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Elaphomyces compleximurus sp. nov. and E. digitatus sp. nov. are described from the Pakaraima Mountains of Guyana. Macromorphological, micromorphological, habitat and DNA sequence data are provided for each new species. This is the first report of Elaphomyces ascomata associated with ectomycorrhizal members of the Fabaceae and also for the genus from the lowland South American tropics.
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New
Elaphomyces
species (Elaphomycetaceae,
Eurotiales, Ascomycota) from Guyana
Michael A. Castellano
USDA, Forest Service, Northern Research Station,
3200 Jefferson Way, Corvallis, Oregon 97331
Terry W. Henkel
1
Department of Biological Sciences, Humboldt State
University, Arcata, California 95521
Steven L. Miller
Department of Botany, University of Wyoming,
Laramie, Wyoming 82071
Matthew E. Smith
Department of Plant Pathology, University of Florida,
Gainesville, Florida 32611
M. Catherine Aime
Department of Plant Pathology and Crop Physiology,
Louisiana State University Agricultural Center,
Baton Rouge, Louisiana 70803
Abstract
:
Elaphomyces compleximurus
sp. nov. and
E.
digitatus
sp. nov. are described from the Pakaraima
Mountains of Guyana. Macromorphological, micro-
morphological, habitat and DNA sequence data are
provided for each new species. This is the first report
of
Elaphomyces
ascomata associated with ectomycor-
rhizal members of the Fabaceae and also for the
genus from the lowland South American tropics.
Key words: Dicymbe
, Guiana Shield, hypogeous
fungi, sequestrate fungi
INTRODUCTION
The hypogeous false truffle genus
Elaphomyces
Fries
(Elaphomycetaceae, Eurotiales, Ascomycota) is com-
posed of ectomycorrhizal (ECM) fungi with a gleba of
powdery, dark ascospores, a thick peridium and large
cleistothecial ascomata relative to other members of
the Eurotiales. Most of the ,67 species of
Elaphomyces
currently described are from north temperate forests
in association with ECM host plants in the Pinaceae,
Fagaceae and Betulaceae (Castellano et al. 1989).
Cooke (1892) and Rodway (1918) provided the first
reports of
Elaphomyces
for the southern hemisphere,
but they assigned European names to their species
(Castellano et al. 2011). The known
Elaphomyces
diversity in the southern temperate zones was in-
creased substantially by Castellano et al. (2011) who
published 13 new species associated with Myrtaceae
and
Nothofagus
host plants in Australia. Three new
Elaphomyces
species associated with
Nothofagus
recently
were described from New Zealand (Castellano et al.
2012).
While
Elaphomyces
is well represented in the
subtropical
Quercus
forests of Florida and records
exist from montane
Quercus
forests of Costa Rica
(Castellano unpubl), records are exceedingly scarce
from the low-latitude, lowland forests of the tropics.
Corner and Hawker (1955) described the first
Elaphomyces
species from the lowland tropics in
association with Dipterocarpaceae in Singapore, but
to date no species have been described from the
lowland South American tropics.
Over the past 13 y macrofungal collecting expedi-
tions in western-central Guyana have revealed a
wealth of ECM fungi in forests dominated by the
ECM Fabaceae canopy tree species
Dicymbe corymbosa
Spruce ex Benth.,
Dicymbe altsonii
Sandw. (subfam.
Caesalpinioideae; Henkel et al. 2011) and
Aldina
insignis
(Benth.) Endl. (subfam. Papilionoideae;
Smith et al. 2011). Recent molecular studies of ECM
fungal communities in these forests have detected
belowground fungal diversity similar to those revealed
by long-term sporocarp surveys in the region, but the
great majority of taxa are basidiomycetes (Smith et al.
2011). So far, one member of the Elaphomycetaceae,
Pseudotulostoma volvata
O.K. Mill. & T.W. Henkel, has
been described from Guyana (Miller et al. 2001).
Here we describe two new
Elaphomyces
species
discovered in Guyana’s
Dicymbe
forests. Morphologi-
cal, habitat and DNA sequence data are provided for
each species. These are the first described species of
Elaphomyces
associated with ECM Fabaceae hosts and
the first records for the genus from the lowland South
American tropics.
MATERIALS AND METHODS
Ascomata were collected during the May–July rainy seasons
of 2000–2002, 2004, 2007 and 2009–2010 from the Upper
Potaro River Basin within a 15 km radius of a permanent
base camp at 5u18904.80N, 59u54940.40W, 710 m (Henkel
2003). More were collected during May–June 2011 from the
Upper Demerara River Basin at Mabura Ecological Reserve
within 2 km of a field station at 5u09919.00N; 58u41958.90W,
100 m. At Potaro ascomata were collected from mono-
dominant forests of
D. corymbosa
and other stands
containing
D. corymbosa
,
D. altsonii
and
A. insignis
;at
Submitted 23 Feb 2012; accepted for publication 30 Mar 2012.
1
Corresponding author. E-mail: twh5@humboldt.edu
Mycologia,
104(5), 2012, pp. 1244–1249. DOI: 10.3852/12-061
#2012 by The Mycological Society of America, Lawrence, KS 66044-8897
1244
Mabura collections were made in
D. altsonii
monodominant
stands. Fresh characteristics of ascomata were recorded in
the field. Color was compared with plates from Kornerup
and Wanscher (1978) and is cited in parenthesis (e.g. 5A4).
