Gardens’ Bulletin Singapore 65(2): 135–142. 2013 135 Two new species of Begonia (Begoniaceae) from Bali and Lombok Wisnu H. Ardi1, I.M. Ardhaka2, M. Hughes3, N.K.E. Undaharta2, D. Girmansyah4 and S. Hidayat1 1 Bogor Botanic Garden, Jl. Ir. H. Juanda No. 13, Bogor, Indonesia wisn001@lipi.go.id 2 Bali Botanic Garden, Candikuning, Baturiti, Tabanan 82191, Indonesia 3 Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh EH3 5LR, Scotland, U.K. 4 Herbarium Bogoriense, Indonesian Institute of Sciences, Cibinong 16911, Indonesia ABSTRACT. Two new species of Begonia, B. lugrae Ardhaka & Undaharta and B. sendangensis Ardi are described from Bali and Lombok, respectively. The species belong to Begonia section Reichenheimea. A checklist and identiication key to the Bali and Lombok species of Begonia are provided. Keywords. Bali, Begonia, Lombok, new species Introduction Begonia is one of the largest angiosperm genera, comprising approximately 1500 species which are distributed in tropical and subtropical Africa, America and Asia and Paciic Islands (Hughes 2008). The Southeast Asian species remain the most poorly known, with many novelties still being discovered recently (Girmansyah 2012; Sang et al. 2013; Phutthai et al. 2012). The irst account dedicated to the Begonia of Bali and Lombok was published by Girmansyah (2009), which reported ive new species and one new record, bringing the total number of species known from the two neighbouring islands to eight species. During ield surveys of Begonia in Gianyar, Bali in 2010 organised by the Bali Botanic Garden, and in Lombok in 2012 led by the Bogor Botanic Garden, two new species of Begonia were collected, here newly named as Begonia lugrae Ardhaka & Undaharta and Begonia sendangensis Ardi. All available specimens from ANDA, BO, E, K, L and SING have been consulted, and hence it must be assumed, at least until more intensive collecting in Bali may reveal otherwise, that the species have a very restricted range (Fig. 1). All the specimens cited are included in the Southeast Asian Begonia Database (Hughes & Pullan 2007), which is accessible online (http://elmer. rbge.org.uk/begonia/). Four of the species are classiied in Begonia sect. Sphenanthera (Hassk.) Warb., another four including the two new species are in Begonia sect. Reichenheimia 136 Gard. Bull. Singapore 65(2) 2013 Fig. 1. Distribution of Begonia lugrae (squares) and B. sendangensis (triangles). (Klotzsch) A.DC., and a single species each are in Begonia sect. Parvibegonia A.DC. and Begonia sect. Petermannia (Klotzsch) A.DC. (Table 1). The two new species exhibit typical characters of Begonia sect. Reichenheimia: rhizomatous or tuberous stems, protandrous inlorescences, and three locular ovaries with entire placentae (Doorenbos et al. 1998). Table 1. The indigenous Begonia species of Bali and Lombok. Section Species Parvibegonia Begonia tenuifolia Dryand. Petermannia Begonia lombokensis Girm. Reichenheimia Begonia coriaceae Hassk. Begonia lugrae Ardhaka & Undaharta Begonia sendangensis Ardi Begonia pseudomuricata Girm. Sphenanthera Begonia baliensis Girm. Begonia lempuyangensis Girm. Begonia longifolia Blume Begonia multibracteata Girm. 137 Bali and Lombok Begonia Key to Begonia from Bali and Lombok 1a. Plant with erect stems........................................................................................... 2 b. Plant repent or stemless ........................................................................................ 6 2a. Female inlorescences basal to male; male and female lowers with 2 tepals; fruit a dry capsule with well developed equal wings ............................. B. lombokensis b. Female and male lowers occurring together in cymose inlorescences; male lowers with 4 tepals, female 5 or 6 tepals; fruit leshy with reduced wings or one wing larger............................................................................................................ 