Infrageneric Revision of the Fern Genus Deparia (Athyriaceae, Aspleniineae, Polypodiales)

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Systematic Botany (2018), 43(3): pp. 645–655 © Copyright 2018 by the American Society of Plant Taxonomists DOI 10.1600/036364418X697364 Date of publication August 10, 2018 Infrageneric Revision of the Fern Genus Deparia (Athyriaceae, Aspleniineae, Polypodiales)

Li-Yaung Kuo,1,7 Atsushi Ebihara,2 Tian-Chuan Hsu,3 Germinal Rouhan,4 Yao-Moan Huang,5 Chun-Neng Wang,1,6,8 Wen-Liang Chiou,3 and Masahiro Kato2 1Institute of Ecology and Evolutionary Biology, National Taiwan University, Taipei 10617, Taiwan 2Department of Botany, National Museum of Nature and Science, Amakubo 4-1-1, Tsukuba, Ibaraki 305-0005, Japan 3Botanical Garden Division, Taiwan Forestry Research Institute, Taipei 10066, Taiwan 4Muséum national d’Histoire naturelle, Institut de Systématique, Evolution, Biodiversité ((ISYEB) CNRS, Sorbonne Université EPHE), Herbier national, 16 rue Buffon CP39, F-75005 Paris, France 5Silviculture Division, Taiwan Forestry Research Institute, Taipei 10066, Taiwan 6Department of Life Science, National Taiwan University, Taipei 10617, Taiwan 7Current address: Boyce Thompson Institute, Ithaca, New York 14853, USA ([email protected]) 8Author for correspondence ([email protected])

Communicating Editor: Sven Buerki

Abstract—Current molecular phylogenetic analyses support the monophyly and circumscription of the athyrioid fern genus Deparia (Athyr- iaceae), which includes previously recognized genera including Athyriopsis, 3Depazium, Dictyodroma, Dryoathyrium (5 Parathyrium), Lunathyrium, and Neotriblemma (5 Triblemma Ching), and 3Neotribleparia. This broad generic concept has been adopted in several recent taxonomic treatments, including the Pteridophyte Phylogeny Group I. However, the infrageneric taxonomy of Deparia still needs further revision. In this study, we provide a new infrageneric classification with five sections and three subsections based on the phylogenetic evidence. We recognize two new sections, sect. Dictyodroma and sect. Erectus, and two new subsections, sect. Deparia subsect. Caespites and subsect. Athyriopsis. In addition, we provide a key to the sections and subsections, a table of diagnostic characters, new combinations for three Deparia and one Diplazium species, and a list of species assigned to the sections/subsections. Hybrids derived from crosses between the sections and subsections are also noted.

Keywords—Athyrioids, Dictyodroma, sect. Erectus, taxonomy.

The fern genus Deparia Hook. & Grev. was established in published a replacing genus name, Neotriblemma. Ching (1964) 1829 and based on Deparia macraei Hook. & Grev. [5 Deparia indicated that Athyriopsis is similar to Lunathyrium but dif- prolifera (Kaulf.) Hook. & Grev.; Fig. 1A]. In recent fern clas- ferent in its slender and non-winged stipe bases, absence of sifications and floristic treatments (e.g. Christenhusz et al. pneumatophores, and long-creeping rhizomes (Fig. 2). Dic- 2011; Rothfels et al. 2012b; He et al. 2013; PPG I 2016), Deparia tyodroma was recognized by a unique combination of anas- belongs to Athyriaceae, and encompasses several genera that tomosing venation, winged distal pinnae and entire proximal had long been kept separate: Lunathyrium Koidz., Dry- pinnae, hairlike scales (a kind of indument morphologically oathyrium Ching (5 Parathyrium Holttum), Athyriopsis Ching, transient from multicellular hairs to scales), and discontinuous Dictyodroma Ching, Neotriblemma Nakaike (5 Triblemma grooves between rachises and costae (Fig. 2). Neotriblemma was Ching), 3Depazium Nakaike, and 3Neotribleparia Nakaike. characterized by having diplazioid sori (i.e. paired but non- Lunathyrium was established by Koidzumi (1932) and based on connected sori on both sides of veinlets), long-creeping rhi- Lunathyrium pycnosorum (Christ) Koidz. [[ Athyrium pycno- zomes, and tuberculate perine (Ching 1978). In addition, Wang sorum Christ [ Deparia pycnosora (Christ) M. Kato; Fig. 1C]; it is (1982) established a new section under Athyriopsis, sect. characterized by its pneumatophores and almost asplenioid Caespites, based on Athyriopsis omeiensis Z. R. Wang [[ Deparia sori (i.e. linear and restricted to the acroscopic sides of veinlets; omeiensis (Z. R. Wang) M. Kato], characterized by its erect Fig. 2). Ching (1941) described Dryoathyrium based on Dry- rhizomes. 3Depazium, originally described as a nothogenus oathyrium boryanum (Willd.) Ching [[ Aspidium boryanum resulting from a cross between Deparia and Diplazium Sw., was Willd. [ Deparia boryana (Willd.) M. Kato], which is charac- based on 3Depazium tomitaroanum (Masam.) Nakaike [[ terized by the non-scaly stipe bases, creeping rhizomes, and Deparia 3tomitaroana (Masam.) R. Sano] (Nakaike 1992). One round-reniform (Fig. 2J) to U- and J-shaped sori. Holttum of the parent species of this hybrid is Diplazium subsinuatum, (1958) described the genus Parathyrium, also based on Deparia which is now, however, a synonym of Deparia lancea. Similarly, boryana, emphasizing its swollen stipe bases, presence of 3Neotribleparia was originally published for inter-generic hairlike scales, and discontinuous grooves between rachises hybrids between Neotriblemma and Deparia (Nakaike 2004) and costae (Fig. 2E and 2I). Ching (1964, 1978) recognized three but Neotriblemma is now included under the genus Deparia. additional new genera, Athyriopsis, Dictyodroma, and Tri- Affinities of species treated under the genera Athyriopsis, blemma, based on Athyriopsis japonica (Thunb.) Ching [[ Dryoathyrium, and Lunathyrium were first indicated by Asplenium japonicum Thunb. [ Deparia japonica (Thunb.) M. Tagawa (1959), and they were transferred to Lunathyrium by Kato; Fig. 1D], Dictyodroma heterophlebia (Mett. ex Baker) Kurata (1961). Taking Kurata (1961) and Ching (1964) into Ching [[ Asplenium heterophlebium Mett. ex Baker [ Deparia account, Ohba (1965) further established three sections within heterophlebia (Mett. ex Baker) R. Sano; Fig. 1G], and Triblemma Lunathyrium s. l.: sect. Lunathyrium, sect. Dryoathyrium, and lancea (Thunb.) Ching [[ Asplenium lanceum Thunb. [ Deparia sect. Athyriopsis. The morphological similarity between lancea (Thunb.) Fraser-Jenk. [ Neotriblemma lancea (Thunb.) Deparia prolifera and Lunathyrium s. l. was first noted by Kato Nakaike 5 Diplazium subsinuatum (Hook. & Grev.) Tagawa; (1977), who proposed four sections under Deparia, three of Fig. 1H], respectively. Because the genus Triblemma by Ching which were transferred from Lunathyrium s. l. This four-section (1978) is illegitimate due to the earlier name of Triblemma classification was detailed in the monographic work by Kato R. Br. ex C. Sprengel in Melastomataceae, Nakaike (2004) (1984); two subsections under sect. Athyriopsis were also 645 646 SYSTEMATIC BOTANY [Volume 43

Fig. 1. The diversity of Deparia (Athyriaceae). A. Deparia prolifera (Kaulf.) Hook. & Grev. B. Deparia dickasonii M. Kato. C. Deparia pycnosora (Christ) M. Kato. D. Deparia japonica (Thunb.) M. Kato. E. Deparia erecta (Z. R. Wang) M. Kato. F. Deparia parvisora (C. Chr.) M. Kato. G. Deparia heterophlebia (Mett. ex Baker) R. Sano. H. Deparia lancea (Thunb.) Fraser-Jenk. Photos: A by John Game; B, D, E, G by Li-Yaung Kuo; C, H by Pi-Fong Lu; and F by Germinal Rouhan. recognized by Wang (1982). The inclusion of Neotriblemma in deparioid genera as distinct: Athyriopsis, Dictyodroma, Dry- Deparia was first implied by Matsumoto and Nakaike (1990), oathyrium, Lunathyrium, and Neotriblemma (i.e. Triblemma). and Fraser-Jenkins (1997) pointed out the similarity in indu- The currently defined Deparia s. l. comprises 60–90 species, ment between Deparia lancea and Deparia sensu Kato (1984); with highest diversity in Asia but also distributed in Africa and this generic treatment was also supported by evidence from islands of the western Indian Ocean, northeastern North the rachis-groove morphology, cytology, and molecular America, the Hawaiian Islands, Australia, New Zealand, and phylogenetic studies (Nakato and Mitui 1979; Matsumoto and South Pacific Islands (Kato 1984; Rothfels et al. 2012b; He et al. Nakaike 1990; Sano et al. 2000b). Sano et al. (2000c) transferred 2013; Kuo et al. 2016, 2018b; PPG I 2016; and this study). Dictyodroma to Deparia, based on their cytological and mo- Irrespective of the marked taxonomic changes, this genus can lecular phylogenetic data (Sano et al. 2000a). However, the be distinguished from other athyrioids by both morphological species that were moved from Neotriblemma and Dictyodroma and cytological features. The hairlike scales (Fig. 2D, E), and still have not been assigned to any section. While He et al. the discontinuous grooves between rachises and costae (2013) transferred most Chinese species to Deparia, some (Fig. 2E) are the diagnostic and synapomorphic characters taxonomists (e.g. Chu et al. 1999) still recognized many (Kato 1973, 1977, 1984; Rothfels et al. 2012b; Sundue and 2018] KUO ET AL.: DEPARIA INFRAGENERIC REVISION 647

