Anthoceros angustus Steph., Sp. Hepat.

Peng, Tao & Zhu, Rui-Liang, 2013, A revision of the genus Anthoceros (Anthocerotaceae, Anthocerotophyta) in China, Phytotaxa 100 (1), pp. 21-35 : 24-28

Anthoceros angustus Steph., Sp. Hepat. 5: 1001. 1916.

Type :— INDIA. Sikkim-Himalaya, prope Kurseong, 1000 m, 1897, Rev. Bretaudeau 1239 (holotype G-12816!) .

= Anthoceros formosae Steph., Sp. Hepat. 5: 1002. 1916. Ξ Aspiromitus formosae (Steph.) R.M.Schust., Hepat. Anthocerotae N. Amer. 6: 742, 785. 1992. Type :— CHINA. Taiwan. “Kushaku”, 6 June 1903, U. J. Faurie 49 (holotype G-19002!).

= Anthoceros grosseinvolucratus Steph., Sp. Hepat. 6: 426. 1923. Type:— INDIA. Sikkim Himalayas , s.d., J. D. Hooker s.n. (holotype G-16583!).

= Anthoceros formosae Steph. fo. gemmulosus S.Hatt., Bull. Tokyo Sci. Mus. 11: 182. 1944. Ξ Anthoceros gemmulosus (S.Hatt.) Schiffn. & Pandé ex Bharadw., J. Indian Bot. Soc. 37: 76. 1958. Type:— JAPAN. Hyuga, Minami-nakagun, Obi, Ohte, S. Hattori 2563 (lectotype designated by Hasegawa (1984) TNS).

Description: — Hasegawa (1984), Asthana & Srivastava (1991).

Anthoceros angustus is characterized by the presence of subspherical to pillow-form gemmae that are spongy, cavernous and densely crowded along the apical margin of the thallus ( Fig. 2 A− C ). This species is highly variation in spore architecture, as described and illustrated by Asthana & Srivastava (1991). Proximal surfaces of spores in Chinese samples are sparsely papillate to spinulate ( Fig. 2 I, K ), but in type specimens sometimes with few false lamellae formed by several closely studded spines ( Fig. 2 N, O ). On the distal spore surface, the distribution of false lamellae is dense ( Fig. 2 J, M ) or dispersed ( Fig. 2 L, P ). Asthana and Srivastava (1991) reported the lack of a distinct pyrenoid in chloroplasts. Ultrastructural studies, however, confirm the presence of a pyrenoid-like area ( Renzaglia et al. 2009). Chloroplasts in Chinese samples possess abundant starch granules ( Fig. 2 G ), as repoted by Vaughn et al. (1992) and Renzaglia et al. (2009). Anthoceros angustus is similar to A. subtilis in sporoderm architecture, but the two species can be separated by the sporoderm architecture on distal surface under SEM. Anthoceros angustus has several closely studded spines forming false lamellate patterns on distal surface of spores ( Fig. 2 J, L, M, P ), while A. subtilis has frequent bifurcated spines ( Fig. 5 E ). Moreover, A. angustus has conspicuously longer pseudoelaters (240– 496 µm) ( Fig. 2 H ) than A. subtilis (77–199 µm) ( Fig. 5 C ).

Habitat:— On soil, wet rocks and sandy soil at 707–2460 m.

Distribution: — China [Fujian, Hunan, Sichuan, Taiwan ( Piippo 1990 as A. formosae ; Hasegawa 1992, 1993b; Gao & Cao 2000 as A. formosae ; Lin 2000 as A. formosae ; Gao & Lai 2003 as A. formosae ; Zhang & Wu 2006 as A. formosae ; Gao & Wu 2010 as A. formosae ), Xizang, Yunnan], Bhutan, India, Japan and Nepal ( Hasegawa 1993b).

