G Model FORECO-12168; No. of Pages 7 ARTICLE IN PRESS Forest Ecology and Management xxx (2010) xxx–xxx Contents lists available at ScienceDirect Forest Ecology and Management journal homepage: www.elsevier.com/locate/foreco Epiphytic lichen diversity in old-growth and managed Picea abies stands in Alpine spruce forests Juri Nascimbene a,∗ , Lorenzo Marini b , Pier Luigi Nimis a a b Department of Life Sciences, University of Trieste, via Giorgieri 10 – 34100 Trieste, Italy Department of Environmental Agronomy and Crop Production, University of Padova, viale dell’Università 16 – 35020 Legnaro, Padova, Italy a r t i c l e i n f o Article history: Received 18 March 2010 Received in revised form 12 May 2010 Accepted 12 May 2010 Keywords: Calicioid species Community nestedness Forest management Italian Alps Rare species Successional stage a b s t r a c t In the last decades, a large body of literature has grown to evaluate the impact of forest management on epiphytic lichens in boreal coniferous forests. However, information is still lacking on coniferous forests of the Alps. This study compares lichen diversity between spruce forest stands of four successional stages: (1) young, (2) intermediate, (3) mature forests managed for timber production with a rotation cycle of 120–180 years, and (4) old-growth protected forests. The emphasis was placed on the occurrence of nationally rare and calicioid species (lichens and fungi traditionally referred to as Caliciales, known to be indicative of forest age and continuity). For each forest successional stage, four plots were selected. In each plot, 7 spruce individuals were surveyed for epiphytic lichens according to a standardised sampling method. Species richness increased from young to mature stands, while no difference was detected between mature and old-growth stands. This pattern was also confirmed for rare and calicioid species which are, however, more frequent in old-growth stands. Differences in species composition were also found between the different forest successional stages. Mature and old-growth plots slightly overlap, indicating that to some extent comparable lichen assemblages could be found in these stands. A nested pattern of species assemblages was found, old-growth stands hosting most of the species which were also found in stands belonging to the previous forest successional stages. Our results support the hypothesis that the management regime applied to spruce forests of the Italian Alps renders mature stands managed for timber production somewhat similar to old-growth stands as lichen habitat. However, we found a higher complexity in old-growth forests, and many species of conservation concern clearly preferred old-growth stands. In this perspective, a further prolongation of the normal cycle it is likely to be a most favourable conservation-oriented management to be recommended at least within protected areas and Natura 2000 sites, where conservation purposes should receive a high priority. © 2010 Elsevier B.V. All rights reserved. 1. Introduction In the last decades, a large body of literature has grown to evaluate the impact of forest management on epiphytic lichens in order to provide guidelines for lichen conservation in boreal coniferous forests (e.g. Dettki and Esseen, 1998, 2003; Esseen et al., 1996; Gustafsson et al., 2004; Kuusinen and Siitonen, 1998; Johansson, 2008; Lommi et al., 2009; Perhans et al., 2007; Pykälä, 2003). However, information is still lacking on coniferous forests of the Alps (but see e.g. Nascimbene et al., 2009) and management guidelines for sustainable forestry developed in boreal regions may not necessarily be applicable in mountain regions of South Europe. ∗ Corresponding author. Tel.: +39 043942894; fax: +39 043942894. E-mail address: junasc@libero.it (J. Nascimbene). Boreal spruce forests are mainly logged by clearcutting over large areas with relatively short rotation cycles (e.g. Dettki and Esseen, 2003). For instance Penttilä et al. (2004) reported that in southern Finland the regeneration cutting age of spruce-dominated forests is 90–100 years and forests older than 120 years have traditionally been considered as overmature from the forestry point of view. Analogously, Gustafsson et al. (2004) reported that in Sweden productive forests (mainly coniferous forests) are managed with a rotation cycle of 60–120 years. Due to economic goals, rotation cycles tend to become progressively shorter (e.g. Bauhus et al., 2009; Linder and Östlund, 1998). Spruce forests are also one of the most widespread and economically relevant formations in the Italian Alps (Pignatti, 1998). Management is less intensive than in the boreal zone, being mainly based on progressive thinning of even-aged trees (shelterwood system) and clear-cut over relatively small areas (<1 ha), rotation cycles being longer (120–180 years) than in boreal forests. Despite the fact that management practices of Alpine forests should include 0378-1127/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2010.05.016 Please cite this article in press as: Nascimbene, J., et al., Epiphytic lichen diversity in old-growth and managed Picea