Abstract
Several polybrominated biphenyl ether (PBDE) congeners were found in all 175 osprey (Pandion haliaetus) eggs collected from the Columbia River Basin between 2002 and 2009. ΣPBDE concentrations in 2008–2009 were highest in osprey eggs from the two lowest flow rivers studied; however, each river flowed through relatively large and populous metropolitan areas (Boise, Idaho and Spokane, Washington). We used the volume of Wastewater Treatment Plant (WWTP) discharge, a known source of PBDEs, as a measure of human activity at a location, and combined with river flow (both converted to millions of gallons/day) created a novel approach (an approximate Dilution Index) to relate waterborne contaminants to levels of these contaminants that reach avian eggs. This approach provided a useful understanding of the spatial osprey egg concentration patterns observed. Individual osprey egg concentrations along the Upper Willamette River co-varied with the Dilution Index, while combined egg data (geometric means) from rivers or segments of rivers showed a strong, significant relationship to the Dilution Index with one exception, the Boise River. There, we believe osprey egg concentrations were lower than expected because Boise River ospreys foraged perhaps 50–75% of the time off the river at ponds and lakes stocked with fish that contained relatively low ΣPBDE concentrations. Our limited temporal data at specific localities (2004–2009) suggests that ΣPBDE concentrations in osprey eggs peaked between 2005 and 2007, and then decreased, perhaps in response to penta- and octa-PBDE technical mixtures no longer being used in the USA after 2004. Empirical estimates of biomagnification factors (BMFs) from fish to osprey eggs were 3.76–7.52 on a wet weight (ww) basis or 4.37–11.0 lipid weight. Our earlier osprey study suggested that ΣPBDE egg concentrations >1,000 ng/g ww may reduce osprey reproductive success. Only two of the study areas sampled in 2008–2009 contained individual eggs with ΣPBDE concentrations >1,000 ng/g, and non-significant (P > 0.30) negative relationships were found between ΣPBDEs and reproductive success. Additional monitoring is required to confirm not only the apparent decline in PBDE concentrations in osprey eggs that occurred during this study, but also to better understand the relationship between PBDEs in eggs and reproductive success.
Similar content being viewed by others
References
Anderson T, MacRae JD (2006) Polybrominated diphenyl ethers in fish and wastewater samples from an area of the Penobscot River in central Maine. Chemosphere 62:1153–1160
Batterman S, Chernyak S, Gwynn E, Cantonwine D, Jia C, Begnoche L, Hickey JP (2007) Trends of brominated diphenyl ethers in fresh and archived Great Lakes fish (1979–2005). Chemosphere 69:444–457
Blus LJ (1984) DDE in birds’ eggs: comparison of two methods for estimating critical levels. Wilson Bull 96:268–276
Braune BM, Mallory ML, Gilchrist HG, Letcher RJ, Drouillard KG (2007) Levels and trends of organochlorines and brominated flame retardants in ivory gull eggs from the Canadian Arctic, 1976–2004. Sci Total Environ 378:403–417
Chen D, Hale RC (2010) A global review of polybrominated diphenyl ether flame retardant contamination in birds. Environ Intern 36:800–811
Chen D, Hale RC, Watts BD, LaGuardia MJ, Harvey E, Mojica EK (2010) Species-specific accumulation of polybrominated diphenyl ether flame retardants in birds of prey from the Chesapeake Bay region, USA. Environ Pollut 158:1883–1889
de Wit CA (2002) An overview of brominated flame retardants in the environment. Chemosphere 46:583–624
Elliott JE, Wilson LK, Wakefield B (2005) Polybrominated diphenyl ether trends in eggs of aquatic and marine birds from British Columbia, Canada, 1979–2002. Environ Sci Technol 39:5584–5591
Elliott JE, Morrisey CA, Henny CJ, Ruelas E, Shaw P (2007) Satellite telemetry and prey sampling reveal contaminant sources to Pacific Northwest ospreys. Ecol Appl 17:1223–1233
Furl C, Meredith C (2010) PBT monitoring: PBDE flame retardants in Spokane River fish, 2009. Washington State Dept. Ecology, Publ. No. 10-03-015, Olympia, 55 pp
Gauthier LT, Hebert CE, Weseloh DVC, Letcher RJ (2007) Current use flame retardants in the eggs of herring gulls (Larus argentatus) from the Laurentian Great Lakes. Environ Sci Technol 41:4561–4567
Gauthier LT, Hebert CE, Weseloh DVC, Letcher RJ (2008) Dramatic changes in the temporal trends of polybrominated diphenyl ethers (PBDEs) in herring gull eggs from the Laurentian Great Lakes: 1982–2006. Environ Sci Technol 42:1524–1530
Gerecke AC, Hartmann PC, Kohler NV, Giger W, Schmid P, Zennegg M, Kohler M (2005) Anaerobic degradation of decabromodiphenyl ether. Environ Sci Technol 39:1078–1083
Hale RC, LaGuardia MJ, Harvey EP, Gaylor MO, Mainor TM, Duff WH (2001) Persistent pollutants in land-applied sludges. Nature 412:140–141
Henny CJ, Grove RA, Kaiser JL, Bentley VR (2004) An evaluation of osprey eggs to determine spatial residue patterns and effects of contaminants along the lower Columbia River, USA. In: Chancellor RD, Meyburg B-U (eds) Raptors Worldwide, Sixth World Conf Birds of Prey and Owls, WWGBP/MME, Budapest, Hungary, pp 369–388
