Olsson & al. • Neckera and Thamnobryum
TAXON 60 (1) • February 2011: 36–50
Neckera and Thamnobryum (Neckeraceae, Bryopsida):
Paraphyletic assemblages
Sanna Olsson,1,2,6 Johannes Enroth, 3 Volker Buchbender,1,6 Lars Hedenäs,4 Sanna Huttunen4,5
& Dietmar Quandt1,6
1 Institute of Botany, Plant Phylogenetics and Phylogenomics Group, Dresden University of Technology, 01062 Dresden, Germany
2 Department of Agricultural Sciences, P.O. Box 27, 00014 University of Helsinki, Finland
3 Department of Biosciences and Botanical Museum, P.O. Box 7, 00014 University of Helsinki, Finland
4 Department of Cryptogamic Botany, Swedish Museum of Natural History, Box 50007, 104 05 Stockholm, Sweden
5 Laboratory of Genetics, Department of Biology, 20014 University of Turku, Finland
6 Nees Institute for Biodiversity of Plants, University of Bonn, Meckenheimer Allee 170, 53115 Bonn, Germany
Authors for correspondence: Sanna Olsson, sanna.olsson@helsinki.fi and Dietmar Quandt, quandt@uni-bonn.de
Abstract Recent phylogenetic analyses indicated that the backbone phylogeny of the pleurocarpous moss family Neckeraceae
falls into three distinct clades. Here the detailed composition and phylogenetic relationships of the two major clades (the Neckera
clade and the Thamnobryum clade) are analysed. The phylogenetic analyses, based on sequence data from the plastid rpl16
intron and the rps4-trnT-trnL-trnF cluster as well as the nuclear ITS1 and 2, retained this tripartition and revealed a strong
biogeographic pattern, especially inside the Neckera clade. In addition, several morphological characters that have been held
as unique and characteristic to a certain group of mosses and therefore valuable in taxonomic classification, were shown to be
highly homoplastic and subjected to convergent evolution. Consequently, the circumscriptions of Leptodon and Thamnobryum
are amended, the new genera Exsertotheca, Echinodiopsis and Thamnomalia (each with two species), and Alleniella (with ten
species) are formally described and several implied nomenclatural changes are proposed, including synonymisation of Alsia
with Neckera and Cryptoleptodon with Leptodon.
Keywords convergent evolution; molecular phylogeny; nomenclature; pleurocarpous mosses; taxonomy
INTRODUCTION
With around 5000 species, pleurocarpous mosses represent
the largest radiation of early land-plants that occur in nearly
all terrestrial ecosystems. Typically they have a creeping, profusely branching habit, and the sporophyte development takes
place in the apices of short, lateral branches. This contrasts to
the so-called acrocarpous condition, in which the sporophytes
develop at the apices of the main shoots. As defined by Bell &
al. (2007) the pleurocarpous mosses form a monophylum (“core
pleurocarps”) with four orders: Hypnodendrales, Ptychomniales, Hookeriales and Hypnales.
The moss family Neckeraceae belongs to the order Hypnales. The family consists of temperate and tropical taxa, with
the total species number estimated to be ca. 200 (Enroth, 1994a;
Olsson & al., 2009a). Most of the species are epiphytic or epilithic, but there are also a few aquatic (rheophytic) species. Most
typically Neckeraceae are large, glossy plants that have a creeping stolon bearing very small leaves and tufts of rhizoids located
just below the leaf insertions, and more or less frondose (rarely
dendroid) stems with or without distinct stipes. The leaf cells are
almost always smooth, relatively short, and the marginal cells are
typically quadrate to short-rectangular in few to several rows.
The sporophyte features are variable but usually fairly consistent
within genera. A more detailed morphological characterisation
of the Neckeraceae was provided by Olsson & al. (2009b). According to the current classification by Goffinet & Buck (2004)
36
the family comprises 28 genera, although detailed phylogenetic
analyses based on a wider taxon sampling suggest that several of
these genera, such as Homaliadelphus and Bissetia (both Miyabeaceae) or Dixonia (OPP-clade) belong elsewhere (Olsson & al.,
2009a,b) and more changes in generic composition are expected.
However, the most recent attempt to resolve the backbone phylogeny and broad relationships of Neckeraceae by Olsson & al.
(2009b) identified three distinct clades. As one of the three, the
well defined Pinnatella clade was already the focus of a detailed
study that clarified most of the taxonomic and nomenclatural
aspects in this group (Olsson & al., 2010). This paper focuses on
the composition, phylogenetic relationships and nomenclature of
the two remaining clades, containing the largest neckeraceous
genera (Neckera, Thamnobryum) that were used to denominate
each clade (Olsson & al., 2009b).
Members of both the Neckera and Thamnobryum clades
as defined by Olsson & al. (2009b) are mainly non-Asiatic and
non-tropical, although the Neckera clade includes some species
which have a wide, often disjunct (possibly relict) distribution,
e.g., Leptodon smithii, Forsstroemia trichomitria and F. producta. Most species of the Neckera clade sensu Olsson & al.
(2009b) have a weak costa and immersed capsules with reduced
peristomes and the teeth at the leaf margins are usually unicellular. In the Thamnobryum clade sensu Olsson & al. (2009b) the
few truly tropical taxa are almost exclusively limited to South
America. The members of this clade are typically fairly robust,
distinctly stipitate, and have a single, at least relatively strong
TAXON 60 (1) • February 2011: 36–50
costa. In addition, the setae are long (capsules exserted) and the
peristomes are well developed, perfect or only somewhat reduced
(in Porotrichodendron) but not as strong as in the Neckera clade.
Due to different concepts of character evolution, i.e., different weighting of morphological characters, the taxonomic
placement of several species and genera that have been discussed in relation to Neckeraceae was subjected to various
changes in the past. In order to avoid a lengthy discussion we
provide a historical overview presenting the relevant treatments
dealing with genera inside the Neckera and Thamnobryum
clades sensu Olsson & al. (2009b). The historical overview
(Table 1) that summarises the distribution, morphology and
systematic placement of these genera, reflects fluctuations in
the systematic treatments according to changes in homology
assumptions or simply different weighting schemes of morphological characters. In general, homology assessment is problematic in these rather inconspicuous organisms and convergent
evolution almost exclusively assessable via molecular phylogenetics (e.g., Hedenäs, 2007; Olsson & al., 2009c; Sotiaux &
al., 2009; Huttunen & Ignatov, 2010).
In contrast to vascular plants, classifications dealing with
bryophytes are traditionally based on gametophytic as well as
sporophytic characters, with the shorter-lived sporophyte generation being regarded as the evolutionarily more conservative
one (e.g., Crum, 2001). The latter view, however, is currently
changing, as molecular approaches in mosses reveal that gametophytic characters provide a better phylogenetic signal on
family-level relationships than sporophytic ones, which seem to
be prone to convergent evolution (e.g., Buck & al., 2000; Goffinet
& al., 2004; Huttunen & al., 2004; Hedenäs, 2007; HernándezMaqueda & al., 2008; Olsson & al., 2009b, Quandt & al., 2009).
Although reports of convergent evolution in bryophytes are
scarce, recent studies indicate that this phenonemon is more
common in mosses than previously thought (e.g., Olsson &
al., 2009c; Sotiaux & al., 2009; Huttunen & Ignatov, 2010).
The aquatic mosses that until recently were often placed in
Platyhypnidium are a good example of a case where morphologically very similar species belong to several distinct evolutionary lineages (Huttunen & Ignatov, 2010). In contrast,
the rheophilic Thamnobryum alopecurum populations differ
considerably from the terrestrial ones to the point that they
have been described as independent species, while molecular
analyses revealed their independent origin from neighbouring
terrestrial populations (Olsson & al., 2009c).
This study aims to evaluate whether the relationships suggested by the traditionally-used morphological characters in
two major clades of the moss family Neckeraceae are congruent with the phylogenetic analyses based on molecular data.
MATERIALS AND METHODS
Taxon sampling and molecular markers. — The taxon
sampling was intended to be representative and to completely
cover the morphological variation within Neckeraceae. The
results from earlier studies together with previous taxonomic
classifications (e.g., Buck & Goffinet, 2000; Goffinet & Buck,
Olsson & al. • Neckera and Thamnobryum
2004; Olsson & al., 2009a,b) were used as guidelines when
choosing the species to be included. Homalia webbiana, Heterocladium dimorphum and Heterocladium procurrens together
with representatives of Lembophyllaceae were used as outgroup since they seem to be the closest relatives of Neckeraceae
(Olsson & al., 2009a,b; Quandt & al., 2009). For this selection of taxa we sequenced three genomic regions: the internal
transcribed spacers of nuclear ribosomal DNA (ITS1 & 2), the
plastid rps4-trnT-trnL-trnF cluster (including the 3′ of the rps4
gene), and the group II intron in rpl16 (plastid).
Two genera could not be included in the analyses due to
lack of material. Neomacounia nitida is a monospecific genus
based on the basionym Forsstroemia nitida. It is known only
from two specimens from Ontario (Canada), collected in 1862
and 1864 (Ireland, 1974). The type locality and its surroundings were searched in the early 1970s to rediscover the taxon,
but it was not found. It seems that Neomacounia is extinct.
Based on the description by Ireland (1974) there is nothing in
the morphology of Neomacounia that belies a placement in
Neckeraceae; it is probably closely related to some Neckera
species. Noguchiodendron sphaerocarpum, the single species of the genus, is distributed in the Himalayan region and
Thailand. As discussed by Ninh & Pócs (1981), it is probably
closely related to Homaliodendron, where it was originally
placed, but it differs in certain morphological characters in the
gametophyte (e.g., presence of a central strand in the stem) as
well as in the sporophyte (e.g., capsule shape, presence of an
annulus), justifying the maintenance of it as a separate genus.
