Desarmillaria caespitosa, a North American vicariant of D. tabescens

Abstract

Desarmillaria caespitosa, a North American vicariant species of European D. tabescens, is redescribed in detail based on recent collections from the USA and Mexico. This species is characterized by morphological features and multilocus phylogenetic analyses using portions of nuc rDNA 28S (28S), translation elongation factor 1-alpha (tef1), the second largest subunit of RNA polymerase II (rpb2), actin (act), and glyceraldehyde-3-phosphate dehydrogenase (gpd). A neotype of D. caespitosa is designated here. Morphological and genetic differences between D. caespitosa and D. tabescens were identified. Morphologically, D. caespitosa differs from D. tabescens by having wider basidiospores, narrower cheilocystidia, which are often irregular or mixed (regular, irregular, or coralloid), and narrower caulocystidia. Phylogenetic analyses of five independent gene regions show that D. caespitosa and D. tabescens are separated by nodes with strong support. The new combination, D. caespitosa, is proposed.

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Desarmillaria caespitosa, a North American
vicariant of D. tabescens
Vladimír Antonín, Jane E. Stewart, Rosario Medel Ortiz, Mee-Sook Kim,
Pierluigi (Enrico) Bonello, Michal Tomšovský & Ned B. Klopfenstein
To cite this article: Vladimír Antonín, Jane E. Stewart, Rosario Medel Ortiz, Mee-Sook Kim,
Pierluigi (Enrico) Bonello, Michal Tomšovský & Ned B. Klopfenstein (2021) Desarmillaria
caespitosa, a North American vicariant of D.�tabescens, Mycologia, 113:4, 776-790, DOI:
10.1080/00275514.2021.1890969
To link to this article: https://doi.org/10.1080/00275514.2021.1890969
Published online: 29 Apr 2021.
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Desarmillaria caespitosa, a North American vicariant of D. tabescens
Vladimír Antonín
a
, Jane E. Stewart
b
, Rosario Medel Ortiz
c
, Mee-Sook Kim
d
, Pierluigi (Enrico) Bonello
e
,
Michal Tomšovský
f
, and Ned B. Klopfenstein
g
a
Department of Botany, Moravian Museum, Zelný trh 6, 659 37 Brno, Czech Republic;
b
Department of Agricultural Biology, Colorado State University,
307 University Avenue, Ft. Collins, Colorado 80523;
c
Centro de Investigación en Micología Aplicada/Universidad Veracruzana, Médicos 5, Col. Unidad
del Bosque, Xalapa, 91010, Veracruz, Mexico;
d
United States Department of Agriculture, Forest Service, Pacific Northwest Research Station, 3200 SW
Jefferson Way, Corvallis, Oregon 97331;
e
Department of Plant Pathology, The Ohio State University, 201 Kottman Hall, 2021 Coffey Road, Columbus,
Ohio 43210;
f
Department of Forest Protection and Wildlife Management, Faculty of Forestry and Wood Technology, Mendel University in Brno,
Zemedelska 3, 613 00 Brno, Czech Republic;
g
United States Department of Agriculture, Forest Service, Rocky Mountain Research Station, 1221 South
Main Street, Moscow, Idaho 83843
ABSTRACT
Desarmillaria caespitosa, a North American vicariant species of European D. tabescens, is redescribed in
detail based on recent collections from the USA and Mexico. This species is characterized by morpho-
logical features and multilocus phylogenetic analyses using portions of nuc rDNA 28S (28S), translation
elongation factor 1-alpha (tef1), the second largest subunit of RNA polymerase II (rpb2), actin (act), and
glyceraldehyde-3-phosphate dehydrogenase (gpd). A neotype of D. caespitosa is designated here.
Morphological and genetic dierences between D. caespitosa and D. tabescens were identied.
Morphologically, D. caespitosa diers from D. tabescens by having wider basidiospores, narrower
cheilocystidia, which are often irregular or mixed (regular, irregular, or coralloid), and narrower caulo-
cystidia. Phylogenetic analyses of ve independent gene regions show that D. caespitosa and
D. tabescens are separated by nodes with strong support. The new combination, D. caespitosa, is
proposed.
ARTICLE HISTORY
Received 27 March 2020
Accepted 12 February 2021
KEYWORDS
28S; act; Armillaria; gpd; new
combination;
Physalacriaceae; rpb2; tef1; 1
new taxon
INTRODUCTION
Two separate genera are distinguished among former
species of Armillaria (Fr.) Staude. The genus Armillaria
s.str. contains the annulate taxa (39 species; He et al.
2019), whereas Desarmillaria (Herink) R.A. Koch &
Aime includes exannulata taxa, of which only two are
known. One of them, D. ectypa (Fr.) R.A. Koch & Aime,
in contrast to other relative species, is not lignicolous
and occurs in Eurasian marshes and peat bogs.
Moreover, it forms single growing basidiomata with an
apparently smooth pileus. The second species,
D. tabescens (Scop.) R.A. Koch & Aime, is lignicolous
and similar to the annulate taxa in many ecological
aspects.
