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Do vineyards in contrasting landscapes contribute to conserve plant species of dry calcareous grasslands?
Science of the Total Environment 545–546 (2016) 244–249
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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Do vineyards in contrasting landscapes contribute to conserve plant species of dry calcareous grasslands? Juri Nascimbene a,b,⁎, Michela Zottini c, Diego Ivan c, Valentina Casagrande a, Lorenzo Marini a a b c
Department of Agronomy, Food, Natural Resources, Animals and the Environment (DAFNAE), University of Padova, viale dell'Università 16, 35020 Legnaro, Padova, Italy Department of Life Sciences, University of Trieste, via Giorgieri 10, 34100 Trieste, Italy Department of Biology, University of Padova, via U. Bassi 58/B, I-35121 Padova, Italy
H I G H L I G H T S
G R A P H I C A L
A B S T R A C T
• The development of vineyards is a major driver of conversion of dry grasslands. • We test the potential of vineyards in contrasting landscapes for plant conservation. • Semi-natural habitats in the landscape positively affect plant diversity of vineyards. • Vineyards provide moderate chance for the conservation of plant of dry grasslands. • Remnants of dry grasslands are refugia for species of conservation concern.
a r t i c l e
i n f o
Article history: Received 3 September 2015 Received in revised form 11 December 2015 Accepted 11 December 2015 Available online xxxx Editor: J. P. Bennett Keywords: Crop landscape Plant conservation Ruderal species Semi-natural landscape Specialist species Species richness and composition
a b s t r a c t The increasing development of vineyards in Mediterranean areas worldwide is considered a major driver of conversion of several habitats of conservation concern, including calcareous dry grasslands that are targeted for biodiversity conservation by the European Union, according to Natura 2000 policies. Here, we aim at evaluating the potential of extensive vineyards located in contrasting landscapes (semi-natural vs crop-dominated) for providing suitable habitat conditions to plant species associated with dry grasslands. This study was carried out in one of the economically most important winemaking districts of Italy, characterized by a hilly landscape with steep slope vineyards. We compared plant communities of vineyards in contrasting landscapes with those of the remnants of dry grasslands. Our study demonstrates that landscape composition strongly affects local plant communities in vineyards, with a positive effect of semi-natural habitats bordering the cultivated areas. Our findings thus supply an additional tool for improving the effectiveness of viticultural landscapes for nature conservation. In particular, our results indicate that vineyards on steep slopes could provide moderate chance for the conservation of plant specialists inhabiting calcareous dry grasslands, depending on the landscape composition: vineyards embedded in semi-natural landscapes have more potential for conservation than those in crop-dominated landscapes. Our study also indicates that conservation efforts should aim at (a) decreasing the current management intensity that likely hampers the beneficial effects of semi-natural habitats in the surrounding
⁎ Corresponding author at: Department of Agronomy, Food, Natural Resources, Animals and the Environment (DAFNAE), University of Padova, viale dell'Università 16, 35020 Legnaro, Padova, Italy. E-mail address: [email protected] (J. Nascimbene).
http://dx.doi.org/10.1016/j.scitotenv.2015.12.051 0048-9697/© 2015 Elsevier B.V. All rights reserved.
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landscape on local plant assemblages, and (b) strictly conserving the remnants of dry grasslands that are irreplaceable refugia for habitat specialists and species of conservation concern. © 2015 Elsevier B.V. All rights reserved.
1. Introduction Biodiversity conservation is increasingly recognized as a crucial task for sustaining several ecosystem services that improve human wellbeing (Cardinale et al., 2012). Agriculture is among the main causes of biodiversity loss worldwide (Frishkoff et al., 2014; Karp et al., 2012; Pignatti, 1982) and there is increasing awareness that future biodiversity conservation will largely depend on the capability of cultivated areas to provide suitable habitats for species and communities of conservation concern (Baudron and Giller, 2014; Green et al., 2005; Phalan et al., 2011; Wright et al., 2012). The increasing development of vineyards in Mediterranean areas worldwide is considered a major driver of conversion of several habitats of conservation concern (e.g. Richter, 1989; Rühl, 2004; Viers et al., 2013), including calcareous dry grasslands that are targeted for biodiversity conservation by the European Union, according to Natura 2000 policies (European Commission, 2007). Habitat conversion results in simplified landscapes where this semi-natural vegetation is restricted to small scattered patches. However, recent research also highlighted that coupling biodiversity conservation with wine production could be a winning strategy both for marketing purposes and for counteracting the negative effects of global change (Bellosi et al., 2013; Hannah et al., 2013; Trivellone et al., 2014; Viers et al., 2013). This view is also reflected by the inclusion of several viticultural landscapes world-wide in the UNESCO world heritage list (http://whc.unesco.org/en/list/). Besides local management intensity, that is among the main drivers of local plant diversity in vineyards (Brugisser et al., 2010; Nascimbene et al., 2012, 2013; Poldini et al., 1998), the potential of vineyards to contribute to the conservation of dry grasslands is likely to be related to landscape composition (Weibull et al., 2003). In general, landscape composition influences local biodiversity of agro-ecosystems, with a positive effect of semi-natural habitats on various components of the
biota (e.g. Tscharntke et al., 2005, 2012b). This rationale would predict that richer plant communities should be expected in vineyards bordered by semi-natural habitats than in vineyards embedded in a landscape dominated by cultivated areas. While this hypothesis has been already tested in vineyard regions for several faunistic groups (e.g. Brittain et al., 2010; Hilty and Merenlender, 2004; Laiolo, 2005; Schmitt et al., 2008), it is still awaiting experimental evidence for plant communities. Here, we aim at evaluating the potential of extensive vineyards located in contrasting landscapes (semi-natural vs cropdominated) for providing suitable habitat conditions to plant species associated with dry grasslands. This study was carried out in one of the economically most important winemaking districts of Italy, characterized by a hilly landscape with steep slope vineyards. In this region, dry grasslands are severely declining due to agriculture intensification, being replaced by vineyards even on the steepest slopes. We compared plant communities of vineyards in contrasting landscapes with those of the remnants of dry grasslands. Besides considering the full species pool, we contrasted among different a-priori selected groups of species indicative of different local conditions (e.g., dry grassland specialists vs ruderal species) and of conservation concern (e.g., red-listed species and orchids). The patterns of these selected groups of species is expected to better help to elucidate the potential of vineyards to provide surrogate habitat for the conservation of plant communities of dry grasslands. On the one hand, we hypothesise that vineyards in semi-natural landscapes could host species assemblages more similar to those of dry grasslands as compared with vineyards in crop-dominated landscapes, especially when specialist species are considered. On the other hand, the vineyards in contrasting landscapes are expected to host similar assemblages of ruderal species, reflecting comparable management intensity, independently of landscape composition.
Fig. 1. Map of the study area, corresponding with the Conegliano-Valdobbiadene DOCG. Dry grasslands, vineyards in crop and in semi-natural landscapes are marked with different labels. Grey areas indicate the vineyards.
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Table 1 Main features (site conditions, management, % of semi-natural habitats in the landscape) of the three types of sites that were compared in this study. SMH = semi-natural habitats. Different letters indicate significant differences (P b 0.05).
