Chemical defenses of the tropical marine seaweed Canistrocarpus cervicornis against herbivory by sea urchin

Bianco, Éverson Miguel; Teixeira, Valéria Laneuville; Pereira, Renato Crespo

Abstracts

This paper reports on the defensive chemical properties of the marine tropical brown seaweed Canistrocarpus cervicornis against herbivory. A natural concentration of dichloromethane crude extract (DCE) obtained from this seaweed significantly inhibited feeding by the sea urchin Lytechinus variegatus. The major metabolite isolated from this active DCE extract was identified as the (4R,7R,14S)-4α,7α-diacetoxy-14-hydroxydolast-1(15),8-diene that strongly inhibited feeding by the same sea urchin. This result suggests that the dolastane diterpenes class may constitute the defensive system of C. cervicornis against herbivory, and probably also of that of other brown seaweeds endowed with a biosynthetic pathway capable of producing compounds of the dolastane-type, a typical skeleton found in Dyctioteae species worldwide. This is the first report showing this compound-type (dolastane diterpenes) as a chemical defense against herbivory in marine seaweeds. This study constitutes an additional report broadening the known spectrum of action and roles of secondary metabolites of the C. cervicornis and Dyctioteae species.

Canistrocarpus cervicornis; Chemical defenses; Dolastanes; Diterpenes

Este artigo demonstra a química defensiva anti-herbivoria da macroalga parda marinha Canistrocarpus cervicornis. Em sua concentração natural, o extrato bruto em diclorometano (DCE) inibiu significativamente o consumo alimentar do ouriço-do-mar Lytechinus variegatus. Deste extrato em DCE foi isolado o metabólito majoritário identificado como o diterpeno (4R,7R,14S)-4α,7α-diacetoxi-14-hidroxidolasta-1(15),8-dieno. Esses resultados comprovam que diterpenos da classe dolastano podem compor o sistema defensivo anti-herbivoria de C. cervircornis e, supostamente, o de outras algas pardas capazes de produzi-los, uma vez que são composto típicos encontrados em esqueletos de Dyctiotas em todo o mundo. Este é o primeiro estudo demonstrando a ação anti-herbivoria desta classe de metabolitos (diterpenos dolastanos) em macroalgas marinhas. Tais informações ampliam o conhecimento sobre o papel desses metabolitos especiais em C. cervicornis e de espécies de Dyctiotae.

