, Volume 26, Issue 10, pp 1392–1407 | Cite as

EROD activity, chromosomal damage, and oxidative stress in response to contaminants exposure in tree swallow (Tachycineta bicolor) nestlings from Great Lakes Areas of Concern

  • Thomas W. CusterEmail author
  • Christine M. Custer
  • Paul M. Dummer
  • Emilie Bigorgne
  • Elias M. Oziolor
  • Natalie Karouna-Renier
  • Sandra Schultz
  • Richard A. Erickson
  • Kevin Aagaard
  • Cole W. Matson


Tree swallow, Tachycineta bicolor, nestlings were collected from 60 sites in the Great Lakes, which included multiple sites within 27 Areas of Concern (AOCs) and six sites not listed as AOCs from 2010 to 2014. Nestlings, approximately 12 days-of-age, were evaluated for ethoxyresorufin-O-dealkylase (EROD) activity, chromosomal damage, and six measures of oxidative stress. Data on each of these biomarkers were divided into four equal numbered groups from the highest to lowest values and the groups were compared to contaminant concentrations using multivariate analysis. Contaminant concentrations, from the same nestlings, included polychlorinated biphenyls (PCBs), polybrominated diphenyl ethers (PBDEs), perfluorinated compounds (PFCs), and 17 elements. Alkylated polycyclic aromatic hydrocarbons (aPAHs) and parent PAHs (pPAHs) were measured in pooled nestling dietary samples. Polychlorinated dibenzo-p-dioxins, polychlorinated dibenzofurans, and pesticides were measured in sibling eggs. Concentrations of aPAHs, pPAHs, chlordane, dieldrin, heptachlor, and PCBs, in that order, were the major contributors to the significant differences between the lowest and highest EROD activities; PFCs, PBDEs, the remaining pesticides, and all elements were of secondary importance. The four categories of chromosomal damage did not separate out well based on the contaminants measured. Concentrations of aPAHs, pPAHs, heptachlor, PCBs, chlordane, and dieldrin were the major contributors to the significant differences between the lowest and highest activities of two oxidative stress measures, total sulfhydryl (TSH) activity and protein bound sulfhydryl (PBSH) activity. The four categories of thiobarbituric acid reacting substances (TBARS), oxidized glutathione (GSSG), reduced glutathione (GSH), and the ratio of GSSG/GSH did not separate well based on the contaminants measured.


Tree swallows Biomarker Chromosomal damage EROD activity Oxidative stress 



This work was funded by the Great Lakes Restoration Initiative (GLRI), USGS, and by the University of Michigan Water Center, a center of the Graham Sustainability Institute. The Water Center is supported by funds from the Fred A. and Barbara M. Erb Family Foundation and the University of Michigan. We thank Christopher Balk, Greg Berner, Crystal Bole, Peggy Boone, Rod Booth Jr., Amanda Bosak, J. Christian Franson, Diane Goldberg, Andrew Haertel, Aaron Heimann, Yvette Hernandez, Melanie Iverson, Matthew Larkin, Adam Lorenz, Sean O’Mara, Ron Mayer, Patrick McKann, Karen McMullen, Melissa Meier, Kristina Artner Mott, Kelsey Prestby, Darin Ripp, Paul Ripple, Clif Schneider, Laura Solem, Dan Tagerson, Joshua Teslaa, Jocelyn Tschaikovsky, Max Weber, and Tesha Zimmerman for field assistance. This work could not have been done without the access granted by more than 75 landowners; their accommodations for our activities were greatly appreciated. We also thank Jack Waide, John Elliott, and Shane de Solla for helpful comments on earlier drafts of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

This article does not contain studies with human participants. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. All animal collections were conducted under appropriate federal (Federal Fish and Wildlife Permit MB123047-0), state, and local permits. All animal procedures were reviewed and approved by the US Geological Survey’s Upper Midwest Environmental Sciences Center Institutional Animal Care and Use Committee.

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Copyright information

© Springer Science+Business Media,LLC (outside the USA)  2017

Authors and Affiliations

  • Thomas W. Custer
    • 1
    Email author
  • Christine M. Custer
    • 1
  • Paul M. Dummer
    • 1
  • Emilie Bigorgne
    • 2
  • Elias M. Oziolor
    • 2
  • Natalie Karouna-Renier
    • 3
  • Sandra Schultz
    • 3
  • Richard A. Erickson
    • 1
  • Kevin Aagaard
    • 1
  • Cole W. Matson
    • 2
  1. 1.U.S. Geological Survey, Upper Midwest Environmental Sciences CenterLa CrosseUSA
  2. 2.Department of Environmental Science and the Center for Reservoir and Aquatic Systems Research (CRASR)Baylor UniversityWacoUSA
  3. 3.U.S. Geological Survey, Patuxent Wildlife Research CenterBeltsvilleUSA

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