Representative specimens examined:— CHINA. Fujian: Dehua Co., Daiyunshan Nature Reserve, Yanghui Village , beside the farm, on soil, 920 m, 3 July 2010, X.- Q . Zhang et al. 20100703-63 B ( HSNU); Hunan: Yongshun Co., township government of Xiaoxi to Xiaoxidukou , on soil, 200 m, 8 May 1999, T . Cao 990601 ( IFP); Sichuan: Muli Tibertan Autonomous Co., No. 913 field, 2460 m, 26 August 1983, K.- K . Chen 598 ( IFP); Xizang: Motuo Co., suburban district of County seat, on sandy soil on slope, 857 m, 29°23.224'N, 95°21. 803'E, 16 October 2011, T . Peng & J . Wang 20111016-5 B ( HSNU), Madi Village , on rock with a thin layer of soil by road, 982 m, 29°23.857'N, 95°22. 911'E, 16 October 2011, T . Peng & J . Wang 20111016-7 B , 20111016-9 B ( HSNU); Yunnan: Fumin Co., Yongding, 1985, Y.- K . Yang 139 ( IFP), Yuanyang Co., Fengchunling , Laocaozhai, on rock by forest, 9 June 1974, M . Zang 4827 ( IFP), Gongshan Co., Cikai North Road , on soil, 1515 m, 27°44.962'N, 98°39.872'E, 20 May 2011, T . Peng & J . Wang 20110520-8, 20110520- 10 B , 20110520-11A, 20110520-13A, 20110520-15 ( HSNU), Dulong Xiang, west slope of Gaoligong Shan, Irrawadi catchment, east bank of Dulong Jiang on road to Hongxin Qiao just south of Bapo , degraded valley slope with secondary scrub, on face of road cut, 1391 m, 27°44.187'N, 98°21.003'E, 3 November 2004, D. G . Long 33859 ( E), Fugong Co., Gaoligong Shan Range, southern end of the Hengduan Shan. Nu Jiang (Salween River) watershed , 1725 m, 27°07.303'N, 98°49.595'E, 25 April 2004, J. R . Shevock 25091 ( E), Jinping Co., Fenshuiling Nature Reserve , on soil, 1975 m, 22°51'49.25"N, 103°13'32.86"E, 24 November 2012, J . Wang et al. 20121124-80 229 ( HSNU), Lvchuan Co., from Lvchun to Jinping , near stream, on soil, 1616 m, 22°52'00.34"N, 102°32'18.22"E, 23 November 2012, J . Wang et al. 20121123-80 ( HSNU), Tengchong Co., Shangying Xiang, Datianpo Cun , west slope of Gaoligong Shan , on road from Bawan to Tengchong , 7 km above Dahaoping, Roadside in evergreen Lithocarpus / Lauraceae /bamboo forest, on damp soil bank, 2130 m, 24°56'52"N, 98°44'46"E, 18 October 2003, D. G . Long 32410 B ( E), Jinghong City, Nabanhe National Nature Reserve, from Xiaonuoshangzhai to Guomenshan Reserve Station , on soil by road, 1240 m, 7 January 2006, T . Cao & G.- Y . Song 060545 ( HSNU). BHUTAN. Punakha District: Mo Chu valley below Tashithang, Wet evergreen broad-leaved forest, on damp gravelly bank, 1630 m, 27°44'31"N, 89°44'18"E, 26 September 1999, D. G . Long 28789 A ( E). NEPAL. Sankhuwasabha District: forested slopes above Tashigaon, degraded evergreen Quercus lamellosa forest, on damp gravelly bank, 2240 m, 27°37ʹN, 87°14ʹE, 24 September 1991, D. G . Long 20541 ( E) .

Anthoceros bharadwajii Udar & A.K.Asthana, Proc. Indian Natl. Sci. Acad. B 51(4): 484. 1985. Type:— INDIA. Kerala, Trichur , ca. 1500 m, September 1982, R. Udar & party, 5446/82 (holotype LWU) .

