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INTRODUCTION
The lichen genus Hypocenomyce M. Choisy grows on bark
and wood, especially on burnt trunks and stumps in conifer for-
ests (Fig. 1). Hypocenomyce sensu lato (s.l.; including Pycnora
Hafellner) is widely distributed in the Northern Hemisphere
and also occurs in Australia. Seventeen species have been as-
signed to Hypocenomyce, of which two have been shown to
belong elsewhere (reviewed below). Timdal (1984a) revised the
genus and identified four evolutionary groups. More recently
described Hypocenomyce species have been assigned to one of
these groups or to a fifth group. The characters uniting the five
groups are mainly morphological and ecological, and Timdal
(1984a: 93) hypothesized that the genus was polyphyletic.
Table 1 shows the main anatomical and chemical differences
between the five species groups based on the data of Timdal
(1984a, 2001, 2002) and Elix (2009). Although the Hypoceno-
myce xanthococca-group (Table 1), which does not grow on
burnt wood, was raised to the level of genus (as Pycnora) by
Hafellner in Hafellner & Türk (2001), all four species assigned
to that group are included in the present study together with
the eleven remaining Hypocenomyce species.
Two Hypocenomyce (H. friesii (Ach.) P. James & Gotth.
Schneid. and H. scalaris (Ach.) M. Choisy) and two Pycnora
(P. sorophora (Vain.) Hafellner and P. xanthococca (Sommerf.)
Hafellner) species were included in a molecular phylogenetic
study of the Lecanoromycetes by Wedin & al. (2005). Their
phylogenetic results corroborated a polyphyletic Hypoceno-
myce s.l.: (1) Hypocenomyce friesii was strongly supported as
sister to Umbilicaria Hoffm.; (2) H. scalaris (two accessions)
was sister to a clade consisting of Boreoplaca Timdal and
Ophioparma Norman; and, (3) a clade of P. sorophora and
P. xanthococca was either sister to the Acarosporaceae (par-
simony) or the Candelariaceae (Bayesian). The H. scalaris–
Boreoplaca–Ophioparma group was corroborated in a sep-
arate study of Lecanoromycetes phylogeny (Miądlikowska
& al., 2006), in which two different collections of H. scalaris
were included.
Molecular phylogenetics and taxonomy of Hypocenomyce
sensu lato (Ascomycota: Lecanoromycetes): Extreme polyphyly
and morphological/ecological convergence
Mika Bendiksby & Einar Timdal
Natural History Museum, Universit y of Oslo, P.O. Box 1172 Blindern, 0318 Oslo, Norway
Author for correspondence: Einar Timdal, einar.timdal@nhm.uio.no
Abstract
We have addressed phylogenetic relationships and tested hypotheses about five presumed subgroups among 15 species
of Hypocenomyce s.l. (including Pycnora) by use of nuclear (ITS, LSU) and mitochondrial (SSU) ribosomal DNA-regions.
Bayesian, likelihood and parsimony phylogenetic analyses, of a dataset with broad Lecanoromycete taxon sampling, mostly
support the five presumed subgroups, but two of these were found to be polyphyletic (the H. friesii-group and Pycnora). The
seven supported Hypocenomyce s.l. clades belong in different genera, families, orders and even subclasses, and represent
a remarkable example of morphological and ecological convergence. Based on our molecular phylogenetic results, we split
Hypocenomyce into four genera placed in two subclasses: (1) Carbonicola gen. nov. (Carbonicolaceae fam. nov., Lecanorales,
Lecanoromycetidae; includ ing C. anthracophila comb. nov., C. foveata comb. nov., and C. myrmecina comb. nov.); (2) Fulgidea
gen. nov. (Umbilicariaceae, Umbilicar iales, Umbilicariomycetidae subcl. nov.; including F. oligospora comb. nov. and F. sierrae
comb. nov.); (3) Hypocenomyce (Ophioparmaceae, Umbilicariales; including H. australis, H. scalaris, and H. tinderryensis; and
(4) Xylopsora gen. nov. (Umbilicariaceae; including X. caradocensis comb. nov. and X. friesii comb. nov.). We split Pycnora
into two genera: (1) Pycnora (Pycnoraceae fam. nov., Candelariales, “Candelariomycetidae”; including P. praestabilis, P. soro -
phora, and P. xanthococca); and (2) Toensbergia gen. nov. (Sporastatiaceae fam. nov., unknown order, Lecanoromycetidae;
including T. leucococca comb. nov.). We place Hypocenomyce isidiosa in Xylographa (Trapeliaceae, Baeomycetales, Ostropo-
mycetidae; X. isidiosa comb. nov.). We place the family Ophioparmaceae in the Umbilicariales. Our type studies have shown
that the epithet “myrmecina” should replace “castaneocinerea”, and lectotypes are chosen for Lecidea friesii Ach., L. scalaris
var. myrmecina Ach., Psora cladonioides va r. albocervina Räsänen, and P. cladonioides var. castaneocinerea Räsänen. Elixia
cretica is reported as new to North America (from Mexico) and Australia.
Keywords
burnt wood; Hypocenomyce; lecideoid lichens; molecular phylogenetics; polyphyly; taxonomy
Supplementary Material
The Electronic Supplement (Figs. S1 and S2) and the alignment files are available in the
Supplementary Data section of the online version of this article (http://www.ingentaconnect.com/content/iapt/tax).
Received: 20 Sep. 2012; revision received: 23 Apr. 2013; accepted: 28 Aug. 2013. DOI: http://dx.doi.org/10.12705/625.18
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Fig. 1.
A,
typical habitat, bur nt stump in boreal pine forest, Norway;
B,
Carbonicola anthracophila, Norway (O L-179442);
C,
C. foveata, Aus-
tralia (O L-50, holotype);
D,
C. myrmecina, Norway (O L-179443);
E,
Fulgidea oligospora, U.S.A. (O L-767, holotype);
F,
F. sierrae, U.S.A.
(O L-60059, holotype);
G,
Hypocenomyce australis, Australia, Elix 6153 (CAN B);
H,
H. scalaris, Sweden (O L-170870);
I,
Pycnora praestabilis,
Sweden (O L-144278);
J,
P. sorophora, Sweden (O L-144312);
K,
P. xanthococca, Norway (O L-149736);
L,
Toensbergia leucococca, Norway
(O L-170828);
M,
Xylographa isidiosa, Australia (CANB 737037-1, isotype);
N,
Xylopsora caradocensis, Norway (O L-73317);
O,
X. friesii,
Norway (O L-158541). ― Photos: E. Timdal.
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Table 1.
Morphological and chemical differences between the five Hypocenomyce species groups. Black dot means presence of the character, black
dot in brackets means that the character is rarely present, and questions mark means unknown.
Species group anthracophila friesii oligospora scalaris xanthococca
Additional species
castaneocinerea
foveata
caradocensis
isidiosa sierrae
australis
tinderryensis
leucococca
praestabilis
sorophora
Apothecia
brown, convex ●
black, plane ●●●●
Proper exciple
entirely conglutinated; hyphae thick-walled, with
thread-like lumina; inner part colorless; rim pale
brown; not containing crystals
●
entirely conglutinated, hyphae thin-walled, with
ellipsoid lumina; inner part and rim blackish brown;
not containing crystals
● ● ●
only partly conglutinated, hyphae thin-walled, with
ellipsoid lumina; inner part colorless; rim green;
containing crystals (lecanoric acid)
●
Epihymenium
brown, N− ● ● ●
green, N+ violet ● ●
without amorphous substances ● ●
with amorphous substances, effusion in K brown ● ●
with amorphous substances, effusion in K violet ●
Paraphyses
capitate, with an apical brown pigment cap ●
not capitate, without pigment cap ●●●●
Ascus
clavate, without cap; tholus with amyloid tube ●
clavate, without cap; tholus with lateral amyloid zone ●
rhombic, with apical cap; tholus small, deeply
amyloid ● ● ?
immature (●) ●
Pycnidum wall
brown, N− ● ● ●
green, N+ violet ● ●
Pycnoconinida
filiform ● ●
bacilliform (●) ● ● (●)
ellipsoid ● ●
subglobose ●
Main secondary compound
alectorialic acid ● ●
colensoic acid ●
friesiic and/or confriesiic acid ●
lecanoric acid ●
thamnolic acid ●
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Taxonomic history. —
Hypocenomyce was introduced
by Choisy (1951) for the single species H. scalaris which had
been placed in Lecidea Ach. sect. Psora (Hoffm.) Schaer. by
Zahlbruckner (1925, as Lecidea ostreata (Hoffm.) Scha er.) The
genus was originally characterized by having a squamulose
thallus, lecideine, adnate apothecia and short, straight, cylin-
drical pycnoconidia. Choisy (1953) later also included H. rubi-
formis (Ach.) M. Choisy in the genus; a species which is now
regarded as belonging in Psora Hoffm. (as P. rubiformis (Ach .)
Hook., cf. Timdal, 1984b; Ekman & Blaalid, 2011) and is not
discussed further in this paper.
Schneider (1980) proposed a new generic arrangement for
the species placed in Lecidea sect. Psora sensu Zahlbruckner.
He accepted Hypocenomyce and added two more squamu-
lose species to it, H. anthracophila (Nyl.) P. James & Gotth.
Schneid. and H. friesii. Three more species were soon added,
one transferred from Toninia A. Massal. (H. caradocensis
(Nyl.) P. James & Gotth. Schneid. in Hawksworth & al., 1980)
and two crustose species from Lecidea sect. Lecidea sensu
Zahlbruckner (H. xanthococca (Sommerf.) P. James & Gotth.
Schneid. in Hawksworth & al., 1980, and H. sorophora (Va in.)
P. James & Poelt in Poelt & Vĕzda, 1981).
Timdal (1984a) revised Hypocenomyce and added four
more species to it (H. australis Timdal, H. castaneocinerea
(Räsänen) Timdal, H. foveata Timdal, and H. praestabilis
(Nyl.) Timdal). He recognized four groups of species within
the genus, based on anatomical and chemical characters:
the H. anthracophila-, H. friesii-, H. scalaris- and H. xan-
thococca-groups (Table 1). The characters uniting the four
groups were found to be mainly morphological (thallus) and
ecological, and he expressed doubts about the homogeneity
of the genus.
Abassi Maaf & Roux (1984) described H. stoechadiana
Abassi & Cl. Roux, but that species is now placed in Waynea
Moberg (Roux & Clerc, 1991) and is not treated further here.
Santesson (in Moberg, 1986) described H. leucococca R. Sant.
from sterile material, and its inclusion in Hypocenomyce seems
to have been based on its general resemblance in morphol-
ogy, secondary chemistry and ecology with species of the
H. xanthococca-group. Hafellner (1993) placed H. anthracoph-
ila and H. foveata in the genus Biatora Fr., a view that was not
supported by Printzen (1995) in his revision of the European
species of Biatora. As mentioned above, Hafellner (in Hafellner
& Türk, 2001) raised the H. xanthococca-group to the level
of genus, but no new data were presented to support this ar-
rangement and we hence include Pycnora in this study. Timdal
(2001) described two new species (Hypocenomyce oligospora
Timdal and H. sierrae Timdal) which in morphological (thallus
shape) and anatomical (apothecial pigments, proper exciple,
ascus type) characters seemed to bridge the H. friesii- and
H. scalaris-groups and also shared the secondary chemistry
(alectorialic acid) with the H. xanthococca-group. The two
species are here regarded as representing a fifth group, the
H. oligospora-group. Finally, Elix (2006, 2007) described two
new species from Australia, H. isidiosa Elix and H. tinderryen-
sis Elix, which may be placed in the H. friesii- and H. scalaris-
groups, respectively.
Aims. —
Our aim with the present study was to test
whether the suggested five species groups are supported by
DNA sequence data, and to reveal their phylogeny. The mo-
lecular phylogenetic study of Wedin & al. (2005) only included
two Hypocenomyce and two Pycnora species, which repre-
sent three of the five presumed Hypocenomyce s.l. subgroups.
In the present study, we included DNA sequences data of all
currently recognized species of Hypocenomyce (11 spp.) and
Pycnora (4 spp.), some presumed relatives, and a broad taxon
sampling of the entire Lecanoromycetes (the latter sequences
obtained from public databases). Based on our molecular phy-
logenetic results, we propose several taxonomic and nomen-
clatural changes.
