Publicado

2019-05-01

Experimental Approaches for the Evaluation of Allelopathic Interactions Between Hermatypic Corals and Marine Benthic Cyanobacteria in the Colombian Caribbean

Aproximaciones experimentales para la evaluación de interacciones alelopáticas entre corales hermatípicos y cianobacterias marinas bentónicas en el Caribe Colombiano

DOI:

https://doi.org/10.15446/abc.v24n2.72706

Palabras clave:

Alellopathy, corals, cyanobacteria, interspecific competition (en)
Alelopatía, cianobacterias, competencia interespecífica, corales (es)

Autores/as

  • Mónica Puyana Universidad Jorge Tadeo Lozano - Departamento de Ciencias Biológicas y Ambientales
  • Julián Alberto Prato Universidad Nacional de Colombia - Sede Caribe
  • Christian Felipe Nieto Universidad Nacional Autónoma de México
  • Freddy Alejandro Ramos Universidad Nacional de Colombia - Sede Bogotá - Departamento de Química
  • Leonardo Castellanos Universidad Nacional de Colombia - Sede Bogotá - Departamento de Química
  • Paola Pinzón Universidad Jorge Tadeo Lozano - Departamento de Ciencias Biológicas y Ambientales
  • Juan Camilo Zárate Investigador científico - CEINER LTDA

Blooms of marine benthic cyanobacteria are recurrent in several locations at the Colombian Caribbean. In these events, cyanobacteria grow over the substrate and benthic organisms although their effect has not been fully assessed. This study evaluated interactions between cyanobacteria and hermatypic corals, in order to identify any deleterious effects that could be related to allelopathic mechanisms. Organic extracts from cyanobacteria collected in San Andres, Old Providence and Rosario islands were tested against embryos of the reef-building coral Orbicella annularis. The indirect effect of cyanobacterial extracts was also assessed by resuspending the extracts in seawater and monitoring polyp retraction and recovery of the coral Madracis mirabilis (=auretenra). Additionally, the effect of direct contact between cyanobacterial extracts and the coral Porites porites was assessed by incorporating cyanobacterial extracts into PhytagelTM gels and placed in direct contact with the coral. After 24, 48 and 72 h of exposure, chromatographic profiles of associated zooxanthellae was evaluated by HPLC. A deleterious effect on the zooxanthellae was evidenced by an increase in pheophytin, a degradation product from chlorophyll. The competitive abilities of algae and cyanobacteria should be considered as a constraint to reef restoration initiatives. Cyanobacteria have the ability to compete with corals due to their growth rates, defenses against herbivory and potentially allelopathic mechanisms.

Afloramientos de cianobacterias marinas bentónicas son recurrentes en varias localidades del Caribe colombiano. En estos eventos, las cianobacterias crecen sobre el sustrato y organismos bentónicos sin que su efecto se haya evaluado completamente. Este estudio evaluó interacciones entre cianobacterias y corales hermatípicos con el fin de identificar efectos perjudiciales que podrían estar relacionados con mecanismos alelopáticos. Extractos orgánicos de cianobacterias recolectadas en las islas de San Andrés, Providencia y las Islas del Rosario fueron evaluados contra embriones del coral hermatípico Orbicella annularis. También se evaluó el efecto indirecto de extractos de cianobacterias resuspendidos en agua de mar para determinar retracción de pólipos y recuperación del coral Madracis mirabilis (=auretenra). Adicionalmente, se evaluó el efecto del contacto directo de extractos de cianobacterias y el coral Porites porites mediante la incorporación de los extractos en geles de PhytagelTM dispuestos en contacto directo con el coral. Después de 24, 48 y 72 h de exposición, los perfiles cromatográficos de las zooxantelas asociadas al coral fueron evaluados por HPLC. Un efecto negativo sobre las zooxantelas se evidenció por el incremento en feofitina, producto de degradación de la clorofila. Las capacidades competitivas de algas y cianobacterias debieran considerarse como un factor que podría incidir negativamente en iniciativas de restauración arrecifal. Las cianobacterias tienen la capacidad de competir con corales debido a sus tasas de crecimiento, defensas contra herbivoría y potenciales mecanismos alelopáticos.

