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Report of two subspecies of an alien turtle, Trachemys scripta scripta and Trachemys scripta elegans (Testudines: Emydidae) sharing the same habitat on the island of Zakynthos, Greece

ALEKSANDAR UROŠEVI Ć

University of Belgrade, Institute for Biological Research “Siniša Stankovi ć”, Bulevar despota Stefana 142, 11000 Belgrade, Serbia, E-mail: [email protected]

Received 11 December 2014 │ Accepted 26 December 2014 │ Published online 28 December 2014.

Introduction of alien aquatic turtles, especially the invasive red-eared slider, Trachemys scripta elegans (Wied-Neuwied 1839) has been noted as a global problem (Scalera 2006; Bringsøe 2006). In Greece only, introductions of the red-eared slider have already been published for several localities: Athens, Corfu, Crete, Kos and Zakynthos (Bruekers 1993; Bruekers et al . 2006; Zenetos et al . 2009). Until the EU banned the import and trade of the red-eared slider (Council Regulation No. 338/97), tens of millions of these turtles had been imported into Europe (Bringsøe 2006). Since the ban, the yellow-bellied slider Trachemys scripta scripta (Schoepff 1792) emerged in the European pet trade as one of the “substitute” species and subspecies (Adrados et al. 2002; Bringsøe 2006). Although it is sold in smaller quantities, and at a higher price, numbers of this subspecies found in the wild in Europe are increasing (Bringsøe 2006). The spread of T. s. scripta has been documented in Spain (Martínez Silvestre et al . 2006; Alarcos et al . 2010; Valdeón et al . 2010), Sweden, Finland (Bringsøe 2006) and Austria (Kleewein 2014). There are also online reports of this subspecies from several islands in Greece: Corfu, Crete and Kos (Balej & Jablonski 2006-2014). A large adult male specimen of T. s. scripta was observed on August 20 th 2014 in the freshwater canal near the Limni Keriou beach on the island of Zakynthos, Greece (2m a.s.l., 37°41'00.44 ʺ N, 20°50'07.08 ʺ E). The canal is situated close to Keri Lake, the largest freshwater lake on the island. The specimen was photographed in situ several times while swimming and basking on the surface (Fig. 1a). On August 24 th , the same specimen was observed, and it was caught and photographed from the ventral side, for more accurate identification (Fig. 1b). The animal had all diagnostic characteristics of the subspecies (Ernst et al. 1994; Bringsøe 2006). Judging by the algae on its shell, this specimen had likely spent a substantial amount of time in the given canal. A juvenile specimen of T. s. elegans (Fig. 1c) was also observed and photographed in situ while swimming and feeding on aquatic plants in the same canal. Native turtle population consisted of large numbers of Emys orbicularis (Linnaeus 1758) and a couple specimens of Mauremys rivulata (Valenciennes in Bory de Saint-Vincent 1833). The canal at Limni Keriou is very close to one of the popular beaches on the island, and there is a parking lot near the canal mouth. It makes the canal an easily accessible spot for disposal of unwanted pet turtles, and collection of native turtles by local people was also observed. Irresponsible owners generally tend to release turtles in water bodies situated in urban or suburban areas (Arvy & Servan 1998; Cadi et al . 2004; Bringsøe 2006). Sometimes, people intentionally introduce alien turtles into ponds or pools because of the perceived “decorative” value (Semenov 2010). Zakynthos is a small island, with the surface of about 408 km 2. Small islands (with surfaces less than 6,000 km 2) are especially vulnerable to introduction of invasive species, with more than two times the establishment success rate compared to large islands or continents (Kraus 2009; Reed & Kraus 2010).

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UROŠEVI Ć

Figure 1. A. Adult specimen of T. s. scripta photographed in situ. B. Ventral side of the same specimen. C. Juvenile T. s. elegans photographed in situ at the same locality.

Negative impact of introduced turtles, mainly T. s. elegans on native ecosystems, mostly through competition with native turtles (for food, basking places and breeding sites) is well documented (Arvy & Servan 1998; Cadi & Joly 2004; Alarcos et al. 2010). Release of adult turtles into the native ecosystems by careless owners is still the most important introduction pathway (Bringsøe 2006; Scalera 2006). However, red-eared sliders can successfully breed in the southern Europe (Cadi et al . 2004; Perez-Santigosa et al . 2008), including the island of Kos, Greece (Bruekers et al . 2006) which can lead to establishment of feral populations. Finding of the juvenile specimen indicates that red eared sliders might have successfully bred in close vicinity of the locality (Cadi et al . 2004; Bruekers et al . 2006; Perez-Santigosa et al . 2008). Yellow-bellied slider is ecologically very similar to red-eared slider (Ernst et al. 1994), and these two subspecies can hybridise (Seidel et al . 1999). Hybrid specimens have already been found in Spain (Valdeón et al . 2010) and Austria (Kleewein 2014). Presence of two introduced subspecies of T. scripta near the largest freshwater ecosystem on the island should be a reason for concern. All cases of introduced yellow-bellied slider should be reported and monitored. Wide availability coupled with irresponsible pet owners made the red-eared slider one of the 100 worst invasive species (Scalera 2006). There is a possibility that the same thing might happen with the yellow-bellied slider or some of the other “substitute” species

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TWO INTRODUCED SUBSPECIES OF TRACHEMYS SCRIPTA FROM ZAKYNTHOS

(Bringsøe 2006; Alarcos et al . 2010; Kleewein 2014). For those reasons, release of the unwanted pets into the wild as well as translocation of already introduced alien (and native) turtles by local wildlife enthusiasts should be discouraged.

