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The inclusion of Acrophorus, Diacalpe, Nothoperanema, and Peranema in Dryopteris: The molecular phylogeny, systematics, and nomenclature of Dryopteris subg. Nothoperanema (Dryopteridaceae)

Authors:
  • Kunming Institute of Botany,Chinese Academy of Sciences,Kunming,China

Abstract and Figures

Dryopteris (Dryopteridaceae) is one of the largest fern genera containing about 300 or more species. Sixty-five accessions representing all four subgenera and all 19 sections of Dryopteris recognized in current classifications, more than two-thirds of the species of Acrophorus, Diacalpe, Nothoperanema, and Peranema, three species of Arachniodes, three species of Cyrtomium, one species of Phanerophlebia, and two species of Polystichum, were sampled as ingroup in this study. Two species of Polystichopsis were used as outgroups. DNA sequences of f ive plastid loci ( psbA-trnH spacer, rbcL gene, rps4-trnS spacer, trnL intron, trnL-F spacer) were used to infer the phylogeny of Dryopteris and related genera. Our study clearly demonstrated that the currently defined Dryopteris is paraphyletic in relation to a clade containing the monophyletic Acrophorus, Diacalpe, Nothoperanema, and Peranema. Peranema is resolved as sister to the remaining three genera, followed by Nothoperanema which in turn is sister to the Acrophorus + Diacalpe clade, but this relationship received low support. Three out of the four subgenera of Dryopteris recognized in current classifications are not recovered as monophyletic. Dryopteris subg. Nothoperanema, well supported as monophyletic by molecular and morphological data, is resurrected and re-circumscribed to contain species of the currently accepted genera Acrophorus, Diacalpe, Nothoperanema, and Peranema. Twenty-seven species are recognized and classified into four sections based on molecular and morphological evidence. Included in this treatment are 25 new combinations, names, species, and statuses, and neotypification or lectotypification of 14 names. The present study further located and cited types of an additional 28 related names, many of which have been unknown to science. Keys to sections and species and distributional information are given and nomenclatural issues are discussed. This paper also synonymized and excluded 33 nomenclaturally confusing names of Dryopteris that were formerly assigned to Acrophorus or Diacalpe.
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INTRODUCTION
The fern genus Dryopteris Adans. (Dryopteridaceae)
is among the most common and species-rich fern genera in
tropical, temperate, and alpine/boreal regions. Estimates of
the number of species in Dryopteris have ranged from 225
(Fraser-Jenkins, 1986) to 300 (Lu, 1993). Dryopteris is a nearly
cosmopolitan genus and species of Dryopteris occur on every
continent and on a number of oceanic islands (e.g., Hawaiian
Islands) except the Antarctic (Fraser-Jenkins, 1986). Although
its highest diversity is clearly found in the Sino-Japanese
and Sino-Himalayan regions and neighboring areas in Asia
(Fraser-Jenkins, 1986; Iwatsuki, 1995; Wu & al., in press),
Dryopteris appears to have well diversified in every major
region of the world (Fraser-Jenkins, 1986) with seven species
in West Africa (Rou x, 2003), 11 species in sub-Saharan Africa
(Roux, 2002), 11 species in Madagascar and neighboring Indian
Ocean islands, includi ng Saint Paul (Roux, 2011), 10 species in
Sri Lanka (Sledge, 1973), 10 species in the Hawaiian Islands
(Palmer, 2003), 13 species in Mexico (Mickel & Smith, 2004),
14 species in North America north of Mexico (Montgomery
& Wagner, 1993), 22 species in Europe (Blockeel, 2006),
57 species in the Indian subcontinent (Fraser-Jenkins, 1989),
61 species in Japan (Iwatsu ki, 1995), and ca. 160 species know n
from China (Wu & al., in press).
Fraser-Jenkins (1986) has conducted the most intensive
taxonomic study in Dryopteris worldwide, partly on the basis
of early work conducted by Itô (1935, 1936) on the Japanese
species and by Ching (1938) on the species in China and the
Himalaya and neighboring areas. Fraser-Jenkins (1986) recog-
nized 225 species that he divided into four subgenera and three
of them further into 16 sections. Wu & Lu (2000) classified
the then known 127 Chinese species of Dryopteris in three
subgenera, and two of them further into 16 sections. Two of
the 16 sections recognized by Wu & Lu (2000) correspond to
two of the three sections proposed by Lu (D. sect. Caespitosae
S.G. Lu, 1990a; D. sect. Chrysocomae S.G. Lu, 1990b; D. sect.
Indusiatae S.G. Lu, 1999).
There has been much debate and confusion regarding the
circumscription of Dryopteris and the evolutionary relation-
ships among taxa, especially when it comes to relationships
between D. subg. Nothoperanema Tagawa and Peranemataceae
sensu Ching (1978; i.e., Acrophorus C. Presl, Diacalpe Blume,
and Peranema D. Don). Tagawa (1938) originally described
The inclusion of Acrophorus, Diacalpe, Nothoperanema, and
Peranema in Dryopteris: The molecular phylogeny, systematics, and
nomenclature of Dryopteris subg. Nothoperanema (Dryopteridaceae)
Li-Bing Zhang1,2 & Liang Zhang1
1 Chengdu Institute of Biolog y, Chinese Academy of Sciences, P.O. Box 416, Chengdu, Sichuan 610041, P. R. China
2 Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166-0299, U.S.A.
Author for correspondence: Li-Bing Zhang, Libing.Zhang@mobot.org
Abstract
Dryopteris (Dryopteridaceae) is one of the largest fern genera containing about 300 or more species. Sixty-five
accessions representing all four subgenera and all 19 sections of Dryopteris recognized in current classifications, more than
two-thirds of the species of Acrophorus, Diacalpe, Nothoperanema, and Peranema, three species of Arachniodes, th ree spe-
cies of Cyrtomium, one species of Phanerophlebia, and two species of Polystichum, were sampled as ingroup in this study.
Two species of Polystichopsis were used as outgroups. DNA sequences of five plastid loci (psbA-trnH spacer, rbcL gene,
rps4-trnS spacer, trnL intron, trnL-F spacer) were used to infer the phylogeny of Dryopteris and related genera. Our study
clearly demonstrated that the currently defined Dryopteris is paraphyletic in relation to a clade containing the monophyletic
Acrophorus, Diacalpe, Nothoperanema, and Peranema. Peranema is resolved as sister to the remaining three genera, fol-
lowed by Nothoperanema which in turn is sister to the Acrophorus + Diacalpe clade, but this relationship received low sup-
port. Three out of the four subgenera of Dryopteris recognized in current classifications are not recovered as monophyletic.
Dryopteris subg. Nothoperanema, well supported as monophyletic by molecular and morphological data, is resurrected and
re-circumscribed to contain species of the currently accepted genera Acrophorus, Diacalpe, Nothoperanema, and Peranema.
Twenty-seven species are recognized and classified into four sections based on molecular and morphological evidence.
Included in this treatment are 25 new combinations, names, species, and statuses, and neotypification or lectotypification
of 14 names. The present study further located and cited types of an additional 28 related names, many of which have been
unknown to science. Keys to sections and species and distributional information are given and nomenclatural issues are
discussed. This paper also synonymized and excluded 33 nomenclaturally confusing names of Dryopteris that we re for merly
assigned to Acrophorus or Diacalpe.
Keywords
Acrophorus; Diacalpe; Dryopteris subg. Nothoperanema; nomenclature; Nothoperanema; Peranema; phylogeny;
subgeneric classification
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the taxon Nothoperanema as a subgenus of Dryopteris. Ching
(1966) elevated it to a genus and lectotypified it with N. squa-
misetum (Hook.) Ching (= D. squamiseta (Hook.) Kuntze).
Nothoperanema has been accepted as a genus by a number of
pteridologists (e.g., Pichi Sermolli, 1977; Ching, 1978; Kuo,
1985; Wu & Ching, 1991; Hsieh, 2000; Roux, 2011). In contrast,
Itô (1939), Copeland (1947), and Ohwi (1957) regarded it as part
of Ctenitis (C. Chr.) C. Chr. Smith & al. (2006) and Christen-
husz & al. (2011) treated it as part of Dryopteris partly based
on Geiger & Ranker’s (2005) finding that Nothoperanema ru-
biginosum (Brack.) A.R. Sm. & D.D. Palmer is nested within a
paraphyletic Dryopteris based on DNA sequences of the plastid
rbcL gene and trnL-F intergenic spacer.
Using DNA sequences of the plastid rbcL gene, Li & Lu
(2006a) resolved Nothoperanema (four species sampled) as
paraphyletic in relation to Acrophorus (two species sampled),
Diacalpe (two species sampled), and Peranema (one species
sampled) with low branch support values. Based on evidence
of the plastid rps4-trnS intergenic spacer, Li & Lu (2006b)
found that Nothoperanema (three species sampled) was again
resolved as paraphyletic but in relation to Dryopteris eryth-
rosora (D.C. Eaton) Kuntze with high branch support values.
In contrast to Li & Lu’s (2006a, b) findings, based on DNA
sequences of plastid atpB and rbcL genes, Liu & al. (2007)
discovered that Nothoperanema (three species sampled) was
well supported as monophyletic and was embedded within a
paraphyletic Peranemataceae sensu Ching (1978). Using DNA
sequences of seven plastid loci, Sessa & al. (2012) provided
evidence that Notho peranema (one species sampled) should be
part of Dryopteris.
It has been clear that Acrophorus, Diacalpe, Nothoper-
anema, and Peranema are closely related to Dryopteris, but
detailed relationships among these five currently recognized
genera have been unclear and previous results have been con-
flicting. Also, previous studies may have failed to sample
enough taxa and/or enough molecular markers to resolve rela-
tionships, and no study has specifically targeted the relation-
ships among these five genera.
The goals of this study included (1) to test the monophyly
of each of Acrophorus, Diacalpe, Dryopteris, Nothoperanema,
Peranema, and Peranemataceae; (2) to clarify the relationships
among Dryopteris, Nothoperanema, and Peranemataceae
(Acrophorus, Diacalpe, Peranema); (3) to re-define Dryopteris
subg. Nothoperanema based on molecular and morphological
evidence and to investigate if this subgenus should be recog-
nized; and (4) to conduct a systematic and nomenclatural study
of the subgenus.
MATERIALS AND METHODS
Taxon sampling for the molecular study. —
Twenty-five
species of Dryopteris representing all four subgenera and all
16 sections recognized by Fraser-Jenkins (1986) and all three
additional sections (D. sect. Caespitosae, D. sect. Chrysoco-
mae, D. sect. Indusiatae) recognized by Lu (1990a, b, 1999)
and partly by Wu & Lu (2000) were sampled. The 25 species
of Dryopteris sampled, together with their subgeneric and
sectional assignments following Fraser-Jenkins (1986) and Lu
(1990a, b, 1999), are listed in Table 1.
We sampled eight accessions representing six (50%) of ca.
12 species of Acrophorus, seven accessions representing four
(50%) of eight species of Diacalpe, 13 accessions represent-
ing seven (88%) of eight species of Nothoperanema, and three
accessions representing both species of the bitypic Peranema.
Type species of all these four genera are included.
We also sampled three species of Arachniodes Blume,
three species of Cyrtomium C. Presl, one species of Phanero-
phlebia C. Presl, and two species of Polystichum Roth (all in
Dryopteridaceae) based on Liu & al. (2007) and Sessa & al.
(2012) where Arachniodes was resolved as sister to a clade
consisting of Acrophorus, Acrorumohra (H. Itô) H. Itô, Dia-
calpe, Dryopsis Holttum & P. J. Edwards, Dryopteris, Noth-
operanema, and Peranema, followed by a clade consisting of
Cyrtomium, Phanerophlebia, and Poly stichum. Two species of
Polystichopsis (J. Sm.) Holttum were used as outgroups based
on Sessa & al. (2012) where Poly stichopsis, together with Poly-
botrya Humb. & Bonpl. ex Willd. and Olfersia Raddi., was re-
solved as sister to a clade containing Arachniodes, Cyrtomium,
Dryopteris, Phanerophlebia, and Polystichum. In total, 67 ac-
cessions representing 65 ingroup and two outgroup species
were sampled. All sequences used in this study together with
their GenBank accession numbers and/or voucher information
are listed in the Appendix.
DNA sequencing. —
Total genomic DNA was extracted
from silica-gel-dried material or sometimes from herbarium
specimens using Plant Genomic DNA Kits (TIANGEN Bio-
Tech., Beijing, China). The PCR protocols followed Zhang
& al. (2001) and Ebihara & al. (2010). DNA sequence data
were obtained for five plastid regions, psbA-trnH spacer, rbcL
gene, rps4-trnS spacer, trnL intron, and trnL-F spacer. The
psbA-trnH spacer was amplified with psbA-Fn1 and tr n H-Rn2
(Ebihara & al., 2010). The rbcL gene was amplified with prim-
ers F1 (Fay & al., 1997) and 1379R (originally designed by
G. Zurawski and modified by Wolf & al., 1999). The primers
for amplifying rps4-trnS intergenic spacer were derived from
Souza-Chies & al. (1997) and Li & Lu (2006b). The trnL intron
and trnL-F intergenic spacer were amplified using primers
fern 1 (Trewick & al., 2002) and universal primer f of Taberlet
& al. (1991). Amplified fragments were purified with TIAN-
quick Mini Pur ification Kits (T IANGEN). Purif ied PCR prod-
ucts were sequenced by Invitrogen (Shanghai, China).
Additional sequences were obtained from GenBank and
had originally been generated by Geiger & Ranker (2005), Li
& Lu (2006a, b), Ebihara & al. (2010), Sessa & al. (2012), etc.
In total, 44, 64, 44, 33, and 54 sequences of psbA-trnH, rbcL,
rps4-trnS, trnL, and trnL-F, respectively, were included in our
analyses.
Data analysis. —
The preliminary alignments of psbA-
trnH spacer, rbcL gene, rps4-trnS spacer, trnL intron, and
trnL-F spacer data were obtained using the default alignment
parameters in Clustal X v.1.83 (T hompson & al., 1997) followed
by manual adjustments. Gap characters were coded as missing
data. Final alignment is available as supplementary data
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Table 1.
