Skip to main content
    • Aa
    • Aa

Invasive species threat: parasite phylogenetics reveals patterns and processes of host-switching between non-native and native captive freshwater turtles

  • O. VERNEAU (a1), C. PALACIOS (a1), T. PLATT (a2), M. ALDAY (a1), E. BILLARD (a1), J.-F. ALLIENNE (a1), C. BASSO (a3) and L. H. DU PREEZ (a4)...

One of the major threats to biodiversity involves biological invasions with direct consequences on the stability of ecosystems. In this context, the role of parasites is not negligible as it may enhance the success of invaders. The red-eared slider, Trachemys scripta elegans, has been globally considered among the worst invasive species. Since its introduction through the pet trade, T. s. elegans is now widespread and represents a threat for indigenous species. Because T. s. elegans coexists with Emys orbicularis and Mauremys leprosa in Europe, it has been suggested it may compete with the native turtle species and transmit pathogens. We examined parasite transfer from American captive to the two native species that co-exist in artificial pools of a Turtle Farm in France. As model parasite species we used platyhelminth worms of the family Polystomatidae (Monogenea) because polystomes have been described from American turtles in their native range. Phylogenetic relationships among polystomes parasitizing chelonian host species that are geographically widespread show patterns of diversification more complex than expected. Using DNA barcoding to identify species from adult and/or polystome eggs, several cases of host switching from exotic to indigenous individuals were illustrated, corroborating that parasite transmission is important when considering the pet trade and in reintroduction programmes to reinforce wild populations of indigenous species.

