Skip to main content
SpringerLink
Log in

Microcontaminants and reproductive impairment of the Forster's tern on Green Bay, Lake Michigan-1983

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

For the 1983 nesting season, Forster's tern (Sterna forsteri) reproductive success was significantly impaired on organochlorine contaminated Green Bay, Lake Michigan compared to a relatively uncontaminated inland location at Lake Poygan, Wisconsin. Compared with tern eggs from Lake Poygan, eggs from Green Bay had significantly higher median concentrations of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD), other polychlorinated dibenzo-p-dioxins (PCDDs), total polychlorinated biphenyls (PCBs), total (three congeners) non-ortho, ortho' PCBs, five individual PCB congeners known to induce aryl hydrocarbon hydroxylase (AHH) and several other organochlorine contaminants. Conversions of analytical concentrations of TCDD and PCB congeners based on relative AHH induction potencies allowed for estimation of total 2,3,7,8-TCDD equivalents. Two PCB congeners, 2,3,3′,4,4′- and 3,3′,4,4′,5-pentachlorobiphenyl (PeCB) accounted for more than 90% of the median estimated TCDD equivalents at both Green Bay and Lake Poygan. The median estimated TCDD equivalents were almost 11-fold higher in tern eggs from Green Bay than in eggs from Lake Poygan (2175 and 201 pg/g). The hatching success of Green Bay sibling eggs from nests where eggs were collected for contaminant analyses was 75% lower at Green Bay than at Lake Poygan. Hatchability of eggs taken from other nests and artificially incubated was about 50% lower for Green Bay than for Lake Poygan. Among hatchlings from laboratory incubation, those from Green Bay weighed approximately 20% less and had a mean liver weight to body weight ratio 26% greater than those from Lake Poygan. In both field and laboratory, mean minimum incubation periods were significantly longer for eggs from Green Bay compared to Lake Poygan (8.25 and 4.58 days, respectively). Mean minimum incubation time for Green Bay eggs in the field was 4.37 days longer than in the laboratory. Hatchability was greatly improved when Green Bay eggs were incubated by Lake Poygan adults in an egg-exchange experiment, but was sharply decreased in Lake Poygan eggs incubated in Green Bay nests. Nest abandonment and egg disappearance were substantial at Green Bay but nil at Lake Poygan. Thus, not only factors intrinsic to the egg, but also extrinsic factors (parental attentiveness), impaired reproductive outcome at Green Bay. The epidemiological evidence from this study strongly suggested that contaminants were a causal factor. AHH-active PCB congeners (intrinsic effects) and PCBs in general (extrinsic effects) appeared to be the only contaminants at the concentrations measured in eggs, capable of producing the effects that were observed at Green Bay.

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

Similar content being viewed by others

References

  • Albro PW, Parker CE (1979) Comparison of the compositions of Aroclor 1242 and Aroclor 1016. J Chromatogr 169:161–166

    Google Scholar 

  • Albro PW, Corbett JT, Schroeder JL (1981) Quantitative characterization of polychlorinated biphenyl mixtures (Aroclors 1248, 1254, and 1260) by gas chromatography using capillary columns. J Chromatogr 205:103–111

    Google Scholar 

  • Andrews J, Lambert I, Robertson L, Bandiera S, Sawyer T, Lovering S, Safe S (1983) The comparative biologic and toxic potencies of polychlorinated biphenyls and polybrominated biphenyls. Toxicol Appl Pharamacol 70:204–215

    Google Scholar 

  • Aulerich RJ, Bursian SJ, Breslin WJ, Olson BA, Ringer RK (1985) Toxicological manifestations of 2,4,5,2′,4′,5′-, 2,3,6,2′,3′,6′-, and 3,4,5,3′,4′,5′-hexachlorobiphenyl and Aroclor 1254 in mink. J Toxicol Environ Health 15:63–79

    Google Scholar 

  • Aulerich RJ, Bursian SJ, Evans MG, Hochstein JR, Koudele KA, Olson BA, Napolitano AC (1987) Toxicity of 3,4,5,3′,4′,5′-hexachlorobiphenyl to mink. Arch Environ Contam Toxicol 16:53–60

    Google Scholar 

  • Ax RL, Hansen LG (1975) Effects of purified polychlorinated biphenyl analogs on chicken reproduction. Poult Sci 54: 895–900

    Google Scholar 

  • Ballschmiter K, Zell M (1980) Analysis of polychlorinated biphenyls (PCB's) by gas capillary gas chromatography, composition of technical Aroclor- and Clophen-PCB mixtures. Fresenius' Z Anal Chem 302:20–31