Referencias

Alvarado E, Acosta A. Fertilidad y fecundidad de Montastraea annularis en un arrecife degradado. Bol Invest Mar Cost. 2009;38(2):91-108. Doi: https://doi.org/10.25268/bimc.invemar.2009.38.2.173

Baumgartner L, Reid R, Dupraz C, Decho A, Buckely D, Spear J, et al. Sulfate reducing bacteria in microbial mats: changing paradigms, new discoveries. Sediment. Geol. 2006;185(3-4):131-145. Doi: https://doi.org/10.1016/j.sedgeo.2005.12.008

Berry JP, Gantar M, Perez MH, Berry G, Noriega FG. Cyanobacterial Toxins as allelochemicals with potential applications as algaecides, herbicides and insecticides. Mar. Drugs. 2008;6(2):117-146. Doi: https://doi.org/10.3390/md20080007

Birkeland C. Life and Death of Coral reefs. Chapman and Hall, New York. 1997. 536 p.

Birrell CL, McCook LJ, Willis BL. Effects of algal turfs and sediment on coral settlement. Mar. Pollut. Bull. 2005;51(1-4):408-414.Doi: https://doi.org/10.1016/j.marpolbul.2004.10.022

Cartaxana P, Jesus B, Brotas V. Pheophorbide and pheophytin a-like pigments as useful markers for intertidal microphytobenthos grazing by Hydrobia ulvae. Estuar. Coast. Shelf S. 2003;58(2):293–297. Doi: https://doi.org/10.1016/S0272-7714(03)00081-7

Chadwick NE, Morrow KM. Competition among sessile organisms on coral reefs. In: Dubinsky Z, Stambler N, editors. Coral reefs: An ecosystem in transition. Springer. Heidelberg, London, New York; 2011. p. 347-371.

Chaves‐Fonnegra A, Castellanos L, Zea S, Duque C, Rodríguez J, Jiménez C. Clionapirrolidine A, a metabolite from the encrusting and excavating sponge Cliona tenuis that kills coral tissue upon contact. J.Chem. Ecol. 2008;34(12):1565–1574. Doi: https://doi.org/10.1007/s10886-008-9565-5

De Nys R, Coll J, Price I. Chemically mediated interactions between the red alga Plocamium hamatum (Rhodophyta) and the octocoral Sinularia cruciata (Alcyonacea). Mar. Biol. 1991;108:315-320.

Diaz-Pulido G, Harii, S, McCook LJ, Hoegh-Guldberg O. The impact of benthic algae on the settlement of a reef-building coral. Coral Reefs. 2010;29(1):203-208. Doi https://doi.org/10.1007/s00338-009-0573-x

Engel S, Pawlik JR. Allelopathic activities of sponge extracts. Mar. Ecol. Prog. Ser. 2000;207:273-281.

Engene N, Choi H, Esquenazi E, Rottacker E, Ellisman MH, Dorrestein PC, et al. Underestimated biodiversity as a major explanation for the perceived rich secondary metabolite capacity of the cyanobacterial genus Lyngbya. Environ. Microbiol. 2011;13(6):1601–1610. Doi: https://doi.org/10.1111/J.1462-2920.2011.02472.X

Engene N, Rottacker EC, Kasvtovsky J, Byrum T, Choi H, Ellisman MH, et al. Moorea producens gen. nov., sp. nov. and Moorea bouillonii comb. nov., tropical marine cyanobacteria rich in bioactive secondary metabolites. Int. J. Syst. Evol. Micr. 2012;62:1171–1178. Doi: https://doi.org/10.1099/ijs.0.033761-0

Engene N, Paul VJ, Byrum T, Gerwick WH, Thor A, Ellisman MH. Five chemically rich species of tropical marine cyanobacteria of the genus Okeania gen. nov. (Oscillatoriales, Cyanoprokaryota). J. Phycol. 2013;49(6):1095–1106. Doi: https://doi.org/10.1111/jpy.12115

Engene N, Gunasekera S, Gerwick WH, Paul VJ. Phylogenetic inferences reveal a large extent of novel biodiversity in chemically rich tropical marine cyanobacteria. Appl. Environ. Microb. 2013;79(6):1882-1888. Doi: https://doi.org/10.1128/AEM.03793-12

Engene N, Tronholm A, Paul VJ. Uncovering cryptic diversity of Lyngbya: the new tropical marine cyanobacterial genus Dapis (Oscillatoriales). J. Phycol. 2018;54(4):435-446. Doi: https://doi.org/10.1111/jpy.12752.

Fearon RJ, Cameron AM. Preliminary evidence supporting the ability of hermatypic corals to affect adversely larvae and early settlement stages of hard coral competitors. J. Chem. Ecol. 1997;23(7):1769-1780.

