Thismia hongkongensis S.S.Mar & R.M.K.Saunders, 2015

Mar, Shek Shing & Saunders, Richard M. K., 2015, Thismia hongkongensis (Thismiaceae): a new mycoheterotrophic species from Hong Kong, China, with observations on floral visitors and seed dispersal, PhytoKeys 46, pp. 21-33 : 22-26

Thismia hongkongensis S.S.Mar & R.M.K.Saunders sp. nov. Figs 1, 2, 3, 4

Diagnosis.

Similar to Thismia brunonis Griff., but differing in bearing a maximum of only three flowers (with a single flower at anthesis), and having a dark red perianth tube with the filiform appendages on the outer tepals remaining upright and forming a loose mitre over the annulus, longer staminal filaments with two distinct teeth at connective apex, and rounded stigmas.

Type.

China: 22°25'N, 114°11'E, Tai Po Kau Nature Reserve, New Territories, Hong Kong, 19 May 2014, S.S. Mar 1 (holotype: HK, in spirit).

Description.

Small achlorophyllous holomycotrophic herbs. Roots clustered, ± horizontal, vermiform, fleshy, 1.2-1.3 mm in diameter, cream-coloured. Stem cream-coloured, unbranched, erect, ca. 1.7 cm tall, 1.8-2 mm in diameter, glabrous, terete, with ca. 12 longitudinal ridges. Leaves white, appressed, clasping stem, narrowly triangular with acute apex, scale-like, 3-5.5 mm long, 1.7-2 mm wide; basal leaves smallest, upper leaves (equivalent to floral bracts) largest. Flowers in clusters of up to 3, developing sequentially with only one anthetic. Perianth actinomorphic, of 6 fused tepals, forming a perianth tube with free apical lobes. Perianth tube pinkish-white, membranous, urceolate, ca. 6.7 mm long, ca. 6.1 mm in diameter, with 12 dark red vertical ribs, abaxial surface distinctly verrucose; apex of perianth tube fused to form a dark red, rounded-hexagonal annulus, ca. 1.4 mm wide (top, externally), ca. 2.3 mm wide (base, externally) and ca. 1 mm (internal aperture); dark red, inverted V-shaped structures (putative nectaries) at apex of adaxial surface of perianth tube, opposite apertures between staminal filaments. Outer tepal lobes triangular, ca. 1.8 mm long, ca. 1.5 mm wide at base; inner tepal lobes spathulate, concave adaxially, ca. 3.3 mm long, ca. 1.7 mm wide at widest point, bearing a dark red filiform appendage on the abaxial surface, ca. 4 mm long, ca. 0.5 mm in diameter (towards base), 0.4 mm in diameter (towards apex); the three filiform appendages remain upright and cross each other, forming a persistent mitre. Stamens 6, pendent from the inner margin of perianth annulus, ca. 2.9 mm long, ca. 1.1 mm wide at widest point; filaments free, ca. 1 mm long; stamens laterally connate, forming an anther tube; individual stamens with two thecae (adaxial, dehiscing towards inner surface of perianth tube), ca. 0.7 mm long; apical connective of stamens ca. 1 mm long, with two distinct teeth, adorned with trichomes, ca. 0.5 mm long. Ovary inferior, obconical, ca. 2.7 mm long, ca. 4 mm wide towards apex; style ca. 0.6 mm long, ca. 0.6 mm in diameter, with three bilobed, rounded stigmas; stigmatic head ca. 1 mm long, ca. 1 mm in diameter. Fruit a capsule ca. 4 mm long, ca. 4.8 mm wide, cup-shaped, carnose, pale orange-brown, dehiscing apically; fruiting peduncle ca. 2.5 mm diameter. Seeds numerous, yellow-brown.

Phenology.

Flowering was observed between May and September. Flower development extends over several weeks (Fig. 1C-H). Based on our field observations, mature flowers are functional for up to three weeks, with up to three flowers developing successively in each individual (Fig. 3A). The perianth tube abscises after fertilization (Fig. 1I, J), with a clear abscission zone (ab in Fig. 2A); the epidermis on the upper surface of the carpel subsequently disintegrates and the stigma is shed, exposing the seeds (Fig. 3A, D). Fruiting was observed between June and October.

Distribution and habitat.

