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Licensed Unlicensed Requires Authentication Published by De Gruyter March 16, 2018

Guidelines for DNA barcoding of coralline algae, focusing on Lithophylloideae (Corallinales) from Brazil

  • Beatriz N. Torrano-Silva

    Beatriz N. Torrano-Silva initial investigation was in invasive species, followed by taxonomy and flora composition based on traditional techniques. For her PhD research she worked at University of São Paulo and also at Universidad Autónoma de Baja Califórnia Sur. Her last years were dedicated to coralline algae diversity, taxonomy and systematics, combining the traditional methodologies with molecular biology as an important ally. She is especially interested in bringing science to society and is currently a professor at Instituto Federal de Educação, Ciência e Tecnologia de São Paulo (IFSP), Brazil.

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    , Bruno R. Vieira

    Bruno R. Vieira works as an editor and author of biology and sciences in Somos Educação S.A., Brazil, and is a volunteer teacher at a nonprofit educational organization. He graduated in biology at University of São Paulo (USP), where he also completed his undergraduate training research in phycology. He has been working with education and scientific divulgation for 9 years. His main goal is to develop different and interesting approaches to teach and attract people’s interest in scientific knowledge. He has edited 21 books, written 10 books and developed more than 150 digital learning objects.

    , Rafael Riosmena-Rodríguez

    Rafael Riosmena-Rodríguez was for over 20 years one of the leading scientists in Mexico in the field of marine botany, and a leading researcher in the field of rhodolith taxonomy and ecology. He contributed largely as the principal investigator and leader of the Marine Botany Laboratory at UABCS. Dr. Riosmena-Rodríguez produced more than a 100 scientific articles, over 40 projects as P.I., 40 book chapters, and 5 books. He was the main advisor of 12 PhD, 20 Master’s and 30 Bachelor’s students. Dr. Riosmena-Rodríguez untimely passed away in March 2016.

    and Mariana C. Oliveira

    Mariana C. Oliveira is a full professor of University of São Paulo (USP), Brazil. Her PhD work was on molecular phylogeny of the Bangiales. Her main expertise is in molecular phylogeny and taxonomy of algae, genomics of algae and bacteria, focusing mainly on red algae. She is interested in the origin, evolution and diversity of Rhodophyta. Presently she integrates the Phycological Society of America as international VP, the coordination committee of the Biota-FAPESP program and is the president of the Botany Advisory committee of CNPq.

From the journal Botanica Marina

Abstract

Multiple-marker (COI-5P, UPA, psbA and rbcL-3P) and two algorithmic approaches [automatic barcode gap discovery (ABGD) and Poisson tree process (PTP)] were used for species delimitation of Lithophylloideae in Brazil. The integrative approach was mostly congruent between markers and algorithmic methods of species delimitation, suggesting the occurrence of 24 species. Based on morphology and molecular data, Amphiroa rigida, Amphiroa vanbosseae, Lithophyllum atlanticum, Lithophyllum kaiseri, Lithophyllum margaritae, Titanoderma pustulatum, Titanoderma prototypum and Paulsilvella huveorum, which were previously reported for Brazil, are confirmed in this work. Six new species are distinguished by both molecular and morphological traits, and they are provisionally named as Amphiroa sp. 1, Amphiroa sp. 2, Amphiroa sp. 3, Lithophyllum sp. 1, Lithophyllum sp. 2 and Lithophyllum sp. 3. Another 10 species are cryptic and cannot be distinguished based on traditionally used morphological traits. These include Amphiroa sp. 4, Lithophyllum sp. 4, three species that are morphologically named under Amphiroa beauvoisii, and six that share the morphology described for Amphiroa fragilissima. All four markers used were useful for species delimitation. However, a combination of practical aspects and levels of intra- and interspecific divergence values led us to propose the use of rbcL-3P as a standard DNA barcode marker for the Corallinales.

