Further discoveries in the ever-expanding genus Begonia ( Begoniaceae ) : fifteen new species from Sumatra

Fifteen new species of Begonia L. from Sumatra are described and illustrated, in Begonia sect. Bracteibegonia (B. beludruvenea M.Hughes sp. nov. and B. jackiana M.Hughes sp. nov.), B. sect. Petermannia (B. harauensis Girm. sp. nov.), B. sect. Platycentrum (B. leuserensis M.Hughes sp. nov.), B. sect. Reichenheimia (B. fluvialis M.Hughes sp. nov., B. halabanensis M.Hughes sp. nov., B. karangputihensis Girm. sp. nov., B. kemumuensis M.Hughes sp. nov., B. korthalsiana Miq. ex M.Hughes sp. nov., B. kudoensis Girm. sp. nov., B. lilliputana M.Hughes sp. nov., B. olivacea Ardi sp. nov., B. raoensis M.Hughes sp. nov., B. simolapensis Ardi sp. nov.) and B. sect. Sphenanthera (B. pseudoscottii Girm. sp. nov.). Using the International Union for the Conservation of Nature criteria, 6 are considered to be Least Concern, 5 Vulnerable and 4 Data Deficient. A key to 58 of the 63 currently accepted Begonia species in Sumatra is provided.


Introduction
Begonia L. (Linnaeus 1753) is a pan-tropical genus of often shade-loving herbs and shrubs, with a number being very popular horticulturally.The number of accepted species in Begonia currently stands at 1803 (Hughes et al. 2015) with Southeast Asia proving to be particularly rich and yielding substantial numbers of new taxa (e.g.Ardi et al. 2013;Averyanov & Nguyen 2012;Chong et al. 2015;Hughes & Takeuchi 2015;Sang et al. 2013;Sang et al. 2015).In Sumatra alone, since the first baseline count of 45 species was published (Hughes 2008) a further 25 endemic species are now known (this study; Ardi & Hughes 2010;Girmansyah 2012;Hughes et al. 2009).This paper describes fifteen new species from Sumatra,  (Warburg 1894) (B. pseudoscottii Girm. sp. nov.).These are not merely variants of previously known species complexes, but in many cases strikingly distinct growth forms not before recorded on the island, such as the rheophytic B. fluvialis and B. lilliputana, and the succulent-stemmed B. kudoensis.Following the synonymisation of some names (Hughes & Girmansyah 2011a) and the removal of some dubious records, we consider the total number of currently accepted names in Begonia for Sumatra to be 63, and a key to the majority of these and the five sections they represent is provided below.
The level of narrow endemism is very high, in particular for the limestone species, and many are known from a single collection or population.When species distributions are so limited, extinction of some of the species newly described here within our lifetime is a high possibility -we must strive not to make it an inevitability.Gunung Leuser National Park is under immense pressure from illegal logging and accelerating land use change (Kelman 2013), which has the potential to affect B. leuserensis, B. lilliputana, B. olivacea and B. simolapensis, and the type and only locality for B. karangputihensis is near a massive limestone quarry near Padang and is therefore under threat from mining expansion.
In addition to the first priority of in situ habitat preservation, specialist ex situ collections such as those held in Bali Botanic Gardens, Bogor Botanic Gardens and the Royal Botanic Garden Edinburgh have a high potential for playing an important role in the conservation of narrowly endemic Begonia species.

Materials and methods
The descriptions and other data in this study are derived from herbarium material (both loans and material collected by the authors) and field observations by the authors during a series of expeditions to Sumatra from 2007 to 2011.All Begonia material from Sumatra in ANDA, B, BM, BO, E, FI, K, L, P, SING has been consulted, along with representative loans from A and MICH, 1431 sheets in total.Stable links (Hyam et al. 2012) to images of specimens held in E are included as hyperlinks in this document.Images of most other specimens cited are available from Hughes et al. (2015).All available type material and protologues of Begonia species from Sumatra and surrounding regions has been examined in order to confirm the novelty of the species described.Measurements are derived from dried specimens and hence will deviate slightly from those in the field.Colour and shape descriptions were recorded from digital photographs taken during expeditions and from material in cultivation in the Centre for Plant Conservation, Bogor, Cibodas Botanic Garden and the Royal Botanic Garden Edinburgh, where available.

