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Korean J. Pl. Taxon > Volume 53(1); 2023 > Article
HYUN, JUNG, NA, HAN, KANG, LEE, CHOI, and CHO: New records and distribution of three taxa in Korea: Leuzea chinensis (Asteraceae), Symplocos nakaharae (Symplocaceae), and Epilobium parviflorum (Onagraceae)

Abstract

Leuzea chinensis (S. Moore) Susanna (Asteraceae), a previously unrecorded species in Korea, was found in Yeongdeok-gun, Gyeongsangbuk-do. Symplocos nakaharae (Hayata) Masam. (Symplocaceae), which had been recorded in the literature but whose native habitat was yet to be identified, was found in Geojedo Island, Gyeongsangnam-do. It was confirmed that Epilobium parviflorum Schreb. (Onagraceae) grew naturally on the islands of Jeollanam-do. Detailed morphological descriptions and geographical distribution of the three taxa are provided.

INTRODUCTION

As detailed studies of the flora and taxonomy in the Korean Peninsula progress, new taxa continue to be published and unrecorded plants continue to be reported (e.g., Symplocarpus koreanus J. S. Lee, S. H. Kim & S. C. Kim, Lee et al., 2022; Sparganium subglobosum Morong, Lim et al., 2017). Moreover, several reports include important taxonomic information about plants whose names were only recorded in past. For example, Fimbristylis ovata (Burm.f.) J. Kern was collected on Jejudo Island in 1908 (Taquet 2081, K) and was listed only on an old Korean plant list (Park, 1949). No other specimen or record existed until its current distribution was reported on Marado Island (Kim and Kim, 2018). The present study contains descriptions and the distributions of three taxa consisting of two unrecorded species and one species for which habitation is uncertain in Korea.
Leuzea chinensis (S. Moore) Susanna of the family Asteraceae is known to be endemic to China and is distributed in Guangdong, Guizhou, Hubei, Jiangxi, and Sichuan (Martins, 2006b). The taxon was published as a member of the genus Serratula L. (Moore, 1875). Later, it was transferred to several genera due to its confusing characteristics, such as its branched inflorescence and the rounded apex of its phyllaries (Kitagawa, 1979; Martins, 2006a, 2006b). To resolve these nomenclatural and taxonomic problems, all taxa treated as Rhaponticum, including L. chinensis, were transferred to Leuzea DC. (Holub, 1973; Susanna, 2022). The habitat of L. chinensis was initially discovered in Korea, and the plant was compared with three domestic taxa consisting of one previously reported Leuzea species and two subspecies of Serratula with similar features.
Symplocos nakaharae (Hayata) Masam. of the family Symplocaceae in Korea was previously announced as S. lucida (Thunb.) Siebold & Zucc. and was recorded as distributed on Jejudo Island (Liu, 1962; Ohwi, 1965; Ahn et al., 1982; Kitamura and Murata, 1984; Satake et al., 1989). The Korean name of this species was recorded originally by Lee and Ahn (1963) as ‘Sa-cheol-keom-eun-jae-na-mu’, but Kim (2007) and Park et al. (2007) excluded it from Korean flora because no specimen had been collected in Korea. In addition, S. nakaharae was once considered to be endemic to Japan, as the only known habitat for this plant was southern Japan (Nagamasu, 1987, 1993; Liu and Qin, 2013). We have confirmed that the distribution of S. nakaharae includes Geojedo Island in Gyeongsangnam-do. Whether it is native to Korea, however, remains uncertain.
Epilobium L. is the largest genus in the family Onagraceae, with approximately 160 species distributed around the world (Chen et al., 1992). In Korea, nine taxa of the genus Epilobium are known to be native. Except for Epilobium ciliatum Raf. and E. fastigiatoramosum Nakai, which are distributed in North Korea, seven taxa grow wild in South Korea: E. hirsutum L., E. pyrricholophum Franch. & Sav., E. amurense Hausskn. subsp. amurense, E. amurense subsp. cephalostigma (Hausskn.) C. J. Chen, Hoch & P. H. Raven, E. platystigmatosum C. B. Rob., E. palustre L., and E. ulleungensis J. M. Chung (Lee et al., 2013; Chung et al., 2017). We discovered Epilobium parviflorum Schreb., which grows naturally on several islands of Jeollanam-do.

