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Short Communication
An updated checklist of Adonis (Ranunculaceae) from Korea, with a new
locality record for Adonis multiflora
Dong Chan Son
a
, Yoon-Young Kim
a
, Beom Kyun Park
b
, Bong Sik Lee
c
, Kae Sun Chang
a
,
*
a
Division of Forest Biodiversity and Herbarium, Korea National Arboretum, Pocheon-si 11186, Republic of Korea
b
Department of Biological Sciences and Biotechnology, Hannam University, Daejeon-si 34054, Republic of Korea
c
76-1 Geumsa-dong, Geumjeong-gu, Busan-si 46332, Republic of Korea
article info
Article history:
Received 9 April 2018
Received in revised form
23 May 2018
Accepted 7 July 2018
Available online 31 July 2018
Keywords:
Adonis L.
Checklist
Disjunct distribution
Korea
Ranunculaceae
abstract
Adonis multiflora Nishikawa & Koji Ito was discovered in Gijang-gun, Busan-si, the Republic of Korea. Until
now, this species was only recorded in Korea (Jeju-do) and Japan (Honshu, Kyushu). This finding is a
remarkable case of disjunct distribution. We provide an updated checklist of Korean Adonis with a new
locality record for A. multiflora and an identification key for all species of Adonis that occur in Northeast
Asia.
Ó2018 National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA), Publishing
Services by Elsevier. This is an open access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction
The genus Adonis L. (Adonis, Pheasant’s eye) comprises the
annual and perennial herbaceous plants of the buttercup family
(Ranunculaceae). It consists of about 30 taxa distributed in the
Northern Hemisphere including Asia, Europe, and North America,
whereas some annual species are found in Southwest Asia to North
Africa and along the shores of the Mediterranean (Mabberley 2008;
Meusel et al 1965). Owing to their ornamental properties, several
taxa are cultivated for gardening. In Northeast Asia (including
northeastern China, Republic of Korea, Japan, and Far East Russia),
seven taxa have been reported (Fu and Robinson 2001; Nishikawa
and Kadota 2006; Son et al 2016, 2018).
The geographical distribution of plants is greatly influenced by
the environment conditions, including current climate state which
is temperature, humidity, sunshine, winds, etc., and soil, but flora
did not always match with environment conditions (Son et al
2008) because distribution of the region of flora and the specific
species is determined by the historical progress of the topography
and climate and then diffusion, reduction, and evolution of the
species (Tateoka 1983).
During extensive field surveys for floristic research, an inter-
esting Adonis population was discovered in Gijang-gun, Busan-si,
the Republic of Korea. Based on detailed examination of morpho-
logical features and relevant publications (Fu and Robinson 2001;
Lee et al 2003; Nishikawa and Kadota 2006; Park 2007; Son
2015), this population seems to consist of Adonis multiflora Nishi-
kawa & Koji Ito individuals. Until now, this species has only been
reported from the islands of Jeju-do, in the Republic of Korea, and
Honshu and Kyushu, in Japan (Kaneko et al 2008; Lee et al 2003;
Park 2007; Son et al 2016). Thus, the present study formally re-
ports an updated checklist of Korean Adonis with a new locality
record for A. multiflora. Based on the detailed morphological fea-
tures examined to classify the A. multiflora individuals found in
Gijang-gun, an identification key for all species of Adonis that are
found in Northeast Asia is also provided.
Material and methods
Observations of morphological features were conducted based
on living plants and on dry specimens. Field photographs were
captured using a digital D810 camera equipped with an AF 105 mm
Macro lens with a GP-1A GPS Unit (all Nikon, Tokyo, Japan).
Morphological characters were measured using a digital vernier
*Corresponding author. Tel.: þ82 31 540 1074; fax: þ82 31 540 1070.
E-mail address: natu17@korea.kr (K.S. Chang).
Peer review under responsibility of National Science Museum of Korea (NSMK) and
Korea National Arboretum (KNA).
Contents lists available at ScienceDirect
Journal of Asia-Pacific Biodiversity
journal homepage: http://www.elsevier.com/locate/japb
https://doi.org/10.1016/j.japb.2018.07.001
pISSN2287-884X eISSN2287-9544/Ó2018 National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA), Publishing Services by Elsevier. This is an open
access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Journal of Asia-Pacific Biodiversity 11 (2018) 462e467
caliper, and data were acquired from field notes. Flowering and
fruiting periods are given as cited on collector’s labels. The voucher
specimen has been deposited in the Korea National Arboretum
(KH), and herbarium acronyms follow Thiers (2018).
