Thismia sahyadrica Sujanapal, Robi & Dantas, 2017

Sujanapal, P., Robi, A. J., Dantas, K. J., Sumod, M. & Merckx, V. S. F. T., 2017, Thismia (Thismiaceae): the first record of the mycoheterotrophic genus to the Flora of India with a new species revealing the phytogeographical significance of Western Ghats, Blumea 62 (2), pp. 97-102 : 97-101

Thismia sahyadrica Sujanapal, Robi & Dantas , sp. nov. — Fig. 1 , 2

Thismia sahyadrica differs from all other species of Thismia in having a mitre with a single opening; it is further characterized by a brownish hypanthium, greenish yellow perianth lobes, a yellow ovary, and two fused outer perianth lobes and spreading third one. — Type: A. J. Robi & K. J. Dantas 28097 (holotype KFRI; isotypes CALI, K, L, MH), India, Kerala, Idukki dist. , Neryamangalam , ± 500 m, 14 July 2014 .

Etymology. The specific epithet ‘ sahyadrica ’ refers to the Sahyadri Hills-

Western Ghats, where the type locality of the species is located.

Terrestrial, achlorophyllous, mycoheterotrophic herb, c. 6 cm high. Roots vermiform, clustering at the base of stem, thick, unbranched, fleshy, puberulent, creamy-white, patent. Stem erect or slightly curved, simple, creamy-white or whitish, puberulent, 2–5 cm tall. Leaves scale-like, few, c. 6 by 2 mm, appressed, triangular-ovate to lanceolate, translucent, apex acute or acumi- nate. Involucral bracts 1–3, similar in shape to the leaves, c. 7 by 2–3 mm, obtuse or irregularly shaped at apex. Flowers solitary, terminal; perianth actinomorphic with 6 tepals, 5 of them fused into a mitre-like structure, the 6th tepal free and leaving a lateral aperture; tepals greenish yellow, c. 2–2.5 mm long, ovate, obtuse at apex, densely silky-puberulent outside; a horn-like appendage is attached to the dorsal side of each perianth lobe, all 6 appendages are free and upwardly pointing, with blunt apex, puberulent; hypanthium c. 1.5–2.0 cm long, obconical, faintly 6-ribbed, brownish with lower part usually yellow, greenish yellow at the apex, annulus prominent; inner surface of the perianth tube with 6 faint longitudinal ribs. Stamens 6, borne on thickened margin of the perianth tube; filaments curved downwards, connective broad, connate to form a hexagonal tube, sparsely silky-villous at base and outside the filament tube; anthers 1 mm long, straight or slightly curved, whitish. Stigma 3-lobed, lobes short, apex tufted with long hairs; style short, whitish, glandular hairy; ovary inferior, triangular, yellow to creamy-white, glabrous. Fruit a capsule, cup-shaped, dehiscing apically, brown, fleshy. Seeds ellipsoid.

Flowering & Fruiting — June to July.

Habitat & Ecology — Thismia sahyadrica is a non-photosynthetic ephemeral herb, appearing briefly to flower and fruit after a period of heavy showers during the monsoon, only in the months of June and July. It is unclear whether they regenerate from seeds or stay dormant below-ground between periods of flowering. A total of 35 flowering individuals of Thismia were found on three locations within one square km. Representatives of the new taxon grow in humus-rich undisturbed forest soil in medium elevation tropical wet evergreen forest interspersed with small rocky boulders with rich lichen and moss cover. The terrain is undulating and sloped. Litter insects, molluscs, annelids, etc. are common. Dysoxylum malabaricum Bedd. ex C.DC. ( Meliaceae ) is a dominant tree in the upper stratum. Syzygium gardneri Thwaites ( Myrtaceae ) is also common. Drypetes malabarica (Bedd.) Airy Shaw , Dimorphocalyx glabellus Thwaites var. lawianus (Hook.f.) Chakrab. & N.P.Balakr. ( Euphorbiaceae ), Dimocarpus longan Lour. ( Sapindaceae ), Ochlandra travancorica (Bedd.) Benth. ex Gamble ( Poaceae ), and Holigarna arnottiana Hook.f. ( Anacardiaceae ) are the other major trees in the middle and lower stratum. Herbaceous and shrubby vegetation is very sparse. Light penetration through the tree canopy is very poor, probably due to the thick canopy. Seasonal rivulets are seen in the area, which finally drain to the Periyar river.

