Abundance and diversity of wood-decay fungi in managed and unmanaged stands in a Scots pine forest in western Poland

Forest Ecology and Management 400 (2017) 438–446

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Abundance and diversity of wood-decay fungi in managed and unmanaged stands in a Scots pine forest in western Poland Hanna Kwas´na a,⇑, Andrzej Mazur b, Robert Kuz´min´ski b, Roman Jaszczak c, Mieczysław Turski c, Jolanta Behnke-Borowczyk a, Krzysztof Adamowicz d, Piotr Łakomy a a

´ University of Life Sciences, Wojska Polskiego 71c, 60-625 Poznan ´ , Poland Department of Forest Pathology, Poznan ´ University of Life Sciences, Wojska Polskiego 71c, 60-625 Poznan ´ , Poland Department of Forest Entomology, Poznan ´ University of Life Sciences, Wojska Polskiego 71c, 60-625 Poznan ´ , Poland Department of Forest Management, Poznan d ´ University of Life Sciences, Wojska Polskiego 71c, 60-625 Poznan ´ , Poland Department of Forest Economics, Poznan b c

a r t i c l e

i n f o

Article history: Received 30 January 2017 Accepted 17 April 2017

Keywords: Coarse woody debris Fungi Managed forest Pinus sylvestris

a b s t r a c t Abundance and diversity of wood-inhabiting fungi were studied in managed (sanitation cutting, commercial thinning and timber harvesting) and unmanaged stands in one 85-year-old Scots pine forest in western Poland. Fungi were detected on coarse woody debris collected in each stand in June 2014: logs, fallen branches, standing dead trees and stumps, in the 1st, 2nd and 3rd classes of decay. Fungi were identified after culturing on synthetic media or as fruit bodies. One taxon of Oomycota and 140 taxa of cultured fungi (19 Zygomycota, 108 Ascomycota and 13 Basidiomycota species) were detected in 34 samples of deadwood. Fruit bodies of three species of Ascomycota and 14 species of Basidiomycota were recorded on 33.8% of coarse woody debris in the managed stand and on 20.6% in the unmanaged stand, with 10 species and 15 species in the respective stands. Abundance of cultured fungi was greater and diversity smaller, both non-significantly, in the managed stand. Eighty-six cultured species (55%) occurred in both stands, while 32 (20%) and 39 (25%) species occurred exclusively in, respectively, the managed and unmanaged stands. Communities in different transects within a stand tended to be more similar than communities in different stands, managed and unmanaged. Logs hosted the greatest number of species. Abundance of cultured fungi increased and diversity decreased in more decayed wood. Known wood-decay species were most abundant in the less decayed wood. Ó 2017 Elsevier B.V. All rights reserved.

1. Introduction Wood-inhabiting fungi have been studied in temperate and boreal ecosystems (Greslebin and Rajchenberg, 2003; Dai et al., 2004; Afyon et al., 2005; Jönsson et al., 2008; Stokland and Larsson, 2011; Brazee et al., 2012, 2014) and in warm mixed and tropical forests (Ortega and Navarro, 2004). Most studies included polyporoid and corticoid fungal species. Only rarely have studies included microfungi, which also play a significant role in wood decomposition (Lumley et al., 2001; Fukasawa et al., 2005, 2011; Kwas´na et al., 2016). Forest management practices provide variable amounts of deadwood and create different microclimates with various chemical and physical conditions in the habitat (with horizontal and vertical gradients). They affect the abundance and diversity of fungi (Küffer and Senn-Irlet, 2005; Ódor et al., 2006; Brazee et al., 2014). ⇑ Corresponding author. E-mail address: [email protected] (H. Kwas´na). http://dx.doi.org/10.1016/j.foreco.2017.04.023 0378-1127/Ó 2017 Elsevier B.V. All rights reserved.

Wood-inhabiting fungi respond to forest management differently in different habitats. Pine-associated species are more flexible and adaptable to new conditions than are spruce-associated species (Stokland and Larsson, 2011). Diverse microhabitats support not only a vast variety of common fungi but also more or less specialized species. Paillet et al. (2009) showed that the increasing abundance of microhabitats in unmanaged forests significantly increased the diversity of wood-inhabiting fungi compared with managed forests. The number of fungi involved in wood decay is unknown. The percentage of fungal species dependent on deadwood is approximately 20–40% of the estimated 1.5 million fungal species worldwide (Siitonen, 2001; Penttilä et al., 2004). More than 2000 species of wood-inhabiting fungi are known from the Nordic countries (Stokland and Meyke, 2008). In Europe, intensive harvesting and utilization of dying or uprooted trees has reduced the quantity and quality of wood debris, which has led to a reduction in the abundance and diversity of wood-inhabiting fungi, including rare species

H. Kwas´na et al. / Forest Ecology and Management 400 (2017) 438–446

(Heilmann-Clausen and Christensen, 2005; Abrego and Salcedo, 2013; Halme et al., 2013). In Poland there is considerable utilization of dying trees, resulting in less deadwood on the forest floor than in most other EU countries. With an average of 5.7 m3 (0–298 m3) per ha of standing and lying deadwood (Czerepko et al., 2008) Poland ranks fourth lowest among EU countries (Anonymous, 2013). There is more deadwood (35% of the total volume) in the national parks than elsewhere. The aims of this study were: (i) to determine the effects of management practices in mature Scots pine forest on the occurrence (abundance and diversity) of wood-inhabiting fungi; (ii) to characterize the wood-inhabiting fungal communities according to specific wood attributes, i.e. species of wood, character of substrate including logs, fallen branches, standing dead trees and stumps, size of sample and class of wood decay; (iii) to detect the common and rare fungal species present in/on deadwood, in a single representative Scots pine forest in western Poland. The hypothesis that forest management in Scots pine forest leads to decreased abundance and diversity of fungi, because of less available deadwood, is tested. 2. Materials and methods 2.1. Site and sampling Samples were collected in June 2014 from two stands (fully managed 263 and unmanaged 264) in mixed forest in Torzym Forest District, Poland (52.31N, 15.08E). Both stands consisted of 85year-old Scots pine (Pinus sylvstris L.) with admixture of 41–85year-old silver birch (Betula pendula Roth.), 85-year-old black locust (Robinia pseudoacacia L.) and 85-year-old spruce (Picea abies (L.) H. Karst.), with Scots pine, spruce, oak (Quercus petraea (Mattuschka) Liebl.) and beech (Fagus sylvatica L.) in the understorey. The shrub and herb layers included Agrostis stolonifera L., Calluna vulgaris (L.) Hull, Convallaria majalis L., Corylus avellana L. (common hazel), Corynephorus canescens (L.) P. Beauv., Galium odoratum (L.) Scopoli, Hepatica nobilis Mill., Poa pratensis L., Polypodium vulgare L., Polytrichum commune Hedw. and Vaccinium myrtillus L. Practices in the managed stand included sanitation cutting in 1999, 2000 and 2001, and commercial thinning and timber harvesting in July 2013. Characteristics of the forest stands are in Table 1. Coarse woody debris (CWD) of Scots pine sampled for analysis included logs (20
20
20 cm sample unit), fallen branches (20–30 cm long, 5–20 cm wide), standing dead trees (30
20
20 cm sample unit) and decayed stumps (top ring 20– 30 cm and 10-cm thick). In each stand, the samples of wood were collected along four transects (each 700
10 m = 7000 m2) located 50 m apart; the first was chosen randomly. The four transects, with a total area of 2.8 ha, were 10% of the area of the stand. All logs and stumps within transects, including those at the edges, were counted and measured. The volume of the timber of standing Scots pine trees was calculated according to the formula:  4 p  d21:3 1 d1:3  6 v7 ¼ h  4  40000 0:2834 þ 0:988  ðd1:3  6Þ d1:3 1 þ 1:2895þ0:90645d 1:3 where d1.3 is a diameter at breast height and h is the tree’s height. That of birch was calculated according to the formula