Herink (1973) was the first author who separated
annulate and exannulate taxa of Armillaria into two
distinct subgenera, Armillaria and Desarmillaria
Herink. However, recognition of these subgenera was
largely overlooked for decades, likely because it was
published in Czech in the proceedings from
a conference about A. mellea (Vahl) P. Kumm (Hašek
1973). Singer (1975, 1986) also divided these species (as
Armillariella P. Karst.) into annulate and exannulate
groups, but without any formal taxonomic solution.
Based on previous multilocus phylogenetic analyses,
armillarioid (Physalacriaceae) were determined to con-
tain three genera: (i) Guyanagaster T.W. Henkel, M.E.
Smith & Aime, a gasteroid genus that is the earliest
diverging lineage; (ii) Desarmillaria, an exannulate
mushroom-forming Armillaria subgenus that was ele-
vated to genus level and comprises two species:
D. tabescens and D. ectypa; and (iii) Armillaria, the sister
lineage of Desarmillaria that comprises annulate mush-
room-forming species that form melanized rhizomorphs
(Koch et al. 2017). Based on morphology and ecology,
Antonín et al. (2006) determined that A. socialis (DC)
Fayod was the correct name for D. tabescens (as
A. tabescens (Scop.) Emel). Subsequently, Redhead
et al. (2012) proposed to conserve the name
A. tabescens, and this proposal was approved
(May 2017).
Based on the biological species concept used for
Armillaria s.l. (e.g., Korhonen 1978; Anderson and
Ullrich 1979), mating tests showed that D. tabescens
(as A. tabescens) isolates from eastern Asia (i.e., Japan,
China) were interfertile with European isolates (Ota
et al. 1998; Qin et al. 2007), whereas D. tabescens (as
CONTACT Vladimír Antonín vantonin@mzm.cz
MYCOLOGIA
2021, VOL. 113, NO. 4, 776–790
https://doi.org/10.1080/00275514.2021.1890969
© 2021 The Mycological Society of America
Published online 29 Apr 2021

A. tabescens) isolates from eastern Asia and Europe were
found intersterile with North American isolates
(Guillaumin et al. 1989; Ota et al. 1998). A previous
study by Darmono et al. (1992) reported interfertility
of D. tabescens (as A. tabescens) isolates of southeastern,
eastern, and central USA, which provided evidence for
a single biological species of D. tabescens in the USA,
whereas other mating tests provided supporting evi-
dence that D. tabescens isolates from Eurasia and
North America were reproductively incompatible. In
reference to mating tests of D. tabescens (as
A. tabescens), Guillaumin et al. (1989) stated that
A. tabescens is probably also a complex including several
species, and Kile et al. (1994) accepted the opinion by
Mohammed and Guillaumin (unpublished; cited by Kile
et al. 1994) that the most appropriate name for the
North American fungus is “Armillaria” monadelpha
(Morgan). Qin et al. (2007) concluded: “It is obvious
that this species needs further investigation.”
Multilocus phylogenetic analyses demonstrate a clear
separation of D. tabescens isolates from Eurasia and those
from North America (e.g., Tsykun et al. 2013; Coetzee
et al. 2015; Guo et al. 2016; Koch et al. 2017), which is
further supported by phylogenetic analysis of translation
elongation factor 1-α (tef1) gene sequences (Klopfenstein
et al. 2017; Coetzee et al. 2018). Based on this evidence,
Klopfenstein et al. (2017) and Coetzee et al. (2018) con-
cluded that a taxonomic study focused on North
American and Eurasian A. socialis/tabescens
(D. tabescens) is needed to determine whether multiple
phylogenetic species exist within the exannulate clade and
to solve the taxonomic treatment of A. tabescens from
Europe, North America, and Asia. Park et al. (2018)
demonstrated the presence of D. tabescens in South
Korea based on both DNA sequences (internal tran-
scribed spacer [ITS] and tef1) and morphology.
According to their results, however, it seems that the
South Korean collections of D. tabescens may be phylo-
genetically different from the European specimens.
Berkeley (1847) described Lentinus caespitosus Berk.
based on material collected in Waynesville, Ohio. Pegler
(1983), who revised the type specimen, mentioned its
identity with A. tabescens. The latter name is older; there-
fore, this fungus was published under this name in the
literature referring to specimens from North American
(e.g., Ross 1970; Cox 2004; Cox et al. 2006; Schnabel et al.
2005, 2006; Kuo 2017). In the case that the American
fungus is different from true D. tabescens, the name
Lentinus caespitosus is the oldest name available for this
taxon.
On the aforementioned bases, the objective of this study
was to compare D. tabescens from North America and
Europe using morphological and multilocus phylogenetic
analyses to determine whether specimens from these con-
tinents are conspecific or allospecific.
MATERIALS AND METHODS
Isolates/specimens and culture.—Five specimens of
D. tabescens from North America and six from Europe
were used for morphological and phylogenetic analyses
(TABLE 1). In addition, several specimens of
D. tabescens were used for studies of morphological
variability within this species. The North American
material was collected in Waynesville, Ohio, USA, and
in Xalapa, Veracruz, Mexico. For comparisons,
European specimens originated from the Burgas region,
Bulgaria; South Moravia, Czech Republic; Bourgogne,
France; Bratislava, Nitra region, and southern parts of
Banská Bystrica region, Slovakia; and Panovec, Slovenia.
