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Molecular phylogeny of Boliniales (Sordariomycetes) with an assessment
of the systematics of
Apiorhynchostoma
,
Endoxyla
and
Pseudovalsaria
Wendy A. Untereiner
1
Mesfin Bogale
Department of Biology, Brandon University, Brandon,
Manitoba, R7A 6A9 Canada
Adrian Carter
PO Box 1137, Cornwall, PEI, C0A 1H0 Canada
H.W. (Bud) Platt
Agriculture and Agri-Food, Charlottetown, PEI, C1A
7M8 Canada
Sven-A
˚ke Hanson
Birkagatan 49, SE-256 55 Helsingborg, Sweden
Thomas Læssøe
Department of Biology, Natural History Museum of
Denmark, University of Copenhagen, DK-1353
Copenhagen, Denmark
Va´clav S
ˇteˇpa´nek
Laboratory of Enzyme Technology, Institute of
Microbiology, Academy of Sciences, 142 20 Prague,
Czech Republic
Martina Re´blova´
Department of Taxonomy, Institute of Botany, Academy
of Sciences, 252 43 Pru
˚honice, Czech Republic
Abstract
:The systematics of the ascomycete genera
Apiorhynchostoma
,
Endoxyla
and
Pseudovalsaria
are re-
evaluated based on the comparison of cultural
characteristics, teleomorph morphology and DNA
sequence data. Analyses of sequences of the internal
transcribed spacer (ITS) of the ribosomal DNA
operon and the large subunit (LSU) of the nuclear
ribosomal DNA gene resolve Boliniales as a robustly
supported lineage comprising
Apiorhynchostoma
,
Ca-
marops
,
Camaropella
,
Cornipulvina
,
Endoxyla
and
Pseudovalsaria
. Within Boliniales, species of
Endoxyla
form a strongly supported lineage.
Apiorhynchostoma
curreyi
and
Pseudovalsaria ferruginea
group with
Cornipulvina ellipsoides
.Speciesof
Camarops
are
paraphyletic and comprise two clades, one of which
includes
Camaropella
. Boliniaceae is emended,
En-
doxyla mallochii
is described as new and
Apiorhynch-
ostoma trabicola
is considered a synonym of
Apior-
hynchostoma altipetum
.Wealsoproposethe
combinations
Endoxyla occulta
,
Endoxylina luteobasis
and
Jobellisia peckii
. Keys to genera included in the
Boliniaceae and to species of
Apiocamarops
,
Apior-
hynchostoma
and
Endoxyla
are provided.
Key words:
Boliniaceae, hyaline cap, infrequently
collected microfungi, lignicolous pyrenomycetes, po-
rate ascospores, systematics
INTRODUCTION
Species of
Apiorhynchostoma
Petrak and
Endoxyla
Fuckel are morphologically similar ascomycetes
found primarily on the wood of gymnosperms in
central and northern Europe and North America
(Untereiner 1993, Rogers et al. 1994b). Members of
both genera possess immersed, perithecial ascomata
with stout necks, unitunicate asci with an inamyloid
apical ring and brown porate ascospores (Mu¨ller and
von Arx 1962, Untereiner 1993). Their stromata are
usually poorly developed and evident only as dark-
ened or discolored wood around or between the
ascomata (Untereiner 1993, Rappaz 1995); in some
species the stromata are described as clypeate
(Sivanesan 1975, Re´blova´ 1998, Wang et al. 2004).
Ascospores of species of
Apiorhynchostoma
are two-
septate and consist of two dark brown cells and a
small, terminal hyaline cell. The brown cell farthest
from the hyaline cell is smaller and possesses a
terminal germ pore (Mu¨ ller and von Arx 1962) that is
covered by an indistinct hyaline cap or appendage
(Sivanesan 1975, Rappaz 1995). Species of
Endoxyla
possess brown, porate ascospores that are septate or
aseptate (Untereiner 1993), and a hyaline cap does
not cover the porate end of the ascospore.
Apiorhynchostoma
and
Endoxyla
are considered
closely related (Untereiner 1993, Rogers et al.
1994b, Re´blova´ 1998), but their taxonomic positions
have remained uncertain. Both genera have been
included in the Clypeosphaeriaceae and have been
compared to
Clypeosphaeria
Fuckel (Barr 1989, 1990;
Untereiner 1993; Rogers et al. 1994b; Re´blova´ 1998;
Wang et al. 2004).
Apiorhynchostoma
and
Endoxyla
also have been treated as members of the Boliniales
(Rappaz 1995, Huhndorf and Miller 2008), an order
inferred as closely related to the Chaetosphaeriales
and Sordariales based on the phylogenetic analysis of
four loci (Zhang et al. 2006).
Determining the phylogenetic positions of
Apior-
hynchostoma
and
Endoxyla
has proven challenging
because these species are collected infrequently.
Endoxyla macrostoma
Fuckel, the type species of the
Submitted 11 Sep 2012; accepted for publication 8 Nov 2012.
1
Corresponding author. E-mail: untereiner@brandonu.ca
Mycologia,
105(3), 2013, pp. 564–588. DOI: 10.3852/12-326
#2013 by The Mycological Society of America, Lawrence, KS 66044-8897
564
genus, has been reported from only three collections
outside Fuckel’s herbarium (Untereiner 1993, Re´-
blova´ 1998, Johnova´ 2009), while
A. altipetum
(Peck)
Rappaz,
A. occultum
Re´blova´,
A. trabicola
You Z.
Wang, Aptroot & K.D. Hyde.,
A. tumulatum
(Cooke)
Sivan. and
E. xanthostroma
Unter. are known from
two or fewer collections (Sivanesan 1975, Untereiner
1993, Rappaz 1995, Re´blova´ 1998, Wang et al. 2004,
Johnova´ 2009). Attempts to obtain cultures of species
of
Apiorhynchostoma
and
Endoxyla
have proven
unsuccessful (Untereiner 1993, Re´blova´ 1998); as a
consequence, the members of these genera are
unrepresented in culture collections and in molecu-
lar phylogenetic studies.
In 2007 we cultured
Apiorhynchostoma curreyi
(Rabenh.) E. Mu¨ ller from material collected in
Sweden. Shortly thereafter we were able to culture
Pseudovalsaria ferruginea
(Nitschke) Rappaz and a
number of species of
Endoxyla
collected in Canada.
One collection of
Endoxyla
represented an unde-
scribed species. Prompted by the availability of
cultures and fresh collections of these taxa, we
obtained nuclear ribosomal gene sequences (rDNA)
and examined the phylogeny of these genera and
their closest relatives. Based on the examination of
recent collections and existing herbarium material,
we describe this new species in
Endoxyla
, propose the
new combination in
Endoxyla
for
Apiorhynchostoma
occultum
, reduce
A. trabicola
to synonymy with
A.
altipetum
and accept a single species,
P. ferruginea
,in
Pseudovalsaria
Spooner. We also propose the combi-
nation in
Endoxylina
Romell for
Sphaeria luteobasis
Ellis and transfer
Valsa peckii
Howe to
Jobellisia
M.E.
Barr. Our analyses of rDNA gene sequences confirm
the placement of
Apiorhynchostoma
,
Endoxyla
and
Pseudovalsaria
in Boliniales.
MATERIALS AND METHODS
Fungal strains and cultural studies.—
The isolates examined
in this study (TABLE I) were obtained from freshly collected,
air-dried collections by streaking the contents of mature
ascomata on modified Leonian’s agar (MLA) (Malloch
1981) containing 2.5%agar, chlortetracycline (50 mg/mL)
and streptomycin sulfate (50 mg/mL). Individual or groups
of germinating ascospores were subcultured to MLA
containing 1.5%agar and maintained at room temperature
(20–21 C). Ascomata of species of
Endoxyla
also were
streaked on MLA amended with the chemical adsorbents
1%bovine serum albumin (BSA, Sigma A-7030, Sigma-
Aldrich, Oakville, Ontario) or 1%a-cyclodextrin (Sigma
C-4642) (Denison 2003).
For comparative purposes, cultures were grown on
filtered oatmeal agar (CBSOA) (Gams et al. 1987),
cornmeal agar (CMA) (Gams et al. 1987) using only 30 g
ground cornmeal, 2%malt extract agar (MEA), MLA and
oatmeal agar (OA) (Tuite 1969). Plates were inoculated in
triplicate with 2 32 mm squares cut from the actively
growing edges of colonies on MLA and incubated at room
temperature. Colony diameter was measured and descrip-
tions of colony morphology were made at 7 d intervals for
21 d. Color descriptions are based on Kornerup and
Wanscher (1978). Unless noted, the color of the reverse
of colonies was the same as the colony surface.
Microscopic examinations of cultures and specimens
were made from preparations mounted in distilled water,
lactophenol containing 0.1%cotton blue (Kirk et al. 2001)
or Melzer’s reagent (Malloch 1981). Asci and ascospores
also were observed from preparations mounted in 1%
aqueous Janus green B (JGB) following removal of stain in
distilled water. Freehand sections of the ascomata and
substratewereexaminedtodeterminetheextentof
stromatal development. The acronyms of herbaria are those
used by Holmgren et al. (1990).
Extraction, amplification and sequencing of DNA.—
Cultures
used for DNA isolations were grown as described in
TABLE I. Sources and accession numbers of the isolates sequenced in this study
Taxon Substrate and geographic origin Sources
a
GenBank accession nos.
ITS LSU
Apiorhynchostoma
curreyi
Decorticated wood of
Pinus sylvestris
L., Sweden
C, UAMH 11088 JX460984 JX460989
Endoxyla macrostoma
Decorticated wood of
Pinus strobus
L., Canada
NBM, UAMH 11491 JX460985 JX460990
E. mallochii
Decorticated wood (
Abies
sp.
or
Picea
sp.), Canada
NBM, UAMH 11087 JX460986 JX460991
E. operculata
Decorticated wood of
Populus
cf.
balsamifera
L., Canada
NBM, UAMH 11085 JX460987 JX460992
Pseudovalsaria
ferruginea
Decorticated wood of
Populus
sp.,
Canada
NBM, UAMH 11490 JX460988 JX460993
a
Vouchers are deposited in the University of Copenhagen Herbarium (C), Copenhagen, Denmark, or in the New Brunswick
Museum (NBM), St John, Canada. Cultures are deposited in the University of Alberta Microfungus Collection and Herbarium
(UAMH), Edmonton, Canada.
UNTEREINER ET AL.: MOLECULAR PHYLOGENY OF BOLINIALES 565
Untereiner et al. (1995) and Re´ blova´ et al. (2011). Total
nucleic acids were extracted from mycelia following the
protocols of Lee and Taylor (1990) or Re´ blova´ et al. (2011).
Methods for amplifying and sequencing the internal
transcribed spacer (ITS) and the large subunit (LSU) of
the nuclear rDNA gene are described in Bogale et al. (2010)
and Re´blova´ et al. (2011). Primers used in the amplification
and sequencing of the ITS included ITS4, ITS5, NS5 (White
et al. 1990), LR0R (Rehner and Samuels 1994), LR1 and
5.8SR (Vilgalys and Hester 1990, Hopple and Vilgalys 1999);
primers used to amplify and sequence the LSU included
LR5, LR6, LR7, LR8, LR16 (Vilgalys and Hester 1990,
Hopple and Vilgalys 1999), JS7 and JS8 (Landvik 1996).
Sequence alignment and phylogenetic analyses.—
Newly gen-
erated sequences were compared to homologous sequences
retrieved from GenBank, primarily from studies of Re´ blova´
et al. (2004), Spatafora et al. (2006), Zhang et al. (2006),
Huhndorf and Miller (2008) and Re´blova´ et al. (2011).
Sequences were manually aligned in BioEdit 7.0.9.0 (Hall
1999). The LSU alignment was enhanced with the
homologous 2D structure of
Saccharomyces cerevisiae
Meyen
ex E.C. Hansen (Gutell et al. 1993). All characters in the ITS
alignment were included in phylogenetic analyses, but we
excluded bp 1–73 from the LSU dataset because of the
incompleteness of the 59– end of the majority of the
available sequences. The combined ITS and LSU dataset
was partitioned into two subsets, ITS (ITS1-5.8S-ITS2) and
LSU. Alignments are deposited in TreeBASE (accession
number 13254).
