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Research Article
Borneocola (Zingiberaceae), a new genus from Borneo
expand article infoYen Yen Sam, Atsuko Takano§, Halijah Ibrahim|, Eliška Záveská, Fazimah Aziz#
‡ Forest Research Institute Malaysia, Selangor, Malaysia
§ Museum of Nature and Human Activities, Sanda, Japan
| University of Malaya, Kuala Lumpur, Malaysia
¶ University of Innsbruck, Innsbruck, Austria
# Universiti Malaysia Sarawak, Kota Samarahan, Malaysia
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Abstract

A new genus from Borneo, Borneocola Y.Y.Sam, is described here. The genus currently contains eight species previously classified as members of the Scaphochlamys Baker. The finding is based on the results of the morphological and molecular studies of Scaphochlamys throughout its geographical range and its closely allied sister groups, Distichochlamys M.F.Newman and Myxochlamys A.Takano & Nagam. Borneocola is nested within the tribe Zingibereae and its monophyly is strongly supported by both ITS and matK sequence data. The genus is characterised by several thin, translucent and marcescent floral bracts, absence of coloured streaks on the labellum and capitate stigma with two dorsal knobs. The genus is distributed in northwest Borneo and all species are very rare and highly endemic.

Keywords

Distichochlamys, Myxochlamys, Scaphochlamys, morphology, phylogeny, taxonomy

Introduction

Southeast Asia is the centre of diversity for the family Zingiberaceae. Here, new taxa are continuously being discovered and named, both at the generic and specific levels. Several of the recent discoveries were further supported by the phylogenetic analyses which give a better understanding of the evolutionary relationships within the family (Kress and Larsen 2001; Kress et al. 2010; Leong-Škorničková et al. 2011). During the revision of the genus Scaphochlamys throughout its entire geographical range by the first author, some distinctive morphological traits were observed in several Bornean species, suggesting they might represent a separate group from the Peninsular Malaysian taxa. This hypothesis was confirmed by the phylogenetic analyses which are presented here and the eight species previously included in the genus Scaphochlamys are recircumscribed in this paper as a new genus, Borneocola Y.Y.Sam.

The genus Scaphochlamys was described by Baker (1892) in the Flora of British India with Scaphochlamys malaccana Baker from Mt. Ophir (now known as Gunung Ledang), Peninsular Malaysia, chosen as the type species. Holttum (1950) carried out the first comprehensive revision of the genus in which he recognised 19 species, all of which were recorded in the peninsula. When Smith (1987) reviewed the tribe Hedychieae in Borneo, she applied the generic delimitation defined by Holttum and recognised five Scaphochlamys species in Borneo. Out of the five, S. polyphylla and S. petiolata were formerly placed in the genus Haplochorema K.Schum. Sakai and Nagamasu (2006) discovered that H. gracilipes K.Schum. also have the characteristics of Scaphochlamys and effected the transfer. Recent years have seen a surge in the new species discovered from Borneo bringing the total number of Bornean Scaphochlamys to 14 (Poulsen and Searle 2005, Meekiong et al. 2011, Ooi and Wong 2014; Meekiong 2015).

Distichochlamys M.F.Newman and Myxochlamys A.Takano & Nagam. are sister genera to Scaphochlamys with several unique characteristics clearly separating them from Scaphochlamys (Newman 1995, Searle and Hedderson 2000, Kress et al. 2002, Ngamriabsakul et al. 2004, Takano and Nagamasu 2007). However, the distinction, based on morphological characters, became ambiguous as several taxa described recently exhibit exceptions to the usual generic characters. For example, S. calcicola A.D.Poulsen & R.J.Searle, a species named in 2005 from Sarawak, has a distichous inflorescence, a distinguishing character for the genus Distichochlamys M.F.Newman. Larsen and Newman (2001) also reported another Scaphochlamys species with a distichous inflorescence from north Peninsular Malaysia. A current study on the morphology of Scaphochlamys also revealed that some species display the characteristics of Distichochlamys and Myxochlamys. To test the validity of the current generic concept of Scaphochlamys and closely related genera Distichochlamys and Myxochlamys, we have examined their relationship by utilising ITS and matK markers together with the analysis of the morphology across these genera.

Materials and methods

Morphological study

The morphological study was based on living plants in the forest, cultivated plants in the nursery of the Forest Research Institute Malaysia and specimens in the herbaria of AAU, BKF, C, FI, E, K, KEP, KLU, PSU, SAN, SAR and SING. A total of 372 herbarium specimens were examined in this study which includes 29 Scaphochlamys species and four Borneocola species (the types of another four Borneocola species were not yet deposited in the herbaria).The morphological characters examined in the study were habit; position of the rhizome, thickness and colour; height of leafy stem, its base (whether swollen to form a bulbous base); distance between leafy stems; characters of bladeless sheath such as colour, indumentum, number and length; ligule length, indumentum and shape; petiole length, indumentum, whether channelled or rounded in cross section; number of leaves per leafy stem; lamina colour on both surfaces, size, shape, venation, texture, indumentum, apex and base; length of the inflorescence and infructescence, arrangement of the floral bracts on the rachis, characters of floral bracts and bracteoles (colour, indumentum, texture, shape); size, colour and shape of calyx, floral tube, corolla lobes, labellum, staminodes, stamen, ovary.

DNA extraction, amplification and sequencing

Fresh leaves from the cultivated plants or silica-dried materials from plants collected in the field were used for genomic DNA extraction.

For the ITS, the genomic DNA was extracted using the DNeasy Plant Mini Kit (Qiagen, Valencia, California, USA) following the manufacturer’s protocol. Two primers, ITS 5P (5’-GGAAGGAGAAGTCGTAACAAGG-3’) and ITS 8P (5’-CACGCTTCTCCAGACTACA3’) (Moller and Cronk 1997) were used to amplify the ITS region during the polymerase chain reaction (PCR). The thermal cycle of PCR for the amplification of the ITS sequences is initial denaturation at 94°C for 2 minutes, 40 cycles of denaturation at 94°C for 30 seconds, primers annealing at 48°C for 2 minutes, an extension at 72°C for 45 seconds and final extension at 72°C for 7 minutes. The PCR products were then purified using MinElute Gel Extraction Kit (Qiagen, Valencia, California, USA).

