TAXON 60 (4) • August 2011: 1123–1137 Hirai & al. • New Neotropical fern genus Moranopteris
Moranopteris: A new Neotropical genus of grammitid ferns (Polypodiaceae) segregated from Asian Micropolypodium
Regina Y. Hirai,1 Germinal Rouhan,2 Paulo H. Labiak,3 Tom A. Ranker4 & Jefferson Prado1
1 Instituto de Botânica, Caixa Postal 68041, CEP 04045-972, São Paulo-SP, Brazil 2 Muséum national d’Histoire naturelle, UMR CNRS 7205 ‘Origine, Structure et Evolution de la Biodiversité’, Botanique, 16 rue Buffon CP 39, 75005 Paris, France 3 Universidade Federal do Paraná, Departamento de Botânica, Caixa Postal 19031, CEP 81531-980, Curitiba-PR, Brazil 4 Department of Botany, University of Hawaii, 3190 Maile Way, Honolulu, Hawaii 96822, U.S.A. Author for correspondence: Regina Y. Hirai, [email protected]
Abstract Moranopteris, a new genus of grammitid ferns here described, is segregated from Micropolypodium on the basis of molecular phylogenetic analyses (plastid sequences including atpB, rbcL, and trnL-trnF) and morphological characters. Bayesian and maximum parsimony analyses support Moranopteris as sister clade to a group that includes Micropolypodium s.str. and 11 or 12 other genera, mostly from the Old World. A morphological synapomorphy for the species of Moranopteris is the presence of minute and slightly catenate branched hairs (with or without a setiform branch) and sometimes unbranched hairs occurring together on the stipes, costae, and laminar tissues abaxially. In contrast, Micropolypodium s.str. has only minute, catenate, and unbranched hairs borne on the same parts of the leaves. The new genus Moranopteris comprises 28 spe- cies—including two new species here described, M. rupicola and M. simplex—and one hybrid, occurring in the Neotropics. The 27 necessary new combinations are here proposed. Our results suggest that Micropolypodium is confined to eastern Asia.
Keywords cpDNA; Grammitidaceae; molecular phylogeny; Neotropics; Paleotropics
Supplementary Material The alignment is available in the Supplementary Data section of the online version of this article (http://www.ingentaconntect.com/content/iapt/tax).
INTRODUCTION netic analyses (using rbcL, atpB, and trnL-F) on a grammitid fern genus. The first phylogenetic study focusing on the gram- Hasebe & al. (1994, 1995) and Pryer & al. (1995) first mitid ferns worldwide, however, was conducted by Ranker investigated fern phylogeny based on rbcL, and morphology & al. (2004), who included 73 species of grammitid ferns (rep- plus rbcL, respectively. Hasebe & al. (1994) showed that Poly- resenting 16 genera) and using molecular (plastid sequences podiaceae Bercht. & J. Presl plus Grammitidaceae Newman atpB and rbcL) as well as morphological characters. Results form a monophyletic group. These studies provided the first of this latter study highlighted that many of the traditionally insight that Polypodiaceae were not monophyletic, because recognized genera were not monophyletic. For example, none of Grammitidaceae appear nested within it. However, in these the classically accepted genera, e.g., Ctenopteris Blume, Gram- studies, the family Grammitidaceae was represented by a single mitis Sw., Prosaptia C. Presl, and Xiphopteris Kaulf. were species, Micropolypodium okuboi (Yatabe) Hayata, the type of supported as monophyletic. Furthermore, some more recently Micropolypodium Hayata. described genera, e.g., Lellingeria A.R. Sm. & R.C. Moran, Using three plastid regions (the two genes rbcL and rps4, and Terpsichore A.R. Sm., were also not supported as mono- and the intergenic spacer rps4-trnS) and expanding the sam- phyletic. pling of so-called polygrammoid ferns (Polypodiaceae s.str. In the last few years, phylogenetic studies have been per- and grammitids) to 98 selected species, Schneider & al. (2004) formed to resolve relationships within predominantly New obtained similar results, and further recovered Grammitida- World grammitids, i.e., Melpomene A.R. Sm. & R.C. Moran ceae as monophyletic but still nested within a larger clade cor- (Lehnert & al., 2009), Lellingeria (Labiak & al., 2010a, b), responding to Polypodiaceae s.l. Grammitidaceae, therefore, Terpsichore (Sundue & al., 2010), and the “Lellingeria myo- are now usually referred to informally as the “grammitid ferns”. suroides clade” (Ranker & al., 2010). Based on these findings, Smith & al. (2006, 2008), in their Ranker & al. (2004) showed that Micropolypodium was classification for the leptosporangiate ferns, included all genera not monophyletic, with species of the genus Terpsichore nested formerly treated as Grammitidaceae (e.g., Parris, 1990; Smith, within it. In their analyses, out of 24 known Micropolypodium 1995) in Polypodiaceae, which, according to this circumscrip- species (Smith, 1992: 22 in the New World and two in the Pa- tion, would comprise ca. 1200 species and 56 genera. leotropics; none shared by these two areas), they sampled only In their study of the Hawaiian Adenophorus Gaudich., three Neotropical species (Micropolypodium taenifolium (Jen- Ranker & al. (2003) were the first to focus molecular phyloge- man) A.R. Sm., M. zurquinum (Copel.) A.R. Sm., M. hyalinum
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(Maxon) A.R. Sm.), and no Asian taxa. Mickel & Smith (2004) to 62 species representing 22 grammitid genera. Voucher in- mentioned some preliminary, unpublished molecular results on formation and GenBank accession numbers are listed in the Neotropical species of Micropolypodium indicating that the Appendix. Asian species (including the type of the generic name, M. oku- DNA extraction. — Genomic DNA was isolated from ei- boi) of Micropolypodium s.str. were not most closely related to ther field-collected, silica gel–dried leaves or from herbarium the Neotropical species. specimens when fresh material was unavailable. Total genomic According to Ranker & al. (2004), the Neotropical spe- DNA was extracted using the Qiagen DNeasy Plant Mini Kit cies of Micropolypodium formed a well-supported clade that (Valencia, California, U.S.A.) following the manufacturer’s included two, and possibly three, species of the Terpsichore protocol, but with an additional proteinase K digestion during achilleifolia group as defined by Smith (1993): T. achilleifolia the lysis step for the herbarium material: 30 μL of proteinase (Kaulf.) A.R. Sm., T. longisetosa (Hook.) A.R. Sm., and, pos- K (20 mg/mL), and 30 μL of β-mercaptoethanol (98%) were sibly, T. gradata (Baker) A.R. Sm. Although the last taxon was added per tube, and the tubes were incubated on a tipping plate not included in analyses by Ranker & al. (2004), it appeared at 42°C for 12 hours. to be related to the two other species of Terpsichore, and all Amplifications and sequencing. — Three plastid DNA three species are morphologically similar to Micropolypodium sequences were amplified by PCR, the two coding regions atpB because of their orangish to golden rhizome scales, leaves with and rbcL, and the non-coding spacer trnL-trnF. For atpB, we determinate growth, conspicuous hydathodes on the adaxial used the primers ESATPB172F and ESATPE45R (Schuettpelz laminar surfaces, and dark red-brown unbranched setae on & Pryer, 2007), for rbcL the primers ESRBCL1F and ESRB- laminar tissues. Based on these results of Ranker & al. (2004), CL1361R (Schuettpelz & Pryer, 2007), and for trnL-trnF the Labiak & Matos (2007) described and assigned a new hybrid primers “e” and “f ” (Taberlet & al., 1991). The two genes were from Rio de Janeiro (Brazil) to Micropolypodium (M. ×bra- typically amplified using a program beginning with one initial dei Labiak & F.B. Matos), and also combined T. achilleifolia denaturation step of 5 min at 94°C, followed by 35 cycles of and T. gradata in the genus (= M. achilleifolium (Kaulf.) Labiak 1 min at 94°C, 1 min at 50°C, 2.5 min at 72°C, and a final & F.B. Matos and M. gradatum (Baker) Labiak & F.B. Matos). extension period of 10 min at 72°C. For trnL-F, we used the Because Ranker & al. (2004) did not include any Paleotrop- following protocol: 5 min at 94°C/35× (1 min, 94°C; 30 s, 50°C; ical Micropolypodium in their sampling, and because levels of 1 min, 72°C)/7 min at 72°C. The PCR products were sequenced morphological homoplasy are high among the Neotropical and by the High-Throughput Genomics Unit at the University of Paleotropical species of Micropolypodium (and more generally Washington, using the amplification primers plus the internal among all grammitid ferns; Ranker & al. 2004), we conducted primers 493F and 910R for atpB (Schuettpelz & Pryer, 2007), molecular phylogenetic studies focused on Micropolypodium and ESRBCL628F and ESRBCL654R for rbcL (Schuettpelz with a much broader sampling of the species named in the & Pryer, 2007). genus. The three major aims of this study were (1) to test the Alignment and phylogenetic analyses. — Forward and monophyly of Micropolypodium s.l.; (2) to confirm the mono- reverse sequences obtained for all species were edited and as- phyly of the Neotropical species of Micropolypodium, as sug- sembled using Sequencher v.4 (Gene Codes Corporation, Ann gested by previous studies (Ranker & al., 2004); and (3) to Arbor, Michigan, U.S.A.). Consensus sequences were then au- investigate the evolutionary relationships between Micropoly- tomatically aligned using Muscle v.3.6 using the default param- podium and other grammitid genera; the here presented results eters (Edgar, 2004), and the resulting alignments were manu- will lay the foundation for a taxonomic revision of the lineage. ally checked using the MUST package (Philippe, 1993) and revised to maximize the similarity between sequences. Data matrices were constructed using TaxonDNA v.1.6.2. (Meier MATERIALS AND METHODS & al., 2006) and analyzed using equally weighted maximum parsimony and Bayesian inference, with indels treated as miss- Taxonomic sampling. — Outgroup taxa were selected ing data. based on the studies by Schneider & al. (2004), and in- Maximum parsimony analyses (MP) were performed us- cluded Polypodium vulgare L., Pecluma eurybasis (C. Chr.) ing the program PAUP* v.4.0b10 (Swofford, 2002). For all MP M.G. Price, Microgramma bifrons (Hook.) Lellinger, Micro- analyses, heuristic searches were performed with 10,000 ran- gramma percussa (Cav.) de la Sota, and Serpocaulon triseriale dom-sequence addition replicates, tree bisection-reconnection (Sw.) A.R. Sm. (TBR), branch swapping, and the Multrees options were on. To test the monophyly of Micropolypodium s.l., and to at- The robustness of each node was assessed by a non-parametric tempt to identify its sister group, representatives of most Neo- bootstrap analysis (BS; Felsenstein, 1985), with 1000 replicates tropical and Paleotropical grammitid genera were included of similar heuristic searches (each replicate with 3 random-se- in the sampling. They represent all major clades known for quence addition replicates). Because all characters were equally grammitids (Ranker & al., 2004). sampled, parsimony-uninformative characters could have had For Micropolypodium, two out of three known Asian spe- a significant effect on robustness and were removed before the cies and 19 out of 24 known Neotropical species (Smith, 1992; bootstrap procedure (Desalle & al., 2002). For comparison, Labiak & Matos, 2007) were sampled, plus Terpsichore longi- another bootstrap procedure was conducted leaving all char- setosa. The final matrix included 75 terminals, corresponding acters including parsimony-uninformative ones; the resulting
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bootstrap values were unchanged or very similar with respect 1997). These leaves were drawn to show the venation patterns to each node (values differed by at most 4% from a procedure and hairs in the genus. Hairs were measured on Herbarium to the other one). specimens. Bayesian analyses (BI) were performed using the program MrBayes v.3.1.2 (Huelsenbeck & Ronquist, 2001; Ronquist & Huelsenbeck, 2003). The GTR + Γ + I model of nucleotide RESULTS substitution was identified as the best fit to the data for each of the three regions under the Akaike information criterion Results for each analysis and for each DNA region, includ- (AIC; Akaike, 1973) as implemented in the program jModelTest ing the number of characters and taxa included, percentages v.0.1.1 (Posada, 2008). Two independent but parallel analy- of variable and informative sites, number of MP trees, tree ses were conducted using flat priors, starting from random lengths, consistency and retention indices (CI; RI), and substi- trees and consisting of four chains each. The analyses were tution models used in BI are summarized in Table 1. run for 5 million generations, sampling every 100 generations. The analyses performed for the combined dataset produced Following completion of the analyses, the output parameter trees with improved resolution and higher support node values estimates through time were explored in order to recognize compared to those obtained from separate datasets. Thus, only the point of convergence to the stationary distribution, using the results from the combined dataset using MP and BI analy- Tracer v.1.5 (Rambaut & Drummond, 2004). This was reached ses are described and discussed. Tree topologies were similar after approximately 150,000 generations, and the first 500,000 regardless of the analytical method employed, i.e., the strict generations (5000 trees) of one of the runs were conservatively consensus obtained in MP was nearly identical to the majority excluded as the “burn-in”. We pooled the post–burn-in trees consensus tree resulting from BI analyses, except for some (45,000 total trees) and computed a 50% majority-rule consen- unresolved relationships and the placement of three terminals, sus with average branch lengths and posterior probability (PP) Chrysogrammitis Parris, Ctenopterella Parris, and Grammitis estimates for all nodes. deplanchei (Baker) Copel. (Fig. 1). Taxonomic treatment. — For the Neotropical Micropoly- The results of these analyses show Micropolypodium s.l. podium clade, which is here described as a new genus, all the as not monophyletic. All Neotropical species of Micropoly- necessary new combinations are proposed, as well as a com- podium s.l. form a clade (M. truncicola (Klotzsch) A.R. Sm. plete list of homotypic synonyms for each species. Based on through M. grisebachii (Underw. ex C. Chr.) A.R. Sm.) that is morphology, two new species are described. In particular, strongly supported (Fig. 1; BS = 94%; PP = 1.0). The two Asian spores and laminar tissues harbor critical characters (the micro- species of Micropolypodium are grouped together (M. okuboi morphology of the perispores and bases of setae, respectively). and M. sikkimense (Hieron.) X.C. Zhang; BS = 78%; PP = 1.0) Taken from herbarium specimens of Micropolypodium at NY and rooted in a broader clade comprising 11 other Paleotropical and UC, spores and laminar tissues were imaged using a scan- grammitid genera in BI (Calymmodon C. Presl, Scleroglossum ning electron microscope (SEM). Spores and laminar tissues Alderw., Tomophyllum (E. Fourn.) Parris, Dasygrammitis Par- were transferred with dissecting needles from the specimens ris, Ctenopterella, Grammitis, Oreogrammitis Copel., Radio- to SEM stubs coated with an adhesive tape. The stubs were grammitis Parris, Themelium (T. Moore) Parris, Prosaptia, then coated with gold-palladium in a sputter-coater for 30 to Ctenopteris) or 12 in MP analyses (adding Chrysogrammitis). 40 seconds and imaged digitally using a JEOL JSM-5410LV Within the Neotropical clade, here treated as the new ge- SEM equipped with a JEOL Orion 5410 software interface. nus Moranopteris, the basal polytomy resulting from the MP The accelerating voltage was 15 kV. analyses precludes the assessment of the relationships among Leaf tissue clearings were made for almost all species, the species. Although this polytomy is resolved in BI, the re- using the Strittmatter method (1973; apud Kraus & Arduin, lationships are poorly supported (PP < 0.9). Two major sister
Table 1. Number of taxa and characters, evolutionary models used in BI, and tree statistics for the MP analyses. atpB rbcL trnL-trnF Combined Total number of taxa/ingroup only 69/31 71/33 57/32 75/36 Included characters 1357 1311 404 3072 Variable characters (%) 359 (26) 346 (26) 259 (64) 964 (31) Parsimony-informative characters (%) 254 (19) 236 (18) 192 (47) 682 (22) Consistency index 0.45 0.43 0.50 0.44 Retention index 0.65 0.65 0.70 0.64 Number of MP trees 156 56,243 458 12 MP tree length 979 987 845 2938 BI substitution model GTR + Г + I GTR + Г + I GTR + Г + I GTR + Г + I
