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Persoonia 38, 2017: 38–57
www.ingentaconnect.com/content/nhn/pimj http://dx.doi.org/10.3767/003158517X693174
RESEARCH ARTICLE
INTRODUCTION
The genus Tricholoma is a classic genus of agarics already pro-
posed as a section by Fries (1821) and subsequently erected
as a genus by Staude (1857).
Over the years more than 850 species epithets have been pu-
blished or combined in the genus. Many of these have since
been transferred to other genera, including Lepista, Leucopaxil-
lus, Lyophyllum and Melanoleuca based on various deviations,
mainly in microscopic characters. Molecular studies have sup-
ported the segregation of most of these more modern genera,
and Tricholoma in its narrow circumscription (e.g. Noordeloos
& Christensen 1999) is supported as a monophyletic genus of
ectomycorrhizal fungi within the Tricholomataceae (e.g. Mon-
calvo et al. 2002). According to Ryberg & Matheny (2012), the
genus seems to have segregated from its ancestral clade some
60–90 million years ago in the late Cretaceous, possibly with
Pinaceae as mycorrhizal partners. A recent study (Sánchez-
García et al. 2014) surveyed in depth the Tricholomataceae
based on several molecular markers and concluded that only
the genera Albomagister, Corneriella, Dennisiomyces, Leuco-
paxillus, Pseudotricholoma, Porpoloma s.str. and Tricholoma
belong to the family, while other previously contained genera
should be assigned to families, including the Lyophyllaceae
and a poorly resolved residual Tricholomatoid clade. Of the
genera included in the Tricholomataceae, also Porpoloma
s.str. is proven ectomycorrhizal, while a biotrophic lifestyle is
indicated to be probable in Albomagister and Pseudotricho-
loma. Only the latter genus is known to occur in Europe, were
Pseudotricholoma metapodium is widespread.
Tricholoma has a worldwide distribution (Tedersoo et al. 2010),
but seems to be most prominent in temperate and subtropical
zones in both the southern and northern hemisphere. All known
species are known or supposed to be ectomycorrhizal (Ryberg
& Matheny 2011), mainly with trees in the Pinaceae, Betulaceae
and Fagaceae, but the genus also contains species that are
associated with Eucalyptus, Dryas and Helianthemum (Bougher
1996, Christensen & Heilmann-Clausen 2013). Some species
form dual ectomycorrhizal and monotropoid associations linking
trees and monotropoid plants (Leake et al. 2004). The centre
of species richness appears to be in North America. According
to Bessette et al. (2013), more than 100 species are reported
from this continent while 63 to 88 species are listed from Eu-
rope (Riva 1988, Bon 1991, Kirby 2012). Several species are
described or reported from Japan, New Zealand and Australia
(e.g. Hongo 1988, Bougher 1996, Orlovich & Cairney 2004), but
the overview of the species diversity in these regions is frag-
mentary due to the lack of modern comprehensive treatments.
Tricholoma species show limited microscopic variation, and are
characterized by hyaline, subglobose to oblong spores, simple
pileipellis structures and lack of well-differentiated sterile ele-
ments, including cystidia. Hence, species identification and
partly also the infrageneric classification has mainly been
based on macromorphology. Singer (1986) divided the genus
in four subgenera, mainly based on pileipellis structure and
the presence or absence of clamp connections. The four sub-
genera were further divided into nine sections, of which three
(Leucorigida, Iorigida and Adusta) do not belong to the genus
in the current circumscription. In their treatment of the genus,
Noordeloos & Christensen (1999) accepted the four subgenera
suggested by Singer (1986), but with a more narrow definition
of sections, especially in subg. Tricholoma, in which seven sec-
Taxonomy of Tricholoma in northern Europe based on
ITS sequence data and morphological characters
J. Heilmann-Clausen1, M. Christensen2, T.G. Frøslev3, R. Kjøller 4
1 University of Copenhagen, Natural History Museum of Denmark, Center
for Macroecology, Evolution and Climate, Universitetsparken 15, DK-2100
Copenhagen, Denmark;
corresponding author e-mail: jheilmann-clausen@snm.ku.dk.
2 Hvidtjørnevej 1, DK-4180 Sorø, Denmark.
3 University of Copenhagen, Natural History Museum of Denmark, Center
for Geogenetics, Øster Voldgade 5-7, 1350 Copenhagen, Denmark.
4 University of Copenhagen, Institute of Biology, Section of Terrestrial Ecol-
ogy, Universitetsparken 15, DK-2100 Copenhagen, Denmark.
Key words
Agarics
biogeography
cryptic species
ectomycorrhizal fungi
host selection
morphological traits
phylogeny
Tricholomataceae
Abstract Based on molecular and morphological data we investigated the taxonomy and phylogeny of the ecto-
mycorrhizal genus Tricholoma in northern Europe. Our phylogenetic tree confirmed the presence of at least 72
well circumscribed species within the region. Of these, three species, viz. T. boreosulphurescens, T. bryogenum
and T. ilkkae are described as new to science, based on morphological, distributional, ecological and molecular
data. Several other terminal branches represent putative cryptic taxa nested within classical species or species
groups. Molecular type studies and/or designation of sequenced neotypes are needed in these groups, before
the taxonomy can be settled. In general our phylogenetic analysis supported previous suprageneric classification
systems, but with some substantial changes. Most notably, T. virgatum and allies were found to belong to sect.
Tricholoma rather than sect. Atrosquamosa, while T. focale was found to be clearly nested in sect. Genuina rather
than in sect. Caligata. In total, ten sections are accepted, with five species remaining unassigned. The combination
of morphological and molecular data showed pileus colour, pileipellis structure, presence of clamp connections and
spore size to be rather conservative characters within accepted sections, while the presence of a distinct ring, and
especially host selection were highly variable within these.
Article info Received: 23 January 2015; Accepted: 12 May 2016; Published: 26 August 2016.
39
J. Heilmann-Clausen et al.: Tricholoma in northern Europe
tions were accepted. Slightly deviating classification systems
have been proposed by other authors, including Bon (1984a,
1991). For a more throughout evaluation see Riva (1988) and
Christensen & Heilmann-Clausen (2013).
Despite their attractive fruit bodies, and a long mycological tradi-
tion, the overall taxonomy in Tricholoma is still poorly resolved in
Europe. Molecular data have been used to study the taxonomy
and phylogeny of some species groups (e.g. Comandini et al.
2004, Jargeat et al. 2010, Ota et al. 2012, Moukha et al. 2013),
typically resulting in the identification of cryptic diversity within
previously accepted species. Simultaneously, several species
have been proposed in recent years without a published test
of taxonomic placement based on molecular markers (e.g.
Kalamees 2001, Musemeci & Contu 2008, Ferrarese & Zaf-
falon 2010, Ludwig 2012), adding to taxonomic confusion in
the genus.
Recently, Christensen & Heilmann-Clausen (2013) monograph-
ed the genus in northern Europe, backed by sequences of the
nuclear ribosomal internal transcribed spacer (ITS). The main
objective of the present paper is to present the results of the
underlying scientific studies in a coherent form, with the fol-
lowing specific aims:
1. to evaluate the monophyly of proposed subgenera and sect-
ions as defined by Singer (1986) and Noordeloos & Chris-
tensen (1999);
2. to investigate the congruence between ITS and morphology
in hypothesized sections; and
3. to resolve the taxonomical delimitation of Tricholoma spe-
cies occurring in northern Europe, with a consideration of
possibly related taxa occurring in other continents, espe-
cially North America.
MATERIALS AND METHODS
Studied material
Specimens studied for this paper were mainly collected by the
first two authors during collection trips throughout Europe, since
the early 1990s. It was the intention to obtain representative col-
lections of all species present in northern Europe according to
modern identification books (Gulden 1969, 1992, Noordeloos &
Christensen 1999, Christensen & Heilmann-Clausen 2012), but
in addition a number of species recorded from southern Europe
were included. Generally, several collections of each species
were included in the analysis, and if possible, specimens from
different geographical regions were selected. In addition to
own material we have studied a number of collections, inclu-
ding type-specimens from various public and private herbaria
throughout Europe, and for the phylogenetic analyses selected
relevant and trustworthy ITS sequences were downloaded
from GenBank and Unite. Finally, we included a few original
ITS sequences kindly provided by Tor Erik Brandrud (Norway)
and Sven-Gunnar Ryman (Sweden).
Scoring of morphological characters
Macromorphological characters were mainly scored on fresh
material or more rarely photographs (for details on studied
collections see Christensen & Heilmann-Clausen 2013). Mor-
phological characters were described according to the standard
terminology published by Knudsen & Vesterholt (2008), while
colours were recorded according to Kornerup & Wanscher
(1974). Microscopical characters were recorded from rehydrated
specimens in 2 % KOH or 5–10 % NH3. From each collection a
minimum of 20 randomly selected spores were measured, avoi-
ding obviously malformed or unripe spores. For this study, data
on pileus and gill colour, pileus surface texture, presence of
a ring-zone, spore size and the presence/absence of clamp
connections were explored in more detail, but many other
characters were described for accepted species in Christensen
& Heilmann-Clausen (2013).
Molecular & phylogenetic methods
DNA was extracted from dried specimens by the CTAB-chloro-
form method described by Gardes & Bruns (1993). Usually,
one lamella was taken with a flamed pair of forceps from the
specimens. The internal transcribed spacer (ITS) region was
amplified with the primer combination ITS1-F and ITS4 (White
et al. 1990, Gardes & Bruns 1993). The PCR products were se-
quenced by Europhins Genomics (previously MWG-Biotech) or
Macrogen (www.macrogen.com). Forward and reverse strands
were sequenced using ITS1F or ITS5 (White et al. 1990) and
ITS4 as sequencing primers. If sequencing of either the ITS-1
or ITS-2 region proved difficult, additional sequencing was
performed using ITS2 and ITS3 (White et al. 1990) as sequen-
cing primers. Sequence contigs were assembled using Se-
quencher (v. 3.1). Alignment was done with MAFFT (online v. 7)
using the settings G-INS-i (Katoh et al. 2005), with minor manual
adjustments in Se-Al (Rambaut 1996) for some sequences
with incomplete ends or internal gaps. Two alignments were
produced, one containing all sequences in the dataset, and one
based on a reduced dataset containing only one representative
of each of 72 end-clusters accepted to represent described or
putative species present in northern Europe. For each align-
ment Maximum Likelihood phylogeny estimates were produced
with RAxML v. 8.1.16 (Stamatakis et al. 2008) with 1 000 fast
bootstrap replicates and GTR + CAT base substitution model.
Both alignments were also subjected to bayesian phylogenetic
analyses using MrBayes v. 3.2 (Ronquist et al. 2011) using
the GTR+I+gamma model (nst = 6, rates = invgamma) with
two independent runs of 4 chains for 5 000 000 generations
with sampling every 1 000th generation. Trees from the last
1 000 000 generations from each run (2 000 trees from each
analysis) were summed in a consensus tree with branch fre-
quencies corresponding to bayesian posterior probabilities.
Sequences used in this study are listed in Table 1 including
source information, geographic origin, and accession numbers.
Alignments can be obtained from the first author.
TAXONOMIC PART
In total we obtained 217 novel ITS sequences for this study,
while 84 published sequences were downloaded from GenBank
(67) and Unite (17). The alignment contained 170 unique se-
quence reads, represented as terminal clusters in the phyloge-
netic tree based on maximum likelihood (Fig. 1). The Bayesian
analyses did not contradict the ML phylogeny. Based on tree
topology these were assigned to 108 putative species hypo-
theses, of which 27 were represented only by extra-continental
sequences, while seven represented accepted species or spe-
cies hypotheses only recorded from southern Europe. Of the
81 species hypotheses identified among European sequences,
72 were selected for scoring of morphological characters and
evaluation of previously published infrageneric classification
systems (Fig. 2).