439

The volume of the logs was calculated according to Huber’s formula

v¼

p  d21=2 40000

l

where d1/2 is the diameter of the log at its mid-point and l is its length. In total, there were 34 samples collected for isolation of fungi: 16 from the managed stand and 18 from the unmanaged stand, in proportion to the amount of deadwood present. Three, 7 and 6 samples (managed stand) and 7, 8 and 3 samples (unmanaged stand) were collected from each type of debris, i.e. logs, fallen branches and decayed stumps, in proportion to their amounts in the stand. Five, seven and four samples from the managed stand were in, respectively, the 1st, 2nd and 3rd decay classes; four, 11 and three samples from the unmanaged stand were in the 1st, 2nd and 3rd decay classes. Wood in the 1st decay class (1–3 years after felling) was sound, with intact structure and original colour, and the bark was intact. In the 2nd class (5–20 years after felling), the wood was moderately soft, its colour had visibly changed, smaller or larger patches or rings were rotted, especially in the outer layers, and the bark had partially fallen off. In the 3rd class (20–30 years after felling) the wood was soft, its colour had already changed, the core was often still solid, the outer layers disintegrated (knife test), and bark was absent. The percentages of wood in the 1st, 2nd and 3rd decay classes in the managed and unmanaged stands are shown in Table 1. 2.2. Species identification of fungi after mycelial isolation On the day after collection, samples were sterilized by flaming after removal of the bark. Thirty-six inocula (0.5 cm3 wood pieces) from each sample, taken at 2–3 cm depth from six evenly distributed places, were put on potato dextrose agar (PDA; 39 g Difco PDA l1, pH 5.5) and synthetic nutrient agar (SNA; KH2PO4 1 g l1, KNO3 1 g l1, MgSO47H2O 0.5 g l1, KCl 0.5 g l1, glucose 0.2 g l1, sucrose 0.2 g l1, agar 20 g l1). After incubation for 20 days at 25 °C all colonies were examined macro- and microscopically and pre-identified on the basis of growth rate, colour, hyphal characteristics and sporulation. Colonies of each species were counted and representatives were identified on the basis of morphology on PDA, SNA, Czapek yeast autolysate agar (CYA; sucrose 30 g l1, powdered yeast extract 5 g l1, KH2PO4 1 g l1, Czapek concentrate 10 ml l1, agar 15 g l1) and 2% malt extract agar (MEA; powdered malt extract 20 g l1, glucose 20 g l1, peptone 1 g l1, agar 20 g l1). Identification was made mainly according to Domsch et al. (1980), Pitt (1979) and Seifert et al. (2011), and fungal taxonomy was updated according to the CBS Fungal Biodiversity Centre nomenclature. All the fruit-body specimens and isolates are preserved in the Department of Forest Pathology, Poznan´ University of Life Sciences. Abundance, measured as numbers of isolates per sample or inoculum, and diversity, measured as numbers of species per sample or inoculum, were calculated for managed and unmanaged stands and for the three classes of decay.

v 7 ¼ eaþbþc

2.3. Fruit body identification

where

In June 2014, all logs, fallen branches, standing dead trees (<2 m tall) and stumps in each stand were examined for fruit bodies of Ascomycota (conidiomata and ascomata) and Basidiomycota (agarics, brackets and corals). Fungus species, character of substrate and class of decay were recorded. Initial identifications of fungi in the forest were confirmed by microscopic analysis of morphological

2

a ¼ 14:3682  1:22276  d1:3  0:002013  d1:3 , b ¼ lnðd1:3 Þ  ð6:07179 ¼ 0:27433  d1:3  0:005024  hÞ, c ¼ 1:3424  lnðhÞ, e = Euler number.

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H. Kwas´na et al. / Forest Ecology and Management 400 (2017) 438–446

Table 1 Characteristics of forest stands. Characteristic

Managed

Unmanaged

Stand area (ha) Soil type History Ground-cover plant Number of trees per ha Tree density Number of living Scots pine:birch per ha Timber volume ratio of Scots pine:birch Average diameter of pine breast height (cm) Average height of pine (m) Average standing timber volume per one pine tree (m3) Standing timber volume of pine per ha (m3) Standing timber volume of all trees per ha (m3)

41.01 Rusty podsolic formed on sand Post-agricultural Moss 380 0.9 362:10 98:2 33.18 26.59 1.08 388.79 395.74

35.78

620 1.0 549:27 95:5 26.68 24.86 0.68 443.10 466.81

Logs Number of Scots pine:birch per ha Average wood volume per one log (m3) Wood volume of pine per ha (m3) Wood volume of all logs per ha (m3)

100:8 0.01 0.97 1.67

121:5 0.1 14.29 14.49

Standing dead trees Number of Scots pine:birch per ha Average wood volume per one tree (m3) Wood volume of pines per ha (m3) Wood volume of all trees per ha (m3)

8:0 0.76 5.85 5.85

43: 1 0.21 8.89 8.94

Stumps Number of decayed stumps

129

62

Percentage of wood in the 1st, 2nd and 3rd decay classes Scots pine logs Stumps

1st

2nd

3rd

1st

2nd

3rd

16.17 7.5

26.95 40.3

14.97 52.2

47.95 1.6

21.73 12.9

28.97 85.5

features of fruit bodies in the laboratory and morphology of colonies on artificial media.

2.4. Molecular analysis Representative isolates of nine species with sparse and noninformative or absent sporulation were selected for DNA sequencing. Extraction of the total genomic fungal DNA was performed with the Qiagen DNeasy Plant Mini Kit (Qiagen Inc., Valencia, California). Fungal DNA was diluted in TE buffer (10 mM Tris-HCl; 1 mM EDTA) to a concentration of 25 ng ll1 and stored at 20 °C. The ITS 1/2 rDNA region was amplified with primers ITS 4 (50 TCC TCC GCT TAT TGA TAT GC) and ITS 5 (50 GGA AGT AAA AGT CGT AAC AAG G) (White et al., 1990). Each 25-ml PCR mixture consisted of 0.2 mM of each primer, 0.25 U of Taq polymerase (MBI Fermentas, St. Leon-Rot, Germany), buffer (10 mM Tris–HCl pH 8.8, 50 mM KCl, 0.08% Nonidet P–40, 0.1 mg ml1 BSA, 1.5 mM MgCl2), 0.2 mM deoxyribonucleoside triphosphates (dNTPs) and 2 ml (200 ng) diluted total DNA. Amplification conditions were: an initial denaturation at 94 °C for 10 min, followed by 30 cycles of 94 °C for 30 s, 42 °C for 1 min and 72 °C for 2 min, and a final extension of 72 °C for 10 min. The PCR products were checked by electrophoresis of 5 ml of product in a 1% agarose gel containing ethidium bromide (0.5 mg ml1). Purification of PCR products was performed with MinElute PCR purification Kit (Qiagen, Crawley, UK). Sequencing was performed with BigDye1 Terminator v3.1 Cycle Sequencing Kit (AB Applied Biosystems, Foster City, CA 94404, USA) and primers ITS 1F (50 CTT GGT CAT TTA GAG GAA GTA A) and ITS 4, at DNA Research Centre Ltd (Poznan´, Poland). BLAST searches for fungi were performed at the NCBI website using the GenBank database. Sequences with more than 99% query coverage were taken into account. Coniochaeta sp. was identified with only 93% match.

