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Pseudosiderastrea formosa sp. nov. (Cnidaria: Anthozoa: Scleractinia) a
New Coral Species Endemic to Taiwan
Michel Pichon1, Yao-Yang Chuang2,3, and Chaolun Allen Chen2,3,4,*
1Museum of Tropical Queensland, 70-102 Flinders Street, Townsville 4810, Australia
2Biodiversity Research Center, Academia Sinica, Nangang, Taipei 115, Taiwan
3Institute of Oceanography, National Taiwan Univ., Taipei 106, Taiwan
4Institute of Life Science, National Taitung Univ., Taitung 904, Taiwan
(Accepted September 1, 2011)
Michel Pichon, Yao-Yang Chuang, and Chaolun Allen Chen (2012) Pseudosiderastrea formosa sp. nov.
(Cnidaria: Anthozoa: Scleractinia) a new coral species endemic to Taiwan. Zoological Studies 51(1): 93-98.
Pseudosiderastrea formosa sp. nov. is a new siderastreid scleractinian coral collected in several localities in
Taiwan. It lives on rocky substrates where it forms encrusting colonies. Results of morphological observations
and molecular genetic analyses are presented. The new species is described and compared to P. tayamai and
Siderastrea savignyana, and its morphological and phylogenic afnities are discussed.
http://zoolstud.sinica.edu.tw/Journals/51.1/93.pdf
Key words: Pseudosiderastrea formosa sp. nov., New species, Scleractinia, Siderastreid, Western Pacic
Ocean.
*To whom correspondence and reprint requests should be addressed. E-mail:michel.pichon@bigpond.com; cac@gate.sinica.edu.tw
A siderastreid scleractinian coral was
collected from several localities around Taiwan
and nearby islands, where it is relatively rare.
The specimens present some morphological
similarities with Pseudosiderastrea tayamai Yabe
and Sugiyama, 1935, the only species hitherto
known from that genus, and with Siderastrea
savignyana Milne Edwards and Haime, 1849,
which is the sole representative in the Indian
Ocean of the genus Siderastrea de Blainville,
1830. In order to ascertain its taxonomic position,
morphological observations were carried out on a
suite of 33 specimens at the Museum of Tropical
Queensland, Townsville, Australia and at the
Biodiversity Research Center, Academia Sinica,
Taipei, Taiwan. Molecular phylogenetic analyses
were also conducted at the Biodiversity Research
Center. The results presented below indicate
that these specimens belong to a new species of
Pseudosiderastrea, described as P. formosa sp.
nov.
MATERIAL AND METHODS
Specimens were collected by scuba diving at
Wanlitung (21°59'48"N, 120°42'10"E) and the outlet
of the 3rd nuclear power plant (21°55'51.38"N,
120°44'46.82"E) on the southeastern coast
of Taiwan in Kenting National Park, Chi-Fai
(23°7'0.59"N, 121°23'49.58"E) in Taitung County,
and at Yeiyu (22°3'1"E, 121°30'35") at Orchid I.
(Lanyu in Chinese). Specimens for morphological
studies were bleached to remove soft tissues
by dipping them in household bleach (sodium
hypochlorite) for 24 h. They were then rinsed with
fresh water and thoroughly dried. Morphological
observations were carried out using a Leica
Zoological Studies 51(1): 93-98 (2012)
93
MX8 stereomicroscope, equipped with an ocular
graticule. Scanning electron microscopy (SEM)
was performed at James Cook Univ., Townsville,
Australia on a JEOL 5410LV instrument.
