Competitive Outcomes Between Wood-Decaying Fungi Are Altered in Burnt Wood Mattias Edman and Anna-Maria Eriksson∗

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 forest structure after fire, such as a more open canopy andan altered composition of dead wood. For example, more than 40% In boreal forests, fire plays an important role as a disturbance of the pre-fire dead wood was consumed in controlled restora- agent. Historically, it has affected such a major part of the tion burnings in Swedish Scots pine (Pinus sylvestris L.) forests, landscape (Zackrisson 1977; Johnson, Miyanishi and Weir 1998; where logs in the late stages of decay were consumed to a much Niklasson and Granstrom¨ 2000) that many forest species, in- higher extent than those in earlier stages of decay (Eriksson et cluding fungi, have adapted to fire disturbance (Granstrom¨ and al. 2013). However, due to a high input of standing fire-killed Schimmel 1993; Penttila¨ and Kotiranta 1996; Hyvarinen,¨ Kouki trees, fires generally cause a net increase in dead wood (Siitonen and Martikainen 2006). Several studies have shown that the 2001; Eriksson et al. 2013). In addition to the structural changes, species composition of wood-decaying fungi is altered after fire, fire also creates unique dead wood substrates, such as burnt and some species seem to be more or less confined to forests and charred wood, which are usually abundant after forest fires that have been affected by fire (Penttila¨ and Kotiranta 1996; Jun- (Eriksson et al. 2013). The influence of these substrates on fun- ninen, Kouki and Renvall 2007; Berglund et al. 2010; Olsson and gal community structure and development within wood is, how- Jonsson 2010; Suominen et al. 2015). The mechanisms behind ever, poorly understood. these community changes are largely attributed to changes in

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Competition is a fundamental process in structuring species allowed six species of wood-decaying basidiomycetes to com- communities. For fungi restricted to a transient resource unit pete in pairs in experimentally burnt wood-discs and unburnt such as dead wood, competition for space and associated re- control discs in microcosms. Specifically, we hypothesized that sources is usually very intense (Boddy 2000). The outcomes of (i) burnt wood alters the competitive outcome of fungal interac- these interactions are largely determined by the species’ com- tions and (ii) the outcomes of interactions are species-specific. petitive ability, but the competitive balance may shift between fungal competitors depending on priority effects (i.e. the order of METHODS species arrival) or the particular abiotic and biotic circumstances (e.g. Fukami et al. 2010). Temperature, moisture, wood proper- Wood material and preparation ties, mycelial size and invertebrate grazing may all influence Three healthy 8 cm base diameter trees of Scots pine (P.sylvestris) competitive outcomes between saprotrophic fungi (Holmer and were harvested in plantations close to Sundsvall in the middle Stenlid 1993; Boddy 2000; Toljander et al. 2006; Crowther, Boddy boreal zone of Sweden. All trees had regenerated at the same and Jones 2011; Edman and Fallstr¨ om¨ 2013). Forest fire may also time after clear-cut harvest. Logs were machined into 1 cm thick, influence fungal interactions. Carlsson et al.(2012) found that 7.0–7.4 cm diameter discs and dried at 30◦C for 6 days in a heat- wood-decaying fungi prevalent in forests characterized by fire ing cabinet. In order to mimic the effect of forest fire, half of the were more resistant to heat, and more successful in competitive wood-pieces were then burnt, one by one, for 2 min using a bu- interactions in wood compared to non-fire associated species tane burner. After about 1.5 min over the gas flame the discs after heating of the wood and fungi to about 56◦C (Carlsson et caught fire and were allowed to burn for ∼30 s before being extin- al. 2014). Still, many mycelia are killed by the fire, which, by va- guished by dropping in water. The temperature inside the discs cating habitat in the heated and charred wood, can allow other after burning was measured on a separate set of 10 discs, which species to establish. were pre-drilled with a 3.5 cm long 1.5 mm diameter hole from The heated and charred wood created by the fire thus pro- the outer bark surface into the core. Instead of dropping these vides new space for fungi to colonize, either through the ex- discs in water, a thin temperature probe connected to a Tinytag tension of surviving mycelia in wood or soil, or by germinating logger was inserted into the pre-drilled hole immediately after spores. However, it is possible that the fire indirectly influences the flame was extinguished by