abies stands in Alpine spruce forests. Forest Ecol. Manage. (2010), doi:10.1016/j.foreco.2010.05.016 G Model FORECO-12168; No. of Pages 7 2 ARTICLE IN PRESS J. Nascimbene et al. / Forest Ecology and Management xxx (2010) xxx–xxx biodiversity conservation, their ability to sustain rich epiphytic lichen communities and to preserve habitats for sensitive and rare species has never been thoroughly evaluated. Epiphytic lichen communities are influenced by several factors whose importance depends on the scale of the analysis, from the tree-level (e.g. Fritz et al., 2008; Fritz and Heilmann-Clausen, 2010; Johansson et al., 2007; Lie et al., 2009; Nascimbene et al., 2008, 2009; Ranius et al., 2008) to the biogeographical scale (e.g. Bolliger et al., 2007; Ellis et al., 2007; Jovan and Mc Cune, 2004; Martínez et al., 2006). Forest management mainly acts at the stand level, where stand-age is known to be a key factor influencing epiphytic lichen communities. Several studies, mainly conducted in boreal coniferous forests, showed that forest age and species diversity are positively related, and that community composition varies with increasing forest age (e.g. Dettki and Esseen, 1998; Hilmo et al., 2009; Hyvärinen et al., 1992; Moning and Müller, 2009; Peterson and Mc Cune, 2001; Rogers and Ryel, 2008). In this framework, research has also focused on the comparison between forests managed for timber production and forests managed for old-growth, showing that old-growth forests play a key role for the conservation of rare (e.g. Pykälä, 2003) and calicioid species (Tibell, 1992; Selva, 2002). Nevertheless, a balance should be found between conservation and productivity, estimating to what extent the oldest age classes in forests managed for timber production could compensate for the scarcity of forests managed for old-growth conditions. In boreal areas, longer rotation cycles (>120–150 years) have been suggested to improve the effectiveness of lichen conservation by enhancing the presence of lichen species associated with old-growth in stands managed for timber (e.g. Dettki and Esseen, 1998, 2003; Kuusinen and Siitonen, 1998; Johansson, 2008; Peterson and Mc Cune, 2001). This study compares lichen diversity between stands of different age managed for timber production, and old-growth forests managed for nature protection, with emphasis on the occurrence of nationally rare and calicioid species. The main aims are: (1) to compare species richness between young (40–70 years), intermediate (80–120 years), mature (>120 years old) stands managed for timber production and old-growth protected stands (>200 years); and (2) to explore species composition patterns in the four forest successional stages, testing also for community nestedness. The study was planned to answer the conservation questions of which successional stages need to be conserved as important habitats for specialized lichen species and whether mature stands for timber production could be considered as good surrogates of old-growthforests managed for nature protection. Management practices are mainly based on progressive thinning of even-aged trees and clear-cut over relatively small areas (<1 ha) in which mature trees (120–180 years) are felled. Trees with more than 200 years are usually rare in these stands. According to the stage of the management cycle, stands can be classified into three main forest successional stages corresponding to even-aged formations: young forests (40–70 years old, dense and unthinned/once thinned), intermediate forests (80–120 years old, thinned at least twice), and mature forests (>120 years old, ready to be harvested). A small part of the forest (80 ha) is currently protected, being classified as a strict nature reserve. In this area, four 1-ha plots were established in 1993 for long-term monitoring (Motta, 2002; Motta et al., 2002). According to Motta (2002) these stands in which trees older than 200 years (“over-mature trees”) are frequent, can be considered as reference point for (near)-natural conditions and they are here referred to as old-growth forests and included in the survey. 2.2. Lichen survey For each forest successional stage, four 1-ha plots were selected in four different parts of the forest with comparable productivity. Minimum distance between plots of the same successional stage is >1000 m to reduce spatial dependence. The borders of the plots are at least 50 m far from the forest edge. In each plot, 7 spruce individuals were selected for lichen survey by completely random sampling, for a total of 112 trees (28 in each forest successional stage, including old-growth stands). Within old-growth stands, we random sampled only among trees older than 200 years. The lichen inventory followed the guidelines proposed by Stofer et al. (2003) for the Forest BIOTA project (Giordani et al., 2006), which are based on the European guidelines for lichen monitoring (Asta et al., 2002). Lichen diversity was sampled using four standard frames of 10 × 50 cm as sampling grids, subdivided into five 10 × 10 cm quadrats, which were attached to the tree trunk at the cardinal points with the shorter lower side