Skip to main content
SpringerLink
Log in

Feast or famine for intertidal grazing molluscs: a mis-match between seasonal variations in grazing intensity and the abundance of microbial resources

  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Distinct seasonal variations in the abundance of photosynthetic microbiota and limpet grazing intensity were recorded at Port St Mary, Isle of Man between January 1994 and June 1996. Microbial abundance was negatively correlated with insolation stress, while grazing intensity was positively correlated with sea and air temperature. These patterns result in a mis-match between the supply of and the demand for microbial resources with maximal grazing intensity during the summer and autumn, but maximal microbial standing stock during the winter and early spring. The importance of top-down control of microbial assemblages by grazing was demonstrated by experimental exclusion of limpets during autumn 1993. This resulted in a four-fold increase in the abundance of cyanobacteria within 6 days, followed by a more gradual proliferation of ephemeral algae during the next 4 weeks. The abundance of diatoms remained relatively constant and was not influenced by the removal of grazers at this time of year. The influence of microbial resource availability on the growth and mortality of limpets was examined using experimental enclosures of differing densities of either Patella vulgata or P. depressa. After 6 months, there were significant relationships between grazer density and both mortality and growth with increased mortality and reduced growth for P. vulgata at increased densities, and reduced growth for P. depressa at increased densities. Hence, the availability of microbial resources may also influence the biomass of grazers on rocky shores from the bottom upwards. A conceptual model is presented which describes seasonal and annual variations in microbial resources and grazing intensity and their potential consequences for other shore dwellers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aleem, A. A., 1950. Distribution and ecology of British marine littoral diatoms. J. Ecol. 38: 75–106.

    Google Scholar 

  • Bowman, R. S. & J. R. Lewis, 1977. Annual fluctuations in the recruitment of Patella vulgata L. J. mar. biol. Ass. U.K. 57: 793–815.

    Google Scholar 

  • Boyden, C. R. & J. R. Zeldis, 1979. Preliminary observations using an attached microphone sensor to study feeding behaviour of an intertidal limpet. Estuar. Coast. mar. Sci. 9: 759–769.

    Google Scholar 

  • Branch, G. M., 1981. The biology of limpets: physical factors, energy flow and ecological interactions. Oceanogr. mar. biol. Ann. Rev. 19: 235–379.

    Google Scholar 

  • Bustamante, R. H., G. M. Branch, S. Eekhout, B. Robertson, P. Zoutendyk, M. Schleyer, A. Dye, N. Hanekom, D. Keats, M. Jurd & C. McQuaid, 1995. Gradients of intertidal primary productivity around the coast of South Africa and their relationships with consumer biomass. Oecologia 102: 189–201.

    Google Scholar 

  • Castenholz, R. W., 1963. An experimental study of the vertical distribution of littoral marine diatoms. Limnol. Oceanogr. 8: 450–462.

    Google Scholar 

  • Coleman, R. A., J. D. Goss-Custard, S. E. A. LeV. Dit Durell & S. J. Hawkins, 1999. Limpet Petella spp. consumption by oystercatchers Haematopus ostralegus: a preference for solitary prey items. Mar. Ecol. Prog. Ser. 183: 253–261.

    Google Scholar 

  • Crisp, D. J., 1974. Factors influencing the settlement of marine invertebrate larvae. In Grant, P. T. & A. M. Mackie (eds), Chemoreception in Marine Organisms. Academic Press, London: 177–265.

    Google Scholar 

  • Dye, A. H. & R. A. White, 1991. Intertidal microalgal production and molluscan herbivory in relation to season and elevation on two rocky shores on the east coast of Southern Africa. S. Afr. J. mar. Sci. 11: 483–489.

    Google Scholar 

  • Farrell, T. M., 1988. Community stability: effects of limpet removal and reintroduction in a rocky intertidal community. Oecologia 75: 190–197.