Corresponding author
*Corresponding author: Olivier Verneau, UMR 5110 CNRS-UPVD, Centre de Formation et de Recherche sur les Environnements Méditerranéens, Université de Perpignan Via Domitia, 52 Avenue Paul Alduy, 66860 Perpignan Cedex, France. Tel.: 33 4 68 66 21 10. Fax: 33 6 07 47 86 07. E-mail:
Hide All
Alarcos Izquierdo G., Flechoso del Cuerto F., Rodríguez-Pereira A. and Lizana Avia M. (2010). Distribution records of non-native terrapins in Castilla and León region (Central Spain). Aquatic Invasions 5, 303308. doi:10.3391/ai.2010.5.3.08
Anderson P. K., Cunningham A. A., Patel N. G., Morales F. J., Epstein P. R. and Daszak P. (2004). Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends in Ecology & Evolution 19, 535544. doi:10.1016/j.tree.2004.07.021
Arvy C. and Servan J. (1998). Imminent competition between Trachemys scripta and Emys orbicularis in France. Mertensiella 10, 3340.
Bertolero A. (1999). Suivi de la population de cistude Emys orbicularis dans le delta de l'Ebre (Ne Espagne). Chelonii 2, 6368.
Bertolero A. and Oro D. (2009). Conservation diagnosis of reintroducing Mediterranean pond turtles: what is wrong? Animal Conservation 12, 581591. doi:10.1111/j.1469-1795.2009.00284.x
Bonin F., Devaux B. and Dupré A. (1998). Toutes les Tortues du Monde. Delachaux et Niestlé, Lausanne. ISBN-13: 978-2603010242
Cadi A., Delmas V., Prévot-Julliard A.-C., Joly P., Pieau C. and 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, 237246. doi:10.1002/aqc.607
Cadi A. and 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). Canadian Journal of Zoology 81, 13921398. doi:10.1139/z03-108
Cadi A. and Joly P. (2004). Impact of the introduction of the read-eared slider (Trachemys scripta elegans) on survival rates of the European pond turtle (Emys orbicularis). Biodiversity and Conservation 13, 25112518. doi:10.1023/B:BIOC.0000048451.07820.9c
Cadi A. and Miquet A. (2004). A reintroduction programme for the European pond turtle (Emys orbicularis) in Lake Bourget (Savoie, France): first results after two years. Biologia 59, 155159.
Chen T.-H. (2006). Distribution and status of the introduced red-eared slider (Trachemys scripta elegans) in Taiwan. In Assessment and Control of Biological Invasion Risks (eds. Koike F., Clout M. N., Kawamichi M., De Poorter M. and Iwatsuki K.), pp. 187195. Shoukadoh Book sellers, Kyoto, Japan and IUCN, Gland, Switzerland. ISBN-13: 978-4879746047
Clay K. (2003). Parasites lost. Nature 421, 585586. doi:10.1038/421585a
Combes C. and Ktari M. H. (1976). Neopolystoma euzeti n. sp. (Monogenea, Polystomatidae) premier représentant du genre Neopolystoma Price, 1939 en Afrique. Annales de Parasitologie Humaine et Comparée 51, 221225.
Combes C. and Thiery A. (1983). Sur un Polystomoides (Monogenea), parasite du chélonien Clemys caspica au Maroc. Bulletin de l'Institut Scientifique (Rabat) 7, 165170.
Da Silva E. and Blasco M. (1995). Trachemys scripta elegans in Southwestern Spain. Herpetological Review 26, 133134.
Daszak P., Berger L., Cunningham A. A., Hyatt A. D., Green D. E. and Speare R. (1999). Emerging infectious diseases and amphibian population declines. Emerging Infectious Diseases 5, 735748.
Daszak P., Cunningham A. A. and Hyatt A. D. (2000). Emerging infectious diseases of wildlife – Threats to biodiversity and human health. Science 287, 443449. doi:10.1126/science.287.5452.443
Du Preez L. H. and Lim L. H. S. (2000). Neopolystoma liewi sp. n. (Monogenea: Polystomatidae) from the eye of the Malayan box turtle (Cuora amboinensis). Folia Parasitologica 47, 1116.
Du Preez L. H., Raharivololoniaina L., Verneau O. and Vences M. (2010). A new genus of polystomatid parasitic flatworm (Monogenea: Polystomatidae) without free-swimming life stage from the Malagasy poison frogs. Zootaxa 2722, 5468.
Du Preez L. H., Verneau O. and Gross D. (2007). Polystoma floridana n. sp. (Monogenea: Polystomatidae) a parasite in the green tree frog, Hyla cinerea (Schneider), of North America. Zootaxa 1663, 3345.
Eiras J. C. (2005). An overview on the myxosporean parasites in amphibians and reptiles. Acta Parasitologica 50, 267275.
Ellstrand N. C. and Schierenbeck K. A. (2000). Hybridization as a stimulus for the evolution of invasiveness in plants? Proceedings of the National Academy of Sciences, USA 97, 70437050. doi:10.1007/s10681-006-5939-3