at 100 cm from the ground. All lichen species inside the frames, including the usually underrepresented crustose lichens (Johansson, 2008), were listed and their frequency was computed as the number of 10 × 10 cm quadrats in which the species occurred. Nomenclature follows Nimis and Martellos (2008). For each plot, the total number of living trees, and mean DBH were assessed (Table 1). Stand age was estimated by averaging the age of the trees selected for the lichen survey (see below). Tree age was measured for each tree by extracting cores using a Pressler-type increment borer at a vertical height of 1.30 m. 2. Materials and methods 2.3. Data analysis 2.1. Study area In the analysis of the data (species richness and composition) three guilds of species were considered: (1) all species, (2) nationally rare lichens, and (3) calicioid species. Nimis and Martellos (2008) have assessed the rarity of the species at the national level on the basis of: (a) number of samples in the TSB lichen herbarium, (b) number of literature records, and (c) expert judgement. Eight commonness-rarity classes were used, from extremely rare to extremely common. The ‘extremely rare’ status is given only to taxa known from less than 5 localities in Italy, or to those that were not mentioned in the literature in the last fifty years. Recently described or dubious taxa are excluded from this category. In our analysis, nationally rare lichens correspond to the ‘extremely rare species’ which can be roughly compared to threatened species (Nimis and Martellos, 2008) according to IUCN criteria (2001) and therefore targeted for conservation purposes at the national level. Calicioid species, including lichens and fungi traditionally referred to Caliciales, are mostly related to old-growth forests and are considered The study was carried out in the Paneveggio spruce forest (Paneveggio-Pale di San Martino Natural Park, Trentino-Alto Adige, N-Italy; 46◦ 18′ N, 11◦ 45′ E) which extends over 3000 ha. Altitude ranges from 1500 to 1900 m, average annual temperature is 2.4 ◦ C, annual rainfall is 1200–1300 mm year−1 . The bedrock is porphyry and the soils are rankers and podsols. This forest is one of the larger spruce forests of the Italian Alps (Pignatti, 1998) and has a long history of forestry. Exploitation of the forest is documented starting from the 16th century, but the first management plan was established by the Austrian-Hungarian Monarchy, who owned it until 1919. Subsequently, the forest was entrusted to the Trentino-Alto Adige region of Italy and since the 1970s it belongs to the Autonomous Province of Trento, being included in the Paneveggio-Pale di San Martino Natural Park (Motta et al., 2002). Presently, the forest is managed for timber production. Please cite this article in press as: Nascimbene, J., et al., Epiphytic lichen diversity in old-growth and managed Picea abies stands in Alpine spruce forests. Forest Ecol. Manage. (2010), doi:10.1016/j.foreco.2010.05.016 G Model ARTICLE IN PRESS FORECO-12168; No. of Pages 7 3 J. Nascimbene et al. / Forest Ecology and Management xxx (2010) xxx–xxx Table 1 Main features (±SD) of the stands belonging to the four forest successional stages. Successional stage Tree (ha−1 ) Volume (m3 ha−1 ) DBH (cm) Age (years) Slope (◦ ) Elevation (m) Young Intermediate Mature Old-growth 1178 641 407 591 530 750 830 780 22 35 46 57 49 96 163 271 16 17 16 18 1610 1650 1630 1700 ± ± ± ± 150 75 105 173 ± ± ± ± 110 158 66 196 as suitable indicators of forest sites worthy of conservation and of forest continuity (Selva, 2002). One-way ANOVA was applied to test the effect of the forest successional stage on species richness both at the tree and at the plot level. At both scale we used plot as replicate. The analysis was performed using the total number of species and the numbers of nationally rare and calicioid species, separately. After the ANOVA, a Tukey’s honest significance test for multiple comparisons was applied to detect differences between the four forest successional stages (p < 0.05). To test the influence of forest successional stages on species composition, ordination methods were applied using CANOCO package (Version 4.5, Ter Braak and Šmilauer, 2002). The response variable was the species by plot matrix based on species frequencies at the plot level. A preliminary Detrended Correspondence Analysis (DCA) was performed. The largest DCA gradient length, expressed in standard deviation (SD) units of species turnover, of the first four DCA axes was below 3 S.D. units (total inertia = 1.875). Thus, the use of linear-based ordination models was appropriate for these data (Ter Braak and Šmilauer, 2002). First, a Principal Component Analysis (PCA) was performed to extract the main part of the variability related to species composition. Second, a Redundancy Analyses (RDA) was applied, using the forest successional stage as a factor quantified by four dummy variables, and a separate Monte Carlo permutation test with 999 permutations (p < 0.05). We quantified the pattern of nestedness with the discrepancy index (BR) (Brualdi and Sanderson, 1999). This index is a count of the number of