The positions of
Apiorhynchostoma
,
Endoxyla
and
Pseudo-
valsaria
within Boliniales (Sordariomycetidae) were in-
ferred based on the analysis of the LSU sequences of 77
taxa representing 13 orders or families of Sordariomycetes.
Saccharomyces cerevisiae
and
Vanderwaltozyma polyspora
(van
der Walt) Kurtzman (Saccharomycetes) were used as
outgroup taxa. We also analyzed the combined ITS and
LSU of sequences of 12 taxa belonging to Boliniales,
Chaetosphaeriales and Sordariales. Outgroup taxa for these
analyses included
Chaetosphaeria innumera
Berk. & Broome
ex Tul. & C. Tul.,
C. pulviscula
(Curr.) C. Booth and
C.
vermicularioides
(Sacc. & Roum.) W. Gams & Hol.-Jech.
MrModeltest 2.3. (Nylander 2008) was used to infer the
appropriate substitution model that would best fit the
model of DNA evolution for our datasets. Maximum
likelihood (ML) and Bayesian inference (BI) analyses were
used to estimate phylogenetic relationships. ML analysis was
performed with RAxML-HPC 7.0.3 (Stamatakis 2006) using
GTR +I+G(LSU datasets) and GTR +G(ITS dataset) models
of evolution. Nodal support was verified by nonparametric
bootstrapping (BS) with 1000 replicates. BI analysis was
performed in a likelihood framework as implemented by
MrBayes 3.0b4 (Huelsenbeck and Ronquist 2001). Multiple
Bayesian searches were conducted using Metropolis-cou-
pled Markov chain Monte Carlo sampling. One cold and
three heated Markov chains were conducted. Analyses were
run 5 000 000 generations, with trees sampled every 1000
generations. The first 20 000 trees, representing the burn-in
phase of the analysis, were discarded. To estimate posterior
probabilities (PP) of recovered branches (Larget and Simon
1999), 50%majority rule consensus trees were created from
the remaining trees with PAUP* 4.0b 10 (Swofford 2003).
RESULTS
Ascospores from fresh, air-dried collections of
Apior-
hynchostoma curreyi
,
Endoxyla macrostoma
,
E. opercu-
lata
(Fr.: Fr.) Sacc. and
Pseudovalsaria ferruginea
germinated within 36–72 h on MLA by forming single
germ tubes that emerged through the germ pore (not
shown). Macroscopically visible colonies were evident
on MLA within 5 d. The ascospores of the unnamed
species of
Endoxyla
were never observed to germinate
on MLA or on MLA containing BSA and a-cyclodex-
trin, but slow growing, orange-white colonies origi-
nated from the remnants of ascomata on all media.
All species produced flat, white or yellow to orange
colonies that consisted largely or entirely of an
immersed mycelium. Conidial anamorphs were not
observed on any of the media used.
The LSU dataset for 77 taxa contained 1286
characters of which 395 were phylogenetically infor-
mative. The ML phylogram and a detailed view of a
robustly supported clade (ML bootstrap 595%,PP5
1.0) within the subclass Sordariomycetidae containing
Boliniales, Chaetosphaeriales, Coniochaetales and
Sordariales are illustrated (FIG. 1). ML analysis of
these data (mean likelihood 5212912; transitions A–
C50.925, A–G 52.845, A–T 51.725, C–G 50.833,
C–T 57.890) resolved Boliniales as a strongly
supported clade (81/0.98) that was sister to Chaeto-
sphaeriales (FIG. 1). Within Boliniales, species of
Endoxyla
comprisedamonophyleticgroup(50/
0.75) that was sister to a lineage comprising two
subclades. The first subclade (61/0.97) included
Apiorhynchostoma curreyi
,
Cornipulvina ellipsoides
Huhndorf, A.N. Mill., F.A. Ferna´ndez & Lodge and
Pseudovalsaria ferruginea
; the second subclade (53/
0.98) consisted of five species of
Camarops
(
C. petersii
[Berk. & M.A. Curtis] Nannf.,
C. polysperma
[Mont.]
J.H. Mill.,
C. rogersii
Huhndorf & Miller,
C. tubulina
[Alb. & Schwein.] Shear and
C. ustulinoides
[Henn.]
Nannf.).
Camarops amorpha
(Boedijn) Nannf. and
C.
microspora
(P. Karst.) Shear grouped with species of
Camaropella
Lar.N. Vassiljeva in a lineage (53/0.94)
that was sister to the clade encompassing
Apiorhynch-
ostoma
,
Cornipulvina
Huhndorf, A.N. Mill., F.A.
Ferna´ndez & Lodge,
Endoxyla
,
Pseudovalsaria
and
five other species of
Camarops
.
The combined ITS and LSU dataset for 12 taxa
consisted of 1808 characters; 263 of these were
phylogenetically informative. In the ML tree (mean
likelihood 526690; ITS partition transitions A–C 5
0.620, A–G 512.054, A–T 514.472, C–G 510.398,
C–T 537.101; LSU partition transitions A–C 50.456,
566 MYCOLOGIA
FIG. 1. Phylogram inferred from ML analysis of LSU rDNA sequences. Part A depicts the entire phylogeny whereas part B shows in detail the robustly supported clade
containing Boliniales, Chaetosphaeriales, Coniochaetales and Sordariales. ML bootstrap and BI posterior probabilities are indicated at the nodes. Branches receiving
significant support (ML BS 5100%,PP51.0) are indicated by an oval.
UNTEREINER ET AL.: MOLECULAR PHYLOGENY OF BOLINIALES 567
A–G 51.278, A–T 50.876, C–G 50.384, C–T 5
5.566), the Boliniales was resolved as a robust clade
(100/1.0) containing two subclades (FIG. 2). Within
the first subclade (96/0.98), species of
Endoxyla
formed a strongly supported monophyletic group
(99/1.0) that was sister to a lineage that included
Camarops polysperma
and
C. ustulinoides
(100/1.0).
The second subclade (2/0.74) included
Apiorhynch-
ostoma curreyi
and
Pseudovalsaria ferruginea
.
DISCUSSION
Boliniaceae, although traditionally allied with the
Xylariales (Munk 1953, Barr 1990, Romero and
Samuels 1991), was shown by Andersson et al.
(1995) to be more closely related to Sordariales based
on the analysis of small subunit ribosomal DNA
sequences. The family, together with Catabotryda-
ceae, was placed subsequently in Boliniales (Kirk et al.
2001). Recent molecular phylogenies demonstrate
that the closest relatives of Boliniaceae within
Sordariomycetes include Chaetosphaeriales, Conio-
chaetales and Sordariales (Huhndorf et al. 2004,
Miller and Huhndorf 2005, Zhang et al. 2006).
Catabotrydaceae is a monotypic family based on
Catabotrys decidua
(Berk. & Broome) Seaver &
Waterson, a widespread species found on the dead
leaves and petioles of tropical monocots that forms
long-necked, perithecial ascomata in superficial,
pulvinate stromata, and ellipsoid, hyaline to lightly
pigmented ascospores (Seaver and Waterson 1946,
Petrak 1954, Barr 1990). Although it is morphologi-
cally similar to some Boliniaceae,
C. decidua
is not
closely allied to this family and was excluded from
Boliniales (Huhndorf et al. 2004). Analysis of a
combined b-tubulin-LSU-RPB2 dataset indicates that
C. decidua
is a member of Diaporthales (Miller and
Huhndorf 2005), but the description of the apical
ring of the asci of
C. decidua
as amyloid (Dingley
1977) supports the earlier suggestion (Hyde et al.
2000) that this species might belong to Xylariales.
Our analyses of LSU sequence data resolve
Apiorhynchostoma
,
Camaropella
,
Camarops
,
Cornipul-
vina
,
Endoxyla
and
Pseudovalsaria
as members of
Boliniales (FIG. 1) and are consistent with molecular
phylogenies that include this order as a strongly
supported lineage within Sordariomycetes (Huhndorf
et al. 2004, Miller and Huhndorf 2005, Zhang et al.
FIG. 2. Phylogram inferred from ML analysis of a combined data ITS-LSU rDNA sequences. ML bootstrap and BI posterior
probabilities are indicated at the nodes. GenBank accession numbers given in the tree after the names are those of ITS/LSU.
Branches receiving significant support (ML BS 5100%,PP51.0) are indicated by an oval.
568 MYCOLOGIA
2006). Molecular data of other genera classified in
Boliniales based on morphology (i.e.
Apiocamarops
Samuels & J.D. Rogers,
Mollicamarops
Lar.N. Vassil-
jeva and
Neohypodiscus
J.D. Rogers, Y.M. Ju & Læssøe)
are not available. Within Boliniales, members of the
genus
Endoxyla
form a strongly supported group that
is not closely related to the morphologically similar
species
A. curreyi
.
Apiorhynchostoma curreyi
, the type
species of the genus, and
P. ferruginea
group with
Corn. ellipsoides
, a species with soft-textured stromata
and hyaline, unicellular ascospores (Huhndorf et al.
2005).
Camarops
, which was inferred to be paraphy-
letic by Huhndorf and Miller (2008), is represented in
our phylogeny by seven species divided between two
clades. One of these clades encompasses two species
of
Camaropella
. Analyses of the combined ITS and
LSU sequences confirms the close relationship of
species of
Endoxyla
(FIG. 2) and resolves these species
as close relatives of
Camarops polysperma
and
C.
ustulinoides
. These species comprise a strongly sup-
ported clade that is sister to a lineage encompassing
A. curreyi
and
P. ferruginea
.
Our results are consistent with investigations that
reported the absence of conidial anamorphs in Boli-
niales (Horn 1984, Petrini 1986, Samuels and Rogers
1987, Callan and Rogers 1989, Rogers et al. 1994a, Ju et
al. 1996, Del Valle Catania and Romero 2003). None of
taxa that we studied in vitro formed fertile ascomata.
Taxa within Boliniales are delimited primarily on
the basis of stromatal, ascomatal and ascospore
morphology, but these characters vary considerably
within some genera and it has yet to be determined
whether the separation of taxa using these features is
supportable. For example, the stromata of
Camarops
,
the largest genus in the order, range from applanate
to peltate or turbinate, can be hard and strongly
carbonized or soft-textured, and dark to lightly or
brightly colored. Species of
Camaropella
were segre-
gated from this genus because of their immersed,
valsoid stromata and clustered long-necked ascomata
(Vasilyeva 1997, Vasilyeva et al. 2007), but they are
inferred in this study and others (Huhndorf and
Miller 2008, Raja et al. 2011) to be close relatives of
species of
Camarops
not sharing these morphological
characteristics. The ascospores of species of
Endoxyla
,
the second-largest genus in Boliniales, are nonseptate,
one- or two-septate and may possess a hyaline cell. Our
phylogenies demonstrate that species of
Endoxyla
possessing two-septate ascospores with a hyaline cell
are more closely related to
E. operculata
than to
A.
curreyi
, a species with morphologically similar asco-
spores, but a limited number of the representatives of
both genera were included in this study. Another
feature that warrants attention in future phylogenetic
studies of the Boliniales is the hyaline cap or
noncellular appendage that covers the germ pore of
the ascospores of some of the members of this order.
This structure, which is interpreted as a localized
thickening of the ascospore wall (Winter 1886; Mu¨ller
and von Arx 1962; Rogers et al. 1994a, 2006; Rappaz
1995), is evident in all species of
Apiorhynchostoma
and
Neohypodiscus
and also has been described for one
member of the genus
Camarops
. The hyaline cap is
often indistinct, but among the taxa examined in this
study, it is best seen in Melzer’s reagent or in
preparations stained with JGB.