MATERIALS AND METHODS
Taxon sampling. —
For this molecular phylogenetic
and taxonomic study of Hypocenomyce, we used herbarium
specimens of varying age (up to 45 years old) held at the fol-
lowing herbaria: ASU, CANB, O, and S. The Hypocenomyce
s.l. specimens studied originated from Australia, Norway,
Russia, Sweden and the U.S.A. We have extracted DNA from
multiple specimens of all Hypocenomyce s.l. species (41 ac-
cessions in total) as well as selected species relevant for the
phylogenetic placement of Hypocenomyce (i.e., Biatora: 1,
Catillaria A. Massal.: 1, Elixia Lumbsch: 5, Ophioparma: 3,
and Xylographa (Fr.) Fr.: 3). These numbers include four col-
lections presumed to belong in Hypocenomyce (collected and
sequenced as Hypocenomyce sp.), but, based on the DNA se-
quences, later identified as Elixia cretica T. Sprib. & Lumbsch
(E. cretica, specimens 1 and 2) and a possibly new species of
Elixia (Elixia sp., specimens 1 and 2). We generated 113 DNA
sequences of the nuclear ribosomal internal transcribed spacer
region (nrITS: ITS1, 5.8S, ITS2) and large subunit (nrLSU;
partial), and the mitochondrial small subunit (mtSSU; partial).
Corresponding sequences of additional taxa (covering most
relevant Lecanoromycete taxa from family level and above)
were obtained from GenBank. We have, mostly during pre-
vious studies, examined the morphology and the secondary
chemistry of type specimens of all currently accepted species
of Hypocenomyce s.l. with the exception of H. scalaris which
has never been typified. Thin-layer chromatography (TLC)
was performed in accordance with the methods of Culberson
(1972), modified by Menlove (1974) and Culberson & Johnson
(1982). See Appendix 1 for voucher information for all DNA
extracted specimens.
DNA extraction. —
We crushed up to 5 mg of tissue (apo-
thecia, if present) from 54 archived specimens in 2 mL plastic
tubes with two tungsten carbide beads in each for 2 × 1.5 min
at 23 Hz on a mixer mill (MM301, Retsch GmbH & Co., Haan,
Germany). We extracted total DNA from the crushed samples
using the E.Z.N.A SP Plant DNA Mini Kit (Omega Bio-tek,
Inc., Norcross, Georgia, U.S.A.) according to the manufacturer’s
manual. We performed additional steps related to the elution
for increasing DNA yield (as suggested in the manual), such as
eluting twice, using the first eluate also the second time, and
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pre-warming to 65°C for 5 min prior to spinning. We deposited
all DNA aliquots used in the present study in the DNA tissue
collection at The Natural History Museum, Oslo (O).
PCR amplification and DNA sequencing. —
We a mpl ifie d
DNA in 25 µL reactions
using the AmpliTaq GOLD DNA
polymerase buffer II kit (Applied Biosystems, Foster City,
California, U.S.A.) containing 0.2 mM of each dNTP, 0.04%
bovine serum albumen (BSA), 0.01 mM tetramethylammo-
nium chloride (TMACl), 0.4 μM of each primer, and 2 μL
unquantified genomic DNA. We performed all amplifications
in a GeneAmp PCR System 9700 (Applied Biosystems)
using
the following cycling conditions: 95°C for 10 min, 32 (nrITS,
nrLSU) or 34 (mtSSU) cycles of 95°C for 30 s, 60°C for 30 s,
72°C for 1 min, followed by 72°C for 10 min and hold forever at
10°C. For DNA extracts that would not amplify using the above
described approach, we amplified shorter fragments or used the
replicate procedure described in Bendiksby & al. (2011). We de-
signed 10 primers for the present study. All primers, which we
used in various combinations and both as PCR and sequencing
primers, are listed with references in Table 2. We purified the
PCR products using 2 µL 10 times diluted ExoSAP-IT (USB
Corporation, Santa Clara, California, U.S.A.) to 8 µL PCR
product, incubating at 37°C for 45 min followed by 15 min
at 80°C. Prepared amplicons for sequencing contained: 9
μL
0–30× diluted purified PCR product (depending on product
strength) and 1
μL of 10 μM primer
. Cycle sequencing was
outsourced to the ABI laboratory at the Centre for Ecological
and Evolutionary Synthesis, Department of Biology, Univer-
sity of Oslo, where the ABI BigDye Terminator sequencing
buffer and v.3.1 Cycle Sequencing kit (Applied Biosystems)
are used. Sequences
were processed
on an ABI 3730 DNA
analyser (Applied Biosystems). We assembled and edited the
sequences using SEQUENCHER v.4.1.4 (Gene Codes Corpo-
ration, Ann Arbor, Michigan, U.S.A.). See Appendix 1 for the
GenBank accession numbers of all sequences included in the
present study.
Alignment and phylogeny reconstructions. —
We aligned
the sequences using the “ClustalW/Multiple alignment” op-
tion in BioEdit v.7.0.9.0 (Hall, 1999) with subsequent manual
adjustments. We analyzed the data using maximum likelihood,
maximum parsimony and Bayesian inference phylogenetic
methods. In order to check for gene-tree incongruence, we
compared preliminary strict consensus trees from parsimony
analyses of the three genetic regions. For selecting optimal
models of nucleotide substitution for the various markers we
used TreeFinder (Jobb & al., 2004). We performed maximum
parsimony phylogenetic analyses using TNT (Goloboff & al.,
2008) applying the traditional search option with equal char-
acter weights, gaps treated as missing (replaced with question
marks prior to analysis), 1000 random entry order replicates
saving 10 trees per replicate, and tree bisection reconnection
(TBR) branch swapping. We performed parsimony jackknif-
ing with 1000 replicates. We also did maximum likelihood
bootstrapping (BS) using RAxML v.7.2.6 (Stamatakis, 2006)
under the GTRCAT model with 500 replicates. For the BI
phylogenetic analyses we used MrBayes v.3.2.1 (Huelsenbeck
& Ronquist, 2001; Ronquist & Huelsenbeck, 2003) with priors
set according to the output of TreeFinder. We determined pos-
terior probabilities by running one cold and three heated chains
for 12 to 20 million generations in parallel mode (the 134 and
166 accessions datasets, respectively, see below), saving trees
every 1000th generation. We performed the analyses twice to
check their convergence for the same topology. To test whether
the Markov Chain converged, we monitored the average stan-
dard deviation of split frequencies (ASDSF), which should fall
below 0.01 when comparing two independent runs. We dis-
carded as burn-in the generations prior to the point where the
ASDSF fell below 0.01 and summarized the remaining trees
Table 2.
List of primers used in the present study with primer sequence and references.
DNA region Primer name / primer sequence 5′ → 3′ direction Reference
nrITS ITS4 / TCCTCCGCTTATTGATATGC (rev) White & al., 1990
ITS5 / GGAAGTAAAAGTCGTAACAAGG(fwd) White & al., 1990
ITS6 / TAAGTTCAGCGGGTATCCCTA (rev) This study
ITS-lichF / TGAATTGCAGAATTCAGTGAAT (fwd) This study
ITS-lichR / ATTCACTGAATTCTGCAATTCA (rev) This study
ITS-hypF / TCTTTGAACGCACATTGCGCC (fwd) This study
ITS-hypR / GGCGCAATGTGCGTTCAAAGA (rev) This study
nrLSU LSU-hypF / CGCTGAACTTAAGCATATC (fwd) This study
LSU-hypR / CTATCCTGAGGGAAACTTCG (rev) This study
LSU-hypR2 / CTTGGTCCGTGTTTCAAGACG (rev) This study
mtSSU mitSSU1 / AGCAGTGAGGAATATTGGTC (fwd) Zoller & al., 1999
mitSSU3R / ATGTGGCACGTCTATAGCCC (rev) Zoller & al., 1999
mtSSU-hypF / AGCATTCCACCTCAAGAGTA (rev) This study
mtSSU-hypR / TACTCTTGAGGTGGAATGCT (rev) This study
Abbreviations: nrITS = nuclear ribosomal internal transcribed spacer; nrLSU = nuclear ribosomal large
subunit; mtSSU = mitochondrial ribosomal small subunit; rev = reverse primer; fwd = forward primer.
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as a 50% majority-rule consensus tree. We used the Bioportal
server, University of Oslo, Norway (http://www.bioportal.uio
.no) for the RAxML analyses.
RES U LT S
Sequences and alignments. —
DNA sequences of all
three genetic regions (nrITS, nrLSU, mtSSU) were success-
fully generated for most of the specimens extracted for this
study, except for a few old and/or poor-quality specimens, from
which only the nrITS region (or parts of it) could be amplified
and sequenced using the methods described herein. GenBank
sequences of the three genetic regions were always based on the
same voucher specimen. The highly variable ITS1 of the nrITS
region was treated as missing data for accessions for which
character homology could not be hypothesized (indicated with
†
in Appendix 1). Lengths in basepairs (bp) of the aligned DNA-
regions were: 650 bp for the nrITS region, 905 bp for the nrLSU
region, and 1037 bp for the mtSSU region. The best-fit nucleo-
tide substitution models, as proposed by TreeFinder based on
the AICc model selection criterion, were general time reversible
with gamma distribution (GTR + G) for the nrLSU and mtSSU
regions and J2 + G for the nrITS region. As no manual exists for
implementing the J2 + G model in MrBayes, the GTR + G model
was used for all three regions. The concatenated matrix of 2592
bp contained 1186 parsimony-informative characters.
Analyses. —
The preliminary parsimony analyses showed
congruent gene trees, although resolved to various extents and
at different levels (not shown). The nrITS increased resolution
of the more recent speciation events, whereas the mtSSU and
nrLSU provided resolution of the backbone relationships. The
nrLSU was less informative than the mtSSU. We therefore ana-
lyzed a concatenated dataset of all three genetic regions (nrITS,
nrLSU, mtSSU), 166 accessions, and 2592 bp (hereafter re-
ferred to as the 166 accession dataset). In the Bayesian analysis,
the ASDSF had fallen to 0.004683 at termination (20 million
generations), and the first 5000 trees (25%) were discarded as
burn-in. The remaining trees were summarized as a Bayesian
50% majority-rule consensus tree, which is presented in Fig. 2.
Since the ITS1 and ITS2 of the nrITS region included several
alignment ambiguities, we also performed a Bayesian analysis
of a dataset consisting of only the more conserved 5.8S part of
the nrITS region in combination with the nrLSU and mtSSU re-
gions. This dataset included 134 accessions (only accessions for
which the mtSSU region was available) and 2081 bp (hereafter
referred to as the 134 accession dataset). At 12 million genera-
tions, the ASDSF had fallen to 0.004653, and the analysis was
terminated. We discarded as burn-in the first 3000 trees (50%),
and summarized the remaining trees into a 50% majority-rule
consensus tree (Electr. Suppl.: Fig. S1). The parsimony strict
and jackknife consensus trees with tree statistics for both data-
sets are provided in the Electr. Suppl.: Fig. S2. The parsimony
results were largely consistent with the Bayesian and likelihood
results, and the resultant topologies from the 166 vs. the 134
accession datasets were highly similar (Fig. 2; Electr. Suppl.:
Figs. S1–S2).
The 15 included species of Hypocenomyce s.l. form
seven strongly supported groups in our molecular phylog-
eny (Fig. 2; Electr. Suppl.: Figs. S1–S2). Through nucleotide
BLAST searches at NCBI (http://www.ncbi.nlm.nih.gov/), it
became clear that the seven groups were far from being each
other’s closest relatives, and a broad taxonomic sampling had
to be included in order to place these groups phylogenetically.
The resultant phylogeny shows that the Hypocenomyce species
belong in different families, orders and even different sub-
classes (Fig. 2).
The backbone of the phylogeny (the oldest speciation
events) received poor support from parsimony jackknifing
(Electr. Suppl.: Fig. S2), and the parsimony strict consensus
trees were partly incongruent with the Bayesian majority-rule
trees (Fig. 2; Electr. Suppl.: Fig. S1). The incongruences (indi-
cated with asterisks on Fig. 2) mainly concerned long-branch
taxa in the Ostropomycetidae and the Lecanoromycetidae. The
backbone support was generally higher with likelihood boot-
strapping (Fig. 2).
See the Discussion for other relevant aspects of our phy-
logenetic results.
The concatenated alignment of 166 accessions and three
genetic regions and the resultant Bayesian phylogenetic tree
are provided as supplementary material.
DISCUSSION
Although Hypocenomyce s.l. (including Pycnora) has been
extensively studied by anatomical and chemical approaches
(e.g., Timdal, 1984a, 2001, 2002; Elix, 2009), the present study
is the first comprehensive molecular phylogenetic investiga-
tion of the genus. Our aim has been to investigate phylogenetic
relationships among the 15 species of Hypocenomyce s.l. and
to test hypotheses about the presumed groups among them
(Table 1).
