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Branched Halymenia species (Halymeniaceae,

Rhodophyta) in the Indo-Pacific region, including
descriptions of Halymenia hawaiiana sp. nov. and H.
tondoana sp. nov.
a b c
Jazmn J. Hernndez-Kantn , Alison R. Sherwood , Rafael Riosmena-Rodriguez ,
d e
John M. Huisman & Olivier De Clerck
a
Irish Seaweed Research Group, University Road, Ryan Institute Annex Building, National
University of Ireland, Galway, Ireland
b
Botany Department, 3190 Maile Way, University of Hawaii, Honolulu, HI, 96822, USA
c
Programa de Investigacin en Botnica Marina, Departamento de Biologa Marina,
Universidad Autnoma de Baja California Sur, Carretera al sur, Km 5.5, Colonia el
Mezquitito, C. P. 23080, Mexico
d
School of Biological Sciences and Biotechnology, Murdoch University, Murdoch, WA
6150, and WA Herbarium, Department of Environment and Conservation, Locked Bag
104, Bentley Delivery Centre, WA 6983, Australia
e
Phycology Research Group and Centre for Molecular Phylogenetics and Evolution, Ghent
University, Krijgslaan 281, Building S8, 9000 Ghent, Belgium
Version of record first published: 29 Oct 2012.

To cite this article: Jazmn J. Hernndez-Kantn, Alison R. Sherwood, Rafael Riosmena-Rodriguez, John M. Huisman &
Olivier De Clerck (2012): Branched Halymenia species (Halymeniaceae, Rhodophyta) in the Indo-Pacific region, including
descriptions of Halymenia hawaiiana sp. nov. and H. tondoana sp. nov. , European Journal of Phycology, 47:4, 421-432

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 Eur. J. Phycol., (2012), 47(4): 421432

Branched Halymenia species (Halymeniaceae, Rhodophyta) in

the Indo-Pacific region, including descriptions of Halymenia
hawaiiana sp. nov. and H. tondoana sp. nov.

JAZMIN J. HERNANDEZ-KANTUN1, ALISON R. SHERWOOD2, RAFAEL RIOSMENA-RODRIGUEZ3,

JOHN M. HUISMAN4 AND OLIVIER DE CLERCK5

1
Irish Seaweed Research Group, University Road, Ryan Institute Annex Building, National University of Ireland, Galway, Ireland
2
Botany Department, 3190 Maile Way, University of Hawaii, Honolulu, HI, 96822, USA
Downloaded by [National University of Ireland - Galway] at 01:36 03 November 2012

3
Programa de Investigacion en Botanica Marina, Departamento de Biologa Marina, Universidad Autonoma de Baja California
Sur, Carretera al sur, Km 5.5, Colonia el Mezquitito, C. P. 23080, Mexico
4
School of Biological Sciences and Biotechnology, Murdoch University, Murdoch, WA 6150, and WA Herbarium, Department of
Environment and Conservation, Locked Bag 104, Bentley Delivery Centre, WA 6983, Australia
5
Phycology Research Group and Centre for Molecular Phylogenetics and Evolution, Ghent University, Krijgslaan 281, Building
S8, 9000 Ghent, Belgium

(Received 15 January 2012; revised 26 May 2012; accepted 7 June 2012)

Several species in the red algal genus Halymenia from the Indo-Pacific have been described with branched thalli, toothed
margins, spinose proliferations on the blade, and a firm gelatinous texture. Previous works have synonymized many of these
morphologically similar species with H. durvillei. Our increased taxon sampling and molecular data indicate that the taxonomy
of the Indo-Pacific Halymenia species is in need of revision, and that several aspects of taxonomies proposed by previous
authors now seem unlikely. Thus, the aim of the present work was to analyse species delimitation in branched Halymenia
species. Molecular and morphological data for specimens from the coral triangle and peripheral Indo-Pacific localities (East
African coast, Hawaii) were used to understand species delimitation for selected branched Halymenia spp. Phylogenetic
analyses based on 29 rbcL gene sequences grouped the specimens in four well-supported clusters at the species level with high
p-distances (2.75.3%). After the morphological analysis, five features were retained as diagnostic to identify the four species
studied. Our analyses led to the recognition and description of two new species, H. hawaiiana from the Hawaiian Islands
(previously erroneously called H. formosa) and H. tondoana from the Philippines. In addition, H. harveyana (currently treated
as a subspecies of H. floresii in Australia) is reassessed and recognized at the species level. Specimens with seven orders of
branching and a thick cortex (70150 mm) formed a monophyletic group, including sequences from previous work, with mostly
well-supported branches and with high p-distances at the species level. We propose to call this group the H. durvillei complex
until further reassessment is completed. None of the sequences studied here grouped with H. floresii from the Mediterranean,
suggesting that previous Indo-Pacific reports of the species were erroneous.