    Google Scholar 

  • Fielding, P. J., K. S. J. Damstra & G. M. Branch, 1988. Benthic diatom biomass, production and sediment chlorophyll in Langebaan lagoon, South Africa. Estuar. coast. shelf Sci. 27: 413–426.

    Google Scholar 

  • Fuji, A., H. Watanabe, K. Ogura, T. Noda & S. Goshima, 1991. Abundance and productivity of microphytobenthos on a rocky shore in southern Hokkaido. Bull. Fac. Fish. Hokkaido Univ. 42: 136–146.

    Google Scholar 

  • Grubb, V. M., 1936. Marine ecology and the exposure factor at Peveril Point, Dorset. J. Ecol. 24: 392.

    Google Scholar 

  • Hartnoll, R. G. & S. J. Hawkins, 1985. Patchiness and Fluctuations on Moderately Exposed Rocky Shores. Ophelia 24: 53–64.

    Google Scholar 

  • Hawkins, S. J., 1981. The Influence of Season and Barnacles on the Algal Colonization of Patella-Vulgata Exclusion Areas.J. mar. biol. Ass. U.K. 61: 1–15.

    Google Scholar 

  • Hawkins, S. J. & R. G. Hartnoll, 1983. Grazing of intertidal algae bymarine invertebrates. Oceanogr. mar. Biol. Ann. Rev. 21: 195–285.

    Google Scholar 

  • Hawkins, S. J., R. G. Hartnoll, J. M. Kain, & T. A. Norton, 1992. Plant-animal interactions on hard substrata in the Northeast Atlantic. In John, D. M., Hawkins, S. J. & Price, J. H. (eds), Plant-Animal Interactions in the Marine Benthos. Oxford University Press, Oxford, U.K.: 1–32.

    Google Scholar 

  • Hawkins, S. J., D. C. Watson, A. S. Hill, S. P. Harding, M. A. Kyriakides, S. Hutchinson & T. A. Norton, 1989. A comparison of feeding mechanisms in microphagous, herbivorous, intertidal, prosobranchs in relation to resource partitioning. J. Mollusc. Stud. 55: 151–165.

    Google Scholar 

  • Hill, A. S. & S. J. Hawkins, 1990. An investigation of methods for sampling microbial films on rocky shores. J. mar. biol. Ass. U.K. 70: 77–88.

    Google Scholar 

  • Hill, A. S. & S. J. Hawkins, 1991. Seasonal and spatial variation of epilithic microalgae distribution and abundance and its ingestion by Patella vulgata on a moderately exposed rocky shore. J. mar. biol. Ass. U.K. 71: 403–423.

    Google Scholar 

  • Huang, R. & A. D. Boney, 1984. Growth interactions between littoral diatoms and juvenile marine algae. J. exp. mar. Biol. Ecol. 81: 21–45.

    Google Scholar 

  • Jenkins, S. R., F. Arenas, J. Arrontes, J. Bussell1, J. Castro, R. A. Coleman, S. J. Hawkins, S. Kay, B. Martínez, J. Oliveros, M. F. Roberts, R. C. Thompson & R. G. Hartnoll, In Press. Seasonal variation in limpet grazing activity and microalgal abundance over a European scale. Mar. Ecol. Prog. Ser.

  • Jernakoff, P., 1985. Interactions between the limpet Patelloida latistrigata and algae on an intertidal rock platform. Mar. Ecol. Prog. Ser. 23: 71–78.

    Google Scholar 

  • Karr, J. R., M. Dionne & I. J. Schlosser, 1992. Bottom-up versus top-down regulation of vertebrate populations: lessons from birds and fish. In Hunter, M. D., T. Ohgushi & P. W. Price (eds), Effects of resource distribution on animal plant interactions. Academic Press, London: 243–286.

    Google Scholar 

  • Kristensen, E., 1993. An In situ method for measuring the primary productivity and standing crop of the epilithic periphyton community in lentic systems. Estuar. coast. shelf Sci. 36: 565–586.

