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Oecologia

, Volume 138, Issue 2, pp 223–230 | Cite as

Chemical settlement inhibition versus post-settlement mortality as an explanation for differential fouling of two congeneric seaweeds

  • Sofia A. WikströmEmail author
  • Henrik Pavia
Population Ecology

Abstract

It has been proposed that seaweed secondary metabolites, e.g. brown algal phlorotannins, may have an ecologically important function as a chemical defence against epiphytes, by acting against colonisation of epiphytic organisms. We tested whether the low epiphytic abundance on the invasive brown seaweed Fucus evanescens, compared to the congeneric F. vesiculosus, is due to a more effective chemical defence against epiphyte colonisation. A field survey of the distribution of the common fouling organism Balanus improvisus (Cirripedia) showed that the abundance was consistently lower on F. evanescens than on F. vesiculosus. However, contrary to expectations, results from experimental studies indicated that F. vesiculosus has a more effective anti-settlement defence than F. evanescens. In settlement experiments with intact fronds of the two Fucus species, both species deterred settlement by barnacle larvae, but settlement was lower on F. vesiculosus both in choice and no-choice experiments. Phlorotannins from F. vesiculosus also had a stronger negative effect on larval settlement and were active at a lower concentration than those from F. evanescens. The results show that Fucus phlorotannins have the potential to inhibit settlement of invertebrate larvae, but that settlement inhibition cannot explain the lower abundance of the barnacle Balanus improvisus on F. evanescens compared to F. vesiculosus. Assessment of barnacle survival in the laboratory and in the field showed that this pattern could instead be attributed to a higher mortality of newly settled barnacles. Observation suggests that the increased mortality was due to detachment of young barnacles from the seaweed surface. This shows that the antifouling mechanism of F. evanescens acts on post-settlement stages of B. improvisus.

Keywords

Antifouling  Balanus improvisus Epiphytes  Fucus Phlorotannins 

Notes

Acknowledgements

We thank G. Toth for help with the phlorotannin analyses and G. Nylund, G. Toth and two anonymous referees for comments which led to improvement of the manuscript. Financial support was provided by The Foundation for Strategic Environmental Research (MISTRA), The Swedish Research council through contract 621–2002–289; the European Union through the European Regional Development Fund, Objective 2 West Sweden; and the Stockholm Marine Research Centre.