There was no adequately fresh material available to be included
in the present molecular analyses.
DNA isolation, PCR-amplification and sequencing. —
DNA was extracted using the DNeasy® Plant Mini Kit from
Qiagen (Qiagen GmbH, Germany) following the manufacturer’s protocol. Methods of cleaning and grinding of plants prior
to extraction and amplification of the ITS1-5.8S-ITS2 as well as
the rps4-trnT-trnL-trnF region followed Olsson & al. (2009a),
whereas the protocols for rpl16 were obtained from Olsson &
al. (2009b). Gel-cleaned PCR products were sequenced by Macrogen Inc., South Korea (www.macrogen.com). Sequences were
edited manually with PhyDE® v0.995 (Müller & al., 2005) and
primer sequences were eliminated. All sequences are deposited
in EMBL; accession numbers are listed together with voucher
information in the Appendix.
Sequence analyses and phylogenetic analyses. — Alignment of the sequence data was performed manually in PhyDE®
v.0.995 (Müller & al., 2005), based on the criteria laid out in
Kelchner (2000), and Quandt & Stech (2005) using the alignment of Olsson & al. (2009a) as scaffold. As length variation
of the sequence data was very low, alignment was straightforward. The reported hairpin-associated inversion in the trnL-F
intergenic spacer (IGS) (Quandt & al., 2004; Quandt & Stech,
2005) was positionally isolated in the alignment and included in
the analysis as reverse complement in order to gain information
from substitutions within the detected inversion, as discussed
in Quandt & al. (2003). Alignments are available on request
from the authors. Indels were incorporated as binary data using
a simple indel coding (SIC) strategy (Simmons & Ochoterena,
37
Olsson & al. • Neckera and Thamnobryum
TAXON 60 (1) • February 2011: 36–50
Table 1. Historical overview of the genera in the Neckera and Thamnobryum clades (plus Touwia), including remarks on species number, distribution, …
Established
Further reference(s)
Other placements
No. of species
Distribution
Leaf shape
Costa
Leaf cells
Cell walls
Alar cells
Paraphyllia
Vegetative propagulae
Sexual condition
Seta
Capsule
Peristome
Established
Further reference(s)
Other placements
No. of species
Distribution
Leaf shape
Costa
Leaf cells
Cell walls
Alar cells
Paraphyllia
Vegetative propagulae
Sexual condition
Seta
Capsule
Peristome
Established
Further reference(s)
Other placements
No. of species
Distribution
Leaf shape
Costa
Leaf cells
Cell walls
Alar cells
Paraphyllia
Vegetative propagulae
Sexual condition
Seta
Capsule
Peristome
38
Alsia
Sullivant (1855)
Lawton (1971)
Cryphaeaceae, Leucodontaceae, Leptodontaceae
1
NW North America
ovate
short and double or single and to 3/4 of leaf length
smooth
thick, porose
distinct, transverse
present
absent
dioicous
3–5 mm
exserted, orthotropous
reduced
Homalia
Schimper (1850)
He (1997)
–
5
wide, tropical-temperate
oblong-ovate to spatulate or nearly rounded, asymmetric
short and double or single and to c. 4/5 leaf length
smooth
firm, mostly not porose
indistinct
absent
flagelliform branches (uncommon)
dioicous (one sp. autoicous)
8–20 mm
exserted, orthotropous or orthogonal
perfect
Porotrichopsis
Herzog (1916)
Enroth (1995)
Thamnobryaceae
1
South America
narrowly elliptic to nearly lingulate
single, to midleaf
smooth
firm, not porose
small, thick-walled
absent
caducous leaves
dioicous
15–28 mm
exserted, orthogonal to homotropous
slightly reduced
Chileobryon
Enroth (1992b)
–
Anomodontaceae
1
Chile
ovate(-oblong)
single, to below leaf apex
papillose
firm, not porose
indistinct
absent
absent
dioicous
?
?
?
Leptodon
Mohr (1803)
Pócs (1960); Nelson (1973); Enroth (1992a)
Leptodontaceae
4
wide, temperate, highly disjunct
ovate(-oblong)
single, to over midleaf
smooth
firm, not porose
fairly distinct, small
present
absent
dioicous
1.5–2.5 mm
exserted, orthotropous
reduced
Porotrichum (incl. Porothamnium)
Hampe (1863)
Sloover (1983); Sastre-De Jesús (1987); Allen (1994)
Thamnobryaceae
ca. 15
Africa, South & Central America
ovate(-oblong)
single, to near leaf apex (rarely short)
smooth or prorulose
firm, not porose
indistinct
absent
flagelliform branches
dioicous
ca. 5–30 mm
exserted, orthotropous
slightly reduced
TAXON 60 (1) • February 2011: 36–50
Olsson & al. • Neckera and Thamnobryum
… and prevalent morphological characters. ? = character unknown. Terminology for the capsule orientation follows Hedenäs (2007).
Cryptoleptodon
Renauld & Cardot (1900)
Buck (1980); Enroth (1992a); Hedenäs (1992)
Leptodontaceae, Pterobryaceae
4
India, East Africa, Macaronesia
ovate(-oblong)
single, to above mid-leaf
smooth/mammillose
firm, not porose
fairly distinct, small
present
absent
dioicous
1.5–6.0 mm
exserted, orthotropous
reduced
Neckera
Hedwig (1801)
Sloover (1977); Sastre-De Jesús (1987)
–
ca. 50
wide, mainly temperate
variable, mostly ovate(-oblong), asymmetric
variable, often short and weak
smooth
firm, porose or not
fairly indistinct, small
mostly absent, sometimes present
flagelliform branches sometimes present
dioicous or autoicous
0.5 to ca. 20 mm
immersed or exserted, orthotropous
reduced
Thamnobryum
Schimper (1852, as Thamnium hom. illeg.); Nieuwland (1917)
Kindberg (1902); Ochyra (1990, 1991); Mastracci (2003)
Thamnobryaceae
ca. 35
temperate, mainly Northern Hemisphere
ovate(-oblong), sometimes lanceolate or ligulate
single, to near leaf apex
smooth, rarely mammillose
firm, not porose
indistinct
absent
absent
dioicous, rarely polyoicous
ca. 10–25 mm
exserted, orthogonal to homotropous
perfect
Echinodium
Juratzka (1866)
Churchill (1986); Stech & al. (2008)
Echinodiaceae
6
Macaronesia, Australasia
ovate-subulate
single, excurrent
smooth
firm, not porose
indistinct
absent
absent
dioicous
11–35 mm
exserted, orthogonal to homotropous
perfect
Pendulothecium
Enroth & He (1991)
–
–
3
Australasia
ligulate to spatulate or obovate
single, to half or 5/6 of leaf length
smooth
firm, not porose
indistinct
absent
flagelliform branches sometimes present
dioicous
13–14 mm
exserted, reclinate to antitropous
perfect
Touwia
Ochyra (1986)
Olsson & al. (2010)
–
3
Southeast Asia, Australasia
lanceolate or elliptic
single, to near leaf apex
smooth
firm, not porose
indistinct
absent
absent
dioicous
15–18 mm
orthogonal
perfect
Forsstroemia
Lindberg (1863)
Stark (1987)
Leucodontaceae, Leptodontaceae
10
wide, temperate-subtropical
ovate(-lanceolate)
single, variable in length
smooth
firm, porose or not
distinct, quadrate to transverse
absent
absent
dioicous or autoicous
to 4.6 mm
immersed to exserted
reduced
Porotrichodendron
Fleischer (1906–08)
Buck (1998)
Lembophyllaceae, Thamnobryaceae
2–3 (Churchill & Linares, 1995)
Central & South America
ovate(-oblong)
single, to above midleaf
smooth
firm, slightly porose
small, thick-walled
absent
flagelliform branches
dioicous
to ca. 40 mm
exserted, orthotropous
slightly reduced
39
Olsson & al. • Neckera and Thamnobryum
2000) as implemented in SeqState (Müller, 2005). Command
files for using the parsimony ratchet (Nixon, 1999) were generated using PRAP2 (Müller, 2007) and executed in PAUP*
v.4.0b10 (Swofford, 2002). Ratchet settings were as follows: 10
random addition cycles of 200 iterations each, with 25% upweighting of the characters in the iterations. Heuristic bootstrap
searches under parsimony were performed with 1000 replicates
and 10 random addition cycles per bootstrap replicate.
Bayesian analyses were performed with MrBayes v.3.1.2
(Huelsenbeck & Ronquist, 2001), applying the GTR + Γ + I
model for the sequences data and the restriction site model for
the binary indel partition. To allow for possible deviating substitution models for the different regions, the dataset was further
divided into three sequence partitions (partition 1: rps4-trnF;
partition 2: rpl16; partition 3: nuclear DNA). The a priori probabilities supplied were those specified in the default settings of
the program. Posterior probability (PP) distributions of trees
were calculated using the Metropolis-coupled Markov chain
Monte Carlo (MCMCMC) method and the search strategies
suggested by Huelsenbeck & al. (2002) and Huelsenbeck & al.
