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Pseudoclitocybaceae fam. nov. (Agaricales, Tricholomatineae), a new arrangement at family, genus and species level

Authors:
  • Università degli Studi di Torino and Institute for Sustainable Plant Protection (IPSP) – CNR, Viale P.A. Mattioli 25, 10125 Torino, Italy
Article

Pseudoclitocybaceae fam. nov. (Agaricales, Tricholomatineae), a new arrangement at family, genus and species level

Abstract

A new classification of several clitocyboid taxa is here proposed to accommodate results from multigenic phylogenetic inference. The analysis of ITS rDNA as well as a combined dataset including 18S and 28S rDNA, tef1 and rpb2 data, support significantly a shared monophyletic origin of the genera Pseudoclitocybe, Musumecia and Pogonoloma, and the species Clitocybe alexandri and C. harperi. The new family Pseudoclitocybaceae is here proposed to name this clade, characterized by the presence of loop-like clamp connections in most species, absence of cystidia, and parallel hymenophoral trama with broad, cylindrical hyphae with intracellular granulations. The new genera Clitopaxillus and Harmajaea are proposed to accommodate the type species C. alexandri and H. harperi, as well as the combination H. wellsiae. In addition, two new species are described: C. fibulatus has a differential distribution of clamp connections in the basidiome, while H. guldeniae is, by now, an exclusively European taxon with brownish pileus, somewhat decurrent gills, ovoid spores and basidia longer than those of H. harperi. Finally, the species concept within Pseudoclitocybe and Pogonoloma is discussed and descriptions of the most representative species are provided.
1 23
Fungal Diversity
An International Journal of Mycology
ISSN 1560-2745
Volume 90
Number 1
Fungal Diversity (2018) 90:109-133
DOI 10.1007/s13225-018-0400-1
Pseudoclitocybaceae fam. nov. (Agaricales,
Tricholomatineae), a new arrangement at
family, genus and species level
Pablo Alvarado, Pierre-Arthur Moreau,
Bálint Dima, Alfredo Vizzini, Giovanni
Consiglio, Gabriel Moreno, Ledo Setti,
Tapio Kekki, et al.
1 23
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Pseudoclitocybaceae fam. nov. (Agaricales, Tricholomatineae), a new
arrangement at family, genus and species level
Pablo Alvarado
1
Pierre-Arthur Moreau
2
Ba
´lint Dima
3,4
Alfredo Vizzini
5,6
Giovanni Consiglio
7
Gabriel Moreno
8
Ledo Setti
9
Tapio Kekki
10
Seppo Huhtinen
11
Kare Liimatainen
12
Tuula Niskanen
12
Received: 27 November 2017 / Accepted: 19 April 2018 / Published online: 24 April 2018
ÓSchool of Science 2018
Abstract
A new classification of several clitocyboid taxa is here proposed to accommodate results from multigenic phylogenetic
inference. The analysis of ITS rDNA as well as a combined dataset including 18S and 28S rDNA, tef1 and rpb2 data,
support significantly a shared monophyletic origin of the genera Pseudoclitocybe,Musumecia and Pogonoloma, and the
species Clitocybe alexandri and C. harperi. The new family Pseudoclitocybaceae is here proposed to name this clade,
characterized by the presence of loop-like clamp connections in most species, absence of cystidia, and parallel hyme-
nophoral trama with broad, cylindrical hyphae with intracellular granulations. The new genera Clitopaxillus and Har-
majaea are proposed to accommodate the type species C. alexandri and H. harperi, as well as the combination H. wellsiae.
In addition, two new species are described: C. fibulatus has a differential distribution of clamp connections in the
basidiome, while H. guldeniae is, by now, an exclusively European taxon with brownish pileus, somewhat decurrent gills,
ovoid spores and basidia longer than those of H. harperi. Finally, the species concept within Pseudoclitocybe and
Pogonoloma is discussed and descriptions of the most representative species are provided.
Keywords Clitocybe Clitopaxillus Harmajaea Musumecia Pogonoloma Pseudoclitocybe
Introduction
Historically, species of the genus Clitocybe (Fr.: Fr.)
Staude were treated in very different ways. Fries
(1821,1838), defined Clitocybe as a ‘‘tribe’’ of the genus
Agaricus L., based on the shape of the pileus and lamellae
insertion of its species, different from those observed in
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s13225-018-0400-1) contains supplementary
material, which is available to authorized users.
Pablo Alvarado and Pierre-Arthur Moreau have equally contributed to
this work.
&Pablo Alvarado
pablo.alvarado@gmail.com
1
ALVALAB, La Rochela 47, 39012 Santander, Spain
2
Univ de Lille, UFR Pharmacie, EA 4483 IMPECS,
59000 Lille, France
3
Department of Plant Anatomy, Eo
¨tvo
¨s Lora
´nd University,
Pa
´zma
´ny Pe
´ter Se
´ta
´ny 1/c, 1117 Budapest, Hungary
4
Department of Biosciences (Plant Biology), Viikki Plant
Science Centre, University of Helsinki, P.O. Box 65,
00014 Helsinki, Finland
5
Dipartimento di Scienze della Vita e Biologia dei Sistemi,
Universita
`di Torino, Viale P.A. Mattioli 25, 10125 Turin,
Italy
6
Institute for Sustainable Plant Protection (IPSP)-CNR, Viale
P.A. Mattioli 25, 10125 Turin, Italy
7
Via C. Ronzani, 61, 40033 Casalecchio di Reno, BO, Italy
8
Departamento Ciencias de la Vida (Botany), Universidad de
Alcala
´, 28805 Alcala
´de Henares, Madrid, Spain
9
Via C. Pavese 1, 46029 Suzzara, MN, Italy
10
Jyva
¨skyla
¨University Museum, University of Jyva
¨skyla
¨,
P.O. BOX 35, 40014 Jyva
¨skyla
¨, Finland
11
Herbarium University of Turku, 20014 Turku, Finland
12
The Jodrell Laboratory, Royal Botanic Gardens, Kew,
Surrey TW9 3AB, UK
123
Fungal Diversity (2018) 90:109–133
https://doi.org/10.1007/s13225-018-0400-1(0123456789().,-volV)(0123456789().,-volV)
Author's personal copy
other ‘‘tribes’’ that were elevated to the rank of genus such
as Tricholoma (Fr.: Fr.) Staude and Pleurotus (Fr.: Fr.) P.
Kumm. Following the advances in microscopical obser-
vations, each new investigated character led to the exclu-
sion of one or a few species from Clitocybe (Patouillard
1887; Maire 1913; Murrill 1915). The evidence of the
amyloid reaction of spores in some species found by
Ku
¨hner and Maire (1934) led to the creation of the genera
Aspropaxillus Ku
¨hner & Maire (smooth spores) and Leu-
copaxillus Boursier (warty spores; Boursier 1925, sup-
ported by Ku
¨hner’s early observations). Singer employed
the same feature for the definition of additional genera such
as the tricholomatoid Porpoloma Singer (Singer 1952) and
the clitocyboid Cantharellula Singer (Singer 1936). Can-
tharellula included the clampless Pseudoclitocybe (Singer)
Singer (Singer 1943) and the clamped Pseudoomphalina
(Singer) Singer (Singer 1948) as subgenera, but they were
later elevated to genus level (Singer 1956). Most of these
taxa and many others were recently confirmed to represent
independent lineages outside the Clitocybeae Fayod clade
by means of DNA analysis (Redhead et al. 2000,2002;
Harmaja 2003; Walther et al. 2005; Ammirati et al. 2007;
Garnica et al. 2007; Vizzini et al. 2010,2011; Ovrebo et al.
2011; Vizzini and Ercole 2012;Sa
´nchez-Garcı
´a et al.
2014,2016; Alvarado et al. 2015), although the relation-
ships of many species remain largely unresolved. Evidence
that Pseudoclitocybe represents an independent clade from
Clitocybeae was first found by Moncalvo et al. (2002),
Walther et al. (2005) and Garnica et al. (2007), and then
confirmed by Vizzini et al. (2011) who described a new
genus in this linage, Musumecia Vizzini & Contu. Later, a
third genus, Pogonoloma (Singer) Sa
´nchez-Garcı
´a was
confirmed to be related to the Pseudoclitocybe clade by
Sa
´nchez-Garcı
´a et al. (2014).
The species epithet for the type species of Pseudocli-
tocybe,P. cyathiformis (Bull.: Fr.) Singer, was sanctioned
by Fries (1821,asAgaricus cyathiformis Bull). Fries
described this species as having a slightly infundibuliform,
subglabrous, dark to blackish pileus turning pale when dry,
with ashy lamellae and with an elastic fibrillose stipe,
found among mosses on forest soil and on rotten logs. In
the same work he also sanctioned the species epithet for P.
expallens (Pers.: Fr.) M.M. Moser (as A. expallens Pers.:
Fr.), and described a very similar species found from
similar habitats with smaller basidiomata and paler, flat to
umbilicate pileus. Later Fries (1838) also proposed a third
infundibuliform species, P. obbata (Fr.) Singer (as A.
obbatus Fr.), with a glabrous, dark greyish tinted stipe, and
associated with Pinus sp. A fourth species, Clitocybe
bacillaris Pers., with violaceous tints in its lamellae first
found near Betula sp. trees in Vincennes (Paris, France),
was transfered by Singer (1961) and named Pseudoclito-
cybe bacillaris (Pers.) Singer after the examination of the
type specimen revealed clampless hyphae. A fifth Euro-
pean species, Clitocybe atra Velen. (Velenovsky
´1934), a
dark brown fungus found among grasses of a Larix sp.
forest was also transfered to Pseudoclitocybe as P. atra
(Velen.) Harmaja by Harmaja (1974,1976) because of its
clampless hyphae and long amyloid spores. Harmaja
reported that this species was very similar to P. cyathi-
formis, but developed a smaller stipe (4.0–6.5 90.3–1.0 in
P. atra vs. 5.0–10.0 90.5–1.0 cm in P. cyathiformis),
abundant dermatocystidia in the pileus, and can be found in
grasslands. Finally, Singer and Kuthan (1980) described P.
beschidica as a new species growing on rotten logs of
Fagus in the Czech Republic differing from P. cyathiformis
because of its shorter spores not exceeding the length of
8.5 lm, although later reports often merge both taxa
(Kuthan et al. 1999; Adamc
ˇı
´k et al. 2007). As a result of
this confusion at the species level, Bas et al. (1995) rec-
ognized only P. cyathiformis and P. obbata as independent
species, the first growing in woods, the second one in sandy
soils. According to Knudsen & Vesterholt (2008), the name
P. cyathiformis should be applied to non-striated speci-
mens, while P. expallens would be the prioritary synonym
over P. obbata and P. atra, and it would apply to striate
collections growing in herbaceous habitats.
A few species of Clitocybe, e.g. C. alexandri (Gillet)
Gillet and C. harperi Murrill share some morphological
traits with the genera in the Pseudoclitocybe clade, sug-
gesting a putative phylogenetic relationship. Clitocybe
alexandri was first described as Paxillus alexandri Gillet
(Gillet 1873) honouring Paul Alexandre, who collected it
growing among mosses in France, probably at the bois de
la Garenne, Ferrie
`re-Brochard, Alenc¸on (Gillet 1869).
Paxillus alexandri was classified within Paxillus subgen.
Lepista, and subsequently combined as Lepista alexandri
by Gillet (1876) when both genera were separated. The
name was later combined into Clitocybe by Gillet (1884).
Moreau (2009) discussed the morphological species con-
cept of C. alexandri when comparing the typical lowland
European specimens with the paler C. alexandri var. alu-
tacea P.-A. Moreau from Moroccan Cedrus forests. He
observed that typical lowland European specimens lacked
clamp connections in most parts of the basidiome (pileus,
stipe, and pileipellis), in contrast to the observations made
by other authors (Bigelow 1965; Kuyper 1995), and
developed loop-like clamps as well as more or less open
‘false clamps’’ in hymenophoral tissues. European speci-
mens resembling C. alexandri but lacking both clamps and
false clamps were often identified as the North American
species C. harperi Murrill. This taxon was first proposed to
accommodate specimens collected in California and
Washington (Murrill 1913), but later it has been reported
also from Tennessee and Canada (Bigelow 1982), Finland
110 Fungal Diversity (2018) 90:109–133
123
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and Sweden (Harmaja 1969), France (Bon 1997), and
Norway (Gulden 2006).
A broad-ranged phylogenetic analysis on clitocyboid
species by the authors suggested that all these apparently
dissimilar species formed a monophyletic lineage including
the tricholomoid genus Pogonoloma. In the present work, a
formal name for the Pseudoclitocybe clade is introduced, as
well as a systematic and taxonomic treatment of the main
European species recognized in the clade after genetic and
morphological analysis of several modern collections. A
new classification for the whole clade at the family, genus
and species levels is proposed.
Materials and methods
Fungal specimens
Collections from the following public herbaria were stud-
ied: Universidad de Alcala
´, Spain (AH), Associazione
Micologia Bresadola (AMB), Jardin Botanique de Mon-
tre
´al, Canada (CMMF), University of Helsinki, Finland
(H), Universite
´de Lille, France (LIP), Museo di Storia
Naturale di Venezia, Italy (MCVE), University of Michi-
gan, USA (MICH), Botanical Museum, University of Oslo,
Norway (O), University of Turin, Italy (TO), University of
Tartu, Estonia (TU), University of Turku, Finland (TUR,
TUR-A), and University of Washington, USA (WTU-F).
Specimens (or duplicates) from private herbaria of Didier
Borgarino (DBo) and Ba
´lint Dima (DB) were also used for
this study (Online Resource 1). For light microscopy (LM),
spores were mounted in water, Melzer’s reagent, lactic acid
in glycerol (Kirk et al. 2001) or alkaline latex L4 (Cle
´m-
enc¸on 1972). Twenty-five to fifty spores per specimen were
arbitrarily selected and measured partly with Mycometre 2
(Fanneche
`re 2006). A standardized protocol to test amy-
loidity was applied: a lamellae sample was hydrated in tap
water for 1–2 h, and then heated in a drop of Melzer’s
reagent in a teaspoon until the boiling point was reached.
The sample immersed in Melzer was immediately removed
from the heat and transferred to a flat Teflon surface, cut
into three or four pieces, and transferred again to a slide
with a drop of fresh Melzer’s reagent. The excess liquid is
then removed and the sample gently squashed, and exam-
ined with a 609or 1009brightfield objective (numerical
aperture NA 1.3, diaphragm open to about 50% range,
aperture field 0.9–1.0).
DNA extraction, PCR amplification
and sequencing
DNA extraction and PCR amplification were performed as
described by Alvarado et al. (2015) or else following Dima
et al. (2016). Primers ITS1F and ITS4 (White et al. 1990;
Gardes and Bruns 1993) were used for the ITS region;
primers LR0R and LR5 (Vilgalys and Hester 1990) were
used for the 28S rDNA, NS19b and NS41 (Hibbett 1996)
for the 18S rDNA, EF1-983F and EF1-1567R (Rehner and
Buckley 2005) for the translation elongation factor 1a
(tef1) gene, and bRPB2-6F, bRPB2-7R, fRPB2-7cR and
bRPB2-7R2 for the DNA-directed RNA polymerase II
second largest subunit two (rpb2) gene (Liu et al. 1999;
Matheny 2005; Matheny et al. 2007), for both PCR and
sequencing. Sequences were edited for errors in MEGA 5
(Tamura et al. 2011).
Phylogenetic analysis
Sequences were aligned with the most similar sequences in
GenBank identified through BLASTn searches (Altschul
et al. 1990). Two alignments were constructed: 41 ITS
sequences and a combined 28S rDNA-rpb2-tef1-18S rDNA
alignment including sequences from 72 specimens.
Homologous sequences were retrieved from Moncalvo
et al. (2002), Matheny et al. (2007), Binder et al. (2010),
Malysheva et al. (2010), Baroni and Matheny (2011),
Baroni et al. (2011), Vizzini et al. (2010,2011,2012), He
et al. (2013), Lodge et al. (2014), Osmundson et al. (2013),
Hofstetter et al. (2014), Musumeci and Contu (2014), Qin
et al. (2014), Sa
´nchez-Garcı
´a et al. (2014,2016), Alvarado
et al. (2015), Musumeci (2014), and Li et al. (2016).
Sequences first were aligned in MEGA 5 (Tamura et al.
2011) with Clustal W (Thompson et al. 1994) and edited
manually. The ITS alignment contained large insertions in
some species, but these regions were excluded from the
final analyses. Alignments are available in TreeBase
(S21775).
Aligned loci were subjected to MrModeltest 2.3 (Ny-
lander 2004) in PAUP*4.0b10. Bayesian analysis was
performed with optimal models in MrBayes 3.1 (Ronquist
and Huelsenbeck 2003) with 28S rDNA-rpb2-tef1-18S
rDNA data partitioned, two simultaneous runs, six chains,
temperature set to 0.2, and sampling every 100th genera-
tion until convergence parameters were met after about
1.45M (ITS) and 1.88M generations (28S rDNA-rpb2-tef1-
18S rDNA). The first 25% trees were discarded as burn-in.
Last, a full query for the best-scoring maximum likelihood
tree was performed in RAxML (Stamatakis 2006) using the
standard search algorithm (28S rDNA-rpb2-tef1-18S rDNA
data partitioned, 2000 bootstrap replications). Support
values were considered significant when bootstrap (BP)
values were above 70% and posterior probability (PP)
values were above 0.95.
