Gardens’Bulletin Singapore 66(2): 153-167. 2014 153 Notes on Singapore native Zingiberales I: A new species of Zingiber and notes on the identities of two further Zingiber taxa & J. Leong-Skomickoval, A. Thame^ P.T. Chew^ ^Herbarium, Singapore Botanic Gardens, National Parks Board, Cluny Road, Singapore 259569 1 [email protected] j ^Conservation Division, Central Nature Reserve, National Parks Board, Cluny Road, Singapore 259569 1 ABSTRACT. A new species of Zingiber singapurense Skomick., is described and illustrated here. It is compared to other species from the Zingiber gracile {Zingiber sect. Zingiber) A alliance. key to this group of species in Peninsular Malaysia and Singapore and a key to all Singapore native and naturalised Zingiber species are provided. The national and international conservation status of the new species and a conservation strategy for it are discussed. Notes on the varietal identity of Zingiber ptiberulum and the presence of Z. ottensii, previously misidentified as Z. zerumbet, in Singapore are given. Keywords. Central Catchment Nature Reserve, conservation, lUCN, Zingiber gracile, Z. griffithii, Z. ottensii, Z. puberulum, Z. singapurense, Z. zerumbet, Zingiberaceae Introduction A conservationproject on Singapore’s native Zingiberales was initiatedbythe Research & Conservation Branch of the Singapore Botanic Gardens, National Parks Board, in January 2011. Although the initial 15 months of funding has expired, the project continues in various forms with support from a wide network of collaborators within and outside NParks. Initially, the project mainly involved intensive surveys offorested areas, marking of all existing populations/mature adult plants ofnative Zingiberales, regular monitoring of flowering and seed-set, and ex situ and in vitro propagation of native material from Singapore stock for re-introduction puiposes. These efforts continue but, as we progress with the project, we are also realising that there is a need We to clarify various taxonomic issues (correct identitifications, nomenclature). are also conducting in-depth studies of reproductive biology and are updating the lUCN conservation status for all native Zingiberales in Singapore. This paper is the first in the series entitled ‘Notes on Singapore Native Zingiberales’. This series will include rediscoveries of taxa presumed to be extinct in Singapore, provide taxonomic and nomenclature updates, and raise awareness of, and encourage an active approach towards, the conservation ofnative Zingiberales and other plants in Singapore. 154 Gard. Bull. Singapore 66(2) 2014 Information on Singapore’s geography and vegetation types, and the affinities ofits flora to those ofPeninsular Malaysia and Sumatra, have recently been discussed in detail (e.g. Chong et al., 2011; Ng et al, 2011; Yee et ah, 2011; Low et al., 2014) and are, therefore, not repeated here. Recently, as interest has increased, numerous surveys have reported new records for Singapore as well as rediscoveries ofpresumed locally extinct species (e.g. Rodda et al., 2012; Yeoh et al., 2013; Low et al., 2014). As Singapore’s flora is comparatively well known, and forested areas with primary 3% and mature secondary forests fairly small (accounting for about - Yee et al., 2011), A reports ofa new plant taxon from Singapore are infrequent. Cry’ptocoryne Fisch. ex Wydler hybrid from Bukit Timah Nature Reserve was reported in 2001 (Bastmeijer & Kiew, 2001). Nine new species of Thottea Rottb. were also described by Yao (2013) from Peninsular Malaysia, of which T. praetermissa T.L.Yao is also found in Singapore. The most recent example is of two Utania G.Don species (Gentianaceae) & occurring in Singapore and the southern part of Peninsular Malaysia (Sugumaran Wong, 2014), based on types from Singapore. The presence ofthe Thottea and the two Utania species were, however, already recorded in Singapore from the 1890s with we multiple collections for all thi'ee taxa, albeit misidentified. In tins paper, present a new ginger species for which no earlier collections are known. In 2012, two sterile living specimens of a small Zingiber Mill, species were collected during a regular survey in Singapore’s Central CatchmentNature Reseiwe by William Ng oftheNational Parks Board, Singapore. Unfortunately, neither ofthe plants survived and the original colleetion locality, said to contain just a few individuals, could not be re-located. In October 2013 and April 2014, the same species was found in three different locations within patches of primary and mature secondary forest in the Central Catchment