A new Korean red algal species, Haraldiophyllum...
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Algae 2011, 26(3): 211-219http://dx.doi.org/10.4490/algae.2011.26.3.211
Open Access
Research Article
Copyright © The Korean Society of Phycology 211 http://e-algae.kr pISSN: 1226-2617 eISSN: 2093-0860
A new Korean red algal species, Haraldiophyllum udoensis sp. nov. (Delesseriaceae, Rhodophyta)
Myung Sook Kim1,* and Jeong Chan Kang1
1Department of Biology, Jeju National University, Jeju 690-756, Korea
The genus Haraldiophyllum comprises seven species worldwide. Six of these are endemics with limited distributions,
whereas the type species H. bonnemaisonii has been reported from the Atlantic Ocean. In Korea, H. bonnemaisonii has
been previously recorded from the southern coast. During a red algal collection at Udo, Jeju Island, Korea, we found a
potentially undescribed Haraldiophyllum species and analyzed its morphology and rbcL sequences. Herein we describe
a new species, H. udoensis sp. nov., and compare our Udo specimen to similar congeners. This new species is charac-
terized by one or several elliptical blades on a short cylindrical stipe with fibrous roots, blades that are monostromatic
except at the base and on reproductive structures, a lack of network and microscopic veins, entire margins, lack of pro-
liferations, growth through many marginal initials, and two distinct tetrasporangia layers. A phylogenetic rbcL sequence
analysis demonstrated H. udoensis was distinct from the United Kingdom’s H. bonnemaisonii, as well as from other
species. Morphological and sequence data indicated a previous misidentification of H. udoensis as the type species H.
bonnemaisonii. Based on maximum likelihood analysis, Myriogramme formed a sister clade with H. udoensis, with rela-
tively low bootstrap support.
Key Words: Delesseriaceae; Haraldiophyllum udoensis sp. nov.; morphology; rbcL; Rhodophyta; taxonomy
INTRODUCTION
Zinova (1981) established the genus Haraldiophyl-
lum based upon Myriogramme bonnemaisonii Kylin
(1924), from Atlantic Europe. The Haraldiophyllum type
species, H. bonnemaisonii, is characterized by a broad,
erect, foliose thallus with a cylindrical stipe, the absence
of a midrib and veins, monostromatic and polystromatic
blades, and tetrasporangia sori formed upon both sides
of the blade (Maggs and Hommersand 1993). To date,
seven species of Haraldiophyllum have been recognized
worldwide (Guiry and Guiry 2011), as follows: H. bonne-
maisonii (Kylin) A. D. Zinova (1981); H. crispatum (J. D.
Hooker & Harvey) Lin, Hommersand & Nelson (2007); H.
erosum (Harvey) A. J. K. Millar & J. M. Huisman (1996); H.
infossum A. J. K. Millar (1994); H. mirabile (Kylin) Zino-
va (1981); H. nottii (Norris & M. J. Wynne) M. J. Wynne
(1983); and H. sinuosum (A. H. S. Lucas) A. J. K. Millar
(1990).
The type species H. bonnemaisonii is typically dis-
tributed in the Atlantic Ocean (Maggs and Hommersand
1993, Hardy and Guiry 2003, John et al. 2004, Barbara et
al. 2005, Lin et al. 2007). The other six species, however,
are endemics with limited distributions. H. mirabile and
H. nottii live only along the western coast of North Amer-
ica (Wynne 1983), H. sinuosum and H. infossum occur
along the eastern coast of Australia and in the southwest-
ern Pacific (Millar 1990, 1994), H. erosum inhabits west-
Received May 15, 2011, Accepted August 13, 2011
*Corresponding Author
E-mail: [email protected]: +82-64-754-3523, Fax: +82-64-756-3541
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://cre-ativecommons.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.
Algae 2011, 26(3): 211-219
http://dx.doi.org/10.4490/algae.2011.26.3.211 212
microscope (ECLIPSE 80i; Nikon) and then imported all
images into PhotoShop 7.0.1 (Adobe Systems, San Jose,
CA, USA) for plate assembly.
