Skip to main content
SpringerLink
Log in

The influence of epilithic microbial films on the settlement of Semibalanus balanoides cyprids – a comparison between laboratory and field experiments

  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Barnacle cypris larvae show considerable exploratory behaviour prior to habitat selection. The influence of natural epilithic microbial fouling organisms on the settlement of Semibalanus balanoides cyprids (Crustacea: Cirripedia) was examined using laboratory and field based investigations. In choice chambers, cues from microbial films were important; cyprids preferred surfaces with a mature microbial film to either unfilmed surfaces or those with a developing film. Cyprids also discriminated between filmed rocks from different tidal heights, preferentially selecting those from the mid-shore which is their usual zone. Filmed surfaces which had previously been colonised by barnacles were selected in preference to unfilmed surfaces, but the presence of an adult barnacle did not enhance settlement on either filmed or unfilmed surfaces. However, laboratory experiments were not consistent with settlement in the field which was predominantly influenced by the proximity of conspecifics and by traces of previous barnacle colonisation. These factors increased settlement, and seemed to over-rule cues from microbiota within the film. Difficulties in the application of laboratory based studies to settlement in the natural environment are discussed.

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.

Similar content being viewed by others

References

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

    Article  Google Scholar 

  • Anderson, M. J. & A. J. Underwood 1994. Effects of substratum on the recruitment and development of an intertidal estuarine fouling assemblage. J. exp. mar. Biol. Ecol. 184: 217–236.

    Article  Google Scholar 

  • Becker, K., 1993. Attachment strength and colonisation patterns of two macrofouling species on substrata with different surface tension (in situstudies). Mar. Biol. 117: 301–309.

    Article  Google Scholar 

  • Bourget, E., 1988. Barnacle larval settlement: the perception of cues at different spatial scales. In G. Chelotti & M. Vennini (eds), Behavioural Adaptations to Intertidal Life. NATO ASI Series. Plenum Press: 155–173.

  • Brancato, M. S. & R.M. Woollacott, 1982. Effect of microbial films on settlement of bryozoan larvae (Bugula simplex, B. stoloniferaand B. turrita). Mar. Biol. 71: 51–56.

    Article  Google Scholar 

  • Cameron, R. A. & R. T. Hinegardner, 1974. Initiation of metamorphosis in laboratory cultured sea urchins. Biol. Bull. Mar. Biol. Lab., Woods Hole, Mass. 146: 335–342.

    Google Scholar 

  • Clare, A. S., R. K. Freet, & M. jr. McClary, 1994. On the antennular secretion of the cyprid of Balanus amphitrite amphitritesettlement pheromone. J. mar. biol. Ass. U.K. 74: 243–250.

    Google Scholar 

  • Clare, A. S., 1995. Chemical signals in barnacles: Old problems, new approaches. In Schram, F. R. & Hoeg, J. T. (eds), New frontiers in barnacle evolution. Crustacean Issues 10. A. A., Balkema, Rotterdam: 49–67.

    Google Scholar 

  • Crisp, D. J., 1955. The behaviour of barnacle cyprids in relation to water movements over a surface. J. exp. Biol. 32: 569–590.

    Google Scholar 

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

    Google Scholar 

  • Crisp, D. J., 1984. An overview of research on marine invertebrate larvae, 1940-1980. In: J. D. Costlow & R. C. Tipper (eds), Marine Biodeterioration: an interdisclipinary study. Naval Institute Press, Annapolis, Maryland: 103–126.

    Google Scholar 

  • Crisp, D. J., 1990. Field experiments on the settlement, orientation and habitat choice of Chthamalus fragilis(Darwin). Biofouling 2: 131–136.

    Google Scholar 

  • Crisp, D. J. & P. S. Meadows, 1963. Adsorbed layers: the stimulus to settlement in barnacles. Proc. r. Soc. London, Series B, 158: 364–387.

    CAS  Google Scholar 

  • Dillon, P. S., J. S. Maki & R. Mitchel, 1989. Adhesion of Enteromorphaswarmers to microbial films. Microb. Ecol. 17: 39–47.

    Article  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. South Afr. J. mar. Sci. 11: 483–489.

    Google Scholar 

  • Edgar, G. J. & C. Shaw, 1995. The production and trophic ecology of shallow-water fish assemblages in southern Australia: II. Diets of fishes and trophic relationships between fishes and benthos at Western Port, Victoria. J. exp. mar. Biol. Ecol. 194: 83–106.

    Article  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 

  • Henschel, J. R., G. M. Branch & P. A. Cook, 1990. The colonization of artificial substrata by marine sessile organisms in False Bay. 2. Substratal material. South Afr. J. mar. Sci. 9: 299–307.

    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 

  • Holland, D. C., D. J. Crisp, R. Huxley & J. Sisson, 1984. Influence of oil shale on intertidal organisms: Effect of oil shale extract on settlement of the barnacle Balanus balanoides(L.). J. exp. mar. Biol. Ecol. 75: 245–255.

