Phylogeny and Taxonomy of Leucotrichum (Polypodiaceae): a New Genus of Grammitid Ferns from the Neotropics

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TAXON 59 (3) • June 2010: 911–921 Labiak & al. • Leucotrichum, a new fern genus from the Neotropics

Phylogeny and taxonomy of Leucotrichum (Polypodiaceae): A new genus of grammitid ferns from the Neotropics

Paulo H. Labiak,1 Germinal Rouhan2 & Michael Sundue3

1 Universidade Federal do Paraná, Departamento de Botânica, Caixa Postal 19031, CEP 81531-980, Curitiba-PR, Brazil 2 Muséum national d’Histoire naturelle, UMR CNRS 7205 ‘Origine, Structure et Evolution de la Biodiversité’, Botanique, 16 rue Buffon CP39, 75005 Paris, France 3 The New York Botanical Garden, 200th St & Southern Blvd. 10458-5126, Bronx, New York, U.S.A. Author for correspondence: Paulo H. Labiak, [email protected]

Abstract A new genus of grammitid ferns, Leucotrichum, is described. Segregated from Lellingeria on the basis of molecular analyses and morphological characters, it comprises five species distributed in the Antilles, Central America, and Southeastern Brazil. We present a phylogeny based on two cpDNA genes, atpB and rbcL, showing the relationships between Leucotrichum and other genera of grammitid ferns. Both Bayesian and Maximum Parsimony analyses support the monophyly of Leucotri- chum, with bootstrap value of 100% and posterior probability value of 1.0, and its sister-group relationship to the Terpsichore lanigera group. Leucotrichum is characterized by seven morphological characters: arching fronds, clathrate rhizome scales, blackish rhizome scale cell walls, laterally marginate petioles, laminar apices subconform to the lateral pinnae, pinna costae without blackish sclerenchyma, and hairs bearing acicular branch cells. We also provide a key, descriptions, complete synonymy, discussions, specimens examined, and illustrations for all the species.

Keywords cpDNA; Grammitidaceae; Lellingeria ; Neotropics; phylogeny; Terpsichore

INTRODUCTION apiculata group (including the type of the genus L. apiculata (Kunze ex Klotzsch) A.R. Sm. & R.C. Moran)—characterized Recent molecular phylogenetic studies have provided valu- by mostly unbranched, hyaline, and acicular hairs, and densely able information on the relationships of major fern groups, es- short-hirsute petioles; (2) the L. suprasculpta group—char- tablishing a more robust and defensible system of classification, acterized by membranaceous, pendent, 1-pinnate-pinnatisect particularly at the order and family ranks (Smith & al., 2006, blades; (3) the L. myosuroides group—characterized by very 2008). Despite these advances, generic circumscriptions and narrow blades, with a single sorus per segment, with evident relationships within some families are still not well understood veins on fertile segments, and glabrous rhizome scales; (4) and and are in need of more focused studies. Among the problematic the L. mitchellae group—characterized by a thickened lamina families are Polypodiaceae, which comprise about 56 genera with numerous, long, tawny hairs that bear an inconspicuous and over 1200 species (Smith & al., 2008), with most of the lateral cell at the base. Smith & al. (1991) mentioned four species species occurring in both the Old and New World tropics. Fol- belonging to this group: L. mitchellae, L. organensis, L. pseu- lowing the most recent classification (Smith & al., 2008), the domitchellae and L. schenckii. ‘grammitid ferns’ are a monophyletic lineage nested within Here, we focus on the Lellingeria mitchellae group, which Polypodiaceae (Ranker & al., 2004; Schneider & al., 2004; has been recovered as sister to the Terpsichore lanigera group Schuettpelz & Pryer 2007), which comprise about 25 genera by recent analyses, instead of being related to the remaining and 750 species, with most of the species occurring as epiphytes species of Lellingeria (Ranker & al., 2004; Sundue & al., in or epipetrically in tropical regions (Parris, 1990, 2007). Recent press). Even though it is clear that this group does not belong to phylogenetic studies demonstrate that several grammitid genera Lellingeria, the limited sampling does not allow assessment the are not monophyletic, and need further study (Ranker & al., actual limits of these clades, and whether they should be consid- 2004; Geiger & al., 2007; Sundue & al., in press). One of these ered a single genus or not. In an attempt to solve this question, is Lellingeria A.R. Sm. & R.C. Moran, which comprises about we have greatly expanded the number of taxa for both genera 60 species and occurs primarily in the Neotropics, but also in (Terpsichore, Lellingeria), and present a more comprehensive Africa, Madagascar, and the southern Pacific (Smith & al. 1991). analysis for these two groups in particular. Previous phylogenetic studies of grammitid ferns, which have Using DNA sequence data from two chloroplast markers, included only a few Lellingeria species, suggest that as tradi- and a morphological data matrix of 87 characters, we aim to tionally defined, Lellingeria comprises two or three distinct test their monophyly and position within the grammitid ferns. clades (Ranker & al., 2004; Sundue & al., in press). Smith & al. As a result, we describe the Lellingeria mitchellae clade a (1991) defined the genus primarily by having a radially symmet- new genus, establish diagnostic characters for it as well as the rical rhizome, unequally forked hairs and clathrate stem scales, Terpsichore lanigera clade, make necessary combinations, and and recognized the following four groups: (1) the Lellingeria present a taxonomic treatment for all of the known species.

