An updated report on the distribution and conservation status of the endangered Cat ’ s Head Rockrose Helianthemum caput-felis ( Magnoliopsida : Violales : Cistaceae ) in Algeria

Helianthemum caput-felis is an Endangered plant species growing in the western Mediterranean basin.  Its distribution is well known to the European and Moroccan regional populations, but no data from its distribution in Algeria have been reported since the middle 20 th century.  In this study, we provide an up-to-date report on the distribution of the species in Algeria.  Fieldwork surveys in the classical locations were unsuccessful in finding the species, probably due to human habitat disturbances; however, a relict location was found in Ain-el-Kerma, near one of the historical known locations.  As there is reduced distribution we point out the main causes that threaten the habitat of H. caput-felis according to IUCN threats classification scheme and we also propose to label it in the Algerian Red List as regionally Critically Endangered (CRreg B1ab(i,ii,iii, v)+2ab(i,ii,iii,v); C2a(i,ii); D).


INTRODUCTION
Helianthemum caput-felis Boiss.(Cistaceae) is a perennial subshrub growing mostly in coastal cliff cracks and dune systems (Agulló et al. 2010), with a narrow fragmented distribution along the western Mediterranean coastlines (López-González 1993).As a consequence, it suffers the direct pressure of urban expansion (Padilla et al. 2014) and also the impact of tourism and human trampling (Fenu et al. 2012(Fenu et al. , 2015)).Consequently, wild populations of H. caputfelis are severely fragmented, the number of mature individuals is decreasing, and active processes of population regression have also been detected (Agulló et al. 2013).Therefore, H. caput-felis is included in the Bern Convention (Appendix I), European Habitat Directive (Appendix 2) and Spanish Biodiversity Law (Appendix 2).According to the Red List, H. caput-felis has been considered as Endangered (EN, Agulló et al. 2013), though Italian and Spanish National Red Lists of threatened flora catalogued it as Critically Endangered (CR, Rossi et al. 2013) and Endangered (EN, Agulló et al. 2011), respectively.No information has been yet reported from northern African territories however, and the species is not included in the recent Algerian Decree for the list of wild plant species under protection (Executive Decree no.12-03, 4 Jan 2012).
Up to now, some specific studies about H. caputfelis have been carried out based on applications of geographic information system (e.g., Marco et al. 2011;Padilla et al. 2014), reproductive biology (Tébar et al. 1997;Rodríguez-Pérez 2005;Agulló et al. 2015), population genetic diversity (Agulló et al. 2011) and conservation issues (Pujol 2001;Agulló et al. 2010;Fenu et al. 2012Fenu et al. , 2015)), but mainly from Spanish and Italian regional populations.Although the presence of this taxon in northern Africa is reported by regional floras or herbarium databases (Quézel & Santa 1962-1963;Fennane et al. 1999;GBIF.org 2015), data are still scarce about the current distribution and conservation status in those African territories.
In Algeria, H. caput-felis was first recorded by the middle of the 19 th century by Munby (1847), who stated its presence "sur les sables prés le Cap Falcon, Oran".Later, other authors also reported it from 'Cap Falcon' and 'Aïn-el-Turk', both areas quite close to Oran (Willkomm 1856;Trabut 1887;Battandier & Trabut 1888).These authors mostly described the habitat of H. caput-felis as coastal sands, though it was also reported as a littoral taxon (cf.Trabut 1887).After that, Doumergue (1918) reported this species from "Andalouses" and "Cap Blanc".The most recent published mention of this taxon was done by Quézel & Santa (1962-1963), who catalogued it as a rare plant in Algeria.These authors only reported the locality 'Aïnel-Turk', which was included in a large geographical area named as littoral Oran subsector (O1, see Quézel & Santa 1962-1963).Besides, H. caput-felis has not been newly collected from 'Aïn-el-Turk' or any other Algerian locality since 1945 (see GBIF.org 2015).
Taking into consideration the notable deficiency of data on H. caput-felis in Algeria, the aim of this paper is to provide details on historic and recent studies on this species, updating its current distribution in Algeria and assessing the current conservation and the IUCN category at regional level.

