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Journal of Plant Research

, Volume 131, Issue 1, pp 67–76 | Cite as

End of an enigma: Aenigmopteris belongs in Tectaria (Tectariaceae: Polypodiopsida)

  • Cheng-Wei Chen
  • Carl J. Rothfels
  • Andi Maryani A. Mustapeng
  • Markus Gubilil
  • Dirk Nikolaus Karger
  • Michael Kessler
  • Yao-Moan Huang
Regular Paper

Abstract

The phylogenetic affinities of the fern genus Aenigmopteris have been the subject of considerable disagreement, but until now, no molecular data were available from the genus. Based on the analysis of three chloroplast DNA regions (rbcL, rps16-matK, and trnL-F) we demonstrate that Aenigmopteris dubia (the type species of the genus) and A. elegans are closely related and deeply imbedded in Tectaria. The other three species of genus are morphologically very similar; we therefore transfer all five known species into Tectaria. Detailed morphological comparison further shows that previously proposed diagnostic characters of Aenigmopteris fall within the range of variation of a broadly circumscribed Tectaria.

Keywords

Ctenitis Dryopteridaceae Fern Morphology Phylogeny Taxonomy 

Introduction

Our understanding of fern phylogeny has increased dramatically over the past 20 years, due in large part to the availability of molecular data and developments in analytical techniques to infer evolutionary relationships. This increased understanding has been reflected in updated classifications, most notably the seminal Smith et al. (2006) fern classification and the recently published Pteridophyte Phylogeny Group classification of ferns and lycophytes (PPG I 2016). Smith et al. (2006) highlighted areas of fern phylogeny that were still uncertain, and in the intervening decade between that classification and the PPG revision (PPG I 2016), the great majority of these outstanding questions have been resolved. These resolved relationships include those among the deeper “family-level” clades [e.g., related to Dryopteridaceae: Zhang and Zhang 2015; Lindsaeaceae: Lehtonen et al. 2012; and Woodsiaceae sensu Smith et al. (2006): Rothfels et al. 2012, Mynssen et al. 2016], and the placement of previously unsampled genera such as Cystoathyrium Ching (belongs in Cystopteris Bernh.; Wei and Zhang 2014), Pseudotectaria Tardieu-Blot [belongs in Ctenitis (C.Chr.) C.Chr.; Duan et al. 2017; Hennequin et al. 2017], Revwattsia D.L.Jones (belongs in Dryopteris Adans.; McKeown et al. 2012), and Adenoderris J.Sm. (one species belongs in Polystichum Roth and another in Dryopteris; McHenry et al. 2013). Of the 337 genera recognized by PPG I (2016), only four had not been included in molecular phylogenetic studies: Aenigmopteris Holttum and Dryopolystichum Copel. (both treated in Dryopteridaceae), Menisorus Alston (treated in Thelypteridaceae), and Thysanosoria A.Gepp (treated in Lomariopsidaceae). Subsequently, molecular data have placed Dryopolystichum within Lomariopsidaceae (Chen et al. 2017), leaving only three genera unsampled.

Aenigmopteris comprises five poorly collected species distributed in Malesia (Philippines, Borneo, and New Guinea). No member of the genus has yet been included in a molecular phylogenetic study, probably due to the paucity of available specimens. The genus name is derived from the Greek ainigma, a riddle, indicating the uncertainty of its relationship with other ferns (Holttum 1984). Its species were traditionally considered to be closely related to Ctenitis (C.Chr.) C.Chr (a genus now treated in Dryopteridaceae; PPG I 2016) due to the similarities of frond division patterns and the free venation (e.g., Copeland 1947), an opinion that was partially supported by Holttum in his description of Aenigmopteris (Holttum 1984). However, Holttum additionally highlighted a close affinity between Aenigmopteris and Tectaria Cav. (a genus now treated in Tectariaceae) because of the similarity of scales and indusia. After its establishment as a new genus by Holttum (1984), no additional arguments on the generic placement of Aenigmopteris have been made. Subsequent studies maintained Aenigmopteris as a distinct genus (e.g., Christenhusz et al. 2011; Kramer et al. 1990; PPG I 2016; Smith et al. 2006) but the disagreement about its phylogenetic placement persists. For example, Ding et al. (2014) treated Aenigmopteris within Dryopteridaceae based on the free venation, finely dissected fronds, and copious ctenitoid hairs, and this treatment was adopted by PPG I (2016), whereas Smith et al. (2006) and Christenhusz et al. (2011) recognized Aenigmopteris within Tectariaceae instead.