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Fig. 1. Concatenated phylogram obtained with the Bayesian inference +/95 Moranopteris truncicola and strict consensus of the 12 most parsimonious trees resulting from +/91 Moranopteris truncicola the MP analysis, based on the combined dataset atpB + rbcL + trnL-F. +/+ Moranopteris taenifolia +/75 Moranopteris taenifolia Irresolution and topology differing in the strict consensus MP tree +/+ Moranopteris caucana are indicated by dashed lines. Statistical support values PP > 0.50 and +/96 Moranopteris caucana +/79 BS > 50 are indicated on the branches as PP/BS, with PP = 1 and BS = -/63 Moranopteris cookii 100% appearing as “+”. Geographic distributions are indicated in the Moranopteris williamsii +/+ Moranopteris microlepis grey frames for the two distinct clades discussed in the text, the new +/91 Moranopteris microlepis +/75 genus Moranopteris and Micropolypodium s.str. Moranopteris plicata .99/- Moranopteris serricula +/+ Moranopteris serricula
+/98 Moranopteris zurquina Neotropics .95/46 +/+ Moranopteris trichomanoides Moranopteris trichomanoides .99/76 Moranopteris blepharidea +/+ Moranopteris hyalina +/84 Moranopteris hyalina Moranopteris hyalina Moranopteris perpusilla Moranopteris nana Moranopteris setosa Moranopteris achilleifolia Moranopteris gradata Moranopteris .98/79 Moranopteris aphelolepis +/94 (formerly: Micropolypodium s.l.) +/+ Moranopteris aphelolepis +/64 Moranopteris basiattenuata +/92 Moranopteris longisetosa Moranopteris longisetosa Moranopteris grisebachii +/75 Oreogrammitis hookeri +/70 Radiogrammitis parva +/96 Themelium conjunctisorum +/51 Prosaptia contigua Prosaptia nutans Ctenopterella denticulata +/- +/84 Grammitis poeppigiana +/97 Grammitis billardierei .92 /- Ctenopteris heterophylla Grammitis deplanchei Ctenopteris lasiostipes
.96/57 Paleotropics +/93 Micropolypodium okuboi +/75 +/75 Micropolypodium okuboi +/78 Micropolypodium s.str. Micropolypodium okuboi .61/67 +/+ Micropolypodium sikkimense + /56 Micropolypodium sikkimense Calymmodon gracilis +/69 +/- Scleroglossum sulcatum Tomophyllum repandulum +/96 Dasygrammitis crassifrons +/+ Chrysogrammitis glandulosa Chrysogrammitis musgraviana -/66 Lellingeria apiculata +/99 Lellingeria limula +/99 +/+ Melpomene moniliformis Melpomene flabelliformis Ascogrammitis pichinchae .99 +/96 Enterosora percrassa Ceradenia spixiana 1 Terpsichore lanigera +/+ 1 Terpsichore cultrata Leucotrichum schenckii +/+ Cochlidium punctatum +/+ Cochlidium serrulatum .92/- Grammitis bryophila +/+ Adenophorus tripinnatifidus -/73 Grammitis tenella +/72 +/+ Terpsichore lehmanniana Terpsichore asplenifolia Serpocaulon triseriale +/65 Microgramma percussa Microgramma bifrons Polypodium vulgare Pecluma eurybasis 0.1 substitution/site
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clades were well supported, the first comprising M. blephari- Calymmodon is putatively sister to Micropolypodium s.str. dea and M. hyalina (4 terminals BS = 84%; PP = 1.0), and the Furthermore, Scleroglossum plus Tomophyllum form a mono- second consisting of 10 species from M. truncicola to M. tri- phyletic group, sister to Micropolypodium s.str. plus Calym- chomanoides (16 terminals, BS = 75%; PP = 1.0). modon; although not strongly supported, these relationships The MP analysis shows a large, poorly supported clade (BS were found in previous studies (Ranker & al., 2004; clade III). = 57%) formed of primarily Paleotropical species of grammitid The placement of Chrysogrammitis is still uncertain, as found genera (including Micropolypodium s.str. and Chrysogrammi- by Ranker & al. (2004). It is strongly supported only with BI, tis) as the sister group to the Neotropical Moranopteris clade. In recovered as the sister clade to Paleotropical grammitid genera the BI analysis, Chrysogrammitis from SE Asia through Male- plus the Neotropical clade of Micropolypodium s.l. (includ- sia to Melanesia (Parris, 1998) is recovered as sister group to the ing the Terpsichore achilleifolia group). By contrast in MP large clade (PP = 1.0) comprising the Neotropical Moranopteris analyses, Chrysogrammitis appeared as a weakly supported clade plus the clade with Micropolypodium s.str. and other sister group to Ctenopterella and Grammitis, both included in Paleotropical genera. the Paleotropical clade. Schuettpelz & Pryer (2007), in their The relationships among Paleotropical genera remain un- phylogenetic study based on three plastid genes (rbcL, atpB, clear with both analyses. Calymmodon is weakly supported (BS atpA), retrieved the Paleotropical Chrysogrammitis musgra- < 70%; PP = 0.61) as sister to Micropolypodium s.str. Addition- viana (Baker) Parris as sister group to Micropolypodium s.l. ally, Scleroglossum and Tomophyllum form a clade that is closely (M. hyalinum and M. taenifolium), although it was not strongly related to Micropolypodium s.str. plus Calymmodon (BS = 56%; supported either. Sundue & al. (2010) obtained a similar result, PP = 1.0). i.e., the Neotropical species of Micropolypodium (including Terpsichore longisetosa) appeared in a strongly supported clade (BS = 100%), and this clade is sister to Chrysogram- DISCUSSION mitis musgraviana. Based on phylogenetic evidence, as well as morphological Our results support two distinct clades of Micropolypo- characters, the Neotropical species of Micropolypodium s.l. dium. One includes all of the sampled Neotropical species are here segregated from Micropolypodium s.str., a name now (Moranopteris) and the other all of the sampled Paleotropical restricted to a group from eastern Asia. We propose a new species, as previously suggested by Ranker & al. (2004) and generic name Moranopteris for the Neotropical clade, with the Mickel & Smith (2004). following description: The Neotropical species of Micropolypodium differ from the Paleotropical species of Micropolypodium most obviously Moranopteris R.Y. Hirai & J. Prado, gen. nov. – Type: Mo- in the morphology of the hairs on fronds. They are slightly cat- ranopteris basiattenuata (Jenman) R.Y. Hirai & J. Prado enate, unbranched and branched on stipes, rachises, or costae (see below). and laminar tissues, mainly abaxially, whereas hairs are only Diagnosis. – Primo aspectu ad Micropolypodio valde ac- catenate and unbranched on the Paleotropical taxa. There may cedit, sed frondibus cum pilis leviter catenulatis ramosis et be other characters that are exclusive to the Neotropical clade non-ramosis, pilis ramosis cum ramis setaceis et non-setaceis of Micropolypodium s.l., but additional studies are necessary (vs. frondibus solum cum pilis non-ramosis), distributio neo- to address this issue (e.g., the ontogeny of setae and leaf vena- tropica (vs. veteri-mundi) distincta. tion patterns). Description. – Plants epiphytic, rarely epipetric or ter- Our results corroborate the placement of the three species restrial. Rhizomes short-creeping, decumbent to ascending, considered in the Terpsichore achilleifolia group (group 5 of slightly dorsiventral to radially symmetric, scaly, the scales Smith, 1993) as being members of the clade with the Neotropi- golden to castaneous, often lustrous, nonclathrate, the cells cal species of Micropolypodium, as first suggested by Ranker of the scales body turgid and shining, margins entire or bear- & al. (2004) and supported by Sundue & al. (2010). In addition ing small, hyaline, lateral projections, or with glanduliform or to the molecular phylogenetic support, taxa of the T. achillei setiform projections, these setiform projections mostly red- folia group are morphologically more similar to Neotropical brown, rarely hyaline, apical or subapical gland-like cells pres- Micropolypodium than to the remaining groups of Terpsichore ent or not. Leaves monomorphic, caespitose, erect to pendent, s.l., from which they differ by displaying orangish to golden determinate, or rarely ± indeterminate (M. caucana, M. kil- rhizome scales and red-brown unbranched setae (Smith, 1993). lipii), short-stipitate, sometimes the stipes almost absent, not Parris (2009) recognized Micropolypodium s.str. in Male- articulate to the rhizomes; laminae mostly linear, sometimes sia as having radial rhizomes with fronds in whorls, and as lanceolate, pinnatifid or pinnatisect, rarely bipinnatisect or having pale to medium brown, non-clathrate and glabrous rhi- pinnate-pinnatisect, sometimes pinnate only at base, gradually zome scales, laminae deeply pinnately divided to pinnate, one tapering proximally to a lateral narrow wing or not, mostly sorus per lobe of pinna, medium to dark brown simple hairs chartaceous, sometimes membranaceous; costae obscured by (i.e., no branched hairs), hydathodes, and glabrous sporangia. greenish laminar tissue or overlain by dark sclerenchyma ab- The Neotropical species of Micropolypodium (= Moranopteris) axially and adaxially; segments ascending to patent, alternate share most of those features with the Paleotropical taxa except to opposite, with an acroscopic hump (segments gibbous) or that they have branched hairs. not, especially in fertile segments, entire, oblong or rounded,
