Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

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data (2 × 2 km2), of both species were (re)constructed using questionnaires, literature, existing databases, unpublished information, and direct monitoring with hair-tubes.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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Bertolino S (2008) Introduction of the American grey squirrel (Sciurus carolinensis) in Europe: a case study in biological invasion. Curr Sci 95:903–906

    Google Scholar 

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

    Article  Google Scholar 

  • Bertolino S, Genovesi P (2005) The application of the European strategy on invasive alien species: an example with introduced squirrels. Hystrix 16:59–69

    Google Scholar 

  • Bertolino S, Lurz PWW (2013) Callosciurus squirrels: worldwide introductions, ecological impacts and recommendations to prevent the establishment of new invasive populations. Mammal Rev 43:22–33

    Article  Google Scholar 

  • 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 141:2564–2575

    Article  Google Scholar 

  • 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 74:210–219

    Google Scholar 

  • 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.):312–316

    Google Scholar 

  • 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 81:1392–1398

    Article  Google Scholar 

  • Carrete M, Tella JL (2008) Wild-bird trade and exotic invasions: a new link of conservation concern? Front Ecol Environ 6:207–211

    Article  Google Scholar 

  • Celada C, Bogliani G, Gariboldi A, Maracci A (1994) Occupancy of isolated woodlots by the red squirrel Scirus vulgaris in Italy. Biol Cons 69:177–183

    Article  Google Scholar 

  • Clavero M, Brotons L, Pons P, Sol D (2009) Prominent role of invasive species in avian biodiversity loss. Biol Cons 142:2043–2049

    Article  Google Scholar 

  • Collen B, Böhm M, Kemp R, Baillie JEM (2012) Spineless: status and trends of the world’s invertebrates. Zoological Society of London, United Kingdom

    Google Scholar 

  • Crooks JA (2005) Lag times and exotic species: the ecology and management of biological invasions in slow-motion. Ecoscience 12:316–329

    Article  Google Scholar 

  • Ehrenfeld JG (2010) Ecosystem consequences of biological invasions. Ann Rev Ecol Evol Syst 41:59–80

    Article  Google Scholar 

  • Ferreira RB, Callahan CM, Poessel SA, Beard KH (2012) Global assessment of establishment success for amphibian and reptile invaders. Wildl Res 39:637–640

    Google Scholar 

  • Fitzgibbon CD (1993) The distribution of grey squirrels in farm woodland: the influence of wood area isolation and management. J Appl Ecol 30:736–742

    Article  Google Scholar 

  • Glen AS, Dickman CR (2008) Niche overlap between marsupial and eutherian carnivores: does competition threaten the endangered spotted-tailed quoll? J Appl Ecol 45:700–707

    Article  Google Scholar 

  • 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)

  • Gurnell J, Pepper H (1993) A critical look at conserving the British red squirrel Sciurus vulgaris. Mammal Rev 23:125–136

    Article  Google Scholar 

  • 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 34:51–74

    Article  Google Scholar 

  • 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 73:26–35

    Article  Google Scholar 

  • 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 66–72

    Google Scholar 

  • Hayes KR, Barry SC (2008) Are there any consistent predictors of invasion success? Biol Invas 10:483–506

    Article  Google Scholar 

  • 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 45:403–414

    Article  Google Scholar 

  • Jeschke JM, Strayer DL (2005) Invasion success of vertebrates in Europe and North America. PNAS 102:7198–7202

    Article  CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • 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 29:113–122

    Google Scholar 

  • Long JL (2003) Introduced mammals of the world. CABI/CSIRO Publishing, Collingwood

    Google Scholar 

  • 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 16:407–420

    Article  Google Scholar 

  • MacArthur R, Levins R (1967) The limiting similarity, convergence, and divergence of coexisting species. Am Nat 101:377–385

    Article  Google Scholar 

  • 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 3:203–219

    Article  PubMed Central  Google Scholar 

  • 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 21:127–136

    Google Scholar 

  • Mayle B, Pepper H, Ferryman M (2003) Controlling grey squirrel damage to woodlands. For Comm Pract Note 4:16

    Google Scholar 

  • Middleton AD (1932) The Grey Squirrel (Sciurus carolinensis) in the British Isles, 1930–1932. J Anim Ecol 1:166–167

    Article  Google Scholar 

  • 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 30:45–56

    Article  Google Scholar 

  • Okubo A, Maini PK, Williamson MH, Murray JD (1989) On the spatial spread of the grey squirrel in Britain. Proc R Soc Lond B 238:113–125

