Services on Demand
- Cited by SciELO
- Access statistics
- Cited by Google
- Similars in SciELO
- Similars in Google
Print version ISSN 0102-695X
Rev. bras. farmacogn. vol.22 no.4 Curitiba July/Aug. 2012 Epub May 24, 2012
Gilberto M. Amado-Filho*, I; Guilherme H. Pereira-FilhoII
IInstituto de Pesquisas Jardim Botânico do Rio de Janeiro, Brazil
IIDepartamento de Botânica, Universidade Federal Rural do Rio de Janeiro, Brazil
Rhodoliths are the free-living forms of a number of nongeniculate coralline algae. Rhodolith beds are a common feature of subtidal environments and have been recognized as important carbonate producers and paleoenvironmental indicators, as well as recognized as habitat-forming species. The rhodolith structure provides a hard three-dimensional substrate serving as microhabitat for a wide range of biodiversity, including commercially importance species. The largest known latitudinal occurrence range of rhodolith beds ais on the Brazilian coastal shelf from 2°N to 25°S. Despite their importance for the Brazilian benthic communities, only in the last decade sampling efforts allowed a more comprehensive understanding of the beds' distribution, their structure and associated communities, as well as data concerning the influence of environmental factors on rhodolith bed structure and dynamics. In this work, we review the available information on the biodiversity associated with the recently described Brazilian rhodolith beds of the continental shelf and oceanic islands, focusing on the associated organisms with potential for bioprospection research.
Keywords: rhodolith beds, bioprospection, algae, benthic communities
Rhodolith (maërl) beds, communities dominated by free living, calcareous, non-geniculate coralline algae, are a common feature of subtidal environments worldwide. Rhodoliths are the free-living forms of a number of nongeniculate coralline algal genera of the Cora llinales and Sporolithales and have been recognized as foundation species (Amado-Filho et al., 2007; Foster et al., 2007; Steller et al., 2007). Well preserved as fossils, they have long been recognized as important carbonate producers and paleoenvironmental indicators (Foster et al., in press). Rhodoliths often occur at high concentrations over large areas, forming rhodolith beds that are among the "Big Four" benthic communities dominated by marine macrophytes, ranking with kelp forests, seagrass meadows and coralline reefs (Foster 2001; Foster et al., in press).
Living rhodolith commonly occur on sediment, often of biogenic origin. The structure of the rhodolith has a large effect on the associated organisms, causing an increase in diversity over that of a purely soft benthic habitat (Steller & Foster, 1995). The rhodolith structure provides a hard, three-dimensional substrate, serving as a microhabitat for a wide diversity of invertebrates, associated algae and fishes, many of whom are of significant commercial importance (Foster et al., 1997; Steller et al., 2003; Littler & Littler, 2008). Thus, rhodoliths are widely recognized as habitat- forming species (e.g., Amado-Filho et al., 2007; Foster et al., 2007; Steller et al., 2007).
Foster (2001) pointed out that current reports indicate that rhodolith beds are especially abundant in the Mediterranean, Gulf of California, the Atlantic coasts of Norway, Ireland, Scotland, northeastern Canada, and the eastern Caribbean, as well as the coasts of southern Japan and western Australia. However, the largest know latitudinal occurrence of rhodolith beds is on the Brazilian continental shelf from 2°N to 25°S, covering an extension of 4.000 km from Pará down to Rio de Janeiro states (Kempf, 1970; Milliman, 1977) with a small bed occurring on the southern coast off Arvoredo Island (Gherardi, 2004). In the 1970´s, many studies of rhodoliths in Brazil derived from investigations of the sedimentary character of the Brazilian shelf, together with the prospects for commercial exploitation (Kempf, 1970; Mabessone et al., 1972; Milliman & Amaral, 1974; Milliman, 1977; Vicalvi & Milliman, 1977). These studies estimated that the rhodolith beds represent a storage of calcium carbonate (CaCO3) of 2x1011 tons.
