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Rapid dissolution of shells of weakly calcified Antarctic benthic macroorganisms indicates high vulnerability to ocean acidification

Published online by Cambridge University Press:  01 October 2009

James B. McClintock ,
Robert A. Angus ,
Michelle R. Mcdonald ,
Charles D. Amsler ,
Shane A. Catledge  and
Yogesh K. Vohra
James B. McClintock*
Affiliation:
Department of Biology, University of Alabama at Birmingham, AL 35294-1170, USA
Robert A. Angus
Affiliation:
Department of Biology, University of Alabama at Birmingham, AL 35294-1170, USA
Michelle R. Mcdonald
Affiliation:
Department of Biology, University of Alabama at Birmingham, AL 35294-1170, USA
Charles D. Amsler
Affiliation:
Department of Biology, University of Alabama at Birmingham, AL 35294-1170, USA
Shane A. Catledge
Affiliation:
Department of Physics, Center for Nanoscale Materials and Biointegration, University of Alabama at Birmingham, AL 35294-1170, USA
Yogesh K. Vohra
Affiliation:
Department of Physics, Center for Nanoscale Materials and Biointegration, University of Alabama at Birmingham, AL 35294-1170, USA
*
*mcclinto@uab.edu
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Abstract

Antarctic calcified macroorganisms are particularly vulnerable to ocean acidification because many are weakly calcified, the dissolution rates of calcium carbonate are inversely related to temperature, and high latitude seas are predicted to become undersaturated in aragonite by the year 2100. We examined the post-mortem dissolution rates of aragonitic and calcitic shells from four species of Antarctic benthic marine invertebrates (two bivalves, one limpet, one brachiopod) and the thallus of a limpet shell-encrusting coralline alga exposed to acidified pH (7.4) or non-acidified pH (8.2) seawater at a constant temperature of 4°C. Within a period of only 14–35 days, shells of all four species held in pH 7.4 seawater had suffered significant dissolution. Despite calcite being 35% less soluble in seawater than aragonite, there was surprisingly, no consistent pattern of calcitic shells having slower dissolution rates than aragonitic shells. Outer surfaces of shells held in pH 7.4 seawater exhibited deterioration by day 35, and by day 56 there was exposure of aragonitic or calcitic prisms within the shell architecture of three of the macroinvertebrate species. Dissolution of coralline algae was confirmed by differences in weight loss in limpet shells with and without coralline algae. By day 56, thalli of the coralline alga held in pH 7.4 displayed a loss of definition of the conceptacle pores and cracking was evident at the zone of interface with limpet shells. Experimental studies are needed to evaluate whether there are adequate compensatory mechanisms in these and other calcified Antarctic benthic macroorganisms to cope with anticipated ocean acidification. In their absence, these organisms, and the communities they comprise, are likely to be among the first to experience the cascading impacts of ocean acidification.

Keywords

Antarcticaaragonitebrachiopodcalcitecoralline algamollusc
Type
Biological Sciences
Information
Antarctic Science , Volume 21 , Issue 5 , October 2009 , pp. 449 - 456
Copyright
Copyright © Antarctic Science Ltd 2009

