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Halophila minor (Hydrocharitaceae), a new record with taxonomic notes of the Halophila from the Hong Kong Special Administrative Region, China PDF

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植 物 分 类 学 报 44 (4): 457–463(2006) doi:10.1360/aps050142 Acta Phytotaxonomica Sinica http://www.plantsystematics.com Halophila minor (Hydrocharitaceae), a new record with taxonomic notes of the Halophila from the Hong Kong Special Administrative Region, China YIP Kwok-Leung* LAI Chuen-Chi, Patrick (The Hong Kong Herbarium, Agriculture, Fisheries and Conservation Department, Room 737, 303 Cheung Sha Wan Road, Kowloon, Hong Kong, China) Abstract Halophila minor (Zoll.) den Hartog is reported as a new record of Halophila species in the Hong Kong Special Administrative Region (SAR), in addition to the two known species H. ovalis and H. beccarii. This also represents the first locality of the species in continental China besides the reported localities in Hainan and Nansha Islands. The Halophila species have a peculiar taxonomic history in China, especially in the Hong Kong SAR where the first record dated back to 1856 (from Kowloon Bay). Recently there has been clear scientific evidence to distinguish H. minor from H. ovata (the latter has been confirmed not occurring in the Hong Kong SAR in this report), though the former was once considered conspecific to the latter. The worldwide distribution and taxonomy of Halophila have recently been made clear and thus permitting correct identifications of the species. Seagrasses are of conservation concerns, as the coastal environment of the Hong Kong SAR has been subject to the threat of rapid infrastructure development. Key words Halophila, Halophila minor, Halophila ovalis, Halophila beccarii, Halophila ovata, new record, key, Hong Kong. Further to the report reviewing seagrasses in the Hong Kong Special Administrative Region (SAR) by Kwok et al. (2005), a new record of a marine vascular plant, Halophila minor (Zoll.) den Hartog has been confirmed based on field observations and authentic herbarium specimens. Comparison to existing herbarium specimens and species descriptions in relevant literature (e.g. Wang & Sun, 1992) has confirmed this seagrass species as having been hitherto unrecorded in the Hong Kong SAR. The present discussion and taxonomic treatment of plant materials from the Hong Kong SAR are based on examination of specimens of Halophila species freshly collected from various localities, including but not limited to those provided by Kwok et al. (2005). This is supplemented with re-examination of herbarium specimens deposited in herbaria in the Hong Kong SAR (mainly in the Hong Kong Herbarium [HK]). The voucher specimens of previous published records of Halophila species in Hong Kong were examined although some of them could not be located. In addition, expert opinion regarding taxonomic identification of difficult species was sought (Dr. John Kuo, personal communication). 1 Taxonomic history The species of Halophila present a peculiar taxonomic history, especially in the Hong Kong SAR. Despite a previous review (Hodgkiss & Morton, 1978a) which claimed that the earliest discovery of Halophila in Hong Kong dated back to 1912 (citing Dunn & Tutcher, 1912), the earliest record of Halophila from Hong Kong was indeed “H. ovata” based on a ——————————— Received: 22 September 2005 Accepted: 6 April 2006 * Author for correspondence. E-mail: <[email protected]>. 