    Google Scholar 

  • Bandiera S, Sawyer T, Romkes M, Zmudzka B, Safe L, Mason G, Keys B, Safe S (1984) Polychlorinated dibenzofurans (PCDFs): Effects of structure on binding to the 2,3,7,8-TCDD cytosolic receptor protein, AHH induction and toxicity. Toxicology 32:131–144

    Google Scholar 

  • Bannister R, Safe S (1987) Aroclor 1254 as a 2,3,7,8-tetrachlorodibenzo-p-dioxin antagonist in C57BL/6J and DBA/2J miceeffects on enzyme induction and thymic atrophy. Toxicologist 7:160 (abstr)

    Google Scholar 

  • Bent AC (1921) Life histories of North American gulls and terns. US Natl Museum Bull 113

  • Biocca GM, McNulty WP, Bell M (1976) Toxicity of selected symmetrical hexachlorobiphenyl isomers. 1. Biological response in chicks and mice. In: Proc National Conf on polychlorinated biphenyls, EPA-560/6-75-004, US Environmental Protection Agency, Washington, DC, p 67

    Google Scholar 

  • Birnbaum LS, Weber H, Harris MW, Lamb JC IV, McKinney JD (1985) Toxic interaction of specific polychlorinated biphenyls and 2,3,7,8-tetrachlorodibenzo-p-dioxin: Increased incidence of cleft palate in mice. Toxicol Appl Pharmacol 77:292–302

    Google Scholar 

  • Birnbaum LS, Harris MW, Crawford DD, Morrissey RE (1987) Teratogenic effects of polychlorinated dibenzofurans in combination in C57BL/6N mice. Toxicol Appl Pharmacol 91:246–255

    Google Scholar 

  • Bleavins MR, Aulerich RJ, Ringer RK (1984) Effects of chronic dietary hexachlorobenzene exposure on the reproductive performance and survivability of mink and European ferret. Arch Environ Contam Toxicol 13:357–365

    Google Scholar 

  • Boersma DL, Ellenton JA, Yagminas A (1986) Investigation of the hepatic mixed-function oxidase system in herring gull embryos in relations to environmental contaminants. Environ Toxicol Chem 5:309–318

    Google Scholar 

  • Bradlaw JA, Casterline JL (1979) Induction of enzyme activity in cell culture: A rapid screen for detection of planar polychlorinated organic compounds. J Assoc Offic Anal Chem 62:904–916

    Google Scholar 

  • Bradlaw JA, Garthoff LH, Hurley NE (1980) Comparative induction of aryl hydrocarbon hydroxylase activityin vitro by analogues of dibenzo-p-dioxin. Food Cosmet Toxicol 18: 627–635

    Google Scholar 

  • Bush B, Tumasonis CF, Baker FD (1974) Toxicity and persistence of PCB homologs and isomers in the avian system. Arch Environ Contam Toxicol 2:195–212

    Google Scholar 

  • Buser HR, Rappe C (1984) Isomer-specific separation of 2378substituted polychlorinated dibenzo-p-dioxins by high-resolution gas chromatography/mass spectrometry. Anal Chem 56:442–448

    Google Scholar 

  • Cantrell JS, Webb NC, Mabis AJ (1969) Identification and crystal structure of a hydropericardium-producing factor: 1,2,3,7,8,9-hexachlorodibenzo-p-dioxin. Acta Crystallogr Sect B 25(1): 150–156

    Google Scholar 

  • Casterline JL, Bradlaw JA, Puma BJ, Ku Y (1983) Screening of freshwater fish and extracts for enzyme-inducing substances by an aryl hydrocarbon hydroxylase induction bioassay technique. J Assoc Offic Anal Chem 66:1136–1139

    Google Scholar 

  • Cecil HC, Bitman J, Lillie RJ, Fries GF, Verret J (1974) Embryotoxic and teratogenic effects in unhatched fertile eggs from hens fed polychlorinated biphenyls (PCBs). Bull Environ Contam Toxicol 11:489–495

    Google Scholar 

  • Cecil HC, Harris SJ, Bitman J, Fries GF (1973) Polychlorinated biphenyl-induced decrease in liver Vitamin A in Japanese quail and rats. Bull Environ Contam Toxicol 9:179–185

    Google Scholar 

  • Chardine JW, Morris RD (1983) Herring gull males eat their own eggs. Wilson Bull 95(3):477–478

    Google Scholar 

  • Cheung MO, Gilbert EF, Peterson RE (1981) Cardiovascular teratogenicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin in the chick embryo. Toxicol Appl Pharmacol 61:197–204

    Google Scholar 

  • Dahlgren RB, Linder RL (1971) Effects of polychlorinated biphenyls on pheasant reproduction, behavior and survival. J Wildl Manage 35:315–319

    Google Scholar 

  • Dahlgren RB, Linder RL, Carlson LW (1972) Polychlorinated biphenyls: Their effects on penned pheasants. Environ Health Perspect 1:89–101

