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NOTES ON SCARCELY COLLECTED INDIAN LIVERWORTS I. HORIKAWAELLA SUBACUTA AND PLEUROZIA PURPUREA

(MARCHANTIOPHYTA)

D.K. Singh and Siddhartha Singh Deo*Botanical Survey o f India,

CGO Complex, 3rd MSO Building, Block F (5th Floor),Salt Lake Sector I, Kolkata - 700 064, India.

ABSTRACT: A number of Indian liverworts are only poorly known in country’s bryoflora with apparently no representation in Indian herbaria. Two such species, viz. Horikawaella subacuta (Herzog) S.Hatt. & Amakawa - an Himalayan endemic, and Pleuroziapurpurea Lindb., widespread in North America, Europe and Southeast Asia, have been described and illustrated here based on recently collected specimens from Arunachal Pradesh in the Eastern Himalaya.

INTRODUCTION

Beginning 1832 (Lehman, 1832), the taxonomic studies on Indian liverworts have so far

resulted into the documentation of over 850 taxa in country’s bryoflora (Udar, 1976; Singh, 2001; Srivastava, 1998; Srivastava and Srivastava, 2002; Asthana and Srivastava, 2003; Manju et al, 2005; Singh and Nath, 2007; Rawat and Srivastava, 2007; Manju et al, 2008; Singh and Singh, 2009; Daniels, 2010; Dey and Singh, 2012; Sanjappa and Singh, 2008, 2009, 2010; Singh and Singh, 2011; Singh et al, 2012, 2013; Singh and Dash, 2014; Singh Deo and Singh, 2014; Singh et al, 2014). But, a number of these taxa are poorly known in the country, sometimes without or with a very cryptic description, and often with no representation in Indian herbaria. Some of these species, viz. Acromastigum inaequilaterum (Lehm. et Lindenb.) A. Evans, Dendrobazzania griffithiana (Steph.) R.M.Schust. & W.B. Schofield, Kurzia tennerrima (Mitt, ex Steph.) Grolle, Lepidozia minima Steph., L. robusta Steph., Chiloscyphus gollani Steph., Heteroscyphus coalitiis (Hook.) Schiffn., Plagiochila fragillima Steph., Cheilolejeunea intertexta (Lindenb.) Steph., Drepanolejeunea pulla (Mitt.) Grolle, Riccardia cardottii (Steph.) Pande & Srivastava, etc., are known only through their type or just a few collections housed in herbaria abroad. On the other hand, many taxa, like Plagiochila carringtonii

subsp. lobuchensis Grolle, R chinensis Steph., P. poeltii Inoue & Grolle, Cololejeunea desciscens Steph., C. raduliloba Steph., Metzgeria macrospora Kuwah., M molokainensis Kuwah., etc., earlier recorded from the country, were excluded from Indian bryoflora in subsequent revisions due to unavailability of their specimens in Indian herbaria (Srivastava and Udar, 1975; Asthana and Srivastava, 2003; Rawat and Srivastava, 2007). This often impedes proper assessment and characterization of such taxa in Indian perspective.

During the course of the present study on liverworts and homworts of the Eastern Himalaya, we came across two such liverworts, viz. Horikawaella subacuta (Herzog) S.Hatt. & Amakawa of the family Solenostomataceae and Pleurozia purpurea Lindb. of Pleuroziaceae, which are apparently not represented in Indian herbaria.

The genus Horikawaella S.Hatt. & Amakawa is endemic to the Himalayas and is presently represented by just two species, viz. H. subacuta from India, Bhutan, China and Nepal, and H. grosse-verrucosa Amakawa & S.Hatt., confined to China and Nepal (Li et al, 2013). The genus is characterized by (i) erect-suberect, robust plants which are usually purplish, (ii) cordate-ovate leaves which are conduplicately concave with subacute to narrowly obtuse apex and conspicuously vemicose

Botanical Survey of India, Central National Herbarium, Howrah -711 103, India.

