Research Article |
Corresponding author: Dai-Ke Tian ( dktian@cemps.ac.cn ) Academic editor: Jan Wieringa
© 2020 Dai-Ke Tian, Yan Xiao, Yan-Ci Li, Ke-Jian Yan.
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:
Tian D-K, Xiao Y, Li Y-C, Yan K-J (2020) Several new records, synonyms, and hybrid-origin of Chinese begonias. PhytoKeys 153: 13-35. https://doi.org/10.3897/phytokeys.153.50805
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Begonia is a mega-genus with about 2500 species by most estimates, with China having over 210 accepted species. After field surveys, literature review and examination of herbarium specimens, some new taxa, new records, synonyms and the hybrid-origin of some taxa have been confirmed. Here, we report that Begonia dioica Buch.-Ham. ex D.Don and B. flagellaris Hara, both from Xizang (Tibet) are new to China; Begonia lipingensis Hance, B. muliensis T.T.Yu and B. sizemoreae Kiew are synonyms of B. circumlobata Hance, B. taliensis Gagnepain and B. longiciliata C.Y.Wu, respectively; and Begonia × lancangensis S.H.Huang and B. × malipoensis S.H.Huang & Y.M.Shui are natural hybrids.
Begoniaceae, China, the Himalayas, natural hybrid, Nepal, stolon, taxonomy, Tibet
Begonia is a mega-genus with an estimated 2500 species (
In September 2017, Daike Tian and his associates searched for wild begonias in Xizang (Tibet) of China. During this trip, two new records of stoloniferous begonias were discovered, namely Begonia dioica Buch.-Ham. ex D.Don (
Begonia dioica Buch.-Ham. ex D.Don [sect. Diploclinium] D. Don, Prodr. Fl. Nepal. 223. 1825: 223; R. Camfield & M. Hughes, Eur. J. Taxon. 396: 35. 2018.
Tuberous, creeping, stoloniferous, dioecious, deciduous herb, 3–11 cm high. All plant parts glabrous. Tubers 2–3 (1–2 old, one new). Stolon: usually one to three developing from previous year’s tuber, red, slender, 5–60 cm long, 1–2 mm thick, usually unbranched, rarely branched or towards the apex with many fibre-like branches in large individuals, one to many tiny white aerial bulbs on stolon tips, gradually turning red after stolons touch moss or rock surface. Stipule: lanceolate, 3–4 × 1–2 mm, glabrous, caduceus. Leaf: 1 per plant, basal, petiole green to red, 1–22 cm long, 1.5–5 mm thick, adaxially shallowly grooved along the full length; lamina narrowly deltate-ovate, basifixed, symmetric, 2.5–17 × 1.5–10 cm, upper surface green, underside green, pink green or red, venation palmate, 8–9, green to red, adaxially impressed, abaxially prominent, tertiary even secondary veins invisible; base shallowly cordate, auricles non-overlapped, margin crenate to dentate or double serrate; apex acuminate. Inflorescence: cymose, usually 1, terminal, 8–22 cm long, rachis pink to red, 6–10 cm long, 1–2 mm thick; peduncle branched up to three times, primary 5–10 cm long, secondary and tertiary 3–5 mm long, with 2–5 female flowers or 3–5 male flowers. Bract: lanceolate 2–8 × 1–2 mm, caduceus. Male flower: pedicel 10–25 mm long; tepals 4; outer tepals ovate-orbicular, 6–15 × 5–10 mm, pink to red, margin entire; inner tepals elliptic, 4–8 × 2–4 mm, white to pale pink; androecium with 15–20 stamens; filaments 1–2 mm long, unequal, fused at base into a short column; anther obovate, 1 mm long, dehiscing via short slits near the tip, not hooded, connective not extended. Female flower: pedicel 12–30 mm long; bracteoles absent; tepals 3 (occasionally 2), persistent, outer two larger, elliptic-ovate, nearly equal, 6–15 × 6–10 mm, pink to red, inner one smaller, lanceolate, 6–7 × 3–5 mm, white to pink; ovary 3–locular, placentae bifid; styles 3, persistent, deeply forked once and spirally 1.5–2 circled. Fruit: pendulous, capsule ellipsoid, 7–10 × 6–8 mm; wings 3, unequal or nearly equal, red or reddish-green, rounded-triangular, 2–6 × 7–12 mm, stalk red, 15–40 mm long, 0.8–1 mm thick.