    Google Scholar 

  • Davis D, Tizard I, Safe S (1987) Immunotoxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin: Antagonism by Aroclor 1254. Toxicologist 7:125 (abstr)

    Google Scholar 

  • DeVault DS (1985) Contaminants in fish from Great Lakes harbors and tributary mouths. Arch Environ Contam Toxicol 14:587–594

    Google Scholar 

  • Eadon G, Kaminsky L, Silkworth J, Aldous K, Hilker D, O'Keefe P, Smith R, Gierthy J, Hawley J, Kim N, DeCaprio A (1986) Calculation of 2,3,7,8-TCDD equivalent concentrations of complex environmental contaminant mixtures. Environ Health Perspect 70:221–227

    Google Scholar 

  • Eisler R (1985) Mirex hazards to fish, wildlife and invertebrates: A synoptic review. US Fish Wildl Serv Biol Rep 85(1.1)

  • -(1986) Dioxin hazards to fish, wildlife and invertebrates: A synoptic review. US Fish Wildl Serv Biol Rep 85(1.8)

  • Eisler R, Jacknow J (1985) Toxaphene hazards to fish, wildlife and invertebrates: A synoptic review. US Fish Wildl Serv Biol Rep 85(1.4)

  • Ellenton JA, Brownlee LJ, Hollebone Br (1985) Aryl hydrocarbon hydroxylase levels in herring gull embryos from different locations on the Great Lakes. Environ Toxicol Chem 4:615–622

    Google Scholar 

  • Firestone D (1973) Etiology of chick edema disease. Environ Health Perspect 5:59–66

    Google Scholar 

  • Flick DF, Firestone D, Higginbotham GR (1972) Studies of the chick edema disease: 9. Response of chicks fed or singly administered synthetic edema-producing compounds. Poult Sci 51:2026–2034

    Google Scholar 

  • Flick DF, O'Dell RG, Childs VA (1965) Studies of the chick edema disease: 3. Similarity of symptoms produced by feeding chlorinated biphenyl. Poult Sci 44:1460–1465

    Google Scholar 

  • Fox GA, Gilman AP, Peakall DB, Anderka FW (1978) Behavioral abnormalities of nesting Lake Ontario herring gulls. J Wildl Manage 42:477–483

    Google Scholar 

  • Friedman L (1962) Progress in the chick edema problem. In: Hearings before the Subcommittee on Energy, Natural Resources, and the Environment of the Committee on Commerce, US Senate Serial 91-60. Government Printing Office, 1970, Washington, DC, p 235

    Google Scholar 

  • Giesy JP, Newsted J, Garling DL (1986) Relationships between chlorinated hydrocarbon concentrations and rearing mortality of chinook salmon (Oncorhynchus tshawytscha) eggs from Lake Michigan. J Great Lakes Res 12(1):82–98

    Google Scholar 

  • Gilbertson M (1983) Etiology of chick edema disease in herring gulls in the Lower Great Lakes. Chemosphere 12:357–370

    Google Scholar 

  • Gilbertson M, Fox GA (1977) Pollutant-associated embryonic mortality of Great Lakes herring gulls. Environ Pollut 12:211–216

    Google Scholar 

  • Gilbertson M, Morris RD, Hunter RA (1976) Abnormal chicks and PCB residue levels in eggs of colonial birds on the Lower Great Lakes. The AUK 93:434–442

    Google Scholar 

  • Gilman AP, Fox GA, Peakall DB, Teeple SM, Carroll TR, Haymes GT (1977) Reproductive parameters and contaminant levels of Great Lakes herring gulls. J Wildl Manage 41(3):458–468

    Google Scholar 

  • Gochfeld M (1975) Developmental defects in common terns of western Long Island, New York. The AUK 92:58–65

    Google Scholar 

  • Goldstein JA (1980) Structure-activity relationships for the biochemical effects and relationship to toxicity. In: Kimbrough RD (ed) Topics in environmental health: Vol. 4. Halogenated biphenyls, terphenyls, naphthalenes, dibenzodioxins and related products. North-Holland, NY, p 151

    Google Scholar 

  • Goldstein JA, Linko P, Huckins JN, Stalling DL (1982) Structure-activity relationships of chlorinated benzenes as inducers of different forms of cytochrome P-450 in rat liver. Chem-Biol Interactions 41:131–139

    Google Scholar 

  • Haake JM, Mayura F, Phillips T, Safe S (1987) Teratogenicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin: Antagonism by Aroclor 1254. Toxicologist 7:124 (abstr)

    Google Scholar 

  • Hale JB (1982) Birds and wetlands. Wisc Acad Rev 29:24–26

    Google Scholar 

  • Harris HJ, Trick JA (1979) Status and nesting ecology of Forster's terns (Sterna forsteri) in Wisconsin. Annual Performance Report, Wisc Dept Nat Res, Off End & Non-Game Spp, Madison

