Advertisement

Mammalian Biology

, Volume 80, Issue 6, pp 518–526 | Cite as

Range expansion of Pallas’s squirrel (Callosciurus erythraeus) introduced in southern France: Habitat suitability and space use

  • Anne Dozières
  • Benoît Pisanu
  • Stefaniya Kamenova
  • Fiona Bastelica
  • Olivier Gerriet
  • Jean-Louis ChapuisEmail author
Original Investigation

Abstract

The study of space use and population density in different habitats is an important step in understanding the expansion process of an introduced species and in gathering useful knowledge for management actions. Pallas’s squirrel (Callosciurus erythraeus) was introduced on the Cap d’Antibes (southeastern France) at the end of the 1960s. We used direct observations from a grid map centred onto the known historical distribution to document the expanding range of Pallas’s squirrel. We assessed habitat suitability in the invaded area through distance sampling and nest counts and examined space use by quantifying the size of the home range and intra- and inter-sexual overlap based on radio-tracking in a suitable habitat. Our results confirm that Pallas’s squirrel has expanded its range exponentially over the past two decades, although with low diffusion coefficients (0.08–0.20km/yr). Squirrels reached the highest relative densities in suburban woodlands, in which females showed no territorial behaviour. Our results indicate that Pallas’s squirrel was able to establish in various habitats in Antibes, preferentially in woodlands and gardens. Densely urbanised areas and the presence of the highway A8 (E80) acted as barriers that slowed range expansion. Such information is crucial to improve the control programme started in 2012 to limit the spread of this potentially invasive squirrel.