Morphology.—The macroscopic description was based
on fresh basidiomata collected in Mexico and the USA.
Color abbreviations followed Kornerup and Wanscher
(1983). The microscopic description was based on dry
basidiomata. Sections were mounted in KOH, Melzer’s
reagent, and Congo red and observed using an Olympus
BX-50 light microscope (Tokyo, Japan) with
a magnification of 1000×. For basidiospores, the factors
Q (quotient of length and width in any one spore) and
mean values were used. Herbarium abbreviations fol-
lowed Thiers (continuously updated) (FIGS. 1–3).
DNA extraction, sequencing, and phylogenetics.—
Following the protocols of Elías-Román et al. (2018),
DNA was extracted from each culture isolate, and DNA
quality and quantity were estimated using a Nanodrop
2000 spectrophotometer (ThermoScientific, Waltham,
Massachusetts). Sequencing of five loci was attempted
for selected isolates (North America: XAL MAX21WF,
OHIO_2018PB-1, OOI-210, OOI-99, AT-MU-S2;
Europe: MENDELU 171, 519, 520, 521, 522, and 525),
including portions of nuc 28S rDNA (28S), tef1,
the second largest subunit of RNA polymerase II (rpb2),
actin (act), and glyceraldehyde-3-phosphate dehydrogen-
ase (gpd) (TABLE 1). Amplification reaction mixtures
(total 25 μL) contained 20‒40 ng of template DNA (or
no DNA template for negative control), 2.5 µL 10×
Standard Taq Reaction Buffer (New England BioLabs,
Ipswich, Massachusetts), 0.5 µL 10 mM dNTPs (Roche
Applied Science, Madison, Wisconsin), 1 µL each of 10
µM primer, and 0.125 µL (0.6 U) Taq DNA Polymerase
(New England BioLabs). Amplifications were performed
using the following polymerase chain reaction (PCR)
MYCOLOGIA 777

Table 1. List of Desarmillaria caespitosa and D. tabescens reference isolates/specimens used for morphological comparison and phylogenetic analyses.
GenBank accession numbers
b
Species
Basidiome-derived culture isolate
a
(herbar-
ium voucher specimen) Source Host Origin ITS tef1 rpb2 gpd 28S act
D. caespitosa XAL MEX21WF
(BRNM 825654)
Kim et al. 2010; this study Araucaria araucana Veracruz, Mexico — MT232066 MN990677 MN996978 MT163178 —
D. caespitosa OHIO_2018PB-1
(DBG F-030611/culture CBS 147612)
This study Acer saccharinum Ohio, USA MT007923 MT232065 MN990681 — MT238204 —
D. caespitosa OOI-210 Schnabel et al. 2005; Ross-
Davis et al. 2012
Prunus persica Georgia, USA AY213590 JF313111 MN990679 MN996984 AY509191 MT225098
D. caespitosa OOI-99 Schnabel et al. 2005; Ross-
Davis et al. 2012
P. persica Georgia, USA AY213589 JF313112 MN990678 MN996985 AY509192 —
D. caespitosa AT-MU-S2
c
Kim et al. 2006; Ross-Davis
et al. 2012
South Carolina, USA AY213588 JF313113 MN990680 — AY509189,
AY509190
MT225099
D. tabescens MENDELU 171 Lochman et al. 2004; this
study
Quercus robur Lanžhot, Cahnov,
Czech Republic
AY175806 MT221654 MN990671 MN996979 MT163172 —
D. tabescens MENDELU 519 Antonín et al. 2006; This study Quercus sp. Břeclav, Czech
Republic
DQ784799 MT221655 MN990672 MN996980 MT163173 MT225095
D. tabescens MENDELU 520 (BRNM 695685) This study Quercus sp. Břeclav, Czech
Republic
— — MN990673 MN996983 MT163174 MT225096
D. tabescens MENDELU 521 (BRNM 695686) This study Quercus sp. Břeclav, Czech
Republic
— MT221656 MN990674 MN996981 MT163175 —
D. tabescens MENDELU 522 (BRNM 695687) This study Ulmus sp. Břeclav, Czech
Republic
— MT221658 MN990675 MN996982 MT163176 —
D. tabescens MENDELU 525 (BRNM 699839) Antonín et al. 2006; this study Acer campestre Břeclav, Czech
Republic
DQ784800 MT221657 MN990676 — MT163177 MT225098
a
More information about isolates is available on the references in parentheses.
b
ITS = internal transcribed spacer; tef1 = translation elongation factor 1-alpha; rpb2 = RNA polymerase II; gpd = glyceraldehyde-3-phosphate dehydrogenase; 28S = nuclear ribosomal large subunit 28S; act = actin.
c
Stipe-derived culture.
