Rare orchid species in Malaysia: New records, recollections and amended descriptions.

Paphiopedilum exul, Calanthe chrysoglossoides, and Luisia brachystachys are reported here as new records for Malaysia, whereas Bryobium cordiferum subsp. borneense, Habenaria rostellifera, and Taeniophyllum rugulosum are three rare orchid species recollected from Sarawak, Perlis, and Perak, respectively. This paper highlights brief descriptions and photographic illustrations of each species for easy identification. Besides, notes on morphological comparisons with the closely related species and artificial taxonomic keys are included as well.

Introduction

Southeast Asia including Peninsular Malaysia and Borneo spans about 3% (4.5 million km2) of earth’s total land area that harbours approximately 20–25% of earth’s higher plant species [1, 2]. Substantial anthropogenic habitat alterations, forest fires, and the overexploitation of wildlife in the said vast region are detrimental to its biodiversity [3]. Malaysian vegetation comprises evergreen, montane, mixed deciduous, heath and alpine, limestone, and ultramafic forests supporting a wealth of plant diversity [4]. Worth mentioning is the northernmost corner of Peninsular Malaysia, including Perlis and Kedah, bordered by Thailand in the north constitutes a significant component of the Thai and Burmese flora [5-7]. The forests lie mainly on hilly terrain of limestone, which is part of the Setul and Chuping limestone formation with unique geological formation and high level of flora endemism [8, 9]. However, these forests are declining rapidly because of forest clearance for quarries, timber extraction and other forms of agricultural and infrastructure developments [7, 10–12]. Thus, uncountable number of the plant species may have gone extinct.

Orchidaceae is the most abundant flowering plant family in Malaysia. Approximately, 978 species recorded in Peninsular Malaysia [13-19] and 3,000 species have been recorded in Sabah and Sarawak [13]. Major collective records of Malaysian orchid species were monographed by many botanists, including R. E. Holttum [20], H. N. Ridley [21], J. J. Smith [22], J. J. Vermeulen [23], I. M. Turner [24], G. Seidenfaden, and J. J. Wood [25]. In the past two decades, several studies on the orchid diversity covering various elevation gradients and vegetation types in Malaysia involved local conservationist. Of these, the most significant studies on Malaysian orchids include [12, 14, 26–28]—limestone forest; [13]—peat swamp forest; [29, 30]—hill forest; [31]—lowland forest; [32-36]—montane forest; [37]—coastal heath forest; [38, 39]—logged forest.

Judging by these past and recent works on orchid flora in Malaysia, it is apparent that Malaysia possesses one of the world’s richest orchid floras in one of the largest remaining areas of tropical rainforest in the Old World. Undoubtedly, there are more species still awaiting discovery in the remaining extensive forests of Peninsular Malaysia and Borneo. We are reporting new orchid species to the flora of Malaysia and recollection of additional two rare species aimed at elucidating the diversity of orchids in Malaysia. The rare taxa were found and identified whilst working on the diversity and conservation of wild orchids in the undisturbed and disturbed forests of Malaysia. This paper provides brief description, taxonomic notes, relevant notes on ecology and distribution, morphological comparisons with the closely related species, artificial taxonomic keys, and photographs to facilitate easy identification of these species in the field.

Materials and methods

Specimen collections were carried with permission from the Forest Department Peninsular Malaysia and Forest Department Sarawak [Access License Ref.—JH/100 Jld. 23 (246); Invitation Letter Ref.—(20)JHS/IAD/600-7/101/Jld.1]. Living specimens were transplanted into an ex-situ conservatory, and then further nurtured into identifiable samples. The complete specimens were processed using standard herbarium preparation technique of [40]. Our locality data are withheld to protect the populations from illegal collections. Prior to the morphological examination, methylated spirit-preserved and fresh flower specimens were dissected, described and photographed under AM4113ZT Dino-Lite Digital Microscope. Alpha taxonomy with reference to the type specimens, monographs and protologues was employed in the identification process, evaluation of the species’ distribution status, and a comparative morphology study with the closely similar species. Digitised images of herbarium collections, botanical drawing and records deposited in National Herbarium of the Netherlands (NHN) accessed through Browse Dutch Natural History Collections: BioPortal (Naturalis) (http://bioportal.naturalis.nl/), Herbarium of Singapore Botanic Gardens (SING) accessed through BRAHMS Online managed by University of Oxford (http://herbaria.plants.ox.ac.uk/bol/sing), Swiss Orchid Foundation (https://orchid.unibas.ch/index.php/en/), Kew Herbarium Catalogue (http://apps.kew.org/herbcat/gotoSearchPage.do), Natural History Museum Specimen Collection (https://data.nhm.ac.uk/), Herbarium of Aarhus University (AAU) (https://www.aubot.dk/search_form.php), Museum National D’Histoire Naturelle (MNHN) (https://science.mnhn.fr/all/search), and Plants of the World Online (POWO) (http://www.plantsoftheworldonline.org/) were examined prior to the taxonomic treatment and assessment on range of distribution for each species. The range of distribution from historical and current localities was plotted in Google Earth maps. The accepted names were validated via KEW World Checklist of Selected Plant Families (WCSP) [41].

Results and discussions

New records for Malaysia

(Ridl.) Rolfe, Orchid Rev. 4: 364 (1896); Fig 1.

Fig 1

Paphiopedilum exul.

A. Single flower. B. Plant. C, D, E. Flower from front, lateral and back view. F. Flower front view showing spotted dorsal sepal and hairy staminode. G. Dorsal sepal. H. Dorsal sepal from dorsal and back view. I. Petals. J. Inflorescence. K. Pedicel-with-ovary. L. Labellum from top view. M. Labellum from lateral view. N. Gymnostemium from lateral view showing anthers. O. Staminode. P. Staminode showing base connate to the gymnostemium. Q. Staminode showing mucronulate apex. R. Anthers. S. Pollinarium. Note: G-S are preserved specimens.

Homotypic synonyms:––Cypripedium insigne var. exul Ridl., Gard. Chron., ser. 3, 10: 94 (1891); Cypripedium exul (Ridl.) Rolfe, J. Hort. Cottage Gard., ser. 3, 22: 301 (1892); Cordula exul (Ridl.) Rolfe, Orchid Rev. 20: 2 (1912). Type: THAILAND. Central Thailand, Bangkok, 1891, Ridley SING0056352 (SING-photo!).

