Revision of the Neotropical fern genus Eupodium ... - Springer Link

KEW BULLETIN VOL. 65: 115–121 (2010)

Revision of the Neotropical fern genus Eupodium (Marattiaceae) Maarten J. M. Christenhusz1 Summary. Previous studies on the classification of Marattiaceae have shown that the Neotropical species of

Marattia are to be divided into two genera: Marattia Sw. and Eupodium J. Sm. Morphological studies show that the latter genus consists of three geographically isolated species: Eupodium laevis in the Greater Antilles, E. pittieri in Central America and Andean South America, and E. kaulfussii in southern Brazil. This paper revises the taxonomy of the genus Eupodium. One new combination is made and a key, descriptions and a distribution map are provided. Key Words. Eusporangiate ferns, Marattia, taxonomy.

Introduction The fern family Marattiaceae is one of the oldest lineages of vascular plants, with extant members that have changed little since the Cretaceous. Together with another ancient family, the horsetails (Equisetaceae), it forms one of the basal lineages of ferns (Pryer et al. 2001). Extant Marattiaceae can be diagnosed morphologically by several characters. They have, for instance, conspicuous thick-walled sporangia that are fused into synangia, producing very large quantities of spores. The vascular system of the rhizomes is complex and polycyclic and the rhizomes bear starchy outgrowths on both sides of the petiole, on which proliferous buds are often formed. The leaves possess swollen bases on petioles and pinna insertions, and the tissue contains numerous mucilage canals (Christenhusz 2007). Modern Marattiaceae have commonly been treated as having four genera: Christensenia Maxon, 1 – 2 species, Southeast Asia-Malesia; Danaea Sm., about 50 species, tropical America; Angiopteris Hoffm., about 30 species, Madagascar, Asian tropics, Australia, Pacific, naturalised in the Neotropics and Hawaii (Christenhusz & Toivonen 2008); and the Pantropical genus Marattia Sw., in its broadest sense with about 36 species (Christenhusz 2007). However, Presl (1845) divided Marattia into five genera. Presl’s classification of other marattioid genera such as Danaea did not hold up in morphological (Christenhusz & Tuomisto 2005) or molecular studies of that genus (Christenhusz 2007; Christenhusz et al. 2008). His classification of the genera within Marattia has been similarly confusing. Marattia is typified by the Jamaican M. alata Sw., but Discostegia C. Presl is also typified by this species. Stibasia C. Presl is based on Marattia douglasii (C. Presl) Baker, which, according to Murdock (2008a), is closely related to M. alata.

Discostegia and Stibasia are thus undoubtedly synonymous to Marattia. Gymnotheca C. Presl was based on Marattia cicutifolia Kaulf. from southern Brazil, which is a morphologically odd species among Neotropical Marattia and more closely resembles those of the Old World. Unfortunately, Murdock (2008a) was not able to include this species in his molecular study, so the placement of Gymnotheca remains tentative, although Murdock (2008b) synonymises it with Marattia. Finally, Presl (1845) also recognised Eupodium J. Sm., which is typified by E. kaulfussii. Unfortunately, he placed the closely related Marattia laevis Sm. (= Eupodium laevis (Sm.) Murdock) in Discostegia, which was followed by De Vriese & Harting (1853) in their monograph of the Marattiaceae. Presl (1845) placed these two very similar species in two different genera, which shows that his generic concept in Marattiaceae should not be followed. Lavalle (2003) revised the Neotropical species of Marattia, but opted for a slightly greater synonymy, in cases where according to her, species delimitations were not clear. For instance, she synonymised M. chiricana Maxon under M. interposita Christ, which clearly differ in pinna size and division of the terminal pinna. She also did not recognise the morphological differences in the M. laevis complex, which in her treatment represents all specimens with awns on the midveins of the pinnules and conspicuously stalked, vascularised synangia. These are exactly the characters on which the genus Eupodium was based. Molecular studies (Murdock 2008a) have shown that the Marattia laevis complex is more closely related to the Old World species of Marattia than to the Neotropical-Hawaiian clade. The placement of the genera Angiopteris and Christensenia made the genus Marattia in its traditional sense polyphyletic. Murdock

Accepted for publication January 2010. 1 Department of Biology, The Natural History Museum, Cromwell Road, London, SW7 5BD, UK. e-mail: [email protected]

