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Introduction and invasion of the red-eared slider and its parasites in freshwater ecosystems of Southern Europe: risk assessment for the European pond turtle in wild environments

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Abstract

The North American red-eared slider Trachemys scripta elegans, which is nowadays considered among the world’s worst invasive species, could constitute a real threat to native freshwater turtles. Because this species shares the same habitats of the European pond turtle Emys orbicularis since its introduction in the European wetlands, we surveyed populations of both alien and indigenous species in France and Spain in order to determine the diversity of platyhelminth parasites (Monogenea, Polystomatidae) in natural environments and to evaluate the levels of risks associated with parasitism. DNA barcoding procedure based on partial cytochrome c oxydase I sequences revealed ten monogenean parasite species within E. orbicularis populations and/or captive animals among which at least eight could be considered as introduced parasites from American freshwater turtles. Results indicated that host switching could have occurred either in natural environments or in captivity, when indigenous turtles were kept with exotic species, demonstrating that captive turtles could act as reservoirs of parasites. The presence of non-native parasite species within wild populations of E. orbicularis in the European freshwater ecosystems also highlighted the risks that these parasites may pose on the survival of natural turtle’s populations and on the dynamics of native parasites.

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References

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

    Google Scholar 

  • Barnosky AD, Matzke N, Tomiya S, Wogan GOU, Swartz B, Quental TB, Marshall C, McGuire JL, Lindsey EL, Maguire KC, Mersey B, Ferrer EA (2011) Has the Earth’s sixth mass extinction already arrived? Nature 471:51–57

    Article  CAS  PubMed  Google Scholar 

  • Barry J, McLeish J, Dodd JA, Turnbull JF, Boylan P, Adams CE (2014) Introduced parasite Anguillicola crassus infection significantly impedes swim bladder function in the European eel Anguilla anguilla (L.). J Fish Dis 37:921–924

    Article  CAS  PubMed  Google Scholar 

  • Buhlmann KA, Akre TSB, Iverson JB, Karapatakis D, Mittermeier RA, Georges A, Rhodin AGJ, Van Dijk PP, Gibbons JW (2009) A global analysis of tortoise and freshwater turtle distributions with identification of priority conservation areas. Chelonian Conserv Biol 8:116–149

    Article  Google Scholar 

  • Butchart SHM, Walpole M, Collen B et al (2010) Global biodiversity: indicators of recent declines. Science 328:1164–1168

    Article  CAS  PubMed  Google Scholar 

  • Böhm M, Collen B, Baillie JEM et al (2013) The conservation status of the world’s reptiles. Biol Conserv 157:372–385

    Article  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, 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). Biodivers Conserv 13:2511–2518

    Article  Google Scholar 

  • Cagle FR (1939) A system of marking turtles for future identification. Copeia 3:170–173

    Article  Google Scholar 

  • Ceballos G, García A, Ehrlich PR (2010) The sixth extinction crisis: loss of animal populations and species. J Cosmol 8:1821–1831

    Google Scholar 

  • Chapin FS III, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, Reynolds HL, Hooper DU, Lavorel S, Sala OE, Hobbie SE, Mack MC, Díaz S (2000) Consequences of changing biodiversity. Nature 405:234–242

    Article  CAS  PubMed  Google Scholar 

  • Cheylan M (1998) Evolution of the distribution of the European pond turtle in the French Mediterranean area since the Post-Glacial. Mertensiella 10:47–65

    Google Scholar 

  • Cheylan M, Courtin J (1976) La consommation de la tortue cistude Emys orbicularis (L.) au post-glaciaire dans la grotte de Fontbregoua (Salernes-Var). Bull Mus Hist nat Marseille 36:41–46

    Google Scholar 

  • Cheylan M, Poitevin F (2003) Les tortues du site de Lattara (IVe s. av. n. è.- IIe s. de n. è.): Intérêt archéozoologique et biologique. Lattara 16:137–145