Canistrocarpus cervicornis; Defesas químicas; Dolastanos; Diterpenos

AMSLER, C. D.; FAIRHEAD, V. A. Defensive and sensory chemical ecology of brown algae. Adv. Bot. Res., v. 43, p. 1-91, 2006.
BARBOSA, J. P.; TEIXEIRA, V. L.; PEREIRA, R. C. A dolabellane diterpene from the brown alga Dictyota pfaffii as chemical defense against herbivores. Bot. Mar., v. 47, p. 147-151, 2004.
BIANCO, E.M.; ROGERS, R.; TEIXEIRA V.L.; PEREIRA, R.C. Antifoulant diterpenes produced by the brown seaweed Canistrocarpus cervicornis J. Appl. Phycol., v. 21, p. 341-346, 2009.
BLUNT J.W.; COPP B.R.; MUNRO, M.H.G.; NORTHCOTE, P.T.; PRINSEP, M.R. Marine natural products. Nat. Prod. Rep., v. 27, p. 165-237, 2010.
CRONIN, G.; HAY, M. E. Chemical defenses, protein content, and susceptibility to herbivory of diploid vs. haploid stages of the isomorphic brown alga Dictyota ciliolata (Phaeophyta). Bot. Mar., v. 39, p. 395-399, 1996.
CRONIN, G.; PAUL, V. J.; HAY, M. E.; FENICAL, W. Are tropical herbivores more resistant than temperate herbivores to seaweed chemical defenses? Diterpenoid metabolites from Dictyota acutiloba as feeding deterrents for tropical versus temperate fishes and urchins. J. Chem. Ecol., v. 23, p. 289-302, 1997.
DE CLERCK, O.; LELIAERT, F.; VERBRUGGEN, H.; LANE, C. E.; DE PAULA, J. C.; PAYO, D. I.; COPPEJANS, E. A revised classification of the Dictyoteae (Dictyotales, Phaeophyceae) based on rbcL and 26S ribosomal DNA sequence data analyses. J. Phycol., v. 42, p. 1271-1288, 2006.
DE LARA-IASSI, G.; ÁLVAREZ-HERNÁNDEZ, S.; COLLADO-VIDES, L. Ichthyotoxic activity of extracts from Mexican marine macroalgae. J. Appl. Phycol., v. 12, p. 45-52, 2000.
DE PAULA, J. C.; CASSANO, V.; YONESHIGUE-VALENTIN, Y.; TEIXEIRA, V. L. Diterpenes from the Brazilian brown alga Dictyota crispata (Dictyotaceae, Phaeophyta). Nat. Prod. Comm., v. 2, p. 135-137, 2007.
GARCIA, D. G.; BIANCO, E. M.; SANTOS, M. C. B.; PREIRA, R. C.; FARIA, M. V. C.; TEIXEIRA, V. L.; BURTH, P. Inhibition of Mammal Na⁺K⁺-ATPase by diterpenes extracted from the Brazilian brown alga Dictyota cervicornis Phytother. Res., v. 23, p. 943-947, 2009.
GONZÁLEZ, A. G.; MARTIN, J. D.; NORTE, M.; RIVERA, P.; PERALES, A.; FAYOS, J. F. Structure and absolute configurations of Dictyota sp. diterpenes. Tetrahedron, v. 39, p. 3355-3357, 1983.
HAY, M. E.; DUFFY, J. E.; PFISTER, C. A.; FENICAL, W. Chemical defense against different marine herbivores: are amphipods insects equivalents? Ecology, v. 68, p. 1567-1580, 1987a.
HAY, M. E.; FENICAL, W.; GUSTAFSON, K. Chemical defense against diverse coral-reef herbivores. Ecology, v. 68, p. 1581-1591, 1987b.
HAY, M. E.; FENICAL, W. Marine plant-herbivore interactions: the ecology of chemical defense. Ann. Rev. Ecol. Syst., v. 19, p. 111-145, 1988.
HAY, M. E.; DUFFY, J. E.; FENICAL, W. Seaweed chemical defenses: among compound and among-herbivore variance. Int. Coral Reef Symp., 6., Australia, 1988. v. 3, 43-48, 1988a.
HAY, M. E.; RENAUD, P. E.; FENICAL, W. Large mobile versus small sedentary herbivores and their resistance to seaweed chemical defenses. Oecologia, v. 75, p. 246-252, 1988b.
HAY, M. E.; DUFFY, J. E.; FENICAL, W. Host-plant specialization decreases predation on a marine amphipod: an herbivore in plant's clothing. Ecology, v. 71, p. 733-743, 1990.
HAY, M. E.; STEINBERG, P. D. The chemical ecology of plant-herbivore interactions in marine versus terrestrial communities. In: ROSENTHAL, G. A.; BERENBAUM, M. R. (Ed.) Herbivores: their interactions with secondary plant metabolites Academic Press, San Diego, California, USA., v 2, p. 371-413, 1992.
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.
JOHN, D. M.; HAWKINS, S. J.; PRICE, J. H. Plant-animal interactions in the marine benthos Clarendon Press, Oxford, England, 1992.
KELECOM, A.; TEIXEIRA, V. L. Dolastane diterpenes from the marine brown alga Dictyota cervicornis Phytochemistry, v. 27, p. 2907-2909, 1988.
LEWIS, S. M. The role of herbivorous fishes in the organization of a Caribbean reef community. Ecol. Monogr., v. 56, p. 183-200, 1986.
LITTLER, M. M.; TAYLOR, P. R.; LITTLER, D. S. Algal resistance to herbivory on a Caribbean barrier reef. Coral Reefs, v. 2, p.111-118, 1983.
MARQUES, L. V.; VILLAÇA, R.; PEREIRA, R. C. Susceptibility of macroalgae to herbivorous fishes at Rocas Atoll, Brazil. Bot. Mar., 49: 379-385, 2006.
PAUL, V. J. Ecological roles of marine natural products, 1^st ed. New York: Comstock Publishing Associates -Cornell University Press, 1992.
PAUL, V. J.; CRUZ-RIVERA, E.; THACKER, R. W. Chemical mediation of macroalgal herbivore interactions: ecological and evolutionary perspectives. In: MCCLINTOCK, J. B.; BAKER, B. J. (Ed.). Marine chemical ecology Boca Raton, Fla.: CRC Press, 2001. p. 227-265, 2001.
PAUL, V. J.; PUGLISI, M. P.; RITSON-WILLIAMS, R. Marine chemical ecology. Nat. Prod. Rep., v. 23, p. 153-180, 2006.
PEREIRA, R. C.; TEIXEIRA, V. L.; KELECOM, A. Chemical defenses against herbivores in marine algae. 1. The brown alga Dictyota dichotoma (Hudson) Lamouroux from Brazil. An. Acad. Bras. Ci., v. 66, p. 229-235, 1994.
PEREIRA, R. C.; CAVALCANTI, D. N.; TEIXEIRA, V. L. Effects of secondary metabolites from the tropical Brazilian brown alga Dictyota menstrualis on the amphipod Parhyale hawaiensis Mar. Ecol. Prog. Ser., v. 205, p. 95-100, 2000a.
PEREIRA, R. C.; DONATO, R.; TEIXEIRA, V. L.; CAVALCANTI, D. N. Chemotaxis and chemical defenses in seaweed susceptibility to herbivory. Rev. Bras. Biol., v. 60, p. 405-414, 2000b.
PEREIRA, R. C.; PINHEIRO, M. D.; TEIXEIRA, V. L.; DA GAMA, B. A. P. Feeding preferences of the endemic gastropod Astraea latispina in relation to chemical defenses of Brazilian tropical seaweeds. Braz. J. Biol., v. 62, p. 33-40, 2002.
PEREIRA, R. C.; DA GAMA, B. A. P. Macroalgal chemical defenses and their role in structuring tropical marine communities. In: AMSLER, C. D. (Ed.). Algal Chemical Ecology New York: Springer, p. 25-55, 2008.
SCHMITT, T. M.; HAY, M. E.; LINDQUIST, N. Constraints on chemically mediated coevolution: multiple functions for seaweed secondary metabolites. Ecology, v. 76, p. 107-123, 1995.
SOUZA, C. F.; OLIVEIRA, A. S.; PEREIRA, R. C. Feeding preference of the sea urchin Lytechinus variagatus (Lamarck, 1816) on seaweeds. Braz. J. Oceanogr., v. 56, p. 239-247, 2008.
SUN, H. H.; MCCONNELL, O. J.; FENICAL, W.; HIROTSU, K.; CLARDY, J. Tricyclic diterpenoids of the dolastane ring system from the marine alga Dictyota divaricata Tetrahedron, v. 37, p. 1237-1242, 1981.
TEIXEIRA, V. L.; KELECOM, A. Geographic distribution of the diterpenes from the marine brown alga Dictyota Lamouroux (Dictyotales, Phaeophyta). Nerítica, v. 2, p. 179-200, 1987.
TEIXEIRA, V. L.; TOMASSINI, T.; FLEURY, B. G.; KELECOM, A. Dolastane and secodolastane diterpenes from the marine brown alga Dictyota cervicornis J. Nat. Prod., v. 49, p. 570-575, 1986a.
TEIXEIRA, V. L.; TOMASSINI, T.; KELECOM, A. Cervicol, a further secodolastane diterpene from the marine brown alga Dictyota cervicornis Kützing. Bull. Soc.Chim. Belg., v. 95, p. 263-268, 1986b.
VALLIM, M. A., DE PAULA, J. C., PEREIRA, R. C., TEIXEIRA, V. L. The diterpenes from Dictyotacean marine brown algae in the Tropical Atlantic American region. Biochem. Syst. Ecol., v. 33, p. 1-16, 2005.

