Skip to main content
Log in

Mercury Bioaccumulation in Lacustrine Fish Populations Along a Climatic Gradient in Northern Ontario, Canada

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

Climate change is predicted to alter many processes in boreal aquatic ecosystems, including mercury (Hg) bioaccumulation in fish. We investigated current patterns in fish Hg across a climatic gradient in northern Ontario, Canada, to assess the possible influence of further climate change. Cohabiting populations of walleye (a piscivore) and white sucker (a benthivore) were sampled from lakes spanning over 9.0° of latitude (45° 24′ N–54° 20′ N). Latitudinal trends were evident in climatic conditions, as well as several other ecosystem characteristics over this range. Muscle total Hg concentration ([THg]) was modelled with respect to climatic variables as well as other physical, chemical, and biological variables, and all models were ranked by Akaike information criterion. Neither long-term mean temperature nor precipitation was a strong predictor of current muscle [THg] in either species across this region. Instead, drainage basin characteristics (for example, mean slope) and lake water chemistry (for example, [DOC], [SO4]) were the strongest predictors, followed by fish biological traits (for example, muscle δ13C). Walleye [THg] was more strongly related to water chemistry, and white sucker [THg] was more strongly related to drainage basin physical characteristics. For both species, muscle [THg] showed unimodal relationships with several predictors (for example, latitude, [SO4], [DOC]), peaking in their mid-ranges. Fish [THg] is not strongly associated with current climatic conditions across northern Ontario but may be influenced by climate change in future through indirect effects on water chemistry and food web structure.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  • Adrian R, O’Reilly CM, Zagarese H, Baines SB, Hessen DO, Keller W, Livingstone DM, Sommaruga R, Straile D, Van Donk E, Weyhenmeyer GA, Winder M. 2009. Lakes as sentinels of climate change. Limnol Oceanogr 54:2283–97.

    PubMed  PubMed Central  Google Scholar 

  • Ahonen SA, Hayden B, Leppänen JJ, Kahilainen KK. 2018. Climate and productivity affect total mercury concentration and bioaccumulation rate of fish along a spatial gradient of subarctic lakes. Sci Total Environ 637–638:1586–96.

    PubMed  Google Scholar 

  • Anderson DR. 2008. Model based inference in the life sciences: a primer on evidence. New York: Springer.

    Google Scholar 

  • Baumann Z, Mason RP, Conover DO, Balcom P, Chen CY, Buckman KL, Fisher NS, Baumann H. 2016. Mercury bioaccumulation increases with latitude in a coastal marine fish (Atlantic silverside, Menidia menidia). Can J Fish Aquat Sci 74:1009–15.

    PubMed  PubMed Central  Google Scholar 

  • Belzile N, Chen Y-W, Gunn JM, Tong J, Alarie Y, Delonchamp T, Lang C-Y. 2006. The effect of selenium on mercury assimilation by freshwater organisms. Can J Fish Aquat Sci 63:1–10.

    CAS  Google Scholar 

  • Benoit JM, Gilmour CC, Heyes A, Mason RP, Miller CL. 2003. Geochemical and biological controls over methylmercury production and degradation in aquatic ecosystems. Cai Y, Braids OC editors. Biogeochemistry of Environmentally Important Trace Elements. Washington, DC, USA: American Chemical Society, pp 262–97.

  • Bodaly RA, Rudd JW, Fudge RJ. 1993. Mercury concentrations in fish related to size of remote Canadian Shield Lakes. Can J Fish Aquat Sci 50:980–7.

    CAS  Google Scholar 

  • Braaten HFV, de Wit HA, Larssen T, Poste AE. 2018. Mercury in fish from Norwegian lakes: the complex influence of aqueous organic carbon. Sci Total Environ 627:341–8.

    CAS  PubMed  Google Scholar 

  • Branfireun BA, Roulet NT, Kelly CA, Rudd JWM. 1999. In situ sulphate stimulation of mercury methylation in a boreal peatland: toward a link between acid rain and methylmercury contamination in remote environments. Global Biogeochem Cycles 13:743–50.

    CAS  Google Scholar 

  • Bravo AG, Bouchet S, Tolu J, Björn E, Mateos-Rivera A, Bertilsson S. 2017. Molecular composition of organic matter controls methylmercury formation in boreal lakes. Nat Commun 8:14255.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burnham KP, Anderson DR. 2004. Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res 33:261–304.

