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The effects of climate, habitat, and trophic position on methylmercury bioavailability for breeding New York songbirds

Abstract

Mercury (Hg) is a global pollutant that affects songbird populations across a variety of ecosystems following conversion to methylmercury (MeHg)—a form of Hg with high potential for bioaccumulation and bioavailability. The amount of bioavailable MeHg in an ecosystem is a function of the amount of total Hg present as well as Hg methylation rates, which vary across the landscape in space and time, and trophic transfer. Using songbirds as an indicator of MeHg bioavailability in terrestrial ecosystems, we evaluated the role of habitat, climate, and trophic level in dictating MeHg exposure risk across a variety of ecosystems. To achieve this objective, 2243 blood Hg samples were collected from 81 passerine and near-passerine species in New York State, USA, spanning 10 different sampling regions from Long Island to western New York. Using a general linear mixed modeling framework that accounted for regional variation in sampling species composition, we found that wetland habitat area within 100 m of capture location, 50-year average of summer maximum temperatures, and trophic position inferred using stable isotope analysis were all correlated with songbird blood Hg concentrations statewide. Moreover, these patterns had a large degree of spatial variability suggesting that the drivers of MeHg bioavailability differed significantly across the state. Mercury deposition, land cover, and climate are all expected to change throughout the northeastern United States in the coming decades. Terrestrial MeHg bioavailability will likely respond to these changes. Focused research and monitoring efforts will be critical to understand how exposure risk responds to global environmental change across the landscape.

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References

  1. Adams EM, Williams KA, Olsen BJ, Evers DC (2019) Mercury exposure across the annual cycle in migratory songbirds: implications for migratory behavior. Ecotoxicology (In press)

  2. Amos HM, Jacob DJ, Streets DG, Sunderland EM (2013) Legacy impacts of all-time anthropogenic emissions on the global mercury cycle. Glob Biogeochem Cycles 27(2):410–421

  3. Bates D, Maechler B, Bolker, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48

  4. Becker PH, Gonzalez-Solis J, Behrends B, Croxall J (2002) Feather mercury levels in seabirds at South Georgia: influence of trophic position, sex, and age. Mar Ecol Prog Ser 243:261–269

  5. Boening DW (2000) Ecological effects, transport, and fate of mercury: a general review. Chemosphere 40:1335–1351

  6. Brasso RL, Cristol DA (2008) Effects of mercury exposure on the reproductive success of Tree Swallows (Tachycineta bicolor). Ecotoxicology 17:133–141

  7. Brooks RT (2009) Potential impacts of global climate change on the hydrology and ecology of ephemeral freshwater systems of the forest of the northeastern United States. Clim Chang 95:469–483

  8. Cabana G, Tremblay A, Kalff J, Rasmussen JB (1994) Pelagic food chain structure in Ontario Lakes: a determinant of mercury levels in Lake Trout (Salvelinus namaycush). Can J Fish Aquat Sci 51:381–389

  9. Correll MD, Wiest WA, Hodgman TP, Shriver WG, Elphick CS, McGill BJ, O’Brien K, Olsen BJ (2017) Predictors of specialist avifaunal decline in coastal marshes. Conserv Biol 31:172–182

  10. Craft C, Clough J, Ehman J, Joye S, Park R, Pennings S, Guo H, Machmuller M (2009) Forecasting the effects of accelerated sea-level rise on tidal marsh ecosystem services. Front Ecol Environ 7(2):73–78

  11. Cristol DA, Brasso RL, Condon AM, Fovargue RE, Hallinger KK, Monroe AP, White AE (2008) The movement of aquatic mercury through terrestrial food webs. Science 320(5874):335

  12. Cizdziel JV, Hinners TA, Pollard JE, Heithmar EM, Cross CL (2002) Mercury concentrations in fish from Lake Mead, USA, related to fish size, condition, trophic level, location, and consumption risk. Arch Environ Contamination Toxicol 43:309–317

  13. Dahl TE (2011) Status and trends of wetland in the conterminous United States 2004–2009. U.S. Department of the Interior, Fish and Wildlife Service, Washington, D.C., p 108

  14. Davis JA, Looker RE, Yee D, Marvin-Di Pasquale M, Grenier JL, Austin CM, McKee LJ, Greenfield BK, Brodberg R, Blum JD (2012) Reducing methylmercury accumulation in the food webs of San Francisco Bay and its local watersheds. Environ Res 119:3–26

