Advanced
A new species of Bangiopsis: B. franklynottii sp. nov. (Stylonematophyceae, Rhodophyta) from Australia and India and comments on the genus
A new species of Bangiopsis: B. franklynottii sp. nov. (Stylonematophyceae, Rhodophyta) from Australia and India and comments on the genus
ALGAE. 2014. Jun, 29(2): 101-109
Copyright © 2014, The Korean Society of Phycology
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
  • Received : January 01, 2014
  • Accepted : May 05, 2014
  • Published : June 15, 2014
Download
PDF
e-PUB
PubReader
PPT
Export by style
Share
Article
Author
Metrics
Cited by
TagCloud
About the Authors
John A. West
School of Botany, University of Melbourne, Parkville, VIC 3010, Australia
jwest@unimelb.edu.au
Susan Loiseaux de Goer
11 Rue des Moguerou, 29680 Roscoff, France
Giuseppe C. Zuccarello
School of Biological Sciences, Victoria University of Wellington, PO Box 600, Wellington 6140, New Zealand
Abstract
Small red algae, especially those previously referred to as ‘primitive’ are often overlooked, but can be quite abundant. These ‘primitive’ red algae are now placed in several classes distinct from the Florideophyceae, for example the Stylonematophyceae. A brownish-red filamentous alga was collected from a sandy tide pool at Cape Tribulation, Queensland, Australia. Cultured specimens were identified as Bangiopsis and conformed to the morphological characters of the genus (multicellular base, erect filaments branched or unbranched, uniseriate to multiseriate-tubular, single multilobed purple-red to red-brown plastid with central pyrenoid, vegetative cells released directly as spores). Molecular data of two plastid genes ( rbc L, psb A) support placement of the Australian isolate and isolates from India in Bangiopsis . The genetic variation between these isolates and isolates from Puerto Rico previously attributed to B. subsimplex indicates that these should be considered as a separate species. As the type locality is in the Atlantic Ocean, French Guiana, and not far from Puerto Rico, and the Puerto Rican isolate has been used often in phylogenetic analyses, we propose that the Indian and Pacific Ocean isolates be designated a new species, B. franklynottii , to acknowledge Ott’s many years of research on inconspicuous freshwater and marine red algae. Our research also highlights the lack of careful descriptions in many of the records of this genus and the lack of morphological characters to distinguish species. Especially within the morphologically simple red algae, morphological distinctness does not necessarily reflect evolutionary divergences.
Keywords
INTRODUCTION
Many red algal morphospecies comprise a grouping of several genetic entities, which are usually referred to as cryptic species ( Le Gall and Saunders 2010 ). Our ability to distinguish these genetic entities using traditional morphological diagnoses, while commendable, may not be achievable ( Verbruggen 2014 ). This is especially true for the more simply constructed red algae (e.g., Zuccarello et al. 2011 ).
The ubiquity and taxonomy of the ‘simple’ red algae once considered in the class Bangiophyceae is slowly being resolved (e.g., Zuccarello et al. 2008 , 2010 , 2011 , Necchi et al. 2013 ). The old Bangiophyceae is now subdivided into six separate classes ( Yoon et al. 2006 ), one of which is the Stylonematophyceae. The Stylonematophyceae is comprised of 14 microscopic genera that are mostly marine but two are freshwater and one is terrestrial ( Zuccarello et al. 2008 ). Most of the genera are filamentous and two are unicellular ( Rhodosorus and Rhodospora ). Stylonema alsidii is probably the most ubiquitous species in the class ( Zuccarello et al. 2008 ). New genera ( Purpureofilum and Rhodaphanes ) have also been described from recent collections ( West et al. 2005 , 2007 ).