About the authors

Beatriz N. Torrano-Silva

Beatriz N. Torrano-Silva initial investigation was in invasive species, followed by taxonomy and flora composition based on traditional techniques. For her PhD research she worked at University of São Paulo and also at Universidad Autónoma de Baja Califórnia Sur. Her last years were dedicated to coralline algae diversity, taxonomy and systematics, combining the traditional methodologies with molecular biology as an important ally. She is especially interested in bringing science to society and is currently a professor at Instituto Federal de Educação, Ciência e Tecnologia de São Paulo (IFSP), Brazil.

Bruno R. Vieira

Bruno R. Vieira works as an editor and author of biology and sciences in Somos Educação S.A., Brazil, and is a volunteer teacher at a nonprofit educational organization. He graduated in biology at University of São Paulo (USP), where he also completed his undergraduate training research in phycology. He has been working with education and scientific divulgation for 9 years. His main goal is to develop different and interesting approaches to teach and attract people’s interest in scientific knowledge. He has edited 21 books, written 10 books and developed more than 150 digital learning objects.

Rafael Riosmena-Rodríguez

Rafael Riosmena-Rodríguez was for over 20 years one of the leading scientists in Mexico in the field of marine botany, and a leading researcher in the field of rhodolith taxonomy and ecology. He contributed largely as the principal investigator and leader of the Marine Botany Laboratory at UABCS. Dr. Riosmena-Rodríguez produced more than a 100 scientific articles, over 40 projects as P.I., 40 book chapters, and 5 books. He was the main advisor of 12 PhD, 20 Master’s and 30 Bachelor’s students. Dr. Riosmena-Rodríguez untimely passed away in March 2016.

Mariana C. Oliveira

Mariana C. Oliveira is a full professor of University of São Paulo (USP), Brazil. Her PhD work was on molecular phylogeny of the Bangiales. Her main expertise is in molecular phylogeny and taxonomy of algae, genomics of algae and bacteria, focusing mainly on red algae. She is interested in the origin, evolution and diversity of Rhodophyta. Presently she integrates the Phycological Society of America as international VP, the coordination committee of the Biota-FAPESP program and is the president of the Botany Advisory committee of CNPq.

Acknowledgements

We thank Dr. Carlos F.D. Gurgel, Dr. Alan Templeton, Dr. Alexandros Stamatakis, Dr. Enrique Lessa, Dr. Guillaume Achaz and Dr. Joan Pons for their help in assessing the applicability of our grouping methods. We thank Dr. Paul Gabrielson and Dr. Judith Sutherland who kindly shared their expertise on coralline material amplification before we began our first steps in this work. The Fundação de Apoio à Pesquisa do Estado de São Paulo (FAPESP) provided scholarship and research funding for B.N.T.S. Funder ID: 10.13039/501100001807 (2010/19234-3 and 2013/11833-3). M.C.O. also thanks the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; 301491/2013-5). Three reviewers provided valuable suggestions to improve this paper.

References

Adey, W.H. and P.J. Adey. 1973. Studies on the biosystematics and ecology of the epilithic crustose Corallinaceae of the British Isles. Br. Phycol. J. 8: 343–407.10.1080/00071617300650381Search in Google Scholar

Ahrens, D., T. Fujisawa, H.J. Krammer, J. Eberle, S. Fabrizi and A.P. Vogler. 2016. Rarity and incomplete sampling in DNA-based species delimitation. Systematic Biol. 65: 478–494.10.1093/sysbio/syw002Search in Google Scholar PubMed

Bailey, J.C. 1999. Plylogenetic positions of Lithophyllum incrustans and Titanoderma pustulatum (Corallinaceae, Rhodophyta) based on 18S rRNA gene sequence analyses, with a revised classification of the Lithophylloideae. Phycologia 38: 208–216.10.2216/i0031-8884-38-3-208.1Search in Google Scholar

Bittner, L., C.E. Payri, G.W. Maneveldt, A. Couloux, C. Cruaud, B. de Reviers and L. Le Gall. 2011. Evolutionary history of the Corallinales (Corallinophycidae, Rhodophyta) inferred from nuclear, plastidial and mitochondrial genomes. Mol. Phylogenet. Evol. 61: 697–713.10.1016/j.ympev.2011.07.019Search in Google Scholar PubMed

