Botánica-Sistemática http://www.icn.unal.edu.co/ Caldasia 33(2):367-396.Gradstein & Uribe 2011 A synopsis of the Frullaniaceae () from Colombia Sinopsis de la familia Frullaniaceae (Marchantiophyta) para Colombia

Robbert Gradstein Muséum National d’Histoire Naturelle, Dept. Systématique et Evolution, UMS 7205, Case Postale 39, 57 rue Cuvier, 75231 Paris cedex 05, France.

Jaime Uribe-M. Instituto de Ciencias Naturales, Facultad de Ciencias, Universidad Nacional de Colombia, Apartado 7495, Bogotá D.C., Colombia. [email protected] Abstract Frullania (Frullaniaceae) is the second-largest liverwort genus of Colombia (after Plagiochila), with 59 recorded in six subgenera. In this paper keys are provided for the identification of 42 Frullania species reported from Colombia together with brief descriptions of their main morphological characters, distribution, habitat and elevation in the country, as well as worldwide distribution. Some species recorded from neighbouring countries, but not yet from Colombia, are also included in the keys. The remaining species reported from Colombia are considered doubtful taxa. Frullania apollinarii Steph. is a new synonym of F. lobato-hastata Steph.

Key words. Colombia, elevational distribution, Frullania, identification keys, liverworts, Marchantiophyta, world distribution-

Resumen Frullania (Frullaniaceae) es el segundo género en número de especies de Colombia (después de Plagiochila), con 59 especies en seis subgéneros. En este artículo se proveen claves para la identificación de 42 especies de Frullania registradas para Colombia, además se incluyen breves descripciones de los caracteres morfológicos diagnósticos, distribución, hábitat y gradiente altitudinal en el país, así como la distribución mundial. Algunas especies registradas de países vecinos, pero aún no registradas para Colombia son incluidas en la clave. Las demás especies registradas para Colombia se consideran taxones dudosos. Frullania apollinari Steph. es un nuevo sinónimo de F. lobato-hastata Steph.

Palabras clave. Colombia, distribución altitudinal, Frullania, claves de identificación, hepáticas, Marchantiophyta, distribución mundial.

INTRODUCTION et al., 2001, with updates). In Colombia, Frullania is the second-largest liverwort The liverwort family Frullaniaceae consists genus (after Plagiochila) with 59 species. of two genera, Frullania with about 300- The first records from Colombia were 350 species worldwide and Neohattoria by Alexander von Humboldt and Aimée with one species in eastern Asia (Gradstein Bonpland who collected Frullania atrata 367 Frullaniaceae from Colombia

(Sw.) Nees (as Jungermannia atrata Sw.) and peruviana; Uribe, 2008) and F. mucronata F. riojaneirensis Raddi (as Jungermannia (Lehm. & Lindenb.) Lehm. & Lindenb. (= F. obscura Sw.) between Popayán and brasiliensis; Uribe & Gradstein, 2003). Almaguer, Dept. Cauca (Kunth, 1822). Gottsche (1864) reported 17 species from In this paper, keys are provided for the various localities based on specimens identification of 42 species of Frullania collected by Alexander Lindig and by José from Colombia which we have been able Jeronimo Triana. The majority of these to recognize with certainty. A few well- early collections from Colombia have not defined species known from neighbouring been re-examined critically; those studied countries but not yet from Colombia are also by Gottsche were presumably destroyed in included in the keys. For each species from 1944 with the bombing of the herbarium of Colombia a brief characterization is given of Berlin. A further 30+ species were reported its distribution, habitat and elevation in the as new to Colombia by Jack & Stephani country, its world distribution, as well the (1892), Stephani (1901-1905), Herzog (1942, main diagnostic morphological characters 1955), Bonner (1965), Robinson (1967) and separating the species from related ones. The others. Stotler (1969) in his revision of the remaining species recorded from Colombia neotropical species of Frullania subgenus are little known taxa that need more study and Thyopsiella Spruce (as subg. “Frullania”) may turn out to be synonyms; they are listed accepted 10 species for Colombia and under “Doubtful taxa” or mentioned briefly in reduced several others to synonymy. Yuzawa the discussions under the species. (1991) in his world monograph of subgenus Chonanthelia Spruce recorded 19 species The species are keyed according to the six from Colombia. subgenera to which they are traditionally assigned (Spruce, 1884; Uribe, 2008): The first edition catalogue of the liverworts subg. Chonanthelia with 17 species from and hornworts of Colombia by Gradstein Colombia, subg. Diastaloba with 2 species, & Hekking (1979) listed 58 species of subg. Frullania (= Trachycolea) with 1 Frullania for the country. This number has species, subg. Homotropantha with 1 species, remained almost unaltered in subsequent subg. Meteoriopsis with 4 species and editions (Uribe & Gradstein, 1998; Gradstein subg. Thyopsiella with 17 species. A first & Uribe, in press) in spite of intensive morphological-phylogenetic analysis of the recent collecting activities and discovery of genus Frullania (Uribe, 2008) recovered species new to the country, such as F. kunzei four of these subgenera as monophyletic s.l. (Pinzón et al., 2003) and F. dulimensis Uribe (incl. paraphyly; Hörandl & Stuessy, 2010): (Uribe, 2006). Thus, the second edition subg. Frullania, subg. Homotropantha, subg. of the catalogue lists 58 species (Uribe & Meteoriopsis and subg. Thyopsiella. The Gradstein, 1998) and the third edition 59 subgenera Chonanthelia and Diastaloba, species (Gradstein & Uribe, in press). The however, proved to be polyphyletic. Hentschel lack of increase in the number of species is et al. (2009) in a molecular-phylogenetic explained by the reduction of various species study based on a broader sampling confirmed to synonymy, thus counterbalancing the new the polyphyly of subg. Diastaloba and floristic records. Examples of recent new the monophyly of subg. Frullania and synonymy include F. atrosanguinea Tayl. subg. Homotropantha; in addition, subg. (= F. peruviana; Uribe, 2008), F. crinoidea Chonanthelia turned out to be monophyletic Spruce ex Steph. (= F. atrata; Uribe & in the latter study. Subgenus Thyopsiella, Gradstein, 2003), F. mathanii Steph. (= F. however, was recovered as two poorly 368 Gradstein & Uribe supported clades, a “temperate” clade cuencensis, dusenii, ecuadorensis, gibbosa, containing the type of subg. Thyopsiella intumenscens, kunzei, macrocephala, (F. tamarisci) and a few other species, montagnei, pittieri, setigera and a “tropical” clade which included the Andes, sometimes extending to Central majority of the Thyopsiella species and the America and Mexico: grandifolia, laxiflora, type of subg. Meteoriopsis (F. peruviana). paradoxa, peruviana, pluricarinata, Accordingly, the temperate clade was called sphaerocephala, standaertii, tetraptera, subg. Thyopsiella and the tropical clade was tunguraguana, winteri called subg. Meteoriopsis. In the present treatment, however, we have retained the Table 1. ���������Number of Frullania species recorded six subgenera of neotropical Frullania from the Departments of Colombia. as traditionally circumscribed. The new Department # Frullania species defintions of Thyopsiella and Meteoriopsis Amazonas 3 proposed by Hentschel et al. (2009) must be Antioquia 10 considered premature due to the lack of robust support for the two clades and the very limited Arauca 0 sampling of the subgenus Meteoriopsis. A Atlántico 0 reclassification of the polyphyletic subgenus Bolívar 0 Diastaloba, finally, should await the urgently Boyacá 21 needed systematic revision of this group, Caldas 4 especially of the neotropical species which Caquetá 0 have not been studied critically. Casanare 6 Cauca 11 DISTRIBUTION PATTERNS Cesar 8 Chocó 8 About half of the species of Frullania Córdoba 0 recorded from Colombia (22) have very wide Cundinamarca 26 geographical ranges and occur throughout Guainía 0 tropical America, from Mexico to southern Guaviare 0 Brazil (see below). Six of them also occur Huila 7 in the Old World tropics and are pantropical La Guajira 0 species. The remaining species (20) are largely restricted to the Andes; some of these Magdalena 10 extend to the mountains of Central America Meta 5 and Mexico and one species (F. standaertii) Nariño 4 occurs also in East Africa. Eight Andean Norte de Santander 2 species occur only in the northern Andes, from Putumayo 2 northern Peru to Venezuela (sometimes also in Quindío 13 Costa Rica) and two species (F. bogotensis, F. Risaralda 19 S a n A n d r é s y dulimensis) are only known from Colombia. 0 The geographical distribution patterns of Providencia Santander 17 the Colombian species of Frullania are as Sucre 0 follows: Pantropical: apiculata, arecae, ecklonii, Tolima 15 ericoides, nodulosa, riojaneirensis Valle del Cauca 7 Neotropical: atrata, beyrichiana, brasiliensis, Vaupés 0 caulisequa, confertiloba, convoluta, Vichada 0 369 Frullaniaceae from Colombia