Bangiopsis is a branched filamentous genus up to 1 cm long. The genus has a complicated taxonomic and nomenclatural history ( Krishnamurthy 1957 , Silva et al. 1996 , Guiry and Guiry 2014 ). Bangiopsis subsimplex (Montagne) F. Schmitz is the type species originally described by Montagne (1850) as Compsopogon subsimplex Montagne based on specimens collected by Leprieur in Cayenne, French Guiana. It was transferred to Bangiopsis by Schmitz (1896) . Borgesen (1916) reported a similar specimen from Christianssted, St. Croix, Danish West Indies that he designated as B. subsimplex , however, Collins and Hervey (1917) thought it to be more like Goniotrichum humphreyi Collins found growing on wood in St. Annes Bay, Jamaica ( Collins 1901 ). Hamel (1929) transferred that to Bangiopsis humphreyi (Collins) G. Hamel but this is now treated as a synonym of Bangiopsis dumontioides (P. L. Crouan & H. M. Crouan) V. Krishnamurthy ( Krishnamurthy 1957 ). Bangiopsis subsimplex was also collected in Puerto Rico at Guajataca Beach by Rintoul and Sherwood in 1997 providing the first specimens of the genus used for molecular analysis ( Muller et al. 2001 ). In 2005 it was also collected by David Ballantine from the same site, cultured by Franklyn Ott and placed in the UTEX The Culture Collection of Algae as LB 2854.
Joly (1965) recorded B. subsimplex in São Paulo, Brazil. This species was also reported by Almeida et al. (2013) using cultured samples from Baía la de Todos os Santos, Bahia, Brazil comparing it with several similar genera of the Stylonematales. Brasileiro et al. (2009) listed, without explanation, B. dumontioides from Cabo Frio, Brazil.
Krishnamurthy (1957) obtained B. subsimplex samples from Mangalore, Karnataka and near Chennai, Tamil Nadu, India. Umamaheswara Rao and Sreeramulu (1970) found B. subsimplex at Visakhapatnam, Andra Pradesh, India. Although this has not been further verified, Krishnamurthy (1957) stated that a Natural History Museum (London) specimen of Bangia fergusoni Grunow from Sri Lanka is identical to B. subsimplex . Moazzam and Shameel (1985) observed B. subsimplex on Petalonia sp. in Pakistan. Tanaka (1952) recorded B. subsimplex growing on rocks and Sargassum sp. near Satoura, Japan. Kapraun and Bowden (1978) recorded B. humphreyi in Fiji but South and Skelton (2003) referred to it as B. subsimplex .
The basic problem with species and generic identification in the Stylonematophyceae is that they are not easily discernible from nomenclatural descriptions, and without molecular data are even more uncertain. Taxonomic progress requires careful field collections, culture and molecular observations. Even though Bangiopsis records are widespread it is difficult to infer the morphological variation from previous reports. Many of the description lack key anatomical details and this makes identification of species and understanding species distribution impossible.
We collected an isolate of Bangiopsis in Australia. Molecular analysis of this isolate compared to available isolates from other parts of the world indicate that it belongs to a new species.
MATERIALS AND METHODS
Pale brown / red microscopic filamentous specimens were collected by Richard Wetherbee in a shallow sandy tidal pool on Jul 6, 2013 just north of Noah Beach car park (ca. 16˚07.896′ S, 145˚27.302′ E), Cape Tribulation, Queensland, Australia. Initially sand samples were placed in culture flasks with seawater from the site and held at about 20 ± 2℃ on a rotary shaker at approximately 25 rpm and 30 ℃mol photons m -2 s -1 cool white LED lighting at 10 : 14 LD daily cycle. Multiseriate filaments were checked for epiphytes and isolated by excising short segments about 1 mm long. These were placed in 50 × 70 mm culture dishes with 1/4 strength Modified Provasoli’s Medium (20 mL enrichment per litre sterile seawater) to supress epiphyte growth. GeO 2 and sodium penicillin G were added to inhibit diatoms and cyanobacteria, respectively ( West 2005 ). For slower growth light was reduced to about 6-7 µmol photons m -2 s -1 . Other conditions were maintained as stated above. The culture was designated as JAW 4835.
Molecular analyses were done on the Australian specimen and two other isolates: UTEX LB 2854 from Guajataca, Puerto Rico (Ott MO 7041) and Ott MO 7045 (isolated Nov 27, 2004 from specimens forming distinct bands on rocks from Fisherman’s Cove, Chennai, India and obtained by V. Krishnamurthy, JAW 4567).
