SciELO - Scientific Electronic Library Online

vol.21 issue2Using Macrocystis pyrifera (L.) C. Agardh from southern Chile as a source of applied biological compoundsPutative benefits of microalgal astaxanthin on exercise and human health author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand




Related links


Revista Brasileira de Farmacognosia

Print version ISSN 0102-695X

Rev. bras. farmacogn. vol.21 no.2 Curitiba Mar./Apr. 2011  Epub Apr 20, 2011 

Overview of the taxonomy and of the major secondary metabolites and their biological activities related to human health of the Laurencia complex (Ceramiales, Rhodophyta) from Brazil



Mutue T. FujiiI,*; Valéria CassanoII; Érika M. SteinIII; Luciana R. CarvalhoI

INúcleo de Pesquisa em Ficologia, Instituto de Botânica, Brazil
IIDepartamento de Botânica, Universidade de São Paulo, Brazil
IIIPrograma de Pós-graduação, Departamento de Botânica, Universidade de São Paulo, Brazil




In Brazil, the Laurencia complex is represented by twenty taxa: Laurencia s.s. with twelve species, Palisada with four species (including Chondrophycus furcatus now that the proposal of its transference to Palisada is in process), and Osmundea and Yuzurua with two species each. The majority of the Brazilian species of the Laurencia complex have been phylogenetically analyzed by 54 rbcL sequences, including five other Rhodomelacean species as outgroups. The analysis showed that the Laurencia complex is monophyletic with high posterior probability value. The complex was separated into five clades, corresponding to the genera: Chondrophycus, Laurencia, Osmundea, Palisada, and Yuzurua. A bibliographical survey of the terpenoids produced by Brazilian species showed that only six species of Laurencia and five of Palisada (including C. furcatcus) have been submitted to chemical analysis with 48 terpenoids (47 sesquiterpenes and one triterpene) isolated. No diterpenes were found. Of the total, 23 sesquiterpenes belong to the bisabolane class and eighteen to the chamigrene type, whose biochemical precursor is bisabolane, two are derived from lauranes and four are triquinols. Despite the considerable number of known terpenes and their ecological and pharmacological importance, few experimental biological studies have been performed. In this review, only bioactivities related to human health were considered.

Keywords: biodiversity, biological activities, Laurencia complex, seaweeds, taxonomy, terpenoids




The red algae of the Laurencia complex comprehend 430 species (and infraspecific taxa) listed in the database at present, of which 134 have been flagged as currently accepted taxonomically. They are reported worldwide from the temperate to tropical shores of the world, occurring from the intertidal to the subtidal zone up to 65 m in depth (Guiry & Guiry, 2010). Laurencia sensu lato is an extremely rich source of halogenated secondary metabolites with diverse structural features (Fenical, 1975; Erickson, 1983) that can be divided into two groups according to their biogenetic origin. The first one is the nonterpenoid group, which contains the acetogenins derived from the metabolism of fatty acids. The other one is the terpenoid group, in which the sesquiterpenes are the most abundant, but also containing diterpenes and triterpenes (Fernández et al., 2005).

The taxonomy of the Laurencia complex has undergone several changes based on the use of new vegetative morpho-anatomical and reproductive features, cladistic analyses of morphological characters and molecular approaches based on the plastidial rbcL gene (Nam et al., 1994; Garbary & Harper, 1998; Nam, 1999, 2006, 2007; Martin-Lescanne et al., 2010). These changes include the resurrection of the genus Osmundea Stackhouse (Nam et al., 1994), the elevation of the subgenus Chondrophycus Tokida & Saito (in Saito, 1967) to the generic rank (Garbary & Harper, 1998), the new delineations of the genera Chondrophycus, Laurencia and Osmundea (Nam, 1999), the definition of the proposal of the genus Palisada (Yamada) K.W. Nam based on Yamada's (1931) section Palisadae (Nam, 2006) and its later validation (Nam, 2007), and the establishment of the genus Yuzurua (K.W. Nam) Martin-Lescanne based on Nam's (1999) subgenus Yuzurua (Martin-Lescanne et al., 2010). Thus, five genera are currently assigned to the Laurencia complex: Laurencia J.V. Lamouroux itself, Osmundea, Chondrophycus, Palisada and Yuzurua. Several morpho-anatomical and reproductive characters used in the taxonomy of the complex have been shown to have diagnostic value at the generic level only (Saito, 1967; Nam et al., 1994; Garbary & Harper, 1998; Nam, 1999, 2006). Many species have no defined taxonomic boundaries and present extensive morphological plasticity, making their taxonomic delimitation difficult. In this context, the use of molecular markers has proven to be useful for delimiting the taxa and inferring their phylogenetic relationships and has corroborated the current classification system (Nam et al., 2000; McIvor et al., 2002; Abe et al., 2006; Fujii et al., 2006; Díaz-Larrea et al., 2007; Cassano et al., 2009; Gil-Rodríguez et al., 2009; Martin-Lescanne et al., 2010; Rocha-Jorge et al., 2010).

