Science of the Total Environment 487 (2014) 110–116

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A multi-taxon approach reveals the effect of management intensity on biodiversity in Alpine larch grasslands Juri Nascimbene a,b,⁎, Veronika Fontana c, Daniel Spitale a a b c

Nature Museum of South Tyrol, Via Bottai 1, 39100 Bolzano, Italy Department of Life Sciences, University of Trieste, Via Giorgieri 10, 34100 Trieste, Italy Department of Ecology, University of Innsbruck, Sternwartestrasse 15, 6020 Innsbruck, Austria

H I G H L I G H T S • • • •

In the Alps larch grasslands form one of the most pleasing aspects of the landscape. A multi-taxon approach was used to evaluate the effects of management intensity. Management intensity influences the biodiversity of autotrophic organisms. Higher biodiversity was found in extensively managed larch grasslands.

a r t i c l e

i n f o

Article history: Received 8 February 2014 Received in revised form 3 April 2014 Accepted 3 April 2014 Available online xxxx Editor: J. P. Bennett Keywords: Abandonment Bryophytes Fertilization Lichens Management intensification Vascular plants

a b s t r a c t In the Alps, larch grasslands form one of the most pleasing aspects of the landscape. However, their effectiveness in contributing to biodiversity conservation may depend on the intensity of their management. We used a multitaxon approach to evaluate the effects of the intensification of management practices and those of abandonment on the biodiversity of the main autotrophic organisms hosted in this habitat, including vascular plants, bryophytes, and lichens. The study was carried out in the eastern part of South Tyrol, in the Italian Alps, where the diversity patterns of these three organismal groups were compared among intensively managed, extensively managed, and abandoned stands. The management intensity was found to strongly influence the biodiversity of the organisms, with a general pattern indicating the best conditions in extensively managed stands. Both abandonment and management intensification were detrimental to biodiversity through different mechanisms that led to species loss or to major shifts in species composition. However, the most negative effects were related to management intensification, mainly due to the high nitrogen supply, providing evidence for the increasing impact of eutrophication on Alpine environments. © 2014 Elsevier B.V. All rights reserved.

1. Introduction In the European Alps, agriculture and forestry played an important role in shaping the economy and the human population structure up to the beginning of the 20th century (Tasser et al., 2013). Several traditional management types, such as coppice forests, orchards, mountain-pasturing and double-use systems, developed over time in rural areas. In the 1950s, technical progress in the machinery and equipment used for agriculture and the growth of tourism and industry strongly influenced the agriculture and forestry in mountain areas

⁎ Corresponding author at: Department of Life Sciences, University of Trieste, Via Giorgieri 10, 34100 Trieste, Italy. Tel./fax: +39 043942894. E-mail addresses: [email protected] (J. Nascimbene), [email protected] (V. Fontana), [email protected] (D. Spitale).

http://dx.doi.org/10.1016/j.scitotenv.2014.04.013 0048-9697/© 2014 Elsevier B.V. All rights reserved.

(Krausmann et al., 2003; Streifeneder et al., 2007) through two contrasting processes: the intensification of land-use in more favorable sites, and complete abandonment of less favorable sites (Zimmermann et al., 2010). Traditional farming practices, which require significant effort and manual labor, declined throughout Europe (MacDonald et al., 2000; Bergmeier et al., 2010). In the Alps, larch grasslands are one of the traditional management types that are still locally maintained across the montane and subalpine belts, forming one of the most pleasing aspects of the landscape (Fontana et al., 2014). Larch grasslands consist of meadows or pastures with scattered larch (Larix decidua Mill.) individuals. This anthropogenic landscape was found to provide several ecosystem services benefiting human well-being, for example, offering opportunities for recreation, providing cultural and historical value and providing diverse habitats that harbor several species of conservation concern (Fontana et al., 2013; Nascimbene et al., 2006).

