Cantharellaceae of Guyana I: New species, combinations and distribution records of Craterellus and a synopsis of known taxa

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DOI: 10.3852/11-412 · Source: PubMed
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Abstract
Members of the Cantharellaceae (Cantharellales, Basidiomycota) are common ectomycorrhizal associates of the leguminous genus Dicymbe in the Pakaraima Mountains of Guyana. Currently eight distinct species or morphospecies are recognized in Craterellus Pers. or Cantharellus Adans. ex Fr. from Guyanese Dicymbe-dominated forests. We evaluated the systematics of these taxa using phylogenetic analyses of DNA sequence data from the nuclear ribosomal regions of the internal transcribed spacer (ITS) and 28S large subunit (LSU). The results of these analyses along with careful assessment of morphology allow us to described two new species, Craterellus atratoides sp. nov. and Craterellus strigosus sp. nov., re-describe Craterellus atratus (Corner) Yomyart et al. based on new material from Guyana, and propose a new combination in Craterellus for Cantharellus pleurotoides T.W. Henkel, Aime & S.L. Mill. Macroscopic illustrations are provided for two additional cantharelloid morphospecies confirmed in Craterellus, as well as the regionally endemic Cantharellus guyanensis Mont. Macromorphological, micromorphological, and habitat data are provided for C. atratoides, C. strigosus, and C. atratus, and ITS and LSU sequence data are provided for each of the eight known Guyanese taxa.
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Cantharellaceae of Guyana I: new species, combinations and distribution
records of
Craterellus
and a synopsis of known taxa
Andrew W. Wilson
Chicago Botanic Garden, Plant Conservation Science,
Glencoe, Illinois 60022
M. Catherine Aime
Department of Plant Pathology & Crop Physiology,
Louisiana State University Agricultural Center, Baton
Rouge, Louisiana 70803
Janina Dierks
Department of Biological Sciences, Humboldt State
University, Arcata, California 95521
Gregory M. Mueller
Chicago Botanic Garden, Plant Conservation Science,
Glencoe, Illinois 60022
Terry W. Henkel
1
Department of Biological Sciences, Humboldt State
University, Arcata, California 95521
Abstract
: Members of the Cantharellaceae (Canthar-
ellales, Basidiomycota) are common ectomycorrhizal
associates of the leguminous genus
Dicymbe
in the
Pakaraima Mountains of Guyana. Eight distinct
species or morphospecies currently are recognized
in
Craterellus
Pers. or
Cantharellus
Adans. ex Fr. from
Guyanese
Dicymbe
-dominated forests. We evaluated
the systematics of these taxa with phylogenetic
analyses of DNA sequence data from the nuclear
ribosomal regions of the internal transcribed spacer
(ITS) and 28S large subunit (LSU). The results of
these analyses along with careful assessment of
morphology let us described two new species,
Craterellus atratoides
sp. nov. and
Craterellus strigosus
sp. nov., redescribe
Craterellus atratus
(Corner)
Yomyart et al. based on new material from Guyana,
and propose a new combination in
Craterellus
for
Cantharellus pleurotoides
T.W. Henkel, Aime & S.L.
Mill. Macroscopic illustrations are provided for two
additional cantharelloid morphospecies confirmed in
Craterellus
, as well as the regionally endemic
Cantha-
rellus guyanensis
Mont. Macromorphological, micro-
morphological and habitat data are provided for
C.
atratoides
,
C. strigosus
and
C. atratus
, and ITS and
LSU sequence data are provided for each of the eight
known Guyanese taxa.
Key words:
Cantharellaceae, chanterelles,
Di-
cymbe
, ectomycorrhiza, Guiana Shield, tropical fungi
I
NTRODUCTION
Species of the ectomycorrhizal (ECM) genera
Crater-
ellus
Pers. and
Cantharellus
Adans. ex Fr. (Cantharel-
laceae, Cantharellales, Basidiomycota) are well repre-
sented in northern temperate zones but also occur in
the tropics. Of the ,365 currently described species
in the two genera worldwide (discounting infraspe-
cific taxa), ,90 appear to have tropical distributions
and most of these are paleotropical. In the more
speciose
Cantharellus
,300 species are described
worldwide with ,76 tropical species; ,34 of these
are known from tropical Africa, including the Congo
Basin, miombo woodlands and Madagascar (e.g.
Heinemann 1958, 1966; Eyssartier and Buyck 1999;
Buyck et al. 2000) and ,31 from southeastern Asia,
including Malaysia, Borneo, Philippines, Sri Lanka,
Java, New Guinea and New Caledonia (e.g. Corner
1966, 1969; Ducousso et al. 2004).
Craterellus
has ,65
species described worldwide, with , 14 tropical
species mostly described more than 45 y ago, half of
which are paleotropical (Corner 1966).
Relative to the Paleotropics knowledge of Cantha-
rellaceae in the Neotropics is limited. Seven species of
Cantharellus
and four of
Craterellus
were recorded
from the South American lowland tropics, primarily
from Brazil, Guyana, French Guiana and Venezuela
(e.g. Montagne 1855, Corner 1966, Singer et al.
1983). Singer (1963) described an additional
Crater-
ellus
species from montane Colombian oak woods.
Several new species of
Cantharellus
recently have
been described from Costa Rican or Colombian oak
woods (Petersen and Mueller 1992, Eyssartier et al.
2003), Guyana (Henkel et al. 2006) and eastern Brazil
(Petersen and Mueller 1992, Wartchow et al. 2012). In
extratropical southern South America at least one
species of
Cantharellus
is known from
Nothofagus
forests (Petersen and Mueller 1992). Only two new
species of
Craterellus
have been described from the
Neotropics in recent decades (Wu and Mueller 1995,
Henkel et al. 2009).
In the central Guiana Shield of northeastern South
America,
Craterellus
and to a lesser extent
Cantha-
rellus
species are well represented in primary rain-
forests dominated by ECM canopy trees of the genus
Dicymbe
(Fabaceae subfam. Caesalpinioideae) (Hen-
kel et al. 2012). Collecting during 15 y in Guyana’s
Pakaraima Mountains has documented
Cantharellus
guyanensis
Mont.,
Cantharellus pleurotoides
T.W.
Henkel, Aime & S.L. Mill., and
Craterellus excelsus
Submitted 10 Dec 2011; accepted for publication 30 Apr 2012.
1
Corresponding author. E-mail: twh5@humboldt.edu
Mycologia,
104(6), 2012, pp. 1466–1477. DOI: 10.3852/11-412
#
2012 by The Mycological Society of America, Lawrence, KS 66044-8897
1466
T.W. Henkel & Aime, plus five additional cantharelloid
morphotaxa (Henkel et al. 2006, 2009, 2011). Four of
these additional taxa are previously undescribed
Craterellus
species. Another taxon is similar to
Cantha-
rellus atratus
Corner originally described from Brazil.
Herein we discuss the taxonomic placement of
Guyanese Cantharellaceae based on morphology,
molecular phylogenetic analysis and geographic
distribution. We describe two new species,
Craterellus
atratoides
sp. nov. and
Craterellus strigosus
sp. nov.,
and propose a new combination in
Craterellus
for
Cantharellus pleurotoides
. We also provide a redescrip-
tion and new distribution record for
Craterellus
atratus
(Corner) Yomyart et al. DNA sequence data
from the internal transcribed spacer (ITS) and large
subunit (28S) of the nuclear ribosomal repeat justify
placement of each of these four species in
Craterellus
.
Two additional cantharelloid morphospecies oc-
curred within
Craterellus
, and
Cantharellus guyanen-
sis
, a new record for Guyana, was identified as the sole
member of
Cantharellus
in the Guyanese assemblage.
These three taxa are presented here in the phyloge-
netic analyses and illustrated. In a forthcoming paper
we will formally describe or redescribe these taxa and
provide a key to the Neotropical Cantharellaceae.
M
ATERIALS AND METHODS
Collections.—
They were made during the May–Jul rainy
seasons of 2000, 2001, 2002, 2006 and 2010 from the Upper
Potaro River Basin, within a 4 km radius of a permanent
base camp at 5u18904.80N, 59u54940.40W, 710 m (Henkel
et al. 2011). Basidiomata were collected from forests dominat-
ed by
Dicymbe corymbosa
Spruce ex Benth. Macromorphologi-
cal features of basidiomata were described fresh in the field.
Colors were described subjectively and coded according to
Kornerup and Wanscher (1978), with color plates noted in
parentheses. Fungi were field-dried with silica gel.
Micromorphological features of fresh specimens were
examined with an EPOI field microscope with light optics;
dried specimens were examined with an Olympus BX51
microscope with light and phase contrast optics. For
basidiospores, basidia, hyphal features and other structures
and at least 20 individual structures were measured.
Rehydrated fungal tissue was mounted in H
2
O, 3% KOH
and Melzer’s solution. Line drawings were made with
tracing paper with digital photomicrographs and modified
with Photoshop CS5 (Adobe, San Jose, California). Guyana
specimens were deposited in the following herbaria: BRG,
University of Guyana; HSU, Humboldt State University;
LSUM, Louisiana State University (Mycology); NY, New
York Botanical Garden (Holmgren et al. 1990). Isotype
specimens of
Cantharellus hystrix
Corner and
Cantharellus
atratus
Corner were examined at the Royal Botanic Garden
Edinburgh Herbarium (E). A specimen of
Craterellus
orinocensis
Pat. & Gaillard was examined from the Tennes-
see Fungus Herbarium (TENN).
