Acessibilidade / Reportar erro

Chemical composition and release in situ due to injury of the invasive coral tubastraea (Cnidaria, Scleractinia)

Abstracts

Defensive chemistry may be used against consumers and competitors by invasive species as a strategy for colonization and perpetuation in a new area. There are relatively few studies of negative chemical interactions between scleratinian corals. This study characterizes the secondary metabolites in the invasive corals Tubastraea tagusensis and T. coccinea and relates these to an in situ experiment using a submersible apparatus with Sep-Paks® cartridges to trap substances released by T. tagusensis directly from the sea-water. Colonies of Tubastraea spp were collected in Ilha Grande Bay, RJ, extracted with methanol (MeOH), and the extracts washed with hexane, dichloromethane (DCM) and methanol, and analyzed by GC/MS. Methyl stearate and methyl palmitate were the major components of the hexane and hexane:MeOH fractions, while cholesterol was the most abundant in the DCM and DCM:MeOH fractions from Tubastraea spp. The organic material retained in Sep-Paks® cartridges was tentatively identified as hydrocarbons. There was a significant difference between treatments and controls for 1-hexadecene, n-hexadecane and n-eicosane contents. The production of defensive substances by the invasive corals may be a threat to the benthic communities of the region, which include endemic species.

Injury; secondary metabolites; Tubastraea coccinea; Tubastraea tagusensis; submersible apparatus


Substâncias químicas de defesa contra consumidores e competidores podem ser usadas por espécies invasoras marinhas como estratégia de colonização e perpetuação em novo ambiente. Entretanto, há poucos estudos experimentais que demonstrem as possíveis interações negativas entre corais escleractínios. Este trabalho tem como objetivo caracterizar os metabólitos secundários dos corais invasores Tubastraea tagusensis e T. coccinea; avaliar através da técnica de amostragem in situ quais são as substâncias de T. tagusensis liberadas na água do mar, com o auxílio de aparelho subaquático com colunas Sep-Paks®. Colônias dos corais invasores Tubastraea spp foram coletadas na Baía de Ilha Grande, RJ, e extraídas com MeOH. Os extratos foram submetidos à eluições com hexano, DCM e MeOH, e analisados por CG-EM. Estearato de metila e palmitato de metila foram as substâncias majoritárias das frações hexânicas e hexano: DCM, enquanto o colesterol foi a substância mais abundante das frações DCM e DCM:MeOH de Tubastraea spp. O material orgânico retido nas colunas Sep-Paks® foi identificado como hidrocarbonetos. Diferenças significativas entre controle e tratamento foram relacionadas a diferentes quantidades de 1-hexadeceno, n-hexadecano e n-eicosano. A produção de substâncias de defesas em Tubastraea spp permite especular sobre a ameaça que estes corais invasores representam para as comunidades bentônicas da Ilha Grande.

lesão artificial; metabólitos secundários; Tubastraea coccinea; Tubastraea tagusensis; aparelho submersível