Diagnosis
The velvety red hairs on the stem and veins are distinctive.B. beludruvenea is nearest to B. verecunda M.Hughes (Hughes et al. 2009) from Gunung Leuser National Park in terms of its habit and leaf shape, but the hairs are denser and fleshier, the male flowers are slightly larger (10-14 mm diameter, not c. 9 mm) and have 2 (not 4) tepals, and the styles are longer in the female flowers (c. 5 mm, not 3-4 mm).
B. verecunda has not been recorded from limestone, whereas B. beludruvenea is a limestone endemic.

Distribution and habitat
Endemic to the Bukit Sebelah limestone in West Sumatra (Fig. 2), where it grows on steep, shaded clay soil banks over the limestone base rock.

Conservation status
The bulk of the distribution lies within the Bukit Sebelah and Batang Pangean protection forest which is likely to represent its full natural range.Although there is low level disturbance around the forest tracks, the reserve is reasonably intact and populations of B. beludruvenea can colonise previously disturbed bare soil banks.Although naturally rare, following IUCN (2012) we consider the species as Least Concern as long as the reserve is well managed.1.5-5.5 cm, not c. 12 × 12 cm).Other distinctive characters are the petioles being triangular in cross section, and the cuneate lamina with up to 3 apical lobes.See also the diagnosis for B. lilliputana below for a comparison with that species.

Distribution and habitat
Only known from two collections from neighbouring streams near Sungai Pinang in West Sumatra (Fig. 4).B. fluvialis grows on moss covered rocks at the side of and emerging from streams running down the mountainside.

Conservation status
The forest habitat of the type locality seems to be well managed and under some community protection.
However the lack of a formally gazetted protected area and the potential for landslides to encroach the streamside habitat means B. fluvialis should be considered Vulnerable under criterion VUD2 of IUCN (2012).

Diagnosis
The peltate and succulent leaves are also found in B. kudoensis, however B. halabanensis has a thickly hairy rhizome and petioles (not glabrous), male flowers with 2 tepals (not 4), larger inflorescences (with c. 80 flowers, not c.40) and fruit with a truncate (not obtuse) apex.The key from couplet 6 onwards deals with all 5 currently described peltate species from Sumatra.

Etymology
The epithet refers to the distribution of the species in Halaban in West Sumatra near Payakumbuh.

Description
Erect acaulescent herb 20-30 cm tall; stem rhizomatous, stout, internodes c. 1 cm long, densely covered in a matted indumentum of reddish brown multi-branched thick hairs c. 1 cm long.Stipules lanceolate, stout, 2-3 × 1.5 cm, fibrous, persistent, with thick, long hairs.Leaves: petiole c. 20 cm long, cross section unknown, with quite dense 5 mm long hairs; lamina peltate, point of petiole attachment placed to within 3 cm of the margin, suborbicular, 10-15 × 10-15 cm, thick and succulent, base rounded, margin entire in outline, with evenly spaced 2 mm long stiff rounded teeth that are recurved underneath, margin also with a fringe of 5 mm long hairs, apex acute, underside with many pale dots of stomatal clusters, venation palmate, main veins 8, quite widely spaced over most of the lamina.Inflorescences axillary, c. 40 cm long and exceeding the leaves, cymose, many-flowered, branching c. 8 times, bisexual, protandrous; bracts elliptic, minute, glabrous, entire, c. 2 × 1.5 mm towards the terminal branches, basal pair not seen.

Distribution and habitat
Found on limestone, endemic to the type locality in Halaban, West Sumatra (Fig. 2).The thick fleshy leaves and densely hairy rhizome of this very distinctive species imply adaptation to dryer habitats.Known only from the type.

Conservation status
The distribution of limestone habitat in the Halaban area is not very well known, and the exact location of the type collection is not clear.Whether the species is already extinct, or in fact thriving in a naturally small population needs further fieldwork in the Halaban region; we assess B. halabanensis to be Data Deficient (IUCN 2012).

