Thismia mucronata Nuraliev, 2014

Nuraliev, Maxim S., Beer, Anton S., Kuznetsov, Andrey N. & Kuznetsova, Svetlana P., 2014, Thismia mucronata (Thismiaceae), a new species from Southern Vietnam, Phytotaxa 167 (3), pp. 245-255 : 246-252

Thismia mucronata Nuraliev , sp. nov. ( Fig. 1–3 ).

Thismia mucronata differs from related T. angustimitra and T. mirabilis by the presence of a mucro at the top of the convex mitre formed by appendages of the inner tepals, the absence of foveae, and the absence of interstaminal glands at the adaxial side of the anther tube. The following combination of morphological traits also characterises this species: entire margin of outer tepals, mitre white and narrower than the hypanthium, annulus almost horizontal and prominent stylar column.

Type:— VIETNAM. Lam Dong province: Bao Lam district, Loc Bac municipality, 22,2 km NNW from Bao Loc town , in the forest, not far from river, elevation ca. 1000 m a.s.l., N 11° 44’ 18’’, E 107° 43’ 22’’, 13 April 2013, M. S. Nuraliev 813 ( MW! holotype), including plants with flowers in liquid collection at Moscow University .

Plant herbaceous, terrestrial, achlorophyllous, generally glabrous ( Fig. 2 ), branching by the formation of root suckers ( Fig. 1a ); rhizomes absent. Roots few, clustered at the base of stem, vermiform, unbranched, thick, Ø 0.5 –1 mm ( Fig. 2d ). Stem erect or sometimes ascending (if growing from under forest litter), unbranched, terete and slightly angled, grayish-white, 0.4–3.5 cm tall (without terminal flower), Ø 1.3 –1.8 mm, bearing (1–)2 flowers (fig. 2b). Leaves 7–11, alternate, scattered, appressed to stem, scale-like, narrowly triangular, grayish-white, up to 7 mm long. Distal leaves up to 6 mm wide at their base, margin entire, apex acute. The leaves become crowded and smaller downwards, basalmost leaves 1 mm long. Involucral bracts 3, inserted less than 1 mm below the ovary and symmetrically arranged around it, equal, appressed to flower base, similar to upper leaves in colour and shape or slightly longer, up to 9 mm long. Flower terminal, actinomorphic, 1.2–1.7 cm long ( Fig. 1b , 3 ); if flowers more than one then the lateral flower is located in the axil of one of the involucral bracts of the terminal flower and bears its own involucral bracts. Hypanthium obconic, ca. 1.5 times higher than involucral bracts, 7–10 mm high (with ovary), ca. 6 mm wide in the upper part, with 12 veins prominent and raised outside ( Fig. 3a, b ); outer surface irregularly papillose especially along veins, dark blue and gradually becoming darker distally but with a narrow whitish collar in the upper part, veins darker than surrounding tissue; inner surface without transversal bars, fenestrate, uniformly translucent dark blue but with a light orange collar in the upper part (above the level of stamen appendages). Perianth of 6 tepals in 2 whorls attached to the hypanthium top ( Fig.3a–e ). Annulus almost horizontally covering the hypanthium to form a closed chamber, dome-shaped, fleshy, milky white, with roundish triangular orifice Ø ca. 1.5 mm ( Fig. 3f ). Outer tepals alternating with involucral bracts, broadly triangular, 1.5–2 mm long, 2–3 mm wide at their base, white and marginally translucent, margin entire, apex acuminate to rounded. Inner tepals at the same radii with involucral bracts, distally arching inward and apically broadly fused (inseparable without tearing) to form a thick convex-topped mitre ca. 1.5–2 mm high (excluding free basal tepal parts) and 4–5.5 mm wide with prominent sutures and leaving 3 broad arch-shaped apertures 3–3.5 mm wide, thick, broadly attached to annulus along its whole radius except its inner margin, basally ca. 2 mm wide, narrowed slightly above to ca. 1 mm wide and broadened towards the mitre; free parts each with marginal thickenings and with prominent dorsal median keel which continues from one of the hypanthial veins; the keels continue till the mitre top where they prolongate into 3 free erect acute pyramidal appendages 0.5–1 mm high; the appendages initially tightly appressed to each other resembling a short but distinct mucro at the top of mitre, later slightly diverging ( Fig. 2c ); foveae absent; the narrowest parts of inner tepals outside blackish blue gradually becoming greenish brown basally and white distally, mitre outside milky white except the appendages, the latter dark to pale blue and later tinged with orange to light brown, the inner tepals including mitre inside uniformly black. Stamens 6, pendulous from the annulus and broadly connected to its inner surface by short and thick filaments, ca. 4–5 mm long (fig. 3g –k); anther connectives dilated, each with median longitudinal furrow at the inner (abaxial) side (fig. 3h) and projecting far beyond thecae into apical prolongation, fused laterally along the whole length except the rounded apices to form a stamen tube with 6 narrow holes remaining between the free filaments in the base of the tube; the apical prolongations bearing skirt-like appendages at the outer (adaxial) side slightly below thecae, concave adaxially below the appendages; each appendage (fig. 1d, 3j, k) wider than stamen, 1.5 mm wide, inclined towards and reaching the connective apex, with perpendicular marginal winglike projections of lamina forming H-shaped structure which are attached to connective tissue so that proximal parts of projections triangularly attenuate and decurrent proximally to the thecae and distal parts rounded; appendages touching the inner surface of hypanthium and isolating the torus-shaped space between stamen tube and hypanthium except for 6 narrow gaps between the appendages of adjacent connectives; thecae 2 in each stamen, adaxial (facing the hypanthium) on the basal part of connective, separate, shallow, narrowly elliptic, longitudinally dehiscent, ca. 1 mm long; androecial indumentum of 3–4 papillae at the apex of each connective prolongation, stiff long needle-like hairs at the margin of appendages, and 2 rows of shorter glandular hairs on the sides of each theca (fig. 1c,d); interstaminal glands absent; stamens white except greenish blue distal portions of prolongations and translucent light orange appendages. Ovary inferior, outside not delimited from hypanthium, obconic, 2.5–3.5 mm long, 3–3.7 mm wide towards apex, flat-roofed, unilocular with 3 fusiform central placentas ( Fig. 1c ); placentas alternate with stylodia, joined at the apex and base of the loculus; ovules numerous, white; stylar column shortly cylindrical, ca. 0.5 mm long, Ø ca. 0.5 mm, dark blue; stylodia 3, ca. 2 mm below stamen apices, upright, appressed to each other, simple, rectangular, 0.8–1 mm long, bearing densely finely papillose stigmas, translucent light blue (fig. 3l). Fruit and seeds unknown.