TAXONOMIC TREATMENT

1. Leuzea chinensis (S. Moore) Susanna, Collect. Bot. 41: e005-2, 2022; Serratula chinensis S. Moore, J. Bot. 13: 228, 1875; Klasea chinensis (S. Moore) Kitag., Neolin. Fl. Manshur. 654, 1979; Rhaponticum chinensis (S. Moore) L. Martins & Hidalgo, Bot. J. Linn. Soc. 152: 461, 2006; Klaseopsis chinensis (S. Moore) L. Martins, Taxon 55: 974, 2006.—Type: CHINA, 1873, Shearer, G. s.n. (isotype: K, photo!)
Korean name: Yeong-deok-chwi (영덕취).
Herb, perennial, 90–160 cm tall. Roots adventitious. Rhizomes elongated. Stem erect, sulcate, branched at the upper part, base glabrous, above villous. Leaves basal and cauline, alternate; basal leaves elliptic or pinnately lobed, falling at anthesis; lower cauline leaves, petioles 2–15 mm long, pubescent, blade elliptic to ovate, 2.0–19.0 × 3.0–9.0 cm, base attenuate, apex dentate, acute, both surface papillate; upper cauline leaves petioles 1.0–4.0 mm long, blade ovate, 2.0– 10.0 × 0.8–5.0 cm. Inflorescences capitula, one at terminus of stem or branches; bracts 1 or 2, 1.0–11.5 × 0.2–5.0 mm, pubescent. Capitulum 3.5–4.2 × 3.3–3.9 cm; involucre bell-shaped, 6 or 7 rows, 1.8–2.1 cm long; outer phyllaries triangular, 1.4–3.5 × 1.2–3.0 mm, pillose; median phyllaries wide ovate to ovate, 4.0–13.2 × 3.0–4.6 mm, base light green or yellow, apex rounded and green, vein distinct, glabrous; inner phyllaries ovate to oblong, 14.5–18.5 × 2.5–4.5 mm, glabrous. Lateral florets 8.5–17.0 × 1.2–2.6 mm; corolla limb purple, 5.8–7.5 mm long, terminal margin 4(–8) lobed; stamens 4(3–5), style 1, persistent. Disk florets 1.3–15.0 × 0.6–0.9 mm. Achenes brown, narrowly oblong, 7.5–8.2 × 1.5– 2.2 mm; pappus light yellow, outer bristles 1.0–2.4 mm long, inner bristles 12.0–14.5 mm long (Fig. 1).
Flowering: August to October.
Fruiting: September to October.
Distribution and habitat: China, Korea. A population of Leuzea chinensis was found in a Quercus dentata forest on the ridge of a mountain in Yeongdeok-gun, Gyeongsangbuk-do in Korea. The population area was 40 × 50 m2. The vegetation structure of the population showed that the tree layer consisted of Ulmus davidiana var. japonica (Rehder) Nakai, Q. dentata, Q. mongolica Fisch. ex Ledeb., and Fraxinus rhynchophylla Hance. In the shrub layer, Ligustrum japonicum Thunb., Acer pictum var. mono (Maxim.) Franch., Actinidia arguta (Siebold & Zucc.) Planch. ex Miq., and Vitis amurensis Rupr. grew. The herb layer was composed of Persicaria thunbergii (Siebold & Zucc.) H. Gross, Ligularia fischeri (Ledeb.) Turcz., Impatiens nolitangere L., Pimpinella brachycarpa (Kom.) Nakai, and Chloranthus japonicus Siebold. The basal leaves and lower cauline leaves wither in the flowering season.
Specimens examined: KOREA. Gyeongsangbuk-do: Yeongdeok-gun, Mt. Myeongdongsan, 14 Aug 2021, J.O. Hyun & M. K. Lee s.n. (KB, KH, NNH, HIBR).
Rhaponticum was frequently used as a genus name of a group of related taxa. Rhaponticum was considered to be a synonym of Centaurea L., and most of the species were transferred to Leuzea (Holub, 1973). Before the recombination of L. chinensis by Susanna (2022), L. chinensis was considered to be a member of Serratula L. (Moore, 1875), Klasea Cass. (Kitagawa, 1979), Rhaponticum Ludwig. (Martins, 2006b), or Klaseopsis L. Martins (2006b) based on the morphologies or molecular phylogenetic relationships (Martins and Hellwig, 2005a, 2005b). Monophyly of Leuzea was confirmed in a molecular phylogenetic study using nearly all Leuzea species (except L. chinensis) (Hidalgo et al., 2006). A phylogenetic analysis using the nuclear ITS region was conducted in the present study, and L. chinensis was found to be nested with Leuzea species in the phylogenetic tree (GenBank accession number: OQ429292, tree not shown). Therefore, L. chinensis (S. Moore) Susanna was accepted in this study. Although the branched stem with several capitula of L. chinensis is similar to those of Korean Serratula species (Kim et al. 2007), the rounded apex of the phyllaries in L. chinensis differentiates it from the Serratula species. A related species, L. uniflora (L.) Holub, is easily distinguished from L. chinensis by the lobed blade of its cauline leaves and by its larger solitary head.