Publication Dates

Publication in this collection
03 Nov 2010
Date of issue
Sept 2010

History

Accepted
14 Apr 2010
Reviewed
25 Mar 2010
Received
02 Nov 2009

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

[1] AMSLER, C. D.; FAIRHEAD, V. A. Defensive and sensory chemical ecology of brown algae. Adv. Bot. Res., v. 43, p. 1-91, 2006.

[2] BARBOSA, J. P.; TEIXEIRA, V. L.; PEREIRA, R. C. A dolabellane diterpene from the brown alga Dictyota pfaffii as chemical defense against herbivores. Bot. Mar., v. 47, p. 147-151, 2004.

[3] BIANCO, E.M.; ROGERS, R.; TEIXEIRA V.L.; PEREIRA, R.C. Antifoulant diterpenes produced by the brown seaweed Canistrocarpus cervicornis J. Appl. Phycol., v. 21, p. 341-346, 2009.

[4] BLUNT J.W.; COPP B.R.; MUNRO, M.H.G.; NORTHCOTE, P.T.; PRINSEP, M.R. Marine natural products. Nat. Prod. Rep., v. 27, p. 165-237, 2010.

[5] CRONIN, G.; HAY, M. E. Chemical defenses, protein content, and susceptibility to herbivory of diploid vs. haploid stages of the isomorphic brown alga Dictyota ciliolata (Phaeophyta). Bot. Mar., v. 39, p. 395-399, 1996.

