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Phylogeny, classification and species delimitation in the liverwort
genus Odontoschisma (Cephaloziaceae)
Silvia C. Aranda,1,2* S. Robbert Gradstein,3* Jairo Patiño,4 Benjamin Laenen,4,5 Aurélie Désamoré4,5
& Alain Vanderpoorten4
1 Departamento de Biogeografía y Cambio Global, Museo Nacional de Ciencias Naturales (CSIC), C/José Gutiérrez Abascal 2,
28006 Madrid, Spain
2 Azorean Biodiversity Group (GBA, CITA-A) and Platform for Enhancing Ecological Research & Sustainability (PEERS),
Universidade dos Açores, Departamento de Ciências Agrárias, Rua Capitão João d’Ávila, 9700-042 Angra do Heroísmo,
Azores, Portugal
3 Muséum National d’Histoire Naturelle, Dept. Systématique et Evolution, Case Postale 39, 57 rue Cuvier, 75231 Paris cedex 05,
France
4 Institute of Botany, University of Liège, 4000 Liège, Belgium
5 Institut für Systematische Botanik, Zollikerstrasse 107, 8008 Zürich, Switzerland
* contributed equally to this paper
Author for correspondence: Silvia C. Aranda, [email protected]
ORCID: SCA, http://orcid.org/0000-0001-6373-8924
DOI http://dx.doi.org/10.12705/635.12
Abstract A species-level phylogeny of Odontoschisma (Jungermanniidae: Cephaloziaceae) was produced to revisit the
infrageneric classification and delimit the species within the genus. New methods of species delimitation have been used
to explicitly contrast taxonomic hypotheses and test the relevance of the morphological traits traditionally used in this
group. The results confirm previous evidence suggesting that the circumscription of Odontoschisma needs to be enlarged
to include Iwatsukia and Cladopodiella, and further indicate that a third genus, Anomoclada, is nested within it. Twentythree molecular entities were recognized based the results of generalized mixed Yule-coalescent (GMYC) analyses. These
entities partly conflicted with traditionally defined species that were shown to belong to different, not necessarily closely
related entities, adding to the growing body of evidence calling for an extensive revision of species delimitations in taxa
with reduced morphologies like leafy liverworts, using an integrative taxonomic approach. A fully revised classification
of Odontoschisma into five sections, twenty species, and three subspecies is presented. While the species reported from
Europe, Asia and North America were of polyphyletic origins, all Neotropical species were resolved as monophyletic, which
could result from a combination of fast speciation rates and reduced dispersal in the Neotropics, and potential extinction in
other areas, especially sub-Saharan Africa.
Keywords GMYC; infrageneric classification; integrated taxonomy; liverworts; molecular phylogeny; Neotropics;
polyphyletic species
Supplementary Material Electronic Supplement (Table S1; Fig. S1) and alignment are available in the Supplementary Data
section of the online version of this article at http://www.ingentaconnect.com/content/iapt/tax
INTRODUCTION
The growing body of molecular data fuelled by ongoing
large-scale barcoding projects, coupled with the fast development of bioinformatics tools, offer a unique context for objective species delimitations (Monaghan & al., 2009; Fujita & al.,
2012). Probably one of the most widely used approaches to date,
the generalized mixed Yule-coalescent (GMYC) method, aims
at delimiting independently evolving species by identifying
the nodes that define the transitions between inter- and intraspecific processes (Fujisawa & Barraclough, 2013; Talavera
& al., 2013). This method has been applied in a wide range of
situations, for example when rapid (Barley & al., 2013) and/
or recent (Brewer & al., 2012) divergence is not accompanied
by morphological change, and in complex patterns of microendemism (Vuataz & al., 2013). Since taxonomic issues in
describing and understanding biodiversity patterns culminate
as organisms decrease in size and observable morphological
complexity (Whittaker & al., 2005), techniques such as GMYC
have been shown to be especially useful in taxa with reduced
morphologies such as amphipods (Murphy & al., 2013) and,
among plants, in algae (Payo & al., 2013) and ferns (Chang
& al., 2013). In bryophytes, cryptic speciation has been repeatedly reported (e.g., Heinrichs & al., 2010; Kreier & al., 2010;
Received: 17 Jan 2014 | returned for first revision: 2 Jul 2014 | last revision received: 1 Sep 2014 | accepted: 1 Sep 2014 | not published online ahead
of inclusion in print and online issues || © International Association for Plant Taxonomy (IAPT) 2014
1008
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Orzechowska & al., 2010; Ramaiya & al., 2010). In the absence
of subsequent morphological re-evaluation, however, cryptic
species have only rarely been formally described, calling for
the increasing need of an integrative taxonomic approach in
the group (Medina & al., 2012, 2013; Heinrichs & al., 2013).
Here, we apply the GMYC model in the context of the
phylogeny of the widespread, tropical-holarctic liverwort
genus Odontoschisma (Dumort.) Dumort. The last comprehensive treatment of the genus, which dates back to the early
20th century (Stephani, 1908), included 30 species that are
now considered to belong to five genera in four families,
including Chiloscyphus Corda (Lophocoleaceae), Lethocolea Mitt. (Acrobolbaceae), Notoscyphus Mitt. (Geocalyceae),
Odonto­schisma and Anomoclada Spruce (Cephaloziaceae)
(e.g., Fulford, 1968; Schuster, 1974, 2002; Gradstein & Costa,
2003; So, 2004; Gradstein, 2013). The genus has been differently classified in Cephalozi­aceae, Adelanthaceae or its own
family, Odontoschismataceae (see Schuster, 1974, for discussion). Recent molecular-phylogenetic studies have unequivocally recovered the genus as a member of Cephaloziaceae
(Forrest & al., 2006; Vilnet & al., 2012). Odontoschisma is
defined by having rigid stems without a hyalodermis, leafless
ventral branches, undivided leaves, leaf cells with conspicuous trigones, underleaves reduced and with slime cells, and
antheridial walls made up of irregularly arranged, non-tiered
cells (Schuster, 1974, 2002). The circumscription of Odonto­
schisma was, however, recently challenged by molecular
analyses showing that Iwatsukia jishibae (Steph.) N.Kitag. and
the two species of Cladopodiella H.Buch are nested within
Odontoschisma (Vilnet & al., 2012), from which they differ
by their bifid instead of unlobed leaves. Furthermore, Anomo­
clada portoricensis (Hampe & Gottsche) Steph., only species
in the genus Anomoclada Spruce, is morphologically very
similar to Odonto­schisma (Stephani, 1908; Gradstein & al.,
2001; Schuster, 2002), but their relationships have not been
analysed yet.
A first infrageneric classification of Odontoschisma was
proposed by Schuster (1974), who arranged the holarctic species
into three sections: sect. Odontoschisma (O. grosseverrucosum Steph., O. prostratum (Sw.) Trevis., O. sphagni (Dicks.)
Dumort.) with only ventral branching, bordered leaves and no
gemmae; sect. Denudata R.M.Schust. (O. denudatum (Nees)
Dumort., O. elongatum (Lindb.) A.Evans) with lateral and ventral branching, unbordered leaves and with gemmae; and sect.
Macounia R.M.Schust. (O. macounii (Austin) Underw.) with
the same characters as sect. Denudata but lacking secondary
pigmentation. A few tropical species were tentatively added by
Schuster (2002), but a classification on a worldwide basis has
not been attempted yet.
In the present study, we produced a species-level phylogeny of Odontoschisma based on three plastid markers. We
first revisited the infrageneric classification and delimitated
the species within the genus, explicitly contrasting traditional
taxonomic hypotheses. We then used the phylogeny to test the
relevance of morphological traits previously used for species
delimitations. Based on these results, a fully revised classification of the genus is proposed.
MATERIALS AND METHODS
Taxonomic sampling and molecular protocols. — Two
sampling strategies were employed to circumscribe Odonto­
schisma. The first was carried out at the level of Cephalozi­
aceae, considering a large sample of the genera included in
the family. The second sampling was performed to define
species within the genus and determine their phylogenetic
relationships. The first set of analyses (Analysis I) included 16
Odontoschisma specimens, each representing one of 18 species currently included in the genus (Fulford, 1968; Schuster,
1974, 2002; Gradstein & Costa, 2003; So, 2004; Váňa & al.,
2013; Gradstein, 2013, unpub.). Cladopodiella fluitans (Nees)
Jørg., C. francisci (Hook.) Jørg., Iwatsukia jishibae, I. bifida
(Fulford) Schust. and Anomoclada portoricensis were also
included in the sampling to test their possible relations with
Odontoschisma. Species of all other genera of Cephaloziaceae
as circumscribed by Crandall-Stotler & al. (2009) and Frey
& Stech (2009), except Haesselia Grolle & Gradst., Metahygrobiella R.M.Schust. and Trabacellula Fulford, were employed
as outgroups, including Nowellia curvifolia (Dicks.) Mitt.,
Fusco­cephaloziopsis lunulifolia (Dumort.) Váňa & L.Söderstr.,
Cepha­lozia bicuspidata (L.) Dumort., Schiffneria hyalina
Steph., Hygrobiella laxifolia (Hook.) Spruce, Pleurocladula
albescens (Hook.) Grolle, Schofieldia monticola J.D.Godfrey
and Alobiellopsis parvifolia (Steph.) R.M.Schust. In the second set of analyses (Analysis II), multiple accessions of each
Odonto­schisma species were sampled whenever possible to test
their monophyly; 46 accessions were analysed in total (Appendix 1). We were unable to sequence the rare Odontoschisma
purpuratum Herzog (Malaysia), O. soratamum Fulford (Colombia) and Iwatsukia spinosa (Fulford) R.M.Schust. (Venezuela)
due to the lack of sufficiently recent specimens for DNA studies. In particular, O. soratamum and I. spinosa are only known
from the type specimen.
DNA extraction was conducted using the DNeasy Plant
Minikit (Qiagen Benelux B.V., Venlo, The Netherlands). In
Analysis I, sequences of the trnL-F region were produced for
the ingroup taxa and downloaded from GenBank (http://www
.ncbi.nlm.nih.gov/genbank) for the outgroups. In Analysis II,
the trnL-F region, the atpB-rbcL intergenic spacer and the
rps4 gene were sequenced for each accession. We initially
used the universal primers described by Shaw & al. (2003),
but due to amplification problems with a considerable number of accessions, we re-designed specific primer pairs for
the atpB-rbcL spacer (atpB_odonto 5′-GTTCCTARAGATA
GAAGATACATTCTC-3′ and rbcL_odonto 3′-AGTCTCCGT
TTGTGGTGACA-5′) and trnL-F region (trnC_odonto 5′-GAT
TGTTTCCATATTCAGGG-3′ and trnF_odonto 3′-CCTCTG
CTCTACCRACTGA-5′).
The three loci were amplified by polymerase chain reaction (PCR) in a 20 µl volume containing 10 µl RNase-free
demineralized H 2O, 4 µl reaction buffer 5×, 0.8 µl dNTPs
(1 mM each), 1.5 µl of 50 mM MgCl2, 0.8 µl of each primer
(10 µM), 0.8 µl bovine serum albumin (BSA), 0.8 µl dimethyl
sulfoxide (DMSO), 0.5 µl of Go Taq DNA polymerase (5 Uµ–1)
and 5 µl DNA. PCR cycling consisted of 5 min denaturation at
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94°C, followed by 30 cycles of 30 s denaturation at 94°C, 30 s
annealing at 52°C, 50 s extension at 72°C and finally 4 min
at 72°C. PCR products were sent to Macrogen (http://www
.macrogen.com/) for purification and DNA sequencing.
Sequences were assembled and edited using Sequencher
v.4.01 (Gene Codes, 1998) and contigs were aligned with
MAFFT v.7 (Katoh & Standley, 2013). Manual refinement of
the aligned sequences was performed with SeaView v.4.4.0
(Gouy & al., 2010), inserting gaps where necessary to preserve
positional homology. Indels were scored as binary characters
regardless of their length using the single indel coding (SIC)
algorithm in SeqState v.1.4.1 (Müller, 2005).