© The Board of Trustees of the Royal Botanic Gardens, Kew, 2010

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(2008b) therefore opted to divide the genus Marattia into three separate genera, two in the Neotropics and one in the Palaeotropics. Even though the division of Marattia is tentative in part, because the placement of Christensenia is not yet fully established, I believe that the Neotropical genera Marattia and Eupodium are morphologically sufficiently different to be kept separated. Further molecular studies including all 30 or so species of Marattia s.l., Christensenia and a broader sampling of Angiopteris are still necessary to verify the monophyly of the genera proposed by Murdock (2008b) and to establish if Eupodium and Ptisana Murdock remain isolated. The genus Eupodium consists of three geographically separate entities that are morphologically quite similar. The group has not been thoroughly revised before, although Murdock (2008b) already pointed out some

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morphological differences, and separated E. kaulfussi and E. laevis based on a comparatively large genetic distance. E. pittieri was not included in that study, but a similar result is to be expected. A key and descriptions of the three species are given below. The distribution of the genus is provided in Map 1.

Taxonomic Treatment Eupodium is easily distinguished from the other Marattiaceae by its stalked synangia (Fig. 1A) and its awns on the midrib of the pinnae (Fig. 1B). The large deltoid blades are generally finely divided, 3-pinnatepinnatifid, with winged rachises. The plants form a large terrestrial cone-shaped rhizome, bearing usually only a single leaf.

Key to Neotropical Species of Eupodium1 1. Awns present on both surfaces of the lamina (less frequent and smaller abaxially). Scales usually absent from lamina surfaces, sparse at bases of primary segments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . E. kaulfussii Awns present only on adaxial surface of the lamina. Blades moderately to densely scaly . . . . . . . . . . . . . . . . . 2 2. Pulvini tuberculate, petiole bases very scaly, blades moderately scaly. . . . . . . . . . . . . . . . . . . . . . . . . . . . . E. laevis Pulvini smooth, petiole bases glabrous to glabrescent, blades densely scaly. . . . . . . . . . . . . . . . . . . . . . E. pittieri

1. Eupodium kaulfussii2 (J. Sm.) J. Sm. (in Hooker 1842: tab. 118). Type: Brazil, without locality, anno 1816, Cunningham s.n. (holotype BM!). Marattia kaulfussii J. Sm. (in Hooker 1839: tab. 26). Marattia raddiana Schott (1834: 3, tab. 5). Gymnotheca raddiana (Schott) C. Presl (1845: 13). Type: Brazil, Rio de Janeiro, Corcovado, Angra dos Reis, Água da Serra, anno 1818, Pohl s.n. in herb. Schott 3870 (lectotype W!, selected here; isolectotypes PRC!). Eupodium kaulfussii (Hook.) J. Sm. var. acuminatum Fée (1869: 215). Type: Brazil, Rio de Janeiro, Alto Macaé, 28 March 1868, Glaziou 2274 (lectotype P!, selected here; isolectotypes P!, S!). Eupodium kaulfussii (Hook.) J. Sm. var. macropteron Fée (1869: 215). Type: Brazil, Rio de Janeiro, Alto Macaé, 28 March 1868, Glaziou 2273 (lectotype P!, selected here; isolectotype P!). Marattia alata auct. non Sw. sensu Raddi (1825: 74, t. 83, 84). Rhizomes globular, radially arranged, up to about 40 cm wide at apex, somewhat resembling a big, fleshy pine cone with closed scales; stipules appressed, half-

orbicular, to 5 cm wide, succulent; leaves 3-pinnatepinnatifid, deltoid-triangular, 2 – 3 m long, petioles to about 1.8 m long, 2 cm thick at the base, sparsely to moderately scaly, the scales 0.5 – 3 mm long, filiform to lanceolate, orange to light-brown, flaccid, often caducous; rachises winged, the wing to 2 mm wide in the distal part of rachis; blades 170 – 180 × 170 – 190 cm; lateral pinnae deltoid-oblong, reduced and confluent with the winged rachises towards the pinnule apex into an entire pinnatifid-crenate terminal segment with a crenate acute apex, the pinnae with about 11 – 15 pairs of pinnules, the oblong pinnules pinnate or deeply lobed; pinnulets elliptic-oblong, 1 – 5.5 (– 8.5) × 0.5 – 1.5 cm, parallel-sided, apices obtuse to rounded-acute, bases acute, margins coarsely crenate, the midvein bearing awns adaxially and (sparsely) abaxially, these 0.2 – 1 mm long; terminal segments rhomboid, 1.9 – 3.2 × 1.7 – 2 cm, widest below the middle, margins crenate, deeply pinnatifid; veins simple or once forked (a fork per lobe), branched in apical pinnules, about 3 – 6 veins per cm (but variable); synangia intramarginal radial to bilateral, 8 – 16 (– 18)-locular, mature ones stalked, the stalks about 0.7 mm long. Fig. 1.