    Google Scholar 

  • Burnham KP, Anderson DR, Huyvaert KP. 2011. AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65:23–35.

    Google Scholar 

  • Cabana G, Rasmussen JB. 1994. Modelling food chain structure and contaminant bioaccumulation using stable nitrogen isotopes. Nature 372:255–7.

    CAS  Google Scholar 

  • Cabana G, Rasmussen JB. 1996. Comparison of aquatic food chains using nitrogen isotopes. Proc Natl Acad Sci USA 93:10844–7.

    CAS  PubMed  Google Scholar 

  • Cabana G, Tremblay A, Kalff J, Rasmussen JB. 1994. Pelagic food chain structure on Ontario lakes: a determinant of mercury levels in lake trout (Salvelinus namaycush). Can J Fish Aquat Sci 51:381–9.

    CAS  Google Scholar 

  • Chen CY, Folt CL. 2005. High plankton densities reduce mercury biomagnification. Environ Sci Technol 39:115–21.

    CAS  PubMed  Google Scholar 

  • Chen CY, Stemberger RS, Kamman NC, Mayes BM, Folt CL. 2005. Patterns of Hg bioaccumulation and transfer in aquatic food webs across multi-lake studies in the northeast US. Ecotoxicology 14:135–47.

    CAS  PubMed  Google Scholar 

  • 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 162:63–73.

    CAS  PubMed  Google Scholar 

  • Coleman Wasik JK, Engstrom DR, Mitchell CPJ, Swain EB, Monson BA, Balogh SJ, Jeremiason JD, Branfireun BA, Kolka RK, Almendinger JE. 2015. The effects of hydrologic fluctuation and sulfate regeneration on mercury cycling in an experimental peatland. J Geophys Res Biogeosci 120:1697–715.

    CAS  Google Scholar 

  • Coleman Wasik JK, Mitchell CPJ, Engstrom DR, Swain EB, Monson BA, Balogh SJ, Jeremiason JD, Branfireun BA, Eggert SL, Kolka RK, Almendinger JE. 2012. Methylmercury declines in a boreal peatland when experimental sulfate deposition decreases. Environ Sci Technol 46:6663–71.

    CAS  PubMed  Google Scholar 

  • Creed IF, Bergström A-K, Trick CG, Grimm NB, Hessen DO, Karlsson J, Kidd KA, Kritzberg E, McKnight DM, Freeman EC, Senar OE, Andersson A, Ask J, Berggren M, Cherif M, Giesler R, Hotchkiss ER, Kortelainen P, Palta MM, Vrede T, Weyhenmeyer GA. 2018. Global change-driven effects on dissolved organic matter composition: implications for food webs of northern lakes. Glob Change Biol 24:3692–714.

    Google Scholar 

  • de Wit HA, Valinia S, Weyhenmeyer GA, Futter MN, Kortelainen P, Austnes K, Hessen DO, Räike A, Laudon H, Vuorenmaa J. 2016. Current browning of surface waters will be further promoted by wetter climate. Environ Sci Technol Lett 3:430–5.

    Google Scholar 

  • Dennis IF, Clair TA, Driscoll CT, Kamman N, Chalmers A, Shanley J, Norton SA, Kahl S. 2005. Distribution patterns of mercury in lakes and rivers of northeastern North America. Ecotoxicology 14:113–23.

    CAS  PubMed  Google Scholar 

  • Downs SG, MacLeod CL, Lester JN. 1998. Mercury in precipitation and its relation to bioaccumulation in fish: a literature review. Water Air Soil Pollut 108:149–87.

    CAS  Google Scholar 

  • Drevnick PE, Canfield DE, Gorski PR, Shinneman ALC, Engstrom DR, Muir DCG, 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 41:7266–72.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Eckley CS, Watras CJ, Hintelmann H, Morrison K, Kent AD, Regnell O. 2005. Mercury methylation in the hypolimnetic waters of lakes with and without connection to wetlands in northern Wisconsin. Can J Fish Aquat Sci 62:400–11.

    CAS  Google Scholar 

  • Edlund M, Almendinger J, Fang X, Hobbs J, VanderMeulen D, Key R, Engstrom D. 2017. Effects of climate change on lake thermal structure and biotic response in northern wilderness lakes. Water 9:678.