J. Nascimbene et al. / Science of the Total Environment 487 (2014) 110–116

The effectiveness of larch grasslands in contributing to biodiversity conservation in Alpine landscapes may, however, depend on the intensity of their management (Tasser and Tappeiner, 2002). In particular, stands managed using traditional methods based on non-intensive practices are expected to benefit several organism groups (MacDonald et al., 2000), hosting a community that is richer in species than either intensively managed or abandoned stands (the intermediate disturbance hypothesis; Grime, 1973; Hilbert et al., 1981; Molino and Sabatier, 2001; Svensson et al., 2007). However, this pattern may differ among organisms exploiting different resources and substrates and may also lead to severe shifts in assemblage composition (Poschlod et al., 2005; Paillet et al., 2009). For example, plant communities are expected to be negatively affected by mowing frequency (Nascimbene et al., 2013a), and many terricolous and epiphytic bryophytes may benefit from abandonment, preferring closed, canopied forests (Fenton and Frego, 2005). However, Paltto et al. (2008) noted that excessive canopy closure related to the development of secondary woodlands could place many epiphytic lichens at a disadvantage (Paltto et al., 2011). Moreover, the augmentation of nitrogen input related to management intensification could lead to a decrease in species richness and to a change in the composition of autotrophic species, as eutrophication is recognized as one of the main threats to vegetation in natural and semi-natural ecosystems (Kleijn et al., 2009). In particular, epiphytic lichens and forest floor bryophytes are extremely sensitive to nitrogen loads, which cause the rarefaction of many forest species and the establishment of nitrogen-tolerant species across Europe (Dirkse and Martakis, 1992; Giordani et al., 2014). This work aimed to evaluate the effects of both intensification of management practices and of abandonment on the biodiversity of Alpine larch grasslands. In particular, our study is based on a multitaxon approach in which we tested the effect of (i) intensively managed stands that are mown and fertilized, (ii) extensively managed stands that are either mown and fertilized or used for grazing, and (iii) abandoned stands, in which forest succession is occurring on larch grasslands that were abandoned 20–50 years ago, on vascular plant and cryptogam (bryophyte and lichen) diversity. These organisms are best suited to encompass the composite habitat structure of Alpine larch grasslands, which provide establishment opportunities for both soil-dwelling and epiphytic species. According to the intermediate disturbance hypothesis (Svensson et al., 2007), we expected greater diversity in extensively managed stands than in the other stand types. However, we hypothesized that the response to management intensity may differ among organisms with different traits and ecological requirements and, due to their strong sensitivity to environmental conditions (e.g., Giordani et al., 2014), we expected that epiphytic lichens would be the most responsive organisms. 2. Materials and methods 2.1. Study area The study was carried out in the eastern part of South Tyrol (7400 km2, Italian Alps) in the region of the Pusteria valley, east of the city of Bressanone (46°43′ N, 11°39′ E; see map in Appendix A in Supplementary data). Because the area is surrounded by mountain chains, i.e., the main Alpine ridge in the north and the Dolomites in the south, large parts of the area lay above 1000 m a.s.l. (ASTAT, 2011). The climate is Northern Central European, with a mean annual precipitation of approximately 1000 mm in the upper montane belt and with the precipitation maxima occurring in summer. The mean annual temperature is 6 °C in the bottom of the valley, while in the alpine belt it is 3 °C (Autonome Provinz Bozen—Südtirol, 2010). In this region, larch grasslands are subject to three main management types, corresponding to a gradient of management intensity: (1) intensively managed stands that are mown and fertilized twice per year (max. 10 Mg ha−1 stall manure per year, corresponding to c. 230 kg ha−1 N

