Fungal Diversity (2017) 84:101–117

DOI 10.1007/s13225-017-0379-z

Using a temporal phylogenetic method to harmonize family-

and genus-level classification in the largest clade of lichen-forming
fungi
Pradeep K. Divakar1 • Ana Crespo1 • Ekaphan Kraichak2 • Steven D. Leavitt3 •

Garima Singh4 • Imke Schmitt4 • H. Thorsten Lumbsch5

Received: 14 January 2017 / Accepted: 7 April 2017 / Published online: 11 April 2017
Ó School of Science 2017

Abstract Although classification at supra-specific ranks is
inherently arbitrary, comparable taxonomic ranks within
clades can facilitate more consistent classifications and
objective comparisons among taxa. Different circumscrip-
tions of the hyper-diverse lichen-forming fungal family
Parmeliaceae and widely different generic circumscriptions
among authors have been proposed. For this study, we use
a recently developed temporal approach that uses time-
calibrated chronograms to identify temporal bands for
specific ranks in Parmeliaceae and allied groups with the
overarching goal of establishing a consistent, stable classi-
fication. A data set of 330 species, representing 73 genera
in the family and 52 species of related families was used to
address the circumscription of Parmeliaceae and its genera
following the proposed temporal approach. Based on the
results of this study, we propose a revised, temporal-based
Electronic supplementary material The online version of this
article (doi:10.1007/s13225-017-0379-z) contains supplementary
material, which is available to authorized users.
& Ekaphan Kraichak
ekaphan.k@ku.th
1
Departamento de Biologı́a Vegetal II, Facultad de Farmacia,
Universidad Complutense de Madrid, 28040 Madrid, Spain
2
Department of Botany, Faculty of Science, Kasetsart
University, Bangkok, Thailand
3
Department of Biology and M.L. Bean Life Science Museum,
Brigham Young University, 4102 Life Science Building,
Provo, UT 84602, USA
4 Classification of organisms predates evolutionary thinking.
Department of Biological Sciences, Institute of Ecology,
Evolution and Diversity, Goethe Universität and Senckenberg
Biodiversity and Climate Research Centre (BiK-F),
Frankfurt am Main, Germany
5
Science & Education, The Field Museum, Chicago, IL, USA
classification for Parmeliaceae, including all clades that
share a common ancestor 102.13–112.88 Ma for families
and a time window of 29.45–32.55 Ma for genera. Forty-
five of the currently accepted genera in Parmeliaceae were
supported in their current circumscription. Two subfamilies
are accepted within Parmeliaceae: Protoparmelioideae
Divakar et al. subfam. nov., including Protoparmelia and
the resurrected genus Maronina, and Parmelioideae,
including the bulk of genera in the family. The new genus
Austromelanelixia Divakar et al. is proposed to accom-
modate a clade of southern Hemisphere species previously
included in Melanelixia. Eumitria and tentatively Dolic-
housnea are resurrected as genera separate from Usnea.
The following genera are reduced to synonymy: Alloce-
traria, Cetrariella, Usnocetraria, and Vulpicida with Ce-
traria; Arctocetraria, Cetreliopsis, Flavocetraria,
Kaernefeltia, Masonhalea, Tuckermanella, and Tucker-
mannopsis with Nephromopsis; and the lichenicolous
genera Nesolechia and Raesaenenia with the lichen-form-
ing genera Punctelia and Protousnea, respectively. A total
of 47 new combinations and three new names at the species
level are proposed.
Keywords Ascomycota
Gypsoplacaceae
Lecanorales

Lichenized fungi
Parmeliaceae
Phylogeny

Protoparmelia
Taxonomy
Taxonomic ranks
Introduction
Linnaeus, who systematically used a ranked classification
(Linnaeus 1767), understood a ‘‘natural system’’ as
reflecting a divine plan and not evolutionary relationships.
Today it is generally accepted that organisms continuously

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evolve and that species are the fundamental unit for evo-
lution. Selection, genetic drift, and gene flow have a
cohesive effect keeping populations together as species
(Coyne and Orr 2004). In contrast, all taxonomic ranks
above species are usually seen as arbitrary (for a deviating
view, see Humphreys and Barraclough (2014); Barra-
clough and Humphreys (2015)). Despite their arbitrariness,
ranks play an important role in the classification of
organisms since they allow a hierarchical approach for
encompassing the vast biological diversity on earth (Liu
et al. 2017). In a phylogenetic context, taxonomic ranks
represent clades with a shared evolutionary history.
Members of a clade often share phenotypic traits since they
are derived from a common ancestor. Comparisons of
floras or faunas often use higher ranks, such as genera,
families or orders, to compare biodiversity in ecological
and conservational studies. However, it has long been
known that ranks in different organismal groups are vastly
different and hence comparisons at supra-specific level are
potentially flawed (Hennig 1966; Simpson 1990; Johns and
Avise 1998; Avise and Johns 1999; Lumbsch 2002; Avise
and Mitchell 2007; Avise and Liu 2011; Holt and Jønsson
2014; Samarakoon et al. 2016).
There have been two major proposals to address the
issue of comparing ‘‘apples versus oranges’’ (Avise and Liu
2011) in biological classification. Proponents of the Phy-
loCode argue for a rankless classification that abandons the
use of any ranks (De Queiroz 2006; Zachos 2011). In
contrast, others have suggested unifying taxonomic ranks
across organismal groups based on objective criteria (Avise
and Johns 1999; Avise and Liu 2011; Holt and Jønsson
2014; Humphreys and Barraclough 2014). For the latter
approach, either differences in branch lengths among
clades (Humphreys and Barraclough 2014; Humphreys
et al. 2016) or time of divergence (Hennig 1966; Avise and
Johns 1999; Avise and Liu 2011; Holt and Jønsson 2014;
Zhao et al. 2016) were proposed as criteria to identify
comparable taxonomic ranks of clades. The use of branch
lengths among clades requires dense sampling to identify
shifts of diversification with statistical support. This is
difficult to achieve, especially in hyper-diverse and poorly
known groups, such as fungi. However, temporal approa-
ches, which base the identification of ranks on the age of
clades, constitute a promising avenue to harmonize the use
of ranks in fungal classification.
Recently, we have developed a method that uses time-
calibrated chronograms derived from multi-gene phyloge-
nies to identify upper and lower thresholds for taxonomic
ranks (Kraichak et al. 2017). This method is based on the
temporal banding approach proposed by Avise and Johns
(1999), which stems from Hennig’s (1966) idea to accept
taxonomic ranks for clades originating at similar time
period. Temporal banding harmonizes the use of taxonomic
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Fungal Diversity (2017) 84:101–117
ranks by identifying thresholds at specified points in time
using dated phylogenies. Our method incorporates the
temporal error score (Holt and Jønsson 2014) to find the
time with the minimal difference to the current classifica-
tion and uses it as a temporal threshold for the new clas-
sification. Here we employ this new method in Ascomycota
to address the circumscription of the family Parmeliaceae
and the generic classification within the family.