Total DNA was isolated from silica gel-dried cultured material using a modified CTAB procedure ( Zuccarello and Lokhorst 2005 ). Amplification and sequencing of the plastid-encoded large subunit of the ribulose bisphosphate carboxylase / oxygenase gene ( rbc L) used amplification primers presented in Freshwater and Rueness (1994) . The psb A (photosystem II reaction center protein D1) gene was amplified using the primers described in Yoon et al. (2002) . Amplified products were checked for correct length, purity and yield on 1% agarose gels. Polymerase chain reaction products were cleaned using ExoSAP-IT (USB, Cleveland, OH, USA) and commercially sequenced (Macrogen Inc., Daejeon, Korea). A selection of members of the Stylonematophyceae and Compsopogonophyceae were used from previous publications ( Zuccarello et al. 2008 , 2011 ). Outgroups used in all analyses were Porphyridium aerugineum Geitler and Flintiella sanguinaria Ott, members of the Porphyridiophyceae and Compsopogon caeruleus (Balbis ex C. Agardh) Montagne of the Compsopogonophyceae.
Sequences were edited, assembled and aligned using the Geneious software package (Biomatters, available from http://www.geneious.com/). Alignment was straight forward as no gaps were found in the data set and the two genes were combined. The program Modeltest version 3.7 ( Posada and Crandall 1998 ) was used to find the model of sequence evolution that best fit the data set by an Akaike Information Criterion (AIC) ( Posada and Crandall 2001 ). Maximum likelihood (ML) was performed with RAxML 7.2.8 ( Stamatakis 2006 ). RAxML was performed with all threes codons partitioned and the GTR + gamma model and 500 non-parametric bootstrap replicates ( Felsenstein 1985 ).
Bayesian inference was performed with MrBayes v3.1.2 ( Ronquist and Huelsenbeck 2003 ). Analyses consisted of two independent simultaneous runs of one cold and three incrementally heated chains, and 3 × 10 6 generations with sampling every 1,000 generations. Codons were partitioned. The log files of the runs were checked with Tracer v1.5 ( Rambaut and Drummond 2007 ) and a burn-in sample of 100 trees was removed from each run before calculating the majority rule consensus tree.
RESULTS
A field specimen grown in culture showed a uniseriate filament branching and forming multiseriate upper sectors that became tubular with a single peripheral layer of cells ( Fig. 1A & C ). Thalli were up to 1.5 cm long and red coloured ( Fig. 1A ). Cell divisions in the uniseriate section were initially transverse and then longitudinal to irregular in orientation forming biseriate and multiseriate sectors ( Fig. 1B ). Older tubular branches were composed of a single peripheral layer of cells containing multicellular packets of a polyhedral appearance with a thick colorless matrix ( Fig. 1C ) and some of these vegetative cells were released directly as spores ( Fig. 1B ). Each cell had a single nucleus laterally displaced by a single multilobed plastid with a large central pyrenoid ( Fig. 1C ). In this Bangiopsis culture small dark brown deposits (10-15 ℃m in diameter) with a lighter brown central area were common ( Fig. 1C , arrowheads). These were similar to brown deposits that were composed of manganese and other elements, as observed previously in cultures of other algae ( West et al. 2013 ).
PPT Slide
Lager Image
Bangiopsis franklynottii 4835. (A) Thallus from field sample with epiphytic diatoms. Thallus basal attachment is not present. Initially the thallus was uniseriate with sparse branching, then becoming multiseriate and tubular. (B) Lower portion of same thallus seen in (A) showing the transverse and longitudinal cell divisions. Spores discharged from cells along the axis (arrows). (C) Tubular portion of thallus with cell divisions in various planes within each aggregate, outline of polysaccharide matrix for each aggregate is clearly visible and empty spaces are where spores were discharged. Single plastid with multiple radiating lobes and a central pyrenoid evident in cells. Brown bodies (arrowheads) are probable manganese deposits. (D) Spore germination and cell division series form diads, tetrads, other larger multicellular structures of the sporeling basal system growing in low light before erect filaments are produced. In low light occasional basal aggregates developed erect shoots (two arrowheads) or a single cell spore produced a uniseriate erect filament (single arrowhead). (E) In brighter light the basal aggregates developed erect filaments more extensively. Scale bars represent: A, 100 μm; B, 50 μm; C & D, 10 μm; E, 20 μm.
