http://dx.doi.org/10.4490/algae.2014.29.1.001 Open Access
New red algal species, Erythroglossum hyacinthinum (Delesseriaceae, Rhodophyta) from Korea
Jeong Chan Kang
1and Myung Sook Kim
1,*
1Department of Biology and Research Institute for Basic Sciences, Jeju National University, Jeju 690-756, Korea
The genus Erythroglossum is characterized by Phycodrys-type apical organization, Polyneura-type procarp, and the presence of a midrib. We collected an unidentified Delesseriaceaen species from deep water off the southern coast of the Korean Peninsula. This alga resembles Polyneura japonica in terms of having broadly flattened thalli with a cylindrical stipe, the presence of a midrib and alternative lateral veins. To confirm the taxonomic status of this entity, we compared the morphological features and rbcL sequences among other species of Erythroglossum and P. japonica. As a result, we assigned the new species, Erythroglossum hyacinthinum, to the genus Erythroglossum because of the presence of a mid- rib. This species is characterized by an elliptical to obovate blade with a short cylindrical stipe, a conspicuous midrib and alternate veins, margins with numerous microscopic dentations, di-trichotomously branching, and bulish-violet iri- descence. The phylogeny of rbcL sequences indicates that E. hyacinthinum is definitely a separate entity, but the genera in the tribe Phycodryeae have inconsistent phylogenetic relationships. This is the first study comparing the molecular phylogeny within the genus Erythroglossum.
Key Words: Delesseriaceae; Erythroglossum hyacinthinum sp. nov.; morphology; Phycodryeae; Polyneura; rbcL;
Rhodophyta; taxonomy
INTRODUCTION
The genus Erythroglossum was established by Agardh (1898) based on the vegetative characteristics such as marginal ramifications and angular-rounded cell shape, and he transferred five species of Delesseria (e.g., D.
schousboei J. Agardh, D. balearica J. J. Rodríguez, D. woodii J. Agardh, D. bipinnatifida Montagne, and D. californica J.
Agardh) to the genus Erythroglossum. Later, Kylin (1924) designated E. schousboei (J. Agardh) J. Agardh as the lec- totype species of Erythroglossum, and he established an- other genus Branchioglossum for E. woodii (J. Agardh) J. Agardh (Wynne 1983). Mikami (1979) reported that E.
bipinnatifidum (Montagne) J. Agardh also has the same characteristics as Branchioglossum. Wynne (1983) agreed
with Mikami and made the new combination, Branchio- glossum bipinnatifidum (Montagne) M. J. Wynne. A total of 12 species of the genus Erythroglossum are currently accepted world-wide, including the original three spe- cies, which were first transferred from Delesseria to Eryth- roglossum by Agardh (1898) (Guiry and Guiry 2013).
Kylin (1924) divided the family Delesseriaceae into 11 groups, which were assigned to two subfamilies (e.g., De- lesserioideae and Nitophylloideae) on the basis of veg- etative and reproductive structures. He additionally as- signed the genus Erythroglossum to his Phycodrys group of the subfamily Nitophylloideae. Wynne (2001) proposed 23 tribes under two subfamilies, and he placed the genus
Received October 20, 2013, Accepted January 19, 2014
*
Corresponding Author E-mail: [email protected]Tel: +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-Com- mercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
MATERIALS AND METHODS
Specimens were collected from 15 localities of the Ko- rean coast and two localities of the coast of Japan, from the intertidal and subtidal (Table 1). Field-collected samples were put into an icebox with seawater and an icepack, and transported to the laboratory. The samples for DNA extraction were each assigned a voucher num- ber, and a small part of the thallus was detached for making silica-gel dried tissue samples. The major part of the thallus was made into a pressed specimen and was deposited in the Herbarium of Jeju National University (JNUB), Jeju, and in the National Institute of Biological Resources (NIBR), Incheon, Korea. Samples for morpho- logical observations were fixed in 5% formalin / seawa- ter. Sections for microscopic examination were made by using a freezing microtome (NK-101-II; Nippon Optical Works Co., Ltd., Tokyo, Japan). For staining, 1% aqueous aniline blue acidified with a drop of 1% HCl was used.
The stained sections were mounted in 30% Karo corn syrup. Photomicrographs were taken using a QImaging 1394 camera (QImaging, Surrey, BC, Canada) attached to a BX50 microscope (Olympus, Tokyo, Japan). For compar- ing molecular data, we used 25 Erythroglossum samples containing the new species from Korea, four E. pinnatum samples from Japan, five Polyneura samples from Korea, and 27 rbcL sequence data from the tribe Phycodryeae and Myriogrammeae (used as an outgroup) from previ- ous studies.
