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Narrow phylogeographic origin of five introduced populations of the Siberian chipmunk Tamias (Eutamias) sibiricus (Laxmann, 1769) (Rodentia: Sciuridae) established in France

Abstract

Large native geographical range and number of introduction events are often invoked to explain the successful establishment of alien mammal species. To infer the native geographic range of the Siberian chipmunks Tamias (Eutamias) sibiricus (Lax.) invasion in France, we identified the subspecies that individuals sampled in 5 out of the 11 established populations belonged. Based on craniometrical measures, variation in the mtDNA sequence of the cytochrome b, and alarm call sonogram shape, all French specimens were members of T. (E.) s. barberi which has the smallest geographical range (Korean peninsula) of the three recognized subspecies. An intense pet trade between European countries and Korea until the 1980’s best explains the success in establishment of this small ground-squirrel in France, where it was released mainly by private owners. Size of the native geographical range should be interpreted with caution in explaining the establishment of an invasive species, at least without a precise knowledge of its introduction pathways and taxonomic status.

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References

  • Bertolino S (2009) Animal trade and non-indigenous species introduction: the world-wide spread of squirrels. Divers Distrib 15:701–708

    Article  Google Scholar 

  • Chapuis J-L (2005) Distribution in France of a naturalized companion animal, the Siberian Chipmunk (Tamias sibiricus). Rev Ecol (Terre Vie) 60:239–253

    Google Scholar 

  • Chapuis J-L (2009) Tamias sibiricus (Laxmann), Siberian chipmunk (Sciuridae, Mammalia). In: Vila M, Basnou C, Gollasch S, Josefsson M, Pergl J, Scalera R (eds) One hundred of the most invasive alien species in Europe, chap 12, Handbook of alien species in Europe, DAISIE. Springer, Berlin, p 372

  • Chapuis J-L, Obolenskaya EV, Pisanu B, Lissovsky AA (2011) Datasheet on Tamias sibiricus. CABI, Wellingford, UK (http://www.cabi.org/isc/)

  • Daümer C, Greve C, Hutterer R, Misof B, Haase M (2012) Phylogeography of an invasive land snail: natural range expansion versus anthropogenic dispersal in Theba pisana pisana. Biol Invasions Online First™, 9 February 2012. doi:10.1007/s10530-012-0179-z

  • Dissanayake R, Oshida T (2012) The systematic of the dusky striped squirrel, Funambulus sublineatus (Waterhouse, 1838) (Rodentia: Sciuridae) and its relationships to Layard’s squirrel, Funambulus layardi Blyth, 1849. J Nat Hist 46:91–116

    Article  Google Scholar 

  • Duncan RP, Blackburn TM, Sol D (2003) The ecology of bird introductions. Annu Rev Ecol Evol Syst 34:71–98

    Article  Google Scholar 

  • Forsyth DM, Duncan RP, Bomford M, Moore G (2004) Climatic suitability, life-history traits, introduction effort, and establishment and spread of introduced mammals in Australia. Conserv Biol 18:557–569

    Article  Google Scholar 

  • Gaubert P, Godoy JA, del Cerro I, Palomares F (2009) Early phases of a successful invasion: mitochondrial phylogeography of the common genet (Genetta genetta) within the Mediterranean Basin. Biol Invasions 11:523–546

    Article  Google Scholar 

  • Jobb G (2008) TREEFINDER version of June 2008. Munich, Germany. Distributed by the author (www.treefinder.de)

  • Kawamichi M (1989) Nest structure dynamics and seasonal use of nests by Siberian chipmunks (Eutamias sibiricus). J Mamm 70:44–57

    Article  Google Scholar 

  • Kawamichi M (1996) Ecological factors affecting annual variation in commencement of hibernation in wild chipmunks (Tamias sibiricus). J Mamm 77:731–744

    Article  Google Scholar 

  • Kawamichi M (1999) Ecological aspects of the solitary ranging squirrel, Siberian chipmunk (Tamias sibiricus). Mamm Sci 78:185–187

    Google Scholar 

  • Kawamichi T, Kawamichi M (1993) Gestation period and litter size of Siberian chipmunk Eutamias sibiricus in Hokkaido, northern Japan. J Mamm Soc Jpn 18:105–109

    Google Scholar 

  • Kawamichi T, Kawamichi M, Kishimoto R (1987) Social organization of solitary mammals. In: Ito Y, Brown JL, Kikkawa J (eds) Animal societies: theories and facts. Japan Science Society Press, Tokyo, pp 173–188

    Google Scholar 

  • Koh HS, Wang J, Lee BK, Yang BG, Heo SW, Jang KH, Chun TY (2009) A phylogroup of the Siberian Chipmunk from Korea (Tamias sibiricus barberi) revealed from the mitochondrial DNA cytochrome b gene. Biochem Genet 47:1–7

