Abstract
On the extensive sedimentary tidal flats of the Wadden Sea, beds of the blue mussel Mytilus edulis represent the only major hard substratum and attachment surface for sessile organisms. On this substratum, the barnacle Semibalanus balanoides is the most frequent epibiont. In summer 1998, it occurred on over 90% of the large mussels (>45 mm shell length) and the dry weight of barnacles reached 65% of mussel dry weight. However, the extent of barnacle overgrowth is not constant and differs widely between years. Periwinkles (Littorina littorea) may reach densities >2000 m−2 on intertidal mussel beds. Field experiments were conducted to test the effect of periwinkle grazing on barnacle densities. An experimental reduction of grazing and bulldozing pressure by periwinkles resulted in increased recruitment of barnacles, while barnacle numbers decreased with increasing snail density. The highest numbers of barnacles survived in the absence of L. littorea. However, a lack of periwinkle grazing activity also facilitated settlement of ephemeral algae which settled later in the year. Field experiments showed that the growth rate of barnacles decreased in the presence of these ephemeral algae. Thus, L. littorea may reduce initial barnacle settlement, but later may indirectly increase barnacle growth rate by reducing ephemeral algae. It is suggested that periwinkle density may be a key factor in the population dynamics of S. balanoides on intertidal mussel beds in the Wadden Sea.
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Albrecht, A. S., 1994. Effects of Fucus vesiculosus covering intertidal mussel beds in the Wadden Sea. Helgoländer Meeresunters. 48: 243–256.
Albrecht, A. S., 1998. Soft bottom versus hard rock: community ecology of macroalgae on intertidal mussel beds in the Wadden Sea. J. exp. mar. Biol. Ecol. 229: 85–109.
Anderson, M. J. & A. J. Underwood, 1997. Effects of gastropod grazers on recruitment and succession of an estuarine assemblage: a multivariate and univariate approach. Oecologia 109: 442–453.
Austen, G., 1994. Hydrodynamics and particulate matter budget of Königshafen, southeastern North Sea. Helgoländer Meeresunters. 48: 183–200.
Austen, I., 1994. The surficial sediments of Königshafen variations over the past 50 years. Helgoländer Meeresunters. 48: 163–171.
Barnes, H. & M. Barnes, 1967. The effect of starvation and feeding on the production of egg masses in the boreo-arctic cirripede Balanus balanoides (L.). J. exp. mar. Biol. Ecol. 1: 1–6.
Barnes, H., M. Barnes & D. M. Finlayson, 1963. The metabolism during starvation of Balanus balanoides. J. mar. biol. Ass. U.K. 43: 213–223.
Bayerl, K. A. & B. Higelke, 1994. The development of northern Sylt during the last Holocene. Helgoländer Meeresunters. 48: 145–162.
Bertness, M. D., 1984. Habitat and community modification by an introduced herbivorous snail. Ecology 65: 370–381.
Bertness, M. D., S. D. Gaines, E. G. Stephens & P. O. Yund, 1992. Components of recruitment in populations of the acorn barnacle Semibalanus balanoides (Linnaeus). J. exp. mar. Biol. Ecol. 156: 199–215.
Buschbaum, C. & K. Reise, 1999. Effects of barnacle epibionts on the periwinkle Littorina littorea (L.). Helgol. Mar. Res. 53: 56–61.
Carroll, M. L., 1996. Barnacle population dynamics and recruitment regulation in southcentral Alska. J. exp. mar. Biol. Ecol. 199: 285–302.
Connell, J. H., 1961. Effects of competition, predation by Thais lapillus, and other factors on natural populations of the barnacle Balanus balanoides. Ecol. Monogr. 31: 61–104.
Crisp, D. J., 1960. Factors influencing growth-rate in Balanus balanoides. J. anim. Ecol. 29: 95–116.
Dayton, P. K., 1971. Competition, disturbance and community organizations: the provision and subsequent utilization of space in a rocky intertidal community. Ecol. Monogr. 41: 351–389.
Denley, E. J. & A. J. Underwood, 1979. Experiments on factors influencing settlement, survival and growth of two species of barnacles in New South Wales. J. exp. mar. Biol. Ecol. 36: 269–293.
Dittmann, S., 1987. Die Bedeutung der Biodeposite für die Benthosgemeinschaft der Wattsedimente. Unter besonderer Berücksichtigung der Miesmuschel Mytilus edulis L. PhD thesis, University of Göttingen, Germany, 182 pp.
Dungan, M. L., 1986. Three-way interactions: barnacles, limpets and algae in a sonoran desert rocky intertidal zone. Am. Nat. 127: 292–316.
Dungan, M. L., 1987. Indirect mutualism: complementary effects of grazing and predation in a rocky intertidal community. In Kerfoot, W. C. & A. Sih (eds), Predation: Direct and Indirect Impacts on Aquatic Communities. University Press of New England, Hanover, NH: 188–200.
Farrell, T. M., 1988. Community stability: effects of limpet removal and reintroduction in a rocky intertidal community. Oecologia 75: 190–197.
Fenske, C., 1997. The importance of intraspecific competition in a Littorina littorea population in the Wadden Sea. Hydrobiologia 355: 29–39.
Hawkins, S. J., 1983. Interactions of Patella and macroalgae with settling Semibalanus balanoides. J. exp. mar. Biol. Ecol. 71: 55–72.
Hawkins, S. J. & R. G. Hartnoll, 1983. Grazing of intertidal algae by marine invertebrates. Oceanogr. Mar. Biol. Annu. Rev. 21: 195–282.
Imbrie, D. W., S. J. Hawkins & C. R. McCrohan, 1989. The olfactory-gustatory basis of food preference in the herbivorous prosobranch, Littorina littorea (Linnaeus). J. Moll. Stud. 55: 217–225.
