Chemical defense of Hymeniacidon heliophila (Porifera: halichondrida) against tropical predators

Ribeiro, Suzi Meneses; Bianco, Éverson Miguel; Rogers, Ricardo; Teixeira, Valéria Laneuville; Pereira, Renato Crespo

Abstracts

Various benthic organisms have chemical defenses which reduce their predators' consumption. Although their efficiency may be noticed in many organisms, many of their effects are not well- known yet. Multiple ecological roles of secondary metabolites are shown in some sponges, which may represent an adaptative advantage considering the high amount of energy used to produce these chemical compounds. The goal of this work was to investigate the defensive property of the extracts from the sponge Hymeniacidon heliophila against the tropical predators: hermit crabs (Calcinus tibicens), sea urchins (Lytechinus variegatus) and generalist fishes. Extracts obtained with n-hexane, ethyl acetate and acetone/methanol were used in assays and all of them were effective in reducing the consumption by C. tibicens; n-hexane extract reduced the consumption by L. variegatus; and medium polarity extracts reduced fish consumption. Either the variation in action or the multiple ecological roles of the extracts indicates that different types of compounds can be associated to the defensive system produced by H. heliophila.

Hymeniacidon heliophila; chemical defenses; predation; tropical predators

Diversos organismos bênticos possuem defesas químicas que ajudam a diminuir a predação. Embora sua eficácia seja comprovada, muitos de seus efeitos são ainda desconhecidos. Múltiplas funções dos metabolitos secundários foram evidenciadas em algumas esponjas e isso pode representar uma vantagem adaptativa, considerando o alto valor energético gasto pelas espécies para produzí-los. O objetivo desse trabalho foi investigar as propriedades defensivas de extratos da esponja Hymeniacidon heliophila contra predadores tropicais: paguros (Calcinus tibicens), ouriços-do-mar (Lytechinus variegatus) e peixes generalistas. Extratos em n-hexano, acetato de etila e acetona/metanol foram usados nos ensaios e todos foram eficientes na redução do consumo por C. tibicen; extratos em n-hexano reduziram o consumo por L. variegatus; e extratos de média polaridade reduziram o consumo por peixes. A variação na ação ou as funções ecológicas múltiplas dos extratos indicam que diferentes tipos de substâncias podem ser associadas ao sistema defensivo produzido por Hymeniacidon heliophila.

