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

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Assessing the global conservation status of the rock rose Helianthemum caput-felis
Assessing the global conservation status of the rock
           rose Helianthemum caput-felis
                                                           ELENA SULIS, GIANLUIGI BACCHETTA, DONATELLA COGONI
                                                                           D O M E N I C O G A R G A N O and G I U S E P P E F E N U

           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
           for conservation actions and the most commonly applied                                S    pecies face numerous threats, principally related to
                                                                                                      human activities, and biodiversity continues to be lost
                                                                                                 (Pimm et al., ; Butchart et al., ; Ceballos et al.,
           method for assessing the extinction risk of a species. In
           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’s Aichi
           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., ; Fenu et al., 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 d.cogoni@unica.it
                                                                                                 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
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. https://doi.org/10.1017/S0030605318001424
Assessing the global conservation status of the rock rose Helianthemum caput-felis
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

                                                                                        Oryx, 2020, 54(2), 197–205 © 2019 Fauna & Flora International doi:10.1017/S0030605318001424
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. https://doi.org/10.1017/S0030605318001424
. https://doi.org/10.1017/S0030605318001424
Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 21 Mar 2021 at 21:38:09, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms
                                                                                                                                                                                                     Oryx, 2020, 54(2), 197–205 © 2019 Fauna & Flora International doi:10.1017/S0030605318001424

                                                                                                                                                                                                                                                                                                   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,
                                                                                                                                                                                                                                                                                                   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
                                                                                                                                                                                                                                                                                                   Italy
                                                                                                                                                                                                                                                                                                   1     Sardinia     Is Arutas (Cabras)                    5–15             0.001                     SmallC          No            None          Confirmed     This study      4.1, 6.1, 8.1,
                                                                                                                                                                                                                                                                                                                                                                                                                                                                                 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;
                                                                                                                                                                                                                                                                                                                      (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;
                                                                                                                                                                                                                                                                                                                                                                                                                                                                                 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;
                                                                                                                                                                                                                                                                                                                      Puerto (Ses Salines)                                                                                                                                       9.4
                                                                                                                                                                                                                                                                                                   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
                                                                                                                                                                                                                                                                                                   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

                                                                                                                                                                                                                                                                                                                                                                                                                                                                                                  Rock rose Helianthemum caput-felis
                                                                                                                                                                                                                                                                                                   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
                                                                                                                                                                                                                                                                                                   17    Alicante     Cala els Pinets, Cala Lobella, Cala   10–20            2.203   2.9 ± 0.74        LargeE          Yes           SCI*          Confirmed     This study      6.1
                                                                                                                                                                                                                                                                                                                      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

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                                                                                                                                                                                                                                                                                                   Table 1 (Cont.)

                                                                                                                                                                                                                                                                                                                                                                                                                                                                                 E. 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
                                                                                                                                                                                                                                                                                                   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;
                                                                                                                                                                                                                                                                                                                                                                                                                                                                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)
                                                                                                                                                                                                                                                                                                   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;
                                                                                                                                                                                                                                                                                                                     (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;
                                                                                                                                                                                                                                                                                                                     (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;
                                                                                                                                                                                                                                                                                                                                                                                                                                                                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;
                                                                                                                                                                                                                                                                                                                                                                                                                                                                6.1
                                                                                                                                                                                                     Oryx, 2020, 54(2), 197–205 © 2019 Fauna & Flora International doi:10.1017/S0030605318001424

                                                                                                                                                                                                                                                                                                   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;
                                                                                                                                                                                                                                                                                                                     Horadada)                                                                                                                                  8.1
                                                                                                                                                                                                                                                                                                   34    Alicante    Río Mar (Pilar de la Horadada)    1–5             1.377   3.7 ± 1.53       LargeE       No          None          Confirmed   This study   1.1; 1.3; 6.1
                                                                                                                                                                                                                                                                                                   35    Nador       Barranco del Quemadero            100–110        36.908   2.4 ± 1.56       LargeE       Yes         SCI           Confirmed   This study   2.2
                                                                                                                                                                                                                                                                                                                     (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

                                                                                                                                                       1.1; 1.3; 2.3;
                                                                                                                                                       6.1; 8.1; 9.4
                                     Threats                                                                                                                                                                                                                                                                                                                                           ( generations = . years; Sulis, ). Following the pre-

                                                                                                                                                                             Determined by counting (superscript C) or estimating (superscript E) the total number of mature plants and categorizing as small (,  individuals), medium (–,) or large (. ,) population.
                                                                                                                                                                                                                                                                                                                                                                                       cautionary principle (IUCN, ), the smaller value of gen-
                                                                                                                                                                                                                                                                                                                                                                                       eration length (i.e. . years) was retained. Extinction risk
                                                                                                                                                                                                                                                                                                                                                                                       was calculated considering three alternative assessments (
                                                                  Agulló et al.

