Research Article |
Corresponding author: Yanqin Xu ( yqxutcm@163.com ) Academic editor: Marco Pellegrini
© 2019 Yanqin Xu, Linjian Liu, Shaoxiong Liu, Yiming He, Renqing Li, Fei Ge.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Xu Y, Liu L, Liu S, He Y, Li R, Ge F (2019) The taxonomic relevance of flower colour for Epimedium (Berberidaceae), with morphological and nomenclatural notes for five species from China. PhytoKeys 118: 33-64. https://doi.org/10.3897/phytokeys.118.30268
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Morphological variations, particularly flower colour, could be considered as an evolutionarily and ornamentally significant taxonomic criterion for Epimedium. Our extensive field investigation based on population studies revealed abundant intraspecific variations in flower colour. Five species, (i.e., E. acuminatum Franch., E. leptorrhizum Stearn, E. pauciflorum K.C.Yen, E. mikinorii Stearn, and E. glandulosopilosum H.R.Liang) were found to possess polymorphic flower colour, which is first described and illustrated here. Moreover, all these species were found to be polymorphic in other diagnostic characters, such as the type of rhizome, the number and arrangement of stem-leaves, and/or their indumentum, which have not been adequately described in previous studies. Therefore, their morphological descriptions have been complemented and/or revised. We also provide notes on the morphology and nomenclature for each species. Additionally, a key to the species in China has been provided. The present study could serve as a basis for understanding their taxonomy and helping their utilisation as an ornamental plant.
intraspecific, morphology, perianth, polymorphism, population, Ranunculales
Epimedium L. is the largest herbaceous genus of Berberidaceae, comprising ca. 60 species distributed in the temperate mountain regions from eastern Asia to northwestern Africa, with enormous distributional gaps within these regions (
The divergence of floral traits is a striking phenomenon in flowering plants, which plays an important role in ecology, plant systematics and conservation (
As part of our ongoing efforts to study the Epimedium diversity in China, we studied the relevance of flower colour variation for the taxonomy of Epimedium based on extensive field studies for five species of Chinese Epimedium, with additional cultivation and herbaria studies. Moreover, we present a comprehensive revision on their taxonomic description, including the variation on rhizome morphology, the number and arrangement of stem-leaves, and indumentum type. Additionally, we provide an identification key for the species of Epimedium recognised in China. The results provide abundant and important information for the taxonomy of Epimedium, and subsidies in its exploration and utilisation, for example, as ornamental plants.
In Epimedium, some diagnostic features, especially those of flowers and inflorescences, are obscured or not visible in the herbarium material. Moreover, the flowers are of frail texture and deciduous. Therefore, it is difficult to infer the exact colouration of in vivo flowers by examining dried specimens. Therefore, the vegetative as well as reproductive characters were examined mainly in their natural habitats, while the herbarium specimens were used as aids. Herbarium specimens were examined from the following herbaria: CDBI, E, GXMI, HGAS, HIB, IBK, IBSC, IMD,
All field investigations and observations were conducted in full bloom from 2012 to 2017. To investigate the morphological variation, we carried out field surveys throughout the Chinese distribution range of Epimedium, especially in Sichuan, Guizhou, Guangxi, Hubei, Hunan, Anhui and Jiangxi provinces and Chongqing municipality. In each province or municipality, a survey, as wide and thorough as possible, was conducted. The species that exhibited variations in flower colour and other characters were then observed and sampled (Table
Species | Population code | Location (China) | Elevation (m) | Latitude (N) | Longitude (E) |
E. acuminatum | CQNC* | Tianxing, Nanchuan, Chongqing | 899 | 29°03'N, 107°07'E | |
SCEM* | Emei Mountain, Leshan, Sichuan | 1049 | 29°34'N, 103°25'E | ||
SCMP* | Muping, Baoxing, Sichuan | 1248 | 30°20'N, 102°48'E | ||
SCSL* | Shangli, Yaan, Sichuan | 862 | 30°11'N, 103°04'E | ||
SCSS* | Shuangshi, Lushan, Sichuan | 928 | 30°15'N, 102°55'E | ||
SCYJ* | Siping, Yingjing, Sichuan | 1448 | 29°43'N, 102°37'E | ||
GZNL | Nanlong, Kaiyang, Guizhou | 986 | 27°05'N, 107°05'E | ||
GZYH | Hekan, Yanhe, Guizhou | 637 | 29°02'N, 108°09'E | ||
GZZA | Fengyi, Zheng’an, Guizhou | 792 | 28°43'N, 107°51'E | ||
CQFL | Mawu, Fuling, Chongqing | 935 | 29°31'N, 107°19'E | ||
CQYC | Chashanzhuhai, Yongchuan, Chongqing | 762 | 29°28'N, 105°58'E | ||
SCHJ | Fubao, Hejiang, Sichuan | 723 | 29°28'N, 105°59'E | ||
SCMB | Dazhubao, Mabian, Sichuan | 1147 | 29°00'N, 103°30'E | ||
SCXH | Xiaohe, Lushan, Sichuan | 1192 | 30°29'N, 103°07'E | ||
SCCM | Caomigang, Lushan, Sichuan | 1534 | 30°26'N, 103°05'E | ||
SCQL | Youzha, Qionglai, Sichuan | 1067 | 30°26'N, 103°14'E | ||
SCMT | Naobao, Qionglai, Sichuan | 1468 | 30°25'N, 103°07'E | ||
SCLG | Lingguan, Baoxing, Sichuan | 1068 | 30°18'N, 102°48'E | ||
SCWN | Wanniansi, Emei Mountain, Sichuan | 1110 | 28°43'N, 107°51'E | ||
E. leptorrhizum | GZGY* | Shuikousi, Guiyang, Guizhou | 1145 | 26°34'N, 106°44'E | |
GZST* | Ganlong, Songtao, Guizhou | 907 | 28°19'N, 108°41'E | ||
HNBJ* | Zhuping, Baojing, Hunan | 978 | 28°36'N, 109°12'E | ||
HBGP | Gongjiaping, Enshi, Hubei | 1523 | 30°10'N, 109°44'E | ||
HBMF | Mufu, Enshi, Hubei | 1080 | 30°17'N, 108°56'E | ||
HBLC | Fubaoshan, Lichuan, Hubei | 1386 | 30°12'N, 108°43'E | ||
HBTB | Tuanbao, Lichuan, Hubei | 1200 | 30°22'N, 109°07'E | ||
GZLC | Longchang, Kaili, Guizhou | 796 | 26°39'N, 107°56'E | ||
GZLS | Lingshan, Guiyang, Guizhou | 1207 | 26°36'N, 106°42'E | ||
GZMH | Muhuang, Yinjiang, Guizhou | 1300 | 28°02'N, 108°42'E | ||
ZJLQ | Cukeng, Longquan, Zhejiang | 1210 | 27°55'N, 119°10'E | ||
GDNL | Ruyuan, Shaoguan, Guangdong | 670 | 24°55'N, 113°03'E | ||
E. pauciflorum | SCWC* | Yanmen, Wenchuan, Sichuan | 1817 | 31°27'N, 103°34'E | |
SCMS* | Miansi, Wenchuan, Sichuan | 1780 | 31°35'N, 103°49'E | ||
SCJZ* | Jingzhou, Maoxian, Sichuan | 1800 | 31°42'N, 103°53'E | ||
E. mikinorii | HBES* | Baiguo, Enshi, Hubei | 754 | 30°14'N, 109°22'E | |
HBXT* | Xintang, Enshi, Hubei | 1370 | 30°13'N, 109°41'E | ||
E. glandulosopilosum | CQWX* | Tongcheng, Wuxi, Chongqing | 1161 | 31°23'N, 109°46'E |
The Flora of China (
Epimediumacuminatum Franch., E. leptorrhizum Stearn, E. pauciflorum K.C.Yen, E. mikinorii Stearn and E. glandulosopilosum H.R.Liang, were found with intraspecific flower colour variation. Moreover, all these species were also morphologically variable in the number and arrangement of stem-leaves, the type of rhizomes and/or indumentum. Location, code, latitude, longitude, and elevation of the referred populations are presented in Table
Epimedium komarovii H.Léveillé, Fedde Repert. Spec. Nov. Regni Veg. 7: 259. 1909. Type: CHINA. Guizhou: Pin-Fa, 1908, Cavalerie 954 (holotype: E00270388!).
