Morphology and Distribution of Sargassum oligocystum (Fucales, Phaeophyceae) in the Ryukyu Islands, Japan

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1 J. Jpn. Bot. 88: (2013) Morphology and Distribution of Sargassum oligocystum (Fucales, Phaeophyceae) in the Ryukyu Islands, Japan Hiromori Shimabukuro a, *, Naho Miyamoto b and Masami Hamaguchi a a National Research Institute of Fisheries and Environment of Inland Sea, Fisheries Research Agency, , Maruishi, Hatsukaichi, Hiroshima, JAPAN; b Momo, Seaweed Research Service, 7-1 Nagahama, Yomitan, Nakagami, Okinawa, JAPAN *Corresponding author: bukuro@affrc.go.jp (Accepted on January 12, 2013) Sargassum oligocystum was first described in 1845 based on specimens collected from Indonesia and is primarily distributed in tropical and subtropical regions. However, no detailed reports have been published on the distribution and the morphological characteristics of this species in Japan. During the present study, S. oligocystum was collected from 7 locations in the Ryukyu Islands of Japan and was typically found on rocky substrata in the subtidal zones inside of coral reefs and bays. The specimens examined for this study were characterized by: (1) the small discoid holdfast; (2) the compressed main branches that showed a smooth surface and that arose from the center of the stem; (3) the lanceolate to narrow lanceolate leaves with a dentate margin; (4) the spherical vesicles, rarely with spines or wing-like structures on top; and (5) the zygocarpic, monoecious compressed receptacles. Sargassum ilicifolium and S. swartzii are morphologically similar to S. oligocystum but were distinctive from it by the morphological characteristics of the leaves, main branches, and receptacles. A new Japanese name HIRAMI-MOKU is proposed for this species as it has a compressed receptacle. Key words: Coastal ecosystem, Fucales, Hirami-moku, morphology, Okinawa, Phaeophyceae, Ryukyu Islands, Sargassum oligocystum. Sargassum C. Agardh is a widely distributed genus of brown algae with distribution ranging from the subarctic to the tropics (Yoshida 1984, Phillips 1995, Phillips and Fredericq 2000). It is the most species-rich genus in Sargassaceae, Phaeophyceae, comprising over 400 valid species, as recorded by Guiry and Guiry (2012). Sargassum oligocystum was first described by Montagne (1845) on the basis of a specimen collected from Lampung Bay, Sumatra, Indonesia. This species is distributed widely within the tropical zone around the equator and is found in the ocean waters around Kenya, in the Red Sea, on the eastern side of Africa (Bolton et al. 2007, Ateweberhan and Prudʼhomme van Reine 2005), India (Sahoo and Debasish 2001), the Philippines, Indonesia, Malaysia, Vietnam (Trono 1992, Noro et al. 1994, Ajisaka et al. 1999, Ajisaka 2002, Abbott et al. 2002, Tsutsui et al. 2005, Tsutsui et al. 2012), China (Tseng 1984, Tseng and Lu 2000), Australia, and Micronesia (Lobban and N Yeurt 2006, Bostock and Holland 2010). Yoshida (1998) reported that this species was 94

2 April 2013 Journal of Japanese Botany Vol. 88 No.2 95 Fig. 1. Distribution of Sargassum oligocystum Montagne in Japan on the specimens deposited in herbaria (SAP, TNS, KAGF, and FEIS) and collected by the author (Shimabukuro). Scale bar: 20 km. found in the southwestern islands off Kyushu, Japan. Further, Noro et al. (1994) identified specimens collected in Amami Ohshima, Kagoshima Prefecture, as S. oligocystum. However, this species has no Japanese name, reflecting its relative obscurity. Hence, there is limited knowledge available on the detailed morphological characteristics and distributions of this species. In this paper, we report the detailed distribution of this species, as well morphological and anatomical observations, on the basis of the specimens deposited in several research institutes in Japan and specimens collected by the authors around the Ryukyu Islands. Materials and Methods The specimens used in this study were collected around the Ryukyu Islands, Japan, from September 2003 to May 2009 and during September 2011 by scuba and skin diving. Specimens were made into dry herbarium specimens after preserving them in 10% formalin/seawater in the laboratory. Gross observations and the use of the stereomicroscope (Olympus SZX7) were used to describe the specimen morphology. The sexuality of the specimens was determined by examining handcut sections of the receptacles under a biological microscope (Nikon Eclipse E600). The handcut sections were stained with 1% cotton blue in glycerol/seawater prior to observation. All images were taken by a digital camera with a microscope and were imported into Adobe Photoshop Elements 10 for plate assembly. The maturation period of this species was estimated based on the presence or absence of receptacles in the specimens collected by the authors and those deposited as herbarium specimens. The voucher herbarium specimens of this species used in this study were deposited in the Department of Botany, National Museum of Nature and Science, Japan (TNS-AL). Additionally, specimens from the herbaria at the Graduate School of Science, Hokkaido University (SAP); the National Research Institute of Fisheries and Environment of Inland Sea (FEIS); the Kagoshima Prefectural Fisheries

