The Toxic Effects of Multiple Persistent Organic Pollutant Exposures on the Post-Hatch Immunity Maturation of Glaucous Gulls

REFERENCES

• Andersen, M., Lie, E., Derocher, A. E., Belikov, S. E., Bernhoft, A., Boltunov, A. N., Garner, G. W., Skaare, J. U., and Wiig, Ø., 2001. Geographic variation of PCB congeners in polar bears (Ursus maritimus) from Svalbard east to the Chukchi Sea, Polar Biol. 24 (2001), pp. 231–238.
   Web of Science ®Google Scholar
• Barrett, R. T., Skaare, J. U., and Gabrielsen, G. W., 1996. Recent changes in levels of persistent organochlorines and mercury in eggs of seabirds from the Barents Sea, Environ. Pollut. 92 (1996), pp. 13–18.
   PubMed Web of Science ®Google Scholar
• Barry, S. J., and Barry, T. W., 1990. Food habits of glaucous gulls in the Beaufort Sea, Arctic 43 (1990), pp. 43–49.
   Web of Science ®Google Scholar
• Bernhoft, A., Wiig, Ø., and Skaare, J. U., 1997. Organochlorines in polar bears (Ursus maritimus) at Svalbard, Environ. Pollut. 95 (1997), pp. 159–175.
   PubMed Web of Science ®Google Scholar
• Bernhoft, A., Skaare, J. U., Wiig, Ø., Derocher, A. E., and Larsen, H. J. S., 2000. Possible immunotoxic effects of organochlorines in polar bear at Svalbard, J. Toxicol. Environ. Health A 59 (2000), pp. 561–574.
   PubMed Web of Science ®Google Scholar
• Bogan, J. A., and Bourne, W. R. P., 1972. Organochlorine levels in Atlantic seabirds, Nature 240 (1972), p. 358.
   PubMed Web of Science ®Google Scholar
• Borgå, K., 1997. Bioaccumulation of organochlorines (OCs) in an Arctic marine food chain. MSc thesis. University of Tromsø, Tromsø; 1997.
   Google Scholar
• Borgå, K., Gabrielsen, G. W., and Skaare, J. U., 2001. Biomagnification of organochlorines along a Barents Sea food chain, Environ. Pollut. 113 (2001), pp. 187–198.
   PubMed Web of Science ®Google Scholar
• Borgå, K., Wolkers, H., Skaare, J. U., Hop, H., Muir, D. C. G., and Gabrielsen, G. W., 2005. Bioaccumulation of PCBs in Arctic seabirds: Influence of dietary exposure and congener biotransformation, Environ. Pollut. 134 (2005), pp. 397–409.
   PubMed Web of Science ®Google Scholar
• Borgå, K., Campbell, L., Gabrielsen, G. W., Norstrom, R. J., Muir, D. C. G., and Fisk, A. T., 2006. Regional and species specific bioaccumulation of major and trace elements in Arctic seabirds, Environ. Toxicol. Chem. 25 (2006), pp. 2927–2936.
   PubMed Web of Science ®Google Scholar
• Brevik, E. M., 1978. Gas chromatographic method for the determination of organochlorine pesticides in human milk, Bull. Environ. Contam. Toxicol. 19 (1978), pp. 281–286.
   PubMed Web of Science ®Google Scholar
• Bustnes, J. O., 2006. Pinpointing potential causative agents in mixtures of persistent organic pollutants in observational field studies: A review of glaucous gull studies, J. Toxicol. Environ. Health A 69 (2006), pp. 97–108.
   PubMed Web of Science ®Google Scholar
• Bustnes, J. O., Erikstad, K. E., Bakken, V., Mehlum, F., and Skaare, J. U., 2000. Feeding ecology and the concentration of organochlorines in glaucous gulls, Ecotoxicology 9 (2000), pp. 175–182.
   Web of Science ®Google Scholar
• Bustnes, J. O., Bakken, V., Erikstad, K. E., Mehlum, F., and Skaare, J. U., 2001. Patterns of incubation and nest-site attentiveness in relation to organochlorine (PCB) contamination in glaucous gulls, J. Appl. Ecol. 38 (2001), pp. 791–801.
   Web of Science ®Google Scholar
• Bustnes, J. O., Folstad, I., Erikstad, K. E., Fjeld, M., Miland, Ø. O., and Skaare, J. U., 2002. Blood concentration of organochlorine pollutants and wing feather asymmetry in glaucous gulls, Funct. Ecol. 16 (2002), pp. 617–622.
   Web of Science ®Google Scholar
• Bustnes, J. O., Erikstad, K. E., Skaare, J. U., Bakken, V., and Mehlum, F., 2003. Ecological effects of organochlorine pollutants in the Arctic: A study of the glaucous gull, Ecol. Appl. 13 (2003), pp. 504–515.