Key words: Australia, Halymenia, Halymenia durvillei, Halymenia floresii, Halymenia hawaiiana, Halymenia tondoana,
Hawaii, Indo-Pacific, Philippines, rbcL, red algae, Rhodophyta, taxonomy

Introduction species that were originally described with a repeat-

edly branched thallus, toothed margins, spinose
The foliose red algal genus Halymenia includes 63
proliferations on the surface of the blade, and a
accepted species and infraspecific names (Guiry &
firm gelatinous texture. Indian Ocean specimens
Guiry, 2011). Several of these are reported from
corresponding to these criteria have been identified
cold temperate areas but the highest diversity is
as H. ceylanica Harvey ex Kutzing, H. durvillei
found in warm temperate and tropical regions.
Bory de Saint-Vincent, H. floresii (Clemente) C.
For example, 41 names have been reported for
Agardh, H. formosa Harvey ex Kutzing, H. micro-
the Indo-Pacific (Guiry & Guiry, 2011). Silva
carpa (Montagne) P.C. Silva or H. venusta
et al. (1996) listed 22 names (including two varie-
Brgesen. In a study of the genus from the
ties) for the Indian Ocean, among which are several
Philippines, however, De Smedt et al. (2001)
Correspondence to: Jazmn J. Hernandez-Kantun. reduced H. ceylanica, H. durvillei var. denudata
E-mail: j.hernandez2@nuigalway.ie Weber-van Bosse, H. durvillei var. edentata
ISSN 0967-0262 print/ISSN 1469-4433 online/12/04000421432 2012 British Phycological Society
http://dx.doi.org/10.1080/09670262.2012.733734
 J. J. Hernandez-Kantun et al.
Weber-van Bosse, H. formosa, H. microcarpa and
H. venusta to synonyms of H. durvillei, based on
comparisons of type material and vegetative and
reproductive morphology. Their broad morpholog-
ical species concept resulted in any tropical Indo-
Pacific Halymenia specimen with a branched thallus
and a margin and surface with branchlets and/or
spines being referred to H. durvillei. The first
study addressing the diversity of Halymenia using
gene sequence data (rbcL; Kawaguchi et al., 2006)
confirmed the conclusions from De Smedt et al.
(2001). The analyses of Kawaguchi et al. (2006)
included specimens from Indonesia, Japan,
Malaysia and Thailand that, based on morpholog-
ical features, would be classified as H. durvillei sensu
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De Smedt et al. (2001).
Another name frequently used for branched spe-
cimens in the Indo-Pacific is H. floresii. De Smedt
et al. (2001) stated that reports of H. floresii from
the region probably refer to H. durvillei, since typ-
ical H. floresii specimens (type locality:
Mediterranean; without surface proliferation and
with a thin cortex and more regular branching
than H. durvillei), were not encountered. In addi-
tion, they stated that the relationship between H.
floresii var. harveyana (J. Agardh) Womersley &
J.A. Lewis and H. floresii was in need of further
study. Nevertheless, Kawaguchi (2004) compared
the morphology of type material of Halymenia
floresii to specimens from India, concluding that
the Indian specimens did indeed correspond to H.
floresii. Recently, however, Schneider et al. (2010)
showed that the morphology of a species from
Bermudas, H. pseudofloresii F.S. Collins & M.A.
Howe, overlapped with that of H. floresii from the
Mediterranean, but that the two were distinct
based on molecular information. These results
cast doubt on identifications based solely on mor-
phology and suggested that molecular methods are
a requirement for species assignment, particularly
for branched specimens.
Thus, H. durvillei and H. floresii in the Indo-
Pacific require re-examination. The conclusions
reached by De Smedt et al. (2001) and their tenta-
tive support by Kawaguchi et al. (2006) seem
unlikely given the results of Schneider et al.
(2010) and also our preliminary sequence data
analyses, which revealed considerable cryptic
diversity. In the present study, we undertook a
molecular and morphological examination of
specimens from the Malay archipelago and
peripheral Indo-Pacific localities (East African
coast, Hawaii), with the aim of understanding
species delimitation in branched Halymenia
species. Our results have led to the recognition of
two new species, which are described herein.
422
Materials and methods
Specimen acquisition and sampling
Samples were acquired from herbarium material housed
at the Trinity College Dublin Herbarium (TCD: type
material of Halymenia formosa TCD0011823), the
Bernice P. Bishop Museum Herbarium Pacificum
(BISH: specimens traditionally identified as H. formosa),
Ghent University Algal Herbarium (GENT: specimens
identified as Halymenia sp., H. durvillei and H. stipitata
I.A. Abbott), and Western Australian Herbarium
(PERTH: specimens identified as H. floresii).
Additionally, photos of the type material of H. har-
veyana J. Agardh, housed in the Botanical Museum,
Lund University (LD), were examined. Information
associated with the specimens and sequences can be
consulted in Supplementary Table 1.
Molecular analyses
Halymenia specimens stored in silica gel and fragments
from herbarium sheets (including type material for H.
formosa TCD0011823) were used in DNA extraction.
Samples were extracted using the DNeasy Plant Mini
Kit (Qiagen, Valencia, CA, USA) following the manu-
facturers protocols. The rbcL gene was amplified using
the F8-R1150, F8-R646 and F765ii-R1381ii primer pairs
(Freshwater & Rueness, 1994; Wang et al., 2000) in TC-
3000 and TC-3000G thermal cyclers (TECHNE). The
25-ml PCR reactions included 12.5 ml of GoTaq
Green Master Mix (Promega, including buffers,
TM
GoTaq , dNTPs and MgCl2), 9 ml of HyPure Cell
culture Grade Water (Thermo Scientific, USA), 2.5 ml
of DNA template (1/10 dilution) and 0.5 ml of each
primer (forward and reverse). The cycling conditions
consisted of an initial denaturation step of 94 C for
2 min, followed by 35 cycles of 30 s at 94 C, 1 min at
51 C and 2 min at 72 C. The primer pair F481R646
(which amplifies a short segment) was used for speci-
mens that did not amplify with previously listed primers
(e.g. herbarium material from BISH and the type speci-
men of H. formosa). We used the same PCR reaction
mix for the short fragment, but with the template DNA
added at a dilution of 1/100. The reaction was run with
an initial denaturation step of 94 C for 1 min, followed
by 35 cycles of 30s at 94 C, 1 min at 51 C and 1 min at
72 C. PCR products were purified using the QIAQuick
Purification Kit (Qiagen, Valencia, CA, USA) following
the manufacturers protocols and were sequenced com-