Epimedium simplicifolium T.S.Ying, Acta Phytotaxon. Sin. 13: 51. 1975. Type: CHINA. Guizhou: Wuchuan, 9 May 1928, P. C. Tsoong 606 (holotype: PE01432137!; isotype: PE01432138!).
Epimedium chlorandrum Stearn, Kew Bull. 52: 660. 1997. Type: CHINA. Sichuan: Baoxing, cultivated in England, Hampshire, Kilmeston, Blackthorn Nursery, April 1996, Ogisu 94003 (holotype: K000340098!).
CHINA. Guizhou: 1858, Perny s.n. (holotype: P, barcode P02327614!; isolectotype: P, barcode P02327612!).
Herbs 20–80(–110) cm tall. Rhizome compact, sometimes long creeping, 2–8 mm in diam. Leaves basal and cauline, usually trifoliolate or occasionally unifoliolate; leaflets of trifoliolate leaves narrowly ovate or lanceolate, 3–19.8 × 1.5–8.9 cm, apex long acuminate, base cordate, lobes rounded or acute, those of the lateral leaflets very unequal; unifoliolate leaves ovate or broadly ovate, 8.7–20 × 6.8–11.5 cm, apex acuminate, base cordate, lobes equal, rounded or rarely acute; leaves leathery when mature, margin spinous-serrate, spines 1–2 mm long, adaxially deep green, glossy, abaxially glaucous, papillose, with dense or sparse shortly appressed stout bristle-like hairs and sometimes densely sericeous. Flowering stem with 2 trifoliolate opposite leaves, sometimes 3-whorled trifoliolate leaves or 2 opposite unifoliolate, rarely with 2 opposite leaves with one trifoliolate and the other unifoliolate, 3 whorled leaves with one trifoliolate and two unifoliolate or 3 whorled unifoliolate leaves. Panicle 6–70(–108)-flowered, 6–33 cm long, with lower peduncles loosely 2–5-flowered, glabrous or occasionally glandular-hairy. Pedicel 1–5 cm long. Flowers large, 3–5 cm in diam. Outer sepals 4, blunt, outer pair ovate-oblong, ca. 3 × 2 mm, inner pair broadly obovate, ca. 4.5 × 4 mm; inner sepals ovate-elliptic, 6–21 × 3–9 mm, apically acute, white, yellowish, pale rose or rose, petals pale yellow, yellow, pale violet, reddish-purple, purple-yellow, pale purple or purple. Petals curving outward, horn-shaped, much longer than inner sepals, 15–25 mm, tamping from the swollen but lamina-less base. Stamens 3–4 mm long; anthers yellow or green, ca. 2.5 mm long. Follicles oblong, ca. 20 mm long, style rostriform. Seeds numerous.
Epimedium acuminatum is one of the most widespread species in the genus, distributed in Sichuan, Guizhou, Chongqing, and northern Yunnan. Its large distribution area is predominantly characterised by mountain land. Epimedium acuminatum is often found on mountain slopes, forest edges or weedy slopes with elevations ranging from 270 m to 2400 m (Fig.
Epimedium acuminatum flowers from April to June, and fruits from May to July.
Before this study, flower colour variation in E. acuminatum had already been recognised. Overall, yellow (B. Y. Peng 47073, F. T. Wang 23329, D. Y. Peng 47070, W. P. Fang 802, Anon. 86, Z. X. Qu 1305, Q. H. Chen et al. 9411) or pale yellow (Sanxia Exped. 0821, X. B. Zhang 19), purple (G. H. Yang 54343, Sichuan Econ. Pl. Exped. 0030, K. J. Guan et al. 0273, Xiong & Z. L. Zhou 91045, Z. Y. Liu 15500, T. H. Tu 3116, S. Z. He 96410, S. W. Teng 0008, P. Zhao 807, Y. Tsiang 4994) or pale purple (P. Zhao 762, Jinfoshan Exped. 0330, Jinfoshan Exped. 0202, G. F. Li 60324), purple-whitish (T. T. Yu 312, Z. Z. Guo 403, J. M. Yuan 003 and J. M. Yuan 005, S. W. Tfng 90093, Z. S. Zhang et al. 401131), and white (K. J. Guan et al. 477, C. H. Li 97-301, K. Y. Lang 3002, K. J. Guan et al. 165) or whitish (Z. X. Qu 1057, Sanxia Exped. 0729 and Sanxia Exped. 0909) were the most frequently recorded flower colours. However, specific colours, for example, reddish (S. P. Pong 6108), yellowish purple (X. Y. He 4050; T. C. Pan & G. F. Wu 105), and pale purple-green (Z. Y. Wu 60) have also been examined from specimens. Colour differences among individuals of the same location have been slightly recorded, but both yellow and purple flowers were recorded in Sichuan Econ. Pl. Exped. 0013. Moreover, continuous variations from yellow to white and from yellow to pale reddish-purple were remarked by T. H. Tu 2763 and B. L. Guo 0608, respectively.
Two synonyms are included in E. acuminatum, namely E. simplicifolium and E. chlorandrum. There were only two specimens of E. simplicifolium for reference. The holotype (P. C. Tsoong 606) recorded yellow flowers with purplish red petals. Since these descriptions were based on flowers that are not fully open – the outer sepals soon falling – the outermost is formed of inner sepals. Therefore, the “yellow flower” actually is “yellow or yellowish inner sepals”. Another specimen (S. Z. He 96410) recorded a purplish red flower, and the inner sepals spotted with purplish red. Epimedium chlorandrum has six specimens. Greenish inner sepals and pale yellow petals have been described in the holotype (Ogisu 94003). Pale yellow inner sepals and petals were recorded in B. L. Guo 0540 and B. L. Guo 0607 while B. L. Guo 0606 described the colour variation of inner sepals as anything from pale yellow to pale purplish red. And B. L. Guo 0608 also described both inner sepals and petals from pale yellow to pale purplish red.
Based on a field survey at the population level, we observed more extensive and continuous colour variation from pale yellow to dark purple (Fig.