(2001). Ten runs with four chains (2.5 × 106 generations each)
were run simultaneously, with the temperature of the heated
chains set to 0.1. Chains were sampled every 1000 generations
and the respective trees written to a tree file. Calculations of
the consensus tree and of the posterior probability of clades
were performed based upon the trees sampled after the chains
converged (less than generation 50,000). Consensus topologies and support values from the different methodological approaches were compiled and drawn using TreeGraph2 (Stöver
& Müller, 2010).
In order to evaluate the monophyly versus para- or polyphyly
of Neckera inside clade A, a topology test was conducted. Therefore a constrained analysis forcing Neckera to be monophyletic
(not including the remote Neckera taxa of clade C: N. himalayana, N. polyclada, N. warburgii, and N. crenulata) using the
program MrBayes v.3.1.2. was performed, and harmonic means
of the likelihoods for both topologies were compared and evaluated using the Bayes Factor (BF; Kass & Raftery, 2007).
RESULTS
Alignment and sequence analyses. — In total 21 hotspots
with poly-homonucleotid repeats were recognized following
Olsson & al. (2009a) and excluded from the analyses (compare
Table 2). The observed inversion was treated as reverse complement for the phylogenetic analyses (compare Table 2). Hotspots
were more frequent in the plastid region (H1–17), while only
four were found in the nrDNA (H18–21). The resulting combined and aligned sequence matrix contained 3464 positions of
which 1476 positions belong to the rps4-trnT-trnL-trnF partition, 880 positions to the rpl16 partition and 1106 positions to
the nuclear ribosomal partition. Of the characters 2760 were
constant and 405 characters were parsimony-informative. Including the data matrix based on indel coding raised the number of parsimony-informative characters to 547 (a total of 3808
characters with 1041 being variable).
40
TAXON 60 (1) • February 2011: 36–50
Phylogenetic analyses. — The parsimony analysis without
indel coding retained 56 most parsimonious trees (MPT, length
1489, consistency index CI = 0.556, retention index RI = 0.783).
After inclusion of the indel matrix 25 MPTs were retained
(length 2039, CI = 0.571, RI = 0.778). The strict consensus tree
of both analyses showed no conflict with the results from the
Bayesian inference (BI), but had less resolution compared to
the BI tree. Therefore, only the BI tree is illustrated in Fig. 1,
with posterior probabilities (PP) indicated and complemented
with bootstrap values (BS) of the parsimony analysis when
applicable. When the indel matrix was included in the analyses, the only topological difference observed was the poorly
resolved position of the clade consisting of Neckera crispa
and N. intermedia. However, differences in the magnitude of
support values at some of the nodes were observed. Therefore,
both the values without and with the indel matrix included
are illustrated and discussed. Values resulting from analyses
without indel coding precede the values from analyses with the
SIC-matrix included. Thus support values from the different
analyses will be referred to in the text following this scheme
(PP/PPsic/BS/BSsic).
The ingroup species belong to Neckeraceae as defined
by Olsson & al. (2009b). Three clades can be distinguished:
Table 2. Location, i.e., absolute position in the combined dataset and
corresponding region of mutational hotspots (H) and the observed
inversion (I). Location of the inversion is given with respect to the
corrected and analysed matrix (i.e., the inversion is included as reverse
complement).
No.
Position
Region
H1
265–266
rps4-trnT IGS
H2
326–330
rps4-trnT IGS
H3
379–394
rps4-trnT IGS
H4
483–484
rps4-trnT IGS
H5
850–852
trnT-trnL IGS
H6
879–881
trnT-trnL IGS
H7
989–991
trnT-trnL IGS
H8
1035–1038
trnT-trnL IGS
H9
1638–1639
rpl16
H10
1682–1687
rpl16
H11
1740–1742
rpl16
H12
1766–1767
rpl16
H13
1977–1978
rpl16
H14
1997–2000
rpl16
H15
2322–2326
rpl16
H16
2336–2338
rpl16
H17
2392–2394
rpl16
H18
2491–2495
ITS1
H19
2737–2740
ITS1
H20
2875–2878
ITS1
H21
3256–3293
ITS2
I1
1451–1457
trnL-trnF IGS
TAXON 60 (1) • February 2011: 36–50
Olsson & al. • Neckera and Thamnobryum
100 100
100 100
100 100
100 100
63 86
100 100
- -
99 99
98 100
91 88
100 100
100 100
100 100
100 100
100 100
99 96
83 69
100 100
99 99
100 100
A
80 62
100 100
93 95
100 100
50 74
100 100
63 -
100 100
100 100
100 62
100 100
66 -
- -
- -
100 100
99 95
95 62
100 100
69 96
51 57
100 100
84 80
94 52
93 77
- -
99 100
100 100
77 78
77 55
92 84
97 98
70 69
92 95
- -
91 94
- -
100 100
100 100
100 100
97 98
85 84
100 96
- -
100 100
63 100 100
100 100
72 77
100 100
- -
99 99
100 100
100 100
100 100
100 100
100 100
54 51
61 61
100 100
86 97
B
96 97
100 100
- 52
62 58
100 100
- -
98 98
65 85
100 100
100 100
99 59
- -
93 71
- -
100 100
58 91
71 80
100 100
100 100
74 77
100 100
100 100
100 100
92 97
97 97
100 100
- -
C
55 -
75 82
98 98
- -
100 100
- -
100 100
65 64
- -
95 79
-
100 100
99 100
100 100
94 93
98 99
84 90
Homalia webbiana
Heterocladium dimorphum
Heterocladium procurrens
Rigodium pseudothuidium
Dolichomitriopsis diversiformis
Lembophyllum clandestinum
Camptochaete arbuscula
Weymouthia mollis
Thamnomalia "Homalia" glabella
Thamnomalia "Thamnobryum" tumidicaulis
Neckera menziesii
Neckera pennata
Neckera "Alsia" californica
Neckera douglasii
Leptodon "Cryptoleptodon" pluvinii
Leptodon "Cryptoleptodon" longisetus
Leptodon smithii
Exsertotheca "Neckera" crispa
Exsertotheca "Neckera" intermedia
Forsstroemia neckeroides
Forsstroemia "Neckera" yezoana
Forsstroemia trichomitria
Forsstroemia "Neckera" goughiana
Alleniella "Neckera" besseri
Alleniella "Neckera" complanata
Alleniella "Neckera" hymenodonta
Alleniella "Neckera" brownii
Alleniella "Neckera" urnigera
Alleniella "Neckera" chilensis
Alleniella "Neckera" scabridens
Alleniella "Neckera" remota
Alleniella "Neckera" submacrocarpa
Alleniella "Neckera" valentiniana
Touwia laticostata
Touwia elliptica
Touwia negrosensis
Homalia lusitanica
Homalia trichomanoides
Homalia giraldii
Thamnobryum neckeroides
Thamnobryum speciosum
Thamnobryum subserratum
Thamnobryum alopecurum
Thamnobryum cataractarum
Thamnobryum fernandesii
Thamnobryum maderense
Thamnobryum rudolphianum
Thamnobryum pumilum
Chileobryon callicostelloides
Pendulothecium punctatum
Echinodiopsis "Echinodium" hispida
Echinodiopsis "Echinodium" umbrosa
Porotrichum bigelovii
Thamnobryum pandum
Thamnobryum fasciculatum
Porotrichopsis flacca
Porotrichum frahmii
Porotrichodendron robustum
Porotrichodendron “Porotrichum” madagassum
Porotrichodendron superbum
Curvicladium kurzii
Neckera himalayana
Circulifolium exiguum
Neckeropsis nitidula
Homaliodendron neckeroides
Homaliodendron flabellatum
Neckera polyclada
Neckera warburgii
Pinnatella kuehliana
Taiwanobryum anacamptolepis
Taiwanobryum speciosum
Taiwanobryum crenulatum
Thamnomalia
Neckera s. str.
Leptodon
Exsertotheca
Forsstroemia
Alleniella
Touwia
Homalia
Thamnobryum
Chileobryon
Pendulothecium
Echinodiopsis
"Poro-" clade
Pinnatella clade
Fig. 1. Phylogenetic relationships of selected Neckeraceae taxa based on rps4-trnT-trnL-trnF, rpl16 and ITS1 & 2 sequences. The PP values from
the MrBayes analyses (without indel coding first, then with indel coding) are indicated above, the bootstrap values of the parsimony analysis
below when applicable (without indel coding first, then with indel coding).
41
Olsson & al. • Neckera and Thamnobryum
clade A formed by Neckera and related taxa, clade B having
Thamnobryum as the most prominent genus, and clade C including Pinnatella and Neckeropsis among others. The positions of the genera Touwia and Homalia s.str. (H. lusitanica,
H. trichomanoides, H. giraldii) remained in a poorly supported
position within a maximally supported clade uniting the Thamnobryum and the Pinnatella clades.
In addition to most of the Neckera species, Forsstroemia,
Cryptoleptodon, Leptodon, Alsia californica, Homalia glabella
and Thamnobryum tumidicaule belong to clade A, which receives maximum support in the BI. The two last-mentioned
species render Homalia and Thamnobryum polyphyletic and
formed a maximally supported clade that is resolved as a sistergroup to all the remaining taxa in this clade. The second
branching lineage included Neckera menziesii, N. pennata,
Alsia californica and Neckera douglasii (100/100/99/96) followed by Leptodon (including Cryptoleptodon). Inside clade A,
Leptodon and Cryptoleptodon are resolved as a third branching lineage in all analyses and with maximal support in the
BI analyses without indels coded. However support for this
clade drops drastically once the indel matrix is included, while
no support was generated using bootstrapping (100/62/–/–).