For the matK, the protocols for DNA extraction, condition, purification and DNA sequencing were described previously by Takano and Nagamasu (2007). The PCR and sequencing primers for matK (cpDNA) were TA-240f (5’-GGGAAA GGATGGGGTCTCCCG-3’), TA-150r (5’-CTCAAGGAGTTTTGTGGTTC-3’), TA-470F (5’-CCCTCTCCCGTCCATATGGA-3’) (all three were designed in the present study), matK8 (Steele and Vilgalys 1994), m5r (Kress et al. 2002), matK8r (Ooi et al. 1995), trnK2621 (Liston and Kadereit 1995), TA-10F, TA-05R, TA-02F and TA-02R (all from Takano and Okada 2002).

Sequence alignment and phylogenetic analysis

Raw sequence data were assembled and edited manually using BioEdit software ver. 7.2.5 (Hall 1999). DNA sequences were aligned with the CLUSTALW 1.83 software package, with default settings and multiple alignments (Thompson et al. 1994). Alignments of the matK sequences of cpDNA and the ITS sequences of nrDNA were combined. Gaps were deleted.

A total of 100 individuals including 54 taxa of Scaphochlamys and allied species were used. The three Siphonochilus species were used as an outgroup (Kress et al. 2002). Materials, accession numbers for the sequences, vouchers and references to the literature are presented in Table 1 at the end of this paper. Three datasets which comprise ITS, matK and ITS+matK combined, each containing 82, 78, and 61 taxa, were constructed. These three datasets were analysed using three methods: maximum parsimony, maximum likelihood and Bayesian analysis. A maximum parsimony (MP) analysis was performed with MEGA 6 (Tamura et al. 2013). Heuristic searches were conducted with RANDOM addition, SPR branch swapping and MULPARS options. Support for each branch was estimated with a bootstrap analysis, with 1000 replications (Felsenstein 1985), in a heuristic search with RANDOM addition and TBR branch swapping. The maximum likelihood (ML), based on the Tamura-Nei model (Tamura and Nei 1993), was also determined with MEGA 6 (Tamura et al. 2013). Neighbor-Join and BioNJ algorithms were applied to a matrix of pairwise distances estimated with the maximum composite likelihood approach; then, the topology that had the best log likelihood value was selected. Bootstrap analysis under the MP criterion was conducted with “fast” stepwise, addition searches, with 1000 replicates. In addition, a Bayesian analysis was carried out with MrBayes software ver. 3.1.2 (Huelsenbeck and Rohnquist 2001; Rohnquist and Huelsenbeck 2003). The best fitting substitution model (the GTR+G model for nrDNA datasets, the GTR+G model for cpDNA datasets and the GTR+I+G model for cpDNA+nrDNA datasets) was selected for Bayesian analysis based on a series of hierarchical likelihood ratio tests, implemented in MrModeltest software ver. 2.3 (Nylander 2004). The analysis was performed with the selected model and two simultaneous runs of two million generations with four chains, sampling every 100 generations. Each analysis reached stationarity (i.e. when the average standard deviation of split frequencies between runs was ≤ 0.01) well before the end of the run. Burn-in trees were discarded and the remaining trees and their parameters were saved. A 50% majority rule consensus tree was constructed. The results of the Bayesian analysis were reported as the posterior probability (PP; Huelsenbeck and Rohnquist 2001), which is equal to the percentage of phylogenetic trees sampled when a given clade was resolved. Only PP scores above 50% are shown.

List of accession details, vouchers and references used in the phylogenetic analyses.

