Colonization Patterns of Wood-Inhabiting Fungi in Boreal Forest

Colonization Patterns of Wood-inhabiting Fungi in Boreal Forest

Jörgen Olsson 2008

Department of Ecology and Environmental Science Umeå University SE-901 87 Umeå

AKADEMISK AVHANDLING Som med vederbörligt tillstånd av rektorsämbetet vid Umeå universitet för erhållande av filosofie doktorsexamen i ekologi kommer att offentligen försvaras fredagen 28 november, kl 13.00 i stora hörsalen (KB3B1), KBC

Examinator: Professor Lars Ericson, Umeå universitet

Opponent: Dr. Agric. Jørund Rolstad, Norwegian Forest and Landscape Institute, Ås, Norway

ORGANISATION DOCUMENT NAME Dept. of Ecology and Environmental Science Doctoral Dissertation Umeå University DATE OF ISSUE SE-901 87 Umeå November 2008

AUTHOR: Jörgen Olsson

TITLE: Colonization patterns of wood-inhabiting fungi in boreal forest

ABSTRACT

Forest management practices have changed the over-all structure of the Fennoscandian forest landscape resulting in a lack of suitable substrates for many wood-inhabiting species. The objectives of this thesis was to describe the colonization patterns of wood-inhabiting fungi, including the potential role of beetles as dispersal vectors, on different types of dead wood substrate and assess the importance of active measures in the forest landscape in order to restore biodiversity i.e. to increase the amount of dead wood and the use of restoration fire. The results clearly demonstrate the importance of restoration fire for wood-inhabiting fungi in a dry Pinus sylvestris forest. The general pattern for the majority of the species was a drastic decline the first two years after fire. However, after four years most of the species had recovered and were frequently found on logs strongly affected by the fire. The early fungal colonization patterns on fresh experimental Picea abies logs revealed no differences between managed forest stands and stands associated with nature reserves. After five years the species assemblage on the experimental logs was affected by stand age, forest site type, and distance to forest reserves. However, very few red-listed species colonized the logs in spite of being fairly common in the reserve stands. We conclude that the experimental period of only five years was too short to fully evaluate the possibilities to use experimental logs for threatened and red-listed species. We assessed the colonization patterns of different fungal functional groups based upon their different nutritional strategies namely mycorrhizal, saprotrophic on litter and humus, saprotrophic on wood causing white rot, and saprotrophic on wood causing brown rot. The results show that the fungal community undergoes a marked change in dominant nutritional strategies during the initial stage of the colonization process both after fire disturbance and on fresh un-colonized experimental logs. To which extent, saproxylic beetles are involved as passive or active vectors in the dispersal and colonization of wood-inhabiting fungi occurring on dead wood is poorly understood. The results clearly showed that some beetle species do discriminate between different fungal substrates and in particular, the bark beetle Dryocoetes autographus showed significant preference for wood with Fomitopsis rosea mycelium.

KEYWORDS: Wood-inhabiting fungi, colonization, dispersal, restoration fire, saproxylic beetles, conservation, forest management, boreal forest.

LANGUAGE: English ISBN: 978-91-7264-691-9 NUMBER OF PAGES: 35

SIGNATURE: DATE: 7 November 2008

Colonization Patterns of Wood-inhabiting Fungi in Boreal Forest

Jörgen Olsson 2008

Department of Ecology and Environmental Science Umeå University Sweden

ISBN: 978-91-7264-691-9 © Jörgen Olsson 2008 Printed by VMC, KBC, Umeå University, Umeå, Sweden, 2008 LIST OF PAPERS

This thesis is a summary and discussion of the following papers, which will be referred to in the text by their Roman numerals.

I Olsson, J., Jonsson, B.G., Hjältén, J., Ericson, L., The early stages of colonization of wood-inhabiting fungi on experimental spruce logs. Manuscript

II Olsson, J., Jonsson, B.G., Restoration fire and wood-inhabiting fungi in a Swedish Pinus sylvestris forest. Manuscript

III Johansson, T., Olsson, J., Hjältén, J., Jonsson, B.G., Ericson, L., Beetle attraction to sporocarps and wood infected with mycelia of decay fungi in old-growth spruce forest of northern Sweden. Forest Ecology and Management 237, 335-341.

IV Olsson, J., Johansson, T., Jonsson, B.G., Hjältén, J., Edman, M., Ericson, L. 2006. Depauperate saproxylic beetle faunas in landscapes with small proportions of old forest. Manuscript

Paper III is reproduced with the kind permission of the publisher.

TABLE OF CONTENTS

INTRODUCTION 7 Wood-inhabiting fungi 10 Dispersal of wood-inhabiting fungi 10 Establishment and community development 12 OBJECTIVES OF THIS THESIS 13 MATERIAL AND METHODS 14 Study areas 14 Study design 15 Sampling methods 15 MAJOR RESULTS AND DISCUSSION 16 Colonization and community development on transplanted log in managed vs. natural forest 16 Conservation value of restoration fire 18 Nutritional based functional groups 23 Attraction of saproxylic beetles 24 CONCLUSIONS 25 ACKNOWLEDGEMENTS 26 REFERENCES 27 TACK 35

