Skip to main content
SpringerLink
Log in

From a lag in vector activity to a constant increase of translocations: invasion of Callosciurus squirrels in Argentina

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

Abstract

Arboreal squirrels of the Asiatic genus Callosciurus have shown high likelihood of establishment from few released animals, in particular, C. erythraeus has established wild populations in Argentina, Belgium, France, Hong Kong, Japan, and The Netherlands. We report the invasion process of C. erythraeus in Argentina in the last four decades and suggest management actions for each foci. Between February 2011 and November 2014 we conducted field surveys and interviews in nine sites in central Argentina to confirm the presence of C. erythraeus, describe their history of introduction, and estimate range expansion and squirrel relative abundance. We report a two decades lag-phase until the onset of translocations of C. erythraeus within national boundaries that resulted in a constant increase of the cumulative number of releases. We confirm nine new release events between 1995 and 2012 and six new invasion foci that yields a total of 13 deliberate releases and 10 invasion foci established in rural and urban areas of Argentina. Spread rate ranged from 0.12 to 0.66 km/year. An intermediate relative density of squirrels (2–7 ind/ha) was found close to release sites except in one case. All introduction events involved squirrels translocated from the first, 40 years old invasion focus, occasionally involving illegal trade. The rate of introduction events in the last decades and the translocation-lag phase described in this study should call the attention in all countries dealing with charismatic, introduced species. Translocation disruption requires urgent attention to slow down the invasion of this and other species.

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

Similar content being viewed by others

References

  • Andow DA, Kareiva PM, Levin SA, Okubo A (1993) Spread of invading organisms: patterns of dispersal. In: Kim KC, McPheron BA (eds) Evolution of insect pests. John Wiley, New York, pp 219–242

    Google Scholar 

  • Aprile G, Chicco D (1999) Nueva especie exótica de mamífero en la Argentina: la ardilla de vientre rojo Callosciurus erythraeus. Mastozoología Neotropical 6:7–14

    Google Scholar 

  • Bayne E, Hobson K (2000) Relative use of contiguous and fragmented boreal forest by red squirrels (Tamiasciurus hudsonicus). Can J Zool 78:359–365

    Article  Google Scholar 

  • Benitez VV, Almada Chavez S, Gozzi AC, Messetta ML, Guichón ML (2013) Invasion status of Asiatic red-bellied squirrels in Argentina. Mamm Biol 78:164–170

    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 (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

    Article  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, Cordero di Montezemolo N, Preatoni DG, Wauters LA, Martinoli A (2014) A grey future for Europe: Sciurus carolinensis is replacing native red squirrels in Italy. Biol Invasions 16:53–62

    Article  Google Scholar 

  • Blackburn TM, Pysek P, Bacher S, Carlton JT, Duncan RP, Jarosik V, Wilson JRU, Richardson DM (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339

    Article  PubMed  Google Scholar 

  • Borgnia M, Benitez V, Gozzi C, Guichón ML (2013) La ardilla de vientre rojo en Argentina y el manejo de especies introducidas como un problema biológico y social. Ecología Austral 23:147–155

    Google Scholar 

  • Bridgman LJ, Benitez VV, Graña Grilli M, Mufato N, Acosta D, Guichón ML (2012) Short perceptual range and yet successful invasion of a fragmented landscape: the case of the red-bellied tree squirrel (Callosciurus erythraeus) in Argentina. Landsc Ecol 27:633–640

    Article  Google Scholar 

  • Cassini G, Guichón ML (2009) Variaciones morfológicas y diagnosis de la ardilla de vientre rojo, Callosciurus erythraeus (Pallas, 1779), en Argentina. Mastozoología Neotropical 16:39–47

    Google Scholar 

  • Clark B (2014) Earth Point, tools for Google Earth. http://www.earthpoint.us/. Accessed 25 Sep 2014

  • 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 

  • Estévez RA, Anderson CB, Pizarro JC, Burgman MA (2014) Clarifying values, risk perceptions, and attitudes to resolve or avoid social conflicts in invasive species management. Conserv Biol. doi:10.1111/cobi.12359

    PubMed  Google Scholar 

  • Gabrielli M, Cardoso Y, Benitez V, Gozzi AC, Guichón ML, Lizarralde M (2014) Genetic characterization of Callosciurus Asiatic squirrels introduced in Argentina. Ital J Zool 81:328–343

    Article  Google Scholar 

  • Gozzi AC, Guichón ML, Benitez VV, Lareschi M (2013) Arthropod parasites of the red-bellied squirrel Callosciurus erythraeus (Rodentia: Sciuridae) introduced into Argentina. Med Vet Entomol 27:203–208

    Article  CAS  PubMed  Google Scholar 

  • Gozzi AC, Guichón ML, Benitez VV, Troyelli A, Navone GT (2014) Gastro-intestinal helminths in the red-bellied squirrel introduced into Argentina: accidental acquisitions and lack of specific parasites. Hystrix 25:97–102

    Google Scholar 

  • Guichón ML, Doncaster CP (2008) Invasion dynamics of an introduced squirrel in Argentina. Ecography 31:211–220