Samples for the molecular phylogenetic
analyses were collected from Bocas del Toro,
Panama (S. radians and S. siderea); Isla Uraba,
Panama (S. glynni); Brazil (S. stellata); Kiunga,
Kenya (S. savignyana); and Kaohsiung (P.
tayamai) and Wanlitung, Taiwan (P. formosa sp.
nov.). For each sample, a piece of about 5 × 5 cm
was stored in a modified guanidine solution or
75% ethanol. DNA extraction methods were as
specified by Fukami et al. (2004). Cytochrome
(Cyt) b sequences were amplied by a polymerase
chain reaction (PCR) with the primer set, AcCytbF
(5'-GCCGTCTCCTTCAAATATAAG-3') and
AcCytbR (5'-AAAAGGCTCTTCTACAAC-3')
(Fukami et al. 2008), with the following PCR
conditions: 94°C for 2 min, followed by 35 cycles
at 94°C for 45 s, 50°C for 30 s, and 72°C for 60 s,
and ending with a nal phase at 72°C for 10 min.
PCR products were directly sequenced.
Se quenc es w ere aligned u si ng c odons ,
and their genetic distances were calculated
using MEGA5 (Tamura et al. 2011). Cyt b, a
highly variable mitochondrial coding region
in Siderastrea, was selected to analyze the
divergence of Pseudosiderastrea specimens
and their evolutionary status with the closely
related genus, Siderastrea (Fukami et al. 2008).
Using the nal dataset, which contained 16 Cyt b
sequences of 771 base pairs (bp), the best tting
evolutionary models were determined by the
Akaike information criterion (AIC) test in ModelTest
(Posada et al. 1998). A phylogenetic analysis
was performed using PhyML 3.0 (Guindon et al.
2010) for maximum-likelihood (ML) and MrBayes
(Ronquist et al. 2003) for Bayesian inference (BI),
under the GTR+I model of DNA evolution. The ML
was performed using Shimodaira and Hasegawa
(SH-like) branch support with 1000 bootstrap
replicates. Sequences obtained from this study
were submitted to GenBank with accession nos.
JN600483-98.
For the BI, 6 runs with 5 × 106 generations
each were calculated, while topologies were saved
every 100 generations. One-fifth of the 50,000
topologies were discarded as burn-in, and the
remaining ones were used to calculate posterior
probabilities.
RESULTS
Family Siderastreidae Vaughan and Wells, 1943
Genus Pseudosiderastrea Yabe and Sugiyama,
1935
Pseudosiderastrea formosa sp. nov.
Synonomy: Siderastrea savignyana Dai & Horng 2008, p. 165.
Material examined: Holotype: Museum of
Tropical Queensland G 64378 Taiwan, Wanlitung
21°59.85'N, 120°42.22'E. Depth 3 m, Coll.
A. Chen, 20 Nov. 2009. Paratypes: Museum
of Tropical Queensland. G 64374-7 Taiwan,
Wanlitung 21°59.85'N, 120°42.22'E. Depth 3 m,
Coll. A. Chen, 20 Nov. 2009.
Other material: Museum of Tropical Queens-
land. G 64352-64, Taiwan, Lanyu (Orchid I.); G
64365-73 Taiwan, Kenting. Biodiversity Research
Center Museum. ASIZC0000958-9, Taiwan, Chi-
Fai.
Description: Colony small, thin, and tightly
encrusting substratum. Most specimens examined
being fragments of colonies up to 5 cm in
maximum dimension. Holotypic colony (fragment)
47 × 22 mm (Fig. 1). Growing margins very thin,
often showing incomplete calcification of corallite
structures. Corallites cerioid and uniform in
shape and size within each specimen examined.
Corallite shape possibly varying from subcircular to
polygonal and even squarish in some specimens.
In latter, arrangement of corallites tending to be
in linear rows. Corallite size range 1.8-4.4 mm in
calicular diameter (mean maximum diameter, 2.8
± 0.2 mm). Septa wedge-shaped (Fig. 2), and
hexamerally arranged in 3 cycles, sometimes part
of 4th (S1 and S2 > S3 and S4). Smaller corallites
with only 18 septa, whereas larger corallites with
up to 34 septa. S3 and S4 tending to curve and
flanking S1 and S2, sometimes deeply fused
in fossa. Such a fusion pattern never involving
more than 3 septa, and rarely present more than
twice in any given corallite. A number of corallites
completely lacking any septal fusion. Septa slightly
exserted, continuous, and convex over corallite
edge. Near corallite edge, septa only moderately
inclined towards calicular center, and then sloping
more steeply towards columellar pit. Septal axial
edges bearing conspicuous ornamentation (Fig. 2)
composed of 7-10 granules, sometimes flattened
transversally (Fig. 3). Septal faces entire and
ornamented with small, pointed granules (Fig.