Indian Journal* of Forestry, Vol. 37 (4): 465-472, 2014

466 D.K. SINGH AND SIDDHARTHA SINGH DEO

surface, (iii) underleaves absent (iv) rhizoids scanty, hyaline or purple, (v) androecia terminal with 3 ^ - pairs of bracts and (vi) gynoecia with bracts in 2 pairs and semi-exserted, fusiform, 4-plicate perianth. Our knowledge of H. subacuta from India has so far been based on the accounts of Herzog (1939) who described Anastrophyllum subacutum Herzog (= Hohkawaella subacuta) from Sikkim. Earlier, Chopra (1938) had described a new species, Cuspidatula nicholsonii R.S. Chopra from Darjeeling in West Bengal, apparently referable to this species but the name is not valid as it lacked a Latin description / a reference to a previously validly published name (see Art.39.1: McNeill et al, 2012).

The genus Pleurozia Dumort., with 11 presently known species [P. acinosa (Mitt.) Trev. (China, Indonesia, Japan, Malayasia, Sri Lanka, Taiwan, Thailand), P. articulata (Lindb.) Lindb. & Lackstrom (New Caledonia, Australia), P. caledonica (Gottsche ex Jack) Steph. (New Caledonia), P. conchifolia (Hook. 8l Am.) Aust. (Hawai, Indonesia, Myanmar, New Guinea), P. curios a B. Thiers (New Caledonia), P. gigantea (F.Weber) Lindb. (China, Fiji, Indonesia, Japan, Macronesia, Malayasia, Mauritius, Myanmar, New Caledonia, New Hebrides, Papua New Guinea, Philippines, Reunion, Sri Lanka, Tanzania), P heterophylla Steph. ex Fulf. (Venezuela-Guyana), P. johannis-winkleri Herzog (Malayasia), P paradoxa (Jack) Schiffn. (Chilie, Colombia, Equador, Venezuela) P. purpurea Lindb. (Bhutan, China, India, Japan, Nepal, Europe, North America, West Indies), and P. subinflata (Aust.) Aust. (China, Hawai, Japan, Sri Lanka, Thailand)] on the other hand, is widely distributed from Australasia to western hemisphere through Asia, Europe and Africa (Theirs, 1993). The genus is characterized by (i) plants forming yellowish green mats or tufts with red-purple pigmentation, (ii) leaves simple, or conduplicate bilobed with explanate or saccate, smaller dorsal lobule, surface verruculose, (iii) saccate lobules almost completely enclosed with the access to its interior controlled by a hinged, spathulate valve, (iv) androecia on very short lateral branches near shoot apex, (v) gynoecia, both fertile and sterile, with female bracts in 2-5 series; fertile perianths usually plicate with ciliate mouth, and

(vi) 8-10 stratose capsule wall with the cells of outermost layer showing biphasic development with 2 nodular thickenings on each secondary wall, cells of innermost layer with reticulate thickenings. P. purpurea is a well-known species elsewhere, but in India it is known only through a report from Jongri in Sikkim by Hattori (1966).

DESCRIPTION AND DISCUSSION

Horikawaella subacuta (Herzog) S.Hatt. & Amakawa, Misc. Bryol. Lichenol. 5 :164 .1911. Anastrophyllum subacutum Herzog, Ann. Bryol. 12: 75. 1939. Cuspidatula subacuta (Herzog) Grolle. J. Jap. Bot. 39: 175.1964. Cuspidatula nicholsonii R.S. Chopra, Proc. Indian Acad. Sci. 8B: 431. 1938 (nom. inval.) (Fig.l).

Plants black - reddish brown in herbarium, ascending, forming dense patches; shoots 0.7-1.5 cm long, 1.5-2.0 mm wide, sparsely branched; branching lateral intercalary, usually confined to the lower half of the plant. Stem elliptical-more or less suborbicular in outline in transverse section, 210-240 X 170-180 )Lim, 12-14 cells across diameter; cortical cells in 1-2 layers, subquadrate-rectangulate, 11-13 X 8-26 iLim, moderately thick-walled, light to dark brown; medullary cells, subquadrate-polygonal, 14-30 X 10-34 jiim, thin-walled, hyaline-yellowish, stem surface strongly verrucose. Rhizoids restricted to stem base, reddish to black. Leaves contiguous- imbricate, subtransversely-transversely inserted, conduplicate-concave, triangular cordate when flat, 0.8-1.4 mm long, 0.6-1.4 mm wide, apex subacute- acute, margin entire, ventral margin slightly decurrent, dorsal margin not so; apical leaf cells quadrate, subquadrate-polygonal 13.0-22.5 x 15.0-22.5 iLim; median leaf cells quadrate-polygonal 17.5-34.0 X 15.0-29.0 iiim; basal leaf cells oblong, polygonal, 30.0-50.0 x 14.0-22.5 |im, walls thin- slightly thick with nodulose trigones, intermediate thickenings absent; surface strongly verrucose; verrucae rounded in apical region, round-striate in mid-basal region; oil-bodies not seen.