For the extraction of total DNA from the silica-gel dried specimens, we used the same methods and prim- ers as Kang and Kim (2013). The polymerase chain reac- tion (PCR) products were purified using the AccuPrep PCR Purification Kit (Bioneer, Daejeon, Korea) and were sequenced commercially (Macrogen, Seoul, Korea). Elec- tropherogram outputs from each sample were edited us- ing Chromas version 1.45 (McCarthy 1996). The total rbcL sequence was organized using the multiple-sequence editing program BioEdit (Hall 1999) and aligned visually (Kang and Kim 2013). None of the alignments posed a problem, as no gaps were observed.
Eleven rbcL sequences of the new species were aligned with 43 sequences of other species belonging to the tribe Phycodryeae, and seven species of Myriogrammeae were used as an outgroup. Maximum likelihood (ML) analyses were produced using RAxML (Stamatakis 2006) with the GTR + Г evolutionary model. We used 200 independent tree inferences by the -# option with default –I (automati- cally optimized SPR rearrangement) and –c (25 distinct rate categories) options of the program to identify the Erythroglossum within the tribe Phycodryeae (Lin et al.
2001a). Recently, Lin et al. (2001a) established the third subfamily as Phycodryoideae, based on molecular analy- sis including large subunit ribosomal DNA and rbcL se- quence data. They assigned the four tribes Phycodryeae, Myriogrammeae, Schizoserideae, and Cryptopleureae to the subfamily Phycodryoideae: however, they did not test any species of Erythroglossum.
In the tribe Phycodryeae (Wynne 2001), there are two groups with different procarp development: 1) Phyco- drys-type having one carpogonial branch with two sterile groups, and 2) Polyneura-type having two carpogonial branches with one sterile group. Five genera including Erythroglossum, Polyneura Kylin, Sorella Hollenberg, Sorellocolax Yoshida & Mikami, and Womersleya Papen- fuss are known to have the Polyneura-type procarp (Yo- shida and Mikami 1991, 1996, 1997, Maggs and Hom- mersand 1993, Kim and Nam 1994, Lin and Kraft 1996, Womersley 2003, Díaz-Tapia et al. 2009). Erythroglossum is distinguished from Sorella by tetrasporangial posi- tion (Hollenberg 1943, Yoshida and Mikami 1991), from Womersleya by the presence of a midrib or vein (Lin and Kraft 1996), and Polyneura by the presence of a midrib (Maggs and Hommersand 1993). The genus Sorellocolax is not comparable to Erythroglossum in terms of size or their host (Yoshida and Mikami 1996). In Erythroglos- sum, morphological features such as thallus habit, blade shape, structure and branching, and veins have been used for separating species (Maggs and Hommersand 1993, Yoshida and Mikami 1997, Díaz-Tapia et al. 2009).
Recently, rbcL sequence data have been used for compar- ing the taxonomic position among the species of the fam- ily Delesseriaceae (Lin et al. 2001b, Lin and Nelson 2010, Kim and Kang 2011).
Three species of Erythroglossum, namely E. minimum Okamura, E. pinnatum Okamura, and E. latum Yoshida
& Mikami, are currently known to occur in the north- western Pacific region, and two of these species (E. mini- mum and E. pinnatum) are in the Korean coast (Guiry and Guiry 2013). The aims of this study are to compare the morphological features of the new species and other Erythroglossum species and to investigate the phyloge- netic relationships in the tribe Phycodryeae based on the analysis of rbcL gene. To compare the molecular data, we collected two species (E. minimum and E. pinnatum) of Erythroglossum and Polyneura japonica from Korea and Japan. Unfortunately, we could not collect E. latum. This is the first study comparing molecular data within the ge- nus Erythroglossum.
Daesambudo, Yeosu on Jul 25, 2012 (JN120725-1, female gametophyte; JN120725-2, tetrasporophyte); Jakdo, Yeo- su on Jul 25, 2012 (JN120726-54, tetrasporophyte); Geo- mundo, Yeosu on Jul 25, 2012 (JN120725-42, female ga- metophyte).
Morphology. Thalli are erect, broadly lobed, shortly stipitate, growing up to 3-6 cm high, 2.5 cm wide in the broadest portion of the lobes, and attached by a discoid holdfast (Fig. 1A-C & E). The blades are at first simple and elliptical to obovate in outline, and later divided di- trichotomously. Each lobe has an elliptical to obovate outline with a round apex (Fig. 1A-C). The margins of the blades are beset with microscopic dentations (Fig. 1D).