The flower colour variations of different populations of E. acuminatum. A SCMP, mainly yellow B SCSL, mainly yellow, occasionally purple-yellow at the base of petals C CQNC, mainly yellow, occasionally rose-purple D SCSS, from yellow to purple E SCEM, mainly purple, occasionally purple-yellow F SCYJ, mainly purple, occasionally purple-yellow G Individual with yellow flowers H Individual with purple-yellow flowers I Individual with purple flowers.
For E. acuminatum, the populations that showed uniform colour (yellow or purple) were excluded from the illustration in this study. We mainly focused on the populations that presented colour variation (Fig.
Combing the geographical distribution of specimens (both field and herbarium specimens) and their flower colour variation of E. acuminatum, we found an interesting result (Fig.
Geographical variation in flower colour patterns within E. acuminatum. The circles and boxes represent wild populations and herbarium specimens, respectively. The colour of the circles and boxes represent flower colour. The 19 population codes are shown in Table
In addition, the number and arrangement of the stem-leaves were significantly diverse in E. acuminatum. It commonly showed 2 trifoliolate opposite leaves, sometimes 3-whorled trifoliolate leaves (G. F Li 60514, Y. Tsiang 4994) or 2 opposite unifoliolate (S. Z. He 96410, P. C. Tsoong 606), rarely with 2 opposite leaves with one trifoliolate and the other unifoliolate (J. H. Xiong 30469), 3 whorled leaves with one trifoliolate and two unifoliolate (J. H. Xiong 30469) or 3 whorled unifoliolate leaves.
CHINA. Sichuan: Chengxiang, Tianquan, 1100–1200 m, 24 March 1983, B. Y. Peng 47070 and B. Y. Peng 47073 (CDBI, yellow flower); Jiulaodong, Mt. Emei, 1800 m, 02 May 1957, G. H. Yang 54343 (PE, KUN, HIB, NAS, purple flower); Lianhuashi, Mt. Emei, 1950 m, 11 May 1964, K. J. Guan et al. 477 (PE, white flower); Mt. Emei, 1100 m, 11 June 1933, S. P. Pong 6108 (PE, reddish flower); Mt. Emei, 1050 m, 13 March 1997, C. H. Li 97–301 (PE, white flower); Mt. Emei, 900 m, 16 April 1932, T. T. Yu 312 (N, purplish white flower); Mt. Emei, 2000 m, 15 July 1931, F. T. Wang 23329 (PE, yellow flower); Mt. Emei, 900 m, 16 April, T. T. Yu 312 (PE, purplish white flower); Mt. Emei, 1700 m, 27 May 1959, Z. Z. Guo 403 (PE, purplish white flower); Mt. Emei, 1952, J. H. Xiong 30469 (PE, 3 whorled leaves with one trifoliolate and two unifoliolate; IBSC, 2 opposite leaves with one trifoliolate and the other unifoliolate); Mt. Emei, 1049 m, 4 April 2015, Y. Q Xu & S. X. Liu 2015029 (
Epimedium brachyrrhizum Stearn, Kew Bull. 52: 659. 1997. Type: CHINA. Guizhou: Mt. Fanjingshan, cultivated in the USA, Massachusetts, Hubbbardston, Darrell Probst CPC940495 (holotype: K000340100!).
CHINA. Guizhou: Guiyang, Bodinier 2184 (holotype: P, barcode P00568282!; isotypes: P, barcodes P00572792!, P00572793!, P00572800!, P00572801!, P00572802!).
Herbs 12–50 cm tall. Rhizome long creeping, or compact, 1–5(–8) mm in diam.; internodes sometimes to 20 cm. Leaves basal and cauline, trifoliolate or occasionally unifoliolate. Leaflets of trifoliolate leaves narrowly ovate or ovate, 3–16 × 2–8.6 cm, apex long acuminate, base deeply cordate with usually rounded lobes nearly touching, those of the lateral leaflets very unequal; unifoliolate leaves ovate or broadly ovate, 8–13.7 × 5–11 cm, apex acuminate, base cordate with lobes equal, rounded and rarely acute; leaves leathery, margin spinous-serrate, adaxially deep green, glossy, abaxially glaucous, papillose, and pubescent along veins, especially dense at the insertion of petioles and petiolules. Flowering stem with 1 trifoliolate leaf or 2 opposite leaves. Inflorescence simple, racemose, 3–14-flowered, 12–25 cm long, glandular. Pedicel 1–2.5 cm long, glandular. Flowers large, ca. 4 cm in diam. Outer sepals green or purplish, outer pair ovate-oblong, 3–5 × 2 mm, apex obtuse, inner pair broadly ovate, 4–5.5 × 3–4.5 mm, apex acuminate; inner sepals white, white tinged with rose, or rose, narrowly elliptic, 11–20 × 4–7 mm, apex acute. Petals subequal to or longer than the inner sepals, white or pale yellow with base yellow or orange, white with base rose or deep rose, rose, deep rose or pale purple, horn-shaped, 15–26 mm, tapering from a swollen but lamina-less base. Stamens ca. 4 mm long; anthers, yellow or green, ca. 3 mm long. Follicles oblong, 8–18 mm long; style rostriform. Seeds numerous.
Epimedium leptorrhizum is distributed in the montane forests or thickets in Guizhou, Hubei, Hunan and Chongqing, in elevations ranging from 350 m to 2100 m (Fig.
Epimedium leptorrhizum flowers from April to May, and fruits from May to June.
Abundant and continuous flower colour variation has been observed and illustrated for this species. The inner sepals presented continuous variation from white, white tinged with rose, through to completely rose. Petals varied from white or pale yellow with base yellow or orange, white with base rose or deep rose to completely rose, deep rose or pale purple (Fig.
In addition, we showed that the rhizome of E. leptorrhizum is usually long-creeping, occasionally compact. The flowering stem is usually with 1 trifoliolate leaf or 2 opposite leaves.
CHINA. Guizhou: Mt. Qianling, Guiyang, 10 March 1957, Anon. 0123-635 (IMD); Mt. Qianling, Guiyang, 28 August 1977, Anon. 5507 (IMD); Qianling Park, Guiyang, 1400 m, 19 March 1959, Qiannan Exped. 0077 (PE); Guiyang, 5 June 1994, B. L. Guo 94018 (IMD); Shuikousi, Guiyang, 1145 m, 2 April 2012, Y. Q. Xu & Y. Xu 2012001 (
Geographical variation in flower colour patterns within E. leptorrhizum (boxes), E. pauciflorum (circles), E. mikinorii (diamonds) and E. glandulosopilosum (triangle). The colour of the boxes, circles, diamonds and triangle represent flower colour. The population codes are shown in Table
Epimedium platypetalum var. tenuis B.L.Guo & P.G.Hsiao, Acta Phytotaxon. Sin. 31: 195. 1993. Type: CHINA. Sichuan: Shuixicun, Mao Xian, 1990 m, H. R. Xie 89023, (holotype: IMD! without accession number or barcode).
CHINA. Sichuan: Dagou, Maowen, 1700 m, K. C. Yen & S. L. Shao 66535 (holotype: GXMI, barcode GXMI004519!; isotype: PE, barcode PE01432167!).
