Abstract
We assessed the ecological risk of mercury (Hg) in aquatic systems by monitoring common loon (Gavia immer) population dynamics and blood Hg concentrations. We report temporal trends in blood Hg concentrations based on 334 samples collected from adults recaptured in subsequent years (resampled 2–9 times) and from 421 blood samples of chicks collected at lakes resampled 2–8 times 1992–2010. Temporal trends were identified with generalized additive mixed effects models and mixed effects models to account for the potential lack of independence among observations from the same loon or same lake. Trend analyses indicated that Hg concentrations in the blood of Wisconsin loons declined over the period 1992–2000, and increased during 2002–2010, but not to the level observed in the early 1990s. The best fitting linear mixed effects model included separate trends for the two time periods. The estimated trend in Hg concentration among the adult loon population during 1992–2000 was −2.6% per year, and the estimated trend during 2002–2010 was +1.8% per year; chick blood Hg concentrations decreased −6.5% per year during 1992–2000, but increased 1.8% per year during 2002–2010. This bi-phasic pattern is similar to trends observed for concentrations of methylmercury and SO4 in lake water of an intensely studied seepage lake (Little Rock Lake, Vilas County) within our study area. A cause-effect relationship between these independent trends is hypothesized.
Similar content being viewed by others
References
Asplund TR (2008) Implications of low water levels for natural lake ecosystems (abstract), Am Water Resour Assoc, 32nd annual meeting of Wisconsin chapter, March 6–7, 2008, Brookfield, WI
Asplund TR, Knight S (2009) Implications of sustained low water levels for seepage lakes in northern Wisconsin (abstract). Am Water Resour Assoc, 33rd annual meeting of Wisconsin chapter, March 5–6, 2009, Stevens Point, WI
Barr JF (1986) Population dynamics of the common loon (Gavia immer) associated with mercury-contaminated waters in northwestern Ontario. Can Wildl Serv Occas Pap 56
Bhavsar SP, Gewurtz SG, McGoldrich DJ, Keir MJ, Backus SM (2010) Changes in mercury levels in great lakes fish between 1970s and 2007. Environ Sci Technol 44:3273–3279
Bloom NS, Watras CJ, Hurley JP (1991) Impact of acidification on the methylmercury cycle of remote seepage lakes. Water Air Soil Pollut 56:477–491
Burgess NM, Meyer MW (2008) Methylmercury exposure associated with reduced productivity in common loons. Ecotoxicology 17:83–91
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York
Chen CY, Folt CL (2005) High plankton densities reduce mercury biomagnification. Environ Sci Technol 39:115–121
Cope WG, Wiener JG, Rada RG (1990) Mercury accumulation in yellow perch in Wisconsin seepage lakes: relation to lake characteristics. Environ Toxicol Chem 9:931–940
Draper NR, Smith H (1981) Applied regression analysis, 2nd edn. Wiley, New York
Drevnick PE, Canfield DE, Gorski PR, Shinneman AL, Engstrom DR, Muir DC, Smith GR, Garrison PJ, Cleckner LB, Hurley JP, Noble RB, Otter RR, Oris JT (2007) Deposition and cycling of sulfur controls mercury accumulation in Isle Royale fish. Environ Sci Technol 41:7266–7272
Evers DC (1993) A replicable capture method for adult and juvenile common loons on their nesting lakes. In: Stockwell F (ed) Proceedings from the 1992 conference on the loon and its ecosystem: status, management and environmental concerns. North American Loon Fund, Holderness, NH, pp 214–220
Evers DC, Kaplan JD, Meyer MW, Reaman PS, Braselton WE, Major A, Burgess N, Scheuhammer AM (1998) A geographic trend in mercury exposure measured in common loon feathers and blood. Environ Toxicol Chem 17:173–183
Fevold BM, Meyer MW, Rasmussen PW, Temple SA (2003) Bioaccumulation patterns and temporal trends of mercury exposure in Wisconsin common loons. Ecotoxicology 12:83–93
Fitzmaurice GM, Laird NM, Ware JH (2004) Applied longitudinal analysis. Wiley, New York