The blades are mostly monostromatic, except for the midrib and lateral veins. The midrib is connected with a stipe, which is conspicuous except near the apical portion of the blade. Lateral veins divide alternately or dichoto- mously from the midrib (Fig. 1A, B, E & F). Microscopic veins or anastomosing nerves are absent. The basis of stipe produces creeping cylindrical branches, from which additional thalli are generated. The stipe is cylindrical in the basal part and is compressed near the starting point of the blade wing. Young blades irregularly initiate from the stipes (Fig. 1E-G). In the cross-section views, the veins are composed of large roundish cells, which are arranged side by side, and are located in the center of the branch with several cortical layers. The numbers of cortical cell layers decrease toward the apical part of veins (Fig. 1H-J).
Fig. 1K shows the apical organization: the growth of thalli is initiated by an apical cell, which divides transversely generating the primary cell row. The cells produced by the transverse division of an apical cell are divided longitudi- nally to form second-order cell rows laterally. After pro- ducing second-order cell rows, certain cells of the prima- ry cell row divide transversely, a process which is termed intercalary division, and also divide longitudinally. The second-cell rows reach the thallus margin, and some continue growth to develop microscopic dentations from the blade margin. The third-order cell rows are mostly cut off abaxially from the second-order cell rows, occasion- ally adaxially. Transverse and longitudinal intercalary cell divisions are frequent in the primary cell row and higher order cell rows.
Gametophytes are dioecious. Procarps are scattered between the midrib and the blade margin in median to upper parts of blades, consisting of a supporting cell, a 7-8 celled sterile group, and two 4-celled carpogonial branches (Fig. 2A-C). Mature cystocarps are hemispheri- cal and 500-700 µm in diameter, more swollen on the os- tiolate side of blade, and composed of a large branched best tree. To generate bootstrap values we used the same
program with the same settings for 1,000 replications (Kang and Kim 2013).
RESULTS
Erythroglossum hyacinthinum J. C. Kang & M. S.
Kim sp. nov.
Description. Thalli erect, 3-6 cm high and 1.5-2.5 cm wide, lobed and membranous with a short cylindrical stipe, attached to the substratum by discoid holdfast, simple or divided di- or trichotomously; blades ellipti- cal to obovate with rounded apex; blade margins beset with microscopic dentations; midribs conspicuous and faint near apical part of lobes, lateral veins divided from midrib alternately to dichotomously; microscopic veins absent; bright red with bulish-violet iridescence in liv- ing condition; cystocarps hemispherical with an ostiole, scattered over the monostromatic areas of the middle to upper blades; procarps consist of a supporting cell, a 7-8 celled sterile group, and two groups of 4-celled carpogo- nial branches; spermatangial sori produced on the lamel- lae between midrib and blade margin in the upper parts of blade; tetrasporangial sori round to irregular shape, scattered on monostromatic portions of middle to upper blades, composed of two layers of tetrasporangia; mature tetrasporangia spherical and divided tetrahedrally.
Holotype. JN130604-1 (tetrasporophyte), collected from 12 m depth of Chujado, Jeju province, Korea (33°58′04.28″ N, 126°17′08.64″ E) on Jun 4, 2013, and de- posited in the Herbarium of Department of Biology, Jeju National University, Korea (JNUB).
Isotypes. JNUB (JN130604-3, JN130604-5 to -9) and KB (NIBRAL0000137942-3).
Etymology. The specific epithet (hyacinthinum) was chosen to represent the color of this species when alive, having a bulish-violet iridescence. Latin: hyacinthinus, -a, -um. adj. A.
Korean name. 푸른빛붉은혀
Habitat. Erythroglossum hyacinthinum was collected at 10-30 m depth where they were growing on bedrock.
Other specimens examined. Sasudo, Jeju on Jun 5, 2013 (JN130605-1, tetrasporophyte; JN130605-2, female gametophyte; JN130605-3, male gametophyte); Gwideok, Jeju on May 31, 2011 (H011 and H015, female gameto- phyte); Jocheon, Jeju on May 20, 2011 (H010, tetrasporo- phyte); Dueokdo, Wando on Jul 26, 2012 (JN120726-23, tetrasporophyte; JN120726-26, female gametophyte);
Fig. 1.
