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Prado & al. • Phylogenetic relationships among PteridaceaeTA XO N 56 (2) • May 2007: 355–368
355
Phylogenetic relationships among Pteridaceae, including Brazilian
species, inferred from rbcL sequences
Jefferson Prado1, Cristiane Del Nero Rodrigues2, Antonio Salatino2
& Maria Luiza F. Salatino2
1 Instituto de Botânica, Caixa Postal 3005, 01061-970, São Paulo, SP, Brazil. jprado@dialdata.com.br
(author for correspondence)
2 Universidade de São Paulo, Instituto de Biociências, Depart. de Botânica, Caixa Postal 11462, 05422-970,
São Paulo, SP, Brazil
Phylogenetic relationships among Pteridaceae were established using rbcL sequences, parsimony and pos-
terior probabilities. The analyses involved 38 Pteridaceae species native in Brazil (12 of them endemic) and
81 species of Dennstaedtiaceae, Lindsaeaceae, Saccolomataceae (outgroups) and Pteridaceae. The resultant
phylogeny comprehends five main clades: Platyzomatoideae-Pteridoideae-Taenitoideae; Ceratopteris-Acros-
tichum; Adiantoideae-vittarioids; Cheilanthoideae; Coniogramme-Cryptogramma-Llavea. The cladograms
support the most recent classification of Pteridaceae and demonstrate the paraphyly of Cheilanthoideae and
the unnaturalness of Ceratopteridoideae, Platyzomatoideae, Pteridoideae, and Taenitidoideae as traditionally
def ined. Adiantoideae can only be recognized if combined with the vittarioids. Several genera of Pteridaceae
appear to be paraphyletic (e.g., as Cheilanthes, Doryopteris, Pellaea, Pteris), and new generic affinities
suggested by consistent internal clades are proposed.
KEYWORDS: ferns, molecular systematics, pteridophytes, rbcL
INTRODUCTION
The Pteridaceae are ferns distributed worldwide,
especially in the tropics; eleven genera are confined to
the New World and nine to the Old World. Most species
inhabit open, often rocky environments, but representa-
tives of some species of Adiantum and Pteris are frequent
in forests. Habitat preferences in the family imply an un-
usual ecological diversity, with Ceratopteris occurring in
aquatic environments, Acrostichum being often associated
with mangroves and Jamesonia a characteristic páramo
genus. Genera of the subfamily Cheilanthoideae are of-
ten prominent components of the flora of xeric habitats
(Tryon & al., 1990).
There has been a lack of consensus as to the circum-
scription and hierarchical status of infra-familial groups
in Pteridaceae. For example, Ching (1940) recognized two
tribes, Lonchitideae with five genera and 27 species, and
Pterideae with six genera and 275 species. In Lonchitideae
he included some genera now included in Dennstaedtia-
ceae, Dryopteridaceae or Tectariaceae. Copeland (1947)
regarded Pteridaceae as a large family, without subdivi-
sions, comprising 63 genera and including taxa as diverse
as the current Dicksoniaceae and Dennstaedtiaceae.
Pichi Sermolli (1977), however, recognized 10 families
among the genera assigned to Pteridaceae, a classification
that emphasizes some less distinctive groups (Tryon &
al., 1990). In this classification, Pteridaceae s.str. have
only eight genera. More recently, Tryon & Tryon (1982)
recognized six tribes in Pteridaceae, which were raised
to subfamilial level by Tryon (1986). In the treatment of
Tryon & al. (1990) Pteridaceae are divided into subfamilies
Adiantoideae, Ceratopteridoideae, Cheilanthoideae, Plat-
yzomatoideae, Pteridoideae, and Taenitidoideae. Relations
among the genera are complex in the latter treatment, some
groups being highly distinctive while others are poorly
defined. Adiantoideae contain only the genus Adiantum,
recognized by pseudoindusia formed by a revolute and
modified lamina margin where the sporangia are located.
The genus is pantropical, with some species spreading to
the subtropics of both hemispheres, and the species occur
in primary and secondary forests at altitudes ranging from
sea level to 5,000 m in the Andes. There are approximately
200 Adiantum species worldwide (Mickel & Smith, 2004),
59 in Brazil (Prado, 2003). Ceratopteridoideae (genus
Ceratopteris) is also monotypic. It is distinguished by
dimorphic leaves, the sterile fronds bilobed to 3-pinnate,
with anastomosed veins, and the fertile ones 1–5-pinnate,
erect and with narrower segments. The sporangia are borne
distantly on the veins. Ceratopteris is a floating aquatic
fern, with three or four species widespread in the tropics
of both hemispheres (Tryon & al., 1990). Cheilanthoideae
are widespread and distinguished by sporangia borne on
the abaxial side of the lamina, covered or not by a mod-
ified marginal pseudoindusium without veins, sporangia
approximate in sori or soral lines, stipe at base with one
vascular bundle, sometimes with two, in the latter case
with lamina not farinose, stem with scales, rarely with
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TA XO N 56 (2) • May 2007: 355–368Prado & al. • Phylogenetic relationships among Pteridaceae
hairs, and spores without an equatorial flange (Tryon & al.,
1990). The subfamily comprises over 300 species, many
from xeric habitats (Gastony & Rollo, 1995), and 12 gen-
era, six of them confined to America (Tryon & al., 1990).
Platyzoma microphyllum R. Br., endemic to Australia, is
the only member of the monotypic Platyzomatoideae. It
is recognized by sterile fronds, dimorphic (varying from
filiform and short to 1-pinnate and long), articulate pin-
nae, and sporangia with 16 to 32 spores. Taenitidoideae
comprise 15 genera and approximately 130 species, most
from open, terrestrial or rocky environments, some species
occurring in forests alongside streams (Tryon & al., 1990).
Five genera and approximately 250 species, mostly from
forest habitats, compose the Pteridoideae, characterized
by paraphyses, sporangia on a marginal commissure or on
and between anastomosing veins. Pteris is the most diverse
genus, its species exhibiting a great variation in size and
architecture of the lamina. Species of Acrostichum occur
in saline swamps and mangroves.
Some authors (Wagner 1969; Mickel 1974; Tryon &
Tryon 1982; Tryon & al. 1990; Smith, 1995) claim that
Pteridaceae have no obvious relationships with other
groups of living ferns, although they have often been re-
garded as having a general affinit y with the Schizaeaceae
or schizaeoid stock.
According to Tryon & al. (1990), Vittariaceae are
closely related to Pteridaceae, members of both groups
sometimes having been merged in a single familiy, for
example as part of Adiantaceae (Holttum, 1949; Crabbe &
al., 1975). It is now clear that Vittaria and other vittarioid
genera (e.g., Ananthacorus, Hecistopteris, Radiovittaria)
are members of Pteridaceae, with close affinities to
Adiantum (Crane & al., 1995; Hasebe & al., 1995; Crane,
1997; Smith & al., 2006). Molecular phylogenetic stud-
ies (Hasebe & al., 1995; Pryer & al., 2004; Schneider
& al., 2004) have shown that Pteridaceae together with
the Eupolypods make up a monophyletic group and that
Pteridaceae are closely related to the dennstaedtioid ferns.