being blown out. different species’ competitiveness and thus the developing fun- All wood-discs to be used in the competition experiment gal community in this new resource. When strongly heated, the were then split across the middle into two equal-sized halves properties of the wood are altered. This is well researched within (semicircles) and sterilized by gamma irradiation at a dosage of the field of wood preservation where heat treatment is usedto 25 kGy (by Isotron Nederland B.V.). Finally, since the discs had slow down the decay process and extend the life of commer- been dried they were soaked in autoclaved, distilled water for 4 cial wood products (Esteves and Pereira 2009). Heat treatment al- h prior to experimental use. To test how the fire treatment af- ters the chemical composition of the wood by degrading cell wall fected the water absorbing ability of the wood we calculated the compounds and extractives (Esteves and Pereira 2009). At 180◦C moisture content (MC) of a subset of 20 treated and 20 untreated –250◦C, the temperature range commonly used for heat treat- discs after having been soaked in water by ments, wood undergoes important chemical changes. Hemicel- lulose and extractives, especially the volatile ones, are degraded or disappear while cellulose and lignin are less affected. How- wet weight − oven dry weight MC = × 100 ever, even lignin and cellulose undergo structural changes when oven dry weight 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 Fungi combustion is inhibited by low oxygen availability (pyrolysis), charring processes start. (Esteves and Pereira 2009). Char is not We used six species of wood-decaying fungi, all of which are a discrete substance but represents a continuum of structures common early- to mid-succession decayers on dead Scots pine with different chemical and physical properties (Czimczik et al. and Norway spruce wood in Fennoscandia (Niemela¨ 2005): Antro- 2002). dia sinuosa ((Fr.) P. Karst.), A. xantha ((Fr.:Fr.) Ryvarden), Fomitop- Given that forest fire has probably been an important factor sis pinicola ((Sw.:Fr.) P. Karst.), Gloeophyllum sepiarium (Wulfen: in shaping boreal forests during the evolution of wood-decaying Fr.), Ischnoderma benzoinum ((Wahlenb.:Fr.) P. Karst.), Oligoporus fungi, some species are likely to have adapted to the unique sericeomollis ((Romell) Bondartseva) (Mid Sweden University Fun- types of dead wood it creates. For example, observations of fruit- gal Collection). Observations of sporocarps indicate that all in- ing bodies suggest an increased prevalence of certain species on cluded species can occur together on the same substrate under charred wood, including some rare and threatened species (Ren- natural conditions (Olsson and Jonsson 2010). Antrodia sinuosa, A. vall 1995; Niemela¨ 2005; Olsson and Jonsson 2010; Zhou and Dai xantha and O. sericeomollis are frequently found on pine logs that 2012). Information on how fire-affected wood influences fungi is have been influenced by forest fire (Olsson and Jonsson 2010; therefore important, not least in light of the fact that these sub- Zhou and Dai 2012; Penttila¨ et al. 2013) while the other species strates have become increasingly rare in Fennoscandian boreal show no such clear association although they do occasionally forest due to increasingly efficient fire prevention since more occur on burnt wood substrates after fire. In addition, based on than a century ago. Further, controlled forest fire is increas- our previous laboratory experience, these species are easy to cul- ingly used as a method to recreate fire-characterized forests and tivate and to recognize in pure culture. Three strains of each associated dead wood in the Nordic countries, and knowledge species were used. The fungi were sub-cultured in vented 15 cm on how fungi are influenced by fire is therefore needed. Inthe diameter Petri dishes with 2% malt extract agar (MEA). Prior to present study we experimentally tested the indirect effect of experimental use the semicircular pieces of wood were added to fire in structuring fungal communities by examining how wood, 2-week-old fungal cultures and incubated in a closed cabinet at modified by fire, influences competitive fungal interactions. We a temperature of 20◦Cfor8weeksuntilallpiecesofwoodwere 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.

Figure 2. Schematic figure showing the two sampling locations (round circles) on completely colonized. The inoculation was randomized with re- each half of the test piece of wood from the disc formed from a pair of semicircles gard to the different individual trees from which the discs were each inoculated with competing species (A and B). Samples were collected ∼1cm made. (dotted line) from the cut edge.

