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Pholiota gallica (Fungi, Strophariaceae): first Balkan collection of a little-known dark-spored agaric

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Assyov, B.: Pholiota gallica (Fungi, Strophariaceae), first Balkan collection of a little-known dark-spored agaric.-Borziana 3: 027-032. 2022-ISSN: 2724-5020 online. The author reports the first Balkan collection of the scarcely featured in the mycological literature Pholiota gallica based on material collected in Bulgaria. Description of the macro-morphology and microscopic features of the studied specimens is included, supplemented with illustrations.
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Boris Assyov
Pholiota gallica (Fungi, Strophariaceae): first Balkan collection of a little-
known dark-spored agaric
Abstract
Assyov, B.: Pholiota gallica (Fungi, Strophariaceae), first Balkan collection of a little-known
dark-spored agaric. — Borziana 3: 027-032. 2022 — ISSN: 2724-5020 online.
The author reports the first Balkan collection of the scarcely featured in the mycological liter-
ature Pholiota gallica based on material collected in Bulgaria. Description of the macro-mor-
phology and microscopic features of the studied specimens is included, supplemented with
illustrations.
Key words: Balkan mycota, biogeography, Pholiota lubrica var. obscura, Strophariaceae,
taxonomy.
Introduction
The genus Pholiota (Fr.) P. Kumm. is one of the genera of the family Strophariaceae
Singer & A.H. Sm., comprising saprobic species, mostly occurring on woody substrates.
The genus attracted the attention of mycologists in Europe for a long time and has been
subject of several monographic treatments (Jacobsson 1991, 1992, 2008; Noordeloos
1999, 2011; Holec 2001) and new species have been recognized (Holec & Niemelä 2000;
Holec & al. 2014). Among these, the name Pholiota gallica Holec & M. Kolařík was
recently proposed to accommodate P. lubrica var. obscura Bon & Chevassut, when elevat-
ed to species rank (Holec & Kolařík 2014). It was later inferred that P. highlandensis
(Peck) Singer var. citrinosquamulosa Maire ex Bidaud & Borgarino is a synonym (Holec
& al. 2016), confirming the variability of the species. Nevertheless, P. gallica still remains
one of the least known species of the genus in Europe. In 2021 the author had the oppor-
tunity to observe and collect P. gallica in Bulgaria. Description and illustrations of the
taxon are reported here.
Materials and Methods
The basidiomata were photographed in situ and the relevant features were noted. The
voucher specimen is deposited in air-dried state in the Mycological Collection of the
Borziana 3: 27-32
https://doi.org/10.7320/Borziana.003.027
Version of Record published online on 19 March 2022
Article
Institute of Biodiversity and Ecosystem Research (SOMF). The microscopic features were
observed under an AmScope T360B light microscope, equipped with AmScope MU900
digital camera. The study of the microscopic characters was performed on preparations
from dried specimens after rehydration with 5% KOH. Congo red in ammonia was added
to the preparations except for the observation of spores, which were measured solely in
KOH solution. Melzer’s reagent was employed in addition to assess the iodine reactions.
The assessment of the size of the microscopic features was performed on pre-calibrated
digital photographs with the aid of Piximètre ver. 5.10 (©A. Henriot & J.-L. Cheype). The
spore measurements are presented below by the minimum and maximum values of length,
width and quotient (Q), followed by the average values for spore length (Lav), width (Wav)
and quotient (Qav); the spore data refer to sample of 30 basidiospores. For the remaining
microscopic features minimum and maximum values are included. The colour terms refer
to the ‘Flora of British Fungi Colour Identification Chart’ (Royal Botanic Garden
Edinburgh 1969) followed in parenthesis by a colour code beginning with the abbreviation
”BFF”. The remaining colour terms are vernacular names rather than chart entries. The
colours in the description of the microscopic structures refer to slides in KOH.
Results
Pholiota gallica Holec & M. Kolařík, Mycotaxon 127: 165 (2014); ≡ Pholiota lubrica
var. obscura Bon & Chevassut, Docums Mycol. 19(fasc. 75): 44 (1989); = Pholiota high-
landensis var. citrinosquamulosa Maire ex Bidaud & Borgarino, Bull. Sem. Féd. Assoc.
Mycol. Médit. 30: 6 (2006). (Figs 1, 2).