INTRODUCTION

The Fennoscandian boreal forest, part of the western Eurasian taiga, is typically dominated by the two coniferous species Pinus sylvestris L. and Picea abies (L.) Karst. In its southern, hemiboreal part the forest landscape is dominated by conifers on more poor soils, and temperate, broad-leaved deciduous trees such as Fraxinus excelsior L., Tilia cordata Mill., Ulmus glabra Huds. and Quercus robur L., on better soils. Further north, the conifers increase in importance. The temperate tree species still occur scattered in the southern boreal zone. Otherwise the boreal zone is dominated by the two conifers with an admixture of deciduous trees such as Betula pubescens Ehrh., B. pendula Roth, Populus tremula L., Salix caprea L., Alnus incana L., Prunus padus L. and Sorbus aucuparia L. (Ahti et al. 1968). The primeval boreal forest was structured by different disturbance regimes. Fire, windstorms, insect, and fungal outbreaks created a variable forest landscape subjected to both large-scale stand-replacing disturbances and small-scale gap dynamics (Esseen et al. 1997; Engelmark and Hytteborn 1999; Kuuluvainen 2002). High biodiversity and characteristics of natural boreal forests were promoted by variation in fire frequency, high volumes of deciduous and coniferous dead wood, and forests that varied in age, structure and species composition (Esseen et al. 1997; Siitonen 2001). Fire was a fundamental process in the boreal forest ecosystem. The variation in fire frequency, its severity, and timing created a mosaic landscape with forest stands of different successional stages (Zackrisson 1977; Wein and MacLean 1983; Pyne et al. 1996; Niklasson and Granström 2000; Ryan 2002). The heterogeneity and variation created by fire was essential for maintaining original biodiversity. In addition, depending on intensity, fires created large input of dead wood, a key substrate for boreal species richness (e.g. Harmon et al 1986; Spies et al. 1988; Siitonen 2001, Jonsson et al 2005). At landscape and centennial scales, species diversity and species richness were favored by fire perturbation since disturbances of intermediate frequency and size enables coexistence of early and late successional species (Connell 1978). Since fire is a natural feature of the boreal forest and as fire-affected substrates are historically a common habitat, evolutionary strategies to cope with fire have evolved and forest living species

7 adapted to or even dependent on fire disturbance are widespread (Rowe 1983; Wikars 1992, 2001; Granström and Schimmel 1993; Penttilä and Kotiranta 1996; Hyvärinen et al. 2006). The natural fire return interval has varied depending on degree of human impact, climate, altitude, and site type (Niklasson and Granström 2000; Niklasson and Drakenberg 2001). In Swedish Pinus sylvestris forests of dry dwarfshrub type (Vaccinium type; Arnborg 1990) the typical fire return interval has been between 20-100 years (Zackrisson 1977; Engelmark 1984; Niklasson and Drakenberg 2001). In Picea abies forests occurring on more mesic-moist sites fire disturbance has varied considerably from one to several centuries, and fire refugia occurred in areas of more oceanic climate in western parts of Fennoscandia (Hofgaard 1993; Ohlson and Tryterud; 1999). The last century of forest management has changed the dynamics and structure of the boreal forest. Especially the last 50 years, has experienced an intense industrial forest management that has dramatically reduced the area of natural forest. Today the boreal forest landscape is dominated by large areas of young, even-aged coniferous monocultures (Linder and Östlund 1998; Axelsson and Östlund 2001; Kouki et al. 2001). Consequently, about 95% of the Swedish boreal forest has been used by modern forestry and only 2% is covered by natural forests (Berg et al. 1994, Fridman 1999). In addition, effective fire suppression has increased the area of even-aged monocultures and early post-fire successional stands are now extremely rare (Esseen et al. 1997; Linder et al. 1997; Kouki et al. 2001; Uotila et al. 2002). Lack of fire has lead to a shift in the forest structure and many unmanaged stands previously dominated by Pinus sylvestris are now dominated by the more shade tolerant and fire sensitive Picea abies (Engelmark 1987). Another significant change is the decline of living and dead deciduous trees (Linder et al. 1997; Niklasson and Drakenberg 2001; Lindbladh et al. 2003; Kouki et al. 2004; Jönsson et al. 2008). As a result of the intense forestry, patches of natural forest now occur isolated in a matrix of managed forest. This fragmentation of natural forest habitats include both habitat loss, edge effects (i.e. patch size) and isolation (i.e. distance), and constitutes a major threat to biodiversity (Andrén 1994; Saunders et al 1991; Harrison and Bruna 1999, Gu et al. 2002). The effects include declining species population sizes, loss of genetic variation and genetic drift, factors that significantly increase extinction risks due