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References

Amsler, C.D., Rowley, R.J., Laur, D.R., Quetin, L.B.Ross, R.M. 1995. Vertical distribution of Antarctic peninsular macroalgae: cover, biomass and species diversity. Phycologia, 34, 424–430.CrossRefGoogle Scholar
Andersson, A.J., Mackenzie, F.T.Bates, N.R. 2008. Life on the margin: implications of ocean acidification on Mg–calcite, high latitude and cold-water marine calcifiers. Marine Ecology Progress Series, 373, 265–273.CrossRefGoogle Scholar
Arntz, W.E., Brey, T.Gallardo, V.A. 1994. Antarctic zoobenthos. Oceanography and Marine Biology, 32, 251–303.Google Scholar
Aronson, R., Thatje, S., Clarke, A., Peck, L.S., Blake, D.B., Wilga, C.D.Seibel, B.A. 2007. Climate change and invasibility of the Antarctic benthos. Annual Review Ecology, Evolution, and Systematics, 38, 129–154.CrossRefGoogle Scholar
Barnes, K.A., Fuentes, V., Clarke, A., Schloss, I.R.Wallace, M.I. 2006. Spatial and temporal variation in shallow seawater temperatures around Antarctica. Deep-Sea Research II, 53, 853–865.CrossRefGoogle Scholar
Barrera, E., Tevesv, M.J.S., Carter, J.G.McCall, P.L. 1994. Oxygen and carbon isotopic composition and shell microstructure of the bivalve Laternula elliptica from the Antarctic. Palaios, 9, 275–287.CrossRefGoogle Scholar
Caldeira, K.Wickett, M.E. 2003. Oceanography: anthropogenic carbon and ocean pH. Nature, 425, 365.CrossRefGoogle ScholarPubMed
Caldeira, K.Wickett, M.E. 2005. Ocean model prediction of chemistry changes from carbon dioxide emission to the atmosphere and ocean. Journal of Geophysical Research, 110, 10.1029/2004JC002671.CrossRefGoogle Scholar
Carter, J.G. 1990. Skeletal biomineralization: patterns, processes and evolutionary trends, vol. 1. New York: Van Nostrand Reinhold, 832 pp.Google Scholar
Clarke, A.Johnston, N.M. 2003. Antarctic marine benthic diversity. Oceanographic Marine Biology, 42, 47–114.Google Scholar
Clarke, A., Prothero-Thomas, E., Beaumont, J.C., Chapman, A.L.Brey, T. 2004. Growth in the limpet Nacella concinna from contrasting sites in Antarctica. Polar Biology, 28, 62–71.Google Scholar
Dupont, S., Havenhand, J., Thorndyke, W., Peck, L.Thorndyke, M. 2008. Near-future level of CO2-driven ocean acidification radically affects larval survival and development in the brittlestar Ophiothrix fragilis. Marine Ecology Progress Series, 373, 285–294.CrossRefGoogle Scholar
Fabry, V.J., Seibel, B.A., Feely, R.A.Orr, J.C. 2008. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES Journal of Marine Science, 65, 414–432.CrossRefGoogle Scholar
Fabry, V.J. 2008. Marine calcifiers in a high-CO2 ocean. Science, 320, 1020–1022.CrossRefGoogle Scholar
Fine, M.P.Tchernov, D.P. 2007. Scleractinian coral species survive and recover from decalcification. Science, 315, 1118–1121.CrossRefGoogle ScholarPubMed
Glover, C.Kidwell, S.M. 1993. Influence of organic matrix on the post-mortem destruction of molluscan shells. Journal of Geology, 101, 729–747.CrossRefGoogle Scholar
Graus, R.R. 1974. Latitudinal trends in the shell characteristics of marine gastropods. Lethaia, 7, 303–314.CrossRefGoogle Scholar
Guinotte, J.M.Fabry, V.J. 2008. Ocean acidification and its potential effects on marine ecosystems. Annals of the New York Academy of Sciences, 1134, 320–342.CrossRefGoogle ScholarPubMed
Hall-Spencer, J.M., Rodolfo-Metalpa, R., Martin, S., Ransome, E.Fine, M. 2008. Climate change: acid test for marine biodiversity. Nature, 454, 96–99.CrossRefGoogle Scholar
Harper, E.M. 2000. Are calcitic layers an effective adaptation against shell dissolution in the Bivalvia? Journal of Zoology, 251, 179–186.CrossRefGoogle Scholar
Hoegh-Guldberg, O., Mumby, P.J., Hooton, A.J., Steneck, R.S., Greenfield, P., Gomez, E., Harvell, C.D., Sale, P.F., Edwards, A.J., Caldeira, K., Knowlton, N., Eakin, C.M., Iglesias-Prieto, R., Muthiga, N., Bradbury, R.H., Dubi, A.Hatziollos, M.E. 2007. Coral reefs under rapid climate change and ocean acidification. Science, 318, 1737–1742.CrossRefGoogle ScholarPubMed
Kuffner, I.B., Andersson, A.J., Jokeil, P.L., Rodgers, K.S.Mackenzie, F.T. 2008. Decreased abundance of crustose coralline algae due to ocean acidification. Nature Geoscience, 1, 114–117.CrossRefGoogle Scholar