    Article  CAS  Google Scholar 

  • Holmes, S. P., C. J. Sturgess & M. S. Davies, 1997. The effect of rock-type on the settlement of Balanus balanoides(L.) cyprids. Biofouling 11: 137–147.

    Article  Google Scholar 

  • Huang, R. & Boney, A. D., 1985. Individual and combined interactions between littoral diatoms and sporelings of red algae. J. exp. mar. Biol. Ecol. 85: 101–111.

    Article  Google Scholar 

  • Jensen, P. G., J. Moyse, J. T. Hoeg & H. Al-Yahya, 1994. Comparative SEM studies on lattice organs: putative sensory structures on the carapace of larvae from Ascothoracida and Cirripedia (Crustacea Maxillopoda Thecostraca). Acta zool. 75: 125–142.

    Article  Google Scholar 

  • Johnson, C. R., D. C. Sutton, R. R. Olson & R. Giddins, 1991. Settlement of crown-of-thorns starfish: Role of bacteria on surfaces of coralline algae and a hypothesis for deep water recruitment. Mar. Ecol. Progr. Ser. 71: 143–162.

    Google Scholar 

  • Johnson, L. E. & R. R. Strathmann, 1989. Settling barnacle larvae avoid substrata previously occupied by a mobile predator. J. exp. mar. Biol. Ecol. 128: 87–103.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Keough, M. J. & P. T. Raimondi, 1996. Responses of settling invertebrate larvae to bioorganic films: Effects of large scale variation in films. J. exp. mar. Biol. Ecol. 207: 59–78.

    Article  Google Scholar 

  • Knight Jones, E. W., 1953. Laboratory experiments on gregariousness during settling in Balanus balanoidesand other barnacles. J. exp. Biol. 30: 584–598.

    CAS  Google Scholar 

  • Knight-Jones, E. W., 1951. Gregariousness and some other aspects of settling behaviour of Spirobis. J. mar. biol. Ass. U.K. 30: 201–222.

    Google Scholar 

  • Le Tourneux, F. & E. Bourget, 1988. Importance of physical and biological settlement cues used at different spatial scales by the larvae of Semibalanus balanoides. Mar. Biol. 97: 57–66.

    Article  Google Scholar 

  • MacLulich, J. H., 1986. Experimental evaluation of methods for sampling and assaying intertidal epilithic microalgae. Mar. Ecol. Progr. Ser. 34: 275–280.

    Google Scholar 

  • Maki, J. S., D. Rittschof & R. Mitchell, 1992. Inhibition of larval barnacle attachment to bacterial films: An investigation of physical properties. Microb. Ecol. 23: 97–106.

    Article  Google Scholar 

  • Maki, J. S., D. Rittschof, M. O. Samuelsson, U. Szewzyk, A. B. Yule, S. Kjelleberg, J. D. Costlow & R. Mitchell, 1990. Effect of marine bacteria and their exopolymers on the attachment of barnacle cypris larvae. Bull. mar. Sci. 46: 499–511.

    Google Scholar 

  • Maxwell, S. E. & H. D. Delaney, 1990. Designing experiments and analysing data. Wadsworth Publishing Company. Belmont, California: 901.

    Google Scholar 

  • Meadows, P. S. & G. B. Williams, 1963. Settlement of Spirobis borealisDaudin larvae on surfaces bearing micro-organisms. Nature 198: 610–611.

    Article  Google Scholar 

  • Mihm, J.W., Banta, W. C., & Loeb, G. I., 1981. Effects of adsorbed organic and primary fouling films on bryozoan settlement. J. exp. mar. Biol. Ecol. 54: 167–179.

    Article  Google Scholar 

  • Neal, A. L. & A. B. Yule, 1994. The tenacity of Elminius modestusand Balanus perforatuscyprids to bacterial films grown under different shear regimes. J. mar. biol. Ass. U.K. 74: 251–257.

    Google Scholar 

  • Norton, T. A., 1992. Dispersal by macroalgae. Brit. Phycol. J. 27: 293–301.

    Google Scholar 

  • Patterson, D. M., R. M. Crawford & C. Little, 1986. The structure of benthic diatom assemblages: a preliminary account of the use and evaluation of low-temperature scanning electron microscopy. J. exp. mar. Biol. Ecol. 96: 279–289.

    Article  Google Scholar 

  • Pawlik, J. R., 1992. Chemical ecology of the settlement of benthic marine invertebrates. Oceanogr. Mar. Biol. annu. Rev. 30: 273–335.

    Google Scholar 

  • Pawlik, J. R. & A. C. Butman, A. C., 1993. Settlement of a marine tube worm as a function of current velocity: Interacting effects of hydrodynamics and behaviour. Limnol. Oceanogr. 38: 1730–1740.

    Article  Google Scholar 

  • Pearce, C. M. & R. E. Scheibling, 1991. Effect of macroalgae, microbial films, and conspecifics on the induction of metamorphosis of the green sea urchin Strongylocentrotus droebachiensis(Mueller). J. exp. mar. Biol. Ecol. 147: 147–162.

