Biological Invasions

, Volume 16, Issue 1, pp 53–62 | Cite as

A grey future for Europe: Sciurus carolinensis is replacing native red squirrels in Italy

  • Sandro Bertolino
  • Nicola Cordero di Montezemolo
  • Damiano G. Preatoni
  • Lucas A. Wauters
  • Adriano Martinoli
Original Paper

Abstract

Introduced mammals can cause extinction of native species due to replacement competition, disease, predation or hybridization. We studied the colonization of Piedmont (NW-Italy) by American grey squirrel (Sciurus carolinensis) and its effect on the native red squirrel (Sciurus vulgaris). Presence/absence data (2 × 2 km2), of both species were (re)constructed using questionnaires, literature, existing databases, unpublished information, and direct monitoring with hair-tubes. In 1970 red squirrels were still widespread and greys were restricted to forests near the introduction site. By 1990, grey squirrels had increased their range to 220 km2, which coincided with the disappearance of native squirrels from 33 squares inside this range. The invasive species continued its spread occupying an area of 2,016 km2 in 2010; within this area red squirrels went extinct in 88 squares. Overall, from 1970 to 2010 red squirrel went extinct in 62 % of 2 × 2 km2 (ca. 1,689 km2), and were replaced by grey squirrels. The spread of the alien species was slow in the first 20 years, but doubled in the successive two decades. Nevertheless spread was slower than in Ireland and England. Grey squirrel adapt to climate and habitats in both North and South Europe, causing extinction of the native red squirrel. A EU LIFE co-funded project with the aim to control the grey squirrel in North Italy and recent trade-restrictions and trade-ban are a first step in reducing the risk of grey squirrels invading other countries, but their effectiveness will have to be evaluated.

Keywords

Sciurus carolinensis Sciurus vulgaris Extinction Interspecific competition Invasive alien species Species range 