3 3a. Fruit wings reduced to three equally short wings or ridges; lamina oblong to lanceolate; margin shallowly toothed to sub-entire; female lowers with 6 tepals…………………………………………………………………B. longifolia b. Fruit with one larger wing; lamina ovate to broadly ovate; margin scalloped; female lowers with 5 tepals ................................................................................. 4 4a. Inlorescence hairy; bracts persistent ......................................... B. multibracteata b. Inlorescence glabrous; bracts caducous .............................................................. 5 5a. Lamina ovate; stem hairy .....................................................................B. baliensis b. Lamina broadly ovate; stem glabrous ...................................... B. lempuyangensis 6a. Plants tuberous ..................................................................................................... 7 b. Plants rhizomatous ............................................................................................... 8 7a. Stem erect and weak; internodes elongated; inlorescence terminal, racemose; female lowers with 5 tepals; ovary with 2 locules; placentation bilamellate........ ............................................................................................................ B. tenuifolia b. Stemless; internodes compressed; inlorescences lateral, cymose; female lowers with 3 tepals; ovary with 3 locules; placentation entire ............... B. sendangensis 8a. Leaves peltate .......................................................................................B. coriacea b. Leaves basiixed ................................................................................................... 9 9a. Lamina 14–16.5 × 12–15 cm; margin crenate or minutely toothed to entire, peduncle shorter than petioles ................................................................. B. lugrae b. Lamina 5.5–10 × 5–9 cm; margin undulate, peduncle longer than petioles .......... ……………………………………………………………… .. B. pseudomuricata 138 Gard. Bull. Singapore 65(2) 2013 The new species Begonia lugrae Ardhaka & Undaharta sp. nov. § Reichenheimia Similar to Begonia pseudomuricata, differing from that species by the broader, asymmetric stipules with a leshy extension, subentire (not undulate) leaf margin, larger leaf lamina (14–16.5 × 12–15 cm) compared to in that species (5.5–10 × 5–9 cm), and the peduncle being shorter than the petioles. TYPE: Ni Kadek Erosi Undaharta RS 03, cultivated at Bali Botanic Garden from vegetative material collected in the wild from Melinggih village, Yeh Ayung River, Gianyar, Bali, Indonesia, 08°26′50.3″S 115°13′55.9″E, 26 Jul 2013 (holo BO; iso E, KRB, Bali Botanic Garden Herbarium). Fig. 2. Perennial, creeping, rhizomatous monoecious herb, 15–17 cm tall. Stems internodes short, 5–8 mm long, glabrous, reddish with white spots at the nodes; stipules semicircular, 6–10 × 12–15 mm, asymmetric, pale green, with an abaxially prominent hirsute reddish midrib up to c. 15 mm long, persistent. Leaves alternate; petioles 24– 33.5 cm long, glabrous, reddish at base and green towards to apex; lamina basiixed, 14–16.5 × 12–15 cm, asymmetric, ovate, base cordate, lobes overlapping, apex shortly attenuate, margin sub-entire, with minute recurved teeth at the end of the veins, adaxial surface glabrous, green, raised slightly between the veins; venation palmate, veins paler green above, primary veins 7–8. Inlorescence cymose, with 5–10 lowers, axillary, protandrous, bisexual; peduncles 19.5–27.5 cm long, pale green, glabrous; bracts sub-orbicular, red, c. 2 × 3 mm, margin slightly imbriate, deciduous. Male lowers: pedicels 5–15 mm, glabrous; tepals 4, white, outer tepals 2, c. 13 × 16 mm, sub-orbicular, base slightly cordate, margin entire, apex rounded or slightly undulate, glabrous; inner tepals 2, c. 13 × 8 mm, narrowly obovate, glabrous; androecium yellow, symmetric, globose; stamens c. 90, ilaments c. 1 mm long, fused at the base, anthers c. 3 mm long, obovate, dehiscing through lateral slits c. 1/2 as long as the anther, connective not projecting. Female lowers: pedicels 7–15 mm, glabrous, bracteoles absent; tepals 3, white, unequal, two outer tepals orbicular to sub-orbicular, 12 × 14 mm, margin