FEMS Microbiology Ecology, 92, 2016, fiw068
doi: 10.1093/femsec/fiw068
Advance Access Publication Date: 7 April 2016
Research Article
RESEARCH ARTICLE
Competitive outcomes between wood-decaying fungi
are altered in burnt wood
Mattias Edman and Anna-Maria Eriksson∗
Department of Natural Sciences, Mid Sweden University, Holmgatan 10, SE-851 70, Sundsvall, Sweden
∗
Corresponding author: Department of Natural Sciences, Midsweden University, Holmgatan 10, 85170 Sundsvall, Sweden.
Tel: +46-101428557; E-mail: [email protected]
One sentence summary: Competitive outcomes between wood-decaying basidiomycetes are altered in burnt wood, indicating that forest fires indirectly
structure fungal communities by modifying dead wood.
Editor: Wietse de Boer
ABSTRACT
Fire is an important disturbance agent in boreal forests where it creates a wide variety of charred and other types of
heat-modified dead wood substrates, yet how these substrates affect fungal community structure and development within
wood is poorly understood. We allowed six species of wood-decaying basidiomycetes to compete in pairs in wood-discs that
were experimentally burnt before fungal inoculation. The outcomes of interactions in burnt wood differed from those in
unburnt control wood for two species: Antrodia sinuosa never lost on burnt wood and won over its competitor in 67% of the
trials compared to 40% losses and 20% wins on unburnt wood. In contrast, Ischnoderma benzoinum won all interactions on
unburnt wood compared to 33% on burnt wood. However, the responses differed depending on the identity of the
competing species, suggesting an interaction between competitor and substrate type. The observed shift in competitive
balance between fungal species probably results from chemical changes in burnt wood, but the underlying mechanism
needs further investigation. Nevertheless, the results indicate that forest fires indirectly structure fungal communities by
modifying dead wood, and highlight the importance of fire-affected dead wood substrates in boreal forests.
Keywords: basidiomycetes; boreal; charred wood; dead wood; interspecific competition; forest fire; polypores
INTRODUCTION
In boreal forests, fire plays an important role as a disturbance
agent. Historically, it has affected such a major part of the
landscape (Zackrisson 1977; Johnson, Miyanishi and Weir 1998;
Niklasson and Granström 2000) that many forest species, including fungi, have adapted to fire disturbance (Granström and
Schimmel 1993; Penttilä and Kotiranta 1996; Hyvärinen, Kouki
and Martikainen 2006). Several studies have shown that the
species composition of wood-decaying fungi is altered after fire,
and some species seem to be more or less confined to forests
that have been affected by fire (Penttilä and Kotiranta 1996; Junninen, Kouki and Renvall 2007; Berglund et al. 2010; Olsson and
Jonsson 2010; Suominen et al. 2015). The mechanisms behind
these community changes are largely attributed to changes in
forest structure after fire, such as a more open canopy and an
altered composition of dead wood. For example, more than 40%
of the pre-fire dead wood was consumed in controlled restoration burnings in Swedish Scots pine (Pinus sylvestris L.) forests,
where logs in the late stages of decay were consumed to a much
higher extent than those in earlier stages of decay (Eriksson et
al. 2013). However, due to a high input of standing fire-killed
trees, fires generally cause a net increase in dead wood (Siitonen
2001; Eriksson et al. 2013). In addition to the structural changes,
fire also creates unique dead wood substrates, such as burnt
and charred wood, which are usually abundant after forest fires
(Eriksson et al. 2013). The influence of these substrates on fungal community structure and development within wood is, however, poorly understood.