3). Fossa up to 2 mm deep, containing a well-
developed, convex, massive columella. Columella
Pichon et al. – Pseudosiderastrea formosa in Taiwan94
circular and up to 1 mm in diameter (average
diameter, 0.8 mm) sometimes reaching up to 1/3
of corallite diameter (Fig. 4). However, some
corallites with a slightly elongate columella,
composed of 2-4 smooth elements. Columella
often visible below oral disc in live specimens.
Wall solid and similar in thickness to septal outer
edge (0.3 mm). Synapticular ring absent within
corallite wall. However, a few synapticulae
possibly present in some corallites, and in such
specimens, some synapticulae also present on thin
growing margin of corallum in a few incompletely
developed peripheral corallites. Corallum white to
light beige. Living colonies grayish-green, beige,
or pink.
Etymology: The species name formosa
(Latin formosus: beautiful, elegant) refers to the
regular and neat aspect of the corallum. It is also
reminiscent of the old name for Taiwan, where this
species is thought to be endemic.
Distribution: Known only from Taiwan and
nearby islands, incrusting bare rocky outcrops at
< 10 m deep (Fig. 5), where it may co-occur with
P. tayamai.
Remarks: Overall, skeletal characters display
Fig. 1. P. formosa sp. nov., holotype MTQ G 64378. Wanlitung,
Taiwan.
5 mm
Fig. 3. P. formosa sp. nov. MTQ G 64373. Scanning electron
microscopic image. Note the laterally flattened septal
dentations and conical ornamentation on the septal sides.
100 μm
Fig. 2. P. formosa sp. nov. MTQ G 64365. Scanning electron
microscopic image. Note the exserted septa and well-
developed septal ornamentation.
1 mm
Fig. 4. P. formosa sp. nov., holotype. Note the non-exserted
septa, solid wall, and well-developed columella.
5 mm
Fig. 5. P. formosa sp. nov. from Wanlitung. A small colony
living on rocky substrate.
95Zoological Studies 51(1): 93-98 (2012)
little variation among specimens, and only minor
differences were observed. They principally
concern the size of the corallites and number
of septa, development of the septal margin
ornamentation, more or less exsert character
of the septa above the common wall, and the
size of the columella. The series of specimens
examined; however, is rather homogeneous, and
no significant variations among the 3 geographic
locations where the specimens were collected
were noted.
Molecular phylogenetic analyses
Fifty-two variable sites containing 50
parsimoniously informative sites were found in 16
sequences of the Siderastrea-Pseudosiderastrea
group examined. Pairwise genetic distances
were calculated under the setting of the Kimura
2-parameter model, and averaged 0.03 between
the Pseudosiderastrea and Siderastrea groups.
The overall distance within Siderastrea was
0.012, while that within Pseudosiderastrea was
only 0.003. Most species of Siderastrea occur in
the Atlantic Ocean (Caribbean and Brazil) (Budd
et al. 1994), and their pairwise genetic distance
was smaller than that found in the single Indo-
Pacific species S. savignyana (Atlantic group:
0.00037; S. savignyana: 0.00086). Within the
genus Pseudosiderastrea, the genetic distance
between P. tayamai and P. formosa sp. nov.
was 0.004, which is much higher than that of
species comparisons among Atlantic species of
Siderastrea.
Porites porites, Dendrophyllia sp., and
Stephanocoenia michelinii were used as outgroups
in the phylogenetic analysis. The resulting ML
and BI topologies were similar for the Siderastrea
and Pseudosiderastrea groups (Patristic distance
correlation = 0.95) (Fourment et al. 2006) (Fig.