Slope (°) Southness(°) Elevation (m) N mowing year−1 N herbicide year−1 N tot treatments year−1 kg N ha−1year−1 SMH 50 m (%) SMH 100 m (%) SMH 250 m (%) SMH 500 m (%)
Vineyards in Vineyards in crop landscapes semi-natural landscapes
Remnants of dry grasslands
38 ± 8a 33 ± 31a 280 ± 66a 3.1 ± 0.3a 0.8 ± 0.6a 9.7 ± 1.4a 19 ± 15a 2 ± 5a 6 ± 6a 22 ± 9a 34 ± 13a
42 ± 9a 41 ± 28a 302 ± 83a – – – – 78 ± 24c 75 ± 23b 72 ± 22b 68 ± 21b
39 ± 7a 39 ± 29a 318 ± 78a 3.1 ± 0.4a 0.8 ± 0.7a 9.6 ± 1.7a 22 ± 20a 52 ± 16b 65 ± 12b 66 ± 19b 59 ± 19b
2. Material and methods 2.1. Study area The study was carried out in the region of the ConeglianoValdobbiadene DOCG, one of the most important areas of north Italy for wine production (the worldwide famous Prosecco), including 6100 ha of vineyards in the northern part of the province of Treviso (Fig. 1; Veneto, NE Italy, N 45°52′40″, E 12°17′5″). This area is characterized by a hilly landscape where elevation ranges between 70 and 450 m, annual precipitation is between 900 and 1000 mm and mean annual temperature is 11 °C. In this hilly landscape vineyards occupy even the steep (N45°), mainly south facing, slopes where the cultivated area is composed by small vineyards, usually between 1 and 2 ha, belonging to several owners. This fragmented arrangement of the ownerships implies that local management practises may vary between adjacent vineyards. However, the severe topographic conditions are a deterrent for intensive, mechanized management. Mowing frequency is usually three times per year, without grass raking, while the use of herbicides may range between 0 and 2 treatments per year. Nitrogen supply is in general very low (0–100 kg ha−1). The wine produced in steep slope vineyards, locally defined by the traditional term “Rive”, is particularly valuable. For this reason, spurred by a growing market demand, the cultivation of steep slopes has drastically increased in the last decades, resulting in a simplification of the landscape matrix. The main impacted habitats, in terms of habitat loss and fragmentation, are dry grasslands that are addressed by the EU among the habitats of conservation concern, according with Natura 2000 policies. Approximately 90% of dry grasslands have been lost in last 40 years, with an acceleration in the last 10 years. In particular, we refer to dry grasslands that are classified under the Natura 2000 codes 6210, semi-natural dry grasslands and scrubland facies on calcareous substrates (Festuco-Brometalia), and 62A0, eastern sub-Mediterranean dry grasslands (Scorzoneretalia village). The former is considered a priority habitat when several orchid species are present. In the study area, these dry grasslands are restricted to very small, scattered, patches usually forming a buffer zone between forests and vineyards. Both natural (unmanaged) and semi-natural
(extensively managed) arid grasslands can be found, hosting highly diverse plant communities, often rich in rare orchid species. 2.2. Sampling design and plant identification Forty vineyards on steep slopes and 20 remnants of dry grasslands were selected for this study (Fig. 1). Vineyards were selected to represent two contrasting landscapes: 20 in landscapes dominated by cultivated areas (crop landscape; b30% of semi-natural habitats), and 20 in landscapes with a high percentage (N40%) of semi-natural habitats (semi-natural landscape), including both forests and dry grasslands. Landscape composition was assessed within a circular buffer of 250 m radius and differences between the two groups of vineyards were also tested (t-test) at smaller (i.e., 50 m and 100 m radius) and larger (500 m radius) spatial scales. Vineyards in both landscapes were selected to have similar exposure, elevation, surface, spontaneous vegetation, and farmers did not sow any seed mix for at least 10 years. Also management intensity did not differ between the vineyards located in the two landscapes: in both cases vineyards were mainly mown three times per year, while herbicides were applied 0–2 times per year (Table 1). Grasslands and vineyards located in contrasting landscapes were spatially interspersed in the study area. In each vineyard and dry grassland, the occurrence (presence-absence sampling) of all the vascular plants was recorded inside a 25 × 5 m plot placed in the center of the sampling site with the longer side disposed along the line of maximum slope. The survey was carried out between April 10 and May 15, 2014, before the first mowing. When possible, plants were identified in the field. However, in several cases species identification was based on the study of specimens (c. 1200) collected and stored in the personal herbarium of the authors. Especially specimens in the families of Poaceae and Cyperaceae were identified in the laboratory using a dissecting microscope. Critical specimens were submitted to a specialist for identification/confirmation. Material lacking fundamental diagnostic characters was identified at the genus level. Nomenclature follows Conti et al. (2005). 2.3. Statistical analysis Differences in species richness among vineyards in crop and seminatural landscapes and dry grasslands were tested by one-way analysis of variance (ANOVA). After the ANOVA, a Tukey's honest significance test for multiple comparison was applied to detect differences between the three types of sites (P b 0.05). Differences were tested on the total number of species per site, as well as on four a-priori defined subsets of species including: (a) species of conservation concern listed in the regional Red List (Buffa et al., in press). In this group we included species whose conservation status was scored under different IUCN categories (IUCN, 2001), including endangered, vulnerable, near threat, and least concern species; (b) orchids, whose presence is used to define the status of priority habitat of dry grasslands according to Natura 2000 policies (European Commission, 2007); (c) dry grassland specialists, and (d) ruderal species. Species of the last two categories were selected on the basis of available literature specific for Italy (Baldoni et al., 2001; Pignatti, 1982; Poldini et al., 1998). Compositional differences among vineyards in contrasting landscapes and dry grasslands were evaluated using a sites × species matrix
Table 2 Comparison of species richness and richness of groups of selected species among the three types of sites. Different letters indicate significant differences (P b 0.05).
Species richness (N of species) N of red listed species N of orchids N of specialists of dry grasslands N of ruderal species
Vineyards in crop landscapes
Vineyards in semi-natural landscapes
Remnants of dry grasslands
43 ± 8a 0.6 ± 0.8 0 4.3 ± 2.5a 20.7 ± 3.1a
69.9 ± 14b 1.7 ± 1.2 0.1 ± 0a 14.5 ± 8.4b 23.9 ± 6.3a
58 ± 10c 3.9 ± 2.3 2.2 ± 1.4b 34.2 ± 10.7c 3.8 ± 4.2b
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Table 3 Results of the multi-response permutation procedures (MRPP) that were used to test compositional differences among vineyards in contrasting landscapes and remnants of dry grasslands. This analysis was applied to the matrix including the full pool of species as well as to the two reduced matrices including only specialists of dry grasslands or ruderal species. P values of pairwise comparisons were adjusted with a Bonferroni correction. VCL = vineyards in crop landscapes; VSMHL = vineyards in semi-natural landscapes; DG = dry grasslands.
Total VCL vs VSMHL VCL vs DG VSMHL vs DG
All the species
Specialists of dry grasslands
Ruderal species
A = 0.41, P b 0.00001 A = 0.18, P b 0.00001 A = 0.44, P b 0.00001 A = 0.34, P b 0.00001
A = 0.20, P b 0.00001 A = 0.044, P = 0.0016 A = 0.22, P = 0.0002 A = 0.16, P = 0.0004
A = 0.21, P b 0.00001 A = 0.012, P = 0.12 A = 0.34, P b 0.00001 A = 0.17, P = 0.00005
including all the species and also using two reduced matrices that included only specialists of dry grasslands and ruderal species, respectively. Differences in species composition were tested by multi response permutation procedures (MRPP) as implemented in PC-ORD (McCune and Mefford, 1999), using the Sørensen distance measure and rank transformation of the distance matrices. MRPP was used to test differences between the three types of habitat (i.e. vineyards in contrasting landscapes and dry grasslands) as well as for the total, i.e. all the habitat types pooled together. We applied a Bonferroni correction to the pairwise P-values to avoid type I error, accounting for the number of pairwise comparisons. The test statistic “A” in MRPP describes the separation between stand types. The pattern of species composition was also visually evaluated using non-metric multidimensional scaling (NMDS; McCune and Grace, 2002) as implemented in PC-ORD
(McCune and Mefford, 1999), using the “slow and thorough” autopilot mode with the Sørensen distance measure. This procedure performed 40 runs with real dataset compared with 50 randomized runs, each run with 400 iterations. This iterative ordination method is based on ranked distances between sample units in the data matrix, known as “species space” (McCune and Grace, 2002); it does not assume normally distributed data and is therefore suited for most ecological data. A final 2-dimensions solution was selected for the matrices with all species and specialists of dry grasslands (stress 14% and 11%, instability 0.007 and 0.00008 respectively), while a final 3-dimensions solution was selected for ruderal species (stress 17%, instability 0.00014). 3. Results 3.1. Species richness In total, 368 species were found (Supplementary material A), 162 in vineyards in crop landscapes, 283 in vineyards in semi-natural landscapes, and 257 in dry grasslands. Red listed and orchid species were respectively 11 and 12, all recorded in dry grasslands. Only 2 red listed species were found in both types of vineyards, and 2 orchids in
Fig. 2. Ordination diagram of sampling sites in the species space based on non-metric multidimensional scaling (NMDS) performed with all the species. Different symbols indicate different types of sites: filled squares = dry grasslands, empty circles = vineyards embedded in landscapes with a high percentage of semi-natural habitats (semi-natural landscape), filled circles = vineyards embedded in landscapes dominated by cultivated areas (crop landscape). Total variation in species composition explained by the two axes was 96% (48% axis 1 and 48% axis 2).