    Article  Google Scholar 

  • Guichón ML, Bello M, Fasola ML (2005) Expansión poblacional de una especie introducida en la Argentina: la ardilla de vientre rojo Callosciurus erythraeus. Mastozoología Neotropical 12:189–197

    Google Scholar 

  • Gurnell J, Wauters LA, Lurz PWW, Tosi G (2004) 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 

  • Heger T, Jeschke JM (2014) The enemy release hypothesis as a hierarchy of hypotheses. Oikos 123:741–750

    Article  Google Scholar 

  • Jacobs MH, Vaske JJ, Dubois S, Fehres P (2014) More than fear: role of emotions in acceptability of lethal control of wolves. Eur J Wildl Res. doi:10.1007/s10344-014-0823-2

    Google Scholar 

  • Jeschke JM (2014) General hypothesis in invasion ecology. Divers Distrib 20:1229–1234

    Article  Google Scholar 

  • Jessen RR, Merrick MJ, Koprowski JL, Ramirez O (2010) Presence of Guayaquil squirrels on the central coast of Peru: an apparent introduction. Mammalia 74:443–444

    Article  Google Scholar 

  • Koprowski JL (2005) The response of tree squirrels to fragmentation: a review and synthesis. Anim Conserv 8:369–376

    Article  Google Scholar 

  • Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228

    Article  PubMed  Google Scholar 

  • Lurz PWW, Hayssen V, Geissler K, Bertolino S (2013) Callosciurus erythraeus (Rodentia: Sciuridae). Mamm Species 45:60–74

    Article  Google Scholar 

  • McNeely JA (2001) An introduction to human dimensions of invasive species. In: McNeely JA (ed) The great reshuffling: human dimensions of invasive alien species. IUCN, Gland, pp 5–20

    Google Scholar 

  • Palmer GH, Koprowski J, Pernas T (2007) Tree squirrels as invasive species: conservation and management implications. In: Witmer GW, Pitt WC, Fagerstone KA (eds) Managing vertebrate invasive species. USDA National Wildlife Research Center Symposia, University of Nebraska, Lincoln, p 273–282

  • Parker T, Nilon C (2008) Gray squirrel density, habitat suitability, and behavior in urban parks. Urban Ecosyst 11:243–255

    Article  Google Scholar 

  • Ruiz GM, Carlton JT (2003) Invasion vectors: a conceptual vector for management. In: Ruiz GM, Carlton JT (eds) Invasive species: vectors and management strategies. Island Press, Washington DC, pp 459–504

    Google Scholar 

  • SIGA (2014) Sistema de información y gestión agrometeorológico. Instituto Nacional de Tecnología Agropecuaria, Argentina. http://siga2.inta.gov.ar/en/datoshistoricos. Accessed 25 Aug 2014

  • Simberloff D (2014) Biologial invasions: what’s worth fighting and what can be won? Ecol Eng 64:112–121

    Article  Google Scholar 

  • With KA (2002) The landscape ecology of invasive spread. Conserv Biol 16:1192–1203

    Article  Google Scholar 

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

    Google Scholar 

  • Wood DJA, Koprowski JL, Lurz PWW (2007) Tree squirrel introduction: a theoretical approach with population viability analysis. J Mammal 88:1271–1279

    Article  Google Scholar 

  • Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice Hall, Englewood Cliffs

    Google Scholar 

Download references

Acknowledgments

We thank A. Troyelli, B. Baguette Pereiro and C. Lallana Ovejero for fieldwork assistance. Local support in each site: V. Dell Arciprete and H. Feigrós in 25 de Mayo; R. Gallardo, T. Cristie and J. Gachet in San Miguel; G. Consoli, G. Facello and P. Heredia in Capitán Sarmiento; S. Ballina, P. Siroski and E. Mosso in Rafaela. Hundreds of residents and personnel of ranches and rural institutes collaborated with our interviews and in some cases also allowed us to survey within their properties. F. Milesi provided several constructive suggestions. This study was supported by the Universidad Nacional de Luján.

Author information

Author notes

  1. M. Laura Guichón

    Present address: Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA, UNCo–CONICET), Centro de Ecología Aplicada del Neuquén (CEAN), Junín de los Andes, Neuquén, Argentina

Authors and Affiliations

  1. Ecología de Mamíferos Introducidos, Departamento de Ciencias Básicas, Instituto de Ecología y Desarrollo Sustentable (INEDES), Universidad Nacional de Luján, Rutas 5 y 7, 6700, Luján, Buenos Aires, Argentina

    M. Laura Guichón, Verónica V. Benitez, A. Cecilia Gozzi, Marina Hertzriken & Mariela Borgnia

Authors
  1. M. Laura Guichón
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Verónica V. Benitez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Cecilia Gozzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marina Hertzriken
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mariela Borgnia
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Laura Guichón.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guichón, M.L., Benitez, V.V., Gozzi, A.C. et al. From a lag in vector activity to a constant increase of translocations: invasion of Callosciurus squirrels in Argentina. Biol Invasions 17, 2597–2604 (2015). https://doi.org/10.1007/s10530-015-0897-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-015-0897-0

Keywords

Search

Navigation