   Web of Science ®Google Scholar
• Bustnes, J. O., Hanssen, S. A., Folstad, I., Erikstad, K. E., Hasselquist, D., and Skaare, J. U., 2004. Immune function and organochlorine pollutants in arctic breeding glaucous gulls, Arch. Environ. Contam. Toxicol. 47 (2004), pp. 530–541.
   PubMed Web of Science ®Google Scholar
• Bustnes, J. O., Erikstad, K. E., Hanssen, S. A., Tveraa, T., Folstad, I., and Skaare, J. U., 2006. Anti-parasite treatment removes negative effects of environmental pollutants on reproduction in an Arctic seabird, Proc. R. Soc. Lond. B 273 (2006), pp. 3117–3122.
   PubMed Web of Science ®Google Scholar
• Catry, P., Ratcliffe, N., and Furness, R. W., 1998. The influence of hatching date on different life-history stages of Great Skuas Catharacta skua, J. Avian Biol. 29 (1998), pp. 299–304.
   Web of Science ®Google Scholar
• Catty, D., 1998. Antibodies: A practical approach. Oxford: IRL Press; 1998.
   Google Scholar
• deSwart, R. L., Ross, P. S., Vos, J. G., and Osterhaus, A. D. M. E., 1996. Impaired immunity in harbour seals (Phoca vitulina) exposed to bioaccumulated environmental contaminants: Review of a long-term feeding study, Environ. Health Perspect. 104 (1996), pp. 823–828.
   PubMed Web of Science ®Google Scholar
• Erikstad, K. E., 1990. Winter diets of four seabird species in the Barents Sea after a crash in the capelin stock, Polar Biol. 10 (1990), pp. 619–627.
   Web of Science ®Google Scholar
• Fairbrother, A., Smits, J., and Grasman, K. A., 2004. Avian immunotoxicology, J. Toxicol. Environ. Health B 7 (2004), pp. 105–137.
   PubMed Web of Science ®Google Scholar
• Grasman, K. A., Fox, G. A., Scanlon, P. F., and Ludwig, J. P., 1996. Organochlorine-associated immunosuppression in prefledgling Caspian terns and herring gulls from the Great Lakes: An ecoepidemiological study, Environ. Health Perspect. 104 (1996), pp. 829–842.
   PubMed Web of Science ®Google Scholar
• Grasman, K. A., and Fox, G. A., 2001. Associations between altered immune function and organochlorine contamination in young Caspian terns (Sterna caspia) from Lake Huron, 1997–1999, Ecotoxicology 10 (2001), pp. 101–114.
   PubMed Web of Science ®Google Scholar
• Heilmann, C., Grandjean, P., Weihe, P., Nielsen, F., and Budtz-Jorgensen, E., 2006. Reduced antibody responses to vaccinations in children exposed to polychlorinated biphenyls, PLoS Med. 3 (2006), pp. 1352–1359, .
   Web of Science ®Google Scholar
• Helgason, L. B., Barrett, R., Lie, E., Polder, A., Skaare, J. U., and Gabrielsen, G. W., 2008a. Levels and temporal trends (1983–2003) of persistent organic pollutants (POPs) and mercury (Hg) in seabird eggs from Northern Norway, Environ. Pollut. 155 (2008a), pp. 190–198.
   PubMed Web of Science ®Google Scholar
• Helgason, L. B., Polder, A., Føreid, S., Bæk, K., Lie, E., Gabrielsen, G. W., Barrett, R. T., and Skaare, J. U., 2008b. Levels and temporal trends (1983–2003) of polybrominated diphenyl ethers (PBDEs) and hexabromocyclododecane (HBCD) in seabird eggs from Northern Norway, Environ. Toxicol. Chem. (2008b), [Epub ahead of print].
   Web of Science ®Google Scholar
• Henriksen, E. O., 1999. Persistent organochlorine pollutants in two Arctic gull species: Levels and possible biochemical effects. Tromsø: PhD thesis, University of Tromsø; 1999.
   Google Scholar
• Henriksen, E. O., Gabrielsen, G. W., and Skaare, J. U., 1998. Validation of the use of blood samples to assess tissue concentrations of organochlorines in glaucous gulls, Larus hyperboreus, Chemosphere 37 (1998), pp. 2627–2643.
   Web of Science ®Google Scholar
• Henriksen, E. O., Gabrielsen, G. W., Trudeau, S., Wolkers, H., Sagerup, K., and Skaare, J. U., 2000. Organochlorines and possible biochemical effects in glaucous gulls (Larus hyperboreus) from Bjørnøya, the Barents Sea, Arch. Environ. Contam. Toxicol. 38 (2000), pp. 234–243.
