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Factors affecting MeHg bioaccumulation in stream biota: the role of dissolved organic carbon and diet

  • Hannah J. BroadleyEmail author
  • Kathryn L. Cottingham
  • Nicholas A. Baer
  • Kathleen C. Weathers
  • Holly A. Ewing
  • Ramsa Chaves-Ulloa
  • Jessica Chickering
  • Adam M. Wilson
  • Jenisha Shrestha
  • Celia Y. Chen
Article

Abstract

The bioaccumulation of the neurotoxin methylmercury (MeHg) in freshwater ecosystems is thought to be mediated by both water chemistry (e.g., dissolved organic carbon [DOC] and dissolved mercury [Hg]) and diet (e.g., trophic position and diet composition). Hg in small streams is of particular interest given their role as a link between terrestrial and aquatic processes. Terrestrial processes determine the quantity and quality of streamwater DOC, which in turn influence the quantity and bioavailability of dissolved MeHg. To better understand the effects of water chemistry and diet on Hg bioaccumulation in stream biota, we measured DOC and dissolved Hg in stream water and mercury concentration in three benthic invertebrate taxa and three fish species across up to 12 tributary streams in a forested watershed in New Hampshire, USA. As expected, dissolved total mercury (THg) and MeHg concentrations increased linearly with DOC. However, mercury concentrations in fish and invertebrates varied non-linearly, with maximum bioaccumulation at intermediate DOC concentrations, which suggests that MeHg bioavailability may be reduced at high levels of DOC. Further, MeHg and THg concentrations in invertebrates and fish, respectively, increased with δ15N (suggesting trophic position) but were not associated with δ13C. These results show that even though MeHg in water is strongly determined by DOC concentrations, mercury bioaccumulation in stream food webs is the result of both MeHg availability in stream water and trophic position.

Keywords

Methylmercury Accumulation Food web Watershed Biogeochemical factors Stable isotopes 

Notes

Acknowledgements

We are grateful to Vivien Taylor, Arthur Baker, and Brian Jackson for analysis of MeHg samples, David Fischer of the Cary Institute for DOC analysis, and Amanda Lindsey and Bethel Steele for technical assistance. We thank the Lake Sunapee Protective Association (LSPA) for logistical support. This research was made possible by an Institutional Development Award (IDeA) from the National Institute of General Medical Sciences of the National institutes of Health, grant number P20GM103506 to Dr. Ronald Taylor, and the Dartmouth Superfund Research Program funded by NIH Grant Number P42 ES007373 from the National Institute of Environmental Health Sciences to Dr. Celia Chen. This manuscript was finalized while KLC was serving at the National Science Foundation.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10646_2019_2086_MOESM1_ESM.docx (1.1 mb)
Supplementary Information

References

  1. Babiarz CL, Benoit JM, Shafer MM, Andren AW, Hurley JP, Webb DA (1998a) Seasonal influences on partitioning and transport of total and methylmercury in rivers from contrasting watersheds. Biogeochemistry 41:237–257CrossRefGoogle Scholar
  2. Babiarz CL, Hurley JP, Benoit JM, Shafer MM, Andren AW, Webb DA (1998b) Seasonal influences on partitioning and transport of total and methylmercury in rivers from contrasting watersheds. Biogeochemistry 41:237–257.  https://doi.org/10.1023/a:1005940630948 CrossRefGoogle Scholar
  3. Bloom NS (1994) Considerations in the analysis of water and fish for mercury. U.S. Environmental Protection Agency, Washington, DCGoogle Scholar
  4. Braaten HFV, de Wit HA, Fjeld E, Rognerud S, Lydersen E, Larssen T (2014) Environmental factors influencing mercury speciation in Subarctic and Boreal lakes. Sci Total Environ 476:336–345.  https://doi.org/10.1016/j.scitotenv.2014.01.030 CrossRefGoogle Scholar