Received: 7 November 2015; Accepted: 28 March 2016
C FEMS 2016. All rights reserved. For permissions, please e-mail: [email protected]
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FEMS Microbiology Ecology, 2016, Vol. 92, No. 6
Competition is a fundamental process in structuring species
communities. For fungi restricted to a transient resource unit
such as dead wood, competition for space and associated resources is usually very intense (Boddy 2000). The outcomes of
these interactions are largely determined by the species’ competitive ability, but the competitive balance may shift between
fungal competitors depending on priority effects (i.e. the order of
species arrival) or the particular abiotic and biotic circumstances
(e.g. Fukami et al. 2010). Temperature, moisture, wood properties, mycelial size and invertebrate grazing may all influence
competitive outcomes between saprotrophic fungi (Holmer and
Stenlid 1993; Boddy 2000; Toljander et al. 2006; Crowther, Boddy
and Jones 2011; Edman and Fällström 2013). Forest fire may also
influence fungal interactions. Carlsson et al. (2012) found that
wood-decaying fungi prevalent in forests characterized by fire
were more resistant to heat, and more successful in competitive
interactions in wood compared to non-fire associated species
after heating of the wood and fungi to about 56◦ C (Carlsson et
al. 2014). Still, many mycelia are killed by the fire, which, by vacating habitat in the heated and charred wood, can allow other
species to establish.
The heated and charred wood created by the fire thus provides new space for fungi to colonize, either through the extension of surviving mycelia in wood or soil, or by germinating
spores. However, it is possible that the fire indirectly influences
different species’ competitiveness and thus the developing fungal community in this new resource. When strongly heated, the
properties of the wood are altered. This is well researched within
the field of wood preservation where heat treatment is used to
slow down the decay process and extend the life of commercial wood products (Esteves and Pereira 2009). Heat treatment alters the chemical composition of the wood by degrading cell wall
compounds and extractives (Esteves and Pereira 2009). At 180◦ C
–250◦ C, the temperature range commonly used for heat treatments, wood undergoes important chemical changes. Hemicellulose and extractives, especially the volatile ones, are degraded
or disappear while cellulose and lignin are less affected. However, even lignin and cellulose undergo structural changes when
heated and although most original extractives disappear, new
ones appear when polysaccharides are degraded (Esteves and
Pereira 2009). At temperatures above 200◦ C and where flaming
combustion is inhibited by low oxygen availability (pyrolysis),
charring processes start. (Esteves and Pereira 2009). Char is not
a discrete substance but represents a continuum of structures
with different chemical and physical properties (Czimczik et al.
2002).
Given that forest fire has probably been an important factor
in shaping boreal forests during the evolution of wood-decaying
fungi, some species are likely to have adapted to the unique
types of dead wood it creates. For example, observations of fruiting bodies suggest an increased prevalence of certain species on
charred wood, including some rare and threatened species (Renvall 1995; Niemelä 2005; Olsson and Jonsson 2010; Zhou and Dai
2012). Information on how fire-affected wood influences fungi is
therefore important, not least in light of the fact that these substrates have become increasingly rare in Fennoscandian boreal
forest due to increasingly efficient fire prevention since more
than a century ago. Further, controlled forest fire is increasingly used as a method to recreate fire-characterized forests and
associated dead wood in the Nordic countries, and knowledge
on how fungi are influenced by fire is therefore needed. In the
present study we experimentally tested the indirect effect of
fire in structuring fungal communities by examining how wood,
modified by fire, influences competitive fungal interactions. We
allowed six species of wood-decaying basidiomycetes to compete in pairs in experimentally burnt wood-discs and unburnt
control discs in microcosms. Specifically, we hypothesized that
(i) burnt wood alters the competitive outcome of fungal interactions and (ii) the outcomes of interactions are species-specific.
METHODS
Wood material and preparation
Three healthy 8 cm base diameter trees of Scots pine (P. sylvestris)
were harvested in plantations close to Sundsvall in the middle
boreal zone of Sweden. All trees had regenerated at the same
time after clear-cut harvest. Logs were machined into 1 cm thick,
7.0–7.4 cm diameter discs and dried at 30◦ C for 6 days in a heating cabinet. In order to mimic the effect of forest fire, half of the
wood-pieces were then burnt, one by one, for 2 min using a butane burner. After about 1.5 min over the gas flame the discs
caught fire and were allowed to burn for ∼30 s before being extinguished by dropping in water. The temperature inside the discs
after burning was measured on a separate set of 10 discs, which
were pre-drilled with a 3.5 cm long 1.5 mm diameter hole from
the outer bark surface into the core. Instead of dropping these
discs in water, a thin temperature probe connected to a Tinytag
logger was inserted into the pre-drilled hole immediately after
the flame was extinguished by being blown out.