Hymeniacidon heliophila; defesas químicas; predação; predadores tropicais

ASSMANN, M.; LICHTE, E.; PAWLIK, J. R.; KOCK, M. Chemical defenses of the Caribbean sponges Agelas widenmayeri and Agelas conifera Mar. Ecol. Prog. Ser., v. 207, p. 255-262, 2000.
AYLING, A. M. The role of biological disturbance in temperate subtidal encrusting communities. Ecology, v. 62, p. 830-847, 1981.
BECERRO, M. A.; THACKER, R. W.; TURON, X.; URIZ, M. J.; PAUL, V. J. Biogeography of sponge chemical ecology: comparisons of tropical and temperate defenses. Oecologia, v. 135, p. 91-101, 2003.
BJORNDAL, K. Digestibility of the sponge Chondrila nucula in the green turtle Chelonia mydas Bull. mar. Sci., v. 47, p. 567-570, 1990.
BLUNT, J. W.; COPP, B. R.; HU, W.; MUNRO M. H. G.; NORTHCOTE, P. T.; PRINSEP, M. Marine natural products. Nat. Prod. Rep, v. 26, p. 170-244, 2009.
BREVES-RAMOS, A.; LAVRADO, H. P.; JUNQUEIRA, A. O. R.; SILVA, S. H. G. Succession in rocky intertidal benthic communities in areas with different pollution levels at Guanabara Bay (RJ-Brazil). Braz. Arch. Biol. Technol., v. 48, p. 951-965, 2005.
BURNS, E.; IFRACH, I.; CARMELI, S.; PAWLIK, J. R.; ILAN, M. Comparison of antipredatory defenses of Red Sea and Caribbean sponges. I. Chemical defense. Mar. Ecol. Prog. Ser., v. 252, p. 105-114, 2003.
CHANAS, B.; PAWLIK, J. R. Defenses of Caribbean sponges against predatory reef fish. II. Spicules, tissue toughness, and nutritional quality. Mar. Ecol. Prog. Ser, v. 127, p. 195-211, 1995
CIMINO, G.; DE ROSA, S.; DE STEFANO, S.; SODANO, G. The chemical defense of four Mediterranean nudibranchs. Comp. Biochem. Physiol., v. 73B, p. 471-474, 1982.
CLAVICO, E. E. G.; MURICY, G.; DA GAMA, B. A. P.; BATISTA, D., VENTURA C. R. R., PEREIRA, R. C. Ecological roles of natural products from the marine sponge Geodia corticostylifera Mar. Biol., v. 148, p. 479-488, 2006.
DUFFY, J. E.; PAUL, V. J. Prey nutritional quality and the effectiveness of chemical defenses against tropical reef fishes. Oecologia, v. 90, p. 333-339. 1992
EPIFANIO, R. de A.; GABRIEL, R.; MARTINS, D. L.; MURICY, G. The sesterterpene variabilin as fish feeding deterrent from Ircinia strobilina Lam. J. chem. Ecol., v. 25, p. 2247-2254, 1999.
FENICAL, W. 2006. Marine pharmaceuticals: Past, present, and future. Oceanography, v. 19, p. 110-119, 2006.
FERREIRA, C. E. L.; GONÇALVES, J. E. A.; COUTINHO, R. Community structure of fishes and habitat complexity on a tropical rocky shore. Environ. Biol. Fish., v. 61, p. 353-369, 2001.
FERREIRA, C. E. L.; FLOETER, S. R.; GASPARINI, J. L.; FERREIRA, B. P.; JOYEUX, J. C. Trophic structure patterns of Brazilian reef fishes: a latitudinal comparison. J. Biogeogr., v. 31, p. 1093-1106, 2004.
GRANATO, A. C.; BERLINCK, R. G. S.; MAGALHÃES, A.; SCHEFER, A. B.; FERREIRA, A. G.; SANCTIS, B.; FREITAS, J. C.; HAJDU, E.; MIGOTTO, A. E. Produtos naturais das esponjas marinhas Aaptos sp., Hymeniacidon aff. heliophila e do nudibrânquio Doris aff. verrucosa Quím. Nova, v. 23, p. 594-599, 2000.