Northern Andes, sometimes extending Table 2. Altitudinal distribution of Colombian to Costa Rica: bicornistipula, clandestina, Frullania. formosa, jelskii, lobato-hastata, meridana, Altitudinal belt Number of species mirabilis, ringens 0-1000 m 15 Colombia only: bogotensis, dulimensis 1000-2000 m 30 2000-3000 m 25 The distribution of the species within 3000-4000 m 20 Colombia is still incompletely known.� above 4000 m 8 The largest number of species is known from Cundinamarca (26 spp.), followed by Boyacá (21 spp.), Risaralda (19 spp.) The number of Frullania species decreases and Santander (17 spp.). �����������������Eight departments to the páramo (17 spp.) but no species of have 5-15 species (Casanare, Cesar, Chocó������,� Frullania is exclusive to the páramo belt Huila, Magdalena, Meta, �Quindío���������������,��������� Tolima, even though F. decidua has been found only Valle de Cauca), 5 departments have 2-4 in páramo at 3800. The latter species occurs species (Amazonas, Caldas, Nariño, Norte de in Ecuador at much lower elevation in the Santander, Putumayo) and 12 departments are forest belt (type location!), indicating that without any species record (see Table 1). The its distribution in Colombia is insufficiently departmental species richness reflects on the known. Species richness is lowest in the one hand the very uneven collecting intensity submontane and lowland areas with only in the different departments, on the other hand 10 and 13 species, respectively. Frullania it shows the typically montane distribution of kunzei and F. nodulosa, are only known from Frullania in Colombia with more than 95% Amazonia below 500 m. The latter two are of the species occurring in the Andean region, common and widespread lowland taxa of above 1000 m. tropical America and F. nodulosa occurs also in tropical Africa and Asia. A third species The elevational distribution of the species recorded from Amazonia, F. caulisequa, is diversity of Frullania in Colombia is typically also known from the Andean region where it hump-shaped which the highest diversity is reported up to 3000 m. The high-Andean (75% of the species) occurring at mid- records of this species should be checked, elevations, between 1000- 2000 m (Table however, because elsewhere in tropical 2). The elevational distribution pattern of America F. caulisequa is a lowland or lower Frullania in Colombia is similar to that of montane species (Gradstein & Costa, 2003; liverworts in general (Uribe & Gradstein. León-Yánez et al., 2006). Possibly, confusion 1999; data from 750 spp.) and apparently with some other member of the subgenus reflects the prevalence of epiphytism in Diastaloba to which F. caulisequa belongs liverworts and the preference of liverworts has occurred. Such confusion may well have for humid ecological conditions. Similar happened since the neotropical species of hump-shaped richness patterns with peaks at subg. Diastaloba have not been revised and mid-elevations have been reported for other are still very poorly known. groups, for example Melastomataceae and ferns, which like liverworts have strong KEYS AND DESCRIPTIONS ecological preferences for humid conditions (Kessler, 2000; Kluge et al., 2006). The Frullania Raddi elevation pattern of species richness detected small to large, reddish-green to in Frullania may thus be similar to that of reddish-brown or purplish, sometimes pure many other plant groups of Colombia. green, creeping, ascending or pendent, 370 Gradstein & Uribe regularly or irregularly 1-3-pinnately 1. Introductory Key branched. Branches Frullania-type; innovations normally lacking. Stems rigid, 1. Lobules distant from the stem, space made up of thick-walled cells. Leaves between stem and lobule wider than the incubous with a very short, subtransverse width of the lobule. Plants very small, insertion, divided into a large dorsal lobe, creeping ...... Key 2 (subg. Diastaloba) a smaller ventral lobule, and a small stylus 1. Lobules close to the stem, space between between lobule and stem. Leaf lobe usually stem and lobule narrower than the width of ovate-orbicular, apex rounded to acute to the lobule. Plants small or large ...... 2 acuminate, margins entire, rarely toothed. 2. Lobules pendent, opening of the lobule Leaf lobule almost free from the dorsal positioned toward the stem or the apex lobe, rounded to elongate, transformed into of the plant. Amazonian lowlands (subg. a sac or flattened, or both. Stylus usually Homotropantha) ...... F. nodulosa linear and minute, rarely large, foliar. Cells 2. Lobules upright, opening of the lobule isodiametrical to (more often) elongate, positioned toward the base of the plant ...3 usually with trigones and intermediate 3. Lobules with a long or short flattened lower thickenings, the trigones often confluent and portion (flattened portion sometimes very cell walls often irregularly undulate-sinuose, short!). Ventral surface of perianth with 2-6 cuticle smooth; oil bodies finely granular; keels ...... Key 3 (subg. Chonanthelia) ocelli sometimes present. Underleaves small 3. Lobules without flattened lower portion. or large, 2-lobed, rarely undivided. Rhizoids Ventral surface of perianths with 0-1(-4) in bundles from underleaf bases. Dioicous keels ...... 4 or autoicous, rarely paroicous. Androecia 4. Leaves distinctly squarrose when moist, usually on a short, globose male branch brittle. Lobules as long as wide. Surface with a few pairs of bracts and bracteoles. of perianth rough by scattered tubercles Gynoecia on short or elongate shoots, each or scale-like outgrowths (subg. Frullania) with 2-5 archegonia. Perianths flattened ...... F. ericoides or inflated, with 0-14 keels, the mouth 4. Leaves not squarrose, not brittle. Lobules contracted into a beak. Seta of numerous longer than wide. Surface of perianth rows of cells. Foot of the sporophyte not without tubercles or scale-like outgrowths, penetrating into the stem. Capsule globose, smooth ...... 5 wall 2-layered. Elaters attached to the 5. Plants long-pendent from branches in cloud capsule valves, arranged vertically inside forest. Leaf bases with 2 very large auricles, the capsule, with 2-3-spirals. Spores large, the auricles similar in size. Leaves convolute multicellular, germination endosporic. around the stem both when dry and when Vegetative reproduction rare, by caducous moist ...... Key 4 (subg. Meteoriopsis) or fragmenting leaves. 5. Plants not long-pendent. Auricles at leaf bases lacking or not similar in size, the Keys to the species of Frullania from dorsal auricle distinctly larger than the Colombia ventral auricle. Leaves ± convolute when dry, spreading when moist ...... Some species recorded from Ecuador and/or ...... Key 5 (subg. Thyopsiella) Venezuela that may occur in Colombia but are not yet known from the country are also included in the key [in brackets].

