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Elaphomyces muricatus (Ascomycota), a new record for hypogeous fungi in Armenia

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Elaphomyces muricatus, new for Armenia, and E. granulatus have been found in the forests of Vanadzor and Dilijan in Armenia. Morphology, anatomy, as well as ecology and geographical distribution of E. muricatus are described. The ecological adaptation and geographical distribution of the genus Elaphomyces are wider than known before.
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Österreichische Zeitschrift für Pilzkunde
Austrian Journal of Mycology
An International Journal of Mycology
ISSN 1021-2450
Volume 22 (2013)
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Österr. Z. Pilzk. 22 (2013) 7
Elaphomyces muricatus (Ascomycota), a new record for hypogeous fungi
in Armenia
ROMAN HOVSEPYAN
Group of Archaeobiology, Institute of Archaeology and Ethnography NAS
15, Charents str.
0025, Yerevan, Armenia
Email: roman.hovsepyan@yahoo.com
Accepted 11. 2. 2013
Key words: Ascomycetes, Elaphomyces muricatus, E. granulatus. – Hypogeous fungi, mycorrhizal
fungi, biodiversity, ecology. – Mycobiota of Armenia.
Abstract: Elaphomyces muricatus, new for Armenia, and E. granulatus have been found in the forests
of Vanadzor and Dilijan in Armenia. Morphology, anatomy, as well as ecology and geographical dis-
tribution of E. muricatus are described. The ecological adaptation and geographical distribution of the
genus Elaphomyces are wider than known before.
Zusammenfassung: Elaphomyces muricatus, neu für Armenien, und E. granulatus wurden in den
Wäldern von Wanadsor und Dilijan in Armenien gefunden. Morphologie, Anatomie sowie Ökologie
und geografische Verbreitung von E. muricatus werden beschrieben. Die ökologische Anpassungs-
fähigkeit und geografische Verbreitung der Gattung Elaphomyces ist größer als bisher bekannt.
Аннотация: Elaphomyces muricatus, новый для Армении гриб, и Е. granulatus были обна-
ружены в лесах Ванадзора и Дилижана в Армении. Морфология, анатомия, а также экология и
географическое распространение E. muricatus описаны. Род Elaphomyces имеет более широкую
экологическую адаптацию и географическое распространение, чем было известно раньше.
The biocycle of the hypogeous fungi, including formation and maturating of fruitbodies, oc-
curs underground and spores are dispersed passively after destruction of fruitbodies and via
animals. Hypogeous fungi include species from Ascomycota, Basidiomycota, Zygomycota,
Glomeromycota and mitosporic fungi. They mostly are mycorrhizal; the main symbionts are
wide spread trees, such as species of Quercus, Fagus, Corylus, Carpinus, Populus, Salix,
Tilia, and Pinus. Many hypogeous fungi are valuable edible species (e.g. Tuber spp., Choi-
romyces meandriformis, Terfezia leonis, Rhizopogon spp.). Some of them have medicinal
features and other uses, for example Elaphomyces muricatus, the fungus discussed below, is
noted to have sacral use in Mexico (GUZMÁN 2008) and was used as aphrodisiac in Europe
(HAWKER 1954).
The following hypogeous fungi have been found in Armenia so far: Tuber aestivum VIT-
TAD. (TASLAKHCHYAN & NANAGULYAN 1988, NANAGULYAN & TASLAKHCHYAN 1991); T.
rufum PICCO, T. rapaeodorum TUL. & C. TUL., T. scruposum R. HESSE (BADALYAN & al.
2005); Tirmania pinoyi (MAIRE) MALENÇON, Hydnotrya tulasnei (BERK.) BERK. & BROOME,
Picoa juniperi VITTAD., Elaphomyces granulatus FR. (NANAGULYAN & TASLAKHCHYAN
1991); E. muricatus F
R. (only shortly noted in HOVSEPYAN 2006) (Ascomycota); Hy-
menogaster griseus VITTAD., H. olivaceus VITTAD., Octaviania stephensii (BERK.) TUL. & C.