Calcium carbonate production by marine organisms is an essential process in the global budget of CO32" (Milliman, 1993; Vecsei, 2004) and this process is largely determined by variations in the pH of seawater (Doney et al., 2009). Ocean acidification is a predictable consequence of rising atmospheric carbon dioxide (CO2) levels. The levels of atmospheric CO2 have increased around 40% in the past 250 years (Solomon et al., 2007) and a third of the anthropogenic carbon added to the atmosphere has been tempered by oceanic uptake (Sabine & Feely, 2007), representing a decrease in pH of approximately 0.1 units, from pH 8.21 to pH 8.10 (Royal Society, 2005). According to the Intergovernmental Panel on Climate Change (IPCC), the projected end-of-century concentration of atmospheric CO2 is 800 ppmv, representing more than twice the current value (Doney et al., 2009). If the atmospheric concentrations reaches this value, a further decrease of 0.3-0.4 pH units of seawater could be expected (Orr et al., 2005), reducing the structural integrity of carbonate-based structures (Doney et al., 2009). Changes in carbonate dissolution represent losses of habitat and, consequently, losses of biodiversity.
The Earth's biodiversity is richer and more varied nowadays than ever before. Around 15,000 to 20,000 new species have been described and, even for relatively well-known areas such as the United States of America, the rate of discovery suggests that only a third of the species of organisms have been discovered so far (Dirzo & Raven, 2003). Some of the new discoveries are of evident economic importance, such as a species of maize, Zea diploperennis, from western Mexico that was discovered only 32 years ago (Iltis et al., 1979). Despite the high expected values of the Earth's diversity, the consequences of the major extinction episode of the Phanerozoic Era can be recognized in current days (May et al., 1995). Habitat loss due to anthropogenic causes is at present a principal driver of extinction (Dirzo & Raven, 2003).
For coralline reefs, the most profound impacts caused by anthropogenic causes occur at depths shallower than 20 m, while reefs in the mesophotic zone (deeper than 30 m) have been reported to be free from the majority of these impacts (Bak et al., 2005; Lesser et al., 2009; Kahng et al., 2010). For many decades, the mesophotic zone was understudied because of technological limitations and the excessive costs of accessing these areas (Hinderstein et al., 2010). A few new phyla and classes of eukaryotic organisms are being found each decade. Most of them are from marine habitats (Dirzo & Raven, 2003), probably because marine ecosystems have been more neglected for decades than terrestrial ones. Current advances in technical diving methods and instrumentation, such as mixed gas diving, remotely operated vehicles (ROV), rebreathers and autonomous underwater vehicles (AUV), together with image analysis techniques, are facilitating the sampling of the mesophotic zone (Hinderstein et al., 2010). The mesophotic coralline reefs consist mainly of species of corals, sponge and algae (Bak et al., 2005; Kahng et al., 2010). We present here a review of the largest coralline reefs of Brazil: the rhodolith beds. In addition, we highlight their importance to marine biodiversity and their potential for harboring many species of importance to bioprospection.
Rhodolith beds in Brazil
Until the second half of the 1990´s, the principal interest in rhodolith studies was the sedimentary character of the Brazilian shelf and the potential of the rhodolith beds for commercial exploitation of carbonates (Kempf et al., 1970; Mabessone et al., 1972; Milliman & Amaral, 1974; Milliman, 1977; Vicalvi & Milliman, 1977). In the mid-90´s, several studies approached the rhodolith beds from a biological point of view, providing consistent information on rhodolith bed structure and mapping a limited area of the northeastern Brazilian coast (e.g., Testa, 1997; Testa & Bosence, 1999; Testa et al., 1997).
Only in the last decade extensive sampling efforts allowed a more comprehensive understanding of the rhodolith bed distribution along the Brazilian coast, of their structure and associated communities and of the influence of environmental factors on rhodolith bed habitats. These recent studies have reported several important new finds related to marine algae: one new species (Lithophyllum depressum) (Villas-Boas et al., 2009), three new occurrences for the Atlantic Ocean (Scinaia aborealis, Sporolithon ptychoides, Hydrolithon rupestris) (Amado Filho et al., 2010; Bahia et al., 2011; Pereira-Filho et al., 2012), two new occurrences for the western Atlantic Ocean (Mesophyllum engelhartii, Reticulocaulis mucosissimus) (Amado Filho et al., 2010; Guimarães & Amado Filho, 2009), five new occurrences for the Southwestern Atlantic Ocean (Acrosymphyton caribaeum, Dudresnaya crassa, Naccaria corymbosa, Platoma sp. and Predaea feldmannii) (Guimarães & Amado Filho, 2008) and four new occurrences for the Brazilian coast (Dasya ramosissima, Halymenia elongate, Udotea abbottiorum, Lithothamnion muelleri) (Riul et al., 2009; Amado Filho et al., 2010).