Key to Leuzea chinensis and related taxa in Korea

  • 1. Phyllaries apex rounded, without a spinule ······················· ···················································· Genus Leuzea 뻐꾹채속

    • 2. Stem branched, cauline leaves unlobed ······················· ··················· L. chinensis (S. Moore) Susanna 영덕취

    • 2. Stem unbranched, cauline leaves pinnatipartite or subpinnatisect ············ L. uniflora (L.) Holub 뻐꾹채

  • 1. Phyllaries apex acute, with a spinule ································· ············································ Genus Serratula 산비장이속

    • 3. Hair of involucre dense, yellowish brown, phyllaries reddish brown, with a long spinule ····························· ······· S. coronata L. subsp. manshurica (Kitag.) O. S. Zhirova 북방산비장이

    • 3. Hair of involucre sparse, yellowish brown, phyllaries green, with a short spinule ············································ ··· S. coronata L. subsp.insularis (Iljin) Kitam. 산비장이

2. Symplocos nakaharae (Hayata) Masam. in Trans. Nat. Hist. Formosa 30: 62, 1940; Symplocos japonica A. DC. var. nakaharae Hayata in Icon. Pl. Formosan. 5: 103, 1915; Symplocos lucida (Thunb.) Siebold & Zucc. var. nakaharae (Hayata) Makino & Nemoto in Fl. Japan. ed. 2. 373, 1925; Bobua japonica (A. DC.) Miers var. nakaharae (Hayata) Sasaki in Cat. Govt. Herb. 407, 1930; Dicalix lucida (Thunb.) Hara var. nakaharae (Hayata) Hara in Enum. Spermatophytarum Japon. 1: 106, 1948.—Type: JAPAN. Ryukyus: Mt. Nago-take, Okinawa Islands, G. Nakahara s.n. (holotype: TI).
Laurus lucida Thunb. in Syst. Veg. ed. 14. 384, 1784; Hopea lucida (Thunb.) Thunb. in Ic. Jap. t. 14, 1800; Symplocos lucida (Thunb.) Siebold & Zucc. in Fl. Jap. (Siebold) 1: 55. t. 24, 1838. non Wall. ex G. Don, 1837; Bobua lucida (Siebold & Zucc.) Kaneh. & Sasaki in List Pl. Formosa 331, 1928; Dicalix lucida (Thunb.) H. Hara in Enum. Spermatophytarum Japon. 1: 105, 1948.—Type: JAPAN. Thunberg s.n. (holotype: UPS).
Korean name: Sa-cheol-geom-eun-jae-na-mu (사철검은 재나무).
Evergreen trees, up to 15 m tall. Twigs ashy brown, terete; young twigs yellowish green, glabrous, ridged below petioles; terminal buds 7–13 mm long, narrowly ovoid to subulate, acute to acuminate, often curved at apex, glabrous. Leaves alternate, petioles 0.4–1.0 cm long, glabrous, adaxially sulcate; blades coriaceous, elliptic, 5.0–7.1 × 1.6–3.1 cm, base cuneate to shortly attenuate, apex rounded, obtuse to acuminate, margin recurved, entire or glandular-crenate with teeth 4– 10 mm apart; both surfaces glabrous, midrib prominent, nerves 5–8 pairs, slightly prominent. Inflorescence axillary, contracted raceme or spike, 2–5 mm long, axis puberulous; bracts and bracteoles persistent, inside glabrous, outside sparsely appressed pubescent, margin ciliolate; bracts ovate to semiorbicular, 1–2 mm long, apex rounded or obtuse; bracteoles depressed ovate, 1–2 mm long, apex