No Subfamily Tribe Species ITS matK References/Voucher
1 Alpinioideae Link Alpinieae A.Rich. Alpinia blepharocalyx K.Schum. AF478709 AF478809 Kress et al. 2002
2 Alpinia elegans K.Schum. AF478713 AF478813 Kress et al. 2002
3 Amomum villosum Lour. AF478824 Harris et al. 2000 (ITS), Kress et al. 2002 (matK)
4 Amomum yunnanense S.Q.Tong AY352012 Xia et al. 2004
5 Elettariopsis kerbyi R.M.Sm. AF414496 AF478845 Pedersen 2004 (ITS)/Kress et al. 2002 (matK)
6 Renealmia battenbergiana Cummins ex Baker AF478779 AF478880 Kress et al. 2002
7 Siphonochileae W.J.Kress Siphonochileae W.J.Kress Siphonochilus aethiopicus (Schweinf.) B.L.Burtt AF478792 AF478893 Kress et al. 2002
8 Siphonochilus decorus (Druten) Lock AF478793 AF478894 Kress et al. 2002
9 Siphonochilus kirkii (Hook.) B.L.Burtt AF478794 AF478895 Kress et al. 2002
10 Tamijioideae W.J.Kress Tamijieae W.J.Kress Tamijia flagellaris S.Sakai & Nagam. AF478797 AF478898 Kress et al. 2002
11 Zingiberoideae Haask. Globbeae Meisn. Gagnepainia thoreliana K.Schum. AF478752 AF478851 Kress et al. 2002
12 Hemiorchis rhodorrhachis K.Schum. AY339706 AY341090 Williams et al. 2004
13 Mantisia wengeri C.E.C.Fischer AF478871 Kress et al. 2002
14 Zingiberoideae Haask. Zingibereae Meisn. Boesenbergia pulcherrima Kuntze AF478725 AF478825 Kress et al. 2002
15 Boesenbergia rotunda (L.) Mansf. AF478727 AF478826 Kress et al. 2002
16 Borneocola biru (Meekiong) Y.Y.Sam LC148403 FRI 50290 (KEP)
17 Borneocola calcicola (A.D.Poulsen & R.J.Searle) Y.Y. Sam LC148062 LC148380 FRI 50290 (KEP)
18 Borneocola sp. FRI 50295 LC148085 LC148404 FRI 50295 (KEP)
19 Borneocola sp. S 99106 LC148086 LC148405 S 99106 (SAR)
20 Borneocola stenophyllus (Ooi & S.Y.Wong) Y.Y.Sam LC148084 LC148400 FRI 50288 (KEP)
21 Borneocola petiolatus (K.Schum.) Y.Y.Sam LC148075 LC148395 FRI 50291 (KEP)
22 Borneocola reticosus (Ridl.) Y.Y.Sam LC148078 LC148398 FRI 50294 (KEP)
23 Camptandra parvula Ridl. AF478730 AF478830 Kress et al. 2002
24 Caulokaempferia saxicola K.Larsen AY478732 AF478831 Kress et al. 2002
25 Cautleya gracilis (Sm.) Dandy AF478734 AF478833 Kress et al. 2002
26 Cautleya spicata Baker AF478735 AF478834 Kress et al. 2002
27 Cornukaempferia aurantiflora J.Mood & K.Larsen AF478736 AF478835 Kress et al. 2002
28 Curcuma bicolor J.Mood & K.Larsen AF478737 AF478837 Kress et al. 2002
29 Curcuma roscoeana Wall. AF478739 AB047741 Kress et al. 2002 (ITS)/Cao et al. unpublished (matK)
30 Distichochlamys citrea M. F. Newman AY424757 Ngamriabsakul et al. 2004
31 Distichochlamys citrea M. F. Newman 2 AB552946 AB552951 Ngamriabsakul 24 (E)
32 Zingiberoideae Haask. Zingibereae Meisn. Distichochlamys sp. AS18 AB552947 AB553309 Adele Smith 18 (E)
33 Distichochlamys sp. Kress01-6848 AF478745 AF478844 Kress et al. 2002
34 Haniffia albiflora K.Larsen & J.Mood AF478756 AF478855 Kress et al. 2002
35 Hedychium longicornutum Griff. ex Baker AF478761 AF478860 Kress et al. 2002
36 Hedychium villosum Wall. AF478762 AF478861 Kress et al. 2002
37 Hitchenia glauca Wall. AF478765 AF478864 Kress et al. 2002
38 Kaempferia parviflora Wall. AB232052 Searle and Hedderson 2000
39 Kaempferia rotunda L. AF478767 AF478868 Kress et al. 2002
40 Kaempferia sp. Kress98-6289 AF478768 AF478869 Kress et al. 2002
41 Myxochlamys mullerensis A.Takano & Nagam. AB245522 AB269791 Takano and Nagamasu 2007
42 Myxochlamys nobilis Nagam. ined. AB552948 AB553310 Nagamasu 8274 (BO, KYO)
43 Pommereschea lackneri Wittm. AF478877 Kress et al. 2002
44 Pyrgophyllum yunnanense (Gagnep.) T.L.Wu & Z.Y.Chen AF478777 AF478878 Kress et al. 2002
45 Rhynchanthus beesianus W.W.Sm. AF478784 AF478885 Kress et al. 2002
46 Roscoea cautleoides Gagnep. AF478736 AF478887 Kress et al. 2002
47 Roscoea purpurea Sm. AF478787 AF478888 Kress et al. 2002
48 Scaphochlamys abdullahii Y.Y.Sam & Saw LC148054 FRI 44375 (KEP)
49 Scaphochlamys abdullahii Y.Y.Sam & Saw LC148055 LC148374 FRI 50198 (KEP)
50 Scaphochlamys atroviridis Holttum LC148056 FRI 68924 (KEP)
51 Scaphochlamys baukensis Y.Y.Sam LC148057 FRI 68955 (KEP)
52 Scaphochlamys biloba (Ridl.) Holttum LC148059 FRI 46606 (KEP)
53 Scaphochlamys biloba (Ridl.) Holttum LC148081 FRI 50224 (KEP)
54 Scaphochlamys biloba (Ridl.) Holttum LC148083 FRI 66331 (KEP)
55 Scaphochlamys biloba (Ridl.) Holttum 1 AF478788 AY478889 Kress et al. 2002
56 Scaphochlamys biloba (Ridl.) Holttum 2 AF202416 Wood et al. 2000
57 Scaphochlamys breviscapa Holttum LC148377 FRI 50269 (KEP)
58 Scaphochlamys breviscapa Holttum LC148060 LC148376 FRI 44984 (KEP)
59 Scaphochlamys burkillii Holttum LC148379 FRI 68928 (KEP)
60 Scaphochlamys burkillii Holttum LC148061 FRI 46504 (KEP)
61 Scaphochlamys concinna (Baker) Holttum AJ388283 Searle and Hedderson 2000
62 Scaphochlamys concinna (Baker) Holttum LC148063 LC148381 FRI 50351 (KEP)
63 Scaphochlamys cordata Y.Y.Sam & Saw LC148064 FRI 44306 (KEP)
64 Scaphochlamys endauensis Y.Y.Sam & Ibrahim LC148383 FRI 50243 (KEP)
65 Scaphochlamys endauensis Y.Y.Sam & Ibrahim LC148080 FRI 50218 (KEP)
66 Scaphochlamys erecta Holttum LC148065 FRI 44987 (KEP)
67 Scaphochlamys grandis Holttum LC148384 FRI47184 (KEP)
68 Scaphochlamys grandis Holttum LC148066 LC148385 FRI 50171 (KEP)
69 Zingiberoideae Haask. Zingibereae Meisn. Scaphochlamys johorensis Y.Y.Sam LC148082 FRI 66566 (KEP)
70 Scaphochlamys klossii (Ridl.) Holttum LC148067 LC148387 FRI 50238 (KEP)
71 Scaphochlamys kunstleri (Baker) Holttum AF478789 AY478890 Kress et al. 2002
72 Scaphochlamys kunstleri (Baker) Holttum var. rubra C.K.Lim AB552950 AB553312 Anon C 8003 & C. Ngamriabsakul 25 (E)
73 Scaphochlamys kunstleri (Baker) Holttum var. kunstleri LC148388 FRI 68926 (KEP)
74 Scaphochlamys kunstleri (Baker) Holttum var. kunstleri LC148068 FRI 68936 (KEP)
75 Scaphochlamys kunstleri var. speciosa C.K.Lim LC148389 FRI 68936 (KEP)
76 Scaphochlamys lanceolata (Ridl.) Holttum LC148069 LC148390 FRI 50130 (KEP)
77 Scaphochlamys laxa Y.Y.Sam & Saw LC148391 FRI 68961 (KEP)
78 Scaphochlamys longifolia (Ridl.) Holttum LC148070 LC148392 FRI 47065 (KEP)
79 Scaphochlamys malaccana Baker LC148393 FRI 50203 (KEP)
80 Scaphochlamys malaccana Baker LC148071 FRI 50208 (KEP)
81 Scaphochlamys minutiflora Jenjitt.& K.Larsen LC148394 3175
82 Scaphochlamys obcordata P.Sirirugsa & K.Larsen AJ388286 Searle and Hedderson 2000
83 Scaphochlamys oculata (Ridl.) Holttum LC148072 LC148396 FRI 50262 (KEP)
84 Scaphochlamys pennipicta Holttum LC148073 FRI 50261 (KEP)
85 Scaphochlamys perakensis Holttum LC148074 FRI 50214 (KEP)
86 Scaphochlamys polyphylla (K.Schum.) B.L.Burtt & R.M.Sm. LC148076 LC148397 FRI 50289 (KEP)
87 Scaphochlamys pusilla Y.Y.Sam LC148077 FRI 50260 (KEP)
88 Scaphochlamys rubromaculata Holttum LC148399 FRI 50178 (KEP)
89 Scaphochlamys rubromaculata Holttum LC148079 LC148378 FRI 50172 (KEP)
90 Scaphochlamys samunsamensis Meekiong & Hidir LC148401 MK 2344 (HUMS)
91 Scaphochlamys sp.nov. LC148402 FRI 68983 (KEP)
92 Scaphochlamys sub-biloba (Burkill ex Ridl.) Holttum LC148375 FRI 75334 (KEP)
93 Scaphochlamys sylvestris (Ridl.)Holttum LC148087 FRI 50197 (KEP)
94 Scaphochlamys tenuis Holttum LC148088 FRI 47233 (KEP)
95 Schaphochlamys cf. gracilipes (K.Schum.) S.Sakai & Nagam. LC148386 K.Meekiong (HUMS)
96 Smithatris supraneanae W.J.Kress & K.Larsen AF478795 AF478896 Kress et al. 2002
97 Stahlianthus involucratus (King ex Baker) R.M.Sm. AF478796 AF478897 Kress et al. 2002
98 Zingiber gramineum Noronha AF478800 AF478902 Kress et al. 2002
99 Zingiber sulphureum Burkill ex I.Theilade AF478801 AF478904 Kress et al. 2002
100 Zingiber wrayii Prain ex Ridl. AF478802 AF478905 Kress et al. 2002