    Google Scholar 

  • Clavero M, Garciaberthou E (2005) Invasive species are a leading cause of animal extinctions. Trends Ecol Evol 20:110–110

    Article  PubMed  Google Scholar 

  • Clavero M, Brotons L, Pons P, Sol D (2009) Prominent role of invasive species in avian biodiversity loss. Biol Cons 142:2043–2049

    Article  Google Scholar 

  • Cox NA, Temple HJ (2009) European red list of reptiles. Office for official publications of the European communities, Luxembourg

    Google Scholar 

  • Cox NA, Chanson J, Stuart S (2006) The status and distribution of reptiles and amphibians of the Mediterranean Basin–IUCN. Gland, Switzerland and Cambridge, UK

    Book  Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife-threats to biodiversity and human health. Science 287:443–449

    Article  CAS  PubMed  Google Scholar 

  • Domènech F, Marquina R, Soler L, Valls L, Aznar FJ, Fernández M, Navarro P, Lluch J (2015) Helminth fauna of the invasive American red-eared slider Trachemys scripta in eastern Spain: potential implications for the conservation of native terrapins. J Nat Hist. doi:10.1080/00222933.2015.1062931

    Google Scholar 

  • Du Preez LH, Maritz MF (2006) Demonstrating morphometric protocols using polystome marginal hooklet measurements. Syst Parasitol 63:1–15

    Article  PubMed  Google Scholar 

  • Fattizzo T (2004) Distribution and conservational problems of Emys orbicularis in Salento (South Apulia, Italy). Biologia 59:13–18

    Google Scholar 

  • Ferri F, Barbuto M, Bain O, Galimberti A, Uni S, Guerrero R, Ferté H, Bandi C, Martin C, Casiraghi M (2009) Integrated taxonomy: traditional approach and DNA barcoding for the identification of filarioid worms and related parasites (Nematoda). Front Zool 6:1–12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ficelota GF, Monti A, Padoa-Schioppa E (2002) First record of reproduction of Trachemys scripta in the Po Delta. Ann Mus Civ St Nat Ferrara 5:125–128

    Google Scholar 

  • Ficetola GF, Thuiller W, Padoa-Schioppa E (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 

  • Flint M, Patterson-Kane JC, Limpus CJ, Work TM, Blair D, Mills PC (2009) Postmortem diagnostic investigation of disease in free-ranging marine turtle populations: a review of common pathologic findings and protocols. J Vet Diagn Invest 21:733–759

    Article  PubMed  Google Scholar 

  • Fritz U, Ayaz D, Hundsdörfer AK, Kotenko T, Guicking D, Wink M, Tok CV, Çiçek K, Buschbom J (2009) Mitochondrial diversity of European pond turtles (Emys orbicularis) in Anatolia and the Ponto-Caspian Region: multiple old refuges, hotspot of extant diversification and critically endangered endemics. Org Divers Evol 9:100–114

    Article  Google Scholar 

  • Gendre T, Verneau O, Palacios C (2013) Projet « Florida » . Interactions entre une espèce envahissante, la tortue de Floride, et deux tortues patrimoniales en Languedoc-Roussillon, la cistude d’Europe (Emys orbicularis) et l’émyde lépreuse (Mauremys leprosa). Conservatoire d’espaces naturels Languedoc-Roussillon

  • Gibbons PM, Steffes ZJ (2013) Emerging infectious diseases of chelonians. Vet Clin Exot Anim 16:303–317

    Article  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 

  • Gozlan R, St-Hilaire S, Feist SW, Martin P, Kent ML (2005) Disease threat to European fish. Nature 435:1046

    Article  CAS  PubMed  Google Scholar 

  • Harwood PD (1931) Some parasites from Oklahoma turtles. J Parasitol 18:98–101

    Article  Google Scholar 

  • Hays DW, McAllister KR, Richardson SA, Stinson DW (1999) Washington State recovery plan for the western pond turtle. Wash Dept Fish and Wild, Olympia