Heterotypic synonyms:––Cypripedium exul var. aureum Rolfe, Orchid Rev. 4: 162 (1896); Paphiopedilum exul var. aureum (Rolfe) Pfitzer in H.G.A.Engler (ed.), Pflanzenr., IV, 50(12): 75 (1903); Paphiopedilum exul f. aureum (Rolfe) O.Gruss & Roellke, Orchidee (Hamburg) 51: 420 (2002).

Specimen examined:––MALAYSIA. Perlis, ca. 100 m elev., 31 October 2019, Besi et al. EDW113 (UPM!).

Description

Plants mostly terrestrial, less often lithophytic, caespitose, ca. 20 cm tall including inflorescence. Stem ca. 1 cm, short. Leaves 7–10 per shoot, 6–21 × 1.7–2 cm, plain green, green to yellowish green, pale green below, venations faint, strap-shaped to oblong elliptic, apex acute with minute cleft, suberect, rigid, fleshy, canaliculated, conduplicate basally, grooved, glabrous, veins prominent below, margin entire. Inflorescence single flowered, ca. 15 cm long, slender, erect, pubescent, green covered with dense dark purple indumentum, pedicel-with-ovary completely covered by a large greenish white bract. Floral bract folded, lanceolate, apex acuminate, hairy basally, grooved, veins sunken, greenish white, more than half the pedicel-with-ovary length, 4.9 × 1.4 cm. Pedicel-with-ovary ca. 2.4 cm long, curved, pubescent, indumentum white, clavate, ridged, reddish green. Flower 4.5 × 3.5 cm, dorsal surface of sepals and petals pubescent with short white and dense indumentum, greenish white in general, sepals suffused green, petals greenish brown with clear dark brown veins arching towards apex, pouch showy and glossy reddish-purple pouch hooded by dorsal sepal. Dorsal sepal 3.4 × 2.7 cm, cucullate, broadly ovate; apex cuspidate, folded, recurved, ca. 5.5 mm long; base rounded; ventral side white suffused yellowish brown, glossy dark brown spots; spots suffused over lower half from basal to the central area, arranged in lines, contrast with the yellow background; dorsal side suffused green, blotched dark brown at base, sparsely hairy; prominent, raised median outer keel covered by dark brown hairs; margin white, entire, covered by dense white indumentum. Synsepalum 3.5 × 2.1 cm, cucullate, ovate, apex obtuse, base cordate, yellowish green, venation green, bordered white, margin covered by dense white indumentum, back side outwardly keeled, suffused green, blotched dark brown at base as in dorsal sepal. Petals 3.4 × 1 cm, more than twice as long as wide, outspread, almost horizontally, oblanceolate, apex obtuse, margins undulate and minutely hairy, proximally black hairs occur on surface at the base, greenish brown at both sides, suffused green towards apex and margins, prominent reddish brown at inner side, minutely spotted at base, recurved forward around the pouch. Pouch or labellum 2.8 × 1.4 cm, slipper-shaped, side lobes rectangular, incurved, glossy, reddish green, pale green at mouth, venation brown, hairy interior at the nectary and dorsal opening. Staminode 8 × 8 mm, obovate, yellowish green, verruculose, hairy, indumentum dark brown, indumentum much longer near the base of the gymnostemium, apex mucronulate, central teeth rounded, base connate to the gymnostemium, anthers and stigma hidden behind staminode, margin slightly recurved; fovea 2 × 0.9 mm, narrowly ovate, yellow, bears a shiny bright yellow knob-like wart at base (umbo); anthers 2, positioned on either one side, 2.5 × 1.4 mm; stigma ca. 4.7 mm, widely ovate. Pollinia 2, 2 × 1.3 mm; gymnostemium ca. 5 mm.

Distribution

It was an endemic species to limestone cliffs on the east side of the Phuket-Krabi Gulf of Peninsular Thailand [41, 42]. In Peninsular Malaysia, the specimen of the first record reported in this paper was collected from Perlis (Fig 2). The exact locality is withheld in this paper to protect the population from illegal collections. P. exul were also reported seen in Kedah, however, we have no authentic specimens to substantiate this claim.

Fig 2

Distribution of Paphiopedilum exul.

Etymology

In Greek, Paphos means birthplace of the mythological goddess Aphrodite; and pedilon means slipper, referring to the slipper-shaped labellum [43]. The species epithet, exul was derived from an English word ‘exile’ by Ridley means ‘banished one’ because of the geographical isolation from the closely allied one, P. insigne (Wall. ex Lindl.) Pfitzer [43]. Hence, the common name, Excluded Paphiopedilum.

Habitat and ecology

It grows on the cliff in a limestone hill forest, dried but shaded (Fig 3).

Fig 3

P. exul growing on the cliff of a limestone forest.

Photos by Muhamad Faizal Md Azmi.

Taxonomic notes

The newly recorded P. exul belongs to subg. Paphiopedilum sect. Paphiopedilum. Subg. Paphiopedilum sect. Paphiopedilum characterised by having single flowered (or at most 2-flowered), linear or spathulate petals that are more than twice as long as broad, pouch side lobes incurved, and strap-shaped and plain green leaves [44]. Paphiopedilum exul has been described by several authors under different names due to the wide variation in pouch, staminode and dorsal sepal morphologies. This species closely resembles P. insigne, but has smaller flowers and belongs in its alliance [45]. The former species differs by having sepals shorter (3.2–3.8 cm vs 5–6.4 cm) [46], staminode apex apiculate instead of emarginated and roundly bilobed, and anthers hidden behind the staminode [47]. In [47], P. exul differs by having the leaves surface yellowish rather than glaucous as in P. insigne. However, this character is rather unreliable as leaf colouration changes depending on the habitat and ecological conditions. Plants found in Perlis has slight variations in dorsal sepal and petals and staminode morphologies if compared to the one found in Peninsular Thailand (see Table 1). The base connate to the gymnostemium rather than bilobed and free as illustrated in [47], and the sepals are shorter [46]. Also, the peculiarity seen at the flower size (Table 1). Minor variation in staminode shape, flower size, and leaf pattern across localities are common in Paphiopedilum [44, 48, 49]. Paphioepdilum exul is having no near allies among the Peninsular Malaysian species. It is easily distinguishable if compared to the other single-flowered with long and spotted petals Paphiopedilum, such as P. barbatum (Lindl.) Pfitzer, P. bullenianum (Rchb.f.) Pfitzer, and P. callosum var. sublaeve (Rchb.f.) P.J.Cribb.