Results and discussion
Checklist of the Korean Adonis
1) Adonis amurensis Regel & Radde, Bull. Soc. Imp. Naturalistes
Moscou 34(2): 35 (1861).
(Figure 1)
Type. RUSSIA: Amur, in montibus Burejae, Radde s.n. (isosyntype,
UPS!)
Adonis vernalis var. amurensis (Regel & Radde) Finet & Gagnep., Bull.
Soc. Bot. France 51: 132 (1904)
Adonanthe amurensis (Regel & Radde) Chrtek & Slavíková, 1978
Preslia 50(1): 24 (1978)
Chrysocyathus amurensis (Regel & Radde) Holub, Preslia 70(2): 102
(1998)
Adonis amurensis var. puberula Honda, Bot Mag. (Tokyo) 52: 49
(1939)
Type. JAPAN: Hokkaido, Kitami, H. Iwamoto 86 (holotype, TI!)
Figure 1. Adonis amurensis Regel & Radde.: A, whole plant; B, stem; C, flower, front view; D, flower, sepals close up at night; E, leaves; F, aggregate fruit; G, fruit receptacle and
achenes. Photographs by Dong Chan Son and Beom Kyun Park.
DC Son et al. / Journal of Asia-Pacific Biodiversity 11 (2018) 462e467 463
Diagnosis. Herbs perennial. Rhizome short. Roots numerous,
fibrous. Stems erect, unbranched, glabrous but scarcely pubescent
at upper part, 2.4- to 27.3-cm tall. Scales membranous, alternate at
lower parts of the stem. Leaves not fully expanded at anthesis,
alternate, 1e3 pinnately compound, petiolate; leaf blade
triangular-ovate, 2.6- to 9.0-cm long, 2.4- to 7.0-cm wide, green,
glabrous, chartaceous, parted or cleft at margin; leaflets deeply
incised; final lobules narrowly ovate, acute at apex; petiole un-
branched, dichotomously branched or ternately branched, 0.1- to
2.2-cm long. Inflorescence solitary. Flower one-flowered, 2.1e
6.0 cm in diameter, yellow. Sepals 8(e9), oblanceolate to oblong,
0.9- to 2.0-cm long, 0.2- to 0.9-cm wide, purple or dark purple
abaxially, glabrate or pubescent. Petals 11e20, yellow, oblong to
obovate, nearly equal or shorter than sepals, 0.6- to 1.8-cm long,
0.2- to 0.8-cm wide, obtuse, round, or incised at apex, glabrous.
Stamens numerous, basifixed; anther two-loculed, oblong, 0.8- to
1.5-mm long; filaments filiform. Pistil numerous, 1.8- to 2.9-mm
long; ovary ovate, puberulous; styles 0.8- to 1.5-mm long,
recurved; stigma globose. Aggregated fruit subglobular to ellip-
soidal, 9.4- to 15.3-mm long, 8.2e14.5 mm in diameter. Achenes
26e111 in number per fruit, obovoid, 2.7- to 4.9-mm long, 1.5- to
3.5- mm wide, pubescent; style 1.0- to 1.3-mm long, recurved at
base. Seed ovate, 1.5- to 2.9-mm long, 1.3- to 1.9-mm wide.
Chromosome number 2n¼16.
Vernacular (Korean) name. Bok-su-cho (복수초)
Phenology. Flowering: Mar. to Apr.; fruiting: May
Figure 2. Adonis pseudoamurensis W.T. Wang.: A, whole plant; B, plant at early flowering time, coetaneous leaf; C, stem, cross-sectional view; D, leaves; E, flower, front view; F,
flower, dorsal view; G, aggregate fruit. Photographs by Yoon-Young Kim, Beom Kyun Park and Dong Chan Son.
DC Son et al. / Journal of Asia-Pacific Biodiversity 11 (2018) 462e467464
Distribution. Korea (Gangwon-do, Gyeonggi-do, Chungcheong-
buk-do, Jeollabuk-do, Gyeongsangbuk-do, and Gyeongsangnam-
do), Japan (Hokkaido), China (E Heilongjiang, Jilin, and Liaoning),
and Russia (Amur).
2) Adonis pseudoamurensis W.T. Wang, Fl. Reipubl. Popularis Sin.
28: 352 (1980).
(Figure 2)
Type. CHINA: Jilin, Huinan, C. Chen 1204 (holotype, PE!)
Chrysocyathus pseudoamurensis (W.T. Wang) Holub, Preslia. 70(2):
102 (1998).
Adonis ramosa subsp. fupingensis W.T. Wang, Acta Phytotax. Sin.