Acknowledgements I would like to thank Jelena Pavlovi ć for help in the field, Ljiljana Tomovi ć for helpful suggestions and Sonja Đor đevi ć for important corrections of the manuscript. I would also thank Serbian Herpetological Society “Milutin Radovanovi ć“ for support. This work was partly funded by the Serbian Ministry of Education, Science and Technological Development grant no. 173043.

References

Adrados, L.C., Veenvliet, P. & Veenvliet, J.K. (2002) Assessment of trade and ecological threat of species, potentially replacing Rana catesbeiana or Trachemys scripta elegans in the European Union. In: Adrados, L. C. & Briggs, L. (eds.), Study of application of EU wildlife trade regulations in relation to species which form an ecological threat to EU fauna and flora, with case studies of American bullfrog (Rana catesbeiana) and red-eared slider (Trachemys scripta elegans). Unpublished study report to the European Commission. Ref. no. B4- 3040/2001/326066/MAR/E.3. pp. 1–27. Alarcos Izquierdo, G., Flechoso del Cueto, F., Rodríguez Pereira, A., Lizana, M. (2010) Distribution records of non- native terrapins in Castilla and León region (Central Spain). Aquatic Invasions, 5(3), 303–308. Arvy, C. & Servan, J. (1998) Imminent competition between Trachemys scripta and Emys orbicularis in France. Mertensiella , 10, 33–40. Balej, P. & Jablonski, D. (eds.) (2006-2014) Balcanica.info. Available from: http://www.balcanica.cz/(05.11.2014) . Bringsøe, H. (2006): NOBANIS–Invasive Alien Species Fact Sheet–Trachemys scripta . From: Online Database of the North European and Baltic Network on Invasive Alien Species–NOBANIS. Available from: http://www.nobanis.org/ (16.09.2014). Bruekers, J. (1993) Schildpadden op het Griekse eiland Kos. De Schildpad , 19, 38–50. Bruekers, J., Uijtterschout, G. & Brouwer, A. (2006) Erstnachweis einer natürlichen Vermehrung der Rotwangen- Schmuckschildkröte (Trachemys scripta elegans) auf der griechischen Insel Kos. Schildkröten im Fokus , 3(3), 29–34. Cadi, A. & Joly, P. (2004) Impact of the introduction of the red-eared slider ( Trachemys scripta elegans ) on survival rates of the European pond turtle ( Emys orbicularis ). Biodiversity and Conservation , 13, 2511–2518. Cadi, A., Delmas, V., Prieevot- Julliard, A.C., Joly, P., Pieau, C. & Girondot, M. (2004) Successful reproduction of the introduced slider turtle ( Trachemys scripta elegans ) in the South of France. Aquatic Conservation: Marine And Freshwater Ecosystems, 14, 237–246. Ernst, C.H., Lovich, J.E. & Barbour, R.W. (1994) Turtles of the United States and Canada. Smithsonian Institution Press, Washington, D.C. 578 pp. Kleewein, A. (2014) Natural reproduction of Trachemys scripta troostii (Holbrook, 1836) x Trachemys scripta scripta (Schoepff, 1792) in Austria. Herpetozoa, 26(3/4), 183–185. Kraus, F. (2009) Global trends in alien reptiles and amphibians. Aliens, 28, 13–18. Martínez Silvestre, A., Soler, J., Gorriz, A., Munne, P. & De Roa, E. (2006) Trachemys scripta elegans and other invasive species of chelonians in Catalonia (North-Eastern Iberian Peninsula). Chelonii, 4, 53–54 Perez-Santigosa, N., Díaz-Paniagua, C. & Hidalgo-Vila, J. (2008) The reproductive ecology of exotic Trachemys scripta elegans in an invaded area of southern Europe. Aquatic Conservation: Marine And Freshwater Ecosystems, 18, 1302–1310. Reed, R.N. & Kraus, F. (2010) Invasive reptiles and amphibians: global perspectives and local solutions. Animal Conservation, 13, 3–4. Scalera, R. (2006) Trachemys scripta. DAISIE (Delivering Alien Invasive Species Inventories for Europe). Available at: http://www.europe-aliens.org/(23.08.2013) . Seidel, M.E., Stuart, J.N. & Degenhardt, W.G. (1999) Variation and species status of slider turtles (Emydidae: Trachemys ) in the southwestern United States and adjacent Mexico. Herpetologica , 55(4), 470–487. Semenov, D.V. (2010) Slider turtle, Trachemys scripta elegans, as invasion threat. (Reptilia, Testudines). Russian Journal of Biological Invasions , 1(4), 296–300. Valdeón, A., Crespo-Diaz, A., Egaña-Callejo, A. & Alberto Gosá, A. (2010) Update of the pond slider Trachemys scripta (Schoepff, 1792) records in Navarre (Northern Spain), and presentation of the Aranzadi Turtle Trap for its population control. Aquatic Invasions, 5(3), 297–302. Zenetos, A., Pancucci-Papadopoulou, M.A., Zogaris, S., Papastergiadou, E., Vardakas, L., Aligizaki, K. & Economou, A.N. (2009) Aquatic alien species in Greece: tracking sources, patterns and effects on the ecosystem. Journal of Biological Research, Thessaloniki, 12, 135–172.

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