  • BAIRD, A. H.; PRATCHETT, M. S.; GIBSON, D. J.; KOZIUMI, N.; MARQUIS, C. P. Variable palatability of coral eggs to a planktivorous fish. Mar. Freshw. Res., v. 6, p. 865-868, 2001 .
  • BENSON, A. A.; MUSCATINE, L. Wax in coral mucus: Energy transfer from corals to reef fishes. Limmol. Oceanogr., v. 19, p. 810-814, 1974.
  • BLUNT, J. W.; COPP, B. R.; HU, W.; MUNRO, M. H. G.; NORTHCOTE, P. T.; PRINSEP, M. R. Marine natural products. Nat. Prod. Rep , v. 24, p. 31-86, 2007.
  • BLUNT, J. W.; COPP, B. R.; HU, W.; MUNRO, M. H. G.; NORTHCOTE, P. T.; PRINSEP, M. R. Marine natural products. Nat. Prod. Rep., v. 25, p. 35-94, 2008.
  • BLUNT, J. W.; COPP, B. R.; HU, W.; MUNRO, M. H. G.; NORTHCOTE, P. T.; PRINSEP, M. R. Marine natural products. Nat. Prod. Rep., v. 26, p. 170-244, 2009.
  • BUDZIKIEWICZ, H.; DJERASSI, C.; WILLIAMS, D.H. Interpretation of mass spectra of compounds San Francisco: Holden-Day, 1964.
  • CASTRO, C. B.; PIRES, D. O. Brazilian coral reefs: what we already know and what is still missing. Bull. mar. Sci., v. 69, p. 357-371, 2001.
  • CHANGYUN, W.; HAIYAN, L; CHANGLUN, S; YANAN, W; LIANG, L; HUASHI, G. Chemical defensive substances of soft corals and gorgonians. Acta Ecol. Sin., v. 28, p. 2320-2328, 2008.
  • CHIANG, I.Z.; HUANG, W.Y.; WU, J.T. Allelochemicals of Botryococcus braunii (Chlorophyceae). J. Phycol., vol. 40, p. 474–480, 2004.
  • CLARK, R. C., Jr.; BLUMER, M. Distribution of n-paraffins in marine organisms and sediment. Limnol. Ocean., v. 12, p. 79-87, 1967.
  • COLL, J. C. The chemistry and chemical ecology of octocorals (Coelenterata, Anthozoa, Octocorallia). Chem. Rev, v. 92, p. 613-631, 1992.
  • COLL, J. C.; BOWDEN, B. F.; TAPIOLAS, D. M.; DUNLAP., W. C. In situ isolation of allelochemicals released from soft corals (Coelenterata: Octocorallia): a totally submersible apparatus. J. expl mar. Biol. Ecol., v. 60, p. 293-299, 1982.
  • CREED, J. C. Two invasive alien azooxanthellate corals, Tubastraea coccinea and Tubastraea tagusensis, dominate the native zooxanthellate Mussismilia hispida in Brazil. Coral Reefs, v. 25, 350, 2006.
  • DE NYS, R.; COLL, J. C.; PRICE, I. R. Chemically mediated interactions between the red alga Plocamium hamatum (Rhodophyta) and the octocoral Sinularia cruciata (Alcyonacea). Mar. Biol., v. 108, p. 315-320, 1991.
  • DE RUYTER VAN STEVENICK, ED.; VAN MULEKOM, L. L.; BREEMAN, A. M. Growth inhibition of Lobophora variegata (Lamouroux) Womersley by scleractinian corals. J. expl Mar. Biol. Ecol , v. 115, p. 169-178, 1988.
  • EPIFANIO, R.A.; MAIA, L.F.; PAWLIK, J.; FENICAL, W. Antipredatory secosterols from Pseudopterogorgia americana Mar. Ecol. Prog. Ser., v. 329, p. 307-310, 2007.
  • ESTES, J. A.; STEINBERG, P. D. Predation, herbivory and kelp evolution. Paleobiology, v. 14, p. 19-36, 1988.
  • FAULKNER, D. J.; WALKER, R. P.; THOMPSON, J. Chemical ecology of a temperate sponge-dominated assemblage. In: INT. SYMP. MAR. NAT. PROD., 3., Brussels, Belgium, 1980. Contribution C-6, 1980.
  • FERREIRA, C. E.L. Non-indigenous corals at marginal sites. Coral Reefs, v. 22, p. 498, 2003.
  • FLEURY, B. G.; LAGES, B. G.; BARBOSA, J. P.; KAISER, C. R.; PINTO, A. C. New hemiketal steroid from the introduced soft coral Chromonephthea braziliensis is a chemical defense against predatory fishes. J. chem. Ecol , v. 34, p. 1-5, 2008.
  • FLEURY, B. G., COLL, J.; SAMMARCO, P. Complementary (secondary) metabolites in a soft coral: sex-specific variability, inter-clonal variability, and competition. Mar. Ecol., v. 27, p. 204–218, 2006.
  • FLEURY, B. G., COLL, J. C., SAMMARCO, P. W., TENTORI, E.; DUQUESNE, S. Complementary (secondary) metabolites in an octocoral competing with a scleractinian coral: effects of varying nutrient regimes. J. expl mar. Biol. Ecol , v. 303, p. 115-131, 2004.