The genera are distinguished by a combination of both vegetative and reproductive characteristics: number of pericentral cells per vegetative axis, position of the first pericentral cell relative to the trichoblast, origin of the tetrasporangia, absence or presence of fertility of the second pericentral cell, number of sterile pericentral cells in the tetrasporangial axis, origin of the spermatangial branches, formation pattern of the spermatangial branches on trichoblasts, the number of pericentral cells in procarp-bearing segments of female trichoblasts, and probably post-fertilization features associated with the formation time of the auxiliary cell. Many of these characters overlap among the genera. Effectively, the genus Laurencia is distinct from the other four genera by the presence of four pericentral cells per axial segment; two pericentral cells occur in Osmundea, Chondrophycus, Palisada and Yuzurua (Nam et al., 1994; Garbary & Harper, 1998; Nam, 1999, 2006; Martin-Lescanne et al., 2010). The genus Osmundea is distinct from the other genera by the tetrasporangial production from random cortical cells rather than from particular pericentral cells and filament-type rather than trichoblast-type spermatangial development (Nam et al., 1994). The genus Chondrophycus is characterized by spermatangial branches produced from two laterals on the suprabasal cell of trichoblasts, but remaining partly sterile, and a tetrasporangial axis with the first and second pericentral cells never fertile (Nam, 1999). In the genus Palisada, the spermatangial branches are produced from one of two laterals on the suprabasal cells of trichoblasts and the second pericentral cell in the tetrasporangial axis is always fertile; the resulting axis has one sterile pericentral cell (Nam, 2006). The genus Yuzurua shares the majority of the morphological characters of Palisada, from which it was recently segregated, but differs by not having palisade-like cells, by the presence of secondary pit-connections between cortical cells, and by procarp-bearing segments with five pericentral cells rather than four (Fujii et al., 1996).

The species of the Laurencia complex are widely distributed along the Brazilian coast from Ceará (Pinheiro-Joventino et al., 1998) to Rio Grande do Sul (Baptista, 1977), growing in different types of habitats (Fujii & Sentíes, 2005) and constituting an important element of Brazilian phycological flora (Oliveira Filho, 1977).

The members of this complex, in particular Laurencia s.s., are prolific synthesizers of structurally elaborate halogenated secondary metabolites and have been reported to produce a numerous diversity of unique compounds, especially terpenes (Martín & Darias, 1978; Erickson, 1983; Pereira & Teixeira, 1999). Although the function of these secondary metabolites has not yet been clearly defined, it has been suggested that these metabolites play a major role in mediating ecological interactions such as algae/herbivore interactions (Hay et al., 1987, Hay & Steinberg, 1992), with these compounds acting as a defense against being eaten or as a deterrent against epibiota, i.e., an antifouling activity (da Gama et al., 2002; Cassano et al., 2008; Lhullier et al., 2009), or protection against pathogens (König & Wright, 1997). Thus, ecological pressures such as competition for space, fouling of the surface, predation, and successful reproduction have led to the evolution of unique secondary metabolites with various biological activities (Ireland et al., 2000). The prominent biological activity of marine terpenes is evident in their ecological role in the marine environment and makes them interesting as potential drugs. Many of these natural products are pharmacologically active and marine algae, especially those from tropical and subtropical seas, are able to produce a wide range of compounds, many of which exhibit at least some degree of bioactivity (Fernández et al., 1998, 2005; da Gama et al., 2002; Cassano et al., 2008; Lhullier et al., 2009; Machado et al., 2010; Santos et al., 2010). In fact, the marine environment represents a treasure trove of useful products awaiting discovery for the treatment of infectious and parasitic diseases (Vairappan et al., 2004; Morales et al., 2006), cancer (Mohammed et al., 2004; Stein et al., 2011), cognitive diseases, inflammatory processes, and viral infections (Sakemi et al., 1986). Despite the many structures known and their ecological and pharmacological importance, only a few biosynthetic studies have been performed on marine terpenoid compounds (Gross & König, 2006). In this paper, the current status of the taxonomy of the Laurencia complex in Brazil is outlined, together with the diversity of secondary metabolites produced and their biological activities of relevance to human health.


Materials and Methods

The present work is a compilation of the data on the Laurencia complex from Brazil, including the current results on the taxonomy and phylogeny of the group, secondary metabolites and their biological activities related to human health.

We performed a phylogenetic analysis using 54 rbcL sequences, with seventeen samples from Brazil (Table 1). Multiple alignments for sequences were constructed using the computer program BioEdit (Hall, 1999). A total of 250 nucleotides were removed from all rbcL sequences at the beginning and end of the sequences because many sequences from the GenBank were incomplete, producing a data set of 1217 base pairs. Phylogenetic relationships were inferred with MrBayes v.3.0 beta 4 (Huelsenbeck & Ronquist, 2001). The model used in the Bayesian analysis was selected based on maximum likelihood ratio tests implemented by the software Modeltest version 3.06 (Posada & Crandall, 1998) with a significance level of 0.01 by the Akaike information criterion. For the Bayesian analysis, four chains of the Markov chain Monte Carlo (one hot and three cold) were used, sampling one tree every ten generations for 1,000,000 generations starting with a random tree. The 50,000 generations were discarded as 'burn in'. The model used in the Bayesian analysis for rbcL sequences was the general-time-reversible model of nucleotide substitution with invariant sites and gamma distributed rates for the variable sites (GTR+I+G).