Fig. 3. Ordination diagram of sampling sites in the species space based on non-metric multidimensional scaling (NMDS) performed with the subset of species that are specialists of dry grasslands. Different symbols indicate different types of sites: filled squares = dry calcareous grasslands, empty circles = vineyards embedded in landscapes with a high percentage of semi-natural habitats (semi-natural landscape), filled circles = vineyards embedded in landscapes dominated by cultivated areas (crop landscape). Total variation in species composition explained by the two axes was 81.6% (46.1% axis 1 and 35.5% axis 2).
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vineyards located in semi-natural landscapes. In total, 114 specialists of dry grasslands were found, 24 in vineyards in crop landscapes, 72 in vineyards in semi-natural landscapes, and 99 in dry grasslands. Eighty-six ruderal species were found: 66 in vineyards in crop landscapes, 80 in vineyards in semi-natural landscapes, and 30 in dry grasslands. The mean species richness was significantly (P b 0.05) higher in vineyards in semi-natural landscapes than in both vineyards in crop landscapes and dry grasslands (Table 2). The mean number of species of conservation concern (red listed species and orchids) was higher in dry grasslands than in vineyards in both landscape types (Table 2). Dry grasslands hosted the highest number of specialist species, vineyards in semi-natural landscape had an intermediate value that was however significantly higher than that of vineyards in crop landscapes. Vineyards in both landscapes hosted a similar number of ruderal species, while dry grasslands hosted a significantly lower number of these species. 3.2. Species composition The three types of sites significantly differed in species composition, as indicated by the MRPP test (Table 3). However, pairwise comparisons also indicated that communities of vineyards in semi-natural landscapes are more similar to those of dry grasslands as compared to vineyards in crop landscapes (lower “A” statistic values). This result is corroborated by the visual interpretation of the NMDS ordination
Fig. 4. Ordination diagram of sampling sites in the species space based on non-metric multidimensional scaling (NMDS) performed with the subset of ruderal species. Different symbols indicate different types of sites: filled squares = dry calcareous grasslands, empty circles = vineyards embedded in landscapes with a high percentage of semi-natural habitats (semi-natural landscapes), filled circles = vineyards embedded in landscapes dominated by cultivated areas (crop landscapes). Total variation in species composition explained by the three axes was 74.1% (25% axis 1, 12.7% axis 2, and 36.4% axis 3). The figure is based on the two most important axes.
(Fig.2), whose two axes account for 96% of the total variation in species composition (each axis 48%). In this ordination, sites belonging to different site types are plotted in the species space. Vineyards in semi-natural landscapes were plotted at an intermediate position between vineyards in crop landscapes and dry grasslands. Differences in species composition were evident also considering the two groups of specialist and ruderal species separately (Table 3). However, this analysis revealed that vineyards in contrasting landscapes were more similar to each other than considering the full pool of species. In particular, they had the same composition of ruderal species, and almost overlapping composition (very low value of the “A” statistic) of specialist species. The two NMDS ordinations (Fig. 3, 4), that explained 81.6% and 74.1% of the total variation in species composition respectively, corroborated these results. Considering specialist species (Fig. 3), sites belonging to vineyards in both landscapes were spatially concentrated in the species space indicating high among-sites similarity. Most of the dry grasslands were clearly separated from vineyards, while some sites were plotted close to vineyards in semi-natural landscapes. Considering ruderal species (Fig. 3), sites of dry grasslands were spatially concentrated in the species space and clearly separated from vineyards. Sites of vineyards in contrasting landscape largely overlapped in the species space. 4. Discussion Our study demonstrates that landscape composition strongly affects local plant communities in vineyards, with a positive effect of seminatural habitats bordering the cultivated areas. This positive relationship was already demonstrated for different types of crop (Marini et al., 2008; Tscharntke et al., 2012b), while experimental evidence for plant communities in viticultural landscapes was still missing. Our findings thus supply an additional tool for improving the effectiveness of viticultural landscapes for nature conservation, whose potential was addressed for a long time in the botanical literature (e.g., Richter, 1989; Sarzo, 2007). In particular, our results indicate that vineyards on steep slopes could provide moderate chance for the conservation of plant specialists inhabiting calcareous dry grasslands, depending on the landscape composition: vineyards embedded in semi-natural landscapes have more potential for conservation than those in cropdominated landscapes. However, the significant differences, in terms of both species richness and composition, between vineyards and the remnants of dry grasslands suggest that the maintenance of seminatural habitats at the landscape level should be coupled with a reduction of local management intensity (Nascimbene et al., 2013). As expected, comparisons among vineyards in contrasting landscapes and remnants of dry grassland yielded different results when the different groups of species were considered. Total species richness peaked in vineyards located in semi-natural landscapes, likely reflecting an additive effect of ruderal plants and dry grasslands specialists acquired by spill-over from the neighbouring semi-natural habitats. When considering both habitat specialists and species of conservation concern (i.e., red listed species and orchids) results revealed a gradient of decreasing habitat suitability from dry grassland remnants to vineyards in crop landscapes. Vineyards in semi-natural landscapes hosted 63% of the specialists of dry grasslands, corroborating their potential as surrogate habitat for these species. However, they were much less effective in hosting species of conservation concern that were only sporadically found in these vineyards. Considering the comparison in terms of ruderal species, we found large similarity between vineyards in contrasting landscapes, supporting the hypothesis that this component reflects the effect of management intensity, independently from the landscape. Accordingly, this component only marginally contributes to plant richness of dry grasslands. Differences in species richness were reflected by compositional differences, corroborating the view that only the dry grassland remnants hosted the target community, rich in species of conservation concern,
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addressed by the EU policies for biodiversity protection (European Commission, 2007). However, the less marked compositional differences between remnants of dry grasslands and vineyards in seminatural landscapes as compared with vineyards in crop landscapes further suggest that they have a greater potential as surrogate habitat for this target community. 5. Implications for management Awareness on the beneficial effects of biodiversity is increasing among farmers and there is increasing consensus on the fact that it is no longer possible to consider the reconciliation between agriculture and biodiversity as something superfluous (Tscharntke et al., 2012a,b). The possibility to improve the area of wildlife-friendly farming (Phalan et al., 2011; Tscharntke et al., 2012a,b) in hilly vineyard landscapes is a challenge that cannot be missed. In this perspective, our study indicates that efforts to enhance the potential of hilly vineyard landscapes for coupling biodiversity conservation and yield production should strongly focus on the maintenance and improvement of seminatural landscapes with a mixed composition of cultivated and seminatural areas adjacent to each other. However, our study also indicates that conservation efforts should aim at (a) decreasing the current management intensity that likely hampers the beneficial effects of seminatural habitats in the surrounding landscape on local plant assemblages, and (b) strictly conserving the remnants of dry grasslands that are irreplaceable refugia for habitat specialists and species of conservation concern. Other active conservation practices may be needed to favour the communities of dry calcareous grasslands within vineyards, especially when the sources of seeds are extremely scanty or very isolated. Acknowledgments This study was conducted as part of the project “ENDOFLORVIT”, funded by the Veneto Region (PSR 2007–2013Mis. 124).We are grateful to Thomas Wilhalm (Naturmuseum Südtirol) for the identification/confirmation of critical specimens and to the owners of the vineyards for kindly allowing us to work on their private land. Filippo Taglietti (Conegliano-Valdobbiadene DOCG Consortium) is thanked for his help in contacting the owners of the vineyards during the planning phase of the study. Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.scitotenv.2015.12.051. References Baldoni, M., Biondi, E., Loiotile, A., 2001. La vegetazione infestante i vigneti delle Marche. Fitosociologia 38, 63–68. Baudron, F., Giller, K.E., 2014. Agriculture and nature: trouble and strife? Biol. Conserv. 170, 232–245. Bellosi, B., Trivellone, V., Jermini, M., Moretti, M., Schoenenberger, N., 2013. Composizione floristica dei vigneti del Cantone Ticino (rvizzera). Bollettino della Società ticinese di scienze naturali 101, 55–60. Brittain, C., Bommarco, R., Vighi, M., Settele, J., Potts, S.G., 2010. Organic farming in isolated landscapes does not benefit flore-visiting insects and pollination. Biol. Conserv. 143, 1860–1867. Brugisser, O.T., Schmidt-Entling, M.H., Bacher, S., 2010. Effects of vineyards management on biodiversity at three trophic levels. Biol. Conserv. 143, 1521–1528. Buffa, G., Carpenè, B., Casarotto, N., Da Pozzo, M., Filesi, L., Lasen, C., Marcucci, R., Masin, R., Prosser, F., Tasinazzo, S., Villani, M., Zanatta, K., 2015. Lista rossa regionale delle piante vascolari. Regione Veneto (in press).
