Mycologia, 104(5), 2012, pp. 10461055. DOI: 10.

3852/11-174
# 2012 by The Mycological Society of America, Lawrence, KS 66044-8897

Stipitate stereoid basidiocarps have evolved multiple times

Elisabet Sjokvist1
Ellen Larsson

hyaline spores, whereas the hyphal system, septation,

presence of sterile organs and number of sterigmata
are variable characters. When fresh, basidiocarps
range from white to shades of brown or red and
from a few millimeters up to 2 dm. The name stipitate
stereoid refers to these fungis resemblance to species
of the genus Stereum Pers., which have a similar tough
consistency and a smooth hymenophore but effusedreflexed instead of stipitate basidiocarps.
Reid (1965) compiled a monograph of the stipitate
stereoid fungi, covering 60 species that he assigned to
the genera Aquascypha D.A. Reid, Cotylidia P. Karst.,
Cymatoderma Jungh., Inflatostereum D.A. Reid, Podoscypha Pat., Stereopsis D.A. Reid, Coralloderma D.A.
Reid, Cyphellostereum D.A. Reid and Dichopleuropus
D.A. Reid. He further classified the genera into two
families, placing the first six in Podoscyphaceae D.A.
Reid and Dichopleuropus in Lachnocladiaceae D.A.
Reid, while leaving Cyphellostereum and Coralloderma
as insertae sedis. This classification was based on
morphological characters and chemical reactivity.
There are presently ca. 70 species described within
Podoscyphaceae sensu Reid (Kirk et al. 2008), the
majority of which can be found in the tropics. Many of
the species appear to be endemic to Africa, eastern
Asia or South America. The life strategies of the
stipitate stereoid fungi are poorly known. Reid (1965)
assumed all were saprotrophic because many of them
were found on deadwood. However, some species are
found on the roots or stems of living trees, on bare
ground or among mosses, which could indicate some
kind of mycorrhizal or parasitic association with green
plants.
Only a few stipitate stereoid fungi have been
sequenced and included in molecular phylogenetic
analyses. The Podoscyphales was introduced after a
molecular phylogenetic analysis based on the nuclear
ribosomal internal transcribed spacer (ITS) in which
Podoscypha multizonata (Berk. & Broome) Pat., P.
venustula (Speg.) D.A. Reid, P. petalodes subsp.
rosulata D.A. Reid, Cymatoderma elegans Jungh., and
C. dendriticum (Pers.) D.A. Reid clustered together
(Boidin et al. 1998). However, the molecular support
for this classification is not clearly stated in the paper
and the sequences have never been made public.
Other molecular studies later recovered Podoscypha
multizonata and P. parvula (Lloyd) D.A. Reid in the
Polyporales (Moncalvo et al. 2002, Redhead et al.
2002, Larsson 2007). Yoon et al. (2003) treated Cymatoderma caperatum (Berk. & Mont) D.A. Reid and Podoscypha elegans (G. Mey.) Pat. under Podoscyphaceae.

University of Gothenburg, Department of Plant and

Environmental Sciences, P.O. Box 461, 405 30
Goteborg, Sweden

Ursula Eberhardt
CBS-KNAW Fungal Biodiversity Centre, P.O. Box
85167, 3508 AD Utrecht, the Netherlands

Leif Ryvarden
University of Oslo, Department of Biology, P.O. Box
1066 Blindern, 0316 Oslo, Norway

Karl-Henrik Larsson
Natural History Museum, University of Oslo, P.O. Box
1172 Blindern, 0318 Oslo, Norway

Abstract: Stipitate stereoid fungi are Basidiomycetes

with a stipe, a spathulate- to funnel-shaped pileus, a
smooth hymenophore, and hyaline, smooth spores.
Representatives of the genera Cotylidia, Cymatoderma,
Muscinupta, Podoscypha and Stereopsis were subjected
to molecular phylogenetic analyses based on nuclear
ribosomal large subunit, 5.8S and ITS sequences. For
four of the genera the type species was included in
analyses. Stereopsis radicans, the type species of
Stereopsis, forms a lineage with the corticioid species
Clavulicium globosum but could not be placed in any
of the presently accepted orders within Agaricomycotina. Stereopsis vitellina falls within the Atheliales,
making it the first pileus- and stipe-forming fungus
recovered in this order. Cotylidia and Muscinupta
again are shown to be members of the Hymenochaetales, whereas Cymatoderma and Podoscypha belong in
the Polyporales. Cymatoderma is polyphyletic and
Cymatoderma sensu stricto is separated from other
stipitate stereoid fungi in the Polyporales, whereas the
remaining Cymatoderma species are nested within a
well supported clade holding all Podoscypha species
but also Abortiporus biennis.
Key words: evolution, fruiting body, Fungi, morphology, Podoscyphaceae
INTRODUCTION
Stipitate stereoid fungi have spathulate- to funnelshaped basidiocarps with a stipe, a more or less tough
consistency, a smooth hymenophore and smooth
Submitted 20 May 2011; accepted for publication 7 Feb 2012.
1
Corresponding author. E-mail: elisabet.sjokvist@bioenv.gu.se