Here, we present the first phylogenetic analysis to include members of the genus, based on three chloroplast DNA regions (rbcL, rps16-matk, and trnL-F). Following the results of phylogenetic analyses, we re-examine the critical morphological characters of Aenigmopteris (e.g., frond division, venation, hairs, indusia, scales, and spores) that have classically been used to infer its phylogenetic placement. We then compare these characters both among the species of Aenigmopteris and with Tectaria sensu (Ding et al. 2014; Zhang et al. 2017).

Materials and methods

Phylogenetic analysis of Aenigmopteris

Total DNA was extracted from silica-dried leaf fragments of Aenigmopteris dubia (DNK 575) and A. elegans (Wade 4705, Fig. S1) collected from Mt. Pisog, Luzon, the Philippines and Mt. Kinabalu, Sabah, Malaysia, respectively, using a modified CTAB-Qiagen column protocol (Kuo 2015). In consideration of both resolving power and the ability to combine our data with previously published sequences, we selected three chloroplast DNA regions (rbcL, rps16-matK, and trnL-F) for amplification and sequencing. The rbcL gene was amplified with primers ESRBCL1F (Schuettpelz and Pryer 2007) and 1379R (Wolf et al. 1999). The matK gene, rps16-matK ORF (Song M, Kuo L-Y, Huiet L, Pryer KM, Rothfels CJ, Li FW unpublished), and rps16-matK intergenic spacer were amplified with primers Tec rps16 F1 and Tec matk R (Ding et al. 2014). The trnL intron and trnL-F intergenic spacer were amplified using the primers FernL 1Ir1 (Li et al. 2010) and F (Taberlet et al. 1991). The PCR amplifications and sequencing reactions were performed following Chen et al. (2013). The six newly generated sequences were deposited in GenBank (see Supplementary file).

To determine the approximate phylogenetic placement of Aenigmopteris, we first BLASTed our newly generated sequences against the GenBank nucleotide archive. At all three regions, the Aenigmopteris sequences were similar to those of Tectaria species. Therefore, we constructed a data matrix from all species of Tectaria and the closely related genus Triplophyllum that had sequences of all three regions available in GenBank. Our final data matrix contains 72 species, representing each of the four major clades of the genus (Ding et al. 2014). Three species of Pteridrys and one of Arthropteris were selected as the outgroup based on published phylogenies (Ding et al. 2014; Zhang et al. 2016).

The matrices for each region were aligned manually, based on visual inspection in AliView v1.18 (Larsson 2014); areas of ambiguous alignment were excluded from subsequent analyses. The loci were concatenated into a master alignment (and ambiguous areas excluded) with abioscripts v0.9.4 (Larsson 2010). From this alignment we inferred the optimal partitioning of the data, and the optimal substitution model for each data subset, using a greedy search and the small-sample correction to the Akaike information criterion (AICc) in PartitionFinder v2.1.1 (Guindon et al. 2010; Lanfear et al. 2012, 2017). For the PartitionFinder run, we provided the program with 11 data blocks: one for each codon position for each of the three coding regions (rbcL, matK, and the open reading frame in the rps16-matK spacer), one for the rps16-matK spacer, and one for trnL-F; PartitionFinder then inferred the optimal clusters of these blocks. Phylogenetic analyses were performed under maximum likelihood (ML) with Garli 2.01 (Zwickl 2006), using the PartitionFinder-derived partitioning scheme and substitution models. The search for the best tree was run 10 times, each from an independent random-addition sequence starting tree. Support was assessed by 960 bootstrap pseudoreplicates, also in Garli, under the same settings, but with each tree search performed from a single random-addition starting tree. These bootstrap analyses were performed online, in the CIPRES Science Gateway (Miller et al. 2010). Support was also assessed in a Bayesian framework, using MrBayes v3.2.6 (Ronquist et al. 2012). The data were partitioned according to the optimal PartitionFinder scheme (above), with each subset given a GTR model with gamma distributed site rates (+G) and/or a proportion of invariant sights (+I), depending on whether those components were in the optimal model for that subset, as determined above by PartitionFinder (Lanfear et al. 2017). Model parameters were unlinked across partitions, and each subset was permitted its own average rate. Four separate analyses were run under these settings, each with four chains (one cold, three heated), for 15 million generations, with the cold chain sampled every 5000 generations. The parameter trace files were inspected in Tracer v1.4 (Rambaut andDrummond 2007); each run converged within 1 million generations. Conservatively, the first 5 million generations were excluded from each run prior to pooling the four posterior samples; final effective sample sizes for each parameter were >6000. Bootstrap and posterior support values were mapped onto the ML tree using the sumtrees v3.3.1 command in the DendroPy v3.12.0 computing library (Sukumaran and Holder 2010).