Parmeliaceae is the most diverse family of lichenized
fungi with almost 2800 currently accepted species (Jakl-
itsch et al. 2016). The family originated during the Creta-
ceous with diversification of major clades during the
Paleogene and a major increase in diversification during
the Miocene, leading to the current hyper-diversity of the
clade (Amo de Paz et al. 2011; Kraichak et al. 2015).
Parmeliaceae has a worldwide distribution, with the highest
diversity in the tropics, but occurring across a broad range
of habitats, from rainforests to deserts to Polar regions.
Species occur on all kind of substrates, including tree bark,
wood, rocks, and soil. Species in the family have been
widely used as biomonitors for air pollution and ecological
health (Hawksworth and Rose 1970, 1976).
Parmeliaceae is an ideal object to study the use of the
temporal banding approach for classification in lichenized
fungi, since both circumscription of the family and the
delimitation of genera within its major clades has been
controversially discussed over the last decades (Hale 1984;
Elix 1993; Mattsson and Wedin 1999; Wedin et al. 1999;
Arup et al. 2007; Crespo et al. 2007, 2010, 2011; Thell
et al. 2012; Singh et al. 2013). The disparities in the cir-
cumscriptions of the family and its genera were due to
different interpretations of the importance of phenotypical
characters in this morphologically and chemically unusu-
ally diverse group of lichenized fungi. Parmeliaceae
includes species with different morphologies, including
crustose, foliose, and fruticose species (and variants
thereof, such as umbilicate), and also lichenicolous fungi
have been shown to belong here (Persoh and Rambold
2002). Variations in secondary chemistry have also widely
been used to circumscribe groups within the family (Elix
1993; Kärnefelt and Thell 1993).
Active phylogenetic research on the family over the last
decades from several research groups has cumulatively
resulted in sufficient DNA sequence data to allow
addressing classification of the clade in a phylogenetic
framework. We use a robust molecular data set and phy-
logenetic reconstructions to address the following research
questions: (1) How disruptive would a classification based
on temporal banding be, e.g., how different is it from the
one in current use?; (2) Can Parmeliaceae be delimited
based on a temporal approach?; and (3) Which genera need
to be re-circumscribed in order to make genera within
Parmeliaceae of comparable age?
Fungal Diversity (2017) 84:101–117
Materials and methods
Data set
Our present study uses a compilation of data sets from two
recently published studies focusing on Parmeliaceae and
other closely related lineages (Divakar et al. 2015; Singh
et al. 2015), and in addition includes 128 newly generated
sequences. Representatives from the families Parmeli-
aceae, Gypsoplacaceae, Cladoniaceae, Lecanoraceae s. lat.,
Mycoblastaceae, Ramboldiaceae, and Stereocaulaceae
were included (Online Resource 1). Species of the family
Mycoblastaceae were used as outgroup based on previous
studies (Crespo et al. 2007; Miadlikowska et al. 2014). The
sampling of Parmeliaceae included 330 species represent-
ing 73 genera in this family (Thell et al. 2012). Most of the
data set represents a compilation of sequences from pre-
vious studies (Divakar et al. 2015; Singh et al. 2015),
where primer sequences and annealing conditions were
reported together with gene amplification and DNA
sequencing conditions; and these were the same—as pre-
viously reported—for newly generated sequences. Overall,
six loci were selected, three ribosomal markers, including
two nuclear loci, the ITS and the nuclear ribosomal large
subunit (nuLSU) and the mitochondrial SSU (mtSSU); and
three protein-coding loci, the largest subunit of RNA
polymerase II (RPB1), the DNA replication licensing factor
mini-chromosome maintenance complex component 7
(MCM7) and the pre-rRNA processing Trypanosoma ser-
ine–arginine 1 protein (TSR1).
DNA sequences for each locus were aligned using the
program MAFFT version 6 (Katoh and Toh 2008). For the
ITS, nuLSU, RPB1, MCM7 and TSR1 loci, we applied the
G-INS-I alignment algorithm, ‘200PAM/K = 2’ scoring
matrix, and offset value = 0.0, with the remaining
parameters set to default values and for the mtSSU we used
the E-INS-I alignment algorithm, ‘200PAM/K = 2’ scor-
ing matrix, and offset value = 0.0. Alignments of nuLSU
and MCM7 were straightforward, but the ITS and mtSSU
alignments contained a number of ambiguous regions and
RPB1 and TSR1 contained insertions. We used the program
Gblocks v0.91b (Castresana 2000; Talavera and Castresana
2007) to delimit and remove regions of alignment uncer-
tainty, using for a ‘less stringent’ selection of ambiguous
nucleotide positions, including the ‘Allow smaller final
blocks’, ‘Allow gap positions within the final blocks’, and
‘Allow less strict flanking positions’ options.
Phylogenetic and molecular dating analyses
A maximum likelihood (ML) analysis of the concatenated
six-locus data set (ITS, nuLSU, mtSSU, RPB1, MCM7,
103
TSR1) was performed in RAxML v 8.1.11with the
GTRGAMMA model, a parameter (C) for rate hetero-
geneity among sites and without a parameter for estimating
the proportion of invariable sites. Each ribosomal locus
was treated as a separate partition, and for the protein-
coding genes we used a three-partition approach, using the
first, second, and third codon positions as separate parti-
tions. Nodal support was evaluated using 1000 bootstrap
pseudoreplicates using the same settings and data partitions
as in the search for the optimal tree. The analyses were
performed using the program RAxML v8.1.11 (Stamatakis
2006; Stamatakis et al. 2008), as implemented on the
CIPRES Web Portal (http://www.phylo.org/portal2/), with
the GTRGAMMA model as described above.
Diversification ages were estimated using an uncorre-
lated Bayesian relaxed molecular clock model imple-
mented in the program BEAST v1.8.0 (Drummond et al.
2006; Drummond and Rambaut 2007). We used the most
likely tree derived from the six-locus RAxML phylogenetic
analysis as the starting tree. The ML topology was con-
verted to an ultrametric tree using nonparametric rate
smoothing (NPRS) (Sanderson 1997) as implemented in
the program TreeEdit v10a10 (Rambaut 2007), with the
divergence of Parmeliaceae node set at 108.96 Ma (Amo
de Paz et al. 2011) for the BEAST analyses. In BEAST, the
partitioned molecular data set was analyzed with unlinked
substitutions models across the loci, and a relaxed clock
model (uncorrelated lognormal) for each partition. A Yule
prior was assigned to the branching process. The most
appropriate model of DNA sequence evolution was selec-
ted for each marker was selected using the program Par-
titionFinder v1.1.1 (Lanfear et al. 2012). Four calibration
points were used: (C1) prior estimates of the crown of
Parmeliaceae of 85.52–136.55 Ma (Amo de Paz et al.
