Conserving Plant Diversity in Europe: Outcomes, Criticisms and Perspectives of the Habitats Directive Application in Italy

Home , Centranthus trinervis, Galium litorale, Paeonia officinalis

Biodivers Conserv DOI 10.1007/s10531-016-1244-1

ORIGINAL PAPER

Conserving plant diversity in Europe: outcomes, criticisms and perspectives of the Habitats Directive application in Italy

1 2 3 4 G. Fenu • G. Bacchetta • V. Giacanelli • D. Gargano • 5 6 2 C. Montagnani • S. Orsenigo • D. Cogoni • 7 8 9 2 G. Rossi • F. Conti • A. Santangelo • M. S. Pinna • 8 10 11 1 F. Bartolucci • G. Domina • G. Oriolo • C. Blasi • 12 7 3 P. Genovesi • T. Abeli • S. Ercole Received: 13 June 2016 / Revised: 11 October 2016 / Accepted: 21 October 2016 Ó Springer Science+Business Media Dordrecht 2016

Abstract Habitat Directive is the core strategy of nature conservation in Europe aiming at halting biodiversity loss. In this study the results of the third Italian assessment regarding the conservation status (CS) of plants listed in the Habitat Directive (Flora of community interest—FCI) was presented. Data was collected from several sources related to plant distribution, population data, habitats and pressures. Following the ofﬁcial European procedure, all parameters were evaluated and combined to give the CS of each taxon in each biogeographical region of presence. A comparison between the recent Italian IUCN

Communicated by Daniel Sanchez Mata.

This article belongs to the Topical Collection: Biodiversity protection and reserves.

& S. Orsenigo [email protected]

1 Dipartimento di Biologia Ambientale, ‘Sapienza’ Universita` di Roma, P.le A. Moro 5, 00185 Rome, Italy 2 Centro Conservazione Biodiversita` (CCB), Dipartimento di Scienze della Vita e dell’Ambiente, Universita` degli Studi di Cagliari, Viale S. Ignazio da Laconi 11-13, 09123 Cagliari, Italy 3 Dipartimento Difesa della Natura, Istituto Superiore per la Protezione e la Ricerca Ambientale, via Vitaliano Brancati 60, 00144 Rome, Italy 4 Dipartimento di Biologia, Ecologia e Scienze della Terra, Universita` della Calabria, Via P. Bucci, 87030 Arcavacata, Italy 5 Department of Earth and Environmental Sciences, University of Milano Bicocca, Piazza della Scienza 1, 20126 Milan, Italy 6 Dipartimento di Scienze Agrarie e Ambientali - Produzione, Territorio, Agroenergia, Universita` degli Studi di Milano, Via G. Celoria 2, 20133 Milan, Italy 7 Dipartimento di Scienze della Terra e dell’Ambiente, Universita` degli Studi di Pavia, Via S. Epifanio 14, 27100 Pavia, Italy 8 Scuola di Bioscienze e Medicina Veterinaria, Universita` di Camerino - Centro Ricerche Floristiche dell’Appennino, Parco Nazionale del Gran Sasso e Monti della Laga, San Colombo, 67021 Barisciano, L’Aquila, Italy 123 Biodivers Conserv and Reporting assessments was performed in order to evaluate the consistency between these two assessments. The official EU checklist comprises 113 Italian plant taxa, 107 of which were examined in this study. Our results showed a critical situation with only 34% of favourable CS, while 50% were unfavourable (40% inadequate plus 10% bad) and 16% unknown, in particular in the Mediterranean bioregion, where the unfavourable assessments reach the 65%. The results of the Report were consistent with those of the IUCN assessment, in which 41.9% of plants were threatened with extinction. This report highlighted some benefits and criticisms at national level, but it may have a wider significance. Although a general advance of knowledge, a great effort is needed to reach the Habitats Directive goals. Despite the limited resources, monitoring activities needs to be improved in order to close information gaps for several plants. A positive outcome was the development of a specific national project funded by the Italian Ministry of Environment, with the ambitious target to set future monitoring activities for FCI and optimize monitoring efforts.

Keywords Conservation status Á Italian ﬂora Á Flora of community interest (FCI) Á IUCN Red List Á Endemic plant Á Science–policy interface

Abbreviations CS Conservation status HD Habitats Directive FCI Flora of community interest

Introduction

The preservation of biodiversity, a well-established priority in global environmental policies, is a key component of the UN 2030 agenda for sustainable development and is a global obligation under the Strategic Plan for Biodiversity 2020. Nowadays biological diversity faces several threats and the loss of biodiversity is constantly increasing (Pimm et al. 1995; Novacek and Cleland 2001; Butchart et al. 2010; Ceballos et al. 2015). IUCN Red Listing process of endangered species is the most applied method to assess the extinction risk of plant and animal species, due to its objective, replicable, and ﬂexible protocol of risk assessment, measuring the distance of a species’ status from the extinction risk (Rodrigues et al. 2006; Collen et al. 2016). Although originally developed for global assessments, the IUCN Red Listing system is widely used at regional scales, where it plays a key role for prioritizing conservation activities (e.g. Moreno Saiz 2008; Bilz et al. 2011; Rossi et al. 2016). However, the European Commission has developed its own speciﬁc