1046

SJOKVIST ET AL.: STIPITATE STEREOID FUNGI PHYLOGENY

Cymatoderma caperatum also surprisingly has been
recovered in the russuloid clade (Hibbett and Binder
2002). Cotylidia diaphana (Schwein.) Lentz was considered a member of the Phanerochaetales by Boidin et al.
(1998), whereas in other studies it was placed along
with Cotylidia aurantiaca (Pers.) A.L. Welden, Cotylidia
aurantiaca var. alba D.A. Reid, and Cyphellostereum leave
(Fr.) D.A. Reid in the hymenochaetoid clade (Moncalvo
et al. 2002, Redhead et al. 2002). The latter arrangement
was confirmed by Larsson et al. (2006) who suggested
that Cotylidia and Cyphellostereum belong to the
Rickenella clade within the Hymenochaetales. Lawrey
et al. (2009) found that the type of Cyphellostereum, C.
pusiolum (Berk. & M.A. Curtis) D.A. Reid, has its closest
relatives among basidiolichens in the Hygrophoraceae (Agaricales). This discovery prompted a transfer
of Cyphellostereum laeve to a new genus Muscinupta
Redhead, Lu
cking & Lawrey. Stereopsis humphreyi (Burt)
Redhead & D.A. Reid, the only Stereopsis species so far
included in molecular phylogenetic analysis, was placed
in the Agaricales but showed no clear connection to any
distinct group (Moncalvo et al. 2002).
Two studies monographed the Stereum-like fungi
from tropical America (Ryvarden 2010, Welden
2010). Ryvarden (2010) described 43 stipitate stereoid
fungi but did not present a classification above genus
rank. Welden (2010) treated 37 stipitate stereoid
fungi in Aquascypha, Coralloderma, Cotylidia, Cymatoderma and Podoscypha. Welden (2010) introduced a
restricted Podoscyphaceae that includes only Cymatoderma and Podoscypha. Cotylidia, together with
Hydnopolyporus, is referred to emended Aphelariaceae Corner. Aquascypha is compared to Veluticeps,
now considered a member of the Gloeophyllales
(Garcia-Sandoval et al. 2011), and Coralloderma and
Stereopsis are regarded as morphologically related and
discussed in relation to Gomphaceae.
The aim of this study was to clarify the phylogenetic
relationships within Podoscyphaceae sensu Reid
(1965) and to test the monophyly of the main genera
referred to the family. Aquascypha and Inflatostereum
could not be included in our analyses because we
were unable to find material suitable for sequencing.
For the phylogenetic analyses we used sequences from
the nuclear ribosomal ITS, 5.8S and LSU regions.
MATERIALS AND METHODS
All specimens used to generate new sequences for this study
are deposited in the herbaria in Oslo (O), Gothenburg
(GB) and New York Botanical Garden (NY). Some
sequences were generated from cultures deposited at the
CBS culture collection and from fungal culture collections
at University of Helsinki and University of Gothenburg
(FCUG). The FCUG collection is no longer maintained,
and its cultures have been transferred to CBS. Data on all

1047

sequences used in the phylogenetic analyses are included

herein (TABLE I). We did not intend to make a taxonomic
revision at species level and thus have accepted the names
already given to the cultures and herbarium specimens
under study.
Taxon sampling.Two datasets were compiled, one with
sequences from 5.8S and the nuclear ribosomal large
subunit (LSU dataset) and one smaller dataset with internal
transcribed spacer sequences alone (ITS dataset). The LSU
dataset contained three representatives from most presently
recognized orders within Agaricomycetes (Hibbett et al.
2007). The exceptions are the Polyporales, for which 16
species were included, subclass Phallomycetidae, for which
three species were selected altogether, and the Sebacinales
that was excluded because its members have strongly
deviating nuclear rDNA sequences that make them difficult
to include in a phylogenetically broad sampling. One
representative of the Auriculariales was included to serve
as an outgroup. A higher number of Polyporales species was
included when initial test analyses (not shown) indicated
that Cymatoderma was non-monophyletic. Two sequences of
Hydnopolyporus fimbriatus (Fr.) D.A. Reid, type of Hydnopolyporus D.A. Reid, were included because they produce
basidiocarps with similarities to stipitate stereoid fungi. Two
sequences of Clavulicium macounii (Burt) J. Erikss. &
Boidin ex Parmasto, the type species of Clavulicium Boidin,
and two sequences of Clavulicium globosum Hjortstam &
Ryvarden were added because they have micromorphological similarities to Stereopsis. In all, 30 sequences from
stipitate stereoid fungi were included and four were
downloaded from GenBank. This resulted in a dataset with
88 sequences.
For the ITS dataset 15 sequences from Podoscypha
specimens and six from Cymatoderma specimens as well as
one sequence each from Abortiporus biennis (Bull.) Singer,
Mycoacia fuscoatra (Fr.) Donk, and Phlebia subochracea
(Bres.) J. Erikss. & Ryvarden were selected. In addition, two
sequences available in GenBank were added as the result
of sequence identity searches performed in emerencia
(Nilsson et al. 2005, http://andromeda.botany.gu.se/) with
the user-specified genus search to find unidentified ITS
sequences that could belong in either Podoscypha, Cymatoderma or Abortiporus. The sequences also were subject to
BLAST queries (http://blast.ncbi.nlm.nih.gov/Blast.cgi)
but gave no additional match of significance. This resulted
in a dataset with 26 sequences.
DNA extraction, PCR and sequencing.Mycelial cultures as
well as dried herbarium specimens were used as DNA
sources. Mycelial cultures were grown in a 5% malt liquid
solution in Erlenmeyer flasks 2 wk at room temperature.
About 1020 mg mycelium was taken for DNA extraction.
From dried specimens 45 pieces of 5 3 5 mm hymenium
were taken. DNA extractions, PCR and sequencing reactions
rstadius
were performed as described in Larsson and O
(2008).
Sequence editing, alignment and phylogenetic analyses.
Sequences were assembled and edited with SequencherTM
4.1 (Gene Codes Corp, Ann Arbor, Michigan). Sequences

