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Nature Geoscience | Letter

Extensive dissolution of live pteropods in the Southern Ocean

Journal name:
Nature Geoscience
Volume:
5,
Pages:
881–885
Year published:
DOI:
doi:10.1038/ngeo1635
Received
Accepted
Published online

The carbonate chemistry of the surface ocean is rapidly changing with ocean acidification, a result of human activities1. In the upper layers of the Southern Ocean, aragonite—a metastable form of calcium carbonate with rapid dissolution kinetics—may become undersaturated by 2050 (ref. 2). Aragonite undersaturation is likely to affect aragonite-shelled organisms, which can dominate surface water communities in polar regions3. Here we present analyses of specimens of the pteropod Limacina helicina antarctica that were extracted live from the Southern Ocean early in 2008. We sampled from the top 200 m of the water column, where aragonite saturation levels were around 1, as upwelled deep water is mixed with surface water containing anthropogenic CO2. Comparing the shell structure with samples from aragonite-supersaturated regions elsewhere under a scanning electron microscope, we found severe levels of shell dissolution in the undersaturated region alone. According to laboratory incubations of intact samples with a range of aragonite saturation levels, eight days of incubation in aragonite saturation levels of 0.94–1.12 produces equivalent levels of dissolution. As deep-water upwelling and CO2 absorption by surface waters is likely to increase as a result of human activities2, 4, we conclude that upper ocean regions where aragonite-shelled organisms are affected by dissolution are likely to expand.

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  1. Scotia Sea showing sampling station positions and frontal positions at time of sampling.
    Figure 1: Scotia Sea showing sampling station positions and frontal positions at time of sampling.

    Dynamic height contours were used to determine the location of the following fronts: SB, Southern Boundary; SACCF, Southern Antarctic Circumpolar Current Front; south and north edge of Polar Front (S-PF, N-PF). Fifteen per cent ice cover is represented by blue shading.

  2. Vertical profiles of [Omega]A across the Scotia Sea (upper) and corresponding dissolution levels in live juvenile L. helicina antarctica (lower).
    Figure 2: Vertical profiles of ΩA across the Scotia Sea (upper) and corresponding dissolution levels in live juvenile L. helicina antarctica (lower).

    N is the number of individuals analysed per station. The horizontal bars denote mean proportional shell area per dissolution level across all specimens; error bars represent 1 s.d. Level I dissolution was significantly higher in Su9 specimens compared with all other stations (Mann–Whitney rank sum test, T = 778, 20 and 35 df, P<0.001). Su9 was also the only station in which level II and III dissolution was observed.

  3. SEM section of the shell of L. helicina antarctica showing the organic layer (periostracum), prismatic layer and crossed-lamellar matrix of aragonite crystals.
    Figure 3: SEM section of the shell of L. helicina antarctica showing the organic layer (periostracum), prismatic layer and crossed-lamellar matrix of aragonite crystals.
  4. SEM images of juvenile L. helicina antarctica (from which the periostracum has been removed) showing different levels of dissolution.
    Figure 4: SEM images of juvenile L. helicina antarctica (from which the periostracum has been removed) showing different levels of dissolution.

    a,b, Intact animal without any indications of dissolution. c, Level I: the upper prismatic layer slightly dissolved. d, Level II: the prismatic layer partially or completely missing and the cross-lamellar matrix partially exposed with increasing porosity in the upper crystalline layer. e,f, Level III: the crossed-lamellar matrix showing signs of dissolution across large areas of the shell, and the shell becoming more fragile owing to fragmentation (high-resolution images are available in the Supplementary Information).

  5. Average (s.d.) proportion of different dissolution levels in live juvenile L. helicina antarctica from the natural environment and ship-board incubations.
    Figure 5: Average (s.d.) proportion of different dissolution levels in live juvenile L. helicina antarctica from the natural environment and ship-board incubations.