. Habitat and morphology of Begonia dioica (Photos by Daike Tian) A, B habitat (rock-moss surface and tree trunk, arrows indicate begonia plants) C individuals with long red stolons (arrows indicate stolons) D plants of different size and stolons with small whitish aerial bulbs (arrows indicate tiny bulbs) E leaves showing glabrous adaxial (upper) and abaxial (low) surfaces F female flowers with three tepals (upper: adaxial view, low: abaxial view) G cross-section of ovary with bilamellate axile placenta and three locules H tubers under moss.
Xizang (Tibet): Chentang Zhen of Dingjie Xian, 87°26'30.70"N, 27°50'54.11"E, alt. 2427 m, on rock surface and tree trunks. 19 Sept 2017, Daike Tian, Yan Xiao and Zhu Lu TDK3306 (CHS).
Southern Xizang of China, northern Pakistan, northern India, Nepal and Bhutan; alt. 1350–2430 m; Flowering July to September, fruiting August to November.
Least Concern (LC). Begonia dioica has numerous suitable habitats throughout its distribution range (
Most of the individuals develop long stolons only from tubers formed in the previous year. The stolons are often branched in large individuals and the branch tops produce one to many tiny whitish bulbs, which grow larger as they touch the surface of a rock, tree trunk, soil or moss and then can develop into small plants in the second year. The tepals of female flowers are always persistent, even as the fruits mature.
Begonia flagellaris Hara [sect. Diploclinium] J. Japan. Bot. 48(12): 358–359, f. 3 (1973).
Tuberous, stoloniferous, dioecious, deciduous herb, 2–20 cm tall. Tubers usually 2–4 (1–3 old, red-brown, one new, white) connected, 3–15 mm diameter. Stolon: developing from underground tubers or inflorescence; usually one per plant, green, unbranched to rarely branched, glabrous, slender, 10–50 cm long, 2–5 mm thick, aerial bulbs produced at stolon tips, 1–5 mm thick. Leaf: usually one basal large and none to several smaller cauline (on stolons or peduncles), petiole green, 2–28 cm long, 1.5–7 mm thick, sparsely hairy; lamina basifixed, symmetric or nearly so, cordate, 2.5–26 × 1.2–28 cm, adaxial surface green, with short warty-base hairs, underside pale green, sparsely hairy; venation palmate, 9–11, green, adaxially impressed, abaxially prominent, base cordate, auricles non-overlapped to slightly overlapped, margin irregularly serrate to occasionally double serrate, rarely one to few shallowly lobed; apex acuminate. Inflorescence: simple umbellate, 1–2 from the lower part of the stem, 6–20 cm long, rachis green to pink, 4–17 cm long, 2–3 mm thick; peduncle nearly erect, glabrous. Male flower: white to pinkish, pedicel 14–28 mm long, 1 mm thick, top sparsely hairy; corolla 18–24 × 10–12 mm, tepals 4, outer 2, ovate, subequal, 7–12 × 7–11 mm, upper one centre thick and concaved, adaxially white hairy, up 1 mm long, less hairy on lower tepal; inner 2, glabrous, obovate to obovate-lanceolate, 7 × 4–5 mm; androecium leaning towards upper tepal, stamens 10–14, filaments free, about 1 mm long, anther elliptic, up to 1.5 mm long, 0.8 mm wide, apex obtuse. Female flower: pedicel 20–35 mm long, 1 mm thick; tepals 5, unequal, glabrous; ovary hairy, 3-locular, placentae bifid; stigmas and styles 3. Fruit: pendulous, capsule ellipsoid, 6–9 × 4.5–5 mm; wings 3, unequal, green, adaxially wing extremely long, narrowly triangular, 10–28 × 5–7 mm, lateral wings extremely narrow to nearly absent; stalk red at lower part, 24–40 mm long, 1 mm thick.