Notes:— 1. Since there is no direct way to distinguish mature flowers from floral buds, the lowermost measurements of sizes of flower and its parts may belong to immature structures and, if so, should not be taken into account.

2. In the taxonomic literature, including the papers cited in the Introduction, the floral parts of Thismia are usually named without strict relation to the floral elements: “floral chamber” or “perianth tube” are used for hypanthium and “annulus” (= “corona”, Thiele & Jordan 2002) as an organ sui generis. In this paper, we generally follow the morphological research by Caddick et al. (2000) in the interpretation and terminology of the floral structure. As shown by these authors, the hypanthium of Thismia represents an expansion of receptacle, the annulus is a result of basal connation (probably congenital) of all six tepals, the stamens are fused postgenitally and expose their adaxial surface outside and abaxial inside.

3. A drastic change of flower coloration was observed shortly after immersing the plants into alcohol. In less than a minute, all the dark parts of the flower became intensively orange. Later, the flowers gradually became colourless.

Taxonomic relationships:— Jonker (1938, 1948) grouped Southeast Asian species of Thismia with mitre-bearing flowers (excluding Geomitra Beccari, 1877: 250 , and Scaphiophora Schlechter, 1921: 39 , which were treated as separate genera on the basis of long free or connate mitre appendages) into sect. Sarcosiphon ( Blume 1850: 65) Jonker (1938: 251). However, he also characterised this section as having coralliform underground parts. Since Thismia mucronata possesses vermiform roots, it seems to be morphologically more close to sect. Rodwaya Schlechter (1921: 38) sensu Jonker (1938), which was stated to be distributed out of Asia. A similar decision was made by Chiang & Hsieh (2011) in respect to the placement of T. huangii P.Y.Jiang & T.H.Hsieh (2011: 139) . Since Asian species of Thismia (in its current broad circumscription) with simultaneous presence of mitre and vermiform roots were not known at the time of Jonker’s work, they cannot be placed in his system with confidence (see also Chantanaorrapint 2008). Nevertheless, some of these species were already placed into sect. Sarcosiphon ( Larsen 1965, Truong et al. 2014) despite the mismatch in the type of root system. Thiele & Jordan (2002) pointed out the inadequacy of Jonker’s generic and infrageneric classification. According to Merckx & Smets (2014), who have extended the classification of Maas et al. (1986, see below), Asian species with such features should be treated within Thismia subgen. Thismia sect. Sarcosiphon , which makes this section morphologically heterogeneous and comprising species with both coralliform and vermiform roots. An exception was made for T. huangii , which was placed into sect. Rodwaya following Chiang & Hsieh (2011) due to its high similarity to T. rodwayi F. Mueller (1890: 115) and T. americana N. Pfeiffer (1914: 123) . Merckx & Smets (2014) also showed non-monophyly of a number of sections of Thismia including Sarcosiphon and Rodwaya and concluded that the current classification of Thismia does not reflect natural relationships of its species.