mercially by GATC Biotech, Konstanz, Germany or on
an ABI 377XL automated sequencer.
Thirteen additional sequences deposited in GenBank
were used as phylogenetic context for the analyses
(Supplementary Table 1). Thamnoclonium dichotomum,
Cryptonemia luxurians, C. lomation, Codiophyllum nata-
lense and Spongophloea tissotii were used as outgroups
following Huisman et al. (2011). Additionally, nine
sequences referred to as H. durvillei by Kawaguchi
et al. (2006) were obtained from the authors and are
deposited in Genbank in the present work
(Supplementary Table 1). A total of 38 rbcL sequences
 Halymenia spp. in the Indo-Pacific
were aligned with Clustal W and p-distances were deter-
mined using the program MEGA5 (Tamura et al., 2011).
For phylogenetic analysis, one copy of each set of
identical sequences was kept (final alignment of 29
sequences). Model selection was performed in
jModeltest under the corrected Akaike Information
Criterion (AICc). Maximum Likelihood (ML) analysis
was performed in Treefinder (Jobb, 2008) with the
GTR G I model and 500 bootstrap replicates.
Bayesian Inference (BI) was performed using Mr
Bayes 3.1.2 (Huelsenbeck & Ronquist, 2001) with set-
tings corresponding to the GTR G I model. Two
runs of Markov Chain Monte Carlo (MCMC) were per-
formed, each with one million generations with default
priors. Trees were sampled every hundred generations
and the program Tracer v.1.5 (Rambaut &
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Drummond, 2007) was used to determine the conver-
gence of the runs. A burn-in sample of 2500 trees was
discarded and the remaining trees were used to construct
the consensus tree.
Morphological analyses
Phylogenetic analysis indicated the presence of four clus-
ters (at the species level) among newly obtained
sequences, and the morphology of their corresponding
vouchers was examined. Characteristics previously used
to distinguish Halymenia species (Womersley & Lewis,
1994; Abbott, 1999; De Smedt et al., 2001) were sum-
marized in a data matrix and were tested to establish
diagnostic character states useful for morphological
identification in the molecular clusters. Anatomical
analyses were performed with small pieces of material
removed from herbarium sheets using a razor blade.
Hand sections were stained with 1% aniline blue, soft-
ened with 1% hydrochloric acid and mounted in 50%
Karo syrup (Englewood Cliffs, NJ, USA).
Photomicrographs were taken on an Olympus BX51
microscope with a DXM1200 digital camera (Nikon
UK, Surrey, UK). Qualitative information and data
ranges (maximum and minimum measurements for
quantitative characteristics) were obtained for each
characteristic of each species treated here. A diagnostic
characteristic used in the present study was a feature
that presented at least two differentiated, non-contigu-
ous states (e.g. spherical versus elongated, 2530 mm
versus 70150 mm). We compared the diagnostic
characteristics with the original descriptions of
related Halymenia species and three additional charac-
teristics were added because they had been identified as
diagnostic in other regions and other species (shape,
maculae on surface and number of cells in the cortex);
in total eight characteristics were used to compare the
four species studied here with other Halymenia species.
Results and discussion
Molecular analyses
The rbcL sequence alignment for phylogenetic
reconstruction included 29 sequences with a total
423
length of 1259 bp. Trees resulting from the ML and
BI analyses were virtually identical and Fig. 1
shows the ML tree with support values from
both analyses. Phylogenetic reconstruction
returned high bootstrap values at the terminal
branches while some internal nodes were poorly
supported (Fig. 1). Outgroup sequences comprised
two groups, one for Thamnoclonium dichotomum
and a second one including species of
Cryptonemia, Codiophyllum and Spongophloea.
The ingroup contained Halymenia floresii (the gen-
eritype from the Mediterranean Sea) and other
Halymenia species, but also other genera, including
Gelinaria ulvoidea and Epiphloea bullosa. The genus
Halymenia as presently circumscribed was not
monophyletic, since G. ulvoidea and E. bullosa
were embedded in a clade containing H. dilatata,
H. maculata and H. stipitata. Most relationships in
the HalymeniaEpiphloeaGelinaria clade were
moderately to well-supported (Fig. 1).
Specimens from the Philippines, Australia
South Africa, and Hawaii were positioned in
three related lineages, which we interpret as species
(labelled H. tondoana, H. harveyana and H. hawaii-
ana, respectively, in Fig. 1: see below, Taxonomic
proposals). There was support for the Philippines
(100/1.00) and Australia South Africa (89/0.99)
lineages, but low to moderate support for samples
from Hawaii (59/0.84). Specimens attributed to H.
durvillei sensu De Smedt et al. (2001) formed a
monophyletic group, which included both the spe-
cimens studied here and those from Kawaguchi
et al. (2006); it had moderate to high support
(84/1.00). Within the H. durvillei clade, there were
at least three major internal branches (which again
we interpret as species-level groups) separating the
specimens from (1) Tanzania, South Africa and Sri
Lanka (92/1.0), (2) Japan (no support) and (3)
Indonesia the Philippines (98/1.0), demonstrating
a clear biogeographical pattern.
Table 1 includes p-distances for the new
sequences and the two additional branches within
H. durvillei from Japan and Indonesia the
Philippines that were detected by Kawaguchi
Table 1. Ranges of p-distances among clusters observed in
the phylogenetic analysis for the genus Halymenia (Fig. 1).
Species pair P-distance (%)
H. hawaiianaH. tondoana 4.4
H. hawaiianaH. harveyana 2.7
H. hawaiianaH. durvillei 3.493.7
H. tondoanaH. harveyana 4.1
H. tondoanaH. durvillei 5.35.4
H. durvilleiH. harveyana 2.512.7
H. durvillei from TanzaniaH. durvillei 2.0
AB038603 Malaysia
H. durvillei from TanzaniaH. durvillei 2.1
KWGSH42 from Indonesia
 J. J. Hernandez-Kantun et al. 424
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Fig. 1. ML phylogenetic reconstruction based on rbcL gene sequences of Halymenia and related genera. ML bootstrap values
at nodes are shown first, followed by BI posterior probabilities. Values under 50% for ML and 0.5 for BI are not shown ().
Scale bar represents substitutions per site. New sequences from the present study are marked in bold. The Halymenia durvillei
sensu De Smedt et al. (2001) cluster is labelled and includes specimens from around the Indo-Pacific.

