Seychellaria barbata Nuraliev & Cheek, 2016

Nuraliev, Maxim S., Cheek, Martin R. & Beer, Anton S., 2016, Seychellaria barbata (Triuridaceae), a new species from Marojejy National Park, Madagascar, Phytotaxa 268 (4), pp. 229-243 : 231-239

Seychellaria barbata Nuraliev & Cheek , sp. nov. ( Fig. 1–5 ).

Seychellaria barbata differs from all other species of this genus by the presence of long tufted hairs at the apex of the larger tepals of the male flowers (and also shorter hairs in female larger tepals) and by the following combination of morphological traits: 6–7 flowers per inflorescence, 1 fully developed flower per node, presence of bracteoles free from bracts, absence of connective appendages, clavate staminodes slightly longer than stamens, and ca. 40–50 carpels in female flower.

Type:— MADAGASCAR. Antsiranana Province: SAVA Region, Andapa District, Marojejy National Park, Camp. 2 area, trail between main trail and Takhtajania trail, dense montane rainforest, 14°26’15’’S, 49°45’35’’E, ca. 950 m, 15 October 2015, P. V. Karpunina, M. S. Nuraliev, A. A. Oskolski, D. Ravelonarivo, V. Razafindrahaja, J. H. Tonkaina 233 (holotype MW!, stored in ethanol and partly critical-point dried and mounted onto SEM stubs).

Plant terrestrial, monoecious, herbaceous, achlorophyllous, generally glabrous, purplish red, more than 10 cm high ( Fig. 1–3 ). Rhizome terete, Ø 1–1.3 mm. Roots few, attached to rhizome arising at 1 or 2 sides from leaf base (1 or 2 per node), unbranched, up to 2.5 cm long or probably longer, Ø 0.8 –0.9 mm at base, white, covered by root hairs up to ca. 4 mm long ( Fig. 1b ). Stem more or less erect (possibly ascending in older plants), rigid, branched with each branch terminating into inflorescence, terete, Ø 0.7 –0.8 mm ( Fig. 1a, b ). Leaves distant (internodes up to 2 cm long) but crowded towards rhizome base, scale-like, triangular-ovate with acute apex, ca. 2 mm long at rhizome and ca. 1.5 mm long at stem, ca. 1 mm wide at base. Inflorescence a raceme, ca. 1.5 cm high (from the lowermost flower), with each node bearing a bract subtending a single fully developed flower ( Fig. 1a , 2a, b , 3a ). Each flower possesses a single bracteole ( Fig. 1a , 3j ). Bracts similar to stem leaves in size and shape. Bracteoles inserted at pedicel base (near bract), lateral (transverse), right or left, free from bracts, narrowly triangular with acute apex, ca. 1 mm long, less than 0.5 mm wide ( Fig. 1e ). Each raceme bearing 6–7 unisexual flowers, of which 3–4 lower female and 3–4 upper male. Male flowers ( Fig. 3b–e , 4a–d ) with spreading pedicels 1.5–2 mm long, nodding, ca. 2–2.5 mm across, Ø ca. 1 mm in bud, light purplish red. Male perianth uniseriate, of 6 basally united tepals, 3 larger alternating with 3 smaller, strongly reflexed at anthesis. One of larger tepals occupying adaxial position; perianth orientation in respect to bracteole variable. Larger tepals triangular-ovate with acute or acuminate apex, 1.3–1.4 mm long, 0.85–1 mm wide, bearing a tuft of unbranched multicellular hairs up to ca. 1 mm long at apex and at margin in distal half (at least just before anthesis, Fig. 4e ). Smaller tepals narrowly triangular with acute apex, 1 mm long (or slightly less), ca. 0.4–0.5 mm wide, glabrous or with 2–3 apical hairs. Fertile stamens 3, at the radii of larger tepals, slightly shorter than smaller tepals, each with a very short pillow-like filament and an extrorse anther. Anther elliptic, broader than long, ca. 0.3–0.4 mm long and ca. 0.7 mm wide, consisting of 2 horizontal thecae and opening by single transversal slit. Connective evident only below the anther (not prolonged into an appendage), divided from filament by prominent articulation ( Fig. 4d ). Pollen grains small ( Ø ca. 20 μm), inaperturate; exine sculpturing spiny gemmate, gemmae small, Ø 1 μm or less ( Fig. 4f ). Staminodes 3, at the radii of smaller tepals (between stamens), slightly longer than stamens, clavate, with ribbon-shaped stipe and elliptic apical swelling. Pistillodes absent. Female flowers ( Fig. 1c–d , 2c–f , 3f, g ) with spreading pedicels 1.5–2.5 mm long, erect, ca. 2 mm across, dark purplish red. Female perianth uniseriate, of (5)6 tepals basally united into a tube less than 0.2 mm long, 3 larger alternating with (2)3 smaller, usually strongly reflexed at anthesis. Larger and smaller tepals correspondingly similar to those of male flowers in size, shape and orientation, hairy at anthesis in the same manner as male tepals but somewhat less pronounced ( Fig. 1c–d ). Gynoecium of numerous (ca. 40–50) free carpels. Each carpel ( Fig. 4 a, b ) unilocular and uniovulate, with one-sided obliquely spherical slightly laterally compressed ovary Ø (0.25) 0.3 mm and with a more or less straight gynobasic style 0.35–0.5 mm long and Ø 0.08 –0.09 mm attached at ventral side. Fruit apocarpous, Ø ca. 3–4 mm, with perianth persistent ( Fig. 1a , 3h, i ). Each fruitlet ( Fig. 5c–e ) dry, strongly laterally compressed, kidney-shaped and up to 1.5 mm long in lateral view, usually with persistent style up to 0.8 mm long, 1-seeded, dehiscent by a single longitudinal slit at outer (dorsal) side. Pericarp thin; seed almost as large as fruitlet. Embryo undifferentiated, oblong, curved to more than 90° ( Fig. 5f, g ).