Broom, J.E.S., D.R. Hart, T.J. Farr, W.A. Nelson, K.F. Neill, A.S. Harvey and W.J. Woelkerling. 2008. Utility of psbA and nSSU for phylogenetic reconstruction in the Corallinales based on New Zealand taxa. Mol. Phylogenet. Evol.46: 958–973.10.1016/j.ympev.2007.12.016Search in Google Scholar PubMed

Carro, B., L. Lopez, V. Peña, I. Bárbara and R. Barreiro. 2014. DNA barcoding allows the accurate assessment of European maerl diversity: a Proof-of-Concept study. Phytotaxa 190: 176–189.10.11646/phytotaxa.190.1.12Search in Google Scholar

Cassano, V., J. Díaz-Larrea, A. Sentíes, M.C. Oliveira, M.C. Gil-Rodríguez and M.T. Fuji. 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: 86–100.10.2216/0031-8884-48.2.86Search in Google Scholar

Cianciola, E.N., T.R. Popolizio, C.W. Schneider and C.E. Lane. 2010. Using molecular-assisted alpha taxonomy to better understand red algal biodiversity in Bermuda. Diversity 2: 946–958.10.3390/d2060946Search in Google Scholar

Clarkston, B.E. and G.W. Saunders. 2010. A comparison of two DNA barcode markers for species discrimination in the red algal family Kallymeniaceae (Gigartinales, Florideophyceae), with a description of Euthora timburtonii sp. nov. Botany 88: 119–131.10.1139/B09-101Search in Google Scholar

Costa, E.S., E.M. Plastino, R. Petti, E.C. Oliveira and M.C. Oliveira. 2012. The Gracilariaceae Germplasm Bank of the University of São Paulo, Brazil – a DNA barcoding approach. J. Appl. Phycol. 24: 1643–1653.10.1007/s10811-012-9828-ySearch in Google Scholar

Farr, T., J. Broom, D. Hart, K. Neill and W. Nelson. 2009. Common coralline algae of northern New Zealand: an identification guide. NIWA Information Series 70, Wellington, New Zealand. pp. 125.Search in Google Scholar

Freshwater, D.W. and J. Rueness. 1994. Phylogenetic relationship of some European Gelidium (Gelidiales, Rhodophyta) species based on rbcL nucleotide sequence analysis. Phycologia 33: 187–194.10.2216/i0031-8884-33-3-187.1Search in Google Scholar

Freshwater, D.W., K. Tudor, K. O’Shaughnessy and B. Wysor. 2010. DNA barcoding in the red algal order Gelidiales: comparison of COI with rbcL and verification of the “barcoding gap.” Cryptogamie Algol. 31: 435–449.Search in Google Scholar

Freshwater, D.W., J.N. Idol, S.L. Parham, C. Fernández-García, N. León, P.W. Gabrielson and B. Wysor. 2017. Molecular assisted identification reveals hidden red algae diversity from the Burica Peninsula, Pacific Panama. Diversity 9: 19.10.3390/d9020019Search in Google Scholar

Fujisawa, T. and T.G. Barraclough. 2013. Delimiting species using single-locus data and the generalized mixed yule coalescent (GMYC) approach: a revised method and evaluation on simulated datasets. Syst. Biol. 62: 707–724.10.1093/sysbio/syt033Search in Google Scholar PubMed PubMed Central

Gabrielson, P.W., K.A. Miller and P.T. Martone. 2011. Morphometric and molecular analyses confirm two distinct species of Calliarthron (Corallinales, Rhodophyta), a genus endemic to the northeast Pacific. Phycologia 50: 298–316.10.2216/10-42.1Search in Google Scholar

Galtier, N., B. Nabholz, S. Glémin and G.D.D. Hurst. 2009. Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Mol. Ecol. 18: 4541–4550.10.1111/j.1365-294X.2009.04380.xSearch in Google Scholar PubMed

Goff, L.J. and D.A. Moon. 1993. PCR amplification of nuclear and plastid genes from algal herbarium specimens and algal spores. J. Phycol. 29: 381–384.10.1111/j.0022-3646.1993.00381.xSearch in Google Scholar