HAY, M. E. Seaweed chemical defenses: their role in the evolution of feeding specialization and in mediating complex interactions. In: PAUL V. J. (ed.). Ecological roles for marine secondary metabolites; explorations in chemical ecology series. New York: Cornell University Press, 1992. p. 93-118.
HAY, M. E. Marine chemical ecology: what's known and what's next? J. expl mar. Biol. Ecol., v. 200, p. 103-134, 1996.
HAY, M. E.; KAPPEL, Q. E.; FENICAL, W. Synergisms in plant defenses against herbivores: interactions of chemistry, calcification, and plant quality. Ecology, v. 75, p. 1714-1726, 1994.
HERB, R.; CARROLL, A. R.; YOSHIDA, W. Y.; SCHEUER, P. J.; PAUL, V. J. Polyalkylated cyclopentindoles: cytotoxic fish anti-feedants from a sponge, Axinella sp. Tetrahedron, v. 46, p. 3089-3092, 1990.
INABA, K.; SATO, H., TSUDA, M.; KOBAYASHI, J. Spongiacidins A-D, new bromopyrrole alkaloids from Hymeniacidon sponge. J. nat. Prod., v. 61, p. 693-695, 1998.
KLAUTAU, M.; CUSTÓDIO, M.; BOROJEVIC, R. In vitro culture of primary cell lines from marine sponges. In: Van Soest, R. W. M.; van kempen T. M. G.; Braekman, J. C. (Ed). Sponges in time and space: biology, chemistry, paleontology. Rotterdam: AA Balkema, 1994. p. 401-406.
KOBAYASHI, J.; NAKAMURA, T.; TSUDA, M. Hymenanide F, a new cyclid heptapeptide from marine sponge Hymeniacidon sp. Tetrahedron, v. 52, p. 6355-6360, 1996.
LERNER, C.; MOTHES, B.; CARRARO, J. L. Novos registros e ampliação de limites meridionais de distribuição de poríferos (Porifera, Demospongiae) no Atlântico sudoeste. Rev. Bras. Zool v. 22, p. 596-612, 2005.
LYSEK, N.; KINSCHERF, R.; CLAUS, R.; LINDEL, T. L-5-hydroxytryptophan: antioxidant and anti-apoptotic principle of the intertidal sponge Hymeniacidon heliophila Z. Naturforsch., v. 58c, 568-572, 2003.
MAYER, A. M. S.; RODRIGUEZ, A. D.; BERLINCK, R.; HAMANN, M. T. Marine pharmacology in 2005-6: Marine compounds with antibacterial, anticoagulant, antifungal, anthelmitic, anti-inflammatory, antiprotozoal, and antiviral activities; affecting the cardiovascular, endocrine, immune and nervous systems and other miscellaneous mechanisms of action. BBA-GEN Subjects, v. 1790, p. 283-308, 2009.
MCCLINTOCK, J. B.; BAKER, D. B. J. A review of the chemical ecology of shallow-water Antarctic marine invertebrates. Am. Zool, v. 37, p. 329-342, 1997.
MCCLINTOCK, J. B.; BAKER, B. J.; HAMMAN, M.; SLATTERY, M.; KOPITZKE, R. W.; HEINE. J. Tube-foot chemotactic responses of the spongivorous sea star Perknaster fuscus to organic extracts of antarctic sponges. J. chem. Ecol., v. 20, p. 859-870, 1994
MCCLINTOCK, J. B.; SWENSON, D.; TRAPIDO-ROSENTHAL, H.; BANGHART, L. Ichthyodeterrent properties of lipophilic extracts from Bermudan sponges. J. chem. Ecol., v. 23, p. 1607-1620, 1997.
MORINAKA, B. I., PAWLIK, J. R.; MOLINSKI, T. F. Amaroxocanes A and B: Sulfated dimeric sterols defend the Caribbean coral reef sponge Phorbas amaranthus from fish predators. J. nat. Prod., 72, p. 259-264, 2009.
MURICY, G.; HAJDU, E. Porifera brasilis. Guia de identificação das esponjas marinhas mais comuns do Sudeste do Brasil. Rio de Janeiro:Museu Nacional , 2006, 104 p. (série Livros 17).
