Argostemma Cordatum (Rubiaceae), a New Species from Vietnam

Phytotaxa 317 (1): 042–052 ISSN 1179-3155 (print edition) http://www.mapress.com/j/pt/ PHYTOTAXA Copyright © 2017 Magnolia Press Article ISSN 1179-3163 (online edition) https://doi.org/10.11646/phytotaxa.317.1.4

Argostemma cordatum (Rubiaceae), a new species from Vietnam

MAXIM S. NURALIEV1,2, ANTON S. BEER2, ANDREY N. KUZNETSOV1,3 & SVETLANA P. KUZNETSOVA1 1Joint Russian-Vietnamese Tropical Scientific and Technological Center, Cau Giay, Hanoi, Vietnam. e-mail: [email protected] 2Department of Higher Plants, Biological Faculty, M.V. Lomonosov Moscow State University, 1, 12, Leninskie Gory, 119234 Moscow, Russia. 3A.N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences, Leninsky 33, Moscow, Russia.

Abstract

Argostemma cordatum, a new species of Rubiaceae, is described and illustrated. The species was discovered in 2014 during a botanical survey of the Chu Yang Sin National Park (Dak Lak province, Southern Vietnam). Argostemma cordatum pos- sesses a solitary large leaf per plant (along with one very small leaf). The new species differs from morphologically similar species mainly by the small size of the enlarged leaf and cordate base of the enlarged leaf. It is also characterized by the following features: plant completely glabrous, stipules minute and reduced to papillate warts, inflorescence with all axes elongated, anthers coherent into anther cone and dehiscent by longitudinal slits, style slightly exserted. An extended description of the vegetation in the area inhabited by A. cordatum is provided.

Keywords: Argostemma, taxonomy, Southern Vietnam, Chu Yang Sin National Park, flora, biodiversity

Introduction

The herbaceous genus Argostemma Wall. in Roxburgh (1824: 324) belonging to Rubiaceae comprises around 100 (Ridley 1927, Puff et al. 1995, 2005, Mabberley 2008, Chen et al. 2011) or up to 220 (Bremer 1989) species. Two of its species are endemic to West Africa, while the rest of its diversity is confined to South, East and Southeast Asia (Chen et al. 2011). The highest number of species of Argostemma is found in the Malay Peninsula and on Borneo (Sridith & Puff 2000). Thus, the genus shows mostly paleotropical distribution with some representatives in the Northern subtropics. Species of Argostemma typically inhabit wet, shady areas of primary (undisturbed) evergreen forests, e.g. moss-covered rock faces, stream banks and surroundings of waterfalls (Sridith & Puff 2000, Puff et al. 2005, Sridith 2007). In Vietnam, six species of Argostemma are currently recognized. Five of them are listed in the most recent accounts (Pham Hoang Ho 2000, Tran Ngoc Ninh 2005, Choudhary et al. 2013). One more species, A. annamiticum Ridley (1927: 40) endemic to Vietnam is accepted by Govaerts et al. (2017) and probably overlooked in the accounts cited above. Here, we report a new species discovered recently in Southern Vietnam, which brings the number of species recorded in this country to seven.

Material & Methods

The new species was collected during an expedition of the Russian-Vietnamese Tropical Centre in the Chu Yang Sin National Park, Dak Lak province, Vietnam, in May 2014. The description and drawings are based on herbarium collections and photographs of living plants. The measurements were performed on dried plants, using a ruler, and also using a vernier calliper under a dissecting microscope (Olympus SZX7) for small parts of the plants. In the morphological description, mean values are given in square brackets after ranges of variation of quantitative characters. These data are based on measurements of 13 individuals all of which bear inflorescences. The information on herbarium collections examined during this study is provided in the Appendix.