Morphological examination of Aenigmopteris

In addition to our four new collections (DNK 575, DNK 619, Wade 4297, and Wade 4705), specimens of Aenigmopteris in UC were also used for morphological examination. In total, eight specimens representing three species [i.e., Aenigmopteris dubia, A. elegans, and A. pulchra (Copel.) Holttum] were examined (Table 1). We paid special attention on the characters considered diagnostic for the genus by Holttum (1984) including blade division, venation, scales, hairs, and indusial shape.

Table 1

Specimens examined in this study

Taxa

Voucher

Country

Herbarium

Aenigmopteris dubia (Copel.) Holttum

DNK 575

The Philippines

UC

Aenigmopteris dubia (Copel.) Holttum

DNK 619

The Philippines

UC

Aenigmopteris dubia (Copel.) Holttum

Edano 5950

The Philippines

UC

Aenigmopteris dubia (Copel.) Holttum

Elmer 9016

The Philippines

UC

Aenigmopteris elegans Holttum

Wade 4297

Malaysia

TAIF

Aenigmopteris elegans Holttum

Wade 4705

Malaysia

TAIF

Aenigmopteris pulchra (Copel.) Holttum

Brass 12848

Papua New Guinea

UC

Aenigmopteris pulchra (Copel.) Holttum

Kluge 9019

Papua New Guinea

UC

Tectaria fuscipes (Wall. ex Bedd.) C.Chr.

Hsu 2721

Taiwan

TAIF

Tectaria kusukusensis (Hayata) Lellinger

Lu 11021

Taiwan

TAIF

Tectaria multicaudata (C.B.Clarke) Ching

Lu s.n

Taiwan

TAIF

Tectaria psomiocarpa S.Y.Dong

Wade 4566

The Philippines

TAIF

Tectaria sagenioides (Mett.) Christenh.

Wade 1332

Vietnam

TAIF

Scales on the rhizome apex, costae, and indusia were transferred to slides and photographed with a digital camera (EOS 7D, Canon, Tokyo, Japan) under a light microscope (Leica, DMR, Wetzlar, Germany). Leaf fragments and spores were transferred to aluminum stubs and coated with gold, then examined by a tabletop scanning electron microscope (TM-3000, Hitachi, Ibaraki, Japan). To provide a point of comparison with Aenigmopteris, we additionally examined the spore morphology of selected species of Tectaria (Table 1).

Results

Phylogenetic analysis of Aenigmopteris

The final concatenated dataset comprises 3637 aligned sites (1219, 1999, and 419 from rbcL, rps16-matK, and trnL-F, respectively) and includes 11.6% missing data (5.7% gaps and 6.0% uncertain character states). The optimal partitioning scheme, as inferred by PartitionFinder, included seven data subsets (their corresponding models are listed in parentheses): rbcL codon position 2 (K81uf + I + G); rbcL position 3 (K81uf + G); rbcL position 1 (GTR + I + G); rps16-matK ORF position 2 (GTR + I); matK position 3 + rps16-matK ORF position 3 (TVM + G); rps16-matK ORF position 1 + matK position 1 + matK position 2 (GTR + I + G); and rps16-matK spacer + trnL-F (GTR + G). Combined, this scheme has 204 free substitution parameters. Under this model, the ML phylogeny found is generally well supported (Fig. 1), including strong support for the monophyly of Tectaria (including Aenigmopteris) and for each of the four major subclades within the genus previously identified by Ding et al. (2014). Aenigmopteris dubia and A. elegans are sister to each other and resolved deep within Tectaria; together they are weakly supported as sister to Tectaria psomiocarpa S.Y.Dong within Clade III of Ding et al. (2014). The newly generated sequences are available in GenBank (see Supplementary file), and the alignment and ML phylogeny are available in TreeBase (study # 20892).

