Advertisement

Patterns of blood mercury variation in two long-distance migratory thrushes on Mount Mansfield, Vermont

  • Christopher C. RimmerEmail author
  • John D. Lloyd
  • Kent P. McFarland
  • David C. Evers
  • Oksana P. Lane
Article

Abstract

We investigated mercury (Hg) blood concentrations in Bicknell’s thrush (Catharus bicknelli) and Swainson’s thrush (C. ustulatus), congeneric long-distance migratory songbirds, from 2000−2017 at a montane forest site in north-central Vermont. We analyzed variation in blood Hg of both species using mixed-effects models, incorporating atmospheric wet Hg deposition data from a nearby sampling location. Although Hg deposition varied among years and seasonally, we detected no temporal trend in either atmospheric deposition or blood Hg, nor evidence of a relationship between the two. Sampling date had the strongest effect on blood Hg concentration, which declined seasonally, followed by age and sex of the individual. The data did not support an effect of species. We believe that the absence of a clear relationship between local atmospheric deposition and thrush blood Hg concentrations suggests that Hg cycling dynamics, mechanisms of transfer, and timing of uptake by montane forest biota are complex and poorly understood. The blood Hg concentrations of ~0.07–0.1 μg/g we documented in Bicknell’s and Swainson’s thrush are below those found to negatively impact physiological or reproductive endpoints in other invertivorous terrestrial passerines. To better evaluate the validity of Bicknell’s thrush as a bioindicator of MeHg availability in montane forest ecosystems, we recommend (1) effects-based investigations, (2) a more robust understanding of Hg and MeHg cycling, (3) more clear geospatial and temporal links between Hg deposition and biotic uptake, and (4) more thorough documentation of Hg burdens across the species’ annual cycle.

Keywords

Mercury bioaccumulation Nearctic-Neotropical migratory songbirds Catharus bicknelli Montane forests 

Notes

Acknowledgements

We thank our many outstanding field assistants who helped collect these data over the years, often under difficult conditions. The Stowe Mountain Resort provided invaluable logistical support for our field work. We are grateful for funding support received from the Charles E. & Edna T. Brundage Charitable Science and Wildlife Conservation Foundation, the Oakland Foundation, the Thomas Marshall Foundation, the USDA Forest Service Northeast Research Station, the U.S. Fish and Wildlife Service, the Vermont Monitoring Cooperative, and friends of the Vermont Center for Ecostudies. We also thank Kevin Regan of Biodiversity Research Institute for conducting lab analyses. Jim Duncan, Mike Finnegan and Miriam Pendleton provided helpful guidance in making available and interpreting atmospheric Hg deposition data from the Forest Ecosystem Monitoring Cooperative. Eric Miller and Jamie Shanley also provided helpful advice. We are grateful to Charles Driscoll, James Shanley, and two anonymous reviewers for constructive comments on earlier drafts of this manuscript.

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. All procedures performed in the handling and blood sampling of thrushes in this study were in accordance with the ethical standards of the Vermont Center for Ecostudies, the U.S. Fish and Wildlife Service, and the University of Vermont.