Grear JS, Meyer MW, Cooley JH, Kuhn A, Piper W, Taylor K, Kenow K, Mitro M, Vogel H, Nacci D (2009) Population growth and demography of a long-lived piscivorous bird in lakes of the northern United States. J Wildl Manage 73:1108–1113
Hrabik TR, Watras CJ (2002) Recent declines in mercury concentration in a freshwater fishery: isolating the effects of deacidification and decreased atmospheric mercury deposition in Little Rock Lake. Sci Tot Environ 297:229–237
Hurley JP, Watras CJ, Bloom NS (1991) Mercury cycling in a northern Wisconsin seepage lake: the role of particulate matter in vertical transport. Water Air Soil Pollut 56:543–551
Kenow KP, Gutreuter S, Hines RK, Meyer MW, Fournier F, Karasov WH (2003) Effects of methyl mercury exposure on the growth of juvenile common loons. Ecotoxicology 12:171–182
Kenow KP, Grasman KA, Hines RK, Meyer MW, Gendron-Fitzpatrick A, Spalding MG, Gray BR (2007a) Effects of methylmercury exposure on the immune function of juvenile common loons. Environ Toxicol Chem 26:1460–1469
Kenow KP, Meyer MW, Hines RK, Karasov WH (2007b) Distribution and accumulation of mercury in tissues and organs of captive-reared common loon (Gavia immer) chicks. Environ Toxicol Chem 26:1047–1055
Kenow KP, Hoffman DJ, Hines RK, Meyer MW, Bickham JW, Matson CW, Stebbins KR, Montagna P, Elfessi A (2008) Effects of methylmercury exposure on glutathione metabolism, oxidative stress, and chromosomal damage in captive-reared common loon (Gavia immer) chicks. Environ Pollut 156:732–738
Kenow KP, Hines RK, Meyer MW, Suarez SA, Gray BR (2010) Effects of methylmercury exposure on the behavior of captive-reared common loon (Gavia immer) chicks. Ecotoxicology 19:933–944
Kenow KP, Meyer MW, Rossmann R, Gendron-Fitzpatrick A, Gray BR (2011) Effects of injected methylmercury on the hatching of common loon (Gavia immer) eggs. Ecotoxicology. doi:10.1007/s10646-011-0743-9
Kenoyer GJ, Anderson MP (1989) Groundwater’s dynamic role in regulating acidity and chemistry in a precipitation dominated lake. J Hydrol 109:287–309
Littell RC, Milliken GA, Stroujp WW, Wolfinger RD (1996) SAS system for mixed models. SAS Institute, Inc., Cary, NC
Madsen ER, Stern HS (2007) Time trends of methylmercury in walleye in northern Wisconsin: a hierarchical Bayesian analysis. Environ Sci Technol 41:4568–4573
Merrill EH, Hartigan JJ, Meyer MW (2005) Does prey biomass or mercury exposure affect loon chick survival in Wisconsin? J Wildl Manage 69:57–67
Meyer MW, Evers D, Daulton T (1995) Common loons nesting on acidified lakes in northern Wisconsin have elevated mercury exposure. Water Air Soil Pollut 80:871–880
Meyer MW, Evers DC, Hartigan JJ, Rasmussen PS (1998) Patterns of common loon (Gavia immer) mercury exposure, reproduction, and survival in Wisconsin, USA. Environ Toxicol Chem 17:184–190
Monson B (2009) Trend reversal of mercury concentrations in piscivorous fish from Minnesota lakes: 1982–2006. Environ Sci Technol 43:1750–1755
Nocera JJ, Taylor PD (1998) In situ behavioral response of common loons associated with elevated mercury (Hg) exposure. Conserv Ecol [online] 2(2): 10. Available at http://www.consecol.org/vol2/iss2/art10/. Accessed 13 June 2011
Ott WR (1995) Environmental statistics and data analysis. Lewis Publishers, Boca Raton, FL
Rasmussen PW, Schrank CS, Campfield PA (2007) Temporal trends of mercury concentrations in Wisconsin walleye (Sander vitreus), 1982–2005. Ecotoxicology 16:541–550
Scheuhammer AM, Atchison CM, Wong AHK, Evers DC (1998) Mercury exposure in breeding common loons (Gavia immer) in central Ontario, Canada. Environ Toxicol Chem 17:191–196
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
Simoneau M, Lucotte M, Garceau S, Laliberte D (2005) Fish growth rates modulate mercury concentrations in walleye (Sander vitreus) from eastern Canadian lakes. Environ Res 98:73–82
Sullivan JR, Delfino JJ (1982) The determination of mercury in fish. J Environ Sci Health A17:265–275