    Google Scholar 

  • Lamontagne, I., A. Cardinal & L. Fortier, 1989. Environmental forcing versus endogenous control of photosynthesis in intertidal epilithic microalgae. Mar. Ecol. Prog. Ser. 51: 1–2.

    Google Scholar 

  • Lock, M. A., 1993. Attached microbial communities in rivers. In Ford, T. A. (ed.), Aquatic Microbiology. Blackwells, Oxford: 113–138.

    Google Scholar 

  • MacLulich, J. H., 1987. Variations in the density and variety of intertidal epilithic microflora. Mar. Ecol. Prog. Ser. 40: 285–293.

    Google Scholar 

  • Mak, Y. M. & G. A. Williams, 1999. Littorinids control high intertidal biofilm abundance on tropical, Hong Kong rocky shores. J. exp. mar. Biol. Ecol. 233: 81–94.

    Google Scholar 

  • Marshall, D. J. & C. D. McQuaid, 1994. Seasonal and Diel Variations of in-Situ Heart-Rate of the Intertidal Limpet Siphonaria-Oculus Kr (Pulmonata). J. exp. mar. Biol. Ecol. 179: 1–9.

    Google Scholar 

  • Menge, B. A., B. A. Daley, J. Lubchenco, E. Sanford, E. Dahlhoff, P. M. Halpin, G. Hudson & J. L. Burnaford, 1999. Top-down and bottom-up regulation of New Zealand rocky intertidal communities. Ecol. Monogr. 69: 297–330.

    Google Scholar 

  • Menge, B. A., B. A. Daley, P. A. Wheeler, E. Dahlhoff, E. Sanford & P. T. Strub, 1997. Benthic-pelagic links and rocky intertidal communities: bottom-up effects on top-down control? Proc. natn. Acad. Sci. U.S.A. 94: 14530–14535.

    Google Scholar 

  • Nagarkar, S., 1998. New records of marine cyanobacteria from rocky shores of Hong Kong. Bot. mar. 41: 527–542.

    Google Scholar 

  • Newell, R. C. & G. M. Branch, 1980. The influence of temperature on the maintenance of metabolic energy balance in marine invertebrates. Adv. mar. Biol. 17: 329–396.

    Google Scholar 

  • Nicotri, M. E., 1977. Grazing effects of four marine intertidal herbivores on the microflora. Ecology 58: 1020–1032.

    Google Scholar 

  • Ogden, N. B., J. C. Ogden & I. A. Abbott, 1989. Distribution, abundance and food of sea urchins on a leeward Hawaiian reef. Bull. mar. Sci. 45: 539–549.

    Google Scholar 

  • Orton, J. H., A. J. Southward & J. M. Dodd, 1956. Studies on the biology of limpets II. The breeding of Patella vulgata L. in Britain. J. mar. biol. Ass. U.K. 35: 149–176.

    Google Scholar 

  • Parsons, T. R., M. Takahashi & B. Hargrave, 1984. Biological oceanographic processes. Butterworth-Heinemann. Oxford, U.K.: 332 pp.

    Google Scholar 

  • Santini, G., G. Chelazzi & P. Della Santina, 1995. Size-related functional and energetic constraints in the foraging of the limpet Patella vulgata (Mollusca, Gastropoda). Funct. Ecol. 9: 551–558.

    Google Scholar 

  • Sokal, R. R. & F. J. Rohlf, 1995. Biometry. Freeman & Co. New York: 850 pp.

    Google Scholar 

  • Sommer, U., 1999. The susceptibility of benthic microalgae to periwinkle (Littorina littorea, Gastropoda) grazing in laboratory experiments. Aquat. Bot. 63: 11–21.

    Google Scholar 

  • Southward, A. J., 1953. The ecology of some rocky shores in the south of the Isle of Man. Proc. Trans. Liverpool Biol. Soc. 59: 1–50.

    Google Scholar 

  • Southward, A. J., 1964. Limpet grazing and the control of vegetation on rocky shores. In Crisp, D. J. (ed.), Grazing in Terrestrial and Marine Environments. Blackwell Scientific Publications, Oxford: 265–273.