Dioicous (?). Androecia not seen. Gynoecia terminal on main shoot; bracts in single pair, embracing perianth, similar to stem leaves, 1,0-1.2

INDIAN JOURNAL OF FORESTRY 467

0.5mm

Fig. 1. Horikawaella subacuta (Herzog) S.Hatt. & Amakawa: 1. A portion o f female plant in ventral view. 2. A portion o f vegetative plant in ventral view. 3. A portion o f the same in dorsal view. 4. Transverse section o f stem. 5-11. Leaves.

12-14. Apical leaf cells. 15. Median leaf cells. 16. Basal leaf cells. 17. Transverse section o f leaf (showing verrucae). 18-19. Female bracts. 20. Perianth apex. 21-23. Transverse sections of perianth. 24. A portion o f same enlarged

showing verrucae (All figures drawn from S. Singh Deo 51006A).


mm long, 0.9-1.1 mm wide, free; bracteoles absent. Perianth fusiform, 1.0-1.4 mm long, 0.5-0.6 mm wide, 4-plicate, with few smaller, secondary plicae, narrowed and twisted towards the mouth, surface densely verrucose. Mature sporophytes not seen.

Habitat and ecology: Terrestrial, growing on rock faces along water stream, in transitional vegetation type between subalpine and alpine zones dominated by species of Abies and Juniperus, in association with Blepharostoma trichophyllum (L.) Dumort., Herbertus aduncus (Dicks.) Gray and mosses.

Distribution: INDIA [Eastem Himalaya (Arunachal Pradesh - present study, Sikkim, West Bengal)], BHUTAN, CHINA, NEPAL (Herzog, 1939 as Anastrophyllum subacutum; Chopra, 1938, 1943 as Cuspidatula nicholsonii; Grolle, 1966 as C. subacuta; Hattori and Amkawa, 1971; Hattori, 1975; Long and Grolle, 1990; SunetaL, 2002; Pradhan and Joshi, 2009; Vana and Long, 2009; Li et al, 2013).

Specimens examined: India - Eastem Himalaya, Arunachal Pradesh, West Siang district, Tato (Mobu Mountain), c. 3000 m, 27.08.2011, S. Singh Deo 51006A (CAL).

H. subacuta is characterized by densely verrucose stem, leaf and perianth surface (Fig. 1: 4, 14-17, 24); incubous, conduplicate-concave, subtransversely- transversely inserted, triangular- cordate leaves with subacute-acute apex (Fig. 1: 5-11) and fusiform, 4-plicate, perianth with few smaller secondary plicae (Fig. 1:1, 21-23). Our plants compare well with those described across its range of distribution, except the length of shoots. Our plants are smaller in length being 0.7-1.5 cm long as compared to other plants. In their small size, our plants show an interesting similarity with the only other species of the genus, H. grosse-verrucosa, but are easily distinguishable from the latter which has ovate leaves with obtuse apex as compared to cordate-triangular leaves with subactute-acute apex in the former.

Pleuroziapurpurea Lindb., Hepaticol. Utveckl. 16, 21,33,50. 1877 (Figs. 2, 3).