discrepancies (absences or presences) that must be erased to produce a perfectly nested matrix. The smaller the BR score is, the stronger is the pattern of nestedness. To test significance we performed a permutation test (n = 1000) using the quasiswap method (Miklós and Podani, 2004). Analyses were run using the vegan R package (R Development Core Team, 2008). An Indicator Species Analysis (ISA; Dufrêne and Legendre, 1997) was used to determine how strongly each species was associated to different forest successional stages. For each species, the Indicator Value (IV) ranges from 0 (no indication) to 100 (maximum indication). Statistical significance of IV was tested by means of a Monte Carlo test, based on 10,000 randomizations. Indicator Species Analysis and Monte Carlo test were performed by PC-ORD (McCune and Mefford, 1999). ± ± ± ± 3 4 5 10 ± ± ± ± 5 29 31 62 ± ± ± ± 4 3 2 2 ± ± ± ± 73 80 68 86 3 and 10 of which were exclusive to mature and old growth stands. These species were absent in young stands. Significant differences in species richness were found among stands of different age (Table 2), both at the tree (mean number of species per tree), and at the plot level (mean number of species per plot). Species richness increased from young to mature stands, while no significant difference was detected between mature and old-growth stands. However, old-growth stands tends to have higher values than mature stands. This pattern was also confirmed for rare and calicioid species. 3.2. Species composition In the PCA ordination (Fig. 1a), the two axes explain 59.2% of the total variation in species composition (38.5% axis 1 and 20.7% axis 2). Plots belonging to different forest successional stages were clearly separated, indicating differences in species composition. However, mature and old-growth plots slightly overlap, indicating that to some extent comparable lichen assemblages could be found in these stands. The heterogeneity of stands within successional stages increases with stand age, young stands being very similar, while old-growth stands had the highest heterogeneity. In the RDA ordination, which is constrained to the forest successional stage (Fig. 1b), the two axes explain 41% of the total variation (31.4% axis 1 and 9.6% axis 2). The number of species was positively associated with stands of increasing age, while no species was associated to young stands. Hypogymnia physodes, and to some extent H. tubulosa and Vulpicida pinastri were mainly associated with intermediate stands, 8 species – including e.g. Chrisotrix candelaris, Parmelia saxatilis, and Platismatia glauca – were associated with mature stands, while 15 species were associated to old-growth stands. Interestingly, among the latter there were 2 rare and 5 calicioid species (e.g. Cyphelium inquinans and C. karelicum). Nestedness analysis revealed a significant nested pattern of species assemblages (nestedness discrepancy BR = 71, p < 0.01). Old-growth stands hosted most of the species which were also found in stands belonging to the previous forest successional stages. The results of the Indicator Species Analysis confirmed this pattern (Appendix A). Most species had their maximum Indicator Value in the older stands (mature and old-growth forests). No species was significantly associated to young and intermediate stands, while 7 species were significantly associated to mature (2 species) and old-growth stands (5 species). 3. Results 3.1. Species richness Sixty-four lichens and two non-lichenised fungi (Chaenothecopsis pusilla and Microcalicium disseminatum) were found (Appendix A). The overall number of species increased from young to oldgrowth stands (18, 31, 45, and 56). Old-growth and mature stands pooled together hosted 95% of the total flora. Nineteen percent of the species occurred in all forest successional stages, the most abundant being Hypogymnia physodes, Ochrolechia microstictoides, Parmelia saxatilis, P. sulcata, and Platismatia glauca. No species was exclusively found in young stands, 2 species were exclusive to intermediate stands, 1 species to mature stands, and 14 to old-growth stands (Appendix A). Five rare and 14 calicioid species were found, Table 2 Results of the one-way ANOVA and Tukey’s honest significance test for multiple comparisons. In the ANOVA at the tree level we used the mean value per plot (n = 16) to avoid pseudoreplication. Characteristics Young Intermediate Tree level Total species Rare species Calicioid species 5.0a 0.0a 0.0a 9.7b 0.5ab 0.6a Plot level Total species Rare species Calicioid species 11.0a 0.0a 0.0 a 19.7b 1.00ab 1.25a Mature Old-growth pa 14.1c 1.0b 3.4b 14.2c 1.2b 4.0b <0.001 0.001 <0.001 26.5c 2.75bc 6.25b 30.0c 3.00c 7.50b <0.001 <0.001 <0.001 Different letters mark mean values which are significantly different. Please cite this article in press as: Nascimbene, J., et al., Epiphytic lichen diversity in old-growth and managed Picea abies stands in Alpine spruce forests. Forest Ecol. Manage. (2010), doi:10.1016/j.foreco.2010.05.016 G Model FORECO-12168; No. of Pages 7 4 ARTICLE IN PRESS J. Nascimbene et al. / Forest Ecology and Management xxx (2010) xxx–xxx Fig. 