Neckera crispa groups together with N. intermedia, receiving
full support in all analyses. The clade including Forsstroemia
neckeroides, Neckera yezoana, Forsstroemia trichomitria and
Neckera goughiana is very well supported (100/100/99/95), but
the relationships within this clade are not totally resolved. Similarly, the placement of the Neckera crispa/N. intermedia clade
was not resolved with confidence. The last major clade receives
maximum support in the BI as well as high bootstrap support
and includes ten species of Neckera. However, Neckera in its
current circumscription is resolved with multiple polyphyletic
branches. Harmonic mean likelihood for the topology (–ln L
= 14,034.94) where Neckera was constrained to monophyly
was significantly lower (BF = 11.32, compare Kass & Raftery,
2007 for details on the interpretation of the BF) than that of the
unconstrained topology with a polyphyletic Neckera (–ln L =
14029.28), and thus strongly supports the polyphyly of Neckera.
Clade B was divided into two well-defined clades: one included only Thamnobryum species and the other has species
of Thamnobryum, Chileobryon, Pendulothecium, Echinodium, Porotrichum, Porotrichopsis and Porotrichodendron,
rendering the genera Porotrichum and Porotrichodendron
polyphyletic. Both clades received maximal or high support
values, but the relationships within the clades are not totally
resolved.
Clade C was composed of diverse taxa: Circulifolium,
Curvicladium, Homaliodendron, Neckeropsis, Pinnatella, Taiwanobryum, and some Asian Neckera species. Even if the clade
received high support in the Bayesian analyses (97/97), the
internal nodes in this clade are largely unresolved or lacking
support, except for the clade containing Pinnatella kuehliana,
Taiwanobryum anacamptolepis, T. speciosum and T. crenulata (100/100/99/100) and two small clades with Circulifolium
exiguum together with Neckeropsis nitidula (100/100/98/98)
and Homaliodendron neckeroides together with H. flabellatum
(100/100/100/100), respectively.
42
TAXON 60 (1) • February 2011: 36–50
DISCUSSION
Additional data is most often expected to increase resolution and group support, especially the addition of microstructural characters has been reported to significantly increase
resolution and support at all levels (e.g., Graham & al., 2000;
Simmons & al., 2001; Hamilton & al., 2003; Müller & Borsch,
2005; Löhne & Borsch 2005; Borsch & al., 2007). In addition,
microstructural characters are often considered less homoplasious compared to substitutions, with secondary losses of acquired simple sequence repeats being less likely, especially with
regard to sequence data from plastid regions (compare Borsch
& Quandt, 2009). The inclusion of the SIC matrix in the presented phylogenetic analyses, however, seems to have slightly
opposite effects in some cases. Similar results were obtained
by, e.g., Sotiaux & al. (2009), where especially indels in the
rpl16 region were shown to be homoplasious on deeper levels
such as the Neckeraceae backbone, but adding information at
shallow nodes, and, e.g., supported a geographic pattern among
Leptodon smithii populations. In the present analyses posterior
probability values for some groups, such as the clade consisting
of Neckera species from N. complanata to N. valentiana, were
clearly higher without indel data. We assume this to be due to
likely convergent evolution of some of the coded indels that can
give slightly misleading evolutionary information. For some
groups, however, inclusion of the indel matrix leads to better
support (for example clade B plus Homalia trichomanoides and
H. giraldii, and the Cryptoleptodon-Leptodon clade). The support seems to be due to a combination of indels rather than to
significant single indel events, since only few indels supporting
these groups were found. Clade B is supported by three indels in
the ITS region (positions 2685–2687, 2723–2725 and 3211–3213
in the original matrix) and the Cryptoleptodon-Leptodon clade
is supported by only one short indel in the ITS region (positions
2693–2694). Overall, it seems that the contribution of indels
towards the phylogenetic signal is more complex than previously
thought and dependent on the study group, the hierarchical level
and the evolutionary constraints of the chosen marker that vice
versa most likely depends on the study group.
Convergent evolution or incongruence between morphology and molecular data? — Incongruence among molecular
partitions is common and can have many different causes, such as
insufficient data, rapid diversification, horizontal gene transfer,
hybridization, incomplete lineage sorting, convergence caused
by natural selection, and variations in evolutionary rate (cf., Wendel & Doyle, 2005). Several of these causes could potentially also
explain incongruence between molecular and morphological
data. Phylogenetic analyses can often not decide which of these
causes is behind a particular case unless additional evidence is
at hand (Wendel & Doyle, 2000).
Incongruence between morphology and molecular data
that have other reasons than convergent morphological evolution are known for other pleurocarps, for example in Isothecium (Draper & al., 2007), Leptodon (Sotiaux & al., 2009) and
Sciuro-hypnum (Draper & Hedenäs, 2009), suggesting that
especially non-coding markers may not always trace the evolution of the morphologically and biologically meaningful species
TAXON 60 (1) • February 2011: 36–50
correctly. We therefore believe it is risky to assume a priori that
molecular information is always superior to morphology, and
suggest that taxonomic novelties should only be proposed when
molecular information or other data leave no doubt regarding
the relationships among the taxa.
Earlier results on the morphological evolution in Neckeraceae (Olsson & al., 2009b) showed that certain morphological
states, especially sporophytic ones, such as reduced peristome
structures or short setae, evolved several times independently.
In addition, conflict between gametophytic and sporophytic
characters has been reported from several other bryophyte
groups such as Grimmiaceae (Hernández-Maqueda & al., 2008),
Splachnaceae (Goffinet & Shaw, 2002), Brachytheciaceae (Huttunen & Ignatov, 2004), Lembophyllaceae (Quandt & al., 2009),
Vittiaceae (Vanderpoorten & al., 2003) and Hypnales in general (Buck & al., 2000). In the present study the phylogenetic
inferences imply that several morphological character states,
especially gametophytic ones that were held as unique and characteristic for Neckera, actually evolved independently. For example, the typical “Neckera characters” (deeply undulate, glossy,
complanate and asymmetric leaves and a weak costa) seem to
represent the ancestral state and were later lost independently in
Leptodon and Forsstroemia, which is in accordance with the ancestral state reconstructions performed by Olsson & al. (2009b)
on a smaller taxon sampling. Compared with angiosperms, the
lack of a sufficient amount of morphological characters in bryophytes makes it more difficult to reveal convergent evolution in
this group based on morphology alone, but with well-resolved
and highly supported phylogenies this can be addressed.
Phylogenetic analyses and taxonomic relationships. —
Generally the phylogenetic analyses rendered nearly all genera
of the family polyphyletic, including the largest genus in the
family, Neckera. Even taxa that were recognized as families
such as Leptodontaceae are deeply nested inside Neckeraceae
and should therefore be merged with the latter (compare Olsson & al., 2009b). Within Leptodontaceae, the paraphyletic
genus Cryptoleptodon should be included in Leptodon (see
also Sotiaux & al., 2009).
Clade A. — In this clade, Thamnobryum tumidicaule and
Homalia glabella form the first diverging branch with high
support. We recognise this clade at the genus level and thus
describe the new genus Thamnomalia below.
Neckera. — In earlier studies evidence accumulated
that this genus, as currently understood, is not monophyletic
(Tsubota & al., 2004; Ignatov & al., 2007; Olsson & al., 2009b),
which is also found in this study based on a more comprehensive
taxon sampling. In the current analyses we included taxa that
cover the morphological variation and geographical distribution
of the genus. Since Neckera pennata is the type of the generic
name, the clade including that species, N. menziesii, N. douglasii
and N. californica (syn. Alsia californica), forms Neckera s.str.
Yet, the majority of the sampled species currently placed in the
genus Neckera belong to another clade containing only “Neckera” species. Additionally, two Neckera species, N. goughiana
and N. yezoana, are resolved in the clade including Forsstroemia
neckeroides and F. trichomitria (type of the generic name), thus
both Neckera species will be transferred to Forsstroemia. A
Olsson & al. • Neckera and Thamnobryum
close relationship of some Neckera species with Forsstroemia
was also suggested by the results of Tsubota & al. (2002), but
due to the sparse taxon sampling (Forsstroemia trichomitria,
F. japonica, F. neckeroides, Neckera urnigera) the supporting
evidence remained weak. The taxon sampling in our analyses
is more comprehensive, and the individual clades are distinct,
receiving good support on a statistically significant level. Therefore, we establish two new genera to accommodate the “Neckera” species that fall outside of Neckera s.str. and Forsstroemia
in clade A. It might be mentioned that the Australasian N. hymenodonta has previously been treated as a taxonomic synonym
of N. pennata (e.g., Fife, 1995). However, Ji & Enroth (2008)
showed that N. hymenodonta is morphologically distinct from
N. pennata (e.g., the former has paraphyllia), which is supported
by the present analysis that resolved N. hymenodonta outside of
Neckera s.str. in one of the new genera described below.
The three “Neckera” species belonging to clade C
(N. himalayana, N. polyclada, N. warburgii) are morphologically different from the other Neckera species and belong in a
peculiar group of robust Asian species (Enroth, 1996; Enroth &
Ji, 2007). According to our results they are neither closely related to the “true” Neckeras nor to the other sampled “Neckera”
species, and they do not form an own clade. As the phylogenetic estimates regarding these three species are inconclusive,
taxonomic changes are not yet warranted. Further analyses
are needed to uncover their phylogenetic relationships and to
provide a taxonomic and evolutionary concept regarding these
morphologically peculiar taxa.