Results and Discussion

In Brazil, the red algae of the Laurencia complex are represented by four of the five genera that integrate the complex: Laurencia itself, Palisada, Osmundea, and Yuzurua. The first is the most diverse with twelve species, followed by Palisada (including Chondrophycus furcatus) with four species and Osmundea and Yuzurua with two species each (Table 2). The habit of several representatives of the Laurencia complex from Brazil and some generic morphological diagnostic characters are displayed in Figures 1-25.





The topology of the Bayesian tree with corresponding Bayesian posterior probabilities values (PP) is shown in Figure 26. The phylogenetic analysis shows a monophyletic Laurencia complex with high PP support (100%) in relation to the members of the outgroup, corroborating the previous results verified for the group (Abe et al., 2006; Fujii et al., 2006; Martin-Lescanne et al., 2010). The Laurencia complex was separated into five clades, corresponding to the genera: Laurencia, Osmundea, Palisada, Chondrophycus, and Yuzurua. The earliest diverging clade was the genus Palisada with six species and high support (100% PP), which included also Chondrophycus furcatus, an endemic species from Brazil. This result shows clearly that C. furcatus must be transferred to the genus Palisada and, with its future nomenclatural change, there will be no more representatives of Chondrophycus in Brazil. The monophyletic genera Chondrophycus and Osmundea were sister groups with a posterior probability of 86%. The monophyletic clade that corresponds to the genus Yuzurua showed higher molecular affinity with Laurencia than Palisada, from which it was recently segregated. The genus Laurencia included fifteen taxa with a posterior probability of 80%. Laurencia marilzae formed a monophyletic clade with high support (100% PP) and was separated from all other Laurencia s.s., forming a distinct lineage, suggesting that L. marilzae represents a new genus within the Laurencia complex.



The bibliographical survey on the terpenoids produced by species of the Laurencia complex from the Brazilian coast shows that only five species of Laurencia and three of Palisada (including C. furtactus) have been submitted to chemical analysis and that, so far, 48 terpenoids have been isolated: 47 sesquiterpenes and one triterpene. Diterpenes have not been found in Brazilian species (Table 3).

The compounds isolated from the native algae include 21 sesquiterpenes belonging to the bisabolane class, seventeen belonging to the chamigrane type, whose biochemical precursor is bisabolane, and four triquinols, that posses a rare structure but are derived from the same biogenetic origin as the bisabolane- and chamigrane-derived terpenoids [2E,6E-farnesylpyrophosphate (FPP)]. Besides bisabolane and chamigrane terpenoids, the introduced seaweed Laurencia caduciramulosa produces two laurane-type compounds not found in Brazilian native algae (Table 3).

With respect to Palisada perforata and P. flagellifera, they generally do not produce sesquiterpenoids or acetogenins, classical metabolites produced by Laurencia. Although the presence of sesquiterpenes was not expected in this group, triquinane alcohols (compounds 47 and 26) were found in P. perforata by using a high sensitivity extraction method (HS-SPME) (Gressler et al., 2011). These compounds were not active against bacterial strains or the yeast Candida albicans, but showed some antioxidant activity. Chondrophycus furcatus is distinct from the other members of Palisada by producing only triterpenoids (Rodriguez-Concepción, 2006) that are synthesized via the same precursor (FPP) as the sesquiterpenoids from Brazilian Laurencia species. However, on the basis of morphology, it does not fit perfectly into either Laurencia or Palisada due to the presence of secondary pit-connections between adjacent cortical cells, a characteristic more related to Laurencia, and to the production of two pericentral cells, instead of four per each axial segment, a characteristic shared by Chondrophycus, Palisada, Yuzurua and Osmundea (Fujii & Sentíes, 2005).

Most of the metabolites (15) that have been isolated from Laurencia dendroidea, L. scoparia, L. microcladia, and L. obtusa [denominations that, in Brazil, refer to the same botanical species (Cassano, 2009)] are derived from chamigrane, with very similar or even identical structures, such as elatol found in L. dendroidea and L. microcladia; L. scoparia produces five sesquiterpenoids from bisabolane and two triquinols. Both L. aldingensis and L. catarinensis synthesize metabolites whose precursor is bisabolane, exhibiting a high degree of similarity between them, as can be seen in Figure 26.

Although species of the Laurencia complex are known to produce interesting active metabolites that possess important pharmacological potential, experimental biological activity assays have been performed with only with six species: Laurencia catarinensis, L. dendroidea, L. translucida, L. aldingensis, L. caduciramulosa, and Palisada flagellifera. The three former are native Brazilian species and the most studied of these is L. dendroidea. More than twenty compounds were identified in this species and several of them showed biological activities such as anthelmintic activity against the parasitic stage of Nippostrongilus brasiliensis (Davyt, 2003; 2006), antileishmanial activity against the insect-stage promastigotes of Leishmania amazonensis (Machado et al., 2010), human pathogenic antifungal properties (Stein et al., 2011), and significant levels of toxicity towards a model tumor cell line (human uterine sarcoma, MES-SA) (Stein et al., 2011). Thus, studies on the biological activities of the secondary metabolites isolated from the Laurencia complex should be encouraged with the goal of finding new sources with pharmaceutical applications.