    Google Scholar 

  • Henke SE, Pence DB, Rue MT (1990) Urinary bladders of freshwater turtles as a renal physiology model potentially biased by monogenean infections. Lab Anim Sci 40:172–177

    CAS  PubMed  Google Scholar 

  • Hidalgo-Vila J, Díaz-Paniagua C, Ribas A, Florencio M, Pérez-Santigosa N, Casanova JC (2009) Helminth communities of the exotic introduced turtle, Trachemys scripta elegans in southwestern Spain: transmission from native turtles. Res Vet Sci 86:463–465

    Article  CAS  PubMed  Google Scholar 

  • Holland DC (1991) A synopsis of the ecology and current status of the western pond turtle (Clemmys marmorata) in 1991. Report to USDIFish and Wildlife Service, National Ecology Research Center, San Simeon, California

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Hulme PE (2007) Biological invasions in Europe: drivers, pressures, states, impacts and responses. Environ Sci Technol 25:56–80

    Google Scholar 

  • Iglesias R, García-Estévez JM, Ayres C, Acuña A, Cordero-Rivera A (2015) First reported outbreak of severe spirorchiidiasis in Emys orbicularis, probably resulting from a parasite spillover event. Dis Aquat Organ 113:75–80

    Article  PubMed  Google Scholar 

  • Jones K, Ariel E, Burgess G, Read M (2016) A review of fibropapillomatosis in green turtles (Chelonia mydas). Vet J 212:48–57

    Article  CAS  PubMed  Google Scholar 

  • Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM (2009) Parasite spillback: a neglected concept in invasion ecology? Ecology 90:2047–2056

    Article  CAS  PubMed  Google Scholar 

  • Knoepffler L-P, Combes C (1977) Présence en Corse de Polystomoides ocellatum (Rudolphi, 1819) chez Emys orbicularis (L., 1758) (Chelonia, Emydidae). Considérations sur la répartition mondiale du genre Polystomoides. Vie Milieu 27:221–230

    Google Scholar 

  • Lambertucci SA, Trejo A, Di Martino S, Sánchez-Zapata JA, Donázar JA, Hiraldo F (2009) Spatial and temporal patterns in the diet of the Andean condor: ecological replacement of native fauna by exotic species. Anim Conserv 12:338–345

    Article  Google Scholar 

  • Littlewood DTJ, Rohde K, Clough KA (1997) Parasite speciation within or between host species? Phylogenetic evidence from site-specific polystome monogeneans. Int J Parasitol 27:1289–1297

    Article  CAS  PubMed  Google Scholar 

  • Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the world’s worst invasive alien species. A selection from the global invasive species database. Hollands Printing Ltd, Auckland

    Google Scholar 

  • Lutz CG (2000) Pet turtle production. SRAC Publication (Mississipi State Univ), vol 439, pp 1–4

  • Lymbery AJ, Morine M, Kanani HG, Beatty SJ, Morgan DL (2014) Co-invaders: the effects of alien parasites on native hosts. Int J Parasitol Parasites Wildl 3:171–177

    Article  PubMed  PubMed Central  Google Scholar 

  • Mack M, D’Antonio CM (1998) Impacts of biological invasions on disturbance regimes. TREE 13:195–198

    CAS  PubMed  Google Scholar 

  • Masin S, Bonardi A, Padoa-Schioppa E, Bottoni L, Ficetola GF (2014) Risk of invasion by frequently traded freshwater turtles. Biol Invasions 16:217–231

    Article  Google Scholar 

  • Meyer (2014) Parasite diversity within native and invasive terrapins: implications for conservation. Thesis dissertation, North West University and University of Perpignan Via Domitia

  • 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 

  • Miller HA (1998) Urinary diseases of reptiles: pathophysiology and diagnosis. Semin Avian Exot Pet Med 7:93–103

    Article  Google Scholar 

  • Mooney HA, Cleland E (2001) The evolutionary impact of invasive species. Proc Natl Acad Sci USA 98:446–451

