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„. “
2 –
99
ANNUAL OF SOFIA UNIVERSITY “ST. KLIMENT OHRIDSKI”
FACULTY OF BIOLOGY
Book 2 – Botany
Volume 99
AEROPHYTIC GREEN ALGAE, EPIMYCOTIC
ON FOMES FOMENTARIUS (L. EX FR.) KICKX.
MAYA P. STOYNEVA1*, BLAGOY A. UZUNOV1 & GEORG GÄRTNER2
1 – Sofi a University “St. Kliment Ohridski”, Faculty of Biology, Department of Botany,
8 bld. Dr. Zankov, BG-1164, Sofi a, Bulgaria; mstoyneva@abv.bg; blagoy_uzunov@abv.bg
2 – Institut für Botanik der Universität, Sternwartestraße 15, A-6020 Innsbruck, Österreich;
georg.gaertner@uibk.ac.at
The paper is dedicated to Prof. D. Temnsikova
on the occasion of her 80th jubilee
Abstract: Four species of green algae were found on the upper surface of Fomes
fomentarius (L. ex Fr.) Kickx. basidiome. Desmococcus vulgaris (represented by both vegetative
cells and aplanosporangia) dominated among them. Trebouxia arboricola (represented by free-
living vegetative cells and autosporangia), and two species of Stichococcus (S. bacillaris, S.
minutus) were the other identified algae. It is proposed to use the term “epimycotic” (from the
greek “epi”- over and “mykes” – fungus) for algae and/or other organisms capable of growing
and developing on the upper surface of fungal fruiting bodies.
Key words: basidiocarp, basidiome, Bulgaria, coccal algae, Danube island, filamentous
algae, fungal host
*corresponding author: M. P. Stoyneva – Sofia University “St. Kliment Ohridski”, Faculty
of Biology, Department of Botany, 8 bld. Dr. Zankov, BG-1164, Sofia, Bulgaria; mstoyneva@
abv.bg
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INTRODUCTION
Aerophytic algae are well known colonists on different substrates as bark,
wood, rocks, buildings, etc. and occur also as epiphytes on living organisms (e.g.
on leaves of trees and shrubs, coniferous needles, lichens, etc. – ETTL & GÄRTNER
1995, 2014). Fruiting bodies of fungi have very rarely been reported to host algae
on their surface and among them only a few species were identified (BURDSALL ET
AL. 1996; ZAVADA & SIMOES 2001). Moreover, it was underlined that the occurrence
of “epiphytes” on Trametes versicolor (L.) Lloyd is common, but not universal
(ZAVADA ET AL. 2004). The recent investigation of an old, intermediate between
bracket- and hoof-like, fruit body of Fomes fomentarius (L. ex Fr.) Kickx., collected
in a floodplain Danube forest, revealed different green algae growing abundantly on
its upper surface. Obviously, the air moisture of the site favors the development of
the aerophytic algae found. For the algae and other organisms capable of growing
and developing on such substrate, the term “epimycotic” is advocated.
MATERIAL AND METHODS
Fomes fomentarius from a Populus sp. trunk was collected in the middle of July
2014, in a floodplain forest at the Bulgarian Danube island Tsibur (=Ibisha). The
island is situated between 716 and 719 river kilometers (Montana district, Bulgaria –
Fig. 1.) and covers area of 0,9 km2. In spite of this small territory, it is very interesting
from nature conservational point of view and contains two protected territories: the
protected area “Ostrov Tsibur” (situated in north-western part of the island with area
of 101,48 ha, declared by State Order RD-292/10.04.2007) and managed reserve
“Ibisha” (situated in the south-eastern part of the island with area of 34,3 ha, declared
by Order RD-394/15.10.1999 of the Bulgarian Ministry of Environment and Waters).
The “Ibisha” reserve is periodically inundated and contains floodplain forest. The
Fomes fruiting body (also basidiocarp, basidiome, basidioma, fruit-body – after
KIRK ET AL. 2008) was collected by Assoc. Prof. Dr. P. MITOV during his work on the
Management Plan of the managed reserve “Ibisha” and on the next day transported to
the Botany Department of Sofia University “St. Kliment Ohridski”.