371 Frullaniaceae from Colombia

Key 2. Frullania subgenus Diastaloba 6. Free margin of the laminate portion of the lobule plane, not folded below the beak. 1. Leaf apex always rounded. Plants creeping, Laminate portion of lobule not wider than regularly or irregularly branched ...... the sac. Very common species ...... F. caulisequa ...... F. riojaneirensis 1. Leaf apex at least in some leaves apiculate. 7. Lobule with a distinct beak ...... Plants regularly (bi)pinnate, ascending from ...... F. tunguraguana the substrate ...... 2 7. Lobule without beak ...... 8 2. Dorsal leaf base distinctly auriculate. 8. Female bracts and bracteoles densely Female bracts strongly toothed. Known imbricate and incurved, forming a globose from Ecuador, not yet recorded from head. Stylus minute, 1(-2) cells long. Colombia ...... [F. serrata Gottsche] Dioicous ...... F. sphaerocephala 2. Dorsal leaf base not auriculate. Female 8. Female bracts and bracteoles spreading, bracts entire ...... F. apiculata not forming a globose head. Stylus 2-3 cells long. Monoicous ...... F. ecklonii Key 3. Frullania subgenus Chonanthelia 9. Leaf apex acute. Described from Ecuador, not yet recorded from Colombia ...... 1. Lobules on the main stem with a very long ...... [F. haematocysta Spruce] laminate (= flattened) portion, which extends 9. Leaf apex broadly rounded ...... 10 downwards beyond the ventral margin of 10. Leaves distinctly squarrose when moist. the leaf lobe (sect. Cladocarpicae) ...... 2 Stylus large, rounded ...... F. gibbosa 1. Lobules on the main stem with a short 10. Leaves plane when moist. Stylus filiform laminate portion, which does not extend or lanceolate, not rounded ...... 11 beyond the ventral margin of the leaf lobe 11. Base of the laminate portion of the lobule (sect. Chonanthelia) ...... 9 folded upwards ...... F. winteri 2. Margins of leaves and underleaves strongly 11. Base of the laminate portion of the lobule undulate. Perianth 8-10-keeled ...... F. arecae plane ...... 12 2. Margins not undulate, plane. Perianth 4- 12. Stylus 10-25 cells long and 4-8 cells wide keeled or 8-10-keeled ...... 3 ...... F. standaertii 3. Stylus large, more than 0.3 mm long, 12. Stylus less than 10 cells long ...... 13 suborbicular. Perianth 4-keeled ...... 13. Underleaves on main stem maximally 3 ...... F. confertiloba times as wide as the stem, distant ...... 14 3. Stylus small, less than 0.1 mm long, filiform 13. Underleaves on main stem more than 3 times ...... 4 as wide as the stem, distant or imbricate ... 4. Laminate portion of the lobule toothed...... 16 Perianth 8-10-keeled ...... F. ringens 14. Underleaves more than 2 times wider 4. Laminate portion of the lobule entire .....5 than the stem, bifid to 1/3. Lobule with a 5. Perianth 4-keeled. Lobule with a distinct beak. Dioicous. Montane forest species beak, formed by the sac extending narrowly ...... F. cuencensis downwards along the free margin of the 14. Underleaves smaller, 1-2 times wider than laminate portion ...... 6 the stem, bifid to 1/6-1/4. Lobule without 5. Perianth 8-14-keeled. Lobule with or beak. Monoicous. Montane forest and without beak ...... 7 páramo ...... 15 6. Free margin of the laminate portion of 15. Perianth 8-10-keeled. Montane forest the lobule strongly folded below the beak...... F. pluricarinata Laminate portion of lobule wider than the 15. Perianth 4-keeled. Páramo ...... sac. Rare species ...... F. bogotensis ...... F. tetraptera 372 Gradstein & Uribe

16. Laminate portion of the lobule large, to toothed. Perianth not exserted beyond the ca. 0.85 mm long. Lobule with a distinct bracts ...... F. grandifolia beak, formed by the sac extending narrowly 4. Underleaf base without auricles. Underleaves downwards along the free margin of the narrow elongate, at least 2 x longer laminate portion ...... 17 than wide ...... F. peruviana 16. Laminate portion of the lobule very small, 4. Underleaf base with very large auricles less than 0.4 mm long. Lobule not beaked (more than 0.15 mm long). Underleaves ...... 18 less than 2 x longer than wide. Known 17. Perianth 4-keeled. Underleaves with large from Ecuador and Venezuela; not yet auricles, auricles approaching each other recorded from Colombia ...... F. laxiflora ...... [F. phalangiflora Steph.] 17. Perianth 8-10-keeled. Underleaves with small auricles, auricles not approaching each Key 5. Frullania subgenus Thyopsiella other. Known from Ecuador, Venezuela and Costa Rica, not yet recorded from Colombia 1. Leaf apex very long and finely acuminate, ...... [F. planifolia Steph.] the acuminate portion to 1 mm long. Known 18. Underleaf apex undivided. Underleaf from Ecuador; not yet recorded from bases with very large auricles, the auricles Colombia ...... [F. aculeata Taylor] ± touching each other. Described from 1. Leaf apex not very long and finely acuminate Venezuela, not yet recorded from Colombia ...... 2 ...... [F. holostipula Hatt. & Griffin] 2. Lobules short, 1-1.5 × longer than wide. 18. Underleaf apex short bifid. Underleaf Plants very small, 0.5-1 mm wide, tightly bases without or with small auricles ...... 19 prostrate. Cells in the upper part of the leaf 19. Underleaves ± rounded. Mouth of the lobes isodiametrical, evenly thickened, lobule narrow (ca. ½ the width of the without trigones. Dorsal leaf base not lobule). Lobule surface folded in the middle auriculate ...... F. kunzei ...... F. dusenii 2. Lobules 1.5-3 × longer than wide. Plants 19. Underleaves longer than wide. Mouth larger. Cells in the upper part of the leaf of the lobule wide (almost as wide as the lobes longer than wide, with trigones. lobule). Lobule surface smooth, not folded Dorsal leaf base auriculate ...... 3 ...... F. jelskii 3. Leaf apex apiculate to acuminate ...... 4 3. Leaf apex rounded to subacute (never Key 4. Frullania subgenus Meteoriopsis apiculate to acuminate) ...... 13 4. Underleaves reniform (much wider than 1. Leaf margins toothed ...... F. dulimensis long), underleaf apex broadly truncate and 1. Leaf margins entire ...... 2 with 2 small, subulate teeth ...... 2. Leaf apex rounded to obtuse. Female bracts ...... F. bicornistipula entire (rarely toothed: F. grandifolia) .....3 4. Underleaves rounded, ovate to oblong, 2. Leaf apex acute to acuminate. Female bracts not reniform; underleaf apex not broadly toothed ...... 4 truncate with 2 small teeth ...... 5 3. Underleaves ovate-oblong, 1.4-2 x longer 5. Underleaf apices long acuminate. Lamina than wide, not overlapping. Female bracts of first branch underleaf undivided, long entire. Perianth distinctly exserted beyond acuminate ...... F. setigera the bracts ...... F. convoluta 5. Underleaf apices acute or obtuse. Lamina 3. Underleaves suborbicular, 1-1.3 x longer of first branch underleaf bifid or undivided, than wide, overlapping. Female bracts rounded to subacute ...... 6

373 Frullaniaceae from Colombia

6. Leaf apex distinctly recurved, apiculate ..7 stem, imbricate. Underleaf margins plane 6. Leaf apex plane ...... 8 ...... F. clandestina 7. Stylus sometimes with a small foliose 15. Underleaves smaller, less than 3 times as appendage at the base, ca. 5-10 cells long wide as the stem, distant to subimbricate. and 3-7 cells wide (underleaves must Underleaf margins recurved or plane ....16 be carefully removed to examine this 16. Plants small, less than 1 mm wide when character). Perianth sharply 3-keeled ...... moist. Lobules often diverging from the ...... F. intumescens stem at an oblique angle. Underleaves as 7. Stylus without foliose appendage. Perianth long as wide, deeply bifid (to ½), underleaf terete or with 3 weak, broad keels near the margins plane ...... F. ecuadorensis apex ...... F. brasiliensis 16. Plants larger. Lobules standing upright, 8. Leaf apex long mucronate to acuminate ± parallel to the stem. Underleaves longer ...... F. pittieri than wide, less deeply bifid (to 1/5-1/3) ...17 8. Leaf apex obtuse to acute to short apiculate 17. Underleaves imbricate, margins strongly ...... 9 recurved. Lamina of the first branch 9. Underleaves almost as large as the leaf underleaf undivided. Margins of female lobes, 3-4 times as wide as the stem, bracts and bracteoles entire .....F. montagnei imbricate ...... 10 17. Underleaves distant to subimbricate, 9. Underleaves much smaller than leaf lobes, margins plane or slightly recurved. Lamina 2-3 times as wide as the stem, distant or of the first branch underleaf bifid. Margins imbricate ...... 11 of female bracts and bracteoles toothed 10. Underleaves longer than wide, distant ...... F. paradoxa ...... F. meridana 10. Underleaves rounded or wider than long, Alphabetical treatment of the Frullania imbricate ...... F. formosa species of Colombia 11. Perianth terete. Female bracts entire ...... F. macrocephala 1. Frullania apiculata (Reinw. et al.) Nees 11. Perianth 3-keeled. Female bracts toothed or entire ...... 12 On bark of trees in lowland and montane rain 12. Underleaf margins recurved ...... F. atrata forest, from sea level to 3000 m. Recorded 12. Underleaf margins plane ...... from Chocó, Quindío and Santander. World ...... F. beyrichiana (incl. F. breuteliana) distribution: pantropical. 13. Ventral leaf base with 2 long and narrow Frullania apiculata (subg. Diastaloba) is appendages, one hanging down and the recognized by the regularly (bi)pinnate other standing up, parallel to the stem branching and the apiculate leaf apex. The ...... F. mirabilis species is common throughout the tropics 13. Ventral leaf base without long appendages and has been described and illustrated ...... 14 in detail by Hattori (1973, 1980) for 14. Underleaves with long undulate auricles, Asia and by VandenBerghen (1976) for auricles ½ or more the length of the Africa. Frullania exilis, described from the underleaf (underleaf length measured from Neotropics and recorded from Colombia, the middle of the insertion to the apex) has been considered a synonym of F...... F. lobato-hastata apiculata (e.g. Gradstein & Ilkiu-Borges, 14. Underleaves without or with short auricles 2009) but this synonymy was not based on ...... 15 examination of type materials and needs 15. Underleaves about as large as the leaf confirmation. lobe, more than 3 times as wide as the 374 Gradstein & Uribe