Nature Reserve. In May 2014, flowering plants were found at all three locations. These collections could not be matched to any Zingiber species from Singapore, Peninsular Malaysia, Borneo or Sumatra after careful study of type material, additional herbarium specimens and the protologues ofall related species of Zingiber sect. Zingiber from the Malesian region by the first author. It was, therefore, concluded that these new collections belong to a taxon as yet unknown to science which we here name Zingiber singapurense. The description and measurements are made from living material from all tliree populations. As previous works by Holttum (1950) and Theilade (1998) were mainly based on herbarium specimens, the dimensions of certain parts from dried material are also given to allow direct comparison to their descriptions and to type material ofrelated taxa. Taxonomy Zingiber singapurense Skomick., sp. nov. Similar to Zingiber aurantiacum (Holttum) Theilade, but differing in the smaller and more slender habit, inflorescences with distinctly convex fertile bracts (versus tightly mm mm appressed bracts), reduced bracteoles (up to 6 long versus c. 25 long) and 8 1 155 Singapore native Zingiberales I. lateral staminodes partly free from labellum (versus staminodes almost fidly connate with labellum). TYPE: Singapore, Central Catchment Nature Reserve, MacRitchie sector, 7 May 2014, J. Leong-Skornickovd & Aung Thame SNG-178 (holotype SING (including spirit material); isotypes E, K, KEP). (Fig. 1, 2) m mm Perennial evergreen rhizomatous herb to 0.8 tall. Rhizome 7-10 in diam., branched, internally light yellow, mildly aromatic. Leafy shoots of mature flowering m individuals 0.7-1.5 long, strongly arching, with 18-30 leaves; basal Va - Vs leafless, mm with 4-5 green glabrous sheathing bracts; leafsheaths green, glabrous; ligule 1-2 long, almost inconspicuous, bilobed, green, tomentose; petiole reduced to pulvinus, mm c. 2-3 long, light green, tomentose; lamina to 1 5-22 x 2-A cm (largest leaves of mature flowering individuals measured; dimensions when dried 14-20 x 1.8-2. cm), narrowly ovate, gradually tapering to a naiTowly attenuate-nan'owly caudate apex, base obtuse to rounded, above dark glossy green and glabrous, lighter green and glabrous beneath (except occasional space hairs near the midrib and the basal part near pulvinus). Inflorescence radical, to 23 cm long, erect; peduncle 5-10(-12) cm (comprising halfofthe length ofthe entire inflorescence); sheathing bracts 4-6, 0.5-3 cm long (basalmost shortest at c. 5 mm, gradually longer towards the spike), tubular at base (2-10 mm), cream-white to light green (those below the leaflitter layer cream- coloured, those above ± light green), with orange-reddish tinge in upper bracts, softly pubescent(hairsappressed);spike7-1 1x1 .5(-2) cmbroad(dimensionswhendried7-1 X 1-1.3 cm), narrowly fusiform, consisting of 8-17 bracts (lowermost and uppermost 2 bracts usually sterile); fertile bracts slightly obovate, lower bracts up to 3.6 x 2.3 cm (gradually smaller towards the apex), with broadly acute to obtuse apex, externally cream-white to light yellow at base, richly tinged orange-red in upper exposed parts, softly pubescent (hairs appressed), internally light yellow, glossy, glabrous, margin c. 0.5 mm, hyaline, translucent white, enclosing single flower; bracteole much reduced, mm mm to 2-7 long, 2-5 wide at base, triangular, translucent white, externally with sparse soft white appressed hairs, internally glabrous. Flower 6-7 cm long; calyx 13- mm 20 long, cylindric in basal third, inflated in apical part, with three inconspicuous teeth, incised unilaterally 6-10 mm, translucent white, sparsely pubescent towards mm the ovary, glabrous in apical half; floral tube 35-42 long, cream-white at base, yellowish towards apex; dorsal corolla lobe ovate-triangular, 26-28 x 9-1 mm, 1 translucent pale yellow, glabrous, apex narrowly acuminate, with indexed margins, rarely minutely cuculate; lateral corolla lobes narrowly ovate-triangular, 23-25 x 5-7 mm, translucent pale yellow, glabrous, apex narrowly acuminate, with inflexed mm mm margins; labellum 21-23 long, 9-1 wide (18-20 imn wide inclusive ofthe 1 lateral staminodes which are connate to the labellum and form a trilobed structure), pale yellow, glabrous; lateral staminodes 13-14 x 4-5 mm, connate to labellum in mm basal Vs, pale yellow, glabrous. Stamen 18-20 long (without straightening out mm mm the anther c\:qsX)\filament 1-1.5 long; anther c. 11 x 4 (excluding the crest), mm connective tissue cream-white, anther crest 11-13 long (straightened), exceeding