List of species of Dryopteris included in the current study and their subgeneric and sectional assignments following Fraser-Jenkins (1986) and Lu (1990a, b, 1999) classifications.
Species
Subgeneric assignment
(Fraser-Jenkins, 1986)
Sectional assignment
(Fraser-Jenkins, 1986)
Sectional assignment
(Lu, 1990a, b, 1999)
Dryopteris aemula (Aiton) Kuntze subg. Dryopteris sect. Aemulae Fraser-Jenk. N/A
D. affinis (Lowe) Fraser-Jenk. subg. Dryopteris sect. Fibrillosae Ching N/A
D. amurensis Christ subg. Dryopteris sect. Lophodium (Newman) C. Chr. ex H. Itô same
D. aquilinoides (Desv.) C. Chr. subg. Dryopteris sect. Marginatae Fraser-Jenk. N/A
D. atrata (Wall) Ching subg. Dryopteris sect. Hirtipedes Fraser-Jenk. same
D. chrysocoma (Christ) C. Chr. subg. Dryopteris sect. Pandae Fraser-Jenk. sect. Chrysocomae S.G. Lu
D. cinnamomea (Cav.) C. Chr. subg. Dryopteris sect. Cinnamomeae Fraser-Jenk. N/A
D. corleyi Fraser-Jenk. subg. Dryopteris sect. Remotae Fraser-Jenk. N/A
D. erythrosora (D. Eaton) Kuntze subg. Erythrovariae (H. Itô) Fraser-Jenk. sect. Erythrovariae same
D. expansa (C. Presl) Fraser-Jenk. & Jermy subg. Dryopteris sect. Lophodium same
D. filix-mas (L.) Schott subg. Dryopteris sect. Dryopteris same
D. fragrans (L.) Schott subg. Dryopteris sect. Dryopteris sect. Caespitosae S.G. Lu
D. futura A.R. Sm. subg. Nephrocystis (H. Itô) Fraser-Jenk. sect. Purpurascentes Fraser-Jenk. N/A
D. glabra (Brack.) Kuntze unplaced unplaced N/A
D. guanchica Gibby & Jermy subg. Dryopteris sect. Lophodium N/A
D. gymnosora (Makino) C. Chr. subg. Erythrovariae sect. Erythrovariae sect. Indusiatae S.G. Lu
D. hasseltii (Blume) C. Chr. subg. Nephrocystis sect. Nephrocystis N/A
D. hawaiiensis (Hillebr.) W.J. Rob. subg. Dryopteris sect. Fibrillosae Ching N/A
D. polita Rosenst. subg. Erythrovariae sect. Politae Fraser-Jenk. sect. Nephrocystis, placed in subg. Dryopteris
D. rubrobrunnea W.M. Chu subg. Dryopteris sect. Splendentes Fraser-Jenk. same
D. sieboldii (T. Moore) Kuntze subg. Pycnopteris (T. Moore) Ching N/A N/A
D. sparsa (Buch.-Ham. ex D. Don) Kuntze subg. Nephrocystis sect. Nephrocystis same, but placed in subg. Dryopteris
D. tokyoensis (Matsum. & Makino) C. Chr. subg. Dryopteris sect. Pandae Fraser-Jenk. same
D. uniformis (Makino) Makino subg. Dryopteris sect. Pallidae Fraser-Jenk. same
D. varia (L.) Kuntze subg. Erythrovariae sect. Variae Fraser-Jenk. same
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Equally weighted maximum parsi mony (MP) tree sea rches
were conducted for each data matrix using 1000 tree-bisection-
reconnection (TBR) searches in PAUP* v.4.0b10 (Swofford,
2002) with MAXTREES set to increase without limit. Parsi-
mony jackknife (JK) analyses (Farris & al., 1996) were con-
ducted using PAU P* with the removal probability set to approx-
imately 37%, and “jac” resampling emulated. One thousand
replicates were performed with 10 TBR searches per replicate
and a maximum of 100 trees held per TBR search. In addition
to the analyses of the four individual regions, MP and ML
analyses of the combined trnL intron and trnL-F spacer were
also conducted since these two linked regions are sometimes
viewed as one locus.
We used jModelTest v.0.1.1 (Posada, 2008) using PhyML
(Guindon & Gascuel, 2003) to select the best-fitting likelihood
model for maximum likelihood (ML; Felsenstein, 1985) analy-
ses. The Akaike information criterion (Akaike, 1974) was used
to select among models instead of the hierarchical likelihood ra-
tio test, following Pol (2004) and Posada & Buckley (2004). The
models selected were GTR + G (for the simultaneous analysis of
all genes; Nixon & Carpenter, 1996), SYM + I + G (rbcL gene),
TIM3 + G (rps4-trnS spacer), TPM1uf + G (psbA-trnH spacer,
trnL intron), TPM2uf + G (trnL-F spacer), and TVM + G (trnL
intron & trnL-F spacer). The selected models and parameters
estimated (Table 2) were then used for tree searches from the
respective data partitions. Two hundred ML jackknife repli-
cates were performed with one TBR search per replicate and a
maximum of 100 trees held per TBR search.
The simultaneous ML analyses of all nucleotide charac-
ters and ML bootstrapping (BS) were repeated five times with
random but different starting seeds using RAxML-HPC2 on
Tetragrid v.7.2.8 (Stamatakis & al., 2008; Miller & al., 2010;
available at http://www.phylo.org/) with 400 bootstrap analyses
followed by a search for the best-scoring tree in a single run.
The total 5 × 400 = 2000 ML bootstrap analyses were then
combined to calculate the values of branch support. The five
best-scoring trees in the five single runs generated the same
topology (Fig. 1).
Taxonomic methods. —
The protologues and nomencla-
tural types of related names were examined. Herbarium speci-
mens of related species in the following herbaria were inspected
via personal visits, online resources (e.g., JSTOR Plant Science,
http://plants.jstor.org), or images provided by herbaria: AK,
BISH, BM, CANB, CDBI, FI, GOET, HENU, HIB, HITBC,
HNWP, HUH, IBK, ISBC, K, KUN, KYO, L, LBG, MICH,
NAS, P, PE, PR, PRC, TAIF, TI, UC, US, and WUG. Nomencla-
tural treatments follow the Vienna Code (McNeill & al., 2006).
RES ULTS
Analyses of individual plastid regions. —
The character-
istics and statistics of the five individual plastid regions from
the MP and ML analyses are presented in Table 3. The five
individual plastid regions as well as the combined trnL intron
and trnL-F spacer yielded similar tree topologies in both MP
and ML analyses (trees not shown). The most parsimonious,
parsimony JK, and likelihood JK and BS trees for all analy-
ses are available upon request. There were no well-supported
( ≥ 70% JK or BS support; Zhang & Simmons, 2006) clades
that conflicted with one another in both the parsimony JK and
likelihood BS trees, therefore, the five plastid regions were
combined for analysis.
Analyses of combined plastid data. —
The combined
data matrix of five plastid regions consisted of 4265 bases. A
combined analysis (Kluge, 1989; Nixon & Carpenter, 1996)
of nucleotides from all plastid regions was conducted as the
primary basis for phylogenetic inference.
Equally weighted MP analysis of the combined dataset
generated 125,840 most parsimonious trees with a length of
1688 steps, a consistency index (CI; Kluge & Farris, 1969) of
0.6742, and a retention index (RI; Farris, 1989) of 0.8122. The
ML analysis generated one optimal tree which is shown in
Fig. 1. The tree topology of the MP analysis was similar to that
of the ML analysis and there were no well-supported conflicts
between the two trees.
Table 2.
Best-fitting models and parameter values for separate (psbA-trnH, rbcL, rps4-trnS, trnL, trnL-F, trnL & trnL-F) and simultaneous plastid
datasets in this study. “
Region
AIC
selected
model
Base frequencies Substitution model (rate matrix)
IGAC G TA–C A–G A–T C–G C–T G–T Ti/tv
psbA-trnH spacer TPM1uf+G 0.2810 0.2139 0.2076 0.2975 1.0000 4.2917 0.0673 0.0673 4.2917 1.0000 – 0 0.4420
rbcL gene SYM+I+G –––– 2.0167 9.6688 1.1318 0.5917 16.6965 1.0000 0.3650 0.3550
rps4-trnS spacer TIM3+G 0.3243 0.1827 0.1946 0.2984 1.3810 6.8605 1.0000 1.3810 8.5716 1.0000 – 0 2.0480
trnL intron TPM1uf+G 0.3208 0.1855 0.2109 0.2828 1.0000 4.4808 0.3419 0.3419 4.4808 1.0000 – 0 0.6080
trnL-F spacer TPM2uf+G 0.3224 0.1981 0.1786 0.3010 0.3565 3.8346 0.3565 1.0000 3.8346 1.0000 0 0.5990
trnL intron & trnL-F spacer TVM+G 0.3196 0.1853 0.1984 0.2968 0.9923 4.8280 0.2903 0.8703 4.8280 1.0000 – 0 0.5850
Simultaneous GTR+G 0.2975 0.2019 0.2180 0.2826 1.3718 6.1826 0.5931 0.7235 8.2352 1.0000 – 0 0.3210
Abbreviations used in column headers and selected models: AIC, Akaike information criterion; G, = gamma distribution shape parameter (Yang,
1994); GTR, general-time-reversible model (Tavaré, 1986); I, proportion of invariable sites; SYM, symmetrical model (Zharkikh, 1994); Ti/Tv,
transition/transversion ratio; TIM, transitional model (Posada, 2003); TPM, Kimura 3-parameter model (K81; Kimura, 1981); TVM, transversional
model (Posada, 2003).
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0.1
Polystichopsis pubescens
Polystichopsis muscosa
Arachniodes denticulata
Arachniodes rhomboidea
Arachniodes aristata
Dryopteris fragrans
Dryopteris amurensis
Dryopteris expansa
Dryopteris sparsa
Dryopteris tokyoensis
Dryopteris futura
Dryopteris cinnamomea
Nothoperanema sp.
Nothoperanema hendersonii
Nothoperanema shikokianum
Nothoperanema shikokianum
Nothoperanema hendersonii
Nothoperanema hendersonii
Nothoperanema hendersonii
Nothoperanema hendersonii
Nothoperanema hendersonii
Nothoperanema squamisetum
Nothoperanema squamisetum
Nothoperanema diacalpioides
Nothoperanema rubiginosum
Acrophorus macrocarpus
Acrophorus nodosus
Acrophorus emeiensis
Acrophorus exstipellatus
Acrophorus paleolatus
Acrophorus paleolatus
Acrophorus sp.
Acrophorus paleolatus
Diacalpe chinensis
Diacalpe aspidioides
Diacalpe aspidioides
Diacalpe christensenae
Diacalpe christensenae
Diacalpe annamensis
Diacalpe annamensis
Peranema luzonica
Peranema cyatheoides
Peranema luzonica
Dryopteris guanchica
Dryopteris glabra
Dryopteris hawaiiensis
Dryopteris aemula
Dryopteris corleyi
Dryopteris gymnosora
Dryopteris erythrosora
Dryopteris varia
Dryopteris hasseltii
Dryopteris polita
Dryopteris aquilinoides
Dryopteris chrysocoma
Dryopteris uniformis
Dryopteris atrata
Dryopteris filix-mas
Dryopteris affinis
Dryopteris sieboldii
Dryopteris rubrobrunnea
Polystichum munitum
Polystichum andersonii
Phanerophlebia nobilis
Cyrtomium falcatum
Cyrtomium macrophyllum
Cyrtomium fortunei
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100
92
95 96
95
57
73
93
99
89
90
98
100
56
85
98
99
61
64
60
66
/
51
100
100
Dryopteris
Dryopteris subg.
Nothoperanema
Nothoperanema
Acrophorus
Diacalpe
Peranema
Dryopteris
A
B
C
D
Dryopteris subg. Erythrovariae
Dryopteris subg. Dryopteris
Dryopteris subg. Dryopteris
Nothoperanema clade
Dryopteris subg. Pycnopteris
Dryopteris subg. Dryopteris
Dryopteris subg. Nephrocystis
unplaced
G
Dryopteris subg. Nephrocystis
E
F
H
J
Fig. 1.
Simultaneous-analysis maximum likelihood tree with parsimony jackknife values above branches, and maximum likelihood bootstrap
values below branches. If a clade was resolved in one analysis but not the other, “/ ” is used to indicate in which analysis that clade was not
resolved. The bar indicates the substitution rate per site. The dashed branch between Polystichopsis and the remaining taxa indicates the dis-
proportional branch length. The subgeneric classification follows Fraser-Jenkins (1986). The species in bold face are those that are currently not
included in Dryopteris but resolved as members of Dryopteris in this study. A–H & J indicate clades discussed in the text.
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DISCUSSION
Monophyly and subgeneric classification of Dryopteris.
Our results suggest that Dryopteris as currently defined
is paraphyletic in relation to a clade containing Acrophorus,
Diacalpe, Nothoperanema, and Peranema (the Nothoperanema
clade; Fig. 1: clade B). Given that Ctenitis has been resolved as
not being closely related to Dryopteris previously (Liu & al.,
2007), our results contrast with the treatment of Nothoper-
anema as part of Ctenitis by Itô (1939), Copeland (1947), and
Ohwi (1957) but are in agreement with the treatment of Noth-
operanema as part of Dryopteris by Smith & al. (2006) and
Christenhusz & al. (2011). The placement of Acrophorus, Dia-
calpe, Nothoperanema, and Peranema within the Dryopteris
clade necessitates the synonymization of these four genera with
Dryopteris in order to maintain a monophyletic Dryopteris
(Fig. 1: clade A). Morphologically, these five genera (Fig. 1:
clade A) share short and erect or ascending rhizomes, caespi-
tose fronds, and catadromic pinnules (except the secondary
segments of the basalmost pair of pinnae). In contrast, species
of the sister genus Arachniodes (Fig. 1: clade G), as resolved
in this and earlier studies (e.g., Sessa & al., 2012), have long
and creeping rhizomes, non-caespitose fronds, and anadromic
pinnules (Wu & Ching, 1991; Wu, 2000).