Table 1

Comparison of morphological characters of P. exul from Perlis and P. exul from Thailand.

Characters	P. exul from Perlis (Besi et al. EDW113)	P. exul from Thailand (Besi et al. EDW114)	P. exul from Thailand [46]
Flowers sizes	ca. 3.5 cm across	ca. 5 cm across	ca. 6.5 cm across
Pedicel-with-ovary	pubescent, reddish green, ca. 2.4 cm long	pubescent, reddish green, ca. 4 cm long	pubescent, yellow-green, 2.2–4 cm long
Dorsal sepal shape	broadly ovate, apex cuspidate	broadly ovate, apex cuspidate	ovate-elliptic, apex obtuse
Dorsal sepal size	3.4 × 2.7 cm	3.8 × 2.7 cm	3–4.8 × 2.5–3 cm
Petals shapes	oblanceolate, apex obtuse, margins undulate	oblanceolate, apex obtuse, margins undulate	oblanceolate to narrowly oblong, apex obtuse, margins undulate
Petals sizes	3.4 × 1 cm	4.1 × 1.5 cm	4.3–5 × 1.4–1.7 cm
Synsepalum shape	ovate, apex obtuse	ovate, apex obtuse	oblong-elliptic, apex obtuse
Synsepalum size	3.5 × 2.1 cm	3.8 × 2.3 cm	3.4–4.7 × 1.6–2.5 cm
Pouch colour	glossy, reddish green with brown veins	glossy, reddish green with brown veins	glossy, yellowish-beige with darker veins
Pouch size	2.8 × 1.4 cm	3.5 × 1.5 cm	3–3.5 × 1.9 cm
Staminode shape	obovate, apex mucronulate with the central teeth rounded, base connate to the gymnostemium	obovate, apex mucronulate with the central teeth rounded, base connate to the gymnostemium	obovate, apex obtuse to rarely retuse, base bilobulate rounded and free
Staminode size	8 × 8 mm	8 × 7 mm	6–8 × 7–9 mm

Artificial key to Paphiopedilum subg. Paphiopedilum from Peninsular Malaysia, with usually single flowers (or at most 2 flowers) per plant

Species reference

Cypripedium insigne var. exul Ridl. [50]; Cypripedium exul var. aureum Rolfe [46], Paphiopedilum exul var. aureum (Rolfe) Pfitzer [47].

Additional specimens examined

THAILAND. Peninsular Thailand, Kasoom, Phangnga, Nov 1897, Curtis SING0141768 (SING-photo!); 1892, Ridley SING0141766 (SING-photo!); 19 November 1901, Communic. ex. Herb. Hort. Bot. Bog., L.1527086 (NHN-photo!); 19 November 1901, Communic. ex. Herb. Hort. Bot. Bog., L.1527085 (NHN-photo!); 12 December 1918, Mhd Haniff SING0141767 (SING-photo!); Central Thailand, Bangkok, 2 April 1925, Kerr K000595625 (K-photo!); 2 August 2020, cultivated Besi et al. EDW114 (UPM!).

J.J.Sm., Bull. Dép. Agric. Indes Néerl. 43: 24 (1910); Fig 4.

Fig 4

Calanthe chrysoglossoides.

A. Inflorescence. B. Plant in the natural habitat. C. Dorsal view of the flower. D. Labellum with a central orange mark. E. Plant (dried specimen). F. Dorsal sepal. G. Lateral sepal. H. Petal. I. Lateral view of the labellum and Gymnostemium showing canaliculated claw. J. Labellum (flattened). K. Close-up of the labellum side lobes. L. Pubescent claw. M. Gymnostemium including foot. N. Anther-cap. O. Pollinia. Note: F-O are preserved specimens.

Type: INDONESIA. Java, Gunung Salabintana (Selabintana), Jackson 1506, 1165 (syntype BO-photos!).

Specimen examined:––MALAYSIA. Selangor, Batang Kali, ca. 1000 m elev., 12 October 2020, Besi et al. EDW122 (UPM!).

Plants terrestrial, ca. 20 tall without inflorescence. Pseudobulbs clustered, single-leaved. Leaves ovate to wide elliptic, apex acuminate, ca. 20 × 8 cm, abruptly narrowed to a ca. 10–15 cm long and sulcate petiole, plicate, very shortly pubescent beneath. Inflorescence ca. 30–40 cm long, arised from pseudobulbs which just forming, emerging together with the leaf; rachis ca. 13 cm long, 10- to 15- flowered placed laxly; floral bracts narrowly triangular, very acute, 5 mm long, greenish yellow, persistent. Flowers 2.2 × 1.5 cm, opening widely, white, the sepals flushed purple or pink on the outside, prominent median nerve, labellum pale pink with a central orange mark, glabrous inside, finely pubescent outside, spur short at ca. 3 mm long. Dorsal sepal 1.2 × 0.5 cm, oblong-ovate, apex acuminate. Lateral sepals 1.2 × 0.4 cm, obliquely elliptic, apex acuminate. Petals 1 × 0.3 cm, oblong-ovate, apex acuminate, base cuneate, finely pubescent outside. Labellum 1.1 × 0.7 cm, flabellate from a short claw, 3-lobed, side lobes very small and rounded, 1 mm long; midlobe 6 × 7 mm, spade-shaped, almost circular, disk slightly concave, minutely apiculate, base cuneate, a deep median ridge running from the base to apex, a 5 mm long linear and verrucose callus at base; claw short, 6 mm long, canaliculated, wall raised and rounded, sparsely pubescent. Gymnostemium 4 mm long including foot, stout, clavate, pubescent below the stigma and on the margins; apex 2.5 × 2 mm; anther-cap 2 × 2 mm, rounded, cucullate; pollinia 2 × 1 mm, triangular, outer surface slightly sulcate.

It was an endemic species to Indonesia, reported from Java, Sumatra, Lesser Sunda Islands, until our recent discovery of a population from Selangor, Malaysia (Fig 5).

