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Macrofungi on fallen oak trunks in the Białowieża
Virgin Forest – ecological role of trunk parameters
and surrounding vegetation
JAN HOLEC1,JAN BĚŤÁK2,DANIEL DVOŘÁK3,MARTIN KŘÍŽ1,MIRIAM KUCHAŘÍKOVÁ1,
RENATA KRZYŚCIAK-KOSIŃSKA 4,TOMÁŠ KUČERA5
1National Museum, Mycological Department, Cirkusová 1740, CZ-193 00 Praha 9, Czech Republic;
jan_holec@nm.cz
2The Silva Tarouca Research Institute for Landscape and Ornamental Gardening, Lidická 25/27,
CZ-602 00 Brno, Czech Republic; janek.betak@gmail.com
3Masaryk University, Department of Botany and Zoology, Kotlářská 2, CZ-611 37 Brno,
Czech Republic; dvorak@sci.muni.cz
4Polish Academy of Sciences, Institute of Nature Conservation, al. A. Mickiewicza 33,
PL-31-120 Kraków, Poland; renata@kosinscy.pl
5University of South Bohemia, Faculty of Science, Branišovská 1645/31a,
CZ-370 05 České Budějovice, Czech Republic; kucert00@prf.jcu.cz
Holec J., Běťák J., Dvořák D., Kříž M., Kuchaříková M., Krzyściak-Kosińska R.,
Kučera T. (2019): Macrofungi on fallen oak trunks in the Białowieża Virgin Forest
– ecological role of trunk parameters and surrounding vegetation. – Czech Mycol.
71(1): 65–89.
All groups of macrofungi were recorded on 32 large fallen trunks of pedunculate oak (Quercus
robur) in various decay stages in the strictly protected zone of Białowieża National Park, Poland. The
total number of species was 187 with 4–38 species per trunk. The mycobiota of individual trunks was
unique, consisting of a variable set of several frequent species, a high number of infrequent to rare
ones, and a considerable proportion of mycorrhizal fungi and species preferring conifer wood. Rela-
tions between trunk parameters, surrounding vegetation and fungal occurrences were analysed us-
ing multivariate statistical methods. The number of fungal species per trunk was significantly corre-
lated with trunk orientation, which reflects the heat load via forest canopy gap, trunk size parame-
ters, percentage of bark cover and contact with the soil. The species-richest trunks were those cov-
ered by bark, of larger volume (thick, long), not exposed to heat from afternoon sun, but, simulta-
neously, with lower canopy cover. Orientation (azimuth) of the fallen trunks proved to be significant
also for the fungal species composition of a particular trunk, which also reflected trunk size charac-
teristics, its moss/bark cover and contact with the soil. Presence of some dominants (Ganoderma
applanatum, Mycena inclinata, Kretzschmaria deusta,Xylobolus frustulatus) had a significant ef-
fect on fungal community composition. Some herbs requiring nutrient-rich soils occurred in the vi-
cinity of trunks with a larger contact area with the soil and in later stages of decay. The process of oak
trunk decay in relation to fungi and surrounding vegetation is outlined.
Key words: lignicolous fungi, Quercus robur, Europe, fungal diversity, ecology, wood decay, trunk
orientation, forest canopy gaps, heat load.
Article history: received 11 March 2019, revised 20 May 2019, accepted 24 May 2019, published on-
line 18 June 2019 (including Electronic supplement).
DOI: https://doi.org/10.33585/cmy.71105
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CZECH MYCOLOGY 71(1): 65–89, JUNE 18, 2019 (ONLINE VERSION, ISSN 1805-1421)
Holec J., Běťák J., Dvořák D., Kříž M., Kuchaříková M., Krzyściak-Kosińska R.,
Kučera T. (2019): Makromycety na padlých kmenech dubu v Bělověžském pra-
lese – ekologický význam vlastností kmenů a okolní vegetace. – Czech Mycol.
71(1): 65–89.
Na 32 velkých padlých kmenech dubu letního (Quercus robur) v různých stadiích tlení, ležících
v přísně chráněné zóně Bělověžského národního parku, byly zaznamenány všechny skupiny makro-
mycetů. Celkem bylo nalezeno 187 druhů, na jednotlivých kmenech 4–38 druhů. Mykobiota každého
kmenu byla unikátní a sestávala z několika hojných druhů, velkého počtu nehojných až vzácných
druhů a nezanedbatelného podílu mykorhizních hub a druhů jinak preferujících dřevo jehličnanů.
Vztahy mezi vlastnostmi kmenů, okolní vegetací a výskytem hub byly analyzovány pomocí mnoho-
rozměrných statistických metod. Počet druhů na kmenu byl pozitivně korelován s velikostními para-
metry kmenu, stupněm jeho pokrytí borkou a negativně s kontaktem s půdou a jeho jihozápadní ori-
entací, která zároveň určovala oslunění skrz mezeru v porostu. Druhově nejbohatší byly kmeny s vel-
kým zakorněním, velkým objemem (tlusté, dlouhé), nevystavené odpolednímu slunečnímu záření,
ale zároveň pod nižším zápojem porostu. Orientace kmenů byla významná i pro druhové složení hub,
které bylo ovlivněno velikostí kmenu, stupněm jeho pokrytí borkou a mechem a procenty kontaktu
kmene s půdou. Přítomnost některých dominantních hub (Ganoderma applanatum, Mycena incli-
nata, Kretzschmaria deusta,Xylobolus frustulatus) měla průkazný efekt na složení společenstva
hub na daném kmenu. V okolí kmenů, které měly velký kontakt s půdou a byly v pokročilejších
stadiích tlení, se vyskytovaly častěji byliny vyžadující bohatší půdy. Byl popsán obecný proces
rozkladu padlých kmenů dubů za součinnosti hub a okolní vegetace.
INTRODUCTION
Oak (Quercus) is a widely distributed genus of trees occurring in many forest
associations around the world. Both living and dead oaks represent an important
source of nutrients and energy for numerous consumers, symbionts and de-
composers, above all animals and fungi. Fungal decomposers play a very impor-
tant role in forest ecosystems (Boddy 2001, Stokland et al. 2012). The process of
wood decomposition is controlled by complex mechanisms like priority effects,
assembly histories, facilitation, and competition between various fungal species
(Ottosson et al. 2014, Hoppe et al. 2016, van der Wal et al. 2016, Hiscox et al.