entire, apex rounded or undulate , one inner tepal, narrowly obovate, 6 × 12 mm; ovary sub-globose, 8–9 × 6–7 mm (excluding wings), locules 3, placentation axile, placentae entire, wings 3, subequal, triangular, rounded at the base and cuneate at the apex, the widest point at the middle of the ovary, glabrous; stigmas 3, shallowly U-shaped, stigmatic surface once spirally twisted. Fruits not seen. Distribution. Endemic to Bali, Gianyar District, Melinggih village, Yeh Ayung River embankment. Habitat. This species grows on the shaded steep rocky cliffs in the Yeh Ayung River embankment at 630 m elevation. IUCN Conservation category. Begonia lugrae is currently only known from a single population, which is not in a formally protected area. Although locally abundant, Bali and Lombok Begonia 139 Fig. 2. Begonia lugrae from cultivated material in the Bali Botanic Garden. A. Habit. B–D. Lamina. E. Rhizomes. F–G. Stipule. H–I. Inlorescence. J. Male lowers. K. Female lower. L. Fruit, side view. M. Fruit, apical view. N. Ovary transverse section. Scale bars: J (1 cm); F, G, I, K–N (2 cm); A–D, H (10 cm). (Photos: A–I & K–N, Gede Wawan; J, Wisnu H. Ardi) with at least 75 plants in the population, this makes the species vulnerable to future disturbance, and a provisional IUCN category of VUD2 is appropriate. Notes. The species is named in honour of the Director of Bali Botanic Garden, I Nyoman Lugrayasa who generously supported many Begonia expeditions. This species is morphologically similar to Begonia pseudomuricata Girmansyah. However B. lugrae is distinct in its bigger leaves 14–16.5 × 12–15 cm (versus 5.5–10 × 5–9 cm) with sub-entire margin, whereas in B. pseudomuricata the margin is undulate. The length of the inlorescence peduncle and the shape of the stipules are further differences: the peduncles of B. lugrae (19.5–27.5 cm long) are always shorter than the petioles (24–33.5 cm long) while in B. psedomuricata the peduncles (10–25 cm 140 Gard. Bull. Singapore 65(2) 2013 long) are always longer than the petioles (5–20 cm long); in B. lugrae the stipules are very distinctive, being asymmetric and having a leshy extension at the tip. Begonia sendangensis Ardi sp.nov. § Reichenheimia B. sendangensis differs from B. pseudomuricata and B. lugrae in its considerably smaller stature and in possessing a tuber; the latter character also distinguishes it from all other Indonesian species of Begonia sect. Reichenheimia. TYPE: WI 82, cultivated at Bogor Botanic Garden from vegetative material collected in the wild from Senaru Village, Sandang Forest Reserve, Bayan Sub district, Lombok Utara District, Nusa Tenggara Barat, Indonesia, 08°18’23.3”S 116°24’47.9”E, 20 Apr 2013 (holo BO). Fig. 3. Perennial, tuberous, monoecious herb, up to 10 cm tall. Stems very reduced, internodes c. 1 mm long; stipules, ovate, c. 3 × 1.5 mm, midrib prominent, sparsely hirsute, tip projecting c. 1.5 mm, persistent. Leaves alternate; petioles, 2.7–3.5 cm long, green, with scattered multicellular glandular hairs; lamina basiixed, 3.3–9 × 2.7–6 cm, asymmetric, ovate, base cordate, lobes rarely overlapping, apex attentuate, margin shallowly lobed, sparsely villose, with minute recurved teeth at the end of the veins, adaxial surface glabrous, green, raised slightly between the veins; venation palmate, veins pale green, primary veins 5–6. Inlorescence cymose, few-lowered, axillary, protandrous, bisexual; peduncles 2.5–3.9 cm long, pale green, glabrous; bracts minute, sub-orbicular, margin slightly imbriate, deciduous. Male lowers: pedicels 14–20 mm long, tepals 4, pink, outer tepals 2, 10–12 × 12–15 mm, sub-orbicular, abaxially sparsely hairy, inner tepals 2, 11–13 × 6–9 mm, obovate to elliptic; androecium yellow, symmetric, globose, stamens c. 35, ilaments fused at base into a short column c. 1.5 mm long; anther c. 1 mm long, narrowly obovate, dehiscing through lateral slits longer than half the length of the anther, apex retuse. Female lowers: 1 or 2, pedicels 15–17 mm long, bracteoles present, subulate, c. 2 mm long, persistent; tepals 3, pink, unequal, two outer tepals broadly