3 96 植物研究雑誌第 88 巻第 2 号 2013 年 4 月 Fig. 2. Habitat of Sargassum oligocystum Montagne, as observed in Arakawa, Ishigaki City, Okinawa Prefecture, Japan (Aug. 31, 2011). Scale bar: 20 cm. Technology and Development Center (KFE) and the corresponding author s herbarium ( bukuroʼ) were used in this study (Fig. 1). Results Sargassum oligocystum grew on coral reef flats, coral blocks, or on rocks in the bay and was found at a depth of 0.5 to 3 m in the subtidal zone (Fig. 2). It rarely grew on small coral pieces where the flow of the seawater was slow. This species was found as part of small mixed communities with S. polycystum, S. polyporum, and Hormophysa cuneiformis. Large communities constituting only S. oligocystum did not occur, in contrast to species such as S. horneri or S. muticum. The life cycle of this species was as follows; the initial leaves began to appear on the rocks in March to May, young thalli grew in June to September of the summer season, and most of the thalli matured in October to January in the cold season. Sargassum oligocystum Montagne 1845 New Japanese name: HIRAMI-MOKU. 新和名 : ヒラミモク Type locality: Lampung Bay, Sumatra, Indonesia. Distribution in Japan and specimens examined: Sani, Kasari Town, Amami City, Kagoshima Prefecture (September 6, 2001, KFE-B 67102; June 17, 2003, KFE-B 67106, 67107); Ujiji-hama, China Town, Oshima County, Kagoshima Prefecture (June 26, 2003, KFE-B ; July 31, 2003, KFE-B , ); Oganeku, Yoron Town, Oshima County, Kagoshima Prefecture (June 3, 1981, KFE-B ); Noho, Iheya Village, Shimajiri County, Okinawa Prefecture (May 18, 2009, FEIS 1204, 1205); Shiraho, Ishigaki City (September 18, 2003, bukuro 470; November 26, 2003, SAP , ; TNS-AL , ; KAGF 1788, 1789, 1796; bukuro 532); Arakawa, Ishigaki City, Okinawa Prefecture (August 31, 2011, FEIS 974, 975, 976); Haemida, Taketomi Town, Yaeyama County (November 8, 2003, SAP , ; TNS-AL ; KAGF 1787; November 26, 2004, bukuro 463, 464, 465). Morphology: Thallus cm, up to 80 cm tall; holdfast small flat discoid, 5 10 mm

4 April 2013 Journal of Japanese Botany Vol. 88 No.2 97 Fig. 3. Thallus of Sargassum oligocystum Montagne (bukuro 532) preserved in 10% formalin/seawater before being dried. Scale bar: 5 cm.

