Skip to main content

Application of Stable Isotopic Ratio Analysis to Identify the Cause of Acute Versus Chronic Lead Poisoning of a Tundra Swan (Cygnus columbianus): A Case Study

Abstract

We utilized lead (Pb) stable isotopes to identify the source of acute Pb poisoning in a Tundra Swan (Cygnus columbianus) and evaluated overall Pb exposure. Upon necropsy, we obtained samples of blood, liver, kidney, heart, thigh, breast, femur, and metallic objects (i.e., fishing sinker, spring and swivels) from the gizzard for Pb isotopic analysis. Pb isotope ratios of blood and soft tissues were essentially identical to the Pb ratios of the sinker, the likely source of acute poisoning. The spring and swivels had lower Pb content and ratios distinct from tissue, suggesting no significant contribution to poisoning. Femur Pb isotopic composition was the most distinct biological sample and indicative of a combination of sources. These results demonstrate isotopic analysis as a viable method for determining the source of acute Pb poisoning, and that Pb isotope ratios in bone most likely record a lifetime-averaged metric of Pb exposure.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Bell K, Blenkinsop J (1981) A geochronological study of the Buchans Area, Newfoundland. In: Swanson EA, Strong DF, Thurlow JG (eds) The Buchans Orebodies: fifty years of geology and mining, vol Special Paper 22. Geological Association of Canada, pp 91–111

  2. Binkowski LJ, Meissner W, Trzeciak M, Izevbekhai K, Barker J (2016) Lead isotope ratio measurements as indicators for the source of lead poisoning in Mute swans (Cygnus olor) wintering in Puck Bay (northern Poland). Chemosphere 164:436–442. https://doi.org/10.1016/j.chemosphere.2016.08.120

    CAS  Article  Google Scholar 

  3. Bollhofer A, Rosman KJR (2001) Lead isotopic ratios in European atmospheric aerosols. Phys Chem Earth B 26:835–838. https://doi.org/10.1016/S1464-1909(01)00094-6

    Article  Google Scholar 

  4. Cade TJ (2007) Exposure of California condors to lead from spent ammunition. J Wildl Manag 71:2125–2133. https://doi.org/10.2193/2007-084

    Article  Google Scholar 

  5. Cai F, Calisi RM (2016) Seasons and neighborhoods of high lead toxicity in New York City: the feral pigeon as a bioindicator. Chemosphere 161:274–279. https://doi.org/10.1016/j.chemosphere.2016.07.002

    CAS  Article  Google Scholar 

  6. Church ME et al (2006) Ammunition is the principal source of lead accumulated by California condors re-introduced to the wild. Environ Sci Technol 40:6143–6150. https://doi.org/10.1021/es060765s

    CAS  Article  Google Scholar 

  7. Cid FD, Fernández NC, Pérez-Chaca MV, Pardo R, Caviedes-Vidal E, Chediack JG (2018) House sparrow biomarkers as lead pollution bioindicators. Evaluation of dose and exposition length on hematological and oxidative stress parameters. Ecotoxicol Environ Saf 154:154–161. https://doi.org/10.1016/j.ecoenv.2018.02.040

    CAS  Article  Google Scholar 

  8. Clemens ET, Krook L, Aronson AL, Stevens CE (1975) Pathogenesis of lead shot poisoning in the mallard duck. Cornell Vet 65:248–285

    CAS  Google Scholar 

  9. Cretacci Y, Parsons PJ (2010) Localized accumulation of lead within and among bones from lead-dosed goats. Environ Res 110:26–32. https://doi.org/10.1016/j.envres.2009.09.005

    CAS  Article  Google Scholar 

  10. Degernes L et al (2006) Epidemiologic investigation of lead poisoning in trumpeter and tundra swans in Washington state, USA, 2000–2002. J Wildl Dis 42:345–358. https://doi.org/10.7589/0090-3558-42.2.345

    Article  Google Scholar 

  11. Diaz-Somoano M et al (2009) Stable lead isotope compositions in selected coals from around the world and implications for present day aerosol source tracing. Environ Sci Technol 43:1078–1085. https://doi.org/10.1021/es801818r

    CAS  Article  Google Scholar 

  12. Doe BR, Delevaux MH (1972) Source of lead in Southeast Missouri galena ores. Econ Geol 67:409–425. https://doi.org/10.2113/gsecongeo.67.4.409

    CAS  Article  Google Scholar 

  13. Fallon JA, Redig P, Miller TA, Lanzone M, Katzner T (2017) Guidelines for evaluation and treatment of lead poisoning of wild raptors. Wildl Soc Bull 41:205–211. https://doi.org/10.1002/wsb.762

    Article  Google Scholar 

  14. Field JD, Appold MS, Renson V, Coveney RM (2018) Lead and sulfur isotope composition of trace occurrences of Mississippi Valley-type mineralization in the U.S. midcontinent. J Geochem Explor 184:66–81. https://doi.org/10.1016/j.gexplo.2017.10.011