The spherical spores were 9-10 ℃m in diameter and displayed slow rotation combined with gliding movement before settling on a substrate. No amoeboid movement was seen. Germination was initiated by a series of cell divisions, with second divisions usually at right angles to the first divisions and then dividing in various planes to form a multicellular aggregate enclosed in a thin matrix ( Fig. 1D ). Erect shoots normally developed from aggregates of 12 or more cells ( Fig. 1D , two arrowheads) but sometimes an erect filament formed directly from an undivided spore ( Fig. 1D , single arrowhead). In low light (6-7 ℃mol photons m -2 s -1 ) the basal system was extensive and erect filaments formed late ( Fig. 1D ). In brighter light (20-22 ℃mol photons m -2 s -1 ) erect branching from the basal system was enhanced ( Fig. 1E ).
Isolate MO1560 (JAW 4283) was analysed for low molecular weight carbohydrates (sorbitol 1,102 mmol kg -1 DW and digeneaside 20 mmol kg -1 DW, floridoside was not detected). Isolate MO70450 (JAW 4509) had sorbitol 485 mmol kg -1 DW, digeneaside 14 mmol kg -1 DW and floridoside 2 mmol kg -1 DW (Ulf Karsten, personal communication).
The topologies of the two gene trees are similar to previous phylogenies of the class Stylonematophyceae, and also similar between the ML and Bayesian analysis. The class Porphyridiophyceae and order Erythropeltidales are both well supported, and Rufusia pilicola is sister to the remaining Stylonematophyceae. The two different plastid gene phylogenies clearly show the Australian isolate groups with Bangiopsis isolates from India ( Figs 2 & 3 ) and are separate from the Puerto Rico samples. The genus Bangiopsis while not supported within these datasets appears to be closely related to Purpureofilum apyrenoidigerum . The well supported differences between the isolates from the Indian and Pacific Oceans versus the samples from the Atlantic Ocean warrant the description of a new species for the non-Atlantic isolates.
PPT Slide
Lager Image
Maximum-likelihood (ML) topology (-log Ln = -9142.548) of rbcL gene data of select Stylonematophyceae, Porphyridiophyceae and Compsopogonophyceae. Composopogon caeruleus was used as an outgroup. * ≥95% ML bootstrap values and ≥0.95 Bayesian posterior probabilities. Other values associated with branches = RaxML bootstrap percentage/Bayesian posterior probabilities. Abbreviations following the species names and culture numbers: MDG, Madagascar; AUS, Australia; IND, India; CRI, Costa Rica; PHI, Philippines; JPN, Japan; VAN, Vanuatu; NCL, New Caledonia; FRA, France; USA, United States; PRI, Puerto Rico. Scale bar represents substitutions/site.
PPT Slide
Lager Image
Maximum-likelihood (ML) topology (-log Ln = -4505.523) of psbA gene data of select Stylonematophyceae. Composopogon caeruleus was used as an outgroup. * ≥95% ML bootstrap values and ≥0.95 Bayesian posterior probabilities. Other values associated with branches = RaxML bootstrap percentage / Bayesian posterior probabilities. Abbreviations following the species names and culture numbers: MDG, Madagascar; IND, India; AUS, Australia; CRI, Costa Rica; JPN, Japan; FRA, France; USA, United States; NCL, New Caledonia; VAN, Vanuatu; PHI, Philippines; PRI, Puerto Rico. Scale bar represents substitutions/site.
Pairwise differences between the two species also support this species distinction. Inter-species pairwise differences are over six times greater than the intra-species variation. For rbc L, intra-species variation is between 0.0-1.2%, while inter-species variation is 8.07-8.28%. For psb A intra-species variation is between 0.0-0.26% and interspecies variation 3.06%.
- Bangiopsis franklynottiisp. nov. J. A. West, de Goër et Zuccarello
Description. Cells with single nucleus and a single central multilobed plastid containing a central pyrenoid. Basal attachment of thallus by a small multicellular disc giving rise to uniseriate and then multiseriate erect shoots by intercalary cell divisions. Mature thallus often becoming a hollow cylinder with a clear thick mucilaginous matrix in which cells are solitary or in packets. Monospores are discharged directly from vegetative cells along the axis.
Culture 4835 (CCMP 3416) was deposited in the National Center for Marine Algae and Microbiota (NCMA, https://ncma.bigelow.org/), 60 Bigelow Drive, PO Box 380, East Boothbay, Maine 04544, USA. A herbarium specimen was deposited at the National Herbarium of Victoria, Royal Botanic Gardens, Birdwood Ave, South Yarra VIC 3141, Australia (MEL 2371924). Genbank accession Nos: rbc L, KJ778645; psb A, KJ778647.