Below we first evaluate the infrageneric classification system,
and subsequently the species level taxonomy is reviewed. We
have applied commonly used section names as practical labels
for clades in order to guide readers. We have not intended to
resolve the nomenclatural history of each section in depth,
as this would require a deeper and quite time-consuming no-
menclatural study on candidate section names. As long as the
details of the infrageneric classification remain open, due to
limited sapling of the genus in North America, and the use of
only one molecular marker, we find the time unripe to perform
40 Persoonia – Volume 38, 2017
Hypsizygus marmoreus HM561970 Malaysia GenBank HM561970 Outgroup
T. ‘Sp. Mex1’ AB510472 Mexico GenBank AB510472
T. acerbum AF377247 Norway GenBank AF377247
JV99-638 1999 Denmark, Jylland, Elbæk Skov This study C C-F-41483 UDB001474 LT000005
MC00-204 2000 Slovenia, Central Slovenia, Vino This study C C-F-96223 UDB002361 LT000134
T. aestuans JV02-540 2002 Denmark, Jylland, Sønder Herreds Plantage This study C C-F-40955 UDB000779 LT000006
MC94-008 1994 Denmark, Jylland, Hårup Sande This study C C-F-59265 LT000007
MC97-072 1997 Sweden, Medelpad, Harrån This study C C-F-58885 UDB001434 LT000153 neotype
T. ‘ aff. sejunctum’ JN021102 Canada, Ontario GenBank JN021102
T. ‘ aff. virgatum’ MC05-201 2005 Nepal, Mustang, Kunjo This study C C-F-96250 UDB002370 LT000115
T. albobrunneum MC99-060 1999 France, Provence This study C C-F-96268 UDB001444 LT000077
UDB001218 Sweden Unite UDB001218
UDB018044 Estonia Unite UDB018044
T. album MC01-201 2001 Slovenia, Ljubljana This study C C-F-96234 UDB001413 LT000135
MC95-159 1995 Denmark, Jylland, Skivum Krat This study C C-F-96254 LT000008
UDB011580 Estonia Unite UDB011580
T. anatolicum AB510358 Turkey GenBank AB510358
AB699646 Morocco GenBank AB699646
T. apium JHC95-049 1995 Sweden, Medelpad, Borgsjö, Bergåsen SÖ This study C C-F-35189 UDB001467 LT000154
JV00-215 2000 Denmark, Jylland, Skagen Klitplantage This study C C-F-41884 UDB001685 LT000009
MC98-034 1998 Norway, Hedmark, Hornmoen This study C C-F-59207 LT000118
T. argyraceum JHC95-112 1995 Denmark, Sjælland, Geel Skov This study C C-F-35092 UDB000780 LT000010
JHC96-244 1996 Denmark, Sjælland, København, Botanisk Have This study C C-F-96212 UDB000781 LT000011
JHC97-092 1997 Sweden, Värmland, Långban S of Lesjöfors This study C C-F-96213 UDB000782 LT000155
JHC97-174 1997 Sweden, Medelpad, Bräcke, Grötingen This study C C-F-96215 UDB001692 LT000156
MC03-251 2003 Slovakia, Presov, Snina This study C C-F-96245 UDB001419 LT000127
MEN9491 1994 The Netherlands, Groningen, Verhildersum near Leens This study L L0374886 UDB000785 LT000198 epitype
T. arvernense MC95-102 1995 Sweden, Medelpad, Borgsjö This study C C-F-59014 LT000157
MC98-020 1998 Norway, Hedmark, Hornmoen This study C C-F-59200 UDB002362 LT000119
MC98-120 1998 France, Franche-Comte, St. Sifolene This study C C-F-59255 UDB001438 LT000078
T. ‘atrosquamosum’ AF349701 USA, Califonia GenBank AF349701
T. atrosquamosum O-F159872 2005 Norway, Hordaland, Granvin, Urdanes NR This study O O159872 LT222019
O-F188799 2003 Norway, Møre og Romsdal, Norddal This study O O188799 LT222024
O-F64018 2010 Norway, Buskerud, Øvre Eiker, Gommerud, Vestfossen This study O O-64018 LT000120
TEB55008 2008 Norway, Aust-Agder, Evje & Hornnes, Dåsvassdalen, Husefjell SW This study TEB LT222031
T. ‘atroviolaceum’ AY750166 USA, Washington GenBank AY750166
T. ‘aurantium’ AF377233 USA, Califonia GenBank AF377233
T. aurantium MC96-303 1996 Italy, Toscana, Cipressa di Agnese This study C C-F-59329 UDB001470 LT000100
MC97-227 1997 Denmark, Møn, Møns Klint This study C C-F-59330 UDB001471 LT000012
T. ‘bakamatsutake’ AB036898 Japan GenBank AB036898
AB856037 Japan GenBank AB856037
T. basirubens MC01-209 2001 Croatia, Primorsko-Goranska, Krk This study C C-F-96240 LT000001
TL5303 1998 Sweden, Öland, Halltorps Haga This study C C-F-38408 LT000158
T. batschii AF377238 USA, Califonia GenBank AF377238
MC01-200 2001 Croatia, Istarska, Kanegra This study C C-F-96233 UDB001412 LT000002
UDB011587 Estonia Unite UDB011587
T. bonii AM181413 Estonia GenBank AM181413
JHC91-721 1991 Denmark, Anholt This study C C-F-96201 UDB000811 LT000013
LUG-F8450 1996 Italy, Probe Brallo, Pavia This study LUG LUG F 8450 UDB000790 LT000101 holotype
MEN96112 1996 Italy, Trento, Spera val Campanella This study L L0354472 UDB000791 LT000102
T. boreosulphurescens IK971187 1997 Finland, Outer Ostrobothnia, Tervola, Peura, Raemäki This study H H6002040 LT000199
JF908737 Finland GenBank JF908737
Table 1 Sequences included in this study. For sequences retrieved from genbank or unite, only accession numbers and country of origin is given, for new sequences obtained for this study, year of collection, locality and fungarium
data is given. Species names are given as in Fig. 1.
Species Voucher Collection Locality Origin of Herbarium Herbarium no. Unite GenBank Notes
year sequence accession no. accession no.
41
J. Heilmann-Clausen et al.: Tricholoma in northern Europe
T. boreosulphurescens (cont.) SAE9507 1995 Sweden, Medelpad, Stöde, V. Västansjö, Kockerabäcken This study C C-F-59441 UDB001475 LT000159
TROM-F21089 2007 Norway, Troms, Storfjord, Lullesletta This study TROM OF21089 LT222032
O-F187683 2004 Norway, Finnmark, Alta, Kålfjordsbotten This study O O187683 LT222023 holotype
T. borgsjoeënse JHC95-067 1995 Sweden, Medelpad, Borgsjö, Julåsen This study C C-F-96211 LT000160
JV95-307 1995 Sweden, Medelpad, Borgsjö, Julåsen This study C C-F-96219 UDB000807 LT000161
TEB22606 2006 Norway, Oppland, Nord-Aurdal, Mjølkebekken nordre This study TEB LT222030
T. boudieri MC01-600 2001 Slovenia, Ljubljana This study C C-F-90092 LT000136 epitype
MC95-317 1995 Denmark, Jylland, Moesgaard Skov This study C C-F-59305 UDB001428 LT000014
T. bresadolanum CL94-166 1994 Sweden, Öland, Haltorp Hage This study C C-F-59442 UDB000792 LT000162
MC96-264 1996 Italy, Toscana, Monte Soldano This study C C-F-59341 UDB000549 LT000103
MC96-265 1996 Italy, Toscana, Monte Soldano This study C C-F-59342 UDB000550 LT000104
TRgmb00652 2006 Italy, Sardegna, Sassari, Calangianus, Baldo This study TR TRgmb00652 LT000105
T. bryogenum MC97-101 1997 Sweden, Jämtland, Brunflo This study C C-F-59167 AY462034 holotype
O-F160040 2006 Norway, Oppland, Øystre Slidre, Heggnes This study O OF160040 LT222020
O-F52108 1979 Norway, Nord-Trøndelag, Levanger, Ytterøya This study O OF52108 LT222026
TROM-F6702 1995 Norway, Troms, Storfjord, Lullesletta This study TROM OF6702 LT222034
T. ‘caligatum’ AF309520 Costa Rica GenBank AF309520
T. caligatum JV07-451 2007 Spain, Valencia, E of Gandía, N of Els This study LT000152
T. ‘caligatum’ KC152249 Mexico GenBank KC152249
T. caligatum KC565866 Algeria GenBank KC565866
PH99-519 1999 France, Provence This study C C-F-96274 UDB000793 LT000079
T. ‘cedrotorum’ MC99049 1999 France, Provence, Massif des Cedres This study C C-F-96265 UDB001442 LT000074
T. ‘ cf. japonicum’ JN021103 Canada, Quebec GenBank JN021103
T. cingulatum MC03-252 2003 Slovakia, Presov, Havesova This study C C-F-96246 UDB001420 LT000128
MC96-134 1996 Denmark This study C C-F-59057 UDB000543 LT000015 neotype
MC96-170 1996 Denmark, Jylland, Borum This study C C-F-59068 UDB000544 LT000016
MEN95210 1995 The Netherlands, Drenthe, Boekweitveentje This study L LT000200
T. colossus MC01-205 2001 Slovenia, Ljubljana This study C C-F-96238 UDB001417 LT000137
MC97-047 1997 Sweden, Jämtland, Ysjö This study C C-F-59154 UDB001433 LT000164
T. columbetta AF349693 Norway GenBank AF349693
MC95-181 1995 Denmark, Jylland, Skivum Krat This study C C-F-58898 UDB001468 LT000017 neotype
T. ‘dryophilum’ AF377239 USA, Califonia GenBank AF377239
T. dulciolens AB738883 Sweden GenBank AB738883 holotype
AF309523 USA, Califonia GenBank AF309523
JF908732 Italy GenBank JF908732
T. equestre MC94-027 1994 Denmark, Jylland, Hoverdal Plantage This study C C-F-58886 UDB001508 LT000018
MC95-187 1995 Denmark, Jylland, Hoverdal This study C C-F-96256 LT000019
MC96-155 1996 Denmark, Jylland, Bakkerne near Ørsted This study C C-F-58890 UDB001469 LT000020
T. filamentosum C-F35924 1996 Sweden, Skåne, Balsberget This study C C-F-35924 UDB001506 LT000165
JHC0-1202 2001 Slovenia, Ljubljana (exhibition) This study C C-F-96191 UDB000804 LT000138
MC00-218 2000 Slovenia, Gorizia, Idria This study C C-F-96226 LT000139
MC03-242 2003 Slovakia, Presov, Rozok This study C C-F-96243 UDB000803 LT000129
T. ‘flavovirens’ AB036895 Japan GenBank AB036895
AF458452 USA, Oregon GenBank AF458452
AF458453 USA, Oregon GenBank AF458453
AF458456 USA, Oregon GenBank AF458456
DQ822834 USA, California GenBank DQ822834
T. ‘focale’ AF309534 USA, Califonia GenBank AF309534
AF377236 USA, Califonia GenBank AF377236
T. focale JV97-239 1997 Sweden, Jämtland, Orrskäret This study C C-F-27500 UDB001501 LT000166 neotype
JV99-603 1999 Denmark, Læsø, Træbakke at Holtemmen This study C C-F-41444 UDB001500 LT000021
MC98-600 1998 Denmark, Jylland, Skagen This study C C-F-96260 UDB002364 LT000022
T. ‘frondosae’ MC98-086 1998 France, Franche-Comte, Winkel This study C C-F-59243 UDB001504 LT000075
T. frondosae type I AF349689 USA, New Mexico GenBank AF349689
MC95-130 1995 Sweden, Medelpad, Borgsjö This study C C-F-59031 LT000167
MC97-151 1997 Sweden, Jämtland, Fillstabäcken This study C C-F-59188 LT000168
T. frondosae type II MC00-225 2000 Slovenia, Gorizia, Idria This study C C-F-96227 LT000140
MC96-235 1996 Denmark, Jylland, Mols This study C C-F-59084 UDB001509 LT000023
42 Persoonia – Volume 38, 2017
T. frondosae type II (cont.) MC97-158 1997 Sweden, Jämtland, Kyckås This study C C-F-59395 UDB002363 LT000169
T. fucatum MC97-149 1997 Sweden, Jämtland, Fillstabäcken This study C C-F-58980 LT000170 neotype
MC98-023 1998 Norway, Hedmark, Sørskogbygdn This study C C-F-59201 LT000121
T. ‘fulvocastanem’ AB289668 Japan GenBank AB289668
DQ067895 Thailand GenBank DQ067895
T. fulvum JHC03-019 2003 Slovakia, Poloniny National Park, Nova Sedlica This study C C-F-96193 UDB001695 LT000130
JHC04-251 2004 Sweden, Halland, Varberg, Åkulla, Valaklitt This study C C-F-96195 UDB001700 LT000171
MC98-078 1998 France, Franche-Comte, Winkel This study C C-F-96259 UDB002365 LT000080
T. guldeniae JuV16997 2000 Finland, Varsinais-Suomi, Vahto, Seppälä, Ryssänvuori This study TURA UDB001701 LT000070
MC95-103 1995 Norway, Akershus This study C C-F-96251 LT000122
T. hemisulphureum JV08-364 2008 Estonia, Saaremaa This study C C-F-96217 LT000065
O-F74354 2005 Norway, Hordaland, Ulvik, Finse This study O O74354 LT222027
T. ‘huronense’ AF377229 USA, Califonia GenBank AF377229
T. ilkkae AB738881 Spain GenBank AB738881
AB738882 Spain GenBank AB738882
MC98-602 1998 Sweden, Gotland This study C C-F-96261 LT000172
S-F173364 2007 Sweden, Uppland, Gräsö par., Djupdal 3 km NE of Gräsö church This study UPS F-173364 LT222028
S-F513823 2000 Sweden, Gotland, Eksta par, Ekstastrand This study UPS F-513823 LT222029 holotype
T. ‘imbricatum’ AF377242 USA, Califonia GenBank AF377242
T. imbricatum MC94-046 1994 Denmark, Jylland, Bakkerne near Ørsted This study C C-F-59268 UDB001421 LT000024 neotype
UDB000699 Sweden Unite UDB000699
T. ‘inamoenum’ AF377246 USA, Califonia GenBank AF377246
T. inamoenum JHC95-042 1995 Sweden, Medelpad, Tubbobäcken This study C C-F-35182 UDB001688 LT000173 neotype
MC95-115 1995 Sweden, Medelpad, Borgsjö This study C C-F-59020 UDB001424 LT000174
T. inocybeoides JHC95-072 1995 Sweden, Medelpad, Borgsjö, Erikslund This study C C-F-35211 UDB000796 LT000175
MC03-229 2003 Denmark, Jylland, Århus This study C C-F-96242 UDB000783 LT000025
MC95-152 1995 Denmark, Jylland, Aarhus This study C C-F-59272 UDB000537 LT000026
MC96-172 1996 Denmark, Jylland, Aarhus This study C C-F-59094 UDB000538 LT000027
MC97-060 1997 Sweden, Jämtland, Østersund This study C C-F-59159 UDB000539 LT000176
T. ‘japonicum’ AB036900 Japan GenBank AB036900
T. ‘joachimii’ HM590876 France GenBank HM590876
T. joachimii MC98-603 1998 Sweden, Gotland This study C C-F-96262 LT000177
TRgmb00060 2005 Italy, Trento, Baselga di Piné, Cané This study TR TR gmb 00600 LT000106
T. ‘joachimii’ O-F167194 2004 Norway, Akershus, Bæarum, Borøya This study O O167194 LT222022
T. josserandii MC99-053 1999 France, Provence, Massif des Cedres This study C C-F-96266 UDB000797 LT000081
MC99-056 1999 France, Provence, Massif des Cedres This study C C-F-96267 UDB000798 LT000082
T. lascivum JHC03-020 2003 Slovakia, Poloniny National Park, Rozok This study C C-F-96194 UDB001696 LT000131
MC00-519 2000 Denmark, Sjælland, Rude Skov This study C C-F-96230 UDB000005 LT000028
MC99-197 1999 Denmark, Sjælland, Lellinge Skovhusvænge This study C C-F-59446 LT000029
T. ‘leucophyllum’ EU597086 Canada, British Columbia GenBank EU597086
JN021108 Canada, Ontario GenBank JN021108
T. ‘luteomaculosum’ AF458448 USA, Oregon GenBank AF458448
T. ‘magnivelare’ AF377224 USA, Califonia GenBank AF377224
T. matsutake AF309538 China, Yunnan GenBank AF309538
JuV23362F 2005 Finland, Koillismaa, Oulanka national park, NWW of biological field station This study TURA LT000071
MC03-600 2003 Sweden, Jämtland This study C C-F-96247 LT000178
TMU62964 South Korea GenBank TMU62964
T. ‘moserii’ AF377211 USA, Califonia GenBank AF377211
T. ‘mutabile’ AF458445 USA, Oregon GenBank AF458445
T. olivaceotinctum JHC95-070 1995 Sweden, Medelpad, Borgsjö, Julåsen This study C C-F-35209 UDB000526 LT000179
KJ1993 1993 Sweden, Lappland, Åsele Lappmark, Risbäck, S slope of arksjöberget This study S UDB000799 LT000180
MC95-135 1995 Sweden, Medelpad, Borgsjö This study C C-F-59036 UDB000527 LT000181
MC97-103 1997 Sweden, Jämtland, Brunflo This study C C-F-59168 UDB000525 LT000182
Table 1 (cont.)