Guiry, M.D. and D.J.A. West. 1983. Life history and hybridization studies on Gigartina stellata and Petrocelis cruenta. J. Phycol.19: 474–494.10.1111/j.0022-3646.1983.00474.xSearch in Google Scholar

Harvey, A.S. and W.J. Woelkerling. 2007. A guide to nongeniculate coralline red algal (Corallinales, Rhodophyta) rhodolith identification. Cienc. Mar.33: 411–426.10.7773/cm.v33i4.1210Search in Google Scholar

Harvey, A.S., W.J. Woelkerling, T.J. Farr, K.F. Neill and W.A. Nelson. 2005. Coralline algae of central New Zealand: An identification guide to common ‘crustose’ species. NIWA Information Series 57, Wellington. 145 pp.Search in Google Scholar

Harvey, A.S., W.J. Woelkerling and A.J.K. Millar. 2009. The genus Amphiroa (Lithophylloideae, Corallinaceae, Rhodophyta) from the temperate coasts of the Australian continent, including the newly described A. klochkovana. Phycologia 48: 258–290.10.2216/08-84.1Search in Google Scholar

Hebert, P.D.N., A. Cywinska, S.L. Ball and J.R. deWaard. 2003. Biological identifications through DNA barcodes. Proc. R. Soc. Lond. B 270: 313–321.10.1098/rspb.2002.2218Search in Google Scholar PubMed PubMed Central

Henriques, M.C., R. Riosmena-Rodriguez, L.M. Coutinho and M.A.O. Figueiredo. 2014. Lithophylloideae and Mastophoroideae (Corallinales, Rhodophyta) from the Brazilian continental shelf. Phytotaxa 190: 112–129.10.11646/phytotaxa.190.1.9Search in Google Scholar

Hernández-Kantún, J.J., F. Rindi, W.H. Adey, S. Heesch, V. Peña, L. Le Gall and P.W. Gabrielson. 2015a. Sequencing type material resolves the identity and distribution of the generitype Lithophyllum incrustans, and related European species L. hibernicum and L. bathyporum (Corallinales, Rhodophyta). J. Phycol. 51: 791–807.10.1111/jpy.12319Search in Google Scholar PubMed

Hernández-Kantún, J.J., R. Riosmena-Rodriguez, J.M. Hall-Spencer, V. Peña, C.A. Maggs and F. Rindi. 2015b. Phylogenetic analysis of rhodolith formation in the Corallinales (Rhodophyta). Eur. J. Phycol. 50: 46–61.10.1080/09670262.2014.984347Search in Google Scholar

Hernández-Kantún, J.J., P. Gabrielson, J.R. Hughey, L. Pezzolesi, F. Rindi, N.M. Robinson, V. Peña, R. Riosmena-Rodriguez, L. Le Gall and W. Adey. 2016. Reassessment of branched Lithophyllum spp. (Corallinales, Rhodophyta) in the Caribbean Sea with global implications. Phycologia 55: 619–639.10.2216/16-7.1Search in Google Scholar

Hind, K.R. and G.W. Saunders. 2013. A molecular phylogenetic study of the tribe Corallineae (Corallinales, Rhodophyta) with an assessment of genus-level taxonomic features and descriptions of novel genera. J. Phycol. 49: 103–114.10.1111/jpy.12019Search in Google Scholar PubMed

Hind, K.R., P.W. Gabrielson and G.W. Saunders. 2014. Molecular-assisted alpha taxonomy reveals pseudocryptic diversity among species of Bossiella (Corallinales, Rhodophyta) in the eastern Pacific Ocean. Phycologia 53: 443–456.10.2216/13-239.1Search in Google Scholar

Iha, C., D. Milstein, S.M.P.B. Guimarães, W. Freshwater and M.C. Oliveira. 2015. DNA barcoding reveals high diversity in the Gelidiales of the Brazilian southeast coast. Bot. Mar. 58: 295–305.10.1515/bot-2014-0069Search in Google Scholar