32(5): 472 (1994).
Type. CHINA: Hebei, Fuping, Chanet A390 (holotype, TIE!)
Adonis amurensis var. dissectipetalis Y.N. Lee, Bull. Korea Pl. Res. 5: 4
(2005).
Type. KOREA: Gauido, J.S. Han s.n. (holotype, KPRP!)
Diagnosis. Herbs perennial. Rhizomes short. Roots numerous,
fibrous. Stem erect, branched, glabrous but scarcely pubescent at
upper part, 12- to 35-cm tall. Scales membranous, alternate at
lower parts of stem, persistent with having leaf on their tip. Leaves
alternate, 1e2 pinnately compound, petiolate; leaf blade rhombic,
1.8- to 8.9-cm long, 1.2- to 7.1-cm wide, green, glabrous, charta-
ceous, parted or cleft at margin; leaflets deeply incised; final lob-
ules lanceolate, acute at apex; petiole unbranched or
Figure 3. Adonis mul tiflora Nishikawa & Koji Ito from Gijang-gun, Busan-si, Republic of Korea: A, whole plant; B, plant at early flowering time, precocious leaf; C, stem, cross-
sectional view; D, leaves; E, flower, front view; F, flower, dorsal view; G, aggregate fruit. Photographs by Yoon-Young Kim and Dong Chan Son.
DC Son et al. / Journal of Asia-Pacific Biodiversity 11 (2018) 462e467 465
dichotomously branched. Stipules present at lower part of cauline
leaves, leaf-like, deeply incised. Inflorescence solitary. Flowers 1e4
flowered, 1.6e5.1 cm in diameter, yellow. Sepals 5(e6), rhombic-
oval to obovate, wider than petals, 0.6- to 2.1-cm long, 0.4- to 1.1-
cm wide, grayish purple to dark green abaxially, moderately to
densely hairy, densely so at base. Petals 11e13, rhombic-oval to
obovate, longer than sepals, 0.8- to 2.9-cm long, 0.3-to 0.9-cm
wide; upper part of abaxial surface of margin yellow or reddish
brown, fading and becoming colorless when dried. Stamens
numerous, 2e3 whorled, basifixed; anthers two-loculed, elliptic,
oblong or oval, yellow or orange; filaments filiform, yellow. Pistils
numerous; styles recurved, persistent; ovaries pubescent. Aggre-
gate fruit ellipsoidal. Achenes 35e91 in number per fruit, ellip-
soidal, 2.5- to 4.7-mm long, 1.5- to 3.1-mm wide, densely
pubescent; style 1.3- to 1.8-mm long, recurved at base. Seed ovate.
Chromosome number 2n¼16.
Vernacular (Korean) name. Gae-bok-su-cho (개복수초)
Phenology. Flowering: Mar. to Apr.; fruiting: Apr. to May
Distribution. Korea (Gangwon-do, Gyeonggi-do, Chungcheong-
buk-do, Chungcheongnam-do, Jeollabuk-do, Jeollanam-do, Gyeong-
sangbuk-do, and Gyeongsangnam-do) and China (Jilin, Liaoning, and
Hebei)
3) Adonis multiflora Nishikawa & Koji Ito, J. Jap. Bot. 64(2): 51
(1989).
(Figure 3)
Type. JAPAN: Shimodaira, Towada C., Aomori Pref. 24 Apr. 1982,
T. Nishikawa s.n. (holotype, SAPS!)
Chrysocyathus multiflorus (Nishikawa & Koji Ito) Holub, Preslia
70(2): 102 (1998)
Diagnosis. Herbs perennial. Rhizomes short. Roots numerous,
stout, fibrous. Stem erect, branched, glabrous but scarcely pubes-
cent at upper part, hollow, 10.8- to 27.4-cm tall. Scales membra-
nous, alternate at lower parts of stem and branches, persistent with
leaves on tips. Leaves alternate,1e2 pinnately compound, petiolate;
leaf blade triangular-ovate to rhombic, 2.4- to 6.8-cm long, 1.7- to
5.5-cm wide, light green to green, glabrous, chartaceous, parted or
cleft at margin; leaflets deeply incised; final lobules linear, acumi-
nate at apex; petiole unbranched, 0.1- to 5.3-cm long, glabrous.