2018).
In temperate regions of Europe, pedunculate oak (Quercus robur L.) is domi-
nant especially in lowlands and hilly areas (Ellenberg 2009). Wood-inhabiting
fungi of oak-dominated forests are treated in numerous descriptive works pub-
lishedinthe20
th century, summarised by e.g. Kreisel et al. (1985). Runge (1980)
formally classified fungal communities on wood of Central European trees in-
cluding oak. Boddy & Rayner (1983, 1984) and Butin & Kowalski (1983) studied
fungi inhabiting oak twigs and Sieber et al. (1995) fungi on stem and twig lesions
of Quercus robur. Fungi typical of natural oak woods in Germany were listed by
Blaschke et al. (2009). Succession of selected macromycetes on decaying trunks
66
CZECH MYCOLOGY 71(1): 65–89, JUNE 18, 2019 (ONLINE VERSION, ISSN 1805-1421)
was studied by Runge (1975) and Lindhe et al. (2004). Diversity of macrofungi in
Irish oak forests was recently described and evaluated with multivariate meth-
ods by O’Hanlon (2011) and O’Hanlon & Harrington (2012). Parfitt et al. (2010)
showed that wood-decay fungi are latently present in functional xylem of
branches and trunks of a wide range of trees including Quercus robur. The pro-
cess of oak wood decay and the role of fungi was recently elaborated by van der
Wal et al. (2015) using 454 pyrosequencing and enzyme assays.
Concerning autecology, the spatial distribution of more conspicuous species
on oak trees was described by Sunhede & Vasiliauskas (1996). Oak polypores
were elaborated by Vasiliauskas et al. (2003). Several studies describe thoroughly
ecological requirements of some oak fungi, e.g. Phellinus robustus (Sunhede &
Vasiliauskas 2002), Inocutis dryophila (Sunhede & Vasiliauskas 2003), Piptoporus
quercinus (Boddy et al. 2004), Stereum hirsutum, Chondrostereum purpureum,
Stereum rugosum and Xylobolus frustulatus (Mirić & Stefanović 2018).
Case studies focusing directly on diversity and ecology of fungi on wood of
Quercus robur are infrequent (Nordén et al. 2004, Irše˙naite˙ & Kutorga 2006,
2007). Data published from South Europe (Bernicchia et al. 2008: Italy) and the
USA (Schmit et al. 1999: Indiana; Rubino & McCarthy 2003: Ohio) are less rele-
vant as they originate from other Quercus species and different environmental
conditions. In this situation, we decided to focus on macrofungi inhabiting thick
fallen trunks of Quercus robur in Białowieża National Park in Poland. The local-
ity represents one of the largest and best-preserved lowland forests in Europe,
where huge oaks up to 400 years old are still present (Faliński 1986). Our focus
on larger trunks was based on the fact that large old trees play unique and diverse
ecological roles (Lindenmayer et al. 2012) and their mycobiota has proved to be
richer in comparison with smaller ones (Lindhe et al. 2004, Irše˙naite˙&Kutorga
2007). Simultaneously, the Białowieża Virgin Forest is a fungal diversity hotspot
with unusually rich mycobiota containing numerous rare fungi and species pre-
ferring old-growth forests (for recent summaries, see Karasiński et al. 2009, 2010,
Karasiński & Wołkowycki 2015, Karasiński 2016). For all these reasons, it is an
ideal place for a case study on the ecology of fungi on decaying oak wood. Our
aim was to reveal trunk and habitat factors influencing diversity and ecology of
macrofungi on decaying oak trunks.
MATERIAL AND METHODS
A b b r e v i a t i o n s. AIC: Akaike Information Criterion values; BNP: Białowieża
National Park; BW1–BW32: codes of studied oak trunks; CCA: canonical corre-
spondence analysis; CoCA: co-correspondence analysis; CWD: coarse woody de-
bris; DCA: detrended correspondence analysis; DBH: diameter at breast height;
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HOLEC J. ET AL.: MACROFUNGI ON FALLEN OAK TRUNKS IN THE BIAŁOWIEŻA VIRGIN FOREST
DD: Daniel Dvořák; E: east; E2: canopy of shrubs and young trees up to a height of
5m;E
3: canopy of mature trees; E32:totalE
2and E3canopy; FA: folded aspect of
fallen trunk azimuth; Fspec: number of fungal species on particular trunk stud-
ied; GAM: generalised additive model; GLM: generalised linear model; GPS:
global positioning system; HL: heat load (folded SW aspect of open gap); JB: Jan
Běťák; JH: Jan Holec; MCPT: Monte Carlo permutation test; MK: Martin Kříž;
MKu: Miriam Kuchaříková; N: north; OTU: operational taxonomic unit; PCA: prin-
ciple component analysis; S: south; TK: Tomáš Kučera; W: west; I, II, III, IV (Latin
numerals): particular decay stages of studied trunks.
S t u d y a r e a. Northeastern Poland, Podlaskie Voivodeship, east of the town
of Hajnówka, Białowieża National Park (Białowieski Park Narodowy), strictly
protected zone of the BNP (Fig. 1). Basic environmental data (Faliński 1986): ele-
vation 147–172 m a.s.l., soils acidic to neutral, developed on Quaternary glacial
deposits with network of rivers and streams, ground water at a depth of 1–4 m,
continental climate, mean annual air temperature 6.8 °C (January: –4.7 °C, July:
+17.8 °C, absolute amplitude: –38.7 °C to +34.5 °C), mean annual precipitation
641 mm (extremes 426–940 mm). In the period 1986–2007 the mean annual air
temperature rose to 7.1 °C (January –3.0 °C, July +19.3 °C, absolute amplitude:
–34.6 °C to +34.6 °C), mean annual precipitation 606 mm (Malzahn et al. 2009).
Data published by the Institute of Meteorology and Water Management show fur-
ther changes in mean annual air temperatures and precipitation. In the years
2008–2016 the mean air temperature was 7.7 °C (January –4.0 °C, July +19.1 °C,
absolute amplitude: –36.2 °C to +34.8 °C) and the mean annual precipitation was
708 mm. Even though the last decade seems to show a higher precipitation than
the previous ones, the year 2015 was exceptionally dry with a total precipitation
of only 511 mm. The precipitation in 2016 was much higher mainly due to the high
precipitation in winter and early spring as well as a very wet beginning of July.
