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Spatial variation in aquatic invertebrate and riparian songbird mercury exposure across a river-reservoir system with a legacy of mercury contamination

  • Allyson K. JacksonEmail author
  • Collin A. Eagles-Smith
  • Colleen Emery
Article

Abstract

Mercury (Hg) loading and methylation in aquatic systems causes a variety of deleterious effects for fish and wildlife populations. Relatively little research has focused on Hg movement into riparian food webs and how this is modulated by habitat characteristics. This study characterized differences in Hg exposure in aquatic invertebrates and riparian songbirds across a large portion of the Willamette River system in western Oregon, starting at a Hg-contaminated Superfund site in the headwaters (Black Butte Hg Mine) and including a reservoir known to methylate Hg (Cottage Grove Reservoir), all downstream reaches (Coast Fork and Willamette River) and off-channel wetland complexes (Willamette Valley National Wildlife Refuge Complex). After accounting for year, date, and site differences in a mixed effects model, MeHg concentrations in aquatic invertebrates varied spatially among habitat categories and invertebrate orders. Similarly, THg in songbird blood varied by among habitat categories and bird species. The highest Hg concentrations occurred near the Hg mine, but Hg did not decline linearly with distance from the source of contamination. Birds were consistently elevated in Hg in habitats commonly associated with enhanced MeHg production, such as backwater or wetlands. We found a positive but weak correlation between aquatic invertebrate MeHg concentrations and songbird THg concentrations on a site-specific basis. Our findings suggest that Hg risk to riparian songbirds can extend beyond point-source contaminated areas, highlighting the importance of assessing exposure in surrounding habitats where methylmercury production may be elevated, such as reservoirs and wetlands.

Keywords

Methylmercury Willamette Black Butte Songbird Aquatic invertebrate 

Notes

Acknowledgements

Funding for this work was provided by the U.S. Geological Survey Contaminant Biology Program. A.K.J. was funded by an Oregon State University Provost Distinguished Graduate Fellowship, Savery Outstanding Doctoral Student Award, David B. and Georgia Leupold Marshall Wildlife Graduate Scholarship, Mastin Wildlife Travel Scholarship, P.F. & Nellie Buck Yerex Graduate Fellowship, Coombs-Simpson Memorial Fellowship, and Munson Wildlife Graduate Scholarship. A.K.J. would like to thank her coadvisor Dr. W. Douglas Robinson and her entire dissertation committee: Dr. Anita Morzillo, Dr. David Evers, Dr. Daniel Cristol and Dr. Sarah Henkel. We would like to thank a variety of organizations for access to the field sites: USEPA, Army Corp of Engineers, Cottage Grove, USFWS, Oregon Parks Department, Benton County, City of Corvallis, City of Albany, City of Salem. Field support was provided by an amazing undergraduate field crew including (2013) Jim Randolph, Mason Wagner, Jessica Greer, Danielle Aquilar, Amanda Wasserman, (2014) Michael Brawner, Noelle Moan, Melanie Holte, Danielle Ramsden. This manuscript was made better by the help of two anonymous reviewers. Laboratory support was provided by James Willacker and John Pierce. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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 samples were collected under authority of appropriate scientific collection permits, including both State (invertebrates: Oregon DFW# 17648; birds: Oregon DFW# 062-13) and Federal (USFWS MBTA# MB28361A; USGS Banding # 20786) agencies. All birds were handled under approved animal care and use protocols (Oregon State University ACUP # 4408).