Fig 5

Distribution of Calanthe chrysoglossoides.

The genus name, Calanthe is from the Greek kalos, means beautiful, and anthos, means flower, in reference to the showy flowers of the type species, whereas the species epithet chrysoglossoides is derived from Greek chrysous, golden, and glossa, tongue, alluding to the colour of the labellum in the type species [43].

Growing in a shaded lower montane forest at elevation ca. 1,000 m. An undisturbed forest area but connected to a highly developed area for hotel and shopping complexes.

Calanthe chrysoglossoides is similar to C. monophylla Ridl. and C. taenioides J.J. Sm. that occur in montane forests and belongs to sect. Monophylla. The two species were the only representative of the single-leaved Calanthe found in Peninsular Malaysia. In comparison, the species are having a creeping rhizome and only one full-sized leaf to a pseudobulb, except C. chrysoglossoides has larger flowers with broader sepals and petals, and ovate or almost circular labellum midlobe instead of narrow or bilobed at apex.

Artificial key to Calanthe sect. Monophylla from Peninsular Malaysia

Calanthe monophylla Ridl. [51] and Calanthe taenioides J.J.Sm. [51, 52].

INDONESIA. Sumatra, Toba, Residency of Tapianoeli, Vicinity of Loemban Loboe, 27 July 1936, Rahmat Si Boeea L.1495195 (NHN-photo!); Sumatra, Toba, Residency of Tapianoeli, Headwaters of Aek Mandosi, 29 September 1936, Rahmat Si Boeea L.1495233 (NHN-photo!); Sumatra, Asahan, 3–15 October 1936, Rahmat Si Boeea L.1495231, L.1495232, L.1495234 (NHN-photo!); Sumatra, east coast, Aek Boeloe Bolon, 7 November 1936, Rahmat Si Boeea L.1495238 (NHN-photo!); Sumatra, North Sumatra, Gunung Leuser Nature Reserves, Aceh, 22 June 1979, Wilde et al. L.1495198 (NHN-photo!); Lesser Sunda Islands, Lombok, 19 June 1909, Elbert L.1495201 (NHN-photo!).

(Lindl.) Blume, Rumphia 4: 50 (1849); Fig 6.

Fig 6

Luisia brachystachys.

A, B. Flowers from top and lateral views. C. Flower’s front view. D. Inflorescence. E. Plant. F. Flower’s lateral view. G. Flower’s dorsal view. H. Dorsal sepal. I. Lateral sepal. J. Petal. K. Labellum and Gymnostemium. L. Labellum’s abaxial view. M. Labellum’s adaxial view. N. Gymnostemium’s front view. O. Gymnostemium’s lateral view, P. Anther-cap, Q. Pollinia.

Homotypic Names:––Mesoclastes brachystachys Lindl., Gen. Sp. Orchid. Pl.: 44 (1830). Type: BANGLADESH. Wallich K000891542 (syntype K-photo!).

Heterotypic Synonyms:––Luisia indivisa King & Pantl., Ann. Roy. Bot. Gard. (Calcutta) 8: 201 (1898); Luisia siamensis Rolfe ex Downie, Bull. Misc. Inform. Kew 1925: 384 (1925). Type: THAILAND. Me Sue, near Chiengmai (Chiangmai), 7 April 1912, Kerr K000891534 (unknown type K-photo!).

Specimen examined:––MALAYSIA. Kedah, Bukit Pedu, ca. 500 m elev., 12 August 2020, Besi et al. HS113 (UPM!).

Plants epiphytic. Stems suberect or curved, branching, lower part brownish grey or glaucous, upper part, greenish, terete, 10–30 cm, stout, ca. 4 mm in diam., internodes 1–2 cm. Leaves 5–13 cm × 2–3 mm, green, sometimes glaucous, terete, apex obtuse, straight to slightly recurved at apex. Inflorescences 3 to 5 per stem, 2 cm long, 2- to 4-flowered; rachis 1 cm; peduncle 8 mm long, wrinkled, swollen; floral bracts ovate-triangular, ca. 1 mm, fleshy. Pedicel-with-ovary 6 mm long, sulcate, greenish brown. Flowers opening widely, 7 × 5 mm, sepals and petals yellowish green, abaxial midvein purplish brown, labellum pale yellow with purplish tint at epichilium, Gymnostemium green, purple margined, anther cap yellow spotted with purple; pedicel and ovary pale yellow, tinged with purplish brown, ca. 6 mm. Dorsal sepal 4 × 2 mm, ovate, apex obtuse. Lateral sepals 5 × 2.5 mm, ovate-oblong, slightly hooded, dorsally slightly carinate, keeled abaxially, keel becoming winged at apex, apex obtuse. Petals 5 × 1 mm, linear-oblong, apex obtuse. Labellum 5 × 3 mm, glabrous, fleshy, hypochilium concave, deep indentation between epichilium and hypochilium, more or less rectangular, ca. 2.8 × 2.8 mm, indistinct lateral lobes at base; epichilium ca. 2 × 3 mm, suborbicular or heart-shaped, 2 × 3 mm, apex obtuse; hypochilium thick, grooved at the middle. Gymnostemium 3 mm long, 2 mm wide at apex, stout; stigma large, orbicular; anther-cap 1 × 2 mm; pollinia 0.5 × 0.5 mm, orbicular.

Distributed in Bangladesh, India, Thailand, Myanmar, Vietnam, Laos, Indonesia, and Malaysia. In Malaysia, the plant was collected from Kedah in the northern part of Peninsular Malaysia (Fig 7).

Fig 7

Distribution of Luisia brachystachys.

The genus name commemorates the Spanish explorer Don Luis de Torres (–1493) who was an interpreter for Christopher Columbus on his first voyage to the Caribbean [53]. The species epithet, brachystachys is from the Greek, brachys means short, whereas stachys means an ear of corn [43]; alluding to the short flower spike of this species.

Grow on tree trunks at tops of a conglomerate hill forest with elevation of 600 m.