All wood-discs to be used in the competition experiment
were then split across the middle into two equal-sized halves
(semicircles) and sterilized by gamma irradiation at a dosage of
25 kGy (by Isotron Nederland B.V.). Finally, since the discs had
been dried they were soaked in autoclaved, distilled water for 4
h prior to experimental use. To test how the fire treatment affected the water absorbing ability of the wood we calculated the
moisture content (MC) of a subset of 20 treated and 20 untreated
discs after having been soaked in water by
MC =
wet weight − oven dry weight
× 100
oven dry weight
Fungi
We used six species of wood-decaying fungi, all of which are
common early- to mid-succession decayers on dead Scots pine
and Norway spruce wood in Fennoscandia (Niemelä 2005): Antrodia sinuosa ((Fr.) P. Karst.), A. xantha ((Fr.:Fr.) Ryvarden), Fomitopsis pinicola ((Sw.:Fr.) P. Karst.), Gloeophyllum sepiarium (Wulfen:
Fr.), Ischnoderma benzoinum ((Wahlenb.:Fr.) P. Karst.), Oligoporus
sericeomollis ((Romell) Bondartseva) (Mid Sweden University Fungal Collection). Observations of sporocarps indicate that all included species can occur together on the same substrate under
natural conditions (Olsson and Jonsson 2010). Antrodia sinuosa, A.
xantha and O. sericeomollis are frequently found on pine logs that
have been influenced by forest fire (Olsson and Jonsson 2010;
Zhou and Dai 2012; Penttilä et al. 2013) while the other species
show no such clear association although they do occasionally
occur on burnt wood substrates after fire. In addition, based on
our previous laboratory experience, these species are easy to cultivate and to recognize in pure culture. Three strains of each
species were used. The fungi were sub-cultured in vented 15 cm
diameter Petri dishes with 2% malt extract agar (MEA). Prior to
experimental use the semicircular pieces of wood were added to
2-week-old fungal cultures and incubated in a closed cabinet at
a temperature of 20◦ C for 8 weeks until all pieces of wood were
Edman and Eriksson
3
Figure 1. Schematic overview of the experimental design showing the two treatments (burnt and unburnt control), number of species, strains and the replicated
pairwise competition setup. Only the scheme for strain 1 of species 1 on burnt
wood is shown, but the procedure was the same for all species and strains. For
all species, the strain 1s were combined pairwise with each other, as were the
strain 2s, and strain 3s. These combinations were then replicated three times,
resulting in 270 trials in total.
completely colonized. The inoculation was randomized with regard to the different individual trees from which the discs were
made.
Experimental setup
The fungus-colonized semicircular pieces of wood were put together, two by two, with the cut sides in full contact, in vented
Petri dishes (100 × 20 mm) with water agar. All possible pairs of
species were allowed to compete with each other, resulting in
15 trials. This was repeated for the three strains, where strain
1 of species 1 was combined with strain 1 of each of the other
species, strain 2 of species 1 was combined with strain 2 of
the other species etc., resulting in 45 trials for each treatment
(burnt and control). This setup, which avoids dependence based
on strain identity among replicates, was replicated three times
making up a total of 270 trials (Fig. 1). The wood-discs were then
incubated for 8 months in darkness at room temperature.
Determining interaction outcomes
We applied a slightly modified version of the classification used
by Crowther, Boddy and Jones (2011) to judge interaction outcomes: (i) overgrowth, where one fungus had grown over another without killing its competitor; (ii) replacement, where
mycelia of one fungus was killed and replaced by its competitor; (iii) mutual replacement, where mycelia from both fungi had
grown into each other’s domain and (iv) deadlock, where neither fungus had gained territory of the other. Overgrowth and
replacement were recorded as being a ‘win’ if the aggressor had
reached at least 1 cm into its competitor’s semicircle, representing roughly 30% of its domain (Fig. 2, Fig. S1, Supporting Information). Mutual replacement was recorded as a ‘draw’ if neither
species had advanced 1 cm into its competitor’s semicircular domain. Likewise, deadlock was recorded as a ‘draw’.
To determine the interaction outcome of each trial we identified the mycelia within each piece of wood. Two small wood
samples, each 0.5 cm diameter, were carved out from each semicircle, 1 cm from the straight edge, using a sharp knife (Fig. 2).