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per year); (2) extensively managed stands that are either mown and fertilized (max. 3 Mg ha− 1 stall manure per year corresponding to c. 70 kg ha− 1 N per year) once per year or used for grazing; and (3) abandoned stands, in which forest succession is allowed to proceed on larch grasslands that were abandoned 20–50 years ago. 2.2. Sampling design The study area was divided into several forest domains corresponding to administrative units for both forestry and agriculture (Appendix A). Using GIS (Arcmap 10), we selected the four forest domains hosting the highest number of larch grasslands according to the official distribution map (Autonome Provinz Bozen — Südtirol, 2011). Information on abandoned larch grasslands was derived from historical land-use maps (land register of Emperor Francis I, 1861, vegetation map; Peer, 1980) and by interviewing the local forest rangers. The mean field size of the individual larch grasslands was approximately 2.5 ha. Subsequently, we randomly selected 7 circular plots (r = 10 m, area = 314 m2) for each of the three stand types (intensively managed, nonintensively managed, and abandoned), in order to encompass the variability of each stand type in the study area. To reduce spatial dependence, the minimum distance between plots of the same management type was chosen to be greater than 500 m. The slope, aspect, elevation, and soil pH were comparable among the management types, while the tree density and the carbon/nitrogen ratio intrinsically differed between the abandoned and managed stands (Table 1). The carbon/nitrogen ratio of the soil was measured for each plot; using a split-tube sampler (Eijkelkamp, diameter = 4.2 cm; height = 20 cm), we collected a soil sample from the center of the plot. Roots were removed and soil samples were sorted into gravel and mineral soil using a sieve (2 mm mesh size). The dry weights of the soil samples were determined after drying at 65 °C for 24 h. The total organic carbon and nitrogen contents of the mineral soil samples were determined using an elemental analyzer (Thermo Scientific, Flash EA 2000). 2.3. Sampling of the biota In each of the plots whose dimensions were between the required minimum area for meadows (25 m2) and that of forests (500 m2, Dierßen, 1990), all vascular plants were recorded, and the abundance was visually estimated for each species according to Braun-Blanquet (1932). The occurrence (i.e., presence/absence) of soil-dwelling bryophytes was recorded in 5 randomly placed 40 × 50 cm frames (total area surveyed per plot = 1 m2). To estimate the average bryophyte biomass in the surface unit, we measured the percent cover by line intercepts (Elzinga et al., 2001) and the biomass standard area. The cover was measured along 3 line intercept transects (length = 23 m × 3) by noting the point along the tape where the cover began and the point at which it ended. The percent cover was the sum of these intercepts divided by the total length. The line transects were positioned along a triangle inset in the plot. In a random bryophyte colony along each line transect, we collected a sample of biomass using a 10 × 10 cm quadrat. Thus, the bryophyte biomass in the plot was estimated by combining the cover data (resulting from the 3 line transects) and the weight data (resulting from the biomass harvested in 3 quadrats). Preliminary surveys executed in spruce forests (Spitale, unpublished) using transects of different lengths and quadrats of different size, showed that, for the same number of replicates, the results were similar using a larger plot size (50 × 50 cm). In the laboratory, we sorted out all the extraneous materials other than bryophytes using a dissecting microscope. The samples were weighed after drying at 40 °C for 12 h. The bryophyte biomass on the forest floor was expressed as Kg/ha. In each plot, on five larch individuals, the epiphytic bryophytes and lichens were recorded using four standard 10 × 50 cm frames as sampling grids, subdivided into five 10 × 10 cm quadrats (Asta et al.,

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Table 1 Main features of the plots belonging to the three management types of Alpine larch grasslands (mean ± SD). The results of ANOVA and the Tukey HSD test for pair-wise comparisons are reported in the last two lines. ab = abandoned, ex = extensive, in = intensive; ns = non-significant. Management type

Elevation (m)

Aspect (°)

Slope (°)

Tree density (trees/ha)

Soil pH

Soil C/N ratio

Intensive (n = 7) Extensive (n = 7) Abandoned (n = 7) ANOVA Tukey HSD

1651 ± 117 1768 ± 128 1785 ± 55 F = 3.39

161 ± 35 199 ± 24 195 ± 26 F = 3.74⁎ ns

7.6 ± 1.9 13.3 ± 4.0 13.6 ± 4.1 F = 6.54⁎⁎ ab = ex N in

141 ± 40 141 ± 51 628 ± 291 F = 18.7⁎⁎⁎ ab N ex = in

5.94 ± 1.04 5.23 ± 1.24 5.25 ± 1.36 F = 0.77

13.4 ± 2.3 16.5 ± 2.3 18.1 ± 3.1 F = 6.02⁎⁎ ab N in

⁎ Significance level at P b 0.05. ⁎⁎ Significance level at P b 0.01. ⁎⁎⁎ Significance level at P b 0.001.