Janke, K., 1990. Biological interactions and their role in community structure in the rocky intertidal of Helgoland (German Bight, North Sea). Helgoländer Meeresunters. 44: 219–263.
Jenkins, S. R., T. A. Norton & S. J. Hawkins, 1999. Settlement and post-settlement interactions between Semibalanus balanoides (L.) (Crustacea: Cirripedia) and three species of fucoid canopy algae. J. exp. mar. Biol. Ecol. 236: 49–67.
Jernakoff, P., 1985. The effect of overgrowth by algae on the survival of the intertidal barnacle Tesseropora rosea Krauss. J. exp. mar. Biol. Ecol. 94: 89–97.
Kendall, M. A., R. S. Bowman, P. Williamson & J. R. Lewis, 1985. Annual variation in the recruitment of Semibalanus balanoides on the North Yorkshire coast. J. mar. biol. Ass. U.K. 65 (4): 1009–1030.
Keough, M. J. & P. T. Raimondi, 1995. Responses of settling invertebrate larvae to bioorganic films: effects of different types of films. J. exp. mar. Biol. Ecol. 185: 235–253.
Kim, J. H., 1997. The role of herbivory, and direct and indirect interactions, in algal succession. J. exp. mar. Biol. Ecol. 217: 119–135.
Lauckner, G., 1984. Impact of trematode parasitism on the fauna of a North Sea tidal flat. Helgoländer Meeresunters. 37: 185–199.
Lubchenco, J., 1978. Plant species diversity in a marine intertidal community: Importance of herbivore food preference and algal competitive abilities. Am. Nat. 112: 23–39.
Lubchenco, J. & S. D. Gaines, 1981. A unified approach to marine plant-herbivore interactions. I. Populations and communities. Ann. Rev. Ecol. Syst. 12: 405–437.
Luther, G., 1987. Seepocken der deutschen Küstengewässer. Helgoländer Meeresunters. 41: 1–43.
Maki, J. S., D. Ritschoff, J. D. Costlow & R. Mitchell, 1988. Inhibition of attachment of larval barnacles, Balanus amphitrite, by bacterial surface films. Mar. Biol. 97: 199–206.
Matsumasa, M. & M. Nishihira, 1994. Habitat structure provided by Mytilus edulis and the modification by sessile inhabitants. Bull. Mar. Biol. Stn. Asamushi 19: 51–63.
Menge, B. A., J. Lubchenco & L. R. Ashkenas, 1986. Experimental separation of effects of consumers on sessile prey in the low zone of a rocky shore in the Bay of Panama: direct and indirect consequences of food web complexity. J. exp. mar. Biol. Ecol. 100: 225–269.
Miller, K. M. & T. H. Carefoot, 1989. The role of spatial and size refuges in the interaction between juvenile barnacles and grazing limpets. J. exp. mar. Biol. Ecol. 134: 157–174.
Nicolaysen, M., 1996. Die Bedeutung von Seegraswiesen (Zostera noltii) für die Strandschnecke (Littorina littorea L.) im Nordsylter Wattenmeer. MSc thesis, University of Kiel, Germany, 67 pp.
Norton, T. A., S. J. Hawkins, N. L. Manley, G. A. Williams & D. C. Watson, 1990. Scraping a living: a review of littorinid grazing. Hydrobiologia 193: 117–138.
Okun, N., 1999. Einfluß der Sedimentation auf die Miesmuschel (Mytilus edulis L.). MSc thesis, University of Hamburg, Germany, 68 pp.
Petraitis, P. S., 1983. Grazing patterns of the periwinkle and their effect on sessile intertidal organisms. Ecology 64: 522–533.
Petraitis, P. S., 1987. Factors organizing rocky intertidal communities of New England: herbivory and predation in sheltered bays. J. exp. mar. Biol. Ecol. 109: 117–136.
Reise, K., 1985. Tidal flat ecology. Springer, Berlin, 191 pp.
Reise, K., E. Herre & M. Sturm, 1994. Biomass and abundance of macrofauna in intertidal sediments of Königshafen in the northern Wadden Sea. Helgoländer Meeresunters. 48: 201–215.
Scherer, B. & K. Reise, 1981. Significant predation on micro-and macrobenthos by the crab Carcinus maenas L. in the Wadden Sea. Kieler Meeresforsch., Sonderh. 5: 490–500.
Sebens, K. P., 1982. Competition for space: growth rate, reproductive output, and escape in size. Am. Nat. 120: 189–197.
Underwood, A. J., E. J. Denley & M. J. Moran, 1983. Experimental analyses of the structure and dynamics of mid-shore rocky intertidal communities in New SouthWales. Oecologia 56: 202–219. Vadas, R. L., 1992. Littorinid grazing and algal patch dynamics. In Grahame, J., Mill, P. J., Reid, D. G. (eds), Proceedings of the Third International Symposium on Littorinid Biology 197–209.
Van Tamelen, P. G., 1987. Early successional mechanisms in the rocky intertidal: the role of direct and indirect interactions. J. exp. mar. Biol. Ecol. 112: 39–48.
Watson, D. C. & T. A. Norton, 1985. Dietary preferences of the common periwinkle Littorina littorea (L.). J. exp. mar. Biol. Ecol. 88: 193–211.
Wilhelmsen, U. & K. Reise, 1994. Grazing on green algae by the periwinkle Littorina littorea in the Wadden Sea. Helgoländer Meeresunters. 48: 233–242.
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Buschbaum, C. Direct and indirect effects of Littorina littorea (L.) on barnacles growing on mussel beds in the Wadden Sea. Hydrobiologia 440, 119–128 (2000). https://doi.org/10.1023/A:1004142306396
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DOI: https://doi.org/10.1023/A:1004142306396