Within classification of Maas et al. (1986), which was developed with main attention to the Neotropics, the genus Thismia was divided into two subgenera and all species with inner tepals fused into mitre fall within subgen. Thismia . T. mucronata fits Thismia subgen. Thismia sect. Rodwaya (Schltr.) Maas & H.Maas in Maas et al. (1986: 166) in having, besides the mitre, cylindrical (i.e. vermiform) roots, terete (not bisulcate) stem with scattered leaves, anther tube, separate thecae and central placentas. These features are shared by T. mucronata and several other species of the genus including T. americana , T. angustimitra Chantanaorrapint (2008: 524) , T. clavarioides K.R.Thiele in Thiele & Jordan (2002: 766), T. huangii , T. mirabilis K.Larsen (165: 171), T. okhaensis and T. rodwayi . It should be noted that the taxonomic usefulness of the mitre was doubted ( Thiele & Jordan 2002) due to morphological heterogeneity of this structure. Furthermore, some species, such as T. abei ( Akasawa, 1950: 193) Hatusima (1976: 7) , T. gongshanensis Hong Qing Li & Y. K.Bi (2013: 25), T. taiwanensis Sheng Z.Yang, R.M.K.Saunders & C.J.Hsu (2002: 485) (see also Yang et al. 2010) and T. tuberculata Hatusima (1976: 4) , demonstrate mitre-like perianth vernation with free and imbricate (rather than fused and valvate) inner tepals. The rhizomes reported for T. clavarioides , T. huangii and several species of Thismia with free inner tepals (e.g. Chantanaorrapint & Sridith 2007, Li & Bi 2013) could possibly represent roots that bear root suckers, as it occurs in T. mucronata . The absence of rhizomes is consistent with general characteristics of the genus Thismia ( Maas et al. 1986) .

Thismia mucronata is morphologically most similar to T. angustimitra and T. mirabilis , both distributed in Thailand ( Larsen 1965, 1987, Chantanaorrapint 2008) (and probably erroneously included in key to the Malaysian species by Tsukaya & Okada 2012). It also finely resembles them in the colour palette of the flower and in the remarkable colour change when immersed into alcohol as described by Larsen (1965). For the purpose of comparison with the newly described species, we also publish here for the first time photos of T. angustimitra ( Fig. 4 ). These photos were taken by Pethch Tripetch at the type locality of this species. The new species differs from both T. angustimitra and T. mirabilis in short but prominent appendages of inner tepals which together look as a mucro at the top of the convex mitre (vs. flat-topped mitre without appendages), in the absence of foveae (vs. three foveae) and in the absence (vs. presence) of interstaminal nectariferous glands at the adaxial side of the anther tube. It also differs from T. mirabilis by a mitre that is more narrow (vs. more broad) than the hypanthium, by the horizontal (vs. erect) annulus and by the anthers fused (vs. free) at the level of thecae. Differences with T. angustimitra are entire (vs. crenate) margin of outer tepals, the prominent (vs. almost absent) stylar column, and the flower coloration including a mostly white (vs. purple to brownish) mitre. One more species, T. okhaensis , also apparently belongs to this morphologically distinct group and is characterised by uniquely large (up to 3 cm) flowers, broad mitre with glandular hairs under its top and tall erect annulus which leaves very narrow apertures below the mitre. Among Thismia species with mitre-bearing flowers, T. okhaensis appears to be most closely distributed geographically to T. mucronata with the distance between their populations about 150 km. The main morphological differences between these four species are summarized in Table 1.

Etymology:— The specific epithet “ mucronata ” is derived from the distinctive mucro at the top of the mitre, which differs this species from the most similar species Thismia angustimitra , T. mirabilis and T. okhaensis .