DNA extraction, amplification, sequencing and phylogenetic
analyses.—
DNA extractions of Cantharellaceae specimens
from Guyana and elsewhere were performed with a
QIAGEN DNeasy Plant Mini Kit (QIAGEN USA, Valencia,
California; http://www.qiagen.com/). Polymerase chain
reactions (PCR) and cycle sequencing were performed to
obtain sequences of nuclear ribosomal DNA from the
internal transcribed spacer (ITS) and the 28S large subunit
(LSU), with primer pairs ITS1F/ITS4 (Gardes and Bruns
1993, White et al. 1990) and LR0R/LR5 (Vilgalys and
Hester 1990) respectively. For PCR reactions the following
reagents were combined per 25
mL reaction: 12.5 mL GoTaq
Master Mix (Promega Corp., Madison Wisconsin), 9
mL PCR
H
2
O, 1.25 mL each of forward and reverse primers and 1 mL
DNA template. Thermal-cycler protocols for the ITS were
94 C initial denature for 2 min. These steps repeated 323:
denature at 94 C for 30 s, anneal at 55 C 30 s, extension at
72 C 1 min; followed by a final extension of 72 C 5 min and
a hold at 14 C indefinitely. The LSU PCRs followed the
same protocols except with a 50 C annealing temperature.
Strong, single-copy PCR product was sequenced directly.
Nearly 60% of the sequences generated had to be cloned
due to intragenomic heterogeneity or weak amplification.
Cloned PCR amplicons were generated with the TA or
TOPO TA Cloning Kits (Invitrogen, Carlsbad, California).
Fresh, cleaned PCR product was ligated to pCR 2.1 vectors
that then were used to transform MAX efficiency DH5a-T1
chemically competent cells of
Escherichia coli
. Approximate-
ly 75 mL transformed cells in liquid SOC medium
(Invitrogen) were incubated up to 24 h at 37 C on Luria-
Bertani (LB) agar prepared with 50
mg/mL of kanamycin
and 50
mL 50 mg/mL X-gal in dimethylformamide.
Transformed colonies were screened with PCR with primers
M13F and M13R (Invitrogen) followed by gel electropho-
resis (1% agarose) with a 1 kb step ladder. A minimum of
three amplicons of the expected size were chosen for
sequencing.
Sequences were processed and assembled with Codon-
Code Aligner 3.5.7 (CodonCode Corp., Dedham, Massachu-
setts; http://www.codoncode.com/). Assembled nucleotide
sequence contigs of ITS and LSU regions were used in
database BLAST queries of GenBank (www.ncbi.nlm.nih.
gov/) and UNITE (unite.ut.ee/; Ko˜ljalg et al. 2005). Query
sequences that produced the closest match to sequences
identified as either
Cantharellus
or
Craterellus
were used in
preliminary alignments and phylogenetic analyses. Addition-
al ITS and LSU sequences of primarily northern temperate
Cantharellaceae species available on GenBank were included
to assemble datasets with high intrafamilial inclusivity.
Specimen and GenBank information for all taxa used in
the study are provided (S
UPPLEMENTARY TABLE I).
Initial alignment of datasets was performed with MUSCLE
(Edgar 2004) followed by manual alignments using Mac-
Clade 4.07 (Maddison and Maddison 2005). Maximum
likelihood (ML) and ML bootstrapping analyses were
performed with RAxML (Stamatakis 2006), which was
implemented on the CIPRES web portal (Miller et al. 2009)
with 1000 bootstrap replicates to generate bootstrap statistics.
Bayesian analyses were performed with MrBayes 3.1.3
(Ronquist and Huelsenbeck 2003) implemented on the
WILSON ET AL.: CANTHARELLACEAE OF GUYANA 1467
CIPRES web portal. These analyses used four chains,
sampling every 1000th tree for 10 000 000 generations. All
other parameters were used at the default settings. In each
analysis, two MCMC analyses were run, which produced two
tree files with ,10 000 trees each. The first one-tenth trees
was removed as burn-in. Both tree files were combined and
a50% majority rule tree was performed in PAUP* 4.0
(Swofford 2003) to ascertain the bayesian posterior proba-
bilities for each dataset.
RESULTS
Phylogenetic analyses.—
ITS and LSU datasets each
consisted of 53 (22 original and 31 from GenBank)
and 72 (26 original and 46 from GenBank) samples
or operational taxonomic units (OTUs), with se-
quences ranging from 269 bp (CLU87986)-925 (
C.
excelsus
TH7515) to 347 bp (DQ202680)-1436
(EF546767). The fully aligned ITS and LSU datasets
consisted respectively of 2390 and 1055 characters.
Despite the difficulties in aligning ribosomal sequence
data among Cantharellaceae taxa, no sequence data
were removed in an effort to preserve the maximum
amount of intraspecies sequence homology among the
Guyana specimens.
Phylogenetic analyses of ITS and LSU sequences
corroborated the monophyly of
Cantharellus
and
Craterellus
within the Cantharellaceae as noted for
example in Moncalvo et al. (2006). Independent
analyses of each gene region resolved the Guyanese
material into eight species-level clades in
Cantharellus
and
Craterellus
, from 21
Dicymbe
-associated Cantha-
rellaceae specimens (F
IG. 1). The clades representing
these species were topologically congruent between
the ITS and LSU trees.
The
Cantharellus
specimens in this study were
represented by 19 ITS and 35 LSU sequences
(S
UPPLEMENTARY TABLE I). The genus was resolved
with 100% maximum likelihood bootstrap support
(MLB) and 1.0 bayesian posterior probability (PP) in
both datasets (F
IG. 1a, b). Three of the Guyana
FIG. 1. ITS (a) and LSU (b) maximum likelihood phylogenies from RAxML analysis of
Cantharellus
and
Craterellus
including tropical and north temperate taxa, depicting a clear separation of
Cantharellus
and
Craterellus
within the
Cantharellaceae. The Guyanese taxa
C. excelsus
,
Craterellus
sp. 1,
C. strigosus
,
C. atratus
,
C. atratoides
,
C. pleurotoides
and
Craterellus
sp. 2 each consisted of multiple collections and are nested within
Craterellus
as distinct species-level taxa (in
boldface).
Cantharellus guyanensis
is the only Guyanese taxon within
Cantharellus
. Maximum likelihood bootstrap
percentages are above the nodes and Bayesian posterior probabilities are below the nodes. Type specimens of new species
described here are indicated next to the specimen name. All taxa with sequences obtained from GenBank or UNITE are
indicated with italics; otherwise sequences were generated in this study.
1468 MYCOLOGIA
specimens identified previously as
Cantharellus guya-
nensis
(MCA981, MCA3112, TH9201) resolved as a
strongly supported species-level taxon (100% MLB,
1.0 PP) within
Cantharellus
in both analyses (FIG. 1).
The
Craterellus
specimens in this study are repre-
sented by 28 ITS and 37 LSU sequences (S
UPPLEMEN-
TARY TABLE
I). The genus was resolved in both ITS
(64% MLB, 0.98 PP) and LSU (100% MLB and 1.0
PP) analyses and identified seven species-level taxa
from the Guyanese specimens (F
IG. 1). These includ-
ed the previously described
C. excelsus
, which was
resolved in close relationship to the undescribed
morphospecies
Craterellus
sp. 1, each with three
specimens. These two morphologically similar taxa
are closely related as indicated by the supported
monophyly of the their clade under analysis of both
ITS (70% MLB, 0.61 PP) and LSU (99% MLB, 1.0
PP).
Craterellus excelsus
and
Craterellus
sp. 1 each were
supported with 100% MLB and 1.0 PP in both the ITS
and LSU analyses (F
IG. 1).
Another two-taxon clade was identified in
Crater-
ellus
containing the morphologically similar, dimin-
utive gray-brown species
C. atratus
and
C. atratoides
sp.nov.(FIG. 1a, b). This clade was weakly supported
in the ITS analysis (0.7 PP; F
IG. 1a) but strongly
supported in the LSU analysis (98% MLB, 1.0 PP;
F
IG. 1b). The three specimens of Guyanese
C.
atratus
were morphologically consistent with the
Brazilian
Cantharellus atratus
originally described by
Corner (1966) and subsequently by Singer et al.
(1983) and recently combined into
Craterellus
by
Yomyart et al. (2011). The second species of this two-
taxon clade, composed of three specimens, differs in
several key morphological features from
C. atratus
,
is distinct at the species-level in both phylogenies
and is described here as a new species,
Craterellus
atratoides
sp. nov.
Another species, represented by MCA1750 and
TH9204, was not closely allied with any other species
in both the ITS and LSU analyses (F
IG. 1) and is
described here as
Craterellus strigosus
sp. nov. At the
species level,
Craterellus
cf.
atratus
,
C. atratoides
and
C. strigosus
each were supported at 100% MLB and
1.0 PP in both phylogenies.
Of the remaining two species resolved by the
phylogenetic analyses,
Cantharellus pleurotoides
is
FIG. 2. Previously described and undescribed Cantharellaceae taxa from Guyana. a.
Craterellus excelsus
T.W. Henkel &
Aime (type; from Henkel et al. 2009). b.
Cantharellus guyanensis
Mont. (
Henkel 9201
). c.
Craterellus
sp. 1 (
Henkel 9075
). d.