Leptodon smithii and the two paraphyletic Cryptoleptodon
species form a clade, implying that Cryptoleptodon should be
included in Leptodon, as it traditionally has been (e.g., Jaeger &
Sauerbeck, 1876–1879: 105). It has been suggested in previous
studies (Maeda & al., 2000; Goffinet & al., 2001; Tsubota &
al., 2004; Olsson & al., 2009a,b) that Forsstroemia, Echinodium, Leptodon, and Anomodon giraldii have close affinities
with Neckera species, although based on limited datasets. The
morphological similarity between Forsstroemia and Leptodon
was pointed out by Stark (1987), and the affinities of Forsstroemia to Neckeraceae (when Leptodontaceae become included
in it) has morphological support as discussed by Buck (1980)
and Enroth (1992a).
Inside clade A several phytogeographically distinct groups
can be recognized with an interesting evolutionary and phytogeographic pattern. For example, the first branching group
consisting of Homalia glabella and Thamnobryum tumidicaule
is South American and tropical. The following group, with four
species of Neckera s.str. is essentially temperate and North
American, with the exception of N. pennata which has a much
wider distribution especially in the Northern Hemisphere, and
which may in fact contain more than one species (cf. Appelgren
& Cronberg, 1999). It thus seems that this group originated
and diversified in the “New World”, since apart from N. pennata, none of the European (N. complanata [which also occurs in North America], N. crispa, N. intermedia, N. besseri),
Asian (N. yezoana, N. goughiana, Forsstroemia neckeroides)
or African (N. remota, N. submacrocarpa, N. valentiniana)
species belong in Neckera s.str. In addition, it should be noted
43
Olsson & al. • Neckera and Thamnobryum
that the South American species N. urnigera, N. chilensis and
N. scabridens as well as the New Zealandian N. brownii and
N. hymenodonta, and the three African species just mentioned
form a clade with maximum support under BI (Fig. 1), with the
African species grouping together.
The topography of the clade from N. besseri to N. valentiniana, which is recognized in the present paper as a new genus,
has some intriguing evolutionary implications. For example,
the first branching species N. besseri and N. complanata are
dioicous (sporophytes rare) and produce flagelliform branchlets
that serve as vegetative propagula; the rest of the species are
autoicous (sporophytes frequent) and lack vegetative propagula.
This suggests that vegetative reproduction compensates for the
infrequent sexual reproduction in the dioicous taxa. Also, the
two basal taxa have long-exserted capsules, while the other
taxa have either immersed or short-exserted (N. chilensis) capsules. These differences may indicate evolutionary trends within
the clade that need to be confirmed by a more comprehensive
evolutionary study based on a more complete taxon sampling.
However, with the present sampling a strong phytogeographic
structure can be observed in this clade. Both species forming the
early branching grade are species from temperate regions of the
Northern Hemisphere. Neckera besseri is a western Eurasiatic
taxon, and N. complanata occurs in North America and western
Eurasia (with some reports from Africa). Whereas Neckera hymenodonta and N. brownii are Australasian species (Australia,
New Zealand) that can be described as Southern Hemisphere
temperate taxa, the remaining taxa occur at high elevations in
the tropics. Neckera urnigera, N. chilensis and N. scabridens
are exclusively South American, and N. remota, N. submacrocarpa and N. valentiniana that form a monophylum occur
exclusively in Africa. Since these taxa occur at relatively high
elevations, mostly above 2000 m (Sloover, 1977; Churchill &
Linares, 1995), their habitats are in some respects similar to
those found in the temperate regions (cf. Hedenäs, 1999).
Clade B. — Enroth & Tan (1994) pointed out that Thamnobryaceae, comprising “the dendroid Neckeraceae sensu
Brotherus (1929) with cross-striolate exostomes” (Buck & Vitt,
1986), cannot be kept separate from Neckeraceae. This view
is supported by recently published molecular phylogenies (see
also Olsson & al., 2009a,b), as well as by the present study that
reveals all “Thamnobryaceae” species to be deeply nested inside
the Neckeraceae, with the largest genus Thamnobryum itself
being highly polyphyletic. For example, Thamnobryum tumidicaule is placed in the first branching lineage of clade A (Neckera
group) forming a new genus together with Homalia glabella, as
described below. Similarly, Touwia elliptica and T. negrosensis
were until recently included in Thamnobryum. The transfer to
Touwia (Olsson, 2010) is not only confirmed in the present study
by the molecular analyses but is also morphologically sound
since the two Thamnobryum species share morphological similarities with the type of the generic name Touwia laticostata,
and are morphologically distinct from Thamnobryum, as noted
earlier by Ochyra (1990). In the new concept, the three species of
Touwia that are all rheophytic (growing in flowing water) have a
restricted distribution area in Australasia and SE Asia (Ochyra,
1986, 1990; Enroth, 1989). However, all the rheophytic taxa in
44
TAXON 60 (1) • February 2011: 36–50
Neckeraceae (cf. Enroth, 1999) do not form a monophyletic
group despite some similar morphological adaptations. It has
been pointed out earlier that, e.g., the rheophytic Thamnobryum
species (T. fernandesii, T. cataractarum, T. angustifolium) are
radiations from the surrounding T. alopecurum populations
showing the same morphological response to the extreme habitat
(Olsson & al., 2009c).
The majority of the Thamnobryum species, including the
type of the generic name T. alopecurum, however, form an almost maximally supported clade sister to the remaining species
of clade B. Although this sister clade also hosts three additional
Thamnobryum species (T. pandum, T. pumilum, T. fasciculatum), the phylogenetic relationships are uncertain. The exclusion of T. tumidicaule and T. fasciculatum (see Fig. 1) from
Thamnobryum renders the peculiar T. liesneri from Venezuela
as the single representative of the genus in the South American
continent (Allen & Churchill, 2002).
We expect that a more thorough sampling inside clade B,
as indicated by an upcoming study (Buchbender & al. unpub.),
will resolve the remaining questions related to the phylogenetic relationships of Thamnobryum pandum, T. pumilum and
T. fasciculatum as well as the other polyphyletic taxa inside the
“Poro-”clade. We therefore refrain from any further nomenclatural changes in this group at this stage. The only exception
is Porotrichum madagassum that is resolved among Porotrichodendron species. Since this grouping also receives morphological support a transfer of Porotrichum madagassum is justified.
The placement of Chileobryon callicostelloides (previously Pinnatella callicostelloides), a unispecific genus from
Chile (including the Juan Fernández Islands), has been uncertain. Our analyses support the view of Brotherus (1925), who
placed it in Neckeraceae. It is in fact not close to Pinnatella but
forms a group together with the Australasian Pendulothecium
punctatum, Echinodium hispidum and E. umbrosum. The latter two species were only recently excluded from Echinodium
s.str., and transferred to Thamnobryum by Stech & al. (2008)
in an attempt to clarify the phylogeography of Echinodiaceae.
Therefore, the sampling inside Neckeraceae was limited, and
with a more extensive taxon sampling it becomes evident that
these species do not belong in Thamnobryum but form an independent clade sister to Pendulothecium punctatum. The sporophytes of the two Echinodium species and the three Pendulothecium species (Enroth & He, 1991) are almost identical, but
the apophysal stomata in the former are immersed (vs. superficial in Pendulothecium) and the spores are smaller (12–14 µm
in the Echinodium species and 16–20 µm in Pendulothecium;
cf. Churchill, 1986; Enroth & He, 1991). However, there are
clearer differences in the gametophytes, justifying erecting a
new genus that we name Echinodiopsis for Echinodium hispidum and E. umbrosum. Those two species have a stem central
strand (lacking in Pendulothecium), foliose pseudoparaphyllia
(lacking in Pendulothecium), long, very strong and excurrent
costae with internal differentiation (in Pendulothecium ending in mid-leaf or reaching to 5/6 leaf length at most, and of
homogeneous cells), and a completely different leaf shape with
bistratose parts. The clade formed of Chileobryon, Pendulothecium and Echinodiopsis is phytogeographically coherent
TAXON 60 (1) • February 2011: 36–50
and southern amphi-Pacific. Chileobryon is known from the
Juan Fernández Islands and mainland Chile, while the two
other genera are distributed in Australasia, especially in New
Zealand and some of the adjacent islands. All species also grow
in very similar, moist and shady habitats, with soil and rocks
being the preferred substrates, but also on tree bases and logs
(Churchill, 1986; Enroth & He, 1991; Enroth, 1992b).
The polyphyly of the genus Homalia is intriguing, since it is
a morphologically fairly coherent group (cf. He, 1997). Homalia
webbiana and H. pennatula were excluded from Neckeraceae in
a previous study (Olsson & al., 2009b), and H. glabella belongs
to clade A in the present study. With the transfer of Homalia
glabella to a new genus, Homalia s.str. is left with three species:
H. lusitanica, H. trichomanoides and H. giraldii. However, in
the current analyses H. lusitanica and the remaining Homalia
species are resolved in a grade to clade B, which contradicts
our previous results based on more extensive sequence data
(Olsson & al., 2009b). However, there is no significant support
backing up this scenario. It is probably an artefact due to the
lesser amount of available sequence-level information, which
was discussed in more detail by Olsson & al. (2010); therefore
there is no need to make any nomenclatural changes considering H. lusitanica. The systematic position of Homalia seems
to differ according to taxon sampling and the markers used
for inferring phylogenies, indicating the importance of taxon
sampling and the quality of the sequence markers.
TAXONOMIC AND NOMENCLATURAL
CHANGES
Forsstroemia goughiana (Mitt.) S. Olsson, Enroth & D. Quandt,
comb. nov. ≡ Neckera goughiana Mitt. in J. Proc. Linn.