    Supersaturated refers to ΩA>1.1, transitional, 0.95–1.1 and undersaturated, 0.75–0.95. N refers to the numbers of specimens analysed. The vertical bars denote the mean proportional shell area per dissolution level; error bars represent 1 s.d. Incubation for 14 days in undersaturated conditions caused a significant increase in level III dissolution compared with all other groupings (Kruskal–Wallis one-way analysis of variance, H = 51.7, 4 df, P<0.001). Extents of level II and III dissolution were statistically indistinguishable between Su9 and 8 day transitional incubations.

References

  1. Feely, R. A., Sabine, C. L., Hernandez-Ayon, J. M., Ianson, D. & Hales, B. Evidence for upwelling of corrosive ‘acidified’ water onto the continental shelf. Science 320, 1490–1492 (2008).
  2. Orr, J. C. et al. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681–686 (2005).
  3. Hunt, B. P. V. et al. Pteropods in Southern Ocean ecosystems. Prog. Oceanogr. 78, 193–221 (2008).
  4. Le Quere, C. et al. Saturation of the Southern Ocean CO2 sink due to recent climate change. Science 316, 1735–1738 (2007).
  5. Fabry, V. J. Shell growth rates of pteropod and heteropod molluscs and aragonite production in the open ocean: Implications for the marine carbonate system. J. Mar. Res. 48, 209–222 (1990).
  6. Broecker, W. S. & Takahashi, T. in The Fate of Fossil Fuel CO2 in the Oceans (eds Andersen, N. R. & Malahoff, A.) 213–241 (1977).
  7. Betzer, P. R. et al. The oceanic carbonate system—a reassessment of biogenic control. Science 226, 1074–1077 (1984).
  8. Feely, R. A. et al. Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305, 362–366 (2004).
  9. Byrne, R. H., Acker, J. G., Betzer, P. R., Feely, R. A. & Cates, M. H. Water column dissolution of aragonite in the Pacific Ocean. Nature 312, 321–326 (1984).
  10. Feely, R. A. et al. Winter-summer variations of calcite and aragonite saturation in the Northeast Pacific. Mar. Chem. 25, 227–241 (1988).
  11. Yamamoto-Kawai, M., McLaughlin, F. A., Carmack, E. C., Nishino, S. & Shimada, K. Aragonite undersaturation in the Arctic Ocean: Effects of ocean acidification and sea ice melt. Science 326, 1098–1100 (2009).
  12. McNeil, B. I. & Matear, R. J. Southern Ocean acidification: A tipping point at 450 ppm atmospheric CO2. Proc. Natl Acad. Sci. USA 105, 18860–18864 (2008).
  13. Steinacher, M., Joos, F., Frolicher, T. L., Plattner, G. K. & Doney, S. C. Imminent ocean acidification in the Arctic projected with the NCAR global coupled carbon cycle-climate model. Biogeosciences 6, 515–533 (2009).
  14. Comeau, S., Jeffree, R., Teyssie, J. L. & Gattuso, J. P. Response of the Arctic pteropod Limacina helicina to projected future environmental conditions. PLoS ONE 5, e11362 (2010).
  15. Comeau, S., Gorsky, G., Alliouane, S. & Gattuso, J. P. Larvae of the pteropod Cavolinia inflexa exposed to aragonite undersaturation are viable but shell-less. Mar. Biol. 157, 2341–2345 (2010).
  16. Roberts, D. et al. Interannual pteropod variability in sediment traps deployed above and below the aragonite saturation horizon in the Sub-Antarctic Southern Ocean. Polar Biol. 34, 1739–1750 (2011).
  17. Heywood, K. J., Garabato, A. C. N. & Stevens, D. P. High mixing rates in the abyssal Southern Ocean. Nature 415, 1011–1014 (2002).
  18. Kahru, M., Mitchell, B. G., Gille, S. T., Hewes, C. D. & Holm-Hansen, O. Eddies enhance biological production in the Weddell-Scotia confluence of the Southern Ocean. Geophys. Res. Lett. 34, L14603 (2007).
  19. Park, J., Ohb, I-S., Kim, H-C. & Yoo, S. Variability of SeaWiFs chlorophyll-a in the southwest Atlantic sector of the Southern Ocean: Strong topographic effects and weak seasonality. Deep-Sea Res Pt. I 57, 604–620 (2010).
  20. Jones, E., Bakker, D., Venables, H. & Watson, A. Dynamic seasonal cycling of inorganic carbon downstream of South Georgia, Southern Ocean. Deep-Sea Res. Pt. II 59–60, 25–35 (2012).
  21. Bednarsek, N., Tarling, G., Fielding, S. & Bakker, D. Population dynamics and biogeochemical significance of Limacina helicina antarctica in the Scotia Sea (Southern Ocean). Deep-Sea Res. Pt. II 59–60, 105–116 (2012).
  22. Jansen, H., Zeebe, R.E. & Wolf-Gladrow, D.A. Modeling the dissolution of settling CaCO3 in the ocean. Glob. Biogeochem. Cycles 16, 1027 (2002).
  23. Francois, R., Honjo, S., Krishfield, R. & Manganini, S. Factors controlling the flux of organic carbon to the bathypelagic zone of the ocean. Glob. Biogeochem. Cycles 16, 1087 (2002).
  24. Fabry, V. J., McClintock, J. B., Mathis, J. T. & Grebmeier, J. M. Ocean acidification at high latitudes: The bell weather. Oceanography 22, 160–171 (2009).
  25. Johnson, K. M., Sieburth, J. M., Williams, P. J. L. & Brandstrom, L. Coulometric total carbon dioxide analysis for marine studies—automation and calibration. Mar. Chem. 21, 117–133 (1987).
  26. Dickson, A. G. An exact definition of total alkalinity and a procedure for the estimation of alkalinity and total inorganic carbon from titration data. Deep-Sea Res. 28, 609–623 (1981).
  27. Lewis, E. & Wallace, D. W. R. co2sys - Program Developed for CO2 System Calculations Report ORNL/CDIAC-105 (Carbon Dioxide Information and Analysis Centre, Oak Ridge Natl. Lab., US Dep. of Energy, 1998).
  28. Mehrbach, C., Culberson, C. H., Hawley, J. E. & Pytkowicz, R. M. Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol. Oceanogr. 18, 897–907 (1973).
  29. Dickson, A. G. & Millero, F. J. A comparison of the equilibrium constants for the dissociationof carbonic acid in seawater media. Deep-Sea Res. 34, 1733–1743 (1987).
  30. Bednarsek, N. et al. Description and quantification of pteropod shell dissolution: A sensitive bioindicator of ocean acidification. Global Change Biol. 18, 2378–2388 (2012).

