A taxonomic revision of Globba subsect. Nudae (Zingiberaceae)

Globba subsect. Nudae K.Larsen is revised. Seven species are recognised and three names are lectotypifi ed. A key to the species and descriptions are provided. Three new species are described and illustrated: G. aranyaniae Sangvir. & M.F.Newman sp. nov., G. lithophila Sangvir. & M.F.Newman sp. nov., and G. macrochila Sangvir. & M.F.Newman sp. nov. Four names based on types from Bangladesh, India and Myanmar remain doubtful. The morphological expression of andromonoecy in this group is described in detail. Provisional IUCN conservation assessments of all species are supplied.


Habitat
The substrate and ecological surroundings are found to relate to plant size. Plants in G. subsect. Nudae are mostly middle-sized, about 50-100 cm tall. Occasionally G. expansa Wall. ex Horan., found in mixed evergreen montane forest, can grow to 1.5 m tall while G. lithophila Sangvir. & M.F.Newman sp. nov., which grows on limestone, is a miniature plant, only 10 cm tall. The most variable species is G. insectifera Ridl., which is large or small depending on the conditions of the dry or the rainy season which determine the production of infl orescence shoots or leafy shoots.

Rhizome
Small, globose, about 3-5 cm in diameter. In one growing season, 5-8 rhizomes can be produced in a moniliform arrangement. The root tubers are spindle-shaped or elongate and function in food storage during the dormant period.

Leafy shoots
Pseudostem consisting of enfolded leaf sheaths. At the base there are 3-5 bladeless sheaths which are usually darker. The ligule is membranaceous, truncate to bilobed, light green with paler or white margin. Normally, ligules of this subsection do not vary greatly but, in the case of G. lancangensis Y.Y.Qian, the ligule appears node-like by embracing the axis of the leafy stem. This is a diagnostic difference between G. lancangensis Y.Y.Qian and G. insectifera Ridl. All leaf blades are arranged distichously, the lowest one smallest then becoming larger towards the apex. A few species have silver striations along the midrib, for instance G. expansa Wall ex Horan. and G. lithophila sp. nov. There is almost always an indumentum on both sides of the leaf blade which may be dense on the midrib and veins above but more evenly spread below. It should be noted that G. expansa Wall. ex Horan. is the sole species having a glabrous blade above. Globba fl agellaris K.Larsen is unique as horizontal shoots protrude from the rhizome at an early stage, looking like fl agella. This characteristic is refl ected in its specifi c epithet (Larsen 1977).

Infl orescence
Terminally produced (on a leafl ess shoot in G. insectifera), erect, and lax. The overall shape is conical consisting of many cincinni arranged spirally. The main rachis and cincinni elongate greatly during fl owering. The lowest cincinnus is the longest one becoming shorter toward top of infl orescence. The rachis is rather short when it is young then may elongate with age. Bulbils may be produced on the rachis at the end of the period of growth. The cincinni are held at nearly 90º to the rachis and are subtended by green, glabrous or pubescent bracts which are very small and caducous, rarely seen on herbarium specimens. The fl owers are produced in two rows at the apex of the cincinni, each fl ower subtended by a bracteole which is usually the same shape as the bract. We recognise two morphological types of cincinnus, lax and crowded, which can be distinguished by the bracteole and fl ower scars on the cincinni. Lax cincinni may be elongate with a very short pedicel (e.g., G. expansa, Fig. 1A) while crowded cincinni may have long pedicels closely packed (e.g., G. fl agellaris and G. lithophila sp. nov., Fig. 1B).
Species in this subsection are often misidentifi ed because they show considerable similarity of habit and infl orescence structures. The fl owers, bracts and bracteoles also easily fall so most herbarium specimens look alike. In this study, the most taxonomically informative character in the key to species is the crowded or lax cincinni. This character is effective and consistent when examining herbarium specimens without fl owers but with good details on their labels. There is only one species, G. aranyaniae sp. nov. that shows both cincinnus types but their distribution areas do not overlap.