A recent molecular fern phylogeny (Smith & al., 2006)
places Dennsteadtiaceae and Pteridaceae at a basal and
unresolved position relative the Eupolypods clade.
As yet, no accurate classification for the subfamilies
of Pteridaceae has been achieved and links among infra-
subfamilial groups have hardly been established. Gastony
& Rollo (1995) commented on the difficulties in reaching
a satisfactory classification of the cheilanthoid ferns, one
of the important reasons being the frequent convergence
of characters in the evolution of the group due to harsh
(xerophytic) habitats. A solution to this problem is the use
of molecular markers presumably neutral to the effect of
arid habitats. Recent molecular phylogenetic analyses of
cheilanthoid and related fern groups have used rbcL se-
quences (e.g., Gastony & Rollo, 1995, 1998). This marker
was also used to infer phylogenetic relationships among
species of Anogramma (Pteridaceae-Taenitidoideae) and
between Anogramma and putative relatives, and to deter-
mine generic relationships and subfamilial placement of
Cosentinia vellea (Nakazato & Gastony, 2003).
Sánchez-Baracaldo (2004a), based on sequence data
of the nuclear external transcribed spacer (ETS), plastid
gene rps4 and intergenic spacer rps4-trnS, investigated
the relationships among Jamesonia and Eriosorus (Pter-
idaceae-Taenitidoideae), two traditionally recognized fern
genera in the Neotropics that together form a monophyletic
group. Other relationships of Taetinidoideae based on the
plastid gene sequences rps4 and intergenic spacer rps4-
trnS plus morphological data were studied by Sánchez-
Baracaldo (2004b).
Zhang & al. (2005) carried out a phylogenetic analysis
of cryptogrammoid ferns and related taxa based on rbcL
sequences. The resulting cladogram places Coniogramme,
Cryptogramma and Llavea into a moderately supported
clade, constituting a cryptogrammoid group distantly
related to the cheilanthoid ferns. The latter comprise a
monophyletic and robustly supported clade. Old World
representatives of the cheilanthoid ferns group together
and are distantly related to American members of Chei-
lanthes. The results indicate that Coniogramme should be
included and Onychium excluded from the cryptogram-
moid group.
Smith & al. (2006) provided the most recent arrange-
ment of Pteridaceae, based on morphological and molecu-
lar data. The authors resolve the Pteridaceae as comprising
five monophyletic groups: (1) Parkeriaceae, or Parke-
rioideae (Acrostichum, Ceratopteris); (2) Adiantaceae,
or Adiantoideae (Adiantum plus the vittarioid genera);
(3) Cryptogrammaceae (Coniogramme, Cryptogramma,
Llavea), no subfamily available; (4) Sinopteridaceae, or
Cheilanthoideae; (5) Pteridaceae s.str., or Pteridoideae
(including Pteris plus the taenitioid ferns).
Many rbcL sequences of Pteridaceae are now available
in GenBank. Results obtained so far have shown that rbcL
sequences are variable enough to provide good resolution
across the taxonomic diversity of fern taxa. The present
study provides a cladistic analysis based on rbcL nucleotide
sequences involving Pteridaceae native in Brazil (including
endemic species) and taxa from other regions. The expecta-
tion is that this analysis will likely provide data that might
complement current assumptions about relationships among
the subfamilies of Pteridaceae, as proposed by Tryon &
Tryon (1982) and Tryon & al. (1990), and clarify doubts
regarding their delimitation (Smith & al., 2006).
MATERIAL AND METHODS
Species used in the analysis and respective collec-
tion numbers are listed in the Appendix. Figure 1 shows
357
Prado & al. • Phylogenetic relationships among PteridaceaeTA XO N 56 (2) • May 2007: 355–368
Fig. 1. Brazilian species used for rbcL and phylogenetic analyses. A, Cheilanthes goyazensis; B, Doryopteris collina; C,
Doryopteris ornithopus; D, Pellaea cymbiformis; E, P. gleich enioides; F, P. pinnata; G, P. riedelii; H, Pteris splendens. A–C
by Pe. Lauro; D–G by Thelma Barbarah; H by J. Prado.
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TA XO N 56 (2) • May 2007: 355–368Prado & al. • Phylogenetic relationships among Pteridaceae
some of the Pteridaceae native in Brazil used for DNA
and phylogenetic analyses. Vouchers of Brazilian species
are deposited in SP with some duplicates in SPF. rbcL
sequences of several Dennstaedtiaceae, Lindsaeaceae,
Pteridaceae, and Saccolomataceae species were obtained
from GenBank (Appendix); EF473675–EF473712 rbcL
sequences were newly generated in this study.
Total DNA of species native in Brazil was extracted
from silica gel-dried leaf tissue, following a modified
CTAB method used by Doyle & Doyle (1987). Amplifi-
cations were carried out with rbcL primers 1F and 1351R
(Gastony & Rollo, 1995). Successfully amplified PCR
products were cleaned using GFX PCR purification kit
(Amersham Biosciences). For amplifications for sequen-
cing, primers 1F, 660F, 675R and 1351R (Gastony & Rollo,
1995). Seque nces were obt ained with Applied Biosystems
automated sequencers models 3100 or 3700, using Big Dye
3.0-3.1 (ABI) following protocols of the manufacturer.
DNA sequences were aligned using Clustal X ver-
sion 1.83 (Thompson & al., 1997). Subsequent manual
100
97
83
90
PLATYZOMATOIDEAE / PTERIDOIDEA
TAENITIDOIDEAE
CHEILANTHOIDEAE
Conniogramme fraxinea
Conniogramme japonica
Lonchitis hirsuta
Lonchitis mannii
Dennstaedtia punctifolia
Microlepia punctifolia
Pteridium aquilinum
Pteridium aquilinum
Pteridium esculentum
Saccoloma moluccanum
Saccoloma elegans
89
95
97
77
100
93
100
100
88
100
86
98
Cryptogramma brunoniana
Llavea cordifolia
Saccoloma inaequale
Microlepia szechuanica
Microlepia strigosa
Dennstaedtia samoensis
ACROSTICHUM / CERATOPTERIS
98
100
ADIANTOIDEAE / VITTARIOIDS
66
60
100
CHEILANTHOIDEA E
Fig. 2. Strict consensus tree of the most parsimonious trees (length = 3,201; CI = 0.28; RI = 0.72; 458 parsimony informative
characters) of Pteridaceae (sensu Tryon & Tryon, 1982, and Tryon & al., 1990) and related fern families, based on rbcL
sequences. Digits at the nodes correspond to bootstrap values.
