Skip to main content
×
Home
    • Aa
    • Aa
  • Get access
    Check if you have access via personal or institutional login
  • Cited by 12
  • Cited by
    This article has been cited by the following publications. This list is generated based on data provided by CrossRef.

    Du Preez, Louis and Van Rooyen, Michelle 2015. A new polystomatid (Monogenea, Polystomatidae) from the mouth of the North American freshwater turtle Pseudemys nelsoni. ZooKeys, Vol. 539, p. 1.


    TINSLEY, RICHARD C. and TINSLEY, MATTHEW C. 2016. Tracing ancient evolutionary divergence in parasites. Parasitology, p. 1.


    Domènech, Francesc Marquina, Rafael Soler, Lydia Valls, Luis Aznar, Francisco Javier Fernández, Mercedes Navarro, Pilar and Lluch, Javier 2016. Helminth fauna of the invasive American red-eared sliderTrachemys scriptain eastern Spain: potential implications for the conservation of native terrapins. Journal of Natural History, Vol. 50, Issue. 7-8, p. 467.


    Doszpoly, Andor Wellehan, James F.X. Childress, April L. Tarján, Zoltán L. Kovács, Endre R. Harrach, Balázs and Benkő, Mária 2013. Partial characterization of a new adenovirus lineage discovered in testudinoid turtles. Infection, Genetics and Evolution, Vol. 17, p. 106.


    Silbernagel, C Clifford, DL Bettaso, J Worth, S and Foley, J 2013. Prevalence of selected pathogens in western pond turtles and sympatric introduced red-eared sliders in California, USA. Diseases of Aquatic Organisms, Vol. 107, Issue. 1, p. 37.


    Héritier, Laurent Badets, Mathieu Du Preez, Louis H. Aisien, Martins S.O. Lixian, Fan Combes, Claude and Verneau, Olivier 2015. Evolutionary processes involved in the diversification of chelonian and mammal polystomatid parasites (Platyhelminthes, Monogenea, Polystomatidae) revealed by palaeoecology of their hosts. Molecular Phylogenetics and Evolution, Vol. 92, p. 1.


    Berthier, Pauline Du Preez, Louis Raharivololoniana, Liliane Vences, Miguel and Verneau, Olivier 2014. Two new species of polystomes (Monogenea: Polystomatidae) from the anuran host Guibemantis liber. Parasitology International, Vol. 63, Issue. 1, p. 108.


    Franch, M. Montori, A. Sillero, N. and Llorente, G. A. 2015. Temporal analysis of Mauremys leprosa (Testudines, Geoemydidae) distribution in northeastern Iberia: unusual increase in the distribution of a native species. Hydrobiologia, Vol. 757, Issue. 1, p. 129.


    Stanley, Margaret C Beggs, Jacqueline R Bassett, Imogen E Burns, Bruce R Dirks, Kim N Jones, Darryl N Linklater, Wayne L Macinnis-Ng, Cate Simcock, Robyn Souter-Brown, Gayle Trowsdale, Sam A and Gaston, Kevin J 2015. Emerging threats in urban ecosystems: a horizon scanning exercise. Frontiers in Ecology and the Environment, Vol. 13, Issue. 10, p. 553.


    Iglesias, R García-Estévez, JM Ayres, C Acuña, A and Cordero-Rivera, A 2015. First reported outbreak of severe spirorchiidiasis in Emys orbicularis, probably resulting from a parasite spillover event. Diseases of Aquatic Organisms, Vol. 113, Issue. 1, p. 75.


    Salzer, Johanna S. Pinto, C. Miguel Grippi, Dylan C. Williams-Newkirk, Amanda Jo Peterhans, Julian Kerbis Rwego, Innocent B. Carroll, Darin S. and Gillespie, Thomas R. 2016. Impact of Anthropogenic Disturbance on Native and Invasive Trypanosomes of Rodents in Forested Uganda. EcoHealth,


    Allender, M.C. Mitchell, M.A. Torres, T. Sekowska, J. and Driskell, E.A. 2013. Pathogenicity of Frog Virus 3-like Virus in Red-eared Slider Turtles (Trachemys scripta elegans) at Two Environmental Temperatures. Journal of Comparative Pathology, Vol. 149, Issue. 2-3, p. 356.


    ×

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)
  • DOI: http://dx.doi.org/10.1017/S0031182011000333
  • Published online: 18 July 2011
Abstract
SUMMARY

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.

