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The relative importance of stand and dead wood types for wood-dependent lichens in managed boreal forests
Fungal Ecology 20 (2016) 166e174
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The relative importance of stand and dead wood types for wooddependent lichens in managed boreal forests € ran Thor a, Måns Svensson a, *, Victor Johansson a, Anders Dahlberg b, Andreas Frisch a, Go Thomas Ranius a a b
Department of Ecology, Swedish University of Agricultural Sciences, P.O. Box 7044, SE-750 07 Uppsala, Sweden Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences, P.O. Box 7026, SE-750 07 Uppsala, Sweden
a r t i c l e i n f o
a b s t r a c t
Article history: Received 2 July 2015 Received in revised form 13 December 2015 Accepted 31 December 2015 Available online xxx
For efficient conservation, we need to consider both what kinds of habitat species require and the landscape-level supply of these habitats. We examined the relative importance of stand and dead wood types for wood-dependent lichens in two managed boreal forest landscapes in Sweden. We found 20 species and modelled their abundance based on stand type and dead wood characteristics using hierarchical Bayesian models or point estimates. Stands <60 years both have a large total extent and a large proportion of dead wood, resulting in the main part of the populations of most wood-dependent lichens occurring there. Older managed stands and unmanaged mires harbour smaller proportions of the populations. Stumps and snags, and to some extent logs, had high abundances of many species of wooddependent lichens in managed forest landscapes, while dead branches were used by few species. Measures taken to produce more snags should benefit wood-dependent lichens in managed landscapes. © 2016 Elsevier Ltd and The British Mycological Society. All rights reserved.
Corresponding editor: Darwyn Coxson Keywords: Biodiversity Coarse woody debris Fine woody debris Forested mires Lignicolous Saproxylic
1. Introduction Forests managed for timber production differ in several respects from forests with natural dynamics: the average tree age is lower, the tree species composition is more homogeneous, and there are € fewer dead and dying trees (Ostlund et al., 1997; Brassard and Chen, 2006; Cyr et al., 2009; Paillet et al., 2010). Therefore, species dependent on old and dead trees are suffering from habitat loss in managed forest landscapes. In forests harvested by clear-felling, there is also a large variation in habitat quality among stands. This is because clear-felling forestry leads to a landscape composed of even-aged stands at various successional stages, which vary widely in the amount and quality of habitat they provide for forest species € fman and Kouki, 2001; Paillet et al., 2010; Turner et al., 2011). (e.g. Lo Numerous forest species are dependent on dead wood (in Fennoscandia: 25e30%; Siitonen, 2001). Forest management for timber and pulp production means that trees are removed that otherwise would have turned into dead wood. Therefore, the amount of large-
* Corresponding author. E-mail address: [email protected] (M. Svensson). http://dx.doi.org/10.1016/j.funeco.2015.12.010 1754-5048/© 2016 Elsevier Ltd and The British Mycological Society. All rights reserved.
diameter dead wood in managed forests is typically only a small fraction of that in old-growth forests (Siitonen, 2001; Brassard and Chen, 2006). As a consequence, the distribution area and the populations of many wood-inhabiting species are decreasing, and many of them are nationally red-listed (e.g. Tikkanen et al., 2006; Stokland et al., 2012). In Europe, only small patches of unmanaged forest remain, and therefore the amount and quality of dead wood in managed forests play a decisive role for landscape-scale dead wood availability (Stokland et al., 2012). The amount of dead wood can be increased by various conservation measures, such as leaving forests unmanaged, prolonging rotation periods, retaining trees and creating dead wood at clear-felling, or by using alternative management systems, such as selective cutting (Jonsson et al., 2005; Stokland et al., 2012). An opposing trend is the increasing interest in intensified forest production, for example involving harvest of wood residues for bioenergy production (Walmsley and Godbold, 2010; Gan and Smith, 2011) and shortened rotation periods (Jactel et al., 2012). Such practices will likely further decrease the amount of dead wood. Lichens on wood comprise a species rich group in boreal forests. In Fennoscandia, 378 lichen species occur on wood, of which 97 are considered dependent on this substratum (Spribille et al., 2008).
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Among wood-dependent lichens, many species are considered to be typical of old forests (Spribille et al., 2008; Swedish Species Information Centre, 2015), but there are also several species known to occur in young managed forests on stumps or slash originating from clear-felling (Caruso et al., 2008; Svensson et al., 2013). A key factor determining the future distribution and abundance of wood-dependent lichens is forest management, which drives habitat availability for many species. To understand the impact of management, knowing the landscape-scale distribution of species is necessary. However, such data are only available to a limited extent for forest organisms (e.g., polypores: Berglund et al., 2011; saproxylic beetles: Schroeder et al., 2007; Jonsell and Schroeder, 2014) and lacking for lichens. Lichens are often only studied in managed mature or unmanaged stands, while young managed forests are not considered ~ hmus and Lo ~ hmus, 2011). Young forests may, however, possess (Lo € m et al., structures which support a high species richness (Lundstro 2011; Rudolphi and Gustafsson, 2011; Fuller, 2013). Another type of land rarely considered is low-productivity land not used for forestry, such as forests on rocky ground or forested mires. Such low-productivity forest has been considered to support low species richness (e.g. Jasinski and Uliczka, 1998), but no field studies have systematically compared the conservation values of lowproductivity forests and more productive forests. When species experts evaluated the potential conservation value of lowproductivity forests in Sweden, they concluded that these forests may be important especially for some insect and lichen species that are favoured by sun exposure and slow-growing trees (Cederberg et al., 1997). Since the area of low-productivity land is often large (in Sweden, 18% of all forest land is low-productive, i.e. with a potential forest growth <1 m3 ha1; Swedish Forest Agency, 2013) such forests may contribute substantially to landscape-scale habitat availability for forest species. The aim of this study is to provide a quantification of wooddependent lichen populations and their distribution among stand types and dead wood types in two boreal forest landscapes. We assessed the landscape-level population size of individual lichen species using models of their abundance on different dead wood types (stumps, logs, snags and branches) in five different stand types in two forest landscapes in southern Sweden. We calculated the proportion of the landscape-scale population that occurs (i) in different stand types, and (ii) on different types of dead wood. Despite their comparatively low total area, we expected the total abundance of several species to be higher in older managed forests, due to a higher abundance per area caused by larger amounts of logs and snags originating from natural tree mortality in these stands. Further, we expected unmanaged, forested mires to serve as a refuge for wood-dependent lichens which may be rare in the managed part of the landscape. Finally, among dead wood types, we expected stumps and branches on the ground to be important for many species, since they constitute major types of dead wood in managed forests. 2. Material and methods 2.1. Study landscapes Two landscapes in southern Sweden were selected for the study, each covering ca. 150 km2. One is located in the provinces of €stmanland (hereafter referred to as the Northern Dalarna and Va € rs, 1999), landscape) in the middle-boreal vegetation zone (Sjo 60 050 N, 14 050 E, elevation 300e400 m.a.s.l.; the other is in € €tland (the Southern landscape) in the boreonemoral zone, Osterg o 58 480 N, 15 410 E, 60e70 m.a.s.l. Both landscapes are dominated by forests managed by clear-felling, with legally protected,
