Skip to main content
SpringerLink
Log in

Chemodiversity of the brown algae Canistrocarpus cervicornis (Dictyotaceae, Phaeophyceae) in tropical and subtropical populations along the southwestern Atlantic coast of Brazil

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Three populations of the brown seaweed Canistrocarpus cervicornis along 1800 km of the southwestern Atlantic coast were studied. Phylogenetic analysis based on the plastid and mitochondrial genes rbcL and nad1, respectively, confirmed that these populations were composed of the same taxon. Crude ethyl acetate extracts were analysed by gas chromatography coupled to a mass spectrometer (GC/MS), which revealed 13 detectable products whose fragment patterns were compatible with those expected for diterpenes. The analysis of fragment patterns identified the diterpenoid 4,7-diacetoxy-14-hydroxydolastane-1 (15), 8-diene as the major product in all the populations. Furthermore, the concentration of this diterpenoid and other products were highly variable among the three populations. However, this plasticity was not observed in sample morphology, which was generally conserved among the populations. Therefore, GC/MS enabled the detection of differences in diterpene chemodiversity within geographically distinct populations of C. cervicornis, and even though natural product abundance varied greatly, molecular markers and morphology were highly conserved.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Amico V (1995) Marine brown algae of family Cystoseiraceae: chemistry and chemotaxonomy. Phytochemistry 39:1257–1279

    Article  CAS  Google Scholar 

  • Ateweberhan M, Bruggemann JH, Breeman AM (2005) Seasonal patterns of biomass, growth and reproduction in Dictyota cervicornis and Stoechospermum polypodioides (Dictyotales, Phaeophyta) on a shallow reef flat in the southern Red Sea (Eritrea). Bot Mar 48:8–17

    Article  Google Scholar 

  • Bianco EM, Rogers R, Teixeira VL, Pereira RC (2009) Antifoulant diterpenes produced by the brown seaweed Canistrocarpus cervicornis. J Appl Phycol 21:341–346

    Article  CAS  Google Scholar 

  • Bianco EM, Teixeira VL, Pereira RC (2010) Chemical defenses of the tropical marine seaweed Canistrocarpus cervicornis against herbivory by sea urchin. Braz J Oceanogr 58:213–218

    Article  Google Scholar 

  • Bittner L, Payri CE, Couloux A, Cruaud C, de Reviers B, Rousseau F (2008) Molecular phylogeny of the Dictyotales and their position within the Phaeophyceae, based on nuclear, plastid and mitochondrial DNA sequence data. Mol Phylogenet Evol 49:211–226

    Article  CAS  PubMed  Google Scholar 

  • Boo GH, Mansilla A, Nelson W, Bellgrove A, Boo SM (2014) Genetic connectivity between trans-oceanic populations of Capreolia implexa (Gelidiales, Rhodophyta) in cool temperate waters of Australasia and Chile. Aquat Bot 119:73–79

  • Brasileiro PS, Yoneshigue-Valentin Y, Bahia RG, Reis RP, Filho GMA (2009) Algas marinhas bentônicas da região de Cabo Frio e arredores: Síntese do conhecimento. Rodriguésia 60(1):39–66

    Article  Google Scholar 

  • Castelão RM, Campos EJD, Miller JL (2004) A modelling study of coastal upwelling driven by wind and meanders of the Brazil Current. J Coast Res 203:662–671

    Article  Google Scholar 

  • Cavalcanti DN, de Oliveira MAR, de Paula JC, Barbosa LS, Fogel T, Pinto MA, Paixão ICNP, Teixeira VL (2011) Variability of a diterpene with potential anti-HIV activity isolated from the Brazilian brown alga Dictyota menstrualis. J Appl Phycol 23:873–876

    Article  CAS  Google Scholar 

  • Cronin G (2001) Resource allocation in seaweeds and marine invertebrates: chemical defense patterns in relation to defenses theories. In: McClintock J, Baker B (eds) Marine chemical ecology. CRC Press, Boca Raton, pp 325–345

    Chapter  Google Scholar 

  • De Clerck O, De Vosb P, Gillisb M, Coppejans E (2001) Molecular systematics in the genus Dictyota (Dictyotales, Phaeophyta): a first attempt based on restriction patterns of the internal transcribed spacer 1 of the rDNA (ARDRA-ITSl). Syst Geogr Plants 35:25–35

    Article  Google Scholar 

  • De Clerck O, Leliaert F, Verbruggen H, Lane CE, De Paula JC, Payo DA, Coppejans E (2006) A revised classification of the Dictyoteae (Dictyotales, Phaeophyceae) based on rbcl and 26s ribosomal DNA sequence analyses. J Phycol 42:1271–1288

    Article  Google Scholar 

  • De Paula JC, Bueno LB, Frugulhetti ICPP, Yoneshigue-Valentin Y, Teixeira VL (2007) Dictyota dolabellana sp. nov. (Dictyotaceae, Phaeophyceae) based on morphological and chemical data. Bot Mar 50:288–293