778 ANTONÍN ET AL.: DESARMILLARIA CAESPITOSA

conditions: 94 C for 1 min, 35 cycles at 95 C for 30 s, 55‒
58 C (depending on the primers used: 28S: 58 C, tef1: 55
C, rpb2: 56 C, act: 57 C, and gpd: 55 C) for 30 s, and 72
C for 45 s, and finally 72 C for 10 min. Primer pairs used
to amplify each locus included LROR and LR5 for 28S
(Rehner and Samuels 1994; Vilgalys and Hester 1999);
EF983F and EF2218R for tef1 (Rehner and Buckley
2005); bRPB2-6F and bRPB2-7.1R for rpb2 (Matheny
2005); ACT-181 and Act-875R for act (F.O.P. Stefani
et al. pers. comm.); and GPD10F and GPD522R for gpd
(F.O.P. Stefani et al. pers. comm.) (TABLE 2). PCR
products were electrophoresed in 1.5% agarose gels
with 0.5× TBE buffer (45 mM Tris-pH 8.3, 45 mM
Boric acid, 1 mM Na
2
EDTA) and stained with GelRed
(Biotium, Fremont, California). Bands were visualized
using ultraviolet light (UV) light. PCR products were
treated with ExoSAP-IT PCR Product Cleanup
(Affymetrix, Santa Clara, California) following the man-
ufacturer’s protocol and sequenced at Eurofins MWG
Operon USA (Louisville, Kentucky). Phylogenies of
the individual five gene regions were inferred with refer-
ence isolates of closely related species. The suite of
reference isolates varied depending on the locus, and
GenBank numbers are shown in FIGS. 4‒8. To test the
genealogical concordance phylogenetic species recogni-
tion (GCPSR; Taylor et al. 2000) criteria on D. tabescens
collected from North American and Europe, phyloge-
nies for each locus were estimated separately to examine
well-supported separation of isolates for each locus
(Taylor et al. 2000). Phylogenies were estimated using
maximum likelihood (ML) in PhyML (Guindon et al.
2010) and Bayesian inference (BI) in MrBayes 3.2
(Ronquist et al. 2012) as implemented in Geneious
(Kearse et al. 2012; https://www.geneious.com/). DT-
ModSel (Minin et al. 2003) was used to estimate the best-
fit nucleotide substitution models for each data set.
Robustness and support for clades for the ML phylogeny
were assessed using 1000 bootstraps (BS). BI was per-
formed with parameter settings suggested by the best-fit
nucleotide substitution models. The Markov chain
Monte Carlo (MCMC) search was run with four chains
for 3 million generations generating 30 001 trees; the
first 6000 trees were discarded as “burn-in,” and node
support was indicated by posterior probability (PP).
Convergence and proper mixing of Bayesian analyses
were assessed by examining the trace plots that were
generated for two independent runs. Analyses were run
until the effective sampling size was >300 for all analyses.
Figure 1. Desarmillaria caespitosa. A‒B. Desarmillaria caespitosa basidiomata from Ohio, USA (pilei 40‒55 mm broad in mature
basidiomata). C. Basidium in 5% KOH. D. Cheilocystidium in 5% KOH. E. Caulocystidium in 5% KOH (microscopic structures from
basidiomata from Mexico) (XAL MEX21WF). Bars: C, D = 10 μm; E = 100 μm. Photographs: E. Bonello (A‒B) and R. Medel (C‒E).
MYCOLOGIA 779

RESULTS
Phylogeny.—A total of 4154 nucleotides were
sequenced at the 28S, tef1, rpb2, act, and gpd loci, with
1591, 561, 834, 681, and 487 bp, respectively. Of all the
loci, the 28S showed the least resolution for all the
Desarmillaria/Armillaria species, including D. tabescens
isolates (MENDELU 171, 519, 520, 521, 522, and 525)
collected from Europe and D. caespitosa isolates (XAL
MEX21WF, OHIO_2018PB-1, AT-MU-S2, OOI-99, and
OOI-210) collected from North America. Desarmillaria
tabescens and D. caespitosa were separated by the
following numbers of sites at each locus: 28S (0), rpb2
(10), gpd (4), act (3), and tef1 (25). Nucleotide variation
did not separate D. tabescens and D. caespitosa isolates at
the 28S region (FIG. 4). However, phylogenies of tef1
and gpd each showed separation of D. tabescens and
D. caespitosa with strong support (100% BS and 1.00
PP) (FIGS. 5, FIGS. 6; TABLE 3). This separation also
occurred in the act phylogeny with 100% BS, but lower
(0.70) PP support (FIG. 7; TABLE 3). However, at the
rbp2, D. caespitosa was contained within a well-
supported monophyletic subclade within a paraphyletic
clade that contained both Desarmillaria species (FIG. 8).
Figure 2. Comparison of microscopic characters of Desarmillaria caespitosa (neotype, left) and D. tabescens (right). A. Cheilocystidia.
B. Basidiospores. C. Terminal cells of stipitipellis hyphae. Bar = 20 µm. Del. V. Antonín.
780 ANTONÍN ET AL.: DESARMILLARIA CAESPITOSA

Sequences at the five loci were not obtained for all iso-
lates; however, representatives of both species were pre-
sent for each locus. At the tef1 locus, comparisons with
D. tabescens collected from widely separated locations
indicate that D. caespitosa is indeed a North American
vicariant (FIG. 5).
