J. Jpn. Bot. 89: 137–141 (2014)

A New Record of Frullanoides tristis (: ) from Thailand

a, a b Jian Wang *, Xia-Fang Cheng , Soonthree Kornochalert a, and Rui-Liang Zhu **

aBryology Laboratory, School of Life Science, East China Normal University, 500, Dongchuan Road, Shanghai, 200241 CHINA; bCMU Herbarium, Department of Biology, Faculty of Science, Chiang Mai University, Chiang Mai, 50200 THAILAND *Corresponding author: [email protected] **Corresponding author: [email protected]

(Accepted on November 23, 2013)

Frullanoides tristis (Steph.) van Slageren, previously known from America, Africa and Asia, is reported here as a new generic record for the Thai bryoflora. This species is well characterized as a paroicous , with broadly ovate to ovate-oblong lobule with 6–9 teeth and each tooth 2–3 cells long, broadly ovate to suborbicular underleaves and the base with small to medium sized ears, and with the keel of female bract with an elliptic to long and narrow wing. A complete description and illustrations of F. tristis are provided.

Key words: Frullanoides tritis, new record, Ptychanthoideae, , Thailand.

Lejeuneaceae, the most speciose family record of Frullanoides for the ptychanthoid of liverworts (Marchantiophyta) has a high flora of Thailand, represented by F. tristis diversity in southeastern Asia. It is subdivided (Steph.) van Slageren. Frullanoides Raddi, into two subfamilies Lejeuneoideae and established in Raddi (1822) based on F. Ptychanthoideae (Mizutani 1961, He et al. 2012, riojaneirensis and F. densifolia collected from Gradstein 2013). Ptychanthoideae, containing Brazil, is a well-defined and neotropical genus 19 genera, is taxonomically better known than of Ptychanthoideae. The genus of Frullanoides Lejeuneoideae (Gradstein 2013). The updated comprises seven species and ranges in altitude revision of Ptychanthoideae for Thailand from sea level up to 3650 m (van Slageren 1985) contains 37 species belonging to 12 genera and the center of diversity is tropical America (Kornochalert et al. 2012). With the continuous with all seven recognized species (Gradstein discovery of new species and new records 1994). Schuster (1966) postulated that widely of bryophytes from northern Thailand, more distributed taxa are monoicous (autoicous interesting lejeuneaceous taxa will be found in or paroicous), whereas narrowly distributed this region (He et al. 2012). taxa are more often dioicous, which holds for During our recently studies of Frullanoides. Frullanoides tristis is the only Ptychanthoideae collected from Thailand, paroicous species of the genus except for some we were surprised to discover a new generic specimens of F. bahamensis and consequently