2011); (C2) the crown of Anzia was calibrated with the
fossil Anzia electra 35–40 Ma in European amber (Rikki-
nen and Poinar 2002); (C3) the node of Parmelia was
calibrated with the fossil Parmelia ambra, 15–45 Ma in
Dominican amber (Poinar et al. 2000); and (C4) the
diversification node of the Alectorioid clade was calibrated
with a fossil in Baltic and Bitterfeld amber (Alectoria,
24–35 Ma) (Kaasalainen et al. 2015). The crown
Parmeliaceae node was fixed by a uniform prior between
85.52 and 136.55 Ma. Three internal nodes were con-
strained with fossil-derived minimum age and the lognor-
mal prior distribution was set on the Alectoria, Anzia, and
Parmelia fossil calibrations. The lognormal distribution
has been shown to be the most appropriate for modelling
paleontological information because lineage origination
should not postdate the fossil occurrence (Ho and Phillips
2009; Magallon 2010). The lognormal mean was equal to
(fossil age ? 10%) Ma, because a clade’s node age is older
that its oldest fossils, and the zero offset was equal to
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(fossil age—1%) Ma, to ensure that the minimum age falls
within the distribution (Magallon 2010; Divakar et al.
2012).
We also compared potential differences between prior
distribution using an exponential and a lognormal prior for
the analyses. Exploratory analyses provided similar results
between both analyses (results not shown), and we selected
the lognormal prior distribution for final analyses. We ran
four different dating analyses with different assumptions,
and for each dating analysis, two independent Markov
chain Monte Carlo (MCMC) runs of 100 million genera-
tions were conducted, sampling one tree every 1000 gen-
erations. The program Tracer v1.5 (Rambaut and
Drummond 2007) was used to evaluate each chain, deter-
mine appropriate burn-in cut-off (25% of sampled trees),
and obtain the effective sample sizes (ESSs) for each
parameter [i.e. ESS C(i.e.. Convergence was also assessed
using the program ‘Are We There Yet?’(AWTY)] to ensure
that standard deviations of split frequencies between runs
approached zero and visualize split probabilities (Nylander
et al. 2008). Using LogCombiner version 1.8.0 and
TreeAnnotator version 1.8.0 the chains were combined to
obtain the mean node heights posterior distributions of
estimated divergence dates (Drummond and Rambaut
2007). Since BEAST has insufficient memory to generate
consensus trees from exceptionally large numbers of trees
(in this case 200,000 trees), we resampled the posterior
distribution of trees by sampling one tree every 10,000
generations after 25% burn-in cut-off, using the program
LogCombiner version 1.8.0. A consensus tree was gener-
ated of the 15,000 resampled trees in TreeAnnotator. Mean
node age, 95% highest posterior density (HPD) and pos-
terior probability (pp) were mapped on the maximum clade
credibility tree. Only the strongly supported nodes were
considered for divergence time estimates.
Phylogenetic trees were drawn using the program Fig-
Tree v1.4.2 (Rambaut 2009).
Temporal banding approach
With the obtained phylogeny, we assigned each OTU (tip)
to a genus and a family according to the current classifi-
cation and used ‘‘temporal error scores’’ (Holt and Jønsson
2014) to calculate the error from the current taxonomy
when a certain temporal threshold was applied. Temporal
error scores compare the total amount of error (departure
from consistent classification) to mean random expecta-
tions. In our method, we applied a series of temporal
thresholds from the tip (time = 0) to the root (the tree
depth) and calculated a temporal error score for each
threshold at both generic and family levels. The temporal
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Fungal Diversity (2017) 84:101–117
threshold (±5 percent error margin) with the minimum
error score was then used as a cut-off point for the new
classification with the temporal approach, where we rec-
ognized all of the monophyletic groups that were more
recent than the cut-off as individual taxa at that level.
Results
New sequences (128) generated for this study have been
deposited in GenBank (Online Resource 1). The concate-
nated six-locus data matrix included 392 operational tax-
onomic units (OTUs) and consisted of 3605
unambiguously aligned nucleotide position characters. The
effective sample sizes (ESSs) of all estimated parameters
were well above 200 in the Bayesian analyses, and the
‘compare plot’ produced by AWTY indicated that parallel
MCMC runs achieved topological convergence (results not
shown).
In the phylogenetic estimate (Fig. 1a–d) Parmeliaceae
and Gypsoplacaceae form a strongly supported sister-group
(pp = 1.0). Some species of the highly polyphyletic genus
Lecanora form a clade (pp = 1.0) and Cladoniaceae forms
a well-supported clade (pp = 1.0), both clades form a well-
supported clade, but the relationships of the three clades
lacks support (pp = 0.71). Species of the highly poly-
phyletic genus Protoparmelia and Miriquidica form a well-
supported monophyletic group (pp = 1.0) that has an
unsupported sister-group relationship to Ramboldiaceae
(pp = 0.94), which are strongly supported (pp = 1.0).
Mycoblastaceae (pp = 1.0) and Stereocaulaceae
(pp = 0.99) are both well-supported monophyletic groups
and form a strongly supported clade including two Lecidea
s. lat. (pp = 0.97). This clade has an unsupported rela-
tionship to two additional Lecidea s. lat. species
(pp = 0.66). Lecanoraceae s. str., including Lecanora s.
str., Lecidella, Protoparmeliopsis, and Rhizoplaca is well
supported as a monophyletic group (pp = 1.0). Parmeli-
aceae is strongly supported (pp = 1.0) and Protoparmelia
as the earliest diverging clade in the family (pp = 1.0),
which forms two major well-supported monophyletic
clades (both pp = 1.0). The phylogenetic relationships
within Parmeliaceae s. str. agree with those discussed
previously (Divakar et al. 2015) and are not treated here in
detail.
The temporal banding approach identified 107.5 Ma as
threshold for the family level, which resulted with a 5%
taxonomic error margin in a temporal band between 102.13
and 112.88 Ma (Fig. 1a–d). For the genus level, the tem-
poral banding approached identified 31 Ma as threshold
and with a 5% taxonomic error margin this resulted in a
temporal band between 29.45 and 32.55 Ma (Fig. 1a–d).
Fungal Diversity (2017) 84:101–117
Fig. 1 a–d Chronogram tree depicting phylogenetic relationships of
Parmeliaceae and related families within Lecanorales. The time line
at the bottom of the tree represents age in millions of years (Ma).
Colored circles indicate posterior probability (PP) support (3) (left
key). Mean age estimates (in Ma) are indicated for the supported
nodes, with node bars showing the associated 95% credibility
105
intervals. The nodes indicated by c represent calibration nodes.
Temporal band for family level indicated by orange lines (upper and
lower level) and those for the genus level are in green (upper and
lower level). This is a phylogenetic estimate based on a six-locus data
set and a maximum likelihood analysis using Beast (details in text)
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Fig. 1 continued

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Fig. 1 continued

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Fig. 1 continued
Discussion
As the Parmeliaceae data sets—except some new sequen-
ces—from Divakar et al. (2015) and Singh et al. (2015)
have been used in this study, we refer to those publications
for a comprehensive discussion of phylogenetic relation-
ships within the family. The close phylogenetic relation-
ship of Gypsoplacaeae and Parmeliaceae has repeatedly
been found (Arup et al. 2007; Singh et al. 2013; Divakar
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Fungal Diversity (2017) 84:101–117
et al. 2015), whereas Miadlikowska et al. (2014) found
Gypsoplaca nested in a clade with Lecidea cyrtidia, L.
floridensis, L. nylanderi, and L. roseotincta, which formed
a sister group to Miriquidica garovaglii. In our analysis and
Singh et al. (2013) with a larger sampling of Miriquidica
and Protoparmelia s. lat. species, M. garovaglii forms a
strongly supported monophyletic group with other Miriq-
uidica spp. and Protoparmelia s. lat. This suggests that the
placement of Gypsoplaca in Miadlikowska et al. (2014)
Fungal Diversity (2017) 84:101–117
might have been due to insufficient taxon sampling. The
relationships of the Gypsoplacaceae ? Parmeliaceae clade
remain unresolved.
