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Songbirds as sentinels of mercury in terrestrial habitats of eastern North America

Ecotoxicology volume 24, pages 453–467 (2015)Cite this article

Abstract

Mercury (Hg) is a globally distributed environmental contaminant with a variety of deleterious effects in fish, wildlife, and humans. Breeding songbirds may be useful sentinels for Hg across diverse habitats because they can be effectively sampled, have well-defined and small territories, and can integrate pollutant exposure over time and space. We analyzed blood total Hg concentrations from 8,446 individuals of 102 species of songbirds, sampled on their breeding territories across 161 sites in eastern North America [geometric mean Hg concentration = 0.25 μg/g wet weight (ww), range <0.01–14.60 μg/g ww]. Our records span an important time period—the decade leading up to implementation of the USEPA Mercury and Air Toxics Standards, which will reduce Hg emissions from coal-fired power plants by over 90 %. Mixed-effects modeling indicated that habitat, foraging guild, and age were important predictors of blood Hg concentrations across species and sites. Blood Hg concentrations in adult invertebrate-eating songbirds were consistently higher in wetland habitats (freshwater or estuarine) than upland forests. Generally, adults exhibited higher blood Hg concentrations than juveniles within each habitat type. We used model results to examine species-specific differences in blood Hg concentrations during this time period, identifying potential Hg sentinels in each region and habitat type. Our results present the most comprehensive assessment of blood Hg concentrations in eastern songbirds to date, and thereby provide a valuable framework for designing and evaluating risk assessment schemes using sentinel songbird species in the time after implementation of the new atmospheric Hg standards.

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References

  • Alberts JM, Sullivan SMP, Kautza A (2013) Riparian swallows as integrators of landscape change in a multiuse river system: implications for aquatic-to-terrestrial transfers of contaminants. Sci Total Environ 463–464:42–50. doi:10.1016/j.scitotenv.2013.05.065

    Article  Google Scholar 

  • Basu N, Scheuhammer AM, Bursian SJ, Elliot J, Rouvinen-Watt K, Chan HM (2007) Mink as a sentinel species in environmental health. Environ Res 103:130–144

    Article  CAS  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2013) lme4: linear mixed-effects models using Eigen and S4. R package version 1.0-5. http://CRAN.R-project.org/package=lme4. Accessed 28 Nov 2014

  • Beeby A (2001) What do sentinels stand for? Environ Pollut 112:285–298

    Article  CAS  Google Scholar 

  • Bossart GD (2006) Marine mammals as sentinel species for oceans and human health. Oceanography 19:134–137

    Article  Google Scholar 

  • Brasso RL, Cristol DA (2008) Effects of mercury exposure on the reproductive success of tree swallows (Tachycineta bicolor). Ecotoxicology 17:133–141. doi:10.1007/s10646-007-0163-z

    Article  CAS  Google Scholar 

  • Brown CL, Luoma SN (1995) Use of the euryhaline bivalve Potamocorbula amurensis as a biosentinel species to assess trace metal contamination in San Francisco Bay. Mar Ecol Press Series 124:129–142

    Article  CAS  Google Scholar 

  • Bundy JG, Keun HC, Sidhu JK, Spurgeon DJ, Svendsen C, Kille P, Morgan AJ (2007) Metabolic profile biomarkers of metal contamination in a sentinel terrestrial species are applicable across multiple sites. Environ Sci Technol 41:4458–4464

    Article  CAS  Google Scholar 

  • Burger J, Gochfeld M (2004) Marine birds as sentinels of environmental pollution. EcoHealth 1:263–274

    Article  Google Scholar 

  • Carlson JR, Cristol D, Swaddle JP (2014) Dietary mercury exposure causes decreased escape takeoff flight performance and increased molt rate in European starlings (Sturnus vulgaris). Ecotoxicology. doi:10.1007/s10646-014-1288-5

    Google Scholar 

  • Commission for Environmental Cooperation Working Group (1997) Ecological regions of North America—toward a common perspective. Commission for Environmental Cooperation, Montreal 71p

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Cowardin LM, Cater V, Golet FC, LaRoe ET (1979) Classification of wetlands and deepwater habitats of the United States. Department of the Interior, Fish and Wildlife Service, Washington, U.S