Phylogenetic analyses and topological hypothesis testing. — Phylogenetic trees were estimated using Bayesian
inference (BI) and maximum likelihood (ML) performed in
MrBayes v.3.2.2 (Ronquist & al., 2012) and RAxML v.8.0
(Stamatakis & al., 2008), respectively. The three loci were
concatenated into a combined dataset after checking visually
the congruence of independent analyses for each locus. Indels
were added to a separate binary character matrix. The general
time reversible (GTR) with a gamma distribution to take variation among sites into account was selected as the best-fit model
based on the minimum Akaike information criterion (AIC)
with jModelTest v.2.1.4 (Darriba & al., 2012). A separate model
with identical forward and reverse transition rates was applied
to the indel matrix. For BI analyses, all model parameters were
unlinked and estimated independently across data partitions
except topology and branch length. Four independent Markov
Chain Monte Carlo (MCMC) chains were run for 5 million
generations, with default uniform priors, and the posterior
distribution was sampled every 1000th generations to ensure
independence from successive sampling. Burn-in was pruned
and effective sample size (ESS) estimation was used to assess
MCMC convergence in Tracer v.1.5 (Rambaut & Drummond,
2007). For ML analyses, support for branches was assessed by
a non-parametric bootstrap analysis with 100 replicates
Constrained analyses were performed to test the likelihood of the topology resulting from the Bayesian inference
(i.e., null hypothesis) against three alternative hypotheses forcing traditional classifications of (1) Cladopodiella fluitans and
C. francisci as sister species, (2) Odontoschisma sphagni and
O. prostratum as different species, and (3) the monophyly of
O. grosseverrucossum accessions. The clades corresponding
to sect. Odontoschisma, sect. Macounia and sect. Denudata
were kept constant in both the null and alternative hypotheses,
following the recommendations of Bergsten & al. (2013). Model
likelihoods were estimated with the stepping-stone method
(Xie & al., 2011) using 196,000 MCMC steps sampled every
500th generations for each of 50 b-values between 1 (posterior)
and 0 (prior) after discarding the first 196,000 generations as
initial burn-in set by default. The contribution to the marginal
likelihood from each step is estimated from a sample-size of
392. Analyses were run for four independent MCMC chains
from which the arithmetic mean of marginal likelihoods was
estimated for each model to calculate Bayes factors (BF).
Phylogenetic species delimitation. — We used the generalized mixed Yule-coalescent (GMYC) model to delimit
1010
putative species on the basis of phylogenetic information (for
review, see Fujisawa & Barraclough, 2013). This method diagnoses species-level clades by identifying the shift in diversification rate associated with the change from reticulate evolution
(a neutral coalescent model) to divergent evolution (a Yule pure
birth model). The null model assumes that the entire sample
derives from a single population undergoing a single coalescent
process, whereas the GMYC model classifies the observed
branching time intervals into two categories, as the result of
either inter- or intraspecific processes of lineage sorting. A likelihood ratio test is then used to identify the best-fit model. The
method was extended to allow multiple thresholds to account
for variation in the timing to speciation (Monaghan & al.,
2009). Although the multiple threshold version may show a certain tendency to oversplitting, its use has been recommended
to explore delimitation changes when the assumptions of the
single threshold needs to be relaxed and when, for instance,
the sampling of individuals across a representative occupancy
range may be achieved (Fujisawa & Barraclough, 2013).
In order to apply the GMYC technique, we first dated the
obtained phylogeny by performing a relaxed-clock analysis
in BEAST v.1.7.5 (Drummond & al., 2012). We employed four
independent MCMCs to sample a prior distribution of absolute
substitution rates derived from the analysis of the entire Liverwort Tree of Life calibrated with 21 fossils (unpub. results). This
distribution had a mean of 4.453 × 10–4 and a standard deviation
of 1.773 × 10–6 substitutions per site per Ma. Each MCMC was
run for 100 million generations, with sampling every 10,000th
generations under a birth-death and a Yule speciation model,
respectively. The latter was selected against the former based
on Bayes factors and employed in subsequent analyses. Convergence and mixing of the four chains was checked using
the program Tracer v.1.5. One thousand trees were discarded
as burn-in and the remaining trees from each of the four runs
were combined.
The 50% majority-rule chronogram derived from the dating analysis was then used to apply the GMYC model. Following Powell & al. (2011), we ran the analyses without removing
the outgroups. The GMYC output also produced a lineagethrough-time plot, which we visually evaluated for changes in
branching rate. Single and multiple-threshold GMYC models
were run using the SPLITS package in R, with default options
(Ezard & al., 2009). After estimating likelihoods for single
(Pons & al., 2006) and multiple thresholds (Monaghan & al.,
2009), a modified Akaike information criterion corrected for
small sample size (AICc; for details see Powell, 2012) was used
to identify the best GMYC model.
Morphological analysis. — Each accession was scored for
20 morphological characters that have been used in the classification of Odontoschisma (Appendix 2). Ancestral character
state reconstructions were performed using a reverse-jump
Markov Chain Monte Carlo (hereafter RJ-MCMC) (Pagel
& Meade, 2006), as implemented in BayesTraits v.2.0 (Pagel
& al., 2004). Character evolution was mapped on the sample
of trees from the posterior probability distribution produced
by the MrBayes analysis (see below) after pruning of the outgroups. At each iteration, the chain samples a tree, one of
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Aranda & al. • Phylogeny of Odontoschisma
TAXON 63 (5) • October 2014: 1008–1025
four transition models (including one or two rate models, and
models wherein either the forward or the backward rate is 0),
and values of rate parameters. The resulting combination of
those parameters is then accepted or rejected depending on
the Metropolis-Hastings term. When a combination of tree and
rate parameters is accepted, the rate values are used to derive
the set of ancestral states at each internal node simultaneously
(“global approach”; Pagel, 1999). The chain was run for 10 million generations, discarding 25% of burn-in and sampling every
10,000th generation. To circumvent the issue associated with
the fact that not all of the sampled trees necessarily contain
the internal nodes of interest, reconstructions were performed
using a most recent common ancestor (MRCA) method. This
method identifies, for each tree in the Bayesian sample, the
MRCA to a group of species and reconstructs the state at the
node, then combines this information across trees. In order to
contrast alternative hypotheses regarding the ancestral state at
key nodes of the phylogeny, we also implemented the “local”
approach, wherein the significance of the reconstruction is
explicitly tested at each node of interest (Pagel, 1999). For that
purpose, we successively fixed each of the nodes of interest at
one of the states it can possibly take. Then, the RJ-MCMC was
re-run as described above. A second, independent chain was
run to sample rate parameters and derive overall likelihoods of
the reconstructions when the node was fixed at its alternative
state(s). Bayes factors were used to determine the support for
alternative states.
Circumscription and intra-generic classification of Odontoschisma. — The 50% majority-rule consensus of the trees
sampled from the posterior probability distribution generated
by the MrBayes analysis of the trnL-F matrix (Analysis I) is
presented in Fig. 1. All Odontoschisma species sampled were
resolved within a clade supported with a posterior probability
(PP) of 100 and a ML bootstrap support (BS) of 100%. The two
species of Iwatsukia, the two species of Cladopodiella, and
Anomoclada were nested within that clade.
In the trnL-F, rps4, and atpB-rbcL matrix (Analysis II),
27.8% of the 1604 sites were variable within Odontoschisma.
The four independent MCMC MrBayes runs showed good mixing with large effective sample sizes (ESS > 200) and converged
successfully to the stationary phase, as shown by an average
standard deviation of split frequencies of 0.006 and average
potential scale reduction factor for parameter values of 1. The
50% majority-rule consensus of the 6622 trees sampled from
the posterior probability distribution is presented in Fig. 2.
Odontoschisma sect. Odontoschisma (including O. prostratum, O. sphagni and O. grosseverrucosum) and sect. Denudata (including O. macounii, O. denudatum, O. sandvicense
(Ångstr.) A.Evans, O. subjulaceum Austin, O. naviculare
(Steph.) Grolle, O. cleefii Gradst. & al., O. longiflorum (Taylor)
Trevis., O. variabile (Lindenb. & Gottsche) Trevis., O. engelii
Gradst. & Burghardt, O. brasiliense Steph., O. portoricense,
O. prostratum O4
98/100
100/100
88/-
RESULTS
Fig. 1. Fifty per cent majority-rule consensus
of the trees sampled from the posterior probability distribution generated by a Bayesian
analysis of the trnL-F region showing the
relationships of Odonto­schisma, Iwatsukia,
Cladopodiella and Anomoclada species in
Cephaloziaceae. Numbers above branches
correspond to Bayesian posterior probabilities (left) and non-parametric bootstrap
proportions (right) from the maximum
likelihood analysis. Accession identifiers
are given for newly generated sequences.
Species names follow the new nomenclature
(see below).
O. sphagni OD6
O. grosseverrucosum OG3
O. fluitans CFLU
88/-
O. bifidum IWA
82/-
O. jishibae
O. macounii OD7
O. denudatum OD8
O. longiflorum O3
100/100
99/-
O. engelii OEN1
100/96
58/-
O. variabile OV4
O. portoricense O8
O. brasiliense OBRA
99/99/-
O. denudatum subsp. naviculare ON3
O. denudatum subsp. sandvicense O11
O. elongatum OE1
O. francisci CFRA
Alobiellopsis parvifolia
69/-
Hygrobiella laxifolia
100/99
Schiffneria hyalina
Nowellia curvifolia
99/89
70/67
Cephalozia bicuspidata
99/52
100/-
Fuscocephaloziopsis lunulifolia
Pleurocladula albescens
Schofieldia monticola
0.05
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1011
1012
Version of Record (identical to print version).
D
93/68
E
72/-
F
73/-
G
H
98/75
K
99/75
51/-
100/100
82/78
100/89
84/84
U
0.04
78/62
100/100
100/100
98/65
100/100
R
OQ
100/98
N
100/94
100/100
T
100/99
V
97/66
J M
I P
100/92
100/100
S
98/-
99/90
L
98/-
100/94 100/100
100/98
100/96
100/100 100/-
C
88/75
100/-
100/100
O. prostratum O4
O. sphagni OSP14
O. prostratum OPR11
O. sphagni OD6
O. prostratum O6
O. sphagni OSP1
O. prostratum OPR2
O. sphagni OSP4
O. prostratum OPR1
O. sphagni OD1
O. grosseverrucosum OG3
O. bifidum IWA
O. jishibae
O. fluitans CFLU
O. macounii OD7
O. macounii OM1
O. macounii OM3
O. macounii OM2
O. denudatum OD18
O. denudatum subsp. sandvicense O11
O. denudatum OD13
O. denudatum OD8
O. denudatum OD12
O. denudatum OD15
O. denudatum OD17
O. denudatum subsp. naviculare ON3
O. cleefii O9
O. longiflorum O3
O. cf. longiflorum OV2
O. engelii OEN1
O. variabile DPAR
O. variabile OV3
O. variabile OV4
O. variabile OV5
O. brasiliense OBRA
O. portoricense O8
O. portoricense OPOR
O. zhui DENA1
O. zhui DENA2
O. zhui ON2
O. elongatum OE2
O. elongatum OE1
O. elongatum OSP10
O. pseudogrosseverrucosum O7
O. pseudogrosseverrucosum OG2
O. francisci CFRA
Schiffneria hyalina
Nowellia curvifolia
Cephalozia bicuspidata
Fuscocephaloziopsis lunulifolia
sect. Cladopodiella
sect. Denudata
sect. Iwatsukia
sect. Neesia
sect. Odontoschisma
Fig. 2. Phylogram of the 50% majority-rule consensus of the trees sampled by the MrBayes analysis based on atpB-rbcL, trnL-F and rps4 sequences within Odontoschisma. The phylogenetic
position of O. jishibae (dashed branch) is only based on trnL-F sequence. Numbers above branches correspond to Bayesian posterior probabilities (left) and non-parametric bootstrap proportions (right) from the maximum likelihood analysis. Branches in bold represent accessions grouped within the same molecular entity by the GMYC analysis. Letters indicate the nodes for
character state reconstruction (see Electr. Suppl.: Table S1).