2. Frullania arecae (Spreng.) Gottsche Fig. 1 distribution: tropical America. Frullania beyrichiana (subg. Thyopsiella) On bark and rock, 1600-3400 m. Recorded is very similar to F. atrata (see under the from Boyacá, Casanare, Cauca, Cesar, latter species). Frullania breuteliana, which Cundinamarca, Huila, Magdalena, Quindío, has been reported from Colombia, may be Risaralda, Santander and Tolima. World a synonym of F. beyrichiana and seems to distribution: pantropical. differ from F. beyrichiana only in the slightly Frullania arecae (subg. Chonanthelia) is a longer leaftip and the somewhat toothed very conspicuous, robust plant with undulate female bracts (entire in F. beyrichiana; see margins of leaves and underleaves. The Stotler, 1969). perianth of F. arecae is 10-keeled and is surrounded by a large and strongly toothed, 5. Frullania bicornistipula Spruce flower-like involucre. The species has been confused with F. ecklonii (Yuzawa, 1991), On bark of trees and soil, 1500-2300 m. but the leaf and underleaf margins in the latter Recorded from Cauca, Huila, Norte de speciers are not undulate. Santander and Risaralda. World distribution: northern Andes and Costa Rica. 3. Frullania atrata (Sw.) Nees Fig. 2 Frullania bicornistipula (subg. Thyopsiella) is a very characteristic species which is Frullania crinoidea Spruce ex Steph. (syn. immediately recognized by the reniform fide Uribe & Gradstein, 2003) underleaves with a broad truncate apex On bark of trees in montane rain forests, bearing 2 short, subulate teeth. The two small 600-3000(-4000) m. Recorded from teeth are standing upwards and separated from Antioquia, Boyacá, Casanare, Cauca, Cesar, each other by some distance. The long filiform Cundinamarca, Huila, Magdalena, Meta, stylus, 6-12 cells long, is another characteristic Santander and Tolima. World distribution: feature of Frullania bicornistipula. tropical America. By the long mucronate leaf apex Frullania Frullania atrata (subg. Thyopsiella) has bicornistipula is similar to F. pittieri but the often been misidentified and confused with peculiar underleaves of F. bicornistipula members of the subgenus Meteoriopsis such readily separate the two species. as F. convoluta and F. peruviana. However, Uribe & Gradstein (2003) showed that F. 6. Frullania bogotensis Steph. Fig. 1 atrata is a member of the subgenus Thyopsiella On logs, 700 m. Recorded from Boyacá, and possibly related to F. intumescens, which Cundinamarca and Santander. World differs by strongly recurved leaf apices (plane distribution: only known from Colombia. in F. atrata). Frullania atrata is also close to Frullania bogotensis (subg. Chonanthelia) F. beyrichiana, which differs from F. atrata is closely related to F. riojaneirensis but by the plane underleaf margins (recurved in F. differs from the latter species by the laminate atrata). The relationships of F. atrata to other portion of the lobule being broader than the members of the subgenus Thyopsiella remain sac (narrower than the sac in F. riojaneirensis) poorly known and need more study. and having a folded margin (Yuzawa, 1991).

4. Frullania beyrichiana (Lehm. & Lindenb.) 7. Frullania brasiliensis Raddi Fig. 3 Lehm. &���������� Lindenb. Frullania mucronata (Lehm. & Lindenb.) On bark of trees, 1800-2100 m. Recorded Lehm. & Lindenb. (syn. fide Uribe & from Antioquia and Cundinamarca. World Gradstein, 2003) 375 Frullaniaceae from Colombia

Figure 1. Frullania bogotensis Steph. A. Leaf lobule. B. Perianth. C and D. Underleaves. E. Stem-leaf, dorsal view. Frullania arecae (Spreng.) Gottsche. F. Part of shoot, ventral view. G. Perianth. H. Underleaf. I. Ventral lobule.

376 Gradstein & Uribe

Figure 2. Frullania atrata (Sw.) Nees. A. Part of shoot, ventral view. B. Stem leaf. C. Underleaf. D and E. Leaf lobules. F. Initial branching appendages. G. Underleaf. H. Stylus.����������� Reproduced from Cryptogamie, Bryologie with permission.

377 Frullaniaceae from Colombia

Common on bark of trees, logs, soil, or rock, 9. Frullania clandestina (Nees & Mont.) 1200-3900 m. Recorded from Antioquia, Nees Boyacá, Caldas, Cauca, Cesar, Chocó, Cundinamarca, Huila, Magdalena, Meta, On bark of trees, 1500 m. Recorded from Nariño, Quindío, Risaralda, Santander, Cauca. World distribution: northern Andes Tolima and Valle del Cauca. World (Colombia, Ecuador, Peru). distribution: common and widespread in Frullania clandestina (subg. Thyopsiella) is tropical America. a rare species from lower montane elevation Frullania brasiliensis is the most common in the northern Andes. The species is neotropical species of subg. Thyopsiella and recognized by the rounded leaf apex and the is recognized by the recurved, apiculate leaf large underleaves which are about as large apices and the terete perianth. Moreover, as the leaf lobes and imbricate. By its large the underleaf margins are always recurved. underleaves, F. clandestina resembles F. According to Stotler (1969), F. brasiliensis formosa Spruce but in the latter species the has deeply bifid underleaves (to 1/3), leaf apex is apiculate. however in material from Colombia and Ecuador of F. brasiliensis the underleaf 10. Frullania confertiloba Steph. Fig. 4 incision varies considerably in depth (1/5- 1/3). On bark of trees and logs, 700-1700 m. Recorded from Boyacá and Santander. 8. Frullania caulisequa (Nees) Nees World distribution: scattered in tropical America. Frullania gymnotis Mont. Frullania confertiloba (subg. Chonanthelia) Frullania obcordata (Lehm. & Lindenb.) is closely related to F. riojaneirensis but Lehm. & Lindenb. differs by the large, rounded stylus (Yuzawa, On bark and rotten wood in lowland and 1991). The species is known from only few montane rainforest areas and woodlands, locations in tropical America and may have from sealevel to about 3000 m. Recorded been overlooked. from Amazonas, Boyacá, Casanare, Cesar, Magdalena, Quindío, Risaralda, Santander 11. Frullania convoluta Lindenb. & Hampe and Tolima. World distribution: tropical Fig. 5 America. Frullania caulisequa (subg. Diastaloba) is On bark of trees, pendent from branches, related to F. apiculata but is immediately in upper montane cloud forest, to 3400 m. separated from the latter by the sparse, Recorded from Boyacá, Cundinamarca, irregular branching and rounded leaftips. Meta, Nariño, Norte de Santander, Putumayo, The species occurs on bark of trees at low Risaralda, Santander and Tolima. World elevations. The species was treated by distribution: Central America, Dominican Schuster (1992) under the names Frullania Republic, tropical Andes, Guayana obcordata (Lehm. & Lindenb.) Lehm. & Highlands. Lindenb. and Frullania gymnotis Mont., Frullania convoluta (subg. Meteoriopsis) is a which are synonyms (see Gradstein & common species of the subgenus Meteriopsis Costa, 2003). Frullania gymnotis is a and is recognized by pendent growth, rounded form of F. caulisequa with toothed female (to obtuse) leaf apex and the rather distant, bracts. ovate-oblong underleaves (Uribe, 2008).