Soc., Bot. 1 (Suppl.): 120. 1859.
Forsstroemia yezoana (Besch.) S. Olsson, Enroth & D. Quandt,
comb. nov. ≡ Neckera yezoana Besch. in Ann. Sci. Nat.,
Bot., sér. 7, 17: 358. 1893.
See Enroth (1994b) for a discussion of the species and its
distribution.
Neckera Hedw., Sp. Musc. Frond.: 200. 1801, nom. cons. –
Type: Neckera pennata Hedw. (typ. cons.).
= Alsia Sull., Proc. Amer. Acad. Arts 3: 184. 1855, syn. nov. –
Type: Alsia californica (Hook. f. & Arn.) Sull. (Neckera
californica Hook. f. & Arn.).
Leptodon D. Mohr, Observ. Bot.: 27. 1803, nom. cons. – Type:
Leptodon smithii (Hedw.) F. Weber & D. Mohr (Hypnum
smithii Hedw.).
= Cryptoleptodon Renauld & Cardot in Bull. Soc. Roy. Bot.
Belgique 38: 30. 1899, syn. nov. – Type (see Enroth, 1992a):
Cryptoleptodon pluvinii (Brid.) Broth.
Leptodon acuminatus (M. Fleisch.) S. Olsson, Enroth &
D. Quandt, comb. nov. ≡ Cryptoleptodon acuminatus
M. Fleisch. in Hedwigia 59: 212. 1917.
Olsson & al. • Neckera and Thamnobryum
Exsertotheca S. Olsson, Enroth & D. Quandt, gen. nov.
Genus Exsertotheca plantis dioicis relative robustis foliis
nitidis undulatis, parietibus cellularum foliorum crassis et porosis et costis vulgo brevissimis, capsulis longe exsertis, typice
operculis oblique et longissime rostratis, in Europa, Macaronesia et Asia austro-occidentali distributum.
Type: Exsertotheca crispa (Hedw.) S. Olsson, Enroth &
D. Quandt.
Plants medium-sized to large, with the fronds irregularly to
pinnately branched. Central strand absent in the stem. Leaves
usually strongly undulate and glossy (although expressions
with smooth and falcate leaves frequent in E. intermedia, rare
in E. crispa), not very complanate, asymmetric, oblong to
elongate-oblong or ovate-oblong, distinctly decurrent, with
a blunt to shortly acuminate apex. Leaf margins plane, entire
or nearly so below and denticulate towards the apex; costa
very short and double, occasionally (in E. crispa) reaching to
2/5 of leaf length. Leaf cells smooth, with strongly to moderately incrassate and distinctly porose walls; alar cells quadrate
or rectangular, often forming triangular groups. Paraphyllia
lacking. Pseudoparaphyllia (cf. Cubero & al., 2006) leaf-like
(sometimes with few filamentous ones intermixed), usually
3–4 (but number varying from 1 to 7) per branch primordium,
to ca. 0.9 mm long. Plants dioicous, sporophytes relatively
infrequently produced. Perichaetial leaves erect and closely
sheathing, oblong to ovate, narrowed to an acuminate apex (in
N. intermedia more abruptly than in N. crispa), with a short,
often double costa; post-fertilization growth considerable, the
inner leaves eventually reaching over 5 mm long. Seta smooth,
in N. crispa 8–12 mm (Brotherus, 1923; Smith, 2004), in N. intermedia 10–17 mm long (Hedenäs, 1992). Capsule orthotropous, ovoid, ca. 2.5 mm long; a columella reaching to over
half of the capsule length present in mature capsules. Apophysal stomata phaneroporous. Peristome double; exostome
teeth yellowish, when dry curved inwards, lacking borders
and with reduced dorsal ridges, striolate and with papillose
upper parts in N. crispa, but rather papillose throughout in
N. intermedia; endostome reduced, consisting of a relatively
high (ca. 100–150 μm), faintly papillose basal membrane and
vestiges of segments. Calyptra cucullate, smooth or with few
hairs in the basal parts. Operculum obliquely long-rostrate.
Spores 15–25(–30) μm in diameter, fairly coarsely papillose.
Exsertotheca is a European—SW Asian genus, both species
also occurring in Macaronesia (Hedenäs, 1992).
Exsertotheca crispa (Hedw.) S. Olsson, Enroth & D. Quandt,
comb. nov. ≡ Neckera crispa Hedw., Sp. Musc. Frond.:
206. 1801.
Exsertotheca intermedia (Brid.) S. Olsson, Enroth &
D. Quandt, comb. nov. ≡ Neckera intermedia Brid.,
Muscol. Recent. Suppl. 2: 24. 1812.
Alleniella S. Olsson, Enroth & D. Quandt, gen. nov.
Genus hoc Neckerae similis. Species duae dioicae, foliis
levibus, setis longis, capsulis exsertis et propagula vegetativa
producentes. Species ceterae huius generis autoicae, foliis
45
Olsson & al. • Neckera and Thamnobryum
praecipue undulatis, setis brevibus, capsulis immersis vel emergentibus et propagula vegetativa non producentes.
Type: Alleniella complanata (Hedw.) S. Olsson, Enroth
& D. Quandt.
Etymology. – The genus is named after Dr. Bruce Allen
of the Missouri Botanical Garden, one of the foremost moss
taxonomists of our time.
Plants from small (A. besseri) to robust; branching more
or less pinnate. Central strand absent in the stem. Leaves complanate, smooth (A. besseri, A. complanata, A. brownii) or distinctly undulate and glossy; the smooth-leaved species with
rounded or obtuse-mucronate leaf apices, the others with more
acute leaf apices. Costa short and often double, or virtually absent. Leaf cells smooth, relatively thin-walled and non-porose
except often near the leaf base; alar cells shorter, often quadrate
or nearly so, but not in sharply delimited groups. Pseudoparaphyllia leaf-like, lanceolate to nearly filamentous. Four species (A. besseri, A. complanata, A. brownii, A. chilensis) lack
paraphyllia, six species have them. Dioicous and often with
flagelliform branchlets as vegetative propagula (A. besseri,
A. complanata) or autoicous and without vegetative propagula.
Perichaetial leaves with strong post-fertilization growth. Seta
7–10 mm long, capsule long-exserted (A. besseri, A. complanata), or seta short and capsule immersed (in A. chilensis capsule short-exserted). Capsule orthotropous, ovoid to cylindric.
Apophysal stomata phaneroporous, in A. besseri, A. complanata, A. brownii and A. hymenodonta very few (less than five
per capsule) and highly vestigial. Peristome double; exostome
teeth papillose throughout or striolate at base and papillose
elsewhere, or rather papillose throughout, unbordered; median
line slightly zig-zag, weakly developed trabeculae at back; endostome with a well-developed, up to ca. 100 μm high basal
membrane, segments mostly subulate, papillose throughout
and often with narrow median perforations. Calyptra cucullate, glabrous or with some hairs in the basal part. Operculum
obliquely rostrate. Spores mostly fairly coarsely papillose,
(15–)20–35 μm in diameter.
Alleniella besseri (Lob.) S. Olsson, Enroth & D. Quandt, comb.
nov. ≡ Homalia besseri Lobarz. in Naturwiss. Abh. (Vienna) 1: 48. 1847 (Neckera besseri (Lobarz.) Jur. in Verh.
Zool.-Bot. Ges. Wien 10: 368. 1860).
Alleniella brownii (Dixon) S. Olsson, Enroth & D. Quandt,
comb. nov. ≡ Neckera brownii Dixon in New Zealand Inst.
Bull. 3(5): 266. 1927.
Alleniella chilensis (Schimp. ex Mont.) S. Olsson, Enroth &
D. Quandt, comb. nov. ≡ Neckera chilensis Schimp. ex
Mont. in Ann. Sci. Nat., Bot., ser. 2, 6: 147. 1836.
Alleniella complanata (Hedw.) S. Olsson, Enroth & D. Quandt,
comb. nov. ≡ Leskea complanata Hedw., Sp. Musc. Frond.:
231. 1801 (Neckera complanata (Hedw.) Huebener, Muscol.
Germ.: 576. 1833).
Alleniella hymenodonta (Müll. Hal.) S. Olsson, Enroth &
46
TAXON 60 (1) • February 2011: 36–50
D. Quandt, comb. nov. ≡ Neckera hymenodonta Müll. Hal.
in Bot. Zeitung (Berlin) 9: 564. 1851.
Alleniella remota (Bruch & Schimp. ex Müll. Hal.) S. Olsson,
Enroth & D. Quandt, comb. nov. ≡ Neckera remota Bruch
& Schimp. ex Müll. Hal., Syn. Musc. Frond. 2: 51. 1850.
Alleniella scabridens (Müll. Hal.) S. Olsson, Enroth &
D. Quandt, comb. nov. ≡ Neckera scabridens Müll. Hal.
in Bot. Zeitung (Berlin) 5: 828. 1847.
Alleniella submacrocarpa (Dixon) S. Olsson, Enroth &
D. Quandt, comb. nov. ≡ Neckera submacrocarpa Dixon
in Smithsonian Misc. Collect. 72(3): 12. 1920.
Alleniella urnigera (Müll. Hal.) S. Olsson, Enroth & D. Quandt,
comb. nov. ≡ Neckera urnigera Müll. Hal., Syn. Musc.
Frond. 2: 57. 1850.
Alleniella valentiniana (Besch.) S. Olsson, Enroth &
D. Quandt, comb. nov. ≡ Neckera valentiniana Besch. in
Ann. Sci. Nat., Bot., sér. 6, 10: 273. 1880.