MURICY, G.; SILVA, O. Esponjas marinhas do Estado do Rio de Janeiro: um recurso renovável inexplorado. In: SILVA, S. H. G.; LAVRADO, H. P. (Ed.). Ecologia dos ambientes costeiros do Estado do Rio de Janeiro Rio de Janeiro, 1999. (Oecol Brasiliensis, v. 7, PPGE -UFRJ, 1999, p. 156-178).
PARKER, G. H. The reactions of sponges, with a consideration of the origin of the nervous system. J. expl Zool., v. 8, p. 765-805, 1910.
PAWLIK, J. R. A sponge-eating worm from Bermuda: Branchiosyllis oculata (Polychaeta, Syllidae). Mar. Ecol. P.S.Z.N.I, v. 4, p. 65-79, 1983.
PAWLIK, J. R.; KERNAN, M. R.; MOLINSKI, T. F.; HARPER, M. K.; FAULKNER, D. J. Defensive chemicals of the Spanish dancer nudibranch Hexabranchus sanguineus and its egg ribbons: macrolides derived from a sponge diet. J. expl mar. Biol. Ecol., v. 119, p. 99-109, 1988.
PAWLIK, J. R.; CHANAS, B.; TOONEN, R. J.; FENICAL, W. Defenses of Caribbean sponges against predatory reef fish. I. Chemical deterrency. Mar. Ecol. Prog. Ser., v. 127, p. 183-194, 1995.
PENNINGS, S. C.; PABLO, S. R.; PAUL, V. J.; DUFFY, J. E. Effects of sponge secondary metabolites in different diets on feeding by three groups of consumers. J. expl Mar. Biol. Ecol., v. 180, p. 137-149, 1994.
POMPONI, S. A.; WILLOUGHBY, R. Sponge cell culture for production of bioactive metabolites. In: VAN SOEST, R. W. M.; VAN KEMPEN, T. M. G.; BRAEKMAN, J. C. (Ed.). Sponges in time and space: biology, chemistry, paleontology. Rotterdam: AA Balkema, p. 395- 400. 1994.
RANDALL, J. E.; HARTMAN, W. D. Sponge feeding fishes of the West-Indies. Mar. Biol. v. 1, p. 216-225, 1968.
ROGERS, S. D.; PAUL, V. J. Chemical defenses of three Glossodoris nudibranchs and their dietary Hyrtios sponges. Mar. Ecol. Prog. Ser., v. 77, p. 221-232, 1991.
RUPPERT, E. E.; BARNES, R. D. Invertebrate Zoology 6th ed. Orlando, FL: Saunders College Publishing, Harcourt Brace and Company, 1994. 1100 p.
RUZICKA, R.; GLEASON, D. F. Latitudinal variation in spongivorous fishes and the effectiveness of sponge chemical defenses. Oecologia, v. 154, p. 785-794, 2008.
SANTOS, C. P.; COUTINHO, A. B.; HAJDU, E. Spongivory by Eucidaris tribuloides from Salvador, Bahia (Echinodermata: Echinoidea). J. mar. Biol. Assoc. U. K., v. 82, p. 295-297, 2002.
STACHOWICZ , J. J.; HAY, M. E. Geographic variation in camouflage specialization by a decorator crab. The Am. Nat., v. 156, p. 59-71, 2000.
THOMPSON, J. E.; WALKER, R. P.; FAULKNER, D. J. Screening and bioassays for biologically-active substances from forty marine sponges from San Diego, California, USA. Mar. Biol, v. 88, p. 11-21, 1985.
VANCE, R. R. Diet foraging patterns of the sea urchin Centrostephanus coronatus as a predator avoidance strategy. Mar. Biol., v. 51, p. 251-258, 1979.
WADDELL, B.; PAWLIK, J. R. Defenses of Caribbean sponges against invertebrate predators. I. Assays with hermit crabs. Mar. Ecol. Prog. Ser., v. 195, p. 125-132, 2000a.
WADDELL, B.; PAWLIK, J. R. Defenses of Caribbean sponges against invertebrate predators. I. Assays with sea stars. Mar. Ecol. Prog. Ser., v. 195, p. 133-144, 2000b.
WILSON, D. M.; PUYANA, M.; FENICAL, W.; PAWLIK, J. R. Chemical defense of the Caribbean reef sponge Axinella corrugata against predatory fishes. J. chem. Ecol., v. 25, p. 2811-2823, 1999.