Our phylogenetic results (Fig. 2), based on three DNA re-
gions of various levels of molecular divergence from two dif-
ferent genomes and with a broad taxonomic sampling, reveal
that Hypocenomyce s.l. is extremely polyphyletic. Although the
backbone of the phylogeny (the oldest speciation events) mostly
receives moderate support from likelihood bootstrapping
(Fig. 2) and parsimony jackknifing (Electr. Suppl.: Fig. S2),
the Bayesian majority-rule consensus topology (Fig. 2) cor-
responds well with all recently published phylogenetic hypoth-
esis (Wedin & al., 2005; Miądlikowska & al., 2006; Hofstetter
& al., 2007; Lumbsch & al., 2007; Ekman & al., 2008; Schoch
& al., 2009; Schmull & al., 2011) that have included similar
sets of taxa, but without the present extensive sampling of
Hypocenomyce s.l. The five presumed subgroups (see Intro-
duction and Table 1) are mostly supported by our molecular
data, but two species, H. isidiosa and P. leucococca, form in-
dependent groups remotely positioned from any of the other
groups (Fig. 2B). The resultant seven subgroups are surpris-
ingly distantly related and clearly belong in different genera,
families, orders and even subclasses. Further below, we dis-
cuss the Hypocenomyce subgroups and their phylogeny, and we
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946 Version of Record (identical to print version).
undertake several taxonomic changes that are now supported
by multiple sources of evidence. In the following paragraph,
“Morphological convergence”, we use the new taxonomy pro-
posed (see Nomenclatural novelties for author names).
Morphological convergence. —
Traditional classifications
are based largely on morphological and ecological aspects of
organisms. Since the early 1990s, molecular phylogenetics
has revolutionized the field of systematics, in particular in the
0.09
Elixia cretica 1 MEXICO
Fuscidea mollis
H. sorophora 4
Umbilicaria proboscidea
H. australis 2
Ophioparma ventosa 1
Myriospora smaragdula
H. xanthococca 2
H. sierrae 1
H. praestabilis 1
Elixia cretica 3 CRETE (holotype)
Elixia flexella 2
H. oligospora 4
Elixia flexella 3
H. sorophora 3
Candelariella coralliza
H. caradocensis 1
H. oligospora 1(holotype)
H. xanthococca 1
H. scalaris 4
Candelariella aurella
H. scalaris 3
H. oligospora 3
H. oligospora 2
Boreoplaca ultrafrigida (holotype)
Elixia sp. 2 U.S.A.
Umbilicaria aprina
Maronea constans
H. tinderryensis 5
Lasallia pustulata
H. tinderryensis 3
H. friesii 3
H. xanthococca 3
Ophioparma lapponica
H. scalaris 5
Elixia cretica 1 AUSTRALIA
H. tinderryensis 2
H. praestabilis 2
H. friesii 4
H. scalaris 2
Candelariella vitellina
H. caradocensis 2
Geoglossum nigritum
Umbilicaria africana
Candelariella reflexa
Candelariella terrigena
Ophioparma ventosa 2
H. friesii 2
H. australis 3(isotype)
H. australis 1
H. tinderryensis 4(holotype)
H. caradocensis 3
Meridianelia maccarthyana (isotype)
H. scalaris 1
Pleopsidium flavum
H. sorophora 5
Candelaria concolor
Elixia flexella 1
Elixia sp. 1 U.S.A.
H. sorophora 1
H. tinderryensis 1
Acarospora peliscypha
Pleopsidium gobiense
H. friesii 1
Umbilicaria spodochroa
Umbilicaria crustulosa
H. australis 4
Ophioparma handelii
Lasallia pennsylvanica
H. sorophora 2
Sarcogyne privigna
H. sierrae 2(holotype)
1
1
1
.95
1
1
1
1
1
1
1
.98
1
.96
.97
.98
1
1
1
1
1
.99
1
1
1
1
1
1
1
1
.97
1
.97
1
1
.92
1
1
.97
1
1
1
.9
1
1
1
1
1
1
100
59
94
100
100
100
100
100
98
85
92
96
96
58
98
74
86
97
98
98
100
58
97
97
89
100
68
92
91
75
90
77
77
74
65
100
100
98
96
100
99
100
82
100
95 100
100
78
93
63
67
54
91
100
Xylopsora gen. nov.
Fulgidea gen. nov.
Umbilicariaceae
Hypocenomyce
Ophioparmaceae
Fuscideaceae
Acarosporaceae
Pycnora Pycnoraceae
fam. nov.
Candelariaceae
Fig. 2A (for Fig. 2B
see next page)
Aca
.
Candelariales
i.s.
Umbilicariales
Acarosporomycedae →
“Candelariomycedae”
(sensu Miądlikowska & al., 2006)
→
Umbilicariomycedae subcl. nov. →
Elixiaceae
Fig. 2.
The 50% majority-rule consensus phylogram (
2A
above,
2B
next page) from a Bayesian analysis of a concatenated matrix with 166
accessions and 2592 basepairs from two nuclear (ITS and LSU) and one mitochondrial (SSU) ribosomal DNA region. The Bayesian posterior
probability values of at least 0.9 are reported above branches, and maximum likelihood bootstrap values of at least 50% are reported below
branches. Asterisks indicate incongruent topology with parsimony results (see Electr. Suppl.: Fig. S2). Multiple accessions of the same species
are numbered according to Appendix 1. The Hypocenomyce s.l. accessions are in bold. One branch was manually shortened to reduce the size
of a broad figure (indicated with a black dot). Names to the right of branches indicate the classification as supported herein. Taxonomic changes
undertaken in the present study from genus and above are also in bold face. — Aca., Acarosporales; i.s., incertae sedis; Ost., Ostropales; Pel.,
Peltigerales; Tel ., Teloschistales.
0.09
Elixia cretica 1 MEXICO
Fuscidea mollis
H. sorophora 4
Umbilicaria proboscidea
H. australis 2
Ophioparma ventosa 1
Myriospora smaragdula
H. xanthococca 2
H. sierrae 1
H. praestabilis 1
Elixia cretica 3 CRETE (holotype)
Elixia flexella 2
H. oligospora 4
Elixia flexella 3
H. sorophora 3
Candelariella coralliza
H. caradocensis 1
H. oligospora 1(holotype)
H. xanthococca 1
H. scalaris 4
Candelariella aurella
H. scalaris 3
H. oligospora 3
H. oligospora 2
Boreoplaca ultrafrigida (holotype)
Elixia sp. 2 U.S.A.
Umbilicaria aprina
Maronea constans
H. tinderryensis 5
Lasallia pustulata
H. tinderryensis 3
H. friesii 3
H. xanthococca 3
Ophioparma lapponica
H. scalaris 5
Elixia cretica 1 AUSTRALIA
H. tinderryensis 2
H. praestabilis 2
H. friesii 4
H. scalaris 2
Candelariella vitellina
H. caradocensis 2
Geoglossum nigritum
Umbilicaria africana
Candelariella reflexa
Candelariella terrigena
Ophioparma ventosa 2
H. friesii 2
H. australis 3(isotype)
H. australis 1
H. tinderryensis 4(holotype)
H. caradocensis 3
Meridianelia maccarthyana (isotype)
H. scalaris 1
Pleopsidium flavum
H. sorophora 5
Candelaria concolor
Elixia flexella 1
Elixia sp. 1 U.S.A.
H. sorophora 1
H. tinderryensis 1
Acarospora peliscypha
Pleopsidium gobiense
H. friesii 1
Umbilicaria spodochroa
Umbilicaria crustulosa
H. australis 4
Ophioparma handelii
Lasallia pennsylvanica
H. sorophora 2
Sarcogyne privigna
H. sierrae 2(holotype)
1
1
1
.95
1
1
1
1
1
1
1
.98
1
.96
.97
.98
1
1
1
1
1
.99
1
1
1
1
1
1
1
1
.97
1
.97
1
1
.92
1
1
.97
1
1
1
.9
1
1
1
1
1
1
100
59
94
100
100
100
100
100
98
85
92
96
96
58
98
74
86
97
98
98
100
58
97
97
89
100
68
92
91
75
90
77
77
74
65
100
100
98
96
100
99
100
82
100
95 100
100
78
93
63
67
54
91
100
Xylopsora gen. nov.
Fulgidea gen. nov.
Umbilicariaceae
Hypocenomyce
Ophioparmaceae
Fuscideaceae
Acarosporaceae
Pycnora Pycnoraceae
fam. nov.
Candelariaceae
Aca
.
Candelariales
i.s.
Umbilicariales
Acarosporomycedae →
→
Umbilicariomycedae subcl. nov. →
Elixiaceae
“Candelariomycedae”
(sensu Miądlikowska & al., 2006)
Fig. 2A (for Fig. 2B
see next page)
947
Bendiksby & Timdal • Polyphyletic Hypocenomyce
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62 (5) • October 2013: 940–956
947Version of Record (identical to print version).
Megasporaceae
Arctomiaceae
Baeomycetaceae
Rhizocarpaceae
H. leucococca 2
Ainoa mooreana
H. castaneocinerea 2
Baeomyces rufus
Neophyllis melacarpa
Xylographa trunciseda
Pertusaria dactylina (Pertusariaceae II)
H. leucococca 1
Thelotrema suecicum
H. foveata
Catillaria chalybeia
Stereocaulon paschale
Ramalina complanata
Arctomia delicatula
Catolechia wahlenbergii
H. anthracophila 3
Scoliciosporum umbrinum (Scoliciosporaceae)
Haematomma ochroleucum
Crocynia pyxinoides
Porpidia macrocarpa
Sporastatia polyspora
Coccotrema cucurbitula (Coccotremataceae)
Miltidea ceroplasta (Miltideaceae)
Cladonia rangiferina
Wawea fruticulosa
Ochrolechia parella (Ochrolechiaceae)
H. isidiosa 1(isotype)
Ptychographa xylographoides
H. castaneocinerea 1
Xylographa opegraphella
Toninia sedifolia
Tremolecia atrata
H. isidiosa 2
Hymenelia lacustris
Orceolina kerguelensis
Loxospora ochrophaea (Sarrameniaceae)
Trapeliopsis granulosa*
Bacidia rubella
Xylographa soralifera
Psilolechia leprosa
Pyrrhospora quernea
Myelochroa aurulenta
Lecanora sulphurea
Psora decipiens
Bryoria capillaris
Teloschistes flavicans
Protoblastenia rupestris
Biatora vernalis
Lecidea atrobrunnea
H. anthracophila 4
Lobothallia radiosa
Lecidella euphorea
Schaereria fuscocinerea (Schaereriaceae)
Pilophorus strumaticus*
Agyrium rufum (Agyriaceae)
Megalaria grossa
Protothelenella sphinctrinoidella (Protothel enellaceae)
Rhizocarpon oederi
Evernia prunastri
Porpidia speirea
Solenopsora holophaea
Placynthiella uliginosa*
Lopadium disciforme (i.s.)
Lecidea tessellata
Lecanora carpinea
Gypsoplaca macrophylla (Gypsoplacaceae)
Diploschistes scruposus
Lecanora polytropa
Xylographa parallela
Mycoblastus sanguinarius
Placopsis santessonii
Thamnolia vermicularis (Icmadophilaceae)
Xanthoria parietina
Aspicilia cinerea
Metus conglomeratus
Micarea adnata
Pertusaria leioplaca (Pertisariaceae I)
Sphaerophorus globosus
Cladia retipora
Rhizoplaca chrysoleuca
Lepraria lobificans
Sporastatia testudinea
Nephroma arcticum (Nephromelataceae)
Parmelina quercina
Gregorella humida
Heterodea muelleri
H. anthracophila 1
Trapelia placodioides
Tephromela atra
Calopadia sp.
Graphis scripta
H. anthracophila 2
Rimularia psephota
Peltigera praetextata (Peltigeraceae)
1
1
1
1
1
1
1
.99
1
1
1
1
1
1
1
1
.92
.96
1
1
1
.97
1
1
1
.99
1
1
1
.97
1
1
1
1
1
1.93
.91
1
.94
1
1
.92
1
.99
.93
1
1
.92
.99
1
1
1
1
1
1
.96
1
1
1
1
1
1
1
1
1
1
1
1
1
0.09
Trapeliaceae
Lecanorales Baeomycetales
Carbonicolaceae
fam. nov.
Os
t.
Pertusariales
Callariaceae
Pel.
Tel.
Pilocarpaceae
Sphaerophoraceae
Psoraceae
Ramalinaceae
Mycoblastaceae
Parmeliaceae
Lecanoraceae
Stereocaulaceae
Cladoniaceae
Lecideaceae
Teloschistaceae
Hymeneliaceae (i.s.)