Unfortunately, the time prior to our research was much drier than average, Sep-
tember in particular (Electronic supplement O).
Vegetation of the BNP (Faliński 1986) is represented by a lowland hemiboreal
virgin forest highly diverse in flora. Tree dominants are Carpinus betulus,
Quercus robur,Tilia cordata,Fraxinus excelsior and Picea abies (Fagus sylvatica
is completely absent), mixed with less frequent species like Acer platanoides,
Ulmus spp., Pinus sylvestris,Alnus glutinosa,Populus tremula,Salix spp. and
Betula spp. Some tree individuals reach a remarkable size and age. The vegeta-
tion mosaic is formed by mesophilous to thermophilous deciduous forests,
mesotrophic, oligotrophic and bog coniferous forests, and deciduous bog and
floodplain forests and bush. The current deciduous vegetation is considerably
homogenised. Kwiatkowska et al. (1997) documented the expansion of Carpinus
betulus as the main cause of the decline of heliophilous species. The vegetation
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CZECH MYCOLOGY 71(1): 65–89, JUNE 18, 2019 (ONLINE VERSION, ISSN 1805-1421)
surrounding all studied trunks is represented by the Tilio-Carpinetum asso-
ciation. Due to different nutrient and soil moisture conditions, the herb layer
varies between its subassociations typicum,stachyetosum,andcaricetosum
(Kwiatkowski & Gajko 2009).
S t u d i e d o a k t r u n k s. The field work was carried out in September 12–16,
2016. The trunks were searched for in the oldest BNP forest stands with a high
percentage of oak. We selected 32 fallen trunks of Quercus robur (Figs. 1, 2) of
larger diameters (60–130 cm at breast height). Their decay stage was estimated in
accordance with the scale defined by Heilmann-Clausen (2001). Its key charac-
ters are given below (shortened):
1 – fallen trunks without visible signs of decay, wood hard, bark intact;
2 – trunks with minor signs of decay, wood still rather hard, bark starting to break up;
3 – trunks with moderate signs od decay, surface wood distinctly softened, bark partly lost;
4 – trunks with strong signs od decay but still with ± original shape, surface wood strongly decayed,
bark lost in most places;
5 – trunks rotten to almost humified, wood very strongly decayed, either to a very soft crumbly sub-
stance or being flaky and fragile.
However, this scale will need a revision in the case of pedunculate oak. Ad-
vanced core rot, usually present at the time of tree death, the highly resistant oak
wood and the large amount of bark accumulating along lying trunks often create
combinations of microhabitats not common in the decomposition of other tree
species. It was difficult to classify some trunks into the abovementioned catego-
ries. Moreover, freshly fallen trunks (stage 1) as well as strongly decayed ones
(stage 5) were rare. Consequently, trunks in stages 2 and 3 prevail in our set of
trunks (Fig. 3) and those in stage 5 are absent (another reason for their absence
from our dataset was the fact that strongly decayed trunks were hard to distin-
guish from similarly decayed trunks of other tree species).
Trunk parameters were collected by MKu and TK (Electronic supplements A, B)
as follows: geographic position (coordinates measured by hand-held Garmin
GPSmap 60CSx device with accurracy ± 3–5 m), total length (length), diameter at
breast height (DBH), number of parts (parts), stump height if present (stump),
decay stage (1–5, see above; indicated by Latin numerals in diagrams), contact
with the soil in % (soil), bark cover in % (bark), moss cover in % (moss). As for
habitat parameters, we recorded the direction of trunk fall from the base to its
top (azimuth), canopy of mature trees (E3, %, estimated from a rectangle covering
the trunk and an extra 1 m on both sides), canopy of shrubs and young trees up to
a height of 5 m (E2, %, estimated like for E3) and total canopy cover (E3+E
2,%).
To assess trunk mass we computed derived parameters, based on DBH and
length: DBH circle area (diameter2), surface area and volume.
To assess sun exposure and direct solar radiation of the studied trunks based
on tan (slope) × cos (azimuth – 180) for different slopes and orientations to open
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HOLEC J. ET AL.: MACROFUNGI ON FALLEN OAK TRUNKS IN THE BIAŁOWIEŻA VIRGIN FOREST
gaps in the vegetation canopy (which are created by trunk falls), we recomputed
the azimuth of fallen trunk orientation to folded aspect of open gap (McCune
2007). The studied trunks were in horizontal positions, therefore the effect of
slope was omitted. The value of folded aspect varied from 0 for northern to 180
for southern direction of the open gap. For direct incident radiation (symmetrical
along the N–S axis), the value of gap folded aspect was FAs = |180 – |azimuth of
fall direction – 180||, where | means absolute value of equation member, and val-
ues are in degrees. Afternoon direct radiation is represented by the gap folded as-
pect for SW orientation (causing the highest ‘heat load’, HL), which is symmetri-
cal along the NE–SW axis (FAsw [~ HL] = |180 – |azimuth – 225||). Additionally,
the azimuth of fall direction was similarly folded around the W–E (FAe = |180 –
|azimuth – 90||), and NW–SE (FAse = |180 – |azimuth – 135||) axes to include
different effects of direct morning radiation.
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CZECH MYCOLOGY 71(1): 65–89, JUNE 18, 2019 (ONLINE VERSION, ISSN 1805-1421)
Fig. 1. Study area and position of studied trunks (BW1–BW32) of pedunculate oak (Quercus robur)
in Białowieża National Park, Poland. For details, see Electronic supplement A. Source of basic map:
www.mapy.cz.
