Addiction of five orchid species to the flora of Bhutan

Bhutan, nestled in the eastern part of the Himalaya Biodiversity Hotspot, harbours a rich flora and fauna. Due to its multiple biogeographic origins, diverse topography, ecological complexity, and a wide range of climatic and soil conditions, it supports a diverse range of floristic complexes (Gyeltshen et al. 2023). However, the Bhutanese flora remains undercollected, and many species have yet to be discovered. Numerous plants found in neighbouring regions are not yet recorded in Bhutan, highlighting a significant gap in our knowledge of the country’s diverse flora (Gyeltshen et al. 2023). Recent advancements in plant systematics call for further investigation into Bhutan’s flora.

The checklist of Orchids of Bhutan initially included 369 species, incorporating records from the neighbouring states of Darjeeling and Sikkim in India (Pearce & Cribb 2002). Subsequently, Gurung (2006) published “An Illustrated Guide to the Orchids of Bhutan”, listing 419 species. Recent publications, such as “A Century of New Orchid Records in Bhutan” by Dalstrom et al. (2017, 2021), have increased the count to 462 species, excluding five uncertain locations and two cases of mistaken identity. There has also been a notable increase in the number of orchid species due to recent discoveries of species new to science and new records for Bhutan. For instance, eight new species (C.Gyeltshen et al. 2019, N.Gyeltshen et al. 2017, 2020, P.Gyeltshen et al. 2020, 2023, Ghalley et al. 2022) and 26 new records (Chaida & Tashi 2020, Dechen et al. 2020, Dorji et al. 2023, P.Gyeltshen et al. 2021, Rabgay & Kumar 2019, Rabgay et al. 2021, Tobgay et al. 2024, Zangpo et al. 2021) have increased Bhutan’s orchid species count to 493. With the addition of five more species from the current study, the total now stands at 498 orchid species in Bhutan.

This paper results from floristic assessments conducted in Bhutan between June 2022 and March 2024. While identifying the material, we consulted literature on the regional orchid flora (Averyanov 2011, Chen & Liu 2003, Chen et al. 2009, Clayton 2017, Dorji 2008, Gurung 2006, Hooker 1894, King & Pantling 1898, Lucksom 2007, Maekawa 1936, Pearce & Cribb 2002, Seidenfaden 1986, Shankar 2021, Tetsana et al. 2019, Vermeulen et al. 2014), and we found five orchid species not previously reported from Bhutan. The abbreviation of the author’s citation followed the International Plant Names Index (IPNI 2024), and the circumscription and terminology adopted for the morphological descriptions followed Pearce & Cribb (2002) and Beentje (2024).

Measurements of the vegetative and reproductive parts were taken in situ from at least 5 to 10 randomly chosen flowers of the species. Geographical details such as elevation and geo-coordinates were collected using a Garmin GPS (eTrex 40), and photographs were taken using a digital camera. Micro images were photographed using a Z-stacking microscope at the National Biodiversity Centre in Thimphu, Bhutan. The coloured plates were prepared and edited using Adobe Photoshop software. Distribution data were plotted on a map using QGIS software version 3.16.2 (QGIS Development Team, 2022), and the collected specimens were deposited at the Bhutan National Herbarium (THIM). Descriptions, distribution maps, habitat characteristics of all five species, and colour photographs are provided to aid in accurate species identification and practical conservation efforts.

Bulbophyllum crabro (C.S.P.Parish & Rchb.f.) J.J.Verm., Schuit. & de Vogel, Phytotaxa 166: 106. 2014. Monomeria crabro C.S.P.Parish & Rchb.f., Trans. Linn. Soc. London 30(1): 143 (1874). Lectotype, (designated by Clayton 2017): Fig. 1.

Monomeria barbata Lindl., Gen. Sp. Orch. 61. 1830.

Epicranthes barbata Rchb.f., Ann. Bot. Syst. (Walpers) 6(2): 265. 1861. Lectotype, (designated by Shankar, 2021): Nepal. Toka, 1821, Wallich 1978 (K [K000974273 digital image!]: Isolectotype, K [K000974243, K001114839 digital images!]; G [G00434759 digital image!]).