Publication Dates

Publication in this collection
31 Jan 2011
Date of issue
Dec 2010

History

Reviewed
11 May 2010
Received
25 Nov 2009
Accepted
28 July 2010

This work is licensed under a Creative Commons Attribution 4.0 International License.

[1] ASSMANN, M.; LICHTE, E.; PAWLIK, J. R.; KOCK, M. Chemical defenses of the Caribbean sponges Agelas widenmayeri and Agelas conifera Mar. Ecol. Prog. Ser., v. 207, p. 255-262, 2000.

[2] AYLING, A. M. The role of biological disturbance in temperate subtidal encrusting communities. Ecology, v. 62, p. 830-847, 1981.

[3] BECERRO, M. A.; THACKER, R. W.; TURON, X.; URIZ, M. J.; PAUL, V. J. Biogeography of sponge chemical ecology: comparisons of tropical and temperate defenses. Oecologia, v. 135, p. 91-101, 2003.

[4] BJORNDAL, K. Digestibility of the sponge Chondrila nucula in the green turtle Chelonia mydas Bull. mar. Sci., v. 47, p. 567-570, 1990.

[5] BLUNT, J. W.; COPP, B. R.; HU, W.; MUNRO M. H. G.; NORTHCOTE, P. T.; PRINSEP, M. Marine natural products. Nat. Prod. Rep, v. 26, p. 170-244, 2009.

[6] BREVES-RAMOS, A.; LAVRADO, H. P.; JUNQUEIRA, A. O. R.; SILVA, S. H. G. Succession in rocky intertidal benthic communities in areas with different pollution levels at Guanabara Bay (RJ-Brazil). Braz. Arch. Biol. Technol., v. 48, p. 951-965, 2005.

[7] BURNS, E.; IFRACH, I.; CARMELI, S.; PAWLIK, J. R.; ILAN, M. Comparison of antipredatory defenses of Red Sea and Caribbean sponges. I. Chemical defense. Mar. Ecol. Prog. Ser., v. 252, p. 105-114, 2003.

[8] CHANAS, B.; PAWLIK, J. R. Defenses of Caribbean sponges against predatory reef fish. II. Spicules, tissue toughness, and nutritional quality. Mar. Ecol. Prog. Ser, v. 127, p. 195-211, 1995

[9] CIMINO, G.; DE ROSA, S.; DE STEFANO, S.; SODANO, G. The chemical defense of four Mediterranean nudibranchs. Comp. Biochem. Physiol., v. 73B, p. 471-474, 1982.

[10] CLAVICO, E. E. G.; MURICY, G.; DA GAMA, B. A. P.; BATISTA, D., VENTURA C. R. R., PEREIRA, R. C. Ecological roles of natural products from the marine sponge Geodia corticostylifera Mar. Biol., v. 148, p. 479-488, 2006.

[11] DUFFY, J. E.; PAUL, V. J. Prey nutritional quality and the effectiveness of chemical defenses against tropical reef fishes. Oecologia, v. 90, p. 333-339. 1992

[12] EPIFANIO, R. de A.; GABRIEL, R.; MARTINS, D. L.; MURICY, G. The sesterterpene variabilin as fish feeding deterrent from Ircinia strobilina Lam. J. chem. Ecol., v. 25, p. 2247-2254, 1999.

[13] FENICAL, W. 2006. Marine pharmaceuticals: Past, present, and future. Oceanography, v. 19, p. 110-119, 2006.

[14] FERREIRA, C. E. L.; GONÇALVES, J. E. A.; COUTINHO, R. Community structure of fishes and habitat complexity on a tropical rocky shore. Environ. Biol. Fish., v. 61, p. 353-369, 2001.

[15] FERREIRA, C. E. L.; FLOETER, S. R.; GASPARINI, J. L.; FERREIRA, B. P.; JOYEUX, J. C. Trophic structure patterns of Brazilian reef fishes: a latitudinal comparison. J. Biogeogr., v. 31, p. 1093-1106, 2004.

[16] GRANATO, A. C.; BERLINCK, R. G. S.; MAGALHÃES, A.; SCHEFER, A. B.; FERREIRA, A. G.; SANCTIS, B.; FREITAS, J. C.; HAJDU, E.; MIGOTTO, A. E. Produtos naturais das esponjas marinhas Aaptos sp., Hymeniacidon aff. heliophila e do nudibrânquio Doris aff. verrucosa Quím. Nova, v. 23, p. 594-599, 2000.

[17] HAY, M. E. Seaweed chemical defenses: their role in the evolution of feeding specialization and in mediating complex interactions. In: PAUL V. J. (ed.). Ecological roles for marine secondary metabolites; explorations in chemical ecology series. New York: Cornell University Press, 1992. p. 93-118.

[18] HAY, M. E. Marine chemical ecology: what's known and what's next? J. expl mar. Biol. Ecol., v. 200, p. 103-134, 1996.

[19] HAY, M. E.; KAPPEL, Q. E.; FENICAL, W. Synergisms in plant defenses against herbivores: interactions of chemistry, calcification, and plant quality. Ecology, v. 75, p. 1714-1726, 1994.