    Google Scholar 

  • 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. 320:335. doi:10.1126/science.1154082

    CAS  Google Scholar 

  • Custer CM, Custer TW, Hill EF (2007) Mercury exposure and effects on cavity-nesting birds from the Carson River, Nevada. Arch Environ Contam Toxicol 52:129–136. doi:10.1007/s00244-006-0103-6

    Article  CAS  Google Scholar 

  • Drewett DVV, Willson JD, Cristol DA, Chin SY, Hopkins WA (2013) Inter- and intraspecific variation in mercury bioaccumulation by snakes inhabiting a contaminated river floodplain. Environ Toxicol Chem 32:1178–1186

    Article  CAS  Google Scholar 

  • Driscoll CT, Mason RP, Chan HM, Jacob DJ, Pirrone N (2013) Mercury as a global pollutant: sources, pathways, and effects. Environ Sci Technol 47:4967–4983

    Article  CAS  Google Scholar 

  • Eagles-Smith CA, Ackerman JT, De La Cruz SEW, Takekawa JY (2009) Mercury bioaccumulation and risk to three waterbird foraging guilds is influenced by foraging ecology and breeding stage. Environ Pollut 157:1993–2002

    Article  CAS  Google Scholar 

  • Edmonds ST, Evers DC, Cristol DA, Mettke-Hoffman C, Powell LL, McGann AJ, Armiger JW, Lane OP, Tessler DF, Newell P, Heyden K, O’Driscoll NJ (2010) Geographic and seasonal variation in mercury exposure of the declining rusty blackbird. Condor 112:789–799

    Article  Google Scholar 

  • Edmonds ST, O’Driscoll NJ, Hillier NK, Atwood JL, Evers DC (2012) Factors regulating the bioavailability of methylmercury to breeding rusty blackbirds in northeastern wetlands. Environ Pollut 171:148–154. doi:10.1016/j.envpol.2012.07.044

    Article  CAS  Google Scholar 

  • Evers DC (2006) Loons as biosentinels of aquatic integrity. Environ Bioindic 1:18–21

    Google Scholar 

  • Evers DC, Burgess NM, Champoux L, Hoskins B, Major A, Goodale WM, Taylor RJ, Poppenga R, Daigle T (2005) Patterns and interpretation of mercury exposure in freshwater avian communities in northeastern North America. Ecotoxicology 14:193–221

    Article  CAS  Google Scholar 

  • Evers DC, Han Y-J, Driscoll CT, Kamman NC, Goodale MW, Lambert KF, Holsen TM, Chen CY, Clair TA, Butler T (2007) Biological mercury hotspots in the Northeastern United States and Southeastern Canada. Bioscience 57:29–43

    Article  Google Scholar 

  • Evers DC, Jackson AK, Tear TH, Osborne CE (2012) Hidden risk: mercury in terrestrial ecosystems of the northeast. BRI Report #2012-07. http://www.briloon.org/uploads/BRI_Documents/Mercury_Center/Hidden%20Risk/HiddenRisk_lr.pdf. Accessed 28 Nov 2014

  • Fair JM, Paul E, Jones J, Clark AB, Davie C, Kaiser G (2010) Chapter 6: Minor manipulative procedures. In: Guidelines to the use of wild birds in research. Ornithological Council, Washington. www.nmnh.si.edu/BIRDNET/guide. Accessed 22 Oct 2014

  • Folsom SB, Evers DC (2008) Assessment of mercury contamination and effects in songbirds on the North Fork of the Holston River, Virginia 2007. BRI Report #2008-01 Submitted to the U.S. Fish and Wildlife Service, Gloucester, Virginia. Biodiversity Research Institute, Gorham, Maine

  • Franceschini MD, Lane OP, Evers DC, Reed JM, Hoskins B, Romero LM (2009) The corticosterone stress response and mercury contamination in free-living tree swallows, Tachycineta bicolor. Ecotoxicology 18:514–521

    Article  CAS  Google Scholar 

  • French JB, Bennett RS, Rossmann R (2010) Mercury in the blood and eggs of American kestrels fed methylmercury chloride. Environ Toxicol Chem 29:2206–2210. doi:10.1002/etc.284