8 to stochastic events (e.g. Rosenzweig 1995; Hanski 1999a). The capacity of boreal forest organisms to colonize remnant and fragmented habitats is related to their dispersal ability and the smaller and more isolated the habitat is, the smaller probability of being colonized (Hanski 1999b). In Fennoscandia there are many examples of species that show strong population declines due the ongoing reduction of natural forest area (Dettki et al. 1998, Edman et al. 2004a; Penttilä et al. 2006; Hedenås and Ericson 2008). Decreasing genetic variation, with reduced heterozygosity (Högberg and Stenlid 1999; Franzén et al. 2007) and reduced spore vitality (Högberg 1998; Edman et al. 2004a) have for instance, been shown for wood-decaying fungi in isolated populations in southern Sweden. Thus there are strong indications that, the fragmented Fennoscandian boreal forest could be facing a great species loss due to a time-lagged extinction dept (Tilman et al. 1994; Hanski 2000; Berglund and Jonsson, in press). The single most important component that has affected species diversity more then any other recent change in the Fennoscandian boreal forest landscape is the decrease in the amount of dead and dying trees (Linder and Östlund 1998; Sippola et al. 1998; Jonsson 2000; Siitonen 2001, Jonsson et al. 2005). Decaying wood is of key importance for a broad range of forest living organisms and also essential for structural heterogeneity, nutrient cycling and carbon dynamics (Harmon et al. 1986; Spies et al. 1988; Siitonen 2001; Jonsson et al. 2005). Depending on intensity, fire disturbance may create large inputs of dead wood (Spies et al. 1988; Linder et al. 1998; Siitonen 2001). In addition, fire will also increase dead wood heterogeneity, with a variation ranging from wood unaffected by fire to heavily charred wood. This variation is important for the species richness of wood-inhabiting fungi (Penttilä and Kotiranta 1996, Penttilä 2004; Olsson and Jonsson, Paper II). However, fire can also consume large amounts of dead wood (Knapp et al. 2005), particularly logs and snags in advanced decay classes (Eriksson et al., in prep.). The average volume of coarse woody debris, CWD (≥10 cm) in Swedish managed forests is today 6 m3 ha-1 compared with an average around 80 m3 ha-1 in natural forests (calculated from Fridman and Walheim 2000 and Siitonen 2001). However, higher volumes of CWD (>10 m3 ha-1) may occur in over-mature managed stands, although usually with smaller variations in size, quality, decay class distribution

9 and lack of large dead trees (Kruys et al. 1999, Siitonen et al. 2000, Rouvinen et al. 2002; Storaunet et al. 2002; Penttilä 2004; Jönsson and Jonsson 2007).

Wood-inhabiting fungi

The concept wood-inhabiting fungi is broad and does not refer to any taxonomically defined group. In this thesis the concept includes mainly polypore and corticoid fungi in the subclass Hymenomycetidae in Basidiomycota (Hansen and Knutson 1997). However, a few wood-inhabiting species in Ascomycota are also included. Wood-inhabiting fungi can be divided into three groups based upon their different nutritional strategies, wood- decaying, mycorrhiza and litter and humus decaying fungi. In Sweden more than 200 polypores and 550 corticoids have been found (Stenlid et al. 2008) and about 200 of these species are red-listed (Gärdenfors 2005). Wood-inhabiting fungi are of considerable importance for a wide range of forest living organisms and processes in the boreal forest. Parasitic wood-inhabiting fungi weaken and kill trees and thus create standing and lying dead wood (Rayner and Boddy 1988). In addition, wood-decaying fungi play an important role in the succession and decomposition of dead wood, and they are involved in important processes creating new substrate and structural heterogeneity, nutrient cycling and carbon dynamics (Harmon et al. 1986; Spies et al. 1988; Siitonen 2001; Jonsson et al. 2005). Siitonen (2001) estimated that at least 4000, maybe up to 5000 or more species are saproxylic. Besides fungi, the majority of the saproxylic species are insects (Coleotera, Hymenoptera and Diptera), that often utilize fruiting bodies and mycelia of wood-inhabiting fungi for feeding and as breeding ground (Jonsell and Nordlander 1995; Økland 1995; Hågvar 1999; Jonsell et al. 1999; Komonen 2001; Johansson et al. 2006).

Dispersal of wood-inhabiting fungi

Among wood-inhabiting fungi, dispersal can be divided into airborne spore dispersal, vegetative mycelial growth and dispersal by various animal vectors. The most common dispersal strategy is with airborne spores. The majority of the species have hyaline and

10 light spores with a size less than 10 μm making them suitable for wind dispersal. Several species have high dispersal ability and spores from Heterobasidion annosum, Laurilia sulcata and Peniophora aurantiaca have been trapped from 100 km up to 1000 km away from the nearest known occurrence (Kallio 1970; Hallenberg and Küffer 2001, Josefsson 2002). In addition, wood-inhabiting species have high spore production. Penttilä et al. (1999) estimated that the corticoid and red-listed species Phlebia cetrifuga released 3 x 104 spores per cm2 hymenium and hour, and for H. annosum Kallio (1970) trapped 7.2 x 105 spores per dm2 hymenium and day, 1 m from the fruiting body. However, only 0.1 % of the spores were collected 100 m from the fruiting body and the generally the majority of wind dispersed spores are deposited close to the fruiting body (Nordén and Larsson 2000). For successful long distance dispersal, fungal spores have to be resistant to dehydration and UV-radiation (Deacon 1997) and this may restrict their dispersal capacity since most of the species have short-lived hyaline spores. Dispersal with vegetative mycelia or rhizomorphs occurs in the soil between suitable substrate units and within single substrate units, searching for new resources. Vegetative growth of the mycelium allows the fungus to translocate water, carbon and mineral nutrients from the surrounding during the establishment (Boddy 1999; Fricker et al. 2008). Mycelial growth between trees or between stumps and trees through root contact is a common strategy for the rot root, H. annosum (Stenlid 1985). Dispersal with growing mycelial cords and rhizomorphs often results in aggregated distribution patterns and is generally found in the wood-decaying genera Recinicium, Phanerochete and Coniophora (Kirby et al. 1990; Boddy 1999; Edman and Jonsson 2001) A well-known example is the parasitic fungus Armillaria bulbosa, were a single clone extending over 15 ha and estimated to be about 1500 years old has been observed (Smith et al. 1992). Vector dispersal by insects can be both active and passive. Active dispersal has been intensively studied among Ascomycete fungi. Bark beetles carry blue stain fungi, e.g. Ophistoma spp. in special pockets called mycocangia (e.g. Lawrence and Britton 1994), and deliberately inoculate the fungus into the tree (Pettey and Shaw 1986; Paine et al. 1997). Another example of this mutualistic relationship is the corticoid Amylostereum areolatum dispersed by wood wasps, Sirex spp. (Talbot 1977; Vasiliauskas et al 1998). It has also been shown that different species of wood-inhabiting fungi, e.g. Fomitopsis