ovate, c. 9–10.5 × 14 mm; sparsely hairy on abaxial surface, one inner tepal elliptic, 9.5 × 5.5 mm, glabrous; ovary 5–7 × 5–5.5 mm (excluding wings), ellipsoid, glabrous, green, locules 3, placentation axile, placentae entire, wings 3, equal, pinkish, rounded at base, rounded to truncate at apex, widest point 6–8 mm long just below the apex; stigmas 3, U-shaped, stigmatic surface once spirally twisted. Fruit with pedicel c. 15–18 mm long, capsule ellipsoid, c. 8 × 6 mm, (excluding wings), dehiscent, splitting along the wing attachments, wing shape as for the ovary, wings widest subapically, c. 8.5 mm wide. Distribution. Endemic to Lombok, in the Sendang Gile Forest Reserve. Habitat. This species grows on limestone cliffs in semi-shade. IUCN Conservation category. Begonia sendangensis is probably a narrow endemic, restricted to the Sendang Gile Forest Reserve, where it does not form large colonies Bali and Lombok Begonia 141 Fig. 3. Begonia sendangensis. A–B. Habit. C. Stipule. D. Lamina. E. Inlorescence. F. Male lower. G. Female lower showing ovary, side view. H. Female lower, top view. I. Fruit. J. Ovary transverse section. Scale bars: C (1 mm); J (5 mm); E–I (1cm); A, B, D (5 cm). (Photos: A–H & J, Wisnu H. Ardi; I, Syamsul Hidayat) 142 Gard. Bull. Singapore 65(2) 2013 but appears to occur as scattered individuals on steep cliffs at the edge of the reserve. The narrow distribution and dependence on limestone means that a provisional IUCN category of VUD2 is appropriate, despite the area being protected. Notes. The epithet ‘sendangensis’ refers to Sendang Gile Forest Reserve from where the type material was collected. Begonia sendangensis is unique in Begonia section Reichenheimia in Indonesia on account of its tuberous habit. The presence of tubers in this species are probably an adaptation to its limestone habitat and the seasonally dry climate in the Lombok region. This is convergent with a number of other species which are found in the seasonally dry limestone habitats of continental Asia (southern China, Indochina, and the Thai Peninsula). Some of these are also currently in Begonia sect. Reichenheimea (e.g., Begonia harmandii Gagnep, B. hymenophylla Gagnep, B.intermixta Irmsch., B. parvula Irmsch.), but are likely to belong to the ‘Diploclinium grade’ (Rajbhandary et al. 2011) which has its centre of diversity in this area. The region also harbours most of the species in Begonia sect. Parvibegonia (e.g., Begonia integrifolia Dalzel., B. bella Putthai, B. sinuata Meisn.) which are characterised by the presence of tubers. Tuberous species are not well represented from the ever-wet areas of the Sunda shelf. ACKNOWLEDGEMENTS. The authors would like to express gratitude to Ir. I Nyoman Lugrayasa (Bali Botanic Garden Director) for supporting Begonia expeditions on Bali; and to the curators of ANDA, BO, E, K, L and SING for allowing us access to herbarium material. References Doorenbos, J., Sosef, M.S.M. & de Wilde, J.J.F.E. (1998) The sections of Begonia including descriptions, keys and species lists (Studies in Begoniaceae VI). Agric. Univ. Wageningen Pap. 98(2): 1–266. Girmansyah, D. (2009) A taxonomic study of Bali and Lombok Begonia (Begoniaceae). Reinwardtia 12(5): 419–434. Girmansyah, D. (2012) Begonia ranaiensis (Begoniaceae), a new species from Mt Ranai, Natuna Island, Indonesia. Kew Bulletin 68:1–4. Hughes, M. (2008) An Annotated Checklist of Southeast Asian Begonia. U.K.: Royal Botanic Garden, Edinburgh. Hughes, M. & Pullan, M. (2007) Southeast Asian Begonia Database. http://elmer.rbge.org.uk/ Begonia/ Sang, J., Kiew, R. & Geri, C. (2013) Revision of Begonia (Begoniaceae) from the Melinau Limestone in Gunung Mulu National Park and Gunung Buda National Park, Sarawak, Borneo, including thirteen new species. Phytotaxa 99(1): 1–34. Phutthai, T., Hughes, M. & Sridith, K. (2012) A new species of Begonia (Begoniaceae) from Peninsular Thailand. Edinburgh J. Bot. 69(2): 287–292. Rajbhandary, S., Hughes, M., Phutthai, T., Thomas, D.C. & Shrestha, K.K. (2011) Asian Begonia: out of Africa via the Himalayas? Gard. Bull. Singapore 63(1&2): 277–286.