2.5. Statistical analyses Differences in abundance of microfungi in managed and unmanaged stands were analysed with chi-square tests (v2). The effects of habitat (transects and stands) on fungal community structure was determined by permutational analysis of variance (Anderson, 2001) implemented by the function Adonis in the R package Vegan. Similarity of fungal communities in geographically closer transects and more distant stands was also analysed with the Mantel test. The similarity between fungal communities in wood in 1st, 2nd and 3rd decay classes was determined by the qualitative Sorensen’s similarity index (CN). Diversity within and between communities of microfungi was compared with Margalef’s diversity index (DMg), Shannon’s diversity index (H’), Simpson’s diversity index (D), Shannon’s evenness index (E) and BergerParker’s index (d) (Magurran, 1988). Relationships between abundance or diversity of fungi and percentage of wood with the different decay classes in forest were determined by Pearson’s correlation coefficient. Statistical analyses were carried out separately for cultured fungi and fungi identified by fruit bodies.

3. Results 3.1. Effects of management on tree and wood debris production The unmanaged stand, in comparison with the managed stand, had 63% more trees (52% more Scots pines and 170% more birches), 11% greater tree density, 15 times greater wood volume of Scots pine logs, 53% more wood volume in standing dead trees and 52% fewer decayed pine stumps (Table 1). Although the average diameter of pine at breast height was almost 20% less, and average height of pine almost 7% less, the much greater number of trees per ha contributed to 18% greater volume of standing timber of all

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trees (including 14% increase of the standing timber volume of pines).

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class was moderately positively correlated with amount of log wood (r = 0.4768; P < 0.0001) and negatively correlated with amount of stump wood (r = -0.5487; P < 0.0001).

3.2. Cultured fungi Decayed wood of Scots pine was colonized by one taxon of Oomycota and 140 taxa of cultured fungi represented by Zygomycota (19 species), Ascomycota (108 species) and Basidiomycota (13 species) (Table 2). Eighty-six fungal species (55%) occurred in both stands, while 32 (20%) species occurred exclusively in managed stands and 39 (25%) in unmanaged stands. Abundance of fungi was nonsignificantly greater in managed (132) than in unmanaged stands (126). Diversity of fungi was non-significantly less in managed (9.2) than in unmanaged stands (9.6). Abundance of fungi per inoculum piece was similar (3.6 and 3.5) in both stands. Diversity of fungi per inoculum piece was identical for the three classes of decay (Table 2). Communities detected in transects within a stand tended to be more similar to each other (Adonis F6,46 = 3.14, R2 = 0.28, P = 0.001) than communities from different, managed and unmanaged, stands (Adonis F2,52 = 1.95, R2 = 0.07, P < 0.001). There was little evidence of spatial correlation between fungal diversity and transect (Mantel r = 0.33, P = 0.003–0.005) and low positive correlation between fungal diversity and type of stand (Mantel r = 0.56, P = 0.007). Sorensen’s qualitative similarity index (CN) showed little difference in diversity of fungi among the 1st, 2nd and 3rd classes of decay in managed or unmanaged stands (range 0.49– 0.51). Beauveria bassiana, C. cylindrosporum, O. tenuissimum O. canum, S. fimicola, S. inflata and S. polyspora occurred only in the managed stand, and A. effusa, C. arxii, Cytospora sp., E. jeanselmei, M. keratinophilum, N. cinnabarina, P. gigantea, S. bacilligera and T. cucurbitula only in the unmanaged stand (Table 2). Diversity of fungi (measured as average number of species per sample) from logs, fallen branches and stumps was similar in managed and unmanaged stands. Abundance of cultured fungi was greater in the 2nd and 3rd decay classes (significantly in the unmanaged stand). Diversity was the greatest in the 1st wood decay class. Logs hosted the largest number of cultured species in the 1st decay class in the managed stand and in the 2nd decay class in the unmanaged stand (Table 2). One hundred twenty-three species occurred in wood in one or two classes of decay and 35 species in wood in all three classes of decay (including C. melinii, Cladosporium spp., C. oxyspora, E. nigrum, M. elegans, M. bulbilosa, Mucor spp., M. schulzeri, Penicillium spp., Phialocephala spp., Phialophora spp., R. atrovirens, S. strictum, S. schenckii and Trichoderma spp.). Acremonium spp., Alternaria spp., Cladosporium spp., Coniochaeta spp., D. fragile, O. tenuissimum and O. canum dominated in the least decayed wood, M. bulbilosa and Phialophora in moderately decayed wood, and C. vermicularioides, C. oxyspora, M. elegans, M. schulzeri, Mucor spp. and Trichoderma spp. in the most decayed wood (Table 2). Margalef’s index (DMg), Shannon’s diversity index (H’) and Simpson’s diversity index (D) indicate a trend for decreased diversity with more advanced wood decay (Table 3). Shannon’s evenness index (E) shows slightly more evenness in the 1st and 3rd decay classes while Berger-Parker’s dominance index (d) shows slightly least dominance of individual species in the 1st decay class. Evenness tended to be least in the 2nd decay class, and dominance most in the 3rd decay class. Abundance of fungi in a particular decay class was negatively correlated with amount of log wood (r = -0.8452; P < 0.0001) and moderately positively correlated with amount of stump wood (r = 0.4861; P < 0.0001). Diversity of fungi in a particular decay