Fig. 2. Diagnostic characters in Deparia and other athyrioids. A. Cross section of broadly U-shaped rachis groove of Diplazium chinense (Baker) C. Chr. B. Narrowly U-shaped rachis groove of Deparia formosana (Rosenst.) R. Sano. C. V-shaped rachis groove of Athyrium opacum (D. Don) Copel. D. Hairlike scale of Deparia formosana (Rosenst.) R. Sano (upper) and gland-tipped hair of Deparia concinna (Z. R. Wang) M. Kato (lower) (provided by Li-Yaung Kuo). E. Discontinuous groove between rachis and costa of Deparia jiulungensis (Ching) Z. R. Wang; rachis and costae are covered by hairlike scales. F. Continuous groove between rachis and costae of Athyrium arisanense (Hayata) Tagawa. G. Anastomosing venation and diplazioid sori of Deparia formosana (Rosenst.) R. Sano. H. Swollen stipe base and pneumatophore (the arrow) of Deparia wilsonii (Christ) X. C. Zhang. I. Longitudinal section of swollen stipe base of Deparia unifurcata (Baker) M. Kato. J. Round-reniform sori of Deparia subfluvialis (Hayata) M. Kato. K. Linear (or asplenioid type), J-shaped, and U-shaped sori of Deparia erecta (Z. R. Wang) M. Kato. L. Toothed indusial margin of Deparia petersenii (Kuntze) M. Kato. M. Echinate perine, with smooth spore underlayer of Deparia erecta (Z. R. Wang) M. Kato. N. Folding perine, with glandular-papillate spore underlayer of Deparia formosana (Rosenst.) R. Sano. Scale bars 5 0.5 mm (D) and 10 mm (M and N). Photos: A–D, H–I, K, M–N by Li-Yaung Kuo; E–G, J, L by Pi-Fong Lu. 648 SYSTEMATIC BOTANY [Volume 43

Rothfels 2014; Kuo et al. 2018b). These features are almost were higher than 1000. Overall, our phylogenies (both ML and absent from other athyrioids although hairlike scales can be BI; Fig. 3) revealed a similar relationship as those from Kuo found in some Diplazium species (Kato 1973; Rothfels et al. et al. (2016, 2018b). Deparia and seven infrageneric clades were 2012b). Compared with the V-shaped rachis grooves in all highly supported as monophyletic (BS $ 99 and PP 5 1; Fig. Athyrium Roth [sensu PPG I (2016) or athyriids sensu Rothfels 3). Three newly included species, D. longipilosa, D. mar- et al. (2012b)] and the broadly U-shaped ones in Diplazium (Fig. ojejyensis, and D. septentrionalis, were nested in the DR clade 2A, C), the rachis grooves in Deparia are narrowly U-shaped (Fig. 3). Together with D. parvisora, these four endemic species (Fig. 2B). The basic chromosome number of Deparia is 40 as in Madagascar formed a monophyletic group (BS 5 100 and well as most Athyrium while 41 is reported for Diplazium (Sano PP 5 1; Fig. 3). Deparia 3nakaikeana and D. polyrhizon were et al. 2000a, b; Rothfels et al. 2012b). nested in the DE and CA clades, respectively. Phylogenetically, Deparia is a monophyletic genus sister to Athyrium 1 Diplazium (Rothfels et al. 2012a; Wei et al. 2017). Discussion Although previous phylogenetic studies revealed synapo- Based on the cpDNA phylogeny, we classify the seven morphies supporting some clades within Deparia (Kuo et al. inferred clades at the infrageneric rather than the generic rank 2018b), none of these clades conform to the previously defined for the following reasons: 1) there are morphological and cy- infrageneric sections or subsections (e.g. Kato 1984) and none tological characters shared by all species within Deparia s. l., as of these sections/subsections are monophyletic (Kuo et al. noted in the introduction; 2) some clades lack unique synapo- 2016, 2018b). Our study aims to revise the infrageneric clas- morphy (Kuo et al. 2018b) and finely divided genera are difficult sification of Deparia based on the evidence from both phylo- to define; and 3) there are several hybrids between the clades genetic analyses and morphology. (Kato 1984; Nakaike 2013; Ebihara 2017). More narrowly defined genera in the deparioid clade will lead to the recognition of Materials and Methods intergeneric hybrids, which is not recommended (PPG I 2016). Our infrageneric revision of Deparia is modified from Kato DNA Sequences—In this study, chloroplast DNA (cpDNA) sequences of rbcL, matK, rps16-matK intergenic spacer (IGS), and trnL-L-F (trnL gene 1 (1984). In this revision, we establish a five-section classification trnL-F IGS) from five Deparia species were newly generated. These five taxa (Fig. 3; Table 1) by adding two new sections, sect. Dictyodroma were Deparia longipilosa Rakotondr., D. marojejyensis (Tardieu) M. Kato, and sect. Erectus, and subsuming sect. Athyriopsis in sect. 3 D. nakaikeana Fraser-Jenk., D. polyrhizon (Baker) Seriz., and D. septen- Deparia.Insect.Deparia, three subsections are recognized, trionalis Rakotondr. DNA extraction, PCR (primers and conditions), and sequencing protocols followed Kuo et al. (2011, 2016), Li et al. (2011), and subsect. Deparia, subsect. Athyriopsis, and subsect. Caespites;the Rothfels et al. (2012a). Sequences for outgroups (11 species from Diplazium last two subsections are segregated from the previous sect. and Athyrium, one from Blechnaceae, and one from Onocleaceae) and 57 Athyriopsis (sensu Kato 1984). In addition, new taxonomic status additional Deparia taxa were obtained from GenBank. Voucher information is provided for four Deparia species, with one species transferred and GenBank accession numbers of Deparia taxa are provided in Appendix to Diplazium. To identify Deparia taxa under each of these sec- 1. Voucher information and GenBank accession numbers for outgroup taxa are same as in Kuo et al. (2016, 2018b). tions and subsections, we also provide a character table for Alignment and Phylogenetic Analyses—Our alignment was slightly comparison (Table 1), a key, and a list of representative species modified from the one used in Kuo et al. (2018b). We added the newly in these infrageneric taxa (Appendix 2). generated sequences of the five Deparia taxa and removed sequences of “Deparia sp.” and “Deparia forsythii-majoris” because these samples were suggested as synonyms of other Deparia species rather than distinct taxa Taxonomic Treatment (Rakotondrainibe and Jouy 2016). Newly added sequences were aligned using BioEdit v. 7.0.5.3 (Hall 1999), and the final alignment was examined DEPARIA Hook. & Grev., Icon. Fil. t. 1829; emend., M. Kato, Bot. manually. In total, the cpDNA alignment included 62 taxa represent- Mag. Tokyo 90: 35. 1977; J. Fac. Sci. Univ. Tokyo III, 13: ing . 71% of species diversity (excluding hybrids) and comprised 4318 381. 1984; Sledge, Bot. J. Linn. Soc. 84: 16 1982. TYPE: characters. Nine partitions were initially identified in the alignment, in- Deparia macraei Hook. & Grev. [5 Deparia prolifera (Kaulf.) cluding each of codon positions in matK, each of codon positions in rbcL, trnL gene, trnL-F IGS, and rps16-matK IGS. We used PartitionFinder2 Hook. & Grev. Basionym: Dicksonia prolifera Kaulf. Lec- (Lanfear et al. 2017) to infer the best partition scheme and substitution totype (designated here): USA. Hawaiian Islands, Oahu, models for both maximum likelihood (ML) and Bayesian inference (BI) without precise date, Chamisso 716 (LE-00008016)] analyses. Garli 2.0 (Zwickl 2006) was used to reconstruct ML phylogeny, and the “genthreshfortopoterm” option was set to 20,000. To search for the Lunathyrium Koidz., Acta Phytotax. Geobot. 1: 30. 1932. TYPE: most likely ML tree, ten independent replicates were carried out, and the Athyrium pycnosorum Christ [[ Deparia pycnosora (Christ) resulting tree with the highest likelihood value was selected. For the ML M. Kato] bootstrap (BS) analysis, 1000 replicates were run. BI was performed using MrBayes v. 3.2.6 with branch supports estimated as posterior probability Dryoathyrium Ching, Bull. Fan Mem. Inst. Biol. 11: 79. 1941. (PP) (Huelsenbeck and Ronquist 2001; Ronquist and Huelsenbeck 2003). TYPE: Aspidium boryanum Willd. [[ Deparia boryana (Willd.) Two simultaneous runs and four chains (two million generations each) were carried out, with each chain sampled every 1000 generations. Tracer M. Kato] v. 1.6 (Rambaut and Drummond 2013) was used to determine convergence Parathyrium Holttum, Kew Bull. 13: 448. 1958, nom. superfl. through generations among chains. The first 25% of the generations were [ conservatively discarded as burn-in, and the rest were used to summarize TYPE: Aspidium boryanum Willd. [ Deparia boryana (Willd.) as the 50% majority-rule consensus tree. M. Kato]