1

Herbarium specimens may be difficult to identify with this key, because they are often fragmentary and incomplete. In these cases one may make an assumption of the identity based on the geographic origin of the sample. 2 If Eupodium kaulfussii were treated under Marattia then Marattia raddiana (1834) would take priority over M. kaulfussii (1839).


DISTRIBUTION. S Brazil (Rio Grande do Sul to Rio de

Janeiro and Minas Gerais) and N Argentina. SPECIMENS EXAMINED. ARGENTINA. Misiones: Gral. M.

Belgrano, Ruta Nac. 101, Salto Andresito, Guaglianone 2975 (SI). BRAZIL. Minas Gerais: Santos, Mosén s.n.

REVISION OF THE NEOTROPICAL FERN GENUS EUPODIUM (MARATTIACEAE)

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Map 1. Distribution of Eupodium. ● E. kaulfussii, ▲ E. laevis, ■ E. pittieri.

(S!). Paraná: Serra do Mar, Dusén 14478 (S!); Ponta Grossa, Furnas Gêmaes, Christenhusz 4788 (UPCB!, SP!, TUR!). Rio de Janeiro: Regnell 264 (S!); Serra dos Órgãos, Morro Assú, Von Luetzelburg 6261 (S!, W!); Pico do Bico do Papagaio, Mynssen 1085 (RB!, TUR!). Rio Grande do Sul: Mun. Rio Pardo, Paz Soledade, Jürgens 71 (PR!, S!). Santa Catarina: Upper Río Uruguay, Sehnem 5735 (B!); Véu-da-Noiva, near Dr Pedrinho, Christenhusz 5000 (SP!, TUR!). São Paulo: Wacket 144 (S!); Ubatuba, Ubatumirim, Parque Estadual da Serra do Mar, núcleo Picinguaba, Christenhusz 4927 (SP!, SPSF!, TUR!).

HABITAT. Atlantic rainforest and Araucaria glades; 300 –

1000 m. CONSERVATION STATUS. Least Concern (LC). VERNACULAR NAMES. Socorro, Vacaria (Santa Catarina,

Brazil, Sehnem 5735 (B)). 2. Eupodium laevis (Sm.) Murdock (2008b: 744). Marattia laevis Sm. (Smith 1790, tab. 47). Type: Dominican Republic, without locality, Thiery 90 (holotype LINN!). Myriotheca laevis (Sm.) Lam. & Poir. (Lamarck & Poiret 1797: 403). © The Board of Trustees of the Royal Botanic Gardens, Kew, 2010

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Fig. 1. Eupodium kaulfussii. A abaxial side of pinnules, Furnas Gêmaes near Ponta Grossa, Paraná, Brazil (Christenhusz 4788), inset shows a stalked synangium; B adaxial side of pinnules, Véu-da-Noiva near Doutor Pedrinho, Santa Catarina, Brazil (Christenhusz 5000), arrows point out some of the awns on the midrib; C in stream in Paranapiacaba, São Paulo, Brazil. PHOTOS MAARTEN CHRISTENHUSZ. © The Board of Trustees of the Royal Botanic Gardens, Kew, 2010


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Fig. 2. Eupodium pittieri. A petiole cross section; B abaxial surface of pinnule with synangia; C proximal half of pinna, note pulvinus-like swelling at base of costa. From Øllgaard et al. 35864 (NY). DRAWN BY R. C. MORAN. Reproduced from Fl. Ecuador with kind permission (Tuomisto & Moran 2001).

