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Aerial and underwater metabolism of Patella vulgata L.: comparison of three intertidal levels

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Abstract

Intertidal molluscs are known to possess specific respiratory organs that permit aerial breathing during emersion. Patella vulgata is a widely distributed intertidal species found from low-water spring tide to high-water neap tidal level. In order to determine metabolic adaptations to habitat, carbon fluxes associated with respiration and calcification of P. vulgata living at high-shore, middle-shore and low-shore levels were compared. Seasonal aerial respiration was measured using an infrared gas analyser; seasonal underwater respiration and calcification were calculated from dissolved inorganic carbon and total alkalinity. P. vulgata showed net CaCO3 deposition at all seasons, although the high-shore level limpet annual calcification rate was relatively low due to longer air exposure. Both aerial and underwater respiration rates were highly correlated with seasonal temperature variations and followed the vertical shore gradient, with stronger fluxes for low-shore tidal level limpets and lower fluxes for high-shore level limpets that must limit energy expenditure. P. vulgata appears to be well adapted to aerial exposure, with average hourly respiration fluxes stronger in air than in water. This study demonstrates that P. vulgata calcification and respiration are reduced in upper shore levels and are important factors determining the upper distribution limit of the species.

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Abbreviations

ANOVA:

Analysis of variance

ANCOVA:

Analysis of covariance

AT:

Total alkalinity

DIC:

Dissolved inorganic carbon

HSD:

Honestly Significant Difference

MAREL:

Measures Automatisées en Réseau pour l’Environnement et le Littoral

PVC:

Polyvinyl chloride

SHOM:

Service Hydrographique et Océanographique de la Marine

SOMLIT:

Service d’Observation en Milieu Littoral

References

  • Abele, D., M. Kruppe, E. Philipp & T. Brey, 2010. Mantle cavity water oxygen partial pressure (PO2) in marine molluscs aligns with lifestyle. Canadian Journal of Fisheries and Aquatic Sciences 67: 977–986.

    Article  CAS  Google Scholar 

  • Alistair, H., 1995. Body-size variation exhibited by an intertidal limpet: influence of wave exposure, tidal height and migratory behavior. Journal of Experimental Marine Biology and Ecology 189: 29–45.

    Article  Google Scholar 

  • Bishop, S. H., L. L. Ellis & J. M. Burcham, 1983. Amino acid metabolism in molluscs The mollusca. vol 1. Academic Press, New York: 243–327.

    Google Scholar 

  • Blackmore, D., 1969. Studies of Patella vulgata L. I. Growth, reproduction and zonal distribution. Journal of Experimental Marine Biology and Ecology 3: 200–213.

    Article  Google Scholar 

  • Boaventura, D., L. Cancela da Fonseca & S. J. Hawkins, 2002. Analysis of competitive interactions between the limpets Patella depressa Pennant and Patella vulgata L. on the northern coast of Portugal. Journal of Experimental Marine Biology and Ecology 271: 171–188.

    Article  Google Scholar 

  • Boaventura, D., L. C. Da Fonseca & S. J. Hawkins, 2003. Size matters: competition within populations of the limpet Patella depressa. Journal of Animal Ecology 72: 435–446.

    Article  Google Scholar 

  • Bourget, E. & D. J. Crisp, 1975. Factors affecting deposition of the shell in Balanus balanoides (L.). Journal of the Marine Biological Association of the United Kingdom 55: 231–249.

    Article  Google Scholar 

  • Branch, G. M., 1978. Respiratory adaptations in the limpet Patella granatina: a comparison with other limpets. Compendium of Biochemistry and Physiology 62 A: 641–647.

    Google Scholar 

  • Branch, G. M., 1981. The biology of limpets: physical factors, energy flow, and ecological interactions. Oceanography and Marine Biology: An Annual Review 19: 235–380.

    Google Scholar 

  • Brinkhoff, W., K. Stöckmann & M. Grieshaber, 1983. Natural occurrence of anaerobiosis in molluscs from intertidal habitats. Oecologia 57: 151–155.

    Article  Google Scholar 

  • Chisholm, J. R. M. & J. P. Gattuso, 1991. Validation of the alkalinity anomaly technique for investigating calcification and photosynthesis in coral reef communities. Limnology and Oceanography 36: 1232–1239.

    Article  CAS  Google Scholar 

  • Clarke, A., 1990. Faecal egestion and ammonia excretion in the Antarctic limpet Nacella continna (Strebel, 1908). Journal of Experimental Marine Biology and Ecology 138: 227–246.