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rarely linear and pinnatisect or pinnatifid (M. achilleifolia), such as in Micropolypodium okuboi (Fig. 3B). We observed this slightly decurrent at base or not, margins plane or slightly revo- ring of cells at the bases of setae in many species of Moranop- lute, sometimes hyaline marginally, basiscopic side not folded teris, but it is inconspicuous in some plants, and it is a difficult over sorus; veins simple or furcate, rarely pinnate, inconspicu- character to use to quickly identify members of the genus. ous, obscured by the laminar tissue or by dark sclerenchyma Hairs are often 1–4-branched, and sometimes there are un- at the bases of segments, hydathodes present, mostly 1 or 2 branched hairs and branched hairs occurring on the same plant (rarely > 2) per segment or pinna, visible adaxially, elliptic, (Fig. 2L–P). The branched hairs can have 1 (Fig. 2P) or some- round, or oblong; setae dark red-brown, present on both sur- times 2 setiform branches. Some species (e.g., Moranopteris faces of the stipes, rachises, and/or costae, also sometimes blepharidea and M. killipii) can be recognized by 1-branched on laminar tissue, rarely absent, ring of cells at base of setae hairs that typically have a longer branch, at least twice as long conspicuous to inconspicuous; hairs present on the stipes, ra- as the main branch (Fig. 2M). chises, and/or costae, also on laminar tissue (mainly near costae Spores of Moranopteris appear to be only slightly differ- abaxially), hyaline, slightly red-brown, mostly branched, or ent from those of Micropolypodium. Tryon & Lugardon (1990) unbranched and branched. Sori superficial, usually at base of described the spores of Grammitis knowltoniorum (= Moranop- the costae/costules or on the acroscopic veinlet, mostly 1 (rarely teris knowltoniorum) as being tuberculate. Perispores of Mo- > 2) per segment or pinna, rounded or elliptic, exindusiate; soral ranopteris basiattenuata also display tuberculate surfaces with paraphyses absent; sporangia glabrous; spores tetrahedral- spherical globules (Fig. 3C, D), whereas they are papillate with globose, papillate to tuberculate with small globules; x = 37 dense globules in Micropolypodium okuboi (Fig. 3E, F), and (Smith, 1992). the surface is depressed with only low papillae in spores of Distribution. – Moranopteris occurs in the Neotropics, with Micropolypodium sikkimense (Fig. 3G, H). 28 known species and one hybrid. It occurs in Mexico, Central Etymology. – The genus is named in honor of Dr. America, Antilles, Andes, southern Venezuela, Guyanas, and Robbin C. Moran, fern specialist and Curator of ferns and ly- Brazil. Andes and Central America are centers of diversity of cophytes at The New York Botanical Garden (NY). the genus, with 14 and 12 species, respectively. In these centers, five species are endemic to the Andes (Moranopteris aphelol- New combinations epis, M. blepharidea, M. killipii, M. simplex, M. williamsii), and one species to Central America (M. zurquina). Three species 1. Moranopteris achilleifolia (Kaulf.) R.Y. Hirai & J. Prado, and one hybrid are endemic to Brazil (M. gradata, M. per- comb. nov. ≡ Polypodium achilleifolium Kaulf., Enum. pusilla, M. setosa, M. ×bradei) and two species are endemic Filic.: 116. 1824 ≡ Ctenopteris achilleifolia (Kaulf.) J. Sm., to the Caribbean region (M. knowltoniorum, M. sherringii). Hist. Fil.: 185. 1875 ≡ Grammitis achilleifolia (Kaulf.) Moranopteris nimbata, primarily a Caribbean species, was also R.M. Tryon & A.F. Tryon in Rhodora 84: 128. 1982 ≡ Terp- reported by Farrar (1967) for North Carolina. It is the unique sichore achilleifolia (Kaulf.) A.R. Sm. in Novon 3: 486. record for Moranopteris outside of the Neotropics. 1993 ≡ Micropolypodium achilleifolium (Kaulf.) Labiak Distinctive morphological characters. – Moranopteris dif- & F.B. Matos in Brittonia 59: 184. 2007. – Distribution: fers from Micropolypodium s.str. in having slightly catenate Coastal Brazil and probably also in Argentina (Missiones). unbranched and branched hairs intermixed together on the same fronds (Fig. 2L–P) vs. only catenate unbranched hairs 2. Moranopteris aphelolepis (C.V. Morton) R.Y. Hirai & (similar to Fig. 2L). J. Prado, comb. nov. ≡ Grammitis aphelolepis C.V. Mor- The rhizome scales are nonclathrate and the cells of the ton in Contr. U.S. Natl. Herb. 38: 97. 1967 ≡ Xiphopteris scale body are often turgid and shining. The margins of rhi- aphelolepis (C.V. Morton) Pic.Serm. in Webbia 28: 472. zome scales are mostly entire, or with small lateral projections, 1973 ≡ Micropolypodium aphelolepis (C.V. Morton) or with setiform or glanduliform projections (Fig. 2G–K). A.R. Sm. in Novon 2: 422. 1992. – Distribution: Colombia, Blade segments sometimes are gibbous, mainly on fertile Ecuador, and Bolivia. segments (Fig. 2F). The number of hydathodes and veins is 1 or 2 (Fig. 2E, F), or sometimes more than two per segment 3. Moranopteris basiattenuata (Jenman) R.Y. Hirai & J. Prado, (Moranopteris achilleifolia; M. gradata, Fig. 2C; M. longise- comb. nov. ≡ Polypodium basiattenuatum Jenman in Bull. tosa, Fig. 2D). Bot. Dept. Jamaica, n.s., 4: 114. 1897 ≡ Xiphopteris basiat- Setae are commonly present on the stipes, rachises, cos- tenuata (Jenman) Copel. in Amer. Fern J. 42: 104. 1952 ≡ tae, and laminar tissue, but are absent in Moranopteris grise- Grammitis basiattenuata (Jenman) Proctor in Bull. Inst. Ja- bachii and M. perpusilla. As noted by Smith (1992), setae in maica, Sci. Ser. 5: 32. 1953 ≡ Micropolypodium basiattenu- the Neotropical species of Micropolypodium look different atum (Jenman) A.R. Sm. in Novon 2: 422. 1992 – Lecto from those of many other grammitid ferns. He described the type first step (Proctor, 1985: 575: “Jenman s.n. (NY)”) setae as bearing a ring of cells at their bases. These cells are and second step (here designated): Jamaica, without exact different from the adjacent surrounding epidermal cells, as in locality, s.d., G.S. Jenman s.n. (NY-127117!); isolectotype: Moranopteris basiattenuata (Fig. 3A) and in several other spe- NY s.n.! – Distribution: Mexico, Guatemala, Honduras, cies examined. Moreover, Smith (pers. comm.) observed that El Salvador, Costa Rica, Jamaica, Dominican Republic, Micropolypodium s.str. species do not have this ring of cells, Guyana, Venezuela, Colombia, and Ecuador.
1128 TAXON 60 (4) • August 2011: 1123–1137 Hirai & al. • New Neotropical fern genus Moranopteris
Fig. 2. Morphology of some species of Moranopteris. A–D, Venation patterns (cleared leaf): A, simple veins, M. cookii (Sundue & al. 1764, NY); B, furcate veins, M. aphelolepis (Boeke & Jaramillo 2701, NY); C, pinnate veins, M. gradata (Hirai & al. 564, SP); D, pinnate veins, M. longiseto- sa (Rojas 3209, NY); E–F, segments: E, not gibbous segments (arrow indicates adaxial hydathode), M. cookii (Sundue & al. 1764, NY); F, gibbous segments at circle (arrows indicate adaxial hydathodes), M. liesneri (Cowan & Wurdack 31415, NY); G–K, rhizome scale types: G, entire margins, M. cookii (Sundue & al. 1764, NY); H, margins with small lateral projections, M. basiattenuata (Breedlove & Thorne 30160, NY); I, margins with glanduliform projections, M. longisetosa (Rojas 3209, NY); J, margins with short setiform projections, M. killipii (Lehmann 7655, K); K, margins with setiform projections, M. microlepis (Rojas 3603, NY); L–P, some hair types (re-hydrated hairs): L, unbranched hairs, M. liesneri (Cowan & Wurdack 31415, NY); M, 1-branched, M. blepharidea (Kessler & al. 11973, UPCB); N, 2-branched, M. longisetosa (Rojas 3209, NY); O, 4-branched, M. setosa (Hirai & al. 598, SP); P, 1-branched with one setiform branch, M. taenifolia (Granville 3557, CAY).
1129 Hirai & al. • New Neotropical fern genus Moranopteris TAXON 60 (4) • August 2011: 1123–1137
Fig. 3. A, Base of a seta showing a ring of cells in Moranopteris basiattenuata (Maxon 9858, NY); B, base of a seta without a ring of cells in Micropolypodium okuboi (Togashi s.n., UC); C–D, spores of M. basiattenuata (Breedlove & Thorne 30160, NY): C, proximal face with spherical globules; D, detail of tuberculate surface; E–F, spores of M. okuboi (Togashi s.n., UC): E, proximal face depressed and densely globulose; F, detail of globules on a irregular surface; G–H, spores of Micropolypodium sikkimense (Miehe 93-32, UC): G, proximal face; H, detail of low pappilae on the surface. A–C, E, G: scale bars = 10 μm; D, F, H: scale bars = 2 μm.