    Google Scholar 

  • De Paula JC, Bueno LB, Cavalcanti DN, Yoneshigue-Valentin Y, Teixeira VL (2008) Diterpenes from the brown alga Dictyota crenulata. Molecules 13:1253–1262

    Article  Google Scholar 

  • De 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

    Article  Google Scholar 

  • Farias de Mesquita MM, Baddini ALDQ, Netto ADP, Araujo JM, Salgueiro F, Lopes Filho EAP, De-Paula JC, Fleury BG, Cavalcanti DN, Teixeira VL (2015) Chemical similarity between Dictyota caribaea and Dictyota menstrualis (Dictyotaceae, Phaeophyceae) from the coast of Rio de Janeiro, Brazil. Biochem Syst Ecol 58:97–101

    Article  CAS  Google Scholar 

  • Fleury BG, Kelecom A, Pereira RC, Teixeira VL (1994) Polyphenols, terpenes and sterols in Brazilian Dictyotales and Fucales (Phaeophyta). Bot Mar 37:457–462

    Article  CAS  Google Scholar 

  • Fraser CI, Winter DJ, Spencer HG, Waters JM (2010) Multigene phylogeny of the southern bull-kelp genus Durvillaea (Phaeophyceae: Fucales). Mol Phylogenet Evol 57:1301–1311

    Article  CAS  PubMed  Google Scholar 

  • Freitas OSP, Oliveira AS, De-Paula JC, Pereira RC, Cavalcanti DN, Teixeira VL (2007) Chemical variation in the diterpenes from the Brazilian brown alga Dictyota mertensii (Dictyotaceae, Phaeophyta). Nat Prod Commun 2:13–15

    CAS  Google Scholar 

  • González AG, Martin JD, Norte M, Rivera P, Perales A, Fayos JF (1983) Structure and absolute configurations of Dictyota sp. diterpenes. Tetrahedron 39:3355–3357

    Article  Google Scholar 

  • Guimaraes M, Coutinho R (1996) Spatial and temporal variation of benthic marine algae at the Cabo Frio upwelling region, Rio de Janeiro, Brazil. Aquat Bot 52:283–299

    Article  Google Scholar 

  • Hay ME (2012) Marine chemical ecology: chemical signals and cues structure marine populations, communities and ecosystems. Annu Rev Mar Sci 1:193–212

    Article  Google Scholar 

  • 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. Academic Press, New York, pp 371–413

    Chapter  Google Scholar 

  • Joshi GV, Gowda CA (1975) Seasonal variations in chemical composition of Sargassum ilicifolium Grun. and sea water. Indian J Mar Sci 4:165–168

    CAS  Google Scholar 

  • Kark S, van Rensburg BJ (2007) Ecotones: marginal or central areas of transition? Isr J Ecol Evol 52:29–53

    Article  Google Scholar 

  • Kelecom A, Laneuville Teixeira V (1986) Diterpenes of marine brown algae of the family Dictyotaceae: their possible role as defense compounds and their use in chemotaxonomy. Sci Total Environ 58:109–115

    Article  CAS  PubMed  Google Scholar 

  • Le Lann K, Kervarec N, Payri CE, Deslandes E, Stiger-Pouvreau V (2008) Discrimination of allied species within the genus Turbinaria (Fucales, Phaeophyceae) using HRMAS NMR spectroscopy. Talanta 74:1079–1083

    Article  PubMed  Google Scholar 

  • Le Lann K, Kraffe E, Kervarec N, Cerantola S, Payri CE, Stiger-Pouvreau V (2014) Isolation of turbinaric acid as a chemomarker of Turbinaria conoides (J. Agardh) Kützing from South Pacific Islands. J Phycol 50:1048–1057

    Article  PubMed  Google Scholar 

  • Marty MJ, Pawlik JR (2015) A fish-feeding laboratory bioassay to assess the antipredatory activity of secondary metabolites from the tissues of marine organisms. J Vis Exp 95:52429

    Google Scholar 

  • Masuda M, Abe T, Sato S (1997) Diversity of halogenated secondary metabolites in the red alga Laurencia nipponica (Rhodomelaceae, Ceramiales). J Phycol 33:196–208

    Article  CAS  Google Scholar 

  • Oliveira AS, Cavalcanti DN, Bianco EM, De Paula JC, Pereira RC, Yoneshigue-Valentin Y, Teixeira VL (2008) Chemical composition of diterpenes from the brown alga Canistrocarpus cervicornis (Dictyotaceae, Phaeophyceae). Nat Prod Commun 3:1469–1472

    Google Scholar 

  • Ortiz-Ramírez FA, Cavalcanti DN, Villaça RC, De-Paula JC, Yoneshigue-Valentin Y, Teixeira VL (2008) Chemical variation in the diterpenes from the Brazilian brown alga Dictyota menstrualis (Dictyotaceae, Phaeophyceae). Nat Prod Commun 3:1879–1884