Taxonomy notes

Luisia brachystacys resembles L. zollingeri Rchb.f. in W.G.Walpers in plant size and having semi-orbicular to heart-shaped epichilium, but differ in having hypochilium separated from the epichilium by a rather indistinct shallow ridge, indistinct and not incurved lateral lobes at base, epichilium lacking of two lateral cushions and upcurved, and narrower oblong (not ovate) petals. On the basis of these morphological variations, the two species can be easily recognized as distinct species if compared to the other Luisia species found in Peninsular Malaysia, for examples, L. antennifera Blume, L. curtisii Seidenf., L. jonesii J.J.Sm. Moreover, hypochilium with 5 to 15 nerves and thickly cushioned epichilium are diagnostic characters for L. zollingeri [54]. Also, the plant that we discovered is very similar to specimens of De Silva K000873795 (K-photo!) and Lobb K000873796 (K-photo!), especially on the morphology of the flowers based on the illustrations on the herbarium sheets.

Artificial key to Luisia from Peninsular Malaysia with small flowers ca. 5 mm wide and petals shorter or same length as sepals

Luisia zollingeri Rchb.f. in W.G.Walpers [53].

THAILAND. Me Sue, near Chiengmai (Chiang Mai), 07 April 1912, 457 m elev., Kerr K000891534 (K-photo!); INDIA. Sikkim, Dooars, Mount Anduson, March 1897, 457 m elev., s. coll. K000891541 (K-photo!); Assam, 01 April 1899–30 April 1899, Prain’s Collector L.1521919 (NHN-photo!); Unknown locality, 1994, De Silva K000873795 (K-photo!); Lobb K000873796 (K-photo!); BANGLADESH. Wallich K000891542 (K-photo!); MYANMAR. Tanintharyi, Dawei, May 1897, Batten BM000538804 (NHM-photo!); VIETNAM. Anam, Nha Trang, 22 March 1960, Sigaldi P00324094 (MNHN-photo!); LAOS. Brikhane, Wiengchan (Vientiane), 27 March 1932, Kerr P00324095 (MNHN-photo!).

Recollections and amended descriptions

Rchb.f., Otia Bot. Hamburg.: 34 (1878); Fig 8.

Fig 8

Habenaria rostellifera.

A. Inflorescence. B, C, D. Flower from lateral and front view. E. Plant. F. Flowers from back view showing spur. G. Spur. H. Floral bract. I. Pedicel-with-ovary and floral bracts. J. Dorsal sepal. K. Lateral sepals. L. Petals. M. Gymnostemium from lateral view showing anther canals. N. Trilobed labellum. O. Gymnostemium from top view showing protruding rostellum. Note: F-O are preserved specimens.

Homotypic synonym:––Pecteilis rostellifera (Rchb.f.) M.A.Clem. & D.L.Jones, Austral. Orchid Rev. 83(6): 53 (2018). Type: THAILAND. Peninsular Thailand, Trang, 30 May 1919, Mhd Haniff SING0047370 (holotype SING-photo!).

Heterotypic synonyms:––Habenaria hancockii Rolfe, Bull. Misc. Inform. Kew 1896: 202 (1896); Habenaria roseata Ridl., J. Straits Branch Roy. Asiat. Soc. 49: 42 (1908). Type: THAILAND. Peninsular Thailand, Trang, Cultivated in the Penang Gardens, 29 June 1906, s.coll. SING0180012 (SING-photo!).

Specimen examined:––MALAYSIA. Perlis, ca. 100 m elev., 2 August 2020, Besi et al. EDW108 (UPM!).

Terrestrial. Plants up to 20 cm tall. Stems ca. 20 cm tall, erect, terete, glabrous, with 2–3 leaves and 1–2 bract-like leaflets. Cataphylls up to 2 cm long, tubular, erect, clasping on the stem, with a protruding ovate apex up to 5 mm long, pale greenish with a distinct pale white margins. Leaves 12–15 × 1–1.4 cm, spreading, widely spaced, narrowly oblanceolate-oblong, apex acute, often apiculate, adaxial green, abaxial glaucous, pale greenish margins, 3-veined. Bract-like leaves 7, up to 2.5 cm long, erect, lanceolate, apex acuminate, basal sheathing, margins minutely denticulate to coarsely, shortly glandular-hairy, green to pale green at apex. Inflorescences lax, 7-flowered, often flowered terminally; rachis 3 cm long. Floral bracts 4–5, lanceolate, acuminate, 8 × 1.5 mm, shorter than the pedicel-with-ovary, margins shortly hairy. Pedicel-with-ovary 1.4 cm long, cylindric-fusiform with a long beak ca. 1.5 mm long. Flowers 1.4 × 0.6 cm, pale salmon-pink, lateral sepals with large brown blotch in the middle, fragrant. Dorsal sepal 4.7 × 2.6 mm, suborbicular, apex cuspidate, margin entire, shortly hairy. Lateral sepals 6 × 5 mm, obliquely ovate to rounded, apex obtuse, reflexed, 3 prominent sunken veins, margins minutely denticulate. Petals 4 × 1.5 mm, oblong, apex cuspidate, margin denticulate, shortly hairy, forming a hood with the dorsal sepal. Labellum ca. 11 mm long, deeply 3-lobed above a short united part; midlobe linear to oblong, apex rounded, canaliculated, 11 × 1 mm; side-lobes divaricate, linear to oblong, apex attenuate, 7 × 0.5 mm; spur cylindric, nearly as long as the ovary to slightly longer, geniculate, thickened and slightly folded apically, ca. 1.7 cm long. Gymnostemium 5.1 mm long; foot ca. 3 mm long; anther hooded by dorsal sepal, canals ca. 5 mm long, geniculate at the middle, narrower towards lobed apex; stigmas ca. 2 mm long, freely projecting, rather short; rostellum 3-lobed with arms ca. 1.7 mm long and a middle 3-lobed tongue protruding, postulate, ca. 1.5 mm long; stelidia oblong, apex rounded, geniculate, ca. 1.7 mm long; wings oblong, grooved, ca. 2 mm long. Pollinia not seen.

Cambodia, China South-Central, Laos, Malaya, Thailand, Vietnam [41]. In Peninsular Malaysia, it was found in Perlis (Fig 9).

Fig 9

Distribution of Habenaria rostellifera.

In Latin, Habena means reins referring to the long, strap-like divisions of the petals and labellum [43]; rostellifera derived from rostellum, a beak, referring to the beak-like and protruding rostellum [55].

Found in open places in deciduous forest.