Molecular study
We air-dried the piece of cleaned thallus and desic-
cated it using silica gel for the DNA extraction. Using the
DNeasy Plant Mini Kit (Qiagen, Hilden, Germany), and
following the manufacturer’s instructions, we ground the
silica gel-dried thallus in liquid nitrogen and extracted
the total genomic DNA. Extracts were dissolved in 200
mL of distilled water. For amplification and sequencing
reactions of genes, we employed the specific primer pairs
rbcLF7-rbcLR753 and rbcLF645-rbcS start (Lin et al. 2001,
Gavio and Fredericq 2002). For all polymerase chain re-
action (PCR) amplifications, we used Swift MaxPro ther-
mal cyclers (ESCO, Singapore) with an AccuPower PCR
PreMix (Bioneer, Daejeon, Korea). The PCR comprised
an initial denaturation step, at 94°C for 4 min, 35 cycles
1 min at 94°C, 1 min at 50°C, 2 min at 72°C, and a final 7
min extension cycle, at 72°C. To purify the PCR products,
we used an AccuPrep PCR Purification Kit (Bioneer) and
then sequenced them commercially (Macrogen, Seoul,
Korea). Both electropherogram outputs from each sam-
ple were edited using the program Chromas version 1.45.
Using BioEdit (Hall 1999), we collated the total se-
quences and then aligned them visually. No alignments
posed problems, as we observed no gaps. The outgroups
we used were Augophyllum delicatum (AF257400) and
Nitophyllum punctatum (AF257402). To confirm the
taxonomic position of a potentially undescribed species
of Haraldiophyllum from Udo, we conducted a maxi-
mum likelihood (ML) analysis, using PAUP 4.0 (Swofford
2002). We determined the best model for the individual
data sets using Modeltest 3.4 software (Posada and Cran-
dall 1998). The best model was a general time reversible
(GTR) evolutionary model with gamma correction for
among-site variation (Γ) and proportion of invariable
sites (I). To estimate ML trees, we used a heuristic search
with 100 random addition sequence replicates and tree
bisection and reconnection (TBR) branch swapping. To
test the node stability, we performed bootstrap analyses
with 1,000 replicated ML searches, using the same pro-
gram and settings.
RESULTS
Haraldiophyllum udoensis M. S. Kim et J. C. Kang, sp. nov.
ern Australia (Millar and Huisman 1996), and H. crispa-
tum occurs in Australia and New Zealand (Lin et al. 2007).
In Asia, Nam and Kim (1996) initially identified H.
bonnemaisonii based on the specimen collected from
Hadong and Kwangyang along the south coast of Korea.
They described the Korean specimens as characteristi-
cally having monostromatic blades (except for the basal
portion), a procarp with one carpogonial branch and two
sterile groups, and tetrasporangial sori on both surfaces
of the blades (Nam and Kim 1996). They also noted that
Korean specimens reached 10-20 cm in height and con-
sisted of flabellate blades on a prominent stipe; however,
Korean H. bonnemaisonii exhibits some differences when
compared to specimens from the British Isles (Maggs and
Hommersand 1993), having deeply cleft and non-dichot-
omously lobed blades.
Because the marine algal flora of Udo, Jeju Island, Ko-
rea remains very poorly documented, we have collected
extensively there to improve our knowledge of red algal
biodiversity. The red algae within the Udo marine forests
consist of a turf community growing around and between
digitate Ecklonia cava holdfasts. While collecting algae
from Udo, we found a potentially undescribed species of
Haraldiophyllum that belonged to the tribe Myriogram-
meae. A careful examination revealed that this alga rep-
resented a new species in the Delesseriaceae. Here, we
report on this newly discovered species based on its veg-
etative morphology and rbcL gene sequences, and dis-
cuss its taxonomic status among the species of the genus.
To elucidate the phylogenetic relationships of the taxa
from Udo, Jeju Island, we downloaded the rbcL sequence
data of four Haraldiophyllum species from GenBank.