42 Accepted by Axel Arriola: 27 Jul. 2017; published: 11 Aug. 2017 Taxonomy

Argostemma cordatum Nuraliev, sp. nov. (Fig. 1–3). Argostemma cordatum is characterized by a single large leaf per plant and differs from all other species of the genus with this feature by the small size of the whole plant (particularly the large leaf, which is 2.6–4.7 cm long) and invariably cordate base of large leaf. This species also differs in the following combination of morphological traits: plant completely glabrous, stipules minute and represented by papillate warts, inflorescences with all axes (peduncle and pedicels) elongated, anthers basifixed, coherent into anther cone and dehisce by longitudinal slits and a style slightly exserted. Type:—VIETNAM. Dak Lak province: Lak district, Bong Krang municipality, Chu Yang Sin National Park, 11 km SSE of Krong Kmar village, in mixed forest, elevation ca. 1250 m a.s.l., N 12° 24’ 53’’, E 108° 22’ 56’’, 22 May 2014, M.S. Nuraliev, A.N. Kuznetsov, S.P. Kuznetsova 960 (holotype MW0595623).

Plant epilithic, herbaceous, perennial, completely glabrous (Fig. 1a, 2a). Tuber ca. 6 mm in diam. in sicco, bearing several buds each with 5 pairs of cataphylls (Fig. 1b). Roots adventitious, attached at base of aerial stem (in cataphyll- bearing nodes) as well as at tuber surface, dense, much-branched, with small nodules. Stem erect, unbranched, 2.2–5.6 [4.0] cm long (Fig. 2b, 3a,b), sometimes with 2 opposite foliaceous scales 1.3–2.5 [1.7] mm long and 0.7–1.0 [0.9] mm wide inserted at 1.1–4.0 [2.0] cm from stem base (Fig. 1a). Stipules minute, each of 2 represented by a wart covered by several papillae, whole structure less than 0.5 mm (Fig. 1c). Leaves opposite, in 1 pair, strongly anisophyllous, sessile. Large leaf always pointing down and inflorescence inclined towards it, with anthetic flowers facing the leaf. Large leaf ovate, 2.6–4.7 [3.8] cm long, 1.4–2.5 [1.9] cm wide, with 4–5(6) pairs of secondary veins, margin entire, apex acuminate to attenuate, base cordate (Fig. 2c); small leaf usually overlapping the large leaf, narrowly to broadly ovate, 2.5–11.8 [3.9] mm long, 1.8–7.7 [2.8] mm wide (Fig. 1c). Inflorescence single, terminal, dichasial with all axes elongated, unbranched to 2 times branched (sometimes unevenly), 1–5-flowered (or probably more) (Fig. 2d, 3c). Peduncle 5–20 [14.3] mm long; bracts on primary axis (= bracteoles of first order flower, single pair) green, 1.4–2.7 [2.0] mm long, 0.5–1.2 [0.9] mm wide; bracts on secondary axes much smaller. Pedicel 3.3–8.0 [5.2] mm long. Flower actinomorphic, 5-merous (except the gynoecium). Calyx shorter than corolla tube (not visible from above), green, with short tube and broadly triangular lobes ca. 0.5 mm long (Fig. 2d, 3d). Corolla broadly rotate (star-shaped), white with pale green area at base of the tube; corolla tube short, ca. 1 mm long; corolla lobes triangular-ovate, conspicuously 3- nerved at base, 3.5–5.2 [4.5] mm long, 2.0–2.5 [2.2] mm wide (Fig. 2e,f, 3e). Stamens inserted at base of corolla tube. Filaments free, tightly appressed to each other (much thinner and loose in sicco), straight, ca. 1 mm long. Anthers fused to each other postgenitally by lateral margins (forming an anther cone), basifixed, oblong with straight base, 2.9–3.5 [3.1] mm long, introrse, dehiscent by longitudinal slits, without apical appendages (sterile prolongations less than 0.3 mm long) (Fig. 1d, 2f, 3e,f). Filaments pale green, anthers light yellow at base gradually becoming white towards apex. Ovary inferior, 2-locular, 0.5–1 mm long, ca. 1 mm wide; style slightly exserted from stamens (for 0.5–0.8 [0.6] mm), filiform, 4.5–5.5 mm long; stigma globose. Fruit and seeds unknown. Notes:—1. The whole genus Argostemma is often characterized by possessing perennial habit due to the presence of rhizomes or tubers (Sridith 1999a, Puff et al. 2005, Tanaka et al. 2010, Choudhary et al. 2013). However, in the descriptions and drawings of some species, including those similar to A. cordatum (e.g. Sridith 1999b, 2009, 2012), no such long-lived (perennial) shoots are shown, and all the roots are attached to the annual stem. According to our observations of A. cordatum, the annual stem occupies lateral position on the tuber, and probably can be easily detached from it. Indeed, in our material most of the plants lack the tuber, and we suppose that it was the result of inaccurate collecting. In other species, similar reasons could lead to the apparent absence of perennial basal part of plants. The precise structure and branching pattern of the tubers in A. cordatum and its congeners remain unknown. 2. It is remarkable that in Argostemma cordatum the appearance of stamen filaments differs substantially in living and dried plants. It is possible that this effect takes place in some other species of the genus, and filaments described and illustrated as not touching each other are in fact tightly appressed, with the style not visible between them. Taxonomic relationships:—Argostemma cordatum belongs to a morphologically distinct group of species which is characterized by strong anisophylly combined with presence of a single pair of stem leaves (or sometimes two pairs). As a result, these species possess a single large leaf in each plant, the other leaf (or three others) being minute and often stipule-like (see also Puff 2009). The other species from this group are A. humile, A. kurzii, A. monophyllum, A. phyllocharis, A. siamense, A. tenue, A. unifolioloides (often misspelt as “unifolioides”), A. unifolium (Ridley 1915, 1923, 1927, Sridith 1999a, 1999b, 2009, 2012, Puff 2009) and a poorly known species A. begoniaceum Miquel (1857: 348) from Java (Ridley 1927). The main morphological differences between species of this group are summarized in Table 1.

