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Eco-morphologic aspects of differentiation and identification of species Armillaria mellea Sensu Lato in Coppice Oakeries of Belgorod Region for the purposes of exploitation of natural resources.


Honey fungus Armillaria mellea (Vahl.) Karst., which was earlier considered as a one polymorphic species, has been divided into 5 groups, which cannot be hybridized among themselves and have the status of a biological species [1-3], with the help of a genetic test. Nowadays instead of talking about Armillaria mellea (Vahl.) Karst. we mention Armillaria mellea sensu lato, that is the Armillaria complex, comprising the following closely related species: A. borealis Marxm. & Korhonen A. cepistipes Velen., A. ostoyae (Romagn.) Herink, A. gallica Marxm. & Romagn., A. mellea (Vahl: Fr.) Kumm. (A. mellea sensu stricto) [3-7]. In Russia, as earlier in Western Europe, all 5 species of A. mellea s. l. mentioned above were discovered and accurately identified (with the help of the genetic test) [3].

Besides genetic incompatibility, distinguished species of A. mellea s. l. have macromorphological (at the level of macrostructures: rhizomorph and fruit body) and ecological differences. On the basis of these differences comparative descriptions of the species A. mellea s. l. were elaborated [4-5, 7-9].

Importance of preliminary (before using the genetic test) differentiation and identification of the species Armillaria in the field can be connected with necessity for receiving source information on occurrence and confinedness of separate species in certain regions, depending on type and tempo of natural resources exploitation. The aim of our work was to detect (differentiate and identify) the species A. mellea s. l. according to eco-macromorphological characters in coppice oakeries of Belgorod region in Russian Federation.


Object of the research is the complex A. mellea s. l. in coppice oakeries of Shebekinsky and Belgorod districts of Belgorod region in Russian Federation. Field studies were carried out in 2010-2013 in oak timber stands with prevailing English oak (ripening and ripe) as part of mountain, ravine and watershed oakeries. In the process of the work implementation we used methods of phytopathology and mycology [10], system analysis [11].

Main part:

General description of representants of A. mellea s. l. in coppice oakeries in Belgorod region. Modern systematics of fungic organisms ( and qualifies honey fungi species A. mellea s. l. as kingdom Fungi (or Mycota), phylum Basidiomycota, class Agaricomycetes, order Agaricales, family Physalacriaceae. They are saprotrophs and semi-saprotrophs (facultative parasites), and are characterized by polytrophy, but at the same time they are distinguished by substrate specificity. They induce white sapwood rot.

Main distinctive macromorphostructures of A. mellea s. l. in the wild are rhizomorphs in surface soil, on trees roots and under cortex, white coat of mycelium under cortex of stressed trees and fruit bodies.

Ecomorphotypes A. mellea s. l. in Belgorod region's oakeries. On the basis of obtained empirical (verbaldescriptive and photo-documentary) material we discriminated 2 ecomorphotypes in the complex A. mellea in loco (fig. 1-2) and composed their detailed description without using biometric parameters (table 1).

Comparative analysis of similarity of local ecomorphotypes descriptions and A. mellea s. l. known species descriptions. Analysis was performed according to known characters-criteria [4-9] taking into account quality of their display distinctiveness.

The most reliable macromorphological criterion for division of species in the complex A. mellea s. l. is peculiarities of construction of a ring on a stipe. The following three species have a stiff and solid ring which does not disappear over time: A. borealis, A. ostoyae and A. mellea s. str. [4-9]. A mealy, web-like ring, which disappears fast, is a distinctive feature for species A. cepistipes and A. gallica [4-9]. Also the last two species belong to the ecological group of saprotrophs [4, 6, 9]. Only in some cases they can be facultative parasites and poor pathogens. In phytopathological processes they usually play a secondary role [9]. If we refer to description of ring's construction peculiarities and ecological peculiarities of local ecomorphotypes (see table 1, fig. 1-2), we should see that both of them belong to the grouping of species A. cepistipes--A. gallica. This conviction is reinforced also by the result of rhizomorphs macrostructure comparison: rhizomorphs of local ecomorphotypes (see table 1) and representants of A. cepistipes--A. gallica [4, 7, 9] are characterized by monopodial ramification. As for geographical information about expansion of A. cepistipes and A. gallica, it is known that these species are found everywhere, both in Western and Eastern Europe, including Belarus, Ukraine and Russia [3], and also in Siberia [4]. Besides, A. gallica was exactly identified in oakeries of Voronezh region [3], which share borders with Belgorod region. Thus, there is no doubt that ecomorphotypes we investigate (see table 1) belong to A. cepistipes--A. gallica.

The next identification stage is detection of belonging of each of two local ecomorphotypes to a certain species: A. cepistipes or A. Gallica according to colour and form of cap, stipe, size and concentration of squames on fruit bodies' caps [4].