Craterellus
sp. 2 (
Henkel 9205
). e.
Craterellus pleurotoides
(T.W. Henkel, Aime & S.L. Mill.) A.W. Wilson (
Henkel 9220
). Bars 5
10 mm.
WILSON ET AL.: CANTHARELLACEAE OF GUYANA 1469
represented by specimens MCA3124 and TH9220 and
supported at the species level with 100% MLB and 1.0
PP in both ITS and LSU analyses (F
IG. 1).
Cantha-
rellus pleurotoides
clearly was nested in
Craterellus
,
forming the basis for its new combination reported
below. The remaining taxon recognized by collectors
as the morphologically distinct
Craterellus
sp. 2,
represented by specimens MCA3186 and TH9250,
was strongly supported at the species level in close
relation to
C. pleurotoides
in the phylogenetic analyses
(F
IG. 1).
Preliminary work has determined that
Craterellus
sp. 1, allied with
C. excelsus
, and
Craterellus
sp. 2,
allied with
C. pleurotoides
, are likely new to science;
their formal description and a new description for
Cantharellus guyanensis
will be provided in a forth-
coming paper. Basidiomata of all previously described
and currently undescribed Guyanese Cantharellaceae
are illustrated (F
IG. 2).
T
AXONOMY
Craterellus atratoides T.W. Henkel, Aime et A.W.
Wilson, sp. nov F
IGS.3,4
MycoBank MB564237
Craterellus atratoides
similis
Cantharelli atrati
Corner
simili griseofusco colore, gracili cylindraceo stipite, bene
definito pileo, et manifesto decurrentique hymenophoro;
sed multo longiore stipite (25–70 vs. 8–30 mm), longioribus
basidiis (79–111 vs. 54–67
mm), in omnibus glabris and
perforatis pileis stipitibusque, griseocaesio hymenophoro,
et terrestricola ubi fructificans differt.
Pileus 5–22.5 mm broad, 2.5–10 mm tall, initially
planate with slightly downturned margin, with age
becoming irregularly convex to uplifted with broadly
wavy, down-curving margin, then strongly centrally
depressed and perforate, dark grayish brown (8F4–
9F4), transitioning to brown toward margin to light
grayish tan at extreme margin; margin finely irregu-
larly crenulate under hand lens, occasionally splitting,
surface entirely glabrous, innately radially fibrillose
under hand lens, moist; trama concolorous. Hyme-
nophore continuous over lower side of pileus and
descending stipe 1–5 mm with well demarcated but
somewhat irregular lower edge, light bluish gray
(19D2–19D3), initially smooth, thickening with age
and becoming irregularly rugulose, hispid under
hand lens due to projecting basidia, drying dark gray.
Stipe 25–70 3 1.5–3 mm, equal, flaring to 2–4 mm
wide under fertile apex, concolorous (8F4–8F5) over
apical two-thirds, somewhat lighter-concolorous over
basal one-third, glabrous, with age flattening and
subcanaliculate, basal mycelium wanting; trama conco-
lorous with hollow core. Primordia filiform-acuminate,
0.5–1 mm tall. Odor none; flavor mildly fungoid,
indistinct. Basidiospores (10)10.8–12(13) 3 7.1–9
mm,
Q range 5 1.2–1.5, Q mean 5 1.4, ellipsoid, smooth,
hyaline to pale yellow in KOH, inamyloid, uniguttulate
or rarely multiguttulate with granulose epiplasm; wall
0.3–0.5
mm thick; hilar appendix 0.7–1 mm long.
Basidia (66)79–111 3 (4.9)7.4–9.9(10.1)
mm, 7.7–
10.1(12.4)
mm wide at apex, 4.9–7.4 m m at base,
FIG. 3. Basidiomata of
Craterellus atratoides
(HOLO-
TYPE;
Henkel 9232
). Bar 5 10 mm.
FIG. 4. Basidia and basidiospores of
Craterellus atratoides
(HOLOTYPE;
Henkel 9232
). Bar 5 10 mm.
1470 MYCOLOGIA
subcylindrical, wall thin, hyaline to faintly pale yellow
in KOH, devoid of obvious contents; sterigmata (2)3–
4–5, (3.7)4.5–6.7(8.6)
mm long, 1.5–2.5 mmwideat
base, somewhat curving. Basidioles numerous, cylin-
drical, densely multiguttulate, pale yellowish brown in
KOH. Cystidia none. Hymenium in transverse section
103–247
mm thick, light brown in KOH. Pileipellis a
tightly interwoven mass of largely periclinal to sub-
anticlinal hyphae, in mass brown in KOH; terminal
elements of nearly equal lengths, undifferentiated and
rounded at apex; individual hyphae hyaline to faintly
yellow in KOH, devoid of obvious internal contents or
occasionally guttulate; cells 24.7–64.2 3 6.2–11.1
mm.
Pileus tramal hyphae smooth, hyaline in KOH,
branching occasionally, devoid of obvious internal
contents or with numerous small guttules of various
sizes; cells 44.5–108.7 3 3.7–12.1(14.8)
mm, somewhat
inflating, constricted at septum when inflated; wall
distinct, 1–1.2
mm thick; secondary septation absent.
Stipitipellis composed of densely interwoven to sub-
parallel hyphae arranged subanticlinally and with
terminal elements often more periclinal, light brown
in KOH; individual hyphae pale yellow brown in KOH,
devoid of obvious internal contents; cells 37.0–74.1 3
4.9–7.4
mm; terminal elements undifferentiated and
rounded at apex, or rarely slightly inflated near apex
and subclavate. Stipe tramal hyphae smooth, hyaline to
faintly yellow in KOH, occasionally branching, occa-
sionally constricted at septum if inflated, devoid of
obvious contents or scattered guttulate; cells 44.5–
111.2 3 3.7–11.1
mm. Clamp connections abundant on
hyphae of all tissues.
Holotype: Henkel 9232
(BRG; ISOTYPE: HSU; NY )
Habit, habitat and distribution:
Solitary to scattered
on the root/humus mat of forest floor under
Dicymbe
corymbosa
on white sand soils; known only from the
type locality in the Upper Potaro Basin of Guyana.
Etymology:
‘‘atratoides’’ refers to the macroscopic
resemblance of the species to
Craterellus atratus
.
Specimens examined:
GUYANA: Region 8, Potaro-Siparuni:
Pakaraima Mountains, Upper Potaro River Basin, ,15 km
east of Mt Ayanganna; 1.5 km northeast of base camp in
mixed
Dicymbe
-
Micrandra
forest on white sand soils, 28 May
2010,
Henkel 9232
(HOLOTYPE: BRG; ISOTYPE: HSU;
NY); vicinity of base camp in
Dicymbe
forest, 17 Jun 2002,
Henkel 8473
(BRG; HSU); ,3 km southwest of base camp
vicinity of
Dicymbe
plot 3, 21 Jun 2000,
Aime 1313
(BRG;
LSUM). VENEZUELA. AMAZONAS: Atabapo, 9 Aug 1987,
Halling 5462
,
Craterellus orinocensis
Pat. & Gaillard!,
(TENN 58453).
Commentary: Craterellus atratoides
is recognized in
the field by the slender, pileate-stipitate basidiomata
with a long stipe relative to pileus width, dark grayish
brown pileus and stipe with glabrous pelli, smooth to
rugulose, decurrent, bluish gray hymenophore and
solitary to scattered terrestrial fruiting habit in
Dicymbe
forest occurring on white sand soils.
While the pileate-stipitate habit and presence of
clamp connections might have led to placement of
this species in
Cantharellus
under traditional mor-
phological taxonomy (Corner 1966), our molecular
data clearly indicate that
C. atratoides
is best placed in
Craterellus
(FIG. 1). The early development of conical
primordia with subsequently perforate pilei in mature
basidiomata of
C. atratoides
, in which the perforation
is continuous with the hollow core of the stipe, are
consistent with both the traditional concept of
Craterellus
(Corner 1966) and also the modern, in
which absence of clamp connections was not consid-
ered universal in the genus (Dahlmann et al. 2000).
Species placed in
Cantharellus
subgen.
Phaeo-
cantharellus
by Corner are gray to brown, have
occasionally hollow stipes and clamp connections
(Corner 1966). Among these,
C. atratoides
is most
similar to the sympatric
C. atratus
reported here,
sharing similar coloration, the slender cylindrical stipe,
well defined pileus and sharply demarcated decurrent
hymenophore.
Craterellus atratoides
is easily distin-
guished from
C. atratus
by its much longer stipe (25–
70 vs. 8–30 mm), longer basidia (79–111 vs. 54–67
mm),
consistently glabrous pileus and stipe, bluish gray
hymenophore and terrestrial fruiting habit. The
Bornean
Cantharellus fuligineus
Corner is notably
similar to
C. atratoides
in coloration and relative sizes
of the elongated, subcylindrical stipe and well defined,
small pileus with down-curved margin but differs
fundamentally in its absence of clamp connections,
smaller basidiospores (7.5–8.5 3 5–6 vs. 10.8–12 3 7.1–
9
mm) and presence of well developed gill folds.
Cantharellus albomarginatus
(Coker) Corner from
North Carolina, while dark overall, differs from
C.
atratoides
in its blackish, subsquamulose pileus with
abruptly white margin and smaller basidiospores (7–
8.5 3 4.2–6 vs. 10.8–12 3 7.1–9
mm).
