Hattoria 12: 41–49. 2021

Encalypta kangchenjungae () a new species from Nepal, India and Bhutan, with new records for other Himalayan species

David G. LONG1 & Pratiksha SHRESTHA2

1 Royal Botanic Garden Edinburgh, Inverleith Row, Edinburgh, EH3 5LR, UK 2 Department of Resources, Ministry of Forests and Environment, Government of Nepal, Kathmandu, Nepal Author for correspondence: David G. LONG, [email protected]

Abstract A new species of Encalypta, E. kangchenjungae D.G.Long & P.Shrestha, is described from seven localities in East Nepal, India (Sikkim) and western Bhutan. It is tentatively placed in Section Rhabdotheca Müll.Hal. and shows similarities to E. rhaptocarpa Schwägr. from which it differs in its shorter stems, its shorter setae and shorter capsules, absence of a peristome, and in its short, smooth, thin and papery translucent calyptrae which are fringed at the base with triangular lobes and are campanulate- cucullate, deeply split up one side with the base consequently spreading out. In this feature it appears to be unique in the genus. It is restricted to strongly calcareous soil and rocky substrates at high altitudes in the East Himalaya. New reports are also given of three other species new to parts of this region, mostly identified by the late Diana Horton: E. alpina Sm. from Sikkim, E. ciliata Hedw. from Sikkim and Bhutan and E. rhaptocarpa Schwägr. from Nepal and Sikkim.

Introduction Eastern Asia is an important centre of diversity of the genus Encalypta Hedw. (Encalyptaceae), though its occurrence is often limited by the presence of calcareous substrates at higher elevations. Sixteen species were reported from Russia (Fedosov 2017); Cao et al. (1992) reported 6 species from China, which has now increased to 11 species (Li et al. 2006; Feng et al. 2016, 2020; Sabiram et al. 2018; Kou et al. 2020). Few species have been reported from the Himalaya, with 6 species treated from the north-west Himalaya of India (Chopra 1975; Kumar 1980) but none reported from the Eastern Himalaya (Gangulee 1969– 1980). Encalypta sibirica (Weinm.) Warnst. was reported from East Nepal by Long (1993a) but this was based on a preliminary misidentification of the new species described below. A number of Encalypta specimens from the Sino-Himalaya collected by the first author were sent on loan from E to the late Diana Horton, Professor Emeritus in the University of Iowa, USA, who studied and annotated them in 1990 and 2009. Her identifications have since

41 been confirmed by the present authors. However, a number were annotated by her as “sp. nov.” but no new species were described from these specimens as a result of her work. In her annotations, she pointed out the present new species as having “setae short; capsules ribbed; no peristomes; calyptrae unusually short and lacerate”. However, some of them, including the type specimen, were not studied by her as they had been tentatively misidentified as “Desmatodon” in the field. Furthermore, she seems to have overlooked the observation that the calyptrae are consistently cucullate, having a split up one side much longer than the basal lacerations, whereas in her thorough treatise of Encalypta in North America (Horton 1982, 1983) she observed “All species of Encalyptaceae are characterized by a mitrate, cylindric- campanulate calyptra that is naked and non-plicate”. This is borne out by her numerous figures of calyptrae of North American Encalypta species, none of which is cucullate. The species name derives from Mount Kangchenjunga, at 8586 m the world’s third highest mountain, straddling the Nepal/Sikkim border; four of the known localities are very close to the mountain and another two relatively close. No specimens have been seen from other parts of the Himalaya or China.

Materials and Methods The specimens on which this account is based were all collected by the first author on botanical expeditions from the Royal Botanic Garden, Edinburgh to Nepal, Sikkim and Bhutan in 1989, 1991, 1992, 1996, 1999 and 2017. The specimens are housed in E with some duplicates in herbaria elsewhere. Specimens were studied primarily by light microscopy, with further details by SEM using a Leo Supra 55VP scanning electron microscope at the Royal Botanic Garden Edinburgh. Dry leaves, capsules and spores were transferred directly from the herbarium specimens to 12 mm carbon discs mounted on 12.5 mm aluminium pin stubs. Specimens were coated with platinum using an Emitech K 575x sputter coater to a thickness of approximately 12 nm at a rate of 25 mA for 1.3 minutes.

Taxonomy Encalypta kangchenjungae D.G.Long & P.Shrestha, sp. nov. Figs. 1 & 2

Diagnosis: similar to Encalypta spathulata Müll.Hal. but calyptra campanulate-cucullate with a longitudinal split from laciniate base almost to base of rostrum and consequently broadening towards base, rostrum proportionately longer, ca. 0.45 of total length of calyptra.