Results

Phylogenetic analyses

The ITS datasets for 82 individuals with 29 taxa of Scaphochlamys and 6 taxa of Borneocola contained 786 characters after alignment, which decreased to 769 after gaps were deleted; 319 of these were parsimony-informative. Likelihood analysis resulted in a ML tree with –lnL = 10438.212. Parsimony analysis produced three parsimonious trees with 1865 steps, a consistency index (CI) of 0.391 and retention index (RI) of 0.609. The ML, MP and Bayesian trees had similar topology; the ML tree is shown with bootstrap (BS) and MP-BS, and Bayesian Posterior Probability (PP) support in Figure 1 below.

Figure 1.

Molecular phylogenetic analysis of the ITS sequence data by the Maximum Likelihood method. Numbers above branches indicate bootstrap values of ML and MP and posterior probability of Bayesian Analysis.

Scaphochlamys formed a well supported clade (ML-BS/MP-BS/BA-PP support, 84/87/1.00). Each Myxochlamys and Borneocola consisted of a well supported subclade and became sisters to each other and they also became sistersto the Scaphochlamys clade. Distichochlamys species formed a well supported subclade and became sister to the Myxochlamys + Scaphochlamys + Borneocola clade (ML-BS/MP-BS/BA-PP 99/100/1.00).

The matK datasets for 78 individuals including 25 taxa of Scaphochlamys and 7 taxa of Borneocola contained 1,599 characters after alignment; 182 of these were parsimony-informative. Likelihood analysis resulted in a ML tree with -lnL = 5952.438. Parsimony analysis produced ten parsimonious trees with 557 steps, a consistency index (CI) of 0.613 and retention index (RI) of 0.080. The ML, MP and Bayesian trees had similar topology; the ML tree is shown with BS and MP-BS, PP support in Figure 2 below.

Figure 2.

Molecular phylogenetic analysis of the matK sequence data by the Maximum Likelihood method. Numbers above branches indicate bootstrap values of ML and MP and posterior probability of Bayesian Analysis.

Each of the two Myxochlamys species and seven Borneocola species formed a strongly supported subclade and became sisters to each other. Scaphochlamys became sister to them, but bootstrap or probability support was weak. The Distichochlamys species formed a well supported subclade, but all the genera that belong to subfamily Zingiberoideae became sisters to Scaphochlamys + Myxochlamys + Borneocola clade and not only to Distichochlamys.

The combined ITS and matK datasets for 61 individuals including 13 taxa of Scaphochlamys and 6 taxa of Borneocola, resulted in 2,336 characters, 488 of these were parsimony-informative (Figure 3 below). Likelihood analysis resulted in a ML tree with lnL = 16671.531. Parsimony analysis produced the most parsimonious trees with 2247 steps, a CI of 0.440 and a RI of 0.635. The ML, MP strict consensus and Bayesian trees had almost the same topology; the ML tree is shown with MP-BS, ML-BS and BA/PP support in Figure 3.

Figure 3.

Molecular phylogenetic analysis of the ITS+matK sequence data by the Maximum Likelihood method. Numbers above branches indicate bootstrap values of ML and MP and posterior probability of Bayesian Analysis.

Two Myxochlamys species and six Borneocola species formed a strongly supported subclade each and became sisters to each other. Scaphochlamys became sister to them and the bootstrap or posterior probability support was moderate. Distichochlamys species formed a well supported subclade and became sister to Scaphochlamys + Myxochlamys + Borneocola clade.

Morphology

The Borneocola and Scaphochlamys species look similar in their vegetative morphologies. They are mostly small-sized gingers without the conspicuous pseudostem, with one to several leaves arranged spirally and tightly on a very short stem at the base. So far, all the Borneocola species examined are unifoliate. Similarly, most of the Scaphochlamys species also bear one leaf except for several species which have leafy shoots composed of multiple leaves, for example, S. grandis, S. lanceolata, S. kunstleri, S. malaccana and S. minutiflora. The basal part of the leaves is covered with a few bladeless sheaths which are rather different for both groups in terms of their texture and colour. For Scaphochlamys, the sheaths are coriaceous, green, green with a red tinge or red and mostly persistent until the end of flowering (Figure 4A, B). On the other hand, the sheaths of Borneocola are thinner in texture with a lighter shade of green or brown. The thin sheaths normally dry up early (Figure 4C) and sometimes they are completely shredded during the time of flowering.

Figure 4.

