Assessing the Global Conservation Status of the Rock Rose Helianthemum Caput-Felis

Assessing the global conservation status of the rock rose Helianthemum caput-felis

E LENA S ULIS,GIANLUIGI B ACCHETTA,DONATELLA C OGONI D OMENICO G ARGANO and G IUSEPPE F ENU

Abstract The assessment of the conservation status of a Introduction species is the first step in developing a conservation strategy. IUCN Red Lists assessments are an important starting point pecies face numerous threats, principally related to for conservation actions and the most commonly applied Shuman activities, and biodiversity continues to be lost   method for assessing the extinction risk of a species. In (Pimm et al., ; Butchart et al., ; Ceballos et al.,  this study, the global conservation status of the rock rose ). Halting, or at least significantly reducing, the loss of Helianthemum caput-felis Boiss. (Cistaceae), a perennial biodiversity requires adequate investment and a compre- Mediterranean plant, was evaluated using the Red List hensive and reliable measure of conservation status (e.g.   criteria. The distribution of the species was determined by Balmford et al., ; Fenu et al., ; Orsenigo et al.,  monitoring historical localities and all other suitable sites ). Target II of Objective I of the Global Strategy for – along the western Mediterranean coasts for  years. For Plant Conservation of the Convention on  each confirmed locality, the ecological and population para- Biological Diversity (CBD; GSPC, ) is the preliminary ’ meters and the main threats were recorded; these data were assessment of the conservation status of the Earth s flora. used in a quantitative analysis of the species’ extinction risk. Evaluation of species conservation status is required ’ Our findings indicate there have been several recent extinc- not only to evaluate progress towards the CBD sAichi – tions, and there is a continuing decline in the species’ area Targets of the Strategic Plan for Biodiversity  of occurrence, habitat quality and number of reproductive (Pimm et al., ) but also to identify and develop effect-  plants. The main threats are related to human activities. ive conservation strategies (Rodrigues et al., ; Mace    Extinction models indicate a probability of quasi-extinction et al., ;Fenuetal., a; Rossi et al., ;Collen   risk of c. % in five generations or c. % in three genera- et al., ; Orsenigo et al., ). The IUCN Red List   tions, with the species likely to become extinct in seven cur- criteria (IUCN, , a) are the accepted standard rently known localities within the next  years. Application for assessing the extinction risk of species (Rodrigues    of the Red List criteria indicates H. caput-felis should be ca- et al., ; Mace et al., ; Collen et al., ;  tegorized as Endangered. This study confirms that legal pro- Orsenigo et al., ).   tection and passive conservation measures are insufficient Habitat Directive / /EEC is the core strategy for na-  to guarantee the persistence of a plant species. Active con- ture conservation in Europe (Balmford et al., ; Pullin    servation and management actions are needed to protect et al., ; Beresford et al., ; Fenu et al., ). this and other threatened species of the Mediterranean Through the implementation of cogent conservation pol- Basin. icies, the Directive promotes the maintenance of a favour- able conservation status for a group of key species and Keywords Cistaceae, conservation status, extinction risk, habitats (European Commission, ; Rossi et al., ; Helianthemum caput-felis, IUCN Red List, Mediterranean Fenu et al., ). It is mandatory for EU member states flora, rock rose, threatened plant that have full responsibility for their conservation efforts Supplementary material for this article is available at to monitor and report the conservation status of all species  https://doi.org/./S listed in the Directive (European Commission, ; Rossi et al., ; Fenu et al., ). One of the key species listed in the Habitat Directive is the rock rose Helianthemum caput-felis Boiss. (Cistaceae), which is protected by several international, national and regional regulations. Helianthemum caput-felis is a ther- ELENA SULIS,GIANLUIGI BACCHETTA,DONATELLA COGONI (Corresponding author, orcid.org/0000-0003-0937-196X) and GIUSEPPE FENU ( orcid.org/0000- mophilous long-lived half shrub that grows in coastal 0003-4762-5043) Dipartimento di Scienze della Vita e dell’Ambiente, Centro environments under the direct influence of the sea, mostly Conservazione Biodiversità, Università degli Studi di Cagliari, Cagliari, Italy E-mail [email protected] on calcareous rocky cliffs with garrigues or scrublands; some populations grow on sand dunes in Majorca, fossil DOMENICO GARGANO Dipartimento di Biologia, Ecologia e Scienze della Terra, Università della Calabria, Arcavacata, Italy dunes in Morocco and rocky slopes bordering inland  Received  May . Revision requested  August . ravines (Fenu et al., b). The species occurs in several Accepted  November . First published online  November . disjunct and fragmented populations throughout the coasts

Oryx, 2020, 54(2), 197–205 © 2019 Fauna & Flora International doi:10.1017/S0030605318001424 Downloaded from https://www.cambridge.org/core. IP address: 170.106.40.40, on 28 Sep 2021 at 15:31:52, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001424 198 E. Sulis et al.