et al. (2006). The complete matrix, with compari-
sons between each pair of sequences used in the
alignment (38 in total), is presented in
Supplementary Table 2. All the P-distances
shown in Table 1 are high enough for species-
level discrimination, based on the correspondence
of morphospecies boundaries and p-distances
studied by Wang et al. (2001), Gavio &
Fredericq (2002) and Mateo-Cid et al. (2005).
However, we defer taxonomic reassessment of
the H. durvillei cluster sensu De Smedt et al.
(2001) until a more comprehensive sampling is
available.
Morphological character analysis
A total of 27 characteristics were analysed for mor-
phological variations and their states are presented
in Table 2. The characteristics that presented at
least two distinctive states without sharing or over-
lapping were the order of branching (with three
states, up to seven orders vs five vs three), spines
on the thallus surface (abundant vs rare), shape of
the cells in the inner cortex (elongated parallel to
the cortex vs spherical) and thickness of cortex
(with three states, 2560 mm vs 70150 mm vs
2530 mm). Stipe size measurements overlapped
for H. hawaiiana and H. tondoana; this character
was observed in just one specimen for H. durvillei
and H. harveyana respectively. Thus, we cannot
discount the possibility of stipe size as a diagnostic
feature until more information is obtained. The
characteristics and their states listed above were
used to construct the diagnoses for the two new
species. The 23 remaining characteristics were trea-
ted as shared and they were used in the description
of the new species.
 Halymenia spp. in the Indo-Pacific 425
Table 2. Morphological and anatomical variation among Halymenia species studied treated here. ND: no data; differential
characters states in bold; n: number of specimens examined.

Character H. durvillei (n 3) H. harveyana (n 1) H. hawaiiana (n 5) H. tondoana (n 5)

Morphology
Blade shape Branched Branched Branched Branched
Orders of branching up to 7 up to 5 up to 3 (palmate) up to 7
Axis ND ND Contorted Flat and contorted
Texture Cartilaginous and Cartilaginous and Cartilaginous and Cartilaginous and
mucilaginous mucilaginous mucilaginous mucilaginous
Margin Dentate and laciniate Dentate Dentate and lacerate Dentate
(not laciniate)
Spines or leaflets on margin Present Present Present Present
Maculae on surface Present Present Present Present
Spines on surface Abundant Abundant Abundant Rare
Axis shape Tapering toward Tapering toward Tapering toward Tapering toward
the apex the apex the apex the apex
Axis width (mm) 1520 1220 2048 1670
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Colour Dark pink Dark pink Pink to dark red Pink

Stipe shape Unbranched Unbranched Unbranched Unbranched
Surface Smooth Smooth Smooth Smooth
Stipe size (mm long) 5 2 210 1030
Vegetative anatomy
Shape of cells in outer cortex Elongated Elongated Elongated Elongated
Shape of cells in inner cortex Elongated parallel Spherical Elongated parallel Spherical
(with reference to the cortex)
Medulla Lax Lax Lax Lax
Refractive ganglionic cells Abundant Common Common Common
Thickness of the blade (mm) 4501000 500650 250800 300700
Thickness of cortex (mm) 70150 2530 4090 2560
Number of cells in cortex 47 45 37 45
Inner cortex cells size (mm) 12.550 1025 1537.5 7.520
Anticlinal filaments diameter (mm) 515 512.5 1017.5 7.515
Refractive ganglionic cells size (mm) 1580 3050 2050 4075
Reproductive anatomy
Tetrasporangia size (mm) ND ND ND 20  12.5
Carpospore size (mm) ND ND 7.510 1015
Spermatangia (mm) ND ND 2.5 2.5