  • FUNG, F. M. Y.; TACHIBANA, S.; CHOU, L. M.; DING, J. L. Cytotoxic and anticancer agents in mucus of Galaxea fascicularis: Purification and characterization. J. mar. Biotechnol., v. 5, p. 50-57, 1997.
  • FUSETANI, N.; ASANO, M.; MATSUNAGA, S.; HASHIMOTO, K. Bioactive marine metabolites-XV. Isolation of aplysinopsin from the scleractinian coral Tubastraea aurea as an inhibitor of development of fertilized sea urchin eggs. Comp. Biochem. Physiol., v. 85B, p. 845-846, 1986.
  • GEORGIEVA, E.; HANDJIEVA, N.; POPOV, S.; EVSTATIEVA, L. Comparative analysis of the volatiles from flowers and leaves of three Gentiana species. Biochem. Syst. Ecol., v. 33, p. 938-947, 2005.
  • GINER, J. L.; ZHAO, H.; TOMAS, C. Sterols and fatty acids of three harmful algae previously assigned as Chattonella Phytochemistry, v. 69, p. 2167-2171, 2008.
  • GLYNN, P.W.; COLLEY, S.B.; MATÉ, J.L.; COTÉS, J.; GUZMAN, H.M.; BAILEY, R.L.; FEINGOLD, J.S.; ENOCHS, I.C. Reproductive ecology of the azooxanthelate coral Tubastraea coccinea in the Equatorial Eastern Pacific: Part V. Dendrophylliidae. Mar. Biol., v. 153, p. 529-544, 2007.
  • GUELLA, G.; MANCINI, I.; ZIBROWIUS, H.; PIETRA, F. Novel Aplysinopsin-Type Alkaloids from scleractinian corals of the family Dendrophylliidae of the Mediterranean and Philippines. Configurational-Assignment Criteria, stereospecific synthesis, and photoisomerization. Helv. Chim. Acta, v. 71, p. 773-782., 1988.
  • HADFIELD, M. G.; SCHEUER, D. Evidence for a soluble metamorphic inducer in Phestilla sibogae: ecological, chemical and biological data. Bull. Mar. Sci, v. 37, p. 556-566, 1985.
  • 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 Chemistry Ecology . Boca Raton, Fla.: C.R.C. Press, 2001. p. 3-69.
  • HAY, M. E.; FENICAL, W. Marine plant-herbivore interactions: the ecology of chemical defense. A. Rev. Ecol. Syst., v. 19, p.111-145, 1988
  • HAY, M. E.; STEINBERG, P. D. The chemical ecology of plant-herbivore interactions in marine versus terrestrial communities. In: ROSENTHAL, J,; BERENBAUM, M.(Ed.) Herbivores: Their interaction with secondary metabolites, evolutionary and ecological processes. San Diego: Academic Press, 1992. p. 371-413.
  • IRFANULLAH, H. M; MOSS, B. Allelopathy of filamentous algae. Hydrobiologia, v. 543, p. 169–179, 2005
  • IKAWA, M.; HANEY, J.F.; SASNER, J.J. Inhibition of Chlorella growth by the lipids of cyanobacterium Microcystis aeruginosa Hydrobiologia, v. 331, p. 167–170, 1996.
  • IWAGAWA, T.; MIYAZAKI, M.; YOKOGAWA, Y.; OKAMURA, H.; NAKATANI, M.; DOE, M.; MORIMOTO, Y.; TAKEMURA, K. Aplysinopsin dimmers from a stony coral Tubastraea aurea Heterocycles, v. . 75, p. 2023-2028, 2008.
  • JACKSON, J.B.C.; BUSS, L. Allelopathy and spatial competition among coral reef invertebrates. Proc. natn. Acad. Sci. U.S.A., v. 72, p. 5160-5163, 1975.
  • JUTTNER, F. Liberation of 5,8,11,14,17-eicosapentaenoic acid and other polyunsaturated fatty acids from lipids as a grazer defense reaction in epilithic diatom biofilms. J. Phycol., v. 37, p. 744–755, 2001.
  • KAKISAWA, H.; ASARI, F.; KUSUMI, T.; TOMA, T.; SAKURAI, T.; OOHUSA, T.; HARA,Y.; CHIHARA, M. An allelopathic fatty acid from the brown alga Cladosiphon okamuranus Phytochem, v. 27, p. 731–735, 1988.
  • KAMAYA, Y., KUROGI, Y., SUZUKI, K. Acute toxicity of fatty acids to the freshwater green alga Selenastrum capricornutum Environ. Toxicol., v. 18, p. 289–294, 2003.
  • KANAZAWA, A. Sterols in marine invertebrates. Fish. Sci., v. 67, p. 997-1007, 2001.