Jesionek, M.B., R.G. Bahia, J.J. Hernández-Kantún, W.H. Adey, Y. Yoneshigue-Valentin, L.L. Longo and G.M. Amado-Filho. 2016. A taxonomic account of non-geniculate coralline algae (Corallinophycidae, Rhodophyta) from shallow reefs of the Abrolhos Bank, Brazil. Algae 31: 317–340.10.4490/algae.2016.31.11.16Search in Google Scholar

Jesus, P.B., F. Nauer, G.M. Lyra, V. Cassano, M.C. Oliveira, J.M.C. Nunes and A.S. Schnaldelbach. 2016. Species-delimitation and phylogenetic analyses of some cosmopolitan species of Hypnea (Rhodophyta) reveal synonyms and misapplied names to H. cervicornis, including a new species from Brazil. J. Phycol. 52: 774–792.10.1111/jpy.12436Search in Google Scholar PubMed

Keats, D.W. 1997. Lithophyllm insipidum Adey, Townsend et Boykins and L. flvescens sp. nov.: two flt lithophylloid coralline algae (Corallinales, Rhodophyta) abundant in shallow reef environments in Fiji. Phycologia: 36: 351–365.10.2216/i0031-8884-36-5-351.1Search in Google Scholar

Kogame, K., S. Uwai, R.J. Anderson, H.-G. Choi and J.J. Bolton. 2017. DNA barcoding of South African geniculate coralline red algae (Corallinales, Rhodophyta). S. Afr. J. Bot. 108: 337–341.10.1016/j.sajb.2016.08.013Search in Google Scholar

Le Gall, L. and G.W. Saunders. 2010. DNA barcoding is a powerful tool to uncover algal diversity: a case study of the Phyllophoraceae (Gigartinales, Rhodophyta) in the Canadian flora. J. Phycol. 46: 374–389.10.1111/j.1529-8817.2010.00807.xSearch in Google Scholar

Martone, P.T., S.C. Lindstrom, K.A. Miller and P.W. Gabrielson. 2012. Chiharaea and Yamadaia (Corallinales, Rhodophyta) represent reduced and recently derived articulated coralline morphologies. J. Phycol. 48: 859–868.10.1111/j.1529-8817.2012.01190.xSearch in Google Scholar PubMed

Mayden, R.L. 1997. A hierarchy of species concepts: the denouement in the saga of the species problem. In: (M.F. Claridge, H.A. Dawah and M.R. Wilson, eds) Species: the units of diversity. Chapman and Hall, London. pp. 381–423.Search in Google Scholar

Mayr, E. 1963. Animal species and evolution. The Belnap Press of Harvard University, Cambridge. pp. i-xvi + 797.10.4159/harvard.9780674865327Search in Google Scholar

Milne, I., F. Wright, G. Rowe, D.F. Marshal, D. Husmeier and G. McGuire. 2004. TOPALi: software for automatic identification of recombinant sequences within DNA multiple alignments. Bioinformatics 20: 1806–1807.10.1093/bioinformatics/bth155Search in Google Scholar PubMed

Milstein, D., A.S. Medeiros, E.C. Oliveira and M.C. Oliveira. 2012. Will a DNA barcoding approach be useful to identify Porphyra species (Bangiales, Rhodophyta)? J. Appl. Phycol. 24: 837–845.10.1007/s10811-011-9702-3Search in Google Scholar

Moura, C.W.N. and S.M.P.B. Guimarães. 2005. O gênero Amphiroa (Lithophylloideae, Rhodophyta) no litoral do Brasil. Monografías Ficológicas 2: 3–65.Search in Google Scholar

Moura, C.W.N., J.E. Kraus and M. Cordeiro-Marino. 1997. Metodologia para obtenção de cortes histológicos com historresina e coloração com azul de toluidina O para algas coralináceas (Rhodophyta, Corallinales). Hoehnea 24: 17–27.Search in Google Scholar

Nauer, F., N.R. Guimarães, V. Cassano, N.S. Yokoya and M.C. Oliveira. 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: 550–575.10.1080/09670262.2014.981589Search in Google Scholar

Padial, J.M., A. Miralles, I. De La Riva and M. Vences. 2010. The integrative future of taxonomy. Front. Zool. 7: 16.10.1186/1742-9994-7-16Search in Google Scholar PubMed PubMed Central