Thalli medium-sized, ecostate, often radially oriented to fan-shaped with slight to deeply dissected lobes at margins, thalli up to 13 mm long and 3–10 mm wide, 0.2–0.3 mm thick; spongy; dorsal epidermis of thallus with single chloroplast per cell, cells irregular in shape, each measuring 25–36 µm across with a central dark pyrenoid region. Dioicous (?). Antheridia not seen. Involucre cylindrical, erect, up to 5 mm high, narrow at mouth. Capsules erect, up to 3.5 cm, bivalved, with well-developed columella. Epidermal cells of capsule rectangular to narrow rectangular, 91–242 × 8–15 µm, thick-walled, stomata scattered, 56–87 × 33–43 µm, each with two reniform guard cells surrounded by 5–7 cells; cells of the inner lining layer of capsule walls rectangular, 40–75 × 28–41 µm, sometimes with irregular dark thin bands on tangential walls. Spores browndark, brown, 35–54 µm in diameter with spinulate blunt projections forming a pseudolamellate pattern; proximal faces marked with distinct trilete mark, bordered on both sides by 2–5 µm wide unsculptured strip, trilete marks reaching periphery or terminating shortly before periphery. Pseudoelaters light-brown, 102–270 µm long, usually 4 cells long, cells narrowly rectangular, mostly 43–76 × 8–21 µm, thin-walled, sometimes branched.

This species, known previously only from India (Western Himalayas, Eastern Himalayas, South India ( Asthana & Srivastava 1991) and Great Himalayan National Park ( Singh & Singh 2008), is newly reported for China and known from Yunnan province.

Anthoceros bharadwajii is similar to A. alpinus and A. fusiformis var. taiwanensis in spore architecture ( Fig. 3 ). The differences between A. bharadwajii and A. alpinus were discussed under A. alpinus . Anthoceros bharadwajii resembles A. fusiformis var. taiwanensis on sporoderm ornamentation with distinct smooth strips along trilete marks. A. bharadwajii is distinct in the possession of spores with pseudolamellate sporoderms ( Fig. 3 D, E ). Thalli of A. fusiformis var. taiwanensis are strap-shaped and further separate the species ( Hasegawa 1993b).

Habitat:— Mostly on soil near roads, rarely on wet rock at 1470–2550 m in China. Distribution:— China (Yunnan) and India.

Representative specimens examined:— CHINA. Yunnan: Anning Co., Caoxi Temple, Zhenzhu Spring, on soil in forest, 13 October 1976, D.- K. Li 03264 ( SHM), Bijiang Co., Gaoligongshan, Pianma to Tingming Lake, 30 July 1978, M. Zang 5734_1 ( IFP), Gaoligongshan, Gubaofeng, on wet rock, 14 July 1978, M. Zang 5501 ( IFP), Baoshan Co. (Longyan Qu), Mangkuan Xiang, east slope of Gaoligong Shan, between Hanlong Village and Shaoxiangpingxi near Baihualing, Subtropical forest slopes with cultivated areas and Juglans trees, on soil bank by path, under Artemisia, 1545 m , 25°17'38.9"N, 98°47'54.7"E, 12 October 2007, D. G. Long & J. Shevock 37521 ( E), Cangyuan Wazu Autonomous Co., Bianfudong, 3 September 1980, S.- Y. Zeng 80-1375 ( IFP), 10 October 1980, S.- Y. Zeng 80-1813 ( IFP), Binchuan Co., Zhongyuanshan, on soil, 2 October 1991, X.- Y. Jia 910186, 910186-1 ( IFP), Gongshan Co., Bingzhongluo Village, from Jiasheng Village to Dulongjiang, on soil by road, 1846 m, 20 September 2010, Y. Yu 20100920-7, 20100920-8 ( HSNU), Gengma Daizu-Wazu Autonomous Co., Banwang Village, 29 August 1980, S.- M. Yu 80-1190 ( IFP), Jingdong Co., Ailaoshan Nature Reserve, Xujiaba, from Ecology station to Bojiba, beside a ditch, on soil, 2512 m, 24°33ʹ42"N, 101°00ʹ07"E, 23 November 2010, Y.- F. Wang 67 B ( HSNU), beside the Tea Garden, on soil, 2486 m, 24°32ʹ52"N, 101°01ʹ38"E, 24 November 2010, Y.- F. Wang 111 ( HSNU), Kunming City, Jindian Temple, on soil by road, 21 September 1976, D.- K. Li 02571 ( HSNU), Lvchuan Co., Lieshimu, on wet soil, 14 September 1973, M. Zang & X.- R. Xu 14 ( IFP), Yulong Naxizu Autonomous Co., Yulongxueshan, 6 August 1985, X.- J. Li 85556 ( IFP), Tengchong Co., Qushi Xiang, Yong’an Cun, Longchuan Jiang valley, east fork of Longchuan Jiang at Yonganqiao Bridge, river bank with exposed granite rocks and scrub, on gravelly bank of road cutting, 1470 m, 25°19'29"N, 98°36'33"E, 22 October 2003, D. G. Long 32514 ( E), Xundian Huizu and Yizu Autonomous Co., Qinglong Temple, on soil by railway, 1920 m, 1 November 1977, W.-X. Xu 77006 ( IFP), Songming Co., on soil, September 1979, G.- H. Feng 6 ( IFP), Menghai Co., Manxinglongla, near the mountain, on soil, 1840 m, 9 January 2006, T. Cao & G.- Y. Song 060913 B ( HSNU). NEPAL. Taplejung District: Tamur River near Hellok, cultivated slopes, on terrace bank, 1670 m, 27°30ʹN, 87°47ʹE, 4 September 1989, D. G. Long 16597 ( E).