458 Acta Phytotaxonomica Sinica Vol. 44 sterile specimen (Harland 282, BM) collected in 1856 by W. A. Harland from “Kau-lung Bay” (i.e. the present day Kowloon Bay) (Hance, 1872). More than a century later, Hodgkiss and Morton (1978b) examined all previous collections at the University of Hong Kong and, following den Hartog’s (1970) treatment, concluded that they all belonged to H. ovata Gaudich. This was in addition to their discovery of H. beccarii Asch. The local knowledge of the taxonomy of Halophila has changed little since 1978. Although only two taxonomic entities were known to exist in the Hong Kong SAR since 1978, three specific names (H. ovalis, H. ovata, and H. beccarii) have appeared in previous literature. Wu et al. (2002) considered H. ovata as a misapplied name of H. ovalis based on a review of the specimens deposited in HK. Nomenclature and delimitations of the species, namely H. ovalis, H. ovata and H. minor, have been revised severally in modern times, initially by den Hartog (1957), then by Doty and Stone (1967), den Hartog (1970), and lastly by Sachet and Fosberg (1973), resulting in different taxonomic concepts concerning the species. Of the three species, den Hartog (1957) recognized only H. ovalis and H. minor (sensu lato, including H. ovata) but later considered that the name H. ovata had priority over H. minor (den Hartog, 1970). Kuo (2000) presented an excellent treatise on the treatments of the species and their respective types by various authorities with the conclusion that H. ovata and H. minor are distinct species. To clarify the taxonomy of the species occurring in the Hong Kong SAR and to provide a basis for the Flora of Hong Kong project conducted by the Hong Kong Herbarium of the Agriculture, Fisheries and Conservation Department (AFCD) and the South China Botanical Garden, the Chinese Academy of Sciences, a taxonomic treatment of the Halophila species including the names previously applied to the taxa are presented here to put them into a systematic context. Each citation to relevant taxonomic literature in which an authentic specimen is quoted or is extant is indicated in this paper by the “*” symbol. 2 Taxonomic treatment of Halophila species found in the Hong Kong SAR Halophila Thouars, Gen. Nov. Madagasc. 2. (17 Nov.) 1806; Benth. & Hook. f., Gen. Pl. 3: 455. 1883; Hartog, The Sea-grasses of the World 260. 1970. Type: Halophila madagascariensis Doty & Stone (typified by Doty & Stone, 1967). A genus of about 13 species in tropical and warm temperate seas (Kuo & den Hartog, 2001). Three species recorded in the Hong Kong SAR. Key to the species 1. Leaves ovate; lateral shoots short, 1 cm or less, often inconspicuous, with only one pair of leaves; cross-veins present, linking the mid-rib and intramarginal veins. 2. Leaf blades 6–13 mm, with 7–12 pairs of cross-veins at an angle of 70o–90o………………1. H. minor 2. Leaf blades 10–40 mm, with 12–25 pairs of cross-veins at an angle of 45 o–60 o……………2. H. ovalis 1. Leaves oblong-ovate to lanceolate; lateral shoots longer, 1–1.5 cm, with 6–10 leaf blades at the top; cross-veins lacking, mid-rib and intramarginal veins present…………………………………3. H. beccarii Halophila sect. Halophila According to Kuo and den Hartog (2001), the section Halophila, which currently comprises nine species, is the most morphologically diverse group in the genus Halophila. Species in this section are monoecious or dioecious, minute to robust plants bearing extremely short erect lateral shoots, with two scales at the base and a pair of petiolate leaves at the top. Petioles are usually longer or as long as the leaf blades and cross-veins are present. Leaf margins are smooth or serrate and leaf surface is naked or hairy. In female flowers, 3 to 6 No. 4 YIP K-L et al.: Halophila minor, a new record with taxonomic notes from Hong Kong 459 styles are present (Kuo & den Hartog, 2001). Besides the two species described below, Halophila australis Doty & Stone (known from South Australia) and H. ovata Gaudich. (known from the Indo-Pacific Region) also belong to this section. 