Habitat and morphology of Begonia flagellaris (Photos by Daike Tian) A, B habitat (rock hill or under bamboos, arrows indicate begonia plants) C individuals with long stolons D flowering plant E individual with aerial bulbs on stolon tips (arrows indicate tiny aerial bulbs) F fruit with extremely unequal wings G large individual with stolons (arrows indicate stolons) and fruits H simple umbellate inflorescence with white male and female flowers I infructescence J male flowers in front, dorsal and side views, respectively K cross-section of an ovary with the bilamellate axile placenta and three locules L underground tubers.
Xizang: Jilong Xian, Jilong Zhen, under bamboos, 85°21'12"N, 28°21'41"E, alt. 2030 m, 23 Sept 2017, Daike Tian, Yan Xiao and Zhu Lu, TDK3343 (CHS); on steep slope under forest or rocky hill, 85°21'43"N, 28°21'48"E, alt. 2360 m, same date, Daike Tian, Yan Xiao and Zhu Lu, TDK3344 (CHS).
China: Xizang, Jilong Xian, Jilong Zhen, border of China and Nepal; Nepal. Alt.1650–2900 m. Flowering August to September (early October), fruiting September to November.
Near Threatened (NT). Begonia flagellaris is distributed in both Nepal and China, and there are many individual plants in each population. However, this species should be considered as Endangered (B1ab(iii)) for China because only two populations have so far been found and both are by the roadside.
Stolons develop from underground tubers or the top of inflorescence (usually on larger plants), with several small leaves. Hara (
-Begonia lipingensis Irmscher, Mitt. Inst. Allg. Bot. Hamburg 6: 353, 1927 (
China, Canton (Guangdong), 05 Oct 1881, Rev. Benjamin Couch Henry s.n. (BM000944652, BM!).
Begonia lipingensis has been treated as a species differing from B. circumlobata in Flora Reipublicae Popularis Sinica (
Begonia lipingensis and B. circumlobata (E–H photos by Daike Tian) A–E Begonia lipingensis: A holotype (WU) (digitalised by Herbarium of Institut fur Botanik der Universitat Wien) B close-up view of type leaf C close-up of male flower from holotype, showing abaxial hairs on the middle of outer tepals D wild blooming plants E, F male flowers showing colour variation G, H Begonia circumlobata: adaxial (G) and abaxial (H) views showing variations of leaf lobes and colour in a single small population.
Begonia circumlobata displays significant variation in plant size, morphology of leaves, and flowers (Fig.
Begonia circumlobata is widely distributed in at least seven provinces of China, from western Hubei to Hunan, Jiangxi, Fujian, Guangdong, Guangxi and Guizhou, growing on flat areas, steep slopes or rock surfaces along or near stream and valley. Alt. 200–1230 m (Fig.
Least Concern (LC) due to wide distribution and usually large populations. However, in some places, a small number of plants with variegated leaves (adaxially white spots) have high value as ornamentals. Therefore, these variegated individuals may be over-collected by humans.
Begonia circumlobata has sparsely hairy leaf blades and outer tepals of male flowers (Fig.
-Begonia sizemoreae Kiew, Gard. Bull. Singap. 54(6): 95–100, 2004. syn. nov. Type: Vietnam, Ha Tay Province: Ba Vi National Park, no date, R. Kiew 5304 (holotype: SING!; isotype: HN!).
China, Guizou: Anlong, alt. 990 m, 14 May 1960, Guizhou Exped. 5117 (holotype: KUN!; isotye: PE!).