Stipules present at lower part of cauline leaves, leaf-like, deeply
incised. Inflorescence solitary. Flowers 1e6flowered, 2.8e5.2 cm in
diameter, yellow, orange or rarely white. Sepals 5(e7), oblanceolate
to oblong, 0.8- to 2.0-cm long, 0.4- to 1.0-cm wide, narrower than
petals, dark green abaxially, moderately to densely hairy, densely
hairy at base. Petals 10e15, oblong to obovate, 1.2- to 2.7-cm long,
0.5- to 1-cm wide, longer than sepals, acute at apex. Stamens
numerous, 2e3 whorled, basifixed; anthers two-loculed, oblong,
1.2- to 2.3-mm long, yellow; filaments filiform. Pistils numerous;
styles recurved, persistent; ovaries pubescent. Aggregate fruit
subglobose, 8.1- to 13.4-mm long, 8.1e12.9 mm in diameter.
Achenes 23e68 in number per fruit, obliquely obovoid, 2.7- to 4.6-
mm long, 1.5- to 3.2-mm wide, pubescent; style 1.0- to 1.3-mm
long, recurved at base. Seed ovate. Chromosome number 2n¼16.
Vernacular (Korean) name. Se-bok-su-cho (세복수초).
Phenology. Flowering: Feb. to Mar.; fruiting: late Mar. to May
Distribution. Korea (Jeju-do and Busan-si) and Japan (Honshu
and Kyushu)
Specimens examined. Korea. Gijang-gun, Busan-si, 20 iii 2018,
D.C. Son & Y.Y. Kim s.n. (KH)
Note. A. multiflora was first described based on the specimens
collected from Shimodaira region, Aomori, farthest north of Hon-
shu, Japan (Nishikawa 1989). Later, Wang (1994) considered
A. multiflora a synonym of A. ramosa Franchet as Japanese endemic
species (Nishikawa and Kadota 2006), whereas Nishikawa and
Kadota (2006) contemplated that A. pseudoamurensis reported by
Wang (1980) is A. multiflora and reported that the species is also
distributed in China (Nishikawa 2016). However, A. multiflora dif-
fers from other species of Adonis by its acuminate leaf apices, linear
final lobes on leaves, scales on stem and branches, and parallel-
perpendicular type of achene epidermal microstructures, among
other features (Lee et al 2003; Son and Ko 2012, 2013; Son et al
2016, 2017). This species has great medicinal value due to the
anticancer properties of its extract (Han 2015). Until now, it was
known from the Republic of Korea (Jeju-do island) and Japan
(Honshu and Kyushu islands) (Kaneko et al 2008; Lee et al 2003;
Park 2007; Son et al 2016). This is, therefore, its first record from
Gijang-gun, Busan-si, Republic of Korea. Geographically, this is a
remarkable case of a relict population due to extinction of other
Korean populations. In addition, it is sole inland population as the
northern limit line of the Korean Peninsula, thereby providing
support for the colonization and evolutionary routes of A. multiflora
from the Republic of Korea to Japan or otherwise, according to
historical geographic changes (Son 2015; Son et al 2016, 2017). A
similar pattern of distribution is known in Euphorbia fauriei H.Lév. &
Vaniot and Daphne kiusiana Miq. (Oh et al 2016). Although the
population of A. multiflora located in Gijang-gun comprises hun-
dreds of mature individuals, it seems to be worthy of special
mention for conservation as this area was recently denuded by
broad-scale logging for planting Chamaecyparis obtusa (Siebold &
Zucc.) Endl.
Key to the Adonis species distributed in Northeast Asia
1. Leaf petiolate......................2
- Leaf sessile....................A. apennina
2. Plant precocious; stem unbranched; flower 1; sepals 8....3
- Plant coetaneous; stem branched; flower 2 or more; sepals 5.4
3. Stem glabrous; leaves glabrous.........A. amurensis
- Stem pubescent; leaves pubescent on abaxial surface
................A. amurensis var. pilosissima
4. Leaf pubescent on abaxial surface, petiole pubescent; sepals
equal to petals..................A. ramosa
- Leaf glabrous on both surfaces, petiole glabrous; sepals shorter
than petals........................5
5. Receptacle pubescent; sepals pubescent..........6
- Receptacle glabrous; sepals glabrous.......A. shikokuensis
6. Leaf lobules lanceolate; sepals wider than petals; aggregate fruit
ellipsoidal.................A. pseudoamurensis
- Leaf lobules linear; sepals narrower than petals; aggregate fruit
subglobose...................A. multiflora
Conflicts of interest
The authors declare that there is no conflicts of interest.
Acknowledgments
The authors would like to thank anonymous reviewers for their
valuable comments and suggestions. This study was supported by
the Korea National Arboretum [project ‘KNA1-1-23, 18-1’].
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