Abstract
Intensive forest management has led to a population decline in many species, including those dependent on dead wood. Many lichens are known to depend on dead wood, but their habitat requirements have been little studied. In this study we investigated the habitat requirements of wood dependent lichens on coarse dead wood (diameter >10 cm) of Scots pine Pinus sylvestris in managed boreal forests in central Sweden. Twenty-one wood dependent lichen species were recorded, of which eleven were confined to old (estimated to be >120 years old) and hard dead wood. Almost all of this wood has emanated from kelo trees, i.e. decorticated and resin-impregnated standing pine trees that died long time ago. We found four red-listed species, of which two were exclusive and two highly associated with old and hard wood. Lichen species composition differed significantly among dead wood types (low stumps, snags, logs), wood hardness, wood age and occurrence of fire scars. Snags had higher number of species per dead wood area than logs and low stumps, and old snags had higher number of species per dead wood area than young ones. Since wood from kelo trees harbours a specialized lichen flora, conservation of wood dependent lichens requires management strategies ensuring the future presence of this wood type. Besides preserving available kelo wood, the formation of this substratum should be supported by setting aside P. sylvestris forests and subject these to prescribed burnings as well as to allow wild fires in some of these forests.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
The boreal forest has an extension of 14.3 million km2 (Kasischke et al. 1995) and is one of the largest biomes on the planet. Forestry has profoundly modified forest habitats in this biome, especially in Northern Europe and Eastern Northern America (Esseen et al. 1997; Cyr et al. 2009). Intensive forest management has led to a decrease of structural diversity (Östlund et al. 1997), including a decrease in the amount of dead wood (Green and Peterken 1997). For instance, the volume of standing dead wood has been estimated to decrease with 90% in a region in Sweden during the past century (Linder and Östlund 1998). In old-growth boreal forests, dead wood is mainly created by self-thinning, pathogens and disturbances such as storms, fire, and insect outbreaks (Esseen et al. 1997; Niklasson and Granström 2000; Stokland et al. 2012). On the contrary, in managed forests trees are harvested before natural processes creating larger quantities of dead wood take effect. Furthermore, in today’s managed forest landscapes in Fennoscandia, fire is usually suppressed and sanitation measures (such as salvage logging) after large disturbances prevent the accumulation of dead wood. As a result, the volume of coarse woody debris (CWD, i.e. wood with a diameter >10 cm) in managed boreal forests has been estimated to be only 2–10% of the amount in natural forests (Siitonen 2001). For certain dead wood types the decrease may have been even stronger. In managed forests, CWD of deciduous species, of large dimension and from late decay stages, are particularly rare (Jonsson et al. 2016). A large proportion of forest-dwelling species requires dead wood (Jonsson et al. 2005). The loss of habitat has led to population declines in many of these species (Siitonen 2001). Thus, the formation and maintenance of CWD are crucial factors for successful biodiversity management in forests (Botting and De Long 2009; Lassauce et al. 2011; Seibold et al. 2015). Which dead wood types that individual species are utilizing has been well explored in some regions, especially for macrofungi (Junninen and Komonen 2011) and beetles (Grove 2002), but less for other wood dependent species groups, such as lichens.
Lichens are a species rich group in boreal forests, being found on bark (corticolous lichens), soil (terricolous lichens), rocks (saxicolous lichens), and decorticated dead wood (lignicolous lichens) (Boch et al. 2013). The loss of a tree’s bark results in a major shift in lichen species composition (Lõhmus and Lõhmus 2001). Ecological studies on lichens in forests have mainly focused on species growing on bark, even though dead wood has been recognized as an important substrate (e.g., Spribille et al. 2008). In Fennoscandia, 378 species have been reported from decorticated dead wood, of which 97 are restricted to this substrate (henceforth “wood dependent lichens”; Spribille et al. 2008). Wood dependent lichens may be more affected by a decreased amount of dead wood than generalist species and are therefore of higher conservation concern. Many species of wood dependent lichens occur in high abundances on stumps, snags, and to some extent logs, while dead branches are colonized by only a few species (Svensson et al. 2016). In several cases, snags have been found to be more species rich than logs (Kuusinen and Siitonen 1998; Humphrey et al. 2002; Runnel et al. 2013), but both these habitats host unique species (Hämäläinen et al. 2014). The age and decay stage of dead wood generally affect lichen species richness and composition (Nascimbene et al. 2008; Botting and De Long 2009; Caruso and Rudolphi 2009; Svensson et al. 2013). In boreal forests, fire has been found to decrease species richness of lichens (Hämäläinen et al. 2014). However, a few lichens, such as Carbonicola anthracophila, C. myrmecina (Bendiksby and Timdal 2013) and Hertelidea botryosa (Esseen et al. 1997; Lõhmus and Kruustük 2010) are fire-dependent and occur predominately on dead pine snags or stumps with charred wood (Grossmann 2014; Källén 2015).