Major macrofungi identified from the habitat are Coprinus disseminatus (Pers.) Gray , Lepiota clypeolaria (Bull.) P.Kumm. , Leucoagaricus rubrotinctus Singer , Leucocoprinus cepistipes (Sowerby) Pat. , Amanita angustilamellata (Höhn.) Boedijn , Marasmius haematocephalus (Mont.) Fr. , Filoboletus manipularis (Berk.) Singer , Ramaria cokeri R.H.Petersen , and Ramaria sp. Among these, Ramaria sp. is often found associated with the new species. Microfungi identified from the habitat are Absidia sp. , Aspergillus niger Tiegh. , Cladosporium cladosporioides (Fresen.) G.A.de Vries , Fusarium oxysporum Schltdl. , Mucor racemosus Fresen. , Penicillium sp. , Rhizopus stolonifer (Ehrenb.) Vuill. , and Trichoderma sp.

Bryophytes recorded from the surface of rocks and bark of the trees in the habitat are Frullania muscicola Steph. , Aerobryum speciosum (Dozy & Molk.) Dozy & Molk. , Meteoriopsis squarrosa (Hook. ex Harv.) M.Fleisch. , Erythrodontium julaceum (Hook. ex Schwägr.) Paris , Entodon laetus (Griff.) A.Jaeger , Asterella khasiana (Griff.) Grolle , Targionia hypophylla L., Cephaloziella kiaeri (Austin) S.W.Arnell , Fossombronia cristula Austin , Anoectangium bicolor Renauld & Cardot , Bryum argenteum Hedw. , Ptychostomum pseudotriquetrum (Hedw.) J.R.Spence & H.P.Ramsay ex Holyoak & N.Pedersen , Groutiella tomentosa (Hornsch.) Wijk & Margad. , and Macromitrium sulcatum (Hook.) Brid.

As the soil is an important component in the ecosystem, especially for the ephemeral flora, soil parameters were also analysed for the three locations. Generally, the soil belongs to the order inceptisols. The soil is loamy sand in texture (sand - 87 %, silt - 7 %, clay - 6 %). The pH of the soils were determined in 1: 2.5 (soil: water) suspension and the soils were found to be strongly acidic, medium in organic carbon, low in available nitrogen, high in available phosphorus and medium in available potassium ( Table 1).

Though the associated species and edaphic factors in the habitat were assessed, most of the available information on the ecology is anecdotal; the reproductive biology and life-cycle of the new species are poorly understood.

Distribution & Phytogeography — The new species is so far known only from the type locality at Neryamangalam forest in the Idukki district of Kerala, India. Phytogeographically, this area is part of the southern division of Western Ghats. Among the three subdivisions of southern Western Ghats ( Nayar 1996), this location falls in the windward region of the Anamalai High Ranges, which is the central and broader (± 210 km) subdivi- sion situated immediately south of the Palghat Gap. The striking feature of the windward region of the Anamalai High Ranges is the high altitudinal gradient from 100–2695 m above sea level and formation of dense tropical evergreen forests as a major forest type dominated by Dipterocarpus , Syzygium , and Cinnamomum in the upper stratum with a wide range of species composition based on the elevation. The associated habitats in the region include moist deciduous forests, semi-evergreen forests and broad-leaved hill forests mainly along the medium and lower altitudes and shola forests - montane grasslands at higher elevations. Each major forest type in the area is com- posed of several edaphic types.