Plant epiphytic or lithophytic, up to 45 cm long. Rhizome creeping, stout, woody, 5-7 mm in diam., sympodial, rooting from both current pseudobulbs and rhizomes. Pseudobulbs spaced on rhizome by 4-10 cm, ovoid, lemon green, c. 3-5 cm in height, 2.0-3.5 cm in diam., green, shiny when new, moderately shrivelled after flowering, getting flaccid with age. Leaf single at apex; petiole, 6-8 cm long; lamina oblong, 16-24 × 3.2-4.0 cm, leathery, glabrous, apex emarginate (mostly symmetrical), base attenuated into petiole. Inflorescence racemose, 30-35 cm long, up to 10-flowered, arising laterally from base of pseudobulbs, stout, ascending, dark purple; peduncle, 9-15 cm long, with 2-3 sheaths, 8-10 × 5.5-6.0 mm; floral bracts lanceolate, 4.5-5.0 × 2.0-2.5 mm, glabrous, persistent; pedicel and ovary, 1-2 cm long, ovary grooved, flushed with dark purple colour. Flower laxly arranged on inflorescence, 1-2 cm apart; dorsal sepal lanceolate, 10-12 × 5.4-5.0 mm, cucullate, adaxially surface brownish colour, abaxial surface yellowish, margin recurved, apex narrowly acute or acuminate, incurved or recurved, 7-veined; lateral sepals connate at base, oblong, 15-20 × 6.8-7.5 mm, pineapple-yellow, tinged with brown dots, veined, adaxially densely hispid, abaxially glabrous, margins recurved, apex acute or acuminate, yellow without tinge, base oblique; petals oblanceolate, 6-10 × 5-7 mm, adnate to base of column and extended other half adnation to posterior side of foot, margin fimbriate, yellowish with maroon spots or flushed with dark purple. labellum panduriform, ca. 8 × 5 mm, 3-lobed, deflexed about middle; lateral lobes narrowly falcate (horn-like), ca. 3 mm long, yellowish or dark purple; mid-lobe oblong when flattened, ca. 5 × 4 mm, glaucous, adaxial surface 4-keeled, base of outer keels merged with lateral lobes and apex with mid lobe, base of inner keels visible at base of labellum, apex converge and connate on mid lobe forming warty structure, flushed with maroon or dark purple, abaxial surface with prominent midrib impression, yellowish-white with pink spots, apex retuse. Column rectangular, ca. 5 × 4 mm, dilated at the base, obtuse, wings yellow spotted with maroon; column foot rectangular, ca. 9 × 4 mm, yellow spotted with maroon; stelidia triangular, ca. 2.5 mm long, yellow. Anther cap subglobose, ca. 2 × 2 mm, abaxially papillose, yellow, apex rounded. Pollinia 4, in 2 pairs; stipe terete, ca. 0.5 mm long, reddish-orange; viscidium ovoid, ca. 0.5 mm long, yellow; pollinarium ovoid, ca. 1 mm long, golden yellow.

Phenology: Flowering from September to November.

Habitat: Bulbophyllum crabro grows on boulders and as an epiphyte on the main trunks of Lyonia ovalifolia (Wall.) Drude, Rhododendron arboreum Sm. (Ericaceae), Quercus griffithii Hook.f. & Thomson ex Miq., and Quercus lanata Sm. (Fagaceae) in warm broadleaved forests at elevations around 1500-1700 m.

Distribution: The species is distributed in India, China, Malaysia, Myanmar, Nepal, Thailand, Vietnam, and Bhutan (Punakha, Woku-Damchi) (Fig. 6). Specimen examined: Bhutan. Punakha District: Kabesa Gewog, Woku-Damchi,17 November 2023, P.Gyeltshen, D.D. Lama & K. Rabgay 121 (THIM22552!, THIM22553!, THIM22554!, THIM22555!).

Notes: According to Vermeulen (2014), Bulbophyllum crabro belongs to Bulbophyllum sect. Monomeria, which is characterized by a creeping rhizome, pseudobulbs that become longitudinally wrinkled with age, racemose inflorescences, flowers with a long column-foot to which the sepals are attached in the apical half, 1-veined, ciliate to erose-fimbriate petals, a mobile and auriculate labellum, stelidia with a winged upper margin, and pollinia attached to a stipe. Bulbophyllum crabro differs from other known Bulbophyllum species by having spotted petals that are longer than wide, twisted lateral sepals, and long triangular stelidia resembling horns on the column.