Fig. 1

Phylogram of Aenigmopteris and relatives from maximum likelihood analysis of the concatenated plastid dataset (three loci; seven data partitions). A.: Arthropteris; P.: Pteridrys; Tr.: Triplophyllum; T.: Tectaria. Maximum likelihood bootstrap support values are above the branches; posterior support is below. Two asterisks indicate 100% bootstrap and 1.0 posterior support. Branches receiving >70% bootstrap support or >0.95 posterior support are thickened. The Aenigmopteris accessions are in bold-face type

Morphological examination of Aenigmopteris

A comparison of morphological characters of three Aenigmopteris species is presented in Figs. 2 and S2. In general, our observations are congruent with those of Holttum (1984). All three species have an ascending rhizome, which is scaly at the apex. The scales are brown to dark brown, and non-clathrate (Fig. S2A). The stipes are ungrooved, with the scales being similar to those on the rhizomes but smaller in size. The laminae are deltate, much longer than wide, with an herbaceous and soft or firm texture. The leaves are 2-pinnate-pinnatifid to 3-pinnate, with the distal pinnae and pinnules are connected by a narrow wing along the rachis and costa (Fig. S1). Venation of all three species is free and branched, with the veins stopping before the laminar margin. The veins in the basal basiscopic pinnule lobes arise mostly from the costules, rather than costae (Fig. S1).

Fig. 2

Spore SEM of three Aenigmopteris species and five Tectaria species from clade III sensu Ding et al. (2014). a Aenigmopteris dubia (Edano 5950). b Aenigmopteris elegans (Wade 4705). c Aenigmopteris pulchra (Brass 12848). d Tectaria fuscipes (Wall. ex Bedd.) C. Chr. (Hsu 2721). e Tectaria kusukusensis (Hayata) Lellinger (Lu 11021). f Tectaria multicaudata (Lu s.n.). g Tectaria psomiocarpa (Wade4566). h Tectaria sagenioides (Mett.) Christenh. (Wade1332). Scale bar 30 µm

There are non-clathrate scales present on the rachises and costae, similar but smaller than those of the rhizome apex and stipe (Fig. S2B). Ctenitoid hairs (articulate multicellular hairs with transverse cell walls) are present, in two different sizes: those on the adaxial surface of lamina are larger, whereas those on the abaxial costae and costules are smaller (Figs. S2C, S2D, S2E, S2F). Small spherical unicellular glands occur on the adaxial costae, costules, and veins. A bulbil is occasionally found on the rachis, in the axil of a pinna, in all the three species. Sori are terminal on veins, with firm-textured reniform to asymmetrically horseshoe-shaped indusia (Fig. S2G). Spores are monolete, with an irregularly spinulose, cristate, or fimbriate perine, sometimes forming areoles (Fig. 2).

Discussion

The composition of Tectariaceae and the relationships among the family’s constituent genera have been greatly clarified in recent years (Ding et al. 2014; Liu et al. 2007; Moran et al. 2014; Wang et al. 2014; Zhang et al. 2016, 2017). Pleocnemia C.Presl, long thought to be a “tectarioid” fern, is instead a member of Dryopteridaceae (Kuo et al. 2011; Lehtonen 2011; Liu et al. 2014), while the superficially similar Pteridrys C.Chr. and Ching was confirmed to be in Tectariaceae (Lehtonen 2011; Liu et al. 2014), and both Hypoderris R.Br. ex Hook. (including some species formerly treated within Tectaria; Moran et al. 2014) and Triplophyllum Holttum (Moran et al. 2014; Wang et al. 2014) are monophyletic and closely related to Tectaria. Among the genera that have often been segregated from Tectaria (e.g., Ctenitopsis Ching ex Tardieu and C.Chr., Fadyenia Hook., Cionidium T.Moore ex Houlston and T.Moore, Quercifilix Copel., Sagenia C.Presl, Heterogonium C.Presl) nearly all have been demonstrated to nest within Tectaria (Ding et al. 2014; Liu et al. 2007; Schuettpelz and Pryer 2007; Wang et al. 2014; Zhang et al. 2017); only Pseudotectaria Tardieu-Blot has been shown to nest within Ctenitis, in Dryopteridaceae (Duan et al. 2017; Hennequin et al. 2017). Finally, two Tectaria species were shown to be more closely related to Pteridrys than to Tectaria, and have been transferred to the recently described genera Draconopteris Li Bing Zhang and Liang Zhang and Malaifilix Li Bing Zhang and Schuettp. (Zhang et al. 2016). The position of Aenigmopteris was arguably the last remaining genus-level uncertainty in the family (Wang et al. 2014), and Aenigmopteris is one of very few genera anywhere in ferns that had not been sampled in a molecular phylogenetic study (PPG I 2016).