TUL. (HOVSEPYAN 2006); Rhizopogon roseolus (CORDA) TH. FR. (MELIK-KHACHATRYAN &
NANAGULYAN 1983); R. luteolus FR. (MELIK-KHACHATRYAN & MARTIROSYAN 1971); Cremeo-
8 R. HOVSEPYAN: Elaphomyces muricatus in Armenia
gaster klikae MATTIR. (NANAGULYAN 1987, NANAGULYAN & OSIPYAN 2000) (Basidiomy-
cota); and Glomus macrocarpum TUL. & C. TUL. (HOVSEPYAN 2006) (Glomeromycota).
Elaphomyces muricatus will be introduced below with details.
Materials and methods
The fruitbodies of Elaphomyces, herbarium of host plants, and soil samples were collected, and notes
of ecological conditions were recorded during field investigations at the forests of Armenia in 2003-
2005. Objects for field observations were hypogeal fruitbodies, vegetation and soil covers, host plants,
geographical and environmental conditions of the localities for hypogeal fungi. Fruitbodies of
hypogeal fungi were found by digging around of roots of the potential host plants. The affiliation to
genetic horizon, soil layer, thickness of litter layer, vegetation cover and position (depth) of fruitbody
were recorded for each soil sample. Types of soils were preliminarily identified in the field. Some
geographical parameters (microrelief) also were recorded during field works.
Light microscopes were used for micromorphological and anatomical studies, identifications, de-
scription and biometry (magnification: × 100-1350). Illustrations of fruitbodies were made with scan-
ner or digital camera, microphotographs with digital camera and microscopes.
Identification of the fruitbodies was carried out with HAWKER (1954), LAWRYNOWICZ (1988) and
PEGLER & al. (1993). Taxonomy and names of authors of species are given according to www.
indexfungorum.org. Plant species have been identified with the "Flora of Armenia" (TAKHTAJYAN 1954-
2010).
The first stages of this study were done in the Scientific centre of soil science, agrochemistry and
melioration MA of Armenia and in the Faculty of Biology, Yerevan State University.
Specimens examined (Herbarium acronyms are given in [ ]: ERHM = Yerevan State University
Cryptogamic Herbarium, FBBL = Fungal Biology and Biotechnology Lab of Yerevan State Univer-
sity, CMI-Unibo = Center of Mycology of Bologna University):
Elaphomyces muricatus: Armenia: district Vanadzor, locality Vanadzor-1, eastward from
“Tsitsernak Children's Camp”, 01. 06. 2003, leg. & det.: R. HOVSEPYAN, specimens no: V1a-q
[FBBL], 2189 [CMI-Unibo]; - idem, 12. 07. 2004, specimen no: 10812 [ERHM]. – Dilijan, locality
Dilijan-5, from right bank of Kalavan river, south from Kalavan village, broad-leaved forest with
domination of Carpinus, 22.07.2005, leg. & det. R. HOVSEPYAN, specimens no: 10813 [ERHM],
D35a-b [FBBL].
Elaphomyces granulatus: Armenia: Vanadzor, locality Vanadzor-2, right bank of Vanadzor river,
park of Pinus, 01. 06. 2003, leg. & det. R. HOVSEPYAN, specimen no: V2 [FBBL].
Description of morphology and anatomy of the specimens found in Armenia
Elaphomyces muricatus FR. forma muricatus
Etymology: Elaphomyces, from Greek ελαφος, a slag and μυκης, a fungus; from
Latin “muricatus”, roughened with short, hard points. English name: Rough-coated deer
truffle.
As c o m a t a : hypogeous cleistothecia, globose or subglobose, sometimes slightly de-
pressed, commonly 5-20 mm in diam., firm, hard when dry, yellowish-ochraceous or
yellowish-brown, usually darker and duller with age, the surface densely covered with
warts (Fig. 1 a).
Sme l l : slight, not distinctive.