Graphidaceae
i.s.
Sporastaaceae
fam.nov.
Carbonicola gen. nov.
for Fig. 2A
see previous page
Toensbergia g en. nov.
Xylographa
i.s.
i.s.
Lecanoromycedae → Ostropomycedae →
60
63
100
100
83
99
84
100
71
96
100
68
95
97
100100
85
64
70
69
99
100
95 67
82
80
92
96
100
83
100
84
93
99
52
100
97
95
83
62
56
59
73
67
86
97
92
100
100
92
72
100
97
100
100
97
87
98
85 99
Fig. 2B
Megasporaceae
Arctomiaceae
Baeomycetaceae
Rhizocarpaceae
H. leucococca 2
Ainoa mooreana
H. castaneocinerea 2
Baeomyces rufus
Neophyllis melacarpa
Xylographa trunciseda
Pertusaria dactylina (Pertusariaceae II)
H. leucococca 1
Thelotrema suecicum
H. foveata
Catillaria chalybeia
Stereocaulon paschale
Ramalina complanata
Arctomia delicatula
Catolechia wahlenbergii
H. anthracophila 3
Scoliciosporum umbrinum (Scoliciosporaceae)
Haematomma ochroleucum
Crocynia pyxinoides
Porpidia macrocarpa
Sporastatia polyspora
Coccotrema cucurbitula (Coccotremataceae)
Miltidea ceroplasta (Miltideaceae)
Cladonia rangiferina
Wawea fruticulosa
Ochrolechia parella (Ochrolechiaceae)
H. isidiosa 1(isotype)
Ptychographa xylographoides
H. castaneocinerea 1
Xylographa opegraphella
Toninia sedifolia
Tremolecia atrata
H. isidiosa 2
Hymenelia lacustris
Orceolina kerguelensis
Loxospora ochrophaea (Sarrameniaceae)
Trapeliopsis granulosa*
Bacidia rubella
Xylographa soralifera
Psilolechia leprosa
Pyrrhospora quernea
Myelochroa aurulenta
Lecanora sulphurea
Psora decipiens
Bryoria capillaris
Teloschistes flavicans
Protoblastenia rupestris
Biatora vernalis
Lecidea atrobrunnea
H. anthracophila 4
Lobothallia radiosa
Lecidella euphorea
Schaereria fuscocinerea (Schaereriaceae)
Pilophorus strumaticus*
Agyrium rufum (Agyriaceae)
Megalaria grossa
Protothelenella sphinctrinoidella (Protothel enellaceae)
Rhizocarpon oederi
Evernia prunastri
Porpidia speirea
Solenopsora holophaea
Placynthiella uliginosa*
Lopadium disciforme (i.s.)
Lecidea tessellata
Lecanora carpinea
Gypsoplaca macrophylla (Gypsoplacaceae)
Diploschistes scruposus
Lecanora polytropa
Xylographa parallela
Mycoblastus sanguinarius
Placopsis santessonii
Thamnolia vermicularis (Icmadophilaceae)
Xanthoria parietina
Aspicilia cinerea
Metus conglomeratus
Micarea adnata
Pertusaria leioplaca (Pertisariaceae I)
Sphaerophorus globosus
Cladia retipora
Rhizoplaca chrysoleuca
Lepraria lobificans
Sporastatia testudinea
Nephroma arcticum (Nephromelataceae)
Parmelina quercina
Gregorella humida
Heterodea muelleri
H. anthracophila 1
Trapelia placodioides
Tephromela atra
Calopadia sp.
Graphis scripta
H. anthracophila 2
Rimularia psephota
Peltigera praetextata (Peltigeraceae)
1
1
1
1
1
1
1
.99
1
1
1
1
1
1
1
1
.92
.96
1
1
1
.97
1
1
1
.99
1
1
1
.97
1
1
1
1
1
1.93
.91
1
.94
1
1
.92
1
.99
.93
1
1
.92
.99
1
1
1
1
1
1
.96
1
1
1
1
1
1
1
1
1
1
1
1
1
Trapeliaceae
Lecanorales Baeomycetales
Carbonicolaceae
fam. nov.
Os
t.
Pertusariales
Callariaceae
Pel.
Tel.
Pilocarpaceae
Sphaerophoraceae
Psoraceae
Ramalinaceae
Mycoblastaceae
Parmeliaceae
Lecanoraceae
Stereocaulaceae
Cladoniaceae
Lecideaceae
Teloschistaceae
Hymeneliaceae (i.s.)
Graphidaceae
i.s.
Sporastaaceae
fam.nov.
Carbonicola gen. nov.
Toensbergia gen. nov.
Xylographa
i.s.
i.s.
Lecanoromycedae → Ostropomycedae →
60
63
100
100
83
99
84
100
71
96
100
68
95
97
100100
85
64
70
69
99
100
95 67
82
80
92
96
100
83
100
84
93
99
52
100
97
95
83
62
56
59
73
67
86
97
92
100
100
92
72
100
97
100
100
97
87
98
85 99
0.09
for Fig. 2A
see previous page
Fig. 2B
948
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948 Version of Record (identical to print version).
most taxonomically challenging groups. Fungi (incl. lichenized
fungi) represent one such taxonomically challenging group due
to few phenotypic characters and a high level of homoplasy.
Hence, fungal molecular phylogenies have resulted in numer-
ous novel classifications (e.g., Lutzoni & al., 2004; James & al.,
2006; Miądlikowska & al., 2006; Hibbet & al., 2007; Schoch
& al., 2009) and revealed numerous instances of convergent
evolution (see Rivas Plata & Lumbsch, 2011, and references
therein; Rivas Plata & al., 2012).
Our phylogeny shows that the great morphological and
ecological similarity between the former Hypocenomyce spe-
cies is the result of convergence in seven clades. Brown, squa-
mulose thalli, often geotropically arranged and with lip-shaped
soralia, occur in Carbonicola, Hypocenomyce, Fulgidea, and
Xylopsora. Ten species in five clades occur on burnt wood (Car-
bonicola, all species; Fulgidea, all species; Hypocenomyce, all
species; Xylographa isidiosa; and Xylopsora friesii). We have
observed that very few crustose lichen species grow on burnt
wood in northern Europe. In addition to Hypocenomyce, these
are mainly Chaenotheca ferruginea (Sm.) Mig., Hertelidea
botryosa (Fr.) Printzen & Kantvilas, Micarea melaenida ( Nyl.)
Hedl., and Trapeliopsis flexuosa (Fr.) Coppins & P. James. The
presence of four clades containing such ecological specialists
in the Umbilicariales (Elixia, Fulgidea, Hypocenomyce, Xylo-
psora) may be explained as a plesiomorphy in this order, in
which case the saxicolous genera Boreoplaca, Lasallia Mérat,
and Umbilicaria have evolved from ancestors growing on burnt
wood. Alternatively, the specialized ecology is a homoplasy
and evolved up to four times in the order, or the topology in
our Umbilicariales phylogeny does not correctly reflect the
evolution of the four clades.
Abundant production of apparently persistently immature
asci occurs in Hypocenomyce (all three species) and Fulgidea
(F. oligospora), and must be a homoplasy of the two genera.
The selective forces behind this character state remain obscure.
In H. scalaris and H. tinderryensis it may be viewed as an
incomplete step in reduction of fertility as a response to the
species having switched to vegetative dispersal (soredia), but in
the two other species (H. australis, F. oligos pora) no vegetative
dispersal units are produced and they should rely only on as-
cospore dispersal. We suggest an ecological study of the effect
of heat from forest fire on spore production in those species.
The chemical similarity between Pycnora and Toe n s -
bergia (alectorialic acid) and between Xylopsora and Xylogra-
pha isidiosa (confriesiic/friesiic acids) are clearly homoplasies.
The Hypocenomyceanthracophila-group. —
There are
no previously published sequences or phylogenies of spe-
cies in this group. In our results (Fig. 2B; Electr. Suppl.: Figs.
S1–S2), the three species comprising the H. anthracophila-
group (H. anthracophila, H. castaneocinerea, H. foveata)
form a monophyletic clade within the order Lecanorales. The
H. anthracophila-group clearly does not belong in any of the
lecanoralean families included in the present phylogeny (i.e.,
Catillariaceae, Cladoniaceae, Gypsoplacaceae, Haematommat-
aceae, Lecanoraceae, Mycoblastaceae, Parmeliaceae, Pilo carp-
aceae, Psoraceae, Ramalinaceae, Scoliciosporaceae, Sphaero-
phoraceae, Stereocaulaceae). We do not have sequence data for
the remaining currently accepted families of the Lecanorales
(Biatorellaceae, Calycidiaceae, Dactylospor aceae, Pachyasca-
ceae). However, judging from anatomical characters, especially
the ascus type, the H. anthracophila-group does not belong
in any of these families. In the Biatorellaceae, the asci are
polysporous and have a well-developed, weakly amyloid tho-
lus which lacks an amyloid tube (Hafellner & Casares-Porcel,
1992). In the Pachyascaceae, the asci are surrounded by a thick,
amyloid gelatinous wall; a small, weakly amyloid tholus, appar-
ently without any tube structure, may be developed in young
asci (Grube, 2002). In the Calycidiaceae the asci are prototuni-
cate and disintegrate early as a part of the formation of a mazae-
dium (Tibell, 1984). In the Dactylosporaceae the asci lack a
tholus and are apically covered by a thick gelatinous sheet;
the ascospores are brown and septate (Bellemere & Hafellner,
1982). The sister clade of the H. anthracophila-group is the
clade consisting of the Cladoniaceae and Stereocaulaceae. As
long as these two families are kept separate, a new family is
needed for the H. anthracophila-group. Hence, we describe
a new genus (Carbonicola Bendiksby & Timdal) and a new
family (Carbonicolaceae) for this clade (see Nomenclatural
novelties, below).
Within the clade, H. foveata is a sister to H. anthracophila
and H. castaneocinerea (Fig. 2B). Hypocenomyce anthracoph-
ila seems to be genetically heterogeneous, as indicated by two
distinct clades among the four accessions included (Fig. 2B)
and should be studied further for a possible phenotypically
cryptic species. Molecular approaches to systematics of lichen-
forming fungi have revealed a substantial number of unrecog-
nized fungal species hidden within traditional phenotype-based
species (Crespo & Lumbsch, 2010; Lumsch & Leavitt, 2011;
Leavitt & al., 2012). Note that our type studies have shown that
the species epithet “myrmecina” should replace “castaneoci-
nerea” (see Nomenclatural novelties, below).
The Hypocenomyce friesii- and H. oligospora-groups. —
The only previously published phylogenetic study of species in
these groups is that of Wedin & al. (2005), who found H. friesii
to be sister to three Umbilicaria species and more distantly
related to H. scalaris. Our phylogenetic results support their
conclusion: H. caradocensis and H. friesii form a monophy-
letic group which is supported as sister to a clade consisting
of seven species of Lasallia and Umbilicaria (Fig. 2A; Electr.
Suppl.: Figs. S1–S2). Hypocenomyce friesii appears paraphy-
letic in our phylogeny and should be studied further for a pos-
sible phenotypically cryptic species. The morphology of the
H. friesii-group differs significantly from the saxicolous, um-
bilicate-foliose lichens of Umbilicaria and Lasallia. We there-
fore describe the new genus Xylopsora Bendiksby & Timdal
for the H. friesii-group (see Nomenclatural novelties, below).
Hypocenomyce isidiosa, which is not known with apothe-
cia, was originally thought to be related to H. friesii because
of its similar secondary chemistry (the rare compounds con-
friesiic and friesiic acids) and its substrate preference (burnt
wood; Elix, 2006). However, our molecular results show that
H. isidiosa is not closely related to Xylopsora but rather nests
within Xylog rapha (Trapeliaceae, Baeomycetales, Ostropo-
mycetidae; Fig. 2B). Morphologically, H. isidiosa resembles
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sorediate species of Xylographa in forming an endoxylic thallus
with vegetative dispersal units bursting out through cracks in
the wood (Fig. 1M). Confriesiic acid occurs in two other genera
of the Trapeliaceae, i.e., Rimularia Nyl. and Tra pel iop sis Hertel
& Gotth. Schneid. Hence, we propose the new combination
Xylographa isidiosa (Elix) Bendiksby & Timdal (see TNomen-
clatural novelties, below).
The H. oligospora-group forms a monophyletic group
moderately supported as sister to the Xylopsora-Lasallia-
Umbilicaria-clade (Fig. 2A; Electr. Suppl.: Figs. S1–S2). But as
the H. oligospora-group cannot be placed in Xylopsora without
making it paraphyletic, and lumping Xylopsora with Lasallia
and Umbilicaria seems impossible, we describe the new genus
Fulgidea Bendiksby & Timdal for the H. oligospora-group (see
Nomenclatural novelties, below).