In the European boreal region, Scots pine Pinus sylvestris is one of the dominant tree species. Under certain conditions, which probably include repeated wild fires, dead wood of P. sylvestris become hard and resin-impregnated and is then very long lasting. In Finland, such old, hard, resin-impregnated, silver-grey and decorticated trunks of P. sylvestris are called kelo trees (Niemelä et al. 2002). Several fungal species, mainly basidiomycetes (such as polypores and corticiaceous fungi) are confined to kelo substrates (Niemelä et al. 2002). Formation and decay of kelo trees are very slow processes. P. sylvestris can become up to 800 years old, and its transformation into kelo trees takes about 40 years after tree death (Sirén 1961; Leikola 1969). Kelo trees can remain standing for over 700 years (Niemelä et al. 2002), and final decay of the fallen stem may take another 200 years (Tarasov and Birdsey 2001). When a kelo tree breaks, the stump and log is quite resistant to further decay as the heartwood is resin-impregnated. As a result, the heartwood remains intact and the surface hard. Formation of kelo trees is not likely to occur in commercially managed forests with fast growing trees and short rotation cycles. Scientific studies on wood dependent lichens on kelo wood are currently lacking.
The aim of this study was to investigate the habitat requirements of wood dependent lichens on P. sylvestris wood. We analyzed to what extent wood type (low stumps, snags, logs), wood hardness, wood age, and occurrence of fire scars affect lichen species density (number of species per dead wood area) and composition. We hypothesized that species density and composition would differ between wood types and that especially old and hard wood would host different lichen species than younger and softer dead wood.
Materials and methods
Study area
Effaråsen, the study area, is located in the province of Dalarna in the southern boreal vegetation zone (Ahti and Jalas 1968) of Sweden (approximate central point 60°58′29″N, 14°01′55″E). Its c. 140 ha of forest land is dominated (i.e. >95%) by P. sylvestris (one of the two dominating tree species in Sweden), about 120–140 years of age, including some older trees. Other less abundant tree species in the area are Norway spruce Picea abies and birch (Betula pendula and B. pubescens). The ground vegetation is dominated by dwarf shrubs (Vaccinium vitis-idaea and V. myrtillus) and lichens (among fruticose species mainly Cladonia spp.). The study area is representative for old pine forests in central and northern Sweden which are close to being logged by clearcutting. The forest has never been clear-felled but traces of historical high-grading can be seen. In more recent time the forest is managed for wood production, including operations of thinning and a main part has been fertilized in 1982 and 2000. In the 1888 the area was hit by a severe fire (Hedberg et al. 1998). Remnants from this fire include fire-scarred P. sylvestris trees and large diameter snags, logs and stumps. Even though the studied forest is intensively managed today, it harbours old and hard wood (low stumps, snags, logs) as a legacy of more natural forest conditions.
Effaråsen is now hosting a large research project, in which trees and dead wood, old and newly created, are retained in different amounts (see Santaniello et al. 2016 for further details). The research treatments were applied 12 months before the lichen sampling took place, and we assume only a negligible effect on lichen species during this short time. Therefore, the studied forest stands represent old pine forests that are close to being logged by clearcutting. Fifteen stands, with a total area corresponding to about 70% of the area of the study landscape, were randomly allotted and homogenously distributed in the landscape, with the aim to cover the whole study area. In some occasions the stands are separated to each other by small forest patches not included in the experiment. Mean size of the inventoried stands was 6 ha (range 4–14.2 ha), mean altitude was 384 meters above sea level (range 370–400 m), mean number of stems per ha was 526 (range 290–640), mean tree height was 17 m (range 17–19 m), mean tree diameter at breast height (DBH) was 25 cm (range 20–30 cm), mean volume of coarse woody debris was 1.5 m3 (range 0.95–3.45 m3) (Table 1). The mean site productivity was 3.1 m3 ha−1 year−1 (range 2.4–4.3 m3 ha−1 year−1) (data from a database provided by the forest company Stora Enso Skog AB).