Bulbophyllum rigidumKing & Pantl., Ann. Roy. Bot. Gard. (Calcutta) 8: 169. 1898. Bulbophyllum conchiferum auct. non Rchb.f.: Hooker, Fl. Br. Ind. 1894. TYPE: India. Sikkim, W.Griffith 5291 (holotype: KDist.-image not seen). Fig. 2.

Plant epiphytic, 18-20 cm tall. Rhizome thick, covered with fibrous sheaths, 10-13 × 4-5 mm. Roots inserted along the rhizome. Pseudobulbs small, conical, attenuate. Leaf 1; petiole 3-6 cm long; lamina oblong-elliptic, 10-20 × 2.0-3.2 cm, thick, leathery, margin entire, base slightly attenuate, apex subacute. Inflorescence erect, arising from the rhizome at the base of the inconspicuous pseudobulbs, laxly 10 to 17 flowered; peduncle slender, 10-13 cm long, deflexed at distal portion while blooming; sheathed, glabrous; sheath lanceolate, 10-14 × 4-5 mm; rachis glabrous, 6-8 cm long. Flowers opening from base; floral bracts lanceolate, 5-6 × 2-3 mm, pale green, apex narrowly acuminate, glabrous; pedicel and ovary, 2-3 mm long; dorsal sepal lanceolate, 5-6 × 4-5 mm, cucullate, broadly acuminate, glabrous, 3-veined; lateral sepals oblong, 5.5-7.0 × 2.5-3.0 mm, lower margin connate towards the base, 3-veined, base oblique, apex obtuse; petals oblong-lanceolate, 3-4 × 1.0-1.5 mm, margin obscurely denticulate, apex broadly acuminate, 1-veined, 1-lateral short vein. Labellum simple, ovate-elliptic, 3.5-4.0 × 2.5-3.0 mm, deflexed in the middle, glabrous, base grooved, apex obtuse. Column stout, 1.0-1.3 mm long, pale yellowish-green; stelidia 2, unevenly bilobed; column foot, rectangular, ca. 2 × 2 mm, adaxially maroon, abaxially pale yellowish-green; anther cap bilobulate 1.0 × 1.4 mm long, depressed. Pollinia 2, ovoid, 0.5 mm long. Seed capsules unknown.

Phenology: Flowering from September to November.

Habitat: Bulbophyllum rigidum is found in warm broadleaved forests at an elevation of 1640 m.

Distribution: The species is distributed in India, Nepal, and Bhutan (Punakha, Rimchu) (Fig. 6).

Specimen examined: Bhutan. Punakha District: Goenshari Gewog, Rimchu,1640 m, 20 November 2023, P. Gyeltshen, D.D. Lama & K. Rabgay 129 (THIM22564!).

Notes: Pearce & Cribb (2002) included this species in the Orchids of Bhutan based on its occurrence in the neighbouring states of India. The occurrence of the species in Bhutan was highlighted following the publication of A Century of New Orchid Records in Bhutan by Dalstrom et al. (2017, 2021), but without voucher specimens. Our field survey and specimen collection now provide a detailed description and habitat information for this species in Bhutan.

Bulbophyllum rigidum is most similar to Bulbophyllum cornu-cervi King & Pantl. but differs by having a larger habit, ≥ 18 cm tall (vs. ≤ 6.5 cm), larger leaves, 8.5-22 × 2-3.4 cm (vs. smaller leaves 2-3 × 1-2 cm), lanceolate dorsal sepal (vs. oblong), oblong petals (vs. lanceolate), and column 1.0-1.9 mm long (vs. 0.3-0.4 mm long).

