Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Explaining variation in Colorado songbird blood mercury using migratory behavior, foraging guild, and diet

Abstract

Methylmercury is a contaminant of growing global concern that has been shown to accumulate in a variety of taxa, including songbirds. Birds in the same area can accumulate mercury to strikingly different levels. While diet and trophic level clearly play an important role in mercury bioaccumulation and biomagnification, other factors including foraging guilds and migratory behavior may influence mercury levels as well. Here we examine interspecific variation in blood mercury levels in songbirds living in the Fountain Creek watershed on the Front Range of Colorado. We found that the species with the highest mercury had blood mercury concentrations over 75 times higher than the species with the lowest levels. Carnivores had the highest blood mercury levels, but ground foraging and long distance migration also were correlated with higher mercury concentrations. This information may shed light on what species are most at risk from mercury pollution and help to target conservation resources at contaminated sites.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

References

  1. Ackerman JT, Eagles-Smith CA, Herzog MP (2011) Bird mercury concentrations change rapidly as chicks age: toxicological risk is highest at hatching and fledging. Environ Sci Technol 45:5418–5425. https://doi.org/10.1021/es200647g

  2. Ackerman JT, Eagles-Smith CA, Herzog MP, Hartman CA, Peterson SH, Evers DC, Jackson AK, Elliot JE, Vander Pol SS, Bryan CE (2016) Avian mercury exposure and toxicological risk across western North America: a synthesis. Sci Total Environ 568:749–769. https://doi.org/10.1016/j.scitotenv.2016.03.071

  3. Ackerman JT, Eagles‐Smith CA, Takekawa JY, Bluso JD, Adelsbach TL (2008) Mercury concentrations in blood and feathers of prebreeding Forster’s terns in relation to space use of San Francisco Bay, California, USA, habitats. Environ Toxicol Chem 27(4):897–908

  4. Beach R (2006) U.S. Geological Survey. Mineral Resources on-line SpatialData: Gold Hill Mesa Tailings. http://mrdata.usgs.gov/mrds/show-mrds.php?dep_id=10311068. Accessed 21 Nov 2016

  5. Borrell A (1993) PCB and DDT in blubber of cetaceans from the northeastern north Atlantic. Mar Pollut Bull 26:146–151. https://doi.org/10.1016/0025-326X(93)90125-4(93)90125-4

  6. Condon AM, Cristol DA (2009) Feather growth influences blood mercury level of young songbirds. Environ Toxicol Chem 28:395–401. https://doi.org/10.1897/08-094.1

  7. 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 320:335–335. https://doi.org/10.1126/science.1154082

  8. DeGraaf RM, Tilghman NG, Anderson SH (1985) Foraging guilds of North American birds. Environ Manag 9:493–536. https://doi.org/10.1007/BF01867324

  9. Gilbertson M, Kubiak T, Ludwig J, Fox G (1991) Great lakes embryo mortality, edema, and deformities syndrome (GLEMEDS) in colonial fish‐eating birds: similarity to chick‐edema disease. J Toxicol Environ Health Part A 33:455–520. https://doi.org/10.1080/15287399109531538

  10. Gray LJ (1993) Response of insectivorous birds to emerging aquatic insects in riparian habitats of a tallgrass prairie stream. Am Midl Nat 129:288–300. https://doi.org/10.2307/2426510

  11. Hallinger KK, Cristol DA (2011) The role of weather in mediating the effects of mercury exposure on reproductive success in tree swallows. Ecotoxicology 20:1369–1377. https://doi.org/10.1007/s10646-011-0694-1

  12. Hecnar SJ (1995) Acute and chronic toxicity of ammonium nitrate fertilizer to amphibians from southern Ontario. Environ Toxicol Chem 14:2131–2137. https://doi.org/10.1002/etc.5620141217

  13. Hipfner JM, Hobson KA, Elliott JE (2011) Ecological factors differentially affect mercury levels in two species of sympatric marine birds of the North Pacific. Sci Total Environ 409:1328–1335. https://doi.org/10.1016/j.scitotenv.2010.12.022