R e c o r d i n g f u n g i. On each oak trunk studied, we recorded all macromycetes
visible with the naked eye, i.e. all occurrences of asco- and basidiomycetes with
fruitbodies or stromata larger than ± 2 mm. Such a delimitation of the studied
group was chosen among others in order to facilitate comparison with other
71
HOLEC J. ET AL.: MACROFUNGI ON FALLEN OAK TRUNKS IN THE BIAŁOWIEŻA VIRGIN FOREST
Fig. 2. Examples of studied trunks of pedunculate oak (Quercus robur) in the strictly protected zone
of Białowieża National Park, Poland. a– trunk in decay stage 1 (BW10); b– trunk in decay stage 2
(BW6); c– trunk in decay stage 3 (BW17); d– trunk in decay stage 4 (BW28); e– species-richest trunk
(BW5: 38 species); f–Aurantiporus croceus.
studies (see Introduction). Due to the dry September 2016 (see Study area and
Electronic supplement O for details), the fructification of fleshy fungi was rather
low. Fungi not determinable in the field as well as rare or taxonomically compli-
cated species were photographed in situ, collected, described, dried, studied un-
der a microscope and identified by JB, JH, DD and MK. Vouchers are kept in her-
baria PRM (mycological herbarium of the National Museum, Prague, collections
of JH, MK), BRNU (Masaryk University, Brno, collections of DD) and the private
herbarium of JB (Electronic supplement E). Corticioid fungi collected by JH and
MK (except for tomentelloid fungi) were identified by specialist Z. Pouzar (Na-
tional Museum, Prague). Records of most polypores were revised by polypore
specialist P. Vampola (Smrčná). Taxonomy and nomenclature of most species fol-
low Bernicchia & Gorjón (2010), Hansen & Knudsen (2000), Knudsen &
Vesterholt (2012), Ryvarden & Gilbertson (1993, 1994), and Ryvarden & Melo
(2014). Recent taxonomic monographs on particular genera were consulted.
Vegetation description. The vegetation around selected oak trunks
was described with phytosociological relevés. Data were recorded by TK (Elec-
tronic supplement F) using the Braun-Blanquet phytosociological method (Kent
2012). Plant cover was estimated separately for tree (E3), shrub (E2) and herb
(E1) layers on an area of 225 m2(15 × 15 m) using the nine-degree Braun-Blanquet
ordinal scale of cover-abundance values: 1 (rare), 2 (less than 1% cover), 3 (1–3%),
4 (4–5%), 5 (6–15%), 6 (16–25%), 7 (26–50%), 8 (51–75%), 9 (76–100%).
Statistical evaluation. The generalised linear modelling in R (R Core
Team 2018) with Poisson distribution and log-link function was used to assess
the variables affecting fungal species richness (for details, see Electronic supple-
ment G). As we detected multicollinearity of some explanatory variables, the re-
gression analysis was performed with matrix plots and Pearson pair-wise correla-
tions between explanatory variables. Bark cover of studied trunks was negatively
correlated with their decay (–0.45, p < 0.01[**]) and canopy cover (–0.62, p <
0.001[***]), while decay was positively correlated with increasing contact with
the soil (+0.41, p < 0.05[*]), and moss cover (+0.37*). Therefore, the multi-
collinear decay (expressed on ordinal scale) was complemented by a categorial
dummy variable including the different decay stages. Moss cover was related
with shrub cover (+0.36*) and trunks under higher canopy cover had a larger
contact area with the soil (+0.49**).
Species occurrence matrices of fungi and vegetation were analysed using gra-
dient analyses in the Canoco 5 software (ter Braak & Šmilauer 2012, Šmilauer &
Lepš 2014). Collinearity of centered and standardised explanatory trunk and hab-
itat variables was inspected by means of principle component analysis (PCA),
which separated groups of response variables along orthogonal axes, similar to
groups resulting from the regression analysis (see above). In species analyses,
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CZECH MYCOLOGY 71(1): 65–89, JUNE 18, 2019 (ONLINE VERSION, ISSN 1805-1421)
singletons and doubletons were deleted due to their rare occurrence (on one or
two trunks or in their vicinity, respectively). Unconstrained detrended corre-
spondence analysis (DCA) of fungal species composition showed a regular dis-
persion of trunks (Electronic supplement J), which was independent of spatial
position (Fig. 1) and therefore meant a negligible effect of spatial autocorrelation
(Electronic supplement K). Neighbour-clustered trunks differed in decay stage
and other parameters. The total lengths of largest distance measured by DCA
were 3.39 (fungi) and 2.21 (plants), which allowed us to use unimodal ordination
methods. A multivariate constrained method, namely canonical correspondence
analysis (CCA), was used to analyse the relationship between the fungal species
pattern and partitioned variation of trunk and habitat predictors (Legendre &
Legendre 2012). The CCA of the influence of dominant fungal species on fungal
assemblages used the presence/absence of dominant species as an explanatory
variable after extraction of the fungus from the species table. The explanatory ef-
fects of particular environmental variables were evaluated with Monte Carlo per-
mutation tests (MCPT, number of permutations was assigned to 999) using the
forward selection procedure which selected variables with the best fit of species
data. Collinearity was avoided using adjusted p-values. Symmetric co-correspon-
dence analysis (CoCA) was used to compare fungal and plant species patterns.
RESULTS
Fungal diversity
The total number of fungal occurrences on 32 trunks studied was 792. We
recorded 187 species of macrofungi (Electronic supplement D). Macroscopic
ascomycetes were represented by 7 species and basidiomycetes by 180 species.
The species-richest genera were Mycena (20 species), Tomentella (13), Botryo-
basidium (8), Hyphodontia (8), Pluteus (6), Trechispora (6), and Entoloma (5).
The most frequent species were Hymenochaete rubiginosa,Phaeohelotium
monticola,Xylobolus frustulatus,Mycena inclinata and Mycena galericulata
(found on more than 70% of trunks; H. rubiginosa on 88%). On the other hand, 84
species (44%) were found on 1 trunk only, 36 species on 2 trunks, and 19 species
on 3 trunks. Species occurring on 1–3 trunks represented 74% of the total fungal
diversity. This means that the species composition on each trunk is rather spe-
cific, consisting of several frequent species plus a variable set of infrequent ones.