Pileus up to 5 cm broad, convex or convex-applanate, sometimes slightly irregular,
almost smooth, radially fibrillose to finely rugulose, with somewhat greasy shine and
slightly sticky, rusty tawny (BFF14) to brick-red (BFF15), sometimes discolouring in
places to cinnamon (BFF10), along the margin yellowish buff (BFF52) to straw (BFF50);
pileal edge appendiculate and usually with brownish remnants of veil. Stipe up to 1 cm
wide, cylindrical, sometimes curved and often widened at the base, buff (BFF52), down-
wards brick (BFF15) to rusty tawny (BFF14), in the upper part with brownish fibrillose
annular zone and with straw to yellowish floccose girdles below, in section in the upper
half hollow; mycelial strands off-white to lemon yellow. Lamellae more or less crowded,
narrowly adnate to adnexed, pale buff (BFF52) to pale vinaceous buff (BFF31), occasion-
ally rusty spotted, edge concolorous, often uneven; lamellulae present, 1–3 between lamel-
lae. Context whitish in the pileus and upper stipe, downwards yellowish, brownish towards
the stipe base. Odour and taste inconspicuous. Exsiccata in UV 365 nm produce yellowish
green fluorescence, located at lamellar edges. Basidiospores 6.3–7.5 × 4–4.8 µm, Q = 1.4–
1.7; Lav = 6.9, Wav = 4.5 µm, Qav = 1.5, ellipsoid, ellipsoid-ovoid to ovoid, some of them
flattened on adaxial side, yellow-brown, with a distinct brown wall up to 0.7 µm thick and
a germ pore. Basidia predominantly 4-spored, occasionally 2-spored, 18.3–23.9 × 5.5–7.2
μm, cylindrical to narrowly clavate; sterigmata 2–2.5 μm long. Leptocystidia on lamellar
edge and faces, partly or entirely with distinctive yellowish, non-refractive content.
Cheilocystidia 30.8–49.9 × 9.6–16.4 µm, fusiform, utriform or lageniform. Pleurocystidia
45.7–68.3 × 8.2–16.2 µm, lageniform, narrowly lageniform or occasionally clavate.
28 Assyov: Pholiota gallica (Fungi, Strophariaceae): first Balkan collection...
Chrysocystidia absent. Lamellar trama of 5.3–15.8 µm wide, cylindrical, septate, hyaline
hyphae. Pileipellis an ixotrichodermium, 3-layered: outer layer composed of 1.5–4.5 µm
wide, encrusted by yellow brown pigment, loosely to densely arranged, septate and
branching hyphae; medium layer of 2–5 µm broad, encrusted by yellow brown pigment
hyphae; inner layer of somewhat inflated, 3.9–9.7 µm wide, sub-parallel, septate hyphae
with reddish brown membrane pigment; pileocystidia absent. Stipitipellis a cutis-like, of
running parallel to stipe axis, 2–5.7 µm broad, septate hyphae with yellowish to brownish
yellow encrusting pigment; caulocystidia not seen; stipe flocci made of densely interwov-
en, 2.5–7.6 µm broad, septate hyphae with yellow outline and encrusting pigments. No
amyloid or dextrinoid microstructures detected. Clamp connections present in all tissues.
Specimen examined. Bulgaria, Blagoevgrad Province, Strumyani Municipality,
between Mikrevo and Kamenitsa villages, 41°38’12.4”N, 23°10’27.2”E, ca 190 m, in
grasslands close to Quercus coccifera L, on non-calcareous, sandy soils, 19 Dec 2021, leg.
B. Assyov (SOMF 30431).
Discussion
The new collection of P. gallica matches the morphological description of the type spec-
imen and other findings of the species as reported by Holec & Kolařík (2014) and Holec
& al. (2016). Basidiomata in the Bulgarian specimen feature darker colours in comparison
Borziana 3 — 2022 29
Fig. 1. Macromorphological features of Pholiota gallica. Scale bar = 1 cm.
with the ones illustrated in Holec & al. (2016) – rusty tawny to brick versus rusty, sienna
to cinnamon with somewhat salmon tint in places. The zonate appearance of the pilei,
found in the mentioned French collection, is absent. However, from the original descrip-
tion of P. lubrica var. obscura (Bon & Chevassut 1989) it is evident that at least in some
collections pilei may be not zonate and darker. Besides, the stipes in the Bulgarian collec-
tion develop brownish tints in the lower parts, which seem to be absent from the studied
specimens in Holec & al. (2016). Microscopically the pileipellis is somewhat distinct, in
some layers containing reddish brown rather than yellowish brown tinge and this seems to
be consistent with the mentioned above darker pileal colours. As far as the remaining
microscopic features are concerned, their morphology and dimensions seem to adhere well
to the data in Holec & Kolařík (2014) and Holec & al. (2016). The presence of two-spored
basidia is noteworthy, while in the previously known specimens only four-spored were
observed (Holec & Kolařík 2014; Holec & al. 2016). Notably, the two-spored basidia seem
to more often have a cylindrical outline than four-spored ones. It was noted by Holec
(2001) that two-spored basidia are present in almost all species of Pholiota. As the vari-
ability of the P. gallica is apparently little-known for the moment, the documented varia-
tions are perceived here to be within the expected range.