Among the few cantharelloid species described
from the lowland South American tropics,
Craterellus
orinocensis
resembles
C. atratoides
in basidioma size
and coloration but differs in its more fully infundib-
uliform basidioma with fascicles of hairs on the stipe,
much shorter (55–60 vs. 79–111
mm), consistently six-
sterigmate basidia and lack of clamp connections
(Patouillard and Gaillard 1888, Corner 1966, Singer
et al. 1983). Examination of a collection identified as
C. orinocensi s
from Atabapo, Venezuela (Halling
5462, TENN 058453) corroborated differences be-
tween
C. orinocensis
with
C. atratoides
in the former’s
much broader infundibuliform stature and yellow-
drying vs. gray-drying hymenium, lack of clamp
connections and decidedly smaller basidiospores
(6.2–8.6 3 4.9–6.9 vs. 10.8–12 3 7.1–9
mm).
W
ILSON ET AL.: CANTHARELLACEAE OF GUYANA 1471
Craterellus strigosus T.W. Henkel, Aime et A.W.
Wilson, sp. nov. F
IGS.5,6
MycoBank MB564238
Craterellus strigosus
similis
Cantharelli hystricis
Corner
parvo (,20 mm) pileo instructo cum densis strigosis
trichomatibus, atrofuliginosis coloribus, laevi decurrenti
hymenophoro, et aequali, parvo, solido stipite; sed griseo-
fusco hymenophoro non violaceosuffuso, longiore stipite
(13–33 mm vs. 12 mm), stipo cum dense-aggregatis strigosis
pilis trichomatibus, et (2–3–4–5 vs. 4–6) sterigmatibus per
basidium differt.
Pileus 4–18 mm broad, 2–9 mm tall, initially convex
to subcampanulate and flattened across the apex,
maturing to more regularly campanulate to plano-
convex and then narrowly centrally depressed and
somewhat out-flaring toward margin, dark brown
(7F4–7F5), lighter concolorous at margin, lacking a
distinct whitish band, surface with erect agglutinated
strigose-fibrillose scales throughout, these more con-
centrated over the disk and 0.75–1 mm tall, otherwise
appressed radially fibrillose to subrivulose near
margin, submoist; extreme margin under hand lens
finely crenulate and occasionally splitting; trama
concolorous, subsolid. Hymenophore continuous
over lower side of pileus and descending stipe 1–
3 mm with well demarcated but irregular lower edge,
gray with brownish overtones (7E2–7E3) throughout,
smooth to finely rugulose, not thickening substantial-
ly, 0.1–0.3 mm thick in section, under hand lens
hispid due to projecting basidia. Stipe 13–33 mm long
up to hymenophore, 1–1.5 mm wide centrally, equal
over basal four-fifths, flaring to 1.5–4 mm wide under
fertile apex, concolorous with pileus, with dense,
brown strigose scales throughout, scales 0.75–1.5 mm
tall, lighter gray-brown at apices, slightly more concen-
trated near stipe base; trama concolorous, subsolid,
lacking a hollow core. Primordia filiform-acuminate.
Odor none; flavor minimal, indistinct. Drying non-
hygrophanous to dark brown. Basidiospores (7)8–10 3
5.9–8(8.5)
mm, Q range 5 1.1–1.5, Q mean 5 1.3,
broadly ellipsoid, smooth, hyaline in KOH, inamyloid,
with one large guttule with uniform, finely granulose
contents, infrequently multiguttulate; wall 0.4–0.8
mm
thick; hilar appendix 0.9–1.2
mm long. Basidia 52–70 3
5.2–9.9
mm, (6.2)7.2–10.4(12.1) mm wide at apex,
(3)3.7–9.6
mm at base, subcylindrical to nearly cylin-
drical, hyaline in KOH, devoid of obvious contents or
occasionally finely granulose; sterigmata 2–3–4–5,
(3.7)4.4–5.7(7.4)
mm long, 1.5–2.5 mm wide at base,
somewhat curving. Basidioles numerous, cylindrical,
non-guttulate, with opaque, finely granulose contents.
FIG. 5. Basidiomata of
Craterellus strigosus
(HOLOTYPE;
Henkel 9204
). Bar 5 10 mm.
FIG. 6. Micromorphological features of
Craterellus
strigosus
(HOLOTYPE;
Henkel 9204
). a. Basidia and
basidiospores. b. Fasciculate hyphae of the stipitipellis.
Bars 5 10
mm.
1472 MYCOLOGIA
Cystidia none. Hymenium in transverse section 74–
284(469)
mm thick. Pileipellis of largely repent to
subanticlinal hyphae interspersed with erect fascicles,
hyphae pale tan-yellow in KOH, slighter darker in
mass, cylindrical, cells (14.8)29.6–54.3(79) 3 4.9–
12.3
mm; fascicles anticlinal, 135–220 3 50–116 mm,
composed of 10–15 parallel to slightly intertwining
hyphae, these of same dimensions as repent pileipellis
elements, terminal cells undifferentiated. Pileus tramal
hyphae smooth, hyaline in KOH, branching occasion-
ally, interwoven, lacking obvious internal contents,
cells 29.6–100 3 4.9–19.5
mm, moderately inflating,
narrowing or constricting near septa when inflated;
secondary septation absent. Stipitipellis hyphae mainly
repent between abundant erect hyphal fascicles;
fascicles (128)198–260 3 (29)46–54(66)
mm, com-
posed of 12–20 parallel hyphae, frequently narrowing
over apex to 3–4 hyphae wide, apex overall subacumi-
nate or blunt with terminal cells of equal length, cells
12.3–39.5 3 3.7–6.2
mm, pale yellow-tan in KOH,
devoid of obvious internal contents. Stipe tramal
hyphae in mass pale brown in KOH, densely interwo-
ven, branching frequently, individual hyphae pale
yellowish in KOH, uninflated. Clamp connections
abundant on hyphae of all tissues.
Holotype: Henkel 9204
(BRG; ISOTYPE: HSU; NY)
Habit, habitat and distribution:
Scattered or in small
troops on humus deposits or directly on live bark on
trunks of
Dicymbe corymbosa
in Guyana. Known only from
the type locality in the Upper Potaro Basin, Guyana.
Etymology:
‘‘Strigosus’’ (L. adj. A) 5 covered with
bristle-like hairs, referring to the prominent vestiture
on the pileus and stipe.
Specimens examined:
GUYANA: Region 8, Potaro-Siparuni:
Pakaraima Mountains, Upper Potaro River Basin, ,15 km
east of Mt Ayanganna; ,1 km west of base camp on trail to
Dicymbe
plot 3, 20 May 2010,
Henkel 9204
(HOLOTYPE:
BRG; ISOTYPE: HSU; NY); 3 km southwest of base camp in
Dicymbe
plot 3, 2 Jun 2001,
Aime 1750
(BRG; LSUM).
SINGAPORE: Botanic Garden, 11 Nov 1934,
Cantharellus
hystrix
Corner!, leg. E.J.H. Corner, s.n., typus herb. Cantab.
(ISOTYPE: E, in formalin-alcohol).
Commentary:
Molecular data clearly indicate that
Craterellus strigosus
is best placed in
Craterellus
,
although the species exhibits several traditional
diagnostic features of
Cantharellus
, including the
presence of clamp connections, a solid stipe and
stipitate/pileate stature. The presence of filiform-
acuminate primordia in
C. stri gosus
, however, is
consistent with both traditional and modern concepts
of
Craterellus
(Corner 1966, Dahlman et al. 2000). In
Guyana,
C. strigosus
has been confirmed via root
molecular analysis as an ECM symbiont of
D.
corymbosa
,
Dicymbe altsonii
Sandw. and
Aldina insignis
(Benth.) Endl. (Smith et al. 2011).
Craterellus strigosus
is similar to
Cantharellus hystrix
Corner, known from the type collection from
Singapore (Corner 1966 p 66–67) and Singer’s
collection, identified as
C. hystrix
, from central Brazil
(Singer et al. 1983 p 14–15). All share the small
(,20 mm) pileus beset with dense, erect strigose
scales, somber colors, the smooth hymenophore that
is decurrent, and the equal, small, solid, concolorous
stipe.
Craterellus strigosus
differs from
C. hystrix
in its
grayish brown hymenophore lacking in violaceous
tones, longer stipe (13–33 mm vs. 12 mm), the
presence of densely aggregated strigose scales on the
stipe and the number of sterigmata per basidium
(2–3–4–5 per basidium vs. 4–6). Examination of the
isotype of
C. hystrix
at E confirmed the more
diminutive basidioma size, paucity of strigose scales
on the stipe and predominance of sterigmata
numbers $4. Wartchow (unpubl) recently reported
a new collection identified as
C. hystrix
, consisting of a
single basidioma, from the Mata Atlantica in Pernam-
buco, Brazil, which is in some agreement with the
Guyanese
C. strigosus
, although the sterigmata num-
ber again varies, 2–3–4–5 in the Guyana material vs.
(4–5)6 in the Pernambuco collection. While the
morphological differences between
C. strigosus
and
C. hystrix
may seem slight, we feel justified in erecting
the new species because: (i) no convincing material of
C. hystrix
has emerged from Asia since the single type
collection of Corner’s from Singapore in 1934; (ii)
sequence data is unobtainable from Corner’s pickled
type; (iii) there are morphological differences; and
(iv) the likelihood of conspecificity between the Asian
and Neotropical material is low. Determining whether
the Guyanese
C. strigosus
is conspecific with Brazilian
material identified as
C. hystrix
by Singer and
Wartchow will require new collections from the
previous localities and generation of appropriate
sequence data for assessment.