The mycobiota consisted especially of corticioid and agaricoid fungi. These
fungi often produced fruitbodies on decaying pieces of wood and bark lying on
the soil below the trunks. The more decayed trunks and woody debris from them
were also occupied by mycorrhizal fungi, e.g. agarics (Amanita,Cortinarius,
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HOLEC J. ET AL.: MACROFUNGI ON FALLEN OAK TRUNKS IN THE BIAŁOWIEŻA VIRGIN FOREST
Hebeloma,Inocybe,Laccaria,Lactarius,Paxillus,Russula,Tri cho lom a), plus
Clavulina, the gasteromycetoid Scleroderma, resupinate fungi (Amphinema,
Byssocorticium, Pseudotomentella,Tomentella), and several ascomycetes
(Helvella,Humaria). In total, 37 species of mycorrhizal fungi (20% of the total
number of species) were found. Interestingly, the group of polypores was rather
species-poor, including a small group of polypores with large fruitbodies
(Aurantiporus croceus,Laetiporus sulphureus,Phellinus robustus,Piptoporus
quercinus,Trametes gibbosa) and several resupinate species of the genera
Antrodia,Datronia,Perenniporia,Physisporinus,Rigidoporus,Schizopora
and Trechispora. Ascomycetes with larger fruitbodies or stromata were infre-
quent (7 species of the genera Ascocoryne,Cudoniella,Helvella,Humaria,
Kretzschmaria,Phaeohelotium and Xylaria). However, small ascomycetes not
recorded by us (e.g. Mollisia,Orbilia, etc.) would add further species to the total
fungal diversity.
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Fig. 3. Range of fungal species richness of all studied trunks in relation to particular stages of trunk
decay (I–IV; n: number of studied trunks). No significant difference in fungal richness between decay
stages was detected.
Individual trunks hosted 4 to 38 species of macrofungi (Electronic supple-
ment C). Trunks inhabited by 30–38 species were in decay stages 2 and 3 with the
three richest ones in stage 2. However, the fungal richness of trunks in stage 2
varied considerably as they hosted both a low (11) and a high (38) number of spe-
cies. Trunks with a low number of species (4–9) were in decay stages 3–4.
Trunk parameters and fungal richness
We tested pairwise correlations between all trunk and habitat parameters and
fungal richness. The number of fungal species is significantly (negatively) corre-
lated with a SW direction of trunk fall, which represents the highest gap heat load
(r = –0.49, p < 0.01[**]). Trunk size parameters (correlation with diameter +0.41,
p < 0.05[*]) are also significant. Of the studied trunks (60–130 cm in diameter),
those with a diameter below 97.5 cm host 16.1 species on average whereas
thicker trunks host 24.5 species on average.
The possible collinearity of trunk parameters was additionally detected using
PCA (Fig. 4). In this diagram, the correlation structure between these variables is
seen. The gradient of decay from the right low quadrant to the upper left quad-
rant represents a temporal succession scale. The most important factor for the
higher number of fungal species (Fspec) is a group of trunk parameters repre-
sented by percentage of bark cover (which is negatively related to the canopy
cover and relative contact area with the soil, all these variables also reflecting de-
cay). Another important group relating to fungal richness consists of trunk diam-
eter, stump height and number of trunk parts (the last two parameters having
a significant effect, p < 0.01, but are present in 4 trunks only, therefore we do not
use them in further considerations). This group is negatively correlated with
folded SW aspect for open gap heat load (HL) and tree layer cover.
Generalised linear and additive models estimating the total richness of fungal
species show an integrated role of decay stage and trunk size parameters
(diameter2: circle area of DBH, Electronic supplement I), with an additional lin-
ear effect of length and other trunk mass parameters (volume, surface), folded
aspect of gap heat load, moss and shrub covers (compare different complexity
degree in individual models, Electronic supplement H). The number of fungal
species on particular trunks does not significantly depend on concrete decay
stages. A slight trend is seen in Fig. 3, showing the highest number of species on
trunks in stage 2 and a subsequent slight decrease in stages 3 and 4 (trunks in
stage 4 show higher variance in number of species), but it is biased by the uneven
number of trunks studied in particular decay stages (Fig. 3).
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Pattern of fungal species occurrence
The composition of frequent fungal species (without single- and doubletons)
reflects the general results regarding total species richness (see Fig. 4, supple-
ments J, K). The main habitat gradient (Fig. 5) relates to gap heat load (which is
negatively correlated with total fungal species richness). The species Hydropus
floccipes, Mycena speirea and Pluteus podospileus are associated with a high
species richness on trunks. In opposite direction, species-poor trunks are pres-
ent, which are characterised by a high HL. Heat-exposed trunks are associated
with e.g. Resinicium furfuraceum, Mycena inclinata and Hypholoma fasci-
culare. The second main gradient (Figs. 4, 5, supplement K: along Y axis) is repre-
sented by trunk size characteristics (diameter, length, number of parts, presence
of a stump), their moss/bark cover and contact with the soil. Species of long,
bark-covered trunks (Fig. 5: upper part of the diagram) are e.g. Kretzschmaria
deusta, Ganoderma applanatum and Tomentella sublilacina.Inthelowerpart
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Fig. 4. Unconstrained ordination biplot (PCA) of trunk parameters with positions of individual
trunks. The clumped arrows (highlighted by left and upper ellipses) show common effects of the pa-
rameters. The angle between arrows indicates pair-wise correlations, which are negative in opposite
direction. For abbreviations, see Material and methods.
of the diagram, high-diameter trunks having a large contact area with the soil are
present, associated with e.g. Aurantiporus croceus, Botryobasidium subcoro-
natum, and to a lesser degree with Phlebiella vaga and Botryobasidium inter-
textum. Trunk decay stage has a low direct effect on fungal species patterns.
We compared the effects of trunk and habitat groups as predictors in variation
partitioning. Constrained analysis CCA (Fig. 6) highlighted more specialised spe-
cies, having significant relation to both the trunk and habitat characteristics.
Bark cover and relative contact area with the soil, together explaining 3.9%
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HOLEC J. ET AL.: MACROFUNGI ON FALLEN OAK TRUNKS IN THE BIAŁOWIEŻA VIRGIN FOREST
Fig. 5. DCA with frequent fungal species and passively projected trunk and environmental para-
meters. The total species richness (Fspec: total number of fungi per trunk including single- and
doubletons) decreases along the first ordinal axis (X). Parameters not favourable for fungi increase
in opposite direction (higher tree and shrub cover and higher gap heat load index). The second axis
(Y) covers trunk parameters. Both first and second axes explain 15% of species variation. See also
Electronic supplements J, K. Individual decay stages are marked by Latin numerals. For full names of
fungi, see Electronic supplement D, for abbreviations of parameters, see Material and methods.
