Antifouling activity of seaweed extracts from Guarujá, São Paulo, Brazil

Abstracts

Marine biofouling historically constitutes one of the major constraints faced by mankind in its oceanic activities. The search for alternatives to TBT-based antifouling paints has led several researchers to focus efforts in the development of environmentally friendly natural compounds. This work has contributed with this search, testing the antifouling potential of crude organic extracts from four seaweed species collected at Praia Branca, Guarujá district, São Paulo, Brazil. Throughout laboratory antifouling assays in which the attachment of a common fouling organism, the brown mussel Perna perna, was employed, antifouling activity (p < 0.05) was detected in natural concentrations of the extracts of Jania rubens (Rhodophyta, Cryptonemiales) and Bryothamnion seaforthii (Rhodophyta, Ceramiales), while Dictyopteris delicatula (Phaeophyta, Dictyotales) and Heterosiphonia gibbesii (Rhodophyta, Ceramiales) did not exhibit fouling inhibition. From the algae that exhibited antifouling activity, J. rubens presented best performance when compared to that of B. seaforthii. Future field studies would be necessary to obtain results that can better reflect natural conditions, as well as to assess the activity spectrum of the antifouling activity presently recorded. Further bioassay-guided purification of the active extracts can lead to new alternatives to the metal-based antifouling paints currently in use.

Antifouling activity; Seaweeds; Secondary metabolites; Marine natural products; Biofouling; Marine chemical ecology; Epibiosis

A incrustação biológica constitui, historicamente, um dos maiores problemas encontrados pelo homem em suas atividades no mar. A busca por alternativas a tintas antiincrustantes contendo tributilestanho (TBT) tem levado diversos pesquisadores a concentrar esforços no desenvolvimento de substâncias naturais menos danosas à biota marinha. Este trabalho procurou contribuir com essa busca, testando o potencial antiincrustante de quatro diferentes espécies de macroalgas da Praia Branca, município de Guarujá, SP. Através de testes antiincrustantes em laboratório utilizando a fixação de um organismo incrustante comum, o mexilhão Perna perna, foi constatado que os extratos de Jania rubens (Rhodophyta, Cryptonemiales) e Bryothamnion seaforthii (Rhodophyta, Ceramiales), à concentração natural, apresentaram atividade antiincrustante significativa (p < 0,05), enquanto Dictyopteris delicatula (Phaeophyta, Dictyotales) e Heterosiphonia gibbesii (Rhodophyta, Ceramiales) não demonstraram eficiência na inibição da fixação de bissos do molusco. Das algas que indicaram potencial atividade contra a incrustação, J. rubens apresentou melhor desempenho em relação a B. seaforthii. Futuras investigações em campo serão necessárias para a obtenção de resultados que possam refletir melhor as condições naturais, bem como avaliar o espectro de ação da atividade antiincrustante observada. A purificação guiada por bioensaios dos extratos ativos poderá levar a novas alternativas para os antiincrustantes metálicos atualmente em uso.

Atividade antiincrustante; Algas marinhas; Metabólitos secundários; Produtos naturais marinhos; Bioincrustação; Ecologia química marinha; Epibiose

