Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-10T15:50:03.088Z Has data issue: false hasContentIssue false
  • English
  • Français

Short-term exposure to hypercapnia does not compromise feeding, acid–base balance or respiration of Patella vulgata but surprisingly is accompanied by radula damage

Published online by Cambridge University Press:  02 June 2010

Hannah K. Marchant ,
Piero Calosi  and
John I. Spicer
Hannah K. Marchant
Affiliation:
Marine Biology and Ecology Research Centre, University of Plymouth, Drake Circus, Plymouth, Devon, PL4 8AA, UK
Piero Calosi*
Affiliation:
Marine Biology and Ecology Research Centre, University of Plymouth, Drake Circus, Plymouth, Devon, PL4 8AA, UK
John I. Spicer
Affiliation:
Marine Biology and Ecology Research Centre, University of Plymouth, Drake Circus, Plymouth, Devon, PL4 8AA, UK
*
Correspondence should be addressed to: P. Calosi, Marine Biology and Ecology Research Centre, University of Plymouth, Drake Circus, Plymouth, Devon, PL4 8AA, UK e-mail: piero.calosi@plymouth.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

The effect of short-term (5 days) exposure to CO2-acidified seawater (year 2100 predicted values, ocean pH = 7.6) on key aspects of the function of the intertidal common limpet Patella vulgata (Gastropoda: Patellidae) was investigated. Changes in extracellular acid–base balance were almost completely compensated by an increase in bicarbonate ions. A concomitant increase in haemolymph Ca2+ and visible shell dissolution implicated passive shell dissolution as the bicarbonate source. Analysis of the radula using SEM revealed that individuals from the hypercapnic treatment showed an increase in the number of damaged teeth and the extent to which such teeth were damaged compared with controls. As radula teeth are composed mainly of chitin, acid dissolution seems unlikely, and so the proximate cause of damage is unknown. There was no hypercapnia-related change in metabolism (O2 uptake) or feeding rate, also discounting the possibility that teeth damage was a result of a CO2-related increase in grazing. We conclude that although the limpet appears to have the physiological capacity to maintain its extracellular acid–base balance, metabolism and feeding rate over a 5 days exposure to acidified seawater, radular damage somehow incurred during this time could still compromise feeding in the longer term, in turn decreasing the top-down ecosystem control that P. vulgata exerts over rocky shore environments.