    Article  Google Scholar 

  • Clavier, J., M. D. Castets, T. Bastian, C. Hily, G. Boucher & L. Chauvaud, 2009. An amphibious mode of life in the intertidal zone: aerial and underwater contribution of Chthamalus montagui to CO2 fluxes. Marine Ecology Progress Series 375: 185–194.

    Article  CAS  Google Scholar 

  • Daniel, M. J., 1982. A comparative study of the pattern of ventilation movements in Hong Kong limpets. In Morton, B. & C.K. Tseng (eds), The Marine Fauna and Ora of Hong Kong and Southern China Hong Kong, Vol. 2. Hong Kong University Press, Hong Kong: 837–847.

  • Das, S. & G. Seshappa, 1948. A contribution to the biology of Patella: on population distribution and sex-proportions in Patella vulgata Linnaeus at Cullercoats, England, vol 117. Wiley, New York: 653–662.

  • Davies, P. S., 1967a. Physiological ecology of Patella. I. The effect of environmental accumulation on metabolic rate. Journal of the Marine Biological Association of the United Kingdom 46: 647–658.

    Article  Google Scholar 

  • Davies, P. S., 1967b. Physiological ecology of Patella. II. Effect of environmental acclimation on the metabolic rate. Journal of the Marine Biological Association of the United Kingdom 47: 61–74.

    Article  Google Scholar 

  • Della Santina, P., G. Santini & G. Chelazzi, 1995. Factors affecting variability of foraging excursions in a population of the limpet Patella vulgata (Mollusca, Gastropoda). Marine Biology 122: 265–270.

    Google Scholar 

  • Denny, M. W. & S. D. Gaines, 2007. Encyclopedia of tidepools and rocky shores. University of California Press, Berkeley.

    Google Scholar 

  • Espinosa, F., J. M. Guerra-García, D. Fa & J. C. García-Gómez, 2006. Effects of competition on an endangered limpet Patella ferruginea (Gastropoda: Patellidae): implications for conservation. Journal of Experimental Marine Biology and Ecology 330: 482–492.

    Article  Google Scholar 

  • Evans, R. G., 1948. The lethal temperatures of some common British littoral molluscs. Journal of Animal Ecology 17: 165–173.

    Article  Google Scholar 

  • Fenger, T., D. Surge, B. Schöne & N. Milner, 2007. Sclerochronology and geochemical variation in limpet shells (Patella vulgata): a new archive to reconstruct coastal sea surface temperature. Geochemistry, Geophysics, Geosystems 8: Q07001.

    Article  Google Scholar 

  • Gazeau, F., C. Quiblier, J. Jansen, J. P. Gattuso, J. J. Middelburg & C. H. R. Heip, 2007. Impact of elevated CO2 on shellfish calcification. Geophysical Research Letters 34: L07603.

    Article  Google Scholar 

  • Gray, D. & E. Naylor, 1996. Foraging and homing behaviour of the limpet, Patella vulgata: a geographical comparison. Journal of Molluscan Studies 62: 121–124.

    Article  Google Scholar 

  • Hartnoll, R. & J. Wright, 1977. Foraging movements and homing in the limpet Patella vulgata L. Animal Behaviour 25: 806–810.

    Article  Google Scholar 

  • Hawkins, S. & R. Hartnoll, 1982. The influence of barnacle cover on the numbers, growth and behaviour of Patella vulgata on a vertical pier. Journal of the Marine Biological Association of the United Kingdom 62: 855–867.

    Article  Google Scholar 

  • Hawkins, S. J. & R. Hartnoll, 1983. Grazing of intertidal algae by marine invertebrates. Oceanography and Marine Biology 21: 195–282.

    Google Scholar 

  • Houlihan, D. & J. Newton, 1978. Respiration of Patella vulgata on the shore. In: McLusky, D. S. & A. J. Berry (eds), 12th European Symposium on Marine Biology Stirling, Scotland: 39–46.

  • Iwasaki, K., 1999. Short- and long-term movements of the patellid limpet Patella flexuosa within gaps in intertidal mussel beds. Journal of Molluscan Studies 65: 295–301.

    Article  Google Scholar 

  • Jacques, T. & M. Pilson, 1980. Experimental ecology of the temperate scleractinian coral Astrangia danae I. Partition of respiration, photosynthesis and calcification between host and symbionts. Marine Biology 60: 167–178.