    Google Scholar 

  • Harris HJ, Kubiak TJ, Trick JA (1985) Microcontaminants and reproductive impairment of the Forster's tern on Green Bay. Final Report to US Fish Wildl Serv, UW Sea Grant Inst, WI Dept Nat Res, Green Bay Metro Sew Dist, Sea Grant Office, ES 105, UW-Green Bay, WI 54301-7001

    Google Scholar 

  • Hays H, Risebrough RW (1972) Pollutant concentrations in abnormal young terns from Long Island Sound. The AUK 89:19–35

    Google Scholar 

  • Heath RG, Spann JW, Kreitzer JF, Vance C (1972) Effects of polychlorinated biphenyls on birds. Proc Int Ornithol Congr 15:475–485

    Google Scholar 

  • Heinz GH (1979) Methylmercury: Reproductive and behavioral effects on three generations of mallard ducks. J Wildl Manage 43(2):394–401

    Google Scholar 

  • Heinz GH, Erdman TC, Haseltine SD, Stafford C (1985) Contaminant levels in fish-eating birds from Green Bay and Lake Michigan, 1975–1980. Environ Monitor Assessm 5:223–236

    Google Scholar 

  • Higginbotham GR, Huang A, Firestone D, Verrett J, Ress J, Campbell AD (1968) Chemical and toxicological evaluations of isolated and synthetic chloroderivatives of dibenzo-pdioxin. Nature 220:702–703

    Google Scholar 

  • Hochstein JR, Aulerich RJ, Bursian SJ (1988) Acute toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin to mink. Arch Environ Contam Toxicol 17:33–37

    Google Scholar 

  • Hoffman DJ, Rattner BA, Sileo L, Docherty D, Kubiak TJ (1987) Embryotoxicity, teratogenicity and aryl hydrocarbon hydroxylase activity in Forster's terns on Green Bay, Lake Michigan. Environ Res 42:176–184

    Google Scholar 

  • Huckins JN, Stalling DL, Petty JD (1980) Carbon-foam chromatographic separation of non-o, o′-chlorine substituted PCBs from Aroclor mixtures. J Assoc Offic Anal Chem 63:750–755

    Google Scholar 

  • Kannan N, Tanabe S, Wakimoto T, Tatsukawa R (1987) Coplanar polychlorinated biphenyls in Aroclor and Kaneclor mixtures. J Assoc Offic Anal Chem 70:451–454

    Google Scholar 

  • Karlsson B (1974) Locomotory and dehydrogenase activities of redstartsPhoenicurus phoenicurus L. (Aves) given PCB and DDT. Environ Pollut 7:53–63

    Google Scholar 

  • Keys B, Piskorska-Pliszczynska J, Safe S (1986) Polychlorinated dibenzofurans as 2,3,7,8-TCDD antagonists:In vitro inhibition of monxygenase enzyme induction. Toxicol Lett 31: 151–158

    Google Scholar 

  • Kreitzer JF, Heinz GH (1974) The effect of sublethal dosages of five pesticides and a polychlorinated biphenyl on the avoidance response of coturnix quail chicks. Environ Pollut 6:21–29

    Google Scholar 

  • Leece B, Denomme MA, Towner R, Li SMA, Safe S (1985) Polychlorinated biphenyls: Correlation betweenin vivo andin vitro quantitative structure-activity relationships (QSARs). J Toxicol Environ Health 16:379–388.

    Google Scholar 

  • Lillie RJ, Cecil HC, Bitman J, Fries GF (1974) Differences in response of caged white leghorn layers to various polychlorinated biphenyls (PCBs) in the diet. Poult Sci 53:726–732

    Google Scholar 

  • Marti EA (1984) Polychlorinated biphenyls in sixteen Lake Michigan tributaries, MS Thesis, University of Wisconsin, Madison

    Google Scholar 

  • Mason G, Farrell K, Keys B, Piskorska-Pliszczynska J, Safe L, Safe S (1986) Polychlorinated dibenzo-p-dioxins: Quantitativein vitro andin vivo structure-activity relationships. Toxicology 41:21–31

    Google Scholar 

  • Masuda U, Kuroki H, Nagayama J (1983) Polychlorinated dibenzofurans in the tissues of patients with Yusho and their enzyme-inducing activities on aryl hydrocarbon hydroxylase. In: Choudhary G, Keith L, Rappe C (eds) Chlorinated dioxins and dibenzofurans in the total environment. Butterworth Publishers, Woburn, MA, p 375