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unmanaged forests making up <0.3% of the area. The forested land is mainly composed of monocultures or mixed stands of Picea abies and Pinus sylvestris, with some deciduous trees intermixed, mainly Betula pendula, Betula pubescens, and Populus tremula. The forests are typically cut after 80e100 yr. In the study landscapes, >95% are owned by a single forest company (Bergvik Skog AB in the Northern landscape and Holmen Skog AB in the Southern landscape), giving us access to stand databases with almost total landscape coverage. We surveyed stands of five types: four age classes of productive forests and one consisting of forested mires. The productive stands were divided into the age classes 0e20 yr (21.6% and 25.2% of the forested area in the Northern and Southern study landscapes, respectively), 21e60 years (40.0% and 45.4%), 61e110 yr (16.7% and 16.1%) and >110 yr (4.4% and 6.0%). The proportion of different age classes is similar to the Swedish average (Swedish Forest Agency, 2013). The forested mires (17% and 7% in the Northern and Southern study landscape, respectively) support open P. sylvestris stands with an annual productivity <1 m3 ha1 and are exempted by law from forest production (Jasinski and Uliczka, 1998; Swedish Forest Agency, 2013). Ten stands of each type were randomly chosen in each study landscape. Thus, 100 stands were sampled in total. 2.2. Sampling dead wood and lichens In every stand, dead wood and wood-dependent lichens were surveyed along two randomly placed transects (Marshall et al., 2000). This method has been used earlier in landscape-scale studies on wood-dependent organisms (e.g., Ekbom et al., 2006; Schroeder et al., 2007). Each transect was 100 m long and 10 m wide. One of the transects in each stand was oriented along a NeS axis and the other along an EeW axis. If a transect reached the stand edge prior to completion, its mid-point was shifted sideways by 20 m, to the north for an EeW transect and to the east for a NeS transect. The transect was then continued in the opposite direction. In the area covered by each transect, all dead wood objects fulfilling the criteria described below were recorded and their wood surface areas were estimated using a measuring tape or plastic grid. The types of wood recorded included logs (all), stumps (up to 100 cm height, all), snags (from 101 cm height, all), and dead branches on the ground (only coniferous, because deciduous branches decompose rapidly and were scarce). Dead branches on living trees were not included, since they have been found to be of little importance for wood-dependent lichens (Svensson et al., 2014). Dead wood objects were included if they had a wood surface area (i.e. area with no bark) of at least 25 cm2 and were at least 0.8 cm thick and 10 cm long. If a dead wood object extended beyond the area delimited by the transect, only the part found within the transect was included in the inventory. Lichens were surveyed in two plots that were 15 10 m each, randomly placed along each transect. In these plots, all dead wood objects were searched for the 96 lichen species classified as wooddependent (“obligate lignicoles”) in Fennoscandia by Spribille et al. (2008), excluding Cladonia botrytes as this species has been shown to be only facultatively lignicolous (Bogomazova, 2012). The abundance of wood-dependent lichens was estimated as the number of occurrences in 5 5 cm squares of a plastic grid, yielding a value equivalent to the proportion of occupied grid squares. Some types of dead wood were too rare to yield a sufficiently large sample size within the plots, and were instead surveyed for lichens along the whole transect. These included all snags, all deciduous wood, and all logs (with the exception of stands 0e20 yr, where logs are common). Lichen species were mainly determined in the field, but samples were collected when necessary and identified later using light microscopy and thin layer chromatography. The nomenclature follows Nordin et al. (2015). Field work was carried out during 2010e2012.
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2.3. Assessing species abundance
2.4. Landscape-scale dead wood simulations
We assessed species abundance in different stand types using two different approaches. Both approaches included the same three steps: (1) calculating estimates of species abundance for different dead wood types and stand types, (2) using stand databases and our dead wood inventory data to calculate landscape-scale dead wood amounts and (3) combining (1) and (2) to get landscape-scale quantifications of species' populations and their distribution among stand types and dead wood types. In this section, we describe step (1). For (2), see Landscape-scale dead wood simulations and for (3), see Combining abundance estimates and dead wood simulations. In the first approach for assessing species abundance, we made point estimates of abundance on different dead wood types in different stand types for all species. This was done by using mean abundances for each species on different dead wood types in each stand type. In the second approach, we modelled species abundance based on the characteristics of dead wood objects and forest stands using hierarchical Bayesian models (Gelman et al., 2004). This approach was in principle preferable as it allowed us to include uncertainty measures for the lichen abundance estimations, but it is more data demanding. Hence, we were only able to use this method for species occurring on >3% of the dead wood objects: Micarea misella, Mycocalicium subtile and Xylographa parallela. The genus Xylographa has been revised (Spribille et al., 2014) after the completion of our field work, which means that our recordings of X. parallela may also include X. pallens. We excluded Micarea denigrata, since a substantial part of the population of this species may occur on dead branches of living trees (Svensson et al., 2014), a dead wood type not included here. We used generalized linear zero-inflated Poisson models (ZIP), which are appropriate for count data (here number of squares in the plastic-grid) with an excessive number of zeroes compared to that assumed by a regular Poisson distribution. The ZIP model includes a binomial sub-model for occurrence probability and a count sub-model for abundance (Zuur et al., 2012). We used a Bernoulli distribution and a logit link function for the occurrence sub-model and a Poisson distribution and a log link function for the abundance sub-model. To account for additional overdispersion not caused by excess zeroes in the abundance part of the model, we included an observation level random error term. This term acts as a latent variable that will pick up any variation that cannot be explained by the explanatory variables or the random intercepts and would otherwise result in overdispersion (Zuur et al., 2012). The hierarchical Bayesian framework enables the utilization of explanatory variables measured at the stand level (i.e. at the higher hierarchical level), as we use them to model the standspecific intercepts (Gelman and Hill, 2007). Hence, the two types of response variable (occurrence and abundance) are explained both by dead wood object characteristics (lower level) and stand characteristics (higher level). Moreover, the model accounts for the unexplained variation between stands by including stand identity as a random error. We constructed the models by comparing versions with different combinations of the explanatory variables using the Deviance Information Criterion (DIC; Spiegelhalter et al., 2002). The models were fitted using OpenBUGS 3.2.2 (Thomas et al., 2006) using Markov Chain Monte Carlo (MCMC). We ran two MCMC chains for 110,000 iterations with a burn-in of 10,000 iterations. We thinned the chains by storing every 20th iteration, resulting in 10,000 stored values per parameter. We used uninformative prior distributions: Normal (0, 0.001) for all parameters associated with dead wood and stand characteristics, and Gamma (0.001, 0.001) for the precision parameters of the random intercepts.
