsin, USA. Arch Environ Contam Toxicol 24:332–344
Anthony RG, Garrett MJ, Schuler CA (1993) Environmental contaminants in bald eagles in the Columbia river estuary. J Wildl Manage 57:10–19
Bishop CA, Weseloh DV, Burgess NM, Struger J, Norstrom RJ, Turle R, Logan KA (1992) An atlas of contaminants in fish-eating colonial birds of the Great Lakes (1970–1988), Vol. 1, Can Wildl Serv Tech Rep Ser No 152, 400 pp
Bosveld ATC, Van den Berg M (1994) Effects of polychlorinated biphenyls, dibenzo-p-dioxins, and dibenzofurans on fish-eating birds. Environ Rev 2:147–166
Bosveld ATC, Gradener J, Murk AJ, Brouwer A, Van Kampen M, Evers EJG, Van den Berg M (1994) Effects of PCDDs, PCDFs, and PCBs in common tern (Sterna hirundo) breeding in estuarine and coastal colonies in the Netherlands and Belgium. Environ Toxicol Chem 14:99–115
Boumphrey RS, Harrad SK, Jones KC, Osborn D (1993) Polychlorinated biphenyl congener patterns in tissues from a selection of British birds. Arch Environ Contam Toxicol 25:346–352
Bowerman WW, Kubiak TJ, Holt Jr JB, Evans DL, Eckstein RG, Sindelar CR, Best DA, Kozie KD (1994) Observed abnormalities in mandibles of nestling bald eagles Haliaeetus leucocephalus. Bull Environ Contam Toxicol 53:450–457
Braune BM, Norstrom RJ (1989) Dynamics of organochlorine compounds in herring gulls. 3. Tissue distribution and bioaccumulation in Lake Ontario gulls. Environ Toxicol Chem 8:957–968
Brown JF (1994) Determination of PCB metabolic, excretion, and accumulation rates for use as indicators of biological response and relative risk. Environ Sci Technol 13:2295–2305
Callum GI, Ferguson MM (1981) Determination of methylmercury in tissue using enzyme proteolysis. Analyst 106:1009–1013
Dwernychuck LW, Levy D (1994) Crofton Environmental Effects Monitoring (EEM) pre-design reference document. Hatfield Consultants, West Vancouver, BC, Canada
Dykstra CJR (1995) Effects of contaminants, food availability, and weather on the reproductive rate of Lake Superior Bald Eagles (Haliaeetus leucocephalus). Unpubl. PhD Thesis, University of Wisconsin-Madison, 247 pp
Eisenreich SJ, Looney BB, Thornton JD (1981) Airborne organic contaminants in the Great Lakes ecosystem. Environ Sci Technol 15:30–38
Elliott JE, Butler RW, Norstrom RJ, Whitehead PE (1989a) Environmental contaminants and reproductive success of great blue herons Ardea herodias in British Columbia, 1986–87. Environ Pollut 59:91–114
Elliott JE, Noble DG, Norstrom RJ, Whitehead PE (1989b) Organochlorine contaminants in seabird eggs from the Pacific coast of Canada, 1971–1986. Environ Monit Assess 12:67–82
Elliott JE, Martin PA, Arnold PW, Sinclair PH (1994) Organochlorines and reproductive success of birds in orchard and non-orchard areas of British Columbia, 1990–1991. Archiv Environ Contam Toxicol 26:435–443
Elliott JE, Whitehead PE, Martin PA, Bellward GD, Norstrom RJ (1995) Effects of pulp mill pollutants on wildlife. In: M.R. Servos, K.R. Munkittrick, J.H. Carey and G.J. Van Der Kraak (eds.). Fate and Effects of Pulp and Paper Mill Effluents. St. Lucie Press, Boca Raton, FL, pp. 297–314
Elliott JE, Norstrom RJ, Lorenzen A, Kennedy SE, Philibert H, Stegeman JJ, Hart LE, Bellward GD, Cheng KM (1996) Biological effects of Polychlorinated dibenzo-p-dioxins, dibenzofuran and biphenyls in bald eagle (Haliaeetus leucocephalus) chicks. Environ Toxicol Chem 15(5):782–793
Environment Canada (1985) National inventory of fluids containing polychlorinated biphenyls (PCBs). EPS 5/HA/1. Ottawa, ON, Canada, 17 pp
Fimreite N, Holsworth WN, Keith JA, Pearce PA, Gruchy IM (1971) Mercury in fish and fish-eating birds near sites of industrial contamination in Canada. Can Field Nat 85:211–220
Frenzel RW, Anthony RG (1989) Relationships of diets and environmental contaminants in wintering bald eagles. J Wildl Manage 53:792–802