Pe r i d i u m : firm, 1.2-2.0 mm thick, two-layered. External layer (cortex) with
small pyramidal warts formed by densely interwoven hyphae, c. 0.5 mm thick, dark
yellowish-brown. Warts in average 164 μm high and (246-)287(-328) μm wide at base.
Österr. Z. Pilzk. 22 (2013) 9
Fig. 1. Elaphomyces muricatus found in Fagus and Carpinus forest in the valley of Vanadzor river
(Vanadzor-1, 01. 06. 2003); a ascocarp, b peridium, c-e asci and ascospores.
10 R. HOVSEPYAN: Elaphomyces muricatus in Armenia
Fig. 2. Habitus of Elaphomyces muricatus in the valley of Kalavan river (Dilijan-5, 22. 07. 2005).
Österr. Z. Pilzk. 22 (2013) 11
Internal layer also consisting of interwoven hyphae, c. 1 mm thick, relatively light col-
oured, yellowish, distinctly marbled when mature (Fig. 1 b).
Gl e b a : with single cavity, at first empty, later permeated with ascogenous hy-
phae, and at maturity filled with a powdery mass of blackish-brown spores. Ascoge-
nous hyphae visible as thin and fine white loosely woven veins originating from pe-
riphery and going to the centre (Fig. 1 a).
A s c i : subglobose, widely ellipsoid or irregular, 30-60 μm, thin-walled, evanescent,
2,3,5-spored (Fig. 1 c-e).
A s c o s p o r e s : globose, (8-)10-20(-26) μm in diam., at first hyaline, yellowish-
brown, becoming dark brown to blackish and almost opaque in transmitted light at
maturity, thick-walled, ornamented with closely spaced blunt spines or rods 2-3 μm
high, irregularly arranged into blocks and variable in appearance (Fig. 1 c-e).
Elaphomyces granulatus FR.
One old and partly decomposed fruitbody of Elaphomyces was found in a Pinus park
at Vanadzor river valley (Location: Vanadzor-2; Sample: V2 [FBBL]), which seems to
be E. granulatus. The fruitbodies of E. muricatus are similar in appearance to those of
E. granulatus but may be readily distinguished by the marbled peridium, smaller
spores (E. muricatus - 10-25 μm, E. granulatus - 20-35 μm) and different number of
spores in the asci (E. muricatus - 2-6, E. granulatus - 6-8; HAWKER 1954, PEGLER &
al. 1993; LAWRYNOWICZ 1988).
Description and ecology of the Elaphomyces localities in Armenia
Fruitbodies of Elaphomyces were found at three places (named Vanadzor-1, Vanad-
zor-2 and Dilijan-5) in the middle mountainous zone forests of North-Eastern Arme-
nia. Type of soil corresponded to the desaturated subtype of mountainous-sylvan gray
type soils, see Soils map of Republic of Armenia (EDILYAN 1990); also verified by
pedological analyses (HOVSEPYAN 2004, 2006). All localities are in the moderate cold
forest climatic zone. Winter is long and snowy with frequent frosts. In Vanadzor the
middle air temperature in winter is from – 5.0 °C to -0.4 °C, and in Dilijan it is from -
2.1 °C to +1.2 °C. Spring also is long and humid. Summer is mild with dominance of
warm weathers. The middle air temperature in summer varies from +14.7 °C to +19.3
°C in Vanadzor and from +15.3 °C to +19.6 °C in Dilijan. Autumn is cold and rainy in
the second half. In Vanadzor and Dilijan annual precipitations are c. 570 mm. Average
monthly precipitation in summer is 72 mm in Vanadzor and 68 mm in Dilijan
(BAGHDASARYAN 1962).
Vanadzor-1 locality is in the south of Vanadzor town, in the valley of Vanadzor
river, which is a tributary of Debed river (tributary of Kura river). Alltogether 19
fruitbodies of Elaphomyces muricatus in different states of maturity were found on
01.06.2003 and 12.07.2004 on a 30-60° inclined slope of northern orientation of the
left bank of the river, about 1520 m s. m., c. 50 m higher than the river. The territory is
covered with beech forest; the dominant species are Fagus orientalis, Acer
platanoides, Cerasus avium, and Sambucus nigra. The fruitbodies were found near
Fagus orientalis, from the surroundings of its roots, were grass cover was extremely
scarce. Litter layer was about 5 cm thick. Fruitbodies were found from А0А genetic
horizon of soil, from 10-15 cm depth.
