Skip to main content
Log in

Speciation leads to divergent methylmercury accumulation in sympatric whitefish

  • Research Article
  • Published:
Aquatic Sciences Aims and scope Submit manuscript

Abstract

Central European lake whitefish (Coregonus spp.) colonized Swiss lakes following the last glacial retreat and have undergone rapid speciation and adaptive radiation. Up to six species have been shown to coexist in some lakes, and individual species occupy specific ecological niches and have distinct feeding and reproductive ecologies. We studied methylmercury (MeHg) accumulation in sympatric whitefish species from seven Swiss lakes to determine if ecological divergence has led to different rates of MeHg bioaccumulation. In four of seven lakes, sympatric species had distinctly different MeHg levels, which varied by up to a factor of two between species. Generally, species with greater MeHg levels were smaller in body size and planktivorous, and species with lower MeHg were larger and benthivorous. While modest disparities in trophic position between species might be expected a priori to explain the divergence in MeHg, δ15N of bulk tissue did not correlate with fish MeHg in five of seven lakes. Results of a nested ANCOVA analysis across all lakes indicated that only two factors (species, lake) explained substantial portions of the variance, with species accounting for more variance (52 %) than inter-lake differences (32 %). We suggest that differences in MeHg accumulation were likely caused by diverging metabolic traits between species, such as differences in energy partitioning between anabolism and catabolism, potentially interacting with species-specific prey resource utilization. These results indicate substantial variability in MeHg accumulation between closely related fish species, illustrating that ecological speciation in fish can lead to divergent MeHg accumulation patterns.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • BAFU (2008) Jahreserträge der Angelfischerei in Seen. BAFU Jagd und Fischerei. http://www.bafu.admin.ch/jagd-fischerei/07831/07867/07871. Accessed 3 April 2011

  • BAFU (2009) Jahresertrag Berufsfischerei. BAFU Jagd und Fischerei. http://www.bafu.admin.ch/jagd-fischerei/07831/07867/07869. Accessed 3 April 2011

  • Bank MS, Chesney E, Shine JP, Maage A, Senn DB (2007) Mercury bioaccumulation and trophic transfer in sympatric snapper species from the Gulf of Mexico. Ecol Appl 17:2100–2110

    Article  PubMed  Google Scholar 

  • Barluenga M, Stolting KN, Salzburger W, Muschick M, Meyer A (2006) Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 439(7077):719–723. doi:10.1038/nature04325

    Article  PubMed  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. In: Braids OC, Cai Y (eds) Biogeochemistry of environmentally important trace metals. American Chemical Society, Washington, DC, pp 262–297

    Google Scholar 

  • Bernatchez L (2004) Ecological theory of adaptive radiation—an empirical assessment from coregonine fishes (Salmoniformes). In: Hendry AP, Stearns SC (eds) Evolution illuminated: Salmon and their relatives. Oxford University Press, New York, pp 175–207

  • Bernatchez L, Chouinard A, Lu GQ (1999) Integrating molecular genetics and ecology in studies of adaptive radiation: whitefish, Coregonus sp., as a case study. Biol J Linn Soc 68(1–2):173–194. doi:10.1006/bijl.1999.0337

    Article  Google Scholar 

  • Bloom NS (1989) Determination of picogram levels of methylmercury by aqueous phase ethylation, followed by cryogenic gas-chromatography with cold vapor atomic fluorescence detection. Can J Fish Aquat Sci 46(7):1131–1140. doi:10.1139/f89-147

    Article  CAS  Google Scholar 

  • Bloom NS (1992) On the chemical form of mercury in edible fish and marine invertebrate tissue. Can J Fish Aquat Sci 49(5):1010–1017

    Article  CAS  Google Scholar 

  • BUWAL (1994) Der Zustand der Seen in der Schweiz. Schriftenreihe Umwelt Nr. 237, Gewässerschutz

  • Cabana G, Rasmussen JB (1994) Modeling food-chain structure and contaminant bioaccumulation using stable nitrogen isotopes. Nature 372(6503):255–257

    Article  CAS  Google Scholar 

  • Cabana G, Rasmussen JB (1996) Comparison of aquatic food chains using nitrogen isotopes. Proc Nat Acad Sci USA 93(20):10844–10847