TAXONOMY
Boliniaceae Rick emend. Unter. & Re´blova´
Stromata immersed to superficial, often erumpent
through the wood or bark of the host plant, crustose,
applanate, peltate, pulvinate, turbinate or clavate,
occasionally irregular and grotesque, hard- or soft-
textured, dark or brightly colored. Ascomata immersed
within the stromata, perithecial, monostichous or
polystichous, with short or elongate necks. Asci
persistent, cylindrical to clavate, long-stipitate, with an
indistinct, inamyloid apical ring. Ascospores hyaline or
various shades of brown, ellipsoid to suballantoid,
sometimes compressed laterally, aseptate, one- or two-
septate, with an inconspicuous apical germ pore that
may be covered by an indistinct hyaline cap, occasion-
ally with a germ pore at both ends, uniseriate within the
asci or biseriate and becoming uniseriate below.
Paraphyses abundant, filiform, longer than the asci.
On the bark and decorticated wood of angiosperms
and gymnosperms, occasionally on polypores, world-
wide. Conidial anamorphs not observed in situ and in
vitro.
KEY TO GENERA OF BOLINIACEAE
1. Stromata immersed, poorly developed to valsoid or
pustulate .............................. 2
1. Stromata erumpent or superficial, crustose to
turbinate or clavate or irregular and grotesque . . 5
2. Stromata poorly developed, typically evident
only as a darkening of the wood surface or the
wood surrounding the ascomata ......... 3
2. Stromata well developed, valsoid or pustu-
late . . . ............................ 4
3. Ascospores brown, two-septate, with a hyaline cell,
porate end covered by an indistinct hyaline
cap .......................
Apiorhynchostoma
3. Ascospores brown, aseptate, one- or two-septate,
with or without a hyaline cell, porate end not
covered by a hyaline cap . . ...........
Endoxyla
4. Ascospores brown, aseptate . . . . .
Camaropella
4. Ascospores brown, one-septate . . .
Pseudovalsaria
5. Ascospores hyaline ..............
Cornipulvina
UNTEREINER ET AL.: MOLECULAR PHYLOGENY OF BOLINIALES 569
5. Ascospores brown or consisting of a brown cell and
a smaller hyaline cell . . ................... 6
6. Ascospores one-septate, consisting of a larger,
porate brown cell and a smaller hyaline
cell ......................
Apiocamarops
6. Ascospores aseptate, one- or two-septate,
entirely brown ...................... 7
7. Stromata hard, ascospores with a hyaline cap at
one or both ends ..............
Neohypodiscus
7. Stromata hard or soft-textured, ascospores lacking
a hyaline cap ........................... 8
8. Stromata thin, soft-textured and brightly
colored, ascomata with stellate ostio-
les ......................
Mollicamarops
8. Stromata thick or thin, typically hard, occa-
sionally soft-textured, ostioles non-stella-
te ...........................
Camarops
Apiocamarops
Samuels & J.D. Rogers, Mycotaxon
28:54. 1987.
MycoBank MB25015
Type species: Apiocamarops alba
Samuels & J.D. Rogers
Specimens examined: Apiocamarops alba
. BRAZIL. Amazo-
nas: Plateau of Serra Araca. 19–24 Feb 1984,
G.J. Samuels
486
,
G.T. Francis and J. Pipoly
(NY, HOLOTYPE); data as
for holotype,
G.J. Samuels 438
,
G.T. Francis and J. Pipoly
(NY). FRENCH GUIANA. Circa 17 km SW of Sa¨ul toward
Mount Galbao, 24, 26, 28 Jan 1986,
G.J. Samuels 3301 and
J.R. Boise
(NY); On road between Sinnary and St Elie,
ECEREX OSTROM Research Area, 20–29 Feb, 1 Mar 1986,
G.J. Samuels 3816
(NY); ca. 10 km SW of Sa¨ul toward Mount
Galbao, Jan–Feb 1986,
G.J. Samuels 3696 and J.R. Boise
(NY);
Paul Isnard Area, Mounts Lucifer and Decou Decou, ca.
150 km S of St Laurent du Maroni, 7–17 Mar 1986,
G.J.
Samuels 4114
(NY); vic. Cayenne, 25 Mar 1986,
G.J. Samuels
4454 and C. Feuillet
(NY).
Apiocamarops cryptocellula
.
GUYANA. Cuyuni-Mazaruni region, foothills S of Mount
Ayanganna, ca. 1 km W of the Pong River, 26 Feb 1987,
G.J.
Samuels 4836
,
J. Pipoly and G. Gharbarran
(NY, HOLOTYPE).
Comments: Apiocamarops
includes species charac-
terized by their superficial, soft-textured to woody,
white to yellowish or orange stromata, and ascospores
that consist of a larger, brown porate cell and a
smaller, hyaline nonporate cell (Samuels and Rogers
1987, Rogers and Samuels 1988, Rogers and Ju 2003).
Apiocamarops alba
, the only species studied in axenic
culture, does not produce a conidial anamorph
(Samuels and Rogers 1987). The two other members
of the genus,
A. cryptocellula
J.D. Roger & Samuels and
A. pulvinata
J.D. Rogers & Ju, have not been cultured.
Species of
Apiocamarops
occur on bark and
decorticated wood, and are known from Central and
South America (i.e. Brazil, Costa Rica, French Guiana,
Guyana, Venezuela) (Samuels and Rogers 1987,
Rogers and Samuels 1988, Rogers and Ju 2003). The
members of this genus are similar anatomically to
Camarops
(Samuels and Rogers 1987), but the
relationship among them has yet to be evaluated
based on molecular data.
KEY TO SPECIES OF
A
PIOCAMAROPS
1. Ascomata superficial, seated directly on wood and
united in a white to yellowish furfuraceous stroma,
ascospores (5–)6–9(–11.5) 3(2.7–)3–3.7(–4)
mm ..............................
A. alba
1. Ascomata immersed in a woody, pulvinate to
discoid stroma . ......................... 2
2. Ascospores 4.5(–5) 32.5(–3) mm....
A. pulvinata
2. Ascospores 6.6–8 33.7 mm, hyaline cell often
collapsing .................
A. cryptocellula
Apiorhynchostoma
Petrak, Ann. Mycol. 21:185. 1923.
MycoBank MB261
Type species
:
Apiorhynchostoma curreyi
(Rabenh.) E.
Mu¨ller
Comments:
Species of
Apiorhynchostoma
possess
immersed, solitary to gregarious, flask-shaped asco-
mata surrounded by a reduced hyphal stroma that is
evident as a darkening of the substrate around the
ostioles and between the ascomata, and two-septate,
uniporate ascospores that consist of two brown cells
and a smaller, terminal hyaline cell (Mu¨ller and von
Arx 1962, Sivanesan 1975, Rappaz 1995). The
members of this genus are distinguished from
Endoxyla
in possessing ascospores with an apical pore
covered by an indistinct hyaline cap. Also, the species
examined are characterized by asci with an apical ring
that stains in JGB. Species of
Apiorhynchostoma
occur
on the decayed, decorticated wood of gymnosperms
in Europe and North America.
Apiorhynchostoma
has been included in the Amphi-
sphaeriaceae and the Clypeosphaeriaceae (Xylariales)
(Barr 1990, 1994; Untereiner 1993; Rogers et al.
1994b; Hyde et al. 1998; Re´blova´ 1998; Kang et al.
1999; Wang et al. 2004) but our phylogenies position
A. curreyi
in the Boliniales. Within this order
A.
curreyi
is most closely related to
Cornipulvina
and
Pseudovalsaria
(FIGS. 1, 2).
KEY TO SPECIES OF
A
PIORHYNCHOSTOMA
1. Ascospores (13–)15–16(–19) 34–6 mm. ....
A. altipetum
1. Ascospores larger ........................ 2
2. Ascospores 20–24(–27) 37–10 mm ...
A. curreyi
2. Ascospores 25–35 39–12 mm ....
A. tumulatum
Apiorhynchostoma altipetum
(Peck) Rappaz, Mycologia
Helvetica 7:153. 1995.
MycoBank MB363311
570 MYCOLOGIA
FIGS. 3–13.
Apiorhynchostoma curreyi
and
Endoxyla macrostoma
. 3–9.
Apiorhynchostoma curreyi
. 3, 4. Tips of ascomatal necks
emerging from the decorticated wood. 5–7. Ascospores, arrows indicate the hyaline cap. 8. Upper part of the ascus bearing
spores. 9. Ascus with distinct apical annulus. 10–13.
Endoxyla macrostoma
. 10, 11. Tips of ascomatal necks emerging from the
decorticated wood. The ascomata are monostichous, immersed and arranged in rows. 12. Longitudinal section of ascomata.
13. Ascospores. 3–9 from S.-A
˚. Hanson 2007-278; 10–13. from M. Re´blova´ 1066. Bars: 3, 4, 10–12 5500 mm; 5–9, 13 510 mm.
UNTEREINER ET AL.: MOLECULAR PHYLOGENY OF BOLINIALES 571
;
Sphaeria altipeta
Peck, Bot. Gaz. 5:34. 1880.
;
Rhynchostoma altipetum
(Peck) Sacc., Syll. Fung. 1:731.
1882.
;
Entosordaria altipeta
(Peck) Ho¨hnel, Sitz. Kaiserl. Akad.
Wiss. Math.-Naturwiss. Cl. Abt 1, 129:183. 1920.
5
Apiorhynchostoma trabicola
You Z. Wang, Aptroot & K.D.
Hyde., Fungal Divers. Res. Ser. 13:142. 2004.
See Rappaz (1995) and Wang et al. (2004) for
descriptions and illustrations of this species.
Habitat:
On rotten, decorticated wood of conifers.
Distribution:
Czech Republic, Sweden, Switzerland,
USA (type locality).
Specimens examined:
SWEDEN.
E.M. Fries
, Scleromyceti
Sueciae 268 (1st ed.), (FH, as
Sphaeria operculata
, collection
mixed). SWITZERLAND. Zu¨rich: Tagelswangen, on wood
of
Abies alba
, 5 Dec 1955,
A. Tonolo
(Z, as
Apiorhynchostoma
apiculata
). USA. New Hampshire: Mount Washington, on
decaying wood,
C.G. Pringle 328
(NYS, HOLOTYPE of
Sphaeria altipeta
).
Comments:
Johnova´ (2009) reported this species
from the Czech Republic but did not cite collection
data.
Apiorhynchostoma altipetum
is distinguished
from the other members of the genus by its smaller
ascospores. The configuration of the ascomata of
A.
altipetum
is reminiscent of
Endoxyla operculata
, and
we examined one collection (Scl. Sueciae 268, 1st ed.)
that contained a mixture of wood fragments bearing
the ascomata of both species. Because we cannot
separate
A. trabicola
from
A. altipetum
based on the
description provided by Wang et al. (2004), we
consider these taxa to be conspecific.
Apiorhynchostoma curreyi
(Rabenh.) E. Mu¨ ller, Beitr.
Kryptogamenfl. Schweiz 11:707. 1962. FIGS. 3–9
MycoBank MB326365
;
Sphaeria curreyi
Rabenh., Fung. Europ. 250. 1860.
5
Sphaeria apiculatum
Curr., Trans. Linn. Soc. London 22:326,
1859,
non
Wallroth, Fl. Cryptogamica Germ. 2:778. 1833.
;
Anthostoma apiculata
(Curr.) Niessl
apud
Kunze, Fungi
Sel. exs. 267. 1880 (fide Mu¨ller and von Arx 1962).
;
Valsaria apiculata
(Curr.) Sacc., Syll. Fung. 1:752. 1882.
;
Rhynchostoma apiculatum
(Curr.) Winter, Rabenh.
Krypt.-Fl. 1:762. 1887.
;
Xylosphaeria apiculata
(Curr.) Cooke, Grevillea 17:86.
1889.
;
Phaeosperma apiculatum
(Curr.) Sacc. & Traverso, Syll.
Fung. 20:326. 1911.
;
Entosordaria apiculata
(Curr.) Ho¨hnel, Sitz. Kaiserl.