Fungal Diversity (2018) 90:109–133 111
123
Author's personal copy
Results
Phylogenetic analysis
Bayesian and ML analyses of the combined 28S rDNA-
rpb2-tef1-18S rDNA dataset (Fig. 1) significantly support
the existence of at least six major lineages within the
Tricholomatineae Aime, Dentinger & Gaya (Dentinger
et al. 2015): those formed by the families Biannulariaceae
Ju
¨lich (= Catathelasmataceae Wasser), Entolomataceae
Kotl. & Pouzar, Lyophyllaceae Ju
¨lich, Tricholomataceae
R. Heim ex Pouzar, as well as the Clitocybeae and the
Pseudoclitocybe clades. A significant relationship was
obtained between Biannulariaceae and Tricholomataceae,
and between Entolomataceae and Lyophyllaceae, as
already noticed by Sa
´nchez-Garcı
´a et al. (2016). Beside the
monophyletic core of the Lyophyllaceae, several lineages
seem more distantly related (Atractosporocybe P. Alvar-
ado, G. Moreno & Vizzini, Clitocybe cf. subditopoda Peck,
Clitolyophyllum Sesli, Vizzini & Contu, Leucocybe Viz-
zini, P. Alvarado, G. Moreno & Consiglio, Rhizocybe
Vizzini, G. Moreno, P. Alvarado & Consiglio, Tephro-
derma Contu & Musumeci), suggesting a putative wider
concept of this family or the existence of multiple lineages
basal to it, in agreement with previous works (Alvarado
et al. 2015; Bellanger et al. 2015). These four families were
significantly related with the Clitocybeae and the lineages
of Pseudoomphalina and Cleistocybe Ammirati, A.D.
Parker & Matheny.
Multigenic (Fig. 1) and ITS rDNA (Fig. 2) analyses
agree to support significantly the monophyletic origin of
Pseudoclitocybe,Musumecia,Pogonoloma,‘Clitocybe’’
alexandri and ‘Clitocybe’’ harperi.Pogonoloma was
consistently found to be the most basal clade of the group.
Three different genetic lineages were found in the ‘Clito-
cybe’’ harperi clade, two of them present in America and
Europe, and the other found only, by now, in Europe. In
addition, two lineages were observed in the clade of ‘Cl-
itocybe’’ alexandri, one of them composed of samples
coming from lowland European areas with ‘‘false’’ clamp
connections in the hymenium and subhymenium, the other
found in alpine or boreal habitats presenting clamp con-
nections all over the basidiome. Based on these phyloge-
netic results, an updated taxonomic arrangement of these
lineages is proposed below, and the main differences
between them are summarized in Table 1.
Taxonomy
Pseudoclitocybaceae Vizzini, Consiglio, P.-A. Moreau &
P. Alvarado, fam. nov.
Mycobank MB 823302
Etymology: from the type genus Pseudoclitocybe
Diagnosis: Large- to medium-sized basidiomes
(5–15 cm), tricholomatoid or clitocyboid, pileus umbilicate
to convex-applanate, sometimes with persistent umbo,
hygrophanous or not, lamellae decurrent, subdecurrent to
uncinate; mycelium usually developed superficially on
substrate as patches with or without rhizomorphs, rooting
in tricholomatoid species; hymenophoral trama subregular
to somewhat divergent; context homomorphous with
cylindrical hyphae [4lm diam., usually with acyano-
philic intracellular globules, mixed or not with thrombo-
plerous hyphae, exclusively sarcodimitic in tricholomatoid
species; subhymenium ramose, repent, easily dissociated;
hymenium usually without cystidia; basidia narrowly cla-
vate, small, mostly \35 98lm, without siderophilic
granulations; loop-like (medallion) clamp connections
usually present at least in mycelium; pileipellis a dry or
weakly gelatinized cutis, frequently diverticulate, occa-
sionally a trichocutis; spores usually smooth, amyloid or
not, acyanophilous, with broad, truncate and prominent
apicule; mating behaviour heterothallic bipolar (for docu-
mented species); nuclear behaviour holocoenocytic (for
documented species, spores binucleate and terminal hyphae
in the primary mycelium plurinucleate). Probably only
saprobic (uncertain for Pogonoloma). Present worldwide,
mostly temperate to boreal.
Type genus: Pseudoclitocybe (Singer) Singer
Clitopaxillus G. Moreno, Vizzini, Consiglio & P.
Alvarado, gen. nov.
Mycobank MB 823303 (Figs. 3b, c, 4a, b, g, h)
Etymology: from Clitocybe and Paxillus, the genera
where C. alexandri was previously classified.
Diagnosis: basidiomes large-sized, clitocyboid, fleshy, with
convex to flattened brownish pileus lacking umbo, glabrous
pileipellis, not hygrophanous. Lamellae deeply decurrent.
Spores slightly amyloid, ovoid. Saprobic, on litter. Clamp
connections present at least on hymenophoral hyphae and
mycelium. Northern Hemisphere, Europe and North Africa.
Type species: Clitopaxillus alexandri (Gillet) G. Mor-
eno, Vizzini, Consiglio & P. Alvarado
Comments: species of Clitopaxillus were previously
considered members of Clitocybe section Disciformes (Fr.)
Que
´l., along with C. harperi (Singer 1986; Bon 1991),
which is also transferred to a new genus in the present
work. Another remarkable member of this section is C.
c
Fig. 1 50% majority rule 28S rDNA-rpb2-tef1-18S rDNA consensus
phylogram of the family Pseudoclitocybaceae and related families of
the tricholomatoid clade obtained in MrBayes from 14,100 sampled
trees. Nodes were annotated if supported by [0.95 Bayesian PP (left)
or [70% ML BP (right). Non-significant support values are excep-
tionally represented inside parentheses
112 Fungal Diversity (2018) 90:109–133
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AFTOL ID-717 Suillus pictus
AFTOL ID-1557 Pseudoarmillariella ectypoides
AFTOL ID-542 Ampulloclitocybe clavipes
AFTOL ID-1508 Infundibulicybe gibba
ALV4344 Infundibulicybe geotropa
GB:0087013 Notholepista subzonalis
TUR 205933 Harmajaea wellsiae
TUR 201099 Harmajaea guldeniae
O-64624 Harmajaea guldeniae
TUR 173042 Harmajaea harperi
LIP 0401361 Harmajaea harp eri
TENN 061314 ‘Pseudoclitocybe sp.
Tang-1778 Musumecia alpina
Yang-090 Musumecia alpina
TO HG2284 Musumecia bettlachensis
LUG18975 Musumecia vermicularis
TO AV45634 Clitopaxillus alexandri
AMB 18221 Clitopaxillus alexandri
TUR 170200 Clitopaxillus fibulatus
TO AV190916 Clitopaxillus fibulatus
AMB 18231 Pseudoclitocybe obbata
AMB 17140 Pseudoclitocybe obbata
AFTOL ID-1998 Pseudoclitocybe cyathiformis
K(M):107286 Pogonoloma spinulosum
TENN:037026 Pogonoloma macrorhizum
GB:0110967 Pseudoclitopilus rhodoleucus
AFTOL ID-1719 Pseudoomphalina angelesiana
T0HG22102011C/GB0066625 Pseudoomphalina kalchbrenneri
AFTOL 721 Cleistocybe vernalis
TENN063842 Cleistocybe carneogrisea
DAOM221514 Catathelasma ventricosum
AFTOL 978 Callistosporium graminicolor
JM99/124 Callistosporium luteoolivaceum
TJB9847 Pleurocollybia imbricata
PBM3028 Clitocybe aff. fellea
GB:0066637 Pseudolaccaria pachyphylla
TH9693 Guyanagarika aurantia
MCA1519 Guyanagarika anomala
PDD97890 Tricho loma virid ioliv acea
AFTOL ID-497 Tricholoma palustre
KMS 590 Tricholoma subaureum
KMS 589 Tricholoma myomyces
TENN:064489 /NYBG:00505218 Pseudotricholoma umbrosum
TENN:064620 Albomagister subaustralis
CFMR BZ 4245 Dennisiomyces sp.
CONC:F0416 Porpoloma sejunctum
DED5462 Corneriella bambusarum
GB:0110968 Leucopaxillus paradoxus
ME Noordeloos 200435 Rhodophana nitellina
N. Dam 05094 Rhodophana stangliana
TB5856 Entocybe trachyospora
TB6949 Entocybe turbidum
TB7526 Entocybe nitida
VHAs0102 Leptonia serrulata
GDGM 27313 Entoloma abortivum
AFTOL ID-523 Entoloma prunuloides
AFTOL ID-524 Entoloma sinuatum
ME Noordeloos 9867 Clitocella popinalis
CBS 129.63 Clitocella fallax
AFTOL ID-521 Clitocella mundula
TB8229 Clitopilus prunulus
TO AV131 Clitopilus cystidiatus
M536 WAT26394 Clitopilus apalus
CBS 577.87 Clitopilopsis hirneola
CoDavid 418 E1589 Rhodocybe lateritia
CoDavid 118 E652 Rhodocybe pallidogrisea
JM99/233 Rhodocybe paurii
HC 84/75 Tricholomella constricta
CBS 683.82 Asterophora parasitica
DUKE-D604/DUKE-D483 Ossicaulis lignatilis
BSI92/245 Sagaranella tylicolor
CBS 717.87 Sphagnurus paluster
CBS 204.47 Tephrocybe rancida
CBS 330.85 Myochromella inolens
HC 77/133 Calocybe ionides
HAe 251.97 Lyophyllum leucophaeatum
HC85/13 Lyophyllum semitale
DUKE-JM/HW Hypsizygus ulmarius
AH44073 Rhizocybe pruinosa
AH44078 Rhizocybe vermicularis
TO AV261012h Atractosporocybe inornata
LUG18989 Tephroderma fuscopallens
KATO Fungi 31 84 Clitolyophyllum akcaabatense
AFTOL 533 Clitocybe cf. subditopoda
JM90c Leucocybe connata
AFTOL ID-541 Leucocybe candicans
TO AV071112a Singerocybe phaeophthalma
TENN:64652 Singerocybe adirondackensis
HKAS:77290 Singerocybe umbilicata
HKAS:75453 Singerocybe clitocyboides
HKAS:74716 Singerocybe alboinfundibuliformis
AFTOL ID-1495 Clitocybe nebularis
CBS 362.65 Clitocybe nebularis
AFTOL ID-815 Lepista cf. irina
IE-BSG-HC95.cp3 Clitocybe dealbata
AFTOL ID-557 Collybia tuberosa
1.00/100
1.00/100
1.00/99
1.00/100
1.00/100
1.00/100
0.79/81
1.00/100
0.98/73
1.00/100
0.82/80
1.00/100
0.96/74
1.00/100
1.00/100
1.00/100
1.00/100
1.00/100
1.00/100
1.00/100
1.00/69
1.00/91
1.00/100
1.00/98
1.00/90
1.00/100
1.00/90
1.00/87
1.00/99
1.00/62
1.00/100
1.00/100
100
1.00/100
0.97/59
1.00/98
1.00/100
1.00/100
1.00/100
1.00/86
1.00/96
1.00/100
1.00/100
1.00/91
1.00/63
1.00/91
0.95/53
1.00/51
0.99/48
1.00/100
0.98/50
1.00/95
1.00/58
1.00/100
1.00/91
1.00/100
1.00/59
0.99/-
1.00/97
1.00/100
1.00/100
1.00/99
0.97/50
(0.83/57)
1.00/79
0.96/44
1.00/98
0.99/72
1.00/96
0.05
Harmajaea gen. nov.
Musumecia
Clitopaxillus gen. nov.
Pseudoclitocybe
Pogonoloma
Pseudoclitocybaceae
fam. nov.
Biannulariaceae
Tricholomataceae
Entolomataceae
Lyophyllaceae s.l.
Clitocybeae
Fungal Diversity (2018) 90:109–133 113
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nebularis, currently retained as the most suitable lectotype
species of Clitocybe (for discussion see Redhead et al.
2002), which lacks a central umbo and loop-like clamp
connections, and has cyanophilous, non-amyloid and rough
spores, and which belongs phylogenetically to the Clito-
cybeae clade (Matheny et al. 2006).
Clitopaxillus alexandri (Gillet) G. Moreno, Vizzini,
Consiglio & P. Alvarado, comb. nov.
Mycobank MB 823304 (Fig. 3b)
Basionym: Paxillus alexandri Gillet, Bull. Soc. Linn.
Normandie, se
´r. 2 7: 157 (1873)
:Lepista alexandri (Gillet) Gillet, Hyme
´nomyce
`tes
(Alenc¸on): 196 (1876)
:Clitocybe alexandri (Gillet) Gillet, Tabl. analyt.
Hyme
´nomyc. France (Alenc¸on): 28 (1884)
=Clitocybe alexandri var. alutacea P.-A. Moreau in
Maire et al., Compl. Fl. Champ. sup. Maroc. G. Malenc¸on
et R. Bertault: 449 (2009)
=Agaricus propinquus var. spadiceus Pers., Mycol. eur.
(Erlanga) 3: 63 (1828) (fide Singer 1961)
=Paxillus extenuatus s. Ricken (1915)
=Clitocybe harperi s. Bon (1991)
Description: Pileus first convex, flattened with age, with
a central umbo, grayish brown to reddish yellow, with
margin enrolled, measuring (5–)10–15(–20) cm in diam.,
smooth, somewhat guttulated and finally cracked. Lamellae
arcuate to decurrent, pale brownish grey to yellowish,
subconcolorous. Stipe 4–10 92–4(–5) cm, solid, cylin-
drical, yellowish white to pale yellow. Context whitish,
dense. Smell cyanic (i.e., bitter almonds). Spores
4.7–5.5 93.5–3.9 lm (n = 32), (average 5.1 93.7 lm),
Q = 1.27–1.49 (Q
m
= 1.38); V
m
=36lm
3
, broadly ellip-
soid to ellipsoid in front view, slightly amygdaliform to
larmiform in side view, hyaline; hilar appendix often very
pronounced, 0.8–1 lm long; in Melzer’s spore wall stains
bluish-gray. Basidia 26–31 94.9–5.8 lm, four-spored, a
few two-spored, long clavate to subcylindrical, sterigmata
up to 5 lm long. Hymenophoral trama subregular, com-
posed of hyphae up to 12 lm wide, hyaline in alkaline
latex L4, yellow in Melzer’s. Cheilocystidia and pleuro-
cystidia not observed. Pileipellis a trichocutis of variously
intertwined, very loose, slightly gelatinized, filamentous
hyphae, 3.0–6.3 lm wide, smooth, with intracellular
brownish pigment, sometimes with a very fine encrusting
epiparietal pigment. Pileitrama hyphae cylindrical, up to
12.6 lm wide, thromboplerous hyphae rare and incon-
spicuous. Clamp connections present at all septa of the
subhymenial hyphae and at the base of basidia and basid-
ioles, occasionally verticillate or unclosed (‘‘false
clamps’’), scattered in mycelium, absent elsewhere.
Ecology: mediterraneo-atlantic, found in deep litter
under pines (P. halepensis,P. pinea,P. sylvestris,P.
uncinata) and oaks (Quercus ilex,Q. pubescens, etc.),
along the Atlantic coasts, also with Cedrus atlantica in
North Africa. Mediterranean basin and Central Europe.
Specimens examined:FRANCE: Pas-de-Calais, Dan-
nes, Mont Saint-Frieux, under a single Quercus ilex in back
of a dune, leg. R. Courtecuisse, 20-X-1991, LIP RC/
F91.232. Vaucluse, Cadenet, les Gardis, on chalk under
Quercus ilex and Pinus halepensis, leg. D. Borgarino,
01-XI-2002, D. Borgarino 021103/LIP 0401379. Vaucluse,
Cadenet, La Roue
`re, under Quercus pubescens and Pinus
halepensis, leg. D. Borgarino, P.-A. Moreau, 26-XI-2011,
LIP 0401301/PAM11112619. ITALY: Bologna, S. Laz-
zaro di Savena, Parco dei Gessi e dei Calanchi dell’Ab-
badessa, Via dell’Eremo, under Quercus pubescens and Q.
cerris, leg. G. Consiglio & G. Spisni, 26-X-1996, AMB
18221/GC 96242. Ibidem, Cerreto di Gaibola, 29-XI-2007,
AMB 18219/GC 07537. Ibidem, Madonna dei Boschi,
31-X-2010, AMB 18220/GC 10181. Torino, Val di Susa,
Colle del Lys, 1300 m a.s.l, under Pinus sylvestris, leg.
A. Vizzini, 21-IX-2013, TO AV45634. Veneto, Vicenza,
Malo, Isola Vicentina, Pinus sp., leg. S. Dalla Valle,
01-XII-2009, MCVE 25090. NORWAY: Telemark,
Bamble, Langøya, calcareous forest, leg. T. H. Dahl, I.
J. Kittilsen, 06-X-2001, 153/2001, O-175145. SPAIN:
Guadalajara, dam of El Vado, Valdesotos, under Pinus
halepensis, leg. R. Gala
´n, 5-XI-2010, AH 39034.
Guadalajara, Anguita, under Quercus ilex and Juniperus
thurifera, on basic soil, leg. D. Martı
´nez, 9-XI-2010, AH
39054. Guadalajara, Budia, under Pinus pinea and Quercus
ilex, leg. J. Menendez, 7-XI-2010, AH 39068.