Dictyodroma Ching, Acta Phytotax. Sin. 9(4): 12. 1978. TYPE: Results Asplenium heterophlebium Mett. ex Baker [[ Deparia heterophlebia (Mett. ex Baker) R. Sano] Details of partition/model schemes inferred from Parti- tionFinder2 were provided in the nexus files deposited in Athyriopsis Ching, Acta Phytotax. Sin. 9: 63. 1964 & 16(3): 12 Dryad (Kuo et al. 2018a). For all parameters in the Bayesian 1978. TYPE: Asplenium japonicum Thunb. [[ Deparia ja- analysis, their effective sample sizes of post-burn-in samples ponica (Thunb.) M. Kato] 2018] KUO ET AL.: DEPARIA INFRAGENERIC REVISION 649

Fig. 3. Maximum likelihood (ML) cpDNA phylogeny of Deparia based on rps16-matK IGS 1 trnL-L-F 1 matK 1 rbcL. Names on the branches within Deparia indicate the clade inferred by Kuo et al. (2016, 2018b), and the colored boxes behind the taxa indicate sections/subsections treated in this study. Taxon names headed with an asterisk (*) are putative hybrid species between clades. ML bootstrap support (BS) supports and posterior probabilities of Bayesian phylogenetic inference (PP) are indicated under each branch as BS/PP. The plus (1) sign represents BS 5 100 or PP 5 1.00, and a dash (–) represents BS , 50. A–G on the nodes indicate some key synapomorphic transitions at the clade level, which are inferred by Kuo et al. (2018b): A 5 Disconnected rachis- costa groove, B 5 Auricled proximal pinnae, C 5 Anastomosing venation, D 5 Stipes without obvious swollen base and pneumatophores, E 5 Spore perine with tuberculate/lamellate/echinate projections, F 5 Spore perine with folded/cristate projections, G 5 Creeping rhizomes.

3Depazium Nakaike, New Fl. Jap. Pterid. 840. 1992. [ Neotriblemma Nakaike, J. Nippon Fernist Club 3(Suppl. 2): 128. 3Neotribleparia Nakaike, J. Nippon Fernist Club 3(Suppl. 2004. [ Asplenium [unranked] Triblemma J. Sm., Ferns Brit. 2): 128. 2004. TYPE: Diplazium tomitaroanum Masam. [[ For. 209. 1866. [ Triblemma Ching, Acta Phytotax. Sin. 16 Deparia 3tomitaroana (Masam.) R. Sano] (3): 24. 1978, nom. illeg. [non Triblemma R. Br. ex C. 650 SYSTEMATIC BOTANY [Volume 43

Table 1. Summary of Deparia sections and subsections, and phylogenetic clade for various morphological characters. Soral type: A 5 asplenioid sori; J 5 J-shaped sori; U 5 U-shaped sori; R 5 round-reniform sori; D 5 diplazioid sori; C 5 cup-shaped sori.

Sections Dryoathyrium Lunathyrium Erectus Dictyodroma Deparia

Subsections Caespites Athyriopsis Deparia Phylogenetic DR LU ER DI CA AT DE clade Blade dissection Bi-quadripinnatifid Bi-tripinnatifid Bipinnatifid Lobed to Bipinnatifid Pinnatifid to Simple to pinnatifid 2-pinnate- tripinnatifid pinnatifid Proximal lateral Non-auricled Mostly auricled, Non-auricled Non-auricled Non-auricled or Mostly auricled Non-auricled pinnules usually reduced slightly auricled proximally Venation Free Free Free Anastomosing Free Free Free Soral type A, J, U, R, D (rare) A, D, J, U A, J, U A, D A, D, J (rare) A, D, J (rare) A, D, C, U (rare) Rhizome habit Short creeping or Short-creeping or Erect Erect Erect Short or Long-creeping erect erect long-creeping or erect Stipe bases Swollen Swollen Slender Slender Slender Slender Slender Pneumatophores Present/absent Mostly present Absent Absent Absent Absent Absent Indusial margin Entire or toothed Entire or toothed Toothed Entire Entire or toothed Toothed Entire or rarely weakly toothed Costae abaxially Hairy or not Hairy or not Hairy Hairy at base Hairy Hairy Non-hairy mostly Perine Elongate- Elongate- Echinate Reticulate Tuberculate / Tuberculate / Echinate or reticulate reticulate folds folds lamellate lamellate tuberculate / folds or tuberculate lamellate

Sprengel]. TYPE: Asplenium lanceum Thunb. [[ Deparia Proximal pinnae auricled or non-auricled. Veins free or anas- lancea (Thunb.) Fraser-Jenk.] tomosing (Fig. 2G). Costal grooves interrupted at the junction to rachis (Fig. 2E). Sori linear, asplenioid, diplazioid, or J-shaped, U- Rhizomes erect to long-creeping. Stipe bases swollen, with or without pneumatophores at both lateral sides (Fig. 2H), or shaped, cup-shaped, or round-reniform at distal vein endings – slender without pneumatophores; with light brown to black, (Fig. 2J K). Indusial margins entire or toothed (Fig. 2L). Spores acuminate, baxifixed, entire scales, rarely with marginal glands. bilateral, each with folded, laminate, tuberculate, or echinate Fronds simple to quadripinnatifid. Grooves on the rachises perine; perine surfaces glandular or smooth (Fig. 2M, N). narrow U-shaped (Fig. 2B). Laminae generally herbaceous, Habitat—Species are terrestrial in forests, occasionally gemmiferous adaxially on costae/rachises or not, densely to rheophilous, or in wet rocky places. sparingly scaly and hairy. Laminal scales light brown to black or Cytology—Chromosome number is x 5 40. mixed with transparent and clathrate scales (hairlike scales), Species Composition—Approximately 92 species are in the multicellular hairs usually with glands at the tip (Fig. 1D). genus (Appendix 2).

Key to Sections and Subsections of Deparia

1. Veins anastomosing ...... …sect. Dictyodroma 1. Veins free ...... …2 2. Stipe bases swollen, with or without pneumatophores 3. Proximal pinnae non-auricled; sori rarely diplazioid, round-reniform or not, or with other types ...... ……sect. Dryoathyrium 3. Proximal pinnae auricled and slightly or hardly reduced; sori frequently diplazioid, not round-reniform ...... ……sect. Lunathyrium 2. Stipes slender, without swollen bases and pneumatophores 4. U-shaped sori always present, sori never diplazioid; fronds without gemmae; rhizomes erect ...... …sect. Erectus 4. Not as the above combination ...... ……5 sect. Deparia 5. Fronds simple ...... …subsect. Deparia (part) 5. Fronds pinnatifid to tripinnatifid ...... 6 6. Rachises non-hairy, without hairlike scales; costae usually non-hairy abaxially ...... subsect. Deparia (part) 6. Rachises hairy, with or without hairlike scales; costae hairy abaxially ...... 7 7. Rhizomes erect; proximal pinnae non-auricled or slightly auricled; rachises without or rarely with hairlike scales . . . . subsect. Caespites 7. Rhizomes long-creeping; proximal pinnae usually auricled; rachises with hairlike scales ...... …subsect. Athyriopsis