The family Thismiaceae is represented in the Western Ghats by Haplothismia , an extremely rare monotypic genus endemic to Parambikulam Wildlife Sanctuary ( Sasidharan & Sujanapal 2000). Thismia sahyadrica is the first record of the genus Thismia in the Western Ghats and together with a Sri Lankan endemic T. gardneriana Hook.f. ex Thwaites represents the only two species of Thismia known from the Indian subcontinent ( Jonker 1938). The new species highlights the broad distribution of the genus. The biogeographic history of Thismia , however, is obscure. The genus is widespread in tropical America and Southeast Asia, but absent from Africa and Madagascar. Although the affinities of T. sahyadrica remain unclear, morphology suggests that the species is closely related to other Paleotropical species of Thismia . In that respect, the new species represents a range expansion of the genus in the Paleotropics ( Map 1 ).

The Western Ghats – Sri Lanka biodiversity hotspot is among the eight hottest biodiversity hotspots on Earth, featuring exceptional concentrations of endemic species and experiencing exceptional loss of habitat ( Myers et al. 2000). Apart from the newly reported species of Thismia in this region, out of nine other mycoheterotrophic taxa so far known from the Western Ghats – Sri Lanka hotspot, five were found nowhere else within the region and habitat ( Hajra 1988, Govaerts et al. 2007, Nayar et al. 2014), indicating a high degree of endemism for mycoheterotrophic species in this region.

Conservation status — All the known occurrences of the new taxon are restricted to medium elevation evergreen forest and all are close to human settlements. This may lead to habitat loss. Most mycoheterotrophs cannot be cultivated ( Merckx et al. 2013) which means that in-situ conservation is currently the only effective and practically viable method for the conservation of this species. Hence the locality needs to be protected from anthropogenic disturbances; also restrictions should be laid down for the road widening and other constructions in adjacent areas, as the State Highway is passing through these forest areas. These forests are only having the status of reserve forests, not of Protected Areas, hence special programmes should be formulated for the conservation of the species and its habitat. The current information on its distribution shows that the area of occupancy and extent of occurrence of the species both are less than 10 km 2. Therefore, the species should be considered et al. 2015, Chantanaorrapint & Sridith 2015, Chantanaorrapint et al. 2016). 1 - Thismia abei (Akasawa) Hatus. ; 2 - T. tuberculata Hatus. ;3 - T. huangii P.Y.Jiang & T.H.Hsieh ; 4 - T. taiwanensis Sheng Z.Yang,R.M.K.Saunders & C.J.Hsu ;

5 - T. gongshanensis Hong Qing Li & Y.K.Bi; 6 - T. hongkongensis Mar & R.M.K.Saunders ; 7 - T. tentaculata K. Larsen & Aver. ;8 - T. gigantea (Jonker) Hroneš ; 9 - T. mucronata Nuraliev ; 10 - T. okhaensis Luu, Tich, G.Tran & Đinh ; 11 - T. annamensis K.Larsen & Aver. ; 12 - T. javanica J.J.Sm. ; 13 - T. puberula Nuraliev ; 14 - T. mirabilis K.Larsen ; 15 - T. angustimitra Chantanaorr. ; 16 - T. filiformis Chantanaorr. ; 17 - T. clandestina (Blume) Miq. ; 18 - T. nigricans Chantanaorr. & Sridith ; 19 - T. alba Holttum ex Jonker ; 20 - T. brunonis Griff. ; 21 - T. arachnites Ridl. ; 22 - T. fumida Ridl. ; 23 - T. racemosa Ridl. ; 24 - T. chrysops Ridl. ; 25 - T. grandiflora Ridl. ; 26 - T. aseroe Becc. ; 27 - T. labiata J.J.Sm. ; 28 - T. ophiuris Becc. ; 29 - T. episcopalis (Becc.) F.Muell. ; 30 - T. goodii Kiew ; 31 - T. hexagona var. grandiflora Tsukaya ; 32 - T. hexagona Dančák, Hroneš, Kobrlová & Sochor ; 33 - T. brunneomitra Hroneš ; 34 - T. bifida M.Hotta ; 35 - T. neptunis Becc. ;36 - T.betung-kerihunensis Tsukaya & H.Okada ;37 - T. lauriana Jarvie ;38 - T. mullerensis Tsukaya & H.Okada ;39 - T. gardneriana Hook.f. ex Thwaites ; 40 - T. sahydrica Sujanapal, Robi & Dantas ; 41 - T. appendiculata Schltr. ; 42 - T. clavigera (Becc.) F.Muell. ; 43 - T. crocea (Becc.) J.J.Sm. ; 44 - T. claviformis Chantanaorr. & J.Wai.