Species Voucher Collection Locality Origin of Herbarium Herbarium no. Unite GenBank Notes
year sequence accession no. accession no.
43
J. Heilmann-Clausen et al.: Tricholoma in northern Europe
T. olivaceotinctum (cont.) OP1981 1981 Sweden, Jämtland, Sällsjö This study UPS UDB000800 LT000183
T. orirubens JHC01-200 2001 Slovenia, Idria, Mehke Dolina This study C C-F-96189 UDB000524 LT000141
JHC93-261 1993 Denmark, Jylland, Trelde Østerskov This study C C-F-96208 UDB000523 LT000030
MC03-243 2003 Slovakia, Presov, Rozok This study C C-F-96244 UDB000801 LT000132
MC96-301 1996 Italy, Toscana, Cipressa di Agnese This study C C-F-59365 UDB000522 LT000107
MC97-258 1997 Denmark, Jylland, Moesgaard Skov This study C C-F-59427 UDB000521 LT000031
MC98-214 1998 England, Surrey, Norbury Park This study C C-F-59315 UDB000520 LT000202
T. ‘palustre’ DQ494699 USA, Massachusetts GenBank DQ494699
T. pardinum JHC01-201 2001 Slovenia, Idria, Pringle This study C C-F-96190 UDB000802 LT000142
T. pessundatum JV04-482 2004 Denmark, Jylland, Ålbæk Klitplantage This study C C-F-43780 UDB001502 LT000032 epitype
UDB011581 Estonia Unite UDB011581
T. populinum MC00-236 2000 Slovenia, Gorizia, Idria This study C C-F-96229 UDB001410 LT000143
UDB011624 Estonia Unite UDB011624
T. portentosum AF349686 USA, Califonia GenBank AF349686
JHC04-431 2004 Sweden, Halland, Hylte, Ödegärdet This study C C-F-96197 UDB001698 LT000184
JHC92-277 1992 Denmark, Lolland, Christianssædeskovene This study C C-F-96202 UDB001686 LT000033
MC00-206 2000 Slovenia, Central Slovenia, Vino This study C C-F-96224 UDB001409 LT000144
MC94-082 1994 Denmark, Sjælland, Ordrup Næs This study C C-F-58959 LT000034
MC96-156 1996 Denmark, Jylland, Bakkerne near Ørsted This study C C-F-59053 UDB001429 LT000035 neotype
MC98-116 1998 France, Franche-Comte, Doubs, St.-Julien les Russey This study C C-F-59262 LT000083
T. psammopus MC04-600 2004 Slovenia, Ljubljana This study C C-F-96248 LT000145
MC96-345 1996 Italy, Toscana, Monte Soldano This study C C-F-59324 LT000108
MC98-048 1998 Denmark, Jylland, Fløjstrup Skov This study C C-F-59212 UDB001472 LT000036
MC99-089 1999 France, Provence This study C C-F-96273 UDB001503 LT000084
T. ‘quercetorum’ MC99-044 1999 Portugal, Leiria This study C C-F-96263 UDB000795 LT000125
T. ‘ramentaceum var. pseudotriste’ HQ184102 France GenBank HQ184102
T. rapipes MC03228 2003 Denmark, Jylland, Stråsø Plantage This study C C-F-96241 UDB001418 LT000037
MC98-106 1998 France, Franche-Comte, Doubs, St.-Julien les Russey This study C C-F-59258 UDB001439 LT000085 epitype
T. roseoacerbum IK881120 1988 Finland, Sompio Lapland, Sodankylä, Jeesiö-Tepsa This study H H6002032 LT000072
IK922945 1992 Finland, Uusimaa, Hanko, Koverhar, Krogars This study H H6002034 LT000073
T. rufenum MC96-376 1996 Italy, Lazio, Monte Rufenum This study C C-F-59393 UDB001432 LT000109
T. saponaceum C-F23337 1992 Denmark, Lolland, Ryde Skov This study C C-F-23337 UDB001499 LT000038
JHC00-049 2000 Norway, Sogn og Fjordane, Leikanger, Horpa This study C C-F-96188 UDB001693 LT000123
JHC03-015 2003 Poloniny National Park, Stuzika This study C C-F-96192 UDB001694 LT000133
JHC04-429 2004 Sweden, Halland, Hylte, Ödegärdet This study C C-F-96196 UDB001697 LT000185
JHC04-439 2004 Sweden, Halland, Laholm, Blåalt This study C C-F-96198 UDB001699 LT000186
JHC95-165 1995 Denmark, Sjælland, Sorø Sønderskov This study C C-F-35147 UDB001505 LT000039
JHC97-237 1997 Denmark, Sjælland, Frederikskilde Skov This study C C-F-96216 UDB001689 LT000040
JV87-682 1987 Denmark, Jylland, Fløjstrup Skov This study C C-F-96218 UDB001507 LT000041
MC98-059 1998 France, Franche-Comte, Foret de Leval This study C C-F-59217 LT000086
TF98-098 1998 France, Doubs, Forêt Valdahon This study C C-F-96276 UDB001498 LT000087
T. ‘saponaceum’ DQ494700 USA, Massachusetts GenBank DQ494700
T. scalpturatum JHC93-263 1993 Denmark, Jylland, Trelde Østerskov This study C C-F-96210 UDB000541 LT000042
JHC94-231 1994 Denmark, Fyn, Tankefuld W. of Svendborg This study C C-F-35309 UDB000542 LT000043
MC00-207 2000 Slovenia, Ljubljana This study C C-F-96225 LT000146
MC95-165 1995 Sweden, Jämtland, Sundsnäs This study C C-F-59399 LT000187 neotype
T. ‘scalpturatum forma meleagroides’ HQ184113 France GenBank HQ184113 holotype
T. ‘scalpturatum var. atrocinctum’ JHC93-243 1993 Denmark, Jylland, Nystrup Klitplantage This study C C-F-96206 UDB000784 LT000004
T. sciodes MC94-007 1994 Denmark, Jylland, Fløjstrup Skov This study C C-F-58902 UDB000547 LT000044
MC95-182 1995 Denmark, Jylland, Borum Skov This study C C-F-96255 UDB000548 LT000045
T. ‘sejunctum’ AB036899 Japan GenBank AB036899
AF377192 USA, Califonia GenBank AF377192
EU819447 USA, Wisconsin GenBank EU819447
T. sejunctum MC95-187 1995 Denmark, Jylland, Enemærket Skov This study C C-F-58998 LT000046
MC96-314 1996 Italy, Toscana, Cipressa di Agnese This study C C-F-58979 UDB001431 LT000110
T. squarrulosum JHC93-224 1993 Denmark, Jylland, Trelde Østerskov This study C C-F-96205 UDB000532 LT000047
JHC93-262 1993 Denmark, Jylland, Trelde Østerskov This study C C-F-96209 UDB000530 LT000048
JHC95-169 1995 Denmark, Sjælland, Lellinge Skovhusvænge This study C C-F-35151 UDB000786 LT000049
44 Persoonia – Volume 38, 2017
T. squarrulosum (cont.) MC01-202 2001 Croatia, Primorsko-Goranska, Krk This study C C-F-96235 UDB001414 LT000003
MC01-700 2001 Slovenia, Ljubljana This study C C-F-96239 UDB000528 LT000147
MC96-269 1996 Italy, Toscana, Monte Soldano This study C C-F-59343 UDB000531 LT000111
MC98-081 1998 France, Franche-Comte, Winkel This study C C-F-59238 UDB000529 LT000088
T. stans MC95-131 1995 Sweden, Medelpad, Borgsjö This study C C-F-59032 UDB001426 LT000188
MC95-145 1995 Sweden, Medelpad, Borgsjö This study C C-F-59042 UDB001427 LT000189 epitype
MC98-018 1998 Norway, Hedmark, Hornmoen This study C C-F-96258 LT000124
T. stiparophyllum MC95-117 1995 Sweden, Medelpad, Borgsjö This study C C-F-96252 LT000190
UDB002398 Scotland Unite UDB002398
UDB011582 Estonia Unite UDB011582
T. sudum JV96-306 1996 Denmark, Læsø, Læsø Klitplantage, Vester Højsandshoved This study C C-F-96221 UDB001684 LT000050
MC98-601 1998 Denmark, Jylland, Råbjerg Plantage This study C C-F-90094 UDB002366 LT000051 neotype
T. sulphurescens clade 1 MC96-296 1996 Italy, Toscana, Cipressa di Agnese This study C C-F-59362 UDB000809 LT000112
MC99-063 1999 France, Provence This study C C-F-96269 UDB002367 LT000089
T. sulphurescens clade 2 TRgmb00062 2005 Italy, Trento, Baselga del Bondone This study TR TR gmb 00062 LT000113
UDB011543 Estonia Unite UDB011543
T. ‘sulphureum’ AF377244 USA, Califonia GenBank AF377244
EU819448 USA, Wisconsin GenBank EU819448
HQ650743 Canada, British Columbia GenBank HQ650743
T. sulphureum clade 1 JHC08-049 2008 Sweden, Halland, Halmstad, Nissaström This study C C-F-96200 LT000191
MC96-245 1996 Denmark, Jylland, Øjesø This study C C-F-59115 AY462037
T. sulphureum clade 2 JHC07-236 2007 Denmark, Lolland, Favrsted Skov This study C C-F-96199 LT000053
MC01-204 2001 Slovenia, Ljubljana This study C C-F-96237 UDB001416 LT000148
MC07-001 2007 Sweden, Skåne, Drakamöllan This study Missing LT000192
MC94-023 1994 Denmark, Jylland, Kås Hoved This study C C-F-58914 AY462036
MC95-188 1995 Denmark, Jylland, Enemærket Skov This study C C-F-59292 AY462038
MC96-162 1996 Denmark, Jylland, Løvenholm Skov This study C C-F-59062 AY462035
MC98-109 1998 France, Franche-Comte, Doubs, St.-Julien les Russey This study C C-F-59260 UDB001440 LT000090
O-F288529 2008 Norway, Oppland, Vang, Uri This study O OF288529 LT222025
TROM-F30019 1996 Norway, Troms, Storfjord, Lullesletta This study TROM OF30019 LT222033
T. sulphureum clade 3 AF377245 Norway GenBank AF377245
TF06045 2006 France, Doubs, Forêt de Levier This study C C-F-96275 LT000091
T. ‘terreum’ EU439339 China, Yunnan GenBank EU439339
EU439340 China, Yunnan GenBank EU439340
T. terreum JHC93-260 1993 Denmark, Jylland, Trelde Østerskov This study C C-F-96207 UDB000536 LT000057
JHC95-118 1995 Denmark, Sjælland, Kongelunden This study C C-F-35098 LT000058
JHC95-172 1995 Denmark, Sjælland, København, Assistens Kirkegård This study C C-F-35154 UDB000812 LT000059
MC01-020 2001 Slovenia, Ljubljana This study C C-F-96232 UDB001411 LT000149
MC05-200 2004 Nepal, Mustang, Lete This study C C-F-96249 UDB002368 LT000116
MC95-119 1995 Sweden, Medelpad, Borgsjö This study C C-F-96253 UDB001425 LT000193
MC98-209 1998 Holland, Schouwen-Duiveland This study C C-F-59313 UDB000533 LT000201
MC99-071 1999 France, Provence, Foret des Caderach This study C C-F-96271 UDB001445 LT000092
MC99-074 1999 France, Provence, Foret des Caderach This study C C-F-96272 UDB001446 LT000093
MEN95192 1995 Germany, Bayern, Sperberslohe near Roth This study L L0374887 UDB000813 LT000098 epitype
O-F165767 2005 Norway, Oppland, Lunner, Grua, Olsknappen This study O O165767 LT222021
TL11317 1993 Denmark, Jylland, Klim Bjerg This study C C-F-96277 UDB000808 LT000060
T. terreum (albinistic) JHC93-222 1993 Denmark, Jylland, Trelde Østerskov This study C C-F-96204 UDB000534 LT000061
JV95-519 1995 Denmark, Jylland, Staksrode Skov This study C C-F-96220 UDB000535 LT000062
T. ‘tridentinum’ JV99-700 1999 France, Provence, Petit Luberon, Massif des Cedres This study C C-F-96222 UDB000805 LT000076
T. triste E3754 1996 Germany, Baden-Württemberg, Seedorfer Wald, Schwarzwald This study L UDB000814 LT000099 neotype
JHC97-169 1997 Sweden, Jämtland, Lockna, W. of Änge This study C C-F-96214 UDB001691 LT000194
JuV5271F 1990 Estonia, Pärnu rajooni, c. 40 km S of Pärnu, Kabli This study TURA LT000066
T. ‘ulvinenii’ IK931613 1993 Finland, Satakunta, Jämijärvi, Hämeenkangas This study H H6002036 LT000067
Table 1 (cont.)
Species Voucher Collection Locality Origin of Herbarium Herbarium no. Unite GenBank Notes
year sequence accession no. accession no.