Keywords

Introduced species Range expansion Habitat suitability Space use Callosciurus erythraeus 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Andow, D.A., Kareiva, P.M., Levin, S.A., Okubo, A., 1993. Spread of invading organisms: patterns of dispersal. In: Kim, K.C., McPheron, B.A. (Eds.), Evolution of Insect Pests. John Wiley, New York, pp. 219–242.Google Scholar
  2. Aprile, G., Chicco, D., 1999. Nueva especie exotica de mamiferoen la Argentina: la ardilla de vientre rojo. Mastozool. Neotropical 6, 7–14, Available at: https://doi.org/www.sarem.org.ar/wp-content/uploads/2012/11/SAREM_MastNeotrop_6-102_Aprile.pdfGoogle Scholar
  3. Barton, K., 2009. MuMIn: Multi-Model Inference, Available at: https://doi.org/r-forge.r-project.org/projects/mumin/
  4. Benitez, V.V., Almada Chavez, S., Gozzi, A.C., Messetta, M.L, Guichon, M.L, 2013. Invasion status of Asiatic red-bellied squirrels in Argentina. Mamm. Biol. 78, 164–170,  https://doi.org/10.1016/j.mambio.2012.10.002CrossRefGoogle Scholar
  5. Benitez, V.V., Gozzi, A.C., Borgnia, M., Almada Chávez, S., Messetta, M.L, Clos Clos, G., Guichon, M.L., 2010. La ardilla de vientre rojo en Argentina: investigacion y educacion, puntos clave para el manejo de una especie invasora. In: GEIB Grupo Especialista en Invasiones Biologicas (Ed.), Invasiones Biologicas: Avances 2009. Serie Tecnica N. 4. Imprenta El Ejido, Leon, pp. 255–260.Google Scholar
  6. Bertolino, S., 2009. Animal trade and non-indigenous species introduction: the world-wide spread of squirrels. Divers. Distrib. 15, 701–708,  https://doi.org/10.1111/j.1472–4642.2009.00574.xCrossRefGoogle Scholar
  7. Bertolino, S., Genovesi, P., 2003. Spread and attempted eradication of the grey squirrel (Sciurus carolinensis) in Italy, and consequences for the red squirrel (Sciurus vulgaris) in Eurasia. Biol. Conserv. 109, 351–358,  https://doi.org/10.1016/S0006-3207(02)00161-1CrossRefGoogle Scholar
  8. Bertolino, S., Lurz, P.W.W., 2013. Callosciurus squirrels: worldwide introductions, ecological impacts and recommendations to prevent the establishment of new invasive populations. Mammal Rev. 43, 22–33,  https://doi.org/10.1111/j.1365–2907.2011.00204.xCrossRefGoogle Scholar
  9. Bertolino, S., di Montezemolo, N.C., Preatoni, D.G., Wauters, LA, Martinoli, A., 2014. A grey future for Europe: Sciurus carolinensis is replacing native red squirrels in Italy. Biol. Invasions 16, 53–62,  https://doi.org/10.1007/s10530-013-0502-3CrossRefGoogle Scholar
  10. Borger, L, Franconi, N., De Michele, G., Gantz, A., Meschi, F., Manica, A., Lovari, S., Coulson, T., 2006. Effects of sampling regime on the mean and variance of home range size estimates. J. Anim. Ecol. 75, 1393–1405,  https://doi.org/10.1111/j.1365–2656.2006.01164.xPubMedCrossRefGoogle Scholar
  11. Bowler, D.E., Benton, T.G., 2005. Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol. Rev. 80, 205–225,  https://doi.org/10.1017/S1464793104006645PubMedCrossRefGoogle Scholar
  12. Buckland, S.T., Anderson, D.R., Burnham, K.P., Laake, J.L., 1993. Distance Sampling: Estimating Abundance of Biological Populations. Chapman & Hall, London.CrossRefGoogle Scholar
  13. Burnham, K.P., Anderson, D.R., 2004. Multimodel inference: understanding AIC and BIC in model selection. Sociol. Methods Res. 33, 261–304.CrossRefGoogle Scholar
  14. Calenge, C, 2006. The package adehabitat for the R software: a tool for the analysis of space and habitat use by animals. Ecol. Model. 197, 516–519,  https://doi.org/10.1016/j.ecolmodel.2006.03.017CrossRefGoogle Scholar