    Article  PubMed  CAS  Google Scholar 

  • Chandra S, Vander Zanden MJ, Heyvaert AC, Richards BC, Allen BC, Goldman CR (2005) The effects of cultural eutrophication on the coupling between pelagic primary producers and benthic consumers. Limnol Oceanogr 50(5):1368–1376

    Article  CAS  Google Scholar 

  • Douglas MR, Brunner PC (2002) Biodiversity of Central Alpine Coregonus (Salmoniformes): impact of one-hundred years of management. Ecol Appl 12(1):154–172

    Article  Google Scholar 

  • Douglas MR, Brunner PC, Bernatchez L (1999) Do assemblages of Coregonus (Teleostei: Salmoniformes) in the Central Alpine region of Europe represent species flocks? Mol Ecol 8(4):589–603

    Article  Google Scholar 

  • Doyon JF, Schetagne R, Verdon R (1998) Different mercury bioaccumulation rates between sympatric populations of dwarf and normal lake whitefish (Coregonus clupeaformis) in the La Grande complex watershed, James Bay, Quebec. Biogeochemistry 40(2–3):203–216. doi:10.1023/a:1005951009950

    Article  CAS  Google Scholar 

  • Eagles-Smith CA, Suchanek TH, Colwell AE, Anderson NL (2008) Mercury trophic transfer in a eutrophic lake: the importance of habitat-specific foraging. Ecol Appl 18(8):A196–A212

    Article  PubMed  Google Scholar 

  • Fenderson OC (1964) Evidence of subpopulations of lake whitefish, Coregonus clupeaformis, involving a dwarfed form. Trans Am Fish Soc 93(1):77–94

    Article  Google Scholar 

  • Fitzgerald WF, Gill GA (1979) Sub-nanogram determination of mercury by 2-stage gold amalgamation and gas-phase detection applied to atmospheric analysis. Anal Chem 51(11):1714–1720

    Article  CAS  Google Scholar 

  • Gachter R (1987) Lake restoration—Why oxygenation and artificial mixing cannot substitute for a decrease in the external phosphorus loading. Swiss J Hydrol (Schweizerische Zeitschrift Fur Hydrologie) 49(2):170–185

    Article  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(7):1419–1429

    Article  CAS  Google Scholar 

  • Grimaldi E (1972) Lago Maggiore—effects of exploitation and introductions on salmonid community. J Fish Res Board Can 29(6):777–785

    Article  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(1–2):13–24

    CAS  Google Scholar 

  • Hammerschmidt CR, Fitzgerald WF (2006a) Bioaccumulation and trophic transfer of methylmercury in Long Island Sound. Arch Environ Contam Toxicol 51(3):416–424. doi:10.1007/s00244-005-0265-7

    Article  PubMed  CAS  Google Scholar 

  • Hammerschmidt CR, Fitzgerald WF (2006b) Methylmercury in freshwater fish linked to atmospheric mercury deposition. Environ Sci Technol 40(24):7764–7770. doi:10.1021/es061480i

    Article  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, Louis VLS, Tate MT (2007) Whole-ecosystem study shows rapid fish-mercury response to changes in mercury deposition. Proc Nat Acad Sci USA 104(42):16586–16591. doi:10.1073/pnas.0704186104

    Article  PubMed  CAS  Google Scholar 

  • Harrod C, Mallela J, Kahilainen KK (2010) Phenotype-environment correlations in a putative whitefish adaptive radiation. J Anim Ecol 79(5):1057–1068. doi:10.1111/j.1365-2656.2010.01702.x

    Article  PubMed  Google Scholar 

  • Herder F, Pfaender J, Schliewen UK (2008) Adaptive sympatric speciation of polychromatic “roundfin” sailfin silverside fish in Lake Matano (Sulawesi). Evolution 62(9):2178–2195. doi:10.1111/j.1558-5646.2008.00447.x

    Article  PubMed  Google Scholar 

  • Hudson AG, Vonlanthen P, Mueller R, Seehausen O (2007) Review: the geography of speciation and adaptive radiation in Coregonines. Adv Limnol 60:111–146

    Google Scholar 

  • Hudson AG, Vonlanthen P, Seehausen O (2011) Rapid parallel adaptive radiations from a single hybridogenic ancestral population. Proc R Soc B Biol Sci 278(1702):58–66. doi:10.1098/rspb.2010.0925