MATERIAL AND METHODS
Fieldwork was undertaken from 2010 to 2014 to verify the presence of H. caput-felis in the northwestern littoral areas close to Oran, following the data reported in the literature and also the plant material kept in the herbaria BC, MA, MPU, P and RAB (Institut Botànic de Barcelona, Real Jardín Botánico de Madrid, Université de Montpellier 2, Muséum National d'Histoire Naturelle de Paris and Institut Scientifique de Rabat, respectively; acronyms according to Thiers 2016) (see Appendix 1).The survey of labels on sheets offered additional information about localities and even ecological aspects about the species in Algeria.Direct field observations would identify the current condition of those reported localities, which could have notably influenced on the up-to-date distribution of H. caput-felis.The status of conservation of H. caput-felis in Algeria was analysed according to the IUCN threat classification scheme, version 3.2 (IUCN 2012a).The threat category was assigned following the guidelines for application of IUCN Red List Categories and Criteria at global and national levels (IUCN 2012b(IUCN , 2014)).The abbreviations of author names follow The International Plant Names Index (IPNI 2015).The collected plant material is conserved at the herbarium ABH (University of Alicante, Spain) (see Appendix 1).

Past distribution based on literature and herbaria data
Based on the studied herbarium vouchers (see Appendix 1), H. caput-felis was mostly collected for almost

Current distribution based on fieldwork
Although most of the collected plant material came from 'Aïn-el-Turk' and 'Cap Falcon', we were not able to locate any specimen of H. caput-felis in these areas.The locality 'Cap Falcon' is a small geographical cape, which nowadays is severely transformed due to the presence of waste, human buildings (including a military restricted area), and livestock.The coastal sand dunes placed between 'Cap Falcon' and the town of 'Aïn-el-Turk', as well as those from 'Les Andalouses' have also been dramatically modified.In the former, an artificial hillside, plenty of ornamental plants, is now found.In the latter, the dune system is currently replaced by tourist urbanizations.Furthermore, field surveys undertaken around these coastal sand habitats, as well as other better-conserved littoral sand dunes between 'Les Andalouses' and 'Aïn-el-Turk' were also unsuccessful.
Fortunately, we found a location of H. caput-felis in the western part of Oran province (Fig. 1), in the municipality of 'Ain-El-Kerma', between 'Madagh forest' and 'Madagh beach', at 170m (35 0 38'56.4"N& 01 0 02'20.40"W).This probably corresponds to the location found in "Cap Blanc, in Wadi Madar" by Doumergue (1918).The number of observed plants was quite reduced, c. 30, though they flowered and fruited normally.The habitat is totally different to those described before for Algeria.In this location, the species grows on littoral calcareous hills (Image 1), not close to the seashore and similarly as it does in Morocco and Melilla, together with shrubby species such as Cistus heterophyllus Desf., C. monspeliensis L., Rosmarinus officinalis L., Sideritis maura de Noé, Lavandula dentata L. and Teucrium polium L. sensu lato, among others.Unlike the abundance of H. caput-felis in X the other northern African locations (i.e., Morocco and Melilla), its presence in Algeria is fairly scarce and not uniformly distributed across the area.This natural area is quite well conserved, without human facilities around, and the accessibility to these calcareous slopes is quite reduced.

IUCN Red List Assessment
The main threats for the historical known locations of H. caput-felis in Algeria have been coastal urbanization, grazing, constructions excavation and retreat from the coastlines, and these could affect the remaining location in the medium-term.According to IUCN threats classification scheme (version 3.2, IUCN 2012a) we supply a list of threats identified for the Algerian regional population (Table 1).
According to the Red List guidelines of IUCN, we used criteria B (geographic range), C (small population size and decline) and D (very small or restricted population) to evaluate the status of H. caput-felis in Algeria.We could not evaluate criteria A (population size reduction measured along 10 years or 3 generations) and E (quantitative analysis), because there was no previous information available.
Criteria B: based on the reduced extent of occurrence (B1, EOO <100km 2 ), area of occupancy (B2, AOO <10km 2 ), on the number of locations (a = 1) and on the inferred and projected continuing decline in the extent of occurrence (b-i), area of occupancy (b-ii), quality of habitat (b-iii), and number of mature individuals (b-v), the population of H. caput-felis in Algeria meets B1ab(i,i i,iii,v)+2ab(i,ii,iii,v) for CR.
Criteria C: based on the number of mature individuals (<250) and a projected and inferred continuing decline of the population size (C2) and, satisfying the number of mature individuals in each subpopulation (a-i, ≤ 50) and the percentage of mature individuals in one subpopulation (a-ii, = 90-100%), the population of H. caput-felis in Algeria meets C2a(i,ii) for CR.