—137— 138 植物研究雑誌 第 89 巻 第 3 号 2014 年 6 月 the only widely distributed species of the genus free margin plane, with 6–9 teeth; teeth 2–4 cells known from America, Africa and Asia. Although long, erect with the upper cell(s) usually inflexed, it is the most common species of Frullanoides in 1–2 cells wide at base; hyaline papilla oblong America and Africa, F. tristis occurs sporadically or pyriform, 14–30 × 10–14 µm, one cell below in Asia reported only from India and Nepal the base of the first tooth, the apex sometimes (Grolle 1966; Awasthi and Srivastava 1988; inflexed, keel straight to slightly curved, Singh et al. 2005). smooth. Underleaves imbricate, broadly ovate to suborbicular, 0.40–0.46 × 0.42–0.50 mm, Frullanoides tristis (Steph.) van Slageren 3–4 times as wide as the stem; apex rounded- in Meded. Bot. Mus. Herb. Rijks Univ. Utrecht truncate; lateral margin slightly recurved, bases 544: 110 (1985) – Lejeunea tristis Steph. in slightly auriculate with small to medium sized Hedwigia 29: 8 (1890) – Brachiolejeunea tristis ears, 50–80 × 40–70 µm; insertion line shallowly (Steph.) Steph., Sp. Hepat. 5: 112 (1912). arched. Androecia on stems located 1–3 series of [Fig. 1] vegetative leaves below the gynoecia; bracts in Type: ETHIOPIA. Ex Herb. Hampe (G– 2–4 pairs, epistatic; bract lobe ovate, 0.60–0.80 holotype; S, W– isotypes, not seen). mm long, 0.46–0.60 mm wide; apex apiculate For further synonyms, see van Slageren and points toward the stem bases; lobule swollen (1985) and Gradstein (1994). The description of at the basal part; free margin with 5–6 teeth. the species is based on Thailand . Gynoecia terminating on stems or branches, Paroicous. Plants dull brown green when always with two pycnolejeuneoid innovations; alive, becoming brown to slight black when bract lobe oblong to obovate, 1.00–1.30 mm dry, ca. 2 cm long, 1.40–1.70 mm wide with long, 0.64–0.80 mm wide; apex obtuse or leaves. Shoots irregularly branched, branching minutely apiculate; lobule narrowly rectangular, Frullania-type, occasionally Lejeunea-type. 1/3–1/2 as long as the lobe; apex rounded to Stems 96–160 µm, transverse section consisting acute; keel with an elliptic to narrowly oblong of 12–16 thin-walled cortical cells and 20–33 wing; wing 0.48–0.56 mm long, 0.34–0.40 thick-walled medullary cells; ventral merophyte mm wide in the middle; bracteoles rectangular, 4–6 cell rows wide. Rhizoids few, brown, at base 1.00–1.30 mm long, 0.64–0.80 mm wide; apex of underleaves. Leaves imbricated; leaf lobes rounded to truncate-emarginate, plane; basal part ovate to ovate-falcate, 0.90–1.00 mm long, 0.50– of bract, bracteole and wing all inserted on the 0.70 mm wide; apex rounded or obtuse; margin innovations. Perianths exserted when mature, entire, ventral margin upcurved, dorsal margin obovoid-cylindrical, 1.00–1.32 mm long, 0.50– cordate at base. Lobe cells slightly thick-walled; 0.60 mm wide, with 10 smooth, rounded keels cell walls often with darkish pigmentation; extending over the upper 1/2–2/3 of the perianth; trigones cordate, intermediate thickenings beak 5–6 cells long. Seta articulate with 16+4 scarce, when present one per each longer cell cell pattern; capsules spherical, 0.32–0.44 mm wall; marginal cells subquadrate, 10–16 × 8–14 in diameter; elaters linear, 260–300 µm long, µm; median cells hexagonal, 24–36 × 16–24 14–24 µm wide, with one brownish, ca. 6 µm µm; basal cells slightly elongate, 28–40 × 20–30 wide spiral. Spores green, subisodiametric or µm. Oil bodies 14–23 per cell, homogeneous, triangular, 46–60 µm in diameter or 44–64 × ellipsoid or fusiformis, 3.30–5.70 × 1.50–2.20 38–46 µm, covered with numerous spinulae and µm. Ocelli absent. Lobules broadly ovate to eight rosettes. ovate-oblong, 0.60–0.70 mm long, 0.34–0.46 Specimens examined: Thailand. Chiang Mai Province: Doi Laung Chiang Dao, 19°23'43.32"N, 98°51'30.25"E, on mm wide, 3/5–2/3 as long as the lobe, gradually tree trunks or vine, 1510–1960 m, 18 Dec. 2011, R.-L. Zhu flattened towards the free margin; apex oblique, 20111218-30B, R.-L. Zhu 20111218-55C (HSNU). June 2014 The Journal of Japanese Botany Vol. 89 No. 3 139

Fig. 1. Frullanoides tristis. 1. Shoot, ventral view. 2. Shoot, dorsal view. 3. Portion of shoot with perianths and androecium, ventral view. 4. Stem section. 5. Marginal lobe cells. 6. Median lobe cells, showing cordate trigones. 7. Basal lobe cells. 8. Median lobe cells. showing homogeneous oil bodies. 9. Female bracteole. 10. Female bract, showing the wing. 11. Apex of leaf lobule, showing a hyaline papilla (arrow), inner surface. 12, 13. Underleaves. 14. Elater. 15. Spores. 16. Cross section of perianth. 17–19. Leaves. 20, 21. Leaf lobule, showing 8–9 lobule teeth. 22. Male bract. 1, 2, 12, 13, 17–21 from R.-L. Zhu 20111218-30B (HSNU); the others from R.-L. Zhu 20111218-55C (HSNU). 140 植物研究雑誌 第 89 巻 第 3 号 2014 年 6 月