11 pinicola, can be isolated from wings and body cavities of bark beetles (Harrington et al. 1981; Pettey and Shaw 1986; Hsiau and Harrington 2003). However, whether animals, birds and insects act as passive or active vectors may vary and is often not known (Harrington et al. 1981; Gilbertson 1984).

Establishment and community development

Wood-inhabiting fungi may colonize dead wood from vegetative mycelia, sexual or asexual spores, and latent present propagules or from animal vectors (Rayner and Boddy 1988; Boddy 1999; Talbot 1977; Pettey and Shaw 1986; Paine et al. 1997). Hence, the establishment processes are dependent on the type of arrival and access to suitable resource, and therefore occurring largely by chance (Boddy 2001). However the often mutualistic relationship with insects (see above) facilitates the fungal entrance, avoiding the hostile surface environment. For example, Amylostereum areolatum carried in mycocangia within the abdomen of female wood wasps (Sirex spp.) is inoculated through the bark together with the wasp eggs (Talbot 1977; Vasiliauskas et al 1998). The wood- inhabiting fungal community can be divided into three major life strategies: ruderal (R- selected), stress-tolerant (S-selected) and competitive (C-selected) (Cooke and Rayner 1984; Rayner and Boddy 1988; Boddy and Heilmann-Clausen 2008). The different strategies overlap and wood-inhabiting fungi may during different environmental conditions combine two or three strategies. In the absence of competitors, fungal establishment of a suitable substrate follows primary resource capture strategies (i.e. dead wood after fire disturbance or fresh logs from windstorms), whereas secondary resource capture occurs later in the succession often involves competition over suitable resources (Rayner and Boddy 1988). The first saprotrophic wood-decaying fungi to colonize fresh logs are usually airborne spores from white rot Basidiomycetes (Rayner and Boddy 1988). Fresh logs is a competition-free substrate which is suitable for ruderal species that have an effective dispersal, early arrival with additionally early exit due to lowering in nutrients, competition from other species or changed microclimate conditions (Boddy 2001). In addition to wind dispersal, latent present fungal propagules within the wood have shown

12 to be an important part of the early fungal community development on angiosperms (e.g. Chapela and Boddy 1988; Boddy 2001). Although not sufficiently studied, this could potentially be an important feature for colonization patterns on conifers as well. However, there are many different features that are important for a successful fungal colonization and community development. Abiotic factors such as different disturbance regimes (e.g. Siitonen 2001) to microclimatic conditions like temperature and moisture play a role during the colonization (Rayner and Boddy 1988). In addition, biotic factors for example the dead-wood quality such as size, host tree, and decay class may also be important (e.g. Renvall 1995). The general characteristic pattern of dead wood communities is that species replace one another through decomposition during changes in moisture and nutritional content. However, several wood-decaying fungal species succeed specific primary decayers. They either utilize the dead or dying mycelia or are otherwise associated with the specific substrate created by the primary decayer (Niemelä et al 1995; Holmer et al. 1997). Such specific successional pathways add to the overall variability of the community structure (Renvall 1995).

OBJECTIVES OF THIS THESIS

The general aim of this thesis is to describe the colonization patterns of wood-inhabiting fungi to better understand the effects on the fungal community of restoration fires and forest management aiming at increasing the amount of dead wood. Specific objectives are: 1. Compare colonization and community development on experimental logs in different stand types with contrasting history of forest management (I). 2. Assess the conservation value of restoration fire for wood-inhabiting fungi (II). 3. Analyse whether different functional groups of wood fungi differ with regard to their colonization of fresh (I) or newly disturbed dead wood substrates (II). 4. Test whether saproxylic beetles distinguish between different types of fungal substrates and may they act as important dispersal vectors (III, IV).

13 MATERIAL AND METHODS

Study areas

The study areas are located within the middle and northern boreal zones (Ahti et al. 1968) in the counties of Västernorrland and Västerbotten, northern Sweden (Fig. 1). The dominant forest site types in the study areas I, III, and IV are of mesic dwarfshrub type and moist dwarfshrub type (Arnborg 1990). Norway spruce, Picea abies (L.) Karst. is dominating the tree layer and to a variable extent mixed with Scots pine, Pinus sylvestris L., birches Betula pendula Roth and B. pubescens Ehrh., and more rarely Aspen, Populus tremula L. and Goat willow, Salix caprea L. The study area in II is dominated by xeric dwarfshrub type to dry dwarfshrub type (Arnborg 1990) with Pinus sylvestris as the dominate tree species with only scattered occurrences of Picea abies. The study areas vary from mature managed forests (I, II, and IV) to old growth forest (I, III and IV).

15° 20° ı ı

- 65°

Umeå - 64°

15° 20° ı ı

- 65°

Umeå - 64°

ı ı 150 km

Figure 1. Location of the study areas. Open squares = Paper I, filled square = Paper II, open circles = Paper III and filled circles = Paper IV.