Erythroglossum hyacinthinum J. C. Kang and M. S. Kim sp. nov. (A) Holotype specimen from Chujado (JN130604-1), Jeju Island on Jun 4, 2013. (B) Habit of young thalli showing simple and elliptical to obovoid outline. (C) In the living condition, the thalli having bulish-violet iridescence. (D) Blade margin with microscopic dentations. (E & F) Basal part of thalli composed of discoid holdfasts (arrowheads) with creeping cylindrical branches (arrows) and short stipes. (G-J) Cross section views of stipe (G), the lower (H), the middle (I), and the upper part (J) of main branch: the blade composed of monostromatic lamellae and a polystromatic midrib. (K) Apical organization of thallus is showing primary (1) and higher order cell-rows (2-4), and cells resulting from intercalary divisions (i). Scale bars represent: A, 2 cm; B & D, 500 µm; E & F, 1,000 µm; G-J, 200 µm; K, 20 µm.A C
D
B
E F G
H I
J
K
Fig. 2.
Erythroglossum hyacinthinum J. C. Kang and M. S. Kim sp. nov. (A) Cystocarps (cp) scattered on the monostromatic lamellae between midrib (md) and blade margin. (B & C) Procarp composed of a supporting cell (sc), two groups of four-celled carpogonial branches (cb) with a trichogyne (tr), and a group of sterile cells (st), which are connected by pit-connections (arrows). (D) A mature cystocarp composed of a large branched fusion cell (fu), short-chained carposporangia (ca) on the terminal of gonimoblast filaments (gb), several cells layer pericarp, and an prominent ostiole on apical portion. (E) Spermatangial sori (ss) produced between midrib (md) and the blade margin. (F) Surface view of spermatangial sorus showing numerous spermatangia (sp). (G) Cross-section view of spermatangial sorus showing spermatangia (sp) produced by spermatangial mother cells (smc), which occur on opposite sides of central cells (cc). (H) Tetrasporangial sori (ts) produced between midrib (md) and blade margin. (I) Surface view of tetrasporangial sorus. (J) Cross-section view of tetrasporangial sorus showing two layers of tetrasporangia.Scale bars represent: A & H, 1,000 µm; B, C, F & G, 20 µm; D, 100 µm; E, 500 µm; I & J, 50 µm.
A C
D B
E
G F
H
I J
Fig. 3.
Maximum likelihood phylogenetic tree (log likelihood = -7,719.609264) for the genus Erythroglossum and putative relatives derived from plastid-encoded rbcL sequence data. The bootstrap values (1,000 replicates) are shown above branches. Scale bar represents: substitution per site.Erythroglossum, Polyneura, Sorella, Sorellocolax, and Womersleya are known to have procarp consisting of a pair of carpogonial branches and one sterile-cell group (Lin and Kraft 1996, Yoshida and Mikami 1996). The diag- nostic morphological characteristics among the five gen- era are as follows: 1) the presence of midrib or midveins, and the marginal position of tetrasporangial sori for Erythroglossum; 2) presence of macroscopic midveins, and median position of tetrasporangial sori for Sorella; 3) midrib absent, presence of macroscopic and microscopic anastomosing nerves, and inter nerves position of tetra- sporangial sori for Polyneura; 4) lack of microscopic and macroscopic veins, and growth by transversely dividing marginal apical cells, with the later formation of a con- tinuous marginal meristem for Womersleya; 5) very small stellate and hemiparasitic thalli on the genus Sorella for Sorellocolax (Hollenberg 1943, Maggs and Hommersand 1993, Yoshida and Mikami 1996, Womersley 2003). The diagnostic characters of the genus Erythroglossum are entirely satisfied by morphology of our new species.
In the genus Erythroglossum, the following diagnostic characters for identification at the species level have been used: habit of thallus, branching patterns, and veins and blade structures (Maggs and Hommersand 1993, Yoshida and Mikami 1997, Díaz-Tapia et al. 2009). In observations of the morphological features, E. hyacinthinum is clearly separated from other species of Erythroglossum from the northwestern Pacific Ocean (Table 1): in terms of thallus size from E. minimum (3-6 cm high and 1.5-2.5 cm width vs. 1-2.5 cm high and 1-2 mm width), branching patterns from E. pinnatum (di-trichotomous vs. 2-3 times pinnate manner), and blade structures from E. latum (mostly monostromatic vs. mostly polystromatic). This new spe- cies more closely resembles Polyneura japonica rather than other Erythroglossum species in terms of discoid holdfast, cylindrical stipe, di-trichotomous branching, presence of midrib and lateral veins, and blade margins with fine teeth, but differs in blade structure (mostly monostromatic vs. mostly polystromatic), iridescence (bulish-violet vs. none), and shapes (elliptical to obovate vs. broadly linear) (Table 2). Upon first observation of E.
hyacinthinum at 30 m depth, we were very confused as to its taxonomic status due to the extensive morphologi- cal similarities with P. japonica. However, we assigned the new species to the genus Erythroglossum because the morphological features (i.e., presence of midrib and lat- eral veins, marginal position of tetrasporangial sori) are more in agreement with the genus Erythroglossum than Polyneura (Maggs and Hommersand 1993).