3.3. Fungal fruit bodies Fruit bodies of three species of Ascomycota (conidiomata and ascomata) and of 14 species of Basidiomycota (agarics, brackets and corals) were recorded on 33.8% of wood samples in the managed stand, which had 10 species, and on 20.6% in the unmanaged stand, which had 15 species (Table 2). In the managed stand, 54%, 23%, 15% and 8% of fruit bodies occurred on fallen branches, standing dead trees, stumps and logs, respectively. In the unmanaged stand, 34% of fruit bodies were on branches, 33% on standing dead trees and 33% on logs. Abundance (measured as number of samples colonized) was 3.4 in the managed stand and 1.4 in the unmanaged stand. Diversity was 0.6 and 0.9, respectively. Pathogenic H. annosum, S. sapinea, C. ferruginosum and saprotrophic T. fuscoviolaceum were the most frequent species in the managed stand. The last species was also frequent in the unmanaged stand. Fruit bodies of H. annosum occurred on 12% of standing dead trees and on 26% of stumps in the managed stand, and on 5% of stumps in the unmanaged stand. Cenangium ferruginosum and S. sapinea occurred, respectively, on 7% and 27% of fallen branches in the managed stand and on 23% and 12% of branches in the unmanaged stand. Fruit bodies of A. ostoyae were found only in the unmanaged stand, always at the base of standing Scots pines. Some rare species, i.e. C. variabilis, D. flavescens, R. pallida, R. bicolor and Therrya sp., were present only in the unmanaged stand. 4. Discussion In forests, wood-decay fungi contribute to nutrient cycling, ensuring the availability of resources for several functional groups of organisms as well as the forest itself (see Lonsdale et al., 2008). In many cases, regeneration of a forest occurs only when fallen logs, branches and stumps decay in situ. Measures aimed at conserving wood-decay fungi can thus be justified on the basis of their contribution to productivity of the forest and to biodiversity. Forest management practices affect the mycobiota. They may cause decreases in abundance and diversity of wood-inhabiting fungi (Bader et al., 1995; Küffer and Senn-Irlet, 2005; Penttilä et al., 2004; Müller and Blaschke, 2007; Stokland and Larsson, 2011) or may have no effect (Lindhe et al., 2004; Lindner et al., 2006; Junninen et al., 2007). This paper presents mycological effects of forest management on abundance and diversity of fungi in deadwood of Scots pine in 85-year-old mixed forest. Samples were taken from two stands lying in close proximity (managed and unmanaged). Sampling from a single forest meant that the research could be based in one homogenous habitat, thus making its conclusions less general (more specific) but strengthening their credibility. The study shows that the forest management applied (sanitation cutting, commercial thinning and timber harvesting, which are associated with less coarse woody debris, CWD) resulted in a small increase in abundance and a small decrease in diversity of fungi in the deadwood. The effects were not statistically significant. Our observations on abundance of fungi differ from those of Küffer and Senn-Irlet (2005) who reported that, in Switzerland, intensively managed forests harboured significantly less abundant wood-inhabiting fungi. Stokland and Larsson (2011) found, however, no difference in abundance of fungi in Scots pine logs in managed and natural forests. The differences usually result from habitat, types of fungi studied and type and quality of substrate

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Table 2 Fungi present in deadwood of Scots pine. Percentage of inocula colonized by cultured fungi Taxon

Managed stand

Unmanaged stand

Decay class 1st

2nd

Oomycota Pythium sp. Zygomycota Absidia californica J.J. Ellis & Hesselt. + A. coerulea Bainier + A. cylindrospora Hagem + A. glauca Hagem + Mortierella alpina Peyronel + M. elongata Linnem. + M. gamsii Milko + M. hyalina (Harz) W. Gams + M. humilis Linnem. ex W. Gams + M. minutissima Tiegh. + M. parvispora Linnem. + M. zonata Linnem. ex W. Gams + M. verticillata Linnem. Mucor hiemalis Wehmer + M. plumbeus Bonord. + M. racemosus Fresen. Umbelopsis isabellina (Oudem.) W. Gams + U. ramanniana (Möller) W. Gams + U. vinacea (Dixon-Stew.) Arx Ascomycota Aequabiliella effusa (Damm & Crous) Crous1 (KX586145) Acremonium charticola (Lindau) W. Gams + Acremonium spp. Alternaria alternata (Fr.) Keissl. + A. botrytis (Preuss) Woudenberg & Crous + A. oudemansii (E.G. Simmons) Woudenberg & Crous Aspergillus versicolor (Vuill.) Tirab. Beauveria bassiana (Bals.-Criv.) Vuill. Bipolaris cf. oryzae (Breda de Haan) Shoemaker Botrytis cinerea Pers. Cadophora melinii Nannf. Chaetosphaeria vermicularioides (Sacc. & Roum.) W. Gams & Hol.-Jech. Chloridium cylindrosporum W. Gams & Hol.-Jech. Cladophialophora arxii Tintelnot Cladosporium cladosporioides (Fresen.) G.A. de Vries + C. herbarum (Pers.) Link + C. sphaerospermum Penz. Clonostachys rosea (Link) Schroers. Samuels. Seifert & W. Gams Coniochaeta hoffmannii (J.F.H. Beyma) Z.U. Khan. Gené & Guarro + C. mutabilis (J.F.H. Beyma) Z.U. Khan. Gené & Guarro + Coniochaeta sp.1 (KX586149) Curvularia cf. tsudae (Tsuda & Ueyama) H. Deng. Y.P. Tan & R.G. Shivas Cyphellophora oxyspora (W. Gams) Réblová & Unter. Cytospora sp. Dicranidion fragile Harkn. Epicoccum nigrum Link Exophiala jeanselmei (Langeron) McGinnis & A.A. Padhye Gibberella zeae (Schwein.) Petch. Lecanicillium lecanii (Zimm.) Zare & W. Gams Mariannaea elegans (Corda) Samson Metapochonia bulbilosa (W. Gams & Malla) Kepler. Rehner & Humber Myriodontium keratinophilum Samson & Polon. Myrmecridium schulzeri (Sacc.) Arzanlou. W. Gams & Crous Nectria cinnabarina (Tode) Fr.1 (KX586144) Oidiodendron tenuissimum (Peck) S. Hughes Ophiostoma canum (Münch) Syd. & P. Syd.1 (KX586141) Paecilomyces divaricatus (Thom) Samson. Houbraken & Frisvad + Paecilomyces sp. Paraconiothyrium fuckelii (Sacc.) Verkley & Gruyter Penicillium adametzii Zaleski + P. aurantiogriseum Dierckx + P. canescens Sopp. + P. citrinum Thom + P. commune Thom + P. dierckxii Biourge + P. glabrum (Wehmer) Westling + P. janczewskii Zaleski + P. raistrickii G. Sm. + P. simplicissimum (Oudem.) Thom + P. spinulosum Thom + P. thomii Maire + P. vinaceum J.C. Gilman & E.V. Abbott + Talaromyces flavus (Klöcker) Stolk & Samson + T. funiculosus (Thom) Samson. N. Yilmaz. Frisvad & Seifert + T. islandicus (Sopp) Samson. N. Yilmaz. Frisvad & Seifert + T. minioluteus (Dierckx) Samson. N. Yilmaz. Frisvad & Seifert + T. variabilis (Sopp) Samson. N. Yilmaz. Frisvad & Seifert Phialocephala botulispora (Cole & W.B. Kendr.) Grünig & T.N. Sieber + P. dimorphospora W.B. Kendr. + Phialocephala sp. Phialophora bubakii (Laxa) Schol-Schwarz + P. cinerescens (Wollenw.) J.F.H. Beyma + P. clavispora W. Gams + P. verrucosa Medlar + Phialophora sp.1 (KX586148) Phoma eupyrena Sacc. + P. glomerata (Corda) Wollenw. & Hochapfel + P. minutella Sacc. & Penz. + Pyrenochaeta cava (Schulzer) Gruyter. Aveskamp & Verkley Pseudogymnoascus pannorum (Link) Minnis & D.L. Lindner Ramichloridium apiculatum (J.H. Mill.. Giddens & A.A. Foster) de Hoog Rhinocladiella atrovirens Nannf. Sarocladium strictum (W. Gams) Summerb. Septotrullula bacilligera Höhn. Simplicillium lamellicola (F.E.V. Sm.) Zare & W. Gams Sordaria fimicola (Roberge ex Desm.) Ces. & De Not. Sporothrix inflata de Hoog1 (KX586142) Sporothrix schenckii Hektoen & C.F. Perkins Sydowia polyspora (Bref. & Tavel) E. Müll. Thyronectria cucurbitula (Tode) Jaklitsch & Voglmayr1 (KX586143) Torula sp. Trichoderma atroviride P. Karst. + T. deliquescens (Sopp) Jaklitsch + T. fertile Bissett + T. hamatum (Bonord.) Bainier + T. harzianum Rifai + T. koningii Oudem. + T. polysporum (Link) Rifai + T. virens (J.H. Mill.. Giddens & A.A. Foster) + T. viride Pers. Truncatella angustata (Pers.) S. Hughes