1. Halophila minor (Zoll.) den Hartog in Steenis, Flora Malesiana, Ser. I, 5 (4): 410. 1957; Kuo & den Hartog in Short & Coles, Global Seagrass Research Methods, 50. 2001.ww Lemnopsis minor Zoll. in Syst. Verz. 1: 75. 1854. Type: Indonesia. Lesser Sunda Islands, Flores, 1847-07-12, Zollinger 3334 (holotype, L; isotypes, BM, P, U) (Kuo, 2000; Sachet & Fosberg, 1973). Halophila lemnopsis Miq., Fl. Ind. Bat. 3: 230. f. 176. 1856. Halophila ovata auct. non Gaudichaud: *Hodgkiss & Morton in Memoirs of the Hong Kong Natural History Society 13: 28–32. 1978; *Hong Kong Herbarium, Check List of Hong Kong Plants 73. 1978 et 77. 1993 [quoad specim. 1978-05, Morton s.n. (HK 33276); 1971-06-23, Thrower s.n. (HK 30426)]. 小喜盐草 Figs. 1, 2 Fig. 1. Halophila minor. Dried plant specimen showing Fig. 2. Halophila minor. Leaf showing veins (AFCD habit (AFCD Marine Parks Division, s.n., HK 38543). Marine Parks Division, s.n., HK 38543). Leaf blades ovate, 6–12 mm long, 3.5–6 mm wide with (4–)7–12 occasionally branched cross-veins, space between intramarginal veins and blade margin narrow. Dioecious. Male flowers with tepals l.5 mm long, anthers 2.5–3.5 mm long. Female flowers with 3 styles, 8–20 mm long. Fruits 2–3.5 mm in diam. (Kuo & den Hartog, 2001). Distribution: China (Hong Kong, Hainan and Nansha Islands), Indo-Pacific Region. Specimens examined: China. Hong Kong (香港): Ho Chung (蚝涌), AFCD Biodiversity Survey (渔护署生物多样性调查) s.n. (HK 39894); Hoi Ha (海下), AFCD Marine Parks Division (渔护署海岸公园科) s.n. (HK 38543); Hong Kong Island (香港岛), Tai Tam Bay (大潭湾), S. L. Thrower s.n. (HK 30426), B. S. Morton s.n. (HK 33276); Lantau Island (大屿山), Yam O (阴澳), AFCD Biodiversity Survey (渔护署生物多样性调查) s.n. (HK 38544); To Kwa Ping (土瓜坪), AFCD Biodiversity Survey (渔护署生物多样性调查) s.n. (HK 38542); Tsam Chuk Wan (斩竹湾), AFCD Biodiversity Survey (渔护署生物多样性调查) s.n. (HK 39895). 2. Halophila ovalis (R. Br.) Hook. f., Fl. Tasm. 2: 25. 1858; den Hartog in Steenis, Fl. Malesiana, Ser. I, 5 (4): 408. 1957; Kuo & den Hartog in Short & Coles, Global Seagrass Research Methods 50. 2001; Y. P. Yang in Fl. Taiwan, ed. 2, 5: 15. 2000; H. Q. Wang & X. 460 Acta Phytotaxonomica Sinica Vol. 44 Z. Sun in Fl. Reip. Pop. Sin. 8: 186. 1992; K. F. Zhao & F. T. Li, Halophytes of China 320. 1999.——Caulinia ovalis R. Br. in Prod. Fl. Nov. Holl. 1: 339. 1810. Type: Australia. Tasmania, R. Brown 5816 (holotype, BM) (Doty & Stone, 1967). Halophila minor auct. non (Zoll.) Hartog: Xing, Ng & Chau in Memoirs of the Hong Kong Natural History Society 23: 122. 2000. Halophila ovata auct. non Gaudichaud: Dunn & Tutcher in Bull. Misc. Inform., Addit. Ser. 10: 257. 1912; Fong in Asian Marine Biology 16: 111. 1999. 喜盐草 Figs. 3, 4 Fig. 3. Halophila ovalis. Dried plant specimen showing Fig. 4. Halophila ovalis. Leaf showing veins (Y. W. Lam habit (Y. W. Lam s.n., HK 38568). s.n., HK 38568). Rhizome internodes and petiole up to 10 cm long. Leaf blade varies in shape from oblong-elliptic, Spatulate, obovate, to ovate, rarely linear, 10–40 mm long, 5–20 mm wide, with 12–28 often branched cross-veins on either side of the midrib. Dioecious. Male flowers with tepals 3–5(–6) mm, anthers 1.5–2.5 mm long. Female flowers with 3 styles, 10–40 mm long. Fruits 3–6 mm in diam. Seeds subglobose (Kuo & den Hartog, 2001). This species is the most common seagrass in the tropical and subtropical regions of the Indo-West Pacific and inhabits various environments, resulting in considerable morphological