                                                                  Agulló et al.

                                                                  Agulló et al.

                                                                  Agulló et al.
                                                                                                                                                                                                                                                                                                                                                                                       years or three generations,  years or five generations, and
                                                                                                                                                                                                                                                                                                                                                                                        years). Quasi-extinction probabilities were calculated
                                     Source

                                                                  (2017)

                                                                  (2017)

                                                                  (2017)

                                                                  (2017)
                                                                                                                                                                                                                                                                                                                                                                                       by  model iterations (van der Meer et al., ).
                                                                                                                                                                                                                                                                                                                                                                                       Matrices were selected at random with replacement (each
                                                                                                                                                                                                                                                                                                                                                                                       matrix had an equal probability of selection; Morris &
                                                                                                                                                       Confirmed
                                                                                                                                                                                                                                                                                                                                                                                       Doak, ). A quasi-extinction threshold of  individuals
                              Current

                                                                  Extinct

                                                                                               Extinct

                                                                                                                          Extinct
                              status

                                                                                                                                                                                                                                                                                                                                                                                       was designated a priori, to help minimize the demographic
                                                                                                                                                                                                                                                                                                                                                                                       stochasticity associated with small population size (Morris
                                                                                                                                                                                                                                                                                                                                                                                       & Doak, ).
                                    Protection2

                                                                                                                                                                                                                                                                                                                                                                                          We also modelled three separate scenarios, one for each
                                                                                                                                                       None

                                                                                                                                                                                                                                                                                                                                                                                       population size class, to examine extinction risk. We developed
                                                                                                                                                                                                                                                                                                                                                                                       each model using the global stochastic growth rate (λs = ;
                                                                                                                                                                             SCI, Site of community importance; PMR, Plant micro-reserve sensu Laguna et al. (); *protection only partially covers the population area.

                                                                                                                                                                                                                                                                                                                                                                                       Sulis, ; Sulis et al., ) and the effective population size.
                              Seedlings
                              present

                                                                                                                                                                                                                                                                                                                                                                                       Results

                                                                                                                                                                                                                                                                                                                                                                                       We located records of H. caput-felis in  localities along the
                              Population

                                                                                                                                                                                                                                                                                                                                                                                       western Mediterranean coasts, mainly in Spain ( localities,
                                                                                                                                                      SmallC

                                                                                                                                                                                                                                                                                                                                                                                       including two in Melilla), followed by Morocco (nine local-
                              size1

                                                                                                                                                                                                                                                                                                                                                                                       ities), Italy and Algeria (four localities in each country;
                                                                                                                                                                                                                                                                                                                                                                                       Table ). We confirmed the presence of H. caput-felis in 
                             Mean density ±
                             SD (plants/m2)

                                                                                                                                                                                                                                                                                                                                                                                       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
                                                                                                                                                                                                                                                                                                                                                                                       (near Hidoun, Nador), field surveys carried out by ourselves
                                                                                                                                                                                                                                                                                                                                                                                       and other researchers failed to locate the species. Following
                              Area
                              (ha)

                                                                                                                                                                                                                                                                                                                                                                                       a precautionary approach, we reported the species as ‘not re-
                                                                                                                                                                                                                                                                                                                                                                                       trieved’ in these localities. We were, however, able to con-
                                                                                                                                                                                                                                                                                                                                                                                       firm recent extinctions at two localities in Europe (Santa
                              Altitudinal
                              range (m)

                                                                                                                                                                                                                                                                                                                                                                                       Pola in Spain, Seu in Italy) and three localities in Algeria.
                                                                                                                          75–80

                                                                                                                                                                                                                                                                                                                                                                                           All sites where occurrence was confirmed are in coastal
                                                                                                                                                       170

                                                                                                                                                                                                                                                                                                                                                                                       environments, with the exception of one population in
                                                                                               50
                                                                  90

                                                                                                                                                                                                                                                                                                                                                                                       Morocco that is . km from the coast. The altitudinal
                                                                                                                                                                                                                                                                                                                                                                                       range at which we located the species was – m. In
                                                                  Cabo Lindlés (Aïn-El-Turk)

                                                                                                                                                                                                                                                                                                                                                                                       Europe, we found the plant below  m, whereas in
                                                                                                                          Aïn-El-Turk (Aïn-El-Turk)
                                                                                               Cap Falcon (Aïn-El-Turk)

                                                                                                                                                                                                                                                                                                                                                                                       North Africa the species occurred in some cases above
                                     Locality (municipality)