As in previous studies (Singh et al. 2013; 2015), the
Protoparmelia atriseda group is closely related to Miriq-
uidica and both form a strongly supported clade that might
warrant taxonomic recognition as a separate family. Poly-
phyly of Lecanoraceae has already been shown in several
studies but usually a core group of Lecanora s. str. and
related genera was recovered as a well-supported mono-
phyletic group (Schmull et al. 2011; Miadlikowska et al.
2014; Zhao et al. 2015). The circumscription and classifi-
cation of Lecanoraceae is in urgent need of revision but this
is beyond the scope of this manuscript.
In our temporal approach, we consider clades that have
originated before the temporal band for a taxonomic rank
as belonging to different taxa at that rank, whereas clades
that have originated after the temporal band as belonging to
the same taxon at that rank. For clades that have evolved
within the temporal band we adopted a conservative
approach of not changing the current classification.
Adopting this approach, the current circumscriptions of the
families Cladoniaceae, Lecanoraceae s. str., Mycoblas-
taceae, Ramboldiaceae, and Stereocaulaceae is supported,
and the data suggest that the clade including Miriquidica
and Protoparmelia s. lat. might require taxonomic recog-
nition at the family level (Fig. 1a–d). The separation of
Gypsoplacaceae and Protoparmelia s. str. from the
majority of Parmeliaceae falls within the temporal band of
families. Hence, we do not suggest changing the current
classification, i.e. accepting Gypsoplacaceae as different
from Parmeliaceae and including Protoparmelia s. str.
within Parmeliaceae. Given the long independent evolu-
tionary history of the Protoparmelia clade we describe a
new subfamily below to accommodate the species in this
clade. The two major groups within the Protoparmelia
clade have separated much earlier than the lower threshold
for genera. Consequently—in contrast to our previous
taxonomic proposal (Papong et al. 2011)—we resurrect the
genus Maronina to accommodate species of the tropical
clade below and accept two genera within the Pro-
toparmelia clade. In fact, the diversification of Maronina is
estimated to have started earlier than the lower threshold
for genera. Additional taxon sampling is needed to evaluate
whether additional genera should be recognized in Ma-
ronina or not.
The large majority of genera in the core Parmeliaceae
are supported in their current circumscription (Lumbsch
and Huhndorf 2010; Miadlikowska et al. 2011; Divakar
et al. 2012; Thell et al. 2012; Divakar et al. 2013; Feren-
cova et al. 2014; Kirika et al. 2015, 2016a, b) by the
temporal banding approach, including Alectoria (incl.
Gowardia), Allantoparmelia, Arctoparmelia,
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Austroparmelina, Brodoa, Bryocaulon, Bryoria, Cano-
parmelia s. str., Cetrelia, Coelopogon, Cornicularia,
Dactylina, Emodomelanelia, Esslingeriana, Evernia,
Everniopsis, Flavoparmelia, Flavopunctelia, Hypogymnia
(incl. Cavernularia), Hypotrachyna (incl. Cetrariastrum,
Everniastrum and Parmelinopsis), Imshaugia, Melanelia,
Melanohalea, Menegazzia, Montanelia, Myelochroa, Nip-
ponoparmelia, Nodobryoria, Notoparmelia, Omphalodium,
Oropogon, Pannoparmelia, Parmelia s. str., Parmelina,
Parmeliopsis, Parmotrema (incl. Crespoa), Platismatia,
Pseudephebe, Pseudevernia, Pseudoparmelia, Psilo-
parmelia, Relicina (incl. Relicinopsis), Remototrachyna,
Sulcaria, and Xanthoparmelia. Major characteristics of
most of these genera can be found in Crespo et al. (2010)
and Thell et al. (2012), whereas the circumscription of
some genera has changed recently: Hypogymnia (Miad-
likowska et al. 2011), Hypotrachyna (Divakar et al. 2013),
Parmotrema (Kirika et al. 2016a), and Relicina (Kirika
et al. 2016b). In addition, the genera Montanelia (Divakar
et al. 2012) and Notoparmelia (Ferencova et al. 2014) were
recently described—discussions on phenotypical traits of
those can be found in the papers cited above.
However, the circumscriptions of several genera were
not supported when applying this temporal banding
approach. The diversification of the genus Usnea predates
the diversification of other genera—the subgenera Dolic-
housnea and Eumitria separated from subgen. Usnea early
on and even the separation of the former two subgenera fall
within the temporal band for the genus level. Hence, in
contrast to our previous taxonomic classification proposal
(Wirtz et al. 2006), we propose to accept the genera
Dolichousnea and Eumitria as circumscribed earlier (Ar-
ticus 2004). This taxonomic change does not require any
nomenclatural novelties, since the genera were accepted
previously (Articus 2004). Our results also question the
classification of Anzia, with the separation of A. colpodes
from other species in the genus earlier than the temporal
band. However, our sampling only includes three out of c.
34 known species—hence additional sampling is required
to address the classification of species currently placed in
Anzia. Monophyly of Lethariella and its relationships to
Letharia also require further study—again our taxon sam-
pling is insufficient to address the delimitation of these
genera. The non-monophyly of Bulbothrix has been found
in numerous previous studies (Divakar et al. 2006; Crespo
et al. 2010; Divakar et al. 2010; Miadlikowska et al. 2014;
Divakar et al. 2015). However, until now it has not been
possible to sequence the type species of the genus, which
would be necessary to identify which of the two clades
represents Bulbothrix s. str. Our analysis suggests that
Bulbothrix clade 1 is a distinct genus separated well before
the threshold for the genus level from its sister-group Re-
mototrachyna, whereas Bulbothrix clade 2 is probably
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congeneric with Parmelinella, the latter being a younger
name (Hale 1974; Elix and Hale 1987).
A clade of Melanelixia species occurring in the southern
Hemisphere diverged from Melanelixia before the pro-
posed temporal band for the circumscribing genera. These
taxa were not included in the original circumscription of
the genus (Blanco et al. 2004), but later included because
of their sister-group relationship to other Melanelixia spe-
cies (Crespo et al. 2010). Based on their early divergence
we below describe the new genus Austromelanelixia to
accommodate these species. The phenotypical characters of
the new genus are discussed below under taxonomy.
The two clades of lichenicolous fungi in Parmeliaceae
have originated recently and hence those are falling below
the threshold for the genus level. Therefore, we propose to
reduce them below to synonymy with their lichen-forming
sister group: Nesolechia with Punctelia and Raesaenenia
with Protousnea, respectively. The enlarged genera Punc-
telia and Protousnea include foliose and fruticose lichen-
forming fungi, respectively and lichenicolous fungi. Fungi
with different life-styles, such as lichen-forming and
lichenicolous or saprophytic species are classified within
the same genus in numerous fungal lineages (Lawrey and
Diederich 2003; Wedin et al. 2004; Lawrey and Diederich
2016).