Herbs 6–30 cm tall. Rhizome long creeping, 1–3 mm in diam.; sometimes creeping to 20–25 cm. Leaves basal and cauline, trifoliolate; leaflets ovate or suborbicular, 1.3–4.5 × 1.2–3.5 cm, abaxially sparsely or occasionally densely puberulent, adaxially glabrous when mature, base deeply cordate with rounded lobes nearly touching, those of lateral leaflets conspicuously unequal, margin coarsely serrate, apex acute or shortly acuminate. Flowering stem with 1 trifoliolate, occasionally 1 unifoliolate leaf or 2 alternate trifoliolate leaves. Inflorescence simple, racemose, few-flowered (ca. 2–6 flowers), 3–13.5 cm long; inflorescence axis and pedicels glandular or pubescent. Pedicel 1–2.3 cm long; bracts ovate, 0.8–1.4 mm. Flowers ca. 2–2.5 cm in diam. Outer sepals fall sooner, greenish, caduceus, narrowly obovate, ca. 4 × 3 mm; inner sepals white, faintly rose-tinged or pale rose, broadly lanceolate, ca. 12 × 5 mm, apex obtuse. Petals declined, white, white tinged with pale rose, rose, pale yellow, pale rose with the base purple yellow, horn-shaped, longer than inner sepals, blunt spurs ca. 15 mm long, expanded at base into a lamina 6 mm high. Stamens ca. 4 mm long; anthers yellow, ca. 2.5 mm long. Follicles oblong, 10–15 cm long; style rostriform. Seeds 4–6.
Epimedium pauciflorum is only known from the mountains of Maowen (the holotype locality, once and now divided into Maoxian, Wenchuan and Lixian) in Sichuan province, usually occurring in forest edges and weedy slopes, at high elevations approximately 1700–2600 m (Fig.
Epimedium pauciflorum flowers from April to May, and fruits also from April to May.
Epimedium pauciflorum is a low-growing species with a few-flowered inflorescence. Some information about the colour variation was recorded in part of the specimens. The colours of three specimens (Z. L. Kun 89022, B. L. Guo & W. K. Bao 97040, B. L. Guo 88182) were described as white, while the other two (B. L. Guo & W. K. Bao 97031 and 97032) were described as yellow. We observed a variety of colour variations; the inner sepals were white, faintly purple-tinged or pale rose, whereas the petals were white, white tinged with pale rose, rose, pale yellow, pale rose with the base purple yellow (Fig.
All the examined specimens were with 1 trifoliolate leaf on the flowering stem uniformly. But 1 unifoliolate leaf (only in SCWC population) or 2 alternate trifoliolate leaves (only in SCJZ population) (Fig.
CHINA. Sichuan: Jingzhou, Maoxian, 1700 m, 16 April 1987, K. C. Yen & S. L. Shao 66535 (PE, GXMI); Jingzhou, Maoxian, 1770 m, 19 April 1997, B. L. Guo & W. K. Bao 97031 and B. L. Guo & W. K. Bao 97032 (IMD); Jingzhou, Maoxian, 1770 m, 19 April 1997, B. L. Guo & W. K. Bao 97040 (IMD); Jingzhou, Maoxian, 1800 m, 2 May 1989, Z. L. Kun 89022 (IMD); Shuishi, Maoxian, 2000 m, 19 May 1989, H. R. Xie 89023 (IMD); Jingzhou, Maoxian, 1800 m, 3 September 1988, B. L. Guo 88182 (IMD); Daheba, Maoxian, 1800 m, 6 September 1988, B. L. Guo 88195 (IMD); Mt. Bianshi (Bianshishan), Maowen, 2600 m, 22 August 1985, F. Li 822-1 (IMD); Mt. Bianshi (Bianshishan), Maowen, 2600 m, 23 August 1985, F. Li 823-1 (IMD); Weizhou, Wenchuan, 2 May 1959, Maowen Exped. 2046 (PE, CDBI); Miansi, Wenchuan, 1780 m, 12 April 2017, Y. M. He et al. 2017007 (
CHINA. Hubei: Enshi, 670 m, April 1995, Ogisu 95039, cultivated at Blackthorn Nursery, Kilmeston, Hampshire; collected by W.T.Stearn, 5 April 1997 (holotype: K, not seem).
Herbs 26–94 cm tall. Rhizome compact. Leaves basal and cauline, trifoliolate; leaflets adaxially dark green, lanceolate, 8–17.4 × 3–8.6 cm, leathery, abaxially glaucous, glabrous or with appressed hairs, base cordate with equal lobes rounded, those of lateral leaflets oblique with outer lobe large and acute, inner lobe smaller and rounded, margin closely spinose-serrulate, apex long acuminate. Flowering stem with 2 opposite or occasionally 3-whorled trifoliolate leaves. Inflorescence compound, loose, 8–50(–85)-flowered, ca. 7–30 cm long, glabrous, with lower peduncles 3–5-flowered. Pedicel 1.0–1.5 cm long, glabrous. Flowers ca. 2.5–3.5 cm in diam. Outer sepals oblong, 4–6 × 2–4 mm; inner sepals yellowish, white, rose-tinged or rose, elliptic, 11–16 × 7–12 mm. Petals longer and much narrower than inner sepals, yellow, orange, purple or purple with yellow-edged lamina ca. 3.5 mm high; spur slightly curved or almost straight, subulate, elongated, 15–20 mm long. Stamens ca. 4 mm long; anthers yellow or green, ca. 3 mm long. Follicles oblong, 8–15 mm long; style rostriform. Seeds numerous.
Epimedium mikinorii is restricted to the mountains of Hubei (Enshi), Western of China, usually occurring at elevations ranging from 500 m to 1700 m (Fig.
Epimedium mikinorii flowers from April to June, and fruits from May to June.
The field investigation found extensive colour variations. The inner sepals have different colours, ranging from white, rose-tinged, purple-tinged, through to rose and pale purple. Petals also exhibited abundant colour variation, such as yellow, orange, purple, purple but laminae yellow-edged or yellow at both ends while purple in the middle. Although the specimens of E. mikinorii that can be referred to are very limited, the characters and the descriptions of some herbarium specimens were consistent with our observations. Some specimens from Enshi had yellow flowers (B. L. Guo & X. Z. Luo 89012) or the flower colour varied from pale yellow to pale purple and purple (B. L. Guo A29, B. L. Guo A50) or from yellow to orange and pale purple (B. L. Guo & J. J. Liu 0810).
According to our field investigation and the common garden experiment on two populations, parts of the spurs were almost straight, while most were slightly curved (Fig.
As far as the indumentum of leaves concerned, we observed that approximately 40% of the individuals from HBES (near its type locality) and some individuals from HBXT were with white appressed hairs abaxially. Moreover, all the previous descriptions and specimens on the flowering stem of E. mikinorii were with 2 opposite trifoliolate leaves. However, 3-whorled trifoliolate was also observed in the HBES population (S. X. Liu et al. 2016017).