rounded, obtuse or acute. Flowers bisexual, calyx lobes widely ovate to ovate, 1–2 mm long, apex rounded or obtuse, glabrous, ciliolate; corolla white or yellowish-white, 4–8 mm long, 5-lobed, lobes elliptic; stamens 20–30, pentadelphous; disk raised, densely soft pilose; style 3.5–4.5 mm long, glabrous; ovary 3 locular. Fruits bluish black, ellipsoidal, 5.3–10.5 mm long, 4.7–7.7 mm in diameter, excluding blunt beak formed by the persistent calyx lobes (Fig. 2).
Flowering: March–April and November–January (The flowers blooming in winter are heteromorphic types and most of them do not develop into fruits; Fig. 2. L).
Fruiting: August–September.
Distribution and habitat: Symplocos nakaharae is newly recorded from Geojedo Island, Geoje-si, Gyeongsangnam-do in Korea. More than 200 individuals, the tallest one being 15 m tall and 23 cm in diameter at breast height, were distributed over an area of 26,000 m2 at 30–100 m a.s.l. on a slope near the coast. The vegetation structure of the population showed that the tree layer was composed of Pinus thunbergii Parl., P. densiflora Siebold & Zucc., Quercus variabilis Blume, Eurya japonica Thunb., and other species, and was dominated by P. thunbergii and P. densiflora. In the subtree layer, E. japonica was dominant and Fraxinus sieboldiana Blume, Ligustrum japonicum Thunb., L. obtusifolium Siebold & Zucc., and Lindera erythrocarpa Makino were the major species. The shrub layer was composed of Rubus tozawae Nakai ex J. Y. Yang, Zanthoxylum piperitum (L.) DC., and Akebia quinata (Houtt.) Decne. The major species in the herb layer were Rhododendron mucronulatum Turcz., Ardisia japonica (Thunb.) Blume, Oplismenus undulatifolius (Ard.) Roem. & Schult., and Trachelospermum asiaticum (Siebold & Zucc.) Nakai.
Specimens examined: KOREA. Gyeongsangnam-do: Geoje-si, Geoje Island, 4 Dec 2021, J.O. Hyun, Y.M. Choi and W.R. Cho, s.n. (KB, KH); 2 Apr 2022, J.O. Hyun, B.W. Han and Y.M. Choi, s.n. (KB, KH, NNH, HIBR); 11 Aug 2022, B.W. Han, M.S. Choi, Y.M. Choi and W.R. Cho, s.n. (KB, KH, NNH, HIBR).
Symplocos nakaharae is not considered to be distributed on the Korean Peninsula, as it has been recorded as S. lucida only in a few studies, and there are no observed records and no specimens collected from Korea. With this study as an opportunity, it is necessary to investigate the distribution of these types of plants more accurately through a close examination and to reflect the results on the plant list of the Korean Peninsula. Other examples include Clethra barbinervis Siebold & Zucc., Taeniophyllum glandulosum Blume, and Actaea cimicifuga L. On the other hand, S. nakaharae as reported in the present study, is considered one of the S. nakaharae complex, with morphological characteristics that slightly differ from the results observed in the latest study (Liu and Qin, 2013). Accordingly, additional research is needed.