Akad. Wiss. Math.-Naturwiss. Cl. Abt 1, 129:166. 1920.
;
Apiorhynchostoma apiculatum
(Curr.) Petrak, Ann.
Mycol. 21:185. 1923.
;
Lopadostoma apiculatum
(Curr.) P. Martin, J. S. African
Bot. 42:75. 1976.
5
Anthostoma trabeum
Niessl, Beitr. z. Kenntn. Pilze p. 56.
1872.
See Mu¨ ller and von Arx (1962), Dennis (1981) and
Hyde et al. (1998) for descriptions of the tele-
omorph. Additional illustrations of this species are
provided by Currey (1859), Niessl (1872), Winter
(1886), Mu¨ ller and von Arx (1962), Dennis (1981),
Rogers et al. (1994b) and Hyde et al. (1998).
Colonies on CBSOA 6 mm in 21 d, flat, appearing
waxy, mycelium immersed entirely, orange-white
(5A2). Medium faintly cleared to 5 mm from the
growing edge of colonies. Colonies on CMA 32–
34 mm in 21 d, flat, appearing moist, mycelium
immersed entirely, light orange (5A4–5) at the center,
mycelium toward the margin brownish gray to brown-
ish orange (5C2-3). Reverse grayish orange to brownish
orange (5B-C3-4). Colonies on MEA 39–43 mm in 21 d,
aerial mycelium short, cottony, felt-like, restricted to
the colony center, white (A1), mycelium toward the
margin immersed, orange-white (5A2). Reverse
orange-white to light orange (5A2-4). Colonies on
MLA 20–21 mm in 21 d, aerial mycelium sparse, short,
restricted to the colony center, appearing felt-like,
light orange to melon (5A4–6), mycelium toward the
margin immersed, orange-white to orange gray (5A–
B2). Reverse brownish orange to grayish or light brown
(5B–C3–5). Colonies on OA 11–15 mm in 21 d, aerial
mycelium sparse, short, restricted to the colony center,
appearing powdery, white (A1), mycelium toward the
margin immersed, appearing waxy, brownish orange
(5C4–6). Reverse brownish orange to grayish or light
brown (5C–D3–4). Margin sharp and regular on MEA,
irregular and not sharply defined on all other media.
Conidial anamorph not observed.
Habitat:
On rotting, decorticated wood of conifers.
Distribution:
Austria, Canada, Germany, Sweden,
UK (type locality).
Specimens examined:
AUSTRIA. Styria: Voitsberg, in
beams of fir (
Abies
sp.), summer, G. de Niessl, Rabenhorst
Fungi Europaei 1531 (DAOM, F, as
Anthostoma trabeum
).
CANADA. British Columbia: Haida Gwaii, Graham Island,
on an exposed log over a stream, along the Yakoun River,
about 5 m north of Yakoun Lake, 16 Jul 1967,
I.M. Brodo
11643 and M.J. Shchepanek
(DAOM 133701). GERMANY.
Hamburg: Sachsenwald, near Hamburg, on wood of
Picea
excelsa
(5
P. abies
),
O. Jaap
, Rehm Ascomyceten 1614b (FH,
as
Rhynchostoma apiculatum
); Oberbayern: Thal near
Thalham, on decaying conifer wood, Jun 1905,
H. Rehm
,
Rehm Ascomyceten 1614 (FH, as
R. apiculatum
); Saxony:
Ko¨nigstein, on old barriers made of conifer wood, May and
Jun 1885 and 1886,
W. Krieger
, Fungi Saxonici 176
Anthostoma apiculatum
(FH, TRTC ex herb. R.F. Cain
No. 4745); Saxony: Helfta near Eisleben, on decorticated
wood of
Pinus sylvestris
, Oct 1879,
J. Kunze
, Fungi Selecti
Exsiccatii 267 (DAOM, FH, as
A. apiculatum
. SWEDEN,
Scania: A
˚hus, Gropaha˚ lets NR, on wood of
Pinus sylvestris
,
25 Jul 2007,
S.-A
˚. Hanson 2007-278
(C; living culture
572 MYCOLOGIA
UAMH 11088 [mass-ascospore isolate]). UK. Batheaston, on
adecayingwoodenfence,1866and1857,
F. Currey
,
Rabenhorst Fungi Europaei 250 (DAOM, ISOTYPE, as
Sphaeria curreyi
); Surrey: Weybridge, Oct 1857,
F. Currey
(K,
HOLOTYPE of
S. apiculata
); Surrey: Shere, May 1865,
M.C.
Cooke
, Fungi Britannici Exsiccati 272 (K, as
S. apiculata
);
Norfolk: King’s Lynn,
C.B. Plowright
, Sphaeriacei Britannici
80 (K, as
S. apiculata
).
Comments:
Judging from the availability of specimens
and the number of descriptions of this species in the
literature,
A. curreyi
is the most frequently collected
member of the genus. Although the hyaline cap covering
the porate end of the ascospores of this species (FIGS.5–
7) has not been illustrated previously, this structure is
evident in all collections examined in this study. Earlier
descriptions of the ascospores of this species (Winter
1886, Mu¨ ller and von Arx 1962) indicate that the cap was
interpreted as a localized thickening of the ascospore
wall. Niessl (1872) described the ascospores of this
species as possessing a gelatinous envelope, but we have
never observed this feature in
A. curreyi
.
As noted by Muller and von Arx (1962),
Apior-
hynchostoma
is based on
Sphaeria apiculata
, a later
homonym of
S. apiculata
Wallroth (5
Plagiostoma
salicellum
[Fr.] Sogonov). The synonymy of the
former species with
Sphaeria curreyi
was recognized
first by Winter (1886).
Anthostoma apiculatum
,as
represented by Fungi Sel. exs. 267, is cited as a
synonym of
A. curreyi
(Winter 1886, Muller and von
Arx 1962), but examples of this exsiccata examined in
the present study (DAOM, FH) are conspecific with a
specimen in Schweiniz’s herbarium (PH) under the
name
Sphaeria lineata
(Alb. & Schwein.) Cooke.
Sphaeria lineata
possesses immersed, nonstromatic
ascomata, cylindrical asci with an inamyloid apical
ring, and large (15–23 37–9 mm), brown, unicellular,
ellipsoid ascospores with a terminal germ pore, and
was identified by Untereiner (1993) as a species of
Anthostoma
Nitschke. Rogers et al. (1994b) also
examined
A. apiculatum
(NY) but did not comment
on its identity, raising the possibility that Fungi Sel.
exs. 267 represents more than a single taxon.
Apiorhynchostoma tumulatum
(Cooke) Sivan., Trans.
Brit. Mycol. Soc. 65:26. 1975.
MycoBank MB308834
;
Sphaeria tumulata
Cooke, Grevillea 7:4. 1878.
;
Amphisphaeria tumulata
(Cooke) Sacc., Syll. Fung.
1:727. 1882.
5
Anthostomella brachystoma
Ellis. & Everh., Bull. Washburn
Coll. Lab. Nat. History 1:5. 1884 (
fide
Rogers et al.
1994b).
;
Xylosphaeria brachystoma
(Ellis & Everh.) Cooke,
Grevillea 17:86. 1889.
See Sivanesan (1975) and Rogers et al. (1994b) for
descriptions and illustrations of this species.
Habitat:
On rotting, decorticated wood of
Pinus
contorta
Dougl. and
Tsuga mertensiana
(Bong.)
Carrie´re.
Distribution:
USA.
Comments: Apiorhynchostoma tumulatum
is distin-
guished from the other members of this genus by its
large ascospores. To date, this species is known only
from North America. The hyaline cap covering the
porate end of the ascospores of
A. tumulatum
noted
by Harkness and Cooke (1878), Ellis and Everhart
(1892) and Sivanesan (1975) is not evident in the
illustrations of this species provided by Rogers et al.
(1994b), suggesting that this structure may be
difficult to observe in some collections.
Camaropella
Lar.N. Vassiljeva, Mikologiya i Fitopato-
logiya, 31:6. 1997.
MycoBank MB27727
Type species: Camaropella pugillus
(Schwein.: Fr.)
Lar.N. Vassiljeva
Comments: Camaropella
encompasses species with
immersed, valsoid stromata, clustered, polystichous
ascomata with long necks that converge in an
erumpent stromatic cushion, and brown, nonseptate,
uniporate ascospores (Vasilyeva 1997, Vasilyeva et al.
2007). The two species assigned to the genus,
Camaropella lutea
(Alb. & Schwein.) Lar.N. Vassiljeva
and
Camaropella pugillus
, are distinguished by the
color of the stromata and the degree to which the
ostioles project above the wood surface (Vasilyeva et
al. 2007). Both species have been studied in pure
culture; neither produces a conidial anamorph, but
the former forms fertile ascomata (Petrini 1986, Del
Valle Catania and Romero 2003).
Camarops rostratus
Romero & Samuels, a species with immersed, pulvi-
nate stromata and long-necked ascomata (Romero
and Samuels 1991), also might belong to
Camaropella
,
according to Vasilyeva et al. (2007). Species of
Camaropella
are known from rotting wood in Europe,
North America and South America (Shear 1940,
Nannfeldt 1972, Vasilyeva 1997, Del Valle Catania
and Romero 2003, Vasilyeva et al. 2007, Huhndorf
and Miller 2008, Johnova´ 2009).
Huhndorf and Miller (2008) confirmed the place-
ment of
Camaropella
in Boliniales based on the
analysis of LSU sequences. They also identified
C.
amorpha
,
C. microspora
and
Corn. ellipsoides
as the
closest relatives of
Camaropella lutea
and
Camaropella
pugillus
, but the clade comprising these species was
weakly supported (Huhndorf and Miller 2008). The
results of our analyses of LSU sequences of 77
members of the Sordariomycetes including 16 repre-
sentatives of the Boliniales (FIG.1) confirm the
UNTEREINER ET AL.: MOLECULAR PHYLOGENY OF BOLINIALES 573
position of
C. amorpha
and
C. microspora
as close
relatives of
Camaropella
and indicate that
Camaropella
could be expanded to include these two species of
Camarops
. For a key to the species of
Camaropella
,see
Vasilyeva et al. (2007).
Camarops
P. Karst., Bd. Ka¨nn. Finl. Nat. Folk 23:6.
1873.
MycoBank MB775
Type species: Camarops hypoxyloides
P. Karst. (5
C.
polysperma
[Mont.] J.H. Mill.)
Comments: Camarops
, which currently includes
more than 25 species, encompasses taxa characterized
by their superficial, applanate or pulvinate to peltate
or turbinate stromata that typically consists of a
compact (and sometimes strongly carbonized) ectos-
troma and a loose entostroma, obpyriform to tubular
ascomata, and small, brown, uni- or biporate asco-
spores that are usually noticeably flattened (Shear
1938, Nannfeldt 1972, Hilber and Hilber 1980,
Rogers and Samuels 1987, Samuels and Rogers
1987, Rogers and Ju 2003, Rogers et al. 2006). Within
the genus,
C. flava
Samuels & J.D. Rogers and
C.
rogersii
are distinctive in possessing thin, soft and
brightly colored stromata (Samuels and Rogers 1987,
Huhndorf and Miller 2008). The former species is
also the only member of the genus with ornamented
ascospores (Samuels and Rogers 1987).
Camarops
antillana
J.D. Rogers, Lechat & J. Fourn. forms soft-
textured, pulvinate, externally blackened stromata
and ascospores with a germ pore that is covered by a
hyaline thickening of the perispore (Rogers et al.
2006). As noted above, two members of the genus
with immersed, valsoid stromata and clustered, long-
necked ascomata have been segregated to
Camar-
opella
(Vasilyeva 1997, Vasilyeva et al. 2007).
A number of
Camarops
have been studied in pure
culture; none have been observed to form a conidial
anamorph, but two species,
C. petersii
and
C.
spathulata
(Berk. & Broome) Nannf., produce tele-
omorphs in vitro (Horn 1984, Callan and Rogers
1989, Del Valle Catania and Romero 2003). Del Valle
Catina and Romero (2003) provided a key to the
members of the genus from Argentina.