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MATERIALS AND METHODS and revised when necessary. The two data matrices were con- structed using Mesquite v.2.6 (Maddison & Maddison, 2009) Taxonomic sampling. — To test the hypothesis that Lel- and analyzed using equally weighted maximum parsimony lingeria and Terpsichore are polyphyletic, and also to access (MP) and a Bayesian inference (BI). which groups are most closely related to the L. mitchellae MP analyses for each dataset were performed using TNT group, a large sampling of the Neotropical grammitid diversity v.1.1 (Goloboff & al., 2008). For all MP analyses, heuristic was included. To assess the relationships between the species searches were performed with 1000 parsimony ratchet repli- within the L. mitchellae group, all four previously described cates (Nixon, 1999) (200 iteration ratchet, the up- and down- species were included. Three of these species (L. mitchellae, weights set to 5% each), holding 20 trees per ratchet, followed L. organensis, L. schenckii) were represented by multiple by TBR-max branch swapping. Support for nodes was calcu- specimens that had been collected from different regions, to lated by bootstrap analyses (expressed in percentages: BP), with identify possible conflicts in species delimitation. In addition, 1000 replicates doing 10 ratchets per replicate, holding 20 trees we sampled one specimen of Xiphopteris mortonii Copel., that per ratchet, and keeping only the strict consensus. likely belongs to the Lellingeria mitchellae group. The Bayesian analyses were performed using MrBayes From the Terpsichore lanigera group, the suspected sister v.3.1.2 (Ronquist & Huelsenbeck, 2003). Nucleotide substitu- group, six species were included; these account for approxi- tion models suggested as best fit to the data under the hier- mately 25% of the estimated species in the group (Moguel, archical likelihood ratio test (hLRT) and the Akaike infor- 2005). Sampling within the remaining groups of Lellingeria mation criterion (AIC), as implemented in MrModeltest v.2.3 included 17 representative species (~35% of the total). Based on (Nylander & al., 2004), were used in the analyses of each studies by Schneider & al. (2004) and Ranker & al. (2004), we separate marker. Both criteria suggested the same model for chose four genera of Polypodiaceae outside of the grammitids both genes, GTR + Г + I. The partition strategy included the as outgroups for the present study: Microgramma percussa, Pe- models and separate codon positions for each marker. Three cluma alfredii, Polypodium glycyrrhiza, and Campyloneurum independent runs were started from random trees, consisting of angustifolium. In total, the final matrix includes 113 terminals, four chains each, one cold and three hot, with the temperature corresponding to 90 species and 24 genera. parameter set to 0.05 to ensure good mixing. The analyses Voucher information and GenBank accession numbers are were run for 10 million generations, sampling every 1000th listed in Table S1 in the Electronic Supplement 1 to the online generation. The “burn-in” period was identified visually and version of this article. trees sampled before stable posterior probability values (PP) DNA extraction. — Genomic DNA was isolated from ei- had been reached were exluded from consensus. In order to ther field-collected, silica gel–dried fronds or from herbarium assess if MCMC reached stationarity, we used AWTY (Wil- specimens. Total genomic DNA was extracted using the Qia- genbusch & al., 2004). gen DNEasy Plant Mini Kit (Valencia, California, U.S.A.), The consensus topologies from each of the two markers following the manufacturer’s protocol, but with an additional analyses were compared for potential conflicts. The combined proteinase K digestion during the lysis step: 30 μL of pro- dataset was analyzed using MP and BI analyses, with settings teinase K (20 mg/mL) and 30 μL of β-mercaptoethanol (98%) as for the separate datasets. added per tube, with the tubes incubated on a tipping plate at Morphological data. — Eighty-seven morphological 42°C for 12 h. characters were scored for all taxa included in this study, and Amplifications and sequencing. — Two chloroplast DNA character states were optimized onto trees generated from genes, atpB, and rbcL, were amplified by PCR, following stan- analysis of the sequence data. Characters and character states dard protocols. For atpB we used the primers ESATPB172F and were largely taken from Sundue & al. (in press), where ad- ESATPE45R (Schuettpelz & Pryer, 2007), and for rbcL the ditional comments about scoring can be found. However, we primers ESRBCL1F and ESRBCL1361R (Schuettpelz & Pryer, have excluded 23 characters that were considered unrelated to 2007). Both genes were typically amplified using a program this study. Characters and states are listed in the Appendix. The beginning with one initial denaturation step of 5 min at 94°C, character state matrix is provided in Electronic Supplement 2 followed by 35 cycles of 1 min at 94°C, 1 min at 50°C, 2.5 min to the online version of this article. The most relevant charac- at 72°C, and a final extension period of 10 min at 72°C. The ters are discussed in the text, and their respective numbers are PCR products were sequenced using the amplification primers denoted parenthetically. plus the internal primers 493F and 910R for atpB, and ESRB- Taxonomic treatment. — For the Lellingeria mitchel- CL1F and ESRBCL654R for rbcL, by the High-Throughput lae clade, which is here described as a new genus, we present Genomics Unit at the University of Washington (http://www. the necessary new combinations, information on the types, htseq.org/index.html). All the 53 newly obtained consensus a complete list of synonyms for each species, a selected list sequences were subsequently submitted to GenBank (Table of specimens examined, and illustrations for all the species. S1 in the Electronic Supplement 1). Additionally, an index of exsiccatae (Table S2 in Electronic Alignment and phylogenetic analyses. — Consensus Supplement 1) is also provided, containing information on sequences were automatically aligned using Muscle v.3.6 about 150 specimens that were borrowed from 27 herbaria (see (Edgar, 2004), and the resulting alignment manually checked Acknowledgments).

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RESULTS DISCUSSION

Results for each analysis and for each marker, including the The analyses presented here do not support Lellingeria as number of characters and taxa included, percentages of variable monophyletic, confirming the results of Ranker & al. (2004). and informative sites, number of MP trees, tree length, consis- Instead, three different clades are resolved. One of these, the tency index (CI), retention index (RI), and substitution models Lellingeria mitchellae group, is not closely related to the re- used in BI, are summarized in Table 1. Because there was no maining groups of Lellingeria, but instead is resolved as sister conflict in tree topologies among analytical methods, or between to the Terpsichore lanigera clade. The other two main clades datasets, only results from analyses of the combined dataset are of Lellingeria form a polytomy with Melpomene, a result in- discussed here. The MP analysis of the combined dataset resulted dicated in previous analyses (e.g., Ranker & al., 2004; Sundue in 128 most parsimonious trees, which are 1785 steps long and & al., in press). Although we increased the sampling in the have CI of 0.35 and RI of 0.76. For the Bayesian analyses, sta- Lellingeria + Melpomene clade from 7 (Ranker & al., 2004) to tionarity was reached for two of the three runs, according to the 27, the persistent lack of resolution in this clade demonstrates cumulative analysis performed using AWTY. that additional species and/or characters are necessary to assess With both analyses (MP and BI), the overall resulting to- the relationships among these groups. pology (Fig. 1) is well resolved with high nodal support values, The clade corresponding to the Terpsichore lanigera confirming and supporting the results presented by Ranker group is morphologically distinctive within the grammitid & al. (2004) and Sundue & al. (in press). Because these two ferns. Monophyly of this group has strong branch support in studies have exhaustively discussed the overall topology and our analyses (BP = 100, PP = 1.00), and is further characterized the relationships between the main clades within grammitids, by five morphological characters at this node: setae present on we focus on the results for the groups of interest, Lellingeria the rhizomes (9), rhizome scales with turgid cells (13), rhizome s.l., and the Terpsichore lanigera group, both of which were scales with ciliate adaxial and abaxial surfaces (23), membra- poorly sampled in those studies. naceous laminae (35), and the presence of episporangial setae Lellingeria was recovered as polyphyletic, falling into (78). Several other characters occur with high frequency in three different clades (Fig. 1). The L. myosuroides clade and this clade and further distinguish it, including pendent fronds, the L. apiculata + L. suprasculpta clade, each strongly sup- blades with indeterminate growth, concolorous (orange to cas- ported (BP = 100, PP = 1.00), are closely related to the genus taneous) rhizome scales with ciliate or sometimes glandular Melpomene (BP = 100, PP = 1.00) and form a polytomy with margins (Fig. 2G; scales absent in T. alfarii (Brack.) A.R. Sm.), that genus in the Bayesian analysis and the strict consensus of and setae that are simple, paired, or stellate (Fig. 2H). shortest trees in the MP analysis. Besides the seven characters that support the Lellingeria The Lellingeria mitchellae group is retrieved as monophy- mitchellae clade, it can be further characterized and distin- letic, supported by high clade support values (BP = 100, PP guished from the Terpsichore lanigera clade by determinate = 1.00) and additionally by seven morphological characters: leaves, clathrate and blackish rhizome scales, veins that are arching fronds (2), clathrate rhizome scales (16), blackish rhi- once-furcate, and setae that are hyaline to whitish. Although zome scale cell walls (17), laterally marginate petioles (30), whitish setae are also present in some species, most of the laminar apices subconform to the lateral pinnae (32), pinna species in the Terpsichore lanigera group possess reddish to costae without blackish sclerenchyma (36), and hairs bear- castaneous setae. Whitish setae are also present in the tropi- ing acicular branch cells (64). The sister group relationship cal Asian genus Tomophyllum (Parris, 2007). Tomophyllum, between the L. mitchellae clade and the Terpsichore lanigera however, is distinct from Leucotrichum mainly by having clade is strongly supported in both analyses (BP = 100, PP = pinnate veins, several sori per segment, and laminae gradu- 1.00) (Fig. 1). Two morphological characters further support ally reduced to a pinnatifid apex. Few Old World grammitid this sister relationship: radially symmetrical rhizomes (5), and clades show any close affinity to Neotropical ones (Ranker setae that are hyaline or whitish (52). & al., 2004).