Before carving, the surfaces of the wood were gently burned over
a gas burner to kill the surface mycelia. The wood pieces cut
Figure 2. Schematic figure showing the two sampling locations (round circles) on
each half of the test piece of wood from the disc formed from a pair of semicircles
each inoculated with competing species (A and B). Samples were collected ∼1 cm
(dotted line) from the cut edge.
from each semicircle were placed on 9 cm Petri dishes with 2%
MEA, and incubated in darkness at 20◦ C. The plates were regularly checked for 4 weeks and the outgrowing mycelia were identified to species by comparing their morphological characteristics with reference cultures of the same age. We mainly looked
at the texture and colour of the aerial mycelium, but in some
cases we also took samples for microscopic identification or did
chemical drop tests (KOH) on the aerial mycelium (e.g. Stalpers
1976). Given that only six species were studied, all with distinct
mycelial characteristics, species identification was straightforward and did not require DNA-based molecular identification.
Statistical analyses
We used ordinal logistic regression to compare the three possible outcomes (win, draw, loss) of fungal interactions on burnt
and unburnt wood. Each of the six fungal species was tested
against all the other species in separate tests, in which competitor species, treatment (burnt and unburnt control) and strain of
the test species were used as factors. Since the same strain combinations were replicated three times, they cannot be seen as
true independent replicates; we therefore used the average values in the analyses. All tests were performed with the statistical package ‘ordinal’ (Christensen 2013) using R 3.0.2 (R development core team 2013).
RESULTS
Temperature and wood moisture
The temperature inside the discs was on average 280◦ C (7.8 SD),
ranging between 273◦ C and 295◦ C, indicating a substantial influence of fire. There were also clear visual signs of the treatment:
the surfaces of the wood pieces were distinctly charred and the
inner parts discoloured by the heat (Fig. S2, Supporting Information). Furthermore, the bark was either wholly consumed or fell
off during the treatment.
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FEMS Microbiology Ecology, 2016, Vol. 92, No. 6
Figure 3. Outcomes of fungal interactions for each of the six species on burnt wood (B) and control wood (C). Species abbreviations are as follows: Antrodia sinuosa
(As), Antrodia xantha (Ax), Fomitopsis pinicola (Fp), Gloeophyllum sepiarium (Gs), Ischnoderma benzoinum (Ib) and Oligoporus sericeomollis (Os). Asterisks indicate significant
differences (logistic regression) between burnt wood and unburnt control wood (∗ ∗ ∗ ≤0.001).
The average MC (standard deviation in parentheses) in untreated and charred wood after 4 h in water was 78.8% (4.1 SD)
and 76.4% (6.0 SD), respectively, indicating that the fire treatment did not affect the water absorbing ability of the wood.
also the only species for which the competitive ability differed
between the three different strains (P = 0.008).
Fungal interactions
Previous laboratory studies have shown that some wooddecaying fungi have a remarkable ability to resist heat above
their growth optimum (Carlsson et al. 2012), and that heating
mimicking fire can alter the relative competitive strength between species already present in the wood (Carlsson et al. 2014).
Here we have shown that even the heated and charred wood per
se can alter the competitive outcome between fungal species establishing after the fire. Depending on the species identity, the
competitive ability increased, decreased or was unaffected on
charred wood, although the response sometimes differed depending on the identity of the competitor, indicating an interaction between competitor and substrate type. Thus, changes in
competitive strength after fire is not just an effect of differences
in heat tolerance of surviving mycelia, as shown in Carlsson et
al. (2014), but is also due to an effect of fire-mediated changes
in the wood’s properties. Fire-mediated changes in this case include both heated and charred wood, but since there is a gradual
change from heated to charred wood, their relative effects are
not easily distinguishable.