Description: small, 2–7(–9) mm tall, yellowish-green above, brown below, growing in small dense mats. Stems simple or little-branched, central strand not developed, rhizoids pale brown, smooth. Leaves weakly twisted and appressed when dry, with tips incurved, erect-spreading when moist, 2.0–2.8 mm long, 0.45–0.75 mm broad, narrowly obovate-oblong, apex rounded-attenuate or apiculate into short hyaline or pale yellowish almost smooth hair-point formed by excurrent costa 15–450 µm long; costa strong, red-brown, abaxially smooth and shiny, adaxially papillose; upper leaf margins entire, somewhat undulate,

42 Figure 1. Encalypta kangchenjungae D.G.Long & P.Shrestha. a: whole plant with mature undehisced capsule and three young emerging capsules with calyptrae. b: leaves. c: upper leaf lamina cells. d: basal leaf lamina cells. e: mature dehisced capsule. f: two calyptrae. Drawn from the holotype, Long 20935 (E) by Malcolm Watling.

plane, with coarse protuberant papillae; upper cells irregularly rounded-quadrate or shortly rectangular, 12–20 µm wide, somewhat broader at margin, densely papillose and with obscure walls; basal cells elongate-rectangular, 50–100×7–22 µm, smooth, with thickened brown transverse walls; 3–4 rows of basal marginal cells forming a±distinct border of thin-walled linear cells 50–120×5–10 µm. Perichaetial leaves not differentiated. Autoicous. Seta erect, 3.5–4.0 mm, yellow above, red-brown at base, twisted in upper half; capsule urn cylindric, 1.5–2.0 mm long, red-brown and distinctly ribbed when ripe, ribs often darker in colour, exothecial cells narrowly rectangular, in longitudinal rows, mouth often bright red, annulus undifferentiated, operculum with slender straight rostrum. Calyptra campanulate-cucullate, covering about 3/4 of mature urn, short, 1.8–2.0 mm long, at its base laciniate with unequal triangular lobes, basal part papery, translucent and pale yellowish, smooth, sometimes with very sparse low papillae above, with a split on one side up to half its length or almost to base of rostrum, above rather suddenly contracted into a brown opaque smooth rostrum, which is ca. 0.45 total length of calyptra. Spores 35–40 µm diameter, somewhat flattened, pale yellow-brown, heteropolar, proximally±weakly ribbed and smooth,

43 Figure 2. Encalypta kangchenjungae D.G.Long & P.Shrestha, SEM images. a: old dehisced capsule. b: spore, oblique proximal view. c: spore, oblique distal view. d: leaf lamina cells. From paratype, Long 22806 (E). distally with coarsely warted papillae, the papillae 5.3–6.3 µm diameter.

Holotype: NEPAL (EAST). Sankhuwasabha District, Upper Barun Khola valley above Mera, 27°49′N, 87°07′E, 4,470 m elev., 4 October 1991, Long 20935 (herbarium E, barcode E-00147032); isotypes CAS, KATH.

Other specimens (paratypes): NEPAL (EAST). Taplejung District, Kambachen to Ramtang, upper Ghunsa Khola, 27°44′N, 88°00′E, 4,120 m elev., Long 16809b (E-01021866); Lhonak to Pang Pema, Kangchenjunga Glacier, 27°47′N, 88°04′E, 4,850 m elev., Long 16846 (E-00276701); ibid., 4,860 m, Long 16850 (E-00276700). INDIA. Sikkim, West District, Samiti Lake (Bungmoteng Chho), foot of Onglakthang Glacier, 27°33′33″N, 88°11′25″E, 4,260 m elev., Long 22792 (E-00276684); Chemathang, E side of Onglakthang Glacier, 27°35′N, 88°11′E, 4,525 m, Long 22806 (E-00276685); North District, Lasha Chhu valley, below Dambochi, 27°54′05″N, 88°33′35″E, 4,240 m elev., Long 26532 (E-00147033); Lasha Chhu between Phaklung and Goichang, 27°55′51″N, 88°36′04″E, 4,605 m, Long 26554 (E-00147016). BHUTAN. Haa District, summit of Chelai La, 27°22′N, 89°20′E, 3,780 m elev., Long 28722a (E-00276680).