    PubMed  Article  CAS  Google Scholar 

  • Koh HS, Zhang M, Bayarlkhagva D, Ham EJ, Kim JS, Jang KH, Park NJ (2010) Concordant genetic distinctness of the phylogroup of the Siberian chipmunk from the Korean Peninsula (Tamias sibiricus barberi), reexamined with nuclear DNA c-myc Gene Exon 2 and mtDNA control region sequences. Biochem Genet 48:696–705

    PubMed  Article  CAS  Google Scholar 

  • Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204

    PubMed  Article  Google Scholar 

  • Lee M-Y, Lissovsky AA, Park S-K, Obolenskaya EV, Dokuchaev NE, Zhang Y-P, Yu L, Kim Y-J, Voloshina I, Myslenkov A, Choi T-Y, Min M-S, Lee H (2008) Mitochondrial cytochrome b sequence variations and population structure of Siberian chipmunk (Tamias sibiricus) in Northeastern Asia and population substructure in South Korea. Mol Cells 26:566–575

    PubMed  CAS  Google Scholar 

  • Lee S-J, Jung G, Min M-S, Kim C-K, Lee H, Kim CB, Lee M-Y (2011) Genetic origin identification of Siberian chipmunks (Tamias sibiricus) in pet shops of South Korea. Anim Cells Syst 15:161–168

    Article  Google Scholar 

  • Lissovsky AA, Obolenskaya EV, Emelyanova LG (2006) The structure of voice signals of Siberian chipmunk (Tamias sibiricus Laxmann 1769; Rodentia: Sciuridae). Russ J Theriol 5:93–98

    Google Scholar 

  • Marmet J (2008) Traits d’histoire de vie du Tamia de Sibérie Tamias sibiricus, espèce exotique naturalisée dans la forêt de Sénart (Essonne): démographie, biologie de la reproduction, occupation de l’espace et dispersion. Unpublished PhD thesis, MNHN, Paris, France, 171 pp

  • Marmet J, Pisanu B, Chapuis J-L (2009) Home range, range overlap, and site fidelity of introduced Siberian chipmunks in a suburban French forest. Eur J Wildl Res 55:497–504

    Article  Google Scholar 

  • Marmet J, Pisanu B, Chapuis J-L (2011) Natal dispersal of introduced Siberian chipmunks, Tamias sibiricus, in a suburban forest. J Ethol 29:23–29

    Article  Google Scholar 

  • Marsot M, Sigaud M, Chapuis J-L, Ferquel E, Cornet M, Vourc’h G (2011) Introduced Siberian chipmunks (Tamias sibiricus barberi) harbour more diverse Borrelia burgdorferi sensu lato genospecies than native bank voles (Myodes glareolus). Appl Environ Microbiol 77:5716–5721

    PubMed  Article  CAS  Google Scholar 

  • Obolenskaya EV (2008) Distribution patterns of the Siberian chipmunk (Tamias sibiricus Laxmann, 1769). Mosc Univ Publ 49:265–279 (in Russian with English summary)

    Google Scholar 

  • Obolenskaya EV, Lee M, Dokuchaev NE, Oshida T, Lissovsky AA (2009) The diversity of Palaearctic chipmunks (Tamias, Sciuridae). Mammalia 73:281–298

    Article  Google Scholar 

  • Pisanu B, Marsot M, Marmet J, Chapuis J-L, Réale D, Vourc’h G (2010) Introduced Siberian chipmunks are more heavily infested by ixodid ticks than are native bank voles in a suburban forest in France. Int J Parasitol 40:1277–1283

    PubMed  Article  CAS  Google Scholar 

  • Vourc’h G, Marmet J, Chassagne M, Bord S, Chapuis J-L (2007) Borrelia burgdorferi sensu lato in Siberian chipmunks (Tamias sibiricus) introduced in suburban forests in France. Vector Borne Zoonotic Dis 7:637–641

    PubMed  Article  Google Scholar 

  • Zheng X, Arbogast BS, Kenagy GJ (2003) Historical demography and genetic structure of sister species: deer mice (Peromyscus) in the North American temperate rain forest. Mol Ecol 12:711–724

    PubMed  Article  Google Scholar 

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Acknowledgments

The Region Ile-de-France, the Conseil Général des Hauts-de-Seine and the Office National des Forêts funded this study. Françoise Cardou kindly commented on this paper and improved the English language.

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Correspondence to J.-L. Chapuis.

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Pisanu, B., Obolenskaya, E.V., Baudry, E. et al. Narrow phylogeographic origin of five introduced populations of the Siberian chipmunk Tamias (Eutamias) sibiricus (Laxmann, 1769) (Rodentia: Sciuridae) established in France. Biol Invasions 15, 1201–1207 (2013). https://doi.org/10.1007/s10530-012-0375-x

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  • DOI: https://doi.org/10.1007/s10530-012-0375-x

Keywords

  • Siberian chipmunk
  • Tamias (Eutamias) sibiricus
  • Introduced species
  • Invasive pet
  • Phylogeography
  • Species range
  • Taxonomy