Thamnomalia S. Olsson, Enroth & D. Quandt, gen. nov.
Genus hoc cognoscitur caulibus frondosis, irregulatim ramosis, areolatione foliorum cellulis apicalibus parietibus satis
crassis et cellulis medianis parietibus clare tenuioribus et cellulis alaribus infirme vel haud differentiatis. Species duo praecipue in America centrali et in archipelago Indiae occidentalis
distributae sunt et plerumque ad rupes in silvis humidis habitant.
Type: Thamnomalia glabella (Hedw.) S. Olsson, Enroth
& D. Quandt.
Plants frondose, branching rather irregular. Central strand
present in the stem (sometimes quite indistinct). Leaves strongly
complanate, symmetric in T. tumidicaulis, asymmetric in
T. glabella. Apical teeth in the leaves of T. glabella unicellular,
in T. tumidicaulis often composed of 2–3 cells. Costa single and
strong, ending shortly below the leaf apex in T. tumidicaulis,
in T. glabella weak and short, often double. Leaf cells smooth;
apical cells relatively strongly incrassate and sometimes porose,
median laminal and their subjacent cells with clearly thinner
walls; alar cells scarcely if at all differentiated. Pseudoparahyllia, foliose, in T. glabella intermingled with filamentous ones.
Dioicous. Sporophytes known only for T. glabella, as described
by He (1997).
Thamnomalia glabella (Hedw.) S. Olsson, Enroth & D. Quandt,
comb. nov. ≡ Leskea glabella Hedw., Sp. Musc. Frond.:
235. 1801. (Neckera glabella (Hedw.) F. Weber & D. Mohr,
Index Mus. Pl. Crypt.: 3. 1803. Hypnum glabellum (Hedw.)
Sw. ex P. Beauv., Prodr. Aethéogam.: 64. 1805. Homalia
glabella (Hedw.) Schimp., Bryol. Eur. 5, fasc. 44–45, Monogr. 2: 54. 1850).
Thamnomalia tumidicaulis (K.A. Wagner) S. Olsson, Enroth & D. Quandt, comb. nov. ≡ Thamnium tumidicaule
K.A. Wagner in Bryologist 55: 145. 1952 (Thamnobryum
TAXON 60 (1) • February 2011: 36–50
tumidicaule (K.A. Wagner) F.D. Bowers in Bryologist 77:
162. 1974).
The two species of Thamnomalia have very similar geographic ranges. Both species occur in Central America and
the West Indies; T. glabella is also known from SE Brazil (cf.
He, 1997; Buck, 1998). Both species grow mainly on rocks and
rarely on tree trunks; T. glabella thrives at 400–2500 m and
T. tumidicaulis at 600–1200 m (Buck, 1998).
Echinodiopsis S. Olsson, Enroth & D. Quandt, gen. nov.
Genus hoc simile generis Echinodii in Macaronesia, se
praecipue cellulis alaribus non differentiatis, cellulis foliorum
plerumque leviter mamillosis et seta gradatim verus capsulam
inspissata differt. In Australasia distributum est.
Type: Echinodiopsis hispida (Hook. f. & Wilson) S. Olsson, Enroth & D. Quandt.
Plants dark-green to blackish, dull, variably branched,
thriving in shady, moist places, and most often growing on
rocks or soil, sometimes also on tree bases. Leaves narrow,
lanceolate or subulate from a triangular or an ovate base. Costa
very strong, long-excurrent in E. hispida and percurrent to
short-excurrent in E. umbrosa. Leaf margins and apical parts
of the lamina at least partly bistratose. Alar cells not differentiated. Pseudoparaphyllia leaf-like. Dioicous. Seta red or
reddish-orange, distinctly flaring below the apophysis. Stomata
immersed. Capsule orientation varying from reclinate to antitropous, sometimes homotropous. Annulus well-differentiated
with 1–3 cell rows. Peristome unreduced “hypnoid”.
Echinodiopsis hispida (Hook. f. & Wilson) S. Olsson, Enroth
& D. Quandt, comb. nov. ≡ Hypnum hispidum Hook. f.
& Wilson in London J. Bot. 3: 552. 1844 (Leskea hispida
(Hook. f. & Wilson) Mitt. in J. Proc. Linn. Soc., Bot. 4: 91.
1859. Echinodium hispidum (Hook. f. & Wilson) Reichardt, Reise Novara 1(3): 127. 1870. Thamnobryum hispidum
(Hook. f. & Wilson) M. Stech & al. in Organisms Divers.
Evol. 8: 290. 2008).
Echinodiopsis umbrosa (Mitt.) S. Olsson, Enroth & D. Quandt,
comb. nov. ≡ Leskea umbrosa Mitt. in J. Linn. Soc., Bot.
4: 92. 1859 (Echinodium umbrosum (Mitt.) A. Jaeger in
Ber. Thätigk. St. Gallischen Naturwiss. Ges. 1876–77: 314.
1878. Thamnobryum umbrosum (Mitt.) M. Stech & al. in
Organisms Divers. Evol. 8: 290. 2008).
Echinodiopsis umbrosa var. glaucoviride (Mitt.) S. Olsson,
Enroth & D. Quandt, comb. nov. ≡ Hypnum glaucoviride
Mitt. in Hooker, Handb. New Zeal. Fl.: 473. 1867 (Sciaromium glaucoviride (Mitt.) Mitt. in Seemann, Fl. Vit.:
400. 1873. Echinodium glaucoviride (Mitt.) A. Jaeger in
Ber. Thätigk. St. Gallischen Naturwiss. Ges. 1876–77:
314. 1878. Echinodium hispidum var. glaucoviride (Mitt.)
Dixon in New Zealand Inst. Bull. 3(5): 249. 1927. Echinodium umbrosum var. glaucoviride (Mitt.) S.P. Churchill
in J. Bryol. 14: 129. 1986. Thamnobryum umbrosum var.
glauco-viride (Mitt.) M. Stech & al. in Organisms Divers.
Evol. 8: 290. 2008).
Olsson & al. • Neckera and Thamnobryum
Note. – Stech & al. (2008) tabulated the morphological
distinctions in the gametophytes of Echinodium s.str. and
in the two species placed here in Echinodiopsis. Most of the
differences are rather relative, and the single clear-cut one is
the well-differentiated alar cells in Echinodium vs. the nondifferentiated alar cells in Echinodiopsis. There are also some
differences in the sporophytes. In Echinodiopsis the capsules
are mostly reclinate to antitropous, while in Echinodium they
vary from nearly orthotropous to orthogonal (Hedenäs, 1992).
The seta in Echinodiopsis distinctly flares below the apophysis.
The stomata in Echinodium (at least in E. setigerum and E. renauldii, cf. Hedenäs, 1992) are superficial, but in Echinodiopsis
they are immersed (Churchill, 1986; also our own observation).
Porotrichodendron madagassum (Kiaer ex Besch.) S. Olsson,
Enroth & D. Quandt, comb. nov. ≡ Porotrichum madagassum Kiaer ex Besch. in Ann. Sci. Nat., Bot., sér. 6, 10: 332.
1880 (Thamnium madagassum (Kiaer ex Besch.) Kindb.
in Hedwigia 41: 236. 1902).
Note. – Crosby & al. (1983) regarded Porotrichum madagassum, Porothamnium hildebrandtii (Müll. Hal.) M. Fleisch.
and Porotrichum pennaefrondeum Müll. Hal. as taxonomic
synonyms of Porothamnium comorense (Müll. Hal.) Sim. According to Sloover (1983) however, Porothamnium comorense
is a synonym of Porotrichum elongatum (Welw. & Duby) Gepp,
Porothamnium hildebrandtii is a synonym of Porothamnium
stipitatum (Mitt.) Touw ex De Sloover (= Porotrichum stipitatum (Mitt.) W.R. Buck), and Porotrichum pennaefrondeum
is a synonym of P. madagassum (cf. also Een, 1976). We agree
with De Sloover’s concepts.
ACKNOWLEDGEMENTS
SO acknowledges financial support by the Helsingin Sanomat
Centennial Foundation and the Research Foundation of the University of Helsinki. Furthermore, the authors received support from two
researcher exchange grants Finnish Academy/DAAD (JE, DQ) and
DAAD/STINT (VB, LH, SH, SO, DQ), which is highly acknowledged.
Research was funded by the Deutsche Forschungsgemeinschaft (DFG
QU 153/3-1 153/3-2) and SYNTHESYS (VB, JE, SO), which was financed by the European Community Research Infrastructure Action
under the FP6 “Structuring the European Research Area” Program
(http://www.sysnthesys.info). Mr. Heino Vänskä, Lic. Phil., is cordially thanked for the Latin diagnoses. In addition, we thank Frank
Müller (Dresden), Andy Cairns (James Cook University), Terry Hedderson (University of Cape Town) and Ron Porley (English Nature)
for providing us with additional research material.
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Appendix. List of specimens used in the study including EMBL or GenBank accession numbers for the sequenced or downloaded regions and voucher details. In three cases sequence data have been already submitted to GenBank from previous studies and thus the accession numbers for rps4-trnT-trnL-trnF
are composed of two different accession numbers. * denotes taxa for which nomenclatural changes are suggested in this article.
DNA no, species, herbarium, voucher ID, EMBL or GenBank acc. no rps4- trnF, rpl16, ITS.