Table 1. Number of taxa and characters, evolutionary models used in BI, and tree statistics for the MP analyses. atpB rbcL Combined Total number of taxa / ingroup only 113 / 109 113 / 109 113 / 109 Included characters 1120 1271 2391 Variable characters (%) 309 (28) 357 (28) 666 (28) Parsimony informative characters (%) 230 (22) 249 (21) 479 (21) Consistency index (CI) 0.36 0.43 0.35 Retention index (RI) 0.76 0.76 0.76 Number of MP trees 144 56 128 MP tree length 846 915 1785 BI substitution model GTR + Г + I GTR + Г + I GTR + Г + I

913 Labiak & al. • Leucotrichum, a new fern genus from the Neotropics TAXON 59 (3) • June 2010: 911–921

Microgramma percussa ** 0.75 * Pecluma alfredii * Polypodium glycyrrhiza 0.99 Campyloneurum angustifolium ** Grammitis tenella * Adenophorus oahuensis * ** * *** Adenophorus epigaeus * 0.510.51 * *** Adenophorus abietinus * Adenophorus hymenophylloides ** Cochlidium serrulatum 0.82 ** * Cochlidium seminudum __ * 0.980.98 Grammitis bryophila Grammitis melanoloma ** Terpsichore lehmanniana * ** Terpsichore eggersii * Terpsichore hanekeana Chrysogrammitis musgraveana Calymmodon luerssenianus ** * *** Scleroglossum sulcatum * 0.950.95 * Scleroglossum sulcatum Ctenopteris repandula 0.680.68 0.990.99 Ctenopteris lasiostipes 0.68 Ctenopteris heterophylla __ * *** * *** Grammitis billardieri * Grammitis ciliata ** Prosaptia pubipes ** 0.520.52 0.940.94 * 0.520.52 0.990.99 Ctenopteris rhodocarpa __ *** 0.92 * 0.99 Prosaptia obliquata 0.830.83 Prosaptia alata 0.52 Oreogrammitis hookeri ** 0.600.60 *** __ Grammitis padangensis * Xiphopteris conjunctisora Ctenopteris nutans 0.970.97 Micropolypodium taenifolium 0.990.99 Micropolypodium zurquinum *** Micropolypodium achilleifolium * Terpsichore longisetosa Lellingeria hartii *** * *** Lellingeria limula Lellingeria 0.830.83 * Lellingeria limula 0.99 Lellingeria saffordii ** myosuroides ** *** Lellingeria myosuroides * * Lellingeria subcoriacea Lellingeria hildebrandtii group ** ** *** Lellingeria subsessilis *** * * *** Lellingeria suspensa * Lellingeria phlegmaria ** Lellingeria suprasculpta *** Lellingeria * Lellingeria brevistipes Lellingeria subsessilis apiculata and 0.990.99 ** Lellingeria apiculata __ * Lellingeria apiculata 0.990.99 ** ** * ** Lellingeria humilis L. suprasculpta *** __ * * * *** * Lellingeria tamandarei ** groups * *** Lellingeria major * Lellingeria major ** *** Lellingeria hirsuta * Melpomene pseudonutans ** 0.980.98 * Melpomene moniliformis 0.98 * Melpomene moniliformis 0.970.97 * Melpomene flabelliformis * 0.930.93 0.810.81 Melpomene pilosissima 0.63 Melpomene pilosissima Melpomene Melpomene pilosissima *** 0.970.97 Melpomene anazalea * 0.64 Melpomene xiphopteroides *** Melpomene erecta * Melpomene firma ** ** Terpsichore subscabra * Terpsichore subscabra Terpsichore subtilis ** ** *** *** Terpsichore amphidasyon * * Terpsichore longipilosa 0.970.97 Terpsichore alsopteris 0.970.97 * 0.67 ** Terpsichore semihirsuta *** * Terpsichore alsopteris 0.640.64 Terpsichore praeceps 0.64 Terpsichore attenuatissima -- Terpsichore attenuatissima ** *** Terpsichore leucosticta * Terpsichore semihirsuta ** Ascogrammitis anfractuosa *** * ** Ascogrammitis david-smithii * ** * ** * Ascogrammitis dilatata * Ascogrammitis pichinchae Enterosora trifurcata 0.960.96 ** Ceradenia kalbreyeri ** ** * Ceradenia spixiana * *** * 0.970.97 Ceradenia intonsa ** *** 0.58 Ceradenia aulaeifolia * ** Ceradenia jungermannioides *** * *** Ceradenia pilipes * Ceradenia pilipes ** *** Terpsichore senilis * Terpsichore senilis *** * Terpsichore aff. cultrata ** Terpsichore ** * Terpsichore aff. cultrata * Terpsichore cultrata ** *** Terpsichore cultrata lanigera * ** Terpsichore lanigera ** * *** * Terpsichore stella group 0.640.64 * Terpsichore lanigera * Terpsichore glandullifera *** * 0.980.98 Leucotrichum mitchellae Leucotrichum mitchellae *** * * Leucotrichum mitchellae Leucotrichum pseudomitchellae *** Leucotrichum * ** Leucotrichum organensis * 0.860.86 Leucotrichum organensis ** * Lellingeria mitchellae *** * Leucotrichum organensis * Leucotrichum schenckii group *** * 0.790.79 Leucotrichum mortonii * Leucotrichum schenckii

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Most of the species in the L. mitchellae clade have glabrous basifixed, 1.5–2.5 mm long, margins ciliate, the cilia hyaline; sporangia. The one exception is L. mitchellae, which bears petioles absent to ca. 10 × 0.2–0.5 mm, greenish to castaneous, setae on the sporangial capsules like all the members of the with whitish, simple and 1-furcate hairs to 2 mm long; laminae Terpsichore lanigera group. erect to slightly arcuate, determinate, linear to linear-oblong, Within grammitid ferns, the distinction between hairs and membranaceous, pinnatifid to pinnatisect, with reduced basal setae, and the establishment of separate sets of character states segments, the lowermost decurrent to the petiole bases (forming for each indument type has been critical in delineating natural short and broad wings), apices abruptly reduced, ending in a groups (Parris 1997, 1998; Bishop, 1988, 1989; Lehnert & al., rounded apical segment, subconform to the lateral segments; 2008; Ranker & al., 2004; Smith & al., 1991; Smith & Mo- rachises with dark sclerenchyma, this not visible abaxially, ran, 1992; Sundue & al., in press). As defined here, setae are often obscured by laminar tissue adaxially, with whitish setae multicellular, uniseriate, terete, and reddish to castaneous or to 3 mm long and simple to 1-furcate hairs, these usually more whitish, whereas hairs are uni- or multicellular, either simple conspicuous on the abaxial side; segments 1–3 × 0.5–1.5 mm, or anisotomously branched, and whitish or reddish. Smith & the margins entire, plane or slightly revolute, symmetric or al. (1991) originally segregated Lellingeria from Grammitis asymmetric at base, apices acute to obtuse, covered by whitish based in part upon the presence of distinctive three-celled, setae ca. 1–3 mm long and 1(2)-furcate hairs 0.2–1.0 mm long, once- to twice-furcate hairs that bear hyaline acicular branch especially on the laminar tissue; veins 1-furcate, obscured by cells. Results presented here demonstrate that this hair type the laminar tissue, adaxially with well-marked hydathodes, (described by us as a suite of four separate characters) should but lacking calcareous deposits; sori inframedial, rounded to in fact be interpreted as homoplastic, having evolved multiple elongate, one per segment, superficial, surrounded by laminar times in the grammitid clade. This comes as no surprise, given hairs; sporangia glabrous or ciliate; spores trilete, 30–40 µm, that similar hairs, which differ only by being reddish, occur in papillate, green. Chromosome number unknown. other distantly related grammitid genera (i.e., Ctenopteris and Distribution. – Leucotrichum occurs in Central America, Prosaptia). Setae, in contrast, appear to have a single origin the Antilles, and in the coastal Atlantic rain forest of southeast- in the Polypodiaceae, and represent a synapomorphy for all ern Brazil. Three species are restricted to Central America and grammitid ferns (Sundue & al., in press), followed by losses the Caribbean (L. mitchellae, L. mortonii, L. pseudomitchellae), in the genera Adenophorus, Cochlidium, Grammitis s.str., Lel- and two are restricted to southeastern Brazil (L. organense, lingeria s.str., and Luisma. The presence of laminar setae in L. schenckii). The genus is apparently absent in the Andes the Lellingeria mitchellae clade unambiguously distinguishes and the Guayana Shield (Guyana, French Guiana, Suriname, it from Lellingeria s.str., and is one of the easiest ways to at- Venezuela). The absence of this genus in the Andes and in the tribute taxa to one or the other clade. Guayana Shield is remarkable, and we are not aware of any Based on this phylogenetic evidence, and its morphologi- other fern genus that has this distribution. cal distinctiveness, the Lellingeria mitchellae group is here The five species of Leucotrichum are divided into two segregated from Lellingeria, and described as a new genus, main clades, one containing two of the Caribbean/Mesoameri- as follows: can species, and another with the two Brazilian species plus the Antillean L. mortonii. The simplest explanation for this distri- Leucotrichum Labiak, gen. nov. – Type: Leucotrichum or- bution is to infer two independent colonization events into the ganense (Gardner) Labiak, comb. nov. ≡ Grammitis or- West Indies—once from Mesoamerica, and once from Brazil. ganensis Gardner in Hooker, Icon. Pl. 6: t. 509. 1843. Distinctive morphological characters. – The rhizome Diagnosis. – Filices parvulae, usque 15 cm longae, ad scales of Leucotrichum (absent in L. pseudomitchellae) are arbores suspensae vel petraeae. Caules erecti, simetrici, squa- clathrate and blackish, with the lumen of the cells almost mosi, squamis clatratis, margine ciliatis. Frondes pinnatifidae obscured by the thick cell walls. Scales are basally attached, vel pinnatisectae, lineari-lanceolatae, villosulae, setis lineari- usually linear-deltate, with simple and hyaline setae along the bus, simplicibus et hyalinis, pilis laminarum plerumque sim- margins and the apex (Fig. 2C). plicibus vel inaequaliter furcatis, hyalinis; segmentis obovatis The presence of hairs and setae impart a villose appearance vel deltato-linearibus; venis 1-furcatis, marginem non attin- to the leaves, especially the fertile ones. The setae are pluricel- gentibus, hydathodis adaxialiter praesentibus. Sori rotundi vel lular and whitish, varying from 1 to 3 mm long, and are usually elongati; sporangiis glabris vel ciliatis; sporis viridibus, trigonis found on petioles, rachises and laminar tissue. Their whitish rotundisque. color and softness (not dark reddish and rigid) is remarkable Description. – Plants epiphytic, rarely epipetric; roots when compared to the setae found in the other groups of gram- not proliferous; rhizomes erect, radial, scaly, the scales dark mitid ferns (e.g., Melpomene, Micropolypodium, Terpischore) brown to blackish, lanceolate to linear-lanceolate, clathrate, (Fig. 2F1). The hairs are of two types: (1) simple and unicellular,