The H. rostellifera complexes including H. rostrata Wall. ex Lindl. and H. erostrata Tang & F.T. Wang has a labellum with three equal and spreading linear lobes and a transversal structure in front of the spur entrance [55]. Another easily visible diagnostic character is the labellum with its three spreading linear and about equally long lobes and the fairly long anther canals which are geniculate bent upwards. The long and filiform 3-lobed labellum differentiate H. rostellifera from any other Habenaria species found in Peninsular Malaysia, H. acuifera Wall. ex Lindl., H. carnea Weathers, H. dentata (Sw.) Schltr., H. kingii Hook.f., H. medioflexa Turrill, H. paradiseoides J.J.Sm, H. reflexa Blume, H. rhodocheila Hance, H. rumphii (Brongn.) Lindl., and H. singapurensis Ridl.. Both H. rostellifera and the following species, H. rostrata, have ovaries with a prominent beak which can also be clearly seen in the fruiting stage [55]. The tongue in front of the rostellum was regarded as an outgrowth of the labellum as shown by [56]. Reichenbach regarded this protruding structure as part of the rostellum, which the epithet name rostellifera was coined after this prominent character [55, 57].

Artificial key to Habenaria from Peninsular Malaysia, has leaves linear and acute, and a labellum with three linear lobes

Habenaria rostellifera Rchb.f. [57]; Habenaria roseata Ridl. [58]; Habenaria hancockii Rolfe [59].

MALAYSIA. Peninsular Malaysia, Terengganu, Rantau Abang, 1903, Down SING0139971 (SING-photo!); THAILAND. Siam. Tung Song, 19 July 1929, Rabil L.1516480 (NHN-photo!); Northeast Thailand, Loie, Sitan, 16 August 1948, Royal Forest Department P00370734 (MNHN-photo!); Chanburi, Makham, 3 June 1965, Phengklai L.1516481 (NHN-photo!); Surat, North of Chumphon, 11 August 1966, 50 m elev., Larsen, Smitinand, Warncke L.1516479 (NHN-photo!); Unknown locality, 17 August 1984, Godefroy-Lebeuf K000364319 (K-photo!); Songkla, Haad Yai, Klong Hoy Kong, 21 November 1984, Maxwell AMES01946805 (AMES-photo!); Chiang Mai, Wieng Haeng, Ban Jong village area, 18 September 1989, 975 m elev., Maxwell L.1516483 (NHN-photo!); Chiang Mai, Muang, Gukao Falls area, 4 October 1989, 525 m elev., Maxwell L.1516482 (NHN-photo!); Trang, 29 June 1906, Haniff 4300 (SING-photo!); VIETNAM. Rüng Bbon Phu, August 1967, Dournes P00439735 (MNHN-photo!); CAMBODIA. Godefroy 14432 (RENZ-photo!); CHINA. Mengtze (Mengzi), Yunnan, June 1983, 1676–1829 m elev., Hancock K000827011 (K-photo!); Yunnan, Kunming, 17 August 1984, Bartholomew & Boufford AMES00140709 (AMES-photo!); Yunnan, Yangpi, Rock AMES00140671 (AMES-photo!); Yunnan, Mengzi, Henry AMES00140669 (AMES-photo!); June 1983, Godefroy-Lebeuf K000364319 (K-photo!).

(J.J.Wood) Schuit., Y.P.Ng & H.A.Pedersen, Bot. J. Linn. Soc. 186: 193 (2018); Fig 10.

Fig 10

Bryobium cordiferum subsp. borneense.

A. Plant. B, C, D. Inflorescence from lateral and front view. E, F. Flowers showing whitish ovate labellum. G. Floral bract. H. Flower from lateral view. I. Petal. J. Dorsal sepal. K. Lateral sepals. L. Labellum from lateral view. M. Labellum from top view showing midlobe. N. Labellum from top view showing two lateral keels. O. Labellum from top view showing basal part. P. Flattened labellum. Q. Gymnostemium. R. Pollinia.

Homotypic synonym:––Eria cordifera subsp. borneensis J.J.Wood, Kew Bull. 39: 84 (1984). Type: MALAYSIA. Sarawak, Gunung Mulu National Park, Rib Anderson Camp, 14 march 1978, Nielsen 652 (holotype AAU-Photo!).

Specimen examined:––MALAYSIA. Sarawak, Kapit, ca. 50 m elev., 2 December 2019, Besi et al. EDW068 (UPM!).

Plants epiphytic, up to 20 cm high. Rhizome very short. Pseudobulbs caespitose, cylindrical, 2-leaved, 2–3 cm long, covered in pale brown, ovate-lanceolate, apex acute to acuminate, membranous sheaths. Leaves blades 13–20 × 1.1–1.8 cm, green above, light green below, erect, linear-lanceolate, apex attenuate and unequally bilobulate, conduplicate towards base. Inflorescence 6- to 8-flowered, lax, much shorter than leaves; peduncle and rachis pubescent, covered by short white indumentum; peduncle 1.8 cm long, with sterile bract; rachis 3.5 cm long. Floral bracts ovate, subacute, minutely puberulus, 3.2 × 1.8 mm. Pedicel-with-ovary sessile, terete, densely pubescent, 3.5 mm long. Flowers 8 × 8 mm, pubescent dorsally, reddish, veins darker, petals and lateral sepals reflexed. Mentum 3 mm long. Dorsal sepal oblong, obtuse, concave, 5.3 × 2 mm. Lateral sepals obliquely ovate, falcate, obtuse, cucullate, 5-veined, 4.4 × 3.5 mm. Petals linear-oblong, obtuse, falcate, glabrous, 4.6 × 1.2 mm. Labellum 3-lobed, strongly recurved, glabrous, 2.6 × 2.8 mm, 4.5 × 3.5 mm when flattened; side lobes erect, widely rounded, ca. 0.9 mm long; midlobe triangular-ovate, acute, fleshy, with widely ovate callus, ca. 1.2 mm long; disc with a median keel, 2 parallel and oblong fleshy lamellae extending from near the base to the base of midlobe, ca. 1.5 mm long; base cuneate. Gymnostemium 4.5 × 1.5 mm, clavate, apex 1.5 mm long, foot 3 mm long, dorsal lobe tooth-like, base lobate, stigma 1 × 0.6 mm, anther cucullate, ovate; pollinia 8, ovate, 0.6 × 0.5 mm.