Cymbidium tortisepalum var. longibracteatum (Y.S.Wu & S.C.Chen) S.C.Chen & Z.J.Liu, Acta Phytotax. Sin. 41(1): 81. 2003. Cymbidium longibracteatum Y.S.Wu & S.C.Chen, Acta Phytotax. Sin. 11(1): 31. 1966. Cymbidium goeringii var. longibracteatum (Y.S.Wu & S.C.Chen) Y.S.Wu & S.C.Chen, Acta Phytotax. Sin. 18(3): 300. 1980. TYPE: China. Sichuan: Cult. Pt., Y. L. Fee 2064 (holotype: PE, destroyed). Neotype (designated by Chen & Liu, 2003): China. W. Sichuan, Dujiangyan, Z.J. Liu 22318 (PE, not seen). Fig. 3.

Plant terrestrial, 30-85 cm tall. Pseudobulbs ovoid, 1.5-2.5 × 1.0-1.3 cm, enclosed in leaf bases, and bladeless sheaths. Roots thick, 4-8 mm in diam. Leaves 5-7, young flexuous, old stiff, lorate, 26-63 × 0.7-1.2 cm, not articulate at the base, margin serrulate, apex acuminate. Inflorescence arising from near base of pseudobulb, erect, 21-25 cm long; peduncle 12-18 cm long, with several sheaths; rachis 5-8 cm long, 2-5-flowered. Floral bracts linear-lanceolate, 28-45 × 4-7 mm, exceeding ovary. Flowers scented sepals and petals light pink, labellum creamy with orange-red spots adaxially, glabrous; pedicel and ovary 2.0-2.5 cm long. Dorsal sepal, elliptic-lanceolate, 30-35 × 7-8 mm, margin entire, apex acuminate, 7-veined. Lateral sepals oblong-lanceolate, 32-35 × 5-6 mm, apex acuminate, 7-veined. Petals lanceolate, 23-26 × 8-9 mm, sometimes slightly twisted, apex broadly acuminate or acute, 7-9 veined. Labellum not fused to basal margins of column, 3-lobed; mid-lobe broadly ovate or elliptic, 17.0-18.6 × 10-12 mm, recurved in the middle, apex obtuse; lateral lobes small, rounded, incurved; disk with 2 longitudinal callus extending from near the base of lip to the base of mid-lobe. Column sub-rectangular and incurved, 13-15 × 3-5 mm, ventrally flat, with minute purplish striations on abaxial surface, apex slightly broadened, with 2 small wings. Anther cap suborbicular, 2 × 3 mm, surface colliculate, light yellow. Pollinia 4, in 2 pairs, pollinium ovoid, 1.0-1.5 × 1 mm, attached to short and triangular viscidium with elastic caudicles.

Phenology: Flowering occurs from September to November.

Habitat: Cymbidium tortisepalum var. longibracteatum grows in association with Cymbidium lancifolium Hook. in warm broadleaved forests at an elevation of 1920 m.

Distribution: The species is distributed in China and Bhutan (Punakha, Gangtharmo). Fig. 6.

Specimen examined: Bhutan. Punakha District: Talo Gewog, Gangtharmo, 1920 m, 15 March 2024, P. Gyeltshen, K. Tobgay & K. Rabgay 255 (THIM22866!, THIM22867!).

Notes: Cymbidium tortisepalum var. longibracteatum is most similar to Cymbidium cyperifolium var. szechuanicum (Y.S.Wu & S.C.Chen) S.C.Chen & Z.J.Liu but differs in several morphological characteristics. The leaves of C. tortisepalum var. longibracteatum are not articulate towards the base, whereas those of C. cyperifolium var. szechuanicum are articulate towards the base. Additionally, the floral bracts of C. tortisepalum var. longibracteatum exceed the ovary, in contrast to usually exceeding only half the length of the ovary in C. cyperifolium var. szechuanicum. The sepals and petals of C. tortisepalum var. longibracteatum are light pink, unlike the dull greenish-yellow or grey-green sepals and petals of C. cyperifolium var. szechuanicum. It should be noted that Cymbidium faberi var. szechuanicum is considered a synonym of C. cyperifolium var. szechuanicum (Chen & Liu 2003)

Galeola cathcartii Hook.f., Fl. Brit. India [J. D. Hooker] 6(17): 89. 1890. Galeola kerrii Rolfe ex Downie, Bull. Misc. Inform. Kew 1925(10): 409. 1925. Galeola siamensis Rolfe ex Downie, Bull. Misc. Inform. Kew 1925(10): 410. 1925. TYPE: India. Sikkim, icon. Cathcart s.n. (holotype: CAL; image of type, K, not seen). Fig. 4.