Flower
For reliable identifi cation to species, the fl ower must be seen. Flower colour seems to be a variable character while, on the other hand, the yellow and orange tone of fl owers in this subsection is clearly different and useful for classifi cation in many cases. A red or brown spot on the labellum is quite common in other groups of Globba but, in G. subsect. Nudae, G. aranyaniae sp. nov. is unique in having a spot ( Fig. 2A).

Andromonoecy
Monoecy is rare in the Zingiberaceae, having been reported in only a few species. Siphonochilus aethiopicus (Schweinf.) B.L.Burtt, an African ginger, shows gynomonoecy in which hermaphrodite and female fl owers are produced on the same plant (Gordon-Gray et al. 1989), while Alpinia sect. Monopleura K.Schum. and Alpinia sect. Myriocrater K.Schum. are considered andronomoecious with hermaphrodite and male fl owers on the same plant (Burtt & Smith 1972). Our investigations of the reproductive biology of G. section Nudae (Sangvirotjanapat et al. 2017b) show that andromonoecy occurs as a synapomorphic character of both subsections. The hermaphrodite (c) and functionally male (♂) fl owers are in the same infl orescence but on separate cincinni, c fl owers arising only on the two to four proximal cincinni. The fact that two fl oral types occur together has great taxonomic relevance because it has led earlier authors to recognise the fl ower types as different species. The differences of morphology between the fl oral types are highlighted below with an asterisk (*) and shown in Fig. 3.

Floral size*
The ♂ fl ower is smaller than the c fl ower and has a shorter fl oral tube.

Ovary and ovules*
These are strikingly dissimilar between the fl oral types. The ovary of the c fl ower is well developed, ellipsoid and longitudinally ridged with fully developed ovules inside. By contrast, the ♂ fl ower has a greatly reduced ovary about 1 mm long with aborted ovules inside.

Calyx
Infundibuliform, trilobed, two of the lobes smaller than the other, with acute or acuminate lobes. SANGVIROTJANAPAT S. et al., Taxonomic revision of Globba subsect. Nudae

Epigynous nectaries or stylodes
All species of Globba have two linear epigynous nectaries above the ovary. Nectar is secreted into the fl oral tube towards the nectar tube.

Floral tube*
A narrow tube, about 1 mm in diameter. The outer surface is pubescent. Within an infl orescence, the c fl ower has a longer and more sharply curved fl oral tube than the ♂ fl ower.

Dorsal and lateral corolla lobes
Hooded, elliptic, oblong or obovate, the dorsal one slightly bigger than the laterals. At anthesis, the lateral corolla lobes are usually concealed by the lateral staminodes or labellum but, in G. lithophila sp. nov., the lateral staminodes are rather narrow so the lateral corolla lobes can be seen clearly. The outer surface of the lobes is slightly pubescent and the colour is the same as the other parts but green tinted.

Lateral staminodes
All gingers possess staminodes derived from stamens. The tribe Globbeae is characterised by its free lateral staminodes and labellum. As for Globba, the lateral staminodes are attached above the lateral corolla lobes and are conspicuous, fl at and patent. The shape can be oblong or obovate. All these differ from other sections in which the lateral staminodes are not as prominent.

Nectar tube and labellum
We consider the labellum of Globba to be made up of two parts. The nectar tube is connected to the fl oral tube but the cavity inside it is larger. Along one side, it is fused to the fi lament. This tube holds the nectar and is the channel for the style to reach the tip of the fl ower. The apex of the nectar tube expands and refl exes to form the labellum which is always triangular, bilobed. The labellum is slightly thicker and darker than the other fl oral organs. In pollination, it serves as a landing platform and the spot may be a nectar guide indicating the position of the nectar tube where the pollinator reward is found.