    Google Scholar 

  • Fitzgerald WF, Engstrom DR, Mason RP, Nater EA. 1998. The case for atmospheric mercury contamination in remote areas. Environ Sci Technol 32:1–7.

    CAS  Google Scholar 

  • French TD, Houben AJ, Desforges JPW, Kimpe LE, Kokelj SV, Poulain AJ, Smol JP, Wang XW, Blais JM. 2014. Dissolved organic carbon thresholds affect mercury bioaccumulation in Arctic lakes. Environ Sci Technol 48:3162–8.

    CAS  PubMed  Google Scholar 

  • Fry B. 2006. Stable isotope ecology. New York: Springer.

    Google Scholar 

  • Gandhi N, Bhavsar SP, Tang RW-K, Arhonditsis GB. 2015. Projecting fish mercury levels in the province of Ontario, Canada and the implications for fish and human health. Environ Sci Technol 49:14494–502.

    CAS  PubMed  Google Scholar 

  • Gandhi N, Tang RWK, Bhavsar SP, Arhonditsis GB. 2014. Fish mercury levels appear to be increasing lately: a report from 40 years of monitoring in the province of Ontario, Canada. Environ Sci Technol 48:5404–14.

    CAS  PubMed  Google Scholar 

  • Gantner N, Muir DC, Power M, Iqaluk D, Reist JD, Babaluk JA, Meili M, Borg H, Hammar J, Michaud W, Dempson B, Solomon KR. 2010. Mercury concentrations in landlocked Arctic char (Salvelinus alpinus) from the Canadian Arctic. Part II: influence of lake biotic and abiotic characteristics on geographic trends in 27 populations. Environ Toxicol Chem 29:633–43.

    CAS  PubMed  Google Scholar 

  • Gilmour CC, Henry EA, Mitchell R. 1992. Sulfate stimulation of mercury methylation in freshwater sediments. Environ Sci Technol 26:2281–7.

    CAS  Google Scholar 

  • Greenfield BK, Hrabik TR, Harvey CJ, Carpenter SR. 2001. Predicting mercury levels in yellow perch: use of water chemistry, trophic ecology, and spatial traits. Can J Fish Aquat Sci 58:1419–29.

    CAS  Google Scholar 

  • Grieb TM, Driscoll CT, Gloss SP, Schofield CL, Bowie GL, Porcella DB. 1990. Factors affecting mercury accumulation in fish in the upper Michigan peninsula, USA. Environ Toxicol Chem 9:919–30.

    CAS  Google Scholar 

  • Håkanson L, Nilsson A, Andersson T. 1988. Mercury in fish in Swedish lakes. Environ Pollut 49:145–62.

    PubMed  Google Scholar 

  • Hall BD, Bodaly RA, Fudge RJP, Rudd JWM, Rosenberg DM. 1997. Food as the dominant pathway of methylmercury uptake by fish. Water Air Soil Pollut 100:13–24.

    CAS  Google Scholar 

  • Hammerschmidt CR, Fitzgerald WF. 2006. Methylmercury in freshwater fish linked to atmospheric mercury deposition. Environ Sci Technol 40:7764–70.

    CAS  Google Scholar 

  • Harris RC, Rudd JWM, Amyot M, Babiarz CL, Beaty KG, Blanchfield PJ, Bodaly RA, Branfireun BA, Gilmour CC, Graydon JA, Heyes A, Hintelmann H, Hurley JP, Kelly CA, Krabbenhoft DP, Lindberg SE, Mason RP, Paterson MJ, Podemski CL, Robinson A, Sandilands KA, Southworth GR, St Louis VL, Tate MT. 2007. Whole-ecosystem study shows rapid fish-mercury response to changes in mercury deposition. Proc Natl Acad Sci USA 104:16586–91.

    CAS  PubMed  Google Scholar 

  • Hecky RE, Hesslein RH. 1995. Contributions of benthic algae to lake food webs as revealed by stable isotope analysis. J N Am Benthol Soc 14:631–53.

    Google Scholar 

  • Hillebrand H. 2004. On the generality of the latitudinal diversity gradient. Am Nat 163:192–211.

    PubMed  Google Scholar 

  • Hintelmann H. 2010. Organomercurials. Their formation and pathways in the environment. In: Sigel A, Sigel H, Sigel RKO, Eds. Organometallics in environment and toxicology. Cambridge: Royal Soc Chemistry. p 365–401.