Section DRYOATHYRIUM (Ching) M. Kato, J. Fac. Sci. Univ. Tokyo Pacific Islands, Africa, Madagascar, and western Indian III, 13: 383. 1984. – Dryoathyrium Ching, Bull. Fan Mem. Oceanic Islands. Cryptic species, apparent from molecular Inst. Biol. 11: 79. 1941. TYPE: Aspidium boryanum Willd. [[ phylogeny (Kuo et al. 2016), occur in Africa and Madagascar, Deparia boryana (Willd.) M. Kato] and two Malagasy species were described recently (i.e. Deparia longipilosa and D. septentrionalis; Rakotondrainibe and Jouy Parathyrium Holttum, Kew Bull. 13: 448. 1958. nom. superfl. 2016). Deparia pterorachis and D. coreana belong here, which TYPE: Aspidium boryanum Willd. [[ Deparia boryana were previously assigned to sect. Lunathyrium by Kato (1984). (Willd.) M. Kato] Note—The diagnostic characters of sect. Dryoathyrium are Diversity and Systematics—About 20 species are distrib- swollen stipe bases, asplenioid, J-shaped, U-shaped, or round- uted in southern and eastern Asia, Himalayan region, south reniform sori (rarely diplazioid sori), and non-auricled 2018] KUO ET AL.: DEPARIA INFRAGENERIC REVISION 651 proximal pinnae (Fig. 2F; Table 1). The latter two characters collection (Price 1990). Due to their unique anastomosing support placement of Deparia pterorachis and D. coreana within venation (in athyrioids), they have been treated either under this section instead of in sect. Lunathyrium. Diplazium (Kato 1973, 1975), or in a distinct genus, Dictyodroma (Ching 1964), or even under a more distantly related genus, Deparia chinensis (Ching ex S. Y. Jin & Y. L. Chen) T. C. Hsu & Diplaziopsis (Price 1990) in Diplaziopsidaceae (Christenhusz L. Y. Kuo, comb. nov. Dryoathyrium chinense Ching ex S. Y. et al. 2011; Rothfels et al. 2012b; PPG I 2016). Evidence from Jin & Y. L. Chen, Cat. Type Spec. China 41. 1994. TYPE: cytology and molecular phylogenetic analyses have shown CHINA. Sichuan, Chenkou, Nov. 17 1958, T. L. Tai 106702 that Dictyodroma formosana belongs to Deparia (Sano et al. (Lectotype designed here: PE-00049936; isolectotype: PE- 2000a). Furthermore, our analysis suggests that all Dictyodroma 00049937). “Dryoathyrium chinense Ching”, Fl. Tsinling 2: species (sensu Chu et al. 1999 and He et al. 2013) form a 101 & 214–215. 1974, nom. inval. “Deparia chinensis Z. R. monophyletic lineage embedded in Deparia (Fig. 3). Based on Wang”, Fl. China. vol. 2–3: 422. 2013, nom. illeg. these results, we establish here a new section for these species. Ching (1974) failed to validly publish Dryoathyrium chinensis The anastomosing veins are a unique synapomorphy and since he cited two specimens as “type”, which is contrary to diagnostic character of this section (Kuo et al. 2018b; Fig. 2G; ICN Art. 40.2 (McNeill et al. 2012). The correct authority is Table 1). attributed to Jin and Chen (1994), who cited Ching’s (1974) Section Erectus L. Y. Kuo, M. Kato & W. L. Chiou, sect. nov. Latin description and validly designated a type specimen. TYPE: Athyriopsis erecta Z. R. Wang [[ Deparia erecta (Z. R. Wang’s new combination under Deparia (in He et al. 2013) is Wang) M. Kato] also invalid because he cited an incorrect reference of basionym, which is contrary to ICN Art. 41.5. Rhizomes erect. Stipe bases slender without pneumatophores. Lateral pinnae non-auricled and short-stalked. Veins Section LUNATHYRIUM (Koidz.) M. Kato, Bot. Mag. Tokyo 90: 37. free. Sori linear, J-shaped, or U-shaped, never diplazioid. 1977; J. Fac. Sci. Univ. Tokyo, Sect. 3, Bot. 13(4): 390. 1984. Spore perine echinate (Fig. 2M), surfaces smooth. Lunathyrium Koidz., Acta Phytotax. Geobot. 1: 30. 1932. Diversity and Systematics—This section contains a single TYPE: Athyrium pycnosorum Christ [[ Deparia pycnosora species, Deparia erecta, and is endemic to China. The species (Christ) M. Kato] was first described in Athyriopsis sect. Caespites (Wang 1982). A Diversity and Systematics—About 26 species occur in later treatment placed this species either in Dryoathyrium (Chu eastern Asia, the Himalayan region, New Guinea, and et al. 1999), based on the similarity of the erect rhizomes and northeastern North America. This section has very high spe- elongate to short-linear, usually curved sori, or in Deparia sect. cies diversity in eastern Asia (. 90%), especially in China and Athyriopsis subsect. Caespites (Kato 1984), because of its slender the Himalayan region. Deparia pterorachis and D. coreana, stipe bases. Based on molecular phylogenetic analyses and placed in this section by Kato (1984), are here moved to sect. perine morphology, Wang et al. (2003, 2006) implied that this Dryoathyrium. Most members of sect. Lunathyrium share the species is closely related to Athyriopsis and distantly related to pinnate-pinnatifid blades and need further research to es- Dryoathyrium. However, their comparison lacked represen- tablish species boundaries, especially for eastern Asian taxa. tatives from the DI and CA clades. Our analysis, based on Note—The diagnostic characters of sect. Lunathyrium are the more comprehensive sampling, suggests that Deparia erecta presence of pneumatophores, swollen stipe bases, and auricled and the DI clade (i.e. sect. Dictyodroma) form a monophyletic proximal pinnae (Fig. 2C; Table 1). group, and this lineage is sister to the CA 1 DE 1 AT clade (i.e. our sect. Deparia; see further comments below; Fig. 3). Placing Deparia wangzhongrenii L. Y. Kuo, M. Kato, & W. L. Chiou, this species in either Athyriopsis or subsect. Athyriopsis thereby nom. nov. Lunathyrium emeiense Z. R. Wang, Fl. Reipubl. results in an artificial classification. Here, we establish sect. Sin. 3: 510. 1999. Deparia emeiensis (Z. R. Wang) Z. R. Erectus and characterize this new section by echinate and Wang, Fl. China vol. 2–3: 431. 2013. TYPE:CHINA. Sichuan, smooth-surfaced perine (Fig. 2M). Emeishan, Sept. 15 1979, Z. R. Wang 61 (holotype: PE- Note—Soral types in sect. Erecta always present U-shaped, 00050464). never diplazioid, and are different from those of our sect. The specific epithets of Deparia emeiensis and D. omeiensis Deparia, which includes subsect. Caespites (see below; Table 1). (Z. R. Wang) M. Kato are derived from the same locality, Mt. Emei or Omei (Wang 1982, 1999), and likely to be confused. Section Deparia Based on ICN Art. 53.3, we treat D. emeienis as a later homonym of D. omeiensis and apply a new name as replacement. The new Diversity and Systematics—Kato (1984) characterized sect. specific epithet is dedicated to a pioneer taxonomist of Chinese Deparia by having slender stipe bases, non-hairy fronds, and athyrioids, Dr. Zhong-Ren Wang, who discovered this species. erect rhizomes. However, the most recent phylogenies revealed that both sect. Deparia and sect. Athyriopsis sensu Kato Section Dictyodroma (Ching) L. Y. Kuo, M. Kato, & W. L. (1984) are polyphyletic (Sano et al. 2000a, b; Tzeng 2002; Wang Chiou, comb. & stat. nov. Dictyodroma Ching, Acta et al. 2003; Ebihara 2011; Kuo et al. 2016, 2018b; Fig. 3). Indeed, Phytotax. Sin. 9(4): 12. 1978. TYPE: Asplenium hetero- some characters, such as erect rhizomes and non-hairy fronds, phlebium Mett. ex Baker [[ Deparia heterophlebia (Mett. ex are similar to some members of sect. Athyriopsis sensu Kato Baker) R. Sano]. Lectotype (designated here): INDIA, (1984). To maintain each section and subsection as mono- Assam, without precise date, Griffith 22 (K-001089385). phyletic groups, we combine sect. Deparia and sect. Athyriopsis Diversity and Systematics—Four species are in this section, sensu Kato (1984), along with Deparia erectus, and divide them and they are distributed in eastern Asia (Japan, China, and into three subsections: subsect. Caespites, subsect. Deparia, and Taiwan), the Himalayan region, and southeastern Asia subsect. Athyriopsis (for the CA, DE, and AT clades, re- (Vietnam). A record from the Philippines is based on a single spectively; Fig. 3). 652 SYSTEMATIC BOTANY [Volume 43

