Advertisement

Ecotoxicology

, Volume 27, Issue 5, pp 605–618 | Cite as

Patterns and trends in lead (Pb) concentrations in bald eagle (Haliaeetus leucocephalus) nestlings from the western Great Lakes region

  • Jason E. Bruggeman
  • William T. Route
  • Patrick T. Redig
  • Rebecca L. Key
Article

Abstract

Most studies examining bald eagle (Haliaeetus leucocephalus) exposure to lead (Pb) have focused on adults that ingested spent Pb ammunition during the fall hunting season, often at clinical or lethal levels. We sampled live bald eagle nestlings along waterbodies to quantify Pb concentrations in 3 national park units and 2 nearby study areas in the western Great Lakes region. We collected 367 bald eagle nestling feather samples over 8 years during spring 2006-2015 and 188 whole blood samples over 4 years during spring 2010-2015. We used Tobit regression models to quantify relationships between Pb concentrations in nestling feathers and blood using study area, year, and nestling attributes as covariates. Pb in nestling feather samples decreased from 2006 to 2015, but there was no trend for Pb in blood samples. Pb concentrations in nestling feather and blood samples were significantly higher in study areas located closer to and within urban areas. Pb in feather and blood samples from the same nestling was positively correlated. Pb in feathers increased with nestling age, but this relationship was not observed for blood. Our results reflect how Pb accumulates in tissues as nestlings grow, with Pb in feathers and blood indexing exposure during feather development and before sampling, respectively. Some nestlings had Pb concentrations in blood that suggested a greater risk to sublethal effects from Pb exposure. Our data provides baselines for Pb concentrations in feathers and blood of nestling bald eagles from a variety of waterbody types spanning remote, lightly populated, and human-dominated landscapes.

Key words

Bald eagle nestlings Blood and feather samples Censored data Haliaeetus leucocephalus Lead (Pb) pollution National Park Service 

Notes

Acknowledgements

We thank the many employees and volunteers at the national parks that assisted with logistics and field sampling. We also appreciate the in-kind support of state, federal, tribal, and non-governmental partners. We thank D. Andersen, J. Glase, B. Lafrancois, C. Morris, D. VanderMeulen, and 2 anonymous reviewers for their technical review of earlier drafts of the manuscript. Use of trade names does not imply endorsement by the U.S. Government or the University of Minnesota.

Funding

Major funding was provided by the U.S. National Park Service, Great Lakes Inventory and Monitoring Network, the National Park Service Biological Resources Division, and the Minnesota Pollution Control Agency. The Wisconsin Department of Natural Resources and Ramsey County (MN) Parks and Recreation provided in-kind support for bald eagle occupancy and productivity flights. JEB was supported as a Research Fellow during data analysis and manuscript preparation at the U.S. Geological Survey, Minnesota Cooperative Fish and Wildlife Research Unit at the University of Minnesota.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

10646_2018_1933_MOESM1_ESM.docx (49 kb)
Supplementary material 1
10646_2018_1933_MOESM2_ESM.docx (4.6 mb)
Supplementary material 2
10646_2018_1933_MOESM3_ESM.docx (155 kb)
Supplementary material 3