◄ Fig. 1. 50% majority rule consensus tree from the Bayesian analyses of the combined dataset. The clade representing the new genus (Leucot- richum) is indicated by the vertical dark line, and its sister group (Terpsichore lanigera group), as well as the clade containing the remaining species of Lellingeria + Melpomene, are indicated by a gray line; asterisks indicate values of posterior probabilities (above the branches) and bootstrap (below the branches) equal to 1 and 100%, respectively.

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usually short (to 2 mm long), straight, and whitish; and (2) (Fig. 2D). They do not seem to be taxonomically informative, branched, the hairs consisting of three or more cells. The most either within the genus or between other grammitid genera. common branched type is composed of a short basal cell from The gametophytes, as well as the chromosome number for which two other cells arise—one short and glandular and an- Leucotrichum are still unknown. other longer and acicular (Fig. 2F2). The other type of branched Like many of other grammitid ferns, the species of Leu- hair comprises three basal cells, the two proximal ones bearing cotrichum are generally epiphytes, and occur most frequently one acicular cell each and the apical one apparently glandular in montane forests. (Fig. 2F3). Hairs can be present on all the parts of the leaf, but Etymology. – From the Greek, leuco-, white, and -trichum, are most conspicuous around the sori (Fig. 2A). hairs. This refers to the usually abundant whitish hairs and The veins in Leucotrichum are 1-furcate, ending in hy- setae on the laminar tissue abaxially. dathodes (Fig. 2B). Only the acroscopic branch on any given vein bears sporangia, and then only one sorus per segment is typically produced. The sori are round or slightly elongate, but Key to the species of Leucotrichum never confluent at maturity. With the exception of L. mitchellae (Fig. 2E), the sporangia are glabrous (Fig. 2A). 1. Sporangial capsule setose ...... 1. L. mitchellae The spores of Leucotrichum resemble those of the other 1. Sporangial capsule glabrous ...... 2 groups of grammitid ferns in being trilete, green, and papillate 2. Rhizomes without scales ...... 4. L. pseudomitchellae

Fig. 2. Morphology of some species of Leucotrichum and Terpsichore reclinata. A–B, L. schenckii (Labiak 2938, UPCB): A, abaxial laminar surface, showing the rachis, setae, and glabrous sporangia; B, hydathode on adaxial side of lamina. C–D, L. organense (La- biak 4499, UPCB): C, rhizome scale with ciliate margins; D, trilete spores. E, L. mitchellae (Ekman 14884, K), ciliate sporangium. F, setae and different hair types in Leucotrichum: F1, seta; F2, branched hair, with a short basal cell, one acicular cell, and one glandular cell; F3, branched hair, with two basal cells, two acicular cells, and one glandular cell at the apex. G–H, Terpsichore reclinata (Labiak 964, UPCB): G, ciliate rhizome scale; H, branched setae on laminar margin.