Taxonomic proposals near stipeblade transition; cortex 4090 mm thick,

Halymenia hawaiiana J.J. Hernandez-Kantun &
A.R. Sherwood, sp. nov.
Figs 29
DIAGNOSIS: Thalli branched up to third order, with
abundant spines on the surface and stipe 210 mm
long. In transverse section, cortex 4090 mm thick
and with inner cortical cells elongated parallel to
the cortex.
DESCRIPTION: Thalli erect, foliose, 1030 cm tall,
pink to dark pink, cartilaginous with a slippery
(mucilaginous) surface texture, with a contorted
primary blade (24.4 cm wide), and 13 orders of
irregular branching (Fig. 2). Stipe small to incon-
spicuous, cartilaginous (210 mm long and 12 mm
in diameter), firm and unbranched, bearing blade
distally. Blades tapering toward apices, branching
distally from the primary blade, with a dentate or
lacerate margin but not laciniate; with abundant
spines on the thalli, macula on the surface
(Fig. 3). Blades 250800 mm thick (Fig. 4), thicker
with 37 cell layers forming anticlinal rows, differ-
entiated into outer and inner cortices (Fig. 5); outer
cortical cells elongate (515 mm long, 57.5 mm in
diameter); inner cortical cells elongated horizon-
tally (1537.5 mm in diameter) and increasing in
size near medullary filaments; medulla lax, consist-
ing of anticlinal filaments 1017.5 mm in diameter
(Fig. 4); refractive ganglionic cells common, 20
50 mm in diameter, irregularly shaped, with four
or five branches connected to each other under
the inner cortex (Fig. 6). Carpogonial ampullae
formed in the inner cortex, surrounded by few sec-
ondary (auxiliary) filaments with third order
branching and with a cup shape; in young cysto-
carps the auxiliary filaments composed of spherical
cells, but becoming elongate in mature cystocarps
(Fig. 7); cystocarps embedded in the medulla, with
an evident carpostome; carpospores 7.510 mm in
diameter (Fig. 8). Spermatangial sori (Fig. 9) scat-
tered over the thallus, the spermatangia formed
from outer cortical cells, one or two spermatangia
 J. J. Hernandez-Kantun et al. 426
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Figs 29. Habit and vegetative anatomy of Halymenia hawaiiana. 2. Herbarium specimen BISH692687 (holotype). Scale
bar 5 cm. 3. Detail of proliferations and maculae on thallus surface (BISH692687). Scale bar 1 cm. 4. Transverse section
of thallus showing anticlinal filaments running from cortex to cortex. Scale bar 100 mm (BISH772927). 5. Detail of the cortex
with inner and external cells. Scale bar 5 mm (BISH692687). 6. Stellate cell (arrow head) with refractive material. Scale
bar 100 mm (BISH772927). 7. View of an ampulla with auxiliary branches and an auxiliary cell. Scale bar 50 mm
(BISH692687). 8. Mature cystocarp with gonimoblast. Scale bar 50 mm (BISH692687). 9. Cortex showing the spermatangial
sori cut off by the cortical cells. Scale bar 25 mm (BISH772927).

