Korean J. Pl. Taxon. 50(1): 1−7 (2020) pISSN 1225-8318 eISSN 2466-1546 https://doi.org/10.11110/kjpt.2020.50.1.1 Korean Journal of RESEARCH ARTICLE

New distribution records of two rare of () in South Korea: Cynanchum thesioides (Freyn) K. Schum. and Cynanchum chinense R. Br.

Bo-Mi NAM1,2, Sungyu YANG3 and Gyu Young CHUNG1* 1Division of Horticulture & Medicinal Plant, Andong National University, Andong 36729, Korea 2International Biological Material Research Center, Korea Research Institute of Bioscience & Biotechnology, Daejeon 34141, Korea 3Herbal Medicine Resources Research Center, Korea Institute of Oriental Medicine, Naju 58245, Korea (Received 12 December 2019; Revised 10 February 2020; Accepted 12 March 2020)

ABSTRACT: Cynanchum L. in the subfamily (Apocynaceae) includes four recognized species on the Korean peninsula, two of which are native to South Korea. However, the species ranges in South Korea are poorly defined. During a field survey, we discovered C. thesioides, previously unrecorded in South Korea, in Gimpo-si, Gyeonggi-do, and found an additional population of C. chinense, for which only one population has been reported in South Korea. The two taxa are considered rare species with extremely restricted distributions in South Korea, especially C. thesioides. We provide fundamental information, including descriptions, images of the habitats and morphological characters, and a taxonomic key for identification and assessments of the con- servation status of Cynanchum species in Korea. Keywords: Cynanchum chinense, C. thesioides, new distribution, rare species, unrecorded species

Rare typically have narrow distributions and highly tomentosa C. Morren & Decne.) are on the Korean Red List specific habitats with limited and/or small populations (Içs ik, as Endangered and Vulnerable species (Korea National 2011). Many rare plants are vulnerable to habitat loss and/or Arboretum, 2008). Despite the highly narrow distributions of disturbances by environmental, human, and genetic factors glabrum (Nakai) Kitag. (= Cynanchum glabrum (Lavergne et al., 2005; Içs ik, 2011). Moreover, the International Nakai) and V. volubile Maxim. (= C. volubile (Maxim.) Union for Conservation of Nature (IUCN) has warned that Hemsl.), they are not included in the list. To establish a approximately 13% of plant species in the world are at risk of conservation management system, accurate identification and extinction (Walter and Gillett, 1998). Accordingly, many comprehensive analyses of habitats, population sizes, and countries have established a Red List and assessed their distributions of Korean Asclepiadoideae taxa are critical. threatened species. In Korea, rare plants are mainly organized Cynanchum L. is a large in the subfamily and protected by the Korea Forest Service and the Ministry of Asclepiadoideae (Apocynaceae) with approximately 200 Environment (Korea National Arboretum, 2008; National species and a wide distribution throughout the world (Liede Institute of Biological Resources, 2012). However, some and Täuber, 2002; Khanum et al., 2016). The genus is species, for which little is known about habitat types and morphologically distinguished from Vincetoxicum Wolf. by population size, are not listed. twining stems, white latex, and mostly heart-shaped leaves; it Among 15 taxa belonging to Asclepiadoideae in Korea, four also exhibits high diversity in floral structures, especially in in Cynanchum and (C. amplexicaule (Siebold & corona shapes (Khanum et al., 2016; Nam and Chung, 2018). Zucc.) Hemsl., C. japonicum (C. Morren & Decne.) Hemsl., In the Korean peninsula, Cynanchum was formerly C. inamoenum (Maxim.) Loes. ex Gilg & Loes., and M. composed of about 10–12 species, and these included

*Author for correspondence: [email protected]