3rd

1st

0.3 0.7 5.8

1.9

1.4 6.0

10.6 2.8

17.6

2.1 17.4 2.8

7.1

1.2 7.5

13.2

1.1 11.7

5.6 7.5

22.2 2.2

7.2 9.4

1.9 2.8

1.1 0.6 1.1 1.1 11.1

1.2

8.7 9.1

5.6 20.8 6.9

2.8

1.4

9.0

32.8

3.2 1.2 9.9

10.0

3.6

10.4

5.0 1.7

0.8

1.1 0.6 7.9

4.0 24.6

3.9 11.7 17.8

3rd

2.1 1.7 2.8

7.8

2nd

21.5

3.5 3.5 5.6 2.8 1.4

22.9 20.8

0.7 2.8

6.9

3.5 2.1

2.5 8.8

4.6 18.5

3.8 2.3 0.5 17.7

4.6

0.3 3.0

0.5 0.3 8.1 23.7 1.3 2.5

9.2

19.4 14.8 13.9

2.8 1.2

0.6 66.1

99.2

75.7

9.4 12.8

1.9 28.6

12.5 5.6

1.7

0.4

2.8

0.4

38.9 5.0

33.7 4.0

3.9 0.6 1.1 4.4 11.7

1.6

36.8 3.5

52.1

0.5 0.5 88.1

100.0

8.3

3.5 28.0

4.6 13.9

7.6

0.8

38.9 1.4

0.3 3.0 51.8 8.1 1.3 0.5

27.8 2.8

1.8

25.9

2.8

2.4

0.5 27.8

3.9

67.1

6.9 90.3

29.2

77.8

2.8

0.5

83.3

H. Kwas´na et al. / Forest Ecology and Management 400 (2017) 438–446

443

Table 2 (continued) Percentage of inocula colonized by cultured fungi Taxon

Managed stand

Unmanaged stand

Decay class

Westerdykella minutispora (P.N. Mathur) Gruyter. Aveskamp & Verkley Non-sporulating often pigmented (10 taxa) Basidiomycota Ceratobasidium sp.1 (KX586147) Hormographella sp. Hyalodendron sp. Phlebiopsis gigantea (Fr.) Jülich Tritirachium oryzae (Vincens) de Hoog Non-sporulating (8 taxa) Number of species Oomycota Zygomycota Ascomycota Basidiomycota Number of samples analysed Number of inocula analysed Total number of isolates Total numer of species Number of isolates per sample Average number of isolates per sample Number of species per sample Average number of species per sample Number of isolates per inoculum Average number of isolates per inoculum Number of species per inoculum Number of species in logs Average number of species in logs Number of species in branches Average number of species in branches Number of species in stumps Average number of species in stumps Percentage of samples colonized by fungi with fruit bodies Ascomycota Cenangium ferruginosum Fr. Sphaeropsis sapinea (Fr.) Dyko & B. Sutton Therrya sp.

1st

2nd

0.6 5.0

0.4 7.9

3rd

1st

2nd

2.1

2.8 6.3

0.5

0.6 4.4 1.7

1.9

3.3

1.2

3.5 7.6

5 54 5 5 180 641 63 128a 132 12.6 9.2 3.5 3.6 0.4 53aA 39 33A 27 41 28

13 46 5 7 252 891 50 127

1 6 23 4 4 144 568 32 142

7.1

8.0

3.5

3.9

0.2 39

0.2 25a

25

19

29

15

3.2 6.5

0.7 2.8 0.7 1.4 13.9

3 47 5 4 144 381 55 95abc 126 13.8 9.6 2.6 3.5 0.4 45 41 35 30 42 30

3.8 0.3 7.3 15.7

2.8

1 12 56 8 11 396 1597 74 145b

3 21 1 3 108 411 25 137c

6.7

8.3

4.0

3.8

0.2 54bAB

0.2 23b

34A

21

30

17

1.5 0.8 0.5

Basidiomycota Armillaria ostoyae (Romagn.) Herink) Crepidotus variabilis (Pers.) P. Kumm. Diplomitoporus flavescens (Bres.) Doman´ski Heterobasidion annosum (Fr.) Bref. Hypholoma fasciculare (Huds.) P. Kumm. Peniophora pini (Schleich.) Boidin Phanerochaete velutina (DC.) P. Karst. Porodaedalea pini (Brot.) Murrill Ramaria pallida (Schaeff.) Ricken Resinicium bicolor (Alb. & Schwein.) Parmasto Steccherinum ochraceum (Pers.) Gray Stereum hirsutum (Willd.) Pers. Trichaptum fuscoviolaceum (Ehrenb.) Ryvarden Typhula sp.

3.2 1.6

0.8 6.3 1.0

Number of species Average percentage of samples colonized Number of species per sample

10 3.4a 0.6

15 1.4a 0.9

12.9 1.6 0.8 1.6 1.6

3rd

0.8 0.3 0.5 2.0 0.5 0.8 2.0 0.3 2.5

0.8

Explanations. 1 Identification was confirmed by ITS1/2 DNA analysis. Sequences with number attached deposited in NCBI GenBank. Results for two species were non-informative; KX586146 – endophyte with 99% of similarity, KX586150 – no reference sequence. a,b,c,A,B,C The same letter indicates a statistically significant difference according to v2 – test, P  0.001 or P  0.05.

provided. The earlier studies included only polyporoid and corticoid fungi. Our analyses included also cultured fungi from Scots pine, which are more adaptive to management practices than others, i.e. spruce-associated fungi (Stokland and Larsson, 2011). Our observations on diversity of fungi agree with results of Penttilä et al. (2004) who, in southern Finland, recorded 38–80% fewer species in managed mature P. abies forests than in unman-

aged ones, and of Müller and Blaschke (2007) who recorded less fungal diversity in thinned broadleaved forests than in nonthinned ones. Less diversity of wood-inhabiting fungi in the managed stand seems to have resulted from reduction of coarse woody debris. This phenomenon is common and has been reported previously (Edman et al., 2004; Penttilä et al., 2004, 2006; Stokland and Kauserud

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H. Kwas´na et al. / Forest Ecology and Management 400 (2017) 438–446

Table 3 Indices for microfungi from decaying wood. Index

Managed stand

Unmanaged stand

Decay class 1st

2nd

3rd

1st

2nd

3rd

Margalef’s diversity index-DMg Shannon’s diversity index-H0 Simpson’s diversity index–D