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Author information

Affiliations

  1. British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge, CB3 0ET, UK

    • N. Bednaršek,
    • G. A. Tarling,
    • S. Fielding,
    • H. J. Venables,
    • P. Ward &
    • E. J. Murphy

  2. School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, UK

    • N. Bednaršek,
    • D. C. E. Bakker &
    • B. Lézé

  3. University of Nova Gorica, Vipavska 13, 5000 Nova Gorica, Slovenia

    • N. Bednaršek

  4. Royal Netherlands Institute for Sea Research, PO Box 59, 1790 AB Den Burg, Texel, The Netherlands

    • E. M. Jones

  5. Department of Geology and Geophysics, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543, USA

    • A. Kuzirian

  6. NOAA, Pacific Marine Environmental Laboratory, Seattle, Washington 98115, USA

    • R. A. Feely

Contributions

G.A.T. and D.C.E.B. conceived the project; N.B. carried out the fieldwork, with the assistance of G.A.T., S.F. and P.W.; E.M.J. and H.J.V. provided supporting environmental data; A.K. helped develop a method of shell preparation for SEM analysis; B.L. developed an image analysis method; G.A.T., N.B. and D.C.E.B. co-wrote the manuscript, with theoretical overviews provided by R.A.F. and all remaining authors commenting.

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The authors declare no competing financial interests.

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