Specimens were field-dried with silica gel. Dried specimens
were rehydrated and examined in 3%KOH, Melzer’s
reagent and cotton blue. Microscopic descriptions are
based on 3%KOH mounts unless specified. Twenty
ascospores were measured from the holotype collection;
dimensions reported include ornamentation. Dried asco-
spores were mounted on aluminum pegs with double-sided
tape and coated with gold for scanning electron microscopy
(SEM) with an AmRay 3300 FE field emission scanning
electron microscope. Specimens are deposited in these
herbaria: (Holmgren et al. 1990): BRG, University of
Guyana; HSU, Humboldt State University; OSC, Oregon
State University; LSUM, Louisiana State University Mycolo-
gy. Ribosomal DNA sequencing for the ITS and LSU
regions followed the protocols of Aime et al. (2005) and
Smith et al. (2011); GenBank accession numbers are
provided in
Specimens examined
.
TAXONOMY
Elaphomyces compleximurus Castellano, T.W. Hen-
kel et S.L. Mill., sp. nov. FIG.1
MycoBank MB564542
Ascomata 9–15 mm tall 310–20 mm broad, nearly
globose to flattened subovate with a distinct, abruptly
tapered base, with roots, sand and dense mycelium
adherent to the base and upward over lower half of the
ascoma, black when fresh, drying to dark gray (near 10F2–
10F3); peridial surface completely covered with dense black
mycelium visible with a hand lens, beneath this mycelium
verrucose throughout except nearly smooth near base; warts
contiguous, separated by narrow lines, angular-sided, up to
1 mm tall and 0.3 mm broad, with rounded apices.
Peridium when dried collapsing to form an exterior,
subreticulate pattern of ridges and folds, these irregular in
length, superimposed over surface warts; in section four-
layered; outer first layer 0.03–0.06 mm thick, dark brown, of
closely appressed mycelium, underlain by a second carbo-
naceous layer 0.1–0.15 mm thick, of nearly black, closely
appressed cells, underlain by a third layer 0.5–0.6 mm thick,
mostly white but a thin, pale tan outer zone, cottony, with
embedded, black-mantled ectomycorrhizas scattered
throughout but most numerous near the ascoma base; the
innermost fourth layer 1.3–2 mm thick, pale gray to pale
brownish gray (6F2–6F3), gradually more pale toward the
gleba, similar in texture to the third layer but lacking
embedded ectomycorrhizas. Gleba grayish black (9F2–9F3)
to black, powdery, with fine, pale dissepiments. Odor mildly
of raw potato with fruity element; taste none. Outer first
layer of peridium composed of thick-walled, brown to dark
brown, septate, segmented and irregular (not straight-
walled) hyphae 1–2 mm broad, these somewhat tuberculate,
loosely interwoven and much branched at nearly 90 degree
angles; carbonaceous second layer dense, of compact, dark
brown to nearly black cells with walls ,2mm thick, quickly
grading downward into the third layer of brown, somewhat
puzzle-like textura epidermoidea, grading into the fourth
layer where the pale brown tissue changes quickly to textura
intricata or textura porrecta forming clusters in cross-
hatched formations, this pattern continuing inward with the
hyphae grading from brown to hyaline to brown near the
gleba; hyphae of fourth layer 5–7 mm wide with walls 1–2 mm
thick. Gleba of ascospores and sinuous, hyaline, septate,
acutely branched, loosely interwoven hyphae, these 2–3 mm
wide, with walls ,0.5 mm thick. Asci not observed.
Ascospores globose, brown, 22–25 mm diam (mean 5
23.2 mm) including the reticulate-alveolate ornamentation;
aveolae well defined, 3.5–5.5 mm broad 32–3 mm tall, nearly
round or with subangular sides with irregular to wavy walls;
under SEM the individual alveolar wall consisting of two
layers separated by vertical ribs; these nearly equally spaced
along the wall, with rib ends at the margin of the wall; the
ascospore surface exposed inside the alveolae an irregular,
slightly roughened, central disk with radiating repent rods
and small depressions extending to the base of the
surrounding alveolar wall.
Holotype. Henkel 8880
(BRG; ISOTYPES HSU;
OSC)
Habit, habitat and distribution.
Scattered to gregar-
ious on the forest floor under
D. corymbosa
or
D.
altsonii
on white sand or brown sand soils; May–July
rainy season and also in late August during dry season
transition; known from the type locality in the Upper
Potaro River Basin of Guyana and ,100 km east in the
Mabura Hill region.
Etymology.
Complexus (Latin adj. B) 5complex +
murus (Latin s.m. II) 5wall, referring to the distinctive,
complex structure of the ascospore ornamentation.
Specimens examined
. GUYANA. REGION 8 POTARO-
SIPARUNI: Pakaraima Mountains, Upper Potaro River
Basin, within a 4 km radius of base camp at 5u18904.80N,
59u54940.40W, 710–750 m; vicinity of base camp, 4 Jun 2000,
S.L. Miller 10096
(BRG; HSU; OSC) and 23 Jun 2000,
S.L.
Miller 10157
(BRG; HSU; OSC); ,0.75 km northeast of
base camp on white sand soils in mixed
D. corymbosa-
Micrandra glabra
forest, 25 Aug 2007,
Henkel 8880
(HOLOTYPE BRG; ISOTYPES HSU, OSC; ITS GenBank
JN711441); 1.5 km west of base camp in mixed
D. corymbosa
-
M. glabra
forest on alluvial sand soils, 3 Jun 2010,
Henkel
9254
(BRG, HSU); REGION 10 UPPER DEMERARA-
BERBICE: Mabura Ecological Reserve, field station located
at 5u09919.00N, 58u41958.90W, ,100 m; vicinity of field
station, under
D. altsonii
on brown sand soils, 28 May 2011,
Aime 4331
(BRG; LSUM).