5 98 植物研究雑誌第 88 巻第 2 号 2013 年 4 月 in diameter; terete stem with smooth surface, short, 2 3 mm long, 3 4 mm in diameter, at the center of the holdfast; 2 to 8 primary branches arising spirally from the top of stem; primary and lateral branches strongly compressed with smooth surface, 3 7 mm wide. Lateral branches compressed with smooth surface like primary branch, up to 150 mm long, attached distichously to primary branch at intervals of 5 30 mm (Figs. 3 5). Leaves lanceolate to linear lanceolate, mm long, up to 15-mm wide, with dentate margins and acute apex; cryptostomata scattered on the surface; midrib diminishing up to apex. Vesicles spherical to ovate with round apex, with rarely attached short stipe and simple coronal leaf on top of the vesicle, up to 6 mm in diameter; stalk shorter than diameter of vesicle; cryptostomata scattered on the surface; medullary strand (Takahashi et al. 2000) present inside the vesicle (Figs. 6, 7). Plant monoecious. Receptacles androgynous, compressed with smooth surface or slightly warty, up to 5 mm long, 1 mm wide, furcated 2 4 times; pseudozygocarpic receptacles with leaves or not. Male and female conceptacles scattered into receptacles, µm in diameter. Oogonia are µm in diameter (Figs. 8, 9). Discussion Sargassum oligocystum is distributed from Amami-Ohshima to the Iriomote Islands and is a native species of this shallow sea area. Sargassum oligocystum grows primarily in tropical to subtropical regions within a range of 18 degrees in the north and south latitudes. Additionally, this species is dispersed from Taiwan to Amami-Ohshima of the Ryukyu Islands by the warm waters of the Kuroshio current system. Amami-Oshima is thought to be the northern limit of the distribution of this species, since it has not been found around Yakushima Island or around the Kyushu mainland more north than Amami-Oshima. The characterization of S. oligocystum in this study revealed this species is distinguished from the known species of the subgenus Sargassum from the Ryukyu Islands and the southeast Asia regions by the following set of morphological characters: (1) small discoid holdfast; (2) compressed primary branches; (3) lanceolate to linear lanceolate leaves with dentate margin; (4) spherical to ovate vesicles; and (5) monoecious sexual system with androgynous receptacles. The morphological features of S. oligocystum are similar to those of S. cristaefolium and S. duplicatum (the latter is regarded as a taxonomic synonym of S. ilicifolium) living in the Ryukyu Islands (Mattio et al. 2009). However, S. oligocystum could be clearly distinguished from S. ilicifolium by the morphological characteristics of the leaves, main branches, and receptacles. In particular, S. oligocystum did not possess the following morphological characteristics of S. ilicifolium: leaves, oblanceolate to elliptical with dentate and cup-shaped margin; slightly compressed or terete main branches; and dioecious receptacles. Additionally, the characteristic of compressed branches is a remarkable feature of the young thallus of S. oligocystum (Fig. 10). Sargassum aquifolium and S. swartzii are distributed in Southeast Asia in tropical and subtropical regions and have compressed main branches like S. oligocystum. In Japan and the adjacent waters, S. aquifolium as S. echinocarpum was reported from Taiwan by Yoshida (1988), and S. swartzii was reported from Ishigaki and Aka Islands in Okinawa Prefecture by Ohba and Aruga (1982) and Ohba (1995). Sargassum oligocystum has compressed receptacles that are not terete, though the leaves have a dentate margin like those of S. aquifolium. Additionally, S. swartzii has terete receptacles and leaves with a smooth margin (Noro et al. 1994). Sargassum oligocystum can be recognized as different species based on the above characteristics for S. aquifolium and S.

6 April 2013 Journal of Japanese Botany Vol. 88 No.2 99 Figs Vegetative anatomies of Sargassum oligocystum Montagne (bukuro 532) preserved in 10% formalin/ seawater before being dried. Fig. 4. Lower part of the thallus showing the holdfast, stem, and main branches. Scale bar: 1 cm. Fig. 5. Upper part of branch with arising leaves, vesicles, and receptacles. Scale bar: 2 cm. Fig. 6. Leaves. Scale bar: 1 cm. Fig. 7. Vesicles. Scale bar: 5 mm. Fig. 8. Close up of androgynous receptacles. Scale bar: 5 mm. Fig. 9. Transverse section of receptacle. F indicates female conceptacles. M. Male conceptacle. Scale bar: 200 µm.