References

  1. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48.  https://doi.org/10.18637/jss.v067.i01 CrossRefGoogle Scholar
  2. Blackwell BD, Driscoll CT (2015) Deposition of mercury in forests along a montane elevation gradient. Environ Sci Technol 49:5363–5370CrossRefGoogle Scholar
  3. Bouland AJ, White AE, Lonabaugh KP, Varian-Ramos CW, Cristol DA (2012) Female-biased offspring sex ratios in birds at a mercury-contaminated river. J Avian Biol 43:244–251CrossRefGoogle Scholar
  4. Burnham KP, Anderson DR (2003) Model selection and multimodel inference: A practical information-theoretic approach. Springer Science & Business Media, New York and BerlinGoogle Scholar
  5. Collier B, Wallace GE (1989) Aging Catharus thrushes by rectrix shape. J Field Ornithol 60:230–240Google Scholar
  6. Cristol DA, Brasso RL, Condon AM, Fovargue RE, Friedman SL, Hallinger KK, Monroe AP, White AE (2008) The movement of aquatic mercury through terrestrial food webs. Science 320:335CrossRefGoogle Scholar
  7. Driscoll CT, Han Y-J, Chen CY, Evers DC, Lambert KF, Holsen TM, Kamman NC, Munson R (2007) Mercury contamination in forest and freshwater ecosystems in the northeastern United States. Bioscience 57:17–28CrossRefGoogle Scholar
  8. Driscoll CT, Mason RP, Chan HM, Jacob DJ, Pirrone N (2013) Mercury as a global pollutant: sources, pathways, and effects. Environ Sci Technol 47:4967–4983CrossRefGoogle Scholar
  9. Evers DC (2017) The effects of methylmercury on wildlife: a comprehensive review and approach for interpretation. Encyclopedia of the Anthropocene. Elsevier, Oxford, pp 181–194Google Scholar
  10. Gerson JR, Driscoll CT, Demers JD, Sauer AK, Blackwell BD, Montesdeoca MR, Shanley JB, Ross DS (2017) Deposition of mercury in forests across a montane elevation gradient: elevational and seasonal patterns in methylmercury inputs and production. J Geophys Res 122:1922–1939.  https://doi.org/10.1002/2016JG003721 CrossRefGoogle Scholar
  11. Hallinger KK, Zabransky DJ, Kazmer KA, Cristol DA (2010) Birdsong differs between mercury-polluted and reference sites. Auk 127:156–161CrossRefGoogle Scholar
  12. Hobson KA, McFarland KP, Wassenaar LI, Rimmer CC, Goetz JE (2001) Linking breeding and wintering grounds of Bicknell’s Thrushes using stable isotope analyses of feathers. Auk 118:16–23CrossRefGoogle Scholar
  13. Jackson AK, Evers DC, Etterson MA, Condon AM, Folsom SB, Detweiler J, Schmerfeld J, Cristol DA (2011) Mercury exposure affects the reproductive success of a free-living terrestrial songbird, the Carolina Wren (Thryothorus ludovicianus). Auk 128:759–769CrossRefGoogle Scholar
  14. Jackson AK, Evers DC, Adams EM, Cristol DA, Eagles-Smith C, Edmonds ST, Gray CE, Hoskins B, Lane OP, Sauer A, Tear T (2014) Songbirds as sentinels of mercury in terrestrial habitats of eastern North America. Ecotoxicology 24:453–467CrossRefGoogle Scholar
  15. Lane OP, Adams EM, Pau N, O’Brien KM, Regan K, Farina M, Moran TS, Zarudsky J (2018) Long-term mercury monitoring in adult saltmarsh sparrows breeding in Maine, Massachusetts and New York, USA, 2000–2017. EcotoxicologyGoogle Scholar
  16. Lawson ST (2003) Cloud water and throughfall deposition of mercury and trace elements in a high-elevation spruce-fir forest at Mt. Mansfield, Vermont. J Environ Monit 5:578–583CrossRefGoogle Scholar
  17. Lloyd JD, McFarland KP (2017) A Conservation Action Plan for Bicknell’s Thrush (Catharus bicknelli). International Bicknell’s Thrush Conservation Group (IBTCG).  https://doi.org/10.6084/m9.figshare.4962608.v1
  18. Ma Y, Branreun BA, Hobson KA, Guglielmo CG (2018) Evidence of negative seasonal carry-over effects of breeding ground mercury exposure on survival of migratory songbirds. J Avian Biol e01656.  https://doi.org/10.1111/jav.01656
  19. McCullagh EA, Phillips JB, Cristol DA (2015) Plumage color and reproductive output of eastern bluebirds (Sialia sialis) nesting near a mercury-contaminated river. J Environ Sci Health 50:1020–1028CrossRefGoogle Scholar
  20. Miller EK, VanArsdale A, Keeler JG, Chalmers A, Poissant L, Kamman NC, Brulotte R (2005) Estimation and mapping of wet and dry mercury deposition across northeastern Noirth America. Ecotoxicology 14:53–70CrossRefGoogle Scholar
  21. Muntean M, Janssens-Maenhout G, Song S, Selin NE, Olivier JGJ, Guizzardi D, Maas R, Dentener F (2014) Trend analysis from 1970 to 2008 and model evaluation of EDGARv4 global gridded anthropogenic mercury emissions. Sci Total Environ 494:337–350CrossRefGoogle Scholar