MATERIALS AND METHODS
Morphology
For our morphological study, we collected the speci-
men on a scuba dive, and preserved them in 4% formalin
/ seawater, with the exception of a small piece of thallus
to be used for molecular study. The voucher specimen
was deposited in the herbarium of Jeju National Uni-
versity (JNUB), Jeju, Korea. We sectioned the preserved
specimen by hand or using a freezing microtome NK-
101-II (Nippon Optical Works Co. Ltd., Tokyo, Japan).
The sectioned preparations were stained with 1% aniline
blue acidified with 1% HCl and mounted in 25-30% Karo
syrup. To photograph the specimen, we used a Digital
Sight DS-Fi1 camera (Nikon, Tokyo, Japan) attached to a
Kim & Kang Haraldiophyllum udoensis sp. nov.
213 http://e-algae.kr
cells divide obliquely; growth is marginal and diffuse,
without distinct apical cells; tetrasporangia occur in el-
liptical sori 2 mm long on median, formed simultaneous-
ly on both surfaces of the blade; mature tetrasporangia
forming two layers, spherical, tetrahedrally divided, to
80-100 µm in diameter.
Holotype. JNU-MSK30601HU, tetrasporophyte, col-
lected on June 14, 2009 (Fig. 1A).
Type locality. Haumokdong, Udo, Jeju Island, Korea
(33°30´21˝ N, 126°56´09˝ E)
Korean name. 우도민엷은잎
Distribution. Known to occur on the south coast (Nam
and Kim 1996) and at Udo, Jeju Island, in this study.
Habitat. We collected Haraldiophyllum udoensis at 12
m in the sublittoral zone of Udo, Jeju Island, Korea. The
thallus grew as an epilithic blade on a stone covered with
Lithophyllum sp. in habitats exposed to strong currents.
Among the plants collected along the south coast of Ko-
Description. Thalli ellipticus, 22 cm longis et 6 cm la-
tis, consisto singuli aut aliquot laminae affixus per fibro-
sus hapteron; lamina in brevis cylindricus stipitis, 2-3 cm
longis et 1 mm crassus; lamina tenuis, monostromaticis
super, tristromaticis in reproductivus area et polystro-
maticis versus basis, microscopicus vena absens, integer
margo et marginalis cellulae divisus oblique; crescens
marginalis et diffuses, sine distinctus cullula apicalis;
tetrasporangia eferens in ellipticus sori 2 mm longis in
medianas factus simultaneous in superficiebus amba-
bus lamina; tetrasporangia matura factus bistromatica,
spherical, tetrahedraliter divisa, ad 80-100 µm diametro.
Thallus elliptical, 22 cm long and 6 cm wide, consisting
of one or several blades attached by a fibrous holdfast;
blade on a short, cylindrical stipe, 2-3 cm long and 1 mm
thick; blade thin, monostromatic above, tristromatic in
reproductive areas, and polystromatic toward the base,
microscopic veins absent; entire margins and marginal
Fig. 1. Haraldiophyllum udoensis sp. nov. (A) Holotype (JNU-MSK 30601HU, tetrasporophyte) specimen deposited in the Herbarium of Jeju Na-tional University (JNUB), Jeju, Korea. (B & C) Enlarged photos of Fig. 1A to show tetrasporangial sori (B) and the blade attached to a stone (C). Scale bars represent: A, 5 cm; B & C, 3 cm.
A B
C
Algae 2011, 26(3): 211-219
http://dx.doi.org/10.4490/algae.2011.26.3.211 214
terspecific p distance) values for the rbcL region within
Haraldiophyllum ranged from 31 bp (2.7%) between H.
mirabile from the United States and Haraldiophyllum
sp. from Chile to 87 bp (6.7%) between H. bonnemaisonii
and Haraldiophyllum sp. from Chile. The most-related
genus, Myriogramme, differed by 109-142 bp (8.3-11%)
from H. udoensis and by 103-169 bp (8-13%) from the rest
of the genera we tested in the present study.
In the phylogenetic tree from rbcL, the new species
formed an independent clade with strong support (99%
for ML) and a sister group with H. mirabile from the Unit-
ed States and Haraldiophyllum sp. from Chile (Fig. 4).