44 Taxonomic discussion: Although Encalypta kangchenjungae appears to be distinct from all other species of the genus in its unique calyptrae which are described as campanulate- cucullate on account of their lateral split (Fig. 1), in all other respects it fits the genus very well, particularly in its leaves with elongated cells in the leaf base with thickened and coloured transverse walls, and in its sporophytes and spores. In Diana Horton’s preliminary study of three of the cited specimens (Long 16850, 22792 and 22806) she identified them as “Encalypta cf. rhaptocarpa Schwägr. s.lat.” which suggests she would have placed them in sect. Rhabdotheca Müll.Hal. In part II of her monograph (Horton 1983: 375) she gave a “Tentative Synopsis of species of Encalypta—see Part III”; unfortunately, Part III was never published. In this synopsis she placed eight species in sect. Rhabdotheca: E. armata Dusén, E. asperifolia Mitt., E. flowersiana D.G.Horton, E. intermedia Juratzka, E. rhaptocarpa Schwägr., E. spathulata Müll.Hal., E. vittiana D.G.Horton and E. vulgaris Hedw. In her key to North American Encalypta species she characterised subg. Rhabdotheca primarily on its “spores with trilete mark obscure or absent on proximal surface, distal surface with±prominent, warty to vermiform protruberances”. On the basis of spore ornamentation (Fig. 2) E. kangchenjungae belongs in this section, as do additionally the following species also described or reported from Asia: E. altunense Mamtimin & Sabiram (Sabiram et al. 2018), E. asiatica J.C.Zhao & Lin Li (Li et al. 2006), E. buxbaumoidea T.Cao, C.Gao & X.L.Bai (Cao & Gao 1990), E. pilifera Funck (Fedosov 2012, 2017; Feng et al. 2020), E. papillosa C.Feng, J.Kou & B.Niu (Kou et al. 2020), E. sinica J.C.Zhao & Min Li (Zhao et al. 1999; Cao et al. 2001), E. tianschanica J.C.Zhao, R.L.Hu & S.He (Cao et al. 2001), E. tibetana Mitt. (Cao et al. 2001) and E. trachymitria Ripart (Fedosov 2017). E. gyangzeana C.Feng, X.M.Shao & J.Kou (Feng et al. 2016) is of unknown placement as spores were lacking when published. In a morphological and molecular study of section Rhabdotheca in Russia (Fedosov 2012), five of these species were studied and they resolved in a single clade; their differences were tabulated. In addition, a sixth species E. intermedia Juratzka was treated as a synonym of E. pilifera Funck. To clarify the distinctiveness and relationships of the above species within sect. Rhabdotheca a full re-assessment of the section is much needed, particularly as the published descriptions of several of the species, especially of the sporophytes, spores and calyptrae, are inadequate. Aside from the campanulate-cucullate structure of the calyptra of E. kangchenjungae, of the other Asiatic species in sect. Rhabdotheca with a fringed calyptra base and lacking a peristome, it is similar overall only to E. spathulata Müll.Hal. (Horton 1979, 1983; Fedosov 2012, 2017; Magill 2007); this differs additionally in its proportionately shorter calyptra rostrum. Another species, E. buxbaumoidea (Cao & Gao 1990; Cao et al. 2001), shows some superficial similarities but has a smooth capsule urn and much shorter calyptra rostrum; the calyptra base is described as “irregularly ragged” but from the illustrations this is clearly not regularly laciniate. Finally, in E. asiatica: (Li et al. 2006) the calyptra rostrum is 1/3 its total length, and the calyptra base is described as “ragged” but the illustration shows it as almost entire and clearly not laciniate as in E. kangchenjungae.

Ecology: Encalypta kangchenjungae is a very high altitude Himalayan species, known from 3,780 to 4,860 m elev. Like other species in the genus, it is restricted to base-rich

45 substrates, particularly metamorphic schists and limestones, which outcrop only locally in the high Himalayas. In some places it is found on moraine ridges associated with extant or former glaciers, but in other places it grows on soil or in crevices of rock outcrops and boulders on eroding rocky slopes, often in the shade of shrubs such as Juniperus and Potentilla species. Predictably, most associated bryophytes noted are also calcicoles, such as Distichium capillaceum (Hedw.) Bruch & Schimp., Ditrichum flexicaule (Schwägr.) Hampe, Encalypta alpina Sm., E. ciliata Hedw., Stegonia latifolia (Schwägr.) Venturi ex Broth., Tortula laureri (Schultz) Lindb., Trematodon brevicollis Hornsch., and the liverworts Plagiochasma cordatum Lehm. & Lindenb., Reboulia hemisphaerica (L.) Raddi and Scapania cuspiduligera (Nees) Müll.Frib.