of the western Mediterranean Basin (south-east Iberian size (sensu IUCN, ) was estimated as d × A × p, where Peninsula, Balearic Islands, Sardinia and north-west Africa; d is an estimate of density within the sampled plots, A is Fenu et al., b and references therein). The global conser- an estimate of the area occupied by the population, and p vation status of H. caput-felis was previously unknown is an estimate of the proportion of mature individuals within because only regional or local assessments were available, the sampled plots. Populations were categorized in three size and there was little information on the species distribution classes, defined a priori as small (,  individuals), me- and conservation status in Africa. Helianthemum caput-felis dium (–,) and large (. ,). The presence or ab- is categorized as Endangered in Europe (Bilz et al., ) and sence of seedlings was also recorded in each locality by Spain (Agulló et al., ), and as Critically Endangered in surveying the population several times during the recruit- Italy (Fenu et al., b) and Algeria (Agulló et al., ). In ment season. Demographic data were collected on  per- addition, according to the European Habitat Directive manent plots in six populations across the species range H. caput-felis has an inadequate conservation status in that were representative of the range of ecological conditions Italy (Fenu et al., ). in which the plant grows (Table ; Sulis et al., ). In each Here, to help establish a conservation plan for H. caput- population, after excluding areas with marginal conditions felis, we evaluated the species’ global conservation status for the species, permanent plots ( ×  m) were placed ran- using the Red List criteria. We aimed to: () describe the domly in the area where the species was found; within the species’ range based on extensive field surveys, () quantify plots all plants present (a total of  in the  plots in the the size and structure of populations, () identify the main first census) were marked, mapped and monitored over a threats to the species’ persistence, () assess the species’ -year period. global conservation status, and () recommend appropriate conservation measures. Data analysis

Methods To assess the extinction risk of H. caput-felis we used the Red List criteria (IUCN, ) and the guidelines for their Data collection application (IUCN, ), considering the criteria A, B and E. To determine whether H. caput-felis fulfilled criterion A The geographical distribution of H. caput-felis was deter- we assessed any potential population reduction (observed, mined through field surveys during – in all estimated or inferred) in the last  years or three genera- localities for which there were herbarium specimens or tions, based on the area of occupancy (AOO; the area within database records (Supplementary Table ) and/or published the extent of occurrence occupied by the taxon, see below; data (Agulló et al., ; Fenu et al., b; Sulis, ). IUCN, ). Additionally, all sites along the coasts of Sardinia, the To apply criterion B, the extent of occurrence (EOO; the Balearic Islands and the Mediterranean coasts of Spain and area contained within the shortest continuous imaginary Morocco with suitable ecological conditions for the species boundary that could be drawn to encompass all known were surveyed. No surveys were made on the Algerian sites of occurrence of a taxon, excluding cases of vagrancy) coast, for which information was obtained from Agulló and the AOO were calculated from the distribution records. et al. (). Extinctions that predated  were excluded from these cal- In each locality where occurrence of the species was con- culations. To estimate EOO, the minimum convex polygon firmed or discovered, the following analyses were under- that included all the occurrences was drawn (IUCN, ), taken. The geographical limits of confirmed localities were with unsuitable areas excluded by deriving the correspond- mapped and their area estimated using ArcGis . (Esri, ent α-hull using the Delauney triangulation (Burgman & Redlands, USA). Localities separated by .  km were con- Fox, ; Gargano et al., ; IUCN, ). The AOO sidered to be geographically separate. At each locality the was calculated by generating a  ×  km grid with ArcGis. altitudinal range, slope, aspect and habitat type according To apply criterion E the estimated quasi-extinction risks to the Habitat Directive were determined. Major threats of populations were calculated based on a demographic to H. caput-felis were identified through field observations study that used both an integral projection model and a (except for Algerian localities), and categorized following matrix population model (Sulis, ; Sulis et al., ; the IUCN Threats Classification Scheme (IUCN, b). Supplementary Material ). The matrix projection model Where possible, population size was determined by a dir- was used to calculate the estimated quasi-extinction risk ect count of the total number of mature plants. In extensive using the popbio package (Stubben & Milligan, )in localities, population size was estimated from a count of all R .. (R Core Team, ). The mean generation time  individuals in – plots (each plot was  m ; the number of (T) extracted from the integral projection model was . plots depended on the location); in these cases population years ( generations = . years) and the mean value

00 42,197 54(2), 2020, , TABLE 1 Localities of Helianthemum caput-felis surveyed in this study, with altitudinal range, area, mean density ± SD, population size, whether seedlings were present, protection status, https://www.cambridge.org/core current status, source and the main threats (IUCN, b). Localities in bold are those selected for study of detailed population dynamics (Sulis et al., ).

Country, Altitudinal Area Mean density ± Population Seedlings Current No. region Locality (municipality) range (m) (ha) SD (plants/m2) size1 present Protection2 status Source Threats – 205 Italy © . – C https://doi.org/10.1017/S0030605318001424 1 Sardinia Is Arutas (Cabras) 5 15 0.001 Small No None Confirmed This study 4.1, 6.1, 8.1, 09Fua&FoaItrainldoi:10.1017/S0030605318001424 International Flora & Fauna 2019 9.4 2 Sardinia Su Tingiosu–Porto Suedda 5–25 12.743 4.8 ± 2.42 LargeE Yes None Confirmed This study 2.1; 2.2; 3.2;

. IPaddress: (Cabras) 6.1; 8.1; 10.3 3 Sardinia Seu (Cabras) None Extinct This study 4 Sardinia Capo Mannu (San Vero Milis)5–55 17.868 4.6 ± 2.25 LargeE Yes SCI Confirmed This study 2.1; 2.2; 6.1;

170.106.40.40 8.1; 10.3 Spain 5 Majorca Punta es Bauç (Santanyí) 8–10 0.012 SmallC No SCI Confirmed This study 6.1 6 Majorca Colònia de Sant Jordi–Playa del 3–8 5.533 1.6 ± 0.74 LargeE No SCI* Confirmed This study 1.1; 1.3; 6.1; , on Puerto (Ses Salines) 9.4

