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

1, 2*Ali Gholamifard, 3Hamid Reza Esmaeili, and 1, 2Nasrullah Rastegar-Pouyani

1Iranian Plateau Research Group (IPHRG), Faculty of Science, Razi University, 6714967346 Kermanshah, Iran 2Department of Biology, Faculty of Science, Razi University, 6714967346 Kermanshah, Iran 3Department of Biology, College of Sciences, Shiraz University, Shiraz, 71454, Iran

Abstract: In the present study we record a considerable translocation of the eastern pond , 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, , translocation, exotic, Arjan wetland, Fars Province, Iran.

Citation: *Gholamifard A, Esmaeili HR, Rastegar-Pouyani N. 2015. A noteworthy record of translocation for Emys orbicularis persica, Eichwald 1831, in southern Iran. Amphibian and Reptile Conservation 9(1): 49-53.

*Corresponding author: Ali Gholamifard, E-mail: [email protected] Submitted 24th Feb. 2014, Published 18th May 2015.

Introduction. The Emydidae Rafinesque, 1815 comprises restricted to the Tigris River basin in southwest of the country a group of freshwater of small and medium sizes (Kami et al. 2006, Fritz and Havaš 2007, Rastegar-Pouyani et al. characterized by a low 12th pair of marginal scutes. The ducts of 2008). 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 is one of the most diverse and the most speciose families of the 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 Emys, E. orbicularis (Linnaeus 1758), and E. trinacris (Fritz et al. 2005), the Emydidae is entirely a New World family (Ananjeva et al. 2006).

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 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 and western Kazakhstan in the east (Fritz 1998, Ananjeva et al. 2006, Van Dijk et al. 2012).

Basic information on the general biology, 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 Figure 1. Map of Iran shows natural habitats (yellow the eastern pond turtle, E. o. persica, which is restricted to placemarks, 1-5) and introduction sites (red placemarks, 6, 7) for Emys northern Iran, the Caspian turtle, caspica (Gmelin orbicularis persica. 1-5: Golestan, Mazandaran, Guilan, Ardebil and 1774, ) with three subspecies and a wide range in East Azerbaijan Provinces, respectively (Hezaveh et al., 2012); 6. northern and western Iran, and the Euphrates softshell turtle, Arjan wetland, 7. Lamerd Township (Source of map is the Google euphraticus (Daudin, 1802, ), which is earth).

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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.

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All Iranian populations of E. orbicularis have been considered Table 1. Morphometric (in mm) characters for the collected specimen as E. o. persica, Eichwald, 1831, that are distributed along the of Emys orbicularis persica from the Arjan wetland, Fars Province, southern coast of the Caspian Sea in north of Iran and in the southern Iran. adjacent regions of Armenia, Azerbaijan, , Russia (Dagestan) and Turkmenistan (Fritz 1998, Ananjeva et al. 2006, Character Size 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 SCL= Straight Carapace Length 159.8 coastal areas of the southern Caspian Sea (Fig. 1) including SCW= Straight Carapace Width 124.30 Golestan, Mazandaran, Guilan, Ardebil and East Azerbaijan Provinces, as these Iranian populations of E. orbicularis occur in CH= Carapace Height 66.78 the southern part of its distribution range (Hojjati et al. 2004, Hezaveh et al. 2012). PL= Plastron Length 148.87

TL1= Tail Length (From the end of plastron to the 7.31 Here, we record this from a freshwater habitat in south first of anus in straight line) 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 TL2= Tail Length (From the first of anus to the 44.31 Gulf basin, in west of Fars Province in June 2011, one specimen end of tail in straight line) of E. o. persica (Fig. 3a) was collected and photographed incidental to the fishes that were the primary objective.

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 Native/Exotic Author(s) Carasobarbus luteus Native Capoeta damascina Native Carassius auratus Exotic Ctenopharyngodon idella Exotic Cypriniformes Cyprinidae *Cyprinus carpio Exotic Hypophthalmichthys molitrix Exotic Hypophthalmichthys nobilis Exotic Esmaeili et al. 2010. Pseudorasbora parva Exotic Teimori et al. 2010. Tor grypus Native Cyprinodontiformes Poeciliidae *Gambusia holbrooki Exotic Mugiliformes Mugilidae Liza abu Native, T Synbranchiformes Mastacembelidae Mastacembelus mastacembelus Native Geoemydidae Mauremys caspica ventrimaculata Native, En Testudines Emydidae *Emys orbicularis persica Native, T

