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Microscale aspects in the diet of the limpet Patella vulgata L.

Published online by Cambridge University Press:  17 April 2015

Gauthier Schaal  and
Jacques Grall
Gauthier Schaal*
Affiliation:
Laboratoire des Sciences de l'Environnement Marin, UMR 6539 CNRS, Institut Universitaire Européen de la Mer, Université de Bretagne Occidentale, Place Copernic. 29280 Plouzané, France
Jacques Grall
Affiliation:
Observatoire du Domaine Côtier FR 3113, Institut Universitaire Européen de la Mer, Université de Bretagne Occidentale, Place Copernic, 29280 Plouzané, France
*
Correspondence should be addressed to: G. Schaal, Laboratoire des Sciences de l'Environnement Marin, UMR 6539 CNRS, Institut Universitaire Européen de la Mer, Université de Bretagne Occidentale, Place Copernic. 29280 Plouzané, France email: [email protected]
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Abstract

The limpet Patella vulgata is a key species of northern Atlantic rocky shore-associated communities, and is commonly considered to be important in regulating populations of canopy-forming Ascophyllum nodosum, through consumption of propagules and young recruits. Although P. vulgata is usually regarded as a non-selective epilithic biofilm grazer, a role in the collapse of established A. nodosum through grazing of adult plants has been repeatedly suggested. Factors controlling the preference of P. vulgata for epilithic biofilm or adult algae are still not clearly established. Here, we test the hypothesis that the diet of P. vulgata is mainly driven by the local availability of food sources. Limpets were sampled along the first 6 metres of an A. nodosum bed–bare rock gradient. Stable isotope ratios of their muscle tissue and digestive glands were measured. The contribution of A. nodosum to the diet of limpets was the highest in the immediate vicinity of macroalgae beds, which confirmed our initial hypothesis. However, the contribution of epilithic biofilm did not match our hypothesis, being the lowest for limpets colonizing bare rock. Instead, these limpets relied on a wide array of sources, including ephemeral green algae, biofilm and drifting A. nodosum fragments. Overall, our results indicate that A. nodosum can be readily grazed by limpets, which challenges the hypothesis that these macroalgae dominate rocky shores due to the absence of strong top-down control exerted by herbivores. Our results also highlight the need to consider the small spatial scale to understand the dynamic of herbivore–algae interactions in natural environments.

Keywords

Patella vulgataAscophyllum nodosumrocky shorestable isotopesspatial variability
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 95 , Issue 6 , September 2015 , pp. 1155 - 1162
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