1. (a) PCA ordination diagram of the 16 plots against the first two principal components and (b) RDA ordination diagram of lichen species occurring in the 16 plots against the first two canonical axes constrained by management stage. In parentheses the explained variation by each axis is reported. () indicate categorical variables; (↑) indicate species. Species abbreviations as provided in Appendix A. 4. Discussion Species richness increased from younger to older stands, but mature stands managed for timber production and old-growth stands host a comparably richer lichen biota, even if a higher complexity was found in old growth stands. A similar pattern was also found by Kuusinen and Siitonen (1998) in their evaluation of epiphytic lichen communities in old-growth and managed spruce forests of Southern Finland, while in boreal Sweden Gustafsson et al. (2004) demonstrated that also old mature (≥110 years) forests managed for timber could be relevant for red-listed lichens. In both cases, the potential role of mature timber managed forests composed by relatively old trees as surrogate for old-growth conditions is stressed against the tendency in boreal areas to decrease the rotation cycles for better achieving the economic targets. While the boreal model based on short rotation and clearcutting is far from allowing the development of any old-growth attribute within production stands, the alpine model based on longer rotation cycle is more easily adaptable to conservation purposes permitting at least the presence of some old-growth attributes such as scattered old trees within production forests. This difference is expected to produce positive effects on old growth-associated lichens. In alpine forests, the similarity of lichen richness between mature stands managed for timber production and old-growth stands could be favoured by the management regime which allows the presence of mature forest patches which reach or even (rarely) exceed 180 years. Actually, the presence of over-mature (>200 years old) trees is the main old-growth attribute of protected stands (Motta, 2002) which could account for the larger overall number of epiphytic lichens and for the differences in species composition, especially related to nationally rare and calicioid species, with mature stands managed for timber production. This hypothesis is also supported by the ISA results, indicating that most of the rare and calicioid species have their maximum indicator value in old-growth stands. Some of these species are strictly associated to old-growth stands, such as the two nationally rare Cyphelium species. This suggests that a potential threat to several epiphytic lichens in the Italian Alps could be reduced by increasing the availability of stands with over-mature trees in timber managed spruce forests. A similar perspective was proposed for beech forests by Fritz et al. (2008) who found that the association to high tree age commonly excludes red-listed lichens from conventionally managed forests with a 100–140-year rotation cycle, while Moning and Müller (2009) calculated a critical forest age threshold of 220 years to maintain high lichen diversity levels, considering both all species and red-listed species. Species assemblages present a nested pattern across stands of different successional stages, communities of young stands being subsets of more diverse assemblages present in the oldest stands. Similarly to the results of Hilmo et al. (2009) in boreal spruce plantations, differences in species composition among forest stands of different age could be attributed to a process of species accumulation with increasing stand age, rather than to species turnover. This nested pattern is also supported by RDA and ISA analyses which revealed the absence of species associated (or exclusive) to the younger stands. As a consequence, older stands play a key role for maintaining lichen diversity at the forest scale, providing the suitable habitat for most of the epiphytic lichen biota. These stands also act as important refuges and sources of propagules which can favourably establish and develop in the surrounding stands (Moning and Müller, 2009; Peck and McCune, 1997; Sillett and Goslin, 1999). 5. Management implications Our results support the hypothesis that the management regime applied to spruce forests of the Italian Alps renders mature stands managed for timber production somewhat similar to old-growth stands as lichen habitat. However, we found a higher complexity in old-growth forests, and many species of conservation concern preferred old-growth stands. Some differences could be less pronounced for timber managed stands which are felled at the maximum of the rotation cycle. In this perspective, a further 20–40 years prolongation of the normal cycle it is likely to be a most favourable conservation-oriented management to be applied at least to a selected number of stands. However, according to many studies many rare species have clumped distribution patterns on different spatial scales, which suggests restricted establishment on different spatial scales. This should also be accounted for when selecting stands that