References

  1. Bertolino S (2008) Introduction of the American grey squirrel (Sciurus carolinensis) in Europe: a case study in biological invasion. Curr Sci 95:903–906Google Scholar
  2. Bertolino S (2009) Animal trade and non-indigenous species introduction: the world-wide spread of squirrels. Divers Distrib 15:701–708CrossRefGoogle Scholar
  3. Bertolino S, Genovesi P (2005) The application of the European strategy on invasive alien species: an example with introduced squirrels. Hystrix 16:59–69Google Scholar
  4. Bertolino S, Lurz PWW (2013) Callosciurus squirrels: worldwide introductions, ecological impacts and recommendations to prevent the establishment of new invasive populations. Mammal Rev 43:22–33CrossRefGoogle Scholar
  5. Bertolino S, Lurz PWW, Sanderson R, Rushton S (2008) Predicting the spread of the American Grey Squirrel (Sciurus carolinensis) in Europe: a call for a co-ordinated European approach. Biol Cons 141:2564–2575CrossRefGoogle Scholar
  6. Bertolino S, Wauters L, Pizzul A, Molinari A, Lurz PWW, Tosi G (2009) A general approach of using hair-tubes to monitor the European red squirrel: a method applicable at regional and national scales. Mamm Bio 74:210–219Google Scholar
  7. Bon M, Fasano D, Mezzavilla F, Zanetti M (2008) L’espansione dello scoiattolo comune, Sciurus vulgaris, in pianura veneta nell’ultimo decennio (1998–2007) (Rodentia: Sciuridae). Boll Museo civ Storia Nat Venezia 58 (suppl.):312–316Google Scholar
  8. 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 81:1392–1398CrossRefGoogle Scholar
  9. Carrete M, Tella JL (2008) Wild-bird trade and exotic invasions: a new link of conservation concern? Front Ecol Environ 6:207–211CrossRefGoogle Scholar
  10. Celada C, Bogliani G, Gariboldi A, Maracci A (1994) Occupancy of isolated woodlots by the red squirrel Scirus vulgaris in Italy. Biol Cons 69:177–183CrossRefGoogle Scholar
  11. Clavero M, Brotons L, Pons P, Sol D (2009) Prominent role of invasive species in avian biodiversity loss. Biol Cons 142:2043–2049CrossRefGoogle Scholar
  12. Collen B, Böhm M, Kemp R, Baillie JEM (2012) Spineless: status and trends of the world’s invertebrates. Zoological Society of London, United KingdomGoogle Scholar
  13. Crooks JA (2005) Lag times and exotic species: the ecology and management of biological invasions in slow-motion. Ecoscience 12:316–329CrossRefGoogle Scholar
  14. Ehrenfeld JG (2010) Ecosystem consequences of biological invasions. Ann Rev Ecol Evol Syst 41:59–80CrossRefGoogle Scholar
  15. Ferreira RB, Callahan CM, Poessel SA, Beard KH (2012) Global assessment of establishment success for amphibian and reptile invaders. Wildl Res 39:637–640Google Scholar
  16. Fitzgibbon CD (1993) The distribution of grey squirrels in farm woodland: the influence of wood area isolation and management. J Appl Ecol 30:736–742CrossRefGoogle Scholar
  17. Glen AS, Dickman CR (2008) Niche overlap between marsupial and eutherian carnivores: does competition threaten the endangered spotted-tailed quoll? J Appl Ecol 45:700–707CrossRefGoogle Scholar
  18. Gottero F, Ebone A, Terzuolo PG, Camerano P (2007) I boschi del Piemonte, conoscenze ed indirizzi gestionali. Blu edizioni, Regione Piemonte, Torino, Italy (in Italian)Google Scholar
  19. Gurnell J, Pepper H (1993) A critical look at conserving the British red squirrel Sciurus vulgaris. Mammal Rev 23:125–136CrossRefGoogle Scholar
  20. Gurnell J, Lurz PWW, Shirley MDF, Cartmel S, Garson PJ, Magris L, Steele J (2004a) Monitoring tred squirrels Sciurus vulgaris and grey squirrels Sciurus carolinensis in Britain. Mammal Rev 34:51–74CrossRefGoogle Scholar
  21. Gurnell J, Wauters LA, Lurz PWW, Tosi G (2004b) Alien species and interspecific competition: effects of introduced eastern grey squirrels on red squirrel population dynamics. J Anim Ecol 73:26–35CrossRefGoogle Scholar