For both approaches and for each study landscape, we simulated all dead wood objects within an area of 3 km2. Within the simulated areas, the proportion covered by each stand type was based on actual values obtained from databases of the landowners. Each simulated stand was allocated a size based on the mean sizes of stands for each study landscape and stand type. These stands were then assigned a number of dead wood objects of each type based on random draws from negative binomial distributions that had been fitted to the observed number of dead wood objects in each stand type (5 stand types and 10 dead wood types/stand type ¼ 50 distributions per study landscape). The size of each dead wood object was based on random draws from normal distributions fitted to the observed wood surface area (log transformed) of each dead wood type in each stand type. The predictions of dead wood objects were replicated in the same way as lichen abundance (i.e. 500 replicates), using one combination of the parameters for each replicate, from which we obtained the number of dead wood objects of each type and their sizes. Hence, for the three modelled species, the predictions of lichen abundance in the whole landscape include the uncertainty in the dead wood predictions. As the point estimates of abundance do not include any uncertainty measure, we used the median of the dead wood distributions for these estimates. 2.5. Combining abundance estimates and dead wood simulations For the first approach of estimating species abundance (see Assessing species abundance), we used the mean abundances on different dead wood types and the amount of these dead wood types in different stand types in a whole landscape (see Landscapescale dead wood simulations). We assessed for each species: abundance/ha in each forest type, the relative importance of different forest types (i.e. the proportional distribution of the total population among different forest types in the whole landscape), and the relative importance of different types of dead wood. For the second approach, we (1) estimated lichen abundance for each simulated dead wood object using the parameter estimates from our fitted models (Fig. S1), and (2) calculated the proportion of the total abundance on each dead wood type and in each stand type. Each estimation process (i.e. for one species in one landscape) was replicated 500 times. For each replicate, we randomly selected one combination of the parameters of the occurrence and abundance models from their joint posterior distributions. 3. Results We recorded 20,324 dead wood objects, of which 5719 were searched for wood-dependent lichens. Stands aged 0e20 yr contained the highest amounts of dead wood surface area per hectare, while forested mires had the lowest (Fig. 1). Snags were the least common substratum type in terms of surface area, while logs were the most common (Fig. 1). We recorded 20 wood-dependent lichens of which 16 occurred in the Southern study area and 18 in the Northern, and 14 species occurring in both study areas. One redlisted species (Hertelidea botryosa) was found. 3.1. The relative importance of stand types The majority of the species (17 out of 20) occurred with a higher abundance per hectare in managed forests and eight of them were only recorded there (Fig. 2). For half of the species, >50% of the landscape-scale populations occurred in managed forests 60 yr old (Figs. 2 and 3). Younger forests (60 yr) tended to be more important for the more abundant species (Figs. 2 and 3). For
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Fig. 1. Wood surface area per land area (mean ± SE) for four types of dead wood in 80 productive stands of four age classes and in 20 forested mires in two study landscapes in southern Sweden. A total of 20,324 dead wood objects were recorded.
instance, more than 80% of the landscape-scale population of the two most abundant species, Mycocalicium subtile and Xylographa parallela, occurred in such forests. For several of the rarer species, older (>60 yr) forests were more important (Fig. 2). Only three species had their highest abundance per hectare in unmanaged mires (Fig. 2), but two of these mires harboured a large proportion of their landscape-level populations. 3.2. The relative importance of dead wood types Stumps were the most important substrate; about a half of the species had >50% of their landscape-scale populations on stumps (Fig. 4). Many of the species on stumps also occurred on logs. Only five species were found on dead branches, and they did not constitute the main substratum. Snags were a comparatively rare type of dead wood (Fig. 1), but still five species had >50% of their landscape-scale population on snags (Fig. 4). 4. Discussion 4.1. The relative importance of stand types Half of the wood-dependent lichen species had >50% of their landscape-level populations in managed forests 60 yr old (Fig. 2).
One factor contributing to the larger proportions of populations found in younger managed forests was the latters large extent in the forest landscapes (71% and 62%, northern and southern studied landscape, respectively). Furthermore, many species had higher abundance per hectare in younger stands, which can be explained by the large amounts of dead wood found there. This is illustrated by the results for the three most common species. The relative abundance of these species in different stand types closely mirrors the relative amount of dead wood (Fig. 3). Thus, the main part of their populations is in managed forests 60 yr old because such forest stands contain the bulk of available dead wood in the landscape. Recent studies have documented high species richness on clear-cuts in different organism groups (e.g. Kaila et al., 1997; Rubene et al., 2015). However, managed forest stands between 20 and 60 yr old have been considered as having low conservation value for dead wood-inhabiting species, and have therefore often been neglected (e.g., McGeoch et al., 2007). Our study reveals that among managed forests, those less than 60 years old are important as habitat for wood-dependent lichens. Therefore, these forests should to a higher extent be considered in conservation research. However, even if younger forests constitute an important habitat for many species, red-listed forest species are typically those associated with older forests, since such forests have become rarer due to forestry (Berg et al., 1994). Of the 25 wood-dependent
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Fig. 2. The proportional distribution of the total abundance among different forest types (left panel) and the abundance per hectare (right panel) for all lichen species based on point estimates from both landscapes taken together. The number of occurrences for each species in the northern (N) and southern (S) landscapes are presented between the panels. Note the logarithmic x-axis of the right panel.