stigma by 1-3 mm, cream-white to pale yellow at base, slightly darker towards apex; 156 Gard. Bull. Singapore 66(2) 2014 Fig. 1. Zingiber singapurense Skomick. A. Habit. B. Inflorescence. C. Rooting plantlet arising from the apical part ofthe leafy shoot. D. Detail ofligule. From type SNG-178. (Photos: Jana Leong-Skomickova) 157 Singapore native Zingiberales I. — — — ^ Fig. 2. Zingiber singapurense Skornick. A. Flower (side view). B. Flower (front view). C. Flower dissection (from left): Floral tube with ovary, calyx and anther attached, dorsal corolla lobe, two lateral corolla lobes, labellum with connated lateral staminodes, bracteole, fertile bract. D. Detail of ovary with epigynous glands, anther (side view) and anther (front view). From type SNG-178. (Photos: Jana Leong-Skornickova) mm anther thecae dehiscing along entire length. Epigynous glands two, c. 3.5 long, c. 0.75 mm in diam., cream-white. Ovary 3^ x 2-3 mm, cream-white, pubescent, hairs light rusty brown; style white, stigma with round, forward-facing ciliate ostiole. Fruits not seen. 158 Gard. Bull. Singapore 66(2) 2014 EcologyandphenologyK Zingibersingapurense occurs in primary andmature secondary forest, preferring moist and shady conditions. Flowering in May-June. Distribution. So far endemic to Singapore. Etymology. The specific epithet of this small and vulnerable yet resilient species is derived from Singapore’s name in Malay, ‘Singapura’. Additionalspecimens examined. SINGAPORE: CentralCatclnnentNature Reserve, MacRitchie sector, 21 May 2014, J. Leong-Skornickovd &Aung Thame GRC-l 79 (E, SING); 29 May 2014, MacRitchie sector, J. Leong-Skornickovd & Aung Thame GRC-l80 (E, SING); lUCN & Provisional conservation assessment consei^ation strategy^. So far only three populations in the Central Catchment Nature Reserve have been discovered with each population only having 10-25 mature individuals and less than 50 mature individuals in total. The Extent ofOccurrence (EOO) is 0.06 km^. Eligh visitor numbers andproposed development plans could adversely affect the quality of the habitat. Following the lUCN criteria (lUCN, 2012) and the criteria for national conservation assessments as outlined by Davison (2008), Zingiber singapurense should be considered nationally and globally Critically Endangered (Blab(iii,iv,v); D). Although the leafy shoots of most Zingiberaceae are pseudostems composed of leaf sheaths, true stems with buds, capable of producing bulbils or seedlings, have been reported in some Globba and Zingiber species. The stems of Zingiber singapurense are arching, a feature more prominent in older stems. The tips eventually touch the ground and new plantlets grow from the buds (Fig. 1C), This capability to reproduce vegetatively makes Zingiber singapurense less dependent on the presence ofpollinators and is certainly a reason behind its resilience, Flowever, it does appear that the populations also reproduce from seeds (assumed from the presence of small independent plantlets not physically connected to adult individuals). Nothing is cun'ently known ofthe genetic diversity in the three existing populations although such work is planned in the near future. Work on DNA barcoding of all native Zingiberales is also in progress (Khew et al., unpublished). The existing populations will continue to be closely monitored for fruit-set and the numbers of seedlmgs and vegetatively produced offsprings. By selective harvesting of young plantlets from overcrowded parts of the populations the chances ofsurvival ofthe remaining plantlets in the field improves. The harvested plantlets will be replanted in Singapore Botanic Gardens as stock for ex situ conservation. Currently, about 15 plants have been successfully established in the ex situ native gingers geraiplasm collection at the Singapore Botanic Gardens. These are individuals from all three populations to retain as much of the original genetic variation as possible. The establishment of cuttings from stem buds and of in vitro propagation to bulk up the number of plants is also in progress. These should produce enough stock for re- introductions into suitable habitats as well as for its introduction into the horticulture trade to lower the risk ofillegal harvesting from the wild populations. 