The ML analysis of rbcL data indicated that H. udoensis
showed clear separation from H. bonnemaisonii and H.
crispatum from New Zealand. The ML tree showed two
groups within Haraldiophyllum, and the bootstrap sup-
ports were quite strong (100% and 91%). The first clade
included H. udoensis as the new species, H. mirabile and
Haraldiophyllum sp., and the second clade contained H.
crispatum and H. bonnemaisonii. The genus Haraldio-
phyllum monophyly had definitive bootstrap support
(100%). The genus Myriogramme formed a sister rela-
tionship with the genus Haraldiophyllum.
DISCUSSION
Haraldiophyllum udoensis is newly described from
Udo, Jeju Island, Korea, based on our detailed morpho-
logical observations and molecular analysis. This new
species is characterized by the following features: 1) one
or several elliptical blades on a short, cylindrical stipe
with fibrous roots; 2) monostromatic blades, except at the
base and on reproductive structures; 3) a lack of network
and microscopic veins; 4) entire margins with a lack of
proliferations; 5) growth by means of many marginal ini-
tials; and 6) an arrangement of two distinct tetrasporan-
gia layers. Molecular phylogenetic analysis based on rbcL
sequences demonstrated H. udoensis’s distinctness from
its congeners, and separated it clearly from the European
H. bonnemaisonii. The genus Haraldiophyllum contains
two clusters of species, one from the United Kingdom
and New Zealand and the other occurring along the Pa-
cific Coasts of Korea, the United States, and Chile. Our
molecular analysis produced similar results to those Lin
et al. (2007) reported. The new species is epilithic in the
sublittoral zone at depths up to 12 m. It was previously
identified in Korea as H. bonnemaisonii (Nam and Kim
1996). Although H. udoensis closely resembles the type
species of Haraldiophyllum (H. bonnemaisonii from the
rea by Nam and Kim (1996) and by us for this study, tetra-
sporophytes were found from March to September. Nam
and Kim (1996) collected male and female gametophytes
in July and September, respectively, but we collected no
gametophytes for this study.
Etymology. We have chosen the specific epithet to
represent the name of the islet collection site-Udo, Jeju
Island.
Morphology. The plant is a greenish red-brown, 22 cm
high, 6 cm broad, foliose, and erect on a cylindrical stipe
up to 2-3 cm long and 1 mm thick (Fig. 1A). The thallus
consists of one or several blades, attached by a small fi-
brous holdfast, that lack midrib and microscopic veins
(Fig. 1B & C). The blade is thin and monostromatic above,
becoming tristromatic in reproductive areas and polys-
tromatic toward the base with evanescent midribs (Fig.
2A-D), and increasing in thickness from 35 µm near the
apices to 100 µm basally. The blade comprises cells that
are elongate-polygonal in surface view (Fig. 3A) and 45-
70 µm long × 15-45 µm wide, linked by secondary pit con-
nections that increase in abundance in the polystromatic
regions. The blade has entire margins, and marginal cells
divide anticlinally or obliquely, growing marginal meri-
stems without distinct apical cells (Fig. 3A).
Tetrasporangia are produced in small, numerous, cir-
cular to elliptical sori, formed randomly on both sides
of the blade, and scattered throughout the blade except
along the margins and the lowermost parts. Tetrasporan-
gial sori are 2 mm long × 0.6 mm wide, and protrude on
either side of the blade, approximately 200 µm thick (Fig.
3B). In the transverse section of the sori, the tetrasporan-
gia appear in two layers between both surface cells (Fig.
3C). The tetrasporangia are produced from inner corti-
cal cells but occasionally also from primary cells. Mature
tetrasporangia are spherical, 80-100 µm in diameter, and
divided tetrahedrally (Fig. 3D).