9.59 3.06 0.07

7.21 2.49 0.13

4.88 2.55 0.11

9.25 2.80 0.09

9.89 2.63 0.11

3.98 2.22 0.16

Shannon’s evenness index-E Berger–Parker’s dominance index-d

0.73 0.10

0.63 0.09

0.73 0.09

0.69 0.14

0.60 0.12

0.68 0.07

(2004). Siitonen (2001) recorded the extinction of 50% of woodinhabiting species followed by a 90% reduction in deadwood volume. Greater diversity of wood-inhabiting fungi usually results from greater heterogeneity of CWD. In the present study, heterogeneity was guaranteed by the different types of wood debris present in the stands, i.e. logs, fallen branches, standing dead trees and decayed stumps, in three classes of decay. Logs, because of their large volume, extensive surfaces for colonization, unequally decomposed sections and higher rate of decomposition (compared with stumps), hosted the greatest diversity of cultured fungi, particularly in the unmanaged stand. This agrees with Lumley et al. (2001) and Stokland and Larsson (2011), who reported greater diversity of fungi in logs in unmanaged forests. Fungal abundance and diversity in dead wood depend on the size of the sample. Brazee et al. (2014) found that medium size samples (20–25 – >40 cm diameter) supported more abundant fungal communities and that smaller samples (<20 cm diameter) had more diverse fungal communities. Heilmann-Clausen and Christensen (2004) reported, however, that fungal diversity increased with size of the wood sample. Our sample sizes of 20– 30 cm diameter were an attempt to compromise between large and small samples and so provide conditions that would produce adequate and credible results on both fungal abundance and diversity. The number of isolates per sample shows the scale of occupation of wood (= abundance). Although this was low in the 1st decay class in the unmanaged stand it is evident that abundance increases with advanced decay of wood. Increased abundance was associated with less fungal diversity and occurred particularly in stumps which, in advanced decay classes, were often intensively colonized by only a few species. This agrees in part with Brazee et al. (2014), who highlighted the significance of the quality of deadwood substrate for fungal colonization. Greater abundance associated with lower diversity seems to result from the domination of single species, species-specific replacement and succession resulting from fungal inter- and intraspecific competition. Degradation of wood changes its structure and chemical composition; the density and C/N ratio decrease and the moisture and lignin contents increase. These stimulate changes in composition of the fungal community. Fungal diversity and wood density are inversely related, and fungal diversity increases with loss of wood density (Rajala et al., 2015). In the present study, diversity of cultured fungi was greatest in the earlier stages of decay. This observation agrees with Bader et al. (1995), Lindblad (1998), Junninen et al. (2008) and Pouska et al. (2011), but not with Rajala et al. (2011, 2012), Kubartová et al. (2012) and Ovaskainen et al. (2013), who found that fungal diversity increased towards the end of succession when wood-inhabiting fungi were eventually replaced by mycorrhizal species. The list of fungi identified from fruit bodies supplemented that of cultured fungi and included Scots pine pathogens (H. annosum, S. sapinea, C. ferruginosum) and common saprotrophs (P. gigantea, T.

fuscoviolaceum). The first two pathogens were the most common. Heterobasidion annosum, the most economically important forest pathogen in the Northern Hemisphere, occurred more frequently in the managed stand, probably because it had more stumps, contributing to the spread of ‘annosum root rot’. Species of Heterobasidion readily colonize dead wood. Fruit bodies of H. annosum were found at the bases of dead pines and pine stumps but not on logs. This agrees with Stokland and Larsson (2011), who also did not find H. annosum on pine logs in either managed or unmanaged forest. However, Kubartová et al. (2012) and Jang et al. (2015) found H. parviporum Niemelä & Korhonen and H. orientale Tokuda, T. Hatt. & Y.C. Dai among the abundant and widespread fungi in logs of Norway spruce and Manchurian fir (Abies holophylla Maxim.). Cies´lak et al. (2015) found that H. annosum genotypes originating from stumps were more invasive than genotypes originating from living trees. Thus, more stumps, as in managed stands, can be a greater reservoir of highly virulent strains of H. annosum, which increases the threat of ‘annosum root rot’. Sphaeropsis sapinea, the cause of ‘Sphaeropsis blight‘ of pine trees, occurred usually on fallen branches, particularly in the managed stand. Our study confirms that wood debris, particularly branches, can be a prolonged source of inoculum of S. sapinea. Cenangium ferruginosum infects young twigs, especially on older Scots pines. This fungus, like S. sapinea, was more frequent on fallen branches in the managed stand. This may support the supposition that earlier occurrence of ‘Cenangium twig blight’ may predispose them to infection by S. sapinea. Phlebiopsis gigantea, a biological agent active against H. annosum, is usually common on conifer logs and stumps but was here recorded only rarely, on logs in the unmanaged stand. Stokland and Larsson (2011) reported that P. gigantea preferred the habitat of managed forest. Trichaptum fuscoviolaceum is common in Poland but is considered an endangered species in other EU countries. This fungus colonizes the wood of different conifers causing white pocket rot. Our study showed that unmanaged, mature Scots pine may favour its occurrence. The presence of B. bassiana and grass-associated Bipolaris sp., Curvularia sp. and G. zeae suggests their adaptation and possible contribution to decay of wood. The latter group, possibly simultaneous inhabitants of the vascular systems of grasses (composed of xylem and phloem) present in the understorey, have previously been considered to be endophytes active in early wood decay of trees in Chile (Oses et al. (2008). Selection of appropriate methods for assessing fungal abundance and diversity is highly dependent on the ecological characteristics and distribution or dispersal of the targeted fungi in both time and space. Two different methods were used here: mycelial isolation followed by identification on the basis of morphology, and the identification of fruit bodies. Using the first method, fungi were isolated from 1224 inocula taken from 34 samples. This classical approach allowed us to gain an understanding of fungal distribution and reproduction in substrate and overall area.

H. Kwas´na et al. / Forest Ecology and Management 400 (2017) 438–446

It was possible to recognize species that were abundant and able to reproduce in wood and those that were merely present in a stand. This allowed recognition of the significance and ecological roles of individual species in biogeochemical processes, i.e. lignin decomposition. Using these methods, 140 species of cultured fungi and 17 taxa of fungi present as fruit bodies were detected. This number of species is more than twice the number of taxa (75) detected elsewhere using three methods (fruit body collection, mycelial isolation and 454 sequencing) in branches and logs of Manchurian fir (Jang et al., 2015). Molecular methods, which were not applied in this study for detection of fungi, may have limited diagnostic value. They will not guarantee a correct estimate of fungal diversity until a highquality reference database, with broad coverage of woodinhabiting fungi, is available. Jang et al. (2015) found greater diversity of fungi by mycelial isolation and fruit body collection than by 454 sequencing. Kubartová et al. (2012) detected fungi by 454 sequencing that were simultaneously detected by fruit body identification. Ovaskainen et al. (2010) detected, by 454 sequencing, only 30% of the species that were detected by fruit body identification. The majority of the 157 fungal species detected were identified to species level. Application of molecular methods and hence identification based on probability may not have guaranteed such accuracy and reliability. In the study of Ovaskainen et al. (2010), which included 62214 sequences, 51% (representing 30 species) and 9% (representing 14 genera) of fungi were identified respectively to species and genus levels (with at least 90% confidence). The remaining 40% of the sequences remained unidentified even to genus level, using 90% probability as the threshold. Results obtained by Nilsson et al. (2009), Siitonen et al. (2009) and Ovaskainen et al. (2010) emphasize two reasons for failure to identify fungal species from sequence data. First is the level of interand intra-species variation in the ITS1-region, and the second is the absence of focal species in the reference database. The results on effects of a particular type of management in one mature Scots pine forest are presented here. Lindner et al. (2006), Penttilä et al. (2006) and Stokland and Larsson (2011) showed that the responses of wood-inhabiting fungi to a changed habitat are very different over time and space. Different responses result from individual species composition, different dispersal abilities in various habitats, productivity of the forest and deadwood input rates. Generalizations on effects of similar management practices on mycobiota in all forest types should therefore not be made. 5. Conclusions 1. Scots pine coarse woody debris hosts abundant and diverse mycobiota. 2. Sanitation cutting, commercial thinning and timber harvesting in the mature Scots pine forest have small effect on abundance and diversity of mycobiota in coarse woody debris. 3. Large-diameter deadwood, particularly logs, is the most relevant substrate type for conservation of fungi. 4. Deadwood at earlier stages of decay increases fungal diversity and at later stages of decay increases abundance.