cut off from each fertile surface
Tetrasporangia not observed.
HOLOTYPE: Housed at the Herbarium Pacificum,
Bernice P. Bishop Museum (BISH692687).
Collected at Kewalo Beach Park, Oahu, Hawaii,
cell. USA, coll. L.M. Hodgson, 31 March 2001: female
gametophyte. Genbank rbcL sequence accession
number: JQ976879.
TYPE LOCALITY: Kewalo Beach Park, Oahu,
Hawaii, USA.
 Halymenia spp. in the Indo-Pacific
ETYMOLOGY: The specific epithet is derived
from the Hawaiian Islands, where the alga was
collected.
SPECIMENS EXAMINED: Hawaii: Waikiki Beach,
Oahu, coll. Erin Cox, 17 April 2007, sterile speci-
men BISH750583; Kewalo Beach Park, Oahu, coll.
L.M. Hodgson, 31 March 2001, female gameto-
phyte BISH692687; Honolulu Harbor, Oahu,
coll. M.S. Doty, without date, sterile specimen
BISH489167; Honolulu Harbor, Oahu, coll. R.
Haroun, 26 January 2001, male gametophyte
BISH772927; Sand Island, Honolulu, Oahu, coll.
Erin Cox, 5 February 2007, sterile specimen
BISH750584.
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Halymenia tondoana O. De Clerck & J.J.
Hernandez-Kantun,, sp. nov.
Figs 1015
DIAGNOSIS: Thalli branched up to seventh order,
with rare spines on the surface and stipe 10
30 mm long. In transverse section, cortex 25
60 mm thick and with spherical cells in the inner
cortex.
DESCRIPTION: Thalli erect, foliose, to 22 cm tall and
1.67 cm wide, pink, with a cartilaginous and slip-
pery (mucilaginous) texture and smooth surface
with spots as granules or macula but rare spiny
proliferations. Primary blade with 57 orders of
branching, without a clear pattern but in some
cases resembling dichotomous bifurcations
(Figs 10, 11); blades gradually tapering to apices,
branching distally from the main axis, margin lac-
erate and with proliferations; stipes conspicuous,
unbranched, cartilaginous, 13 cm long, to 3 mm
in diameter (Figs 10, 11), bearing the blade distally.
Blades 300700 mm thick (Fig. 12); cortex 25
60 mm thick with four or five cell layers, forming
anticlinal rows, differentiated into inner and outer
cortices, each with two or three cell layers (Fig. 13);
outer cortical cells elongated (57.5 mm long,
2.55 mm in diameter); inner cortical cells spheri-
cal (7.520 mm in diameter) and increasing in
size near medullary filaments; medulla lax, consist-
ing of anticlinal filaments 7.515 mm in diameter
(Fig. 12); refractive ganglionic cells common,
4075 mm in diameter, irregular in shape, cells
with five or six branches. Carpogonial ampullae
formed in the inner cortex, surrounded by few
secondary (auxiliary) filaments with three orders
of branching and with a cup shape (Figs 14,
15); cystocarps within medulla (150200 mm diam-
eter) with an evident carpostome, carpospores
1015 mm in diameter. Dioecious plants with
spermatangial sori scattered over the thallus,
spermatangia (2.5 mm in diameter) formed from
427
the outer cortical cells. Tetrasporangia not
observed.
HOLOTYPE: Housed at Ghent University algal her-
barium (GENT HV847), from Dancalan, N of
Bulusan, SW Luzon, Philippines, coll. Heroen
Verbruggen, Roxie Diaz, Cristine Galanza and
Dinky Olandesca, 11 February 2004. Genbank
rbcL sequence accession number: JQ976881.
TYPE LOCALITY: Dancalan, N of Bulusan, SW
Luzon, Philippines.
ETYMOLOGY: The specific epithet is derived from
the Kingdom of Tondo (from the 10th century to
1591) in Luzon Island, Philippines.
SPECIMENS EXAMINED: Philippines: Dapdap,
Bulusan, SW Luzon, coll. Heroen Verbruggen,
Roxie Diaz, Cristine Galanza and Dinky
Olandesca, 11 February 2004, tetrasporophyte
GENT HV801, male gametophyte GENT
HV802, sterile specimen GENT HV803, sterile spe-
cimen GENT HV806, female gametophyte GENT
HV847.
Halymenia harveyana J. Agardh (1892), pp. 5556
CHARACTERISTICS: Thalli branched up to fifth
order, abundant spines on the surface and stipe
2 mm long. In transverse section, cortex 2530 mm
thick and inner cortical cells spherical.
SYNONYM: Halymenia floresii subsp. harveyana
(J. Agardh) Womersley & Lewis (1994, p. 191,
figs 55 AC, 56B).
LECTOTYPE: Harvey, Australian algae Exsiccatae
435E: Agardh Herbarium, LD 22 337 (Figs 16, 17).
TYPE LOCALITY: Port Phillip Heads, Victoria,
Australia.
SPECIMENS EXAMINED: Australia: Jurien Bay,
Western Australia, coll. Undetermined, sterile spe-
cimen JB700. South Africa: mile Reef, Sodwana
Bay, coll. De Clerck, Fredericq, Freshwater,
Leliaert, Millar, Schills and Tronchin, 11
February 2001, sterile specimen GENT
KZN2150, Fig. 17.
NOTES: This species was placed in synonymy with
Halymenia floresii by Womersley & Lewis (1994),
based on the morphological similarity in branching
pattern and the blade thickness. In the present
study, the branching pattern of the type of H. har-
veyana LD 22 337 agrees with the specimen studied
and listed above. Additionally, the Halymenia spe-
cimens are separated in a highly supported clade
which is positioned far from H. floresii (Fig. 1).
Based on these findings, we propose to keep the
specific name H. harveyana.
 J. J. Hernandez-Kantun et al. 428
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Figs 1015. Morphology and anatomy of Halymenia tondoana. 10. Herbarium specimen GENT HV847 (holotype). Scale
bar 5 cm. 11. Herbarium specimen GENT HV802. Scale bar 5 cm. 12. Transverse section of thallus showing anticlinal
filaments running from cortex to cortex. Scale bar 100 mm (GENT HV847). 13. Detail of the cortex with inner and external
cells. Scale bar 50 mm (GENT HV847). 14. View of an ampulla with auxiliary branches and an auxiliary cell. Scale
bar 50 mm (GENT HV847). 15. Mature cystocarp with a compact mass of carpospores surrounded by sterile filaments.
Scale bar 50 mm (GENT HV847).
 Halymenia spp. in the Indo-Pacific
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Figs 16, 17. Morphology of Halymenia harveyana. 16.
Lectotype, Herbarium Agardh, LD 22337. 17. Herbarium
accession GENT KZN2150. Scale bar 1 cm.
Halymenia durvillei complex (De Smedt et al., 2001,
Figs 1-6, Tables 1, 2)
CHARACTERISTICS: Thalli branched up to seventh
order, abundant spines on the surface and stipe
5 mm long. In transverse section, cortex
70150 mm thick and inner cortical cells elongated
parallel to the outer cortex.
SPECIMENS EXAMINED: South Africa: mile Reef,
Sodwana Bay, coll. De Clerck, Fredericq,
Freshwater, Leliaert, Millar, Schills and
Tronchin, 11 February 2001, sterile specimen
GENT KZN2149. Tanzania: Zanzibar, Matemwe,
coll. Undetermined, 22 August 1994, sterile speci-
men GENT HEC10537. South Africa: Mabibi
Reef, coll. De Clerck, Fredericq, Freshwater,
Leliaert, Millar, Schills and Tronchin, 13
February 2001, sterile specimen GENT KZN2177.
NOTES: The broad concept of H. durvillei by De
Smedt et al. (2001) included specimens with
branched thalli, proliferation on the surface, no
mottling, inner cortex >3 cell layers and >25 mm
thick, external cells >8 mm long and medulla
>200 mm. Based on those characteristics, any of
the specimens studied in the present work, includ-
ing those now separated into H. hawaiiana and H.
tondoana, could easily be identified with that name.
Nevertheless, in the present study, after the molec-
ular and morphological analysis, we found some
429
additional characteristics to identify cryptic species
within the broad concept of H. durvillei. The two
most distinctive are H. hawaiiana and H. tondoana
(Fig. 1, Tables 1 and 2), but even after these have
been removed from H. durvillei, it is evident from
the molecular analysis that the remaining branches
represent a complex of at least three species (Fig. 1,
Table 1). The description by De Smedt et al. (2001)
specifies the presence of a high branching pattern
(up to seventh order) and a thick cortex (50
100 mm) for H. durvillei; these characteristics are
shared with the specimens we studied (branching
up to seventh order and 70150 mm cortex thick-
ness: Table 2). Additionally, Kawaguchi et al.
(2006) reported that the nine specimens they stud-
ied and identified as H. durvillei had branching up
to seventh order and a cortex thickness of 50
60 mm (measured from their photographs) using
specimens from Japan, Thailand and Indonesia.
Since all previously and newly sequenced speci-
mens share the same thickness of the cortex and
branching order considered to be characteristic of
H. durvillei by De Smedt et al. (2001), we propose
to use these characters to identify the Halymenia
durvillei complex, until a more informed decision
can be made on the number of species in the
complex.
General discussion
The phylogenetic reconstruction presented here
(Fig. 1) shows that the genus Halymenia, as pres-
ently circumscribed, is not monophyletic and that
the clade containing the generitype (H. floresii)
also includes Gelinaria and Epiphloea. However,
our analysis was based only on rbcL and it will
be necessary to increase the number of phylogenet-
ically informative characters, through use of more
molecular markers (possibly psbA, EF2 or SSU), in
order to elucidate generic boundaries in the
Halymeniales. Molecular information will also
make it possible to calibrate morphology at the
level of genera and higher taxonomical ranks.
For example, the characteristics pertaining to the
cystocarp that have been used to distinguish genera
(Balakrishnan, 1961; Chiang, 1970) have not been
analysed with a molecular approach.
The present phylogenetic reconstruction based
on rbcL clearly separated four related clusters
among Halymenia specimens (Fig. 1). Additionally,
p-distances were sufficiently high among the
groups of sequences to delimit species (Table 1),
with values agreeing with the interspecific values
of 1.510% that have been reported for
Grateloupia (Halymeniaceae) (Wang et al., 2001;
Gavio & Fredericq, 2002; Mateo-Cid et al., 2005)
or the 0.516.85% for Phycodrys (Delesseriaceae:
Lin & Nelson, 2010).
 J. J. Hernandez-Kantun et al. 430