    CAS  Article  Google Scholar 

  15. Finkelstein ME et al (2010) Feather lead concentrations and 207Pb/206Pb ratios reveal lead exposure history of California condors (Gymnogyps californianus). Environ Sci Technol 44:2639–2647. https://doi.org/10.1021/es903176w

    CAS  Article  Google Scholar 

  16. Finkelstein ME, Kuspa ZE, Welch A, Eng C, Clark M, Burnett J, Smith DR (2014) Linking cases of illegal shootings of the endangered California condor using stable lead isotope analysis. Environ Res 134:270–279. https://doi.org/10.1016/j.envres.2014.07.022

    CAS  Article  Google Scholar 

  17. Fisher IJ, Pain DJ, Thomas VG (2006) A review of lead poisoning from ammunition sources in terrestrial birds. Biol Conserv 131:421–432. https://doi.org/10.1016/j.biocon.2006.02.018

    Article  Google Scholar 

  18. Fleming DE, Boulay D, Richard NS, Robin JP, Gordon CL, Webber CE, Chettle DR (1997) Accumulated body burden and endogenous release of lead in employees of a lead smelter. Environ Health Perspect 105:224–233. https://doi.org/10.1289/ehp.97105224

    CAS  Article  Google Scholar 

  19. Franson JC, Hansen SP, Creekmore TE, Brand CJ, Evers DC, Duerr AE, DeStefano S (2003) Lead fishing weights and other fishing tackle in selected waterbirds. Waterbirds 26(345–352):348

    Google Scholar 

  20. Haig SM et al (2014) The persistent problem of lead poisoning in birds from ammunition and fishing tackle. Condor 116:408–428. https://doi.org/10.1650/Condor-14-36.1

    Article  Google Scholar 

  21. Helander B, Axelsson J, Borg H, Holm K, Bignert A (2009) Ingestion of lead from ammunition and lead concentrations in white-tailed sea eagles (Haliaeetus albicilla) in Sweden. Sci Total Environ 407:5555–5563. https://doi.org/10.1016/j.scitotenv.2009.07.027

    CAS  Article  Google Scholar 

  22. Hernández M, Margalida A (2009) Assessing the risk of lead exposure for the conservation of the endangered Pyrenean bearded vulture (Gypaetus barbatus) population. Environ Res 109:837–842. https://doi.org/10.1016/j.envres.2009.05.001

    CAS  Article  Google Scholar 

  23. Jacks G, Bystrom M, Johansson L (2001) Lead emissions from lost fishing sinkers. Boreal Env Res 6:231–236

    CAS  Google Scholar 

  24. Jochum KP, Nohl U, Herwig K, Lammel E, Stoll B, Hofmann AW (2005) GeoReM: a new geochemical database for reference materials and isotopic standards. Geostand Geoanal Res 29:333–338. https://doi.org/10.1111/j.1751-908X.2005.tb00904.x

    CAS  Article  Google Scholar 

  25. Kenntner N, Tataruch F, Krone O (2001) Heavy metals in soft tissue of white-tailed eagles found dead or moribund in Germany and Austria from 1993 to 2000. Environ Toxicol Chem 20:1831–1837. https://doi.org/10.1002/etc.5620200829

    CAS  Article  Google Scholar 

  26. Lambertucci SA, Donázar JA, Huertas AD, Jiménez B, Sáez M, Sanchez-Zapata JA, Hiraldo F (2011) Widening the problem of lead poisoning to a South-American top scavenger: lead concentrations in feathers of wild Andean condors. Biol Conserv 144:1464–1471. https://doi.org/10.1016/j.biocon.2011.01.015

    Article  Google Scholar 

  27. McClelland SC et al (2019) Sub-lethal exposure to lead is associated with heightened aggression in an urban songbird. Sci Total Environ 654:593–603. https://doi.org/10.1016/j.scitotenv.2018.11.145

    CAS  Article  Google Scholar 

  28. Millaku L, Imeri R, Trebicka A (2015) Bioaccumulation of heavy metals in tissues of house sparrow (Passer domesticus). Res J Environ Toxicol 9:107–112. https://doi.org/10.3923/rjet.2015.107.112

    Article  Google Scholar 

  29. Millen TM, Zartman RE, Van Heyl A, Survey G (1995) Lead isotopes from the Upper Mississippi Valley district: a regional perspective. U.S. Government Printing Office

  30. Nakhaee S, Amirabadizadeh A, Brent J, Mehrpour O (2019) Impact of chronic lead exposure on liver and kidney function and haematologic parameters. Basic Clin Pharmacol Toxicol 124:621–628. https://doi.org/10.1111/bcpt.13179

    CAS  Article  Google Scholar 

  31. Nilsson U, Attewell R, Christoffersson JO, Schutz A, Ahlgren L, Skerfving S, Mattsson S (1991) Kinetics of lead in bone and blood after end of occupational exposure. Pharmacol Toxicol 68:477–484. https://doi.org/10.1111/j.1600-0773.1991.tb01273.x