A
100/100
98/-
B
100/100
100/98
83/-
77/99
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O. zhui Gradst. & al., O. elongatum and O. pseudogrosseverrucosum Gradst. & al.) were resolved with PP/BS values of
100/100 and 72/-, respectively. Section Odontoschisma showed
a synapomorphic acquisition of bordered leaves and a transition of leaf surface from concave to ± flat, while the absence of
lateral branches was homoplastic (see, respectively, characters
6, 12 and 3 in Appendix 2). The inclusion of O. portoricense
(= Anomoclada portoricensis) within sect. Denudata was supported by lateral branches, unbordered leaves and presence
of gemmae, and its sister relationship with O. brasiliense by
a synapomorphic increase in gametophyte size (character 1,
Appendix 2). Anomoclada-type branches, previously considered exclusive to O. portoricense, were observed in several
unrelated species of sect. Denudata (node M, Fig. 2; Table
S1), so that the evolution of this trait was homoplastic (character 4, Appendix 2). Section Macounia was nested within sect.
Denudata; some of its characteristic features were independently acquired by several other members of sect. Denudata.
Thus, mid-leaf cell size (character 10) showed a synapomorphic
increase independently in sect. Macounia and in the clade of
O. portoricense and O. brasiliense (nodes G and R in Fig. 2,
respectively), and the cuticle (character 16) shifted independently from finely verruculose to smooth in sect. Macounia and
O. elongatum (Appendix 2). Odontoschisma francisci (Hook.)
L.Söderstr. & Váňa (= Cladopodiella francisci) was sister to
sect. Denudata, whereas O. fluitans (Nees) L.Söderstr. & Váňa
(= C. fluitans) and the position of the two Iwatsukia species
was unresolved outside of these two main sections. Morphologically, Iwatsukia spp. and O. fluitans are unique within
Odonto­schisma in having leaves divided to 1/3 of their length
(Appendix 2). The polyphyletic origin of the two Cladopodiella species was further supported by the constrained analyses, where forcing the two species into monophyly resulted in
a substantial decrease in the marginal log-likelihood (BF =
26.21). Accordingly, traits previously identified as diagnostic
for Cladopodiella, including the presence of nodular thickenings on alternate long walls in the capsule epidermis (character
20) and bifid leaves (character 7), were reconstructed as having
evolved at least twice independently (Table S1).
Within sect. Denudata, the first dichotomy resolved a clade
with a posterior probability of 72 but lacking ML bootstrap
support, comprised of two accessions of O. pseudogrosseverrucosum on the one hand, and the remaining species of the
section on the other, which were characterized by the synapomorphic lack of underleaves and appressed to squarrose
gemmiparous leaves (characters 17 and 18 in Appendix 2).
The South American accessions of the section formed a fully
supported clade (node O, Fig. 2), whose most recent common
ancestor was dated at 29 (21–39) Ma (Electr. Suppl.: Fig. S1).
The sister clade (node J, Fig. 2) was formed by accessions of
O. denudatum from Europe, Australasia and Hawaii, which
were morphologically characterized by the shared presence of
Anomoclada-type branches (character 4, Appendix 2). Within
clade O, the relationship between O. longiflorum, O. engelii,
and O. variabile was supported by the synapomorphic transition towards elongate leaves with a length to width ratio of up
to 1.5 : 1 (character 8, Appendix 2).
Phylogenetic species delimitation within Odontoschisma.
— The single-threshold GMYC was identified as the best-fit
model (AICc = 134.05) over models with multiple thresholds.
Under the single-threshold model, the null hypothesis (i.e., all
specimens belong to a single species) could be significantly
rejected (P = 0.011). Twenty-three molecular entities were
identified by the GMYC model within the genus (Fig. 2), 9 as
distinct clusters of haplotypes and 14 as singletons.
All accessions of O. sphagni and O. prostratum but one
(OD1) were identified as a single species morphologically characterized by the synapomorphic transition from obtuse or acute
to long acuminate or ciliate female bract apices (character 19,
Appendix 2). The respective accessions of these two species
did not form monophyletic groups, and constraining the accessions of O. sphagni on the one hand, and of O. prostratum on
the other, to monophyly, resulted in a substantial decrease in
log-likelihood (BF = 34.19). Species represented by a single
accession, including O. fluitans, O. francisci, O. bifidum,
O. brasiliense and O. engelii were not recognized as closest
relatives to each other. Multiple accessions of O. longiflorum,
O. macounii, O. portoricense, O. elongatum and O. variabile
were resolved as monophyletic with high supported values of
and were recognized as distinct species by the GMYC analysis
(Fig. 2). The three accessions of O. grosseverrucosum (labelled
as O. pseudogrosseverrucosum and O. grosseverrucosum in
Fig. 2) were resolved as polyphyletic, two accessions from
Japan forming a fully supported clade that was sister to the
remainder of sect. Denudata and one accession from China
that was included within sect. Odontoschisma with full support.
Consistent results were shown by constraint analyses enforcing the three accessions together, which did not support the
monophyly hypothesis (BF = 119.11). Odontoschisma denudatum
as previously circumscribed was polyphyletic. One accession
from Colombia (labelled as O. cleefii in Fig. 2) was resolved
within a clade also comprised of O. longiflorum and O. engelii.
Three monophyletic accessions from China initially labelled as
O. zhui in Fig. 2 were recovered as a distinct species (PP/BS
values of 100/100). The group was supported by a synapomorphic transition towards appressed gemmiparous leaves (character 18, Appendix 2). The remaining accessions of O. denudatum were resolved as paraphyletic. The core group of four
European accessions was recognized by the GMYC model as
a distinct species sister to a clade comprised of two accessions
from Hawaii (node L in Fig. 2), one of O. denudatum (= O. subjulaceum) and the other of O. denudatum subsp. sandvicense
(= O. sandvicense). These two clades were sister to a clade
comprised of two accessions (node N, Fig. 2), one of O. denudatum from Japan and one of O. denudatum subsp. naviculare
(= O. naviculare), each recovered as a distinct species.
DISCUSSION
Circumscription and infrageneric classification of Odontoschisma. — The present analyses confirm previous evidence
suggesting that the circumscription of Odontoschisma needs
to be enlarged to include Iwatsukia and Cladopodiella (Vilnet
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& al., 2012) and further indicate that a third genus, Anomoclada, is nested within it. In contrast to recent taxonomic treatments identifying Anomoclada as a separate genus (Fulford,
1968; Gradstein & al., 2001; Gradstein & Costa, 2003), the
present results indicate that Anomoclada needs to be synonymized with Odontoschisma, adding to the growing body of
evidence challenging the taxonomic status of the large number
of monotypic liverwort genera described from South America
(Gradstein & al., 2001). The inclusion of Anomoclada into the
synonymy of Odontoschisma is consistent with the general
morphological similarity between the two taxa, which both
have prostrate stems with ventral stolons and without hyalodermis, succubous undivided leaves, thick-walled leaf cells with
distinct trigones and rudimentary underleaves with slime cells.
The two main features that led Spruce (1876) and subsequent
taxonomists to recognize Anomoclada at the genus level were
the abundant secretion of slime by the underleaves and the
development of the leafy branches from the dorsal side of the
stem, so-called Anomoclada-type branches (Crandall-Stotler,
1969). Evans (1903), however, showed that mucilage secretion
on underleaves also occurs in Odontoschisma, yet to a much
lesser degree. The close morphological similarity of the two
genera is further supported by the presence of Anomocladatype branches in O. denudatum (Schuster, 1974) and newly
reported here in O. longiflorum. Ancestral character state
reconstructions indicated that evolution of this trait has been
homoplastic and cannot serve as a criterion that warrants recognition of Anomoclada as a distinct genus.
Two of the three sections identified within Odontoschisma
(Schuster, 1974), namely sect. Odontoschisma and sect. Macounia, were resolved as monophyletic, but the recognition of the
latter would render sect. Denudata paraphyletic. This suggests
that sect. Macounia should be merged with sect. Denudata,
which is consistent with the sharing of morphological traits
between O. macounii and other members of sect. Denudata,
such as presence of lateral branching, concave leaves without border, mid-leaf cells 25–40 µm, rounded to acute apices of female bracts, and asexual reproduction by gemmae.
The circumscription of sect. Denudata needs to be further
expanded to include O. portoricense, O. brasiliense, O. longiflorum, O. variabile, O. engelii, O. sandvicense, O. naviculare,
O. macounii and three new species (see below). The inclusion of O. brasiliense within sect. Denudata is at odds with its
strongly bordered leaves and apparent lack of gemmae, which
are characteristic of sect. Odontoschisma. The species deviates
from members of sect. Odontoschisma, however, by producing lateral branches (even though sparingly), which are always
absent in the species of that section.
The inclusion of Iwatsukia spp., O. fluitans, and O. francisci in Odontoschisma, but outside of sect. Odontoschisma
and sect. Denudata, makes it necessary to accommodate these
taxa in new sections. The two species formerly included in
Iwatsukia form a clade and are accommodated within the new
section Iwatsukia. Conversely, the two species of the former
genus Cladopodiella are resolved as polyphyletic and are
therefore accommodated into two new Odontoschisma sections, sect. Cladopodiella comb. nov. and sect. Neesia sect.
1014
nov., respectively. The polyphyly of the two species previously
included in Cladopodiella indicates that the sharing of morphological traits by these two species, such as bifid leaves, tiered
antheridial wall cells (Schuster, 1974), and the tendency for
nodular thickenings in the capsule epidermis to be developed
on all longitudinal walls instead of on alternate longitudinal
walls only, is homoplastic. The development of nodular thickenings on alternate walls is a characteristic and constant feature of
several liverwort families, including Calypogeiaceae, Cephaloziaceae (excluding Hygrobiella Spruce), Lepidoziaceae, and
Pleurozi­aceae (Schuster, 1984; Crandall-Stotler & al., 2009), so
that the independent acquisition of this trait in O. fluitans and
O. francisci was highly unexpected. The presence of species
with undivided or bilobed leaves in a single genus was hitherto
unknown in Cephaloziaceae. Nevertheless, genera including
species with either undivided or bilobed leaves are not rare in
leafy liverworts such as Kymatocalyx Herzog (Cephaloziell­
aceae), Marsupella Dumort. (Gymnomitriaceae), Plagiochila
(Dumort.) Dumort. (Plagiochilaceae), Syzygiella Spruce (Jamesoniellaceae), and various genera of Lepidoziaceae and Lophocoleaceae, even though leaves in these genera may sometimes
be shallowly bifid only. In leafy liverworts, leaves usually possess two or more growing points, each with its own embryonic
apical cell, so that developing leaves are initially typically lobed
(Schuster, 1984). Undivided leaves could therefore theoretically
be considered as ontogenetically derived, although phylogenetic evidence is equivocal (contrast, e.g., the order of acquisition of undivided vs. bilobed leaves in Plagiochila, Groth & al.,
2002; Roivainenia Perss. [= Syzygiella], Feldberg & al., 2010;
and Lophocolea (Dumort.) Dumort., Hentschel & al., 2007).
Species delimitation within Odontoschisma. — Twentythree molecular entities were recognized based on the results
of the GMYC analyses. These entities partly conflicted with
traditionally defined species that were shown to belong to different, not necessarily closely related entities. This adds to the
growing body of evidence showing the need for extensive revision of species delimitations in taxa with reduced morphologies like bryophytes using an integrative taxonomic approach
(Sukkharak & al., 2011; Dong & al., 2012; Hutsemékers & al.,
2012; Medina & al., 2012, 2013, Hedenäs & al., 2014).