Experimental setup from each semicircle were placed on 9 cm Petri dishes with 2% MEA, and incubated in darkness at 20◦C. The plates were regu- The fungus-colonized semicircular pieces of wood were put to- larly checked for 4 weeks and the outgrowing mycelia were iden- gether, two by two, with the cut sides in full contact, in vented tified to species by comparing their morphological characteris- Petri dishes (100 × 20 mm) with water agar. All possible pairs of tics with reference cultures of the same age. We mainly looked species were allowed to compete with each other, resulting in at the texture and colour of the aerial mycelium, but in some 15 trials. This was repeated for the three strains, where strain cases we also took samples for microscopic identification or did 1 of species 1 was combined with strain 1 of each of the other chemical drop tests (KOH) on the aerial mycelium (e.g. Stalpers species, strain 2 of species 1 was combined with strain 2 of 1976). Given that only six species were studied, all with distinct the other species etc., resulting in 45 trials for each treatment mycelial characteristics, species identification was straightfor- (burnt and control). This setup, which avoids dependence based ward and did not require DNA-based molecular identification. 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. Statistical analyses We used ordinal logistic regression to compare the three possi- Determining interaction outcomes ble outcomes (win, draw, loss) of fungal interactions on burnt and unburnt wood. Each of the six fungal species was tested We applied a slightly modified version of the classification used against all the other species in separate tests, in which competi- by Crowther, Boddy and Jones (2011) to judge interaction out- tor species, treatment (burnt and unburnt control) and strain of comes: (i) overgrowth, where one fungus had grown over an- the test species were used as factors. Since the same strain com- other without killing its competitor; (ii) replacement, where binations were replicated three times, they cannot be seen as mycelia of one fungus was killed and replaced by its competi- true independent replicates; we therefore used the average val- tor; (iii) mutual replacement, where mycelia from both fungi had ues in the analyses. All tests were performed with the statisti- grown into each other’s domain and (iv) deadlock, where nei- cal package ‘ordinal’ (Christensen 2013) using R 3.0.2 (R develop- ther fungus had gained territory of the other. Overgrowth and ment core team 2013). replacement were recorded as being a ‘win’ if the aggressor had reached at least 1 cm into its competitor’s semicircle, represent- ing roughly 30% of its domain (Fig. 2, Fig. S1, Supporting Infor- RESULTS mation). Mutual replacement was recorded as a ‘draw’ if neither Temperature and wood moisture species had advanced 1 cm into its competitor’s semicircular domain. Likewise, deadlock was recorded as a ‘draw’. The temperature inside the discs was on average 280◦C(7.8SD), To determine the interaction outcome of each trial we iden- ranging between 273◦C and 295◦C, indicating a substantial influ- tified the mycelia within each piece of wood. Two small wood ence of fire. There were also clear visual signs of the treatment: samples, each 0.5 cm diameter, were carved out from each semi- the surfaces of the wood pieces were distinctly charred and the circle, 1 cm from the straight edge, using a sharp knife (Fig. 2). inner parts discoloured by the heat (Fig. S2, Supporting Informa- Before carving, the surfaces of the wood were gently burned over tion). Furthermore, the bark was either wholly consumed or fell a gas burner to kill the surface mycelia. The wood pieces cut off during the treatment. 4 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 un- also the only species for which the competitive ability differed treated and charred wood after 4 h in water was 78.8% (4.1 SD) between the three different strains (P = 0.008). and 76.4% (6.0 SD), respectively, indicating that the fire treatment did not affect the water absorbing ability of the wood. DISCUSSION

Fungal interactions Previous laboratory studies have shown that some wood- decaying fungi have a remarkable ability to resist heat above The outcomes of interactions differed between burnt wood and their growth optimum (Carlsson et al. 2012), and that heating the unburnt control wood for two of the six tested species. Antro- mimicking fire can alter the relative competitive strength be- dia sinuosa never lost on burnt wood and won over its competitor tween species already present in the wood (Carlsson et al. 2014). in 67% of the trials compared to 40% losses and 20% wins on un- Here we have shown that even the heated and charred wood per burnt wood (z = 3.35, P < 0.001) (Fig. 3). In contrast, I. benzoinum se can alter the competitive outcome between fungal species es- won all interactions on unburnt wood compared to 33% on burnt tablishing after the fire. Depending on the species identity, the wood (z =−4.42, P < 0.001). Although I. benzoinum waslesscom- competitive ability increased, decreased or was unaffected on petitive on burnt wood, it was usually able to defend its original charred wood, although the response sometimes differed de- territory, resulting in deadlock in 67% of the interactions. When pending on the identity of the competitor, indicating an interac- ranked according to the number of wins, the species dominance tion between competitor and substrate type. Thus, changes in hierarchy on burnt wood was A. sinuosa > O. sericeomollis > G. competitive strength after fire is not just an effect of differences sepiarium > I. benzoinum > A. xantha > F. pinicola. The correspond- in heat tolerance of surviving mycelia, as shown in Carlsson et ing dominance hierarchy on unburnt wood was I. benzoinum > O. al.