14 Study design

Details on the design of the four studies are given in the respective papers and here only brief descriptions are given Paper I, is an experiment including transplanted logs in mature managed forest and protected forest areas (7 of each category). The early colonization was followed during the first four years with an inventory of colonized species at one and four years after log transplantation. Complementary data on stand structure and a pre-inventory of the wood fungal community were also collected. Paper II, is a study of the colonization of wood fungi after a restoration fire. It includes one area burned and a stand of similar structure as a control. Inventories were done the year before the fire and the changes in the fungal community of 319 logs were followed during 5 years after the fire. Papers III and IV, address the possibility that certain beetles are attracted by the odor of fungi and thus have the potential to act as dispersal vectors. The first study (III), screens for the presence of specific species showing attraction to four fungi (Fomitopsis rosea, F pinicola, Phellinus chrysoloma and Phlebia centrifuga) and also compares mycelia with fruiting bodies. The second study (IV), extends the first by comparing the attraction in different forest landscapes representing a gradient in forestry intensity.

Sampling methods

The fungal community was sampled on the experimental logs (I) and natural logs (II) by the presence of fruiting bodies. Although, representing only a subset of the fungal community, this is standard procedure when studying dead wood fungi, as alternative methods based on the occurrence of mycelia are impossible to perform in studies including a large number of logs. To allow reliable identification of the species, numerous samples were collected in the field and subsequently checked by using microscopic characters. Some difficult specimens were also sent to experts for verification.

15 A window trap which allowed the use of bait was constructed. These traps were baited with either pieces of dead wood, pieces of fruiting bodies or fungal mycelium. Empty un-baited traps were used as controls. The different mycelium substrates (III and IV) consisted of dikaryotic mycelium that I isolated from fresh fruiting bodies (Fomitopsis pinicola, F. rosea and Phlebia centrifuga). The isolated mycelium was grown on Hagem agar and after two weeks small pieces of mycelium was placed on sterilized 0.8 cm thick P. abies discs with a diameter of 7 – 8.5 cm. The wood discs were then incubated in serial environment in room temperature for 2.5 months. I sampled fruiting bodies (III) from F. pinicola, F. rosea and Phellinus chrysoloma one day before exposure and kept them separated in paper bags at low temperature. The different substrates were put in sterile mesh bags and placed in special window traps (see Paper III for description of the window trap).

MAJOR RESULTS AND DISCUSSION

Colonization and community development on transplanted log in managed vs. natural forest

Intensive forest management has dramatically reduced the area of natural forest in boreal Fennoscandia, a process that has negatively affected saproxylic organisms including many wood-inhabiting fungi. Today differences in species richness and species composition, between natural and managed forests are striking. (Bader et al. 1995; Edman et al. 2004b; Penttilä et al. 2004; Stokland and Kauserud 2004; Junninen et al. 2006). Our data on the early colonization of the experimental spruce logs revealed no significant difference in species composition between the two stand types. This contrasted to the difference in species composition on the existing CWD found in the pre- inventory and the different spore deposition patterns found between the stand types (Fig. 2).

16 700

600

500

400

300

200

100 Spore deposition per m2 x 24 h 24 m2 x per deposition Spore 0 F. pinicola F. rosea P. centrifuga S. odora

Figure 2. Average spore deposition (± SE) for Fomitopsis pinicola, F. rosea, Phlebia centrifuga and Skeletocutis odora in three (Gammtratten, Herrbergsliden and Rödberget) out of the seven forest areas included in (I). Grey: reserve stands, white: managed stands. The values are calculated from the number of heterokaryotisations found on exposed wood discs inoculated with primary mycelia.

The lack of difference between the two stand types implies a relatively fast colonization regardless of the general abundance of fungi in the local stand. In addition, differences in existing volumes of lying dead wood had only minor influence on the fungal species composition. This pattern was somewhat unexpected, since dead wood is one of the most important components for biodiversity in the boreal forest (e.g. Siitonen 2001). On the other hand, some of the managed stands in the study area showed old-growth qualities with relatively high volumes of lying dead wood (Fig. 1 in I) compared with the average volume of about 6 m3 ha-1 for lying dead wood in managed forests in Sweden (Fridman and Walheim 2000). Most of the fungi recorded on the logs were common ruderal species that have the ability to rapidly utilize new substrates. However, one species namely Fomitopsis pinicola clearly deviated from this pattern. F. pinicola is a common wood- decaying species throughout the boreal forest, and fruiting bodies were found on 72 logs in the reserve stands while only on 43 logs in the managed stands (p-value = 0.017). In addition, spore deposition also differed between the stand types (Fig. 2). The spore deposition patterns for F.roesa and P. centrifuga (Fig. 2) are in line with findings by Edman et al. (2004c) and Jönsson et al. (2008), who found that the actual colonization is influenced by the local availability of species. The colonization pattern of the experimental logs showed a major difference between the seven study areas. Study area as a covariate in the ordination analysis

17 explained as much as 68% in 2003 and 55% in 2006 of the variation in the species assemblage. During this early stage we may assume that the fungal community is mainly composed of fairly frequent and “ruderal” species. Many, if not most, declining and red- listed species are confined to the later stages of decay. In addition, many threatened wood-inhabiting fungal species require substrates of specific quality e.g. coarse woody debris, pre-rotted wood by specific fungal species, dead trees created by fire, wind, parasitic fungi and insects (Niemelä et al. 1995; Renvall 1995; Penttilä 2004; Edman et al. 2006), qualities which these logs are largely lacking. As the current study only concerns the initial stages of colonization we cannot yet answer to what extent the conservation value of a given log is dependent on the presence of an established population of threatened species.