This study was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (Proc. 473322/2008-0), and the Fundação de Amparo à Pesquisa do Estado de São Paulo (Proc. 10/50193-1, Proc. 10/52244-2). Additional support was provided by the Ministerio de Ciencia e Innovación of the Spanish Government (CGL 2010-14881). MT Fujii thanks the CNPq for a Research Productivity Fellowship (Proc. 301438/2009-9) and EM Stein thanks FAPESP for a Master's Student Fellowship (Proc. 2008/07775-0). Beneficiary of financial support from CAPES-Brazil.



Abe T, Kurihara A, Kawaguchi S, Terada R, Masuda M 2006. Preliminary report on the molecular phylogeny of the Laurencia complex (Rhodomelaceae). Coast Mar Sci 30: 209-213.         [ Links ]

Amado Filho GM, Horta PA, Brasileiro PS, Barros-Barreto MB, Fujii MT 2006. Subtidal benthic marine algae of the Marine State Park of Laje de Santos (São Paulo, Brazil). Braz J Oceanogr 54: 225-234.         [ Links ]

Baptista LRM 1977. Flora marinha de Torres (Chlorophyta, Xanthophyta, Phaeophyta, Rhodophyta). Bol Inst Biociências, Univ Federal do Rio Grande do Sul (Bot) 37: 1-244.         [ Links ]

Brito LVR, Széchy MTM, Cassano V 2002. Levantamento taxonômico das macroalgas da zona das marés de costões rochosos adjacentes ao Terminal Marítimo Almirante Maximiano Fonseca, Baía da Ilha Grande, RJ. Atlântica 24: 17-26.         [ Links ]

Carvalho LR, Fujii MT, Barbizan DS 2000. Estudo químico dos metabólitos de Laurencia flagellifera (Ceramiales, Rhodophyta) como subsídio à quimiossistemática In XIII Congresso da Sociedade Botânica de São Paulo. São Paulo, Brazil. p. 184.         [ Links ]

Carvalho LR, Fujii MT, Roque NF, Kato MJ, Lago JHG 2003. Aldingenin A, new brominated sesquiterpene from red algae Laurencia aldingensis. Tetrahedron Lett 44: 2637-2640.         [ Links ]

Carvalho LR, Fujii MT, Roque NF, Lago JHG 2006. Aldingenin derivatives from the red alga Laurencia aldingensis. Phytochemistry 67: 1331-1335.         [ Links ]

Cassano V 2009. Taxonomia e filogenia do complexo Laurencia (Ceramiales, Rhodophyta), com ênfase no estado do Rio de Janeiro, Brasil. São Paulo, 328 p. Tese de Doutorado, Instituto de Botânica de São Paulo.         [ Links ]

Cassano V, Széchy MTM, Fujii MT 2006. Laurencia caduciramulosa (Ceramiales, Rhodophyta) from Ilha Grande Bay, Rio de Janeiro, Brazil: a recently introduced species into the Atlantic Ocean? Cryptogamie, Algol 27: 265-277.         [ Links ]

Cassano V, De-Paula JC, Fujii MT, Teixeira VL 2008. Sesquiterpenes from the introduced red seaweed Laurencia caduciramulosa (Rhodomelaceae, Rhodophyta). Biochem Syst Ecol 36: 223-226.         [ Links ]

Cassano V, Díaz-Larrea J, Sentíes A, Oliveira MC, Gil-Rodriguez MC, Fujii MT 2009. Evidence for the conspecificity of Palisada papillosa with P. perforata (Ceramiales, Rhodophyta) from the western and eastern Atlantic Ocean on the basis of morphological and molecular analyses. Phycologia 48: 86-100.         [ Links ]

Cocentino ALM. 1994. Família Rhodomelaceae (Ceramiales, Rhodophyta) na Praia de Serrambi – Ipojuca-PE - Brasil. Recife, 193 p. Dissertação de Mestrado, Programa de Pós-Graduação em Botânica, Universidade Federal Rural de Pernambuco.         [ Links ]

Cocentino ALM, Fujii MT, Guimarães NCL 2006. A descoberta de Chondrophycus gemmiferus (Ceramiales, Rhodophyta) na Plataforma continental da bacia potiguar, RN, confirma a ocorrência da espécie na flora ficológica brasileira. XI congresso Brasileiro de Ficologia & Simpósio Latino-americano sobre algas nocivas. Itajaí, Brazil.         [ Links ]

Cordeiro-Marino M 1978. Rodofíceas bentônicas marinhas do estado de Santa Catarina. Rickia 7: 1-243.         [ Links ]

Cordeiro-Marino M, Fujii MT 1985. Laurencia catarinensis (Rhodomelaceae, Rhodophyta), a new species from Ilha de Santa Catarina, Brazil. Rev Bras Bot 8: 47-53.         [ Links ]

Cordeiro-Marino M, Fujii MT, Pinheiro-Joventino F 1994. Morphological and cytological studies of Laurencia furcata Cordeiro-Marino and Fujii (Rhodophyta, Rhodomelaceae): a new species from Brazil. Cryptogamic Bot 4: 373-380.         [ Links ]

Da Gama BAP, Pereira RC, Carvalho AGV, Coutinho R, Yoneshigue-Valentin Y 2002. The effects of seaweed secondary metabolites on biofouling. Biofouling 18: 13-20.         [ Links ]