249
Cardinale, B.J., Duffy, J.E., Gonzalez, A., Hooper, D.U., Perrings, C., Venail, P., Narwani, A., Mace, G.M., Tilman, D., Wardle, D.A., Kinzig, A.P., Daily, G.C., Loreau, M., Grace, J.B., Larigauderie, A., Srivastava, D., Naeem, S., 2012. Biodiversity loss and its impact on humanity. Nature 486, 59–67. Conti, F., Abbate, G., Alessandrini, A., Blasi, C., 2005. An Annotated Checklist of the Italian Vascular Flora. Palombi, Roma. European Commission DG Environment Nature and Biodiversity, 2007. Interpretation manual of European Union habitats, EUR27. Frishkoff, L.O., Karp, D.S., M'Gonigle, L.K., Mendenhall, C.D., Zook, J., Kremen, C., Hadly, E.A., Daily, G.C., 2014. Loss of avian phylogenetic diversity in neotropical agricultural systems. Science 345, 1343–1346. Green, R.E., Cornell, S.J., Scharlemann, J.P.W., Balmform, A., 2005. Farming and fate of wild nature. Science 307, 550–555. Hannah, L., Roehrdanz, P.R., Ikegami, M., Shepard, A.V., Shaw, M.R., Tabor, G., Zhi, L., Marquet, P.A., Hijmans, R.J., 2013. Climate change, wine and conservation. Proc. Natl. Acad. Sci. U. S. A. 110, 6907–6912. Hilty, J.A., Merenlender, A.M., 2004. Use of riparian corridors and vineyards by mammalian predators in Northern California. Conserv. Biol. 18, 126–135. IUCN, 2001. IUCN Red List Categories and Criteria, Version 3.1. IUCN Species Survival Commission, IUCN, Gland and Cambridge. Karp, D.S., Rominger, A.J., Zook, J., Ranganathan, J., Ehrlich, P.R., Daily, G.C., 2012. Intensive agriculture erodes β-diversity at large scales. Ecol. Lett. 15, 963–970. Laiolo, P., 2005. Spatial and seasonal patterns of bird communities in Italian agroecosystems. Conserv. Biol. 19, 1547–1556. Marini, L., Scotton, M., Klimek, S., Pecile, A., 2008. Patterns of plant species richness in Alpine hay meadows: local vs. landscape controls. Basic Appl. Ecol. 9, 365–372. McCune, B., Grace, J.B., 2002. Analysis of Ecological Communities. MjM Software, Gleneden Beach, Oregon, US. McCune, B., Mefford, M.J., 1999. Multivariate Analysis of Ecological Data, Version 4.25. MjM Software, Gleneden Beach, Oregon, US. Nascimbene, J., Marini, L., Paoletti, M.G., 2012. Organic farming benefits local plant diversity in vineyard farms located in intensive agricultural landscapes. Environ. Manag. 49, 1054–1060. Nascimbene, J., Marini, L., Ivan, D., Zottini, M., 2013. Management intensity and topography determined plant diversity in vineyards. PLoS ONE 8 (10), e76167. http://dx.doi. org/10.1371/journal.pone.0076167. Phalan, B., Onial, M., Balmford, A., Green, R.E., 2011. Reconciling food production and biodiversity conservation: land sharing and land sparing compared. Science 333, 1289–1291. Pignatti, S., 1982. Flora d'Italia. 3 vol. Edagricole. Poldini, L., Oriolo, G., Mazzolini, G., 1998. The segetal vegetation of vineyards and crop fields in Friuli-Venezia Giulia (NE Italy). St. Geobot. 16, 5–32. Richter, M., 1989. UntersuchungenzurVegetationsentwicklung und zum Standortwandel auf mediterranen Rebbrachen. Braun-Blanquetia 4 196 pp. Rühl, J., 2004. Analisi dei processi di rinaturalizzazione nei vigneti e cappereti abbandonati del paesaggio terrazzato di Pantelleria (canale di Sicilia). Naturalista Sicil. 28, 1125–1146. Sarzo, A., 2007. Il paesaggio dell'abbandono nel circondario agreste di Senter (Valle di Terragnolo, Trentino). Ann. Mus. Civ. Rovereto 22, 110–170. Schmitt, T., Augenstein, B., Finger, A., 2008. The influence of changes in viticulture management on the butterfly (lepidoptera) diversity in a wine growing region of southwestern Germany. Eur. J. Entomol. 105, 249–255. Trivellone, V., Schoenenberger, N., Bellosi, B., Jermini, M., de Bello, F., Mitchell, E.A.D., More, M., 2014. Indicators for taxonomic and functional aspects of biodiversity in the vineyard agroecosystem of Southern Switzerland. Biol. Conserv. 170, 103–109. Tscharntke, T., Klein, A.M., Kruess, A., Steffan-Dewenter, I., Thies, C., 2005. Landscape perspectives on agricultural intensification and biodiversity – ecosystem service management. Ecol. Lett. 8, 857–874. Tscharntke, T., Clough, Y., Wanger, T.C., Jackson, L., Motzke, I., Perfecto, I., Vandermeer, J., Whitbread, A., 2012a. Global food security, biodiversity conservation and the future of agricultural intensification. Biol. Conserv. 151, 53–59. Tscharntke, T., Tylianakis, J.M., Rand, T.A., Didham, R.K., Fahrig, L., Batary, P., Bengtsson, J., Clough, Y., Crist, T.O., Dormann, C.F., Ewers, R.M., Frund, J., Holt, R.D., Holzschuh, A., Klein, A.M., Kleijn, D., Kremen, C., Landis, D.A., Laurance, W., Lindenmayer, D., Scherber, C., Sodhi, N., Steffan-Dewenter, I., Thies, C., van der Putten, W.H., Westphal, C., 2012b. Landscape moderation of biodiversity patterns and processes — eight hypotheses. Biol. Rev. 87, 661–685. Viers, J.H., Williams, J.N., Nicholas, K.A., Barbosa, O., Kotzè, I., Spence, L., Webb, L.B., Merenlender, A., Reynolds, M., 2013. Vinecology: pairing wine with nature. Conserv. Lett. 6, 287–299. Weibull, A.C., Ostman, O., Granqvist, A., 2003. Species richness in agroecosystems: the effect of landscape, habitat and farm management. Biodivers. Conserv. 12, 1335–1355. Wright, H.L., Lake, I.R., Dolman, P.M., 2012. Agriculture-a key element for conservation in the developing world. Conserv. Lett. 5, 11–19.