  14. Hissler C, Probst JL (2006) Impact of mercury atmospheric deposition on soils and streams in a mountainous catchment (Vosges, France) polluted by chlor-alkali industrial activity: the important trapping role of the organic matter. Sci Total Environ 361:163–178. https://doi.org/10.1016/j.scitotenv.2005.05.023

  15. Hitchcock DJ, Andersen T, Varpe Ø, Borjå K (2019) Effects of maternal reproductive investment on sex-specific pollutant accumulation in seabirds: a meta-analysis. Environ Sci Technol 53:7821–7829. https://doi.org/10.1021/acs.est.9b01296

  16. Jackson AK (2017) You are what, when, where, and how you eat: mercury in avian food webs across multiple spatial scales, PhD Thesis. Oregon State University, Corvallis, OR

  17. 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. Ecotoxicol 2:1–15. https://doi.org/10.1007/s10646-014-1394-4

  18. Jackson AK, Evers DC, Folsom SB, Condon AM, Diener J, Goodrick LF, McGann AJ, Schmerfeld J, Cristol DA (2011) Mercury exposure in terrestrial birds far downstream of an historical point source. Environ Pollut 159:3302–3308. https://doi.org/10.1016/j.envpol.2011.08.046

  19. Kahle S, Becker PH (1999) Bird blood as bioindicator for mercury in the environment. Chemosphere 39:2451–2457. https://doi.org/10.1016/S0045-6535(99)00154-X

  20. Keller RH, Xie L, Buchwalter DB, Franzreb KE, Simons TR (2014) Mercury bioaccumulation in Southern Appalachian birds, assessed through feather concentrations. Ecotoxicol 23:304–316. https://doi.org/10.1007/s10646-013-1174-6

  21. Kleinow KM, Melancon MJ, Lech JJ (1987) Biotransformation and induction: implications for toxicity, bioaccumulation and monitoring of environmental xenobiotics in fish. Environ Health Perspect 71:105–119

  22. Ma WC (1989) Effect of soil pollution with metallic lead pellets on lead bioaccumulation and organ/body weight alterations in small mammals. Arch Environ Contam Toxicol 18:617–622. https://doi.org/10.1007/BF01055030

  23. Mac MJ, Edsall CC (1991) Environmental contaminants and the reproductive success of lake trout in the Great Lakes: an epidemiological approach. J Toxicol Environ Health 33:375–394. https://doi.org/10.1080/15287399109531536

  24. Majidi Y, Bahramifar N, Ghasempouri SM (2015) Pattern of mercury accumulation in different tissues of migratory and resident birds: western reef heron (Egretta gularis) and Siberian gull (Larus heuglini) in Hara International Wetland—Persian Gulf. Environ Monit Assess 187:4082. https://doi.org/10.1007/s10661-014-4082-1

  25. Miller EK, Vanarsdale A, Keeler GJ, Chalmers A, Poissant L, Kamman NC, Brulotte R (2005) Estimation and mapping of wet and dry mercury deposition across northeastern North America. Ecotoxicol 14:53–70. https://doi.org/10.1007/s10646-004-6259-9

  26. Nimmo DR, Herrmann SJ, Carsella JS, McGarvy CM, Foutz HP, Herrmann-Hoesing LM, Gregorich JM, Turner JA, Heuvel BV (2016) Mercury and selenium in fish of Fountain Creek, Colorado (USA): possible sources and implications. SpringerPlus 5:437. https://doi.org/10.1186/s40064-016-2088-6

  27. 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. Ecotoxicol 14:223–240. https://doi.org/10.1007/s10646-004-6270-1

  28. Rimmer CC, Miller EK, McFarland KP, Taylor RJ, Faccio SD (2010) Mercury bioaccumulation and trophic transfer in the terrestrial food web of a montane forest. Ecotoxicol 19:697–709. https://doi.org/10.1007/s10646-009-0443-x

  29. Seewagen CL, Cristol DA, Gerson AR (2016) Mobilization of mercury from lean tissues during simulated migratory fasting in a model songbird. Sci Rep. 6:25762. https://doi.org/10.1038/srep25762