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4. Moranopteris blepharidea (Copel.) R.Y. Hirai & J. Prado, (Maxon) Copel. in Amer. Fern J. 42: 107. 1952 ≡ Gram- comb. nov. ≡ Polypodium blepharideum Copel. in Univ. mitis hyalina (Maxon) F. Seym. in Phytologia 31: 174. Calif. Publ. Bot. 19: 304. pl. 64. 1941 ≡ Xiphopteris blepha- 1975 ≡ Micropolypodium hyalinum (Maxon) A.R. Sm. in ridea (Copel.) Copel. in Amer. Fern J. 42: 99. 1952 ≡ Micro- Novon 2: 422. 1992. – Distribution: Costa Rica, Colombia, polypodium blepharideum (Copel.) A.R. Sm. in Novon Ecuador, and Peru. 2: 422. 1992 ≡ Grammitis blepharidea (Copel.) Stolze in Fieldiana, Bot., n.s., 32: 112. 1993. – Distribution: Colom- 10. Moranopteris killipii (Copel.) R.Y. Hirai & J. Prado, comb. bia, Peru, and Bolivia. nov. ≡ Xiphopteris killipii Copel. in Amer. Fern J. 42: 105, t. 10. 1952 ≡ Grammitis killipii (Copel.) Lellinger in Amer. 5. Moranopteris caucana (Hieron.) R.Y. Hirai & J. Prado, Fern J. 74: 58. 1984. – Distribution: Endemic to Andes comb. nov. ≡ Polypodium caucanum Hieron. in Bot. from Colombia and Ecuador. Jahrb. Syst. 34: 503. 1904 ≡ Xiphopteris caucana (Hieron.) Copel. in Amer. Fern J. 42: 98. 1952 ≡ Grammitis caucana 11. Moranopteris knowltoniorum ( Hodge) R.Y. Hi rai & J. Prado, (Hieron.) C.V. Morton in Contr. U.S. Natl. Herb. 38: 96. comb. nov. ≡ Polypodium knowltoniorum Hodge in Amer. 1967 ≡ Micropolypodium caucanum (Hieron.) A.R. Sm. Fern J. 31: 105, p. 1, f. 4–6. 1941 ≡ Xiphopteris knowlto- in Novon 2: 422. 1992. – Distribution: Nicaragua, Costa niorum (Hodge) Copel. in Amer. Fern J. 42: 108. 1952 ≡ Rica, Panama, Guyana, Venezuela, Colombia, Ecuador, Grammitis knowltoniorum (Hodge) Proctor in Rhodora Peru, Bolivia, and Brazil. 63: 35. 1961 ≡ Micropolypodium knowltoniorum (Hodge) A.R. Sm. in Novon 2: 422. 1992. – Distribution: Endemic 6. Moranopteris cookii (Underw. & Maxon) R.Y. Hirai & to the Lesser Antilles. J. Prado, comb. nov. ≡ Polypodium cookii Underw. & Maxon in Contr. U.S. Natl. Herb. 17: 408. 1914 ≡ Xiphop- 12. Moranopteris liesneri (A.R. Sm.) R.Y. Hirai & J. Prado, teris cookii (Underw. & Maxon) Copel. in Amer. Fern J. 42: comb. nov. ≡ Grammitis liesneri A.R. Sm. in Ann. Mis- 98. 1952 ≡ Grammitis cookii (Underw. & Maxon) F. Seym. souri Bot. Gard. 77: 257. 1990 ≡ Micropolypodium liesneri in Phytologia 31: 173. 1975 ≡ Micropolypodium cookii (A.R. Sm.) A.R. Sm. in Novon 2: 422. 1992. – Distribution: (Underw. & Maxon) A.R. Sm. in Novon 2: 422. 1992. – Endemic to Venezuela. Distribution: Guatemala, Costa Rica, Panama, and Ec- uador. 13. Moranopteris longisetosa (Hook.) R.Y. Hirai & J. Prado, comb. nov. ≡ Polypodium longisetosum Hook., Sp. Fil. 7. Moranopteris gradata (Baker) R.Y. Hirai & J. Prado, 4: 225, t. 278 A. 1864 ≡ Terpsichore longisetosa (Hook.) comb. nov. ≡ Polypodium gradatum Baker in Martius, A.R. Sm. in Novon 3: 487. 1993. – Distribution: Costa Fl. Bras. 1(2): 513. 1870 ≡ Polypodium hirsutulum Fée, Rica, Venezuela, Colombia, Ecuador, Peru, and Bolivia. Crypt. Vasc. Brésil 1: 87. 1869, nom. illeg. (ICBN Art. 53.1), non G. Forst. (1786) ≡ Ctenopteris gradata (Baker) 14. Moranopteris microlepis (Rosenst.) R.Y. Hirai & J. Prado, Copel. in Philipp. J. Sci. 84: 437. 1955 ≡ Grammitis gradata comb. et stat. nov. ≡ Polypodium blepharodes Maxon var. (Baker) R.M. Tryon & A.F. Tryon in Rhodora 84: 128. microlepis Rosenst. in Repert. Spec. Nov. Regni Veg. 22: 1982 ≡ Terpsichore gradata (Baker) A.R. Sm. in Novon 3: 14. 1925. – Distribution: Costa Rica, Panama, Jamaica, 486. 1993 ≡ Micropolypodium gradatum (Baker) Labiak and Guadeloupe. & F.B. Matos in Brittonia 59: 184. 2007. – Distribution: Endemic to Coastal Brazil. 15. Moranopteris nana (Fée) R.Y. Hirai & J. Prado, comb. nov. ≡ Polypodium nanum Fée, Mém Foug. 5, Gen. Filic.: 238. 8. Moranopteris grisebachii (Underw. ex C. Chr.) R.Y. Hirai & 1852 ≡ Xiphopteris nana (Fée) Copel. in Amer. Fern J. 42: J. Prado, comb. nov. ≡ Polypodium grisebachii Underw. 107. 1952 ≡ Micropolypodium nanum (Fée) A.R. Sm. in ex C. Chr., Index Filic.: 531. 1906, based on P. exiguum Novon 2: 422. 1992. – Distribution: Costa Rica, Panama, Griseb., non Heward (1838) ≡ Polypodium exiguum Trinidad and Tobago (restricted to the island of Trinidad), Griseb., Fl. Br. W. Ind.: 701. 1864, nom. illeg. (ICBN Art. French Guiana, Suriname, Guyana, Venezuela, Colombia, 53.1), non Heward (1838) ≡ Xiphopteris grisebachii (Un- Peru, and Brazil. derw. ex C. Chr.) Copel. in Amer. Fern J. 42: 95. 1952 ≡ Grammitis grisebachii (Underw. ex C. Chr.) Proctor in 16. Moranopteris nimbata (Jenman) R.Y. Hirai & J. Prado, Bull. Inst. Jamaica, Sci. Ser. 5: 33, t. 2(7–8). 1953 ≡ Mi- comb. nov. ≡ Polypodium nimbatum Jenman in J. Bot. cropolypodium grisebachii (Underw. ex C. Chr.) A.R. Sm. 24: 271. 1886 ≡ Xiphopteris nimbata (Jenman) Copel. in in Novon 2: 422. 1992. – Distribution: Endemic to the Amer. Fern J. 42: 108. 1952 ≡ Grammitis nimbata (Jenman) Greater Antilles and the Lesser Antilles. Proctor in Bull. Inst. Jamaica, Sci. Ser. 5: 34. 1953 ≡ Micro- polypodium nimbatum (Jenman) A.R. Sm. in Novon 2: 422. 9. Moranopteris hyalina (Maxon) R.Y. Hirai & J. Prado, 1992. – Distribution: U.S.A. (North Carolina; Farrar, 1967) comb. nov. ≡ Polypodium hyalinum Maxon in Contr. and the Greater Antilles. U.S. Natl. Herb. 17: 406. 1914 ≡ Xiphopteris hyalina
1131 Hirai & al. • New Neotropical fern genus Moranopteris TAXON 60 (4) • August 2011: 1123–1137
17. Moranopteris perpusilla (Maxon) R.Y. Hirai & J. Prado, 1788 ≡ Grammitis trichomanoides (Sw.) Ching in Bull. Fan comb. nov. ≡ Polypodium perpusillum Maxon in Contr. Mem. Inst. Biol. 10: 16. 1940 ≡ Xiphopteris trichomanoi- U.S. Natl. Herb. 17: 409, pl. 13-A. 1913 ≡ Xiphopteris per- des (Sw.) Copel., Gen. Fil.: 215. 1947 ≡ Micropolypodium pusilla (Maxon) Copel. in Amer. Fern J. 42: 95. 1952 ≡ Mi- trichomanoides (Sw.) A.R. Sm. in Novon 2: 423. 1992. cropolypodium perpusillum (Maxon) A.R. Sm. in Novon – Distribution: Mexico, Guatemala, Honduras, Cuba, Ja- 2: 422. 1992. – Distribution: Endemic to Southeast Brazil. maica, Haiti, and Dominican Republic.
