Influence of the Habitat on Marine Macroalgae Toxicity
Annual Research & Review in Biology,
Page 1-9
DOI:
10.9734/arrb/2019/v33i130113
Abstract
Macroalgae synthesize molecules that may be toxic to other organisms. These molecules are synthesized as a defense strategy against herbivores. It has been proven that the synthesis process is directed by several physiological, chemical and even spatial-temporal variables. The purpose of this study was to determine whether the complexity of the habitat influences on the expression of marine macroalgae toxicity. Algae of 31 species (39 samples) were collected in localities with different habitat morphology: a coral reef in the Mexican Caribbean, three myxohaline localities in the Yucatán peninsula and six rocky intertidal localities, four of these in the Mexican Pacific and two in the Gulf of Mexico. Results identified 19 strongly toxic species from the reef, followed by algae collected in the rocky intertidal area, and the least number of toxic species in the myxohaline environments. The results support the hypothesis established by several researchers worldwide regarding the complexity of coral reefs, which promotes the synthesis of toxic substances as a defense against herbivores. These substances have been employed as molecules that are useful in the fight against diseases or as synthesis matrices of other compounds with pharmacological potential.
Keywords:
- Toxicity
- ichthyotoxicity
- macroalgae
- habitat
- Mexico
How to Cite
Alvarez-Hernández, S., Lozano-Ramírez, C., & Rodríguez-Palacio, M. (2019). Influence of the Habitat on Marine Macroalgae Toxicity. Annual Research & Review in Biology, 33(1), 1-9. https://doi.org/10.9734/arrb/2019/v33i130113
References
Singh S, Kate BN, Banerjee UC. Bioactive compounds from cyanobacteria and microalgae: An overview. Critical Reviews in Biotechnology. 2005;25:73-95.
Russell JSO, Stüken A, Murray SA, Jakobsen KS. Evolution and distribution of saxitoxin biosynthesis in dinoflagellates. Marine Drugs. 2013;11(8):2814-2828.
Dittmann E, Fewer DP, Neilan BA. Cyanobacterial toxins: Biosynthetic routes and evolutionary roots. FEMS Microbiology Review. 2013;37:23-43.
Tang LT, Williamson RT, Gerwick WH. cis, cis- and trans, trans-Ceratospongamide, new bioactive cyclic heptapeptides from the Indonesian red alga Ceratodictyon spongiosum and symbiotic sponge Sigmadocia symbiotica. Journal of Organic Chemistry. 2000;65:419-425.
Puyana M, Pawlik J, Blum J, Fenical W. Metabolite variability in Caribbean sponges of the genus Aplysina. Revista Brasileira de Farmacognosia-Brazilian Journal of Pharmacognosy. 2015;25:592-599.
Teo SLM, Ryland JS. Toxicity and palatability of some British ascidians. Marine Biology. 1994;120(2):297-303.
Teruya T, Suenaga K, Maruyama S, Kurotaki M, Kigoshi H. Biselides A–E: Novel polyketides from the Okinawan ascidian Didemnidae sp. Tetrahedron. 2005;61(27):6561-6567.
Watters DJ. Ascidian toxins with potential for drug development. Marine Drugs. 2018;16(5):162.
La Barrre SC, Coll JC, Sanmarco PW. Competitive strategies of soft corals (Coelenterata: Octocorallia). III. Spacing and aggressive interactions between alcyonaceans. Marine Ecology Progress Series. 1986;128:147-156.
Rezanka T, Dembitsky VM. -Lactones from the soft corals Sarcophyton trocheliophorum and Lithophyton arboretum. Tetrahedron. 2001;57(41): 8743-8749.
Ben-Ari H, Paz M, Sher D. The chemical armament of reef-building corals: inter- and intra-specific variation and the identification of an unusual actinoporin in Stylophora pistilata. Nature Scientific Reports. 2018;8: 251.
Cavalier-Smith T. Origins of secondary metabolism. In: Derek J. Chadwick & Julie Whelan (Eds) Ciba Foundation Symposium 171 ‐ Secondary Metabolites: Their Function and Evolution. 1992;64-87.