lichens on the Swedish Red List, many are associated with weathered wood in the agricultural landscape or driftwood, but several indeed occur in late-successional natural forests (Swedish Species Information Centre, 2015). The species found in our study e Hertelidea botryosa e was quite evenly dispersed among stand types, indicating that this species is not strictly associated with older forests, nor particularly dispersal limited. Several of the rarer species were more abundant in older stands, which may reflect an association with certain forest conditions or characteristics of the dead wood that are rarely present in younger forests. However, there were large uncertainties in the abundance estimates (Fig. 4) and these uncertainties increase with decreasing number of recorded occurrences. Consequently, rare species could appear absent in some stand types due to mere chance. Therefore, we have only weak indications for the presence of lichens that depend on older forest in our study landscapes. One reason for the low number of old forest lichens could be that old stages, with presence of dead wood types that these species need, are never given the time to develop because stands are cut at a relatively early age (Stokland et al., 2012). The major dead wood input in our study landscapes occurs at clear-felling, and not due to mortality in older stands. This differs from forest landscapes with a shorter history of industrial forestry, where old forest have never been clear-felled, or with longer rotations, where the tree mortality increases before the forests are cut (e.g., Ekbom et al., 2006). Predicted warmer climate may result in shortening of rotation periods, both because of €ki et al., 1997) and as a way increased forest growth rates (Kelloma
to meet the increased risk for damages in older forests (Vulturius and Swartling, 2013). Therefore, forest landscapes where clearfelling is the major driver of the occurrence patterns of dead wood will likely be more common in the future. This will have negative consequences for many species, which may be compensated for by leaving more forests unmanaged or by prolonging rotation at some sites (Lassauce et al., 2013). The unmanaged mires in our landscape harboured relatively small proportions of the populations of wood-dependent lichens. This is because most species found on mires also occurred in managed forest stands, where higher amounts of dead wood contributed to their high abundance. The low amount of dead wood in forested mires is consistent with theoretical expectations for low-productive forest (Ranius et al., 2004). A long history of extensive management may also have depleted dead wood amounts in mires (Rydin and Jeglum, 2013). However, for some species these mires are important: two species (Lecanora anopta and Pycnora sorophora) mainly occurred at forested mires. The importance of forested mires for other organism groups dependent on dead wood has not been studied, but the low amount of dead wood present there suggests that forested mires are of limited value for them as well. 4.2. The relative importance of dead wood types For wood-dependent lichens, stumps were the most important dead wood type. 85% of the species used stumps as a substratum,
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Fig. 3. The proportion of the total abundance of three wood-dependent lichens in different stand types and on different main types of dead wood based on predictions of occurrence and abundance on all dead wood objects in a 3 km2 area in two study landscapes in Sweden. Mean (short vertical line) and 95% confidence limits (horizontal line) are shown.
and for about a half of the species stumps were also the major substratum. Although stumps in young managed forests have previously been shown to be comparatively rich in lichen species (Caruso et al., 2008; Svensson et al., 2013), this is the first time that the relative landscape-scale importance of stumps has been assessed. Since wood-dependent species have evolved on naturally occurring dead wood types, the large proportion of the lichen populations found on artificially created stumps may be viewed as surprising. However, most species occurring on stumps were also observed on logs or snags, indicating that these dead wood types are the most important substrate for these species in natural forest landscapes, while in managed forests, stumps are more abundant and consequently more important. We found that branches were only used by 30% of the species and only by the most abundant ones, for which they constitute a small part of their substrate. Earlier studies (Caruso et al., 2008; Dittrich et al., 2014; Svensson et al., 2014) have also found that the relative importance of fine woody debris, including branches, is generally low for lichens. These occurrence patterns have implications for the expected effects of harvesting of wood residues for bioenergy production. Extracting stumps on clear-cuts for bioenergy production purposes will reduce the available habitat for many lichens. If implemented at high intensity, landscape-level lichen populations may decrease considerably, and species with low colonization ability may be at risk of going locally extinct (Johansson et al., 2015). In contrast, extraction of slash, which is already conducted at relatively high intensity, has smaller effects on the populations of wood-
dependent lichens. Snags were the most important substratum for five species (Fig. 4), which is a quite high number, given the low amount of snags in the landscape. However, snags represent a different set of microclimatic conditions compared to ground-level wood such as stumps and logs and are known to be preferred by several lichen ~ hmus and Lo ~hmus, 2001; Svensson et al., 2005). In species (e.g., Lo managed forests, snags are typically rather rare, due to thinnings, short rotation periods, and removal of dead trees for pest management (e.g., Fridman and Walheim, 2000; Sweeney et al., 2010). For wood-dependent lichens, an important conservation measure could thus be the implementation of management practices that increase the number of snags, such as altered thinning procedures €nkko € nen et al., 2014), green tree retention (Runnel et al., 2013), (Mo the setting aside of forest stands, or, as to some extent already practiced in our study landscapes, artificial creation of snags (Jonsson et al., 2006). However, since it takes time from the creation of snags until they become suitable for lichens, so far little has been done to test how such practices affect lichens. 5. Conclusions In managed boreal forest landscapes, stands of young or intermediate age (<60 yr) both have a large total extent and contain a large proportion of the dead wood, which results in the main part of the populations of most wood-dependent lichens occurring there as well. Older managed stands and unmanaged mires harbour
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Fig. 4. The proportional distribution of the total abundance among the dead wood types: branches (green), stumps (blue), logs (yellow), and snags (red) in the two study landscapes combined.
smaller proportions of the populations. Older forest may possess conditions and dead wood types that are rare in younger forests but required by certain lichen species; however we only obtained some support for that in our landscapes. Such requirements do not seem to be met by unmanaged, forested mires, most likely because they contain low amounts of dead wood. Consequently, productive forest habitats should be retained to obtain late-successional forest habitats for wood-dependent lichens. This can be achieved by setting aside larger areas or by retention within the production
stands. Within the production forest stands, we suggest retaining coarse dead wood, and especially snags, rather than thin branches. Since snags are rare in managed forests, artificial creation and other measures to obtain more snags should benefit lichens. Acknowledgements
no.