At present, the fauna associated with rhodoliths seems to be the greatest gap in our knowledge. Santos et al. (2011) described a new species of Polychaeta associated with rhodolith beds (Sabellaria corallinea) and reported, for the first time, the occurrence of Sabellaria pectinata in the western Atlantic Ocean. The diversity of other groups such as Sponges, Echionoderms and Tunicates that can be found associated with rhodoliths still remains unknown. Because large areas of the Brazilian shelf are covered by rhodolith beds (Foster et al., in press), an increase in the number of new occurrences is expected as more areas are better sampled for the associated fauna.
Recent advances in mixed-gas diving techniques (Figure 1A), complemented by ROV observations and high-resolution, multibeam, bathymetric mapping systems, have allowed us to determine extent, structure and dynamics of rhodolith beds much better. These tools are now being used to investigate extensive areas of the mesophotic zone of the continental shelf (e.g., the Abrolhos Bank) (Amado Filho et al., 2012), the tops of seamounts (Vitoria-Trindade Ridge) (Pereira-Filho et al., 2012) and around oceanic islands (e.g., Trindade Island and Fernando de Noronha Island) (Pereira-Filho et al., 2011).
Rhodoliths and bioprospection
In the last forty years, drug discovery efforts have changed their focus from terrestrial plants and microorganisms to marine environments, where invertebrates (e.g. Sponges, Corals and Tunicates) and benthic algae have been the subject of screening programs (Tabares et al., 2011). Marine benthic algae contain minerals, polysaccharides, amino acid derivatives, carotenoids and phenolic compounds that are often of economic interest. Extracts obtained from different species have shown important pharmacological effects in vivo, including hypolipidemic (Ara et al., 2002), antioxidant (Yuan & Walsh, 2006), immunological (Saker et al., 2004), antitumoral (Lee & Sung, 2003), antiviral (Rinehart et al., 1983) and antibacterial activities (Lima-Filho et al., 2002).
The number of algal species associated with rhodolith beds in Brazil varies between 56 and 190 species and their amount varies from 1.88 g.m-2 to 225.8 g.m-2 (Riul et al., 2009; Amado Filho et al., 2010; Bahia et al., 2010). The biomass of the algae associated with rhodolith beds is influenced by the season, depth, latitudinal gradient and distance from the continent (Bahia et al., 2010). Amansia multifida, Bryothamnion seaforthii, Halymenia floridana, and Plocamium brasiliense, as well as brown algae members of the family Dictyotaceae (e.g., Lobophora variegata, Stypopodium zonale, Dictyopteris jolyana (Figure 1B), Dictyopteris plagiogramma, Dictyopteris jamaicensis, and Dictyota mertensii), have been reported as the dominant species associated with rhodolith beds in Brazil (Riul et al., 2009; Amado Filho et al., 2010; Bahia et al., 2010).
Lima-Filho et al. (2002) found that extracts of A. multifida showed activity against enteric Gram-negative bacteria. In addition, Neves et al. (2007) reported that A. multifida was the source of a lectin with antinociceptive properties. Teixeira et al. (2007) found that lectins extracted from B. seaforthii that inhibited the adherence of streptococci to teeth could play an important role in preventing caries in the early stages. Ferreira et al. (2010) reported a high reduction in the infectivity of the virus HSV-1 in the presence of a crude extract of P. brasiliense. Dictyotaceae are well known to be a rich source of sesquiterpenes with a great range of bioactivities: antifungal, antitumoral, antibiotic, anti-inflamatory, insecticidal, anti-bacterial and others (see Paula et al., 2011).
One of the most interesting features of the Brazilian rhodolith beds in the mesophotic zone, recently investigated using technical diving (Figure 1C), are the associated populations of the endemic deep-water kelp Laminaria abyssalis (Figures 1D and E) (Marins et al., 2012). Besides the known importance of Laminaria in the food industry and for alginate extraction, polysaccharides from Laminaria japonica have been observed to have antithrombotic potential (Xie et al., 2011). Species of Laminaria may also be an important biomass for biofuels (Adams et al., 2011). Laminaria abyssalis occurs on the continental shelf at latitudes of 19º-23ºS and depths of 45-120 m, where the bottom can be completely covered by rhodoliths (Amado Filho et al., 2007). Kelp populations are closely associated with the rhodoliths, the L. abyssalis holdfasts being attached to one or more rhodoliths (Figures 1D and E). Graham et al. (2007) suggested that such deep-water kelp refugia are potential hotspots for tropical marine diversity and productivity. This suggestion has been confirmed in the Brazilian deep-water rhodolith-kelp beds, where endemic species of different taxonomic groups have been found in this area.