Diagnosis
The inflorescence and habit of B. harauensis most closely resembles that of B. laruei M.Hughes (Hughes et al. 2009) from North Sumatra and Aceh, but it is a smaller species (c.50 cm tall, not to c. 100 cm tall) with narrower leaves (2-5.5 cm wide, not 3.5-10 cm wide) without lobes, which are so asymmetric as to almost displace the point of petiole attachment to the side of the leaf.The shrinkage that occurs upon drying accentuates this, giving the leaves a tear-drop shape.

Etymology
The epithet refers to the distribution of the species, Lembah Harau in West Sumatra near Payakumbuh.

Distribution and habitat
Endemic to Lembah Harau and immediate surroundings (Fig. 2), where it grows on stream banks and at the base of sandstone cliffs.

Conservation status
Begonia harauensis is assessed as Least Concern due to its distribution overlapping the Lembah Harau Protection Forest, and the large number of specimens in ANDA giving an indication of a quite common, if locally endemic, plant.

Diagnosis
Begonia jackiana is unique amongst Sumatran members of sect.Bracteibegonia in its small leaf size (2.5-5.5 × 1.2-2.5 cm) and bristles on the upper leaf surface.Its shares a dentate-denticulate hairy leaf margin with B. bracteata Jack, which differs in being densely softly pilose above.

Etymology
The epithet commemorates the Scottish botanist William Jack , as this species was found whilst following in Jack's footsteps in Bengkulu Province (Hughes & Girmansyah 2011a).

Distribution and habitat
Only known from the forests in Kapahiang Regency in Bengkulu (Fig. 4).Found growing in small colonies by the roadside, near a damp ditch in the shade of other herbs.

Conservation status
The fact that this species has some ability to cope with secondary habitats may make it less likely to become threatened.However it is only known from one locality, and hence is best considered as Vulnerable under VUD2 (IUCN 2012) as the only known locality is not in a gazetted protected area.

Diagnosis
Begonia karangputihensis differs from the peltate B. goegoensis which is also native to West Sumatra in being a smaller plant, with smaller (up to 7 cm wide, not c.9-15 cm wide), less rugose leaves, terete petioles (not triangular) and flowers with flat membranous tepals (not cup-shaped and fleshy).

Distribution and habitat
Endemic to the Bukit Karang Putih limestone near Padang in West Sumatra (Fig. 2), where it grows on cliffs and in shallow caves.

Conservation status
We assess B. karangputihensis to be Vulnerable under criteria VUD2 (IUCN 2012), as the type locality is only 1 kilometre away from an industrial limestone mine and just outside the edge of Kerinci Seblat National Park.

Etymology
The epithet is derived from the locality where this species was discovered, near the village of Kemumu.

Distribution and habitat
Known only from the type locality along a forest trail near the old concrete dam by Kemumu waterfall in Bengkulu Province (Fig. 4).

Conservation status
Known from a single location which is currently a well-managed recreation forest.The single location means the species is prone to the risk of extinction through chance events, so we consider the IUCN category of Vulnerable to apply using criterion VUD2 (IUCN 2012).dehiscing through slits running nearly the entire length of the anther, the slits positioned on the outer face of the anther.Female flowers: pedicel 11 mm long; ovary glabrous, 6 × 10 mm including wings; capsule elliptic, 5 × 3 mm, 3 locular, placentae entire; wings 3, subequal, rounded triangular; tepals 2, orbicular, 6 × 5 mm, margin entire; styles 3, stigmatic surface once spirally twisted, caducous.Fruit recurved on a 2-2.5 cm pedicel; wings subequal, rounded-triangular, 12 × 18 mm in total; capsule elliptic, 9 × 6 mm, glabrous; apex obtuse.

Distribution and habitat
Frustratingly Korthals did not give a precise locality for his collection, which is the only other collection of this species apart from the type.Although he did visit Kayu Tanam ("Kajoetanam") on April 25 th 1834, where Beccari made his collection of this species, Korthals also visited many other locations in Sumatra.The species is likely endemic to Kayu Tanam in West Sumatra near Padang (Fig. 4).

