Abstract
Based on morphological studies, four species of Chondracanthus Kützing were previously reported on the Brazilian coast: C. acicularis (Roth) Fredericq, C. elegans (Greville) Guiry, C. saundersii C.W.Schneider and C.E.Lane and C. teedei (Mertens ex Roth) Fredericq. In the present study, specimens of Chondracanthus were collected from intertidal and subtidal zones (up to 18 m depth); morphological, molecular and phylogenetic analyses were performed using DNA barcoding (cox1) as a tool in a survey of Rhodophyta biodiversity in São Paulo state. Unlike what we expected, C. saundersii is widely distributed, and many specimens were misidentified as C. acicularis or C. teedei before this study, suggesting the necessity of an accurate revision in the previous identifications of the species of Chondracanthus in Brazil. Tetrasporangial and cystocarpic structures of C. saundersii are described for the first time. Our results confirm that the utilization of cox1 sequences as DNA barcode is an efficient tool to complement morphological identification for species of the genus Chondracanthus.
Similar content being viewed by others
Abbreviations
- cox1:
-
Cytochrome c oxidase
- GTR:
-
General-time-reversible model invariable sites and shape parameter of the gamma distribution
- MP:
-
Maximum parsimony
- NJ:
-
Neighbor-joining
- PP:
-
Posterior probability
- rbcL:
-
Gene coding for the large subunit of RUBISCO
References
Amado-Filho GM, Horta PA, Brasileiro PS, Barros-Barreto MBB, Fujii MT (2006) Sub-tidal benthic marine algae of the Marine State Park of Laje de Santos (São Paulo, Brazil). Braz J Oceanogr 54:225–234. https://doi.org/10.1590/S1679-87592006000300006
Baptista LRM (1977) Flora Ilustrada do Rio Grande do Sul. Bol Inst Biocienc Univ Fed Rio Grande do Sul 37:1–248
Braga MRA (1986) Estudos taxonômicos em Gigartina teedei (Roth) Lamouroux e G. elegans Greville in Saint-Hilaire (Rhodophyta, Gigartinales). Rev Bras Bot 9:191–199
Braga MRA (1990) Reproductive characteristics of Gigartina teedei (Roth) Lamouroux (Rhodophyta, Gigartinales), a turf-forming species: Field and laboratory cultures studies. Bot Mar 33:401–409
Bustamante DE, Won BY, Miller KN, Cho TO (2017) Wilsonosiphonia gen. nov. (Rhodomelaceae, Rhodophyta) based on molecular and morpho-anatomical characters. J Phycol 53:368–380. https://doi.org/10.1111/jpy.12512
Carvalho FAF (1983) Bionomia Bêntica do Complexo Recifal no Litoral do Estado da Paraíba, com Ênfase nas Macrófitas. Dissertation, São Paulo University, São Paulo
Cordeiro-Marino M (1978) Rodofíceas Bentônicas Marinhas do Estado de Santa Catarina. Rickia 7:1–243
Correia MMF (1987) Rodofíceas Marinhas Bentônicas do Litoral Oriental do Estado do Maranhão. Coleç Cienc Biol, Ser Bo. 1:1–256
Freshwater DW, Rueness J (1994) Phylogenetic relationships of some European Gelidium (Gelidiales, Rhodophyta) species, based on rbcL nucleotide sequence analysis. Phycologia 33:187–194. https://doi.org/10.2216/i0031-8884-33-3-187.1
Guimarães SMPB (2006) A revised checklist of benthic marine Rhodophyta from the state of Espírito Santo, Brazil. Bol Inst Bot 17:143–194
Guimarães SMPB, Fujii MT, Pupo D, Yokoya NS (2004) Reavaliações das características morfológicas e implicações taxonômicas no gênero Polysiphonia sensu lato (Ceramiales, Rhodophyta) do litoral dos Estados de São Paulo e Espírito Santo, Brasil. Rev Bras Bot 27:163–183. https://doi.org/10.1590/S0100-84042004000100017
Guiry MD, Guiry GM (2018) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org. Accessed on 22 March 2018
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Holmgren PK, Holmgren NH (2018) Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. http://sweetgum.nybg.org/ih/. Accessed on 22 March 2018
Hommersand MH, Guiry MD, Fredericq S, Leister GL (1993) New perspectives in the taxonomy of the Gigartinaceae (Gigartinales, Rhodophyta). Hydrobiologia 260(261):105–120. https://doi.org/10.1007/BF00049009
Hommersand MH, Fredericq S, Freshwater DW, Hughey J (1999) Recent developments in the systematics of the Gigartinaceae (Gigartinales, Rhodophyta) based on rbcL sequence analysis and morphological evidence. Phycol Res 47:139–151. https://doi.org/10.1046/j.1440-1835.1999.00168.x