  5. Bradley PM et al. (2011) Spatial and seasonal variability of dissolved methylmercury in two stream basins in the eastern United States. Environ Sci Technol 45:2048–2055.  https://doi.org/10.1021/es103923j CrossRefGoogle Scholar
  6. Brett MT et al. (2017) How important are terrestrial organic carbon inputs for secondary production in freshwater ecosystems? Freshw Biol 62:833–853.  https://doi.org/10.1111/fwb.12909 CrossRefGoogle Scholar
  7. Brigham ME, Wentz DA, Aiken GR, Krabbenhoft DP (2009) Mercury cycling in stream ecosystems. 1. Water column chemistry and transport. Environ Sci Technol 43:2720–2725.  https://doi.org/10.1021/es802694n CrossRefGoogle Scholar
  8. Brown RE, Nelson SJ, Saros JE (2017) Paleolimnological evidence of the consequences of recent increased dissolved organic carbon (DOC) in lakes of the northeastern USA. J Paleolimnol 57:19–35.  https://doi.org/10.1007/s10933-016-9913-3 CrossRefGoogle Scholar
  9. Browne DR, Rasmussen JB (2009) Shifts in the trophic ecology of brook trout resulting from interactions with yellow perch: an intraguild predator–prey interaction. Trans Am Fish Soc 138:1109–1122.  https://doi.org/10.1577/t08-113.1 CrossRefGoogle Scholar
  10. Buckman KL et al. (2015) Influence of a Chlor-alkali Superfund site on mercury bioaccumulation in periphyton and low-trophic level fauna. Environ Toxicol Chem  https://doi.org/10.1002/etc.2964
  11. Burns DA, Aiken GR, Bradley PM, Journey CA, Schelker J (2012) Specific ultra-violet absorbance as an indicator of mercury sources in an Adirondack River basin. Biogeochemistry 113:451–466.  https://doi.org/10.1007/s10533-012-9773-5 CrossRefGoogle Scholar
  12. Burns DA, Aiken GR, Bradley PM, Journey CA, Schelker J (2013) Specific ultra-violet absorbance as an indicator of mercury sources in an Adirondack River basin. Biogeochemistry 113:451–466.  https://doi.org/10.1007/s10533-012-9773-5 CrossRefGoogle Scholar
  13. Burns DA, Riva-Murray K (2018) Variation in fish mercury concentrations in streams of the Adirondack region, New York: a simplified screening approach using chemical metrics. Ecol Indic 84:648–661CrossRefGoogle Scholar
  14. Campbell LM, Norstrom RJ, Hobson KA, Muir DCG, Backus S, Fisk AT (2005) Mercury and other trace elements in a pelagic Arctic marine food web (Northwater Polynya, Baffin Bay). Sci Total Environ 351:247–263.  https://doi.org/10.1016/j.scitotenv.2005.02.043 CrossRefGoogle Scholar
  15. Caron S, Lucotte M, Teisserenc R (2008) Mercury transfer from watersheds to aquatic environments following the erosion of agrarian soils: a molecular biomarker approach. Can J Soil Sci 88:801–811CrossRefGoogle Scholar
  16. Chasar LC, Scudder BC, Stewart AR, Bell AH, Aiken GR (2009) Mercury cycling in stream ecosystems. 3. Trophic dynamics and methylmercury bioaccumulation. Environ Sci Technol 43:2733–2739.  https://doi.org/10.1021/es8027567 CrossRefGoogle Scholar
  17. Chaves-Ulloa R et al. (2016) Dissolved organic carbon modulates mercury concentrations in insect subsidies from streams to terrestrial consumers. Ecol Appl  https://doi.org/10.1890/15-0025.1
  18. Chen CY et al. (2014) Benthic and pelagic pathways of methylmercury bioaccumulation in estuarine food webs of the Northeast United States PLoS ONE 9:11. e89305.  https://doi.org/10.1371/journal.pone.0089305
  19. Chen CY, Stemberger RS, Klaue B, Blum JD, Pickhardt PC, Folt CL (2000) Accumulation of heavy metals in food web components across a gradient of lakes. Limnol Oceanogr 7.  https://doi.org/10.4319/lo.2000.45.7.1525
  20. Chen CY, Dionne M, Mayes BM, Ward DM, Sturup S, Jackson BP (2009) Mercury bioavailability and bioaccumulation in estuarine food webs in the Gulf of Maine. Environ Sci Technol 43:1804–1810.  https://doi.org/10.1021/es8017122 CrossRefGoogle Scholar