Odontoschisma cleefii sp. nov. (Fig. 3), previously tentatively identified as a subspecies of O. denudatum on morphological grounds, is the most common species of the genus in
the páramos of the northern Andes and currently only known
from Colombia but expected to occur in neighbouring countries
as well. The new species is characterized by its concave leaves
densely covered by large papillae (ca. 4–15 µm long and 4–10 µm
wide), which are present all over the inner leaf surface. Such
large papillae are observed only in the eastern Asian species
O. grosseverrucosum and O. pseudogrosse­verrucosum. Further characteristics of O. cleefii include the frequent presence of
a whitish leaf border consisting of collapsed leaf-margin cells,
the presence of gynoecia in the upper portion of the stem, while
they occur in the lower portion of the stem in other species, and
the broadly rounded to somewhat obtuse apices of the female
bracts and bracteoles, which are never acute-acuminate like in
the other species of the genus. The plants are typically small in
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TAXON 63 (5) • October 2014: 1008–1025
size (0.8–1.5 mm wide) and dark purplish, which is presumably
an adaption to the strong irradiation in the high tropic-alpine
environment. Because of their dark pigmentation, most collections were previously identified as O. atropurpureum Steph.,
a name given in the past to all small, dark purplish pigmented
páramo plants of the genus including O. cleefii, O. denudatum
and O. variabile, to which the type of O. atropurpureum is now
assigned (Gradstein, 2013). Odontoschisma cleefii is separated
from O. denudatum and O. variabile by its coarsely papillose
leaf surfaces. In O. denudatum and O. variabile, the papillae
are usually very small, less than 2.5 µm long and only well
visible at the leaf margin, the leaf surfaces appearing smooth.
Odontoschisma variabile, moreover, differs by having flat,
not concave leaves.
The polyphyly of O. grosseverrucosum as previously circumscribed indicates that the focus on the presence of conspicuous papillae to identify one unique Asian species (Hattori,
1962; Gao & Cao, 2000; So, 2004) was misleading and that
they belong to two distinct species in different sections. The
existence of two species within O. grosseverrucosum s.l. was
noted by Hattori (1950), who described plants belonging to
O. pseudo­grosseverrucosum as “O. grosseverrucosum” and
the true O. grosseverrucosum as O. lutescens S.Hatt. In later
publications, however, Hattori (1962) did not maintain this distinction, and So (2004) showed that O. lutescens is a synonym
of the true O. grosseverrucosum. The accession from China,
resolved within sect. Odontoschisma, fully matches the morphological characters of the type, whereas the two accessions
from Japan are described as O. pseudogrosseverrucosum sp.
nov. (Fig. 4). Re-study of herbarium material showed that the
two species clearly differ in plant size, stem epidermis, branching, presence of asexual reproduction and leaf characters.
Odontoschisma pseudogrosseverrucosum is a smaller plant
than O. grosseverrucosum, measuring only 0.5–0.65(–0.8) mm
in width (0.8–1.6 mm in O. grosseverrucosum), the dorsal epidermis cells are smaller, subquadrate and thick-walled (rectangular and rather thin-walled in O. grosseverrucosum), the
leaves are distinctly concave and never bordered (rather flat
and bordered in O. grosseverrucosum) and lateral branches and
gemmae may be present (absent in O. grosseverrucosum). The
two species have also different geographical ranges, O. pseudo­
grosseverrucosum occurring in temperate eastern Asian (central Japan, South Korea, Russian Far East), whereas O. grosseverrucosum is a subtropical species ranging from southern
Japan to northern Thailand and Vietnam.
The specimens assigned here to O. zhui sp. nov. (Fig. 5)
were previously identified as O. denudatum on morphological grounds, but were resolved in the molecular analysis as a
separate lineage that is sister to O. elongatum. Odontoschisma
zhui is morphologically similar to O. denudatum but differs
from the latter by smaller leaf cells (13–22 µm long in midleaf), asymmetrical, curved-subfalcate leaves, and appressed
leaves on gemmiparous branches. In its peculiar leaf shape and
gemmi­parous shoots O. zhui is also similar to O. naviculare
from tropical SE Asia and New Caledonia, but it differs from
the latter by smaller leaf cells, absence of a dorsal leaf-free
strip, and predominantly ventral branching.
Within the O. denudatum clade, which includes O. denudatum, O. sandvicense and O. naviculare, the GMYC model
identified five molecular entities: a core European O. denudatum (4 accessions), O. naviculare (New Caledonia; 1 accession),
O. sandvicense (Hawaii; 1 accession), O. subjulaceum (Hawaii;
1 accession), and one further accession of O. denudatum from
Japan sister to O. naviculare. As a result, O. denudatum is paraphyletic in our analysis. One taxonomic interpretation would
be to strictly follow the GMYC criterion and indeed recognize
five species. We refrain, however, from doing so because the
accessions of O. denudatum and O. subjulaceum were morphologically identical, perfectly matching the morphological circumscription of the species. We believe that recognizing a truly
cryptic species in a genus where all other species display clear
morphological differentiation would not be sound and therefore
consider O. subjulaceum as a synonym of O. denudatum. A
second option would be to recognize three species, including
the core European O. denudatum, O. sandvicense (including the
O. denudatum subsp. sandvicense accession and the Hawaiian
O. denudatum), and O. naviculare (including the O. denudatum
subsp. naviculare accession and the Japanese accessions of
O. denudatum). In fact, the paraphyly of O. denudatum and the
strong geographic partitioning of genetic variation is consistent
with the phylogenetic patterns expected under budding speciation (Funk & Omland, 2003). This solution, however, would
render O. sandvicense and O. naviculare heterogeneous and
indistinguishable at the morphological level. Since these two
species can each be distinguished from O. denudatum by one
morphological trait, O. sandvicense differing by flat leaves
(concave in O. denudatum) and O. naviculare by curved-falcate
leaves (straight in O. denudatum) (see Appendix 1), we treat
O. sandvicense and O. naviculare as subspecies of O. denudatum. The use of subspecies has intimately been associated
with the idea of geographic separation (the “Rassenkreis” or
“geographical subspecies” in Meikle, 1957) and evolutionary
biologists traditionally used the subspecies category to diagnose geographically distinct populations that were thought to be
in the early stages of speciation (Mayr, 1963). Attribution of the
subspecies rank to O. sandvicense and O. naviculare is further
warranted by the fact that subspecies are unlikely to meet the
criterion of monophyly (Crandall & al., 2000) because they
represent an incipient stage of differentiation prior to reciprocal
monophyly (Zink, 2004).
The GMYC model failed to resolve O. sphagni and
O. prostratum as distinct. Constrained analyses further indicated that a monophyletic origin of accessions assigned to each
species can be rejected. Morphologically, O. prostratum differs
from O. sphagni mainly by smaller leaf cells and plant size.
The size difference is especially pronounced in eastern North
America, where both species occur. Moreover, the two species
differ in habitat preference, O. prostratum usually occurring
on soil or rock, whereas O. sphagni typically grows on peaty
soil (Schuster, 1974). In spite of their different ecological preferences, O. sphagni and O. prostratum show much overlap in
their morphology. European populations of O. sphagni may
be as small as those of O. prostratum, with leaves measuring
only 0.7–0.8 mm long. These plants can only be separated from
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O. prostratum by their somewhat larger leaf cells, measuring
20–35 µm long in O. sphagni and 15–22(–25) µm in O. prostratum. The trigones in O. sphagni are usually medium-sized and
the lumina are rounded, whereas O. prostratum typically has
small trigones and subquadrate lumina. Specimens of O. prostratum with medium-sized trigones and rounded lumina can,
however, be observed. Except for their habitat and slightly
smaller cells, these plants are inseparable from O. sphagni.
The leaf border can be slightly wider in O. prostratum (1–4 cells
wide) than in O. sphagni (1–2(–3) cells wide) (Schuster, 1974).
However, the leaf border is often not well-defined, its width
varies and clearly shows much overlap in both species, so that
this character does not allow for separating the two taxa. In the
light of the polyphyletic origin of accessions of both species
and the continuum in morphological variation in traits assumed
to be diagnostic, O. prostratum is reduced to synonymy under
O. sphagni, as proposed by Vilnet & al. (2012).
Biogeographic patterns in Odontoschisma. — The synonymy of O. prostratum and O. sphagni, and the polyphyly of
different accessions from North America, Europe, and Azores,
is reminiscent of similar evidence for recurrent trans-Atlantic
migrations across the North Atlantic in moss species (Szöevenyi
& al., 2008; Stenøien & al., 2011). Conversely, mounting evidence indicates that amphi-Atlantic bryophyte species sometimes correspond to complexes of semi-cryptic endemic species
(e.g., Heinrichs & al., 2011; Hutsemekérs & al., 2012; Medina
& al., 2012, 2013). Altogether, these observations suggest that
previous assessments of the patterns of amphi-Atlantic disjunctions in bryophytes based on check-lists, with 43% of the species of mosses found in North America also found in Europe,
and 70% of the moss species in Europe also found in North
America (Frahm & Vitt, 1993), need to be revised.
While the species reported from Europe, Asia and North
America were of polyphyletic origins, all of the Neotropical
species were resolved in a fully supported clade and only one
species of the group, O. variabile, has a disjunct Afro-American
range. Three hypotheses could be proposed to explain this pattern. First, the Neotropics appear as a center of diversification
for liverwort diversity (Gradstein & al., 2001; Vanderpoorten
& al., 2010b), potentially triggered by the Miocene uplift of the
Andes (Heinrichs & al., 2005a), and the recent origin of Neotropical species explains their endemicity. This hypothesis is,
however, at odds with the timing of diversification of the Neotropical Odontoschisma clade, 30 Ma. Second, the Neotropical
species have a low long-distance dispersal capacity owing, for
instance, to the poor tolerance of their spores to the drought and
frost conditions that prevail in high-altitude air currents. This
hypothesis is supported by the fact that spores of the páramo
endemic O. cleefii show a very poor drought resistance, losing
their capability of germination after one day of drying (Van
Zanten & Gradstein, 1988). Third, the Neotropical species of
Odontoschisma could be paleo-endemics. In particular, the comparatively low levels of Afro-American disjunctions (about 5%
of the flora of tropical America; Gradstein, 2013) as compared to
the North Atlantic disjunction, could be interpreted in terms of
the influence of extensive drought periods in Africa during the
Pleistocene, which led to an extensive decline of moist forests
1016
and possibly to the extinction of parts of the local hepatic flora
(Heinrichs & al., 2005b). These hypotheses are, however, not
mutually exclusive, and the high levels of Neotropical endemic
diversity observed in Odontoschisma, also reported in other
liverwort genera such as Diplasiolejeunea (Spruce) Schiffn.
(Dong & al., 2013), Leptoscyphus Mitt. (Vanderpoorten & al.,
2010a), and Plagiochila (Heinrichs & al., 2006), could result
from a combination of fast speciation rates, reduced dispersal
capacities and potential extinctions in other areas.
TAXONOMY
Based on the analyses presented here, the following classification of Odontoschisma is presented, with citation of
accepted name, basionym and type. Full synonymies, species
descriptions, keys to species, geographic distribution and ecological preferences are given in the forthcoming monograph of
the genus (Gradstein & Ilkiu-Borges, in press). Three species
not available for molecular analysis (O. purpuratum, O. soratamum, O. spinosum) are marked by an asterisk.
Odontoschisma (Dumort.) Dumort., Recueil Observ. Jungerm.:
19. 1835 ≡ Pleuroschisma sect. Odontoschisma Dumort.,
Syll. Jungerm. Europ.: 68. 1831 – Type: Odontoschisma
sphagni (Dicks.) Dumort. (≡ Jungermannia sphagni Dicks.).
= Anomoclada Spruce in J. Bot. 14 [= n.s. 5]: 133. 1876, syn. nov.
– Type: Anomoclada mucosa Spruce (= Odontoschisma
porto­ricense (Hampe & Gottsche) Steph.).
I. Odontoschisma sect. Odontoschisma
Branching exclusively ventral-intercalary. Leaves undivided. Leaf margins bordered. Mid-leaf cells 10–30 µm long,
with trigones. Cuticle smooth or papillose. Gemmae lacking.
Apices of female bracts long acuminate. Antheridial jacket
cells irregularly arranged.
1. Odontoschisma sphagni (Dicks.) Dumort., Recueil Observ.
Jungerm.: 19. 1835 ≡ Jungermannia sphagni Dicks., Fasc.
Pl. Crypt. Brit. [1]: 6. 1785 – Holotype: England, Surrey, “in
palustribus, Sphagno palustri frequenter adhaerens prope
Croydon Surriense” (BM n.v. [coll. Dickson; fide Grolle,
1976]; isotypes: S Nos. B29108!, B29109!, B29110!, B29111!,
UPS-THUNB n.v. [fide Grolle, 1976]).
