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Fluctuations in the strength of chemical antifouling defenses in a red macroalga in response to variations in epibiont colonization pressure

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Abstract

Marine macroalgae in temperate regions are constantly exposed to colonization by fouling organisms, but the intensity of fouling fluctuates in time. We, therefore, hypothesized that a macroalgal species from these latitudes should be able to adjust its antifouling defense to the prevailing colonization pressure. To test this assumption, fouling pressure in the Western Baltic Sea as well as the activity of surface extracts gained from the non-native Gracilaria vermiculophylla against the diatom Stauroneis constricta and the filamentous alga Ceramium tenuicorne were assessed over one vegetation period on a monthly basis. We used two solvents with different polarities to extract chemical compounds from the alga. Both, hexane and dichloromethane (DCM) surface extracts, inhibited settlement of C. tenuicorne, while only hexane surface extracts deterred S. constricta. Furthermore, the activities of both extracts fluctuated on the scale of months and the fluctuations in the activity against C. tenuicorne, which were observed in DCM extracts, correlated with the intensity of fouling pressure that C. tenuicorne inflicted on G. vermiculophylla in the field. Thus, G. vermiculophylla appears to be able to adjust its antifouling defenses—at least partly—to fouling pressure.

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References

  • Abreu MH, Pereira R, Sousa-Pinto I, Yarish C (2011) Ecophysiological studies of the non-indigenous species Gracilaria vermiculophylla (Rhodophyta) and its abundance patterns in Ria de Aveiro lagoon, Portugal. Eur J Phycol 46:453–464

    Article  Google Scholar 

  • Amade P, Lemée R (1998) Chemical defence of the Mediterranean alga Caulerpa taxifolia: variations in caulerpenyne production. Aquat Toxicol 43:287–300

    Article  CAS  Google Scholar 

  • Arrontes J (1990) Composition, distribution on host, and seasonality of epiphytes on three intertidal algae. Bot Mar 33:205–211

    Article  Google Scholar 

  • Bayne BL (1964) Primary and secondary settlement in Mytilus edulis L. J Anim Ecol 33:513–523

    Article  Google Scholar 

  • Bold HC, Wynne MJ (1978) Introduction to the algae: structure and reproduction. Prentice-Hall, Englewood Cliffs

    Google Scholar 

  • Brock E, Nylund GM, Pavia H (2007) Chemical inhibition of barnacle larval settlement by the brown alga Fucus vesiculosus. Mar Ecol Prog Ser 337:165–174

    Article  Google Scholar 

  • Buschmann AH, Gómez P (1993) Interaction mechanisms between Gracilaria chilensis (Rhodophyta) and epiphytes. Hydrobiologia 261:345–351

    Article  Google Scholar 

  • Cebrian J, Enriquez S, Fortes M, Agawin N, Vermaat JE, Duarte CM (1999) Epiphyte accrual on Posidonia oceanica (L.) Delile leaves: implications for light absorption. Bot Mar 42:123–128

    Article  Google Scholar 

  • Chapman J, Hellio C, Sullivan T, Brown R, Russell S, Kiterringham E, Le Nor L, Regan F (2014) Bioinspired synthetic macroalgae: examples from nature for antifouling applications. Int Biodeterior Biodegrad 86:6–13

    Article  CAS  Google Scholar 

  • Clare AS (1996) Marine natural product antifoulants: status and potential. Biofouling 9:211–229

    Article  CAS  Google Scholar 

  • Costerton JW, Cheng KJ, Geesey GG, Ladd TI, Nickel JC, Dasgupta M, Marrie TJ (1987) Bacterial biofilms in nature and disease. Annu Rev Microbiol 41:435–464

    Article  PubMed  CAS  Google Scholar 

  • da Gama BAP, Carvalho AGV, Weidner K, Soares AR, Coutinho R, Fleury BG, Teixeira VL, Pereira RC (2008) Antifouling activity of natural products from Brazilian seaweeds. Bot Mar 51:191–201

    Google Scholar 

  • da Gama BAP, Plouguerne E, Pereira RC (2014) The antifouling defence mechanisms of marine macroalgae. Sea plants. Elsevier Science Ltd, London, pp 413–440

    Chapter  Google Scholar 

  • Davis TA, Volesky B, Mucci A (2003) A review of the biochemistry of heavy metal biosorption by brown algae. Water Res 37:4311–4330

    Article  PubMed  CAS  Google Scholar 

  • de Nys R, 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 assays. Biofouling 8:259–271

    Article  Google Scholar 

  • de Nys R, Dworjanyn SA, Steinberg PD (1998) A new method for determining surface concentrations of marine natural products on seaweeds. Mar Ecol Prog Ser 162:79–87