378 Gradstein & Uribe

Figure 3. Frullania brasiliensis Raddi. A. Part of shoot, ventral view. B. Perianth. C and D. Leaf lobules. Reproduced from Cryptogamie, Bryologie with permission.

379 Frullaniaceae from Colombia

Figure 4. Frullania confertiloba Steph. A. Part of shoot, ventral view. B. Leaf lobule and discoid stylus. C. Stem leaf, dorsal view. Reproduced from Cryptogamie, Bryologie with permission. The species closely resembles Frullania bifid underleaves (to 1/3) which are 2-3 times grandifolia, which is the only other member wider than the stem. The species has been of subgenus Meteriopsis with a rounded confused with F. tetraptera, but the latter leaf apex; for differences between the two species has narrower and less deeply bifid species see the key. Frullania convoluta has underleaves and occurs at higher elevation. sometimes been confused with F. peruviana, which is also widespread in tropical America, 13. Frullania dulimensis Uribe Fig. 6 but in the latter species the leaf apices are acute. On bark of isolated trees in open areas in the upper montane belt, growing together 12. Frullania cuencensis Tayl. with other pendent species of the subgenus Meteriopsis (F. peruviana, F. convoluta), On bark and logs, to 3000 m. Recorded 3200 m. Recorded from Tolima (Uribe, 2006). from Cundinamarca and Santander. World World distribution: only known from the type distribution: tropical America. specimen from Colombia. Frullania cuencensis (subg. Chonanthelia) is Frullania dulimensis (subg. Meteoriopsis) recognized by the beaked lobule with a large is readily separated from the other members sac and short laminate part, and rather deeply of the subgenus Meteoriopsis by the toothed 380 Gradstein & Uribe leaves. The species is only known from a the small, distant underleaves which are single collection from Colombia. hardly wider than the stem, deeply bifid (to ½), cuneate at the base and with flat margins. 14. Frullania dusenii Steph. The lobules in the species are often somewhat diverging and positioned at an oblique angle On bark and rock, ca. 1700 m. Recorded from with the stem (Stotler, 1969). Frullania Cesar, Cundinamarca and Magdalena. World ecuadorensis has been described based on distribution: tropical America. sterile material and its affinities remain little Frullania dusenii (subg. Chonanthelia) is known. recognized by the saccate lobule with a very short lamina, a narrow mouth (ca. half the 17. Frullania ericoides (Nees) Mont. width of the sac) and a plicate surface, and the rather large, rounded, imbricate underleaves Common on bark and rock in rather dry, which are 3-4 times wider than the stem. open woodlands, from sea level to 2800 m. According to Yuzawa (1991), the species is Recorded from Antioquia, Boyacá, Casanare, largely restricted to elevations above 2000 Chocó, Cundinamarca, Quindío, Risaralda, m. Frullania dusenii may be confused with Santander and Tolima. World distribution: F. gibbosa but the latter species has squarrose pantropical. leaves and a large, leaf-like stylus, and occurs Frullania ericoides (subg. Frullania) is at lower elevations. one of the most drought-tolerant epiphytic liverworts and one of the few leafy liverwort 15. Frullania ecklonii (Spreng. ) Gottsche species that occur in the arid lowland belt of et al. the Galapagos Islands (Gradstein, 2008). The species is readily recognized by the squarrose On bark and rock at high elevations, and rather brittle leaves, which reproduce 3000-3500 m. Recorded from Boyacá, asexually by leaf fragmentation. The lobules Cundinamarca and Tolima. World are highly variable and may be saccate in some distribution: pantropical. populations and laminate, without formation Frullania ecklonii (subg. Chonanthelia) of watersac, in others. Frullania ericoides is recognized by the 10-keeled perianth, may be confused with Frullania gibbosa the smooth margins of leaves, lobules and which also has squarrose leaves and occurs underleaves, and the absence of a well- in the same habitat. The two species can be developed lobule beak. The species has readily separated by their different sizes, sometimes been treated as a synonym of F. gibbosa being a larger plant with leafy Frullania arecae but in the latter species stems more than 2 mm wide (1-1.5 mm in F. the leaf and underleaf margins are undulate ericoides). Moreover, the leaves in F. gibbosa and the lobule is distinctly beaked (Yuzawa, are not brittle, the lobules are more broadly 1991). attached to the lobe, the perianth surfaces are smooth and the stylus is large, leaf-like (small 16. Frullania ecuadorensis Steph. subulate in F. ericoides).

On bark of trees and soil, 700-1200 m. 18. Frullania formosa Spruce Recorded from Boyacá and Risaralda. World distribution: scattered in tropical America. On branches of trees in lowland rain forest at Frullania ������������ecuadorensis (subg. Thyopsiella) is the foot of the Andes, ca. 500 m. Recorded characterized by the small plant size (width from Risaralda. World distribution: only less than 1 mm), the rounded leaf apex and known from Colombia and Ecuador. 381 Frullaniaceae from Colombia

Figure 5. Frullania convoluta Lindenb. & Hampe. A and B. Part of shoot, ventral view. C. Perianth. D and E. Underleaves. F. Leaf. G. Initial branching appendages. H. Apical cells. I. Median cells. J. Androecium. Reproduced from Cryptogamie, Bryologie with permission.

382 Gradstein & Uribe

Figure 6. Frullania dulimensis Uribe. A and B. Part of shoot, ventral view. C, D and E. Stem leaf-lobes. F and G. Androecia. H. Stylus. I. Initial branching appendages. J and K. Leaf lobules. L. Stem underleaf. M. Basal cells. N. Median cells. O. Apical cells. Reproduced from Cryptogamie, Bryologie with permission.

383 Frullaniaceae from Colombia

Frullania formosa (subg. Thyopsiella) is 21. Frullania intumescens (Lehm. & recognized by the flat and short apiculate leaf Lindenb.) Lehm. & Lindenb. apex, and the large, imbricate underleaves, which are more than 3 times as wide as the On bark and rock in montane rain forest areas stem (Stotler, 1969). By the characters of and páramo, 1000-3800 m. Recorded from the underleaves F. formosa is similar to F. Antioquia, Boyacá, Cauca, Cesar, Chocó, clandestina but in the latter species the leaf Cundinamarca, Huila, Magdalena, Quindío, apex is rounded, never apiculate. Risaralda, Santander, Tolima and Valle del Cauca. World distribution: tropical America. 19. Frullania gibbosa Nees Frullania intumescens (subg. Thyopsiella) is similar to F. brasiliensis but differs by Common on bark and rock, usually in rather the perianth with 3 sharp keels (terete in F. dry, open places, 500-3200 m. Recorded from brasiliensis). Yuzawa & Koike (1989), in Antioquia, Boyacá, Caldas, Casanare, Cauca, addition, found that the two species differ Cesar, Cundinamarca, Magdalena, Risaralda, by the presence of a small foliose appendage Santander and Tolima. World distribution: at the base of the stylus in F. intumescens widespread in tropical America. (Yuzawa & Koike, 1989). We have studied Frullania gibbosa (subg. Chonanthelia) the type material of F. intumescens (Jamaica, differs from all other members of the subgenus Bancroft s.n., ex hb. Hooker 1833, lectotype Chonanthelia by the squarrose leaves and in hb. S [no. B27792]) and can confirm the the large, foliose stylus. The stylus is usually observations of Yuzawa & Koike (1989). covered the large and densely imbricate (and However, we have not observed this appendage shallowly bifid) underleaves, and can be in any Colombian specimen identified as F. observed only by removing the underleaves. intumescens. Frullania gibbosa grows in rather open Stotler (1969) treated F. intumescens in locations at low elevations, often together with a broader sense, including plants with F. ericoides with which it may be confused. and without an appendaged stylus in F. For differences between the two see under F. intumescens. According to Yuzawa & Koike ericoides. (1989), the plants without appendaged stylus belong to F. closterantha which was described 20. Frullania grandifolia Steph. Fig. 7 from Ecuador by Spruce (1884) and was treated as a synonym of F. intumescens s.l. by On bark in upper montane forest, 3400 m. Stotler (1969). It should be noted, however, Recorded from Tolima (Uribe, 2008). World that, Stotler listed eight further species as distribution: rare species, known from a few synonyms of F. intumescens that were not localities in Central America (Mexico, Costa studied by Yuzawa and Koike. Three of them Rica) and the northern Andes (Colombia, (F. baptistae Gottsche, F. cucullata Lindenb. Ecuador). & Gottsche, F. longicollis Lindenb. & Frullania grandifolia (subg. Meteoriopsis) Gottsche) are older names than F. closterantha is recognized by the pendent growth, the that might have priority and should therefore rounded leaf apex, the large, imbricate, ± be studied (types should be in W). rounded underleaves, and the toothed female bracts. The species is closely related to F. 22. Frullania jelskii Loitlesb. convoluta but in the latter the underleaves are distinctly longer than wide and not imbricate, This rare species was recorded from and the margins of the female bracts are entire Colombia by Yuzawa (1991) without further (Uribe, 2008). information on habitat and distribution. 384 Gradstein & Uribe