Fraser-Jenkins (1986) recognized four subgenera within
the traditionally defined Dryopteris, i.e., D. subg. Dryopteris,
D. subg. Erythrovariae (H. Itô) Fraser-Jenk., D. subg. Neph-
rocystis (H. Itô) Fraser-Jenk., and D. subg. Pycnopteris
(T. Moore) Ching. In our study, except D. subg. Pycnopteris
of which only one species was sampled, all other subgenera
sensu Fraser-Jenkins (1986) are resolved as paraphyletic.
Dryopteris subg. Dryopteris is resolved as paraphyletic in re-
lation to the other taxa of Dryopteris sampled and the Noth-
operanema clade. Dryopteris subg. Erythrovariae would be
monophyletic if D. hasseltii (Blume) C. Chr., a member of
D. subg. Nephrocystis, would be included in this subgenus
(Fig. 1; clade D: MP JK 92%, ML BS 95%). Our resolution of
D. hasseltii is in accordance with Li & Lus (2006b) results.
The inclusion of D. hasseltii in D. subg. Nephrocystis appears
consistent with its morphology. Fraser-Jenkins (1986) already
noticed some similarities between D. sect. Nephrocystis and
D. subg. Erythrovariae (e.g., asymmetrical pinnules). Two ad-
ditional species of D. subg. Nephrocystis, D. futura A.R. Sm.
and D. sparsa (Buch.-Ham. ex D. Don) Kuntze, were sampled
in our study. The resolution of these two, together with that of
D. hasseltii, showed that D. subg. Nephrocystis is paraphyletic
(Fig. 1: clades D & F). This is accordant with Sessa & al.’s
(2012) resolution. Dryopteris subg. Pycnopteris is embedded
within a monophyletic clade consisting of a portion of D. subg.
Dryopteris (Fig. 1: clade E).
Three of the four genera in the Nothoperanema clade
(Fig. 1), Acrophorus, Diacalpe, and Peranema, constitute the
family Peranemataceae sensu Ching (1978) and Wu (1983,
1999). Our study provides the first strong evidence that the
traditionally defined Peranemataceae are paraphyletic in rela-
tion to Nothoperanema, a genus never treated as a member of
Peranemataceae because of its reniform indusia (Tagawa, 1938;
Ching 1966; Wu, 2000). This resolution is consistent with Liu
& al.’s (2007) findings based on atpB and rbcL sequences. The
Nothoperanema clade is well support ed as monophyletic in our
study (Fig. 1: clade B; MP JK: 98%; ML BS: 99%). Interest-
ingly, Kuo (1985) placed the four genera in the Nothoperanema
clade in his tribe Peranemateae C. Presl under Dryopteridaceae.
Species of the Nothoperanema clade are similar to one another
in having non-glandular hairs.
Our sampling was not dense enough to assess the over-
all subgeneric classification of Dryopteris by Fraser-Jenkins
(1986) or Wu & Lu (2000). However, based on our data it seems
clear that three of the four currently recognized subgenera
should be re-defined to maintain their monophyly and D. subg.
Pycnopteris should be a synonym of D. subg. Dryopteris. Ear-
lier, Geiger & Ranker (2005), Li & Lu (2006a, b), Liu & al.
(2007), and Sessa & al. (2012) partially rejected the monophyly
of these four subgenera of Dryopteris. However, a thorough
re-arrangement of subdivisions of Dryopteris awaits more
sampling and more molecular data, especially nuclear data.
Most interestingly, the Nothoperanema clade in our study
(Fig. 1: clade B), strongly supported as monophyletic by mo-
lecular and morphological evidence, cannot be accommodated
in any existing subgenus of Dryopteris but deserves to be
Table 3.
Data-matrix and tree statistics for each of the analyses.
Matrix
No. of
accessions
No. of
characters
PI
characters
% miss./
inappl.
MPT
length
# MP JK /
ML JK(BS)
clades
avg. MP JK /
ML JK(BS)
support (%) CI RI
psbA-trnH spacer 44 617 72 13 205 18 / 18 89 / 89 0.7659 0.8345
rbcL gene 64 1323 152 4 467 40 / 42 80 / 82 0.5953 0.8017
rps4-trnS spacer 44 1093 172 23 446 28 / 28 85 / 86 0.7197 0.8120
trnL intron 33 787 116 32 262 21 / 21 87 / 88 0.7634 0.8727
trnL-F spacer 54 445 91 13 269 27 / 28 77 / 79 0.6766 0.8371
trnL intron & trnL-F spacer 54 1232 207 13 534 30 / 33 82 / 82 0.7154 0.8511
Simultaneous 67 4265 639 0 1688 50 / 53 85 / 87 0.6742 0.8122
Abbreviations used in column headers are as follows: PI, parsimony-informative; % miss./inappl., percentage of cells in the data matrix scored as
missing or inapplicable; MPT, most parsimonious tree(s); MP, maximum parsimony; ML, maximum likelihood; JK, jackknife; BS, bootstrap; CI,
consistency index; RI, retention index.
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recognized as a subgeneric entity. The earliest available sub-
generic name for the Nothoperanema clade is D. subg. Notho-
peranema Tagawa (1938). Here D. subg. Nothoperanema is
re-circumscribed to include the genera Acrophorus, Diacalpe,
Nothoperanema, and Peranema.
Evolution of flat vs. bullate scales in Dryopteris. —
Wu
& Lu (2000) did not recognize one of the four subgenera of
Dryopteris proposed by Fraser-Jenkins (1986), D. subg. Neph-
rocystis, because species of this subgenus have only f lat scales,
a character shared with D. subg. Dryopteris and D. subg. Pyc-
nopteris. Notably, species with bullate scales appear only in
clade D in our Fig. 1. Therefore, our results demonstrate that
flat scales in Dryopteris do not seem to be a morphological
synapomorphy defining any of the subgenera, but rather are a
plesiomorphy of the genus. This hypothesis is reinforced by the
fact that species of the sister genus of Dryopteris, Arachniodes
(Fig. 1: clade G), also have only flat scales. Furthermore, the
Cyrtomium + Phanerophlebia + Polystichum clade (Fig. 1: clade
H), as the sister of the Arachniodes + Dryopteris clade (Fig. 1:
clade J), has only flat scales as well.
Within the bullate-scales-bearing Dryopteris subg. Eryth-
rovariae clade (Fig. 1: D), D. hasseltii is resolved as sister
to D. polita Rosenst. Neither of these two species has bul-
late scales. The clade containing these two species is sister to
D. varia (L.) Kuntze and these three species together are sister
to a clade containing D. erythrosora (D. Eaton) Kuntze and
D. gymnosora (Makino) C. Chr. All three of the latter species
have bullate scales (Fraser-Jen kins, 1986; Wu & Lu, 2000). Our
resolution of these five species and the distribution pattern of
bullate scales in the subgenus suggest that the bullate scales
in D. subg. Erythrovariae might have evolved once from flat
scales in the most recent common ancestor of clade D and that
there has been at least one reversal of bullate scales to flat
scales in the D. hasseltii + D. polita clade. The flat scales in the
D. hasseltii + D. polita clade and those in D. subg. Dryopteris
and D. subg. Nephrocystis are not homologous. This evolu-
tionary pattern of bullate scales is consistent with Fraser-Jen-
kins’s (1986) inclusion of some species without bullate scales
(e.g., D. polita) in D. subg. Erythrovariae, but contrasts with
Lu’s (1999) and Wu & Lu’s (2000) exclusion of D. polita from
D. subg. Erythrovariae. Dryopteris hasseltii was assigned to
D. subg. Nephrocystis by Fraser-Jenkins (1986). More samples
are needed for molecular studies to better understand how many
reversals of bullate scales to flat scales have taken place during
the evolutionary history of D. subg. Erythrovariae.
Relationships within Dryopteris subg. Nothoperanema.
Acrophorus, Diacalpe, Nothoperanema, and Peranema are
each recovered as monophyletic groups with relatively high
support values (MP JK: 80%–99%; ML BS: 85%–100%). Our
resolution of Nothoperanema is consistent with Liu & al.s
(2007) results but contrasts with Li & Lu’s (2006b) results
where Nothoperanema was resolved as paraphyletic in relation
to Dryopteris erythrosora with high branch support values. The
well-supported monophyly of these four genera is not surprising
given that they are morphologically well defined. Acrophorus
is characterized by having cordate and often persistent scales at
the bases of costae, membranaceous and semi-globose indusia,
a few multi-celled septate clavate paraphyses on the lower por-
tion of sporangiate stalks, and a few, short multi-celled clavate
appendages on the margins of scales at the bases of petioles
(Wu, 1983, 1999; Wu & Ching, 1991). The most important mor-
phological synapomorphy of Nothoperanema is the presence of
short and stout setae on each side of the costae and at the forking
position of the midribs (Ching, 1966). Peranema is morpho-
logically distinguishable from Diacalpe by havi ng stalked sori,
no paraphyses on the lower portion of sporangiate stalks, and
a few short and single-celled clavate hairs on the margins of
scales at the bases of the stipes (Wu, 1983, 1999; Wu & Ching,
1991). Diacalpe is char acteri zed by havi ng unstalked sori, a few
single-celled, long and clavate paraphyses on the lower portions
of sporangiate stalks, and entire scales at the bases of stipes
(Wu, 1983, 1999; Wu & Ching, 1991). A few authors treated
Diacalpe as a synonym of Peranema (e.g., Nayar & Kaur, 1966;
Kramer, 1990; Smith & al., 2006; Fraser-Jenkins, 2008). This
treatment is not supported by our analyses (Fig. 1), which did
not even resolve these two taxa as sister to each other.
Within Dryopteris subg. Nothoperanema (Fig. 1: clade
B), Peranema is resolved as the sister to the remaining three
genera, followed by Nothoperanema which in turn is resolved
as sister to a clade containing Acrophorus and Diacalpe. How-
ever, the support values for such relationships are not high
(MP JK: 60%–61%; ML BS: 64%–66%). If the relationships
of these four taxa discovered by our data are correct, the most
parsimonious hypothesis for the evolution of indusia in D. subg.
Nothoperanema would be that the flat and reniform indusia
evolved once to globose indusia in the most recent common
ancestor of D. subg. Nothoperanema, then reversed to flat and
reniform indusia in Nothoperanema but remained unchanged
or only modified in Acrophorus and Diacalpe.
TAXONOMIC TREATMENT AND
NOMENCLATURAL ACCOUNT
Dryopteris subg. Nothoperanema Tagawa in Acta Phytotax.
Geobot. 7: 199. 1938 Nothoperanema (Tagawa) Ching
in Act a Phytotax. Sin. 11: 25. 1966 Lectoype (designated
by Ching in Acta Phytotax. Sin. 11: 25. 1966): Nothoper-
anema squamisetum (Hook.) Ching (= Dryopteris squa-
miseta (Hook.) Kuntze).
About 27 species distributed mainly in tropical and sub-
tropical areas of Africa, Asia, Madagascar, Papua New Guinea,
and Polynesia, including the Hawaiian Islands.
Dryopteris subg. Nothoperanema can be divided into
four sections. All four sections are strongly supported as
monophyletic based on molecular (Fig. 1) and morphological
(Tagawa, 1938; Ching, 1966; Wu, 1983, 1999; Kramer, 1990;
Wu & Ching, 1991) evidence. In fact, the four sections are strik-
ingly different in morphology and are often treated as different
genera (Ching, 1966, 1978; Pichi Sermolli, 1977; Kuo, 1985;
Wu, 1983, 1999; Kramer, 1990; Wu & Ching, 1991; Smith & al.,
2006; Christenhusz & al., 2011; see our discussion above). The
four sections are distinguishable from one another using the
following characters:
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Key to sections
1. Indusia above sori, flat, reniform ..........................
.................................. 1. D. sect. Nothoperanema
1. Indusia beneath sori, globose or semi-globose .......... 2
2. Pinnae and pinnules of every order with or without a
large cordate or ovate-lanceolate and often persistent
scale at base; indusia membranaceous, semi-globose, in-
dehiscent; lower portion of sporangiate stalk with a few
multicellular clavate septate paraphyses; scales at base of
petiole with multicellular clavate appendages on margin
....................................... 2. D. sect. Acrophorus
2. Pinnae and pinnules of every order without a large cordate
scale at base; indusia leathery, globose, often splitting into
2–3 valves at maturity; lower portion of sporangiate stalk
with single-celled clavate septate paraphyses or without
any paraphyses; scales at base of petiole with single-celled
clavate appendages on margin or without any append-
ages ......................................................... 3
3. Sori sessile; lower portion of sporangiate stalk with single-
celled clavate septate paraphyses; scales at base of petiole
with entire margins .................. 3. D. sect. Diacalpe
3. Sori stalked; lower portion of sporangiate stalk without
any paraphyses; scales at base of petiole with single-celled
clavate appendages on margin ..... 4. D. sect. Peranema
Dryopteris sect. Nothoperanema (Tagawa) Li Bing Zhang, stat.
nov. D. subg. Nothoperanema Tagawa in Acta Phytotax.
Geobot. 7: 199. 1938 ≡ Nothoperanema (Tagawa) Ching
in Acta Phytotax. Sin. 11: 25. 1966 – Type: Dryopteris
squamiseta (Hook.) Kuntze.
Dryopteris sect. Nothoperanema is different from all other
three sections in Dryopteris subg. Nothoperanema by having
superior (above sori), flat, and reniform indusia.
There are ca. eight (six described) species in Dryopteris
sect. Nothoperanema distributed in East, northeastern, and
South Asia, central, southern, and East Africa, the Himalaya,
Madagascar and Mascarene Islands (including La Réunion),
New Guinea, and Polynesia (including the Hawaiian Islands).
The six known species can be distinguished from one another
with the following key (cf. Ching, 1966; Smith & Palmer, 1995;
Hsieh, 2000; Palmer, 2003).