Plants yellowish red-purple coloured in herbarium, ascending, in loose mats; shoots 7-10 cm

long, 2-3 mm wide, mostly unbranched; branching when present lateral intercalary. Stem elliptical in outline in transverse section, 310-400 x 280-300 jiim, 14-18 cells across diameter; cortical cells in2-4 layers, rectangulate-polygonal, 12.5-15.0 x7.0-10.0 |im, thick-walled, dark brown; medullary cells, subquadrate-polygonal, 12.5-22.5 x 17.5- 40.0 jLim, thin to thick-walled, yellowish-light brown. Rhizoids not seen. Leaves closely imbricate, conduplicate-bilobed; ventral lobe widely triangular,2.1-3.5 mm long, 1.6-1.9 mm wide, concave, apex bifid to 1/5-1/4 of the leaf length, margin dentate at apex, ventral margin strongly arched with 1-4 triangular teeth near base bearing a hyaline papilla, dorsal margin slightly curved, folded, without tooth; apical leaf lobe cells subquadrate, quadrate - polygonal, 12.5-30.0 x 10.0-20.0 |Lim; median leaf lobe cells quadrate-rectangulate, 17.5-44.0 x 17.5-22.5 jLim ; basal leaf lobe cells oblong, rectangulate, 30.0-57.5 X 17.5-22.5 jiim, walls thin with bulging, confluent trigones, intermediate thickenings absent; dorsal lobe saccate, deltoid, inflated, completely enclosed, 3/5-1/2 the size of ventral lobe, 1.5-1.8 mm long, 0.7-1.1 mm wide, with an elongated, funnel-like groove towards stem ending in an aperture capped by spathulate-rounded movable flap/valve; surface smooth-verruculose. Oil-bodies not seen.

Dioicous (?). Androecia not seen. Gynoecia fertile, on short lateral branches; bracts in 2-3 pairs,1.3-2.8 mm long, 1.5-2.9 mm wide, 2-3-lobed to 1/5-1/2 of its length, apex acute, margin dentate, dorsal lobe of bract open, not sac-like. Perianth oblong ovate, 4.8-5.8 mm long, 1.5-1.7 mm wide, with 3-4 obtuse, swollen folds extending above the middle of perianth, mouth contracted, divided into 10-12 small lobes each with 2-4 cilia at apex,3-6 cells long, uniseriate. Capsule ovoid, brown, dehiscing into up to 12 segments; capsule wall4-5 stratose; cells of the outer layer subquadrate to rectangulate, 29-58 x 23-48 jum with a pair of nodular thickening on the walls; those of inner layer rectangulate, 46-69 (-115) x 18-34 |Lim, with complete - incomplete, reticulate, semiannular thickening bands. Spores globose to subglobose, yellowish brown, 20-26 \im in diameter, spinulose


Fig. 2. Pleurozia purpurea Lindb.: 1. A portion of plant in dorsal view. 2. A portion of the same in ventral view.3. A portion of female plant in dorsal view. 4. Transverse section o f stem. 5-6. Leaves. 7. Apical leaf lobe cells.

8. Median leaf lobe cells. 9. Basal leaf lobe cells. 10-12. Marginal (ventral) teeth. 13. Movable flap of dorsal lobe. 14-16. Female bracts. 17-19. Transverse sections of perianth. 20. Perianth apex. 21. Cells from the outer layer of

capsule wall. 22. Cells from the inner layer o f capsule wall. 23. Transverse section of the capsule wall. 24-29. Spores. 30. An elater (All figures drawn from S. Singh Deo 50845A).


Fig. 3. Pleiirozia purpurea Lindb.: 1. Dorsal leaf lobe showing movable flap/valve and funnel-like groove/depression under SEM. 2. A spore under SEM.

to papillose. Elaters elongated, yellowish brown, 185-275 j.im long, 12.5-16.2 )iim wide with bispiral thickening bands.

Under SEM. the spores exhibit more or less pitted surface with verrucose ornamentation sparsely studded with baculae usually with 2-4-fid apices.

Habitat and ecology. Epiphytic, growing in moist and shady conditions in subtropical to subaipine forests in association with Anastrophyllum donniannm (Hook.) Steph., Bazzania pearsonii Steph. B. sumhavensis (Gottsche ex Steph.) Steph., B. tricrenata (Wahlenb.) Trevis., B/epharostoma trichophyllum (L.) Dumort., FruHania duthiana Steph., Herhertiis adimcus (Dicks.) Gray, H. annitamis (Steph.) H.A. Mill., H. dicramis (Taylor ex Gottsche et al.) Trevis., Lepidozia hrevifolia Mitt., Plagiochila gracilis Lindenb. & Gottsche, P. semidecurrens (Lehm. & Lindenb.) Lehm. & Lindenb., Plagiochilion hraimiamim (Nees) S.Hatt., Scapania ornithopoides (With.) Waddell, S. verrucosa Heeg. The species grows in abundance and dominates the microhabitat. It has also been found growing epiphytically on branches of trees in relatively drier habitat possibly due to its water storage mechanism in dorsal lobe of leaves.