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2. Rhizomes scaly ...... 3 Nature Reserve, Ek Xux Canyon, 16°31′05″ N, 88°54′54″ W, 3. Laminae to 0.6 cm wide, pinnatifid, incised 1/3–1/4 to the 400–610 m, Davidse 36126 (MO). Guatemala. Vicinity rachis ...... 3. L. organense of Secanquim, Alta Verapaz, 450 m, Maxon & Hay 3195 (M, 3. Laminae to 0.4 cm wide, pinnatisect, incised 2/3–3/4 to NY, US). Belize. Stann Creek Valley, Antelope Ridge, Gentle the rachis ...... 4 3190 (NY, US); Toledo, Peck 972 (NY). Honduras. Moutain 4. Segments ascending (60°–70° to rachis), the apices acute Pine Ridge, Bartlett 11277 (US); Honduras–Guatemala bound- (Brazil) ...... 5. L. schenckii ary, 2700 ft., Schimp s.n. (US). Costa Rica. Alajuela, Upala, 4. Segments patent (80°–90° to rachis), the apices obtuse Dos Ríos, 5 km al Sur de Brasilia, 10°55′ N, 85°20′ W, 500 m, (Antilles) ...... 2. L. mortonii Herrera 1022 (MO). Panama. Distrito de Montijo, Isla Coiba, Playa Hermosa, Araúz 193 (US). 1. Leucotrichum mitchellae (Baker ex Hemsl.) Labiak, Distribution. – Cuba, Dominican Republic, Haiti, Mex- comb. nov. ≡ Polypodium mitchellae Baker ex Hemsl., ico, Belize, Guatemala, Honduras, Costa Rica, Panama; 200– Biol. Cent.-Amer., Bot. 3: 664. 1885. Xiphopteris mitch- 1000 m. ellae (Baker ex Hemsl.) Copel. in Amer. Fern J. 42: 97. Discussion – Leucotrichum mitchellae is readily recog- 1952. Grammitis mitchellae (Baker ex Hemsl.) F. Seym. in nized by its setose sporangial capsules, unique among the spe- Phytologia 31: 174. 1975. Lellingeria mitchellae (Baker ex cies of Leucotrichum (Figs. 2E and 3P). Hemsl.) A.R. Sm. & R.C. Moran in Amer. Fern J. 81: 86. Maxon (1914) described Polypodium shaferi based on a 1991 – Type: Belize (as British Honduras). Orange Walk, single specimen from Cuba, but the differences he presented Mitchell s.n. (lectotype, designated here, K!). (size of the rhizome scales, indument of the laminae, and tex- = Polypodium shaferi Maxon in Contr. U.S. Natl. Herb. 17: ture) are variable, and overlap with many specimens in the 410, pl. 13B. 1914 ≡ Grammitis shaferi (Maxon) Lellinger in Greater Antilles and Mesoamerica. Therefore, that name is Amer. Fern J. 74: 59. 1984. Lellingeria shaferi (Maxon) A.R. treated here as a synonym. Sm. & R.C. Moran in Amer. Fern J. 81: 86. 1991 – Type: Cuba. Oriente, near Camp la Gloria, south of Sierra Moa, 2. Leucotrichum mortonii (Copel.) Labiak, comb. nov. ≡ Shafer 8071 (holotype NY!; isotype US!). Figure 3N–P. Xiphopteris mortonii Copel. in Amer. Fern J. 42: 97. 1952. Plants epiphytic; rhizomes erect, with dark brown to black- Grammitis mortonii (Copel.) Lellinger in Amer. Fern J. 74: ish, oblong-lanceolate, clathrate rhizome scales 0.5–1.0 mm 59. 1984 – Type: Cuba. Oriente, crest of Sierra Maestra, long, margins ciliate; petioles absent to ca. 3.0 × 0.2 mm, between Pico Turquino and La Bayamesa, 1350 m, Morton greenish, with whitish, simple and 1-furcate hairs to 1 mm & Acuña 3547 (holotype US n.v.). Figure 3A–D. long; laminae erect to slightly arcuate, linear to linear-oblong, Plants epiphytic; rhizomes erect, with dark brown to black- texture membranaceous, pinnatisect, incised 1/2–2/3 to the ish, oblong-lanceolate, clathrate rhizome scales 1–2 mm long, rachis, to 7.0 × 0.5 cm, abruptly reduced at the base, with 1–2 margins ciliate; petioles absent to ca. 10 × 0.3 mm, stramine- reduced basal segments, the lowermost decurrent onto the peti- ous, with whitish, simple and 1-furcate hairs to 0.5 mm long; oles (forming short and broad wings), apices abruptly reduced, laminae erect to slightly arcuate, linear, texture membrana- ending in a rounded apical segment; rachises with dark scle- ceous, pinnatisect, incised 2/3–3/4 to the rachis, to 8 × 3(4) cm, renchyma, this not visible abaxially, obscured by laminar tissue abruptly reduced proximally, with 1–2 reduced basal segments, adaxially (sometimes visible on the lower third), with whitish the lowermost decurrent onto petioles (forming short and broad setae and simple to 1-furcate hairs, these conspicuous abaxi- wings), apices abruptly reduced, ending in a rounded apical ally, and scattered adaxially, 0.5–1.0 mm long; segments 2–3 × segment; rachises with dark sclerenchyma not visible abaxi- 1.0–1.5 mm, the margins entire, plane or slightly revolute, set ally, obscured by laminar tissue adaxially (sometimes visible 60°–70° to the rachis, the bases asymmetric, the apices obtuse, on the lower third), with whitish setae to 3 mm long, and simple covered by conspicuous whitish setae to 3 mm long and by to 1-furcate hairs, these conspicuous abaxially and scattered simple to 1-furcate hairs 0.5–1.0 mm long on the laminar tis- adaxially, to 0.5 mm long; segments 1.0–1.5 × 1.0 mm, the mar- sue; sinuses narrower than the segment width; veins 1-furcate, gins entire, plane or slightly revolute, set 80°–90° to rachises, obscured by the laminar tissue, adaxially with well–marked often overlapping, slightly asymmetric at base, apices rounded, hydathodes, these lacking a calcareous deposit; sori medial, covered by conspicuous whitish setae 2–3 mm long and simple round, one per segment, superficial, often surrounded by lami- to 1-furcate hairs 0.3–0.5 mm long on laminar tissue; sinuses nar setae; sporangial capsules setose. much narrower than the segment width; veins 1-furcate, ob- Additional specimens examined. – Cuba. Oriente, south scured by laminar tissue, adaxially with well-marked hyda- of lumber camp, crest of Sierra Nipe, 600–700 m, Morton & thodes, but these lacking a calcareous deposit; sori inframedial, Acuna 3141 (UC, US). Dominican Republic. Santo Do- rounded, only one per segment, superficial, often surrounded mingo, Península de Panama, Prov. de Samaná, topo de pan de by laminar setae; sporangia glabrous. Azucar, 510 m, Ekman 14884 (K, NY, S, US). Haiti. Massif du Additional specimens examined. – Dominican Repub- Nord, Emery, top of Mount Perroy, 1075 m, Ekman 8438 (S, US). lic. Cordillera Central, Bao River, upper Bao valley, 1700 m, Mexico. Chiapas, southeast of Palenque on road to Ocosingo Liogier 12876 (NY); Guáraca river valley, La Guáraca arriba, along the Jol Uk’um, Mun. Ocosingo, 550 m, Breedlove 48307 tributary to Bao River, Cordillera Central, 1300–1400 m, Lio- (NY). Belize. Toledo, Southern Maya Mountains, Bladen gier 13506 (NY), ibid., 1650–1950 m, Liogier 16026 (NY);

917 Labiak & al. • Leucotrichum, a new fern genus from the Neotropics TAXON 59 (3) • June 2010: 911–921

Loma Redonda, Ciénaga de La Culata, Constanza, 1600–1900 Discussion. – Leucotrichum mortonii is known only by a m, Liogier 16044 (NY); Loma Campanario, Ciénaga de la Cu- few collections from Cuba and the Dominican Republic. It is lata, Constanza, 2000 m, Liogier 17106 (NY); Loma de Torro, closely related to the Brazilian endemic L. schenckii, which Feb 1981, Phillips 121 (K). can be distinguished by the more acute, ascending and non- Distribution. – Cuba, Dominican Republic; 1300–2000 m. overlapping segments.

Fig. 3. A–D, Leucotrichum mortonii (Liogier 12876, NY): A, habit; B, rhizome scale; C, sporangium; D, hairs from the abaxial laminar surface. E–H, L. organense (Labiak 4499, UPCB): E, habit; F, rhizome scale; G, branched hair from costa; H, sporangium. I–L, L. schenckii (Labiak 2938, UPCB): I, habit; J, rhizome scale; K, hairs from the abaxial side of laminar tissue; L, Sporangium. M, L. pseudomitchellae (Mickel 3033, NY): habit. N–P, L. mitchellae (Ekman 14884, K): N, habit; O, rhizome scale; P, sporangium.

