A noteworthy record of translocation for Emys orbicularis persica, Eichwald 1831, in southern Iran

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1 Copyright: This is an open-access article distributed under the terms of the Creative Commons Attribution Non Commercial No Derivs 3.0 Unported License, which permits conditional use for non-commercial and education purposes, provided the original author and source are credited, and prohibits the deposition of material from including PDFs, images, or text onto other websites without permission of the International Chapter at Amphibian and Reptile Conservation 9(1): A noteworthy record of translocation for Emys orbicularis persica, Eichwald 1831, in southern Iran 1, 2* Ali Gholamifard, 3 Hamid Reza Esmaeili, and 1, 2 Nasrullah Rastegar-Pouyani 1 Iranian Plateau Herpetology Research Group (IPHRG), Faculty of Science, Razi University, Kermanshah, Iran 2 Department of Biology, Faculty of Science, Razi University, Kermanshah, Iran 3 Department of Biology, College of Sciences, Shiraz University, Shiraz, 71454, Iran Abstract: In the present study we record a considerable translocation of the eastern pond turtle, Emys orbicularis persica to a rich freshwater habitat in southern Iran. Several scenarios for its introduction to Fars Province are also proposed. Key words. Emys orbicularis persica, Emydidae, translocation, exotic, Arjan wetland, Fars Province, Iran. Citation: *Gholamifard A, Esmaeili HR, Rastegar-Pouyani N A noteworthy record of translocation for Emys orbicularis persica, Eichwald 1831, in southern Iran. Amphibian and Reptile Conservation 9(1): *Corresponding author: Ali Gholamifard, ali.gholamifard.bio@gmail.com Submitted 24th Feb. 2014, Published 18th May Introduction. The family Emydidae Rafinesque, 1815 comprises a group of freshwater turtles of small and medium sizes characterized by a low 12th pair of marginal scutes. The ducts of the musk glands are present and are represented by a single (anterior) pair (Ananjeva et al. 2006, see more details in Vitt and Caldwell 2009). This family with 12 genera and 46 species is one of the most diverse and the most speciose families of the order Testudines Batsch, 1788 (Fritz and Havaš 2013) distributed in Europe to Ural Mountains and North America southward to eastern Brazil (Vitt and Caldwell 2009). With the exception of two species of pond turtles of the genus Emys, E. orbicularis (Linnaeus 1758), and E. trinacris (Fritz et al. 2005), the Emydidae is entirely a New World family (Ananjeva et al. 2006). restricted to the Tigris River basin in southwest of the country (Kami et al. 2006, Fritz and Havaš 2007, Rastegar-Pouyani et al. 2008). The European pond turtles of the genus Emys Duméril, 1805, are turtles of a medium size leading an aquatic mode of life. Emys orbicularis (Linnaeus 1758) with eight described subspecies is a widely distributed Palearctic species as inhabits one of the largest distribution areas among the turtles of the world. The distribution area covers an extensive territory from southern, central and Eastern Europe, Asia Minor and north-western Africa to western Turkmenistan and western Kazakhstan in the east (Fritz 1998, Ananjeva et al. 2006, Van Dijk et al. 2012). Basic information on the general biology, taxonomy and morphology of Palearctic turtle species are readily available from the literature (e.g. Fritz 1998; Fritz et al. 1998; Mitrus and Zemanek 2000; Ananjeva et al. 2006; Fritz et al. 2007; Van Dijk et al. 2012). Iran hosts three taxa of freshwater turtles including the eastern pond turtle, E. o. persica, which is restricted to northern Iran, the Caspian turtle, Mauremys caspica (Gmelin 1774, Geoemydidae) with three subspecies and a wide range in northern and western Iran, and the Euphrates softshell turtle, Rafetus euphraticus (Daudin, 1802, Trionychidae), which is Figure 1. Map of Iran shows natural Caspian Sea habitats (yellow placemarks, 1-5) and introduction sites (red placemarks, 6, 7) for Emys orbicularis persica. 1-5: Golestan, Mazandaran, Guilan, Ardebil and East Azerbaijan Provinces, respectively (Hezaveh et al., 2012); 6. Arjan wetland, 7. Lamerd Township (Source of map is the Google earth) Volume 9(1):

2 Figure 2. a) Water outflow of a spring in the Arjan wetland, b) the spring-fed marshes of Arjan with Phragmites communis, Typha and Juncus along with aquatic vegetation. Images by Ali Gholamifard Volume 9(1):