  15. Chapuis, J.–L., Dozières, A., Pisanu, B., 2012. Les écureuils en France. Muséum National d’Histoire Naturelle, Paris, https://doi.org/ecureuils.mnhn.fr (accessed 27.04.15).Google Scholar
  16. Chapuis, J.–L., Dozières, A., Pisanu, B., Berlin, S., Pauvert, S., 2011. Plan national de lutte relatif à l’écureuil à ventre rouge (Callosciurus erythraeus) dans les Alpes-Maritimes. Rapport MNHN, MNH-Nice, Ministère de l’écologie (MEDDE), Available at: https://doi.org/ecureuils.mnhn.fr/sites/default/files/documents/plan-national-lutte-ecureuil-ventre-rouge.pdf
  17. Chapuis, J.–L., Pisanu, B., Gerriet, O., Pauvert, S., 2014. Plan national de lutte relatif à l’écureuil à ventre rouge (Callosciurus erythraeus) dans les Alpes-Maritimes: bilan et perspectives. Rapport MNHN, MNH-Nice, Ministère de l’écologie (MEDDE), Available at: https://doi.org/ecureuils.mnhn.fr/sites/default/files/documents/plan_evr_bilan_2012-2014_et_perspectives_2015-2018.pdf
  18. Dijkstra, V., Overman, W., Verbeylen, G., 2009. Inventarisatie Pallas’ eekhoorn bij Weert. In: Zoogdiervereniging rapport 2009.21. Zoogdiervereniging, Arnhem, The Netherlands, pp. 1–39, Available at: https://doi.org/zoogdierwinkel.nl/node/252Google Scholar
  19. Dozières, A., (PhD) 2012. Conservation de l’écureuil roux en France: de l’état des populations aux enjeux liés à l’introduction de l’écureuil à ventre rouge. Muséum national d’Histoire naturelle, Paris, Available at: https://doi.org/ecureuils.mnhn.fr/sites/default/files/documents/theseannedozieres1.pdfGoogle Scholar
  20. Gerriet, O., 2009. Répartition de l’écureuil à ventre rouge Callosciurus erythraeus (Pallas, 1779) (Rodentia, Sciuridae) dans les Alpes-maritimes (France). Biocosme Mésogéen. 26, 139–148, Available at: https://doi.org/www.researchgate.net/publication/260623594.Google Scholar
  21. Guichon, M.L., Doncaster, C.P., 2008. Invasion dynamics of an introduced squirrel in Argentina. Ecography31, 211–220,  https://doi.org/10.1111/j.0906–7590.2008.5308.xCrossRefGoogle Scholar
  22. Gurnell, J., Lurz, P.W.W., Shirley, M.D.F., Cartmel, S., Garson, P.J., Magris, L., Steele, J., 2004. Monitoring red squirrels Sciurus vulgaris and grey squirrels Sciurus carolinensis in Britain. Mammal Rev. 34,51–74,  https://doi.org/10.1046/j.0305-1838.2003.00028.xCrossRefGoogle Scholar
  23. Hanski, I., 1999. Metapopulation Ecology. Oxford University Press, Oxford.Google Scholar
  24. Hansteen, T.L., Andreassen, H.P., Ims, R.A., 1997. Effects of spatiotemporal scale on autocorrelation and home range estimators. J. Wildl. Manage. 61, 280–290, Available at: https://doi.org/www.jstor.org/stable/3802583CrossRefGoogle Scholar
  25. Ho, C.Y., (M.Phil. thesis) 1994. The Ecology of Exotic Squirrels (Sciuridae) in Hong Kong, with Special Reference to Callosciurus erythraeus Thai (Kloss). University of Hong Kong, Hong Kong, Available at: https://doi.org/hub.hku.hk/bitstream/10722/32492/1/FullText.pdfCrossRefGoogle Scholar
  26. Hori, M., Yamada, M., Tsunoda, N., 2006. Line census and gnawing damage of introduced Formosan squirrels (Callosciurus erythraeus taiwanensis) in urban forests of Kamakura, Kanagawa, Japan. In: Koike, F., Clout, M.N., Kawamichi, M., De Poorter, M., Iwatsuki, K. (Eds.), Assessment and Control of Biological Invasion Risks. Shoukadoh Book Sellers, Kyoto, pp. 204–209.Google Scholar
  27. Di Pierro, E., Molinari, A., Tosi, G., Wauters, LA., 2008. Exclusive core areas and intrasexual territoriality in Eurasian red squirrels (Sciurus vulgaris) revealed by incremental cluster polygon analysis. Ecol. Res. 23, 529–542,  https://doi.org/10.1007/s11284-007-0401-0CrossRefGoogle Scholar