6), and consisted of 4 clades: clade I included
Siderastrea species from the A tl an ti c Oce an
group (Forsman et al. 2005); clade II included all
specimens of S. savignyana collected from the
Indian Ocean; and clades III and IV contained all
specimens of Pseudosiderastrea. All clades had
strong statistical support (≥ 75%) in both the ML
(bootstrap) and BI (posterior probability) analyses.
DISCUSSION
The genus Pseudosiderastrea was estab-
lished by Yabe and Sugiyama (1935) for
the species P. tayamai from Aru Is., but
was subsequently treated as a subgenus of
Anomastraea (Vaughan and Wells 1943, Wells
1956). However, more recently it was again
treated as a genus in its full right (Veron and
Pichon 1979). In the original description, Yabe
Fig. 6. Phylogenetic analyses based on Bayesian inference and maximum likelihood of the partial mitochondrial cytochrome (Cyt) b
gene. Ten Siderastrea and 6 Pseudosiderastrea specimens were included and separated into 4 clades, including clades I and II for
Siderastrea and clades III and IV for Pseudosiderastrea. Stephanocoenia, Dendrophyllia, and Porites were chosen as outgroups.
Sgl_3108 Siderastrea glynni
Sra_2832 Siderastrea radians
Sra_2834 Siderastrea radians
Ssi_2831 Siderastrea siderea
Ssi_2832 Siderastrea siderea
Sst_2844 Siderastrea stellata
Sst_2846 Siderastrea stellata
Ssa_3155 Siderastrea savignyana
Ssa_3153 Siderastrea savignyana
Ssa_3154 Siderastrea savignyana
Psp_5349
Psp_ 5350
Psp_5353
Pta_5348 Pseudosiderastrea tayamai
Pta_2196 Pseudosiderastrea tayamai
Pta_5341 Pseudosiderastrea tayamai
AB441313 Stephanocoenia michelinii
AB441324 Dendrophyllia sp.
NC_008166 Porites porites
77/71
75/96
100/100
99/99
99/100
-/100
75/98
99/100
77/96 Pseudosiderastrea from Wanlitung
Outgroup
I
II
III
IV
Pichon et al. – Pseudosiderastrea formosa in Taiwan96
and Sugiyama (1935) remarked that P. tayamai
was close to the Atlantic S. radians and S.
siderea, which were the only Siderastrea species
available for them to compare. According to Yabe
and Sugiyama (1935), the major morphological
differences between these 2 genera were the
absence of septal perforations and the reduced
development of synapticulae in Pseudosiderastrea.
They also remarked that Pseudosiderastrea has
similar features to Anomastraea, the latter differing
by the presence of perforated septa and septal
dentation increasing in size towards the center
of the calice, with a tendency to form pali-like
structures.
The relative regularity of the corallite shape
within each colony of P. formosa sp. nov., in
the material examined, is reminiscent of S .
savignyana Milne Edwards & Haime (1849), which
is particularly widespread in the western Indian
Ocean (Fig. 7). By comparison, Pseudosiderastrea
specimens most often display a more-irregular
corallite shape, although occasionally some
regularly shaped corallites were noted (see Veron
and Pichon 1979, fig. 145). However, the solid
walls and septa, and the almost total absence of
synapticulae and synapticular rings leave no doubt
as to the generic position of our specimens, which
clearly belong to the genus Pseudosiderastrea,
for which they represent a new species.
Pseudosiderastrea formosa sp. nov. differs from P.
tayamai (Fig. 8) in having more-regularly-shaped
corallites, a smaller number of septa which are
slightly wedge-shaped and seldom fused at their
inner margin, coarser septal ornamentation, and a
very developed, highly conspicuous columella.