    Google Scholar 

  • Holmer M, Storkholm P. 2001. Sulphate reduction and sulphur cycling in lake sediments: a review. Freshw Biol 46:431–51.

    CAS  Google Scholar 

  • Huckabee JW, Elwood JW, Hildebrand SG. 1979. Accumulation of mercury in freshwater biota. Nriagu JO editor. The biogeochemistry of mercury in the environment. Amsterdam: Elsevier/North-Holland Biomedical Press, pp 277–302.

  • Intergovernmental Panel on Climate Change. 2013. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM editors. Cambridge, UK, and New York, NY, USA.

  • Jardine TD, McGeachy SA, Paton CM, Savoie M, Cunjak RA. 2003. Stable isotopes in aquatic systems: Sample preparation, analysis, and interpretation. Canadian Manuscript Report of Fisheries and Aquatic Sciences, pv + 39.

  • Jeffries DS, Brydges TG, Dillon PJ, Keller W. 2003. Monitoring the results of Canada/USA acid rain control programs: some lake responses. Environ Monit Assess 88:3–19.

    CAS  PubMed  Google Scholar 

  • Jeppesen E, Meerhoff M, Holmgren K, González-Bergonzoni I, Teixeira-de Mello F, Declerck SAJ, De Meester L, Søndergaard M, Lauridsen TL, Bjerring R, Conde-Porcuna JM, Mazzeo N, Iglesias C, Reizenstein M, Malmquist HJ, Liu Z, Balayla D, Lazzaro X. 2010. Impacts of climate warming on lake fish community structure and potential effects on ecosystem function. Hydrobiologia 646:73–90.

    CAS  Google Scholar 

  • Johnson JB, Omland KS. 2004. Model selection in ecology and evolution. Trends Ecol Evol 19:101–8.

    PubMed  Google Scholar 

  • Johnston TA, Bodaly RA, Mathias JA. 1991. Predicting fish mercury levels from physical characteristics of boreal reservoirs. Can J Fish Aquat Sci 48:1468–75.

    CAS  Google Scholar 

  • Johnston TA, Ehrman AD, Hamilton GL, Nugent BK, Cott PA, Gunn JM. 2019. Plenty of room at the bottom: niche variation and segregation in large-bodied benthivores of boreal lakes. Can J Fish Aquat Sci 76:1411–22.

    Google Scholar 

  • 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 565:211–21.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Karimi R, Chen CY, Pickhardt PC, Fisher NS, Folt CL. 2007. Stoichiometric controls of mercury dilution by growth. Proc Natl Acad Sci 104:7477–82.

    CAS  PubMed  Google Scholar 

  • Kaufman SD, Johnston TA, Leggett WC, Moles MD, Casselman JM, Schulte-Hostedde AI. 2007. Relationships between body condition indices and proximate composition in adult walleyes. Trans Am Fish Soc 136:1566–76.

    Google Scholar 

  • Keller W. 2007. Implications of climate warming for Boreal Shield lakes: a review and synthesis. Environ Rev 15:99–112.

    CAS  Google Scholar 

  • 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 80:1011–15.

    CAS  Google Scholar 

  • Koinig KA, Schmidt R, Sommaruga-Wögrath S, Tessadri R, Psenner R. 1998. Climate change as the primary cause for pH shifts in a high alpine lake. Water Air Soil Pollut 104:167–80.

    CAS  Google Scholar 

  • Kolka RK, Grigal DF, Verry ES, Nater EA. 1999. Mercury and organic carbon relationships in streams draining forested upland/peatland watersheds. J Environ Qual 28:766–75.

    CAS  Google Scholar 

  • Kopáček J, Kaňa J, Bičárová S, Fernandez IJ, Hejzlar J, Kahounová M, Norton SA, Stuchlík E. 2017. Climate change increasing calcium and magnesium leaching from granitic alpine catchments. Environ Sci Technol 51:159–66.

    PubMed  Google Scholar 

  • Lavoie RA, Jardine TD, Chumchal MM, Kidd KA, Campbell LM. 2013. Biomagnification of mercury in aquatic food webs: a worldwide meta-analysis. Environ Sci Technol 47:13385–94.

    CAS  PubMed  Google Scholar 

  • Lehnherr I. 2014. Methylmercury biogeochemistry: a review with special reference to Arctic aquatic ecosystems. Environ Rev 22:229–43.