9 Dipartimento di Biologia, Universita` degli Studi di Napoli, c/o Orto Botanico, via Foria 223, 80139 Naples, Italy 10 Dipartimento di Scienze agrarie e forestali, Universita` degli Studi di Palermo, Via Archiraﬁ, 38, 90123 Palermo, Italy 11 Localita` Basovizza 16, 34149 Trieste, Italy 12 Servizio Consulenza Faunistica, Istituto Superiore per la Protezione e la Ricerca Ambientale, via Vitaliano Brancati 44, 00144 Rome, Italy

123 Biodivers Conserv methodology (conceptually opposed) to assess the conservation status (CS, hereafter) of species (and habitat) protected by the Habitats Directive 92/43/EEC (HD, hereafter) in the 27 EU countries. The main difference between the two assessment of species’ conservation status (IUCN and HD protocols), is that the former measures the distance of a species from the risk of extinction, while the latter measures the distance from a ‘‘Favourable Con- servation Status’’. However, these two different, but generally comparable, schemes provide an opportunity for a comparison to explore potential uncertainties involved in such assessments (Moser et al. 2016) and/or between scientists’ Red Lists, and nature protection legislation enacted by governments (Mendoza-Fernańdez and Mota 2016); this issue deserve a relevant interests because setting conservation actions largely depends on the agreement among experts on the conservation status of species (Moser et al. 2016). Habitat Directive and the Natura 2000 network with more than 27,000 sites covering about 18% of the terrestrial surface of the EU (European Commission 2015), represent the core strategy of nature conservation in the EU and the most important tools aiming at halting, or at least significantly reducing, biodiversity loss (e.g. Balmford et al. 2005; Maiorano et al. 2007; Pullin et al. 2009). Through the implementation of cogent conservation policies, the HD promotes the conservation of natural habitats and species in a favourable conservation status (European Commission 1992). In order to assess the effects of the conservation policies and the effectiveness of HD, the EU Commission requires the assessment of the CS of species and habitats at national and biogeographical levels, with a 6-year interval (Evans and Arvela 2011). Specifically, article 17 requires to report about the HD implementation and the conservation status of species (and habitat), and all EU Member States have full responsibility for their conservation, especially for endemic species (Bock et al. 2005; Fenu et al. 2015b; Rossi et al. 2016). However, HD application and interpretation is not always clear; the key concept of favorable CS, for example, contains several aspects that led in the past to misinterpretation (e.g. Vela´zquez et al. 2010; Flather et al. 2011; Epstein et al. 2015). Accordingly, must be noted that some key concepts (e.g. FRV is favourable reference value, FRP is favourable reference population, etc.) are being discussed by a specific working group of the EC, and further guidance is thus expected to be developed in the next future. Overcoming such problems would be important for the correct application of HD, in EU as a whole and in each Member State. For what concern Italy, though the Directive does not include the complete national floristic diversity, it represents the main legal tool for the conservation of wild plants, because a national law is still lacking (Rossi et al. 2014). Italy hosts a high number of plant taxa of community interest (vascular plants, bryophytes and lichens) favoured by an extremely diversified territory, encompassing three biogeographical regions (Alpine, Continental, and Mediterranean) and the Mediterranean marine region: hence monitoring and reporting efforts required by HD are particularly demanding. Additionally, the high endemism rate of the Italian flora determines a significant national responsibility, at national and regional levels as previously demonstrated (e.g. Bacchetta et al. 2012; Fenu et al. 2015b; Rossi et al. 2016). The previous monitoring reports (1994–2000, 2001–2006) highlighted several specific weaknesses in the implementation of HD. The first report addressed the legal implementation of the HD, the progress in establishing the Natura 2000 network and highlighted several problems (e.g. lack of available data, unclear definition of some habitats, exclusion or addition of habitat type or species in a certain geographical area or in a Member State; European Commission 2004). The second report presented the first CS assessment of habitats and species, indicating that only 17% for both species and habitats was in a favourable CS. This report also demonstrated that only a few member states had invested 123 Biodivers Conserv sufficient resources in species monitoring (European Commission 2009). In general, the second report may have caused an overestimation of ‘favourable’ assessments (Sipkova et al. 2011) for some Mediterranean countries (i.e. Italy and Greece), for which data was available mainly from protected areas and the presence of a species in such areas was simply considered a guarantee of its conservation, though this assumption is not always valid. Additionally, as detected for Italy, the lack of data for some parameters may have also led to an overestimation of favourable evaluations (MATTM 2008). In this paper, the results of the third Italian assessment of the CS of FCI included in the HD are presented. The report, referring to the whole territory, has been realised through a collaborative effort among public institutions (i.e. Ministry of the Environment, Institute for Environmental Protection and Research, Administrative Regions), scientific societies and botanists from several Italian universities (Genovesi et al. 2014). In particular, this paper aims to: (1) provide an overall picture of the CS of the Italian flora listed in the HD, also considering the results achieved at the EU level; (2) analyse the CS data at a biogeographical level, and identify the main pressures/threats affecting the Italian flora listed in the HD; (3) verify the relationships between the results of the HD report and the recent assessment of the policy species against the IUCN Categories and Criteria (Rossi et al. 2014, 2016); (4) highlight the major issues encountered during the monitoring process, and suggest possible ways for their solutions.