  21. Chen CY, Driscoll CT, Kamman NC (2012a) Mercury hotspots in freshwater ecosystems: drivers, processes, and patterns. In: Bank MS (ed.) Mercury in the environment: pattern and process. University of California Press, Berkeley and Los Angeles, CaliforniaGoogle Scholar
  22. Chen CY, Folt CL (2005) High plankton densities reduce mercury biomagnification. Environl Sci Technol 39:115–121.  https://doi.org/10.1021/es0403007 CrossRefGoogle Scholar
  23. Chen CY, Kamman N, Williams J, Bugge D, Taylor V, Jackson B, Miller E (2012b) Spatial and temporal variation in mercury bioaccumulation by zooplankton in Lake Champlain (North America). Environ Pollut 161:343–349.  https://doi.org/10.1016/j.envpol.2011.08.048 CrossRefGoogle Scholar
  24. Chen MM, Lopez L, Bhavsar SP, Sharma S (2018) What’s hot about mercury? Examining the influence of climate on mercury levels in Ontario top predator fishes. Environ Res 162:63–73CrossRefGoogle Scholar
  25. Chiasson-Gould SA, Blais JM, Poulain AJ (2014) Dissolved organic matter kinetically controls mercury bioavailability to bacteria. Environ Sci Technol 48:3153–3161.  https://doi.org/10.1021/es4038484 CrossRefGoogle Scholar
  26. Chumchal MM, Hambright KD (2009) Ecological factors regulating mercury contamination of fish from Caddo Lake, Texas, USA. Environ Toxicol Chem 28:962–972.  https://doi.org/10.1897/08-197.1 CrossRefGoogle Scholar
  27. Chumchal MM et al. (2011) Mercury speciation and biomagnification in the food web of Caddo Lake, Texas and Louisiana, USA, a Subtropical Freshwater Ecosystem. Environ Toxicol Chem 30:1153–1162.  https://doi.org/10.1002/etc.477 CrossRefGoogle Scholar
  28. Clark JM et al. (2010) The importance of the relationship between scale and process in understanding long-term DOC dynamics. Sci Total Environ 408:2768–2775.  https://doi.org/10.1016/j.scitotenv.2010.02.046 CrossRefGoogle Scholar
  29. Clarkson TW, Magos L, Myers GJ (2003) The toxicology of mercury— current exposures and clinical manifestations. New Engl J Med 349:1731–1737.  https://doi.org/10.1056/NEJMra022471 CrossRefGoogle Scholar
  30. Clayden MG, Kidd KA, Ct John, Hall BD, Garcia E (2014) Environmental, geographic and trophic influences on methylmercury concentrations in macroinvertebrates from lakes and wetlands across Canada. Ecotoxicology 23:273–284CrossRefGoogle Scholar
  31. Curtis AN, Bugge DM, Buckman KL, Feng XH, Faiia A, Chen CY (2017) Influence of sample preparation on estuarine macrofauna stable isotope signatures in the context of contaminant bioaccumulation studies. J Exp Mar Biol Ecol 493:1–6.  https://doi.org/10.1016/j.jembe.2017.03.010 CrossRefGoogle Scholar
  32. Dittman JA, Shanley JB, Driscoll CT, Aiken GR, Chalmers AT, Towse JE (2009) Ultraviolet absorbance as a proxy for total dissolved mercury in streams. Environ Pollut 157:1953–1956.  https://doi.org/10.1016/j.envpol.2009.01.031 CrossRefGoogle Scholar
  33. Dittman JA, Shanley JB, Driscoll CT, Aiken GR, Chalmers AT, Towse JE, Selvendiran P (2010) Mercury dynamics in relation to dissolved organic carbon concentration and quality during high flow events in three northeastern US streams. Water Resour Research 46:15, W07522.  https://doi.org/10.1029/2009wr008351
  34. Dodson SI, Arnott SE, Cottingham KL (2000) The relationship in lake communities between primary productivity and species richness. Ecology 81:2662–2679.  https://doi.org/10.1890/0012-9658(2000)081[2662:trilcb]2.0.co;2 CrossRefGoogle Scholar
  35. Driscoll CT, Blette V, Yan C, Schofield CL, Munson R, Holsapple J (1995) The role of dissolved organic-carbon in the chemistry and bioavailability of mercury in remote Adirondack Lakes. Water Air Soil Pollut 80:499–508.  https://doi.org/10.1007/bf01189700 CrossRefGoogle Scholar