DISCUSSION
Our data clearly show that the isolates from Australia and the isolates from India are different from the Atlantic Ocean isolates from Puerto Rico. These genetic analyses clearly show that these isolates are distinct and probably have a common ancestor a long time ago. Based on rbc L mutation rate calibration from the red alga Caloglossa ( Kamiya et al. 2004 ) the time to the most recent common ancestor for these two Bangiopsis species was approximately 69 (75-65) million years ago. Although this calibration from the Ceramiales must be taken with great caution, a great deal of time has passed since these species shared a common ancestor. As the type locality is Cayenne, French Guiana ( Montagne 1850 ) in the Atlantic Ocean and these isolates are clearly distinct, we recognize the Indian and Australian isolates as a new species, B. franklynottii . This new species is not morphologically different from description of Bangiopsis subsimplex in the literature. There are probably several reasons for this. The first is that many descriptions of these small red algae are cursory and lack detail and certainly lack details that could only be revealed in culture ( Table 1 ). Most of the characters overlap, for example cell dimensions, or are based on few specimens in which phenotypic plasticity was not investigated. Secondly, it is likely that morphology has not changed in this time. This lack of morphological characters to distinguish species, genera and even orders is becoming increasingly apparent with the influx of molecular data ( West et al. 2008 , Sutherland et al. 2011 ). It could be that many species can only be identified by using molecular data ( Verbruggen 2014 ). Therefore our ability to link historical names, and old specimens that are not easily usable, to present collections is limited ( De Clerck et al. 2012 ). Krishnamurthy (1957) provided a complete morphological investigation of field and herbarium material of Bangiopsis including comparisons of the type specimens of B. subsimplex and B. dumontioides (P. L. Crouan & H. M. Crouan) V. Krishnmurthy. He based species distinctness on the cells being slightly larger in B. dumontioides and the cells more widely spaced in B. dumontioides and also the more amount of branching. We do not believe that these characters would be stable to clearly identify these species from the field. Unfortunately no molecular data is available for B. dumontioides . The only non-molecular criteria at the moment to identify these two species is their location in different ocean basins.
Comparison of morphological and anatomical features ofBangiopsisfrom the literature and this study
PPT Slide
Lager Image
NI, no information.
West et al. (2005) compared Bangiopsis (now B. franklynottii ) from Visakhapatnam, Andra Pradesh, India with Purpureofilum apyrenoidigerum J. A. West, Zuccarello et J. L. Scott from Australia. These two genera seems to be sister species in our phylogenetic analyses. Both genera contain digeneaside and sorbitol as do most genera of the Stylonematophyceae ( Karsten et al. 1999 , 2003 , Zuccarello et al. 2008 , Yoon et al. 2010 ). Purpureofilum apyrenoidigerum chloroplasts lack a pyrenoid whereas those of Bangiopsis have a well-defined central pyrenoid. The ecophysiology of the Indian isolate of B. franklynottii (as B. subsimplex ) revealed a wide environmental tolerance characteristic of algae growing in the upper intertidal ( Eggert et al. 2007 ).
Spore formation and germination are very similar in cultured specimens from Australia and India although the mature thalli in the Australian isolate are clearly tubular with a peripheral single-celled layer. The tubular thalli were not evident in the culture of the Indian isolate ( West et al. 2005 ) but Krishnamurthy (1957) observed tubular thalli in field specimens from India.
Bangiopsis subsimplex from the Visakhapatnam coast in India exhibited a diurnal monospore discharge rhythm peaking between 1,300-1,400 h daily and also had maximum discharge at 40 psu salinity (range, 10 to 70) and 50 ℃mol photons m -2 s -1 lighting (range, 0 to 97) ( Narasimha Rao and Rangaiah 1991 ).
As with many of these small red algae their distribution and diversity has been poorly explored. Careful culture observations are needed, along with molecular analysis to confirm species identity (e.g., Zuccarello et al. 2010 ). Critical evidence on the geographic distribution and genetic variation of Bangiopsis requires more research using these techniques.