Our phylogenetic analyses unambiguously place Aenigmopteris within Tectaria sensu Ding et al. (2014) and Zhang et al. (2017) (Fig. 1). A close relationship of Aenigmopteris with Tectaria had previously been suggested by Holttum (1984, 1987), who noted that Aenigmopteris has nearly all the characters of Tectaria except: (1) the ultimate segments of the blades are very small; (2) the veins in the basal basiscopic pinnule lobes do not arise from the costae (but from costules); and (3) the indusia of distal sori are asymmetric. In the following paragraphs, we re-examine these putative diagnostic characters and other characters that have been used to infer the phylogenetic relationship of Aenigmopteris. We then further discuss these characters in the light of our newly inferred phylogeny and under a broadly circumscribed Tectaria.

The finely divided laminae of Aenigmopteris (2-pinnate-pinnatifid to 3-pinnate) is one of the most commonly invoked characters in favor of a close relationship with Ctenitis (e.g., Copeland 1947). Although most species of Ctenitis have a more dissected lamina (Kramer et al. 1990), less divided blades can be also found in Ctenitis, such as in C. sinii (Ching) Ohwi, which has a pinnate-pinnatifid frond (2-pinnate only at the basal pinna). Moreover, laminar division has been shown to be homoplastic in Tectaria (Ding et al. 2014; Zhang et al. 2017). In addition, our phylogenetic analyses resolved Aenigmopteris in the Ctenitopsis clade (sensu Ding et al. 2014), a clade comprised of mostly species with highly divided blades (2- to 3-pinnate).

Venation patterns have also been used as a diagnostic character to distinguish Ctenitis and Tectaria. For example, both Ching (1938) and Copeland (1947) accepted in Tectaria only the species with fully anastomosing venation and placed those species resembling Tectaria but with free or partly free venation into Ctenitopsis or Ctenitis, respectively. However, venation is homoplastic in Tectaria and the small genera separated from Tectaria mainly by venation differences (i.e., Camptodium Fée, Ctenitopsis, Fadyenia, Heterogonium, Lenda Koidz., Microbrochis C.Presl, Phlebiogonium Fée, and Psomiocarpa C.Presl) are embedded in Tectaria (Ding et al. 2014; Liu et al. 2007, 2014; Wang et al. 2014; Zhang et al. 2017). Venation was also proposed as a diagnostic feature of Aenigmopteris by Holttum (1984). Under his concept, Tectaria differed from most of the tectarioid genera (including Aenigmopteris) in having the basal basiscopic vein of a vein group arising from the costa, but not from the costule. However, as reported by Kaur (1978), this vein arises from the costule (rather the costa) in two Tectaria species [T. polymorpha (Wall. ex Hook.) Copel. and T. wightii (C.B.Clarke) Ching], providing further support that the venation of Aenigmopteris actually falls into the range of variation of Tectaria. Moreover, such variation is also observed within Aenigmopteris, where we found that although the veins in basal basiscopic lobes of pinnules mostly arise from the costules, as described by Holttum (1984), the veins can instead arise from the junction of the costa and costule, or, rarely, from the costa itself as illustrated in Flora Malesiana (Holttum 1991).