  28. Horne, J.S., Garton, E.O., 2006a. Likelihood cross-validation versus least squares cross-validation for choosing the smoothing parameter in kernel home-range analysis. J. Wildl. Manage. 70, 641–648,  https://doi.org/10.2193/0022-541X(2006)70[641:LCVLSC]2.0.CO;2CrossRefGoogle Scholar
  29. Horne, J.S., Garton, E.O., 2006b. Selecting the best home range model: an information theoretic approach. Ecology 87, 1146–1152,  https://doi.org/10.1890/0012-9658(2006)87[1146:STBHRM]2.0.CO;2PubMedCrossRefGoogle Scholar
  30. Horne, J.S., Garton, E.O., 2009. Animal Space Use 1.3, Available at: https://doi.org/www.webpages.uidaho.edu/population_ecology/animal_space_use.htm
  31. Hulme, P.E., 2006. Beyond control: wider implications for the management of biological invasions. J. Appl. Ecol. 43, 835–847,  https://doi.org/10.1111/j.1365-2664.2006.01227.xCrossRefGoogle Scholar
  32. Jouanin, C, 1986. Une espèce inattendue pour la faune francaise: un écureuil asiatique acclimaté sur le Cap d’Antibes. Rev. Ecol.-Terre Vie 41, 107–109.Google Scholar
  33. Jouanin, C, 1992. L’écureuil à ventre rouge d’Antibes, in: Introductions et réintroductions de mammifères sauvages. In: Sénotier, J.-L. (Ed.), XIVème colloque de la S.F.E.P.M. Orléans, 20–21 October 1990, pp. 277–284.Google Scholar
  34. Kokko, H., Lopez-Sepulcre, A., 2006. From individual dispersal to species ranges: perspectives for a changing world. Science 313, 789–791,  https://doi.org/10.1126/science.1128566PubMedCrossRefGoogle Scholar
  35. Koprowski, J.L., 2007. Reproductive strategies and alternative reproductive tactics of tree squirrels. In: Wolff, J.O., Sherman, P.W. (Eds.), Rodent Societies: An Ecological and Evolutionary Perspective. Chicago University Press, pp. 86–95.Google Scholar
  36. Lane, J.E., Boutin, S., Gunn, M.R., Coltman, D.W., 2009. Sexually selected behavior: red squirrel males search for reproductive success. J. Anim. Ecol. 78, 296–304,  https://doi.org/10.1111/j.1365-2656.2008.01502.xPubMedCrossRefGoogle Scholar
  37. Lin, Y.S., Yo, S.P., 1981. Population dynamics of the Red-Bellied Tree Squirrel (Callosciurus erythraeus). Bull. Inst. Zool. Acad. Sinica 20, 31–41.Google Scholar
  38. Lurz, P.W.W., Gurnell, J., Magris, L., 2005. Sciurus vulgaris. Mamm. Species 769, 1–10,  https://doi.org/10.1644/1545–1410(2005)769[0001:SV]2.0.CO;2CrossRefGoogle Scholar
  39. Lurz, P.W.W., Hayssen, V., Geissler, K., Bertolino, S., 2013. Callosciurus erythraeus (Rodentia: Sciuridae). Mamm. Species 48, 60–74,  https://doi.org/10.1644/902.1CrossRefGoogle Scholar
  40. 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,  https://doi.org/10.1007/s10344-009-0266-3CrossRefGoogle Scholar
  41. Marmet, J., Pisanu, B., Chapuis, J.L., Jacob, G., Baudry, E., 2012. Factors affecting male and female reproductive success in a chipmunk (Tamias sibiricus) with a scramble competition mating system. Behav. Ecol. Sociobiol. 66,1449–1457,  https://doi.org/10.1007/s00265-012-1399-zCrossRefGoogle Scholar
  42. Miyamoto, A., Tamura, N., Sugimura, K., Yamada, F., 2004. Predicting habitat distribution of the alien Formosan squirrel using logistic regression model. Global Environ. Res. 8, 13–21.Google Scholar
  43. Novillo, A., Ojeda, R.A., 2008. The exotic mammals of Argentina. Biol. Invasions 10, 1333–1344,  https://doi.org/10.1007/s10530-007-9208-8CrossRefGoogle Scholar