Davyt D, Fernandez R, Suescun L, Mombrú AW, Saldaña J, Dominguez L, Coll J, Fujii M T, Manta E 2001. New sesquiterpene derivatives from the red alga Laurencia scoparia. Isolation, structure determination, and anthelmintic activity. J Nat Prod 64: 1552-1555.         [ Links ]

Davyt D, Fernandez R, Suescun L, Mombrú AW, Saldaña J, Dominguez L, Coll J, Fujii M T, Manta E 2006. Bisabolanes from the red alga Laurencia scoporia. J Nat Prod 69: 1113-1116.         [ Links ]

Díaz-Larrea J, Sentíes A, Fujii MT, Pedroche FF, Oliveira MC 2007. Molecular evidence for Chondrophycus poiteaui var. gemmiferus comb. et stat. nov. (Ceramiales, Rhodophyta) from the Mexican Caribbean Sea: implications for the taxonomy of the Laurencia complex. Bot Mar 50: 250-256.         [ Links ]

Erickson KL 1983. Constituents of Laurencia. In Scheuer PJ (ed.) Marine natural products: chemical and biological perspectives vol. 5. New York: Academic Press, p. 131-257.         [ Links ]

Estevam C, Carvalho LR, Fujii MT 2001. Estudos morfológicos e quimiotaxomicos comparativos em Laurencia papillosa e L. perforata (Ceramiales, Rhodophyta) do litoral brasileiro. V Encontro de Iniciação Científica do Instituto de Botânica. São Paulo, Brazil, p. 31.         [ Links ]

Estevam C, Carvalho LR 2002. Estudo químico dos metabólitos secundários de Laurencia furcata Cord.-Marino et Fujii (Ceramiales, Rhodophyta). VI Encontro de Iniciação Científica do Instituto de Botânica. São Paulo, Brazil, p. 32.         [ Links ]

Fenical W 1975. Halogenation in the Rhodophyta, a review. J Phycol 11: 245-259.         [ Links ]

Fernández JJ, Souto ML, Gil LV, Norte M 1998. Evaluation of the cytotoxic activity of the polyethers isolated from Laurencia. Bioorg Med Chem 6: 2237-2243.         [ Links ]

Fernández JJ, Souto ML, Gil LV, Norte M 2005. Isolation of naturally occurring dactylomelane metabolites as Laurencia constituents. Tetrahedron 61: 8910-8915.         [ Links ]

Figueiredo-Creed MA de O, Yoneshigue-Valentin Y 1997. Chlorophyta, Phaeophyta e Rhodophyta. In Marques MCM (ed.). Mapeamento da cobertura vegetal e listagens das espécies ocorrentes na Área de Proteção Ambiental de Cairuçu, Município de Parati, RJ. Série Estudos e Contribuições, Instituto de Pesquisas do Jardim Botânico do Rio de Janeiro, Rio de Janeiro, Brasil, p. 30-36.         [ Links ]

Figueiredo MA de O, Barros-Barreto MBB, Reis RP 2004. Caracterização das macroalgas nas comunidades marinhas da Área de Proteção Ambiental de Cairuçú, RJ - subsídios para futuros monitoramentos. Rev Bras Bot 27: 11-17.         [ Links ]

Fistarol Z, Carvalho LR 2002. Estudos químicos de Laurencia translucida (Ceramiales, Rhodophyta). São Paulo, 48 p. Monografia de Conclusão de Curso, Faculdade de Ciências da Saúde de São Paulo.         [ Links ]

Fujii MT 1990. Gênero Laurencia (Rhodomelaceae, Rhodophyta) no Estado de São Paulo: aspectos biológicos e taxonômicos. Rio Claro, 145 p. Dissertação de Mestrado, Universidade Estadual Paulista.         [ Links ]

Fujii MT 1998. Estudos morfológicos, quimiotaxonômicos e citogenéticos em quatro espécies selecionadas de Laurencia (Ceramiales, Rhodophyta) do litoral brasileiro. Rio Claro, 176 p. Tese de Doutorado, Universidade Estadual Paulista.         [ Links ]

Fujii MT, Cordeiro-Marino M 1996. Laurencia translucida sp. nov. (Ceramiales, Rhodophyta) from Brazil. Phycologia 35: 542-549.         [ Links ]

Fujii MT, Sentíes A 2005. Taxonomia do complexo Laurencia (Rhodomelaceae, Rhodophyta) do Brasil, com ênfase nas espécies dos estados de São Paulo e do Espírito Santo. In Sentíes A, Dreckmann KM (eds) Monografias Ficológicas. II. Universidad Autônoma Metropolitana–Iztapalapa, México e Instituto de Botânica, São Paulo, Brasil, p. 69-135.         [ Links ]

Fujii MT, Villaça R 2003. On the occurrence of Laurencia caraibica (Ceramiales, Rhodophyta) in Atol das Rocas, Brazil. Hidrobiológica 13: 33-38.         [ Links ]

Fujii MT, Collado-Vides L, Cordeiro-Marino M 1996. Morphological studies of Laurencia gemmifera and Laurencia poiteaui (Rhodomelaceae, Rhodophyta) from the Nichupté Lagoon System, Quintana Roo, Mexico. Bot Mar 39: 317-326.         [ Links ]

