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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
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
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
floresii to specimens from India, concluding that GoTaq , dNTPs and MgCl2), 9 ml of HyPure Cell
culture Grade Water (Thermo Scientific, USA), 2.5 ml
the Indian specimens did indeed correspond to H.
of DNA template (1/10 dilution) and 0.5 ml of each
floresii. Recently, however, Schneider et al. (2010) primer (forward and reverse). The cycling conditions
showed that the morphology of a species from consisted of an initial denaturation step of 94 C for
Bermudas, H. pseudofloresii F.S. Collins & M.A. 2 min, followed by 35 cycles of 30 s at 94 C, 1 min at
Howe, overlapped with that of H. floresii from the 51 C and 2 min at 72 C. The primer pair F481R646
Mediterranean, but that the two were distinct (which amplifies a short segment) was used for speci-
based on molecular information. These results mens that did not amplify with previously listed primers
cast doubt on identifications based solely on mor- (e.g. herbarium material from BISH and the type speci-
men of H. formosa). We used the same PCR reaction
phology and suggested that molecular methods are
mix for the short fragment, but with the template DNA
a requirement for species assignment, particularly added at a dilution of 1/100. The reaction was run with
for branched specimens. an initial denaturation step of 94 C for 1 min, followed
Thus, H. durvillei and H. floresii in the Indo- by 35 cycles of 30s at 94 C, 1 min at 51 C and 1 min at
Pacific require re-examination. The conclusions 72 C. PCR products were purified using the QIAQuick
reached by De Smedt et al. (2001) and their tenta- Purification Kit (Qiagen, Valencia, CA, USA) following
tive support by Kawaguchi et al. (2006) seem the manufacturers protocols and were sequenced com-
unlikely given the results of Schneider et al. mercially by GATC Biotech, Konstanz, Germany or on
(2010) and also our preliminary sequence data an ABI 377XL automated sequencer.
analyses, which revealed considerable cryptic Thirteen additional sequences deposited in GenBank
diversity. In the present study, we undertook a were used as phylogenetic context for the analyses
(Supplementary Table 1). Thamnoclonium dichotomum,
molecular and morphological examination of
Cryptonemia luxurians, C. lomation, Codiophyllum nata-
specimens from the Malay archipelago and
lense and Spongophloea tissotii were used as outgroups
peripheral Indo-Pacific localities (East African following Huisman et al. (2011). Additionally, nine
coast, Hawaii), with the aim of understanding sequences referred to as H. durvillei by Kawaguchi
species delimitation in branched Halymenia et al. (2006) were obtained from the authors and are
species. Our results have led to the recognition of deposited in Genbank in the present work
two new species, which are described herein. (Supplementary Table 1). A total of 38 rbcL sequences
Halymenia spp. in the Indo-Pacific 423
were aligned with Clustal W and p-distances were deter- length of 1259 bp. Trees resulting from the ML and
mined using the program MEGA5 (Tamura et al., 2011). BI analyses were virtually identical and Fig. 1
For phylogenetic analysis, one copy of each set of shows the ML tree with support values from
identical sequences was kept (final alignment of 29 both analyses. Phylogenetic reconstruction
sequences). Model selection was performed in returned high bootstrap values at the terminal
jModeltest under the corrected Akaike Information
branches while some internal nodes were poorly
Criterion (AICc). Maximum Likelihood (ML) analysis
was performed in Treefinder (Jobb, 2008) with the supported (Fig. 1). Outgroup sequences comprised
GTR G I model and 500 bootstrap replicates. two groups, one for Thamnoclonium dichotomum
Bayesian Inference (BI) was performed using Mr and a second one including species of
Bayes 3.1.2 (Huelsenbeck & Ronquist, 2001) with set- Cryptonemia, Codiophyllum and Spongophloea.
tings corresponding to the GTR G I model. Two The ingroup contained Halymenia floresii (the gen-
runs of Markov Chain Monte Carlo (MCMC) were per- eritype from the Mediterranean Sea) and other
formed, each with one million generations with default Halymenia species, but also other genera, including
priors. Trees were sampled every hundred generations Gelinaria ulvoidea and Epiphloea bullosa. The genus
and the program Tracer v.1.5 (Rambaut & Halymenia as presently circumscribed was not
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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- least two distinctive states without sharing or over-
sons between each pair of sequences used in the lapping were the order of branching (with three
alignment (38 in total), is presented in states, up to seven orders vs five vs three), spines
Supplementary Table 2. All the P-distances on the thallus surface (abundant vs rare), shape of
shown in Table 1 are high enough for species- the cells in the inner cortex (elongated parallel to
level discrimination, based on the correspondence the cortex vs spherical) and thickness of cortex
of morphospecies boundaries and p-distances (with three states, 2560 mm vs 70150 mm vs
studied by Wang et al. (2001), Gavio & 2530 mm). Stipe size measurements overlapped
Fredericq (2002) and Mateo-Cid et al. (2005). for H. hawaiiana and H. tondoana; this character
However, we defer taxonomic reassessment of was observed in just one specimen for H. durvillei
the H. durvillei cluster sensu De Smedt et al. and H. harveyana respectively. Thus, we cannot
(2001) until a more comprehensive sampling is discount the possibility of stipe size as a diagnostic
available. feature until more information is obtained. The
characteristics and their states listed above were
Morphological character analysis used to construct the diagnoses for the two new
A total of 27 characteristics were analysed for mor- species. The 23 remaining characteristics were trea-
phological variations and their states are presented ted as shared and they were used in the description
in Table 2. The characteristics that presented at 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.