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The first impression of the collectors was that the turtle was M. caspica and E. o. persica were imported and translocated to c. caspica, the only freshwater turtle species of Fars Province. Fars Province from other Iranian Provinces, especially north of Thus, the specimen languished, but was not forgotten, for nearly Iran, and different freshwater habitats of Fars Province, for sale three years, when in February 2014, it was checked by the first in pet shops especially for the Nowruz, Iranian Festival of the author and identified as E. o. persica. This specimen is deposited New Year. In one case in March 2011, the first author observed and cataloged in the Zoological Museum-Collection of the one of these illegal shipments of turtles in Lamerd Township Biology Department of Shiraz University (ZMCBSU), Iran as (Fig. 3b), a hot and dry area in southwest of Fars Province museum number of ZM-CBCU-R112. Some morphometric without the natural occurrence of any species of aquatic characters, as according to Terentev and Chernov 1949, of the Testudines. collected specimen are given in Table 1. Despite some observations of the eastern pond turtle of Fars The Dasht-e Arjan lake or Arjan wetland, 29°37'N, 51°59'E, is a Province in nature during the last few years by the authors and Ramsar Site, as well as one of the four internationally important local people nothing is still known about any stable population wetlands of the nine Biosphere Reserves of Iran, situated within of this taxon. Due to suitable environment of the Arjan wetland the Arjan Protected Area in the Zagros Mountains, 40-80 km such as extensive freshwater resources with rich bed of water west of Shiraz, the capital of Fars Province. The Dasht-e Arjan weeds and presence of enough foods such as different species of with an area about 2,200 ha, is a shallow, eutrophic, freshwater native fishes of different sizes (Table. 2), E. o. persica is lake with extensive reed-beds (Fig. 2b, Coad 2014). The lake lies expected to establish and extend its range to other freshwater in an enclosed basin and is fed by two large springs on its bodies of this basin and became as a natural element fauna western side and local run-off from winter rainfall and snow- within the next decades. For example, the Abu mullet, Liza abu, melt (Coad 2014). The lake margin and the spring-fed marshes an inhabitant of the brackish water of the endorheic basin of have Phragmites communis, Typha and Juncus along with Maharlu Lake has been translocated to the Parishan wetland aquatic vegetation (Fig. 2b). (Helleh basin) and became a well established species.

Several native and exotic fish species have been recorded from Emys o. persica may threaten native fauna of the Arjan wetland the Arjan and Parishan wetlands, about 15 km apart within the as this is an omnivore species. As the introduction of a non- Arjan Protected Area, among which some Chinese carps have native predator may affect populations of native fishes and been introduced for aquaculture, as well as incidental species turtles as well as other creatures through predation, competition, (e.g. Pseudorasbora parva; see Table 2). habitat changes, genetic changes, and introduction of parasites and diseases, special care should be taken to prevent such Mauremys caspica is the only turtle species natural to Fars introductions (Cadi and Joly 2003; Hojjati et al. 2004; Pazooki Province. Mauremys c. ventrimaculata is endemic to the and Aghaei Moghadam 2004; Kami and Aghaei Moghadam highlands of the Kor River and Maharlu Lake basins of Fars 2005; Kami et al. 2006). Whether eradication programs can be Province along with M. c. siebenrocki (Fritz et al. 2008, successful in the case of this species needs to be assessed. There Gholamifard et al. 2012). Emys orbicularis persica is a common is a possible chance of success because of the yet very limited freshwater turtle in the southern Caspian Sea basin of Iran. distribution and records. However, such programs have to be accompanied by a public awareness campaign to ensure that the Considering the presence of E. o. persica outside of its natural aquarium trade and hobbyists do not release these ornamental range of distribution, several scenarios about its introduction in creatures into natural habitats. Fars Province can be proposed as follows: Acknowledgements.—We are thankful to Shiraz University for 1. It has most likely been released by hobbyists or local people financial support, and Sustainability America, Belize, for who brought it home from a holiday. As part of Iranian logistical support for article production. tradition, people release wild creatures, particularly fish and in recent years turtles, into the wild during certain festivals (new Literature Cited year). In the case of fish, many of them are released into freshwater habitats such as rivers, ponds and reservoirs and can Ananjeva NB, Orlov NL, Khalikov RG, Darevsky IS, Ryabov thus result in the establishment of non-native fishes in new SA, Barabanov AV. 2006. The of Northern environments. In the recent years some native and endemic Eurasia: Taxonomic Diversity, Distribution, Conservation species of salamanders and turtles have also been traded in Status. Zoological Institute, Russian Academy of Sciences. aquarium marketing. Sofia: Pensoft Series Faunistica, No 47. 2. Probably this turtle was translocated to Fars Province with Cadi A, Joly P. 2003. Competition for basking places between commercial purposes for sale in pet-shops as the illegal trade and introduction has resulted in invasion of the species into the the endangered European pond turtle (Emys orbicularis nature of Fars Province. galloitalica) and the introduced redeared slider ( 3. It seems that E. o. persica was incidentally introduced along scripta elegans). Canadian Journal of Zoology 81: 1392- with commercially important cyprinids from the Caspian Sea 1398. basin (fish ponds of the southern Caspian Sea Provinces such as Coad BW. 2014. Freshwater Fishes of Iran. [Online]. Available: Guilan and Mazandaran) to the Arjan wetland by the Fisheries http://www.briancoad.com [Accessed 22 February 2014]. Department of Iran. Esmaeili HR, Coad BW, Gholamifard A, Nazari N, Teimory A. 2010. Annotated checklist of the freshwater fishes of Iran. Some naturalists and pet-shop owners (aquarists) claimed that Zoosystematica Rossica 19(2): 361-386. during the recent years several hundreds of juvenile of M.

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