References

  1. Akritas MG, Murphy SA, Lavalley MP (1995) The Theil-Sen estimator with doubly censored data and applications to astronomy. J Am Stat Assoc 90(429):170–177CrossRefGoogle Scholar
  2. Anthony RG, Garrett MG, Schuler CA (1993) Environmental contaminants in bald eagles in the Columbia River estuary. J Wildl Manage 57:10–19CrossRefGoogle Scholar
  3. Arenal CA, Halbrook RS (1997) PCB and heavy metal contamination and effects in European starlings (Sturnus vulgaris) at a superfund site. Bull Environ Contam Toxicol 58:254–262CrossRefGoogle Scholar
  4. Avery D, Watson RT (2009) Regulation of lead-based ammunition around the world. In: Watson RT, Fuller M, Pokras M, Hunt WG (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, pp 161–168Google Scholar
  5. Bates D, Maechler M, Bolker B, Walker S, Haubo Bojesen Christensen R, Singmann H, and Dai B (2015) Package ‘LME4’ version 1.1-7, linear-mixed effects models using Eigen and S4. http://lme4.r-forge.r-project.org/. Accessed 18 Feb 2015
  6. Beyer WN, Pattee OH, Sileo L, Hoffman DJ, Mulhern BM (1985) Metal contamination in wildlife living near two zinc smelters. Environ Pollut A 38:63–86CrossRefGoogle Scholar
  7. Blanco G, Frías O, Jiménez B, Gómez G (2003) Factors influencing variability and potential uptake routes of heavy metals in black kites exposed to emissions from a solid-waste incinerator. Environ Toxicol Chem 22:2711–2718CrossRefGoogle Scholar
  8. Blus LJ (2011) DDT, DDD, and DDE in birds. In: Beyer WN, Meador JP (eds) Environmental contaminants in biota: interpreting tissue concentrations. CRC, Boca Raton, p 425–446CrossRefGoogle Scholar
  9. Bortolotti GR (1986) Influence of sibling competition on nestling sex ratios of sexually dimorphic birds. Am Nat 127:495–507CrossRefGoogle Scholar
  10. Burger J (1993) Metals in avian feathers: bioindicators of environmental pollution. Rev Environ Toxicol 5:203–311Google Scholar
  11. Burger J (1995) A risk assessment for lead in birds. J Toxicol Environ Health 45:369–396CrossRefGoogle Scholar
  12. Burger J, Gochfeld M (1990) Tissue levels of lead in experimentally exposed herring gull (Larus argentatus) chicks. J Toxicol Environ Health 29:219–233CrossRefGoogle Scholar
  13. Burger J, Gochfeld M (2000) Effects of lead on birds (Laridae): a review of laboratory and field studies. J Toxicol Environ Health 3:59–78CrossRefGoogle Scholar
  14. Burger J, Gotchfeld M (2005) Effects of lead on learning in herring gulls: an avian wildlife model for neurobehavioral deficits. Neurotoxicology 26:615–624CrossRefGoogle Scholar
  15. Burger J, Gotchfeld M (2009) Comparison of arsenic, cadmium, chromium, lead, manganese, mercury and selenium in feathers in bald eagle (Haliaeetus leucocephalus), and comparison with common eider (Somateria mollissima), glaucous-winged gull (Larus glaucescens), pigeon guillemot (Cepphus columba), and tufted puffin (Fratercula cirrhata) from the Aleutian Chain of Alaska. Environ Monit Assess 152:357–367CrossRefGoogle Scholar
  16. Burnham KP, Anderson DR (2002) Model selection and multi-model inference. Springer, NewYorkGoogle Scholar
  17. Cade TJ (2007) Exposure of California condors to lead from spent ammunition. J Wildl Manage 71:2125–2133CrossRefGoogle Scholar
  18. Canfield RL, Henderson CR, Cory-Slechta DA, Cox C, Jusko TA, Lanphear BP (2003) Intellectual impairment in children with blood lead concentrations below 10 µg per deciliter. N Engl J Med 348:1517–1526CrossRefGoogle Scholar