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Vincetoxicum species (Lee, 1996; Lee, 2007; Korea National Arboretum, 2017). However, there are now four recognized species based on morphological and phylogenetic studies: C. chinense R. Br., C. purpureum (Pall.) K. Schum., C. thesioides (Freyn) K. Schum., and C. wilfordii (Maxim.) Hemsl. (Khanum et al., 2016; Nam and Chung, 2018). C. purpureum and C. thesioides have been reported in North Korea, C. chinense is restricted to South and North Korea, and C. wilfordii is distributed from the seashore to mountain slopes in the Korean peninsula (Lee, 1996; Im, 1999; Chang et al., 2014). We report new distribution records of two rare species, C. chinense and C. thesioides, based on a field investigation in South Korea, including the first observation of C. thesioides in the country. The aims of this study are to evaluate the distribution in South Korea of two rare species with careful morphological examination based on the original descriptions and type specimens, and to provide fundamental information for further studies assessing their conservation status.

Taxonomic Treatment

Cynanchum thesioides (Freyn) K. Schum., Nat. Pflanzenfam. 4: 252, 1895; Vincetoxicum thesioides Freyn, Oestrr. Bot. Z. 40: 124, 1890.—TYPE: RUSSIA. Dahuria, Nertschinsk, 1889, Karo, F.K. 145 (syntypes: K, barcode K000872723!; Z, barcode Fig. 1. Distribution map based on voucher specimens of Z-000001810!). Cynanchum thesioides and Cynanchum chinense in South Korea. ★, Cynanchum thesioides; ●, Cynanchum chinense. Perennial herbs. Roots long, cylindrical tuberous. Stems erect or upper part twining, ca 25 cm long, branched or not, white latex, densely pubescent. Leaves opposite, rarely 3-whorled, 0.5– 250 µm long, ca. 120 µm wide; style heads conical, 2-divided 1.8 mm long or subsessile; blades linear to narrowly lanceolate or umbonate. Fruits not seen. sometimes oblong, 2.7–4.8 cm long, 2.0–8.0 mm wide, apex acute Phenology: Flowering from July to August. Fruiting not or rarely rounded, base cordate or truncate, sometimes oblique with observed. colleters at middle part of leaf base, margin entire, ciliolate, Korean name: Yang-ban-pul (양반풀) (Lee, 1996; Chang midvein elevated abaxially, lateral veins obscure, puberulent on et al., 2014; Korea National Arboretum, 2017). both sides. umbel-like, axillary to terminal; cymules Distribution: Kazakhstan, China, Mongolia, Russia, and 1–10-flowered, solitary or clustered; peduncles 2.7–4.6 mm long, Korea (Gyeonggi-do) (Fig. 1). puberulent; pedicels 1.2–3.8 mm long, puberulent. Flowers calyx Habitat and ecology: Grows on semi-shady slopes of rocky tube very short; lobes 5, triangular 2.3–2.8 mm long, puberulent, mountains (elev. 343 m) along with Acer pictum Thunb. var. ciliate, colleters between inside lobes; corollas white-green, mono (Maxim.) Maxim. ex Franch., Lindera obtusiloba Blume, glabrous; tube very short; lobes 5, narrowly triangular to oblong, Quercus mongolica Fisch. ex Ledeb., Fraxinus rhynchophylla 3.5–4.3 mm long, mostly twisted with one direction; coronas Hance, and Securinega suffruticosa (Pall.) Rehder, among others. consisting of fused staminal and interstaminal parts at base; lobes Voucher specimen: KOREA. Gyeonggi-do: Gimpo-si, 5, laminar, triangular-lanceolate, up to middle of anthers, apex Wolgot-myeon, Munsusan Mt., 17 Aug 2019, B.-M. Nam & acute; gynostegia sessile; anthers 5, square, with white appendages, S. Y. Yang 190817-001 (ANH). triangular-ovate, as long as gynostegia; pollinaria 5; corpusculum Note: Cynanchum thesioides mainly grows in open ovoid, ca. 200 µm long, ca. 100 µm wide; caudicles ca. 150 µm disturbed areas, sand dunes, grasslands, and roadsides of long, attached to apical pollinia; pollinia pendulous, ellipsoid, ca. Kazakhstan, western China, central and Far East of Russia,

Korean Journal of Plant Taxonomy Vol. 50 No. 1 (2020) New populations of two rare Cynanchum species in Korea 3

Fig. 2. Photographs of Cynanchum thesioides in South Korea. A. Habit. B. Habitat (Gimpo-si, Gyeonggi-do). C. Root. D. Stem with latex. E. Petiole. F. Leaf. G. . H. Flower (one corolla lobe removed). I, J. Corona and gynostegium (side and front views). K. Pollinarium.