Note—The diagnostic characters defining section Deparia Diversity and Systematics—About 20 species are in this are slender stipe bases, free venation, diplazioid sori (except subsection, and they are widely distributed in eastern, for Deparia prolifera), and lamellate to echinate perine. Different southeastern, and southern Asia. Species are also distributed subsections within sect. Deparia cannot be defined by using a in South Pacific islands, Australia, New Zealand, and islands single morphological character (Table 1). Rhizome habit and in the western Indian Ocean. Deparia petersenii is also natu- frond indument are salient key characters in identifying these ralized worldwide, and now occurs in the Hawaiian Islands, subsections (see Key and Table 1). Central America, and South America. Except for Deparia otomasui, D. 3lobatocrenata, and D. 3zeylanica, our concept of subsect. Athyriopsis includes most members previously Subsection Deparia regarded by Kato (1984) as his sect. Athyriopsis. Deparia oto- Neotriblemma Nakaike, J. Nippon Fernist Club 3(Suppl. 2): 128. masui is similar to species belonging to this subsection in 2004. [ Asplenium [unranked] Triblemma J. Sm., Ferns Brit. having long-creeping rhizomes and toothed indusial margins For. 209. 1866. [ Triblemma Ching, Acta Phytotax. Sin. 16 (Kato 1984; Fig. 2), but these morphological similarities have (3): 24. 1978, nom. illeg. [non Triblemma R. Br. ex C. resulted from evolutionary convergence (Kuo et al. 2018b). 3 3 Sprengel]. TYPE: Asplenium lanceum Thunb. [[ Deparia Deparia lobatocrenata and D. zeylanica were putative hy- lancea (Thunb.) Fraser-Jenk.] brids in having irregular meiosis and irregular spores. Com- — bining evidence from morphology and molecular phylogenetic Diversity and Systematics Eight species are in this sub- analyses suggest that they are most likely inter-subsectional section, and they occur in eastern Asia, the Himalayan region, hybrids (see discussion below). This subsection has some southeastern Asia (Vietnam, Thailand, Borneo, and the Phil- polyploid species complexes (e.g. D. petersenii; Shinohara et al. ippines), Sri Lanka, and the Hawaiian Islands. Two species are 2006), and, in order to clarify their constituent taxa, further endemic to Japan and five to the Hawaiian Islands. Deparia investigation is needed. lancea is the only widely distributed species. Based on the Note—The diagnostic characters of this subsection are the molecular phylogeny (Fig. 3), we further include two addi- creeping rhizomes, hairy rachis with hairlike scales, and tional species in subsect. Deparia: D. lancea and D. otomasui. toothed indusial margins (Fig. 2L; Table 1). In most species, the Both species are similar to members of sect. Deparia sensu Kato proximal pinnae are auricled (Fig. 1D; Table 1). (1984) in having non-hairy fronds, but they differ in having long-creeping rhizomes. Deparia lancea is unique in having Deparia deflexa (Kunze) L. Y. Kuo, M. Kato, & W. L. Chiou, simple laminae, and is the type of Neotriblemma (Ching 1978; comb. nov. Allantodia deflexa Kunze, Bot. Zeit. 6: 191. 1848. Nakaike 2004). A diagnostic character of our revised subsect. Deparia petersenii (Kunze) M. Kato subsp. deflexa (Kunze) Deparia is non-hairy rachises lacking hairlike scales, sometimes M. Kato, J. Fac. Sci. Univ. Tokyo, Sect. 3, Bot. 13: 425. 1984. with a few brown, dense scales on the proximal part (Table 1). TYPE:INDONESIA. Java, without precise date, H. Zollinger Deparia species with gemmiferous fronds occur only in this 1962 (isotype: Z-000002125). subsection. The cpDNA phylogeny (Fig. 3) suggests that this taxon is — Note The combination of these three characters, abaxially distantly related to Deparia petersenii and should not be sub- non-hairy costae, non-auricled proximal pinnae, and entire sumed under it. Therefore, we provide a new combination for indusial margins, will usually distinguish subsect. Deparia this taxon at the species level. from other subsections (see Key and Table 1). These characters Hybrid Species Between Sections/Subsections—Several also support inclusion of D. lancea and D. otomasui in this described Deparia species are putative hybrids between species subsection. in different sections or subsections. Deparia 3kiyozumiana Subsection Caespites (Ching & Z. R. Wang) L. Y. Kuo, M. Kato is a putative hybrid from D. coreana (sect. Dryoathyrium) & W. L. Chiou, comb. & stat. nov. Sect. Athyriopsis subsect. and D. jiulungensis (sect. Lunathyrium) (Nakaike 2013). Caespites (Ching & Z. R. Wang) M. Kato, J. Fac. Sci. Univ. Deparia 3togakushiensis was published as a presumed hybrid Tokyo, Sect. 3, Bot. 13: 402. 1984. TYPE: Athyriopsis between D. jiulungensis [syns. D. orientalis and D. pycnosora omeiensis Z. R. Wang [5 Deparia omeiensis (Z. R. Wang) M. var. albosquamata (sect. Lunathyrium)] and D. conilii (sect. Kato] Deparia subsect. Athyriopsis) (Otsuka and Fujiwara 1999). In sect. Deparia, hybridization between different subsections Diversity and Systematics—Five species are known in this seems relatively frequent, and morphologically, the follow- subsection, and distributed in eastern Asia (Japan and China), ing four species are regarded as putative hybrids between D. the Himalayan region, and Sri Lanka. Deparia erecta was lancea (subsect. Deparia) and species of subsect. Athyriopsis: previously included either in Athyriopsis sect. Caespites sensu D. 3lobatocrenata, D. 3tomitaroana, D. 3zeylanica,and Wang (1982) or in subsect. Caespites sensu Kato (1984), but it is D. 3nakaikeana. Deparia 3nakaikeana was described as a hy- here placed in sect. Erectus. brid between D. lancea and D. petersenii (Fraser-Jenkins 2008). Note—The combination of three characters (erect rhizomes, Given that cpDNA is known to be maternally inherited in abaxially hairy costae, and rachises lacking or with rare Deparia species (Kuo et al. 2018c), the maternal lineage of hairlike scales) distinguish subsect. Caespites from other sub- D. 3lobatocrenata is from subsect. Athyriopsis,andthema- sections (see Key and Table 1). ternal lineage of D. 3tomitaroana and D. 3nakaikeana is allied Subsection Athyriopsis (Ching) L. Y. Kuo, M. Kato & W. L. with D. lancea (Fig. 3; Kuo et al. 2018c). To study and possibly Chiou, comb. & stat. nov. Athyriopsis Ching, Acta Phy- confirm both parental lineages of these hybrids, further in- totax. Sin. 9: 63 1964 & 16(3): 12. 1978. Deparia sect. vestigation using nuclear markers is needed. Athyriopsis (Ching) M. Kato, J. Fac. Sci. Univ. Tokyo, Sect. Other Species Morphologically Similar to Deparia—Athyrium 3, Bot. 13: 401. 1984. TYPE: Asplenium japonicum Thunb. [[ parvum Copel. is a species originally described from Cata- Deparia japonica (Thunb.) M. Kato] nduanes (Luzon, the Philippines), and is treated as a synonym 2018] KUO ET AL.: DEPARIA INFRAGENERIC REVISION 653 of Diplazium cordifolium Blume (e.g. Price 1990). Notably, this Christenhusz, M. J. M., X.-C. Zhang, and H. Schneider. 2011. A linear D. cordifolium sequence of extant families and genera of lycophytes and ferns. species is slightly different from in having – anastomosing venation (areoles usually hexagonal or hep- Phytotaxa 54: 7 54. Chu, W.-M., Z.-R. Wang, X.-C. Zhang, Z.-R. He, and Y.-T. Hsieh. 1999. tagonal vs. diamond-shaped or pentagonal). Venation in A. Athyriaceae. Pp. 32–511 in Flora of Reipublicae Popularis Sinicae, vol. parvum is very similar to venation in Diplaziopsis (Diplaziop- 3(2). Beijing: Science Press. sidaceae) and Deparia sect. Dictyodroma. However, examination Ebihara, A. 2011. RbcL phylogeny of Japanese pteridophyte flora and of the type materials of A. parvum (holotype: MICH-1190134; implications on infrafamilial systematics. Bulletin of the National Museum of Nature and Science. Series B, Botany 37: 63–74. isotype: UC-370501) reveals that it has no hairlike scales on Ebihara, A. 2017. Deparia. Pp. 98–118, 342–353 in The Standard of Ferns and fronds (a typical character in Deparia), and its rhizome scales are Lycophytes in Japan, vol. 2. Tokyo: Gakken Plus. blackish and weakly toothed at the margins (a character typical Fraser-Jenkins, C. R. 1997. New Species Syndrome in Indian Pteridology and the of many Diplazium species; Wei et al. 2013). Moreover, the Ferns of Nepal. Dehra Dun: International Book Distributors. perine of A. parvum comprises long and thin wings (L.