Fujii MT, Guimarães SMPB, Alves JP 2005. Ocorrência de Laurencia venusta (Ceramiales, Rhodophyta) no Espírito Santo, Brasil: distribuição biogeográfica disjunta ou introdução recente? In Pereira RC et al. (orgs). Formação de Ficólogos: um compromisso com a sustentabilidade dos recursos aquáticos. Rio de Janeiro: Museu Nacional, p. 527-536.         [ Links ]

Fujii MT, Guimarães SMPB, Gurgel CF, Fredericq S 2006. Characterization and phylogenetic affinities of the red alga Chondrophycus flagelliferus (Rhodomelaceae, Ceramiales) from Brazil on the basis of morphological and molecular evidence. Phycologia 45: 432-441.         [ Links ]

Garbary DJ, Harper JT 1998. A phylogenetic analysis of the Laurencia complex (Rhodomelaceae) of the red algae. Cryptogamie, Algol 19: 185-200.         [ Links ]

Gil-Rodríguez MC, Sentíes A, Díaz-Larrea J, Cassano V, Fujii MT 2009. Laurencia marilzae sp. nov. (Ceramiales, Rhodophyta) from the Canary Islands, Spain, based on morphological and molecular evidence. J Phycol 45: 264-271.         [ Links ]

Gressler V, Stein EM, Dörr F, Fujii MT, Colepicolo P, Pinto E 2011. Sesquiterpenes from the essential oil of Laurencia dendroidea (Ceramiales, Rhodophyta): isolation, biological activities and distribution among seaweeds. Rev Bras Farmacogn 21: _____-         [ Links ]___..

Gross H, König GM 2006. Terpenoids from marine organisms: unique structures and their pharmacological potential. Phytochem Rev 5: 115-141.         [ Links ]

Guimarães SMPB 2006. Checklist of Rhodophyta from the State of Espírito Santo. Bolm Inst Bot 17: 143-194.         [ Links ]

Guiry MD, Guiry GM 2010. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway., access December 2010.         [ Links ]

Hall TA 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41: 95-98.         [ Links ]

Hay ME, Fenical W, Gustafson K 1987. Chemical defense against diverse coral-reef herbivores. Ecology 68: 1581-1591.         [ Links ]

Hay ME, Steinberg PD 1992. The chemical ecology of plant–herbivore interactions in marine versus terrestrial communities. In Rosenthal J, Berenbaum M (eds) Herbivores: Their Interaction with Secondary Plant Metabolites, vol. II, Evolutionary and Ecological Processes. New York: Academic Press, p. 371-413.         [ Links ]

Horta PA 2000. Macroalgas do infralitoral do sul e sudeste do Brasil: taxonomia e biogeografia. São Paulo, 301 p. Tese de doutorado, Universidade de São Paulo.         [ Links ]

Howe MA, Taylor WR. 1931. Notes on new or little-known marine algae from Brazil. Brittonia 1: 7-33.         [ Links ]

Huelsenbeck JP, Ronquist FR 2001. MrBayes. Bayesian inference of phylogeny. Biometrics 17: 754-755.         [ Links ]

Ireland CM, Copp BR, Foster MP, McDonald LA, Radisky DC, Swersey JC 2000. Bioactive compounds from the sea. In Martin RE, Carter EP, Davis LM (eds.) Marine and freshwater products handbook. Lanceaster: Technomic Publishing, p. 641-661.         [ Links ]

Joly AB 1965. Flora marinha do litoral norte do estado de São Paulo e regiões circunvizinhas Fac Fil Ciênc Letr Univ S Paulo (Bot) 21: 1-393.         [ Links ]

König GM, Wright AD 1997. Sesquiterpene content of the antibacterial dichloromethane extract of the marine red alga Laurencia obtusa. Planta Med 63: 186-187.         [ Links ]

Lhullier C, Donnangelo A, Caro M, Palermo JA, Horta PA, Falkenberg M, Schenkel EP 2009. Isolation of elatol from Laurencia microcladia and its palatability to the sea urchin Echinometra lucunter. Biochem Syst Ecol 37: 254-259.         [ Links ]

Lhullier C, Falkenberg M, Ioannou E, Quesada A, Papazafiri P, Horta PA, Schenkel EP, Vagias C, Roussis V 2010. Cytotoxic halogenated metabolites from the Brazilian red alga Laurencia catarinensis. J Nat Prod 73: 27-32.         [ Links ]

Machado FL, Pacienza-Lima Wallace, Rossi-Bergmann B, Gestinari LMS, Fujii MT, De-Paula JC, Costa SS, Lopes NP, Kaiser CR, Soares AR 2011. Antileishmanial sesquiterpenes from the Brazilian red alga Laurencia dendroidea. Planta Med 76: DOI: 10.1055/s-0030-1250526 .         [ Links ]

Martín JD, Darias J 1978. Algal sesquiterpenoids. In Schevev PJ (ed.). Marine Natural Products vol 1. New York: Academic Press, p. 125-173.         [ Links ]

Martin-Lescanne J, Rousseau F, De Reviers B, Payri C, Couloux A, Cruaud C, Le Gall L 2010. Phylogenetic analyses of the Laurencia complex (Rhodomelaceae, Ceramiales) support recognition of five genera: Chondrophycus, Laurencia, Osmundea, Palisada and Yuzurua stat. nov. Eur J Phycol 45: 51-61.         [ Links ]