Pardo, C., L. Lopez, V. Peña, J. Hernández-Kantún, L. Le Gall, I. Bárbara and R. Barreiro. 2014. A multilocus species delimitation reveals a striking number of species of coralline algae forming maerl in the OSPAR maritime area. PLoS One 9: e104073. doi:10.1371/journal.pone.0104073.10.1371/journal.pone.0104073Search in Google Scholar PubMed PubMed Central

Peña, V., J.J. Hernández-Kantún, J. Grall, C. Pardo, L. Lopez, I. Barbara, L. Le Gall and R. Barreiro. 2014. Detection of gametophytes in the maerl-forming species Phymatolithon calcareum (Melobesioideae, Corallinales) assessed by DNA barcoding. Cryptogamie Algol. 35: 15–25.10.7872/crya.v35.iss1.2014.15Search in Google Scholar

Peña, V., O. De Clerck, J. Afonso-Carrillo, E. Ballesteros, I. Barbara, R. Barreiro and L. Le Gall. 2015a. An integrative systematic approach to species diversity and distribution in the genus Mesophyllum (Corallinales, Rhodophyta) in Atlantic and Mediterranean Europe. Eur. J. Phycol. 50: 20–36.10.1080/09670262.2014.981294Search in Google Scholar

Peña, V., C. Pardo, L. Lopez, B. Carro, J. Hernández-Kantún, W.H. Adey, I. Barbara, R. Barreiro and L. Le Gall. 2015b. Phymatolithon lusitanicum sp. nov. (Hapalidiales, Rhodophyta): the third most abundant maerl-forming species in the Atlantic Iberian peninsula. Cryptogamie Algol. 36: 429–459.10.7872/crya/v36.iss4.2015.429Search in Google Scholar

Presting, G.G. 2006. Identification of conserved regions in the plastid genome: implications for DNA barcoding and biological function. Can. J. Bot. 84: 1434–1443.10.1139/b06-117Search in Google Scholar

Puillandre, N., A. Lambert, S. Brouillet and G. Achaz. 2012. ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Mol. Ecol. 21: 1864–1877.10.1111/j.1365-294X.2011.05239.xSearch in Google Scholar PubMed

Reid, N.M. and B.C. Carstens. 2012. Phylogenetic estimation error can decrease the accuracy of species delimitation: a Bayesian implementation of the general mixed Yule-coalescent model. Evol. Biol. 12: 196.10.1186/1471-2148-12-196Search in Google Scholar PubMed PubMed Central

Richards, J.L., P.W. Gabrielson and S. Fredericq. 2014. New insights into the genus Lithophyllum (Lithophylloideae, Corallinaceae, Corallinales) from deepwater rhodolith beds offshore the NW Gulf of Mexico. Phytotaxa 190: 162–175.10.11646/phytotaxa.190.1.11Search in Google Scholar

Riosmena-Rodríguez, R., W.J. Woelkerling and M.S. Foster. 1999. Taxonomic reassessment of rhodolith-forming species of Lithophyllum (Corallinales, Rhodophyta) in the Gulf of California, Mexico. Phycologia 38: 401–417.10.2216/i0031-8884-38-5-401.1Search in Google Scholar

Robba, L., S.J. Russell, G.L. Barker and J. Brodie. 2006. Assessing the use of the mitochondrial cox1 marker for use in DNA Barcoding of red algae (Rhodophyta). Am. J. Bot. 93: 1101–1108.10.3732/ajb.93.8.1101Search in Google Scholar PubMed

Rösler, A., F. Perfectti, V. Peña and J.C. Braga. 2016. Phylogenetic relationships of corallinaceae (Corallinales, Rhodophyta): taxonomic implications for reef-building corallines. J. Phycol. 52: 412–431.10.1111/jpy.12404Search in Google Scholar PubMed

Sanger, F., S. Nicklen and A.R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. P. Natl. Acad. Sci. USA 74: 5463–5467.10.1073/pnas.74.12.5463Search in Google Scholar PubMed PubMed Central