   PubMed Web of Science ®Google Scholar
• Hertz-Picciotto, I., Park, H. Y., Dostal, M., Kocan, A., Trnovec, T., and Sram, R., 2008. Prenatal exposures to persistent and non-persistent organic compounds and effects on immune system development, Basic Clin. Pharmacol. Toxicol. 102 (2008), pp. 146–154.
   PubMed Web of Science ®Google Scholar
• Jakob, E. M., Marshall, S. D., and Uetz, G. W., 1996. Estimating fitness: A comparison of body condition indices, Oikos 77 (1996), pp. 61–67.
   Web of Science ®Google Scholar
• Janeway, C. A., 2005. Immunobiology: the immune system in health and disease. New York: Garland Science; 2005.
   Google Scholar
• Jolicoeur, P., and Mosimann, J. E., 1960. Size and shape variation in the painted turtle. A principal component analysis, Growth 24 (1960), pp. 339–354.
   PubMedGoogle Scholar
• Lavoie, E. T., and Grasman, K. A., 2007. Effects of in ovo exposure to PCBs 126 and 77 on mortality, deformities and post-hatch immune function in chickens, J. Toxicol. Environ. Health A 70 (2007), pp. 547–558.
   PubMed Web of Science ®Google Scholar
• Lie, E., Larsen, H. J. S., Larsen, S., Johnsen, G. M., Derocher, A. E., Lunn, N. J., Norstrom, R. J., Wiig, Ø., and Skaare, J. U., 2004. Does high organochlorine (OC) exposure impair the resistance to infection in polar bears (Ursus maritimus)? Part 1: Effect of OCs on the humoral immunity, J. Toxicol. Environ. Health A 67 (2004), pp. 555–582.
   PubMed Web of Science ®Google Scholar
• Lie, E., Larsen, H. J. S., Larsen, S., Johansen, G. M., Derocher, A. E., Lunn, N. J., Norstrom, R. J., Wiig, Ø., and Skaare, J. U., 2005. Does high organochlorine (OC) exposure impair the resistance to infection in polar bears (Ursus maritimus)? Part II: Possible effect of OCs on mitogen- and antigen-induced lymphocyte proliferation, J. Toxicol. Environ. Health A 68 (2005), pp. 457–484.
   PubMed Web of Science ®Google Scholar
• Lyche, J. L., Larsen, H. J. S., Skaare, J. U., Tverdal, A., Dahl, E., Johansen, G., and Ropstad, E., 2004. Effects of perinatal exposure to low doses of PCB 153 and PCB 126 on lymphocyte proliferation and hematology in goat kids, J. Toxicol. Environ. Health A 67 (2004), pp. 889–905.
   PubMed Web of Science ®Google Scholar
• Lyche, J. L., Larsen, H. J. S., Skaare, J. U., Tverdal, A., Johansen, G. M., and Ropstad, E., 2006. Perinatal exposure to low doses of PCB 153 and PCB 126 affects maternal and neonatal immunity in goat kids, J. Toxicol. Environ. Health A 69 (2006), pp. 139–158.
   PubMed Web of Science ®Google Scholar
• Løvenskiold, H. L., 1964. Avifauna Svalbardensis: With a discussion on the geographical distribution of the birds in Spitsbergen and adjacent islands. Oslo: Norwegian Polar Institute; 1964.
   Google Scholar
• Mancini, G., Vaerman, J. P., Garbonara, A., and Heremans, J. F., 1964. "A single-radial difusion method for the immunological quantification of proteins". In: Peeters, H., ed. Protides of the biological fluids, Proceedings of the 11th Colloquium, Bruges, 1963. Amsterdam: Elsevier; 1964. pp. 370–373.
   Google Scholar
• Mehlum, F., and Daelemans, F. F., 1995. PCBs in Arctic seabirds from the Svalbard region, Sci. Total Environ. 160/161 (1995), pp. 441–446.
   Web of Science ®Google Scholar
• Muir, D. C. G., Norstrom, R. J., and Simon, M., 1988. Organochlorine contaminants in Arctic marine food-chains—Accumulation of specific polychlorinated-biphenyls and chlordane-related compounds, Environ. Sci. Technol. 22 (1988), pp. 1071–1079.
   PubMed Web of Science ®Google Scholar
• Murvoll, K. M., Jenssen, B. M., and Skaare, J. U., 2005. Effects of pentabrominated diphenyl ether (PBDE-99) on vitamin status in domestic duck (Anas platyrhynchos) hatchlings, J. Toxicol. Environ. Health A 68 (2005), pp. 515–533.