Comments: No original or topotypical collection of C.
alexandri could be traced, but the original locality near
Alenc¸on (western France), in a hilly area under Atlantic
climate, matches the species described here, rather than the
boreo-alpine lineage described below as C. fibulatus.No
typification of C. alexandri is proposed at this time, in
expectation of collections found around the original
locality. Singer (1961) studied original material of Agari-
cus propinquus var. spadiceus Pers. and concluded that this
taxon could be a synonym of C. alexandri, but he could not
check any specimen of A. propinquus Pers. var. propinquus
(synonymized to A. vinosus Bull.: Fr., Fries 1832), avoid-
ing any nomenclatural change. Paxillus extenuatus Fr., not
interpreted in modern taxonomy, has also been applied to
C. alexandri, for instance by Ricken (1915), but Fries
(1838) described its pileus as umbonate at first and a base
c
Fig. 2 50% majority rule consensus ITS rDNA phylogram of the
family Pseudoclitocybaceae obtained in MrBayes from 10,875
sampled trees. Nodes were annotated if supported by [0.95 Bayesian
PP (left) or [70% ML BP (right). Non-significant support values are
exceptionally represented inside parentheses
114 Fungal Diversity (2018) 90:109–133
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KT122792 Infundibulicybe geotropa
JQ639162 Pogonoloma macrorhizum -Italy
JF908328 Pogonoloma macrorhizum -Italy
KP453700 Pogonoloma macrorhizum -Austria
JF908326 ‘Leucopaxillus nauseosodulcis-Italy
Pogonoloma macrorhizum LIP 0101353 -Switzerland
Pogonoloma macrorhizum AMB 18232 -Italy
Pogonoloma spinulosum LIP 0101354 - France
Pogonoloma spinulosum LIP 0401167 - France
Pogonoloma spinulosum LIP 0401166 - France
KP453706 Pogonoloma spinulosum - United Kingdom
KP453705 Pogonoloma spinulosum - United Kingdom
KP453703 Pogonoloma spinulosum - United Kingdom
KP453704 Pogonoloma spinulosum - United Kingdom
UDB001486 Pogonoloma spinulosum -Denmark
Harmajaea harperi TUR 173042 -Finland
Harmajaea harperi TUR 164187 -Finland
Harmajaea harperi H 6067456 -Finland
KP453697 ‘Pseudoclitocybe sp.’ -USA
Harmajaea harperi LIP 0401361 -USA
Harmajaea harperi WTU-F-006299 -USA
Harmajaea harp eri CMMF 014712 - Canada
Harmajaea guldeniae TUR 201099 - Finland
Harmajaea guldeniae O-74110 -Norway
Harmajaea guldeniae O-64624 -Norway
Harmajaea guldeniae H 6067433 - Finland
Harmajaea guldeniae H 6067444 - Finland
Harmajaea guldeniae H 6067455 - Finland TYPE
Harmajaea guldeniae H 6067432 - Finland
Harmajaea guldeniae H 6051797 - Finland
Harmajaea wellsiae TUR 205933 -Finland
Harmajaea wellsiae WTU-F-024810 -USA
Harmajaea wellsiae MICH 10217 -USA TYPE
KF941322 Musumecia vermicularis -France
KF941323 Musumecia vermicularis -France
KF941324 Musumecia vermicularis -France
KT122794 Musumecia sardoa -Italy
JF926520 Musumecia bettlachensis -France
KR909097 Musumecia alpina -China
KR909098 Musumecia alpina -China
KR909099 Musumecia alpina -China
KF291250 Pseudoclitocybe cyathiformis -USA
Pseudoclitocybe sp. LIP 0401355 -USA
HQ533021 Cantharellula foetida - New Zealand
GU187553 Pseudo clitocy be cya thifor mis -USA
KC505562 Pseudoclitocybe cyathiformis - China
JF926522 Pseudoclitocybe cyathiformis - Italy
Pseudoclitocybe cyathiformis LIP 0901300 -France
HM191730 Pseudoclitocybe cyathiformis - Russia
Pseudoclitocybe cyathiformis LIP 0401359 -France
Pseudoclitocybe cyathiformis AMB 18225 -Italy
UDB011432 Pseudo clitoc ybe cyat hiform is -Estonia
Pseudoclitocybe cyathiformis AMB 18226 -Italy
Pseudoclitocybe cyathiformis AMB 18227 -Italy
KP453710 Pseudoclitocybe cyathiformis -Sweden
KP453709 Pseudoclitocybe cyathiformis -USA
Pseudoclitocybe cyathiformis AMB 18228 -Italy
HM191729 Pseudo clitocy be cya thifor mis -Russia
Pseudoclitocybe cyathiformis LIP 0401360 -France
UDB015516 Pseudoclitocybe expallens -Estonia
Pseudoclitocybe cyathiformis TO HG123012A -Italy
KR673477 Pseudoclitocybe cyathiformis -South Korea
Pseudoclitocybe obbata LIP 0401357 -France
JF926524 Pseudoclitocybe expallens -Italy
Pseudoclitocybeobbata AH 46369 -Spain
Pseudoclitocybe obbata LIP 0401358 -France
KF482480 ‘Laccaria laccata’ - Portugal
Pseudoclitocybe obbata AMB 18229 -Italy
Pseudoclitocybe obbata AMB 18230 -Italy
Pseudoclitocybe obbataAMB 18231 -Italy
Clitopaxillus alexandri TO AV45634 -Italy
Clitopaxillus alexandri AH 39034 -Spain
Clitopaxillus alexandri AH 39068 -Spain
Clitopaxillus alexandri LIP RC/F91.232 -France
Clitopaxillus alexandri AH 39054 -Spain
Clitopaxillus alexandri AMB 18221 -Italy
Clitopaxillus alexandri AMB 18220 -Italy
Clitopaxillus alexandri AMB 18219 -Italy
Clitopaxillus alexandri MCVE 25090 -Italy
Clitopaxillus alexandri LIP 0401301 -France
Clitopaxillus alexandri LIP 0401379 -France
Clitopaxillus alexandri O-175145 -Norway
Clitopaxillus fibulatus O-82070 -Norway
Clitopaxillus fibulatus O-82069 -Norway
Clitopaxillus fibulatus O-74584 -Norway
Clitopaxillus fibulatus LIP 0401380 -France
Clitopaxillus fibulatus AMB 18222 -Italy
Clitopaxillus fibulatus LIP 0401381 -France
Clitopaxillus fibulatus AMB 18223 -Italy
Clitopaxillus fibulatus TUR 165285 -Finland
Clitopaxillus fibulatus TUR 170200 -Finland
Clitopaxillus fibulatus TUR-A-140440 -Finland
Clitopaxillus fibulatus AMB 18224 -Italy TYPE
Clitopaxillus fibulatus TO AV190916 -Italy
Clitopaxillus fibulatus TU 106015 -Estonia
JF907816 Clitocybe cf. alexandri -Italy
Clitopaxillus fibulatus DB 6191 -Norway
1.00/100
0.51/95
1.00/100
0.90/90
1.00/100
1.00/100
0.99/100
0.98/90
0.79/85
1.00/100
0.93/79
0.99/73
0.99/79
1.00/97
(0.74/69)
1.00/100
0.91/97
1.00/100
1.00/73
0.92/83
0.59/80
0.91/76
0.88/92
1.00/100
1.00/98
1.00/100
0.97/65
1.00/65
0.5
Pogonoloma macrorhizum
Pogonoloma spinulosum
Harmajaea harperi
Harmajaea guldeniae
sp. nov.
Harmajaea wellsiae
Musumecia vermicularis
Musumecia alpina
Musumecia sardoa
Musumecia belach ensis
Pseudoclitocybe
cyathiformis (I)
Pseudoclitocybe
cyathiformis (II)
Pseudoclitocybe obba ta
Clitopaxillus alexandri
Clitopaxillus fibulatus
sp. nov.
Pogonoloma Harmajaea Musumecia Pseudoclitocybe Clitopaxillus
Fungal Diversity (2018) 90:109–133 115
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‘tuberoso-radicato’’, two features recalling A. vinosus Bull.
cited above (Bulliard 1782: tab. 54) and incompatible with
any species of Clitopaxillus known to us.
Clitopaxillus fibulatus P.-A. Moreau, Dima, Consiglio, &
Vizzini, sp. nov.
Mycobank MB 823305 (Figs. 3c, 4a, b, g, h)
Etymology: from Latin ‘fibula’ (brooch) referring to the
hyphal clamps present on all septa.
Diagnosis: basidiomes 4–10 cm in diam., clitocyboid,
fleshy, with convex to flattened brownish pileus lacking
umbo, glabrous pileipellis, not hygrophanous. Lamellae
adnate to decurrent. Spores 6.1 94.4 lm on average,
slightly amyloid, ellipsoid; hymenial cystidia present.
Saprobic, on litter. Clamp connections present at all septa.
Boreo-alpine, under Picea abies and Abies alba in Europe.
Type collection: ITALY: Trentino, Pozza di Fassa,
Valle S. Nicolo
`, under Picea abies, leg. G. Consiglio,
22-VIII-1997, AMB 18224/GC 97079 (holotype).
Description: Pileus first convex then expanded or
slightly depressed with age, cream to ochraceous grey or
buff with margin enrolled, measuring 4–10 cm in diam.,
finely tomentose when young developing distinctive, con-
centric wrinkles and cracks with age. Lamellae crowded,
adnate to decurrent, cream to yellowish buff. Stipe
3.5–8.0 91.5–3.0 cm, solid, cylindrical to clavate, cov-
ered with whitish fibrils, later becoming buff, whitish
cream tomentose at base with well-developed whitish
mycelial strands. Context whitish cream, firm when young,
later spongy. Smell aromatic, spicy. Spores
5.7–6.4 94.1–4.6 lm (n = 32), (average 6.1 94.4 lm),
Q = 1.30–1.47 (Q
m
= 1.39); V
m
=62lm
3
, broadly ellip-
soid to ellipsoid, hyaline or with dull, granuliform content,
usually with one big oily drop; slightly amyloid in a not
very pronounced gray, smooth. Basidia
21–33 95.8–7.8 lm, four-spored, clavate, sterigmata up
to 5.2 lm long. Hymenophoral trama irregular, composed
of hyphae until 12 lm wide, hyaline in alkaline latex L4,
yellow in Melzer’s. Cheilocystidia 31–41 97.8–8.3 lm,
long lageniform to long clavate, scattered on the lamellar
edge. Pleurocystidia scattered, similar to cheilocystidia.
Pileipellis a trichocutis of subparallel to variously inter-
twined, gelatinized, filamentous hyphae, 2–7 lm wide,
yellow in Melzer’s, smooth, with intracellular brownish
pigment, some with a very fine encrusting epiparietal
pigment. Pileitrama hyphae cylindrical, up to 12 lm wide,
mixed with numerous branched thromboplerous hyphae
with pale yellowish content in Melzer’s, otherwise
colourless, clamped at base. Clamp connections loop-like,
present at all septa.
Ecology: boreo-alpine, occurring in mountain to alpine
habitats of Central and Mediterranean Europe, as well as
North Europe. Mainly in litter of conifers, under Abies alba
and Picea abies on limestone or volcanic soils, also
reported from calcareous alpine zone.
Specimens examined:ITALY: Abruzzo, L’Aquila,
Campo Imperatore, Fonte Vetica, under Picea abies, leg.
G. Consiglio & M. Maletti, 03-X-2015, AMB 18222/GC
15186. Ibidem. AMB 18223/GC 15187. Trentino, Passo di
Redebus (TN), 1450 m a.s.l., under Picea abies, leg.
A. Tatti, 19-IX-2016, TO AV190916. FINLAND: Keski-
Pohjanmaa, Vimpeli, Kotakangas, in abandoned limestone
quarry, in grassy-mossy thicket mixed with Picea abies,
Betula sp., Salix sp., Populus sp., Sorbus sp., leg. M.-L.
Heinonen, P. Heinonen, 25-IX-2003, TUR 165285. Varsi-
nais-Suomi, Pernio
¨, Lupaja, Alhonma
¨ki, W slope, fairly
rich forest with mainly Picea abies, leg. J. Vauras, 01-X-
2004, TUR 170200. Varsinais-Suomi, Parainen, Lemlaxo
¨n,
Brattna
¨s, ca. 4 km SE of the limestone processing factories,
rather moist mossy forest of mainly Picea abies and Pinus
sylvestris, leg. J. Vauras, 07-X-1991, TUR-A-140440.
FRANCE: Haute-Loire, Cayres, Lac du Bouchet, volcanic
soil, under Abies alba and Picea abies, with some Fagus,
1140 m a.s.l., leg. D. Borgarino, 2003, D. Borgarino
031048/LIP 0401380. Ibidem, leg. D. Borgarino, G. Cla-
vel, J.-M. Moingeon, 02-X-2014, P. Roux 5622/D. Bor-
garino 141100/LIP 0401381. NORWAY: Buskerud, Hole,
Vik, in coniferous forest on calcareous ground, leg.
G. Gulden, 15-X-1967, Gulden 679/67, O-82070. Bus-
kerud, Ringerike, slightly west of Gullerud Nature Reserve,
rich coniferous forest on calcareous ground, leg.
G. Gulden, 09-X-2006, Gulden 307/06, O-74584. Bus-
kerud, Royken, Høvik, leg. G. Gulden, 29-IX-1963,
O-82069. Oppland, Gran, Jøvika, in mossy coniferous
forest with Picea abies on limestone, on steep slope, leg.
T. E. Brandrud, B. Dima, 14-IX-2016, DB 6191.
Comments:Clitopaxillus fibulatus is here proposed to
accommodate the collections formerly identified as C.
alexandri but with clamp connections present in all tissues
of the basidiomes (and not only in hymenophoral tissues
and mycelium as in C. alexandri), the presence of hymenial
cystidia, and occurring in alpine or boreal habitats, as first
suggested by Moreau (2009). Kuyper (1995) informally
proposed the name ‘C. subalexandri’ for specimens with
smaller spores (4.0–5.0 93.0–3.5 lm), and scarce clamp
connections in the pileipellis and hymenophoral trama, but
still some of them present at the base of basidia. However,
these features do not match any of the specimens studied
by Moreau (2009) or the present work. The only sequence
of ‘C. alexandri’ in GenBank (JF907816, Osmundson
et al. 2013) seems to match the concept of C. fibulatus
rather than the true C. alexandri. It was obtained from
collection MCVE 5953, found by Emanuele Campo at S.
Cassiano in Badia, close to Italian Alps, at 1650 m a.s.l.,
16-VIII-1994. In UNITE database, sequence UDB015076
(TU 106015) found by Vello Liiv at Estonia matches also
116 Fungal Diversity (2018) 90:109–133
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Table 1 Comparison of the key characters of genera of the Pseudoclitocybaceae treated in this study
Pogonoloma Musumecia Pseudoclitocybe Clitopaxillus Harmajaea
Habit Tricholomatoid Clitocyboid Clitocyboid Clitocyboid Clitocyboid
Stipe Rooting Aggutinating Aggutinating Aggutinating Aggutinating
Pileus umbonate to flat umbilicate umbilicate depressed depressed
Lamellae Emarginate Strongly decurrent Moderately decurrent Moderately decurrent Adnate to slightly decurrent
Spore amyloidity ??/0 ?± ±
Spore size 5–6.5 93.5–4.2 lm 5.5–10.0 93.5–5 lm 6.5–10.5 94–7 lm 4.5–6.5 93.5–4.5 lm 4.5–6 93.2–3.8 lm
Basidia 26–32 95–7 lm 28–45 93.5–8 lm 22–52 95–8.5 lm 20–33 95–8 lm 15–34 95–7 lm
Pileitrama Sarcodimitic Homomorphic Homomorphic Homomorphic Homomorphic
Clamps All septa ?/0 Mycelium Mycelium, hymenium Mycelium
Smell Aromatic Herbaceous
Cystidia Marginal hairs ?/0 None None None
Pileipellis Trichocutis Ixocutis Ixocutis Cutis Trichocutis
Pigments Intraparietal ?intracellular Intraparietal ?incrusting Intraparietal ?intracellular Intraparietal ?intracellular
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118 Fungal Diversity (2018) 90:109–133
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the concept of C. fibulatus, in agreement with the alpine
and boreal distribution of this species. Sequence
KY084307 (Zhou & Guo, unpublished) is significantly
related to those of Clitopaxillus, but probably represents an
undescribed taxon from the Guancen Mountains (Shanxi,
China).
Harmajaea Dima, P. Alvarado & Kekki,gen. nov.
Mycobank MB 823306 (Figs. 3d–i, 4c–f)
Etymology: We want to dedicate this new genus to Dr.
Harri Harmaja because he was the first who reported a
species of this genus from Europe, and also because of his
huge contribution to the knowledge of clitocyboid fungi.
Diagnosis: large fleshy species with convex pileus, dry,
smooth or subscaly surface at centre, pale yellowish, pale
beige to brown or dark brown, not hygrophanous; spores
small, 4.5–6 93–3.8 lm, ovoid to cylindrical, faintly
amyloid, not cyanophilous. Hymenophoral trama regular.
Thromboplerous hyphae abundant in subpellis and hyme-
nial trama. Clamp connections absent in basidiome, scat-
tered in mycelium. Smell and taste none. Saprobic, on thick
forest litter. Northern Hemisphere, present in North
America and North Europe.
