Lophocolea fragrans subsp. cocosana subsp. nov. and L. tenerrima ...

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PrePub Article

Nova Hedwigia published online September 2017

Lophocolea fragrans subsp. cocosana subsp. nov. and L. tenerrima (Marchantiophyta: Lophocoleaceae) new to Central America Gregorio Dauphin1*, S. Robbert Gradstein2, Maria I. Morales3 and Joaquín Sánchez1 1

Herbario Nacional, Museo Nacional de Costa Rica, Apartado 749-1000, San José, Costa Rica

2

Muséum National d’Histoire Naturelle, Dept. Systématique et Evolution, Paris, France

3

Escuela de Biología, Universidad de Costa Rica, San Pedro, San José, Costa Rica

With 2 figures

Abstract: Lophocolea fragrans subsp. cocosana G.Dauphin, Gradst. & M.I.Morales subsp. nov. is described from Cocos Island and L. tenerrima Spruce, known only from Ecuador, is recorded from Costa Rica. The two taxa are described and illustrated. Key words: Costa Rica, liverworts, Lophocolea, Lophocolea fragrans, Lophocolea tenerrima, taxonomy.

Introduction Our knowledge of the genus Lophocolea (Dumort.) Dumort. in tropical America is largely based on the work of Fulford (1976), who recognized 42 species of Lophocolea in Latin America including nine in Central America. Two further species, L. fragmentissima R.M.Schust. and Lophocolea "sp. nov.", were recorded from Central America (Costa Rica) by Gradstein et al. (1994). Based on recent molecular and morphological studies, several species treated by Fulford as Lophocolea have been transferred to other genera, including Chiloscyphus, Cryptolophocolea, Heteroscyphus and Leptoscyphus (e.g., Söderström et al. 2016). As a result, six Lophocolea species are currently known from Central America: L. aberrans Lindenb. & Gottsche, L. bidentata (L.) Dumort., L. fragmentissima, L. liebmanniana Gottsche, L. muricata (Lehm.) Nees and Lophocolea "sp. nov.".

*Corresponding author: [email protected] © 2017 J. Cramer in Gebr. Borntraeger Verlagsbuchhandlung, Stuttgart, Germany. DOI: 10.1127/nova_hedwigia/2017/0422

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www.borntraeger-cramer.de 0029-5035/2017/0422 $ 2.00

According to Söderström et al. (2013), Lophocolea is a distinct genus with "moderate to strong support", comprising taxa previously assigned to Chiloscyphus subg. Lophocolea [excluding C. subg. Lophocolea sect. Bicornuti (Spruce 1885: 424) Engel & Schuster (1985: 409) = C. subg. Connati (Engel 2010)], C. subg. Microlophocolea (Spruce 1885: 426) Engel (1999: 22), C. subg. Fragilifoliae (Schuster 1978: 245) Engel & Schuster (1985: 409) and C. subg. Spinoscyphus Engel (2010: 1999). Thus defined, Lophocolea includes plants with opposite to alternate leaves, leaf apex bifid to trifid, leaf margins entire or toothed, leaf cells thin-walled or with small trigones, leaf surface smooth or sometimes covered above by teeth-like projections, underleaves deeply bifid, free from leaves or narrowly attached to leaves on one side, gynoecia on long stems or branches, and perianths deeply trigonous. The ongoing preparation of a Catalogue of Central American Marchantiophyta and Anthocerotophyta (Dauphin et al. in prep.) has brought about several taxonomical and distributional novelties including a new subspecies and a rare species of Lophocolea new to Costa Rica and Central America. The purpose of the present paper is to describe and illustrate the newly recorded taxa. Results 1. Lophocolea fragrans (Moris & De Not.) Gottsche, Lindenb. & Nees subsp. cocosana G.Dauphin, Gradst. & M.I.Morales subsp. nov. Fig. 1 Differs from subsp. fragrans (western Europe, Africa) by the presence of caducous leaves; caducous leaves smaller than ordinary leaves, with 1–6 teeth at the apex and an occasional tooth on the ventral and dorsal margins. Type: COSTA RICA. punTarenas: Cocos Island, 200 m, 1994, Isla de Cocos, mirador a Bahía Wafer, sobre tronco de Sacoglottis holdridgei Cuatr., 13 Jun 1994, G.Dauphin 1210 (holotype, CR; isotype, USJ, MO). PARATYPE: Ibid., entre Bahía Chatham y Wafer, alrededores de la torre de telecomunicaciones del ICE, 5°32'49"N, 87°32'58"W, 240 m, Jun 2016, J.Sánchez 2690, 2708 (CR).