Acknowledgements The study was supported by the Polish State Forests National Forest Holding through the project ‘‘The threshold values of deadwood and biodiversity of insects and fungi”.

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References Abrego, N., Salcedo, I., 2013. Variety of woody debris as the factor influencing woodinhabiting fungal richness and assemblages: is it a question of quantity or quality? For. Ecol. Manage. 291, 377–385. Afyon, A., Konuk, M., Yagiz, D., Helfer, S., 2005. A study of wood decaying macrofungi of the western Black Sea Region, Turkey. Mycotaxon 93, 19–322. Anderson, M.J., 2001. A new method for non-parametric multivariate analysis of variance. Aust. Ecol. 26, 32–46. Anonymous, 2013. Forest Europe, (2013) State of Europe’s Forest 2012. Status and Trends in Sustainable Forest Management In Europe. UNECE/Food and Agriculture Organization of the United Nations, Rome. Bader, P., Jansson, S., Jonsson, B.G., 1995. Wood-inhabiting fungi and substratum decline in selectively logged boreal spruce forests. Biol. Conserv. 72, 355–362. Brazee, N.J., Lindner, D.L., D’Amato, A.W., Fraver, S., Forrester, J.A., Mladenoff, D.J., 2014. Disturbance and diversity of wood-inhabiting fungi: effects of canopy gaps and downed woody debris. Biodivers. Conserv. 23, 2155–2172. Brazee, N.J., Lindner, D.L., Fraver, S., D’Amato, A.W., Milo, A.M., 2012. Woodinhabiting, polyporoid fungi in aspen-dominated forests managed for biomass in the U.S. Lake States. Fungal Ecol. 5, 600–609. Cies´lak, R., Behnke-Borowczyk, J., Raz´ny, T., Molin´ska-Glura, M., Ratajczak, A., S´wietlik, A., Łakomy, P., 2015. Description of Heterobasidion annosum population occurring in Scots pine stands in Człopa Forest Districts. II. Mycelium development in a dead wood. Acta Sci. Pol. Silv. Colendar. Rat. Ind. Lignar. 14 (2), 93–102. Czerepko, J. (Ed.), Boczon´, A., Cies´la, A., Forycka, A., Ksepko, M., Obidzin´sk, A., Paluch, _ ´ ski, W., Sokołowski, K., Szwed, W., Wróbel, M., 2008. R., Rodziewicz, A., Rózan _ ´ ci biologicznej lasów w Polsce na podstawie powierzchni Stan róznorodnos obserwacyjnych monitoringu. (Biodiversity condition of Polish forests on the basis of monitoring plots). Instytut BadawczyLes´nictwa, Se˛kocin Stary, 1–135. Dai, Y.C., Wei, Y.L., Wang, Z., 2004. Wood-inhabiting fungi in southern China—2. Polypores from Sichuan Province. Ann. Bot. Fenn. 41, 319–329. Domsch, K.H., Gams, W., Anderson, T.-H., 1980. Compendium of Soil Fungi. Academic Press, New York, USA, pp. 1–860. Edman, M., Gustafsson, M., Stenlid, J., Jonsson, B.G., Ericson, L., 2004. Spore deposition of wood-decaying fungi: importance of landscape composition. Ecography 27, 103–111. http://dx.doi.org/10.1111/j.0906-7590.2004.03671.x. Fukasawa, Y., Osono, T., Takeda, H., 2005. Microfungus communities of Japanese beech logs at different stages of decay in a cool temperate deciduous forest. Can. J. For. Res. 39, 1606–1614. http://dx.doi.org/10.1139/X09-080. Fukasawa, Y., Osono, T., Takeda, H., 2011. Wood decomposing abilities of diverse lignicolous fungi on non-decayed and decayed beech wood. Mycologia 103 (3), 474–482. http://dx.doi.org/10.3852/10-246. Greslebin, A., Rajchenberg, M., 2003. Diversity of Corticiaceae sens. lat. in Patagonia, Southern Argentina. NZ J. Bot. 41, 437–446. Halme, P., Ódor, P., Christensen, M., Piltaver, A., Veerkamp, M., Walleyn, R., Siller, I., Heilmann-Clausen, J., 2013. The effect of habitat degradation on metacommunity structure of wood-inhabiting fungi in European beech forests. Biol. Conserv. 168, 24–30. Heilmann-Clausen, J., Christensen, M., 2004. Does size matter? On the importance of various dead wood fractions for fungal diversity in Danish beech forests. Forest Ecol. Manag. 201, 105–117. Heilmann-Clausen, J., Christensen, M., 2005. Wood-inhabiting macrofungi in Danish beech-forests—conflicting diversity patterns and their implications in a conservation perspective. Biol. Conserv. 122, 633–642. http://dx.doi.org/ 10.1016/j.biocon.2004.10.001. Jang, Y., Jang, S., Min, M., Hong, J.H., Lee, H., Lee, H., Lim, Y.W., Kim, J.J., 2015. Comparison of the diversity of Basidiomycetes from dead wood of the Manchurian fir (Abies holophylla) as evaluated by fruiting body collection, mycelial Isolation, and 454 Sequencing. Microb. Ecol. 70 (3), 634–645. http://dx. doi.org/10.1007/s00248-015-0616-5. Jönsson, M.T., Edman, M., Jonsson, B.G., 2008. Colonization and extinction patterns of wood-decaying fungi in a boreal old-growth Picea abies forest. J. Ecol. 96, 1065–1075. Junninen, K., Kouki, J., Renvall, P., 2008. Restoration of natural legacies of fire in European boreal forests: an experimental approach to the effects on wooddecaying fungi. Can. J. For. Res. 38, 202–215. Junninen, K., Penttilä, R., Martikainen, P., 2007. Fallen retention aspen trees on clear-cuts can be important habitats for red-listed polypores: a case study in Finland. Biodivers. Conserv. 16, 475–490. Kubartová, A., Ottosson, E., Dahlberg, A., Stenlid, J., 2012. Patterns of fungal communities among and within decaying logs, revealed by 454 sequencing. Mol. Ecol. 21, 4514–4532. Küffer, N., Senn-Irlet, B., 2005. Influence of forest management on the species richness and composition of wood-inhabiting basidiomycetes in Swiss forests. Biodivers. Conserv. 14, 2419–2435. Kwas´na, H., Łakomy, P., Gornowicz, R., 2016. Grzyby saproksyliczne w resztkach pozre˛bowych sosny zwyczajnej. (Saproxylic fungi in the Scots pine woody debris.). Sylwan 160 (5), 355–364. Lindblad, I., 1998. Wood-inhabiting fungi on fallen logs of Norway spruce: relations to forest management and substrate quality. Nord. J. Bot. 18, 243–255. Lindhe, A., Asenblad, N., Torenson, H.-G., 2004. Cut logs and high stumps of spruce, birch, aspen and oak— nine years of saproxylic fungi succession. Biol. Conserv. 119, 443–454.