Plant climbing vine, up to 6 m long. Stem fibrous, 0.9-1.5 cm in diameter, rooting at nodes with triangular stem scales, fleshy, 2-3 × 2.0-3.5 cm. Rhizome woody; scales ovate to ovate-oblong or triangular scales 2 × 1.5-2.5 cm. Inflorescence branching, with branches 16-60 cm long, laxly bearing many flowers, flowering in succession from lowest to the tip, flower buds rusty hairy. Pedicel and ovary 1.5-5.0 cm long, rusty hairy. Floral bracts fleshy, triangular, 9-12 mm long, apex acute. Flowers do not open widely, ca. 2.5 cm across, yellow, lip with orange-red veins on sidewalls inside, petals and sepals recurved, apex obtuse, adaxial surface yellow, glaucous, abaxial surface fainted with rusty hairs, petals glaucous. Floral bracts triangular, 0.5-1.5 × 0.7-2.5 cm, apex acute. Dorsal sepal oblong to oblong-elliptic, ca. 20 × 4 mm, apex obtuse. Lateral sepals, similar to dorsal sepals, larger, 2.0-2.6 cm long, 0.4-0.6 cm wide. Petals oblanceolate, ca. 23 × 4 mm, slightly undulate along the upper margin or entire apex obtuse. Labellum broadly obovate, 1.6-1.8 × 0.8-1.0 cm, strongly concave, adaxial surface hairy, abaxial surface glabrous, margin irregularly incised and undulate upper half portions, with somewhat rounded or obtuse apex and without short callus near the base. Column clavate, 8-10 mm long, nearly straight. Anther cap 2 mm wide, reddish-orange. Pollinia 2, ca. 1 mm long, grooved. Seed capsules unknown.

Phenology: Flowering occurs from June to July.

Habitat: In Bhutan, Galeola cathcartii is found in the semi-shaded area of warm broadleaved forest at elevations between 1400 and 2000 m. Associated include Ageratina adenophora (Spreng.) R.M.King & H.Rob. (Asteraceae), Acer oblongum Wall. ex DC. (Sapindaceae), Casearia glomerata Roxb. (Salicaceae), Chloranthus erectus Sweet (Chloranthaceae), Daphne sureil W.W.Sm. & Cave (Thymelaeaceae), Elatostema lineolatum Wight, Elatostema platyphyllum Wedd. (Urticaceae), Eriobotrya hookeriana Decne. (Rosaceae), Neolitsea cuipala (D.Don) Kosterm. (Lauraceae), Oplismenus compositus (L.) P.Beauv. (Poaceae), Persicaria chinensis (L.) H.Gross (Polygonaceae), Piper betleoides C.DC., Piper pedicellatum C.DC. (Piperaceae), as well as Blumea sp. (Asteraceae), Boehmeria sp. (Urticaceae), Diplazium sp. (Athyriaceae) and Pteris sp. (Pteridaceae).

Distribution: Galeola cathcartii is distributed in India, Thailand, and Bhutan (Trongsa, Wangling). Fig. 6.

Specimen examined: Bhutan. Trongsa Distrct: Langthel, Wangling, 1662 m, 20 July 2022, Phuentsho & P. Namgyal BTN682 (THIM15891!, THIM15892!, THIM15893!, THIM15894!, THIM15895!, THIM15896!, THIM15897!, THIM15898!, THIM15899!).

Notes: Galeola cathcartii is similar to Galeola nudifolia Lour. but differs in having oblong sepals (vs. lanceolate sepals) and an obovate labellum with a cuneate base (vs. suborbicular, cordate).

Liparis kumokiri F.Maek., J. Jap. Bot. 12(2): 95. 1936. Liparis auriculata var. kumokiri (F.Maek.) M.Hiroe, Orchid Flowers 2: 78 (1971). TYPE: Japan. Hondo: Hitachi Province, Mount Tsukuba, 13 July 1895, C. Owatari s.n. (holotype: TInot seen). Fig. 5.