Keywords

acid–base balancehypercapniamolluscocean acidificationoxygen uptakeradula
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 90 , Issue 7 , November 2010 , pp. 1379 - 1384
Copyright
Copyright © Marine Biological Association of the United Kingdom 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Caldeira, K. and Wickett, M.E. (2003) Anthropogenic carbon and ocean pH. Nature 425, 325.CrossRefGoogle ScholarPubMed
Davies, M.S., Proudlock, D.J. and Mistry, A. (2005) Metal concentrations in the radula of the common limpet, Patella vulgata L., from 10 sites in the UK. Ecotoxicology 14, 465–475.CrossRefGoogle ScholarPubMed
Dickson, A.G. (1990) Thermodynamics of the dissociation of boric acid in synthetic seawater from 273.15 to 318.15 K. Deep-Sea Research 37, 755–766.Google Scholar
Dickson, A.G. and Millero, F.J. (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Research 34, 1733–1743.CrossRefGoogle Scholar
Ellis, R., Bersey, J., Rundle, S.D., Hall-Spencer, J.M. and Spicer, J.I. (2009) Subtle but significant effects of CO2 acidified seawater on embryos of the intertidal snail, Littorina obtusata. Aquatic Biology 5, 41–48.CrossRefGoogle Scholar
Hall-Spencer, J.M., Rodolfo-Metalpa, R., Martin, S., Ransome, E., Fine, M., Turner, S.M., Rowley, S.J., Tedesco, D. and Buia, M.-C. (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454, 96–99.Google Scholar
Haugan, P.M. and Drange, H. (1996) Effects of CO2 on the ocean environment. Energy Conversation Management 37, 1019–1022.CrossRefGoogle Scholar
Hawkins, S.J. and Hartnoll, R.G. (1983) Grazing of intertidal algae by marine invertebrates. Oceanography and Marine Biology: an Annual Review 21, 195–282.Google Scholar
Houghton, J.T., Ding, Y., Griggs, D.J., Noguer, M., Linden P.J., van der and Xiaosu, D. (2001) Climate Change 2001: the scientific basis. In IPCC Third Assessment Report: Climate Change 2001. Cambridge: Cambridge University Press.Google Scholar
Jonsson, P.R., Granhag, L., Moschella, P.S., Aberg, P., Hawkins, S.J. and Thompson, R.C. (2006) Interactions between wave action and grazing control the distribution of intertidal macroalgae. Ecology 87, 1169–1178.Google Scholar
Lindinger, M.I., Lauren, D.J. and McDonald, D.G. (1984) Acid–base balance in the sea mussel, Mytilus edulis. 3. Effects of environmental hypercapnia on intracellular and extracellular acid–base balance. Marine Biology Letters 5, 371–381.Google Scholar
Mann, S., Perry, C.C., Webb, J., Luke, B. and Williams, R.J.P. (1986) Structure, morphology, composition and organization of the biogenic materials in limpet teeth. Proceedings of the Royal Society B 227, 179–190.Google Scholar
Mehrbach, C., Culberson, C.H., Hawley, J.E. and Pytkowicz, R.M. (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnology and Oceanography 18, 897–907.CrossRefGoogle Scholar
Michaelidis, B., Ouzounis, C., Paleras, A. and Pörtner, H.O. (2005) Effects of long-term moderate hypercapnia on acid–base balance and growth rate in marine mussels Mytilus galloprovincialis. Marine Ecology Progress Series 293, 109–118.CrossRefGoogle Scholar
Morris, S. and Taylor, A.C. (1983) Diurnal and seasonal variation in physico-chemical conditions within intertidal rock pools. Estuarine, Coastal and Shelf Science 17, 339–355.CrossRefGoogle Scholar
Orr, J.C., Fabry, V.J., Aumont, O., Bopp, L., Doney, S.C., Feely, R.A., Gnanadesikan, A., Gruber, N., Ishida, A., Joos, F., Key, R.M., Lindsay, K., Maier-Reimer, E., Matear, R., Monfray, P., Mouchet, A., Najjar, R.G., Plattner, G.K., Rodgers, K.B., Sabine, C.L., Sarmiento, J.L., Schlitzer, R., Slater, R.D., Totterdell, I.J., Weirig, M.F., Yamanaka, Y. and Yool, A. (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681–686.CrossRefGoogle ScholarPubMed
Pane, E.F. and Barry, J.P. (2007) Extracellular acid–base regulation during short-term hypercapnia is effective in a shallow-water crab, but ineffective in a deep-sea crab. Marine Ecology Progress Series 334, 1–9.CrossRefGoogle Scholar
Pierrot, D., Lewis, E. and Wallace, D.W.R. (2006) MS Excel program developed for CO2 system calculations, ORNL/CDIAC-105. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, Tennessee, USA.Google Scholar
Pörtner, H.-O., Langenbuch, M. and Reipschlager, A. (2004) Biological impact of elevated ocean CO2 concentrations: lessons from animal physiology and earth history. Journal of Oceanography 60, 705–718.CrossRefGoogle Scholar
Raven, J., Caldeira, K., Elderfield, H., Hoegh-Guldberg, O., Liss, P.S., Riebesell, U., Sheperd, J. and Watson, A.J. (2005) Ocean acidification due to increasing atmospheric carbon dioxide. Royal Society Policy Document 12/05, 1–60.Google Scholar
Spicer, J.I. and Eriksson, S.P. (2003) Does the development of respiratory regulation always accompany the transition from pelagic larvae to benthic fossorial postlarvae in the Norway lobster Nephrops norvegicus (L.)? Journal of Experimental Marine Biology and Ecology 295, 291–243.CrossRefGoogle Scholar
Spicer, J.I., Taylor, A.C. and Hill, A.D. (1988) Acid–base status in the sea urchins Psammechinus miliaris and Echinus esculentus (Echinodermata: Echinoidea) during emersion. Marine Biology 99, 527–534.CrossRefGoogle Scholar
Truchot, J.P. (1976) Carbon dioxide combining properties of the blood of the shore crab Carcinus maenas (L.): carbon dioxide solubility coefficient and carbonic acid dissociation constants. Journal of Experimental Biology 64, 45–57.CrossRefGoogle ScholarPubMed
Widdicombe, S. and Spicer, J.I. (2008) Predicting the impact of ocean acidification on benthic biodiversity: what can animal physiology tell us? Journal of Experimental Marine Biology and Ecology 366, 187–197.CrossRefGoogle Scholar
Wood, H.L., Spicer, J.I. and Widdicombe, S. (2008) Ocean acidification may increase calcification rates but at a cost. Proceedings of the Royal Society B 275, 1767–1773.CrossRefGoogle ScholarPubMed
Wootton, J.T., Pfister, C.A. and Forester, J.D. (2008) Dynamic patterns and ecological impacts of declining ocean pH in a high-resolution multi-year dataset. Proceedings of the National Academy of Sciences. Published online before print 24 November 2008, doi:2010.1073/pnas.0810079105.Google Scholar