The basidiome was about 55 cm in diameter and up to 22 cm thick (measured
on the highest part from top to basis) – Figs. 2a-b. The upper surface was tough,
bumpy, hard and woody, mainly greyish. It was covered with many spots – light to
dark-green, rounded or irregular in shape, 3 mm to 3 cm, and even in bigger size
(Figs. 2a-b). Samples from six spots (marked with different coloured mini-flags
and numbers – Fig. 2b) were taken with sterile needles and transferred directly to
slides for investigation in light microscope. Microscopy was done with a Motic
400 microscope (40x and 100x immersion objectives). Photomicrographs were
taken with a Motic Cam 2,0 and processed with software Motic Images Plus 2,0.
Cell walls were stained with Methylene Blue and starch was coloured with Lugol’s
21
solution (ETTL & GÄRTNER 1995, 2014). The taxonomic identification followed
ETTL & GÄRTNER (2014).
Fig. 1. Map of Bulgaria with the location of the managed reserve “Ibisha”, and Fomes
fomentarius, respectively.
Fig. 2a-b: a) Basidiome of Fomes fomen-
tarius with dark-green spots of epimycotic
green algae; b) Locations of sampling
points, marked with small coloured fl ags
and numbers (1–6).
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RESULTS AND DISCUSSION
Different live stages of the most common aerophytic green alga Desmococcus
olivaceus (Pers. ex Ach.) Laundon (Trebouxiophyceae, Prasiolales) were found in
all investigated samples from the upper surface of the basidiome. The alga formed
2–4-celled cuboidal packets with short unbranched filaments of 3–4 cells (Figs.
3a-d, 4a-c). The cells were rounded, relatively compressed in filamentous stages
(Fig. 3a, 4c), with a well-developed, even massive, wall. The parietal chloroplast
(one per cell) with irregularly lobed margin contained a small pyrenoid, covered
with a fine starch sheath (visible when stained with Lugol’s solution). Additionally,
aplanosporangia with thick irregular cell walls, were recorded in one of the samples
(Fig. 3d). Dimensions of vegetative cells in the few-celled filaments varied from 7
to 12 m. D. olivaceus was firstly reported for Bulgaria as a distinct taxon (from
cultures) by STOYNEVA & GÄRTNER (2009), who recorded it from moist rock surfaces
of the tunnel cave “Prohodna and from an old glass piece, found in the entrance of
the same cave. Most probably, it was found earlier in Bulgaria by PETKOFF (1925)
on tree barks in Pirin Mts. and included in the algal flora of VODENICHAROV ET AL.
(1971) under the unclear name Protococcus viridis Agardh, which led to taxonomic
confusions (UZUNOV et al. 2008).
Fig. 3a-f. Epimycotic algae on Fomes fomentarius. 3a-d: Desmococcus olivaceus:
a-c) Vegetative stages of cuboidal cell packets and short fi laments; d) Aplanosporangium of
Desmococcus olivaceus with thick cell wall. 3e-f: Trebouxia arboricola: e) vegetative cells
with nucleus in the sinus of chloroplast; f) autosporangium with 8 autospores of different
size. 3g-h: Stichococcus: g) vegetative cells of St. bacillaris; h) vegetative cells of St.
minutus. Scale bars on the fi gs. – 10 m.
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Trebouxia arboricola Puymaly (Trebouxiophyceae, Trebouxiales) was detected
in two of the surface samples (green and light-blue flags /= sites 3 and 6 on Fig. 2b).