Study design
All sampling was conducted in plots along transects laid out across the longest possible distance in each of the 15 study stands. Ten 100 m2 circular plots (radius 5.64 m) were established along each transect with 15–35 m distance between their mid-points depending on the length of the transect. In some stands there was not enough space for 10 plots along the transect. Then we laid out an additional transect covering the second longest distance for the remaining plots. Due to an error, only nine plots were established in one of the stands.
The amount of dead wood in terms of total area available for lichen colonization on different types of substrates was recorded in July–September 2013 (Santaniello et al. 2016). The coverage of wood dependent lichens and the amount and quality of dead wood was surveyed in September 2014. We surveyed only wood of P. sylvestris, which constitute >95% of the total dead wood available.
Dead wood inventory
In both the inventories carried out in this study, the dead wood characteristics were recorded as follows. All coarse woody debris (diameter >10 cm) within the circular plots was surveyed in order to assess the quality and quantity of dead wood. We divided the dead wood objects into groups according to their characteristics: (1) wood type (low stump, snag and log), (2) wood hardness (five categories), (3) occurrence of fire scars, and (4) wood age (long or short time since tree death). We divided standing dead wood into two height categories, low stumps are ≤50 cm tall (mostly stumps from harvested trees) and snags are >50 cm (stumps from harvested trees and naturally formed snags). Wood hardness was estimated using the method of Siitonen and Saaristo (2000), which is based on the depth a knife can be pushed into the wood. The scale is from 1 to 5, where 1 is very hard wood, 2 is hard wood, 3 is mid-hard wood, 4 is soft wood and 5 is very soft and highly decayed wood. Wood age was assessed by dividing dead wood into two distinct categories: (1) dead wood from trees judged to have died before or during the large forest fire in 1888 (hereafter termed “>120 years old”), with a characteristic furrowed surface and resin-impregnated wood) and (2) wood created from trees that had died more recently, probably mostly during the last 50 years (hereafter termed “<120 years old”). Diameter (at breast height, 130 cm above the ground) and height or length was measured, and the area of dead wood covered by bark and bryophytes was estimated. For the studied lichens, only dead wood without bark and bryophytes are available for colonization. Therefore, the area of dead wood that was available for lichens was calculated by first estimating its total surface area, assuming that every object was cylindrical, and then reducing the area by the estimated proportion of bark and bryophyte cover. The cut surfaces on stumps and logs were included in the calculations. For snags taller than 2 m the cut surface was not included since lichens were not inventoried there. Dead wood created at the experimental cutting in 2012–2013 was excluded, as we assumed that this wood was not colonised by any visible dead wood dependent lichens until the inventory. Old snags fallen after November 2012 were treated as standing as it is unlikely that wood dependent lichens had already reacted to this.
Lichen inventory
All lichen species classified as wood dependent by Spribille et al. (2008) were surveyed by G. Thor including Cladonia botrytes, which later has been shown to be only facultatively lignicolous (Bogomazova 2012). In Effaråsen, C. botrytes was searched for on the ground along all transects, but was only found lignicolous. Only dead wood objects with an overall area of exposed wood ≥25 cm2 were inventoried. For objects partly outside the plot area, only the part inside the plot was inventoried. Standing objects were inventoried up to 2 m above the ground. The area covered by each lichen species was measured in cm2 for each object. For every dead wood object with lichen occurrence, their characteristics were measured as described above. Micarea denigrata and M. nowakii are difficult to separate in the field and noted as M. denigrata/nowakii. The presence of M. denigrata was confirmed in the collected material, but not M. nowakii. The taxonomy of the genus Xylographa follow Spribille et al. (2015). Small specimens of Xylographa parallela and X. pallens can be difficult to separate in the field and, as small specimens were common in our study, these species were treated as X. parallela/pallens. The presence of both species in the area was confirmed in collections. Trapeliopsis sp. might represent an undescribed species. Reference material of lichens will be deposited in herbarium UPS (Museum of Evolution, Uppsala University).