    Google Scholar 

  • Southward, A. J. & E. C. Southward, 1978. Recolonisation of rocky shores in Cornwall after use of toxic dispersants to clean up the Torrey Canyon spill. J. Fish. Res. Bd Can. 35: 682–706.

    Google Scholar 

  • Stahl, L. J., H. Van Gemerded & W. E. Krumbein, 1985. Structure and development of benthic marine microbial mat. Fems Microbiol. Ecol. 31: 111–125.

    Google Scholar 

  • Steneck, R. S. & L. Watling, 1982. Feeding capabilities and limitation of herbivorous molluscs: a functional group approach. Mar. Biol. 68: 299–319.

    Google Scholar 

  • Thompson, R. C., 1996. The Ecology of Epilithic Microalgae on Manx Shores. School of Biological Sciences. Liverpool University, Liverpool: 244 pp.

    Google Scholar 

  • Thompson, R. C., L. E. Johnson & S. J. Hawkins, 1997. A method for spatial and temporal assessment of gastropod grazing intensity in the field: the use of radula scrapes on wax surfaces. J. exp. mar. Biol. Ecol. 218: 63–76.

    Google Scholar 

  • Thompson, R. C., S. J. Hawkins & T. A. Norton, 1998. The influence of epilithic microbial films on the settlement of Semibalanus balanoides cyprids-a comparison between laboratory and field experiments. Hydrobiologia 375/376 (Dev. Hydrobiol. 132): 203–216.

    Google Scholar 

  • Thompson, R. C., M. L. Tobin, S. J. Hawkins & T. A. Norton, 1999. Problems in extraction and spectrophotometric determination of chlorophyll from epilithic microbial biofilms: towards a standard method. J. mar. biol. Ass. U.K. 79: 551–558.

    Google Scholar 

  • Underwood, A. J., 1979. The ecology of intertidal gastropods. Adv. mar. Biol. 16: 111–210.

    Google Scholar 

  • Underwood, A. J., 1984a. Microalgal food and the growth of the intertidal gastropods Nerita atramentosa Reeve and Bembicium nanum (Lamarck) at four heights on a shore. J. exp. mar. Biol. Ecol. 79: 277–291.

    Google Scholar 

  • Underwood, A. J., 1984b. Vertical and seasonal patterns in competition for microalgae between intertidal gastropods. Oecologia 64: 211–222.

    Google Scholar 

  • Underwood, A. J., 1984c. The vertical distribution and seasonal abundance of intertidal microalgae on a rocky shore in New South Wales. J. exp. mar. Biol. Ecol. 78: 199–220.

    Google Scholar 

  • Underwood, A. J., M. G. Chapman, S. A. Richards & M. B. Sage, 1997. GMAV for Windows. Institute of Marine ecology, Sydney.

    Google Scholar 

  • Wahl, M., 1989. Marine epibiosis. I. Fouling and antifouling: Some basic aspects. Mar. Ecol. Prog. Ser. 58: 1–2.

    Google Scholar 

  • Williams, G. A., 1994. The relationship between shade and molluscan grazing in structuring communities on a moderatelyexposed tropical rocky shore. J. exp. mar. Biol. Ecol. 178: 79–95.

    Google Scholar 

  • Workman, C., 1983. Comparisons of energy partitioning in contrasting age-structured populations of the limpet Patella vulgata (L). J. exp. mar. Biol. Ecol. 68: 81–103.

    Google Scholar 

Download references

Authors
  1. R.C. Thompson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M.F. Roberts
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T.A. Norton
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S.J. Hawkins
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Thompson, R., Roberts, M., Norton, T. et al. Feast or famine for intertidal grazing molluscs: a mis-match between seasonal variations in grazing intensity and the abundance of microbial resources. Hydrobiologia 440, 357–367 (2000). https://doi.org/10.1023/A:1004116505004

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1004116505004

Search

Navigation