The first specimen was collected from the 4th Division, Gunung Mulu National Park by Nielsen in 1978 [60]. Since then, there was no further record on its recollection, until now. Our specimen was collected from Kapit, Sarawak (Fig 11).

Fig 11

Distribution of Bryobium cordiferum subsp. borneense.

In Greek, bryon means moss and bios as in the English ‘bios’ means life [43]. The species epithet cordiferum (latin) means cordate, heart-shaped, with the notch at the base, referring to the heart-shaped labellum [61].

Mixed forest on sandy soil with scattered limestone rock [60], and along the riverine forest with alluvial vegetation (Fig 12).

Fig 12

The plants growing as epiphyte on a tree in a riverine forest in Kapit, Sarawak.

According to J. J. Wood in his paper [60], Bryobium cordiferum subsp. borneense differs from B. cordiferum subsp. cordiferum from Papua New Guinea in having shorter pseudobulbs and leaves, much smaller floral bracts and less hairy flowers [60]. Though our specimen has leaves much wider than Wood’s specimen of B. cordiferum subsp. borneense from Gunung Mulu National Park and Schlechter’s specimen of B. cordiferum subsp. cordiferum (Table 2). But, presumably, both Wood’s and Schlechter’s descriptions were based on dried specimens, hence, the reduced sizes of the specimens. Also, our specimen showing the vegetative structure is very much similar to the subsp. cordiferum rather than the subsp. borneense (Table 2). However, the bracts and flowers showing affinity to the subsp. borneense, especially on the tepals sizes and widely ovate callus on the midlobe (Table 2). Bryobium cordiferum differs from the other two species of Bryobium species found in Peninsular Malaysia, B. hyacinthoides (Blume) Y.P.Ng & P.J.Cribb and B. pudicum (Ridl.) Y.P.Ng & P.J.Cribb, by having pseudobulbs small and inconspicuous, completely covered by rather thick and triangular sheaths.

Table 2

Comparison of morphological characters of B. cordiferum subsp. borneense found in Kapit, B. cordiferum subsp. borneense found in Gunung Mulu National Park, and B. cordiferum subsp. cordiferum found in Papua New Guinea.

Characters	B. cordiferum subsp. borneense found in Kapit	B. cordiferum subsp. borneense found in Gunung Mulu National Park [55]	B. cordiferum subsp. cordiferum found in Papua New Guinea [57]
Pseudobulbs size	2–3 cm long	0.8–1.4 cm long	2.5–5 cm long
Leaves shape	linear-lanceolate, apex attenuate	linear-lanceolate, apex acute to attenuate	linear, apex acute
Leaves sizes	13–20 × 1.1–1.8 cm	10–14 × 0.5–0.7 cm	17–25 × 0.5–0.8 cm
Floral bracts shape	ovate, apex subacute	ovate, apex subacute	elliptic, apex obtuse
Floral bracts sizes	3.2 mm long	2.5 mm long
Dorsal sepal shape	oblong, apex obtuse	oblong, apex obtuse	oblong, apex obtuse
Dorsal sepal size	5.3 mm long	5 mm long	6.5 mm long
Lateral sepals size	4.4 mm long	5 mm long	2.8 mm long
Petals shapes	linear-oblong, apex obtuse	linear-oblong, apex obtuse to acute	obliquely elliptic to strap-shaped, apex obtuse
Labellum size	2.6 × 2.8 mm	4.5 × 3 mm	6.5 × 6.5 mm
Labellum midlobe	widely ovate callus	widely ovate callus	large heart-shaped callus
Labellum lateral lobes	widely rounded	rounded	divergent, triangular, obtuse

Artificial key to Bryobium from Malaysia with caespitose pseudobulbs

Eria cordifera Schltr. [62]; Eria cordifera subsp. borneensis J.J.Wood [60].

MALAYSIA. Sarawak, Gunung Mulu National Park, Rib Anderson Camp, 14 march 1978, Nielsen 652 (holotype AAU-Photo!); PAPUA NEW GUINEA. Kani Gebirges, 10 May 1908, ca. 1000 m elev., Schlechter L.0058744 (isotype NHN-photo!); Kani Gebirges, 10 May 1908, ca. 1000 m elev., Schlechter K000827429 (isotype K-photo!).

Carr, Gard. Bull. Straits Settlem. 7: 72 (1932); Fig 13.

Fig 13

Taeniophyllum rugulosum.

A. Plant growing on a fallen twig of Neonauclea sp. (Rubiaceae) tree in a riverine forest. B, C, D, E. Inflorescence from lateral and front view. F. Plant’s top view showing wrinkled roots (spirit-preserved). G. Flower’s lateral view (spirit-preserved). H. Sepals and petals (spirit-preserved). I. Labellum’s lateral view (spirit-preserved).

Type: MALAYSIA. Peninsular Malaysia, Pahang, Sat River, August 1929, Carr K000942486 (unknown type K-photo!).

Specimen examined:––MALAYSIA. Perak, Lenggong, ca. 100 m elev., 3 April 2021, Besi et al. HS107 (UPM!).

Plants leafless epiphytic herb forming tangled colonies, often several joined together in a chain, culminates more than 10 inflorescences when flowering. Roots thin, flattened, wrinkled, 3–15 × 0.1–0.3 cm, green. Stems 1–3 mm long. Leaves absent. Inflorescence an axillary raceme, ca. 1–1.5 cm long, peduncle filiform, glabrous, apex with alternate and sinuous bracts, green; rachis 5–10 mm long, flattened. Flowers 1 or 2 per inflorescence, resupinate, porrect, tubular, 5 × 2 mm, yellowish green, borne successively, spur 1 mm long, tubular; buds, open flowers and capsules often present simultaneously; sepals, petals and labellum almost having the same length, barely distinguishable. Pedicel-with-ovary 3 mm long, cylindric. Sepals and petals somewhat fleshy, basally fused, spreading only in upper half, triangular. Dorsal sepal free part ca. 3.3 × 0.9 mm, narrowly triangular, apex acute. Lateral sepals free part ca. 3.2 × 0.5 mm, triangular, wider at base, apex acute, longer than petals. Petals free part ca. 3 × 0.5 mm, narrowly triangular, apex acute. Labellum ca. 3 × 0.7 mm, unlobed, pyriform when flattened; apex small, obtuse, upcurved, falcate; spur 1 mm long. Gynostemium porrect, at slight angle to ovary, less than 1 mm long. Capsules porrect, ellipsoid, ca. 7 mm long.