1048
TABLE I.

MYCOLOGIA
Details of the specimens used in this study
Taxon1

Abortiporus biennis (Bull.) Singer

Athelia decipiens (Hohn. & Litsch.) J. Erikss.
Athelopsis subinconspicua (Litsch.) Julich
Brevicellicium olivascens (Bres.) K.H. Larss.
& Hjortstam
Byssomerulius corium (Pers.) Parmasto
Cerrena unicolor (Bull.) Murrill
Chaetodermella luna (D.P. Rogers &
H.S. Jacks.) Rauschert
Chondrostereum purpureum (Pers.) Pouzar
Clavariadelphus ligula (Schaeff.) Donk
Clavulicium globosum Hjortstam & Ryvarden
Clavulicium globosum
Clavulicium macounii (Burt) Parmasto
Clavulicium macounii
Clavulina cristata (Holmsk) J. Schrot.
Climacocystis borealis (Fr.) Kotl. & Pouzar
Columnocystis abietina (Pers.) Pouzar
Cotylidia aurantiaca var. alba D.A. Reid
Cotylidia diaphana (Schwein.) Lentz
Cotylidia pannosa (Sowerby) D.A. Reid
Cotylidia undulata (Fr.) P. Karst.
Cymatoderma caperatum (Berk. & Mont.)
D.A. Reid
Cymatoderma dendriticum (Pers.) D.A. Reid
Cymatoderma dendriticum
Cymatoderma dendriticum
Cymatoderma elegans Jungh.
Cymatoderma elegans
Cymatoderma pallens Berthet & Boidin
Galzinia sp.
Gloeophyllum sepiarium (Wulfen) P. Karst.
Grifola frondosa (Dicks.) Gray
Grifola sordulenta (Mont.) Singer
Hericium erinaceus (Bull.) Pers.
Hydnopolyporus fimbriatus (Fr.) D.A. Reid
Hydnopolyporus fimbriatus
Hydnum repandum L.
Hygrophoropsis aurantiaca (Wulfen) Maire
Hymenochaete rubiginosa (Dicks.) Lev.
Hyphodontia abieticola (Bourdot & Galzin)
J. Erikss.
Hypochnicium subrigescens Boidin
Inocybe rimosa (Bull.) P. Kumm.
Junghuhnia nitida (Pers.) Ryvarden
Hydnocristella himantia (Schwein.)
R.H. Petersen
Laetisaria fuciformis (McAlpine) Burds.
Lepista sordida (Schumach.) Singer
Meripilus giganteus (Pers.) P. Karst.
Muscinupta laevis (Fr.) Redhead, Lucking
& Lawrey
Mycoacia fuscoatra (Fr.) Donk
Oxyporus corticola (Fr.) Ryvarden
Phlebia radiata Fr.

Herb., voucher/culture2

Origin

Genbank nr3

GB, EL65-03
O, JS4930
GB, KHL13458

Sweden
Norway
Sweden

JN649325
AY463381/AY586632
JN649326

GB, KHL8571
GB, KHL8593
GB, KHL s.n.

Sweden
Norway
Sweden

JN649327
AY463389/AY586640
JQ031127

GB, FCUG 251-1

GB, EL59-97
GB, KHL8560
GB, KHL11228
GB, KHL12592
GB, Norden 37145
GB, KHL12129
GB, EL7-00
GB, KHL 13318
GB, KHL12474
RV.PR98/28
DAOM, DAOM 182136
GB, MJ05-1005
GB, Olsson011101

Sweden
USA
Sweden
Costa Rica
Costa Rica
Sweden
Sweden
Finland
Estonia
Sweden
Puerto Rico
Hungary
Sweden

JN649328
AY463393/AY586644
JN649329
JN649330
JN649331
JN649332
JN649333
AM259213/JQ031126
EU118619
AF261458
AF261459
JN649334
JN649335

O, LR37567
O, Delgado300697
, CBS 615.73
LY 3568, CBS 207.62
, CBS 491.76
NY, Halling 9064
LY 3055, CBS 327.66
GB, K14/475
H, OM12420
CUW, D Hibbett s.n.
TENN, TENN55054
DAOM, DAOM 196448
O, Meijer3729
O, LR40855
GB, KHL8552
GB, EL42 99
O, JS4227

Venezuela
Costa Rica
Sri Lanka
Cameroon
Japan
Australia
Cameroon
Sweden
Finland
USA
Argentina
USA
Brazil
Puerto Rico
Sweden
Sweden
Norway

JN649336
JN649337
JN649338
JN649339
JN649340
JN649341
JN649342
JN649343
JN649344
AY854084/AY629318
AY854085/AY645050
JN649345
JN649346
JN649347
JN649348
AY463411/AY586659
AY463417/AY586665

GB,
GB,
GB,
GB,

KHL12498
KHL 11968
EL75-05
KHL11903

Sweden
Norway
Sweden
Sweden

DQ873601
JQ031128
JN649349
EU118638

GB,
GB,
GB,
GB,

LL36041
Hjm18391
EL4-03
EL2-02

Sweden
Sweden
Sweden
Sweden

AY463435/AY586682
EU118639
JN649350
JN649351

GB, JJ020909
GB, KHL13275
GB, KHL13217

Sweden
Estonia
Estonia

EU118621
JN649352
DQ873641
AY854087/AF287885

SJOKVIST ET AL.: STIPITATE STEREOID FUNGI PHYLOGENY

TABLE I.