Moreover, we suggest that Fulgidea and Xylopsora are
included in the Umbilicariaceae. Thus, the concept of the
previously exclusively foliose family Umbilicariaceae is ex-
tended to include crustose and squamulose genera. We find
this not unreasonable as we believe thallus growth form is not
a character of great importance at the family level (compare,
e.g., the current concept of the Physciaceae, Ramalinaceae
and Teloschistaceae; Lumbsch & Huhndorf, 2010). Whether
the Elixiaceae (which consists of only three known species)
should be accepted as a separate family is here left for future
studies. But when Fulgidea and Xylopsora are included in the
Umbilicariaceae, there are hardly any morphological, anatomi-
cal, or ecological arguments for accepting the Elixiaceae. Note
that two specimens growing on burnt wood and identified as
Hypocenomyce sp. in our study were identified as Elixia cre-
tica (Fig. 2A: Elixia cretica 1 and 2) and represent the first
report of this species, recently described from Greece (Spribille
& Lumbsch, 2010), in North America and Australia. Two ad-
ditional collections (Fig. 2A: Elixia sp., specimen 1 and 2) may
represent a new species of Elixia (see Appendix 1 for voucher
information).
The Hypocenomyce scalaris-group. —
Our molecular phy-
logenic results support the monophyly of the H. scalaris-group,
consisting of H. australis, H. scalaris, and H. tinderryensis
(Fig. 2A; Electr. Suppl.: Figs. S1–S2). The separation of H. tin-
derryensis from H. australis is, however, not supported and
should be studied further. The H. scalaris-group is sister to
a clade consisting of Boreoplaca and Ophioparma (Fig. 2A),
corroborating previous findings by Wedin & al. (2005) and
Miądlikowska & al. (2006; although with a different internal
topology). The circumscription of Hypocenomyce should hence
be restricted to the H. scalaris-group (see Nomenclatural novel-
ties, below).
Our phylogeny further supports a sister-relationship of the
Hypocenomyce-Boreoplaca-Ophioparma clade (Ophioparm-
aceae) with the Umbilicariaceae-Elixiaceae clade (Fig. 2A),
partly corroborating the phylogenetic topologies published
by Wedin & al. (2005) and Miądlikowska & al. (2006). In
Miądlikowska & al. (2006), Fuscideaceae was sister to the
Ophioparmaceae (and this group again sister to the Umbili-
cariaceae), a sister-relationship neither supported nor strongly
contradicted by our data (Fig. 2A; Electr. Suppl.: Figs. S1–S2).
Miądlikowska & al. (2006) considered the Fuscideaceae-
Ophioparmaceae-Umbilicariaceae clade as the Umbili-
cariales, and noted that the subclass Umbilicariomycetidae
should be considered for this group in the future. Regardless,
Lumbsch & Huhndorf (2010) and Hodkinson (2012) kept the
Umbilicari ales among the Lecanoromycetes orders incertae
sedis. Lumbsch & Huhndorf (2010) placed the Fuscideaceae
and the Ophioparmaceae among the Lecanoromycetidae fami-
lies incertae sedis, whereas Hodkinson (2012) recognized their
inclusion in the Umbilicariales. Our phylogenetic results, with
increased taxon sampling, support a clade consisting of the
Elixiaceae, Ophioparmaceae and Umbilicariaceae (Fig. 2A;
Electr. Suppl.: Figs. S1–S2). We refer to this clade as the
Umbilicariales and the Umbilicariomycetidae subcl. nov. in
this paper (see Nomenclatural novelties, below). We leave it to
future more comprehensive studies to consider the inclusion
of the Fuscideaceae in the Umbilicariomycetidae, but would
like to point out that our microscopical examination of asci in
Umbilicaria revealed a type similar to the Fuscidea-type, i.e.,
with amyloid layers lining both the inside and outside of the
ascus wall near its apex.
The Hypocenomyce xanthococca-group (Pycnora). —
In
Wedin & al. (2005), Pycnora sorophora and P. xanthococca
formed a strongly supported group that was sister to the Aca-
rosporaceae (parsimony) or Candelariaceae (Bayesian). In our
phylogeny (Fig. 2A), which includes multiple accessions of
all four Pycnora species, all, except P. leucococca, form a
strongly supported clade. The already existing name for the
H. xanthococca-group, Pycnora, hence comprises the three
species P. praestabilis (Nyl.) Hafellner, P. sorophora, and
P. xanthococca (se e Nomenclatural novelties, below).
Our phylogenetic results support a sister-relationship be-
tween Pycnora and the Candelariaceae (Fig. 2A; Electr. Suppl.:
Figs. S1–S2), corroborating the Bayesian results by Wedin & al.
(2005). Although only representatives from two Candelariaceae
genera have been included here (i.e., Candelaria A. Massal. and
Candelariella Müll. Arg.), Westberg & al. (2007) showed that
the family also comprises the two genera Candelina Poelt and
Placomaronea Räsänen. We believe differences in the second-
ary chemistry (pulvinic acid derivatives vs. dibenzofurans)
and in the apothecia (lecanorine and biatorine vs. lecideine)
between the Candelariaceae and Pycnora justify placing the
latter in the new family Pycnoraceae, and we include it in the
order Candelariales. This order may be placed in the “Cande-
lariomycetidae” (nom. inval.).
Our results (Fig. 2) support the previously published find-
ing that the Candelariales is distinct from the Lecanorales
(Wedin & al., 2005; Miądlikowska & al., 2006; Hofstetter & al.,
2007; Lumbsch & al., 2007); a finding that made Lumbsch
& Huhndorf (2010) place Candelariales among the Lecano-
romycetes orders incertae sedis. The six-gene phylogenetic
results by Schoch & al. (2009: fig. 3), however, shed doubts on
whether Candelariales at all belong in the Lecanoromycetes.
Based on the phylogenetic results by both Miądlikowska & al.
(2006) and Schoch & al. (2009), Hodkinson (2012) recognized
the “Subclass Candelariomycetidae”, but, no formal description
has been provided (see Nomenclatural novelties, below). Our
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restricted ascomycote taxon sampling does not provide infor-
mation about the phylogenetic placement of “Candelariomy-
cetidae”, but in the six-gene Ascomycota tree by Schoch & al.
(2009), Candelariales fell outside all well-supported classes
in superclass Leotiomyceta (sensu Eriksson & Winka, 1997).
Pycnora sorophora seems to be a polyphyletic species
(Fig. 2A). We hypothesize that this species evolved as a soredi
-
ate taxon from both P. praestabilis and P. xanthococca. This
should be investigated further with more accessions and a bet-
ter geographic coverage of all three species.
The fourth species of the H. xanthococca-group, Pyc-
nora leucococca (R. Sant.) R. Sant., occurs remotely from the
other Pycnora species in the phylogeny (Fig. 2B). Pycnora
leucococca groups with strong support with two accessions
of the genus Sporastatia A. Massal. (Fig. 2B; Electr. Suppl.:
Figs. S1–S2). In Miądlikowska & al. (2006), a clade consisting
of Rhizocarpaceae and Sporastatia was recovered and sup-
ported. This relationship was not recovered here. In the pres-
ent study, the P. lecococca–Sporastatia clade is sister group
to Rhizocarp aceae plus all remaining members of subclass
Lecanoromycetidae (Fig. 2B; Electr. Suppl.: Figs. S1–S2). It
should be noted, however, that regardless of the placement of
Rhizocarpaceae, the phylogenetic results support the removal
of Sporastatia from the Catillariaceae (Lecanorales; Fig. 2B;
Electr. Suppl.: Figs. S1–S2; Miądlikowska & al., 2006).
Fruiting bodies are not known in P. leucococca, but from
a morphological and ecological point of view, it seems im-
possible to include P. leucococca in Sporastatia. Hence, we
describe a new genus, Toensbergia Bendiksby & Timdal, for
this species and place it in the new family Sporastatiaceae
based on our molecular phylogenetic results (see Nomencla-
tural novelties, below).
NOMENCLATURAL NOVELTIES
“Candelariomycetidae” Miądl. & al. in Mycologia 98: 1091.
2006, nom. inval. (Art. 39.1). See Fig. 2A and Electr. Suppl.
Fig. S1 for clade “Candelariomycetidae” as applied to by
Miądlikowska & al. (2006).
Candelariales Miądl., Lutzoni & Lumbsch in Mycol. Res.
111: 530. 2007.
Pycnoraceae Bendiksby & Timdal, fam. nov. [MB 804835] –
Type: Pycnora Hafellner.
Diagnostic characters. – The Pycnoraceae is the clade
sister to the Candelariaceae and differs in forming lecideine,
black apothecia with consistently octosporous asci and con-
sistently simple ascospores, and in the secondary chemistry
of dibenzofurans (alectorialic acid). In the Candelariaceae, the
apothecia are lecanorine or biatorine, yellow to orange, the
asci are often polysporous, the ascospores often septate, and
the secondary chemistry consists of pulvinic acid derivatives.
Pycnora Hafellner in Stapfia 76: 157. 2001 – Type: Pycnora
xanthococca (Sommerf.) Hafellner.
Included species. – Pycnora praestabilis (Nyl.) Hafellner,
P. sorophora (Vain.) Hafellner, P. xanthococca (Sommerf.)
Hafellner.
Lecanoromycetidae Miądl., Lutzoni & Lumbsch in Mycol.
Res. 111: 529. 2007.
Lecanorales Nannf. in Nova Acta Regiae Soc. Sci. Upsal., ser.
4, 8(2): 68. 1932.
Carbonicolaceae Bendiksby & Timdal, fam. nov. [MB
804836] – Type: Carbonicola Bendiksby & Timdal.
Diagnostic characters. – The Carbonicolaceae is the clade
sister to a clade consisting of the Cladoniaceae and Stereo-
caulaceae. It differs from those families in forming a purely
crustose to squamulose, dark brown thallus with a thick, shiny
upper cortex, and in having a strong preference for the substrate
charred wood and bark. The core genera of the Cladoniaceae
and Stereocaulaceae form a fruticose secondary thallus, which
is absent in the Carbonicolaceae.
Carbonicola Bendiksby & Timdal, gen. nov. [MB 804837]
– Type: Carbonicola anthracophila (Nyl.) Bendiksby
& Timdal.
Diagnostic characters. – Thallus squamulose, adnate or
ascending and geotropically oriented, (greenish to) medium to
dark brown, shiny, epruinose, without hypothallus. Apothecia
brown, convex, weakly marginate when young, soon becoming
immarginate, epruinose; exciple composed of conglutinated,
thick-walled hyphae with thread-like lumina, colorless in inner
part, pale brown in the rim, K−, N−, lacking crystals; epihy-
menium brown, N−, without amorphous substances; ascus cla-
vate, octosporous, without an apical amyloid cap, with a well-
developed, amyloid tholus containing a deeper amyloid tube.
Pycnidium wall brown, N−; pycnoconidia filiform. Chemistry:
colensoic acid, 4-O-methylphysodic acid and related com-
pounds (in all species), fumarprotocetraric and protocetraric
acid (in C. anthracophila).
Etymolog y. – The name refers to its preferred substrate,
burnt wood (lat. carbo: charcoal, -cola: dweller).
Notes. – The genus differs from the other genera formerly
included in Hypocenomyce in having brown, convex, more or
less immarginate apothecia; a pale exciple composed of en
-
tirely conglutinated hyphae; a brown epihymenium lacking
amorphous substances; asci with a deeply amyloid tube; and
in the main secondary chemistry consisting of compounds of
the colensoic acid complex. Biatora, in which Hafellner (1993)
placed two Carbonicola species, differs mainly in forming a
crustose or at most a subsquamulose thallus and in having
a conical amyloid zone in the tholus (ascus of Bacidia-type,
typical of the Ramalinaceae).
Carbonicola anthracophila (Nyl.) Bendiksby & Timdal, comb.
nov. [MB 804838] ≡ Lecidea anthracophila Nyl. in
Flora 48: 603. 1865 ≡ Psora anthracophila ( Nyl.) Arnold
in Flora 53: 471. 1870 ≡ Biatora anthracophila (Nyl.)
Tuck., Syn. N. Amer. Lich. 2: 14. 1888 ≡ Hypocenomyce
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anthracophila (Nyl.) P. James & Gotth. Schneid. in Bib-
lioth. Lichenol. 13: 81. 1980 ≡ Biatora anthracophila (Nyl.)