    Google Scholar 

  • Nishizawa H, Tabata R, Hori T, Mitamura H, Arai N (2014) Feeding kinematics of freshwater turtles: what advantage do invasive species possess? Zoology 117:315–318

    Article  PubMed  Google Scholar 

  • Novaro AJ, Funes MC, Walker RS (2000) Ecological extinction of native prey of a carnivore assemblage in Argentine Patagonia. Biol Conserv 92:25–33

    Article  Google Scholar 

  • Oi M, Araki J, Matsumoto J, Nogami S (2012) Helminth fauna of a turtle species introduced in Japan, the red-eared slider turtle (Trachemys scripta elegans). Res Vet Sci 93:826–830

    Article  CAS  PubMed  Google Scholar 

  • Paul AA (1938) Life history studies of North American freshwater polystomes. J Parasitol 24:489–510

    Article  Google Scholar 

  • Pearson SH, Avery 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 

  • Peeler EJ, Oidtmann BC, Midtlyng PJ, Miossec L, Gozlan RE (2011) Non-native aquatic animals introductions have driven disease emergence in Europe. Biol Invasions 13:1291–1303

    Article  Google Scholar 

  • Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288

    Article  Google Scholar 

  • Platt TR (2000) Neopolystoma fentoni n. sp. (Monogenea: Polystomatidae) a parasite of the conjunctival sac of freshwater turtles in Costa Rica. Mem Inst Oswaldo Cruz 95:833–837

    Article  CAS  PubMed  Google Scholar 

  • Pleguezuelos JM, Márquez R, Lizana M (2002) Atlas y libro rojo de los anfibios y reptiles de España. Dirección General de Conservación de la Naturaleza-Asociación Herpetologica Española (2nd printing), Madrid, 587 pp

  • Polo-Cavia N, López P, Martin J (2008) Interspecific differences in responses to predation risk may confer competitive advantages to invasive freshwater turtle species. Ethology 114:115–123

    Article  Google Scholar 

  • Polo-Cavia N, López P, Martin J (2009a) Interspecific differences in chemosensory responses of freshwater turtles: consequences for competition between native and invasive species. Biol Invasions 11:431–440

    Article  Google Scholar 

  • Polo-Cavia N, López P, Martin J (2009b) Interspecific differences in heat exchange rates may affect competition between introduced and native freshwater turtles. Biol Invasions 11:1755–1765

    Article  Google Scholar 

  • Polo-Cavia N, López P, Martin J (2010) Competitive interactions during basking between native and invasive freshwater turtle species. Biol Invasions 12:2141–2152

    Article  Google Scholar 

  • Polo-Cavia N, López P, Martin J (2011) Aggressive interactions during feeding between native and invasive freshwater turtles. Biol Invasions 13:1387–1396

    Article  Google Scholar 

  • Polo-Cavia N, López P, Martin J (2012) Feeding status and basking requirements of freshwater turtles in an invasion context. Physiol Behav 105:1208–1213

    Article  CAS  PubMed  Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • Poulin R, Mouillot D (2003) Host introductions and the geography of parasite taxonomic diversity. J Biogeogr 30:837–845

    Article  Google Scholar 

  • Prévot-Julliard AC, Gousset E, Archinard C, Cadi A, Girondot M (2007) Pets and invasion risks: is the slider turtle strictly carnivorous? Amphib-Reptil 28:139–143

    Article  Google Scholar 

  • R Development Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Roy H (2016) Control wildlife pathogen too. Nature 530:281

    Article  CAS  PubMed  Google Scholar 

  • Rudolphi CA (1819) Entozoorum synopsis cui accedunt mantissa duplex et indices locupletissimi. Berolini. 811 pp

  • Sala OE, Chapin FS III, Armesto JJ (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774

    Article  CAS  PubMed  Google Scholar 

  • Schlaepfer MA, Hoover C, Dodd KJR (2005) Challenges in evaluating the impact of the trade in amphibians and reptiles on wild populations. Bioscience 55:256–264