Commentary.
The distinctly reticulate-alveolate asco-
spores of
E. compleximurus
easily distinguish it from
nearly all other described
Elaphomyces
species. The
only known
Elaphomyces
species to combine the
features of a tapered base of the ascoma, black,
verrucose peridium and some degree of reticulate
ascospore ornamentation are the European
E. cyano-
sporus
Tul. & C. Tul. and
E. persoonii
Vittad. Both are
easily separated from
E. compleximurus
by their larger
CASTELLANO ET AL.: NEW SPECIES OF
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LAPHOMYCES
1245
FIG.1.
Elaphomyces compleximurus
(HOLOTYPE;
Henkel 8880
). a. Ascomata in clusters and in longitudinal section. b.
Longitudinal section of ascoma showing the powdery gleba (gl) and the embedded ectomycorrhizas (ec) within the peridium. c.
Peridial layer 2 with carbonaceous cells (ep). d. Mature ascospores under bright field microscopy showing ornamentation in outline
and surface view of aveolae. e. Ascospores under scanning electron microscopy (SEM) showing the irregularly sided aveolae. f. Aveolae
under SEM showing complex ornamentation of ribs between alveolar wall layers. Bars: a 515 mm; b 52mm;c,d,e510 mm; f 51mm.
1246 MYCOLOGIA
ascospores; in
E. cyanosporus
the ascospore diameter
ranges from 27–30 mm (mean 528 mm), for
E.
persoonii
29–33 mm(mean531.1 mm), vs. 22–25 mm
(mean 523.2 mm) for
E. compleximurus
.Both
E.
compleximurus
and
E. persoonii
have ectomycorrhizas
embedded within the outer layers of the peridium, a
condition otherwise highly unusual in sequestrate
fungi.
This is the first report of
Elaphomyces
ascomata
associated with fabaceous hosts. However, an ITS
rDNA sequence of another
Elaphomyces
species
(ECM1108, GenBank JN168718) as yet undiscovered
as ascomata recently was reported from ectomycor-
rhizas of
D. corymbosa
(Smith et al. 2011) and also
found on
D. jenmanii
(Smith and Henkel unpubl),
indicating that taxa beyond those described here
exist in the region. In Guyana
Elaphomyces complex-
imurus
has been encountered less frequently than
E.
digitatus
(described below), but the former is harder
to find in the field because of its dark color.
Pseudotulostoma volvata
, another sympatric taxon
from the Elaphomycetaceae, is common in
Dicymbe
-
dominated forests both as ascomata and on ECM
roots and also has the unusual peridium-embedded
ectomycorrhizas (Miller et al. 2001; Henkel et al.
2006, 2011).
Elaphomyces digitatus Castellano, T.W. Henkel et
S.L. Mill., sp. nov. FIG.2
MycoBank MB564543
Ascomata 4–11 mm tall 34–31 mm broad, nearly globose
to flattened or ellipsoidal, occasionally furrowed, when
immature cream (5A2–5A3) to light orange (5A5), light
yellow (4A5) or grayish orange (5B3), at maturity brownish
orange (5B3–5B8–5C8) to occasionally darker brown (6E8–
6F8), with fine surface tomentum throughout that is
occasionally absent at maturity; ectomycorrhizas with
adherent soil irregularly covering the lower one-quarter to
one-half of the ascoma, forming a loose exterior agglomer-
ation, not embedded within the peridial structure, occa-
sionally attached to more extensive fine roots extending
into soil; peridial surface beneath the tomentum finely
roughened macroscopically, under hand lens verrucose,
consisting of fine, contiguous concolorous warts except
where damaged; warts ,0.13 mm tall and 0.25 mm broad,
pyramidal with obtuse apices, with 4–6 sides of irregular
dimensions. Peridium when fresh leathery and tough, 0.9–
1.8 mm thick overall; in dried section 0.5–0.75 mm thick
overall, three-layered; outer layer of brownish orange
pyramidal, blunt warts up to 0.13 mm tall, underlain by a
dull creamy white to off-white layer 0.1–0.15 mm thick, this
grading into an innermost, gray to reddish gray layer 0.25–
0.3 mm thick. Gleba dark brown (7F8) to dark rusty brown
(8F8) when mature, powdery, with numerous, fine, white
dissepiments throughout. Odor musky or skunky or of latex
when sectioned; taste none. Outer layer of peridium of
small pyramidal warts up to 125 mm tall, red-brown at apex
and yellow-brown near base; cells short, pigmented, with
walls 1–2 mm thick; the pyramids intraspace 50–60 mm deep
of hyaline, more or less parallel, inflated cells that are 5–
10 mm broad; outer layer grading inward into a disorganized
textura epidermoidea of interwoven, hyaline hyphae 10–
12 mm wide with walls 2–4 mm thick, grading quickly inward
into a darker layer tinted yellow-brown from scattered dark
concolorous granules; hyphae immediately adjacent to the
gleba occasionally inflated up to 35 mm broad. Mature gleba
of ascospores and sinuous, interwoven, hyaline, septate
hyphae, these 2–3 mm broad with walls ,0.5 mm thick,
intermixed with inflated hyphae up to 6 mm broad and
encrusted with brown, amorphous deposits. Asci present in
immature gleba, globose, 42–65 mm diam, walls 1–2 mm
thick, containing 2–8 ascospores (mostly 8), with a
constricted base up to 12 37mm attached to a knot of
granulated, pale brown, thick-walled hyphae 67mm wide
with walls 2–3 mm thick. Ascospores globose, dark red-
brown, (16)20–23(24) mm diam (mean 521.9 mm) includ-
ing the irregular, labyrinthine-ridged ornamentation that
forms a partial reticulum of dark, crowded ridges 3–4 mm
tall; under SEM reticulum walls wavy, fully fused near
margins but separating downward into columnar basal
elements near ascospore surface; margins with numerous
short, irregular, digitate projections.