Hafellner in Herzogia 9: 729. 1993 – Lectotype (designated
by Timdal, 1984a): Finland, “Evois ad lignium [sic!] car-
bonatum”, 1865, J.P. Norrlin s.n. (H-NYL No. 20375 p.p.!)
= Psora cladonioides var. albocervina Räsänen, Lichenes Fen
-
niae Exsiccati: No. 281. 1936 ≡ Lecidea cladonioides var.
albocervina (Räsänen) Zahlbr., Cat. Lich. Univ. 10: 346.
1939– Lectotype (designated here): Finland, Karelia bo-
realis, Pielisjärvi, Louhivaara, ad orientem versus ab lacu
Ylinen Pitkäjärvi, ad lignum vetustum carbonatum trunci
erecti altique Pini silvestris in pineto aprico deserto, July
1936, M. Laurila s.n. = Räsänen, Lichenes Fenniae Exsic-
cati No. 281 (O No. L-894!; isotypes: BM!, S!, UPS No.
L-533305!).
= Lecidea cladonioides Fr. ex Th. Fr., Lichenogr. Scand.: 417.
1874, nom. illeg. superfl. (nomenclaturally superfluous
name for L. anthracophila Nyl.; Ar t. 52.1) ≡ Psora cladoni-
oides (Th. Fr.) Elenkin, Fl. Lishaynikov Sredney Rossii
[Lichenes Florae Rossiae Mediae] 2: 345. 1907.
– “Biatora ostreata var. cladonioides” Fr., Summa Veg. Scand.:
111. 1845, nom. nud.
Carbonicola foveata (Timdal) Bendiksby & Timdal, comb.
nov. [MB 804840] ≡ Hypocenomyce foveata Timdal in
Nordic J. Bot. 4: 98. 1984 ≡ Biatora foveata (Timdal)
Hafellner in Herzogia 9: 729. 1993 – Holotype: Austra-
lia, Victoria, Cultivation Creek, Billywing area, Western
Grampians, 37°15′ S, 142°16′ E, August 1981, H. Krog
Au 1401 (O No. L-50!).
Carbonicola myrmecina (Ach.) Bendiksby & Timdal, comb.
nov. [M B 804841] ≡ Lecidea scalaris var. myrmecina Ach.,
Methodus: 78. 1803 ≡ Lecidea myrmecina (Ach.) Fr. in
Kongl. Vetensk. Akad. Handl. 1822: 257. 1822 ≡ Parmelia
ostreata var. myrmecina (Ach.) Torss., Enum. Lich. Bys-
sacearum Scand.: 14. 1843 ≡ Lecidea ostreata var. myr-
mecina (Ach.) Nyl., Lich. Scand.: 243. 1861 ≡ Psora ostreata
var. myrmecina (Ach.) Th. Fr. in Nova Acta Regiae Soc. Sci.
Upsal., ser. 3, 3: 269. 1861 ≡ Psora myrmecina (Ach.) Boistel,
Nouv. Fl. Lich. 2: 94. 1902 ≡ Psora scalaris var. myrmecina
(Ach.) Räsänen, Lichenes Fenniae Exsiccati: No. 825. 1943
– Lectotype (designated here): [s. loco], “Parmelia (Pso-
roma) myrmecina, e collect. cel. Acharii accepi” [scrips.
G. Wahlenberg], ex herb. G. Wahlenberg (UPS-ACH No.
256!). Probable isolectotypes: [s. loco], ex herb. Agrelius
(UPS-ACH No. 251!); “Svecia” (H-ACH No. 312D photo!).
= Hypocenomyce castaneocinerea (Räsänen) Timdal in Nordic
J. Bot. 4: 97. 1984 ≡ Psora cladonioides var. castaneocine
-
rea Räsänen, Lichenes Fenniae Exsiccati: No. 282. 1936
≡ Lecidea cladonioides var. castaneocinerea (Räsänen)
Zahlbr., Cat. Lich. Univ. 10: 346. 1939 – Lectotype (desig-
nated here): Finland, Karelia borealis, Pielisjärvi, Kitsin-
vaara, Ylinen Pitkäjärvi, ad truncum erectum carbonatum
Pini silvestris in silva aprica deserta, July 1936, M. Laurila
s.n. = Räsänen, Lichenes Fenniae Exsiccati: No. 282 (O No.
L-895!; isotypes: BM!, UPS No. L-533306!).
Note. – UPS-ACH 256 contains colensoic acid, 4-O-methyl-
physodic acid, ± norcolensoic acid and possibly trace of phy-
sodic acid (by TLC).
Lecanoromycetidae families incertae sedis
Sporastatiaceae Bendiksby & Timdal, fa m. nov. [M B 804842]
– Type: Sporastatia A. Massal.
Diagnostic characters. – Thallus crustose, containing uni-
cellular green algae, lacking cephalodia. Apothecia lecideine,
black. Ascus narrowly clavate, polysporous, with a well-devel-
oped, deeply amyloid tholus without further amyloid structures.
Ascospores hyaline, thin-walled, non-halonate, simple.
Notes. – The family consists of two genera, Sporastatia and
Toensbergia, and the description of the apothecia given above
is made from the former as the latter is not known from fertile
material. Sporastatia is currently placed in the Catillariaceae
(Lumbsch & Huhndorf, 2010) because of its Catillaria-type
ascus, but it differs from that family in its polyspory.
Toensbergia Bendiksby & Timdal, gen. nov. [MB 804843]
– Type: Toensbergia leucococca (R. Sant.) Bendiksby
& Timdal.
Diagnostic characters. – Thallus of minute, adnate, crenu-
late, grayish white areolae, lacking a hypothallus, containing
alectorialic acid.
Etymology. – The name honors Dr. Tor Tønsberg (born
1948), Bergen, in appreciation of his important work on soredi-
ate, corticolous lichens.
Notes. – The genus consists of a single, sterile species
which was originally placed in Hypocenomyce, later in Pyc-
nora, apparently due to its morphological, ecological and chem-
ical resemblance with species of the H. xanthococca-group.
Toensbergia leucococca (R. Sant.) Bendiksby & Timdal, comb.
nov. [MB 804845] ≡ Hypocenomyce leucococca R. Sant.
in Thunbergia 2: 3. 1986 ≡ Pycnora leucococca (R. Sant.)
R. Sant. in Santesson & al., Lichen-forming Lichenicol.
Fungi Fennoscand.: 275. 2004 – Holotype: Sweden, Härje-
dalen, Tännäs par., ca. 1 km E of Ramundbergets Fjällgård,
63°42′ N, 12°25′ E, alt. ca. 750 m, on the trunk of a birch
in the subalpine birch forest, August 1977, R. Santesson
27901 = Moberg, Lichenes Selecti Exsiccati Upsaliensis
No. 6 (UPS No. L-86993!; isotype: O No. L-328!).
Ostropomycetidae Reeb, Lutzoni & Cl. Roux in Molec. Phylo-
gen. Evol. 32: 1055. 2004.
Baeomycetales Lumbsch, Huhndorf & Lutzoni in Mycol. Res.
111: 529. 2007.
Trapeliaceae Hertel in Vorträge Gesamtgeb. Bot., n.s., 4: 181.
1970 – Type: Trape lia M. C hoi sy.
Xylographa (Fr.) Fr., Fl. Scan.: 344. 1836 ≡ Stictis subg. Xylo-
grapha Fr., Syst. Mycol. 2: 197. 1822 – Type: Xylographa
parallela (Ach.) Fr.
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Xylographa isidiosa (Elix) Bendiksby & Timdal, comb. nov.
[MB 804846] ≡ Hypocenomyce isidiosa Elix in Myco-
taxon 94: 219. 2006 – Holotype: Australia, Western Aus-
tralia, Avon district, Charles Gardner Flora Reserve, cen-
tral track, 20 km SW of Tammin along old York Road,
31°47′24″ S, 117°28′07″ E, alt. 305 m, on dead, charred
wood in Eucalyptus woodland with Casuarina and Acacia
in shallow gully, 22 April 2004, J.A. Elix 31849 (PERTH
n.v.; isotype: CANB No. 737037!).
Umbilicariomycetidae Miądl. & al. ex Bendiksby, Hestmark
& Timdal, subcl. nov. [MB 805269]
Description. – Thallus containing green algae, lacking
cephalodia, crustose, squamulose, peltate, or umbilicate-
foliose. Apothecia lecideine or lecanorine. Ascus rhombic to
clavate, usually covered by an amyloid cap, usually with an
amyloid inner layer near the ascus apex (± Fuscidea-type) or
with a small, amyloid tholus, mono- to octosporous.
Note. – Miądlikowska & al. (2006) published the name as
a nomen nudum.
Umbilicariales J.C. Wei & Q.M. Zhou in Mycosystema 26:
44. 2007.
Ophioparmaceae R.W. Rogers & Hafellner in Lichenologist
20: 172. 1988 – Type: Ophioparma Norman.
Hypocenomyce M. Choisy in Bull. Mens. Soc. Linn. Lyon 20:
133. 1951 – Type: H. scalaris (Ach.) M. Choisy.
Included species. – Hypocenomyce australis Timdal,
H. scalaris (Ach.) M. Choisy, H. tinderryensis Elix.
Umbilicariaceae Chevall., Fl. Gen. Env. Paris 1: 640. 1826 –
Type: Umbilicaria Hoffm.
Fulgidea Bendiksby & Timdal, gen. nov. [MB 804847] – Type:
Fulgidea oligospora (Timdal) Bendiksby & Timdal.
Diagnostic characters. – Thallus squamulose, adnate or
ascending and geotropically oriented, grayish green to dark
brown, dull to shiny, epruinose, without hypothallus. Apo-
thecia black, plane, persistently marginate, egyrose, epru-
inose; exciple composed of conglutinated, rather thin-walled
hyphae with ellipsoid to shortly cylindrical lumina, inner part
and rim blackish brown, the pigment partly dissolving in K
with a brown effusion, N−, lacking crystals; epihymenium
brown, N−, containing amorphous substances dissolving in
K with a brown effusion; ascus narrowly rhombic, with an
apical amyloid cap and a small, amyloid tholus containing a
non- amyl oid ce ntr al plug. Pycn idium wall brown, N−; pyc no-
conidia bacilliform, 7–10 × ca. 1 µm. Chemistry: alectorialic
and thamnolic acids.
Etymolog y. – The name refers to its preferred substrate,
burnt wood (lat. fulgur: lightning), and to its morphological
resemblance to Lecidea species.
Notes. – The genus differs from Hypocenomyce mainly
in the anatomy of the exciple which in Hypocenomyce is col-
orless in the inner part, green in the rim (K−, N+ violet), and
composed of only partly conglutinated hyphae which are sepa-
rated by crystals of lecanoric acid (C+ red). Furthermore, in
Hypocenomyce the epihymenium and the pycnidium wall are
green, N+ violet, and the epihymenium contains lecanoric acid
and lacks amorphous substances. The pycnoconidia are gener-
ally longer in Hypocenomyce, i.e., bacilliform to filiform.
Fulgidea differs from Pycnora mainly in the ascus, which
in Pycnora is broadly clavate, lack an amyloid cap, have a
well-developed, amyloid tholus with a parietal deeper amy-
loid area (fig. 3 in Timdal 1984a). Furthermore, in Pycnora
the thallus is strictly crustose, the epihymenium is green, N+
violet, containing amorphous substances dissolving in K with
a violet effusion, the pycnidium wall is green, N+ violet, and
the pycnoconidia shorter (subglobose to shortly bacilliform).
Elixia differs from Fulgidea in forming a crustose or en-
doxylic thallus, star-shaped to lirelloid apothecia, capitate pa-
raphyses with a sharply delimited pigment zone in the top of
the apical cell, and in lacking secondary compounds.
See also Xylopsora, below.
Fulgidea oligospora (Timdal) Bendiksby & Timdal, comb.
nov. [MB 804848] ≡ Hypocenomyce oligospora Timdal
in Mycotaxon 77: 446. 2001 – Holotype: U.S.A., Ari-
zona, Gila Co., Little Diamond Rim above Beaver Valley,
34°20′30″ N, 111°18′30″ W, alt. 1840 m, piñon-juniper wood-
land, on burned Juniperus wood, March 1999, T.H. Nash
42735a = Nash, Lichenes Exsiccati Distributed by Arizona
State University No. 311 (O No. L-767!).
Fulgidea sierrae (Timdal) Bendiksby & Timdal, comb. nov.