    CAS  Article  Google Scholar 

  32. Pain DJ, Mateo R, Green RE (2019) Effects of lead from ammunition on birds and other wildlife: a review and update. Ambio 48:935–953. https://doi.org/10.1007/s13280-019-01159-0

    Article  Google Scholar 

  33. Perrins CM, Cousquer G, Waine J (2003) A survey of blood lead levels in Mute Swans Cygnus olor. Avian Pathol 32:205–212. https://doi.org/10.1080/0307946021000071597

    CAS  Article  Google Scholar 

  34. Pokras MA, Chafel R (1992) Lead toxicosis from ingested fishing sinkers in adult common loons (Gavia immer) in New England. J Zoo Wildl Med 23:92–97

    Google Scholar 

  35. Potra A, Garmon WT, Samuelsen JR, Wulff A, Pollock ED (2018) Lead isotope trends and metal sources in the Mississippi Valley-type districts from the mid-continent United States. J Geochem Explor 192:174–186. https://doi.org/10.1016/j.gexplo.2018.07.002

    CAS  Article  Google Scholar 

  36. Rattner BA, Franson JC, Sheffield SR, Goddard CI, Leonard NJ, Stang D, Wingate PJ (2008) Sources and implications of lead ammunition and fishing tackle on natural resources, vol 08-01. Bethesda, Maryland

  37. Scheuhammer AM, Templeton DM (1998) Use of stable isotope ratios to distinguish sources of lead exposure in wild birds. Ecotoxicology 7:37–42. https://doi.org/10.1023/A:1008855617453

    CAS  Article  Google Scholar 

  38. Scheuhammer AM, Bond DE, Burgess NM, Rodrigue J (2003) Lead and stable lead isotope ratios in soil, earthworms, and bones of American woodcock (Scolopax minor) from eastern Canada. Environ Toxicol Chem 22:2585–2591. https://doi.org/10.1897/02-361

    CAS  Article  Google Scholar 

  39. Scott SR, Stanton NV, Gorski PR, Dahman C, Overdier JT, Shafer MM (2020) The effects of a known exposure source on Pb isotopes in bones from Pb-dosed cows. Appl Geochem 121:104699. https://doi.org/10.1016/j.apgeochem.2020.104699

    CAS  Article  Google Scholar 

  40. Sherman LS, Blum JD, Dvonch JT, Gratz LE, Landis MS (2015) The use of Pb, Sr, and Hg isotopes in Great Lakes precipitation as a tool for pollution source attribution. Sci Total Environ 502:362–374. https://doi.org/10.1016/j.scitotenv.2014.09.034

    CAS  Article  Google Scholar 

  41. Smith KE, Shafer MM, Weiss D, Anderson HA, Gorski PR (2017) High-precision (MC-ICPMS) isotope ratio analysis reveals contrasting sources of elevated blood lead levels of an adult with retained bullet fragments, and of his child, in Milwaukee, Wisconsin. Biol Trace Elem Res 177:33–42. https://doi.org/10.1007/s12011-016-0872-3

    CAS  Article  Google Scholar 

  42. Strelow FWE, Toerien FVS (1966) Separation of Lead(2) from Bismuth(3), Thallium(3), Cadmium(2), Mercury(2), Gold(3), Platinum(4), Palladium(2), and other elements by anion exchange chromatography. Anal Chem 38:545–548. https://doi.org/10.1021/Ac60236a006

    CAS  Article  Google Scholar 

  43. Thirlwall MF (2002) Multicollector ICP-MS analysis of Pb isotopes using a (207)pb-(204)pb double spike demonstrates up to 400 ppm/amu systematic errors in Tl-normalization. Chem Geol 184:255–279. https://doi.org/10.1016/S0009-2541(01)00365-5

    CAS  Article  Google Scholar 

  44. Thomas VG, Scheuhammer AM, Bond DE (2009) Bone lead levels and lead isotope ratios in red grouse from Scottish and Yorkshire moors. Sci Total Environ 407:3494–3502. https://doi.org/10.1016/j.scitotenv.2009.02.003

    CAS  Article  Google Scholar 

  45. Williams RJ, Holladay SD, Williams SM, Gogal RM (2018) Environmental lead and wild birds: a review. Rev Environ Contam Toxicol 245:157–180. https://doi.org/10.1007/398_2017_9

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This study was self-funded by the WSLH with integral cooperation of the DCHS Wildlife Center. This manuscript was greatly benefited by the comments of three anonymous reviewers.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Patrick R. Gorski.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gorski, P.R., Scott, S.R. & Lemley, E.M. Application of Stable Isotopic Ratio Analysis to Identify the Cause of Acute Versus Chronic Lead Poisoning of a Tundra Swan (Cygnus columbianus): A Case Study. Bull Environ Contam Toxicol 106, 250–256 (2021). https://doi.org/10.1007/s00128-020-03064-9

Download citation

Keywords

  • Lead isotopes
  • Avian toxicology
  • Waterfowl
  • Environmental lead
  • Fishing tackle