2002), which were attached to tree trunks at the North and South cardinal points (Nascimbene et al., 2010), both at 100 cm from the ground and at the base of the trunk. In each plot, we surveyed a total area of 1 m2 (5 trees, 4 frames per tree), the same surface area used for the soil bryophytes. All bryophyte and lichen species inside the frames were listed, and their frequency was computed as the number of 10 × 10 cm quadrats in which the species occurred. Because tree age and size, which are usually intercorrelated, may affect epiphyte diversity (Nascimbene et al., 2009), we kept the tree circumference comparable among the plots (mean = 175 cm ± 26 SD). 2.4. Species identification and nomenclature Most of the vascular plant species were identified in the field, while most of the bryophyte and lichen specimens were collected for detailed morphological analyses. For the lichens, routine chemical spot tests were performed for most specimens, while the identification of sterile crustose lichens (including all Lepraria species; c. 150 specimens) was based on standardized thin-layer chromatography (TLC) analyses following the protocols of White and James (1985) and Orange et al. (2001). Vascular plant nomenclature follows Wilhalm et al. (2006), moss nomenclature follows Hill et al. (2006), liverwort nomenclature follows Ros et al. (2007), and lichen nomenclature follows Nimis and Martellos (2008). 2.5. Data analyses To test the effect of management type on the species richness (cumulative number of species per plot) of each of the three groups of organisms, we used GLM with and without covariates. Because the sampling sites were located on different lithologies (calcareous and metamorphic bedrocks), for the vascular plants and soil bryophytes we performed partial linear regression to estimate how much of the variation of the response variable could be attributed exclusively to the management type once the effect of bedrocks had been taken into account (Legendre and Legendre, 1998). For the epiphytic bryophytes and lichens, the effect of management was tested with one-way ANOVA. Compositional differences among the management types were tested by permutational multivariate analysis of variance. This analysis partitions the dissimilarity matrix for the sources of variation and uses permutation tests with pseudo-F ratios to inspect statistical significance. Because the sampling sites were located on different lithologies, for the vascular plants and soil bryophytes, we performed the analysis of variance with the substrate as a covariate to partition out its effect (Legendre and Legendre, 1998). The patterns of species composition were also visually evaluated using non-metric multi-dimensional scaling (NMDS; McCune and Grace, 2002), which is commonly regarded as the most robust unconstrained ordination method in community ecology (Minchin, 1987). NMDS and permutational multivariate analysis of variance were computed using Bray–Curtis dissimilarity matrices.

Indicator Species Analysis (ISA; Dufrêne and Legendre, 1997) was used to determine how strongly each species was associated with each management type. For each species, the Indicator Value (INDVAL) ranged from 0 (no indication) to 1 (maximum indication). This index combines the mean abundance of a species and its frequency of occurrence in a cluster. A high indicator value was obtained when a given species had both a high mean abundance in one group compared to that in the other groups (specificity) and occurred in most plots of that group (fidelity). The statistical significance of the indicator values was tested by means of a permutation test. All the analyses were performed in R (R Development Core Team, 2013) with the packages labdsv and vegan. 3. Results Two-hundred-seventeen species of vascular plants, 58 species of bryophytes and 83 species of lichens were found (see Appendix B in Supplementary data). Once the bedrocks effect was partitioned out, the plant richness was lower in the abandoned (mean = 25 ± 7.2 SD, F = 12.301; P = 0.005, Fig 1) than in the currently managed stands, while it did not differ between the extensively and intensively managed stands (41 ± 9.1 SD and 42 ± 3.4 SD, respectively). The soil bryophyte richness differed among the management types once the bedrock effect was removed (F = 4.671, P = 0.025). However, the effect size was narrow, and a Tukey post-hoc comparison of the main effect failed to reveal significant differences among the management types. The epiphytic bryophyte richness did not differ among the management types, while the bryophyte biomass on the soil increased from the intensively managed (26.0 ± 34 SD Kg/ha) to the abandoned (78.1 ± 57 SD Kg/ha) and extensively managed stands (287.8 ± 243 SD Kg/ha, Fig 2). The lichen species richness was higher in the extensively managed stands (33 ± 4.2 SD species, F = 11.0, P b 0.001, Fig 1), while it did not differ between the abandoned and intensively managed stands (23 ± 4.6 SD and 23 ± 5.2 SD, respectively). The species assemblages of the three taxonomic groups were significantly different among the management types (Table 2 and Fig 3). However, the vascular plant and soil bryophyte assemblages in the abandoned and extensively managed stands displayed broad overlap. The same response was found for the epiphytic bryophyte assemblages, which broadly overlapped among the three management types. This result takes into account the different lithologies of the plots, as we performed the analysis of variance by keeping the substrate as a covariate to partition out its effect. The most relevant differences in species composition were found for the epiphytic lichens (Table 2 and Fig 3), whose assemblages highly differed among the management types. Several vascular plants (19 species) and lichens (22 species) were significantly associated with one management type (Table 3). In particular, 8 plants were associated with extensively managed stands, including 7 species related to infertile soils; 10 were associated with intensively managed stands, including 6 species related to fertile soils; and one plant species was associated with abandoned larch grasslands. Three nitrogen-tolerant lichens were associated with the intensively