Form of a cap of ripe fruit bodies of A. cepistipes is often characterized [4, 9] as a flat-convex, its colour is grey, yellow or flesh. Form of a cap of ripe fruit bodies of A. gallica is often characterized [4, 9] as convex with a mount in the centre, its colour is red, yellow, brown or olive. Cap's edge is striped with remains of partial veil.

Cap's squames of A. gallica are bigger and more dense than of A. cepistipes--especially it is noticeable with young fruit bodies [4]. Squames of ripe fruit bodies partially disappear [4]. Opinions on squames' concentration are discrepant [4-9], so we do not consider this character.

Stipes of both A. cepistipes and A. gallica is cylindrical, often has a claviform thickening at the bottom [49]. Stipe of A. cepistipes below a ring is usually lighter, without remains of partial veil, sometimes is of a lightyellow hue at the bottom. Ring of A. cepistipes is neat, whitish-grey [4, 9]. A. gallica's stipe below a ring is usually darker, with remains of partial veil, yellowing at the bottom. Ring of A. gallica is whitish with an express yellow hue and uneven edges [4, 9], when ring disappears--a yellow print may appear on a stipe.

Gills of A. cepistipes are decurrent, at first white, then reddish with spots [4]. Gills of A. gallica are adnate or slightly decurring on to a stipe, at first white, then up to pink-brown [4].

Fruit bodies of A. cepistipes grow in groups, joints or separately on stumps and trunks of foliage trees [4, 9]. Fruit bodies of A. gallica grow separately and in solitary groups on cavings of burnt wood, on windfall and stumps of foliage species [4, 9], often at the bottom of living trees [4, 9].


Considering above given descriptions of peculiarities of A. cepistipes and A. gallica, known from special sources, we successively compared characters of one of the known species (A. cepistipes) with corresponding characters of, in turn, ecomorphotype #1 and ecomorphotype #2 (see table 1, fig. 1-2). Then of another one--A. gallica--with corresponding characters of, in turn, ecomorphotype #1 and ecomorphotype #2 (see table 1, fig. 1-2). Results were recorded as a conditional similarity quotient, expressed in fractional form, where denominator is general number of categories of characters under comparison, and numerator is number of descriptions coinciding in essence. Ecomorphotype #1--A. cepistipes (1/8), A. gallica (8/8). Ecomorphotype #2--A. --cepistipes (8/8), A. gallica (1/8). From this it follows that ecomorphotype #1 is most probably a species A. gallica, and ecomorphotype #2--A. cepistipes.


Thus, we can draw conclusion that in coppice oakeries of Belgorod region of Russian Federation the complex Armillaria mellea sensu lato is represented by two species A. cepistipes Velen. and A. gallica Marxm. & Romagn. For each of two species an eco-macromorphological description was composed; these descriptions allow to differentiate and identify them in the field with high confidence.


Article history:

Received 25 March 2014

Received in revised form 20 April 2014

Accepted 15 May 2014

Available online 5 June 2014


The research was supported by the Russian Science Foundation (project N[degrees] 14-17-00171) regarding subject: "Regional responses of environmental components caused by climate change with different periodicity : South Central Russian upland forest".


[1] Korhonen, K., 1978. Interfertility and clonal size in the Armillaria mellea complex. Karstenia, 18: 31-42.

[2] Radzievskaja, M.G., 1989. Struktura kompleksa Armillaria sensu lato. Avtoref. diss...kand. biol. nauk. Moskva, 23s.

[3] Selochnik, N.N., 2008. Biologicheskie vidy roda Armillaria v Rossii / Materialy 2-go S#ezda mikologov Rossii. Tezisy dokladov.--M.: Nacional'naja akademija mikologii, S. 90.

[4] Pavlov, I.N., A.G. Mironov, N.P. Kutaf'eva, 2006. Morfologicheskie priznaki gribov kompleksa Armillaria mellea sensu lato Cirkumboreal'noj oblasti // Hvojnye boreal'noj zony. Teoreticheskij i nauchno prakticheskij zhurnal. Federal'noe Agentstvo Obrazovanija. Gl. red. I.N. Pavlov., 3: S. 14-21.

[5] Watling, R., et al., 1982. The genus Armillaria--nomenclature, typification, the identity of Armallaria mellea and species differentiation. Trans. Br. Mycol. Soc., 78(2): 271-285.

[6] Guillaumin, J.J., et al., 1993. Geographical distribution and ecology of the Armillaria species in western Europe. Eur. J. For. Path., 23: 321-341.

[7] Kile, G.A., et al., 1993. Biogeography and pathology of Armillaria. Proc. 8th Int. Conf. Root and Butt Rots (eds. Johansson and Stenlid), Uppsala, Swed. Univ. Agric. Sci., pp: 411-436.