Key to Symplocos species in Korea, modified from Kim (2007)

  • 1. Leaves deciduous; inflorescences terminal, panicles

    • 2. Bark transversely fissured; leaves ovate to elliptic, lower surface glaucous; drupes black at maturity ······ ······························· S. tanakana Nakai 검노린재나무

    • 2. Bark longitudinally fissured or exfoliating; leaves obovate, elliptic, oblong or ovate, lower surface pale green but not glaucous; drupes blue or dark blue at maturity

    • 3. Leaves obovate to elliptic, apex acute to acuminate, margin serrulate; panicles with a few small leaves; drupes blue ··· S. sawafutagi Nagam. 노린재나무

    • 3. Leaves ovate to obovate, apex acuminate to caudate, margin glandular dentate; panicles without leaves; drupes dark blue ······················································· ············ S. coreana (H. Lév.) Ohwi 섬노린재나무

  • 1. Leaves persistent; inflorescences axillary, racemes

    • 4. Young twigs gray; midrib of leaf impressed on upper surface, prominent on lower surface; racemes 10 to 30- flowered; bracts and bracteoles caducous; seeds straight ····· S. sumuntia Buch.-Ham. ex D. Don 검은재나무

    • 4. Young twigs green; midrib of leaf prominent on both surfaces; racemes contracted, 3- to 8-flowered; bracts and bracteoles persistent; seeds J-shaped to slightly curved ···· ········ S. nakaharae (Hayata) Masam. 사철검은재나무

3. Epilobium parviflorum Schreb., Spic. Fl. Lips. 146, [155], 1771.—Type: GERMANY (not located)
Epilobium parviflorum var. vestitum Benth. ex C. B. Clarke in J. D. Hooker, Fl. Brit. India 2: 584, 1879. [Epilobium vestitum Benth. in Wallich, Numer. List 216, n.6327, 1832, nomen nudum.].—Type: NEPAL, Sheopuri Hills, near Rivulet Rocks, N of Katmandu, 1821, Wallich 6327 (holotype: K, photo!)
Korean name: Gaet-ba-neul-kkot (갯바늘꽃).
Herbs perennial, robust. Stems erect, 0.3–1.1 m tall, branched, densely greyish white villous, and glandular puberulent distally. Leaves opposite, alternate distally, subsessile or lower ones with petioles 1–2 mm long, sessile distally; middle cauline blade broadly lanceolate to oblong-lanceolate, 30–105 × 5–22 mm, base rounded to cuneate, apex acute, margin serrulate, both surfaces villous. Inflorescences racemes or leafy panicles. Flowers erect, pedicels 1–3 mm long; sepals 4, lanceolate, 2.5–5.0 × 1.0–1.5 mm, covered with villous and glandular pubescence; petals 4, light pink, obovate, 4–7 × 3–4 mm, apex emarginate to obcordate, apical notch 1.0–2.5 mm; stamens 8, in two unequal whorls, filaments of longer stamens 3–6 mm long, anthers ca. 1 mm long; style white, 3–5 mm long, glabrous, stigma shallowly 4-lobed or clavate, subequal to anthers. Fruits capsule, 35–65 mm long, glandular puberulent and villous, rarely glabrescent. Seeds numerous, brown, obovoid, 0.7–1.0 × 0.3–0.4 mm, surface papillose; coma easily detached, white, 6–12 mm long (Fig. 3).
Flowering and fruiting: June to September.
Distribution and habitat: Southern islands of Korea. It grows with emergent plants such as Phragmites australis (Cav.) Trin. ex Steud., Juncus and Typha in abandoned paddy fields, wet meadows near reservoirs and ditches around coastal regions. It is native to Eurasia, from Japan and China to the Caucasus and Europe and North Africa, and was introduced in North America and New Zealand.
Specimen examined: KOREA. Jeollanam-do: Sinan-gun: Anjwa-myeon, Jara-ri, Jarado Island, 18 Jun 2019, B.W. Han 19061825 (KB, KH, HIBR); 30 Jul 2019, B.W. Han 19073002 (KB, KH, HIBR); Bakji-ri, Bakjido Island, 30 Jul 2019, B.W. Han 19073001 (KB, KH, HIBR); Palgeum-myeon, Jingo-ri, Palgeumdo Island, 3 Aug 2020, M.K. Lee 20080325 (KB, KH); Jangsan-myeon Paengjin-ri, Jangsando Island, 5 Aug 2020. M.K. Lee 20080535 (KB); Wando-gun: Gogeummyeon, Sedong-ri, Gogeumdo Island, 16 Aug 2017, M.K Lee 17081601 (KB, KH, HIBR); Cheongsan-myeon, Cheonggyeri, Cheongsando Island, 21 Jul 2021, K.S. Kang 21072174 (KB, KH, HIBR); Wando-eup, Daesin-ri, Wando Island, 22 Jul 2021, K.S. Kang 21072256 (KB, HIBR).
This species is registered as a cultivated plant on the “Standard Checklist of Cultivated Plants in Korea” (Lee et al., 2016). However, it is considered a native plant owing to its discontinuous distribution on the southern islands of Korea and its nativity to two neighboring countries, China and Japan (Chen et al., 1992). The shape of the stigma is the key characteristic when distinguishing Epilobium species. Epilobium parviflorum was originally described as having a distinct 4-cleft stigma with spreading lobes. However, the shape of the stigma of the Korean taxon reported in this study differs from that in the original description (Schreber, 1771). Whereas it was previously reported that the lobes of the stigma of E. parviflorum were erect in the beginning and later became recurved (Chen et al., 1992), we could not observe stigma with 4-spreading lobes at the anthesis stage. It is thus necessary to examine how certain characteristics of the shape of the stigma, including the cleft depth and lobes direction, differ in other samples.