Acknowledgements
We thank Maren Preuss for technical assistance. This work was partially supported by the School of Botany Foundation, University of Melbourne. Nair Yokoya kindly sent us the pertinent pages onBangiopsis humphreyifromJoly (1965). We are grateful to Tim Entwisle for depositing a voucher specimen in the Royal Botanical Garden, Melbourne and to Julie Sexton for accepting a unialgal culture at the National Center for Marine Algae and Microbiota, East Boothbay, Maine, USA.
References
Almeida W. R. , Guimaraes S. M. P. B. , Moura C. W. N. 2013 Bangiopsis subsimplex (Mont.) F. Schmitz (Stylonematales, Rhodophyta) on the northeastern coast of Brazil Acta Bot. Bras. http://dx.doi.org/10.1590/S0102-33062013000100022 27 231 - 236
Børgesen F. 1920 The marine algae of the Danish West Indies. Vol. 2. Rhodophyceae Dansk. Bot. Ark. 3 1 - 412
Brasileiro P. S. , Yonieshigue-Valentin Y. , Bahia R. G. , Reis R. P. , Amado Filho G. M 2009 Algas marinhas bentonicas da regiao de Cabo Frio e arredores: Sintese do conhecimento Rodriquesia 60 39 - 66
Collins F. S. 1901 The algae of Jamaica Proc. Am. Acad. Arts Sci. http://dx.doi.org/10.2307/20021659 37 231 - 270
Collins F. S. , Hervey A. B. 1917 The algae of Bermuda Proc. Am. Acad. Arts Sci. http://dx.doi.org/10.2307/20025740 53 3 - 195
De Clerck O. , Guiry M. D. , Leliaert F. , Samyn Y. , Verbruggen H. 2012 Algal taxonomy: a road to nowhere? J. Phycol. 49 215 - 225
Eggert A. , , Nitschke U. , West J. A. , Michalik D. , Karsten U. 2007 Acclimation of the intertidal red alga Bangiopsis subsimplex (Stylonematophyceae) to salinity changes J. Exp. Mar. Biol. Ecol. http://dx.doi.org/10.1016/j.jembe.2006.11.015 343 176 - 186
Felsenstein J. 1985 Confidence limits on phylogenies: an approach using the bootstrap Evolution http://dx.doi.org/10.2307/2408678 39 783 - 791
Freshwater D. W. , Rueness J. 1994 Phylogenetic relationships of some European Gelidium (Gelidiales, Rhodophyta) species, based on rbcL nucleotide sequence analysis Phycologia http://dx.doi.org/10.2216/i0031-8884-33-3-187.1 33 187 - 194
Guiry M. D. , Guiry G. M. 2014 AlgaeBase World-wide electronic publication, National University of Ireland Galway http://www.algaebase.org
Hamel G. 1929 Contributions à la flore algologique des Antilles Ann. Crypt. Exot. 2 53 - 58
Joly A. B. 1965 Flora marinha do litoral norte do estado de Saõ Paulo e regiões circunvizinhas Bol. Fac. Filos. Ciênc. Let. Univ. São Paulo Bot. 21 5 - 393
Kamiya M. , Zuccarello G. C. , West J. A. 2004 Phylogeography of Caloglossa leprieurii and related species (Delesseriaceae, Rhodophyta) based on the rbcL gene sequences Jpn. J. Phycol. 52 ((Suppl.)) 147 - 151
Kapraun D. F. , Bowden W. A. 1978 Additions to the benthic marine algal flora of Fiji Micronesica 14 199 - 207
Karsten U. , West J. A. , Zuccarello G. C. , Engbrodt R. , Yokoyama A. , Hara Y. , Brodie J. 2003 Low molecular weight carbohydrates of the Bangiophycidae (Rhodophyta) J. Phycol. http://dx.doi.org/10.1046/j.1529-8817.2003.02192.x 39 584 - 589
Karsten U. , West J. A. , Zuccarello G. C. , Nixdorf O. , Barrow K. D. , King R. J. 1999 Low molecular weight carbohydrate patterns in the Bangiophyceae (Rhodophyta) J. Phycol. http://dx.doi.org/10.1046/j.1529-8817.1999.3550967.x 35 967 - 976
Krishnamurthy V. 1957 The genus Bangiopsis Schmitz from South India Phytomorphology 7 102 - 112