Henny CJ, Grove RA, Kaiser JL (2008) Osprey distribution, abundance, reproductive success and contaminant burdens along the lower Columbia River, 1997/1998 versus 2004. Arch Environ Contam Toxicol 54:525–534
Henny CJ, Kaiser JL, Grove RA (2009a) PCDDs, PCDFs, PCBs, OC pesticides and mercury in fish and osprey eggs from the Willamette River, Oregon (1993, 2001 and 2006) with calculated biomagnification factors. Ecotoxicology 18:151–173
Henny CJ, Kaiser JL, Grove RA, Johnson BL, Letcher RJ (2009b) Polybrominated diphenyl ether flame retardants in eggs may reduce reproductive success of ospreys in Oregon and Washington, USA. Ecotoxicology 18:802–813
Henny CJ, Grove RA, Kaiser JL, Johnson BL (2010) North American osprey populations and contaminants: historic and contemporary perspectives. J Toxicol Environ Health Part B 13:579–603
Hollander M, Wolfe DA (1973) Nonparametric statistical methods. Wiley, New York
Johnson A, Seiders K, Deligeannis C, Kinney K, Sandvik P, Era-Miller B, Alkire D (2006) PBDE flame retardants in Washington rivers and lakes: concentrations in fish and water, 2005–06. Washington State Dept. Ecology, Publ. No. 06-03-027, Olympia, 102 pp
Johnson BL, Kaiser JL, Henny CJ, Grove RA (2008) Prey of nesting ospreys on Willamette and Columbia Rivers, Oregon and Washington. Northwest Sci 82:229–236
Kuo Y, Sepúlveda MS, Sutton TM, Ochoa-Acuňa HG, Muir AM, Miller B, Hua I (2010) Bioaccumulation and biotransformation of decabromodiphenyl ether and effects on daily growth in juvenile lake whitefish (Coregonus clupeaformis). Ecotoxicology 19:751–760
Manugian R (2004) Focus on interim chemical action plan for PBDE flame retardants. Washington State Dept. Ecology, Publ. No. 04-03-055, Olympia, 2 pp
Poole AF (1989) Ospreys: a natural and unnatural history. Cambridge University Press, Cambridge, 246 pp
Postupalsky S (1977) A critical review of problems in calculating osprey reproductive success. In: Ogden JC (ed) Transactions North American Osprey research conference, Transactions and Proceedings Series No. 2, National Park Service, Washington, DC, pp 1–11
Rayne S, Ikonomou MG, Antcliffe B (2003) Rapidly increasing polybrominated diphenyl ether concentrations in the Columbia River system from 1992–2000. Environ Sci Technol 37:2847–2854
Song M, Chu SG, Letcher RJ, Seth R (2006) Fate, partitioning and mass loading of polybrominated diphenyl ethers (PBDEs) during the municipal treatment processing of wastewater. Environ Sci Technol 40:6241–6246
Stapleton HM, Brazil B, Holbrook RD, Mitchelmore CL, Benedict R, Konstantinov A, Potter D (2006) In vivo and in vitro debromination of decabromodiphenyl ether (BDE 209) by juvenile rainbow trout and common carp. Environ Sci Technol 40:4653–4658
Stickel LF, Wiemeyer SN, Blus LJ (1973) Pesticide residues in eggs of wild birds: adjustment for loss of moisture and lipid. Bull Environ Contam Toxicol 9:193–196
Sullivan C, Mitchelmore CL, Hale RC, VanVeld PA (2007) Induction of CYP1A and DNA damage in the fathead minnow (Pimephales promelas) following exposure to biosolids. Sci Total Environ 384:221–228
Watts BD, Paxton BJ (2007) Ospreys of the Chesapeake Bay: population recovery, ecological requirements, and current threats. Waterbirds 30:39–49
Wydoski RS, Whitney RR (2003) Inland fishes of Washington, 2nd edn. University Washington Press, Seattle
Acknowledgments
We thank the electric utility companies (Avista, Inland Power and Light, Idaho Power, Emerald People’s Utility District, Eugene Water and Electric Board, Pacific Power and Light Company, Salem Electric, Portland General Electric Company, Consumers Power, Inc.) associated with all of the study areas for providing bucket trucks and personnel to access the nests on power poles. The US Coast Guard kindly permitted access to osprey nests built on navigation aids in the Columbia River. D. MacCoy (USGS) provided fish from the Boise River. We are grateful to the numerous landowners who permitted access to their property to survey nesting osprey. P. Haggerty (USGS) and C. Meredith (WSDE) kindly drafted the study area maps. D. Wise (USGS) provided Wastewater Treatment Plant discharge information. We acknowledge L. Periard and L. Gauthier in the Letcher Research Group (at NWRC, Ottawa) for chemical analysis of PBDEs. An earlier draft of the manuscript was improved by comments from G. Heinz, B. Rattner and R. Lazarus (all USGS). The study was funded by the US Geological Survey with the Spokane River study area partially funded by Washington State Department of Ecology. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the US Government or State of Washington.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Henny, C.J., Grove, R.A., Kaiser, J.L. et al. Wastewater dilution index partially explains observed polybrominated diphenyl ether flame retardant concentrations in osprey eggs from Columbia River Basin, 2008–2009. Ecotoxicology 20, 682–697 (2011). https://doi.org/10.1007/s10646-011-0608-2
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-011-0608-2