45
J. Heilmann-Clausen et al.: Tricholoma in northern Europe
T. ‘ulvinenii’ (cont.) JuV13229F 1997 Finland, Varsinais-Suomi, Dragsfjärd, Ölmos This study TURA LT000068
JuV26740F 2008 Finland, Satakunta, Alastaro, Virttaankangas This study TURA LT000069
UDB011557 Estonia Unite UDB011557
UDB011558 Estonia Unite UDB011558
UDB011559 Estonia Unite UDB011559
T. umbonatum type I MC00A01 2000 Denmark, Lolland, Roden Skov This study C C-F-96231 UDB002369 LT000063
T. umbonatum type II TRgmb00651 2006 Italy, Veneto, Belluno, Meleré This study TR TRgmb00651 LT000114
T. ustale AF377234 The Netherlands GenBank AF377234
JHC92-299 1992 Denmark, Sjælland, Suserup Skov This study C C-F-96203 UDB000551 LT000064
T. ‘ustaloides’ AF377240 USA, Califonia GenBank AF377240
T. ustaloides MC99-047 1999 Portugal, Leiria This study C C-F-96264 UDB000816 LT000126
MC99-067 1999 France, Provence, Foret des Caderach This study C C-F-96270 UDB000815 LT000094
UDB011564 Estonia Unite UDB011564
T. vaccinum MC00-229 2000 Slovenia, Gorizia, Idria This study C C-F-96228 UDB001511 LT000150
MC95-109 1995 Sweden, Medelpad, Borgsjö This study C C-F-59017 UDB001423 LT000195
T. ‘venenatum’ AF377230 USA, Califonia GenBank AF377230
T. virgatum JHC95-063 1995 Sweden, Medelpad, Björnö, Björkviken This study C C-F-35203 UDB000546 LT000196
MC01-203 2001 Slovenia, Ljubljana This study C C-F-96236 UDB001415 LT000151
MC97-164 1997 Sweden, Jämtland, Halåsen This study C C-F-59398 UDB000545 LT000197 neotype
T. viridilutescens type I MC98-061 1998 France, Franche-Comte, Bois de la Brosse This study C C-F-59219 UDB001436 LT000095
MC98-080 1998 France, Franche-Comte, Winkel This study C C-F-59237 UDB001473 LT000096
MC98-093 1998 France, Franche-Comte, Bois Lachat This study C C-F-59249 UDB001437 LT000097
T. viridilutescens type II UDB011588 Estonia Unite UDB011588
UDB011595 Estonia Unite UDB011595
T. ‘viridiolivaceum’ MC96-002 1996 New Zealand, Arthurs Pass National Park This study C C-F-96257 LT000117
‘Uncultured ectomycorrhiza’ FJ197008 Mexico GenBank FJ197008
such a study. In the section on species level taxonomy nomen-
clatural details are given on all species epithets.
Infrageneric classification and congruence with
morphology
The phylogenetic analysis did not support a clear division of
the genus in four subgenera as proposed by Singer (1986)
and adopted by most subsequent authors. However, ten sec-
tions could be reasonably separated based on molecular data
and scoring of morphological traits (Fig. 2), with some species
remaining unclassified. Pileus colour, pileipellis structure,
pre sence of clamp connections and spores size and shape
appeared as rather constant characters supporting the validity
of sections, while the presence of a distinct ring, and especially
host selection was variable within sections. It is well known that
the ITS region alone is poorly suited for resolving higher level
phylogenies (e.g. Frøslev et al. 2005), and our infrageneric
classification should be viewed as phylogenetic supported, but
preliminary. However, we do trust the sections defined below
as relevant hypothetical monophyletic entities that should be
tested in future studies combining a global taxon sampling with
multiple molecular markers.
Species with a greyish, radially fibrillose, squamulose to
felty cap
Species with a dry, grey and a radially fibrillose, squamulose
to felty pileipellis quite clearly represent a paraphyletic group,
that we here split across four sections; Terrea, Atrosquamosa,
Tricholoma and Pardinicutis (Fig. 2). Section Terrea contains
species characterized by a dry, felty or squamulose pileipellis,
predominantly greyish colours, and spores with a relatively high
Q-value. Our concept of the section is narrow, and corres ponds
to stirps Terrea in Singer (1986). Most previous authors, includ-
ing Noordeloos & Christensen (1999) operated with a much
broader concept of the section, which included also the stirps
Virgata and Atrosquamosa ss. Singer (1986). Here, we accept
the latter as a separate section, although our ITS phylogeny
provide only limited support for monophyly, especially in the
maximum likelihood analysis (Fig. 2). The similarity in morpho-
logical traits of the assigned species is, however, striking. Spe-
cies in the section are morphologically very similar to species
in sect. Terrea, but tend to have spores with a higher Q-value,
and are characterized by peculiar smells reminding of honey,
ground pepper or cedar wood (compared to absent to farina-
ceous in sect. Terrea). The species belonging to stirps Virgata
in the sense of Singer (1986) (i.e. T. aestuans, T. bresadolanum,
T. sciodes and T. virgatum) were in our analysis deeply nested
in sect. Tricholoma. As discussed later, this makes good sense
morphologically. Finally, our analysis supported sect. Pardini-
cutis as a separate section. The members of this section are
characterized by a grey, scaly pileipellis, large spores and the
presence of clamp connections, a combination that has lead
most modern authors to accept Pardinicutis at the subgenus
level.
Species with a reddish brown cap
For the reddish brown species our ITS phylogeny showed a
division in three relatively well-supported sections, sect. Cali-
gata, sect. Genuina and sect. Megatricholoma (Fig. 2). The
members of sect. Caligata are characterized by an annulate
stipe, a whitish, pale brown to dark reddish brown squamose
pileus, rather large spores with low Q-value, and a strong per-
fumed smell. All European species are associated with conifers,
but according to Murata et al. (2013) basal members of the clade
from other parts of the world associate with deciduous hosts.
The annulate species T. focale has traditionally been included
in the section (e.g. Noordeloos & Christensen 1999), but the
current study shows it to be deeply nested in sect. Genuina,
46 Persoonia – Volume 38, 2017
Fig. 1 Phylogeny inferred from ITS regions for the full dataset, with branch lengths based on the Maximum Likelihood analysis. No notable differences in
branching patterns were observed between the Bayesian and the Maximum Likelihood analysis. Maximum Likelihood bootstrap values are indicated above
branches, while Bayesian posterior probabilities are indicated below branches. * Denotes 100 % support in both analyses. New sequences obtained for this
study are indicated in regular letters, while sequences obtained from GenBank or Unite are given in italics. Species names without quotes represent our in-
terpretation of relevant taxa as discussed in this paper. Names in quotes are not interpreted by us, but are given as in the original source, or by the collector.
Hypothesized sections are indicated by background shadings with names in capital letters.
UDB011543_sulphurescens type II_EE
JV08-364_hemisulphureum_EE
MC03-229_inocybeoides_DK
MC99-071_terreum_FR
MC05-200_terreum_NEPAL
TROM-F6702_bryogenum_NO
TROM-F30019_sulphureum type II_NO
MC95-115_inamoenum_SE
EU439340_"terreum"_CHINA
AF377245_sulphureum type III_NO
O-F288529_sulphureum type II_NO
JHC95-112_argyraceum_DK
MC01-200_terreum_SI
JHC95-042_inamoenum*_SE
JHC93-260_terreum_DK
MC95-152_inocybeoides_DK
MC97-060_inocybeoides_SE
AF377244_"sulphureum"_USA
MC01-201_album_SI
MC94-023_sulphureum type II_DK
MC95-119_terreum_SE
AF377246_"inamoenum"_USA
MC98-109_sulphureum type II_FR
UDB002398_stiparophyllum_UK
MC96-172_inocybeoides_DK
JuV5271F_triste_EE
MC03-251_argyraceum_SK
HQ184113_"scalpturatum f. meleagroides”_FR
E3754_triste*_DE
MC95-165_scalpturatum*_SE
MC03-242_filamentosum_SK
SAE9507_boreosulphurescens_SE
JHC97-169_triste_SE
JHC01-202_filamentosum_SI
MC99-063_sulphurescens type I_FR
JHC95-072_inocybeoides_SE
JHC01-201_pardinum_SI
HQ184102_"ramentaceum var. pseudotriste*”_FR
AF377230_"venenatum"_USA
MEN95192_terreum*_DE
MC95-159_album_DK
JHC93-263_scalpturatum_DK
JHC95-172_terreum_DK
MC00-519_lascivum_DK
JHC03-020_lascivum_SK
MC96-162_sulphureum type II_DK
O-F160040_bryogenum_NO
JHC94-231_scalpturatum_DK
MC00-207_scalpturatum_SI
EU819448_"sulphureum"_USA
MC98-209_terreum_NL
MC99-197_lascivum_DK
JV95519_terreum(albinistic)_DK
MC97-101_"bryogenum"_SE
MC07-001_sulphureum type II_SE
HQ650743_"sulphureum"_CANADA
AY750166_"atroviolaceum"_USA
JHC93-243_"scalpturatum var. atrocinctum”_DK
JHC97-092_argyraceum_SE
MEN96112_bonii_IT
JHC08-049_sulphureum type I_SE
AF377229_"huronense"_USA
JHC95-118_terreum_DK
MEN95210_cingulatum_NL
O-F74354_hemisulphureum_NO
JHC97-174_argyraceum_SE
MC95-188_sulphureum type II_DK
MC99-074_terreum_FR
MC03-252_cingulatum_SK
MC01-204_sulphureum type II_SI
JHC96-244_argyraceum_DK
JHC91-721_bonii_DK
EU439339_"terreum"_CHINA
JHC95-067_borgsjoeense_SE
JHC07-236_sulphureum type II_DK
AF377211_"moserii"_USA
MEN9491_argyraceum*_NL
O-F52108_bryogenum_NO
O-F187683_boreosulphurescens*_NO
UDB011580_album_EE
UDB011582_stiparophyllum_EE
JHC93-222_terreum(albinistic)_DK
MC95-117_stiparophyllum_SE
JF908737 _boreosulphurescens_FI
TF0 6045 _sulphureum type III_FR
TROM-F21089_boreosulphurescens_NO
MC96-296_sulphurescens type I_IT
TRgmb00062_sulphurescens type II_IT
MC96-134_cingulatum*_DK
IK971187_boreosulphurescens_FI
LUG F 8450_bonii*_IT
AM181413_bonii_EE
MC9 6-245_ sulphureum type I_DK
O-F-165767_terreum_NO
MC96-170_cingulatum_DK
C-F35924_filamentosum_SE
TEB22606_”borgsjoeensi”s_NO
MC00-218_filamentosum_SI
TL11317_terreum_DK
JV95-307_borgsjoeense_SE
52
0.69
69
0.89
89
1
*
91
1
99
1
99
1
76
1
98
1
32
0.56
75
0.99
96
1
80
1
TERREA
PARDINICUTIS
LASCIVA S.STR.
SERICELLA
LASCIVA P.P.