could have prolonged rotation periods (e.g. vicinity to old-growth stands should, thus, also be considered). This strategy would employ the concept of flexibility to achieve the multiplicity of functions which are currently assigned to forests. However, despite the fact that extended and flexible rotation cycles could positively influence the old-growth attributes of forests related to the presence of large, old trees, Bauhus et al. Please cite this article in press as: Nascimbene, J., et al., Epiphytic lichen diversity in old-growth and managed Picea abies stands in Alpine spruce forests. Forest Ecol. Manage. (2010), doi:10.1016/j.foreco.2010.05.016 G Model ARTICLE IN PRESS FORECO-12168; No. of Pages 7 5 J. Nascimbene et al. / Forest Ecology and Management xxx (2010) xxx–xxx (2009) stressed the importance of a multi-task approach to increase the degree of old-growth characteristics in managed forested landscapes. For example, Dettki and Esseen (2003), and Johansson (2008) indicated that an effective strategy to maintain large lichen populations and rare species should include long rotation cycles in combination with the presence of set-aside forest reserves. This could also apply to our study area in which forest reserves are included in a matrix mainly composed by stands managed for timber production and could explain the exceptional richness of its overall lichen biota (Thor and Nascimbene, 2007). The long and flexible rotation cycles which ensure the presence of forest patches hosting old, large trees, combined with the presence of scattered patches of unmanaged stands could be an effective strategy to improve long term epiphytic lichen conservation in the future forest landscape of the Italian Alps without causing relevant economic losses. This model should be tested within protected areas and Natura 2000 sites, where conservation purposes should receive a high priority. Species Bacidia absistens Lepraria lobificans Melanelixia fuliginosa Parmelia sulcata Rinodina capensis Bryoria capillaris Buellia griseovirens Chaenotheca stemonea Evernia prunastri Hypogymnia physodes Hypogymnia tubulosa Micarea prasina Ochrolechia arborea Ochrolechia microstictoides Pertusaria amara Ramalina farinacea Ramalina obtusata Tuckneraria laureri Vulpicida pinastri Calicium glaucellum Calicium viride Caloplaca herbidella Chaenotheca hispidula Chaenotheca subroscida Chaenothecopsis pusilla Chrysothrix candelaris Cladonia coniocraea Hypogymnia bitteri Lecanora argentata Lecanora cadubriae Lepraria rigidula Lopadium disciforme Mykoblastus affinis Ochrolechia androgyna Parmelia saxatilis Platismatia glauca Schismatomma pericleum Bryoria fuscescens Buellia schaereri Chaenotheca chrysocephala Chaenotheca ferruginea Chaenotheca laevigata Chaenotheca trichialis Cladonia digitata Cyphelium inquinans Cyphelium karelicum Cyphelium tigillare Evernia divaricara Hypogymnia austerodes Hypogymnia farinacea Imshaugia aleurites Lecanora circumborealis Lecanora pulicaris Species abbreviations baabs leplob melful parsulc rincap brycap bugris chast evprun hypphy hyptub micpra ocharb ochmicr peram ramfar ramobt tucklau vulpin calgla calvir calohe chahis chasub chapus chrcan clacon hypbit lecarg leccad leprig lopdisc mykaff ochand parsax plagla schper bryfus busch chachr chafer chalae chatric cladig cypinq cypkar cyptigi evediv hypaus hypfar imsale leccirc lecpul NRS Cal + + + + + + + + + + + + + + + + + + Acknowledgements The work was funded and supported by the Parco Naturale Paneveggio-Pale di San Martino (Trento). We are also grateful to the Agenzia Provinciale delle Foreste Demaniali for providing information on forest management and for logistic support during the field work. Andrea Laschi (Firenze) and Marilena Dalle Vedove (Feltre) are thanked for their contribution during the field work. The Editor, Péter Ódor, and two anonymous referees are thanked for providing stimulating improvements to the manuscript. Appendix A. Species list. Species are ordered according to the successional stage in which the indicator value is maximum, following the results of the indicator species analysis. Nomenclature follows Nimis and Martellos (2008). Frequency in the management stage (%) Y I M O 75 25 25 100 50 0 50 0 0 100 0 50 0 75 25 0 0 0 100 0 0 0 0 0 0 0 0 25 0 0 0 0 0 25 75 100 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 25 0 0 100 0 75 75 25 50 100 75 50 50 100 75 50 25 50 75 0 50 0 0 25 0 0 0 100 0 25 0 0 50 0 100 100 50 75 0 25 0 0 0 0 0 0 0 25 0 0 0 0 0 0 0 0 75 0 50 50 0 0 100 75 0 50 100 50 25 25 50 75 100 100 25 25 50 25 100 25 75 25 25 25 25 100 50 100 100 100 25 25 100 0 25 100 25 50 50 0 75 0 0 0 0 25 0 0 0 100 0 75 75 0 0 100 0 0 25 75 75 50 25 50 25 100 100 0 25 0 25 50 25 50 25 25 25 25 50 25 100 100 25 50 50 75 50 50 100 50 100 100 25 75 25 50 25 25 25 Successional stage Indicator value Y Y Y Y Y I I I I I I I I I I I I I I M M M M M M M M M M M M M M M M M M O O O O O O O O O O O O O O O O 47.4 25.0 25.0 36.1 50.0 38.1 31.9 25.0 50.0 30.8 51.6 33.3 30.0 37.4 26.4 45.6 12.5 32.6 32.8 69.5* 43.0 25.0 19.1 32.7 16.2 77.4** 12.5 33.7 12.5 15.5 19.2 12.5 50.5 17.7 36.6 45.9 51.8 36.7 28.3 48.3 50.0 20.0 