Ford AK, Bejarano S, Nugues MM, Visser PM, Albert S, Ferse SCA. Reefs under Siege-the Rise, putative drivers, and consequences of benthic cyanobacterial Mats. Front. Mar. Sci. 2018;5:18. Doi: https://doi.org/10.3389/fmars.2018.00018

Horvarth C, Melander W, Molnar I, Molnar P. Enhancement of retention by ion-pair formation in Liquid Chromatography with Nonpolar Stationary Phases. Anal. Chem. 1977;49(14):2295-2305.

Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, et al. Phase shifts, herbivory and the resilience of coral reefs to climate change. Curr. Biol. 2007;17(4):360-365. Doi: https://doi.org/10.1016/j.cub.2006.12.049

Jennings S, Polunin NVC. Impacts of fishing on tropical reef ecosystems. Ambio 1996;25(1):44–49.

Jüttner F, Todorova AK, Walch N, von Philipsborn W. Nostocyclamide M. A cyanobacterial cyclic peptide with allelopathic activity from Nostoc 31. Phytochemistry. 2001,57(4):613-619. Doi: https://doi.org/10.1016/S0031-9422(00)00470-2

Kleppel G, Dodge R, Reese C. Changes in pigmentation associated with the bleaching of stony corals. Limnol. Oceanogr. 1989;34(7):1331-1335.

Knowlton N, Rohwer F. Multispecies Microbial Mutualisms on Coral Reefs: The Host as a Habitat. Am. Nat. 2003;(162):S51-S62.

Komárek J, Anagnostidis K. Cyanoprokaryota. 2 Teil/2nd Part: Oscillatoriales. In: Büdel B, Krienitz L, Gärtner G, Schagerl M, editors. Süsswasserflora von Mitteleuropa. Vol. 19/2. Elsevier/Spektrum. Heidelberg. 2005. p. 1-759.

Kuffner IB, Paul VJ. Effects of the benthic cyanobacterium Lyngbya majuscula on larval recruitment of the reef corals Acropora surculosa and Pocillopora damicornis. Coral Reefs. 2004;23(3):455–458. Doi: https://doi.org/ 10.1007/s00338-004-0416-8

Kuffner IB, Walters LJ, Becerro MA, Paul VJ, Ritson-Williams R, Beach KS. Inhibition of coral recruitment by macroalgae and cyanobacteria. Mar. Ecol. Prog. Ser. 2006;323:107-117. Doi: https://doi.org/10.3354/meps323107

Leão PN, Engene N, Antunes A, Gerwick WH, Vasconcelos V. The chemical ecology of cyanobacteria. Nat. Prod. Rep. 2012;29(3):372-391. Doi: https://doi.org/10.1039/c2np00075j.

Levy O, Dubinsky Z, Achituv Y. Photobehavior of stony corals: responses to light spectra and intensity. J. Exp. Biol. 2003;206:4041-4049.

Littler DS, Littler MM. Epizoic red alga allelopathic (?) to a Caribbean coral. Coral Reefs. 1997,16:168.

Louda J, Loitz J, Rudnick D, Baker E. Early diagenetic alteration of chlorophyll-a and bacteriochlorophyll-a in a contemporaneous marl ecosystem, Florida Bay. Org. Chem. 2000;31(12):1561-1580. Doi: https://doi.org/10.1016/S0146-6380(00)00071-1

McCook LJ, Jompa J, Diaz-Pulido G. Competition between corals and algae on coral reefs: A review of evidence and mechanisms. Coral Reefs. 2001;19(4):400-417. Doi: https://doi.org/10.1007/s003380000129

Moberg F, Folke C. Analysis: Ecological goods and services of coral reef ecosystems. Ecol. Econ. 1999;29(2):215-233. Doi: https://doi.org/10.1016/S0921-8009(99)00009-9

Mumby PJ, Steneck R. Coral reef management and conservation in the light of rapidly evolving ecological paradigms. Trends Ecol. Evol. 2008,23(10):555-563. Doi: https://doi.org/10.1016/j.tree.2008.06.011

Nagle D, Paul VJ. Chemical defense of a marine cyanobacterial bloom. J. Exp. Mar. Biol. Ecol. 1998;225(1):29-38. Doi: https://doi.org/10.1016/S0022-0981(97)00205-0

Paul VJ, Thacker R, Banks K, Golubic S. Benthic cyanobacterial bloom impacts the reefs of South Florida (Broward County, USA). Coral Reefs. 2005,24(4):693-697. Doi: https://doi.org/10.1007/s00338-005-0061-x

Petrichtcheva NV, Duque C, Dueñas A, Zea S, Hara N, Fujimoto Y. New Nitrogenous eudesmane-type compounds isolated from the Caribbean Sponge Axinyssa ambrosia. J. Nat. Prod. 2002;65(6):851-855.