  36. Driscoll CT et al. (2007) Mercury contamination in forest and freshwater ecosystems in the Northeastern United States. Bioscience 57:17–28.  https://doi.org/10.1641/b570106 CrossRefGoogle Scholar
  37. Driscoll CT, Yan C, Schofield CL, Munson R, Holsapple J (1994) The mercury cycle and fish in the Adirondack Lakes. Environ Sci Technol 28:A136–A143.  https://doi.org/10.1021/es00052a003 CrossRefGoogle Scholar
  38. Eagles-Smith CA, Herring G, Johnson B, Graw R (2016) Conifer density within lake catchments predicts fish mercury concentrations in remote subalpine lakes. Environ Pollut 212:279–289.  https://doi.org/10.1016/j.envpol.2016.01.049 CrossRefGoogle Scholar
  39. Evers DC et al. (2007) Biological mercury hotspots in the Northeastern United States and Southeastern Canada. BioScience 57:29–43.  https://doi.org/10.1641/b570107 CrossRefGoogle Scholar
  40. Evers DC et al. (2008) Adverse effects from environmental mercury loads on breeding common loons. Ecotoxicology 17:69–81.  https://doi.org/10.1007/s10646-007-0168-7 CrossRefGoogle Scholar
  41. Findlay S, McDowell WH, Fischer D, Pace ML, Caraco N, Kaushal SS, Weathers KC (2010) Total carbon analysis may overestimate organic carbon content of fresh waters in the presence of high dissolved inorganic carbon. Limnol Oceanogr-Methods 8:196–201.  https://doi.org/10.4319/lom.2010.8.196 CrossRefGoogle Scholar
  42. Fitzgerald WF, Engstrom DR, Mason RP, Nater EA (1998) The case for atmospheric mercury contamination in remote areas. Environ Sci Technol 32:1–7.  https://doi.org/10.1021/es970284w CrossRefGoogle Scholar
  43. French TD et al. (2014) Dissolved organic carbon thresholds affect mercury bioaccumulation in Arctic Lakes. Environ Sci Technol 48:3162–3168.  https://doi.org/10.1021/es403849d CrossRefGoogle Scholar
  44. Gilbert-Diamond D et al. (2011) Rice consumption contributes to arsenic exposure in US women. Proc Natl Acad Sci USA 108:20656CrossRefGoogle Scholar
  45. Gorski PR, Armstrong DE, Hurley JP, Krabbenhoft DP (2008) Influence of natural dissolved organic carbon on the bioavailability of mercury to a freshwater alga. Environ Pollut 154:116–123.  https://doi.org/10.1016/j.envpol.2007.12.004 CrossRefGoogle Scholar
  46. Gram WK et al. (2004) Distribution of plants in a California serpentine grassland: are rocky hummocks spatial refuges for native species? Plant Ecol 172:159–171.  https://doi.org/10.1023/B:VEGE.0000026332.57007.7b CrossRefGoogle Scholar
  47. Grigal DF (2002) Inputs and outputs of mercury from terrestrial watersheds: a review. Environ Rev 10:1–39CrossRefGoogle Scholar
  48. Haro RJ, Bailey SW, Northwick KR, Rolfus MB, Sandheinrich JG, Wiener JG (2013) Burrowing dragonfly larvae as biosentinels of methylmercury in freshwater food webs. Environ Sci Technol 47:8148–8156Google Scholar
  49. Hightower JM, Moore D (2003) Mercury levels in high-end consumers of fish. Environ Health Perspect 111:604–608.  https://doi.org/10.1289/ehp.5837 CrossRefGoogle Scholar
  50. Jackson B, Taylor B, Baker RA, Miller E (2009a) Low-level mercury speciation in freshwaters by isotope dilution GC-ICP-MS. Environ Sci Technol 43:2463–2469CrossRefGoogle Scholar
  51. Jackson B, Taylor V, Baker RA, Miller E (2009b) Low-Level Mercury Speciation in Freshwaters by Isotope Dilution GC–ICP–MS. Environ Sci Technol 43:2463–2469.  https://doi.org/10.1021/es802656p CrossRefGoogle Scholar
  52. Jardine TD, Kidd KA, O’ Driscoll N (2013) Food web analysis reveals effects of pH on mercury bioaccumulation at multiple trophic levels in streams. Aquat Toxicol 132-133:46–52CrossRefGoogle Scholar
  53. Jardine TD, Kidd KA, Rasmussen JB (2012) Aquatic and terrestrial organic matter in the diet of stream consumers: implications for mercury bioaccumulation. Ecol Appl 22:843–855CrossRefGoogle Scholar