= Odontoschisma prostratum (Sw.) Trevis. in Mem. Reale
Ist. Lombardo Sci., Ser. 3, Cl. Sci. Mat. 4: 419. 1877 ≡
Jungermannia prostrata Sw., Prodr.: 143. 1788 – Holotype: JAMAICA. “ad radices arborum in montibus”,
Swartz s.n. (S No. B98897!; isotypes: S Nos. B98896! [hb.
Lehmann] & B98895! [hb. Lehmann ex hb. Weber], STR!
[coll. Nees]).
2. Odontoschisma grosseverrucosum Steph. in Bull. Herb.
Boissier, sér. 2, 8: 593. 1908; Sp. Hepat 3: 377. 1908 – Lecto­
type (designated by So in J. Hattori Bot. Lab. 95: 252.
2004): TAIWAN. Mt. Taitum, Faurie 22 (G No. 000640
[barcode G00112865]!; isolectotype: BM).
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TAXON 63 (5) • October 2014: 1008–1025
II. Odontoschisma sect. Iwatsukia (N.Kitag.) Gradst., S.C.
Aranda & Vanderp. in Phytotaxa 162: 232. 2014 ≡ Iwatsukia
N.Kitag. in J. Hattori Bot. Lab. 27: 178. 1964 – Type: Iwatsukia exigua N.Kitag. (= Odontoschisma jishibae (Steph.)
L.Söderstr. & Váňa).
Branching exclusively ventral-intercalary. Leaves bifid,
apices acute to long acuminate. Leaf margins unbordered.
Mid-leaf cells 10–30 µm long, walls evenly thickened,
trigones absent. Cuticle along the middle lamella of the cell
walls densely and finely papillose. Gemmae lacking. Apices
of female bracts long acuminate. Arrangement of antheridial
jacket cells unknown.
3. Odontoschisma jishibae (Steph.) L.Söderstr. & Váňa in
Phyto­taxa 112: 13. 2013 ≡ Cephalozia jishibae Steph., Sp.
Hepat. 6: 437. 1924 ≡ Iwatsukia jishibae (Steph.) N.Kitag.
in Acta Phytotax. Geobot. 21: 114. 1965 – Lectotype (designated here): JAPAN. Shinano, Mt. Yaku, July 1908,
Jishiba 203 (G barcode G00061127!; isolectotype: JE!).
= Iwatsukia exigua N.Kitag. in J. Hattori Bot. Lab. 27: 178. 1964
(fide Gradstein & al., 2014) – Holotype: MALAYSIA.
Sabah, S slope of Mt. Kinabalu below Paca Cave, Iwatsuki
1070 (NICH!; isotype: JE!).
4. Odontoschisma bifidum (Fulford) Gradst., S.C.Aranda &
Vanderp. in Phytotaxa 162: 232. 2014 ≡ Cladomastigum bifidum Fulford in Acta Bot. Venez. 2: 80. 1967 ≡ Iwatsukia bifida (Fulford) R.M.Schust. in Bull. Natl. Sci.
Mus. Tokyo 11: 314. 1968 – Holotype: VENEZUELA.
Bolivar, Auyan-tepui, along Río Churún, SE of the “second wall”, 1690 m, 21 May 1963, Steyermark 93300 (NY
barcode 00713605!).
*5. Odontoschisma spinosum (Fulford) Gradst., S.C.Aranda
& Vanderp. in Phytotaxa 162: 232. 2014 ≡ Cladomastigum
spinosum Fulford in Mem. New York Bot. Gard. 23: 840.
1972 ≡ Iwatsukia spinosa (Fulford) R.M.Schust. in Trop.
Bryol. 2: 249. 1990 – Holotype: VENEZUELA. Bolivar,
summit of Meseta de Jáua, Steyermark 98009 (CINC n.v.).
III. Odontoschisma sect. Neesia Gradst., S.C.Aranda & Vanderp., sect. nov. – Type: Odontoschisma fluitans (Nees)
L.Söderstr. & Váňa (≡ Jungermannia fluitans Nees).
Branching exclusively ventral-intercalary. Leaves bifid,
apices rounded. Leaf margins unbordered. Mid-leaf cells large,
30–60 µm long, without trigones. Cuticle smooth. Gemmae
lacking. Apices of female bracts rounded to acute. Antheridial
jacket cells arranged in tiers.
6. Odontoschisma fluitans (Nees) L.Söderstr. & Váňa in
Phytotaxa 112: 12. 2013 ≡ Jungermannia fluitans Nees in
Funck, Krypt. Gew. Fichtelgeb. 29: specimen 593. 1823
≡ Cladopodiella fluitans (Nees) Jørg. in Bergens Mus.
Skrift., n.s., 16: 276. 1934 – Holotype: CZECH REPUBLIC. Riesengebirge, Schneekoppe, “in stehenden Wässern
der Weißwiese”, Funck s.n. (STR!).
IV. Odontoschisma sect. Cladopodiella (H.Buch) Gradst.,
S.C.Aranda & Vanderp., comb. & stat. nov. ≡ Cladopodiella H.Buch in Memoranda Soc. Fauna Fl. Fenn. 1: 89.
1927 – Type: Odontoschisma francisci (Hook.) L.Söderstr.
& Váňa (≡ Jungermannia francisci Hook.).
Branching exclusively ventral-intercalary. Leaves bifid,
apices subacute. Leaf margins unbordered. Mid-leaf cells
20–30 µm long, with small trigones. Cuticle smooth. Gemmae
present. Apices of female bracts narrowly rounded to subacute.
Antheridial jacket cells arranged in tiers.
7. Odontoschisma francisci (Hook.) L.Söderstr. & Váňa in
Phytotaxa 112: 12. 2013 ≡ Jungermannia francisci Hook.,
Brit. Jungermann.: pl. 49. 1816 ≡ Cladopodiella francisci
(Hook.) Jørg. in Bergens Mus. Skr., n.s., 16: 274. 1934 –
Lectotype (designated by Váňa & al. in Phytotaxa 112: 12.
2013): England, Hampshire, 1812, Lyell s.n. (BM barcode
BM001146107!).
V. Odontoschisma sect. Denudata R.M.Schust., Hepat. Anthocerotae N. Amer. 3: 833. 1974 (“Denudatae”) – Type:
Odonto­schisma denudatum (Nees) Dumort. (≡ Jungermannia denudata Nees).
= Odontoschisma sect. Macounia R.M.Schust., Hepat. Anthocerotae N. Amer. 3: 848. 1974 (“Macouniae”), syn. nov.
– Type: Odontoschisma macounii (Austin) Underw. (≡
Sphagnoecetis macounii Austin).
Branching lateral-intercalary and ventral-intercalary.
Leaves undivided or emarginate. Leaf margins unbordered,
occasionally bordered. Mid-leaf cells 10–40 µm long, with
trigones. Cuticle smooth or papillose. Gemmae usually present.
Apices of female bracts rounded to acute to short acuminate.
Antheridial jacket cells irregularly arranged.
8. Odontoschisma brasiliense Steph., Sp. Hepat. 3: 369. 1908 –
Lectotype (designated here): BRAZIL. Rio de Janeiro,
Glaziou 11760 (G barcode G00112855!; isolectotypes: BM!,
NY!).
9. Odontoschisma cleefii Gradst., S.C.Aranda & Vanderp., sp.
nov. – Holotype: COLOMBIA. Cundinamarca, páramo
Cruz Verde, laguna El Verjón, on humid soil in grass
páramo, 3300 m, 26 May 2012, Laura V. Campos 717
(COL!; isotype: PC barcode 0703249!). — For drawings
from the holotype, see Fig. 3.
Characterized by purplish color, concave leaves covered
by large papillae, frequent presence of a whitish leaf border
of collapsed cells, occurrence of gynoecia in upper portions
of shoots and broadly rounded to somewhat obtuse apices of
female bracts and bracteoles.
Plants prostrate to ascending, usually purplish in color,
older stem portions colorless, growing in small mats or creeping
loosely among other bryophytes. Leafy shoots 0.8–1.5 mm wide,
leafy branches ventral-intercalary or ventrolateral-intercalary,
stolons frequent, short or long, sometimes branched. Stems
0.15–0.2 mm in diameter, in cross section made up of 18–20
thick-walled epidermal cells surrounding larger and almost
Version of Record (identical to print version).
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Aranda & al. • Phylogeny of Odontoschisma
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thin-walled medullary cells; dorsal epidermis cells in surface
view quadrate to shortly rectangular, narrowly and evenly thickened arranged in straight rows. Leaves concave, contiguous to
imbricate, lamina standing upwards to spreading, insertion line
reaching dorsal midline, dorsal leaf-free strip absent; leaves
shortly ovate to subquadrate to suborbicular, ca. 0.5–0.7 mm
long, about as wide as long to slightly longer than wide, slightly
asymmetrical, apex rounded to truncate, dorsal margin curved,
dorsal base shortly decurrent, ventral margin curved and distinctly narrowed at the base, leaf sometimes with a whitish border. Leaf cells isodiametrical-hexagonal to slightly elongate,
20–30 µm long in mid-leaf, trigones medium-sized to large, light
brown to violet, darker pigmented than lumen, lumen rounded to
stellate, middle lamella indistinct; leaf margin cells sometimes
whitish-decolorate, especially along ventral and apical margin,
with a conspicuously thickened outer wall (5–12 µm thick), forming a whitish leaf border; oil-bodies not observed; cuticle covered
by large, low, colorless papillae, papillae rounded to slightly
elongate, 4–15 µm × 4–10 µm, 1–10 per cell, present all over leaf
surface but most prominent in lower half of leaf. Underleaves
Fig. 3. Odontoschisma cleefii (from the holotype). A, habit, dorsal
view; B, stem cross section; C, habit, ventral view; D, dorsal leaf-free
strip; E, leaf; F, mid-leaf cells; G, leaf margin. — Scale bars: A, C
= 500 µm; B = 50 µm; D = 200 µm; E = 250 µm; F, G = 25 µm. —
Drawn by A.-L. Ilkiu-Borges.
1018
rudimentary, broad scale-like, sometimes bifid with 2 short,
narrowly lanceolate lobes, with a few slime cells at margins and
on surface. Gemmae present or lacking, pale green, 1–2-celled,
± thick-walled, produced in whitish clusters on tips of stout,
upright, flagelliform shoots with appressed, scale-like leaves and
underleaves. Androecia very small, in whitish catkin-like spikes,
with 4–10 pairs of bracts. Gynoecia on short-ventral branches in
upper portion of stem, whitish to violet, bracts and bracteoles in
4 series, ± free, inner bracts 1.2 × 0.6 mm, unequally bifid to 1/3,
apex of longest lobe obtuse, of shortest lobe broadly rounded,
margins entire or with 1–2 remote laciniate teeth, surface of
bracts low substriate-papillose by large papillae, margins with
a white border of thicker-walled cells; inner bracteole as long as
bracts, very shortly bifid and with rounded lobes, margins entire
or with a short, laciniate tooth. Perianth large, cylindrical, 5 mm
long, uniformly deep violet in color, cells smooth, mouth crenate.
Sporophyte not observed.
Etymology. – The new species is dedicated to Professor
Antoine M. Cleef, world specialist on the flora and vegetation of
the páramo, who made numerous collections of the new species.
Distribution and ecology. – Only known from the high
Andes of Colombia where it is common in páramo vegetation
of the eastern, central and western cordilleras, at elevations
between 2300 and 4000 m, growing on humid soil in grass
páramo, bamboo páramo and in Sphagnum bogs. In the eastern
cordillera the species was exclusively found above 3300 m, in
the central and western cordilleras also at lower elevation in
azonal páramo vegetation and on low summits (e.g., Chocó:
summit of Cerro del Torrá, 2770 m. Huila: páramo del Río la
Candelaria, 2300 m).