P. japonica was originally described by Yamada as Het- fusion cell generating numerous radiate gonimoblast
filaments, 2-4 chains of ovoid to pyriform carposporan- gia terminating each gonimoblast filament, and 5-7 cells thick pericarp (Fig. 2D). Spermatangial sori are produced between the midrib and blade margin in the upper parts of the blades, roundish to elliptical at first and later ex- pand and become irregular in shape, consisting of a layer of central cells, two layers (each layer on opposite sides of central cells) of quadrangular spermatangial mother cells, which bearing elongate spermatangia (Fig. 2H-G).
Tetrasporangial sori are scattered between veins and blade margin in median to upper parts of blades, circular at first and adjacent sori becoming coalescent as they ex- pand, consisting of two layers of tetrasporangia. Mature tetrasporangia are spherical, 400-500 µm in diameter and divide tetrahedrally (Fig. 2I & J).
Molecular analysis. We determined a total of 61 rbcL sequence data: 25 Erythroglossum samples containing the new species from Korea, four E. pinnatum samples from Japan, five Polyneura samples from Korea, and 27 rbcL from the tribe Phycodryeae as putative relatives, and the tribe Myriogrammeae as an outgroup. We aligned 1187 nucleotide base pairs of rbcL gene, and of all sites, 383 (32.2%) were variable and 270 (22.7%) were phyloge- netically informative. Eleven specimens of E. hyacinthi- num from seven sites in Korea formed a clade with 0-0.2%
divergence within the clade. E. hyacinthinum showed 2.7- 3.3% divergence from other Erythroglossum species, and 1.8-2.0% divergence from Polyneura japonica.
In the phylogenetic tree (Fig. 3), the clade contain- ing Erythroglossum spp., P. japonica, and P. latissima was clearly separated from the other species of the tribe Phycodryeae, and strongly supported monophyly by the 100% ML bootstrap value. The clade of E. hyacinthinum formed a sister clade with P. japonica in a 70% boot- strap value. However, the Polyneura-type procarpic spe- cies (i.e., Erythroglossum spp., P. japonica, P. latissima, P.
bonnemaisonii, and Womersleya monanthos) were not monophyletic. In contrast, the Phycodrys-type procarpic species (i.e., Phycodrys, Nienburgia, Heterodoxia, and Hy- menenopsis) were monophyletic with low bootstrap sup- port (69%).
DISCUSSION
Our data clearly indicates that we have collected a new species of Erythroglossum in Korea, E. hyacinthinum.
This species does not match any other species present- ly described. In the tribe Phycodryeae, the five genera
Ta bl e 1.
Collection information of samples used in this study Taxa Collection informationHabitat (depth / substratum) VoucherGenBank accession No.References Erythroglossum hyacinthi- num sp. nov.Chujado, Jeju, Korea; Jun 4, 201312-15 m depth / bed rockJN130604-1 ()KF305299This study Chujado, Jeju, Korea; Jun 4, 201312-15 m depth / bed rockNIBRAL0000137942 (♂)KF305300This study Daesambudo, Yeosu, Korea; Jul 25, 201225-30 m depth / bed rockJN120725-2 ()KF305294This study Dueokdo, Wando, Korea; Jul 27, 201210 m depth / bed rockJN120727-23 ()KF305295This study Gwideok, Jeju, Korea; May 31, 201125 m depth / bed rockH011 (♀)KF305297This study