General DisTribuTion: Costa Rica (Cocos Island). Plants very delicate, to 1.5 cm long and 1.15 mm wide, sometimes smaller and flagelliform, whitish green to yellowish green, creeping loosely among other bryophytes. Stems fragile, very thin, ca. 0.05–0.08 mm in diameter, with 12–17 rows of cortical cells surrounding about the same number of medullary cells, dorsal epidermal cells as large as ventral ones, rectangular in optical view, all cell walls evenly thickened. Branching frequent, lateral-intercalary, some branches with caducous leaves. Ordinary stem leaves alternate, succubous and almost longitudinally inserted, very flat, slightly distant to imbricate, ovate-subrectangular, widest towards the base, 240–250 µm wide and 300–370 µm long, ca. 1.2–1.5× longer than wide, apex mostly bifid to about 1/5, sometimes trifid due to the presence of a large tooth on the ventral margin near apex, lobes diverging outwards, 2–3 cells wide, with a 1–2 cells long uniseriate tip, sinus between the lobes U-shaped or V-shaped, lobes sometimes reduced to an acute angle; leaf margins crenulate due to convex cell walls, ventral leaf margin frequently with 1(–2) teeth, the teeth 1–2 cells long. Leaf cells isodiametric-hexagonal or quadrate to subrectangular, 14–23 × 15–32 µm in the leaf lamina, becoming slightly smaller 2 eschweizerbart_xxx

Fig. 1. Lophocolea fragrans subsp. cocosana G.Dauphin, Gradst. & M.I.Morales. A. Habit, showing gametoecia and innovation. B. Midleaf cells. C. Underleaf. D. Stem in dorsal view. E. Leaf apices. F. Branch with caducous leaves. G. Apex and margin of caducous leaf. (All drawn from the holotype).


towards apex, thin-walled, trigones lacking, cuticle smooth; oil-bodies not seen. Caducous leaves in situ imbricate, obovate to subrectangular, slightly smaller than ordinary stem leaves, decreasing in size towards branch apex, apex with 1–6 teeth, the teeth 1–2 cells long, 2 cells wide at base, ventral and dorsal margins with an occasional single-celled tooth; cells as in normal leaves but with conspicuous trigones towards leaf base. Underleaves slightly wider than the stem, bifid to almost near the base, 200 × 275 µm, lobes lanceolate to subulate, 1–5 seriate, outer margins with a 1–2 cells long tooth, bases cuneate, free from the leaves. Autoicous. Gynoecia terminal on main stems or long branches with one sterile or fertile innovation, innovating up to 3 times, bracts and bracteoles similar to leaves and underleaves. Perianth strongly trigonous, keels toothed to laciniate. Androecia intercalary on main branches or on an innovation, bracts in up to 22 pairs, imbricate, saccate, apex emarginate to bifid to 1/5. Vegetative reproduction by caducous leaves. Lophocolea fragrans subsp. cocosana stands out by producing caducous leaves. This character was not known in this species and is uncommon in Lophocoleaceae, occurring furthermore in L. fragmentissima (= Campanocolea fragmentissima (R.M.Schust.) R.M.Schust.) and Leptoscyphus cuneifolius (Hook.) Mitt. (Schuster 1997). Lophocolea fragrans is a rare Old World species that is known from western Europe, Macaronesia, North Africa (Morocco), and scattered in eastern and southern Africa (Tanzania, South Africa, Reunion, Comores). The species is recorded here for the first time from the New World. It is a member of L. sect. Microlophocolea and is very closely related to L. liebmanniana and L. muricata (Hentschel et al. 2006, as Chiloscyphus). Lophocolea fragrans is recognized by its small size, small leaf cells (12–23 cells wide), bifid leaves with a supplementary tooth on the dorsal or ventral leaf margins near the apex, and toothed (or entire) perianth keels. When the tooth on the ventral leaf margin is well developed, the leaf apex appears trifid. 2. Lophocolea tenerrima Spruce, Trans. & Proc. Bot. Soc. Edinburgh 15: 439. 1885. Fig. 2 = L. erosa Gradst., Mem. N.Y. Bot. Gard. 84: 66. 1999, nom. inval. et illeg. (non L. erosa (J.J.Engel) L.Söderstr. et al.). specimens examineD: COSTA RICA. carTaGo: Paraíso, Orosi, base del Cerro Asunción, área de páramo alterado al borde de Carretera Interamericana Sur, 9°34'54.2220N, 83°45'50.4240W, 3350 m, en la base de talud rocoso, a media sombra, sobre el talo y entre los rizoides de Marchantia polymorpha L., 30 Sep 2016, G.Dauphin, M.Morales & J.Sánchez 4605 (CR, USJ, PC). SAN JOSé: Cerro de La Muerte, along the Panamerican Highway, 3200 m, on moist earth in rock fissures along the road, in deep shade, 29 Sep 1994, S.R. Gradstein 9744 (U, USJ). ECUADOR. pichincha: "Andes Quitenses", Mt. Pichincha, alt. 3000–3700 m, on soil near rivers, R. Spruce s.n. (holotype, MANCH CC 7930!). Furthermore recorded in Ecuador from the provinces of Carchi and Cotopaxi (León-Yánez et al. 2006, Gradstein in prep.).