(2014), but is also due to an effect of fire-mediated changes sericeomollis > G. sepiarium > A. sinuosa > A. xantha > F. pinicola. in the wood’s properties. Fire-mediated changes in this case in- With the exception of A. sinuosa and I. benzoinum changing place, clude both heated and charred wood, but since there is a gradual the hierarchy was identical on both substrates. change from heated to charred wood, their relative effects are The outcomes of interactions were dependent on the iden- not easily distinguishable. tity of the competitor for three of the species: I. benzoinum, A. The effect of heating and charring of wood on fungi have sinuosa and O. sericeomollis (Fig. 4). Ischnoderma benzoinum was rarely been studied from an ecological perspective. However, clearly less successful against A. sinuosa (z = 2.83, P < 0.01) and within the research field of wood preservation several studies O. sericeomollis (z = 3.47, P < 0.001), compared to its competi- have shown that heat-treated wood is more resistant to decay tive ability against other species. This was, however, caused by by fungi (Kamden, Pizzi and Jermannaud 2002; Weiland and Guy- poorer competitive ability against those species on burnt wood onnet 2003; Hakkou et al. 2006). For example, Kamden, Pizzi and (Fig. 4). Antrodia sinuosa was less competitive against I. benzoinum Jermannaud (2002) studied the decay by G. trabeum, Rhodonia pla- (z = 2.73, P < 0.01) relative to its competitive ability against other centa and Irpex lacteus and found that heat-treated pine wood species, which was caused by poor competitive ability on un- decayed 80%, 13% and 20% slower, respectively, than untreated burnt wood. In fact, I. benzoinum always outcompeted A. sinuosa control wood. Thus, the effect of heating on fungal decay differs on unburnt wood. Still, A. sinuosa was the most successful com- between species, which also may be reflected in their competi- petitor against I. benzoinum, due to its strong competitive ability tive strength. Three hypotheses have been formulated to explain on burnt wood. Another interesting observation was that A. sin- the reason for increased decay resistance (Hakkou et al. 2006): (i) uosa efficiently replaced the common generalist species F. pini- the low affinity of heat-treated wood to water, (ii) the generation cola on burnt wood, but usually lost or deadlocked on unburnt of toxic compounds during heating and (iii) the chemical mod- wood. Oligoporus sericeomollis was less successful against A. sinu- ification and degradation of the main wood polymers. Among osa, G. sepiarium and I. benzoinum compared to its success against these, chemical modifications have been suggested as being the A. xantha and F. pinicola (P < 0.01), a pattern that was fairly sim- most plausible explanation (Hakkou et al. 2006). Chemical mod- ilar between the treatments (Fig. 4). Oligoporus sericeomollis was ifications are also likely to underpin the results in the present 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 impor- the decomposition of pyrolized wood by G. sepiarium and Pycno- tant chemical modification is the degradation of hemicellulose, porus cinnabarinus, two species that are often found on charred which is an important and fairly easily accessible energy source wood after forest fire. In agreement with our observations they for fungi (Weiland and Guyonnet 2003). This happens already at found that the fungi were able to colonize char but in most cases temperatures as low as 180◦C (Kollmann and Fengel 1965), which the amount of fungal hyphae was moderate and the growth was was clearly exceeded in the present study. Further, at the maxi- slow. Furthermore, they found that an increased pyrolysis tem- mum temperature reached in the discs (273◦C–295◦C) derivatives perature affected fungal growth negatively. However, Wengel et of extractives, hemicelluloses, cellulose and lignin are generated al.(2006) investigated the decomposition of char by the basid- (e.g. Kamden, Pizzi and Jermannaud 2002). These chemical mod- iomycete fungus Schizophyllum commune andfoundthatitwas ifications may have affected the studied species differently, with indeed able to degrade it, but only at a very low rate. consequences for the interaction outcomes. Charred wood is a unique substrate that can only be created Although decomposition was not studied in the present naturally by forest fire. Eriksson et al.(2013) measured charred study, we visually observed that the growth rate of surface logs after restoration fire and found that fire increased themean mycelia was generally slower on burnt wood. In addition, the proportion of charred surface area on logs by as much as 60% mycelia of especially F. pinicola, O. sericeomollis and A. xantha, or more. Inventories of fruiting bodies have shown that some were clearly less dense compared to on unburnt wood. However, species fructify more frequently on charred surfaces. For exam- the burnt wood was only charred on the surface why our study ple, both Olsson and Jonsson (2010) and Penttila¨ et al.(2013)have is not really comparable to those investigating more completely found that A. sinuosa, which was the strongest competitor on charred wood. Pure char has been shown to have a strongly in- burnt wood in our study, increases on charred dead wood af- hibiting effect on fungal growth and decay in laboratory stud- ter restoration fire. Further, O. sericeomollis, which was the sec- ies. Ascough, Sturrock and Bird (2010) showed that both Coriolus ond best competitor on burnt wood, has also been observed versicolor and Pleurotus pulmonarius were able to grow on the sur- to fructify frequently on charred wood (Niemela¨ 2005;Zhou face and in cracks of charred wood blocks, but they were unable and Dai 2012). However, in natural charred logs some proper- to decompose them. Similarly, Kymal¨ ainen¨ et al.(2014) studied ties not accounted for in the present study are also likely to be 6 FEMS Microbiology Ecology, 2016, Vol. 92, No. 6

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