The sori and indusia are another two important characters used in fern taxonomy. In Tectaria, some small segregate genera have been separated by either their acrostichoid sori (i.e., Hemigramma Christ and Quercifilix), exindusiate sori (i.e., Amphiblestra C.Presl and Psomiocarpa), or different indusia shape (not round or reniform as in most Tectaria species; i.e., Cionidium, Dictyoxiphium Hook., and Luerssenia Kuhn ex Luerssen). All these genera have been shown to be embedded in Tectaria (Ding et al. 2014; Liu et al. 2007, 2014; Wang et al. 2014; Zhang et al. 2017). In contrast to the heterogeneous sorus/indusium morphology in a broadly circumscribed Tectaria, the diagnostic character of indusium shape in Aenigmopteris, as proposed by Holttum (1984; i.e., reniform but variously asymmetric distally), is rather slight and within the range of variation of Tectaria (Holttum 1991).

The ctenitoid hairs are another prominent character of Aenigmopteris, and earlier studies have shown this character to be shared with both Ctenitis and Tectaria (e.g., Holttum 1983). When segregating the subgenus Ctenitis from Dryopteris mainly based on the character of ctenitoid hairs, Christensen (1911) already noticed the similarity with Tectaria. In this study, we compared the ctenitoid hairs of Aenigmopteris, Ctenitis, and Tectaria, and were unable to discern any prominent differences among them (data not shown).

Non-clathrate scales are present at the rhizome apexes, stipes, rachises, costae, or sometimes costules in Aenigmopteris (Holttum 1984; Kramer et al. 1990, Figs. S2A, S2B). Holttum (1983) is probably the first to clearly distinguish Ctenitis and Tectaria by the character of scales; they are clathrate in the former but non-clathrate in the latter. In this study, we examined the scales of three Aenigmopteris species and our observation of non-clathrate scales was congruent with previous studies (Holttum 1984, Fig. S2), consistent with the inclusion of Aenigmopteris in Tectaria.

A diverse range of spore perine structures has been reported in Tectaria (Nayar and Devi 1964; Tryon and Lugardon 1990), including inflated folds, cristate wings, and echinate, echinulate, or fenestrate ornamentation. In this study, we examined five species placed in clade III sensu Ding et al. (2014) and heterogeneity was observed even in such a limited sample (Fig. 2). Finally, chromosome number is now known to differ between Ctenitis and Tectaria. The basal number of the former is 41 (e.g., Ctenitis eatonii (Baker) Ching in Tsai and Shieh 1984, Ctenitis decurrentipinnata (Ching) Ching in Kato 1999) and of the latter is 40 (reviewed in Ding et al. 2014). Unfortunately, we were unable to collect living material for chromosome squashes in this study. Future study is needed to confirm the chromosome number of Aenigmopteris.

Due to the paucity of available specimens, we were unable to examine two of the five Aenigmopteris species. Aenigmopteris katoi is known only from the holotype in K, whereas A. mindanaensis is known from the holotype in BO plus another duplicate in US. However, as described by Holttum (1984) when he published both names, the differences between these two species and A. elegans are minor. Specifically, Aenigmopteris katoi is distinguished from A. elegans by having more divided fronds and more rigid hairs on the adaxial lamina surface, whereas A. mindanaensis is distinguished by the presence of thick hairs on the abaxial surface of veins (Holttum 1984). As a result, we hypothesize that all five species are closely related, and that the morphological distinctiveness of each species needs further study.

Conclusion

Molecular phylogenetic analysis unambiguously resolved Aenigmopteris dubia and A. elegans in Tectaria. Consistent with this result, detailed morphological comparison further showed that the putative diagnostic characters of Aenigmopteris fall within the range of variation of Tectaria sensu Wang et al. (2014), Ding et al. (2014), and Zhang et al. (2017). We suggest the inclusion of Aenigmopteris in Tectaria and provide two replacement names and three new combinations under the latter.

Taxonomic treatment

Tectaria aenigma C.W.Chen and C.J.Rothf., nom. nov.

Dryopteris dubia Copel., Elmer, Leafl. Philipp. Bot. 1: 235. 1907.

Ctenitis dubia (Copel.) Copel., Gen. Fil. 124. 1947.

Aenigmopteris dubia (Copel.) Holttum, Blumea 30(1): 4. 1984.