28 Sep2021 at15:31:52 7 Majorca Colònia de Sant Jordi–Es Trenc 2–4 0.493 3.0 ± 1.41 LargeE Yes SCI Confirmed This study 6.1 (Ses Salines) 8 Majorca Sa Ràpita–backdune (Campos)2–10 10.495 7.8 ± 5.57 LargeE Yes SCI Confirmed This study 6.1 9 Majorca Sa Ràpita–nautical club 3–6 0.416 9.6 ± 1.85 LargeE Yes None Confirmed This study 1.1; 2.1; 4.1; (Campos) 6.1; 8.1 10 Majorca Cap Blanc (Llucmajor) 90–110 101.359 2.5 ± 1.14 LargeE Yes SCI Confirmed This study 4.1; 10.3

, subjectto theCambridgeCore termsofuse,available at 11 Majorca Cala Pi (Llucmajor) 15–20 0.120 SmallC No SCI Confirmed This study 1.1; 1.3; 4.1; 6.1 12 Majorca Maioris (Llucmajor) Not This study retrieved 13 Ibiza Cala Conta (San José) Not This study retrieved 14 Alicante Cap d’Or (Teulada) 40–50 0.210 SmallC No SCI* Confirmed This study 15 Alicante Cala del Portitxolet (Teulada) 9–14 1.038 1.4 ± 0.86 LargeE No PMR* Confirmed This study 1.1; 1.3; 4.1; 6.1; 8.1 rose Rock 16 Alicante L’Andragó–Les Platgetes 6–12 0.166 1.4 ± 0.54 MediumC No None Confirmed This study 1.1; 1.3; 4.1; (Teulada) 6.1 – ± E

17 Alicante Cala els Pinets, Cala Lobella, Cala 10 20 2.203 2.9 0.74 Large Yes SCI* Confirmed This study 6.1 caput Helianthemum de l’Advocat (Benissa) 18 Alicante Cala Fustera (Benissa) 7–11 0.182 1.2 ± 0.57 MediumE No SCI, PMR Confirmed This study 1.1; 6.1; 10.3 19 Alicante Cala de les Bassetes (Benissa) 6–20 0.969 2.8 ± 1.04 LargeE Yes SCI, PMR Confirmed This study 1.1; 6.1 20 Alicante La Caleta (Calpe) 6–10 0.129 1.5 ± 0.79 MediumC Yes SCI*, PMR Confirmed This study 1.1 21 Alicante Calpe (Calpe) 5–10 0.084 3.0 ± 1.37 MediumC Yes SCI* Confirmed This study 1.3; 6.1; 8.1 22 Alicante Cabo de Santa Pola (Santa Pola) Extinct Serra et al. (2000); this - study felis 199 https://www.cambridge.org/core/terms Downloaded from 0 .Slse al. et Sulis E. 200

Table 1 (Cont.) https://www.cambridge.org/core Country, Altitudinal Area Mean density ± Population Seedlings Current No. region Locality (municipality) range (m) (ha) SD (plants/m2) size1 present Protection2 status Source Threats 23 Alicante Cabo Cervera (Torrevieja) 5–14 1.676 1.1 ± 0.65 LargeE No None Confirmed This study 1.1; 1.3; 4.1; 6.1; 8.1; 10.3 24 Alicante Torrevieja (Torrevieja) 2–3 0.039 1.4 ± 0.82 MediumC No None Confirmed This study 1.1; 1.3; 6.1; . https://doi.org/10.1017/S0030605318001424 8.1; 9.4 25 Alicante Cala Mosca and Punta Prima 2–18 9.723 1.8 ± 0.34 LargeE Yes None Confirmed This study 6.1; 8.1 (Orihuela) . IPaddress: 26 Alicante Rambla de las Estacas–Cala de 1–10 0.282 SmallC No SCI* Confirmed This study 1.1; 8.1 las Estacas (Orihuela) 27 Alicante Barranco de la Cala del Capitan 15–20 0.067 SmallC No None Confirmed This study 1.1; 1.3; 2.2; 170.106.40.40 (Orihuela) 8.1; 9.4 28 Alicante Casa de Los Leoncios (Orihuela) 15–20 0.381 SmallC No SCI* Confirmed This study 1.1; 2.2; 6.1 29 Alicante Cala Mosca–Playa Flamenca 1–9 9.723 2.0 ± 0.50 LargeE Yes PMR* Confirmed This study 1.1; 1.3; 4.1;

, on (Orihuela) 6.1; 8.1; 10.3 30 Alicante Cabo Roig (Orihuela)3–7 0.906 3.5 ± 1.67 LargeE No None Confirmed This study 1.1; 1.3; 6.1; 28 Sep2021 at15:31:52 10.3 31 Alicante Punta de la Glea (Orihuela) 5–17 4.179 3.1 ± 3.53 LargeE Yes PMR Confirmed This study 1.1; 1.3; 4.1; Oryx 6.1 00 42,197 54(2), 2020, , 32 Alicante Dehesa de Campoamor 5–10 0.117 1.5 ± 0.20 MediumC No None Confirmed This study 1.1; 1.3; 6.1; (Orihuela) 8.1; 10.3 33 Alicante Mil Palmeras (Pilar de la 3–7 1.178 7.7 ± 1.53 LargeE No None Confirmed This study 1.1; 1.3; 6.1; , subjectto theCambridgeCore termsofuse,available at Horadada) 8.1 – ± E – 34 Alicante Río Mar (Pilar de la Horadada) 1 5 1.377 3.7 1.53 Large No None Confirmed This study 1.1; 1.3; 6.1 205 35 Nador Barranco del Quemadero 100–110 36.908 2.4 ± 1.56 LargeE Yes SCI Confirmed This study 2.2 ©