TAXONOMY
Desarmillaria caespitosa (Berk.) Antonín, J.E. Stewart
& Medel, comb. nov. FIGS. 1‒3
MycoBank MB837370, MBT393843
Basionym: Lentinus caespitosus Berk., in Hooker,
London J Bot 6:317. 1847.
Table 2. PCR primers used for amplifications.
Region/gene Primers Nucleotide sequence (5′ → 3′) Source
nuclear large subunit 28S rDNA (28S) LROR
LR5
ACC CGC TGA ACT TAA GC
TCC TGA GGG AAA CTT CG
Rehner and Samuels 1994; Vilgalys and
Hester 1999
translation elongation factor 1-alpha
(tef1)
EF983F
EF2218R
GCY CCY GGH CAY CGT GAY TTY AT ATG ACA CCR
ACR GCR ACR GTY TG
Rehner and Buckley 2005
RNA polymerase II (rpb2) bRPB2-6F
bRPB2-7.1R
TGG GGY ATG GTN TGY CCY CG
CC CAT RGC YGT YTT MCC CAT DGC
Matheny 2005
glyceraldehyde-3-phosphate
dehydrogenase (gpd)
GPD10F
GPD522R
GCN TCN TGC ACV ACS AAC TG
YCC SRA CTC GTT GTC GTA CC
F.O.P. Stefani, J.A. Berube, and R.C.
Hamelin pers. comm.
actin (act) ACT-181F
Act-875R
GAA CAG GGA GAA GAT GAC C
TCA GCA ATA CCA GGG AAC
F.O.P. Stefani, J.A. Berube, and R.C.
Hamelin pers. comm.
Figure 3. Pileipellis scales hyphae. A. Desarmillaria caespitosa (neotype). B. D. tabescens. Bar = 20 µm. Del. V. Antonín.
MYCOLOGIA 781

≡ Agaricus caespitosus (Berk.) Berk. & M.A. Curtis,
J Linn Soc Bot 10:287. 1869. — Pleurotus caespitosus
(Berk.) Sacc., Syll Fung 5:352. 1887. — Pocillaria caespitosa
(Berk.) Kuntze, Revisio generum plantarum 2:865. 1891. —
Dendrosarcus caespitosus (Berk.) Kuntze, Revisio generum
plantarum 3:463. 1898. — Monadelphus caespitosus (Berk.)
Murrill, Mycologia 3:192. 1911.
= Agaricus monadelphus Morgan, J Cincinnati Soc Nat
Hist 6:69. 1883. — Clitocybe monadelpha (Morgan) Sacc.,
Syll Fung 5:164. 1887.
Typification: USA. OHIO: Waynesville, in woods on the
ground, 8 Sep 1844, T.G. Lea (K, C, type; Pegler 1983).
Material missing (lost) in both herbaria (see notes below).
USA. OHIO: Franklin County, Westerville, 6524 Cherokee
Rose Drive, 40°05′29.75″N, 82°54′03.77″W, alt. 262 m, on
Silver maple (Acer saccharinum) root in the middle of
a lawn, 27 Aug 2018, M. Bellizzi (neotype BRNM 825655;
isoneotype DBG F-030611; designated here).
Selected images: Miller (1981), Lincoff (1992), both as
Armillariella tabescens.
Figure 4. Maximum likelihood phylogeny of a portion of the 28S region with Desarmillaria tabescens and D. caespitosa forming a single
clade with strong bootstrap and posterior probability support (BS/PP). Isolates of both D. tabescens and D. caespitosa are described in
TABLE 1.
782 ANTONÍN ET AL.: DESARMILLARIA CAESPITOSA

Basidiomata caespitose, frequently gregarious, ligni-
colous. Pileus 40‒55 mm wide, convex to plano-convex
when mature, center umbonate, becoming depressed in
age, orbicular in apical view; margin straight, lobed, edge
entire to dentate; hygrophanous and zonate, surface of
the margin smooth; yellowish brown, grayish red (7B3),
reddish white (7A2) with reddish brown (9E3) when
fresh to light brown (6C6; 6D5, 6D6) or brown (6D7)
at the center when dry; squamules light brown (6D3‒
6D4), arranged mainly at the center and around it.
Lamellae close, decurrent, adnate, thick, 3‒5 mm
broad; whitish when young, then reddish gray (8B2‒
8B3, 9B2) when fresh to blond to olive brown (4C4‒
4D4) or brown to light brown (6D6‒6D7) when dry;
edges smooth; lamellulae present, developed in 2‒3 ser-
ies. Stipe 45‒75 mm length, 9‒10 mm wide at the part
attached to the pileus and tapering toward the stipe base
up to 5 mm, central, cylindrical, hollow; annulus absent,
longitudinally distinctly fibrillose to slightly grooved;
white (1A1) with irregular grayish red (7B3) tones
throughout the stipe when fresh, yellowish white to
yellowish gray (4A2‒4B2) and fibrillose when dry; rhi-
zomorphs frequently absent. Taste and smell of fresh
specimens not observed.