Distribution and habitat:— Currently only known from Lam Dong province in Southern Vietnam ( Fig. 5). The species is probably abundant at the type locality where four compact groups of up to eight above-ground shoots were found. It was also observed in a locality (N 11° 44’ 18’’, E 107° 42’ 30’’, river bank) at a distance of 1.5 km from the type locality as well as in two other places around this point. It grows amongst forest litter, along the river banks as well as in the forest not far from the river under the canopy of long-boled monsoon tropical mountain forests of middle elevation with upper storey of the canopy formed by trees belonging to families Anacardiaceae , Magnoliaceae , Sapindaceae , Dipterocarpaceae , Euphorbiaceae , Fagaceae , Theaceae , Sapotaceae , Fabaceae , Altingiaceae , Hamamelidaceae , Elaeocarpaceae , Podocarpaceae , Lauraceae , Sterculiaceae . Wet season May to October, dry season December to March, mean annual precipitation about 2000 mm. The area is also inhabited by several mycoheterotrophic species of Orchidaceae : Cephalanthera exigua Seidenfaden (1975: 71) , Epipogium roseum (D. Don, 1825: 30) Lindley (1857: 177) and Vietorchis furcata Averyanov & Nuraliev in Averyanov et al. (2013: 253).

Phenology:— In mid-April, T. mucronata was in the beginning of flowering with frequent immature above-ground shoots but no fruits or withered flowers. This is consistent with the general assumption that species of Thismia flower after rains ( Ho et al. 2009). Furthermore, the majority of the collected shoots had a single (terminal) flower in anthetic or preanthetic condition, whereas second flower in the axil of the involucral bract was severely underdeveloped and not visible without a close examination. In some (older) shoots, the lateral flower was well developed and apparently functioned normally, which indicates that the lateral flowers are not abortive (which was suggested for T. mirabilis by Larsen 1965) at least in some cases ( Fig. 2c ). Possibly, the shoots can bear more than two flowers organized into a fewflowered monochasial inflorescence (cincinnus, according to Maas-Van de Kamer 1998, Larsen & Averyanov 2007) and blooming successively. This type of inflorescence is typical for many species of Thismia . It is also highly possible that the stem elongates significantly until the end of the flowering period, and the pedicel develops, as it was described for some other species ( Chantanaorrapint 2008, 2012, Yang et al. 2002, 2010, Chiang & Hsieh 2011). The flower is initially white with blue and appearance of red or brown tinges probably indicates later flowering stages, along with diverging of appendages of inner tepals.

Flower and fruit biology:— Details of flower morphology and coloration of T. mucronata support the idea of myophily ( Stone 1980, Maas et al. 1986) and correspond with the manner of pollinator behavior hypothesized by Thiele & Jordan (2002). As the latter authors suggested, the pollinator could pass inside the hypanthium chamber through the orifice of the annulus and the stamen tube, touch the stigmas, then follow up the hypanthium wall being constrained by the stamen appendages in order to touch the thecae and leave the chamber through one of the gaps between stamen filaments and the annulus orifice. Floral biology has never been studied in the genus Thismia , but visitation by dipteran species was recorded once in T. gongshanensis ( Li & Bi 2013) . No nectar or nectaries were found in T. mucronata ; this indicates the possibility of pollination by fungus gnats deceived through brood-site imitation ( Maas et al. 1986, Maas-Van de Kamer 1998, Thiele & Jordan 2002), though pollination by pollen-eating insects cannot be excluded.

Figures

FIGURE 1. Thismia mucronata. A. Plant with flower. B. Flower, side view. C. Longitudinal section of flower. D. Part of stamen tube, detached and flattened; note papillae at connective apices, needle-like hairs at margin of appendages, and glandular hairs along thecae.All drawn from type Nuraliev 813 by A.Beer.

FIGURE 2. Thismia mucronata. A. Plants in natural habitat; note young shoots (arrows). B. Flowering plant (above-ground part). C. Shoot with anthetic terminal flower (note divergent brownish mitre appendages) and preanthetic lateral flower. D. Plants with underground parts (liquid specimen); in central plant hypanthium removed. Nuraliev 813. All photos by M.Nuraliev.

FIGURE 3. Flower of Thismia mucronata. A–C. Side view. D,E. Perianth. F. Annulus, top view (mitre removed). G. Cross section at the level of attachment of stamens. H. Longitudinal section. I. Side view with hypanthium partly removed. J. Stamen appendages, side-bottom view. K. Stamen tube, side view. L. Stylodia, top view. Nuraliev 813. All photos by M.Nuraliev.

FIGURE 4. Thismia angustimitra. A. Plants in natural habitat. B. Flowers. All photos by P.Tripetch.