Contents lists available at ScienceDirect
Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Do vineyards in contrasting landscapes contribute to conserve plant species of dry calcareous grasslands? Juri Nascimbene a,b,⁎, Michela Zottini c, Diego Ivan c, Valentina Casagrande a, Lorenzo Marini a a b c
Department of Agronomy, Food, Natural Resources, Animals and the Environment (DAFNAE), University of Padova, viale dell'Università 16, 35020 Legnaro, Padova, Italy Department of Life Sciences, University of Trieste, via Giorgieri 10, 34100 Trieste, Italy Department of Biology, University of Padova, via U. Bassi 58/B, I-35121 Padova, Italy
H I G H L I G H T S
G R A P H I C A L
A B S T R A C T
• The development of vineyards is a major driver of conversion of dry grasslands. • We test the potential of vineyards in contrasting landscapes for plant conservation. • Semi-natural habitats in the landscape positively affect plant diversity of vineyards. • Vineyards provide moderate chance for the conservation of plant of dry grasslands. • Remnants of dry grasslands are refugia for species of conservation concern.
a r t i c l e
i n f o
Article history: Received 3 September 2015 Received in revised form 11 December 2015 Accepted 11 December 2015 Available online xxxx Editor: J. P. Bennett Keywords: Crop landscape Plant conservation Ruderal species Semi-natural landscape Specialist species Species richness and composition
a b s t r a c t The increasing development of vineyards in Mediterranean areas worldwide is considered a major driver of conversion of several habitats of conservation concern, including calcareous dry grasslands that are targeted for biodiversity conservation by the European Union, according to Natura 2000 policies. Here, we aim at evaluating the potential of extensive vineyards located in contrasting landscapes (semi-natural vs crop-dominated) for providing suitable habitat conditions to plant species associated with dry grasslands. This study was carried out in one of the economically most important winemaking districts of Italy, characterized by a hilly landscape with steep slope vineyards. We compared plant communities of vineyards in contrasting landscapes with those of the remnants of dry grasslands. Our study demonstrates that landscape composition strongly affects local plant communities in vineyards, with a positive effect of semi-natural habitats bordering the cultivated areas. Our findings thus supply an additional tool for improving the effectiveness of viticultural landscapes for nature conservation. In particular, our results indicate that vineyards on steep slopes could provide moderate chance for the conservation of plant specialists inhabiting calcareous dry grasslands, depending on the landscape composition: vineyards embedded in semi-natural landscapes have more potential for conservation than those in crop-dominated landscapes. Our study also indicates that conservation efforts should aim at (a) decreasing the current management intensity that likely hampers the beneficial effects of semi-natural habitats in the surrounding
⁎ Corresponding author at: Department of Agronomy, Food, Natural Resources, Animals and the Environment (DAFNAE), University of Padova, viale dell'Università 16, 35020 Legnaro, Padova, Italy. E-mail address: [email protected] (J. Nascimbene).
http://dx.doi.org/10.1016/j.scitotenv.2015.12.051 0048-9697/© 2015 Elsevier B.V. All rights reserved.
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landscape on local plant assemblages, and (b) strictly conserving the remnants of dry grasslands that are irreplaceable refugia for habitat specialists and species of conservation concern. © 2015 Elsevier B.V. All rights reserved.
1. Introduction Biodiversity conservation is increasingly recognized as a crucial task for sustaining several ecosystem services that improve human wellbeing (Cardinale et al., 2012). Agriculture is among the main causes of biodiversity loss worldwide (Frishkoff et al., 2014; Karp et al., 2012; Pignatti, 1982) and there is increasing awareness that future biodiversity conservation will largely depend on the capability of cultivated areas to provide suitable habitats for species and communities of conservation concern (Baudron and Giller, 2014; Green et al., 2005; Phalan et al., 2011; Wright et al., 2012). The increasing development of vineyards in Mediterranean areas worldwide is considered a major driver of conversion of several habitats of conservation concern (e.g. Richter, 1989; Rühl, 2004; Viers et al., 2013), including calcareous dry grasslands that are targeted for biodiversity conservation by the European Union, according to Natura 2000 policies (European Commission, 2007). Habitat conversion results in simplified landscapes where this semi-natural vegetation is restricted to small scattered patches. However, recent research also highlighted that coupling biodiversity conservation with wine production could be a winning strategy both for marketing purposes and for counteracting the negative effects of global change (Bellosi et al., 2013; Hannah et al., 2013; Trivellone et al., 2014; Viers et al., 2013). This view is also reflected by the inclusion of several viticultural landscapes world-wide in the UNESCO world heritage list (http://whc.unesco.org/en/list/). Besides local management intensity, that is among the main drivers of local plant diversity in vineyards (Brugisser et al., 2010; Nascimbene et al., 2012, 2013; Poldini et al., 1998), the potential of vineyards to contribute to the conservation of dry grasslands is likely to be related to landscape composition (Weibull et al., 2003). In general, landscape composition influences local biodiversity of agro-ecosystems, with a positive effect of semi-natural habitats on various components of the
biota (e.g. Tscharntke et al., 2005, 2012b). This rationale would predict that richer plant communities should be expected in vineyards bordered by semi-natural habitats than in vineyards embedded in a landscape dominated by cultivated areas. While this hypothesis has been already tested in vineyard regions for several faunistic groups (e.g. Brittain et al., 2010; Hilty and Merenlender, 2004; Laiolo, 2005; Schmitt et al., 2008), it is still awaiting experimental evidence for plant communities. Here, we aim at evaluating the potential of extensive vineyards located in contrasting landscapes (semi-natural vs cropdominated) for providing suitable habitat conditions to plant species associated with dry grasslands. This study was carried out in one of the economically most important winemaking districts of Italy, characterized by a hilly landscape with steep slope vineyards. In this region, dry grasslands are severely declining due to agriculture intensification, being replaced by vineyards even on the steepest slopes. We compared plant communities of vineyards in contrasting landscapes with those of the remnants of dry grasslands. Besides considering the full species pool, we contrasted among different a-priori selected groups of species indicative of different local conditions (e.g., dry grassland specialists vs ruderal species) and of conservation concern (e.g., red-listed species and orchids). The patterns of these selected groups of species is expected to better help to elucidate the potential of vineyards to provide surrogate habitat for the conservation of plant communities of dry grasslands. On the one hand, we hypothesise that vineyards in semi-natural landscapes could host species assemblages more similar to those of dry grasslands as compared with vineyards in crop-dominated landscapes, especially when specialist species are considered. On the other hand, the vineyards in contrasting landscapes are expected to host similar assemblages of ruderal species, reflecting comparable management intensity, independently of landscape composition.
Fig. 1. Map of the study area, corresponding with the Conegliano-Valdobbiadene DOCG. Dry grasslands, vineyards in crop and in semi-natural landscapes are marked with different labels. Grey areas indicate the vineyards.
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Table 1 Main features (site conditions, management, % of semi-natural habitats in the landscape) of the three types of sites that were compared in this study. SMH = semi-natural habitats. Different letters indicate significant differences (P b 0.05).