  54. Jeremiason JD, Reiser TK, Weitz RA, Berdnt ME, Aiken GR (2016) Aeshnid dragonfly larvae as bioindicators of methylmercury contamination in aquatic systems impacted by elevated sulfate loading. Ecotoxicology 25:456–468CrossRefGoogle Scholar
  55. Jonsson S et al. (2017) Terrestrial discharges mediate trophic shifts and enhance methylmercury accumulation in estuarine biota. Sci Adv 3.  https://doi.org/10.1126/sciadv.1601239
  56. Julian P (2012) Mercury hotspot identification in Water Conservation Area 3, Florida, USA. Ann GIS 19:79–88.  https://doi.org/10.1080/19475683.2013.782469
  57. Kamman NC et al. (2005) Mercury in freshwater fish of northeast North America—a geographic perspective based on fish tissue monitoring databases. Ecotoxicology 14:163–180.  https://doi.org/10.1007/s10646-004-6267-9 CrossRefGoogle Scholar
  58. Karimi R, Chen CY, Folt CL (2016) Comparing nearshore benthic and pelagic prey as mercury sources to lake fish: the importance of prey quality and mercury content. Sci Total Environ 565:211–221.  https://doi.org/10.1016/j.scitotenv.2016.04.162 CrossRefGoogle Scholar
  59. Karimi R, Chen CY, Pickhardt PC, Fisher NS, Folt CL (2007) Stoichiometric controls of mercury dilution by growth. Proc Natl Acad Sci USA 104:7477–7482.  https://doi.org/10.1073/pnas.0611261104 CrossRefGoogle Scholar
  60. Kassambara A (2018) ggpubr: ‘ggplot2' Based Publication Ready Plots. http://www.sthda.com/english/rpkgs/ggpubr
  61. Kenney LA, Eagles-Smith CA, Ackerman JT, von Hippel FA (2014) Temporal Variation in Fish Mercury Concentrations within Lakes from the Western Aleutian Archipelago, Alaska. PLoS ONE 9.  https://doi.org/10.1371/journal.pone.0102244
  62. Kidd KA et al. (2012) Biomagnification of mercury through lake trout (Salvelinus namaycush) food webs of lakes with different physical, chemical and biological characteristics. Sci Total Environ 438:135–143.  https://doi.org/10.1016/j.scitotenv.2012.08.057 CrossRefGoogle Scholar
  63. Klaus JE, Hammerschmidt CR, Costello DM, Burton GAJ (2016) Net methylmercury production in 2 contrasting stream sediments and associated accumulation and toxicity to periphyton. Environ Toxicol Chem 35:1759–1765CrossRefGoogle Scholar
  64. Kusnierz PC, Stimmell SP, Leonard JBK (2014) Migration, size, and age structure of Brook Trout (Salvelinus fontinalis) from two Lake Superior Tributaries. Am Midl Nat 172:119–130.  https://doi.org/10.1674/0003-0031-172.1.119 CrossRefGoogle Scholar
  65. Kutner MH, Nachtsheim CJ, Neter J, Li W (2005) Applied linear statistical models, 5th edn. McGraw-Hill Irwin, New York, NYGoogle Scholar
  66. Lawson NM, Mason RP (2001) Concentration of mercury, methylmercury, cadmium, lead, arsenic, and selenium in the rain and stream water of two contrasting watersheds in western Maryland. Water Res 35:4039–4052CrossRefGoogle Scholar
  67. Leggett MF, Servos MR, Hesslein R, Johannsson O, Millard ES, Dixon DG (1999) Biogeochemical influences on the carbon isotope signatures of Lake Ontario biota. Can J Fish Aquat Sci 56:2211–2218.  https://doi.org/10.1139/f99-151 CrossRefGoogle Scholar
  68. Lenth R, Singhmann H, Love J, Buerkner P, Herve M (2019) emmeans: estimated marginal means, aka least-squares means. https://github.com/rvlenth/emmeans
  69. Mahaffey KR, Clickner RP, Jeffries RA (2009) Adult women's blood mercury concentrations vary regionally in the United States: associations with patterns of fish consumption (NHANES 1999–2004). Environ Health Perspect 117:47–53CrossRefGoogle Scholar
  70. Mergler D, Anderson HA, Chan LHM, Mahaffey KR, Murray M, Sakamoto M, Stern AH (2007) Methylmercury exposure and health effects in humans: a worldwide concern. Ambio 36:3–11CrossRefGoogle Scholar
  71. Merritt RW, Cummins KW, Berg WB (2008) An introduction to the aquatic insects of North America. 4th edn. Kendall/Hunt Publishing Company, Dubuque, IowaGoogle Scholar