So far, the species has only been recorded in Peninsular Malaysia and Borneo [25, 41] (Fig 14). However, the occurrence is still not well-known. Due to the inconspicuous appearance of these plants, small, recurrently occurring high in the forest canopy with small short-lived flowers, they are easily overlooked in the field and often preserved in poor conditions [63].

Fig 14

Distribution of Taeniophyllum rugulosum.

In Greek, tainia means fillet and phyllon means leaf, and Taeniophyllum referrring to the long filamentous leaves of the plant [43]. Meanwhile, the species epithet, rugulosum, in Latin, ruga means finely rugose, referring to the roots having many small wrinkles.

The plant was growing as epiphytes in a lowland riverine forest, on a common riverine tree. Plants were growing on twigs about 3 cm thick.

Taeniophyllum rugulosum is belonging to subg. Codonosepalum sect. Sepalocodon, a group characterised by having sepals and petals adnate at base and bracts alternate [64]. Our specimen is characterised by the flattened roots, flattened 2-ranked and alternate bracts, yellowish-green and flowers 5 mm long, triangular tepals and labellum, sepals and petals basally fused into a tube, and the free part of sepals always longer than tube. Some of these characters are also shared with the closely-related species, T. campanulatum Carr, T. intermedium Carr, and T. stella Carr. The absence of incurved spine on the labellum and the wrinkled roots differentiate T. rugulosum from T. stella [63].

Artificial key to Taeniophyllum subg. Codonosepalum sect. Sepalocodon from Peninsular Malaysia

Taeniophyllum campanulatum Carr [64], Taeniophyllum intermedium Carr [64], Taeniophyllum stella Carr [64].

MALAYSIA. Pahang, Tembeling, Sat River, August 1929, ca. 152 m elev., Carr K000942486 (K-photo!).

Comparison on distinctive morphological characters.

A. Paphiopedilum Subgenus Paphiopedilum from Peninsular Malaysia, with usually single flowers (or at most 2 flowers) per plant. B. Calanthe Sect. Monophylla from Peninsular Malaysia. C. Luisia from Peninsular Malaysia with small flowers ca. 5 mm wide and petals shorter or same length as sepals. D. Habenaria from Peninsular Malaysia, has leaves linear and acute, and a labellum with three linear lobes. E. Bryobium from Malaysia with caespitose pseudobulbs. F. Taeniophyllum Subgenus Codonosepalum Section Sepalocodon from Peninsular Malaysia.

(DOCX)

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List of specimens examined, including information on localities, collectors, date of collection, and habitat.

A. Paphiopedilum exul (Ridl.) Rolfe. B. Calanthe chrysoglossoides J.J.Sm.. C. Luisia brachystachys (Lindl.) Blume. D. Habenaria rostellifera Rchb.f.. E. Bryobium cordiferum subsp. borneense (J.J.Wood) Schuit. F. Taeniophyllum rugulosum Carr.

(DOCX)

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Leaves elliptic to oblong-elliptic, yellowish or bluish green, usually mottled; flowers bluish green………………….P. bullenianum, P. barbatum, P. callosum var. sublaeve (sect. Barbata)

Leaves strap-shaped to oblong-elliptic, plain green; flowers yellowish green…………P. exul (sect. Paphiopedilum)

1	Flowers glabrous, yellowish white ………………………………………‥C. taenioides
	Flowers finely pubescent outside, pinkish white………………………………………2
2	Labellum apically bilobed, lobules diverging and rounded……………‥C. monophylla
	Labellum apically unlobed, apiculate…………………………….C. chrysoglossoides

1	Plants and flowers usually large; plants pendant more than 30 cm long; flowers more than 1 cm wide; petals filiform, longer than sepals…………L. antennifera, L. curtisii, L. jonesii
	Plants and flowers small; plants less than 30 cm long; flowers ca. 5 mm wide; petals shorter or same length as sepals…………………………………………………………2
2	Petals ovate, as long as dorsal sepal, together forming a hood; labellum bilobed………………………………………………………………………L. zollingeri
	Petals linear, narrower than dorsal sepal, 1 mm wide; labellum simple……………L. brachystachys

1	Leaves wide, more than 2 cm wide, ovate to oblanceolate…………H. acuifera, H. carnea, H. dentata., H. kingii, H. medioflexa, H. reflexa, H. rhodocheila, H. rumphii, H. singapurensis
	Leaves linear to narrowly lanceolate, 0.5 to 1.5 cm wide……………………………….2
2	Flowers white, lateral sepals oblong with acute tips; labellum lobes linear, more than 1 mm wide………………………………………………………………H. paradiseoides
	Flowers pale salmon pink, lateral sepals ovate to rounded; labellum lobes filiform, 0.5–1 mm wide………………………………………………………………‥H. rostellifera

1	Pseudobulbs conspicuous, 6–11 cm long………………………………‥B. hyacinthoides
	Pseudobulbs caespitose, 1–3 cm long……………………………………………………2
2	Pseudobulbs conical bearing single leaf; flowers scented; labellum midlobe with irregular callus………………………………………………………………‥B. pudicum
	Pseudobulbs inconspicuous, covered by triangular and alternate sheaths, bearing two leaves; flowers unscented; labellum midlobe with prominent ovate callus…………………………………………………….B. cordiferum subsp. borneense

1	Rachis short, 3 mm long………………………………………………………………2
	Rachis long, 5–10 mm long……………………………………………………………3
2	Flowers campanulate; free parts of petals and sepals shortly triangular, shorter than the fused part, 1 mm long…………………………………………………T.campanulatum
	Flowers conical; free parts of petals sepals subulate, adnate at the middle in to a tube, spreading and reflexed, ca. 5 mm long…………………………………………T. stella
3	Sepals and petals shortly adnate at the base into a tube for a 1 mm long…………………………………………………………………………………………….T. intermedium
	Sepals and petals adnate at the middle into a tube for a 2.5 mm long……………………………………………………………………………………………….T. rugulosum