Sauer, J. and B. Hausdorf. 2012. A comparison of DNA-based methods for delimiting species in a Cretan land snail radiation reveals shortcomings of exclusively molecular taxonomy. Cladistics 28: 300–316.10.1111/j.1096-0031.2011.00382.xSearch in Google Scholar PubMed

Saunders, G.W. 2005. Applying DNA barcoding to red macroalgae: a preliminar y appraisal holds promise for future applications. Philos. T. Roy. Soc. B 360: 1879–1888.10.1098/rstb.2005.1719Search in Google Scholar PubMed PubMed Central

Saunders, G.W. 2008. A DNA barcode examination of the red algal family Dumontiaceae in Canadian waters reveals substantial cryptic species diversity. 1. The foliose Dilsea-Neodilsea complex and Weeksia. Botany 86: 773–789.10.1139/B08-001Search in Google Scholar

Saunders, G.W. and B. McDonald. 2010. DNA barcoding reveals multiple overlooked Australian species of the red algal order Rhodymeniales (Florideophyceae), with resurrection of Halopeltis J. Agardh and description of Pseudohalopeltis gen. nov. Botany 88: 639–667.10.1139/B10-038Search in Google Scholar

Saunders, G.W. and T.E. Moore. 2013. Refinements for the amplification and sequencing of red algal DNA barcode and RedToL phylogenetic markers: a summary of current primers, profiles and strategies. Algae 28: 31–43.10.4490/algae.2013.28.1.031Search in Google Scholar

Seo, K.S., T.O. Cho, J.S. Park, E.C. Yang, H.S. Yoon and S.M. Boo. 2003. Morphology, basiphyte range, and plastid DNA phylogeny of Campylaephora borealis stat. nov. (Ceramiaceae, Rhodophyta). Taxon 52: 9–19.10.2307/3647298Search in Google Scholar

Setchell, W.A. 1943. Mastophora and the Mastophoreae: genus and subfamily of Corallinaceae. P. Natl. Acad. Sci. USA 29: 127–135.10.1073/pnas.29.5.127Search in Google Scholar PubMed PubMed Central

Sherwood, A.R. and G.G. Presting. 2007. Universal primers amplify a 23S rDNA plastid marker in Eukaryotic algae and cyanobacteria. J. Phycol. 43: 605–608.10.1111/j.1529-8817.2007.00341.xSearch in Google Scholar

Sherwood, A.R., A. Kurihara, K.Y. Conklin, T. Sauvage and G.G. Presting 2010a. The Hawaiian Rhodophyta Biodiversity Survey (2006–2010): a summary of principal findings. BMC Plant Biol. 10: 258.10.1186/1471-2229-10-258Search in Google Scholar PubMed PubMed Central

Sherwood, A.R., T. Sauvage, A. Kurihara, K.Y. Conklin and G.G. Presting 2010b. A comparative analysis of COI, LSU and UPA marker data for the Hawaiian florideophyte Rhodophyta: implications for DNA barcoding of red algae. Cryptogamie Algol. 31: 451–465.Search in Google Scholar

Sissini, M.N., M.C. Oliveira, P.W. Gabrielson, N.R. Robinson, Y.B. Okolodkov, R. Riosmena-Rodríguez and P.A. Horta. 2014. Mesophyllum erubescens (Corallinales, Rhodophyta) – so many species in one epithet. Phytotaxa 190: 299–319.10.11646/phytotaxa.190.1.18Search in Google Scholar

Spalding, M.D., H.E. Fox, G.R. Allen, N. Davidson, Z.A. Ferdaña, M. Finlayson, B.S. Halpern, M.A. Jorge, A. Lombana, S.A. Lourie, K.D. Martin, E. McManus, J. Molnar, C.A. Recchia and J. Robertson. 2007. Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57: 573–583.10.1641/B570707Search in Google Scholar

Torrano-Silva, B.N., R. Riosmena-Rodrígues and M.C. Oliveira. 2014. Systematic position of Paulsilvella in the Lithophylloideae (Corallinaceae, Rhodophyta) confirmed by molecular data. Phytotaxa 190: 94–111.10.11646/phytotaxa.190.1.8Search in Google Scholar