    Article  Google Scholar 

  • Kahilainen KK, Malinen T, Tuomaala A, Alajaervi E, Tolonen A, Lehtonen H (2007) Empirical evaluation of phenotype-environment correlation and trait utility with allopatric and sympatric whitefish, Coregonus lavaretus (L.), populations in subarctic lakes. Biol J Linn Soc 92(3):561–572. doi:10.1111/j.1095-8312.2007.00856.x

    Article  Google Scholar 

  • Kahilainen KK, Siwertsson A, Gjelland KO, Knudsen R, Bohn T, Amundsen PA (2011) The role of gill raker number variability in adaptive radiation of coregonid fish. Evol Ecol 25(3):573–588. doi:10.1007/s10682-010-9411-4

    Article  Google Scholar 

  • Kehrig HA, Palermo EFA, Seixas TG, Branco CWC, Moreira I, Malm O (2009) Trophic transfer of methylmercury and trace elements by tropical estuarine seston and plankton. Estuar Coast Shelf Sci 85(1):36–44. doi:10.1016/j.ecss.2009.05.027

    Article  CAS  Google Scholar 

  • Kidd KA, Hesslein RH, Fudge RJP, Hallard KA (1995) The influence of trophic level as measured by delta-N-15 on mercury concentrations in fresh-water organisms. Water Air Soil Pollut 80(1–4):1011–1015

    Article  CAS  Google Scholar 

  • Kidd KA, Bootsma HA, Hesslein RH, Muir DCG, Hecky RE (2001) Biomagnification of DDT through the benthic and pelagic food webs of Lake Malawi, East Africa: importance of trophic level and carbon source. Environ Sci Technol 35(1):14–20

    Article  PubMed  CAS  Google Scholar 

  • Kidd KA, Bootsma HA, Hesslein RH, Lockhart WL, Hecky RE (2003) Mercury concentrations in the food web of Lake Malawi, East Africa. J Great Lakes Res 29:258–266

    Article  CAS  Google Scholar 

  • Kiljunen M, Grey J, Sinisalo T, Harrod C, Immonen H, Jones RI (2006) A revised model for lipid-normalizing delta C-13 values from aquatic organisms, with implications for isotope mixing models. J Appl Ecol 43(6):1213–1222. doi:10.1111/j.1365-2664.2006.01224.x

    Article  CAS  Google Scholar 

  • Lamborg CH, Fitzgerald WF, Damman AWH, Benoit JM, Balcom PH, Engstrom DR (2002) Modern and historic atmospheric mercury fluxes in both hemispheres: global and regional mercury cycling implications. Glob Biogeochem Cycles 16(4):1104. doi:10.1029/2001GB001847

    Google Scholar 

  • Matthews B, Mazumder A (2003) Compositional and interlake variability of zooplankton affect baseline stable isotope signatures. Limnol Oceanogr 48(5):1977–1987

    Article  CAS  Google Scholar 

  • Matthews B, Marchinko KB, Bolnick DI, Mazumder A (2010) Specialization of trophic position and habitat use by sticklebacks in an adaptive radiation. Ecology 91(4):1025–1034

    Article  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(1):3–11

    Article  PubMed  CAS  Google Scholar 

  • Mueller R, Stadelmann P (2004) Fish habitat requirements as the basis for rehabilitation of eutrophic lakes by oxygenation. Fish Manage Ecol 11(3–4):251–260

    Article  Google Scholar 

  • Muir AM, Sutton TM, Arts MT, Claramunt RM, Ebener MP, Fitzsimons JD, Johnson TB, Kinnunen RE, Koops MA, Sepulveda MM (2010) Does condition of Lake Whitefish spawners affect physiological condition of juveniles? J Great Lakes Res 36:92–99. doi:10.1016/j.jglr.2009.07.006

    Article  Google Scholar 

  • Ohlberger J, Mehner T, Staaks G, Holker F (2008) Temperature-related physiological adaptations promote ecological divergence in a sympatric species pair of temperate freshwater fish, Coregonus spp. Funct Ecol 22(3):501–508. doi:10.1111/j.1365-2435.2008.01391.x

    Article  Google Scholar 

  • Parkman H, Meili M (1993) Mercury in macroinvertebrates from Swedish forest lakes - influence of lake type, habitat, life-cycle, and food quality. Can J Fish Aquat Sci 50(3):521–534