359
Prado & al. • Phylogenetic relationships among PteridaceaeTA XO N 56 (2) • May 2007: 355–368
corrections were carried out with BioEdit version 5.0.9.
The resultant matrix is available from the corresponding
author upon request.
Outgroup members used in this analysis belong to
Dennstaedtiaceae, Lindsaeceae and Saccolomataceae,
families selected based on papers by Hasebe & al. (1995),
Pryer & al. (2004), Schneider & al. (2004) and Smith &
al. (2006) (see Appendix).
Cladistic analyses were run with PAUP* version
4.0b5 (Swofford, 2001) using Fitch parsimony (Fitch,
1971), including autapomorphies, and ACCTRAN op-
timization and heuristic searches. Search strategy used
1,000 replicates of random taxon entry additions, option
MULTREES and tree bisection-reconnection (TBR)
swapping, holding 10 trees per replicate and saving all
shortest trees. Strength of clade support was assessed
using 1,000 bootstrap replicates (Felsenstein, 1985). A
Bayesian Markov chain Monte Carlo (B/MCMC) analy-
sis was carried out, using MrBayes v. 3.06 (Huelsenbeck
& Ronquist, 2001). A hierarchical likelihood ratio test
in Modeltest (Posada & Crandall, 1998) determined a
GTR + I + G as the model of sequence evolution for
the analyzed rbcL dataset. Two independent B/MCMC
analyses were carried out using the above model and
four chains. Chains were run for 5 million generations,
trees being saved after every 1,000 generations. An eval-
uation was conducted to determine the point where the
trees likelihood converged on a maximum value, which
corresponded to 500 trees and 500,000 generations. All
trees prior to this “burn-in” phase were discarded. The
majority-rule consensus and the posterior probabilities
for all resolved nodes were determined.
Fig. 3. Partial cladogram, corresponding to subfamily Cheilanthoideae (sensu Tryon & Tryon, 1982, and Tryon & al., 1990),
based on rbcL sequences and maximum parsimony. Digits at the nodes correspond to bootstrap values. Asterisks indi-
cate species native in Brazil, whose rbcL sequences were determined in the present investigation.
Bommeria ehrenbergiana
Hemionitis elegans
Cheilanthes allosuroides
Cheilanthes horridula
Cheilanthes lanosa
Cheilanthes bonariensis
Notholaena delicatula
Notholaena fendleri
Pellaea andromedifolia
Pellaea pringlei
Pellaea rotundifolia
Pellaea cordifolia
Notholaena sulfurea
Notholaena rosei
Cheilanthes aurea
Cheilanthes californica
Doryopteris concolor
Doryopteris pedata
Doryopteris sagittifolia*
Doryopteris nobilis*
Doryopteris rediviva*
Doryopteris collina*
Doryopteris pentagona*
Pellaea riedelii*
Pellaea cymbiformis*
Pellaea gleichenioides*
Pellaea pinnata*
Doryopteris lomariacea*
Doryopteris paradoxa*
Doryopteris ornithopus*
Cheilanthes goyazensis*
Cheilanthes flexuosa*
Adiantopsis radiata*
Adiantopsis clorophylla*
Trachypteris pinnata
Hemionitis levyi
Hemionitis tomentosa*
Pellaea boivinii
99
99
98
92
81
97
96
95
96
80
74
98
100
72
72
66
51
100
100
84
80
79
87
99
83
96
97
90
93
Pellaea
Doryopteris
Ormopteris
Lytoneuron
→ Pellaea
C
h
e
i
l
a
n
t
h
o
i
d
e
a
e
360
TA XO N 56 (2) • May 2007: 355–368Prado & al. • Phylogenetic relationships among Pteridaceae
RESULTS
The resultant rbcL matrix comprises 1,143 characters.
Among these, 566 are invariable, 119 are variable but phy-
logenetically uninformative, and 458 are informative. The
most parsimonious trees obtained (over 2,000) have 3,201
steps, consistency index 0.28, retention index 0.72 and
homoplasy index 0.76.
Fig. 2 shows the strict consensus tree of 2,000 equally
most parsimonious trees. Members of Lindsaeaceae (Lon-
chitis), Dennstaedtiaceae (Dennstaedtia, Microlepia, Pter-
idium) and Saccolomataceae do not group coherently with
the respective family circumscriptions. For example, the
species of Pteridium (Dennstaedtiaceae) form a clade apart
of that of Dennstaedtia and Microlepia, and Lonchitis hir-
suta and L. mannii (Lindsaeaceae) group with Saccoloma
inaequale (Saccolomataceae). These results indicate that
the families involved are not monophyletic; analyses with
ampler samplings are needed to reach conclusive results
about their relationships. The Lonchitis/Saccoloma inae-
quale clade is closest to the Pteridaceae clade (Fig. 2).
Pteridaceae constitute a monophyletic and supported
group with bootstrap (BS) value of 100. Five clades are
immediately apparent, corresponding to the following
groups: (1) Coniogramme fraxinea, C. japonica, Cryp-
togramma brunoniana, and Llavea cordifolia (all Chei-
lanthoideae sensu Tryon & Tryon, 1982, and Tryon & al.,
1990; all Cryptogrammaceae sensu Smith & al., 2006);
(2) Platyzomatoideae, Pteridoideae and Taenitidoideae;
(3) Ceratopteris and Acrostichum; (4) Adiantoideae plus
vittarioids; and (5) Cheilanthoideae. A basal polytomy
precludes visualizing all phyletic relationships among
these major clades (Fig. 2). Nonetheless, subfamilies
Adiantoideae with vittarioids and part of Cheilanthoid-
eae comprise a moderately supported clade (BS 89). The
cladogram of Fig. 2 evidences that Cheilanthoideae as
delimited by Tryon & Tryon (1982) and Tryon & al. (1990)
is paraphyletic because Coniogramme, Cryptogramma
Antrophyum boryanum
Antrophyum ensiforme
Vittaria dimorpha
Vittaria lineata
Radiovittaria gardneriana
Vittaria stipitata
Haplopteris anguste-elongata
Haplopteris zosterifolia
Haplopteris ensiformis
Haplopteris flexuosa
97
100
100
100
92
100
100
90
56 100
78
100
100
99
97
100
65
100
100
100 57
91
100
100
98
97
100
Hecistopteris pumila
Adiantum capillus-veneris
Adiantum pedatum
Adiantum serratodentatum*
Adiantum terminatum*
Adiantum latifolium*
Adiantum obliquum*
Adiantum cajennense*
Adiantum pentadactylon*
Adiantum subcordatum*
Adiantum raddianum
Adiantum cuneatum*
Adiantum raddianum*
Ananthacorus angustifolius
Vittaria isoetifolia
Vittaria lineata*
Vittaria graminifolia
Polytaenium cajennense
Polytaenium lanceolatum
Polytaenium lineatum
Antrophyum plantagineum
Antrophyum reticulatum
Vittaria remota
Radiovittaria minima
Adiantoideae
Vittarioids
50
Fig. 4. Partial cladogram, corresponding to subfamily Adiantoideae (sensu Tryon & Tryon, 1982, and Tryon & al., 1990) and
vittarioids, based on rbcL sequences and maximum parsimony. For further explanation see Fig. 3.