Filament
Long and arching with a groove for the style in the lower part. In this paper, the measurement of the fi lament is calculated from the point of fusion with the nectar tube to the anther sac. This makes the length seem longer than is noted in the literature. Traditionally, only the part of the fi lament which extends from the labellum is measured. An approximate conversion can be made by adding or subtracting the length of the nectar tube.

Anther
Consisting of two thecae, each with loculicidal dehiscence along its entire length.

Anther appendages*
Both fl oral types have four-appendaged fl owers. The appendages of this subsection consist of an upper and a lower pair of triangular appendages. They are fused at the base while the tips are completely free from each other. Consequently, the number of appendages when looking at the base is two while, at the tip, it is four. The c fl ower has larger appendages which occupy the whole length of the anther. The appendages are deeply bifi d, and the upper pair is decurrent to the crest (Fig. 3C). The appendages of the ♂ fl ower are split half-way with their bases fused together like a swallow's tail. The anther crest is much less prominent in the ♂ fl ower than in the c fl ower (Fig. 3D). This difference in size was fi rst mentioned by Smith (1988) but she noted that the smaller crest may have been an effect of dehydration.

Style
Filiform, as long as the fl ower, the tip near the stigma held in position by the anther thecae.

Stigma*
In the c fl ower, bigger and completely full of stigmatic fl uid to promote germination of pollen tubes.

Fruit
Ellipsoid and ridged in G. subsect. Nudae, except in G. lancangensis which has nearly globose and shallowly ridged fruits. The apex of the fruit in Globba always bears a persistent calyx.

Diagnosis
The main distinguishing character within G. subsect. Nudae is the red or brown spot on the labellum. Laotian and northern Thai populations resemble G. fl agellaris and G. macrochila sp. nov. by their condensed cincinni, and orange-toned fl owers with rather broad lateral staminodes (> 5 mm). Central and eastern Thai populations resemble G. expansa by their lax cincinni, orange-toned fl owers, and ellipsoid fruits.

Etymology
The epithet 'aranyaniae' derives from 'Aranyani' who is a princess in the myth relating to the name of the type locality, Pha Nang Khoy ('Cave of the Lady who Waits').  Isotype THAILAND • Same data as for the holotype; E00726636; E.

Distribution and habitat
Laos and Thailand, at 100-700 m a.s.l., on limestone in mixed evergreen forest or near streams.

Conservation status
Least Concern. This species occurs in protected areas and suitable habitats across its range. In recent years, no major threat to this species has been reported so it is of Least Concern.

Notes
This species grows on limestone bedrock from the Louangphabang range to the Sankamphaeng range. It is the only species in G. subsect. Nudae with a spot on the labellum, which varies from red to brown. The vegetative parts of this species vary between the two main distribution areas. In Laotian and northern Thai populations, the infl orescences consist of condensed cincinni packed with bracteoles and pedicels at the tip of each cincinnus, and bulbils produced at the base of the peduncle, while, in central and eastern Thai populations, the cincinni are more elongate, and the bulbils are usually produced at the tip of the cincinni or protrude from the leaf sheaths. In eastern Thailand, the plants are found in more humid places so there may be an ecological difference between the populations but the fl oral morphology is very uniform, especially the diagnostic characters, namely the spot on the labellum and broad lateral staminodes.

Distribution and habitat
Myanmar, Laos, Thailand, 174-1350 m a.s.l., growing in mixed evergreen forest along the trail under semi shade. Usually found as dense clump.

Conservation status
Least Concern. The species occurs in a number of protected areas across its range. The species is grown in ex situ collections at two botanic Gardens (BGCI 2018).