Kurihara, H. 2008. Effects of CO2-driven ocean acidification on the early development stages of invertebrates. Marine Ecology Progress Series, 373, 275–284.CrossRefGoogle Scholar
Kurihara, H.Shirayama, Y. 2004. Effects of increased atmospheric CO2 on sea urchin early development. Marine Ecology Progress Series, 274, 161–169.CrossRefGoogle Scholar
Kurihara, H., Shimode, S.Shirayama, Y. 2004. Sub-lethal effects of elevated concentration of CO2 on planktonic copepods and sea urchins. Journal of Oceanography, 60, 743–750.CrossRefGoogle Scholar
Lockwood, R.Work, L.A. 2006. Quantifying taphonomic bias in molluscan death assemblages from the upper Chesapeake Bay: patterns of shell damage. Palaios, 21, 442–450.CrossRefGoogle Scholar
Marshall, J.D., Pirrie, D., Clarke, A., Nolar, C.P.Sharman, J. 1996. Stable-isotopic composition and skeletal carbonates from living Antarctic marine invertebrates. Lethaia, 29, 203–212.CrossRefGoogle Scholar
Mcclintock, J.B., Ducklow, H.Fraser, W. 2008. Ecological responses to climate change on the Antarctic Peninsula. American Scientist, 96, 302–310.CrossRefGoogle Scholar
Mcneil, B.I.Matear, R.J. 2008. Southern Ocean acidification: a tipping point at 450-ppm atmospheric CO2. Proceedings of the National Academy of Sciences of the United States, 105, 18860–18864.CrossRefGoogle ScholarPubMed
Morse, J.W., Mucci, A.Millero, F.J. 1980. The solubility of calcite and aragonite in seawater of 35 ppt salinity at 25°C and atmospheric pressure. Geochimica et Cosmochimica Acta, 44, 85–94.CrossRefGoogle Scholar
Mucci, A. 1983. The solubility of calcite and aragonite in seawater at various salinities, temperatures and one atmosphere total pressure. American Journal of Science, 283, 780–799.CrossRefGoogle Scholar
Nicol, J.A.C. 1967. The biology of marine animals. London: Wiley Interscience, 699 pp.Google Scholar
Pearse, J.S., Mcclintock, J.B.Bosch, I. 1991. Reproduction of Antarctic benthic marine invertebrates: tempos, modes and timing. American Zoologist, 31, 65–80.CrossRefGoogle Scholar
Pearson, P.N.Palmer, M.R. 2000. Atmospheric carbon dioxide concentrations over the past 60 million years. Nature, 406, 695–699.CrossRefGoogle ScholarPubMed
Peck, L.S.Bullough, L.W. 1993. Growth and population structure in the infaunal bivalve Yoldia eightsi in relation to iceberg activity at Signy Island, Antarctica. Marine Biology, 117, 235–241.CrossRefGoogle Scholar
Peck, L.S., Brockington, S.Brey, T. 1997. Growth and metabolism in the Antarctic brachiopod Liothyrella uva. Philosophical Transactions of the Royal Society of London, B352, 851–858.CrossRefGoogle Scholar
Ralph, R.Maxwell, J.H.G. 1977. Growth of two Antarctic lamellibranchs: Adamussium colbecki and Laternula elliptica. Marine Biology, 42, 171–175.CrossRefGoogle Scholar
Revelle, R.Fairbridge, R. 1957. Carbonates and carbon dioxide. Geological Society of American Memoirs, 67, 239–296.CrossRefGoogle Scholar
Scurr, D.J.Eichhorn, S.J. 2005. Structure/property relationships in seashells. In Viney, C., Katti, K., Ulm, F-J., Hellmich, C., eds. Mechanical Properties of Bioinspired Materials. Warrendale, PA: Materials Research Society Symposium Proceedings, 87–92.Google Scholar
Sundquist, E.T. 1993. The global carbon dioxide budget. Science, 259, 934–941.CrossRefGoogle Scholar
Taylor, J.D.Reid, D.G. 1990. Shell microstructure and mineralogy of the Littorinidae; ecological and evolutionary significance. Hydrobiologia, 193, 199–215.CrossRefGoogle Scholar
Thatje, S., Anger, K., Calcagno, J.A., Lovrich, G.A., Portner, H.-O.Arntz, W.E. 2005. Challenging the cold: crabs reconquer the Antarctic. Ecology, 6, 619–625.CrossRefGoogle Scholar
Vermeij, G.J. 1978. Biogeography and adaptation: patterns of marine life. Boston, MA: Harvard University Press, 332 pp.Google Scholar
Vermeij, G.J. 1993. A natural history of shells. Princeton, NJ: Princeton University Press, 207 pp.Google Scholar
Wigley, T.M.L., Richels, R.Edmonds, J.A. 1996. Economic and environmental choices in the stabilization of atmospheric CO2 concentrations. Nature, 379, 240–243.CrossRefGoogle Scholar