Copyright
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: verneau@univ-perp.fr
Linked references
Hide All

This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

G. Alarcos Izquierdo , F. Flechoso del Cuerto , A. Rodríguez-Pereira and M. Lizana Avia (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

P. K. Anderson , A. A. Cunningham , N. G. Patel , F. J. Morales , P. R. Epstein and P. Daszak (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

A. Bertolero and D. Oro (2009). Conservation diagnosis of reintroducing Mediterranean pond turtles: what is wrong? Animal Conservation 12, 581591. doi:10.1111/j.1469-1795.2009.00284.x

F. Bonin , B. Devaux and A. Dupré (1998). Toutes les Tortues du Monde. Delachaux et Niestlé, Lausanne. ISBN-13: 978-2603010242

A. Cadi , V. Delmas , A.-C. Prévot-Julliard , P. Joly , C. Pieau and M. Girondot (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

A. Cadi and P. Joly (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

A. Cadi and P. Joly (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

T.-H. Chen (2006). Distribution and status of the introduced red-eared slider (Trachemys scripta elegans) in Taiwan. In Assessment and Control of Biological Invasion Risks (eds. F. Koike , M. N. Clout , M. Kawamichi , M. De Poorter and K. Iwatsuki ), pp. 187195. Shoukadoh Book sellers, Kyoto, Japan and IUCN, Gland, Switzerland. ISBN-13: 978-4879746047

K. Clay (2003). Parasites lost. Nature 421, 585586. doi:10.1038/421585a

P. Daszak , L. Berger , A. A. Cunningham , A. D. Hyatt , D. E. Green and R. Speare (1999). Emerging infectious diseases and amphibian population declines. Emerging Infectious Diseases 5, 735748.

P. Daszak , A. A. Cunningham and A. D. Hyatt (2000). Emerging infectious diseases of wildlife – Threats to biodiversity and human health. Science 287, 443449. doi:10.1126/science.287.5452.443

L. H. Du Preez and L. H. S. Lim (2000). Neopolystoma liewi sp. n. (Monogenea: Polystomatidae) from the eye of the Malayan box turtle (Cuora amboinensis). Folia Parasitologica 47, 1116.

N. C. Ellstrand and K. A. Schierenbeck (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

G. F. Ficetola , W. Thuiller and E. Padoa-Schioppa (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

S. Guindon and O. Gascuel (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696704. doi:10.1080/10635150390235520

P. A. W. Harper , D. C. Hammond and W. P. Heuschele (1982). A herpesvirus-like agent associated with a pharyngeal abscess in a desert tortoise. Journal of Wildlife Diseases 18, 491494.

P. D. Harwood (1932). The helminths parasitic in the Amphibia and Reptilia of Houston, Texas and vicinity. Proceedings of the United States National Museum 81, 171.

J. Hidalgo-Vila , C. Díaz-Paniagua , C. de Frutos-Escobar , C. Jiménez-Martínez and N. Pérez-Santigosa (2007). Salmonella in free living terrestrial and aquatic turtles. Veterinary Microbiology 119, 311315. doi:10.1016/j.rvsc.2008.01.011

J. Hidalgo-Vila , C. Díaz-Paniagua , N. Pérez-Santigosa , C. de Frutos-Escobar and A. Herrero-Herrero (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

J. Hidalgo-Vila , C. Díaz-Paniagua , A. Ribas , M. Florencio , N. Pérez-Santigosa and J. C. Casanova (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

J. P. Huelsenbeck and F. Ronquist (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754755. doi:10.1093/bioinformatics/17.8.754

G. R. Huxel (1999). Rapid displacement of native species by invasive species: effects of hybridization. Biological Conservation 89, 143152. doi:10.1016/S0006-3207(98)00153-0

R. M. Keane and M. J. Crawley (2002). Exotic plant invasions and the enemy release hypothesis. Trends in Ecology & Evolution 17, 164170. doi:10.1016/S0169-5347(02)02499-0

K. H. Kikillus , K. M. Hare and S. Hartley (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

D. T. J. Littlewood , K. Rohde and K. A. Clough (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

A. D. Mihalca , C. Gherman , I. Ghira and V. Cozma (2007). Helminth parasites of reptiles (Reptilia) in Romania. Parasitology Research 101, 491492. doi:10.1007/s00436-007-0486-y

A. D. Mihalca , K. Racka , C. Gherman and D. T. Lonescu (2008). Prevalence and intensity of blood apicomplexan infections in reptiles from Romania. Parasitology Research 102, 10811083. doi:10.1007/s00436-008-0912-9

C. E. Mitchell and A. G. Power (2003). Release of invasive plants from fungal and viral pathogens. Nature 421, 625627. doi:10.1038/nature01317