09Fua&FoaItrainldoi:10.1017/S0030605318001424 International Flora & Fauna 2019 (Melilla) 36 Nador Barranco del Nano (Melilla) 85–110 24.630 3.2 ± 1.04 LargeE Yes SCI Confirmed This study Morocco 37 Nador Near Beni Chiker (Beni Chiker) 130–150 0.082 SmallC No None Confirmed This study 2.2; 3.2; 9.4 38 Nador Taxdirt–Cabo de Tres Forcas 100–210 115.639 3.2 ± 1.56 LargeE Yes None Confirmed This study 2.2; 3.2 (Beni Chiker) 39 Nador Near Beni Sidel (Beni Sidel) 180–200 0.142 SmallC No None Confirmed This study 2.2; 8.1 40 Nador Road to Cap de Trois Fourches 180–220 0.150 1.3 ± 0.70 MediumE Yes None Confirmed This study 4.1; 8.1 (Cap de Trois Fourches) 41 Nador Douar Ighzar-n-Yamrabthan 42–67 0.090 1.5 ± 1.10 MediumE Yes None Confirmed This study (Douar Ighzar-n-Yamrabthan) 42 Nador Duar Izzemmouren (Ras 40–50 4.211 2.3 ± 1.20 LargeE Yes None Confirmed This study 2.2; 2.3 Kebdana) 43 Nador Ras El Má (Ras Kebdana) 35–52 3.686 2.3 ± 1.01 LargeE No None Confirmed This study 2.2; 9.4 44 Nador Near Hidoun (Hidoun) Not This study retrieved 45 Nador Târia n Tît (Charrana) 30–52 0.540 SmallC No None Confirmed This study Rock rose Helianthemum caput-felis 201

extracted from the matrix projection model was . years ( generations = . years; Sulis, ). Following the precautionary principle (IUCN, ), the smaller value of gen-

1.1; 1.3; 2.3; 6.1; 8.1; 9.4 eration length (i.e. . years) was retained. Extinction risk was calculated considering three alternative assessments ( ) population. 

 years or three generations, years or five generations, and ,  ) ) ) )  years). Quasi-extinction probabilities were calculated . by  model iterations (van der Meer et al., ). 2017 2017 2017 2017 ( ( ( ( Matrices were selected at random with replacement (each

) or large ( matrix had an equal probability of selection; Morris &   

, Doak, ). A quasi-extinction threshold of individuals  – was designated a priori, to help minimize the demographic  Extinct Agulló et al. Extinct Agulló et al. Current statusExtinct Source Agulló et al. Threats stochasticity associated with small population size (Morris 2 & Doak, ). We also modelled three separate scenarios, one for each population size class, to examine extinction risk. We developed None Confirmed Agulló et al. each model using the global stochastic growth rate (λs=; Sulis, ;Sulisetal.,) and the effective population size. individuals), medium ( 

, Results Seedlings present Protection We located records of H. caput-felis in  localities along the western Mediterranean coasts, mainly in Spain ( localities, C

1 including two in Melilla), followed by Morocco (nine local-

Population size ities), Italy and Algeria (four localities in each country;  

) Table ). We confirmed the presence of H. caput-felis in ± 2 localities,  of which we verified in the field, and one of which was documented in Agulló et al. (; no.  in Table ). In two localities on the Balearic Islands (Cala Conta in Ibiza, Maioris in Majorca) and one in Morocco Mean density SD (plants/m

); *protection only partially covers the population area. (near Hidoun, Nador), field surveys carried out by ourselves and other researchers failed to locate the species. Following  a precautionary approach, we reported the species as ‘not re- Area (ha) trieved’ in these localities. We were, however, able to confirm recent extinctions at two localities in Europe (Santa Pola in Spain, Seu in Italy) and three localities in Algeria.

80 All sites where occurrence was confirmed are in coastal –

Altitudinal range (m) environments, with the exception of one population in Morocco that is . km from the coast. The altitudinal range at which we located the species was – m. In Europe, we found the plant below  m, whereas in North Africa the species occurred in some cases above  m. The slope of localities is –°. The area occupied  by the species in each locality was variable, from  m at Is Arutas in Sardinia to  and  ha at Taxdirt and Cap Blanc, respectively. Mean plant density was . ± SD .   plants/m , varying from . ± SD . plants/m (Cabo  Cervera, Alicante) to . ± SD . plants/m (Sa Ràpita, Majorca). Population size ranged from a few mature plants

.) (Is Arutas, Cabras) to more than tens of thousands (Cap Blanc, Llucmajor). More than half of localities (.%) had Cont a population size . , mature plants. The population Country, region Locality (municipality) size was #  individuals in .% of localities. The popu- SCI, Site of community importance; PMR, Plant micro-reserve sensu Laguna et al. ( Determined by counting (superscript C) or estimating (superscript E) the total number of mature plants and categorizing as small ( 49 Oran Aïn-El-Kerma (Oran) 170 Small 48 Oran Aïn-El-Turk (Aïn-El-Turk) 75 No. 47 Oran Cap Falcon (Aïn-El-Turk) 50 Algeria 46 Oran Cabo Lindlés (Aïn-El-Turk) 90 Table 1 (   lation structure was mainly characterized by reproductive

FIG. 1 Number of localities subject to each of the main threats (Table ) to the rock rose Helianthemum caput-felis populations; data for Algeria was obtained from Agulló et al. ().

