Dense Mytilus Beds Along Freshwater-Influenced Greenland Shores: Resistance to Corrosive Waters Under High Food Supply

  • Carlos M. DuarteEmail author
  • Alejandro B. Rodriguez-Navarro
  • Antonio Delgado-Huertas
  • Dorte Krause-Jensen


Arctic calcifiers are believed to be particularly vulnerable to ocean acidification as the Arctic already experiences low carbonate saturations states due to low temperature and high inputs of freshwater. Here, we report the finding of dense beds of Mytilus growing in tidal lagoons and river mouths, where the availability of carbonate ions is remarkably low Ωarag < 0.5. Although these Mytilus grow in the intertidal zone, and therefore are covered by seawater during high tide, δ18O isotopes of shell carbonate were low − 2.48 ± 0.05‰, confirming that their shells were deposited under low salinity conditions, i.e., reflecting a contribution from 18O-depleted freshwater. δ18O isotopes of shell carbonate became heavier with increasing salinity, with mean values of − 0.74 ± 0.96‰ for Mytilus growing in tidal pools. We calculated, based on δ18O isotopic composition standardized to a common temperature, that freshwater accounted for 7% of the carbonate oxygen in the shells of Mytilus at the habitats with near full-strength seawater salinity compared with 25% in shells collected at sites temporarily exposed to freshwater. The composition of the periostracum revealed a trend for shells from river mouths and brackish tidal lagoons to be more depleted in polysaccharides than shells exposed to higher salinity. We conclude that the high food supply associated with riverine discharge allows Mytilus to cope with the low saturation states by using energy to calcify and modify their periostracum to protect the shells from dissolution. These findings suggest that Arctic Mytilus are highly resistant to low saturation states of carbon minerals if supplied with sufficient food.


Bivalve Shell Ocean acidification Carbonate 



We thank the staff of the Greenlandic Institute of Natural Resources GINR, Nuuk, Greenland for help with fieldwork in 2015 and Kjeld Akaaraq Emil Mølgaard and Frode Vest Hansen, Arctic Station, Disko Island, University of Copenhagen, Denmark for help with fieldwork in 2016. The study is also a contribution to the marine Greenland Ecosystem Monitoring program ( MarineBasis in Nuuk and Disko Bay.

Funding Information

This research was funded by a grant from The Carlsberg Foundation grant number CF15-0639.

Supplementary material

12237_2019_682_MOESM1_ESM.docx (17 kb)
ESM 1 (DOCX 17 kb)