In rhodolith beds where the rhodoliths are dense and large enough to decrease their rate of turnover, sponges often seem to be associated with them (Pereira-Filho et al., 2012). Sponges are often associated with a large amount of a phylogenetically diverse microbial composition, which can account for around half of the animal's biomass (Taylor et al., 2007). The Order Actinomycetes (Phylum Actinobacteria) has been identified in sponges and are of particular interest due to their unmatched capacity to produce novel and bioactive secondary metabolities with anticancer and antitumoral activities (Fenical et al., 2009; Kwon et al., 2006; Tabares et al., 2011).
More than 50 secondary metabolites have been isolated from Tunicates and many of them are bioactive peptides (Vo et al., 2011). Eudistomins and didemnins, isolated from Tunicates, displayed high antiviral activity against Herpex simplex viruses (Rinehart et al., 1983). Other groups of invertebrates with expected potential for bioprospection such as Echinoderms, Mollusks and Bryozoa (Vo et al., 2011) are also associated with rhodolith beds. However, except for Polychaeta (Santos et al., 2011; Berlandi et al., 2012), there are no published data on invertebrates associated with Brazilian rhodolith beds.
Given the large areas covered by rhodolith beds in the Brazilian Exclusive Economic Zone (EEZ) (Amado-Filho et al., 2007; Riul et al., 2009; Amado Filho et al., 2010; Pereira-Filho et al., 2012; Amado Filho et al., 2012), their vulnerability to global changes (Feely et al., 2004; Doney et al., 2009) and the high diversity of organisms with recognized potential for bioprospection associated with them, research programs and public policies to conserve their biodiversity and to maintain the sovereignty of these areas are urgently needed.
This review was prepared with specific funding from the Brazilian National Research Council (CNPq), CAPES and FAPERJ to GM Amado-Filho and GH Pereira-Filho.
Adams JMM, Toop TA, Donnison IS, Gallagher JA 2011. Seasonal variation in Laminaria digitata and its impact on biochemical conversion routes to biofuels. Bioresource Technol 102: 9976-9984. [ Links ]
Amado-Filho GM, Maneveldt G, Manso RCC, Marins Rosa BV, Pacheco MR, Guimarães SMPB 2007 Structure of rhodolith beds from 4 to 55 meters deep along the southern coast of Espírito Santo State, Brazil. Cienc Mar 33: 399-410. [ Links ]
Amado-Filho GM, Maneveldt GW, Pereira-Filho GH, Manso RCC, Bahia RG, Barros-Barreto MB, Guimarães SMPB 2010. Seaweed diversity associated with a Brazilian tropical rhodolith bed. Cienc Mar 36: 371-391. [ Links ]
Amado-Filho GM, Moura RL, Bastos AC, Salgado LT, Sumida PY, Guth AZ, Francini-Filho RB, Pereira-Filho GH, Abrantes DP, Brasileiro PS, Bahia RG, Leal RN, Kaufman L, Kleypas JA, Farina M, Thompson FL (2012). Rhodolith beds are major CaCO3 bio-factories in the tropical south west atlantic. Plos One 7: e35171. [ Links ]
Ara J, Sultana V, Qasim R, Ahmad VU 2002. Hypolipidaemic activity of seaweed from Karachi Coast. Phytother Res 16: 479-483. [ Links ]
Bahia RG, Abrantes DP, Brasileiro PS, Pereira-Filho GH, Amado Filho GM 2010. Rhodolith bed structure along a depth gradient on the northern coast of Bahia State, Brazil. Braz J Oceanogr 58: 323-337. [ Links ]
Bahia RG, Riosmena-Rodriguez R, Maneveldt GW, Amado Filho GM 2011. First report of Sporolithon ptychoides (Sporolithales, Corallinophycidae, Rhodophyta) for the Atlantic Ocean. Phycol Res 59: 64-69. [ Links ]
Bak RPM, Nieuwland G, Meesters EH 2005. Coral reef crisis in deep and shallow reefs: 30 years of constancy and change in reefs of Curacao and Bonaire. Coral Reefs 24: 475-479. [ Links ]