Materials and methods

Checklist elaboration

The official EU checklist comprises 113 Italian plants listed in the HD annexes, including vascular plants, bryophytes and lichens. More in detail, 90 plant taxa are listed in Annex II (32 of priority interest), and 23 (20 species and 3 genera) in Annexes IV and V. The checklist was revised according to the most recent taxonomical and nomenclatural updates (e.g. Conti et al. 2005, 2007; Ros et al. 2013; Aleffi et al. 2008; Peruzzi et al. 2014; Fenu et al. 2014). Further taxonomical and nomenclatural revisions were derived from the ‘‘New Red List of the Italian Flora’’ database (Rossi et al. 2014, 2016). The catalogue of the Italian endemic plants (Peruzzi et al. 2014, 2015), and the checklist of hornworts, liverworts and mosses of Italy (Aleffi et al. 2008), were followed in order to calculate the endemism rate.

Data collection

Data collection of FCI was carried out for two years (2011–2013), and included available data from several sources related to plant distribution, population data, and habitat prop- erties and pressures. Distributive and population data were ﬁrstly derived from Regions and Autonomous Provinces databases, strongly implemented with the data derived from the ‘‘New Red List of the Italian Flora’’ database (Rossi et al. 2014, 2016); specialised bibliography, ﬂoras and atlas have been also viewed (e.g. Aeschimann et al. 2004; Conti et al. 2005, 2007; Scoppola and Spampinato 2005). All records were validated, involving local botanists that often provided new or unpublished records. All vascular species belonging to each of the genera listed in the annexes (e.g. Sphagnum sp., Lycopodium sp.) were considered all together as a single unit (=a single

123 Biodivers Conserv taxon) in order to be included in the analyses; similarly all lichens belonging to Cladonia, which was considered as a complex (Ravera et al. 2016), were considered as single unit.

Data analysis

Data analysis was carried out in 2013, following the methodology defined by the European Commission official guidelines (Evans and Arvela 2011). The assessment protocol requires a separate evaluation for each plant species in each bioregion; because some species occurred in more than one bioregion, the number of assessments compiled was higher than the number of plant included in the checklist. Following the standard procedure, different parameters (i.e. range, population size, habitat for the species and future prospects) were evaluated for each plant species, and then combined to give an overall assessment of its CS. Article 17 places particular emphasis on the estimation and assessment of plant species ranges, considered as an envelope generalizing the distribution with major discontinuities excluded. For this purpose a specific ‘Range Tool’ is provided by the EC (Mac Sharry 2012). Only for species with narrow ecological niche and fragmented or particular dis- tributions (e.g. small islands or coastal habitat) the range was manually computed (Ercole and Giacanelli 2014). The distribution and range maps have been developed using the standard 10 9 10 km European grid (Lambert azimuthal equal area projection, ETRS89- LAEA5210). Distribution data, including those from the ‘‘New Red List of the Italian Flora’’ database and unpublished records from local botanists, were uploaded in the standard 10 9 10 km grid. To define the population size, an estimation of the number of ‘mature individuals’ (i.e. adult individuals known or thought to be capable of reproducing) per population is primarily recommended (Evans and Arvela 2011). When not available, the number of localities or the number of grid cells (2 9 2 and 10 9 10 km) where a plant species grows is admitted as alternative units. The EC methodology also requires the evaluation of the FRV for range and population; to date, in Italy quantitative data for these threshold values are lacking; as a consequence, the comparison between FRV and the observed situation was based only on experts judgment by estimating the deviation of the actual size of range/population from the optimal value. The habitat for the plant species, considered as the biological and physical resources used by a plant during its life, requires evaluation of habitat extent (in km2), quality and trend (Evans and Arvela 2011); area occupied is currently lacking for Italian plant species, thus only the fields concerning habitat quality and trend were filled when available. Besides the actual situation, the assessment of the overall CS takes into account the future perspectives (predictable status in the next 12 years). Such prospects should con- sider the more likely future status and trends, which will depend on pressures (negative influence) and conservation measures (potential positive influence). Pressures, defined as current factors affecting the long-term viability of assessed species, were selected from the official list provided by EC specifying also the relative intensity (high, medium, low). In this study only the medium and high intensity pressures were considered because they are those that have a real impact on the populations. Finally, from the combination of all parameters by the evaluation matrix, according to the EC guidelines, derived the assessment of the overall CS of each taxon in each biogeographical region of presence. The CS can be expressed through one of the following categories: Favourable (the species is expected to prosper without any change to existing management or policies), 123 Biodivers Conserv unfavourable–inadequate (a change in management or policy is required to bring back the species to favourable conditions, but there is no danger of extinction in the foreseeable future), and unfavourable–bad (species in serious danger of becoming extinct, at least regionally). In case of scarce data, the CS can be reported as unknown.