  44. Oshida, T., Torii, H., Lin, L.K., Lee, J.–K., Chen, Y.J., Endo, H., Sasaki, M., 2007. A preliminary study on origin of Callosciurus squirrels introduced into Japan. Mamm. Study 32, 75–82,  https://doi.org/10.3106/1348-6160(2007)32[75:APSOOO]2.0.CO;2CrossRefGoogle Scholar
  45. Palmer, G.H., Koprowski, J.L, Pernas, T., 2007. Tree squirrels as invasive species: conservation and management implications. In: Witmer, G.W., Pitt, W.C., Fagerstone, K.A. (Eds.), Managing Vertebrate Invasive Species: Proceedings of an International Symposium. USDA/APHIS Wildlife Services, National Wildlife Research Center, Fort Collins, CO, USA, Available at: https://doi.org/digitalcommons.unl.edu/nwrcinvasive/36Google Scholar
  46. Pinheiro, J., Bates, D., 2000. Mixed-effects Models in S and S-PLUS. Springer, New York.CrossRefGoogle Scholar
  47. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., 2014. Package ‘nlme’, Available at: https://doi.org/cran.r-project.org/web/packages/nlme/nlme.pdf
  48. R Development Core Team, 2012. The R Foundation for Statistical Computing, Available at: https://doi.org/www.r-project.org.
  49. Reffet, F., 2004. Analyse de la saturation routière en PACA. Préparation du débat public. Réseau Ferré de France, 48 pp. Available at: https://doi.org/cpdp.debatpublic.fr/cpdp-lgvpaca/docs/pdf/etudes/saturation_routiere/LGV_PACA_saturation.routiere_CETE_nov_2004.pdf
  50. Romeo, C, Wauters, LA, Preatoni, D., Tosi, G., Martinoli, A., 2010. Living on the edge: space use of Eurasian red squirrels in marginal high-elevation habitat. Acta Oecol. 36, 604–610,  https://doi.org/10.1016/j.actao.2010.09.005CrossRefGoogle Scholar
  51. Signorile, A.L., Paoloni, D., Reuman, D.C., 2014. Grey squirrels in central Italy: a new threat for endemic red squirrel subspecies. Biol. Invasions 16, 2339–2350,  https://doi.org/10.1007/s10530-014-0668-3CrossRefGoogle Scholar
  52. Steele, MA, Koprowski, J.L, 2001. North America Tree Squirrels. Smithsonian Institution Press, Washington and London.Google Scholar
  53. Stuyck, J., Baert, K., Breyne, P., Adriaens, T., 2009. Invasion history and control of Callosciurus erythraeus in Dadizele, Belgium. In: Segers, H., Branquart, E. (Eds.), Science Facing Aliens. Proceedings of a Scientific Meeting on Invasive Alien Species. Brussel, Available at: https://doi.org/www.researchgate.net/publication/228357744.Google Scholar
  54. Swihart, R.K., Slade, NA, 1985. Testing for independence of observations in animal movements. Ecology 66, 1176–1184, Available at: https://doi.org/www.jstor.org/stable/1939170CrossRefGoogle Scholar
  55. Symonds, M.R.E., Moussalli, A., 2011. A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav. Ecol. Sociobiol. 65, 13–21,  https://doi.org/10.1007/s00265-010-1037-6CrossRefGoogle Scholar
  56. Tamura, N., 2004. Population dynamics and expansion of introduced Formosan squirrels in Kanagawa Prefecture, Japan. Jpn. J. Conserv. Ecol. 9, 37–44 (in Japanese; Abstract in English).Google Scholar
  57. Tamura, N., 2012. Datasheet on Callosciurus erythraeus. Cambridge Agricultural Bureau International, Wallingford, Available at: https://doi.org/www.cabi.org/iscGoogle Scholar
  58. Tamura, N., Hayashi, F., Miyashita, K., 1989. Spacing and kinship in the Formosan squirrel living in different habitats. Oecologia 79, 344–352,  https://doi.org/10.1007/BF00384313PubMedPubMedCentralCrossRefGoogle Scholar