This study was supported by the Swedish Energy Agency, grant 30651-1 (to GT), the Swedish Research Council for
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Environment, Agricultural Sciences and Spatial Planning (Formas), grant no. 2015-904 (to TR), and the research program “Tree-stump harvesting and its environmental consequences”, financed by the Swedish Energy Agency, the NL Faculty at the Swedish University of Agricultural Sciences and a consortium of forest companies (to TR). n and Mattias Lif for assistance in the field We thank Mathias Live €rgen Rudolphi for comments on an earlier and laboratory, and Jo draft of the manuscript. Holmen Skog AB and Bergvik Skog AB are thanked for granting us access to their forest databases. Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.funeco.2015.12.010. References €m, B., Gustafsson, L., Hallingba €ck, T., Jonsell, M., Weslien, J., 1994. Berg, Å., Ehnstro Threatened plant, animal, and fungus species in Swedish forests: distribution and habitat associations. Conserv. Biol. 8, 718e731. Berglund, H., Hottola, J., Penttil€ a, R., Siitonen, J., 2011. Linking substrate and habitat requirements of wood-inhabiting fungi to their regional extinction vulnerability. Ecography 34, 864e875. Bogomazova, K., 2012. Ecology of Cladonia botrytes in Sweden. Degree project. Dept. of Ecology, SLU. http://stud.epsilon.slu.se. Brassard, B.W., Chen, H.Y.H., 2006. Stand structural dynamics of North American boreal forests. Crit. Rev. Plant Sci. 25, 115e137. Caruso, A., Rudolphi, J., Thor, G., 2008. Lichen species diversity and substrate amounts in young planted Picea abies forests: a comparison between slash and stumps of Picea abies. Biol. Conserv. 141, 47e55. € m, B., Ga €rdenfors, U., Hallingb€ € g, T., Tjernberg, M., Cederberg, B., Ehnstro ack, T., Ingelo €dba €rande impedimentens betydelse fo € r ro €dlistade arter. ArtData1997. De tra banken Rapp. 1, 1e51. Cyr, D., Gauthier, S., Bergeron, Y., Carcaillet, C., 2009. 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Fungal Ecology journal homepage: www.elsevier.com/locate/funeco
The relative importance of stand and dead wood types for wooddependent lichens in managed boreal forests € ran Thor a, Måns Svensson a, *, Victor Johansson a, Anders Dahlberg b, Andreas Frisch a, Go Thomas Ranius a a b
Department of Ecology, Swedish University of Agricultural Sciences, P.O. Box 7044, SE-750 07 Uppsala, Sweden Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences, P.O. Box 7026, SE-750 07 Uppsala, Sweden
a r t i c l e i n f o
a b s t r a c t
Article history: Received 2 July 2015 Received in revised form 13 December 2015 Accepted 31 December 2015 Available online xxx
For efficient conservation, we need to consider both what kinds of habitat species require and the landscape-level supply of these habitats. We examined the relative importance of stand and dead wood types for wood-dependent lichens in two managed boreal forest landscapes in Sweden. We found 20 species and modelled their abundance based on stand type and dead wood characteristics using hierarchical Bayesian models or point estimates. Stands <60 years both have a large total extent and a large proportion of dead wood, resulting in the main part of the populations of most wood-dependent lichens occurring there. Older managed stands and unmanaged mires harbour smaller proportions of the populations. Stumps and snags, and to some extent logs, had high abundances of many species of wooddependent lichens in managed forest landscapes, while dead branches were used by few species. Measures taken to produce more snags should benefit wood-dependent lichens in managed landscapes. © 2016 Elsevier Ltd and The British Mycological Society. All rights reserved.
Corresponding editor: Darwyn Coxson Keywords: Biodiversity Coarse woody debris Fine woody debris Forested mires Lignicolous Saproxylic
1. Introduction Forests managed for timber production differ in several respects from forests with natural dynamics: the average tree age is lower, the tree species composition is more homogeneous, and there are € fewer dead and dying trees (Ostlund et al., 1997; Brassard and Chen, 2006; Cyr et al., 2009; Paillet et al., 2010). Therefore, species dependent on old and dead trees are suffering from habitat loss in managed forest landscapes. In forests harvested by clear-felling, there is also a large variation in habitat quality among stands. This is because clear-felling forestry leads to a landscape composed of even-aged stands at various successional stages, which vary widely in the amount and quality of habitat they provide for forest species € fman and Kouki, 2001; Paillet et al., 2010; Turner et al., 2011). (e.g. Lo Numerous forest species are dependent on dead wood (in Fennoscandia: 25e30%; Siitonen, 2001). Forest management for timber and pulp production means that trees are removed that otherwise would have turned into dead wood. Therefore, the amount of large-
* Corresponding author. E-mail address: [email protected] (M. Svensson). http://dx.doi.org/10.1016/j.funeco.2015.12.010 1754-5048/© 2016 Elsevier Ltd and The British Mycological Society. All rights reserved.
diameter dead wood in managed forests is typically only a small fraction of that in old-growth forests (Siitonen, 2001; Brassard and Chen, 2006). As a consequence, the distribution area and the populations of many wood-inhabiting species are decreasing, and many of them are nationally red-listed (e.g. Tikkanen et al., 2006; Stokland et al., 2012). In Europe, only small patches of unmanaged forest remain, and therefore the amount and quality of dead wood in managed forests play a decisive role for landscape-scale dead wood availability (Stokland et al., 2012). The amount of dead wood can be increased by various conservation measures, such as leaving forests unmanaged, prolonging rotation periods, retaining trees and creating dead wood at clear-felling, or by using alternative management systems, such as selective cutting (Jonsson et al., 2005; Stokland et al., 2012). An opposing trend is the increasing interest in intensified forest production, for example involving harvest of wood residues for bioenergy production (Walmsley and Godbold, 2010; Gan and Smith, 2011) and shortened rotation periods (Jactel et al., 2012). Such practices will likely further decrease the amount of dead wood. Lichens on wood comprise a species rich group in boreal forests. In Fennoscandia, 378 lichen species occur on wood, of which 97 are considered dependent on this substratum (Spribille et al., 2008).
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Among wood-dependent lichens, many species are considered to be typical of old forests (Spribille et al., 2008; Swedish Species Information Centre, 2015), but there are also several species known to occur in young managed forests on stumps or slash originating from clear-felling (Caruso et al., 2008; Svensson et al., 2013). A key factor determining the future distribution and abundance of wood-dependent lichens is forest management, which drives habitat availability for many species. To understand the impact of management, knowing the landscape-scale distribution of species is necessary. However, such data are only available to a limited extent for forest organisms (e.g., polypores: Berglund et al., 2011; saproxylic beetles: Schroeder et al., 2007; Jonsell and Schroeder, 2014) and lacking for lichens. Lichens are often only studied in managed mature or unmanaged stands, while young managed forests are not considered ~ hmus and Lo ~ hmus, 2011). Young forests may, however, possess (Lo € m et al., structures which support a high species richness (Lundstro 2011; Rudolphi and Gustafsson, 2011; Fuller, 2013). Another type of land rarely considered is low-productivity land not used for forestry, such as forests on rocky ground or forested mires. Such low-productivity forest has been considered to support low species richness (e.g. Jasinski and Uliczka, 1998), but no field studies have systematically compared the conservation values of lowproductivity forests and more productive forests. When species experts evaluated the potential conservation value of lowproductivity forests in Sweden, they concluded that these forests may be important especially for some insect and lichen species that are favoured by sun exposure and slow-growing trees (Cederberg et al., 1997). Since the area of low-productivity land is often large (in Sweden, 18% of all forest land is low-productive, i.e. with a potential forest growth <1 m3 ha1; Swedish Forest Agency, 2013) such forests may contribute substantially to landscape-scale habitat availability for forest species. The aim of this study is to provide a quantification of wooddependent lichen populations and their distribution among stand types and dead wood types in two boreal forest landscapes. We assessed the landscape-level population size of individual lichen species using models of their abundance on different dead wood types (stumps, logs, snags and branches) in five different stand types in two forest landscapes in southern Sweden. We calculated the proportion of the landscape-scale population that occurs (i) in different stand types, and (ii) on different types of dead wood. Despite their comparatively low total area, we expected the total abundance of several species to be higher in older managed forests, due to a higher abundance per area caused by larger amounts of logs and snags originating from natural tree mortality in these stands. Further, we expected unmanaged, forested mires to serve as a refuge for wood-dependent lichens which may be rare in the managed part of the landscape. Finally, among dead wood types, we expected stumps and branches on the ground to be important for many species, since they constitute major types of dead wood in managed forests. 2. Material and methods 2.1. Study landscapes Two landscapes in southern Sweden were selected for the study, each covering ca. 150 km2. One is located in the provinces of €stmanland (hereafter referred to as the Northern Dalarna and Va € rs, 1999), landscape) in the middle-boreal vegetation zone (Sjo 60 050 N, 14 050 E, elevation 300e400 m.a.s.l.; the other is in € €tland (the Southern landscape) in the boreonemoral zone, Osterg o 58 480 N, 15 410 E, 60e70 m.a.s.l. Both landscapes are dominated by forests managed by clear-felling, with legally protected,