McIvor L, Maggs CA, Guiry MD, Hommersand MH 2002. Phylogenetic analysis of the geographically disjunct genus Osmundea Stackhouse (Rhodomelaceae, Rhodophyta). Constancea 83.9 [online publication of the Jepson Herbarium, UC, Berkeley:         [ Links ]

Mohammed KA, Hossain CF, Zhang L, Bruick RK, Zhou YD 2004. Laurediterpineol, a new diterpene from the tropical marine alga Laurencia intricata that potently inhibits HIF-1 mediated hypoxic signaling in breast tumor cells. J Nat Prod 67: 2002-2007.         [ Links ]

Morales JL, Cantillo-Ciau ZO, Sanchez-Molina I, Mena-Rejon GJ. 2006. Screening of antibacterial and antifungal activities of six marine macroalgae from coasts of Yucatan peninsula. Pharm Biol 44: 632-635.         [ Links ]

Nam KW 1999. Morphology of Chondrophycus undulata and C. parvipapillata and its implications for the taxonomy of the Laurencia (Ceramiales, Rhodophyta) complex. Eur J Phycol 34: 455-68.         [ Links ]

Nam KW 2006. Phylogenetic re-evaluation of the Laurencia complex (Rhodophyta) with a description of L. succulenta sp. nov from Korea. J Appl Phycol 18: 679-697.         [ Links ]

Nam KW 2007. Validation of the generic name Palisada (Rhodomelaceae, Rhodophyta). Algae 22: 53-55.         [ Links ]

Nam KW, Maggs CA, Garbary DJ 1994. Resurrection of the genus Osmundea with an emendation of the generic delineation of Laurencia (Ceramiales, Rhodophyta). Phycologia 33: 384-395.         [ Links ]

Nam KW, Maggs CA, McIvor L, Stanhope MJ 2000. Taxonomy and phylogeny of Osmundea (Rhodomelaceae, Rhodophyta) in Atlantic Europe. J Phycol 36: 759-772.         [ Links ]

Nunes JMC 1998. Catálogo de algas marinhas bentônicas do estado da Bahia, Brasil. Acta Bot Malac 23: 5-21.         [ Links ]

Nunes JMC 2005. Rodofíceas marinhas bentônicas do estado da Bahia, Brasil. São Paulo, 410 p. Tese de doutorado, Instituto de Biociências, Universidade de São Paulo.         [ Links ]

Oliveira Filho EC 1969. Algas marinhas do sul do estado do Espirito Santo (Brasil). I. Ceramiales. Bolm Fac Fil Ciênc Letr Univ S Paulo (Bot) 26: 1-277.         [ Links ]

Oliveira Filho E C 1977. Algas marinhas bentônicas do Brasil. São Paulo, 407 p. Tese de Livre Docência, Instituto de Biociências, Universidade de São Paulo.         [ Links ]

Oliveira Filho EC, Ugadim Y 1974. New references of benthic marine algae to Brazilian flora. Bol Bot Univ São Paulo 2: 71-91.         [ Links ]

Oliveira Filho EC, Ugadim Y 1976. A survey of the marine algae of Atol das Rocas (Brazil). Phycologia 15: 41-44.         [ Links ]

Paes e Mello LB, Pereira SMB 1990. Estudos taxonômicos sobre a Família Rhodomelaceae (Rhodophyta - Ceramiales) no litoral Oriental do Estado do Rio Grande do Norte. I. Gênero Laurencia Lamouroux. Trab Oceanogr, Univ. Federal de Pernambuco 21: 165-185.         [ Links ]

Pedrini AG. 1980. Algas marinhas bentônicas da Baía de Sepetiba e arredores. Rio de Janeiro, 379 p. Dissertação de Mestrado, Museu Nacional, Universidade Federal do Rio de Janeiro.         [ Links ]

Pedrini AG de, Gonçalves JEA, Fonseca MCS, Zaú AS, Lacorte CC 1989. A survey of the marine algae of Trindade Island, Brazil. Bot Mar 32: 97-99.         [ Links ]

Pereira RC, Teixeira VL 1999. Sesquiterpenos das algas marinhas Laurencia Lamouroux (Ceramiales, Rhodophyta). 1. Significado ecológico. Quim Nova 22: 369-374.         [ Links ]

Pereira SMB, Carvalho MFO, Angeiras JA, Pedrosa MEB, Oliveira NMB, Torres J, Gestinari LMS, Concentino AM, Santos MD, Nascimento PRF, Cavalcanti DR 2002. Algas marinhas bentônicas do estado de Pernambuco. In Tabarelli M, Silva JMC (orgs). Diagnóstico da biodiversidade de Pernambuco. Recife: Secretaria de Ciência, Tecnologia e Meio Ambiente, Editora Massangana, v. 1, p. 97-124.         [ Links ]

Pereira SMB, Bandeira-Pedrosa ME, Burgos DC 2005. Macroalgae from the Saint Peter's and Saint Paul's Archipelago (Brazil). Phycologia suppl 36: 80.         [ Links ]

Pinheiro-Joventino F, Dantas NP, Maraschin CDH 1998. Distribuição de algas marinhas no litoral de Fortaleza, Ceará, Brasil. Arq Cien Mar 31: 29-40.         [ Links ]

Posada D, Crandall KA 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817-818.         [ Links ]