Berlandi RM, Figueiredo MAO, Paiva PC 2012. Rhodolith morphology and the diversity of polychaetes off the southeastern Brazilian coast. J Coast Res 28: 280-287. [ Links ]
Dirzo R, Raven PH 2003. Global state of biodiversity and loss. Annu Rev Env Resour 28: 137-167. [ Links ]
Doney SC, Victoria JF, Richard AF, Kleypas JA 2009. Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1: 169-192. [ Links ]
Feely RA, Sabine CL, Lee K, Berelson W, Kleypas J, Fabry VJ, Millero FJ 2004. Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305: 362-366. [ Links ]
Fenical W, Jensen PR, Palladino MA, Lam KS, Lloyd GK, Potts BC 2009. Discovery and development of the anticancer agent salinosporamide A (NPI-0052). Bioorgan Med Chem 17: 2175-2180. [ Links ]
Ferreira WJ, Amaro R, Cavalcanti DN, Rezende CM, Silva VAGG, Barbosa JE, Izabel CNDPP, Teixeira VL 2010. Anti-herpetic activities of chemical components from the Brazilian red alga Plocamium brasiliense. Nat Prod Commun 5: 1167-1170. [ Links ]
Foster MS, Riosmena-Rodríguez R, Steller D, Woelkerling WMJ 1997. Living rhodolith beds in the Gulf of California and their significance for paleoenvironmental interpretation. In: Johnson M, Ledesma-Vazquez, (org.). Pliocene carbonates and related facies flanking the Gulf of California, Baja California, Mexico. Special Paper Number 318. Colorado: Geological Society of America, p. 127-139. [ Links ]
Foster MS 2001. Mini-review: Rhodoliths, between rocks and soft places. J Phycol 37: 659-657. [ Links ]
Foster MS, McConnico LM, Lundsten L, Wadsworth T, Kimball T, Brooks LB, Medina-López M, Riosmena-Rodríguez R, Hernández-Carmona G, Vásquez-Elizondo RM, Johnson D, Steller DS 2007. Diversity and natural history of Lithothamnion muelleri-Sargassum horridum community in the Gulf of California. Cienc Mar 33: 367-384. [ Links ]
Foster MS, Amado Filho GM, Kamenos NA, Riosmena-Rodriguez R, Steller DS (In press). Rhodolith and rhodolith beds. In: Lang M (org.). Contribution of SCUBA diving to research and discovery in marine environments. Washington DC: Smithsonian Institution Scholarly Press. [ Links ]
Gherardi DFM 2004. Community structure and carbonate production of a temperate rhodolith bank from Arvoredo Island, southern Brazil. Braz J Oceanogr 52: 207-224. [ Links ]
Graham MH, Kinlan BP, Dreuhl LD, Garske LE, Banks S 2007. Deep-water kelp refugia as potential hotspots of tropical marine diversity and productivity. P Natl Acad Sci USA 104: 16576-16580. [ Links ]
Guimarães SMPB, Amado Filho GM 2008. A community of gelatinous rhodophytes in the sublittoral of southern Espírito Santo State, Brazil. Bot Mar 51: 378-387. [ Links ]
Guimarães SMPB, Amado-Filho GM 2009. First record of Reticulocaulis mucosissimus I. A. Abbott (Naccariaceae, Rhodophyta) for the western Atlantic Ocean. Rev Bras Bot 32: 671-675. [ Links ]
Hinderstein LM, Marr JCA, Martinez FA, Dowgiallo MJ, Puglise KA, Pyle RL, Zawada DG, Appeldoorn RA 2010. Theme section on "Mesophotic Coral Ecosystems: characterization, ecology and management". Coral Reefs 29: 247-251. [ Links ]
Iltis HH, Doebley JF, Guzmán R, Pazy B 1979. Zea diploperennis (Graminae): a new teosinte from México. Science 203: 186-188. [ Links ]
Kahng SE, Garcia-Sais JR, Spalding HL, Brokovich E, Wagner D, Weil E, Hinderstein L, Toonen RJ 2010. Community ecology of mesophotic coral reef ecosystems. Coral Reefs 29: 255-275. [ Links ]
Kempf M 1970. Notes on the benthic bionomy of the N-NE Brazilian shelf. Mar Biol 5: 213-224. [ Links ]
Kwon HC, Kauffman CA, Jensen PR, Fenical W 2006. Marinomycins A-D, antitumor-antibiotics of a new structure class from a marine actinomycete of the recently discovered genus "Marinispora". J Am Chem Soc 128: 1622-1632. [ Links ]