Data analysis
In the statistical analyses, we considered each dead wood category in each stand as a replicate. From the dead wood inventory, we estimated the total surface area of dead wood. Furthermore, we calculated the area covered by each lichen species (Table 2).
Non-metric multidimensional scaling
Species composition was analysed for different dead wood categories (according to wood type, wood hardness, wood age and occurrence of fire scars) with non-metric multidimensional scaling (NMDS), using the Jaccard similarity coefficients (Jaccard distance) (Jaccard 1908; Pielou 1984) in a 2-dimensional space. The NMDS is an ordination method based on ranked Euclidean distances between samples. The data from the circular plots were pooled for each of the 15 forest stands. All ordination analyses were performed using R (version 3.2.1 and the packages Vegan, MASS and BiodiversityR) (R Core Team 2014; Oksanen et al. 2007). We calculated the stress and performed a permutational multivariate analysis of variance using a distance matrix to statistically compare the samples using the function “adonis” (Anderson 2001).
Rarefaction curves
In order to compare the species density on dead wood with different characteristics, we used sample-based rarefaction curves (Gotelli and Colwell 2001). The analysis was based on the following comparisons: (1) wood type, (2) wood hardness, (3) wood age, (4) wood hardness and age, (5) wood type and age. We used one hundred random re-samplings among sample units (i.e. each plot) and 95% confidence intervals (CI) for the statistical evaluations. The rarefaction curves were computed using the software EstimateS, version 9.1.0 (Colwell 2013). In order to compare the number of lichen species on equal amounts of available wood area, the x-axis was rescaled to represent the cumulative surface area. Calculations were made using the total bark and bryophytes free surface area of dead wood per plot.
Results
Among a total number of 523 dead wood objects inventoried, 242 (46%) were colonized by dead wood dependent lichens. The total number of lichen observations was 422. The total area of dead wood inventoried was 306.3 m2 (low stumps: 27.3 m2; snags: 44.4 m2; logs: 234.6 m2). The area covered by wood dependent lichens was c. 8.8 m2 (low stumps: 0.2 m2; snags: 7.1 m2; logs: 1.5 m2). Among the 21 wood dependent lichen species, four were red-listed (Swedish Species Information Centre 2015) (Table 2).
Wood age
The species density was about three times higher for old (>120 years old) dead wood than for young dead wood (Fig. 1a), a significant difference according to the 95% CI. Also species composition was clearly affected by wood age; the adonis test showed a significant difference in species composition between old and young dead wood (Fig. 2a). Thirteen species were only found on old dead wood, including three red-listed species (Table 2).
Wood hardness
Wood from hardness category 2 (the second hardest on a 5-level scale) had higher species density than both harder and softer wood (Fig. 1b). NMDS analyses revealed a significant difference in species composition between the hardness categories (Fig. 2b). This was especially the case for the hardest dead wood (category 1), which was clearly separated from the others. Fourteen species were only or almost only found on wood from hardness 1 and 2, including all four red-listed species (Table 2).
Wood type
Snags had the highest species density (Fig. 3a) of studied wood types. Snags >120 years old had a species density that was more than twice as high as that of the younger snags (Fig. 3b). The NMDS analyses revealed a significant difference in species composition between the three wood types (low stumps, snags, logs) (Fig. 2d).
Occurrence of fire scars
Fourteen species were found on burnt wood of which three were found only here (Table 2). Rarefaction analyses were not possible in this case, due to the low number of observations on burnt wood. The NMDS analyses revealed a significant difference in species composition (Fig. 2c), underlined by the graphical clear division between presence and absence of fire scars.
Old and hard wood
All the 21 species observed in this study occurred on old and hard wood (with age >120, hardness category 1 and 2). Eleven species were exclusive and two highly associated with such wood (Table 2). Of the four red-listed species, two were exclusive to old and hard wood and two almost only occurred here (Table 2). For dead wood >120 years old, there were most species in hardness category 1, followed by hardness category 2 (Fig. 1c).