  72. Mierle G, Ingram R (1991) The role of humic substances in the mobilization of mercury from watersheds. Water Air Soil Pollut 56:349–357.  https://doi.org/10.1007/bf00342282 CrossRefGoogle Scholar
  73. Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ 15N and animal age. Geochim Cosmochim Acta 48:1135–1140.  https://doi.org/10.1016/0016-7037(84)90204-7 CrossRefGoogle Scholar
  74. Minor E, Stephens B (2008) Dissolved organic matter characterics within the Lake Superior watershed. Org Geochem 39:1489–1501CrossRefGoogle Scholar
  75. Monteith DT et al. (2007) Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry. Nature 450:U537–U539.  https://doi.org/10.1038/nature06316 CrossRefGoogle Scholar
  76. Mullane JM, Flury M, Iqbal H, Freeze PM, Hinman C, Cogger CG, Shi ZQ (2015) Intermittent rainstorms cause pulses of nitrogen, phosphorus, and copper in leachate from compost in bioretention systems. Sci Total Environ 537:294–303.  https://doi.org/10.1016/j.scitotenv.2015.07.157 CrossRefGoogle Scholar
  77. Pennak RW (1953) Fresh-water invertebrates of the United States. The Ronald Press Company, New York, NYGoogle Scholar
  78. Peterson BJ, Fry B (1987) Stable isotope in ecosystem studies. Annu Rev Ecol Syst 18:293–320.  https://doi.org/10.1146/annurev.ecolsys.18.1.293 CrossRefGoogle Scholar
  79. Peterson BJ, Howarth RW, Garritt RH (1985) Multiple stable isotopes used to trace the flow of organic-matter in estuarine food webs. Science 227:1361–1363.  https://doi.org/10.1126/science.227.4692.1361 CrossRefGoogle Scholar
  80. Pickhardt PC, Fisher NS (2007) Accumulation of inorganic and methylmercury by freshwater phytoplankton in two contrasting water bodies. Environ Sci Technol 41:125–131.  https://doi.org/10.1021/es060966w CrossRefGoogle Scholar
  81. Pickhardt PC, Folt CL, Chen CY, Klaue B, Blum JD (2002) Algal blooms reduce the uptake of toxic methylmercury in freshwater food webs. Proc Natl Acad Sci USA 99:4419–4423.  https://doi.org/10.1073/pnas.072531099 CrossRefGoogle Scholar
  82. Point D et al. (2007) Simultaneous determination of inorganic mercury, methylmercury, and total mercury concentrations in cryogenic fresh-frozen and freeze-dried biological reference materials. Anal Bioanal Chem 389:787–798.  https://doi.org/10.1007/s00216-007-1516-4 CrossRefGoogle Scholar
  83. Post JR, McQueen DJ (1994) Variabil-ity in first-year growth of Yellow Perch (Perca flavescens)—predictions from a simple-model, observations, and an experiment. Can J Fish Aquat Sci 51:2501–2512.  https://doi.org/10.1139/f94-249 CrossRefGoogle Scholar
  84. Power M, Klein GM, Guiguer K, Kwan MKH (2002) Mercury accumulation in the fish community of a sub-Arctic lake in relation to trophic position and carbon sources. J Appl Ecol 39:819–830.  https://doi.org/10.1046/j.1365-2664.2002.00758.x CrossRefGoogle Scholar
  85. Riva-Murray K et al. (2013) Influence of dietary carbon on mercury bioaccumulation in streams of the Adirondack Mountains of New York and the Coastal Plain of South Carolina, USA. Ecotoxicology 22:60–71.  https://doi.org/10.1007/s10646-012-1003-3 CrossRefGoogle Scholar
  86. Riva-Murray K, Chasar LC, Bradley PM, Burns DA, Brigham ME, Smith MJ, Abrahamsen TA (2011) Spatial patterns of mercury in macroinvertebrates and fishes from streams of two contrasting forested landscapes in the eastern United States. Ecotoxicology 20:1530–1542CrossRefGoogle Scholar
  87. Roebuck HJ (2009) Methylmercury production and accumulation in relation to water chemistry, landscape, and biotic characteristics of the Lake Sunapee Watershed, New Hampshire. Bates CollegeGoogle Scholar
  88. Romani AM, Vazquez E, Butturini A (2006) Microbial availability and size fractionation of dissolved organic carbon after drought in an intermittent stream: biogeochemical link across the stream–riparian interface. Microb Ecol 52:501–512.  https://doi.org/10.1007/s00248-006-9112-2 CrossRefGoogle Scholar