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Grove RA, Henny CJ, Kaiser JL (2009) Osprey: worldwide sentinel species for assessing and monitoring environmental contamination in rivers, reservoirs, and estuaries. J Toxicol Environ Health Part B 12:25–44

    Article  Google Scholar 

  • Hallinger KK, Zabransky DJ, Kazmer KA, Cristol DA (2010) Birdsong differs between mercury-polluted and reference sites. Auk 127:156–161

    Article  Google Scholar 

  • Jackson AK, Evers DC, Etterson MA, Condon AM, Folsom SB, Detweiler J, Schmerfeld J, Cristol DA (2011a) Mercury exposure affects the reproductive success of a free-living terrestrial songbird, the Carolina wren (Thryothorus ludovianus). Auk 128:759–769

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Keller RH, Xie L, Buchwalter DB, Franzreb KE, Simons TR (2014) Mercury bioaccumulation in southern Appalachian birds, assessed through feather concentrations. Ecotoxicology 23(2):304–316. doi:10.1007/s10646-013-1174-6

    Article  CAS  Google Scholar 

  • Kuznetsova A, Brockhoff PB, Christensen RHB (2014) lmerTest: tests for random and fixed effects for linear mixed effect models (lmer objects of lme4 package). R package version 2.0-6. http://CRAN.R-project.org/package=lmerTest. Accessed 28 Nov 2014

  • Lane OP, O’Brien KM, Evers DC, Hodgman TP, Major A, Pau N, Ducey MJ, Taylor R, Perry D (2011) Mercury in breeding saltmarsh sparrows (Ammodramus caudacutus caudacutus). Ecotoxicology 20:1984–1991

    Article  CAS  Google Scholar 

  • Lenth R (2014) lsmeans: least-squares means. R package version 2.00-5. http://cran.r-project.org/web/packages/lsmeans/lsmeans.pdf. Accessed 28 Nov 2014

  • Lewis CA, Cristol DA, Swaddle JP, Varian-Ramos CW, Zwollo P (2013) Decreased immune response in zebra finches exposed to sublethal doses of mercury. Arch Environ Contam Toxicol 64:327–336. doi:10.1007/s00244-012-9830-z

    Article  CAS  Google Scholar 

  • McKay JL, Maher CR (2012) Relationship between blood mercury levels and components of male song in Nelson’s sparrows (Ammodramus nelsoni). Ecotoxicology 21:2391–2397

    Article  CAS  Google Scholar 

  • Nakano S, Murakami M (2001) Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. Proc Natl Acad Sci 98:166–170

    Article  CAS  Google Scholar 

  • National Research Council (1991) Animals as sentinels of environmental health hazards. Committee on Animals as Monitors of Environmental Hazards, National Academy Press, Washington

    Google Scholar 

  • Newman MC, Xu X, Condon A, Liang L (2011) Floodplain methylmercury biomagnification factor higher than that of the contiguous river (South River, Virginia USA). Environ Poll 159:2840–2844

    Article  CAS  Google Scholar 

  • Osborne CE, Evers DC, Duron M, Schoch N, Yates D, Buck D, Lane OP, Franklin J (2011) Mercury contamination within terrestrial ecosystems in New England and Mid-Atlantic states: profiles of soil, invertebrates, songbirds, and bats. BRI Report #2011-09. http://www.briloon.org/uploads/BRI_Documents/Mercury_Center/Hidden%20Risk/BRI_2011-09_Osborne.etal.2011.pdf. Accessed 28 Nov 2014

  • Poole A (eds) (2013) The birds of North America online: Cornell Laboratory of Ornithology, Ithaca. http://bna.birds.cornell.edu/BNA/. Accessed 3 Jan 2013

  • 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 14:223–240

    Article  CAS  Google Scholar 

  • 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. Ecotoxicology 19:697–709. doi:10.1007/s10646-009-0443-x

    Article  CAS  Google Scholar 

  • Scheuhammer AM, Meyer MW, Sandheinrich MB, Murray MW (2007) Effects of environmental methylmercury on the health of wild birds, mammals, and fish. Ambio 36:12–18