The bulk of changes in classification, however, are
restricted to the cetrarioid group. This agrees with previous
studies that genera in this group have low genetic distances
(Lumbsch 2002; Nelsen et al. 2011) and several studies
concluded that the generic delimitation in this group is in
need of revision (Thell 1995; Thell et al. 2009, 2012).
Consequently, we here propose to accept two genera within
the cetrarioid core for the two major clades—Cetraria and
Nephromopsis. The necessary new combinations are pro-
posed below under taxonomy.
It has been suggested that an adoption of a temporal
approach to classification would necessitate ‘‘dramatic rank
changes for many taxa’’ (Avise and Johns 1999) and if
standardized among all organismal groups this would cer-
tainly be true. However, we show here that this approach
does not necessarily require an extraordinary amount of
taxonomic changes when applied to specific taxonomic
groups. In our opinion taxonomic ranks can only serve a
role if they are comparable, otherwise they are potentially
misleading. Taxonomic classification serves an important
role and is being used by biologists and conservationists
that are not taxonomists. Hence, we feel it is the respon-
sibility of taxonomists to provide users with a classification
that is as objective as possible.
We anticipate that our study will encourage colleagues
to explore the temporal approach to classification in other
groups of fungi. For example, different generic classifica-
tion in Lecanoraceae and Teloschistaceae have been
123
Fungal Diversity (2017) 84:101–117
proposed (Gaya et al. 2008, 2012; Arup et al. 2013; Kon-
dratyuk et al. 2013, 2014a, b,c; Miadlikowska et al. 2014;
Zhao et al. 2015) and it would be interesting to examine
how the temporal approach can be used to more objectively
circumscribe comparable taxonomic units.
Taxonomy
Based on our temporal approach, a number of taxonomic
changes are necessary that are proposed below.
Parmelioideae
The nominal subfamily includes all genera in Parmeliaceae
with the exception of Maronina and Protoparmelia, which
are placed in the new subfamily Protoparmelioideae.
Austromelanelixia Divakar, Crespo & Lumbsch, gen. nov.
Mycobank MB 820132
Type: Austromelanelixia piliferella (Essl.) Divakar, Crespo
& Lumbsch
Etymology. The epithet refers to the distribution of the
genus in the southern Hemisphere and the superficial
resemblance of its species with Melanelixia spp.
Diagnosis. Thallus foliose; upper surface olive-green to
dark brown, often with hyaline cortical hairs on lobe apices
or isidial tip, maculate especially on lobe margins, lacking
pseudocyphellae; upper cortex covered by a pored (fenes-
trate) epicortex. Ascospores ellipsoid, colourless, simple,
10–18 9 7–10 lm. Conidia bifusiform, hyaline,
5–7 9 1 lm. Medulla containing gyrophoric acid. Aus-
tralasian distribution.
Remarks. Austromelanelixia is characterized by a combi-
nation of features, including hyaline cortical hairs on lobe
apices, lack of pseudocyphellae, maculate upper surface,
pored or fenestrated epicortex, and the presence of gyro-
phoric acid as major constituent. It has an austral distri-
bution. The genus includes four species, which grow on
bark (rarely on rock) in eastern and southeastern Australia,
Tasmania and New Zealand. One species (A. subglabra)
also occurs in southern South America. This new genus is
only known from the southern Hemisphere, whereas the
superficially similar sister-group Melanelixia s. str. has its
center of distribution in the northern Hemisphere.
Austromelanelixia calva (Essl.) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820133) Basionym: Parmelia
calva Essl., J. Hattori Bot. Lab. 42: 60 (1977) : Me-
lanelia calva (Essl.) Essl., Mycotaxon 7: 47
(1978) : Melanelixia calva (Essl.) A. Crespo, Divakar &
Elix, Taxon 59: 1750 (2010).
Fungal Diversity (2017) 84:101–117
Austromelanelixia fuscosorediata (Essl.) Divakar,
Crespo & Lumbsch, comb. nov. (MB 820135) Basionym:
Parmelia fuscosorediata Essl., J. Hattori Bot. Lab. 42: 68
(1977) : Melanelia fuscosorediata (Essl.) Essl., Myco-
taxon 7: 47 (1978).
Austromelanelixia glabratuloides (Essl.) Divakar,
Crespo & Lumbsch, comb. nov. (MB 820134) Basionym:
Parmelia glabratuloides Essl., J. Hattori Bot. Lab. 42: 72
(1977) : Melanelia glabratuloides (Essl.) Essl., Myco-
taxon 7: 48 (1978) : Melanelixia glabratuloides (Essl.)
A. Crespo, Divakar & Elix, Taxon 59: 1750 (2010).
Austromelanelixia piliferella (Essl.) Divakar, Crespo
& Lumbsch, comb. nov. (MB 820136) Basionym: Par-
melia piliferella Essl., J. Hattori Bot. Lab. 42: 83
(1977) : Melanelia piliferella (Essl.) Essl., Mycotaxon 7:
48 (1978) : Melanelixia piliferella (Essl.) A. Crespo,
Divakar & Elix, Taxon 59: 1750 (2010).
Austromelanelixia subglabra (Räs.) Divakar, Crespo
& Lumbsch, comb. nov. (MB 820137) Basionym: Par-
melia subaurifera var. subglabra Räs., Ann. Bot. Soc.
Zool.-Bot. Fenn. Vanamo 2(1): 19 (1932) : Parmelia
subglabra (Räs.) Essl., Bryologist 76: 307 (1973) : Me-
lanelia subglabra (Essl.) Essl., Mycotaxon 7: 48
(1978) : Melanelixia subglabra (Essl.) A. Crespo, Diva-
kar & Elix, Taxon 59: 1750 (2010).
Cetraria Ach., Meth. Lich.: 292 (1803)
=Allocetraria Kurok. & M.J. Lai, Bull. Natn. Sci. Mus.,
Tokyo, B 17: 60 (1991)
=Cetrariella Kärnefelt & A. Thell, Bryologist 96: 402
(1993)
=Usnocetraria M.J. Lai & J.C. Wei, J. Natnl. Taiwan Mus.
60: 57 (2007)
=Vulpicida J.E. Mattsson & M.J. Lai, Mycotaxon 46: 427
(1993)
The genus Cetraria is here accepted to include all species
in the Cetraria clade (Nelsen et al. 2011) or cetrarioid
clade A (Thell et al. 2009). The majority of species have
available names in Cetraria with the exception of eight,
mostly recently described, species that are combined into
the genus below. Cetraria as here circumscribed includes
species with brown or yellowish green, dorsiventral,
mainly erect foliose (rarely foliose), subfruticose or cae-
spitose thallus; with or without pseudocyphellae, pseudo-
cyphellae marginal or laminal on the lower surface;
predominantly marginal apothecia and pycnidia; ellipsoid
ascospores; with a single swelling (apical or central) i.e.
oblong, citriform, sublageniform or filiform shape conidia;
with centre of diversity in the Himalaya and Europe.
Cetraria corrugata (R.F. Wang, X.L. Wei & J.C. Wei)
Divakar, Crespo & Lumbsch, comb. nov. (MB 820138)
111
Basionym: Allocetraria corrugata R.F. Wang, X.L. Wei &
J.C. Wei, Mycotaxon 130: 585 (2015).