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Fig. 1. Boxplot for the species richness of the soil bryophytes, vascular plants, epiphytic bryophytes and lichens. Differences among the management types were tested by ANOVA and Tukey's post-hoc procedure (different letters are placed between significant differences).

managed stands; 18 were associated with the extensively managed stands, mainly including nitrogen-intolerant acidophytic species preferring well-lit conditions; and one was associated with the abandoned stands. Only one bryophyte was overrepresented in the abandoned stands.

4. Discussion 4.1. General overview Our study reveals that in Alpine larch grasslands, different management types strongly affect the biodiversity of bryophytes, vascular plants, and lichens. However, some contrasting patterns were found among the organism groups, corroborating the hypothesis that the response to management intensity may differ among organisms with different traits and ecological requirements (Poschlod et al., 2005; Löbel et al., 2006). This result also supports the view that typically overlooked organisms, such as cryptogams, should be included in evaluations of the effects of intensification and abandonment on

biodiversity in wooded grasslands. While these organisms are likely to greatly contribute to wooded grassland biodiversity (e.g., Nascimbene et al., 2006), even for species of conservation concern, their diversity patterns in relation to management intensity have thus far been overlooked in agricultural Alpine landscapes. Although our sampling was designed to keep the topographic variables comparable among the management types, the slope was significantly higher in the abandoned and extensively managed stands than in the intensively managed stands, reflecting the fact that intensive stands are those that are more suitable for mechanized agriculture. However, we are confident that this difference is not likely to affect our results due to the small length of the gradient, including sites with moderate slopes, for all the stand types.

4.2. Responses of the organism groups As expected, the epiphytic lichens were the most sensitive organisms, with a diversity pattern that was predicted by the intermediate disturbance hypothesis. Their richest communities developed in the extensively managed stands, where the species assemblages were comparable to those of natural, subalpine, larch-dominated forests, being composed of certain nitrogen-sensitive (e.g., Letharia vulpina; Nascimbene et al., 2008) and red-listed species (e.g., Tuckneraria

Table 2 Multivariate analysis of variance using Bray–Curtis dissimilarity matrices on species assemblages. The factor was the management type used in the Alpine larch grasslands. ab = abandoned, ex = extensive, in = intensive.

Soil bryo Epi bryo Vascular Fig. 2. Box plot for soil bryophyte biomass. Differences among the management types were tested by ANOVA and Tukey's post-hoc procedure (different letters are placed between significant differences).

Lichens

Factor Residual Factor Residual Factor Residual Factor Residual

Df

MS

F

Pr (NF)

ab vs ex

ab vs in

es vs in

2 17 2 18 2 17 2 18

2.224 12.366 0.285 0.224 22.907 62.872 0.584 0.102

1.529

0.045

0.570

0.010

0.250

1.272 0.876 3.097

0.227

–

–

–

0.005

0.005

0.005

0.005

5.739 0.611

0.000

0.005

0.005

0.005

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Fig. 3. Ordination plots for the soil bryophytes, vascular plants, epiphytic bryophytes and lichens according to the results of non-metric multidimensional scaling. In = intensively managed stands, ex = extensively managed stands, ab = abandoned stands.