Vanarsdale A, Weiss J, Keeler G, Miller E, Boulet G, Brulotte R, Poissant L (2005) Patterns of mercury deposition and concentration in northeast North America (1996–2002). Ecotoxicology 14:37–52
Venables WN, Dichmont CM (2004) GLMs, GAMs, and GLMMs: an overview of theory for applications in fisheries research. Fish Res 70:319–337
Verbeke G, Molenberghs G (2000) Linear mixed models for longitudinal data. Springer, New York
Watras CJ (2009) Mercury pollution in remote freshwaters. In: Likens GE (ed) Encyclopedia of inland waters, vol 3. Oxford, UK, pp 100–109
Watras CJ, Morrison KA (2008) The response of two remote temperate lakes to changes in atmospheric mercury deposition, sulfate, and the water cycle. Can J Fish Aquat Sci 65:100–116
Watras CJ, Bloom NS, Hudson RJM, Gherini S, Munson R, Claas SA, Morrison KA, Hurley J, Wiener JG, Fitzgerald WF, Mason R, Vandal G, Powell D, Rada R, Rislove L, Winfrey M, Elder J, Krabbenhoft D, Andren AW, Babiarz C, Porcella DB, Huckabee JW (1994) Sources and fates of mercury and methylmercury in Wisconsin lakes. In: Watras CJ, Huckabee JW (eds) Mercury pollution: integration and synthesis. Lewis Publishers, Boca Raton, FL, pp 153–177
Watras CJ, Morrison KA, Hudson RJM, Frost TM, Kratz TK (2000) Decreasing mercury in northern Wisconsin: temporal patterns in bulk precipitation and a precipitation dominated lake. Environ Sci Technol 34:4051–4057
Watras CJ, Morrison KA, Kent A, Price N, Regnell O, Eckley C, Hintelmann H, Hubachert T (2005) Sources of methylmercury to a wetland-dominated lake in northern Wisconsin. Environ Sci Technol 39:4747–4758
Watras CJ, Morrison KA, Regnell O, Kratz TK (2006) The methylmercury cycle in Little Rock Lake during experimental acidification and recovery. Limnol Oceanogr 51:257–270
Webster KE, Kratz TK, Bowser CJ, Magnuson JJ (1996) The influence of landscape position on lake chemical responses to drought in northern Wisconsin. Limnol Oceanogr 41:977–984
Wentz DA, Rose WJ, Webster KE (1995) Long-term hydrologic and biogeochemical responses of a soft water seepage lake in north central Wisconsin. Water Resour Res 31:199–212
Wiener JG, Krabbenhoft DP, Heinz GH, Scheuhammer AM (2003) Ecotoxicology of mercury. In: Hoffman DJ, Rattner BA, Burton GA, Cairns J (eds) Handbook of ecotoxicology, 2nd edn. Lewis Publishers, Boca Raton, FL, pp 409–463
Wood SN (2006) Generalized additive models: an introduction with R. Chapman and Hall, CRC Press, Boca Raton, FL
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York
Acknowledgments
Several dozen field staff endured the long nights of loon capture and sampling over the past 20 years to provide the data for this study. Dr. David Evers, Biodiversity Research Institute, conducted the initial sampling and trained WDNR staff in proper common loon capture and handling techniques. R. Arneson (WDNR) coordinated the project’s laboratory work at the Wisconsin State Laboratory of Hygiene where analytical services were provided by D. Kennedy-Parker and staff. Supervisory support for long-term Hg monitoring at WDNR was provided by G. Bartelt, D. Knauer, K. Martin, R. Dumke, and J. Sullivan, Bureau of Science Services. This project was supported through the WDNR with funds from the Federal Aid in Wildlife Restoration Project W-160-P, the Wisconsin Acid Deposition Research Council, the Wisconsin Utilities Association, the Electric Power Research Institute, USEPA Science To Achieve Results grant R82-905, the USGS Upper Midwest Environmental Science Center, and BioDiversity Research Institute. We thank C. Schrank (WDNR) and B. Gray (USGS UMESC) for reviewing an earlier draft of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Meyer, M.W., Rasmussen, P.W., Watras, C.J. et al. Bi-phasic trends in mercury concentrations in blood of Wisconsin common loons during 1992–2010. Ecotoxicology 20, 1659–1668 (2011). https://doi.org/10.1007/s10646-011-0759-1
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-011-0759-1