(i.e. Carpobrotus sp., Agave sp., Acacia sp. and Ricinus com- munis L.; .%), roads and railroads (.%), wood and pulp plantations (.%), and the presence of rubbish (IUCN threat classification ‘garbage and solid waste’; .%). In .% of localities, all in Europe, avalanches or landslides appear to threaten the persistence of H. caput- felis (Fig. , Table ). According to the generation time extracted from the integral projection model, there was no extinction risk for three generations (Fig. ), but there was an extinction probability of c. % for a five generation period (. years; Fig. ). Considering the generation time extracted from the matrix population model, the length of three generations was . years, which corresponded to a quasi-extinction risk of c. %(Fig. ). The quasi-extinction risk models for the three population size classes, considering each locality to be isolated, FIG. 2 Simulated cumulative distribution functions of the showed that seven small populations (,  plants) are likely number of years for populations of H. caput-felis to reach a to become extinct within the next  years, small popula- quasi-extinction threshold of  individuals: a, three generations tions with ,  individuals had a quasi-risk extinction (integral projection model); b, five generations (integral   projection model); c, three generations based on generation time probability of %in years, and medium populations from the matrix population model. The lines are separate had quasi-extinction probabilities of  and %in estimates of the cumulative distribution of extinction and  years, respectively. Only large populations (. , probabilities based on  iterations of population growth over individuals) are not at risk of extinction.  years (see Stubben & Milligan,  for further details).

Conservation status assessment and juvenile plants (. %). Despite repeated surveys in the recruitment season, we observed seedlings in only .% Considering the mean distance between localities ( km) of localities, with recruitment absent in all small popula- and the results of the Delauney triangulation, the current tions and in the .% of medium and large populations EOO of H. caput-felis, including all confirmed localities, is   (Table ). , km (Fig. ), and the AOO is  km (  ×  km The main threats affecting the persistence of H. caput- cells). Since  the extinction of H. caput-felis has been felis populations are related to human activities (Fig. ), documented in five localities (Table ). However, the reduction including recreational activities (i.e. disturbance effects in EOO was negligible (.%) because these localities were posed by recreation; .% of localities), housing and within the convex polygon or close to the edge. However, AOO  urban areas (.%) and tourism and recreation (i.e. habi- decreased by three cells ( km ), which gave a decline .% tat effects of tourism and recreation sites with a substantial since .Suchvaluesdonotreachtheminimumthreshold footprint; .%). Other threats were invasive alien species for threatened taxa under Red List criterion A.

our research presented here is the first global assessment of the range and conservation status of H. caput-felis. The distribution of H. caput-felis is concentrated in the westernmost Mediterranean Basin along the eastern Iberian coasts, reaching its easternmost limit in Su Tingiosu (Italy), northernmost in Capo Mannu (Italy), westernmost in Beni Chiker and southernmost in Beni Sidel (both in Morocco). The status of the species in North Africa remains unclear, however. In three Algerian localities where occurrence was documented by recent herbarium specimens Agulló et al. () were unable to confirm presence but did locate the species in a previously undocu- FIG. 3 Extent of Occurrence (EOO) calculated for H. caput-felis. mented locality. The species’ status also requires clarifica- tion in Morocco, where we could not confirm presence in Under Red List criterion B the species distribution has one previously documented locality. Considering that this ‘ ’  severe fragmentation (sensu IUCN, ). Our quantita- species can grow in locations that may be difficult to explore  tive models indicate c. % of confirmed localities (eight (e.g. vertical coastal cliffs, sandy and fossil dunes, inland  medium and small populations) are below the viability ravines), additional surveys are needed. threshold and therefore could be prone to extinction, close Our global assessment of H. caput-felis as Endangered is  ‘ ’ to the % threshold for severe fragmentation . The Red List consistent with previous regional assessments (Agulló et al., guidelines recommend integrating this evaluation with a , ; Bilz et al., ; Fenu et al., b; Rossi et al., ’ species biological traits, in particular dispersal ability. A ) based only on distribution data (i.e. criterion B). population genetic study in the Alicante (the core of the Assessments based on geographical data are the most com- species range, on the Iberian Peninsula), Melilla (North mon for plants, because distribution data are the easiest to ob- Africa) and Balearic Islands localities, indicated significant tain. However, our integration of criteria B and E provides a genetic divergence, which would indicate genetic isolation more complete conservation assessment. In addition, the ab- and limited gene flow among these populations (Agulló sence of seedling recruitment and the high juvenile mortality  et al., ), suggesting that localities separated by longer rate recorded in several localities were further negative indica- distances (i.e. those in Algeria and Sardinia) may be func- tors (Sulis, ;Sulisetal.,). The null or limited recruit- tionally isolated. Taken together, these findings suggest ment rate in some populations could be partially explained the species is severely fragmented. Helianthemum caput- by the effect of drought during – in eastern Spain felis could therefore be categorized as Endangered based (García de la Serrana et al., ;Laguna&Ferrer,).   on B ab(ii, iii, iv, v); i.e. its small AOO ( ), highly fragmen- A combination of some recent extinction events and the ted distribution (a) and calculated/observed decline (b) in fact that we were unable to relocate the species at some pre- AOO (ii), habitat quality (iii), number of localities (iv) viously documented locations indicates that the AOO of H. and number of mature plants (v). caput-felis is contracting, probably as a result of continuing Helianthemum caput-felis could also be categorized as loss of habitat quality and reproductive individuals. Habitat Endangered under criterion E as a result of a quasi-extinction reduction and degradation appear to be mainly a result of    risk probability of c. % in five generations ( . years based the expansion of infrastructure, a key element in biodi-  on the integral projection model) and c. %inthreegenera- versity loss (e.g. Newbold et al., ). In particular, as   tions ( . years based on the matrix population model). described for several Mediterranean plant species (e.g. Fenu et al., ; Ballantyne & Pickering, ; Fois et al.,   Discussion ; Orsenigo et al., ), the main threats to H. caput-felis are related to the degradation of the species’ habitat from Although many countries are contracting parties to inter- tourism and recreational activities and the expansion of national conventions and other international regulations, such housing and urban areas. Both the Spanish (Giménez as the European Habitat Directive, that encourage monitor- et al., ; Agulló et al., ; Marco et al., , ; ing and protection of wild flora, global protection remains Zaragozí et al., ) and Algerian (Agulló et al., ) coasts insufficient, with c. % of known vascular plant species threa- have experienced extensive urban development linked to tened with extinction (Royal Botanic Gardens, ). Moreover, tourism. We did not find that climate change, although a the number of global species assessments, as required by the major driver of species extinctions (Gómez et al., ; targets of the Global Strategy for Plant Conservation and the Fenu et al., ; Orsenigo et al., ), is a threat to H. CBD, is low, and such assessments particularly challenging caput-felis but this could be because of the difficulty of de- when a species occurs in several countries. We believe that tecting its effects (Fenu et al., ). However, the long-term