General DisTribuTion: Ecuador, Costa Rica. Plants delicate, to 1.5 cm long and 1–2 mm wide, often smaller and flagelliform, whitish green, creeping loosely or in small mats. Stems fragile and often broken, thin, with 10–24 rows of medullary cells surrounded about the same number of cortical cells, dorsal epidermal cells as large as ventral ones, rectangular in optical view, all cell


Fig. 2. Lophocolea tenerrima Spruce. A. Habit in dorsal view. B. Leaf margin. C. Midleaf cells. D. Stem leaf. E-F. Underleaves. G. Bracteole. (All drawn from Dauphin et al. 4605).


walls evenly thickened. Branching frequent or scarce, lateral- or ventral-intercalary, the plants sometimes appearing dichotomous. Leaves alternate, succubous and almost longitudinally inserted, assurgent-secund, standing upwards to obliquely spreading, distant to subimbricate, subquadrate to rectangular to obcuneate, widest above, to 0.8 mm long × 0.6 mm wide, often smaller, 1.1–1.4 × longer than wide, ± irregularly bifid to 1/4–1/3, lobes narrow-triangular, straight or diverging outwards, 2–3 cells wide and with 1–3 cells long uniseriate tips, lobes very fragile and often broken, sinus between the lobes U-shaped or V-shaped, margins irregularly toothed in the upper half or ± entire, teeth 1–3 cells long and 1–2 cells wide at the base in the type material, to over 6 cells long and 1–3 cells wide at the base in the material from Costa Rica, leaf margins crenulate due to convex cell walls. Cells quadrate to rectangular or isodiametric-hexagonal, very transparent, 25–35 × 31–67 µm in midleaf, becoming slightly smaller towards apex, very thin-walled, trigones lacking, cuticle smooth. Oil bodies finely granular, ovoid to ellipsoid, almost hyaline, 5.5–13.5 µm long, (1–)2(–4) per cell, present in all leaf cells. Underleaves smaller to slightly wider than the stem, irregularly shaped, bifid to almost near the base, lobes lanceolate to filiform with fragile tips uniseriate to 5 (–7) cells long, but frequently broken; margins entire or with an occasional tooth; underleaf bases cuneate, free from the leaves. Dioicous. Gynoecia terminal on short or long lateral branches, without innovations; bracts ca. 3× larger than leaves, suborbicular, concave, apex unequally laciniate, the lacinia ending in an uniseriate, to 13 cells long tip, margins toothed; bracteoles more or less lingulate, ca. 0.7 mm long × 4 mm wide, bifid to 1/2, sometimes unequally trifid, lobes triangular, to 6 cells wide at the base and 11 cells long, 130 × 130 µm, supplementary marginal teeth usually present, teeth to 60 µm long. Perianth not seen. Androecia (seen in the type of L. tenerrima): intercalary on the main stem. Vegetative reproduction by fragmenting leaf- and underleaf-lobes. During fieldwork in Costa Rica in 1992, SRG collected a Lophocolea in the tropicalpine region of the Cordillera de Talamanca, at the base of Cerro Buenavista (Cerro de La Muerte), which he labeled as Lophocolea sp. nov. (Gradstein et al. 1994). The species, characterized by copious fragmentation of leaf apices, was additionally recorded from the Andes of Ecuador. Since the specimens were invariably sterile the species was not formally described. Five years later, SRG proposed the name "Lophocolea erosa" for the plant (Gradstein 1999; see also León et al. 2006), again without formal description. In September 2016, fertile material of the species was collected in Costa Rica by GD, MM and JS, very near to the locality where the species was originally detected. The gynoecia on long shoots confirmed that the species was a member of Lophocolea. Further study revealed that the plants belonged to L. tenerrima Spruce (1885), a species hitherto known only from the 150 years old type specimen from the Ecuadorian Andes and not treated by Fulford (1976). By the assurgent-secund leaves with eroded tips leaves and underleaves L. tenerrima can hardly be confused with any other species of Lophocolea. Eroded leaf tips also occur in L. subviridis (Hook.f & Tayl.) Gottsche from southern South America but in the latter species the leaf tips become disfigured by the formation of linear propagules. Moreover, L. subviridis is very different from L. tenerrima in leaf and underleaf shape (see Fulford 1976, Hässel de Menendez 1995 as Chiloscyphus subviridis (Hook.f. & 6 eschweizerbart_xxx