Conservation value of restoration fire

The growing awareness of the negative consequences of the long and efficient fire prevention has resulted in an increasing use of prescribed and restoration fires in boreal Fennoscandia. Prescribed fire has been and is used in forest management for soil preparation after clear-felling and to reduce forest fuel to prevent catastrophic wildfires. However, the primary purpose with restoration fire is to recreate features of natural forest that have been lost during the long period of fire suppression. Compared with prescribed fire, restoration fire should try to mimic natural forest fires as far as possible. Results from the studied restoration fire (II) are consistent with findings by Penttilä and Kotiranta (1996), that the wood-inhabiting fungal assemblage was strongly influenced by fire disturbance and that species composition and community development following the fire are highly dynamic (Fig. 3, in paper II). The fire had a drastic effect on the logs present before the fire (Eriksson et al, in prep). Fire consumed large amounts of wood, particular in the decay stages 4 to 6 (Fig. 3). In addition, more than 65% of the logs were heavily charred (>60% log surface; Fig. 4) and the ground contact showed a marked decrease (Fig. 5).

18 50

10 Percent of consumption of Percent

0 123456 Decay stage

Figure 3. The wood consumption in the different decay stages (unpublished data, Eriksson in prep).

20 Number of logs of Number 10

0 0-20 21-40 41-60 61-80 81-100 Percent of charred surface area

Figure 4. Percentage charred surface area of logs after the restoration fire (n=150; unpublished data, Eriksson in prep.).

100

40 Number of logs of Number 20

0 0-20 21-40 41-60 61-80 81-100 Percent of ground contact

Figure 5. The ground contact of logs (n=150) before (white) and after (black) the restoration fire. Ground contact decreased significantly (p-value < 0.001, paired t-test), (unpublished data, Eriksson in prep.).

19 Large-scale disturbances such as forest fires are considered to support species of ruderal strategies with effective dispersal and fast colonization ability. Also stress- tolerant species that can cope with the new conditions following fire may increase as the conditions will become unsuitable for the majority of species dominant prior to the fire (e.g. Pugh and Boddy 1988; Penttilä and Kotiranta 1996). The early fungal community following fire is characterized by both non-decaying species together with species less effective in decaying wood, while in later stages more competitive species will increase in importance (Rayner and Boddy 1988). Our results (II) agree with these observations and during the first two years the majority of the colonizing species represent ruderal and stress tolerant strategies including species like Athelia spp., Botryobasidium obtusisporum, Galzinia incrustans, and the Ascomycetes Costantinella spp., Trichoderma viride. T. viride is a blue-green anamorphic mould that is common on ephemeral substrates. It was found abundantly on charred log surfaces but only in the same year as the fire. Despite the initial decline in species richness and the loss of some woody substrates due to the fire, most of the declining species showed an increase after four years and they were frequently found on logs strongly influenced by the fire. However, the fungal species composition was still quite different from the pre-fire community (Fig. 2 in II). Species that increased after the fire and which frequently occurred on charred logs four years after the restoration fire were; Antrodia sinuosa, B. obtusisporum, Phlebia subserialis and Tomentella spp. Three threatened, red-listed and fire-favored species (Renvall 1995; Penttilä 2004; Junninen et al. 2008; Stenlid et al. 2008) were found on the heavily charred logs in the fire area namely, Antrodia primaeva, Dichomitus squalens and Gloeophyllum carbonarium. These species have only been recorded a few times in Sweden; A. primaeva 11 times, D. squalens 15 times, while G. carbonarium has only been found 3 times in Europe (ArtDatabanken). However, not all species recovered after the fire. The red-listed species Antrodia albobrunnea, Odonticium romellii and Skeletocutis lenis all growing on heavily decayed logs were still missing four years after the fire (see Appendix in II).

20 Several of the species that decreased after the fire grew on logs in decay stages 4 to 6 (Fig 2 in II) that were strongly affected by fire (Fig. 3). However, it is difficult to evaluate if these species are unable to survive fire inside a fire area and thus depend on re-colonization from the surrounding landscape. Although fires will consume part of the wood substrate, fire disturbance may also create a large input of dead wood (e.g. Siitonen 2001). Four years after the restoration fire 61 new logs were found in the fire area compared with only 16 logs in the control area. In addition, the fire injured and killed a number of trees (data not shown) and this will even further increase the amount of lying dead wood. Pugh and Boddy (1988) called this type of disturbance for “enrichment disturbance”. This is mirrored by the fact that after four years twice as many species and four times as many records were observed on the new logs in the fire area compared with control area (Table 1). Including also colonization on new logs Penttilä (2004) showed that it took 6 years for the fungal community to host equal number of polypore species as in the pre-fire inventory. The relatively fast response of the fungal community in our study is probably related to fire-intensity. Our fire was of much lower intensity, compared with that studied by Penttilä (2004) where most of the living trees were killed. Thus, each restoration fire is unique and depending upon its intensity and other environmental conditions the outcome will vary.