Begonia longiciliata (Fig.
Morphological variation of Begonia longiciliata in China(Photos by Daike Tian) A–E population from Guizhou Province: A individual with dark green leaves and white variegation (near white ring or isolated white spots) B pure green-leaved individual C fruit with one long wing and two short wings D comparison of adaxial (upper) and abaxial (low) views of leaf variation in colour and variegation E male flower (deep-pink one not shown) F–J population from Yunnan province: F female flower, showing pink variant G cross-section of ovary showing two locules and bilamillate placenta H dark-green leaved individual with a light-green ring band I male flower showing very long anther in upper portion of androecium J comparison of adaxial (upper five leaves) and abaxial (lower five leaves), showing differences in leaf colour and variegation of different individuals.
Begonia longiciliata has been wrongly treated as B. rex in China (
Comparison on hairy and glabrous adaxial leaf surface of B. longiciliata A plant with hairs (cultivated as Begonia U388, American Begonia Society Conference 2012) B Guizhou population with hairs (arrow direction) C Yunnan population with glabrous adaxial leaf surface.(Photos by Daike Tian).
China: Yunnan, Jiangcheng: Kukazai Qushui, 14 Dec. 1991, Guoda Tao 49032; Tukahe, 18 Dec 1991, Guoda Tao 47818, 49127 (HITBC); Jiahe, 23 Sept 2015, Daike Tian et al. TDK2659 (CHS). Pingzhangzhai, Pingzhang village, Jiahe, 30 Oct 2012, Jiangcheng Survey Team 5308260564 (IMDY); Jiahe to Xiaoheijiang, 21 Oct 2011, Daike Tian et al. TDK252, TDK253 (CHS); Jiangcheng county to Daheishan, 21 Oct 2011, Daike Tian et al. TDK257 (CHS). Jinping: Riverside, 22 Oct 2008, Xiaohua Jin 9467 (PE); Laomeng, 22 Nov 2007, Yumin Shui et al. 80105 (KUN). Lüchun: Laomenghe, 22 May 1974, Lüchun Team 1092 (KUN); Huanglianshan, 30 Oct 1995, Sugong Wu et al. 379 (KUN), 31 Oct 1995, Sugong Wu et al. 3354 (KUN), Sugong Wu et al. 3354 (PE), 01 Nov 1995, Sugong Wu et al. 2609 (KUN); Xiaohejiang, 18 Oct 2000, Yumin Shui & Wenhong Chen 13132, 13797 (KUN); Erpu to Banpo, 22 Oct 2000, Yumin Shui & Wenhong Chen 13620, 13696 (KUN); Erpu to Dapu, 23 Oct 2000, Yumin Shui & Wenhong Chen 14138 (KUN); 24 Oct 2000, Yumin Shui & Wenhong Chen 13848 (KUN); Xinzhai, Erpu, 03 Nov 2007, Yumin Shui et al. 72970 (KUN); Shiyazi, Daheishan, 22 Nov. 2011, Jianghai He et al. HLS0353 (KUN); Lüchun county to Manhao of Gejiu county, 25 Aug 2013, Daike Tian et al. TDK1281, TDK1283 (CHS); Daheishan, 23 Sept 2015, Daike Tian et al. TDK2661 (CHS); Dashuigou, 23 Sept 2015, Daike Tian et al. TDK2663 (CHS); Cheli of Pinghe, 23 Sept 2015, Daike Tian et al. TDK2680 (CHS); Xiaoheijiang, Xinzhai of Pinghe, 24 Sept 2015, Daike Tian et al. TDK2683, 2685 (CHS). Luquan: Mayu, 30 Oct 1995, Sugong Wu et al. 379 (PE). Mengla: Xishuangbanna Tropical Botanical Garden, Menglun, 21 Sept 2015, Daike Tian et al. TDK2629 (CHS) (cultivated). Guangxi, Longlin: Jinzhongshan, 23 May 1977, Zhou Fakai 3-0701 (GXMI); Same locality, 24 Sept 1984, Chinese Medicine Team 0185 (GXMI). Tian’e: Xiangyang, 01 May 1978, Tian’e Team 4-6-0255 (GXMI). Guizhou, Anlong: Huali of Tingya, 14 May 1960, Zhisong Zhang & Yongtian Zhang 3320 (PE); Xiaojiatang, Lishu village of Dushan, 15 Oct 2017, Daike Tian et al. TDK3473 (CHS); Xiaoanhe, Pojing of Dushan, 15 Oct 2017, Daike Tian et al. TDK3474 (CHS). Xingyi: Daojiao, Gongqiao of Zerong, 14 Oct 2017, Daike Tian et al. TDK3460 (CHS). Zhenfeng: 19 Sept 1936, Shiwei Deng 90987 (IBSC). Unknown county: Feb 1921, M. Cavalerie, unknown collection no. (P06841311) (P); Oct 1917, M. Esquirol, unknown collection no. (P05495115) (P).