Sammarco PW, Coll JC. Secondary metabolites – or primary? Re-examination of a concept through a marine example. Proceedings of the 8th International Coral Reef Symposium. 1997;2:1245-1250.
Giordano D, Coppola D, Russo R, Denaro R, Giuliano L, Lauro FM, di Prisco G, Cinzia V. Marine microbial secondary metabolites: Pathways, evolution and physiological roles. In: Poole, R. K. (Ed) Advances in Microbial Physiology. Elsevier. 2015;66:357-428.
Amsler CD. Induced defenses in macroalgae: The herbivore makes a difference. Journal of Phycology. 2001;37: 353-356.
Paul VJ, van Alstyne KL. Activation of chemical defenses in the tropical green algae Halimeda spp. Journal of Experimental Marine Biology and Ecology. 1992;160:191-203.
Cronin G, Hay ME. Induction of seaweed chemical defenses by amphipod grazing. Ecology. 1996;77(8):2287-2301.
Sotka EE, Wares JP, Hay ME. Geographic and genetic variation in feeding preference for chemically defended seaweeds. Evolution. 2003;57(10):2262-2276.
Pal A, Kamthania MC, Kumar A. Bioactive compounds and properties of seaweeds – A review. Open Access Library Journal. 2014;1:e752.
Bhadury P, Wright PC. Exploitation of marine algae: Biogenic compounds for potential antifouling applications. Planta. 2004;219:561-578.
Maréchal J-P, Culioli G, Hellio C, Thomas-Guyon H, Callow ME, Clare AS, Ortalo-Magné 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. Journal of Experimental Marine Biology and Ecology. 2004;313:47-62.
Suzuki M, Wakana I, Denboh T, Tatewaki M. An allelopathic polyunsaturated fatty acid from red algae. Phytochemistry. 1996;43(1):63-65.
Suzuki Y, Takabayashi T, Kawaguchi T, Matsunaga K. Isolation of an allelopathic substance from the crustose coralline algae, Lithophyllum spp., and its effect on the brown alga, Laminaria religiosa Miyabe (Phaeophyta). Journal of Chemical Ecology. 1998;225(1):69-77.
Gross E. Allelopathy of aquatic autotrophs. In: Critical Reviews in Plant Science. 2003;22(3-4):313-339.
Faulkner DJ. Marine natural products. Natural Products Report. 1997;14:259- 301.
Hay ME, Fenical W. Marine plant-herbivores interactions: The ecology of chemical defense. Annual Review of Ecology and Systematics. 1988;19:111-145.
Dicky G, Davis J, Vasanthi AHR. Seaweed metabolite database (SWMD): A database of natural compounds from marine algae. Bioinformation. 2011;5(8):361-364.
Hay ME. The role of seaweed chemical defenses in the evolution of feeding specialization and in the mediation of complex interactions. In: Paul, VJ (Ed) Ecological Roles of Marine Natural Products. Cornell University Press, Ithaca and London. 1992;93-118.
Hay ME, Steinberg PD. The chemical ecology of plant-herbivore interactions in marine versus terrestrial communities. In: Rosenthal J & M Berenbaum (Eds) Herbivores: Their Interaction with Secondary Plant Metabolites. Evolutionary and Ecological Processes. Academic Press, New York. 1992;2:371-413.
Schmitt TM, Hay ME, Lindquist N. Constraints on chemically mediated coevolution: Multiple functions of seaweed secondary metabolites. Ecology. 1995;76: 107-123.
Demko AM, Amsler CD, Hay ME, Long JD, McClintock JB, Paul VJ, Sotka EE. Declines in plant palatability from polar to tropical latitudes depend on herbivore and plant identity. Ecology. 2017;98(9):2312-2321.
Faulkner DJ. Marine natural products: Metabolites of marine algae and herbivorous marine mollusks. Natural Products Report. 1984;1:251-280.
Fenical W. Halogenation in the Rhodophyta: A review. Journal of Phycology. 1975;11:245-259.
Retz de Carvalho L, Roque NF. Correlations between primary and secondary metabolites in Ceramiales (Rhodophyta). Biochemical Systematics and Ecology. 2004;32(3):337-342.