laureri; Nascimbene et al., 2013c). Compositional shifts were found for both the abandoned and intensively managed stands. However, they were likely driven by contrasting processes. Compared to the extensively managed stands, the assemblages of the abandoned stands lacked the most shade-intolerant species, indicating that canopy closure is the main process responsible for species loss and compositional shifts (Nascimbene et al., 2013b; Paltto et al., 2011). The marked difference in species assemblages also suggests that the shift between the two communities could be relatively fast after abandonment. In the intensively managed stands, nitrogen enrichment is the main process driving lichen diversity patterns, resulting in communities mainly composed of nitrogen-tolerant species. This hypothesis was also corroborated by ISA analysis, with three nitrogen-tolerant species being overrepresented in this management type. Epiphytic lichens are notoriously sensitive to eutrophication, which is among the main sources of diversity loss across different ecosystems (Giordani et al., 2014). According to Johansson et al. (2011, 2012), the compositional shift from extensively to intensively managed stands is likely related to differential species responses to nitrogen input. The responses of the vascular plants depended on contrasting patterns between species richness and composition. Abandonment negatively affected plant richness, while management intensification caused major compositional shifts. The assemblages of the abandoned and extensively managed stands displayed broad overlap, indicating that species loss may determine minor compositional differences in the first decades after abandonment. This situation, which was common to both the plants and soil-dwelling bryophytes, indicates

the possibility of recuperating species-rich communities through the restoration of abandoned habitats within a time span of a few decades. Species turnover likely determined the main compositional differences between the extensively and intensively managed stands, which did not differ in species richness. As for lichens, nitrogen enrichment is the main process associated with management intensification that influences assemblage composition (Marini et al., 2011). This view is corroborated by ISA results indicating that several nitrogen-tolerant species, such as Anthriscus sylvestris and Taraxacum officinale, are overrepresented in intensively managed stands, while plants of nutrient poor soils, such as Arnica montana and Gentiana acaulis, are overrepresented in extensively managed stands. Bryophytes were the least species rich group, whose most detectable response to management intensity was in terms of biomass shifts, with the highest values in the extensively managed stands. In the intensively managed stands, the nitrogen supply stimulated the growth of tall grasses, causing the exclusion of bryophytes (both in terms of species richness and biomass; van der Wal et al., 2005; Müller et al., 2012) due to strong light competition. Under the extensive management regimes, large pleurocarpous mosses, such as Rhytidium rugosum and Pleurozium schreberi, were allowed to establish, indicating that light was not a limiting factor. However, large pleurocarpous mosses may in turn limit the establishment of smaller species, making the species richness similar to that observed in the intensively managed stands. In the abandoned stands, light was again a limiting factor due to increased tree density, which hindered bryophyte biomass growth.

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Table 3 List of the species that were overrepresented (indicator species; Dufrêne and Legendre, 1997) in one of the different management types. The indicator species for each management type are listed in alphabetical order. IndVal = Indicator Value; in = intensively managed stands, ex = extensively managed stands, ab = abandoned stands; P = significance level; Records = number of plots in which the species was found. IndVal

Epiphytic bryophytes Vascular plants

Lichens

Lophocolea heterophylla Alchemilla vulgaris agg. Anthriscus sylvestris Leucanthemum vulgare agg. Poa alpina Ranunculus acris Silene dioica Taraxacum officinale agg. Trifolium pratense Trifolium repens Trisetum flavescens Arnica montana Gentiana acaulis Helianthemum nummularium s. lat. Persicaria vivipara Ranunculus montanus agg. Sesleria albicans Thesium alpinum Trifolium montanum Cirsium acaule Amandinea punctata Melanohalea exasperatula Xanthoria candelaria Bryoria subcana Cladonia digitata Cyphelium tigillare Evernia mesomorpha Hypocenomyce scalaris Hypogymnia bitteri Imshaugia aleurites Letharia vulpina Parmelia saxatilis Parmeliopsis hyperopta Pseudevernia furfuracea v. ceratea Trapeliopsis flexuosa Tuckermannopsis chlorophylla Tuckneraria laureri Usnea barbata Usnea hirta Usnea subfloridana Vulpicida pinastri Chaenotheca chrysocephala

Relative abundance

in

ex

ab

in

ex

ab

0.066 0.490 0.714 0.600 0.762 0.655 0.584 0.584 0.560 0.714 0.714 0.000 0.000 0.000 0.071 0.022 0.010 0.018 0.000 0.018 0.758 0.623 0.935 0.099 0.114 0.067 0.089 0.168 0.042 0.106 0.000 0.000 0.077 0.206 0.133 0.042 0.004 0.024 0.135 0.023 0.090 0.000

0.082 0.163 0.000 0.171 0.016 0.000 0.013 0.052 0.286 0.054 0.000 0.684 0.714 0.500 0.589 0.549 0.571 0.625 0.491 0.000 0.000 0.005 0.026 0.654 0.520 0.605 0.552 0.456 0.741 0.532 1.000 0.673 0.558 0.475 0.655 0.778 0.649 0.595 0.446 0.496 0.457 0.241