Further specimens. – COLOMBIA. Arauca: Sierra
Nevada del Cocuy, Quebrada El Playon, 3350 m, Cleef 9178
(U). Boyacá: Vado Hondo, páramo between Peña Arnical y
Alto de Mogetes, Cleef 9245, 9258, 9489 (U); páramo de la
Sarna entre Sogamoso and Vado Hondo, Cleef 9523a (U); Péna
de Arnical N de Vado Hondo, Cleef 9489 (U); páramo de la
Rusia, 3820 m, Cleef 7476 (U). Casanare: páramo de Pisba,
3500 m, Aguirre & al. 2905 (COL, U). Chocó: San José del
Palmar, Cerro del Torrá, ca. 2750 m, Silverstone-Sopkin & al.
1830 (U). Cundinamarca: páramo de Palacio, headwaters of
Río Negro, 3360 m, Cleef 3819 (U), ibid., 1.5 km S of Lagunas
de Buitrago, 3560 m, Cleef 4127 (COL, U); páramo Cruz Verde,
3325–3600 m, Cleef 2885, 3086, 3243, 3304 (COL, U), 3089,
3244, 3277 (U); páramo between Cogua and San Cayetano,
3660–3700 m, Cleef 6248, 6269 (COL, U), 6221, 6372, 6497 (U);
páramo de Chingaza, Santana & Aguirre 337, 358, 381, 382, 388
(COL); páramo de Sumapaz, 3500–4000 m, Cleef 1637a, 8403
(U). Huila: La Plata, headwaters of Río La Candelaria, 2300 m,
Aguirre & al. 6556 (COL, U), ibid., Van Zanten & al. 815, as
O. atropurpureum (Van Zanten & Gradstein, 1988) (U). Meta:
páramo de Sumapaz, 3600 m, Cleef 1197 (COL).
10. Odontoschisma denudatum (Nees) Dumort., Recueil
Observ. Jungerm.: 19. 1835 ≡ Jungermannia denudata Nees
in Martius, Fl. Crypt. Erlang.: XIV. 1817 – Holotype: GERMANY. Erlangen, Martius s.n., c. gemmis (STR! [coll.
Nees]; isotype (?): S No. B73168!).
Version of Record (identical to print version).
Aranda & al. • Phylogeny of Odontoschisma
TAXON 63 (5) • October 2014: 1008–1025
10a. Odontoschisma denudatum subsp. denudatum
= Odontoschisma subjulaceum Austin in Bull. Torrey Bot. Club
6: 303. 1879, syn. nov. – Lectotype (designated by So in
J. Hattori Bot. Lab. 95: 257. 2004): [U.S.A.] Hawaii, Maui,
on soil, 2600 m, Dec 1875, Baldwin 233, hb. Levier 1439 (G
No. 20698!; isolectotypes: FH!, NY!).
10b. Odontoschisma denudatum subsp. naviculare (Steph.)
Gradst., S.C.Aranda & Vanderp., comb. & stat. nov. ≡
Jamesoniella navicularis Steph., Sp. Hepat. 6: 101. 1917 ≡
Odontoschisma naviculare (Steph.) Grolle in Acta Bot.
Fenn. 125: 71. 1984 – Holotype: New Caledonia, Mt. Dogny,
1050 m, Jul 1909, Mme L. Le Rat 208 (G No. 13519 [barcode
G00128131]!; isotypes: L!, PC!).
10c. Odontoschisma denudatum subsp. sandvicense (Ångstr.)
Gradst., S.C.Aranda & Vanderp., comb. & stat. nov. ≡
Sphagnoecetis sandvicensis in Öfvers. Kongl. Vetensk.Akad. Förh. 29(4): 22. 1872 (“Sphagnaectis”) ≡ Odontoschisma sandvicense (Ångstr.) A.Evans in Trans. Connecticut Acad. Arts Sci. 8: 256. 1892 (“1891”) – Holotype:
[U.S.A.] Hawaii, Honolulu, Jun 1852, Andersson s.n. (S No.
B47419; isotypes: G No. 22402 [barcode G00265225]!, S
No. B47418!).
So (2004) designated B47419 in S as the lectotype of
O. sandvicense. However, since this is the only specimen from
the Ångström herbarium (its duplicate, S-B47418, is from the
Möller hb.), since Ångström holotypes are in S and since the
label is in Angström’s handwriting, it should be considered
the holotype.
Austin in Bull. Torrey Bot. Club 3: 13. 1872 – Holotype:
CANADA. Ontario, Lake Superior, 25 miles north of
Michepicoten and near Otter Head, Macoun s.n. (MANCH
No. 20340 n.v. [cf. Grolle, 1976]).
15. Odontoschisma portoricense (Hampe & Gottsche) Steph.
in Hedwigia 27: 269. 1888 ≡ Sphagnoecetis portoricensis
Hampe & Gottsche in Linnaea 25: 343. 1853 (“1852”) ≡
Anomoclada portoricensis (Hampe & Gottsche) Váňa,
in Bryologist 92: 344. 1989 – Holotype: Puerto Rico,
Schwanecke s.n. (BM!).
16. Odontoschisma pseudogrosseverrucosum Gradst., S.C.
Aranda & Vanderp., sp. nov. – Holotype: JAPAN. Honshu:
Hiroshima Province, Hiroshima-shi, Aki-ku, Ayno-cho,
Mt. Egesan, 35°19′10″ N, 132°32′22″ E, ca. 550–570 m, on
rock, 15 Apr 2012, T. Katagiri 3525, c. gyn. (PC barcode
PC0703247!; isotype: HIRO Nr. 1015793!). — For drawings
from the holotype, see Fig. 4.
Differs from O. grosseverrucosum by smaller plant size,
11. Odontoschisma elongatum (Lindb.) A.Evans in Rhodora 14:
13. 1912 ≡ O. denudatum f. elongatum Lindb. in Helsingfors Dagblad 45: 2. 1874 – Lectotype (designated by Grolle
in Trans. Brit. Bryol. Soc. 6: 263–64. 1971): SWEDEN.
Lappland, Lycksele, Ångström s.n., Hep. Eur. Exsicc. 440
(ed. Gottsche & Rabenhorst) as Sphagnoecetis communis
(H-SOL!; isolectotypes: G!, H!, JE!, S!, etc.).
12. Odontoschisma engelii Gradst. & Burghardt in Fieldiana, Bot., n.s., 47: 194. 2008 – Holotype: ECUADOR.
Loja, Cordillera Oriental, Parque Nacional Podocarpus,
Cajanuma, lower margin of páramo, 3150 m, on the vertical, slightly overhanging and partially shaded side of a
large, crystalline boulder in the páramo, at the junction of
the trail leading to the lakes and the “mirador”, forming
dense, low, brownish mats, 19 Sep 2006, Gradstein & al.
10178 (GOET!; isotype: QCA!).
13. Odontoschisma longiflorum (Taylor) Trevis. in Mem.
Reale Ist. Lombardo Sci., Ser. 3, Cl. Sci. Mat. 4: 419. 1877
≡ Sphagnoecetis longiflora Taylor in London J. Bot. 5: 281.
1846 – Holotype: JAMAICA. s. coll. (FH n.v.; isotypes: S
Nos. B47414! & B47415!).
14. Odontoschisma macounii (Austin) Underw. in Bull. Illinois
State Lab. Nat. Hist. 2: 92. 1884 ≡ Sphagnoecetis macounii
Fig. 4. Odontoschisma pseudogrosseverrucosum (from the holotype).
A, habit, dorsal view; B, leaf apex; C, habit, ventral view; D, mid-leaf
cells; E, stem cross section; F, underleaf; G, leaf; H, portion of shoot
showing dorsal leaf-free strip. — Scale bars: A, C, H = 500 µm; B, D
= 25 µm; E, F = 50 µm; G = 250 µm. — Drawn by A.-L. Ilkiu-Borges.
Version of Record (identical to print version).
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Aranda & al. • Phylogeny of Odontoschisma
TAXON 63 (5) • October 2014: 1008–1025
subquadrate dorsal epidermis cells with thick walls, concave,
unbordered leaves, and occasional presence of lateral branches
and gemmae.
Plants prostrate, green to dark green to brown, in flat mats,
small, well-developed leafy shoots 0.5–0.65(–0.8) mm wide,
1–1.5 cm long, little and irregularly branched, leafy branches
ventral-intercalary and occasionally lateral-intercalary (in
material from Russian Far East), ventral stolons frequent, stems
sometimes terminating in a long stolon or microphyllous shoot.
Stems ca. 0.15 mm in diameter, stem surface smooth, epidermis cells thick-walled (rarely thin-walled), small, quadrate to
subrectangular, 15–25 µm long × 12–20 µm wide. Leaves undivided, distinctly concave with margins upcurved, obliquely to
widely spreading, distant to imbricate, insertion line oblique
to substransverse, not extending to dorsal midline, dorsal leaffree strip 1–4 cells wide; leaves ovate, small, ca. 0.35 mm long
× 0.25 mm wide when well developed, often smaller, slightly
longer than wide, subsymmetrical with ventral margin slightly
more strongly curved than dorsal margin, apex broadly rounded
to asymmetrically emarginate, ventral base narrowed, dorsal base narrowed or not. Leaf cells small, 10–20 µm long in
mid-leaf, isodiametrical to somewhat elongate, slightly larger
to base, 20–25 µm, not smaller to margin; trigones small to
large, cell-lumen varying from quadrate to stellate, middle
lamella distinct or indistinct; leaf border absent; oil-bodies
rounded to elongate, finely granular-papillose, 2–4 per cell,
rather small, 4–9 × 4–6 µm; cuticle covered by large, rounded
to elongate papillae in lower half of leaf lamina (in large leaves)
or over whole leaf lamina (in small leaves), papillae 3–10(–15)
× 3–10 µm, 1–5(–8) per cell. Underleaves vestigial or rather
well-developed, lanceolate to subquadrate, to 0.15 × 0.1 mm,
apex undivided or shortly bifid, margins sometimes with a
tooth; slime papillae not seen. Gemmae present, scarce, pale
green, ovate, 2-celled, 20–25 × 13–16 µm, produced in dense
pale-green clusters on upright, swollen shoots apices or at
tips of short microphyllous branches, gemmiparous leaves
densely imbricate and appressed, underleaves on gemmiparous shoots much smaller than leaves. Dioicous. Androecia not
seen. Gynoecia whitish, on short-specialized ventral branches,
bracts and bracteoles in 3 series, made up of smooth cells; inner
bracts ovate, concave, shallowly and unequally bifid, apices
acute, margins entire to irregularly crenate; inner bracteole as
long as bracts, apex rounded or shortly bifid. Perianths rare,
cylindrical, bluntly trigonous. Sporophytes not seen.
Distribution and ecology. – Temperate and subtropical
East Asia: Eastern Russia, Korea and Japan (Honshu, Kyushu,
southwards to Yakushima Island), ca. 100–1650 m. On moist
limestone rock and cliffs, also on decaying wood, in evergreen
forest.
Further specimens (all originally annotated as “Odonto­
schisma grosseverrucosum”). – RUSSIA. Far East: Khasansky Distr., Kedrovaya Pad’ State Reserve, Bakalin P-3-26-7
(PC, VLA). SOUTH KOREA. Kyong Nam: Chiri Mt., Bakalin
Kor-12-3b-09, Kor-12-10b-9 (PC, VLA). JAPAN. Honshu:
Segari, Kobe-shi, Hyogo-ken, Kodama s.n., Hep. Japon. Exsicc.
1036 (ed. S. Hattori & M. Mizutani) (GOET, L, PC); Naganoken, Shiokawa valley, Katagiri 889 (HIRO); Hatsukaichi-shi,
1020
Miyajima I., Y. Inoue 174 (HIRO, PC). Kyushu: Miyazaki,
Faurie 1296 (G, syntype of O. grosseverrucosum); Kumamoto, Hitoyohi, Mayebara s.n., Hep. Japon. Exsicc. 108 (ed.
S. Hattori) (BM, GOET, PC, S, U); Yakushima, ca. 1500 m,
Takaki & Mizutani s.n., Hep. Japon. Exsicc. 793 (ed. S. Hattori)
(PC, U).
*17. Odontoschisma purpuratum Herzog in Trans. Brit. Bryol.