Horta PA (2000) Macroalgas do Infralitoral do Sul e Sudeste do Brasil: taxonomia e biogeografia. Dissertation, São Paulo University, São Paulo
Hughey JR, Hommersand MH (2008) Morphological and molecular systematic study of Chondracanthus (Gigartinaceae, Rhodophyta) from Pacific North America. Phycologia 47:124–155. https://doi.org/10.2216/07-06.1
Iha C, Milstein D, Guimarães SMPB, Freshwater DW, Oliveira MC (2015) DNA barcoding reveals high diversity in the Gelidiales of the Brazilian southeast coast. Bot Mar 58:295–305. https://doi.org/10.1515/bot-2014-0069
Iha C, Jamas M, Guimarães SMPB, Fujii MT, Freshwater WD, Oliveira MC (2017) Pterocladiella (Gelidiales, Rhodophyta) species of Brazil including morphological studies of Pterocladiella media and a reassessment of Pterocladiella taylorii. Phycologia 56:624–637. https://doi.org/10.2216/17-8.1
Jamas M, Iha C, Guimarães SMPB, Oliveira MC, Fujii MT (2017) Morphological and molecular studies on Gelidiaceae and Gelidiellaceae (Gelidiales, Rhodophyta) from Brazil with description of the new species Gelidium calidum. Phytotaxa 314:195–218. https://doi.org/10.11646/phytotaxa.314.2.2
Joly AB (1965) Flora marinha do litoral norte do Estado de São Paulo e regiões circunvizinhas. Univ São Paulo: Fac Filos Cienc Let Bot 21:1–393. https://doi.org/10.11606/issn.2318-5988.v21i1p5-393
Kano CH, Sena FS, Cassano V, Fujii MT (2017) Caloglossa species diversity (Delesseriaceae, Rhodophyta) based on morphology and DNA data with emphasis on southeastern Brazil. Braz J Bot 40:551–564. https://doi.org/10.1007/s40415-016-0360-1
Le Gall L, Saunders G (2010) DNA barcoding is a powerfull tool to uncover algal diversity: a case study of the Phyllophoraceae (Gigartinales, Rhodophyta) in the Canadian flora. J Phycol 46:374–389. https://doi.org/10.1111/j.1529-8817.2010.00807.x
Miranda PTC (1986) Composição e distribuição das Macroalgas Bentônicas no Manguezal do Rio Ceará (Estado do Ceará-Brasil). Dissertation, Federal University of Pernambuco, Recife
Nauer F, Guimarães NR, Cassano V, Yokoya NS, Oliveira MC (2014) Hypnea species (Gigartinales, Rhodophyta) from the southeastern coast of Brazil based on molecular studies complemented with morphological analyses, including descriptions of Hypnea edeniana sp. nov. and H. flava sp. nov. Eur J Phycol 49:550–575
Nauer F, Cassano V, Oliveira MC (2015) Description of Hypnea pseudomusciformis sp. nov., a new species based on molecular and morphological analyses, in the context of the H. musciformis complex (Gigartinales, Rhodophyta). J Appl Phycol 27:2405–2417
Nauer F, Cassano V, Oliveira MC (2016) Hypnea wynnei and Hypnea yokoyana (Cystocloniaceae, Rhodophyta), two new species revealed by a DNA barcoding survey on the Brazilian coast. Phytotaxa 268:123–134
Nunes JMC, Santos ACC, Minervino A, Brito KS (1999) Algas marinhas bentônicas do município de Ilhéus, Bahia, Brasil. Acta Bot Malac 24:5–12
Pereira SMB, Oliveira-Filho EC, Araújo MSVB, Paes E, Mello LB, Fernandes De Carvalho FA, Câmara Neto CT (1981) Prospecção dos bancos de algas marinhas do estado do Rio Grande do Norte—2ª Parte: profundidade de 10-45 metros. Série: Brasil. Sudene. Estudos de Pesca 9:25–81
Pereira SMB, Oliveira-Carvalho MF, Angeiras JAP, Bandeira-Pedrosa ME, Oliveira NMB, Torres J, Gestinari LMS, Cocentino ALM, Santos MD, Nascimento PRF, Cavalcanti DR (2002) Algas marinhas bentônicas do Estado de Pernambuco. In: Tabarelli M, Silva JMC (eds) Diagnóstico da Biodiversidade de Pernambuco. Secretaria de Ciência Tecnologia e Meio Ambiente, Recife, pp 97–124
Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818. https://doi.org/10.1093/bioinformatics/14.9.817
Robba L, Russel SJ, Barker GL, Brodie J (2006) Assessing the use of the mitochondrial cox1 marker for use in DNA barcoding of red algae (Rhodophyta). Am J Bot 93:1101–1108. https://doi.org/10.3732/ajb.93.8.1101
Rocha-Jorge R, Harari J, Fujii MT (2012) Macroalgal composition and its association with local hydrodynamics in the Laje de Santos Marine State Park, Southwestern Atlantic, São Paulo, Brazil. Braz J Oceanogr 60:405–419. https://doi.org/10.1590/S1679-87592012000300012