    CAS  Google Scholar 

  • Lemes M, Wang F. 2009. Methylmercury speciation in fish muscle by HPLC-ICP-MS following enzymatic hydrolysis. J Anal At Spectrom 24:663–8.

    CAS  Google Scholar 

  • Lescord GL, Emilson EJS, Johnston TA, Branfireun BA, Gunn JM. 2018a. Optical properties of dissolved organic matter and their relation to mercury concentrations in water and biota across a remote freshwater drainage basin. Environ Sci Technol 52:3344–53.

    CAS  PubMed  Google Scholar 

  • Lescord GL, Johnston TA, Branfireun BA, Gunn JM. 2018b. Percentage of methylmercury in the muscle tissue of freshwater fish varies with body size and age and among species. Environ Toxicol Chem 37:2682–91.

    CAS  PubMed  Google Scholar 

  • Lucotte M, Paquet S, Moingt M. 2016. Climate and physiography predict mercury concentrations in game fish species in Quebec lakes better than anthropogenic disturbances. Arch Environ Contam Toxicol 70:710–23.

    CAS  PubMed  Google Scholar 

  • Lumley T. 2009. Leaps: regression subset selection. R Package Version 2.9.: Available at: http://CRAN.R-project.org/package=leaps.

  • Magnuson JJ, Webster KE, Assel RA, Bowser CJ, Dillon PJ, Eaton JG, Evans HE, Fee EJ, Hall RI, Mortsch LR, Schindler DW, Quinn FH. 1997. Potential effects of climate changes on aquatic systems: laurentian Great Lakes and Precambrian Shield region. Hydrol Process 11:825–71.

    Google Scholar 

  • Mannio J, Verta M, Kortelainen P, Rekolainen S. 1986. The effect of water quality on the mercury concentration of northern pike (Esox lucius, L.) in Finnish forest lakes and reservoirs. Vesientutkimuslaitoksen Julkaisuja 65:32–43.

    CAS  Google Scholar 

  • Mattieu CA, Furl CV, Roberts TM, Friese M. 2013. Spatial trends and factors affecting mercury bioaccumulation in freshwater fishes of Washington State, USA. Arch Environ Contam Toxicol 65:122–31.

    PubMed  Google Scholar 

  • Mazerolle M. 2006. Improving data analysis in herpetology: using Akaike’s Information Criterion (AIC) to assess the strength of biological hypotheses. Amphibia-Reptilia 27:169–80.

    Google Scholar 

  • Mazerolle MJ. 2015. AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package version 2.03. http://CRAN.R-project.org/package=AICcmodavg.

  • McKenney DW, Hutchinson MF, Papadopol P, Lawrence K, Pedlar J, Campbell K, Milewska E, Hopkinson RF, Price D, Owen T. 2011. Customized spatial climate models for North America. Bull Am Meteor Soc 92:1611–22.

    Google Scholar 

  • McKenney DW, Pedlar JH, Papadopol P, Hutchinson MF. 2006. The development of 1901-2000 historical monthly climate models for Canada and the United States. Agric For Meteorol 138:69–81.

    Google Scholar 

  • McMurtry MJ, Wales DL, Scheider WA, Beggs GL, Dimond PE. 1989. Relationship of mercury concentrations in lake trout (Salvelinus namaycush) and smallmouth bass (Micropterus dolomieui) to the physical and chemical characteristics of Ontario lakes. Can J Fish Aquat Sci 46:426–34.

    CAS  Google Scholar 

  • Megaritis AG, Murphy BN, Racherla PN, Adams PJ, Pandis SN. 2014. Impact of climate change on mercury concentrations and deposition in the eastern United States. Sci Total Environ 487:299–312.

    CAS  PubMed  Google Scholar 

  • 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 36:3–11.

    CAS  PubMed  Google Scholar 

  • Mierle G, Ingram R. 1991. The role of humic substances in the mobilization of mercury from watersheds. Water Air Soil Pollut 56:349–57.

    CAS  Google Scholar 

  • Mills RB, Paterson AM, Lean DRS, Smol JP, Mierle G, Blais JM. 2009. Dissecting the spatial scales of mercury accumulation in Ontario lake sediment. Environ Pollut 157:2949–56.

    PubMed  Google Scholar 

  • Miskimmin BM, Rudd JWM, 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 49:17–22.