Present study
H. tondoana
In the analysis to establish diagnostic character-

Branched
istics for morphological identification many of the

Up to 7

Present

Round
1030

2560
Rare
measurements and features were shared by the four

45
species studied and only five characters were con-
sidered diagnostic (Table 2). After comparing the

tetrasporangia
H. stipitata

species studied in the present study with some

Abbott, 1998

Triangular
other related species (Table 3), we established
Present if

60100
Simple

that H. harveyana differs from H. chiangiana I.A.

ND Abbott & Kraft by the presence in the latter of a
20

3
simple blade without branches and a smaller stipe.
Ruiz, 2004
Ballantine &
H. mirabilis

Halymenia hawaiiana and H. mirabilis D.L.

Branched
Up to 5

Ballantine & H. Ruiz are separated by the more

Present

Round
2530

highly branched thallus (up to fifth order), a thin-

ND
10

ner cortex (2530 mm), and the round shape of the

Up to 3 (palmate)

cells in the inner cortex of H. mirabilis. The two

H. hawaiiana
Downloaded by [National University of Ireland - Galway] at 01:36 03 November 2012

new species can be discriminated from H. floresii

Present study

and H. stipitata by at least two characteristics,

Abundant

Elongated
parallel
Branched

Present

which are illustrated in Table 3. We recommend

4090
210

the use of molecular identification since the mor-

37

phology could vary in other populations not

Present study
H. harveyana

included here. For the remainder of the species in

Abundant
Branched

the genus, additional morphological information is

Up to 5

Present

Round
2530

necessary to establish characteristics that could be

45

useful in identification.
2

Based on the molecular analysis of the H. durvil-

H. floresii (Lectotype)

lei complex in Fig. 1 (and the p-distances; Table 2),

the main branches within it should be separated at
the species level. Nevertheless, we propose to refer
Kawaguchi,

Branched

to these taxa as the H. durvillei complex (based on

Up to 3

Absent

Absent
2004

Round

the sequences and morphological characteristics

ND
35

45
Table 3. Comparison of diagnostic characteristics for Halymenia species. ND no data.

presented) until further information is available

and more detailed reassessments of the species
Round to stellate
De Smedt et al.

are possible using type material and a wide range

H. durvillei

of samples from different regions. Morphological

Abundant
Branched
Up to 7

identifications must be considered preliminary

Absent
2001

50100
0.514

until comparative molecular data are also

68

available.
Present study

RbcL could not be successfully amplified from

H. durvillei

Abundant

Elongated
parallel

the fragment of type material of H. formosa used in

Branched
Up to 7

Present

70150

the present study, and so the phylogenetic position

47

of this species cannot be established until fresh

5

specimens from the type locality become available.