Discostegia laevis (Sm.) C. Presl (1845: 12). Marattia alata Sw. var. laevis (Sm.) Farw. (Farwell 1931: 308). Rhizomes erect, globular, radially arranged, often partly subterranean, but recorded to form erect trunks to 1 m tall, up to about 40 cm wide at apex; stipules appressed, half-orbicular, to 4 cm wide, succulent; leaves 3-pinnatepinnatifid, deltoid-triangular, 2 – 4 m long, petioles to about 2 m long, 2 cm thick and tuberculate at the base, very scaly, the scales 0.5 – 3 mm long, filiform to lanceolate, orange to light-brown, flaccid, often caducous; rachises winged, the wing to 2 mm wide in the distal part of rachis; blades 170 – 180 × 170 – 190 cm, moderately scaly; lateral pinnae deltoid-oblong, reduced and confluent with the winged rachises towards the pinnule apex into an entire pinnatifid-crenate terminal segment with a crenate acute apex, the pinnae with about 11 – 15 pairs of pinnules, the oblong pinnules pinnate or deeply lobed; pinnulets ellipticoblong, 1 – 5.5 (– 8.5) × 0.5 – 1.5 cm, parallel-sided, apices obtuse to rounded-acute, bases acute, margins coarsely crenate, the midvein bearing awns adaxially

only, these 0.2 – 1 mm long; terminal segments rhomboid, 1.9 – 3.2 × 1.7 – 2 cm, widest below the middle, margins crenate, deeply pinnatifid; veins simple or once forked (a fork per lobe), branched in apical pinnules, about 3 – 6 veins per cm (but variable); synangia intramarginal, bilateral, 8 – 16 (– 18)-locular, mature ones stalked, the stalks about 0.7 mm long. DISTRIBUTION. Greater Antilles (excl. Jamaica). SPECIMENS EXAMINED. CUBA. Oriente: Sierra Maestra,

Loma del Gato, El Cobre, Clément (Téteau) 2408 (MICH, US!). DOMINICAN REPUBLIC. Constanza, Von Türckheim 3058 (W!); Reserva Cientifica Ebano Verde, en la Vanada de Maria, Zanoni et al. 46434 (MAPR!); Barahona, Cuatro Alas, woods NE of La Culata, Liogier 13077 (IJ!). PUERTO RICO. Mun. Adjuntas, Monte Guilarte State Forest, upper slopes of Monte Guilarte, Proctor 40110 (IJ!, SJ!); Mun. Jajuya, 5.5 miles W of road 149 & 134 intersection, near Ponce radio antennas, Mejía 2163 (MAPR!). HABITAT. In montane rainforest and elfin woodland; 950 – 1600 m. CONSERVATION STATUS. Vulnerable (VU). © The Board of Trustees of the Royal Botanic Gardens, Kew, 2010

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3. Eupodium pittieri3 (Maxon) Christenh., comb. nov. http://www.ipni.org/urn:lsid:ipni.org:names:77104367-1 Marattia pittieri Maxon, Contr. U. S. Natl. Herb. 17: 421 (1914). Type: Panama, Chiriquí, Humid forest along the upper Caldera R., near “Camp I,” Holcomb’s trail, above El Boquete, 1450 – 1650 m, 22 – 24 March 1911, Maxon 5704 (holotype US!, 6 sheets; isotypes NY!, P!, fragments). Rhizomes erect, globular, radially arranged, often partly subterraneous, but recorded to form erect trunks to 1 m tall, up to about 40 cm wide at apex, somewhat resembling a fleshy big pine-cone with closed scales; stipules appressed, half-orbicular, to 4 cm wide, succulent; leaves 3-pinnate-pinnatifid, deltoid-triangular, 2 – 4 m long, petioles to about 2 m long, 2 cm thick at the base, smooth, glabrous or glabrescent (sparsely scaly), the scales when present 1 – 3 mm long, filiform to lanceolate, orange to light-brown, flaccid, often caducous; rachises winged, the wing to 2 mm wide in the distal part of rachis; blades 170 – 180 × 170 – 190 cm, densely scaly; lateral pinnae deltoid-oblong, reduced and confluent with the winged rachises towards the pinnule apex into an entire pinnatifid-crenate terminal segment with a crenate acute apex, the pinnae with about 11 – 15 pairs of pinnules, the oblong pinnules pinnate or deeply lobed; pinnulets elliptic-oblong, 1 – 5.5 (– 8.5) × 0.5 – 1.5 cm, parallel-sided, apices obtuse to rounded-acute, bases acute, margins coarsely crenate, the midvein bearing awns adaxially only, these 0.2 – 1 mm long; terminal segments rhomboid, 1.9 – 3.2 × 1.7 – 2 cm, widest below the middle, margins crenate, deeply pinnatifid; veins simple or once forked (a fork per lobe), branched in apical pinnules, about 3 – 6 veins per cm (but variable); synangia intramarginal, bilateral, 8 – 16 (– 18)-locular, mature ones stalked, the stalks about 0.7 mm long. Fig. 2. DISTRIBUTION. Widely distributed from S Mexico to Bolivia and east to Venezuela and Trinidad. SPECIMENS EXAMINED. BOLIVIA. Cochabamba: Chapare, San Jacinto, Steinbach 9043 (GH, MO, NY!, S!). Santa Cruz: Florida Prov., Canton Mairana Parque Nacional Amboro, 7 km NNE from Mairana, Moran 5909 (AAU!). COLOMBIA. Boyaca: Valle del Rio Cusiana entre Sogamoso y Corinto, Murillo 1385 (AAU!). Caldas: Carretera Manizales-Bogotá, km 14.6 desde El Batallón de Infantería N° 22 (Ayacucho),