Gwideok, Jeju, Korea; May 31, 201125 m depth / bed rockH015 (♀)KF305296This study Jakdo, Yeosu, Korea; Jul 26, 201220-25 m depth / bed rockJN120726-54 ()KF305293This study Jocheon, Jeju, Korea; May 20, 201130 m depth / bed rockH010 ()KF305298This study Sasudo, Jeju, Korea; Jun 5, 201312-15 m depth / bed rockJN130605-1 ()KF305301This study Sasudo, Jeju, Korea; Jun 5, 201312-15 m depth / bed rockJN130605-2 (♀)KF305302This study Sasudo, Jeju, Korea; Jun 5, 201312-15 m depth / bed rockJN130605-3 (♂)KF305303This study Erythroglossum minimum OkamuraBiyangdo, Jeju, Korea; Nov 22, 201210 m depth / Cladophora wrightianaJN121122-4 ()KF305292This study Biyangdo, Jeju, Korea; Nov 22, 201210 m depth / C. wrightianaJN121122-6 (♀)KF305291This study Biyangdo, Jeju, Korea; Feb 26, 2013Low intertidal / bed rockJN130226-11 ()KF305287This study Biyangdo, Jeju, Korea; Nov 22, 2012Low intertidal / bed rockJN130226-8 ()KF305282This study Dokdo, Uleung, Korea; Apr 22, 20135-10 m depth / bed rockJN130422-6 ()KF305284This study Dokdo, Uleung, Korea; Apr 22, 20135-10 m depth / bed rockJN130422-9 ()KF305283This study Gapado, Jeju, Korea; Mar 26, 20138-12 m depth / C. wrightianaJN130326-13 (♀)KF305285This study Gapado, Jeju, Korea; Mar 26, 20138-12 m depth / C. wrightianaJN130326-14 (♂)KF305286This study Gapado, Jeju, Korea; Mar 26, 20138-12 m depth / C. wrightianaJN130326-21 ()KF305288This study Jeongdori, Wando, Korea; Jun 9, 2012Low intertidal / bed rockJN120609-29KF305289This study Jeongdori, Wando, Korea; Jan 16, 2013Low intertidal / bed rockJN130116-9 ()KF305290This study Erythroglossum pinnatum OkamuraMunseom, Jeju, Korea; Jan 30, 20134 m depth / bed rockJN130130-15 (♀)KF305275This study Munseom, Jeju, Korea; Jan 30, 20134 m depth / bed rockJN130130-19 (♂)KF305277This study Munseom, Jeju, Korea; Jan 30, 20134 m depth / bed rockJN130130-20 ()KF305276This study Misaki, Japan; Apr 10, 2013Low intertidal / bed rockJN130410-79KF305281This study Shimoda, Japan; Apr 12, 2013Low intertidal / bed rockJN130412-1 ()KF305279This study Shimoda, Japan; Apr 12, 2013Low intertidal / bed rockJN130412-2 ()KF305280This study Shimoda, Japan; Apr 12, 2013Low intertidal / bed rockJN130412-3 ()KF305278This study Polyneura japonica (Yamada) MikamiChuja, Jeju, Korea; Jun 4, 201312 m depth / bed rockJN130604-10KF305274This study Ganjeolgot, Ulsan, Korea; Jul 21, 2012Washed up on the shoreJN120721-13KF305271This study Gwanganri, Busan, Korea; Dec 20, 20125-10 m depth / bridge postJN121220-48 (♀)KF305273This study Jeongdori, Wando, Korea; Jun 9, 2012Washed up on the shoreJN120609-27KF305270This study Songjeong, Busan, Korea; Dec 20, 20128-12 m depth / bed rock JN121220-06KF305272This studyTa bl e 1.
Continued Taxa Collection informationHabitat (depth / substratum)Voucher GenBank accession No. References Cladodonta lyallii (J. D. Hooker & Harvey) Skottsberg
Rookery Bay, Stanley, E. Falkland Islands; Jan 4, 1998
--AF254169Lin et al. (2001a) Haraldiophyllum bonnemaisonii (Kylin) A. D. ZinovaNear Fanad Head, Co. Donegal, UK; May 21, 2000--AF312311Lin et al. (2001a) Haraldiophyllum crispatum (J. D. Hooker & Harvey) Lin, Hommersand & Nelson