Paul VJ, Fenical W. Isolation of halimedatrial: Chemical defense adaptation in the calcareous reef-building alga Halimeda. Science. 1983;221:747-749.
Paul VJ, Fenical W. Chemical defense in tropical green algae, Order Caulerpales. Marine Ecology Progress Series. 1986;34: 157-169.
Paul VJ, van Alstyne KL. Chemical defenses and chemical variation in some tropical Pacific species of Halimeda (Halimedaceae; Chlorophyta). Coral Reefs. 1988;6:263-269.
El Gamal AA. Biological importance of marine algae. Saudi Pharmaceutical Journal. 2010;18(1):1-25.
Carvalho LRS, Barros F. Physical habitat structures in marine ecosystems: The meaning of complexity and heterogeneity. Hydrobiologia. 2017;797:1-9.
Kovalenko KE, Thomaz SM, Warfe DM. Habitat complexity: Approaches and future directions. Hydrobiologia. 2012;685:1–17.
McCoy ED, Bell SS. Habitat structure: The evolution and diversification of a complex topic. In: Bell SS, McCoy ED & Mushinsky HR, (Eds), Habitat Structure: The physical arrangement of objects in space. Chapman and Hall, London. 1991;3–27.
Tews J, Brose U, Grimm V, Tielborger K, Wichmann MC, Schwager M, Jeltsch F. Animal species diversity driven by habitat heterogeneity/diversity: The importance of keystone structures. Journal of Biogeography. 2004;31:79–92.
Tokeshi M, Arakaki S. Habitat complexity in aquatic systems: Fractals and beyond. Hydrobiologia. 2011;685:27-47.
Wiens JA. Ecological heterogeneity: An ontogeny of concepts and approaches. In: Hutchings MJ, EA John & AJA Stewart, (Eds). The Ecological Consquences of Environmental Hewterogeneity. Blackwell Science, Oxford. 2000;9-31.
Paul VJ. Seaweed chemical defense on coral reefs. p. 24-50. In: Paul VJ (Ed) Ecological Roles of Marine Natural Products. Comstock Publication Association, USA. 1992;245.
Eynaud Y, McNamara DE, Sandin SA. Herbivore space use influences coral reef recovery. Royal Society Open Science. 2016;3(6):160262.
González-González J, Gold M, León H, Candelaria C, León D, Serviere E, Fragoso D. Catálogo onomástico (nomenclator) y bibliográfico indexado de las algas bentónicas marinas de México. Cuaderno 29. Instituto de Biología. UNAM. México. 1994;494.
De Lara-Isassi G, Álvarez-Hernández S, Collado-Vides L. Ichthyotoxic activity of extracts from Mexican marine macroalgae. Journal of Applied Phycology. 2000;12. Sreenivasa-Rao PR, Parekh KS. Anti-bacterial activity of Indian seaweed extracts. Botanica Marina. 1981;24:577-582.
Lopes RV, Fernández N, Martins RF, Vasconcelos V. Primary screening of the bioactivity of brackishwater Cyanobacteria: Toxicity of crude extracts to Artemia salina Larvae and Paracentrotus lividus Embryos. Marine Drugs. 2010;8(3):471–482.
Rodríguez-Palacio MC, Crisóstomo-Vázquez L, Álvarez-Hernández S, Lozano-Ramírez C. Strains of toxic and harmful microalgae, from wastewater, marine, brackish and freshwater. Food Additives & Contaminants: Part A. 2011;29(2):304–313.
Green G. Ecology of toxicity in marine sponges. Marine Biology. 1977;40:207-215.
Hammer Ø, Harper DAT, Ryan PD. PAST: Paleontological Statistics Software Package for education and data analysis. Palaeontologia Electronica. 2001;4(1):9.
Hay ME. Predictable spatial scapes from herbivory: How do these affect the evolution of herbivore resistance in tropical marine communities? Oecology. 1984;64: 396-407.
Matlock DB, Ginsburg DW, Paul VJ. Spatial variability in secondary metabolite production by the tropical red alga Portieria hornemannii. Hydrobiologia. 1999;398/399: 267-273.