    Article  Google Scholar 

  • Dobretsov S, Wahl M (2001) Recruitment preferences of blue mussel spat (Mytilus edulis) for different substrata and microhabitats in the White Sea (Russia). Hydrobiologia 445:27–35

    Article  Google Scholar 

  • Duffy JE, Hay ME (2000) Strong impacts of grazing amphipods on the organization of a benthic community. Ecol Monogr 70:237–263

    Article  Google Scholar 

  • Dworjanyn SA, Wright JT, Paul NA, de Nys R, Steinberg PD (2006) Cost of chemical defence in the red alga Delisea pulchra. Oikos 113:13–22

    Article  CAS  Google Scholar 

  • Field A, Miles F (2012) Discovering statistics using R. Sage Publications Ltd., New York, p 992

  • Grosser K, Zedler L, Schmitt M, Dietzek B, Popp J, Pohnert G (2012) Disruption-free imaging by Raman spectroscopy reveals a chemical sphere with antifouling metabolites around macroalgae. Biofouling 28:687–696

    Article  PubMed  CAS  Google Scholar 

  • Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms: I. Cyclotella nana Hustedt, and Detonula confervacea (Cleve) Gran. Can J Microbiol 8:229–239

    Article  PubMed  CAS  Google Scholar 

  • Hammann M, Buchholz B, Karez R, Weinberger F (2013a) Direct and indirect effects of Gracilaria vermiculophylla on native Fucus vesiculosus. Aquat Invasions 8:121–132

    Article  Google Scholar 

  • Hammann M, Wang G, Rickert E, Boo SM, Weinberger F (2013b) Invasion success of the seaweed Gracilaria vermiculophylla correlates with low palatibility. Mar Ecol Prog Ser 486:93–103

    Article  Google Scholar 

  • Hellio C, Marechal JP, Veron B, Bremer G, Clare AS, Le Gal Y (2004) Seasonal variation of antifouling activities of marine algae from the Brittany coast (France). Mar Biotechnol 6:67–82

    Article  PubMed  CAS  Google Scholar 

  • Hemmi A, Makinen A, Jormalainen V, Honkanen T (2005) Responses of growth and phlorotannins in Fucus vesiculosus to nutrient enrichment and herbivory. Aquat Ecol 39:201–211

    Article  CAS  Google Scholar 

  • Honkanen T, Jormalainen V (2005) Genotypic variation in tolerance and resistance to fouling in the brown alga Fucus vesiculosus. Oecologia 144:196–205

    Article  PubMed  Google Scholar 

  • Lehvo A, Back S, Kiirikki M (2001) Growth of Fucus vesiculosus L. (Phaeophyta) in the northern Baltic proper: energy and nitrogen storage in seasonal environment. Bot Mar 44:345–350

    Article  Google Scholar 

  • Leonardi PI, Miravalles AB, Faugeron S, Flores V, Beltrán J, Correa JA (2006) Diversity, phenomenology and epidemiology of epiphytism in farmed Gracilaria chilensis (Rhodophyta) in northern Chile. Eur J Phycol 41:247–257

    Article  Google Scholar 

  • Lion U, Wiesemeier T, Weinberger F, Beltran J, Flores V, Faugeron S, Correa J, Pohnert G (2006) Phospholipases and galactolipases trigger oxylipin-mediated wound-activated defence in the red alga Gracilaria chilensis against epiphytes. ChemBioChem 7:457–462

    Article  PubMed  CAS  Google Scholar 

  • Lutz RA, Kennish MJ (1992) Ecology and morphology of larval and early postlarval mussels. In: Gosling EM (ed) The mussel mytilus: ecology, physiology, genetics and culture. Elsevier, Amsterdam, pp 53–85

  • Maréchal JP, Culioli G, Hellio C, Thomas-Guyon H, Callow ME, Clare AS, Ortalo-Magne A (2004) Seasonal variation in antifouling activity of crude extracts of the brown alga Bifurcaria bifurcata (Cystoseiraceae) against cyprids of Balanus amphitrite and the marine bacteria Cobetia marina and Pseudoalteromonas haloplanktis. J Exp Mar Biol Ecol 313:47–62

    Article  Google Scholar 

  • McArthur DM, Moss BL (1977) The ultrastructure of cell walls in Enteromorpha intestinalis (L.) link. Br Phycol J 12:359–368

    Article  Google Scholar 

  • Michetti KM, Miravalles AB, Hughes MH, Leonardi PI (2016) Infection process of Ceramium rubrum (Rhodophyta, Ceramiales) on the agarophyte Gracilaria chilensis (Rhodophyta, Gracilariales). Bot Mar 59:51–61