18. Moranopteris plicata (A.R. Sm.) R.Y. Hirai & J. Prado, 24. Moranopteris truncicola (Klotzsch) R.Y. Hirai & J. Prado, comb. nov. ≡ Grammitis plicata A.R. Sm. in Ann. Mis- comb. nov. ≡ Polypodium truncicola Klotzsch var. major souri Bot. Gard. 77: 258. 1990 ≡ Micropolypodium plica- Klotzsch in Linnaea 20: 374. 1847 ≡ Xiphopteris trunci- tum (A.R. Sm.) A.R. Sm. in Novon 2: 422. 1992. – Distri- cola (Klotzsch) Copel. in Amer. Fern J. 42: 101. 1952 ≡ bution: Costa Rica, Venezuela, Colombia, Ecuador, Peru, Grammitis truncicola (Klotzsch) C.V. Morton in Contr. and Brazil. U.S. Natl. Herb. 38: 98. 1967 ≡ Micropolypodium truncic- ola (Klotzsch) A.R. Sm. in Novon 2: 423. 1992. – Distribu- 19. Moranopteris serricula (Fée) R.Y. Hirai & J. Prado, comb. tion: Costa Rica, Guyana, Venezuela, Colombia, Ecuador, nov. ≡ Polypodium serricula Fée, Mém. Foug. 5, Gen. Peru, Bolivia, and Brazil. Filic.: 238. 1852 ≡ Xiphopteris serricula (Fée) Copel. in Amer. Fern J. 42: 101. 1952 ≡ Grammitis serricula (Fée) 25. Moranopteris williamsii (Maxon) R.Y. Hirai & J. Prado, Proctor in Rhodora 63: 35. 1961 ≡ Micropolypodium ser- comb. nov. ≡ Polypodium williamsii Maxon in Contr. ricula (Fée) A.R. Sm. in Novon 2: 422. 1992. – Distribu- U.S. Natl. Herb. 17: 547, t. 34. 1916 ≡ Xiphopteris williamsii tion: Dominica, Guadeloupe, Martinique, Trinidad and To- (Maxon) Copel. in Amer. Fern J. 42: 101. 1952 ≡ Grammitis bago (restricted to the island of Trinidad), and Venezuela. williamsii (Maxon) Lellinger in Amer. Fern J. 74: 59. 1984 ≡ Micropolypodium williamsii (Maxon) A.R. Sm. in Novon 20. Moranopteris setosa (Kaulf.) R.Y. Hirai & J. Prado, comb. 2: 423. 1992. – Distribution: Endemic to Bolivia. nov. ≡ Xiphopteris setosa Kaulf., Enum. Filic.: 275. 1824 ≡ Grammitis setosa (Kaulf.) C. Presl, Tent. Pterid.: 208. 26. Moranopteris zurquina (Copel.) R.Y. Hirai & J. Prado, 1836, nom. illeg. (ICBN Art. 53.1), non Blume (1828) ≡ comb. nov. ≡ Xiphopteris zurquina Copel. in Amer. Fern J. Polypodium micropteris C. Chr., Index Filic.: 545. 1906, 42: 99. 1952 ≡ Grammitis zurquina (Copel.) F. Seym. in nom. nov. for X. setosa Kaulf. ≡ Grammitis micropteris Phytologia 31: 175. 1975 ≡ Micropolypodium zurquinum (C. Chr.) Brade in Sellowia 18: 81. 1966 ≡ Micropolypo- (Copel.) A.R. Sm. in Novon 2: 423. 1992. – Distribution: dium setosum (Kaulf.) A.R. Sm. in Novon 2: 422. 1992. Endemic to Costa Rica. – Distribution: Endemic to Coastal Brazil. 27. Moranopteris ×bradei (Labiak & F.B. Matos) R.Y. Hirai 21. Moranopteris sherringii (Baker) R.Y. Hirai & J. Prado, & J. Prado, comb. nov. ≡ Micropolypodium ×bradei Labiak comb. nov. ≡ Polypodium sherringii Baker in J. Bot. 20: & F.B. Matos in Brittonia 59: 182. 2007. – Distribution: 26. 1882 ≡ Xiphopteris sherringii (Baker) Copel. in Amer. Known only from Rio de Janeiro State, southeastern Brazil. Fern J. 42: 104. 1952 ≡ Grammitis sherringii (Baker) Proc- tor in Bull. Inst. Jamaica, Sci. Ser. 5: 35. 1953 ≡ Micropoly- New species podium sherringii (Baker) A.R. Sm. in Novon 2: 423. 1992. – Distribution: Endemic to the Greater Antilles. 1. Moranopteris rupicola R.Y. Hirai & J. Prado, sp. nov. – Type: Guyana. Mazaruni-Potaro, Roraima, summit, La 22. Moranopteris taenifolia (Jenman) R.Y. Hirai & J. Prado, Proa Camp, east of the border, near Lake Gladys, 2800 m, comb. nov. ≡ Polypodium taenifolium Jenman in Bull. Bot. 05°15′36″ N, 60°13′ W, 14 Apr 1988, R.L. Liesner 23289 Dept. Jamaica, n.s., 4: 114. 1897 ≡ Xiphopteris taenifolia (holotype: MO; isotypes: UC, VEN). Figure 4. (Jenman) Copel. in Amer. Fern J. 42: 109. 1952 ≡ Grammi- Diagnosis. – Moranopteris rupicola similis Moranopteridi tis taenifolia (Jenman) Proctor in Bull. Inst. Jamaica, Sci. taenifoliae sed a qua habitu rupiculous et pilis ramosis cum Ser. 5: 35. 1953 ≡ Micropolypodium taenifolium (Jenman) 1 vel 2 ramis (vs. habitu epiphyticus, pilis non-ramosis et pilis A.R. Sm. in Novon 2: 423. 1992. – Distribution: Mexico, ramosis cum 1 vel 2 ramis setaceis) differt. Belize, Guatemala, Honduras, Nicaragua, Costa Rica, Pa- Description. – Plants epipetric. Rhizomes erect with api- nama, Jamaica, Haiti, Dominican Republic, Puerto Rico, cal scales, the scales 2.1–2.7 × 0.3–0.4 mm, yellow-brown, Saint Kitts and Nevis, Guadeloupe, Martinique, Trinidad lanceolate, bases slightly cordate, apices acute, mostly with and Tobago (restricted to the island of Trinidad), French apical or subapical gland-like cells, margins with long seti- Guiana, Suriname, Guyana, Venezuela, Colombia, Ecua- form projections, or with also small lateral projections, rarely dor, Peru, Bolivia, and Brazil. setiform projections occurring on the scale surfaces, setiform projections red-brown, 0.15–0.30 mm long. Leaves erect to 23. Moranopteris trichomanoides (Sw.) R.Y. Hirai & J. Prado, arcuate, determinate, 5.5–13.0 × 0.45–1.00 cm, sparsely setose; comb. nov. ≡ Polypodium trichomanoides Sw., Prodr.: 131. stipes 0.5–1.0 cm long, yellow-brown to dark-brown, narrowly
1132 TAXON 60 (4) • August 2011: 1123–1137 Hirai & al. • New Neotropical fern genus Moranopteris
Fig. 4. Moranopteris rupicola. A, Habit; B, detail of the fertile segments showing sori and setae abaxially; C, detail of the segments showing setae and hydathodes adaxially; D, detail of the venation (cleared leaf); E, rhizome scale; F, detail of the apex of the rhizome scale; G, unbranched and branched hairs from the costa (re-hydrated hairs). A–C, E, F: Liesner 23289 (MO); D, G: Steyermark & al. 115650 (UC).
1133 Hirai & al. • New Neotropical fern genus Moranopteris TAXON 60 (4) • August 2011: 1123–1137
Fig. 5. Moranopteris simplex. A, Habit; B, detail of the fertile segments showing sori and setae abaxially; C, detail of the segments showing setae and hydathodes adaxially; D, detail of the venation (cleared leaf); E, rhizome scale; F, unbranched and branched hairs from the costa (re-hydrated hairs). A–C, E: Mägdefrau 464 (B); D, F: Quijada 4 (VEN).