Molecular analysis of rbcL. To align the five Haraldio-
phyllum species with putative relative genera in the fami-
ly Delesseriaceae, we used a 1,303 nucleotide (nt) portion
of rbcL gene and two outgroups. Variable sites occurred
at 464 positions (35.6%), and 350 positions (26.9%) were
parsimoniously informative. In the ML analysis, we es-
timated the –ln likelihood score as 7,899.6647 under
the GTR + Г + I model. The sequences differed by up to
a 72 bp (5.5%) pairwise distance between H. udoensis
from Korea and H. bonnemaisonii from the United King-
dom. The new species differed from H. crispatum from
New Zealand, H. mirabile from the United States, and
Haraldiophyllum sp. from Chile by 64, 32, and 39 bp,
respectively. The uncorrected sequence divergence (in-
Kim & Kang Haraldiophyllum udoensis sp. nov.
215 http://e-algae.kr
Fig. 2. Haraldiophyllum udoensis sp. nov. (A-D) Transverse section of the blade, which is monostromatic (A & B), tristromatic (C), and polystro-matic toward the base (D). Scale bars represent: A, 50 μm; B & C, 30 μm; D, 100 μm.
A
C
D
B
Fig. 3. Haraldiophyllum udoensis sp. nov. (A) Surface view of blade showing elongate-polygonal cells. (B) Small elliptical tetrasporangial sori. (C) Transverse section of sori forming two tetrasporangia layers. (D) Mature tetrasporangia, divided tetrahedrally. Scale bars represent: A & D, 30 μm; B & C, 50 μm.
A
C
D
B
Algae 2011, 26(3): 211-219
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nottii are 2-7 cm smaller than other species (Millar 1994,
Womersley 2003, Lin et al. 2007). In particular, H. infos-
sum from Australia differs from all other species in the
genus due to its diminutive size (up to 1.9 cm). Haraldio-
phyllum sinuosum is by far the largest of the genus with
plants reaching lengths of 20-35 cm. Haraldiophyllum
erosum and H. mirabile are of medium size at around 10
cm (Millar and Huisman 1996), but the new species H.
udoensis is approximately 20 cm in length. The shapes of
the base and margins have been demonstrated as valid
characteristics for delineating some species of Haral-
diophyllum, as for example Millar and Huisman (1996)
showed changes of the Haraldiophyllum species’ mar-
gins display a continuum from species with entire mar-
gins to those with fringed margins. Most of Haraldiophyl-
lum species including the new species H. udoensis have
entire or dentate margins, except for two: H. erosum and
H. infossum (Millar 1994). According to Millar and Huis-
man (1996), H. erosum from western Australia has an
unusual marginal fringe with numerous multicellular
British Isles), H. bonnemaisonii has a distinct thallus that
divides regularly and dichotomously into overlapping
lobes, frequently proliferating on the blade and forming
a single tetrasporangia layer in a zigzag manner (Maggs
and Hommersand 1993, Lin et al. 2007). In addition, the
reproductive structure in H. udoensis is larger; the cysto-
carp diameter of > 700 µm contrasts with the < 600 µm in
H. bonnemaisonii, and tetrasporangia in H. udoensis are
> 80 µm in diameter, as opposed to < 70 µm in H. bonne-
maisonii (Table 1).
In recognizing the species of Haraldiophyllum, which
currently contains seven species, the vegetative char-
acteristics are viewed as important diagnostic features,
such as whether thallus size is diminutive, whether shape
of the base and margins are dentate or entire, whether
the branching pattern is dichotomous, whether the
lobed blade is deeply cleft, and the presence or absence
of stipes (Table 1). Thallus size is useful for identifying
species of Haraldiophyllum; H. bonnemaisonii and H.
crispatum reach 20-25 cm, whereas H. infossum and H.
Fig. 4. Phylogenetic tree for Haraldiophyllum and relatives, derived from maximum likelihood using plastid-encoded rbcL sequence data. The bootstrap values shown above branches are from bootstrap analyses employing 1,000 replicated maximum likelihood searches.
Kim & Kang Haraldiophyllum udoensis sp. nov.
217 http://e-algae.kr
Tabl
e 1.
Mor
phol
ogic
al c
ompa
rison
s of
spe
cies
in th
e ge
nus
Har
aldi
ophy
llum
H. u
doe
nsi
ssp
. nov
.H
. bon
nem
aiso
nii
(K
ylin
) A. D
. Z
inov
a
H. c
risp
atu
m (
J. D
. H
oo
ker
& H
arve
y)
Lin
, Ho
mm
ersa
nd
&
Nel
son
H. e
rosu
m
(Har
vey)
A. J
. K
. Mil
lar
& J
. M.