Relationship between conservation status (CS) and IUCN risk category

Recently, in order to evaluate the effectiveness of existing protection measures at the national level, the ‘‘New Red List of the Italian Flora’’ project assessed the conservation status of the 197 Italian policy plant species listed in the Bern Convention and in the HD annexes (Rossi et al. 2014, 2016), according to the current IUCN categories and criteria (IUCN 2001, 2003). Article 17 and Red Lists aim to assess the status of a species using quantitative indicators such as size and trends in the area of occurrence, population size and trends (Moser et al. 2016); nonetheless, they adopt similar but different criteria. There is not a one to one relationship between a IUCN and the CS categories. However, considering that both methods are based on similar type of data (population size, range, population trends, etc.), a comparison may be possible, keeping on mind that species with a favourable conservation status according to the HD reporting method should, by definition, not be threatened by extinction; and, vice versa, highly threatened species according to the IUCN method are unlikely to be in a favourable conservation status: it is expected that a species considered critically endangered by the IUCN protocol would normally be assessed as unfavourable– bad by the reporting (Evans and Arvela 2011). Despite this conceptual difference, com- paring these two closely related assessments may help to understand how the policies introduced with the HD can influence the value of the extinction risk of the species as well as to detect potential uncertainties involved in such assessments. In order to check the relationships between the two assessment outcomes a similar approach proposed by Moser et al. (2016) was applied here. For plants showing a diverse CS among different biogeographical regions, the worst CS was chosen based on the precautionary principle. Plant species categorised as DD in the Red List, and those with unknown CS under article 17 were not included in the comparison. To assess the association level between the CS emerged from the reporting procedure and the IUCN risk category a correlation analysis was conducted between two ordinal variables. The first (IUCN) consisted in five levels reflecting an increasing extinction risk (LC = 1; NT = 2; VU = 3; EN = 4; CR = 5), while the second (Art. 17) included three levels indicating a decreasing CS (FV = 3; U1 = 2; U2 = 1). Then, a correlation analysis was performed in SPSS 23.0 (SPSS, Chicago, IL, USA) to evaluate direction and strength of the association between the two ordinal variables. This was done by calculating the Spearman’s Rho and Kendall’s tau-b, two correlation measures suitable for semi-quantitative variables (Legendre and Legendre 1998).

Results

Updating the checklist of Italian plants of community interest

Although ofﬁcial lists indicate that the Italian FCI comprises 113 plant taxa, our updates showed that three plant species (Asplenium hemionitis, Colchicum corsicum, and Myosotis

123 Biodivers Conserv rehsteineri) were reported in the past because of misidentiﬁcation or insufﬁcient taxonomic knowledge, but they do not occur in Italy (see Appendix Table 5 for details). Additionally, two taxa (Aldrovanda vesiculosa, Caldesia parnassifolia) became extinct in the last years. Moreover, Centranthus trinervis should be excluded because it is absent from Sardinia, where occurs Centranthus amazonum. The inclusion of the latter species among those protected by the HD has been formalised only in 2016 and for this reason this plant was not previously considered. Thus, excluding the three species erroneously indicated for Italy, the two extinct plants and the case of Centranthus trinervis, the third report for the Italian FCI considered 107 taxa (96 vascular, 10 bryophytes, one lichen).

Distribution data of FCI

Distribution and range maps have been developed at national scale for 103 of the 107 taxa assessed; data was lacking for three bryophyte (Sphagnum, Leucobryum glaucum, Mannia triandra) and one vascular group (Lycopodium sp.). At the biogeographical level, 82 taxa (76.63% of the total) are conﬁned to one bioregion, while 12 occur in two, and 13 in all the three bioregions (Table 1). The highest number of vascular plants occurred in the Mediterranean bioregion, while the bryophytes are mainly recorded in the Alpine region (Table 1). The endemism rate of Italian vascular plants of European interest is 57.29% (55 endemic species); there are no endemics among non-vascular plants. The distribution data showed the prevalence of plants with narrow or extremely narrow ranges; in particular, 11 plant species (10.67%) occurred in only 1 grid-cell and 28 (27.18%) in a range of 2–5 grid-cells. Twelve taxa, all included in annex IV and V, occurred in more than 50 cells. The density map, obtained by overlapping all the 103 plant distribution maps (Fig. 1), showed the areas with the highest FCI density, corresponding to the areas with higher conservation interest in Italy according to the HD. Highest densities were found in restricted areas: islands, coastal territories bordering Campania, Calabria and Lucania and in mountainous areas of the Northern and Central Apennines, the Maritime, Ligurian and South-Eastern Alps; the Trieste Karst and the Upper Adriatic coastal sector also showed high plant density values (Fig. 1). Species richness and endemism rate were particularly high in Sardinia, Sicily and Friuli-Venezia Giulia regions.