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A
B
(F = 1.6, p < 0.001, see Fig. 6A), and heat load with total canopy cover, explaining
4.2% (F = 1.7, p < 0.001, Fig. 6B) of the fungal species pattern, were chosen using
the forward selection approach (separately for each group). A negative fraction
of intersection of both groups indicates that trunk and habitat predictors, if con-
sidered together, explain the fungal species pattern better than the sum of the in-
dividual effects of group variables (7.3%, F = 1.6, p < 0.001). In the upper right
quadrant (Fig. 6A), species found on trunks with a high bark cover (connected
with lower decay stages) are situated, e.g. Xylaria polymorpha,Pluteus
cervinus,Galerina marginata and Kretzschmaria deusta. In the opposite upper
left quadrant, species of later decay stages typical by their larger contact area
with the soil are placed. The group of species connected with a high canopy
cover (lower part of Fig. 6B) is rather rich. This group is mainly represented by
corticioids and agarics with tiny basidiomata. In the upper left quadrant of
Fig. 6B, species of trunks with a high heat load, i.e. more exposed to the sun
(but also to precipitation via forest gaps) are found, e.g. Kavinia alboviridis,
Hymenochaete cinnamomea,Marasmius torquescens and Athelia decipiens.
These diagrams (Fig. 6) have a higher explanatory value as for the ecological
niche of the depicted fungi (the niche being defined by selected explanatory vari-
ables) than the previous one (Fig. 5). Interestingly, some distinctive species like
Aurantiporus croceus, Hydropus floccipes and Xylobolus frustulatus are in
a central, ‘intermediate’, position in the diagrams. As shown in the previous para-
graph, individual levels of decay stage do not have a direct significant effect
on species composition. However, there are some differences (Electronic
supplement J). Decay stage 2 situated in the left part of the biplot differs from
stages 3 and 4, which overlap (but stage 4 includes more species).
We explored whether the presence/absence of some fungal dominants (i.e.
species occurring on a higher number of trunks and forming large or many
fruitbodies) influences species composition of a trunk. Of the tested spe-
cies, Ganoderma applanatum (p-ratio = 0.01), Mycena inclinata (p = 0.025),
Kretzschmaria deusta (p = 0.037) and Xylobolus frustulatus (p = 0.05) had a sig-
nificant effect, whereas Laetiporus sulphureus and Aurantiporus croceus were
not significant. However, the presence of species with the strongest effect,
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£Fig 6. Ordination biplots (CCA) with fungal species. Only significant explanatory variables are
displayed for trunk (A) and habitat (B) groups of characteristics. For full names of fungi, see Elec-
tronic supplement D, for abbreviations of parameters, see Material and methods. The fifty fungal spe-
cies with the highest fit are projected.
A: Contact with the soil explained 5.3% of total variance [F-ratio = 1.7, P-value = 0.002, P(adjusted) =
0.008], bark cover explained 4.4% (1.4, 0.019, 0.076). The first two axes cover 9.7% of fungal cumula-
tive variance (adjusted 3.5%).
B: Heat load (HL: 5.2%, 1.6, 0.002, 0.012) and total canopy cover (E32: 4.7%, 1.5, 0.01, 0.06); first two
axes cover 9.9% (adjusted 3.6%) of fungal variance.
Ganoderma applanatum (Electronic supplement L), does not influence the total
species richness (including single- and doubletons).
Vegetation characteristics of fungal habitats
Most of our vegetation relevés represent various subassociations of the Tilio-
Carpinetum association in which shade-tolerant species prevail. The plant spe-
cies richness corresponds to the E direction of the trunk fall and its volume. Sur-
prisingly, no effect of forest lighting was found in the SW direction. A higher pro-
portion of shrub cover only had a low effect on both plant and fungal species
richness (through shadowing). The plant species pattern in unconstrained DCA
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Fig. 7. First two axes of CCA biplot of plant species pattern with the only significant trunk parame-
ter: contact with the soil. This parameter explains 5.1% of species variance on the first constrained
axis (X). Thirty species with a higher fit are projected. The species in the left part of the diagram are
typical of nutrient-rich mesic soils. For full names of plants, see Electronic supplement F.
generally reflects two main ecological gradients – soil moisture and nutrients
(Electronic supplement M). After removing spatial covariance, no trunk parame-
ter affects the plant species pattern except for contact with the soil (F-value =
1.6, p-ratio = 0.023). Plants requiring nutrient-rich soils occur in the vicinity of
trunks having a larger contact area with the soil and later decay stages (Fig. 7).
The shared CoCA analysis of fungal and plant communities showed non-signifi-
cant cross-correlations, but supported the relation of some plants to enriched
soils (Electronic supplement N).
DISCUSSION
Fungal diversity
The number of 187 species recorded on just 32 oak trunks during one visit rep-
resents a rather high fungal diversity. It seems that the results were not substan-
tially negatively influenced by the dry September 2016, as the previous months
were rich in precipitation (Electronic supplement O) and lignicolous fungi could
have used the water accumulated in the wood before. We suppose that the por-
tion of agarics and corticioids with ephemeral fruitbodies not observed by us due
to the September drought was negligible.
Works using permanent plots/sites each containing several dead wood units
(e.g. stumps, logs, branches; but mostly of smaller volume than in our case) usu-
ally report 70–100 species (Tab. 1) with a peak of 203 species (Irše˙naite˙&Kutorga
2006, 2007). The reasons for high diversity found out by us were certainly the
large size of the studied trunks (documented also in our trunk size gradient, see
Results) plus the detailed way of our field work focused on all groups of macro-
fungi including tiny agarics, corticioids and heterobasidiomycetes, and also on
mycorrhizal fungi fructifying on rotten oak wood and wood debris (usually omit-
ted in previous works). Such a detailed approach was used only by Nordén et al.
(2004) and partly Grosse-Brauckmann & Grosse-Brauckmann (1983). Another
reason seems to be the high fungal richness of the Białowieża Virgin Forest
(Karasiński et al. 2009, 2010, Karasiński & Wołkowycki 2015, Karasiński 2016),
which represents a huge pool of spreading mycelia and spores of more than 1800
macrofungal species.
