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Threat or fiction: is the pond slider (Trachemys scripta) really invasive in Central Europe? A case study from Slovenia

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Abstract

Using samples of non-native pond sliders (Trachemys scripta) from three different climatic zones in Slovenia, we perform parentage analyses and use population genetic approaches to find out whether they successfully reproduce and are able to establish populations. Based on 14 highly polymorphic microsatellite loci, we provide evidence for successful reproduction and invasiveness of pond sliders not only for the Mediterranean and sub-Mediterranean regions of Slovenia, but also for the central part of the country having a temperate continental climate. Our results suggest that the pond slider should be classified as an invasive species (introduced species spreading in a non-native region) for Slovenia and other European regions with similar climatic conditions. Since the negative impact of pond sliders is out of question for native European turtle species, we suggest the immediate removal of pond sliders from all habitats. Our study provides for the first time hard evidence for the capability of pond sliders to reproduce in Central Europe. Thus, it contributes to the understanding of the invasiveness of pond sliders in Europe and delivers an important foundation for decision-makers in conservation.

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References

  • Arvy C, Servan J (1998) Imminent competition between Trachemys scripta and Emys orbicularis in France. Mertensiella 10:33–40

    Google Scholar 

  • Bonin F (2004) Concordia Turtle Farm—Die größte Rotwangen-Schmuckschildkröten-Farm der USA. Radiata 13:18–24

    Google Scholar 

  • Bringsøe H (2001) Trachemys scripta (Schoepff, 1792)—Buchstaben-Schmuckschildkröte. In: Fritz U (ed) Handbuch der Reptilien und Amphibien Europas. Vol. 3/IIIa Schildkröten (Testudines) (Bataguridae, Testudinidae, Emydidae). Aula, Wiebelsheim, pp 525–583

    Google Scholar 

  • Bringsøe H (2006) NOBANIS—Invasive alien species fact sheet, Trachemys scripta. Online database of the North European and Baltic Network on Invasive Alien Species. http://www.nobanis.org. Accessed 29 Jan 2015

  • Bruekers J, Uijtterschout G, Brouwer A (2006) Erstnachweis einer natürlichen Vermehrung der Rotwangen-Schmuckschildkröte (Trachemys scripta elegans) auf der griechischen Insel Kos. Schildkr Fokus 3(3):29–34

    Google Scholar 

  • Cadi A, Joly P (2003) Competition for basking places between the endangered European pond turtle (Emys orbicularis galloitalica) and the introduced red-eared slider (Trachemys scripta elegans). Can J Zool 81:1392–1398

    Article  Google Scholar 

  • Cadi A, Delmas V, Prévot-Julliard AC, Joly P, Pieau C, Girondot M (2004) Successful reproduction of the introduced slider turtle (Trachemys scripta elegans) in the south of France. Aquat Conserv 14:237–246

    Article  Google Scholar 

  • Case TJ, Bolger DT (1991) The role of introduced species in shaping the distribution and abundance of island reptiles. Evol Ecol 5:272–290

    Article  Google Scholar 

  • Colautti RI, MacIsaac HJ (2004) A neutral terminology to define ‘invasive’ species. Divers Distrib 10:135–141

    Article  Google Scholar 

  • Crescente A, Sperone E, Paolillo G, Bernabo I, Brunelli E, Tripepi S (2014) Nesting ecology of the exotic Trachemys scripta elegans in an area of Southern Italy (Angitola Lake, Calabria). Amphibia-Reptilia 35:366–370

    Article  Google Scholar 

  • Earl DA, vonHoldt BM (2012) structure harvester: a website and program for visualizing structure output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Ernst CH, Lovich JE (2009) Turtles of the United States and Canada, 2nd edn. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Ficetola GF, Monti A, Schioppa EP (2002) First records of reproduction of Trachemys scripta in the Po Delta. Ann Mus Civ Stor nat Ferrara 5:125–128

    Google Scholar 

  • Ficetola GF, Thuiller W, Schioppa EP (2009) From introduction to the establishment of alien species: bioclimatic differences between presence and reproduction localities in the slider turtle. Divers Distrib 15:108–116

    Article  Google Scholar 

  • Fritz U, Stuckas H, Vargas-Ramírez M, Hundsdörfer AK, Maran J, Päckert M (2012) Molecular phylogeny of Central and South American slider turtles: implications for biogeography and systematics (Testudines: Emydidae: Trachemys). J Zool Syst Evol Res 50:125–136