Table 1 Number and distribution in the biogeographic regions of the Italian plant taxa of community interest listed in the Habitats Directive Taxonomic group Total Percentage (%)

Vascular plant Bryophytes Lichen (Cladonia)

One bioregion 77 5 0 82 76.63 Two bioregions 10 2 0 12 11.21 Three bioregions 9 3 1 13 12.14 Total 96 10 1 107 100 Alpine 37 9 1 47 Continental 32 5 1 38 Mediterranean 55 4 1 60

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Fig. 1 Density map of the Italian Flora of community interest (FCI); a Density map of the plant species listed in all annexes (II, IV, V). b Density map of the plants listed only in the Annex II (90 plant species). The boundaries of the biogeographical and administrative Italian regions were also indicated

Demographic data

Data on ‘‘number of mature plants’’ per population were available only for a subset of 29 taxa listed in the HD annex II. For the other taxa, different units were used, like the number of presence localities (22 taxa) or the number of grid-cells occupied. No data were available for Lycopodium sp., Drepanocladus vernicosus, Leucobryum glaucum, Mannia triandra, and Sphagnum sp. Short-term demographic trend (the last 12 years) was available only for 20 plant species, while in the remaining cases it was estimated following an expert-based criterion. This parameter remain unknown for 27 taxa, including bryophytes and vascular species, due to the complete absence of information. Available information highlighted a critical situation in all the biogeographical regions. Only in two cases (Armeria helodes, Erucastrum palustre), both in the continental region, the population size increased over time; on the contrary, the population size decreased for 33 taxa. Such a trend was emphasised in the Mediterranean bioregion, where 37.7% of the known population size was expected in decline, compared to 20.51 and 16.32% in the Continental and Alpine bioregions, respectively. The number of taxa with unknown population trends always showed high percentages, reaching 21.31% in the Mediterranean bioregion, 35.90 in the Continental bioregion and 40.81% in the Alpine bioregion (Table 2).

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Table 2 Population trend of the ﬂora of community interest (FCI) at the biogeographical level deﬁned as improving, stable or declining Biogeographical region Improving Stable Declining Unknown Total

Alpine 0 21 8 20 49 Continental 2 15 8 14 39 Mediterranean 0 25 23 13 61

Main pressures for the Italian plants of community interest

The prevailing pressures (Fig. 2) were related to agriculture and natural system modifications (66.35% of the total plant species), human intrusions and disturbances (56.07%) and natural biotic and abiotic processes (46.73%). Within these main pressure categories, the most critical factors were related to grazing by livestock and human-induced changes in hydraulic conditions (both affecting the 43.92% of the total plant species), followed by outdoor sports and recreational activities (37.71%) and natural biocenotic succession (34.58%). No threat was reported for four plant species (Riccia breidleri, Campanula zoysii, Saxifraga florulenta, and Herniaria latifolia subsp. litardierei), the first three located in the Alpine bioregion and the latter in the Mediterranean bioregion. At the biogeographic level the same general pattern was confirmed, with only few differences in the Alpine bioregion, where the main pressures were related to natural ecosystem evolution (natural biotic and abiotic processes and natural system modifications

Fig. 2 Main pressures (medium and high intensity) reported for plant species listed in the Habitats Directive (Italian FCI) 123 Biodivers Conserv with 42.86 and 38.77% of the total plants, respectively) followed by the biological resource use (i.e. gathering terrestrial plants) and agriculture (37.73 and 34.69%, respectively). Contrarily to expectations, extremely low impacts were reported for invasive plants and global climate change (11.21% of the total plants). At biogeographical level, invasive plants represented a relevant pressure especially in the Mediterranean bioregion, while they had a lower impact in the other bioregions.

Conservation status (CS) of FCI and relationship between IUCN category

In the third Report, a total of 145 CS assessments were compiled; the results showed a critical situation (Fig. 3): only 34% of CS assessments were favourable, while 50% were unfavourable (40% inadequate plus 10% bad) and 16% unknown (Fig. 3a). It should also be noted that all species in bad CS (and almost all of those in Inadequate CS) are listed in the HD annex II (Fig. 3b). Results highlight a particularly critical situation in the Mediterranean bioregion, with 31 and 8 taxa in Inadequate and Bad CS, respectively; hence, the 65% of plants growing in the Mediterranean bioregion are in unfavourable CS conditions, compared with the 45% and the 36% in the Continental and Alpine regions, respectively (Table 3). The geographical areas with the highest concentration of species with unfavourable (Inadequate plus Bad) CS are located in the Alps and Apennines mountains (in particular Piedmont and Trentino Alto Adige regions), and in Calabria, Sicily and Sardinia (Fig. 4). The comparison between the IUCN and HD assessments shows a strong negative correlation between variables, indicating a worsening of the CS with increased the IUCN risk category (Table 4). This scenario is expected to worsen in the future, because the deteriorating CS of several EN and NT taxa suggest that many of these species are likely to pass into categories of high extinction risk in the next years (Fig. 5).