Key to species
1. Rachis scales long-subulate .............................. 2
1. Rachis scales lanceolate or linear-lanceolate ........... 5
2. Plant 60–110 cm tall; basalmost pinnae 14–21 cm long; pri-
mary segments 5–7 cm long; secondary segments 1–1.6 cm
long ......................................................... 3
2. Plant 120–150 cm tall; basalmost pinnae up to 38 cm long;
primary segments up to 17 cm long; secondary segments
up to 2 cm long ......................... 4. D. grandifrons
3. Rachis scales almost black when dried; pinnae acute api-
cally ...................................... 1. D. squamiseta
3. Rachis scales brown to rust colored when dried; pinnae
acute or obtuse apically ................................... 4
4. Plant 60–70 cm; pinnae obtuse apically; middle pinnae ca.
3 cm wide .............................. 2. D. diacalpioides
4. Plant 70–100 cm; pinnae acute apically; middle pinnae up
to 3.5 cm wide ............................ 3. D. rubiginosa
5. Sori indusiate; rachis scales reddish brown; ultimate seg-
ments serrate apically .................. 5. D. hendersonii
5. Sori exindusiate; rachis scales dark brown; ultimate seg-
ments entire or undulate apically ...... 6. D. shikokiana
1. Dryopteris squamiseta (Hook.) Kuntze, Revis. Gen. Pl. 2:
813. 1891 ≡ Nephrodium squamisetum Hook., Sp. Fil. 4:
140, pl. 268. 1862 ≡ Aspidium squamisetum (Hook.) Kuh n,
Filic. Decken.: 24. 1867 ≡ Nothoperanema squamisetum
(Hook.) Ching in Acta Phytotax. Sin. 11: 27. 1966 Lecto-
type (designated here): Equatorial Guinea, Fernando Po,
Clarence Peak, alt. 4000 ft., 1860, Gustav Mann 380 ( K-
000351166!; isolectotype: K-000351167!).
= Nephrodium buchananii Baker in Hooker & Baker, Syn.
Fil., ed. 2: 498. 1874 ≡ Lastrea buchananii (Baker) Bedd.,
Handb. Ferns Brit. India: 255. 1883 ≡ Dryopteris buchana-
nii (Baker) Kuntze, Revis. Gen. Pl. 2: 812. 1891 – Lectotype
(designated here): South Africa, Natal, J. Buchanan 108
(K-000351169!; isolectotype: K000351168!), J. Buchanan
s.n. (paratype: US-00135332).
= Dryopteris atrosetosa Rosenst. in Hedwigia 56: 342. 1915
Type: China, Taiwan, Arisan, alt. 2500 m, Mai 1914,
Faurie 382 (herbarium unknown).
= Dryopteris thrichorachis Hayata, Icon. Pl. Formos. 4: 185,
f. 123. 1914 Ctenitis thrichorachis (Hayata) H. Itô in
Nakai & Honda, Nova Fl. Jap. 4: 90. 1939 – Lectotype
(designated here): China, Taiwan, Arisan, Jan 1912,
B. Hayata & Sasaki s.n. (“Typus - PLANTAE FORMO-
SANAE - Dryopteris thrichorachis - Hay. - Loc. Arisan
– Leg. B. Hayata, 1912”, TI!).
The type material of Dryopteris atrosetosa Rosenst. was
not found in B or M where Rosenstock’s material is deposited
(Stafleu & Cowan, 1983).
Two accessions of Dryopteris squamiseta from Yunnan
and La Réu nion, respectively, were included in our study. They
formed a monophyletic clade and had identical rbcL sequences.
The occurrence of this species in La Réunion is best explained
as the result of long-distance dispersal from Asia.
This species occurs in central and southern Africa, Bhu-
tan, China (Taiwan, Xizang, Yunnan), India, La Réunion, and
Madagascar.
2. Dryopteris diacalpioides (Ching) Li Bing Zhang, comb.
nov. Nothoperanema diacalpioides Ching in Acta Phy-
totax. Sin. 11: 28. 1966 – Holotype: China, Yunnan, Jin-
ping (King-ping), in shady moist places in forest, alt. ca.
2400 m, Yunnan Complex Exp. 2455 (PE-00044596!).
This species is currently known to be endemic to southern
Yunnan (Jinping, Pingbian), China but might occur in northern
Vietnam, too.
3. Dryopteris rubiginosa (Brack.) Kuntze, Revis. Gen. Pl. 2:
813. 1891 ≡ Lastrea rubiginosa Brack., U.S. Expl. Exped.,
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Filic. 16: 201. 1854 ≡ Ctenitis rubiginosa (Brack.) Copel.,
Gen. Fil.: 125. 1947 ≡ Nothoperanema rubiginosum
(Brack.) A.R. Sm. & D.D. Palmer in Amer. Fern J. 85: 63.
1995 – Holot ype: U.S.A., Hawaii, in forest above saw mill,
1838, Wilkes Explor. Exped. 18 (US-00135244!).
This species is endemic to the Hawaiian Islands.
4. Dryopteris grandifrons Li Bing Zhang, nom. nov. Noth-
operanema giganteum Ching in Acta Phytotax. Sin. 11:
28. 1966 Lectotype (designated here): China, Yun-
nan, Gongshan (Kung-shan), Champutung, in thickets in
ravine, alt. 1700–1800 m, 28 Sep 1940, K.M. Feng 8073
(KUN-1216726!).
When this species is transferred to Dryopteris, a new
combination based on Nothoperanema giganteum Ching is
blocked by Dryopteris gigantea (Blume) Kuntze (Revis. Gen.
Pl. 2: 812. 1891) and D. gigantea (Mett.) C. Chr. (Index Filic.:
267. 1905).
Presumably there is an isolectotype of Nothoperanema
giganteum Ching at PE.
It is endemic to northwestern Yunnan (Gongshan), China.
5. Dryopteris hendersonii (Bedd.) C. Chr., Index Filic.: 270.
1905 Lastrea hendersonii Bedd., Suppl. Ferns S. Ind.:
17. t. 377. 1876 Ctenitis hendersonii (Bedd.) H. I in
Nakai & Honda, Nov. Fl. Jap. 4: 89, t. 5(106), 10(212),
14(311), 18(423). 1938 Holo type: India, Shillong Hill,
Khasya, alt. 6,000 ft, Henderson s.n. (not found at K)
Neotype (designated here): Lastrea hendersonii Bedd.,
Suppl. Ferns S. Ind.: t. 377. 1876.
= Dryopteris leptorhachis Hayata, Icon. Pl. Formos. 4: 162,
f. 102. 1914 (“leptorhachia”) Ctenitis leptorhachis
(Hayata) Ching in Bull. Fan Mem. Inst. Biol. 8: 280. 1938
(“lepterachis”) – Lecto type (designated by Chiou & al.,
2000): China, Taiwan, Arisan, Jan 1912, B. Hayata & Sa-
saki s.n. (TAIF-1034!).
= Ctenitis mearnsii Copel. in Philipp. J. Sci. 81: 24. 1952 –
Lecto type (designated here): Philippines, Luzon, Ben-
guet, Haight’s in the Oaks, 1907, E.A. Mearns BS 4216
(MICH-1190185!).
The type material of Lastrea hendersonii Bedd. was not
found in K (A. Haigh, pers. comm.). The accompanying illus-
tration in the protologue is designated as the neotype.
No type material of Dryopteris leptorhachia Hayata was
found at TI (J. Murata, pers. comm.) where Z. Hayata’s major
types are deposited (Stafleu & Cowan, 1979). The citation of
TAIF-1034 by Chiou & al. (2000) is accepted here as lecto-
typification although their citation is not indicated by the term
“lectotypus”, or its abbreviation, or its equivalent in a modern
language (Art. 9.21; McNeill & al., 2006).
This species occurs in China (Taiwan, Yunnan), northern
India, southern Japan, Malaysia, Myanmar, Nepal, and the
Philippines.
6. Dryopteris shikokiana (Makino) C. Chr., Index Filic.: 292.
1905 Nephrodium shikokianum Makino in Bot. Mag.
(Tokyo) 13: 62. 1899 Ctenitis shikokiana (Makino)
H. Itô in Nakai & Honda, Nov. Fl. Jap. 4: 88. t. 5(104–
105), 10(211), 18(422), 28(46). 1938 ≡ Nothoperanema shi-
kokianum (Makino) Ching in Acta Phytotax. Sin. 11: 28.
1966 – Syntypes: Japan, Shikoku Island, Prov. Tosa, Mt.
Honokawa-yama, 10 Aug 1887, T. Makino s.n. (herbarium
unknown); Mt. Imano-yama, 7 Aug 1889, T. Makino s.n.
(herbarium unknown).
The type material was not found in MAK or TI (J. Murata,
pers. comm.) where T. Makino’s major types are deposited
(Stafleu & Cowan, 1981).
This species occurs in China (Guangxi, Guizhou, Hunan,
Sichuan, Yunnan) and Japan.
Dryopteris sect. Acrophorus (C. Presl) Li Bing Zhang, comb.
& stat . nov.Acrophorus C. Presl, Tent. Pterid.: 93. 1836
– Type: Dryopteris nodosa (C. Presl) Li Bing Zhang).
There are ca. 12 (11 described) species in Dryopteris sect.
Acrophorus distributed in Southeast Asia, westward reaching
Papua New Guinea and Polynesia. The 11 known species can
be distinguished from one another with the following key (cf.
Wu, 1983, 1999).
Key to species
1. Lamina quadripinnate to quinquepinnatifid .............
............................................. 17. D. raiateensis
1. Lamina tripinnate to quadripinnatifid ................... 2
2. Lobes only up to 1 mm wide; rachis and costae densely
covered with scales ...... 16. D. papuae-novae-guineae
2. Lobes up to 2 or 3 mm wide or wider; rachis and costae
subglabrous or with a few scales ........................ 3
3. Pinnae and segments of every order without large cordate
scale but with a small ovate-lanceolate or broadly lanceo-
late scale at base ....................... 15. D. exstipellata
3. Pinnae and segments of every order with a large cordate
and often persistent scale at base ........................ 4
4. Secondary segments of upper pinnae acuminate or acute
apically ..................................................... 5
4. Secondary segments of upper pinnae rounded apically 9
5. Secondary segments elliptic-lanceolate, ultimate segments
with a deciduous scale at base; when the scale has fallen
off, a scale scar visible ................... 11. D. emeiensis
5. Secondary segments lanceolate, ultimate segments with a
persistent scale at base ..................................... 6
6. Rachis scabrous; sori ca. 0.8 mm in diam. 7. D. nodosa
6. Rachis glabrous ............................................ 7
7. Lobes rectangular; sori ca. 1 mm in diam. ...............
............................................ 10. D. acrophorus
7. Lobes elliptic; sori ca. 0.5 mm in diam. ................. 8
8. Fertile pinnules with up to 6 sori per lobe ...............
............................................... 8. D. paleolata
8. Fertile pinnules with 1–2 sori per lobe ....................
......................................... 9. D. loxoscaphoides
9. Lamina herbaceous; middle ultimate segments of middle
pinnae up to 1 cm wide .............. 14. D. leucorhachis
9. Lamina papery; middle ultimate segments of middle pin-
nae up to 3 mm wide ......................................10
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10. Pinnules of middle pinnae 1–1.5 cm long; lobes up to 2 mm
wide; sori ca. 0.5 mm in diam. ....... 12. D. wusugongii
10. Pinnules of middle pin nae 1.5–3 cm long; lobes up to 3 mm
wide; sori ca. 1 mm in diam. ...... 13. D. wuzhaohongii
7. Dryopteris nodosa (C. Presl) Li Bing Zhang, comb. nov.
Aspidium nodosum Blume, Enum. Pl. Javae 2: 171. 1828,
non Willd. (Sp. Pl. 5: 211. 1810) Acrophorus nodo-
sus C. Presl, Tent. Pterid.: 94, t. 3, f. 2. 1836 ≡ Peranema
nodosum (C. Presl) Fraser-Jenk., Taxon. Revis. Indian
Subcontinental Pteridophytes: 317. 2008 (nodosa”) Ac-
rophorus blumei Ching ex C. Chr. in Gard. Bull. Straits
Settlem. 7: 226. 1934, nom. illeg. – Lectotype (designated
here): Indonesia, Java, Burangrang, C.L. Blume s.n. (L-
0063159! [Acc. #91032664]).
There are five syntypes of Aspidium nodosum Blume at
L, collected by C.L. Blume in Burangrang, Java, Indonesia:
L-0063159 (Acc. #91032664), L-0063160 (Acc. #91032661),
L-0063161 (Acc. #91032662), L-0063162 (Acc. #91032663),
and L-0063163 (Acc. #91032665). Morphological observations
show that they represent the same species. L-0063159 is desig-
nated as lectotype here.
This species is often regarded to be a synonym of Acro-
phorus stipellatus (Wall.) Moore (= Dryopteris paleolata (Pic.
Serm.) Li Bing Zhang; e.g., Wu, 1983, 1999; He, 2006) or vice
versa (e.g., Iwatsuki, 1995), but Dryopteris nodosa has more
finely dissected leaves, scabrous rachis, and larger indusia.
Dryopteris nodosa occurs in China (Taiwan), Fiji, Indonesia,
southern Japan (Kyushu), Malaysia, and the Philippines, and
probably in Polynesia, but not in mainland China and the Hi-
malayan regions. Molecular data show that these two species
are not even closely related and should be separated from each
other (Fig. 1).
8. Dryopteris paleolata (Pic. Serm.) Li Bing Zhang, comb. nov.
Acrophorus paleolatus Pic. Serm. in Webbia 31(1): 252.
1977 ≡ Peranema paleolatum (Pic. Serm.) Fraser-Jenk.,
Taxon. Revis. Indian Subcontinental Pteridophytes: 317.
2008 (“paleolulata”) Holotype: India, Darjiling, Birch
Hill, alt. 6500 ft, 19 Sep 1879, H.C. Levinge 99 (FI!).
The name Acrophorus stipellatus (Wall.) T. Moore, based
on Davallia stipellata Wall., a nomen nudum, is not validly
published.