    Article  Google Scholar 

  • Raimondi, P. T., 1988a. Rock type affects settlement, recruitment, and zonation of the barnacle Chthamalus anisopomaPilsbury. J. exp. mar. Biol. Ecol. 123: 253–267.

    Article  Google Scholar 

  • Raimondi, P. T., 1988b. Settlement cues and determination of the vertical limit of an intertidal barnacle. Ecology 69: 400–407.

    Article  Google Scholar 

  • Raimondi, P. T., 1991. Settlement behaviour of Chthalamus anisopomalarvae largely determines the adult distribution. Oecologia 85: 349–360.

    Article  Google Scholar 

  • Rittschof, D., A. S. Clare, D. J. Gerhart, M. Sister Avelin & J. Bonaventura, 1992. Barnacle in vitroassays for biologically active substances: Toxicity and settlement inhibition assays using mass cultured Balanus amphitrite amphitriteDarwin. In L. Evans (ed.), Aspects of Current Research in the US Navy Biofouling Program: 115–122.

  • Rodriguez, S. R., F. P. Ojeda & N. C. Inestrosa, 1993. Settlement of benthic marine invertebrates. Mar. Ecol. Progr. Ser. 97: 193–207.

    Google Scholar 

  • Santelices, B., 1990. Patterns of reproduction, dispersal and recruitment in seaweeds. Oceanogr. Mar. Biol. annu. Rev. 28: 177–276.

    Google Scholar 

  • Scheltema, R. S., 1961. Metamorphosis of the veliger larvae of Nassarius obsoletus(Gastropoda) in response to bottom sediment. Biol. Bull. Mar. Biol. Lab. Woods Hole, Mass., 120: 92–109.

    Google Scholar 

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

    Google Scholar 

  • Strathmann, R. R., E. S. Branscomb & K. Vedder, 1981. Fatal errors in set as a cost of dispersal and the influence of intertidal flora on set of barnacles. Oecologia 48: 13–18.

    Article  Google Scholar 

  • Todd, C. D. & M. J. Keough, 1994. Larval settlement in hard substratum epifaunal assemblages: A manipulative field study of the effects of substratum filming and the presence of incumbents. J. exp. mar. Biol. Ecol. 181: 159–187.

    Article  Google Scholar 

  • Tritar, S., D. Prieur & R. Weiner, 1992. Effects of bacterial films on the settlement of the oysters, Crassostera gigas(Thunberg, 1793) and Ostrea edulis, Linnaeus, 1750 and the Scallop Pecten maximus(Linnaeus, 1758). J. Shellfish Res. 11: 235–330.

    Google Scholar 

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

    Article  Google Scholar 

  • Underwood, A. J., 1984b. 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.

    Article  Google Scholar 

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

    Google Scholar 

  • Walker, G. & A. B. Yule, 1984. Temporary adhesion of the barnacle cyprid: The existence of an antennular adhesive secretion. J. mar. Biol. Ass. U.K. 64: 679–686.

    Google Scholar 

  • Walker, G., 1995. Larval settlement: Historical and future perspectives. In Schram, F. R. & J. T. Hoeg (eds), New Frontiers in Barnacle Evolution. Crustacean Issues 10. A. A., Balkema, Rotterdam: 69–85.

    Google Scholar 

  • Wethey, D. S., 1984. Spatial pattern in barnacle settlement: Day to day changes during the settlement season. J. mar. Biol. Ass. U.K., 64: 687–698.

    Article  Google Scholar 

  • Wieczorek, S. K., A. S. Clare & C. D. Todd, 1995. Inhibitory and facilitatory effects of microbial films on settlement of Balanus amphitrite amphitritelarvae. Mar. Ecol. Progr. Ser. 119: 1–3.

    Google Scholar 

  • Wilson, D. P., 1955. The role of micro-organisms in the settlement of Ophelia bicornisSavigny. J. mar. Biol. Ass. U.K., 34: 531–543.

    Google Scholar 

  • Winer, B. J., D. R. Brown & K. M. Michels, 1971. Statistical Principles in Experimental Design. McGraw-Hill, New York.

    Google Scholar 

  • Yule, A. B. & D. J. Crisp, 1983. Adhesion of cypris larvae of the barnacle, Balanus balanoides, to clean and arthropodin-treated surfaces. J. mar. Biol. Ass. U.K. 63: 261–271.

    Article  Google Scholar 

  • Yule, A. B. & G. Walker, 1984. The temporary adhesion of barnacle cyprids: Effects of some differing surface characteristics. J. mar. Biol. Ass. U.K. 64: 429–439.

    Article  Google Scholar 

  • Zar, J. H., 1984. Biostatistical Analysis. Prentice-Hall Inc., New Jersey, USA. 718 pp.

    Google Scholar 

Download references

Authors
  1. R. C. Thompson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. A. Norton
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. 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.C., Norton, T.A. & Hawkins, S.J. The influence of epilithic microbial films on the settlement of Semibalanus balanoides cyprids – a comparison between laboratory and field experiments. Hydrobiologia 375, 203–216 (1998). https://doi.org/10.1023/A:1017036301082

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1017036301082

Search

Navigation