    Article  CAS  Google Scholar 

  • Koroleff, F., 1970. Direct determination of ammonia in natural waters as indophenol blue. Paper presented at the International council for the exploration of the sea, Copenhagen.

  • Lejart, M., J. Clavier, L. Chauvaud & C. Hily, 2012. Respiration and calcification of Crassostrea gigas: contribution of an intertidal invasive species to coastal ecosystem CO2 fluxes. Estuaries and Coasts 35: 622–632.

    Article  CAS  Google Scholar 

  • Little, C., 1989. Factors governing patterns of foraging activity in littoral marine herbivorous molluscs. Journal of Molluscan Studies 55: 273–284.

    Article  Google Scholar 

  • Little, C., G. A. Williams & C. D. Trowbridge, 2009. The biology of rocky shores. Oxford University Press, New York.

  • Lutz, R. A. & G. R. Clark, 1984. Seasonal and geographic variation in the shell microstructure of a salt-marsh bivalve (Geukensia demissa (Dillwyn)). Journal of Marine Research 42: 943–956.

    Article  Google Scholar 

  • Marshall, D. J. & C. D. McQuaid, 1991. Metabolic rate depression in a marine pulmonate snail: pre-adaptation for a terrestrial existence? Oecologia 88: 274–276.

    Article  Google Scholar 

  • Marshall, D. J. & C. D. McQuaid, 1992. Comparative aerial metabolism and water relations of the intertidal limpets Patella granularis L. (Mollusca: Prosobranchia) and Siphonaria oculus Kr. (Mollusca: Pulmonata). Physiological Zoology 65: 1040–1056.

    Google Scholar 

  • McConnaughey, T. A. & D. P. Gillikin, 2008. Carbon isotopes in mollusk shell carbonates. Geo-Marine Letters 28: 287–299.

    Article  CAS  Google Scholar 

  • Newell, R. C., 1979. Biology of intertidal animals. Marine Ecological Surveys, Faversham, Kent.

    Google Scholar 

  • Obermüller, B. E., S. A. Morley, M. S. Clark, D. K. A. Barnes & L. S. Peck, 2011. Antarctic intertidal limpet ecophysiology: a winter–summer comparison. Journal of Experimental Marine Biology and Ecology 403: 39–45.

    Article  Google Scholar 

  • Pannella, G. & C. MacClintock, 1968. Biological and environmental rhythms reflected in molluscan shell growth. Journal of Paleontology 42: 64–80.

    Google Scholar 

  • Pierrot, D., E. Lewis & D. Wallace, 2006. MS Excel program developed for CO2 system calculations ORNL/CDIAC-105, US Department of Energy. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, Oak Ridge, Tennessee.

  • Plagányi, E. & G. M. Branch, 2000. Does the limpet Patella cochlear fertilize its own algal garden? Marine Ecology Progress Series 194: 113–122.

    Article  Google Scholar 

  • Ribeiro, P. A., R. Xavier, A. M. Santos & S. J. Hawkins, 2009. Reproductive cycles of four species of Patella (Mollusca: Gastropoda) on the northern and central Portuguese coast. Journal of the Marine Biological Association of the United Kingdom 89: 1215–1221.

    Article  Google Scholar 

  • Roy, R. N., L. N. Roy, K. M. Vogel, C. Porter-Moore, T. Pearson, C. E. Good, F. J. Millero & D. M. Campbell, 1993. The dissociation constants of carbonic acid in seawater at salinities 5 to 45 and temperatures 0 to 45 C. Marine Chemistry 44: 249–267.

    Article  CAS  Google Scholar 

  • Santini, G., R. C. Thompson, C. Tendi, S. J. Hawkins, R. G. Hartnoll & G. Chelazzi, 2004. Intra-specific variability in the temporal organisation of foraging activity in the limpet Patella vulgata. Marine Biology 144: 1165–1172.

    Article  Google Scholar 

  • Santini, G., G. A. Williams & G. Chelazzi, 2000. Assessment of factors affecting heart rate of the limpet Patella vulgata on the natural shore. Marine Biology 137: 291–296.

    Article  Google Scholar 

  • Schöne, B. R., D. L. Rodland, A. Wehrmann, B. Heidel, W. Oschmann, Z. Zhang, J. Fiebig & L. Beck, 2007. Combined sclerochronologic and oxygen isotope analysis of gastropod shells (Gibbula cineraria, North Sea): life-history traits and utility as a high-resolution environmental archive for kelp forests. Marine Biology 150: 1237–1252.