    CAS  Google Scholar 

  • Morel FMM, Kraepiel AML, Amyot M. 1998. The chemical cycle and bioaccumulation of mercury. Annu Rev Ecol Syst 29:543–66.

    Google Scholar 

  • Muir DCG, Wang X, Yang F, Nguyen N, Jackson TA, Evans MS, Douglas M, Köck G, Lamoureux S, Pienitz R, Smol JP, Vincent WF, Dastoor A. 2009. Spatial trends and historical deposition of mercury in eastern and northern Canada inferred from lake sediment cores. Environ Sci Technol 43:4802–9.

    CAS  PubMed  Google Scholar 

  • Munthe J, Bodaly RA, Branfireun BA, Driscoll CT, Gilmour CC, Harris R, Horvat M, Lucotte M, Malm O. 2007. Recovery of mercury-contaminated fisheries. Ambio 36:33–44.

    CAS  PubMed  Google Scholar 

  • Nürnberg GK. 1996. Trophic state of clear and colored, soft- and hardwater lakes with special consideration of nutrients, anoxia, phytoplankton and fish. Lake Reserv Manag 12:432–47.

    Google Scholar 

  • Nürnberg GK. 2004. Quantified hypoxia and anoxia in lakes and reservoirs. Sci World J 4:42–54.

    Google Scholar 

  • Obrist D, Agnan Y, Jiskra M, Olson CL, Colegrove DP, Hueber J, Moore CW, Sonke JE, Helmig D. 2017. Tundra uptake of atmospheric elemental mercury drives Arctic mercury pollution. Nature 547:201.

    CAS  PubMed  Google Scholar 

  • Ontario Ministry of Natural Resources and Forestry. 2015. User Guide for Ontario Flow Assessment Tool (OFAT). Toronto, ON, Canada: Ontario Ministry of Natural Resources and Forestry, Mapping and Information Resources Branch, p 79.

  • Pacyna JM, Travnikov O, de Simone F, Hedgecock IM, Sundseth K, Pacyna EG, Steenhuisen F, Pirrone N, Munthe J, Kindbom K. 2016. Current and future levels of mercury atmospheric pollution on a global scale. Atmos Chem Phys 16:12495–511.

    CAS  Google Scholar 

  • Paranjape AR, Hall BD. 2017. Recent advances in the study of mercury methylation in aquatic systems. FACETS 2:85–119.

    Google Scholar 

  • Perron T, Chetelat J, Gunn J, Beisner BE, Amyot M. 2014. Effects of experimental thermocline and oxycline deepening on methylmercury bioaccumulation in a Canadian Shield lake. Environ Sci Technol 48:2626–34.

    CAS  PubMed  Google Scholar 

  • Peterson BJ, Fry B. 1987. Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320.

    Google Scholar 

  • Pickett STA. 1989. Space-for-time substitution as an alternative to long-term studies. Likens GE editor. Long-term studies in ecology: approaches and alternatives. New York: Springer, pp 110–35.

  • 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 99:4419–23.

    CAS  PubMed  Google Scholar 

  • Power M, Klein GM, Guiguer KRRA, 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 39:819–30.

    CAS  Google Scholar 

  • Price DT, Alfaro RI, Brown KJ, Flannigan MD, Fleming RA, Hogg EH, Girardin MP, Lakusta T, Johnston M, McKenney DW, Pedlar JH, Stratton T, Sturrock RN, Thompson ID, Trofymow JA, Venier LA. 2013. Anticipating the consequences of climate change for Canada’s boreal forest ecosystems. Environ Rev 21:322–65.

    Google Scholar 

  • R Core Team. 2017. R: a language and environment for statistical computing, version 3.4.0. Vienna, Austria: R Foundation for Statistical Computing.

  • Ramlal PS, Kelly CA, Rudd JWM, Furutani A. 1993. Sites of methyl mercury production in remote Canadian shield lakes. Can J Fish Aquat Sci 50:972–9.

    CAS  Google Scholar 

  • Rasmussen PE, Villard DJ, Gardner HD, Fortescue JAC, Schiff SL, Shilts WW. 1998. Mercury in lake sediments of the Precambrian Shield near Huntsville, Ontario, Canada. Environ Geol 33:170–82.

    CAS  Google Scholar 

  • Rasmussen PW, Schrank CS, Campfield PA. 2007. Temporal trends of mercury concentrations in Wisconsin walleye (Sander vitreus), 1982–2005. Ecotoxicology 16:541–50.