Holotype. Henkel 8887
(BRG; ISOTYPES HSU;
OSC)
Habit, habitat and distribution.
Usually in clusters of
2–5 ascomata in hilly country on red lateritic soils at
,710 m in
D. corymbosa
monodominant forest, also in
similar terrain in mixed
D. altsonii
,
D. corymbosa
and
A. insignis
forest, infrequently in sandy, alluvial soil
partially embedded in humic material on forest floor
under
D. corymbosa
, rarely elevated 1–2 m up the bole
of a
D. altsonii
in mixed
Dicymbe
forest, or in
D.
altsonii
-dominated stands at low elevation on brown
sand soils; May–July and December–January rainy
seasons; known from the type locality in the Upper
Potaro River Basin of Guyana and ,100 km east in the
Mabura Hill region.
Etymology.
Digitatus (Latin adj. A) 5digitate,
referring to the small, finger-like projections emanat-
ing from the outer ascospore ornamentation.
Specimens examined
. GUYANA. REGION 8 POTARO-
SIPARUNI: Pakaraima Mountains, Upper Potaro River
Basin, within a 15 km radius of Potaro base camp at
5u18904.80N, 59u54940.40W, 710–750 m; old Ayanganna
airstrip, 21 May 2000,
S.L. Miller 10041
(BRG; HSU;
OSC) and 21 May 2000,
Aime 995
(BRG; LSUM); ,200 m
southwest of base camp at
D. altsonii
site, 22 May 2000,
Henkel 7448
(BRG; HSU; OSC) and
S.L. Miller 10053
(BRG; HSU; OSC);
Dicymbe
plot 1, 28 May 2000,
Aime 1047
(BRG; OSC; LSUM) and 14 May 2010,
Aime 3914
(BRG;
LSUM); vicinity of base camp, 30 May 2000,
Aime 1079
(BRG; OSC; LSUM) and 5 Jul 2004,
Henkel 8744
(BRG;
HSU; OSC) and 26 Aug 2007,
Henkel 8887
(HOLOTYPE
BRG; ISOTYPE HSU, OSC; ITS GenBank JQ657705);
Benny’s ridge under
D. corymbosa
on lateritic ironstone
CASTELLANO ET AL.: NEW SPECIES OF
E
LAPHOMYCES
1247
FIG.2.
Elaphomyces digitatus
(HOLOTYPE;
Henkel 8887
). a. Fresh ascomata including transverse section. b. Outermost
peridium layer showing stacked hyaline cells in of space between warts. c. Interior peridium layer with scattered dark granules (gr)
interspersed with hyaline hyphae. d. Mature ascospores under bright field microscopy with ornamentation in outline. e. Ascospores
under scanning electron microscopy (SEM) with the labyrinthine-ridged ornamentation. f. Individual ascospore under SEM with
the digitate protrusions on the wall margins of ornamentation. Bars: a 510 mm; b 550 mm; c 520 mm; d, e 510 mm; f 55mm.
1248 MYCOLOGIA
soils, 1 Jun 2000,
S.L. Miller 10088
(BRG; HSU; OSC) and 4
Jun 2000,
S.L. Miller 10105
(BRG; HSU; OSC) and 10 Jun
2000,
S.L. Miller 10124
(BRG; HSU; OSC);
Dicymbe
plot 3,
18 May 2001,
Aime 1512
(BRG; OSC; LSUM; LSU GenBank
JN713147) and 8 Jun 2002,
Aime 1923
(BRG; OSC; LSUM;
LSU GenBank JN713148); near Tadang base camp in mixed
Dicymbe–Aldina
forest on lateritic soils, 27 Dec 2009,
Henkel
9161
(BRG; HSU) and attached directly to roots of
A.
insignis
, 29 Dec 2009,
Henkel 9166
(BRG; HSU); REGION
10 UPPER DEMERARA-BERBICE: Mabura Ecological Re-
serve, field station at 5u09919.00N, 58u41958.90W, ,100 m;
vicinity of field station, under
D. altsonii
on brown sand
soils, 24 May 2011,
Aime 4284
(BRG; LSUM).
Commentary.
Theorangeperidiumof
E. digitatus
is
distinctive in the genus, and this along with the sub-
epigeous presentation of ascomata in clusters makes
them relatively easy to find in the field. The European
species
E. aculeatus
Vittad.,
E. anthracinus
Vittad.,
E.
echinatus
Vittad.,
E. leveillei
Tul. & C. Tul. and
E.
leucosporus
Vittad. have ascospores of similar size as
E.
digitatus
, but each has a black carbonaceous peridium
and a different pattern of ascospore ornamentation.
Elaphomyces cyanosporus
and
E. persoonii
have similarly
reticulate ascospore ornamentations with short, finger-
like projections from the wall margin, but both have
significantly larger ascospores than
E. digitatus
(28.0 mm
and 31.3 mm vs. 21.9 mmmeandiamrespectively).
Elaphomyces austrogranulatus
Castellano, Trappe &
Vernes from Australia has a brown peridium and
relatively small ascospores like
E. digitatus
but its
ascospore ornamentation is irregularly verrucose (Cas-
tellano et al. 2011). Other Australian
Elaphomyces
species
with ascospores of similar size have a black peridium.