The species occurs in China, the Himalaya, northern Thai-
land , and Vietnam. It has been resolved as sister to the remain-
ing species of Dryopteris sect. Acrophorus (Fig. 1).
9. Dryopteris loxoscaphoides (Ba ker) C. Ch r., Index Filic.: 276.
1905 Polypodium loxoscaphoides Baker in J. Bot. 28: 107.
1890 ≡ Leucostegia loxoscaphoides (Ba ker) C. Ch r., Index
Filic., Supplementum Tertium: 120. 1934 ≡ Acrophorus
loxoscaphoides (Baker) Alston in J. Bot. 77: 288. 1939 –
Holotype: Papua New Guinea, Mount Musgrave, on Owen
Stanley Range, habit of Davallia (Laxoscaphe) giibberosa
and nigrescens, alt. 9200 ft, 5 Jun 1889, W. MacGregor 46
(K-000665044!).
This species has been placed under different genera in the
literature. Our morphological examinations of the type confirm
its placement in Dryopteris sect. Acrophorus.
It is known only from Papua New Guinea.
10. Dryopteris acrophorus Li Bing Zhang, nom. nov. Acro-
phorus diacalpioides Ching & S.H. Wu in Acta Phytotax.
Sin. 21(4): 381. 1983 – Holotype: Burma: Sadon, 13 Nov
1922, J.F. Rock 7392 (US; isotype: BM-001066119!)
When this species is transferred to Dryopteris, a new com-
bination based on Acrophorus diacalpioides Ching & S.H. Wu
is blocked by Dryopteris diacalpioides (Ching) Li Bing Zhang
(this paper).
This species occurs in China (Yunnan) and Myanmar.
11. Dryopteris emeiensis (Ching) Li Bing Zhang, comb. nov.
Acrophorus emeiensis Ching in Acta Phytotax. Sin. 21(4):
380, pl. 2 f. 2–4. 1983 – Holotype: China, Sichuan, Emei
Shan, in Abies forest, alt. 2700 m, R.C. Ching 186 (PE).
When this species is transferred to Dryopteris, its original
epithet emeiensis is available in spite of the existence of the
name Dryopteris omeiensis (Baker) C. Chr. (Index Filic. 5:
280. 1905).
This species is endemic to China (Sichuan).
12. Dryopteris wusugongii Li Bing Zhang, nom. nov.Acro-
phorus dissectus Ching in Acta Phytotax. Sin. 21(4): 382.
1983 – Holotype: China, Yunnan, S.K. Wu 4226 (PE-
00044788; isotype: KUN-1216844!).
When this species is transferred to Dryopteris, a new com-
bination based on Acrophorus dissectus Ching is blocked by
Dryopteris dissecta (G. Forst.) Kuntze (Revis. Gen. Pl. 2: 812.
1891). The new epithet is dedicated to the collector of the type
and a specialist of Dryopteris, Prof. Sugong Wu at KUN.
This species is endemic to China (Yunnan).
13. Dryopteris wuzhaohongii Li Bing Zhang, nom. nov.
Acrophorus macrocarpus Ching & S.H. Wu in Acta Phyto-
ta x. Sin. 21(4): 381, pl. 2 f. 1. 1983 – Holoty pe: Chi na, Yun-
nan, Deqin, Cizhong, in mixed forests, alt. 2900–3300 m,
18 Dec 1962, K.M. Feng 5512 (PE-00044791; isotype: PE-
00044790).
When this species is transferred to Dryopteris, a new com-
bination based on Acrophorus macrocarpus Ching & S.H. Wu
is blocked by Dryopteris macrocarpa Stewart (in Bull. Torrey
Bot. Club 72: 406. 1945). The new epithet is dedicated to a
specialist of ferns and one of the authors of the original name,
Prof. Zhaohong Wu (Shiew-Hung Wu) at IBSC.
This species is endemic to China (Taiwan, Yunnan).
14. Dryopteris leucorhachis (Cheeseman) C. Chr., Index Filic.:
274. 1905 Nephrodium leucorhachis Chees eman in Trans.
Linn. Soc. London, Bot. 6(6): 309. 1903 Acrophorus leu-
corhachis (Cheeseman) Brow nlie in Brownlie & Philipson,
Pacific Sci. 25: 507. 1971 – Lectotype (designated here):
French Polynesia, Cook Islands, Rarotonga, Summit of
Mount Tekou, alt. 1800 ft, Mai–Jul 1898, T.F. Cheeseman
s.n. (AK-114317!; isolectotype: AK-112192!).
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Sometimes this species is treated as a synonym of
Dry opteris raiateensis (J.W. Moore) Li Bing Zhang (e.g.,
McCormack, 2007). In fact, D. leucorhachis has a tripinnati-
fid to tripinnate lamina (vs. quadripinnate to quinquepinnatifid
in D. raiateensis) and ultimate pinnules up to 1 cm (vs. up to
4 mm in D. raiateensis) wide in the middle.
The species is endemic to Polynesia and known only from
three sites in Cook Islands (McCormack, 2007).
15. Dryopteris exstipellata (Ching & S.H. Wu) Li Bing Zhang,
comb. nov. Acrophorus exstipellatus Ching & S.H. Wu
in Acta Phytotax. Sin. 21(4): 383. 1983 – Holotype: China,
Sichuan, Ebian, Wenba, south of Beijing Bridge, on south-
ern slope, in mixed forest, alt. 2250 m, Zhongtian Guan
(C.T. Kuan) 6592 (PE-00044789!).
This species occurs in China (Guangdong, Sichuan, etc.).
16. Dryopteris papuae-novae-guineae Li Bing Zhang, nom.
& stat. nov. Acrophorus stipellatus var. montanus
Rosenst. in Repert. Spec. Nov. Regni Veg. 12: 166. 1913
(“montana”) – Lectotype (designated here): Papua New
Guinea, in montibus Bolan dictis, K. Wilhelms Land, alt.
2400–3000 m, 1912, C. Keysser 65 (S-P-601!; isolectotype:
BM-001066118!), C. Keysser 76 (paratype: S-P-602!).
When this taxon is transferred to Dryopteris, a new combi-
nation based on Acrophorus stipellatus var. montanus Rosenst.
is blocked by Dryopteris montana Kuntze (Revis. Gen. Pl. 2:
813. 1891).
When describing Acrophorus stipellatus var. montanus
Rosenst., Rosenstock (1913) cited two gatherings (syntypes),
C. Keysser 65 and 76. These two gatherings clearly belong to
the same species. One of them is designated as lectotype here.
Copeland (1949) erroneously cited a specimen of the gathering
C. Keysser 76 as an “isotype” without specifying the herbaria
holding the gathering. Copeland’s (1949) “designation” is not
accepted as lectotypification.
Copeland (1949) subsumed Dryopteris papuae-novae-
guineae under Acrophorus stipellatus (= Dryopteris paleolata
(Pic. Serm.) Li Bing Zhang), but the former has very narrow
lobes (up to 1 mm wide) and its rachis and costae are densely
covered with scales, different from any species in D. sect.
Acrophorus.
The species occurs in Papua New Guinea.
17. Dryopteris raiateensis (J.W. Moore) Li Bing Zhang, comb.
nov.Acrophorus raiateensis J.W. Moore in Bull. Bernice
P. Bishop Mus. 102: 6. 1933 – Holotype: French Polynesia,
Society Islands, Island of Raiates, Îles Sous le Vent, south
end of Temehani Range, alt. 700 m, 15 Apr 1927, John Wil-
liam Moore 738 (BISH-1000025!; isotypes: BISH-100026!,
CANB-354743!, UC-1440311!, US-3556586!, US-3239203!).
Th is species has a quad ripinnate to qu inquepin natifid lam-
ina, different from any species in Dryopteris sect. Acrophorus.
It is endemic to Polynesia (Society Islands).
Dryopteris sect. Diacalpe (Blume) Li Bing Zhang, comb.
& stat. nov. Diacalpe Blume, Enum. Pl. Javae 2: 241.
1828 – Type: Dryopteris pseudocaenopteris (Kunze) Li
Bing Zhang).
There are eight species in Dryopteris sect. Diacalpe dis-
tributed in tropical and subtropical Asia, Pacific islands, Ca-
ribbean islands, and South America. The eight species can be
distinguished from each other with the following key (cf. Wu,
1999).
Key to species
1. Primary segments of lower pinnae truncate apically and
shallowly undulate on margin; ultimate segments rounded
apically and entire or slightly toothed on margin ........
........................................... 25. D. annamensis
1. Primary segments of lower pinnae acuminate or obtuse
apically, toothed to more or less pinnatifid on margin . . 2
2. Rachis and rachillae of every order abaxially glabrous or
subglabrous; primary segments obtuse apically and with
only 3–7 teeth ......................... 24. D. medogensis
2. Rachis and costae of every order abaxially with scales or
scales falling off leaving scabrous surfaces; primary seg-
ments acuminate or mucronate and with only 2–3 teeth . 3
3. Plant robust; pinnae slightly angled upward; lamina with
glands along veins ......................................... 4
3. Plant slender; pinnae strongly angled upward; lamina
nearly without glands ...................................... 7
4. Lamina chartaceous; acroscopic primary segments 1
1.5 cm apart from rachis; non-basal pinnae nearly sessile
......................................... 18. D. christensenae
4. Lamina papery; acroscopic primary segments 3–5 mm
apart from rachis; pinnae obviously stalked ............. 5
5. Pinnules more or less right-angled with rachillae; sori ca.
1.5 mm in diam.; whole plant densely scaly ..............
................................................21. D. diacalpe
5. Pinnules angled upward; sori ca. 0.8 mm in diam.; only
lower portion of plant densely scaly ..................... 6
6. Pin nae with stalk 5–10 cm long and pinnules short-stalked
................................... 19. D. pseudocaenopteris
6. Pinnae and pinnules sessile .......... 20. D. hookeriana
7. Plant ca. 80 cm tall; lamina 40–45 cm long, ca. 30 cm
wide, basalmost pinnae 23–28 cm long, angled slightly
acroscopically ............................ 22. D. kungiana
7. Plant 30–35 cm tall; lamina ca. 20 cm long, 6–9 cm wide,
basalmost pinnae ca. 10 cm long, angled strongly acro-
scopically .............................. 23. D. adscendens
18. Dryopteris christensenae (Ching) Li Bing Zhang, comb.
nov. Diacalpe christensenae Ching in Bull. Fan Mem.
Inst. Biol., n.s. 1: 291. 1949 – Holotype: China, Yunnan,
Lincang, (Mienning, Po-shang Hsien), upon the trunk of a
tree, alt. 2500 m, 12 Oct 1938, T.T. Yü 18045 (PE-00050275!;
isotypes: IBSC, PE-00050273!, PE- 00050274!).
This species is endemic to China (Yunnan).
19. Dryopteris pseudocaenopteris (Kunze) Li Bing Zhang,
comb. nov. Diacalpe pseudocaenopteris Kunze in
Bot. Zeitung (Berlin) 4: 457. 1846 – Holotype: Indonesia,
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Sumbawa Island (Lesser Sunda Isl.), M. Batn Sante, 4000–
5000 ft., 1842–1848, Zollinger 1721 (herbarium unknow n;
isotype: UC-414487!).
= Diacalpe aspidioides Blume, Enum. Pl. Javae: 241. 1828 ≡
Physematium aspidioides (Blume) Kunze, Analecta Pteri-
dogr.: 43. 1837 ≡ Cyathea aspidioides (Blume) Moritz, Syst.
Verz.: 108. 1845Peranema aspidioides (Blume) Mett.,
Fil. Lechl. 2: 33. 1859 – Holotype: Indonesia, Java, Buran-
grang, C.L. Blume s.n. (L-0051510! [Acc. #908331505]).
= Diacalpe aspidioides var. minor Ching ex S.H. Wu in Acta
Phytotax. Sin. 21: 375. 1983 – Holoty pe: Yunnan, Yanshan,
Ta-ker-di, 10 Oct 1939, C.W. Wang 84289 (PE-00044794!).
When this species is transferred to Dryopteris, a new
combination based on Diacalpe aspidioides Blume is blocked
by Dryopteris aspidioides (Willd.) C. Chr. (Index. Filic.: 253.
1905).
This species occurs in China (Hainan, Taiwan, Yunnan),
Bhutan, India, Indonesia, Malaysia, Myanmar, Nepal, New
Guinea, Philippines, Sri Lanka, Thailand, and Vietnam.
20. Dryopteris hookeriana (T. Moore) Li Bing Zhang, comb.
nov. Diacalpe hookeriana T. Moore in Gard. Chron.
1854: 135. 1854 ≡ Diacalpe aspidioides Blume var. hooke-
riana (T. Moore) Ching & S.K. Wu in C.Y. Wu, Fl. Xi-
zang. 1: 194. Mar 1983 – Type:Sphaeropteris hookeriana
Wall.”, Numer. List.: 248. 1828, Wall. Cat. 775 (K, not
seen).
None of the following related names is validly published:
Sphaeropteris hookeriana Wall., Numer. List.: 248. 1828
(nom. nud.); “Diacalpe aspidioides var. himalayensis Ching
& S.K. Wu” in Acta Phytotax. Sin. 21: 376. post Sep 1983
(nom. nud.); “Diacalpe aspidioides var. hookeriana Wall. ex
Ching & S.H. Wu” in Acta Phytotax. Sin. 21: 376. post Sep
1983 (isonym).
This species is sometimes treated as a variety of Dryopteris
pseudocaenopteris (Kunze) Li Bing Zhang (e.g., Wu, 1983).
Dryopteris hookeriana differs from the latter in its subsessile
pinnae and pinnules.
This species occurs in China (Xizang), India, and Nepal.
21. Dryopteris diacalpe Li Bing Zhang, nom. nov. Diacalpe
chinensis Ching & S.H. Wu in Acta Phytotax. Sin. 21(4):
376, pl. 1 f. 4. 1983 – Holotype: China, Yunnan, Taron-
Taru Divide, under shady rocks, alt. 2300 m, 28 Aug. 1938,
T.T. Yü 20037 (PE-00050272!; isotype: PE-00044796!).