   PubMed Web of Science ®Google Scholar
• http://www.nifes.no Last accessed 2008. , NIFES. 2008. Seafood data. National Institute of Nutrition and Seafood Research (NIFES).
   Google Scholar
• Norstrom, R. J., and Muir, D. C. G., 1994. Chlorinated hydrocarbon contaminants in arctic marine mammals, Sci. Total Environ. 154 (1994), pp. 107–128.
   PubMed Web of Science ®Google Scholar
• Norstrom, R. J., Belikov, S. E., Born, E. W., Garner, G. W., Malone, B., Olpinski, S., Ramsay, M. A., Schliebe, S., Stirling, I., Stishov, M. S., Taylor, M. K., and Wiig, O., 1998. Chlorinated hydrocarbon contaminants in polar bears from eastern Russia, North America, Greenland, and Svalbard: Biomonitoring of Arctic pollution, Arch. Environ. Contam. Toxicol. 35 (1998), pp. 354–367.
   PubMed Web of Science ®Google Scholar
• Perrins, C. M., 1970. Timing of birds breeding seasons, Ibis 112 (1970), pp. 242–255.
   Web of Science ®Google Scholar
• R Development Core Team, , 2008. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2008.
   Google Scholar
• Ross, P. S., de Swart, R. L., van der Vliet, H., Willemsen, L., de Klerk, A., van Amerongen, G., Groen, J., Brouwer, A., Schipholt, I., Morse, D. C., van Lovere, H., Osterhaus, A. D. M. E., and Vos, J. G., 1997. Impaired cellular immune response in rats exposed perinatally to Baltic Sea herring oil or 2,3,7,8-TCDD, Arch. Toxicol. 71 (1997), pp. 563–574.
   PubMed Web of Science ®Google Scholar
• Rothman, K. J., 1990. No adjustments are needed for multiple comparisons, Epidemiology 1 (1990), pp. 43–46.
   PubMedGoogle Scholar
• Sagerup, K., Henriksen, E. O., Skorping, A., Skaare, J. U., and Gabrielsen, G. W., 2000. Intensity of parasitic nematodes is associated with organochlorine levels in the glaucous gull (Larus hyperboreus), J. Appl. Ecol. 37 (2000), pp. 1–9.
   Web of Science ®Google Scholar
• Segre, M., Arena, S. M., Greeley, E. H., Melancon, M. J., Graham, D. A., and French, J. B., 2002. Immunological and physiological effects of chronic exposure of Peromyscus leucopus to Aroclor 1254 at a concentration similar to that found at contaminated sites, Toxicology 174 (2002), pp. 163–172.
   PubMed Web of Science ®Google Scholar
• Tryphonas, H., 1994. Immunotoxicity of polychlorinated biphenyls: Present status and future considerations, Exp. Clin. Immunogenet. 11 (1994), pp. 149–162.
   PubMedGoogle Scholar
• Tryphonas, H., 2005. Investigative immunotoxicology. Boca Raton, FL: Taylor & Francis; 2005.
   Google Scholar
• Van den Berg, M., Birnbaum, L. S., Denison, M., De Vito, M., Farland, W., Feeley, M., Fiedler, H., Hakansson, H., Hanberg, A., Haws, L., Rose, M., Safe, S., Schrenk, D., Tohyama, C., Tritscher, A., Tuomisto, J., Tysklind, M., Walker, N., and Peterson, R. E., 2006. The 2005 World Health Organization reevaluation of human and mammalian toxic equivalency factors for dioxins and dioxin-like compounds, Toxicol. Sci. 93 (2006), pp. 223–241.
   PubMed Web of Science ®Google Scholar
• Verreault, J., Skaare, J. U., Jenssen, B. M., and Gabrielsen, G. W., 2004. Effects of organochlorine contaminants on thyroid hormone levels in arctic breeding glaucous gulls, Larus hyperboreus, Environ. Health Perspect. 112 (2004), pp. 532–537.
   PubMed Web of Science ®Google Scholar
• Vos, J. G., and Luster, M., 1989. "Immune alteration". In: Kimbrough, R., and Jensen, A., eds. Halogenated biphenyls, terphenyls, naphthalenes, dibenzodioxins, and related products. Amsterdam: Elsevier; 1989. pp. 295–322.
   Google Scholar
• Walker, C., 1990. Persistent pollutants in fish-eating sea birds—Bioaccumulation, metabolism and effects, Aquat. Toxicol. 17 (1990), pp. 293–324.
   Web of Science ®Google Scholar
• Walker, C. H., Hopkin, S. P., Sibly, R. M., and Peakall, D. B., 2006. Principles of ecotoxicology. Boca Raton, FL: Taylor & Francis; 2006.
   Google Scholar