Other specimen seen (paratype):— MADAGASCAR. Antsiranana Province: SAVA region, Andapa District, Marojejy National Park, Camp. 2 area, trail between Camp. 2 and Camp. 3, dense montane rainforest, 14°26’04’’S, 49°45’33’’E, ca. 800 m, 15 October 2015, P. V. Karpunina, M. S. Nuraliev, A. A. Oskolski, D. Ravelonarivo, V. Razafindrahaja, J. H. Tonkaina 214 ( MW, stored in ethanol and partly critical-point dried and mounted onto SEM stubs).

Notes: —1.Measurements of male flowers are based only on the pre-anthetic flower of the type specimen(Karpunina et al. 233) investigated by SEM, because the open male flower visible on photos of the paratype (Karpunina et al. 214, Fig. 3 ) was lost during field manipulations with the material. For this reason, a possibility exists that the size and shape of the mature male structures differ to some extent from those described above. In particular, the staminodes of type seem to be relatively longer (in comparison with tepals) than those of the paratype, and possibly more cylindrical. This might be a result of elongation of tepals during anthesis, or of intraspecific variation of staminode shape and length.

2. The staminodes in male flowers which distinguish Seychellaria from Sciaphila and other genera of Triuridaceae are interpreted by Rudall (2008) as morphological novelties, i.e. not homologous to any floral elements but corresponding to other projections found in various parts of flower in several representatives of the family. Rudall (2008) uses the morphologically neutral term “filamentous structures” for all such appendages; however, this assumption remains speculative since the androecial nature of staminodes in Seychellaria has still not been refuted.

Moreover, the floral units of Triuridaceae commonly referred to as “flowers”, especially in taxonomic literature, were argued to represent structures of uncertain homology. According to Rudall (2003, 2008) and Rudall & Bateman (2006), these floral units can equally plausibly be interpreted as inflorescences (pseudanthia), particularly the female and hermaphroditic ones. The pseudanthial interpretation has not been widely accepted and was not corroborated by an alternative structural analysis ( Ambrose et al. 2006). In this paper, we follow the traditional terminology of reproductive structures of Triuridaceae keeping in mind their debatable morphological nature.

3. With dimorphic tepals (3 large + 3 small), 3 fertile stamens and 3 staminodes, the male flowers of Seychellaria appear to be most similar to the typical trimerous pentacyclic monocot flowers among reproductive structures seen in Triuridaceae . Accepting this view suggests that the apparently hexamerous uniseriate perianth of Seychellaria and many other Triuridaceae is derived from two-whorled trimerous perianth. “Homogenization of whorls” is suggested to appear in some other monocots, such as Aspidistra ( Vislobokov et al. 2014) .