Cetraria endochrysea (Lynge) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820139) Basionym: Dactylina
endochrysea Lynge, Skr. Svalbard Ishavet 59: 27
(1933) : Allocetraria endochrysea (Lynge) Kärnefelt &
A. Thell, Nova Hedwigia 62: 507 (1996).
Cetraria flavonigrescens (A. Thell & Randlane)
Divakar, Crespo & Lumbsch, comb. nov. (MB 820140)
Basionym: Allocetraria flavonigrescens A. Thell & Rand-
lane, Flechten Follmann: 359 (1995) : Usnocetraria
flavonigrescens (A. Thell & Randlane) M.J. Lai & J.C.
Wei, J. Natnl. Taiwan Mus. 60: 57 (2007).
Cetraria isidiigera (Kurok. & M.J. Lai) Divakar, Cre-
spo & Lumbsch, comb. nov. (MB 820141) Basionym:
Allocetraria isidiigera Kurok. & M.J. Lai, Bull. Natn. Sci.
Mus., Tokyo, B 17: 62 (1991).
Cetraria laii Divakar, Crespo & Lumbsch, nom. nov.
(MB 820142) Basionym: Evernia stracheyi C. Bab., Hoo-
ker’s J. Bot. Kew Gard. Misc. 4: 244 (1852) : Alloce-
traria stracheyi (C. Bab.) Kurok. & M.J. Lai, Bull. Natn.
Sci. Mus., Tokyo, B 17: 62 (1991); non Cetraria stracheyi
C. Bab., Hooker’s J. Bot. Kew Gard. Misc. 4: 245 (1852).
Cetraria sinensis (X.Q. Gao) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820143) Basionym: Alloce-
traria sinensis X.Q. Gao, Flechten Follmann: 365
(1995) : Usnocetraria sinensis (X.Q. Gao) M.J. Lai &
J.C. Wei, J. Natnl. Taiwan Mus. 60: 57 (2007).
Cetraria wangii Divakar, Crespo & Lumbsch, nom.
nov. (MB 820145) Basionym: Allocetraria yunnanensis
R.F. Wang, L.S. Wang & J.C. Wei, Lichenologist 47: 33
(2015); non Cetraria yunnanensis (Nyl.) Zahlbr., Trav.
Sous-Sect. Troitzkossawsk-Khiakta, sect. Pays d’Amour
Soc. Imp. Russ. Géogr. 12: 89 (1911)
Cetraria weii Divakar, Crespo & Lumbsch, nom. nov.
(MB 820146) Basionym: Allocetraria capitata R.F. Wang,
L.S. Wang & J.C. Wei, Mycosystema 33: 21 (2014); non
Cetraria capitata Lynge, Lich. Nov. Zemlya: 207 (1928).
Nephromopsis Müll. Arg., Flora 74: 374 (1891)
=Ahtiana Goward, Bryologist 88: 370 (1985)
=Arctocetraria Kärnefelt & A. Thell, Bryologist 96: 402
(1993)
=Cetrariopsis Kurok., Mem. Natn. Sci. Mus., Tokyo 13:
140 (1980)
=Cetreliopsis M.J. Lai, Quarterly J. Taiwan Mus. 33: 218
(1980)
=Flavocetraria Kärnefelt & A. Thell, Acta Bot. Fenn. 150:
81 (1994)
=Flavocetrariella Awasthi, A Compendium of the Mac-
rolichens from India, Nepal and Sri Lanka: 161 (2007)
=Kaernefeltia A. Thell & Goward, Bryologist 99: 125
(1996)
123
112
=Masonhalea Kärnefelt, Bot. Not. 130: 101 (1977)
=Tuckermanella Essl., Mycotaxon 85: 135 (2003)
=Tuckermannopsis Gyeln., Acta Faun. Fl. Univ., ser. 2,
Bot. 1(5-6): 6 (1933)
=Tuckneraria Randlane & A. Thell, Acta Bot. Fenn. 150:
144 (1994)
We here accept the genus Nephromopsis for all species in
the Nephromopsis clade (Nelsen et al. 2011) or cetrarioid
clade B (Thell et al. 2009). 30 new combinations are
necessary that are proposed below. Nephromopsis as here
circumscribed includes species with yellowish grey or
straw-yellow or brown, dorsiventral, foliose (rarely sub-
fruticose) thallus; often pseudocyphellate, pseudocyphellae
either on both surfaces or marginal; predominantly mar-
ginal apothecia and pycnidia; subglobose or globose (rarely
ellipsoid) ascospores; conidia with two apical or subapical
swellings, dumb-bell to disc-bar shaped conidia (rarely
without swelling, baciliform); with centres of distribution
in western North American and east Asia.
Nephromopsis americana (Spreng.) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820147) Basionym: Nephroma
americana Spreng., Kgl. svensk. Vetensk.-Akad. Handl.
46: 49 (1820) : Tuckermannopsis americana (Spreng.)
Hale, Bryologist 90: 164 (1987).
Nephromopsis andrejevii (Oxner) Divakar, Crespo &
Lumbsch, comb. nov. (MB MB820148) Basionym: Ce-
traria andrejevii Oxner, J. Bot. Acad. Sci. RSS Ukraine
1(3–4): 44 (1940) : Arctocetraria andrejevii (Oxner)
Kärnefelt & A. Thell, Bryologist 96: 402 (1993).
Nephromopsis arizonica (Essl.) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820149) Basionym: Tucker-
manella arizonica Essl., Mycotaxon 85: 137 (2003).
Nephromopsis aurescens (Tuck.) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820150) Basionym: Cetraria
aurescens Tuck., Proc. Amer. Acad. Sci. 1: 208
(1846) : Tuckermannopsis aurescens (Tuck.) Hale, Bry-
ologist 90: 164 (1987) : Ahtiana aurescens (Tuck.) A.
Thell & Randlane, Bryologist 98: 599 (1995).
Nephromopsis chlorophylla (Willd.) Divakar, Crespo
& Lumbsch, comb. nov. (MB 820151) Basionym: Lichen
chlorophyllus Willd., in Humboldt, Fl. Friberg. Spec.: 20
(1872) : Cetraria chlorophylla (Willd.) Poetsch, Medd.
Soc. Fauna Fl. Fenn. 6: 121 (1872) : Tuckermannopsis
chlorophylla (Willd.) Hale, Bryologist 90: 164 (1987).
Nephromopsis coralligera (W.A. Weber) Divakar,
Crespo & Lumbsch, comb. nov. (MB 820152) Basionym:
Cetraria fendleri f. coralligera W.A. Weber, Univ. Colo.
Stud., Biol. Ser. 10: 11 (1963) : Cetraria coralligera
(W.A. Weber) Hale, Bryologist 70: 414 (1968) : Tuck-
ermannopsis coralligera (W.A. Weber) W.A. Weber,
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Fungal Diversity (2017) 84:101–117
Bryologist 94: 399 (1991) : Tuckermanella coralligera
(W.A. Weber) Essl., Mycotaxon 85: 139 (2003).