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unmanaged forests making up <0.3% of the area. The forested land is mainly composed of monocultures or mixed stands of Picea abies and Pinus sylvestris, with some deciduous trees intermixed, mainly Betula pendula, Betula pubescens, and Populus tremula. The forests are typically cut after 80e100 yr. In the study landscapes, >95% are owned by a single forest company (Bergvik Skog AB in the Northern landscape and Holmen Skog AB in the Southern landscape), giving us access to stand databases with almost total landscape coverage. We surveyed stands of five types: four age classes of productive forests and one consisting of forested mires. The productive stands were divided into the age classes 0e20 yr (21.6% and 25.2% of the forested area in the Northern and Southern study landscapes, respectively), 21e60 years (40.0% and 45.4%), 61e110 yr (16.7% and 16.1%) and >110 yr (4.4% and 6.0%). The proportion of different age classes is similar to the Swedish average (Swedish Forest Agency, 2013). The forested mires (17% and 7% in the Northern and Southern study landscape, respectively) support open P. sylvestris stands with an annual productivity <1 m3 ha1 and are exempted by law from forest production (Jasinski and Uliczka, 1998; Swedish Forest Agency, 2013). Ten stands of each type were randomly chosen in each study landscape. Thus, 100 stands were sampled in total. 2.2. Sampling dead wood and lichens In every stand, dead wood and wood-dependent lichens were surveyed along two randomly placed transects (Marshall et al., 2000). This method has been used earlier in landscape-scale studies on wood-dependent organisms (e.g., Ekbom et al., 2006; Schroeder et al., 2007). Each transect was 100 m long and 10 m wide. One of the transects in each stand was oriented along a NeS axis and the other along an EeW axis. If a transect reached the stand edge prior to completion, its mid-point was shifted sideways by 20 m, to the north for an EeW transect and to the east for a NeS transect. The transect was then continued in the opposite direction. In the area covered by each transect, all dead wood objects fulfilling the criteria described below were recorded and their wood surface areas were estimated using a measuring tape or plastic grid. The types of wood recorded included logs (all), stumps (up to 100 cm height, all), snags (from 101 cm height, all), and dead branches on the ground (only coniferous, because deciduous branches decompose rapidly and were scarce). Dead branches on living trees were not included, since they have been found to be of little importance for wood-dependent lichens (Svensson et al., 2014). Dead wood objects were included if they had a wood surface area (i.e. area with no bark) of at least 25 cm2 and were at least 0.8 cm thick and 10 cm long. If a dead wood object extended beyond the area delimited by the transect, only the part found within the transect was included in the inventory. Lichens were surveyed in two plots that were 15 10 m each, randomly placed along each transect. In these plots, all dead wood objects were searched for the 96 lichen species classified as wooddependent (“obligate lignicoles”) in Fennoscandia by Spribille et al. (2008), excluding Cladonia botrytes as this species has been shown to be only facultatively lignicolous (Bogomazova, 2012). The abundance of wood-dependent lichens was estimated as the number of occurrences in 5 5 cm squares of a plastic grid, yielding a value equivalent to the proportion of occupied grid squares. Some types of dead wood were too rare to yield a sufficiently large sample size within the plots, and were instead surveyed for lichens along the whole transect. These included all snags, all deciduous wood, and all logs (with the exception of stands 0e20 yr, where logs are common). Lichen species were mainly determined in the field, but samples were collected when necessary and identified later using light microscopy and thin layer chromatography. The nomenclature follows Nordin et al. (2015). Field work was carried out during 2010e2012.
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2.3. Assessing species abundance
2.4. Landscape-scale dead wood simulations
We assessed species abundance in different stand types using two different approaches. Both approaches included the same three steps: (1) calculating estimates of species abundance for different dead wood types and stand types, (2) using stand databases and our dead wood inventory data to calculate landscape-scale dead wood amounts and (3) combining (1) and (2) to get landscape-scale quantifications of species' populations and their distribution among stand types and dead wood types. In this section, we describe step (1). For (2), see Landscape-scale dead wood simulations and for (3), see Combining abundance estimates and dead wood simulations. In the first approach for assessing species abundance, we made point estimates of abundance on different dead wood types in different stand types for all species. This was done by using mean abundances for each species on different dead wood types in each stand type. In the second approach, we modelled species abundance based on the characteristics of dead wood objects and forest stands using hierarchical Bayesian models (Gelman et al., 2004). This approach was in principle preferable as it allowed us to include uncertainty measures for the lichen abundance estimations, but it is more data demanding. Hence, we were only able to use this method for species occurring on >3% of the dead wood objects: Micarea misella, Mycocalicium subtile and Xylographa parallela. The genus Xylographa has been revised (Spribille et al., 2014) after the completion of our field work, which means that our recordings of X. parallela may also include X. pallens. We excluded Micarea denigrata, since a substantial part of the population of this species may occur on dead branches of living trees (Svensson et al., 2014), a dead wood type not included here. We used generalized linear zero-inflated Poisson models (ZIP), which are appropriate for count data (here number of squares in the plastic-grid) with an excessive number of zeroes compared to that assumed by a regular Poisson distribution. The ZIP model includes a binomial sub-model for occurrence probability and a count sub-model for abundance (Zuur et al., 2012). We used a Bernoulli distribution and a logit link function for the occurrence sub-model and a Poisson distribution and a log link function for the abundance sub-model. To account for additional overdispersion not caused by excess zeroes in the abundance part of the model, we included an observation level random error term. This term acts as a latent variable that will pick up any variation that cannot be explained by the explanatory variables or the random intercepts and would otherwise result in overdispersion (Zuur et al., 2012). The hierarchical Bayesian framework enables the utilization of explanatory variables measured at the stand level (i.e. at the higher hierarchical level), as we use them to model the standspecific intercepts (Gelman and Hill, 2007). Hence, the two types of response variable (occurrence and abundance) are explained both by dead wood object characteristics (lower level) and stand characteristics (higher level). Moreover, the model accounts for the unexplained variation between stands by including stand identity as a random error. We constructed the models by comparing versions with different combinations of the explanatory variables using the Deviance Information Criterion (DIC; Spiegelhalter et al., 2002). The models were fitted using OpenBUGS 3.2.2 (Thomas et al., 2006) using Markov Chain Monte Carlo (MCMC). We ran two MCMC chains for 110,000 iterations with a burn-in of 10,000 iterations. We thinned the chains by storing every 20th iteration, resulting in 10,000 stored values per parameter. We used uninformative prior distributions: Normal (0, 0.001) for all parameters associated with dead wood and stand characteristics, and Gamma (0.001, 0.001) for the precision parameters of the random intercepts.