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Mongolia, and North Korea (Hwanghae-do and Ledeb., Fraxinus rhynchophylla Hance, and Securinega Pyeongannam-do) (Li et al., 1995; Lee, 1996; Im, 1999; suffruticosa (Pall.) Rehder. Two individuals flowered, and Chang et al., 2014). It is morphologically characterized by fruit set was not observed. We believe that this is the only linear to narrowly lanceolate leaves, mostly puberulent; an population in South Korea and that the species is dependent erect stem with twining apical parts; triangular-lanceolate mainly on asexual reproduction. The species can be corona lobes; and broadly fusiform follicles (Li et al., 1995) categorized as critically endangered (CR) based on the B2 (Fig. 2). During the field survey, we discovered the first criterion of IUCN (IUCN Standards and Petitions population of C. thesioides in Gimpo-si, Gyeonggi-do, Committee, 2019) because its area of occupancy in South South Korea, very close to North Korea (Figs. 1, 3A, B). Korea is smaller than 10 km2. However, to assess the The population only included 18 individuals along with Acer conservation status, an intensive investigation is required, pictum Thunb. var. mono (Maxim.) Maxim. ex Franch., including analyses of population/individual sizes with Lindera obtusiloba Blume, Quercus mongolica Fisch. ex careful taxonomic revision.

Fig. 3. Photographs of habitats of Cynanchum thesioides and Cynanchum chinense in South Korea. A, B. Habitat of C. thesioides (Gimpo-si, Gyeonggi-do). C, D. Habitat of C. chinense (Hwaseong-si, Gyeonggi-do).

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Fig. 4. Photographs of Cynanchum chinense in South Korea. A. Habitat (Hwaseong-si, Gyeonggi-do). B. Root. C. Stem with latex. D. Leaf. E. Inflorescence. F. Flower and calyx. G. Flower. H. Corona (partly removed) and gynostegium. I. Corona with appendages. J. Pollinarium. K. Gynoecium. L. Fruit. M. Seed with coma.