[6] CRONIN, G.; PAUL, V. J.; HAY, M. E.; FENICAL, W. Are tropical herbivores more resistant than temperate herbivores to seaweed chemical defenses? Diterpenoid metabolites from Dictyota acutiloba as feeding deterrents for tropical versus temperate fishes and urchins. J. Chem. Ecol., v. 23, p. 289-302, 1997.

[7] DE CLERCK, O.; LELIAERT, F.; VERBRUGGEN, H.; LANE, C. E.; DE PAULA, J. C.; PAYO, D. I.; COPPEJANS, E. A revised classification of the Dictyoteae (Dictyotales, Phaeophyceae) based on rbcL and 26S ribosomal DNA sequence data analyses. J. Phycol., v. 42, p. 1271-1288, 2006.

[8] DE LARA-IASSI, G.; ÁLVAREZ-HERNÁNDEZ, S.; COLLADO-VIDES, L. Ichthyotoxic activity of extracts from Mexican marine macroalgae. J. Appl. Phycol., v. 12, p. 45-52, 2000.

[9] DE PAULA, J. C.; CASSANO, V.; YONESHIGUE-VALENTIN, Y.; TEIXEIRA, V. L. Diterpenes from the Brazilian brown alga Dictyota crispata (Dictyotaceae, Phaeophyta). Nat. Prod. Comm., v. 2, p. 135-137, 2007.

[10] GARCIA, D. G.; BIANCO, E. M.; SANTOS, M. C. B.; PREIRA, R. C.; FARIA, M. V. C.; TEIXEIRA, V. L.; BURTH, P. Inhibition of Mammal Na⁺K⁺-ATPase by diterpenes extracted from the Brazilian brown alga Dictyota cervicornis Phytother. Res., v. 23, p. 943-947, 2009.

[11] GONZÁLEZ, A. G.; MARTIN, J. D.; NORTE, M.; RIVERA, P.; PERALES, A.; FAYOS, J. F. Structure and absolute configurations of Dictyota sp. diterpenes. Tetrahedron, v. 39, p. 3355-3357, 1983.

[12] HAY, M. E.; DUFFY, J. E.; PFISTER, C. A.; FENICAL, W. Chemical defense against different marine herbivores: are amphipods insects equivalents? Ecology, v. 68, p. 1567-1580, 1987a.

[13] HAY, M. E.; FENICAL, W.; GUSTAFSON, K. Chemical defense against diverse coral-reef herbivores. Ecology, v. 68, p. 1581-1591, 1987b.

[14] HAY, M. E.; FENICAL, W. Marine plant-herbivore interactions: the ecology of chemical defense. Ann. Rev. Ecol. Syst., v. 19, p. 111-145, 1988.

[15] HAY, M. E.; DUFFY, J. E.; FENICAL, W. Seaweed chemical defenses: among compound and among-herbivore variance. Int. Coral Reef Symp., 6., Australia, 1988. v. 3, 43-48, 1988a.

[16] HAY, M. E.; RENAUD, P. E.; FENICAL, W. Large mobile versus small sedentary herbivores and their resistance to seaweed chemical defenses. Oecologia, v. 75, p. 246-252, 1988b.

[17] HAY, M. E.; DUFFY, J. E.; FENICAL, W. Host-plant specialization decreases predation on a marine amphipod: an herbivore in plant's clothing. Ecology, v. 71, p. 733-743, 1990.

[18] HAY, M. E.; STEINBERG, P. D. The chemical ecology of plant-herbivore interactions in marine versus terrestrial communities. In: ROSENTHAL, G. A.; BERENBAUM, M. R. (Ed.) Herbivores: their interactions with secondary plant metabolites Academic Press, San Diego, California, USA., v 2, p. 371-413, 1992.

[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] JOHN, D. M.; HAWKINS, S. J.; PRICE, J. H. Plant-animal interactions in the marine benthos Clarendon Press, Oxford, England, 1992.

[21] KELECOM, A.; TEIXEIRA, V. L. Dolastane diterpenes from the marine brown alga Dictyota cervicornis Phytochemistry, v. 27, p. 2907-2909, 1988.

[22] LEWIS, S. M. The role of herbivorous fishes in the organization of a Caribbean reef community. Ecol. Monogr., v. 56, p. 183-200, 1986.

[23] LITTLER, M. M.; TAYLOR, P. R.; LITTLER, D. S. Algal resistance to herbivory on a Caribbean barrier reef. Coral Reefs, v. 2, p.111-118, 1983.