  89. Rounick JS, Winterbourn MJ, Lyon GL (1982) Differential utilization of allochthonous and autochthonous inputs by aquatic invertebrates in some New Zealand streams—a stable carbon isotope study. Oikos 39:191–198.  https://doi.org/10.2307/3544485 CrossRefGoogle Scholar
  90. Roy V, Amyot M, Carignan R (2009) Beaver ponds increase methylmercury concentrations in Canadian Shield Streams along vegetation and pond-age gradients. Environ Sci Technol 43:5605–5611CrossRefGoogle Scholar
  91. Scheulhammer 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.  https://doi.org/10.1579/0044-7447(2007)36[12:eoemot]2.0.co;2 CrossRefGoogle Scholar
  92. Schuster PF et al. (2008) Mercury and organic carbon dynamics during runoff episodes from a northeastern USA watershed. Water Air Soil Pollut 187:89–108.  https://doi.org/10.1007/s11270-007-9500-3 CrossRefGoogle Scholar
  93. Selin NE, Jacob DJ (2008) Seasonal and spatial patterns of mercury wet deposition in the United States: constraints on the contribution from North American anthropogenic sources. Atmos Environ 42:5193–5204CrossRefGoogle Scholar
  94. Shanley JB, Kamman NC, Clair TA, Chalmers AT (2005) Physical controls on total ant methylmercury concentrations in streams and lakes of the northeastern. Ecotoxicology 14:125–134CrossRefGoogle Scholar
  95. Shanley JB et al. (2008) Comparison of total mercury and methylmercury cycling at five sites using the small watershed approach. Environ Pollut 154:143–154.  https://doi.org/10.1016/j.envpol.2007.12.031 CrossRefGoogle Scholar
  96. Simonin HA, Loukmas JJ, Skinner LC, Roy KA (2008) Lake variability: Key factors controlling mercury concentrations in New York State fish. Environ Pollut 154:107–115.  https://doi.org/10.1016/j.envpol.2007.12.032 CrossRefGoogle Scholar
  97. 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 51:1065–1076.  https://doi.org/10.1139/f94-106 CrossRefGoogle Scholar
  98. Sunderland EM (2007) Mercury exposure from domestic and imported estuarine and marine fish in the U.S. seafood market. Environ Health Perspect 115:235–242CrossRefGoogle Scholar
  99. Taylor VF, Carter A, Davies C, Jackson BP (2011) Trace-level automated mercury speciation analysis. Anal Methods 3:1143–1148.  https://doi.org/10.1039/c0ay00528b CrossRefGoogle Scholar
  100. Taylor VF, Jackson BP, Chen CY (2008) Mercury speciation and total trace element determination of low-biomass biological samples. Anal Bioanal Chem 392:1283–1290.  https://doi.org/10.1007/s00216-008-2403-3 CrossRefGoogle Scholar
  101. Team RC (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing. http://www.R-project.org/
  102. Thorp JH, Covich AP (2010) Ecology and classification of North American freshwater Invertebrates. Elsevier Inc, Boston, MAGoogle Scholar
  103. Tremblay A, Cloutier L, Lucotte M (1998) Total mercury and methylmercury fluxes via emerging insects in recently flooded hydroelectric reservoirs and a natural lake. Sci Total Environ 219:209–221.  https://doi.org/10.1016/s0048-9697(98)00227-7 CrossRefGoogle Scholar
  104. Tsui MTK, Blum JD, Finlay JC, Balogh SJ, Kwon SY, Nollet YH (2013) Photodegradation of methylmerucy in stream ecosystems. Limnol Oceanogr 58:13–22CrossRefGoogle Scholar
  105. Tsui MTK, Finlay JC (2011) Influence of dissolved organic carbon on methylmercury bioavailability across Minnesota stream ecosystems. Environ Sci Technol 45:5981–5987.  https://doi.org/10.1021/es200332f CrossRefGoogle Scholar
  106. Tsui MTK, Finlay JC, Balogh SJ, Nollet YH (2010) In situ production of methylmercury within a stream channel in Northern California. Environ Sci Technol 44:6998–7004.  https://doi.org/10.1021/es101374y CrossRefGoogle Scholar