    Article  Google Scholar 

  • Gemel R, Marolt M, Ochsenhofer G (2005) Ungewöhnliche “Naturbrut“einer Rotwangen-Schmuckschildkröte (Trachemys scripta elegans) in der Steiermark. ÖGH-Aktuell 15:9–11

    Google Scholar 

  • Gibbons JW, Scott DE, Ryan TJ, Buhlmann KA, Tuberville TD, Metts BS, Greene JL, Mills T, Leiden Y, Poppy S, Winne CT (2000) The global decline of reptiles, déjà vu amphibians. Bioscience 50:653–666

    Article  Google Scholar 

  • Glaubitz JC (2004) convert: a user friendly program to reformat diploid genotypic data for commonly used population genetic software packages. Mol Ecol Notes 4:309–310

    Article  CAS  Google Scholar 

  • Goudet J (1995) fstat version 1.2: a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Gurevitch J, Padilla DK (2004) Are invasive species a major cause of extinctions? Trends Ecol Evol 19:470–474

    Article  PubMed  Google Scholar 

  • Hidalgo-Vila J, Ribas A, Florencio M (2006) Falcaustra donanaensis sp. nov. (Nematoda: Kathlaniidae) a parasite of Mauremys leprosa (Testudines, Bataguridae) in Spain. Parasitol Res 99:410–413

    Article  PubMed  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332

    Article  PubMed  PubMed Central  Google Scholar 

  • Kalinowski ST (2004) Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conserv Genet 5:539–543

    Article  CAS  Google Scholar 

  • Kalinowski ST (2005) hp-rare: a computer program for performing rarefaction on measures of allelic diversity. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

  • Kalinowski ST, Wagner AP, Taper ML (2006) ml-relate: a computer program for maximum likelihood estimation of relatedness and relationship. Mol Ecol Notes 6:576–579

    Article  CAS  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program cervus accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    Article  PubMed  Google Scholar 

  • Kleewein A (2014) First record of reproduction in open land of Trachemys scripta troostii (Holbrook, 1836) with the nominate species Trachemys scripta (Schoepff, 1792) in Austria. Herpetozoa 26:183–185

    Google Scholar 

  • Krofel M, Cafuta V, Planinc G, Sopotnik M, Šalamun A, Tome S, Vamberger M, Žagar A (2009) Razširjenost plazilcev v Sloveniji: pregled podatkov, zbranih do leta 2009. Natura Sloveniae, Revija za terensko biologijo, J Field Biol 11:61–99

    Google Scholar 

  • Lowe S, Browne M, Boudjelas S, De Poorter S (2000) 100 of the World’s Worst Invasive Alien Species. A selection from the Global Invasive Species Database. Aliens 12:1–12

    Google Scholar 

  • Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Silvestre A, Soler J, Sole R, Gonzalez FX, Sampere X (1997) Nota sobre la reproducción en condiciones naturales de la Tortuga de Florida (Trachemys scripta elegans) en Masquefa (Catalaña, España). Bol Asoc Herpetol Esp 8:40–42

    Google Scholar 

  • Meyer L, Du Preez L, Bonneau E, Héritier L, Quintana MF, Valdeón A, Sadaoui A, Kechemir-Issad N, Palacios C, Verneau O (2015) Parasite host-switching from the invasive American red-eared slider, Trachemys scripta elegans, to the native Mediterranean pond turtle, Mauremys leprosa, in natural environments. Aquat Invasions 10:79–91

    Article  Google Scholar 

  • Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. PNAS 98:5446–5451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moravec F, Vargas-Vázquez J (1998) Some endohelminths from the freshwater turtle Trachemys scripta from Yucatán, México. J Nat Hist 32:455–468

    Article  Google Scholar 

  • Pearson SH, Arvey HW, Spotila JR (2015) Juvenile invasive red-eared slider turtles negatively impact the growth of native turtles: implications for global freshwater turtle populations. Biol Conserv 186:115–121

    Article  Google Scholar 

  • Pérez-Santigosa N, Díaz-Paniagua C, Hidalgo-Vila J (2008) The reproductive ecology of exotic Trachemys scripta elegans in an invaded area of southern Europe. Aquat Conserv 18:1302–1310