World distribution: only known from Peru 24. Frullania laxiflora Spruce (type) and Colombia. Frullania jelskii (subg. Chonanthelia) is On bark in montane rain forest areas, 1500- characterized by the large saccate lobule with 3500 m. Recorded from Cauca and Tolima. a very short lamina, the broadly recurved leaf World distribution: scattered in the tropical apex, and the large underleaves (ca. 4 times Andes (Bolivia to Venezuela) and the as wide as the stem). The species is closely Galapagos Islands. related to F. dusenii but the latter species Frullania ���������laxiflora (subg. Chonanthelia) is is readily separated from F. jelskii by the characterized by the strongly concave leaves, narrow mouth of the sac, rounded underleaves the rather long laminate portion of the lobule, (slightly longer than wide in F. jelskii), and the which is about as long as the sac yet does not plicate lobule surface (Yuzawa, 1991). extend beyond the ventral lobe margin, the decurrent beak of the lobule, and the broad, 23. Frullania kunzei (Lehm. & Lindenb.) rounded underleaves with large basal auricles Lehm. & Lindenb. (Yuzawa, 1991). The species may be confused with F. riojaneirensis but in the latter species Frullania neesii Lindenb. (fide Gradstein & the laminate portion of the lobule extends Costa, 2003) beyond the ventral lobe margin and the beak On bark in rather open lowland woodlands and is not decurrent. isolated trees, also on rock, 200 m. Recorded from Amazonas. World distribution: tropical 25. Frullania lobato-hastata Steph. Fig. 8 America. Frullania kunzei (subg. Thyopsiella) is Frullania apollinarii Steph., syn. nov. readily recognized by the very small plants, On bark, 1800-3400 m. Colombia: less than 1 mm wide, which are creeping Cundinamarca, Quindio and Santander. World on bark or rock, sometimes over larger distribution: northern Andes (Colombia, bryophytes or lichens, and always tighly Ecuador). appressed to the subtrate. The rather short Frullania lobato-hastata (subg. Thyopsiella) lobules (less than 1.5 times longer than is a robust plant from high elevation in the wide), the isodiametrical, evenly thickened northern Andes. The species is recognized by upper leaf cells and the total absence of the very long, undulate auricules at underleaf auricles at leaf bases, separate F. kunzei bases, which are at least half as long as the from other neotropical members of the underleaf lamina (lamina length measured subgenus Thyopsiella (Schuster, 1992). The from the middle of the underleaf insertion species may be confused with members of line to apex). The leaf apex is broadly rounded the subgenus Diastaloba (e.g. F. caulisequa) or, occasionally, short apiculate. �����������The species which resemble F. kunzei by small size and resembles F. brasiliensis in the almost terete prostrate growth, but the very different lobule perianth but the leaf apex in F. brasiliensis is in the latter species (positioned at some always apiculate and the underleaf auricles distance from the stem, not close to the stem) are small and not undulate. readily distinguishes them from F. kunzei. Frullania apollinarii Steph., published by Frullania kunzei is the only heteroicous Stephani in the same volume of the Species member of the genus Frullania in the Hepaticarum as F. lobato-hastata but 3 month Neotropics; the dioicous phenotype of the later, is a synonym of the latter species (see species has been described as F. neesii, which Uribe, 2004a for description and illustration is a synonym (Gradstein & Costa, 2003). of F. apollinarii).

385 Frullaniaceae from Colombia

Figures 7. Frullania grandifolia Steph. A. Part of shoot, ventral view. B. and C. Stem leaf-lobes. D. Perianth. E. Underleaf. F. Initial branching appendages. G. Androecium. H. Leaf-lobule. I. Median cells. J. Apical cells. K. Basal cells. Reproduced from Cryptogamie, Bryologie with permission. 386 Gradstein & Uribe

Figure 8. Frullania lobato-hastata Steph. ���������������������������������������������A. Part of shoot, ventral view. B and C. Stem leaves. D and E. Underleaves. F. Leaf lobule. G. Androecium. H. Perianth. Reproduced from Caldasia with permission.