Anthoceros fusiformis Austin var. taiwanensis J.Haseg., Acta Phytotax. Geobot. 44(2): 100. 1993. Type :— CHINA. Taiwan , Chiayi Hsien, Mt. Ali, Mt. Tsu-Tson-san, 2300–2900 m, S. Kurokawa 4004 (holotype TNS) .

Description: — Hasegawa (1993b).

Illustrations: — Hasegawa (1993b, p. 100, fig. 1).

Anthoceros fusiformis var. taiwanensis is characterized and recognized by strap-shaped thalli, dark brown spores, 32–42 µm in diameter, the proximal surfaces of spores with distinct and wider smooth strips along the trilete marks, spores with spinulate-lamellate outgrowths ( Hasegawa 1993b).

Habitat:— 2300–2900 m in Taiwan ( Hasegawa 1993b).

Distribution: — China ( Hasegawa 1993b). A rare species, known only from Mt. Ali and Mt. Tsu-Tsonsan, Chiayi Hsien in Taiwan.

Figures

FIGURE 2. Anthoceros angustus Steph. A. Thallus with marginal gemmae. B. Male thallus, with androecia linearly arranged along the median line. C. Gemma. D. Dehisced antheridia with orange chromoplasts in jacket cells. E. Transverse section of thallus showing large mucilage cavities. F. Elongated epidermal cells of a young capsule, showing thin-walled cells and two stomata. G. Epidermis of thallus, showing solitary chloroplasts with starch granules. H. Elongated, thin-walled pseudoelater. I, K, N, O. SEM micrographs showing proximal spore faces with distinct trilete marks and shortly papillate to spinulate-blunt protuberances. J, L, M, P. SEM micrographs showing distal spore faces with adherent studded spines forming a false lamellate pattern. A and C–M from T.Peng & J. Wang 20110520-8 (HSNU), B and D from T. Peng & J. Wang 20111011-9 (HSNU), N–P from Rev. Bretaudeau 1239 (holotype of Anthoceros angustus: G-12816). Scale bars: A, B=1 mm; C, E=100 µm; D, F, H=50 µm; G, I–P=10 µm.

FIGURE 3. Anthoceros bharadwajii Udar & A.K.Asthana. A. Dorsal epidermis of thallus with solitary chloroplasts spread across cells and round, central pyrenoids. B. Pseudoelater with thin-walls and irregular thickenings. C. Capsule epidermis with thin-walled cells and a stoma. D. SEM micrograph showing proximal face of spore marked by a distinct trilete mark and parallel wide unsculptured strips. E. SEM micrograph showing distal spore face with densely studded tuberculate-baculate projections. A–C from Y. Yu 20100920-8 (HSNU), D and E from D.-K. Li 03264 (SHM). Scale bars: A, C=50 µm; B =20 µm; D, E=10 µm.

FIGURE 5. Anthoceros subtilis Steph. A. Capsule epidermis with thin walls and stomata. B. SEM micrograph showing sporophyte fragment with tetrads and pseudoelaters. C. Pseudoelaters with thin-walls and irregular thickenings. D. SEM micrograph showing proximal face of spore which is spinulose and has distinct trilete mark. E. SEM micrograph showing distal spore face which is papillate to spinulose with spines often united at the base. All from R.-H. Dai PX95106 (GACP). Scale bars: A, C=50 µm; B, D, E=10 µm.