Several new records, synonyms, and hybrid-origin of Chinese begonias

Abstract 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.


Introduction
Begonia is a mega-genus with an estimated 2500 species (Tian et al. 2018) and, so far, there are about 1978 known accepted species (Hughes et al. 2015-present). China has over 210 accepted names of Begonia and its southwest region is one of the distribution centres of this genus. In the past two years, ten Begonia species were newly described (Chen et al. 2018aDing et al. 2018;Li et al. 2018Li et al. , 2019He et al. 2019;Tong et al. 2019;Wang et al. 2019a) and many more are likely awaiting discovery and description in China. At the same time, several newly-recorded Chinese Begonia species (Yang et al. 2015;Wang et al. 2019b) and synonyms (Shui and Chen 2017;Chen et al. 2018b) have also recently been reported. With the support of the National Natural Science Foundation of China, we conducted many field surveys along with a review of literature and herbarium specimens related to Chinese Begonia. The diversity of Chinese Begonia is now better understood and several taxonomic issues have been resolved. Here, we report two new records, three new synonyms and two hybrid-origins of Begonia in China. Their conservation status was evaluated according to Guidelines for Using the International Union for Conservation of Nature (IUCN) Red List Categories and Criteria (v. 14) (IUCN Standards and Petitions Subcommittee 2019).
Remarks. 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. Description. 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. Remarks. Stolons develop from underground tubers or the top of inflorescence (usually on larger plants), with several small leaves. Hara (Hara 1973) compared the similarity between this species and B. picta J.E.Smith (Smith 1805); however, the two are quite different in appearance. Begonia flagellaris is mostly similar to B. adscendens C.B.Clarke (1890: 26), but differs mainly by having long stolons and more hairs on the outer tepals of the male flowers.  (Ku 1999) and Flora of China (Gu et al. 2007). The species was based on small-sized mature plants that were collected from Liping County of Guizhou Province, China ( Fig. 3A-C). However, the species could not be separated when comparing the specimens and living plants in the wild. Many specimens stored in herbaria of China or other countries were identified with both names. After our careful review of type specimens and comprehensive field surveys on a large number of populations of both entities, it was confirmed that no differences could be found between them. Since B. lipingensis was described later, it should be considered as a synonym of B. circumlobata.

Begonia circumlobata
Begonia circumlobata displays significant variation in plant size, morphology of leaves, and flowers ( Fig. 3E-H). The leaves may be shallowly to very deeply lobed in the same population, even for the same individual and very few of the plants are shallowly double-lobed like B. jinyunensis C.I Peng, B.Ding & Q.Wang (Ding et al. 2014) (Fig. 3G, H). The leaves of most plants are pure green on two sides, while others may have deep green leaves with abxially red surface. Occasionally, variegated plants with white-spotted leaves could be seen in some populations such as in Huangsang National Nature Reserve of Suining, Hunan Province. Flowers can be white, whitish-pink, pink or nearly red (Fig. 3D, E).
Distribution and phenology. 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. 4). Flowering June to September, fruiting July to October.
Conservation status. 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.
Remarks. Begonia circumlobata has sparsely hairy leaf blades and outer tepals of male flowers (Fig. 3C). It is most similar to B. jinyunensis and B. laminariae, particularly in the morphology of its leaves, flowers and fruits. Begonia circumlobata is also easily confused with some individuals of B. pedatifida Lév. (Léveillé 1909), particularly when examining herbarium specimens. Unpublished morphological and molecular data (Tian et al.) suggests that B. jinyunensis should be treated as a subspecies of B. circumlobata. At the same time, a study is ongoing concerning the taxonomic relationship of B. circumlobata, B. lamiariae Irmsch. (Irmscher 1951)  Note. Begonia longiciliata (Fig. 5) is mostly close to B. rex Putz. (Putzey, 1857), but differs mainly by its narrower tepals of both its male and female flowers and longer anthers (up to 4 mm long) with acuminate tips that occur towards the apex of the androecium (Fig. 5I). Notably, it has large variation in leaf colour, variegation patterns and flower colour varying from white, pink to even nearly red (Fig. 5). Begonia rex is only found in India, while B. longiciliata has a wide distribution from Guizhou, Guangxi and southern Yunnan of China, to the north of both Laos and Vietnam (Fig. 7). The name longiciliata probably refers to the long fibre-like hairs found on the adaxial leaf surface in some populations of this taxon in Guizhou Province (type locality) (Fig. 6B), but most populations have glabrous adaxial leaf surface or nearly so (Fig. 6C) particularly in Yunnan Province. It is also similar to B. annulata K.Koch (Koch, 1837) in leaf morphology, but can be easily separated by the latter's hairy (vs. glabrous) tepals of both male and female flowers and fruits (Camfield and Hughes 2018).
Begonia longiciliata has been wrongly treated as B. rex in China (Ku 1999;Gu et al. 2007) and was even treated as a new species (B.    (Fig. 7). Alt. 300-1300 m. Flowering May to November, fruiting June to December.
Conservation status. Near Threatened (NT). Begonia longiciliata has a relatively broad distribution, particularly in the borders of China, Laos and Vietnam (Fig. 7); however, the size of most populations is small and the habitats are fragmented. Its distribution range is extremely narrow in both Guangxi and Guizhou provinces of China. Several populations exist with less than 20 or even 10 individuals. In these two provinces, the population size continues to decrease, with very little seedling recruitment, due to habitat deterioration and disturbance from agricultural activities. This species also needs an environment that has a high level of humidity to survive well. Additionally, because of its beautiful foliage, wild plants are at risk of overharvesting, therefore, it should be considered Vulnerable (B2ab(iv)) in China.