[MB 804849] ≡ Hypocenomyce sierrae Timdal in Myco-
taxon 77: 449. 2001 – Holotype: U.S.A., California, Los
Angeles Co., San Gabriel Mts, along State Hwy 2, 0.3 mi
NE (road) of Newcomb Ranch, 34°20.3′ N, 117°59.6′ W,
alt. 1650 m, on trunk of Libocedrus decurrens, on lower,
partly charred parts, March 1998, E. Timdal SON1251
(O No. L-60059!).
Xylopsora Bendiksby & Timdal, gen. nov. [MB 804850] –
Type: Xylopsora friesii (Ach.) Bendiksby & Timdal.
Diagnostic characters. – Thallus squamulose, adnate or
irregularly bullate, grayish green to dark brown, dull to shiny,
epruinose, without hypothallus. Apothecia black, plane, per-
sistently marginate, often gyrose, epruinose; exciple composed
of conglutinated, rather thin-walled hyphae with ellipsoid to
shortly cylindrical lumina, inner part and rim blackish brown,
the pigment partly dissolving in K with a brown effusion, N−,
lacking crystals; epihymenium brown, N−, containing amor-
phous substances dissolving in K with a brown effusion; ascus
narrowly rhombic, with an apical amyloid cap and a small, amy-
loid tholus containing a non-amyloid central plug. Pycnidium
wall brown, N−; pycnoconidia narrowly ellipsoid to shortly
bacilliform, 2.5–5 × ca. 1 µm. Chemistry: friesiic acid (major;
also confriesiic acid as minor or trace, according to Elix, 2006).
Etymolog y. – The name refers to its preferred substrate,
wood (gr. xylos), and its previous inclusion in Lecidea sect.
Psora.
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953Version of Record (identical to print version).
Abassi Maaf, L. & Roux, C. 1984. Hypocenomyce stoechadiana
nova likenspecio (Hypocenomyce stoechadiana espece nouvelle
de lichen). Bull. Soc. Linn. Provence 36: 189 –19 4.
Bellemere, A. & Hafellner, J. 1982. L’ultrastructure des asques du
genre Dactylospora (Discomycetes) et son interet taxonomique.
Cryptog. Mycol. 3: 71–93.
Notes. – The genus is morphologically and anatomically
very similar to Fulgidea, and differs mainly in two characters:
the size of the pycnoconidia (2.5–5 vs. 7–10 µm long) and the
secondary chemistry friesiic acid (depsido-depsone) vs. alec-
torialic acid (benzyl ester) and thamnolic acid (β-orcinol meta-
depside). Xylopsora differs from Elixia, Hypocenomyce, and
Pycnora in the same characters as listed under Fulgidea, above.
Xylopsora caradocensis (Nyl.) Bendiksby & Timdal, comb.
nov. [MB 804 851] ≡ Lecidea caradocensis Leight. ex Nyl.
in Actes Soc. Linn. Bordeaux 21: 383. 1857 ≡ Psora cara-
docensis (Leight. ex Nyl.) Mudd, Man. Brit. Lich.: 169.
1861 ≡ Toninia caradocensis (Leight. ex Nyl.) J. Lahm
in Jahres-Ber. Westfäl. Prov.-Vereins Wiss. 11: 125. 1884
≡ Bilimbia caradocensis (Leight. ex Nyl.) A.L. Sm. in
Crombie & Smith, Monogr. Lich. Britain 2: 133. 1911 ≡
Hypocenomyce caradocensis (Nyl.) P. James & Gotth.
Schneid. in Lichenologist 12: 107. 1980 – Lectotype (des-
ignated by Timdal, 1992): U.K., Wales, Shropshire, Caer
Caradoc, W. Leighton s.n. = Leighton, Lichenes Britannici
Exsiccati No. 160 (BM!; isotypes: O No. L-450!; UPS!).
Xylopsora friesii (Ach.) Bendiksby & Timdal, comb. nov. [MB
804852] ≡ Lecidea friesii Ach. in Liljeblad, Utkast Sv. Fl.,
ed . 3: 610. 1816 ≡ Psora friesii (Ach.) Hellb. in Kongl. Sven-
ska Vetensk. Acad. Handl., nov. ser., 9 (no. 11): 61. 1870 ≡
Biatora friesii (Ach.) Tuck., Syn. N. Amer. Lich. 2: 15. 1888
≡ Psora ostreata f. friesii (Ach.) Boistel, Nouv. Fl. Lich. 2:
94. 1902 ≡ Hypocenomyce friesii (Ach.) P. James & Gotth.
Schneid. in Biblioth. Lichenol. 13: 84. 1980 – Lectotype
(designated here): “Lecidea friesiana. Suecia” (H-ACH
No. 436A photo!).
ACKNOWLEDGEMENTS
We acknowledge generous financial support (Project no.
70184216) from the Norwegian Taxonomy Initiative (Norske Arts-
prosjektet) administered by The Norwegian Biodiversity Information
Centre (Artsdatabanken). Thanks are also due to the curators of ASU,
CANB, and S for the loan of specimens; to UPS for access to type
material during our visit; to H for preparing high-resolution photo-
graphs of type specimens in the Acharius herbarium; to John A. Elix
for providing a specimen of H. isidiosa, to Geir Hestmark, Jolanta
Mi ądl ikow sk a and Mar tin Westb er g fo r discu ss io ns on the Umbil ic ari -
omycetidae and “Candelariomycetidae”; to Siri Rui for assistance in
the lab, and to Toby Spribille and two anonymous reviewers for helpful
feedback on an earlier version of this work.
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Appendix 1.
Taxa and GenBank accession numbers for all samples included in this study; voucher infor mation is given for newly generated sequences. An
asterisk after the accession number indicates sequences reported here for the first time.
Taxon, voucher, accession number of nrITS, nrLSU, mtSSU. — Signs/symbols used: – missing data; * newly generated sequence; † only 5.8S and ITS2;
♦ sequences less than 200 bp that are provided below Appendix 1 because Gen Bank does not accept sequences shorter than 200 bp.
Acarospora peliscypha Th. Fr., DQ374132, –, DQ374108. Agyrium rufum (Pers.) Fr., –, EF581826, EF581823. Ainoa mooreana (Carroll) Lumbsch & I. Schmit t,
–, AY212828, AY212850. Arctomia delicatula Th. Fr., –, AY853355, AY853307. Aspicilia cinerea (L.) Körb., HQ650637†, DQ986779, DQ986890. Bacidia
rubella (Hoffm.) A. Massal., AF282087†, –, AY567723. Baeomyces rufus (Huds.) Rebent., AF448458†, DQ871008, DQ871016. Biatora vernalis (L.) Fr.,
Norway, J.T. Klepsland JK09-L616 (O L-165159), KF360369*†, KF360446*, K F360418*. Boreoplaca ultrafrigida Timdal, HM161512, AY853360, AY853312.
Bryoria capillaris (Ach.) Brodo & D. Hawksw., AF058032†, DQ923655, DQ923626. Calopadia sp., –, EU601752, EU601739. Candelaria concolor (Dicks.)
Stein, GU929922, DQ986791, DQ986806. Candelariella aurella (Hoffm.) Zahlbr., EF535162, AY853361, AY853313. Candelariella coralliza (Nyl.) H. Magn.,
AF182074, AY853362, AY853314. Candelariella ref lexa (Nyl.) Lettau, EF535190, DQ912331, DQ912272. Candelariella terrigena Räsänen, HQ650602,
DQ986745, –. Candelariella vitellina (Hoffm.) Müll. Arg., AJ640085, AY853363, AY853315. Catillaria chalybeia (Borrer) A. Massal., Norway, R. Haugan
7947 (O L-155291), KF360370*†, KF360447*, –. Catolechia wahlenbergii (Ach.) Körb., AF250792, DQ986794, DQ986811. Cladia retipora (Labill.) Nyl.,
GQ500918†, AY340540, AY340487. Cladonia rangiferina (L.) F.H. Wigg, EU266113†, AY300832, AY300881. Coccotrema cucurbitula (Mont.) Müll. Arg.,
AF 329162†, AF274092, AF329161. Crocynia pyxinoides Nyl., AF517920†, AY584653, AY584615. Diploschistes scruposus (Schreb.) Norman, HQ650716†,
AF279389, AY584692. Elixia cretica T. Sprib. & Lumbsch 1, Australia, New South Wales, Tinderry Range, 10 km E of Michelago, H. Streimann & J.A.
Curnow 50968 p.p. (CANB-9304299 p.p.), KF360371*, KF360 448*, –. 2, Mexico, Chihuahua, along route 16 ca. 20 km W of Basaseachic, E. Timdal SON78/03
(O L-15969), KF360372*, KF360449*, KF360419*. 3, –, –, GQ892058. Elixia flexella (Ach.) Lumbsch 1, Austria, J. Halda, S. Palica & J. Steinova 12407
(O L-157191), KF360373*, KF36 0450*, KF360420*. 2, –, AY853368, AY853320. 3, –, AY30 0837, AY30 088 7. Elixia sp. T. Sprib. & Lumbsch 1, U.S.A., Arizona ,
Gila Co., McFadden Peak, 15 mi S of Young, T.H. Nash III 11177 (ASU), KF360374*, K F360451*, –. 2, U.S.A., Arizona, Cochise Co., Chiricahua National
Monument, along the Loop Trail, T.H. Nash III 41750 (ASU ), KF360375*, KF360452*, –. Evernia prunastri (L.) Ach., HQ650611†, AF107562, AF351162.
Fuscidea mollis (Wahlenb.) V. Wirth & Vezda, –, AY853369, AY853321. Geoglossum nigritum (Fr.) Cooke, DQ491490, AY544650, AY544740. Graphis
scripta (L.) Ach., AF229195†, AY853370, AY853322. Gregorella humida (Kullh.) Lumbsch, AF429263†, AY853378, –. Gypsoplaca macrophylla (Zahlbr.)
Timdal, –, DQ899298, –. Haematomma ochroleucum (Neck.) J.R. Laundon, EU075536†, AY756350, AY756367. Heterodea muelleri (Hampe) Nyl., GQ500906†,
AY340545, AY340494. Hymenelia lacustris (With.) M. Choisy, –, AY853371, AY853323. Hypocenomyce anthracophila (Nyl.) P. James & Gotth. Schneid. 1,
Norway, B.P. Løfall & A. Ognedal L10657 (O L-129736), K F360376*, KF360 453*, KF3 60421*. 2, Norway, J.T. Klepsland JK08-L282 (O L-158 453), KF 360377*,
KF360454*, KF360422*. 3, Norway, E. Timdal 11024 (O L-158536), KF360378*, KF360455*, KF360423*. 4, Norway, E. Timdal 11027 (O L-158539), KF36037 9*,
KF360456*, KF360424*. Hypocenomyce australis Timdal 1, Australia, J.A. Elix 19801 (O L-144372), KF360380*†, –, –. 2, Australia, H. Krog Au14/2
(O L-144373), ♦*, –, –. 3, Australia, W.A. Weber & D. McVean s.n., 1967–10–11 (O L-201, isotype), KF360381*†, –, –. 4, Australia, G. Thor 6047a (S), KF36 0382*,
–, –. Hypocenomyce caradocensis (Nyl.) P. James & Gotth. Schneid. 1, Norway, E. Timdal 2410 (O L-32967), KF360383*†, –, –. 2, Sweden, G. Westling s.n.,
1992 –04 –05 (S -L-53582), KF360384*†, –, –. 3, Sweden, G. Odelvik 599 (S-L-29227), KF360385*, –, KF360425*. Hypocenomyce castaneocinerea (Rä sänen)
Timdal 1, Norway, R. Haugan 9677 (O L-166561), KF360386*, KF360457*, KF360426*. 2, Norway, E. Timdal 11028 (O L-158540), KF360387*, KF360458*,
KF360427*. Hypocenomyce foveata Timdal, Australia, G. Thor 6047b (S), ♦*, –, –. Hypocenomyce friesii (Ach.) P. James & Gotth. Schneid. 1, Norway,
E. Timdal 11029 (O L-158541), KF360388*, KF360459*, KF360428*. 2, Norway, A. Breili 3615 (O L-167185), KF360389*, KF360460*, KF360429*. 3, –,
AY85 3372, AY8 53324 . 4, Norway, E. Timdal 1055 (O L-56480), KF360390*†, –, –. Hypocenomyce isidiosa Elix 1, Australia, J.A. Elix 31849 (CANB -737037.1,
isotype), KF360391*, K F360461*, KF360430*. 2, Australia, J.A. Elix 39837 (O L-171593), KF360392*, KF360462*, K F3 60431*. Hypocenomyce leucococca
R. Sant. 1, Norway, E. Timdal 12232 (O L-170732), KF360393*, KF360463*, KF360432*. 2, Norway, E. Timdal 12328 (O L-170828), KF360394*, KF360464*,
KF360433*. Hypocenomyce oligospora Timdal 1, U.S.A., T.H. Nash III 42735a (O L-767, holotype), KF360395*, KF360465*, –. 2, U.S.A., S. Rui & E. Timdal
US 215/01 (O L-59862), KF360396*, KF360466*, KF360434*. 3, U.S.A., S. Rui & E. Timdal US272/01 (O L-59992), KF360397*, KF360467*, KF360435*. 4,
Russia, R. Haugan & E. Timdal YAK04/05 (O L-18713), KF360398*, KF360468*, –. Hypocenomyce praestabilis (Nyl.) Timdal 1, U.S.A., E. Timdal SON70/13
(O L-15871), KF360399*, –, –. 2, Sweden, E. Timdal 2860 (O L-144277), KF360400*, KF360469*, –. Hypocenomyce scalaris (Ach.) M. Choisy 1, Norway, E.