consequences of climate change, especially drought or ir- AGULLÓ, J.C., JUAN, A., ALONSO, M.Á. & CRESPO, M.B. () regular rainfall, need to be considered for coastal plants Helianthemum caput-felis Boiss. In Atlas y Libro Rojo de la Flora  such as H. caput-felis (García de la Serrana et al., ; Vascular Amenazada de España. Adenda . Dirección General de  Medio Natural y Política Forestal (Ministerio de Medio Ambiente, Laguna & Ferrer, ). y Medio Rural y Marino)—Sociedad Española de Biología de la Although several populations of H. caput-felis (c. %of Conservación de Plantas (eds Á. Bañares, G. Blanca, J. Güemes, all localities and c. .% of those in Europe) are currently J.C. Moreno & S. Ortiz), pp. –. Ministerio de Medio Ambiente, protected (i.e. within a Site of community importance and/ y Medio Rural y Marino, y Sociedad Española de Biología de la or Plant micro-reserve), our findings nevertheless indicate Conservación de Plantas, Madrid, Spain. AGULLÓ, J.C., JUAN, A., CRESPO, M.B., ALONSO, M.Á. & TERRONES, that H. caput-felis faces a substantial risk of extinction A. () An updated report on the distribution and conservation over the short to medium term in the absence of additional status of the Endangered cat’s head rockrose Helianthemum management actions. As demonstrated for other species caput-felis (Magnoliopsida: Violales: Cistaceae) in Algeria. Journal (e.g. Aguilella et al., ; Rossi et al., ; Fenu et al., of Threatened Taxa, , –. ), our data indicate that current legal protection and pas- AGULLÓ, J.C., JUAN, A., GUILLÓ, A., ALONSO, M.Á. & CRESPO, M.B. () Genetic diversity and phylogeographical assessment of sive conservation measures are insufficient to guarantee the Helianthemum caput-felis Boiss. (Cistaceae) based on AFLP persistence of H. caput-felis. This is contrary to EU legislation, markers. Fitosociologia, , –. which states that conservation of this species is mandatory BALLANTYNE,M.&PICKERING, C.M. () Tourism and recreation: and that member states are responsible for its conservation. a common threat to IUCN red-listed vascular plants in Europe.  – Helianthemum caput-felis requires a transnational con- Biodiversity and Conservation, , . BALMFORD, A., BENNUN, L., TEN BRINK, B., COOPER,D,CÔTÉ, I.M, servation strategy focusing on protection of each locality CRANE,P.etal.() The Convention on Biological Diversity’s in which it occurs, to avoid further decline or extinctions,  target. Science, , –. habitat restoration in degraded localities, mainly in Spain BERESFORD, A.E., BUCHANAN, G.M., SANDERSON, F.J., JEFFERSON,R. and Algeria, and reduction of the impacts of recreational ac- &DONALD,P.F.() The contributions of the EU nature tivities and urban sprawl. Furthermore, as already underway directives to the CBD and other multilateral environmental  – in Melilla (M. Tapia, pers. comm.), translocations could be agreements. Conservation Letters, , . BILZ, M., KELL, S.P., MAXTED,N.&LANSDOWN, R.V. () European carried out in suitable areas and reintroductions at sites Red List of Vascular Plants. Publications Office of the European from which the species has recently disappeared. Previous Union, Luxembourg, Luxembourg. experiences with threatened Mediterranean coastal plants BURGMAN, M.A. & FOX, J.C. () Bias in species range estimates have demonstrated that these activities would be low-cost from minimum convex polygons: implications for conservation and  – projects with good chance of success (e.g. Cogoni et al., options for improved planning. Animal Conservation, , . BUTCHART, S.H.M., WALPOLE, M., COLLEN, B., VAN STRIEN, A., ; Fenu et al., ; Laguna et al., ). Finally, monitor- SCHARLEMANN, J.P.W., ALMOND, R.E.A. et al. () Global ing is required of all known localities in which the species biodiversity: indicators of recent declines. Science, , –. persists. Although it could be challenging to sustain long- CEBALLOS, G., EHRLICH, P.R., BARNOSKY, A.D., GARCÍA, A., term monitoring, it is fundamental for assessment of con- PRINGLE, R.M. & PALMER, T.M. () Accelerated modern servation status and for effective local conservation. human-induced species losses: entering the sixth mass extinction. Science Advances, ,e.  Acknowledgements We thank Sergio Sulis, Iván Ramos Torrens COGONI, D., FENU, G., CONCAS,E.&BACCHETTA,G.( ) and Eva Moragues Botey (Servicio de Protección de Especies de la The effectiveness of plant conservation measures: the Dianthus  – Consejería de Medio Ambiente, Agricultura y Pesca de las Islas morisianus reintroduction. Oryx, , . Baleares), Jaime Güemes (Jardín Botánico Valencia), Manuel Tapia COLLEN, B., DULVY,N.K.,GASTON,K.J.,GÄRDENFORS,U.,KEITH,  Claro (Guelaya-Ecologistas en Acción Melilla) and Jaime X. Soler for D.A., P UNT,A.E.etal.( ) Clarifying misconceptions of extinction   their help with fieldwork, and the anonymous reviewers and the Editor risk assessment with the IUCN Red List. Biological Letters , .     for their constructive comments. EUROPEAN COMMISSION ( ) Council Directive / /EEC of May  on the Conservation of Natural Habitats and of Wild Fauna and Author contributions Conception, design, drafting text: ES, GF; Flora. The Council of the European Communities, Brussels, Data collection: GB, DC, GF; data analysis: ES, DC, GD, GF; finalizing Belgium. text: all authors. FENU, G., BACCHETTA, G., GIACANELLI, V., GARGANO, D., MONTAGNANI, C., ORSENIGO, S. et al. () Conserving plant Conflicts of interest None. diversity in Europe: outcomes, criticisms and perspectives of the Habitats Directive application in Italy. Biodiversity and  – Ethical standards This research abided by the Oryx guidelines on Conservation , .  ethical standards. FENU, G., COGONI,D.&BACCHETTA,G.( ) The role of fencing in the success of threatened plant species translocation. Plant Ecology, , –. References FENU, G., COGONI, D., PINNA, M.S. & BACCHETTA,G.(a) Threatened Sardinian vascular flora: a synthesis of  years of AGUILELLA, A., FOS,S.&LAGUNA,E.() Catálogo Valenciano de monitoring activities. Plant Biosystems, , –. Especies Amenazadas de Flora. Conselleria de Medi Ambient, Aigua, FENU, G., COGONI, D., SULIS,E.&BACCHETTA,G.(b) Ecological Urbanisme i Habitatge. Generalitat Valenciana, Valencia, Spain. response to human trampling and conservation status of