• BHADURY, P.; WRIGHT, P. C. Exploitation of marine algae: biogenic compounds for potential antifouling applications. Planta, v. 219, p. 561-578, 2004.
• BURGESS, J. G.; BOYD, K. G.; ARMSTRONG, E.; JIANG, Z.; YAN, L.; BERGGREN, M.; MAY, U.; PISACANE, T.; GRANMO, A.; ADAMS, D.R. The development of a marine natural product–based antifouling paint. Biofouling, v. 19, p. 197-205, 2003.
• CAMILLO, E.; QUADROS, J.; CASTRO, I. B. DE; FERNANDEZ, M.. Imposex in Thais rustica (Mollusca: Neogastropoda) (Lamark, 1822) as an indicator of organotin compounds pollution at Maceio Coast (northeastern Brazil). Braz. J. Oceanogr., v. 52, p. 101-105, 2004.
• CHAMP, M. A. & LOWENSTEIN, F. L. TBT: The dilemma of high technology antifouling paints. Oceanus, v. 35, p. 69-77, 1987.
• COUTINHO, R. Estudo sobre incrustações em mina de fundeio na enseada do Forno (Arraial do Cabo, RJ). Pesq. Naval, v. 5, p. 265-275, 1992.
• CRONIN, G. Resource allocation in seaweeds and marine invertebrates: chemical defense patterns in relation to defense theories. In: MCCLINTOCK, J.B.; BAKER, B.J.,(Ed.) Marine Chemical Ecology Boca Raton, Fla.: CRC Press, 2001. p. 325-354.
• DA GAMA, B. A. P. Papel multifuncional de produtos naturais da alga marinha Laurencia obtusa (Hudson) Lamouroux (Rodophyta, Ceramiales). Tese de Doutorado.Programa de Pós-Graduação em Biotecnologia Vegetal, Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro, 2001. 139 p.
• DA GAMA, B. A. P. & PEREIRA, R. C.. Produtos não-poluentes contra a incrustação. Ciência Hoje, Rio de Janeiro, v. 19, p. 16-25, 1995a.
• DA GAMA B. A. P. & PEREIRA, R. C. Poluição por TBT no ambiente marinho: o dilema das tintas antiincrustantes. In: CONGRESSO BRASILEIRO DE DEFESA DO MEIO AMBIENTE, 4. Rio de Janeiro, Clube de Engenharia. Anais ..., 1995b. p. 275-285.
• DA GAMA, B. A. P.; CARVALHO, A. G. V.; COUTINHO, R. & PEREIRA, R.C.. Perspectivas de substituição de TBT por produtos naturais de organismos marinhos no combate à bioincrustação. In: CONGRESSO BRASILEIRO DE DEFESA DO MEIO AMBIENTE, 5. Rio de Janeiro, Clube de Engenharia. Anais..., 1999.
• DA GAMA, B.A.P.; PEREIRA, R.C.; CARVALHO, A.G.V.; COUTINHO, R.; YONESHIGUE-VALENTIN, Y. The effects of seaweed secondary metabolites on biofouling. Biofouling, v. 18, p. 13-20, 2002.
• DA GAMA, B.A.P.; PEREIRA, R.C.; SOARES, A.R.; TEIXEIRA, V.L.; YONESHIGUE-VALENTIN, Y. Is the mussel test a good indicator of antifouling activity? A comparison between laboratory and field assays. Biofouling, v. 19, p. 161-169, 2003.
• DAVIS, A.R., TARGETT, N.M., MCCONNEL O.J.; YOUNG C.M. Epibiosis of marine algae and benthic invertebrates: natural products chemistry and other mechanisms inhibiting settlement and overgrowth. Bioorg. mar. Chem, v. 3, p. 85-114, 1989
• DAVIS, A.R.; MORENO, C.A. Selection of substrata by juvenile Choromytilus chorus (Mytilidae): are chemical cues important? J. exp. mar. Biol. Ecol, v. 191, p. 167-180, 1995.
• DEVI, P.; VENNAM, J.; NAIK, C.G.; PARAMESHWARAN, P.S.; RAVEENDRAN, T.V.; YESHWANT, K.S. Antifouling activity of Indian invertebrates against the green mussel Perna viridis Mar. Biotechnol, v. 6, p. 229-232, 1998.
• FERNANDEZ, M. A.; WAGENER, A. D. R.; LIMAVERDE, A.M.; SCOFIELD, A.L.; PINHEIRO, F.M.; RODRIGUES, E. Imposex and surface sediment speciation: a combined approach to evaluate organotin contamination in Guanabara Bay, Rio de Janeiro, Brazil. Mar. environ. Res., v. 59, p. 435-452, 2005.
• FULTON-HOWARD, B. E.; FORT, A. A comparison of fouling organisms over four months at three sites: Rhode River, Rockhold Creek and the Mid Chesapeake Bay. STAR (Students Training in Aquatic Research) SYMPOSIUM, Smithsonian Environmental Research Center, 2004.
• FUSETANI, N. Biofouling and antifouling. Nat. Prod. Rep,v. 21, p. 94-104, 2004.