0.467 0.041 0.000 0.014 0.000 0.067 0.013 0.000 0.006 0.014 0.000 0.135 0.000 0.018 0.009 0.011 0.019 0.000 0.134 0.500 0.009 0.022 0.026 0.066 0.240 0.008 0.138 0.265 0.048 0.228 0.000 0.061 0.264 0.203 0.005 0.011 0.232 0.000 0.365 0.113 0.386 0.496

0.154 0.571 1.000 0.600 0.889 0.765 0.818 0.818 0.560 0.714 1.000 0.000 0.000 0.000 0.250 0.154 0.067 0.125 0.000 0.125 0.935 0.885 0.727 0.231 0.200 0.235 0.207 0.235 0.148 0.149 0.000 0.000 0.135 0.288 0.310 0.148 0.027 0.167 0.189 0.158 0.157 0.000

0.192 0.286 0.000 0.300 0.111 0.000 0.091 0.182 0.400 0.190 0.000 0.684 1.000 0.875 0.688 0.769 0.800 0.875 0.688 0.000 0.000 0.038 0.091 0.654 0.520 0.706 0.552 0.456 0.741 0.532 1.000 0.786 0.558 0.475 0.655 0.778 0.649 0.833 0.446 0.579 0.457 0.421

0.654 0.143 0.000 0.100 0.000 0.235 0.091 0.000 0.040 0.095 0.000 0.316 0.000 0.125 0.063 0.077 0.133 0.000 0.313 0.875 0.065 0.077 0.182 0.115 0.280 0.059 0.241 0.309 0.111 0.319 0.000 0.214 0.308 0.237 0.034 0.074 0.324 0.000 0.365 0.263 0.386 0.579

5. Conclusions Management intensity was demonstrated to strongly influence the biodiversity of plants and cryptogams in Alpine larch grasslands, with a general pattern indicating that the best conditions existed in the extensively managed stands. Both abandonment and management intensification were detrimental to biodiversity through different mechanisms, which led to species loss or to major shifts in species composition. Our study provides evidence of the detrimental effects of the abandonment of traditional Alpine agriculture (MacDonald et al., 2000; Marini et al., 2011) and also highlights that restoration actions may depend on the type of organism considered. However, the most negative effects on biodiversity were found to be related to management intensification, mainly due to increased nitrogen supply, demonstrating the increasing impact of eutrophication in Alpine environments (Tasser and Tappeiner, 2002). From this perspective, the long-term maintenance of traditionally managed larch grasslands should be fully addressed as a measure for biodiversity conservation in Alpine environments, especially in protected areas and Natura 2000 sites, where conservation should receive a high priority.

P

Records

0.053 0.040 0.004 0.014 0.001 0.010 0.009 0.008 0.014 0.002 0.004 0.008 0.002 0.037 0.015 0.021 0.015 0.014 0.045 0.036 0.001 0.002 0.009 0.001 0.006 0.006 0.029 0.037 0.002 0.016 0.001 0.003 0.004 0.049 0.004 0.002 0.002 0.011 0.009 0.04 0.027 0.044

11 12 5 12 7 8 7 7 13 10 5 10 5 5 9 7 7 6 8 5 8 9 9 14 17 9 14 18 12 17 7 8 17 18 11 10 13 6 19 10 18 10

Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.scitotenv.2014.04.013. Conflict of interest We have no conflict of interest. Acknowledgments JN contributed in the framework of the project “Biodiversità, biomonitoraggio e conservazione dei licheni epifiti negli ambienti forestali della provincia di Bolzano,” funded by the Autonomous Province of Bolzano (Ripartizione Diritto allo studio, Università e Ricerca scientifica). VF contributed in the framework of the project “EcoRAlps,” supported by the Stemmler and Immerschitt Foundation within the Stifterverband für die Deutsche Wissenschaft, the Foundation of the Free University of Bozen-Bolzano and the Foundation of the University of Innsbruck. DS wishes to thank the Autonomous Province of Bolzano (Ripartizione Diritto allo studio, Università e Ricerca scientifica) for funding the project “Integrity assessment of South Tyrol forests by means of bryophytes distribution analysis.”

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