Helianthemum caput-felis (Cistaceae) at the eastern periphery of its MARCO, J.A., GIMÉNEZ, P., PADILLA,A.&SÁNCHEZ,A.() range. Botany Letters , –. Crecimiento urbano y extinción de flora rara: aplicaciones FENU,G.,MATTANA,E.&BACCHETTA,G.() Distribution, status and cartográficas en el caso de Helianthemum caput-felis Boiss. conservation of a Critically Endangered, extremely narrow endemic: Serie Geográfica, , –. Lamyropsis microcephala (Asteraceae) in Sardinia. Oryx, , –. MARCO, J.A., GIMÉNEZ, P., PADILLA,A.&SÁNCHEZ,A.() FOIS, M., BACCHETTA, G., CUENA-LOMBRAÑA, A., COGONI, D., Cartografía corológica y área de ocupación de Helianthemum PINNA, M.S, SULIS,E.&FENU,G.() Using extinctions in caput-felis Boiss. en la Península Ibérica. In Avances en Biogeografía. species distribution models to evaluate and predict threats: Áreas de Distribución: Entre Puentes y Barreras (eds J. Gómez a contribution to plant conservation planning on the island Zotano, J. Arias, J.A. Olmedo & J.L. Serrano), pp. –. Tundra of Sardinia. Environmental Conservation, , –. Ediciones & Editorial Universidad de Granada, Almenara & GARCÍA DE LA SERRANA, R., VILAGROSA,A.&ALLOZA, J.A. () Granada, Spain. Pine mortality in southeast Spain after an extreme dry and warm MORRIS,W.F.&DOAK, D.F. () Quantitative Conservation year: interactions among drought stress, carbohydrates and bark Biology: the Theory and Practice of Population Viability Analysis. beetle attacks. Trees, , –. Sinauer, Sunderland, USA. GARGANO, D., FENU, G., MEDAGLI, P., SCIANDRELLO,S.& NEWBOLD, T., HUDSON, L.N., HILL, S.L., CONTU, S., LYSENKO, I., BERNARDO,L.() The status of Sarcopoterium spinosum SENIOR, R.A. et al. () Global effects of land use on local (Rosaceae) at the western periphery of its range: ecological terrestrial biodiversity. Nature, , –. constraints lead to conservation concerns. Israel Journal of Plant ORSENIGO,S.,MONTAGNANI,C.,FENU,G.,GARGANO,D.,PERUZZI,L., Sciences, , –. ABELI,T.etal.() Red Listing plants under full national GIMÉNEZ, P., SÁNCHEZ, A., PADILLA,A.&MARCO, J.A. () responsibility: extinction risk and threats in the vascular flora Integración de una cartografía corológica a escala de detalle endemic to Italy. Biological Conservation, , –. mediante GPS en el proceso urbanizador: Halianthemum caput-felis PIMM, S.L., JENKINS, C.N., ABELL, R., BROOKS, T.M., GITTLEMAN, J.L., Boiss. en el litoral sur de Alicante (España). In La Perspectiva JOPPA, L.N. et al. () The biodiversity of species and their rates of Geográfica ante los retos de la Sociedad y el Medio Ambiente en el extinction, distribution, and protection. Science, , . Contexto Ibérico—Ponencias XI Coloquio Ibérico de Geografía PIMM, S.L., RUSSEL, G.J., GITTLEMAN, J.L. & BROOKS, T.M. () (eds J. Bosque & V. Rodríguez-Espinosa), pp. –. Universidad de The future of biodiversity. Science, , –. Alcalá de Henares, Madrid, Spain. PULLIN, A.S., BALDI, A., CAN, O.E., DIETERICH, M., KATI,V., GÓMEZ, J.M., GONZÁLEZ-MEGÍAS, A., LORITE, J., ABDELAZIZ,M.& LIVOREIL, B. et al. () Conservation focus on Europe: major PERFECTTI,F.() The silent extinction: climate change and the conservation policy issues that need to be informed by conservation potential hybridization-mediated extinction of endemic science. Conservation Biology, , –. high-mountain plants. Biodiversity and Conservation, , –. RCORE TEAM () R: a Language and Environment for Statistical GSPC (GLOBAL STRATEGY FOR PLANT CONSERVATION)() Computing. R Foundation for Statistical Computing, Vienna, Http://www.cbd.int/gspc [accessed  October ]. Austria. Http://www.R-project.org [accessed  May ]. IUCN () IUCN Red List Categories and Criteria v .. IUCN RODRIGUES, A.S., PILGRIM, J.D., LAMOREUX, J.F., HOFFMANN,M.