Nephromopsis culbersonii (Hale) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820153) Basionym: Cetraria
culbersonii Hale, Bryologist 70: 414 (1967) : Melanelia
culbersonii (Hale) A. Thell, Nova Hedwigia 60: 419
(1995).
Nephromopsis cucullata (Bellardi) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820154) Basionym: Lichen
cucullatus Bellardi., Osservaz. Bot. 1: 54 (1788) : Ce-
traria cucullata (Bellardi) Ach., Meth. Lich.: 293
(1803) : Flavocetraria cucullata (Bellardi) Kärnefelt &
A. Thell, Acta Bot. Fenn. 150: 81 (1994) : Allocetraria
cucullata (Bellardi) Randlane & Saag, Mycotaxon 44: 492
(1992).
Nephromopsis fendleri (Nyl.) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820155) Basionym: Platysma
fendleri Nyl., Syn. meth. lich. 1(2): 309 (1860) : Cetraria
fendleri (Nyl.) Tuck., Gener. Lich.: 33 (1872) : Tucker-
mannopsis fendleri (Nyl.) Hale, Bryologist 90: 164
(1987) : Tuckermanella fendleri (Nyl.) Essl., Mycotaxon
85: 139 (2003).
Nephromopsis gilva (Asahina) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820156) Basionym: Cetraria
gilva Asahina, J. Jap. Bot. 28: 139 (1953) : Tucker-
mannopsis gilva (Asahina) M.J. Lai, Quarterly J. Taiwan
Museum 33: 225 (1980).
Nephromopsis iberica (Crespo & Barreno) Divakar,
Crespo & Lumbsch, comb. nov. (MB 820157) Basionym:
Cetraria iberica Crespo & Barreno, An. Jard. Bot. Madrid
37: 205 (1980) : Kaernefeltia iberica (Crespo & Bar-
reno) Crespo & Barreno, Bibl. Lichenol. 110: 57 (2016).
Nephromopsis inermis (Nyl.) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820158) Basionym: Cetraria
crispa f. inermis Nyl., Bull. Soc. linn. Normand., sér. 4 1:
214 (1887) : Cetraria inermis (Nyl.) Krog, Bryologist
76: 299 (1973) : Tuckermannopsis inermis (Nyl.)
Kärnefelt, Bryologist 96: 403 (1993) : Masonhalea
inermis (Nyl.) Lumbsch, Nelsen & A. Thell, Nordic Lichen
Flora 4: 67 (2011).
Nephromopsis laeteflava (Zahlbr.) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820159) Basionym: Cetraria
laeteflava Zahlbr., Fedd. Rep. 33: 60 (1933) : Nephro-
mopsis straminea var. laeteflava (Zahlbr.) Räs., Kuopion
Luonnon Ystäv. Yhdstyksen Julkais., ser. B 2(6): 50
(1952) : Cetreliopsis laeteflava (Räs.) Randlane & Saag,
Crypt. Bryol. Lichén. 16: 51 (1995).
Nephromopsis merrillii (Du Rietz) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820160) Basionym: Cetraria
merrillii Du Rietz, Ark. Bot. 20A(11): 42
(1926) : Kaernefeltia merrillii (Du Rietz) A. Thell &
Goward, Bryologist 99: 128 (1996).
Fungal Diversity (2017) 84:101–117
Nephromopsis microphyllica (W.L. Culb. & C.F.
Culb.) Divakar, Crespo & Lumbsch, comb. nov. (MB
820161) Basionym: Cetraria microphyllica W.L. Culb. &
C.F. Culb., Bryologist. 70: 161 (1967) : Tuckermannop-
sis microphyllica (W.L. Culb. & C.F. Culb.) M.J. Lai,
Quarterly J. Taiwan Museum 33: 226 (1980).
Nephromopsis nigricascens (Nyl.) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820163) Basionym: Platysma
nigricascens Nyl., Medd. Soc. Fauna Fl. Fenn. 18: 50
(1891) : Cetraria nigricascens (Nyl.) Elenkin, Izv. Imp.
St.-Petersb. Bot. Sada 27: 14 (1909) : Arctocetraria
nigricascens (Nyl.) Kärnefelt & A. Thell, Bryologist 96:
402 (1993).
Nephromopsis nivalis (L.) Divakar, Crespo & Lumb-
sch, comb. nov. (MB 820164) Basionym: Lichen nivalis
L., Sp. Plant. 2: 1145 (1753) : Cetraria nivalis (L.) Ach.,
Meth. Lich.: 294 (1803) : Flavocetraria nivalis (L.)
Kärnefelt & A. Thell, Acta Bot. Fenn. 150: 84
(1994) : Allocetraria nivalis (L.) Randlane & Saag,
Mycotaxon 44: 492 (1992).
Nephromopsis orbata (Nyl.) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820166) Basionym: Platysma
orbatum Nyl., Flora 52: 442 (1869) : Cetraria orbata
(Nyl.) Fink, Mycologia 11: 298 (1919) : Tucker-
mannopsis orbata (Nyl.) M.J. Lai, Quarterly J. Taiwan
Museum 33: 226 (1980).
Nephromopsis papuae (Randlane & Saag) Divakar,
Crespo & Lumbsch, comb. nov. (MB 820169) Basionym:
Cetreliopsis papuae Randlane & Saag, Crypt. Bryol.
Lichén. 16: 52 (1995).
Nephromopsis pseudoweberi (Essl.) Divakar, Crespo
& Lumbsch, comb. nov. (MB 820171) Basionym: Tuck-
ermanella pseudoweberi Essl., Mycotaxon 85: 139 (2003).
Nephromopsis rickieae (Essl.) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820181) Basionym: Tucker-
manella rickieae Essl., Bibl. Lichenol. 110: 498 (2016).
Nephromopsis richardsonii (Hook.) Divakar, Crespo
& Lumbsch, comb. nov. (MB 820173) Basionym: Cetraria
richardsonii Hook., in Richardson, Narrat. Journ. Polar-
Sea, App. 6: 33 (1823) : Masonhalea richardsonii
(Hook.) Kärnefelt, Bot. Not. 130: 104 (1977).
Nephromopsis sphaerosporella (Müll. Arg.) Divakar,
Crespo & Lumbsch, comb. nov. (MB 820175) Basionym:
Parmelia sphaerosporella Müll. Arg., Flora 74: 378
(1891) : Ahtiana sphaerosporella (Müll. Arg.) Goward,
Bryologist 88: 370 (1986).
Nephromopsis subalpina (Imshaug) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820176) Basionym: Cetraria
subalpina Imshaug, Mycologia 42: 30 (1951) : Tucker-
mannopsis subalpina (Imshaug) Kärnefelt, Bryologist 96:
403 (1993).
Nephromopsis subfendleri (Essl.) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820177) Basionym: Cetraria
113
subfendleri Essl., Mycologia 65: 610 (1973) : Tucker-
manella subfendleri (Essl.) Essl., Mycotaxon 85: 140
(2003).
Nephromopsis thailandica (Elix & M.J. Lai) Divakar,
Crespo & Lumbsch, comb. nov. (MB 820179) Basionym:
Cetreliopsis thailandica Elix & M.J. Lai, Mycotaxon 84:
356 (2002).