Elaphomyces digitatus
was found fairly frequently in
long-term
D. corymbosa
macrofungal study plots in the
Upper Potaro Basin, with ascomata recorded in 16.3%
of 630, 100 m
2
sampling quadrats over 7 y (Henkel et al.
2011). The congener
E. compleximurus
(described
above) was never found in the study plots but recovered
sporadically in ‘‘off-plot’’ collecting forays. In addition
to
Dicymbe
spp.,
E. digitatus
appears to form mycorrhi-
zae with the papilionoid leguminous tree
A. insignis
.In
one collection of
E. digitatus
(
Henkel 9166
) the
ascomata were found directly attached to ECM roots
of this confirmed ECM host (Smith et al. 2011).
ACKNOWLEDGMENTS
This research was made possible by grants to TWH from the
National Science Foundation grant DEB-0918591, National
Geographic Society’s Committee for Research and Explora-
tion, Smithsonian Institution’s Biological Diversity of the
Guiana Shield Program, Linnaean Society of London, Hum-
boldt State University Foundation and to MCA from the
Explorer’s Club, Washington Group and NSF DEB-0732968.
Additional support was provided by a grant to SLM from NSF
DEB-1050292. Dillon Husbands functioned as Guyanese field
counterpart for several of the expeditions and assisted with
collection and description of specimens. Additional field
assistance in Guyana was provided by Mimi Chin, Christopher
Andrew, Leonard Williams, Valentino Joseph, Francino Ed-
mond and Luciano Edmond. Research permits were granted
by the Guyana Environmental Protection Agency. This paper is
No. 182 in the Smithsonian Institution’s Biological Diversity of
the Guiana Shield Program publication series.
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CASTELLANO ET AL.: NEW SPECIES OF
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LAPHOMYCES
1249
... Meanwhile, extra-European reports of Elaphomyces have regu larly been made, from South America (Spegazzini 1879), North America (Dodge 1929, Linder 1939, Trappe & Kimbrough 1972, Danielson 1979, Zhang & Minter 1989, Cázares et al. 1992, Beug et al. 2014, Castellano & Stephens 2017, Japan (Imai 1929, 1938, 1939-1940, Kobayasi 1960, South-Eastern Asia (Corner & Hawker 1953, Zhang 1991, and recently Taiwan (Hosaka et al. 2010), Guyana (Castellano et al. 2012c(Castellano et al. , 2016, tropical Africa (Buyck et al. 2016, Castellano et al. 2016) and Madagascar (Buyck et al. 2016). Recent investigations in Australia and New Zealand led to the recognition of 16 new species by Castellano et al. (2011Castellano et al. ( , 2012a. ...
... Finally, a new and remarkable genus close to Elaphomyces: Pseudotulostoma, was described from Guyana and Japan (Miller et al. 2001, Asai et al. 2004, Henkel et al. 2006). All these works concur in suggesting that the lineage Elaphomyces has an old Gondwanian origin, and current species have a continental or even regional distribution , 2012c, Reynolds 2011. Only very few worldwide distributed species are recognized (if any, possibly recently introduced), contrasting with high regional specific diversity, as described from Europe, Eastern Asia and Australia, and probably overlooked elsewhere, especially in Africa. ...
... Holotype: Pseudotulostoma volvatum ('volvata') O. K. Mill. & T.W. Henkel (after Reynolds 2011, Castellano et al. 2012c). Synonym. ...
Article
Elaphomyces (‘deer truffles’) is one of the most important ectomycorrhizal fungal genera in temperate and subarctic forest ecosystems, but also one of the least documented in public databases. The current systematics are mainly based on macromorphology, and is not significantly different from that proposed by Vittadini (1831). Within the 49 species recognised worldwide, 23 were originally described from Europe and 17 of these were described before the 20th century. Moreover, very recent phylogenetic treatments of the genus are mainly based on a few extra-European species and most common European species are still poorly documented. Based on an extensive taxonomic sampling mainly made in the biogeographically rich Cantabrian area (Spain), complemented with collections from France, Greece, Italy, Norway, Portugal and Sweden, all currently recognized species in Europe have been sequenced at the ITS and 28S of the rDNA. Combined phylogenetic analyses yielded molecular support to sections Elaphomyces and Ceratogaster (here emended), while a third, basal lineage encompasses the sections Malacodermei and Ascoscleroderma as well as the tropical genus Pseudotulostoma. Species limits are discussed and some taxa formerly proposed as genuine species based on morphology and biogeography are re-evaluated as varieties or forms. Spore size and ornamentation, features of the peridial surface, structure of the peridium, and the presence of mycelium patches attached to the peridial surface emerge as the most significant systematic characters. Four new species: E. barrioi, E. quercicola, E. roseolus and E. violaceoniger, one new variety: E. papillatus var. sulphureopallidus, and two new forms: E. granulatus forma pallidosporus and E. anthracinus forma talosporus are introduced, as well as four new combinations in the genus: E. muricatus var. reticulatus, E. muricatus var. variegatus, E. papillatus var. striatosporus and E. morettii var. cantabricus. Lectotypes and epitypes are designated for most recognised species. For systematic purposes, new infrageneric taxa are introduced: E. sect. Ascoscleroderma stat. nov., E. subsect. Sclerodermei stat. nov., E. subsect. Maculati subsect. nov., E. subsect. Muricati subsect. nov., and E. subsect. Papillati subsect. nov. Lastly, E. laevigatus, E. sapidus, E. sulphureopallidus and E. trappei are excluded from the genus and referred to Rhizopogon roseolus, Astraeus sapidus comb. nov., Astraeus hygrometricus and Terfezia trappei comb. nov. (syn.: Terfezia cistophila), respectively.