                                                                                                                                                       Aïn-El-Kerma (Oran)

                                                                                                                                                                                                                                                                                                                                                                                        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
           Table 1 (Cont.)
                                  Country,
                              No. region

                                                                                                                                                                                                                                                                                                                                                                                       Blanc, Llucmajor). More than half of localities (.%) had
                                                               46 Oran

                                                                                               Oran

                                                                                                                          Oran

                                                                                                                                                       Oran

                                                                                                                                                                                                                                                                                                                                                                                       a population size . , mature plants. The population
                                                               Algeria

                                                                                                                                                                                                                                                                                                                                                                                       size was #  individuals in .% of localities. The popu-
                                                                                               47

                                                                                                                          48

                                                                                                                                                       49

                                                                                                                                                                                                                                                                                                                                                                                       lation structure was mainly characterized by reproductive
                                                                                                                                                                                                                                                                       
                                                                                                                                                                             

             Oryx, 2020, 54(2), 197–205 © 2019 Fauna & Flora International doi:10.1017/S0030605318001424
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202         E. Sulis et al.

                                                                                                                                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 in-
                                                                                                   tegral projection model, there was no extinction risk for
                                                                                                   three generations (Fig. ), but there was an extinction prob-
                                                                                                   ability 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 popula-
                                                                                                   tion 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 . Such values do not reach the minimum threshold
             footprint; .%). Other threats were invasive alien species                         for threatened taxa under Red List criterion A.

                                                                                        Oryx, 2020, 54(2), 197–205 © 2019 Fauna & Flora International doi:10.1017/S0030605318001424
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. https://doi.org/10.1017/S0030605318001424
Rock rose Helianthemum caput-felis                    203

                                                                                                 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 herb-
                                                                                                 arium 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, ; Sulis et al., ). 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. % in three genera-                         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

           Oryx, 2020, 54(2), 197–205 © 2019 Fauna & Flora International doi:10.1017/S0030605318001424
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. https://doi.org/10.1017/S0030605318001424
204         E. Sulis et al.

             consequences of climate change, especially drought or ir-                               A G U L L Ó , J.C., J U A N , A., A LO N S O , M.Á. & C R E S P O , M.B. ()
             regular rainfall, need to be considered for coastal plants                                  Helianthemum caput-felis Boiss. In Atlas y Libro Rojo de la Flora
                                                                                                         Vascular Amenazada de España. Adenda . Dirección General de
             such as H. caput-felis (García de la Serrana et al., ;
                                                                                                         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
                                                                                                         Conservación de Plantas, Madrid, Spain.
             or Plant micro-reserve), our findings nevertheless indicate
                                                                                                     A G U L L Ó , J.C., J U A N , A., C R E S P O , M.B., A LO N S O , M.Á. & T E R R O N E S ,
             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-                         A G U L L Ó , J.C., J U A N , A., G U I L L Ó , A., A LO N S O , M.Á. & C R E S P O , 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                             B A L L A N T Y N E , M. & P I C K E R I N G , 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, , –.
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                                                                                                         C R A N E , P. et al. () The Convention on Biological Diversity’s
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                                                                                                         agreements. Conservation Letters, , –.
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             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                                B U R G M A N , M.A. & F O X , J.C. () Bias in species range estimates
             have demonstrated that these activities would be low-cost                                   from minimum convex polygons: implications for conservation and
                                                                                                         options for improved planning. Animal Conservation, , –.
             projects with good chance of success (e.g. Cogoni et al.,
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             persists. Although it could be challenging to sustain long-                             C E B A L LO S , G., E H R L I C H , P.R., B A R N O S K Y , A.D., G A R C Í A , A.,
             term monitoring, it is fundamental for assessment of con-                                   P R I N G L E , R.M. & P A L M E R , T.M. () Accelerated modern
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                                                                                                         Science Advances, , e.
             Acknowledgements We thank Sergio Sulis, Iván Ramos Torrens                              C O G O N I , D., F E N U , G., C O N C A S , E. & B AC C H E T TA , 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                        C O L L E N , B., D U LV Y , N.K., G A S T O N , K.J., G Ä R D E N F O R S , U., K E I T H ,
             Claro (Guelaya-Ecologistas en Acción Melilla) and Jaime X. Soler for                        D.A., P U N T , A.E. et al. () 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.                                                        E U R O P E A N C O M M I S S I O N () 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.                                                                      F E N U , G., B AC C H E T T A , G., G I AC A N E L L I , V., G A R G A N O , D.,
                                                                                                         M O N TA G N A N I , C., O R S E N I G O , 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.                                                                      F E N U , G., C O G O N I , D. & B A C C H E T TA , G. () The role of fencing in
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                                                                                                         , –.
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