Mill Creek Estuary, Oban, Stewart Island, New Zealand; Oct 31, 2004--DQ916305Lin et al. (2007) Haraldiophyllum mirabile (Kylin) A. D. ZinovaCanove Island, San Juan Island, Washington, USA; Jun 29, 1998--AF254185Lin et al. (2001a) Haraldiophyllum sp.La Herradura, Coquimbo, Chile; Jan 19, 1995--AF254188Lin et al. (2001a) Haraldiophyllum udoensis M. S. Kim & J. C. KangHaumokdong, Udo, Jeju, Korea; Jun 14, 200912 m depth / stoneJNU-MSK30601HU ()JN561293Kim and Kang (2011) Heterodoxia denticulata (Kuntze) J. AgardhWarrnambool, Victoria, Australia; Jul 13, 1995--AF254190Lin et al. (2001a) Hymenenopsis heterophylla S. -M. Lin, W. A. Nelson & M. H. Hommersand Marfells Beach, Marborough, South Island, New Zealand; Nov 5, 2010
- WELT A030892JF495097Lin et al. (2012) Myriogramme livida (J. D. Hooker & Harvey) KylinSealion Island, Falkland Islands; Jan 7, 1998--AF257391Lin et al. (2001a) Myriogramme manginii (Gain) SkottsbergBahia Elefante, Base Frei, King George I., Antarctic Peninsula; Feb 5, 1994--AF257392Lin et al. (2001a) Nienburgia andersoniana (J. Agardh) KylinHorseshoe Cove, Bodega Bay, CA, USA; Jan 19, 1993--AF257396Lin et al. (2001a) Nienburgia borealis (Kylin) KylinMosquito Bay, Washington, USA; Jul 2, 1998--AF257398Lin et al. (2001a) Phycodrys adamsiae S. -M. Lin & W. A. NelsonBland Bay, North Island, New Zealand; Dec 30, 2007- WELT A028764GQ479940Lin and Nelson (2010) Phycodrys antarctica (Skottsberg) SkottsbergWendy's Rock, Borradile I., Balleny Islands, Antarctica; Feb 22, 2006--GQ479932Lin and Nelson (2010) Phycodrys austrogeorgica SkottsbergHero Inlet, Avers I., Antarctica; Apr 19, 2003--GQ479930Lin and Nelson (2010) Phycodrys fimbriata (Kuntze) KylinCape Nosappu, Hokkaido, Japan; Jul 26, 2002--GQ479929Lin and Nelson (2010)
Ta bl e 1.
Continued Taxa Collection informationHabitat (depth / substratum)Voucher GenBank accession No. References Phycodrys franiae S. -M. Lin & W. A. NelsonMarfells Beach, Marlborough, South I., New Zealand; Dec 7, 2007-WELT A023691GQ479941Lin and Nelson (2010) Phycodrys novae-zelandiae S. -M. Lin & W. A. NelsonMarfells Beach, Marlborough, South I., New Zealand; Dec 7, 2007-WELT A023503GQ479934Lin and Nelson (2010) Phycodrys ovifolia (Kützing) M. J. WynneIsla Mancerra, Bahia coral, Prov. Valdivia, Chile; Jan 11, 1998--AF257423Lin et al. (2001a) Phycodrys quercifolia (Bory de Saint-Vincent) Skottsberg
Rookery Bay, Stanley, E. Falkland Islands; Jan 4, 1998--AF257424Lin et al. (2001a) Phycodrys radicosa (Okamura) Yamada & InagakiGingdao, Shuntung Peninsula, China; Jun 23, 1994--AF257427Lin et al. (2001a) Phycodrys riggii N. L. GardnerKittilngook Bay, St. Lawrence Island, Alaska, USA; Jul 5, 1996--AF257430Lin et al. (2001a) Phycodrys rubens (Linnaeus) BattersWest Angle Bay, Pembrokeshire, UK; Jul 22, 1997--AF257429Lin et al. (2001a) Polyneura bonnemaisonii (C. Agardh) Maggs & HommersandIle Verte, Roscoff, Brittany, France; Jun 22, 1993--AF257437Lin et al. (2001a) Polyneura latissima (Harvey) KylinSeal Rock, Oregon, USA; May 16, 1999--AF257438Lin et al. (2001a) Polyneura japonica (Yamada) MikamiOhara, Chiba, Japan; Mar 26, 2008--CQ479943Lin et al. (2001a) Womersleya monanthos (J. Agardh) PapenfussPt. Lansdale, Victoria, Australia; Jul 30, 1995--AF257457Lin et al. (2001a)
Ta bl e 2.