7 100 植物研究雑誌第 88 巻第 2 号 2013 年 4 月 Fig. 10. Young stage of Sargassum oligocystum Montagne. Scale bar: 2 cm. swartzii. Sargassum oligocystum has no Japanese name (Yoshida 1998, Yoshida and Yoshinaga 2010). A limited knowledge of the distribution pattern and of other ecological features of this species in Japan may be the underlying reason. However, the distribution and detailed morphological characteristics of this species have become clear in this study. Yamada (1942) named S. swartzii HIRAE-MOKU based on the specific morphological features of the compressed branches. The peculiar morphological characters of S. oligocystum, such as the compressed branches and receptacles, distinguish it from other Sargassum species in Japan (Noro et al. 1994, Ajisaka et al. 1999, this study). Therefore, the authors suggest HIRAMI- MOKU as the Japanese name for S. oligocystum based on the compressed receptacles. In the Ryukyu Islands, the genus Sargassum composes seaweed beds with several species rather than simply constituting entire beds and grows in shallow waters of up to 3 m deep in coral reef flats. Sargassum oligocystum is one of the important species constituting seaweed beds and contributes to the biodiversity in the Ryukyu Islands. However, shallow water areas are susceptible to environmental changes resulting from warming temperatures and landfill work. In recent years, these environmental changes have caused a shift in the geographical distribution of Sargassum species and have resulted in the loss of many Sargassum species. We will continue to monitor seaweeds, including those of the genus Sargassum, on the border of the tropical and subtropical regions in Ryukyu Islands to evaluate the ongoing impact of these environmental changes. We sincerely thank Prof. Tateo Horiguchi and Assoc. Prof. Kazuhiro Kogame, Graduate School of Science, Hokkaido University; Dr. Taiju Kitayama, Department of Botany, National Museum of Nature and Science; Dr.

8 April 2013 Journal of Japanese Botany Vol. 88 No Ryuta Terada, Kagoshima University, Faculty of Fisheries; and Mr. Shigemitsu Tokunaga, Kagoshima Prefectural Fisheries Technology and Development Center, for giving us the privilege of examining the specimens housed in the herbaria of their institutions. Additionally, we are grateful to Dr. Tadahide Noro, Kagoshima University, Faculty of Fisheries. References Abbott I. A., Fisher J. and McDermid K. J Newly reported and revised marine algae from the vicinity of Nha Trang, Vietnam. In: Abbott I. A. (ed.), Taxonomy of Economic Seaweeds with Reference to Some Pacific Species. 8: California Sea Grant College, La Jolla. Ajisaka T., Phang S. M. and Yoshida T Preliminary report of Sargassum species collected from Malaysian coasts. In: Abbott I. A. (ed.), Taxonomy of Economic Seaweeds with Reference to Some Pacific Species. 7: California Sea Grant College, La Jolla. Ajisaka T Sargassum specimens from Singapore and Malaysia in the Herbarium of the Bishop Museum. In: Abbott I. A. (ed.), Taxonomy of Economic Seaweeds with Reference to Some Pacific Species. 8: California Sea Grant College, La Jolla. Ateweberhan M. and Prudʼhomme van Reine W. F A taxonomic survey of seaweeds from Eritrea. Blumea 50: Bolton J. J., Oyieke H. A. and Gwanda P The seaweeds of Kenya: checklist, history of seaweed study, coastal environment, and analysis of seaweed diversity and biogeography. South African J. Bot. 73: Bostock P. D. and Holland A. E Census of the Queensland Flora. 320 pp. Queensland Herbarium Biodiversity and Ecosystem Sciences, Department of Environment and Resource Management, Brisbane. Guiry M. D. and Guiry G. M AlgaeBase. Worldwide electronic publication, National University of Ireland, Galway. searched on 28 March Lobban C. S. and NʼYeurt A. D. R Provisional keys to the genera of seaweeds of Micronesia, with new records for Guam and Yap. Micronesica 39: Mattio L., Payri C. E. and Verlaque M., Taxonomic revision and geographic distribution of the subgenus Sargassum (Fucales, Phaeophyceae) in the western and central Pacific islands based on morphological and molecular analyses. J. Phycol. 45: Montagne C Plant cellulaires. in: Hombron and Jacquinot, Botanique. Voyage au pole sud et dans lʼocéanie, sur les corvettes lʼastrolabe et la Zélée pp. Gide, Paris. Noro T., Ajisaka T. and Yoshida T Species of Sargassum subgenus Sargassum (Fucales) with compressed primary branches. In: Abbott I. A. (ed.), Taxonomy of Economic Seaweeds. 4: California Sea Grant College, La Jolla. Ohba H. and Aruga Y Seaweeds from Ishigaki Island and adjacent islet in Yaeyama Islands, southern Japan. Jpn. J. Phycol. 30: (in Japanese). Ohba H A list of seaweeds of Akajima Island and its vicinity in Kerama Islands, Okinawa Prefecture, Japan. Midoriishi 6: (in Japanese). Phillips N Biogeography of Sargassum (Phaeophyta) in the Pacific basin. In: Abbott I. A. (ed.), Taxonomy of Economic Seaweeds. 5: California Sea Grant College, La Jolla. Phillips N. and Fredericq S Biogeographic and phylogenetic investigations of the Pantropical genus Sargassum (Fucales, Phaeophyceae) with respect to Gulf of Mexico species. Gulf of Mexico Science 18: Sahoo D., Nivedita and Debasish, Seaweeds of Indian Coast. 283 pp. A. P. H. Publishing, New Delhi. Takahashi A., Inoue I. and Tanaka J Morphology of the vesicle s medullary strand in Fucales (Phaeophyceae). J. Jpn. Bot. 75: (in Japanese). Trono Jr. G The genus Sargassum in the Philippines. In: Abbott I. A. (ed.), Taxonomy of Economic Seaweeds with Reference to Some Pacific and Western Atlantic Species. 2: California Sea Grant College, La Jolla. Tseng C. K Common Seaweeds of China. 318 pp. Science Press, Beijing. Tseng C. K. and Lu B Flora algarum marinarum sinicarum Tomus III Phaeophyta No. II Fucales. 237 pp. Science Press, Beijing. Tsutsui I., Huybh Q. N., Nguyên H. D., Arai S. and Yoshida T The common marine plants of southern Vietnam. 250 pp. Japan Seaweed Association, Usa. Tsutsui I., Hamano K., Aue-Umneoy D., Songphatkaew J., Srisapoome P., Ruangsomboon S., Klomkling S., Ganmanee M., Taveekijakarn T. and Maeno Y Common Underwater Plants in Coastal Areas of Thailand. 171 pp. Japan International Research Center for Agricultural Science, Tsukuba. Yamada Y Notes on Sargassum from the southern parts of Japan (1). J. Jpn. Bot. 18: (in Japanese). Yoshida T Taxonomic and distributional accounts on the Sargassum (Fucales, Phaeophyta) 1. Aquabiology 34: (in Japanese). Yoshida T Japanese and Taiwanese species of Sargassum subgenus Sargassum. In: Abbott I. A. (ed.), Taxonomy of Economic Seaweeds. 2: California