Using 454 pyrosequencing of ITS, van der Wal et al. (2015) discovered 447 fun-
gal OTUs (among them 262 ascomycetes and 148 basidiomycetes) in 46 decaying
stumps of Quercus robur in the Netherlands (young stumps up to 5 years after cut-
ting, i.e. initial stages of wood decay, diameter 20–22 cm). These results are not
comparable with ours, as they were obtained by a different method from another
kind of substrate, but suggest that real fungal diversity in oak wood is much higher
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HOLEC J. ET AL.: MACROFUNGI ON FALLEN OAK TRUNKS IN THE BIAŁOWIEŻA VIRGIN FOREST
than diversity documented by fruitbody-based research. However, the dominance
of basidiomycetes over ascomycetes in later decay stages observed by us agrees
with formerly published data (e.g. Nordén et al. 2004, Irše˙naite˙ & Kutorga 2006).
Tab . 1. Overview of published data on biodiversity of fungi on decaying oak wood (mostly Quercus
robur) in Europe. The studies are arranged according to the number of visits.
Source Years
of study
Number
of visits
Number of trunks /
wood units / plots
Number
of fungal
species
Studied groups of fungi
This study: Poland 1 1 32 trunks (1 site) 187 All macrofungi with
fruitbodies larger than 2 mm
in diameter
Běťák 2016:
Czech Republic
1 3 32 trunks (1 site) 165 All macrofungi with
fruitbodies larger than 2 mm
in diameter
Irše˙naite˙&Kutorga
2006, 2007: Lithuania
21per
plot
321 units (46.5 m3)
of coarse woody
debris of oak in 50
plots (10 sites)
203 All macrofungi
O’Hanlon &
Harrington 2012:
Ireland
2–3 4–6 5 plots (5 sites) 94 All macrofungi with
fruitbodies larger than 5 mm
in diameter
Grosse-Brauckmann &
Grosse-Brauckmann
1983: Germany
3 20 1 site, traditional
field survey
71 Aphyllophorales, other groups
of macrofungi less intensely
Županić et al. 2009:
Croatia
3 ? 4 sites, traditional
field survey
72 Macrofungi with conspicuous
fruitbodies
Our dataset contains many oak specialists and oak-favouring fungi, both com-
mon species like Hymenochaete rubiginosa,Mycena inclinata,Laetiporus
sulphureus, and generally rare ones (Vasiliauskas et al. 2003, Blaschke et al.
2009) like Aurantiporus croceus,Hydropus floccipes,Perenniporia medulla-
panis,Piptoporus quercinus and Vararia ochroleuca. It also includes opportun-
ists (Pluteus cervinus,Hypholoma spp., Mycena galericulata, etc.). Surprisingly,
quite a lot of species usually preferring spruce or generally coniferous wood were
recorded (Botryobasidium intertextum,Crustoderma dryinum,Gloeopenio-
phorella convolvens,Hyphodontia abieticola,Jaapia ochroleuca,Rigidoporus
crocatus,Scytinostromella heterogenea). Their occurrence on oak trunks in the
Białowieża Forest is presumably enabled by the specific tree composition of
hemiboreal forests, where spruce and oak have co-existed for thousands of years
since the late Holocene (Milecka et al. 2009), and also by the long period without
human intervention, which has led to an extraordinary number of various sub-
strates for lignicolous fungi. Several species not listed for BNP by Karasiński et
al. (2010) were also documented during our study. We will focus on them in a sep-
arate study in the future.
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Trunk parameters and fungal richness
Analysis of our data highlighted that the species-richest trunks are volumi-
nous (thick, long), with a high bark cover, and in younger stages of decay. Such
trunks are exposed to direct precipitation due to the gap in forest canopy caused
by the fall of the tree (until the gap is closed by the growth of surrounding shrubs
and trees). Additionally, high fungal richness is supported by trunk fragmentation
(stump + log or trunk broken into two or more parts). Surprisingly, orientation of
the fallen trunks also proved to be very important. We found that the species-
richest trunks were oriented ‘properly’, i.e. in north-east directions (N, NE, E)
representing a minimal heat load through the gap. Vegetation surrounding such
gaps protects especially large lower trunk parts from direct sun radiation (espe-
cially the afternoon sun) and consequent desiccation (which has a negative ef-
fect on fungal fructification and/or occurrence). Lindhe et al. (2004) also studied
the influence of sun exposure on fungal richness. They found that numbers of
species were not related to the level of sun exposure. However, their study was
carried out under different habitat conditions (cut stumps and logs). The impor-
tance of wood moisture and fungal richness on oak wood decay was recently
stressed by van der Wal et al. (2015).
The positive effect of oak CWD volume on fungal richness was also men-
tioned by Irše˙naite˙ & Kutorga (2007) and Lindhe et al. (2004). In a study from
Ohio, USA, Rubino & McCarthy (2003) further showed that fungal species rich-
ness was positively correlated with volume of woody debris in the study plot and
with volume of studied logs, amount of bark, and amount of fragmented wood. It
seems that the trunk parameters shown to be significant for fungal richness in
our and other studies are of general validity, at least for oak CWD.
Concerning the heat load, the afternoon direct solar radiation causes higher
temperature maxima than equivalent morning radiation. Geiger et al. (2003) men-
tion near-ground temperatures to be up to 5 °C higher in comparison with shad-
owed stands, depending on the ratio of gap diameter to height of surrounding
stand. Indeed, we found that a SW orientation of the studied trunks (and gaps
which they create during the fall) has a significantly negative effect on species
richness. This is also connected with the fact that a falling tree crown creates
a wider gap in its SW part which enlarges the sun exposure of the lower tree half
(especially from the most intensive afternoon radiation). Moreover, gap size in-
fluences the amount of precipitation. Slavík et al. (1957) documented that rainfall
below trees was about 20–30% lower in comparison with the gap centre, while
rainfall on the SW gap edge was increased by over 100% by transmisson of precip-
itation by wind. Optimal gaps have a ratio of diameter to height of surrounding
stand in the range 1–2 (Geiger et al. 2003, Muscolo et al. 2014). Such gaps exhibit
a lower direct sky view and longwave radiation loss, lower evaporation, better
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HOLEC J. ET AL.: MACROFUNGI ON FALLEN OAK TRUNKS IN THE BIAŁOWIEŻA VIRGIN FOREST
protection against wind and late frosts, higher nocturnal temperature minima
and dew point (affecting air humidity). All these microclimatological characteris-
tics differ on shaded southern vs. sunny northern edges of the gap (Geiger et al.