Ficetola G. F., Monti A. and Padoa-Schioppa E. (2002). First record of reproduction of Trachemys scripta in the Po Delta. Annali del Museo Civico di Storia Naturale di Ferra 5, 125128.
Ficetola G. F., Thuiller W. and Padoa-Schioppa E. (2009). From introduction to the establishment of alien species: bioclimatic differences between presence and reproduction localities in the slider turtle. Diversity and Distributions 15, 108116. doi:10.1111/j.1472-4642.2008.00516.x
Frye F. L., Oshiro L. S., Dutra F. R. and Carney J. D. (1977). Herpesvirus-like infection in two pacific pond turtles. Journal of the American Veterinary Medical Association 17, 882884.
Gonzales J. P. and Mishra G. S. (1977). Polystomoides tunisiensis n. sp. (Monogenea, Polystomatidae) et Telorchis temimi n. sp. (Digenea, Telorchiidae). Deux nouvelles espèces de Trématodes de tortues paludines de Tunisie. Archives de l'Institut Pasteur de Tunis 54, 2938.
Guindon S. and Gascuel O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696704. doi:10.1080/10635150390235520
Harper P. A. W., Hammond D. C. and Heuschele W. P. (1982). A herpesvirus-like agent associated with a pharyngeal abscess in a desert tortoise. Journal of Wildlife Diseases 18, 491494.
Harwood P. D. (1932). The helminths parasitic in the Amphibia and Reptilia of Houston, Texas and vicinity. Proceedings of the United States National Museum 81, 171.
Hays D. W., McAllister K. R., Richardson S. A. and Stinson D. W. (1999). Washington State Recovery Plan for the Western Pond Turtle. Washington Department of Fish and Wildlife, Olympia, Washington.
Hidalgo-Vila J., Díaz-Paniagua C., de Frutos-Escobar C., Jiménez-Martínez C. and Pérez-Santigosa N. (2007). Salmonella in free living terrestrial and aquatic turtles. Veterinary Microbiology 119, 311315. doi:10.1016/j.rvsc.2008.01.011
Hidalgo-Vila J., Díaz-Paniagua C., Pérez-Santigosa N., de Frutos-Escobar C. and Herrero-Herrero A. (2008). Salmonella in free living exotic and native turtles in pet exotic turtles from SW Spain. Research in Veterinary Science 85, 449452. doi:10.1016/j.rvsc.2008.01.011
Hidalgo-Vila J., Díaz-Paniagua C., Ribas A., Florencio M., Pérez-Santigosa N. and Casanova J. C. (2009). Helminth communities of the exotic introduced turtle, Trachemys scripta elegans in southwestern Spain: transmission from native turtles. Research in Veterinary Science 86, 463465. doi:10.1016/j.rvsc.2008.08.003
Huelsenbeck J. P. and Ronquist F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754755. doi:10.1093/bioinformatics/17.8.754
Huxel G. R. (1999). Rapid displacement of native species by invasive species: effects of hybridization. Biological Conservation 89, 143152. doi:10.1016/S0006-3207(98)00153-0
Keane R. M. and Crawley M. J. (2002). Exotic plant invasions and the enemy release hypothesis. Trends in Ecology & Evolution 17, 164170. doi:10.1016/S0169-5347(02)02499-0
Kikillus K. H., Hare K. M. and Hartley S. (2009). Minimizing false-negatives when predicting the potential distribution of an invasive species: a bioclimatic envelope for the red-eared slider at global and regional scales. Animal Conservation 13, 515. doi:10.1111/j.1469-1795.2008.00299.x
Knoepffler L.-P. and 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, Série C 27, 221230.
Littlewood D. T. J., Rohde K. and Clough K. A. (1997). Parasite speciation within or between host species? Phylogenetic evidence from site-specific polystome monogeneans. International Journal for Parasitology 27, 12891297. doi:10.1016/S0020-7519(97)00086-6
MacCallum G. A. (1918). Studies on the Polystomatidae. Zoopathologica 1, 103120.
Mihalca A. D., Gherman C., Ghira I. and Cozma V. (2007). Helminth parasites of reptiles (Reptilia) in Romania. Parasitology Research 101, 491492. doi:10.1007/s00436-007-0486-y
Mihalca A. D., Racka K., Gherman C. and Lonescu D. T. (2008). Prevalence and intensity of blood apicomplexan infections in reptiles from Romania. Parasitology Research 102, 10811083. doi:10.1007/s00436-008-0912-9
Miquet A. and Cadi A. (2002). Réintroduction de la cistude d'Europe en Savoie. Premier bilan (2000/2001). Bulletin de la Société Herpétologique de France 104, 5461.
Mishra G. S. and Gonzalez J. P. (1978). Les parasites des tortues d'eau douce en Tunisie. Les archives de l'Institut Pasteur de Tunis 55, 303326.