Among Guyanese cantharelloids
C. strigosus
super-
ficially resembles
C. atratus
, also reported here, in its
small basidioma, colorations and decurrent, sharply
demarcated hymenophore.
C. strigosus
can be distin-
guished macroscopically from
C. atratus
by its darker
brown and regular occurrence of dense, erect scales
covering the pileus, especially over the disk, and over
the surface of the stipe. In addition
C. strigosus
dries
in a non-hygrophanous manner to dark brown, unlike
the hygrophanous
C. atratus
.
Craterellus atratus
also
lacks the finely granulose, opaque contents of the
basidiospores and basidioles regularly apparent in
C.
strigosus
. In addition, molecular phylogenetic analy-
ses clearly separate the two species (F
IG. 1).
The sympatric
C. atratoides
is also a small, somber,
fuliginous
Craterellus
, but differs from
C. strigosus
in
lacking strigose scales on its glabrous pelli, having a
W
ILSON ET AL.: CANTHARELLACEAE OF GUYANA 1473
much longer stipe (25–70 vs. 13–33 mm), longer
basidiospores (10.8–12 vs. 8–10
mm), longer basidia
(79–111 vs. 52–70
mm) and a consistently terrestrial
fruiting habit.
Craterellus atratus
(Corner) Yomyart, Watling, Phosri,
Piapukiew & Sihanonth FIGS.7,8
;
Cantharellus atratus
Corner. A monograph of
cantharelloid fungi. Ann Bot Mem 2:62. nom. nov.
Pileus 9–32 mm broad, 5–7 mm tall, initially
campanulate and flattened across apex, broadly
campanulate with out-flaring margin to nearly plane
with age, centrally depressed throughout develop-
ment, initially dark brown (6F5–7F5) throughout with
slightly lighter narrow marginal zone, with age light
brown or paler (6E3–6E4, 5D4 or 4C2) over central
two-thirds, transitioning toward margin to a nearly off-
white marginal zone 1–2 mm wide; surface initially
with scattered erect, low strigose scales, these less
prominent with age becoming nearly glabrous,
otherwise appressed radially fibrillose, canescent,
and finely rugulose under hand lens, moist; margin
finely and irregularly crenulate to nearly crowded-
setose, occasionally splitting with age; trama conco-
lorous, 1–1.5 mm thick, thickening somewhat above
stipe, subsolid. Hymenophore continuous over lower
side of pileus and descending stipe 2–9 mm with well
demarcated but irregular lower edge, initially light
gray or ashy gray (6B1–7B1, 4B1), slightly lighter with
advanced age, initially nearly smooth to finely
rugulose under hand lens, with age thickening
substantially and rugose to radially canaliculate, finely
hispid under hand lens due to projecting basidia; 0.3–
0.5 mm thick in longitudinal section. Stipe 8–30 mm
long up to hymenophore, 0.75–2 mm broad centrally,
subequal, subsolid-flexible, 2.5–6 mm broad under
descending hymenophore near apex, concolorous
with pileus throughout development, generally gla-
brous macroscopically, under hand lens with minute,
scattered, erect-acuminate strigose scales, less pro-
nounced with age, more concentrated and persistent
toward base; trama solid, concolorous, lacking a
hollow core. Primordia filiform-acuminate. Odor
none; flavor mild initially, slightly acrid with time.
Drying hygrophanous to light gray, hymenophore
becoming dull tan. Basidiospores 9–10(11) 3 7–
8.5(9)
mm, Q range 5 1.1–1.4, Q mean 5 1.2,
subellipsoid, smooth, hyaline in KOH, inamyloid,
with one large guttule, rarely multiguttulate; wall 0.5–
1.0
mm thick; hilar appendix 0.8–1.0 mm long. Basidia
54–67(73) 3 7.4–9.9(11.9)
mm, 9.9–12.4(13.6) mm
wide at apex, 4.9–7.7(9.4)
mm at base, subcylindrical,
wall thin, hyaline in KOH, devoid of obvious contents
or uniformly granulose and opaque, rarely with
numerous small guttules; sterigmata (2)3–4–5,
(3.7)4.9–7.4(10.1)
mm long, 1.2–2.5 mm wide at base,
somewhat curving. Basidioles numerous, cylindrical,
with numerous opaque guttules of various sizes.
Cystidia none. Hymenium in transverse section 113–
358
mm thick. Pileipellis of largely periclinal elements,
in mass light grayish brown in KOH, arranged
sporadically into subanticlinal to anticlinal hyphal
fascicles; fascicles 259–424 3 96–163
mm, of 25–40
loosely to more closely packed hyphae, these subpar-
allel to slightly interwoven, light grayish tan in KOH,
subacuminate or rounded over collective apex;
individual hyphae of a fascicle uninflated, cells 22–
56 3 4.9–8.6
mm, terminal cells undifferentiated and
rounded at tips, hyaline to pale grayish yellow in
KOH, thin-walled. Pileus tramal hyphae smooth,
hyaline in KOH, branching occasionally, lacking in
FIG. 7. Basidiomata of
Craterellus atratus
(
Henkel 9203
).
Bar 5 10 mm.
FIG. 8. Basidia and basidiospores of
Craterellus atratus
(
Henkel 9203
). Bar 5 10 mm.
1474 MYCOLOGIA
obvious internal contents, cells 37.1–113.6(190) 3
4.7–14.4
mm, inflating somewhat, occasionally narrow-
ing to rarely constricted near septa; secondary
septation absent. Stipitipellis essentially a cutis inter-
spersed with frequent erect hyphal fascicles; fascicles
102–320 3 40–80
mm, of 6–15 loosely to more closely
packed hyphae, subacuminate or rounded over
collective apex; individual fascicle hyphae uninflated,
cells 17–30 3 7–10
mm, terminal cells undifferentiat-
ed, hyaline to pale yellow in KOH, thin-walled. Stipe
tramal hyphae interwoven with longitudinal orienta-
tion, branching occasionally, hyaline in KOH, thin-
walled, devoid of obvious contents, cells 27.2–
59.3(69.2)
mm 3 (5)7.4–9.9 mm, barely inflating;
secondary septation absent. Clamp connections abun-
dant on hyphae of all tissues.
Habit, habitat and distribution:
Scattered or in small
troops on humus deposits or directly on live bark on
trunks of
D. corymbosa
in Guyana. Also known from
eastern and central Brazil and possibly southeastern
Asia.
Specimens examined:
GUYANA: Region 8, Potaro-Siparuni:
Pakaraima Mountains, Upper Potaro River Basin, ,15 km
east of Mt Ayanganna; 0.75 km west of Potaro base camp on
line to
Dicymbe
plot 3, 20 May 2010,
Henkel 9203
(BRG;
HSU); 100 m west of old Ayanganna airstrip 20 May 2000,
Aime 990
(BRG; LSUM); ,3 km southeast of base camp in
Dicymbe
plot 1, 28 May 2001,
Aime 1070
(BRG; LSUM).
BRAZIL: Rio de Janeiro, Corcovado, 20 Nov 1948,
Cantharellus atratus
Corner!, leg. E.J.H. Corner, typus in
herb. Cantab. (ISOTYPE: E, in formalin-alcohol).
Commentary: Craterellus atratus
is easily recognized
in Guyana’s
Dicymbe
forests by its small gray, centrally
stipitate-pileate basidiomata lacking pronounced stri-
gose scales and occurring in small to large troops in
elevated positions on humic deposits on the trunks of
D. corymbosa
. Molecular data clearly indicate that the
Guyanese taxon is best placed in
Craterellus
, although
it exhibits several traditional diagnostic features of
Cantharellus
, including the presence of clamp con-
nections, a solid stipe and stipitate/pileate stature.
The presence of filiform-acuminate primordia in
C.
atratus
, however, is consistent with both traditional
and modern concepts of
Craterellus
(Corner 1966,
Dahlman et al. 2000). We are applying the name
Craterellus atratus
to the Guyana taxon due to its
regional co-occurrence and high morphological
congruence with previously described Brazilian col-
lections of
Cantharellus atratus
.
The Guyana collections of
Craterellus atratus
agree
well with the Brazilian type description for
Cantha-
rellus atratus
of Corner (1966 p 62), confirmed by our
examination of the isotype at E. The salient macro-
morphological features are consistent, including the
small, campanulate pileus becoming nearly plane
with out-flaring margin, pileus surface with varying
densities of short, erect scales, the smooth, thickening
hymenophore that is decurrent and abruptly demar-
cated from the stipe, the slender, short stipe, a
general concurrence of all colors, and gregarious
fruiting habit. Corner’s original description indicated
a lack of stipe strigose scales, which are variably
present in the Guyana material, depending on
basidioma age and in greater concentration toward
the stipe base. Another description of the species by
Singer et al. (1983 p 13–15), based on the type and a
second Brazilian collection, notes that stipe strigose
scales are present on some basidiomata, and all other
morphological features are in concordance with the
Guyana material. While it is impossible to determine
the ECM host plants associated with the type
collection from southeastern Brazil, Singer’s second
collection came from campinarana forests on sand
soils with leguminous ECM host trees similar to those
occurring in Guyana (Singer et al. 1983).