    Article  Google Scholar 

  • Schumacher J (2006) Selected infectious diseases of wild reptiles and amphibians. J Exot Pet Med 15:18–24

    Article  Google Scholar 

  • Servan J, Arvy C (1997) Introduction de la tortue de Floride Trachemys scripta en France. Un nouveau compétiteur pour les espèces de tortues d’eau douce européennes. Bull Fr Pêche Piscic 344/345:173–177

  • Sherrard-Smith E, Elizabeth A, Chadwick A, Cable J (2014) The impact of introduced hosts on parasite transmission: opisthorchiid infections in American mink (Neovison vison). Biol Invasions 17:115–122

    Article  Google Scholar 

  • Simberloff D (2013) Biological invasions: prospects for slowing a major global change. Elem Sci Anth 1:1–4

    Article  Google Scholar 

  • Stacy BA, Wellehan JFX, Foley AM, Coberley SS, Herbst LH, Manire CA, Garner MM, Brookins MD, Childress AL, Jacobson ER (2008) Two herpesviruses associated with disease in wild Atlantic loggerhead sea turtles (Caretta caretta). Vet Microbiol 126:63–73

    Article  CAS  PubMed  Google Scholar 

  • Steffen W, Grinevald J, Crutzen P, McNeill J (2011) The Anthropocene: conceptual and historical perspectives. Phil Trans R Soc A 369:842–867

    Article  PubMed  Google Scholar 

  • Stunkard HW (1916) On the anatomy and relationships of some North American trematodes. J Parasitol 3:21–27

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Telecky TM (2001) United States import and export of live turtles and tortoises. Turtle Tortoise Newsl l4:8–13

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Todd BD, Willson JD, Gibbons JW (2010) The global status of reptiles and causes of their decline. In: Sparling DW, Linder G, Bishop CA, Krest SK (eds) Ecotoxicology of amphibians and reptiles, 2nd edn. CRC Press, Taylor &Francis Group, Boca Raton, London, New York, pp 47–68

  • Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630

    Article  CAS  PubMed  Google Scholar 

  • UICN France, MNHN & SHF (2009) La liste rouge des espèces menacées en France—Chapitre reptiles et amphibiens de France métropolitaine. Paris, France

  • UICN France, MNHN & SHF (2015) La liste rouge des espèces menacées en France—Chapitre reptiles et amphibiens de France métropolitaine. Paris, France

  • Valdéon A, Rada V, Ayres C, Iglesias R, Longares LA, Lázaro R, Sancho V (2013) Distribution of Polystomoides ocellatum (Monogenea: Polystomatidae) in Spain parasitizing the European pond turtle (Emys orbicularis). 17th European Congress of Herpetology, Veszprêm, Hungary

  • Van Dijk PP, Iverson JB, Rhodin AGJ, Shaffer HB, Bour R (2014) Turtles of the world, 7th edition: annotated checklist of taxonomy, synonymy, distribution with maps, and conservation status. Chelonian Res Monogr 5:329–479

    Google Scholar 

  • Verneau O (2004) Origine et évolution des monogènes Polystomatidae, parasites d’amphibiens et de chéloniens d’eau douce. HDR dissertation, Université de Perpignan Via Domitia

  • Verneau O, Palacios C, Platt T, Alday M, Billard E, Allienne J, Basso C, Du Preez L (2011) Invasive species threat: parasite phylogenetics reveals patterns and processes of hostswitching between non-native and native captive freshwater turtles. Parasitology 138:1778–1792

    Article  CAS  PubMed  Google Scholar 

  • Vitousek PM (1994) Beyond global warming: ecology and global changes. Ecology 75:1861–1876

    Article  Google Scholar 

  • Vitousek PM, D’Antonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468–478

    Google Scholar 

  • Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997a) Human domination of earth’s ecosystems. Science 277:494–499