Soc. 1(4): 297. 1950 – Holotype: MALAYSIA. Sarawak,
ridge of Mt. Dulit, on tree trunk near ground, in mossy forest on exposed peak, ca. 1400 m, 5 Oct 1932, P.W. Richards
2162, c. andr. (JE!; isotypes: BM!, L!).
*18. Odontoschisma soratamum Fulford in Mem. New York
Bot. Gard. 11: 338. 1968 – Holotype: COLOMBIA. Amazonas-Vaupes, Rio Apoporis, Soratama, 250 m, Schultes
& Cabrera 12883 (FH!).
19. Odontoschisma variabile (Lindenb. & Gottsche) Trevis.
in Mem. Reale Ist. Lombardo Sci., Ser. 3, Cl. Sci. Mat. 4:
419. 1877 ≡ Sphagnoecetis variabilis Lindenb. & Gottsche
in Gottsche & al., Syn. Hepat.: 688. 1847 – Holotype:
MEXICO. Oaxaca, Tepinapa, “ad terram”, Liebmann 315a
(W n.v.; isotypes: C!, S Nos. B47422! & B47423!).
20. Odontoschisma zhui Gradst., S.C.Aranda & Vanderp., sp.
nov. – Holotype: CHINA. Zhejiang Prov., Longquan City,
Fengyangshan Nature Reserve, Yangtiancao, ca. 1500 m,
on moist sandstone rock in evergreen forest in deep river
valley, in shade, 3 Dec 2012, S.R. Gradstein & R.-L. Zhu
12384 (PC barcode PC0703248!; isotype: HSNU!). — For
drawings from the holotype, see Fig. 5.
Characterized by leaves tending to become curved-subfalcate, small leaf cells (13–22 µm long in mid-leaf), and a smooth
cuticle. Moreover, branching is predominantly ventral-intercalary and the leaves and underleaves of specialized gemiparous
shoots are appressed.
Plants prostrate, light green to dark green to reddish-brown
or purplish, forming loose to dense mats, leafy shoots 1–1.3 mm
wide, leafy branches usually ventral-intercalary, rarely ventrolateral-intercalary, ventral stolons simple or branched, present
near base of stem, occasionally higher up stem, leafy shoot
sometimes terminating in a long stolon. Stems ca. 0.15–0.16 mm
in diameter, rigid, epidermis composed of small, quadrate to
rectangular, thick-walled cells, dorsal epidermis cells in almost
straight rows. Leaves concave with margins ± upcurved (especially dorsal margin), obliquely to widely spreading, becoming
curved-subfalcate, subimbricate, insertion line usually reaching dorsal midline, dorsal leaf-free strip 0(–1) cell wide; leaves
shortly ovate, ± asymmetrical, 0.5–0.8 × 0.5–0.6.5 mm, as wide
as long or longer than wide (1–1.3 : 1), apex rounded, dorsal margin almost straight to curved and slightly narrowed at base, dorsal base not or very slightly decurrent, ventral margin broadly
arched and narrowed at base, margins entire or slightly crenulate
by projecting margin cells. Leaf cells small, isodiametrical to
elongate, in mid-leaf 13–18(–22) µm long and 11–18 µm wide, cells
slightly smaller towards leaf margin and slightly larger towards
Version of Record (identical to print version).
Aranda & al. • Phylogeny of Odontoschisma
TAXON 63 (5) • October 2014: 1008–1025
leaf base; trigones small to large and swollen, contiguous, celllumen rounded to stellate, middle lamella indistinct; leaf border
lacking; oil-bodies not seen; cuticle smooth or slightly verruculose. Underleaves lacking (except on gemmiparous shoots and
in gametoecia). Gemmae present, whitish-green, 1–2-celled,
rounded to ellipsoid, thick-walled, walls ca. 2–8 µm thick, produced on tips of upright, flagelliform shoots with appressed to
obliquely spreading leaves and underleaves, underleaves becoming progressively larger towards apex of gemmiparous shoot.
Dioicous. Androecia very small, in short, whitish, catkin-like
spikes near stem base, with 4–5 pairs of bracts. Gynoecia on
short ventral branches near stem base, whitish-green, bracts
and bracteoles in 2 series, inner bracts unequally bifid, apex of
lobes acute, margins entire or remotely crenate, surface of bracts
finely striate-papillose; inner bracteole about as long as bracts,
bifid and with acute lobes. Perianth cylindrical, ± 3 mm long,
whitish above, green below, deeply plicate, cells smooth, mouth
contracted, crenate. Sporophyte not seen.
Etymology. – The new species is dedicated to Professor RuiLiang Zhu, specialist of Lejeuneaceae and liverworts of China.
Distribution and ecology. – Subtropical East Asia (central
and southeastern China, southern Japan), from near sea level
to about 1600 m. On sandstone rock and rotten wood in deep
river valleys, in subtropical evergreen forest.
Further specimens. – CHINA. Guanxsi: Maoershan
Nature Reserve, Longtrangjiang, 480 m, Zhu & al. 2004090847 as O. grosseverrucosum (HSNU). Huan: Yizhang Co., Mt.
Mangshan, Koponen & al. 50768 as O. denudatum (GOET,
H), 51488, 55589 as O. denudatum (H, S); Yanling Co., Taoyuandong, Koponen & al. 55308 as O. grosseverrucosum (H,
TNS), Zhejiang: Fengyangshan Nature Reserve, Zhu & Wei
20110418-37 as O. denudatum (HSNU), Gradstein & Zhu 12385,
12386 (c. andr.), 12387 (c. gyn.) (HSNU, PC). JAPAN. Honshu:
Nigata Pref., Sado I., Homma 4580 as O. grosseverrucosum (NICH); Toyama Pref., Kurobe valley, Mizutani s.n. as
O. grosse­verrucosum (NICH); Fukui Pref., Mt. Fujikura,
Mizutani 4373 as O. grosseverrucosum (NICH); Shiga Pref.,
Kanzaki-gun, Echigawa valley, Kodama 27161 as O. grosse­
verrucosum (NICH). Shikoku: Kochi Pref., Kitagawa-mura,
Hashimoto & al. 1603002 as O. grosseverrucosum (NICH),
ibid., Tai-mura, H. Inoue 643 as O. denudatum (TNS). Kyushu:
Yakushima I., Hattori 6972, 7677 as O. grosseverrucosum
forma (NICH).
ACKNOWLEDGEMENTS
The authors thank three anonymous referees for their constructive comments on the manuscript. Thanks are also due to the curators
of the herbaria cited in the text for the loan of specimens. We furthermore express our warmest gratitude to Anna Luiza Ilkiu-Borges for
preparing the drawings of the three new species of Odontoschisma
and to the following colleagues who kindly sent us samples for the
molecular study: V.A. Bakalin (Russia), L.V. Campos (Colombia),
P.G. Davidson (U.S.A.), K. Georgson (Sweden), T. Hallingbäck (Sweden), T. Katagiri (Japan), J. Larrain (Chicago), E. Lavocat-Bernard
(Guadeloupe), H. van Melick (The Netherlands), D. Pinheiro da Costa
(RB), B. Shaw (U.S.A.), T. Tyler (Sweden), Yong K.T. (Malaysia) and
R.-L. Zhu (China). The second author (SRG) is very grateful to L. Ellis
(BM), L. Hedenäs and I. Bisang (S), M. Hoff (STR), S. Léon-Yánez
(QCA), M. Price (G), M. Stech (L) and J. Uribe (COL) for making facilities available and help during his visits to these herbaria, to T. Katagiri
and R.-L. Zhu for help with literature, and to R.-L. Zhu for hosting
his visit to China. Work of SRG in the Stockholm herbarium and of
SCA, BL and AD at Leiden University was supported by Synthesys
grants. SCA was supported by a Spanish JAEPre grant from CSIC. AV
acknowledges financial support from the Fonds Léopold III.
Fig. 5. Odontoschisma zhui (A, D–F, I, J, L from the holotype; B, C,
G, H, K, M from Gradstein & Zhu 12387). A, habit, ventral view;
B, habit, dorsal view; C, ibid., with gynoecia; D–E, underleaves; F–G,
stem cross sections; H–I, leaf margin; J, leaf; K–L, mid-leaf cells; M,
gemmiparous shoot, dorsal view. — Scale bars: A, B, M = 500 µm;
C, J = 250 µm; D–G = 50 µm; H, I, K, L = 25 µm. — Drawn by A.-L.
Ilkiu-Borges.
LITERATURE CITED
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Appendix 1. Voucher information and GenBank accession numbers for the specimens of Odontoschisma and outgroup taxa used in this study. Sequences in
bold where obtained from GenBank.
Taxon, origin, voucher (herbarium), Lab. ID, atpB-rbcL, trnL-F, rps4
O. bifidum (Fulford) Gradst., S.C.Aranda & Vanderp. (= Iwatsukia bifida), Venezuela, Halling 5568 (NY), IWA, KJ620667, KJ620713, –; O. brasiliense Steph.,
Brasil, Rio de Janeiro, Santos & Costa 568 (RB), OBRA, KJ620655, KJ620692, KJ620747; O. cleefii Gradst., S.C.Aranda & Vanderp., Colombia, Campos 717
(COL, PC), O9, KJ620649, KJ620698, KJ620746; O. denudatum (Nees) Dumort., Azores, Terceira, Vanderpoorten TER4 (LG), OD8, KJ620644, KJ620682,
KJ620738; O. denudatum (Nees) Dumort., Sweden, Georgson s.n. (PC), OD12, KJ620646, KJ620680, KJ620737; O. denudatum (Nees) Dumort., France,
Gradstein s.n. (PC), OD13, KJ620643, KJ620681, KJ620735; O. denudatum (Nees) Dumort., The Netherlands, Van Melick 214610 (PC), OD15, KJ620645,
KJ620683, KJ620736; O. denudatum (Nees) Dumort., Japan, Hiroshima, Miyauchi 1331 (HIRO, PC), OD17, KJ620647, KJ620693, KJ620750; O. denudatum
(= O. subjulaceum Austin), Hawaii, Frahm 472 (hb. Frahm), OD18, KJ620642, KJ620696, KJ620733; O. denudatum subsp. naviculare (Steph.) Gradst.,
S.C.Aranda & Vanderp. (= O. naviculare), New Caledonia, Larrain s.n. (hb. Larrain, LG), ON3, KJ620648, KJ620695, KJ620739; O. denudatum subsp. sandvicense (Ångstr.) Gradst., S.C.Aranda & Vanderp. (= O. sandvicense), Hawaii, Patino s.n. (LG), O11, KJ620668, KJ620697, KJ620734; O. elongatum (Lindb.)
A.Evans, Sweden, Hallingbäck 4259 (hb. Hallingbäck), OE2, KJ620663, KJ620702, KJ620728; O. elongatum (Lindb.) A.Evans, Sweden, Hallingbäck 44271 (hb.
