Distribution and conservation status of Emys orbicularis in Morocco

The distribution and conservation status of Emys orbicularis occidentalis is reviewed for Morocco. Populations are highly fragmented and vulnerable. The species is largely restricted to mountainous areas in the western Rif and Middle Atlas, with scattered observations of isolated individuals in the Gharb plain and the eastern Rif. Our literature survey and fieldwork indicate an accelerated regression of Emys populations along the Moroccan Atlantic coast due to habitat loss. At the same time, we found European pond turtles having a wider distribution in the Rif Mountains than previously known. However, in the central and western Rif, the species is increasingly threatened by expanding cannabis plantations. Other country-wide menaces include water pollution, catching of turtles for pets, desertification, and possibly competition with another terrapin species (Mauremys leprosa).


Introduction
The European pond turtle (Emys orbicularis) is a wide spread species, distributed from the Maghreb region in North Africa through many parts of Europe, Turkey and the Caucasus region to the former Aral Sea (Fritz 2003).Throughout its highly fragmented distribution range, the species is clearly in regression (cf.Fritz & Chiari 2013).
Comprehensive, nearly rangewide phylogeographic studies have identified nine genetic lineages of E. or bi cu la ris and elucidated its evolutionary history (e.g.Lenk et al. 1999;Fritz et al. 2007;2009;VeLo-antón et al. 2008VeLo-antón et al. , 2011;;PedaLL et al. 2011;StuCkaS et al. 2014;Vam berger et al. 2015).One of the genetic lineages, line age VI, is distributed in Morocco and across most of the Iberian Peninsula (Fritz et al. 2007;VeLoantón et al. 2011;StuCkaS et al. 2014), with a contact zone with two other lineages in northeastern Iberia (Fritz et al. 2007;PedaLL et al. 2011).Based on phylogenetic and popula tion genetic data, all populations of lineage VI are now identified with the subspecies E. o. occidentalis (StuCkaS et al. 2014), which originated in North Africa and later colonized the Iberian Peninsula, with a subsequent north ward range expansion across Spain and Portugal (VeLoantón et al. 2008).
The distribution of E. o. occidentalis is well known for Spain and Portugal (PLeguezueLoS 2002;Loureiro et al. 2010), and it has been a target species of numerous conservation projects throughout the Iberian Peninsula (ayreS et al. 2013; teixeira et al. 2013).In contrast, the present distribution and conservation status of Moroccan populations are still poorly known.
With this note we aim (i) to summarize all available distribution records for E. o. occidentalis in Morocco, and (ii) to identify the major threats for Moroccan popu lations based on a literature review and own recent obser vations.

Materials and Methods
Here we review and summarize all previously published records of Emys orbicularis occidentalis for Morocco and combine these with our observations.We present all distribution data using an UTM grid (10 × 10 km) and distinguish between records after 1996 and before 1996, the year of publication of the distribution atlas by bonS & geniez (1996).In Morocco, E. o. occidentalis is gener ally considered rare and as having a patchy distribution (Fahd & PLeguezueLoS 1996;Fahd et al. 2009;mateo et al. 2003).The species occurs mostly within humid and subhumid bioclimatic regions in small ponds and streams with abundant vegetation (bonS & geniez 1996).For Morocco, its presence was reported for 21 locali ties corresponding to 13 UTM squares (bonS & geniez 1996; Fig. 1), including the Middle Atlas Mountains (near Ifrane), the northwestern Atlantic coast (Gharb plain), the Rif Mountains (Tingitana Peninsula), and isolated individuals in the eastern Rif (Oued Kert; Fahd & PLeguezueLoS 1992).Additional recent records were published for the northern Rif (Fahd & PLeguezueLoS 1996;mateo et al. 2003;donaire et al. 2011), the Middle Atlas (Fahd et al. 2009), and the Jebala region (Tingitana Peninsula), with an isolated population at Jebel Haouch Ben Kre'aa (mediani et al. 2009).