CHINA. Hubei: Baiguo, Enshi, 754 m, 21 April 2016, S. X. Liu et al. 2016017 (
CHINA. Chongqing: Wushan, 850 m, 25 April 1987, H. R. Liang 144 (holotype: BCMM, lost); Chongqing: Wushan, 1000 m, 19 April 1989, B. L. Guo 89003 (neotype, designated by
Herbs 16–80 cm tall. Rhizome long creeping or compact, 1–5 mm in diam., internodes can be more than 10 cm. Leaves basal and cauline, usually trifoliolate or occasionally unifoliolate; leaflets of trifoliolate leaves narrowly ovate or lanceolate, 4.6–15.3 × 2.4–7.6 cm, apex acuminate, base deeply or shallowly cordate with a narrow sinus, terminal leaflet with equal and obtuse lobes, lateral leaflets conspicuously oblique with inner lobe small and obtuse, outer lobe larger and obtuse, acute or acuminate. Unifoliolate leaves ovate, broadly ovate or lanceolate, 5.0–13.0 × 2.5–6.5 cm, apex acuminate, base deeply cordate with lobes equal and obtuse or acute. Leaves coriaceous, margin spinous-serrate, adaxially deep green, obtuse, abaxially covered with villi. Petiolule, petiole and flowering stem with multicellular glandular hairs and villi, which are densest at nodes. Flowering stems usually have 2 opposite trifoliolate leaves, sometimes with 3 whorled trifoliolate leaves, 1 unifoliolate or trifoliolate leaf, rarely with 2 opposite unifoliolate or 2 leaves (alternate or opposite) with one trifoliolate and the other unifoliolate. Inflorescence racemose or compound with 8–24(–36)-flowered, 9.6–16 cm long; inflorescence axis and pedicels glandular pubescent. Pedicel 1–3 cm long. Flowers, ca. 3 cm, pale yellow, pale purple or purple. Sepals 8 in 2 whorls; outer sepals ovate, ca. 3.5 × 2 mm, red-purple; inner sepals narrowly ovate, 8–10 × 4–6 mm, white to faintly pink. Petals spurred without lamina, pale yellow, pale purple or purple, horn-shaped, 13–20 mm long. Stamens ca. 4 mm long; anthers yellow or green, ca. 3 mm long. Follicles oblong, 12–19 mm long; style rostriform. Seeds numerous.
Endemic to Chongqing, Western of China, usually occurs in forests or thickets. The elevations ranged from 850 m to 1160 m (Fig.
Epimedium glandulosopilosum flowers from April to May, and fruits from May to June.
The observations of the present study showed that only several individuals had yellowish flowers, while the rest had pale purple or purple flowers (Fig.
The protologue and the Flora of China described E. glandulosopilosum as “outer sepals narrowly ovate, 8–9 × 4–5 mm, inner sepals similar to outer sepals in size and shape” (
In the present study, all individuals from the population CQWX (Wuxi) were with long creeping and slender rhizomes (1–3 mm in diam.) (Fig.
The leaves of some individuals were densely covered with golden-yellow villi on the abaxial side. And the petiolule, petiole and flowering stem were covered with multicellular glandular-hairs and golden-yellow villous, which are densest at the nodes. However, these indumentum characters were not stable and exhibited great variation in colour and thickness. Depending on the individuals and/or developmental stage (young or old), the indumentum of the abaxial villi varied continuously from dense to sparse, and the colour was also not always typical golden-yellow, ranging from white to yellow.
Our field investigation showed that the flowering stem primarily had 2 opposite trifoliolate leaves. In addition, abundant variations, such as 1 unifoliolate or trifoliolate leaf, 2 opposite unifoliolate leaves or 2 alternate leaves with one trifoliolate and the other unifoliolate, were also observed. And all these styles were presented in two specimens (Wushan: B. L. Guo & X. Z. Luo 89003 and Wuxi: B. L. Guo A15).
CHINA. Chongqing: Tongcheng, Wuxi, 1159 m, 14 April 2004, B. L. Guo A15 (IMD); Tongcheng, Wuxi, 1161 m, 109°46', 31°23', 23 April 2016, S. X. Liu et al. 2016018 (
Key to the species of Epimedium in China
In total, 57 species and 6 varieties have been described from China, although 16 of these were designated as synonyms. Epimedium platypetalum var. tenue B.L.Guo & P.K.Hsiao was treated as synonym of E. pauciflorum (
1 | Leaves always unifoliolate | 2 |
– | Leaves usually trifoliolate, leaflets 3 or 9, sometimes 7 or 5, occasionally unifoliolate | 3 |
2 | Rhizome long creeping, 1.5–3 mm diam.; flowering stem usually with 1 leaf, occasionally with 2 leaves; leaves cordate, 2.5–4 × 3–4 cm, abaxially sparsely pubescent; inflorescence raceme or panicle; inner sepal light pink, 4.6–6 × 1.8–3.2 mm; spurs orange red, saccate, 1.5–2 mm long | E. elachyphyllum Stearn |
– | Rhizome compact, 2–5 mm diam.; flowering stem usually with 2 opposite leaves; leaves broadly ovate, 5–7 × 3–5 cm, glabrous on both surfaces; inflorescence panicle; inner sepal whitish, 4.5 ×2 mm; spurs yellowish brown, 2 mm long | E. muhuangense S.Z.He & Y.Y.Wang |
3 | Petals flat or flat with slightly cucullate base; flowers campanulate, spurless, yellow | 4 |
– | Petals saccate, slipper-shaped, or with spurs; flowers not campanulate, white, pink, purple or yellow | 7 |
4 | 30–50 cm tall; rhizome compact; leaflets coriaceous; inflorescence panicle, 30–80-flowered, 30–35 cm long, glandular; flower ca. 7 mm in diam.; petals flat with slightly cucullate base | E. reticulatum C.Y.Wu ex S.Y.Bao |
– | 20–50 cm tall; rhizome compact or long creeping; leaflets membranous; inflorescence raceme or panicle, 2–43-flowered, 7–23 cm long, glabrous or glandular; flower ca. 10 mm in diam.; petals flat | 5 |
5 | 35–50 cm tall; rhizome always compact, 4–6 mm in diam.; leaflets ovate, 4.5–6 × 2.5–4 cm; inflorescence panicle, 15–43-flowered, 11–23 cm long, glabrous; inner sepals red-tinged; petals spurless, obovate, 6–8 × 5–7 mm | E. campanulatum Ogisu |
– | 20–40 cm tall; rhizome long creeping or compact, 1–3 mm in diam.; leaflets subrounded or ovate, 2.5–4.5 × 2–4 cm; inflorescence raceme, 2–14-flowered, 7–16 cm long, glandular; inner sepals purple-red; petals spurless, oblong or obovate, 6–8 × 4–5 mm | 6 |