Hay ME, Paul VJ, Lewis SM, Gustafson K, Tucker J, Trindell RN. Does the tropical seaweed Halimeda reduce herbivory by growing at night? Diel patterns of growth, nitrogen content, herbivory, and chemical versus morphological defenses. Oecologia. 1988;81:418-427.
Paul VJ, Littler MM, Littler DS, Fenical W. Evidence for chemical defense in tropical green algae Caulerpa ashmeadii (Caulerpaceae: Chlorophyta): Isolation of a new bioactive sesquiterpenoid. Journal of Chemical Ecology. 1987;13:1171-1185.
Nagarajan S, Mathaiyan M. Emerging novel anti HIV biomolecules from marine algae: An overview. Journal of Applied Pharmaceutical Science. 2015;5(09):153-158.
Russell JSO, Stüken A, Murray SA, Jakobsen KS. Evolution and distribution of saxitoxin biosynthesis in dinoflagellates. Marine Drugs. 2013;11(8):2814-2828.
Dittmann E, Fewer DP, Neilan BA. Cyanobacterial toxins: Biosynthetic routes and evolutionary roots. FEMS Microbiology Review. 2013;37:23-43.
Tang LT, Williamson RT, Gerwick WH. cis, cis- and trans, trans-Ceratospongamide, new bioactive cyclic heptapeptides from the Indonesian red alga Ceratodictyon spongiosum and symbiotic sponge Sigmadocia symbiotica. Journal of Organic Chemistry. 2000;65:419-425.
Puyana M, Pawlik J, Blum J, Fenical W. Metabolite variability in Caribbean sponges of the genus Aplysina. Revista Brasileira de Farmacognosia-Brazilian Journal of Pharmacognosy. 2015;25:592-599.
Teo SLM, Ryland JS. Toxicity and palatability of some British ascidians. Marine Biology. 1994;120(2):297-303.
Teruya T, Suenaga K, Maruyama S, Kurotaki M, Kigoshi H. Biselides A–E: Novel polyketides from the Okinawan ascidian Didemnidae sp. Tetrahedron. 2005;61(27):6561-6567.
Watters DJ. Ascidian toxins with potential for drug development. Marine Drugs. 2018;16(5):162.
La Barrre SC, Coll JC, Sanmarco PW. Competitive strategies of soft corals (Coelenterata: Octocorallia). III. Spacing and aggressive interactions between alcyonaceans. Marine Ecology Progress Series. 1986;128:147-156.
Rezanka T, Dembitsky VM. -Lactones from the soft corals Sarcophyton trocheliophorum and Lithophyton arboretum. Tetrahedron. 2001;57(41): 8743-8749.
Ben-Ari H, Paz M, Sher D. The chemical armament of reef-building corals: inter- and intra-specific variation and the identification of an unusual actinoporin in Stylophora pistilata. Nature Scientific Reports. 2018;8: 251.
Cavalier-Smith T. Origins of secondary metabolism. In: Derek J. Chadwick & Julie Whelan (Eds) Ciba Foundation Symposium 171 ‐ Secondary Metabolites: Their Function and Evolution. 1992;64-87.
Sammarco PW, Coll JC. Secondary metabolites – or primary? Re-examination of a concept through a marine example. Proceedings of the 8th International Coral Reef Symposium. 1997;2:1245-1250.
Giordano D, Coppola D, Russo R, Denaro R, Giuliano L, Lauro FM, di Prisco G, Cinzia V. Marine microbial secondary metabolites: Pathways, evolution and physiological roles. In: Poole, R. K. (Ed) Advances in Microbial Physiology. Elsevier. 2015;66:357-428.
Amsler CD. Induced defenses in macroalgae: The herbivore makes a difference. Journal of Phycology. 2001;37: 353-356.
Paul VJ, van Alstyne KL. Activation of chemical defenses in the tropical green algae Halimeda spp. Journal of Experimental Marine Biology and Ecology. 1992;160:191-203.