Distribution Records
Rif Mountains: The European pond turtle was observed until the end of the last century in different sites along the western part of the Rif (UTM 30S: TD67, TE80, TE90, UD09, UD09; bonS & geniez 1996), and an isolated population was reported from the Oued Kert in the east ernmost Rif (VD88; Fahd & PLeguezueLoS 1992).In this century, numerous fieldwork campaigns led to an increase of the known range in the western part of Rif (UTM 30S: TD63, TD64, TD97, TD69, TE61, TE70, TE42, TE43;mateo et al. 2003;mediani et al. 2009;donaire et al. 2011; present study; Fig. 1).The species is frequently found in ponds and streams near Bouhachem and south of Bab Taza, even though recent efforts failed to record it in the mountains north of Bab Taza (Talassemtane National Park).In a small pond near Bouhachem, we have noticed declining individual numbers, from some dozens of European pond turtles found in 2009 to less than 10 individuals in 2012, coinciding with the arrival of the Mediterranean stripe-necked terrapin Mauremys leprosa.A small and isolated Emys population occurs in the northwestern Rif (Jebel Haouch Ben Kre'aa) and a few isolated individuals were recently observed in sever al localities near Ouezzane.A major threat for the species in this area comes from cannabis plantations (Fahd et al. 2005), which are rapidly growing along the central and western Rif (LabrouSSe & romero 2001) and increasing ly threaten habitats (CharCo 1999) by desiccating water bodies (e.g.Bab Taza surroundings, pers.observ.).These habitat alterations are also threatening species such as vi pers (brito et al. 2011).
Emys orbicularis occidentalis is probably more wide spread along the central Rif Mountains.However, the central Rif Mountains are a dangerous region with many cannabis dealers hampering surveys in this area.On the other hand, we could not confirm the presence of E. o. oc cidentalis in the Oued Kert (eastern Rif) during our field surveys.However, we could sample a captive individual from there during a trip in 2007, which was said to have been recently caught.The record in this isolated area (Fahd & PLeguezueLoS 1992) may result from migrating turtles from the eastern Rif Mountains, a region that has been also understudied.
Using microsatellite and mitochondrial data, the Rif turtles are genetically differentiated from the popula tions of the Middle Atlas and Gharb plain (StuCkaS et al. 2014).

Gharb plain:
During the last century, Emys orbicularis oc cidentalis was widespread in the Gharb plain (UTM 29S: QT03, QT27, QT29, QU51, QU60, QU45, QU56, QV60; UTM 30S: TD39; Fahd et al. 2009), but our recent fieldwork in this coastal region indicates massive habitat loss due to recent and intense human development (trans formation of natural humid areas into crop, vegetable and cane fields, urbanization; CharCo 1999;ramdani et al. 2001;CutteLod et al. 2008;Fahd et al. 2009).For the same reasons, local extinction of Vipera latastei has also been suggested (brito et al. 2011).Only a few isolated pond turtles have been observed in the southern Gharb plain (near Dar Gueddari; UTM 29S: QU40) and near Larache (UTM 29S: QU68QU69; F. Jiménez CazaLLa pers.comm.).Two individuals from the southern Gharb plain (Kenitra province) grouped in population genetic analyses with the Middle Atlas populations (StuCkaS et al. 2014), but further work is needed for a better under standing of the genetic differentiation of possibly surviv ing remnant populations in the Gharb plain.

Middle Atlas Mountains:
In these mountains, some pop ulations have been studied during several surveys since 2008, which match with the UTM localities of bonS & geniez (1996).These populations occur in several ponds near Sidi Mimoune (UTM 30S: UC12) and Ifrane (UTM 30S: UC01).Further surveys are needed to iden tify the current range of the species in this wide mountain region.

Discussion
It is obvious that populations of Emys orbicularis oc cidentalis are at present highly fragmented and vulner able in Morocco.European pond turtles are now largely restricted to mountainous areas in the western Rif and in the Middle Atlas, with few additional observations of isolated individuals in the Gharb plain and the eastern Rif.The turtles from the Gharb plain might represent the last survivors of formerly abundant populations in this region (Fig. 1), which has been massively modified since the 1950s (Fahd et al. 2009).Accordingly, our literature and fieldwork surveys indicate an accelerated regression of Emys populations due to habitat loss in this area.At the same time, we found pond turtles having a wider dis tribution in the Rif Mountains than previously thought.However, in the central and western Rif, the species is increasingly threatened by expanding cannabis planta tions.Other menaces include water pollution, catching of turtles for pets and desertification.Furthermore, in one population in the Rif, we observed a declining individual number, which could be associated with the recent arrival of the Mediterranean stripe-necked terrapin Mauremys leprosa, which could outcompete and displace European pond turtles.Finally, we wish to highlight the importance of further surveys for assessing the current situation of E. o. occidentalis in Morocco, which is the rarest turtle species in this country and much more endangered than Testudo graeca.For getting an accurate picture of the dis tribution range of E. o. occidentalis, any misidentifica tions and confusions with the abundant M. leprosa have to be excluded.

Fig 1 .
Fig 1. Records of Emys orbicularis occidentalis in Morocco.Coloured cells represent UTM squares (10 km).The three main regions (Gharb plain, Rif and Middle Atlas Mountains) where the species occurs are highlighted.