  15. Demers JD, Driscoll CT, Fahey TJ, Yavitt JB (2007) Mercury cycling in litter and soil in different forest types in the Adirondack region, New York, USA. Ecol Appl 17(5):1341–1351

  16. Driscoll CT, Han Y-J, Chen CY, Evers DC, Lambert KF, Holsen TM, Kamman NC, Munson RK (2007) Mercury contamination in forest and freshwater ecosystems in the Northeastern United States. BioScience 57:17–28

  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(10):4967–4983

  18. Driscoll CT, Buonocore JJ, Levy JI, Lambert KF, Burtraw D, Reid SB, Fakhraei H, Schwartz J (2015) US power plant carbon standards and clean air and health co-benefits. Nat Clim Change 6:535–540

  19. Eagles-Smith CA, Silbergeld EK, Basu N, Bustamante P, Diaz-Barriga F, Hopkins WA, Nyland JF (2018) Modulators of mercury risk to wildlife and humans in the context of rapid global change. Ambio 47(2):170–197

  20. Edmonds ST, Evers DC, Cristol DA, Mettke-Hofmann 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(4):789–799

  21. 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. https://doi.org/10.1016/j.envpol.2012.07.044

  22. Evers DC, Clair TA (2005) Mercury in northeastern North America: a synthesis of existing databases. Ecotoxicology 14:7–14

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

  24. Evers DC, Savoy L, DeSorbo C, Yates DE, Hanson W, Taylor KM, Siegel L, Cooley JH, Bank MS, Major A, Munney K, Mower B, Vogel HS, Schoch N, Pokras M, Goodale MW, Fair J (2008) Adverse effects from environmental mercury loads on breeding common loons. Ecotoxicology 17(2):69–81

  25. Furness RW (1993) Birds as monitors of pollutants. In: Furness RW, Greenwood JJD (eds) Birds as monitors of environmental change. Springer, Dordrect

  26. Gibb H, O’Leary KG (2014) Mercury exposure and the health impacts among individuals in the artisan and small-scale gold mining community: a comprehensive review. Environ Health Perspect 122(7):667

  27. Hawley DM, Hallinger KA, Cristol DA (2009) Compromised immune competence in free-living tree swallows exposed to mercury. Ecotoxicology 18(5):499–503

  28. Hayhoe K, Wake CP, Huntington TG, Luo L, Schwartz MD, Sheffield J, Wood E, Anderson B, Bradbury J, DeGaetano A, Troy TJ, Wolfe D (2007) Past and future changes in climate and hydrological indicators in the US Northeast. Clim Dyn 28(4):381–407

  29. Hayhoe K, Wake B, Anderson X-Z, Liang E, Maurer J, Zhu J, Bradbury A, DeGaetano A, Hertel, Wuebbles D (2008) Regional climate change projections for the northeast U.S. Mitig Adapt Strateg Glob Change 13(5-6):425–436

  30. Heinz GH, Hoffman DJ (2009) Mercury accumulation and loss in mallard eggs. Environ Toxicol Chem 23(1):222–224

  31. Hobson KA (1999) Stable-carbon and nitrogen isotope ratios of songbird feathers grown in two terrestrial biomes: implications for valuating trophic relationship and breeding origins. Condor 101:799–805

  32. Homer CG, Dewitz JA, Yang L, Jin S, Danielson P, Xian G, Coulston J, Herold ND, Wickham JD, Megown K (2015) Completion of the 2011 National Land Cover Database from the conterminous United States—representing a decade of land cover change information. Photogramm Eng Remote Sens 81(5):345–354

  33. 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(4):759–769

  34. Jackson A, Evers D, Adams E, Cristol D, Eagles-Smith C, Edmonds S, Gray C, Hoskins B, Lane O, Sauer A, Tear T (2015) Songbirds as sentinels of mercury in terrestrial habitats of eastern North America. Ecotoxicology 24:453–467

  35. Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool 78(1):1–27

  36. Kidd KA, Hesslein RH, Fudge RJP, Hallard KA (1995) The influence of trophic level as measured by δ15N on mercury concentrations in freshwater organisms. Water Air Soil Pollut 80:1011–1015

  37. Kirwan ML, Megonigal JP (2013) Tidal wetland stability in the face of human impacts and sea-level rise. Nature 504:53–60