Discussion
Wood age
The highest number of wood dependent species was found on old dead wood (>120 years). Also previous studies have shown that abundance of lichen species varies with the age of the wood (Humphrey et al. 2002). This may be because old dead wood has certain characteristics, such as less cellulose and lignin content (Stokland et al. 2012) and higher nitrogen content due to fungal mycelia, which are rich in nitrogen (Cowling and Merrill 1966). Higher frequency of occurrences on older substrate may also be because lichens have had a longer time for colonization than on more recently formed substrate (Johansson et al. 2012). Our result highlights the importance of old dead wood for lichen occurrence.
Wood hardness
Species density was highest for hardness wood categories 2 and 3 (Fig. 1b). This can be due to that intermediate decomposition stages often show a wider range of microhabitats than earlier or later decay stages (Caruso and Rudolphi 2009; Kruys and Jonsson 1999; Wagner et al. 2014). Moreover, the progressive decrease of substratum stability over time is probably negative to lichens (Nascimbene et al. 2008).
Wood type
Species density was highest for old snags. This may be due to microclimatic and structural differences between dead wood types. Also previously, snags have been found to host more lichen species than e.g. logs (Humphrey et al. 2002; Lõhmus and Lõhmus 2001; Nascimbene et al. 2008; Svensson et al. 2016). Snags are considerably drier and more exposed to light. This is because logs are to a higher degree shaded by vegetation and covered by snow. Light exposition seems to be a very important variable for lichens (Rudolphi and Gustafsson 2011). For instance, Svensson et al. (2005) have found that the lichen species richness differs between the northern and southern side of snags.
Fire scar presence
The results indicate that many species occur on wood with fire scars (Table 2). Carbonicola anthracophila and C. myrmecina have been found to grow on burned wood even 300 years after fire (Esseen et al. 1997) indicating that species occurring on this substratum can survive for a long time on individual dead wood objects.
Old and hard wood
Our field experience is that almost all old (>120 years old) and hard (hardness category 1 and 2) wood has emanated from kelo trees. Though only rather few remaining standing kelo trees were found, logs, stumps and tops remaining from historical high-grading in the 19th century or earlier are scattered in the area. Our study shows that kelo wood had the highest species density, and a high proportion of wood dependent lichens depend on kelo wood. All the species found during the inventory occurred on such wood, and 11 species were confined to kelo wood. Of the four red-listed species, two were exclusive to kelo wood and two almost only occurred here, indicating the importance of this substrate to red-listed lichens. To fully understand lichens’ habitat requirements, it is important to also consider the interactions between environmental variables, in this case age and hardness of the substratum.
Conservation and management implications
Of the 21 wood dependent lichen species found eleven species were confined to kelo wood (wood >120 years old and with wood hardness 1 and 2) and two almost only occurred here (Table 2). Of the four red-listed species, two were exclusive to old and hard wood and two almost only occurred here (Table 2). This shows that kelo wood is an important substrate for dead wood dependent lichens in boreal P. sylvestris forests. Also in the agricultural landscape, kelo wood is important to wood dependent lichens (cf. Svensson et al. 2005). Special care should therefore be dedicated to such wood. Fire history data indicate that most past fires in boreal forests in Fennoscandia have not been stand replacing and many of the older Pinus sylvestris survived several fires (Kuuluvainen and Aakala 2011). These trees potentially could become kelo trees. Periodic occurrence of fire is important for the maintenance of the Pinus-dominated landscape as fire prevents the invasion of Picea and deciduous trees, while at the same time enhancing conditions for Pinus regeneration, facilitated by the continuous presence of large fire-tolerant Pinus trees (Kuuluvainen et al. 2002). During forest management operations, preserving what is already available of kelo wood is important. For instance, soil scarification practices should be avoided in stands where kelo wood is abundant. Moreover, the formation of this wood type should be supported by setting aside P. sylvestris forests as reserves in which prescribed burnings are carried out and where wild fires are accepted. Even though fire may promote the creation of kelo trees, it may also eliminate existing kelo wood. Therefore, in forests with high conservation values associated to dead wood, prescribed burning may be avoided. Probably it is difficult to create and conserve kelo trees in forests harvested by clearfelling and thinning in the long term, since there is a risk that future forestry operations will destroy future and currently available kelo wood. In general, it is valuable to maintain or develop old-growth forest structural attributes in managed forest landscapes (Bauhus et al. 2009). However, to our knowledge it has not been tested in Sweden if it is possible to create kelo trees in managed boreal landscapes. More knowledge is needed on how to sustain the formation of kelo trees.