variation (Kuo & den Hartog, 2001). Distribution: China (Hong Kong, Guangdong, Taiwan, Hainan and Nansha Islands), North Pacific, South Africa, Indo-Pacific and South Australia. Specimens examined: China. Hong Kong (香港): Lai Chi Wo (茘枝窝), AFCD Biodiversity Survey (渔护署生物多样性调 查) s.n. (HK 39897); Lantau Island (大屿山), San Tau (散头), Y. W. Lam (林英伟) 794 (HK 36160), 821 (HK 36161), s.n. (HK 38567, HK 38568); Kai Kuk Shu Ha (鸡谷树下), Y. W. Lam (林英伟) s.n. (HK 38570); Siu Tan (小滩), AFCD Biodiversity Survey (渔护署生物多样性调查) s.n. (HK 39898). Halophila sect. Microhalophila Ascherson Plants in this section are delicate, minute, monoecious with two scales at the base of erect lateral shoots, which bear a pseudo-whorl of 4 to 10 leaves at the top. The leaf blades, with naked surface and smooth or slightly serrulate margins, lack cross-veins. The male and female flowers develop on different floral shoots of the same plant (Kuo & den Hartog, 2001). Halophila beccarii, which occurs in Hong Kong, is the only species classified in this section (Kuo & den Hartog, 2001). 3. Halophila beccarii Asch. in Nuov. Giorn. Bot. Ital. 3: 302. 1871; Fl. Malesiana, Ser. I, 5 (4): 411. 1957; Kuo & Hartog in Short & Coles, Global Seagrass Research Methods 50. 2001; No. 4 YIP K-L et al.: Halophila minor, a new record with taxonomic notes from Hong Kong 461 Y. P. Yang in Fl. Taiwan, ed. 2, 5: 15. 2000; H. Q. Wang & X. Z. Sun in Fl. Reip. Pop. Sin. 8: 188. 1992. Type: Borneo. Sarawak, near the mouth of Bintula River, Beccari 3666 (isotype, S) (den Hartog, 1957). 贝克喜盐草 Thin rhizomes with 2 scales covering the base of the erect stem bearing a group of 4–10 leaves at the top. Blades lanceolate, up to 13 mm long, 1–2 mm wide, with pointed apex but lacking cross-veins. Female flowers with 2 styles, 10–15 mm long. Fruits ellipsoid to ovoid, 4–5 mm by 1.2 mm. Seeds globose, 1.2×1 mm. The lack of cross-veins clearly distinguishes this species from other Halophila species. The species is usually associated with mangrove communities and often exposed at low tide (Kuo & den Hartog, 2001), and has high fecundity and rapid rhizome extension rates so that it can colonize some areas in very short time and disappear quickly when unfavourable conditions come (Fong, 1999). Distribution: China (Hong Kong, Hainan, Guangdong, Taiwan), Indo-Pacific Region. Specimens examined: China. Hong Kong (香港): Ha Pak Nai (下白泥), Y. W. Lam (林英伟) 698 (HK 36162); Hong Kong Island (香港岛), Tai Tam Bay (大潭湾), B. S. Morton s.n. (HK 33275); Lantau Island (大屿山), Tai Ho Wan (大蚝湾), Y. W. Lam (林英伟) 667 (HK 36163); Nam Chung (南涌), AFCD Biodiversity Survey (渔护署生 物多样性调查) s.n. (HK 39064); Tsim Bei Tsui (尖鼻咀), B. S. Morton s.n. (HK 33274). 3 Dubious records Halophila ovata auct. non Gaudichaud The species Halophila ovata was first published in: Freycinet, Voy. Bot. 430. t. 40 f. 1. 1829. The type specimen, Gaudichaud s.n. (P), was collected in Mariana Islands, but the exact locality and date are unknown (Kuo, 2000). Based on our examination of herbarium specimens, all records previously reported under the name “Halophila ovata” in the Hong Kong SAR are mostly misidentifications of H. ovalis and in rare cases H. minor. Vegetatively, H. ovata is a species similar in size to H. minor but much smaller in leaf length and fewer in the number of cross-veins. Moreover, H. ovata is distributed chiefly in the southeastern part of the Indo-Pacific Region such as in the Philippines, Guam and Micronesia Islands, whereas H. minor is known from the northern and western part of the same region (including Kenya, India, Malaysia and northern Australia) and has a disjunct distribution (Kuo & den Hartog, 2001). The “Halophila ovata” described