    Google Scholar 

  • McArthur MLB, Fox GA, Peakall DB, Philogene BJR (1983) Ecological significance of behavioral and hormonal abnormalities in breeding ring doves fed an organochlorine chemical mixture. Arch Environ Cotam Toxicol 12:343–353

    Google Scholar 

  • McKinney JD, Chae K, Gupta BN, Moore JA, Goldstein JA (1976) Toxicological assessment of hexachlorobiphenyl isomers and 2,3,7,8-tetrachlorodibenzofuran in chicks. 1. Relationship of chemical parameters. Toxicol Appl Pharamcol 36:65–80

    Google Scholar 

  • McKinney JD, Chae K, McConnell EE, Birnbaum LS (1985) Structure-induction versus structure-toxicity relationships for polychlorinated biphenyls and related aromatic hydrocarbons. Environ Health Perspect 60:57–68

    Google Scholar 

  • McLaughlin J Jr, Marliac JP, Verrett MJ, Mutchler MK, Fitzhugh OG (1963) The injection of chemicals into the yolk sac of fertile eggs prior to incubation as a toxicity test. Toxicol Appl Pharmacol 5:760–771

    Google Scholar 

  • McNulty WP (1985) Toxicity and fetotoxicity of TCDD, TCDF and PCB isomers in Rhesus Macaques (Macaca mulatta). Environ Health Perspect 60:77–88

    Google Scholar 

  • Milby TH, Miller TL, Forrester TL (1985) PCB-containing transformer fires: Decontamination guidelines based on health considerations. J Occupational Med 27:351–356

    Google Scholar 

  • Mineau P, Fox GA, Norstrom RJ, Weseloh DV, Hallett DJ, Ellenton JA (1984) Using the herring gull to monitor levels and effects of organochlorine contamination in the Canadian Great Lakes. In: Nriagu JO, Simmons MS (eds) Toxic contaminants in the Great Lakes. J Wiley and Sons, NY, p 425

    Google Scholar 

  • Nisbet ICT, Reynolds LM (1984) Organochlorine residues in common terns and associated estuarine organisms, Massachusetts, USA, 1971–1981. Marine Environ Res 11:33–66

    Google Scholar 

  • Nisbet ICT, Welton MJ (1984) Seasonal variations in breeding success of common terns: Consequences of predation. The Condor 86:53–60

    Google Scholar 

  • Norstrom RJ, Risebrough RW, Cartwright DJ (1976) Elimination of chlorinated dibenzofurans associated with polychlorinated biphenyls fed to mallards (Anas platyrhynchos). Toxicol Appl Pharmacol 37:217–228

    Google Scholar 

  • Norstrom RJ, Hallett DJ, Sonstegard RA (1978) Coho salmon (Oncorhynchus kisutch) and herring gulls (Larus argentatus) as indicators of organochlorine contamination in Lake Ontario. J Fish Res Board Can 35:1401–1409

    Google Scholar 

  • Norstrom RJ, Hallett DJ, Simon M, Mulvihill MJ (1982) Analyses of Great Lakes herring gull eggs for tetrachlorodibenzo-p-dioxins. In: Hutzinger O, Frei RW, Merian E, Pocchiari F (eds) Chlorinated dioxins and related compounds: Impacts on the environment. Pergamon Press, Oxford, p 173

    Google Scholar 

  • Ontario Ministry of the Environment (1985) Scientific criteria document for standard development, No. 4–84. Polychlorinated dibenzodioxins (PCDDs) and polychlorinated dibenzofurans (PCDFs). Toronto, Canada

  • Parkinson A, Cockerline R, Safe S (1980a) Polychlorinated biphenyl isomers and congeners as inducers of both 3-methylcholanthrene- and phenobarbitone-type microsomal enzyme activity. Chem-Biol Interactions 29:277–289

    Google Scholar 

  • Parkinson A, Robertson L, Safe L, Safe S (1980b) Polychlorinated biphenyls as inducers of hepatic microsomal enzymes: Structure-activity rules. Chem-Biol Interactions 30:271–285

    Google Scholar 

  • Parkinson A, Safe SH, Robertson LW, Thomas PE, Ryan DE, Reik LM, Levin W (1983) Immunochemical quantitation of cytochrome P-450 isozymes and epoxide hydrolase in liver microsomes from polychlorinated or polybrominated biphenyl-treated rats. J Biol Chem 258:5967–5976

    Google Scholar 

  • Peakall DB, Peakall ML (1973) Effect of a polychlorinated biphenyl on the reproduction of artificially and naturally incubated dove eggs. J Appl Ecol 10:863–868

    Google Scholar 

  • Peakall DB, Fox GA, Gilman AD, Hallett DJ, Norstrom RJ (1980) Reproductive success of herring gulls as an indicator of Great Lakes water quality. In: Afghan BK, MacKay D (eds) Hydrocarbons and halogenated hydrocarbons in the aquatic environment. Plenum, NY, p 337