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References

REFERENCES

Bode, A., Alvarez-Ossorio, M.T. and Varela, M. (2006) Phytoplankton and macrophyte contributions to littoral food webs in the Galician upwelling estimated from stable isotopes. Marine Ecology Progress Series 318, 89–102.CrossRefGoogle Scholar
Bodin, N., Le Loc'h, F. and Hily, C. (2007) Effect of lipid removal on carbon and nitrogen stable isotope ratios in crustacean tissues. Journal of Experimental Marine Biology and Ecology 341, 168–175.CrossRefGoogle Scholar
Bruno, J.F. and Bertness, M.D. (2001) Habitat modification and facilitation in marine benthic communities. In Bertness, M.D., Gaines, S.D. and Hay, M.E. (eds) Marine community ecology. Sunderland, MA: Sinauer Associates, pp. 201–218.Google Scholar
Bustamante, R.H. and Branch, G.M. (1996) The dependence of intertidal consumers on kelp-derived organic matter on the west coast of South Africa. Journal of Experimental Marine Biology and Ecology 196, 1–28.CrossRefGoogle Scholar
Camus, P.A., Daroch, K. and Opazo, L.F. (2008) Potential for omnivory and apparent intraguild predation in rocky intertidal herbivore assemblages from northern Chile. Marine Ecology Progress Series 361, 35–45.CrossRefGoogle Scholar
Coleman, R.A., Underwood, A.J., Benedetti-Cecchi, L., Aberg, P., Arenas, F., Arrontes, J., Castro, J., Hartnoll, R.G., Jenkins, S.R., Paula, P., Della Santina, P. and Hawkins, S.J. (2006) A continental scale evaluation of the role of limpet grazing on rocky shores. Oecologia 147, 556–564.CrossRefGoogle ScholarPubMed
Davies, A.J., Johnson, M.P. and Maggs, C.A. (2007) Limpet grazing and the loss of Ascophyllum nodosum canopies on decadal time scales. Marine Ecology Progress Series 339, 131–141.CrossRefGoogle Scholar
Davies, A.J., Johnson, M.P. and Maggs, C.A. (2008) Subsidy by Ascophyllum nodosum increases growth rate and survivorship of Patella vulgata. Marine Ecology Progress Series 366, 43–48.CrossRefGoogle Scholar
De Niro, M.J. and Epstein, S. (1977) Mechanism of isotope carbon fractionation associated with lipid synthesis. Science 197, 261–263.CrossRefGoogle ScholarPubMed
Evans, M.R. and Williams, G.A. (1991) Time partitioning of foraging in the limpet Patella vulgata. Journal of Animal Ecology 60, 563–575.CrossRefGoogle Scholar
Golléty, C., Migné, A. and Davoult, D. (2008) Benthic metabolism on a sheltered rocky shore: role of the canopy in the carbon budget. Journal of Phycology 44, 1146–1153.CrossRefGoogle ScholarPubMed
Golléty, C., Riera, P. and Davoult, D. (2010) Complexity of the food web structure of the Ascophyllum nodosum zone evidenced by a δ13C and δ15N study. Journal of Sea Research 64, 304–312.CrossRefGoogle Scholar
Guest, M.A. and Connolly, R.M. (2004) Fine-scale movement and assimilation of carbon in saltmarsh and mangrove habitat by resident animals. Aquatic Ecology 38, 599–609.CrossRefGoogle Scholar
Hawkins, S.J. and Hartnoll, R.G. (1983) Grazing on intertidal algae by marine invertebrates. Oceanography and Marine Biology: an Annual Review 21, 195–282.Google Scholar
Hawkins, S.J., Watson, D.C., Hill, A.S., Harding, S.P., Kyriakides, M.A., Hutchinson, S. and Norton, T.A. (1989) A comparison of feeding mechanisms in microphagous, herbivorous, intertidal, prosobranchs in relation to resource partitioning. Journal of Molluscan Studies 55, 151–165.CrossRefGoogle Scholar
Hill, A.S. and Hawkins, S.J. (1991) Seasonal and spatial variation of epilithic micro algal distribution and abundance and its ingestion by Patella vulgata on a moderately exposed rocky shore. Journal of the Marine Biological Association of the United Kingdom 71, 403–423.CrossRefGoogle Scholar
Jenkins, S.R., Hawkins, S.J. and Norton, T.A. (1999) Direct and indirect effects of a macroalgal canopy and limpet grazing in structuring a sheltered inter-tidal community. Marine Ecology Progress Series 188, 81–92.CrossRefGoogle Scholar
Jenkins, S.R., Moore, P., Burrows, M.T., Garbary, D.J., Hawkins, S.J., Ingólfsson, A., Sebens, K.P., Snelgrove, P.V.R., Wethey, D.S. and Woodin, S.A. (2008) Comparative ecology of north Atlantic shores: do differences in players matter for process? Ecology 89, S3–S23.CrossRefGoogle ScholarPubMed
Khailov, K.M. and Burlakova, Z.P. (1969) Release of dissolved organic matter by marine seaweeds and distribution of their total organic production to inshore communities. Limnology and Oceanography 14, 521–527.CrossRefGoogle Scholar
Kon, K., Kurokura, H. and Hayashizaki, K. (2007) Role of microhabitats in food webs of benthic communities in a mangrove forest. Marine Ecology Progress Series 340, 55–62.CrossRefGoogle Scholar