Supplementary material

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Supplementary Information

References

  1. Ambers RKR, Hygelund BN (2001) Contamination of two Oregon reservoirs by cinnabar mining and mercury amalgamation. Environ Geol 40(6):699–707CrossRefGoogle Scholar
  2. Bates DM, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects model using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  3. Brasso RL, Cristol DA (2008) Effects of mercury exposure on the reproductive success of tree swallows (Tachycineta bicolor). Ecotoxicology 17:133–141CrossRefGoogle Scholar
  4. Chasar LC, Scudder BC, Stewart AR, Bell AH, Aiken GR (2009) Mercury cycling in stream ecosystem: 3. Trophic dynamics and methylmercury bioaccumulation. Environ Sci Tech 43:2733–2739CrossRefGoogle Scholar
  5. Chumchal MM, Drenner RW (2015) An environmental problem hidden in plain sight? Small human-made ponds, emergent insects, and mercury contamination of biota in the Great Plains. Environ Toxicol Chem 34(6):1197–1205CrossRefGoogle Scholar
  6. Cristol DA, Brasso RL, Condon AM et al. (2008) The movement of aquatic mercury through terrestrial food webs. Science 320:335–335CrossRefGoogle Scholar
  7. Curtis LR, Morgans DL, Thoms B, Villenueve D (2013) Extreme precipitation appears a key driver of mercury transport from the watershed to Cottage Grove Reservoir, Oregon. Environ Poll 176:178–184CrossRefGoogle Scholar
  8. Dudgeon D, Arthington AH, Gessner MO, Kawabata S-I, Knowler DJ et al. (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev 81:163–182CrossRefGoogle Scholar
  9. Eagles-Smith CA, Wiener JG, Eckley CS et al. (2016) Mercury in western North America: a synthesis of environmental contamination, fluxes, bioaccumulation, and risk to fish and wildlife. Sci Total Environ 568:1213–1226CrossRefGoogle Scholar
  10. Eagles-Smith CA, Silbergeld EK, Basu N et al. (2018) Modulators of mercury risk to wildlife and humans in the context of rapid global change. Ambio 47:170–197CrossRefGoogle Scholar
  11. Eckley CS, Luxton TP, McKernan JL, Goetz J, Goulet J (2015) Influence of reservoir water level fluctuations on sediment methylmercury concentrations downstream of the historical Black Butte mercury mine, OR. Appl Geochem 61:284–293CrossRefGoogle Scholar
  12. Gratton CG, Vander Zanden MJ (2009) Flux of aquatic insect productivity to land: comparison of lentic and lotic systems. Ecology 90(10):2689–2699CrossRefGoogle Scholar
  13. Gregory SD, Hulse D, Payne S, Branscomb A, Ashkenas L (2002) Priorities for restoration. In: Hulse D, Gregory S and Baker J (eds) Willamette river basin planning atlas: trajectories of environmental and ecological change. Oregon State University Press, Corvallis, ORGoogle Scholar
  14. Hawley DM, Hallinger KK, Cristol DA (2009) Compromised immune competence in free-living tree swallows exposed to mercury. Ecotoxicology 18:499–503CrossRefGoogle Scholar
  15. Heinz GH, Hoffman DJ, Klimstra JD, Stebbins KR, Kondrad SR, Erwin SA (2009) Species differences in the sensitivity of avian embryos to methylmercury. Arch Environ Contam Toxicol 56:129–138CrossRefGoogle Scholar
  16. Henny CJ, Kaiser JL, Packard HA, Grove RA, Taft MR (2005) Assessing mercury exposure and effects to American Dippers in headwater streams near mining sites. Ecotoxicology 14:709–725CrossRefGoogle Scholar
  17. Henny CJ, Kaiser JL, Grove RA (2009) PCDDs, PCDFs, PCBs, OC pesticides and mercury in fish and osprey eggs from Willamette River, Oregon (1993, 2001, and 2006) with calculated biomagnification factors. Ecotoxicology 18:151–173CrossRefGoogle Scholar
  18. Hope BK (2005) A mass budget for mercury in the Willamette River Basin, Oregon USA. Water, Air Soil Pollut 161:365–382CrossRefGoogle Scholar
  19. Hsu-Kim H, Eckley CS, Acha D, Feng X, Gilmour CC, Jonsson S, Mitchell CPJ (2018) Challenges and opportunities for managing aquatic mercury pollution in altered landscapes. Ambio 47:141–169CrossRefGoogle Scholar
  20. Iwata T, Nakano S, Murakami M (2003) Stream meanders increase insectivorous bird abundance in riparian deciduous forests. Ecography 26(3):325–337CrossRefGoogle Scholar
  21. Jackson AK, Evers DC, Etterson MA et al. (2011a) Mercury exposure affects the reproductive success of a free-living terrestrial songbird, the Carolina Wren (Thryothorus ludovicianus). Auk 128:759–769CrossRefGoogle Scholar
