Hydrobiologia

, Volume 375, Issue 0, pp 203–216 | Cite as

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

  • R. C. Thompson
  • T. A. Norton
  • S. J. Hawkins
Article

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.

barnacle biofilm cypris recruitment fouling microalgae succession rocky intertidal 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aleem, A. A., 1950. Distribution and ecology of British marine littoral diatoms. J. Ecol. 38: 75–106.CrossRefGoogle Scholar
  2. 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.CrossRefGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. 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.Google Scholar
  5. 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.CrossRefGoogle Scholar
  6. 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
  7. 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
  8. 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
  9. 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
  10. 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
  11. 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
  12. Crisp, D. J., 1990. Field experiments on the settlement, orientation and habitat choice of Chthamalus fragilis(Darwin). Biofouling 2: 131–136.Google Scholar
  13. Crisp, D. J. & P. S. Meadows, 1963. Adsorbed layers: the stimulus to settlement in barnacles. Proc. r. Soc. London, Series B, 158: 364–387.Google Scholar
  14. Dillon, P. S., J. S. Maki & R. Mitchel, 1989. Adhesion of Enteromorphaswarmers to microbial films. Microb. Ecol. 17: 39–47.CrossRefGoogle Scholar
  15. 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
  16. 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.CrossRefGoogle Scholar
  17. 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
  18. 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
  19. 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
  20. 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.CrossRefGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. 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.CrossRefGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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
  25. 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.CrossRefGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. 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.CrossRefGoogle Scholar
  28. Knight Jones, E. W., 1953. Laboratory experiments on gregariousness during settling in Balanus balanoidesand other barnacles. J. exp. Biol. 30: 584–598.Google Scholar
  29. 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
  30. 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.CrossRefGoogle Scholar
  31. MacLulich, J. H., 1986. Experimental evaluation of methods for sampling and assaying intertidal epilithic microalgae. Mar. Ecol. Progr. Ser. 34: 275–280.Google Scholar
  32. 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.CrossRefGoogle Scholar
  33. 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
  34. Maxwell, S. E. & H. D. Delaney, 1990. Designing experiments and analysing data. Wadsworth Publishing Company. Belmont, California: 901.Google Scholar
  35. Meadows, P. S. & G. B. Williams, 1963. Settlement of Spirobis borealisDaudin larvae on surfaces bearing micro-organisms. Nature 198: 610–611.CrossRefGoogle Scholar
  36. 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.CrossRefGoogle Scholar
  37. 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
  38. Norton, T. A., 1992. Dispersal by macroalgae. Brit. Phycol. J. 27: 293–301.Google Scholar
  39. 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.CrossRefGoogle Scholar
  40. Pawlik, J. R., 1992. Chemical ecology of the settlement of benthic marine invertebrates. Oceanogr. Mar. Biol. annu. Rev. 30: 273–335.Google Scholar
  41. 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.CrossRefGoogle Scholar
  42. 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.CrossRefGoogle Scholar
  43. Raimondi, P. T., 1988a. Rock type affects settlement, recruitment, and zonation of the barnacle Chthamalus anisopomaPilsbury. J. exp. mar. Biol. Ecol. 123: 253–267.CrossRefGoogle Scholar
  44. Raimondi, P. T., 1988b. Settlement cues and determination of the vertical limit of an intertidal barnacle. Ecology 69: 400–407.CrossRefGoogle Scholar
  45. Raimondi, P. T., 1991. Settlement behaviour of Chthalamus anisopomalarvae largely determines the adult distribution. Oecologia 85: 349–360.CrossRefGoogle Scholar
  46. 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.Google Scholar
  47. Rodriguez, S. R., F. P. Ojeda & N. C. Inestrosa, 1993. Settlement of benthic marine invertebrates. Mar. Ecol. Progr. Ser. 97: 193–207.Google Scholar
  48. Santelices, B., 1990. Patterns of reproduction, dispersal and recruitment in seaweeds. Oceanogr. Mar. Biol. annu. Rev. 28: 177–276.Google Scholar
  49. 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
  50. 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
  51. 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.CrossRefGoogle Scholar
  52. 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.CrossRefGoogle Scholar
  53. 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
  54. 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.CrossRefGoogle Scholar
  55. 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.CrossRefGoogle Scholar
  56. Wahl, M., 1989. Marine epibiosis. I. Fouling and antifouling: Some basic aspects. Mar. Ecol. Progr. Ser. 58: 1–2.Google Scholar
  57. 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
  58. 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
  59. 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.CrossRefGoogle Scholar
  60. 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
  61. 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
  62. Winer, B. J., D. R. Brown & K. M. Michels, 1971. Statistical Principles in Experimental Design. McGraw-Hill, New York.Google Scholar
  63. 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.CrossRefGoogle Scholar
  64. 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.CrossRefGoogle Scholar
  65. Zar, J. H., 1984. Biostatistical Analysis. Prentice-Hall Inc., New Jersey, USA. 718 pp.Google Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • R. C. Thompson
  • T. A. Norton
  • S. J. Hawkins

There are no affiliations available

Personalised recommendations