Lee EJ, Sung MK 2003. Chemoprevention of azoxymethaneinduced rat colon carcinogenesis by seatangle, a fiber-rich seaweed. Plant Food Hum Nutr 58: 1-8. [ Links ]
Lesser MP, Slattery M, Leichter JJ 2009. Ecology of mesophotic coral reefs. J Exp Mar Biol Ecol 375: 1-8. [ Links ]
Lima-Filho JVM, Carvalho AFFU, Sissi MF, Melo VMM 2002. Antibacterial activity of extracts of six macroalgae from the northeastern Brazilian coast. Braz J Microbiol 33: 311-313. [ Links ]
Littler MM, Littler DS 2008. Coralline algal rhodoliths form extensive benthic communities in the gulf of Chiriqui, pacific Panama. Coral Reefs 27: 553-553. [ Links ]
Mabesoone JM, Kempf M, Coutinho PN 1972. Characterization of surface sediments on the northern and eastern Brazilian shelf. Trab Oceanogr Univ Fed Pe 13: 41-48. [ Links ]
Marins BV, Longo LL, Barreto MBB, Amado Filho GM 2012. Taxonomy of the southwestern Atlantic endemic kelp: Laminaria abyssalis and Laminaria brasiliensis (Phaeophyceae, Laminariales) are not different species. Phycol Res 60: 51-60. [ Links ]
May RM, Lawton JH, Stork NE 1995. Assessing extinction rates. In: Lawton JH, May RM (org.). Extinction Rates. Oxford: Oxford Univ Press, p. 1-24. [ Links ]
Milliman JD 1977. Role of calcareous algae in Atlantic continental margin sedimentation. In: Fluguel E (org). Fossil Algae. Berlin: Springer-Verlag, p. 232-247. [ Links ]
Milliman JD 1993. Production and accumulation of calcium carbonate in the ocean: budget of a nonsteady state. Global Biogeochem Cy 7: 927-957. [ Links ]
Milliman JD, Amaral CAB 1974. Economic potential of Brazilian continental margin sediments. An Congr Brasil Geo 28: 335-344. [ Links ]
Neves SA, Freitas ALP, Souza BWS, Rocha MLA, Correia MVO, Sampaio DA, Viana GSB 2007. Antinociceptive properties in mice of a lectin isolated from the marine alga Amansia multifida Lamouroux. Braz J Med Biol Res 40: 127-134. [ Links ]
Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner G, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig M, Yamanaka Y, Yool1 A 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437: 681-686. [ Links ]
Paula JC, Vallim MA, Teixeira VL 2011. What are and where are the bioactive terpenoids metabolites from Dictyotaceae (Phaeophyceae). Rev Bras Farmacogn 21: 216-228. [ Links ]
Pereira-Filho GH, Amado-Filho GM, Guimarães SMPB, Moura RL, Sumida PY, Abrantes DP, Bahia RG, Güth AZ, Jorge RR, Francini-Filho RB 2011. Reef fish and benthic assamblages of the Trindade and Martin Vaz Island Group, Southwestern Atlantic. Braz J Oceanogr 59: 201-212. [ Links ]
Pereira-Filho GH, Amado-Filho GM, Moura RL, Bastos AC, Guimarães SMPB, Salgado LT, Francini-Filho RB, Bahia RG, Abrantes DP, Guth AZ, Brasileiro PS 2012. Extensive Rhodolith beds cover the summits of southwestern atlantic ocean seamounts. J Coastal Res 28: 261-269. [ Links ]
Rinehart Jr KL, Gloer JB, Wilson GR, Hughes Jr RG, Li LH, Renis HE, McGovren JP 1983. Antiviral and antitumor compounds from tunicates. Fed Proc 42: 87-90. [ Links ]
Riul P, Lacouth P, Pagliosa PR, Christoffersen ML, Horta PA 2009. Rhodolith beds at the easternmost extreme of South America: Community structure of an endangered environment. Aquat Bot 90: 315-320. [ Links ]
Royal Society 2005. Ocean acidification due to increasing atmospheric carbon dioxide. London: The Royal Society. [ Links ]
Sabine CL, Feely RA 2007. The oceanic sink for carbon dioxide. In: Reay D, Hewitt N, Grace J, Smith K (org.). Greenhouse gas sinks. Oxfordshire: CABI Publishing, p. 31-49. [ Links ]