Hu
ism
an
H. i
nfo
ssu
m A
. J. K
. M
illa
rH
. mir
abi
le (K
ylin
) Z
inov
aH
. not
tii (
No
rris
&
M. J
. Wyn
ne)
M. J
. W
ynn
e
H. s
inu
osu
m
(A. H
. S. L
uca
s) A
. J.
K. M
illa
r
Loca
lity
Ud
o, Je
ju Is
lan
d,
Ko
rea
Shet
lan
d Is
lan
d,
UK
; Ire
lan
dC
amp
bel
l Isl
and
, N
ew Z
eala
nd
Gar
den
Isla
nd,
W
este
rn A
ustr
alia
New
So
uth
Wal
es,
Au
stra
liaA
lask
a, U
SAW
ash
ingt
on
, USA
New
So
uth
Wal
es,
Au
stra
lia
Hab
itat
12 m
in s
ub
litto
ral
zon
eE
xtre
me
low
wat
er
to 2
1 m
24 m
, dre
dge
d a
nd
d
rift
Dre
dge
d fr
om 4
1 m
, dri
ft, e
pip
hyt
ic1-
20 m
, tu
rf c
om
-m
un
ity
-
Shal
low
to d
eep
w
ater
-
Size
(h
eigh
t × w
idth
, cm
)22
× 6
15
× 2
0 25
13
1.
98-
10
2-7
20-3
5
Hab
itO
ne
to s
ever
al
ellip
tica
l bla
de
wit
h fi
bro
us
roo
ts, n
ot d
ich
ot-
om
ou
sly
bla
de
On
e to
sev
eral
fan
-sh
aped
bla
de,
d
ich
oto
mo
usl
y d
ivid
ed
Del
icat
e to
ro
bu
st,
sin
gle
or
seve
ral
bla
des
Dic
ho
tom
ou
sly
or
irre
gula
rly
lob
edO
vate
to e
lon
gate
, ov
erla
p in
im-
bri
cate
arr
ange
-m
ent,
cre
epin
g
-D
ich
oto
mo
usl
y b
ran
chin
g-
Bla
de
Th
in, m
emb
ra-
no
us,
mo
no
-st
rom
atic
an
d
po
lyst
rom
atic
Mo
no
stro
mat
ic
wh
en y
ou
ng,
in
crea
sin
g th
ick-
nes
s
Exc
eed
ingl
y va
ri-
able
in s
hap
e,
elo
nga
te o
r fa
n-
shap
ed, d
ivid
ed
Irre
gula
rly
shap
ed
ho
les
in d
ivid
e su
rfac
es, m
on
o-
stro
mat
ic
Mo
no
stro
mat
ic,
irre
gula
rly
bra
nch
ed b
lad
es
aris
ing
fro
m a
st
olo
nif
ero
us
bas
e
Ro
un
dis
h to
d
eep
ly o
r cl
eft
Th
in, f
ork
ed, fl
at-
bra
nch
ed, m
on
o-
stro
mat
ic
Sho
rt, b
lun
t lo
bes
Stip
eSh
ort
cyl
ind
rica
lC
ylin
dri
cal
Cyl
ind
rica
l Sh
ort
dis
tan
ce-
Less
pro
min
ent
Sho
rt, n
arro
wSh
ort
(6-
7 m
m)
Vein
sA
bse
nt
Ab
sen
tA
bse
nt
Ab
sen
tA
bse
nt
-A
bse
nt
-
Mar
gin
sE
nti
reE
nti
re o
r d
enta
teSm
oo
th o
r cr
isp
ed, e
nti
re o
r d
enti
cula
te
Frin
ged
by
mu
l-ti
cellu
lar
pro
-ce
sses
Pro
min
entl
y d
en-
tate
-Sm
oo
th, e
nti
re, a
fe
w m
inu
te te
eth
En
tire
Pro
lifer
atio
ns
Ab
sen
tP
rese
nt
Som
etim
es p
rese
nt
--
--
-
Cle
ft b
lad
eA
bse
nt o
r d
eep
ly
clef
tSo
met
imes
to
bas
eD
isse
cted
irre
gu-
larl
y in
to b
ran
ch-
--
-A
bse
nt
Gro
wth
Mar
gin
al g
row
thD
iffu
se in
mar
-gi
nal
mer
iste
ms
Mar
gin
al g
row
thM
eris
tem
atic
re
gio
nM
argi
nal
init
ials
-M
argi
nal
wit
h in
ter-
cala
ry d
ivis
ion
s-
Pro
carp
Bo
th s
urf
aces
of
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Algae 2011, 26(3): 211-219
http://dx.doi.org/10.4490/algae.2011.26.3.211 218
group cutting off from the supporting cell prior to the
initial carpogonial branch. The production of the second
sterile cell group delays until after carpogonial branch
formation. The same sequence occurs in H. crispatum, H.