446

H. Kwas´na et al. / Forest Ecology and Management 400 (2017) 438–446

Lindner, D.L., Burdsall, H.H., Stanosz, G.R., 2006. Species diversity of polyporoid and corticioid fungi in northern hardwood forests with differing management histories. Mycologia 98, 195–217. Lonsdale, D., Pautasso, M., Holdenrieder, O., 2008. Wood-decaying fungi in the forest: conservation needs and management options. Eur. J. Forest. Res. 127, 1– 22. Lumley, T.C., Gignac, L.D., Currah, R.S., 2001. Microfungus communities of white spruce and trembling aspen logs at different stages of decay in disturbed and undisturbed sites in the boreal mixedwood region of Alberta. Can. J. Bot. 79, 76– 92. Magurran, A.E., 1988. Ecological Diversity and Its Measurement. Princeton University Press. USA, Princeton, NJ. Müller, H., Blaschke, E.M., 2007. Assemblages of wood-inhabiting fungi related to silvicultural management intensity in beech forests in southern Germany. Eur. J. Forest Res. 126, 513–527. Nilsson, R.H., Ryberg, M., Abarenkov, K., Sjokvist, E., Kristiansson, E., 2009. The ITS region as a target for characterization of fungal communities using emerging sequencing technologies. Fems Microbiol. Lett. 296, 97–101. Ódor, P., Heilmann-Clausen, J., Christensen, M., Aude, E., van Dort, K.W., Piltaver, A., Siller, I., Veerkamp, M.T., Walleyn, R., Standovar, T., van Hees, A.F.M., Kosec, J., Matocec, N., Kraigher, H., Grebenc, T., 2006. Diversity of dead wood inhabiting fungi and bryophytes in seminatural beech forests in Europe. Biol. Conserv. 131, 58–71. http://dx.doi.org/10.1016/j.biocon.2006.02.004. Ortega, A., Navarro, F.B., 2004. A myco-ecological analysis (lignicolous Aphyllophorales sensu lato, Basidiomycota) of the Abies pinsapo, Quercus and Pinus forests of Andalusia (southern Spain). Nova Hedwigia 78, 485–499. http:// dx.doi.org/10.1127/0029-5035/2004/0078-0485. Oses, R., Valenzuela, S., Freer, J., Sanfuentes, E., Rodriguez, J., 2008. Fungal endophytes in xylem of healthy Chilean trees and their possible role in early wood decay. Fungal Divers. 33, 76–87 http://www.fungaldiversity.org/fdp/sfdp/ 33-4.pdf. Ovaskainen, O., Nokso-Koivisto, J., Hottola, J., Rajala, T., Pennanen, T., Ali-Kovero, H., Miettinen, O., Oinonen, P., Auvinen, P., Paulin, L., Larsson, K.-H., Mäkipää, R., 2010. Identifying wood-inhabiting fungi with 454 sequencing—what is the probability that BLAST gives the correct species? Fungal Ecol. 3, 274–283. Ovaskainen, O., Schigel, D., Ali-Kovero, H., Auvinen, P., Paulin, L., Norden, B., Norden, J., 2013. Combining high-throughput sequencing with fruit body surveys reveals contrasting life-history strategies in fungi. ISME J. 7, 1696–1709. Paillet, Y., Bergès, L., Hjältén, J., Odor, P., Avon, C., Bernhardt-Römermann, M., Bijlsma, R.J., De Bruyn, L., Fuhr, M., Grandin, U., Kanka, R., Lundin, L., Luque, S., Magura, T., Matesanz, S., Mészáros, I., Sebastià, M.T., Schmidt, W., Standovár, T., Tóthmérész, B., Uotila, A., Valladares, F., Vellak, K., Virtanen, R., 2009.

Biodiversity differences between managed and unmanaged forests: metaanalysis of species richness in Europe. 2009. Conserv. Biol. 24, 101–112. Penttilä, R., Lindgren, M., Miettinen, O., Rita, H., Hanski, I., 2006. Consequences of forest fragmentation for polyporous fungi at two spatial scales. Oikos 114, 225– 240. Penttilä, R., Siitonen, J., Kuusinen, M., 2004. Polypore diversity in managed and oldgrowth boreal Picea abies forests in southern Finland. Biol. Conserv. 117, 271– 283. http://dx.doi.org/10.1016/j.biocon.2003.12.007. Pitt, J.I., 1979. The Genus Penicillium and Its Teleomorphic States Eupenicillium and Talaromyces. Academic Press, London-New York-Toronto-Sydney-San Francisco, pp. 1–634. Pouska, V., Leps, J., Svoboda, M., Lepsova, A., 2011. How do log characteristics influence the occurrence of wood fungi in a mountain spruce forest? Fung. Ecol. 4, 201–209. Rajala, T., Peltoniemi, M., Hantula, J., Mäkipää, R., Pennanen, T., 2011. RNA reveals a succession of active fungi during the decay of Norway spruce logs. Fungal Ecol. 4, 437–448. Rajala, T., Peltoniemi, M., Pennanen, T., Mäkipää, R., 2012. Fungal community dynamics in relation to substrate quality of decaying Norway spruce (Picea abies [L.] Karst.) logs in boreal forests. FEMS Microbiol. Ecol. 81, 494–505. Rajala, T., Tuomivirta, T., Pennanen, T., Mäkipää, R., 2015. Habitat models of woodinhabiting fungi along a decay gradient of Norway spruce logs. Fungal Ecol. 18, 48–55. Seifert, K.A., Kendrick, B., Morgan-Jones, G., Gams, W., 2011. The Genera of Hyphomycetes. CBS Fungal Biodiversity Centre, the Netherlands, pp. 1–997. Siitonen, J., 2001. Forest management, coarse woody debris and saproxylic organisms: Fennoscandian boreal forests as an example. Ecol. Bull. 49, 11–41. Siitonen, J., Hottola, J., Immonen, A., 2009. Differences in stand characteristics between brook-side key habitats and managed forests in Southern Finland. Silva Fenn. 43, 21–37. Stokland, J.N., Kauserud, H., 2004. Phellinus nigrolimitatus-a wood-decomposing fungus highly influenced by forestry. Forest Ecol. Manag. 87, 333–343. Stokland, J.N., Larsson, N., 2011. Legacies from natural forest dynamics: different effects of forest management on wood-inhabiting fungi in pine and spruce forests. Forest Ecol. Manage. 261, 1707–1721. Stokland, J.N., Meyke, E., 2008. The saproxylic database: an emerging overview of the biological diversity in dead wood. Revue d’Ecologie (Terre Vie) 10 (Suppl.), 37–48. White, T.J., Bruns, T., Lee, S., Taylor, J.W., 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, M.A., Gelgard, D.H., Snisky, J.J., White, T.J. (Eds.), PCR Protocols: A Guide to Methods and Applications. Academic Press, New York, NY, pp. 315–322.