It was non-lichenized, free-living and appeared in both stages of vegetative cells and
autosporangia (Figs. 3e-f, 4c–d). The vegetative cells possessed all typical diagnostic
features of Trebouxia aboricola: they were globular, sometimes slightly ellipsoidal,
with a parietal massive, lobed to incised chloroplast with a naked pyrenoid, which
lacks a distinct starch sheath. The nucleus was eccentric in the cell lumen, situated
in an expressed sinus of the chloroplast (Fig. 3e, 4e). The cells were 13–15 m in
diameter and coincided with the authentic strain (or “type culture”) investigated
by GÄRTNER (1975). The observed autosporangia contained mainly 8 autospores
of slightly different size (Fig. 4f). T. arboricola was reported for Bulgaria by
VODENICHAROV ET AL. (1971) as found on tree bark in Rodopi Mts, without mentioning
of cultures. Later on, it was collected in a free-living stage and cultivated from granite
stone monuments (GÄRTNER & STOYNEVA 2003), from the walls of the tunnel cave
“Prohodna” (STOYNEVA & GÄRTNER 2009) and from the surface of sandstones of the
rock phenomenon “Belogradshishki Skali” (MANCHEVA 2013).
Two species of the very common aerophytic green filamentous genus
Stichococcus Nägeli (Trebouxiophyceae, Prasiolales) were found in one of the
studied samples (green flag/=site 3 on Fig. 2b): S. bacillaris Nägeli and S. minutus
Grintzesco & Péterfi. Both algae differ in size and morphology of chloroplasts in
their vegetative cells (HINDÁK 1996). The cells of S. bacillaris were ± cylindrical,
3m broad and 7 (10) m long, each with a median inserted chloroplast (Fig. 3g,
4d). By contrast, the vegetative cells of S. minutus were more rounded, 2–3m
broad and 4m long, with a polar chloroplast within the cell lumen (Fig. 3h, 4d).
Stichococcus bacillaris was recorded in many sites of Bulgaria (VODENICHAROV
ET AL. 1971; UZUNOV ET AL. 2007, 2008), whereas S. minutus was found only by
UZUNOV (2009) in soils of Pirin Mts.
The recent findings are the first documented observations of Desmococcus olivaceus,
Trebouxia arboricola, Stichococcus bacillaris and S. minutus as “epiphytic” algae on
a basidiome surface in Bulgaria. According to our knowledege, this is also their first
documentation on Fomes fomentarius, whereas “Characium sp. and Coccomyxa sp.”
were found on Bridgeoporus nobilissimus (W.B. Cooke) Volk, Burdsall & Ammirati
(BURDSALL et al. 1996), “Hormidium sp., Stichococcus bacillaris, Chlorococcum sp.,
and Trebouxia sp.” were determined on Trametes versicolor and it was suggested that
the basidiocarps of T. versicolor have the potential to be lichenized (ZAVADA et SIMOES
2001). Later on, ZAVADA et al. (2004) proved the capacity for T. versicolor to exploit
algae as a carbon source. We believe that many algologists, mycologists and ecologists
know the possibility algae (and particularly green algae) to develop on the surface of
different fungi. However, it is obvious that this so-well-known knowledge remained
very less documented, at least in the literature available and checked for this study. In
any case, we found illogical to continue to use the term “epiphytes” for the organisms
from such surfaces, since long-ago it is clear that fungi do not belong to the Plant
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Kingdom. Therefore, we plead to use for algae and/or other organisms growing on the
upper surface of fungal fruiting bodies, the term “epimycotic” (from the greek “epi”-
over and “mykes” – fungus), which occasionally and without discussions has been used
(e.g. REYNOLDS 1978; REDBERG et al. 2003).
Fig. 4a-f. Photomicrographs of epimycotic algae on Fomes fomentarius.
4a-c: Desmococcus olivaceus: a) Single cells in binary division; b) Cuboidal packages of
vegetative cells; c) Short fi laments. 4d: Stichococcus: vegetative cells of S. bacillaris (arrow
heads) and of S. minutus (arrows). 4e: Trebouxia arboricola – vegetative cells. Scale bars
on the fi gs. – 10 m.
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REFERENCES
BURDSALL H. H., VOLK T. J. & J. F. AMMIRATI JR. 1996. Bridgeoporus, a new genus to accom-
modate Oxyporus nobilissimus (Basidiomycota, Polyporaceae). – Mycotaxon 60: 387–395.
ETTL H. & GÄRTNER G. 1995. Syllabus der Boden-, Luft-und Flechtenalgen, Fischer, Stuttgart,
Jena, New York, 721 pp.