-Y. Kuo Fraser-Jenkins, C. R. 2008. Taxonomic Revision of Three Hundred Indian Subcontinental Pteridophytes with a Revised Census-list: A New pers. obs.). These indument and perine features do not occur in Picture of Fern-Taxonomy and Nomenclature in the Indian Sub- Deparia species but can be found in Diplaziopsis or Diplazium continent. Dehra Dun: Bishen Singh Mahendra Pal Singh. species, particularly in the latter genus. Thus, Athyrium parvum Hall, T. 1999. BioEdit: A user-friendly biological sequence alignment editor seems to be more closely related to Diplaziopsis or Diplazium. and analysis program for Windows 95/98/NT. Nucleic Acids Sym- – Deparia florensiae Rakotondr. is a Malagasy species charac- posium Series 41: 95 98. He, Z.-R., Z.-R. Wang, and M. Kato. 2013. Deparia (Athyriaceae). terized by hairy costae and rachises and diplazioid sori, which Pp. 418–442 in Flora of China, vol. 2–3, eds. Z.-Y. Wu, P. H. Raven, and also appear in some Deparia species. Based on re-examination D.-Y. Hong. Beijing: Science Press, and St. Louis: Missouri Botanical of the types, we found that this species has shallow, confluent Garden Press. adaxial grooving connecting rachises to costae and spore Holttum, R. E. 1958. Notes on Malayan ferns, with descriptions of a new – perine with thin wings. Such characters are not found in any genus and new species. Kew Bulletin 13: 447 455. Huelsenbeck, J. P. and F. Ronquist. 2001. MRBAYES: Bayesian inference of other Deparia taxa (Kuo et al. 2018b) but are known in some phylogenetic trees. Bioinformatics 3: 754–755. Diplazium species. cpDNA sequences (GenBank accessions: Jin, S. and Y. Chen. 1994. A Catalogue of Type Specimens (Cormophyta) in MG722870–71, MG722876–77, MG722888–89) generated from the Herbaria of China. Beijing: Science Press. type material of D. florensiae (isotypes: P-00835665) and an- Kato, M. 1973. Taxonomical evaluation of the articulated hairs found in the Acta Phytotaxonomica et Geobotanica – other collection (P-02434436) further confirm exclusion from Athyriaceae. 25: 119 126. Kato, M. 1975. Reticulate venation of Diplazium heterophlebium. Acta Deparia; rather it is nested within Diplazium (data not shown). Phytotaxonomica et Geobotanica 26: 160–163. Accordingly, we here make this new combination: Kato, M. 1977. Classification of Athyrium and allied genera of Japan. The Botanical Magazine 90: 23–40. Diplazium florensiae (Rakotondr.) Rouhan & L. Y. Kuo, comb. Kato, M. 1984. A taxonomic study of the athyrioid fern genus Deparia with nov. Deparia florensiae Rakotondr., Candollea 71(2): 361. main reference to the Pacific species. Journal of the Faculty of Science – 2016. TYPE:MADAGASCAR. Oct. 1999, F. Rakotondrainibe Section III 13: 371 430. and D. Florens 4887 (holotype, 2 sheets: P-00179472!, Koidzumi, G. 1932. Contributiones ad cognitionem florae asiae orientalis. Acta Phytotaxonomica et Geobotanica 1: 11–33. P-00179473!; isotypes: P-00835665!, TAN). Kuo, L.-Y., F.-W. Li, W.-L. Chiou, and C.-N. Wang. 2011. First insights into fern matK phylogeny. Molecular Phylogenetics and Evolution 59: 556–566. Acknowledgments Kuo, L.-Y., A. Ebihara, W. Shinohara, G. Rouhan, K. R. Wood, C.-N. Wang, and W.-L. Chiou. 2016. Historical biogeography of the fern genus We thank Pi-Fong Lu and John Game for providing photos of Deparia, Deparia (Athyriaceae) and its relation with polyploidy. Molecular – Che-Wei Lin for preparing images, and staffs in herbaria MICH and UC for Phylogenetics and Evolution 104: 123 134. help with further examination of type materials; Alan R. Smith, Fay-Wei Li, Kuo, L.-Y., A. Ebihara, T.-C. Hsu, G. Rouhan, Y.-M. Huang, C.-N. Wang, and two anonymous reviewers provided comments. We appreciate the W.-L. Chiou, and M. Kato. 2018a. Data from: Infrageneric revision of Japan-Taiwan Exchange Association, Taiwan Society of Plant Systematics, the fern genus Deparia (Athyriaceae, Aspleniineae, Polypodiales). Mr. Shann-Jye Moore Memorial Scholarship, and Dr. Yu-Pin Cheng Me- Dryad Digital Repository. https://doi.org/10.5061/dryad.7530v. morial Scholarship for providing financial support for this study. Col- Kuo, L.-Y., A. Ebihara, M. Kato, G. Rouhan, T. A. Ranker, C.-N. Wang, and lecting permits in Madagascar were granted to GR by Madagascar W.-L. Chiou. 2018b. Morphological characterization of infra-generic – National Parks and the Minist`ere de l’Environnement, de l’Ecologie et des lineages in Deparia (Athyriaceae; Polypodiales). Cladistics 34: 78 92. Forets.ˆ We are also grateful for field assistance from CNRE-Madagascar Kuo, L.-Y., T.-Y. Tang, H.-J. Su, F.-W. Li, W.-L. Chiou, Y.-M. Huang, and and MBG-Madagascar. C.-N. Wang. 2018c. Organelle genome inheritance in Deparia ferns (Athyriaceae, Aspleniineae, Polypodiales). Frontiers of Plant Science 9: 486. Author Contributions Kurata, S. 1961. Notes on Japanese ferns (21). Journal of Geobotany 9: 95–100. Lanfear, R., P. B. Frandsen, A. M. Wright, T. Senfeld, and B. Calcott. 2017. LYK designed this study and did all the experiments. LYK, AE, and GR PartitionFinder 2: New methods for selecting partitioned models of collected the samples. YMH, WLC, and CNW provided facilities to evolution for molecular and morphological phylogenetic analyses. complete this study. All authors provided comments on taxonomic Molecular Biology and Evolution 34: 772–773. treatments and drafts of this manuscript. Li, F.-W., L.-Y. Kuo, C. J. Rothfels, A. Ebihara, W.-L. Chiou, M. D. Windham, and K. M. Pryer. 2011. RbcL and matK earn two Literature Cited thumbs up as the core DNA barcode for ferns. PLoS One 6: e26597. Matsumoto, S. and T. Nakaike. 1990. Cytological observations of some Ching, R.-C. 1941. The studies of Chinese ferns XXXV. Bulletin of the Fan ferns in Nepal (1). On the related taxa in Japan. Cryptogams of the Memorial Institute of Biology 11: 79–82. Himalayas 2: 163–178. Ching, R.-C. 1964. On some confused genera of the family Athyriaceae. McNeill, J., F. R. Barrie, W. R. Buck, V. Demoulin, W. Greuter, Zhiwu Fenlei Xuebao 9: 41–84. D. L. Hawksworth, P. S. Herendeen, S. Knapp, K. Marhold, J. Prado, Ching, R.-C. 1974. Dryoathyrium chinense Ching. Pp. 214–215 in Flora W. F. Prud’homme van Reine, G. F. Smith, J. H. Wiersema, and Tsinlingensis, vol. 2. Beijing: Academia Scientiarum Sinicae. N. J. Turland. 2012. International Code of Nomenclature for Algae, Fungi, Ching, R.-C. 1978. The Chinese fern families and genera: Systematic ar- and Plants (Melbourne Code). Regnum Vegetabile 154. K¨onigstein: Koeltz rangement and historical origin (cont.). Zhiwu Fenlei Xuebao 16: 16–37. 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Nakaike, T. 1992. New Flora of Japan: Pteridophyta. Tokyo: Shibundo. Appendix 1. Voucher specimens and GenBank accession numbers for Nakaike, T. 2004. Index to scientific names of Japanese pteridophytes. Deparia cpDNA sequences used in this study. Information is presented in Journal of the Nippon Fernist Club 3(Suppl. 2): 1–207. the following order: taxon name, collection number (deposited herbarium), Nakaike, T. 2013. A Checklist of Lycophytes and Ferns of Japan. Shizuoka: locality (country), matK, rbcL, trnL-L-F, rps16-matK IGS. An asterisk (*) Youshi Press. indicates the new sequences generated in this study, and dash (–) indicates Nakato, N. and K. Mitui. 1979. Intraspecific polyploidy in Diplazium that information is not available. subsinuatum (Wall.) Tagawa. Journal of Japanese Botany 54: 129–140. Ohba, H. 1965. Considerations on the genus Lunathyrium in Japan (1). Deparia acrostichoides (Sw.) M. Kato, Kuo 120 (TAIF), Massachusetts Science Report of the Yokosuka City Museum 11: 48–55. (USA), JN673820, JN673929, JN673904, KX656083. Deparia acuta (Ching) Otsuka, K. and R. Fujiwara. 1999. A new hybrid of Deparia (Woodsiaceae) Fraser-Jenk., Kuo 2274 (TAIF), Sichuan (China), KY296505, KY296514, from Nagano Prefecture, central Japan. Journal of Phytogeography and KY296532, KY296523. Deparia aff. glabrata (Mett. ex Kuhn) M. Kato, MO- Taxonomy 47: 107–110. 