Comparison of distinguishing morphological characters among Erythroglossum hyacinthinum sp. nov. and putative relatives CharacteristicsE. hyacinthinum sp. nov. E. latum E. minimum E. pinnatum Polyneura japonica Height 3-6 cmUp to 10 cmUp to 2.5 cm5-10 cmUp to 12 cm Width of blade1.5-2.5 cm1.2 cm1-2 mm5-10 mm1.0-1.5 cm Blade shape Elliptical to obovateLanceolate to linear lanceolateLinear or lenear-lanceolateBroadly linearBroadly linear Shape of lateral branchElliptical to obovateBroad lanceolate to ovoidObovate or linear-oblongBroadly linearBroadly linear Blade marginNumerous microscopic dentateWeakly undulateA few microscopic teethMinute teethIrregularly fine teeth Base of lateral branchNot taperingSlightly taperingTaperingTapering to cuneate baseNot tapering Branching patternSimple or di-trichoto- mouslyAlternately pinnatePinnate with 1-2 timesPinnate with 2-3 timesRepeatedly di-tri-pin- nately HoldfastsDiscoid, cylindrical creeping branch-Root processes from basal uder-surface and marginScutate disc Scutate disc, slender stolon-like roots StipeCylindrical---Cylindrical VeinsMidrib, alternate veinsMidribAbsentMidribMidrib, alternate veins Blade structureMonostromatic except veinsPolystromatic except blade marginMonostromatic except me- dian portionPolystromatic except blade marginPolystromatic except blade margin Iridescence Bulish-violet---- Type locality Chujado, Jeju, KoreaShioyazaki, Fukushima, JapanChiba, JapanChiba, JapanOhara, Chiba, Japan References This study Yoshida and Mikami (1997)Okamura (1932b), Mikami (1976), Yoshida (1998)
Okamura (1932b), Mikami (1977), Yoshida (1998) Yamada (1930), Okamura (1932a), Mikami (1973)
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Kim, M. S. & Kang, J. C. 2011. A new Korean red algal spe- cies, Haraldiophyllum udoensis sp. nov. (Delesseriaceae, Rhodophyta). Algae 26:211-219.
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Kylin, H. 1935. Zur Nomenklatur einiger Delesseriaceen. Fys- iogr. Sällsk. Förh. 5:1-5.
Lin, S. -M., Fredericq, S. & Hommersand, M. H. 2001a. Sys- tematics of the Delesseriaceae (Ceramiales, Rhodophy- ta) based on large subunit rDNA and rbcL sequences, including the Phycodryoideae, subfam. nov. J. Phycol.
37:811-899.
Lin, S. M., Hommersand, M. H. & Kraft, G. T. 2001b. Charac- terization of Hemineura frondosa and the Hemineureae trib. nov. (Delesseriaceae, Rhodophyta) from southern Australia. Phycologia 40:135-146.
Lin, S. -M., Hommersand, M. H. & Nelson, W. A. 2007. An assessment of Haraldiophyllum (Delesseriaceae, Rho- dophyta), inclucing H. crispatum (J.D. Hooker et Har- vey) comb. nov. from New Zealand based on rbcL and LSU sequence analysis and morphological evidence.
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eronema japonica in 1930, and was then transferred to the genus Nienburgia in 1935 by Kylin (Yamada 1930, Mi- kami 1973). Later, Mikami (1973) confirmed that this spe- cies had Phycodrys-type apical organization and Polyneu- ra-type procarp. At that time, Mikami was aware that the specimens had both midrib and lateral veins; however, he transferred the species to the genus Polyneura citing the presence of a midrib in Polyneura gmelinii (J. V. Lamour- oux) Kylin. In Korea, Kim and Nam (1994) mentioned the possibility of establishing a new taxonomic group for P.
japonica and P. gmelinii because these species have a midrib, lateral veins, and distinctive apical organization differently other species of Polyneura. However, P. gmeli- nii is currently treated as a taxonomic synonym of Eryth- roglossum laciniatum (Lightfoot) C. A. Maggs & Hommer- sand (Maggs and Hommersand 1993). The results of our molecular analyses demonstrate the possibility that P. ja- ponica is more closely related with the genus Erythroglos- sum than Polyneura (Fig. 3). To fully resolve this issue, we need more morphological and molecular evidence from other taxonomic groups, including the type species of each genus, Erythroglossum, Polyneura, and Sorella.
In conclusion, we collected a new species that has similar morphological features with P. japonica. To con- firm the taxonomic position of that species, we collected other species of the tribe Phycodryeae and performed morphological and molecular analyses. As the result, we identified a new species, E. hyacinthinum sp. nov. In ad- dition, our molecular phylogenetic results highlight the problems of taxonomic position in the genera of the tribe Phycodryeae, namely showing the polyphyletic taxon among Polyneura-type procarp group.
ACKNOWLEDGEMENTS
We thank the staff of Dadohaehaesang National Park for assisting with transportation and underwater guid- ance, and we thank Miss H. S. Choi for her transla- tion of Japanese articles. This work was supported by a grant from the National Institute of Biological Resources (NIBR), as funded by the Ministry of Environment (MOE) of the Republic of Korea (NIBR No. 2013-02-001 for the collecting samples, and 1834-302 for molecular analyses).
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