9 102 植物研究雑誌第 88 巻第 2 号 2013 年 4 月 Sea Grant College, California. Yoshida T Marine Algae of Japan pp. Uchida Rokakuho Publishing, Tokyo (in Japanese). Yoshida T. and Yoshinaga K Check List of Marine Algae of Japan (Revised in 2000). Jpn. J. Phycol. 58: (in Japanese). a 島袋寛盛, b 宮本奈保, a 浜口昌己 : 琉球列島に生育す る Sargassum oligocystum( ヒバマタ目 褐藻綱 ) の形態と分布 Sargassum oligocystum Montagne は,1845 年にインドネシアで採集された標本を元に記載され, 主に熱帯 亜熱帯域に分布している. 日本産の本種については, 分布や形態についての報告が少なく和名もついていない. 本研究では, 琉球列島の 7 地点で本種の生育を確認した. 本研究で採集された S. oligocystum は以下のような形態をもつ.1) 小さな盤状の付着器 ;2) 扁圧で表面が滑らかな主枝が茎の上部から伸びる ;3) 葉は披針形から細長い披針形で縁辺に鋸歯が並ぶ ;4) 気胞は 球形で, 上部に棘や冠葉が生じるものもある ;5) 生殖器床は扁圧で zygocarpic の特徴を有する. 形態的に似た種類にS. ilicifolium とS. swartzii があるが, 葉や主枝, 生殖器床の形態的特徴により区別することができた. 扁圧する生殖器床の特徴から, 本種の和名をヒラミモクとした. ( a 独立行政法人水産総合研究センター瀬戸内海区水産研究所, b 海草藻類調査藻茂 )