  22. Gurnell J, Kenward RE, Pepper H, Lurz PWW (2008) Grey Squirrel Sciurus carolinensis. In: Harris S, Yalden DW (eds) Mammals of the British Isles: handbook, 4th edn. The Mammal Society, Southampton, pp 66–72Google Scholar
  23. Hayes KR, Barry SC (2008) Are there any consistent predictors of invasion success? Biol Invas 10:483–506CrossRefGoogle Scholar
  24. Hulme PE, Bacher S, Kenis M, Klotz S, Kuhn I, Minchin D, Nentwig W, Olenin S, Panov V, Pergl J, Pysek P, Roques A, Sol D, Solarz W, Vila M (2008) Grasping at the routes of biological invasions: a framework for integrating pathways into policy. J Appl Ecol 45:403–414CrossRefGoogle Scholar
  25. Jeschke JM, Strayer DL (2005) Invasion success of vertebrates in Europe and North America. PNAS 102:7198–7202PubMedCrossRefGoogle Scholar
  26. Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. TREE 16:199–204PubMedGoogle Scholar
  27. Lawton C, Cowan P, Bertolino S, Lurz PWW, Peters AR (2010) Consequences of introduction of non-indigenous species: two case studies, the grey squirrel in Europe and the brushtail possum in New Zealand. OIE Rev Scient Tech 29:113–122Google Scholar
  28. Long JL (2003) Introduced mammals of the world. CABI/CSIRO Publishing, CollingwoodGoogle Scholar
  29. Lurz PWW, Rushton SP, Wauters LA, Bertolino S, Currado I, Mazzoglio PJ, Shirley MDF (2001) Predicting grey squirrel expansion in North Italy: a spatially explicit modelling approach. Landsc Ecol 16:407–420CrossRefGoogle Scholar
  30. MacArthur R, Levins R (1967) The limiting similarity, convergence, and divergence of coexisting species. Am Nat 101:377–385CrossRefGoogle Scholar
  31. Marsico TD, Burt JW, Espeland EK, Gilchrist GW, Jamieson MA, Lindstrom L, Swope S, Roderick GK, Szucs M, Tsutsui ND (2010) Underutilized resources for studying the evolution of invasive species during their introduction, establishment and lag phases. Evol Appl 3:203–219PubMedCentralCrossRefGoogle Scholar
  32. Martinoli A, Bertolino S, Preatoni DG, Balduzzi A, Marsan A, Genovesi P, Tosi G, Wauters LA (2010) Headcount 2010: the multiplication of the grey squirrel populations introduced in Italy. Hystrix 21:127–136Google Scholar
  33. Mayle B, Pepper H, Ferryman M (2003) Controlling grey squirrel damage to woodlands. For Comm Pract Note 4:16Google Scholar
  34. Middleton AD (1932) The Grey Squirrel (Sciurus carolinensis) in the British Isles, 1930–1932. J Anim Ecol 1:166–167CrossRefGoogle Scholar
  35. O’Teangana D, Reilly S, Montgomery WI, Rochford J (2000) Distribution and status of the red squirrel (Sciurus vulgaris) and grey squirrel (Sciurus carolinensis) in Ireland. Mammal Rev 30:45–56CrossRefGoogle Scholar
  36. Okubo A, Maini PK, Williamson MH, Murray JD (1989) On the spatial spread of the grey squirrel in Britain. Proc R Soc Lond B 238:113–125PubMedCrossRefGoogle Scholar
  37. Peacock DE (2009) The grey squirrel Sciurus carolinensis in Adelaide, South Australia: its introduction and eradication. Vic Nat 126:150–155Google Scholar
  38. Reynolds JC (1985) Details of the geographic replacement of the Red Squirrel (Sciurus vulgaris) by the Grey Squirrel (Sciurus carolinensis) in Eastern England. J Anim Ecol 54:149–162CrossRefGoogle Scholar
  39. Rodrìguez A, Andrén H (1999) A comparison of Eurasian red squirrel distribution in different fragmented landscapes. J Appl Ecol 36:649–662CrossRefGoogle Scholar
  40. Rushton SP, Lurz PWW, Gurnell J, Nettleton P, Bruemmer C, Shirley MDF, Sainsbury AW (2006) Disease threats posed by alien species: the role of a poxvirus in the decline of the native red squirrel in Britain. Epidem Infect 134:521–533CrossRefGoogle Scholar
  41. Sainsbury AW, Nettleton P, Gilray J, Gurnell J (2000) Grey squirrels have high seroprevalence to a parapox virus associated with deaths in red squirrels. Animal Cons 3:229–233CrossRefGoogle Scholar
  42. Signorile AL, Evans J (2007) Damage caused by the American grey squirrel (Sciurus carolinensis) to agricultural crops, poplar plantations and semi-natural woodland in Piedmont, Italy. Forestry 80:89–98CrossRefGoogle Scholar