Continued
Taxon1

Phlebia subochracea (Alb. & Schwein.)

J. Erikss. & Ryvarden
Phellodon niger (Fr.) P. Karst.
Physisporinus vitreus (Pers.) P. Karst.
Piloderma olivaceum (Parmasto) Hjortstam
Podoscypha bolleana (Mont.) Boidin
Podoscypha brasiliensis D.A. Reid
Podoscypha elegans (G. Mey.) Pat.
Podoscypha involuta (Klotzsch) Imazeki
Podoscypha involuta
Podoscypha mellissii (Sacc.) Bres.
Podoscypha multizonata (Berk. &
Broome) Pat.
Podoscypha parvula (Lloyd) D.A. Reid
Podoscypha parvula
Podoscypha petalodes ssp. rosulata D.A. Reid
Podoscypha petalodes ssp. rosulata
Podoscypha ravenelii (Berk. & M.A.
Curtis) Pat.
Podoscypha sp.
Podoscypha venustula (Speg.) D.A. Reid
Podoscypha venustula
Podoscypha vespillonea (Berk.) Boidin & Lanq.
Porpomyces mucidus (Pers.) Julich
Protodontia piceicola (Bourdot) G.W. Martin
Pseudomerulius aureus (Fr.) Julich
Punctularia strigosozonata (Schwein.)
P.H.B. Talbot
Ramaria abietina (Pers.) Quel.
Russula nauseosa (Pers.) Fr.
Sarcodon imbricatus (L.) P. Karst.
Scopuloides hydnoides (Cooke & Massee)
Hjortstam & Ryvarden
Sistotrema brinkmannii (Bres.) J. Erikss.
Steccherinum ochraceum (Pers.) Gray
Stereopsis humphreyi (Burt) Redhead &
D.A. Reid
Stereopsis radicans (Berk.) D.A. Reid
Stereopsis radicans
Stereopsis radicans
Stereopsis vitellina (Plowr.) D.A. Reid
Stereum subtomentosum Pouzar
Suillus grevillei (Klotzsch) Singer
Tomentellopsis bresadoliana (Sacc. & Trotter)
Julich & Stalpers
Trechispora farinacea (Pers.) Liberta
Uncultured ectomycorrhiza
Uncultured fungus
Vuilleminia macrospora (Bres.) Hjortstam
1

1049

Herb., voucher/culture2

Origin

Genbank nr3

GB, KGN 162-95

TAA, 152713
GB, KHL 11959
GB, EL34-99
LY 5292, CBS 333.66
O, LR37812
CBS 426.51
GB, E. Larsson s.n.
LY 6035, CBS 113.74
O, LR41658

Sweden
JN649353
Estonia
AY463448/AY586694
Norway
JQ031129
Estonia
DQ469289
Central African Rep. JN649354
Venezuela
JN649355
Argentina
JN649356
Thailand
JN649357
Central African Rep. JN649358
Jamaica
JN649359

GB, Jahn751012
LY 5264, CBS 331.66
DAOM, DAOM171399
, CBS 659.84
, CBS 332.66

Germay
JN649360
Central African Rep. JN649361
AF261534
Pakistan
JN649362
Pakistan
JN649363

, CBS 664.84
O, LR43794
O, LR40821
, CBS 656.84
LY 6733, CBS 111.74
GB, KHL8620
GB, KHL11803
GB, Norden 991019

USA
Costa Rica
Venezuela
French Guiana
unknown
Norway
Sweden
Sweden

JN649364
JN649365
JN649366
JN649367
JN649368
AF347092
DQ873660/AY463455/AY586701

O, LR40885
GB, EL61-03
GB, SJ97015
TAA, 152707

Puerto Rico
Sweden
Sweden
Estonia

AY463456/AY586702
JN649369
AF506462
AY463465/AY586711

GB, KHL 11916

GB, NH11412
GB, KHL 11902

Sweden
Turkey
Sweden

EU118665
AF506473/JQ031130

DAOM, DAOM185795
CFMR, PR5760
O, LR45395
CORT, TB8943
GB, Gilsenius
GB, EL11-97
GB, EL38-99

Puerto Rico
Belize
Venezuela
Sweden
Canary Islands
Sweden

AF261382
JN649370
JN649371
JN649372/JN649373
JN649374
AF506482
AF347102

GB, JEH031011
GB, KHL8793

Sweden
Sweden

GB, EL21-99

Canary Islands

EU118674
AF347089
DQ377440
FM999612
AY463483/586726

Type species of stipitate stereoid fungi are given in bold face.

Culture numbers are given in italics. Such numbers are preceded by the corresponding voucher number and/or its
herbarium acronym.
3
Where there are two Genbank numbers they indicate 5.8S (ITS) and LSU respectively.
2

1050

MYCOLOGIA

initially were aligned in Clustal X (Thompson et al. 1997),

followed by manual optimization in SeaView (Gouy et al.
2010). ITS1 and ITS2 as well as 340 positions in
hypervariable regions within LSU were excluded from
analyses of the LSU dataset. In the analysis of the ITS
dataset only 273 characters were used.
Bayesian inference was performed in MrBayes 3.1.2
(Ronquist and Huelsenbeck 2003) using evolutionary
models suggested by MrModeltest 2.3 (Nylander 2004).
The 5.8S was set to model SYM + G and LSU was set to GTR
+ I + G, ITS1 was set to HKY + G and ITS2 K80 + G. Two
runs of eight Monte Carlo Markov chains were performed
for 10 000 000 generations for the LSU dataset and
5 000 000 generations for the ITS dataset, which was at the
point where standard deviation of split frequencies had
stabilized under 0.01, starting from random trees and
sampling respectively one tree every 4000 and every 5000
generations. Burn-in was set to 25%, and a consensus tree
was generated from the sampled trees.