Puyana M. The fate of corals: will they overcome competition with algae and cyanobacteria in a changing environment? In: Duque Beltran C, Tello Camacho E. editors. Corals in a changing world. Croatia: InTech Publishers. 2018. Doi: http://www.doi.org/10.5772/intechopen.71568

Puyana M, Acosta A, Bernal-Sotelo K, Velásquez-Rodríguez T, Ramos F. Spatial scale of cyanobacterial blooms in Old Providence Island, Colombian Caribbean. Univ. Sci. 2015;20(1):83-105. Doi: http://www.doi.org/10.11144/Javeriana.SC20-1.sscb.

Puyana M, Prato J. Overgrowth of reef organisms by benthic cyanobacteria in the Colombian Caribbean. Mutis 2013;3(2):58-60. Doi: https://doi.org/10.21789/22561498.885

Rasher D, Hay, M. Chemically rich seaweeds poison corals when not controlled by herbivores. PNAS. 2010,107(21):9683-9688. Doi: https://doi.org/doi.org/10.1073/pnas.0912095107

Reyes J, Santodomingo N, Flórez P. Corales escleractinios de Colombia. INVEMAR Serie de Publicaciones Especiales No. 14., Santa Marta. 2010. 246 p.

Richelle-Maurer E, De Kluijver M, Feio S, Gaudencio S, Gaspar H, Gomez R, et al. Localization and ecological significance of oroidin and sceptrin in the Caribbean sponge Agelas conifera. Biochem. Syst. Ecol. 2003;31(10):1073–1091. Doi: https://doi.org/10.1016/S0305-1978(03)00072-3

Ritson-Williams R, Arnold SN, Fogarty ND, Steneck RS, Vermeij MJA, Paul VJ. New perspectives on ecological mechanisms affecting coral recruitment on reefs. In: Lang MA, MacIntyre IG, Rützler K, editors. Proceedings of the Smithsonian Marine Science Symposium. Smithsonian Institution Scholarly Pres., Washington DC. 2009. p. 437-457.

Sam TW. Toxicity testing using the brine shrimp: Artemia salina. In: Colegate S, Molineux RB, editors. Bioactive Natural Products: Detection, isolation and structural determination. CRC Press Inc. Boca Raton, Fl. 1993. p. 441-456

Sánchez JA, Alvarado EM, Gil M, Charry H, Arenas OL, Chasqui L, et al. Synchronous mass spawning of Montastraea annularis (Ellis & Solander) and Montastraea faveolata (Ellis &Solander) (Faviidae: Scleractinia) at Rosario Islands, Caribbean coast of Colombia. Bull. Mar. Sci. 1999;65(3):873-879.

Smith JE, Kuwabara J, Flanagan K, duPlessis S, Coney J, Beets J, et al.

An unusual cyanobacterial bloom in Hawai´i. Coral Reefs. 2008;27(4):851. Doi: https://doi.org/10.1007/s00338-008-0417-0

Steinberg P, De Nys R, Kjelleberg S. Chemical inhibition of epibiota by Australian seaweeds. Biofouling. 1998;12:227-244. Doi: https://doi.org/10.1080/08927019809378356

Tan LT, Goh BPL. Chemical ecology of marine cyanobacterial secondary metabolites: a mini review. Coast. Dev. 2009;13(1):1-9.

Thacker RW, Becerro MA, Lumbang WA, Paul VJ. Allelopathic Interactions between Sponges on a Tropical Reef. Ecology 1998;79(5):1740–1750. Doi: https://doi.org/10.2307/176792

Titlyanov E, Yakovleva I, Titlyanova T. Interaction between benthic algae (Lyngbya bouillonii, Dictyota dichotoma) and scleractinian coral Porites lutea in direct contact. J. Exp. Mar. Biol. Ecol. 2007;342(2):282-291. Doi: https://doi.org/10.1016/j.jembe.2006.11.007

Venn A, Wilson M, Trapido-Rosenthal H, Keely BY, Douglas A. The impact of coral bleaching on the pigment profile of the symbiotic alga, Symbiodinium. Plant Cell Environ. 2006;29(12):2133-2142. Doi: https://doi.org/10.1111/j.1365-3040.2006.001587.x

Cómo citar

APA

Puyana, M., Prato, J. A., Nieto, C. F., Ramos, F. A., Castellanos, L., Pinzón, P. & Zárate, J. C. (2019). Experimental Approaches for the Evaluation of Allelopathic Interactions Between Hermatypic Corals and Marine Benthic Cyanobacteria in the Colombian Caribbean. Acta Biológica Colombiana, 24(2), 243–254. https://doi.org/10.15446/abc.v24n2.72706

ACM

[1]
Puyana, M., Prato, J.A., Nieto, C.F., Ramos, F.A., Castellanos, L., Pinzón, P. y Zárate, J.C. 2019. Experimental Approaches for the Evaluation of Allelopathic Interactions Between Hermatypic Corals and Marine Benthic Cyanobacteria in the Colombian Caribbean. Acta Biológica Colombiana. 24, 2 (may 2019), 243–254. DOI:https://doi.org/10.15446/abc.v24n2.72706.