Basidiospores (6‒)6.5‒8.5(‒9.5) × (4‒)4.5‒5.5(‒6) μm,
average = 7.5 × 4.9 μm, Q = (1.21‒)1.27‒1.72, average =
1.46, ellipsoid, broadly ellipsoid, less frequently dacryoid,
ovoid, often slightly thick-walled, less frequently thin-
Figure 5. Maximum likelihood phylogeny of the translation elongation factor 1-alpha (tef1) with well-supported nodes (BS/PP)
separating sequences of Desarmillaria tabescens and D. caespitosa. Isolates of both D. tabescens and D. caespitosa are described in
TABLE 1.
MYCOLOGIA 783

walled; white (1A1) to yellowish white (4A2) in deposit.
Basidia 22‒35 × (6‒)7‒10 μm, 4-spored, clavate, clamped.
Basidioles 15‒33 × 3‒8 μm, clavate, (sub)cylindrical, sub-
fusoid, clamped; with scattered, 20‒30 × 5‒11 μm, irregu-
larly clavate, subutriform or (sub)capitate cells intermixed
with basidia and basidioles in hymenium or on edge.
Cheilocystidia (13‒)20‒35(‒40) × (6‒)8‒22 μm, numerous,
forming a sterile band; (broadly) clavate, (broadly) fusoid,
sphaeropedunculate, pyriform, vesiculose, rarely subla-
geniform, rarely with apical wart, sometimes rostrate,
sometimes 2-celled; often slightly thick-walled; subhyme-
nium of cylindrical, gelatinized, branched, thin-walled
hyphae 2‒6 μm wide. Pileipellis a cutis composed of cylind-
rical or subfusoid, thin- to slightly thick-walled, clampless
hyphae 3‒9 μm wide; terminal cells clavate to subcylindri-
cal, up to 12 μm wide; scales composed of chains of
cylindrical, ellipsoid, barrel-shaped, (sub)fusoid, often
short, clampless, mostly slightly thick-walled cells; terminal
cells 15‒60 × (6‒)8‒19(‒23) μm, fusoid, conical, subutri-
form, subcylindrical, subulate, subellipsoid, slightly thick-
walled, obtuse, rarely irregular. Stipitipellis (apex) of
cylindrical, parallel, slightly thick-walled, sometimes
slightly gelatinized hyphae 2‒7 μm wide; terminal cells
(20‒)30‒57(‒90) × (8‒)12‒20(‒35) μm, numerous, clavate,
fusoid, subcylindrical, less frequently 2-celled or in short
chains, ± slightly thick-walled.
Ecology and distribution: In hardwood and mixed
woodlands, orchards, and urban areas, usually on stumps
and buried wood of hardwoods (frequently Quercus but
also Acer, Cornus, Ilex cornuta, Pyracantha, Raphiolepis
indicus, Ulmus parviora, and Prunus), less frequently on
conifers (Araucaria araucana, Juniperus squamata, Pinus,
Thuja occidentalis) and palms (Butia capitata).
Distributed primarily in southeastern, eastern, and central
USA, Mexico, and Central America (Costa Rica).
Basidiomata occurring mostly occurring mostly Jun–
Nov with infrequent records from Mar to May and Dec
(mushroomobserver.org, mycoportal.org).
Other specimens examined: MEXICO. VERACRUZ:
Xalapa, Frente al Asadero cien, stump of Araucaria
araucana, 26 Jul 2009, R. Medel 1899 (XAL
MEX21WF, BRNM 825654).
Desarmillaria tabescens (all as Armillaria tabescens or
A. socialis). BULGARIA. Banja near Nesebar, between
Figure 6. Maximum likelihood phylogeny of the glyceraldehyde-3-phosphate dehydrogenase (gpd) gene highlighting with well-
supported nodes (BS/PP) separating sequences of Desarmillaria tabescens and D. caespitosa. Isolates of both D. tabescens and
D. caespitosa are described in TABLE 1.
784 ANTONÍN ET AL.: DESARMILLARIA CAESPITOSA

Obzor and Slančev Briag, 30 Aug 1983, F. Kotlaba (PRM
831855); Stara Planina, Lovno chanče, 2 Aug 1979, B. Bill &
F. Kotlaba (PRM 821423); Primorsko near Burgas, in the
direction of Mičurin, 21 Sep 1984, S. Hejný (PRM 837720).