... Elaphomyces are hypogeous ectomycorrhizal false-truffles and there are about 70 to 101 species (Castellano et al. 2011(Castellano et al. , 2012a(Castellano et al. , b, 2016(Castellano et al. , 2017(Castellano et al. , 2018(Castellano et al. , 2021Shirakawa et al. 2020;Wijayawardene et al. 2020 (Castellano et al. 2016(Castellano et al. , 2012a. One ecological feature documented by Paz et al. (2017) indicates that Elaphomyces are widely eaten and dispersed by animals, particularly mammals. ...
... Elaphomyces are hypogeous ectomycorrhizal false-truffles and there are about 70 to 101 species (Castellano et al. 2011(Castellano et al. , 2012a(Castellano et al. , b, 2016(Castellano et al. , 2017(Castellano et al. , 2018(Castellano et al. , 2021Shirakawa et al. 2020;Wijayawardene et al. 2020 (Castellano et al. 2016(Castellano et al. , 2012a. One ecological feature documented by Paz et al. (2017) indicates that Elaphomyces are widely eaten and dispersed by animals, particularly mammals. ...
Article
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Pseudotulostoma is a genus described for fungi with stipitate sporocarps that have an exposed gleba and a woody, volvate base. The two species that belong to this genus (P. volvatum and P. japonicum) form unusual epigeous ascomata that are atypical among the hypogeous members of the Elaphomycetaceae. The genus was first described from the Guiana Shield and was suggested to be restricted to rainforests dominated by the ectomycorrhizal tree Dicymbe corymbosa (Leguminosae-Detarioideae). Pseudotulostoma volvatum was also later described from Colombia in association with Pseudomonotes tropenbosii (Dipterocarpaceae- Monotoidea). Here we report a new occurrence of P. volvatum that is also the first occurrence of an ectomycorrhizal Ascomycota fungus in a native host plant in Brazil. The description includes images of the macroscopic and microscopic characteristics, a discussion of the distinctive features, and phylogenetic placement using the nLSU of this fungus among Elaphomyces species. This new collection (third known location) demonstrates that P. volvatum also occurs in a white-sand forest composed of the canopy tree Aldina heterophylla (Leguminosae-Papilionoideae). Thus, we provide additional information regarding P. volvatum that expands its known distribution.
... Recently, some new Hysterangium species have been found in the Neotropics, associated with native tropical taxa. For example two undescribed Hysterangium species growing on a Dicymbe-dominated forest in the Guyana Shield region , as part of an ectomycorrhizal community, previously unknown to occur in those latitudes (Hosaka et al. 2008;Henkel et al. 2010;Castellano et al. 2012). Similarly, our studies showed an undocumented community of EcM fungi, including some hypogeous taxa, co-occurring in native fragments of the Atlantic rainforest in northeast Brazil (Sulzbacher et al. 2013;Sulzbacher et al. 2016;Sulzbacher et al. 2017). ...
Article
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Hysterangium basidiomata were collected associated with Coccoloba alnifolia and C. laevis (Polygonaceae), in the Guaribas Biological Reserve in the Atlantic rainforest, of northeastern Brazil during the rainy seasons of 2012-2013. Based on its unique morphological and molecular traits, this new taxon is described as Hysterangium atlanticum sp. nov. The most prominent morphological characters that separate H. atlanticum from other close relatives are the large size of the basidiomata, the white peridium that rapidly turns greyish-orange to pale-red where bruised or exposed to air, and the ellipsoid to suboblong spores with a minutely verrucose surface. Molecular analyses of the LSU, SSU, atp6, and EF-1α markers were done. The analyses of the concatenated atp6-EF-1α matrix confirmed the placement of the new species in the /hysterangium lineage. Moreover, at the infra-generic level, Hysterangium atlanticum sp. nov. forms a sister clade with Hysterangium sp. from Dicymbe forests located in neighboring Guyana. Moreover, the ectomycorrhizae (EcM) formed by H. atlanticum and roots of Coccoloba species was confirmed, based on identical ITS nrDNA sequences obtained from basidiomata and EcM root tissues. The main conspicuous features of the EcM are: a well-developed plectenchimatous mantle, the ramarioid, abundant emanating hyphae with clamps and covered with crystals, the presence of oleoacanthocystidia, and the whitish rhizomorphs. This is the first report of a Hysterangium species forming EcM with native members of Coccoloba spp. in South America.
... Members of the genus are characterized by fruiting-bodies consisting of a central chamber filled with yellow to brown, olive-brown to black or blue black powdery spore mass surrounded by a thick peridium (Hawker, 1954;Trappe, 1979;Castellano et al., 2012a,b). While Elaphomyces is a widespread genus and well represented in the north temperate forests and subtropical forests (Castellano et al., 2012b), only two members, Elaphomyces leucocarpus Vittad. and E. muricatus Fr., have so far been reported from Turkey (Türkoğlu et al., 2015). ...
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The hypogeous Ascomycete species, Elaphomyces granulatus is reported for the first time in Turkey. The morphological and microscopic characters of the species recorded in Turkey are reported together with the localities of collection, and the photographs related to its macro and micromorphology are provided.