RESULTS
After exclusion of ambiguous regions the LSU
alignment consisted of 1388 characters. All the
sampled orders of Agaricomycetes were recovered as
monophyletic except the Polyporales, which was split
in two well supported lineages (FIG. 1). This was not
unexpected because ribosomal genes alone do not
resolve the Polyporales well (Matheny et al. 2007). All
stipitate stereoid species are included in one of the
orders except Stereopsis radicans. Genus Stereopsis is
not monophyletic; S. radicans forms a highly supported clade with Clavulicium globosum as a separate
lineage in Agaricomycetes, whereas Stereopsis vitellina
(Plowr.) D.A. Reid was recovered within the Atheliales
and S. humphreyi confirmed as a member of the
Agaricales. Clavulicium macounii does not appear
with C. globosum, neither does this species seem to
belong to any previously identified order. Cotylidia
and Cyphellostereum formed a monophyletic group
with members of the Hymenochaetales. All Cymatoderma and Podoscypha species were recovered in the
Polyporales. Podoscypha forms three lineages, a P.
involuta/P. vespillonea clade with strong support, a
lineage solely represented by P. multizonata, and a
lineage formed by the majority of studied Podoscypha
representatives. Cymatoderma elegans and C. caperatum formed a lineage separate from remaining
Cymatoderma and Podoscypha species. Two more
lineages were formed by the singletons C. dendriticum, represented by three specimens, and C. pallens
Berthet & Boidin.
After exclusion of ambiguous regions the ITS
alignment consisted of 273 characters. The sequences
were highly dissimilar, and a considerable number of
characters had to be excluded to incorporate all

Cymatoderma and Podoscypha specimens. Cymatoderma dendriticum, C. pallens and Abortiporus biennis
all formed separate branches (FIG. 2). Podoscypha
multizonata appeared most closely related to P.
involuta (Klotzsch) Imazeki and P. vespillonea (Berk.)
Boidin & Lanq., which formed a well supported
lineage. Cymatoderma elegans and C. caperatum
likewise form a well supported lineage, as do Mycoacia
fuscoatra and Phlebia subochracea. All remaining
sequences belong to Podoscypha and formed a single
distinct and well supported group.
DISCUSSION
We have confirmed that Podoscyphaceae sensu Reid
(1965) is not a monophyletic taxon, as had been
indicated through several studies (e.g. Moncalvo et al.
2002). We concur with Welden (2010) that the family, if
at all retained, can contain only two of the originally
included genera, namely Podoscypha and (part of)
Cymatoderma. This taxon belongs in the Polyporales but
its limits, be it on family or another level, can be
established only through a more comprehensive
phylogenetic study of the order. Other stipitate stereoid
fungi that we included in our analyses were recovered
in the Agaricales, Atheliales and Hymenochaetales.
The most unexpected result is what appears to be a
new lineage within Agaricomycetes formed by Stereopsis radicans and Clavulicium globosum. Clavulicium
macounii, which in morphology is very similar to C.
globosum, also appeared as a new lineage, separate
from the S. radicans/C. globosum clade. Clavulicium
species form strictly resupinate and effused basidiocarps but share with Stereopsis radicans the presence
of two-sterigmate basidia, enclosed gloeocystidia with
refractive contents and globose to ovoid spores. With
the genetic markers selected for this study these
species cannot be assigned to any of the orders
recognized by Hibbett et al. (2007).
The recovery of Stereopsis vitellina among species in
the Atheliales also is remarkable because all known
members of the Atheliales have soft, resupinate,
effused basidiocarps attached to the underside of
logs and twigs. Stereopsis vitellina would be the first
pileus- and stipe-forming species in this order. The
taxonomic implications of the new findings regarding
Stereopsis will be dealt with in separate papers.
As expected Stereopsis humphreyi was recovered as a
member of the Agaricales, confirming Moncalvo et al.
(2002). The remaining species presently assigned to
Stereopsis are morphologically variable and cannot be
redistributed with support from the results presented
here.
Cotylidia and Muscinupta laevis belong in the
Hymenochaetales. This was already well established

SJOKVIST ET AL.: STIPITATE STEREOID FUNGI PHYLOGENY

1051

FIG. 1. Bayesian 50% majority rule consensus phylogram of 5.8S and LSU nuclear rDNA. Bayesian posterior probabilities of
1 are shown as bold branches, and those of 0.90.99 are indicated above or below the supported branch. Stipitate stereoid taxa
are are shown with different colors according to genus. GenBank submission numbers are given where there are more than
one sequence per species.

1052

MYCOLOGIA

FIG. 2. Bayesian 50% majority-rule consensus star phylogram of ITS1 and ITS2 nuclear rDNA . Bayesian posterior
probabilities of 0.91 are indicated next to the supported branch.