[8] Volk, T.J., Key to the North American Armillaria species: URL: Date: 03.03.14.

[9] Paul, F. Hamlyn. Honey Fungus--Friend or Foe? Published in the October 2001 issue of NWFG Newsletter (ISSN 1465-8054).

[10] Shevchenko, S.V., A.V. Ciljurik, 1986. Lesnaja fitopatologija.--Kiev: Vishha shkola, 384 s.

[11] Ushakov, E.V, 2005. Vvedenie v filosofiju i metodologiju nauki / E.V Ushakov.--M.: Izd-vo "Jekzamen", 528.

Dunayev Alexander Vladimirovich, Kalugina Svetlana Viktorovna, Tokhtar Valeriy Konstantinovich, Dunayeva Elena Nikolaevna, Kukharuk Natalya Stepanovna, Mitryaykina Antonina Mikhailovna, Polshina Marina Aleksandrovna

Belgorod State University, Pobedy St., 85, Belgorod, 308015, Russia

Corresponding Author: Dunayev Alexander Vladimirovich, Belgorod State University, Pobedy St., 85, Belgorod, 308015, Russia

able 1: Description of ecomorphotype in the complex A. mellea
s. l. in Belgorod oakeries.

Ecomorphotype #1                             Ecomorphotype #2
1                                                   2

Ecological group, pathologic role

Saprotroph, in some cases               Saprophyte, in some cases
facultative parasite on weakened         facultative parasite on
trees. Often met on oaks, weakened      weakened and dying trees,
by butt rot invaders (beefsteak            secondary parasite.
fungus Fistulina hepatica
(Schaeff.) With. and sulphur
polypore Laetiporus sulphureus
(Bull.) Murrill).

Confinedness to forest sites and
host plants

Confined to maple-linden and ash      Confined to oak timber stands
oak timber stands in conditions.      with some aspens or cultivated
[D.sub.2]Met mainly on oaks.          oaks in aspen cutover areas in
                                         conditions [D.sub.2-3],
                                       [D.sub.3].   Met on oaks and


Dark brown coming near to black,       Black, penetrating soil with
glossy, densely penetrating top         underground tree remains,
soil, monopodially ramifying on          monopodially ramifying.
roots and under cortex of stressed
trees and stumps.

Fruit bodies

Formed epiphytically on rhizomorphs      Formed epiphytically on
or laid under cortex of stressed      rhizomorphs or endophytically
trees and stumps.                        on subcortial mycelium.

Continuation of table 1

1                                                   2

Fruit bodies' macrocharacters

Cap has little difference colour       Cap of young fruit bodies is
intensity of young and ripe fruit      darker, grey-brown, then it
bodies, it is usually of reddish       lightens to buff-grey with a
hues (meat-red, yellowish red,        darker centre; at first it is
reddish brown); cap is convex         convex, then almost extended,
spherical or campanulate in case of   sometimes with depression and
young bodies and pitching convex        mount in the centre. Cap's
umbrella-shaped in case of ripe         edge is often flexuose and
bodies. Cap's edge preserves white    declinate. Squames are small,
flake-like remains of partial veil.    scarce, cover the whole cap.
Squames of young specimens' caps
are dense and big, over time they
disappear on the periphery of a

Stipe is cylindrical, young fruit      Stipe is cylindrical, thin,
bodies are quite thick, and ripe      sometimes with a thickening at
ones are more or less thin, with a     the bottom; above a ring it
claviform thickening at the bottom;   has a cap's colour, below it--
above a ring it is whitish, below a    it is darker. Stipe's flesh
ring it has a cap's colour or is of       may be mealy, whitish.
darker, browner hues; its bottom
has yellow shade. Stipe preserves
flake-like remains of partial veil,
yellowish on the place of
disappearing ring. Stipe's flesh is
stiff, white or pinkish.

Ring is mealy, web-filmy, with          Ring is less mealy, filmy,
uneven yellowish edge; disappears      with more or less even edge,
fast.                                  greyish-white, may disappear
                                                over time.

Gills of young specimens are           Gills of young specimens are
yellowish-pink, over time they        whitish, over time they darken
darken to rusty brown, with darker    to flesh-brown, sometimes with
spots; adnate or decurrent on to          darker spots; slightly
stipe. Spore print is whitish.         decurring on to stipe. Spore
                                             print is white.

Period and peculiarities of

End of September--beginning of          Second half of September--
November; bears fruit solitarily,      beginning of November; bears
in small groups, rarely--               fruit in small groups and
acervately.                                acervately, rarely--
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Author:Vladimirovich, Dunayev Alexander; Viktorovna, Kalugina Svetlana; Konstantinovich, Tokhtar Valeriy; N
Publication:Advances in Environmental Biology
Article Type:Report
Geographic Code:4EXRU
Date:May 1, 2014
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