Introduction
The protection of the Italian flora has been addressed only by laws ratifying international agreements or European Union (EU) directives (Rossi et al., Reference Rossi, Montagnani, Abeli, Gargano, Peruzzi and Fenu2014a), and acts adopted by some administrations at local level (e.g. LR 10/2008, Lombardy Region; LR 45/2009, Valle d'Aosta Region; LR 9/2007, Friuli Venezia Giulia Region). The 1982 Bern Convention on the Conservation of European Wildlife and Natural Habitats, and the Habitats Directive (1992/43/EEC) are therefore the most important environmental regulations at the EU and national levels. Monitoring and reporting the conservation status of species listed in the Habitats Directive is mandatory for all EU member states. The EU has also established preferential funds targeted for the conservation of these species and their habitats (i.e. the LIFE Programme). These species (known as policy species) represent a heterogeneous group legally protected at the EU and national levels based on their supposed rarity, threatened status, and/or socioeconomic importance.
Using the IUCN Red List criteria to assess the extinction risk of policy taxa is a suitable and rapid method for verifying the effectiveness of national and EU conservation policies (Moreno Saiz et al., Reference Moreno Saiz, Domínguez Lozano and Sainz Ollero2003). The IUCN Red List procedure assesses the relative extinction risk of threatened taxa (IUCN, 2013). Globally, this procedure is the most widely used protocol for species risk assessment (Rodrigues et al., Reference Rodrigues, Pilgrim, Lamoreux, Hoffmann and Brooks2006) because it facilitates objective, replicable and flexible assessments (Gärdenfors et al., Reference Gärdenfors, Hilton-Taylor, Mace and Rodríguez2001; De Grammont & Cuarón, Reference De Grammont and Cuarón2006). Although the IUCN Red List criteria were developed for global assessments they are also widely used at regional (subglobal) scales (Gärdenfors et al., Reference Gärdenfors, Hilton-Taylor, Mace and Rodríguez2001; IUCN, 2012a), as exemplified by the numerous national and subnational Red Lists that have been produced in the last decade (e.g. Király, Reference Király2007; Tsintides et al., Reference Tsintides, Christodoulou, Delipetrou and Georghiou2007; Moreno Saiz, Reference Moreno Saiz2008; Kålås et al., Reference Kålås, Viken, Henriksen and Skjelseth2010; Rassi et al., Reference Rassi, Hyvärinen, Juslén and Mannerkoski2010; Turis et al., Reference Turis, Kliment, Feráková, Dítě, Eliáš and Hrivnák2014; Foggi et al., Reference Foggi, Viciani, Baldini, Carta and Guidi2015). Regional assessments of species extinction risk provide a basis for conservation planning and allocation of funds, not only at the administrative level (e.g. Bilz et al., Reference Bilz, Kell, Maxted and Lansdown2011) but also at a given biogeographical scale (Gentili et al., Reference Gentili, Rossi, Abeli, Bedini and Foggi2011). For these reasons up-to-date Red Lists are an important starting point for further conservation action and may provide useful information for monitoring changes in the conservation status of species. Despite these advantages relatively few taxa listed in the European policy instruments have been assessed recently in Italy using the latest version of the IUCN categories and criteria (version 3.1; e.g. de Montmollin & Strahm, Reference de Montmollin and Strahm2005; Fenu et al., Reference Fenu, Mattana and Bacchetta2011, Reference Fenu, Mattana and Bacchetta2012), and the currently available national and regional reports consider only few policy species and are based on older protocols (Conti et al., Reference Conti, Manzi and Pedrotti1992, Reference Conti, Manzi and Pedrotti1997).
Here we present the results of a national assessment, based on IUCN guidelines (IUCN, 2012a,b), of the conservation status of all Italian policy species, comprising vascular plants, bryophytes and lichens, listed in the annexes of the Bern Convention and the Habitats Directive 1992/43/EEC. The outcomes of Red List assessments can give an indication of the effectiveness of EU laws for the preservation of plant diversity. In particular, with this assessment we aim to identify the most threatened species and highlight threats and taxa that require urgent conservation action in Italy.