    Article  CAS  Google Scholar 

  • Scheuhammer AM, Basu N, Evers DC, Heinz GH, Sandheinrich MB, Bank MS (2012) Ecotoxicology of mercury in fish and wildlife: Recent Advances. In: Bank MS (ed) Mercury in the environment: pattern and process. Univ. California Press, Berkeley, pp 223–238

    Chapter  Google Scholar 

  • Scoville SA, Lane OP (2013) Cerebellar abnormalities typical of methylmercury poisoning in a fledged saltmarsh sparrow, Ammodramus caudacutus. Bull Environ Contam Toxicol 90:616–620

    Article  CAS  Google Scholar 

  • Shanley JB, Bishop K (2012) Mercury cycling in terrestrial watersheds. In: Bank MS (ed) Mercury in the environment: pattern and process. Univ. California Press, Berkeley, pp 119–142

    Chapter  Google Scholar 

  • Stahl RG (2008) Can mammalian and non-mammalian “sentinel species” data be used to evaluate the human health implications of environmental contaminants? Human Ecol Risk Assess 3:329–335

    Article  Google Scholar 

  • Townsend JM, Driscoll CT, Rimmer CC, McFarland KP (2014) Avian, salamander, and forest floor mercury concentrations increase with elevation in a terrestrial ecosystem. Environ Toxicol Chem 33:208–215

    Article  CAS  Google Scholar 

  • United States Environmental Protection Agency (USEPA) (2011). “Mercury and Air Toxics Standards (MATS) for Power Plants.”

  • Van der Schalie WH, Gardner HS, Bantle JA, De Ross CT, Finch RA, Reif JS, Reuter RH, Backer LC, Buger J, Folmar LC, Stokes WS (1999) Animals as sentinels of human health hazards of environmental chemicals. Environ Health Perspect 107:309–315

    Article  Google Scholar 

  • Varian-Ramos CW, Swaddle JP, Cristol DA (2013) Mercury reduces avian reproductive success and imposes selection: an experimental study with adult- or lifetime-exposure in zebra finch. PLoS ONE 9:e95674

    Article  Google Scholar 

  • Wada H, Cristol DA, McNabb FMA, Hopkins WA (2009) Suppressed adrenocortical responses and thyroid hormone levels in birds near a mercury-contaminated river. Environ Sci Technol 43:6031–6038

    Article  CAS  Google Scholar 

  • Walters DM, Fritz KM, Otter RR (2008) The dark side of subsidies: adult stream insects export organic contaminants to riparian predators. Ecol Appl 18:1835–1841

    Article  Google Scholar 

  • Walters DM, Mills MA, Fritz KM, Raikow DF (2010) Spider-mediated flux of PCBs from contaminated sediments to terrestrial ecosystems and potential risks to arachnivorous birds. Environ Sci Technol 44:2849–2856. doi:10.1021/es9023139

    Article  CAS  Google Scholar 

  • Warner SE, Shriver WG, Pepper MA, Taylor RJ (2010) Mercury concentrations in tidal marsh sparrows and their use as bioindicators in Delaware Bay, USA. Environ Monit Assess 171:671–679. doi:10.1007/s10661-010-1312-z

    Article  CAS  Google Scholar 

  • Wiener JG (2013) Mercury exposed: advances in environmental analysis and ecotoxicology of a highly toxic metal. Environ Toxicol Chem 32:2175–2178

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wren CD, Harris S, Harttrup N (1995) Ecotoxicology of mercury and cadmium. In: Hoffman DJ, Rattner BA, Burton GA, Cairns J (eds) Handbook of Ecotoxicology. Lewis Publishers, Boca Raton, pp 392–423

    Google Scholar 

  • Yates DE, Adams EM, Angelo SE, Evers DC, Schmerfeld J, Moore MS, Kunz TH, Divoll T, Edmonds ST, Perkins C, Taylor R, O’Driscoll NJ (2014) Mercury in bats from the northeastern United States. Ecotoxicology 23:45–55