Type species: Harmajaea harperi (Murrill) Dima & P.
Alvarado
Comments: This new genus Harmajaea differs from
Clitopaxillus because it completely lacks clamp connec-
tions or ’’false’’ clamps, has a slenderer stipe, and a more
depressed pileus. Clitocybe harperi was first reported from
Europe by Harmaja (1969), who also transferred it to
Rhodocybe (Harmaja 1978,1979) on the account of wrin-
kled spores under SEM and lack of clamps. The present
results show that collections identified as C. harperi from
North America and Scandinavia cluster on a single clade
sister to Pseudoclitocybe,Clitopaxillus and Musumecia.
Harmajaea is characterized by a complete absence of
clamps in the basidiome (present in the mycelium of H.
guldeniae and H. wellsiae), and a spectacular abundance of
yellowish, frequently branched thromboplerous hyphae in
the hymenophore and subpellis. Macroscopically, some
Harmajaea species recall Atractosporocybe because of its
pale colors and dry cap, grooved pileus at margin, and
faintly decurrent gills, but the latter has fusoid spores, more
greyish tinges and a strong fishy smell (Gulden 2006).
Clitopaxillus can look similar, but has deeply decurrent,
‘paxilloid’’ lamellae. Three distinct genetic lineages of
Harmajaea were found in the present work, two of them
are identified with the existing species C. harperi and C.
wellsii, and a third one is described here as a new taxon.
Harmajaea harperi (Murrill) Dima & P. Alvarado,
comb. nov.
Mycobank MB 823307 (Figs. 3g–i, 4c–e)
Basionym: Clitocybe harperi Murrill, Mycologia 5(4):
209 (1913)
:Rhodocybe harperi (Murrill) Harmaja, Karstenia
18(1): 30 (1978)
Description: Pileus 5–11 cm, slightly depressed and
presenting a central umbo with age, margin enrolled,
smooth or minutely scaly, dry, whitish or grayish in color,
brown or pale brown at the center. Lamellae shortly
decurrent, crowded, thin, pale brown or gray to whitish.
Stipe 4.5–8 91.3–2.2 cm, solid, cylindrical, concolorous
with the pileus. Context whitish to brownish. Spores (4.5–)
5.0–6.0 (–7.0) 9(2.5–) 3.0–3.7 lm (on average
5.3 93.5 lm), Q = 1.40–1.65 (Q
m
= 1.53), V
m
=
34 lm
3
, ellipsoid in front view, somewhat obovoid or
amygdaliform in side view, smooth, spore wall slightly
amyloid after a few minutes, not cyanophilous, not col-
lapsing and not adhering in tetrads. Basidia
15–23 93.8–5.8 lm, 4-spored, cylindro-clavate, with
sterigmata 4 lm long, without carminophilic/siderophilous
granulation, apical portion slightly amyloid. Cheilocystidia
26 98lm, cylindrical, scattered, with apical protrusions
like ‘‘stag’s antlers’’. Pleurocystidia absent. Subhymenium
ramose, arbuscular, 15 lm thick, hyphae shortly branched
3.0–3.5 lm wide. Hymenophoral trama regular, made of
broad cylindrical to inflate hyphae 5–16 lm wide, and of
thromboplerous hyphae 5–7 lm wide, with yellow content,
especially frequent towards in the otherwise hardly dif-
ferentiated hymenopodium, as well as towards edge.
Pileipellis a dry trichocutis of radially arranged, inflate
hyphae 5–12 lm wide, with intracellular yellow pigment
forming minute granulations, mixed with slender hyphae
2.5–3.0 lm wide, scattered, narrowed at septa, with
incrusted wall. Subpellis thick, characterized by an abun-
dance of thromboplerous hyphae with yellowish content in
Melzer’s reagent, mixed with regular cylindrical thin-
walled hyphae 3–8 lm wide. Pileitrama homomorphous,
made of mostly parallel hyphae 4.0–6.5 lm wide, with
walls 0.3–0.8 lm thick, smooth, mixed with thrombo-
pleurous hyphae 5–9 lm wide, branching and
bFig. 3 aPogonoloma macrorhizum (AMB 18232, photo: M. Bar-
bieri). bClitopaxillus alexandri (LIP 0401301, photo: D. Borgarino).
cClitopaxillus fibulatus (TU 106015, photo: V. Liiv). dHarmajaea
guldeniae (H 6067444). eHarmajaea guldeniae (H 6067455).
fHarmajaea wellsiae (TUR 205933). gHarmajaea harperi (CMMF
014712, photo: G. Poulet). hHarmajaea harperi (LIP 0401361,
photo: R. Pastorino). i. Harmajaea harperi (H 6067456). jPseudo-
clitocybe cyathiformis I (LIP 0901300, photo: P. Clowez). kPseudo-
clitocybe cyathiformis I (AMB 18227). lPseudoclitocybe
cyathiformis I (TU 106216, photo: V. Liiv). mPseudoclitocybe
cyathiformis II (TU 118376, photo: V. Liiv). nPseudoclitocybe
cyathiformis II (AMB 18228). oPseudoclitocybe cyathiformis II
(PAM 14112110b). pPseudoclitocybe obbata (LIP 0401358).
qPseudoclitocybe obbata (AMB 18231). rPseudoclitocybe obbata
(AMB 18229)
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anastomosing, with homogeneous yellowish content,
especially abundant towards subpellis. Stipitipellis a
caulohymenium. Clamp connections absent, even at the
base of basidia and mycelium.
Ecology: widespread in North America (western USA to
eastern Canada) and Northern Europe. Under conifers such
as Pseudotsuga,Pinus sylvestris and Picea abies.
Specimens examined:CANADA: Que
´bec, Shipshaw,
under conifers, leg. G. Gue
´rin, 27-XI-1986, Gue
´rin
1591/CMMF 014712. FINLAND: Etela
¨-Savo, Savonlinna,
Hevonmaa, a gorge W of pond Silma
¨lammi, lush vegeta-
tion with Betula,Populus,Salix caprea,Abies, leg.
S. Huhtinen, 17-IX-2003, TUR164187. Pera
¨-Pohjanmaa,
Keminmaa, Kallinkangas, grassy calcareous spruce forest,
leg. T. Kekki, 18-IX-2016, Kekki 2722/H 6067456.
Varsinais-Suomi, Pernio
¨, Arpalahti, Kaapinma
¨ki, along a
small brook, in a rocky, virgin forest site with dominant
trees of Alnus,Betula,Sorbus,Juniperus,Ribes alpinum,
and few young Quercus, under dense spruces in deep litter
with Oxalis but without much moss coverage, leg. M.-L.
Heinonen, P. Heinonen, 08-XI-2003, TUR 173042.
NORWAY: Oppland, Etnedal, Kluftøygard, in calcareous
Picea abies forest, leg. T. E. Brandrud, B. Dima, 21-VIII-
2017, DB 6315. USA: California, Sonoma County, Anna-
del State Park, mixed woods, Pseudotsuga menziesii, bay
laurel and live oak, leg. R. Pastorino, 20-I-2015, LIP
0401361. Washington, Pierce Co., Penrose State Park, leg.
H. Koonz, 23-XI-2001, WTU-F-006299, PBM 2677.
Comments: This species can be easily differentiated
because of its habit, ecology and clampless hyphae.
Weakly amyloid spores were observed on the collections
studied here as well as TENN 061314 (USA, North Car-
olina, Sa
´nchez-Garcı
´a pers. comm.), while spores of C.
harperi are usually described as inamyloid, even by such
reliable observers as Harmaja (1979) or Bigelow (1982).
This could suggest that this feature varies within the same
taxon, depending on age, environment, strain, or most
probably, on the specific protocol employed. Clitocybe
griseifolia Murrill was proposed in the same work as C.
harperi (Murrill 1913) from Seattle (USA), and was sep-
arated from C. harperi because of its broad lamellae, white
stipe, and fragrant odor different from the crowded
lamellae, concolorous stipe, and odorless basidiome of C.
harperi (Bigelow 1965,1982). However, some authors
(Harmaja 1979) considered C. griseifolia a synonym of C.
harperi because of their very similar macro- and micro-
scopical features, as well as identical chemical reactions of
the types to Melzer’s reagent (inamyloid), cotton blue
(cyanophobic, but weakly cyanophilic in spore and basidia
walls) and acetocarmine (carminophobic spore and basidia
walls, carminophilic spore nuclei) (Harmaja 1979). Our
collections of C. harperi have medium-distanced lamellae,
a concolorous stipe, and odorless basidiomes, so they do
not match C. griseifolia. A single report from France of H.
harperi by Bon (1997), corresponding to coll. 741006 in
herb. Bon (LIP), was checked under the microscope and
revealed clamps in hymenophoral tissues, so it is here re-
interpreted as C. alexandri. Finally, some confusion might
have existed because of the name Lepista harperi (Murrill)
Singer, originally described by Murrill (1913)asMe-
lanoleuca harperi, and later combined to Lepista by Singer
(1951) on account of its verrucose spores. When Bigelow
(1982) subsumed Lepista within Clitocybe, he noticed the
existence of Clitocybe harperi Murrill, and renamed the
first species as Clitocybe brunneocephala H.E. Bigelow.
Harmajaea guldeniae Dima, P.-A. Moreau, P. Alvarado
& Kekki sp. nov.
MycoBank MB 823308 (Figs. 3d, e, 4f)
=Clitocybe harperi s. Harmaja (1969), s. Gulden (2006)
Etymology: We are glad to dedicate the new taxon to Dr.
Gro Gulden on account of her work on this species and
many others in Clitocybe.
Diagnosis: clitocyboid basidiome, depressed, with an
umbo, yellowish-brown or beige, lamellae decurrent, ovoid
spores 4.5–5.0 lm long, faintly amyloid. Differs from H.
harperi because of its brownish pileus, more decurrent
gills, longer basidia, clamped mycelium and, by now,
exclusively European distribution under conifers.
Type collection: FINLAND:Pera
¨-Pohjanmaa, Tervola,
Raema
¨ki, calcareous grassy spruce forest, leg. T. Kekki,
8-IX-2016, Kekki 2580/H 6067455 (holotype).
Description: Pileus 5–11 cm diam., soon depressed with
a persistent small central umbo, rather thin-fleshed; surface
matt, dry, smooth to faintly scurfy especially at centre, not
hygrophanous, yellowish-brown to beige or leather-col-
ored, towards centre with darker, velvet brown patches;
margin persistently enrolled, grooved. Lamellae decurrent,
crowded, with many lamellulae, narrow, almost white to
pale greyish; edge darkening to brown with age. Stipe
4.5–8.0 (–11) 91.3–2.2 cm, cylindrical to moderately
clavate, solid; surface fibrillose, concolorous with the
pileus; mycelium white, abundant, tomentose, aggregating
litter debris. Context white, becoming somewhat brownish.
Smell and taste indistinct or slightly fungoid. Spores
4.3–5.1 93.0–3.8 lm (on average 4.7 93.3 lm),
bFig. 4 a,bClitopaxillus fibulatus (AMB 18222) acystidia. bClamp-
connection detail. ceHarmajaea harperi (TUR 164187) cepicutic-
ular hyphae with vacuolar pigments. dWeak amyloid reaction of
spores in Melzer. eSpores. fHarmajaea guldeniae (TUR 201099)
spores. gClitopaxillus fibulatus (AMB 18224) spores. hClitopaxillus
fibulatus (AMB 18222) clamped hyphae. iMusumecia sardoa (GC
04275) spores in Melzer, amyloid reaction of apiculus. Bars:
A=10lm, B = 3 lm, C–D = 10 lm, E–G = 5 lm, H = 10 lm,
I=5lm
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Q = 1.29–1.57 (Q
m
= 1.43), V
m
=27lm
3
, smooth, faintly
amyloid spore wall, not cyanophilic, broadly ellipsoid to
oblong in front view, sometimes larmiform, with protrud-
ing hilar appendix about 0.8 lm, not aggregated in tetrads
and not collapsing. Basidia 19–34 95.0–7.5 lm,
4-spored, narrowly clavate, with sterigmata 3.5 lm long,
apical portion slightly amyloid. Cystidia not observed.
Subhymenium ramose, made of short cylindrical hyphae
2–3 lm wide. Hymenophoral trama with a differentiated
hymenopodium 15–20 lm thick, made of parallel cylin-
drical hyphae 3–7 lm wide, and a mediostratum made of
broad cylindrical to slightly inflate hyphae 5–16 lm wide.
Pileipellis a trichocutis made of fasciculate slender hyphae
with narrowed terminal elements 40–70 92.5–4 lm,
especially developed towards margin, slightly becoming
gelatinized and collapsing with age from the centre.
Subpellis made of parallel, cylindrical hyphae 3.5–9.0 lm
wide, smooth, with pale brown intraparietal pigment.
Pileitrama made of parallel hyphae 4–12 lm wide, with
numerous colorless intracellular globules measuring
3.0–5.5 lm diam., and abundant thromboplerous hyphae
5–10 lm wide, often branched, uniformly yellowish in
KOH. Stipitipellis a caulohymenium. Mycelium made of
cylindrical hyphae 2.5–9 lm wide, mostly with thickened
wall (0.3–0.5 lm thick), some with yellowish granular
content. Clamp connections absent from all septa in the
basidiome, but present in basal mycelium (about 10% of
septa clamped).
Specimens examined:FINLAND: Kainuu, Paltamo,
Antinma
¨ki, mixed forest of Picea abies and deciduous
trees, leg T. Kekki, 9-IX-2016, Kekki 2593/H 6067433.
Kainuu, Paltamo, Melalahti, in calcareous spruce forest,
leg T. Kekki, 9-IX-2016, Kekki 2596/H 6067444. Pohjois-
Pohjanmaa, Tervola, E of Raema
¨ki, in spruce forest, leg.
T. Kekki, 02-IX-2012, TUR 201099. Pohjois-Savo, Var-
kaus, Itkonharju, in rich mixed forest of Picea abies,Pinus
sylvestris and Betula, leg. T. Kekki, 31-VIII-2014, Kekki
1505, H 6051797. Pohjois-Savo, Varkaus, Itkonharju, in
rich spruce forest, leg. T. Kekki, 17-IX-2016, Kekki
2700/H 6067432. NORWAY: Buskerud, Hole, Vik, in a
spruce forest on Cambrio-Silurian calcareous rocks, leg.
G. Gulden, 22-X-1967, Gulden 731/67, O-64624. Oppland,
Gran, Askimlandet, in calcareous Picea abies forest, leg.
T. E. Brandrud, B. Dima, 11-IX-2017, DB 6456. Ringerike,
Gullerud, near the lake, leg. G. Gulden, 25-IX-2004, Gul-
den GG150/04, O-74110.
Ecology: known only from Picea abies forests in North
Europe.
Comments: This species fits the concept of Clitocybe
harperi as proposed by Harmaja (1969) and Gulden (2006).
However, it is morphologically, phylogenetically and bio-
geographically distinct from the original concept of C.
harperi, because of its brownish pileus, decurrent gills,
longer basidia, clamped mycelium and, by now, exclu-
sively European distribution under conifers. A very similar
taxon, C. wellsiae H.E. Bigelow (Bigelow 1982), was
found in spruce woods of Alaska (USA), and has a
brownish pileus, adnexed to decurrent lamellae, and similar
microscopy. However, genetics show that H. guldeniae is a
different taxon. Harmaja’s nom. prov. ‘Clitocybe sub-
harperi’ (Harmaja 1979), a fungus found in calcareous
areas of Finland with a slightly pruinose pileus darker than
that of C. harperi, and a spore print with reddish tinges,
was considered by Bigelow (1982) a putative synonym of
C. wellsiae, but the reddish tinges in the spore print are
different from those of C. guldeniae and its identity
remains to be precised.
Harmajaea wellsiae (H.E. Bigelow) P. Alvarado, Kekki
& P.-A. Moreau comb. nov.
MycoBank MB 823309 (Fig. 3f)
:Clitocybe wellsiae H.E. Bigelow, Beih. Nova Hed-
wigia 72: 64 (1982) (as ‘Clitocybe wellsii H.E. Bigelow’’)
Description: Pileus 8–16 cm diam., slightly depressed,
surface mat, dry, smooth to faintly tomentose especially at
centre, not hygrophanous, pale-brown to cinnamon brown,
darker towards centre; margin persistently enrolled, whit-
ish. Lamellae adnate-shortly decurrent, crowded, with many
lamellulae, narrow, almost white; edge darkening to brown
with drying. Stipe 6–9 91.5–2 cm, cylindrical, solid; sur-
face fibrillose, lighter than the pileus; mycelium white,
abundant, tomentose, aggregating litter debris, with some
rhizoids. Context white; smell and taste indistinct. Spores
(3.7–) 4.3–5.0–5.9 (–6.9) 9(2.0–) 2.5–3.0–3.5 lm,
Q = 1.35–1.67–2.05, slightly but distinctly amyloid,
larmiform to cylindro-allantoid before maturity, at maturity
cylindrical to narrowly ellipsoid with rounded base; wall
slightly thickened, smooth; content microguttulate before
maturity, hyaline when mature. Basidia 18–26 94–7 lm,
4-spored, cylindro-clavate at maturity, filled with colourless
droplets when mature. Cystidia not observed. Subhyme-
nium ramose, 10–12 lm thick, made of shortly cylindrical
hyphae with guttulate content. Hymenophoral trama with a
differentiated hymenopodium made of parallel to slightly
divergent cylindrical hyphae 2.5–6.0 lm wide, frequently
branched, and a mediostratum of subregular structure with
broad cylindrical hyphae 4–10 lm wide, often inflated
before septa, colourless, smooth, with intracellular colour-
less droplets, with sparsed thromboplerous hyphae 5–6 lm
wide with pale yellow content. Pileipellis a faintly gela-
tinized trichocutis 60–100 lm thick, made of cylindrical
hyphae 3.5–11.0 lm wide, some with yellowish homoge-
neous content, with frequent clavate terminations more or
less fasciculate towards margin, adpressed and confusedly
intervowen elsewhere; wall slightly thickened, with min-
utely incrusting epiparietal pigment. Subpellis 40–70 lm
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thick, not gelatinized, made of parallel, broad hyphae
4–7 lm wide, abundantly guttulate. Stipitipellis mostly
covered by a fertile caulohymenium. Stipititrama made of
parallel, cylindrical hyphae 7–15 lm wide, moderately
thick-walled, smooth, colourless; no thromboplerous
hyphae observed. Mycelium made of slender cylindrical
hyphae 2.5–5.0 lm wide, colourless, smooth wall up to
0.3 lm thick, frequently with attenuated apices, sometimes
(typus) mixed with coralloid elements and more yellowish
and thick-walled hyphae and cylindro-clavate cystidioid
elements with guttulate content, 5–6 lm wide at apex.