75.0* 40.0 86.5* 88.3** 25.0 46.2 25.0 50.0 25.0 25.0 16.7 Please cite this article in press as: Nascimbene, J., et al., Epiphytic lichen diversity in old-growth and managed Picea abies stands in Alpine spruce forests. Forest Ecol. Manage. (2010), doi:10.1016/j.foreco.2010.05.016 G Model ARTICLE IN PRESS FORECO-12168; No. of Pages 7 6 J. Nascimbene et al. / Forest Ecology and Management xxx (2010) xxx–xxx Appendix A (Continued) Species Species abbreviations Lecanora varia Lecidea leprarioides Lepraria elobata Letharia vulpina Microcalicium disseminatum Mykoblastus sanguinarius Ochrolechia alboflavescens Parmeliopsis ambigua Parmeliopsis hyperopta Pseudevernia furfuracea Ramalina thrausta Tuckermannopsis chlorophylla Usnea hirta lecvar lecilep lepelo lethvul micrdis myksan ochalb paramb parhyp psfur ramthr tuckchl usnhir NRS Cal Frequency in the management stage (%) Y + 0 0 0 0 0 0 0 25 0 50 0 25 0 I M O 0 25 0 0 0 0 0 75 0 100 0 100 0 0 50 0 0 0 0 50 100 0 75 0 50 0 25 50 25 25 50 25 50 100 75 100 25 100 25 Successional stage Indicator value O O O O O O O O O O O O O 25.0 21.8 25.0 25.0 50.0 25.0 34.2 54.6* 75.0* 66.9 25.0 74.3 25.0 Species abbreviations are those which are used in the ordination plots of Fig. 1. NRS: Nationally rare species. Cal: Calicioid species. Species frequency in each successional stage is expressed by the percentage of plots of each stage in which the species occurred. Y: young stands; I: intermediate stands; M: mature stands; O: old-growth stands. “*” marks significant indicator species at p < 0.05, and “**” at p < 0.01. References Asta, J., Erhardt, W., Ferretti, M., Fornasier, F., Kirschbaum, U., Nimis, P.L., Purvis, W., Pirintsos, S., Scheidegger, C., Van Haluwyn, C., Wirth, V., 2002. Mapping lichen diversity as an indicator of environmental quality. In: Nimis, P.L., Scheidegger, C., Wolseley, P. (Eds.), Monitoring with Lichens, Monitoring Lichens. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 273– 279. Bauhus, J., Puettmann, K., Messier, C., 2009. Silviculture for old-growth attributes. Forest Ecol. Manag. 258, 525–537. Bolliger, J., Bergamini, A., Stofer, S., Kienast, F., Scheidegger, C., 2007. Predicting the potential spatial distributions of epiphytic lichen species at the landscape scale. Lichenologist 39, 279–291. Brualdi, R.A., Sanderson, J.G., 1999. Nested species subsets, gaps, and discrepancy. Oecologia 119, 256–264. Dettki, H., Esseen, P.A., 1998. Epiphytic macrolichens in managed and natural forest landscapes: a comparison at two spatial scales. Ecography 21, 613– 624. Dettki, H., Esseen, P.A., 2003. Modelling long-term effects of forest management on epiphytic lichens in northern Sweden. Forest Ecol. Manage. 175, 223–238. Dufrêne, M., Legendre, P., 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol. Monogr. 67, 345–366. Ellis, C.J., Coppins, B.J., Dawson, T.P., Seaward, M.R.D., 2007. Response of British lichens to climate change scenarios: trends and uncertainties in the projected impact for contrasting biogeographic groups. Biol. Conserv. 140, 217–235. Esseen, P.A., Renhorn, K.E., Pettersson, R.B., 1996. Epiphytic lichen biomass in managed and old-growth boreal forests: effect of branch quality. Ecol. Appl. 6, 228–238. Fritz, Ö., Niklasson, M., Churski, M., 2008. Tree age is a key factor for the conservation of epiphytic lichens and bryophytes in beech forests. Appl. Veg. Sci. 12, 93– 106. Fritz, Ö., Heilmann-Clausen, J., 2010. Rot holes create key microhabitats for epiphytic lichens and bryophytes on beech (Fagus sylvatica). Biol. Conserv. 143, 1008–1016. Giordani, P., Brunialti, G., Nascimbene, J., Gottardini, E., Cristofolini, F., Isocrono, D., Matteucci, E., Paoli, L., 2006. Aspects of biological diversity in the CONECOFOR plots. III. Epiphytic lichens. Ann. Ist. Sper. Selv. 30, 43–50. Gustafsson, L., Appelgren, L., Jonsson, F., Nordin, U., Persson, A., Weslien, J.O., 2004. High occurrence of red-listed bryophytes and lichens in mature managed forests in boreal Sweden. Basic Appl. Ecol. 5, 123–129. Hilmo, O., Holien, H., Hytteborn, Ely-Aalstrup, H., 2009. Richness of epiphytic lichens in differently aged Picea abies plantations situated in the oceanic region of Central Norway. Lichenologist 41, 97–108. Hyvärinen, M., Halonen, P., Kauppi, M., 1992. Influence of stand age and structure on the epiphytic lichen vegetation in the middle-boreal forests of Finland. Lichenologist 24, 165–180. IUCN, 2001. IUCN Red List Categories and Criteria: Version 3.1. IUCN Species Survival Commission. Gland, Cambridge: IUCN. 30 p. 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. Johansson, P., 2008. Consequences of disturbance on epiphytic lichens in boreal and near boreal forests. Biol. Conserv. 141, 1933–1944. Johansson, P., Rydin, H., Thor, G., 2007. Tree age relationships with epiphytic lichen diversity and lichen life history traits on ash in southern Sweden. Ecoscience 14, 81–91. Jovan, S., Mc Cune, B., 2004. Regional variation in epiphytic macrolichen communities in northern and central California forests. Bryologists 107, 328–339. Lie, M.H., Arup, U., Grytnes, J.A., Ohlson, M., 2009. The importance of host tree age, size and growth rate as determinats of epiphytic lichen diversity in boreal spruce forests. Biodivers. Conserv. 