21 Table 1. Observed wood-inhabiting fungi (mainly corticoids and polypores) on new logs, four years after the restoration fire in the fire area (n=61 logs) and the control area (n=16 logs). Red-listed species according to Gärdenfors (2005): NT = near-threatened.

Species fire area control area Botryobasidium obtusisporum 13 5 Hyphoderma praetermissum 12 6 Athelia epiphylla 9 3 Dacryobolus karstenii 8 1 Trichaptum fusco-violaceum 8 1 Panellus mitis 7 - Antrodia sinuosa 6 - Athelia fibulatat 5 2 Coniophora puteana 4 - Tubulicrinis subulatus 4 3 Antrodia xantha 3 - Botryobasidium botryosum 3 1 Botryobasidium subcoronatum 3 - Coniophora arida 3 - Hyphoderma setigerum 3 - Junghuhnia luteoalba NT 3 - Phlebiopsis gigantea 3 - Hypochnicium punctulatum 2 - Gloeophyllum sepiarium 2 - Hyphodontia hastata 2 1 Skeletocutis biguttulata 2 - Trichaptum abietinum 2 2 Athelia singularis 1 - Ceraceomyces sublaevis 1 1 Costantinella michenerii 1 - Hyphodontia breviseta 1 3 Hyphodontia subalutacea 1 1 Oligoporus hibernicus NT 1 - Oligoporus tephroleucus 1 - Peniophora pithya 1 - Phanerochaete sordida 1 - Phlebia radiata 1 - Phlebia subserialis 1 - Phlebiella boralis 1 - Pseudomerulius aureus 1 - Skeletocutis amorpha 1 - Stereum sanguinolentum 1 - Tubulicrinis calothrix 1 - Tubulicrinis gracillimus 1 - Tubulicrinis medius 1 - Tomentella sp. 1 - Amylocorticium cebennense - 1 Athelia bombacina - 1 Globulicium hiemale - 1 Hyphodontia pallidula - 1 Phanerochaete sanguinea - 1 Number of sampled logs 61 16 Number of species 41 19 Number of records 126 35

22 Nutritional based functional groups

Based upon their nutritional strategies, wood-inhabiting fungi can be classified in four different functional groups, namely wood-decaying fungi causing white rot, wood- decaying fungi causing brown rot, litter- and humus-decaying fungi, and mycorrhizal fungi (I, II). However, this classification into functional groups is complicated by the complex life style of many wood-inhabiting fungi. For example, some fungi may change strategy from biotrophic to saprotrophic (Cooke and Whipps 1993). Several studies have also shown that ectomycorrhizal fungi may compete with saprotrophs for organic nutrients (Gadgil and Gadgil 1971, Lindahl et al. 1999), and wood-inhabiting ectomycorrhizal fungi contain genes for ligninolytic enzymes (Chambers et al. 1999, Chen et al. 2001). In addition, Vasiliauskas et al. (2007) found that some wood-decay fungi have the ability to colonize fine roots of tree seedlings. Both on the experimental logs (I), and after the restoration fire (II) the litter- and humus-decaying fungi showed a rapid response to the “new” substrate followed by a decline to more natural levels already after a few years (Fig. 4 in I, Fig 4 in II). Characteristic features for the litter- and humus-decaying group are; thin, often inconspicuous fruiting bodies and occurrence on dead wood in many different decay stages, as well as on other kinds of organic debris and soil. White-rot fungi also responded relatively fast to the input of new substrate and dominated after five years (Fig. 4 and 5 in I). White rotting Basisiomycetes are the first wood-decaying fungi to colonize fresh logs (Rayner and Boddy 1988). Important white- rot fungi on the experimental logs were Phlebiopsis gigantea, Stereum sanguinolentum and especially Trichaptum abietinum that occurred on more than 60 % of the logs (Appendix in II). However, the white-rot fungi declined the first two years following the restoration fire (Fig. 4 in II). The restoration fire consumed rather much of the logs in decay stage 4 to 6 and since strongly decayed logs often have higher lignin contents, much of the suitable substrate for white-rot fungi was lost. Hence, white-rot fungi are often the dominating nutritional strategy in both the early and late stages of wood decay (Renvall 1995).

23 Brown-rot fungi play a fundamental role in the decomposition of coniferous wood, generally preferring intermediate decay stages. In particular, they characterize Pinus sylvestris logs in dry habitats (Renvall 1995). Their response to fire paralleled that of the white-rot fungi, although less pronounced (Fig. 4 in II). However, it is reasonable to assume that brown-rot fungi will continue to increase in coming years since other studies have shown that many brown-rotting species show a general increase in frequency after fire disturbance, for example species such as Antrodia spp., Coniophora arida, Gloeophyllum spp., Leucogyrophana romellii, Oliogoporus placenta, and O. sericeomollis (Eriksson 1958; Renvall 1995; Penttilä and Kotiranta 1996; Lindgren 2001; Penttilä 2004). The mycorrhizal fungi were infrequent in the early succession but after five years they showed the same frequency on the experimental logs as in the pre-inventory (Fig. 4 in I). Amphinema byssoides and Piloderma byssinum were commonly found on experimental logs after five years. After the fire disturbance the mycorrhizal fungi showed an unchanged occurrence compared to the pre-fire inventory which may reflect that the restoration fire was of rather low intensity (cf. Dahlberg 2002). However, Tomentella spp. and Tomentellopsis echinospora increased and were only found on heavily fire-affected logs with high degree of burn and their fruiting bodies were common on charred log surfaces (Appendix in II).