CZECH REPUBLIC. Lanžhot, Ranšpurk National Nature
Reserve, on the base of a dead, ca. 300-y-old Quercus stem,
alt. 150 m, 25 Aug 1966, J. Lazebníček & A. Vágner (BRNM
266006); Břeclav, Nové Mlýny, Křivé jezero National
Nature Reserve, alt. 150 m, on stump of Quercus robur, 8
Sep 2005, V. Antonín 05.123, 05.124, and 05.125 (BRNM
695685, 695686, and 695687); ibid., 14 Sep 2005,
L. Jankovský (BRNM 699839). FRANCE. Bourgogne,
Aiserey, Forêt d´Izeure, alt. 200 m, in oak-hornbeam forest
on calcareous clayed soil, on stump of a broadleaved tree,
12 Oct 1992, J.-C. Verpeau (CB M-6803). SLOVAKIA.
Malé Karpaty Mts., Bratislava, Turecký vrch hill, in beech
forest, 25 Sep 1994, I. Kautmanová (BRA 4994); Krupinská
planina Mt., Čabradský Vrbovok, on dead stem of Quercus,
alt. 320 m, 23 Sep 1987, J. Kuthan (BRA 4992); Strážovské
vrchy Mts., Nitrianské Rudno, in the rivulet Rudnianka
valley, on stump of Quercus, alt. 360 m, 14 Jul 1984,
J. Kuthan (BRA 4993); Pohronský Inovec Mts., Čaradice,
xerophytic, broad-leaved forest with Quercus cerris and
Q. petraea, with mixed Pinus, on the base of Quercus
stem, 19 Sep 1987, V. Antonín 87.117 (BRNM 418969);
Zlaté Moravce, Quercus forest, 19 Aug 1975, J. Pokorný
(BRNM 266003). SLOVENIA. Panovec, 13°40′37.3″E, 45°
57′08.9″N, on declining standing tree of Quercus petraea, 3
Sep 2006, G. Seljak (LJF 2856, neotype; BRNM 737504,
isoneotype; designated by Redhead et al. [2012]).
DISCUSSION
Desarmillaria caespitosa was described as Lentinus cae-
spitosus from Waynesville, Ohio, by Berkeley in 1847.
The type specimens were preserved at Kew (K) and the
University of Copenhagen Herbarium (C) (Pegler 1983).
Pegler (1983) revised these materials and synonymized
the name with Armillaria tabescens. This opinion was
supported by Volk and Burdsall (1995). However, both
type specimens are missing at K and C, where it was on
loan several years ago (pers. comm., C and K curators).
Figure 7. Maximum likelihood phylogeny of the actin (act) gene with well-supported nodes (BS/PP) separating sequences of
Desarmillaria tabescens and D. caespitosa. Isolates of both D. tabescens and D. caespitosa are described in TABLE 1.
MYCOLOGIA 785

Therefore, we decided to designate a neotype from
recent material close to the type locality in Ohio.
Desarmillaria tabescens differs from D. caespitosa by the
broader basidiospores [(6.0–)7.5–10(–11) × (4.5–)5–7 μm,
Q = 1.3–1.8, average = 1.3–1.7], narrower cheilocystidia
[(12–)17–41 × 5.0–10 μm], which are often irregular or
mixed with regular, irregular, or coralloid ones, and nar-
rower caulocystidia [(11–)20–50 × 7–14 μm] (Antonín et al.
2006). Desarmillaria tabescens mostly occurs in the south-
ern part of Europe (Guillaumin and Lung 1985). The north-
ern distribution limit runs through central Europe,
including the Czech Republic and Slovakia (Antonín et al.
2006), latitude about 49° north. In Eurasia, D. tabescens
(reported as A. tabescens or A. socialis) has been reported in
association with diverse hosts, primarily in southern
Europe and eastern Asia, where it can cause root disease
or function as an orchid symbiont (Terashita and Chuman
1987; Cha and Igarashi 1995; Ota et al. 1998; Baumgartner
et al. 2011; Guo et al. 2016). It has not been found in the
Southern Hemisphere. Typically in Europe, D. tabescens
has been reported in association with oaks (Quercus), maple
(Acer), silver birch (Betula pendula), strawberry tree
(Arbutus unedo), and introduced eucalypts (Eucalyptus)
(Guillaumin et al. 1993; Antonín et al. 2006).
In the USA, this fungus (identified as A. tabescens or
Clitocybe tabescens) is very common in southeastern states,
west to Texas and Oklahoma, especially as a severe patho-
gen of oaks, silver maple, and peach (Prunus persica) (Cox
2004; Schnabel et al. 2005; Kuo 2017). In North America, it
has a reported distribution in association with diverse hosts
east of the Rocky Mountains and eastern Mexico, where it
frequently causes root disease. As examples, D. tabescens
was found in oak forests of the Ozark Mountains of south-
eastern Missouri and northwestern Arkansas (Bruhn et al.
Figure 8. Maximum likelihood phylogeny of the RNA polymerase II (rpb2) with well-supported nodes (BS/PP) separating Desarmillaria
tabescens and D. caespitosa. Isolates of both D. tabescens and D. caespitosa are described in TABLE 1.
Table 3. Node support (bootstrap and posterior probabilities) for the phylogenetic separation of Desarmillaria tabescens and
D. caespitosa.
Locus
a
Bootstrap Posterior probability
28S — —
tef1 99 1.00
gpd 100 1.00
rbp2 100 1.00
act 100 0.70
a
28S = nuclear large ribosomal subunit 28S rDNA; tef1 = translation elongation factor 1-alpha; gpd = glyceraldehyde-3-phosphate dehydrogenase; rpb2 = RNA
polymerase II; act = actin.