ETTL H. & GÄRTNER G. 2014. Syllabus der Boden-, Luft-und Flechtenalgen. 2. Aufl ., Springer,
Berlin, Heidelberg, 773 pp.
GÄRTNER G. 1975. Die Gattung Trebouxia Puymaly. – Algol. Stud. 41: 495–548.
GÄRTNER G. & STOYNEVA M. P. 2003. First Study of Aerophytic Cryptogams on Monuments in
Bulgaria.- Ber. nat.- med. Verein Innsbruck 90: 73–82.
HINDÁK F. 1996. Klú na urovanie nerozkonárených vláknitých zelených rias (Ulotrichineae,
Ulotrichales, Chlorophyceae) [Key to unbranched fi lamentous green algae (Ulotrichineae,
Ulotrichales, Chlorophyceae)]. – Bull. Slov. Bot. Spol., Bratislava, Suppl. 1: 1–77 (In
Slovakian).
KIRK P. M., CANNON P. F., MINTER D. W. & STALPERS J. A. (eds.) 2008. Ainsworth and Bisby’s
Dictionary of the Fungi. Tenth Edition prepared by CABI Europe – UK, 784 pp.
MANCHEVA A. 2013. Aerophytic algae from the rock phenomenon and nature monument
Belogradchishki Skali. PhD Thesis, Sofi a Univrsity, Fac. Biology, 191 pp. (In Bulgarian).
PETKOFF S. 1925. La fl ore algologique du mont Pirin-planina. – Sbornik na Bulgarskata
Akademiya na Naukite 20: 1–128 (In Bulgarian).
REDBERG G. L., HIBBERT D. S., AMMIRATI JR J. F. & RODRIGUEZ R. J. 2003. Phylogeny and genetic
diversity of Bridgeoporus nobilissimus inferred using mitochondrial and nuclear rDNA
sequences. – Mycologia 95 (5): 836–845.
REYNOLDS D. R. 1978. Foliculous Ascomycetes 1: The Capnodiaceous genus Scorias,
Reproduction. – Contributions in Science, Natural History Museum of Los Angeles 288:
1–15.
STOYNEVA M. P. & GÄRTNER G. 2009. Remarkable and newly recorded aeroterrestric
Cyanoprokaryotes and algae in Bulgaria. – In: IVANOVA D. (ed.), Plant, fungal and Habitat
diversity investigation and conservation. Proceedings of IV Balkan Botanical Congress,
Sofi a, 20–26 June 2006. Institute of Botany, Sofi a, 122–127.
UZUNOV B. A. 2009. Aeroterrestrial algae from Pirin Mountain (Bulgaria). PhD Thesis, Innsbruck
University, 182 pp.
UZUNOV B. A., STOYNEVA M. P. & GÄRTNER G. 2007. Review of the studies on aero-terrestrial
cyanoprokaryotes and algae in Bulgaria with a Checklist of recorded species. I. – Phytol.
Balcan. 13 (1): 65–73.
UZUNOV B. A., STOYNEVA M. P. & GÄRTNER G. 2008. Review of the studies on aero-terrestrial
cyanoprokaryotes and algae in Bulgaria with a Checklist of the recorded species. II. –
Phytol. Balcan. 14: 11–18.
VODENICHAROV D., DRAGANOV S. J. & TEMNISKOVA D. 1971. Flora of Bulgaria. Algae. Izd.
Narodna Prosveta, Sofi a, 642 pp. (In Bulgarian).
ZAVADA M. S. & SIMOES P. 2001. The possible demi-lichenization of the basidiocarps of Trametes
versicolor (L.: Fries) Pilat (Polyporaceae). – Northeastern Naturalist 8 (1): 101–112.
ZAVADA M. S., DIMICHELE L. & TOTH C. R. 2004. The demi-lichenization of Trametes versicolor
(L.: Fries) Pilat (Polyporaceae): The transfer of fi xed 14CO2 to T. versicolor. – Northeastern
Naturalist 11 (1): 33–40.
Accepted 26 November 2014