    Article  Google Scholar 

  • Nylund GM, Pavia H (2005) Chemical versus mechanical inhibition of fouling in the red alga Dilsea carnosa. Mar Ecol Prog Ser 299:111–121

    Article  Google Scholar 

  • Nylund GM, Gribben PE, de Nys R, Steinberg PD, Pavia H (2007) Surface chemistry versus whole-cell extracts: antifouling tests with seaweed metabolites. Mar Ecol Prog Ser 329:73–84

    Article  Google Scholar 

  • Nylund GM, Cervin G, Persson F, Hermansson M, Steinberg PD, Pavia H (2008) Seaweed defence against bacteria: a poly-brominated 2-heptanone from the red alga Bonnemaisonia hamifera inhibits bacterial colonisation. Mar Ecol Prog Ser 369:39–50

    Article  CAS  Google Scholar 

  • Patel P, Callow ME, Joint I, Callow JA (2003) Specificity in the settlement—modifying response of bacterial biofilms towards zoospores of the marine alga Enteromorpha. Environ Microbiol 5:338–349

    Article  PubMed  CAS  Google Scholar 

  • Paul VJ, Ritson-Williams R (2008) Marine chemical ecology. Nat Prod Rep 25:662–695

    Article  PubMed  CAS  Google Scholar 

  • Prendergast GS (2010) Settlement and Behaviour of marine fouling organisms. In: Dürr S, Thomason JC (eds) Biofouling. Wiley-Blackwell, Oxford. https://doi.org/10.1002/9781444315462.ch3

  • Pulfrich A (1996) Attachment and settlement of post-larval mussel (Mytilus edulis L.) in the Schleswig-Holstein Wadden Sea. J Sea Res 36:239–250

    Article  Google Scholar 

  • Rickert E, Karsten U, Pohnert G, Wahl M (2015) Seasonal fluctuations in chemical defenses against macrofouling in Fucus vesiculosus and Fucus serratus from the Baltic Sea. Biofouling 31:363–377

    Article  PubMed  CAS  Google Scholar 

  • Rickert E, Lenz M, Barboza FR, Gorb SN, Wahl M (2016) Seasonally fluctuating chemical microfouling control in Fucus vesiculosus and Fucus serratus from the Baltic Sea. Mar Biol 163:203

    Article  CAS  Google Scholar 

  • Saha M, Wahl M (2013) Seasonal variation in the antifouling defence of the temperate brown alga Fucus vesiculosus. Biofouling 29:661–668

    Article  PubMed  CAS  Google Scholar 

  • Saha M, Rempt M, Grosser K, Pohnert G, Weinberger F (2011) Surface-associated fucoxanthin mediates settlement of bacterial epiphytes on the rockweed Fucus vesiculosus. Biofouling 27:423–433

    Article  PubMed  CAS  Google Scholar 

  • Saha M, Rempt M, Gebser B, Grueneberg J, Pohnert G, Weinberger F (2012) Dimethylsulphopropionate (DMSP) and proline from the surface of the brown alga Fucus vesiculosus inhibit bacterial attachment. Biofouling 28:593–604

    Article  PubMed  CAS  Google Scholar 

  • Saha M, Wiese J, Weinberger F, Wahl M (2016) Rapid adaptation to controlling new microbial epibionts in the invaded range promotes invasiveness of an exotic seaweed. J Ecol 104:969–978

    Article  Google Scholar 

  • Schauer M, Balague V, Pedros-Alio C, Massana R (2003) Seasonal changes in the taxonomic composition of bacterioplankton in a coastal oligotrophic system. Aquat Microb Ecol 31:163–174

    Article  Google Scholar 

  • Schories D, Selig U (2006) Die Bedeutung eingeschleppter Arten (alien species) für die Europäische Wasserrahmenrichtlinie am Beispiel der Ostsee. Rostock Meeresbiol Beitr 15:147–158

    Google Scholar 

  • Sfriso A, Wolf MA, Maistro S, Sciuto K, Moro I (2012) Spreading and autoecology of the invasive species Gracilaria vermiculophylla (Gracilariales, Rhodophyta) in the lagoons of the north-western Adriatic Sea (Mediterranean Sea, Italy). Estuar Coast Shelf Sci 114:192–198

    Article  CAS  Google Scholar 

  • Stirk WA, Reinecke DL, van Staden J (2007) Seasonal variation in antifungal, antibacterial and acetylcholinesterase activity in seven South African seaweeds. J Appl Phycol 19:271–276