Slope (°) Southness(°) Elevation (m) N mowing year−1 N herbicide year−1 N tot treatments year−1 kg N ha−1year−1 SMH 50 m (%) SMH 100 m (%) SMH 250 m (%) SMH 500 m (%)
Vineyards in Vineyards in crop landscapes semi-natural landscapes
Remnants of dry grasslands
38 ± 8a 33 ± 31a 280 ± 66a 3.1 ± 0.3a 0.8 ± 0.6a 9.7 ± 1.4a 19 ± 15a 2 ± 5a 6 ± 6a 22 ± 9a 34 ± 13a
42 ± 9a 41 ± 28a 302 ± 83a – – – – 78 ± 24c 75 ± 23b 72 ± 22b 68 ± 21b
39 ± 7a 39 ± 29a 318 ± 78a 3.1 ± 0.4a 0.8 ± 0.7a 9.6 ± 1.7a 22 ± 20a 52 ± 16b 65 ± 12b 66 ± 19b 59 ± 19b
2. Material and methods 2.1. Study area The study was carried out in the region of the ConeglianoValdobbiadene DOCG, one of the most important areas of north Italy for wine production (the worldwide famous Prosecco), including 6100 ha of vineyards in the northern part of the province of Treviso (Fig. 1; Veneto, NE Italy, N 45°52′40″, E 12°17′5″). This area is characterized by a hilly landscape where elevation ranges between 70 and 450 m, annual precipitation is between 900 and 1000 mm and mean annual temperature is 11 °C. In this hilly landscape vineyards occupy even the steep (N45°), mainly south facing, slopes where the cultivated area is composed by small vineyards, usually between 1 and 2 ha, belonging to several owners. This fragmented arrangement of the ownerships implies that local management practises may vary between adjacent vineyards. However, the severe topographic conditions are a deterrent for intensive, mechanized management. Mowing frequency is usually three times per year, without grass raking, while the use of herbicides may range between 0 and 2 treatments per year. Nitrogen supply is in general very low (0–100 kg ha−1). The wine produced in steep slope vineyards, locally defined by the traditional term “Rive”, is particularly valuable. For this reason, spurred by a growing market demand, the cultivation of steep slopes has drastically increased in the last decades, resulting in a simplification of the landscape matrix. The main impacted habitats, in terms of habitat loss and fragmentation, are dry grasslands that are addressed by the EU among the habitats of conservation concern, according with Natura 2000 policies. Approximately 90% of dry grasslands have been lost in last 40 years, with an acceleration in the last 10 years. In particular, we refer to dry grasslands that are classified under the Natura 2000 codes 6210, semi-natural dry grasslands and scrubland facies on calcareous substrates (Festuco-Brometalia), and 62A0, eastern sub-Mediterranean dry grasslands (Scorzoneretalia village). The former is considered a priority habitat when several orchid species are present. In the study area, these dry grasslands are restricted to very small, scattered, patches usually forming a buffer zone between forests and vineyards. Both natural (unmanaged) and semi-natural
(extensively managed) arid grasslands can be found, hosting highly diverse plant communities, often rich in rare orchid species. 2.2. Sampling design and plant identification Forty vineyards on steep slopes and 20 remnants of dry grasslands were selected for this study (Fig. 1). Vineyards were selected to represent two contrasting landscapes: 20 in landscapes dominated by cultivated areas (crop landscape; b30% of semi-natural habitats), and 20 in landscapes with a high percentage (N40%) of semi-natural habitats (semi-natural landscape), including both forests and dry grasslands. Landscape composition was assessed within a circular buffer of 250 m radius and differences between the two groups of vineyards were also tested (t-test) at smaller (i.e., 50 m and 100 m radius) and larger (500 m radius) spatial scales. Vineyards in both landscapes were selected to have similar exposure, elevation, surface, spontaneous vegetation, and farmers did not sow any seed mix for at least 10 years. Also management intensity did not differ between the vineyards located in the two landscapes: in both cases vineyards were mainly mown three times per year, while herbicides were applied 0–2 times per year (Table 1). Grasslands and vineyards located in contrasting landscapes were spatially interspersed in the study area. In each vineyard and dry grassland, the occurrence (presence-absence sampling) of all the vascular plants was recorded inside a 25 × 5 m plot placed in the center of the sampling site with the longer side disposed along the line of maximum slope. The survey was carried out between April 10 and May 15, 2014, before the first mowing. When possible, plants were identified in the field. However, in several cases species identification was based on the study of specimens (c. 1200) collected and stored in the personal herbarium of the authors. Especially specimens in the families of Poaceae and Cyperaceae were identified in the laboratory using a dissecting microscope. Critical specimens were submitted to a specialist for identification/confirmation. Material lacking fundamental diagnostic characters was identified at the genus level. Nomenclature follows Conti et al. (2005). 2.3. Statistical analysis Differences in species richness among vineyards in crop and seminatural landscapes and dry grasslands were tested by one-way analysis of variance (ANOVA). After the ANOVA, a Tukey's honest significance test for multiple comparison was applied to detect differences between the three types of sites (P b 0.05). Differences were tested on the total number of species per site, as well as on four a-priori defined subsets of species including: (a) species of conservation concern listed in the regional Red List (Buffa et al., in press). In this group we included species whose conservation status was scored under different IUCN categories (IUCN, 2001), including endangered, vulnerable, near threat, and least concern species; (b) orchids, whose presence is used to define the status of priority habitat of dry grasslands according to Natura 2000 policies (European Commission, 2007); (c) dry grassland specialists, and (d) ruderal species. Species of the last two categories were selected on the basis of available literature specific for Italy (Baldoni et al., 2001; Pignatti, 1982; Poldini et al., 1998). Compositional differences among vineyards in contrasting landscapes and dry grasslands were evaluated using a sites × species matrix
Table 2 Comparison of species richness and richness of groups of selected species among the three types of sites. Different letters indicate significant differences (P b 0.05).
Species richness (N of species) N of red listed species N of orchids N of specialists of dry grasslands N of ruderal species
Vineyards in crop landscapes
Vineyards in semi-natural landscapes
Remnants of dry grasslands
43 ± 8a 0.6 ± 0.8 0 4.3 ± 2.5a 20.7 ± 3.1a
69.9 ± 14b 1.7 ± 1.2 0.1 ± 0a 14.5 ± 8.4b 23.9 ± 6.3a
58 ± 10c 3.9 ± 2.3 2.2 ± 1.4b 34.2 ± 10.7c 3.8 ± 4.2b
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Table 3 Results of the multi-response permutation procedures (MRPP) that were used to test compositional differences among vineyards in contrasting landscapes and remnants of dry grasslands. This analysis was applied to the matrix including the full pool of species as well as to the two reduced matrices including only specialists of dry grasslands or ruderal species. P values of pairwise comparisons were adjusted with a Bonferroni correction. VCL = vineyards in crop landscapes; VSMHL = vineyards in semi-natural landscapes; DG = dry grasslands.
Total VCL vs VSMHL VCL vs DG VSMHL vs DG
All the species
Specialists of dry grasslands
Ruderal species
A = 0.41, P b 0.00001 A = 0.18, P b 0.00001 A = 0.44, P b 0.00001 A = 0.34, P b 0.00001
A = 0.20, P b 0.00001 A = 0.044, P = 0.0016 A = 0.22, P = 0.0002 A = 0.16, P = 0.0004
A = 0.21, P b 0.00001 A = 0.012, P = 0.12 A = 0.34, P b 0.00001 A = 0.17, P = 0.00005
including all the species and also using two reduced matrices that included only specialists of dry grasslands and ruderal species, respectively. Differences in species composition were tested by multi response permutation procedures (MRPP) as implemented in PC-ORD (McCune and Mefford, 1999), using the Sørensen distance measure and rank transformation of the distance matrices. MRPP was used to test differences between the three types of habitat (i.e. vineyards in contrasting landscapes and dry grasslands) as well as for the total, i.e. all the habitat types pooled together. We applied a Bonferroni correction to the pairwise P-values to avoid type I error, accounting for the number of pairwise comparisons. The test statistic “A” in MRPP describes the separation between stand types. The pattern of species composition was also visually evaluated using non-metric multidimensional scaling (NMDS; McCune and Grace, 2002) as implemented in PC-ORD
(McCune and Mefford, 1999), using the “slow and thorough” autopilot mode with the Sørensen distance measure. This procedure performed 40 runs with real dataset compared with 50 randomized runs, each run with 400 iterations. This iterative ordination method is based on ranked distances between sample units in the data matrix, known as “species space” (McCune and Grace, 2002); it does not assume normally distributed data and is therefore suited for most ecological data. A final 2-dimensions solution was selected for the matrices with all species and specialists of dry grasslands (stress 14% and 11%, instability 0.007 and 0.00008 respectively), while a final 3-dimensions solution was selected for ruderal species (stress 17%, instability 0.00014). 3. Results 3.1. Species richness In total, 368 species were found (Supplementary material A), 162 in vineyards in crop landscapes, 283 in vineyards in semi-natural landscapes, and 257 in dry grasslands. Red listed and orchid species were respectively 11 and 12, all recorded in dry grasslands. Only 2 red listed species were found in both types of vineyards, and 2 orchids in
Fig. 2. Ordination diagram of sampling sites in the species space based on non-metric multidimensional scaling (NMDS) performed with all the species. Different symbols indicate different types of sites: filled squares = dry grasslands, empty circles = vineyards embedded in landscapes with a high percentage of semi-natural habitats (semi-natural landscape), filled circles = vineyards embedded in landscapes dominated by cultivated areas (crop landscape). Total variation in species composition explained by the two axes was 96% (48% axis 1 and 48% axis 2).