Craterellus atratus
from Guyana microscopically
agrees with Brazilian material placed in
C. atratus
by Corner and Singer for most features. The Guyana
material deviates from Corner’s Brazilian type de-
scription in having consistently shorter basidia (54
67[73] vs. 70–100
mm), which was confirmed by
microscopic examination of the isotype. Corner
noted that the Brunei collection also cited in the
original description has basidia 47–65
mm long, in
concordance with our material and also with the short
basidia (41–48
mm) recorded by Singer for his
Brazilian material. Comparison of
C. atratus
with
the superficially similar, sympatric
C. strigosus
can be
found above.
Craterellus atratus
is one of the most frequently
fruiting ECM fungi in Guyana’s monodominant
D.
corymbosa
forests, with basidiomata occurring in
66.2% of 630 sampling quadrats over 7 y of rainy
season surveys (Henkel et al. 2012). The discovery of
Craterellus atratus
in Guyana provides a putative
range extension of nearly 1000 km to the north from
the central Brazilian Amazon (Singer et al. 1983). In
Guyana,
Craterellus atratus
has been confirmed via
root molecular analysis as an ECM symbiont of
D.
corymbosa
,
D. altsonii
and
A. insignis
(Smith et al.
2011).
Craterellus pleurotoides (T.W. Henkel, Aime & S.L.
Mill.) A.W. Wilson, comb. nov.
;
Cantharellus pleurotoides
T.W. Henkel, Aime & S.L.
Mill. 2006. Mycol Res 110, p 1410.
Commentary:
The combination is warranted due to
the molecular phylogenetic placement of
C. pleur-
otoides
within the
Craterellus
lineage of the Cantha-
rellaceae (F
IG. 1).
Cantharellus pleurotoides
, with a
highly reduced, pleurotoid basidioma atypical of the
W
ILSON ET AL.: CANTHARELLACEAE OF GUYANA 1475
Cantharellaceae, in the absence of definitive molec-
ular data, originally was placed in
Cantharellus
based
on the presence of clamp connections and a down-
curved primordial margin (Henkel et al. 2006).
A
CKNOWLEDGMENTS
The authors thank the following for financial support:
National Science Foundation DEB-0918591, the National
Geographic Society’s Committee for Research and Explo-
ration to TWH, NSF DEB-0732968 to MCA, and the Chicago
Botanic Garden for molecular analysis. Dillon Husbands
functioned as Guyanese local counterpart and assisted with
field collecting, descriptions and specimen processing.
Additional field assistance in Guyana was provided by M.
Chin, C. Andrew, V. Joseph, P. Joseph, F. Edmond, and L.
Edmond. Jessie K. Uehling provided the line drawings. Roy
Watling provided helpful discussions of the taxa and access
to Corner’s specimens at E. Ron Petersen provided access to
specimens at TENN. Two anonymous reviewers provided
very useful comments on earlier versions of the manuscript.
Research permits were granted by the Guyana Environmen-
tal Protection Agency. This paper is No. 190 in the
Smithsonian Institution’s Biological Diversity of the Guiana
Shield Program publication series.
LITERATURE CITED
Buyck B, Eyssartier G, Kivaisi A. 2000. Addition to the
inventory of the genus
Cantharellus
(Basidiomycota,
Cantharellaceae) in Tanzania. Nova Hedwig 71:491–
502.
Corner EJH. 1966. A monograph of cantharelloid fungi.
Ann Bot Mem No. 2. Oxford, UK: Oxford Univ. Press.
255 p.
———. 1969. Notes on cantharelloid fungi. Nova Hedwig
18:783–818.
Dahlman M, Danell E, Spatafora JW. 2000. Molecular
systematics of
Craterellus
: cladistic analysis of nuclear
LSU rDNA sequence data. Mycol Res 104:388–394,
doi:10.1017/S0953756299001380
Ducousso M, Contesto C, Cossegal M, Prin Y, Rigault F,
Eyssartier G. 2004.
Cantharellus garnierii
sp. nov., une
nouvelle chanterelle des maquis miniers nicke´life`res de
Nouvelle-Cale´donie. Cryptogamie Mycol 25:115–125.
Edgar R. 2004. MUSCLE: multiple sequence alignment with
high accuracy and high throughput. Nucleic Acids Res
32:1792–1797, doi:10.1093/nar/gkh340
Eyssartier G, Buyck B. 1999. Contributions a un inventaire
Mycologique du Madagascar 2. Nouveaux taxa dans le
genre
Cantharellus
. Mycotaxon 70:203–211.
———, ———, Halling RE. 2003. Une nouvelle chanterelle
du Costa Rica:
Cantharellus atrolilacinus
sp. nov.
Cryptogamie Mycol 24:21–25.
Gardes M, Bruns TD. 1993. ITS primers with enhanced
specificity for basidiomycetes—application to the iden-
tification of mycorrhizae and rusts. Mol Ecol 2:113–118,
doi:10.1111/j.1365-294X.1993.tb00005.x
Heinemann P. 1958. Champignons recoltes au Congo Belge
par Madame Goossens-Fontana. III. Cantharellineae.
Bull Jardin Bot l’E
´
tat Bruxelles 28:335–438.
———. 1966. Cantharellineae du Katanga. Bull Jardin Bot
l’E
´
tat Bruxelles 36:352–365.
Henkel TW, Aime MC, Chin M, Miller SL, Vilgalys R, Smith
ME. 2012. Ectomycorrhizal fungal sporocarp diversity
and discovery of new taxa in
Dicymbe
monodominant
forests of the Guiana Shield. Biodivers Conserv,
doi:10.1007/s10531-011-0166-1
———, ———, Mehl HK, Miller SL. 2006.
Cantharellus
pleurotoides
, a new and unusual basidiomycete from
Guyana. Mycol Res 110:1409–1412, doi:10.1016/j.
mycres.2006.09.010
———, ———, ———. 2009.
Craterellus excelsus
sp. nov.
from Guyana. Mycotaxon 107:201–208, doi:10.5248/
107.201
Holmgren PK, Holmgren NH, Barnett LC. 1990. Index
herbariorum I. The herbaria of the world. New York:
New York Botanical Garden. 693 p.
Kornerup A, Wanscher JH. 1978. Methuen handbook of
colour. 3rd ed. London: Eyre Methuen. 252 p.
Ko˜ljalg U, Larsson K-H, Abarenkov K, Nilsson RH, Alexander
IJ, Eberhardt U, Erland S, Hoiland K, Kjoller R, Larsson
E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Vralstad
T, Ursing BM. 2005. UNITE: a database providing web-
based methods for the molecular identification of
ectomycorrhizal fungi. New Phytol 166:1063–1068,
doi:10.1111/j.1469-8137.2005.01376.x
Maddison DR, Maddison WP. 2005. MacClade 4. Sunder-
land, Massachusetts: Sinauer Associates.
Miller MA, Holder MT, Vos R, Midford PE, Liebowitz T,
Chan L, Hoover P, Warnow T. 2009. The CIPRES
Portals. (http://www.phylo.org/sub_sections/portal)
Moncalvo JM, Nilsson RH, Koster B, Dunham SM, Bernauer
T, Matheny PB, Porter TM, Margaritescu S, Weiss M,
Garnica S, Danell E, Langer G, Langer E, Larsson E,
Larsson KH, Vilgalys R. 2006. The cantharelloid clade:
dealing with incongruent gene trees and phylogenetic
reconstruction methods. Mycologia 98:937–948, doi:10.
3852/mycologia.98.6.937
Montagne C. 1855. Cryptogamia guyanensis. Ann Sci Nat 1:
299.
Patouillard NT, Gaillard MA. 1888. Champignons du
Venezuela et principalement de la region du Haut-
Orenoque, recoltes en 1887 par M.A. Gaillard. Bull Soc
Mycol Fr 4:7–46.
Petersen RH, Mueller GM. 1992. New South American taxa
of
Cantharellus
,
C. nothofagorum
,
C. xanthoscyphus
and
C. lateritius
var.
colombianus
. Bol Soc Argent Bot 28:
195–200.
Ronquist F, Huelsenbeck J. 2003. MrBayes 3: Bayesian
phylogenetic inference under mixed models. Bioinfor-
matics 19:1572–1574, doi:10.1093/bioinformatics/
btg180
Singer R. 1963. Oak mycorrhiza fungi in Colombia.
Mycopathol Mycol Appl 20:239–250, doi:10.1007/
BF02089212
———, Araujo I, Ivory MH. 1983. The ectotrophically
mycorrhizal fungi of the Neotropical lowlands, espe-
cially central Amazonia. Beih Nova Hedwig 77:1–352.
1476 MYCOLOGIA
Smith ME, Henkel TW, Fremier AK, Vilgalys R. 2011.
Ectomycorrhizal fungal diversity and community struc-
ture on three co-occurring leguminous canopy tree
species in a Neotropical rainforest. New Phytol 192:
699–712, doi:10.1111/j.1469-8137.2011.03844.x
Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-
based phylogenetic analyses with thousands of taxa
and mixed models. Bioinformatics 22:2688–2690,
doi:10.1093/bioinformatics/btl446
Swofford DL. 2003. PAUP* 4.0: phylogenetic analysis using
parsimony (*and other methods). Sunderland, Massa-
chusetts: Sinauer Associates.