  38. Kirwan ML, Guntenspergen GR, D’Alpaos A, Morris JT, Mudd SM, Temmerman S (2010) Limits on the adaptability of coastal marshes to rising sea level. Hydrol Land Surf Stud 37:L23401

  39. Kramar D, Goodale WM, Kennedy LM, Carstensen LW, Kaur T (2005) Relating land cover characteristics and common loon mercury levels using geographic information systems. Ecotoxicology 14(1-2):253–262

  40. 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

  41. Lane O, Adams EM, Pau N, O’Brien KM, Reagan K, Farina M, Schneider-Moran T, Zarudsky J. (2019). Long-term monitoring of mercury in adult saltmarsh sparrows breeding in Maine, Massachusetts and New York, USA 2000–2017. Ecotoxicology (In press)

  42. Lee C-S, Lutcavage ME, Chandler E, Madigan DJ, Cerrato RN, Fisher NS (2016) Declining mercury concentrations in Bluefin Tuna reflect reduced emissions to the North Atlantic Ocean. Environ Sci Technol 50(23):12825–12830

  43. Longcore JR, Haines TA, Halteman WA (2007) Mercury in tree swallow food, eggs, bodies, and feathers at Acadia National Park, Maine, and an EPA Superfund site, Ayer, Massachusetts. Environ Monit Assess 126(1-3):129–143

  44. Lyons JE, Runge MC, Laskowski HP, Kendall WL (2008) Monitoring in the context of structured decision-making and adaptive management. J Wildl Manag 72(8):1683–1692

  45. Mao H, Ye Z, Driscoll C (2017a) Meteorological effects on Hg wet deposition in a forested site in the Adirondack region of New York during 2000–2015. Atmos Environ 168:90–100

  46. Mao H, Hall D, Ye Z, Zhou Y, Felton D, Zhang L (2017b) Impacts of large-scale circulation on urban ambient concentrations of gaseous elemental mercury in New York, USA. Atmos Chem Phys 17(18):11655

  47. Marra PP, Hobson KA, Holmes RT (1998) Linking winter and summer events in a migratory bird by using stable-carbon isotopes. Science 282:1884–1886

  48. Meehl GA, Stocker TF, Collins WD, Friedlingstein P, Gaye T, Gregory JM, Kitoh A, Knutti R, Murphy JM, Noda A et al. (2007) Global climate projections. Cambridge University Press, Cambridge, UK

  49. Michener R, Lajtha K (2007) Stable isotopes in ecology and environmental science. Blackwell Publishing, Malden, Massachusetts, USA.

  50. Miskimmin BM, Rudd JWMN, Kelly CA (1992) Influence of dissolved organic carbon, pH, and microbial respiration rates on mercury methylation and demethylation in lake water. Can J Fish Aquat Sci 49(1):17–22

  51. Mitsch WJ, Hernandez ME (2013) Landscape and climate change threats to wetlands of North and Central America. Aquat Sci 75:133–149

  52. Podar M, Gilmour CC, Brandt CC, Soren A, Brown SD, Crable BR, Palumbo AV, Somenahally AC, Elias DA (2015) Global prevalence and distribution of genes and microorganisms involved in mercury methylation. Sci Adv 1(9):e1500675

  53. R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  54. Ramlal PS, Kelly CA, Rudd JWM, Furutani A (1993) Sites of methyl mercury production in remote Canadian Shield lake. Can J Fish Aquat Sci 50:972–979

  55. Reis AT, Rodrigues SM, Araújo C, Coelho JP, Pereira E, Duarte AC (2009) Mercury contamination in the vicinity of a chlor-alkali plant and potential risks to local population. Sci total Environ 407(8):2689–2700

  56. 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

  57. Risch MR, Kenski DM (2018) Spatial patterns and temporal changes in atmospheric-mercury deposition for the Midwestern USA, 2001–2016. Atmosphere 9(1):29

  58. Rodenhouse NL, Lowe WH, Gebauer RLE, McFarland KP, Bank MS (2019) Mercury bioaccumulation in temperature forest food webs associated with headwater streams. Sci Total Environ 665:1125–1134

  59. Sauer AK, Driscoll CT, Evers DC, Adams EM, Yang Y. (2019) Mercury exposure in songbird communities within Sphagnum Bog and upland forest ecosystems in the Adirondack Park (New York, USA). Ecotoxicology (In press)

  60. Scheuhammer AM, Meyer MW, Sandheinrich MB, Murray MW (2007) Effects of environmental mercury on the health of wild birds, mammals, and fish. AMBIO: J Hum Environ 36:12–19