    Article  CAS  PubMed  Google Scholar 

  • Peacock DE (2009) The grey squirrel Sciurus carolinensis in Adelaide, South Australia: its introduction and eradication. Vic Nat 126:150–155

    Google Scholar 

  • 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 54:149–162

    Article  Google Scholar 

  • Rodrìguez A, Andrén H (1999) A comparison of Eurasian red squirrel distribution in different fragmented landscapes. J Appl Ecol 36:649–662

    Article  Google Scholar 

  • 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 134:521–533

    Article  CAS  Google Scholar 

  • 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 3:229–233

    Article  Google Scholar 

  • 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 80:89–98

    Article  Google Scholar 

  • Strayer DL (2012) Eight questions about invasions and ecosystem functioning. Ecol Lett 15:1199–1210

    Article  PubMed  Google Scholar 

  • 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 16:99–112

    Google Scholar 

  • 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 8:1605–1619

    Article  Google Scholar 

  • 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 269:529–533

    Article  Google Scholar 

  • Verbeylen G, De Bruyn L, Matthysen E (2003) Patch occupancy, population density and dynamics in a fragmented red squirrel Sciurus vulgaris population. Ecography 26:118–128

    Article  Google Scholar 

  • 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 180

    Google Scholar 

  • 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 3:117–124

    Google Scholar 

  • 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 79–88

    Google Scholar 

  • 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 52:332–341

    Article  Google Scholar 

  • 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 51:360–367

    Article  Google Scholar 

  • 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 16:27–40

    Google Scholar 

  • Wauters LA, Verbeylen G, Preatoni D, Martinoli A, Matthysen E (2010) Dispersal and habitat cuing of Eurasian red squirrels in fragmented habitats. Pop Ecol 52:527–536

    Article  Google Scholar 

  • Wauters LA, Preatoni D, Martinoli A, Verbeylen G, Matthysen E (2011) No sex bias in natal dispersal of Eurasian red squirrels. Mamm Bio 76:369–372

    Google Scholar 

  • Williamson M (1996) Biological invasions. Chapman and Hall, Great Britain

    Google Scholar 

  • Wittenberg R, Cock MJW (2001) Invasive alien species: a toolkit of best prevention and management practices. CABI Publishing, Wallingford

    Book  Google Scholar 

  • Zollner PA (2000) Comparing the landscape level perceptual abilities of forest sciurids in fragmented agricultural landscapes. Landsc Ecol 15:523–533

    Article  Google Scholar 

Download references

Acknowledgments

This paper is dedicated to Prof. Italo Currado (1936–2005) who first raised the attention on the risks posed by the presence of the grey squirrel in Italy. The surveys of the two squirrel species were funded by grants to the University of Turin from Provincia di Torino Servizio Tutela della Fauna e della Flora, Regione Piemonte Settore Pianificazione delle Aree Protette, Parco dei Laghi di Avigliana and Direzione Agricoltura Osservatorio faunistico regionale. We are grateful to Peter John Mazzoglio, the personnel of the Piedmont regional parks and all the other people that collaborated to the surveys. Constructive comments by two anonymous referees helped to improve the manuscript. This work was realized under the LIFE09 NAT/IT/000095 EC-SQUARE Project. This is paper n. 1 of the EC-SQUARE project.

Author information

Authors and Affiliations

  1. Department of Agriculture, Forest and Food Sciences, University of Turin, Via L. da Vinci 44, 10095, Grugliasco (TO), Italy

    Sandro Bertolino & Nicola Cordero di Montezemolo

  2. Environment Analysis and Management Unit, Guido Tosi Research Group, Department of Theoretical and Applied Sciences, University of Insubria, Varese, Italy

    Damiano G. Preatoni, Lucas A. Wauters & Adriano Martinoli

Authors
  1. Sandro Bertolino
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nicola Cordero di Montezemolo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Damiano G. Preatoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lucas A. Wauters
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Adriano Martinoli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lucas A. Wauters.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bertolino, S., di Montezemolo, N.C., Preatoni, D.G. et al. A grey future for Europe: Sciurus carolinensis is replacing native red squirrels in Italy. Biol Invasions 16, 53–62 (2014). https://doi.org/10.1007/s10530-013-0502-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-013-0502-3

Keywords

Search

Navigation