• GODWIN, S. Hull fouling of maritime vessels as a pathway for marine species invasions to the Hawaiian Islands. Biofouling, v. 19, p. 123-131, 2003.
• GOTO, R.; KADO, R.M. & KAMIYA, H. Fatty acids as antifoulants in a marine sponge. Biofouling, v. 6, p. 61-68, 1992.
• HARPER, M. K.; BUGNI, T. S.; COPP, B. R.; JAMES, R. D.; LINDSAY, B.S.; RICHARDSON, A.D.; SCHNABEL, P.C.; TASDEMIR, D.; VANWAGONER, R.M.; VERBITSKI, S.M.; IRELAND, C.M. Introduction to the chemical ecology of marine natural products. In: MCCLINTOCK, J.B.; BAKER, B.J., (Ed.). Marine chemical ecology Boca Raton, Fla.: CRC Press, 2001. p. 3-70.
• HAY, M. E.; DUFFY, J. E.; FENICAL, W.; GUSTAFSON, K. Chemical defenses in seaweed Dictyopteris delicatula: differential effects against reef fishes and amphipods. Mar. Ecol. Prog. Ser, v. 48, p. 185-192, 1988.
• HAY, M. E.; FENICAL, W. Chemical mediation of seaweed-herbivore interactions. In: JOHN, D.M; HAWKINS, S.J.; PRICE, J.H., (Ed.). Plant-animal interactions in the marine benthos Oxford: Clarendon Press, 1992. p. 319-333.
• HAY, M. E.; STEINBERG, P. D. The chemical ecology of plant-herbivore interactions in marine versus terrestrial communities. In: ROSENTHAL, J. & BARENBAUM, M. (Ed.). Herbivores: their interaction with secondary plant metabolites, v. 2: Evolutionary and ecological processes. New York: Academic Press, 1992. p. 371-413.
• HELLIO, C.; BERGE, J.P.; BEAUPOIL, C.; LE GAL, Y.; BOURGOUGNON, N. Screening of marine algal extracts for anti-settlement activities against microalgae and macroalgae. Biofouling, v. 18, p. 205-015, 2002.
• HELLIO, C.; MARÉCHAL, J.; VERON, B.; BREMER, G.; CLARE, A. S.; LE GAL, Y. Seasonal variation of antifouling activities of marine algae from the Brittany Coast (France). Mar. Biotechnol, v. 6, p. 67-82, 2004.
• INA, K.; TAKASAWA, R.; YAGI, A.; YAMASHITA, M.; ETOH, H.; SAKATA, K.An improved bioassay method for antifouling substances using the blue mussel, Mytilus edulis. Agric. Biol. Chem, v. 53, p. 3319-3321, 1989.
• JOLY, A.B. Gêneros de algas marinhas da costa atlântica latino-americana São Paulo: Ed. da Universidade., 1967. 461 p.
• KAREZ, R., ENGELBERT, S.; SOMMER, U. 'Co-consumption' and 'protective coating': two new proposed effects of epiphytes on their macroalgal hosts in mesograzer-epiphyte-host interactions. Mar. Ecol. Prog. Ser, v. 20, p. 85-93, 2000.
• LIMAVERDE, A. M.; WAGENER, A. L. R.; FERNANDEZ, M. A.; SCOFIELD A. L.; COUTINHO, R. Stramonita haemastoma as a bioindicator for organotin contamination in coastal environments. Mar. Environ. Res. v. 64, p. 384-398, 2007.
• LITTLER, M. M.; LITTLER, D. S. Epithallus sloughing: a self-cleaning mechanism for coralline algae. Coral Reefs, v. 18, p. 204, 1999.
• MACAYA, E. C., ROTHAUSLER, E., THIEL, M., MOLIS, M. & WAHL, M. Induction of defenses and within-alga variation of palatability in two brown algae from northern central coast of Chile: effects of mesograzers and UV radiation. J. exp. mar.. Biol. Ecol, v. 325, p. 214-227, 2005.
• MAGALHÃES, C. A.; STRUCHI, P. P.; ASBAHR, M. Evidências de imposex em populações de Stramonita haemastoma (Gastropoda: Prosobranchia) em áreas portuárias do Estado de São Paulo. Sci. total Environ, v. 188, p. 205-223, 1997.
• MARÉCHAL, J. F.; CULIO, G.; HELLIO, C.; THOMAS-GUYON, H.; CALLOW, M. E.; CLARE, A. S.; ORTALO-MAGNE, A. 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., v. 313, p. 47-62, 2004.
• MASUDA, M.; ABE, T.; SATO, S. Diversity of halogenated secondary metabolites in the red algae Laurencia nipponica (Rhodomelaceae, Ceramiales). J. Phycol, v. 33, p. 196-208, 1997.
• MINCHIN, D.; GOLLASCH, S. Fouling and ships' hulls: how changing circumstances and spawning events may result in the spread of exotic species. Biofouling, v. 19, p. 111-122, 2003.