  61. Schile LM, Callway JC, Morris JT, Stralberg D, Parker VT, Kelly M (2014) Modeling tidal marsh distribution with sea-level rise: evaluating the role of vegetation, sediment, and upland habitat in marsh resiliency. PLOS ONE 9(2):e88760

  62. Schindler DW (2001) The cumulative effects of climate warming and other human stresses on Canadian freshwaters in the new millennium. Can J Fish Aquat Sci 58:18–29

  63. Seewagen CL (2018) The threat of global mercury pollution to bird migration: potential mechanisms and current evidence. Ecotoxicology. https://doi.org/10.1007/s10646-018-1971-z

  64. Sellers P, Kelly CA, Rudd JWM, MacHutchon AR (1996) Photodegradation of methylmercury in lakes. Nature 380:694–697

  65. St. Louis VL, Rudd JWM, Kelly CA, Beaty KG, Bloom NS, Flett RJ (1994) Importance of wetlands as sources of methyl mercury to boreal forest ecosystems. Can J Fish Aquat Sci 51(5):1065–1076

  66. St. Louis VL, Rudd JWM, Kelly CA, Bodaly RA, Paterson MJ, Beaty KG, Hesslein RH, Heyes A, Majewski AR (2004) The rise and fall of mercury methylation in an experimental reservoir. Environ Sci Technol 38:1348–1358

  67. Stern GA, Macdonald RW, Outridge PM, Wilson S, Chetelat J, Cole A, Hintelmann H, Loseto LL, Steffen A, Wang F, Zdanowicz C (2012) How does climate change influence Arctic mercury? Sci Total Environ 414:22–42

  68. Taylor VF, Buckman KL, Seelen EA, Mazrui NM, Balcom PH, Mason RP, Chen CY (2019) Organic carbon content drives methylmercury levels in the water column and estuarine food webs across latitudes in the Northeast United States. Environ Pollut 246:639–649

  69. Telmer KH, Veiga MM (2009) World emissions of mercury from artisanal and small scale gold mining. In: Mercury Fate and Transport in the Global Atmosphere: Measurements, Models, and Policy Implications Interim Report. UNEP Global Mercury Partnership, Chapter 6, p 96–130. Springer, Boston, MA

  70. 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

  71. Tsui MTK, Adams EM, Jackson AK, Evers DC, Blum JD, Balogh SJ (2017) Understanding sources of methylmercury in songbirds with stable mercury isotopes: challenges and future directions. Environ Toxicol Chem 37(1):166–174

  72. Ullrich SM, Tanton TW, Abdrashitova SA (2001) Mercury in the aquatic environment: a review of factors affecting methylation. Crit Rev Environ Sci Technol 31(3):241–293

  73. 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). Ecotoxicology 14:37–52

  74. Wada H, Cristol DA, McNabb FMA, Hopkins WA (2009) U.S. Department of Agriculture. 2015. Summary Report: 2012 National Resources Inventory, Natural Resources Conservation Service, Washington DC, and Center for Survey Statistics and Methodology. Iowa State University, Ames, Iowa

  75. 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

  76. Warren RS, Niering WA (1993) Vegetation change on a northeast tidal marsh: interaction of sea-level rise and marsh accretion. Ecology 74(1):96–103

  77. Whitney MC, Cristol DA (2017) Impacts of sublethal mercury exposure on birds: a detailed review. In: Reviews of environmental contamination and toxicology, Springer, Cham, vol 244, p 113–163

  78. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer-Verlag New York. Suppressed adrenocortical responses and thyroid hormone levels in birds near a mercury-contaminated river. Environ Sci Technol 43:6031–6038

  79. Wickham H, Francois R, Henry L, Muller K (2018) dplyr: a grammar for data manipulation. R package version 0.7.5. https://CRAN.R-project.org/package=dplyr

  80. Williams JW, Jackson ST (2007) Novel climates, no-analog communities, and ecological surprises. Front Ecol Environ 5(9):475–482

  81. Wilman H, Belmaker J, Simpson J, de la Rosa C, Rivadeneira MM, Jetz-Elton W (2014) Traits 1.0: species-level foraging attributes of the world’s birds and mammals. Ecology 95:2027. https://doi.org/10.1890/13-1917.1