  • KELMAN, D.; BENAYAHU, Y.; KASHMAN,Y. Chemical defense of the soft coral Parerythropodium fulvum fulvum (Forskal) in the Red Sea against generalist reef fish. J. expl Mar. Biol. Ecol., v. 238, p. 127-137, 1999.
  • KOH, E. G. L.; SWEATMAN, H. Chemical warfare among scleractinians: bioactive natural products from Tubastraea falkneri Wells kill larvae of potential competitors. J. expl mar. Biol. Ecol., v. 251, p. 141-160, 2000.
  • KOH, E. G. L. Do scleractinian corals engage in chemical warfare against microbes? J. Chem. Ecol., v. 23, p. 379-398, 1997.
  • KOH, L. L.; GOH, N. K. C.; CHOU, L. M.; TAN, Y.W. Chemical and physical defenses of Singapore gorgonians (Octocorallia: Gorgonacea). J. expl Mar. Biol. Ecol, v. 251, p. 103-115, 2000.
  • KONTIZA, I.; ABATIS, D.; MALAKATE, K.; VAGIAS, C.; ROUSSIS, V. 3-Keto steroids from the marine organisms Dendrophyllia cornigera and Cymodocea nodosa. Steroids, v. 71, p. 177-181, 2006.
  • KVITEK, R.G.; DEGANGE, A.R.; BEITLER, M. K. Paralytic shellfish poisoning toxins mediate feeding behavior of sea otters. Limnol. Oceanogr., v. 36, p. 393-404, 1991.
  • LA BARRE, S. C.; COLL, J. C.; SAMMARCO, P. W. Competitive strategies of soft corals (Coelenterata: Octocorallia) III Spacing and aggressive interactions between alcyonaceans. Mar. Ecol. Prog. Ser , v. 28, p. 147-156, 1986.
  • LAGES, B. G., FLEURY, B. G., PINTO, A. C.; CREED, J. C. Chemical defenses against generalist fish predators and fouling organisms in two invasive ahermatypic corals in the genus Tubastraea Mar. Ecol., v. 31, p. 473-482, 2010.
  • LAGES, B. G.; FLEURY, B. G.; FERREIRA, C. E. L.;PEREIRA, R. C. Chemical defense of an exotic coral as invasion strategy. J. expl mar. Biol. Ecol., v. 328, p. 127-135, 2006.
  • LUBCHENCO, J.; GAINES, S. D. A unified approach to marine plant-herbivore interactions. I. populations and communities. A. Rev. Ecol. Syst., v. 12, p. 405-437, 1981.
  • MAIDA, M.; SAMMARCO, P. W.; COLL, J. C. Effects of soft corals on scleractinian coral recruitment. II. Allelopathy, spat survivorship and reef community structure. Mar. Ecol., v. 22, p. 397–414, 2001.
  • MAIDA, M.; SAMMARCO, P. W.; COLL, J. C. Preliminary evidence for directional allelopathic effects of the soft coral Sinularia flexibilis (Alcyonacea: Octocorallia) on scleractinian coral recruitment. Bull. mar. Sci , v.56, p. 303-311, 1995.
  • MEYER, M.; DELBERGHE, F.; LIRON, F.; GUILLAUME, M.; VALENTIN, A.; GUYOT, M. An antiplasmodial new (bis)indole alkaloid from the hard coral Tubastraea sp. Nat. Prod. Res., v. 23, p. 178-182, 2009.
  • MEYERS, P. A. Fatty acids and hydrocarbons of Caribbean corals. In: INT. CORAL REEF SYMP., 3., Miami, USA, 1977. p. 530-536.
  • MUNDT, S.; KREITLOW, S.; JANSEN, R. Fatty acids with antibacterial activity from the cyanobacterium Oscillatoria redekei HUB 051. J. appl. Phycol.,v. 15, p. 263–267, 2003.
  • NAKAJIMA, R.; YOSHIDA,T.; AZMAN, B. A. R.; ZALEHA, K.; OTHMAN, B. H. R.; TODA, T. In situ release of coral mucus by Acropora and its influence on the heterotrophic bacteria. Aquat. Ecol., v. 43, p. 815-823, 2009.
  • PAUL, V. J.; RITSON-WILLIAMS, R. Marine chemical ecology. Nat. Prod. Rep., v. 25, p. 662-695, 2008.
  • PAUL, V. J.; PUGLISI, M. P.; RITSON-WILLIAMS, R. Marine chemical ecology. Nat. Prod. Rep., v. 23, p. 153-180, 2006.
  • PAULA, A. F.; CREED, J. C.Two species of the coral Tubastraea (Cnidaria, Scleractinia) in Brazil: a case of accidental introduction. Bull mar. Sci., v. 74, p. 175-183, 2004.
  • PAULA, A. F.; CREED, J. C. Spatial distribution and abundance of nonindigenous coral genus Tubastraea (Cnidaria, Scleractinia) around Ilha Grande, Brazil. Braz. J. Biol , v. 65, p. 661-673, 2005.
  • PAWLIK, J. R. Marine invertebrate chemical defense. Chem. Rev, v. 93, p. 1911-1922, 1993.