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Although only the image of the type at US has been seen, Serra dos Órgãos, Glaziou 4486 (P). Rio Grande do Sul: Bom the description provided by Copeland (1952) clearly describes Jesus, Aparados da Serra, Serra da Rocinha, 1000 m, Sehnem the main features defining this species: glabrous sporangia, 974 (PACA). Santa Catarina: Bom Retiro, Campo dos Padres, ciliate rhizome scales, and approximate segments. Leucotri- 1700 m, Sehnem 6972 (PACA). São Paulo: Serra da Bocaina, chum pseudomitchellae and L. mitchellae occur in the same Loefgren 4667 (S, SP, SPF). area, but the former differs by lacking rhizome scales, and the Distribution. – Endemic to the coastal Atlantic rain forests latter differs by having setose sporangial capsules. of southeastern and southern Brazil; 800–2000 m. Discussion. – Leucotrichum organense has the least di- 3. Leucotrichum organense (Gardner) Labiak, comb. nov. vided laminae in the genus (1/3 to 1/4 to the rachis). The most ≡ Grammitis organensis Gardner in Hooker, Icon. Pl. 6: closely related species is L. schenckii, which can be distin- tab. 509. 1843. Polypodium organense (Gardner) Mett. in guished by the narrower blades (to 0.4 cm wide) and more Abh. Senckenberg. Naturf. Ges. 2: 39. 1857. Lellingeria divided laminae (2/3 to the rachis). Some intermediate speci- organensis (Gardner) A.R. Sm. & R.C. Moran in Amer. mens can be found, and hybrids are expected between these Fern J. 81: 83. 1991 – Type: Brazil. Rio de Janeiro, Serra two species. dos Órgãos, Gardner 5913 (lectotype, designated here, K!; isolectotype BM!). 4. Leucotrichum pseudomitchellae (Lellinger) Labiak, = Grammitis organensis Fée, Crypt. Vasc. Brésil 2: 264. comb. nov. ≡ Grammitis pseudomitchellae Lellinger in 1873, nom. illeg., non Gardner (1843) – Type: Brazil. Rio Proc. Biol. Soc. Wash. 89: 383. 1985. Lellingeria pseudo- de Janeiro, “Habitat in brasilia fluminensi” Glaziou 3573 mitchellae (Lellinger) A.R. Sm. & R.C. Moran in Amer. (lectotype, here designated, P!; isolectotyes BM!, US! frag- Fern J. 81: 86. 1991 – Type: Costa Rica. Heredia, 10 km N ment). of San Rafael de Heredia on Volcán Barba, 1950 m, Mickel = Polypodium schenckii Hieron. var. villosa C. Chr. ex Dutra, 3033 (holotype NY!). Figure 3M. Anais Reuniao Sul-Amer. Bot. 2: 55. 1940, nom. nud. Plants epiphytic; rhizomes erect, without scales; petioles = Xiphopteris reitzii Alston in Lilloa 30: 110. 1960. Gram- absent to ca. 4 × 0.2 mm, greenish, with whitish, simple and mitis reitzii (Alston) Brade in Sellowia 18: 80. 1966 – Type: 1-furcate hairs to 1.5 mm long; laminae erect to slightly arcu- Brazil. Santa Catarina, Cambajuva, Reitz 3446 (holotype ate, linear to linear-oblong, texture membranaceous, pinnatifid, BM!; isotypes HB!, US!). incised 1/2–2/3 to the rachis, to 4.0 × 0.5 cm, abruptly reduced Figure 3E–H. proximally, with 1–2 reduced basal segments, the lowermost Plants epiphytic; rhizomes erect, with dark brown to black- decurrent onto petioles (forming short and broad wings), api- ish, oblong-lanceolate, clathrate rhizome scales 1.5–2.5 mm ces abruptly reduced, ending in a rounded apical segment; ra- long, margins ciliate; petioles absent to ca. 10 × 0.3 mm, green- chises with dark sclerenchyma, this visible abaxially, obscured ish, with whitish, simple and 1-furcate hairs to 1 mm long; by laminar tissue adaxially (sometimes visible on the lower laminae erect to slightly arcuate, linear to linear-oblong, texture third), with whitish setae 2–3 mm long and simple to 1-furcate membranaceous, pinnatifid, incised 1/3–1/4 to rachis, to 10 × hairs, these conspicuous abaxially and scattered adaxially, to 0.6 cm, abruptly reduced at the base, with 1–2 reduced basal 1.5 mm long; segments 1.0–1.5 × 1.0–1.5 mm, the margins segments, the lowermost decurrent onto petioles (forming short entire, plane or slightly revolute, not overlapping, set 60°–70° and broad wings), apices abruptly reduced, ending in a rounded to rachis, asymmetric at bases, apices obtuse, conspicuously apical segment; rachises with dark sclerenchyma, this not vis- covered by whitish setae and simple to 1-furcate hairs to 1 mm ible abaxially, obscured by laminar tissue adaxially (sometimes long on laminar tissue; sinuses narrower than segment width; visible on the lower third), with whitish setae 2–3 mm long, and veins 1-furcate, obscured by laminar tissue, adaxially with simple to 1-furcate hairs, these conspicuous abaxially, scattered well-marked hydathodes but lacking a calcareous deposit; adaxially, to 0.5 mm long; segments 2.0–2.5 × 1.0 mm, the sori inframedial, round, one per segment, superficial, often margins entire, plane or slightly revolute, not overlapping, set surrounded by laminar setae; sporangial capsules glabrous. 75°–85° to the rachises, the bases symmetric, the apices obtuse, Additional specimens examined. – Costa Rica. San covered by conspicuous whitish setae 1–2 mm long and by José, along Rio Zurqui (downstream from Guápiles highway), simple to 1(2)-furcate hairs 0.2–1.0 mm long on laminar tissue; Cordillera Central, 10°03′ N, 84°01′ W, 1400–1500 m, A.R. sinuses narrower than segment width; veins 1-furcate, obscured Smith & al. 1729 (UC). Panama. Cordillera above Camp 1, by laminar tissue, adaxially with well-marked hydathodes, but El Boquete, 1800–2000 m Killip 5289a (US); humid forest of these lacking a calcareous deposit; sori inframedial, elongate, the Cordillera, east of Río Caldera, 2150 m, Killip 5331 (US). one per segment, superficial, often surrounded by laminar se- Distribution. – Costa Rica, Panama; 1400–2150 m. tae; sporangial capsules glabrous. Discussion. – Leucotrichum pseudomitchellae can be rec- Additional specimens examined. – Brazil. Bahia: Morro ognized by the absence of rhizome scales, dark sclerenchyma do Chapéu, Morrão, 1200 m, Hatschbach 42410 (MBM, PACA). of rachises exposed abaxially, and by glabrous sporangia. It Espírito Santo: Castelo, Forno Grande, 1600 m, Brade 19853 resembles L. mitchellae in size and laminar shape, but that (RB). Minas Gerais: Camanducaia, Vila Monte Verde, 1500 m, species differs by having ciliate rhizome scales and setose spo- Handro 1020 (SP, SPF). Paraná: Morretes, Parque Estadual do rangial capsules. This species has the most narrowly restricted Marumbi, 1400 m, Labiak & al. 3404 (UPCB). Rio de Janeiro: distribution within the genus.