Clamps loop-like, scattered in mycelium, mostly on thick-
walled hyphae, not observed anywhere on the basidiome.
Specimens examined:FINLAND: Kittila
¨n Lappi, Kolari,
A
¨ka
¨sjoensuu, leg. T. Kekki, calcareous forest of Picea and
Pinus, 03-IX-2016, Kekki 2523/TUR 205933. USA:
Alaska, Fairbanks North Star, Larson property, Yankovitch
Rd, Fairbanks, gregarious in deep moss in Picea sp. woods,
leg. V. Wells & P. Kempton, 24-VIII-1965, MICH 10217
(holotype). Alaska, Dalton Highway, Mile 229, with Picea
sp., Betula sp., Salix sp., Alnus sp., leg. G. A. Laursen,
18-VIII-1992, WTU-F-024810.
Ecology: known from boreal Picea sp. forests in Alaska
and northern Finland.
Comments: After studying the holotype collection of Cl-
itocybe wellsii (MICH 10218, Wells & Kempton 2506), and
producing ITS rDNA data from it, we here propose the new
combination H. wellsiae (the epithet is corrected from
‘‘ wellsii’’ t o ‘‘ wellsiae’ because the species was dedicated to
the late Virginia Wells, ICN Art. 60.12). The holotype
material studied was not completely mature and most spores
were still attached to basidia; their shape was remarkably
elongate to even subfusiform (roughly 5.8–7.0 9
3.0–3.2 lm), and their amyloid reaction was only distinct
towards the apiculus. Similar long spores were only found
rarely attached to basidia in the fully mature collection Kekki
2523 (TUR 205933). The holotype was also distinct from
Kekki 2523 because of the presence of well differentiated
cystidioid elements with yellow content in mycelium. Har-
majaea wellsiae is quite similar to H. guldeniae because of
its macro and microscopical features, but it is more robust,
has almost adnate lamellae and a boreal distribution in
America and Europe. Other clampless species of Clitocybe
from North America include Clitocybe griseifolia, found at
Seattle (USA), but this is most probably a synonym of H.
harperi, since both taxa share a similar grayish pileus, fruit in
autumn, and occur in similar habitats in California, Oregon
and Washington. ‘Clitocybe subharperi’ (nom. prov. in
Harmaja 1979), was also found in calcareous areas of Fin-
land, but had reddish tinges in its spore print.
Pseudoclitocybe (Singer) Singer Mycologia 48(5): 725
(1956) (Figs. 3j–r)
Basionym: Cantharellula subgen. Pseudoclitocybe
Singer, Annls mycol. 41(1/3): 64 (1943)
Description: Pileus 2–12 cm, depressed to umbilicate,
hygrophanous, striate or not, slightly gelatinized, smooth to
pruinose at margin. Lamellae: adnate to deeply decurrent,
crowded, thin, whitish to gray. Stipe 4.5–8 91.3–2.2 cm,
fistulose, cylindrical to compressed at maturity, concolor-
ous with the pileus, usually with a white zone at apex;
mycelium usually abundant, patch-like, without rhi-
zomorphs. Context whitish to grey when moist. Smell
herbaceous. Spores globose to ellipsoid, smooth, distinctly
amyloid, acyanophilic, with hyaline content. Basidia
4-spored, without carminophilic/siderophilous granulation.
Cystidia absent. Subhymenium branching, prostrate, easily
dissociated. Hymenophoral trama subregular to slightly
divergent, cylindrical hyphae with elements 4–6 lm wide.
Pileipellis a radially arranged ixocutis, sparsely to densely
diverticulate. Clamp connections loop-like, present in
mycelium in all species, absent or very rare elsewhere,
absent at the base of basidia. Saprobe, terricolous, ligni-
colous to coprophilous. Temperate areas, Northern and
Southern Hemispheres.
Comments: At least four distinct genetic lineages were
found within genus Pseudoclitocybe in the ITS rDNA
analysis (Fig. 2): one of them found in Europe, North
America and Asia (Pseudoclitocybe cyathiformis), one
known only from Europe (Pseudoclitocybe obbata),
another one found in North America (KF291250 and LIP
0401355, maybe Pseudoclitocybe oregonensis (Murrill)
Singer?), and last a single sequence coming from New
Zealand (HQ533021). Two cryptic lineages within P.
cyathiformis (I and II) were sometimes significantly sup-
ported, although frequently merged together in the analyses
because of the presence of apparently intermediate
sequences (KP453709, KR673477).
The intracellular globules characteristic of most Pseu-
doclitocybaceae are only frequent in the stipititrama of
Pseudoclitocybe, and clamp connections have only been
detected on mycelial hyphae (except for a few on stipi-
tipellis of P. cyathiformis Lineage II). Subpellis is hardly
differentiated in P. cyathiformis Lineage II, perceptible in
P. cyathiformis Lineage I, and absent in P. obbata. The
development of the hymenopodium (always with slender,
anastomosing hyphae with divergent structure) follows the
same pattern. Mediostratum is rather regular excepting in
P. obbata where it looks more entangled. Suprapellis
structures are rather specific, an ixotrichocutis with few,
unbranched erected elements in P. cyathiformis Lineage I,
or rich in terminations either simple and cylindro-clavate
(P. obbata) or versiform (P. cyathiformis Lineage II).
Incrusting pigment is abundant in P. obbata and present in
P. cyathiformis Lineage I, nearly absent in P. cyathiformis
Lineage II. All species have parietal pigmentation in
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pileipellis and/or subpellis, and a yellow intracellular pig-
ment in some hyphae of pileipellis. Vascular (thrombo-
plerous) hyphae with deep yellow–brown content have
been seen only in P. obbata, mostly in the hypophyllum
region.
Pseudoclitocybe cyathiformis (Bull.) Singer Mycologia
48(5): 725 (1956) (Figs. 3j–o)
Basionym: Agaricus cyathiformis Bull., Herb. Fr. (Paris)
12: tab. 575 (1792), sanctioned by Fries, Syst. Mycol. 1:
173 (1821)
:Clitocybe cyathiformis (Bull.) P. Kumm., Fu
¨hr. Pilzk.
(Zerbst): 120 (1871)
:Omphalia cyathiformis (Bull.) Que
´l., Me
´m. Soc.
E
´mul. Montbe
´liard, Se
´r. 2 5: 129 (1872)
Description: Pileus 5–9.5 cm, a bit fleshy, first convex
with a central depression and papillate, soon strongly
depressed, funnel-shaped; margin enrolled then incurved
downwards, at last applanate, a bit grooved because of the
lamellae print and the thin flesh; surface smooth and opa-
que, with very fine fibrils, grey bistre, dark brown flushed
olive, fading to grey-brown, ochraceous brown on drying, a
bit hygrophanous. Lamellae adnate-decurrent, moderately
crowded, very broad, with numerous lamellulae; pale grey-
brown to brownish grey. Stipe 8–11 90.5–1.2 cm,
straight, cylindrical, a bit inflated toward the base, solid
then stuffed; surface tomentose-fibrillose, greyish brown,
paler than the pileus. Context thin, fragile, watery, greyish.
Smell and taste not distinctive. Spores (7.8–) 8.0–9
(–10.8) 95.2–6.0 lm, ovoid-ellipsoid with adnate base,
thin-walled, distinctly amyloid, smooth, not guttulate.
Basidia 4-spored, 22–34 97–8.5 lm, clavate-subcapitate
before maturity, microguttulate, unclamped. Cystidia not
observed; cystidioles sparse on lamella edge, arising from
subhymenium, cylindrical sinuose, sometimes forking on
old specimens. Subhymenium ramose, 12–20 lm thick.
Hymenophoral trama with a well-developed hymenopo-
dium, 40–50 lm thick, made of parallel slender hyphae
3.5–5.0 lm wide, straight, slightly thick-walled. Medios-
tratum subregular, well-developed, made of broad and
mostly short, cylindrical to inflate hyphae 7–16 lm wide,
smooth, moderately thick-walled. Pileipellis an ixocutis,
40–60 lm thick, made of mostly parallel hyphae 3–5 lm
wide, cylindrical, partly with microguttulate content, with
frequent obtuse terminations, superficial hyphae forming
short erected lateral, non-septate branches especially fre-
quent at margin and sometimes fasciculate, up to 40 lm
long; wall smooth to minutely incrusted. Subpellis weakly
differentiated, yellowish in KOH, 50–80 lm thick, mostly
made of parallel welded hyphae mixed with broader, sin-
uose hyphae, 3–9 lm wide, frequently forked and anasto-
mosed, wall thick, yellowish, punctuate to minutely zebra-
striped. Pileitrama colourless, made of entangled,
cylindrical hyphae 5–12 lm wide, frequently branched and
anastomosed, wall faintly thickened and smooth; vascular
hyphae absent. Stipitipellis a trichocutis of mostly prostrate
cylindrical hyphae 3.5–5.0 lm wide, with frequent pros-
trate to sparsely erected, rarely fasciculate hairs
40–90 94.5–10 lm, the largest arising from deeper
hyphae. Stipititrama made of parallel, cylindrical or inflate
hyphae 7–25 lm wide, mostly with intracellular globules
2–5 lm diam. Mycelial hyphae slender, 3.0–4.5 lm wide,
cylindrical, slightly thick-walled (0.3 lm), smooth, spar-
sely branched, usually with one lateral ramifications per
hypha close to septa; clamps present but not at all septa,
loop-like. Birefringent crystals rare. Cystidioid elements
not seen. Clamp connections present in the mycelium.
Specimens examined:
Lineage I)FRANCE: Oise, Carlepont, Fore
ˆt domaniale de
Ourscamps, under Picea abies plantation, 64 m asl, leg.
P. Clowez, 23-XI-2016, LIP 0901300. Savoie, Beaufort,
Are
`ches, les Envers, at the bottom of a recently manured
road side under Picea abies, 25-VIII-2014, leg. P.-A.
Moreau, PAM14102509/LIP 0401359. ITALY: Emilia
Romagna, Bologna, San Benedetto Val di Sambro, Val
Serena, brodleaved and pine trees, leg. G. Consiglio, G.
Bordoni, 24-XI-2000, AMB 18225/GC 00220. Emilia-
Romagna, Vidiciatico (Bologna), Rio Ri, under Fagus
sylvatica and Abies alba, leg. G. Consiglio, G. Spisni,
21-IX-2016, AMB 18226/GC 16021. Lucca, Fosciandora,
Prade Garfagnine, under Castanea sativa, leg. G. Con-
siglio, P. Petrucci, 4-X-1996, AMB 18227/GC 96168.
Lineage II)FRANCE: Corse-du-Sud, Bastelica, near
Porticcio, pont de Zippitoli, Mediterranean oak forest, in a
decaying branch of Quercus ilex, leg. Socie
´te
´Mycologique
d’Ajaccio, 21-XI-2014, PAM14112110b/LIP 0401360.
ITALY: Lucca, Castiglione di Garfagnana, Passo delle
Radici, under Castanea sativa, leg. G. Consiglio, D.
Antonini, M. Antonini, 19-X-2000, AMB 18228/GC
00060. Sardinia, Carana, Diga del Liscia, under Alnus, leg.
M. Contu, 30-XII-2012, TO HG123012A.
Ecology: forming small groups, found in broadleaved
and conifer forests, in open spaces and pathways, in tem-
perate areas of Europe, America, and Asia. Summer to late
autumn or winter.
Comments: The original concept of the type species is
here interpreted as a dark-colored wood-associated taxon
present in northern Europe as well as temperate forests of
Mediterranean countries. Spore size rarely exceeds 10 lm,
in agreement with Saccardo (1887), who noticed a conflict
with spore measurements by Britzelmayr (up to
10–12 95.0 lm). Pseudoclitocybe beschidica (Singer &
Kuthan 1980) was separated from P. cyathiformis because
of its shorter spores not exceeding 8.5 lm long, but the
present observations suggest that this would be an average
124 Fungal Diversity (2018) 90:109–133
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value rather than an upper limit. Two distinct genetic lin-
eages were found among samples identified as P. cyathi-
formis, but only slight differences in their morphology
were detected. The description above refers to the appar-
ently most frequent one, Lineage I. Lineage II differs
mainly because of a less developed hymenopodium
20–25 lm (instead of 40–50 lm), and a pileipellis
70–100 lm thick (instead of 40–60 lm) made of hyphae
6.5–9.0 lm wide (instead of 3–5 lm). Both lineages occur
in northern Europe, but no samples of Lineage I were found
up to now in Mediterranean lowland habitats. The appli-
cation of the name P. expallens to any of these lineages is
controversial, since Fries used ambiguous characters such
as size and color to separate it from P. cyathiformis. In the
present work we observed great variations in these features
among specimens studied, and so avoided employing the
name P. expallens to any of the genetic lineages of P.
cyathiformis until some evidence for this decision is found.
Pseudoclitocybe obbata (Fr.) Singer Sydowia 15(1-6): 52
(1962) [1961] (Figs. 3p–r)
Basionym: Agaricus obbatus Fr., Epicr. syst. mycol.
(Upsaliae): 74 (1838) [1836–1838]
:Clitocybe obbata (Fr.) Que
´l., Me
´m. Soc. E
´mul.
Montbe
´liard, Se
´r. 2 5: 90 (1872)
:Cantharellula obbata (Fr.) Bousset, Bull. trimest.
Soc. mycol. Fr. 55: 123 (1939)
:‘‘Omphalia obbata’’ (Fr.) Ku
¨hner & Romagn., Fl.
Analyt. Champ. Supe
´r. (Paris): 129 (1953) (nom. inval., no
full and direct reference to the replaced synonym, ICN Art.
41.5)
Description: Pileus 1.5–6.0 cm diam., early flattened
then broadly depressed at centre, without forming a narrow
depression; surface greasy, entirely white-pruinose and
remaining so if not washed by rain, on blackish, dark
brown to reddish brown ground when fresh, striate only
with age, hygrophanous, quickly drying from centre, when
dry uniformly pale ochraceous; margin a long time enrol-
led, white, pruinose. Lamellae 24–38 reaching the stipe,
two series of lamellulae, adnexed, arcuate, then shortly
decurrent when expanded, ash-grey and remaining so,
rarely paler, with a coppery shade while ageing; edge
smooth, concolorous, becoming rusty-brown with age.
Stipe 4–9 90.4–0.8 cm, hollow, cylindrical, often com-
pressed, entirely covered by a dense white fibrillum, early
removed, on ash-grey to later grey-brown ground. Context
grey when moist, pale ochraceous when dry. Smell
herbaceous, weak. Spores (6.5–) 8.0–8.5 (–9.1) 9
5.0–5.2 lm, broadly ellipsoid to subglobose, thick-walled,
distinctly amyloid, smooth, micro-guttulate at maturity.
Basidia 4-spored, 35–52 98.0–11.5 lm, clavate before
maturity, abundantly guttulate, unclamped. Cystidia not
observed. Subhymenium ramose, 25–30 lm thick.
Hymenophoral trama with a well-developed hymenopo-
dium, 30–50 lm thick, made of parallel slender hyphae
2.0–3.5 lm wide, smooth, anastomosing. Mediostratum
subregular to somewhat interwoven, well-developed, made
of cylindrical, short and often sinuous hyphae 4–13 lm
wide, smooth to minutely punctuate. Pileipellis a tricho-
cutis 50–70 lm thick, slightly gelatinized, made of cylin-
drical hyphae 3.5–6.0 lm wide, with abundant, cylindrical
to clavate terminations; wall distinctly incrusted, minutely
on the broadest hyphae, distinctly and scale-like on slen-
derer ones. Subpellis not differentiated. Pileitrama with
yellowish and colourless zones, made of parallel and
mostly cylindrical, 3–8 lm thick hyphae, partly with yel-
low incrusted wall, with frequent thromboplerous hyphae
especially in hypophyllum with deep yellow content.