Species of
Camarops
are found worldwide and have
been collected in Africa, Asia, Europe, North America
and South America, where they occur on the
corticated branches and trunks of angiosperms, on
decaying, decorticated wood of angiosperms and
gymnosperms (Shear 1938; Nannfeldt 1972; Rogers
1981; Rogers and Samuels 1987; Samuels and
Rogers 1987; Del Valle Catania and Romero 2003;
Rogers et al. 2006, 2007) and occasionally on
polypores (Samuels and Rogers 1987, Lodge et al.
2002). A number of European species with conspic-
uous stromata are restricted to old growth and
minimally managed stands, and their rarity has been
attributed to modern silvicultural practices and the
removal of woody debris and fallen, decaying tree
from forests (Nannfeldt 1972, Holec 2005, Johnova´
2009). In Germany, the occurrence of
C. polysperma
in near-natural forests is related to the availability of
large-diameter logs (Ba¨ssler et al. 2010).
Phylogenetic analysis of the LSU sequences of the
taxa examined in this study divides species of
Camarops
between two moderately well supported clades. The
first includes
C. amorpha
,
C. microspora
and species of
Camaropella
. The second includes
C. petersii
,
C.
polysperma
,
C. rogersii
,
C. tubulina
and
C. ustulinoides
.
Within this second group, two isolates of
C. ustulinoides
are not resolved as close relatives. Although
Camar-
opella
could be expanded to include
C. amorpha
and
C.
microspora
, we hesitate to formally transfer these species
pending the analysis of sequences from additional gene
regions of the members of both genera.
Cornipulvina
Huhndorf, A.N. Mill., F.A. Ferna´ndez &
Lodge, Fungal Divers 20:61. 2005.
MycoBank MB501318
Type species: Cornipulvina ellipsoides
Huhndorf, A.N.
Mill., F.A. Ferna´ndez & Lodge
Comments:
This monotypic genus is characterized
by its superficial, soft-textured stromata, monosti-
chous ascomata with long, projecting necks, and
hyaline, unicellular ascospores (Huhndorf et al. 2005,
Huhndorf and Miller 2008).
Cornipulvina ellipsoides
occurs on decorticated wood and has been collected
in Brazil, Puerto Rico and Venezuela (Huhndorf et al.
2005).
Cornipulvina ellipsoides
was resolved as the member
of a weakly supported clade that also encompassed
C.
amorpha
,
C. microspora
and species of
Camaropella
in
a study based on the analysis of LSU sequences
(Huhndorf and Miller 2008). Our LSU phylogeny
positions this species as the member of a clade that
includes
A. curreyi
and
P. ferruginea
(FIG. 1).
Endoxyla
Fuckel, Jb. Nassau. Ver. Naturk. 25–26:321.
1871.
MycoBank MB1813
Type species: Endoxyla macrostoma
Fuckel
Comments: Endoxyla
encompasses species occur-
ring on decayed, decorticated wood of angiosperms
and gymnosperms in Europe and North America
that possess immersed, poorly developed to pulvinate
stromata, solitary to gregarious, flask-shaped asco-
mata, and uniporate, aseptate, or one- or two-septate
ascospores that may or may not possess a hyaline cell
574 MYCOLOGIA
(Untereiner 1993). Members of the genus studied in
pure culture (see below) have not been observed to
produce conidial anamorphs. Species of
Endoxyla
are
ecologically and morphologically similar to
Apior-
hynchostoma
(Dennis 1981, Rogers et al. 1994b) but
differ in possessing ascospores that lack a hyaline cap
and asci with an apical ring that does not stain in
JGB.
Endoxyla
has been treated as the member of a
number of ascomycete families (Barr 1990, 1994:
Untereiner 1993; Rogers et al. 1994b). Our phyloge-
nies (FIGS. 1, 2) support Rappaz (1995) who referred
this genus to the Boliniaceae based on morphology.
KEY TO SPECIES OF
E
NDOXYLA
(ADAPTED
FROM UNTEREINER 1993)
1. Ascospores aseptate, (8–)10–12.5(–14.5) 32–3.7
(–5) mm ......................
E. operculata
1. Ascospores septate, septum delimiting a hyaline
cell or dividing a pigmented portion of the
ascospore, or both . . . .................... 2
2. Ascospores without a hyaline cell, one-septate,
(9.5–)11–14.5(–15.5) 32.3–3.5(–4.5) mm.....
......................
E. parallela
2. Ascospores with a hyaline cell, one- or two-
septate ............................ 3
3. Pigmented portion of the ascospore septate . . . . . 4
3. Pigmented portion of the ascospore aseptate . . . . 5
4. Ascospores (10–)11.3–14.8(–17.8) 32.6–3.6
(–4) mm .....................
E. munkii
4. Ascospores (22–)24–31 34.5–5(–7) . . .
E. occulta
5. Ascospores ellipsoid or ellipsoid-inequilateral to
crescentic, (15–)20–25(–36.5) 37.5–9(–10.5)
mm ...........................
E. mallochii
5. Ascospores ellipsoid-cylindric or suballantoid,
smaller . . .............................. 6
6. Ascospores suballantoid, 9.0–12.3(–13.3) 3
2.2–3.4(–4.0) mm ............
E. macrostoma
6. Ascospores ellipsoid-cylindric, 8.3–11 32.3–
3.5 mm ..................
E. xanthostroma
Endoxyla macrostoma
Fuckel, Jb. Nassau. Ver. Naturk.
25–26:322. 1871. FIGS. 10–13
MycoBank MB165617
;
Valsa macrostoma
(Fuckel) Winter, Rabenh. Krypt.-Fl.
1(2): 689. 1886.
See Untereiner (1993) for a description of the
teleomorph. Additional illustrations of this species
are provided by Berlese (1905) and Untereiner
(1993).
Colonies on CBSOA 5–6 mm in 21 d, flat,
appearing moist and waxy, mycelium immersed
entirely, yellowish white to pale yellow (3A2–3).
Colonies on CMA 7–8 mm in 21 d, flat, appearing
moist and waxy, mycelium immersed entirely, yellow
(3A6–8). Reverse light yellow (3A5). Colonies on OA
6–8 mm in 21 d, aerial mycelium sparse, short,
appearing powdery, yellowish white (3A2), mycelium
at the colony margin yellow (3A6–8). Reverse pale
yellow (3A3). Colonies on MEA 25–27 mm in 21 d,
mycelium immersed entirely, flat, center olive brown
(4F4–5), margin yellowish gray (4B2). Colonies on
MLA 20–25 mm in 21 d, aerial mycelium short,
sparse, restricted to the colony center, yellowish white
to pale yellow (3A2–3), mycelium toward the margin
immersed, slightly furrowed, appearing mealy,
orange-white (5A2) but becoming pale orange to
light orange (5–6A3–4) toward the colony margin.
Margin sharp and regular on all media except MLA.
Conidial anamorph not observed.
Habitat:
On decorticated wood of angiosperms and
gymnosperms.
Distribution:
Canada, Czech Republic, Germany
(type locality), Sweden.
Specimens examined:
CANADA. Prince Edward Island:
Queens County, Brookvale Demonstration Woodlot, on
decorticated wood of
Pinus strobus
, 28 Apr 2009,
A. Carter
(NBM; living culture UAMH 11491 [mass-ascospore iso-
late]); Queens County, Black Creek Road, on decaying
gymnosperm wood (
Abies
sp. or
Picea
sp.), 11 May 2008,
A.
Carter
(NBM). CZECH REPUBLIC. Southern Bohemia:
S
ˇumava Mts., Z
ˇelezna´ Ruda, glacial cirque of the C
ˇerne´
Jezero Lake, 19 Jul 1997, on decaying wood of
Picea abies
,
M. Re´blova´ 1066
. See Untereiner (1993) for additional
collections.
Endoxyla mallochii Unter., A. Carter & Re´blova´, sp.
nov. FIGS. 14–23
MycoBank MB801137
Stromata absent or poorly developed and evident
only as a light brown discoloration of the wood
around the necks of the ascomata. Ascomata im-
mersed, rarely solitary, monostichous in regular or
irregular linear groups, ampulliform, 900–1100 3
600–650 mm, black, with cylindrical, separately erum-
pent necks 350–400 3200–250 mm, apices of necks
pulvinate, projecting slightly above the surface of the
wood. Ascomatal walls 30–60 mm wide, composed of
two layers, the outer layer of brown, thick-walled cells
forming a textura angularis to a textura prismatica,
the inner layer of thin-walled, compressed hyaline
cells forming a textura prismatica. Asci unitunicate,
eight-spored, cylindrical, long-stipitate, total length
245–305(–375) mm, pars sporifera 130–190(–245) 3
9–12.5 mm, with an indistinct, inamyloid apical ring
that is unstained in JGB. Ascospores ellipsoid to
ellipsoid-inequilateral or crescentic, (15–)20–25(–
36.5) 37.5–9(–10.5) mm, uniseriate or occasionally
apically biseriate and becoming uniseriate below,
UNTEREINER ET AL.: MOLECULAR PHYLOGENY OF BOLINIALES 575
FIG. 14.
Endoxyla mallochii
. A. Asci. B. Habit sketch of ascomata. C. Enlarged ascospores from a two-spored ascus. D.
Ascospores from eight-spored asci. From A. Carter 880, NBM (Holotype). Bars: A 520 mm, B 5500 mm, D 510 mm.
576 MYCOLOGIA
FIGS. 15–23.
Endoxyla mallochii
. 15, 16. Groups of ascomata immersed in decorticated wood with only necks emerging. 17.
Apical annulus. 18–20. Ascospores. 21, 22. Long-stipitate asci. 23. Paraphyses. 15, 23 from M. Re´ blova´ 1392; 16, 22 from M.
Re´blova´ 1388; 17–21 from M. Re´blova´ 1466. Bars: 15, 16 5500 mm; 17–20 510 mm; 21–23 525 mm.
UNTEREINER ET AL.: MOLECULAR PHYLOGENY OF BOLINIALES 577
bicellular, composed of a hyaline cell 1.5–2.5 32–
2.5 mm, and a brown cell with an apical germ pore,
porate end acute, without a fixed orientation within
the asci. Paraphyses filiform, septate, 1.5–3 mm diam.
Colonies on CBSOA, MEA, MLA and OA orange-
white (5A2). Colonies on CMA white (A1). Colonies
flat and immersed entirely on all media except MLA.
Colonies on CBSOA and OA 5–6 mm in 21 d,
appearing waxy. Colonies on CMA 5–6 mm in 21 d,
appearing moist. Colonies on MEA 41–45 mm in 21 d.
Colonies on MLA 13–14 mm in 21 d, aerial mycelium
short, restricted to the colony center, appearing felt-
like, mycelium toward the margin immersed, appear-
ing waxy. Margin regular and sharply defined on all
media. Conidial anamorph not observed.
Etymology:
Named in honor of David Malloch, a
distinguished Canadian mycologist and mentor to AC
and WAU.
Habitat:
On decorticated wood of conifers.
Distribution:
Canada (type locality), Czech Repub-
lic, Ukraine.
HOLOTYPE. CANADA. Prince Edward Island: Queens
County, Fort Amherst Park, on decorticated wood (
Abies
sp. or
Picea
sp.), 2 Jun 2008,
A. Carter 880
(NBM; living
culture UAMH 11087 ex-type, isolated from ascomatal
tissue).
Additional specimens examined:
CANADA. Prince Ed-
ward Island: Queens County, Fort Amherst Park, on
rotted fallen log (Pinaceae), 9 Jul 2008,
A. Carter 914
(NBM); ibid., on decorticated wood (
Abies
sp. or
Picea
sp.), 8 Jun 2008,
A. Carter 951
(NBM); ibid., on
decorticated wood (
Abies
sp. or
Picea
sp.), 8 Aug 2008,
A. Carter 955
(NBM); Queens County, woods at Black
Creek Road, on fallen log (
Picea
sp.), 15 Oct 2009,
A.