  22. Pyle P (1997) Identification to North American birds. Part I: Columbidae to Ploceidae. Slate Creek Press, Bolinas, CAGoogle Scholar
  23. R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  24. Rich TD, Beardmore CJ, Berlanga H, Blancher PJ, Bradstreet MSW, Butcher GS, Demarest DW, Dunn EH, Hunter WC, Iñigo-Elias EF, Kennedy JA, Martell AM, Panjabi AO, Pashley DN, Rosenberg KV, Rustay CM, Wendt JS, Will TC (2005) Partners in Flight Landbird Conservation Plan. Cornell Lab of Ornithology, Ithaca, NYGoogle Scholar
  25. Rimmer CC, McFarland KP, Evers DC, Miller EK, Aubry Y, Busby D, Taylor RJ (2005) Mercury concentrations in Bicknell’s Thrush and other insectivorous passerines in montane forests of northeastern North America. Ecotoxicology 14:223–240CrossRefGoogle Scholar
  26. Rimmer CC, Miller EK, McFarland KP, Taylor RJ, Faccio SD (2009) Mercury bioaccumulation and trophic transfer in the terrestrial food web of a montane forest. Ecotoxicology 19:697–709CrossRefGoogle Scholar
  27. Risch MR, DeWild JF, Gay DA, Zhang L, Boyer EW, Krabbencroft DP (2017) Atmospheric mercury deposition to forests in the eastern USA. Environ Pollut 228:8–18CrossRefGoogle Scholar
  28. Scheuhammer AM, Meyer MW, Sandheinrich MB, Murray MW (2007) Effects of environmental methylmercury on the health of wild birds, mammals, and fish. Ambio 36:12–19CrossRefGoogle Scholar
  29. Stenhouse IJ, Adams EM, Goyette JL, Regan KJ, Goodale MW, Evers DC (2018) Changes in mercury exposure of marine birds breeding in the Gulf of Maine, 2008–2013. Mar Pollut Bull 128:156–161CrossRefGoogle Scholar
  30. Townsend JM, Rimmer CC, Driscoll CT, McFarland KP, Iñigo-Elias EE (2013) Mercury concentrations in tropical resident and migrant songbirds on Hispaniola. Ecotoxicology 22:86–93CrossRefGoogle Scholar
  31. Townsend JM, Driscoll CT, Rimmer CC, McFarland KP (2014) Avian, salamander and forest floor mercury concentrations increase with elevation in a forested terrestrial ecosystem. Environ Toxicol Chem 33:208–215CrossRefGoogle Scholar
  32. Townsend JM, McFarland KP, Rimmer CC, Ellison WG, Goetz JE (2015) Bicknell’s Thrush (Catharus bicknelli). In: Poole A (Ed.) The Birds of North America. Cornell Lab of Ornithology, Ithaca.Google Scholar
  33. Weiss-Penzias PS, Gay DA, Brigham ME, Parsons MT, Gustin MS, ter Schure A (2016) Trends in mercury wet deposition and mercury air concentrations across the U.S. and Canada. Sci Total Environ 568:546–556CrossRefGoogle Scholar
  34. Wenny DG, Devault TL, Johnson MD, Kelly D, Sekercioglu CH, Tomback DF, Whelan CJ (2011) The need to quantify ecosystem services provided by birds. Auk 128:1–14CrossRefGoogle Scholar
  35. Whelan CJ, Wenny DJ, Marquis RJ (2008) Ecosystem services provided by birds. Ann New Y Acad Sci 1134:25–50CrossRefGoogle Scholar
  36. Whitney MC, Cristol DA (2017a) Impacts of sublethal mercury exposure on birds: a detailed review. Rev Environ Contam Toxicol 244:113–163Google Scholar
  37. Whitney MC, Cristol DA (2017b) Rapid depuration of mercury in songbirds accelerated by feather molt. Environ Toxicol Chem 36:3120–3126CrossRefGoogle Scholar
  38. Wood SN (2017) Generalized additive models: An introduction with r. CRC pressGoogle Scholar
  39. Yates DE, Adams EM, Angelo SE, Evers DC, Schmerfeld J, Moore MS, Kunz TH, Divoll T, Edmonds ST, Perkins C, Taylor R (2014) Mercury in bats from the northeastern United States. Ecotoxicology 23:45–55CrossRefGoogle Scholar
  40. Zhang YX, Jacob DJ, Horowitz HM, Chen L, Amos HM, Krabbenhoft DP, Slemr F, St Louis VL, Sunderland EM (2016) Observed decrease in atmospheric mercury explained by global decline in anthropogenic emissions. Proc Natl Acad Sci USA. 113:526–531.  https://doi.org/10.1073/pnas.1516312113.
  41. Zhou H, Zhou C, Lynam MM, Dvonch JT, Barres JA, Hopke PK, Cohen M, Holsen TM (2017) Atmospheric mercury temporal trends in the northeastern United States from 1992 to 2014: are measured concentrations responding to decreasing regional emissions? Environ Sci Technol Lett 4:91–97CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Vermont Center for EcostudiesNorwichUSA
  2. 2.Biodiversity Research InstitutePortlandUSA
  3. 3.American Wind Wildlife InstituteWashingtonUSA

Personalised recommendations