12 R. HOVSEPYAN: Elaphomyces muricatus in Armenia
Soil sample analyses showed that it is a heavy sandy-clay soil (i.e. ratio of particles
between 1.00-0.01 mm and smaller particles respectively is 54.3% and 45.7%) with a
high stoniness level (i.e. stones, particles larger than 3 mm, 10.4%; gravel, particles
between 1-3 mm, 3.0%; and fine soil, particles smaller than 1 mm, 86.6% of the total
weight), rich in organics (23%) and humus rich (14.5%). There are no carbonates in
that soil and it has a slightly acid reaction (pHH2O = 5.95) (HOVSEPYAN 2006).
Vanadzor-2 locality is several hundred meters north of Vanadzor-1, on the right
bank of Vanadzor river. One old fruitbody of Elaphomyces was found on 01. 06. 2003
from a 30° inclined slope of north-eastern orientation, c. 1400 m s. m. The slope is
covered with pines. The fruitbody was found under Pinus kochiana. Grasses were
practically absent under the trees.
Dilijan-5 locality is several hundred meters south of Kalavan village, in the valley
of Kalavan river, which is a tributary of Getik, and Getik is a tributary of Aghstev
(tributary of Kura). The locality is in the territory of the Palaeolithic archaeological
site of Kalavan-1. One mature and one immature fruitbody of Elaphomyces muricatus
were found amongst roots of Carpinus betulus, on 22. 07. 2005 on a 30° inclined slope
of south-western orientation of the right bank of the river, at 1650 m s. m., several ten
meters higher than the river. The slope is covered with a hornbeam-oak forest, where
Carpinus betulus, Quercus macranthera, Fagus orientalis, Ulmus laevis, Acer
campestre and A. platanoides are the main species and also species of Salix, Fraxinus,
Rosa, Crateagus, Lonicera, Malus, Pyrus, Cerasus, Viburnum and Prunus are present.
The fruitbodies were found directly near Carpinus betulus, between its roots (Fig. 2).
Fruitbodies were found in the soil genetic horizon А, in 10 cm depth.
Soil sample analyses from 5-20 cm depth of genetic horizon А showed that it is a
middle sandy-clay soil (ratio of particles between 1.00-0.01 mm and smaller particles
respectively was 55.2% and 44.8%) with middle level stoniness (stones, 8.1%, gravel,
5.6%, and fine soil, 86.3% of the total weight). The soil was also rich in organics
(15%) and had middle humus content (7.1%). There were no carbonates and it had a
neutral reaction (pHH2O=6.60) (HOVSEPYAN 2006).
Discussion
Elaphomyces muricatus and E. granulatus very often occur in the same territories and
can be considered as two of the most widely distributed species of the genus. Those
species occur throughout Europe, and are also known from Asia and North America.
The finding of Elaphomyces muricatus in Armenia along with recent findings of this
and other Elaphomyces species from other countries (KONSTANTINIDIS & KAOUNAS
2012, LACHEVA 2012, WANG 2011, LÆSSØE & al. 2009, KUTORGA & KATARŽYTĖ
2008) shows that geographical distribution and ecological adaptation of these fungi are
wider than known so far. Recent publications show that Elaphomyces, particularly E.
muricatus and E. granulatus, grow also in northernmost countries (e.g., Norway), can
reach up to middle and high mountainous zones (e.g. E. muricatus and E. granulatus
in Armenia and E. granulatus in Taiwan) and that the preference of host plants and
soil conditions are wider (for details see also PEGLER & al. 1993, LAWRYNOWICZ
1988, HAWKER 1954, KONSTANTINIDIS & KAOUNAS 2012, CAZARES 1992, WANG
2011).