DISCUSSION
Our study highlights the fragile situation of H. caput-felis in Algeria.The significant anthropogenic degradation of the habitat in the historical locations of the species in 'Aïn-el-Turk', 'Cap Falcon' and 'Les Andalouses' should have alerted about the conservation requirements of this species.In the light of the fieldwork results, the continued expansion of residential areas and the rising of tourism activities in the locations where H. caput-felis grew should have induced the Algerian authorities to list the species in the decree regulating the conservation of wild plant species.On the contrary, the lack of actions and policies in the conservation of H. caput-felis could have contributed to the extinction of the species in these historical areas.
Fortunately, the finding of a relict location gives some hope in the conservation of this species in one of its border historical national range.Due to the growth of this species under different environments (e.g., vertical coastal cliffs, sand and fossil dunes, inland ravines), further field surveys are needed to identify additional locations of H. caput-felis across the whole geographical area, especially towards the seashore in the areas between Madagh and Oran, and westwards to the Moroccan border.With the reference of the discovery of this locality, and the probable extinction of H. caput-felis in 'Cap Falcon' and the littoral dunes of 'Aïn-el-Turk', the up-to-date distribution of H. caputfelis in Algeria points out to consider this taxon as an extremely rare plant.
Additionally, the current status and threats of the Algerian regional population had led us to propose its inclusion in the regional Red List.Following the IUCN guidelines (IUCN 2014), the draft assessment resulted in CR(Regional) B1ab(i,ii,iii,v)+2ab(i,ii,iii,v); C2a(i,ii); D. However, the assessment requires adjusting the preliminary Red List Category to determine the final estimate extinction risk within the region by considering whether extra-regional populations may affect the extinction risk of the regional population (see IUCN 2012b).Because the regional population does not seem to experience any significant immigration of propagules likely to reproduce in the region, the regional population behaves as an endemic and the Red List Category should be left unchanged (see above).The small geographic range occupied by the species, the very small and restricted regional population and the continuing decline in the extent, quality of habitat and number of individuals instigated by human pressures in the past and the present allow us to project a grim future for the species if no conservation strategies are implemented.