Mitchell C. E. and Power A. G. (2003). Release of invasive plants from fungal and viral pathogens. Nature 421, 625627. doi:10.1038/nature01317
Mooney H. A. and Cleland E. E. (2001). The evolutionary impact of invasive species. Proceedings of the National Academy of Sciences, USA 98 (Suppl.) S446S451. doi:10.1073/pnas.091093398
Mosimann D. and Cadi A. (2004). On the occurrence and viability of the European pond turtle (Emys orbicularis) in Moulin-de-Vert (Geneva, Switzerland): 50 years after first introduction. Biologia 59, 109112.
Pasmans F., De Herdt P., Dewulf J. and Haesebrouck F. (2002). Pathogenesis of infections with Salmonella enterica subsp. enterica serovar Muenchen in the turtle Trachemys scripta scripta. Veterinary Microbiology 87, 315325. doi:10.1016/S0378-1135(02)00081-0
Perez-Santigosa N., Diaz-Paniagua C. and 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, 13021310. doi:10.1002/aqc.974
Platt T. R. (2000). Helminth parasites of the western painted turtle, Chrysemys picta belli (Gray), including Neopolystoma elizabethae n. sp. (Monogenea: Polystomatidae), a parasite of the conjunctival sac. Journal of Parasitology 86, 815818. doi:10.1645/0022-3395(2000)086[0815:HPOTWP]2.0.CO;2
Polo-Cavia N., López P. and Martín J. (2008). Interspecific differences in responses to predation risk may confer competitive advantages to invasive freshwater turtle species. Ethology 114, 115123. doi:10.1111/j.1439-0310.2007.01441.x
Polo-Cavia N., López P. and Martín J. (2009 a). Interspecific differences in chemosensory responses of freshwater turtles: consequences for competition between native and invasive species. Biological Invasions 11, 431440. doi:10.1007/s10530-008-9260-z
Polo-Cavia N., López P. and Martín J. (2009 b). Interspecific differences in heat exchange rates may affect competition between introduced and native freshwater turtles. Biological Invasions 11, 17551765. doi:10.1007/s10530-008-9355-6
Polo-Cavia N., Gonzalo A., López P. and Martín J. (2010 a). Predator recognition of native but not invasive turtle predators by naïve anuran tadpoles. Animal Behaviour 80, 461466. doi:10.1016/j.anbehav.2010.06.004
Polo-Cavia N., López P. and Martín J. (2010 b). Competitive interactions during basking between native and invasive freshwater turtle species. Biological Invasions 12, 21412152. doi:10.1007/s10530-009-9615-0
Polo-Cavia N., López P. and Martín J. (2011). Aggressive interactions during feeding between native and invasive freshwater turtles. Biological Invasions (in press). doi:10.1007/s10530-010-9897-2
Posada D. and Crandall K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817818. doi:10.1093/bioinformatics/14.9.817
Prenter J., MacNeil C., Dick J. T. A. and Dunn A. M. (2004). Roles of parasites in animal invasions. Trends in Ecology & Evolution 19, 385390. doi:10.1016/j.tree.2004.05.002
Ramsay N. F., Ng P. K. A., O'riordan R. M. and Chou L. M. (2007). The red-eared slider (Trachemys scripta elegans) in Asia: a review. In Biological Invaders in Inland Waters: Profiles, Distribution, and Threat (ed. Gherardi F.), pp. 161174. Springer series in Invasion Ecology. ISBN-13: 978-1402060281
Richarson J. P. M. and Brooks D. R. (1987). Polystomoidella mayesi n. sp. (Monogenea: Polystomatidae) from the urinary bladder of a Malaysian box turtle, Cuora amboinensis. Canadian Journal of Zoology 65, 15671569.
Rohde K. (1963). Polystomoides malayi n. sp. (Monogenea, Polystomatidae) aus der Harnblase von Cyclemys amboinensis in Malaya. Zeitschrift für Parasitenkunde 22, 278282.
Rohde K. (1965). Studies on the genus Polystomoides Ward, 1917 (Monogenea). I. Description of 4 Malayan species, a key to the known species, and a comparison of the subcuticular layers in Polystomoides and some digenetic trematodes. Zoologische Jahbuecher Abteilung fuer Systematik Oekologie und Geographie der Tiere 92, 345368.
Rudolphi C. A. (1819). Entozoorum synopsis cui accedunt mantissa duplex et indices locupletissimi. Berolini.
Salo P., Korpimäki E., Banks P. B., Nordström M. and Dickman C. R. (2007). Alien predators are more dangerous than native predators to prey populations. Proceedings of the Royal Society of London. Series B 274, 12371243. doi:10.1098/rspb.2006.0444