  59. Tamura, N., Nakane, M., Satou, S., Hayashi, F., 1987. Home range size of the Formosan squirrel. Callosciurus erythraeus thaiwanensis, estimated by radio tracking. J. Mamm. Soc.Jpn. 12, 69–72, Available at: https://doi.org/www.jstage.jst.go.jp/article/jmammsocjapan1987/12/1-2/121-2_69/_pdf.Google Scholar
  60. Tamura, N., Yong, H.S., 1993. Vocalizations in response to predators in three species of Malaysian Callosciurus (Sciuridae). J. Mammal. 74, 703–714, Available at: https://doi.org/www.jstor.org/stable/1382292CrossRefGoogle Scholar
  61. Waterman, J., 2007. Male mating strategies in rodents. In: Wolff, J.O., Sherman, P.W. (Eds.), Rodent Societies: An Ecological and Evolutionary Perspective. Chicago University Press, pp. 27–41.Google Scholar
  62. Wauters, LA., Bertolino, S., Adamo, M., Van Dongen, S., Tosi, G., 2005. Food shortage disrupts social organization: the case of red squirrels in conifer forests. Evol. Ecol. 19, 375–404,  https://doi.org/10.1007/s10682-005-8311-5CrossRefGoogle Scholar
  63. Wauters, LA., Dhondt, A.A., 1992. Spacing behaviour of red squirrels, Sciurus vulgaris: variation between habitats and the sexes. Anim. Behav. 43, 297–311,  https://doi.org/10.1016/S0003-3472(05)80225-8CrossRefGoogle Scholar
  64. Wauters, LA., Gurnell, J., Preatoni, D., Tosi, G., 2001. Effects of spatial variation in food availability on spacing behaviour and demography of Eurasian red squirrels. Ecography 24, 525–538,  https://doi.org/10.1111/j.1600-0587.2001.tb00487.xCrossRefGoogle Scholar
  65. Wauters, LA., Preatoni, D.G., Molinari, A., Tosi, G., 2007. Radio-tracking squirrels: performance of home range density and linkage estimators with small range and sample size. Ecol. Model. 202, 333–344,  https://doi.org/10.1016/j.ecolmodel.2006.11.001CrossRefGoogle Scholar
  66. White, T.A., Lundy, M.G., Montgomery, W.I., Montgomery, S., Perkins, S.E., Lawton, C, Meehan, J.M., Hayden, T.J., Heckel, G., Reid, N., Searle, J.B., 2012. Range expansion in an invasive small mammal: influence of life-history and habitat quality. Biol. Invasions 14, 2203–2215,  https://doi.org/10.1007/s10530-012-0225-xCrossRefGoogle Scholar
  67. Witey, J.C., Bloxton, T.D., Marzluff, J.M., 2001. Effects of tagging and location error in wildlife radiotelemetry studies. In: Millspaugh, J.J., Marzluff, J.M. (Eds.), Radiotracking and Animal Populations. Academic Press, San Diego, pp. 45–75.Google Scholar
  68. With, K.A., 2002. The landscape ecology of invasive spread. Conserv. Biol. 16, 1192–1203,  https://doi.org/10.1046/j.1523-1739.2002.01064.xCrossRefGoogle Scholar
  69. Worton, B.J., 1989. Kernel methods for estimating the utilization distribution in home-range studies. Ecology 70, 164–168,  https://doi.org/10.2307/1938423CrossRefGoogle Scholar
  70. Yo, S.P., Lin, Y.S., Howard, W.E., 1992. Home range dynamics of red-bellied tree squirrels (Callosciurus erythraeus) inChitou. Bull. Inst. Zool. Acad. Sinica31, 199–211.Google Scholar
  71. Zuur, A.F., Ieno, E.N., Elphick, C.S., 2010. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1, 3–14,  https://doi.org/10.1111/j.2041-210X.2009.00001.xCrossRefGoogle Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2015

Authors and Affiliations

  • Anne Dozières
    • 1
  • Benoît Pisanu
    • 1
  • Stefaniya Kamenova
    • 1
  • Fiona Bastelica
    • 1
  • Olivier Gerriet
    • 1
    • 2
  • Jean-Louis Chapuis
    • 1
    Email author
  1. 1.Muséum National d’Histoire Naturelle, Centre d’Ecologie et des Sciences de la Conservation (CESCO UMR 7204)Sorbonne Universités, MNHN, CNRS, UPMC, CP 53ParisFrance
  2. 2.Muséum d’Histoire Naturelle de NiceNiceFrance

Personalised recommendations