The effect of heating and charring of wood on fungi have
rarely been studied from an ecological perspective. However,
within the research field of wood preservation several studies
have shown that heat-treated wood is more resistant to decay
by fungi (Kamden, Pizzi and Jermannaud 2002; Weiland and Guyonnet 2003; Hakkou et al. 2006). For example, Kamden, Pizzi and
Jermannaud (2002) studied the decay by G. trabeum, Rhodonia placenta and Irpex lacteus and found that heat-treated pine wood
decayed 80%, 13% and 20% slower, respectively, than untreated
control wood. Thus, the effect of heating on fungal decay differs
between species, which also may be reflected in their competitive strength. Three hypotheses have been formulated to explain
the reason for increased decay resistance (Hakkou et al. 2006): (i)
the low affinity of heat-treated wood to water, (ii) the generation
of toxic compounds during heating and (iii) the chemical modification and degradation of the main wood polymers. Among
these, chemical modifications have been suggested as being the
most plausible explanation (Hakkou et al. 2006). Chemical modifications are also likely to underpin the results in the present
The outcomes of interactions differed between burnt wood and
the unburnt control wood for two of the six tested species. Antrodia sinuosa never lost on burnt wood and won over its competitor
in 67% of the trials compared to 40% losses and 20% wins on unburnt wood (z = 3.35, P < 0.001) (Fig. 3). In contrast, I. benzoinum
won all interactions on unburnt wood compared to 33% on burnt
wood (z = −4.42, P < 0.001). Although I. benzoinum was less competitive on burnt wood, it was usually able to defend its original
territory, resulting in deadlock in 67% of the interactions. When
ranked according to the number of wins, the species dominance
hierarchy on burnt wood was A. sinuosa > O. sericeomollis > G.
sepiarium > I. benzoinum > A. xantha > F. pinicola. The corresponding dominance hierarchy on unburnt wood was I. benzoinum > O.
sericeomollis > G. sepiarium > A. sinuosa > A. xantha > F. pinicola.
With the exception of A. sinuosa and I. benzoinum changing place,
the hierarchy was identical on both substrates.
The outcomes of interactions were dependent on the identity of the competitor for three of the species: I. benzoinum, A.
sinuosa and O. sericeomollis (Fig. 4). Ischnoderma benzoinum was
clearly less successful against A. sinuosa (z = 2.83, P < 0.01) and
O. sericeomollis (z = 3.47, P < 0.001), compared to its competitive ability against other species. This was, however, caused by
poorer competitive ability against those species on burnt wood
(Fig. 4). Antrodia sinuosa was less competitive against I. benzoinum
(z = 2.73, P < 0.01) relative to its competitive ability against other
species, which was caused by poor competitive ability on unburnt wood. In fact, I. benzoinum always outcompeted A. sinuosa
on unburnt wood. Still, A. sinuosa was the most successful competitor against I. benzoinum, due to its strong competitive ability
on burnt wood. Another interesting observation was that A. sinuosa efficiently replaced the common generalist species F. pinicola on burnt wood, but usually lost or deadlocked on unburnt
wood. Oligoporus sericeomollis was less successful against A. sinuosa, G. sepiarium and I. benzoinum compared to its success against
A. xantha and F. pinicola (P < 0.01), a pattern that was fairly similar between the treatments (Fig. 4). Oligoporus sericeomollis was
DISCUSSION
Edman and Eriksson
5
Figure 4. Outcomes of interactions between species on burnt (B) and unburnt control wood (C) expressed as percentage of each species’ wins (dark grey), draws (light
grey) and losses (white) against the different competitors. Abbreviations are same as in Fig. 3.
study since MC did not differ between the treatments. An important chemical modification is the degradation of hemicellulose,
which is an important and fairly easily accessible energy source
for fungi (Weiland and Guyonnet 2003). This happens already at
temperatures as low as 180◦ C (Kollmann and Fengel 1965), which
was clearly exceeded in the present study. Further, at the maximum temperature reached in the discs (273◦ C–295◦ C) derivatives
of extractives, hemicelluloses, cellulose and lignin are generated
(e.g. Kamden, Pizzi and Jermannaud 2002). These chemical modifications may have affected the studied species differently, with
consequences for the interaction outcomes.