For both approaches and for each study landscape, we simulated all dead wood objects within an area of 3 km2. Within the simulated areas, the proportion covered by each stand type was based on actual values obtained from databases of the landowners. Each simulated stand was allocated a size based on the mean sizes of stands for each study landscape and stand type. These stands were then assigned a number of dead wood objects of each type based on random draws from negative binomial distributions that had been fitted to the observed number of dead wood objects in each stand type (5 stand types and 10 dead wood types/stand type ¼ 50 distributions per study landscape). The size of each dead wood object was based on random draws from normal distributions fitted to the observed wood surface area (log transformed) of each dead wood type in each stand type. The predictions of dead wood objects were replicated in the same way as lichen abundance (i.e. 500 replicates), using one combination of the parameters for each replicate, from which we obtained the number of dead wood objects of each type and their sizes. Hence, for the three modelled species, the predictions of lichen abundance in the whole landscape include the uncertainty in the dead wood predictions. As the point estimates of abundance do not include any uncertainty measure, we used the median of the dead wood distributions for these estimates. 2.5. Combining abundance estimates and dead wood simulations For the first approach of estimating species abundance (see Assessing species abundance), we used the mean abundances on different dead wood types and the amount of these dead wood types in different stand types in a whole landscape (see Landscapescale dead wood simulations). We assessed for each species: abundance/ha in each forest type, the relative importance of different forest types (i.e. the proportional distribution of the total population among different forest types in the whole landscape), and the relative importance of different types of dead wood. For the second approach, we (1) estimated lichen abundance for each simulated dead wood object using the parameter estimates from our fitted models (Fig. S1), and (2) calculated the proportion of the total abundance on each dead wood type and in each stand type. Each estimation process (i.e. for one species in one landscape) was replicated 500 times. For each replicate, we randomly selected one combination of the parameters of the occurrence and abundance models from their joint posterior distributions. 3. Results We recorded 20,324 dead wood objects, of which 5719 were searched for wood-dependent lichens. Stands aged 0e20 yr contained the highest amounts of dead wood surface area per hectare, while forested mires had the lowest (Fig. 1). Snags were the least common substratum type in terms of surface area, while logs were the most common (Fig. 1). We recorded 20 wood-dependent lichens of which 16 occurred in the Southern study area and 18 in the Northern, and 14 species occurring in both study areas. One redlisted species (Hertelidea botryosa) was found. 3.1. The relative importance of stand types The majority of the species (17 out of 20) occurred with a higher abundance per hectare in managed forests and eight of them were only recorded there (Fig. 2). For half of the species, >50% of the landscape-scale populations occurred in managed forests 60 yr old (Figs. 2 and 3). Younger forests (60 yr) tended to be more important for the more abundant species (Figs. 2 and 3). For
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Fig. 1. Wood surface area per land area (mean ± SE) for four types of dead wood in 80 productive stands of four age classes and in 20 forested mires in two study landscapes in southern Sweden. A total of 20,324 dead wood objects were recorded.
instance, more than 80% of the landscape-scale population of the two most abundant species, Mycocalicium subtile and Xylographa parallela, occurred in such forests. For several of the rarer species, older (>60 yr) forests were more important (Fig. 2). Only three species had their highest abundance per hectare in unmanaged mires (Fig. 2), but two of these mires harboured a large proportion of their landscape-level populations. 3.2. The relative importance of dead wood types Stumps were the most important substrate; about a half of the species had >50% of their landscape-scale populations on stumps (Fig. 4). Many of the species on stumps also occurred on logs. Only five species were found on dead branches, and they did not constitute the main substratum. Snags were a comparatively rare type of dead wood (Fig. 1), but still five species had >50% of their landscape-scale population on snags (Fig. 4). 4. Discussion 4.1. The relative importance of stand types Half of the wood-dependent lichen species had >50% of their landscape-level populations in managed forests 60 yr old (Fig. 2).
One factor contributing to the larger proportions of populations found in younger managed forests was the latters large extent in the forest landscapes (71% and 62%, northern and southern studied landscape, respectively). Furthermore, many species had higher abundance per hectare in younger stands, which can be explained by the large amounts of dead wood found there. This is illustrated by the results for the three most common species. The relative abundance of these species in different stand types closely mirrors the relative amount of dead wood (Fig. 3). Thus, the main part of their populations is in managed forests 60 yr old because such forest stands contain the bulk of available dead wood in the landscape. Recent studies have documented high species richness on clear-cuts in different organism groups (e.g. Kaila et al., 1997; Rubene et al., 2015). However, managed forest stands between 20 and 60 yr old have been considered as having low conservation value for dead wood-inhabiting species, and have therefore often been neglected (e.g., McGeoch et al., 2007). Our study reveals that among managed forests, those less than 60 years old are important as habitat for wood-dependent lichens. Therefore, these forests should to a higher extent be considered in conservation research. However, even if younger forests constitute an important habitat for many species, red-listed forest species are typically those associated with older forests, since such forests have become rarer due to forestry (Berg et al., 1994). Of the 25 wood-dependent
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Fig. 2. The proportional distribution of the total abundance among different forest types (left panel) and the abundance per hectare (right panel) for all lichen species based on point estimates from both landscapes taken together. The number of occurrences for each species in the northern (N) and southern (S) landscapes are presented between the panels. Note the logarithmic x-axis of the right panel.