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Article
We describe two new species of deer truffle, Elaphomyces marmoratus and E. fuscus spp. nov., collected from a secondary forest dominated by Quercus serrata, in Tokyo, Japan. Both species have morphological similarities to E. muricatus and E. granulatus; however, the former has a gleba without a purplish color and the latter has reticulated ascospores more closely resembling E. asperulus. Molecular phylogenetic analyses also support the assignment of these specimens as new species. ITS rDNA homologies with known species were low (<91% and <97%). In addition, phylogenetic trees using neighbor-joining and maximum likelihood methods showed that the sequences of the two new species each formed a monophyletic group within section Elaphomyces with bootstrap support of 99%. Analyses of ectomycorrhizal roots collected concurrently with the ascomata revealed that E. marmoratus is associated with at least Pinus densiflora, while E. fuscus is associated with at least Q. serrata.
Article
The North European species of Elaphomyces section Elaphomyces ( Eurotiales , Pezizomycotina ) are studied. Three new species, E. citrinopapillatus , E. pusillus , and E. roseoviolaceus are introduced and verified by morphology and sequence data from ITS, nuclear LSU, mitochondrial SSU, and β-tubulin. A lectotype for Elaphomyces granulatus is selected. Elaphomyces granulatus and E. muricatus are epitypified with sequenced material from the Femsjö region in South Sweden. Elaphomyces striatosporus is epitypified with sequenced material from the vicinity of the type locality in Norway. A key to all species of Elaphomyces occurring in Denmark, Norway, and Sweden is provided.
Article
A hypogeous, sequestrate, ectomycorrhizal fungus belonging to Elaphomyces was found in a Shorea plantation at Haurbentes Research Forest, West Java, Indonesia. Elaphomyces tropicalis is described as a new species based on morphological characters and molecular phylogenetic analysis of the ITS rDNA sequence. Sequences of E. tropicalis formed a distinct clade close to E. hassiacus, and sister to E. granulatus and E. asperulus. Elaphomyces tropicalis is not closely related to the E. papillatus clade. Morphologically, E. tropicalis is similar to E. (subsect Papillati) papillatus var. striatosporus with its crested spore ornamentation, but differs by having larger ascomata and different associated hosts. Shorea selanica and S. leprosula are the presumed hosts of E. tropicalis. This is the first report of an Elaphomyces species with Shorea species thus widening the previously known Elaphomyces host range.
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We describe three new species of Elaphomyces from eastern North America. Of the three, Elaphomyces loebiae is the rarest, known only from North Carolina and South Carolina, and appears to associate primarily with ectomycorrhizal hardwoods but possibly also with conifers. Elaphomyces cibulae is widely distributed but disjunct from Florida, Mississippi, and North Carolina. Elaphomyces cibulae seems to primarily associate with Quercus species. Elaphomyces mitchelliae has the widest distribution of the three species, from Florida, Maryland, North Carolina, Virginia, and West Virginia, and appears to associate with either ectomycorrhizal hardwoods and/or conifers. In the course of comparing our new Elaphomyces species to previously described European species we discovered that E. persoonii var. minor is conspecific in all essential details with and thus a synonym of E. cyanosporus.
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The sequestrate ascomycete genus Elaphomyces is described and illustrated from Australia. The following thirteen new species are described: Elaphomyces aurantias, E. austrogranulatus, E. chlorocarpus, E. cooloolanus, E. coralloideus, E. laetiluteus, E. nothofagi, E. pedicellaris, E. queenslandicus, E. rugosisporus, E. suejoyceae, E. symeae, and E. timgroveii. A key is provided to all Elaphomyces species from Australia.
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Ectomycorrhizal (ECM) fungi historically were considered poorly represented in Neotropical forests but in the central Guiana Shield substantial areas are dominated by leguminous ECM trees. In the Upper Potaro Basin of Western Guyana, ECM fungi were sampled for 7 years during the rainy seasons of 2000–2008 in three 1-ha plots in primary monodominant forests of the ECM canopy tree Dicymbe corymbosa (Fabaceae subfam. Caesalpinioideae). Over the plot sampling period sporocarps of 126 species of putative or confirmed ECM fungi were recovered. These taxa represented 13 families and 25 genera of primarily Agaricomycetes, but also Ascomycota (Elaphomycetaceae), the majority of which are new to science. Russulaceae contained the most species (20 Russula; 9 Lactarius), followed by Boletaceae (8 genera, 25 spp.), Clavulinaceae (17 Clavulina), and Amanitaceae (16 Amanita). An additional 46 species of ECM fungi were collected in forests of the Upper Potaro Basin outside the study plots between 2000 and 2010, bringing the regional number of ECM species known from sporocarps to 172. This is the first longterm ECM macrofungal dataset from an ECM-dominated Neotropical forest, and sporocarp diversity is comparable to that recorded for ECM-diverse temperate and boreal forests. While a species accumulation curve indicated that ECM sporocarp diversity was not fully recovered inside of the plots, nearly 80% of the total species were recovered in the first year. Sequence data from ECM roots have confirmed the ECM status of 56 taxa represented by corresponding sporocarp data. However, around 50% of ECM fungal species from roots remain undiscovered as sporocarps, leading to a conservative estimate of at least 250 ECM species at the Potaro site. Dicymbe forests in Guyana are a hotspot for ECM fungal diversity in the Neotropics.