(Moncalvo et al. 2002, Redhead et al. 2002, Larsson

et al. 2006), and the sampling we used here was not
designed to add further resolution to the position of
these genera within that order. We concur with
Larsson et al. (2006) that Cotylidia and Muscinupta
are likely closely related and members of what has
been tentatively called the Rickenella clade.
In our analysis of the LSU dataset Podoscypha and
Cymatoderma are firmly placed in the Polyporales
sensu Hibbett et al. (2007). They form together with a
number of other genera, such as Cerrena, Hypochnicium, Mycoacia, Phlebia and Steccherinum, a strongly
supported clade that corresponds to the phlebioid
clade of Larsson et al. (2004) and the residual polypore
clade of Binder et al. (2005). The phylogenetic structure of the Polyporales remains largely unresolved, and
our restricted sampling was not intended to remedy
this situation. However, the sampling still gives a strong
indication that Cymatoderma is non-monophyletic and
that Cymatoderma elegans, the type species of Cymatoderma, together with Cymatoderma caperatum, form a
distinct lineage that is well separated from a lineage

consisting of Podoscypha, the residual Cymatoderma,

and Abortiporus.
Cymatoderma species, just like Podoscypha species,
have four-sterigmate basidia, enclosed gloeocystidia,
and a di- or trimitic hyphal system with clamped
generative hyphae. As in Podoscypha, some species
have thick-walled, metuloid cystidia. The morphological distinction between the two genera is not striking.
Reid (1965) said that Cymatoderma has a folded to
veined hymenium and a radiately crested pileus
surface while both hymenium and pileus surface are
smooth in Podoscypha. Cymatoderma species also have
a tomentum on the pileus with regularly clamped
hyphae, while most Podoscypha species have a
glabrous pileus and if a tomentum exists its hyphae
are irregularly clamped.
Nine species presently are accepted in Cymatoderma
(Kirk et al. 2008). Cymatoderma blumei (Lev.) D.A.
Reid, C. elegans, and C. plicatum (Lloyd) D.A. Reid
have metuloid cystidia, while C. dendriticum, C.
fuscum (Cooke) D.A. Reid, C. sclerotioides (Lloyd)
D.A. Reid, C. africanum Boidin, C. pallens and C.

SJOKVIST ET AL.: STIPITATE STEREOID FUNGI PHYLOGENY

caperatum lack such cystidia. Cymatoderma elegans has
been reported from dead stumps, trunks and fallen
branches, C. caperatum from the same substrates but
also from roots and C. pallens was described from the
trunk of a dead tree. Cymatoderma dendriticum
likewise has been reported from deadwood, but there
is also one collection from flat stony soil with no
presence of deadwood or roots found by digging
(Reid 1965). Cymatoderma africanum is reported to
grow on the ground, according to Reid (1965) arising
from buried wood, but it also has been found among
litter. Remaining Cymatoderma species all have been
collected from deadwood.
In our phylogenetic analyses Cymatoderma is not
monophyletic but forms two or even three lineages.
Cymatoderma elegans, the type species, and C.
caperatum are well separated from the other two
species included in the analyses and also from
Podoscypha. Cymatoderma dendriticum, on the other
hand, occurs as sister taxon to the core group of
Podoscypha and C. pallens appears as yet another
lineage. Cymatoderma dendriticum is the type species
of Cladoderris Pers. ex Berk., a name that for a long
time was used for all Cymatoderma species before the
older name, Cymatoderma, was reintroduced.
The key to Cymatoderma in Reid (1965) divided the
species in two groups according to spore size, and this
observation is congruent with our phylogenetic tree.
Cymatoderma elegans, C. caperatum and three other
species have larger spores, generally 512 mm, elliptical to subcylindrical whereas C. dendriticum and two
other species have smaller, subglobose spores, only 3
4 mm. Cymatoderma pallens was not described when
Reid treated the genus, and it does not fit into a
division based on spore form and size (Berthet and
Boidin 1966). The spores in Cymatoderma pallens are
subglobose making them similar to C. dendriticum,
but with a maximum size around 56 mm they fall
within the range of the C. elegans group. Cymatoderma
sclerotioides also has spores of an intermediate type, 4
5.5 mm long, subcylindrical.
Podoscypha was not recovered as monophyletic but
split into at least two clades. The majority of species
formed a well supported clade that apparently
represents Podoscypha sensu stricto, whereas P.
vespillonea and P. involuta formed another well
supported and clearly separate clade. Podoscypha
multizonata clusters with P. vespillonea and P.
involuta, but this grouping lacks support and the
position of P. multizonata remains unresolved in this
study.
Species in the Podoscypha s.s. clade have a wide
distribution in tropical-subtropical regions and are
found on deadwood, fallen branches, roots, fruits or
on the ground. The type species P. nitidula (Berk.)

1053

Pat. unfortunately is not included in this study but

can be expected to belong to this group because
morphologically it is a typical Podoscypha, with small,
thin, funnel-shaped basidiocarps and with gloeocystidia but no other kinds of cystidia. It most often is
found on the ground and only occasionally reported
from trunks. Because Patouillard (1900) did not
explicitly select a type for his new genus, this was done
later. At first Thelephora elegans G. Mey. was recognized
as type because it was the first species to be listed along
with the original genus description (Cooke 1953).
However, because this name had been variously
interpreted and no type material ever recovered, Reid
(1965) considered that a better defined species should
be selected and suggested Stereum surinamense Lev.
(syn. Podoscypha nitidula) as type.
Podoscypha vespillonea and P. involuta both have
thick-walled encrusted cystidia in addition to the
gloeocystidia and a well developed tomentum on the
pileus. These species are observed mainly in the
paleotropics and are reported to grow on deadwood.
Reid considered P. vespillonea to be synonomous with
P. involuta. However, after negative mating tests
Boidin and Lanquetin (1973) accepted them as
separate species.
Podoscypha multizonata is distinguished from most
other Podoscypha species by forming compound,
rosette-like basidiocarps directly on the ground and
is the only species that develops gloeocystidia on the
upper pileus surface. It is recorded from temperate
Europe and Russian Far East but is not known from
tropical regions, according to Reid (1965).
There is a great morphological resemblance between Podoscypha multizonata and Abortiporus biennis,
and neither show a clear relation to any of the other
studied species in the analyses. Both species grow as
large rosettes on the ground, and the main difference
is that Abortiporus forms a hymenium with shallow
pores. The added GenBank sequence FM999612 of
Abortiporus biennis was generated during a mycorrhizal root tip analysis (Parrent et al. 2006), and
sequence DQ377440 stems from a soil and root study
(Burke et al. 2009). This could suggest that Abortiporus might have a nutritional strategy that is not
based purely on saprotrophy. Because many Podoscypha and Cymatoderma species also are reported to
grow on soil or on roots, the whole clade may display
more varied life strategies than usually considered.
It seems clear that the genera Podoscypha and
Cymatoderma must be revised and that also Abortiporus
should be included in such an endeavor. The
topology and support values recovered in our analyses
indicate two possible outcomes of a revision. Either
two genera could be recognized, one small genus
corresponding to Cymatoderma s.s. and one large