    Article  Google Scholar 

  • Segal, E., 1956. Microgeographic variation as thermal acclimation in an intertidal mollusc. The Biological Bulletin 111: 129–152.

    Article  Google Scholar 

  • Silva, A. C. F., S. J. Hawkins, D. M. Boaventura & R. C. Thompson, 2008. Predation by small mobile aquatic predators regulates populations of the intertidal limpet Patella vulgata (L.). Journal of Experimental Marine Biology and Ecology 367: 259–265.

    Article  Google Scholar 

  • Smith, S. & G. Key, 1975. Carbon dioxide and metabolism in marine environments. Limnology and Oceanography 20: 493–495.

    Article  CAS  Google Scholar 

  • Sokal, R. R. & F. J. Rohlf, 1981. Biometry: the principles and practice of statistics in biological research, 2nd ed. Freeman, New York.

    Google Scholar 

  • Solorzano, L., 1969. Determination of ammonia in natural waters by the phenolhypochlorite method. Limnology and Oceanography 14: 799–801.

    Article  CAS  Google Scholar 

  • Somero, G. N., 2002. Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs of living. Integrative and Comparative Biology 42: 780–789.

    Article  PubMed  Google Scholar 

  • Southward, A., 1958. The zonation of plants and animals on rocky sea shores. Biological Reviews 33: 137–177.

    Google Scholar 

  • Underwood, A. J., 1973. Studies on zonation of intertidal prosobranch molluscs in the Plymouth Region. Journal of Animal Ecology 42: 353–372.

    Article  Google Scholar 

  • Vermeij, G. J., 1972. Intraspecific shore-level size gradients in intertidal molluscs. Ecology 53: 693–700.

    Article  Google Scholar 

  • Vermeij, G. J., 1973. Morphological patterns in high-intertidal gastropods: adaptive strategies and their limitations. Marine Biology 20: 319–346.

    Article  Google Scholar 

  • White, T. J., 1968. Metabolic activity and glycogen stores of two distinct populations of Acmaea scabra. Veliger 11: 102–104.

    Google Scholar 

  • Wright, J. & R. Hartnoll, 1981. An energy budget for a population of the limpet Patella vulgata. Journal of the Marine Biological Association of the United Kingdom 61: 627–646.

    Article  Google Scholar 

  • Yonge, C. M., 1947. The pallial organs in the aspidobranch Gastropoda and their evolution throughout the Mollusca. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences:443-518.

  • Zar, J. H., 2010. Biostatistical Analysis, 5th ed. Prentice hall, New Jersey.

    Google Scholar 

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Acknowledgments

This study was supported by the ANR CHIVAS (Chimie des Valves de la Coquille Saint Jacques Européenne) programme. We are grateful to MAREL Iroise for sea surface temperature (http://www-iuem.univ-brest.fr/observatoire/marel.php. Data were collected and processed according to the terms of the framework agreement jointly signed by IFREMER, CNRS (INSU) and UBO (on behalf of IUEM) (no. 11/2-210922). We are grateful to SOMLIT group for providing nutrients data and gas-analyser calibration (http://somlit.epoc.u-bordeaux1.fr/fr/). We thank the IUEM observatory for help with species identification, and we thank M. Franzetti for help with calculations.

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  1. Laboratoire des Sciences de l’Environnement Marin (LEMAR) (UMR CNRS 6539), Institut Universitaire Européen de la Mer (IUEM), rue Dumont d’Urville, 29280, Plouzané, France

    Morgana Tagliarolo, Laurent Chauvaud & Jacques Clavier

  2. IUEM Observatory UMS 3113 CNRS, Institut Universitaire Européen de la Mer, rue Dumont d’Urville, 29280, Plouzané, France

    Jacques Grall

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  1. Morgana Tagliarolo
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  2. Jacques Grall
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  3. Laurent Chauvaud
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  4. Jacques Clavier
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Correspondence to Morgana Tagliarolo.

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Handling editor: Pierluigi Viaroli

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Tagliarolo, M., Grall, J., Chauvaud, L. et al. Aerial and underwater metabolism of Patella vulgata L.: comparison of three intertidal levels. Hydrobiologia 702, 241–253 (2013). https://doi.org/10.1007/s10750-012-1328-1

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