When this species is transferred to Dryopteris, a new
combination based on Diacalpe chinensis Ching & S.H. Wu
is blocked by Dryopteris chinensis (Baker) Koidz. (Fl. Symb.
Orient.-Asiat.: 39. 1930).
Diacalpe chinensis is characterized by having large sori.
It is endemic to China (Sichuan, Yunnan).
22. Dryopteris kungiana Li Bing Zhang, nom. nov.Dia-
calpe omeiensis Ch ing in Bull. Fan Mem. Inst. Biol., n.s., 1:
293. 1949 – Lectotype (designated here): China, Sichuan,
Emei Shan, 15 Oct 1940, T.C. Lee 3934 (PE-00050278!;
isolectotype: US-00048849!).
When this species is transferred to Dryopteris, a new com-
bination based on Diacalpe omeiensis Ching is blocked by
Dryopteris omeiensis (Baker) C. Chr. (Index Filic.: 280. 1905).
The specific epithet in the new name is in honor of the
late Professor Hsian-Shiu Kung (Xian-Xu Kong), a specialist
of ferns and lycophytes in Sichuan, based at CDBI.
In the protologues (Ching, 1949) three collections from the
same mountain are cited without designating the type: T.C. L ee
3934 (PE, US), C.S. Cheng 639, and 675 (PE). One sheet of
T.C. Lee 3934 at PE is designated here as lectotype.
This species is endemic to China (Sichuan).
23. Dryopteris adscendens (Ching ex S.H. Wu) Li Bing Zhang,
comb. nov.Diacalpe adscendens Ching ex S.H. Wu in
Acta Phytotax. Sin. 21(4): 378. 1983 – Lectotype (desig-
nated here): China, Yunnan, Jingdong, Wuliang Shan,
alt. 2900 m, Apr 1954, Wenxuan Xu (W.H. Hsu) 210 (PE-
00044793!; isolectotypes: PE-00044792!, YUNU).
In the protologue the type is erroneously cited as “260”.
This species is endemic to China (Yunnan).
24. Dryopteris medogensis (Ching & S.K. Wu) Li Bing Zhang,
comb. nov. Diacalpe medogensis Ching & S.K. Wu in
C.Y. Wu, Fl. Xizang. 1: 196, t. 46 f. 4– 6. Ma r 1983 – Holo-
type: China, Xizang (Tibet), Mêdog, in forest, alt. 1800 m,
6 Aug 1974, Qinghai-Xizang Complex Exp. 74-4150 (PE-
00044797!; isotype: PE-00969199!).
= Diacalpe laevigata Ching & S.H. Wu in Acta Phytotax. Sin.
21(4): 377, pl. 1 f. 3. post Sep 1983 – Holotype: China,
Yunnan, near Kunming, Maire 2820 (P).
In the protologue of Dryopteris medogensis (Ching
& S.K. Wu) Li Bing Zhang, the type is cited as “5150”, a typo
of “4150”.
This species is endemic to China (Xizang, Yunnan).
25. Dryopteris annamensis (Tagawa) Li Bing Zhang, comb.
nov.Diacalpe annamensis Tagawa in Acta Phytotax.
Geobot. 14: 46. 1950 – Holotype: Vietnam, Khanh Hoa
Province: Nha Trang, alt. 2000 m, in cool place in forest,
in clay soil, 21 Mai 1922, Poilane 3589 (KYO- 00037379!).
= Diacalpe caudifolia Ching & S.K. Wu in C.Y. Wu, Fl. Xi-
zang. 1: 194. 1983 – Holotype: China, Xizang: Mêdog, near
Dekougong, 10 Sep 1974, Qinghai-Xizang Complex Exp.
74-5070 (: PE-00044795!).
The species occurs in China (Hainan, Taiwan, Xizang,
Yunnan) and Vietnam.
Dryopteris sect. Peranema (D. Don) Li Bing Zhang, comb. &
stat. nov. Peranema D. Don, Prodr. Fl. Nepal.: 12. 1825
– Type: Dryopteris peranema Li Bing Zhang.
There are two species in Dryopteris sect. Peranema dis-
tributed in China, India, Myanmar, Nepal, and the Philippines.
Sometimes the two taxa are treated as two varieties (e.g., Wu,
1983, 1999) but they are very different in morphology (He,
2006). Our molecular data support the treatment of the two as
different species (Fig. 1). The two species can be distinguished
from each other with the following key (cf. He, 2006).
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Key to species
1. Plant up to 1.8 m; rhizome, petiole, and rachis densely
covered with darkish brown and subulate scales; scales
on rhizome and petiole base up to 3.5 cm long ...........
............................................. 26. D. peranema
1. Plant up to 1.5 m; rhizome, petiole, and rachis densely
covered with darkish brown to light brown and ovate-
lanceolate scales; scales on rhizome and petiole base up
to 2 cm long ......................... 27. D. zhuweimingii
26. Dryopteris peranema Li Bing Zhang, nom. nov. Per-
anema cyatheoides D. Don, Prodr. Fl. Nepal.: 12. 1825
Lectotype (designated here): Nepal, Nepalia, 1820,
Sphaeropteris barbata Wall.”, N. Wallich 183, Wall. Herb.
1823 (K-000674134!; isolectotype: UC-267864!; fragment
of isolectotype: MICH-1191382!).
In addition to the lectotype selected here, the Wallich 183
collection cited by D. Don in the protologue contains three
sheets of specimens collected at least at two different loca-
tions and at least at two different times: Napal, N. Wallich 183
(K-000674164); Nepal, Chandagiri, 19 Dec 1821, N. Wallich
183 (K-000674165); and Nepal, N. Wallich 183 (K-000674166).
When this species is transferred to Dryopteris, a new com-
bination based on Peranema cyatheoides D. Don is blocked
by Dryopteris cyatheoides (Kaulf.) Kuntze (Revis. Gen. Pl.
2: 812. 1891).
The species occurs in China (southeastern Xizang, north-
western Yunnan) and the Himalaya.
27. Dryopteris zhuweimingii Li Bing Zhang, nom. nov. Per-
anema luzonicum Copel. in Philipp. J. Sci. 4(2): 111. 1909
(“luzonica”) ≡ Peranema cyatheoides var. luzonicum (Co-
pel.) Ching & S.H. Wu in Acta Phytotax. Sin. 21(4): 373.
1983Lectotype (designated here): Philippines, Luzon,
Benguet, Mt. Pulog, Jan 1909, H.M. Curran, M.L. Merritt,
T.C. Zschokke 16280 (US-00135287!).
= Peranema formosanum Hayata in Bot. Mag. (Tokyo) 26:
110. 1912 (“formosana”) – Lectotype (designated here):
China, Taiwan, Arisan, 23 Jan 1912, B. Hayata & S. Sa-
saki s.n. (TI-0216!; isolecto types: TAIF-1469!, 1470!, 1471!,
1472!, TI-0209!, 0210!, 0211!, 0212!, 0213!, 0214!, 0215!,
0217!, 0218!, 0219!, 0220!).
When this species is transferred to Dryopteris, new com-
binations based on Peranema luzonicum Copel. and P. formo-
sanum Hayata are blocked by Dryopteris luzonica Christ (in
Philipp. J. Sci. 2(3): 196. 1907) and D. formosana (Christ) C. Ch r.
(Index Filic.: 266. 1905). The new epithet is dedicated to Profes-
sor Wei-Ming Chu (Wei-Ming Zhu), founder of the herbarium
PYU and a specialist of ferns and lycophytes of China.
The holding of other isolectotypes of Peranema luzonicum
Copel. is unknown, but they do not seem to be at UC or MICH
where E.B. Copeland’s original and duplicate material is held.
Chiou & al. (2000) listed four syntypes of Peranema for-
mosanum Hayata at TAIF without designating a lectotype.
After studying all syntypes at TAIF and TI, we select TI-0216
as lectotype.
The species occurs in China (Guizhou, Guangxi, Hubei,
Hunan, Sichuan, Taiwan, Yunnan) and the Philippines.
Species excluded from Dryopteris
The following related 33 names were historically as-
signed to Acrophorus or Diacalpe but should be excluded from
Dryopteris based on our study of protologues, literature (e.g.,
Christensen, 1905; Copeland, 1927; Fraser-Jenkins, 2008; Kato
& Tsutsumi, 2008; Lehtonen & al., 2010), personal commu-
nications, and examination of corresponding type material,
specimens, and illustrations.
Acrophorus aff inis (J. Sm.) Moore in Proc. Linn. Soc. Lon-
don 2: 286. 1854 Leucostegia affinis J. Sm. in J. Bot.
(Hooker) 3: 416. 1841 Davallia affinis (J. Sm.) Hook., Sp.
Fil. 1: 158, t. 52B. 1845 ?= Davallodes hymenophylloides
(Blume) M. Kato & Tsutsumi in Acta Phytotax. Geobot.
59(1): 12. 2008.
Acrophorus assamicus Bedd., Ferns Brit. India: t. 94. 1865
Davallia assamica (Bedd.) Baker in Hooker & Baker, Syn.
Fil.: 452. 1868; ed. 2: 467. 1874.
Acrophorus bifidus (Kaulf.) T. Moore, Index Fil.: xci. 1857 Da-
vallia bifida Kaulf., Enum. Filic.: 222. 1824 ≡ Lindsaea bi-
fida (Kaulf.) Mett. ex Ku hn., Chaetopterides: 346. 1882; Fes t-
schr. 50 Jähr. Jub. Königstädt. Realschule Berlin: 26. 1882.
Acrophorus chaerophyllus Moore in Proc. Linn. Soc. London 2:
286. 1854 = Davallodes pulchra (D. Don) M. Kato & Tsu-
tsumi in Acta Phytotax. Geobot. 59(1): 13. 2008.
Acrophorus cuneifolius (C. Presl) T. Moore, Index Fil.: 41.
1857 ≡ Lindsaea cuneifolia C. Presl, Reliq. Haenk. 1(1):
60. 1825 (“Lindsaya cuneifolia) = Odontosoria retusa
(Cav.) J. Sm. in Seemann, Bot. Voy. Herald: 430. 1857 –
Holotype: Philippines, Luzon, 1792, Thaddaeus Haenke
s.n. (PR- 612486!).
Acrophorus falcinellus (C. Presl) T. Moore, Index Fil.: 2. 1857
Davallia falcinella C. Presl, Reliq. Haenk. 1: 66. t. 11,
f. 2. 1825 ≡ Trogostolon falcinellus (C. Presl) Copel. in
Philipp. J. Sci. 34: t. 4. 1927.
Acrophorus goudotianus (Kun ze) T. Moore, Index Fil.: 2. 1857
Davallia goudotiana Kunze, Analecta Pteridogr.: 35.
1837 Lindsaea goudotiana (Kunze) Mett. ex Kuhn,
Filic. Afr.: 68. 1868 ≡ Sphenomeris goudotiana (Kunze)
Tardieu in Mém. Inst. Sci. Madagascar, Sér. B, Biol. Vég.
7: 36. 1956.
Acrophorus hemipterus (Bory) T. Moore, Index Fil.: 295. 1861
Davallia hemiptera Bory in Bélanger, Voy. Indes Or.
2: 73, t. 7, f. 2. 1833 = Lindsaea repens var. hemiptera
(Bory) Alderw.
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Acrophorus hispidus Moore”, Proc. Linn. Soc. London 2:
286. 1854, nom. nud. = Leptolepia novae-zelandiae (Col.)
Kuhn, Chaetopterides: 28. 1882; Festschr. 50 hr. Jub.
Königstädt. Realschule Berlin: 26. 1882.
Acrophorus hookeri T. Moore ex Bedd., Ferns Brit. India: t. 95.
1865Araiostegia hookeri (T. Moore ex Bedd.) Ching in
Chien & Chun, Fl. Reipubl. Popularis Sin. 2: 291. 1959
Araiostegiella hookeri (T. Moore ex Bedd.) Fraser-Jenk.,
Taxon. Revis. Indian Subcontinental Pteridophytes: 355.
2008.
Acrophorus hymenophylloides (Blume) T. Moore, Index Fil.:
2. 1857 ≡ Lindsaea hymenophylloides Blume, Enum.
Pl. Javae 2: 218. 1828 ≡ Davallodes hymenophylloides
(Blume) M. Kato & Tsutsumi – Holotype: Indonesia, Java,
(L; isotype: Herb. G. Mettenius in B-200145209!).
Acrophorus hymenophyllus Parish ex Bedd., Ferns Brit. In-
dia: t. 96. 1865 Holotype: Myanmar, near Moulmein,
1860, C.S. Parish s.n. (P-00630810!; isot ype: P-00630809!)
= Tectaria hymenophylla (Bedd.) Holttum in Indian
Fern J. 1(1–2): 35. 1985.
Acrophorus immersus (Wall. ex C. Presl) T. Moore in Proc.
Linn. Soc. London 2: 286. 1854 ≡ Leucostegia immersa
Wall. ex C. Presl, Tent. Pterid.: 95, pl. 4, f. 11. 1836 ≡
Davallia immersa Wall. ex Hook., Sp. Fil. 1: 156. 1845
Humata immersa (Wall. ex C. Presl) Mett., Fil. Hort. Bot.
Lips.: 102. 1856.
Acrophorus imrayanus (Hook.) T. Moore, Index Fil.: 295. 1861
Saccoloma imrayanum Hook. in Kunze, Farrnkräuter 1:
86. 1842 ≡ Lindsaea imrayana ( Hook .) Pérez Abreláez,
Bot. Abh. 14: 55. 1928 Ormoloma imrayanum ( Hook.)
Maxon in Proc. Biol. Soc. Washington 46: 144. 1933.
Acrophorus jamaicensis (Hook.) T. Moore in Proc. Linn. Soc.
London 2: 286. 1854 ≡ Davallia jamaicensis Hook., Sp.
Fil. 1: 183. 1845 Microlepia jamaicensis (Hook.) Fée,
Mém. Foug. 11: 92. 1866.