    Google Scholar 

  • Platonow NS, Reinhart BS (1973) The effects of polychlorinated biphenyls (Aroclor 1254) on chicken egg production, fertility and hatchability. Can J Compar Med 37:341–346

    Google Scholar 

  • Poland A, Glover E (1973) Chlorinated dibenzo-p-dioxins: Potent inducers of δ-aminolevulinic acid synthethase and aryl hydrocarbon hydroxylase. II. A study of the structure-activity relationship. Mol Pharmacol 9:736–747

    Google Scholar 

  • — (1974) Comparison of 2,3,7,8-tetrachlorodibenzo-pdioxin, a potent inducer of aryl hydrocarbon hydroxylase, with 3-methylcholanthrene. Mol Pharmacol 10:349–359

    Google Scholar 

  • — (1977) Chlorinated biphenyl induction of aryl hydrocarbon hydroxylase activity: A study of the structure-activity relationship. Mol Pharmacol 13:924–938

    Google Scholar 

  • Poland A, Greenlee WF, Kende AS (1979) Studies on the mechanism of action of the chlorinated dibenzo-p-dioxins and related compounds. Ann NY Acad Sci 320:214–230

    Google Scholar 

  • Poland A, Knutson JC (1982) 2,3,7,8-tetrachlorodibeezo-pdioxin and related halogenated aromatic hydrocarbons: Examination of the mechanism of toxicity. Ann Rev Pharmacol Toxicol 22:517–554

    Google Scholar 

  • Prudelkiewicz WJ, Boucher RV, Callenbach EW, Miller RC (1959) Some physiological responses of New Hampshire chickens to a mixture of penta- and hexachloronaphthalenes. Poult Sci 38:424–430

    Google Scholar 

  • Rappe C, Buser HR, Kuroki H, Masuda Y (1979) Identification of polychlorinated dibenzofurans (PCDFs) retained in patients with Yusho. Chemosphere 8:259–266

    Google Scholar 

  • Ribick MA, Smith IM, Dubay GR, Stalling DL (1981) Applications and results of analytical methods used in monitoring environmental contaminants. In: Branson DR, Dickson KL (eds) Aquatic toxicology and hazard assessment: Fourth conference. ASTM STP 737, Philadelphia, p 249

  • Rifkind AB, Muschick J (1983) Benoxaprofen suppression of polychlorinated biphenyl toxicity without alteration of mixed function oxidase function. Nature 303:524–526

    Google Scholar 

  • Roznick FD (1978) Response of the yellow headed blackbird to vegetation and water level changes in coastal marshes of Green Bay, Wisconsin. MS Thesis, University of Wisconsin, Green Bay

    Google Scholar 

  • Rush GF, Smith JH, Maita K, Bleavins M, Aulerich RJ, Ringer RK, Hook JB (1983) Perinatal hexachlorobenzene toxicity in the mink. Environ Res 31:116–124

    Google Scholar 

  • Ryan JJ, Lau PY, Pilon JC, Lewis D (1983) 2,3,7,8-tetrachlorodibenzo-p-dioxin and 2,3,7,8-tetrachlorodibenzofuran in Great Lakes commercial and sport fish. In: Choudhary G, Keith L, Rappe C (eds) Chlorinated dioxins and dibenzofurans in the total environment. Butterworth Publishers, Woburn, MA, p 87

    Google Scholar 

  • Ryan JJ, Lau P, Pilon JC, Lewis D, McLeod HA, Gervais A (1984) Incidence and levels of 2,3,7,8-tetrachlorodibenzo-p-dioxin in Lake Ontario commerical fish. Environ Sci Technol 18:719–721

    Google Scholar 

  • Safe S (1984) Polychlorinated biphenyls (PCBs) and polybrominated biphenyls (PBBs): Biochemistry, toxicology, and mechanism of action. CRC Critical Reviews Toxicol 13: 319–395

    Google Scholar 

  • — (1987) Determination of 2,3,7,8-TCDD toxic equivalent factors (TEFs): Support for the use of thein vitro AHH induction assay. Chemosphere 16:791–802

    Google Scholar 

  • Safe S, Parkinson A, Robertson L, Cockerline R, Safe L, Bandiera S, Okey A (1982) PCBs as AHH inducers. In: Hutzinger O, Frei R, Merian E, Pocchiari F (eds) Chlorinated dioxins and related compounds: Impact on the environment. Pergamon Press, NY, p 383

    Google Scholar 

  • Safe S, Bandiera S, Sawyer T, Robertson L, Safe L, Parkinson A, Thomas PE, Ryan DE, Reik LM, Levin W, Denomme MA, Fujita T (1985a) PCBs: Structure-function relationships and mechanism of action. Environ Health Perspect 60:47–56