    CAS  PubMed  Google Scholar 

  • Ravichandran M. 2004. Interactions between mercury and dissolved organic matter—a review. Chemosphere 55:319–31.

    CAS  PubMed  Google Scholar 

  • Rypel AL. 2010. Mercury concentrations in lentic fish populations related to ecosystem and watershed characteristics. Ambio 39:14–19.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sandheinrich MB, Drevnick PE. 2016. Relationship among mercury concentration, growth rate, and condition of northern pike: a tautology resolved? Environ Toxicol Chem 35:2910–15.

    CAS  PubMed  Google Scholar 

  • Sandstrom S, Rawson M, Lester N. 2013. Manual of Instructions for Broad-scale Fish Community Monitoring; using North American Gillnets (NA1) and Ontario Small Mesh Gillnets (ON2). Version 2013.2. Peterborough, Ontario: Ontario Ministry of Natural Resources, p 35.

  • Schindler DW. 1998. A dim future for boreal waters and landscapes. Bioscience 48:157–64.

    Google Scholar 

  • Selin NE. 2009. Global biogeochemical cycling of mercury: a review. Annu Rev Environ Resour 34:43–63.

    Google Scholar 

  • 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 42:5193–204.

    CAS  Google Scholar 

  • Selvendiran P, Driscoll CT, Bushey JT, Montesdeoca MR. 2008. Wetland influence on mercury fate and transport in a temperate forested watershed. Environ Pollut 154:46–55.

    CAS  PubMed  Google Scholar 

  • Serreze MC, Walsh JE, Chapin FS, Osterkamp T, Dyurgerov M, Romanovsky V, Oechel WC, Morison J, Zhang T, Barry RG. 2000. Observational evidence of recent change in the northern high-latitude environment. Clim Change 46:159–207.

    Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Snucins E, Gunn J. 2000. Interannual variation in the thermal structure of clear and colored lakes. Limnol Oceanogr 45:1639–46.

    Google Scholar 

  • Sonesten L. 2003. Catchment area composition and water chemistry heavily affects mercury levels in perch (Perca fluviatilis L.) in circumneutral lakes. Water Air Soil Pollut 144:117–39.

    CAS  Google Scholar 

  • Sorensen JA, Glass GE, Schmidt KW, Huber JK, Rapp GRJ. 1990. Airborne mercury deposition and watershed characteristics in relation to mercury concentrations in water sediments plankton and fish of eighty northern Minnesota lakes, USA. Environ Sci Technol 24:1716–27.

    CAS  Google Scholar 

  • St Louis VL, Rudd JWM, Kelly CA, Barrie LA. 1995. Wet deposition of methyl mercury in northwestern Ontario compared to other geographic locations. Water Air Soil Pollut 80:405–14.

    CAS  Google Scholar 

  • 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 51:1065–76.

    CAS  Google Scholar 

  • St. Louis VL, Graydon JA, Lehnherr I, Amos HM, Sunderland EM, St. Pierre KA, Emmerton CA, Sandilands K, Tate M, Steffen A, Humphreys ER. 2019. Atmospheric concentrations and wet/dry loadings of mercury at the remote Experimental Lakes Area, northwestern Ontario, Canada. Environ Sci Technol 53:8017–26.

    CAS  PubMed  Google Scholar 

  • Stasko AD, Gunn JM, Johnston TA. 2012. Role of ambient light in structuring north-temperate fish communities: potential effects of increasing dissolved organic carbon concentration with a changing climate. Environ Rev 20:173–90.

    CAS  Google Scholar 

  • Symonds MRE, Moussalli A. 2011. A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21.

    Google Scholar 

  • Tang RWK, Johnston TA, Gunn JM, Bhavsar SP. 2013. Temporal changes in mercury concentrations of large-bodied fishes in the boreal shield ecoregion of northern Ontario, Canada. Sci Total Environ 444:409–16.

    CAS  PubMed  Google Scholar 

  • Ullrich SM, Tanton TW, Abdrashitova SA. 2001. Mercury in the aquatic environment: a review of factors affecting methylation. Critical Reviews in Environmental Science and Technology 31:241–93.