Carter 1086
(NBM); Queens County, Cornwall, Corwall
Ferry Road, on well rotted, decorticated wood (Pina-
ceae), 23 Apr 2009,
A. Carter 1128
(NBM). CZECH
REPUBLIC. Northeastern Bohemia: Chrˇibsko, Labske´
Pı´skovce Mountains, on decayed wood of
Picea abies
,23
Apr 1998,
M. Re´blova´1207
. Southern Bohemia, S
ˇumava
Mountains, Z
ˇelezna´ Ruda, glacial cirque of the C
ˇerne´
jezero lake, on decaying wood of
Picea abies
, 27 Aug 1998,
M. Re´blova´ 1388
,
1392
; 13 Aug 1999,
M. Re´blova´1466
.
UKRAINE. Carpathian Mountains, Sinevirskaja Poliana
Massif., Sinevir, on decayed wood of
Abies alba
,20Jul
1998,
M. Re´blova´1244
.
Comments: Endoxyla mallochii
resembles
E. macro-
stoma
and
E. xanthostroma
Unter. in possessing
uniseptate ascospores composed of a small hyaline cell
and a larger brown cell with an apical germ pore. This
species can be distinguished from the other members of
the genus by its larger, ellipsoid to crescentic ascospores
and longer, cylindrical asci. The asci in some collections
of
E. mallochii
occasionally contain only two or four
ascospores that are considerably larger than the asco-
spores in eight-spored asci. Abnormal ascospores of
E.
mallochii
may possess or lack a hyaline cell, but we have
never observed the pigmented portion to be septate.
Endoxyla munkii
Unter., Mycologia 85:299. 1993.
MycoBank MB357546
This species is described and illustrated by Unte-
reiner (1993).
Habitat:
On decaying, decorticated wood of species
of
Pinus
.
Distribution:
Finland, Russia (type locality), Swe-
den, USA.
Comments: Endoxyla munkii
resembles
E. parallela
(Fr.: Fr.) Sacc., the only other member of the genus
Endoxyla
associated with
Scotiosphaeria endoxylinae
Sivan. (Sivanesan 1977).
Endoxyla munkii
has been
compared to
Apiorhynchostoma altipetum
(Rappaz
1995), but it can be distinguished from this species
by its smaller and more centrally septate ascospores
that lack a hyaline cap.
Endoxyla occulta (Re´blova´) Unter. & Re´blova´, comb.
nov. FIGS. 24–26
Basionym.
Apiorhynchostoma occultum
Re´blova´, Sydowia
50:230. 1998.
MycoBank MB801134
See Re´blova´ (1998) for a description and additional
illustrations of the teleomorph.
Habitat:
On decorticated, decaying wood of
Picea
abies
(L.) H. Karst.
Distribution:
Czech Republic.
Specimens examined:
CZECH REPUBLIC. Southern Bo-
hemia: S
ˇumava Mountains, glacial cirque of the C
ˇerne´
jezero Lake, on decayed wood of a trunk of
Picea abies
,22
Oct 1996,
M. Re´blova´
(HOLOTYPE, PRM 842971); data as
for holotype, 27 Aug 1998,
M. Re´blova´ 1387
.
Comments: Endoxyla occulta
resembles
E. munkii
but it can be distinguished from this species by its
larger ascospores. Re´blova´ (1998) interpreted the
somewhat more refractive walls at the porate end of
the ascospores of this species as an appendage, but a
hyaline cap equivalent to the structure observed in
species of
Apiorhynchostoma
is not present.
Endoxyla
occulta
is known only from the type locality.
Endoxyla operculata
(Fr.: Fr.) Sacc., Syll. Fung. 1:181.
1882.
MycoBank MB165783
;
Sphaeria operculata
Pers.
dd seriata
Alb. & Schwein.,
Conspect. Fung. Lusat., p. 40. 1805.
;
Sphaeria operculata
Fr.: Fr., Syst. Mycol. 2:479. 1823,
non
Persoon, Syn. Meth. Fung. p. 80. 1801.
;
Valsa operculata
(Fr.: Fr.) Nitschke, Pyrenomyc. Germ.
1:153. 1867.
;
Anthostoma operculatum
(Fr.: Fr.) J. Schro¨t., Krypt.-Fl.
Schlesien 3:432. 1897.
578 MYCOLOGIA
;
Ceratostoma operculatum
(Fr.: Fr.) Petrak, Fl. Boh. et
Mor. Exs. Ser. ii, 1 Abt. Pilze, Lfg. xx, 968. 1914.
5
Rosellinia gomzeensis
Mouton, Bull. Soc. Roy. Bot. Belg.
36:12. 1897 (fide Rappaz 1995).
5
Ceratostoma crassicolle
Kirschst., Verh. Bot. Vereins Prov.
Brandenburg 48:52. 1906.
5
Endoxyla operculata
(Fr.: Fr.) Sacc. var. c
ompressispora
Kauffman, Pap. Michigan Acad. Sci. 11:161. 1929.
5
Phaeognomoniella avocetta
(Cooke & Ellis) Romero, Bol.
Soc. Argent. Bot. 34:76. 1999 (
fide
Re´blova´ 2006).
;
Sphaeria avocetta
Cooke & Ellis, Grevillea 8:15. 1879.
;
Ceratostoma avocetta
(Cooke & Ellis) Sacc., Syll. Fung.
1:216. 1882.
;
Anthostoma avocetta
(Cooke & Ellis) von Arx & E.
Mu¨ller, Beitr. Kryptogamenfl. Schweiz 11:317. 1954 (as
A. avocetta
(M.A. Curtis & Ellis) von Arx & E. Mu¨ller).
;
Endoxyla avocetta
(Cooke & Ellis) Romero & Samuels,
Sydowia 43:231. 1991.
See Untereiner (1993) for a description of this
species. Illustrations of
E. operculata
are provided by
Berlese 1905, Untereiner 1993 and Re´blova´ 2006
(figures labeled as
E. parallela
).
Colonies on CBSOA 7–15 mm in 21 d, flat,
appearing moist, mycelium immersed entirely, white
(A1). Colonies on CMA 45–52 mm in 21 d, flat,
appearing moist, mycelium scant and immersed
entirely, white (A1). Colonies on MEA 68–70 mm in
21 d, flat, mycelium immersed entirely, orange-white
(5A2). Colonies on MLA 33–37 mm in 21 d, aerial
mycelium sparse, short, restricted to the center of the
colony, appearing powdery, yellowish white (4A2),
mycelium toward the margin immersed, orange-white
(5A2). Reverse orange-white (5A2). Colonies on OA
18–24 mm in 21 d, aerial mycelium sparse, short,
cottony, restricted to the center of the colony, white
to orange-white (5A1–2), mycelium toward the
margin immersed, orange-white (5A2). Margin irreg-
ular, sharply defined on CMA and MLA, regular and
sharply defined on all other media. Conidial ana-
morph not observed.
Habitat:
On rotting decorticated wood of angio-
sperms and gymnosperms.
Distribution:
Canada, Czech Republic, Finland,
France, Germany, Sweden (type locality), USA.
Specimens examined:
CANADA. New Brunswick: Resti-
gouche County, Jacquet River Gorge Protected Area, 9.5 km
SW of Highway 11 on Archibald Road, on decorticated
wood of
Populus
sp., 21 Jun 2009,
A. Carter JRAC 14
(NBM);
Prince Edward Island: Queens County, Cumberland
514711, on rotten decorticated wood of
Populus
cf.
balsamifera
, 1 Jun 2008,
A. Carter
(NBM; living cultures
FIGS. 24–26.
Endoxyla occulta
. 24, 25. Tips of ascomtal necks emerging from the decorticated wood. 26. Ascospores. From
M. Re´blova´ 1387. Bars: 24 5500 mm, 25 5200 mm, 26 510 mm.
UNTEREINER ET AL.: MOLECULAR PHYLOGENY OF BOLINIALES 579
UAMH 11085 [mass-ascospore isolate], UAMH 11086
[single-ascospore isolate]); ibid., on rotted log (Salicaceae),
20 Jul 2008,
A. Carter 942
(NBM); ibid., Cumberland 51471,
on rotted cut logs (Salicaceae), 23 Jun 2008,
A. Carter 903
(NBM), See Untereiner (1993) for additional specimens.
Comments
. As discussed by Re´blova´ (2006), type
material of
Sphaeria avocetta
at BPI and K represents
Endoxyla operculata
. The genus
Phaeognomoniella
Romero, introduced for
S. avocetta
, was based on
misidentified type material (Romero 1999). The
fungus formerly classified as
Endoxyla avocetta
sensu
Romero and Samuels (1991) is unrelated to
Endoxyla
(Untereiner 1993) and is conspecific with
Xylome-
lasma sordida
Re´blova´(Re´blova´ 2006).
Endoxyla
operculata
is the most frequently collected species of
Endoxyla
and, with the exception of
E. macrostoma
,it
is the only member of the genus recorded from the
wood of both angiosperms and gymnosperms.
Endoxyla parallela
(Fr.: Fr.) Sacc., Syll. Fung. 1:181.
1882.
MycoBank MB140870
;
Sphaeria parallela
Fr., Kongl. Veten-skapsakad. Handl.,
ser. 3, vol. 4:155. 1816.
;
Sphaeria parallela
Fr.: Fr., Syst. Mycol. 2:373. 1823.
;
Valsa parallela
(Fr.: Fr.) Nitschke, Pyrenomyc. Germ.
1:154. 1867.
;
Eutypa parallela
(Fr.: Fr.) P. Karst., Bd. Ka¨nn. Finl. Nat.
Folk 26:130. 1873.
;
Eutypopsis parallela
(Fr.: Fr.) P. Karst., Meddeland. Soc.
Fauna Fl. Fenn. 2:182. 1878.
;
Xylosphaeria parallela
(Fr.: Fr.) Cooke, Grevillea 7:86.
1879.
;
Endoxylina parallela
(Fr.: Fr.) Berlese, Icon. Fung.
3:105. 1905.
5
Endoxylina crocea
Kirschst., Ann. Mycol. 33:214. 1935.
5
Endoxylina pini
Sivan., Trans. Brit. Mycol. Soc. 69:117.
1977.
See Untereiner (1993) for a description of the
teleomorph. Sivanesan (1977) and Untereiner
(1993) have illustrated this species.
Habitat:
On rotting, decorticated wood of conifers.
Distribution:
Canada, Czech Republic, Finland,
Germany, Scotland, Sweden (type locality), USA.
Specimens examined:
CANADA. Prince Edward Island:
Queens County, Green Road Creek, on fallen log (
Abies
sp.
or
Picea
sp.), 15 Aug 2008,
A. Carter 981
(NBM); ibid., Queens
County, McPhail Woods, Orwell, on fallen log of
Pinus
sp., 24
Jul 2009,
A. Carter 1022
(NBM); ibid., on fallen log of
Pinus
strobus
, 24 Jul 2009,
A. Carter 1023
(NBM); ibid., Queens
County, Route 244 (Peter’s Road) near Emyvale, on well
rotted log (
Abies
sp. or
Picea
sp.), 11 Sep 2009,
A. Carter 1062
(NBM). See Untereiner (1993) for additional specimens.
Comments: Endoxyla parallela
may be confused with
E. munkii
in that
Scotiosphaeria endoxylinae
occasion-
ally is found on the exposed necks of these taxa and
because of the occurrence of mixed collections that
include both species.
Endoxyla parallela
also has been
confused with
Sphaeria luteobasis
, a species with
brown, uniseptate and nonporate ascospores (see
DOUBTFUL AND EXCLUDED SPECIES).
Endoxyla xanthostroma
Unter., Mycologia 85:305.
1993.
MycoBank MB359760
See Untereiner (1993) for the description and
illustrations of this species.
Habitat:
On rotting, decorticated wood of
Pinus
sp.
Distribution:
USA.
Comments: Endoxyla xanthostroma
is known only
from the type collection. It is the only member of the
genus
Endoxyla
with a yellowish stroma.