ACS

(1)
Puyana, M.; Prato, J. A.; Nieto, C. F.; Ramos, F. A.; Castellanos, L.; Pinzón, P.; Zárate, J. C. Experimental Approaches for the Evaluation of Allelopathic Interactions Between Hermatypic Corals and Marine Benthic Cyanobacteria in the Colombian Caribbean. Acta biol. Colomb. 2019, 24, 243-254.

ABNT

PUYANA, M.; PRATO, J. A.; NIETO, C. F.; RAMOS, F. A.; CASTELLANOS, L.; PINZÓN, P.; ZÁRATE, J. C. Experimental Approaches for the Evaluation of Allelopathic Interactions Between Hermatypic Corals and Marine Benthic Cyanobacteria in the Colombian Caribbean. Acta Biológica Colombiana, [S. l.], v. 24, n. 2, p. 243–254, 2019. DOI: 10.15446/abc.v24n2.72706. Disponível em: https://revistas.unal.edu.co/index.php/actabiol/article/view/72706. Acesso em: 22 mar. 2026.

Chicago

Puyana, Mónica, Julián Alberto Prato, Christian Felipe Nieto, Freddy Alejandro Ramos, Leonardo Castellanos, Paola Pinzón, y Juan Camilo Zárate. 2019. «Experimental Approaches for the Evaluation of Allelopathic Interactions Between Hermatypic Corals and Marine Benthic Cyanobacteria in the Colombian Caribbean». Acta Biológica Colombiana 24 (2):243-54. https://doi.org/10.15446/abc.v24n2.72706.

Harvard

Puyana, M., Prato, J. A., Nieto, C. F., Ramos, F. A., Castellanos, L., Pinzón, P. y Zárate, J. C. (2019) «Experimental Approaches for the Evaluation of Allelopathic Interactions Between Hermatypic Corals and Marine Benthic Cyanobacteria in the Colombian Caribbean», Acta Biológica Colombiana, 24(2), pp. 243–254. doi: 10.15446/abc.v24n2.72706.

IEEE

[1]
M. Puyana, «Experimental Approaches for the Evaluation of Allelopathic Interactions Between Hermatypic Corals and Marine Benthic Cyanobacteria in the Colombian Caribbean», Acta biol. Colomb., vol. 24, n.º 2, pp. 243–254, may 2019.

MLA

Puyana, M., J. A. Prato, C. F. Nieto, F. A. Ramos, L. Castellanos, P. Pinzón, y J. C. Zárate. «Experimental Approaches for the Evaluation of Allelopathic Interactions Between Hermatypic Corals and Marine Benthic Cyanobacteria in the Colombian Caribbean». Acta Biológica Colombiana, vol. 24, n.º 2, mayo de 2019, pp. 243-54, doi:10.15446/abc.v24n2.72706.

Turabian

Puyana, Mónica, Julián Alberto Prato, Christian Felipe Nieto, Freddy Alejandro Ramos, Leonardo Castellanos, Paola Pinzón, y Juan Camilo Zárate. «Experimental Approaches for the Evaluation of Allelopathic Interactions Between Hermatypic Corals and Marine Benthic Cyanobacteria in the Colombian Caribbean». Acta Biológica Colombiana 24, no. 2 (mayo 1, 2019): 243–254. Accedido marzo 22, 2026. https://revistas.unal.edu.co/index.php/actabiol/article/view/72706.

Vancouver

1.
Puyana M, Prato JA, Nieto CF, Ramos FA, Castellanos L, Pinzón P, Zárate JC. Experimental Approaches for the Evaluation of Allelopathic Interactions Between Hermatypic Corals and Marine Benthic Cyanobacteria in the Colombian Caribbean. Acta biol. Colomb. [Internet]. 1 de mayo de 2019 [citado 22 de marzo de 2026];24(2):243-54. Disponible en: https://revistas.unal.edu.co/index.php/actabiol/article/view/72706

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