3

Maxon (1914) stated that this taxon differs from E. kaulfussii by its enormous size and larger, differently shaped segments. E. pittieri is indeed larger in stature than E. kaulfussii but the segment size and shape are within the variability of both species.



Arbeláez 488 (AAU!, NY). Cundinamarca: La Vega– Facatativa highway, Haught 6145 (S!). Santander: San Pedro, Idinoël 2564 (DUKE!); S slope of Mt San Martin, near Charta, Killip 19145 (GH, NY, S!). COSTA RICA. Alajuela: Palma, Brade 498 (S!). ECUADOR. Carchi: Valle de Maldonado, Holm-Nielsen 6250 (AAU!). Loja: Parque Nacional Podocarpus, Madsen 75557 (AAU!). Morona-Santiago: Cumanda, 6 km W of Mera, Harling & Andersson 17305 (AAU!). Napo: Slopes of Guagra Urcu, on the Loma above Río Bretania, Holm-Nielsen 26825 (AAU!). Pastaza: Hacienda San Antonio del Barón von Humboldt, 2 km al NE de Mera, Baker 5774 (AAU!, MO, NY, QAME, QCNE). Pichincha: Canton Quito, Rio Guajalito reserve, Fay 3345 (AAU!). Zamora-Chinchipe: Road Loja – Zamora, km 24 – 25, Holm-Nielsen 3534 (AAU!, B!, NY). MEXICO. Oaxaca: without locality, Galeotti 6349 (P). PANAMA. Darien: Cerro Pirre, Folsom 4547 (AAU!). PERU. Amazonas: Bagua, 12 km E of La Peca, Barbour 4279 (AAU!). Huanuco: Churubamba, trail Puente Durand to Exito, Mt. Santo Toribio, Mexia 8250 (B!, F, GH, MI, S!). TRINIDAD. Aripo Heights, Prestoe s.n. anno 1866 (BM!, TRIN). VENEZUELA. Aragua: Colonia Tovar, Walter 13 (B!). Mérida: On road up mountainside behind Tabay (15 km from Merida towards Barinas), White 1970112 (DUKE!). Trujillo: Distrito Bocono, 22 km SE of Bocono, road to Guaramacal, A. R. Smith 1505 (AAU!, UC). HABITAT. In montane rainforest, cloud forest and elfin woodland; 1000 – 3000 m. CONSERVATION STATUS. Least Concern (LC).

Acknowledgements Thanks are due to Jefferson Prado, Claudine Mynssen, Samuli Lehtonen and Pedro Bond Schwartzburt for their help and company during the field work in Brazil. I also thank the curators of several herbaria (AAU, B, BM, DUKE, IJ, MAPR, PR, RB, S, SJ, SP, TUR, U, UPCB, W), who made their material available for study. Additionally, I thank Claes Persson for permission to reproduce Fig. 2 from the Flora of Ecuador. References Christenhusz, M. J. M. (2007). Evolutionary history and taxonomy of Neotropical marattioid ferns: Studies of an ancient lineage of plants. Ann. Univ. Turku., AII, 216. ____ & Toivonen, T. K. (2008). Giants invading the tropics: The oriental vessel fern, Angiopteris evecta (Marattiaceae). Biol. Invasions 10: 1215 – 1228. ____ & Tuomisto, H. (2005). Some notes on the taxonomy, biogeography and ecology of Danaea (Marattiaceae). Fern Gaz. 17: 217 – 222. ____, ____, Metzgar, J. S. & Pryer, K. M. (2008). Evolutionary relationships within the Neotropical,


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