Fig. 3 Conservation status (CS) of the Italian FCI listed in the Annexes of the Habitats Directive. a CS of the 107 plant taxa listed in all Annexes (calculated on a total of 145 assessments) and b CS of FCI listed in the Annex II of the Habitats Directive 123 Biodivers Conserv

Table 3 Conservation status at biogeographical level of the ﬂora of community interest (FCI) Biogeographical Favourable Unfavourable- Unfavourable-bad Unknown No. region (%) inadequate (%) (%) (%) taxa

Alpine 19 (40.5) 16 (34.0) 1 (2.1) 11 (23.4) 47 Continental 14 (36.9) 11 (28.9) 6 (15.8) 7 (18.4) 38 Mediterranean 16 (26.7) 31 (51.7) 8 (13.3) 5 (8.3) 60

Fig. 4 Density map of the FCI with unfavourable conservation status (inadequate and bad): location on the Italian territory of the areas with the highest density of FCI in unfavourable CS corresponding to the areas in need of more attention for conservation. The boundaries of biogeographical regions and administrative Italian regions were also indicated

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Table 4 Results of correlation analysis between the two ordinal variables (IUCN categories and CS according to the reporting under Article 17 of the HD) based on the Spearman’s Rho and Kendall’s tau-b correlation measures Parameter Value Asymptotic SE Approx. T value p value

Kendall’s Tau coefﬁcient (s) -0.694 0.040 -15.157 0.000 Spearman coefﬁcient (q) -0.774 0.039 -11.784 0.000

N = 95

Fig. 5 Comparison between the IUCN and HD assessments of the Italian FCI

Discussion

The protection of biodiversity is a well-recognised priority for the EU legislation but achieving this ambitious target urgently needs a comprehensive and reliable measure of the status of biodiversity, as well as adequate investments of resources in monitoring and reporting activities (European Commission 2009). The EU is considered to possess one of the most effective intergovernmental biodiversity policy instrument (e.g. Maiorano et al. 2007; Pullin et al. 2009; Beresford et al. 2016), but several criticisms in the interpretation of rules and practical problems (e.g. data acquisition, economic funding, local responsi- bilities) need to be urgently solved. In addition, it must be observed that to reach the goal of favourable CS in those species currently in an inadequate CS, massive ﬁnancial and