• NYLUND, G.M.; PAVIA, H. Inhibitory effects of red algal extracts on larval settlement of the barnacle Balanus improvisus Mar. Biol, v. 143, p. 875-882, 2003.
• NOGATA, Y.; YOSHIMURA, E.; SHINSHIMA, K.; KITANO, Y.; SAKAGUCHI, I. Antifouling substances against larvae of the barnacle Balanus amphitrite from the marine sponge, Acanthella cavernosa Biofouling, v. 19, p. 193-196, 2003.
• PAUL, V. J.; CRUZ-VIEIRA, E.; THACKER, R. W. Chemical mediation of macroalgal -herbivore interactions: ecological and evolutionary perspectives. In: MCCLINTOCK, J. B.; BAKER, B. J. (Eds.). Marine chemical ecology. Boca Raton, Fla.: CRC Press, 2001. p. 3-70
• PAUL, V. J.; PUGLISI, M. P.; RITSON-WILLIAMS, R. Marine chemical ecology. Nat. Prod. Rep, v. 23, p. 153-180, 2006.
• PEREIRA, R. C. Ecologia Química Marinha. In: SOARES-GOMES, A.; PEREIRA, R.C. (Ed.). Biologia Marinha Rio de Janeiro: Interciência, 2002. p. 281-310
• PEREIRA, R. C.; CARVALHO, A. G. V.; DA GAMA, B. A. P. & COUTINHO, R. Field experimental evaluation of secondary metabolites from marine invertebrates as antifoulants. Braz. J. Biol, v. 62, 311-320, 2002.
• PEREIRA, R. C.; DA GAMA, B. A. P.; COUTINHO, R.; YONESHIGUE-VALENTIN, Y. Ecological roles of natural products of the brazilian red seaweed Laurencia obtusa Braz. J. Biol, v. 63, p. 665-672, 2003.
• RAILKIN, A. I. Marine biofouling: Colonization processes and defenses. Boca Raton, Fla.: CRC Press, 2003. 320 p.
• RITTSCHOF, D. Natural product antifoulants and coatings development. In: MCCLINTOCK, J. B.; BAKER, B. J. (Ed.). Marine Chemical Ecology Boca Raton, Fla.: CRC Press, 2001. p. 543-557.
• SAFRIEL, U. N.; COHEN, Y.; EREZ, N.; GATENO, D.; KEASAR, T.; DOLEV, Y. Biological control of marine biofouling. Oebalia, v. 19, p. 193-199, 1993.
• SENNETT, S. H. Marine chemical ecology: application in marine biomedical prospecting. In: MCCLINTOCK, J. B.; BAKER, B. J. (Ed.). Marine chemical ecology Boca Ratton, Fla.: CRC Press, 2001. p. 523-542.
• STEINBERG, P. D; DE NYS, R.; KJELLEBERG, S. Chemical mediation of surface colonization. In: McClintock, J.B. & Baker, B.J. (Ed.). Marine chemical ecology Boca Ratton, Fla., CRC Press, 2001. p. 355-388.
• STUPAK, M. E.; GARCIA, M. T.; PEREZ, M. C. Non-toxic alternative compounds for marine antifouling paints. Int. Biodeter. Biodegr, v. 52, p. 49-52, 2003.
• TEIXEIRA, V. L. Produtos naturais marinhos. In: SOARES-GOMES, A.; PEREIRA, R.C. (Ed.). Biologia Marinha Rio de Janeiro: Interciência, 2002. p. 250-279.
• VAN ALSTYNE, K. L.; DETHIER, M.N.; DUGGINS, D.O. Spatial patterns in macroalgal chemical defenses. In: MCCLINTOCK, J. B.; BAKER, B. J. (Ed.). Marine chemical ecology Boca Ratton, Fla.: CRC Press, 2001. p. 301-319.
• VILLAS-BÔAS, A. B.; FIGUEIREDO, M. A. O. Are anti-fouling effects in coralline algae species specific? Braz. J. Oceanogr. v. 52, p. 11-18, 2004.
• WEIDNER, K.; LAGES, B .G.; DA GAMA, B. A. P.; MOLIS, M.; WAHL, M; PEREIRA, R. C. Effect of mesograzers and nutrient levels on induction of defenses in several Brazilian macroalgae. Mar. Ecol. Prog. Ser., v. 283, p. 113-125, 2004.
• W.H.O.I (Woods Hole Oceanographic Institution). The effects of fouling. In: US NAVAL INSTITUTE. Marine fouling and its prevention Contrib. nº 580. Woods Hole Oceanographic Institution, Annapolis, 1967. 388 p.
• YAN, T. & YAN, W. X. Fouling of offshore structures in China - a review. Biofouling, v. 13, p. 33-138, 2003.
• ZAR, J. H. Biostatistical analysis 4^th ed. New Jersey.: Prentice Hall, 1999. 918 p.

Publication Dates

• Publication in this collection
  15 Jan 2008
• Date of issue
  Dec 2007

History

• Accepted
  30 Aug 2007
• Reviewed
  16 Apr 2007
• Received
  09 June 2006