    Google Scholar 

  • Safe S, Bandiera S, Sawyer T, Zmudzka B, Mason G, Romkes M, Denomme MA, Sparling J, Okey AB, Fujita T (1985b) Effects of structure on binding to the 2,3,7,8-TCDD receptor protein and AHH induction-halogenated biphenyls. Environ Health Perspect 61:21–33

    Google Scholar 

  • Sawyer T, Safe S (1982) PCB isomers and congeners: Induction of aryl hydrocarbon hydroxylase and ethoxyresorufino-deethylase enzyme activities in rat hepatoma cells. Toxicol Lett 13:87–94

    Google Scholar 

  • — (1985)In vitro AHH induction by polychlorinated biphenyl and dibenzofuran mixtures: Additive effects. Chemosphere 14:79–84

    Google Scholar 

  • Sawyer TW, Vatcher AD, Safe S (1984) Comparative aryl hydrocarbon hydroxylase induction activities of commercial PCBs in Wistar rats and rat hepatoma H-4-II E cells in culture. Chemosphere 13:695–701

    Google Scholar 

  • Schmitt CJ, Zajicek JL, Ribick MA (1985) National pesticide monitoring program: Residues of organochlorine chemicals in freshwater fish, 1980–1981. Arch Environ Contam Toxicol 14:225–260

    Google Scholar 

  • Schwartz TR, Campbell RD, Stalling DL, Little RL, Petty JD, Hogan JW, Kaiser EM (1984) Laboratory data base for isomer-specific determination of polychlorinated biphenyls. Anal Chem 56:1303–1308

    Google Scholar 

  • Schwartz TR, Lehman RG (1982) Determination of polychlorinated biphenyls in plant tissue. Bull Environ Contam Toxicol 28:723–727

    Google Scholar 

  • Smith LM, Stalling DL, Johnson JL (1984) Determination of part-per-trillion levels of polychlorinated dibenzofurans and dioxins in environmental samples. Anal Chem 56:1830–1842

    Google Scholar 

  • Stalling DL, Norstrom RJ, Smith LM, Simon M (1985) Patterns of PCDD, PCDF and PCB contamination in Great Lakes fish and birds and their characterization by principal components analysis. Chemosphere 14:627–643

    Google Scholar 

  • Stalling DL, Schwartz TR (1989) Polychlorinated biphenyls: Data reduction, treatment and chemometrics. In: Rappe C, Buser HR (eds) Environmental Carcinogens—Methods of Analysis and Exposure Measurement. Volume II—Polychlorinated Dibenzodioxins Dibenzofurans and Biphenyls. International Agency for Research on Cancer, IARC: Lyons, France Ch 10 (in press)

    Google Scholar 

  • Stalling DL, Smith LM, Petty JD, Hogan JW, Johnson JL, Rappe C, Buser HR (1983) Residues of polychlorinated dibenzo-p-dioxins and dibenzofurans in Laurentian Great Lakes fish. In: Tucker RE, Young AL, Gray AP (eds) Human and environmental risks of chlorinated dioxins and related compounds. Plenum, NY, p 221

    Google Scholar 

  • Stegeman JJ, Kloepper-Sams PJ, Farrington JW (1986) Monoxygenase induction and chlorobiphenyls in the deep-sea fishCorypohaenoides armatus. Science 231:1287–1289

    Google Scholar 

  • Sullivan JR, Delfino JJ (1982) A select inventory of chemicals used in Wisconsin's Lower Fox River Basin. University of Wisconsin Sea Grant Inst, WIS-SG-82-238, Madison

  • Supelco Inc (1982) Supelco Reporter. Bellefonte, PA, 16823-0048 1(4)1

  • Tanabe S, Kannan N, Wakimoto T, Tatsukawa R (1987a) Method for the determination of three toxic non-orthochlorine substituted coplanar PCBs in environmental samples at partper-trillion levels. Intern J Environ Anal Chem 29:199–213

    Google Scholar 

  • Tanabe S, Kannan N, Subramanian AN, Watanabe S, Tatsukawa R (1987b) Highly toxic coplanar PCBs: Occurrence, source, persistency and toxic implications to wildlife and humans. Environ Pollut 47:147–163

    Google Scholar 

  • Tori GM, Mayer LP (1981) Effects of polychlorinated biphenyls on the metabolic rates of mourning doves exposed to low ambient temperatures. Bull Environ Contam Toxicol 27:678–682

    Google Scholar 

  • Toxic Substances Task Force (1983) Final report on the Toxic Substances Task Forces on the Lower Fox River Systemcooperating agencies—Wisc Dept Nat Res, US Geol Surv, US Fish Wildl Serv, US Environmental Protection Agency, Univ Wisc Water Chem Dept, Madison