Österr. Z. Pilzk. 22 (2013) 13
In Armenia hypogeal fungi are rare and have a very limited distribution thus they
need protection. We suggest including Elaphomyces muricatus in the Red List of
Fungi of Armenia.
My appreciations go to Dr S. G. NANAGULYAN, Dr L. L. OSIPYAN (Chair of Botany, Faculty of
Biology, Yerevan State University) and Dr I. KRISAI-GREILHUBER for constructive criticism, which
enabled me to make important improvements in the final version of this article. Field work at Vanad-
zor was done with great help of GEVORG and YEGOR APRESYANS.
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... Ecology: Elaphomyces granulatus was reported to grow under the members of needle or broad-leaved trees such as Pinus, Picea, Quercus, Cistus, Fagus and Castanea (Arroyo et al., 2005;Kutorga and Kataržytė 2008 Elaphomyces granulatus is one of the most common and the earliest scientifically named hypogeous species of the genus Elaphomyces (Paz et al., 2017) and often occurs in the same territories with E. muricatus. The fruitbodies of the two species are similar in appearance, but E. muricatus differs from E. granulatus with the marbled peridium, smaller spores and lower spore number in the asci (2-6) (Hovsepyan, 2013). ...
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The study of hypogeous fungi has been neglected in Britain from the time of Berkeley & Broome until that of the present investigation. During the years 1948-53 some 700 collections have been made, mainly in the Bristol area, but also from other parts of England, Scotland, North Wales and Northern Ireland. These include members of the Phycomycetes (Endogone spp.), Ascomycetes (Elaphomycetaceae, Tuberales) and Basidiomycetes (Gasteromycetes). Some species were found sufficiently often to permit tentative conclusions to be drawn relating to the effect of weather and soil conditions on the production of fruit-bodies. Most of the species previously recorded in Britain have been collected and some new records made. Descriptions are given of all recorded British species, and most of these are illustrated by line drawings made from fresh material. Details of development are given for representative species and the probable relationships within the group and with other fungi are discussed.
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Hallucinogenic Mushrooms in Mexico: An Overview. Psilocybe, with 53 known hallucinogenic species in Mexico, is the most important and diverse group of sacred mushrooms used by Mexican indigenous cultures. Psilocybe caerulescens, known by the present-day Nahuatl Indians as teotlaquilnanácatl, is hypothesized to be the ceremonially-used teonanácatl mushroom cited by Sahagún in the 16th century, the true identity of which has remained obscure for centuries. Correcting a widely disseminated error derived from early published information on Mexican hallucinogenic mushrooms, emphasis is placed on the fact that Panaeolus species have never been used traditionally in Mexico. Reports of the use of species of Amanita, Clavaria, Conocybe, Cordyceps, Dictyophora, Elaphomyces, Gomphus, Lycoperdon, Psathyrella, and Stropharia as sacred or narcotic mushrooms are discussed. A brief history of the discovery of hallucinogenic mushrooms in Mexico is presented, as well as notes on their taxonomy, distribution, and traditional use in Mexico.
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BAGHDASARYAN, A. B., 1962: Climate. -In: Geology of Armenian SSR, 1 (Geomorphology), pp. 23-53. -Yerevan: Publ. AS Arm. SSR. / БАГДАСАРЯН, А. Б., 1962: Климат. -В кн.: Геология Арм. ССР, 1 (Геоморфология), с. 23-53. -Ереван: Изд. АН Арм. ССР.
1990: Soils map of Republic of Armenia
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EDILYAN, R. A., (Chief Ed.), 1990: Soils map of Republic of Armenia. – Yerevan. / АТЛАС ПОЧВ РЕСПУБЛИКИ АРМЕНИЯ, ЭДИЛЯН Р. А., (Глав. ред.) 1990. – Ереван.
British hypogeous fungi. – Philos. Transact
HAWKER, L. E., 1954: British hypogeous fungi. – Philos. Transact. Roy. Soc. London, ser. B, Biol. Sci. 237 (No. 650): 429-546.