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Ecotoxicology

, Volume 24, Issue 2, pp 453–467 | Cite as

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

  • Allyson K. JacksonEmail author
  • David C. Evers
  • Evan M. Adams
  • Daniel A. Cristol
  • Collin Eagles-Smith
  • Samuel T. Edmonds
  • Carrie E. Gray
  • Bart Hoskins
  • Oksana P. Lane
  • Amy Sauer
  • Timothy Tear
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.

Keywords

Bioaccumulation Mercury Passeriformes Sentinel Songbird 

Notes

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.

Supplementary material

10646_2014_1394_MOESM1_ESM.docx (44 kb)
Supplementary material 1 (DOCX 44 kb)
10646_2014_1394_MOESM2_ESM.xlsx (150 kb)
Supplementary material 2 (xlsx 151 kb)

References

  1. 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 CrossRefGoogle Scholar
  2. Basu N, Scheuhammer AM, Bursian SJ, Elliot J, Rouvinen-Watt K, Chan HM (2007) Mink as a sentinel species in environmental health. Environ Res 103:130–144CrossRefGoogle Scholar
  3. 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
  4. Beeby A (2001) What do sentinels stand for? Environ Pollut 112:285–298CrossRefGoogle Scholar
  5. Bossart GD (2006) Marine mammals as sentinel species for oceans and human health. Oceanography 19:134–137CrossRefGoogle Scholar
  6. 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 CrossRefGoogle Scholar
  7. 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 124:129–142CrossRefGoogle Scholar
  8. 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 41:4458–4464CrossRefGoogle Scholar
  9. Burger J, Gochfeld M (2004) Marine birds as sentinels of environmental pollution. EcoHealth 1:263–274CrossRefGoogle Scholar
  10. 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
  11. Commission for Environmental Cooperation Working Group (1997) Ecological regions of North America—toward a common perspective. Commission for Environmental Cooperation, Montreal 71pGoogle Scholar
  12. 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 CrossRefGoogle Scholar
  13. 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.SGoogle Scholar
  14. 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 Google Scholar
  15. 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 CrossRefGoogle Scholar
  16. 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 32:1178–1186CrossRefGoogle Scholar
  17. 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
  18. 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 157:1993–2002CrossRefGoogle Scholar
  19. 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 112:789–799CrossRefGoogle Scholar
  20. 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 CrossRefGoogle Scholar
  21. Evers DC (2006) Loons as biosentinels of aquatic integrity. Environ Bioindic 1:18–21Google Scholar
  22. 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 14:193–221CrossRefGoogle Scholar
  23. 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 57:29–43CrossRefGoogle Scholar
  24. 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
  25. 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
  26. 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, MaineGoogle Scholar
  27. 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 18:514–521CrossRefGoogle Scholar
  28. 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 CrossRefGoogle Scholar
  29. Gray LJ (1993) Response of insectivorous birds to emerging aquatic insects in riparian habitats of a tallgrass prairie stream. Am Midl Nat 129:288–300CrossRefGoogle Scholar
  30. 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 12:25–44CrossRefGoogle Scholar
  31. Hallinger KK, Zabransky DJ, Kazmer KA, Cristol DA (2010) Birdsong differs between mercury-polluted and reference sites. Auk 127:156–161CrossRefGoogle Scholar
  32. 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 128:759–769CrossRefGoogle Scholar
  33. 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 CrossRefGoogle Scholar
  34. 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 CrossRefGoogle Scholar
  35. 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
  36. 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 20:1984–1991CrossRefGoogle Scholar
  37. 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
  38. 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 CrossRefGoogle Scholar
  39. McKay JL, Maher CR (2012) Relationship between blood mercury levels and components of male song in Nelson’s sparrows (Ammodramus nelsoni). Ecotoxicology 21:2391–2397CrossRefGoogle Scholar
  40. Nakano S, Murakami M (2001) Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. Proc Natl Acad Sci 98:166–170CrossRefGoogle Scholar
  41. National Research Council (1991) Animals as sentinels of environmental health hazards. Committee on Animals as Monitors of Environmental Hazards, National Academy Press, WashingtonGoogle Scholar
  42. 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 159:2840–2844CrossRefGoogle Scholar
  43. 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
  44. 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
  45. 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
  46. 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 CrossRefGoogle Scholar
  47. Scheuhammer AM, Meyer MW, Sandheinrich MB, Murray MW (2007) Effects of environmental methylmercury on the health of wild birds, mammals, and fish. Ambio 36:12–18CrossRefGoogle Scholar
  48. 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 223–238CrossRefGoogle Scholar
  49. Scoville SA, Lane OP (2013) Cerebellar abnormalities typical of methylmercury poisoning in a fledged saltmarsh sparrow, Ammodramus caudacutus. Bull Environ Contam Toxicol 90:616–620CrossRefGoogle Scholar
  50. 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 119–142CrossRefGoogle Scholar
  51. 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 3:329–335CrossRefGoogle Scholar
  52. 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 33:208–215CrossRefGoogle Scholar
  53. United States Environmental Protection Agency (USEPA) (2011). “Mercury and Air Toxics Standards (MATS) for Power Plants.”Google Scholar
  54. 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 107:309–315CrossRefGoogle Scholar
  55. 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:e95674CrossRefGoogle Scholar
  56. 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 43:6031–6038CrossRefGoogle Scholar
  57. Walters DM, Fritz KM, Otter RR (2008) The dark side of subsidies: adult stream insects export organic contaminants to riparian predators. Ecol Appl 18:1835–1841CrossRefGoogle Scholar
  58. 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 CrossRefGoogle Scholar
  59. 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 CrossRefGoogle Scholar
  60. Wiener JG (2013) Mercury exposed: advances in environmental analysis and ecotoxicology of a highly toxic metal. Environ Toxicol Chem 32:2175–2178CrossRefGoogle Scholar
  61. 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 CrossRefGoogle Scholar
  62. 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 392–423Google Scholar
  63. 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 23:45–55CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Allyson K. Jackson
    • 1
    • 2
    Email author
  • David C. Evers
    • 1
  • Evan M. Adams
    • 1
  • Daniel A. Cristol
    • 3
  • Collin Eagles-Smith
    • 4
  • Samuel T. Edmonds
    • 1
    • 5
  • Carrie E. Gray
    • 1
  • Bart Hoskins
    • 6
  • Oksana P. Lane
    • 1
  • Amy Sauer
    • 1
    • 7
  • Timothy Tear
    • 8
  1. 1.Biodiversity Research InstitutePortlandUSA
  2. 2.Department of Fisheries and WildlifeOregon State UniversityCorvallisUSA
  3. 3.Department of BiologyCollege of William and MaryWilliamsburgUSA
  4. 4.U.S. Geological Survey, Forest and Rangeland Ecosystem Science CenterCorvallisUSA
  5. 5.TRC Companies, IncAugustaUSA
  6. 6.U.S. Environmental Protection Agency, New England Regional LaboratoryChelmsfordUSA
  7. 7.Department of BiologySyracuse UniversitySyracuseUSA
  8. 8.Grumeti FundArushaTanzania

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