  • PAWLIK, J. R.; BURCH, M. T.; FENICAL, W. Patterns of chemical defense among Caribbean gorgonian corals: a preliminary survey. J. expl mar. Biol. Ecol., v. 108, p. 55-66, 1987.
  • QUINN, G. P.; KEOUGH, M. J. Experimental design and data analysis for biologists. Cambridge: Cambridge University Press, 2002.
  • RASHID, M. A.; GUSTAFSON, K. R.; CARDELLINA, I. J. H.; BOYD, M. R. Mycaloides D and E, new cytotoxic macrolides from a collection of the stony coral Tubastraea faulkneri J. Nat. Prod, v. 58, p. 1120-1125, 1995.
  • SAMMARCO, P. W., COLL, J. C.; LA BARRE, S. Competitive strategies of soft corals (Coelenterata: Octocorallia). II. Variable defensive responses and susceptibility to scleractinian corals. J. expl mar. Biol. Ecol., v. 91, p. 199-215, 1985.
  • SCHMITT, T. M., HAY, M. E., LINDQUIST, N. Constraints on chemically mediated coevolution: multiple functions of seaweed secondary metabolites. Ecology, v. 76, p. 107-123, 1995.
  • SCHULTE, B. A.; DE NYS R.; BAKUS, G. J.; CREWS, P.; EID, C.; NAYLOR, S.; MANES, L. V. A modified allomone collecting apparatus. J. Chem. Ecol., v. 17, p. 1327-1332, 1991.
  • SLATTERY, M. ; HAMANN, M. T.; MCCLINTOCK, J. B.; PERRY, T. L.; PUGLISI, M. P.; YOSHIDA, W. Y. Ecological roles for water-borne metabolites from Antarctic soft corals. Mar. Ecol. Prog. Ser , v. 161, p. 133–144, 1997.
  • SPRUELL, J.A. Response to algae and zooplankton to C18 fatty acids of Chlamydomonas reinhardtii Hydrobiologia, v. 114, p. 9–12, 1984.
  • STACHOWICZ, J. J. Chemical ecology of mobile benthic invertebrates: Predators and prey, allies and competitors. In: MCCLINTOCK, J.B.; BAKER, B.J. (Ed.). Marine Chemical Ecology Boca Raton, Fla.: C.R.C. Press, 2001. p. 157-193.
  • SULLIVAN, B.; FAULKNER, D. J.; WEBB, L. Siphonodictidine, a metabolite of the burrowing sponge Siphonodictyon sp. that inhibits coral growth. Science, v. 221, p. 1175-1176, 1983.
  • SUZUKI, M.; WAKANA, I.; DENBOH, T.; TATEWAKI, M. An allelopathic polyunsaturated fatty acid from red algae. Phytochem., v. 43, p. 63–65, 1996.
  • TARRANT, A. M.; BLOMQUIST, C. H.; LIMA, P. H.; ATKINSON, M. J.; ATKINSON, S. Metabolism of estrogens and androgens by scleractinian corals. Comp. Biochem. Physiol, v. 136B, p. 473–485, 2003.
  • THACKER, R. W.; BECERRO, M. A.; LUMBANG., W. A.; PAUL, V. J. Allelopathic interactions between sponges on a tropical reef. Ecology, v. 79, p. 1740-1750, 1998.
  • TOMONO, Y.; HIROTA, H.; FUSETANI, N. Isogosterones A-D, antifouling 13,17-Secosteroids from an Octocoral Dendronephthya sp. J. org. Chem, v. 6, p. 2272–2275, 1999.
  • VAN ALSTYNE, K. L.; DUGGINS, D. O.; DETHIER, M. N. Spatial patterns in macroalgal chemical defenses. In: MCCLINTOCK, J. B.; BAKER, B.J. (Ed.). Marine Chemical Ecology. Boca Raton, Fla.: C.R.C. Press, 2001. p. 301-324.
  • VAN ALSTYNE, K.L.; WYLIE, C.R.; PAUL, V.J. Antipredator defenses in tropical Pacific soft corals (Coelenterata: Octocorallia). II. The relative importance of chemical and structural defenses in three species of Sinularia J. expl mar. Biol. Ecol., v. 178, p. 17-34, 1994.
  • YAMASHIRO, H.; OKU, H.; HIGA, H.; CHINEN, I.; SAKAI, K. Composition of lipids, fatty acids and sterols in Okinawan corals. Comp. Biochem. Physiol., v. 122, p. 397-407, 1999.

Publication Dates

  • Publication in this collection
    14 Feb 2011
  • Date of issue
    2010

History

  • Accepted
    23 Aug 2010
  • Reviewed
    25 May 2010
  • Received
    04 June 2009
Universidade de São Paulo, Instituto Oceanográfico Praça do Oceanográfico, 191 , 05508-120 Cidade Universitária, São Paulo - SP - Brasil, Tel.: (55 11) 3091-6501, Fax: (55 11) 3032-3092 - São Paulo - SP - Brazil
E-mail: io@usp.br