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5. Leucotrichum schenckii (Hieron.) Labiak, comb. nov. ≡ CNPq Proc. no. 201782/2008-1). Fieldwork was partially funded by Polypodium schenckii Hieron. in Hedwigia 44: 87. 1905. the Fundação O Boticário de Proteção à Natureza (Proc. 0756/2007-2). Polypodium setosum Schenck in Hedwigia 35: 166. 1869, We thank The New York Botanical Garden and the Cullman Program nom. illeg., non Thunberg (1784). Xiphopteris schenckii for Molecular Systematics, for providing herbarium and laboratory (Hieron.) Copel. in Amer. Fern J. 42: 94. 1952. Grammitis facilities. Part of this work utilized the resources of the Computational schenckii (Hieron.) Brade in Sellowia 18: 81. 1966. Lel- Biology Service Unit from Cornell University that is partially funded lingeria schenckii (Hieron.) A.R. Sm. & R.C. Moran in by Microsoft Corporation. We thank the Curators of AAU, B, BM, Amer. Fern J. 81: 83. 1991 – Type: Brazil. Santa Catarina, BR, F, FR, GH, HB, HBR, K, MAPR, MBM, MICH, MO, NY, P, Joinville, Schenck 1243 (holotype B!). Figure 3I–L. PACA, R, RB, S, SP, SPF, U, UC, UPCB, US, and WU for loans. We Plants epiphytic; rhizomes erect, with dark brown to black- also thank Thomas Couvreur for his help with the Bayesian analysis, ish, oblong-lanceolate, clathrate rhizome scales 1–2 mm long, Alan R. Smith for his helpful comments, Jefferson Prado and William margins ciliate; petioles absent to ca. 10 × 0.3 mm, green- Rodrigues for their help with the Latin diagnosis, and Diana Carneiro ish, with whitish, simple and 1-furcate hairs to 0.5 mm long; for preparing the line drawings. Finally, we are especially grateful to laminae erect to slightly arcuate, linear, texture membrana- Dr. Robbin Moran, whose support was fundamental to the develop- ceous, pinnatisect, incised 2/3–3/4 to the rachis, to 8 × 3(4) cm, ment of this study. abruptly reduced proximally, with 1–2 reduced basal segments, the lowermost decurrent to the petiole bases (forming short and broad wings), apices abruptly reduced, ending in a rounded LITERATURE CITED apical segment; rachis with dark sclerenchyma, this not visible abaxially, obscured by laminar tissue adaxially (sometimes vis- Bishop, L.E. 1988. Ceradenia, a new genus of Grammitidaceae. Amer. Fern J. 78: 1–5. ible on the lower third), with whitish setae to 2 mm long and Bishop, L.E. 1989. Zygophlebia, a new genus of Grammitidaceae. Amer. with simple to 1-furcate hairs, these conspicuous abaxially and Fern J. 79: 103–118. scattered adaxially, to 0.5 mm long; segments 1.0–1.5 × 1.0 mm, Copeland, E.B. 1952. The American species of Xiphopteris. Amer. the margins entire, plane, or slightly revolute, not overlapping, Fern J. 42: 93–110. set 60°–70° to rachis, slightly asymmetric at base, the apices Edgar, R.C. 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32: 1792–1797. obtuse, covered by conspicuous whitish setae ca. 2 mm long Geiger, J.M.O., Ranker, T.A., Ramp Neale, J.M. & Klimas, S.T. and by simple to 1-furcate hairs 0.3–0.5 mm long on laminar 2007. Molecular biogeography and origins of the Hawaiian fern tissue; sinuses narrower than segment width; veins 1-furcate, flora. Brittonia 59: 142–158. obscured by laminar tissue, adaxially with well-marked hy- Goloboff, P.A., Farris, J.S. & Nixon, K.C. 2008. TNT, a free program dathodes, but lacking a calcareous deposit; sori inframedial, for phylogenetic analysis. Cladistics 24: 774–786. round, one per segment, superficial, often surrounded by lami- Lehnert, M., Kessler, M., Schimdt-Lebuhn, A.N., Klimas, S.A., Fehlberg, S.D. & Ranker, T.A. 2008. Phylogeny of the fern ge- nar setae; sporangial capsules glabrous. nus Melpomene (Polypodiaceae) inferred from morphology and Specimens examined. – Brazil. Paraná: Ypiranga, 18 chloroplast DNA analysis. Syst. Bot. 34: 17–27. Sep 1908, Dusén 6735 (S). Rio de Janeiro: Campos Brejos, Maddison, W.P. & Maddison. D.R. 2009. Mesquite: A modular system Glaziou 7480B (P). Santa Catarina: Blumenau, Spitzkopf, for evolutionary analysis, version 2.6. http://mesquiteproject.org. 26°53′ S, 49°06′ W, 50–997 m, Smith & Reitz 6277 (US). São Maxon, W.R. 1914. Studies of tropical American ferns, new species of Paulo: Serra da Bocaina, próximo Casa do Peixe, Pabst 4759 Polypodium. Contr. U.S. Natl. Herb. 17: 398–411. Moguel, A. 2005. Taxonomische Revision der Artgruppe um Terpsi- (HB). Rio Grande do Sul: São Francisco de Paula, Dutra 759 chore lanigera. Ph.D. Thesis, University of Göttingen, Göttingen, (PACA). Germany. Distribution. – Endemic to the coastal Atlantic rain forest Nixon, K.C. 1999. The parsimony ratchet, a new method for rapid par- of southern and southeastern Brazil. simony analysis. Cladistics 15: 407–414. Discussion. – Leucotrichum schenckii is characterized Nylander, J.A.A., Ronquist, F., Huelsenbeck, J.P. & Nieves-Aldrey, J.L. 2004. Bayesian phylogenetic analysis of combined data. Syst. by its narrow, linear laminae (to 4 mm wide), incised 2/3–3/4 Biol. 53: 47–67. to the rachis, segments ascending with acute apices, glabrous Parris, B.S. 1990. Grammitidaceae. Pp. 153–157 in: Kramer, K.U. & sporangia, and scaly rhizomes. The most closely related spe- Green, P.S. (eds.), The families and genera of vascular plants, vol. cies is L. mortonii from the Antilles, which is distinguished by 1, Pteridophytes and gymnosperms. Berlin Springer. its rounded and more patent segments. Some small specimens Parris, B.S. 1997. Themelium, a new genus of Grammitidaceae (Fili- of L. organense can be confused with L. schenckii, especially cales). Kew Bull. 52: 737–741. Parris, B.S. 1998. Chrysogrammitis, a new genus of Grammitidaceae when the leaves are folded by dryness. However, they can be (Filicales). Kew Bull. 53: 909–918. distinguished by the laminar dissection. Parris, B.S. 2007. Five new genera and three new species of Gram- mitidaceae (Filicales) and the re-establishment of Oregrammitis. Gard. Bull. Singapore 58: 233–274. ACKNOWLEDGMENTS Ranker, T.A., Smith, A.R., Parris, B.S., Geiger, J.M.O., Haufler, C.H., Straub, S.C.K. & Schneider, H. 2004. Phylogeny and evolution of grammitid ferns (Grammitidaceae): A case of rampant This study was funded largely by a grant from the United States morphological homoplasy. Taxon 53: 415–428. National Science Foundation, to Dr. Robbin Moran (DEB 0717056), Ronquist, F. & Huelsenbeck, J.P. 2003. MrBayes 3: Bayesian phyloge- and by a grant to the senior author from the CNPq – Brazil (PDE netic inference under mixed models. Bioinformatics 19: 1572–1574.

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Schneider, H., Smith, A.R., Cranfill, R., Hildebrand, V., Haufler, H. & Wolf, P.G. 2006. A classification for extant ferns. Taxon C. H. & Ranker, T. A. 2004. Unraveling the phylogeny of poly- 55: 705–731. grammoid ferns (Polypodiaceae and Grammitidaceae): Exploring Smith, A.R., Pryer, K.M., Schuettpelz, E., Korall, P., Schneider, H. aspects of the diversification of epiphytic plants. Molec. Phylog. & Wolf, P.G. 2008. Fern classification. Pp. 417–467 in: Ranker, Evol. 31: 1041–1063. T.A. & Haufler, C.H. (eds.), Biology and evolution of ferns and Schuettpelz, E. & Pryer, K.M. 2007. Fern phylogeny inferred from lycophytes. Cambridge: Cambridge Univ. Press. 400 leptosporangiate species and three plastid genes. Taxon 56: Sundue, M.A., Islam, M. & Ranker, T.A. In press. Systematics of 1037–1050. grammitid ferns (Polypodiaceae): Using morphology and plastid Smith, A.R. 1993. Terpsichore, a new genus of Grammitidaceae (Pte- sequence data to resolve the circumscription of Melpomene and ridophyta). Novon 3: 478–489. portions of the polyphyletic genera Lellingeria and Terpsichore. Smith, A.R. & Moran, R.C. 1992. Melpomene, a new genus of Gram- Syst. Bot. mitidaceae (Pteridophyta). Novon 2: 426–432. Wilgenbusch, J.C., Warren, D.L. & Swofford, D.L. 2004. AWTY: A Smith, A.R., Moran, R.C. & Bishop L.E. 1991. Lellingeria, a new system for graphical exploration of MCMC convergence in Bayes- genus of Grammitidaceae. Amer. Fern J. 81: 76–88. ian phylogenetic inference. Available at http://ceb.csit.fsu.edu/ Smith, A.R., Pryer, K.M., Schuettpelz, E., Korall, P., Schneider, awty.

