Skip to main content
SpringerLink
Log in

Perfluoroalkyl Contaminant Exposure and Effects in Tree Swallows Nesting at Clarks Marsh, Oscoda, Michigan, USA

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

Abstract

A site in northeastern Michigan, Oscoda Township, has some of the highest recorded exposure in birds to perfluorinated substances (PFASs) in the United States. Some egg and plasma concentrations at that location exceeded the lowest reproductive effect threshold established for two avian laboratory species. The objectives of this study were to determine whether there were reproductive effects or physiological responses in a model bird species, the tree swallow (Tachycineta bicolor), associated with this extremely high exposure to PFASs. The lack of exposure above background to other contaminants at this site allowed for an assessment of PFAS effects without the complication that responses may be caused by other contaminants. A secondary objective was to determine the distribution of PFASs in multiple tissue types to better understand and interpret residues in different tissues. This can best be done at highly exposed locations where tissue concentrations would be expected to be above detectable levels if they are present in that tissue. There were no demonstrable effects of PFAS exposure on reproduction nor on most physiological responses.

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

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • AVMA (2013) AVMA guidelines for the euthanasia of animals, 2013th edn. American Veterinary Medical Association, Schaumburg

    Google Scholar 

  • Beesoon S, Martin JW (2015) Isomer-specific binding affinity of perfluorooctanesulfonate (PFOS) and perfluorooactnoate (PFOA) to serum proteins. Environ Sci Technol 49:5722–5731. https://doi.org/10.1021/es505399w

    Article  CAS  Google Scholar 

  • Bermejo JL, Sauck WA, Atekwana EA (1997) Geophysical discovery of a new LNAPL plume at the former Wurtsmith AFB, Oscoda, Michigan. Groundw Monit Remediat 17:131–137. https://doi.org/10.1111/j.1745-6592.1997.tb01273

    Article  Google Scholar 

  • Boening DW (2000) Ecological effects, transport, and fate of mercury: a general review. Chemosphere 20:1335–1351

    Article  Google Scholar 

  • Butt CM, Berger U, Bossi R, Tomy GT (2010) Levels and trends of poly- and perfluorinated compounds in the arctic environment. Sci Total Environ 408:2936–2965

    Article  CAS  Google Scholar 

  • Clarke RK, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. Plymouth Marine Laboratory, UK

  • Custer CM (2011) Swallows as a sentinel species for contaminant exposure and effect studies. In: Elliott JE, Bishop CA, Morrissey CA (eds) Wildlife ecotoxicology: forensic approaches, emerging topics in ecotoxicology: book, vol 3, pp 45–91. https://doi.org/10.1007/978-0-387-89432-4_3

    Google Scholar 

  • Custer CM, Custer TW, Allen PD, Stromborg KL, Melancon NJ (1998) Reproduction and environmental contamination in tree swallows nesting in the Fox River drainage and Green Bay, Wisconsin, USA. Environ Toxicol Chem 17:1765–1987

    Article  Google Scholar 

  • Custer CM, Custer TW, Dummer PM, Munney KL (2003) Exposure and effects of chemical contaminants on tree swallows nesting along the Housatonic River, Berkshire County, Massachusetts, USA, 1998–2000. Environ Toxicol Chem 22:1605–1621

    CAS  Google Scholar 

  • Custer CM, Custer TW, Schoenfuss HL, Poganski BH, Solem L (2012) Exposure and effects of perfluoroalkyl compounds on tree swallows nesting at Lake Johanna in eastcentral Minnesota, USA. Reprod Toxicol 33(4):556–562. https://doi.org/10.1016/j.reprotox.2011.01.005

    Article  CAS  Google Scholar 

  • Custer TW, Dummer PM, Custer CM et al (2013) Perfluorinated compound concentrations in great blue heron eggs near St. Paul, Minnesota USA in 1993 and 2010–2011. Environ Toxicol Chem 32:1077–1083. https://doi.org/10.1002/etc.2146

    Article  CAS  Google Scholar 

  • Custer CM, Custer TW, Dummer PM et al (2014) Exposure and effects of perfluoroalkyl substances in tree swallows nesting in Minnesota and Wisconsin, USA. Arch Environ Contam Toxicol 66:120–138. https://doi.org/10.1007/s00244-013-9934-0

    Article  CAS  Google Scholar 

  • Custer TW, Custer CM, Dummer PM et al (2017a) Organic contamination in tree swallow (Tachycineta bicolor) nestlings at United States and Binational Great Lakes Areas of Concern. Environ Toxicol Chem 36:735–748. https://doi.org/10.1002/etc.3598