Methods
The conservation status of all the Italian policy species was assessed with the IUCN categories and criteria (IUCN, 2012b). Data on species distribution were collected from field surveys, herbarium specimens, and published and unpublished data since 2003. In some cases, for taxa occurring in stable habitats (e.g. remote forests or vertical cliffs), data since 1993 were used. All records were validated by a selected group of botanists, and revised taxonomically according to the most recent national checklist (Conti et al., 2005, Reference Conti, Alessandrini, Bacchetta, Banfi, Barberis and Bartolucci2007; Peruzzi, Reference Peruzzi2010) that incorporates the latest taxonomic updates (i.e. the Angiosperm Phylogeny Group (APG) III system). In cases where groups of species were included in the Bern Convention and Habitats Directive (e.g. at the genus level: Sphagnum L. spp., Lycopodium L. spp., Cladonia P. Browne subgenus Cladina (Nyl.) Nyl.) all of the species belonging to the genus and occurring in Italy were treated separately. The data were organized in a database, including distribution of taxa, population trends, and the main threats identified by expert-based observations, and then categorized according to the IUCN threats classification scheme (version 3.2; IUCN, 2012c). The distribution data were organized in a geo-database, in which each georeferenced record of a species was reported in a grid of 2 x 2 km cells generated using ArcGIS v. 9.2 (ESRI, Redlands, USA) and superimposed on a map of Italy (Gargano, Reference Gargano2011). This ensured standardized calculations of Area of Occupancy, as are required under criterion B2 (IUCN, 2013). In a few cases, when reliable data on population trends or population size were available, other criteria were also applied (e.g. A, C and D; IUCN, 2012b; Rossi et al., Reference Rossi, Montagnani, Gargano, Peruzzi, Abeli and Ravera2013a). Following the precautionary approach suggested in Butchart et al. (Reference Butchart, Stattersfield and Brooks2006) and the IUCN guidelines (version 9.0, 2011), species that were not recorded during the previous 3 decades but for which there remained uncertainty regarding extinction were categorized as Critically Endangered (Possibly Extinct).
Results
A total of 203 policy species were assessed, based on 10,957 georeferenced records. The taxa considered in the assessment included 60 (29.6%) species endemic to Italy, 35 (58.3%) of which were assigned to a threat category. The risk category for each species, and the criteria applied in each assessment, are summarized in Supplementary Table S1. One species, Aldrovanda vesiculosa L., was categorized as extinct in Italy (Regionally Extinct). Ten species (seven vascular plants and three bryophytes) had not been recorded in recent years and were categorized as Critically Endangered (Possibly Extinct). Eighty-five taxa (41.9%) were assigned to a risk category (Critically Endangered (Possibly Extinct), Critically Endangered, Endangered, Vulnerable; Table 1). An additional 24 species (11.8%) were categorized as Near Threatened, and 43 species (21.2%) were categorized as Least Concern. Fifty policy species (24.6%), mostly bryophytes (32), were categorized as Data Deficient because the available data did not permit a robust assessment (Table 1). The assessment was based primarily on criterion B because most of the data used were distribution records, and there was little information available on population dynamics (only 11 taxa assessed using criteria C or D).
Table 1 Numbers of EU policy plant species (grouped as vascular plants, bryophytes and lichens) present in Italy assigned to each Red List category, with the numbers of Italian endemic species in parentheses.
Most of the species evaluated were affected by multiple threats (IUCN, 2012c), mainly related to human-mediated habitat modifications (Fig. 1). Threats in the major category of natural system modifications were the most frequent (30%); these included modifications of processes underlying natural and semi-natural systems (e.g. fire, water use, degradation, abandonment). One-fifth of taxa were also threatened by human intrusion and disturbance, including recreational activities and tourism. Other significant threats included agriculture and aquaculture (10%), which affect mainly wetlands and grasslands (i.e. intensification of grazing, inadequate agro-pastoral practices), residential and commercial development (7%), which affects the coastal areas of Italy, and invasive and other problematic species (7%).