CONSERVATION RECOMMENDATIONS
According to the results of our study, the H. caputfelis regional population in Algeria is close to extinction and needs urgent conservation measures.It is necessary to establish the appropriate monitoring of the known locality of this species and to activate in situ and ex situ conservation strategies to protect this particularly rare species from irreversible decline and total extinction in Algeria.Particularly, a greater effort should be made to minimise the direct anthropogenic impact, including urban sprawl and unsustainable tourism.
Thus, recreational activities should be regulated around the sole location of the species, preferably by establishing a protected area or a Plant Micro-Reserve (see Kadis et al. 2013) to ensure the viability of the species in the wild.In this respect, Yahi et al. (2011Yahi et al. ( , 2012) ) have recently proposed the designation of several Important Plant Areas (IPAs) in northern Algeria, in order to prioritise the best sites for plant conservation.Additionally, ex situ strategies should be put into practice.Seed collection and conservation in seed banks and cultivation in botanical gardens will ensure the possibility of future reinforcement or reintroduction of H. caput-felis in eventual suitable habitats, as already done in some Spanish regions and lately proposed for Sardinia (Fenu et al. 2015).Moreover, the species should be included in the National Red List and protected by law, incorporating it in the Algerian Decree for the list of wild plant species under protection.
T h r e a tt e n e d T a x a T h e J o u r n a l o f T h r e a tt e n e d T a x a fi s d e d fi c a tt e d tt o b u fi l d fi n g e v fi d e n c e f o r c o n s e r v a fi o n g l o b a l l y b y p u b l fi s h fi n g p e e r -r e v fi ew e d a r fi c l e s o n l fi n e e v e r y m o n tt h a tt a r e a s o n a b l y r a p fi d r a tt e a tt www .tt h r e a tt e n e d tt a x a .o r g.A l l a r fi c l e s p u b l fi s h e d fi n J o T T a r e r e g fi s tt e r e d u n d e r C r e a fi v e C omm o n s A tt r fi b u fi o n 4 .0 I n tt e r n a fi o n a l L fi c e n s e u n l e s s o tt h e rw fi s e m e n fi o n e d .J o T T a l l ow s u n r e s tt r fi c tt e d u s e o f a r fi c l e s fi n a n y m e d fi um , r e p r o d u c fi o n , a n d d fi s tt r fi b u fi o n b y p r o v fi d fi n g a d e q u a tt e c r e d fi tt tt o tt h e a u tt h o r s a n d tt h e s o u r c e o f p u b l fi c a fi o n .O P E N A C C E S S P a r tt n e r www .tt h r e a tt e n e d tt a x a .o r g I S S N 0 9 7 4 -7 9 0 7 ( O n l fi n e ) | I S S N 0 9 7 4 -7 8 9 3 ( P r fi n tt ) B u fi l d fi n g e v fi d e n c e f o r c o n s e r v a fi o n g l o b a l l y J o u r n a l o f T h r e a tt e n e d T a x a P u b l fi s h e r / H o s tt F o r F o c u s , S c o p e , A fim s , P o l fi c fi e s a n d G u fi d e l fi n e s v fi s fi tt h tt p : / / tt h r e a tt e n e d tt a x a .o r g / A b o u tt _ J o T T .a s p F o r A r fi c l e S u bm fi s s fi o n G u fi d e l fi n e s v fi s fi tt h tt p : / / tt h r e a tt e n e d tt a x a .o r g / S u bm fi s s fi o n _ G u fi d e l fi n e s .a s p F o r P o l fi c fi e s a g a fi n s tt S c fi e n fi fi c M fi s c o n d u c tt v fi s fi tt h tt p : / / tt h r e a tt e n e d tt a x a .o r g / J o T T _ P o l fi c y _ a g a fi n s tt _ S c fi e n fi fi c _M fi s c o n d u c tt .a s p F o r r e p r fi n tt s c o n tt a c tt < fi n f o@ tt h r e a tt e n e d tt a x a .o r g > Status of Helianthemum caput-felis in AlgeriaAgulló et al.a century from three different Algerian localities, 'Aïnel-Turk' (e.g., MPU028393, MPU028398, MPU028387, RAB077965, P04747855, P05375076), 'Cap Falcon' (e.g., MPU028397, MPU028388, P05375155), and to a lesser extent from 'Plaine des Andalouses' (e.g., MPU028399, P05375154); all these localities belonging to Oran province.This taxon was first collected by G.F. Reuter in 1849 from "Oran, in arenosis, plaine des Andalous" (MPU028399, in sched.);however, none of the published Algerian floras made any mention to this specific locality (cf.Munby 1847;Battandier & Trabut 1888; Quézel &  Santa 1962-1963).H. caput-felis was also reported and harvested from the coastal sandy dunes close to 'Cap Falcon' and to 'Aïn-el-Turk' (cf.Munby 1847; Willkomm 1856; MPU028505, P04729331), the most recent herbarium material (RAB077964, P04750436) belonging to these localities.

Figure 1 .
Figure 1.Up-to-date distribution of Helianthemum caput-felis in Argelia.Open square ( ) depicts the location where the plant species was found, whereas black crosses ( ) indicate locations where the species was cited (including classical locations), but currently not found.
Image 2. A -a fruiting individual of Helianthemum caput-felis; B -an overview of the habitat where it grows in Algeria.© A. Terrones.

Table 1 . List of the direct threats identified in the Algerian regional population of Helianthemum caput-felis, according to IUCN threats classification scheme. Status of Helianthemum caput-felis in Algeria Agulló et al.
for CR.Accordingly, we propose to include H. caput-felis in the Red List in Algeria, as regionally Critically Endangered D