Argostemma cordatum, a new species from Vietnam Phytotaxa 317 (1) © 2017 Magnolia Press • 43 FIGURE 1. Argostemma cordatum. A. General view of a plant with 1-flowered inflorescence. B. Tuber with roots, buds and annual shoot. C. Node with large leaf base, small leaf and stipules. D. Flower, longitudinal section. All drawn from type Nuraliev, Kuznetsov, Kuznetsova 960 by A.Beer.

44 • Phytotaxa 317 (1) © 2017 Magnolia Press NURALIEV ET AL. FIGURE 2. Argostemma cordatum at type locality. A. General view of population. B. Flowering individual. C. Individual with 1-flowered inflorescence, view in plane of large leaf. D. Dichasium with flower buds. E, F. Flower, apical and oblique view. Nuraliev, Kuznetsov, Kuznetsova 960. All photos by M.Nuraliev.

Argostemma cordatum, a new species from Vietnam Phytotaxa 317 (1) © 2017 Magnolia Press • 45 FIGURE 3. Argostemma cordatum at second recorded locality. A, B. General view of a plant, showing its orientation relative to the ground. C. Twice branched inflorescence. D. Flower, view from below showing calyx and ovary. E. Flower, side view. F. Close-up of anther cone. All photos by M.Nuraliev.