Fig. 1 The percentage of 203 policy species of the Italian flora subject to each major threat category according to the IUCN Threats Classification Scheme (version 3.2; IUCN, 2012c).
Discussion
The EU is considered to possess one of the most advanced and effective intergovernmental biodiversity policy instruments (Trouwborst, Reference Trouwborst2009) but, based on previous reports at EU level, only 17% of the species and habitats legally protected by the Habitats Directive 1992/43/EEC have a favourable conservation status (Condé et al., Reference Condé, Jones-Walters, Torre-Marin and Romão2010). The data from Italy are consistent with those of a European assessment of the policy species, in which 44.9% of vascular plants were categorized as threatened (Bilz et al., Reference Bilz, Kell, Maxted and Lansdown2011). There are also similarities between Europe as a whole and Italy in terms of threats, with human-mediated habitat loss, degradation and fragmentation being among the most prevalent threats (Bilz et al., Reference Bilz, Kell, Maxted and Lansdown2011).
The results of this assessment indicate that significant work remains to reach the conservation targets of the Habitats Directive, the Global Strategy for Plant Conservation, and the European Strategy for Plant Conservation, and that the efforts undertaken in the last 20 years are insufficient to maintain an acceptable conservation status for many taxa. According to EU legislation the conservation of policy species is mandatory (art.8 Directive 1992/43/EEC), and member states have full responsibility for their conservation, especially for endemic species.
This assessment revealed that the legal protection of entire groups of species (e.g. Sphagnum, Lycopodium, Cladonia subgenus Cladina) does not ensure their conservation. Because single species are not distinguished within these groups, the risk level assigned to most threatened taxa is misleadingly reduced by the contributions of less threatened species. In addition, such groups encompass species adapted to various habitats (e.g. Cladonia spp.), reducing the possibility of effective habitat-based conservation measures. Hence, the conservation approach that encompasses entire groups of taxa should be avoided and a single-taxon approach used. Conservation action plans, which currently are available only for a few taxa (Devillers-Terschuren, Reference Devillers-Terschuren1999), are required.
IUCN criterion B was the most commonly used criterion for risk categorization because of the ease of collecting distribution data. This is as a result of the lack of detailed information on population dynamics (such as number of mature individuals, population viability analysis) of the species. There is a particular problem with non-vascular taxa. Detailed occurrence data for bryophytes (i.e. Sphagnum spp.) are available only for some areas of Italy, and the population trends of these species are mostly unknown. This led to the categorization of a significant proportion of species as Data Deficient. Eleven percent of vascular plants have also been categorized as Data Deficient, indicating that further biogeographical and ecological analyses of policy species should be undertaken. As highlighted by Crain & White (Reference Crain and White2013), continuing field and herbarium research is fundamental to confirm and update the distribution of threatened plants and to facilitate conservation of these species. Moreover, mapping plant distributions is useful for revealing localized areas most in need of attention and, given that availability of funding is often the main limitation to conservation, helps to focus attention on legal protection and targeted management for small geographical areas with relatively high levels of plant diversity (Médail & Quézel, Reference Médail and Quézel1999; Laguna et al., Reference Laguna, Ballester, Ranz, Fabregat, Olivares and Serra2003; Crain et al., Reference Crain, White and Steinberg2011; Cañadas et al., Reference Cañadas, Fenu, Peñas, Lorite, Mattana and Bacchetta2014).