6 | 20–40 cm tall; rhizome always long creeping; leaves trifoliolate, 5-foliolate, sometimes 7-foliolate, leaflets ovate, 2.5–4 × 2–3 cm; inflorescence usually 7–14-flowered, 10–16 cm long, glandular; pedicels 1–2 cm long, glandular; out sepals pale purple, broadly ovate, 4 × 1.5 mm; inner sepals elliptic, 5 × 1.5 mm | E. ecalcaratum G.Y.Zhong |
– | 25–35 cm tall; rhizome compact or long creeping; leaves always trifoliolate, leaflets subrounded, 4.5 × 4 cm; inflorescence usually 2–6-flowered, 7–12 cm long, pedicels 0.5–1 cm long, out sepals green, triangular-lanceolate, 2 × 1 mm; inner sepals ovate, 4 × 1.5 mm | E. platypetalum K.Meyer |
7 | Petals with elongated curved spurs and basal laminae | 8 |
– | Petals with long slender spurs but without lamina, or petals very short | 23 |
8 | Leaves on flower stem biternate (leaflets 9), or 7-, 5-, 3-foliolate | 9 |
– | Leaves on flower stem always 3-foliolate, occasionally unifoliolate | 12 |
9 | 15–40 cm tall; rhizome long creeping; flowering stem always with 1 biternate leaf, leaflets ovate, 3–13 × 2–8 cm; inflorescence raceme, usually 3–8-flowered, 6–12 cm long, glabrous; pedicels 1–2 cm long, glabrous; flower yellowish or white, 2.5–3 cm in diam.; inner sepals narrowly ovate to lanceolate, 8–10 × 3–4 mm; spurs 10–15 mm; laminae ca. 6 mm high | E. koreanum Nakai |
– | 25–60 cm tall; rhizome compact; flowering stem usually with 2–4 leaves or 1 leaf (5, 3-foliolate); inflorescence raceme or panicle with 2–5-flowered peduncles below, usually 4–60-flowered, 6–32 cm long, glandular; pedicels 1.5–3 cm long, glandular; flower pale yellow or pale sulphur yellow, 2–4 cm in diam.; spurs 10–19 mm; laminae 6–13 mm high | 10 |
10 | 25–44 cm tall; flowering stem usually with 1 leaf or 2–3 leaves (5-, 3-foliolate); inflorescence raceme; usually 4–18-flowered, 6–17 cm long; inner sepals yellow, 11 × 4 mm; spur 10–14 mm | E. flavum Stearn |
– | 33–60 cm tall; flowering stem with 2–4 leaves (biternate or 7-, 5-, 3-foliolate); inflorescence panicle with 2–5-flowered peduncles below; usually 11–60-flowered, 14–32 cm long; inner sepals purplish red, 4–6.5 × 2–4 mm; spur 10–19 mm | 11 |
11 | 50–60 cm tall; flowering stem usually with 3 leaves, biternate, or leaflets 7, 5, 3; inflorescence 20–60-flowered, 20–30 cm long; petal spurs horizontally spreading, spurs 17–19 mm; laminae 6–7 mm high | E. xichangense Y.J.Zhang |
– | 33–60 cm tall; flowering stem usually with 2 leaves, leaflets 5 or 3; inflorescence 11–44-flowered, 14–32 cm long; petal spurs downward-curved, spurs 10–15 mm; laminae 7–13 mm high | E. davidii Franch. |
12 | Rhizome long creeping or compact; inflorescences usually raceme, occasionally compound below | 13 |
– | Rhizome always compact; inflorescences always panicle | 20 |
13 | Petals slightly shorter or nearly as long as inner sepals | 14 |
– | Petals longer than inner sepals | 15 |
14 | 25–35 cm tall; rhizome long creeping, 1 mm in diam.; leaflet ovate or narrowly ovate, 3–6 × 1–3 cm, almost glabrous or with scattered hairs; inflorescence 3–12-flowered, 12–14 cm long; pedicels 2–3 cm long, glabrous; flower 2.5 cm in diam., inner sepals white, spurs white, 15–18 mm, nearly as long as inner sepals; laminae 7–8 mm high | E. ogisui Stearn |
– | 18 cm (or longer) tall; rhizome compact, 4.5–8 mm in diam.; leaflet narrowly ovate, 6.5–11.2 × 3.7–6.1 cm, with scattered hairs; inflorescence 8–22-flowered, 10–17 cm long; pedicels 2–2.7 cm long, glabrous or sometime glandular; flower 3–3.8 cm in diam., inner sepals white, spurs deep purple, 15–17 mm, shorter or nearly as long as inner sepals; laminae 5–6 mm high | E. shennongjiaensis Y.J.Zhang & J.Q.Li |
15 | Flowers large, ca. 4–5 cm in diam | 16 |
– | Flowers less than 4 cm in diam | 17 |
16 | 30 cm tall; leaflet narrowly ovate, 6–9 × 2.5–4 cm, with scattered, short, erect hairs; inflorescence raceme, 8-flowered, ca. 20 cm long; pedicels 2.5–5 cm long, glabrous; flower 4–5 cm in diam., inner sepals white, elliptic, 16 × 8–9 mm; spurs white, slight yellowish or purple-tinged at base, 25 mm, elongated; laminae 7 mm high | E. latisepalum Stearn |
– | 25 cm tall; leaflet narrowly ovate, 4–8 × 2.5–5.5 cm, almost glabrous, or with scattered, appressed hairs; inflorescence raceme, 6–10-flowered, ca. 13 cm long; pedicels 2 cm long, glabrous; flower 4.5 cm in diam., inner sepals reddish, cymbiform, 6 × 2.5 mm; spurs pale yellow, 22 mm, elongated; laminae 10 mm high | E. fangii Stearn |
17 | Flowering stem usually with 1 trifoliolate, occasionally 1 unifoliolate leaf or 2 alternate trifoliolate leaves; 3–6-flowered | E. pauciflorum K.C.Yen. |
– | Flowering stem with 2 opposite trifoliolate leaves, occasionally 1 trifoliolate leaves or 3 whorled leaves; 6–18-flowered | 18 |
18 | Rhizome always long creeping, 1.5–2.5 mm in diam.; leaflet narrowly ovate, 4–5.5 × 2–2.5 cm, abaxially with appressed hairs; inflorescence always raceme, 6–9-flowered, 6–7 cm long; pedicels 1–1.5 cm long, glabrous; flower 1.5–2 cm in diam., inner sepals red, ovate-oblong, 5 × 2–3 mm; petals yellow, spur subulate, obviously curved, 12 mm long, much longer inner sepals; laminae 7 mm high | E. shuichengense S.Z.He |
– | Rhizome compact or long creeping, 2.1–5.6 mm in diam.; leaflet narrowly ovate, 6.8–19 × 2.5–6.3 cm, almost glabrous; inflorescence raceme or sometimes compound with 3-flowered peduncles below, 6–18-flowered, 8–15 cm long; pedicels 1.5–3 cm long, glabrous or glandular; flower 3–3.5 cm in diam., inner sepals white to pinkish, ovate, 11–14 × 5–10 mm; spur slightly curved, 15–16 mm long, a little longer inner sepals; laminae 5–7 mm high | 19 |
19 | 12–68 cm tall; rhizome long creeping or compact; leaflet narrowly ovate, 6.8–13.5 × 2.9–6.3 cm, almost glabrous or with minute hairs; flower stem with 2 opposite trifoliolate leaves or 1 trifoliolate leaf; flower ca. 3 cm in diam., inner sepals white to pale pink; petals purple, laminae 5 mm high | E. epsteinii Stearn |
– | 15–25 cm tall; rhizome long always compact; leaflet narrowly ovate, 7–19 × 2.5–5.5 cm, glabrous; flower stem with 2 opposite trifoliolate leaves; flower 3–3.5 cm in diam., inner sepals pinkish-lilac; petals chestnut-brown, spur pale greenish, laminae 7 mm high | E. stearnii Ogisu & Rix |