Taxonomic relationships:— The main morphological differences between Seychellaria barbata and all previously known species of this genus are summarized in Table 1. The most significant diagnostic feature of the new species is the presence of long tufted hairs at the apex of the larger tepals of male flowers (and also shorter hairs in female larger tepals), since all three other species of Seychellaria completely lack indumentum on the perianth of both sexes. The other important features of S. barbata are: 6–7 flowers per inflorescence, 1 fully developed flower per node, presence of bracteoles free from bracts, absence of connective appendages, clavate staminodes slightly longer than stamens, and ca. 40–50 carpels in female flower. Seychellaria barbata is most similar to S. africana and differs from the latter (besides the indumentum of male tepals) by the lower number of flowers in the inflorescence, the bracteoles free from the bracts, the shape and colour of the staminodes and the higher number of carpels in female flowers. The only other species of Seychellaria known from Madagascar, S. madagascariensis , is morphologically most distinct from S. barbata . Besides the differences listed in Table 1, S. barbata possesses a remarkable articulation between the stamen filament and the anther connective, which is absent in S. madagascariensis ( Rudall 2008, fig. 5 C). This feature is hardly visible without SEM investigations and remains uninvestigated for the two other species of Seychellaria .

Notably, the fusion between bract and bracteole of S. africana is not clearly evident from the drawing in its protologue ( Vollesen 1982, see also Vollesen 1985), which may indicate fusion of postgenital type, if any. In case they are congenitally united, they would show a highly unusual phenomenon of fusion of phyllomes of different axes within inflorescence of angiosperms; on the other hand, it is not clear how to distinguish this compound structure from a single longitudinally bilobed bract. Moreover, our investigation of the type specimen of S. madagascariensis has revealed similar morphological traits: the bract is deeply three-lobed, with the lateral lobes completely detached from the central lobe in some cases. This structure can be interpreted as either just a single phyllome (bract) of unusual shape, or as two bracteoles fused with the bract. Clearly, this question cannot be resolved with confidence with our current status of knowledge, and further investigations are needed. Since the inflorescence of S. madagascariensis possesses more than one flower at each node, the clarification of its branching pattern will be important here (see Discussion). For the purposes of morphological comparison between species of Seychellaria , we preliminarily follow the latter option, i.e. presence of bracteoles, for S. madagascariensis . This is also consistent with a single free bracteole illustrated for S. perrieri ( Giesen 1938, fig. 1, 9), which is currently included in S. madagascariensis .

The absence of perianth indumentum was for a long time considered as a characteristic feature of the genus Seychellaria and used for its delimitation from its closest relative Sciaphila ( Hemsley 1907, Giesen 1938, Perrier de la Bâthie 1946, Maas-Van de Kamer & Weustenfeld 1998). Indeed, many species of Sciaphila possess so-called “bearded” tepal tips, i.e. provided with dense tufts of multicellular soon-decaying hairs, only in male or in all flowers ( Hemsley 1907, Van de Meerendonk 1984, Maas & Rübsamen 1986, Maas-van de Kamer & Maas 1994, Maas & Maas 2005, Averyanov 2007, Daniel 2010, Merckx et al. 2013, Tsukaya & Okada 2013, Tsukaya & Suetsugu 2014). Our finding of hair tufts of exactly the same structure in Seychellaria barbata provides further evidence for the close relationship between Seychellaria and Sciaphila . This feature does not contradict the recent phylogenetic hypothesis which implies paraphyly of Sciaphila with respect to Seychellaria ( Mennes et al. 2013) . On the other hand, we do not consider it as support for such phylogenetic reconstruction, because the perianth indumentum is now known to be variable in both related genera, and further investigation is needed to elucidate the evolutionary pathway of this feature. Currently we can only state high lability of perianth indumentum in the tribe Sciaphileae .

In contrast to Seychellaria barbata , which has prominent hair tufts only at the apex of the larger tepals (at the same radii with stamens) and almost lacks hairs on the smaller tepals, all species of Sciaphila with bearded tepals are characterized by uniform tepal indumentum on each and every tepal of a flower (see references above). This is an additional confirmation of the taxonomic and functional importance of the hair tufts in Sciaphileae (see Maas-van de Kamer 1995) and of the complicated evolution of this feature.

Etymology:— The specific epithet “ barbata ” means “bearded” and refers to the tuft of long unbranched hairs at the apex and margins of the larger tepals of male flowers which makes this species unique within the genus Seychellaria .

Distribution and habitat:— Currently only known from Marojejy National Park (Antsiranana province) in Northern Madagascar ( Fig. 6 ). Two known specimens (type and paratype) are represented each by a single individual. However, no special attempts to find more individuals and assess the population size were performed. For this reason, we suppose that this species is probably not rare in its type locality.