  1. Arrigo, K.R., and G.L. van Dijken. 2015. Continued increases in Arctic Ocean primary production. Progress in Oceanography 136: 60–70. Scholar
  2. Bamber, J., M. den Broeke, J. Ettema, J. Lenaerts, and E. Rignot. 2012. Recent large increases in freshwater fluxes from Greenland into the North Atlantic. Geophysical Research Letters 39: 19. Scholar
  3. Bhatia, M.P., S.B. Das, L. Xu, M.A. Charette, J.L. Wadham, and E.B. Kujawinski. 2013. Organic carbon export from the Greenland ice sheet. Geochimica et Cosmochimica Acta 109: 329–344. Scholar
  4. Bechmann, R.K., J.C. Taban, S. Westerlund, B.F. Godal, M. Arnberg, S. Vingen, A. Ingvarsdottir, and T. Baussant. 2011. Effects of ocean acidification on early life stages of shrimp Pandalus borealis and mussel Mytilus edulis. Journal of Toxicology and Environmental Health, Part A 74 (7–9): 424–438. Scholar
  5. Bubel, A. 1973. An electron-microscope study of periostracum repair in Mytilus edulis. Marine Biology 20: 235–244.Google Scholar
  6. Dickson, A.G., and F.J. Millero. 1987. A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Research 34: 1733–1743.CrossRefGoogle Scholar
  7. Duarte, C.M., and D. Krause-Jensen. 2018. Greenland tidal pools as hot spots for community metabolism and calcification. Estuaries and Coasts 41 (5): 1314–1321. Scholar
  8. Duarte, C., J.M. Navarro, K. Acuña, R. Torres, P.H. Manríquez, M.A. Lardies, C.A. Vargas, N.A. Lagos, and V. Aguilera. 2015. Intraspecific variability in the response of the edible mussel Mytilus chilensis Hupe to ocean acidification. Estuaries and Coasts 382 (2): 590–598. Scholar
  9. Gazeau, F., J.-P. Gattuso, C. Dawber, A.E. Pronker, F. Peene, J. Peene, C.H.R. Heip, and J.J. Middelburg. 2010. Effect of ocean acidification on the early life stages of the blue mussel Mytilus edulis. Biogeosciences 77: 2051. Scholar
  10. Gray, M.W., C.J. Langdon, G.G. Waldbusser, B. Hales, and S. Kramer. 2017. Mechanistic understanding of ocean acidification impacts on larval feeding physiology and energy budgets of the mussel Mytilus californianus. Marine Ecology Progress Series 563: 81–94. Scholar
  11. Hasholt, B., and B. Hagedorn. 2000. Hydrology and geochemistry of river-borne material in a high arctic drainage system, Zackenberg, Northeast Greenland. Arctic Antarctic and Alpine Research 32: 84–94. Scholar
  12. Kroeker, K.J., R.L. Kordas, R.N. Crim, and G.G. Singh. 2010. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecology Letters 1311: 1419–1434. Scholar
  13. Lawson, E.C., J.L. Wadham, M. Tranter, M. Stibal, G.P. Lis, C.E.H. Butler, J. Laybourn-Parry, P. Nienow, D. Chandler, and P. Dewsbury. 2014. Greenland Ice Sheet exports labile organic carbon to the Arctic oceans. Biogeosciences 11: 4015–4028. Scholar
  14. Leng, M.J., and N.J. Anderson. 2003. Isotopic variation in modern lake waters from western Greenland. The Holocene 13: 605–611. Scholar
  15. McConnaughey, T.A., and D.P. Gillikin. 2008. Carbon isotopes in mollusk shell carbonates. Geo-Marine Letters 28: 287–299. Scholar
  16. Mackenzie, C.L., S.A. Lynch, S.C. Culloty, and S.K. Malham. 2014. Future oceanic warming and acidification alter immune response and disease status in a commercial shellfish species, Mytilus edulis L. PLoS One 96: e99712. Scholar
  17. Mathiesen, S.S., J. Thyrring, J. Hemmer-Hansen, J. Berge, A. Sukhotin, P. Leopold, M. Bekaert, M.K. Sejr, and E.E. Nielsen. 2017. Genetic diversity and connectivity within Mytilus spp. in the subarctic and Arctic. Evolutionary Applications 101 (1): 39–55. Scholar
  18. McCrea, J.M. 1950. On the isotopic chemistry of carbonates and a paleotemperature scale. The Journal of Chemical Physics 18: 849–857.CrossRefGoogle Scholar
  19. Mehrbach, C., C.H. Culberson, J.E. Hawley, and R.M. Pytkowicz. 1973. Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnology and Oceanography 18: 897–907.CrossRefGoogle Scholar
  20. Orr, J.C., V.J. Fabry, O. Aumont, L. Bopp, S.C. Doney, R.E. Feely, A. Gnanadesikan, N. Gruber, A. Ishida, F. Joos, and R.M. Key. 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437 (7059): 681. Scholar
  21. Peck, V.L., R.L. Oakes, E.M. Harper, C. Manno, and A.G. Tarling. 2018. Pteropods counter mechanical damage and dissolution through extensive shell repair. Nature Communications 9: 264. Scholar
  22. Pierrot, D., D.E. Lewis, and D.W.R. Wallace. 2006. CO2SYS.EXE—MS excel program developed for CO2 system calculations. ORNL/CDIAC-105a. Oak Ridge, Tennessee. Carbon Dioxide Information Center, Oak Ridge National Laboratory, U.S. Department of Energy.
  23. Ramajo, L., L. Prado, A.B. Rodriguez-Navarro, M.A. Lardies, C.M. Duarte, and N.A. Lagos. 2016a. Plasticity and trade-offs in physiological traits of intertidal mussels subjected to freshwater-induced environmental variation. Marine Ecology Progress Series 553: 93–109. Scholar