    Article  Google Scholar 

  • Pérez-Santigosa N, Florencio M, Hidalgo-Vila J, Díaz-Paniagua C (2011) Does the exotic invader turtle, Trachemys scripta elegans, compete for food with coexisting native turtles? Amphibia-Reptilia 32:167–175

    Article  Google Scholar 

  • Phillips BL, Shine R (2006) An invasive species induces rapid adaptive change in a native predator: cane toads and black snakes in Australia. Proc R Soc B-Biol Sci 273:1545–1550

    Article  Google Scholar 

  • Phillips BL, Brown GP, Webb JK, Shine R (2006) Invasion and the evolution of speed in toads. Nature 439:803

    Article  CAS  PubMed  Google Scholar 

  • Pieh A, Laufer H (2006) Die Rotwangen-Schmuckschildkröte (Trachemys scripta elegans) in Baden-Württemberg—mit Hinweis auf eine Reproduktion im Freiland. Z Feldherpetol 13:225–234

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Randi E (2008) Detecting hybridization between wild species and their domesticated relatives. Mol Ecol 17:285–293

    Article  PubMed  Google Scholar 

  • Rataj AV, Lindtner-Knific R, Vlahović K, Mavri U, Dovč A (2011) Parasites in pet reptiles. Acta Vet Scand 53:33

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosenberg NA (2004) distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Shen L, Shi H, Wang R, Liu D, Pang X (2011) An invasive species red-eared slider (Trachemys scripta elegans) carrying Salmonella pathogens in Hainan island. Mol Pathogen 2:4

    Google Scholar 

  • Simberloff D (2003) Confronting introduced species: a form of xenophobia? Biol Invasions 5:179–192

    Article  Google Scholar 

  • Simison WB, Sellas AB, Feldheim KA, Parham JF (2013) Isolation and characterization of microsatellite markers for identifying hybridization and genetic pollution associated with red-eared slider turtles (Trachemys scripta elegans). Conserv Genet Resour 5:1139–1140

    Article  Google Scholar 

  • Vamberger M (2009) European pond turtle (Emys orbicularis) in Slovenia. In: Rogner M (ed) European pond turtle (Emys orbicularis). Edition Chimaira, Frankfurt am Main, pp 191–193

    Google Scholar 

  • Vamberger M (2012) Želvica, želva, brezdomka? Temporaria 11:12–15

    Google Scholar 

  • Vamberger M, Lipovšek G, Gregorič M (2012) First reproduction record of Trachemys scripta (Schoepff, 1792), in Slovenia. Herpetozoa 25:76–79

    Google Scholar 

  • van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Wüthrich F (2004) Naturbruten im Jahr 2003 in der Schweiz. Testudo 13:5–20

    Google Scholar 

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Acknowledgments

This study was partially funded from Mestna občina Ljubljana by supporting the project “Izboljšanje habitata močvirske sklednice v Krajinskem parku Tivoli, Rožnik in Šišenski hrib 2014”, which was carried out by the society “Herpetološko društvo – Societas Herpetologica Slovenica”. We would like to thank Anke Müller for help with field work, Katarina Lipovšek, Lara Lipovšek, Marjetka Šemrl, Daniela Vlačič, Irena and Ciril Hanžič for accommodation and care during fieldwork, Marijan Govedič and Ali Šalamun from the Centre for Cartography of Fauna and Flora (CKFF) for the traps, logistic support and making maps of Slovenia. Special thanks also to Rastislav Pogelšek from Sport Fishing Club Renče.

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Authors and Affiliations

  1. Museum of Zoology (Museum für Tierkunde), Senckenberg Dresden, A. B. Meyer Building, 01109, Dresden, Germany

    Benjamin Standfuss, Uwe Fritz & Melita Vamberger

  2. Herpetološko društvo – Societas herpetologica slovenica, Večna pot 11, 1000, Ljubljana, Slovenia

    Gregor Lipovšek & Melita Vamberger

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  1. Benjamin Standfuss
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  2. Gregor Lipovšek
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  4. Melita Vamberger
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Correspondence to Melita Vamberger.

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Standfuss, B., Lipovšek, G., Fritz, U. et al. Threat or fiction: is the pond slider (Trachemys scripta) really invasive in Central Europe? A case study from Slovenia. Conserv Genet 17, 557–563 (2016). https://doi.org/10.1007/s10592-015-0805-2

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