Bladeless sheaths A Green and coriaceous in Scaphochlamys klossii (Peninsular Malaysia) B Red and coriaceous in Scaphochlamys abdullahii (Peninsular Malaysia) C Papery and marcescent in Borneocola calcicola (Sarawak). (Photographs by Y.Y. Sam).

The inflorescences of Borneocola and Scaphochlamys are terminal, stalked and consisted of few to many floral bracts. The differences lie in the characteristics of the floral bracts and flowers. Borneocola species have thin, translucent, early decaying and marcescent floral bracts. The colours of the bracts can be pink, pale brown, pale or light green (Figure 5A). On the contrary, the bracts of Scaphochlamys are coriaceous and sometimes hard in texture. They are usually green, green tinged red, red or reddish brown and remain fresh throughout the flowering (Figure 5B, C).

Figure 5.

A–C Floral bracts A Green and coriaceous in Scaphochlamys klossii B Red and coriaceous in Scaphochlamys pusilla C Scarious and marcescent in Borneocola petiolatus D–F Variegation on labellum D White labellum with purple lines beside the median band in Scaphochlamys malaccana E White labellum with red streaks beside the band in Scaphochlamys concinna F Lilac labellum without coloured streaks beside the band in Borneocola petiolatus. (Photographs by Y.Y. Sam)

Besides the characteristics of the floral bracts, the variegation on the labellum can give a quick guide to the two genera. Most Scaphochlamys have white flowers with a yellow median band and lilac, purple, red streaks or patches flanking the band on the labellum (Figure 5D, E). However, there is no such variegation on the labellum of Borneocola (Figure 5F). The whole labellum of Borneocola is pale pink, lilac, violet or white with a light yellow or greenish yellow median band.

Both Borneocola and Scaphochlamys have a long slender floral tube which is mostly puberulent externally in Borneocola (except for B. calcicola) but glabrous for Scaphochlamys. Another marked difference observed is in the stigma shape. Scaphochlamys has a funnel-shaped or beak-like stigma (Figure 6A, B) while it is almost oblate with two dorsal knobs in Borneocola (Figure 6C).

Figure 6.

Stigma A Funnel-shaped in Scaphochlamys endauensis B Beak-like in Scaphochlamys biloba C Capitate in Borneocola petiolatus. (Photographs by A & C N.M. Aidil, B Y.Y. Sam)

Taxonomic treatment

Borneocola Y.Y.Sam, gen. nov.

Diagnosis

Similar to Scaphochlamys and Myxochlamys. Borneocola has thin, translucent and marcescent floral bracts, absence of coloured streaks on labellum and two dorsal knobs on the stigma versus the coriaceous and persistent floral bracts, coloured streaks on labellum and absence of dorsal knobs on the stigma in Scaphochlamys. The mucilage on the floral bracts and the versatile anther of Myxochlamys are absent in Borneocola.

Type species

Borneocola reticosus (Ridl.) Y.Y.Sam, comb. nov. Gastrochilus reticosa Ridl., J. Straits Branch Roy. Asiat. Soc. 44: 195 (1905).

Description

Terrestrial rhizomatous herb, evergreen, rarely exceeding 50 cm in height. Rhizome creeping on the ground, terminal decumbent, rhizome elements short or long; roots fine, extensive, not tuberous. Leafy stem unifoliate, enclosed by a few bladeless sheaths at base, bladeless sheaths linear, papery, glabrous to hairy, light green or light brown, decaying early, leaf sheath glabrous or hairy, base swollen, margin thin and narrow; ligule membranous, inconspicuous, decaying early; petiole channelled in cross section, glabrous, lamina narrowly ovate to elliptic, rarely oblong, asymmetric, margin entire, smooth.

Inflorescence flowering from base to apex; peduncle short, usually hidden within leaf sheath; spike composed of compact rachis and 2–5 (–13) fertile bracts, bracts spirally and closely overlapping (rarely distichous), boat-shaped, 2-keeled, pink, pale brown, pale or light green, thin, translucent, glabrous or hairy, decaying early, marcescent, amplexicaul at the base of the bract, cincinni compact, 2–3 flowers in each cincinnus. First bracteole directly opposite floral bract and enclosing all the flowers and subsequent bracteoles, linear-shaped, 2-keeled, shorter than bracts, rarely same length. Flowers thin, delicate, ephemeral. Calyx tubular, splitting unilaterally on one side, floral tube long slender, usually puberulent externally, inner surface with a groove enveloping the style, corolla lobes 3, triangular ovate, translucent, glabrous, dorsal lobe apex hooded, lateral lobes 2, narrower than dorsal lobe. Staminodes elliptic to narrowly obovate, white, light yellow or green, spreading laterally, lined with translucent veins from base to apex, covered with glandular hairs on adaxial surface. Labellum obovate, flat, bilobed distally, rarely entire, translucent veins spread from base to apical part, pale white, pink, lilac or violet, median band light yellow or greenish yellow, without coloured streaks or patches beside the band, adaxial surface covered with glandular hairs. Stamen bends forward over labellum, usually white and covered with glandular hairs on abaxial surface, filament grooved, short, anther theacae 2, linear, dehiscing along entire length, basal ending with or without short spur, anther crest short, not recurved. Ovary ellipsoid, glabrous or sparsely hairy, unilocular, with basal placentation, less than 10 locules. Stigma small, held at apex of thecae, near oblate, 2 dorsal knobs, ostiole forward facing, ciliate. Epigynous glands 2, filiform, yellow. Fruit a capsule, ellipsoid or ovoid. Seeds not seen.

Etymology

This new genus is named after the island of Borneo and -cola (Latin) means dweller or inhabitant. This is to recognise the extremely rich and unique biodiversity that is found in Borneo.

Distribution

Borneo. The genus is currently known to occur only in the northwest and possibly central Borneo. Eight species are recorded from Sarawak, Malaysia and many more are undescribed.