3 All Iranian populations of E. orbicularis have been considered as E. o. persica, Eichwald, 1831, that are distributed along the southern coast of the Caspian Sea in north of Iran and in the adjacent regions of Armenia, Azerbaijan, Georgia, Russia (Dagestan) and Turkmenistan (Fritz 1998, Ananjeva et al. 2006, Kami et al. 2006, Rastegar-Pouyane et al. 2008, Hezaveh et al. 2012, Van Dijk et al. 2012). In Iran E. o. persica, has been recorded from swamps and wetlands in five provinces along the coastal areas of the southern Caspian Sea (Fig. 1) including Golestan, Mazandaran, Guilan, Ardebil and East Azerbaijan Provinces, as these Iranian populations of E. orbicularis occur in the southern part of its distribution range (Hojjati et al. 2004, Hezaveh et al. 2012). Table 1. Morphometric (in mm) characters for the collected specimen of Emys orbicularis persica from the Arjan wetland, Fars Province, southern Iran. Character Size SCL= Straight Carapace Length SCW= Straight Carapace Width CH= Carapace Height PL= Plastron Length Here, we record this terrapin from a freshwater habitat in south of Iran (Figs. 1, 2a,b). During field work on the ichthyofauna of the Arjan wetland (Fig. 2a,b), the Helleh basin of the Persian Gulf basin, in west of Fars Province in June 2011, one specimen of E. o. persica (Fig. 3a) was collected and photographed incidental to the fishes that were the primary objective. TL1= Tail Length (From the end of plastron to the first of anus in straight line) TL2= Tail Length (From the first of anus to the end of tail in straight line) Figure 3. a) Wild female of E. o. persica from the Arjan wetland and b) a male specimen of E. o. persica in captivity from Lamerd Township. Note the yellow and red copper color of iris as a diagnostic key for females (a) and males (b), respectively. Images by Ali Gholamifard. Table 2. Previous and present (*) recorded native and exotic fish and turtle species from Arjan and Parishan wetlands (Helleh basin). (T = translocated species, En = endemic species). Order Family Species / Author(s) Carasobarbus luteus Cypriniformes Cyprinidae Capoeta damascina Carassius auratus Ctenopharyngodon idella *Cyprinus carpio Hypophthalmichthys molitrix Hypophthalmichthys nobilis Pseudorasbora parva Tor grypus Cyprinodontiformes Poeciliidae *Gambusia holbrooki Mugiliformes Mugilidae Liza abu, T Synbranchiformes Mastacembelidae Mastacembelus mastacembelus Testudines Geoemydidae Mauremys caspica ventrimaculata, En Emydidae *Emys orbicularis persica, T Esmaeili et al Teimori et al Volume 9(1):

4 The first impression of the collectors was that the turtle was M. c. caspica, the only freshwater turtle species of Fars Province. Thus, the specimen languished, but was not forgotten, for nearly three years, when in February 2014, it was checked by the first author and identified as E. o. persica. This specimen is deposited and cataloged in the Zoological Museum-Collection of the Biology Department of Shiraz University (ZMCBSU), Iran as museum number of ZM-CBCU-R112. Some morphometric characters, as according to Terentev and Chernov 1949, of the collected specimen are given in Table 1. The Dasht-e Arjan lake or Arjan wetland, 29 37'N, 51 59'E, is a Ramsar Site, as well as one of the four internationally important wetlands of the nine Biosphere Reserves of Iran, situated within the Arjan Protected Area in the Zagros Mountains, km west of Shiraz, the capital of Fars Province. The Dasht-e Arjan with an area about 2,200 ha, is a shallow, eutrophic, freshwater lake with extensive reed-beds (Fig. 2b, Coad 2014). The lake lies in an enclosed basin and is fed by two large springs on its western side and local run-off from winter rainfall and snowmelt (Coad 2014). The lake margin and the spring-fed marshes have Phragmites communis, Typha and Juncus along with aquatic vegetation (Fig. 2b). Several native and exotic fish species have been recorded from the Arjan and Parishan wetlands, about 15 km apart within the Arjan Protected Area, among which some Chinese carps have been introduced for aquaculture, as well as incidental species (e.g. Pseudorasbora parva; see Table 2). Mauremys caspica is the only turtle species natural to Fars Province. Mauremys c. ventrimaculata is endemic to the highlands of the Kor River and Maharlu Lake basins of Fars Province along with M. c. siebenrocki (Fritz et al. 2008, Gholamifard et al. 2012). Emys orbicularis