Change history
04 September 2018
In the original publication of the article, in Table 2 under the column “Observed frequency fire scars”, the values of species Mycocalicium subtile were published incorrectly as “1” and “0”. However, the values should be “0” and “1”.
References
Ahti L, Jalas J (1968) Vegetation zones and their sections in northwestern Europe. Ann Bot Fenn 5:169–211
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26:32–46. doi:10.1111/j.1442-9993.2001.01070.pp.x
Bauhus J, Puettmann K, Messier C (2009) Silviculture for old-growth attributes. For Ecol Manag 258:525–537. doi:10.1016/j.foreco.2009.01.053
Bendiksby M, Timdal E (2013) Molecular phylogenetics and taxonomy of Hypocenomyce sensu lato (Ascomycota: Lecanoromycetes): extreme polyphyly and morphological/ecological convergence. Taxon 62:940–956. doi:10.12705/625.18
Boch S, Prati D, Hessenmöller D, Schulze ED, Fischer M (2013) Richness of lichen species, especially of threatened ones, is promoted by management methods furthering stand continuity. PLoS ONE 8(1):e55461. doi:10.1371/journal.pone.0055461
Bogomazova K (2012) The ecology of Cladonia botrytes in Sweden. Degree project, Department of Ecology, SLU, Uppsala. http://stud.epsilon.slu.se
Botting RS, De Long C (2009) Macrolichen and bryophyte responses to coarse woody debris characteristics in sub-boreal spruce forest. For Ecol Manag 258:S85–S94. doi:10.1016/j.foreco.2009.08.036
Caruso A, Rudolphi J (2009) Influence of substrate age and quality on species diversity of lichens and bryophytes on stumps. Bryologist 112:520–531. doi:10.1639/0007-2745-112.3.520
Colwell RK (2013) Estimate S: Statistical Estimation of Species Richness and Shared Species from Samples. Version 9.1.0. and earlier. User’s Guide and Application. http://purl.oclc.org/estimates. Accessed Nov 2014
Cowling EB, Merrill W (1966) Nitrogen in wood and its role in wood deterioration. Can J Bot 44:1539–1554. doi:10.1139/b66-167
Cyr D, Gauthier S, Bergeron Y, Carcaillet C (2009) Forest management is driving the eastern North American boreal forest outside its natural range of variability. Front Ecol Environ 7:519–524. doi:10.1890/080088
Esseen P-A, Ehnström B, Ericson L, Sjöberg K (1997) Boreal forests. Ecol Bull 46:16–47
Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391. doi:10.1046/j.1461-0248.2001.00230.x
Green P, Peterken GF (1997) Variation in the amount of dead wood in the woodlands of the Lower Wye Valley, UK in relation to the intensity of management. For Ecol Manag 98:229–238
Grossmann F (2014) Environmental variables determining the occurrence of the red-listed Carbonicola anthracophila and C. myrmecina in boreal forests. Degree project, Department of Ecology, SLU, Uppsala. http://stud.epsilon.slu.se
Grove SJ (2002) Saproxylic insect ecology and the sustainable management of forests. Annu Rev Ecol Syst 33:1–23. doi:10.1146/annurev.ecolsys.33.010802.150507
Hämäläinen A, Kouki J, Lõhmus P (2014) The value of retained Scots pines and their dead wood legacies for lichen diversity in clear-cut forests: the effects of retention level and prescribed burning. For Ecol Manag 324:89–100. doi:10.1016/j.foreco.2014.04.016
Hedberg J, Johansson T, Angelstam P (1998) Dalaskog. Pilotprojekt i landskapsanalys. Rapport 3/1998. Skogsstyrelsens förlag, Jönköping (In Swedish)
Humphrey JW, Davey S, Peace AJ, Ferris R, Harding K (2002) Lichens and bryophyte communities of planted and semi-natural forests in Britain: the influence of site type, stand structure and deadwood. Biol Conserv 107:165–180. doi:10.1016/S0006-3207(02)00057-5
Jaccard P (1908) Nouvelles recerches sur la distribution florale. Bull Soc Vaudoise Sci Nat 44:223–270