123 Biodivers Conserv human resources should be invested, in particular for widespread plants and in countries with high species diversity. Among the European states, Italy hosts a high number of plants of community interest, exceeded only by Spain and Portugal (211 and 188 plants, respectively; see for details: https://circabc.europa.eu/faces/jsp/extension/wai/navigation/container.jsp). In addition, Italian FCI shows a high endemism rate (ca. 50% of the total), which consequently implies an extraordinary national responsibility in preserving this unique heritage. The regional responsibility criterion has been recognised as the main instrument to set priority at the local level (Gauthier et al. 2010; Bacchetta et al. 2012) and, although conservation actions for the FCI is per se mandatory, a complementary national priority list should be created in order to better identify the target species needing urgent conservation measures at the regional level (Bacchetta et al. 2012; Rossi et al. 2014, 2016). Since there have been methodological changes in reporting procedures, it is difficult to evaluate whether the results of the third report highlight a true deterioration/improvement in conditions or reflects procedural differences or knowledge improvements (EEA 2015). However, the third Italian Report reveals an inadequate CS for about half of the FCI, independently of the fact that this worsening situation may originate by advances in assessment methodology, knowledge improvements, or an effective worsening of the CS. Moreover, species classified as ‘‘unknown’’ decreased from 31 to 17%, indicating an increase in knowledge. A similar general pattern was observed for all EU Member States (with the exception of Greece for which no data was available; EEA 2015); considering the remaining 26 member states (https://circabc.europa.eu/faces/jsp/extension/wai/navigation/container.jsp), only Cyprus and Estonia showed a predominance of favourable CS for FCI (100 and 64% of favourable CS, respectively), while the remaining countries predominantly showed negative or unknown CS assessments ([50% of the total plant species). At the biogeographical level, the results for the Italian Mediterranean bioregion are particularly alarming and confirm the general pattern observed at the European level with a particularly high rate of unfavourable and unknown CS assessments (EEA 2015), where, land-use changes, declines in natural and agricultural habitats and increases in urban areas have been reported in the last decades (Falcucci et al. 2007; Pullin et al. 2009). The high percentage of unknown CS reported in 13 states ([20% in Portugal, Italy, Spain, Denmark and UK), highlights the urgency to promote accurate research on FCI at continental level. In fact, in Italy as in other countries there are still information gaps for some plant species of community interest as well as for several parameters requested by the HD. Despite the field efforts in recent years (e.g. Gentili et al. 2010; Fenu et al. 2011, 2015a, b) long-term monitoring data were available only in few cases, while a severe knowledge gap in population size was often detected. In several cases the general population trends and the population size could be extrapolated from the literature or provided by specialists (expert- based judgment), but updated field data are necessary to obtain reliable assessments. However, this requires significant economic resources and qualified personnel specialised in detection methods for different taxa (i.e. researchers and conservation biologists). Another problem with population size is that it can be obtained only for a fraction of FCI. The number of individuals (genet or ramet) may be impossible to be detected in plant species with high clonal reproduction (e.g. Marsilea quadrifolia). At present, as a consequence of the criticisms highlighted by the last report, the EC and the European Envi- ronment Agency are working to develop a methodology revision and improvement. The main pressures affecting Italian FCI are consistent with those identified at European scale: so far the most frequently reported pressures are related to agriculture intensification 123 Biodivers Conserv and modification of natural conditions. In general, human-induced pressures greatly exceed the pressures related to natural factors (EEA 2015). It must be highlighted that this pressures are easily detected also by quite evident signals. Conversely some threatening factors (e.g. climate change, invasive species) have a lower impact and our data are in agreement with global patterns that identify the human-induced change in land use as main threatening factors for global biodiversity (Thuiller 2007). Furthermore, the Italian trend fits with the European situation (EEA 2015), even if at a global level climatic change and alien species are currently considered two of the most alarming drivers of global changes leading to species extinction (Go´mez et al. 2015; Bellard et al. 2016). It’s important to note that effects of climate change and biological invasions may be hardly detectable due to the way and scale of agency of threats themselves and to the lack of reliably risk assessment methods (Kumschick et al. 2015); given that their potential effects may not be yet fully detectable, these phenomena must not be disregarded and their monitoring and analysis are urgently needed (Go´mez et al. 2015; Downey and Richardson 2016). Importantly, the results of the third Italian Report were consistent with the IUCN assessment of the Italian policy vascular plants, 41.9% of which were threatened with extinction (Rossi et al. 2016). This result is in contrast to the discrepancies between the two types of assessment and the more pessimistic scenario depicted by Red Lists at the EU scale (Moser et al. 2016). This lack of correlation is likely due to data heterogeneity. In contrast, both the Italian Red List and HD report lie on data provided by the same large group of botanists, which reduces uncertainties and heterogeneity in the raw data (e.g. distribution, population trends, etc.); it follows that our comparison between Red Lists and HD report is particularly sound.

Conclusions

Although the Italian third report of the HD highlighted an advance of knowledge, demonstrates that a great effort is needed to reach the HD goals of species favourable CS. Indeed no adequate conservation measures have been taken or planned for several priority plants listed in Annex II, despite the EU provides resources and instruments (e.g. LIFE program). Protected areas alone (e.g. Natura 2000 sites, natural parks) do not guarantee the species conservation (Heywood and Iriondo 2003). Although conserving all species in a favourable CS was the ultimate goal of the HD and, therefore, the economic resources should be primarily targeted at the most endangered and/or the poorly known plant species, as a precautionary and urgent action would be to concentrate the conservation activities in the areas richest of plant in unfavourable or unknown CS. However, a priority list of plant species in unfavourable CS should be elaborated to set conservation priorities and, consequently, to allocate resources at European and national levels, as already done in some local contexts (e.g. Sardinia; Bacchetta et al. 2012). Monitoring activities needs to be intensiﬁed and improved in order to overcome information gaps for several plant species, but poor ﬁnancial resources limit the monitoring activity. Additionally, the efforts for widespread taxa (i.e. Ruscus aculeatus, Galanthus nivalis in Italy) may be disproportionate, causing a waste of resources to the disadvantage of highly threatened FCI. Data about threats and pressures must be considered in a realistic and critical way, always relating the estimation of their impact to the real efforts that can be implemented to monitor them. Always keeping track of immediate threatening factors, strengthening monitoring programmes and easy-detectable indicators addressed to the most ‘‘silent’’ and long-term threats could reduce the risk of disregarding important drivers of extinction (i.e. climatic change, biological invasions). 123 Biodivers Conserv

Red list data and assessments emerged as a complementary resource to EU report processes, offering a different rapid metric to evaluate the conservation status of species from a different point of view. In our study, the pressures highlighted by the two evaluation systems are quite congruent, but the evaluation at the biogeographic level and the intensity scale of threats considered in the HD report allow a more realistic analysis. Red list assessments could improve EU judgment, highlighting critical situations deserving more attention. In this sense, the future scenario depicted by the comparison between the results of IUCN and Article 17 assessments indicates a concrete worsening situation with a possible increase in unfavourable CS for many Italian plants of community interest. A positive outcome of the third report was the development of a speciﬁc national project funded by the Ministry of Environment (MATTM), with the ambitious target to set future monitoring activities for FCI and optimize monitoring efforts at national scale. In particular, it aims to develop species-speciﬁc monitoring schemes and methodologies in order to address the requirements of the European reporting system. Standardized data collection method should lead to achieve comparable results and to overcome some current problems related to data heterogeneity and discrepancies from the standards required by the EC and would allow greater repeatability and comparability over time.