  19. Chen CY, Stemberger RS, Klaue B, Blum JD, Pickhardt PC, Folt CL (2000) Accumulation of heavy metals in food web components across a gradient of lakes. Limnol Oceanogr 45:1525–1536CrossRefGoogle Scholar
  20. Cruz LM, Redig PT, Deen J (2012) Lead from spent ammunition: a source of exposure and poisoning in bald eagles. Hum-Wildl Interact 6:94–104Google Scholar
  21. Dauwe T, Bervoets L, Pinxten R, Blust R, Eens M (2003) Variation of heavy metals within and among feathers of birds of prey: effects of molt and external contamination. Environ Pollut 124:429–436CrossRefGoogle Scholar
  22. Dunstan TC, Harper JF (1975) Food habits of bald eagles in north-central Minnesota. J Wildl Manage 39:140–143CrossRefGoogle Scholar
  23. Dykstra CR, Meyer MW, Stromborg KL, Warnke DK, Bowerman WW, Best DA (2001) Association of low reproductive rates and high contaminant levels in bald eagles on Green Bay, Lake Michigan. J Gt Lakes Res 27:239–251CrossRefGoogle Scholar
  24. Dykstra CR, Meyer MW, Rasmussen PW, Warnke DK (2005) Contaminant concentrations and reproductive rate of Lake Superior bald eagles, 1989-2011. J Gt Lakes Res 31:227–235CrossRefGoogle Scholar
  25. Dykstra CR, Route WT, Meyer MW, Rasmussen PW (2010) Contaminant concentrations in bald eagles nesting on Lake Superior, the upper Mississippi River, and the St. Croix River. J Gt Lakes Res 36:561–569CrossRefGoogle Scholar
  26. Ecke F, Singh NJ, Arnemo JM, Bignert A, Helander B, Berglund AMM, Borg H, Bröjer C, Holm K, Lanzone M, Miller T, Nordström A, Räikkönen J, Rodushkin I, Agren E, Hörnfeldt B (2017) Sublethal lead exposure alters movement behavior in free-ranging golden eagles. Environ Sci Technol 51:5729–5736CrossRefGoogle Scholar
  27. Edelsein S, Fullmer CS, Wasserman RH (1984) Gastrointestinal absorption of lead in chicks: involvement of the cholecalciferol endocrine system. J Nutr 114:692–700CrossRefGoogle Scholar
  28. Elliott JE, Butler RW, Norstrom RJ, Whitehead PE (1989) Environmental contaminants and reproductive success of great blue herons Ardea Herodias in British Columbia, 1986-87. Environ Pollut 59:91–114CrossRefGoogle Scholar
  29. Elliott JE, Harris ML (2001) An ecotoxicological assessment of chlorinated hydrocarbon effects on bald eagle populations. Rev Toxicol 4:1–60Google Scholar
  30. Elliott KH, Cesh LS, Dooley JA, Letcher RJ, Elliott JE (2009) PCBs and DDE, but not PBDEs, increase with trophic level and marine input in nestling bald eagles. Sci Tot Environ 407:3867–3875CrossRefGoogle Scholar
  31. Eulares I, Covaci A, Herzke D, Eens M, Sonne C, Moum T, Schnug L, Are Hanssen S, Vidar Johnsen T, Ove Bustnes J, Jaspers VLB (2011) A first evaluation of the usefulness of feathers of nestling predatory birds for non-destructive biomonitoring of persistent organic pollutants. Environ Int 37:622–630CrossRefGoogle Scholar
  32. Fallon JA, Redig P, Miller TA, Lanzone M, Katzner T (2017) Guidelines for evaluation and treatment of lead poisoning of wild raptors. Wildl Soc B 41:205–211CrossRefGoogle Scholar
  33. Fisher IJ, Pain DJ, Thomas VG (2006) A review of lead poisoning from ammunition sources in terrestrial birds. Biol Conserv 131:421–432CrossRefGoogle Scholar
  34. Franson JC, Russell RE (2014) Lead and eagles: demographic and pathological characteristics of poisoning, and exposure levels associated with other causes of mortality. Ecotoxicology 23:1722–1731CrossRefGoogle Scholar
  35. Franson JC, Pain DJ (2011) Lead in birds. In: Beyer WN, Meador JP (eds) Environmental contaminants in biota: interpreting tissue concentrations. CRC, Boca Raton, p 563–583CrossRefGoogle Scholar