Harding LE, Pomeroy WM (1990) Dioxin and furan levels in sediments, fish and invertebrates from fishery closure areas of coastal British Columbia. Environment Canada, Vancouver, BC, Canada, Regional Rep 90–09, 66 pp
Hebert CE, Norstrom RJ, Simon M, Braune BM, Weseloh DV, Macdonald CR (1994) Temporal trends and sources of PCDDs and PCDFs in the Great Lakes: herring gull egg monitoring, 1981–1991. Environ Sci Technol 28:1268–1277
Helander B, Olsson M, Reuterhardh L (1982) Residue levels of organochlorine and mercury compounds in unhatched eggs and their relationships to breeding success in white-tailed sea eagles Heliaeetus albicilla in Sweden. Holarctic Ecol 5:39–366
Janz DM (1995) Effects of early in ovo 2,3,7,8-tetrachlorodibenzo-p-dioxin exposure on perinatal thyroid and sex steroid hormone levels in three avian species. University of British Columbia, Unpubl. PhD thesis
Kawano M, Matsushita S, Inqoue T, Tanaka H, Tatsukawa R (1986) Biological accumulation of chlordane compounds in marine organisms from the northern North Pacific and Bering Sea. Mar Pollut Bull 17:512–516
Knight RL, Randolph PJ, Allen GT, Young LS, Wigen RJ (1990) Diets of nesting bald eagles, Haliaeetus leucocephalus, in western Washington. Can Field Nat 104:545–551
Kubiak TJ, Harris HJ, Smith LM, Schwarz TR, Stalling DL, Trick JA, Sileo L, Docherty DE, Erdman TC (1989) Microcontaminants and reproductive impairment of the Forster's Tern on Green Bay, Lake Michigan-1983. Archiv Environ Contam Toxicol 18:706–727
Letcher RJ, Norstrom RJ, Lin S, Ramsey MA, Bandiera SM (1996) Immunoquantitation and microsomal monooxygenase activities of hepatic cytochromes P450 1A and P450 2B and chlorinated hydrocarbon contaminant levels in polar bear (Ursus maritimus). Toxicol Appl Pharmacol 137:127–140
Luthe CE, Berry RM, Voss RH, Fleming BI (1990) Dioxins and furans in pulp: mill questions - research answers. Pulp and Paper Research Institute of Canada, Misc Rep 175, 15 pp
Mullin MD, Pochini CM, McCrindle S, Ronkes M, Safe SH, Safe LM (1984) High resolution PCB analysis: synthesis and chromatographic properties of all 209 PCB congeners. Environ Sci Technol 18:458–476
Nomeir AA, Hajjar NP (1987) Metabolism of chlordane in mammals. Rev Environ Contam Toxicol 100:1–22
Norstrom RJ, Simon M, Muir DCG, Schweinsburg R (1988) Organochlorine contaminants in Arctic marine food chains: identification, geographical distribution and temporal trends in polar bears. Environ Sci Technol 22:1063–1071
Norstrom RJ, Simon M (1991) Determination of specific polychlorinated dibenzo-p-dioxins and dibenzofurans in biological matrices by gel-permeation/carbon chromatography and gas chromatography-mass spectrometry. In C. Rappe, H.R. Buser, B. Dodet and I.K. O'Neill, eds., Polychlorinated dibenzo-p-dioxins and dibenzofurans. World Health Organization, Lyon, France. pp 281–297
Peterson RE, Theobald HM, Kimmel GL (1993) Developmental and reproductive toxicity of dioxins and related compounds: cross species comparisons. Crit Rev Toxicol 23:283–335
Rinella JF, Hamilton PA, McKenzie SW (1993) Persistence of the DDT pesticide in the Yakima River basin, Washington. U.S. Geological Survey, Circular 1090, 24 pp
Safe S (1990) Polychlorinated biphenyls (PCBs), dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs), and related compounds: environmental and mechanistic considerations which support the development of toxic equivalency factors (TEFs). Crit Rev Toxicol 21:51–88
Sanderson JT, Norstrom RJ, Elliott JE, Hart LE, Cheng KM, Bellward GD (1994a) Biological effects of polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls in double-crested cormorant chicks (Phalacrocorax auritus). J Toxicol Environ Health 41:247–265