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Dominance of primary rain forests by the ectomycorrhizal, leguminous canopy tree Dicymbe corymbosa (Caesalpiniaceae) was investigated in the Pakaraima Mountains of western Guyana. In five 1-ha forest inventory plots in the Upper Ireng and Upper Potaro River drainages basal areas of D. corymbosa ranged from 38.4-52.8 m2 ha-1 (63-85% of total) among all trees [greater-than-or-equal]10 cm diameter at breast height (dbh), values in the upper range for tropical moist forests worldwide. The high basal areas for D. corymbosa were due to the prevalence of large (>150 cm dbh), multi-stemmed individuals. Stem densities in Dicymbe plots ranged from 276-433 ha-1, with D. corymbosa contributing 24.6-59.8%. In three 1-ha mixed forest plots adjacent to the Dicymbe plots, D. corymbosa was absent. In the mixed forests, stem densities were higher (480-585 ha-1), basal areas were lower (36.7-39.8 m2 ha-1), species diversity was higher, and canopy tree species were more equitably distributed than in the Dicymbe plots. Tree community composition was not qualitatively different between Dicymbe and mixed forests. In the Dicymbe plots, mean sapling and seedling densities of D. corymbosa were significantly higher than most other canopy species, indicating persistent monodominance. Edaphic variation did not account for variation in forest composition. Life history traits are discussed which may contribute to clumping in D. corymbosa, including coppicing and mast-fruiting, and the potential role of litter-trapping physiognomy and ectomycorrhiza-mediated nutrient dynamics in promoting monodominance is noted.
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Pseudotulostoma volvata gen. sp. nov. is described from the south-central Pakaraima Mountains of Guyana. Pseudotulostoma volvata is associated with ectomycorrhizal Dicymbe corymbosa trees (Caesalpiniaceae) and placed in the Ascomycota, Eurotiales, Elaphomycetaceae. Included are a description of the genus and species, illustrations of the macroscopic and microscopic features, and a discussion of the distinctive features and phylogenetic placement of this fungus.
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• The ectomycorrhizal (ECM) symbiosis was historically considered restricted to the temperate zones, but recent studies have shown the importance of this symbiosis across the tropics. We examined ECM fungal diversity, host plant phylogeny and ECM host preferences in a rainforest dominated by the leguminous host plants Dicymbe corymbosa, Dicymbe altsonii and Aldina insignis. • Ectomycorrhizal fungi were identified by internal transcribed spacer rDNA sequencing and host species were verified with chloroplast trnL sequencing. To test whether Dicymbe and Aldina represent independent gains of the ECM symbiosis, we constructed a Fabaceae phylogeny using MatK and trnL. We identified four independent ECM lineages within the Fabaceae. • We detected a diverse community of 118 ECM species dominated by the /clavulina, /russula-lactarius, /boletus, and /tomentella-thelephora lineages. Ectomycorrhizal species in Agaricales, Atheliales and Polyporales may represent previously unrecognized tropical-endemic ECM lineages. Previous studies suggested that ECM fungi did not diversify in the tropics, but the /clavulina lineage appears to have a center of diversity in tropical South America. • Dicymbe and Aldina represent independent gains of the ECM symbiosis in Fabaceae but their fungal symbionts showed no host preferences. Spatial factors are more important than hosts in structuring the ECM fungal community in this ecosystem.
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Advances in phylogenetic systematics have clarified the position of most major homobasidiomycete lineages. In contrast, the status of the Crepidotaceae, a historically controversial family of dark-spored agarics, remains unaddressed. In this paper, current morphology-based classifications of the agaric genera of the Crepidotaceae were evaluated by parsimony and constraint analyses of sequence data from the nuclear large subunit rDNA. Taxa analyzed included the type species for each agaric genus allied in the family by Singer: Crepidotus, Simocybe, Pleurotellus, Tubaria, and Melanomphalia. Contrary to traditional classifications, results suggest that the crepidotoid fungi have three separate origins within the euagarics. The Crepidotaceae sensu stricto (s.s.) includes Crepidotus and Simocybe and represents a separate lineage of dark-spored euagarics. Pleurotellus is congeneric with Crepidotus. Results indicate the exclusion of both Tubaria and Melanomphalia from the Crepidotaceae s.s. Tubaria is allied with the strophariaceous taxa Phaeomarasmius and Flammulaster, while Melanomphalia has arisen from within a lineage of light-spored omphalinoid euagarics representing an independent acquisition of basidiospore pigmentation. Other pleisiomorphic and newly uncovered synapomorphic characters are discussed in detail along with the taxonomic status of each genus, and a revised family description is provided.
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Pseudotulostoma volvata (O. K. Mill. and T. W. Henkel) is a morphologically unusual member of the otherwise hypogeous Elaphomycetaceae due to its epigeous habit and exposed gleba borne on an elevated stalk at maturity. Field observations in Guyana indicated that P. volvata was restricted to rain forests dominated by ectomycorrhizal (EM) Dicymbe corymbosa (Caesalpiniaceae), suggesting an EM nutritional mode for the fungus. In this paper, we confirm the EM status of P. volvata with a combination of morphological, molecular, and mycosociological data. The EM status for P. volvata corroborates its placement in the ectotrophic Elaphomycetaceae.
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The following species are described: Hydnangium virescens n.sp., H. echinulatum n.sp., Arcangeliella beccarii (Petri) Dodge & Zeller, A. malaiencis n.sp., Elasmomyces borneensis (Petri) Dodge & Zeller, E. malaiensis n.sp., Stephanospora penangensis n.sp., Wakefieldia striaespora n.gen., n.sp., Chamonixia mucosa (Petri) Corner & Hawker n.comb., C. octorugosa n.sp., Dendrogaster cambodgensis Patouillard, D. aurantius n.sp., Hymenogaster viscidus Massee & Rodway, Hysterangium purpureum Zeller & Dodge var. malaiense n.var., Elaphomyces singaporensis n.sp., E. carbonaceus n.sp.