lichens on the Swedish Red List, many are associated with weathered wood in the agricultural landscape or driftwood, but several indeed occur in late-successional natural forests (Swedish Species Information Centre, 2015). The species found in our study e Hertelidea botryosa e was quite evenly dispersed among stand types, indicating that this species is not strictly associated with older forests, nor particularly dispersal limited. Several of the rarer species were more abundant in older stands, which may reflect an association with certain forest conditions or characteristics of the dead wood that are rarely present in younger forests. However, there were large uncertainties in the abundance estimates (Fig. 4) and these uncertainties increase with decreasing number of recorded occurrences. Consequently, rare species could appear absent in some stand types due to mere chance. Therefore, we have only weak indications for the presence of lichens that depend on older forest in our study landscapes. One reason for the low number of old forest lichens could be that old stages, with presence of dead wood types that these species need, are never given the time to develop because stands are cut at a relatively early age (Stokland et al., 2012). The major dead wood input in our study landscapes occurs at clear-felling, and not due to mortality in older stands. This differs from forest landscapes with a shorter history of industrial forestry, where old forest have never been clear-felled, or with longer rotations, where the tree mortality increases before the forests are cut (e.g., Ekbom et al., 2006). Predicted warmer climate may result in shortening of rotation periods, both because of €ki et al., 1997) and as a way increased forest growth rates (Kelloma
to meet the increased risk for damages in older forests (Vulturius and Swartling, 2013). Therefore, forest landscapes where clearfelling is the major driver of the occurrence patterns of dead wood will likely be more common in the future. This will have negative consequences for many species, which may be compensated for by leaving more forests unmanaged or by prolonging rotation at some sites (Lassauce et al., 2013). The unmanaged mires in our landscape harboured relatively small proportions of the populations of wood-dependent lichens. This is because most species found on mires also occurred in managed forest stands, where higher amounts of dead wood contributed to their high abundance. The low amount of dead wood in forested mires is consistent with theoretical expectations for low-productive forest (Ranius et al., 2004). A long history of extensive management may also have depleted dead wood amounts in mires (Rydin and Jeglum, 2013). However, for some species these mires are important: two species (Lecanora anopta and Pycnora sorophora) mainly occurred at forested mires. The importance of forested mires for other organism groups dependent on dead wood has not been studied, but the low amount of dead wood present there suggests that forested mires are of limited value for them as well. 4.2. The relative importance of dead wood types For wood-dependent lichens, stumps were the most important dead wood type. 85% of the species used stumps as a substratum,
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Fig. 3. The proportion of the total abundance of three wood-dependent lichens in different stand types and on different main types of dead wood based on predictions of occurrence and abundance on all dead wood objects in a 3 km2 area in two study landscapes in Sweden. Mean (short vertical line) and 95% confidence limits (horizontal line) are shown.
and for about a half of the species stumps were also the major substratum. Although stumps in young managed forests have previously been shown to be comparatively rich in lichen species (Caruso et al., 2008; Svensson et al., 2013), this is the first time that the relative landscape-scale importance of stumps has been assessed. Since wood-dependent species have evolved on naturally occurring dead wood types, the large proportion of the lichen populations found on artificially created stumps may be viewed as surprising. However, most species occurring on stumps were also observed on logs or snags, indicating that these dead wood types are the most important substrate for these species in natural forest landscapes, while in managed forests, stumps are more abundant and consequently more important. We found that branches were only used by 30% of the species and only by the most abundant ones, for which they constitute a small part of their substrate. Earlier studies (Caruso et al., 2008; Dittrich et al., 2014; Svensson et al., 2014) have also found that the relative importance of fine woody debris, including branches, is generally low for lichens. These occurrence patterns have implications for the expected effects of harvesting of wood residues for bioenergy production. Extracting stumps on clear-cuts for bioenergy production purposes will reduce the available habitat for many lichens. If implemented at high intensity, landscape-level lichen populations may decrease considerably, and species with low colonization ability may be at risk of going locally extinct (Johansson et al., 2015). In contrast, extraction of slash, which is already conducted at relatively high intensity, has smaller effects on the populations of wood-
dependent lichens. Snags were the most important substratum for five species (Fig. 4), which is a quite high number, given the low amount of snags in the landscape. However, snags represent a different set of microclimatic conditions compared to ground-level wood such as stumps and logs and are known to be preferred by several lichen ~ hmus and Lo ~hmus, 2001; Svensson et al., 2005). In species (e.g., Lo managed forests, snags are typically rather rare, due to thinnings, short rotation periods, and removal of dead trees for pest management (e.g., Fridman and Walheim, 2000; Sweeney et al., 2010). For wood-dependent lichens, an important conservation measure could thus be the implementation of management practices that increase the number of snags, such as altered thinning procedures €nkko € nen et al., 2014), green tree retention (Runnel et al., 2013), (Mo the setting aside of forest stands, or, as to some extent already practiced in our study landscapes, artificial creation of snags (Jonsson et al., 2006). However, since it takes time from the creation of snags until they become suitable for lichens, so far little has been done to test how such practices affect lichens. 5. Conclusions In managed boreal forest landscapes, stands of young or intermediate age (<60 yr) both have a large total extent and contain a large proportion of the dead wood, which results in the main part of the populations of most wood-dependent lichens occurring there as well. Older managed stands and unmanaged mires harbour
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Fig. 4. The proportional distribution of the total abundance among the dead wood types: branches (green), stumps (blue), logs (yellow), and snags (red) in the two study landscapes combined.
smaller proportions of the populations. Older forest may possess conditions and dead wood types that are rare in younger forests but required by certain lichen species; however we only obtained some support for that in our landscapes. Such requirements do not seem to be met by unmanaged, forested mires, most likely because they contain low amounts of dead wood. Consequently, productive forest habitats should be retained to obtain late-successional forest habitats for wood-dependent lichens. This can be achieved by setting aside larger areas or by retention within the production
stands. Within the production forest stands, we suggest retaining coarse dead wood, and especially snags, rather than thin branches. Since snags are rare in managed forests, artificial creation and other measures to obtain more snags should benefit lichens. Acknowledgements
no.
This study was supported by the Swedish Energy Agency, grant 30651-1 (to GT), the Swedish Research Council for
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Environment, Agricultural Sciences and Spatial Planning (Formas), grant no. 2015-904 (to TR), and the research program “Tree-stump harvesting and its environmental consequences”, financed by the Swedish Energy Agency, the NL Faculty at the Swedish University of Agricultural Sciences and a consortium of forest companies (to TR). n and Mattias Lif for assistance in the field We thank Mathias Live €rgen Rudolphi for comments on an earlier and laboratory, and Jo draft of the manuscript. Holmen Skog AB and Bergvik Skog AB are thanked for granting us access to their forest databases. Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.funeco.2015.12.010. References €m, B., Gustafsson, L., Hallingba €ck, T., Jonsell, M., Weslien, J., 1994. Berg, Å., Ehnstro Threatened plant, animal, and fungus species in Swedish forests: distribution and habitat associations. Conserv. Biol. 8, 718e731. 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