    Article  CAS  Google Scholar 

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Acknowledgments

Funding and in kind support for this synthesis project came from a variety of sources including The Nature Conservancy (TNC) Rodney Johnson and Katherine Ordway Stewardship Endowment, New York State Energy Research and Development Authority (NYSERDA), U.S. Fish and Wildlife Service (USFWS), National Parks Service (NPS), and the Wildlife Conservation Society (WCS) and the U.S. Geological Survey. Special thanks to those people who helped secure funding, including Greg Lampman at NYSERDA, and Ken Karwowski, Ann Secord, Anne Condon and John Schmerfeld at USFWS. Many researchers contributed data or logistical support for this project, including: David Braun (Sound Science), Chris Rimmer and Kent McFarland (Vermont Center for Ecostudies), Greg Shriver (University of Delaware), Jeff Loukmas (New York State Department of Environmental Conservation), Chad Seewagen (WCS), Bill DeLuca, Bill Schuster (Black Rock Forest), Bob Mulvihill (Powdermill Avian Research Center), Mike Fowles (Army Corp of Engineers), Tom LeBlanc (Allegany State Park), Bruce Connery (Acadia National Park), Dr. Mark Ford (Fernow Experimental Forest), and Henry Caldwell (Dome Island). We are indebted to those that provided site access, including staff at Montezuma National Wildlife Refuge (NWR), Rachel Carson NWR, Wertheim NWR, Parker River NWR, Ninigret NWR, McKinney NWR, Great Meadows NWR, Maine Department of Inland Fisheries and Wildlife, Tonawanda Wildlife Management Area, Marine Nature Study Area and the town of Hempstead, NY, and everyone at the Cornell Lab of Ornithology. R.L. Brasso and A. Condon helped revise a previous draft of this manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Biodiversity Research Institute, 276 Canco Road, Portland, ME, 04103, USA

    Allyson K. Jackson, David C. Evers, Evan M. Adams, Samuel T. Edmonds, Carrie E. Gray, Oksana P. Lane & Amy Sauer

  2. Department of Fisheries and Wildlife, Oregon State University, 104 Nash Hall, Corvallis, OR, 97331-3803, USA

    Allyson K. Jackson

  3. Department of Biology, College of William and Mary, Williamsburg, VA, 23187, USA

    Daniel A. Cristol

  4. U.S. Geological Survey, Forest and Rangeland Ecosystem Science Center, 3200 SW Jefferson Way, Corvallis, OR, 97331, USA

    Collin Eagles-Smith

  5. TRC Companies, Inc, 14 Gabriel Drive, Augusta, ME, 04330, USA

    Samuel T. Edmonds

  6. U.S. Environmental Protection Agency, New England Regional Laboratory, 11 Technology Drive, Chelmsford, MA, 01863, USA

    Bart Hoskins

  7. Department of Biology, Syracuse University, Syracuse, NY, 13244, USA

    Amy Sauer

  8. Grumeti Fund, Mawalla Park, Olasiti Road, P.O. Box 0, Arusha, Tanzania

    Timothy Tear

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  1. Allyson K. Jackson
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  2. David C. Evers
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  3. Evan M. Adams
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  4. Daniel A. Cristol
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  5. Collin Eagles-Smith
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  6. Samuel T. Edmonds
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  7. Carrie E. Gray
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  8. Bart Hoskins
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  9. Oksana P. Lane
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  10. Amy Sauer
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  11. Timothy Tear
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Correspondence to Allyson K. Jackson.

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Any use of trade, product, or organization names is for descriptive purposes only and does not imply endorsement by the U.S. Government. The views expressed in this article are solely those of the authors, and do not necessarily reflect the views, policies or official positions of the U.S. EPA. This paper has been peer reviewed and approved for publication consistent with USGS Fundamental Science Practices (http://pubs.usgs.gov/circ/1367/).

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Jackson, A.K., Evers, D.C., Adams, E.M. et al. Songbirds as sentinels of mercury in terrestrial habitats of eastern North America. Ecotoxicology 24, 453–467 (2015). https://doi.org/10.1007/s10646-014-1394-4

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Keywords

  • Bioaccumulation
  • Mercury
  • Passeriformes
  • Sentinel
  • Songbird