6262952 (MO), Kakamega (Kenya), KX656032, KX656062, KX656144, PPG I. 2016. A community-derived classification for extant lycophytes and KX656084. Deparia aff. jiulungensis Z. R. Wang, TNS-763886 (TNS), Saitama ferns. Journal of Systematics and Evolution 54: 563–603. Pref. (Japan), JN673855, AB574957, JN673897, KX656085. Deparia auriculata Price, M. G. 1990. Philippine fern notes. Contributions from the University of (W. M. Chu & Z. R. Wang) Z. R. Wang, Kuo 1300 (TAIF), Yunnan (China), Michigan Herbarium 17: 267–278. KX656033, KX656063, KX656145, KX656086. Deparia biserialis (Baker) M. Rakotondrainibe, F. and A. Jouy. 2016. Revision of the genus Deparia Kato, Shinohara 0810501 (KYO), Kinabalu (Indonesia), JN673822, JN673931, Hook. & Grev. (Pteridophyta, Athyriaceae) from Madagascar: JN673906, KX656087. Deparia bonincola (Nakai) M. Kato, TNS-774841 Three new species, a new synonymy and putative hybrids. Can- (TNS), Bonin Is. (Japan), JN673823, AB574940, JN673865, KX656088. dollea 71: 357–371. Deparia boryana (Willd.) M. Kato, P-02432539 (P), Saint-Louis (La R´eunion), Rambaut, A. and A. J. Drummond. 2013. Tracer v. 1.6. http://tree.bio.ed. KX656034, KX656064, KX656146, KX656089. Deparia cataracticola M. Kato, – ac.uk/software/tracer/. Wood 12767 (PTBG), Hawaii (USA), KX656035, , KX656147, KX656090; – – – Ronquist, F. and J. P. Huelsenbeck. 2003. MrBayes 3: Bayesian phylogenetic Kato H-105 (TI), Hawaii (USA), , AB046982, , . Deparia concinna (Z. R. inference under mixed models. Bioinformatics 19: 1572–1574. Wang) M. Kato, Kuo 2268 (TAIF), Sichuan (China), KX656036, KX656065, Rothfels, C. J., A. Larsson, L.-Y. Kuo, P. Korall, W.-L. Chiou, and KX656148, KX656091. Deparia deflexa (Kunze) L. Y. Kuo, M. Kato, & W. L. Chiou, Wade 1096 (TAIF), Java (Indonesia), JN673846, JN673948, JN673923, K. M. Pryer. 2012a. Overcoming deep roots, fast rates, and short – internodes to resolve the ancient rapid radiation of eupolypod II ferns. KX656118. Deparia confluens (Kunze) M. Kato, (cultivated in Koshikawa Systematic Biology 61: 490–509. Botanical Garden), Sumbawa (Indonesia), JN673824, JN673932, JN673907, Rothfels, C. J., M. A. Sundue, L.-Y. Kuo, A. Larsson, M. Kato, KX656092. Deparia conilii (Franch. & Sav.) M. Kato, TNS-768165 (TNS), Deparia E. Schuettpelz, and K. M. Pryer. 2012b. A revised family-level clas- Hachijo Is. (Japan), JN673825, AB574941, JN673867, KX656093. coreana (Christ) M. Kato, TNS-776382 (TNS), Aomori Pref. (Japan), sification for eupolypod II ferns (Polypodiidae: Polypodiales). Taxon JN673826, AB574942, JN673868, KX656094. Deparia dickasonii M. Kato, Liu 61: 515–533. 9433 (TAIF), Yunnan (China), JN673827, JN673933, JN673908, KX656095. Sano, R., M. Ito, S. Kurita, and M. Hasebe. 2000a. Deparia formosana Deparia dimorphophylla (Koidz.) M. Kato, TNS-764256 (TNS), Kagoshima (Rosenst.) R. Sano, a new name for Diplazium formosanum Rosenst. Pref. (Japan), JN673828, AB574943, JN673870, KX656096. Deparia dolosa Acta Phytotaxonomica et Geobotanica 51: 17–20. (Christ) M. Kato, Kuo 1315 (TAIF), Yunnan (China), JN673829, JN673934, Sano, R., M. Takamiya, M. Ito, S. Kurita, and M. Hasebe. 2000b. Phylogeny JN673909, KX656097. Deparia edentula (Kunze) X. C. Zhang, TNS-1112754 of the lady fern group, tribe Physematieae (Dryopteridaceae), based (TNS), Java (Indonesia), KX656037, KX656066, KX656149, KX656098. on chloroplast rbcL gene sequences. Molecular Phylogenetics and Evo- Deparia erecta (Z. R. Wang) M. Kato, Kuo 2219 (TAIF), Sichuan (China), lution 15: 403–413. KX656039, KX656068, KX656151, KX656100. Deparia fenzliana (Luers.) M. Sano, R., M. Takamiya, S. Kurita, M. Ito, and M. Hasebe. 2000c. Diplazium Kato, Oppenheimer H20920 (TAIF), Hawaii (USA), KX656040, –, KX656152, subsinuatum and Di. tomitaroanum should be moved to Deparia KX656101; Hasebe s.n. (TI), Hawaii (USA), –, D43900, –, –. Deparia formosana according to molecular, morphological, and cytological characters. – (Rosenst.) R. Sano, Kuo 2306 (TAIF), Yilan (Taiwan), KX656041, KX656069, Journal of Plant Research 113: 157 163. KX656153, KX656102. Deparia glabrata (Mett. ex Kuhn) M. Kato, P-01515373 Shinohara, W., T.-W. Hsu, S.-J. Moore, and N. Murakami. 2006. Genetic (P), Oloitia (Equatorial Guinea), KX656043, KX656071, KX656155, analysis of the newly found diploid cytotype of Deparia petersenii KX656104. Deparia gordonii (Baker) M. Kato, TNS-9527761 (TNS), Viti Levu (Woodsiaceae: Pteridophyta): Evidence for multiple origins of the – – – Deparia hainanensis 01385619 – (Fiji), , , KY296541, . (Ching) R. Sano, PE- tetraploid. International Journal of Plant Sciences 167: 299 309. (PE), Hainan (China), KX656044, KX656072, KX656156, KX656105. Deparia Sundue, M. A. and C. J. Rothfels. 2014. Stasis and convergence characterize henryi (Baker) M. Kato, Kuo 3953 (TAIF), Hubei (China), KY296506, morphological evolution in eupolypod II ferns. Annals of Botany 113: KY296515, KY296533, KY296524, Deparia heterophlebia (Mett. ex Baker) R. – 35 54. Sano, Liu 9426 (TAIF), Yunnan (China), KX656045, KX656073, KX656157, Tagawa, M. 1959. Coloured Illustrations of the Japanese Pteridophyta. KX656106. Deparia japonica (Thunb.) M. Kato, TNS-763869 (TNS), Ibaraki Osaka: Hoikusha. Pref. (Japan), JN673831, AB574945, JN673873, KX656107. Deparia jiu- Tzeng, Y.-H. 2002. Phylogenetic Relationships of Athyrioid Ferns Inferred lungensis (Ching) Z. R. Wang, TNS-763932 (TNS), Tokyo Metropolis (Ja- from Chloroplast DNA Sequences. M.S. thesis. Kaohsiung: National pan), JN673850, AB574956, AB575594, KX656115. Deparia kaalaana (Copel.) Sun Yat-Sen University. M. Kato, TNS-1191621 (TNS), Hawaii (USA), KY296507, KY296516, Wang, M.-L., Z.-D. Chen, X.-C. Zhang, S.-G. Lu, and G.-F. Zhao. 2003. KY296534, KY296525, Deparia kiusiana (Koidz.) M. Kato, TNS-764364 Phylogeny of the Athyriaceae: Evidence from chloroplast trnL-F re- (TNS), Nara Pref. (Japan), JN673832, AB574946, JN673874, KX656108. – gion sequences. Zhiwu Fenlei Xuebao 41: 416 426. Deparia lancea (Thunb.) Fraser-Jenk., Kuo 1914 (TAIF), Taipei (Taiwan), Wang, M.-L., H. Xu, and L. Zheng. 2006. Dryoathyrium erectum is a member JN673839, JN673941, JN673916, KX656109. Deparia 3lobatocrenata – of the genus Athyriopsis. Zhiwu Fenlei Xuebao 44: 204 210. (Tagawa) M. Kato, Kuo 3953 (TAIF), Cultivated (Japan), KY296508, Wang, Z.-R. 1982. Four new species of Athyriaceae from Emei Shan, KY296517, KY296535, KY296526. Deparia longipes (Ching) Shinohara, Liu – Sichuan. Zhiwu Fenlei Xuebao 20: 236 240. 9352 (TAIF), Yunnan (China), KX656046, KX656074, KX656158, KX656130. – Wang, Z.-R. 1999. Lunathyrium. Pp. 294 325 in Flora Reipublicae Popularis Deparia longipilosa Rakotondr., P-00835667 (P), Antsiranana (Madagascar), Sinicae vol. 3(2). Beijing: Science Press. MG722869*, MG722875*, MG722887*, MG722882* Deparia marginalis Wei, R., H. Schneider, and X.-C. Zhang. 2013. Toward a new circum- (Hilleb.) M. Kato, Oppenheimer H20917 (TAIF), Hawaii (USA), KX656047, –, scription of the twinsorus-fern genus Diplazium (Athyriaceae): A KX656159, KX656110; Kato H-21 (TI), Hawaii (USA), –, AB046981, –, –. molecular phylogeny with morphological implications and infrage- Deparia macdonellii (Bedd.) M. Kato, TNS-731529 (TNS), Sikyan (Pakistan), neric taxonomy. Taxon 62: 441–457. KY296509, KY296518, KY296536, KY296527. Deparia marojejyensis (Tar- Wei, R., Y.-H. Yan, A. J. Harris, J.-S. Kang, H. Shen, Q.-P. Xiang, and dieu) M. Kato, Bauret & Rouhan s.n. (P), Antsiranana (Madagascar), X.-C. Zhang. 2017. Plastid phylogenomics resolve deep relationships MG722867*, MG722873*, MG722885*, MG722880*. Deparia medogensis among eupolypod II ferns with rapid radiation and rate heteroge- (Ching & S. K. Wu) Z. R. Wang, Liu 9453 (TAIF), Yunnan (China), neity. Genome Biology and Evolution 9: 1646–1657. KX656048, KX656075, KX656160, KX656111. Deparia minamitanii Seriz., Zwickl,D.J.2006.GeneticAlgorithmApproachesforthePhylogenetic TNS-774852 (TNS), Miyazaki Pref. (Japan), JN673847, AB574948, JN673889, Analysis of Large Biological Sequence Datasets under the Maxi- KX656112. Deparia 3nakaikeana Fraser-Jenk., TNS-9507647 (TNS), Kath- mum Likelihood Criterion. Ph.D. thesis. Austin: The University of mandu (Nepal), MG722865*, –, MG722883*, MG722878*. Deparia okuboana Texas. (Makino) M. Kato, TNS-764345 (TNS), Shizuoka Pref. (Japan), JN673848, 2018] KUO ET AL.: DEPARIA INFRAGENERIC REVISION 655