Although decomposition was not studied in the present
study, we visually observed that the growth rate of surface
mycelia was generally slower on burnt wood. In addition, the
mycelia of especially F. pinicola, O. sericeomollis and A. xantha,
were clearly less dense compared to on unburnt wood. However,
the burnt wood was only charred on the surface why our study
is not really comparable to those investigating more completely
charred wood. Pure char has been shown to have a strongly inhibiting effect on fungal growth and decay in laboratory studies. Ascough, Sturrock and Bird (2010) showed that both Coriolus
versicolor and Pleurotus pulmonarius were able to grow on the surface and in cracks of charred wood blocks, but they were unable
to decompose them. Similarly, Kymäläinen et al. (2014) studied
the decomposition of pyrolized wood by G. sepiarium and Pycnoporus cinnabarinus, two species that are often found on charred
wood after forest fire. In agreement with our observations they
found that the fungi were able to colonize char but in most cases
the amount of fungal hyphae was moderate and the growth was
slow. Furthermore, they found that an increased pyrolysis temperature affected fungal growth negatively. However, Wengel et
al. (2006) investigated the decomposition of char by the basidiomycete fungus Schizophyllum commune and found that it was
indeed able to degrade it, but only at a very low rate.
Charred wood is a unique substrate that can only be created
naturally by forest fire. Eriksson et al. (2013) measured charred
logs after restoration fire and found that fire increased the mean
proportion of charred surface area on logs by as much as 60%
or more. Inventories of fruiting bodies have shown that some
species fructify more frequently on charred surfaces. For example, both Olsson and Jonsson (2010) and Penttilä et al. (2013) have
found that A. sinuosa, which was the strongest competitor on
burnt wood in our study, increases on charred dead wood after restoration fire. Further, O. sericeomollis, which was the second best competitor on burnt wood, has also been observed
to fructify frequently on charred wood (Niemelä 2005; Zhou
and Dai 2012). However, in natural charred logs some properties not accounted for in the present study are also likely to be
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FEMS Microbiology Ecology, 2016, Vol. 92, No. 6
important to certain fungal species. The black wood surface has
a very low albedo resulting in an increased temperature and
higher water evaporation, which should benefit drought resistant species and species with high temperature optima. Further, in natural charred logs, and in our wood-discs, a gradient
from heated to completely charred wood is represented, so the
specific effect of char is unknown. Given that different fungal
species apparently have different abilities to utilize char as a
resource, the extent of charring may still have contributed to
our observed results. Nevertheless, we present evidence that
some fungal species have a competitive advantage in charred
and heated wood, supporting the observed incidence patterns
of fruit bodies on charred logs.
CONCLUSION
Fire, once the dominant disturbance in boreal forests, creates
a wide array of unique woody substrates (Eriksson et al. 2013).
Our knowledge concerning the importance of these substrates
to wood-decaying fungi is, however, still poor, although field
inventories have found higher prevalence of certain species in
fire areas and on burnt wood (Renvall 1995; Penttilä and Kotiranta 1996; Junninen, Kouki and Renvall 2007; Olsson and Jonsson 2010; Penttilä et al. 2013; Suominen et al. 2015). Here we
have shown that the outcomes of competitive interactions between wood-decaying fungi differ in burnt and unburnt wood,
probably reflecting chemical changes in the wood caused by the
fire. The results indicate the important role of forest fire in indirectly structuring fungal communities, and highlight the importance of fire-affected dead wood substrates in boreal forests.
Our study represents the fungal establishment and competition on burnt fresh wood, but during a forest fire under natural conditions a variety of wood decomposition stages will be
affected. However, the chemical changes in fresh and decayed
wood are probably different, and the fungal species community
also changes along with the decomposition. To advance our understanding of the effects of heat-modified and charred wood
on fungal interactions, we propose future studies to investigate
the chemical modifications that occur in wood at different degrees of decay when it is burnt, and to relate such modifications
to fungal interactions and fungal development within wood. We
also suggest that future experimental work should be done under field conditions where the variety of factors that may influence fungal interactions under natural conditions might also be
included.
SUPPLEMENTARY DATA
Supplementary data are available at FEMSEC online.
ACKNOWLEDGEMENTS
We thank Ida Fällström for much appreciated lab assistance
and Bengt Gunnar Jonsson, Anders Dahlberg and two anonymous reviewers for valuable comments on an earlier draft of this
manuscript.
FUNDING
This work was supported by The Swedish Research Council FORMAS (2008-1590 to ME).
Conflict of interest. None declared.
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