[24] MARQUES, L. V.; VILLAÇA, R.; PEREIRA, R. C. Susceptibility of macroalgae to herbivorous fishes at Rocas Atoll, Brazil. Bot. Mar., 49: 379-385, 2006.

[25] PAUL, V. J. Ecological roles of marine natural products, 1^st ed. New York: Comstock Publishing Associates -Cornell University Press, 1992.

[26] PAUL, V. J.; CRUZ-RIVERA, E.; THACKER, R. W. Chemical mediation of macroalgal herbivore interactions: ecological and evolutionary perspectives. In: MCCLINTOCK, J. B.; BAKER, B. J. (Ed.). Marine chemical ecology Boca Raton, Fla.: CRC Press, 2001. p. 227-265, 2001.

[27] PAUL, V. J.; PUGLISI, M. P.; RITSON-WILLIAMS, R. Marine chemical ecology. Nat. Prod. Rep., v. 23, p. 153-180, 2006.

[28] PEREIRA, R. C.; TEIXEIRA, V. L.; KELECOM, A. Chemical defenses against herbivores in marine algae. 1. The brown alga Dictyota dichotoma (Hudson) Lamouroux from Brazil. An. Acad. Bras. Ci., v. 66, p. 229-235, 1994.

[29] PEREIRA, R. C.; CAVALCANTI, D. N.; TEIXEIRA, V. L. Effects of secondary metabolites from the tropical Brazilian brown alga Dictyota menstrualis on the amphipod Parhyale hawaiensis Mar. Ecol. Prog. Ser., v. 205, p. 95-100, 2000a.

[30] PEREIRA, R. C.; DONATO, R.; TEIXEIRA, V. L.; CAVALCANTI, D. N. Chemotaxis and chemical defenses in seaweed susceptibility to herbivory. Rev. Bras. Biol., v. 60, p. 405-414, 2000b.

[31] PEREIRA, R. C.; PINHEIRO, M. D.; TEIXEIRA, V. L.; DA GAMA, B. A. P. Feeding preferences of the endemic gastropod Astraea latispina in relation to chemical defenses of Brazilian tropical seaweeds. Braz. J. Biol., v. 62, p. 33-40, 2002.

[32] PEREIRA, R. C.; DA GAMA, B. A. P. Macroalgal chemical defenses and their role in structuring tropical marine communities. In: AMSLER, C. D. (Ed.). Algal Chemical Ecology New York: Springer, p. 25-55, 2008.

[33] SCHMITT, T. M.; HAY, M. E.; LINDQUIST, N. Constraints on chemically mediated coevolution: multiple functions for seaweed secondary metabolites. Ecology, v. 76, p. 107-123, 1995.

[34] SOUZA, C. F.; OLIVEIRA, A. S.; PEREIRA, R. C. Feeding preference of the sea urchin Lytechinus variagatus (Lamarck, 1816) on seaweeds. Braz. J. Oceanogr., v. 56, p. 239-247, 2008.

[35] SUN, H. H.; MCCONNELL, O. J.; FENICAL, W.; HIROTSU, K.; CLARDY, J. Tricyclic diterpenoids of the dolastane ring system from the marine alga Dictyota divaricata Tetrahedron, v. 37, p. 1237-1242, 1981.

[36] TEIXEIRA, V. L.; KELECOM, A. Geographic distribution of the diterpenes from the marine brown alga Dictyota Lamouroux (Dictyotales, Phaeophyta). Nerítica, v. 2, p. 179-200, 1987.

[37] TEIXEIRA, V. L.; TOMASSINI, T.; FLEURY, B. G.; KELECOM, A. Dolastane and secodolastane diterpenes from the marine brown alga Dictyota cervicornis J. Nat. Prod., v. 49, p. 570-575, 1986a.

[38] TEIXEIRA, V. L.; TOMASSINI, T.; KELECOM, A. Cervicol, a further secodolastane diterpene from the marine brown alga Dictyota cervicornis Kützing. Bull. Soc.Chim. Belg., v. 95, p. 263-268, 1986b.

[39] VALLIM, M. A., DE PAULA, J. C., PEREIRA, R. C., TEIXEIRA, V. L. The diterpenes from Dictyotacean marine brown algae in the Tropical Atlantic American region. Biochem. Syst. Ecol., v. 33, p. 1-16, 2005.

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Chemical defenses of the tropical marine seaweed Canistrocarpus cervicornis against herbivory by sea urchin

Abstracts

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History