Mollicamarops
Lar.N. Vassiljeva, Mycotaxon 99:160.
2007.
MycoBank MB510602
Type species: Mollicamarops stellata
Lar.N. Vassilyeva
Comments: Molliocamarops
includes a single species
characterized by its superficial, soft, brightly colored
stromata and ascomata with stellate ostioles that is
known from one collection on the decaying wood of a
deciduous tree in eastern Russia (Vasilyeva 2007).
The ascospores of
M. stellata
are unicellular, ellipsoid
and brown, but the description of this species does
not mention the presence of a germ pore.
Mollica-
marops
has been compared to
Camarops flava
(Vasilyeva 2007, Huhndorf and Miller 2008), but the
phylogenetic position of the genus has not yet been
examined with molecular data.
Neohypodiscus
J.D. Rogers, Y.M. Ju & Læssøe, Mycolo-
gia 86:684. 1994.
MycoBank MB27387
Type species: Neohypodiscus rickii
(Lloyd) J.D. Rogers,
Y.M. Ju & Læssøe
Comments: Neohypodiscus
encompasses species with
large subglobose to pulvinate to irregular stromata
with a hard exterior, asci with an inamyloid apical
ring, and large, brown, aseptate or one- or two-
septate, uniporate ascospores that possess a hyaline
cap at each pole; anamorphs are not known for the
genus, and cultures obtained from the stromata of the
type species were sterile (Rogers et al. 1994a). The
genus includes three species that occur on wood in
the Caribbean, North America and South America
(Rogers et al. 1994a). Rogers et al. (1994a) provided a
key to the members of the genus.
Rogers et al. (1994a) placed
Neohypodiscus
in
Amphisphaeriaceae and compared the asci and
ascospores of the members of the genus to
Apiorhynch-
580 MYCOLOGIA
ostoma
. Andersson et al. (1995) included
Neohypodiscus
in Boliniaceae, but its relationship to the other
members of this family has not yet been assessed based
on the comparison of DNA sequence data.
Pseudovalsaria
Spooner, Trans. Brit. Mycol. Soc.
86:405. 1986.
MycoBank MB25775
Type species: Pseudovalsaria foedans
(P. Karst.) Spoo-
ner (5
Pseudovalsaria ferruginea
[Nitschke] Rappaz).
Comments: Pseudovalsaria
was established for
Phaeosperma foedans
P. Karst. (Spooner 1986), a
species found on the corticated or decorticated wood
of angiosperms that possesses immersed, erumpent
stromata, perithecial ascomata with long necks that
emerge in a common stromatic disk, cylindrical asci
with an indistinct, inamyloid apical ring, and brown,
uniseptate ascospores with a single terminal germ pore.
Untereiner (1993) examined the type of
Anthos-
toma ferrugineum
Nitschke and noted the similarity of
this species to
Pseudovalsaria foedans
. Rappaz (1995)
subsequently transferred
A. ferrugineum
to
Pseudoval-
saria
and distinguished it from the type species of the
genus based on ascospore shape. This distinction was
not accepted by Ju et al. (1996), who treated
P.
foedans
as a synonym of
P. ferruginea
. We agree that
the ascospores of this species range from straight to
slightly curved and concur that
P. ferruginea
is the
earliest available name for this species.
Two other species assigned to the genus include
P.
allantospora
(Ellis & Everh.) M.E. Barr and
P. peckii
(Howe) M.E. Barr. According to Ju et al. (1996), the
former belongs to
Endoxylina
; our examination of
collections of this species supports their observation
that this taxon is diatrypaceous. The latter species,
which possesses cylindrical, unitunicate asci and
brown, uniseptate ascospores with a germ pore at
each end (Barr 1994), is also not a species of
Pseudovalsaria
(see DOUBTFUL AND EXCLUDED SPE-
CIES).
Pseudovalsaria ferruginea
(Nitschke) Rappaz, Mycol.
Helvetica 7:159. 1995.
MycoBank MB363314
;
Anthostoma ferrugineum
Nitschke, Pyrenomyc. Germ.
1:118. 1867.
;
Camarops ferruginea
(Nitschke) Shear, Mycologia
30:588. 1938.
5
Anthostoma fennicum
P. Karst., Fung. Fenn. Exs. 774.
1868 (fide Ju et al. 1996).
;
Phaeosperma fennicum
(P. Karst.) P. Karst., Bd. Ka¨nn.
Finl. Nat. Folk 23:54. 1873.
;
Valsaria fennica
(P. Karst.) Sacc., Syll. Fung. 1:752.
1882.
5
Phaeosperma foedans
P. Karst., Bd. Ka¨nn. Finl. Nat. Folk
23:54. 1873.
;
Valsaria foedans
(P. Karst.) Sacc., Syll. Fung. 1:748.
1882.
;
Pseudovalsa foedans
(P. Karst.) Cooke, Grevillea 14:55.
1885.
;
Pseudovalsaria foedans
(P. Karst.) Spooner, Trans. Brit.
Mycol. Soc. 86:405. 1986.
5
Phaeosphaeria niesslii
Winter, Hedwigia 13:131. 1874
(fide Spooner 1986).
;
Valsaria niesslii
(Winter) Sacc., Syll. Fung. 1:749. 1882.
;
Pseudovalsaria niesslii
(Winter) Cooke, Grevillea 14:55.
1885.
?5
Valsaria anthostomoides
Sacc., Atti Soc. Venet. Trent.
Sci. Nat. Padova 4:18. 1875 (fide Ju et al. 1996).
5
Diatrype moroides
Cooke & Peck, Ann. Rep. New York
State Mus. 29:63. 1878.
;
Valsaria moroides
(Cooke & Peck) Sacc., Syll. Fung.
1:750. 1882.
5
Valsaria salicina
Ellis & Everh., Proc. Acad. Nat. Sci. Phil.
42:236. 1890 (fide Ju et al. 1996).
5
Valsaria lignicola
S. Teng & Ou, Sinensia 7:515. 1936
(fide Spooner 1986).
This species is illustrated by Spooner (1986) and
Rappaz (1995).
Colonies on CBSOA 22–24 mm in 21 d, flat,
appearing waxy, mycelium immersed entirely, white
(A1). Medium faintly cleared to 5 mm from the point
of inoculation. Margin irregular, not sharply defined.
Colonies on CMA 28–30 mm in 21 d, flat, appearing
waxy, yellowish white (3A2), aerial short mycelium
short, sparse, and restricted to the colony center.
Margin sharply defined, irregular. Colonies on MEA
47–52 mm in 21 d, as for CMA except yellowish white
(4A2). Colonies on MLA 49–53 mm in 21 d, aerial
mycelium short, cottony, felt-like, covering nearly the
entire surface of the colony, appearing powdery,
yellowish white (3–4A2), mycelium at the margin
immersed, white (A1). Margin regular, sharply
defined. Colonies on OA 50–54 mm, aerial mycelium
short, cottony, appearing powdery, restricted to the
colony center, white to yellowish white (4A1-2),
mycelium toward the margin immersed, light yellow
to reddish yellow (4A4–6), becoming white (A1) at
margin. Margin sharp, regular. Conidial anamorph
not observed.
Habitat:
On bark and decaying wood of angio-
sperms.
Distribution:
Canada, China, Finland (type locality),
Germany, Sweden, Taiwan, UK, USA.
UNTEREINER ET AL.: MOLECULAR PHYLOGENY OF BOLINIALES 581
Specimens examined:
CANADA. British Columbia: Prince
George, on
Alnus
sp., 18 Sep 1955,
W.G. Ziller
(DAOM
170603); Ontario: Carleton County, Merivale, on
Alnus
rugosa
, 1 Oct 1953,
S.J. Hughes
(DAOM 141814, as
Valsaria
moroides
); Dorset, Forest Ranger School, on
Betula allegha-
niensis
, 19 Sep 1953,
R. Horner YB 134
,
J. Newman and
A.W. Hill
(DAOM 139655, as
Valsaria moroides
); Prince
Edward Island: Queens County, Black Creek Road, on
rotting, decorticated branch of
Populus
sp., 9 May 2009,
A.
Carter
(NBM; living culture UAMH 11490 [mass-ascospore
isolate]). GERMANY. Aepfelbach, forest near Oestrich, on
prostrate, rotting branches of
Carpinus betulus
,
L. Fuckel
,
Fungi rhenani 2451 (FH); Westphalia: Nienberge near
Mu¨nster, Apr 1865,
T. Nitschke
(B, HOLOTYPE of
Anthostoma ferrugineum
). USA. Maine: Paynes Swamp, on
Alnus
sp., 7 Sep 1923,
R. Thaxter
(DAOM 195736 dupl. ex
FH, as
Valsaria moroides
); Massachusetts: Cambridge,
Charles River, on
Betula alba
, 19 Sep 1925,
L.E. Wehmeyer
P172b
(DAOM 120806 ex herb. L.E. Wehmeyer 3598, as
Valsaria moroides
); New Hampshire: Chocorua, on bark of
Alnus
sp., 23 Jul 1910,
W.G. Farlow
(DAOM 170079 dupl. ex
FH, as
Valsaria moroides
). Additional records are provided
by Spooner (1986), Rappaz (1995) and Ju et al. (1996).
Comments: Pseudovalsaria ferruginea
also was cul-
tured by Ju et al. (1996) who reported the production
of ascomata in vitro after 6 mo incubation; an
anamorph was not observed. These authors listed
‘‘
Endoxylina moroides
(Cooke & Peck) Shoemaker &
Egger’’ (;
Diatrype moroides
Cooke & Peck) as a
synonym of
P. ferruginea
, but this species has never
been combined in
Endoxylina
; the taxon considered
by Shoemaker and Egger (1982) in the reference
noted by Ju et al. (1996) (Fungi Canadensis 227,
1982) is
Endoxylina allantospora
(Ellis & Everh.)
Shoemaker & Egger.
Stromata development varies among collections of
P. ferruginea
and may reflect differences between
corticated and noncorticated substrates. For example,
the stromata of collections on corticated wood are
often well developed and strongly valsoid (e.g. DAOM
141814, DAOM 170603, DAOM 195736) while those
formed in decorticated wood typically hardly raise the
surface of the substrate. The collection of
P.
ferruginea
we cultured (UAMH 11490) corresponds
closely to the material described by Rappaz (1995)
with respect to this characteristic. We have adopted
the broad circumscription of this taxon provided by
Ju et al. (1996) pending the study and molecular
characterization of collections of
P. ferruginea
from a
wider geographic area and a greater number of hosts.
The resemblance of
P. ferruginea
to species of
Endoxyla
was noted by Nitschke (1867) and Nannfeldt
(1972). Barr (1994) placed
Endoxyla
and
Pseudoval-
saria
in the Clypeosphaeriaceae, but Rappaz (1995)
recognized these genera as members of the Bolinia-
ceae. In our phylogenies (FIGS.1,2)
P. ferruginea
is
inferred as the member of a clade that includes
Apiorhynchostoma curreyi
.
DOUBTFUL AND EXCLUDED SPECIES
Endoxylina allantospora
(Ellis & Everh.) Shoemaker &
Egger, Fungi Canad. No. 227. 1982.
MycoBank MB124750
;
Valsaria allantospora
Ellis & Everh., Proc. Acad. Nat.
Sci. Phil., p 343. 1894.
;
Valsaria coloradensis
Ellis & Everh., Amer. Nat. 32:342.
1897.
;
Pseudovalsaria allantospora
(Ellis & Everh.) M.E. Barr,
Mycotaxon 46:53. 1993.
This species is illustrated by Shoemaker and Egger
(1982).
Habitat:
On branches and bark of
Acer negundo
L.
Distribution:
Canada, USA.
Specimens examined:
CANADA. Saskatchewan: Dundurn,
on twigs of
Acer negundo
, 22 Jun 1967,
A Simpson 892
(DAOM 177173
ex
WINF). USA. Colorado: On
Acer
sp. (as
Negundo
sp.), Jan 1897, E. Bethel (NY, as
Valsaria
coloradensis
); Colorado: Overland, on bark of dead
Acer
negundo
(as
Negundo aceroides
), 16 Nov 1896 (NY, as
Valsaria coloradensis
).