Absent (abundant
Kraft & Abbott,

Halymenia formosa has been the name commonly

H. chiangiana

projections)

used for branched specimens from the Hawaiian

Islands (BISH692687, BISH489167 and

1997

Round
Simple

3540

BISH772927). We propose a new name for this

ND

46
15

species, H. hawaiiana, since H. formosa has been

synonymized with H. durvillei by De Smedt et al.
(with reference to the outer cortex)

(2001) and, as we have shown, H. durvillei is a dif-

ferent group of species (Fig. 1, Table 2).
Additionally, the type specimen of H. formosa
Number of cells in cortex
Thickness of cortex (mm)

has up to seven orders of branching and lacks a

Inner cortex cells shape
Orders of branching

stipe. Unfortunately the material was difficult to

Maculae on surface
Stipe length (mm)

Spines on surface

rehydrate and did not allow precise anatomical

Source of data

measurements (Supplementary information, Figs

Blade shape

S1, S2), but the cells in the inner cortex were

observed to be elongated parallel to the cortex as
in H. durvillei (Table 2). Due to the reduced
s
 Halymenia spp. in the Indo-Pacific
number of characteristics observed in the type
material of H. formosa, we agree cautiously that
H. formosa may be synonymous with H. durvillei,
as suggested by De Smedt et al. (2001).
Two new Halymenia species are presented here,
H. hawaiiana and H. tondoana, both of which have
branched blades. However, there are at least five
other species with branched blades, namely H. acu-
minata (Holmes) J. Agardh, H. cromwellii I.A.
Abbott, H. microcarpa (Montagne) P.C. Silva
and H. tenuispina Kutzing (Supplementary
Table 2), that were not included in the present
study. Most of the original descriptions of these
species do not include the characteristics used in
the present study; thus, as with H. formosa, further
Downloaded by [National University of Ireland - Galway] at 01:36 03 November 2012
molecular and morphological information from
specimens from the type localities will be necessary
to completely understand species boundaries and
relationships.
We recognize H. harveyana as a separate species,
distinct from H. floresii (Fig. 1, Table 2), where it
had been placed as a subspecies by Womersley &
Lewis (1994). Although material from the type
locality (Port Phillip Bay, Victoria, Australia)
was not sequenced, the morphological similarities
between our specimens and the type and other spe-
cimens described by Womersley & Lewis (1994)
support our identification. Further morphological
and molecular studies are necessary to determine
the geographical and morphological range of this
species in Australia.
The presence of H. floresii in the Indo-Pacific is
doubtful and previous reports of this species may
refer to other, morphologically similar species. In
Bermuda (the type locality of H. pseudofloresii),
Schneider et al. (2010) found that sequences from
specimens identified as H. floresii (also reported in
the area) clustered with H. pseudofloresii and were
far from the cluster of Mediterranean specimens
(type locality of H. floresii), effectively removing
H. floresii from the Bermudan flora. Based on
our molecular analyses, none of the branched spe-
cies from the Indo-Pacific are related to H. floresii
from the Mediterranean (Fig. 1), so this species
should no longer be considered as part of the
floras of the areas studied, pointing to a very
restricted distribution in the Mediterranean.
Acknowledgements
J.H.K. is supported by CONACyT-211950 (National
Council for Science and Technology, Mexico) and
SEP (Secretariat for Public Education, Mexico) with
a PhD scholarship. Laboratory facilities were pro-
vided by the Beaufort Award for Marine
Biodiscovery to the National University of Ireland,
Galway (European Community through the FP6-
funded project HIPPOCRATES NMP3-CT-2003-
431
505758). Funding for the molecular analyses was pro-
vided by a grant from the National Science
Foundation (DEB-0542608) to A.R.S. and G.G.
Presting. Funding was provided by CONABIO
(V044), CONACYT-SEMARNAT (2004-01-243)
and CONACYT-SEP (34118-V and 23 967) to
R.R.R. J.M.H. acknowledges the financial support
of the Australian Biological Resources Study. We
would like to thank BISH for the loan of herbarium
material and the collection manager Amanda
Harbottle for information provided. Thanks are
also due to Patrik Froden, curator of the Botanical
Museum (LD), Lund University, and to John Parnell,
curator of the Herbarium, Botany School, Trinity
College, Dublin. We appreciate the comments of the
associated editor Heroen Verbruggen and an anony-
mous reviewer. J.H.K. is grateful to Dr Fabio Rindi
and Dr Svenja Heesch for valuable suggestions.
Supplementary information
The following supplementary material is available
for this article, accessible via the Supplementary
Content tab on the articles online page at http://
dx.doi.org/10.1080/09670262.2012.733734.
Supplementary Table 1. Complementary infor-
mation related with the sequences used in the pre-
sent study.
Supplementary Figs S1, S2. Morphology and
anatomy of the type material of Halymenia for-
mosa TCD0011823.
Supplementary Fig. S1. Morphology of the spe-
cimens with a branching pattern of up to the sixth
or seventh order. Scale bar 1 cm.
Supplementary Fig. S2. Transverse section
showing the cortex with five or six layers of cells.
The rehydration of the tissue was poor and the size
of the cortex is less than 10 mm. Scale bar 50 mm.
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