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winged; laminae linear, pinnatisect, gradually tapering proxi- abaxially; segments slightly ascending, ca. 60°–80° to costae, mally to a narrow wing, chartaceous; costae visible or slightly 18–35 pairs, spaced ca. 1.1–1.7 mm, subopposite, gibbous, visible with dark sclerenchyma abaxially, slightly visible with asymmetric, 2.5–3.8 × 1.1–1.6 mm, oblong to oblong-lanceo- dark sclerenchyma adaxially; segments slightly ascending, late, deltate toward bases, decurrent at base, apices rounded to 60°–80° to costae, 17–36 pairs, spaced (0.4–)0.6–1.8 mm, sub- slightly acute, margins slightly revolute, without hyaline cells; opposite, gibbous, asymmetric, 2.8–4.9 × 1.9–2.9 mm, oblong, veins usually furcate, at least in fertile segments, or sometimes decurrent at bases, apices rounded to slightly acute, margins simple in sterile segments, obscure, (1)2 hydathodes per seg- plane, without hyaline cells, or inconspicuous; veins usually ment, rarely 3 hydathodes, elliptic or obovate, sometimes round; furcate, at least in fertile segments, or sometimes simple in ster- setae 1.1–2.7 mm long, dark red-brown, on both surfaces of the ile segments, obscure, (1)2 hydathodes per segment, obovate or costae and laminar tissue; hairs scattered all along the costae, oblong; setae 1.6–2.4 mm long, dark red-brown, on both sides laminar tissue abaxially, and margins, hyaline to yellowish or of the stipes, costae, and laminar tissue; hairs present on the slightly red-brown, unbranched and branched, the unbranched costae and laminar tissue, rarely on the margins (mainly near hairs 2-celled, 0.05–0.15 mm long, the branched hairs 1- or to costae abaxially), hyaline or slightly red-brown, branched or 2-branched, mostly 1-branched, the main branch 2- or 3-celled, rarely unbranched, the branched hairs mostly 1- or 2-branched, (<)0.1(–0.2) mm long, 1st branch 1- or 2-celled, 0.10–0.15 mm the main branch 2- or 3-celled, 0.15–0.25 mm long, 1st branch long, 2nd branch, if present, 1-celled, (<)0.1 mm long. Sori one 1- or 2-celled, or sometimes 2-celled in the same insertion per segment, round or nearly so, 1.4–1.8 mm diam. point, (<)0.10–0.15 mm long, 2nd branch, if present, 1-celled, Additional specimens examined. – Venezuela. Ara- < 0.1 mm long, the unbranched portion, 1-celled, < 0.1 mm long. gua, Colonia Tovar, s.d., Moritz s.n. p.p. (P-637667, P-696244); Sori one per segment, rounded, 1.5–1.8 mm diam. Distrito Federal, Caracas, Monte Grappa, 18 Aug 1985, Quijada Additional specimens examined. – Venezuela. Bolívar, 4 (VEN); El Junquito, 1925 m, 26 Mar 1943, Killip & Rohl Cumbre del Ptari-tepuí, al norte de la Misión de Santa Teresita 37170 (US). de Kavanayén, 2360–2420 m, 05°45′ N, 61°45′ W, 23 Feb 1978, Distribution. – Endemic to Venezuela; 1600–1925 m. Steyermark & al. 115650 (GH, UC, VEN). Discussion. – Moranopteris simplex is easily distinguished Distribution. – Guyana and Venezuela, to be expected in by hairs that are mostly yellowish, unbranched and 1-branched, northern Brazil; 2360–2800 m. scattered all along on the laminar tissue abaxially (Fig. 5). Discussion. – Moranopteris rupicola has rhizome scales The most similar species is Moranopteris trichomanoides, with red-brown, long, setiform projections on the margins, which occurs in the Greater Antilles and Central America. That sparsely setose leaves, gibbous segments, furcate veins, usu- differs by having mostly 2–4-branched hairs, near and on the ally two hydathodes per segment, and mostly branched hairs costae abaxially, unbranched hairs absent. mainly near and on the costae (Fig. 4). Moranopteris rupicola Etymology – The specific epithet refers to the hairs which resembles M. taenifolia by the habit and by the position of are less branched when compared to those of the most similar the hairs mostly occurring near and on the costae abaxially. species (Moranopteris trichomanoides). However, M. taenifolia differs in having unbranched hairs and branched hairs with a setiform branch. Etymology. – The specific epithet refers to the rocky habi- ACKNOWLEDGMENTS tat of the species in the Venezuelan tepuis. This study was largely funded by a grant to the first author from 2. Moranopteris simplex R.Y. Hirai & J. Prado, sp. nov. – Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Type: Venezuela. Aragua: Maracay, Choroní-Passes, grant no. 06/06215-5). We thank The New York Botanical Garden 1600 m, 28 Feb 1958, K. Mägdefrau 464 (holotype: for providing herbarium and other facilities during the visit of the B-200077185). Figure 5. first author, Judith Garrison Hanks, and Luciana Benjamim Bena- Diagnosis. – Species quam maxime affinis Moranopteridi tti for SEM images (setae and spores, respectively), and Alejandra trichomanoidea, sed plerumque pilis non-ramosis et pilis furca- Vasco, Luz A. Triana-Moreno, Michael Kessler, Marcus Lehnert, and tis sparsis in lamina abaxialiter (vs. pilis ramosis cum 2–4-ra- Michael Sundue for providing us with silica-dried material. Finally, mis, approximatis et in costa abaxialiter) differt. we are especially grateful to Dr. Robbin Moran, whose support was Description. – Plants epiphytic. Rhizomes erect with api- fundamental to the development of this study (grant from the United cal scales, the scales 2.0–2.2 × 0.20–0.25 mm, yellow-brown, States National Science Foundation, DEB 0717056). We also thank lanceolate to linear-lanceolate, bases slightly cordate, apices the two anonymous reviewers for their comments on the manuscript. acute, with apical or subapical gland-like cells, margins en- tire or with small lateral projections, simple or furcate. Leaves erect to arcuate, determinate, 3.5–7.6 × 0.50–0.75 cm, moder- LITERATURE CITED ately setose; stipes almost absent, brown to dark-brown, nar- rowly winged; laminae linear, pinnatisect, sometimes deeply Akaike, H. 1973. Information theory as an extension of the maximum pinnatifid, gradually tapering proximally to a narrow wing, likelihood principle. Pp. 267–281 in: Petrov, B.N. & Csaki, F. (eds.), chartaceous; costae obscured by laminar tissue abaxially and Second International Symposium on Information Theory. Buda- adaxially, sometimes slightly visible with dark sclerenchyma pest: Akademiai Kiado.
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Appendix. Species, vouchers (collector, collector number, and herbarium), locality, and GenBank accession numbers of the DNA sequences used in this paper (rbcL, atpB, trnL-F). Missing data: –. Asterisks indicate newly obtained sequences. Adenophorus tripinnatifidus Gaudich., Ranker 1102 (COLO), Hawaiian Islands, U.S.A., AF468207, AF469783, AF469796; Ascogrammitis pichinchae (Sodiro) Sundue, Dassler 94-7-13-1 (ILLS), Colombia, AY460675, AY459508, GU476711; Calymmodon gracilis (Fée) Copel., Chiou 97-09-12-01 (COLO, TAIF, UC), Taiwan, AY362341, AY459451, GU476618; Ceradenia spixiana (Mart. ex Mett.) L.E. Bishop, Salino 3008 (UC), Brazil, AY460623, AY459457, –; Chrysogram- mitis glandulosa (J. Sm.) Parris, Ranker 2195 (BORH, SAN, SNP, COLO), Malaysia, JF514014*, JF514082*, JF514048*; Chrysogrammitis musgraviana (Baker) Parris, Kessler 12570 (UC), Sabah, Malaysia, AY460624, AY459458, GU476630; Cochlidium serrulatum (Sw.) L.E. Bishop, Hirai & Schwartsburd 541 (SP), Brazil, JF514010*, JF514078*, JF514044*; Cochlidium punctatum (Raddi) L.E. Bishop, Silva 3914 (UC), Brazil, JF513987*, JF514057*, GU476631; Ctenopterella denticulata (Blume) Parris, Ranker 2113 (BORH, SAN, SNP, COLO), Malaysia, JF514013*, JF514081*, JF514047*; Ctenopteris heterophylla (Labill.) Tindale, Parris 12419 (AK), New Zealand, AY460629, AY459462, –; Ctenopteris lasiostipes (Mett.) Brownlie, Hodel 1448 (UC), New Caledonia, AY460630, AY459463, –; Dasygrammitis crassifrons (Baker) Parris, Game 95-80 (UC), Fiji, JF513992*, JF514062*, JF514026*; Enterosora percrassa (Baker) L.E. Bishop, Moraga