Fig. 3. Ordination diagram of sampling sites in the species space based on non-metric multidimensional scaling (NMDS) performed with the subset of species that are specialists of dry grasslands. Different symbols indicate different types of sites: filled squares = dry calcareous grasslands, empty circles = vineyards embedded in landscapes with a high percentage of semi-natural habitats (semi-natural landscape), filled circles = vineyards embedded in landscapes dominated by cultivated areas (crop landscape). Total variation in species composition explained by the two axes was 81.6% (46.1% axis 1 and 35.5% axis 2).
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vineyards located in semi-natural landscapes. In total, 114 specialists of dry grasslands were found, 24 in vineyards in crop landscapes, 72 in vineyards in semi-natural landscapes, and 99 in dry grasslands. Eighty-six ruderal species were found: 66 in vineyards in crop landscapes, 80 in vineyards in semi-natural landscapes, and 30 in dry grasslands. The mean species richness was significantly (P b 0.05) higher in vineyards in semi-natural landscapes than in both vineyards in crop landscapes and dry grasslands (Table 2). The mean number of species of conservation concern (red listed species and orchids) was higher in dry grasslands than in vineyards in both landscape types (Table 2). Dry grasslands hosted the highest number of specialist species, vineyards in semi-natural landscape had an intermediate value that was however significantly higher than that of vineyards in crop landscapes. Vineyards in both landscapes hosted a similar number of ruderal species, while dry grasslands hosted a significantly lower number of these species. 3.2. Species composition The three types of sites significantly differed in species composition, as indicated by the MRPP test (Table 3). However, pairwise comparisons also indicated that communities of vineyards in semi-natural landscapes are more similar to those of dry grasslands as compared to vineyards in crop landscapes (lower “A” statistic values). This result is corroborated by the visual interpretation of the NMDS ordination
Fig. 4. Ordination diagram of sampling sites in the species space based on non-metric multidimensional scaling (NMDS) performed with the subset of ruderal species. Different symbols indicate different types of sites: filled squares = dry calcareous grasslands, empty circles = vineyards embedded in landscapes with a high percentage of semi-natural habitats (semi-natural landscapes), filled circles = vineyards embedded in landscapes dominated by cultivated areas (crop landscapes). Total variation in species composition explained by the three axes was 74.1% (25% axis 1, 12.7% axis 2, and 36.4% axis 3). The figure is based on the two most important axes.
(Fig.2), whose two axes account for 96% of the total variation in species composition (each axis 48%). In this ordination, sites belonging to different site types are plotted in the species space. Vineyards in semi-natural landscapes were plotted at an intermediate position between vineyards in crop landscapes and dry grasslands. Differences in species composition were evident also considering the two groups of specialist and ruderal species separately (Table 3). However, this analysis revealed that vineyards in contrasting landscapes were more similar to each other than considering the full pool of species. In particular, they had the same composition of ruderal species, and almost overlapping composition (very low value of the “A” statistic) of specialist species. The two NMDS ordinations (Fig. 3, 4), that explained 81.6% and 74.1% of the total variation in species composition respectively, corroborated these results. Considering specialist species (Fig. 3), sites belonging to vineyards in both landscapes were spatially concentrated in the species space indicating high among-sites similarity. Most of the dry grasslands were clearly separated from vineyards, while some sites were plotted close to vineyards in semi-natural landscapes. Considering ruderal species (Fig. 3), sites of dry grasslands were spatially concentrated in the species space and clearly separated from vineyards. Sites of vineyards in contrasting landscape largely overlapped in the species space. 4. Discussion Our study demonstrates that landscape composition strongly affects local plant communities in vineyards, with a positive effect of seminatural habitats bordering the cultivated areas. This positive relationship was already demonstrated for different types of crop (Marini et al., 2008; Tscharntke et al., 2012b), while experimental evidence for plant communities in viticultural landscapes was still missing. Our findings thus supply an additional tool for improving the effectiveness of viticultural landscapes for nature conservation, whose potential was addressed for a long time in the botanical literature (e.g., Richter, 1989; Sarzo, 2007). In particular, our results indicate that vineyards on steep slopes could provide moderate chance for the conservation of plant specialists inhabiting calcareous dry grasslands, depending on the landscape composition: vineyards embedded in semi-natural landscapes have more potential for conservation than those in cropdominated landscapes. However, the significant differences, in terms of both species richness and composition, between vineyards and the remnants of dry grasslands suggest that the maintenance of seminatural habitats at the landscape level should be coupled with a reduction of local management intensity (Nascimbene et al., 2013). As expected, comparisons among vineyards in contrasting landscapes and remnants of dry grassland yielded different results when the different groups of species were considered. Total species richness peaked in vineyards located in semi-natural landscapes, likely reflecting an additive effect of ruderal plants and dry grasslands specialists acquired by spill-over from the neighbouring semi-natural habitats. When considering both habitat specialists and species of conservation concern (i.e., red listed species and orchids) results revealed a gradient of decreasing habitat suitability from dry grassland remnants to vineyards in crop landscapes. Vineyards in semi-natural landscapes hosted 63% of the specialists of dry grasslands, corroborating their potential as surrogate habitat for these species. However, they were much less effective in hosting species of conservation concern that were only sporadically found in these vineyards. Considering the comparison in terms of ruderal species, we found large similarity between vineyards in contrasting landscapes, supporting the hypothesis that this component reflects the effect of management intensity, independently from the landscape. Accordingly, this component only marginally contributes to plant richness of dry grasslands. Differences in species richness were reflected by compositional differences, corroborating the view that only the dry grassland remnants hosted the target community, rich in species of conservation concern,
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addressed by the EU policies for biodiversity protection (European Commission, 2007). However, the less marked compositional differences between remnants of dry grasslands and vineyards in seminatural landscapes as compared with vineyards in crop landscapes further suggest that they have a greater potential as surrogate habitat for this target community. 5. Implications for management Awareness on the beneficial effects of biodiversity is increasing among farmers and there is increasing consensus on the fact that it is no longer possible to consider the reconciliation between agriculture and biodiversity as something superfluous (Tscharntke et al., 2012a,b). The possibility to improve the area of wildlife-friendly farming (Phalan et al., 2011; Tscharntke et al., 2012a,b) in hilly vineyard landscapes is a challenge that cannot be missed. In this perspective, our study indicates that efforts to enhance the potential of hilly vineyard landscapes for coupling biodiversity conservation and yield production should strongly focus on the maintenance and improvement of seminatural landscapes with a mixed composition of cultivated and seminatural areas adjacent to each other. However, our study also indicates that conservation efforts should aim at (a) decreasing the current management intensity that likely hampers the beneficial effects of seminatural habitats in the surrounding landscape on local plant assemblages, and (b) strictly conserving the remnants of dry grasslands that are irreplaceable refugia for habitat specialists and species of conservation concern. Other active conservation practices may be needed to favour the communities of dry calcareous grasslands within vineyards, especially when the sources of seeds are extremely scanty or very isolated. Acknowledgments This study was conducted as part of the project “ENDOFLORVIT”, funded by the Veneto Region (PSR 2007–2013Mis. 124).We are grateful to Thomas Wilhalm (Naturmuseum Südtirol) for the identification/confirmation of critical specimens and to the owners of the vineyards for kindly allowing us to work on their private land. Filippo Taglietti (Conegliano-Valdobbiadene DOCG Consortium) is thanked for his help in contacting the owners of the vineyards during the planning phase of the study. Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.scitotenv.2015.12.051. References Baldoni, M., Biondi, E., Loiotile, A., 2001. La vegetazione infestante i vigneti delle Marche. Fitosociologia 38, 63–68. Baudron, F., Giller, K.E., 2014. Agriculture and nature: trouble and strife? Biol. Conserv. 170, 232–245. Bellosi, B., Trivellone, V., Jermini, M., Moretti, M., Schoenenberger, N., 2013. Composizione floristica dei vigneti del Cantone Ticino (rvizzera). Bollettino della Società ticinese di scienze naturali 101, 55–60. Brittain, C., Bommarco, R., Vighi, M., Settele, J., Potts, S.G., 2010. Organic farming in isolated landscapes does not benefit flore-visiting insects and pollination. Biol. Conserv. 143, 1860–1867. Brugisser, O.T., Schmidt-Entling, M.H., Bacher, S., 2010. Effects of vineyards management on biodiversity at three trophic levels. Biol. Conserv. 143, 1521–1528. Buffa, G., Carpenè, B., Casarotto, N., Da Pozzo, M., Filesi, L., Lasen, C., Marcucci, R., Masin, R., Prosser, F., Tasinazzo, S., Villani, M., Zanatta, K., 2015. Lista rossa regionale delle piante vascolari. Regione Veneto (in press).