  107. Tsui MTK, Finlay JC, Nater EA (2009) Mercury bioaccumulation in a stream network. Environ Sci Technol 43:7016–7022.  https://doi.org/10.1021/es901525w CrossRefGoogle Scholar
  108. USEPA (1996) Method 1669: Sampling ambient water for trace metals at EPA water quality criteria levels. Office of Water, Engineering and Analysis Division, US Environmental Protection Agency, Washington, DCGoogle Scholar
  109. USEPA (2013) National listing of fish advisories. Technical fact sheet: EPA-820-F-11-727 009Google Scholar
  110. Vander Zanden MJ, Rasmussen JB (2001) Variation in d15N and d13C trophic fractionation: Implications for aquatic food web studies. Limnol Oceanogr 46:2061–2066.  https://doi.org/10.4319/lo.2001.46.8.2061 CrossRefGoogle Scholar
  111. Vidon P, Carleton W, Mitchell MJ (2014a) Mercury proxies and mercury dynamics in a forested watershed of the US Northeast. Environ Monit Assess 186:7475–7488CrossRefGoogle Scholar
  112. Vidon P, Carleton W, Mitchell MJ (2014b) Spatial and temporal variability in stream dissolved organic carbon quantity and quality in an Adirondack forested catchment. Appl Geochem 46:10–18CrossRefGoogle Scholar
  113. Vidon P, Wagner LE, Soyeux E (2008) Changes in the character of DOC in streams during storms in two Midwestern watersheds with contrasting land uses. Biogeochemistry 88:257–270CrossRefGoogle Scholar
  114. Vuorio K, Meili M, Sarvala J (2006) Taxon‐specific variation in the stable isotopic signatures (δ13C and δ15N) of lake phytoplankton. Freshw Biol 51:807–822.  https://doi.org/10.1111/j.1365-2427.2006.01529.x CrossRefGoogle Scholar
  115. Wang Y, Gu BH, Lee MK, Jiang SJ, Xu YF (2014) Isotopic evidence for anthropogenic impacts on aquatic food web dynamics and mercury cycling in a subtropical wetland ecosystem in the US. Sci Total Environ 487:557–564.  https://doi.org/10.1016/j.scitotenv.2014.04.060 CrossRefGoogle Scholar
  116. Ward DM, Nislow KH, Folt CL (2010) Bioaccumulation syndrome: identifying factors that make some stream food webs prone to elevated mercury bioaccumulation. Year in ecology and conservation biology. Blackwell Publishing, Oxford, pp. 62–83Google Scholar
  117. Ward DM, Nislow KH, Folt CL (2012) Do low-mercury terrestrial resources subsidize low-mercury growth of stream fish? Differences between species along a productivity gradient. PLoS ONE 7.  https://doi.org/10.1371/journal.pone.0049582
  118. Watras CJ, Back RC, Halvorsen S, Hudson RJM, Morrison KA, Wente SP (1998) Bioaccumulation of mercury in pelagic freshwater food webs. Sci Total Environ 219:183–208.  https://doi.org/10.1016/s0048-9697(98)00228-9 CrossRefGoogle Scholar
  119. Wickham H (2017) tidyverse: easily install and load the ‘Tidyverse’. https://CRAN.R-project.org/package=tidyverse
  120. Wiener JG, Krabbenhoft DP, Heinz GH, Scheuhammer AM (2003) Ecotoxicology of mercury. In: Hoffman DJ, Rattner BA, Burton GAJ, Cairns JJ (eds) Handbook of ecotoxicology, 2nd edn. Lewis Publishers, Boca Raton, FL, USAGoogle Scholar
  121. Wiggins GB (2000) Larvae of the North American caddisfly genera (Trichoptera), 2nd edn. Toronto Press, Buffalo, New YorkGoogle Scholar
  122. Zhang L, Campbell LM, Johnson TB (2012) Seasonal variation in mercury and food web biomagnification in Lake Ontario, Canada. Environ Pollut 161:178–184CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of Environmental ConservationUniversity of MassachusettsAmherstUSA
  2. 2.Department of Biological SciencesDartmouth CollegeHanoverUSA
  3. 3.Environmental Studies ProgramBates CollegeLewistonUSA
  4. 4.Department of Natural and Environmental SciencesColby-Sawyer CollegeNew LondonUSA
  5. 5.Cary Institute of Ecosystem StudiesMillbrookUSA
  6. 6.Department of General EducationWestern Governors UniversitySalt Lake CityUSA

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