Sanderson JT, Elliott JE, Norstrom RJ, Whitehead PE, Hart LE, Cheng KM, Bellward GD (1994b) Monitoring biological effects of polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls in great blue heron chicks (Ardea herodias) J Toxicol Environ Health 41:435–450
Scheuhammer AM, Bond D (1991) Factors affecting the determination of total mercury in biological samples by continuous-flow cold vapour atomic absorption spectrophotometry. Biolog Trace Element Res 31:119–129
Thomson RE (1981) Oceanography of the British Columbia coast. Can Spec Publ Fish Aquat Sci 56–291 pp
Turle R, Norstrom RJ, Collins B (1991) Comparison of PCB quantitation methods: re-analysis of archived specimens of herring gull eggs from the Great Lakes. Chemosphere 22:201–213
Van den Berg M, Olie K, Hutzinger O (1985) Polychlorinated dibenzofurans (PCDFs): environmental occurrence and physical, chemical and biological properties. Toxicol Environ Chem 9:171–217
Van den Berg M, Blank F, Heeremans C, Wagenaar H, Olie K (1987) Presence of polychlorinated dibenzo-p-dioxins and polychlorinated dibenzofurans in fish-eating birds and fish from the Netherlands. Archiv Environ Contam Toxicol 16:149–158
Van den Berg M, Craane BL, Sinnige T, Van Mourik S, Dirksen S, Boudewijn T, Van der Gaag M, Lutke-Schipholt IJ, Spenkelink B, Brouwer A (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 13:803–816
Vermeer K, Morgan KH, Butler RW, Smith GEK (1989a) Population, nesting habitat, and food of bald eagles in the Gulf Islands. In: The Ecology and status of marine and shoreline birds in the Strait of Georgia, British Columbia, K. Vermeer and R.W. Butler (eds.). Canadian Wildlife Service, Special Publ., Ottawa, ON, pp 123–130
Watson JW, Garrett MG, Anthony RG (1991) Foraging ecology of bald eagles in the Columbia River estuary. J Wildl Manage 45:492–499
Welch LJ (1994) Contaminant burdens and reproductive rates of bald eagles breeding in Maine. Unpubl. Msc. Thesis, Univ. of Maine, Old Town, MA, 86 pp
White DH, Seginak JT (1994) Dioxins and furans linked to reproductive impairment in wood ducks. J Wildl Manage 58:100–106
Whitehead PE (1989) Toxic chemicals in Great Blue Heron (Ardea herodias) eggs in the Strait of Georgia. In K. Vermeer and R.W. Butler (eds.) The ecology and status of marine and shoreline birds in the Strait of Georgia, British Columbia. Wolf et al. 1984. Spec Publ Can Wildl Serv Ottawa, Canada, pp 177–183
Whitehead PE, Elliott JE, Norstrom RJ, Vermeer K (1990) PCDD and PCDF contamination of waterfowl in the Strait of Georgia British Columbia, Canada: 1989–90. Organohalogen Compounds 1:459–462
Whitehead PE, Norstrom RJ, Elliott JE (1992) Dioxin levels in eggs of great blue herons (Ardea herodias) decline rapidly in response to process changes in a nearby kraft pulp mill. Organohalogen Compounds 9:325–328
Whitehead PE, Elliott JE, Norstrom RJ, Steeger C, Van Oostdam J, Smith GEJ (1993) Chlorinated hydrocarbon levels in eggs of ospreys nesting near pulp mills in British Columbia, Canada. Organohalogen Compounds 12:231–234
Wiemeyer SN, Bunck CM, Stafford CJ (1993) Environmental contaminants in bald eagle eggs—1980–84—and further interpretations of relationships to productivity and shell thickness. Archiv Environ Contam Toxicol 24:213–227
Yamashita N, Tanabe S, Ludwig JP, Kurita H, Ludwig MI, Tatsukawa R (1993) Embryonic abnormalities and organochlorine contamination in double-crested cormorants (Phalacrocorax auritus) and caspian terns (Hydroprogne caspia) from the upper Great Lakes in 1988. Environ Pollut 79:163–173
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Elliott, J.E., Norstrom, R.J. & Smith, G.E.J. Patterns, trends, and toxicological significance of chlorinated hydrocarbon and mercury contaminants in bald eagle eggs from the pacific coast of Canada, 1990–1994. Arch. Environ. Contam. Toxicol. 31, 354–367 (1996). https://doi.org/10.1007/BF00212674
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00212674