  82. Windham-Myers L, Fleck JA, Ackerman JT, Marvin-DiPasquale M, Stricker CA, Heim WA, Bachand PAM, Eagles-Smith CA, Gill G, Stephenson M, Alpers CN (2014) Mercury cycling in agriculture and managed wetlands: a synthesis of methylmercury production, hy6drological export, and bioaccumulation from an integrate field study. Sci Total Environ 484:221–231

  83. Ye Z, Mao H, Driscoll CT (2019) Primary effects of changes in meteorology vs. anthropogenic emissions on mercury wet deposition: a modeling study. Atmos Environ 198:215–225

  84. Yu X, Driscoll CT, Huang J, Holsen TM, Blackwell BD (2013) Modeling and mapping of atmospheric mercury deposition in Adirondack Park, New York. PloS ONE 8(3):e59322

  85. Zedler JB, Kercher S (2005) Wetland resources: status, trends, ecosystem services, and restorability. Annu Rev Environ Resour 30:39–74

  86. Zhang Y, Jacob DJ, Horowitz HM, Chen L, Amos HM, Krabbenhoft DP, Slemr F, St. Louis VL, Sunderland EN (2016) Observed decrease in atmospheric mercury explained by global decline in anthropogenic emissions. PNAS 113(3):526–531

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Acknowledgements

Sample collection occurred under all required state (NYS DEC Scientific License to Collect and Possess Permits #1873, 1893; NYS Temporary Revocable Permits #2386, 2262, 8957, 2057/8128, 1979/7493) and federal permits (USGS BBL Permit #22636). Kathryn Williams provided comments on the manuscript and assistance in field sampling. The work of many trained songbird biologists was needed for this large sampling effort; the work of Melissa Duron and Sarah Johnson is specifically acknowledged. We would also like to thank the many field technicians that provided assistance during the course of the project: Katherine Gilbert, Kylie O’Driscoll, Mike Brennan, Paul Josephson, Tom Daniel, Lyneé Sauer, and Bob Sauer. We would like to acknowledge the many individuals and organizations for their generous support and collaboration as part of our research efforts: Adirondack League Club, Elizabeth Ballantine, Dan Josephson, Neil Gifford and the Albany Pine Bush Preserve, Black Rock Forest Consortium, Cornell University, Boston University, Harvard University, Massawepie Scout Camps, NYS Department of Environmental Conservation, New York State Parks, Frost Valley YMCA, SUNY-ESF Huntington Wildlife Forest, Syracuse University, Michael Farina, Rob Longiaru, Tara Schneider-Moran, John Zarudsk and many others with The Town of Hempstead Department of Conservation and Waterways, Mashomack Preserve, The Nature Conservancy (Adirondack Chapter, Central and Western NY Chapter, Eastern NY Chapter, Joe Jansen, Nicole Maher, Derek Rogers and many others from the Long Island Chapter), Alison Kocek and the field crew from SUNY ESF for collecting samples in the New York City region, and the US Geological Survey. This work could not have been done without extensive publicly available online resources. We acknowledge the World Climate Research Programme's Working Group on Coupled Modeling, which is responsible for CMIP, and we thank the climate modeling groups for producing and making available their model output. For CMIP the U.S. Department of Energy's Program for Climate Model Diagnosis and Intercomparison provides coordinating support and led development of software infrastructure in partnership with the Global Organization for Earth System Science Portals.

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Correspondence to Evan M. Adams.

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This study was funded by the New York State Energy Research and Development Authority (NYSERDA, Award # 34358). All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

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Appendix. Estimates of methylmercury exposure across all species and all regions

Appendix. Estimates of methylmercury exposure across all species and all regions

Eighty-three species were sampled across all regions, including 214 unique species/region combinations. Here we include a figure that summarizes the average blood Hg concentrations (ppm ww) of all species/region combinations as estimated in the analysis. These averages (and 95% confidence intervals) are based on the generalized linear mixed modeling approach described in the text to identify species with elevated blood Hg concentrations in each region. Here we document the results for all species (Table 2).

Table 2 Model-estimated mean blood Hg concentrations for all species in each region using a general linear mixed modeling framework

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Adams, E.M., Sauer, A.K., Lane, O. et al. The effects of climate, habitat, and trophic position on methylmercury bioavailability for breeding New York songbirds. Ecotoxicology (2019). https://doi.org/10.1007/s10646-019-02151-w

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Keywords

  • Mercury
  • Methylmercury
  • Songbirds
  • Stable isotopes
  • Climate
  • Wetlands