    Article  CAS  Google Scholar 

  • Custer TW, Custer CM, Dummer PM (2017b) EROD activity, chromosomal damage, and oxidative stress in response to contaminant exposure to tree swallows (Tachycineta bicolor) nesting in Great Lakes Areas of Concern. Ecotoxicology 26:1392–1407

    Article  CAS  Google Scholar 

  • Custer CM, Custer TW, Etterson MA et al (2018) Reproductive success and contaminant associations in tree swallows (Tachycineta bicolor) used to assess a Beneficial Use Impairment in U.S. and Binational Great Lakes’ Areas of Concern. Ecotoxicology 27:457–476

    Article  CAS  Google Scholar 

  • Dauwe T, Van de Vijver K, De Coen W, Eens W (2007) PFOS levels in the blood and liver of a small insectivorous songbird near a fluorochemical plant. Environ Int 33:357–361

    Article  Google Scholar 

  • European Food Safety Authority (2008) Perfluorooctane sulfonate (PFOS), perfluorooctanoic acid (PFOA) and their salts. EFSA J 653:1–131

    Google Scholar 

  • Gebbink WA, Letcher RJ (2012) Comparative tissue and body compartment accumulation and maternal transfer of eggs of perfluoroalkyl sulfonates and carboxylates in Great Lakes herring gulls. Environ Pollut 162:40–47

    Article  CAS  Google Scholar 

  • Giesy JP, Kannan K (2001) Global distribution of perfluorooctane sulfonate in wildlife. Environ Sci Technol 35:1339–1342

    Article  CAS  Google Scholar 

  • Groffen T, Lopez-Antia A, D’Hollander W et al (2017) Perfluoroalkylated acids in the eggs of great tits (Parus major) near a fluorochemical plant in Flanders, Belgium. Environ Pollut 228:140–148

    Article  CAS  Google Scholar 

  • Groffen T, Lasters R, Lopez-Antia A et al (2019) Limited reproductive impairment in a passerine bird species exposed along a perfluoroalkyl acid (PFAA) pollution gradient. Sci Total Environ 652:718–728

    Article  Google Scholar 

  • Han X, Snow TA, Kemper RA, Jepsen GW (2003) Binding of perfluorooctanoic acid to rat and human plasma proteins. Chem Res Toxicol 16:775–781

    Article  CAS  Google Scholar 

  • Haukås M, Berger U, Hop H et al (2007) Bioaccumulation of per-and polyfluorinated alkyl substances (PFAS) in selected species from the Barents Sea food web. Environ Pollut 148:360–371

    Article  Google Scholar 

  • Holmström KE, Berger U (2008) Tissue distribution of perfluorinated surfactants in common guillemot (Uria aalge) from the Baltic Sea. Environ Sci Technol 42:5879–5884

    Article  Google Scholar 

  • Kammann U, Lang T, Vobach M, Wosniok W (2005) Ethoxyresorufin-O-deethylase (EROD) activity in Dab (Limanda limanda) as biomarker for marine monitoring. Environ Sci Pollut Res 12:140–145

    Article  CAS  Google Scholar 

  • Kelly BC, Ikonomou MG, Blair JD (2009) Perfluoroalkyl contaminants in an arctic marine food web: trophic magnification and wildlife exposure. Environ Sci Technol 43:4037–4043

    Article  CAS  Google Scholar 

  • Liu C, Chang VWC, Gin KYH (2013) Environmental toxicity of PFCs: an enhanced integrated biomarker assessment and structure–activity analysis. Environ Toxicol Chem 32:2226–2233

    Article  CAS  Google Scholar 

  • Lohnes KL (2006) Impact of reconstructed wetlands on the tree swallow (Tachycineta bicolor). Master of Science, University of Maryland, College Park, MD

  • Lopez-Antia A, Dauwe T, Meyer J, Maes K, Bervoets L, Eens M (2017) High levels of PFOS in eggs of three bird species in the neighbourhood of a fluoro-chemical plant. Ecotoxicol Environ Saf 139:165–171

    Article  CAS  Google Scholar 

  • McNabb FMA, Jang DA, Larsen CT (2004) Does thyroid function in developing birds adapt to sustained ammonium perchlorate exposure? Toxicol Sci 82:106–113