Saker KE, Fike JH, Veit H, Ward DL 2004. Brown seaweed-(Tasco) treated conserved forage enhances antioxidant status and immune function in heat-stressed wether lambs. J Anim Physiol An N 88: 122-130. [ Links ]
Santos AS, Riul P, Brasil ACS, Christoffersen ML 2011. Encrusting Sabellariidae (Annelida: Polychaeta) in rhodolith beds, with description of a new species of Sabellaria from the Brazilian coast. J Mar Biol Assoc UK 91: 425-438. [ Links ]
Steller DL, Foster MS 1995. Environmental factors influencing distribution and morphology of rhodoliths in Bahia Concepción, BCS Mexico. J Exp Mar Biol Ecol 194: 201-212. [ Links ]
Steller DL, Riosmena-Rodríguez R, Foster MS, Roberts C 2003 Rhodolith bed diversity in the Gulf of California: The importance of rhodolith structure and consequences of anthropogenic disturbances. Aquat Conserv 13: S5-S20. [ Links ]
Steller DL, Hernández-Ayón M, Riosmena-Rodríguez R, Cabello-Pasini A 2007. Effect of temperature on photosynthesis, growth and calcification rates of the free-living coralline alga Lithophyllum margaritae. Cienc Mar 33: 441-546. [ Links ]
Solomon S, Qin D, Manning M, Chen Z, Marquis M and others 2007. Climate change 2007: the physical science basis: contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge: Cambridge University Press. [ Links ]
Tabares P, Pimentel-Elardo SM, Schirmeister T, Hünig T, Hentschel U 2011. Anti-protease and immunomodulatory activities of bacteria associated with Caribbean Sponges. Mar Biotechnol 13: 883-892. [ Links ]
Taylor MW, Radax R, Steger D, Wagner M 2007. Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol R 71: 295-347. [ Links ]
Teixeira EH, Napimoga MH, Carneiro VA, Oliveira TM, Nascimento KS, Nagano CS, Souza JB, Havt A, Pinto VPT, Gonçalves RB, Farias WRL, Saker-Sampaio S, Sampaio AH, Cavada BS 2007. In vitro inhibition of oral streptococci binding to the acquired pellicle by algal lectins. J Appl Microbiol 103: 1001-1006. [ Links ]
Testa V 1997. Calcareous algae and corals in the inner shelf of Rio Grande do Norte, NE, Brazil. Int Coral Reef Symp 8: 737-742. [ Links ]
Testa V, Bosence DW 1999. Physical and biological controls on the formation of carbonate and siliciclastic bedforms on the northeast Brazilian shelf. Sedimentology 46: 279-301. [ Links ]
Testa V, Bosence DW, Vianna ML 1997. Submerged lithologies as indicators of relative sealevel oscillations in Rio Grande do Norte, NE Brazil. Proc 4th Cong Brasileiro de Estudos do Quaternario, p. 155-160. [ Links ]
Vecsei A 2004. A new estimate of global reefal carbonate production including the fore-reefs. Global Planet Change 43: 1-18. [ Links ]
Vicalvi MA, Milliman JD 1977. Calcium carbonate sedimentation on continental shelf off southern Brazil with special reference to benthic foraminifera. In: Frost SH, Weiss MP, Saunders JB (eds). Studies in Geol, 4, AAP p.313-328. [ Links ]
Villas-Boas AB, Riosmena-Rodriguez R, Amado-Filho GM, Maneveldt G, Figueiredo MAO 2009. Rhodolith-forming species of Lithophyllum (Corallinales; Rhodophyta) from Espírito Santo State, Brazil, including the description of L. depressum sp. nov. Phycologia 48: 237-248. [ Links ]
Vo T, Ngo D, Ta QV, Kim S 2011. Marine organisms as a therapeutic source against herpes simplex vírus infection. Eur J Pharm Sci 44: 11-20. [ Links ]
Xie L, Meng-Hua C, Jing L, Yang XM, Huang QJ 2011. Antithrombotic effect of a polysaccharide fraction from Laminaria japonica from the south China Sea. Phytother Res 25: 1362-1366. [ Links ]
Yuan YV, Walsh NA 2006. Antioxidant and antiproliferative activities of extracts from a variety of edible seaweeds. Food Chem Toxicol 44: 1144-1150. [ Links ]
Received 18 Nov 2011
Accepted 6 Jan 2012