Le Gall L. , Saunders G. W. 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. http://dx.doi.org/10.1111/j.1529-8817.2010.00807.x 46 374 - 389
Moazzam M. , Shameel M. 1985 Studies on Bangiophyceae (Rhodophyta) from the coast of Karachi Pak. J. Bot. 17 141 - 152
Montagne C. 1850 Cryptogamia guyanensis, seu plantarum cellularium in Guyana gallica: annis 1835-1849 a Cl. Leprieur collectarum enumeratio universalis Ann. Sci. Nat. Bot. Ser. 14 283 - 309
Müller K. M. , Oliveira M. C. , Sheath R. G. , Bhattacharya D. 2001 Ribosomal DNA phylogeny of the Bangiophycidae (Rhodophyta) and the origin of secondary plastids Am. J. Bot. http://dx.doi.org/10.2307/3558445 88 1390 - 1400
Narasimha Rao G. M. , Rangaiah G. S. 1991 Control of spore shedding from some marine algae of the Visakhapatnam coast, India Br. Phycol. J. http://dx.doi.org/10.1080/00071619100650321 26 353 - 360
Necchi O. , Fo A. S. G. , Salomaki E. D. , West J. A. , Aboal M. , Vis M. L. 2013 Global sampling reveals low genetic diversity within Compsopogon (Compsopogonales, Rhodophyta) Eur. J. Phycol. http://dx.doi.org/10.1080/09670262.2013.783626 48 152 - 162
Ott F. D. 2009 Handbook of the taxonomic names associated with the non-marine Rhodophycophyta J. Cramer, Stuttgart 969 -
Posada D. , Crandall K. A. 1998 MODELTEST: testing the model of DNA substitution Bioinformatics http://dx.doi.org/10.1093/bioinformatics/14.9.817 14 817 - 818
Posada D. , Crandall K. A. 2001 Selecting the best-fit model of nucleotide substitution Syst. Biol. http://dx.doi.org/10.1080/106351501750435121 50 580 - 601
Rambaut A. , Drummond A. J. 2007 Tracer http://beast.bio.ed.ac.uk/Tracer
Ronquist F. , Huelsenbeck J. P. 2003 MrBayes 3: Bayesian phylogenetic inference under mixed models Bioinformatics http://dx.doi.org/10.1093/bioinformatics/btg180 19 1572 - 1574
Schmitz F. 1896 Bangiaceae. In Engler, A. & Prantl, K. (Eds.) Die naturlichen Pflanzenfamilien nebst ihren Gattungen und wichtigeren Arten insbesondere den Nutzpflanzen unter Mitwirkung zahlreicher hervorragender Fachgelehrten, Teil 1, Abt. 2 Wilhelm Engelmann Leipzig 307 - 316
Silva P. C. , Basson P. W. , Moe R. L. 1996 Catalogue of the benthic marine algae of the Indian Ocean Univ. Calif. Publ. Bot. 79 1 - 1259
South G. R. , Skelton P. A. 2003 Catalogue of the marine benthic macroalgae of the Fiji Islands South Pacific. Aust. Syst. Bot. http://dx.doi.org/10.1071/SB03011 16 699 - 758
Stamatakis A. 2006 RAxML-VI-HPC: maximum likelihoodbased phylogenetic analyses with thousands of taxa and mixed models Bioinformatics http://dx.doi.org/10.1093/bioinformatics/btl446 22 2688 - 2690
Sutherland J. E. , Lindstrom S. C. , Nelson W. A. , Brodie J. , Lynch M. D. J. , Hwang M. S. , Choi H. -G. , Miyata M. , Kikuchi N. , Oliveira M. C. , Farr T. , Neefus C. , Mols-Mortensen A. , Milstein D. , Muller K. M. 2011 A new look at an ancient order: generic revision of the Bangiales (Rhodophyta) J. Phycol. http://dx.doi.org/10.1111/j.1529-8817.2011.01052.x 47 1131 - 1151
Tanaka T. 1952 The systematic study of the Japanese Protoflorideae Mem. Fac. Fish. Kagoshima Univ. 2 1 - 92
Taylor W. R. 1960 Marine algae of the eastern tropical and subtropical coasts of the Americas University of Michigan Press Ann Arbor, MI 870 -
Umamaheswara Rao M. , Sreeramulu T. 1970 An annotated list of the marine algae of Visakhapatnam (India) Bot. J. Linn. Soc. http://dx.doi.org/10.1111/j.1095-8339.1970.tb02300.x 63 23 - 45