361
Prado & al. • Phylogenetic relationships among PteridaceaeTA XO N 56 (2) • May 2007: 355–368
and Llavea constitute a distinct clade as suggested by
Smith & al. (2006).
Inside the large Cheilanthoideae clade (Fig. 3) the spe-
cies of Pellaea are distributed in three groups: (1) part of
the species of sect. Pellaea comprise a monophyletic g roup
sharing a supported clade (BS 92) with Notholaena delica-
tula and Cheilanthes bonariensis; (2) four species of Pel-
laea sect. Ormopteris (P. cymbiformis, P. gleichenioides,
P. pinnata, P. riedelii) form a clade (BS 80) with species of
Doryopteris section Lytoneuron; (3) another species of sect.
Pellaea (P. boivinii) has a close affinity with Hemionitis.
Hence, sect. Pellaea is paraphyletic. Doryopteris is also
paraphyletic: the species of sect. Lytoneuron share a clade
(BS 80) with species of Pellaea sect. Ormopteris while
the species of sect. Doryopteris form a clade (BS 98) with
D. concolor, sister to the Lytoneuron/Ormopteris clade.
Cheilanthes is also paraphyletic (or polyphyletic): four
species (C. allosuroides, C. bonariensis, C. horridula, C.
lanosa) constitute a well-supported (BS 98) monophyletic
group, but C. aurea is closely related to Notholaena rosei
and N. sulfurea, C. flexuosa to Adiantopsis, C. goyazensis
to Doryopteris and Pellaea, while C. californica lies in a
basal polytomy of a large clade combining Adiantopsis,
Doryopteris, Hemionitis, Pellaea, Trach ypter i s and other
species of Cheilanthes (Fig. 3). Another cheilanthoid genus
of taxonomic concern is Hemionitis. While H. levyi and H.
tomentosa comprise a clade with BS 92, sister to Pellaea
boivinii, H. elegans is resolved in a clade with Bommeria
Onychium japonicum
Actiniopteris radiata
Onychium lucidum
Anogramma caespitosa
Anogramma leptophylla
Anogramma guatemalensis
Anogramma lorentzii
Cosentinia vellea
Anogramma chaerophylla
Anogramma novogaliciana
Anogramma osteniana
Pteris fauriei
Ceratopteris thalictroides
Pityrogramma calomelanos
Pteris vittata
Anogramma chaerophylla
Pityrogramma calomelanos*
Pityrogramma trifoliata
Jamesonia canescens
Eriosorus flexuosus
Eriosorus myriophyllus*
Taenitis blechnoides
Pteris splendens*
Pteris brasiliensis*
Pteris lechleri*
Pteris denticulata*
Pteris leptophylla*
Pteris decurrens*
Pteris deflexa*
Pteris cretica
Pteris vittata*
Platyzoma microphyllum
Ceratopteris pteridoides
Ceratopteris richardii
Acrostichum danaeifolium*
Acrostichum aureum
95
98
99
96
97
100
69
100
100
72
62
53
78
100
87
98
93
89
94 100
99
100
100
100
100
100
77
Taenitidoideae
Pteridoideae
Platyzomatoideae
Ceratopteridoideae
Pteridoideae
98
Fig. 5. Partial cladogram, corresponding to subfamilies Ceratopteridoideae, Platyzomatoideae, Pteridoideae and Taen-
itidoideae (sensu Tryon & Tryon, 1982, and Tryon & al., 1990), based on rbcL sequences and maximum parsimony. For
further explanation see Fig. 3.
362
TA XO N 56 (2) • May 2007: 355–368Prado & al. • Phylogenetic relationships among Pteridaceae
ehrenbergiana with support (BS 99), at the base of the
Cheilanthoideae main clade (Fig. 3). The two species of
Adiantopsis constitute a clade with BS 97, sister to Chei-
lanthes flexuosa. Trachypteris pinnata is basal and sister
to a clade (BS 79) comprising Adiantopsis, Doryopteris,
Hemionitis, and Pellaea sect. Ormopteris (Fig. 3).
In a large clade including the Adiantoideae plus vittari-
oids (Fig. 4), the latter constitute a clade with BS 100, sister
to a poorly resolved Adiantum group. Vittaria emerges as a
monophyletic genus with BS 100. Radiovittaria is another
monophyletic group (BS 100) sister to Hecistopteris. Poly-
taenium is a consistent group (BS 100), while Anthrophyllum
is paraphyletic, two species (A. plantagineum and A. reticu-
latum) forming a clade basal to a clade (BS 99) comprising
Anantachorus, Polytaenium, Vittaria plus a clade with the
other two Anthrophyllum species (A. boryanum, A. ensifor-
mis) (Fig. 4). The Vittariaceae clade is sister to Adiantoideae,
which constitute a poorly resolved group. Adiantum radia-
num and A. cuneatum form a clade with support of BS 100
and the re seem s to be reasons to consider it as di sti nct from
the other Adiantum group (possibly a subgenus). Another
supported clade (BS 100) is formed by A. serratodentatum,
A. obliquum, A. latifolium, and A. terminatum. The last
main clade in the present rbcL-based phylogeny comprises
members of four currently recognized subfamilies, namely
Ceratopteridoideae, Platyzomatoideae, Pteridoideae and
ADIANTOIDEAE / VITTARIOIDS
CHEILANTHOIDEAE
Lonchitis hirsuta
Dennstaedtia punctifolia
Pteridium aquilinum
Saccoloma moluccanum
100
Llavea cordifolia
Conniogramme fraxinea
Conniogramme japonica
Cryptogramma brunoniana
Microlepia punctifolia
Microlepia szechuanica
Microlepia strigosa
Dennstaedtia samoensis
Saccoloma inaequale
Lonchitis mannii
Pteridium esculentum
Pteridium aquilinum
Saccoloma elegans
100
100
100 100
100 100
100
91
89
98
51
100
100
100
100
100
100
88
PLATYZOMATOIDEAE / PTERIDOIDEAE /
TAENITIDOIDEAE
ACROSTICHUM / CERATOPTERIS
98
100
100
CHEILANTHOIDEA E
Fig. 6. Bayesian halfcompact consensus tree of Pteridaceae (sensu Tryon & Tryon, 1982, and Tryon & al., 1990) and related
fern families, based on rbcL sequences. For further explanation see Fig. 3.