Rocha-Jorge R 2010. Diversidade de macroalgas do Parque Estadual Marinho da Laje de Santos, SP, Brasil. São Paulo, 176 p. Dissertação de Mestrado, Programa de Pós-Graduação em Biodiversidade Vegetal e Meio Ambiente, Instituto de Botânica.         [ Links ]

Rocha-Jorge R, Cassano V, Oliveira MC, Fujii MT 2010. The occurrence of Laurencia marilzae (Ceramiales, Rhodophyta) in Brazil based on morphological and molecular data. Bot Mar 53: 143-162.         [ Links ]

Rodriguez-Concepción M 2006. Early steps in isoprenoid biosynthesis: multilevel regulation of the supply of common precursors in plant cells. Phytochem Rev 5: 1-15.         [ Links ]

Saito Y 1967. Studies on Japanese species of Laurencia, with special reference to their comparative morphology. Mem Fac Fish Hokkaido Univ 15: 1-81.         [ Links ]

Sakemi S, Higa T, Jefford CW, Bernardinelli G. Venustatriol 1986. A new, antiviral, triterpene tetracyclic ether from Laurencia venusta. Tetrahedron Lett 27: 4287-4290.         [ Links ]

Santos AO, Veiga-Santos P, Ueda-Nakamura T, Dias Filho BP, Sudatti DB, Bianco EM, Pereira RC, Nakamura CV 2010. Effect of elatol, isolated from red seaweed Laurencia dendroidea on Leishmania amazonensis. Mar Drugs 8: 2733-2743.         [ Links ]

Silva IB 2010. Diversidade de algas marinhas bentônicas dos recifes e ambientes adjacentes de Maracajaú, APA dos Recifes de Corais, RN, Brasil. São Paulo, 334 p. Tese de Doutorado, Programa de Pós-Graduação em Biodiversidade Vegetal e Meio Ambiente, Instituto de Botânica.         [ Links ]

Stein EM, Andreguetti DX, Sousa C, Fujii MT, Baptista M, Colepicolo P, Indig GL 2011. Search for citotoxic agents in multiple Laurencia sensu lato seaweed species (Ceramiales, Rhodophyta) harvested from the Atlantic Ocean zone that bates the Brazilian State of Espírito Santo. Rev Bras Farmacogn 21: in press.         [ Links ]

Széchy MTM, Paula EJ de 1997. Macroalgas epífitas em Sargassum (Phaeophyta – Fucales) do litoral dos estados do Rio de Janeiro e São Paulo, Brasil. Leandra 12: 1-10.         [ Links ]

Széchy MTM, Nassar CAG 2005. Flora ficológica bentônica da Baía da Ribeira, sul do estado do Rio de Janeiro: Avaliação após duas décadas de operação da Central Nuclear Almirante Álvaro Alberto. In Pereira RC et al. (orgs). Formação de Ficólogos: um compromisso com a sustentabilidade dos recursos aquáticos. Rio de Janeiro: Museu Nacional, p. 373-397.         [ Links ]

Széchy MTM, Nassar CAG, Falcão C, Maurat MCS 1989. Contribuição ao inventário das algas marinhas bentônicas de Fernando de Noronha. Rodriguésia 67: 53-61.         [ Links ]

Széchy MTM, Amado Filho GM, Cassano V, De-Paula JC, Barros-Barreto MBB, Reis RP, Marins-Rosa BV, Moreira FM 2005. Levantamento florístico das macroalgas da Baía de Sepetiba e adjacências, RJ: ponto de partida para o Programa GloBallast no Brasil. Acta Bot Bras 19: 587-596.         [ Links ]

Taylor WR 1960. Marine algae of the eastern tropical and subtropical coasts of the Americas. Michigan: Ann Arbor, The University of Michigan Press.         [ Links ]

Torrano Silva BN 2010. Flora de macrófitas marinhas do Arquipélago de Abrolhos e do Recife Sebastião Gomes (BA). São Paulo, 422 p. Dissertação de Mestrado, Programa de Pós-Graduação em Botânica, Universidade de São Paulo.         [ Links ]

Vairappan CS, Kawamoto T, Miwa H, Suzuki M 2004. Potent antibacterial activity of halogenated compounds against antibiotic-resistant bacteria. Planta Med 70: 1087-1090.         [ Links ]

Yamada Y 1931. Notes on Laurencia, with special reference to the Japanese species. Univ Calif Publ Bot 16: 185-310.         [ Links ]

Yoneshigue Y 1985. Taxonomie et ecologie des algues marines dans la region de Cabo Frio, (Rio de Janeiro), Brésil. Marseille, France, 466 p. Tese de Doutorado, Faculte des Sciences de Luminy, Uníverisité d' Aix-Marseille II.         [ Links ]

Yoneshigue-Valentin Y, Fujii MT, Gurgel F D 2003. Osmundea lata (Howe & Taylor) comb. nov. (Ceramiales, Rhodophyta) from southeastern Brazilian continental shelf. Phycologia 42: 301-307.         [ Links ]



Received 23 Dec 2010
Accepted 22 Jan 2011



* E-mail:, Tel. +55 11 5067 6123; Fax: +55 11 5073 3678.

Creative Commons License All the contents of this journal, except where otherwise noted, is licensed under a Creative Commons Attribution License