Vilgalys R, Hester M. 1990. Rapid genetic identification and
mapping of enzymatically amplified ribosomal DNA
from several
Cryptococcus
species. J Bacteriol 172:4238–
4246.
Wartchow F, Buyck B, Maia LC. 2012.
Cantharellus
aurantioconspicuus
(Cantharellales), a new species
from Pernambuco, Brazil. Nova Hedwig 94:129–137,
doi:10.1127/0029-5035/2012/0094-0129
White TJ, Bruns TD, Lee S, Taylor JW. 1990. Amplification
and direct sequencing of fungal ribosomal RNA genes
for phylogenies. In: Innis MA, Gelfand DH, Sninsky JJ,
White TJ, eds. PCR protocols: a guide to methods and
applications. San Diego: Academic Press. p 315–322.
Wu QX, Mueller GM. 1995. The genus
Craterellus
(Basid-
iomycetes, Aphyllophorales) in Costa Rica and Colom-
bia. Doc Mycol 25:487–496.
Yomyart S, Watling R, Phosri C, Piapukiew J, Sihanonth P.
2012. Two interesting cantharelloids from Nan and
Kanchanaburi Province, Thailand. Mycotaxon. (in
press).
WILSON ET AL.: CANTHARELLACEAE OF GUYANA 1477
  • ... Considerable taxonomic chaos exists in these genera and consequently several taxa have been transferred among these genera based on the weight given to a particular morphological feature. This taxonomic chaos in Cantharellaceae is now being resolved with the use of molecular data leading to an upsurge in the molecular phylogenetic studies in the family (Pine et al. 1999;Dahlman et al. 2000;Moncalvo et al. 2006;Matheny et al. 2010;Wilson et al. 2012;Buyck et al. 2013;Henkel et al. 2014;Buyck et al. 2017;Das et al. 2017;Hembrom et al. 2017;Olariaga et al. 2017). ...
    ... Clamp connections absent in all tissues. (Wilson et al. 2012), resembles C. albostrigosus in most of the macro and microscopic features. However, the neotropical species differs from C. albostrigosus by having smaller basidiomata with a dark brown non-hygrophanous pileus, grayish to brownish hymenophore, slightly smaller, broadly ellipsoid basidiospores (8-10 × 5.9-8(8.5) ...
    ... Craterellus pleurotoides (T.W. Henkel, Aime & S.L. Mill.) A.W. Wilson (2012Wilson ( : 1475 originally described as Cantharellus pleurotoides T.W. Henkel, Aime & S.L. Mill. (2006: 1410 from Guyana resembles C. inusitatus in having cyphelloid, pleurotoid, astipitate basidiomata, the smooth hymenophore covering the entire lower surface and in habitat. ...
    Article
    Full-text available
    Two new species, Crepidotus volubilis and Crepidotus palodensis are described from Kerala State, India based on morphological and molecular (nrLSU) phylogenetic data. The new taxa were assigned to section Echinospori due to the verrucose basidiospores and presence of clamp connections in the hyphae. Comprehensive descriptions, photographs and comparisons with phenetically similar and phylogenetically related species are discussed. The nrLSU-based phylogenetic analysis performed using Maximum Likelihood (ML) method, supported the novelty of the species.
  • ... Considerable taxonomic chaos exists in these genera and consequently several taxa have been transferred among these genera based on the weight given to a particular morphological feature. This taxonomic chaos in Cantharellaceae is now being resolved with the use of molecular data leading to an upsurge in the molecular phylogenetic studies in the family (Pine et al. 1999;Dahlman et al. 2000;Moncalvo et al. 2006;Matheny et al. 2010;Wilson et al. 2012;Buyck et al. 2013;Henkel et al. 2014;Buyck et al. 2017;Das et al. 2017;Hembrom et al. 2017;Olariaga et al. 2017). ...
    ... Clamp connections absent in all tissues. (Wilson et al. 2012), resembles C. albostrigosus in most of the macro and microscopic features. However, the neotropical species differs from C. albostrigosus by having smaller basidiomata with a dark brown non-hygrophanous pileus, grayish to brownish hymenophore, slightly smaller, broadly ellipsoid basidiospores (8-10 × 5.9-8(8.5) ...
    ... Craterellus pleurotoides (T.W. Henkel, Aime & S.L. Mill.) A.W. Wilson (2012Wilson ( : 1475 originally described as Cantharellus pleurotoides T.W. Henkel, Aime & S.L. Mill. (2006: 1410 from Guyana resembles C. inusitatus in having cyphelloid, pleurotoid, astipitate basidiomata, the smooth hymenophore covering the entire lower surface and in habitat. ...
    Article
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    Two unusual species of Craterellus have been collected numerous times from the evergreen tropical forests in Kerala State, India. The species Craterellus albostrigosus and Craterellus inusitatus are described as new based on morphological and phylogenetic analyses of nrLSU-rDNA gene region. Complete morphological descriptions, photographs and comparisons with similar species are provided as well as a key to the known species of Craterellus from India.
  • ... Considerable taxonomic chaos exists in these genera and consequently several taxa have been transferred among these genera based on the weight given to a particular morphological feature. This taxonomic chaos in Cantharellaceae is now being resolved with the use of molecular data leading to an upsurge in the molecular phylogenetic studies in the family (Pine et al. 1999;Dahlman et al. 2000;Moncalvo et al. 2006;Matheny et al. 2010;Wilson et al. 2012;Buyck et al. 2013;Henkel et al. 2014;Buyck et al. 2017;Das et al. 2017;Hembrom et al. 2017;Olariaga et al. 2017). ...
    ... Clamp connections absent in all tissues. (Wilson et al. 2012), resembles C. albostrigosus in most of the macro and microscopic features. However, the neotropical species differs from C. albostrigosus by having smaller basidiomata with a dark brown non-hygrophanous pileus, grayish to brownish hymenophore, slightly smaller, broadly ellipsoid basidiospores (8-10 × 5.9-8(8.5) ...
    ... Craterellus pleurotoides (T.W. Henkel, Aime & S.L. Mill.) A.W. Wilson (2012Wilson ( : 1475 originally described as Cantharellus pleurotoides T.W. Henkel, Aime & S.L. Mill. (2006: 1410 from Guyana resembles C. inusitatus in having cyphelloid, pleurotoid, astipitate basidiomata, the smooth hymenophore covering the entire lower surface and in habitat. ...
    Article
    Full-text available
    Two unusual species of Craterellus have been collected numerous times from the evergreen tropical forests in Kerala State, India. The species Craterellus albostrigosus and Craterellus inusitatus are described as new based on morphological and phylogenetic analyses of nrLSU-rDNA gene region. Complete morphological descriptions, photographs and comparisons with similar species are provided as well as a key to the known species of Craterellus from India.
  • ... The diversity of species in Cantharellus Adans.: Fr., in combination with their ectomycorrhizal nature (mycobionts of several plant lineages), as well as their highly prized value as edible wild mushrooms, have attracted the attention of specialists from different fields worldwide (Smith and Morse 1947, Trappe 1962, Chandra 1989, Molina et al. 1992, Homola 1993, Thoen 1993, Watling 1997, Danell 1999, Pilz et al. 2002, Lee et al. 2003,Yun and Hall 2004, Boa 2005, Agerer 2006, Arora and Dunham 2008, Kumari et al. 2011, Wilson et al. 2012. ...
    ... Cantharellus encompasses fungi with long-lived, gymnocarpic, fleshy, variedly coloured, trumpet-shaped basidiomes with nearly smooth, veined, gill-like folded to distinctly lamellate hymenophore, pileipellis poorly differentiated, cystidia lacking, smooth and thin-walled spores, with or without clamps (Wilson et al. 2012. In many cases, basidiomes of members of closely related species or inclusive, unrelated look-alike species are difficult to identify in a strict sense, especially if there is not an accurate record of the variation of morpho-anatomical characters and colours in fresh condition. ...
    ... Taxonomic research on Cantharellus has increased substantially in the last decade, especially by combining DNA and morphological information to support the definition of early recognised species and others recently discovered , Tibuhwa et al. 2012, Wilson et al. 2012, 2016a, 2016b, Foltz et al. 2013, Shao et al. 2014, Shao et al. 2016, Leacock et al. 2016. ...
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    During explorations of tropical oak forests in central Veracruz (eastern Mexico), the authors discovered a Cantharellus species that produces basidiomes with strikingly violet pileus and a hymenium with yellow, raised gill-like folds. It is harvested locally and valued as a prized edible wild mushroom. Systematic multiyear sampling of basidiomes allowed the recording of the morphological variation exhibited by fresh fruit bodies in different growth stages, which supports the recognition of this Cantharellus species from others in the genus. Two molecular phylogenetic analyses based on a set of sequences of species of all major clades in Cantharellus , one including sequences of the transcription elongation factor 1-alpha (tef-1α) and a combined tef-1α and nLSU region (the large subunit of the ribosome), confirm the isolated position of the new species in a clade close to C.lewisii from USA, in the subgenus Cantharellus. Detailed macroscopic and microscopic descriptions, accompanied by illustrations and a taxonomic discussion are presented.
  • ... 28S follows the thermal-cycler protocol: 96 C for 2 min; 35 cycles of 96 C for 30 s, 55 C for 30 s and 72 C for 90 s; 72 C for 10 min; ending with an infinite 14 C step (Wilson et al. 2012). PCR amplification of EF1a follows the thermalcycler protocol: 94 C for 2 min; nine cycles of 94 C for 30 s, 66 C for 30 s, 72 C for 60 s; 35 cycles of 94 C for 30 s, 56 C for 30 s and 72uC for 60 sec; 72 C for 10 min; ending with an infinite 14 C step. ...