Conservation status
As 140 years have passed since the last collection of this species, it seems reasonable to assume it is a very local and scarce endemic of low-altitude forest.As Kayu Tanam is now a mix of suburban and agricultural areas on the main road between Padang city and Padangpanjang, it is possible that B. korthalsiana is extinct.However there are still expanses of forest that need exploring between Kayu Tanam and Lake Singkarak before this is declared; until then we assess B. korthalsiana to be Data Deficient (IUCN 2012).

Etymology
The epithet is derived from the name of the type locality, Gunung Batu Kudo in West Sumatra.

Distribution and habitat
Known only from the type locality at Batu Kudo in West Sumatra (Fig. 4), where it grows on bare vertical limestone cliffs at an altitude of 250-400 m.

Conservation status
The vegetation at the base of the cliffs is disturbed and is being encroached by coffee plantations.The succulent leaves and stems mean the species is adapted to dryer conditions and seems to cope in the current conditions, although further disturbance to tree cover near to the cliffs should be discouraged.
In  (Tebbitt & Dickson 2000) in being a lower growing plant (c.30 cm tall, not c.60-80 cm) with lobed leaves (not entire) having dense red hairs on the leaf veins (not white sparsely puberulent), and differs from B. areolata Miq.(Miquel 1855) in having leaves which are smooth above (not densely bullate).Begonia leuserensis differs from both in having 6 (not 5) tepals in the female flowers.

Etymology
The epithet is derived from the type locality of Gunung Leuser National Park, to where the species is endemic.

Description
Repent caulescent herb on earth banks, c. 30 cm tall.Stem with dense red short fleshy hairs, becoming nearly glabrous with age, rhizomatous at base with short internodes < 1 cm long, becoming longer (to c. 25 cm long) on flowering stems.Stipules persistent, with fine hairs, denser at the base, lanceolate, 2 × 1 cm, apex long acuminate.Leaves: petiole 4-25 cm long, terete, the longer petioles being borne on the rhizomatous part of the stem, densely red hairy; lamina asymmetric, broadly ovate, lobed, divided up to ½ the way to the midrib, 8-18 × 5-14 cm, basifixed, base cordate, sinus 1-5 cm deep, upper surface glossy, nearly glabrous except for a few short fleshy hairs, under surface with dense red short hairs on the veins; margin denticulate, sparsely hairy.Inflorescences terminal, subtended by a pair of leaves, cymose, with c. 10 flowers, protandrous, bisexual; primary peduncle 8-12 cm long, red hairy; bracts: lanceolate, basal pair fused, tipped with a fringe of several points, 1-3 cm long, hairy at the base externally, bracts in the rest of the inflorescence much smaller.Male flowers: pedicel 15 mm long, hairy; tepals 4, outer 2 tepals ovate, 20 × 15 mm, white, red hairy externally, entire, inner 2 tepals elliptic,

Distribution and habitat
Endemic to Gunung Leuser National Park (Fig. 2), found on steep slopes on the forest floor at 400-800 m altitude, where it grows in leaf litter around rotting logs and at the base of trees.

Conservation status
Currently the montane forests in Gunung Leuser National Park are not under pressure, and the two known locations for the species are in the centre of the reserve.It seems likely that the species may be found on other nearby peaks at similar altitudes.We consider an IUCN category of Least Concern to be appropriate.

Etymology
The name is derived from the adjective lilliputian (English) meaning very small, derived from the name of the fictional island nation of Lilliput.

Distribution and habitat
Currently known only from the type locality near the Soraya Research Station (Fig. 4) in Gunung Leuser National Park, where it grows as a rheophyte tightly attached to rocks at the base of waterfalls, in the shade of overhanging trees.

Conservation status
Begonia lilliputana is assessed as Data Deficient (IUCN 2012) as its full range within the Gunung Leuser National Park is unknown; the Soraya Research Station is on the southernmost edge of the core reserve.