  24. Ramajo, L., E. Pérez-León, I.E. Hendriks, N. Marbà, D. Krause-Jensen, M.K. Sejr, M.E. Blicher, N.A. Lagos, Y.S. Olsen, and C.M. Duarte. 2016b. Food supply confers calcifiers resistance to ocean acidification. Scientific Reports 6: 19374. Scholar
  25. Rodolfo-Metalpa, R., F. Houlbrèque, É. Tambutté, F. Boisson, C. Baggini, F.P. Patti, R. Jeffree, M. Fine, A. Foggo, J.-P. Gattuso, and J.M. Hall-Spencer. 2011. Coral and mollusc resistance to ocean acidification adversely affected by warming. Nature Climate Change 16: 308. Scholar
  26. Rodríguez-Navarro, A.B., N. Dominguez-Gasca, A. Muñoz, and M. Ortega-Huertas. 2013. Change in the chicken egg-shell cuticle with hen age and egg freshness. Poultry Science 92 (11): 3026–3035. Scholar
  27. Rysgaard, S., and M. Sejr. 2007. Vertical flux of particulate organic matter in a High Arcic fjord: Relative importance of terrestrial and marine sources, p. 109–121. In Carbon cycling in Arctic marine ecosystems: Case study Young Sound. Medd. Groenland. Bioscience, ed. S. Rysgaard and R. Glud, vol. 58, 110–119.Google Scholar
  28. Sejr, M.K., D. Krause-Jensen, T. Dalsgaard, S. Ruiz-Halpern, C.M. Duarte, M. Middelboe, R.N. Glud, J. Bendtsen, T.J.S. Balsby, and S. Rysgaard. 2014. Seasonal dynamics of autotrophic and heterotrophic plankton metabolism and pCO2 in a subarctic Greenland fjord. Limnology and Oceanography 59: 1764–1778.CrossRefGoogle Scholar
  29. Stapp, L.S., J. Thomsen, H. Schade, C. Bock, F. Melzner, H.O. Pörtner, and G. Lannig. 2017. Intra-population variability of ocean acidification impacts on the physiology of Baltic blue mussels Mytilus edulis: integrating tissue and organism response. Journal of Comparative Physiology B 1874 (4): 529–543. Scholar
  30. Steinacher, M., F. Joos, T.L. Frölicher, G.K. Plattner, and S.C. Doney. 2009. Imminent ocean acidification in the Arctic projected with the NCAR global coupled carbon cycle-climate model. Biogeosciences 6: 515–533.CrossRefGoogle Scholar
  31. Thomsen, J., I. Casties, C. Pansch, A. Körtzinger, and F. Melzner. 2013. Food availability outweighs ocean acidification effects in juvenile Mytilus edulis: laboratory and field experiments. Global Change Biology 194: 1017–1027. Scholar
  32. Thyrring, J., M.E. Blicher, J.G. Sørensen, S. Wegeberg, and M.K. Sejr. 2017. Rising air temperatures will increase intertidal mussel abundance in the Arctic. Marine Ecology Progress Series 584: 91–104. Scholar
  33. Wahl, M., S. Schneider Covachã, V. Saderne, C. Hiebenthal, J.D. Müller, C. Pansch, and Y. Sawall. 2018. Macroalgae may mitigate ocean acidification effects on mussel calcification by increasing pH and its fluctuations. Limnology and Oceanogaphy 631: 3–21. Scholar
  34. Waldbusser, G.G., E.L. Brunner, B.A. Haley, B. Hales, C.J. Langdon, and F.G. Prahl. 2013. A developmental and energetic basis linking larval oyster shell formation to acidification sensitivity. Geophysical Research Letters 40: 2171–2176. Scholar
  35. Waldbusser, G.G., B. Hales, C.J. Langdon, B.A. Haley, P. Schrader, E.L. Brunner, M.W. Gray, C.A. Miller, and I. Gimenez. 2015. Saturation-state sensitivity of marine bivalve larvae to ocean acidification. Nature Climate Change 5 (3): 273. Scholar
  36. Wanamaker, A.D., K.J. Kreutz, H.W. Borns, D.S. Introne, S. Feindel, S. Funder, S.P.D. Rawson, and B.J. Barber. 2007. Experimental determination of salinity, temperature, growth, and metabolic effects on shell isotope chemistry of Mytilus edulis collected from Maine and Greenland. Paleoceanography 22: PA2217. Scholar
  37. Wiercigroch, E., E. Szafraniec, K. Czamara, M.Z. Pacia, K. Majzner, K. Kochan, A. Kaczor, M. Baranska, M., and K. Malek. 2017. Raman and infrared spectroscopy of carbohydrates: a review. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 185: 317–335. doi: Scholar
  38. Yarra, T., K. Gharbi, M. Blaxter, L.S. Peck, and M.S. Clark. 2016. Characterization of the mantle transcriptome in bivalves: Pectenmaximus, Mytilus edulis and Crassostreagigas. Marine Genomics 27: 9–15. Scholar

Copyright information

© Coastal and Estuarine Research Federation 2020

Authors and Affiliations

  1. 1.Red Sea Research Center (RSRC) and Computational BioScience Research Center (CBRC)King Abdullah University of Science and Technology KAUSTThuwalSaudi Arabia
  2. 2.Arctic Research Centre, Department of BioscienceAarhus UniversityArhus CDenmark
  3. 3.Departamento de Mineralogía y PetrologíaUniversidad de GranadaGranadaSpain
  4. 4.Instituto Andaluz de Ciencias de la Tierra CSIC-UGRArmillaSpain
  5. 5.Department of BioscienceAarhus UniversityArhus CDenmark

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