erosum, and H. nottii, but that of H. infossum differs in
forming the two sterile cell groups before initiating the
carpogonial branch (Millar 1994). Millar and Huisman
(1996), therefore, concluded these differences appear to
be stable within the Haraldiophyllum species. In the new
species, H. udoensis, procarp formation and cystocarp
development follow a pattern similar to those previous
studies describe (Millar 1994, Millar and Huisman 1996,
Nam and Kim 1996, Lin et al. 2007).
While researchers often use the female reproductive
organ’s structure to distinguish species within the genus
and genera in the family, they have not considered the
number of layers in the tetrasporangia arrangement to
be of any significance in this genus. The type species H.
bonnemaisonii has only a single layer of tetrasporangia
arranged in a zigzag manner, and the same feature oc-
curs in H. crispatum, H. infossum, and H. nottii. However,
two species, H. udoensis sp. nov. and H. erosum, form two
layers of tetrasporangia. To verify the importance of the
number of layers in the tetrasporangia arrangement from
a phylogenetic perspective, further observation and mo-
lecular analysis for all seven species are necessary.
The genus Haraldiophyllum superficially resembles
two genera, Myriogramme and Nitophyllum, although
Haraldiophyllum clearly belongs to the tribe Myrio-
grammeae based on vegetative and reproductive devel-
opmental characteristics (Hommersand and Fredericq
1997). The genus Haraldiophyllum is readily separated
from the genus Myriogramme by carposporangia orga-
nization, which is terminal solitary in Haraldiophyllum
but terminal chains in Myriogramme (Wynne 1983, Lin
et al. 2007). The new species H. udoensis forms a separate
clade from Myriogramme based on molecular analysis of
rbcL sequence data. However, the new species is linked
to Myriogramme as a sister clade with low bootstrap
support in the ML analysis. Haraldiophyllum is distin-
guished from the genus Nitophyllum by the number of
sterile cell groups in the procarps, with two for Haraldio-
phyllum and only one for Nitophyllum, as well as by the
two periaxial cells’ alignment with respect to the frond’s
longitudinal axis, showing a parallel manner in Haral-
diophyllum and a perpendicular manner in Nitophyllum
(Zinova 1981, Wynne 1983). In the molecular phylogenet-
ic tree, the Haraldiophyllum clade is distantly separate
from the Nitophyllum clade including its type species, N.
punctatum from Spain.
processes. They report these marginal processes are of-
ten polysiphonous and divaricately branched, and they
always terminate single apical cell in a transversely-di-
viding (Millar and Huisman 1996). H. infossum often has
a stoloniferous base and prominently dentate blade mar-
gins (Millar 1994).
The branching pattern in relation to the presence or
absence of lobed blades and stipes can also be an impor-
tant distinguishing feature. H. bonnemaisonii comprises
one to several fan-shaped blades, borne on cartilaginous
stipes and dividing dichotomously into overlapping
lobes with rounded apices (Maggs and Hommersand
1993, Lin et al. 2007). H. crispatum has an exceedingly
variable shape, dividing partially into broad lobes with
rounded margins or cleaving into irregular, dichoto-
mously-branched segments with proliferations (Lin et al.