  43. Strayer DL (2012) Eight questions about invasions and ecosystem functioning. Ecol Lett 15:1199–1210PubMedCrossRefGoogle Scholar
  44. Tattoni C, Preatoni DG, Martinoli A, Bertolino S, Wauters LA (2005) Application of modelling techniques to manage a population of grey squirrels (Sciurus carolinensis) in Lombardy, northern Italy, and analysis of parameters estimates used in simulations Italian. Hystrix 16:99–112Google Scholar
  45. Tattoni C, Preatoni DG, Lurz PWW, Rushton SP, Tosi G, Martinoli A, Bertolino S, Wauters LA (2006) Modelling the expansion of grey squirrels (Sciurus carolinensis) in Lombardy, Northern Italy: implications for squirrel control. Biol Invasions 8:1605–1619CrossRefGoogle Scholar
  46. Tompkins DM, Sainsbury AW, Nettleton P, Buxton D, Gurnell J (2002) Parapoxvirus causes a deleterious disease in red squirrels associated with UK population declines. Proc R Soc Lond B 269:529–533CrossRefGoogle Scholar
  47. Verbeylen G, De Bruyn L, Matthysen E (2003) Patch occupancy, population density and dynamics in a fragmented red squirrel Sciurus vulgaris population. Ecography 26:118–128CrossRefGoogle Scholar
  48. Vié JC, Hilton-Taylor C, Stuart SN (eds) (2009) Wildlife in a changing world—an analysis of the 2008 IUCN red list of threatened species. IUCN, Gland, p 180Google Scholar
  49. Wauters LA, Gurnell J, Currado I, Mazzoglio PJ (1997a) Grey squirrel Sciurus carolinensis management in Italy—squirrel distribution in a highly fragmented landscape. Wildl Biol 3:117–124Google Scholar
  50. Wauters LA, Currado I, Mazzoglio PJ, Gurnell J (1997b) Replacement of red squirrels by introduced grey squirrels in Italy: evidence from a distribution survey. In: Gurnell J, Lurz PWW (eds) The conservation of red squirrels Sciurus vulgaris L. PTES, London, pp 79–88Google Scholar
  51. Wauters LA, Gurnell J, Martinoli A (2002a) Interspecific competition between native Eurasian red squirrels and alien grey squirrels: does resource partitioning occur? Behav Ecol Sociobiol 52:332–341CrossRefGoogle Scholar
  52. Wauters LA, Tosi G, Gurnell J (2002b) Interspecific competition in tree squirrels: do introduced grey squirrels (Sciurus carolinensis) deplete tree seeds hoarded by red squirrels (S. vulgaris)? Behav Ecol Sociobiol 51:360–367CrossRefGoogle Scholar
  53. Wauters LA, Tosi G, Gurnell J (2005) A review of the competitive effects of alien grey squirrels on behaviour, activity and habitat use of red squirrels in mixed, deciduous woodland in Italy. Hystrix 16:27–40Google Scholar
  54. Wauters LA, Verbeylen G, Preatoni D, Martinoli A, Matthysen E (2010) Dispersal and habitat cuing of Eurasian red squirrels in fragmented habitats. Pop Ecol 52:527–536CrossRefGoogle Scholar
  55. Wauters LA, Preatoni D, Martinoli A, Verbeylen G, Matthysen E (2011) No sex bias in natal dispersal of Eurasian red squirrels. Mamm Bio 76:369–372Google Scholar
  56. Williamson M (1996) Biological invasions. Chapman and Hall, Great BritainGoogle Scholar
  57. Wittenberg R, Cock MJW (2001) Invasive alien species: a toolkit of best prevention and management practices. CABI Publishing, WallingfordCrossRefGoogle Scholar
  58. Zollner PA (2000) Comparing the landscape level perceptual abilities of forest sciurids in fragmented agricultural landscapes. Landsc Ecol 15:523–533CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Sandro Bertolino
    • 1
  • Nicola Cordero di Montezemolo
    • 1
  • Damiano G. Preatoni
    • 2
  • Lucas A. Wauters
    • 2
  • Adriano Martinoli
    • 2
  1. 1.Department of Agriculture, Forest and Food SciencesUniversity of TurinGrugliasco (TO)Italy
  2. 2.Environment Analysis and Management Unit, Guido Tosi Research Group, Department of Theoretical and Applied SciencesUniversity of InsubriaVareseItaly

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