Johansson V, Ranius T, Snäll T (2012) Epiphyte metapopulation dynamics are explained by species traits, connectivity, and patch dynamics. Ecology 93:235–241. doi:10.1890/11-0760.1
Jonsson BG, Kruys N, Ranius T (2005) Ecology of species living on dead wood–lessons for dead wood management. Silva Fenn 39:289–309
Jonsson BG, Ekström M, Esseen P-A, Grafström A, Ståhl G, Westerlund B (2016) Dead wood availability in managed Swedish forests—policy outcomes and implications for biodiversity. For Ecol Manag 376:174–182. doi:10.1016/j.foreco.2016.06.017
Junninen K, Komonen A (2011) Conservation ecology of boreal polypores: a review. Biol Conserv 144:11–20. doi:10.1016/j.biocon.2011.04.013
Källén I (2015) Environmental variables determining the occurrence of Cladonia parasitica and Hertelidea botryosa, two boreal lichens confined to wood. Degree project, Department of Ecology, SLU. http://stud.epsilon.slu.se
Kasischke ES, Christensen NL, Stocks BJ (1995) Fire, global warming, and the carbon balance of boreal forests. Ecol Appl 5:437–451. doi:10.2307/1942034
Kruys N, Jonsson BG (1999) Fine woody debris is important for species richness on logs in managed boreal spruce forests of northern Sweden. Can J For Res 29:1295–1299
Kuuluvainen T, Aakala T (2011) Natural forest dynamics in boreal Fennoscandia: a review and classification. Silva Fenn 45(5):823–841
Kuuluvainen T, Aapala K, Ahlroth P, Kuusinen M, Lindholm T, Sallantaus T, Siitonen J, Tukia H (2002) Principles of ecological restoration of boreal forested ecosystems: Finland as an example. Silva Fennica 36:409–422
Kuusinen M, Siitonen J (1998) Epiphytic lichen diversity in old-growth and managed Picea abies stands in southern Finland. J Veg Sci 9:283–292. doi:10.2307/3237127
Lassauce A, Paillet Y, Jactel H, Bouget C (2011) Deadwood as a surrogate for forest biodiversity: meta-analysis of correlations between deadwood volume and species richness of saproxylic organisms. Ecol Indic 11:1027–1039. doi:10.1016/j.ecolind.2011.02.004
Leikola M (1969) The influence of environmental factors on the diameter growth of forest trees. Auxanometric study. Acta For Fenn 92:1–44
Linder P, Östlund L (1998) Structural changes in three mid-boreal Swedish forest landscapes, 1885–1996. Biol Conserv 85:9–19. doi:10.1016/S0006-3207(97)00168-7
Lõhmus P, Kruustük K (2010) Lichens on burnt wood in Estonia: a preliminary assessment. Folia Cryptogam Est 47:37–41
Lõhmus P, Lõhmus A (2001) Snags, and their lichen flora in old Estonian peatland forests. Ann Bot Fenn 38:265–280
Nascimbene J, Marini L, Motta R, Nimis PL (2008) Lichen diversity of coarse woody habitats in a Pinus-Larix stand in the Italian Alps. Lichenologist 40:153–163. doi:10.1017/S0024282908007585
Niemelä T, Wallenius T, Kotiranta H (2002) The kelo tree, a vanishing substrate of specified wood-inhabiting fungi. Polish Bot J 47:91–101
Niklasson M, Granström A (2000) Numbers and sizes of fires: long-term spatially explicit fire history in a Swedish boreal landscape. Ecology 81:1484–1499. doi:10.1890/0012-9658(2000)081[1484:NASOFL]2.0.CO;2
Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, Suggests MASS (2007) The vegan package. Community ecology package, 10
Östlund L, Zackrisson O, Axelsson A-L (1997) The history and transformation of a Scandinavian boreal forest landscape since the 19th century. Can J For Res 27:1198–1206
Pielou EC (1984) The interpretation of ecological data. Wiley InterScience, New York
R Core Team (2014) R: a language and environment for statistical computing. http://www.r-project.org/
Rudolphi J, Gustafsson L (2011) Forests regenerating after clear-cutting function as habitat for bryophyte and lichen species of conservation concern. PLoS ONE 6(4):e18639. doi:10.1371/journal.pone.0018639