2007). H. erosum’s blades have dichotomous or irregular
lobes and often have irregularly-shaped holes in the sur-
faces (Millar and Huisman 1996). H. infossum has ovated
to elongated individual blades that often overlap in an
imbricate arrangement with the creeping stoloniferous
parts compressed (Millar 1994). H. mirabile from Alaska
has less prominent stipes, and the blades are roundish
to deeply lobed or cleft (Kylin 1925). The blades of H.
nottii are complicated and subdichotomously branched
with lobed, narrow stipes (Norris and Wynne 1968). The
blades of H. sinuosum are generally entire and not deep-
ly cleft but have short, blunt lobes, and the plants have
short stipes that do not persist into the lower blades (Lu-
cas 1913). The new species H. udoensis appears to differ
from other species mostly by its one to several elliptical,
non-lobed blades.
Researchers have documented the diagnostic char-
acteristics of the genus Haraldiophyllum’s reproductive
structures for the female reproductive organs, such as the
procarp, carposporangia, and cystocarp. The procarps
contain two groups of sterile cells, one group of cover cells
and two periaxial cells parallel to the frond’s longitudinal
axis (Millar 1994). The carposporangia are borne singly
and terminally on gonimoblast filaments. The cystocarp
has a fusion cell incorporating gametophytic cells at the
floor of the cystocarpic cavity. Kylin (1925) noted this fea-
ture of the cystocarp fusion cell is probably useful for ge-
neric recognition of the genus Haraldiophyllum. Maggs
and Hommersand (1993) and Millar (1994) also included
this characteristics in their generic circumscription of
Haraldiophyllum, while Millar and Huisman (1996) rec-
ognized two different sequences of cell formation lead-
ing to the procarp’s final structure in Haraldiophyllum.
They observed H. bonnemaisonii has only one sterile cell
Kim & Kang Haraldiophyllum udoensis sp. nov.
219 http://e-algae.kr
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Lin, S. -M., Hommersand, M. H. & Nelson, W. A. 2007. An
assessment of Haraldiophyllum (Delesseriaceae, Rho-
dophyta), including H. crispatum (J. D. Hooker et Har-
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LSU sequence analysis and morphological evidence.
Eur. J. Phycol. 42:391-408.
Lucas, A. H. S. 1913. Notes on Australian marine algae, I.
Proc. Linn. Soc. N. S. W. 38:49-60.
Maggs, C. A. & Hommersand, M. H. 1993. Seaweeds of the
British Isles. Vol. 1. Rhodophyta. Part 3A. Ceramiales.
HMSO, London, 444 pp.
Millar, A. J. K. 1990. Marine red algae of the Coffs Harbour re-
gion, northern New South Wales. Aust. Syst. Bot. 3:293-
593.
Millar, A. J. K. 1994. Haraldiophyllum infossum sp. nov. (De-
lesseriaceae, Rhodophyta), a diminutive turf-forming
red alga from the south-western Pacific. Bot. Mar.
37:125-132.
Millar, A. J. K. & Huisman, J. M. 1996. Haraldiophyllum ero-
sum comb. nov. (Delesseriaceae, Rhodophyta) from
Southern and Western Australia. Aust. Syst. Bot. 9:61-69.
Nam, K. W. & Kim, Y. S. 1996. Haraldiophyllum (Rhodophy-
ta): a Delesseriaceous genus newly recorded in Korea.
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Norris, R. E. & Wynne, M. J. 1968. Notes on marine algae of
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Our ongoing studies of the Delesseriaceae from Jeju Is-
land, Korea have thus far clarified the generic placement
of Haraldiophyllum and led to the recognition of a new
species, H. udoensis. On Jeju Island, many delesseria-
ceous taxa remain that require critical reexamination in
light of recent taxonomic developments within the family.
ACKNOWLEDGEMENTS
This work was supported by a National Research Foun-
dation of Korea grant, funded by the Korean Government
(2011-0003792), and as part of the Survey of Indigenous
Biology of Korea by the National Institute of Biological
Resources (NIBR).
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