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.
Similar content being viewed by others
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
Amade P, Lemée R (1998) Chemical defence of the Mediterranean alga Caulerpa taxifolia: variations in caulerpenyne production. Aquat Toxicol 43:287–300
Arrontes J (1990) Composition, distribution on host, and seasonality of epiphytes on three intertidal algae. Bot Mar 33:205–211
Bayne BL (1964) Primary and secondary settlement in Mytilus edulis L. J Anim Ecol 33:513–523
Bold HC, Wynne MJ (1978) Introduction to the algae: structure and reproduction. Prentice-Hall, Englewood Cliffs
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
Buschmann AH, Gómez P (1993) Interaction mechanisms between Gracilaria chilensis (Rhodophyta) and epiphytes. Hydrobiologia 261:345–351
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
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
Clare AS (1996) Marine natural product antifoulants: status and potential. Biofouling 9:211–229
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
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
da Gama BAP, Plouguerne E, Pereira RC (2014) The antifouling defence mechanisms of marine macroalgae. Sea plants. Elsevier Science Ltd, London, pp 413–440
Davis TA, Volesky B, Mucci A (2003) A review of the biochemistry of heavy metal biosorption by brown algae. Water Res 37:4311–4330
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
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
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
Duffy JE, Hay ME (2000) Strong impacts of grazing amphipods on the organization of a benthic community. Ecol Monogr 70:237–263
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
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
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
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
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
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
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
Honkanen T, Jormalainen V (2005) Genotypic variation in tolerance and resistance to fouling in the brown alga Fucus vesiculosus. Oecologia 144:196–205
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
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
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
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
McArthur DM, Moss BL (1977) The ultrastructure of cell walls in Enteromorpha intestinalis (L.) link. Br Phycol J 12:359–368
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
Nylund GM, Pavia H (2005) Chemical versus mechanical inhibition of fouling in the red alga Dilsea carnosa. Mar Ecol Prog Ser 299:111–121
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
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
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
Paul VJ, Ritson-Williams R (2008) Marine chemical ecology. Nat Prod Rep 25:662–695
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
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
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
Saha M, Wahl M (2013) Seasonal variation in the antifouling defence of the temperate brown alga Fucus vesiculosus. Biofouling 29:661–668
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
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
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
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
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
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
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
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
Taylor PD, Wilson MA (2003) Palaeoecology and evolution of marine hard substrate communities. Earth Sci Rev 62:1–103
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
Wahl M (1989) Marine epibiosis. I. Fouling and antifouling: some basic aspects. Mar Ecol Prog Ser 58:175–189
Wahl M (2008) Ecological lever and interface ecology: epibiosis modulates the interactions between host and environment. Biofouling 24:427–438
Wahl M, Hay ME, Enderlein P (1997) Effects of epibiosis on consumer–prey interactions. Hydrobiologia 355:49–59
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
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
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
Weinberger F (2007) Pathogen-induced defense and innate immunity in macroalgae. Biol Bull 213:290–302
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
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
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
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).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
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.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Data accessibility
All experimental data underlying this publication are available from the PANGAEA repository (doi: https://doi.pangaea.de/10.1594/PANGAEA.871582).
Additional information
Responsible Editor: M.Y. Roleda.
Reviewed by B. A. Perez Da Gama and G. Culioli
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-018-3365-4