H. A. Mooney and E. E. Cleland (2001). The evolutionary impact of invasive species. Proceedings of the National Academy of Sciences, USA 98 (Suppl.) S446S451. doi:10.1073/pnas.091093398

F. Pasmans , P. De Herdt , J. Dewulf and F. Haesebrouck (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

N. Perez-Santigosa , C. Diaz-Paniagua and J. Hidalgo-Vila (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

T. R. Platt (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

N. Polo-Cavia , P. López and J. Martín (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

N. Polo-Cavia , P. López and J. Martín (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

N. Polo-Cavia , A. Gonzalo , P. López and J. Martín (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

N. Polo-Cavia , P. López and J. Martín (2010 b). Competitive interactions during basking between native and invasive freshwater turtle species. Biological Invasions 12, 21412152. doi:10.1007/s10530-009-9615-0

N. Polo-Cavia , P. López and J. Martín (2011). Aggressive interactions during feeding between native and invasive freshwater turtles. Biological Invasions (in press). doi:10.1007/s10530-010-9897-2

D. Posada and K. A. Crandall (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817818. doi:10.1093/bioinformatics/14.9.817

J. Prenter , C. MacNeil , J. T. A. Dick and A. M. Dunn (2004). Roles of parasites in animal invasions. Trends in Ecology & Evolution 19, 385390. doi:10.1016/j.tree.2004.05.002

N. F. Ramsay , P. K. A. Ng , R. M. O'riordan and L. M. Chou (2007). The red-eared slider (Trachemys scripta elegans) in Asia: a review. In Biological Invaders in Inland Waters: Profiles, Distribution, and Threat (ed. F. Gherardi ), pp. 161174. Springer series in Invasion Ecology. ISBN-13: 978-1402060281

J. P. M. Richarson and D. R. Brooks (1987). Polystomoidella mayesi n. sp. (Monogenea: Polystomatidae) from the urinary bladder of a Malaysian box turtle, Cuora amboinensis. Canadian Journal of Zoology 65, 15671569.

C. A. Rudolphi (1819). Entozoorum synopsis cui accedunt mantissa duplex et indices locupletissimi. Berolini.

P. Salo , E. Korpimäki , P. B. Banks , M. Nordström and C. R. Dickman (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

P. Segade , C. Crespo , C. Ayres , A. Cordero , M. C. Arias , J. M. García-Estévez and R. I. Iglesias Blanco (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

K. Shea and P. Chesson (2002). Community ecology theory as a framework for biological invasions. Trends in Ecology & Evolution 17, 170176. doi:10.1016/S0169-5347(02)02495-3

H. W. Stunkard (1916). On the anatomy and relationships of some North American trematodes. Journal of Parasitology 3, 2127.

H. W. Stunkard (1924). On some trematodes from Florida turtles. Transactions of the American Microscopical Society 43, 97117.

K. Tamura , J. Dudley , M. Nei and S. Kumar (2007). MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 15961599. doi:10.1093/molbev/msm092


J. D. Thompson , D. G. Higgins and T. J. Gibson (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

D. M. Tompkins , A. W. Sainsbury , P. Nettleton , D. Buxton and J. Gurnell (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

M. E. Torchin , K. D. Lafferty , A. P. Dobson , V. J. McKenzie and A. M. Kuris (2003). Introduced species and their missing parasites. Nature 421, 628630. doi:10.1038/nature01346

M. E. Torchin , K. D. Lafferty and A. M. Kuris (2001). Release from parasites as natural enemies: increased performance of a globally introduced marine crab. Biological Invasions 3, 333345. doi:10.1023/A:1015855019360

Y. Une , K. Uemura , Y. Nakano , J. Kamiie , T. Ishibashi and Y. Nomura (1999). Herpesvirus infection in tortoises (Malacochersus tornieri and Testudo horsfieldii). Veterinary Pathology 36, 624627. doi:10.1354/vp.36-6-624

A. Valdeón , A. Crespo-Diaz , A. Egaňa-Callejo and A. Gosá (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

O. Verneau , S. Bentz , N. D. Sinnappah , L. Du Preez , I. Whittington and C. Combes (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

O. Verneau , L. H. Du Preez , V. Laurent , L. Raharivololoniaina , F. Glaw and M. Vences (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

P. M. Vitousek , H. A. Mooney , J. Lubchenco and J. M. Metillo (1997). Human domination of hearth's ecosystems. Science 277, 494499. doi:10.1126/science.277.5325.494

Recommend this journal

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

Parasitology
  • 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? *
×

Keywords:

Type Description Title
UNKNOWN
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)

 Unknown (34 KB)
34 KB