Verbruggen, H., M.J.L. Brookes and J.F. Costa. 2017. DNA barcodes and morphometric data indicate that Codium fragile may consist of two species (Bryopsidales, Chlorophyta). Phycologia 56: 54–62.10.2216/16-54.1Search in Google Scholar

Vieira-Pinto, T., M.C. Oliveira, J. Bouzon, M. Sissini, J.L. Richards, R. Riosmena-Rodríguez and P.A. Horta. 2014. Lithophyllum species from Brazilian coast: range extension of Lithophyllum margaritae and description of Lithophyllum atlanticum sp. nov. (Corallinales, Corallinophycidae, Rhodophyta). Phytotaxa 190: 355–369.10.11646/phytotaxa.190.1.21Search in Google Scholar

Villas-Boas, A.B., R. Riosmena-Rodriguez, G.M. Amado-Filho, G. Maneveldt and M.A. Figueiredo. 2009. Rhodolith-forming species of Lithophyllum (Corallinales; Rhodophyta) from Espírito Santo state, Brazil, including the description of L. depressum sp. nov. Phycologia 48: 237–248.10.2216/08-35.1Search in Google Scholar

Walker, R.H., J. Brodie, S. Russel and L.M. Irvine. 2009. Biodiversity of coralline algae in the Northeastern Atlantic including Corallina caespitosa sp. nov. (Corallinoideae, Rhodophyta). J. Phycol. 45: 287–297.10.1111/j.1529-8817.2008.00637.xSearch in Google Scholar PubMed

Woelkerling, W.J. 1988. The coralline red algae: an analysis of the genera and subfamilies of nongeniculate Corallinaceae. British Museum (Natural History) and Oxford University Press, London. pp. i–xi + 268.Search in Google Scholar

Woelkerling, W.J. and S.J. Campbell. 1992. An account of southern Australian species of Lithophyllum (Corallinaceae, Rhodophyta). Bull. Br. Mus. Nat. Hist. Bot 22: 1–107.Search in Google Scholar

Woelkerling, W.J., L.M. Irvine and A. Harvey. 1993. Growth-forms in non-geniculate coralline red algae (Corallinales, Rhodophyta). Aust. Syst. Bot. 6: 277–293.10.1071/SB9930277Search in Google Scholar

Woelkerling, W.M.J., G. Sartoni and S. Bod. 2002. Paulsilvella huveorum gen. & sp. nov. (Corallinaceae, Rhodophyta) from the Holocene of Somalia and Kenya, with a reassessment of Lithothrix antiqua from the Late Pleistocene of Mauritius. Phycologia 41: 358–373.10.2216/i0031-8884-41-4-358.1Search in Google Scholar

Yang, E.C. and S.M. Boo. 2004. Evidence for two independent lineages of Griffithsia (Ceramiaceae, Rhodophyta) based on plastid protein-coding psaA, psbA, and rbcL gene sequences. Mol. Phylogenet. Evol. 31: 680–688.10.1016/j.ympev.2003.08.014Search in Google Scholar PubMed

Yoon, H.S., J.D. Hackett and D. Bhattacharya. 2002. A single origin of the peridinin and fucoxanthin containing plastids in dinoflagellates through tertiary endossymbiosis. Proc. Nat. Acad. Sci. Unit. St. Am. 99: 11724–11729.10.1073/pnas.172234799Search in Google Scholar PubMed PubMed Central

Zhang, J., P. Kapli, P. Pavlidis and A. Stamatakis. 2013. A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29: 2869–2876.10.1093/bioinformatics/btt499Search in Google Scholar PubMed PubMed Central


Supplemental Material:

The online version of this article offers supplementary material (https://doi.org/10.1515/bot-2017-0040).



Article note:

We dedicate this paper to our friend and admired colleague, Dr. Rafael Riosmena-Rodríguez, and his family. He has inspired us all. Rafael Riosmena-Rodríguez passed away in March 2016.


Received: 2017-4-26
Accepted: 2018-2-15
Published Online: 2018-3-16
Published in Print: 2018-3-28

©2018 Walter de Gruyter GmbH, Berlin/Boston

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