    Google Scholar 

  • Trick JA (1982) Reproductive success and foraging success as related to populations of Forster's terns (Sterna forsteri) on Green Bay, Lake Michigan. MS Thesis, University of Wisconsin, Green Bay

    Google Scholar 

  • Trotter WJ, Young SJV, Casterline JL, Bradlaw JA, Kamps LR (1982) Induction of aryl hydrocarbon hydroxylase activity in cell cultures by Aroclors, residues from Yusho oil samples and polychlorinated biphenyl residues from fish samples. J Assoc Offic Anal Chem 65:838–841

    Google Scholar 

  • Tumasonis CF, Bush B, Baker FD (1973) PCB levels in egg yolks associated with embryonic mortality and deformity of hatched chicks. Arch Environ Contam Toxicol 1:312–324

    Google Scholar 

  • USEPA (1987) Interim procedures for estimating risks associated with exposures to mixtures of chlorinated dibenzo-p-dioxins and-dibenzofurans (CDDs and CDFs). EPA-625/3-87/012. Risk Assessment Forum, US Environmental Protection Agency, Washington, DC

    Google Scholar 

  • 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. Arch Environ Contam Toxicol 16: 149–158

    Google Scholar 

  • Veret MJ (1970) Witness statement. In: Hearings before the Subcommittee on Energy, Natural Resources and the Environment of the Committee on Commerce, US Senate, Serial 91-60. US Govt Printing Office, Washington DC, p 190

    Google Scholar 

  • Vos JG (1972) Toxicology of PCBs for mammals and for birds. Environ Health Perspect 1:105–117

    Google Scholar 

  • Walker CR (1976) Pre-1972 knowledge of nonhuman effects of polychlorinated biphenyls. In: Proc National Conf on polychlorinated biphenyls, EPA-560/6-75-004. US Environmental Protection Agency, Washington, DC, p 268

    Google Scholar 

  • Weber H, Harris MW, Haseman JK, Birnbaum LS (1985) Teratogenic potency of TCDD, TCDF and TCDD-TCDF combinations in C57BL/6N mice. Toxicol Lett 26:159–167

    Google Scholar 

  • Wiemeyer SN, Lamont TG, Bunck CM, Sindelar CR, Gramlick FJ, Fraser JD, Byrd MA (1984) Organochlorine pesticide, polychlorobiphenyl, and mercury residues in bald eagle eggs-1969–1979- and their relationships to shell thinning and reproduction. Arch Environ Contam Toxicol 13:529–549

    Google Scholar 

  • Wren CD, Leatherland JF, Stokes PM (1987) The effects of polychlorinated biphenyls and methylmercury, singly and in combination on mink. II: Reproduction and kit development. Arch Environ Contam Toxicol 16:449–454

    Google Scholar 

  • Yamamoto H, Yoshimura H, Fujita M, Yamamoto T (1976) Metabolic and toxicologic evaluation of 2,3,4,3′,4′-pentachlorobiphenyl in rats and mice. Chem Pharm Bull 24:2168–2174

    Google Scholar 

Download references

Author information

Author notes

  1. L. M. Smith

    Present address: Hatfield Marine Science Center, U.S. Environmental Protection Agency, 97365, Newport, Oregon

Authors and Affiliations

  1. U.S. Fish and Wildlife Service, Habitat Enhancement Field Office, University of Wisconsin-Green Bay, 54302, Green Bay, Wisconsin, USA

    T. J. Kubiak

  2. Sea Grant Institute, University of Wisconsin-Green Bay, 54302, Green Bay, Wisconsin, USA

    H. J. Harris & J. A. Trick

  3. U.S. Fish and Wildlife Service, National Fisheries Contaminant Research Center, Route 1, 65201, Columbia, Missouri, USA

    L. M. Smith, T. R. Schwartz & D. L. Stalling

  4. U.S. Fish and Wildlife Service, National Wildlife Health Center, 6006 Schroeder Road, 53711, Madison, Wisconsin, USA

    L. Sileo & D. E. Docherty

  5. Richter Museum of Natural History, University of WisconsinGreen Bay, 54302, Green Bay, Wisconsin, USA

    T. C. Erdman

Authors
  1. T. J. Kubiak
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H. J. Harris
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. L. M. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. T. R. Schwartz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. D. L. Stalling
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. J. A. Trick
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. L. Sileo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. D. E. Docherty
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. T. C. Erdman
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kubiak, T.J., Harris, H.J., Smith, L.M. et al. Microcontaminants and reproductive impairment of the Forster's tern on Green Bay, Lake Michigan-1983. Arch. Environ. Contam. Toxicol. 18, 706–727 (1989). https://doi.org/10.1007/BF01225009

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01225009

Keywords

Search

Navigation