363
Prado & al. • Phylogenetic relationships among PteridaceaeTA XO N 56 (2) • May 2007: 355–368
Taenitidoideae (Fig. 5). Ceratopteris (Ceratopteridoideae)
and Acrostichum (Pteridoideae) form a basal clade, with BS
100 support and coherent and consistent (BS 100) internal
circumscriptions. Pteridoideae are paraphyletic with species
of Pteris lying inside another clade, showing affinity with
Platyzoma (Fig. 5). All Taenitidoideae form a clade, which,
however, lacks support (Fig. 5). Inside Taenitidoideae, Ac-
tiniopteris and Onychium grouped with strong support (BS
95). This clade is sister to a group lacking support (BS 53),
formed by a trichotomy, constituted by clades strongly (BS
100) or moderately (BS 87 and 72) supported. The former is
ma de up of four Anogramma species and Cosentinia vellea.
Because other species of the former genus have closer af-
finities with Pityrogramma, Eriosorus or Jamesonia (Fig.
5), Anogramma is paraphyletic (or polyphyletic). A clade
with BS 100 is fo rme d by Anogramma osteniana, Eriosorus
flexuosus and Jamesonia canescens. But Eriosorus myr-
iophyllus groups consistently (BS 93) with Taenit i s ble ch-
noides (Fig. 5). These results suggest that, with exception
of Pityrogramma, all Taenitidoideae genera sampled in this
study require revision as to their circumscription. Pteris is
paraphyletic. Nine species of the latter genus constitute a
clade with BS 94, but P. vittata seems to have affinity with
Platyzoma microphyllum, both species lying at the base
of the main Pteris clade (Fig. 5). Anogramma is another
paraphyletic genus, formed by two clades, each with BS
100, one akin to Cosentinia and another to Pityrogramma.
The latter association is defined by a clade with BS 72,
but the Pityrogramma species form a supported clade (BS
100). Another Anogramma species, A. osteniana, is akin to
Cheilanthes allosuroides
Cheilanthes horridula
Cheilanthes lanosa
Cheilanthes bonariensis
Pellaea riedelii*
Pellaea cymbiformis*
Pellaea gleichenioides*
Pellaea pinnata*
Doryopteris lomariacea*
Doryopteris paradoxa*
Doryopteris ornithopus*
Cheilanthes goyazensis*
Cheilanthes flexuosa*
Adiantopsis radiata*
Adiantopsis clorophylla*
Trachypteris pinnata
Notholaena delicatula
Notholaena fendleri
Pellaea andromedifolia
Pellaea rotundifolia
Pellaea pringlei
Pellaea cordifolia
Cheilanthes aurea
Notholaena rosei
Notholaena sulfurea
Cheilanthes californica
Doryopteris concolor
Doryopteris pedata
Doryopteris sagittifolia*
Doryopteris nobilis*
Doryopteris rediviva*
Doryopteris collina*
Doryopteris pentagona*
Hemionitis levyi
Hemionitis tomentosa*
Pellaea boivinii
Bommeria ehrenbergiana
Hemionitis elegans
100
100
100
100 100
100
100
100
61
100
100 99
100
100 100
100
93
87
65
100
100
100
81
99
100
100
98
100
99
100
100
100
Pellaea
Doryopteris
Ormopteris
Lytoneuron
Pellaea
C
h
e
i
l
a
n
t
h
o
i
d
e
a
e
¤
100
Fig. 7. Partial cladogram, corresponding to subfamily Cheilanthoideae (sensu Tryon & Tryon, 1982, and Tryon & al., 1990),
based on rbcL sequences and Bayesian analysis. For further explanation see Fig. 3.
364
TA XO N 56 (2) • May 2007: 355–368Prado & al. • Phylogenetic relationships among Pteridaceae
Eriosorus, Jamesonia, and Taenitis, an affinity defined by a
clade with BS 87, but with an internal supported clade (BS
100) formed by Anogramma and Eriosorus (Fig. 5). The
topology of the commented clades suggests that Eriosorus
is paraphyletic.
Figure 6 shows the Bayesian halfcompact consensus
tree, with posterior probabilities at the clade nodes. The
topology of this Bayesian phylogeny is similar to the Max-
imum parsimony (MP) phylogeny. A difference comparing
Figs. 2 and 6 refers to the outgroup clade, which is closest
to Pteridaceae: while the MP phylogeny indicates the
Lonchitis/Saccoloma, the Bayesian analysis points to the
Dennstaedtia/Microlepia clade. Another relevant difference
between the two analyses refers to the resolution among
major Pteridaceae clades: while the MP analysis ended
up in a trichotomy (Fig. 2), the Baysian analysis yielded a
completely resolved tree (Fig. 6). As in the MP phylogeny,
the Coniogramme/Cryptogramma/Llavea cla de is sist er to
the larger Pteridaceae clade in the latter analysis.
With regard to subfamilies, the similarities between
the results obtained with the two methods are again
very high. Thus, topologies of the main Cheilanthoideae
clade, are identical (Figs. 3, 7). BS values and posterior
probabilities (PP) are roughly proportional comparing
one and another phylogeny, PP figures invariably being
higher, as is typical in such comparisons. Topologies of
Adiantoideae phylogenies are highly similar (Figs. 4, 8),
the only differences being: (1) MP analysis resulted in
two trichotomies while Bayesian analysis rendered a com-
pletely resolved cladogram; and (2) consistencies of the in-
ner clades, characterized by higher values in the Bayesian
analysis. As to the Ceratopteridoideae/Platyzomatoideae/
Pteridoideae/Tenitidoideae clade, the MP and Bayesian
topologies are also highly similar (Figs. 5, 9), but incom-
Adiantum capillus-veneris
Adiantum pedatum
Adiantum terminatum*
Adiantum latifolium*
Adiantum obliquum*
Adiantum serratodentatum*
Adiantum cajennense*
Adiantum pentadactylon*
Adiantum subcordatum*
Ananthacorus angustifolius
Antrophyum boryanum
Antrophyum ensiforme
Vittaria dimorpha
Vittaria lineata
Vittaria isoetifolia
Vittaria lineata*
Vittaria graminifolia
Polytaenium cajenense
Polytaenium lanceolatum
Polytaenium lineatum
Antrophyum plantagineum
Antrophyum reticulatum
Hecistopteris pumila
Radiovittaria gardneriana
Radiovittaria stipitata
Radiovittaria remota
Radiovittaria minima
Haplopteris anguste-elongata
Haplopteris zosterifolia
Haplopteris ensiformis
Haplopteris flexuosa
Adiantum raddianum
Adiantum cuneatum*
Adiantum raddianum*
88
100
70
96
100
92
100
78
100
100
58
94 99
100
100
100
99 100
100
100
100
100
100
86
62
100
100
100
100
100
100
100
Adiantoideae
Vittarioids
Adiantoideae
Fig. 8. Partial cladogram, corresponding to subfamily Adiantoideae (sensu Tryon & Tryon, 1982, and Tryon & al., 1990) and
vittarioids, based on rbcL sequences and Bayesian analysis. For further explanation see Fig. 3.