Nephromopsis tuckermanii (Tuck.) Divakar, Crespo &
Lumbsch, nom. nov. (MB 820180) Basionym: Cetraria
californica Tuck., Amer. J. Sci. Arts, ser. 2 28: 203
(1859) : Cornicularia californica (Tuck.) Du Rietz, Ark.
Bot. 20A(11): 32 (1926) : Kaernefeltia californica
(Tuck.) A. Thell & Goward, Bryologist 99: 126 (1996);
non Nephromopsis californica Gyeln., Ann. Crypt. Exot. 4:
169 (1931).
Nephromopsis ulophylloides (Asahina) Divakar, Cre-
spo & Lumbsch, comb. nov. (MB 820182) Basionym:
Cetraria ulophylloides Asahina, J. Jap. Bot. 28: 138
(1953) : Tuckermannopsis ulophylloides (Asahina) M.J.
Lai, Quarterly J. Taiwan Museum 33: 226 (1980).
Nephromopsis weberi (Essl.) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820183) Basionym: Cetraria
weberi Essl., Mycologia 65: 607 (1973) : Tuckermanella
weberi (Essl.) Essl., Mycotaxon 85: 140 (2003).
Protousnea (Motyka) Krog, Norw. J. Bot. 23: 9 (1976)
:Usnea subgen. Protousnea Motyka, Lich. Gen. Usnea
Monogr. 1: 7 (1936)
=Raesaenenia D. Hawksw., Boluda & H. Lindgr., New
Phytologist 208: 1221 (2015)
As discussed above, the recently originated lichenicolous
genus Raeasenenia is here reduced to synonymy with its
sister-group Protousnea. A new combination for the single
species is proposed below.
Protousnea huuskonenii (Räsänen) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820185) Basionym: Phacopsis
huuskonenii Räsänen, Lichenoth. Fenn. 21: no. 525
(1948) : Raesaenenia huuskonenii (Räsänen) D.
Hawksw., Boluda & H. Lindgr., New Phytologist 208:
1221 (2015).
Punctelia Krog, Nord. J. Bot. 2: 290 (1982), nom. cons.
prop.
=Nesolechia A. Massal., Misc. Lichenol.: 43 (1856)
The lichenicolous genus Nesolechia is very closely related
to Punctelia and in fact has separated from the lineage so
recently that we reduce the genus to synonymy with
Punctelia. Since the generic placement of species currently
included in Nesolechia and its separation from Phacopsis is
poorly known with three independent origins of licheni-
colous life-style within Parmeliaceae (Triebel and
123
114
Rambold 1988; Rambold and Triebel 1992; Triebel et al.
1995; Persoh and Rambold 2002; Divakar et al. 2015), we
only transfer the type species below. The generic name
Nesolechia predates Punctelia. To ensure that the widely
used name Punctelia is protected, it is being formally
proposed for conservation.
Punctelia oxyspora (Tul.) Divakar, Crespo, D.L.
Hawksw. & Lumbsch, comb. nov. (MB 820184) Basio-
nym: Abrothallus oxysporus Tul., Ann. Sci. Naot., Bot. sér.
3, 17: 116 (1852) : Nesolechia oxyspora (Tul.) A. Mas-
sal., Misc. Lichenol.: 43 (1856) : Phacopsis oxyspora
(Tul.) Triebel & Rambold, Nova Hedwigia 47: 300 (1988).
Protoparmelioideae Divakar, Crespo & Lumbsch, subfam.
nov.
Mycobank MB 820178
Type: Protoparmelia M. Choisy, Bull. Soc. Bot. Fr. 76: 523
(1929)
Diagnosis. Thallus crustose, rimose to verrucose-areolate,
saxicolous or epiphytic, upper surface pale grey-brown to
chestnut-brown to dark brown. Photobiont trebouxioid.
Apothecia laminal, lecanorine, with a cupulate exciple.
Asci clavate, Lecanora-type; outer wall intensely amyloid;
tholus well-developed, with intensely amyloid flanks and a
generally weakly amyloid, fuzzy, masse axiale; ocular
chamber poorly developed; 8-spored or multispored.
Ascospores narrow, one-celled, hyaline, ellipsoidal, fusi-
form-ellipsoidal, oblong-ellipsoidal or oblong. Conidia
bacilliform or filiform or short-acicular, or curved, hyaline.
Medulla containing alectoronic, lobaric or norstictic acid.
The two crustose genera Maronina and Protoparmelia
form a sister-group to all remaining Parmeliaceae and are
here classified in a separate subfamily. The subfamily
consists of two major clades: one occurring in temperate
regions and growing on siliceous rocks (Protoparmelia s.
str.) and a second clade consisting of mostly tropical spe-
cies growing on bark (Maronina). The following new
combinations are necessary:
Maronina badiola (Müll. Arg.) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820174) Basionym: Lecanora
badiola Müll. Arg., Rev. mycol. 10 (38): 61
(1888) : Protoparmelia badiola (Müll. Arg.) Kalb, Lich.
Neotrop. 8: no. 344 (1984).
Note: Aptroot et al. (2013) interpreted the name as
‘‘dadiola’’ but in the protologue the epithet is given as
‘‘badiola’’ and in the discussion there is a reference to
Protoparmelia badia, indicating that Müller Argoviensis
intended the name to be badiola (Müller 1888).
Maronina capitata (Lendemer) Divakar, Crespo &
Lumbsch, comb. nov. (MB 820172) Basionym: Pro-
toparmelia capitata Lendemer, Lichenologist 40: 332
(2008).
123
Fungal Diversity (2017) 84:101–117
Maronina corallifera (Kantvilas & Papong) Divakar,
Crespo & Lumbsch, comb. nov. (MB 820170) Basionym:
Maronina orientalis var. corallifera Kantvilas & Papong,
Lichenologist 42: 557 (2010) : Protoparmelia corallifera
(Kantvilas & Papong) Papong, Kantvilas & Lumbsch,
Lichenologist 43: 564 (2011).
Maronina isidiata (Diederich, Aptroot & Sérus.)
Divakar, Crespo & Lumbsch, comb. nov. (MB 820167)
Basionym: Protoparmelia isidiata Diederich, Aptroot &
Sérus., Bibl. Lichenol. 64: 146 (1997).
Maronina microspora (Córdova-Chávez, Aptroot &
Cáceres) Divakar, Crespo & Lumbsch, comb. nov. (MB
820165) Basionym: Protoparmelia microspora Córdova-
Chávez, Aptroot & Cáceres, Crypt. Mycol. 35: 161 (2014).
Maronina pulchra (Diederich, Aptroot & Sérus.)
Divakar, Crespo & Lumbsch, comb. nov. (MB 820162)
Basionym: Protoparmelia pulchra Diederich, Aptroot &
Sérus., Bibl. Lichenol. 64: 147 (1997).
Acknowledgements The project was financially supported by the
Spanish Ministerio de Ciencia e Innovacion (CGL2013-42498-P), and
the Negaunee Foundation (‘The greatest radiation in the fungal
kingdom’). GS was supported by a fellowship from the German
Academic Exchange Service (DAAD) and EK by a visiting scholar-
ship from The Field Museum.
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