159 Singapore native Zingiberales I. Notes. Zingiber is the largest genus in the sub-family Zingiberoideae with more than 200 names coiTesponding to approximately 100-150 species (Wu & Larsen, 2000; & Kishor Leong-Skomickova, 2013). The genus is well characterised by lateral staminodes connate to the labellum, an elongated hom-like anther crest wrapped around the stigma, and the presence of a pulvinus. Zingiber has been traditionally divided into four sections based on the position of the inflorescence {Zingiber sect. Zingiber, sect. Dymczewiczia (Horan.) Benth., sect. Pleuranthesis Benth. and sect. Cry’ptanthium Horan.). While a recent molecular study based on a single marker and limitedmaterialhints i\\3tZingibersect.Dymczewiczia andZingibersect.Pleuranthesis are not well segregated from Zingiber sect. Zingiber (Theerakulpisut et al., 2012), the old classification remains in use until a new classification is formally proposed. In its general habit and the position ofthe inflorescence, Zingiber singapurense falls clearly into Zingiber sect. Zingiber. In its narrowly fusifonn orange to red inflorescences and pale yellow flowers, it can be further narrowed to the group of species inthe Zingibergracile alliance (for akeyto Zingiber in PeninsularMalaysia see Theilade, 1998), The complexity ofthis group in Peninsular Malaysia was previously noted by Holttum (1950), who recognised four varieties (Zingibergracile van gracile, Z. gracile van aurantiacum Holttum, Z. gracile van elatius Ridl. and Z. gracile van petiolatum Holttum). Theilade (1998), who revised the genus Zingiber for Peninsular Malaysia, upgraded all varieties to the specific level (Z. gracile Jack, Z. aurantiacum (Holttum) Theilade, Z. elatius (Ridl.) Theilade and Z. petiolatum (Holttum) Theilade). Theilade also described an additional species fi’om this group. Zingiber suphureum & Burkill ex Theilade (Cowley Theilade, 1995). Lim (2003) added another two species & with nan*owly fusiform inflorescences to this group, Zingiber raja C.K.Lim Kharuk. and Z. kelantanense C.K.Lim. Ofthe seven species in the Zingiber gracile alliance, four have elliptic to ovate laminae with an approximate length:width ratio of < 4.5. The large Zingiber raja m (type from Perak, Belum F.R.), with pseudostems to 2.5 tall and elliptic laminae (lengthiwidth ratio 3.6-4.23; based on the protologue), can be excluded on account of its very long inflorescences (peduncles to 62 cm, spikes to 36 cm), markedly distinct dark maroon labellum, and staminodes with yellow blotches. Zingiber kelantanense m (type from Kelantan, Stong F.R.) is also a large species to 2.5 in height, with elliptic, plicate and prominently petiolate laminae (length:width ratio 3^.1; based m on the protologue). The following two species are smaller in habit to 1 in height. Zingiber gracile (type from Penang), stands out in this gi'oup due to its long, papery, thin ligules (up to 1,8 cm in the type herbarium material) and elliptic lamina (to 16 x 4.2 cm, length:width ratio 3.8; based on the lectotype) and well-developed bracteoles mm (c. 20-25 long). Zingiber sulphureum (type from Taman Negara) differs in its 15^5 elliptic to ovate, abaxially hairy lamina (to cm, length:width ratio 3; based on an isotype), sulphur yellow bracts at anthesis, prominently bilobed papery ligules to 6 mm long and completely missuig bracteoles. Zingiber singapurense has dark green, narrowly ovate to naiTOwly elliptic laminae (14-20 x 1 .8-2.8 cm, length:width ratio 7. 1-7.8; based on herbarium material ofthe holotype and isotypes) and short ligules, therefore in general habit similar to the 160 Gard. Bull. Singapore 66(2) 2014 remaining three species. Delimitation of Zingiber singapurense within this group is, however, straightforward as it is the only species which has much reduced triangular mm bracteoles (to 2-7 long) and distinctly convex bracts, giving the inflorescence a bullate appearance (Fig. IB). It is also the smallest and most delicate species in the m group, with leafy shoots to 1.5 long, but distinctly arching and not exceeding 0.8 m in height. The bracteoles are well developed in Zingiber aurantiacum (c. 25 mm), Z elatius (25-30 mm) and Z. petiolatum (c. 30 nmi). Zingiberpetiolatum (type from m Kedah) is a much larger species, up to 3 tall, with somewhat petiolate leaves up to 34/40 X 5.5 cm, and inflorescences up to 86/110 cm long, inclusive of the spike to 34/44 cm long (measured from the lectotype/isolectotype; lamina length:width ratio 6.2/7.2). Zingiber elatius (type from Penang Hill) is clearly distinct in the inflorescence composed of a long peduncle (to 36 cm; in type material), an ovoid spike composed of bronze to red-purple bracts (c. 11 x 2.6 cm; in isolectotype), and flowers with a pale yellow labelhim ornamented with fine dark purple lines and tinged in the centre. The lamina length:width ratio is c. 10 (Fig. 3A, B). Zingiber aurantiacum (type from m