Laos: Phongsaly, Tan et al. L0559 (HITBC) (
Vietnam: Ba Vi National Park, Ha Tay province, R. Kiew 5304 (SING, HN); Tonkin (Mountain Bavi), Dec 1887, B. Balansa 3765 (P); Tonkin, 29 Apr 1936, M. Polane 25811 (P).
China: Guangxi (Longlin, Tian’e), Guizhou (Anlong, Xingyi, Zhenfeng), Yunnan (Jiangcheng, Jinping, Lüchun, Luquan); Laos (Phongsaly); Vietnam (Ba Vi) (Fig.
Near Threatened (NT). Begonia longiciliata has a relatively broad distribution, particularly in the borders of China, Laos and Vietnam (Fig.
Begonia longiciliata has been treated as a synonym of B. rex for a long time in China (
-Begonia muliensis T.T.Yu, Bull. Fan. Mem. Inst. Biol., 1:119, 1948 (
China,Yunnan: Tali (Dali), 4 Sept. 1883, J.M. Delavay 220 (Lectotype, P!, designated here).
Begonia taliensis is relatively widely distributed in many counties from Yunnan Province to Sichuan Province in China (Fig.
Habitat and morphology of B. taliensis (Photos by Daike Tian) A habitat B population with pure-green leaves C, D blooming individuals with variegated leaves E comparison of variegated and solid green-leaved individuals (adaxially and abaxially views) F–H inflorescence of large individuals and young fruits with red lines (G) I underground tubers (usually 2–3 connected) with numerous roots.
China: Sichuan (Daocheng, Dechang, Luding, Meigu, Mianning, Muli, Panzhihua, Shimian, Tianquan, Yanbian, Xide); Yunnan (Dali, Eyuan, Heqing, Lijiang, Yangbi, Yongsheng, Zhongdian) (Fig.
Begonia taliensis has a relatively-wide distribution (recorded or observed in nearly 20 counties of two provinces in China, Fig.
The leaf colour of B. taliensis varies amongst populations and occasionally even amongst the individuals of a small population. The plants usually have leaves with abaxially purple-red blotches. Sometimes, a few plants or even all individuals of a small population are pure green in leaf colour. The leaf could be shallowly to 1/2 deeply lobed (vs. over 2/3 deeply lobed for B. imitans) depending on plant size or distribution site. The flower number ranges from around 10 for a small flowering individual to over 100 for a large one.
Comparison of types of Begonia taliensis (A–C) and B. muliensis (D) A Ducloux No. 5184 (Yunnan) B Delavay No. 220 (Yunnan) C Henry 8946 (Sichuan) D T.T. Yü #14024 (Sichuan) (A accessed JSTOR and imaged by Botanical Museum Berlin-Dahlem B, C. Photos by Daike Tian at Herbarium Museum of Paris D accessed JSTOR, Imaged by Herbarium of the Arnold Arboretum, Harvard University).