Notes
Globba expansa is the most common species in this subsection, growing widely in northern Myanmar, Thailand, and Laos. Usually found in evergreen forest or deciduous forest, it is easily noticed by its large infl orescence with bright orange fl owers on elongate cincinni. As its distribution is wide, this species has been described twice from Myanmar and Thailand. Type specimens and living specimens at the type locality of G. yeatsiana were compared. In the case of G. expansa from Myanmar, Wallich's specimens no. 6536 are in good condition, especially no. 6536C which has a male fl ower attached to the sheet. As for G. yeatsiana from Thailand, type specimens were studied alongside living plants found predominantly at 800-1000 m a.s.l. in evergreen forest of Doi Suthep-Pui. Both specimens shared the same morphological characteristics, such as oblong to narrowly obovate lateral staminodes, labellum shape, anther appendage shape, and fl oral part ratio. As a result, G. yeatsiana is placed in synonymy under the earlier name, G. expansa.

Distribution and habitat
Chiang Mai, Mae Hong Son, and Nan provinces, Thailand, 450-1100 m a.s.l. It grows in dense populations in rather moist areas, often near streams.

Conservation status
Least Concern. Globba fl agellaris has a small area AOO of 32 km 2 and EOO of 5619 km 2 , suggesting a status of Vulnerable. As it grows in protected areas, however, as well as ex situ in Queen Sirikit Botanic Garden, it is therefore of Least Concern.

Synonyms
G. kerrii Craib, Bulletin of Miscellaneous Information, Royal Botanic Gardens, Kew 1912: 398 (Craib 1912  The type locality of each species is indicated by a bigger symbol.

Distribution and habitat
Myanmar and Thailand, 240-1500 m a.s.l. Common in dipterocarp or grass forest in open areas. The plants grow over large areas but not covering the ground densely.

Conservation status
Least Concern. Globba insectifera is fairly widespread in Thailand and Myanmar with an extent of occurrence of 77 052 km 2 . Threats to the species are mostly localized and are not of major concern. In addition, many populations grow in national parks so the species is assessed as Least Concern.

Notes
The growth pattern of G. insectifera from the dry to the rainy season was monitored at Doi Suthep-Pui, Chiang Mai province, Thailand, and the results showed that this species produces infl orescences twice a year. The fi rst infl orescences appear in the middle of summer (April to early May) with only very small leafl ets at the base. Later, infl orescences are produced terminally on the leafy shoots during the rainy season following the normal pattern of this genus. This information is useful for taxonomic treatment of this species.
Specimens collected in the dry season have been described twice as G. insectifera and G. nuda. Ridley's specimen grew spontaneously from plants collected in the Shan state, Myanmar, labelled as "Paphiopedilum bellatulum" and cultivated in Singapore Botanic Gardens. Ridley mentioned that this species had an infl orescence shoot and that its fl ower looked like a butterfl y because of its large lateral staminodes. This species was lectotypifi ed by Turner (2000) on a colour illustration deposited at Singapore Botanic Garden which we have seen. The other name, G. nuda, was described from Doi Suthep-Pui, Chiang Mai province, Thailand. Larsen diagnosed this species by its infl orescence shoot which had no leaves, giving it the specifi c epithet 'nuda', meaning without leaves. Larsen did not mention G. insectifera. We have seen the holotype of G. nuda at AAU and other specimens from Thailand. Furthermore, we have visited Doi Suthep-Pui which is the type locality of G. nuda.
As for specimens growing in the rainy season, Craib (1912) described G. kerrii from Doi Suthep-Pui which he diagnosed by its wide lateral staminodes. One of the isotype sheets at E (E00097476 and E00097477), which we have seen, has an infl orescence shoot remaining at the base of the plant. This was not mentioned in the protologue but it gives strong support for the placement of G. kerrii and G. nuda in synonymy under G. insectifera (Fig. 9A-D).

Conservation status
Least Concern. Although G. lancangensis has a small AOO of 20 km 2 and EOO of 1897 km 2 , this species occurs in the Xishuangbanna Biosphere Reserve. It may also occur in the adjoining Nam Ha reserve in Lao PDR. Surveys should be carried out to see if the species occurs in this area. The species is also in ex situ cultivation at one botanical garden (BGCI 2018).