    ... ). Cantharellus guyanensis Mont. was used as outgroup in the ITS and 28S datasets, which follows its placement basal to the rest of Cantharellus inWilson et al. (2012). Craterellus tubaeformis (Fr.) ...
    Article
    Full-text available
    Recent molecular systematic studies of Cantharellus cibarius sensu lato have revealed previously unknown species in different regions of North America. This study investigates yellow chanterelles in the Midwest using phylogenetic analysis of three DNA regions: nuc rDNA internal transcribed spacer 2 (ITS2) and 28S sequences and translation elongation factor 1α gene (EF1α). This analysis reveals a locally common taxon Cantharellus chicagoensis sp. nov. as distinct from sympatric species present in northeastern Illinois, northwestern Indiana and Wisconsin. This chanterelle features a pileus that often has a greenish yellow margin when immature, a squamulose disk when mature, a yellow spore print and the absence of a fragrant odor. Multiple Cantharellus specimens group with C. flavus and C. phasmatis, expanding their known range and others with C. roseocanus The our observations highlight the diversity of Cantharellus in midwestern USA and further document the need for additional systematic focus on the region's fungi.
  • ... Morphological characters allowed for identification at the genus level. Whenever possible, we identified the specimens to the species level based on morphology using keys and taxonomic descriptions (e.g., Corner, 1950;Bas, 1978;Pegler and Fiard, 1983;Singer et al., 1983;Simmons et al., 2002;Henkel et al., 2011Henkel et al., , 2012Uehling et al., 2012aUehling et al., , 2012bWilson et al., 2012). Due to the lack of literature documenting tropical fungal species and the high number of species that might be new to science, we also consulted taxonomic specialists (e.g., Leif Ryvarden, professor emeritus at University of Oslo, an expert on Coltricia and Coltriciella). ...
    Article
    Full-text available
    The genera Dicymbe and Aldina (Fabaceae) host ectomycorrhizal fungi (EcM) and are common in white sand forests (WSFs), a highly specialized habitat with a high level of plant endemism compared with terra-firme forests. In this study, we visited four times a 1-ha permanent plot established in a small patch of a WSF in the south of Colombia Amazonia. Forty-eight species of EcM fungi were recovered from sporocarps and 15 ITS species-level were detected from root tips. Seventeen species were new reports to Colombia and seven corresponded to undescribed species. These results confirm that this WSF supports a significant EcM fungal diversity. Most of the species found in this study have been previously reported to be associated with other legume and/or dipterocarp species from geographically distant forests. The long-distance occurrence combined with low host specificity, suggest the possibility of gene flow between geographically distant populations of EcM fungi in neotropical lowland rainforests.
  • ... As mentioned previously, species of Laccaria have not been found in association with the typical EcM hosts of these areas, e.g., caesalpinioid legumes, neotropical dipterocarps, Coccoloba (Polygonaceae), and members of the Nyctaginaceae. This is in contrast to other EcM fungal genera-such as Cantharellus and Craterellus (Wilson et al. 2012a;Henkel et al. 2014), Amanita (Sánchez-Ramírez et al. 2015), Inocybaceae (Matheny et al. 2009), and Russula (Looney et al. 2015)-that have various distributions and associations with hosts from sub-Saharan Africa and tropical South America. ...
    Chapter
    Full-text available
    The mushroom genus Laccaria is one of the very few ectomycorrhizal lineages whose diversity has been explored from the phylogenetic, population genetic, genomic, and ecological perspectives. The genus serves as a model for understanding the biology of ectomycorrhizal fungi. This chapter provides an in-depth overview of the systematic diversity, ecology, host associations, and phylogenetic relationships that helped shape the current distribution of Laccaria species. This chapter discusses the challenges in identifying and delimiting species of Laccaria, along with the potential influence of life-history strategy and ecological role on the speciation and dispersal of Laccaria. The biogeographic histories of several well-documented and important ectomycorrhizal hosts of Laccaria are reviewed. These histories provide a backdrop to examine potential migration and dispersal routes during the diversification of Laccaria. They reveal historical distribution patterns that explain how ectomycorrhizal symbioses likely shaped the biogeography of Laccaria. The phylogenetic history and global systematic diversity of Laccaria is reviewed in the final sections, which include discussions of the Southern Hemisphere origins of the genus, a hypothesis for dispersal to the Northern Hemisphere, and the challenges of correlating diversity and distribution patterns in the Northern Hemisphere. Altogether, Laccaria represents a genus that is rich with opportunities to explore the ecological and evolutionary forces shaping the biogeography of ectomycorrhizal fungi.
  • Article
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    ABSTRACT True fungi (Fungi) and fungus-like organisms (e.g. Mycetozoa, Oomycota) constitute the second largest group of organisms based on global richness estimates, with around 3 million predicted species. Compared to plants and animals, fungi have simple body plans with often morphologically and ecologically obscure structures. This poses challenges for accurate and precise identifications. Here we provide a conceptual framework for the identification of fungi, encouraging the approach of integrative (polyphasic) taxonomy for species delimitation, i.e. the combination of genealogy (phylogeny), phenotype (including autecology), and reproductive biology (when feasible). This allows objective evaluation of diagnostic characters, either phenotypic or molecular or both. Verification of identifications is crucial but often neglected. Because of clade-specific evolutionary histories, there is currently no single tool for the identification of fungi, although DNA barcoding using the internal transcribed spacer (ITS) remains a first diagnosis, particularly in metabarcoding studies. Secondary DNA barcodes are increasingly implemented for groups where ITS does not provide sufficient precision. Issues of pairwise sequence similarity-based identifications and OTU clustering are discussed, and multiple sequence alignment-based phylogenetic approaches with subsequent verification are recommended as more accurate alternatives. In metabarcoding approaches, the trade-off between speed and accuracy and precision of molecular identifications must be carefully considered. Intragenomic variation of the ITS and other barcoding markers should be properly documented, as phylotype diversity is not necessarily a proxy of species richness. Important strategies to improve molecular identification of fungi are: (1) broadly document intraspecific and intragenomic variation of barcoding markers; (2) substantially expand sequence repositories, focusing on undersampled clades and missing taxa; (3) improve curation of sequence labels in primary repositories and substantially increase the number of sequences based on verified material; (4) link sequence data to digital information of voucher specimens including imagery. In parallel, technological improvements to genome sequencing offer promising alternatives to DNA barcoding in the future. Despite the prevalence of DNA-based fungal taxonomy, phenotype-based approaches remain an important strategy to catalog the global diversity of fungi and establish initial species hypotheses.
  • Article
    Suillus spraguei, synonym S. pictus, has been reported from eastern North America and eastern Asia associated with Pinus subgenus Strobus. Published phylogenetic analyses of rRNA internal transcribed spacer (ITS) sequence and population genetic studies indicated that S. spraguei as currently circumscribed might contain several geographically distinct species. This study examined this possibility through a multigene analysis of S. spraguei specimens from eastern North America and eastern Asia. These specimens were associated with Pinus strobus, P. koraiensis, P. armandii, and P. kwangtungensis. The multigene analysis included three genomic regions: the genes for translation elongation factor 1α (TEF1) and RNA polymerase II largest subunit (RPB1), and the nuc rRNA segments ITS1-5.8S-ITS2 (ITS) and 28S D1-D2 domains (28S). This study confirms that the S. spraguei complex consists of at least three cryptic species: S. spraguei sensu stricto associated with P. strobus in eastern North America; S. phylopictus associated with multiple species in Pinus subgenus Strobus (5-needle pines) throughout China and Japan; and S. kwangtungensis, currently found only in P. kwangtungensis forests in southeastern China. A third new species from Japan and Korea was suggested based on ITS phylogeny. Morphologically, S. spraguei and S. phylopictus resemble each other, whereas S. kwangtungensis is covered with more floccose scales. The new species add to the knowledge of macrofungal diversity in eastern Asia and highlight the necessity of comparing broadly distributed species complexes using morphological, molecular, and ecological data.
  • Article
    Lichenicolous species are widely distributed in the Basidiomycota, and many are known to produce sclerotia or bulbils with few additional structures to permit taxonomic placement. The Cantharellales include many of these species and we here describe a new species that grows over Cladonia rangiferina and forms yellow-orange, initially immersed bulbils similar to Burgella flavoparmeliae Diederich & Lawrey, a familiar species in the order. We obtained sequences of nuLSU representing an isolated culture and herbarium specimen of the species, and initial searches in GenBank indicated it was a member of the Cantharellales. We inferred its phylogenetic placement in the order using an existing dataset that included all known lichenicolous species. Our results indicate that it is not closely related to any described lichenicolous species or to any other described bulbilliferous species in the order. Based on these results, we are now establishing a new genus and species, Neoburgoa freyi, in the Hydnaceae sensu Hibbett et al. (2014). We also introduce the new name Adamflakia for the genus Bulbilla as the latter coincides with the technical term 'bulbilla' used in previous descriptions of bulbil-forming species and is therefore not validly published following the ICN (Art. 20.2); Adamflakia applanata comb. nov. is proposed. © 2016 by The American Bryological and Lichenological Society, Inc.