365
Prado & al. • Phylogenetic relationships among PteridaceaeTA XO N 56 (2) • May 2007: 355–368
pletely resolved. They are complementary, with uncer-
tainty due to polytomy in one analysis being clarified by
complete resolution of the same clades in the other. For
example, the polytomy in the Bayesian phylogeny of Plat-
yzoma microphyllum, Pteris vittata and the Pteridoideae
and Taenitidoideae clades (Fig. 9) is resolved in the MP
phylogeny (Fig. 5). Similary, the obscure relationships
among the Anogramma/Cosentinia (BS 100), Anogramma/
Pityrogramma (BS 72) and Anogramma/Eriosorus/Jame-
sonia/Taenitis (BS 87) clades in the MP phylogeny are
resolved in the Bayesian phylogeny (Fig. 9).
DISCUSSION
The rbcL gene has been the preferred DNA region by
far for inferring phylogenies at the family level and above
(Soltis & Soltis, 1998). It should follow that the gene is
too conserved and inappropriate for comparisons at lower
taxonomic levels. This is often true regarding angiosperm
phylogeny. For other groups of photosynthetic organisms
including pteridophytes, however, rbcL has been shown
phylogenetically useful at a broad range of taxonomic
hierarchy (e.g., Wolf, 1995; Wolf & al., 1998; and other
refs. cited in the Introduction). It could be reasoned that
applicability of rbcL at lower hierarchic levels is a conse-
quence of the antiquity of the group and the consequent
accumulation of nucleotide substitutions over the several
hundred s of m illion years of pteridophy te evolution. T his
is probably not true for ferns, because it has been shown
by means of molecular chronology that most extant fern
groups, including 80% of polypods, have origins nearly
as recent as those of many angiosperm taxa (Pryer & al.,
2004). The origin of the pteridoids in particular has been
Actiniopteris radiata
Onychium japonicum
Onychium lucidum
Anogramma caespitosa
Anogramma leptophylla
Anogramma guatemalensis
Anogramma lorentzii
Consentinia vellea
Anogramma chaerophylla
Anogramma chaerophylla
Anogramma novogaliciana
Pityrogramma calomelanos
Pityrogramma trifoliata
Pityrogramma calomelanos*
Anogramma osteniana
Jamesonia canescens
Eriosorus flexuosus
Eriosorus myriophyllus*
Taenitis blechnoides
Pteris splendens*
Pteris brasiliensis*
Pteris lechleri*
Pteris denticulata*
Pteris leptophylla*
Pteris decurrens*
Pteris deflexa*
Pteris cretica
Pteris vittata
Pteris vittata*
Platyzoma microphyllum
Ceratopteris thalictroides
Ceratopteris pteridoides
Ceratopteris richardii
Acrostichum danaeifolium*
Acrostichum aureum
100
100
100
100
100
100
100
100
100 100
100
68
100
100
Taenitidoideae
Pteridoideae
Ceratopteridoideae
Pteridoideae
Platyzomatoideae
100
100
100
100 100
100
68
100
100
100
100
87
100
89
100
100
100
100
100
100
100
100
100
100
100 100
68
100
100
100
100
Pteris fauriei
100
100
Fig. 9. Partial cladogram, corresponding to subfamilies Ceratopteridoideae, Platyzomatoideae, Pteridoideae, and Taenit-
idoideae (sensu Tryon & Tryon, 1982, and Tryon & al., 1990), based on rbcL sequences and Bayesian analysis. For further
explanation see Fig. 3.
366
TA XO N 56 (2) • May 2007: 355–368Prado & al. • Phylogenetic relationships among Pteridaceae
estimated at less than 100 million years (Schneider & al.,
2004). Hasebe & al. (1995) concluded that Ks and Ka
values between families and between genera within fam-
ilies are higher in ferns than in angiosperms. Given that
most extant fern groups are not substantially older than
angiosperms, nucleotide substitution rates are probably
faster in ferns, which makes rbcL sequences useful for
phylogenetic analysis even at the interspecific level.
The present analyses support the classification of
Pteridaceae by Smith & al. (2006); both our cladograms
(Figs. 2 and 6) and the mentioned classification recognize
five groups within the family and in both the composition
of the groups is si milar. From t he 54 gene ra list ed in Sm ith
& al. (2006) as comprising the Pteridaceae, the present
analyses included 32, i.e., nearly 60%. The present MP
phylogeny is in agreement with previous suggestions
that Dennstaedtiaceae is probably the group closest to
Pteridaceae (Hasebe & al., 1995; Pryer & al., 1995, 2004;
Schneider & al., 2004; Smith & al., 2006). However, the
Bayesian analysis suggests that Lindsaeaceae may be
closer to Pteridaceae than Dennstaedtiaceae.
Platyzomatoideae seem to be the subfamily with
closest affinities with the Pteridoideae. Similar results
have been reported by Hasebe & al. (1995) and Pryer
& al. (1995, 2004). While Adiantoideae, including the
vittarioid genera (formerly assumed as comprising the
family Vittariaceae, Tryon & al., 1990), form a consist-
ent monophyletic group, Pteridoideae are paraphyletic,
because Acrostichum groups with Ceratopteris (Figs. 5,
9). This association was previously reported by Pryer &
al. (1995) and Hasebe & al. (1995), and is one of the five
monophyletic groups in Pteridaceae accepted by Smith &
al. (2006). Results of the present work are coherent with
the other assumed monophyletic groups: (1) Adiantoid-
eae (Adiantum plus vittarioid genera; Figs. 4, 8); (2) the
Cheilanthoideae Coniogramme/Cryptogramma/Llavea
(Figs. 2, 4); (3) the remainder Cheilanthoideae (Figs. 3,
7); (4) Pteridoideae without Acrostichum and with Taenit-
idoideae (Figs. 5, 9). The close phyletic affinities between
Taenitidoideae and Pteridoideae have already been noticed
by Sánchez-Baracaldo (2004a, b). Taenitidoideae require
further study; the present results suggest segregation of
Actinopteris and Onychium (Figs. 5, 9) to constitute a
group of their own. The Coniogramme/Cryptogramma/
Llavea clade (BS 100; Figs. 2, 6) in a sister condition to the
rest of the Pteridaceae suggests segregation of these taxa
from Cheilanthoideae, in disagreement with Tryon & al.
(1990) and in accordance with Zhang & al. (2005).
The need of redefinit ion of some genera as evidenced
by the present results, for example in the case of Cheilan-
thes, had already been pointed out by Smith & al. (2006).
The uncertainty as to the status of Pteris is now clarified:
the genus is paraphyletic and may acquire monophyly if
P. vittata is segregated. Similarly, Adiantum would gain
monophyly only if Adiantum cuneatum and A. radianum
were segregated to another taxon (Figs. 4, 8). Further
examples are commented on above.
Traditionally, Pteridaceae has been one of the largest
fern families. The recent inclusion of the vittarioid gen-
era turned it into an even larger group. The existence of
consistent clades inside the Pteridaceae now seems firmly
consolidated. However, the molecular analyses indicate
that much further work is needed to eliminate the many
paraphylies and polyphylies pervading the family.