A. tuberous, large (8)12.7–22.9 cm 5–6 or around 9 cordate to narrowed (broadly cuneate) up to 2.5 cm or almost absent similar to small leaf panicle of umbel- like cymes unknown unknown unknown not exserted Peninsular Malaysia A. unifolioloides tuberous, large 7.6–25 cm 9–14 round to cordate absent similar to small leaf but narrower panicle of umbel- like cymes unknown unknown by longitudinal slits not exserted Peninsular Thailand, Peninsular Malaysia A. tenue tuberous, very small 5–14 cm 10 cuneate 2.5 mm or absent unknown panicle of umbel-like cymes unknown unknown unknown unknown Peninsular Malaysia A. siamense absent (at drawing) 4.5–14 cm several (8–12) acute or cuneate subobsolete ca. 1–8 × 0.5 mm, ovate umbel-like or sometimes ± lax free coherent into anther cone by longitudinal slits exserted for ca. 1–1.5 mm Thailand, Laos A. phyllocharis absent (at drawing) 8–10 cm several (8 in drawing) acute to slightly cordate absent 3–5 × 4 mm, elliptic- ovate umbel-like fused around middle free, connivent into cone-like structure by apical pores slightly exserted (for ca. 0.5 mm) Thailand Northern and similar species, and their geographical distribution. The characters of previously described A. monophyllum tuberous, small 2–13 cm 4–5 rounded or acuminate absent unknown umbel-like or nearly so free free by apical pores unknown India Argostemma Argostemma cordatum A. kurzii absent (at drawing) 5–16 cm several (7–9) round to cordate absent or present ca. 1 × 2–5 mm, oblong or elliptic-ovate umbel-like free free, connivent into cone-like structure (but stated as separated by Sridith 2012) by apical pores long exserted (for 2–4 mm) Thailand Myanmar, (from Northern to Peninsular) A. humile unknown 4–5 cm 5 narrow very short or almost absent small, ovate umbel-like free free by apical pores unknown Peninsular Malaysia (Penang) A. cordatum tuberous 2.6–4.7 [3.8] cm 4–5(6) cordate absent minute (papillate warts) all axes elongated free coherent into anther cone by longitudinal slits slightly exserted (for 0.5–0.8 [0.6] mm) Vietnam Morphological differences between Characters Rhizome Length of large leaf Number of secondary vein leaf pairs in large leaf Base of large Petiole of large leaf Stipules Inflorescence (dichasium) Stamen filaments Anthers Anther dehiscence Style Geographical distribution TABLE TABLE 1. & Lanorsavanh (2006), Chayamarit & Puff 2012), 2009, (1999b, Sridith 1927), 1925, 1923, (1915, Ridley (1903), Gamble & King (1880), Hooker from taken are species Chantaranothai (2013) and from specimens studied.

Argostemma cordatum, a new species from Vietnam Phytotaxa 317 (1) © 2017 Magnolia Press • 47 Argostemma cordatum differs from the above-mentioned related species by the smaller sizes of the whole plant and particularly the enlarged leaf. Furthermore, A. cordatum is distinctive in possessing an invariably cordate base of the large leaf, whereas the large leaf of all other species shows an acute, cuneate or rounded base in all or some of the individuals. Other important features of A. cordatum are: plant completely glabrous, stipules minute and reduced to papillate warts, all inflorescence axes elongated (not umbel-like), anthers basifixed, coherent into anther cone and dehiscent by longitudinal slits, style slightly exserted. It should be noted that comparison of species from this group is complicated by the scarcity of illustrations of flower morphology: for most of them, including observed in recent years, photographs are not provided, and drawings are hardly informative, most probably prepared on the basis of dried material. At the same time, descriptions are too complicated and sometimes controversial. For instance, Sridith (2009) stated anthers of A. kurzii to be connivent into a cone-like structure, while later he described this species as having separated free stamens and opposed it to the species with anthers connivent or coherent into a cone-like structure (Sridith 2012). Etymology:—The specific epithet “cordatum” refers to the prominently cordate base of large leaf which distinguishes the new species from its relatives. Distribution and habitat:—Argostemma cordatum is currently only known from Dak Lak province in Southern Vietnam (Fig. 4), where it occurs in large populations in areas with appropriate habitats. It is found at elevation from 950 to 1250 m a.s.l., in forests (including shady stream banks) and inhabits vertical granite rock surfaces covered by mosses. The type specimen was collected on slopes covered by polydominant mixed tropical mountain forest of middle elevation, characterized by a well-developed hydrological network. Granite rocks up to 2 m in diam. are common on the surface. The forest stand can be subdivided into three stories of which upper and lower ones are well developed. Trees of the first forest stratum are 20–22 m (up to 24–26 m) high, with trunks 40–70 cm DBH; canopies 2–4 m in diam., approaching each other but not overlapping. Trunks are covered by mosses from base to 4–7 m height. Apart from the location of the holotype, A. cordatum was observed in several other places at a distance of up to 5 km from it. One of them (N 12° 23’ 50’’ E 108° 21’ 00’’, 1100 m a.s.l., see Fig. 3) is very close to the type locations of three other recently described species (Averyanov et al. 2013, Nuraliev et al. 2015, Wood et al. 2017). In these publications, extended data on forest composition in this area are provided. Phenology:—The plants observed in late May showed open flowers and numerous flower buds. In some individuals, inflorescences were considerably underdeveloped. Thus, the very beginning of flowering probably takes place in this season. As the inflorescence is dichasial, it can possibly develop subsequent branches of several higher orders after the first flower opens, and bear more flowers than indicated above. We therefore suppose that the flowering time is at least May–June.