Conservation: The type specimen was collected in 1991, the same year that the locality (Barun Khola valley) was included in the newly designated Makalu-Barun National Park (Bhuju et al. 2007). For bryophytes, this area was found to be exceptionally rich, where several other important bryological discoveries were made, such as Asterella grollei D.G.Long new to science (Long 1999) and the genus Sphaerocarpos new to Asia (Long 1993b). The Nepalese localities around Kangchenjunga are part of the Kangchenjunga Conservation Area designated in 1997 (Bhuju et al. 2007), while in India the eastern side of the mountain was designated in 1977 as the first State Park in Sikkim, later becoming the Khangchendzonga National Park and then in 2016 a UNESCO World Heritage Site (O’Neill 2017). However, the Lasha Chhu valley in Sikkim is not in a protected area at present, nor is the Chelai La in Bhutan (Tharchen 2013).

New reports of other Himalayan Encalypta species 1. Encalypta alpina Sm. INDIA: Sikkim, West District, Samiti Lake (Bungmoteng Chho), foot of Onglakthang Glacier, 27°33′33″N, 88°11′25″E, grassy hillside with large calcareous schist boulders, on soil on top of boulder, 4,260 m elev., Long 22794 (E). This appears to be the first record for Sikkim, Chopra (1975), Kumar (1980) and Dandyota et al. (2011) reported it in the Indian Himalayas only from Kashmir; Noguchi & Iwatsuki (1975) reported it from Nepal.

2. Encalypta ciliata Hedw. BHUTAN: Haa District, summit of Chelai La, 27°22′N, 89°20′E, open rocky hillside; in crevices of rocks, 3,780 m elev., Long 28722b (E); Trongsa District, between Yendu Chu and Wangchelakh, Black Mountain, 27°22′07.8″N, 90°20′05.8″E, open grazed hillside, in crevices of isolated calcareous schist boulder, 4,195 m elev., Long 45272 (E). INDIA: Sikkim, West District, tributary of Prek Chhu opposite Lambi, N of Thangshing, 27°31′N, 88°11′E, bouldery gully, on shady soil bank amongst boulders, 4,065 m elev., Long 22729 (E); Prek Chhu valley between Thangshing and Onglakthang, 27°32′N, 88°11′E, huge calcareous boulders on river bank, on bank under rock face, 4,075 m elev., Long 22773 (E); Chemathang, E side of Onglakthang Glacier, 27°35′N, 88°11′E, grassy banks beside sandy plain, in crevices of

46 calcareous schist boulder, 4,525 m elev., Long 22807 (E); North District, Lasha Chhu valley, NE of Thanggu, 27°53′39″N, 88°32′44″E, open grazed slopes with dwarf shrubs, on bank under Cotoneaster, 4,130 m elev., Long 26530 (E). These constitute the first records for this species from Bhutan and Sikkim although the second report from Bhutan was mentioned by Long et al. (2018); Kumar (1980) reported it from Kashmir and Himachal Pradesh; Dandyota et al. (2011) reported it from Kashmir and Uttarakhand, and Noguchi & Iwatsuki (1975) reported it from East Nepal.

3. Encalypta rhaptocarpa Schwägr. NEPAL (WEST): [Myagdi District] Ghorepani, WSW of Annapurna, on ground in Rhododendron forest, 8 November 1978, Davies s.n. (E); Manang District, Braga, Marsyandi River valley SE of Muktinath, at edge of snow patch, 1 November 1978, Davies s.n. (E); both det. D.G. Horton. INDIA: Sikkim, West District, Samiti Lake (Bungmoteng Chho), foot of Onglakthang Glacier, 27°33′33″N, 88°11′25″E, grassy hillside with calcareous schist boulders, on soil amongst boulders, 4,400 m elev., Long 22835 (E). These appear to be the first records for Nepal and Sikkim; Chopra (1975) and Kumar (1980) reported it from Kashmir and Himachal Pradesh.

Acknowledgements Research at the Royal Botanic Garden, Edinburgh is supported by the Scottish Government’s Rural and Environment Science and Analytical Services Division. The second author wishes to acknowledge the Department of Plant Resources, Kathmandu, for support for her bryological work, and the Edinburgh Botanic Garden (Sibbald) Trust is thanked for facilitating her study visit to RBGE. The late Diana Horton (University of Iowa) is gratefully acknowledged for her study and valuable annotations on some of the cited specimens. Frieda Christie (RBGE) is thanked for guidance and training of the second author in SEM techniques. Malcolm Watling (Blaenau Ffestiniog) is thanked for preparing the illustration. Jan Kučera (University of South Bohemia) is thanked for helpful comments on the final draft. Colleagues and government departments in Bhutan, Sikkim and Nepal are thanked for logistical support on RBGE plant-collecting expeditions over many years and for granting permission to collect specimens for research purposes. A range of organisations in UK are also thanked for generous financial support for these expeditions, as are many colleagues at the Royal Botanic Gardens, Edinburgh and Kew.

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