Remarks.
Begonia longiciliata has been treated as a synonym of B. rex for a long time in China (Ku 1999;Gu et al. 2007). Several horticultural cultivars have been produced by crossing it with other Begonia taxa at Kunming Botanical Garden of China (Tian et al. 2001(Tian et al. , 2002. However, B. rex has not been collected or observed in the wild in China. It was recorded in several locations from Arunachal Pradesh (Camfield and Hughes 2018) (called southern Tibet by China), a currently China-India disputed region. In addition, B. longiciliata was previously cultivated under the code U3888 (with long hairs on adaxial leaf surface, Fig. 6A) by the American Begonia Society and these cultivated plants were correctly identified as B. longiciliata by Golding (Golding 2004), but were later treated by other researchers as B. rex (Ku 1999;Gu et al. 2007) or B. sizemoreae (Tebbitt 2005). Begonia longiciliata is officially established, based on our extensive field surveys, literature review, specimen examination and the observation of plants in cultivation. According to their morphological similarity and adjacent distribution, B. longiciliata and B. rex are similar to each other and they may have differentiated possibly due to geographic isolation. Further investigation is needed on their relationship and whether it is more reasonable to treat B. longiciliata as a subspecies or variety of B. rex. -Begonia muliensis T.T. Yu, Bull. Fan. Mem. Inst. Biol., 1:119, 1948(Yu 1948 Note. Begonia taliensis is relatively widely distributed in many counties from Yunnan Province to Sichuan Province in China (Fig. 9). It exhibits considerable variation in size of plant, leaf and inflorescence, shape of lobes, leaf colour and blade variegation patterns (Fig. 8). However, its net-like pattern of red lines on the fruits is a stable character (Fig. 10F, left corner). There is no distinction in distribution and morphology between it and B. muliensis (isotype, Fig. 10D) (HU). In addition, when B. taliensis was described and published, the author (Gagnepain 1919) cited three collections of specimens: Ducloux 5184 (B), Delavay 220 (P), and Henry 8946 (P) (Fig. 10). Unfortunately, he did not assign a type specimen. Of these, Ducloux 5184 and Delavay 220 were collected from Dali in Yunnan Province and both are significantly different only in plant size. However, Henry 8946 was collected from somewhere (possibly near Kangding County) in Sichuan Province. Dali and Kangding are at least 600 km apart. In fact, Henry 8946 is a specimen of B. imitans Irmsch. (1939: 51) (Fig. 10C) (lobed over 2/3). The relationship between B. taliensis and B. imitans remains unknown and further study is undergoing. Based on our literature review, field survey and type specimens, Delavay 220 is designated here as the lectotype of B. taliensis and Dulcoux 5184 as its syntype. The syntype Henry 8946 belongs to another species and should not be considered for future nomenclatural decisions.
Conservation status. Begonia taliensis has a relatively-wide distribution (recorded or observed in nearly 20 counties of two provinces in China, Fig. 8), but the size of most populations is usually small. In addition, many of its distribution sites are near roadsides; therefore, the habitats could be easily disturbed by human activities. Additionally, this species is used as an ornamental due to its beautiful foliage and flowers or as a vegetable by local residents (Yang et al. 2018). Continuous human collection for different purposes may cause a decrease in population size and individual numbers. Therefore, its conservation status should be currently considered Near Threatened (NT).
Remarks. 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.