Discussion

Terminology of stamen morphology in Argostemma The genus Argostemma shows considerable diversity of androecium structure which implies a degree of stamen union (most probably, exclusively postgenital), modes of anther dehiscence and presence or absence of apical appendages (Puff et al. 1995). In respect to the stamen union, Sridith (2007) indicated two kinds of androecium: with “anthers coherent in a cone-like structure (anther cone)” and with “free stamens”. This is consistent with the generic description given by Bremer (1989): stamens “coherent into an anther cone or free; if coherent then fused along the whole anther or partially so”. However, in a later paper Sridith (2009) described the stamens of A. kurzii as free with “anthers connivent into a cone-like structure”, which brings a new meaning to the term “cone-like structure” (now contrasting the anther cone, instead of being synonymous to it) and represents a third condition of the stamen arrangement. Moreover, A. phyllocharis is stated to possess “filaments fused around the middle of the length and forming a short filament tube” and “anthers free, connivent into a cone-like structure” (Sridith 2012). From this description it is evident that the presence or absence of filament fusion should be regarded as a separate feature. For the purpose of clearer understanding of morphological terms, we propose (and use here) the following expanded classification of stamen arrangement in Argostemma: 1. Filaments are (a) free or (b) fused. 2. Anthers are (a) free and loosely arranged (separated), (b) free and connivent into a cone-like structure or (c) fused (= coherent) into an anther cone.

We are grateful to D.D. Sokoloff for consultation on botanical Latin, to I.A. Savinov and I.A. Schanzer for digitizing some of the literature sources and to Sally Dawson for searching for the type specimens in K. Sarah Sigsworth and Suzanne Cubey are acknowledged for taking images of the specimens in E. The work of MSN and ASB was carried out in accordance to Government order for the Lomonosov Moscow State University (projects No. AAAA-A16- 116021660105-3 and АААА-A16-116021660045-2 correspondingly).

References

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APPENDIX

A list of herbarium collections examined, all of them accessed online.