Appendix. Characters and character states used in this study. HABIT—1 Growth habit: (0) epiphytic, (1) epipetric, (2) terrestrial. 2 Position of fronds: (0) erect, (1) arching, (2) pendant, (3) prostrate or appressed to the substrate. ROOTS—3 Root insertion: (0) radial, (1) ventral. 4 Root proliferations: (0) absent, (1) present. RHIZOMES —5 Rhizome symmetry: (0) radial, (1) dorsiventral. 6 Internode length: (0) short-creeping with petioles contiguous or closely spaced along the rhizome, (1) long-creeping with petioles spaced at least five times the width of the petiole. 7 Phyllopodia: (0) absent, (1) present. 8 Rhizome branching: (0) commonly branched, (1) commonly unbranched. 9 Setae on rhizomes: (0) absent, (1) present. 10 Hairs on rhizomes: (0) absent, (1) present. 11 Rhizome scales: (0) absent, (1) present. 12 Rhizome scale attachment: (0) basifixed, (2) peltate. 13 Rhizome scale cell depth: (0) flattened or semiturgid, (1) turgid. 14 Rhizome scale base shape: (0) non-auriculate, (1) auriculate. 15 Rhizome scale shape: (0) ovate, (1) lanceolate. 16 Rhizome scale lumen: (0) concolorous, (1) clathrate. 17 Rhizome scale color: (0) orange to castaneous, (1) dark reddish to blackish, (2) light reddish-brown, (3) tan. 18 Rhizome scale iridescence: (0) non-iridescent, (1) iridescent. 19 Rhizome scale marginal indument: (0) absent, (1) present. 20 Rhizome scale marginal indument distribution: (0) distributed evenly along the margin, (1) restricted to scale apex. 21 Rhizome scale indument type: (0) unicellular, and egandular cilia, (1) simple glandular hairs which are either unicellular or multicellular. 22 Rhizome scale cilia color: (0) orange to castaneous, (1) clear to whitish, (2) reddish, (3) tan. 23 Rhizome scale abaxial and adaxial surface: (0) glabrous, (1) provided with indument. 24 Rhizome scale apical papillate cells: (0) absent (1) present. 25 Rhizome scales, number of apical and subapical papillate cells: (0) one, (1) two or more. FRONDS—26 Frond growth: (0) determinate, (1) indeterminate. PETIOLES—27 Leaf articulation: (0) non-articulate, (1) articulate. 28 Epidermis of petiole: (0) sclerenchymatous, (1) parenchymatous. 29 Petioles, number of vascular bundles: (0) 1, (1) 2, (2) ≥3. 30 Petiole lateral margin: (0) marginate throughout, (1) distally marginate, (2) without any lateral margin. LAMINAE—31 Lamina base shape: (0) tapered, (1) truncate. 32 Laminar apex shape: (0) gradually reduced, (1) abruptly reduced to a conform terminal segment. 33 Laminar dissection at base: (0) simple (undivided), (1) pinnatifid, (2) pinnatisect, (3) 1-pinnate. 34 Pinna apex shape: (0) acute, (1) rounded. 35 Lamina texture: (0) chartaceous, (1) membranaceous, (2) coriaceous. VENATION—36 Presence of sclerenchyma on veins: (0) present only along the pinna costa, (1) present on pinna costa as well as next order veins, (2) present on pinna costa and next order veins but absent on second order veins, (3) present only on the proximal half of first order veins, (4) absent entirely. 37 Sclerenchyma of midrib abaxially: (0) not visible, (1) visible. 38 Sclerenchyma of midrib adaxially: (0) not visible, (1) visible. 39 Sclerenchyma of pinna costae abaxially: (0) not visible, (1) visible throughout its length, (3) visible only in the proximal portion. 40 Sclerenchyma of pinna costae adaxially: (0) not visible, (1) visible. 41 Sclerenchyma of veins abaxially: (0) not visible, (1) visible. 42 Sclerenchyma of veins adaxially: (0) not visible, (1) visible. 43 Vein order: (0) two, (1) three, (2) four or more, (3) none [veins beyond the pinna costa absent]. Scored here with the pinna costa considered as the first order vein. 44 Secondary vein branching pattern: (0) dichotomous, (1) anisotomous. Not applicable for simple secondary veins. 45 Vein fusion: (0) absent, (1) present (at least in sterile fronds). 46 Hydathodes: (0) absent, (1) present. 47 Cretaceous deposit from hydathodes: (0) absent, (1) present. Not applicable for taxa that lack hydathodes. LAMINAR INDUMENT—48 Laminar scales: (0) absent, (1) present. 49 Laminar scale color: (0) concolorous, (1) clathrate. 50 Setae of fronds: (0) absent, (1) present. 51 Seta branching pattern: (0) simple, (1) bifurcate, (2) stellate. Not applicable for taxa that lack setae. 52 Seta color: (0) reddish, (1) whitish. 53 Setae on petiole: (0) absent, (1) present. Not applicable for taxa that lack setae. 54 Setae on adaxial midrib: (0) absent, (1) present. Not applicable for taxa that lack setae. 55 Rachis setae uni- formity: (0) uniform in length, (1) with distinctly long and short hairs mixed. 56 Setae along laminar margins: (0) absent, (1) present. Not applicable for taxa that lack setae. 57 Distribution of setae along laminar margins: (0) evenly spaced, (1) confined to apex of pinna or segment. Not applicable for taxa that lack marginal setae or that lack setae entirely. 58 Setae on adaxial laminar surface: (0) absent, (1) present. Not applicable for taxa that lack setae. 59 Setae on abaxial laminar surface: (0) absent, (1) present. Not applicable for taxa that lack setae. 60 Setae on adaxial pinna costa: (0) absent, (1) present. Not applicable for taxa that lack setae. 61 Hairs of fronds: (0) absent, (1) present. 62 Branching pattern of hairs: (0) simple, (1) 1-furcate, (2) 2-furcate, (3) 3-furcate. Not applicable for 1-celled hairs. 63 Number of cells in hairs: (0) 2-celled, (1) 3-celled, (2) greater than 3-celled, (3) unicellular. 64 Shape of hair cells, or hair branch cells: (0) acicular, (1) setose, (2) capitate including globose or glandular, (3) unmodified. 65 Color of capitate or glandular cell in hairs: (0) white and opaque, (1) translucent. Not applicable for taxa that do not have glandular cells in their hairs. 66 Gland cell secretion: (0) secretory, (1) non-secretory. Not applicable for taxa with glandular cells that are not secretory, and taxa that lack glands. SORUS AND SPORANGIA—67 Sori distinct or confluent: (0) distinct, (1) confluent, forming a coenosorus. 68 Soral position relative to laminar margin and penultimate axis (0) inframedial, (1) medial, (2) intramarginal. Not applicable for those that have more than a single series of sori between the margin and the penultimate axis. 69 Distribution of sori: (0) throughout the lamina, (1) confined to the distal portion of lamina. 70 Outline of mature sorus: (0) round, (1) elliptic—up to 2× as long as wide, (2) elongate—more than 2× longer than wide. 71 Sorus position relative to surface of lamina: (0) complanate upon the surface of the lamina, (1) immersed into the surface of the lamina. 72 Sori embossed on adaxial side of the lamina: (0) not embossed, (1) embossed. 73 Sori partially covered by infolded lamina margin: (0) not folded, (1) folded, (2) partially folded. 74 Paraphyses: (0) absent (1) present. Receptacular setae are scored separately. 75 Cells of paraphyses: (0) unmodified cells, (1) whitish, opaque glands, (2) translucent glands, (3) setose branches, (4) acicular branches, (5) reddish glands. 76 Receptacular setae: (0) absent, (1) present. Not applicable for plants that lack setae. 77 Sporangial stalk width at mid-stalk: (0) 2–3 cells wide, (1) 1 cell wide. 78 Episporangial indument: (0) absent, (1) present. 79 Position of episporangial indument: (0) the side wall of the capsule, (1) from the annulus. Not applicable for taxa that lack episporangial indument. 80 Aggregation of episporangial indument: (0) scattered, (1) aggregated. Not applicable for taxa that lack episporangial indument. SPORES—81 Spore color: (0) yellow, (1) green. 82 Spore number: (0) 64, (1) 32, (2) 16. 83 Spore laesurae: (0) linear, (1) triradiate. 84 Number of cells in newly shed spores: (0) one, (1) two, (2) three to four. CHROMOSOME BASE NUMBER—85 Chromosome base number: (0) 37, (1) 35, (2) 33, (3) 32. FUNGAL RELATIONS—86 Mycelia and ascomes of Acrospermum: (0) absent, (1) present. SECONDARY COMPOUNDS—87 Aromatic when dry: (0) absent, (1) present.

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