and illustrated by Hodgkiss and Morton (1978b) is a misidentification of H. minor (which is treated in this paper, after a re-examination of a voucher specimen deposited in HK). Halophila minor and H. ovata can be distinguished by several major characters (Kuo, 2000; Kuo & den Hartog, 2001) as shown in Table 1. Table 1 Distinguishing morphological characters of Halophila ovata and H. minor Character H. ovata H. minor Space between intramarginal vein and blade margin 0.4–0.6 mm 0.15–0.19 mm Space between two cross-veins 1–1.75 mm 0.65–0.85 mm Number of cross-veins 4–8 (4–)7–12 (–13) Branching of cross-veins never branched rarely branched The name Halophila minor (Zoll.) den Hartog listed by Xing et al. (2000) is followed by citing a synonym, H. ovata Gaudich., and localities at Tung Chung and Lai Chi Wo. That synonymy was likely based on the previous understanding (e.g. den Hartog, 1970) and earlier 462 Acta Phytotaxonomica Sinica Vol. 44 records. Fong (1999) stated that “H. ovata” was known from three localities in the Hong Kong SAR, namely San Tau in Tung Chung, Sheung Sze Wan in Sai Kung and Lai Chi Wo. So far, based on recent field surveys and herbarium records, no authentic specimen of H. minor is known from Tung Chung and Lai Chi Wo. The “Halophila minor” reported in Xing et. al. (2000) and the “Halophila ovata” reported in Fong (1999) were likely based on misidentification of H. ovalis. 4 Discussion Despite the fact that some authors considered H. ovata and H. minor as being conspecific, Kuo (2000), based on detailed studies of specimens from their ranges of distribution including the use of electron microscopy, has confirmed that the two species are distinct. The world distribution of these two species are also different. The recent publications by Kuo (2000) and Kuo & den Hartog (2001) of the worldwide distribution and taxonomy of seagrasses including Halophila provide a vast reservoir of information on seagrass taxonomy and ecology and thus permit correct identifications of the species. Halophila minor was previously overlooked in the Hong Kong SAR probably owing to the reliance on the outdated taxonomy and misapplied names in local literature. This paper reports H. minor as a new record of a third species of the genus Halophila in the Hong Kong SAR, in addition to the two known species, H. ovalis and H. beccarii (Hong Kong Herbarium, 2004), and confirms that H. ovata does not occur in the Hong Kong SAR although the species name appeared in previous literature. This also represents the first locality of the species in continental China besides the reported localities in Hainan and Nansha Islands (Xing & Wu, 1996; Zhao & Li, 1999). Seagrasses are of local conservation concern, as the coastal environment of the Hong Kong SAR has been subject to the threat of rapid infrastructure development. This paper has only addressed the taxonomic aspect of Halophila. A better understanding of the ecology of Halophila species is required. Field observations revealed that the species could occupy a long stretch of intertidal area under favourable conditions. However, the populations could disappear or reduce greatly in coverage in the next year without apparent observed changes or disturbance to the habitat. Understanding the ecology of Halophila, in particular, habitat requirements, life-history patterns as well as reproductive and dispersal strategies would be useful in formulating appropriate conservation measures for Halophila. Acknowledgements We gratefully acknowledge the assistance of Dr. John KUO (University of Western Australia) who kindly provided relevant information and his expert advice regarding Halophila. We