Comments:
Shoemaker and Egger (1982) trans-
ferred
Valsaria allantospora
to
Endoxylina
and noted
the similarity of this species to
E. astroidea
(Fr.)
Romell, the type of the genus. Barr (1993) later
compared
E. allantospora
to
Pseudovalsaria foedans
(5
P. ferruginea
) and treated it as a member of the
genus
Pseudovalsaria
. The ascospores of
E. allantos-
pora
are thick-walled in the middle and become
noticeably thinner at each end, but they lack a germ
pore. As noted by Ju et al. (1996), this species is a
member of the Diatrypaceae.
Endoxylina luteobasis (Ellis) Unter. & Re´blova´, comb.
nov. FIGS. 27–34
Basionym: Sphaeria
(
Byssisedae
)
luteobasis
Ellis, Bull.
Torrey Bot. Club. 6:134. 1877.
MycoBank MB801135
;
Eutypa luteobasis
(Ellis) Sacc., Syll. Fung. 1:171. 1882.
;
Byssosphaeria luteobasis
(Ellis) Cooke, Grevillea 15:122.
1887.
;
Lasiosphaeria luteobasis
(Ellis) Ellis & Everh., N. Am.
Pyrenomy. p 147. 1892.
;
Endoxyla luteobasis
(Ellis) M.E. Barr, Mycotaxon 46:53.
1993.
This species is also illustrated by Barr (1993).
Habitat:
Decorticated wood of species of
Pinus
sp.
and
Quercus
sp.
Distribution:
Czech Republic, Finland, USA.
Specimens examined:
CZECH REPUBLIC. Southern Bo-
hemia: S
ˇumava Mountains, Z
ˇelezna´ Ruda, glacial cirque of
the C
ˇerne´ Jezero Lake, on decaying wood of
Picea abies
,12
Aug 1999,
M. Re´blova´ 1595
;S
ˇumava Mountains, glacial
582 MYCOLOGIA
FIGS. 27–34.
Endoxylina luteobasis
. 27–29. Ascomata immersed in stromata, with only tips of the necks emerging. 30.
Longitudinal section of ascomata. 31. Paraphyses. 32. Ascospores. 33, 34. Long-stipitate asci with a spore-bearing part filled
with eight ascospores. 27, 31–34 from M. Re´blova´ 1572; 29 from M. Re´blova´ 1165; 28, 30 from M. Re´blova´ 1654. Bars: 27–30 5
500 mm; 31, 33, 34 550 mm; 32 510 mm.
UNTEREINER ET AL.: MOLECULAR PHYLOGENY OF BOLINIALES 583
cirque of the C
ˇertovo Jezero Lake, on decaying wood of
Picea abies
, 17 Jun 1997,
M. Re´blova´ 1165
, 12 Aug 1999,
M.
Re´blova´ 1572
. Modrava. Ptacˇı´na´ drzˇ, on decaying wood of
Picea abies
, 14 Aug 1999,
M. Re´blova´ 1654
.Finland.
FINLAND. On
Pinus
sp., 31 Oct 1868,
P. Karsten
, Fungi
Fenniae 777 (NY, ex herb. J.B. Ellis, as
Valsa parallela
).
USA. New Jersey: Near Willow Grove, on an old pine limb,
20 Apr 1879,
J.B. Ellis
(FH, ex herb. J.B. Ellis,
ex
herb. W.G.
Farlow, as
Endoxyla
(
Kalmusia
)
parallela
) and identified as
S. luteobasis
by J.B. Ellis); on decaying pine wood,
J.B. Ellis
,
North American Fungi 99
Sphaeria luteobasis
(TRTC); on
decaying limbs of
Quercus
(
coccinea
)? on the ground, Nov
1887,
J.B. Ellis
, North American Fungi Second Series 1959
Byssosphaeria luteobasis
(TRTC).
Comments: Sphaeria luteobasis
was described as
possessing dark, ostiolate ascomata scattered over or
enveloped within a yellow, hyphal stroma, clavate asci,
and curved, hyaline ascospores (Ellis 1887). Cooke
(1887) also described the ascospores of
S. luteobasis
as
hyaline, whereas later studies (Saccardo 1882, Ellis
and Everhart 1892) characterized them as olivaceous
and olive brown.
Rappaz (1987) suggested that
S. luteobasis
be-
longed to
Endoxyla
, but he did not formally propose
this combination. Untereiner (1993) commented on
the similarity of this species and
E. parallela
based on
the examination of material annotated
S. luteobasis
in
Ellis’ hand at FH (sub nom.
Endoxyla
[
Kalmusia
]
parallela
ex herb. W.G. Farlow) but hesitated to
transfer this species to
Endoxyla
because she had not
studied Ellis’ exsiccata.
Sphaeria luteobasis
subse-
quently was treated as
Endoxyla luteobasis
by Barr
(1993) based on her examination of the type
specimen of this species on
Quercus
(NY), NAF 99
S. luteobasis
and NAF 1959
Byssosphaeria luteobasis
.
Study of collections annotated by Ellis indicates
that he considered
S. luteobasis
and
S. parallela
to be
similar. For example, he noted that
S. luteobasis
and
S. parallela
were ‘‘hardly distinguishable’’ on the
packet of a specimen of the latter species collected on
pine in 1884 (FH, sub nom.
S. parallela
) and observed
that a collection of
S. parallela
from Fries (NY, ex
herb. M.C. Cooke) contained material that ‘‘appears
to be
S. luteobasis
Ell.’’. When
S. luteobasis
was treated
in
Lasiosphaeria
Ces. & de Not., Ellis and Everhart
(1892) described it as occurring on decorticated
limbs of
Quercus
on the ground but added that
specimens on pinewood in NAF 90 were equivalent to
Kalmusia parallela
(;
E. parallela
), a species cited in
the same study as represented by NAF 99.
Our examination of NAF 99 (on pine) and NAF
1959 (on
Quercus
) (both in TRTC) revealed that the
ascospores of
S. luteobasis
are smaller (8.8–12 32–
3mm) than those of
E. parallela
and lack a germ pore.
The ascospores of the specimen annotated
S.
luteobasis
in Ellis’ hand at FH (sub nom.
Endoxyla
[
Kalmusia
]
parallela
ex herb. W.G. Farlow) and of a
collection from NY (P.A. Karsten, Finland Fungi 777),
which Untereiner (1993) misidentified as
E. parallela
,
also proved to be nonporate upon re-examination.
Ascomata configuration and stromata development
vary among collections of
E. luteobasis
. The ascomata
in NAF 99 and NAF 1959 are immersed to erumpent
and superficial, and the distinctive yellow stroma
described for this species is best developed where the
ascomata are superficial. The wood between and
beneath the ascomata in these collections is also
bright yellow. In other collections the stroma is
rudimentary and evident only as a darkening of the
wood around the necks of the ascomata (FH, NY,
PRM). In one collection on
Picea abies
from the
Czech Republic (M. Re´blova´ 1654) a compact
entostroma encloses small groups of immersed to
erumpent ascomata. The stroma surrounding the
ascomata in this material is lighter than the surround-
ing wood and the stromata surface is brownish yellow
or greenish brown. Collections with poorly developed
stromata otherwise conform to the description of this
species provided by Ellis (1887) and Ellis and Ever-
hart (1892).
Jobellisia peckii (Howe) Unter. & Re´blova´, comb.
nov.
Basionym: Valsa peckii
Howe, in C.H. Peck, Ann. Rep. New
York State Mus. Nat. History 27:109. 1875.
MycoBank MB801136
;
Pseudovalsa peckii
(Howe) Sacc., Syll. Fung. 1:746.
1882.
;
Pseudovalsaria peckii
(Howe) M.E. Barr, Mycotaxon
51:210. 1994.
This species is illustrated by Barr (1994).
Habitat:
On dead branches of Ericaceae.
Distribution:
USA.
Comments: Valsa peckii
was described for a species
on
Kalmia latifolia
L. that forms gregarious, im-
mersed, long-necked ascomata with erumpent osti-
oles surrounded by a gray tomentum, and ellipsoid,
brown, uniseptate ascospores (Peck 1875). Barr
(1994) expanded the concept of
Pseudovalsaria
to
accommodate
V. peckii
and described the ascospores
of this species as biporate and heavily pigmented on
each side of the septum. Although we have not
studied material of
V. peckii
, it is strongly reminiscent
of
Jobellisia
M.E. Barr (Jobellisiaceae, Sordariomyceti-
dae incertae sedis), a genus of perithecial ascomycetes
encompassing species with large, papillate or long-
necked ascomata, cylindrical asci with an inamyloid
apical ring, and ellipsoid, brown, porate ascospores
that are darker at the septum (Re´blova´ 2008). Within
this genus,
V. peckii
most closely resembles
J. fraterna
Huhndorf, Lodge & F.A. Ferna´ndez, a Neotropical
584 MYCOLOGIA
species that occurs on decaying wood (Huhndorf et
al. 1999).
Valsaria nudicollis
(Berk. & M.A. Curtis) Sacc., Syll.
Fung. 1:753. 1882.
MycoBank MB175115
;
Hypoxylon nudicolle
Berk. & M.A. Curtis, Grevillea 4:93.
1876.
Specimen examined:
USA. Carolina: on wood of
Pinus
sp.,
M.J. Berkeley
, Car. Inf. 3275 (HOLOTYPE, K).
Comments: Valsaria nudicollis
forms small (200–
360 mm diam), black, perithecial ascomata with short,
indistinctly porate, papiliform necks (50–70 wide, 80–
100 mm long), abundant, filiform paraphyses, cylin-
drical, long-stipitate asci (100–110 mm long, pars
sporifera 60–70 37.7–9.0 mm) with an indistinct
inamyloid ring that does not stain in JGB, and brown,
ellipsoid-oblong, uniseptate, inequilateral ascospores
(10–13.5 33.3–4.8 mm) that possess a single apical
germ pore. The ascomata are typically superficial,
gregarious, monostichous, highly compressed, sur-
rounded by a brownish tomentum, and form a thin
crust over the wood surface. The ascomata are also
occasionally immersed in the substrate where they
occur singly or in short rows.
This species was excluded from
Hypoxylon
Bull. by
Miller (1961) and treated as a synonym of
Endoxyla
parallela
by Ju et al. (1996). Despite its resemblance to
species of
Endoxyla
,
V. nudicollis
differs from the
members of this genus in possessing superficial
ascomata embedded in a brownish stroma and
ascospores that are constricted at the septum. This
species is distinguished from
Pseudovalsaria ferrugi-
nea
in lacking a well developed, immersed stroma and
in possessing less intensely pigmented ascospores.
Valsaria nudicollis
may represent a new genus within
the Boliniales, but we hesitate to treat it as such
pending the study of additional collections.
ACKNOWLEDGMENTS
We are grateful for the help of Gary McNeely, Walter Gams
and two anonymous reviewers for their useful suggestions
and critical comments that improved this paper. We also
thank the curators of DAOM, FH, K, NBM, NY, PRM and Z
for the loan of specimens in their care. Special thanks are
extended to Jennifer Wilkinson (DAOM) for providing
information regarding a number of critical herbarium
labels. David Malloch is acknowledged for encouraging
one of us (WAU) to study
Endoxyla
for her MSc thesis and
to continue working on these and other infrequently
collected Boliniales. Our work was financially supported
by a discovery grant from the Natural Science and
Engineering Research Council (NSERC) of Canada to
WAU, by National Foundation of the Czech Republic
(GAP 506/12/0038) to MR, and as a long-term research
development project of the Institute of Botany, Academy of
Sciences (No. RVO 67985939) and of the Institute of
Microbiology, Academy of Sciences (No. RVO 61388971).
The Canada Foundation for Innovation is also gratefully
acknowledged for infrastructure awards to WAU.
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