Acrophorus javensis (Willd.) T. Moore, Index Fil.: 2. 1857
Aspidium javense Willd., Sp. Pl., ed. 4, 5: 284. 1810 ≡
Cystopteris javensis (Willd.) Desv. in Mém. Soc. Linn.
Paris 6(3): 265. 1827 – Holotype: Indonesia, Java, W. Ven-
tenat s.n. (B-W-19830- 010!) = Hypolepis alpina (Blume)
Hook., Sp. Fil. 2: 63. 1852.
Acrophorus macraeanus (Hook. & Arnott) Carruth. ex See-
mann, Fl. Vit.: 336. 1873 Davallia macraeana Hook.
& Arn., Bot. Beechey Voy.: 108. 1832 Lindsaea repens
var. macraeana (Hook. & Arn.) Mett. ex Kuhn in Ann.
Mus. Bot. Lugduno-Batavi 4: 277. 1869.
Acrophorus membranulosus (Wall. ex Hook.) T. Moore
in Proc. Linn. Soc. London 2: 286. 1854 ≡ Davallodes
membranulosa (Wall. ex Hook.) Copel. in Philipp. J. Sci.
34(3): 245. 1927.
Acrophorus multidentatus (Wall. ex Hook.) Bedd., Ferns Brit.
India 3: 2. 1870 ≡ Davallia multidentata Wall. ex Hook.
in Hooker & Baker, Syn. Fil.: 91. 1867 ≡ Davallodes mul-
tidentata (Wall. ex Hook.) M. Kato & Tsutsumi in Acta
Phytotax. Geobot. 59(1): 13. 2008.
Acrophorus parkeri (Hook.) T. Moore, Index Fil.: xci. 1857
Davallia parkeri Hook., Sp. Fil. 1: 176, t. 53C. 1845
Lindsaea parkeri (Hook.) Kuhn., Chaetopterides: 26.
1882; Festschr. 50 Jäh r. Jub. Königstädt. Realschule Berlin:
26. 1882.
Acrophorus parvulus (Wall. ex Hook. & Grev.) Moore in Proc.
Linn. Soc. London 2: 286. 1854 ≡ Davallia parvula Wall.
ex Hook. & Grev., Icon. Filic.: t. 138. 1829 ≡ Leucostegia
parvula (Wall. ex Hook. & Grev.) J. Sm. in London J. Bot.
1: 426. 1842 ≡ Humata parvula (Wall. ex Hook. & Grev.)
Mett., Fil. Hort. Bot. Lips.: 102, t. 27 f. 7, 8. 1856 – Holo-
type: Singapore, Nathaniel Wallich s.n. (?K; isotype: Herb.
J.H. Redfield 2124 [MO-1865420!]).
Acrophorus pseudocystopteris (Kunze) T. Moore, Index Fil.:
3. 1857 ≡ Davallia pseudocystopteris Kunze in Bot. Zei-
tung (Berlin) 6: 68. 1850 ≡ Davallodes pseudocystopteris
(Kunze) M. Kato & Tsutsumi in Acta Phytotax. Geobot.
59(1): 13. 2008.
Acrophorus pulcher (D. Don) T. Moore, Index Fil.: 3. 1857 ≡
Davallia pulchra D. Don, Prod r. Fl. Nepal.: 11. 1825Ara-
iostegia pulchra (D. Don) Copel. in Philipp. J. Sci. 34: 241.
1927 Davallodes pulchra (D. Don) M. Kato & Tsutsumi
in Acta Phytotax. Geobot. 59(1): 13. 2008.
Acrophorus repens (Bory) T. Moore, Index Fil.: xci. 1857 ≡
Dicksonia repens Bory, Voy. Iles Afrique 2: 323. 1804 ≡
Lindsaea repens (Bory) Thwaites, Enum. Pl. Zeyl.: 388.
1864.
Acrophorus tenuifolius (Blume) T. Moore, Index Fil.: xci. 1857
Lindsaea tenuifolia Blume, Enum. Pl. Javae 2: 219. 1828.
Acrophorus thomsonii T. Moore”, Index Fil.: 4. 1857, nom.
nud. = Davallodes multidentata (Wall. ex Hook.) M. Kato
& Tsutsumi.
Diacalpe burgessiana (Gerr.) Trevis. in Nuovo Giorn. Bot. Ital.
7: 161. 1875 Woodsia burgessiana Gerrard in Hooker
& Baker, Syn. Fil.: 48. 1866.
Diacalpe foeniculacea (Hook.) C.B. Clarke in Tra ns. Linn. Soc.
London, Bot. 1(7): 434. 1880 ≡ Aspidium foeniculaceum
Hook., Sp. Fil. 4: 36, t. 237. 1862 ≡ Lastrea foeniculacea
(Hook.) Bedd., Ferns Brit. India: t. 36. 1865 ≡ Polysti-
chum foeniculaceum (Hook.) J. Sm., Hist. Fil.: 220. 1875
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Akaike, H. 1974. A new look at the statistical model identification.
I.E.E.E. Trans. Automatic Control 19: 716–723.
Blockeel, T.L. 2006. The liverworts, mosses and ferns of Europe. Col-
chester: Harley Books.
Ching, R.-C. 1938. A revision of the Chinese and Sikkim-Himalayan
Dryopteris with reference to some species from neighboring re-
gions. Bull. Fan Mem. Inst. Biol. 8: 157–268, 275–334, 363–507.
Ching, R.-C. 1949. The study of Chine se fern s XXXV. Bull. Fan Mem.
Inst. Biol., n.s., 1: 267–314.
Ching, R .-C. 1966. Three new fern genera. Acta Phytotax. Sin. 11: 17–19.
Ching, R.-C. 1978. The Chinese fern families and genera: Systematic
arrangement and historical origin. Acta Phytotax. Sin. 16(3): 1–19.
Chiou, W.-L., Yang, K.-C., Yang, Y.-P., Hsu, K.-S. & Chen, S.-Y.
2000. Type specimens in the herbarium of Taiwan Forestry Re-
search Institute. I, Pteridophyta. Taipei: Taiwan Forestry Research
Institute.
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sequence of extant families and genera of lycophytes and ferns.
Phytotaxa 19: 7–54.
Christensen, C. 1905. Index filicum. Copenhagen: apud H. Hagerup.
Copeland, E.B. 1927. Davallodes and related genera. Philipp. J. Sci.
34: 239–271.
Copeland, E.B. 1947. Genera filicum: The genera of ferns. Waltham:
Chronica Botanica Co.
Copeland, E.B. 1949. Aspidiaceae of New Guinea. Philipp. J. Sci. 78:
389 475.
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cation with rich floristic sampling: DNA barcoding the pterido-
phyte flora of Japan. PLoS One 5(12): e15136, doi: 10.1371/jou rnal
.pone.0 015136.
Farris, J.S. 1989. The retention index and the rescaled consistency
index. Cladistics 5: 417–419.
Lithostegia foeniculacea (Hook.) Ching in Sin. Contr.
4: 2. 1933 ≡ Arachniodes superba Fraser-Jenk., New Sp.
Syndr. Indian Pteridol.: 39. 1997.
Diacalpe fragilis (Trevir.) Trevis. in Nuovo Giorn. Bot. Ital. 7:
160. 1875 ≡ Dicksonia fragilis Trevir. in Mag. Neuesten
Entdeck. Gesammten Natu rk. Ges. Naturf. Freunde Berlin
7: 155, t. 3 f. 18. 1816 Woodsia fragilis (Trevir.) T. Moore,
Index Fil.: ci. 1857 = Woodsia mollis (Kaulf.) J. Sm. in
J. Bot. (Hooker) 4: 191. 1841.
Diacalpe guatemalensis (Hook.) Trevis. in Nuovo Giorn. Bot.
Ital. 7: 160. 1875 Woodsia guatemalensis Hook., Sp. Fil.
1: 60, t. 21A. 1844 = Woodsia mollis (Kaulf.) J. Sm.
Diacalpe manchuriensis (Hook.) Trevis. in Nuovo Giorn. Bot.
Ital. 7: 160. 1875 ≡ Woodsia manchuriensis Hook., Sec.
Cent. Ferns: 98, pl. 98. 1861.
Diacalpe microphylla (Mett.) T. Moore, Index Fil.: c. 1857 ≡
Cyathea microphylla Mett., Fil. Lechl. 1: 23, t. 3 f. 1–6.
1856 Lectotype (designated here): Peru, Puno, St. Gaban
(Rio San Gaban), Tatanara, Aug 1854, W. Lechler 2569
(P-00633066; isolectotypes: GOET-007209, K-000589966,
K-000589967, K-000589968, P-00633067).
“2160” is possibly a typo of 2569 in the protologue, since
Lechler 2160 is also cited under Cyathea schan-chin Mart.
Diacalpe peruviana (Hook.) Trevis. in Nuovo Giorn. Bot. Ital.
7: 160. 1875 Woodsia peruviana Hook., Sp. Fil. 1: 61,
t. 21B. 1844.
Species insufficiently known
The following names are insufficiently known:
Acrophorus adiantoides (Blume) T. Moore, Index Fil.: xci.
1857 ≡ Aspidium adiantoides Blume, Enum. Pl. Javae 2:
145. 1828 ≡ Saccoloma adiantoides (Blume) C. Presl, Tent.
Pterid.: 126. 1836 ≡ Davallia adiantifolia Hook., Sp. Fil.
1: 176. 1845Odontoloma adiantoides (Blume) C. Presl,
Epimel. Bot.: 97. 1851 Lindsaea adiantoides ( Blume)
Kuhn, Ann. Mus. Bot. Lugduno-Batavi 4: 278. 1869, not
J. Sm. in J. Bot. (Hooker) 3: 415. 1841 – Syntypes: Indo-
nesia, Moluccas.
It is highly likely that this species is not conspecific with
Lindsaea adiantoides J. Sm. (in J. Bot. (Hooker) 3: 415. 1841) –
Holotype: Philippines, Luzon, Hugh Cuming 176 (K; isotypes:
MO-255663!, P-00633754!, P-00633755!).
Diacalpe madagascariensis Fée, Mém. Foug. 5, Gen. Filic.: 339.
1850 – Ty p e: Habitat in insula Nos Beh [Nosy Be] Mada-
gascariensium (Pervillié [Pervillé]) (herbarium unknown).
The type material of Diacalpe madagascariensis Fée was
not found in B, G, or P, where Fée’s material is possibly depos-
ited (Stafleu & Cowan, 1976).
This name might not belong to Dryopteris. It was described
in 1850, a time when Wood sia was often mixed with Diacalpe
(see above). Diacalpe madagascariensis is included neither in
Tardieu-Blot (1958) nor in a recent revision of Dryopteris and
Nothoperanema in Madagascar and neighboring Indian Ocean
islands, including Saint Paul (Roux, 2011).
ACKNOWLEDGEMENTS
We than k two anonymous reviewers, Gerry Moore, and Michael
D. Pirie for valuable suggestions and comments, and the directors
and curators of herbaria AK, BISH, BM, CANB, CDBI, FI, GOET,
HENU, HIB, HITBC, HNWP, HUH, IBK, ISBC, K, KUN, KYO, L,
LBG, MICH, NAS, P, PE, PR, PRC, TAIF, TI, UC, US, and WUG,
for providing access to herbarium material in their care. Thanks go
to the following people for their various help and support: Angela
Bond, Patrick Brownsey, Ewen Cameron, Shi-Yong Dong, Atsushi
Ebihara, Christopher Fraser-Jenkins, Anna Haigh, Hai He, Sabine
Hennequi n, Pet er Hovenka mp, Eliz ab et h Howard, Joachi m W. Ka de -
reit, Takeh iko Kak utani, Ti mote Le Péchon, Marcus Lehner t, Ende
Liu, Samuli Lehtonen, Hong-Mei Liu, Egildo Luccioli, Jin Murata,
Hidetoshi Nagamasu, Tetsuo Ohi-Toma, Hans P. Nooteboom, Leon
Perrie, Haining Qin, Dhahara Ranatunga, Akiko Shimizu, Ota Sida,
Alan R. Smith, James Solomon, Franz Stadler, Nicholas J. Turland,
and Luc Willemse.
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Appendix.
List of taxa sampled with information related to taxonomy, voucher information (for new sequences only) and GenBank accession numbers.
Acrophorus emeiensis Ching: psbA-trnH J X6 48114, rbcL JX648111 (China, Sichuan, L . Zhang 1474, CDBI), rps4-trnS JX535815 (China, Sichuan, L. Zhang
1474, CDBI), trnL JX535916 (Chi na, Sichuan, L. Zhang 1474, CDBI), trnL-F JX535867 (China, Sichuan , L. Zhang 1474, CDBI). A. exstipellatus Chi ng & S.H.
Wu: psbA-trnH JX648115 (China, Guangdong, S .-Y. Dong 3682, IBSC), rbcL JX535857 (China, Guangdong, S.-Y. Dong 36 82, IBSC), trnL JX535914 (China,
Guangdong, S.-Y. Dong 3682, IBSC), trnL-F JX535865 (China, Guangdong, S.-Y. D ong 36 82, IBSC), rps4-trnS JX535813 (China, Guangdong, S.-Y. Dong 3682,
IBSC). A. macrocarpus Ching & S.H. Wu: rbcL DQ054522 (“A. emeiensis Ching”). A. nodosus C. Presl: psbA-trnH AB575693, rbcL AB575065, rps4-trnS
JX535814 (Japan, Kagoshima Pref., S. Tagane & K. Fuse TF111, VS763152, TNS), trnL JX535915 (Japan, Kagoshima Pref., S. Tagane & K. Fuse TF111,
VS763152, TNS), trnL-F JX535866 (Jap an, Kagoshi ma Pref., S. Tagane & K. Fuse TF111, VS763152, TNS). A. paleolatus Pic. Serm . (“A. stipellatus T. Moore”):
rbcL DQ508756 EF463106, trnL and trnL-F DQ514500 EF540696 DQ480130. Acrophorus sp.: rbcL DQ054510 (“A. stipellatus”). Arachniodes aristata (G.