  30. Townsend JM, Rimmer CC, Driscoll CT, McFarland KP, Inigo-Elias E (2013) Mercury concentrations in tropical resident and migrant songbirds on Hispaniola. Ecotoxicol 22:86–93. https://doi.org/10.1007/s10646-012-1005-1

  31. Tsipoura N, Burger J, Feltes R, Yacabucci J, Mizrahi D, Jeitner C, Gochfeld M (2008) Metal concentrations in three species of passerine birds breeding in the Hackensack Meadowlands of New Jersey. Environ Res 107:218–228. https://doi.org/10.1016/j.envres.2007.11.003

  32. U.S. Environmental Protection Agency (1994) Analytical results report site inspection, Gold Hill Tailings site EPA ID# COD983801275. Doc. #448808 1994-10-14 00:00:00.0. Morrison Knudsen Corp., Englewood

  33. VanArsdale A, Weiss J, Keeler G, Miller E, Boulet G, Brulotte R, Poissant L (2005) Patterns of mercury deposition and concentration in northeastern North America (1996–2002). Ecotoxicol 14:37–52. https://doi.org/10.1007/s10646-004-6258-x

  34. Varanasi U, Casillas E, Arkoosh MR, Hom T, Misitano DA, Brown DW, Chan SL, Collier TK, McCain BB, Stein JE (1993) Contaminant exposure and associated biological effects in juvenile Chinook salmon (Oncorhynchus tshawytscha) from urban and nonurban estuaries of Puget Sound. NOAA Technical Memorandum NMFS NWFSC-8

  35. Varian-Ramos CW, Condon AM, Hallinger KK, Carlson-Drexler KA, Cristol DA (2011) Stability of mercury concentrations in frozen avian blood samples. Bull Environ Contam Toxicol 86:159–162. https://doi.org/10.1007/s00128-010-0164-0

  36. Volta P, Tremolada P, Neri MC, Giussani G, Galassi S (2009) Age-dependent bioaccumulation of organochlorine compounds in fish and their selective biotransformation in top predators from Lake Maggiore (Italy). Water Air Soil Pollut 197:193–209. https://doi.org/10.1007/s11270-008-9803-z

  37. Wada H, Cristol DA, McNabb FA, Hopkins WA (2009) Suppressed adrenocortical responses and thyroid hormone levels in birds near a mercury-contaminated river. Environ Sci Technol 43:6031–6038. https://doi.org/10.1021/es803707f

  38. Warner SE, Shriver WG, Olsen BJ, Greenberg RG, Taylor RJ (2012) Mercury in wing and tail feathers of hatch-year and adult tidal marsh sparrows. Arch Environ Contam Toxicol 63:586–593. https://doi.org/10.1007/s00244-012-9783-2

  39. Winder VL, Emslie SD (2011) Mercury in breeding and wintering Nelson’s sparrows (Ammodramus nelsoni). Ecotoxicol 20:218–225. https://doi.org/10.1007/s10646-010-0573-1

Download references

Acknowledgements

Funding for this study was provided by a SEED grant from Colorado State University–Pueblo and support from the Biology Department and Colorado State University–Pueblo. We would like to thank the numerous undergraduate research assistants who helped with data collection including Audrey Curtis, Hilary Eisenbraun, Ashley Glasser, Bradley Gonzales, Ashley Minsnich, Austin Reed, Elizabeth Smith, and Alyssa Torres.

Author information

Correspondence to Claire W. Varian-Ramos.

Ethics declarations

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 studies involving animals were in accordance with the ethical standards of Colorado State University–Pueblo and were approved by the University’s Animal Care and Use Committee (Assurance Number: A3425-01).

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

Knutsen, C.J., Varian-Ramos, C.W. Explaining variation in Colorado songbird blood mercury using migratory behavior, foraging guild, and diet. Ecotoxicology (2019). https://doi.org/10.1007/s10646-019-02141-y

Download citation

Keywords

  • Bioaccumulation
  • Blood mercury
  • Interspecific variation
  • Methylmercury
  • Passeriformes