    Article  CAS  Google Scholar 

  • Vitousek PM, D’Antonio CM, Loope LL, Rejmanek M, Westbrooks R (1997b) Introduced species: a significant component of human-caused global change. N Z J Ecol 21:1–16

    Google Scholar 

  • Warwick C (1991) Conservation of red-eared terrapins, Trachemys scripta elegans: threats from international pet and culinary markets. Testudo 3:34–44

Download references

Acknowledgements

We are grateful to Laurent Barthe, Valérie Bosc, Ludovic Cases, Lionel Courmont, Marine Couronne, Anthony Labouille, Guilhem Mollera, Julie Peinado, Anthony Olivier, Denis Reudet, Zoé Owen-Jones and people from Fédération de l’Hérault pour la Pêche et la Protection du Milieu Aquatique, Maison de la Nature de Lattes and EPTB du Vistre for their help in collecting turtles and/or their parasites in French wetlands, to César Ayres for his help for collecting turtles and/or their parasites in Galicia and to Françoise Malirach, Paul Barbazange and Roger Oller for facilities in collecting polystome eggs in turtle farms. We also thank two anonymous reviewers for their valuable comments. Financial support for this research was provided by grants from the CNRS, région Languedoc-Roussillon and Veolia Eau Perpignan.

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Authors and Affiliations

  1. Univ. Perpignan Via Domitia, Centre de Formation et de Recherche sur les Environnements Méditerranéens, UMR 5110, 66860, Perpignan, France

    Laurent Héritier, Carmen Palacios & Olivier Verneau

  2. CNRS, Centre de Formation et de Recherche sur les Environnements Méditerranéens, UMR5110, 66860, Perpignan, France

    Laurent Héritier, Carmen Palacios & Olivier Verneau

  3. Department of Geography and Regional Planing, University of Zaragoza, Pedro Cerbuna, 12 50009, Zaragoza, Spain

    Aitor Valdeón

  4. Department of Herpetology, Aranzadi Society of Sciences, Zorroagagaina, 11 20014, Donostia-San Sebastián, Gipuzkoa, Spain

    Aitor Valdeón

  5. Laboratoire de Biodiversité et Environnement: Interactions, Génomes, Faculté des Sciences Biologiques, Université des Sciences et de la Technologie Houari Boumedienne, El Alia, 16111, Bab-Ezzouar, Algeria

    Amel Sadaoui & Nadia Kechemir-Issad

  6. Conservatoire d’Espaces Naturels du Languedoc-Roussillon, Le Thèbes, 26 Allée de Mycènes, 34000, Montpellier, France

    Thomas Gendre

  7. Tour du Valat, Centre de Recherche pour la Conservation des Zones Humides Méditerranéennes, Le Sambuc, 13200, Arles, France

    Sébastien Ficheux

  8. Equipe Eco-Evo, UMR 6282 Biogéosciences, Université de Bourgogne, 6 bd Gabriel, 21000, Dijon, France

    Sébastien Ficheux

  9. Département Performances des Systèmes de Production et de Transformation Tropicaux, Station CIRAD de Neufchâteau, 97130, Capesterre-Belle-Eau, Guadeloupe, France

    Salah Bouamer

  10. Unit for Environmental Sciences and Management, North-West University, Potchefstroom, 2520, South Africa

    Louis Du Preez & Olivier Verneau

  11. South African Institute for Aquatic Biodiversity, Somerset Street, Grahamstown, 6139, South Africa

    Louis Du Preez

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  1. Laurent Héritier
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  2. Aitor Valdeón
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  3. Amel Sadaoui
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Correspondence to Olivier Verneau.

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Communicated by Angus Jackson.

This article belongs to the Topical Collection: Invasive species.

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Héritier, L., Valdeón, A., Sadaoui, A. et al. Introduction and invasion of the red-eared slider and its parasites in freshwater ecosystems of Southern Europe: risk assessment for the European pond turtle in wild environments. Biodivers Conserv 26, 1817–1843 (2017). https://doi.org/10.1007/s10531-017-1331-y

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