The closest European ally of P. gallica was shown to be P. chocenensis Holec & Kolařík
(Holec & Kolařík 2014; Holec & al. 2014, 2016). It is a non-pyrophilous taxon, similarly
to P. gallica lacking caulocystidia (Holec & al. 2014). Macrosopically P. chocenensis
seems to differ by the colour of floccose remnants on stipe, which are yellow rusty to rusty
orange (Holec & al. 2014). In addition, this species was described as having two-layered
pileipellis (Holec & al. 2014).
30 Assyov: Pholiota gallica (Fungi, Strophariaceae): first Balkan collection...
Fig. 2. Microscopic characters of Pholiota gallica: a. basidiospores, b. basidia, c. cheilocystidia, d.
pleurocystidia, e. pileipellis hyphae (encrusting pigments shown partly). Scale bars = 10 μm.
Among the known species, the pyrophylous Pholiota brunnescens A.H. Sm. & Hesler
seems to be similar to the species presented here. Originally described from North
America, it has been shown recently to have intercontinental distribution occurring also in
Central and Eastern Asia, but its presence is so far not confirmed in Europe (Smith &
Hesler 1968; Matheny & al. 2018; Tian & Matheny 2021). It seems to differ by microscop-
ic characters and the distinction of P. gallica should not be difficult. Smith & Hesler (1968)
and Matheny & al. (2018) outlined as the most prominent character of P. brunnescens the
large caulocystidia, while P. gallica does not have caulocystidia (Holec & Kolařík 2014;
Holec & al. 2016). Among the distinctive features of P. brunnescens Smith & Hesler
(1968) to be considered is the presence of numerous forked pleurocystidia, which are not
mentioned in the more recent description of Matheny & al. (2018). This character thus
needs more observations. The description in Smith & Hesler (1968) also hints at possible
subtle differences in the spore dimensions, the width in particular – 4.5 μm. Holec &
Kolařík (2014) found broader spores in the holotype of Pholiota gallica (up to 5.5 μm),
although in the present specimens spore width does not exceed 4.8 µm. Subsequent assess-
ments of additional specimens by Matheny & al. (2018) and Holec & al. (2016) however
have shown that the spore dimensions in the two species overlap considerably and are thus
unlikely to be a useful character for separating of the two entities.
Pholiota castanea A. H. Sm. & Hessler is another pyrophilous North American species,
phylogenetically related to the cluster of P. gallica (Matheny & al. 2018). Apart of its habi-
tat it seems to differ from P. gallica by the more delicate stipe, lacking yellow flakes,
according to the descriptions of Smith & Hessler (1968) and Matheny & al. (2018). The
American species has predominantly cylindrical or subcylindrical caulocystidia and differ-
ent architecture of the pileipellis (Matheny & al. 2018).
The distribution of Pholiota gallica is still fragmentary known. However, it is apparent-
ly a taxon with a southern distribution, found so far both in Mediterranean European coun-
tries and North Africa. Collections of this species have so far been reported from France,
Algeria, Morocco and Cyprus (Holec & Kolařík 2014; Holec & al. 2016, Loizides 2016,
2021). This paper expands its distribution to the Balkan Peninsula and reports the first
finding of the species in Bulgaria. The Bulgarian collection confirms the occurrence of P.
gallica on non-burnt ground in association with Mediterranean vegetation (Holec &
Kolařík 2014; Holec & al. 2016; Loizides 2016, 2021), in the present case dry grasslands
in close proximity to evergreen oaks.
Acknowledgements
This work was supported by project ‘Phylogeny, distribution and sustainable use of fungi’. The
author extends his thanks to Dr. Pierre-Arthur Moreau and Mr. Michael Loizides for drawing atten-
tion to the presented here collection. The critical reading and the useful suggestions of M. Loizides
and the anonymous reviewers are gratefully acknowledged.
References
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Address of the author:
Boris Assyov,
Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences,
2 Gagarin Str., 1113 Sofia, Bulgaria. Email: contact@boletales.com, Orcid ID: 0000-
0002-7365-2443
32 Assyov: Pholiota gallica (Fungi, Strophariaceae): first Balkan collection...
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Pholiota highlandensis var. citrinosquamulosa Maire ex Bidaud & Borgarino is a Mediterranean fungus growing in connection above all with Pinus halepensis and/or Quercus ilex, either on soil or on their wood. Its distinguishing characters are stout basidiomata, red-brown pileus with paler, lemon yellow margin, distinct lemon yellow scales on stipe, ellipsoid-ovoid spores and fusiform to lageniform cheilo- and pleurocystidia. Morphological and DNA study of its type and other collections showed that it does not belong to P. highlandensis but is conspecific with Pholiota gallica Holec & Kolařík. This species bears a recently published replacement name for Pholiota lubrica var. obscura, a taxon described by Bon & Chevassut from the same habitats as P. h. var. citrinosquamulosa. Basic data on taxonomy, nomenclature and ecology of P. gallica, the correct name for all the taxa mentioned, are summarized. A key for identification of P. gallica and similar taxa is proposed.