Key to Borneocola species (modified from Ooi and Wong 2014)

1 Adaxial lamina with distinctly raised tessellate venation 6 Borneocola reticosus
Adaxial lamina without distinctly raised tessellate venation 2
2 Lamina broadly oblanceolate and elliptic to oblong, lateral veins conspicuously raised on adaxial surface 1 Borneocola argenteus
Lamina linear, lanceolate to broadly ovate and elliptic, lateral veins not conspicuously raised on adaxial surface 3
3 Lamina linear to very narrowly lanceolate, < 3 cm wide 8 Borneocola stenophyllus
Lamina lanceolate, ovate to elliptic, > 3 cm wide 4
4 Leaf sheath plus petiole < 10 cm long; lamina apex broadly acute to rounded, base cuneate 4 Borneocola iporii
Leaf sheath plus petiole > 10 cm long; lamina apex acute to acuminate, base attenuate, cordate, rounded or truncated 5
5 Lamina lanceolate to ovate, < 7 cm wide 6
Lamina elliptic to broadly elliptic and ovate, > 7 cm wide 7
6 Basal lamina rounded to truncated; inflorescence stalk 3–9 cm long; labellum pale lilac 5 Borneocola petiolatus
Basal lamina attenuate; inflorescence stalk 1–2 cm long; labellum purplish blue 2 Borneocola biru
7 Inflorescence about 3 cm long; labellum pale pink 7 Borneocola salahuddinianus
Inflorescence > 7 cm long; labellum white 3 Borneocola calcicola

Borneocola argenteus (R.M.Sm.) Y.Y.Sam, comb. nov.

Scaphochlamys argentea R.M.Sm., Notes Roy. Bot. Gard. Edinburgh 44: 209 (1987).

Scaphochlamys depressa Mas Izzaty, A.Ampeng & K.Meekiong, Folia Malaysiana 14(2): 19 (2013).

Type

MALAYSIA. Sarawak, First Division, Lundu, near foot of Gunung Perigi, 6 Aug 1962, Burtt B2700 (holotype: E!).

Notes

It is one of the most distinctive species, either in the field or herbarium sheet. This dainty plant has a long creeping rhizome and well spaced leafy shoots, prominently stiff lateral veins raised on its adaxial lamina, both on living plants and dried specimens.

Scaphochlamys depressa Mas Izzaty, Ampeng & Meekiong is unmistakably the same as S. argentea with its prominent raised lateral veins, broadly elliptic lamina and well spaced leafy shoots. Meekiong (2015) explained that the inflorescence of S. depressa which exerted from the petiole is different from S. argentea where the inflorescence emerges from the base of the petiole. This observation is incorrect as all gingers have terminal inflorescences.

Borneocola biru (Meekiong) Y.Y.Sam, comb. nov.

Scaphochlamys biru Meekiong, Folia Malaysiana 16(1): 37 (2015).

Type

MALAYSIA. Sarawak, Kuching Division, Matang Wildlife Centre, 21 May 2014 Meekiong et al. s.n. (holotype: SAR; isotype: Herbarium, Universiti Malaysia Sarawak. Types not yet deposited as of 5 May 2016).

Notes

Borneocola biru is the most recent species described from Sarawak. It has a deep purplish blue labellum, different from all other Borneocola species which are white or in lighter shades.

Borneocola calcicola (A.D.Poulsen & R.J.Searle) Y.Y.Sam, comb. nov.

Scaphochlamys calcicola A.D.Poulsen & R.J.Searle, Gard. Bull. Singapore 57: 29 (2005).

Type

MALAYSIA. Sarawak, Kuching Division, Bau area, Gunung Tai Ton, 1°24'N, 110°8'E, 20 June 2003, Poulsen, Jugah & Clausager 2022 (holotype: SAR!; isotypes: AAU, E!, K!, L).

Notes

Borneocola calcicola is the largest amongst the Borneocola species. Poulsen and Searle (2005) observed that the distichous inflorescence is one of the characteristics of the plant. However, a recent collection of B. calcicola, Sam FRI 50290, from Seromah, Bau, showed spirally arranged floral bracts. There was a mixture of spirally and distichously arranged floral bracts in its population in Bau, Sarawak.

Borneocola iporii (Meekiong & A.Ampeng) Y.Y.Sam, comb. nov.

Scaphochlamys iporii Meekiong & A.Ampeng, Folia Malaysiana 12(1): 19 (2011).

Type

MALAYSIA. Sarawak, Kapit, Lanjak Entimau Wildlife Sanctuary, Bukit Menyarin, 3 April 2008, Meekiong MK1839 (holotype: SAR; isotype Herbarium, Universiti Malaysia Sarawak. Types not yet deposited as of 5 May 2016).

Notes

Borneocola iporii is a small ginger creeping on the humus rich forest floor. It is most similar to B. argenteus with both having a unifoliate shoot, leafy shoots far apart, broad lamina, short inflorescence and compact rachis. However, the conspicuously raised lateral veins of B. argenteus can readily distinguish it from B. iporii.

Borneocola petiolatus (K.Schum.) Y.Y.Sam, comb. nov.

Haplochorema petiolatum K.Schum. in Engler, Pflanzenr. IV, 46 (Heft 20): 90 (1904). Scaphochlamys petiolata (K.Schum.) R.M.Sm., Notes Roy. Bot. Gard. Edinburgh 44: 210 (1987).

Type

MALAYSIA. Sarawak, First Division, Mt. Singhi (= Gunung Singai), Dec 1892, Haviland 2026 (lectotype: K! designated by Searle 2010; isolectotype: E!, SAR!).

Notes

Borneocola petiolatus is distinguished by its long petiole and narrow leaves from the other species. Its lamina length is almost 3 times the width (12–21.5 × 3.1–7.1 cm). Smith (1987) found that B. petiolatus has small inflorescences as in B. argenteus. However, both can be easily separated by their leaf characters. Borneocola petiolatus has much longer petioles compared to B. argentea (12.7–31.5 cm versus 3–6 cm). Borneocola argenteus also has prominently raised lateral veins on the adaxial surface of lamina, more conspicuous on dried specimens than fresh materials. This character is lacking in B. petiolatus.

Borneocola reticosus (Ridl.) Y.Y.Sam, comb. nov.

Gastrochilus reticosa Ridl., J. Straits Branch Roy. Asiat. Soc. 44: 195 (1905). Boesenbergia reticosa (Ridl.) Merr., Bibl. Enum. Born. Pl. 122 (1921). Scaphochlamys reticosa (Ridl.) R.M.Sm., Notes Roy. Bot. Gard. Edinburgh 44: 209 (1987).

Type

Cultivated in Singapore Botanic Gardens, originally from Borneo, Sarawak, First Division, Bidi, 22 Nov 1904, Ridley s.n. (holotype: SING!).

Notes

Borneocola reticosus is chosen as the type species as it is the easiest to recognise in the genus. Its reticulate lamina readily distinguishes it from other Borneocola species.