Plant terrestrial, up to 15 cm tall. Pseudobulbs aggregated, ovoid, 2-3 × 2 cm, distally 2-leafed, enclosed several membranaceous sheaths; sheaths ovate-lanceolate, 1-3 cm long, apex shortly subacute. Leaf 2; petiole base sheathing, enclosing peduncle, winged, 3-9 cm long; lamina elliptic or ovate-elliptic, 8.5-10.0 × 4.5-5.6 cm, conduplicate, plicate, green, apex obtuse, margin undulate, glabrous. Inflorescence terminal, racemose, 5-9 flowered; peduncle slender, 15-18 cm long, green, glabrous. Floral bracts triangular, ca. 2 mm long, apex acute or narrowly acute, green. Pedicel and ovary twisted at base, 1.0-1.7 cm long, green. Flowers yellowish-green, widely open, labellum green or purple especially in middle. Dorsal sepal oblong-lanceolate, ca. 10 × 3 mm, apex subacute or obtuse, strongly revolute, yellowish-green. Lateral sepals oblong-lanceolate, ca. 10 × 3 mm, yellowish-green, slightly oblique, apex subacute, strongly revolute. Petals falcate, obscurely oblanceolate when flattened, 9-10 × 1.0-1.5 mm, greenish, apex obtuse, margin strongly revolute, pendulous. Labellum obovate, ca. 8 × 7 mm, narrowed toward base, apex roundly truncate and mucronate, inconspicuously clawed, strongly recurved from the middle, green. Column ca. 5 mm long, incurved, with obtuse wings at apex, much dilated at base, pale-green to white towards the base. Anther cap suborbicular, 1.3 × 1.6 mm, 2-celled, cells surrounded by a whitish rim, apex obtuse, not beaked, pale green. Pollinia 4 in 2 pairs, ovoid, waxy, yellow. Seed capsules clavate, 10-15 × 4-5 mm.

Phenology: Flowering occurs from June to July, and fruiting from July to September.

Habitat: Liparis kumokiri is found in shaded areas of cool broadleaved forests at an elevation of 2400 m.

Distribution: The species is distributed in Russia, Korea, Japan, and Bhutan (Punakha, Pangkarpo) (Fig. 6).

Specimen examined: Punakha District: Talo Gewog, Pangkarpo, 2400 m, 20 June 2022, P.Gyeltshen & K.Rabgay 136 (THIM22575!).

Notes: Liparis kumokiri is most similar to Liparis cathcartii Hook.f. but differs by having longer floral bracts ca. 2 mm long (vs. ca. 0.5 mm long), lateral sepals not appressed to lower surface of the labellum (vs. appressed to lower surface of the labellum), and a green labellum that is strongly recurved in the middle (vs. purple, not curved or slightly curved at the base). It is also similar to Liparis deflexa Hook.f. but differs by having an obtuse or subacute leaf apex (vs. acuminate) and small erect triangular floral bracts (vs. deflexed, lanceolate floral bracts).

The authors express their gratitude to Dr. Pankaj Kumar of Texas Tech University, Lubbock, USA, and Mr. Ba Vuong Truong of Vietnam for their valuable contributions and for sharing relevant literature. We extend our thanks to the Department of Forest and Park Services, Ministry of Energy and Natural Resources for necessary permission and support. We are also thankful to Dr. Karma D. Dorji, Program Director at the National Biodiversity Centre, and staff for their continuous support and motivation.

Author contributions. Research concept and design. P.Gyeltshen and K.Tobgay. Collection and/or assembly of data. P.Gyeltshen, K.Rabgay, Phuentsho, K.Tobgay & P.Namgyel. Data analysis and interpretation. P.Gyeltshen, K.Rabgay & K.Tobgay. Writing the article. P.Gyeltshen, K.Rabgay, Phuentsho, K.Tobgay & P.Namgyel. Critical revision of the article. P.Gyeltshen & K.Tobgay. Final approval of article. P.Gyeltshen, K.Rabgay, Phuentsho, K.Tobgay & P.Namgyel.

Funding. The study was supported by Royal Government of Bhutan (RGoB).

Conflict of interests. The authors declare that there is no conflict of interests associated with this publication.