Pahang, Fraser’s Hill), is a more robust, montane species up to 2 tall, with larger leaves (to 26 x 4.1 cm, length:width ratio c. 6.2; based on the lectotype), reddish leaf- sheaths in young shoots, larger inflorescences (to 43 cm in type material) with tightly appressed bright orange fertile bracts at anthesis, and lateral staminodes almost fiilly connate with the labellum (Fig. 3C, D). Key to species from the Zingiber gracile alliance in Peninsular Malaysia and Singapore la. Lamina elliptic to ovate (length:width ratio < 4.5) 2 lb. Lamina narrowly ovate to narrowly elliptic (length:width ratio >6) 5 2a. Ligules short (c. 2 mm), labellum and staminodes dark maroon with yellow Z blotches raja 2b. Ligules 4-22 mm, flowers light yellow 3 m Z 3a. Plant to 2.5 tall, lamina petiolate, prominently plicate kelantanense m 3b. Plant to 1 tall, lamina ± sessile, smooth or weakly bullate 4 4a. Ligules to 18 mm, fertile bracts orange to pink at anthesis, bracteoles well Z developed gracile 4b. Ligules 4-6 mm, fertile bracts sulphur yellow at anthesis, bracteoles absent Z sulphureum mm 5a. Bracts prominently convex, bracteoles reduced (to 7 long) Z singapurense mm) 5b. Bracts tightly appressed, bracteoles well-developed (25-30 6 161 Singapore native Zingiberales I. 6a. Spike ovoid, bracts bronze to red-purple at anthesis, labelliim pale yellow ornamented by fine dark purple lines and tinged in the centre Z. elatius 6b. Spike narrowly fusiform, bracts orange to rose-pink at anthesis, labellum plain pale yellow 7 m 7a. Leafy shoots 2-3 tall, inflorescence to 110 cm long (peduncle to 65 cm long, spike to 44 cm long) Z. petiolatum m 7b. Leafy shoots 1-2 tall, inflorescence to 56 cm long (peduncle to 40 cm long, cm spike to 1 6 long) Z. aurantiacum The genus Zingiber in Singapore In Singapore only two Zingiber species are cun'ently considered native: Zingiber griffithii Baker and Zingiber puberulum Ridl. Both are easy to distinguish from Zingiber singapurense even when sterile (Fig. 4). Zingiber griffithii has leafy shoots m 0.5-0.8 tall, with 5-8(-10) leaves per shoot, leaf sheaths almost glabrous at base, with sparse long silky appressed hair at apical part, lamina elliptic, thin, bright green, slightly plicate, c. 12-25 x 5-8 cm, with long silky appressed hairs abaxially. Zingiber m puberulum is a more robust species with leafy shoots up to 2 tall, withup to 23 leaves per shoot, leaf sheaths puberulous to pubescent, lamina elliptic, slightly leathei'y, mid to dark green, sometimes with dull silvery finish, almost flat (plication negligible), c. 20-35 X 5-8 cm, adaxially puberulous. Zingiber singapurense is a delicate plant, not m m exceeding 0.8 in height (though its arching leafy shoots might be up to 1.5 long), with 18-26 leaves per shoot, lamina narrowly ovate, slightly leathery, dark glossy green, flat (not plicate) 15-22 x 2-A cm, glabrous adaxially, lighter green and almost glabrous abaxially (except occasional space hairs near the midrib and the basal part near pulvinus). The above measurements given are from living material in Singapore populations. The habit of Zingiber singapurense blends very well with other understorey vegetation and at first glance is reminiscent of young palm fronds or even some terrestrial orchids (e.g. Bromhaediafinlaysoniana (Lindl.) Miq.). Unless it is flowering it is fairly hard to spot this rare species, which is likely the reason why it has been overlooked until now. Tliree varieties ofZingiberpuberulum are currently recognised (Holttum, 1950; Theilade 1998), Z. puberulum var. puberulum, Z. puberulum var. chryseum (Ridl.) Holttum and Z. puberulum var. ovoideum (Ridl.) Holttum), ofwhich two are based on Singapore material. Zingiberpuberulum war. puberulum was described from material collected in Bukit Timah Nature Reserve (Singapore) where it is still present. All extant Shigapore material of this species belongs to this variety. Zingiber puberulum var. chryseum was described in 1908 by Ridley (as Z. chryseum) from the woods in the Stagmount area (Singapore). The forest in this area was cleared shortly thereafter and no further material of this taxon has ever been collected. It is presumed, therefore, to 162 Gard. Bull. Singapore 66(2) 2014 Fig. 3. Zingiber elatius (Ridl.) Theilade, photographed at Penang Hill (type locality). A. Habit and detail ofligule (inset). B. Inflorescence and detail offlower (inset). Zingiber aurantiacum (Holttum) Theilade, photographed at Fraser’s Hill (type locality). C. Habit and detail ofligule (inset). D. Inflorescence and detail offlower (inset). (Photos: Jana Leong-Skomickova)