Diagnosis
The nearest species morphologically to Begonia olivacea is B. nurii Irmsch.(Irmscher 1929) from Kelantan in Peninsular Malaysia, the former differing in being a slightly smaller plant (leaves 2.7-4.5 × 2.6-3.7 cm, not c. 4 × 4-6 cm), having 3 (not 2) tepals in the female flowers, sparsely hairy petioles (not red-woolly), and duller green leaves (Kiew 2005).Also similar is B. droopiae Ardi (Ardi & Hughes 2010) from limestone in West Sumatra, which has more asymmetric leaves with darker variegation, and which is smoothly bullate between the veins (not mostly flat).See under B. simolapensis for a comparison with that species.

Etymology
The epithet reflects the dull greenish brown olive colour of the leaves.

Distribution and habitat
North Sumatra and Aceh, Gunung Leuser National Park (Fig. 4).This species grows in meagre, dusty soil on limestone rock at 250-600 m altitude.

Conservation status
The limestone habitat of the Gunung Leuser National Park in the Simolap area where this species occurs is relatively intact.As long as this remains the case, B. olivacea can be considered as belonging to the IUCN category of Least Concern.

Etymology
The epithet refers to the village Rao nearby the type locality.

Distribution and habitat
Only known from the type collection from a steep soil bank with some surface water and overhanging roadside scrubby vegetation in West Sumatra near Rao village (Fig. 2).

Diagnosis
Begonia simolapensis grows sympatrically on limestone with B. olivacea described above and has a similar habit (growing flat against the substrate) and leaf shape; it differs in having larger (5-9.5 × 4-8 cm, not 2.7-4.5 × 2.6-3.7 cm), glossier leaves which are a nearly uniform deep green (not olive green with paler variegation) and longer, denser hairs on the petioles.

Etymology
The epithet refers to the type locality of Simolap.

Fig. 2 .
Fig. 2. Map of Sumatra showing the full known species distributions based on collection localities.Each point may represent more than one collection.

Fig. 8 .
Fig. 8. Begonia karangputihensis Girm.sp.nov. A. Habit.B. Male flower.C. Plant with young leaves showing transition from basifixed to peltate.D. Mature fruit on a recurved pedicel.E. Ovary.F. Female flower.A,C, D taken at the type locality of Bukit Karang Putih; the floral insets B, E, F were photographed from plants in cultivation at the Royal Botanic Garden Edinburgh, accession 20111545.Scale bars on insets: B, D-F = 1 cm; C = 10 cm.

Fig. 9 .
Fig. 9. Begonia kemumuensis M.Hughes sp.nov. A. Habit.B. Fruit.C. Male flower.D. Stipules.E. Young inflorescence.A-C, E from the type locality of Kemumu waterfall; D from a plant in cultivation at the Royal Botanic Garden Edinburgh (accession 20101656, derived from the type DEDEN1506).Scale bars on insets = 1 cm.

Fig. 11 .
Fig. 11.Begonia kudoensis Girm.sp.nov. A. Habit (Gunung Batu Kudo, type collection Puglisi et al.CP67).B. Male flower, from cultivated plant in Bali Botanic Garden derived from CP67. C. Leaf lamina edge showing recurved teeth.D. Whole plants showing different colour forms.E. Female flower from cultivated plant in Bali Botanic Garden derived from CP67.F. Fruit on a pendulous pedicel (type collection Puglisi et al.CP67).C & D taken at the type locality.Scale bars on insets: B, C, E, F = 1 cm; D = 5 cm.

Fig. 12 .
Fig. 12. Begonia leuserensis M.Hughes sp.nov. A. Habit.B. Male flower back view.C. Male flower.D. Female flower.E. Lobed leaf.A-D from Air Panas of the type collection Wilkie et al.PW791; E from PW778.Scale bars on insets: B-D = 1 cm; E = 10 cm.

Fig. 14 .
Fig. 14.Begonia olivacea Ardi sp.nov. A. Habit, showing petiole elongation in older leaves.B. Green colour form.C. Female flower bud and ovary.D. Plant with male flower.E. Male flowers.A, B, D photographed at the type locality of Simolap; C, E taken from a plant in cultivation at Bogor Botanic Garden (accession B2013070037, derived from material collected at the type locality).Scale bars on insets: B, D = 5 cm; C, E = 1 cm.