0.05
99
1
93
1
*
84
1
51
0.74
*
*
*
*
*
*
*
*
*
*
*
95
1
*
*
*
*
*
*
*
*
47
J. Heilmann-Clausen et al.: Tricholoma in northern Europe
Fig. 1 (cont)
UDB011559_"ulvinenii"_EE
JuV26740F_"ulvinenii"_FI
AF349689_frondosae type I_USA
JN021102_"aff_sejunctum"_CANADA
JuV16997_guldeniae_FI
JN021108_"leucophyllum"_CANADA
MC95-187_”equestre”_DK
JuV13229F_"ulvinenii"_FI
DQ494699_"palustre"_USA
O-F167194_"joachmii"_NO
UDB011558_"ulvinenii"_EE
MC05-201_"aff_virgatum"_NEPAL
MC00-225_frondosae type II_SI
MC01-203_virgatum_SI
AF349686_portentosum_USA
HM590876_"joachimii"_FR
MC95-187_sejunctum_DK
AF458456_"flavovirens"_USA
MC96-265_bresadolanum_IT
AF377192_"sejunctum"_USA
JHC04-431_portentosum_SE
AB036899_"sejunctum"_JAPAN
MC95-182_sciodes_DK
CL94-166_bresadolanum_SE
AF349693_columbetta_NO
TRgmb00651_umbonatum type II_IT
AB036895_"flavovirens"_JAPAN
TRgmb00060_joachimii_IT
MC94-008_aestuans_DK
MC96-264_bresadolanum_IT
MC98-080_viridilutescens type I_FR
AF458453_"flavovirens"_USA
MC96-156_portentosum*_DK
MC94-082_portentosum_DK
MC95-181_columbetta*_DK
MC96-235_frondosae type II_DK
EU597086_"leucophyllum"_CANADA
DQ822834_"flavovirens"_USA
MC94-027_equestre_DK
UDB011588_viridilutescens type II_EE
EU819447_"sejunctum"_USA
MC98-116_portentosum_FR
UDB011557_"ulvinenii"_EE
MC97-158_frondosae type II_SE
MC98-603_joachimii_SE
MC97-151_frondosae type I_SE
MC96-314_sejunctum_IT
MC98-093_viridilutescens type I_FR
TRgmb00652_bresadolanum_IT
UDB011595_virdilutescens type II_EE
MC94-007_sciodes_DK
IK931613_"ulvinenii"_FI
MC00-A01_umbonatum type I_DK
MC96-155_equestre_DK
JV02-540_aestuans_DK
MC98-086_"frondosae"_FR
MC95-103_guldeniae_NO
MC97-072_aestuans*_SE
AF458452_"flavovirens"_USA
MC00-206_portentosum_SI
MC98-061_viridilutescens type I_FR
JHC95-063_virgatum_SE
MC97-164_virgatum*_SE
MC96-376_rufenum_IT
MC95-130_frondosae type I_SE
JHC92-277_portentosum_DK
53
0.93
95
1
87
0.99
22
0.59
45
0.57
66
1
65
0.9
38
0.6
67
0.96
89
1
97
1
45
0.84
35
0.85
68
0.99
94
1
62
1
0.05
MC03-600_matsutake_SE
MC98-023_fucatum_NO
MC99-056_josserandii_FR
AB699646_anatolicum_MOROCCO
AF309538_matsutake_CHINA
AB289668_"fulvocastaneum"_JAPAN
AF377224_"magnivelare"_USA
AF309520_"caligatum"_COSTA RICA
TMU62964_matsutake_SOUTH KOREA
MC98-602_ilkkae_SE
AB856037_"bakamatsutake"_JAPAN
AF458445_”mutabile”_USA
JV07-451_caligatum_ES
AB5 103 58_anatolicum_TR
JF908732_dulciolens_IT
AB510472_"Sp. Mex1”_MEXICO
S-F173364_ilkkae_SE
JuV23362F_matsutake_FI
S-F513823_ilkkae*_SE
DQ067895_"fulvocastaneum"_THAILAND
AB738881_ilkkae_SP
AF309523_dulciolens_USA
AB738882_ilkkae_SP
AB738883_dulciolens*_SE
MC99-053_josserandii_FR
KC152249_"caligatum"_MEXICO
AB036898_"bakamatsutake"_JAPAN
KC565866_caligatum_ALGERIA
MC97-149_fucatum*_SE
PH99-519_caligatum_FR
95
1
86
1
90
0.97
73
1
59
0.99
71
0.98
CALICATA
TRICHOLOMA
*
*
*
*
*
99
1
99
1
*
*
*
99
1
*
92
1
64
0.96
88
1
95
1
86
0.98
*
96
1
83
0.96
82
1
**
88
1
*
61
0.96
*
*
*
*
*
*
*
*
*
91
1
82
1
41
0.47
48 Persoonia – Volume 38, 2017
Fig. 1 (cont)
UDB011564_ustaloides_EE
IK922945_roseoacerbum_FI
MC95-131_stans_SE
AF377240_"ustaloides"_USA
JHC04-251_fulvum_SE
AF377242_"imbricatum"_USA
UDB011581_pessundatum_EE
AF377233_"aurantium"_USA
MC96-303_aurantium_IT
JV99-638_acerbum_DK
JHC95-049_apium_SE
MC00-236_populinum_SI
MC97-047_colossus_SE
MC98-048_psammopus_DK
MC95-145_stans*_SE
UDB011624_populinum_EE
MC98-020_arvernense_NO
MC97-227_aurantium_DK
MC99-067_ustaloides_FR
FJ197008_"Uncult._ectom_MEXICO
MC98-034_apium_NO
MC99-060_albobrunneum_FR
JV99-700_"tridentinum"_FR
MC98-120_arvernense_FR
AF309534_"focale"_USA
MC00-204_acerbum_SI
AF377239_"dryophilum"_USA
AF458448_"luteomaculosum"_USA
AB036900_"japonicum"_JAPAN
UDB018044_albobrunneum_EE
MC98-018_stans_NO
JV99-603_focale_DK
MC01-205_colossus_SI
MC99-047_ustaloides_PT
AF377234_ustale_NL
JHC92-299_ustale_DK
MC95-102_arvernense_SE
IK881120_roseoacerbum_FI
JV04-482_pessundatum*_DK
MC95-109_vaccinum_SE
UDB001218_albobrunneum_SE
MC99-044_"quercetorum"_PT
MC99-089_psammopus_FR
JV97-239_focale*_SE
MC00-229_vaccinum_SI
MC94-046_imbricatum*_DK
MC99-049_"cedrotorum"_FR
MC96-345_psammopus_IT
JN021103_"cf. japonicum_CANADA
MC98-078_fulvum_FR
UDB000699_imbricatum_SE
JHC03-019_fulvum_SK
MC98-600_focale_DK
AF377247_acerbum_NO
MC04-600_psammopus_SI
JV00-215_apium_DK
85
1
33
0.72
44
0.89
99
1
26
0.62
52
0.9
63
0.89
95
1
25
0.93
AF377236_”focale”_USA
MC01-200_batschii_HR
UDB011587_batschii_EE
AF377238_batschii_USA
JHC93-261_orirubens_DK
MC03-228_rapipes_DK
JHC95-070_olivaceotinctum_SE
MC01-600_boudieri*_SI
MC96-301_orirubens_IT
MC97-258_orirubens_DK
MC98-106_rapipes*_FR
MC98-214_orirubens_UK
JHC03-015_saponaceum_SK
JHC00-049_saponaceum_NO
JV87-682_saponaceum_DK
MC98-059_saponaceum_FR
OP1981_olivaceotinctum_SE
JHC04-429_saponaceum_SE
TF98098_saponaceum_FR
MC97-103_olivaceotinctum_SE*
JHC93-262_squarrulosum_DK
MC95-317_boudieri_DK
JHC01-200_orirubens_SI
JHC97-237_saponaceum_DK
JHC93-224_squarrulosum_DK
DQ494700_"saponceum"_USA
O-F188799_atrosquamosum_NO
HM561970_Hypsizygus_marmoreus (outgroup)
O-F159872_atrosquamosum_NO
TL5303_basirubens_SE
MC96-002_"viridiolivaceum"_NEW ZEALAND
MC98-081_squarrulosum_FR
MC95-135_olivaceotinctum_SE
KJ1993_olivaceotinctum_SE
AF349701_"atrosquamosum"_USA
MC96-269_squarrulosum_IT
MC01-700_squarrulosum_SI
MC03-243_orirubens_SK
MC98-601_sudum*_DK
MC01-209_basirubens_HR
TEB55008_atrosquamosum_NO
JHC04-439_saponaceum_SE
MC01-202_squarrulosum_HR
O-F64018_atrosquamosum_NO
JHC95-165_saponaceum_DK
JV96-306_sudum_DK
JHC95-169_squarrulosum_DK
C-F23337_saponaceum_DK
98
100
92
1
83
1
90
0.99
74
0.99
0.05
ATROSQUAMOSA
CONTEXTOCUTIS
MEGATRICHOLOMA
GENUINA
99
1
88
0.95
60
0.82
37
0.85
44
0.91 49
0.84
*
*
99
1
72
1
*
98
1
38
0.73
41
0.62
*
*
96
0.94
41
0.6
80
0.93
54
0.84
*
*
*
69
1
*
*
*
73
0.97
95
100
91
100
*
*
49
J. Heilmann-Clausen et al.: Tricholoma in northern Europe
close to the subannulate T. batschii (Fig. 2). The species lack
a perfumed smell and has no broad scales on the pileus so this
makes sense morphologically. Section Megatricholoma was
originally erected as a monotypic genus to accommodate
T. colossus (Kost 1984). Based on detailed morphological and
ontological studies the genus was by its author suggested to
be only distantly related to Tricholoma s.str., a view that was
challenged by Christensen & Noordeloos (1999) who recom-
bined Megatricholoma as a section in Tricholoma. Our study
supports this disposition, and gives reasonable support for the
inclusion of T. acerbum and T. roseoacerbum in the section
(Fig. 2). In the preliminary phylogeny presented in Christensen
& Heilmann-Clausen (2013) there was no support for this, but
the broader taxon sampling and more careful alignment in the
current analysis has changed this. All three species share a very
robust and short stipe, close lamellae, and an involute pileus
margin, but T. colossus stands apart by its annulate stipe, and
large spores. Section Genuina in our circumscription include
species with a reddish brown and glutinous pileipellis, as well
as several species with paler brown colours and/or a dry squa-
mulose pileus. Noordeloos & Christensen (1999) divided these
in sect. Imbricata (with a dry fibrillose to squamulose pileipel-
lis) and sect. Albobrunnea (with glutinous pelipellis). Both are
moderately well supported in our ITS phylogeny, but at present
we prefer to treat them as entities below the section level.
Species with a smooth, white to yellowish cap
Species with a smooth, white to yellowish, dry pileipellis and
presence of clamp connections were divided across four clades
in our tree, which we here assign to three sections; Contex-
tocutis, Sericella and Lasciva (Fig. 2). Members of sect. Con-
textocutis are characterized by reddening flesh, a soapy odour,
greenish to greyish colours and small spores, and the section
has long been recognized as a separate entity, often at the
subgenus level (e.g. Singer 1986, Noordeloos & Christensen
1999). In contrast most previous authors have not separated
Sericella and Lasciva at the section level (e.g. Bon 1984a,
Singer 1986, Riva 1988, Noordeloos & Christensen 1999).
However, Bon (1984a) and Riva (1988) distinguished two
subsections, Sulphurea (corresponding to our sect. Sericella)
and Lasciva. Our analysis do not suggest the two sections to
be closely related, and they are morphologically well differen-
tiated. Thus, species in sect. Sericella are characterized by
very large spores, a strong gas-like odour and white to yellow
colours, while members of sect. Lasciva have small spores,
initially whitish to yellowish grey pileus colours, and a strong,
complex odour combining aromatic flowery, gas-like and rancid
components. A single member of sect. Sericella, i.e. T. inamoe-
num, was by Noordeloos & Christensen (1999) assigned to a
separate sect. Inamoena, but our analysis clearly shows this
section to be redundant. The species assigned to sect. Lasciva
is in our analysis divided among two terminal clades (Fig. 2),
one containing species with non-yellowing context close to
T. lascivum, the other species with yellowing context. Based
on morphological similarities, we expect that future multigene
phylogenies will show the two clades to be more closely related
than our current analysis proposes, and at present we prefer
to keep sect. Lasciva as a single taxonomic unit.
Species with a radially fibrillose, whitish, greyish, greenish or
yellow cap
The great majority of species characterized by an innately
fibrillose to squamulose pileipellis and whitish, greyish, green-
ish or yellow colours, were joined in one terminal clade in our
tree. These are here assigned to sect. Tricholoma in accord-
ance with Noordeloos & Christensen (1999). The T. equestre
group including T. columbetta and T. umbonatum form a well-
supported core clade. Tricholoma columbetta has traditionally
been assigned to the separate sect. Albata (e.g. Noordeloos
& Christensen 1999), but this is not supported by our analysis.
Two less well-supported subclades are formed by T. sejunctum
and allied species, and by sect. Virgata in the sense of Singer
(1986) with T. portentosum taking up an intermediate position.
Tricholoma guldeniae appears to be the most deviant and basal
member of the section. We previously did not consider it as
a member of this section (Christensen & Heilmann-Clausen
2013), but our current phylogenetic analysis gives reasonable
support for its inclusion.
For five species, viz. T. apium, T. avernense, T. borgejoensis,
T. fucatum and T. josserandii, our analysis do not support a
clear assignment to traditionally accepted sections (Fig. 1, 2),
and appear to represent deviant lineages. These species are
discussed further in the next section.
Species level taxonomy
Below we give an overview of the accepted sections, and their
circumscribed species accepted by us to occur in northern
Europe. We compare our results with earlier studies and com-
ment on further taxa revealed by the analysed ITS data. For
further details on the ecology, morphology and practical differ-
entiation of discussed taxa we refer to Christensen & Heilmann-
Clausen (2013).
Section Terrea
Our detailed phylogenetic tree supports the presence of
seven well-differentiated terminal clades in this section, viz.
T. argyraceum, T. cingulatum, T. scalpturatum, T. inocybeoides,
T. terreum, T. bonii and T. triste (Fig. 1). All of these are known
from northern Europe. Many authors (e.g. Huijsman 1968,
Krieglsteiner 1982, Clémençon 1983, Riva 1988) accepted
T. gausapatum and T. myomyces as distinct species close to
T. terreum, differing by small differences in pileipellis struc-
ture, veil development and colouration. Based on our quite
intensive sampling, we have found no congruence between
variation in these traits and ITS phylogeny, and we doubt that
T. gausapatum and T. myomyces as typically interpreted auct.
are taxonomically different from T. terreum. Also material fitting
with T. leucoterreum show no ITS difference to typical T. ter-
reum, and we interpret this taxon to represent an albinistic form
of T. terreum. In fact, albinism seems to be rather common in
the section, with albinistic forms and varieties described also
in T. cingulatum and T. scalpturatum (Hermosilla & Sánchez
1994, Bidaud & Thévenard 2003). Also T. bonii was originally
described as a species with whitish colours (Basso & Candusso
1997), but the type shows 100 % ITS sequence similarity
with collections with greyish pileus colours. The taxonomy
and phylogeny of the species group around T. argyraceum
was studied in great detail by Jargeat et al. (2010) using
three molecular markers. The study found very consistent
phylogenies for all markers, supporting the clear delimitation
of T. argyraceum, T. inocybeoides, T. cingulatum and T. scalp-
turatum as biological species. Especially T. argyraceum was
shown to encompass forms and varieties described to differ
in colouration from pure white to strongly coloured. Two re-
cently described species from Europe, T. urbicum and T. dis-
tantifoliaceum, have been assigned to the section. They are
unknown to us, and type-material should be sequenced to
compare their relatedness to more classical species. Tricholoma
moseri described from North America clearly also belongs to
this section, and is close to or even conspecific with T. triste,
as suggested by our ITS analysis. Both species share small
fruit bodies and very long elongate spores. Based on ITS data
T. triste is also present in China, which is also the case for
T. bonii (Fig. 1).
50 Persoonia – Volume 38, 2017
0.05
Hypsizygus_marmoreus
rapipes
josserandii
focale
roseoacerbum
triste
sulphurescens type II
colossus
saponaceum
squarrulosum
filamentosum
orirubens
fulvum
bresadolanum
imbricatum
sulphureum type II
sulphurescens type I
viridilutescens type I
hemisulphureum
aestuans
virgatum
arvernense
umbonatum type II
lascivum
boudieri
basirubens
albobrunneum
cingulatum
album
olivaceotinctum
inocybeoides
joachimii
atrosquamosum
batschii
bonii
inamoenum
sudum
columbetta
apium
boreosulphurescens
scalpturatum
vaccinum
ustaloides
terreum
virdilutescens type II
caligatum
portentosum
aurantium
sulphureum type III
borgsjoëense
argyraceum
sulphureum type I
sejunctum
fucatum
ilkkae
dulciolens
stiparophyllum
psammopus
frondosae type II
populinum
frondosae type I
guldeniae
matsutake
equestre
umbonatum type I
sciodes
bryogenum
acerbum
ustale
pessundatum
”ulvinenii”
pardinum
stans
56
0.83
80
62
0.99
98
1
95
1
72
0.99
63
0.98
97
1
71
90
0.99
Cap Colour
Gill Colour
Ring/velum
2
Pileus surface
3
Spore size
Clamps
Host selection
1
?