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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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 cell. USA, coll. L.M. Hodgson, 31 March 2001: female
Tetrasporangia not observed. gametophyte. Genbank rbcL sequence accession
number: JQ976879.
HOLOTYPE: Housed at the Herbarium Pacificum,
Bernice P. Bishop Museum (BISH692687). TYPE LOCALITY: Kewalo Beach Park, Oahu,
Collected at Kewalo Beach Park, Oahu, Hawaii, Hawaii, USA.
Halymenia spp. in the Indo-Pacific 427
ETYMOLOGY: The specific epithet is derived the outer cortical cells. Tetrasporangia not
from the Hawaiian Islands, where the alga was observed.
collected.
HOLOTYPE: Housed at Ghent University algal her-
SPECIMENS EXAMINED: Hawaii: Waikiki Beach, barium (GENT HV847), from Dancalan, N of
Oahu, coll. Erin Cox, 17 April 2007, sterile speci- Bulusan, SW Luzon, Philippines, coll. Heroen
men BISH750583; Kewalo Beach Park, Oahu, coll. Verbruggen, Roxie Diaz, Cristine Galanza and
L.M. Hodgson, 31 March 2001, female gameto- Dinky Olandesca, 11 February 2004. Genbank
phyte BISH692687; Honolulu Harbor, Oahu, rbcL sequence accession number: JQ976881.
coll. M.S. Doty, without date, sterile specimen
TYPE LOCALITY: Dancalan, N of Bulusan, SW
BISH489167; Honolulu Harbor, Oahu, coll. R.
Luzon, Philippines.
Haroun, 26 January 2001, male gametophyte
BISH772927; Sand Island, Honolulu, Oahu, coll. ETYMOLOGY: The specific epithet is derived from
Erin Cox, 5 February 2007, sterile specimen the Kingdom of Tondo (from the 10th century to
BISH750584. 1591) in Luzon Island, Philippines.
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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 429
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
Triangular
other related species (Table 3), we established
Present if
60100
Simple
3
simple blade without branches and a smaller stipe.
Ruiz, 2004
Ballantine &
H. mirabilis
Round
2530
Elongated
parallel
Branched
Present
Present
Round
2530
useful in identification.
2
Branched
Absent
Absent
2004
Round
45
Table 3. Comparison of diagnostic characteristics for Halymenia species. ND no data.
50100
0.514
available.
Present study
Abundant
Elongated
parallel
Present
70150
projections)
Round
Simple
3540
46
15
Spines on surface
number of characteristics observed in the type 505758). Funding for the molecular analyses was pro-
material of H. formosa, we agree cautiously that vided by a grant from the National Science
H. formosa may be synonymous with H. durvillei, Foundation (DEB-0542608) to A.R.S. and G.G.
as suggested by De Smedt et al. (2001). Presting. Funding was provided by CONABIO
Two new Halymenia species are presented here, (V044), CONACYT-SEMARNAT (2004-01-243)
H. hawaiiana and H. tondoana, both of which have and CONACYT-SEP (34118-V and 23 967) to
branched blades. However, there are at least five R.R.R. J.M.H. acknowledges the financial support
other species with branched blades, namely H. acu- of the Australian Biological Resources Study. We
minata (Holmes) J. Agardh, H. cromwellii I.A. would like to thank BISH for the loan of herbarium
material and the collection manager Amanda
Abbott, H. microcarpa (Montagne) P.C. Silva
Harbottle for information provided. Thanks are
and H. tenuispina Kutzing (Supplementary
also due to Patrik Froden, curator of the Botanical
Table 2), that were not included in the present
Museum (LD), Lund University, and to John Parnell,
study. Most of the original descriptions of these curator of the Herbarium, Botany School, Trinity
species do not include the characteristics used in College, Dublin. We appreciate the comments of the
the present study; thus, as with H. formosa, further associated editor Heroen Verbruggen and an anony-
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molecular and morphological information from mous reviewer. J.H.K. is grateful to Dr Fabio Rindi
specimens from the type localities will be necessary and Dr Svenja Heesch for valuable suggestions.
to completely understand species boundaries and
relationships.
We recognize H. harveyana as a separate species, Supplementary information
distinct from H. floresii (Fig. 1, Table 2), where it The following supplementary material is available
had been placed as a subspecies by Womersley & for this article, accessible via the Supplementary
Lewis (1994). Although material from the type Content tab on the articles online page at http://
locality (Port Phillip Bay, Victoria, Australia) dx.doi.org/10.1080/09670262.2012.733734.
was not sequenced, the morphological similarities Supplementary Table 1. Complementary infor-
between our specimens and the type and other spe- mation related with the sequences used in the pre-
cimens described by Womersley & Lewis (1994) sent study.
support our identification. Further morphological Supplementary Figs S1, S2. Morphology and
and molecular studies are necessary to determine anatomy of the type material of Halymenia for-
the geographical and morphological range of this mosa TCD0011823.
species in Australia. Supplementary Fig. S1. Morphology of the spe-
The presence of H. floresii in the Indo-Pacific is cimens with a branching pattern of up to the sixth
doubtful and previous reports of this species may or seventh order. Scale bar 1 cm.
refer to other, morphologically similar species. In Supplementary Fig. S2. Transverse section
Bermuda (the type locality of H. pseudofloresii), showing the cortex with five or six layers of cells.
Schneider et al. (2010) found that sequences from The rehydration of the tissue was poor and the size
specimens identified as H. floresii (also reported in of the cortex is less than 10 mm. Scale bar 50 mm.
the area) clustered with H. pseudofloresii and were
far from the cluster of Mediterranean specimens
(type locality of H. floresii), effectively removing References
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