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Cynanchum chinense R. Br., Mem. Wern. Nat. Hist. Soc. Carex sp. (dominant species), Phragmites australis (Cav.) Trin. 1: 44, 1810.—TYPE: CHINA. Provincia Pechiley, Georgius ex Steud., Artemisia lancea Vaniot, Conyza canadensis (L.) Staunton, Baronettus, Staunton s.n. (holotype: BM, barcode Cronquist, etc. BM001014201!). Voucher specimens: KOREA. Gyeonggi-do: Hwaseong-si, C. pubescens Bunge, Enum. Pl. China Bor. 44, 1831; Namyang-eup, Munho-ri, 17 Aug 2019, B.-M. Nam & S. Y. Vincetoxicum pubescens (Bunge) Kuntze, Revis. Gen. Pl. 2: Yang 190817-002–005 (KIOM). Incheon: Ganghwa-gun, 423, 1891. Samsan-myeon, Seongmodo Isl., 2 Sep 2014, B.-M. Nam & C. deltoideum Hance, Ann. Sci. Nat., Bot., sér. 5: 228, 1866. G.Y. Chung 140902-100–109 (ANH); 9 Aug 2016, B.-M. Nam & G.Y. Chung 160809-100–103 (ANH). Perennial herbs. Roots long, cylindrical tuberous. Stems Note: Cynachum chinense mainly occurs in thickets, twining, many branched, terete, pubescent, white latex. roadsides, seashores, and riverbanks in China, Mongolia, and Leaves opposite, petiole 22.6–41.0 mm long, 1.0–1.6 mm Korea (Li et al., 1995). It is clearly distinguished from other wide; blades triangular or triangular-ovate, 1.6–7.9 cm species within the genus Cynanchum by its triangular leaves long, 3.1–7.1 cm wide, apex acute or acuminate, base with cordate bases and a tubular corona with long and slender rounded or cordate rarely truncate, 4–7 colleters at base, appendages (Nam and Chung, 2018) (Fig. 4). Previously, the margin entire, ciliolate, lateral veins 5–9 pairs, pubescent species has only been observed on the seashore and saltern usually on veins. Inflorescences axillary to terminal, areas of Is. Seokmodo, Incheon, South Korea. We found an dichasial cyme, 2 to 32-flowered, usually branched at base, additional natural population in the inland area of Hwaseong- 11.7–73.4 mm long; peduncles 1.2–29.2 mm long, 0.4– si, Gyeonggi-do (Figs. 1, 3C, D). C. chinense is considered 1.2 mm wide, pubescent; pedicels 1.5–6.0 mm long, 0.2– a rare species, found in only two locations in South Korea; 0.6 mm wide, pubescent; bracts lanceolate, 0.8–1.9 mm however, no attempts have been made to assess its long, 0.1–1.1 mm wide. Flowers calyx longer than corolla conservation status to date. To determine the correct IUCN tube; tube short; lobes 5, lanceolate, apex acute, pubescent, category, more data for population size and demographic 1–2 colleters between inside lobes; corollas white; lobes changes are needed. 5, linear-lanceolate, rounded, recurved, glabrous; coronas white; tubular, laminar, as long as gynostegium; lobes 5, Key to the genus Cynanchum fused with tube inside, apex linear, longer than in South Korea gynostegium, usually recurved; corona appendages threadlike on lobes inside, shorter than lobes; gynostegia 1. Stems erect, apically twining; leaf blades linear to sessile; anthers 5, triangular-ovate, appendages exceeding narrowly lanceolate ···················· C. thesioides (양반풀) gynostegium; lateral 2 anther wings projected on base; 1. Stems twining, leaf blades triangular to ovate anther wings parallel to each other; pollinaria 5; 2. Leaf basal lobes incurved; inflorescences dichasium; corpusculum ellipsoid, 163–300 µm long, 100–133 µm corolla lobes white; coronas tubular; follicles linear ··· wide; caudicles 60–70 µm long, attached to apical ··········································· C. chinense (가는털백미) pollinium; pollinia pendulous, ellipsoid, 233–333 µm long, 2. Leaf basal lobes not incurved; inflorescences umbellate 100–167 µm wide; style heads conical, 2-divided cyme; corolla lobes yellow-green; coronas deeply umbonate. Fruit follicles, usually one per flower, linear, lobed; follicles fusiform ············ C. wilfordii (큰조롱) 84.0–129.8 mm long, 4.6–7.5 mm wide, pubescent. Seeds 36–64 per follicle, oblong, 4.3–6.9 mm long, 1.8–3.1 mm ORCID: Bo-Mi NAM: https://orcid.org/0000-0002-6769-9317; wide, winged, brown, glabrous; comas 17.7–40.6 mm long. Sungyu YANG: https://orcid.org/0000-0001-5081-0296; Gyu Phenology: Flowering in August, fruiting from September Young CHUNG: https://orcid.org/0000-0002-4891-1140 to October. Korean name: Ga-neun-teol-baek-mi (가는털백미) Acknowledgments (Chang et al., 2014; Korea National Arboretum, 2017). Distribution: China, Mongolia, and Korea (Incheon and The authors deeply thank to Mr. C. J. Lee for providing the Gyeonggi-do) (Fig. 1). information on the habitat of C. thesioides. This research was Habitat and ecology: In Korea, the species grows in open supported by a grant (18172MFDS201) from the Ministry of areas of seashore, swamp edges, and roadsides, along with Food and Drug Safety in 2019.

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