also thank Prof. WU Telin (IBSC) for his valuable advice and discussion. The assistance of the Costal Community Working Group of AFCD Biodiversity Survey in providing fresh specimens for examination and that of Mr. SO Pui-Sang (HK) in imaging are also acknowledged. The senior author would like to thank Dr. Tim UTTERIDGE (K) and Dr. Roy VICKERY (BM) for their assistance provided during his recent visits to the Herbarium of the Royal Botanic Gardens, Kew and the Department of Botany, The Natural History Museum, London. References Den Hartog C. 1957. Halophila Du Petit-Thouars. In: van Steenis C G G J ed. Flora Malesiana. Groningen: Noodhoff. 5: 407–413. Den Hartog C. 1970. Sea-grasses of the World. Amsterdam: North-Holland Publ. Co. Doty M S, Stone B C. 1967. Typification for the generic name Halophila Thouars. Taxon 16: 414–418. Dunn S T, Tutcher W J. 1912. Flora of Kwangtung and Hong Kong (China). London: HMSO. No. 4 YIP K-L et al.: Halophila minor, a new record with taxonomic notes from Hong Kong 463 Fong T C W. 1999. Conservation and management of Hong Kong seagrasses. Asian Marine Biology 16: 109–121. Hance H F. 1872. Florae Hongkongensis Supplementum. Journal of the Linnean Society, Botany 13: 95–144. Hodgkiss I J, Morton B. 1978a. Zostera nana Roth. (Potamogetonaceae)—a new record for Hong Kong. Memoirs of the Hong Kong Natural History Society 13: 23–27. Hodgkiss I J, Morton B. 1978b. Halophila beccarii Ascherson (Hydrocharitaceae)—a new record for Hong Kong, with notes on other Halophila species. Memoirs of the Hong Kong Natural History Society 13: 28–32. Hong Kong Herbarium (香港植物标本室). 2004. Check List of Hong Kong Plants 2004 (香港植物名录 2004). Hong Kong: Agriculture, Fisheries and Conservation Department. Kuo J. 2000. Taxonomic notes on Halophila ovata and Halophila minor. Biologia Marina Mediterranea 7 (2): 79–82. Kuo J, den Hartog C. 2001. Seagrass taxonomy and identification key. In: Short F T, Coles R G eds. Global Seagrass Research Methods. Amsterdam: Elsevier Science. 31–58. Kwok W, Yang J, Tong P, Lam C P. 2005. Distribution of seagrasses in Hong Kong. Hong Kong Biodiversity (8): 12–14. Sachet M-H, Fosberg F R. 1973. Remarks on Halophila (Hydrocharitaceae). Taxon 22: 439–443. Wang H-Q (王徽勤), Sun X-Z (孙祥钟). 1992. Halophila Thou. In: Flora Reipublicae Popularis Sinicae (中国 植物志). Beijing: Science Press. 8: 185–190. Wu T-L (吴德邻), Hu Q-M (胡启明), Xia N-H (夏念和). 2002. Check List of Hong Kong Plants 2001 (Chinese Version) (香港植物名录2001, 中文版). Hong Kong: Agriculture, Fisheries and Conservation Department. Xing F-W (邢福武), Wu T-L (吴德邻). 1996. Flora of Nansha Islands and their Neighbouring Islands (南沙群 岛及其邻近岛屿植物志). Beijing: China Ocean Press. Xing F-W, Ng S-C, Chau K-C. 2000. Gymnosperms and angiosperms of Hong Kong. Memoirs of the Hong Kong Natural History Society 23: 21–135. Zhao K-F (赵可夫), Li F-T (李法曾). 1999. Halophytes of China (中国盐生植物). Beijing: Science Press. 喜盐草属在中国香港特别行政区的 新记录及分类补注 叶国梁* 黎存志 (香港植物标本室, 渔农自然护理署, 香港九龙长沙湾道303号737室) 摘要 报道小喜盐草Halophila minor (Zoll.) den Hartog在香港的首次记录, 同时也是除沿海岛屿(海南 及南沙群岛)以外中国大陆的首次记录。喜盐草属在中国最早的记录可追溯至1856年(香港九龙湾), 包 括喜盐草H. ovalis及贝克喜盐草H. beccarii在内, 目前已知3种喜盐草属植物分布香港。尽管从前小喜盐 草及圆叶喜盐草H. ovata曾作同种处理, 现已有最新证据清楚区别这两种喜盐草(本文证实圆叶喜盐草 不产香港)。因本属的世界分布及分类最近已被全面修订, 使得准确鉴别各种喜盐草成为可能。香港的 海岸面对高速发展, 海草的保育尤需关注。 关键词 喜盐草属; 小喜盐草; 喜盐草; 贝克喜盐草; 圆叶喜盐草; 新记录; 检索; 香港 分种检索表 1. 叶卵形至椭圆形, 侧枝短, 长1 cm或以下, 多不明显, 节上生1对叶片; 具横脉, 与中脉和缘脉相连。 2. 叶片长 6–13 mm, 具7–12对横脉, 横脉与中脉交角为 70o–90o……………1. 小喜盐草 H. minor 2. 叶片长10–40 mm, 具12–25对横脉, 横脉与中脉交角为45o–60o………………2. 喜盐草 H. ovalis 1. 叶长椭圆形至披针形; 侧枝较长, 长 l–1.5 cm, 叶片 6–10 枚簇生枝顶; 无横脉, 仅具有中脉和缘 脉………………………………………………………………………………3. 贝克喜盐草 H. beccarii

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