Stipitipellis a cutis of prostrate cylindrical hyphae
3.0–5.5 lm wide, moderately thick-walled, nearly smooth,
with sparse to fasciculate unseptate hairs. Stipititrama
made of parallel, cylindrical or inflate hyphae 5–26 lm
wide, without intracellular globules; vascular hyphae rare
with yellow–brown content. Mycelium whitish, made of
cylindrical, abundantly ramose hyphae 3.5–6.0 lm wide,
with smooth- to slight punctuate wall, and with numerous
terminal articles with obtuse apex, unbranching and with
microguttulate content. Calcium oxalate crystals not seen.
Clamps only present on mycelial hyphae, loop-like.
Specimens examined:FRANCE: Ain, Vanchy, Car-
rie
`res de Vanchy, dry grassland, leg. R. Fillion, P.-A.
Moreau, 17-XII-2000, PAM00121703/LIP 0401357. Nord,
Liessies, mont de Baives, mesophilic calcareous grassland,
leg. C. Le
´curu, P.-A. Moreau, 6-XI-2005, PAM05110604/
LIP 0401358. ITALY: Bologna, Grizzana Morandi,
Tudiano, under Castanea sativa, leg. G. Consiglio, R.
Trimarco, 16-XI-1997, AMB 18229/GC 97181. Bologna,
Pontecchio Marconi, Villa Grifone, broadleaved and pine
trees, leg. G. Consiglio, R. Trimarco, 01-XII-1998, AMB
18230/GC 98186. Bologna, Sasso Marconi, Prati di Mug-
nano, under Quercus pubescens, leg. G. Consiglio, R.
Trimarco, 6-XII-1998, AMB 18231/GC 98189. SPAIN:La
Rioja, Lardero, La Barranca, arid basic steep soil, among
moss with Quercus coccifera,Rosmarinus officinalis and
Cistus albidus near a Pinus halepensis plantation, leg.
Carlos M. Pe
´rez del Amo, 30-I-2016, CMP1558/AH
46369.
Ecology: found in grasslands, as well as temperate and
Mediterranean broadleaved or conifer forests. Autumn and
early winter.
Comments: Knudsen and Vesterholt (2008) suggested
that P. expallens could be an earlier synonym of both P.
atra and P. obbata, but the lack of details in Fries original
protologues of A. expallens and A. obbatus provides too
weak support for a definitive decision. Basidiome size,
colour and striated pileus seem not reliable features to
Fungal Diversity (2018) 90:109–133 125
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discriminate between the observed genetic clades. The
lineage identified here with P. obbata is found sometimes
in treeless grasslands, but also in forests (especially in
Mediterranean countries), maybe suggesting more xer-
ophilic preferences. This lineage has a trichodermal cutis
similar to that reported by Harmaja (1974) for specimens
identified as P. atra, suggesting that he was probably
studying the same taxon, but unfortunately no samples
coming from northern Europe could be examined. On the
other hand, Kuyper (1995) observed P. atra has clamps at
all septa in mycelium, and even hyphae in the pileus
context are sparsely clamped also, suggesting that this
taxon is actually different from P. obbata and might cor-
respond to P. cyathiformis Lineage I. The possibility of a
new species cannot be rejected; Harmaja’s and Bon’s
descriptions of P. atra match some of our atypical col-
lections of P. cyathiformis I (for instance PAM14082509)
with especially pruinose and non-umbilicate pileus.
Other specimens examined: Pseudoclitocybe sp.: USA:
California, Santa Cruz Co., Nisene Marks State Park, leg.
C. Schwarz, 13-XII-2015, MO 225374/LIP 0401355.
Pogonoloma (Singer) Sa
´nchez-Garcı
´ain Sa
´nchez-Garcı
´a
et al., Taxon 63(5): 1001 (2014)
Basionym: Porpoloma subgen. Pogonoloma Singer in
Sydowia 15: 53. 1962 (‘‘1961’’)
:Porpoloma sect. Pogonoloma (Singer) Bon in Doc.
Mycol.9(33): 25. 1978 (Fig. 3a)
Description: Habit tricholomoid. Pileus umbonate to
flat, surface spinose or tomentose at margin, tending to
break into scales from centre. Lamellae crowded, emargi-
nate, turning yellowish with age. Stipe rooting, smooth,
without veil, staining yellow with age. Context fleshy,
white, yellowing with age; smell strong, aromatic, nau-
seous when old. Spores small, 5–7 93.5–4.2 lm, ovoid to
shortly cylindrical, smooth, microguttulate at maturity,
strongly amyloid, acyanophilic. Basidia small and slender,
26–32 95–7 lm, guttulate before maturity. Lamellae
edge fertile, with sparse cystidioid elements. Pileipellis a
trichocutis of long fasciculate hyphae, gelatinized or not.
Pigment intracellular. Pileitrama and mediostratum of the
hymenophoral trama of sarcodimitic structure, with long
broad physalohyphae and slender cylindrical hyphae,
mixed with sparse to frequent thromboplerous hyphae
branched at ends. On ground, ‘‘presumably saprotrophic’
(Sa
´nchez-Garcı
´a et al. 2014).
Pogonoloma spinulosum (Ku
¨hner & Romagn.) Sa
´nchez-
Garcı
´ain Sa
´nchez-Garcı
´a et al., Taxon 63(5): 1001 (2014)
Basionym: Tricholoma spinulosum Ku
¨hner & Romagn.,
Bull. mens. Soc. Linn. Soc. Bot. Lyon 16: 136 (1947)
:Leucopaxillus spinulosus (Ku
¨hner & Romagn.)
Konrad & Maubl., Encyclop. Mycol. 14: 409 (1949)
:Porpoloma spinulosum (Ku
¨hner & Romagn.) Singer,
Sydowia 15(1–6): 53 (1962)
=Tricholoma guttatum s. J.E. Lange Flora Agaricina
Danica I, p. 55, pl. 24 fig. E (1935) (as ‘‘Tricholoma gut-
tatum Barla nec al.’’).
=Porpoloma macrorhizum s. Bon, Docums. Mycol.
9(33): 26 (1978)
Description: Pileus 3–9 cm, broadly umbonate, covered
by a thin silky fibrillum on a smooth, dry ground, foxy
yellow at centre, light ash-grey progressively fading
towards margin; margin white, enrolled till the end, min-
utely spinulose. Lamellae crowded, 56 at stipe, 3 series of
lamellulae, sinuate, deeply uncinate, cream white; edge
thin, minutely serrulate, concolorous. Stipe
5–12 90.8–1.2 cm, minutely pruinose all over, white,
cream to dirty yellowish if bruised; base rooting. Context
white, firm; smell of banana; taste bitterish. Spores
5.0–6.5 93.5–4.2 lm, ovoid to ellipsoid, smooth, strongly
amyloid, acyanophilous; content microguttulate at matu-
rity. Basidia 26–32 96–6.5 lm, 4-spored, narrowly cla-
vate, guttulate before maturity. Lamellae edge fertile, with
cylindrical cystidioles sparsely protruding up to 25 lm.
Pleurocystidia none. Subhymenium ramose, divergent,
15–20 lm thick. Hymenophoral trama with a differentiated
hymenopodium 30–40 lm thick, slightly divergent, made
of slender hyphae 4–6 lm wide. Mediostratum of regular
structure, made of broad parallel hyphae 5–22 lm wide,
mixed with slender hyphae 3–47 lm wide, with sparse pale
yellow thromboplerous hyphae. Pileipellis when young an
ixotrichocutis made of long slender hyphae 3.5–5 lm wide,
smooth to very faintly punctuate, with vacuolar pigment,
fasciculate towards margin, prostrate and collapsing at
centre and with age. Subpellis 60 lm thick, weakly dif-
ferentiated, made of slender parallel hyphae 3.5–4.5 lm
wide. Pileitrama of sarcodimitic structure, made of broad
physalohyphae 7–10 lm wide with colourless intracellular
granules, mixed with slender cylindrical hyphae 3–6 lm
wide, all smooth and slightly thick-walled, and sparse
thromboplerous hyphae with pale yellow content, 3–5 lm
wide, often ramose. Clamps present at all septa, loop-like.
Specimens examined: FRANCE. Dordogne, Notre-
Dame de Sanilhac, La Male
´tie, boadleaved forest on clay-
calcareous soil, leg. G. Eyssartier, 24-VIII-1995, M. Bon
95040 (LIP, as ‘Porpoloma macrocephalum’), not
sequenced. Loire-Atlantique, Saint-Philibert-de-Grand-
Lieu, under Quercus sp., leg. G. Mabon, 01-X-1992, Coll.
J. Mornand 9266/M. Bon (LIP 0101354, as ‘‘Porpoloma
macrocephalum’’ ). Pas-de-Calais, Desvres, Fore
ˆt doma-
niale, Rue Noire, broadleaved thickets under Carpinus
betulus and Quercus robur on calcareous soil, leg.
R. Courtecuisse, 9-IX-2016, PAM16070903/LIP 0401167.
Pas-de-Calais, Desvres, La Drouille, mixed broadleaved
forest with Quercus robur, leg. J.-P. Gave
´riaux, 11-IX-
126 Fungal Diversity (2018) 90:109–133
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2016, PAM16091102/LIP 0401166. Yonne, A6 motorway
rest area near Auxerre, mixed broadleaved trees on cal-
careous ground, leg. G. Redeuilh, 14-IX-1981, M. Bon
8109 (LIP, as ‘Porpoloma cf. macrocephalum’), not
sequenced.
Ecology: found in European temperate broadleaved
forests, but originally reported from Picea abies (Ku
¨hner &
Romagnesi 1947). In autumn.
Pogonoloma macrorhizum (Que
´l.) Dima & P.-A. Mor-
eau, comb. nov.
MycoBank MB 824745 (Fig. 3a)
Basionym: Gyrophila macrorhiza Que
´l., Enchir. Fung.:
13 (1886) [cites ‘‘Lasch. Kalch. t. 3, fig. 1’’, indirectly
referring to Agaricus macrorhizus Lasch, Linnaea 3: 396
(No. 240) (1828), nom. illeg., non Agaricus macrorhizus
Pers., Observ. mycol. (Lipsiae) 1: 47 (1796)].
:Tricholoma macrorhizum (Que
´l.) Sacc., Syll. fung.
(Abellini) 5: 105 (1887)
:Armillaria macrorhiza (Que
´l.) Jacobashch, Verh. bot.
Ver. Prov. Brandenb. 37: LXI (1895) [citing basionym as
‘‘ Tricholoma macrorhizum (Lasch) Fr.’’]
:Leucopaxillus macrorhizus (Que
´l.) Sacconi & Laz-
zari, Boll. Gruppo Micol. G. Bresadola Trento 23(5–6):
114 (1980)
:Porpoloma macrorhizum (Que
´l.) Bon, Docums
Mycol. 20(no. 78): 38 (1990)
:Agaricus macrocephalus Schulzer in Kalchbrenner,
Icon. Sel. Hymenomyc. Hung. (Budapest): 11, tab. 3
(1873) nom. illeg. Lectotype: icone, Kalchbrenner &
Schulzer, Icon. Sel. Hymenomyc. Hung. tab. III, fig. 1.
1873 [Designated by Sa
´nchez-Garcı
´a, Matheny, Palfner &
Lodge, Taxon 63(5):1001. 2014, MycoBank MBT
381114], non Agaricus macrocephalus Schumach., Enum.
pl. (Kjbenhavn) 2: 264 (1803).
:‘‘Coolia macrocephala’’ Huijsman, Medded. Nedl.
Mycol. Ver. 28: 60 (1943) [as ‘‘(Schulz.) Huijsman comb.
nov.’’, nom. invalid., published in an invalid genus, ICN
Art. 39.1]
:‘‘ Squamanita macrocephala’ M.M. Moser, in Gams,
Kl. Krypt.—Fl. Mitteleuropa—Die Bla
¨tter- und Bauchpilze
(Agaricales und Gastromycetes) (Stuttgart) 2: 66 (1953),
nom invalid. [as ‘‘(Schulz.) M.M. Moser comb. nov.’’, no
full and direct reference to the replaced synonym, ICN Art.
41.5]
:‘‘Leucopaxillus macrocephalus’’ Bohus, Fragm. Bot.
Mus. Hist.-Nat. Hung. 4(1–4): 37 (1966), nom. invalid. [as
‘(Schulz.) Bohus comb. nov.’’, nom. inval., no full and
direct reference to the replaced synonym, ICN Art. 41.5]
:Porpoloma macrocephalum Bon, Docums Mycol.
9(33): 26 (1978) [replacement name as ‘‘(Schulzer apud
Kalchbrenner) comb. nov.’’, ICN Art. 6.11, Art. 41.6, 41.8]
:Pogonoloma macrocephalum (Bon) Sa
´nchez-Garcı
´a
in Sa
´nchez-Garcı
´a, Matheny, Palfner & Lodge, Taxon
63(5): 1001 (2014) [corrected authority ‘‘(Schulzer) Sa
´n-
chez-Garcı
´a comb. nov.’’]
Description: Pileus 5–30 cm broad, hemispherical then
convex, finally applanate, sometimes somewhat depressed
in the centre, with the margin a longtime enrolled, wavy-
lobed. Cuticle tomentose, opaque, creamy then brownish
ochre with a shade of orange, soon dissociated in patches.
Lamellae rather crowded, adnate-emarginate, whitish,
reddening when bruised, with the edge irregular, concol-
orous. Stipe 2.5–16.0 91.5–8.0 cm, often with many
specimens grown together emerging from a common base,
thickset, solid, cylindrical to ventricose, often rooting,
whitish, ochre when bruised, minutely furfuraceous. Con-
text tough, firm, whitish, slowly yellowing when cut. Smell
complex, with a component of wet mould over a scent of
over-ripe fruit or cornsilk; taste unpleasant. Spore print
whitish. Spores 5.0–6.5 93.5–4.5 lm, shortly cylindrical
to broadly ellipsoid, smooth, hyaline, amyloid. Basidia
25–32 95–7 lm, 4-spored with short sterigmata, nar-
rowly clavate; content densely granular before maturity;
base clamped, often crozier-like. Lamellae edge fertile,
with sparse broad, clavate cystidioid elements
12–25 96–16 lm, colourless, thin-walled and often
incrusted by small granulations. Subhymenium ramose,
erected, made of short cylindrical hyphae. Hymenophoral
trama parallel, made of long cylindrical hyphae 3.5–8.0 lm
wide, partly with refringent content, some thromboplerous-
like and spreading abundant resinoid content in KOH.
Pileipellis a dry trichocutis formed by fascicles of long
slender hyphae with smooth, slightly thickened wall, ter-
minal element 80–150 94–5.5 lm, cylindrical. Subpellis
hardly differentiated, 40–60 lm thick, made of hyphae
3–5.5 lm wide, abundantly clamped. Pileitrama radially
oriented, of sarcodimitic structure made of broad physa-
lohyphae 7–10 lm wide with granular content, and slender
cylindrical hyphae 3–5 lm wide, and frequent thrombo-
plerous hyphae 5–8 lm wide, cylindrical and branched
towards ends with pale yellow homogeneous content.
Clamps present at all septa, loop-like and voluminous.
Specimens examined: ITALY. Emilia-Romagna,
Monghidoro (Bologna), Valgattara, under Castanea sativa
and Quercus pubescens, leg. M. Barbieri, 20-VI-2017,
AMB 18232. SWITZERLAND. Ticino, Bruzella-Cabbio,
leg. A. Marchand, 22-VIII-1981, coll. M. Bon, LIP
0101353 (as ‘Porpoloma macrocephalum’).
Ecology: Central European temperate broadleaved for-
ests, in tufts with numerous specimens growing together,
under broadleaved trees, mainly larger oaks. Spring to
autumn. Widespread but rare.
Comments: the nomenclature of this taxon is obscure,
and the treatment proposed here is purely nomenclatural.
Fungal Diversity (2018) 90:109–133 127
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The name Agaricus macrocephalus Schulzer was probably
mentioned for the first time in Schulzer’s unpublished
manuscript ‘Schwa
¨mme und Pilze aus Ungarn und Sla-
wonien’ deposited at the Hungarian Academy of Sciences
in 1869 (Gombocz 1936; Tortic
´1981). Schulzer’s illegit-
imate basionym (published in Kalchbrenner 1873) was
unfortunately combined into different genera without fully
citing the basionym (ICN Art. 41.5), therefore most
replacement names based on these combinations are inva-
lid. A combination into genus Coolia Huijsman (Huijsman
1943) fully cites Schulzer’s basionym, but Coolia is an
invalid genus (ICN Art. 39.1), and so a replacement name
based on it would not be possible. The oldest valid
replacement name seems to be attributable to Bon (1978)
who published a combination in the genus Porpoloma,
citing explicitly Schulzer’s basionym. The combination
into Pogonoloma by Sa
´nchez-Garcı
´a et al. (2014)
employed Schulzer’s replaced synonym as basionym, a
correctable formal error amended here using Bon’s
replacement name. Unfortunately, while Bon’s validation
would have provided a stable solution to the taxonomy of
this remarkable species, an old confusion due to Fries
(1878, p. 58) between Schulzer’s taxon and the hardly
interpretable Ag. macrorhizus Lasch (1828) forces to
renounce to Sa
´nchez-Garcı
´a et al. (2014) name. After Fries
proposed the two names as synonyms, Que
´let (1886, p. 13)
introduced the name Gyrophila macrorhiza, based on
Lasch’s illegitimate name (later homonym of Ag. macro-
rhizus Pers., 1796), but considered here as a new name
(rather than a replacement name) because based exclu-
sively on Schulzer’s description and citing Kalchbrenner’s
plate 3 fig. 1 as reference. This plate cited by Que
´let is
interpreted under the current Code of nomenclature as the
only original material (therefore only possible lectotype)
for Gyrophila macrorhiza Que
´l. Because this plate is also
the lectotype of Porpoloma macrocephalum Bon, the two
names are automatically nomenclatural synonyms.