1136 TAXON 60 (4) • August 2011: 1123–1137 Hirai & al. • New Neotropical fern genus Moranopteris
Appendix. Continued. & Rojas 508 (UC), Costa Rica, AY460635, AY459468, GU476636; Grammitis billardierei Willd., Parris 12421 (AK), New Zealand, AY460637, AY459469, JF514042*; Grammitis bryophila (Maxon) F. Seym., Rojas & al. 3240 (UC), Costa Rica, AF468208, AF469784, AF469797; Grammitis deplanchei (Baker) Copel., Hodel 1450 (UC), New Caledonia, AY460639, AY459471, –; Grammitis poeppigiana (Mett.) Pic.Serm., Weber 13772 (COLO), Australia, AY460647, Taylor 6072 (UC), Chile, AY459479, –; Grammitis tenella Kaulf., Ranker 1352 (COLO); Hawaiian Islands, U.S.A., AF468198, AF469773, AF469786; Lellin- geria apiculata (Kunze ex Klotzsch) A.R. Sm. & R.C. Moran, Salino 3009 (UC), Brazil, AY362343, AY459480, GU476642; Lellingeria limula (Christ) A.R. Sm. & R.C. Moran, Sundue 1736 (INB, NY, UC, UPCB), Costa Rica, GU476903, GU476765, GU476651; Leucotrichum schenckii (Hieron.) Labiak, Salino 4547 = 4538 (UC, BHCB), Brazil, AY460651, AY459483, GU476657; Melpomene flabelliformis (Poir.) A.R. Sm. & R.C. Moran, Sanchez 183 (UC), Colombia, AY460656, AY459488, –; Melpomene moniliformis (Lag. ex Sw.) A.R. Sm. & R.C. Moran, Moraga & Rojas 446 (INB), Costa Rica, AY460654, AY459486, GU476664; Microgramma bifrons (Hook.) Lellinger, Neill & al. 8309 (UC), Ecuador, AY362582, van der Werff 18062 (UC), Peru, EF463499, DQ642224; Microgramma percussa (Cav.) de la Sota, Smith 1357 (UC), Venezuela, AY362574, AY459516, GU476669; Micropolypodium okuboi (Yatabe) Hayata, Par- ris 12154 (AK), Japan, JF513994*, JF514064*, JF514028*; Kanebira & Sasaki 21672 (UC), Formosa, JF513998*, –, –; Wilson 2387 (UC), Japan, JF514018*, JF514086*, JF514053*; Micropolypodium sikkimense (Hieron.) X.C. Zhang, Miehe 00-093-32 (UC), Bhutan, JF513999*, JF514068*, JF514032*; Xian & al. s.n. (UC), China, JF514019*, JF514087*, JF514054*; Moranopteris achilleifolia (Kaulf.) R.Y. Hirai & J. Prado, Cordeiro & Ribas 1398 (MBM, UC), Brazil, AY460666, AY459499, –; Moranopteris aphelolepis (C.V. Morton) R.Y. Hirai & J. Prado, Borke & Jaramillo 2701 (NY), Ecuador, –, –, JF514021*; Jiménez & Vidarre 557 (UC), Bolivia, JF513996*, JF514066*, JF514030*; Moranopteris basiattenuata (Jenman) R.Y. Hirai & J. Prado, Breedlove & Thorne 30160 (NY), Mexico, JF513988*, JF514058*, JF514022*; Moranopteris blepharidea (Copel.) R.Y. Hirai & J. Prado, Jiménez 708 (GOET), Bolivia, JF513995*, JF514065*, JF514029*; Moranopteris caucana (Hieron.) R.Y. Hirai & J. Prado, van der Werff & al. 13445 (UC), Ecuador, JF513991*, JF514061*, JF514024*; Lehnert 182 (GOET), Ecuador, JF514002*, JF514071*, JF514035*; Moranopteris cookii (Underw. & Maxon) R.Y. Hirai & J. Prado, Sundue & al. 1771 (NY), Costa Rica, JF514007*, JF514076*, JF514040*; Moranopteris gradata (Baker) R.Y. Hirai & J. Prado, Hirai & al. 537 (SP), Brazil, JF514009*, JF514077*, JF514043*; Mo- ranopteris grisebachii (Underw. ex C. Chr.) R.Y. Hirai & J. Prado, Maxon 9961 (NY), Jamaica, JF514008*, –, JF514041*; Moranopteris hyalina (Maxon) R.Y. Hirai & J. Prado, Rojas & al. 3210 (CR, INB, MO, UC), Costa Rica, AY362344, AY459490, GU476670; Lehnert 1426 (GOET), Ecuador, JF514001*, JF514070*, JF514034*; Sundue 1148 (NY), Ecuador, JF514006*, JF514075*, JF514039*; Moranopteris longisetosa (Hook.) R.Y. Hirai & J. Prado, Rojas & al. 3209 (CR, INB, MO, UC), Costa Rica, AY460674, AY459507, –; Lehnert 596 (GOET), Bolivia, JF514003*, JF514072*, JF514036*; Moranopteris microlepis (Rosenst.) R.Y. Hirai & J. Prado, Smith 2584 (UC), Costa Rica, JF513986*, JF514056*, JF514020*; Kluge 2003 (UC), Costa Rica, JF513997*, JF514067*, JF514031*; Moranopteris nana (Fée) R.Y. Hirai & J. Prado, Diaz & al. 4747 (NY), Venezuela, JF513990*, –, –; Moranopteris perpusilla (Maxon) R.Y. Hirai & J. Prado, Hirai & al. 574 (SP), Brazil, JF514011*, JF514079*, JF514045*; Moranopteris plicata (A.R. Sm.) R.Y. Hirai & J. Prado, Lehnert 929 (GOET, UC), Ecuador, JF514005*, JF514074*, JF514038*; Moranopteris serricula (Fée) R.Y. Hirai & J. Prado, Feldmann s.n. (P), Guadeloupe, –, –, JF514025*; Wilbur & al. 8084 (NY), Dominica, JF514017*, JF514085*, JF514052*; Moranopteris setosa (Kaulf.) R.Y. Hirai & J. Prado, Hirai & al. 599 (SP), Brazil, JF514012*, JF514080*, JF514046*; Moranopteris taenifolia (Jenman) R.Y. Hirai & J. Prado, Rothfels 08-116 (DUKE), Costa Rica, –, JF514060*, JF514023*; Triana-Moreno s.n. (SP), Costa Rica, JF514015*, JF514083*, JF514050*; Moranopteris trichomanoides (Sw.) R.Y. Hirai & J. Prado, Gomez 114 (NY), Honduras, JF513993*, JF514063*, JF514027*; Zanoni & al. 45973 (NY), Dominica, –, –, JF514055*; Moranopteris truncicola (Klotzsch) R.Y. Hirai & J. Prado, Lehnert 862 (GOET), Ecuador, JF514004*, JF514073*, JF514037*; Vasco & Sundue 626 (NY), Colombia, JF514016*, JF514084*, JF514051*; Moranopteris williamsii (Maxon) R.Y. Hirai & J. Prado, Kessler & al. 7173 (UC), Bolivia, JF514000*, JF514069*, JF514033*; Moranopteris zurquina (Copel.) R.Y. Hirai & J. Prado, Rojas & Mata 3021 (UC), Costa Rica, AY460659, AY459492, –; Oreogrammitis hookeri (Brack.) Parris, Ranker 1116 (COLO), Hawaiian Islands, U.S.A., AY460642, AY459473, EF178655; Pecluma eurybasis (C. Chr.) M.G. Price, Danton s.n. (GOET), Bolivia, EF463255, EF463504, Kessler s.n. (GOET), Bolivia, FJ825691; Polypodium vulgare L., Schneider s.n. (GOET), Germany, EF551065, EF463510, EF551119; Prosaptia contigua (G. Forst.) C. Presl, Chiou 97-09-12-05 (TAIF, COLO, UC), Taiwan, AY362345, AY459494, EF178663; Prosaptia nutans (Blume) Mett., Ranker & Trapp 1765 (COLO, UC), Papua New Guinea, AY460631, AY459464, –; Radiogrammitis parva (Brause) Parris, Ranker 1763a (COLO, UC), Papua New Guinea, AY460644, AY459476, –; Scleroglossum sulcatum (Kuhn) Al- derw., Bowden-Kerby in Raulerson 24182b (GUAM, UC), Pohnpei, AY460665, AY459498, JF514049*; Serpocaulon triseriale (Sw.) A.R. Sm., Jiménez 1994 (UC), Bolivia, DQ151926, EF463516, DQ151980; Terpsichore asplenifolia (L.) A.R. Sm., Moraga & Rojas 506 (INB), Costa Rica, JF513989*, JF514059*, –; Terpsichore cultrata (Willd.) A.R. Sm., Dassler 94-7-19-1 (ILLS), Colombia, AY460669, AY459502, –; Terpsichore lanigera (Desv.) A.R. Sm., Léon 3647 (USM, UC), Peru, AY460672, AY459505, GU476718; Terpsichore lehmanniana (Hieron.) A.R. Sm., Wilson 2589 (UC), Ecuador, AY460673, AY459506, –; Themelium conjunctisorum (Baker) Parris, Ranker & Trapp 1758 (COLO, UC), Papua New Guinea, AY460680, AY459514, –; Tomophyllum repandulum (Mett.) Parris, Ranker & Trapp 1767 (COLO, UC), Papua New Guinea, AY460633, AY459466, –.
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