    Google Scholar 

  • Paul VJ, Ritson-Williams R, Sharp K (2011) Marine chemical ecology in benthic environments. Nat Prod Rep 28:345–387

    Article  CAS  PubMed  Google Scholar 

  • Plouguerné E, Hellio C, Cesconetto C, Thabard M, Mason K, Véron B, Pereira RC, Gama BAP (2010) Antifouling activity as a function of population variation in Sargassum vulgare from the littoral of Rio de Janeiro (Brazil). J Appl Phycol 22:717–724

    Article  Google Scholar 

  • Rhoades DF (1979) Evolution of plant chemical defense against herbivores. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interactions with secondary plant metabolites. Academic Press, New York, pp 3–54

    Google Scholar 

  • Saunders G, Druehl L (1992) Nucleotide sequences of the small-subunit ribosomal RNA genes from selected Laminariales (Phaeophyta). J Phycol 28:544–549

  • Silberfeld T, Rousseau F, Reviers B (2014) An updated classification of brown algae (Ochrophyta, Phaeophyceae). BioOne 35:117–156

    Google Scholar 

  • Spalding MD, Fox HE, Allen GR, Davidson N, Ferdaña ZA, Finlayson M, Halpern BS, Jorge MA, Lombana A, Lourie SA, Martin KD, McManus E, Molnar J, Recchia CA, Robertson J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience 57:573–583

    Article  Google Scholar 

  • Sudatti DB, Fujii MT, Rodrigues SV, Turra A, Pereira RC (2011) Effects of abiotic factors on growth and chemical defenses in cultivated clones of Laurencia dendroidea J. Agardh (Ceramiales, Rhodophyta). Mar Biol 158:1439–1446

    Article  CAS  Google Scholar 

  • Sun HH, McConnell OJ, Fenical W, Hirotsu K, Clardy J (1981) Tricyclic diterpenoids of the dolastane ring system from the marine alga Dictyota divaricata. Tetrahedron 37:1237–1242

    Article  CAS  Google Scholar 

  • Széchy MTM, De Paula JC (2016) Phaeophyceae: Lista de Espécies da Flora do Brasil. Rio de Janeiro: Jardim Botânico do Rio de Janeiro. [cited 2015 Sept 25]. Available from: http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB99411

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tronholm A, Steen F, Tyberghein L, Leliaert F, Verbruggen H, Siguan MAR, De Clerck O (2010) Species delimitation, taxonomy, and biogeography of Dictyota in Europe (Dictyotales, Phaeophyceae). J Phycol 46:1301–1321

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank Roberta Pacheco Silva and Samara Ribeiro da Silva for their help in the molecular biology laboratory, Dr. Silvia Mattos Nascimento for the comments that improved our manuscript, and the Program for Technological Development in Tools for Health-PDTISFIOCRUZ (Fundação Oswaldo Cruz) for use of its facilities. This work was supported by the Fundação Carlos Chagas Filho de Apoio à Pesquisa do Estado do Rio de Janeiro (BIOTA 2012 – FAPERJ E-26/111.397/2012) and a Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) scholarship to JMA.

Author information

Authors and Affiliations

  1. Programa de pós-graduação em Biodiversidade Neotropical, Universidade Federal do Estado do Rio de Janeiro, Av. Pasteur 458, 409, Rio de Janeiro, 22290-255, Brazil

    Juliana Magalhães de Araujo, Erick Alves Pereira Lopes-Filho, Fabiano Salgueiro & Joel Campos De Paula

  2. Fundação Oswaldo Cruz, Rede de Plataformas Tecnológicas, Av. Brasil, 4365 - Manguinhos, Rio de Janeiro, 21040-900, Brazil

    Marcelo Raul Romero Tappin

  3. Instituto de Biologia, Universidade Federal do Estado do Rio de Janeiro, Av. Pasteur 458, Rio de Janeiro, 22290-255, Brazil

    Rafael da Rocha Fortes

Authors
  1. Juliana Magalhães de Araujo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marcelo Raul Romero Tappin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rafael da Rocha Fortes
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Erick Alves Pereira Lopes-Filho
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fabiano Salgueiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Joel Campos De Paula
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joel Campos De Paula.

Electronic supplementary material

ESM 1

(DOCX 1.17 mb)

ESM 2

(DOCX 34.7 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Araujo, J.M., Tappin, M.R.R., da Rocha Fortes, R. et al. Chemodiversity of the brown algae Canistrocarpus cervicornis (Dictyotaceae, Phaeophyceae) in tropical and subtropical populations along the southwestern Atlantic coast of Brazil. J Appl Phycol 30, 611–618 (2018). https://doi.org/10.1007/s10811-017-1249-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-017-1249-5

Keywords

Search

Navigation