B116, Alsia californica (Hook. & Arn.) Sull.*, B, Bryo 234031, FM210280, FM160946, FM161073; B141, Anomodon giraldii Müll. Hal*, H, H3194078, AM990342,
FM210763, FM161075; SH10, Camptochaete arbuscula var. tumida (Sm.) Reichardt, H, Streimann 51408, AM990353, FM160955, FM161087; B617, Chileobryon
callicostelloides (Broth. ex Thér.) Enroth, H, H 3107865, FM210283, FM200841, FM161088; B423, Cryptoleptodon longisetus (Mont.) Enroth*, H, H3038483,
AM990356, FM160957, FM161091; B421, Cryptoleptodon pluvinii (Brid.) Broth.*, Huttunen, Huttunen s.n., China, Hunan, FM210284, FM160958, FM161092;
B223, Curvicladium kurzii (Kindb.) Enroth, NYBG, Akiyama Th-85, FM210285, FM160959, FM161093; SH146, Dolichomitriopsis diversiformis (Mitt.) Nog.,
H, MHA, Nedoluzhko s.n., AM990362; (trnLF = AF397777), FM160963, FM161098; B195, Echinodium hispidum (Hook. f. & Wilson) Reichardt*, Buchbender,
Downing s.n., 29.10.2000, FM210286, FM160964, FM161099; B258, Echinodium umbrosum (Mitt.) A. Jaeger var. glaucoviride (Mitt.) S.P. Churchill*, SchäferVerwimp, Streimann 49634, EU434010, FM160965, EU477602; B768, Forsstroemia neckeroides Broth., H, Akiyama & al. 381, FN868963, FN868978, FN868972;
B226, Forsstroemia producta (Hornsch.) Paris, H, Koponen 46545, FM201504, FM160967, FM161102; B196, Forsstroemia trichomitria (Hedw.) Lindb., Buchbender, Streimann & Pocs 65120A, AM990365, FM160968, FM161103; B349, Heterocladium dimorphum (Brid.) Schimp., H, H3212307, AM990376, FM160970,
FM161115; B352, Heterocladium procurrens (Mitt.) A. Jaeger, H, H3212289, AM990379, FM160973, FM161118; B422, Homalia glabella (Hedw.) Schimp.*, H,
Townsend 93/291, AM990382, FM160977, FM161123; B111, Homalia lusitanica Schimp., B, B275202, AM990383, FM160978, FM161124; B218, Homalia trichomanoides (Hedw.) Schimp., Quandt, Olsson 105, AM990385, FM160980, FM161126; B474, Homalia webbiana (Mont.) Schimp., H, Müller K68, AM990387,
FM160982, FM161127; B110, Homaliodendron exiguum (Bosch & Sande Lac.) M. Fleisch, B, B263509, AM990389, FM160984, FM161130; B230, Homaliodendron flabellatum (Sm.) M. Fleisch., H, H3071675, FM210290, FM160985, FM161132; B424, Homaliodendron neckeroides Broth., H, H3071953, FM210306,
FM161015, FM161168; SH103, Lembophyllum clandestinum (Hook. f & Wilson) Lindb., H, Vitt 29644, AM990401; (trnLF = AF397823), FM160996, FM161145;
B131, Leptodon smithii (Hedw.) F. Weber & D. Mohr, B, B268385, AM990403, FM160997, FM161147; B253, Neckera besseri (Lobarz.) Jur.*, Quandt, Olsson
107, FM210294, FM161003, FM161156; B367, Neckera brownii Dixon*, H, Tangney 2330, FM210295, FM161004, FM161157; B106, Neckera chilensis Taylor*, B,
B264587, FM210304, FM161013, FM161166; B193, Neckera complanata (Hedw.) Huebener*, Buchbender, Buchbender 204, AM990413, FM161005, FM161158;
B248, Neckera crenulata Harv., H, Long 33980, FM210297, FM161006, FM161159; B192, Neckera crispa Hedw.*, Buchbender, Buchbender 385, FM210298,
FM161007, FM161160; B127, Neckera douglasii Hook., B, B253879, FM210299, FM161008, FM161161; B249, Neckera goughiana Mitt.*, H, Koponen 46476,
FM210300, FM161009, FM161162; B128, Neckera himalayana Mitt., B, B253876, FM210301, FM161010, FM161163; B427, Neckera hymenodonta Müll. Hal.*,
H, H3206871, FM210302, FM161011, FM161164; B471, Neckera intermedia Brid.*, H, Samaniego & Manso s.n. 12.10.1999, FM210303, FM161012, FM161165;
B161, Neckera menziesii Drumm., NYBG, Halse 4878, FM210305, FM161014, FM161167; B347, Neckera pennata Hedw., H, H3203794, AM990414, FM161016,
FM161169; B250, Neckera polyclada Müll. Hal., H, Koponen 45441, FM210307, FM161017, FM161170; B307, Neckera remota Bruch & Schimp. ex Müll. Hal.*, S,
B29895, AM990415, FM161018, FM161171; B105, Neckera scabridens Müll. Hal.*, H, Kürschner & al. 95-498, FM210308, FM161019, FM161172; B470, Neckera
submacrocarpa Dixon*, Enroth, Pocs 90021/AL, FM210309, FM161020, FM161173; SH301, Neckera urnigera Müll. Hal.*, S, B15194, AM990416, FM161021,
FM161174; B544, Neckera valentiniana Besch.*, Bolus Herb., Univ. Cape Town, Hedderson 16404, FM210310, FM161022, FM161175; B298, Neckera warburgii
Broth., B, Bryo 253855, FM210311, FM161023, FM161176; B251, Neckera yezoana Besch.*, H, Enroth 70675, FM210312, FM161024, FM161177; B313, Neckeropsis
nitidula (Mitt.) M. Fleisch., S, B105713, AM990419, FM161030, FM161183; B476, Pendulothecium punctatum (Hook. f. & Wilson) Enroth & S. He, S, Streimann
53845, AM990421, FM161033, FM161187; B260, Pinnatella anacamptolepis (Müll. Hal.) Broth., S, B104516, FM210318, FM161036, FM161190; B472, Pinnatella
kuehliana (Bosch & Sande Lac.) M. Fleisch., Enroth, Müller S116, FM20150, FM161038, FM161192; B099, Porotrichodendron robustum Broth., B, B264620,
AM990426, FM200845, FM161197; B294, Porotrichodendron superbum (Taylor) Broth., H, H3121100, AM990427, FM161043, FM161198; SH372, Porotrichopsis
flacca Herzog, S, Churchill & al. 17201, FM201506, FM161044, FM161199; B244, Porotrichum bigelovii (Sull.) Kindb., H, Shevock & Kellman 27467, AM990428,
FM161045, FM161200; B117, Porotrichum frahmii (Enroth) Enroth, B, B255332, AM990429, FM161046, FM161201; SH252, Porotrichum madagassum Kiaer ex
Besch.*, Vanderpoorten, Quandt, Vanderpoorten FSA 244, FM210322, FM210764, FM161203; B559, Rigodium pseudothuidium Dusén, NYBG, NYBG 00892248,
–, –, FM161210; Rp47, Rigodium pseudothuidium Dusén, H, H3134254, AM990438 (trnLF = AF543547), FM161051, –; B149, Taiwanobryum speciosum Nog.,
H, Enroth 64877, AM990442, FM161055, FM161216; B238, Thamnobryum alopecurum (Hedw.) Nieuwl. ex Gangulee, Buchbender, Buchbender s.n. 11.7.2003,
AM990444, FM161056, FM161218; B539, Thamnobryum cataractarum N. Hodgetts & Blockeel, S, B3725, FM201507, FM161057, FM161219; B546, Thamnobryum ellipticum (Bosch & Sande Lac.) Nieuwl.*, Enroth, Müller S114, FM210325, FM161058, FM161220; B190, Thamnobryum fasciculatum (Sw. ex Hedw.) I.
Sastre, NYBG, Buck 26902, FM210326, FM161059, FM161221; B549, Thamnobryum fernandesii Sérgio, S, B9965, FM201508, FM161060, FM161222; SH300,
Thamnobryum maderense (Kindb.) Hedenäs, S, B44108, AM990445, FM161061, FM161223; B165, Thamnobryum neckeroides (Hook.) E. Lawton, NYBG,
Buck 37648, FM201509, FM161062, FM161224; B420, Thamnobryum negrosense (E.B. Bartram) Z. Iwats. & B.C. Tan*, H, Schäfer-Verwimp & Verwimp 16852,
FM210327, FM161063, FM161225; B311, Thamnobryum pandum (Hook. f. & Wilson) I.G. Stone & G.A.M. Scott, H, H3208440, FM210328, FM161064, FM161226;
B120, Thamnobryum pumilum (Hook. & Wilson) B.C. Tan, B, B268163, FM210329, FM200843, FM161227; B574, Thamnobryum rudolphianum Mastracci,
BM, BM000919859, FM201510, FM161065, FM161228; B233, Thamnobryum speciosum (Broth.) Hoe, H, H3141827, FM201511, FM161066, FM161229; B148,
Thamnobryum subserratum (Hook. ex Harv.) Nog. & Z. Iwats., H, Enroth 64595, AM990446, FM161067, FM161230; B429, Thamnobryum tumidicaule (K.A.
Wagner) F.D. Bowers*, H, H3141850, AM990447, FM161068, FM161231; B261, Touwia laticostata Ochyra, JCT, Cairns B349, FM210330, FM161070, FM161233;
DQ, Weymouthia mollis (Hedw.) Broth., CHR, Quandt, 99-Mo2, AM990452, FM161072, FM161237.
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