  36. Fullmer CS (1991) Intestinal calcium and lead absorption: effects of dietary lead and calcium Environ Res 54:159–169CrossRefGoogle Scholar
  37. Furness RW (1993) Birds as monitors of pollutants. In: Furness RW, Greenwood JJD (eds) Birds as monitors of environmental change. Chapman and Hall, New York, p 86–143CrossRefGoogle Scholar
  38. Gangoso L, Álvarez-Lloret P, Rodríguez-Navarro AAB, Mateo R, Hiraldo F, Donázar JA (2009) Long-term effects of lead poisoning on bone mineralization in vultures exposed to ammunition sources. Environ Pollut 157:569–574CrossRefGoogle Scholar
  39. Grier JW (1982) Ban of DDT and subsequent recovery of reproduction in bald eagles. Science 218:1232–1235CrossRefGoogle Scholar
  40. Harris ML, Elliott JE (2011) Effects of polychlorinated biphenyls, dibenzo-p-dioxins and dibenzofurans, and polybrominated diphenyl ethers in wild birds. In: Beyer WN, Meador JP (eds) Environmental contaminants in biota: interpreting tissue concentrations. CRC, Boca Raton, p 477–530CrossRefGoogle Scholar
  41. Helsel DR (2006) Fabricating data: how substituting values for nondetects can ruin results, and what can be done about it. Chemosphere 65:2434–2439CrossRefGoogle Scholar
  42. Helsel DR (2012) Statistics for censored environmental data using Minitab and R. Wiley, New JerseyGoogle Scholar
  43. Hunt WG (2012) Implications of sublethal lead exposure in avian scavengers. J Raptor Res 46:389–393CrossRefGoogle Scholar
  44. Hunt WG, Burnham W, Parish CN, Burnham KK, Mutch B, Oaks JL (2006) Bullet fragments in deer remains: implications for lead exposure in avian scavengers. Wildl Soc B 34:167–170CrossRefGoogle Scholar
  45. Jackson AK, Evers DC, Adams EM, Cristol DA, Eagles-Smith C, Edmonds ST, Gray CE, Hoskins B, Lane OP, Sauer A, Tear T (2015) Songbirds as sentinels of mercury in terrestrial habitats of eastern North America. Ecotoxicology 24:453–467CrossRefGoogle Scholar
  46. Jacobs DE, Clickner RP, Zhou JY, Viet SM, Marker DA, Rogers JW, Zeldin DC, Broene P, Friedman W (2002) The prevalence of lead-based paint hazards in U.S. housing. Environ Health Perspect 110:A599–A606CrossRefGoogle Scholar
  47. Kozie KD, Anderson RK (1991) Productivity, diet, and environmental contaminants in bald eagles nesting near the Wisconsin shoreline of Lake Superior. Arch Environ Contam Toxicol 20:41–48CrossRefGoogle Scholar
  48. Kramer JL, Redig PT (1997) Sixteen years of lead poisoning in eagles, 1980-95: an epizootiologic view. J Raptor Res 31:327–332Google Scholar
  49. Lee L (2015) Package ‘NADA’ version 1.5-6, nondetects and data analysis for environmental data. http://www.r-project.org/. Accessed 12 Feb 2015
  50. Livingston SA, Todd CS, Krohn WB, Owen Jr RB (1990) Habitat models for nesting bald eagles in Maine. J Wildl Manage 54:644–653CrossRefGoogle Scholar
  51. Meyer E, Sparling D, Blumenshine S (2013) Regional inhibition of cholinesterase in free-ranging western pond turtles (Emys marmorata) occupying California mountain streams. Environ Toxicol Chem 32:692–698CrossRefGoogle Scholar
  52. Mykkanen HM, Wasserman RH (1981) Gastrointestinal absorption of lead (203Pb) in chicks: influence of lead, calcium and age. J Nutr 111:1757–1765CrossRefGoogle Scholar
  53. Pain DJ, Fisher IJ, Thomas VG (2009) A global update of lead poisoning in terrestrial birds from ammunition sources. In: Watson RT, Fuller M, Pokras M, Hunt WG (eds) Ingestion of lead from spent ammunition: implications for wildlife and humans. The Peregrine Fund, Boise, pp 99–118Google Scholar