786 ANTONÍN ET AL.: DESARMILLARIA CAESPITOSA

2000; Kelley et al. 2009). In the southeastern USA,
D. tabescens was reported to cause root disease of sand
pine (Pinus clausa), peach, Chinese holly (Ilex cornuta),
singleseed juniper (Juniperus squamata), Indian hawthorn
(Raphiolepis indicus), northern white cedar (Thuja occiden-
talis), and pindo palm tree (Butia capitata) (Ross 1970;
Schnabel et al. 2005, 2006). Because sequences from the
isolates reported as A. tabescens from southeastern USA,
including some sequences of isolates from Schnabel (2005),
cluster within the same clade as D. caespitosa, it seems
probable that the abovementioned hosts and root diseases
are associated with D. caespitosa as it is presently recog-
nized. Desarmillaria caespitosa was found causing root dis-
ease on an ornamental monkey puzzle tree (Araucaria
araucana) in Veracruz, Mexico (Kim et al. 2010, as
A. tabescens).
In Japan, D. tabescens (as A. tabescens) has been reported
from Kyushu and central and southern parts of Honshu
(Ota et al. 1998) on ornamental cherries (e.g., Prunus
hybrids) in urban areas (Hasegawa 2005). It is also men-
tioned from China, where it is considered a pathogen on
economically valuable trees, including woody ornamentals
and fruit trees (Qin et al. 2007). As examples in eastern Asia,
D. tabescens has been reported on diverse hardwood hosts,
such as Prunus, Quercus, Populus, and Salix (Lee and Cho
1977; Ota et al. 1998; Qin et al. 2007), and in symbiotic
association with orchids, such as Gastrodia elata (Cha and
Igarashi 1995; Guo et al. 2016) and Galeola septentrionalis
(Terashita and Chuman 1987; Ota et al. 1998). However,
this Asian taxon may represent a separate species according
to phylogenetic analysis (Park et al. 2018).
Desarmillaria ectypa is distinctly different from both
D. caespitosa and D. tabescens by the single growing basi-
diomata with an apparently smooth pileus and, especially,
by the nonlignicolous habitat in marshes and peat bogs
(e.g., Zolciak et al. 1997; Ohenoja 2006). It occurs in
Eurasia (e.g., Legon and Henrici 2005; Ota et al. 2005;
Ohenoja 2006; Stasińska 2015; Klopfenstein et al. 2017),
but not in North America or the Southern Hemisphere.
This study is not the only case of North American/
European vicariance between species of similar mor-
phology. Similar examples can be also found in other
fungal groups, e.g., Hymenochaetales (Inonotus ander-
sonii (Ellis & Everh.) Černý [America; A]/I. krawtzewii
(Pilát) Pilát [Europe; E]; Zhou et al. 2014); Russulales
(Heterobasidion irregulare Garbel. & Otrosina [A]/
H. annosum (Fr.) Bref. [E]; Otrosina and Garbelotto
2010); Polyporales (Resinoporia sitchensis (D.V. Baxter)
Audet [A]/R. piceata (K. Runnel, Spirin & Vlasák) Audet
[E]; Spirin et al. 2015; Resinoporia is the former Antrodia
crassa group); Polyporales (Sparassis americana R.H.
Petersen [A]/S. crispa (Wulfen) Fr. [E]; Hughes et al.
2014); and Agaricales (Hohenbuehelia angustata (Berk.)
Singer [A]/H. wilhelmii Consiglio & Setti [E]; Consiglio
and Setti 2017). Based on the vicariance paradigm
observed in the present and previous studies,
Armillaria/Desarmillaria, and other members of the
Basidiomycota with similar species in Europe, North
America, Asia, and/or other regions warrant compara-
tive morphological, ecological, and phylogenetic ana-
lyses to determine the appropriate taxonomic status of
the vicariant species.
ACKNOWLEDGMENTS
The authors wish to thank the curators of the herbaria BRA, C,
CB, K, and XAL for information about collections or their loans
respectively. The authors also thank the Sam Mitchel Herbarium
of Fungi at Denver Botanic Gardens. The authors also thank Luis
Alberto Parra Sanchez (Aranda de Duero, Spain) for valuable
nomenclatural comments; K. Otto, Dr. J. Ibarra-Caballero, and
B. Lalande for excellent laboratory assistance; and M. Bellizzi for
assistance in collections. The authors also wish to thank to all
reviewers and editors of Mycologia. Mention of trade names does
not constitute endorsement by the United States Department of
Agriculture (USDA) Forest Service.
FUNDING
The studies of the A.V. were enabled by institutional support
of long-term conceptual development of research institutions
provided by the Ministry of Culture of the Czech Republic
(MK000094862). Participation of M.T. was supported by the
European Regional Development Fund, Project Phytophthora
Research Centre CZ.02.1.01/0.0/0.0/15_003/0000453. Funding
for baseline studies of Armillaria identification and phyloge-
netics was provided by the USDA Forest Service, Forest Health
Protection Service, Special Technology Development
Program, and Joint Venture Agreements 15-JV-11221633-
160, 19-JV-11221633-093, and 20-JV-11221633-141 (to J.E.S.).
ORCID
Vladimír Antonín http://orcid.org/0000-0002-6000-7285
Jane E. Stewart http://orcid.org/0000-0001-9496-6540
Rosario Medel Ortiz http://orcid.org/0000-0003-3351-
991X
Mee-Sook Kim http://orcid.org/0000-0001-7073-6708
Pierluigi (Enrico) Bonello http://orcid.org/0000-0002-
7207-7651
Michal Tomšovský http://orcid.org/0000-0002-9505-6175
Ned B. Klopfenstein http://orcid.org/0000-0002-9776-3973
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