20 | Flower yellow or pale yellow, 3.5–4 cm in diam., petals with obvious basal laminae 7–8 mm high | 21 |
– | Flower usually purple, occasionally yellow, 2.5–3 cm in diam., petals with slight basal laminae 2–3.5 mm high | 22 |
21 | Leaflet oblong-elliptic or narrowly ovate, 8.1–15.5 ×3.6–6.3 cm, almost glabrous or sparingly pubescent; inflorescence compound with 2–3-flowered peduncles below, 7–38-flowered, 9–24 cm long, almost glabrous; pedicels 1–2 cm, glandular; flower 3.5 cm in diam., inner sepals broadly elliptic, 5–6 × 3–4 mm, purplish red; petals yellow, spur 15–18 mm long, much longer inner sepals; laminae 8 mm high | E. hunanense (Hand.-Mazz.) Hand.-Mazz. |
– | Leaflet lanceolate or narrowly lanceolate, 6.4–23 × 1.8–6.3 cm, abaxially pubescent; inflorescence panicle, 9–70(–100)-flowered, 13–30 cm long, sparsely glandular or glabrous; pedicels 0.7–1.5 cm, almost glabrous; flower ca. 4 cm in diam., inner sepals ovate, 12 × 6–8 mm, milky white; petals pale yellow, spur 20 mm long, much longer inner sepals; laminae 7 mm high | E. wushanense T.S.Ying |
22 | 27–54 cm tall; leaflet narrowly ovate to narrowly lanceolate, 6–14.2 × 2–6.1 cm, abaxially sparingly pubescent; inflorescence panicle, 11–45-flowered, 13–22 cm long, glabrous; inner sepals ovate or broadly ovate, 8–13 × 4–8 mm; spurs of petals slightly longer than inner sepals, 10–15 mm long, laminae 2–3 mm high | E. pseudowushanense B.L.Guo |
– | 26–94 cm tall; leaflet lanceolate, 8–17.4 × 3–8.6 cm, abaxially glabrous or sometimes sparingly pubescent; inflorescence panicle, 8–50(–85)-flowered, 7–30 cm long, glabrous; inner sepals elliptice, 11–16 × 7–12 mm; spurs of petals obviously longer than inner sepals, 15–20 mm long, laminae ca. 3.5 mm high | E. mikinorii Stearn |
23 | Petals very short, 2–8 mm, and much shorter than the inner sepals | 24 |
– | Petals with long slender spurs, 12–26 mm, without lamina | 33 |
24 | Rhizome always compact; stamens 7–10 mm long, conspicuous, protruding, filament much longer than anther | 25 |
– | Rhizome long creeping or compact; stamens 2–6 mm long, filament equalling or much shorter than anther | 27 |
25 | Inner sepals always spreading, narrowly elliptic, 8–10 × 3–4.5 cm; petals cucullate, obviously incurved; filament yellowish, 4.5–5 mm long; anthers green, 2.5 mm long | E. dolichostemon Stearn |
– | Inner sepals reflexing or slightly reflexing, ovate or narrowly lanceolate, 11–18 × 2.5–5 cm; petals almost straight; filament purple or white, 4–5 mm long; anthers green or yellow, 2–4 mm long | 26 |
26 | Leaflets narrowly ovate, 6.5–13.5 × 2.7–5.7 cm, abaxially glabrous; inflorescences panicle, 19–69-flowered, 10–28 cm long, glabrous; inner sepals ovate, 11 × 5 mm; petals purple, straight, 4 mm long; filaments purple; anthers green | E. qingchengshan G.Y.Zhong &B.L.Guo |
– | Leaflets narrowly ovate, 7.5–14.4 × 2.3–6.4 cm, abaxially glabrous or sparsely pubescent; inflorescences panicle, 9–48-flowered, 9.2–28.6 cm long, glandular; inner sepals narrowly lanceolate, 15–18 × 2.5–3.5 mm; petals purple, with whitish tip, straight, 6.5–9.5 mm long; filaments purple or white; anthers green or yellow | E. fargesii Franch. |
27 | Flower stem with 1 biternate leaf, 9 leaflets | E. brevicornu Maxim. |
– | Flower stem with 2 (occasionally 3) trifoliate leaves | 28 |
28 | Plant glabrous throughout; the two lateral leaflets not cordate at base but obliquely truncate | E. truncatum H.R.Liang |
– | Plant always with hairs; the leaflets all cordate at base | 29 |
29 | Inner sepals 5–12 mm long and flowers more than 10 mm in diam.; inflorescences glandular | 30 |
– | Inner sepals 3–5 mm mm long and flowers 6–8(–10) mm in diam.; inflorescences usually glabrous | 31 |
30 | Rhizome always compact; leaflets ovate, 8–9 × 4–7 cm; inflorescences 20–40-flowered; inner sepals lanceolate, 12 × 3–3.5 mm; petals with slight laminae and blunt spur | E. stellulatum Stearn |
– | Rhizome compact, sometimes elongated; leaflets ovate, narrowly ovate or lanceolate, 3–15 × 2–8 cm; inflorescences many-flowered, usually more than 50 flowers; inner sepals narrowly lanceolate, 5–10 × 1.5–2.5 mm; petals with blunt spur, almost straight, saccate | E. pubescens Maxim. |
31 | Inflorescences narrow and straight, 4–5 cm broad, 21–153-flowered; petals saccate, blunt, 2–4 mm long | E. sagittatum (Sieb. & Zucc.) Maxim. |
– | Inflorescences loose, 7–15 cm broad, 54–1140-flowered; petals slipper-shaped, 2–3 mm long | 32 |
32 | Leaflets narrowly ovate, 9.1–16.4 × 4.2–10.3 cm; inflorescences 7–9 cm broad, 54–572-flowered; outer sepals black or dark purple, petals orange-yellow and red | E. myrianthum Stearn |
– | Leaflets lanceolate or narrowly lanceolate, 13–18 × 2.5–4 cm; inflorescences usually 12–18 cm broad, 61–1142-flowered; outer sepals purplish, petals yellow | E. borealiguizhouense S.Z.He & Y.K.Yang |
33 | Leaves on flower stem biternate (9 leaflets) | E. elongatum Komarov |
– | Leaves on flower stem with 3 leaflets, occasionally 1 leaflet | 34 |
34 | Inflorescences usually raceme | 35 |
– | Inflorescences usually panicle | 40 |
35 | Leaflet 3.2–9.5 × 2.2–6 cm; flower 2–3 cm in diam.; inner sepals ovate, 5–7 × 2–4 mm | 36 |
– | Leaflet 3–16 × 2–8.6 cm; flower 3–4.5 cm in diam.; inner sepals narrowly ovate, narrowly lanceolate or narrowly elliptic 8–20 × 3–7 mm | 37 |
36 | Rhizome long creeping; leaflets ovate-deltoid to lanceolate, 3.7–8.2 × 2.2–3.4 cm; raceme with 8–15 flowers, inner sepals reddish, ovate, 5–7 × 2–4 mm, 1/3 to 1/4 length of petals, petals yellow, horn shaped, 15–22 mm | E. zhaotongense G.W.Hu |
– | Rhizome compact; leaflets elliptic or broadly ovate, 3.2–9.5 × 2.5–6 cm; raceme with 11–20 flowers, inner sepals pale yellow, 6–7 × 3.2–3.7 mm, more than 1/2 length of petals, petals pale yellow, nearly straight, 7–12 mm | E. enshiense B.L.Guo |
37 | Rhizome always compact; flower stem usually with 2 opposite leaves; inflorescences glabrous; flowers ca. 4.5 cm in diam.; inner sepals pale yellow, ca. 2/5 length of petals, petals sulphur-yellow, ca. 20 mm | E. franchetii Stearn |