UTEX The Culture Collection of Algae http://web.biosci.utexas.edu/utex/default.aspx
Verbruggen H. 2014 Morphological complexity, plasticity and species diagnosability in the application of old species names in DNA-based taxonomies J. Phycol. http://dx.doi.org/10.1111/jpy.12155 50 26 - 31
West J. A. 2005 Long term macroalgal culture maintenance. In Andersen, R. A. (Ed.) Algal Culturing Techniques Academic Press New York 157 - 163
West J. A. , Kamiya M. , Loiseaux de Goer S. , Karsten U. , Zuccarello G. C. 2013 Observations on some mangrove-associated algae from the western Pacific (Guam, Chuuk, Kosrae, and Pohnpei) Algae http://dx.doi.org/10.4490/algae.2013.28.3.241 28 241 - 266
West J. A. , Scott J. L. , West K. A. , Karsten U. , Clayden S. L. , Saunders G. W. 2008 Rhodachlya madagascarensis gen. et sp. nov.: a distinct acrochaetioid represents a new order and family (Rhodachlyales ord. nov., Rhodachlyaceae fam. nov.) of the Florideophyceae (Rhodophyta) Phycologia http://dx.doi.org/10.2216/07-72.1 47 203 - 212
West J. A. , Zuccarello G. C. , Scott J. , Pickett-Heaps J. , Kim G. H. 2005 Observations on Purpureofilum apyrenoidigerum gen. et sp. nov. from Australia and Bangiopsis subsimplex from India (Stylonematales, Bangiophyceae, Rhodophyta) Phycol. Res. http://dx.doi.org/10.1111/j.1440-1835.2005.tb00357.x 53 49 - 66
West J. A. , Zuccarello G. C. , Scott J. L. , West K. A. , Karsten U. 2007 Rhodaphanes brevistipitata gen. et sp. nov. a new member of the Stylonematophyceae (Rhodophyta) Phycologia http://dx.doi.org/10.2216/07-03.1 46 440 - 449
Yoon H. S. , Hackett J. D. , Pinto G. , Bhattacharya D. 2002 The single, ancient origin of chromist plastids Proc. Natl. Acad. Sci. U. S. A. http://dx.doi.org/10.1073/pnas.242379899 99 15507 - 15512
Yoon H. S. , Müller K. M. , Sheath R. G. , Ott F. D. , Bhattacharya D. 2006 Defining the major lineages of red algae (Rhodophyta) J. Phycol. http://dx.doi.org/10.1111/j.1529-8817.2006.00210.x 42 482 - 492
Yoon H. S. , Zuccarello G. C. , Bhattacharya D. 2010 Evolutionary history and taxonomy of red algae. In Seckbach, J. & Chapman, D. J. (Eds.) Red Algae in the Genomic Age Springer Heidelberg 27 - 42
Zuccarello G. C. , Kikuchi N. , West J. A. 2010 Molecular phylogeny of the crustose members of the Erythropeltidales (Compsopogonophyceae, Rhodophyta): new genera Pseudoerythrocladia and Madagascaria and the evolution of the upright habit J. Phycol. http://dx.doi.org/10.1111/j.1529-8817.2010.00810.x 46 363 - 373
Zuccarello G. C. , Lokhorst G. M. 2005 Molecular phylogeny of the genus Tribonema (Xanthophyceae) using rbcL gene sequence data: monophyly of morphologically simple algal species Phycologia http://dx.doi.org/10.2216/0031-8884(2005)44[384:MPOTGT]2.0.CO;2 44 384 - 392
Zuccarello G. C. , West J. A. , Kikuchi N. 2008 Phylogenetic relationships in the Stylonematales (Stylonematophyceae, Rhodophyta): biogeographic patterns do not apply to Stylonema alsidii J. Phycol. http://dx.doi.org/10.1111/j.1529-8817.2008.00467.x 44 384 - 393
Zuccarello G. C. , Yoon H. S. , Kim H. J. , Sun L. , Loiseaux de Goer S. , West J. A. 2011 Molecular phylogeny of the upright Erythropeltidales (Compsopogonophyceae, Rhodophyta): multiple cryptic lineages of Erythrotrichia carnea J. Phycol. http://dx.doi.org/10.1111/j.1529-8817.2011.00985.x 47 627 - 637