Forst.) Tindale: psbA-trnH AB575697, rbcL AY268851, trnL-F AY268782. A. assamica (Ku hn) Ohw i: rps4-t rnS DQ191891. A. denticulata (Sw.) Ching: psbA-
trnH JN189425, rbcL JN189533, rps4-trnS JN189207, trnL-F JN189102 . A. rhomboidea (Wall. ex Mett.) Ching: psbA-trnH JN189424 , rbcL JN189532, rps4-trnS
JN189206, trnL-F DQ514485. Cyrtomium falcatum C. Presl: psbA-trnH AB575726, rbcL A B575726, rps4-trnS AY694796, trnL and trnL-F HQ676521.
C. fort unei J. Sm.: psbA-trnH AB575730, rbcL AB598689, rps4 -trnS AY736348, trnL and trnL-F AY736348. C. macrophyllum (Makino) Tagawa: psbA-trnH
AB575733, rbcL A B575109, rps4-trnS EU106 600, trnL and trnL-F AY736343. Diacalpe annamensis Tagawa: rbcL EF463125, trnL and trnL-F DQ480132
EF540698. D. aspidioides Blume: rbcL DQ054523 EF463126, trnL and trnL-F DQ514490. D. chinensis Ching & S.H. Wu: psbA-trnH JX648117 (China, Yun-
nan, X.-H. Jin & L . Zhang 11221, CDBI), rbcL JX535859 (China, Yunnan, X.-H. Jin & L . Zhang 11221, CDBI), rps4-trnS JX535819 (China, Yunnan, X.-H. Jin
& L. Zhang 11221, CDBI), trnL JX535921 (China, Yunnan, X.-H. Jin & L. Zhang 11221, CDBI), trnL-F JX535872 (China, Yunnan , X.-H. Jin & L. Zhang 11221,
CDBI). D. christensenae Ching: rbcL DQ054518 EF540699, trnL-F DQ480131 EF540699, rps4-trnS DQ480131 EF540699. Dryopteris aemula (Aiton) Ku ntze:
psbA-trnH JN189407, rbcL AY268881, trnL-F AY268816, rps4-trnS J N189189. D. affinis (Lowe) Fraser-Jenk.: psbA-trnH JN189408, rbcL AY268849, rps4-
trnS J N189190, trnL-F AY268849. D. amurensis Christ: psbA-trnH AB575736, rbcL AB 575112, rps4-trnS JX535816 (Japan, Hokkaido Pref., A. Uchida s.n.,
VS768171, TNS), trnL JX535918 (Japan, Hokkaido Pref., A. Uchida s.n ., VS768171, TNS), trnL-F JX535869 (Japan, Hok ka ido Pref., A. Uchida s.n., VS768171,
TNS). D. aquilinoides (Desv.) C. Chr.: psbA-trnH J N189 429, rbcL AY268868, rps4-t rnS J N189211, trnL-F AY268803. D. atrata (Wall) Ching: psbA-trnH
AB575739, rbcL AB 575115, rps4-trnS JX535817, trnL-F JX535919. D. chrysocoma (Ch rist) C. Chr.: psbA-t rnH JN189434, rbcL DQ508773, rps4-trnS DQ191832,
trnL & trnL-F DQ514495. D. cinnamomea (Cav.) C. Chr.: psbA-trnH JN189420, rbcL J N189 528, r ps4-trnS JN189 202, trnL & trnL-F J N189 097. D. corleyi
Fraser-Jenk.: rbcL AY268873, trnL-F AY268808. D. er ythrosora (D. Eaton) Kuntze: psbA-trnH A B575749, rbcL DQ508774, rps4-trnS JN189255, trnL &
trnL-F DQ514496. D. expansa (C. Presl) Fraser-Jenk. & Jermy: psbA-trnH AB575750, rbcL AY268844, rps4-t rnS J N189180, trnL-F AY268775. D. filix-mas
(L.) Schott: psbA-trnH JN189398 , rbcL AY268845, rps4-trnS JN189181, trnL-F AY268776. D. fragrans (L.) Schott: psbA-trnH J N1894 03, rbcL AB575129,
rps4-trnS J N189185, trnL & trnL-F FR731981. D. futura A.R. Sm.: psbA-trnH JN189426, rbcL JN189534, rps4-t rnS J N189208, trnL-F J N189103. D. glabra
(Brack.) Kuntze: rbcL AY268830, trnL-F AY268767. D. guanchica Gibby & Jermy: psbA-trnH J N189463, rbcL J N189573, rps4-trnS JN189246, trnL-F
JN189137. D. hasseltii (Blu me) C. Ch r.: psbA-trnH AB575758, rbcL AB575136 , rps4-trnS DQ191888, trnL & trnL-F DQ514 479. D. hawaiiensis (Hilleb r.) W.J.
Rob.: psbA-trnH JN189 470, rbcL J N189580, rps4-trnS JN189253, trnL-F JN18914 4. D. gymnosora (Makino) C. Chr.: psbA-trnH AB575754, rbcL AB575132,
rps4-trnS JX535824 (China, Henan, L. Zhang & Z.-M. Zhu 1102, CDBI), trnL JX535926 (Ch ina, Hena n, L. Zhang & Z.-M. Zhu 1102, CDBI), trnL-F JX535877
(China, Henan, L. Zhang & Z.-M. Zhu 1102, CDBI). D. polita Rosenst.: psbA-trnH JN189496, rbcL AB575158, rps4-trnS JN1892 81, trnL-F JN189173. D. ru-
brobrunnea W.M. Chu: rbcL JX535862 (Ch ina , Yunnan , X.-H. Jin & L. Zhang 11851, CDBI), rps4-trnS J X535840 (Chi na, Yunnan, X.-H. Jin & L. Zhang 11851,
CDBI), trnL JX535942 (China, Yunnan, X.-H. Jin & L. Zhang 11851, CDBI), trnL-F JX535893 (China, Yunnan, X.-H. Jin & L. Zhang 11851,
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CDBI). D. sieboldii (T. Moore) Kuntze: psbA-trnH AB575790, rbcL AB575169, rps4-tr nS J X535846 (Japan, Miyaz aki Pref., A. Ebihara KS2007-284, VS762696,
TNS), trnL JX535948 (Japan, Miyazaki Pref., A. Ebihara KS2007-284, VS762696, TNS), trnL-F JX535900 (Japan, Miyazaki Pref., A. Ebihara KS2007-284,
VS762696, TNS). D. sparsa (Buch.-Ham. ex D. Don) Kuntze: psbA-trnH AB575794, rbcL AB575173, rps4-trnS JX535849 (Japan, Kagoshima Pref., S. Tagane
& K. Fuse TF018, VS763059, TNS), trnL JX535951 (Japan, Kagoshima Pref., S. Tagane & K. Fuse TF018, VS763059, TNS), trnL-F J X535903 (Jap an, Kagoshi ma
Pref., S. Tagane & K. Fuse TF018, VS763059, TNS). D. tokyoensis (Matsum. & Makino) C. Chr.: psbA-trnH AB575795, rbcL AY268861, rps4 -trnS JN1892 51,
trnL-F AY 268795. D. uniformis (Makino) Makino: psbA-trnH AB575797, rbcL AB57517 7, rps4-trnS J N1680 69, trnL JX535953 (Japan, Chiba Pref., cult.
Tsukuba Botanical Garden, VS774834, TNS), trnL-F JX535905 (Japan, Chiba Pref., cult. Tsukuba Botanical Garden, VS774834, TNS). D. varia (L.) Kuntze:
psbA-trnH AB575798, rbcL AB575178, rps4-trnS JX535852 (Japan, Wakayama Pref., cult. Tsukuba Botanical Garden, VS763911, TNS), trnL JX535954 (Japan ,
Wakayama Pref., cult. Tsukuba Botanical Garden, VS763911, TNS), trnL-F JX535906 (Japan, Wakayama Pref., cult. Tsukuba Botanical Garden, VS763911,
TNS). Notho peranema diacalpioides Ching: rbcL DQ054511 (“N. hendersonii (Bedd.) Ching”), rps4-t rnS DQ191885 (“N. hendersonii”). N. hendersonii (B edd.)
Ching: psbA-t rnH AB575760 JN189439, rbcL AB575138 DQ50 8783 DQ 05450 9 (“N. shikokianum (Ma kino) Ch ing”) EF463135 JN189547, rps4-trnS DQ191885
DQ191886 (“N. shikokianum”) JN189221, trnL D Q514507, trnL-F DQ514507 J N189116. N. rubiginosum (Brack.) A.R. Sm. & D.R. Palmer: rbcL AY268836,
trnL-F AY268771. N. shikokianum (Makino) Ching: psbA-tr nH JX648118 (China, Sichuan, L. Zhang 1472, CDBI), rbcL AB575167 JX648112 (China, Sichuan,
L. Zhang 1472, CDBI), rps4-trnS DQ191886 JX535856 (China, Sichuan, L. Zhang 1472, CDBI ), trnL JX535960 (China, Sichuan, L. Zhang 1472, CDBI), trnL-F
JX535912 (China, Sichuan, L. Zhang 1472, CDBI). N. squamisetum (Hook.) Ching: rbcL DQ054512 EF463182, rps4 -trnS DQ1918 87, trnL JX535961 (China,
Yun nan , S.-Y. Do ng 2788, ISBC), trnL-F JX535913 (Chin a, Yun nan, S.-Y. Dong 2788, ISBC). N. sp.: rbcL EF4 63136 (“N. shikokianum). Peranema cyatheoides
D. Don: rbcL DQ054513. P. luzonicum Cop el.: psbA-trnH JX648119 (China, Sichuan, H. He 1692, CTC), rbcL DQ508784 (“P. cyatheoides D. Don”) JX6 48113
(China, Sichuan, H. He 1692, CTC), rps4-trnS JX648110 (China, Sichuan, H. He 1692, CTC), trnL DQ514509 JX648120 (China, Sichuan, H. He 1692, CTC),
trnL-F DQ514509 (“P. cyatheoides D. Don”) JX648121 (China, Sichuan, H. He 1692, CTC). Polystichum andersonii Hopkins: psbA-trnH JN189401, rbcL
JN189510, rps4-trnS JN189183, trnL-F JN189078 . P. munit um (Kaulf.) C. Presl: psbA-trnH JN18939 9, rbcL JN189508 , rps4-trnS JN189182, trnL-F JN105309.
Phanerophlebia nobilis (S chlecht. & Cham.) C. Presl: psbA-trnH JN189459, rbcL JN189569, rps4-trnS J N189242, trnL-F DQ514511. Polystichopsis muscosa
(L.) C.V. Morton: psbA-trnH JN189 450, rbcL JN189559, rps4-trnS J N189233, trnL-F JN189128. P. pubescens (L.) C. V. Morton: psbA-trnH JN189451, rbcL
JN189560, rps4-trnS JN189234.
Appendix.
Continued.
... Based on molecular phylogenetic evidence, several genera are nested within Dryopteris, such as Acrophorus C. Presl, Acrorumohra (H. Itô) H. Itô, Diacalpe Blume, Dryopsis Holttum & P. J. Edwards, Nothoperanema (Tagawa) Ching and Peranema D. Don (Zhang and Zhang 2012;Zhang et al. 2012). Most species in Dryopteris share a short rhizome and catadromous arrangement of frond segments, compared to its sister genus, Arachniodes Blume, which has long-creeping rhizomes and anadromous laminae (Zhang et al. 2012;Wu et al. 2013). ...
... Based on molecular phylogenetic evidence, several genera are nested within Dryopteris, such as Acrophorus C. Presl, Acrorumohra (H. Itô) H. Itô, Diacalpe Blume, Dryopsis Holttum & P. J. Edwards, Nothoperanema (Tagawa) Ching and Peranema D. Don (Zhang and Zhang 2012;Zhang et al. 2012). Most species in Dryopteris share a short rhizome and catadromous arrangement of frond segments, compared to its sister genus, Arachniodes Blume, which has long-creeping rhizomes and anadromous laminae (Zhang et al. 2012;Wu et al. 2013). ...
... Itô) H. Itô, Diacalpe Blume, Dryopsis Holttum & P. J. Edwards, Nothoperanema (Tagawa) Ching and Peranema D. Don (Zhang and Zhang 2012;Zhang et al. 2012). Most species in Dryopteris share a short rhizome and catadromous arrangement of frond segments, compared to its sister genus, Arachniodes Blume, which has long-creeping rhizomes and anadromous laminae (Zhang et al. 2012;Wu et al. 2013). The species of this genus usually grow in forests, open vegetation and, occasionally, in the rocky area of temperate and tropical regions (Fraser-Jenkins 1986;Kramer et al. 1990;Wu et al. 2013). ...
Article
Full-text available
Dryopteris wulingshanensis , a new species growing on limestone in the Wulingshan Mountains, Hunan, China, is described and illustrated. This species is most similar to D. jishouensis and D. gymnophylla on general morphological traits, such as the form of scales, rhizome and sori, but differs by the number of vascular bundles at the base of the petiole, length to width ratio of lamina, stalk length of basal pinnae, division of the lamina, apex form of the pinnule and habitat. Moreover, molecular phylogenetic analysis using the chloroplast rbc L gene suggested that D. wulingshanensis , as the sister group of D. jishouensis , is a monophyletic clade. According to its restricted geographic range, small populations and few individuals, D. wulingshanensis should be considered endangered, according to the IUCN Red List criteria.
Chapter
Ferns are one of the earliest groups of vascular plants, originated around 400 Ma, that attained remarkable levels of diversity and abundance from the Carboniferous period to the Jurassic period (from c. 300 to 150 million years ago). They were especially prevalent in Paleozoic terrestrial ecosystems, before the rise of seed plants, and maintained their dominance even into the Early Cretaceous (~145 Mya). Many classifications and evolutionary schemes have been proposed reflecting different interpretations based on morphological evidences. Ferns are the only major lineage of vascular plants not represented by a sequenced nuclear genome. However, recent genomic evidences have helped to strengthen the basic understanding of the ideas of possible relationships, and classification has changed accordingly. Now more nuclear data are being available, and new systems of classification are emerging. We have examined such data in the light of available earlier data and systems. This mini review provides an overview of the available information based on nuclear data for future researchers.