[20] HERB, R.; CARROLL, A. R.; YOSHIDA, W. Y.; SCHEUER, P. J.; PAUL, V. J. Polyalkylated cyclopentindoles: cytotoxic fish anti-feedants from a sponge, Axinella sp. Tetrahedron, v. 46, p. 3089-3092, 1990.

[21] INABA, K.; SATO, H., TSUDA, M.; KOBAYASHI, J. Spongiacidins A-D, new bromopyrrole alkaloids from Hymeniacidon sponge. J. nat. Prod., v. 61, p. 693-695, 1998.

[22] KLAUTAU, M.; CUSTÓDIO, M.; BOROJEVIC, R. In vitro culture of primary cell lines from marine sponges. In: Van Soest, R. W. M.; van kempen T. M. G.; Braekman, J. C. (Ed). Sponges in time and space: biology, chemistry, paleontology. Rotterdam: AA Balkema, 1994. p. 401-406.

[23] KOBAYASHI, J.; NAKAMURA, T.; TSUDA, M. Hymenanide F, a new cyclid heptapeptide from marine sponge Hymeniacidon sp. Tetrahedron, v. 52, p. 6355-6360, 1996.

[24] LERNER, C.; MOTHES, B.; CARRARO, J. L. Novos registros e ampliação de limites meridionais de distribuição de poríferos (Porifera, Demospongiae) no Atlântico sudoeste. Rev. Bras. Zool v. 22, p. 596-612, 2005.

[25] LYSEK, N.; KINSCHERF, R.; CLAUS, R.; LINDEL, T. L-5-hydroxytryptophan: antioxidant and anti-apoptotic principle of the intertidal sponge Hymeniacidon heliophila Z. Naturforsch., v. 58c, 568-572, 2003.

[26] MAYER, A. M. S.; RODRIGUEZ, A. D.; BERLINCK, R.; HAMANN, M. T. Marine pharmacology in 2005-6: Marine compounds with antibacterial, anticoagulant, antifungal, anthelmitic, anti-inflammatory, antiprotozoal, and antiviral activities; affecting the cardiovascular, endocrine, immune and nervous systems and other miscellaneous mechanisms of action. BBA-GEN Subjects, v. 1790, p. 283-308, 2009.

[27] MCCLINTOCK, J. B.; BAKER, D. B. J. A review of the chemical ecology of shallow-water Antarctic marine invertebrates. Am. Zool, v. 37, p. 329-342, 1997.

[28] MCCLINTOCK, J. B.; BAKER, B. J.; HAMMAN, M.; SLATTERY, M.; KOPITZKE, R. W.; HEINE. J. Tube-foot chemotactic responses of the spongivorous sea star Perknaster fuscus to organic extracts of antarctic sponges. J. chem. Ecol., v. 20, p. 859-870, 1994

[29] MCCLINTOCK, J. B.; SWENSON, D.; TRAPIDO-ROSENTHAL, H.; BANGHART, L. Ichthyodeterrent properties of lipophilic extracts from Bermudan sponges. J. chem. Ecol., v. 23, p. 1607-1620, 1997.

[30] MORINAKA, B. I., PAWLIK, J. R.; MOLINSKI, T. F. Amaroxocanes A and B: Sulfated dimeric sterols defend the Caribbean coral reef sponge Phorbas amaranthus from fish predators. J. nat. Prod., 72, p. 259-264, 2009.

[31] MURICY, G.; HAJDU, E. Porifera brasilis. Guia de identificação das esponjas marinhas mais comuns do Sudeste do Brasil. Rio de Janeiro:Museu Nacional , 2006, 104 p. (série Livros 17).

[32] MURICY, G.; SILVA, O. Esponjas marinhas do Estado do Rio de Janeiro: um recurso renovável inexplorado. In: SILVA, S. H. G.; LAVRADO, H. P. (Ed.). Ecologia dos ambientes costeiros do Estado do Rio de Janeiro Rio de Janeiro, 1999. (Oecol Brasiliensis, v. 7, PPGE -UFRJ, 1999, p. 156-178).

[33] PARKER, G. H. The reactions of sponges, with a consideration of the origin of the nervous system. J. expl Zool., v. 8, p. 765-805, 1910.