1054

MYCOLOGIA

genus that will include Abortiporus, the residual

Cymatoderma, and the entire genus Podoscypha. The
oldest name for this large genus would be Cladoderris
(Reid 1965). On the other hand several genera could
be recognized, in which case Abortiporus, Cymatoderma, Cladoderris and Podoscypha could be retained
and a new genus introduced for the P. involuta/P.
vespillonea clade and perhaps two other genera for
Podoscypha multizonata and Cymatoderma pallens
respectively. The former solution may seem appealing, because it would hold together many species of
the same general morphology, although Cymatoderma
s.s. must be kept separate. The latter solution
corresponds more closely with current classifications
but causes difficulties for a clear morphological
definition of the genera. We are not prepared to
propose one of the solutions but suggest that further
analyses including more species and more genes are
carried out first.
It appears to us as if the stipitate stereoid
basidiocarp type has evolved on several occasions.
Our study thus supports the observation from other
studies of basidiomycete evolution, that complex,
similar-looking basidiocarps might have multiple
origins (Hibbett et al. 1997, Pine et al. 1999,
Bodensteiner et al. 2004). Stereopsis radicans and
Stereopsis vitellina seem to have independently
evolved from corticoid fungi with effused, resupinate
basidiocarps. It is possible that other groups of
stipitate stereoid fungi also evolved from corticoid
ancestors, although our data in this study does not
clearly resolve such a trend.
ACKNOWLEDGMENTS
We thank Bernard Pfeil and David Hibbett for valuable
comments on the manuscript. This research was supported
by a grant to K-H Larsson from the Swedish Species
Information Centre (35/07 1.4).

LITERATURE CITED
Berthet P, Boidin J. 1966. Observations sur quelques
Hymenomyce`tes recoltes en Republique Camerounaise. Cahiers de la Maboke 4:2754.
Binder M, Hibbett DL, Larsson K-H, Larsson E, Langer E,
Langer G. 2005. The phylogenetic distribution of
resupinate forms in the homobasidiomycetes. Syst
Biodivers 3:113157, doi:10.1017/S1477200005001623
Bodensteiner B, Binder M, Moncalvo J-M, Agerer R, Hibbett
DS. 2004. Phylogenetic relationships of cyphelloid
homobasidiomycetes. Mol Phylogenet Evol 33:510
515, doi:10.1016/j.ympev.2004.06.007
Boidin J, Lanquetin P. 1973. Podoscypha involuta (Klotzsch)
Imaz. est une espe` ce composite (Basidiomyce` tes,
Podoscyphaceae). Persoonia 7:141150.

, Mugnier J, Canales R. 1998. Taxonomie moleculaire des Aphyllophorales. Mycotaxon 66:445491.