Although in situ conservation measures are the best methods for preserving plant diversity (UNEP, 2002), ex situ conservation provides an alternative method for preventing immediate extinction (UNEP, 2002; Godefroid et al., Reference Godefroid, Rivière, Waldren, Boretos, Eastwood and Vanderborght2011a). More importance should be given to ex situ conservation in seed banks (Mattana et al., Reference Mattana, Fenu and Bacchetta2012; Rossi et al., Reference Rossi, Orsenigo, Dhital, Shrestha, Shrestha and Maharjan2014b), which may support further interventions requiring detailed biological and ecological knowledge (Gentili et al., Reference Gentili, Abeli, Rossi, Li, Varotto and Sgorbati2010; Abeli et al., Reference Abeli, Orsenigo, Ardenghi, Lucassen and Smolders2013) and the careful use of plant material, such as translocations (Godefroid et al., Reference Godefroid, Piazza, Rossi, Buord, Stevens and Aguraiuja2011b; Maschinski & Haskins, Reference Maschinski and Haskins2012; Cogoni et al., Reference Cogoni, Fenu, Concas and Bacchetta2013; Rossi et al., Reference Rossi, Amosso, Orsenigo and Abeli2013b; Soorae, Reference Soorae2013). Conservation priorities and intervention strategies should be established at the national scale, as has been accomplished in some cases at the regional level in Italy (e.g. Sardinia; Bacchetta et al., Reference Bacchetta, Fenu and Mattana2012). The results of this assessment can be used to determine those species at the brink of extinction (Critically Endangered, e.g. Isoetes malinverniana Ces. & De Not., Abeli et al., Reference Abeli, Barni, Siniscalco, Amosso and Rossi2012; Barni et al., Reference Barni, Minuzzo, Gatto, Lonati, Abeli and Amosso2013), for which conservation is a pressing need, and to define specific plans, including both in situ and ex situ measures (e.g. Devillers-Terschuren, Reference Devillers-Terschuren1999; Grunau et al., Reference Grunau, Handwerk and Spackman-Panjabi2011).
At present EU member states are required to draw up a report every 6 years on the conservation status of species and habitats listed in the Habitats Directive (ex art. 17). However, for those species at the brink of extinction, monitoring activities should be more frequent (at least every 2 years) and conservation actions should start immediately for all species assigned to a threat category (including Vulnerale and Endangered).
As demonstrated by Stanton et al. (Reference Stanton, Shoemaker, Pearson and Akçakaya2015) and Akçakaya et al. (Reference Akçakaya, Butchart, Watson and Pearson2014) for species threatened by climate change, conservation actions should begin as soon as a species is listed as Vulnerable, because 50% of species have gone extinct within 20 years of becoming categorized as Critically Endangered. Protocols for listing threatened species are useful for forecasting extinctions (Keith et al., Reference Keith, McCarthy, Regan, Regan, Bowles and Drill2004) and in this sense the results presented here are alarming.
In conclusion, the current legal protection is insufficient to guarantee plant conservation, and Red Lists are a valuable tool to focus the attention of policymakers and conservation planners, as well as the general public, on the most threatened species. However, there is an urgent need for conservation action and management strategies. Otherwise we risk losing a large portion of plant diversity within the next few decades.
Acknowledgements
The authors are grateful to the Italian Ministry for the Environment, Land and Sea, Directorate for Nature Protection, for its financial support of the Red List assessment programme described here, and to the secretariat of the Italian Botanical Society for its support during the process. We thank the more than 200 Italian botanists who provided field data, without whose collaboration these assessments would have been impossible.
Biographical sketches
The authors are all members of the Italian Botanical Society (SBI), founded in Florence in 1888. The SBI is organized into working groups dealing with specific areas of interest. The activities of the Working Group for Nature Conservation are focused on issues inherent to the preservation of the Italian floristic heritage. Since 2006 the Working Group for Nature Conservation, supported by other groups of the SBI (Floristic, Lichenology, Bryology, and Mycology), has promoted the development of a new and comprehensive Red List of the Italian Flora based on the most recent IUCN protocol, and has collaborated with IUCN specialists by contributing to the European Red List and other continent-wide assessment programmes.