  22. Jackson AK, Evers DC, Folsom SB et al. (2011b) Mercury exposure in terrestrial birds far downstream of an historical point source. Environmental Pollut 159:3302–3308CrossRefGoogle Scholar
  23. Jackson AK (2017) You are what, when, where and how you eat: mercury in avian food webs across multiple spatial scales. Dissertation, Oregon State University, Corvallis, ORGoogle Scholar
  24. Kennedy ED, White DW (2013) Bewick’s Wren (Thryomanes bewickii). In: Rodewald PGEd. The Birds of North America. Cornell Lab of Ornithology, Ithaca, NYGoogle Scholar
  25. Kuznetsova A, Brockhoff PB, Cristensen RHB (2016) lmerTest: tests in linear mixed effects models. https://cran.r-project.org/web/packages/lmerTest/lmerTest.pdf
  26. 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 64:327–336CrossRefGoogle Scholar
  27. Nakano S, Murakami M (2001) Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. Proc Natl Acad Sci USA 98(1):166–170CrossRefGoogle Scholar
  28. Nilsson C, Berggren K (2000) Alterations of riparian ecosystems caused by river regulation. BioScience 50:783–792CrossRefGoogle Scholar
  29. Ormerod SJ, Dobson M, Hildrew AG, Townsend CR (2010) Multiple stressors in freshwater ecosystems. Freshwater Biol 55:1–4CrossRefGoogle Scholar
  30. Ortega C, Hill GE (2010) Black-headed Grosbeak (Pheuticus melanocephalus). In: Rodewald PG Ed. The Birds of North America. Cornell Lab of Ornithology, Ithaca, NYGoogle Scholar
  31. Payne S, Baker J (2002) “Study Area.” In Willamette River basin atlas: trajectories of environmental and ecological change. Oregon State University Press, Corvallis, ORGoogle Scholar
  32. Ravichandran M (2004) Interactions between mercury and dissolved organic matter––a review. Chemosphere 55:319–331CrossRefGoogle Scholar
  33. 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
  34. Schoch N, Glennon MJ, Evers DC, Duron M, Jackson AK, Driscoll CT, Ozard JW, Sauer AK (2014) The impacts of mercury exposure on the CommonLoon (Gavia immer) population in the Adirondack Park, New York, USA. Waterbirds 37(sp1):133–146CrossRefGoogle Scholar
  35. Seewagen CL, Cristol DA, Gerson AR (2016) Mobilization of mercury from lean tissues during simulated migratory fasting in a model songbird. Sci Rep 6:25762CrossRefGoogle Scholar
  36. 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
  37. Tweedy BN, Drenner RW, Chumchal MM, Kennedy JH (2013) Effects of fish on emergent insect-mediated flux of methylmercury across a gradient of contamination. Environ Sci Technol 43:1614–1619Google Scholar
  38. Ullrich SM, Tanton TW, Abdrashitova SA (2001) Mercury in the aquatic environment: a review of factors affecting methylation. Critical Rev Environ Sci Technol 31:241–293CrossRefGoogle Scholar
  39. U.S. Environmental Protection Agency, (2001). Methyl mercury in water by distillation, aqueous ethylation, purge and trap, and cold-vapor atomic fluorescence spectrometry. Office of Water and Office of Science and Technology, Washington, DC. Method 1630. EPA-821-R-01-020Google Scholar
  40. U.S. Fish and Wildlife Service (2011) Willamette Valley National Wildlife Refuges: Final comprehensive conservation plan and environmental assessment, Corvallis, OR. https://www.fws.gov/pacific/planning/main/docs/OR/Willamette%20Valley/WillValleyFinalCCPforWeb.pdf
  41. Varian-Ramos CW, Swaddle JP, Cristol DA (2013) Familial differences in the effects of mercury on reproduction in Zebra Finches. Environ Pollut 182:316–323CrossRefGoogle Scholar
  42. Vitousek PM (1997) Human domination of earth’s ecosystems. Science 277:494–499CrossRefGoogle Scholar
  43. 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
  44. 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
  45. 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 44:2849–2856CrossRefGoogle Scholar
  46. Willacker JJ, Eagles-Smith CA, Lutz MA, Tate MT, Lepak JM, Ackerman JT (2016) Reservoirs and water management influence fish mercury concentrations in the western United States and Canada. Sci Total Environ 568:739–748CrossRefGoogle Scholar

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

Authors and Affiliations

  1. 1.Department of Environmental StudiesPurchase College SUNYPurchaseUSA
  2. 2.Department of Fisheries and WildlifeOregon State UniversityCorvallisUSA
  3. 3.U.S. Geological SurveyForest and Rangeland Ecosystem Science CenterCorvallisUSA

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