    Article  CAS  Google Scholar 

  • Sudatti DB, Rodrigues SV, Coutinho R, da Gama BAP, Salgado LT, Amado Filho GM, Pereira RC (2008) Transport and defensive role of elatol at the surface of the red seaweed Laurencia obtusa (Ceramiales, Rhodophyta). J Phycol 44:584–591

    Article  PubMed  Google Scholar 

  • Taylor PD, Wilson MA (2003) Palaeoecology and evolution of marine hard substrate communities. Earth Sci Rev 62:1–103

    Article  Google Scholar 

  • Thevanathan R, Nirmala M, Manoharan A, Gangadharan A, Rajarajan R, Dhamothrarn R, Selvaraj S (2000) On the occurrence of nitrogen fixing bacteria as epibacterial flora of some marine green algae. Seaweed Res Utiln 22:189–197

    Google Scholar 

  • Wahl M (1989) Marine epibiosis. I. Fouling and antifouling: some basic aspects. Mar Ecol Prog Ser 58:175–189

    Article  Google Scholar 

  • Wahl M (2008) Ecological lever and interface ecology: epibiosis modulates the interactions between host and environment. Biofouling 24:427–438

    Article  PubMed  Google Scholar 

  • Wahl M, Hay ME, Enderlein P (1997) Effects of epibiosis on consumer–prey interactions. Hydrobiologia 355:49–59

    Article  Google Scholar 

  • Wahl M, Shahnaz L, Dobretsov S, Saha M, Symanowski F, David K, Lachnit T, Vasel M, Weinberger F (2010) Ecology of antifouling resistance in the bladder wrack Fucus vesiculosus: patterns of microfouling and antimicrobial protection. Mar Ecol Prog Ser 411:33–48

    Article  Google Scholar 

  • Wang S, Wang G, Weinberger F, Bian D, Nakaoka M, Lenz M (2017a) Anti-epiphyte defences in the red seaweed Gracilaria vermiculophylla: non-native algae are better defended than their native conspecifics. J Ecol 105:445–457

    Article  CAS  Google Scholar 

  • Wang S, Weinberger F, Xiao L, Nakaoka M, Wang G, Krueger-Hadfield SA, Sotka EE, Bian D, Lenz M (2017b) In situ common garden assays demonstrate increased defense against natural fouling in non-native populations of the red seaweed Gracilaria vermiculophylla. Mar Biol 164:193

    Article  CAS  Google Scholar 

  • Weinberger F (2007) Pathogen-induced defense and innate immunity in macroalgae. Biol Bull 213:290–302

    Article  PubMed  CAS  Google Scholar 

  • Weinberger F, Buchholz B, Karez R, Wahl M (2008) The invasive red alga Gracilaria vermiculophylla in the Baltic Sea: adaptation to brackish water may compensate for light limitation. Aquat Biol 3:251–264

    Article  Google Scholar 

  • Wikström SA, Pavia H (2004) Chemical settlement inhibition versus post-settlement mortality as an explanation for differential fouling of two congeneric seaweeds. Oecologia 138:223–230

    Article  PubMed  Google Scholar 

  • Yamamoto K, Endo H, Yoshikawa S, Ohki K, Kamiya M (2013) Various defense ability of four sargassacean algae against the red algal epiphyte Neosiphonia harveyi in Wakasa Bay, Japan. Aquat Bot 105:11–17

    Article  Google Scholar 

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Acknowledgements

Shasha Wang was supported by a scholarship from the China Scholarship Council (CSC) at GEOMAR-Helmholtz-Zentrum für Ozeanforschung Kiel. We greatly appreciate the support and technical advices for experimental design by Prof. Dr. Martin Wahl. We acknowledge Renate Schütt for her great help in epibiont classification.

Funding

This study was funded by the China Scholarship Council (CSC) (number 201206330050).

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Correspondence to Shasha Wang.

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Shasha Wang declares that she has no conflict of interest. Florian Weinberger declares that he has no conflict of interest. Mark Lenz declares that he has no conflict of interest.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

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All experimental data underlying this publication are available from the PANGAEA repository (doi: https://doi.pangaea.de/10.1594/PANGAEA.871582).

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Responsible Editor: M.Y. Roleda.

Reviewed by B. A. Perez Da Gama and G. Culioli

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Wang, S., Weinberger, F. & Lenz, M. Fluctuations in the strength of chemical antifouling defenses in a red macroalga in response to variations in epibiont colonization pressure. Mar Biol 165, 107 (2018). https://doi.org/10.1007/s00227-018-3365-4

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  • DOI: https://doi.org/10.1007/s00227-018-3365-4

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