    Article  CAS  Google Scholar 

  • Moody CA, Hebert GM, Strauss SH, Field JA (2003) Occurrence and persistence of perfluorooctanesulfonate and other perfluorinated surfactants in groundwater at a fire-training area at Wurtsmith Air Force Base, Michigan, USA. J Environ Monit 5:341–345

    Article  CAS  Google Scholar 

  • Newsted JJ, Jones PD, Coady K, Giesy JP (2005) Avian toxicity reference values for perfluorooctane sulfonate. Environ Sci Technol 39:9357–9362

    Article  CAS  Google Scholar 

  • Place BJ, Field JA (2012) Identification of novel fluorochemicals in aqueous film-forming foams used by the US military. Environ Sci Technol 46:7120–7127. https://doi.org/10.1021/es301465n

    Article  CAS  Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rainio MJ, Kanerva M, Wahlberg N, Nikinmaa M, Eeva T (2012) Variation of basal EROD activities in ten passerine bird species: relationships with diet and migration status. PLoS ONE 7:e33926

    Article  CAS  Google Scholar 

  • Rüdel H, Müller J, Jürling H, Koschorreck J (2011) Survey of patterns, levels, and trends of perfluorinated compounds in aquatic organisms and bird eggs from representative German ecosystems. Environ Sci Pollut Res 18:1457–1470

    Article  Google Scholar 

  • Sanchez W, Piccini B, Ditche JM, Porcher JM (2008) Assessment of seasonal variability of biomarkers in three-spined stickleback (Gasterosteus aculeatus L.) from a low contaminated stream: Implication for environmental biomonitoring. Environ Int 34:791–798

    Article  Google Scholar 

  • Sleiderink HM, Beyer J, Everaarts JM, Boon JP (1995) Influence of temperature on cytochrome P450 1A in dab (Limanda limanda) from the Southern North Sea: results from field surveys and a laboratory study. Mar Environ Res 39:67–71

    Article  CAS  Google Scholar 

  • Stapleton MK, Robertson RJ (2006) Female tree swallow home-range movements during their fertile period as revealed by radio-tracking. Wilson J Ornithol 118:502–507

    Article  Google Scholar 

  • Verreault J, Houde M, Gabrielsen GW et al (2005) Perfluorinated alkyl substances in plasma, liver, brain, and eggs of glaucous gulls (Larus hyperboreus) from the Norwegian arctic. Environ Sci Technol 39:7439–7445

    Article  CAS  Google Scholar 

  • Ward S, Bryant DM (2006) Barn swallows Hirundo rustica form eggs mainly from current food intake. J Avian Biol 37:179–189

    Article  Google Scholar 

  • Weiss JM, Andersson PL, Lamoree MH et al (2009) Competitive binding of Poly- and perfluorinated compounds to the thyroid hormone transport protein transthyretin. Toxicol Sci 109:206–216

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Greg E. Berner, Dana Shugart, Paul Thompson, Matthew Lark, M. Lovelace, C. Brooks, and B. Fetting for weekly nest checks, the U.S. Forest Service, Huron-Manistee National Forest, MI for access to the site, and Mike Boogaard, and 2 anonymous reviewers for comments on earlier versions of this manuscript. Funding was provided by U.S. Geological Survey and Great Lakes Restoration Initiative.

Author information

Authors and Affiliations

  1. U.S. Geological Survey, Upper Midwest Environmental Sciences Center, 2630 Fanta Reed Rd., La Crosse, WI, 54603, USA

    Christine M. Custer, Thomas W. Custer & Paul M. Dummer

  2. Michigan Department of Environmental Quality, P.O. Box 30473, Lansing, MI, 48909-7973, USA

    Robert Delaney

  3. U.S. Geological Survey, Patuxent Wildlife Research Center, 10300 Baltimore Avenue, Beltsville, MD, 20705, USA

    Sandra Schultz & Natalie Karouna-Renier

Authors
  1. Christine M. Custer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thomas W. Custer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robert Delaney
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paul M. Dummer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sandra Schultz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Natalie Karouna-Renier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christine M. Custer.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PPTX 64 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Custer, C.M., Custer, T.W., Delaney, R. et al. Perfluoroalkyl Contaminant Exposure and Effects in Tree Swallows Nesting at Clarks Marsh, Oscoda, Michigan, USA. Arch Environ Contam Toxicol 77, 1–13 (2019). https://doi.org/10.1007/s00244-019-00620-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-019-00620-1

Search

Navigation