Argostemma humile Benn. in Bennett et al. (1838: 94): Malaysia, Penang, W. Jack 8391 (K001125372). A. kurzii C.B.Clarke in Hooker (1880: 45): Myanmar, Paungdaw, 08.1961, J. Keenan, U. Tun Aung, R.H. Rule 723 (E00038577); Myanmar, Paungdaw, 08.1961, J. Keenan, U. Tun Aung, R.H. Rule 823 (E00038576); Myanmar, Paungdaw, 08.1961, J. Keenan, U. Tun Aung, R.H. Rule 5352 (E00038578); Myanmar, Moulmein, 1839, Parish 62 (type: K000031021); Thailand, Phang Nga, Mueang Phang-nga, 11.06.2005, Saithip, K. Sridith, K. Maneenoon 45 (E00209568). A. monophyllum Ridley (1927: 27): India, 18.06.1850, J.D. Hooker, T. Thomson 1099 (type: K000031018); India, J.D. Hooker, T. Thomson s.n. (types: E00038580, L0043126, L2849753, probable syntype: NY00130865); India, Khasya Hills, 10.1835, Griffith 2873 (probable syntype: NY00130866). Specimens from India stored under a doubtful name “A. humile Wall.”, which most probably belong to A. monophyllum (see Ridley 1927): J.D. Hooker, T. Thomson s.n. (P04009695, P04009696, P04935705); Griffith 2874 (P04009694). A. siamense Puff (2009: 139): Thailand, Uttaradit, Klong Dtrong (Tron) National Park, 16.10.2005, J.F. Maxwell 05- 590 (L4193147); Thailand, Loei, Phu Luang, 19.08.1966, S. Phusomsaeng, K. Bunchuai 8 (isotype: K001067590); Thailand, Loei, Phu Luang, 24.06.1968, K. Bunchuai 1683 (paratype: L2058261); Thailand, Loei, Phu Kradueng, 15.10.1967, P. Sangkhachand 1037 (L2058260); Thailand, Nakhon Phanom, Phu Langka National Park, 29.07.2008, R. Pooma, P. Karaket, N. Pattharahirantricin, U. Kawatkul 7276 (L4215884); Thailand, Nakhon Ratchasima, Khao Lotung, 09.08.1968, K. Larsen, T. Santisuk, E. Warncke 3173 (paratype: E00038618, L2058262); Thailand, Nakhon Nayok, Khao Yai National Park, 07.09.2006, R. Pooma, K. Phattarahirankanok, S. Sirimongkol 6267 (L4200198); Thailand, Chonburi, Chan Ta Then falls, 17.08.1974, J.F. Maxwell 74-815 (paratype: L2058263); Thailand, Chonburi, Ang Chang Nam, 02.09.1975, J.F. Maxwell 75-971 (paratype: L2058264). A. cf. siamense: Cambodia, border of Kampong Speu and Kampot, 13.06.1930, E. Poilane 17600 (P00077329). A. tenue Ridley (1915: 39): Peninsular Malaysia, 16.09.1913, H.C. Robinson s.n. (lectotype: K000172891); Peninsular Malaysia, H.C. Robinson s.n. (isotype: P00077341). A. unifolioloides King in King & Gamble (1903: 148) var. glabra King in King & Gamble (1903: 148): Thailand, Satun, Thale Ban National Park, 09.09.2010, D.J. Middleton, K. Bunpha, P. Karaket, S. Lindsay, T. Phutthai, S. Suddee, N. Tetsana 5347 (E00596941); Thailand, Narathiwat, Sungai Padi, 18–19.10.1970, Ch. Charoenphol, K. Larsen, E. Warncke 3978 (P04009640); Malaysia, Perak, Maxwell Hill, 09.09.1949, J. Sinclair 6019 (E00038592);

Argostemma cordatum, a new species from Vietnam Phytotaxa 317 (1) © 2017 Magnolia Press • 51 Malaysia, Perak, Maxwell Hill, 16.09.1949, J. Sinclair 6160 (E00038591); Peninsular Malaysia, 08.1888, L. Wray 2814 (paratype: K000172899); Malaya, B. Scortechini 384 (lectotype of A. unifolioloides: K000172887); Malaya, B. Scortechini 412 (paratype: P04009639). A. unifolium Benn. in Bennett et al. (1838: 94): Malaysia, Penang, 1831, J.D. Hooker s.n. (E00038572); Malaysia, Penang (Prince of Wales Island) (E00038585). A. unifolium var. sessile Ridley (1925: 315): Peninsular Malaysia, Kedah Peak, 08.12.1915, H.C. Robinson, C.B. Kloss 6116 (type: K000172865).

The isotype of A. phyllocharis Sridith (2012: 85) is absent from K (Sally Dawson, a curator in K, pers. comm.) though stated to be deposited there (Sridith 2012).