Thismia hongkongensis is only known from the type locality in Hong Kong. The habitat is lowland secondary forest (west-facing slope, ca. 240 m above sea level); the site is not close to a stream and is therefore likely to dry out during periods of low precipitation. Cooccurring species include Adiantum flabellulatum L. ( Adiantaceae ), Ardisia quinquegona Blume ( Myrsinaceae ), Breynia fruticosa (L.) Hook.f. ( Euphorbiaceae ), Burmannia wallichii (Miers) Hook.f. ( Burmanniaceae ), Clematis meyeniana Walp. ( Ranunculaceae ), Cratoxylum cochinchinense (Lour.) Blume ( Clusiaceae ), Desmos chinensis Lour. ( Annonaceae ), Diplospora dubia (Lindl.) Masam. ( Rubiaceae ), Garcinia oblongifolia Champ. ex Benth. ( Clusiaceae ), Lindsaea orbiculata (Lam.) Mett. ex Kuhn ( Lindsaeaceae ), Lophatherum gracile Brogn. ( Poaceae ), Lygodium japonicum (Thunb.) Sw. ( Lygodiaceae ), Machilus chekiangensis S.K.Lee ( Lauraceae ), Psychotria asiatica L. ( Rubiaceae ), Psychotria serpens L. ( Rubiaceae ), Rourea microphylla (Hook. & Arn.) Planch. ( Connaraceae ), Sarcandra glabra (Thunb.) Nakai ( Chloranthaceae ), and Sciaphila ramosa Fukuy. & T.Suzuki ( Triuridaceae ).

Etymology.

The specific epithet reflects the geographical origin of the species in Hong Kong.

Additional specimens examined

(paratypes). China. Hong Kong: 22°25'N, 114°11'E, Tai Po Kau Nature Reserve, New Territories, 29 May 2014, S.S. Mar 2 (HK, dissected flower in spirit); idem, 2 October 2014, S.S. Mar 3 (HK, immature fruit in spirit).

Discussion.

Thismia hongkongensis is most similar to Thismia brunonis Griff. ( 1844, 1845; as ' Thismia brunoniana ' in the latter), the type species in the genus. Thismia brunonis is only known from a single collection from Tenasserim in Myanmar, dating from October 1834. According to Jonker’s (1938) supraspecific classification of the genus, both species would be included in sect. Thismia (' Euthismia ') subsect. Brunonithismia Jonker as they have unequal and free tepal lobes. Comparison of the two species reveals several significant differences, however, including flower number per inflorescence. The protologue of Thismia brunonis includes reference to flowers clustered in a terminal raceme ("Flores pauci, in racemum brevem terminalem dispositi": Griffith 1845: 341) with the accompanying illustration in the same publication (Fig. 1 in Pl. XXXIX) showing inflorescences with four and six flowers; Jonker (1938) subsequently described the species as bearing 3-8 flowers per raceme. In contrast, Thismia hongkongensis invariably has fewer flowers, with a maximum of three per inflorescence, reaching anthesis consecutively. The perianth tube of Thismia brunonis is pale yellow with red ribs ( Griffith 1845), whilst it is pink with red ribs in Thismia hongkongensis (Figs 1G-J, 2A, B). The filiform appendages on the outer tepals of Thismia brunonis appear to be spreading at maturity ( Griffith 1845: Pl. XXXIX), whereas those of Thismia hongkongensis invariably remain upright and cross each other to form a loose mitre over the annulus (Figs 1G-J, 2A, B, 4A). Thismia brunonis also differs from Thismia hongkongensis as it has a much shorter filament: although a measurement was not included in Griffith’s descriptions of Thismia brunonis , the accompanying plate ( Griffith 1845: Fig. 7 in Pl. XXXIX) indicates that it is considerably shorter than the rest of the stamen. The shape of the stigma lobes also differs: it is acute in Thismia brunonis ( Griffith 1845: Fig. 9 in Pl. XXXIX; Jonker 1938), but rounded in Thismia hongkongensis (Fig. 4D).

Thismia hongkongensis is strikingly different from its congener in Hong Kong. Thismia tentaculata has a white perianth tube with a bright yellow annulus, and three divergent orange-red filiform appendages on the inner tepals ( Ho et al. 2009).

IUCN conservation status.

CR D ( IUCN 2001). Only one population is known, consisting of ca. 10 individuals, covering an area of approximately 4-5 m2. The population is located within the Tai Po Kau Nature Reserve, but is close to a major hiking path and the population is therefore susceptible to human disturbance and vegetation clearance.

Pollination ecology

Although the Burmanniaceae s.l. (inclusive of Thismia ) are reported to be protandrous ( Vogel 1998), this inference was based on a paraphyletic circumscription of the family and it is unclear whether protandry has specifically been observed in Thismia . Dissections of late-anthetic flowers of Thismia hongkongensis allow tentative confirmation of protandry, however, as the thecae are completely devoid of pollen (th in Fig. 2C).