    Article  CAS  Google Scholar 

  • Pickhardt PC, Folt CL, Chen CY, Klaue B, Blum JD (2002) Algal blooms reduce the uptake of toxic methylmercury in freshwater food webs. Proc Nat Acad Sci USA 99(7):4419–4423. doi:10.1073/pnas.072531099

    Article  PubMed  CAS  Google Scholar 

  • Popp BN, Graham BS, Olson RJ, Hannides CCS, Lott MJ, López-Ibarra GA, Galván-Magaña F, Fry B (2007) Insight into the trophic ecology of Yellowfin Tuna, Thunnus albacares, from compound-specific nitrogen isotope analysis of proteinaceous amino acids. Stable isotopes as indicators of ecological change: terrestrial ecology. Elsevier/Academic press, Amsterdam

    Google Scholar 

  • Post DM (2002) Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology 83(3):707–718

    Article  Google Scholar 

  • Rufli H (1978) Present sympatric whitefish populations of Lake Thun and Lake Biel and their morphology. Swiss J Hydrol (Schweizerische Zeitschrift Fur Hydrologie) 40(1):7–31

    Google Scholar 

  • Sanderson SL, Cheer AY, Goodrich JS, Graziano JD, Callan WT (2001) Crossflow filtration in suspension-feeding fishes. Nature 412(6845):439–441. doi:10.1038/35086574

    Article  PubMed  CAS  Google Scholar 

  • Schluter D (1996) Ecological speciation in postglacial fishes. Philos Trans R Soc Lond Ser B Biol Sci 351(1341):807–814

    Article  Google Scholar 

  • Seehausen O (2006) Conservation: losing biodiversity by reverse speciation. Curr Biol 16(9):R334–R337. doi:10.1016/j.cub.2006.03.080

    Article  PubMed  CAS  Google Scholar 

  • Seehausen O, Terai Y, Magalhaes IS, Carleton KL, Mrosso HDJ, Miyagi R, van der Sluijs I, Schneider MV, Maan ME, Tachida H, Imai H, Okada N (2008) Speciation through sensory drive in cichlid fish. Nature 455(7213):U620–U623. doi:10.1038/nature07285

    Article  Google Scholar 

  • Senn DB, Chesney EJ, Blum JD, Bank MS, Maage A, Shine JP (2010) Stable isotope (N, C, Hg) study of methylmercury sources and trophic transfer in the Northern Gulf of Mexico. Environ Sci Technol 44(5):1630–1637. doi:10.1021/es902361j

    Article  PubMed  CAS  Google Scholar 

  • St-Cyr J, Derome N, Bernatchez L (2008) The transcriptomics of life-history trade-offs in whitefish species pairs (Coregonus sp.). Mol Ecol 17(7):1850–1870. doi:10.1111/j.1365-294X.2008.03696.x

    Article  PubMed  CAS  Google Scholar 

  • Steinmann P (1950) Ein neues System der mitteleuropäischen Coregonen. Rev Suisse Zool 57(3):517–525

    Google Scholar 

  • Steinmann P (1951) Monographie der schweizerischen Koregonen. Beitrag zum Problem der Entstehung neuer Arten. Die insubrischen Seen. Swiss J Hydrol (Schweizerische Zeitschrift für Hydrologie) 12:109–189

    Google Scholar 

  • Swain EB, Engstrom DR, Brigham ME, Henning TA, Brezonik PL (1992) Increasing rates of atmospheric mercury deposition in midcontinental North America. Science 257(5071):784–787

    Article  PubMed  CAS  Google Scholar 

  • Swanson HK, Johnston TA, Schindler DW, Bodaly RA, Whittle DM (2006) Mercury bioaccumulation in forage fish communities invaded by rainbow smelt (Osmerus mordax). Environ Sci Technol 40:1439–1446

    Article  PubMed  CAS  Google Scholar 

  • Taylor EB, Boughman JW, Groenenboom M, Sniatynski M, Schluter D, Gow JL (2006) Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Mol Ecol 15(2):343–355. doi:10.1111/j.1365-294X.2005.02794.x

    Article  PubMed  CAS  Google Scholar 

  • Trudel M, Rasmussen JB (1997) Modeling the elimination of mercury by fish. Environ Sci Technol 31(6):1716–1722