Besides, the specimen Buerki 24, collected in the Galoko massif in Antsiranana province, Diana region, during an intensive inventory of the Northern Mountains Complex (see Callmander et al. 2009) and currently determined as Seychellaria madagascariensis ( Madagascar Catalogue 2016), is very likely to belong to S. barbata , as it is described as having hairs at the margin of its tepals.

Seychellaria barbata appears to be the second species of this genus known from Madagascar (if not accepting S. perrieri as a distinct species). The other one, S. madagascariensis , is rather widespread in lowland humid evergreen forests along the east coast (Toamasina and Fianarantsoa provinces) and in the northern extremity (Antsiranana province) of the island, but had not been found in Marojejy National Park ( Perrier de la Bâthie 1946, Madagascar Catalogue 2016), until recently (Gautier 3880, G identification confirmed while preparing this paper). Otherwise the collections of S. madagascariensis nearest to Marojejy (Perrier 2185, Maroantsetra and Schatz 2372, Nosy Mangabe) are at a distance of about 115 km to the South from the locus classicus of S. barbata .

Phenology:— In mid-October, two individuals were observed, each with inflorescences at various stages of functioning. In one plant (Karpunina et al. 214), the first inflorescence bore ripening fruits and the second – anthetic male and female flowers, along with pedicels of abscised male flowers and immature female flower buds. In another plant (Karpunina et al. 233), one inflorescence was dying-off with all fruitlets dehisced and most seeds fallen away, and the second showed anthetic female flowers and male flower buds. Most probably, Seychellaria barbata possesses a prolonged flowering period for each individual due to the gradual stem branching which allows the inflorescences to develop and bloom successively.

In the fully open male flower of the paratype (Karpunina et al. 214) the hair tufts of the larger tepals are not visible on photos, which is consistent with the idea of their ephemerality leading to distinctness in young flowers only, as reported for these structures in Sciaphila ( Maas & Rübsamen 1986, Daniel 2010).

Conservation:— Seychellaria barbata is a discrete plant currently known only by two mature individuals in the Marojejy Protected Area with a very restricted area of occupancy. We estimate the population to fewer than 1,000 individuals and assigned the new species a preliminary conservation status of Vulnerable [VU D1] following IUCN Red List ( IUCN 2012).

Figures

FIGURE 1. Seychellaria barbata. A. Shoot with fruiting terminal and anthetic lateral inflorescences. B. Rhizome with roots. C. Female flower, side view.D. Female flower, view from the pedicel. E. Uppermost node of the lateral inflorescence illustrated in (A) showing bract, flower pedicel and bracteole which subtends an axillary structure.All drawn from paratype Karpunina et al. 214 by A.Beer.

FIGURE 2. Seychellaria barbata, holotype Karpunina et al. 233. A, B. Inflorescence with 2 open female flowers in lower part, 3 male flower buds in upper part and pedicel of abscised flower between them. C. Female flower in axil of its subtending bract, side view. D. Female flower, front view. E. Female flower, view from the pedicel showing tepals which are bent backwards. F. Close-up of gynoecium. All photos by M.Nuraliev.

FIGURE 3. Seychellaria barbata, paratype Karpunina et al. 214. A. Shoot with fruiting terminal and anthetic lateral inflorescences. B, C. Male flower, front view. D, E. Male flower, oblique view. F, G. Female flower, side view. H. Close-up of fruit. I. Fruit, side view. J. Inflorescence with all flowers abscised except 1 male and 1 female; note bracteoles (arrows). All photos by M.Nuraliev.

FIGURE 4. Seychellaria barbata, holotype Karpunina et al. 233, SEM images of male flower.A, B. Half-opened flower, front view. C. Flower with larger tepal and anther removed, side view. D. Flower with larger tepal, anther and adjacent staminode removed, side view. E. Apex of larger tepal with tuft of hairs. F. Pollen grain.

FIGURE 5. Seychellaria barbata, paratype Karpunina et al. 214, SEM images. A. Carpel, side view. B. Carpel with artificially opened ovary showing its single ovule. C. Fruitlet with persistent style, side view. D. Fruitlet with pericarp partly removed showing seed, side view. E. Seed, side view. F, G. Embryo, side view.

FIGURE 6. Map of Northern Madagascar with distribution of Seychellaria barbata. Red four-pointed star: location of the type and paratype in Marojejy National Park; star filled with white: location of the specimen Buerki 24 which possibly belongs to this species.