– | Rhizome long-creeping, sometimes compact; flower stem with 2 opposite leaves or 1 leaf; inflorescences glandular; flowers 3–4 cm in diam.; inner sepals whitish, pale pink or rose, 2/3 to 3/4 length of petals, petals pale purplish red, rose, pale yellow or whitish, 13–26 mm | 38 |
38 | 16–80 cm tall; inflorescences raceme, sometimes panicle, 8–24 (–36) flowers, ca. 3 cm in diam.; inner sepals narrowly ovate, 8–10 × 4–6 mm; petals horn-shaped, 13–20 mm | E. glandulosopilosum H.R.Liang |
– | 12–50 cm tall; inflorescences always raceme, 3–14 flowers, ca. 3–4 cm in diam.; inner sepals narrowly lanceolate or narrow elliptic, 11–20 × 3–7 mm; petals horn-shaped, 15–26 mm | 39 |
39 | Rhizome always long-creeping, 1–3 mm in diam.; leaflets ovate or narrowly ovate, 3–11 × 2.3–5.7 mm, almost glabrous with only a few scattered hairs; inner sepals narrowly lanceolate, 15–17 × 3–4 mm; petals purplish red, 15–20 mm | E. sutchuense Franchet |
– | Rhizome long-creeping or compact, 1–5(–8) mm in diam.; leaflets narrowly ovate or ovate, 3–16 × 2–8.6 cm; inner sepals narrowly elliptic, 11–20 × 4–7 mm; petals rose, pale purple, occasionally yellowish, 15–26 mm | E. leptorrhizum Stearn |
40 | Leaflets broadly ovate or ovate, 4–6 × 2–3 mm; flower stem with 2 opposite or alternate leaves; inner sepals red, 1/5 to 1/4 length of the petals | E. membranceum K.Mey. |
– | Leaflets narrowly lanceolate, lanceolate, narrowly ovate, or ovate; flower stem with 2 opposite or occasionally 3 whorled leaves; inner sepals white, pale yellow, purple or reddish-purple, 1/4 to 3/4 length of the petals | 41 |
41 | Leaflets abaxially densely and fully covered with long and tangled white hairs, thick as a blanket; inner sepals 3/4 length of the petals; petals deep purple; spur 2.3–3 cm | E. zhushanense K.F.Wu & S.X.Qian |
– | Leaflets abaxially glabrous or pubescent; inner sepals 1/4 to 2/3 length of the petals; petals white, pale yellow, yellow or purple; spur13–25 mm | 42 |
42 | Flower purple, purplish or yellowish; pedicels glabrous or occasionally glandular, 1–5 cm; inner sepals 1/2 to 2/3 length of the petals | 43 |
– | Flower always yellow; pedicels glandular, 1.5–2 cm; inner sepals 1/4 to 1/3 length of the petals | 44 |
43 | 40–60 cm tall; rhizome always compact; leaflets thick, fleshy, ovate to narrowly ovate, 4.1–5.6 × 2.1–2.7 mm, abaxially glabrous; flower 2–4 cm in diam.; inner sepals margin corrugated, ovate-elliptic, 6–21 × 3–9 mm; petals a little longer than inner sepals, 1.3–2.0 cm; chromatids 4n=24 | E. yingjiangense M.Y.Sheng & X.J.Tian |
– | 20–80 cm tall; rhizome compact, sometimes long creeping; leaflets leathery, narrowly ovate to lanceolate, 3–19.8 × 1.5–8.9 mm, abaxially with dense or sparse hairs or glabrous; flower 3–5 cm in diam.; inner sepals with smooth margin, ovate-elliptic, 6–21 × 3–9 mm; petals much longer than inner sepals, 15–25 mm; chromatids 2n=12 | E. acuminatum Franch. |
44 | 40–86 cm (usually 70–80 cm) tall; leaflet lanceolate to narrowly lanceolate, 11.5–17.6 × 2.7–4.1 cm, abaxially glabrous or sparingly pubescent; inflorescence panicle, 20–100-flowered, 20–40 cm long, glandular; inner sepals ovate, 5–6 × 3 mm, inner sepals 1/4 length of the petals; spur horn-shaped, 15–25 mm | E. jingchengshanense Y.J.Zhang & J.Q.Li |
– | 28–59 cm tall; leaflet lanceolate, 8–12 × 1.2–4.1 cm, abaxially sparingly or densely pubescent; inflorescence panicle, 25–32-flowered, 12–23 cm long, glandular; inner sepals elliptic or narrowly ovate, 10–12 × 5-6 mm, inner sepals 1/2 to 1/3 length of the petals; spur horn-shaped, 20 mm | E. ilicifolium Stearn |
Although the genus Epimedium is colourful in flower, from white, through yellow, to rose and purple, intraspecific flower colour variation is relatively uncommon. Before this study, only the polymorphism of E. grandiflorum and E. acuminatum has been described in the monograph or in the Flora of China (
Epimedium acuminatum was the species with the best-known colour variation. The flower colour of E. acuminatum was described as “white, yellow, rose-purple or pale violet” in Flora of China (
It is very interesting and unexpected that we observed abundant intraspecific flower colour diversity. Our study suggests that the flower colour is not as stable as previously imagined. Therefore, flower colour seems to be a feature liable to great variation within some species and its taxonomic value should be discounted. From the geographical distribution of the five species, the results are consistent with the viewpoint that the comparatively unstable species often occur in western China where the genus is best represented and its evolution is still ongoing (
Although abundant flower colour variation has been observed in the present study, the reason for, or mechanism of, the colour variation is still unclear. The natural variation in flower colour may occur via the deposition of various anthocyanin pigments (
From another perspective, our results could have important implications for the utilisation of germplasm. Bearing lovely foliage and graceful flowers, Epimedium plants were previously mainly introduced as garden plants in Europe and America (
In this study, based on the extensive field investigation of populations during flowering seasons, comprehensive descriptions and illustrations for five Epimedium species were established. The flower colour used to be an important character in delimiting species in Epimedium (Stearn, 2002;
This research is supported by the National Science Foundation of China (31360036; 31100146), the National Science Foundation of Jiangxi Province (20181BAB205075) and Yong Scientists Fellowship of Jiangxi Province (20133BCB23024). We thank the Herbariums that made their specimens accessible for this study. We also give sincere thanks to Dr. Qiner Yang for his constructive comments on our earlier version of this manuscript. Finally, we express special gratitude to Subject editor (Marco Pellegrini) and reviewers (Rafael Felipe de Almeida, Joachim Kadereit and an anonymous reviewer) for their excellent comments that improved our paper.