Key to Epilobium parviflorum and related taxa in Korea

  • 1. Leaves sessile, clasping; sepals 6–10 mm long; petals 9– 20 mm long, pink to red-purple

    • 2. Stigma deeply 4-lobed ··················································· ································ Epilobium hirsutum L. 큰바늘꽃

    • 2. Stigma tetragonal ························································· ················· E. ulleungensis J. M. Chung 울릉바늘꽃

  • 1. Leaves subsessile, not clasping; sepals 2.5–5.0 mm long; petals 4–7 mm long, light pink ········································· ····································· E. parviflorum Schreb. 갯바늘꽃

NOTES

CONFLICTS OF INTEREST
The authors declare that there are no conflicts of interest.

Fig. 1.
Photographs and illustration of Leuzea chinensis (S. Moore) Susanna. A. Specimen. B. Illustration. C. Habitat. D. Whole plants. E. Basal leaves. D. Basal leaves with pinnately lobed margin. G. Inflorescences. H. Involucre. I. Corollas.
kjpt-53-1-69f1.jpg
Fig. 2.
Photographs of Symplocos nakaharae (Hayata) Masam. A. Specimen. B. Whole plant. C. Bark. D. Young twig. E. Terminal winter bud. F. Adaxial leaf surface with serrulate margin. G. Abaxial leaf surface with serrulate margin. H. Adaxial leaf surface with entire margin, I. Abaxial leaf surface with entire margin. J, K. Inflorescences in spring. L. Heteromorphic inflorescences in winter. M. Axillary infructescences and immature fruit. N. Mature fruits. O. Drupe without pericarp. P. Transverse section of fruit.
kjpt-53-1-69f2.jpg
Fig. 3.
Photographs of Epilobium parviflorum Schreb. A. Specimen. B. Habitat. C, D. Upper stems and leaves. E. Whole plants. F. Adaxial leaf surface. G. Abaxial leaf surface. H. Inflorescences. I, J. Flowers. K. Sepals and petals in a lateral view. L. Longitudinal section of flower. M. Capsules. N. Dry capsule bursting to release seeds with coma. O. Seeds.
kjpt-53-1-69f3.jpg

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