ACKNOWLEDGMENTS
The authors thank CNPq (Conselho Nacional do Desen-
volvimento Científico e Tecnológico, Brasil) for provision of
funds.
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Appendix. Species of Pteridaceae, Dennstaedtiaceae, Lindsaeaceae, Saccolomataceae and vittarioids used in the phy-
logenetic inference based on rbcL sequences, with respective numbers of collection, localities in Brazil (AC, Acre; MG,
Minas Gerais; RJ, Rio de Janeiro; SP, São Paulo States) and numbers of GenBank accession.
FAMILY, Subfamily, Species, Numbers of collection, Localities in Brazil, References, Numbers of GenBank accession;
PTERIDACEAE, Adiantoideae, Adiantum cajennense Willd., Prado & al. 1201, AC: Cruzeiro do Sul, this study, EF473675; A.
capillus-veneris L., – , – , Hasebe & al. (1993), D14880; A. cuneatum Langsd. & Fisch., Prado & Yano 1078, SP: Cunha, this study,
EF473676; A. latifolium Lam., Prado & al. 1294, AC: Cruzeiro do Sul, this study, EF473677; A. obliquum Willd., Prado & al. 1345,
AC: Cruzeiro do Sul, this study, EF473678; A. pedatum L., – , – , Hasebe & al. (1994), U05602; A. pentadactylon Langsd. & Fisch.,
Prado & al. 1085, RJ: Petrópolis, this study, EF473679; A. raddianum C. Presl., Prado & Yano 1077, SP: Cunha , th is s tudy, EF47368 0;
A. raddianum C. Presl., – , – , Wolf & al. (1994), U05906; A. serratodentatum Humb. & Bonpl. ex Willd., Prado & al. 1545, SP:
Ubatuba, th is study, EF473681; A. subcordatum Sw., Prado & Yano 1075, SP: Cunha, this study, EF473682; A. terminatum Kunze ex
Miq., Prado & al. 1354, AC: Cruzeiro do Sul, this study, EF473683; Ceratopteridoideae, Ceratopteris pteridoides (Hook.) Hieron.,
– , – , Masuyama & al. (2002), AB059584; C. richardii Brongn., – , – , Masuyama & al. (2002), AB059585; C. thalictroides (L.) Brongn.,
– , – , Hasebe & al. (1994), U05609; Cheilanthoideae, Adiantopsis chlorophylla (Sm.) Fée, Prado & Yano 1047, SP: Campos do Jordão,
368
TA XO N 56 (2) • May 2007: 355–368Prado & al. • Phylogenetic relationships among Pteridaceae
this study, EF473684; A. radiata (L.) Fée, Prado & Yano 1046, SP: Campos do Jordão, this study, EF473685; Bommeria ehrenber-
giana (Klotzsch) Underw., – , – , Gastony & Rollo (1995), U19497; Cheilanthes allosuroides Mett., – , – , Gastony & Rollo (1995),
U27239; C. aurea Baker, – , – , Gastony & Rollo (1995), U28786; C. bonariensis (Willd.) Proctor, – , – , Gastony & Rollo (1995),
U19499; C. californica (Hook.) Mett., – , – , Gastony & Johnson (2001), AF336101; C. flexuosa Kunze, Forza & Mello-Silva 1503,
MG: Diamantina, this study, EF473686; C. goyazensis (Taub.) Domin, Prado & B.-Blubaugh 1403, MG: Diamantina, this study,
EF473687; C. horridula Maxon, – , – , Gastony & Rollo (1995), U27448; C. lanosa (Michx.) D.C. Eaton, – , – , Gastony & Rollo (1995),
U27205; Coniogramme fraxinea (Don) Diels, – , – , Korall & al. (2006), AM177359; C. japonica (Thunb.) Diels, – , – , Hasebe & al.
(1994), U05611; Cryptogramma brunoniana Wall., – , – , Zhang & al. (2004), AY266407; Doryopteris collina (Raddi) J. Sm., Prado
& B.-Blubaugh 1402, MG: Diamantina – , – , this study, EF473688; D. concolor (Langsd. & Fisch.) Kuhn, – , – , Hasebe & al. (1994),
U05621; D. lomariacea Klotzsch, Prado & Yano 1045, SP: Campos do Jordão, this study, EF473689; D. nobilis (T. Moore) C. Chr.,
Prado & al. 1119, RJ: Itatiaia, this study, EF473690; D. ornithopus (Hook. & Baker) J. Sm., Prado & B.-Blubaugh 1399, MG: Gouveia ,
this study, EF473691; D. paradoxa (Fée) Chirst., Prado & al. 1131, RJ: Itatiaia, this st udy, EF473692; D. pedata (L.) Fée, – , – , Gastony
& Rollo (1995), U27206; D. pentagona Pic. Serm., Prado & al. 1100, RJ: Sta. Maria Magdalena, this study, EF473693; D. rediviva
Fée, Prado & al. 1107, RJ: Itatiaia, this study, EF473694; D. sagittifolia (Raddi) J. Sm., Prado & al. 1108, RJ: Itatiaia, this study,
EF473695; Hemionitis elegans Davenp., – , – , Gastony & Rollo (1995), U27729; H. levyi Fourn., – , – , Gastony & Rollo (1995), U27725;
H. tomentosa (Lam.) Raddi, Prado & al. 1092, RJ: Nova Friburgo, this study, EF473696; Llavea cordifolia Lag., – , – , Gas tony &
Rollo (1995), U27726; Notholaena delicatula Maxo & Weath., – , – , Gastony & Rollo (1995), U19500; N. fendleri Kunze, – , – , Gastony
& Rollo (1995), U27727; N. rosei Maxon, – , – , Gastony & Rollo (1995), U27728; N. sulphurea (Cav.) J. Sm., – , – , Gastony & Rollo
(1995), U28254; Pellaea andromedifolia (Kaulf.) Fée, – , – , Gastony & Rollo (1995), U19501; P. boivinii Hook., – , – , Gastony & Rollo
(1995), U29132; P. cordifolia (Sessé & Moc.) A.R. Sm., – , – , Gastony & Rollo (1995), U28253; P. cymbiformis J. Prado, Prado &
B.-Blubaugh 1404, MG: Gouveia, this study, EF473697; P. gleichenioid es (Hook.) Christ, Prado & B.-Blubaugh 1398, MG: Gouveia,
this study, EF473698; P. pinnata (Kaulf.) Prantl, Prado & B.-Blubaugh 1407, MG: Diamantina, this study, EF473699; P. pringlei
Davenp., – , – , Gastony & Rollo (1995), U28787; P. ried elii Baker, Forza & Mello-Silva 1515, MG: Diamantina, this study, EF473700;