Le Hir, M. and Hily, C. (2005) Macrofaunal diversity and habitat structure in intertidal boulder fields. Biodiversity and Conservation 14, 233–250.CrossRefGoogle Scholar
Le Roux, A. (2005) Les patelles et la régression des algues brunes dans le Morbihan. Penn ar Bed 192, 1–22.Google Scholar
Lorenzen, S. (2007) The limpet Patella vulgata L. at night in air: effective feeding on Ascophyllum nodosum monocultures and stranded seaweeds. Journal of Molluscan Studies 73, 267–274.CrossRefGoogle Scholar
McCutchan, J.H. Jr, Lewis, W.M. Jr, Kendall, C. and McGrath, C.C. (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulphur. Oikos 102, 378–390.CrossRefGoogle Scholar
McGuiness, K.A. and Underwood, A.J. (1986) Habitat structure and the nature of communities on intertidal boulders. Journal of Experimental Marine Biology and Ecology 104, 97–123.CrossRefGoogle Scholar
McIntyre, P.B. and Flecker, A.S. (2006) Rapid turnover of tissue nitrogen of primary consumers in tropical freshwaters. Oecologia 148, 12–21.CrossRefGoogle ScholarPubMed
Noël, L.M.-L.J., Hawkins, S.J., Jenkins, S.R. and Thompson, R.C. (2009) Grazing dynamics in intertidal rockpools: connectivity of microhabitats. Journal of Experimental Marine Biology and Ecology 370, 9–17.CrossRefGoogle Scholar
Parnell, A.C., Inger, R., Bearhop, S. and Jackson, A.L. (2010) Source partitioning using stable isotopes: coping with too much variation. PloS ONE 5, e9672.CrossRefGoogle ScholarPubMed
Pavia, H. and Toth, G.B. (2000) Inducible chemical resistance to herbivory in the brown seaweed Ascophyllum nodosum. Ecology 81, 3212–3225.CrossRefGoogle Scholar
Post, D.M., Layman, C.A., Arrington, D.A., Takimoto, G., Quattrochi, J. and Montaña, C.G. (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152, 179–189.CrossRefGoogle Scholar
Raikow, D.F. and Hamilton, S.K. (2001) Bivalve diets in a Midwestern U.S. stream: a stable isotope enrichment study. Limnology and Oceanography 46, 514–522.CrossRefGoogle Scholar
Richoux, N.B. and Ndhlovu, R.T. (in press) Temporal variability in the isotopic niches of rocky shore grazers and suspension-feeders. Marine Ecology.Google Scholar
Riera, P., Escaravage, C. and Leroux, C. (2009) Trophic ecology of the rocky shore community associated with the Ascophyllum nodosum zone (Roscoff, France): a δ13C vs δ15N investigation. Estuarine, Coastal and Shelf Science 81, 143–148.CrossRefGoogle Scholar
Sarà, G., De Pirro, M., Romano, C., Rumolo, P., Sprovieri, M. and Mazzola, A. (2007) Sources of organic matter for intertidal consumers on Asophyllum-shores (SW Iceland): a multi-stable isotope approach. Helgoland Marine Research 61, 297–302.CrossRefGoogle Scholar
Schaal, G., Riera, P. and Leroux, C. (2009) Trophic significance of the kelp Laminaria digitata (Lamour.) for the associated food web: a between-sites comparison. Estuarine, Coastal and Shelf Science 85, 565–572.CrossRefGoogle Scholar
Schaal, G., Riera, P. and Leroux, C. (2011) Microscale variations of food web functioning within a rocky shore invertebrate community. Marine Biology 158, 623–630.CrossRefGoogle Scholar
Southward, A.J. and Southward, E.C. (1978) Recolonization of rocky shores in Cornwall after use of toxic dispersants to clean up the Torrey Canyon spill. Journal of the Fisheries Research Board of Canada 35, 682–706.CrossRefGoogle Scholar
Steneck, R.S. and Watling, L. (1982) Feeding capabilities and limitation of herbivorous molluscs: a functional group approach. Marine Biology 68, 299–319.CrossRefGoogle Scholar
Thompson, R.C., Norton, T.A. and Hawkins, S.J. (2004) Physical stress and biological control regulate the producer-consumer balance in intertidal biofilms. Ecology 85, 1372–1382.CrossRefGoogle Scholar
Tieszen, L.L., Boutton, T.W., Tesdahl, K.G. and Slade, N.A. (1983) Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57, 32–37.CrossRefGoogle ScholarPubMed
Vadas, R.L., Wright, W.A. and Miller, S.L. (1990) Recruitment of Ascophyllum nodosum: wave action as a source of mortality. Marine Ecology Progress Series 61, 263–272.CrossRefGoogle Scholar
Vanderklift, M.A. and Ponsard, S. (2003) Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136, 169–182.CrossRefGoogle ScholarPubMed
Vander Zanden, M.J. and Rasmussen, J.B. (2001) Variation in δ15N and δ13C trophic fractionation: Implications for aquatic food web studies. Limnology and Oceanography 46, 2061–2066.CrossRefGoogle Scholar
Wenne, R. and Polak, L. (1989) Lipid composition and storage in the tissues of the bivalve, Macoma balthica. Biochemical Systematics and Ecology 17, 583–587.CrossRefGoogle Scholar