?
TERREA
LASCIVA P.P.
ATROSQUAMOSA
CONTEXTOCUTIS
?
?
?
MEGATRICHOLOMA
GENUINA
PARDINICUTIS
LASCIVA S.STR.
?
?
?
SERICELLA
CALIGATA
TRICHOLOMA
?
Subg. Tricholoma Subg. Sericeicutis Subg. pardinicutis Subg. Contextocutis
1Host selection: : Deciduous, : Coniferous, : Coniferous and deciduous, : (within other symbols), Specific host genus
Legends:
2Ring/velum: : Pseudonannular zone, : Cobwebby, : Membranous, : Cottony to skin like
3Pileus surface: : Glutinuous, : Dry, : (within other symbols), Squarrulose : (within other symbols), Squamose,
: (within other symbols), Radially fibrillose
10 μm
basirubens
squarrulosum
olivaceotinctum
atrosquamosum
orirubens
0.96
1
0.65
*
*
51
J. Heilmann-Clausen et al.: Tricholoma in northern Europe
Section Atrosquamosa
Our analysis supports the presence of five well-circumscribed
European species in this section, viz. T. atrosquamosum, T. ori-
rubens, T. basirubens, T. squarrulosum and T. olivaceotinctum
(Fig. 1). The European species fall in two distinct clades with
T. squarrulosum and T. orirubens as central species, respec-
tively. As discussed thoroughly by Christensen & Heilmann-
Clausen (2009) we use the name T. atrosquamosum differently
than done by Noordeloos & Christensen (1999), and apply it
for a taxon close to T. orirubens, but mainly associated with
conifers and lacking yellow mycelia. Conversely T. basirubens,
that was first described as a variety to T. orirubens (Bon 1975),
is closely related to T. squarrulosum based on our data. The
section appears to be well represented, but poorly resolved in
North America. Tricholoma michinganense clearly belongs to
this section but appears to be poorly represented in modern
literature. Bessette et al. (2013) presented three photographs
labelled as T. squarrulosum, which appear to be somewhat
deviant from our concept of this species, based on the slender
stipe and occurrence under conifers. The included American
sequence labelled as ‘T. atrosquamosum’ in our tree, is clearly
deviant from included European taxa, but it is unknown if it cor-
responds to T. michinganense or T. squarrulosum in the sense
of Bessette et al. (2013).
Section Pardinicutis
Our analysis supports five species in this section (Fig. 1), of
which only two, i.e. T. filamentosum and T. pardinum, are known
with certainty from Europe. Bon (1991) included a number of
additional taxa in his treatment of the section, including T. tumi-
dum, T. cookeanum and T. cedrorum, the latter two being
described from Morocco. All are unknown to us. At least three
North American taxa are described in this section, viz. T. hu-
ronense, T. venenatum and T. vernaticum. Our tree supports
the two former as distinct species, assuming that the two se-
quenced specimens have been correctly labelled.
Section Caligata
Our analysis supports at least ten species in this section (Fig.
1), of which only two are known to occur in northern Europe,
viz. T. matsutake and T. dulciolens. Two further species, viz.
T. caligatum and T. anatolicum occur in southern Europe or
adjacent regions. Kytövuori (1988) made a careful taxonomic
treatment of the section in Europe, and described T. dulciolens
as new to science based on collections from Fennoscandia,
while T. anatolicum was recently described from Cedrus forests
in Turkey (Intini et al. 2003). This species has since been re-
corded from Morocco (Ota et al. 2012), and might well occur in
southern Europe. A fifth species, T. ilkkae, is here described as
new to science. It has long been known from the Swedish island
of Gotland in the Baltic Sea, but has been identified as either
T. dulciolens or T. caligatum. Tricholoma ilkkae share small
spores with the first mentioned species, and general coloura-
tion with the latter, so the confusion is not surprising. ITS data,
however, show that T. ilkkae is clearly differentiated from both
species, showing most affinity to T. dulciolens. We have stud-
ied material of the species only from Sweden, but have seen
photographs of the species from Norway, and ITS sequence
data show that it is also present in Spain (Murata et al. 2013)
and Turkey (unpubl. data from Nicklas Bergius). Most likely it
is widely distributed but rare in Europe. Quite likely, Armillaria
caligata forma gracilis represent an earlier synonym, but as the
name has not been combined in Tricholoma or proposed at the
species level, it has limited nomenclatural relevance.
The global phylogeny of the section has been studied rather
intensively (Chapela & Garbelotto 2004, Ota et al. 2012, Murata
et al. 2013, Gulden et al. 2014). These studies show T. mat-
sutake (possibly as a species complex) to be present in both
Europe, Asia and North America, while T. dulciolens so far is
confirmed from Europe and North America. The other recog-
nized species appear to be restricted to smaller biogeographic
regions, i.e. T. anatolicum, T. caligatum and T. ilkkae to Europe
(including adjacent North Africa and Asia Minor), T. bakamat-
sutake, T. fulvocastaneum to eastern Asia and T. magnivelare
and at least two undescribed lineages (one denoted as ‘Mexican
magnivelare’ in Gulden et al. (2014), and one or two labelled
as T. caligatum) in Chapela & Garbelotto (2004), to North
America. These taxa are represented in our dataset, as ‘T. sp.
Mex1.’ from Mexico and ‘T. caligatum’ from Mexico and Costa
Rica, respectively.
Section Genuina
Our analysis supports the presence of at least 18 species
in this section in Europe, which fall in two more or less well-
supported subclades (Fig. 1).
The largest subclade contains species with reddish brown col-
ours and a glutinous pileipellis, i.e. T. focale, T. batschii, T. pes-
sundatum, T. populinum, T. stans, T. aurantium, T. albobrun-
neum, T. fulvum, T. ustale and T. ustaloides, all known from
northern Europe. Many authors have accepted T. pseudonicti-
tans as a separate species close to T. fulvum, but differing by
less pronounced yellow tinges in the gills and flesh of the
stipe, and by the association with conifers. Our ITS data do
not support this separation (JHC04-251 and MC98-078 were
collected under Picea and Abies, respectively, while JHC03-109
was collected under Betula), and hence we treat T. pseudo-
nictitans as a synonym to T. fulvum (see also Christensen &
Heilmann-Clausen 2013). On the other hand, collections from
southern Europe identified as T. cedretorum and T. quercetorum
appear to represent distinct species based on ITS, but we have
studied too little material and literature to have any opinion on
the correct nomenclatural judgments regarding these. Further
European taxa characterized by a reddish brown and glutinuous
pileus include T. tridentinum, T. ustale var. rufoaurantiacum,
T. ustaloides var. aurantiodes and T. ezcarayense. The latter
taxon, T. ezcarayense, however possesses clamp connections
(Hermosilla & Sánchez 1994), which are otherwise absent in
the section and is probably unrelated. The North American
sequences included in the tree suggest that T. aurantiacum,
T. batschii, T. focale and T. stans are present also on this con-
tinent, with T. zelleri and T. dryophilum being potential synonyms
to the two latter species. In contrast, the included American
sequence assigned to T. ustaloides represents a distinct taxon
not closely related to our concept of this species. Judging from
photos and descriptions in Bessette et al. (2013) T. muricatum,
T. pudorinum ined. and T. transmutans are further North Ameri-
can taxa in this group, with T. fulvum, T. pessundatum, T. po-
pulinum and T. ustale being also recorded as North American.
Grubisha et al. (2012) investigated the phylogeography of T. po-
pulinum in Scandinavia and North America, and found no signs
←
Fig. 2 Phylogeny inferred from ITS regions for a reduced dataset, based on representative sequences for 72 well-circumscribed species or species hypoth-
eses. Branch lengths and branching patterns are based on the Maximum Likelihood analysis. Branching patterns were similar in the Bayesian analysis, except
for sect. Atrosquamosa, were the alternative configuration is shown as an insert. Maximum Likelihood bootstrap values are indicated above branches, while
Bayesian posterior probabilities are indicated below branches for proposed sections indicated with background shadings and names in capital letters. * Denotes
100 % support in both analyses. Coloured bars show the affiliation to subgenera in the sense of Singer (1986). Host selection and six different morphological
traits are scored using different symbols, to illustrate their distribution across the phylogeny, and to the proposed sections.
52 Persoonia – Volume 38, 2017
of recent intercontinental gene flow in this specific partner of
Populus spp. Based on the molecular clock approach they
estimated divergence between European and American popula-
tions to have happened between 1 and 1.7 million years ago.
A smaller, and slightly less well-supported subclade contain
species with a dry, squamulose pileus. Our analysis include
only three European species in this group, viz. T. psammopus,
T. vaccinum and T. imbricatum, but Moreau (2011) presented
and discussed two additional central-European taxa, viz. T. in-
odermeum and T. subfusipes. Both appear to be well delimited
species, close to T. imbricatum and T. vaccinum, respectively,
but with slightly different macroscopic characters (Moreau 2011)
and deviant ITS data (P.-A Moreau pers. comm.). Ecologically,
T. subfusipes differs from T. imbricatum by being associated with
Larix rather than Pinus. A third species, T. pseudoimbricatum,
described from Denmark is by us regarded as a synonym to
T. imbricatum (for details see Christensen & Heilmann-Clausen
2013). The included North American sequence of T. imbricatum
is quite deviant from the two European sequences, and might
represent a distinct species. Both T. imbricatum and T. vaccinum
are illustrated with several photographs from various American
states in Bessette et al. (2013). The variation in colouration,
stature and pileipellis structure is quite striking, and suggests
the presence of several additional species on the continent.
Section Megatricholoma
This relatively well-supported section was not accepted in
Christensen & Heilmann-Clausen (2013) but as mentioned
above the present analysis has lead us to treat it in a wider
sense than done previously, by including the non-annulate spe-
cies T. acerbum and T. roseoacerbum beside the types species
T. colossus. Thus, our con cept of the section includes three well
known species in Europe (Fig. 1, 2), with T. robustum represent-
ing a tentative fourth, badly known member (see Christensen &
Heilmann-Clausen 2013). Tricholoma roseoacerbum appears
to be remarkably widely distributed, with almost perfect ITS
sequence matches connecting collections and environmental
samples from Finland, Japan, Canada and Mexico. Tricholoma
japonicum probably represents the oldest valid name for this
species, with T. radotinense representing a further potential
synonym. Also T. manzanitae described from North America
belongs to this group, judging from the presentation in Bessette
et al. (2013).
Section Sericella
This section contains six well-separated European end-
clusters in our tree. Two additional sequences appear to re-
present distinct taxa occurring in Canada and the USA (Fig.
1). Across continents, only three of these can be assigned to
well-known species, i.e. T. inamoenum, T. hemisulphureum
and T. sulphureum, while a forth, T. bryogenum is described as
new to science in this paper. Already Comandini et al. (2004)
reported the presence of cryptic diversity within the section,
but mainly concluded that T. bufonium, described to differ from
T. sulphureum by more reddish to purplish pileus colours,
could not be readily separated from T. sulphureum. Our studies
partly confirm pileus colours to be poorly suited to differenti-
ate taxa within the section (Christensen & Heilmann-Clausen
2013), but we are not convinced that the cryptic taxa detected
by the phylogenetic analysis are truly indistinguishable from
T. sulphureum s.str. The colours of the lamellae and basal
mycelium appear to be promising characters in this respect,
but we also expect differences in ecology and biogeography.
At least this is the case for T. bryogenum that differs from
T. sulphureum s.lat. by its habitat in boreal coniferous forests,
the dull yellow colours and the whitish basal mycelium. No
modern type exists of T. sulphureum, and hence it remains
unknown which of the three additional lineages in our tree
corresponds to T. sulphureum s.str. Hence they are labelled
as type I to III in correspondence with Comandini et al. (2004)
and Christensen & Heilmann-Clausen (2013). A large number
of varieties have been described in T. sulphureum (see Bon
1991 for an overview). Some of these might correspond to the
presently cryptic species in our tree. According to our phylo-
genetic tree, T. inamoenum occurs also in North America, at
least based on ITS data. Another species from this continent
that clearly belongs to this section is T. odorum.
Section Contextocutis (= section Rigida)
This section contains at least four European taxa in our
tree, viz. T. saponaceum, T. sudum, T. rapipes (comb. nov.)
and T. boudieri (Fig. 1, 2). Of these, the two latter are normally
not differentiated from T. saponaceum at the species level,
but we find that differences in morphology and ITS sequence
data warrant their distinguishing. A large number of further
varieties have been described in the section, mainly based on
pileus colours and surface texture of the stipe (see Bon 1991).
Our studies indicate that these characters are quite plastic
characters with limited taxonomic relevance (Christensen &
Heilmann-Clausen 2013). Based on the collections studied
by us, T. saponaceum and T. boudieri are associated with
deciduous hosts, while T. rapipes and T. sudum are associ-
ated with conifers (Christensen & Heilmann-Clausen 2013).
We are far from convinced that these preferences are strict,
and await future studies testing host selection and taxonomy
in the group. Our current analysis indicates that our concept of
T. boudieri could cover more than one species, and we would
not be surprised if more dedicated studies would prove the exis-
tence of additional species in the section in Europe. The two
included extralimital sequences from New Zealand and North
America represent further independent species in the section,
which judging from the photographs given in Besseette et al.
(2013) contains several different species in North America.
Section Lasciva
In our tree this section is split across two subclades, containing
a total of five species (Fig. 1, 2) in northern Europe, viz. T. lasci-
vum, T. album, T. stiparophyllum, T. sulphurescens and T. boreo-
sulphurescens. The latter is described as new to science in this
paper. A sequence labelled a T. sulphurescens from Estonia,
appears to represent a further, undescribed species. The taxo-
nomy of the section was discussed in detail by Christensen &
Noordeloos (1999) who neotypified T. lascivum, T. album and
T. stiparophyllum. Tricholoma albidum and T. farinaceum in the
sense of Bessette et al. (2013) appear to represent North
American members of this section.