18, 3579–3596. Linder, P., Östlund, L., 1998. Structural changes in three mid-boreal forest landscapes, 1885–1996. Biol. Conserv. 85, 9–19. Lommi, S., Berglund, H., Kuusinen, M., Kuuluvainen, T., 2009. Epiphytic lichen diversity in late-successional Pinus sylvestris forests along local and regional forest utilization gradients in eastern boreal Fennoscandia. Forest Ecol. Manage. 259, 883–892. Martínez, I., Carreño, F., Escudero, A., Rubio, A., 2006. Are threatened lichen species well-protected in Spain? Effectiveness of a protected areas network. Biol. Conserv. 133, 500–511. McCune, B., Mefford, M.J., 1999. Multivariate analysis of ecological data. Version 4.25. MjM Software, Gleneden Beach, Oregon, US. Miklós, I., Podani, J., 2004. Randomization of presence/absence matrices: comments and new algorithms. Ecology 85, 86–92. Moning, C., Müller, J., 2009. Critical forest age thresholds for the diversity of lichens, molluscs and birds in beech (Fagus sylvatica L.) dominated forests. Ecol. Ind. 9, 922–932. Motta, R., 2002. Old-growth forests and silviculture in the Italian Alps: the case–study of the strict reserve of Paneveggio (TN). Plant Biosyst. 136, 223– 232. Motta, R., Nola, P., Piussi, P., 2002. Long-term investigations in a strict forest reserve in the eastern Italian Alps: spatio-temporal origin and development in two multi-layered subalpine stands. J. Ecol. 90, 495–507. Nascimbene, J., Marini, L., Motta, R., Nimis, P.L., 2009. Influence of tree age, tree size and crown structure on lichen communities in mature Alpine spruce forests. Biodivers. Conserv. 18, 1519–1522. Nascimbene, J., Marini, L., Carrer, M., Motta, R., Nimis, P.L., 2008. Influences of tree age and tree structure on the macrolichen Letharia vulpina: a case study in the Italian Alp. Ecoscience 15, 423–428. Nimis, P.L., Martellos, S., 2008. ITALIC—The Information System on Italian Lichens. Version 4.0. University of Trieste, Dept. of Biology, IN4.0/1 (http://dbiodbs.univ.trieste.it/). Peck, J.L.E., McCune, B., 1997. Remnant tress and canopy lichen communities in Western Oregon: a retrospective approach. Ecol. Appl. 7, 1181–1187. Penttilä, R., Siitonen, J., Kuusinen, M., 2004. Polypore diversity in managed an old-growth boreal Picea abies forests in southern Finland. Biol. Conserv. 117, 271–283. Perhans, K., Gustafsson, L., Jonsson, F., Nordin, U., Weibull, H., 2007. Bryophytes and lichens in different types of forest set-asides in boreal Sweden. Forest Ecol. Manage. 242, 374–390. Peterson, E., Mc Cune, B., 2001. Diversity and succession of epiphytic macrolichen communities in low-elevation managed conifer forests in Western Oregon. J. Veg. Sci. 12, 511–524. Pignatti, S., 1998. I Boschi d’Italia. Sinecologia e Biodiversità. UTET, Torino. Pykälä, J., 2003. Effects of new forestry practices on rare epiphytic macrolichens. Conserv. Biol. 18, 831–838. R Development Core Team, 2008. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3900051-07-0, URL http://www.R-project.org. Ranius, T., Johansson, P., Niclas, B., Niklasson, M., 2008. The influence of tree age and microhabitat quality on the occurrence of crustose lichens associated with old oaks. J. Veg. Sci. 19, 653–662. Rogers, P.C., Ryel, R.J., 2008. Lichen community change in response to succession in aspen forests of the Rocky Mountains, USA. Forest Ecol. Manage. 256, 1760–1770. Please cite this article in press as: Nascimbene, J., et al., Epiphytic lichen diversity in old-growth and managed Picea abies stands in Alpine spruce forests. Forest Ecol. Manage. (2010), doi:10.1016/j.foreco.2010.05.016 G Model FORECO-12168; No. of Pages 7 ARTICLE IN PRESS J. Nascimbene et al. / Forest Ecology and Management xxx (2010) xxx–xxx Selva, S.B., 2002. Indicator species—restricted taxa approach in coniferous and hardwood forests of northeastern America. In: Nimis, P.L., Scheidegger, C., Wolseley, P. (Eds.), Monitoring with Lichens, Monitoring Lichens. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 349–357. Sillett, S.C., Goslin, M.N., 1999. Distribution of epiphytic macrolichens in relation to remnant trees in a multiple-age Douglas-fir forest. Can. J. Forest Res. 29, 1204–1215. Stofer, S., Catalayud, V., Ferretti, M., Fischer, R., Giordani, P., Keller, C., Stapper, N., Scheidegger, C., 2003. Epiphytic Lichen Monitoring within the 7 EU/ICP Forests Biodiversity Test-Phase on Level II 28 plots. Available from: http://www.forestbiota.org. Ter Braak, C.J.F., Šmilauer, P., 2002. CANOCO Reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination (version 4.5). Microcomputer Power, Ithaca, USA. Thor, G., Nascimbene, J., 2007. A floristic survey in the Southern Alps: additions to the lichen flora of Italy. Cryptogamie Mycol. 28, 247–260. Tibell, L., 1992. Crustose lichens as indicators of forest continuity in boreal coniferous forests. Nord. J. Bot. 12, 427–450. Please cite this article in press as: Nascimbene, J., et al., Epiphytic lichen diversity in old-growth and managed Picea abies stands in Alpine spruce forests. Forest Ecol. Manage. (2010), doi:10.1016/j.foreco.2010.05.016