This remarkable and rare European species differs from
P. spinulosum by larger basidiomata, caespitose growth,
fruiting in spring and summer (sometimes autumn as well),
a different, stronger and nauseous smell (of banana in P.
spinulosum), and a pileipellis not gelatinized, not forming
spines but a tomentum at margin, and early dissociating in
broad imbricated scales. In Hungary, the heaviest basid-
iomata measured so far was 1.75 kg (Siller et al. 2006).
The species has gained legal protection in Hungary since
2005 (Siller et al. 2006). The Italian collection identified as
Leucopaxillus nauseodulcis and sequenced by Osmundson
et al. (2013, GenBank JF908326) is likely a misidentifi-
cation. Pogonoloma macrorhizum was at least reported
once from France (fore
ˆtdeSe
´nart, near Paris) by Ku
¨hner
and Romagnesi (1947). On the other side, all collections
described by Bon (1976) as ‘Porpoloma macrorhizum’’
revealed to correspond to old specimens of P. spinulosum
described above. The Swiss collection LIP0101354 was
described and illustrated by Marchand (1986)asPor-
poloma macrocephalum.
Excluded taxa
Pseudoclitocybe sphagneti Raithelh., Metrodiana 3(1):
XXIV (1972)
Material studied: Germany, Baden-Wu
¨rttemberg, near
Calw, Wu
¨rzbacher Moor, leg. J. Raithelhuber, PtD-11171
(isotype: ZT Myc 58861)
=Fayodia gracilipes (Britzelm.) Bresinsky & Stangl
Comments: the isotype deposited at ZT (Zu
¨rich, CH)
consists in a well-preserved half-specimen. Contrary to the
original description, microscopical features of the speci-
men are all typical of Fayodia gracilipes (Britzelm.)
Bresinsky & Stangl (= F. bisphaerigera (J.E. Lange)
Singer), especially the inconfundible spores which are
globose, thick-walled with characteristically pitted myx-
osporium, and amyloid perisporium. The synonymy is
therefore established here.
Discussion
In the present work, two species of Clitocybe section
Disciformes,C. harperi and C. alexandri, are shown to be
genetically separate from the Clitocybeae. Clitocybe
alexandri is proposed as a type species of the new genus
Clitopaxillus, and C. harperi as a type species of Harma-
jaea. The monophyletic lineage composed of Pseudocli-
tocybe,Musumecia,Clitopaxillus,Harmajaea, and
Pogonoloma, is here proposed as the new family Pseudo-
clitocybaceae. The purpose of this name is to reflect the
monophyletic status of several lineages not related to Cli-
tocybeae, Tricholomataceae or any other family, which
often display characteristic morphological features such as
absent or poorly differentiated cystidia and clamp con-
nections in the basidiomes, and show amyloid spores. None
of these traits is constant within Pseudoclitocybaceae,
making this family apparently heterogeneous and difficult
to define based on morphology. However, some remarkable
features exist, such as loop-like or medallion-type clamps
(where present), an ‘‘archaic’’ feature found in a few other
genera within Agaricales such as Gliophorus Herink, Hu-
midicutis (Singer) Singer and Porpolomopsis Bresinsky
(Hygrophoraceae) (Lodge et al. 2014)orClavaria P. Mich.
ex L. (Clavariaceae) (Birkebak et al. 2013); or a homo-
morphic structure of the whole basidiome, based on
cylindrical hyphae of wide diameter ([5–6 lm), with
frequent internal globules, and forming a regular trama.
Interestingly, Ku
¨hner (1980) pointed out that species of
Pseudoclitocybe and C. alexandri have plurinucleate
128 Fungal Diversity (2018) 90:109–133
123
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terminal hyphae in secondary mycelium (holocoenocytic
mycelium sensu Boidin 1964 and Stalpers 1978), a feature
which might play a role in the disjunct distribution of
clamps in mycelia and basidiomes, and a bipolar
heterothallism (unusual in Agaricales, Petersen 1995). No
comparable information is available either from Po-
gonoloma or Musumecia species.
Other families in the suborder Tricholomatinae, such as
Biannulariaceae, Entolomataceae, Lyophyllaceae, Tri-
cholomataceae and the Clitocybeae lineage can easily be
discriminated from Pseudoclitocybaceae by means of DNA
analysis. Biannulariaceae (as Catathelasmataceae in Sa
´n-
chez-Garcı
´a et al. 2016), Entolomataceae (Co-David et al.
2009; Baroni et al. 2011; Kluting et al. 2014), Tricholo-
mataceae (Sa
´nchez-Garcı
´a et al. 2014), and Lyophyllaceae
(Hofstetter et al. 2014; Redhead 2014; Bellanger et al.
2015) have been recently reviewed and re-organized,
resulting in several genera being proposed or amended to
accommodate the multigenic data obtained from an
increasing number of species. Morphologically, Lyophyl-
laceae species have siderophilous basidia (Bellanger et al.
2015), and Entolomataceae produce pinkish spore prints,
and their spores have a voluminous lipidic droplet, a tri-
angular apicule and bumps and/or ridges formed by an
epicorium (Co-David et al. 2009; Baroni et al. 2011;
Kluting et al. 2014), but no evident synapomorphic feature
has been identified so far for either Biannulariaceae, Tri-
cholomataceae or Clitocybeae lineages. Tricholomataceae
are loosely characterized by their tricholomatoid habit
(large and fleshy, convex pileus, lamellae commonly not
decurrent), while Clitocybeae almost always have clamped
hyphae, a feature sometimes present also in Pseudoclito-
cybaceae. Biannulariaceae have been recently amended to
include several genera previously classified in different
taxa, such as Callistosporium Singer, Macrocybe Pegler &
Lodge, Pleurocollybia Singer, or Pseudolaccaria Vizzini,
Contu & Z.W. Ge, and is mainly defined by means of
genetic inference at the present time (Sa
´nchez-Garcı
´a et al.
2016).
Pseudoclitocybaceae shares several morphological traits
with Tricholomataceae and Clitocybeae, but can be dis-
criminated because of their often decurrent or subdecurrent
lamellae, cystidia and clamp connections usually absent,
and often amyloid spores. The singular hyphal structure,
lacking slender hyphae \4lm wide in all species studied
but Pogonoloma spp., the broad, loop-like clamps (absent
only in Musumecia bettlachensis, and not proved to be
lacking in the mycelium of Harmajaea harperi), the
hymenophoral trama with usually long, parallel or sub-
parallel hyphae, the presence of globules in most hyphae of
context, and the tendency of most species to turn yellowish
to dirty brown when drying are hypothesized here as sig-
nificant features for defining this family, but should be
more systematically investigated in related lineages. Such a
definition based on ‘‘secondary’’ morphological features
implies a revision of many species through reference
herbarium material and fresh collections, since these fea-
tures are rarely described in protologues and in taxonomic
literature in general.
Clamps are either present throughout the basidiome in
C. fibulatus or restricted to specific areas and at most
transformed into ‘‘false’ clamps elsewhere in C. alexandri,
while Harmajaea species completely lack clamp connec-
tions on basidiomata (but they are present on mycelium).
This variability, which seems to have a specific value in
this whole lineage, suggests that maybe clampless species
could be present also in Clitopaxillus, making it difficult to
establish clear-cut limits between both genera. Clamp
connections are sparsely present in Pseudoclitocybe spe-
cies, and either abundant, sparsed or absent in the sister
genus Musumecia. Similarly, spore amyloidity was
recently shown to vary between species of Musumecia as
new taxa are found and described (Li et al. 2016). Identi-
fication of H. harperi is relatively easy, because of the
differences with other clitocyboid taxa lacking clamp
connections: Clitocybe griseifolia (Murrill 1913) is the
most similar, but has broader lamellae, white stipe, and
fragrant odor (Bigelow 1965,1982), while other species
lacking clamp connections described by Bigelow (1983),
such as C. borealis H.E. Bigelow, C. adustiterricola H.E.
Bigelow, C. payettensis H.E. Bigelow, C. hesleri H.E.
Bigelow, and C. solumophila H.E. Bigelow, are all much
smaller in size than C. harperi (0.5–1.5 cm on average vs.
8–10 cm in C. harperi). Harmajaea wellsiae differs
because of its brownish pileus, almost adnate lamellae and
a boreal distribution, while the new taxon H. guldeniae has
also a brownish pileus, clearly decurrent lamellae, longer
basidia, and clamped mycelium.
Species in Pseudoclitocybe usually produce funnel-
shaped basidiomata lacking cystidia and clamp connec-
tions, although the latter can be observed on secondary
mycelia in culture (Ku
¨hner 1980) and at the base of the
stipe and underlying mycelium (Kuyper 1995). Thorough
observations on the collections cited above confirm that the
distribution of clamp connections in Pseudoclitocybe is
also a specific feature: in P. cyathiformis (Linages I and II)
clamp connections are only observed in mycelium, and
only on some septa, whereas in collections identified as P.
obbata hyphae are clamped at all septa in mycelium, and
sparsely in pileus context. Considering this, Kuyper’s
(1995) observations might not concern P. cyathiformis s.
str. but the most abundantly clamped species in Europe,
i.e., P. obbata as interpreted here.
Musumecia was named by Vizzini et al. (2011) to honor
Swiss mycologist Enzo Musumeci, who was the first to
report it from Alsace (France). Molecular data as well as
Fungal Diversity (2018) 90:109–133 129
123
Author's personal copy
some shared morphological traits linked Musumecia and
Pseudoclitocybe: cutis-like pileipellis, elongated basidia,
smooth, acyanophilous spores, and absence of clamp con-
nections in basidiomata (although Pseudoclitocybe spp.
form clamps in mycelium). However, Musumecia was
considered an independent genus, because of its hygro-
phoroid habit (non-depressed, convex pileus and distant
thick lamellae), the darkening of lamellae and stipe, and
non-amyloid spores, as well as for the evident genetic
differences between both lineages. The type species, M.
bettlachensis Vizzini & Contu (Vizzini et al. 2011), is
whitish and grows caespitose in Abies alba,Fraxinus sp.
and Fagus sylvatica forests, while M. vermicularis Musu-
meci (Musumeci 2014), has a zonate brownish dark pileus,
is gregarious but not caespitose, grows under Carpinus
betulus, and produces rhizomorphs. Moreover M. vermic-
ularis is abundantly clamped in rhizomorphs and basid-
iomes (although not at all septa, and with occasionally
unclosed or verticillate clamps, like C. alexandri).
Recently, two other species of Musumecia have been pro-
posed in Li et al. (2016): M. sardoa Consiglio, Vizzini &
Setti with scarce clamps present only in subpellis and
pileitrama, and M. alpina L.P. Tang, J Zhao & S.D. Yang,
which has abundant clamps all over the basidiome.
Musumecia alpina produces hymenial cystidia and verru-
culose non-amyloid spores, while M. sardoa has no cys-
tidia and clearly amyloid spores. Although Musumecia was
originally described with inamyloid spores (Vizzini et al.
2011), the spores of M. bettlachensis holotype (TO
HG2284) examined under a standardized procedure by
some of the present authors turned out to be weakly
amyloid in grey colour. The spores of C. alexandri and H.
harperi showed also a weak amyloid reaction with this
procedure (Fig. 4d), suggesting that this feature should be
further investigated, and definitions amended to accom-
modate these findings.
The tricholomatoid genus Pogonoloma had already been
reported to be closely related to Pseudoclitocybe and
Musumecia (Sa
´nchez-Garcı
´a et al. 2014). The genus was a
new rank for Porpoloma subgen. Pogonoloma Singer,
proposed to accommodate the type species Porpoloma
spinulosum (Ku
¨hner & Romagn.) Singer, as well as P.
macrocephalum (Schulzer) Singer, after preliminary data
suggested Porpoloma was actually polyphyletic (Vizzini
et al. 2012). Both species have a felted-subsquamulose
pileus surface, a trichocutis-like pileipellis forming a thick
tomentum or spines at margin, intracellular pigmentation,
amyloid spores, lack of typical cystidia (only scarce
‘marginal hairs’’), and present clamp connections at all
septa (Ku
¨hner and Romagnesi 1947; Bon 1991; Kuyper
1995), features shared by other members of Pseudoclito-
cybaceae but also widespread across the Agaricales.
Moreover the tricholomatoid habit as well as the doubtfully
saprobic (possibly ectomycorrhizal?) behaviour are
extralimital in this family. In the present work we chose to
include it in the new family because of its significant
genetic relationship, but also because they share the same
features observed as characteristic in the clitocyboid
members of the family: hymenophoral trama made of
broad, cylindrical hyphae [5lm wide, many with inter-
nal globules, hymenophoral trama subregular, loop-like
clamp connections, and loosely branched subhymenium. In
the original description of P. spinulosum (Ku
¨hner &
Romagnesi 1947), all these features were already men-
tioned but no systematic importance was given to them at
that time. Ku
¨hner pointed out the ‘‘large clamps’’ and the
parallel hymenophoral trama with mostly broad, cylindrical
hyphae, and Romagnesi the ‘‘intracellular punctuations’’ in
hyphae of pileipellis. Interestingly, the parallel hymeno-
phoral trama is conform to the general definition of the
family given here, but the pileus trama shows a sar-
codimitic structure (Ku
¨hner and Romagnesi 1947) with a
majority of thick fusiform physalohyphae and a few gen-
erative hyphae of smaller diameter, figuring a possible
evolutional step towards the homomorphic structure of the
whole basidiome in the derived clitocyboid lineages. Po-
gonoloma seems to represent a basal clade of Pseudocli-
tocybaceae, so far only documented by two rare European
species, and therefore its position could be re-evaluated in
case new data become available to fill in biodiversity gaps.
Acknowledgements We are grateful to Raymond Archambault,
Didier Borgarino, Tor Erik Brandrud, Marco Clericuzio, Philippe
Clowez, Guillaume Eyssartier, Jean-Pierre Gave
´riaux, Gro Gulden,
Didier Huart, Gary A. Laursen, Vello Liiv, Jean-Marc Moingeon,
Ronald Pastorino, Carlos Pe
´rez del Amo, Christian Schwarz, Alessia
Tatti, Jukka Vauras, and Øyvind Weholt, for providing samples,
images, and/or ecological data of the species studied, as well as
Reinhard Berndt (herbarium ZT, Zu
¨rich) for the loan of an isotype of
Pseudoclitocybe sphagneti, and Re
´gis Courtecuisse and Christophe
Le
´curu (herbarium LIP, Lille) for having put their own material as
well as Marcel Bon’s collections and unpublished notes at our dis-
posal. We thank also Jean-Michel Bellanger, Marisol Sa
´nchez-Garcı
´a,
and Brandon Matheny, for providing useful data and DNA sequences
for the present work, and Shaun Pennycook for his expert advice
about nomenclature of Pogonoloma macrorhizum.
References
Adamc
ˇı
´k S, Christensen M, Heilmann-Clausen J, Walleyn R (2007)
Fungal diversity in the Poloniny National Park with emphasis on
indicator species of conservation value of beech forests in
Europe. Czech Mycol 59(1):67–81
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic
local alignment search tool. J Mol Biol 215:403–410
Alvarado P, Moreno G, Vizzini A, Consiglio G, Manjo
´n JL, Setti L
(2015) Atractosporocybe,Leucocybe and Rhizocybe: three new
clitocyboid genera in the Tricholomatoid clade (Agaricales) with
notes on Clitocybe and Lepista. Mycologia 107(1):123–136
130 Fungal Diversity (2018) 90:109–133
123
Author's personal copy
Ammirati J, Parker AD, Matheny PB (2007) Cleistocybe, a new genus
of Agaricales. Mycoscience 48:282–289
Baroni TJ, Matheny PB (2011) A re-evaluation of gasteroid and
cyphelloid species of Entolomataceae from eastern North
America. Harvard Pap Bot 16(2):293–310
Baroni TJ, Hofstetter V, Largent DL, Vilgalys R (2011) Entocybe is
proposed as a new genus in the Entolomataceae (Agari-
comycetes, Basidiomycota) based on morphological and molec-
ular evidence. N Am Fungi 6(12):1–19
Bas C, Kuyper TW, Noordeloos ME (1995) Flora Agaricina
Neerlandica 3. CRC Press, Boca Raton
Bellanger JM, Moreau P-A, Corriol G, Bidaud A, Chalange R,
Dudova Z, Richard F (2015) Plunging hands into the mushroom
jar: a phylogenetic framework for Lyophyllaceae (Agaricales,
Basidiomycota). Genetica 143(2):169–194
Bigelow HE (1965) The genus Clitocybe in North America.
Section Clitocybe. Lloydia 28:139–180
Bigelow HE (1982) North American species of Clitocybe. I. Beih
Nova Hedwig 72:1–280
Bigelow HE (1983) Some clampless species of Clitocybe. Crypt
Mycol 4:93–98
Binder M, Larsson K-H, Matheny PB, Hibbett DS (2010) Amylo-
corticiales ord. nov. and Jaapiales ord. nov.: early diverging
clades of Agaricomycetidae were dominated by corticioid forms.