Burke DJ, Lopez-Gutierrez JC, Smemo KA, Chan CR. 2009.
Vegetation and soil environment influence the spatial
distribution of root-associated fungi in a mature beechmaple forest. Appl Environ Microbiol 75:76397648,
doi:10.1128/AEM.01648-09
Cooke WB. 1953. The genera of Homobasidiomycetes
(exclusive of the Gastromycetes). USDA Div. Mycol. &
Dis. Surv., Special Publication 3. 100 p.
Garcia-Sandoval R, Wang Z, Binder M, Hibbett DS. 2011.
Molecular phylogenetics of the Gloeophyllales and
relative ages of clades of Agaricomycotina producing a
brown rot. Mycologia 103:510524, doi:10.3852/10-209
Gouy M, Guindon S, Gascuel O. 2010. SeaView 4: a
multiplatform graphical user interface for sequence
alignment and phylogenetic tree building. Mol Biol
Evol 27:221224, doi:10.1093/molbev/msp259
Hibbett DS, Binder M. 2002. Evolution of complex fruitingbody morphologies in homobasidiomycetes. Proc R Soc
Lond B 269:19631969, doi:10.1098/rspb.2002.2123
, , Bischoff JF, Blackwell M, Cannon PF,
Eriksson OE, Huhndorf S, James T, Kirk PM, Lucking
R, Lumbsch T, Lutzoni F, Matheny PB, Mclaughlin DJ,
Powell MJ, Redhead S, Schoch CL, Spatafora JW,
Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R,
Begerow D, Benny GL, Castlebury LA, Crous PW, Dai
YC, Gams W, Geiser DM, Griffith GW, Gueidan C,
Hawksworth DL, Hestmark G, Hosaka K, Humber RA,
Hyde K, Ironside JE, Koljalg U, Kurtzman CP, Larsson
KH, Lichtwardt R, Longcore J, Miadlikowska J, Miller A,
Moncalvo JM, Mozley-Standridge S, Oberwinkler F,
Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L,
Sampaio JP, Schussler A, Sugiyama J, Thorn RG, Tibell
L, Untereiner WA, Walker C, Wang Z, Weir A, Weiss M,
White MM, Winka K, Yao Y-J, Zhang N. 2007. A higherlevel phylogenetic classification of the Fungi. Mycol Res
111:509547, doi:10.1016/j.mycres.2007.03.004
, Pine EM, Langer E, Langer G, Donoghue MJ. 1997.
Evolution of gilled mushrooms and puffballs inferred
from ribosomal DNA sequences. Proc Natl Acad Sci
USA 94:1200212006, doi:10.1073/pnas.94.22.12002
Kirk PM, Cannon PF, David JC, Stalpers JA, eds. 2008.
Dictionary of the Fungi. 10th ed. Wallingford, UK:
CABI Publishing. 771 p.
rstadius L. 2008. Fourteen coprophilous species
Larsson E, O
of Psathyrella identified in the Nordic countries using
morphology and nuclear rDNA sequence data. Mycol
Res 112:11651185, doi:10.1016/j.mycres.2008.04.003
Larsson K-H. 2007. Re-thinking the classification of corticioid fungi. Mycol Res 111:10501063.
, Larsson E, Koljalg U. 2004. High phylogenetic
diversity among corticioid homobasidiomycetes. Mycol
Res 108:9831002, doi:10.1017/S0953756204000851
, Parmasto E, Fischer M, Langer E, Nakasone K,
Redhead SA. 2006. Hymenochaetales: a molecular
phylogeny of the hymenochaetoid clade. Mycologia
98:926936, doi:10.3852/mycologia.98.6.926
Lawrey JD, Lucking R, Sipman HJM, Chaves JL, Redhead
SA, Bungartz F, Sikaroodi M, Gillevet PM. 2009. High

SJOKVIST ET AL.: STIPITATE STEREOID FUNGI PHYLOGENY

concentration of basidiolichens in a single family of
agaricoid mushrooms (Basidiomycota: Agaricales: Hygrophoraceae). Mycol Res 113:11541171, doi:10.1016/
j.mycres.2009.07.016
Matheny PB, Wang Z, Binder M, Curtis JM, Lim YW, Nilsson
RH, Hughes KW, Hofstetter V, Ammirati JF, Schoch
CL, Langer E, Langer G, McLaughlin DJ, Wilson AW,
Frslev T, Ge Z-W, Kerrigan RW, Slot JC, Yang Z-L,
Baroni TJ, Fischer M, Hosaka K, Matsuura K, Seidl MT,
Vauras J, Hibbett DS. 2007. Contributions of rpb2 and
tef1 to the phylogeny of mushrooms and allies
(Basidiomycota, Fungi). Mol Phylogenet Evol 43:430
451, doi:10.1016/j.ympev.2006.08.024
Moncalvo J-M, Vilgalys R, Redhead SA, Johnson JE, James
TY, Aime MC, Hofstetter V, Verduin SJW, Larsson E,
Baroni TJ, Thorn RG, Jacobsson S, Clemencon H,
Miller OK. 2002. One hundred seventeen clades of
euagarics. Mol Phyl Evol 23:357400, doi:10.1016/
S1055-7903(02)00027-1
Nilsson RH, Kristiansson E, Ryberg M, Larsson K-H. 2005.
Approaching the taxonomic affiliation of unidentified
sequences in public databasesan example from the
mycorrhizal fungi. BMC Bioinformatics 6: 1 7,
doi:10.1186/1471-2105-6-178
Nylander JA. 2004. MrModeltest 2.2. Evolutionary Biology
Centre, Uppsala University, Uppsala. Program distributed by the author.
Parrent JL, Morris WF, Vilgalys R. 2006. CO2 enrichment
and nutrient availability alter ectomycorrhizal fungal

1055

communities. Ecology 87:22782287, doi:10.1890/

0012-9658(2006)87[2278:CANAAE]2.0.CO;2
Patouillard N. 1900. Essai taxonomique sur les familles et les
genres des Hymenomyce`tes. Lons-le-Saunier, France:
Imprimerie et Lithographie Lucien Declume. 184 p.
Pine EM, Hibbett DS, Donoghue MJ. 1999. Phylogenetic
relationships of cantharelloid and clavarioid homobasidiomycetes based on mitochondrial and nuclear rDNA
sequences. Mycologia 91:944963, doi:10.2307/3761626
Redhead SA, Moncalvo JM, Vilgalys R, Lutzoni F. 2002.
Phylogeny of agarics: partial systematics solutions for
bryophilous omphalinoid agarics outside the Agaricales
(euagarics). Mycotaxon 82:151168.
Reid DA. 1965. A monograph of stipitate stereoid fungi.
Beih Nova Hedwig 18:1382.
Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian
phylogenetic inference under mixed models. Bioinformatics 19:15721574, doi:10.1093/bioinformatics/btg180
Ryvarden L. 2010. Stereoid fungi of America. Syn Fung 28:
1206.
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F,
Higgins DG. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res
25:48764882, doi:10.1093/nar/25.24.4876
Welden AL. 2010. Stereum s.l. Flora Neotropica Monograph
106:179.
Yoon SI, Kim SE, Lim YW, Jung HS. 2003. Phylogenetic evaluation of stereoid fungi. J Microbiol Biotechnol 13:406414.