387 Frullaniaceae from Colombia

26. Frullania macrocephala (Lehm. & and having distinctly recurved margins, the Lindenb.) Lehm. & Lindenb. undivided lamina of the first branch underleaf, and the entire margins of female bracts and On bark of trees and rocks, 1400-2900 m. bracteoles (see Key). Recorded from Boyacá, Cundinamarca, Quindío, Risaralda and Santander. World 30. Frullania nodulosa (Reinw. et al.) distribution: tropical America. Gottsche et al. Frullania macrocephala������������ (subg. Thyopsiella) closely resembles F. brasiliensis but differs by In crowns of trees in dense lowland rain forest, the ± flat leaf apex (recurved inF. brasiliensis; and lower down on bark of trees and shrubs in see Stotler, 1969). savannas and other open places, 200-250 m. Recorded from Amazonas and Vaupés. World 27. Frullania meridana Steph. Fig. 9 distribution: pantropical. The small, pendent lobules in Frullania On bark of trees, 1500-3200 m. Recorded from nodulosa (subg. Homotropantha) readily Cundinamarca, Risaralda and Tolima. World separate this species from all other neotropical distribution: northern Andes (Venezuela members of the genus Frullania. The species (type), Colombia). is furthermore characterized by its robust size, Frullania meridana (subg. Thyopsiella) is the regularly pinnate to 2-pinnate branching, characterized by the characters given in the the suborbicular leaves with a broadly rounded key. The species is known from only few apex and the large, imbricate underleaves collections, and only from male plants (Uribe, with a very shallow incision at the apex and 2004b). with large basal auricles (Gradstein & Ilkiu- Borges, 2009). The species is widespread 28. Frullania mirabilis Jack & Steph. in the lowlands of Amazonia but has been surprisingly little collected in Colombia. On bark of trees and soil, 1200-2400 m. Recorded from Antioquia, Cauca, Chocó, 31. Frullania paradoxa Lehm. & Lindenb. Meta, Nariño and Valle. World distribution: northern Andes, Costa Rica. On bark of trees, 3000-3700 m. Recorded Frullania mirabilis (subg. Thyopsiella) is from Boyacá, Cauca, Cundinamarca, Quindío, easily recognized by the two long appendices Risaralda and Valle. World distribution: at the ventral base of the leaf, one standing up tropical Andes. and one hanging down. The species has also Frullania paradoxa�������� (subg. Thyopsiella) been described under the name F. pendulostyla is characterized by the rounded leaf apex, Steph. (Stotler, 1969) the longer than wide and rather narrow underleaves which are hardly wider than 29. Frullania montagnei Gottsche the stem, the shallowly bifid lamina (to ¼) of the first branch underleaf, and the sharply On bark, 1500-2100 m. Recorded from 3-keeled perianth surrounded by bracts and Magdalena, Santander and Tolima. World bracteoles with ciliate-laciniate margins distribution: tropical America. (Stotler, 1969). Frullania flexicaulis Spruce, Frullania montagnei (subg. Thyopsiella) recorded from Colombia, is very similar to resembles F. paradoxa by the rounded leaf F. paradoxa and may be a synonym of the apex and the rather narrow underleaves which latter. The species differs from F. paradoxa are less than 3 times as wide as the stem, by the female bract lobes with entire margins but differs by underleaves being imbricate (usually toothed in F. paradoxa) and the 388 Gradstein & Uribe somewhat more deeply bifid lamina (to ½) distribution: scattered in the Andes and the of the first branch underleaf. mountains of Central America, from Chile to Mexico. 32. Frullania peruviana Gottsche Fig. 10 Frullania �������������pluricarinata (subg. Chonanthelia) is very similar to F. tetraptera but differs Frullania mathanii Steph. (syn. fide Uribe, by the 8-10-keeled perianth (4-keeled in F. 2008) tetraptera). The two species seem to differ Frullania atrata sensu Spruce (non typus) somewhat in elevational range, F. tetraptera (fide Uribe, 2008) being most common in páramo whereas F. On bark of tree branches in montane cloud pluricarinata seems to occur mainly in the forest areas, 1800-3800 m. Recorded upper montane belt. from Antioquia, Boyacá, Caldas, Chocó, Cundinamarca, Magdalena, Nariño, 35. Frullania ringens Spruce Quindío, Risaralda, Tolima and Valle. World distribution: Central America, tropical Andes, On bark of trees, 3400 m. Recorded from Galapagos Islands. Cauca. World distribution: northern Andes Frullania peruviana (subg. Meteoriopsis) is (Colombia, Ecuador). recognized by the pendent growth, acute leaf Frullania ringens (subg. Chonanthelia) is apices and underleaves without basal auricles recognized by the large, 2-3-toothed laminate (Uribe, 2008). The species is very common portion of the lobule, the long, the decurrent in the Andean region and has been described beak of the lobule, the large, rounded under several different names. Spruce (1884) underlaves with 2 very large auricles which in his famous handbook on the liverworts of are usually overlapping each other, and 10- the Amazon region and the Andes, described keeled perianths (Yuzawa 1991). Frullania the species under the name Frullania atrata, ringens is most closely related to F. ecklonii which is a different species, however, and not but differs from the latter by the lobule with related to F. peruviana (see under F. atrata). a long beak and toothed lamina (beak ± lacking and lamina entire in F. ecklonii) and 33. Frullania pittieri Steph. the larger underleaf auricles, which are often overlapping each other (not overlapping in Frullania mucronata auct. (non typus) (fide F. ecklonii). Uribe & Gradstein, 2003) On bark of trees, occasionally on shaded, wet 36. Frullania riojaneirensis (Raddi) rock, from sea level to 2500 m. Recorded from Ångstr. Boyacá, Cauca, Chocó, Quindío and Risaralda. World distribution: tropical America. On bark and rock, 500-3800 m. Recorded Frullania pittieri (subg. Thyopsiella) is from Antioquia, Boyacá, Caldas, Casanare, recognized by the flat and longly mucronate Cauca, Cesar, Chocó, Cundinamarca, Huila, to acuminate leaf apices (Stotler, 1969). The Magdalena, Quindío, Risaralda, Santander species has sometimes been misidentified and Tolima. World distribution: pantropical. as F. mucronata, which is a synonym of F. Frullania riojaneirensis (subg. Chonanthelia) brasiliensis (Uribe & Gradstein, 2003). is a very common species of lower montane elevations and is recognized by the large 34. Frullania pluricarinata Gott. laminate portion of the lobule (to be examined on the leaves of the main stem) with a flat On bark of trees, 1700-3000 m. Recorded margin and distinct beak, and the 4-keeled from Cundinamarca and Magdalena. World perianth. 389 Frullaniaceae from Colombia

Figure 9. Frullania meridana Steph. A. Part of shoot, ventral view. B. Leaf lobe, dorsal view. C. Underleaf. D and E. Leaf-lobules. F. androecium. G. Apical cells. H. Stylus. Reproduced from Tropical Bryology with permission.

390 Gradstein & Uribe

Figure 10. Frullania peruviana Gottsche. A. Part of shoot, ventral view. B. and C. Leaf lobes. D. Perianth. E, F and G. Underleaves. H and I. Leaf lobules. J. Stylus. K. Basal cells. L. Median cells. M and N. Apical cells. Reproduced from Cryptogamie, Bryologie with permission. 391 Frullaniaceae from Colombia

37. Frullania setigera Steph. Fig. 11 39. Frullania standaertii Steph.

On bark of trees, soil, rocks and logs, 900- On bark of trees, 1500-4000 m. Recorded 3600 m. Recorded from Antioquia, Boyacá, from Cundinamarca and Santander. World Cauca, Chocó, Huila, Santander and Valle. distribution: in páramos of the tropical Andes World distribution: scattered in tropical from Colombia to Bolivia; also in East Africa America. (Kenya). Frullania setigera (subg. Thyopsiella) is Frullania standaertii (subg. Chonanthelia) a little-known species that is recognized is recognized by the short laminate portion by the triangular-ovate underleaves with of the lobule and the long, lanceolate stylus narrowly acuminate apices and auriculate (Yuzawa, 1991). A a long, lanceolate stylus bases, and by the long acuminate apex of is also present in F. albertii Steph. and F. the lamina of the first branch underleaf arsenii Steph., which are very similar to F. (Stotler, 1969). The leaf apex in F. setigera standaertii and have been recorded from is apiculate to short acuminate, plane or Colombia; probably they are synonyms of recurved, and the perianth is 3-keeled. Frullania standaertii. Frullania standaertii is a characteristic species of the páramos of the 38. Frullania sphaerocephala Spruce tropical Andes; in addition there is one record from East Africa. On bark of trees in montane cloud forest areas and páramo, 1700-3900 m. Recorded from 40. Frullania tetraptera Nees & Mont. Cundinamarca, Meta, Quindío, Risaralda and Tolima. World distribution: tropical Andes On bark of trees, 2000-3800 m. Recorded from Bolivia to Colombia. from Cundinamarca, Meta and Risaralda. Frullania sphaerocephala ( s u b g . World distribution: common at high elevations Chonanthelia) resembles F. ecklonii by the in Central America and the Andes, from pluriplicate perianth, the smooth, entire Mexico to Chile and Argentina. leaves and underleaves, and the lobule with Frullania tetraptera (subg. Chonanthelia) is a large appendage without distinct beak, but a characteristic species of the páramo and is is easily separated from F. ecklonii by the recognized by its rather small size (plants ca. large, inflated female bracts and bracteoles, 1-1.4 mm wide), the short laminate portion of which are closely imbricate and incurved, the lobule, the very small stylus, the narrow forming a globose head. Morover, F. ecklonii underleaves that are hardly wider than the is monoicous whereas F. sphaerocephala is stem, and the monoicous sexuality (Yuzawa, dioicous. By its peculiar, ball-shaped female 1991). The species has sometimes been involucres F. sphaerocephala cannot be confused with F. cuencensis but the latter confused with any other neotropical species species has larger underleaves and is dioicous. of Frullania. Further characteristics of F. Frullania tetraptera is also very similar to sphaerocephala are the minute, 1(-2)-celled F. pluricarinata, which is a poorly known stylus, the large trigones of the leaf cells and species from high elevation in the Andes, but the large auricles of leaves and underleaves. the latter species has a pluriplicate perianth The species is characteristic of upper montane (see Key). cloud forests and shrubby páramo, above 2500 m.

392 Gradstein & Uribe

Figure 11. Frullania setigera Steph. A. Part of shoot, ventral view. B. Initial branching appendages. C. Leaf lobe. D. Leaf lobule. F. Underleaf. G. Apical cells. H. Perianth. Reproduced from Tropical Bryology with permission.