Natural hybridisation is very common in Begonia and 50 populations of 31 natural hybrids involving 29 species have been recorded in Chinese wild begonias (
-Begonia langcangensis S.H.Huang, Acta Bot. Yunnanica 21:13, 1999; S.H. Huang & Y.M. Shui in C.Y. Wu (ed.), Fl Yunnan 12: 230, 2006; T.C. Ku et al. in C.Y. Wu & P.H. Raven (eds), Fl. China 13: 181, 2007.
Begonia langcangensis was described and published in 1999 and its type collection was made from Fazhan He of Lancang County in Yunnan Province. Since then, no additional specimens have been collected. During our field surveys in 2010 and 2017, respectively, we did not find any plants of this taxon in the type locality and only observed B. acetosella Craib (
China: Yunnan, Lancang, only seen in type locality, alt. 1600 m; Laos: Luang Namtha Province, Nam Ha National Biodiversity Conservation Area, Near Na Lun Village, alt. 687 m (
Regionally Extinct (RE). The living plants of Begonia × lancangensis have not been found in the type locality during field surveys after its first description. Recently, however, other researchers found wild plants in Laos (
Like B. acetosella, B. handelii and B. silletensis C.B.Clarke (
-Begonia malipoensis S.H.Huang & Y.M.Shui, Acta Bot. Yunnanica 16:333, 1994.
Begonia malipoensis was described for the first time in 1994 and its type locality is Douchidian of Malipo Xian, Yunnan Province (
Begonia × malipoensis and its parents (B. hemsleyana and B. versicolor) (Photos by Daike Tian) A habitat of a natural hybrid zone of B. versicolor × B. hemsleyana B–E variation of B. × malipoensis F B. hemsleyana G, H B. versicolor with variegated and pure green leaves I, J comparison of B. × malipoensis (middle two leaves) and its parents B. hemsleyana (left) and B. versicolor (right two leaves) (I adaxial view J abaxial view).
The hybrid B. × malipoensis is derived from either B. hemsleyana × B. versicolor or B. versicolor × hemsleyana. No significant differences were observed in the hybrid when either B. hemsleyana or B. versicolor acts as the mother plant. However, based on a presumed closer distance with mother plants and molecular data (
B. × malipoensis has only been seen in Malipo and Pingbian counties in Yunnan Province. Flowering June to July, fruiting July to September.
Critically Endangered (C2a(i)). It is extremely narrowly distributed with less than 100 mature individuals and can only be found in the hybrid zones of two locations in China. The hybrid plants are continuously collected by horticultural researchers or plant enthusiasts, mainly for ornamental purposes.
B. × malipoensis is difficult to bloom under ex-situ cultivation. When the seeds from an artificial cross between B. hemsleyana and B. versicolor were sown, the plants produced had various types of leaf colour and colour patterns (
The National Natural Science Foundation of China (Grant code: 31570199) and the Shanghai Administration Bureau of Landscape and City Appearance (Grant code: F122416) funded this study. The authors are also grateful to Li-Zhi Tian from Songjiang Agricultural Investment Co. Ltd., Pei-Song Zhang from Xishuangbanna National Nature Reserve of Yunnan, Zheng-Ming Zhu from Huanglianshan National Nature Reserve of Yunnan and Ce-Hong Li from Emeishan Botanical Garden of Sichuan for their help on field surveys and to Wen-Ke Dong from Beijing Green Garden Group Co. Ltd. for his suggestion on manuscript improvement. Specimens were accessed by http://plants.jstor.org/ or examined by visiting herbaria of the Museum National d’Histoire Naturelle Paris, the Botanic Garden and Botanical Museum Berlin, Royal Botanic Garden Edinburgh and Harvard University. Special thanks are given to Stephen Maciejewski, Vice-president of American Begonia Society and Michael LoFurno, Adjunct Professor of Temple University, Philadelphia, USA, for editorial assistance.