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

Parasitology Research volume 114, pages 2621–2628 (2015)Cite this article

Abstract

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.

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Acknowledgments

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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Authors and Affiliations

  1. Department of Veterinary Sciences and Public Health, Università degli Studi di Milano, Via Celoria 10, 20133, Milan, Italy

    Claudia Romeo, Nicola Ferrari & Paolo Lanfranchi

  2. Department of Biosciences, Università degli Studi di Milano, Via Celoria 26, 20133, Milan, Italy

    Claudia Romeo & Nicola Saino

  3. Department of Theoretical and Applied Sciences, Università degli Studi dell’Insubria, Via J.H. Dunant, 3, 21100, Varese, Italy

    Francesca Santicchia, Adriano Martinoli & Lucas A. Wauters

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  1. Claudia Romeo
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  2. Nicola Ferrari
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  5. Francesca Santicchia
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Correspondence to Claudia Romeo.

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Romeo, C., Ferrari, N., Lanfranchi, P. et al. Biodiversity threats from outside to inside: effects of alien grey squirrel (Sciurus carolinensis) on helminth community of native red squirrel (Sciurus vulgaris). Parasitol Res 114, 2621–2628 (2015). https://doi.org/10.1007/s00436-015-4466-3

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  • DOI: https://doi.org/10.1007/s00436-015-4466-3

Keywords

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