Ti md al 11 022 (O L-158534), KF360401*, KF360 470*, KF360436*. 2, DQ782852, DQ782914, DQ912274. 3, HQ650632, DQ986748, DQ986861. 4, –, AY85337 3,
AY853325. 5, –, AY853374, AY853326. Hypocenomyce sierrae Timdal 1, U.S. A., S. Rui & E. Timdal US249/01 (O L-59964), KF360402*, KF 360471*, KF360 437*.
2, U.S.A., E. Timdal SON125/01 (O L-60059, holotype), KF360403*, –, –. Hypocenomyce sorophora (Vain.) P. James & Poelt 1, Norway, M. Bendiksby & J.
Klepsland MB-L1 (O L -175410), KF36 040 4*, –, KF360438*. 2, Norway, E. Timdal 2643 (O L- 60179), KF 360405*†, –, –. 3, Norway, E. Timdal 3343 (O L-2824 8),
KF360406*, –, KF360439*. 4, Sweden, E. Timdal 2908 (O L -144310), ♦*†, –, –. 5, FJ959357, AY853387, AY853338. Hypocenomyce tinderryensis Elix 1,
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Australia, J.A. Elix 38733 (CANB-790800), KF360407*, –, KF360440*. 2, Australia, J.A. Eli x 33386 (CANB-9801742.1), KF360408*†, –, –. 3, Australia, J.A.
Eli x 33387 (CANB-676257), KF360409*†, –, –. 4, Australia, H. Streimann & J.A. Curnow 50968 (CANB-9304299, holotype), KF360410*, –, –. 5, Australia,
H. Streimann & J.A. Cur now 35001 (CA NB- 610213.1), ♦*†, –, –. Hypocenomyce xanthococca (Sommerf.) P. James & Gotth. Schneid. 1, Norway, R. Haugan
8090 (O L-160472), KF360411*, KF360472*, K F3604 41*. 2, Norway, E. Timdal 11646 (O L-163707), KF360412*, KF360473*, KF360442*. 3, AY853388,
AY853388, AY853339. Lasallia pennsylvanica (Hoffm.) Llano, HM161513, AF356665, AY631278. Lasallia pustulata (L.) Mérat, HM161456, DQ883690,
DQ986889. Lecanora carpinea (L.) Vain., AF070020†, DQ787363, DQ787364. Lecanora polytropa (Hoffm.) Rabenh., HQ650643†, DQ986792, DQ986807.
Lecanora sulphurea (Hoffm.) Ach., AF070030†, –, EF105419. Lecidea atrobrunnea (Lam. & DC.) Schaer., EU259897, AY532993, GU074510. Lecidea tes-
sellata Flörke, EU263926, AY532998, GU074491. Lecidella euphorea (Flörke) Hertel, HQ650596†, –, DQ986784. Lepraria lobificans Nyl., HQ650623,
DQ986768, DQ986887. Lobothallia radiosa (Hoffm.) Hafellner, JF703124†, DQ780306, DQ780274. Lopadium disciforme (Flot.) Kullh., –, AY756355,
AY75637 3. Loxospora ochrophaea (Tuck.) R.C. Harris, HQ650641†, DQ986750, DQ986900. Maronea constans ( Nyl.) Hepp, –, AY640956, EF659771. Meg-
alaria grossa (Nyl.) Hafellner, AF282074†, AY756356, AY762095. Meridianelia maccarthyana Kantvilas & Lumbsch, –, –, FJ763185. Metus conglomeratus
(F. Wilson) D.J. Galloway & P. James, GQ500912†, AY340555, AY340510. Micarea adnata Coppins, AY756468†, AY756326, AY567751. Miltidea ceroplasta
(C. Bab.) D.J. Galloway & Hafellner, –, HQ391558, HQ391557. Mycoblastus sanguinarius (L.) Norman, DQ782842†, DQ912333, DQ912276. Myelochroa
aurulenta (Tuck.) Elix & Hale, –, DQ973025, DQ972972. Myriospora smaragdula ( Wah lenb.) Näg eli, AY853354, AY853354, AY853306 . Neophyllis melacarpa
F. Wilson, –, AY340556, AY340511. Nephroma arcticum (L.) Torss., –, DQ973040, –. Ochrolechia parella (L.) A. Massal., AF332123†, AF274097, AF329173.
Ophioparma handelii (Zahlbr.) Printzen & Rambold, Ch ina, W. Obermayer 5135 (O L-168529), KF360 413*, –, –. Ophioparma lapponica (Räsänen) Hafellner
& R.W. Roge rs, Norway, E. Timdal 12353 (O L-170853), KF360414*, –, KF3604 43*. Ophioparma ventosa (L.) Norman 1, Norway, R. Haugan 7615 (O L -151477 ),
KF36 0415*, KF 360474*, KF360444*. 2, AY011013, AY853380, AY853331. Orceolina kerguelensis (Tuck.) Hertel, AY212814, AY212830, AF381561. Parmelina
quercina (Wil ld.) Hale, AY611105†, AY607818, AY611164. Peltigera praetextata (Sommerf.) Zopf, –, AF286813, –. Pertusaria dactylina (Ach.) Nyl., DQ782843†,
DQ782907, DQ912307. Pertusaria leioplaca DC., AF 33212 5†, AY300852, AY300903. Pilophorus strumaticus Cro mb ., AF517931†, AY340560, AY340517.
Placopsis sp. D.L. Galloway, ined., AY21282 6, AY 2128 45, AY2128 67. Placynthiella uliginosa (Sch rad.) Coppins & P. James, HQ650633, DQ986774, DQ986877.
Pleopsidium flavum Körb., AY853385, AY853385, AY853336. Pleopsidium gobiense (H. Magn.) Hafellner, HQ650723, DQ883698, DQ991755. Porpidia
macrocarpa (DC.) Hertel & A.J. Schwab, EU263923, AY532964, GU074512. Porpidia speirea (Ach.) Kremp., HQ650631, DQ986758, DQ986865. Protoblas-
tenia rupestris (Scop.) J. Steiner, EF524318†, AY756358, –. Protothelenella sphinctrinoidella (Nyl.) H. Mayrhofer & Poelt, –, AY607735, AY607747. Psilolechia
leprosa Coppins & Purvis, AY756496†, AY756333, AY567730. Psora decipiens (Hedw.) Hoffm., HQ650619†, DQ986760, –. Ptychographa xylographoides
Nyl., –, –, AY212872. Pyrrhospora quernea (Dicks.) Körb., AF517930†, AY300858, AY567712. Ramalina complanata (Sw.) Ach., –, DQ973038, DQ972986.
Rhizocarpon oederi (Weber) Körb., AF483612, DQ986804, DQ986788. Rhizoplaca chrysoleuca (Sm.) Zopf, AF159940†, DQ787353, DQ787354. Rimularia
psephota (Tuck.) Hertel & Rambold, –, DQ871012, DQ871019. Sarcogyne privigna (Ach.) A. Massal., DQ374145, AY853392, DQ374124. Schaereria fusco-
cinerea (Nyl.) Clauzade & Cl. Roux, AF274090†, AY300860, AY300910. Scoliciosporum umbrinum (Ach.) Arnold, AY541277†, AY300861, AY300911.
Solenopsora holophaea (Mont.) Samp., AM292708†, –, –. Sphaerophorus globosus (L.) DC., HQ650622†, DQ986767, DQ986866. Sporastatia polyspora
(Nyl.) Grummann, –, AY640968, AY584724. Sporastatia testudinea (Ach.) A. Massal., –, AY640969, AY584725. Stereocaulon paschale (L.) Hoffm.,
HQ650690†, AY340568, AY584726. Teloschistes flavicans (Sw.) Norman, –, EU680955, –. Tephromela atra (Huds.) Hafellner, HQ650608†, DQ986766,
DQ986879. Thamnolia vermicularis (Sw.) Schaer., EU714437†, –, AY853345. Thelotrema suecicum (H. Magn.) P. James, AJ508684†, AY30 0867, AY3 00917.
Toninia sedifolia (Scop.) Timdal, HQ650689†, DQ973039, DQ972987. Trapelia placodioides Coppins & P. James, AF274081, AF274103, AF431962. Trap e-
liopsis granulosa (Hoff m.) Lumbsch, AF353569, AF274119, AF381567. Tremolecia atrata (Ach.) Hertel, –, AY853397, AY853397. Umbilicaria africana (Jat ta)
Krog & Swinscow, HM161482, HM161545, HM161572. Umbilicaria aprina Ach., HM161483, HM161514, HM161573. Umbilicaria crustulosa (Ach.) Lamy,
HM161496, HM161590, HM161612. Umbilicaria proboscidea (L.) Schrad., FR799305, AY300870, AY300920. Umbilicaria spodochroa Hof fm., HM161481,
DQ986773, DQ986815. Wawea fruticulosa Henssen & Kantvilas, –, DQ007347, DQ871023. Xanthoria parietina (L.) Beltr., –, AF356687, –. Xylographa
opegraphella Rothr., Norway, E. Timdal 12066 (O L-170568), –, KF360475*, –. Xylographa parallela (Ach. : Fr.) Fr., Norway, E. Timdal 10892 (O L-152948),
KF36 0416*, KF360476*, KF360445*. Xylographa trunciseda (Th. Fr.) Redinger, Norway, R. Haugan ål2804c2 (O L-131751) , K F 36 0417*, KF360477*, –.
Xylographa soralifera Holien & Tønsberg, –, AY212849, AY212878.
♦ Sequences shorter than 200 bp:
Hypocenomyce australis 2, Australia, H. Krog Au14/2 (O L-144373), ITS1 and 5.8S ribosomal RNA gene, partial
AGGCCGAACCTCCCACCCTTTGTGTACCTTACCTTTGTTGCTTTGGCGGGCCCGTGGGGATCACCCACCGTCGGCTCCGGTTGACGCGTGCC
CGCCAGA
Hypocenomyce foveata, Australia, G. Thor 6047b (S), 5.8S ribosomal RNA gene and ITS2, partial sequences:
CTTTGAACGCACATTGCGCCCCTTGGTATTCCGGGGGGCATGCCTGTTCGAGCGTCATTGCAACCCTCAAGCGCAGCTTGGTGTTGGGCCTC
CGCCCCCCTGGGCGTGCCCGAAAAGCAGTGGCGGTCCGGGATGACTCCAAGCGAAGTAGAATTTTTCCGCTTCCGGAGTTCGCCCCGTGGC
CCGCCAGACAACCAC
Hypocenomyce sorophora 4, Sweden, E. Timdal 2908 (O L-144310), 5.8S ribosomal RNA gene and ITS2, partial sequences:
ACGCACATTGCGCCCCTTGGTATTCCGAGGGGCATGCCTGTTCGAGCGTCATTACACCACTCAAGCTCAGCTTGGTATTGGGCCTTCACCCCT
CGCGGGTGTGCCTAAAAATCAGTGGCGGTGCCGCCTGGCTTCAAGCGTAGTAATTATTTCTCGCTCTGGAAGTCCGGGTGCGTTGCCTGCCAT
CAACCCCC
Hypocenomyce tinderryensis 5, Australia, H. Streimann & J.A. Curnow 35001 (CANB-610213.1), 5.8S ribosomal RNA gene and ITS2, partial sequences:
GCACATTGCGCCCCTCGGTATTCCKAGGGGCATGCSTGTTCGAGCGTCATTACACCCCTCAAGCCCTGCTTGGTCTTGGGCCTCGTCCCCCGG
GACGTGCCCGAAAGTCAGTGGNGGCCCGGTCCGACTTCAAGCGTAGTAAATACATCATTCCGCTTTGGAAGCCTCTGGGCCGGTC
Appendix 1.
Continued.