as Critically Endangered (CR) according to the IUCN Red List Categories and Criteria ( IUCN 2012).

Additional specimens examined (Paratype). INDIA, Kerala, Idukki dist., Nerymangalam, Kulamankuzhikudi , A. J. Robi & M. Sumod 28096 ( KFRI), c. 500 m, 26 June 2014 .

Taxonomic notes — Thismia sahyadrica is unique in the genus by having a mitre with a single opening. Mitre-bearing species of Thismia are found in the sections Pyramidalis , Rodwaya , Sarcosiphon , Glaziocharis , Geomitra , and Scaphiophora ( Merckx & Smets 2014) . The relatively short, thick, unbranched roots of the new species show similarities with species in the sections Sarcosiphon , Geomitra , and Scaphiophora , which have short coralloid roots (except for T. mirabilis and T. angustimitra ). On the other hand, both the single free and five fused tepals of T. sahyadrica have short filiform appendages, a characteristic that is only present in the section Glaziocharis . Therefore, until further molecular phylogenetic studies are undertaken the taxonomic affinities of T. sahyadrica remain obscure.

Acknowledgments The authors are grateful to the Director, Kerala Forest Research Institute, Peechi, Kerala, India for providing facilities and support, and also thankful to Kerala State Forest Department for necessary permis- sions;AJR is thankful to the Principal of Bishop Abraham Memorial College, Thuruthicad,Pathanamthitta.The authors also wish to thank Dr.Mallikarjuna Swamy, Scientist,Pathology department and Dr. S. Sandeep, Scientist, Soil Science department of KFRI for their help in the identification of fungi and soil analysis, respectively. Also grateful to Dr. T.J. Roby for preparing the map, Dr. E. Sanoj for the illustration and to anonymous reviewers for their critical comments.

Figures

Map 1 Distribution of Thismia in Asia (Compiled from Govaerts et al. 2007, Larsen & Averyanov 2007, Chantanaorrapint 2008, 2012, Chiang & Hsieh 2011, Tsukaya & Okada 2012, Merckx et al. 2013, Dančák et al. 2013, Li & Bi 2013, Truòng et al. 2014, Nuraliev et al. 2014, 2015, Mar & Saunders 2015, Hroneš

Fig. 1 Thismia sahyadrica Sujanapal, Robi & Dantas. a. Habit; b. flower enlarged; c. outer view of tepals; d. inner view of tepals; e. lateral view of tepals with appendage; f. inner of pendulous stamens and annulus; g. anther with connective; h. gynoecium with short style and papillose stigma — Scale bars: a–b = 1 cm; c–h = 1 mm. — Drawing by E. Sanoj.

Fig. 2 Thismia sahyadrica Sujanapal, Robi & Dantas. a. Habitat; b–c. habit; d. young flowers; e. plants with flowers; f. flowers enlarged with pedicel and bract; g. outer view of tepals; h. inner and lateral view of tepals; i. hypanthium with lateral opening; j. longitudinal section of hypanthium together with annulus and stamen tube; k. stamens with connective; l. gynoecium with short style and papillose stigma. — Scale bars: g–h, j = 5 mm; i = 1 cm; k = 3 mm; l = 2 mm. — Photos by A.J. Robi.