References

  1. Alstyne KL van (1995) Comparison of three methods for quantifying brown algal polyphenolic compounds. J Chem Ecol 21:45–58Google Scholar
  2. Barnes H, Barnes M (1962) The distribution and general ecology of Balanus balanoides together with some observations on Balanus improvisus in the waters around the coasts of Denmark, Southern Sweden and North-east Germany. Acta Univ Lund N F Avd 2 58(8):1–41Google Scholar
  3. Berntsson KM, Jonsson PR (2003) Temporal and spatial patterns in recruitment and succession of a temperate marine fouling assemblage: a comparison of static panels and boat hulls during the boating season. Biofouling 19:187–195Google Scholar
  4. Berntsson KM, Jonsson PR, Lejhall M, Gatenholm P (2000) Analysis of behavioral rejection of micro-textured surfaces and implications for recruitment by the barnacle Balanus improvisus. J Exp Mar Biol Ecol 251:59–83PubMedGoogle Scholar
  5. Bokn TL, Murray SN, Moy FE, Magnusson JB (1992) Changes in the fucoid distributions and abundances in the inner Oslofjord, Norway: 1974–80 versus 1988–90. Acta Phytogeogr Suec 78:117–124Google Scholar
  6. Buschmann AH, Gómez P (1993) Interaction mechanisms between Gracilaria chilensis (Rhodophyta) and epiphytes. Hydrobiologia 260/261:345–351Google Scholar
  7. Carlson DJ, Carlson ML (1984) Reassessment of exudation by fucoid macroalgae. Limnol Oceanogr 29:1077–1087Google Scholar
  8. Clare AS (1996) Marine natural products antifoulants: status and potential. Biofouling 9:211–229Google Scholar
  9. D’Antonio C (1985) Epiphytes on the rocky intertidal red alga Rhodomela larix (Turner) C. Agardh: negative effects on the host and food for herbivores? J Exp Mar Biol Ecol 86:197–218CrossRefGoogle Scholar
  10. Davis AR, Targett NM, McConnell OJ, Young CM (1989) Epibiosis of marine algae and benthic invertebrates: natural products chemistry and other mechanisms inhibiting settlement and overgrowth. In: Scheuer PJ (ed) Bioorganic marine chemistry. Springer, Berlin Heidelberg New York, pp 85–114Google Scholar
  11. Filion-Myklebust CC, Norton TA (1981) Epidermis shedding in the brown seaweed Ascophyllum nodosum L. Le Jolis. Mar Biol Lett 2:45–51Google Scholar
  12. Gonzalez MA, Goff LJ (1989) The red algal epiphytes Microcladia coulteri and M. californica (Rhodophyceae, Ceramiaceae). II. Basiophyte specificity. J Phycol 25:558–567Google Scholar
  13. Hay ME (1996) Marine chemical ecology: what’s known and what’s next? J Exp Mar Biol Ecol 200:103–134Google Scholar
  14. Hunt HL, Scheibling RE (1997) Role of early post-settlement mortality in recruitment of benthic marine invertebrates. Mar Ecol Prog Ser 155:269–301Google Scholar
  15. Jennings JG, Steinberg PD (1994) In situ exudation of phlorotannins by the sublittoral kelp Ecklonia radiata. Mar Biol 121:349–354Google Scholar
  16. Jennings JG, Steinberg PD (1997) Phlorotannins versus other factors affecting epiphyte abundance on the kelp Ecklonia radiata. Oecologia 109:461–473CrossRefGoogle Scholar
  17. Johnson CR, Mann KH (1986) The crustose coralline alga Phymatoliton Foslie inhibits the overgrowth of seaweeds without relying on herbivores. J Exp Mar Biol Ecol 199:249–267Google Scholar
  18. Kupper FC, Kloareg B, Guern J, Potin P (2001) Oligoguluronates elicit an oxaditive burst in the brown algal kelp Laminaria digitata. Plant Physiol 125:278–291CrossRefPubMedGoogle Scholar
  19. Langlois GL (1975) Effect of algal exudates on substratum selection by motile telotrochs of the marine peritrich ciliate Voticella marina. J Protozool 22:115–123Google Scholar
  20. Lau SCK, Qian P-Y (1997) Phlorotannins and related compounds as larval settlement inhibitors of the tube-building polychaete Hydroides elegans. Mar Ecol Prog Ser 159:219–227Google Scholar
  21. Lau SCK, Qian P-Y (2000) Inhibitory effect of phenolic compounds and marine bacteria on larval settlement of the barnacle Balanus amphitrite amphitrite Darwin. Biofouling 16:47–58Google Scholar
  22. Lemée R, Pesando D, Durand-Clément M, Dubreuil A, Meinesz A, Guerriero A, Pietra F (1993) Preliminary suvey of toxicity of the green alga Caulerpa taxifolia introduced into the Mediterranean. J Appl Phycol 5:485–493Google Scholar
  23. Littler MM, Littler DS (1999) Blade abandonment/proliferation: a novel mechanism for rapid epiphyte control in marine macrophytes. Ecology 80:1736–1746Google Scholar
  24. Nys R de, Steinberg PD, Willemsen P, Dworjanyn SA, Gabelish CL, King RJ (1995) Broad spectrum effects of secondary metabolites from the red alga Delisea pulchra in antifouling asseys. Biofouling 8:259–271Google Scholar
  25. Pavia H, Toth GB (2000) Inducible chemical resistence to herbivory in the brown seaweed Ascophyllum nodosum. Ecology 81:3212–3225Google Scholar
  26. Powell HT (1957) Studies in the genus Fucus L. II. Distribution and ecology of forms of Fucus distichus L. Emend. Powell in Britain and Ireland. J Mar Biol Ass UK 36:663–693Google Scholar
  27. Ragan MA, Glombitza K-W (1986) Phlorotannins, brown algal polyphenols. Prog Phycol Res 4:129–241Google Scholar
  28. Schmitt TM, Hay ME, Lindquist N (1995) Constraints on chemically mediated coevolution: multiple functions for seaweed secondary metabolites. Ecology 76:107–123Google Scholar
  29. Schueller GH, Peters AF (1994) Arrival of Fucus evanescens (Phaeophyceae) in Kiel Bight (western Baltic). Bot Mar 37:471–477Google Scholar
  30. Sieburth JM, Conover JT (1965) Sargassum tannin, an antibiotic which retards fouling. Nature 208:52–53Google Scholar
  31. Steinberg PD, de Nys R (2002) Chemical mediation of colonisation of seaweed surfaces. J Phycol 38:621–629CrossRefGoogle Scholar
  32. Steinberg PD, de Nys R, Kjelleberg S (2001) Chemical mediation of surface colonization. In: McClintoc JB, Baker BJ (eds) Marine chemical ecology. CRC, Boca Raton, Fla., pp 355–387Google Scholar
  33. Targett NM, Arnold TM (1998) Predicting the effects of brown algal phlorotannins on marine herbivores in tropical and temperate oceans. J Phycol 34:195–205Google Scholar
  34. Toth GB, Pavia H (2001) Removal of dissolved brown algal phlorotannins using insoluble polyvinylpolypyrrolidone (PVPP). J Chem Ecol 27:1899–1910CrossRefPubMedGoogle Scholar
  35. Vogt H, Schramm W (1991) Conspicuous decline of Fucus in Kiel Bay (western Baltic): what are the causes. Mar Ecol Prog Ser 69:189–194Google Scholar
  36. Wahl M (1989) Marine epibiosis. I. Fouling and antifouling: some basic aspects. Mar Ecol Prog Ser 58:175–189Google Scholar
  37. Weinberger F, Friedlander M (2000) Response of Gracilaria conferta (Rhodophyta) to oligoagars results in defense against agar-degrading epiphytes. J Phycol 36:1079–1086CrossRefGoogle Scholar
  38. Wikström SA, Kautsky L (in press) Invasion of a habitat-forming seaweed: effects on associated biota. Biol Invas 5Google Scholar
  39. Wikström SA, von Wachenfeldt T, Kautsky L (2002) Establishment of the exotic species Fucus evanescens C.Ag. (Phaeophyceae) in Öresund, southern Sweden. Bot Mar 45:510–517Google Scholar
  40. Worm B, Sommer U (2000) Rapid direct and indirect effects of a single nutrient pulse in a seaweed-epiphyte-grazer system. Mar Ecol Prog Ser 202:283–288Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Department of BotanyStockholm UniversityStockholmSweden
  2. 2.Tjärnö Marine Biological Laboratory, Department of Marine EcologyGöteborg UniversityStrömstadSweden

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