Rocha-Jorge R, Cassano V, Barros-Barreto MB, Díaz-Larrea J, Sentíes A, Gil-Rodriguez MC, Fujii MT (2013) Osmundea sanctarum sp. nov. (Ceramiales, Rhodophyta) from the southwestern Atlantic Ocean. Phytotaxa 100:41–56. https://doi.org/10.11646/phytotaxa.100.1.5
Ronquist F, Huelsenbeck JP (2003) Mr Bayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. https://doi.org/10.1093/bioinformatics/btg180
Saunders GW (2005) Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Philos Trans Royal Soc Lond B Biol Sci 360:1879–1888. https://doi.org/10.1098/rstb.2005.1719
Schneider CW, Lane CE (2005) Notes on the marine algae of the Bermudas. 7. Additions to the flora including Chondracanthus saundersii sp. nov. (Rhodophyta, Gigartinaceae) based on rbcL sequence analysis. Phycologia 44:72–83
Soares LP, Fujii MT (2012) Epiphytic macroalgae from Boa Viagem Beach, Recife, Pernambuco State, Brazil. Check List. J Species List Distrib 8:662–665. https://doi.org/10.15560/8.4.662
Soares LP, Carneiro PBM, Fujii MT (2018) New records of red marine algae to the coast of Ceará, northeastern Brazil. Hoehnea 45:323–347. https://doi.org/10.1590/2236-8906-41/2017
Swofford DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Methods). Version 4. Sinauer Associates, Sunderland. https://doi.org/10.1111/j.0014-3820.2002.tb00191.x
Ugadim Y (1975) Algas Marinhas Bent Bentônicas do Litoral Sul do Estado de São Paulo e do Litoral do estado do Paraná. III—Divisão Rhodophyta (2): Cryptonemiales, Gigartinales e Rhodymeniales. Bol Bot São Paulo Univ 3:115–164. https://doi.org/10.11606/issn.2316-9052.v3i0p115-163
Vasconcelos ERTPP, Bernardi J, Reis TNV, Cocentino ALM, Mallea AJA, Fujii MT (2016) Influência da urbanização no padrão de distribuição vertical das comunidades bentônicas da região entremarés dos recifes de arenito de Pernambuco, Brasil. Serie Oceanologica 15:74–88
Villaça R, Pedrini AG, Pereira SMB, Figueiredo MAO (2006) Flora Marinha Bentônica das Ilhas Oceânicas Brasileiras. In: Alves RJV, Castro JWA (eds) Ilhas Oceânicas Brasileiras: da Pesquisa ao Manejo. MMA, SBF, Brasília, pp 107–146
Wynne MJ (2017) A checklist of benthic marine algae of the tropical and subtropical western Atlantic: fourth revision. Nova Hedwigia Beihefte 145:1–202
Yang MY, Macaya EC, Kim MK (2015) Molecular evidence for verifying the distribution of Chondracanthus chamissoi and C. teedei (Gigartinaceae, Rhodophyta). Bot Mar 58:103–113. https://doi.org/10.1515/bot-2015-0011
Yoneshigue Y (1985) Taxonomie et Ecologie des Algues Marines dans la Region de Cabo Frio, Rio de Janeiro, Bresil. Dissertation, L’Universite D’Aix-Marseille II, Luminy
Acknowledgements
We thank the technical help from Carolina de Oliveira Franco. We acknowledge Fundação de Amparo à Pesquisa no Estado de São Paulo (FAPESP, BIOTA Proc. 07/51270-7; 2016/50370-7) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq Proc. 484647/2012-1; 440523/2015-0) for the project financial support. RRJ thanks FAPESP for PhD Fellowship (Proc. 2010/20559-4). MCO, MTF and ONJ thank CNPq for Research Productivity Fellowships; This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior Brasil (CAPES) Finance Code 001. Molecular data from French specimens were produced at the Service de Systématique Moléculaire of the Muséum National d’Histoire Naturelle (CNRS - UMS 2700) with funds provided by the ATM ‘Taxonomie moléculaire: DNA Barcode et gestion durable des collections.’ Sequencing was performed by Genoscope through the projects entitled ‘Speed ID’ and ‘Bibliothèque du Vivant.’
Author information
Authors and Affiliations
Contributions
RRJ, MTF, FN, IBS and MCO conducted field work. RRJ and MTF conducted taxonomic work, gathered and analyzed data. FN sequenced specimens and conducted molecular biology work. FN, ONJ, LLG and MCO gathered data and conducted phylogenetic analysis. MTF and MCO supervised the study and contributed to the discussion. All authors were involved in writing and discussion of the manuscript.
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Rocha-Jorge, R., Nauer, F., Silva, I.B. et al. Diversity of Chondracanthus (Gigartinaceae, Rhodophyta) on the Brazilian coast based on molecular and morphological evidences. Braz. J. Bot 41, 889–900 (2018). https://doi.org/10.1007/s40415-018-0501-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40415-018-0501-9