& Species Survival Commission Gland, Switzerland and Cambridge, BROOKS, T.M. () The value of the IUCN Red List for UK, IUCN Species Survival Commission. Http://www.iucnredlist. conservation. Trends in Ecology and Evolution, , –. org/technical-documents/categories-and-criteria [accessed  ROSSI, G., ORSENIGO, S., MONTAGNANI, C., FENU, G., GARGANO, D., July ]. PERUZZI, L. et al. () Is legal protection sufficient to ensure plant IUCN (a) IUCN Red List Categories and Criteria v. .. nd conservation? The Italian Red List of policy species as a case study. edition. IUCN Species Survival Commission, Gland, Switzerland. Oryx, , –. Https://www.iucnredlist.org/resources/categories-and-criteria ROYAL BOTANIC GARDENS () The State of the World’s Plants. [accessed  September ]. Royal Botanic Gardens, Kew, UK. IUCN (b) Threats Classification Scheme v. .. Http://www. SERRA, L., FABREGAT, C., HERRERO-BORGOÑÓN,J.&LÓPEZ UDIAS, iucnredlist.org/technical-documents/classification-schemes/ S. () Distribución de la Flora Vascular Endémica, Rara o threats-classification-scheme [accessed  August ]. Amenazada en la Comunidad Valenciana. Colección Biodiversidad, IUCN () Standards and Petitions Subcommittee Guidelines for Generalitat Valenciana, Spain. Using the IUCN Red List Categories and Criteria v.. Prepared by STUBBEN,C.&MILLIGAN,B.() Estimating and analyzing the Standards and Petitions Subcommittee. Http://www.iucnredlist. demographic models using the popbio package in R. Journal of org/documents/RedListGuidelines.pdf [accessed  December ]. Statistical Software, , –. LAGUNA, E., DELTORO, V.I., PÉREZ-BOTELLA, J., PÉREZ-ROVIRA,P., SULIS,E.() Ecological features, populations traits and conservation SERRA, L., OLIVARES,A.&FABREGAT,C.() The role of small status of Helianthemum caput-felis along its distribution range. reserves in plant conservation in a region of high diversity in eastern PhD thesis. University of Cagliari, Cagliari, Italy. Spain. Biological Conservation, , –. SULIS, E., BACCHETTA, G., COGONI,D.&FENU,G.() LAGUNA,E.&FERRER,P.P.() Global environmental changes in an Short-term population dynamics of Helianthemum caput-felis, unique flora: endangered plant communities in the Valencia region. a perennial Mediterranean coastal plant: a key element for an Mètode Science Studies Journal, , –. effective conservation programme. Systematics and Biodiversity, LAGUNA, E., NAVARRO, A., PÉREZ-ROVIRA, P., FERRANDO,I.& , –. FERRER-GALLEGO,P.P.() Translocation of Limonium VAN DER MEER, S., DAHLGREN, J.P., MILDÉN,M.&EHRLÉN,J.() perplexum (Plumbaginaceae), a threatened coastal endemic. Differential effects of abandonment on the demography of the Plant Ecology, , –. grassland perennial Succisa pratensis. Population Ecology, , –. MACE, G.M., COLLAR, N.J., GASTON, K.J., HILTON‐TAYLOR, C., ZARAGOZÍ, B., GIMÉNEZ, P., NAVARRO, J.T., DONG,P.&RAMÓN,A. AKÇAKAYA, H.R., LEADER‐WILLIAMS,N.&STUART, S.N. () () Development of free and open source GIS software for Quantification of extinction risk: IUCN’s system for classifying cartographic generalisation and occupancy area calculations. threatened species. Conservation Biology, , –. Ecological Informatics, , –.