249
Cardinale, B.J., Duffy, J.E., Gonzalez, A., Hooper, D.U., Perrings, C., Venail, P., Narwani, A., Mace, G.M., Tilman, D., Wardle, D.A., Kinzig, A.P., Daily, G.C., Loreau, M., Grace, J.B., Larigauderie, A., Srivastava, D., Naeem, S., 2012. Biodiversity loss and its impact on humanity. Nature 486, 59–67. Conti, F., Abbate, G., Alessandrini, A., Blasi, C., 2005. An Annotated Checklist of the Italian Vascular Flora. Palombi, Roma. European Commission DG Environment Nature and Biodiversity, 2007. Interpretation manual of European Union habitats, EUR27. Frishkoff, L.O., Karp, D.S., M'Gonigle, L.K., Mendenhall, C.D., Zook, J., Kremen, C., Hadly, E.A., Daily, G.C., 2014. Loss of avian phylogenetic diversity in neotropical agricultural systems. Science 345, 1343–1346. Green, R.E., Cornell, S.J., Scharlemann, J.P.W., Balmform, A., 2005. Farming and fate of wild nature. Science 307, 550–555. Hannah, L., Roehrdanz, P.R., Ikegami, M., Shepard, A.V., Shaw, M.R., Tabor, G., Zhi, L., Marquet, P.A., Hijmans, R.J., 2013. Climate change, wine and conservation. Proc. Natl. Acad. Sci. U. S. A. 110, 6907–6912. Hilty, J.A., Merenlender, A.M., 2004. Use of riparian corridors and vineyards by mammalian predators in Northern California. Conserv. Biol. 18, 126–135. IUCN, 2001. IUCN Red List Categories and Criteria, Version 3.1. IUCN Species Survival Commission, IUCN, Gland and Cambridge. Karp, D.S., Rominger, A.J., Zook, J., Ranganathan, J., Ehrlich, P.R., Daily, G.C., 2012. Intensive agriculture erodes β-diversity at large scales. Ecol. Lett. 15, 963–970. Laiolo, P., 2005. Spatial and seasonal patterns of bird communities in Italian agroecosystems. Conserv. Biol. 19, 1547–1556. Marini, L., Scotton, M., Klimek, S., Pecile, A., 2008. Patterns of plant species richness in Alpine hay meadows: local vs. landscape controls. Basic Appl. Ecol. 9, 365–372. McCune, B., Grace, J.B., 2002. Analysis of Ecological Communities. MjM Software, Gleneden Beach, Oregon, US. McCune, B., Mefford, M.J., 1999. Multivariate Analysis of Ecological Data, Version 4.25. MjM Software, Gleneden Beach, Oregon, US. Nascimbene, J., Marini, L., Paoletti, M.G., 2012. Organic farming benefits local plant diversity in vineyard farms located in intensive agricultural landscapes. Environ. Manag. 49, 1054–1060. Nascimbene, J., Marini, L., Ivan, D., Zottini, M., 2013. Management intensity and topography determined plant diversity in vineyards. PLoS ONE 8 (10), e76167. http://dx.doi. org/10.1371/journal.pone.0076167. Phalan, B., Onial, M., Balmford, A., Green, R.E., 2011. Reconciling food production and biodiversity conservation: land sharing and land sparing compared. Science 333, 1289–1291. Pignatti, S., 1982. Flora d'Italia. 3 vol. Edagricole. Poldini, L., Oriolo, G., Mazzolini, G., 1998. The segetal vegetation of vineyards and crop fields in Friuli-Venezia Giulia (NE Italy). St. Geobot. 16, 5–32. Richter, M., 1989. UntersuchungenzurVegetationsentwicklung und zum Standortwandel auf mediterranen Rebbrachen. Braun-Blanquetia 4 196 pp. Rühl, J., 2004. Analisi dei processi di rinaturalizzazione nei vigneti e cappereti abbandonati del paesaggio terrazzato di Pantelleria (canale di Sicilia). Naturalista Sicil. 28, 1125–1146. Sarzo, A., 2007. Il paesaggio dell'abbandono nel circondario agreste di Senter (Valle di Terragnolo, Trentino). Ann. Mus. Civ. Rovereto 22, 110–170. Schmitt, T., Augenstein, B., Finger, A., 2008. The influence of changes in viticulture management on the butterfly (lepidoptera) diversity in a wine growing region of southwestern Germany. Eur. J. Entomol. 105, 249–255. Trivellone, V., Schoenenberger, N., Bellosi, B., Jermini, M., de Bello, F., Mitchell, E.A.D., More, M., 2014. Indicators for taxonomic and functional aspects of biodiversity in the vineyard agroecosystem of Southern Switzerland. Biol. Conserv. 170, 103–109. Tscharntke, T., Klein, A.M., Kruess, A., Steffan-Dewenter, I., Thies, C., 2005. Landscape perspectives on agricultural intensification and biodiversity – ecosystem service management. Ecol. Lett. 8, 857–874. Tscharntke, T., Clough, Y., Wanger, T.C., Jackson, L., Motzke, I., Perfecto, I., Vandermeer, J., Whitbread, A., 2012a. Global food security, biodiversity conservation and the future of agricultural intensification. Biol. Conserv. 151, 53–59. Tscharntke, T., Tylianakis, J.M., Rand, T.A., Didham, R.K., Fahrig, L., Batary, P., Bengtsson, J., Clough, Y., Crist, T.O., Dormann, C.F., Ewers, R.M., Frund, J., Holt, R.D., Holzschuh, A., Klein, A.M., Kleijn, D., Kremen, C., Landis, D.A., Laurance, W., Lindenmayer, D., Scherber, C., Sodhi, N., Steffan-Dewenter, I., Thies, C., van der Putten, W.H., Westphal, C., 2012b. Landscape moderation of biodiversity patterns and processes — eight hypotheses. Biol. Rev. 87, 661–685. Viers, J.H., Williams, J.N., Nicholas, K.A., Barbosa, O., Kotzè, I., Spence, L., Webb, L.B., Merenlender, A., Reynolds, M., 2013. Vinecology: pairing wine with nature. Conserv. Lett. 6, 287–299. Weibull, A.C., Ostman, O., Granqvist, A., 2003. Species richness in agroecosystems: the effect of landscape, habitat and farm management. Biodivers. Conserv. 12, 1335–1355. Wright, H.L., Lake, I.R., Dolman, P.M., 2012. Agriculture-a key element for conservation in the developing world. Conserv. Lett. 5, 11–19.