Cronin G, Hay ME. Induction of seaweed chemical defenses by amphipod grazing. Ecology. 1996;77(8):2287-2301.
Sotka EE, Wares JP, Hay ME. Geographic and genetic variation in feeding preference for chemically defended seaweeds. Evolution. 2003;57(10):2262-2276.
Pal A, Kamthania MC, Kumar A. Bioactive compounds and properties of seaweeds – A review. Open Access Library Journal. 2014;1:e752.
Bhadury P, Wright PC. Exploitation of marine algae: Biogenic compounds for potential antifouling applications. Planta. 2004;219:561-578.
Maréchal J-P, Culioli G, Hellio C, Thomas-Guyon H, Callow ME, Clare AS, Ortalo-Magné 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. Journal of Experimental Marine Biology and Ecology. 2004;313:47-62.
Suzuki M, Wakana I, Denboh T, Tatewaki M. An allelopathic polyunsaturated fatty acid from red algae. Phytochemistry. 1996;43(1):63-65.
Suzuki Y, Takabayashi T, Kawaguchi T, Matsunaga K. Isolation of an allelopathic substance from the crustose coralline algae, Lithophyllum spp., and its effect on the brown alga, Laminaria religiosa Miyabe (Phaeophyta). Journal of Chemical Ecology. 1998;225(1):69-77.
Gross E. Allelopathy of aquatic autotrophs. In: Critical Reviews in Plant Science. 2003;22(3-4):313-339.
Faulkner DJ. Marine natural products. Natural Products Report. 1997;14:259- 301.
Hay ME, Fenical W. Marine plant-herbivores interactions: The ecology of chemical defense. Annual Review of Ecology and Systematics. 1988;19:111-145.
Dicky G, Davis J, Vasanthi AHR. Seaweed metabolite database (SWMD): A database of natural compounds from marine algae. Bioinformation. 2011;5(8):361-364.
Hay ME. The role of seaweed chemical defenses in the evolution of feeding specialization and in the mediation of complex interactions. In: Paul, VJ (Ed) Ecological Roles of Marine Natural Products. Cornell University Press, Ithaca and London. 1992;93-118.
Hay ME, Steinberg PD. The chemical ecology of plant-herbivore interactions in marine versus terrestrial communities. In: Rosenthal J & M Berenbaum (Eds) Herbivores: Their Interaction with Secondary Plant Metabolites. Evolutionary and Ecological Processes. Academic Press, New York. 1992;2:371-413.
Schmitt TM, Hay ME, Lindquist N. Constraints on chemically mediated coevolution: Multiple functions of seaweed secondary metabolites. Ecology. 1995;76: 107-123.
Demko AM, Amsler CD, Hay ME, Long JD, McClintock JB, Paul VJ, Sotka EE. Declines in plant palatability from polar to tropical latitudes depend on herbivore and plant identity. Ecology. 2017;98(9):2312-2321.
Faulkner DJ. Marine natural products: Metabolites of marine algae and herbivorous marine mollusks. Natural Products Report. 1984;1:251-280.
Fenical W. Halogenation in the Rhodophyta: A review. Journal of Phycology. 1975;11:245-259.
Retz de Carvalho L, Roque NF. Correlations between primary and secondary metabolites in Ceramiales (Rhodophyta). Biochemical Systematics and Ecology. 2004;32(3):337-342.
Paul VJ, Fenical W. Isolation of halimedatrial: Chemical defense adaptation in the calcareous reef-building alga Halimeda. Science. 1983;221:747-749.
Paul VJ, Fenical W. Chemical defense in tropical green algae, Order Caulerpales. Marine Ecology Progress Series. 1986;34: 157-169.
Paul VJ, van Alstyne KL. Chemical defenses and chemical variation in some tropical Pacific species of Halimeda (Halimedaceae; Chlorophyta). Coral Reefs. 1988;6:263-269.
El Gamal AA. Biological importance of marine algae. Saudi Pharmaceutical Journal. 2010;18(1):1-25.
Carvalho LRS, Barros F. Physical habitat structures in marine ecosystems: The meaning of complexity and heterogeneity. Hydrobiologia. 2017;797:1-9.