Segade P., Crespo C., Ayres C., Cordero A., Arias M. C., García-Estévez J. M. and Iglesias Blanco R. I. (2006). Eimeria species from the european pond turtle, Emys orbicularis (Reptilia: Testudines), in Galicia (NW Spain), with description of two new species. Journal of Parasitology 92, 6972. doi:10.1645/GE-3491.1
Servan J. and 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. Bulletin Français de la Pêche et de la Pisciculture 344/345, 173177.
Shea K. and Chesson P. (2002). Community ecology theory as a framework for biological invasions. Trends in Ecology & Evolution 17, 170176. doi:10.1016/S0169-5347(02)02495-3
Stunkard H. W. (1916). On the anatomy and relationships of some North American trematodes. Journal of Parasitology 3, 2127.
Stunkard H. W. (1924). On some trematodes from Florida turtles. Transactions of the American Microscopical Society 43, 97117.
Swofford D. L. (2002). PAUP*: Phylogenetic Analysis Using Parsimony (* and Other Methods), version 4.0b9 Sinauer Associates, Sunderland, Massachusetts.
Tamura K., Dudley J., Nei M. and Kumar S. (2007). MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 15961599. doi:10.1093/molbev/msm092
Taraschewski H. (2006). Hosts and parasites as aliens. Journal of Helminthology 80, 99128. doi:10.1079/JOH2006364
Telecky T. M. (2001). United States import and export of live turtles and tortoises. Turtle and Tortoise Newsletter. The Newsletter of Chelonian Conservationists and Biologists 4, 813.
Thompson J. D., Higgins D. G. and Gibson T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignments through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 46734680. doi:10.1093/nar/22.22.4673
Tompkins D. M., Sainsbury A. W., Nettleton P., Buxton D. and Gurnell J. (2002). Parapoxvirus causes a deleterious disease in red squirrels associated with UK population declines. Proceedings of the Royal Society of London. Series B 269, 529533. doi:10.1098/rspb.2001.1897
Torchin M. E., Lafferty K. D., Dobson A. P., McKenzie V. J. and Kuris A. M. (2003). Introduced species and their missing parasites. Nature 421, 628630. doi:10.1038/nature01346
Torchin M. E., Lafferty K. D. and Kuris A. M. (2001). Release from parasites as natural enemies: increased performance of a globally introduced marine crab. Biological Invasions 3, 333345. doi:10.1023/A:1015855019360
Une Y., Uemura K., Nakano Y., Kamiie J., Ishibashi T. and Nomura Y. (1999). Herpesvirus infection in tortoises (Malacochersus tornieri and Testudo horsfieldii). Veterinary Pathology 36, 624627. doi:10.1354/vp.36-6-624
Valdeón A., Crespo-Diaz A., Egaňa-Callejo A. and 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, 297302. doi:10.3391/ai.2010.5.3.07
Verneau O. (2004). HDR – Origine et évolution des monogènes Polystomatidae, parasites d'amphibiens et de chéloniens d'eau douce. Université de Perpignan, France.
Verneau O., Bentz S., Sinnappah N. D., Du Preez L., Whittington I. and Combes C. (2002). A view of early vertebrate evolution inferred from the phylogeny of polystome parasites (Monogenea : Polystomatidae). Proceedings of the Royal Society of London. Series B 269, 535543. doi:10.1098/rspb.2001.1899
Verneau O., Du Preez L. H., Laurent V., Raharivololoniaina L., Glaw F. and Vences M. (2009). The double odyssey of Madagascan polystome flatworms leads to new insights on the origins of their amphibian hosts. Proceedings of the Royal Society 276, 15751583. doi: 10.1098/rspb.2008.1530
Vitousek P. M., Mooney H. A., Lubchenco J. and Metillo J. M. (1997). Human domination of hearth's ecosystems. Science 277, 494499. doi:10.1126/science.277.5325.494
Wright R. R. (1879). Contributions to American helminthology. Proceedings of the Canadian Institute 1, 5475.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *


Type Description Title
Supplementary Appendix

Verneau Supplementary Appendix
Appendix S1. Genetic distances (uncorrected p-distances) inferred from comparison of the 55 COI nucleic acid haplotypes (345 aligned positions)

 Word (34 KB)
34 KB


Full text views

Total number of HTML views: 9
Total number of PDF views: 34 *
Loading metrics...

Abstract views

Total abstract views: 263 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 19th October 2017. This data will be updated every 24 hours.