Distrihutiom INDIA [Eastern Himalaya (Amnachal Pradesh - present study, Sikkim)], BHUTAN, CHINA, JAPAN, NEPAL, EUROPE (DENMARK, NORWAY, UNITED KINGDOM), NORTH AMERICA (CANADA, U.S.A]), WEST INDIES (Guadeloupe) (Long and Grolle, 1990; Ikegami, 1957; Hattori, 1966; Thiers, 1993; Zhu, 2006; Pradhan and Joshi, 2009).

Specimens examined: India - Eastern Himalaya, Arunachal Pradesh, West Siang, between Zupuk and Damingla forests, c. 3500 m, 08.05.2011, S. Singh Deo 50842D; 50845A; 50849A (CAL); on way to Tato, c. 1200m, 22.08.2011, S. Singh Deo 50892G (CAL); Tato (Sidora), c.2300 m, 26.08.2011, S. Singh Deo 51003B (CAL); Tato (Mobu Mountain), c. 3000 m, 27.08.2011, S. Singh Deo 51009B; 51010A;51026 (CAL).

P. purpurea is characterized by conduplicate- bilobed, closely imbricate leaves with widely triangular, strongly concave larger ventral lobes having bifid dentate apex (Fig. 2: 5-6); dorsal lobe saccate, inflated, deltoid, 3/5-1/2 the size of ventral lobe with a funnel-like groove toward stem, capped by spathulate-rounded, movable flap/valve (Fig. 2: 5-6, 13); oblong-ovate perianth with 3-4 obtuse, swollen folds extending above the middle of


perianth and contracted mouth divided into 10-12 small lobes with ciliate apex (Fig. 2: 3, 17-19, 20).

The conduplicate bilobed leaves in majority of the species of the genus Pleurozia are interesting and for long the smaller, dorsal lobe of the leaf was considered to be ventral (Jack, 1886; Goebel, 1893; Ikegami, 1957). The saccate dorsal lobe is unique in the genus, and in P. purpurea it is a completely enclosed structure having an elongate groove/depression in the centre of the lobule. This depression or groove has a small aperture at one end, i.e. towards the stem, which is the only opening to the interior of the lobe. The aperture is complex structure having a spathulate to more or less rounded movable flap/valve fitting in a concave abutment. These lobes are interesting water storage apparatus as water movement is regulated by a valve. The position of groove/depression and aperture complex varies amongst different species of the genus.

Sexuality of the species is still uncertain, as Thiers (1993) reported Rpurpurea to be dioicous, whereas Damsholt (2002) described the plants from Denmark as monoicous with “androecia at very short lateral branches, near apex of shoot, sometimes followed by short branches with female inflorescences, developed even closer to shoot apex”. The Himalayan plants reported here bear only gynoecia on short lateral branches, with no trace of androecium, and are probably dioicous. Although rhizoids were not seen in our plants, the orientation of the plant suggests that the larger lobe is ventral and the smaller one is dorsal.

P. purpurea can be easily distinguished from other species of the genus by dentate ventral leaf lobe apex and saccate, deltoid dorsal leaf lobe. Unlike Horikawaella subacuta, Pleurozia purpurea shows much extended range of distribution across East and South-east Asia, Europe, North and Central America. Both the species have also been collected recently from Sikkim (D. Singh, pers. com.).

ACKNOWLEDGEMENTS

The authors thank the Director, Botanical Survey of India for facilities and financial assistance

to one of us (SSD) under ‘Flora of India’ Project; Dr John Steel, New Zealand, Dr. Bu Zhaojun, China, Dr. Xue-Liang Bai, China and Dr. Ye Wen, China for the help with relevant literature and the Chief Wildlife Warden, Arunachal Pradesh State Forest Department for facilitating the exploration work.

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