393 Frullaniaceae from Colombia

41. Frullania tunguraguana Clark & Frye Frullania crenulifolia Jack & Steph. – Recorded from Antioquia On soil, 1600 m. Recorded from Santander. Frullania granatensis Gottsche - Recorded World distribution: scattered in the tropical from Cundinamarca Andes (Venezuela to Argentina) and in Frullania guadalupensis Gottsche ex Steph. Mexico. - Recorded from Magdalena Frullania tunguraguana (subg. Chonanthelia) Frullania harpantha Herz. – Recorded from is characterized by the pluriplicate perianth Cundinamarca and the distincly beaked lobule with a long Frullania moritziana Lindenb. ���������& Gott. - laminate portion (longer than the sac) whose Recorded from Risaralda margins are entire and smooth, not folded Frullania occanniensis Steph. - Recorded or undulate. Also, the margins of leaves from Antioquia and underleaves in this species are never Frullania repanda Gottsche - Recorded from undulate like in the closely related F. arecae. Cundinamarca Frullania tunguraguana somewhat resembles Frullania sabanetica Gottsche – Recorded F. riojaneirensis but in the latter species the from Cundinamarca perianths have only 4 keels while those in Frullania trianae Gottsche – Recorded from F. tunguraguana have more 12-14 keels Nova Granata, S. L. (Yuzawa, 1991). Frullania tunguraguana is Frullania trollii Herz. – Recorded from known from only very few collections in spite Cundinamarca of its wide neotropical distribution. Acknowledgments 42. Frullania winteri Steph. We thank Dr. Lars Hedenas, Stockholm, for On bark of trees, 1700-2500 m. Recorded from the loan of the type material of Frullania Boyacá, Quindio, Risaralda and Santander. intumescens and Mr. Denis Lamy for the World distribution: northern Andes, Mexico. permission to reproduce some figures from Frullania winteri (subg. Chonanthelia) is Cryptogamie, Bryologie. recognized by the lobule with a short laminate portion whose lateral margin is folded and LITERATURE CITED projecting upwards towards the sac. Two varieties have been recognized in this species: Bonner, C. E. B. 1965. Index Hepaticarum var. winteri with a relatively large stylus V. Delavayella to Geocarpus. Weinheim. (10-13 cells long, 5-10 cells wide) and var. 480 pp. vanderhammenii (Haarbrink) Yuzawa with a Gottsche, C. M. 1864. Hepaticae. In: J. J. smaller stylus (5-8 cells long, 1-2 cells wide). Triana, J. J. & J. E. Planchon, Prodromus The material from Colombia and Ecuador florae novo- granatensis. Annales des belongs to var. vanderhammenii (Yuzawa, Sciences Naturelles 5, Botanique 1: 95- 1991). The species is known from only few 198. collections. Gradstein, S.R. 2008. ����������������������Annotated catalogue of liverworts and hornworts of the Galapagos Doubtful taxa Islands. Bibliotheca����������������������������� Lichenologica 99: 143-162. Frullania armata Herz. - Recorded from Gradstein, S. R. & D. P. Costa. 2003. The Cesar and Magdalena Hepaticae and Anthocerotae of Brazil. Frullania atropurpurea Steph. – Recorded Memoirs of the New York Botanical Garden from Cundinamarca 87: 1-317.����� 394 Gradstein & Uribe

Gradstein, S. R. & W. H. A. Hekking. 1979. Kluge, J., M. Kessler & R. Dunn. 2006. Studies on Colombian Cryptogams IV. A What drives elevational patterns of Catalogue of the Hepaticae of Colombia. diversity? A test of geometric constraints, Journal of the Hattori Botanical Laboratory climate, and species pool effects for 45: 93-144. pteridophytes on an elevational gradient Gradstein, S.R. & A.-L. Ilkiu-Borges. 2009.����� in Costa Rica. Global Ecology and Guide to the Plants of Central French Biogeography 15: 358-371. Guiana. Part IV. Liverworts and Hornworts. Kunth, C. S. 1822. Synopsis Plantarum, quas Memoirs of the New York Botanical in intere ad plagam aequinoctialem orbis Garden 76,4: 1-140. novi collegerunt A. de Humboldt et Am. Gradstein, S. R. & J. Uribe-M. In��������� press. Bonpland 1: 40-45. Paris. Marchantiophyta. In: Bernal, R., M. Celis León-Yánez, S., S. R. Gradstein & C. & S. R. Gradstein (eds.), Catalogue of the Wegner. �������������������������������2006. Hepáticas y Antoceros del Plants of Colombia. Bogotá. Ecuador. Herbario QCA, Quito. 101 pp. Gradstein, S. R., S. P. Churchill & N. Pinzón, M., E. L. Linares & J. Uribe-M. 2003. Salazar Allen. 2001. Guide to the Hepaticas del Medio Caquetá (Amazonia Bryophytes of Tropical America. Memoirs Colombiana). Caldasia��������������������� 25: 297-311. of the New York Botanical Garden 86: Robinson, H. 1967a. Preliminary studies on 1-577. the bryophytes of Colombia. Bryologist Hattori, S. 1973. Two South American 70:1-61. Frullanias, F. mirabilis and F. pendulostyla. Schuster, R. M. 1992. The Hepaticae and Journal of Japanese Botany 48: 104-110. Anthocerotae of North America V. Chicago. Hattori, S. 1980. Notes on Asiatic species of 854 pp. the genus Frullania, Hepaticae XII. Journal Spruce, R. 1884. Frullania. En: Hepaticae of the Hattori Botanical Laboratory 47: Amazonicae et Andinae. Trans. Proc. Bot. 85-125. Soc. Edinburgh 15:3-59. Hentschel, J., M.J. von Konrat, T. Pócs, A. Stephani, F. 1901-05. Species Hepaticarum Schäfer-Verwimp, A. J. Shaw, H. Schneider II. Geneva. & J. Heinrichs. �����������������������������2009. Molecular insights into Stotler, R. E. 1969. The genus Frullania the phylogeny and subgeneric classification subgenus Frullania in Latin America. Nova of Frullania Raddi (Frullaniaceae, Hedwigia 18: 397-555. ). ���������������������������Molecular Phylogenetics and Uribe, J. 2004a. Type studies on Frullania Evolution 52: 142-156. subgenus Meteoriopsis (Hepaticae). II. On Herzog, T. 1942. Beiträge zur Kenntnis F. apollinarii and F. paranensis. Caldasia neotropischer Bryophyten. Beihefte zum 26: 89-93. Botanischen Centralblatt 61: 559-590. Uribe, J. 2004b. Estudios��������������������������� en ejemplares tipo Herzog, T. 1955. Hepaticae aus Columbia und del género Frullania. ����������III. Sobre F. meridana Peru. �������������������������������Feddes Repertorium 57: 156-203. Steph. y F. setigera Steph. Tropical Bryology Hörandl, E. & T. Stuessy. 2010. Paraphyletic 25: 9-34. groups as natural units of biological Uribe, J. 2006. Type studies on Frullania classification. Taxon 59:1641-1653. subgenus Meteoriopsis (Hepaticae). Jack, J. B. & F. Stephani. 1892. Hepaticae Frullania dulimensis sp. nov. from Colombia. Wallisianae. Hedwigia 31: 11-27. Cryptogamie, Bryologie 27:309-312. Kessler, M. 2000. Elevational gradients in Uribe, J. 2008. Monografia������������������������ del subgenero species richness and endemism of selected Meteoriopsis del género Frullania plant groups in the central Bolivian Andes. (Frullaniaceae, Marchantiopsida). Caldasia Plant Ecology 149: 181-193. 30: 49-94. 395 Frullaniaceae from Colombia

Uribe, J. & S. R. Gradstein. ���������������1998. Catalogue VandenBerghen, C. 1976. Frullaniaceae of the Hepaticae and Anthocerotae of (Hepaticae) africanae. Bulletin������������������ du Jardin Colombia. Bryophytorum Bibliotheca 53: Botanique National de Belgique 46: 1- 1-99. 220. Uribe M., J. & S. R. Gradstein. 1999. Estado Yuzawa, Y. 1991. A���������������������� monograph of subgen. del conocimiento de la flora de hepáticas Chonanthelia of gen. Frullania (Hepaticae) de Colombia. Revista de la Academia of the World. ��������������������������������Journal of the Hattori Botanical Colombiana de Ciencias Exactas, Físicas y Laboratory 70: 181-291. Naturales 23, 87:315-318. Yuzawa, Y. & N. Koike. 1989. Studies of the Uribe, J. & S. R. Gradstein. 2003. Type type specimens of Latin American Frullania studies on Frullania subgenus Meteoriopsis. species (1). Journal of the Hattori Botanical I. Cryptogamie, Bryologie 24: 193-207. Laboratory 66: 343-358.�

Recibido: 07/03/2011 Aceptado: 19/08/2011

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