Parasitology Research

, Volume 114, Issue 7, pp 2621–2628 | Cite as

Biodiversity threats from outside to inside: effects of alien grey squirrel (Sciurus carolinensis) on helminth community of native red squirrel (Sciurus vulgaris)

  • Claudia Romeo
  • Nicola Ferrari
  • Paolo Lanfranchi
  • Nicola Saino
  • Francesca Santicchia
  • Adriano Martinoli
  • Lucas A. Wauters
Original Paper


Biological invasions are among the major causes of biodiversity loss worldwide, and parasites carried or acquired by invaders may represent an added threat to native species. We compared gastrointestinal helminth communities of native Eurasian red squirrels (Sciurus vulgaris) in the presence and absence of introduced Eastern grey squirrels (Sciurus carolinensis) to detect alterations induced by the alien species. In particular, we investigated whether spillover of a North American nematode Strongyloides robustus occurs and whether prevalence of a local parasite Trypanoxyuris sciuri in red squirrels is affected by grey squirrel presence. The probability of being infected by both parasites was significantly higher in areas co-inhabited by the alien species, where 61 % of examined red squirrels (n = 49) were infected by S. robustus and 90 % by T. sciuri. Conversely, in red-only areas, the two parasites infected only 5 and 70 % of individuals (n = 60). Overall, our findings support the hypothesis that red squirrels acquire S. robustus via spillover from the alien congener and suggest that invaders’ presence may also indirectly affect infection by local parasites through mechanisms diverse than spill-back and linked to the increased competitive pressure to which red squirrels are subjected. These results indicate that the impact of grey squirrel on red squirrels may have been underestimated and highlight the importance of investigating variation in macroparasite communities of native species threatened by alien competitors.


Invasive species Spillover Parasite-mediated competition Strongyloides robustus Trypanoxyuris sciuri Spill-back 



The project was supported by the Italian Ministry of Education, University and Research (PRIN 2010–2011, 20108 TZKHC to Università degli Studi dell’Insubria, Varese). We would like to thank Adda Nord, Valle del Lambro and Pineta di Appiano Gentile e Tradate Regional Parks, Cuneo and Turin Provinces, Comune di Gallarate, Villa Castelbarco and other private estate owners for allowing field collection. Finally, sample collection would not have been possible without the help of the LIFE09 NAT/IT/00095 EC-SQUARE, Ambrogio Molinari, Mattia Panzeri and Dimitri Sonzogni.

Ethical approval

Traps were checked frequently and handling time was minimised to reduce animal stress, and all applicable international, national and institutional guidelines for the care and use of animals were followed. Permits for trapping and handling red squirrels were granted by Italian Institute for Environmental Protection and Research (ISPRA), Lombardy Region (Authorization No.: 3892, 02/05/2011), Cuneo Province (Permit No.: 473, 12/05/2011) and Torino Province (Permit No.: 180-14616/2011).

This article does not contain any studies with human participants performed by any of the authors.

Conflict of interest

The authors declare that they have no conflict of interest.


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Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Claudia Romeo
    • 1
    • 2
  • Nicola Ferrari
    • 1
  • Paolo Lanfranchi
    • 1
  • Nicola Saino
    • 2
  • Francesca Santicchia
    • 3
  • Adriano Martinoli
    • 3
  • Lucas A. Wauters
    • 3
  1. 1.Department of Veterinary Sciences and Public HealthUniversità degli Studi di MilanoMilanItaly
  2. 2.Department of BiosciencesUniversità degli Studi di MilanoMilanItaly
  3. 3.Department of Theoretical and Applied SciencesUniversità degli Studi dell’InsubriaVareseItaly

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