Advertisement

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

Abstract

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.

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

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 99

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Arrigo, K.R., and G.L. van Dijken. 2015. Continued increases in Arctic Ocean primary production. Progress in Oceanography 136: 60–70. https://doi.org/10.1016/j.pocean.2015.05.002.

  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. https://doi.org/10.1029/2012GL052552.

  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. https://doi.org/10.1016/j.gca.2013.02.006.

  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. https://doi.org/10.1080/15287394.2011.550460.

  5. Bubel, A. 1973. An electron-microscope study of periostracum repair in Mytilus edulis. Marine Biology 20: 235–244.

  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.

  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. https://doi.org/10.1007/s12237-018-0368-9.

  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. https://doi.org/10.1007/s12237-014-9845-y.

  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. https://doi.org/10.5194/bg-7-2051-2010.

  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. https://doi.org/10.3354/meps11977.

  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. https://doi.org/10.1080/15230430.2000.12003342.

  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. https://doi.org/10.1111/j.1461-0248.2010.01518.x.

  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. https://doi.org/10.5194/bg-11-4015-2014.

  14. Leng, M.J., and N.J. Anderson. 2003. Isotopic variation in modern lake waters from western Greenland. The Holocene 13: 605–611. https://doi.org/10.1191/0959683603hl620rr.

  15. McConnaughey, T.A., and D.P. Gillikin. 2008. Carbon isotopes in mollusk shell carbonates. Geo-Marine Letters 28: 287–299. https://doi.org/10.1007/s00367-008-0116-4.

  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. https://doi.org/10.1371/journal.pone.0099712.

  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. https://doi.org/10.1111/eva.12415.

  18. McCrea, J.M. 1950. On the isotopic chemistry of carbonates and a paleotemperature scale. The Journal of Chemical Physics 18: 849–857.

  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.

  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. https://doi.org/10.1038/nature04095.

  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. https://doi.org/10.1038/s41467-017-02692-w.

  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. http://cdiac.ornl.gov/ftp/co2sys/. 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. https://doi.org/10.3354/meps11764.

  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. https://doi.org/10.1038/srep19374.

  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. https://doi.org/10.1038/nclimate1200.

  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. https://doi.org/10.3382/ps.2013-03230.

  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.

  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.

  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. https://doi.org/10.1007/s00360-016-1053-6.

  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.

  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. https://doi.org/10.1111/gcb.12109.

  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. https://doi.org/10.3354/meps12369.

  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. https://doi.org/10.1002/lno.10608.

  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. https://doi.org/10.1002/grl.50449.

  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. https://doi.org/10.1038/NCLIMATE2479.

  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. https://doi.org/10.1029/2006PA001352.

  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: https://doi.org/10.1016/j.saa.2017.05.045.

  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. https://doi.org/10.1016/j.margen.2016.04.003.

Download references

Acknowledgments

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 (www.GEM.dk) MarineBasis in Nuuk and Disko Bay.

Funding Information

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

Author information

Correspondence to Carlos M. Duarte.

Additional information

Communicated by Silvana Birchenough

Electronic Supplementary Material

ESM 1

(DOCX 17 kb)

Placeholder Text

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Duarte, C.M., Rodriguez-Navarro, A.B., Delgado-Huertas, A. et al. Dense Mytilus Beds Along Freshwater-Influenced Greenland Shores: Resistance to Corrosive Waters Under High Food Supply. Estuaries and Coasts (2020) doi:10.1007/s12237-019-00682-3

Download citation

Keywords

  • Bivalve
  • Shell
  • Ocean acidification
  • Carbonate