[34] PAWLIK, J. R. A sponge-eating worm from Bermuda: Branchiosyllis oculata (Polychaeta, Syllidae). Mar. Ecol. P.S.Z.N.I, v. 4, p. 65-79, 1983.

[35] PAWLIK, J. R.; KERNAN, M. R.; MOLINSKI, T. F.; HARPER, M. K.; FAULKNER, D. J. Defensive chemicals of the Spanish dancer nudibranch Hexabranchus sanguineus and its egg ribbons: macrolides derived from a sponge diet. J. expl mar. Biol. Ecol., v. 119, p. 99-109, 1988.

[36] PAWLIK, J. R.; CHANAS, B.; TOONEN, R. J.; FENICAL, W. Defenses of Caribbean sponges against predatory reef fish. I. Chemical deterrency. Mar. Ecol. Prog. Ser., v. 127, p. 183-194, 1995.

[37] PENNINGS, S. C.; PABLO, S. R.; PAUL, V. J.; DUFFY, J. E. Effects of sponge secondary metabolites in different diets on feeding by three groups of consumers. J. expl Mar. Biol. Ecol., v. 180, p. 137-149, 1994.

[38] POMPONI, S. A.; WILLOUGHBY, R. Sponge cell culture for production of bioactive metabolites. In: VAN SOEST, R. W. M.; VAN KEMPEN, T. M. G.; BRAEKMAN, J. C. (Ed.). Sponges in time and space: biology, chemistry, paleontology. Rotterdam: AA Balkema, p. 395- 400. 1994.

[39] RANDALL, J. E.; HARTMAN, W. D. Sponge feeding fishes of the West-Indies. Mar. Biol. v. 1, p. 216-225, 1968.

[40] ROGERS, S. D.; PAUL, V. J. Chemical defenses of three Glossodoris nudibranchs and their dietary Hyrtios sponges. Mar. Ecol. Prog. Ser., v. 77, p. 221-232, 1991.

[41] RUPPERT, E. E.; BARNES, R. D. Invertebrate Zoology 6th ed. Orlando, FL: Saunders College Publishing, Harcourt Brace and Company, 1994. 1100 p.

[42] RUZICKA, R.; GLEASON, D. F. Latitudinal variation in spongivorous fishes and the effectiveness of sponge chemical defenses. Oecologia, v. 154, p. 785-794, 2008.

[43] SANTOS, C. P.; COUTINHO, A. B.; HAJDU, E. Spongivory by Eucidaris tribuloides from Salvador, Bahia (Echinodermata: Echinoidea). J. mar. Biol. Assoc. U. K., v. 82, p. 295-297, 2002.

[44] STACHOWICZ , J. J.; HAY, M. E. Geographic variation in camouflage specialization by a decorator crab. The Am. Nat., v. 156, p. 59-71, 2000.

[45] THOMPSON, J. E.; WALKER, R. P.; FAULKNER, D. J. Screening and bioassays for biologically-active substances from forty marine sponges from San Diego, California, USA. Mar. Biol, v. 88, p. 11-21, 1985.

[46] VANCE, R. R. Diet foraging patterns of the sea urchin Centrostephanus coronatus as a predator avoidance strategy. Mar. Biol., v. 51, p. 251-258, 1979.

[47] WADDELL, B.; PAWLIK, J. R. Defenses of Caribbean sponges against invertebrate predators. I. Assays with hermit crabs. Mar. Ecol. Prog. Ser., v. 195, p. 125-132, 2000a.

[48] WADDELL, B.; PAWLIK, J. R. Defenses of Caribbean sponges against invertebrate predators. I. Assays with sea stars. Mar. Ecol. Prog. Ser., v. 195, p. 133-144, 2000b.

[49] WILSON, D. M.; PUYANA, M.; FENICAL, W.; PAWLIK, J. R. Chemical defense of the Caribbean reef sponge Axinella corrugata against predatory fishes. J. chem. Ecol., v. 25, p. 2811-2823, 1999.

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Chemical defense of Hymeniacidon heliophila (Porifera: halichondrida) against tropical predators

Abstracts

Publication Dates

History