Runnel K, Rosenvald R, Lõhmus A (2013) The dying legacy of green-tree retention: different habitat values for polypores and wood-inhabiting lichens. Biol Conserv 159:187–196. doi:10.1016/j.biocon.2012.11.029
Santaniello F, Line DB, Ranius T, Rudolphi J, Widenfalk O, Weslien J (2016) Effects of partial cutting on logging productivity, economic returns and dead wood in boreal pine forest. For Ecol Manag 365:152–158. doi:10.1016/j.foreco.2016.01.033
Seibold S, Bässler C, Brandl R, Gossner MM, Thorn S, Ulyshen MD, Müller J (2015) Experimental studies of dead-wood biodiversity—a review identifying global gaps in knowledge. Biol Conserv 191:139–149. doi:10.1016/j.biocon.2015.06.006
Siitonen J (2001) Forest management, coarse woody debris and saproxylic organisms: Fennoscandian boreal forest as an example. Ecol Bull 49:11–41
Siitonen J, Saaristo L (2000) Habitat requirements and conservation of Pytho kolwensis, a beetle species of old-growth boreal forest. Biol Conserv 94:211–220. doi:10.1016/S0006-3207(99)00174-3
Sirén G (1961) Skogsgränstallen som indikator för klimatfluktuationerna i norra Fennoscandien under historisk tid. Metsäntutkimuslaitoksen Tiedonantoja 54:1–66
Spribille T, Thor G, Bunnell FL, Goward T, Björk CR (2008) Lichens on dead wood: species-substrate relationships in the epiphytic lichen floras of the Pacific Northwest and Fennoscandia. Ecography 31:741–750. doi:10.1111/j.1600-0587.2008.05503.x
Spribille T, Resl P, Ahti T, Pérez-Ortega S, Tønsberg T, Mayrhofer H, Lumbsch HT (2015) Molecular systematics of the wood-inhabiting lichen-forming genus Xylographa (Baeomycetales, Ostropomycetidae) with eight new species. Symb Bot Upsal 37(1):1–87
Stokland J, Siitonen J, Jonsson BG (2012) Biodiversity in dead wood. Cambridge University Press, Cambridge
Svensson M, Johansson P, Thor G (2005) Lichens of wooden barns and Pinus sylvestris snags in Dalarna, Sweden. Ann Bot Fenn 42:351–363
Svensson M, Dahlberg A, Ranius T, Thor G (2013) Occurrence patterns of lichens on stumps in young managed forests. PLoS ONE 8(4):e62825. doi:10.1371/journal.pone.0045701
Svensson M, Johansson V, Dahlberg A, Frisch A, Thor G, Ranius T (2016) The relative importance of stand and dead wood types for wood-dependent lichens in managed boreal forests. Fungal Ecol 20:166–174. doi:10.1016/j.funeco.2015.12.010
Swedish Species Information Centre (2015) Rödlistade arter i Sverige. ArtDatabanken, SLU (In Swedish)
Tarasov ME, Birdsey RA (2001) Decay rate and potential storage of coarse woody debris in the Leningrad region. Ecol Bull 49:137–147
Wagner C, Schram LJ, McMullin RT, Hunt SL, Anand M (2014) Lichen communities in two old-growth pine (Pinus) forests. Lichenologist 46:697–709. doi:10.1017/S002428291400022X
Acknowledgements
We thank Stora Enso Skog AB and Bergvik Skog AB for help during the logging operations in 2012–2013 and Greensway AB for field work assistance and GIS support during the dead wood inventory. This research has been supported by the EU through the Marie Curie Initial Training Networks (ITN) action CASTLE, Grant Agreement No. 316020. The contents of this publication reflect only the authors’ views and the European Union is not liable for any use that may be made of the information contained therein.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by David Hawksworth.
This article belongs to the Topical Collection: Forest and plantation biodiversity.
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
About this article
Cite this article
Santaniello, F., Djupström, L.B., Ranius, T. et al. Large proportion of wood dependent lichens in boreal pine forest are confined to old hard wood. Biodivers Conserv 26, 1295–1310 (2017). https://doi.org/10.1007/s10531-017-1301-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-017-1301-4