Borneocola salahuddinianus (Meekiong, A.Ampeng & Ipor) Y.Y.Sam, comb. nov.

Scaphochlamys salahuddiniana Meekiong, A.Ampeng & Ipor, Folia Malaysiana 12(1): 22 (2011).

Type

MALAYSIA. Sarawak, Kapit, Ulu Katibas, Lanjak Entimau Wildlife Sanctuary, Bukit Sepali, 30 April 2008, Meekiong MK1856 (holotype SAR; isotype Herbarium, Universiti Malaysia Sarawak.. Types not yet deposited as of 5 May 2016).

Note

Borneocola salahuddinianus is unique amongst the Bornean species with its broadly elliptic or ovate lamina held by a long slender petiole. It is doubtful that B. salahuddinianus is a lithophyte as observed by Meekiong et al. (2011). The plants are more of an opportunist growing on humus-rich substrate accumulated on the rocks.

Borneocola stenophyllus (I.H.Ooi & S.Y.Wong) Y.Y.Sam, comb. nov.

Scaphochlamys stenophylla I.H.Ooi & S.Y.Wong, Willdenowia 44(2): 241-245 (2014).

Type

MALAYSIA. Sarawak, Kuching Division, Bau, Gunung Buan, 1°33'28.9"N, 10°08'35.2"E, 92 m, 21 Nov 2013, Ooi Im Hin & Jepom ak Tisai OIH74 (holotype: SAR. Type not yet deposited as of 5 May 2016).

Note

Borneocola stenophyllus is another new species recently discovered from Sarawak. Its grass-like leaves instantly separate it from other species in the genus.

Incompletely known species

Scaphochlamys anomala (Hallier f.) R.J.Searle, Edinburgh J. Bot. 67: 85 (2010).

Kaempferia anomala Hallier f., Bull. Herb. Boissier 6: 357 (1898). Gastrochilus anomalum (Hallier f.) K.Schum. in Engler, Pflanzenr. IV, 46 (Heft 20): 92 (1904). Boesenbergia anomala (Hallier f.) Schltr., Repert. Spec. Nov. Regni Veg. 12: 315 (1913).

Gastrochilus hallieri (Hallier f.) Ridl., J. Straits Branch Roy. Asiat. Soc. 32: 109 (1899), nom. illegit.

Type. INDONESIA. Cultivated in Bogor, originally from Liang Gagang, Kalimantan Borneo, Hallier s.n. (original material: BO, specimen lost; lectotype (designated by Searle, 2010) Figure drawn from original Hallier’s material and published as t. IX, fig. 3, Bull. Herb. Boissier 6: 357 (1898).

Notes. The type, the only specimen ever collected, was lost. However, Hallier (1898) gave a very detailed description and drawing of the plant and this has convinced Searle (2010) to place it in the genus Scaphochlamys. The drawing, which is based on the type specimen and designated by Searle as the lectotype, is the only material that gives a glimpse of the appearance of the species. In the drawing, the flower and spirally arranged floral bracts are typical of both Scaphochlamys and Borneocola. Until another specimen is collected and is available for close examination, we prefer to retain this imperfectly known species in Scaphochlamys.

Discussion

The phylogenetic analyses confirm the distinctive character of Borneocola and Scaphochlamys and their placement in the tribe Zingibereae (Figures 1, 2, 3). The Borneocola species form a monophyletic group which is sister to Myxochlamys. It is surprising to find Borneocola having a closer affinity to Myxochlamys than to Scaphochlamys, considering it shares more morphological similarities with Scaphochlamys than with Myxochlamys.

Morphologically, Myxochlamys is very different from Borneocola. There are two Myxochlamys species named so far: M. amphiloxa and M. mullerensis (Takano and Nagamasu 2007; Searle and Newman 2010) and a third undescribed species, also from Borneo. All three Myxochlamys species are very robust plants that can attain a height of 70 cm. Most Borneocola species examined so far are small-sized (not more than 50 cm tall), except for B. calcicola which can grow to 60 cm tall. Myxochlamys has 3–10 large leaves (50–60 cm long) in each shoot whereas Borneocola are unifoliate and the leaves are small (less than 20 cm long except for B. calcicola). The leaves of Myxochlamys are sessile compared to the conspicuously stalked leaves in Borneocola. The most marked difference is in the inflorescence structure. Borneocola has small inflorescences consisting of less than 15 fertile bracts but Myxochlamys has large torch-like inflorescences with easily more than 40 bracts. The bracts of Borneocola are membranous and marcescent, often measuring less than 2 cm long (except for B. calcicola measuring 2.5–3.2 cm long). By contrast, the floral bracts of Myxochlamys are coriaceous, persistent, measuring 2.5–5 cm long and most notably are covered with transparent slimy mucilage. In addition, the unique versatile anthers of Myxochlamys, a rare feature in the Zingiberaceae, are distinct from the adnate anthers in Borneocola and also from all its sister genera. Based on morphological features, Myxochlamys is more similar to Scaphochlamys, the closest being S. grandis. Both have large sessile leaves and decurrent lamina base, large, coriaceous and persistent floral bracts,their bracts being concave with reflexed and spreading apices.

Based on morphology, Borneocola is also similar to Distichochlamys. However, Distichochlamys is distinguished from Borneocola, Myxochlamys and Scaphochlamys by its unique tubular bracteoles, floral tube without a groove on the inner surface and trilocular ovary (Newman 1995). Other characteristics such as distichous floral bracts, 2-keeled bracteoles, thecae without basal spurs have been observed in the three closely allied sister genera in this study (Table 2).

Comparison between the morphological characters of Borneocola, Distichochlamys, Myxochlamys and Scaphochlamys.