P. rotundifolia (G. Forst.) Hook., – , – , Gastony & Rollo (1995), U28788; Tra chy pt eri s pinnata (Hook. f.) C. Chr., – , – , Gastony &
Rollo (1995), U27450; Platyzomatoideae, Platyzoma microphyllum R. Br., – , – , Nakazato & Gastony (2003), AY168721; Pteridoi-
deae, Acrostichum aureum L., – , – , Hasebe & al. (1994), U05601; A. danaeifolium Langsd. & Fisch., Prado & al. 1536, SP: Ubatuba,
this study, EF473701; Pteris brasiliensis Raddi, Prado & al. 1086, RJ: Petrópolis, this study, EF473702; P. cretica L., – , – , Gastony
& Johnson (2001), AF360360; P. decurrens C. Presl., Prado & Yano 1082, SP: Sto. André, this study, EF473703; P. deflexa Link,
Prado & al. 1089, RJ: Petrópolis, this study, EF473704; P. denticulata Sw., Prado & al. 1084, RJ: Petrópolis, this study, EF473705;
P. fauriei Hieron., – , – , Hasebe & al. (1994), U05647; P. lechleri Mett., Prado & al. 1093, RJ: Nova Friburgo, this study, EF473706;
P. le ptophylla Sw., Boldrin & al. 160, SP: Guarujá, this study, EF473707; P. splend ens Kaulf., Prado 1131a, SP: São Paulo, this study,
EF473708; P. vittata L., Salatino s.n., SP: São Paulo, this study, EF473709; P. vittata L., – , – , Wolf & al. (1994), U05941; Taenitidoi-
deae, Actiniopteris radiata (Sw.) Link, – , – , Gastony & Johnson (2001), AF336100; Anogramma caespitosa Pic. Serm., – , – , Naka-
zato & Gastony (2003), AY168718; A. chaerophylla (Desv.) Link (A), – , – , Nakazato & Gastony (2003), AY168713; A. chaerophylla
(Desv.) Link (B), – , – , Nakazato & Gastony (2003), AY168712; A. guatemalensis (Domin) C. Chr., – , – , Nakazato & Gastony (2003),
AY168716 ; A. leptophylla (L.) Link, – , – , Nakazato & Gastony (2003), AY168717; A. lorentzii (Hieron.) Diels, – , – , Gastony &
Johnson (2001), AF336102; A. novogaliciana Mickel, – , – , Nakazato & Gastony (2003), AY168714; A. osteniana Dutra, – , – , Naka-
zato & Gastony (2003), AY168711; Cosentina vellea (Aiton) Tod., – , – , Nakazato & Gastony (2003), AY168720; Eriosorus flexuosus
(Kunth) Copel., – , – , Nakazato & Gastony (2003), AY168709; E. myriophyllus (Sw.) Copel., Prado & Yano 1033, SP: Campos do
Jordão, this study, EF473710; Jamesonia canescens (Klotzsch) Kunze, – , – , Nakazato & Gastony (2003), AY168710; Onychium
japonicum (Thunb.) Kunze, – , – , Hasebe & al. (1994), U05641; O. lucidum Spreng., – , – , Gastony & Johnson (2001), AF360359;
Pityrogramma calomelanos (L.) Link, Prado & al. 1030, SP: Bertioga, this st udy, EF473711; P. calom elan os (L.) Link, – , – , Gastony
& Johnson (2001), AF336103; P. tr ifoli ata (L.) R.M. Tryon, – , – , Gastony & Johnson (2001), AF336104; Tae ni ti s blechnoides (Willd.)
Sw., – , – , Hasebe & al. (1994), U05654; DENNSTAEDTIACEAE, Dennstaedtia punctiloba J. Sm., – , – , Wolf & al. (1994), U05918;
D. samoensis (Brack.) T. Moore, – , – , Wolf & al. (1994), U18637; Microlepia strigosa (Thunb.) C. Presl., – , – , Wolf & al. (1994),
U05931; M. platyphylla (D. Don) J. Sm., – , – , Wolf (1995), U18642; M. szechuanica Ching, – , – , Wolf (1995), U18643; Pteridium
aquilinum (L.) Kuhn (A), – , – , Schneider & al. (2004), AY300097; P. aquilinum (L.) Kuhn (B), – , – , Hasebe & al. (1994), U05646;
P. esculentum (G. Forst.) Kunh, – , – , Wolf & al. (1994), U05940; LINDSAEACEAE, Lonchitis hirsuta L., – , – , Wolf & al. (1994),
U05929; L. mannii (Hook. & Baker) Alston, – , – , Wolf (1995), U18641; SACCOLOMATACEAE, Saccoloma elegans Kaulf., – , – ,
Wolf (unpubl.), U18645; S. inaequale (Kunze) Mett., – , – , Pryer & al. (2004), AY612682; S. moluccanum Mett., – , – , Wolf (1995),
U18649; VITTARIOID, Ananthacorus angustifolius Underw. & Maxon, – , – , Crane & al. (1995), U20932; Antrophyum boryanum
Blume, – , – , Crane & al. (1995), U20930; A. ensiforme Hook., – , – , Crane & al. (1995), U20931; A. plantagineum (Cav.) Kaulf., – ,
– , Crane & al. (1995), U21285; A. reticulatum (G. Forst.) Kaulf., – , – , Hasebe & al. (1994), U05604; *Haplopteris anguste-elongata
(Hayata) E.H. Crane, – , – , Crane & al. (1995), U21291; *H. ensiformis (Sw.) E.H. Crane, – , – , Crane & al. (1995), U21290; *H.
flexuosa (Fée) E.H. Crane, – , – , Hasebe & al. (1994), U05656; *H. zosterifolia (Willd.) E.H. Crane, – , – , Crane & al. (1995), U21296;
Hecistopteris pumila (Spreng.) J. Sm., – , – , Crane & al. (1995), U21286; Polytaenium cajenense (Desv.) Benedict, – , – , Crane & al.
(1995), U20934; P. lanceolatum (L.) Benedict, – , – , Crane & al. (1995), U21287; P. lineatum (Sw.) J. Sm., – , – , Crane & al. (1995),
U20935; *Radiovittaria gardneriana (Fée) E.H. Crane, – , – , Crane & al. (1995), U21294; *R. minima (Baker) E.H. Crane, – , – , Crane
& al. (1995), U21288; *R. remota (Fée) E.H. Crane, – , – , Crane & al. (1995), U21289; *R. stipitata (Kunze) E.H. Crane, – , – , Crane
& al. (1995), U21293; Vittaria dimorpha Müll., – , – , Crane & al. (1995), U21292; V. gra mi n ifolia Kaulf., – , – , Crane & al. (1995),
U21295; V. isoetifolia Bory, – , – , Crane & al. (1995), U20936; V. lineata (L.) Sm., Prado & Yano 1411, SP: Campos do Jordão, this
study, EF473712; V. lineata (L.) Sm., – , – , Crane & al. (1995), U20937.
* Deposited in GenBank as Vittaria
Appendix. Continued.