    CAS  Google Scholar 

  • Verta M, Salo S, Korhonen M, Porvari P, Paloheimo A, Munthe J. 2010. Climate induced thermocline change has an effect on the methyl mercury cycle in small boreal lakes. Sci Total Environ 408:3639–47.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Watras CJ, Grande D, Latzka AW, Tate LS. 2018. Mercury trends and cycling in northern Wisconsin related to atmospheric and hydrologic processes. Can J Fish Aquat Sci 76:831–46.

    Google Scholar 

  • Weise L, Ulrich A, Moreano M, Gessler A, E. Kayler Z, Steger K, Zeller B, Rudolph K, Knezevic-Jaric J, Premke K. 2016. Water level changes affect carbon turnover and microbial community composition in lake sediments. FEMS Microbiology Ecology 92: fiw035.

  • Weyhenmeyer GA, Müller RA, Norman M, Tranvik LJ. 2016. Sensitivity of freshwaters to browning in response to future climate change. Clim Change 134:225–39.

    Google Scholar 

  • Wiener JG, Knights BC, Sandheinrich MB, Jeremiason JD, Brigham ME, Engstrom DR, Woodruff LG, Cannon WF, Balogh SJ. 2006. Mercury in soils, lakes, and fish in Voyageurs National Park (Minnesota): importance of atmospheric deposition and ecosystem factors. Environ Sci Technol 40:6261–8.

    CAS  PubMed  Google Scholar 

  • Wiener JG, Martini RE, Sheffy TB, Glass GE. 1990. Factors influencing mercury concentrations in walleyes in northern Wisconsin lakes. Trans Am Fish Soc 119:862–70.

    CAS  Google Scholar 

  • Woodward G, Perkins DM, Brown LE. 2010. Climate change and freshwater ecosystems: impacts across multiple levels of organization. Philos Trans R Soc B Biol Sci 365:2093–106.

    Google Scholar 

  • Wren CD, Scheider WA, Wales DL, Muncaster BW, Gray IM. 1991. Relation between mercury concentrations in walleye (Stizostedion vitreum vitreum) and northern pike (Esox lucius) in Ontario lakes and influence of environmental factors. Can J Fish Aquat Sci 48:132–9.

    CAS  Google Scholar 

  • Wright DR, Hamilton RD. 1982. Release of methyl mercury from sediments: effects of mercury concentration, low temperature, and nutrient addition. Can J Fish Aquat Sci 39:1459–66.

    CAS  Google Scholar 

  • Zhang Y, Jacob DJ, Horowitz HM, Chen L, Amos HM, Krabbenhoft DP, Slemr F, St. Louis VL, Sunderland EM. 2016. Observed decrease in atmospheric mercury explained by global decline in anthropogenic emissions. Proc Natl Acad Sci 113:526–31.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Kelsey Bender, Graham Burrows, Jennifer Cole, Andrew Corston, Michelle Gillespie, Lee Haslam, and Ashley Stasko for field and laboratory support, and Jocelyne Heneberry and Emily Smenderovac for assistance with data analysis. Water chemistry analyses and data were provided by the Ontario Ministry of Environment and Climate Change. We are grateful to the staff of the Biotron Centre for Climate Change Research at Western University for analytical and training support for Hg analyses. Funding and in-kind support for this research were generously provided by the Ontario Ministry of Natural Resources and Forestry, the Natural Sciences and Engineering Research Council (NSERC) Strategic Networks Program and Discovery Grants Program, the Wildlife Conservation Society, the W. Garfield Weston Foundation, the Northern Scientific Training Program (NSTP), and the Fisheries and Oceans Canada Habitat and Restoration Scholarship. Constructive criticisms on earlier drafts of this work were provided by Nelson Belzile, Rob Mackereth, Stephanie Melles, Heidi Swanson, and four anonymous reviewers.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T. A. Johnston.

Additional information

Author’s Contributions

AWS, TAJ, and JMG designed study; AWS, TAJ, and GLL performed research and analysed data; AWS, TAJ, GLL, BAB, and JMG wrote the paper.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 26 kb)

Supplementary material 2 (DOCX 62 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sumner, A.W., Johnston, T.A., Lescord, G.L. et al. Mercury Bioaccumulation in Lacustrine Fish Populations Along a Climatic Gradient in Northern Ontario, Canada. Ecosystems 23, 1206–1226 (2020). https://doi.org/10.1007/s10021-019-00464-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-019-00464-9

Keywords

Navigation