Acknowledgements The authors would like to thank all the Italian botanists who provided their unpublished data, expert judgments and general support for the third Italian Report of the Habitats Directive. The authors thank the two anonymous reviewers for their constructive comments that improved the previous versions of the paper.

Appendix

See Table 5.

Table 5 Summary table of the conservation status according to reporting under Article 17 Taxon Conservation status IUCN category

Abies nebrodensis U2 CR Adenophora liliifolia FV NT Adonis distorta U1 EN Anchusa crispa.U1EN Androsace mathildae U1 LC Aquilegia alpina FV LC Aquilegia bertolonii FV NT Armeria helodes U2 EN Arnica montana FV LC Artemisia genipi FV LC Asplenium adulterinum FV LC Aster sorrentinoi U1 VU Astragalus aquilanus.U1EN Astragalus centralpinus FV NT Astragalus maritimus U2 CR Astragalus verrucosus U1 CR Athamanta cortiana U1 CR

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Table 5 continued

Taxon Conservation status IUCN category

Bassia saxicola U1 EN Brassica glabrescens FV NT Brassica insularis FV NT Brassica macrocarpa U1 CR Buxbaumia viridis U1 CR Campanula morettiana FV LC Campanula sabatia U1 VU Campanula zoysii FV LC Carex panormitana U1 EN Centaurea horrida U1 EN Centaurea kartschiana U1 LC Cladonia U1 EN Crambe tataria U1 NT Crocus etruscus FV NT Cypripedium calceolus FV LC Cytisus aeolicus U1 EN Daphne petraea FV LC Dianthus rupicola FV LC Dicranum viride U1 EN Dracocephalum austriacum U1 EN Drepanocladus vernicosus XX DD Eleocharis carniolica U1 EN Erucastrum palustre U2 EN Eryngium alpinum U2 EN Euphrasia genargentea U1 CR Euphrasia marchesettii U1 EN Galanthus nivalis FV LC Galium litorale U1 NT Genista holopetala FV NT Gentiana ligustica FV LC Gentiana lutea FV NT Gladiolus palustris U1 NT Gypsophila papillosa XX EN Helianthemum caput-felis U1 CR Herniaria latifolia FV LC Himantoglossum adriaticum U1 LC Iris marsica FV NT Isoetes malinverniana U2 CR Jonopsidium savianum FV LC Kosteletzkya pentacarpos U1 CR Lamyropsis microcephala U2 CR Leontodon siculus FV NT Leucobryum glaucum XX DD

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Table 5 continued

Taxon Conservation status IUCN category

Leucojum nicaeense U2 CR Lilium rubrum XX EN Limonium insulare U1 EN Limonium pseudolaetum U1 VU Limonium strictissimum U1 VU Linaria flava U1 EN Linaria pseudolaxiflora U1 NT Linaria tonzigii XX NT Lindernia procumbens XX DD Linum mulleri U1 EN Liparis loeselii U2 EN Lycopodium XX LC Mannia triandra XX DD Marsilea quadrifolia U2 EN Marsilea strigosa U1 LC Moehringia tommasinii U1 NT Muscari gussonei U1 EN Ophrys lunulata FV LC Orthotrichum rogeri U1 EN Paeonia officinalis FV VU Petagnia saniculifolia U1 EN Petalophyllum ralfsii U2 CR Physoplexis comosa FV LC Primula apennina FV LC Primula glaucescens FV LC Primula palinuri U1 VU Primula spectabilis FV LC Ribes sardoum U2 CR Riccia breidleri U1 EN Rouya polygama U1 EN Ruscus aculeatus FV LC Salicornia veneta FV LC Saxifraga berica XX NT Saxifraga florulenta FV VU Saxifraga presolanensis FV NT Saxifraga tombeanensis U1 EN Saxifraga valdensis XX DD Scapania massalongi U1 CR Silene hicesiae U1 CR Silene velutina FV NT Sphagnum XX DD Spiranthes aestivalis U1 EN Stipa austroitalica FV LC

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Table 5 continued

Taxon Conservation status IUCN category

Stipa veneta U2 EN Trichomanes speciosum U2 CR Trifolium saxatile XX EN Woodwardia radicans U1 EN FV Favourable, U1 unfavourable–inadequate, U2 unfavourable–bad, XX unknown) and the IUCN risk category (data from Rossi et al. 2016) of the Italian FCI. For few taxa with different CS in the biogeographical regions, the worst CS was chosen based on the precautionary principle

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