Molecular phylogenetic afnities
The Pseudosiderastrea spp. clade grouped
as a sister group to Siderastrea spp. (Fig. 6),
and as such, the monophyletic status of both
genera is confirmed. Using cytochrome oxidase
subunit 1 (COI) and Cyt b, Fukami et al. (2008)
reexamined the familial and generic relationships
of many scleractinian representatives, and
found that the Pacific “Siderastrea” (samples
collected from Wanlitung, Taiwan), which in fact
belonged to P. formosa sp. nov., and the Atlantic
Siderastrea specimens were a monophyletic
group. The monophyletic origins of Siderastrea
and Pseudosiderastrea were also conrmed by the
COI phylogeny of scleractinian corals proposed
by Kitahara et al. (2010). Those results clearly
indicated that Pseudosiderastrea and Siderastrea
have a very recent common ancestor.
Following morphological observations
provided herein, the Cyt b phylogeny indicated
that P. formosa sp. nov. and P. tayamai belong to
the same genus based on monophyletic support
of Cyt b phylogeny (clades III and IV, Fig. 6). The
genetic distance of Cyt b between P. formosa sp.
nov. and P. tayamai (p = 0.004) was relatively
larger than the interspecific distance for species
in the Atlantic clade (clade I), which contains the
most recently diverged Siderastrea species from
the Atlantic Ocean, S. glynni (p = 0-0.0006 for Cyt
b in this study) (Forsman et al. 2005). The smaller
distance we showed in Pseudosiderastrea is due
to the slower evolution of mitochondrial DNA in
anthozoans (Shearer et al. 2002). Comparing our
results with others using the same marker, the
Fig. 7. Siderastrea savignyana. Specimen from Kuwait clearly
showing the well-developed synapticular rings. (Photo: P.
Harrison)
Fig. 8. Pseudosiderastrea tayamai (MTQ G 64630) from
Kaohsiung, Taiwan, showing irregularly shaped and sized
corallites and frequent fusion of the predominantly lamellar
septa.
97Zoological Studies 51(1): 93-98 (2012)
genetic distance between P. formosa sp. nov. and P.
tayamai was equivalent to the interspecic distance
of Cyt b found in Acropora (p = 0.004 between P.
formosa sp. nov. and P. tayamai, p = 0.0039 in
interspecic comparisons of Acropora; Chen et al.
2008). The genetic distance between P. formosa
sp. nov. and P. tayamai implies that the genetic
divergence of these 2 species is sufciently large
to support P. formosa sp. nov. being a different
species from P. tayamai.
Acknowledgments: The authors acknowledge
the assistance of Dr. P. Muir (S.E.M. and pictures)
and Ms. B. Done (collection manager), both of
the Museum of Tropical Queensland, Townsville,
Australia. We are also grateful to Dr. H. Fukami
and Dr. Z. Forsman for gifts of Siderastrea DNA
samples from Panama, to Dr. D. Obura for
providing material from Kenya, his input in the
early stages of the project, and comments on the
manuscript, to Dr. P. Harrison for permission to
reproduce an illustration of S. savignyana, and
to 2 anonymous reviewers, Dr. D. Miller, and
members of the Coral Reef Evolutionary Ecology
and Genetics (CREEG) laboratory, Biodiversity
Research Center, Academia Sinica (BRCAS) for
constructive comments. A collection permit was
granted by the Kenting National Park, Ministry
of the Interior, Pingtung, Taiwan. This study was
made possible by grants from Academia Sinica
and the National Science Council, Taiwan to C.A.C.
This is the CREEG-BRCAS contribution no. 72.
REFERENCES
Blainville HM de. 1830. “Zoophytes”. In Dictionnaire des
Sciences Naturelles. Paris, 60, pp. 295-364.
Budd AF, HM Guzman. 1994. Siderastrea glynni, a new
species of scleractinian coral (Cnidaria, Anthozoa) from
the eastern Pacic. P. Biol. Soc. Wash. 107: 591-599.
Chen IP, CY Tang, CY Chiou, JH Hsu, NV Wei, CC Wallace
et al. 2008. Comparative analyses of coding and
noncoding DNA regions indicate that Acropora (Anthozoa:
Scleractina) possesses a similar evolutionary tempo of
nuclear vs. mitochondrial genomes as in plants. Mar.