Section Tricholoma
This section contains at least 13 species in northern Europe,
viz. T. virgatum, T. sciodes, T. bresadolanum, T. aestuans, T. por-
tentosum, T. sejunctum, T. viridilutescens, T. equestre, T. fron-
dosae, T. joachimii, T. columbetta, T. umbonatum and T. gul-
deniae, but several included subclades have complex ITS
sequence patterns, and remain poorly resolved in our tree.
This is especially the case in the T. equestre group, but also
T. sejunctum/viridilutescens and T. umbonatum represent spe-
cies complexes based on our phylogeny. The complex phylo-
geny of T. equestre s.lat. was noted previously by Horton (2002)
based on North American specimens, and have been confirmed
by subsequent studies, dealing with the group across the north-
ern hemisphere (Moukha et al. 2013). Even before molecular
phylogenies were available, a number of taxa were proposed
but often synonymized in this group, with T. equestre, T. aura-
tum and T. flavovirens representing classical names. Kala mees
(2001) studied the group based on ecological and morpho-
53
J. Heilmann-Clausen et al.: Tricholoma in northern Europe
logical characters. He described two new species, T. fron-
dosae and T. ulvinenii, and at the same time assigned T. aura-
tum and T. flavovirens as synonyms to T. equestre. The study
was not supported by molecular sequences, and unfortunately
we have been unsuccessful in our attempts to extract DNA from
the types of the two new species. In our analysis collections
labelled as T. frondosae form three groupings in the tree, but
we are quite convinced that T. frondosae type I match the type,
as all collections have been characterized by warm colours
and small spores as emphasized in the diagnosis. Tricholoma
frondosae type II have larger spores and more greenish colours
and seem to represent an undescribed species. A further col-
lection from France (MC98-086) is only distantly related to the
T. equestre core group based on ITS data.
Collections labelled as T. ulvinenii fall in two distinct clusters
within the poorly resolved core T. equestre clade, and it is un-
known if any of these represent the type concept of this species.
Collections identified as T. ulvinenii by Kuulo Kalamees (viz.
UDB011557–UDB011559) are separated on both groups, indi-
cating them to be difficult to separate based on morphological
characters. In our simplified overview tree (Fig. 2) T. ulvinenii
is represented by the upper terminal clade containing four col-
lections labelled with this name, and illustrated in Christensen
& Heilmann-Clausen (2013: 103).
Collections labelled as T. joachimii appear on three widely
divided branches in the tree. We have not studied the type of
this species, and as far we know no type sequence is available
to test the correct position of this species in the phylogeny.
The included extra-liminal sequences add to the complexity of
the groups. A global analysis including multiple genetic mark-
ers, and renewed attempts to sequence type collections is
needed to resolve the taxonomy of the group, which also con-
tains T. chrysophyllum, described from southern Europe (Riva
1988), and T. intermedium, described from North America.
Somewhat surprisingly, the two whitish species with radially
fibrillose pileipellis, T. columbetta and T. umbonatum seem to
have a basal position to the T. equestre complex. As already
emphasized by Christensen & Heilmann-Clausen (2013) col-
lections labelled as T. umbonatum fall in two distinct subclades.
We are quite convinced that type II, as illustrated in Chris-
tensen & Heilmann-Clausen (2013), corresponds to the original
concept of this species as presented by Clémençon & Bon in
Bon (1984b). Judging from Bessette et al. (2013) also T. sub-
resplendens belongs to this species group.
The T. sejunctum/ viridilutescens group is another poorly
resolved subclade in sect. Tricholoma. Except for the South-
European taxon T. rufenum that has a grey pileus, the European
members of this group are characterized by greenish to yel-
lowish pileus colours. In our recent monograph, we accepted
only two species viz. T. sejunctum and T. viridilutescens to
occur in northern Europe, but the current analysis shows that
our concept of T. viridilutescens as presented in Christensen
& Heilmann-Clausen (2013) circumscribes two well separated
species based on ITS. These are here denoted as T. viridilute-
scens type I and II, respectively. Further collections from North
America labelled as T. sejunctum and T. leucophyllum represent
further distinct terminal branches. In our data T. viridilutescens
type I is represented by two collections from France, quite
close to the type locality in the Austrian Alps, and it might well
represent T. viridilutescens s.str. Type II is represented by two
collections from Estonia, that have high ITS similarity to col-
lections from Canada and Japan. Tricholoma subsejunctum
described from eastern North America is a relevant candidate
name for these collections. We have studied the type collection
of T. subsejunctum which is in poor condition and unlikely to
yield usable ITS data. Tricholoma eosinobasis and T. clavocystis
are additional European species described in this group and
represent further candidate names (or synonyms) for T. viri-
dilutescens type I and II. Types of the mentioned taxa have not
been studied by us.
Also T. viridifucatum and T. luridum are characterized by green-
ish to olivaceous pileus colours and both may belong to this
group, even if the squamulose stipe in the former and the grey-
ish lamellae in the latter are deviant. We have been unsuc-
cessful in obtaining sequence data for these two taxa. Chapon
(2011) compared T. viridifucatum with a further taxon denoted
as T. coryphaeum. This species might well belong to this
group but could also be part of the T. equestre complex. For
a nomenclatural discussion on this name see Christensen
& Heilmann-Clausen (2013). Judging from descriptions and
photos in Bessette et al. (2013), also the North American taxa
T. davisiae and T. subluteum belong to this group, probably
together with T. muscarium described from Japan (e.g. Hongo
1988). Comprehensive studies using a global sampling strategy,
type studies and multiple molecular markers are needed to
resolve the taxonomy of this difficult species complex.
Species with a grey or yellow, radially fibrillose dry pileus (sect.
Virgata ss. Singer 1986) form a relatively well-resolved sub-
clade in our tree, with the glutinous T. portentosum having a
more distant position. According to our data, T. bresadolaum is
heterogeneous in the ITS region, and in general we would not
be surprised if a more comprehensive sampling would show
the subclade to contain more species in Europe. Several ad-
ditional species have been described in the group, including
T. lilacinocinereum, T. sciodellum and T. vinaceogriseum, and
some authors also distinguish T. hordum as a separate species
close to T. sciodes (but see Christensen & Heilmann-Clausen
2013). The subclade seems to be richly represented in North
America. Judging from Bessette et al. (2013) at least T. acris,
T. argenteum, T. atrodiscus, T. palustre and T. pullum belongs
here. The included sequence of the latter species is close to
T. aestuans. Finally, the sequence of T. aff. virgatum from Nepal
clearly represent a separate taxon close to T. virgatum.
Unassigned species
Apart from the species that are assigned to the ten hy-
pothesized sections discussed above, five sequenced North-
European species, viz. T. arvernense, T. josserandii, T. fucatum,
T. borgsjoeënse and T. apium, remain unclassified at section
level (Fig. 2). Despite the presence of clamp connections, T. ar-
vernense has traditionally been assigned to the clampless
sect. Tricholoma (e.g. Riva 1988, Noordeloos & Christensen
1999), but in our tree it forms an isolated cluster with a se-
quence identified as T. luteomaculosum from North America
(Fig. 1). This species is characterized by a greyish, fibrillose
to squamulose pileus and yellowing flesh and in contrast to
T. arvernense, it is described to lack clamp connections (Ovrebo
1986). Smith (1942), who described the species, pointed out
its similarity with T. scalpturatum, which lead Singer (1986) to
regard it as a possible member of sect. Terrea. This placement
is not supported by our analysis. The second unclassified
species, T. josserandii, has traditionally been considered as a
close relative to T. virgatum (Bon 1984a, Riva 1988), but this
is disapproved by our analysis. Instead, the species clusters
closely with two sequences from North America identified as
T. mutabile, and more distantly so with a third unassigned spe-
cies, T. fucatum, that has traditionally been assigned to sect.
Tricholoma (e.g. Riva 1988, Noordeloos & Christensen 1999).
All three species are characterized by slender fruit bodies
with a cylindrical stipe, a radially fibrillose pileipellis and large
spores. Based on photographs and descriptions in Bessette et
al. (2013), the North American T. aurantio-olivaceum appears to
be a close relative of T. fucatum, together with T. olivaceobrun-
54 Persoonia – Volume 38, 2017
neum. All the above species might form an evolutionary lineage
worth accepting at the section level. A further deviant lineage is
formed by T. borgsjoeënse that clusters closely with a sequence
of T. atroviolaceum from North America. Both species share
a dark grey, felty to squamulose pileus, greyish lamellae and
large spores. When describing T. borgsjoeënse, Jacobsson et
al. (2006) assigned the species to sect. Terrea, but the current
phylogenetic analysis indicates it to be only distantly related to
this section. The large spores and the quite special pileipellis
structure (see Christensen & Heilmann-Clausen 2013: 20) sup-
port the isolated position among European Tricholoma species.
Interestingly, our analysis points to substantial variation in the
ITS region in T. borgsjoeënse, with the Norwegian collection
deviating considerably from the two Swedish collections that
both stem from the type locality.
Finally, T. apium appears to be isolated among the species
analysed. Noordeloos & Christensen (1999) classified it in
sect. Imbricata (here a part of sect. Genuina). The species
do show some morphological resemblance to species in this
section, and might have a basal position in it, as suggested by
the maximum likelihood analysis.
NEW COMBINATIONS
Tricholoma rapipes (Krombh.) Heilm.-Claus. & Mort.Chr.,
comb. nov. — Mycobank MB816908
Basionym. Agaricus rapipes Krombh. (1836: 22).
Description in Christensen & Heilmann-Clausen (2013).
DIAGNOSES AND DESCRIPTIONS OF NEW SPECIES
Tricholoma ilkkae Mort.Chr., Heilm.-Claus., Ryman & Niclas
Bergius, sp. nov. — MycoBank MB816909; Fig. 3a, b
Etymology. Latin ‘ilkkae’ in honour of the Finnish mycologist Ilkka Kutö-
vuori.
Holotype. Sweden, Gotland, Eksta par, Ekstastrand, coniferous forest do-
minated by Pinus sylvestris, with scattered Picea abies on old beach ridges,
21 Sept. 2000, leg. Svengunnar Ryman 9080 (UPS, F-513823).
Diagnosis — A medium-sized to large Tricholoma, with a dis-
tinct ring, and fawn to dark brick, confluent fibrillose patches
on the pileus and girdles on the stipe. Mycorrhizal with Pinus
and possibly Picea.
Pileus 40–100 mm, at first hemispherical to convex with involute
margin, later convex to flattened, often with low, broad umbo,
in central part soon breaking up into appressed, ± confluent
scales, which are fawn, orange brown to dark brick, on a cream
to straw yellow background; scales gradually or more abruptly
thinning out towards the marginal zone, which is typically white
to straw yellow or pale mouse grey; margin in young fruit bodies
shaggy due to remnants of veil, but soon ± smooth to somewhat
felty-costate. Lamellae emarginate, with even to somewhat
eroded edges, whitish, with age sometimes with orange brown
spots, rather close to medium spaced. Stipe 50–100 × 15–25
mm, cylindrical or tapering downwards, often somewhat rooting,
with a distinct, persistent, cuff-like, cottony-woolly ring, whitish
and granulose or slightly fibrillose above ring, below ring with
irregular, fawn, orange brown to dark brick confluent girdles and
patches on a whitish background, basal part occasionally with
a weak greenish tinge. Flesh whitish; smell sweetish, perfumed
fruity, similar to Inocybe corydalina or Hemipholiota heteroclita;
taste unknown. Spores 4.5–6.7 × 3.9–5.5 μm, average 5.1–6.0
× 4.4–4.9 μm, predominantly broadly ellipsoid, Q = 1.0–1.5,
average 1.15–1.31. Basidia 30–40 × 6 – 8 μm, 4-spored.
Cheilocystidia not observed. Pileipellis cutis made up of cylindri-
cal, warm brown hyphae, 50–300 × 5 –15(–20) μm, pigment
not incrusting. Clamp connections absent.
Ecology & Habitat — Ectomycorrhizal with Pinus and pos-
sibly Picea, mainly in forests on calcareous ground.
Known distribution — Central Sweden (holotype), Norway,
Spain and Turkey; most likely widespread in Europe.
Additional material examined. Sweden, Gotland, Eksta Par., Ekstastrand,
coniferous forest on old beach walls, 9 Oct. 1998 (MC98-602, C-F-96261); ibid.,
18 Sept. 2000 (UPS-F013888); ibid., associated with T. aurantium, T. fracti-
cum, Hydnum albidum, Hygrophorus latitabundus and Sarcodon fuligineovio-
laceous, 3 Oct. 2009, Irene Anderson & Michael Krikorev (MKR 091003-4,
IMG: 100/1208-11); ibid., 29. Sept. 2011 (TF2011-201); Uppland, Gräsö par.,
Djupdal 3 km NE of Gräsö church (Grid: RN1648667 x 6697072), in needle
bed under Picea abies in old Picea /Pinus forest, 2 Oct. 2007, Gillis Aronsson
(UPS-F173364); Uppland, Börstil par., the turnaround on NW Tvärnö (Grid:
RN1648788 x 6681279), under Picea abies and Pinus sylvestris in older,
grass-dominated forest on old slag heap, 13 Sept. 2007 (UPS-F173264);
ibid., 24 Sept. 2009, Gillis Aronsson (UPS-F173265).
Notes — According to the phylogenetic analysis the new spe-
cies is close to T. dulciolens. Both species share small spores,
but T. ilkkae is easily distinguished from T. dulciolens by the
shorter stem and much darker pileus scales and stipe girdles.
Another similar species is T. caligatum, which is distinguished
by larger spores and by slightly darker, more contrasting pileus
scales and stipe girdles. In addition, the two species differ in
habitat and distribution, as T. caligatum seems to be a strictly
Mediterranean species, in contrast to T. ilkkae, which so far is
known from more temperate environments. Finally, T. matsutake
differs by duller colours, larger fruit bodies and larger spores.
Armillaria caligata var. gracilis, as illustrated by Bresadola
(1927), matches well with T. ilkkae, but we don’t know if authen-
tical material exists that could prove this. A potential synonymy
will not have nomenclatural consequences as Armillaria caligata
var. gracilis has never been combined as a species epithet.