AB574949, AB575587, KX656113. Deparia omeiensis (Z. R. Wang) M. Kato, auriculata (W. M. Chu & Z. R. Wang) Z. R. Wang, Deparia brevipinna Liu 9671 (TAIF), Sichuan (China), JN673849, JN673949, JN673924, (Ching & K. H. Shing ex Z. R. Wang) Z. R. Wang, Deparia dolosa (Christ) KX656114. Deparia otomasui (Sa. Kurata) Seriz., TNS-764339 (TNS), M. Kato, Deparia giraldii (Christ) X. C. Zhang, Deparia hirtirachis (Ching Kumamoto Pref. (Japan), JN673851, AB574950, JN673893, KX656116. ex Z. R. Wang) Z. R. Wang, Deparia jiulungensis (Ching) Z. R. Wang, Deparia parvisora (C. Chr.) M. Kato, P-00243925 (P), Marojejy (Madagascar), Deparia 3kanghsienense (Ching & Y. P. Hsu) Z. R. He, Deparia liangshanensis KX656049, KX656076, KX656161, KX656117. Deparia petersenii var. peter- (Ching ex Z. R. Wang) Z. R. Wang, Deparia ludingensis (Z. R. Wang & Li senii (Kuntze) M. Kato, Kuo 1922 (TAIF), Taipei (Taiwan), JN673852, Bing Zhang) Z. R. Wang, Deparia mucilagina (M. Kato) Nakaike, Deparia JN673950, JN673925, KX656119. Deparia petersenii var. yakusimensis (H. Ito) macdonellii (Bedd.) M. Kato, Deparia medogensis (Ching & S. K. Wu) Z. R. M. Kato, Kuo 1084 (TAIF), Yakushima (Japan), KY296510, KY296519, Wang, Deparia 3nanchuanense (Ching & Zheng Y. Liu) Z. R. He, Deparia KY296537, KY296528. Deparia polyrhizon (Baker) Seriz., US-2424570 (US), pycnosora (Christ) M. Kato, Deparia shennongensis (Ching, Boufford & K. H. Nuwara Eliya (Sri Lanka), MG722866*, MG722872*, MG722884*, Shing) X. C. Zhang, Deparia sichuanensis (Z. R. Wang) Z. R. Wang, Deparia MG722879*. Deparia prolifera (Kaulf.) Hook. & Grev., Wood 13449 (PTBG), sikkimensis (Ching) Nakaike & S. Malik, Deparia subsimilis (Christ) Fraser- Hawaii (USA), KX656050, –, KX656162, KX656120; Kato H-65 (TI), Hawaii Jenk., Deparia truncata (Ching ex Z. R. Wang) Z. R. Wang, Deparia vegetior (USA), –, D43906, –, –. Deparia pseudoconilii (Seriz.) Seriz., TNS-764016 (Kitag.) X. C. Zhang, Deparia vermiformis (Ching, Boufford & K. H. Shing) Z. (TNS), Okinawa Pref. (Japan), JN673853, AB574952, JN673895, KX656121. R. Wang, Deparia wilsonii (Christ) X. C. Zhang, Deparia wongzongrenii L. Y. Deparia pterorachis (Christ) M. Kato, TNS-766637 (TNS), Nagano Pref. Kuo, M. Kato, & W. L. Chiou. (Japan), JN673854, AB574954, JN673896, KX656122. Deparia pycnosora (Christ) M. Kato, Lu 14388 (TAIF), Changbai Mt. (China), KX656051, Sect. DRYOATHYRIUM 3 Sect. LUNATHYRIUM. Deparia 3kiyozumiana (Sa. KX656077, KX656163, KX656123. Deparia septentrionalis Rakotondr., Kurata) Shimura. P-00084929 (P), Marojejy (Madagascar), MG722868*, MG722874*, MG722886*, MG722881*. Deparia sichuanensis (Z. R. Wang) Z. R. Wang, Kuo Sect. ERECTUS. Deparia erecta (Z. R. Wang) M. Kato. 2243 (TAIF), Sichuan (China), KX656052, KX656078, KX656164, KX656124. Deparia subfluvialis (Hayata) M. Kato, Kuo 168 (TAIF), Nantu (Taiwan), Sect. DICTYODROMA. Deparia formosana (Rosenst.) R. Sano, Deparia hai- JN673857, JN673951, JN673926, KX656126. Deparia tenuifolia (Kirk) M. nanensis (Ching) R. Sano, Deparia heterophlebia (Mett. ex Baker) R. Sano, Kato, Perrie 6488 (WELT), North Island (New Zealand), –, KJ400018, Deparia yunnanensis (Ching) R. Sano. KJ400019, –. Deparia timetensis (E. Brown) M. Kato, Wood 10048 (PTBG), Marquesas (French Polynesia), KX656054, KX656080, KX656166, –. Sect. DEPARIA subsect. DEPARIA. Deparia bonincola (Nakai) M. Kato, Deparia 3tomitaroana (Masam.) R. Sano, TNS-771521 (TNS), Kochi Pref. Deparia cataracticola M. Kato, Deparia fenzliana (Luers.) M. Kato, Deparia (Japan), KY296512, KY296521, KY296539, KY296530. Deparia unifurcata kaalaana (Copel.) M. Kato, Deparia lancea (Thunb.) Fraser-Jenk., Deparia (Baker) M. Kato, Kuo 2197 (TAIF), Sichuan (China), KX656055, KX656081, otomasui (Sa. Kurata) Seriz., Deparia marginalis (Hilleb.) M. Kato, KX656167, KX656127. Deparia viridifrons (Makino) M. Kato, TNS-766472 Deparia prolifera (Kaulf.) Hook. & Grev. (TNS), Nara Pref. (Japan), JN673861, AB574959, JN673903, KX656128. Deparia wangzhongrenii L. Y. Kuo, M. Kato & W. L. Chiou, Liu 9703 (TAIF), Sect. DEPARIA subsect. CAESPITES. Deparia concinna (Z. R. Wang) M. Kato, Sichuan (China), KX656038, KX656067, KX656150, KX656099. Deparia Deparia dickasonii M. Kato, Deparia omeiensis (Z. R. Wang) M. Kato, Deparia wilsonii (Christ) X. C. Zhang, Kuo 2087 (TAIF), Sichuan (China), KX656056, minamitanii Seriz., Deparia polyrhizon (Baker) Seriz. KX656082, KX656168, KX656129. Deparia yunnanensis (Ching) R. Sano, Kuo 3283 (TAIF), Yunnan (China), KY296513, KY296522, KY296540, KY296531. Sect. DEPARIA subsect. ATHYRIOPSIS. Deparia abbreviata (W. M. Chu) Z. R. He, Deparia 3angustata (Nakaike) Nakaike, Deparia 3birii Fraser-Jenk., Appendix 2. Representative species in each Deparia section and Deparia biserialis (Baker) M. Kato, Deparia confluens (Kunze) M. Kato, subsection. Deparia conilii (Franch. & Sav.) M. Kato, Deparia deflexa (Kunze) L. Y. Kuo, M. Kato, & W. L. Chiou, Deparia dimorphophylla (Koidz.) M. Kato, Deparia Sect. DRYOATHYRIUM. Deparia boryana (Willd.) M. Kato, Deparia chinensis japonica (Thunb.) M. Kato, Deparia jinfoshanensis (Z. Y. Liu) Z. R. He, Deparia (Ching ex S. Y. Jin & Y. L. Chen) T. C. Hsu & L. Y. Kuo, Deparia confusa kiusiana (Koidz.) M. Kato, Deparia lushanensis (J. X. Li) Z. R. He, (Ching & Y. P. Hsu) Z. R. Wang, Deparia coreana (Christ) M. Kato, Deparia Deparia lasiopteris (Kunze) Nakaike, Deparia longipes (Ching) Shinohara, edentula (Kunze) X. C. Zhang, Deparia falcatipinnula (Z. R. Wang) Z. R. Deparia 3musashiensis (H. Ohba) Seriz., Deparia oldhamii (Hook. & Baker) Y. Wang, Deparia glabrata (Mett. ex Kuhn) M. Kato, Deparia gordonii (Baker) M. C. Oh & C. S. Lee, Deparia petersenii (Kuntze) M. Kato, Deparia pachyphylla Kato, Deparia henryi (Baker) M. Kato, Deparia longipilosa Rakotondr., Deparia (Ching) Z. R. He, Deparia pseudoconilii (Seriz.) Seriz., Deparia shandongensis marojejyensis (Tardieu) M. Kato, Deparia okuboana (Makino) M. Kato, (J. X. Li & Z. C. Ding) Z. R. He, Deparia tenuifolia (Kirk) M. Kato, Deparia Deparia parvisora (C. Chr.) M. Kato, Deparia pterorachis (Christ) M. Kato, timetensis (E. Brown) M. Kato. Deparia septentrionalis Rakotondr., Deparia setigera (Ching ex Y. T. Hsieh) Z. R. Wang, Deparia stenopterum (Christ) Z. R. Wang, Deparia subfluvialis Sect. DEPARIA subsect. DEPARIA 3 Sect. DEPARIA subsect. ATHYRIOPSIS. (Hayata) M. Kato, Deparia unifurcata (Baker) M. Kato, Deparia viridifrons Deparia 3lobatocrenata (Tagawa) M. Kato, Deparia 3tomitaroana (Masam.) R. (Makino) M. Kato. Sano, Deparia 3nakaikeana Fraser-Jenk., Deparia 3zeylanica (Hook.) M. Kato.

Sect. LUNATHYRIUM. Deparia acrostichoides (Sw.) M. Kato, Deparia acuta Sect. LUNATHYRIUM 3 Sect. DEPARIA subsect. ATHYRIOPSIS. Deparia 3 (Ching) Fraser-Jenk., Deparia allantodioides (Bedd.) M. Kato, Deparia togakushiensis Otsuka & Fujiw.