Distribution and ecology: Frullanoides Frullanoides tristis is most closely related tristis almost exclusively epiphytic grows on to and was synonymized with F. liebmanniana bark, trunks, stems and twigs of living trees and by Gradstein (1990). The two species can easily shrubs, occasionally epiphyllous, rarely on logs be separated by the dioicous inflorescence, flat or shaded rocks (van Slageren 1985, Singh et ventral margin and the very large lobule with al. 2005). This species usually occurs at rather 3–5 small teeth in F. liebmanniana (paroicous low elevations below 1000 m, rarely up to inflorenscence, upcurved ventral margin and 2000 m in the neotropics, however, it can reach the smaller lobule with 6–9 distinct teeth in F. much higher elevations in Africa and Nepal. In tristis). Thailand, the species occurs from 1510–1960 Although F. tritis was described and m and growing on tree trunks and vines illustrated by Grolle (1966 as Brachiolejeunea intermingled with Lejeunea flava (Sw.) Nees, poeltii), van Slageren (1985) and Gradstein Frullania sp. and Radula sp. (1994), and the oil bodies was illustrated by Awasthi and Srivastava (1988), the detailed Discussion descriptions of the oil bodies in this species is Frullanoides is most closely related to provided here for the first time and the oil bodies Acrolejeunea (widely distributed in Thailand) of F. tristis are similar to those of other species and to the Asiatic genus Trocholejeunea. of the genus. The species Frullanoides, however, can easily be recognized by their somewhat The first author thanks Prof. S. R. Gradstein blackish pigmentation, more or less and Dr. Phiangphak Sukkharak for providing auriculate underleaves, and the presence of literature. We are grateful to two anonymous pycnolejeuneoid innovations. The genus of reviewers for constructive comments on the Trocholejeunea is immediately distinguished manuscript. This research was supported by the from Frullanoides by their lack of blackish National Natural Science Foundation of China secondary pigmentation, non-articulate seta (nos. 31170190, 31300171), PhD Program with 16–17 rows of outer cells and 8–10 rows Scholarship Fund of ECNU 2009, and the of inner ones, and the presence of the Frullania- Fundamental Research Funds for the Central type innovations. Universities. The distinctive features of F. tristis are (1) paroicous plant, (2) lobule with 6–9 teeth References and each tooth 2–3 cells long, (3) the base of Awasthi U. S. and Srivastava S. C. 1988. Status of underleaves with small to medium sized ears, Brachiolejeunea (Spruce) Schiffn. in India. Proc. Ind. Acad. Sci. (Plant Sci.) 98: 1–12. (4) the keel of female bract with an elliptic to Gradstein S. R. 1990. A key to the New World species of long and narrow wing. The main diagnostic holostipous Lejeuneaceae. Trop. Bryol. 3: 45–57. character of the species is that F. tristis is the Gradstein S. R. 1994. Lejeuneaceae: Ptychanthoideae, only paroicous species of the genus Frullanoides Brachiolejeuneae. Fl. Neotrop. 62: 1–216. except for some specimens of F. bahamensis. Gradstein S. R. 2013. A classification of Lejeuneaceae (Marchantiophyta) based on molecular and The latter, however, differ from F. tristis by morphological evidence. Phytotaxa 100: 6–20. the absent underleaf ears and the small size of Grolle R. 1966. Die Lebermoose Nepals. In: Hellmich W. plants (1.0–1.6 mm wide vs 1.4–2.2 mm wide). (ed.), Khumbu Himal, Ergebn. Forsch. Unternehm. As the lobe of male bract is similar to the lobe Nepal Himalaya 1: 262–298. He Q., Zhu R.-L., Chantanaorrapint S., Kornochalert S. of vegetative leaf, F. tristis was erroneously and Printarakul N. 2012. Drapanolejeunea laciniata describe as a dioicous plant by Singh et al. (Lejeuneaceae), a new species from northern Thailand. (2005) Cryptog., Bryol. 33: 291–298. June 2014 The Journal of Japanese Botany Vol. 89 No. 3 141

Kornochalert S., Santanachote K. and Wang J. Schuster R. M. 1966. The Hepaticae and Anthocerotae of 2012. Lejeuneaceae subfamily Ptychanthoideae North America. I. Columbia University Press, New (Marchantiophyta) in Thailand. Cryptog., Bryol. 33: York. 39–63. Singh A. P., Nath V. and Asthana A. K. 2005. Frullanoides Mizutani M. 1961. A revision of Japanese Lejeuneaceae. J. tristis (Steph.) van Slageran a new addition to east Hattori Bot. Lab. 24: 115–302. Himalayan bryoflora. Cryptog., Bryol.26 : 435–440. Raddi G. 1822. Crittogame brasiliane raccolte e descritte Slageren M. W. van. 1985. A taxonomic monograph of the dal Signor Guiseppe Raddi. Memoria. Modena, pp. genera Brachiolejeunea and Frullanoides. Meded. Bot. 1–33 (preprint). (Also published in Mem. Mat. Fis. Mus. Herb. Rijks Univ. Utrecht 544: 1–309. Soc. Ital. Sci. Modena 19: 27–57. 1823).

J. Wanga，X.-F.Chenga，S. Kornochalertb，R.-L. a Zhu ：Frullanoides tristis（クサリゴケ科，苔類），タ イに産する 2011 年の現地調査でタイからクサリゴケ科の 1 種， づいて記載と図を付し，標本は華東師範大学の標本庫 Frullanoides tristis (Steph.) van Slageren を初めて見出 (HSNU) に収めた． した．本種は広く熱帯に分布するがアジアからはネパー （a 中国・華東師範大学 School of Life Science， ルとインドから報告があった．タイ産の植物体にもと b タイ・Chiang Mai 大学理学部生物学教室 CMU 標本館）