Notes
Globba lancangensis is endemic in China. It is similar to G. insectifera in its habit, broad lateral staminodes, and labellum shape but differs by its fruit shape, the form of the leafy stem and the colour of the lateral staminodes. Sangvir. & M.F.Newman sp. nov. urn:lsid:ipni.org:names:77195004-1 Figs 2E, 6, 11-12 Diagnosis Similar to G. fl agellaris and G. macrochila sp. nov. in its condensed cincinni and bright orange fl owers, but differing from them by its clearly visible lateral corolla lobes, oblong and patent lateral staminodes, smaller size and ecological requirements, being found only in pockets of soil in cracks in limestone.

Distribution and habitat
Thailand, 450-800 m a.s.l., only found in small pockets of soil in or very near limestone.

Conservation status
Least Concern. Globba lithophila sp. nov. has a small AOO of 28 km 2 and EOO of 2600 km 2 , suggesting a status of Endangered but it grows in Lum Nam Pai Wildlife Sanctuary as well as ex situ in Queen Sirikit Botanic Garden so it is of Least Concern. It is a lithophyte which makes it sensitive to environmental factors so good management of protected areas is important to keep it in its natural habitat.

Notes
Globba lithophila sp. nov. has been compared closely to G. fl agellaris, with which it is sympatric in north Thailand. Both species were cultivated in the same place at the Zingiberaceae nursery of Queen Sirikit Botanic Garden under controlled conditions. After two years of growth, the vegetative parts of the plants were larger than those of wild plants, while the fl oral parts and ratios of sizes remained the same. We conclude that these are two separate species and that G. lithophila sp. nov. is not merely a part of the variation of G. fl agellaris.

Diagnosis
Similar to G. fl agellaris in its bright orange fl owers, but differing by its much longer labellum, 19-20 mm long (vs short labellum, 10-12 mm long) and growing in dry areas (vs moist areas).
Isotypes THAILAND • Same data as for the holotype; C, K, P.

Distribution and habitat
Myanmar and Thailand, 100-350 m a.s.l., in rather dry forest.

Conservation status
Least Concern. Although this species has a small AOO of 32 km 2 , the populations in Kanchanaburi province, where this species is commonest, are found in several protected areas. It is also grown in Queen Sirikit Botanic Garden.

Notes
Usually found in somewhat dry areas, such as bamboo forest. The labellum is remarkable, being longer than the lateral staminodes. It always covers the lateral corolla lobes. Plants were cultivated under more humid test conditions in Bangkok to fi nd out the stability of the morphological characters. After growing for one season, the environmental factors affected only vegetative structures, i.e., leafy stem size, infl orescence size but did not infl uence the ratios of the fl oral parts.

Notes
Collett & Hemsley placed G. subscaposa in G. sect. Ceratanthera (Horan.) Petersen because it has two anther appendages but the description in the protologue and the appearance of the type convince us that it belongs in G. subsect. Nudae. Dissection of a fl ower on the type shows that it is morphologically similar to G. insectifera by the shape of the anther appendages of a functionally male fl ower and its broad lateral staminodes but it differs by its rather clump-forming habit (not tending to grow as solitary shoots), and densely villous indumentum on the leafy stem and infl orescence (vs glabrous to minutely pubescent).

Discussion
Of the fourteen validly published species names in G. subsect. Nudae, seven are accepted while three are placed in synonymy. The characteristics, distribution ranges and habitats of these species have been clarifi ed and a key to their determination has been provided. Four doubtful species cannot be further defi ned until exploration at their type localities can be carried out.
All species are assessed as of least concern using IUCN conservation status criteria, although some species have a small area of area of occupancy (AOO) and extent of occurrence (EOO) suggesting a higher degree of threat. These grow in protected areas and botanical gardens so the threats to them are thought not to be serious in the immediate future.