Attraction of saproxylic beetles

Wood-inhabiting fungi house a species rich fauna of various insects that either feed on their mycelia or fruiting bodies (Ehnström and Axelsson 2002). Several insect species also known to act as vectors (Talbot 1977, Piane et al. 1997). To which extent, saproxylic beetles are involved as passive or active vectors for the dispersal and colonization of wood-inhabiting fungi that occur on lying dead wood is however poorly understood. In one study, we examined whether mycelium-infected wood and fruiting bodies attracted different beetles species (III). The results clearly showed that some beetle species do discriminate between different fungal substrates. The bark beetle Dryocoetes autographus (Ratz.) was significantly more often attracted to traps baited with growing

24 mycelia of Fomitopsis rosea compared with fruiting bodies of F. rosea as well as other fungal substrates. Furthermore, it was also common on sterilized wood (Fig. 1 in III, Fig. 4 in IV). In addition, the predatory staphlinid Lordithon lunulatus (L.) also discriminated between the substrates and preferred fruiting bodies of F. pinicola compared with the control and sterilized wood and also tended to be overall more common on the fungal substrates (Fig. 1 in III). The preference for growing F. rosea mycelium shown by D. autographus is interesting since F. rosea is a red-listed and rare species in managed Fennoscandian forest and D. autographus is a common cambium-feeding bark beetle attacking recently dead spruce trees and fresh logs (Ehnström and Axelsson 2002). D. autographus is also well adapted to cool climates as it has a flexible generation time (up to three years) and can have several generations on the same substrate (Johansson et al. 1994a,b). D. autographus has recently been found to utilize experimental logs up to at least three years (Therese Johansson, pers. com.). As F. rosea may produce fruiting bodies already on 4 – 5-year old logs it is reasonable to assume that D. autographus may be involved in the colonization process, or utilize the growing mycelia of F. rosea. This suggests that the role of saproxylic beetles needs to be assessed further and in particular whether the ongoing fragmentation of boreal forest will result in linked extinctions (cf. Komonen et al. 2000). In the associated study assessing whether forest landscapes that differ with regard to the amount of old-growth forest we documented major effects on the assemblage of saproxylic beetles (IV).

CONCLUSIONS

My work has dealt with the importance of downed dead wood, a substrate of key importance for wood-inhabiting fungal biodiversity in the boreal forest. In total, around 50 %, of the red-listed and threatened species in the Swedish forest landscape including several hundreds fungi suffer from insufficient amounts of dead wood (Gärdenfors 2005). This shortage of dead wood does not only concern crude volumes but, as indicated by the results from the restoration fire, the lack of specific qualities of dead wood. Although

25 only found on single logs, the presence of the vary rare and post-fire favored Gloeophyllum carbonarium, Antrodia primaeva and Dichomitus squalens on logs strongly affected by fire indicate the potential to increase the abundance of fire influenced and charred logs in the forest landscape. The majority of the “older” dead wood in the Fennoscandian boreal forest originated in a primeval forest landscape structured by a variation of natural disturbance regimes. Differences in fire frequency and severity created a variation of standing and lying dead wood, including wood from different tree species. In addition, repeated fires created fire-scarred trees, and especially in pines with a high content of resinous wood. These special types of dead wood may favor many of the red-listed species utilizing dead pine-wood either by strict dependence or by changed competitive interactions with generalist species. Active measures in the silvicultured forest landscape such as creating different types of dead wood are needed and currently discussed as, at least a part of, management and restoration of protected forests. An important measure for increasing the boreal forest biodiversity is to create substrates and habitats like dead wood, largely missing in the present managed forest. However, it is still too early to evaluate the conservation value of cut logs for specific red-listed and threatened species but clearly several species will benefit from these substrates.

ACKNOWLEDGEMENTS

Thank to Lars Ericson, Bengt Gunnar Jonsson, Mattias Edman and Antoine Bos for commenting and correcting on earlier versions of the thesis. The work in this thesis has been funded by the centre of Environmental Research in Umeå (grants to J. Hjältén, L. Ericson and B.G. Jonsson).

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34 TACK

Jag vill först tacka mina härliga handledare Lars Ericson och Bengt Gunnar Jonsson för ert stöd och engagemang. Lasse för ditt brinnande intresse för allt vad ekologi heter. Bege för att du alltid är positiv och intresserad av att diskutera mina idéer å det var ju så det började en gång med ex-jobbet.

Mattias som kompis och kollega har det alltid varit givande och kul att diskutera allt från vedsvampar till fågelskådning.

Forskargruppen det har alltid varit roligt att träffas och diskutera forskning med er – Bege, Nic, Mattias, Håkan, Karin, Marie, Shawn, Anna-Maria och Fredrik.

Joakim och Therese för givande samarbete

Alla som hjälpt till i fält – Peter, Patte, Ante, Lena, Daniel, Marita, Pappa, Hjalmar, Elsa och Cilla

Alla Doktorandpolare under de här dryga fem åren

Alla som jag har haft nöjet att undervisa med – Åsa H, Åsa G, Anders, Olle, Tommy, Per-Anders, Elisabet, Henrik, Sovapåmagen-Marcus, Tussan, Ullis, Stig-Olof, Darius, Johannes, Patte

Alla kollegor på institutionen

Pappa och mamma för all hjälp och support

Mina älskade barn – Hjalmar, Elsa, Ebba och Rut

Min älskade Cecilia