Taylor) J.J.Engel & R.M.Schust.). The leaf margins in L. tenerrima are irregularly toothed-ciliate in the upper half in the type and in the Costa Rican material, but in other Ecuadorian collections they are ± entire. Well-developed plants may occur mixed with small, flagelliform shoots. The underleaves are highly variable in shape and frequently broken. Spruce (1885) classified L. tenerrima in sect. Microlophocolea Spruce, suggesting a close relationship to L. liebmanniana. However, by its rather large leaf cells (25– 35 µm wide) L. tenerrima differs from the members of L. sect. Microlophocolea, which stand out by small leaf cells, 10–20(–25) µm wide (e.g., Vogelpoel 1977, Schuster 1980). The relationships of L. tenerrima need further study. Key to Central American species of Lophocolea 1 Leaf surface covered by numerous teeth-like projecting cells .................................. L. muricata 1' Leaf surface smooth....................................................................................................................2 2

Leaves transverse, deeply bifid to more than 1/2 of leaf length, strongly caducous. Plants minute, ca. 0.5 mm wide. On bark of trees in upper montane cloud forest and páramo, above 3000 m ......................................................................................................................... L. fragmentissima 2' Leaves almost longitudinally inserted, succubous, entire or bifid to 1/4–1/3, not caducous (except L. fragrans: couplet 5), sometimes with fragmenting tips. Plants usually more than 0.5 mm wide (sometimes very small and flagelliform in L. tenerrima) ..................................................3

3. Leaf tips very fragile, usually broken and disfigured. On soil and rock above 2500 m ............... ..................................................................................................................................L. tenerrima 3' Leaf tips not fragile.....................................................................................................................4 4

Plants very small, 0.7–1.2 mm wide. Leaf cells small, 13–23 µm wide in midleaf. Leaf margins with one or more teeth ................................................................................................................5 4' Plants and leaf cells larger. Leaf margins entire .........................................................................6 5. Leaf margin with 1(–2) teeth near apex, otherwise entire. Caducous leaves present. Cocos I..... .........................................................................................................L. fragrans subsp. cocosana 5' Leaf margin with 5–20 teeth. Caducous leaves absent. In lowland and lower montane rainforest ...................................................................................................................L. liebmanniana 6

Leaf apex entire to shallowly retuse, lobes rounded to acute. Underleaves narrowly attached to leaves on one side ...................................................................................................... L. aberrans 6' Leaf apex clearly bidentate, lobes apiculate to acuminate. Underleaves free from the leaves ..... ...................................................................................................................................L. bidentata

noTe: Morales (1991) additionally recorded Lophocolea cf. granatensis Gottsche from Costa Rica. The material on which this record was based (CARTAGO: Paraíso, Orosi, P.N. Tapantí, Griffin & Morales 161) has not been found. However, as L. granatensis has proved to be a synonym of Cryptolophocolea connata (Sw.) L. Söderstr. & Váňa (Gradstein in prep.), the name L. granatensis should be removed from the Central American checklist. Acknowledgments We are grateful to the Departamento de Historia Natural, Museo Nacional de Costa Rica for funding the 2016 field trip to Cerro de La Muerte, to Ethel Sánchez from Centro de Investigaciones


en Estructuras Microscópicas (CIEMIC), Universidad de Costa Rica, for access to optical and photographical equipment, and to the curators of herbaria MANCH and USJ for the loan of specimens.

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Manuscript submitted January 11, 2017; accepted April 21, 2017.