Little is known of the pollinators of Thismia , although several authors have suggested that the flowers may be visited by small flies ( Vogel 1962; Stone 1980; Rübsamen 1986). These inferences were based on perianth morphology, the presence of osmophores on the tepals ( Vogel 1962), the presence of nectaries either at the base of the perianth ( Poulsen 1890) or along the suture between contiguous anthers (e.g., Groom 1895; Pfeiffer 1918; Jonker 1938, 1948; Cribb 1986, 1995; Thiele and Jordan 2002; Ho et al. 2009), and the formation of sticky pollen ( Cranwell 1953). The only previous observational report of insect visitors to Thismia flowers is of small, unidentified flies entering the perianth tube of Thismia gongshanensis (Li & Bi, 2013).

Several researchers have inferred that fungus gnats are likely to pollinate Thismia flowers based on structural mimicry (e.g., tepal extensions and reticulate patterning on the inner surface of the perianth tube), perianth colour and the emission of fungus-like floral scents ( Vogel 1978; Rübsamen 1986; Thiele and Jordan 2002). We retrieved a fungus gnat (belonging to either the Mycetophilidae or Sciaridae ) from within the perianth tube of a late-anthetic specimen of Thismia hongkongensis ; unfortunately the poor state of preservation of the fly precluded further identification. We also retrieved an isolated insect wing from within the floral chamber which had the characteristic venation typical of a scuttle fly ( Phoridae ). Fungus gnats and scuttle flies are generally associated with decaying organic matter and are often reported to feed on fungi ( Hill et al. 1982).

The pollinators presumably enter the floral chamber of Thismia hongkongensis via the aperture within the annulus (a in Figs 2C, 4C). Assuming that the flower is protandrous as suggested, the movements of the pollinators are likely to differ depending on whether the flower is in its early anthetic (staminate) or late anthetic (pistillate) phase. In staminate-phase flowers, the flies are likely to be attracted to the putative nectaries (arrowed in Fig. 2D) located at the apex of the perianth tube, behind the pendent staminal ring. We hypothesize that the irregular surface on the adaxial surface of the perianth tube resulting from the reticulate venation (Fig. 2D) possibly enables the insects to climb and access these nectaries. The flies are likely to make contact with the thecae (th in Figs 2C, 4C) and inadvertently collect pollen whilst feeding from the nectaries, before departing via the small apertures (ca. 0.5 mm diameter) located between the filaments (f in Figs 2C, 4C) of adjacent stamens. If the flies enter late-anthetic pistillate-phase flowers, however, it is possible that they might be prevented from accessing the nectaries because of the raised lateral appendages of the stamens (la in Figs 2C, 4C), thereby increasing the time in which contact with the stigma is possible. The possible trapping of flies may explain the frequency with which flies are observed inside the perianth tube of late-anthetic flowers. Similar interpretations of pollinator movement, involving climbing the inner wall of the perianth tube and exiting via the apertures between the filaments, has previously been suggested by Maas et al. (1986) and Thiele and Jordan (2002) for other Thismia species.

Seed dispersal

Several different interpretations of seed dispersal have been proposed for Thismia , including movement by earthworms with secondary dispersal possible if the worms are eaten by birds ( Beccari 1890). Stone (1980) suggested that Thismia seeds are likely to be dispersed by raindrops that splash seeds out of the fruit-cup. The size and shape of the fruit-cups of Thismia hongkongensis closely resemble functionally similar rain-splash dispersal structures in phylogenetically disparate groups ( Nakanishi 2002): the upper surface of the fruit disintegrates at maturity (Fig. 3A), resulting in an upright, cup-like hypanthium (ca. 4.8 mm in diameter) with seeds that are fully exposed (Fig. 3D). Studies of other plant groups indicate dispersal of up to 1 m ( Nakanishi 2002), although there are inevitably many variables (including plant height, seed weight, etc.) that affect potential dispersal distance; it is perhaps significant that the stem of Thismia hongkongensis elongates as the fruit matures (Fig. 3C), thereby possibly increasing seed dispersal distance.

Brodie (1951) observed that seeds of species that are rain-splash dispersed are often coated with a hydrophilic colloid that rapidly absorbs water, and which may act as a lubricant, facilitating separation of seeds by rain drops. Thismia hongkongensis seeds are surrounded by a conspicuous mucilage-like substance (Fig. 3D) that may function in this way.

The fruits of Thismia hongkongensis appear to remain functional for several weeks. Although the plants are inevitably subjected to periods of desiccation, the fruits appear to be able to rehydrate effectively (Fig. 3E, F), thereby prolonging the period for seed dispersal.