Biotechnol. (NY) 11: 141-152.
Dai C, S Horng. 2008. Scleractinia fauna of Taiwan. I. The
complex group. Taipei, Taiwan: National Taiwan Univ.,
172 pp.
Forsman ZH, HM Guzman, CA Chen, GE Fox, GM Wellington.
2005. An ITS region phylogeny of Siderastrea (Cnidaria:
Anthozoa): Is Siderastrea glynni endangered or intro-
duced? Coral Reefs 24: 343-347.
Fourment M, MJ Gibbs. 2006. Patristic: a program for
calculating patristic distances and graphically comparing
the components of genetic change. BMC Evol. Biol. 6: 1.
Fukami H, A Budd, G Paulay, A Sole-Cava, C Chen, K Iwao, N
Knowlton. 2004. Conventional taxonomy obscures deep
divergence between Pacific and Atlantic corals. Nature
427: 832-835.
Fukami H, CA Chen, AF Budd, A Collins, C Wallace, YY Chuang
et al. 2008. Mitochondrial and nuclear genes suggest
that stony corals are monophyletic but most families of
stony corals are not (order Scleractinia, class Anthozoa,
phylum Cnidaria). PloS One 3: e3222.
Guindon S, JF Dufayard, V Lefort, M Anisimova, W Hordijk,
O Ga scuel. 2 010 . New algo rithms and m ethods to
estimate maximum-likelihood phylogenies: assessing the
performance of phyml 3.0. Syst. Biol. 59: 307-321.
Kitahara MV, SD Cairns, J Stolarski, D Blair, DJ Miller. 2010. A
comprehensive phylogenetic analysis of the scleractinia
(Cnidaria, Anthozoa) based on mitochondrial COI
sequence data. PLoS One 5: e11490.
Milne Edwards H, J Haime. 1849. Recherches sur les poly-
piers. 4eme mémoire: monographie des astréides (suite).
Ann. Sci. Nat. Paris, 3: 95-197.
Posada D, KA Crandall. 1998. Modeltest: testing the model of
DNA substitution. Bioinformatics 14: 817-818.
Ronquist F, JP Huelsenbeck. 2003. MrBayes 3: Bayesian
phylogenetic inference under mixed models. Bioinfor-
matics 19: 1572-1574.
Shearer TL, MJH Van Oppen, SL Romano, G Worheide. 2002.
Sl ow mit ochon dri al DNA seq uen ce evo lut ion in the
anthozoa (Cnidaria). Mol. Ecol. 11: 2475-2487.
Tamura K, D Peterson, N Peterson, G Stecher, M Nei, S Kumar.
2011. MEGA5: Molecular Evolutionary Genetics Analysis
using maximum likelihood, evolutionary distance, and
maximum parsimony methods. Mol. Biol. Evol. (In press).
Vaughan TW, JW Wells. 1943. Revision of the suborders,
families and genera of the Scleractinia. New York:
Geological Society of America Special Paper 44, 363 pp.,
51 plates.
Veron JEN, M Pichon. 1979. Scleractinia of eastern Australia.
Part III Families Agariciidae, Siderastreidae, Fungiidae,
Oculinidae, Merulinidae, Mussidae, Pectiniidae,
Caryophylliidae, Dendrophylliidae. Australia: Australian
Institute of Marine Science Monograph Series no. 4, 422
pp.
Wells JW. 1956. “Scleractinia.” In RC Moore, ed. Treatise
on invertebrate paleontology. Part F: Coelenterata.
Geological Society of America, Kansas: Univ. Kansas
Press, pp. F328-F440.
Yabe H, T Sugiyama. 1935. A new living coral,
Pseudosiderastrea tayamai, from Dobo in Wamar, Aru
Islands. Proc. Imp. Acad. Tokyo 11: 373-375.
Pichon et al. – Pseudosiderastrea formosa in Taiwan98