Tricholoma bryogenum Mort.Chr., Heilm.-Claus. & Vauras,
sp. nov. — MycoBank MB816910; Fig. 3c
Etymology. From Greek ‘βρύον’ (moss) and ‘γεννώ’ (born), referring to
the habitat in mossy Picea-forests.
Holotype. Sweden, Jämtland, Brunflo, under Picea abies on rich soil,
among mosses, 4 Sept. 1997, Morten Christensen MC97-101 (C-F59167).
Diagnosis — A small to medium-sized Tricholoma, with dull yel-
low colours on stipe, lamellae and pileus margin and a strong,
chemical smell. Differing from the closely related T. sulphureum
by the duller colours, white basal mycelium and by the occur-
rence in mossy Picea forests.
Pileus 30 –100 mm, at first conical, bell-shaped or convex,
soon low convex to plane, with or without a low umbo, smooth,
glossy, at margin whitish chrome to pale chrome, with age
and towards centre darker, pinkish buff to ochraceous orange.
Lamellae adnate to deeply emarginate, rather broad and thick,
medium spaced to rather distant, lemon yellow to lemon chrome
or honey, more saturated than the margin of the pileus. Stipe
50–130 × 8–25 mm, cylindrical or slightly club-shaped, smooth
or more often distinctly fibrillose, at base often with white tomen-
tum, straw yellow, pale yellow to light chrome, darkest and most
yellow towards base, with age often duller, pale cream to cream,
with a ± fibrillose brownish covering; basal mycelium whitish to
faintly yellowish. Flesh rather firm, coloured more or less like the
surface; smell strong, tar- or gas-like as in T. sulphureum, after
cutting more farinaceous; taste unpleasant, mild, farinaceous-
rancid to slightly bitter. Spores 8.2 –14.4 × 4.7–8.4 μm, average
9.4–12.3 × 5.6–7.5 μm, ellipsoid to elongate or amygdaliform,
Q = 1.3–2.0, average 1.62–1.69. Basidia 35–60 × 7.5 –10.0
μm, mainly 2-spored. Cheilocystidia not observed. Pileipellis
an interwoven cutis with individual hyphal elements generally
55
J. Heilmann-Clausen et al.: Tricholoma in northern Europe
50–150 × 3– 6 μm; subpellis poorly differentiated. Clamp con-
nections not observed, apparently absent.
Ecology & Habitat — Ectomycorrhizal with Picea and pos-
sibly Pinus, mainly in rich, mixed forests on calcareous soils.
Most records are from moist, eutrophic depressions, or spring-
fed slopes with abundant bryophytes, but there are also some
records from drier soils.
Known distribution — Central Sweden, Norway and Finland;
most likely widespread in Fennoscandia, and possibly in the
mountains of central Europe.
Additional material examined. Finland, Koillismaa, Kuusamo, Iivaara,
E slope, S of Saunakunnas, near Isokorpi, forest with mainly Picea abies and
scattered Pinus sylvestris, Alnus incana and Betula, eutrophic depression,
29 Aug. 2007, Jukka Vauras (25068, TURA); Perä-Pohjanmaa, Rovaniemi
rural commune, Jaatila, Jaatilanvaara, near Kylmäojao brook, fairly rich,
gently W-sloping, spring-fed forest with Picea abies, Betula, Alnus incana,
Populus tremula and Pinus sylvestris, 11 Aug. 1999, Jukka Vauras (15082F,
TURA); ibid., 19 Aug. 1999, Jukka Vauras (15223F, TURA).
Notes — The new species is distinguished from T. sulphure-
um mainly by its habitat, the dull yellow colours and the whitish
basal mycelium. The difference in coloration is distinct even in
exsiccata, which are typically pale buff in T. bryogenum, but
cinnamon to greyish brown in T. sulphureum. A further difference
may be the absence of clamp connections in T. bryogenum,
but we are not certain if this character difference is truly stable.
Tricholoma bryogenum is quite similar to T. odorum described
from North America, but the latter taxon has more crowded
lamellae.
Tricholoma boreosulphurescens Mort.Chr. & Heilm.-Claus.,
sp. nov. — MycoBank MB816911; Fig. 3d
Etymology. From latin ‘borealis’ (northern) combined with the species
epithet of Tricholoma sulphurescens, a closely related and morphologically
almost similar relative with a southern distribution in Europe.
Holotype. norway, Finnmark, Alta, Kåfjordsbotten, S of Hesteskovattnet,
under Betula, 18 Aug. 2004, Per Marstad 197-04 (O-F187683).
Diagnosis — A medium-sized to large Tricholoma, with whitish
colours and strongly yellowing context. Mycorrhizal with Betula
and possibly Picea in boreal and subalpine forests on calcare-
ous soils. Morphologically very similar to T. sulphurescens, but
with substantial differences in the mitochondrial ITS region and
a different ecology and distribution range.
Pileus 30–100 mm, at first bell-shaped to convex, soon low
convex to plane or slightly depressed, often irregularly wavy,
with or without a low umbo, dry and dull, very finely velutinate,
without radial structure, white when young, becoming pale
chrome, ochraceous or yellowish brown with age, especially
in central part, strongly yellowing when touched, after some
time fading to ochre. Lamellae adnate to emarginate, medium
broad, medium spaced to rather crowded, whitish to cream
or pale chrome, with age becoming lemon yellow to honey,
especially near the edges or when damaged. Stipe 50–100 ×
10–20 mm, ± cylindrical, mostly widened at base, more rarely
tapering, smooth, but mostly finely floccose to squamulose at
top, at base often velutinate, at first white to whitish chrome,
staining lemon yellow to pale chrome, especially when touched,
slowly fading to clay buff reddish brown. Flesh rather firm,
white to cream, staining lemon yellow to sulphur yellow after
cutting; smell strong, at first recalling lemons, then complex
nauseating, combining aromatic flowery, gas-like and rancid
components; taste first mild, but after a while somewhat acrid
to bitter. Spores 4.5–7.6 × 3.9 – 6.0 μm, average 5.6 – 6.4 ×
4.2–5.1 μm, predominantly broadly ellipsoid, Q = 1.0–1.5, aver-
age 1.20–1.25. Basidia 25–35 × 5.5–8 μm, mainly 4-spored.
Cheilocystidia not observed. Pileipellis an irregularly interwoven
cutis with individual hyphal elements generally 50–200 × 4–10
μm; subpellis poorly differentiated. Clamp connections present
at some septa.
c
b
d
a
Fig. 3 Fruitbodies of Trichloma species. a. Tricholoma ilkkae (holotype); b. Tricholoma ilkkae, older specimens (UPS-F173364); c. Tricholoma bryogenum
(holotype); d. Tricholoma boreosulphurescens (holotype). — Scale bars = 1 cm.
56 Persoonia – Volume 38, 2017
Ecology & Habitat — Ectomycorrhizal with Betula and pos-
sibly Picea on calcareous soils in rich, mixed Picea dominated
forests and in subalpine Betula forests near the timber line.
Known distribution — Seemingly with an eastern distribution
in Fennoscandia; known from several localities in the northern
part of Finland, but only from scattered localities in Sweden and
Norway. Probably distributed eastwards in Russia, and perhaps
even present in other parts of Europe, e.g. in subalpine forests
in central European mountain chains.
Additional material examined. Finland, Outer Ostrobothnia (PeP/Obu),
Tervola, Peura, Raemäki, E of the forest road to Syvälampi, between the pond
Pikku-Ruuntana and Raemäenjänkä, S-sloping, grass-herb spruce forest with
spring-fed depressions on calcareous ground, 11 Oct.1997, Ilkka Kytövuori
97-1187 (H6002040); Koillismaa, Kuusamo, Oulanka National Park, N of the
biological field station, E of Puukkosuo, herb rich forest with Picea abies,
Pinus sylvestris, Betula, Populus tremula and Salix, eutrophic depression with
Daphne mezereum, Filipendia ulmaria, Goodyera repens, Cirsium helenoides
and Elymus caninus, 4 Sept. 2005, Jukka Vauras (23414F, TURA); Koil-
lismaa, Kuusamo, Oulanka National Park, Ampumavaara, E of Puukkosuo,
S of the main road, margin of eutrophic depression with Picea abies, Pinus
sylvestris, Alnus incana, Betula and Salix. 30 Aug. 2007, Emanuele Campo
& Jukka Vauras (25089F, TURA).
Notes — Tricholoma sulphurescens has long been known
as rare but easily identified species characterized by whitish
colours and strongly yellowing context. While working with the
volume on Tricholoma in Fungi of Northern Europe (Christensen
& Heilmann-Clausen 2013) we realized that collections from
boreal to subalpine Fennoscandia represented a clearly dif-
ferent lineage, than collections from southern Europe that are
typically associated with Fagus and Quercus, on warm calcare-
ous soils. Since T. sulphurescens was originally described from
Italy (Bresadola 1905) we here describe the new species as
T. boreosulphurescens emphasizing its boreal distribution. The
new species is very similar to T. sulphurescens in all important
morphological characters. Our updated phylogeny presented
here strongly indicates the presence of a third cryptic taxon
in the group represented by one collection from Italy and one
from a boreonemoral forest with Quercus and Tilia in Estonia.
It remains to be determined which of the two non-boreal line-
ages corresponds to the type specimen of T. sulphurescens
originally described by Bresadola, and the degree to which they
are separable based on morphological or ecological characters.
DISCUSSION
With the present study we have provided a first comprehensive
phylogenetically supported taxonomic overview of the genus
Tricholoma in northern Europe. Based on this we consider sec-
tions Caligata, Atrosquamosa and Terrea as rather well evalu-
ated taxonomically on the European continental scale. All three
sections have been sampled intensively in this or other stud-
ies, and we would be surprised if future studies will change
fundamentally with the species delimitations presented here
and elaborated in more detail by Christensen & Heilmann-
Clausen (2013). For all other sections our sampling is limited
and additional European species are likely to occur, not least
in southern Europe. The sections Genuina, Contextocutis, Seri-
cella and Tricholoma in particular are in need of further phylo-
genetic studies with T. equestre s.lat., T. sulphureum s.lat. and
T. viridilutescens/sejunctum representing species complexes
with considerable cryptic diversity. These are all represented
across the northern hemisphere and future studies address-
ing these two groups should apply a comprehensive sampling
strategy and apply multiple genetic markers to unravel the
complex phylogeography of both groups.
Many Tricholoma species appear to have a circumboreal
distribution based on the data presented in our study. At least
T. aurantium, T. batschii, T. bonii, T. dulciolens, T. focale, T. fron-
dosae, T. inamoenum,T. matsutake, T. portentosum, T. roseo-
acerbum T. stans and T. triste have almost exact ITS similarity
across two or three continents, and according to Jargeat et
al. (2010) the same applies for T. argyraceum and T. cingula-
tum. Most extreme in this respect is T. roseoacerbum, which
according to our data, is present in Finland, Canada, Japan
and Mexico. In Europe it is considered a rarity (Riva 1988,
Christensen & Heilmann-Clausen 2013), making the wide
distribution particularly intriguing. The above-mentioned spe-
cies with an intercontinental distribution are all associated with
widely distributed boreal host tree genera: T. dulciolens and T.
inamoenum are primarily associated with Picea, T. frondosae
with Populus, T. cingulatum with Salix, while T. aurantium and T.
argyraceum have a broad host selection. The remaining species
are associated primarily or exclusively with Pinus. Thus, none
of the species associated exclusively with nemoral deciduous
hosts, including Fagus and Quercus occurs across continents
based on our data. Grubisha et al. (2012), investigated in more
detail the phylogeography of T. populinum and found substan-
tial divergence between North American and Fennoscandian
populations, pointing to a reproductive isolation established
1–1.7 million years ago. Similar studies investigating the phy-
logeography of the apparently circumboreal species mentioned
above would be interesting.
Regarding the higher level taxonomy, our study has provided
support for several classical sections accepted in Tricholoma,
but with some modifications. Most importantly our data showed
T. focale to be a member of sect. Genuina, rather than sect.
Caligata, while T. sciodes and allied taxa were shown to belong
to sect. Tricholoma rather than to sections Terrea or Atrosqua-
mosa. While ITS appears to be a stable marker for species
delimitations in Tricholoma (Mouhamadou et al. 2008, Jargeat
et al. 2010) there are no reasons to believe that the region can
resolve higher taxonomic relationships at a sufficiently detailed
level (e.g. Frøslev et al. 2005). Hence the here suggested in-
frageneric classification should be viewed as preliminary, and
we encourage further studies using multiple molecular mark-
ers to investigate the infrageneric phylogeny of the genus. As
the majority of known species in Tricholoma occurs in North
America it is obvious that a careful sampling of North American
taxa should be part of such a study, but even Asia, Australia,
New Zealand and southern South America host Tricholoma
species that are highly relevant to include in future attempts to
unravel the biodiversity, evolution and phylogeography of this
important ectomycorrhizal genus.
Acknowledgements Irene Andersson, Niclas Bergius, Tor Erik Brandrud,
Gro Gulden, Liz Holden, Claes Ingvert, Thomas S. Jeppesen, Kuulo Kala-
mees, Tommy Knutsson, Michael Krikorev, Lasse Kosonen, Ilkka Kytövuori,
Christian Lange, Perry Larsen, Thomas Læssøe, Jens Maarbjerg, Michal
Mikšik, Pierre-Arthur Moreau, Siw Muskos, Johan Nitare, Machiel Noordeloos,
Clark Ovrebo, Scott Redhead, Alfredo Riva, Svengunnar Ryman, Sigvard
Svensson, Jukka Vauras and Jan Vesterholt† are thanked for valuable discus-
sions, for giving us the opportunity to study their interesting collections and
for allowing us to use their sequence data. The curators of the herbaria C,
E, H, K, L, LIP, LUG, M, O, OULU, S, TAA and UPS are thanked for arrang-
ing loans. We want to thank the J. E. Lange and the Flora Agaricina Danica
Foundations for supporting collection trips outside Denmark, while UNITE
is thanked for supporting the sequencing of collections.
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