Mycologia 102:865–880
Birkebak JM, Mayor JR, Ryberg M, Matheny PB (2013) A
systematic, morphological and ecological overview of the
Clavariaceae (Agaricales). Mycologia 105:896–911
Boidin J (1964) Valeur des caracte
`res culturaux et cytologiques pour
la taxinomie des Thelephoraceae re
´supine
´sete
´tale
´s-re
´fle
´chis
(Basidiomyce
`tes). Bull Soc Bot Fr 111(7–8):309–315
Bon M (1978) Tricholomataceae de France et d’Europe occidentale -
5- (Sous-famille Leucopaxilloideae (Singer) Bon). Doc Mycol
9(33):1–79
Bon M (1991) Tricholomataceae (1re partie). (Tricholomoideae et
Leucopaxilloideae). Genres: Tricholoma,Tricholomopsis,Cal-
listosporium,Porpoloma,Floccularia,Leucopaxillus et Me-
lanoleuca. Flore Mycologique d’Europe n°2. Doc Mycol Me
´m
Hors Se
´r 2:1–163
Bon M (1997) Tricholomataceae (2e partie). Genres: Clitocybe,
Armillaria,Lepista,Ripartites,Omphalina,Gerronema,Rick-
enella,Chrysomphalina,Haasiella,Gamundia,Omphaliaster,
Cantarellula,Pseudoomphalina,Clitocybula,Pseudoclitocybe,
Myxomphalia,Fayodia. Flore Mycologique d’Europe n°4. Doc
Mycol Me
´m Hors Se
´r 4:1–181
Boursier J (1925) Leucopaxillus nov. gen. Bull Trim Soc Mycol Fr
41:391–393
Bulliard JBF (1782) Herbier de la France 2:49–96
Cle
´menc¸on H (1972) Zwei verbesserte Pra
¨parierlo
¨sungen fu
¨r die
microskopische Untersuchung von Pilze. Z Pilzkd 38:49–53
Co-David D, Langeveld D, Noordeloos ME (2009) Molecular
phylogeny and spore evolution of Entolomataceae. Persoonia
23:147–176
Dentinger BTM, Gaya E, O’Brien H, Suz LM, Lachlan R, Dı
´az-
Valderrama JR, Koch RA, Aime MC (2015) Tales from the
crypt: genome mining from fungarium specimens improves
resolution of the mushroom tree of life. Biol J Linn Soc
117:11–32
Dima B, Lindstro
¨m H, Liimatainen K, Olson A
˚, Soop K, Kyto
¨vuori I,
Dahlberg A, Niskanen T (2016) Typification of Friesian names
in Cortinarius sections Anomali,Spilomei, and Bolares, and
description of two new species from northern Europe. Mycol
Prog 15:903–919
Fanneche
`re G (2006) Mycome
`tre 2. Accessed Oct 2017
Fries EM (1821) Systema mycologicum. Lund 1:1–520
Fries EM (1832) Systema mycologicum 3:261–524
Fries EM (1836–1838) Epicrisis systematis mycologici. Uppsala
Fries EM (1878) Hymenomycetes Europaei. Uppsala
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity
for Basidiomycetes—application to the identification of mycor-
rhizae and rusts. Mol Ecol 2:113–118
Garnica S, Weiss M, Walther G, Oberwinkler F (2007) Reconstruct-
ing the evolution of agarics from nuclear gene sequences and
basidiospore ultrastructure. Mycol Res 111:1019–1029
Gillet C-C (1869) Note sure l’agaric de
´licieux. Bull Soc Linn
Normandie 2e se
´rie 4:247–257
Gillet C-C (1876) Les Hyme
´nomyce
`tes ou Description de tous les
Champignons qui Croissent en France 1:177–560
Gillet C-C (1884) Tableaux analytiques des Hyme
´nomyce
´tes.
Alenc¸on
Gillet C-C in Vieillard M (1873) Se
´ance du 5 mai 1873. Bull Soc
Linn Normandie 2e serie 7:153–183
Gombocz E (1936) A magyar botanika to
¨rte
´nete: A magyar flo
´ra
kutato
´i. Budapest. [in Hungarian]
Gulden G (2006) Clitocybe harperi—a rare Clitocybe species in
Europe. Agarica 26:65–68
Harmaja H (1969) The genus Clitocybe (Agaricales) in Fennoscandia.
Karstenia 10:5–121
Harmaja H (1974) A revision of the generic limit between Clitocybe
and Lepista. Karstenia 14:82–92
Harmaja H (1976) A further revision of the generic limit between
Lepista and Clitocybe. Karstenia 15:13–15
Harmaja H (1978) New species and combinations in the pale-spored
Agaricales. Karstenia 18:29–30
Harmaja H (1979) Type studies in Clitocybe 3. Karstenia 19:22–24
Harmaja H (2003) Notes on Clitocybe s. lato (Agaricales). Ann Bot
Fenn 40:213–218
He X-L, Li T-H, Xi P-G, Jiang Z-D, Shen Y-H (2013) Phylogeny of
Entoloma s.l. subgenus Pouzarella, with descriptions of five new
species from China. Fungal Divers 58(1):227–243
Hibbett DS (1996) Phylogenetic evidence for horizontal transmission
of group I introns in the nuclear ribosomal DNA of mushroom-
forming fungi. Mol Biol Evol 13(7):903–909
Hofstetter V, Redhead SA, Kauff F, Moncalvo J-M, Matheny PB,
Vilgalys R (2014) Taxonomic revision and examination of
ecological transitions of the Lyophyllaceae (Basidiomycota,
Agaricales) based on a multigene phylogeny. Crypt Mycol
35(4):399–425
Huijsman HSC (1943) Observations sur le ‘‘genre’Lepiota. Medd
Nedl Mycol Ver 28:3–60
Kalchbrenner K (1873) Icones selectae Hymenomycetum Hungariae
I. Budapest
Kirk PM, Cannon PF, David JC, Stalpers JA (2001) Ainsworth and
Bisby’s dictionary of the fungi, 9th edn. CABI publishing,
Wallingford
Kluting KL, Baroni TJ, Bergemann SE (2014) Toward a stable clas-
sification of genera within the Entolomataceae: a phylogenetic
re-evaluation of the Rhodocybe-Clitopilus clade. Mycologia
106(6):1127–1142
Knudsen H, Vesterholt J (eds.) (2008) Funga Nordica. Copenhagen
Ku
¨hner R (1980) Les Hymenomycetes agaricoides (Agaricales,
Tricholomatales, Pluteales, Russulales). Etude ge
´ne
´rale et clas-
sification. Bull Mens Soc Linn Lyon 49, n8special:1–1027
Ku
¨hner R, Maire R (1934) E
´tude de la re
´action de la membrane
sporique a
`l’iode dans les divers genres d’Agarics leucospore
´s.
Bull Trim Soc Mycol Fr 50:1–24
Ku
¨hner R, Romagnesi H (1947) Caracte
`res et affinite
´sduTricholoma
guttatum au sens de Lange. Bull Mens Soc Linn Lyon 7:134–137
Kuthan J, Adamc
ˇı
´k S, Terray J, Antonı
´n V (1999) Huby na
´rodne
´ho
parku Poloniny (Fungi of the National Park Poloniny). Kos
ˇice
Fungal Diversity (2018) 90:109–133 131
123
Author's personal copy
Kuyper TW (1995) Clitocybe (Fr.) Staude. In: Bas C, Kuyper TW,
Noordeloos ME, Vellinga EC (eds) Flora Agaricina Neerlandica
3. A.A. Balkema, Rotterdam, pp 42–62
Li GJ, Hyde KD, Zhao RL, Hongsanan S, Abdel-Aziz FA, Abdel-
Wahab MA, Alvarado P, Alves-Silva G, Ammirati J, Ariya-
wansa HA et al (2016) Fungal diversity notes 253–366:
taxonomic and phylogenetic contributions to fungal taxa. Fungal
Divers 78(1):1–237
Liu YJ, Whelen S, Hall BD (1999) Phylogenetic relationships among
ascomycetes: evidence from an RNA polymerse II subunit. Mol
Biol Evol 16(12):1799–1808
Lodge DJ, Padamsee M, Matheny PB, Aime MC, Cantrell SA,
Boertmann D, Kovalenko A, Vizzini A, Dentinger BTM, Kirk
PM et al (2014) Molecular phylogeny, morphology, pigment
chemistry and ecology in Hygrophoraceae (Agaricales). Fungal
Divers 64:1–99
Maire R (1913) Etudes mycologiques. Ann Mycol 11:331–358
Malysheva EF, Morozova OV, Contu M (2010) New combinations in
Clitocybula: a study of cystidiate Pseudoomphalina species
(Basidiomycota, Agaricomycetes). Sydowia 63(1):85–104
Marchand A (1986) Champignons du Nord et du Midi. Tome 9. Les
tricholomes. Perpignan
Matheny PB (2005) Improving phylogenetic inference of mushrooms
with RPB1 and RPB2 nucleotide sequences (Inocybe; Agari-
cales). Mol Phyl Evol 35:1–20
Matheny PB, Curtis JM, Hofstetter V, Aime MC, Moncalvo J-M, Ge
Z-W, Yang Z-L, Slot JC, Ammirati JF, Baroni TJ et al (2006)
Major clades of Agaricales: a multilocus phylogenetic overview.
Mycologia 98(6):982–995
Matheny PB, Wang Z, Binder M, Curtis JM, Lim YW, Nilsson RH,
Hughes KW et al (2007) Contributions of rpb2 and tef1 to the
phylogeny of mushrooms and allies (Basidiomycota, Fungi).
Mol Phyl Evol 43:430–451
Moncalvo J-M, Vilgalys R, Redhead S, Johnson JE, James TY et al
(2002) One hundred seventeen clades of euagarics. Mol Phyl
Evol 23:357–400
Moreau P-A (2009) In: Maire J-C., Moreau P-A, & Robich G. (eds).
Re
´vision des Tricholomataceae clitocyboı
¨des et omphaloı
¨des in
Comple
´ments a
`la Flore des champignons supe
´rieurs du Maroc
de G. Malenc¸on et R. Bertault. Confe
´de
´ration Europe
´enne de
Mycologie Me
´diterrane
´enne, Nice, pp 449–453
Murrill WA (1913) The Agaricaceae of the Pacific Coast—IV. New
species of Clitocybe and Melanoleuca. Mycologia 5(4):206–223
Murrill WA (1915) The genus Lepista. Mycologia 7(2):105–107
Musumeci E (2014) Fungi non delineati raro vel haud perspecte et
explorate descripti aut definite picti. Pars LXVII–LXIX. Con-
tributo alla conoscenza della Micoflora europea: Specie nuove
endemiche, funghi rari con microclima localizzato. Candusso
Edizioni, I-Alassio-(SV)
Musumeci E, Contu M (2014) Una nuova specie di Clitocybe della
sezione Aberrantissimae (Basidiomycetes, Tricholomataceae)
dalla Francia. Micol Vegetazione Mediterr 29(1):3–12
Nylander JAA (2004) MrModeltest v2. Program distributed by the
author. Evolutionary Biology Centre, Uppsala University,
Uppsala
Osmundson TW, Robert VA, Schoch CL, Baker LJ, Smith A, Robich
G, Mizzan L, Garbelotto MM (2013) Filling gaps in biodiversity
knowledge for macrofungi: contributions and assessment of an
herbarium collection DNA barcode sequencing project. PLoS
ONE 8(4):E62419
Ovrebo CL, Lodge DJ, Aime MC (2011) A new Cantharocybe from
Belize with notes on the type of Cantharocybe gruberi.
Mycologia 103:1102–1109
Patouillard NT (1887) Les Hyme
´nomyce
`tes d’Europe: Anatomie
ge
´ne
´rale et classification des champignons supe
´rieurs. P. Klinck-
sieck, Paris
Petersen RH (1995) Contributions of mating studies to mushroom
systematics. Can J Bot 73(1):S831–S842
Qin J, Feng B, Yang ZL, Li YC, Ratkowsky D, Gates G, Takahashi H,
Rexer KH, Kost GW, Karunarathna SC (2014) The taxonomic
foundation, species circumscription and continental endemisms
of Singerocybe: evidence from morphological and molecular
data. Mycologia 106(5):1015–1026
Que
´let L (1886) Enchiridion Fungorum. O. Doin, Paris
Redhead SA (2014) Nomenclatural novelties. Index Fungorum 202:1
Redhead SA, Ammirati JF, Norvell LL, Seidl MT (2000) Notes on
western North American snowbank fungi. Mycotaxon
76:321–328
Redhead SA, Lutzoni F, Moncalvo JM, Vilgalys R (2002) Phylogeny
of agarics: partial systematics solutions for core omphalinoid
genera in the Agaricales (euagarics). Mycotaxon 83:19–57
Rehner SA, Buckley E (2005) A Beauveria phylogeny inferred from
nuclear ITS and EF1-a sequences: evidence for cryptic diversi-
fication and links to Cordyceps teleomorphs. Mycologia
97(1):84–98
Ricken A (1915) Die Bla
¨tterpilze (Agaricaceae) Deutschlands und der
angrenzenden La
¨nder, besonders Oesterreichs und der Schweiz.
Leipzig
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phyloge-
netic inference under mixed models. Bioinformatics
19:1572–1574
Saccardo PA (1887) Sylloge Fungorum V. Patavii
Sa
´nchez-Garcı
´a M, Matheny PB, Palfner G, Lodge DJ (2014)
Deconstructing the Tricholomataceae (Agaricales) and introduc-
tion of the new genera Albomagister,Corneriella, Pogonoloma
and Pseudotricholoma. Taxon 63(5):993–1007
Sa
´nchez-Garcı
´a M, Henkel TW, Aime MC, Smith ME, Matheny PB
(2016) Guyanagarika, a new ectomycorrhizal genus of Agari-
cales from the Neotropics. Fungal Biol 120(12):1540–1553
Siller I, Dima B, Albert L, Vasas G, Fodor L, Pa
´l-Fa
´m F, Bratek Z,
Zagyva I (2006) Protected macrofungi in Hungary. Mikol
Ko
¨zlem Clusiana 45(1–3):3–158
Singer R (1936) Notes sur quelques Basidiomycetes. II. Rev Mycol
1:279–293
Singer R (1943) Das system der Agaricales. III. Ann Mycol 41:1–189
Singer R (1948) New genera of fungi. IV. Mycologia 40(2):262–268
Singer R (1951) New genera of fungi V. Mycologia 43(5):598–604
Singer R (1952) The agarics of the Argentine sector of Tierra del
Fuego and limitrophous regions of the Magallanes area. Sydowia
6(1–4):165–226
Singer R (1956) New genera of fungi. VII. Mycologia 48(5):719–727
Singer R (1961) Type studies on Basidiomycetes. X. Persoonia
2(1):1–62
Singer R (1986) The agaricales in modern taxonomy. Koenigstein
Singer R, Kuthan J (1980) Comparison of some lignicolous white-
spored American agarics with European species. C
ˇeska
´Mykol
34(2):57–73
Stalpers JA (1978) Identification of wood-inhabiting Aphyllophorales
in pure culture. Stud Mycol 16:1–248
Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood based
phylogenetic analyses with thousands of taxa and mixed models.
Bioinformatics 22:2688–2690
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S
(2011) MEGA5: molecular evolutionary genetics analysis using
maximum likelihood, evolutionary distance, and maximum
parsimony methods. Mol Biol Evol 28(10):2731–2739
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W:
improving the sensitivity of progressive multiple sequence
alignment through sequence weighting, position-specific gap
penalties and weight matrix choice. Nucl Acids Res
22:4673–4680
132 Fungal Diversity (2018) 90:109–133
123
Author's personal copy
Tortic
´M (1981) Schulzer’s polypores from Slavonia (Croatia,
Yugoslavia). Acta Bot Croat 40:183–199
Velenovsky
´J (1934) Monographia discomycetum bohemiae. Prague
Vilgalys R, Hester M (1990) Rapid genetic identification and
mapping of enzymatically ampliWed ribosomal DNA from
several Cryptococcus species. J Bacteriol 172:4238–4246
Vizzini A, Ercole E (2012) Paralepistopsis gen. nov. and Paralepista
(Basidiomycota, Agaricales). Mycotaxon 120:253–267
Vizzini A, Musumeci E, Murat C (2010) Trichocybe, a new genus for
Clitocybe puberula (Agaricomycetes, Agaricales). Fungal Divers
42:97–105
Vizzini A, Contu M, Ercole E (2011) Musumecia gen. nov. in the
Tricholomatoid clade (Basidiomycota, Agaricales) related to
Pseudoclitocybe. Nord J Bot 29:1–7
Vizzini A, Ercole E, Contu M (2012) A contribution to the ITS-LSU
phylogeny of the genus Leucopaxillus (Tricholomatoid clade,
Agaricales), with three new genera and notes on Porpoloma.
Mycosphere 3(1):79–90
Walther G, Garnica S, Weiß M (2005) The systematic relevance of
conidiogenesis modes in the gilled Agaricales. Mycol Res
109:525–544
White TJ, Bruns TD, Lee S, Taylor JW (1990) Amplification and
direct sequencing of fungal ribosomal RNA genes for phyloge-
netics. In: Innis MA, Gelfand DH, Sninsky J, White TJ (eds)
PCR protocols: a guide to methods and applications. Academic,
San Diego
Fungal Diversity (2018) 90:109–133 133
123
Author's personal copy