    Article  CAS  Google Scholar 

  • Trudel M, Tremblay A, Schetagne R, Rasmussen JB (2001) Why are dwarf fish so small? An energetic analysis of polymorphism in lake whitefish (Coregonus clupeaformis). Can J Fish Aquat Sci 58(2):394–405

    Article  Google Scholar 

  • Tseng CM, Hammerschmidt CR, Fitzgerald WF (2004) Determination of methylmercury in environmental matrixes by on-line flow injection and atomic fluorescence spectrometry. Anal Chem 76(23):7131–7136. doi:10.1021/ac049118e

    Article  PubMed  CAS  Google Scholar 

  • Vadeboncoeur Y, Jeppesen E, Vander Zanden MJ, Schierup HH, Christofferson K, Lodge DM (2003) From Greenland to green lakes: cultural eutrophication and the loss of benthic pathways in lakes. Limnol Oceanogr 48(4):1408–1418

    Article  Google Scholar 

  • Vander Zanden MJ, Rasmussen JB (2001) Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnol Oceanogr 46(8):2061–2066

    Article  CAS  Google Scholar 

  • Vonlanthen P, Roy D, Hudson AG, Largiader CR, Bittner D, Seehausen O (2009) Divergence along a steep ecological gradient in lake whitefish (Coregonus sp.). J Evol Biol 22(3):498–514. doi:10.1111/j.1420-9101.2008.01670.x

    Article  PubMed  CAS  Google Scholar 

  • Vonlanthen P, Bittner D, Hudson AG, Young KA, Müller R, Lundsgaard-Hansen B, Roy D, Di Piazza S, Largiader CR, Seehausen O (2012) Eutrophication causes speciation reversal in whitefish adaptive radiations. Nature. doi:10.1038/nature10824

    PubMed  Google Scholar 

  • Ward DM, Nislow KH, Chen CY, Folt CL (2010) Rapid, efficient growth reduces mercury concentrations in Stream-dwelling Atlantic salmon. Trans Am Fish Soc 139(1):1–10. doi:10.1577/t09-032.1

    Article  PubMed  CAS  Google Scholar 

  • Wiener JG, Krabbenhoft DP, Heinz GH, Scheuhammer AM (2003) Ecotoxicology of mercury. Handbook of Ecotoxicology. Lewis Publishers, Boca Raton

    Google Scholar 

  • Wiener JG, Bodaly RA, Brown SS, Lucotte M, Newman MC, Porcella DB, Reash RJ, Swain EB (2006a) Monitoring and evaluating trends in methylmercury accumulation in aquatic biota. In: Harris RC, Krabbenhoft DP, Mason RP, Murray MW, Reash RJ, Saltman T (eds) Ecosystem responses to mercury contamination: indicators of change. CRC Press/Taylor and Francis, Boca Raton, Florida, pp 87–122

  • Wiener JG, Knights BC, Sandheinrich MB, Jeremiason JD, Brigham ME, Engstrom DR, Woodruff LG, Cannon WF, Balogh SJ (2006b) Mercury in soils, lakes, and fish in Voyageurs National Park (Minnesota): importance of atmospheric deposition and ecosystem factors. Environ Sci Technol 40:6261–6268

    Article  PubMed  CAS  Google Scholar 

  • Zennegg M, Kohler M, Gerecke AC, Schmid P (2003) Polybrominated diphenyl ethers in whitefish from Swiss lakes and farmed rainbow trout. Chemosphere 51(7):545–553. doi:10.1016/s0045-6535(03)00047-x

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors extend their appreciation to J. Wiederhold, K. Barmettler, and R. Kretzchmar (ETH-Zurich) for providing access to Hg analysis instrumentation, to M. Coray and S. Bishop for assistance with stable isotope measurements, and to A. Drewek for statistical assistance. Funding for this project came from the Swiss Federal Office for the Environment (BAFU).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David B. Senn.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 76 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Blank, N., Hudson, A.G., Vonlanthen, P. et al. Speciation leads to divergent methylmercury accumulation in sympatric whitefish. Aquat Sci 75, 261–273 (2013). https://doi.org/10.1007/s00027-012-0271-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00027-012-0271-6

Keywords

Navigation