Morphology Borneocola Distichochlamys Myxochlamys Scaphochlamys
Plant height to 50(–60) cm to 60 cm 70 cm to 100 cm
Number of leaf in each leafy shoot 1 1–3 3–10 1–7
Bladeless sheath Papery, drying fast Papery, decaying fast Not mentioned Coriaceous, persistent
Leaf (cm) 6–37 × 1–18; petiolate 15–28 × 8.3–14.5; petiolate 50–65 × 7–17; sessile 9–50 × 3–24; petiolate or sessile
Inflorescence height (cm) 3–11.5 to 15.5 6.5–18 4–28
Number of floral bracts 3–13 7–13 c. 40 4–44
Arrangement of floral bracts Spiral, rarely distichous Distichous Spiral Spiral, rarely distichous
Floral bracts Thin, translucent, without mucilage; drying fast Without mucilage; persistent Coriaceous, with mucilage; persistent Coriaceous, without mucilage; persistent
Flowers In cincinni In cincinni Solitary In cincinni
First bracteole Open to base, 2-keeled Tubular, 2-keeled Open to base, 2-keeled Open to base, 2-keeled
Floral tube With a groove in inner surface, glabrous to puberulent externally Without a groove in inner surface, glabrous externally With a groove in inner surface, glabrous externally With a groove in inner surface, glabrous externally
Labellum Bilobed, rarely entire, not concave; without coloured streaks beside median band Bilobed, not concave; without coloured streaks beside median band Not bilobed, entire, concave; without coloured streaks beside median band Bilobed, rarely entire, not concave; with coloured streaks beside median band
Thecae Spurs absent or with short free basal spurs Spurs absent Spurs present and long Spurs absent or with short free basal spurs
Anther Adnate Adnate Versatile Adnate
Ovary Unilocular with basal placentation Trilocular with axile placentation Unilocular with basal placentation Unilocular with basal placentation
Chromosome number 2n=10 (Šída et al., unpublished data) 2n=26 2n=28
Geographical distribution Borneo Vietnam Borneo Southern Thailand, Peninsular Malaysia, Sumatra, Borneo

Haplochorema K.Schum. is another small-sized genus endemic to Borneo, which can be mistaken for Borneocola. It has short and few-flowered inflorescences as in Borneocola but its flowers appear somewhat quadrate with the labellum and lateral staminodes held flat, more resembling Kaempferia L. Haplochorema has distichous floral bracts, single-flowered cincinni and the flowering proceeds from apex to base, to name some of the characters which distinguish it from Borneocola. In fact, the genus is more allied to Boesenbergia Kuntze than Borneocola.

Borneocola is morphologically most similar to Scaphochlamys but both can be distinguished by the texture of the bladeless sheath and floral bracts, variegation on the labellum, indumentum on the floral tube and the stigma shape. The current study recognises eight Borneocola species while S. gracilipes, S. polyphylla B.L.Burtt & R.Sm., S. limiana Meekiong & K.Yazid and S. samunsamensis Meekiong & Hidir from Borneo remain in the genus Scaphochlamys. There are no recent collections of S. gracilipes but the lax inflorescence and persistent floral bracts in the type specimens clearly distinguish it from the Borneocola species. Scaphochlamys polyphylla, S. limiana and S. samunsamensis can be readily distinguished from the Borneocola species by their papery bladeless sheath and large, green or green tinged red, coriaceous floral bracts. This shows that the distinct morphologies that separate Borneocola and Scaphochlamys are significant and are also supported by the phylogenetic analyses (Figures 1, 2 and 3). An anatomical study on the leaves also discovered some characteristics that separate Borneocola from Scaphochlamys (Norhati, pers. comm).

The morphology of Borneocola is very similar to Scaphochlamys but, combining both, necessitates synonymising Myxochlamys and possibly Distichochlamys and this will result in a very heterogenous genus. A similar situation is observed in the naming of Newmania N.S. Lý & Škorničk, a genus very similar in morphology to Haniffia Holttum but appears as its sister group in the molecular phylogenetic analyses. The authors decided against placing Newmania under Haniffia which would create a heterogenous group. The current description of Borneocola is further supported by the chromosome number with 2n=10 (Šída et al., unpublished data), different from Distichochlamys (2n=26) and Scaphochlamys (2n=28). Such significant differences in molecular data and chromosome number have conclusively supported the circumscription of the new genus Borneocola.

Key to the genera of the Zingibereae tribe in Borneo

1 Inflorescence arising directly from the rhizome on a leafless shoot 2
Inflorescence emerging at the terminal of the leafy shoot 3
2 Distinct swelling at the base of the petiole; anther with long extended crest wrapped around the style Zingiber
No swelling at the base of the petiole; anther crest short, not long extended and not wrapped around the style Haniffia
3 Flowers with versatile anther 4
Flowers with adnate anther 5
4 Inflorescence with few to many floral bracts, bracts mucilage Myxochlamys
Inflorescence with one single large floral bract, bracts not mucilage Camptandra
5 Flowers opening from top to bottom of inflorescence 6
Flowers opening from bottom to top of inflorescence 7
6 Flowers appearing quadrate with the two petaloid staminodes Haplochorema
Flowers no quadrate appearance, staminodes not petaloid Boesenbergia
7 Flowers with long narrow corolla lobes and long exserted stamens Hedychium
Flowers without such features 8
8 Floral bracts coriaceous and persistent, labellum with coloured streaks on both sides of the median band Scaphochlamys
Floral bracts thin, translucent and marcescent, labellum without coloured streaks on both sides of the median band Borneocola

Acknowledgements

The authors wish to thank the Forestry Department of Peninsular Malaysia and its State Forestry Departments, Sarawak Forestry Department, Department of Wildlife and National Parks and Johor Parks Corporation for permission to conduct research in their forests; herbaria of AAU, BKF, C, FI, E, K, KEP, KLU, PSU, SAN, SAR and SING for the loan of specimens; Lucy Chong and Julia Sang from the Sarawak Forestry Corporation, Wong Sin Yeng and Peter C. Boyce from Universiti Malaysia Sarawak, Sarawak for their hospitality and logistics help in Sarawak. We are also grateful to Kalu Meekiong from the Universiti Malaysia Sarawak, Sarawak and John Mood for the leaf samples for the molecular study; J.F. Veldkamp for advice on the genus and epithet names; Jana Leong-Škorničková, Richard C.K. Chung, Leng Guan Saw, Ruth Kiew and the reviewers for their critical comments and suggestions to improve the manuscript. This work is supported by the Malaysian Ministry of Higher Education through the Fundamental Research Grant Scheme (FRGS FP 075/2007C) and Special Research University Grant (FR 150/2007A), University of Malaya, the Ministry of Science, Technology and Innovation (Project No. 01-04-01-0000 Khas2), the Ministry of Natural Resources and Environment under the 10th and 11th Malaysian Plans (SPPII No. P23085100010021 & P23085100018003 respectively) and Grants-inAid (KAKENHI) for Scientific Research (No.26440227) from the Japan Society for the Promotion of Science.

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