Type: The Philippines. Luzon, Tayabas Prov., Lucban, Elmer 9016 (holo: MICH [MICH1190423]; iso: BO [BO1527634], GH [GH00112504], K [K000235996], L [L0050908], UC [UC697949], US [US00386226]).

Blocking name: Tectaria dubia (C.B.Clarke and Baker) Ching, Sinensia 2: 23, f. 5. 1931. The basionym of this name is Nephrodium cicutarium Baker var. dubium C.B.Clarke and Baker, rather than Aspidium dubium (C.B.Clarke and Baker) Bedd. as sometimes cited.

The new specific epithet recalls the former generic treatment (A. dubia is the type of Aenigmopteris), and the long-standing taxonomic puzzle posed by these plants.

Tectaria sabahensis C.W.Chen and C.J.Rothf., nom. nov.

Aenigmopteris elegans Holttum, Blumea 30(1): 8, f. 1b, c, pl. 1b. 1984.

Type: Malaysia. Sabah, Mt. Kinabalu, Parris and Croxall 9135 (holo: K [K000235986]).

Blocking name: Tectaria elegans Copel., Sargentia 1: 3. 1942.

Tectaria sabahensis is known only from Sabah, where it has been collected from Mt. Kinabalu and Mt. Trus Madi.

Tectaria katoi (Holttum) C.W.Chen and C.J.Rothf., comb. nov.

Aenigmopteris katoi Holttum, Blumea 30(1): 8, f. 1d. 1984.

Type: Indonesia. Kalimantan Selatan, Gunung Besar, M. Kato, Gen Murata and J. Mogea B3820 (holo: K [K000235991]).

Tectaria mindanaensis (Holttum) C.W.Chen and C.J.Rothf., comb. nov.

Aenigmopteris mindanaensis Holttum, Blumea 30(1): 7. 1984.

Type: The Philippines. Mindanao, Bukidnon Subprov., Ramos and Edaho BS 39139 (holo: BO [BO1258409]; iso: US [US00386227]).

Tectaria pulchra (Copel.) C.W.Chen and C.J.Rothf., comb. nov.

Dryopteris pulchra Copel., Univ. Calif. Publ. Bot. 18: 219. 1942.

Ctenitis pulchra (Copel.) Copel., Gen. Fil. 124. 1947.

Aenigmopteris pulchra (Copel.) Holttum, Blumea 30: 7. 1984.

Type: Indonesia. Irian Jaya Barat, Idenburg River, Brass 13455 (holo: MICH [MICH 1190477]; iso: BM [BM001048625], BO [not found], BRI [AQ0024572], FI [FI004139], GH [GH00021146], L [L0051175]).

Notes

Acknowledgements

We are grateful to the curators and staff of the TAIF and UC herbaria for providing access to their collections. Alan Smith, Michael Sundue, and four anonymous reviewers provided valuable comments on an earlier draft of this manuscript. We also thank Wita Wardani for checking specimens at BO. For the fieldwork in Sabah, we thank the Sabah Biodiversity Centre, Sabah Forestry Department, and Sabah Parks for permission and collecting permits. Wei-Hsiu Wu, Pi-Fong Lu, and the staff of SNP (Sabah National Park) Herbarium provided important assistance in the field. For the fieldwork in Luzon, we thank the officials of the Department of Environment and Natural Resources (DENR) and Torrey Rodgers for logistical support.

Supplementary material

10265_2017_966_MOESM1_ESM.pdf (377 kb)
Supplementary material 1 (PDF 376 KB)
10265_2017_966_MOESM2_ESM.xlsx (16 kb)
Supplementary material 2 (XLSX 15 KB)

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Copyright information

© The Botanical Society of Japan and Springer Japan KK 2017

Authors and Affiliations

  1. 1.Division of SilvicultureTaiwan Forestry Research InstituteTaipeiTaiwan
  2. 2.University Herbarium and Department of Integrative BiologyUniversity of CaliforniaBerkeleyUSA
  3. 3.Forest Research CentreSabah Forestry DepartmentSandakanMalaysia
  4. 4.Institute of Systematic BotanyUniversity of ZürichZurichSwitzerland
  5. 5.Swiss Federal Research Institute WSLBirmensdorfSwitzerland

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