  54. Pittman HT, Bowerman WW, Grim LH, Grubb TG, Bridges WC (2011) Using nestling feathers to assess spatial and temporal concentrations of mercury in bald eagles at Voyageurs National Park, Minnesota, USA. Ecotoxicology 20:1626–1635CrossRefGoogle Scholar
  55. Pittman HT, Bowerman WW, Grim LH, Grubb TG, Bridges WC, Wierda MR (2015) Using nestling plasma to assess long-term spatial and temporal concentrations of organochlorine compounds in bald eagles within Voyageurs National Park, Minnesota, USA. Chemosphere 123:79–86CrossRefGoogle Scholar
  56. Pokras MA, Kneeland MR (2009) Understanding lead uptake and effects across species lines: a conservation medicine based approach. In: Watson RT, Fuller M, Pokras M, Hunt WG (eds) Ingestion of lead from spent ammunition: Implications for wildlife and humans. The Peregrine Fund, Boise, Idaho, p 7–22Google Scholar
  57. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org/. Accessed 16 Jan 2015Google Scholar
  58. Rattner BA, Franson JC, Sheffield SR, Goddard CI, Leonard NJ, Stang D, Wingate PJ (2008) Sources and implications of lead-based ammunition and fishing tackle to natural resources. Wildlife Society Technical Review. The Wildlife Society, Bethesda, MarylandGoogle Scholar
  59. Rattner BA, Scheuhammer AM, Elliott JE (2011) History of wildlife toxicology and the interpretation of contaminant concentrations in tissues. In: Beyer WN, Meador JP (eds) Environmental contaminants in biota: interpreting tissue concentrations. CRC, Boca Raton, p 9–46CrossRefGoogle Scholar
  60. Route B, Elias J (2007) Long-term Ecological Monitoring Plan, Great Lakes Inventory and Monitoring Network, Natural Resource Report NPS/GLKN/NRR-2007-001. National Park Service, Fort Collins, Colorado. https://science.nature.nps.gov/im/units/glkn/publications.cfm?tab=4
  61. Route B, Bowerman W, Kozie K (2009) Protocol for monitoring environmental contaminants in bald eagles, Version 1.2: Great Lakes Inventory and Monitoring Network, Natural Resource Report NPS/GLKN/NRR-2009/092. National Park Service, Fort Collins, Colorado. https://science.nature.nps.gov/im/units/glkn/publications.cfm?tab=3
  62. Route WT, Dykstra CR, Rasmussen PW, Key RL, Meyer MW, Mathew J (2014a) Patterns and trends in brominated flame retardants in bald eagle nestlings from the upper Midwestern United States. Environ Sci Technol 48:12516–12524CrossRefGoogle Scholar
  63. Route WT, Russell RE, Lindstom AB, Strynar MH, Key RL (2014b) Spatial and temporal patterns in concentrations of perfluorinated compounds in bald eagle nestlings in the upper midwestern United States. Environ Sci Technol 48:6653–6660CrossRefGoogle Scholar
  64. Rutkiewicz J, Nam D, Cooley T, Neumann K, Bueno Padilla I, Route W, Strom S, Basu N (2011) Mercury exposure and neurochemical impacts in bald eagles across several Great Lakes states. Ecotoxicology 20:1669–1676CrossRefGoogle Scholar
  65. Sánchez-Chardi A, Nadal J (2007) Bioaccumulation of metals and effects of landfill pollution in small mammals. Part I. The greater white-toothed shrew. Crocidura russula Chemosphere 68:703–711CrossRefGoogle Scholar
  66. Scheuhammer AM (1987) The chronic toxicity of aluminum, cadmium, mercury, and lead in birds: a review. Environ Pollut 46:263–295CrossRefGoogle Scholar
  67. Scheuhammer AM, Norris SL (1996) The ecotoxicology of lead shot and lead fishing weights. Ecotoxicology 5:279–295CrossRefGoogle Scholar
  68. Shore RF, Pereira MG, Walker LA, Thompson DR (2011) Mercury in nonmarine birds and mammals. In: Beyer WN, Meador JP (eds) Environmental contaminants in biota: interpreting tissue concentrations. CRC, Boca Raton, p 609–626CrossRefGoogle Scholar