Hallingbäck), OE1, KJ620664, KJ620701, KJ620729; O. elongatum (Lindb.) A.Evans, U.S.A., Alaska, B. Shaw 7389 (DUKE), OSP10, KJ620665, KJ620711,
KJ620730; O. engelii Gradst. & Burghardt, Ecuador, Burghardt 6990 (PC, QCA), OEN1, KJ620659, KJ620686, KJ620755; O. fluitans (Nees) L.Söderstr. &
Váňa (= Cladopodiella fluitans), Belgium, Vanderpoorten K626-6 (LG), CFLU, KJ620666, KJ620712, KJ620754; O. francisci (Hook.) L.Söderstr. & Váňa
(= Cladopodiella francisci), Belgium, Sotiaux 37952 (hb. Sotiaux), CFRA, KJ620641, KJ620710, KJ620753; O. grosseverrucosum Steph., China, Zenjiang,
Gradstein 12388 (PC), OG3, KJ620634, KJ620676, KJ620723; O. jishibae (Steph.) L.Söderstr. & Váňa, EU791722, –; O. longiflorum (Taylor) Trevis., Ecuador,
Gradstein 12112 (PC), O3, KJ620654, KJ620684, KJ620740; O. cf. longiflorum (Taylor) Trevis., Ecuador, 1990 m, Burghardt 7076 (PC), OV2, KJ620656,
KJ620685, KJ620741; O. macounii (Austin) Underw., Iceland, Vanderpoorten 4470 (LG), OD7, KJ620635, KJ620704, KJ620724; O. macounii (Austin)
Underw., Sweden, Hallingbäck 2031 (hb. Hallingbäck, PC), OM2, KJ620638, KJ620705, KJ620726; O. macounii (Austin) Underw., Russian Far East, Bakalin
Mag-12-11-10 (VLA), OM1, KJ620636, KJ620706, KJ620725; O. macounii (Austin) Underw., Russian Far East, Bakalin S-32-28a-06 (VLA), OM3, KJ620637,
KJ620707, KJ620727; O. portoricense (Hampe & Gottsche) Steph. (= Anomoclada portoricensis), Suriname, Allen 20342 (MO), O8, KJ620657, KJ620690,
KJ620749; O. portoricense (Hampe & Gottsche) Steph. (= Anomoclada portoricensis), Suriname, Allen 20379 (MO), OPOR, KJ620658, KJ620691, KJ620748;
O. prostratum (Sw.) Trevis., U.S.A., North Carolina, B. Shaw 12994 (DUKE, PC), O4, KJ620631, KJ620669, KJ620722; O. prostratum (Sw.) Trevis., U.S.A.,
North Carolina, Vanderpoorten s.n. (LG), O6, KJ620628, KJ620671, KJ620714; O. prostratum (Sw.) Trevis., U.S.A., Alabama, Davidson 8150 (PC), OPR2,
KJ620629, KJ620673, KJ620716; O. prostratum (Sw.) Trevis., U.S.A., North Carolina, B. Shaw 12993 (DUKE, PC), OPR1, KJ620630, KJ620672, KJ620721;
O. prostratum (Sw.) Trevis., U.S.A., Connecticut, B. Shaw 7184 (DUKE), OPR11, KJ620633, KJ620677, KJ620718; O. pseudogrosseverrucosum Gradst.,
S.C.Aranda & Vanderp., Japan, Katagari 3525 (HIRO, PC), O7, KJ620639, KJ620708, KJ620751; O. pseudogrosseverrucosum Gradst., S.C.Aranda & Vanderp., Japan, Y. Inoue 174 (HIRO, PC), OG2, KJ620640, KJ620709, KJ620752; O. sphagni (Dicks.) Dumort., Azores, S. Jorge, Vanderpoorten & Patino (LG),
OD6, KJ620626, KJ620670, KJ620719; O. sphagni (Dicks.) Dumort., Azores, Terceira, Frahm Az-110 (hb. Frahm), OSP1, KJ620627, KJ620675, KJ620715; O.
sphagni (Dicks.) Dumort., Azores, Pico, Vanderpoorten & Patino OD1 (LG), OD1, KJ620632, KJ620679, KJ620717; O. sphagni (Dicks.) Dumort.,
Belgium, Gradstein 12380 (PC), OSP4, KJ620624, KJ620674, KJ620720; O. sphagni (Dicks.) Dumort., U.K., Scotland, Long 37024 (E), OSP14,
KJ620625, KJ620678, KJ620756; O. variabile (Lindenb. & Gottsche) Trevis., Colombia, Campos 718 (COL, PC), DPAR, KJ620650, KJ620694,
KJ620742; O. variabile (Lindenb. & Gottsche) Trevis., Ecuador, 3035 m, Schäfer-Verwimp 31776 (hb. Schäfer-Verwimp), OV3, KJ620651, KJ620689,
KJ620744; O. variabile (Lindenb. & Gottsche) Trevis., Ecuador, 2250 m, Burghardt 7047 (PC), OV4, KJ620652, KJ620687, KJ620743; O. variabile
(Lindenb. & Gottsche) Trevis., Ecuador, 2400 m, Schäfer-Verwimp 31991 (hb. Schäfer-Verwimp), OV5, KJ620653, KJ620688, KJ620745; O. zhui
Gradst., S.C.Aranda & Vanderp., China, Zenjiang, Gradstein 12385 (PC), DENA1, KJ620660, KJ620700, KJ620731; O. zhui Gradst., S.C.Aranda
& Vanderp., China, Zenjiang, Gradstein 12384 (PC), DENA2, KJ620661, KJ620699, –; O. zhui Gradst., S.C.Aranda & Vanderp., China, Hunan,
Koponen 50933 (H), ON2, KJ620662, KJ620703, KJ620732; Alobiellopsis parvifolia (Steph.) R.M.Schust., JX630020, –; Cephalozia bicuspidata
(L.) Dumort., JX630025, JX308561; Fuscocephaloziopsis lunulifolia (Dumort.) Váňa & L.Söderstr., JX629958, AM398315; Hygrobiella laxifolia
(Hook.) Spruce, JX630054, –; Nowellia curvifolia (Dicks.) Mitt., JX629997, AY608094; Pleurocladula albescens (Hook.) Grolle, JX629992, –;
Schiffneria hyalina Steph., AY463585, JF513488; Schofieldia monticola J.D.Godfrey, JX629988, –
1024
Version of Record (identical to print version).
Aranda & al. • Phylogeny of Odontoschisma
TAXON 63 (5) • October 2014: 1008–1025
Appendix 2. Matrix of 20 morphological characters in Odontoschisma s.l. (including Anomoclada, Cladopodiella and Iwatsukia). Missing characters are scored as “ ? ”. Characters based on morphological study of the vouchers (Appendix 1) and additional herbarium material, as well as on
literature (Fulford, 1968; Schuster, 1968, 1974; Konstantinova, 2004; So, 2004).
Characters
O. bifidum IWA
O. brasiliense OBRA
O. cleefii O9
O. denudatum OD8
O. denudatum OD12
O. denudatum OD13
O. denudatum OD15
O. denudatum OD17
O. denudatum OD18
O. denudatum subsp. naviculare ON3
O. denudatum subsp. sandvicense O11
O. elongatum OE1
O. elongatum OE2
O. elongatum OSP10
O. engelii OEN1
O. fluitans CFLU
O. francisci CFRA
O. grosseverrucosum OG3
O. jishibae JIS
O. longiflorum O3
O. cf. longiflorum OV2
O. macounii OD7
O. macounii OM2
O. macounii OM1
O. macounii OM3
O. portoricense O8
O. portoricense OPOR
O. prostratum O4
O. prostratum OPR11
O. prostratum O6
O. prostratum OPR1
O. prostratum OPR2
O. pseudogrosseverrucosum O7
O. pseudogrosseverrucosum OG2
O. sphagni OD6
O. sphagni OSP1
O. sphagni OD1
O. sphagni OSP4
O. sphagni OSP14
O. variabile DPAR
O. variabile OV3
O. variabile OV4
O. variabile OV5
O. zhuii DENA1
O. zhuii DENA2
O. zhuii ON2
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
0
2
1
1
1
1
1
1
1
1
1,2
1
1
1
0
1
0
1
0
1
1
1
1
1
1
2
2
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
2
0
0
0
0
0
0
0
0
0
0
1
1
1
0
0
0
2
2
2
0
2
2
2
2
0
0
0
0
0
0
0
1
1
0
0
0
0
0
0
0
0
0
0
0
0
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
1
1
0
0
0
0
0
0
0
0
1
1
1
1
1
0
0
1
1
1
1
1
0
0
0
0
0,1
0,1
0,1
1
1
1
0
0
0
0
0
0
1
1
1
1
1
1
1
1
1
1
0
1
1
1
1
1
0
0
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1,2
2
0
0
0
0
0
0
0
1
1
0
0
0
0
0
0
1,2
1
2
1
0
0
0
0
0
0
2
2
2
2
2
1,2
1,2
2
2
2
2
2
1
1
1
1
0
0
0
2
0
2
2
2
2
2
2
2
2
0
2
2
2
2
0
2
1
2
0
1
2
2
2
2
0
0
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
2
2
2
2
0
0
0
0
0
0
0
0
0
0
0
0
0
0
2
1
0
3
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
2
0
0
0
0
0
0
0
0
0,1
0
0
0
0
2
1
0
0
0,1
0,1
0,1
0
0
0
0
2
2
0,1
0,1
0,1
0,1
0,1
0
0
0,1
0,1
0,1
0,1
0,1
0,1
0,1
0,1
0,1
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
1
1
2
1
1
1
1
1
1
1
2
2
1
1
1
1
2
1
0
1
2
1
2
2
2
2
2
2
1
1
1
1
1
0
0
1
1
1
1
1
1
1
1
1
0
0
0
3
0
1
1
1
1
1
1
1
1
1
1
1
1
1
3
3
0
3
0
1
2
2
2
2
1
1
0
0
0
0
0
0
0
0
0
0
0
0
1
1
1
1
1
1
1
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
1
0
0
0
0
0
0
0
1
1
1
1
1
0
0
1
1
1
1
1
0
0
0
0
0
0
0
0
1
0,1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
2
2
2
0
0
0
0
1
0
0
1
1
1
1
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
2
1
1
1
1
1
1
1
1
0
0
0
0
0
0,1
2
1
1
1
0
0
0
0
1
1
1
1
1
1
1
2
2
1
1
1
1
1
1
1
1
1
0,1
0,1
0,1
2
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
0
2
0
0
1
1
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
2
2
0
1
1
1
1
1
1
0
0
1
1
1
0
2
0
2
2
1
1
0
0
0
0
0
0
2
2
2
2
2
0
0
2
2
2
2
2
1
1
1
1
0
0
0
1
?
0
1
1
1
1
1
1
?
1
1
1
1
1
0,1
0,1
?
1
1
1
1
1
1
1
1
1
2
2
2
2
2
?
?
2
2
2
2
2
1
1
1
1
1
1
1
?
?
?
1
1
1
1
1
1
?
?
1
1
1
?
0
0
?
0
?
1
1
1
1
1
?
?
1
1
1
1
1
?
?
1
1
1
1
1
1
1
1
1
?
?
?
1. Plant width: less than 1 mm wide (0), 1–2 mm wide (1), 2–4 mm wide (2); 2. Pigmentation: plants with reddish or purplish pigmentation (0),
pigmented but never with reddish or purplish (1), not pigmented (2); 3. Lateral branches: present (0) or absent (1); 4. Anomoclada-type branches:
present (0) or absent (1); 5. Leaf-free strip: 0–1 cell wide (0), 1–2(–3) cells wide (1), 3–8 cells wide (2); 6. Leaf lamina: surface and margins
flat (0), surface flat to slightly concave, dorsal margin upcurved (1), surface always concave, margins upcurved (2); 7. Leaf apex: undivided (0)
or bifid to 1/5 (1), 1/3 (2) or 1/2 (3); 8. Leaf elongation: leaf about as wide as long (0), elongate, up to 1.5 : 1 (1), strongly elongate, 1.5–2.5 : 1
(2); 9. Leaves: straight (0), curved-falcate (1); 10. Mid-leaf cell size: 9–16(–20) µm (0), 16–25(–30) µm (1), 25–40 µm (2); 11. Trigones: small
to medium-sized (0), medium-sized to large (1), very large (2), indistinct, walls evenly thickened (3); 12. Leaf border: lacking (0), present (1);
13. Outer wall of leaf margin: thickened to ca. 5 µm (0), very strongly thickened, to 12 µm (1); 14. Middle lamella of leaf cells: indistinct (0),
distinct, colorless (1), distinct, brown (2); 15. Transverse walls of leaf cells ornamented by numerous verruculae (sometimes interpreted as plasmodesmata): absent (0), present (1); 16. Cuticle: completely smooth (0), finely verruculose (1), coarsely verrucose (2); 17. Underleaves: absent or
rudimentary (0), present but small (1) well developed, to 1/2× leaf length (1); 18. Gemmiparous leaves appressed (0), appressed to squarrose (1),
lacking (2); 19. Female bract apices rounded to obtuse (0), obtuse to acute to short acuminate (1), long acuminate to ciliate (2); 20. Capsule epidermis: with nodular thickenings on all long walls (0), on alternate long walls (1).
Version of Record (identical to print version).
1025