Kovalenko KE, Thomaz SM, Warfe DM. Habitat complexity: Approaches and future directions. Hydrobiologia. 2012;685:1–17.
McCoy ED, Bell SS. Habitat structure: The evolution and diversification of a complex topic. In: Bell SS, McCoy ED & Mushinsky HR, (Eds), Habitat Structure: The physical arrangement of objects in space. Chapman and Hall, London. 1991;3–27.
Tews J, Brose U, Grimm V, Tielborger K, Wichmann MC, Schwager M, Jeltsch F. Animal species diversity driven by habitat heterogeneity/diversity: The importance of keystone structures. Journal of Biogeography. 2004;31:79–92.
Tokeshi M, Arakaki S. Habitat complexity in aquatic systems: Fractals and beyond. Hydrobiologia. 2011;685:27-47.
Wiens JA. Ecological heterogeneity: An ontogeny of concepts and approaches. In: Hutchings MJ, EA John & AJA Stewart, (Eds). The Ecological Consquences of Environmental Hewterogeneity. Blackwell Science, Oxford. 2000;9-31.
Paul VJ. Seaweed chemical defense on coral reefs. p. 24-50. In: Paul VJ (Ed) Ecological Roles of Marine Natural Products. Comstock Publication Association, USA. 1992;245.
Eynaud Y, McNamara DE, Sandin SA. Herbivore space use influences coral reef recovery. Royal Society Open Science. 2016;3(6):160262.
González-González J, Gold M, León H, Candelaria C, León D, Serviere E, Fragoso D. Catálogo onomástico (nomenclator) y bibliográfico indexado de las algas bentónicas marinas de México. Cuaderno 29. Instituto de Biología. UNAM. México. 1994;494.
De Lara-Isassi G, Álvarez-Hernández S, Collado-Vides L. Ichthyotoxic activity of extracts from Mexican marine macroalgae. Journal of Applied Phycology. 2000;12. Sreenivasa-Rao PR, Parekh KS. Anti-bacterial activity of Indian seaweed extracts. Botanica Marina. 1981;24:577-582.
Lopes RV, Fernández N, Martins RF, Vasconcelos V. Primary screening of the bioactivity of brackishwater Cyanobacteria: Toxicity of crude extracts to Artemia salina Larvae and Paracentrotus lividus Embryos. Marine Drugs. 2010;8(3):471–482.
Rodríguez-Palacio MC, Crisóstomo-Vázquez L, Álvarez-Hernández S, Lozano-Ramírez C. Strains of toxic and harmful microalgae, from wastewater, marine, brackish and freshwater. Food Additives & Contaminants: Part A. 2011;29(2):304–313.
Green G. Ecology of toxicity in marine sponges. Marine Biology. 1977;40:207-215.
Hammer Ø, Harper DAT, Ryan PD. PAST: Paleontological Statistics Software Package for education and data analysis. Palaeontologia Electronica. 2001;4(1):9.
Hay ME. Predictable spatial scapes from herbivory: How do these affect the evolution of herbivore resistance in tropical marine communities? Oecology. 1984;64: 396-407.
Matlock DB, Ginsburg DW, Paul VJ. Spatial variability in secondary metabolite production by the tropical red alga Portieria hornemannii. Hydrobiologia. 1999;398/399: 267-273.
Hay ME, Paul VJ, Lewis SM, Gustafson K, Tucker J, Trindell RN. Does the tropical seaweed Halimeda reduce herbivory by growing at night? Diel patterns of growth, nitrogen content, herbivory, and chemical versus morphological defenses. Oecologia. 1988;81:418-427.
Paul VJ, Littler MM, Littler DS, Fenical W. Evidence for chemical defense in tropical green algae Caulerpa ashmeadii (Caulerpaceae: Chlorophyta): Isolation of a new bioactive sesquiterpenoid. Journal of Chemical Ecology. 1987;13:1171-1185.
Nagarajan S, Mathaiyan M. Emerging novel anti HIV biomolecules from marine algae: An overview. Journal of Applied Pharmaceutical Science. 2015;5(09):153-158.
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