2003). Consequently, the fallen trunks represent a continuous gradient of micro-
climatically diverse microhabitats (along their length).
Pattern of fungal species occurrence
Our data show that the fungal community composition on particular trunks is
significantly influenced by gap orientation and resulting heat load. Trunks ex-
posed to more intensive afternoon sun radiation have a different (and species-
poorer) mycobiota than the shaded, more species-rich ones, inhabited by e.g.
Hydropus floccipes, Mycena speirea and Pluteus podospileus. As far as we
know, the role of fallen trunk orientation on their fungal richness and species pat-
tern has not been paid attention to date.
Further important factors are trunk size parameters, canopy cover, percent-
age of bark and moss cover and relative contact area with the soil. The influence
of these parameters on fungal communities has not been assessed in detail in tra-
ditional ‘oak’ studies. Irše˙naite˙ & Kutorga (2006) only stressed the role of wood
decay stage. They showed that there is a difference in community composition
between early (1–2) and later (4–5) stages (principally the same situation was de-
scribed by van der Wal et al. 2015), but no strong preference of most fungal spe-
cies for wood of a particular decay stage. Van der Wal et al. (2015) showed in their
molecular study that key factors of decay rate change in time: the variance of de-
cay rate in initial sapwood is significantly correlated with wood moisture con-
tent, whereas it is related to the composition and OTU richness of the fungal
community in later stages.
Our data also show that wood decay stage has a low direct effect on commu-
nity composition. We observed that the decay of thick oak trunks considerably
differs from e.g. beech or spruce (Renvall 1995, Heilmann-Clausen 2001). It often
starts simultaneously from the surface (by decortication and subsequent decay
or separation of thin wood layers, forming wood debris below the trunk, which
often hosts interesting fungi) and in the inner trunk part (resulting in creation of
a large central cavity). Consequently, estimation of the ‘average’ decay stage of
the whole trunk (especially of stages 2–4) was not easy. In some cases it was
a compromise between wood hardness and overall trunk appearance. This ambi-
guity is probably also a reason why some common species, generally preferring
later stages of wood decay (e.g. Pluteus cervinus,Galerina marginata) occu-
pied trunks covered with bark (see Fig. 6A). In fact, their mycelium probably
favoured more decayed wood inside such trunks.
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Boddy (2001) showed that fungal decomposers have a great effect on the
wood decay process. Their interactions, above all competition (recently stressed
by e.g. van der Wal et al. 2016 and Hiscox et al. 2018), result in highly variable fun-
gal communities, differing in each wood unit (Kubartová et al. 2012, van der Wal
et al. 2015). Our analyses show considerable influence of some dominant species
(Ganoderma applanatum,Mycena inclinata,Kretzschmaria deusta,Xylobolus
frustulatus) on fungal community composition. The differences are most proba-
bly explainable by the competitive power of these species. Another reason for
community variation is the random way of fungal spread (via spores or mycelia)
and the presence of some wood-decaying species already in living trees (Parfitt
et al. 2010).
Trunks, their decay, and surrounding vegetation
All of the studied trunks were situated in a generally closed forest stand. How-
ever, the canopy cover directly above individual trunks differs considerably
(Electronic supplement B). Initially, the fall of either a living or a dead trunk (by
uprooting or breakage) opens the tree and shrub layer by creating a canopy gap.
If the fallen trunk still has thick branches, it is mostly not in full contact with the
soil, as the branches lift it from the soil surface. Later on, the trunk slowly ‘sits’
down on the floor (the supporting branches slowly disappearing by breakage or
decay), decorticates (also due to the fungal activity), and is covered by mosses
(simultaneously its fungal richness slowly decreases).
The different shading described in previous chapters has an effect on plant
species richness. Our data showed that plant richness increases with eastern ori-
entation of the gap (morning radiation, Electronic supplement H). The trunk vol-
ume also has an important effect on plants (similar to the case of fungal rich-
ness). Larger trunks create larger gaps and enhance the abovementioned effects.
During this initial phase, shading caused by a higher proportion of shrubs has
a positive effect on plant richness. Later on, the surrounding shrubs and trees
continue to grow and finally close the canopy gap. The revegetation process is
accelerated not only by eastern orientation of the fallen trunk, but probably also
by an increasing amount of available water and nutrients which are not extracted
by living large trees. The increasing cover of the shrub layer positively affects
fungal richness only in the initial decay stages (shading and consequent lower
gap heat load). Longer lying trunks are gradually overgrown by shrubs and trees,
thus sheltered from rainfall, and both plant and fungal richness decrease (Fig. 3,
Electronic supplements H, K).
Trunks in advanced decay stages have a larger contact area with the soil (Fig. 4),
which can potentially enrich the soil below and around the trunk. Our results
show that nutrient enrichment is reflected by the surrounding plants, where
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HOLEC J. ET AL.: MACROFUNGI ON FALLEN OAK TRUNKS IN THE BIAŁOWIEŻA VIRGIN FOREST
species requiring a higher level of nutrients and moisture prevail (Fig. 7). This
agrees with data by Chećko et al. (2015), who reported an increase in local plant
species cover and frequency directly on logs and their surroundings, with some
species facilitating deadwood decomposition. Similarly, the plant species re-
ported as the most frequent by them were similar to the species occurring in our
vegetation samples around trunks with a larger contact area with the soil. How-
ever, Harmon & Hua (1991) documented slower decomposition and a temporal
lag of nutrient release from woody debris in comparison to litter.
ACKNOWLEDGEMENTS
We thank the Białowieża National Park authorities for approving our research
and providing permission to enter the strictly protected zone. We thank Z. Pouzar
(Prague, Czech Republic) for identification of some corticioids, P. Vampola
(Smrčná, Czech Republic) for identification or revision of most polypores, and
D. Karasiński (Kraków, Poland) for help with literature on fungi of the Białowieża
Forest. The work of Jan Holec and Miriam Kuchaříková was financially sup-
ported by the Ministry of Culture of the Czech Republic as part of the long-term
development of research organisation National Museum (DKRVO 2019-2023/3.I.a,
00023272).
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