persica is a common freshwater turtle in the southern Caspian Sea basin of Iran. Considering the presence of E. o. persica outside of its natural range of distribution, several scenarios about its introduction in Fars Province can be proposed as follows: 1. It has most likely been released by hobbyists or local people who brought it home from a holiday. As part of Iranian tradition, people release wild creatures, particularly fish and in recent years turtles, into the wild during certain festivals (new year). In the case of fish, many of them are released into freshwater habitats such as rivers, ponds and reservoirs and can thus result in the establishment of non-native fishes in new environments. In the recent years some native and endemic species of salamanders and turtles have also been traded in aquarium marketing. 2. Probably this turtle was translocated to Fars Province with commercial purposes for sale in pet-shops as the illegal trade and introduction has resulted in invasion of the species into the nature of Fars Province. 3. It seems that E. o. persica was incidentally introduced along with commercially important cyprinids from the Caspian Sea basin (fish ponds of the southern Caspian Sea Provinces such as Guilan and Mazandaran) to the Arjan wetland by the Fisheries Department of Iran. Some naturalists and pet-shop owners (aquarists) claimed that during the recent years several hundreds of juvenile of M. caspica and E. o. persica were imported and translocated to Fars Province from other Iranian Provinces, especially north of Iran, and different freshwater habitats of Fars Province, for sale in pet shops especially for the Nowruz, Iranian Festival of the New Year. In one case in March 2011, the first author observed one of these illegal shipments of turtles in Lamerd Township (Fig. 3b), a hot and dry area in southwest of Fars Province without the natural occurrence of any species of aquatic Testudines. Despite some observations of the eastern pond turtle of Fars Province in nature during the last few years by the authors and local people nothing is still known about any stable population of this taxon. Due to suitable environment of the Arjan wetland such as extensive freshwater resources with rich bed of water weeds and presence of enough foods such as different species of native fishes of different sizes (Table. 2), E. o. persica is expected to establish and extend its range to other freshwater bodies of this basin and became as a natural element fauna within the next decades. For example, the Abu mullet, Liza abu, an inhabitant of the brackish water of the endorheic basin of Maharlu Lake has been translocated to the Parishan wetland (Helleh basin) and became a well established species. Emys o. persica may threaten native fauna of the Arjan wetland as this is an omnivore species. As the introduction of a nonnative predator may affect populations of native fishes and turtles as well as other creatures through predation, competition, habitat changes, genetic changes, and introduction of parasites and diseases, special care should be taken to prevent such introductions (Cadi and Joly 2003; Hojjati et al. 2004; Pazooki and Aghaei Moghadam 2004; Kami and Aghaei Moghadam 2005; Kami et al. 2006). Whether eradication programs can be successful in the case of this species needs to be assessed. There is a possible chance of success because of the yet very limited distribution and records. However, such programs have to be accompanied by a public awareness campaign to ensure that the aquarium trade and hobbyists do not release these ornamental creatures into natural habitats. Acknowledgements. We are thankful to Shiraz University for financial support, and Sustainability America, Belize, for logistical support for article production. Literature Cited Ananjeva NB, Orlov NL, Khalikov RG, Darevsky IS, Ryabov SA, Barabanov AV The Reptiles of Northern Eurasia: Taxonomic Diversity, Distribution, Conservation Status. Zoological Institute, Russian Academy of Sciences. Sofia: Pensoft Series Faunistica, No 47. Cadi A, Joly P Competition for basking places between the endangered European pond turtle (Emys orbicularis galloitalica) and the introduced redeared slider (Trachemys scripta elegans). Canadian Journal of Zoology 81: Coad BW Freshwater Fishes of Iran. [Online]. Available: [Accessed 22 February 2014]. 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