Hybrid-origin taxa
Natural hybridisation is very common in Begonia and 50 populations of 31 natural hybrids involving 29 species have been recorded in Chinese wild begonias (Tian et al. 2017). Based on morphological and molecular analysis (Tian et al. 2017), two previously published species are considered to be of hybrid origin: B. lancangensis S.H.Huang (Shui and Huang 1999: 13) and B. malipoensis S.H. Huang & Y.M.Shui (Huang and Shui 1994). Therefore, these two species are formally recognised here as hybrids.
Begonia × langcangensis S.H.Huang Fig. 11A Note. 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 (Craib 1912: 347) (Fig. 11C, D), B. handelii Irmsch. (Irmscher 1921) (Fig. 11E, F) (Fig. 11A, B). Therefore, we confirmed that B. langcangensis is a natural hybrid. It is very similar to the hybrid (unpublished) in the same section of B. acetosella × B. silletensis subsp. mengyanensis Tebbitt & K.Y.Guan (Tebbitt and Guan 2002), which has hairy stems and petioles and larger leaves (Tian et al. 2017). Distribution and phenology. 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 (Ding et al. 2020). Flowering March to May, fruiting April to July.
Conservation status. 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 (Ding et al. 2020).
Remarks. Like B. acetosella, B. handelii and B. silletensis C.B.Clarke (Clarke 1879), dioecious Begonia × lancangensis has berry-like fruits and was previously classified in section Sphenanthera, but has recently been integrated into section Platycentrum (Moonlight et al. 2018). In the wild, B. acetosella, B. handelii and B. silletensis often have overlapping distributions, meaning natural cross fertilisation is possible due to their overlapping flowering periods. The hybrid plants are usually very few and, therefore, rarely observed, due to a low chance of a natural cross. Natural crossings may generate new hybrids in the future. Note. Begonia malipoensis was described for the first time in 1994 and its type locality is Douchidian of Malipo Xian, Yunnan Province (Huang and Shui 1994). In the wild, it grows closely with B. hemsleyana Hook.f. (Curtis et al. 1899) (Fig. 12F) and B. versicolor Irmsch (Irmscher 1939) (Fig. 12E, F). Later, Daike Tian (Tian 1999) conducted field surveys on the diversity of B. versicolor in southeastern Yunnan and found a few plants of B. malipoensis in the same locality and at Daweishan National Nature Reserve of Pingbian County, Yunnan Province. Based on the very limited number of individuals and intermediate morphology between B. hemsleyana and B. versicolor, B. malipoensis is considered a natural hybrid and this supposition was confirmed by artificial cross experiments (Tian 1999). From natural hybrids, one type, with densely white-spotted leaves, was selected as a new cultivar, B. × malipoensis 'White Snow' (Tian et al. 2001). The hybrid status of B. ×malipoensis was further supported by molecular evidence (Tian et al. 2018).  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 (Tian et al. 2017), more wild hybrids occurred with B. hemsleyana as a mother plant in Malipo county, while more with B. versicolor as mother plant were observed in a hybrid zone in Pingbian county.
Distribution and phenology. B. × malipoensis has only been seen in Malipo and Pingbian counties in Yunnan Province. Flowering June to July, fruiting July to September.
Conservation status. 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.
Remarks. 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 (Tian 1999).