  69. Spahn SA, Sherry TW (1999) Cadmium and lead exposure associated with reduced growth rates, poorer fledging success of little blue heron chicks (Egretta cerulean) in south Louisiana wetlands. Arch Environ Contam Toxicol 37:377–384CrossRefGoogle Scholar
  70. Stalmaster MV (1987) The bald eagle. University Books, New YorkGoogle Scholar
  71. Steidl RJ, Griffin CR, Niles LJ (1991) Contaminant levels of osprey eggs and prey reflect regional differences in reproductive success. J Wildl Manage 55:601–608CrossRefGoogle Scholar
  72. Therneau TM (2015) Package ‘SURVIVAL’ version 2.38-3, survival analysis. http://www.r-forge.r-project.org/. Accessed 16 Jan 2015
  73. Tobin J (1958) Liquidity preference as behavior towards risk. Rev Econ Stud 25:65–86CrossRefGoogle Scholar
  74. Tsipoura N, Burger J, Newhouse M, Jeitner C, Gochfeld M, Mizrahi D (2011) Lead, mercury, cadmium, chromium, and arsenic levels in eggs, feathers, and tissues of Canada geese of the New Jersey Meadowlands. Environ Res 111:775–784CrossRefGoogle Scholar
  75. U.S. Department of Health and Human Services (2000) Health consultation: Pigs Eye Landfill, St. Paul, Ramsey County, Minnesota, Cerclis No. MND980609085. Division of Health Assessment and Consultation, Atlanta, GeorgiaGoogle Scholar
  76. U.S. Environmental Protection Agency (USEPA) (1996) Method 1638: determination of trace elements in ambient waters by inductively coupled plasma-mass spectrometry. U.S. Environmental Protection Agency, Washington, DCGoogle Scholar
  77. U.S. Environmental Protection Agency (USEPA) (2013) Integrated Science Assessment for lead. EPA/600/R-10/075F, U.S. Environmental Protection Agency, Research Triangle Park, North CarolinaGoogle Scholar
  78. U.S. Environmental Protection Agency (USEPA) (2015) National trends in lead levels. http://www3.epa.gov/airtrends/lead.html. Accessed 1 Nov 2015
  79. Venier M, Wierda M, Bowerman WW, Hites RA (2010) Flame retardants and organochlorine pollutants in bald eagle plasma from the Great Lakes region. Chemosphere 80:1234–1240CrossRefGoogle Scholar
  80. Warner SE, Britton EE, Becker DN, Coffey MJ (2014) Bald eagle lead exposure in the upper Midwest. J Fish Wildl Manage 5:208–216CrossRefGoogle Scholar
  81. Wasserman RH, Taylor AN (1968) Vitamin D-dependent calcium-binding protein: response to some physiological and nutritional variables. J Biol Chem 243:3987–3993Google Scholar
  82. Watson JW, Garrett MG, Anthony RG (1991) Foraging ecology of bald eagles in the Columbia River estuary. J Wildl Manage 55:492–499CrossRefGoogle Scholar
  83. Wiemeyer SN, Frenzel RW, Anthony RG, McClelland BR, Knight RL (1989) Environmental contaminants in blood of western bald eagles. J Raptor Res 23:140–146Google Scholar
  84. Wood PB, White JH, Steffer A, Wood JM, Facemire CF, Percival HF (1996) Mercury concentrations in tissues of Florida bald eagles. J Wildl Manage 60:178–185CrossRefGoogle Scholar
  85. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Jason E. Bruggeman
    • 1
  • William T. Route
    • 2
  • Patrick T. Redig
    • 3
  • Rebecca L. Key
    • 2
  1. 1.Minnesota Cooperative Fish and Wildlife Research Unit, Department of Fisheries, Wildlife and Conservation BiologyUniversity of MinnesotaSt. PaulUSA
  2. 2.U.S. National Park Service, Great Lakes Inventory and Monitoring NetworkAshlandUSA
  3. 3.The Raptor CenterUniversity of MinnesotaSt. PaulUSA

Personalised recommendations