Biodiversity threats from outside to inside: effects of alien grey squirrel (Sciurus carolinensis) on helminth community of native red squirrel (Sciurus vulgaris)
- 687 Downloads
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.
KeywordsInvasive 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.
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.
- Bartlett C (1995) Morphology, homogonic development, and lack of a free-living generation in Strongyloides robustus (Nematoda, Rhabditoidea), a parasite of North American sciurids. Folia Parasitol (Praha) 42:102–114Google Scholar
- Crawley MJ (2012) The R Book. John Wiley & SonsGoogle Scholar
- Davidson WR (1976) Endoparasites of selected populations of gray squirrels (Sciurus carolinensis) in the southeastern United States. Proc Helminthol Soc Wash 43:211–217Google Scholar
- Dunn AM (2009) Parasites and biological invasions. Adv Parasitol 68:161–184. doi: 10.1016/S0065-308X(08)00607-6
- Eckerlin RP (1974) Studies on the life cycles of Strongyloides robustus Chandler 1942, and a survey of the helminths of Connecticut sciurids. PhD Dissertation, University of ConnecticutGoogle Scholar
- Foreyt WJ (2011) Veterinary parasitology reference manual, 5th edn. Wiley-Blackwell, IowaGoogle Scholar
- Guberti V, Stancampiano L, Ferrari N (2014) Surveillance, monitoring and survey of wildlife diseases: a public health and conservation approach. Hystrix Ital J Mammal 25:3–8Google Scholar
- Hill WA, Randolph MM, Mandrell TD (2009) Sensitivity of perianal tape impressions to diagnose pinworm (Syphacia spp.). Infections in rats (Rattus norvegicus) and mice (Mus musculus). J Am Assoc Lab Anim Sci JAALAS 48:378–380Google Scholar
- Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70Google Scholar
- Parker JC (1971) Protozoan, helminth and arthropod parasites of the gray squirrel in southwestern Virginia. Polytechnic Institute, Virginia, PhD DissertationGoogle Scholar
- Romeo C, Pisanu B, Ferrari N, Basset F, Tillon L, Wauters LA, Martinoli A, Saino N, Chapuis J-L (2013) Macroparasite community of the Eurasian red squirrel (Sciurus vulgaris): poor species richness and diversity. Parasitol Res 112:3527–3536. doi: 10.1007/s00436-013-3535-8 PubMedCrossRefGoogle Scholar
- Romeo C, Wauters LA, Cauchie S, Martinoli A, Matthysen E, Saino N, Ferrari N (2014a) Faecal egg counts from field experiment reveal density dependence in helminth fecundity: Strongyloides robustus infecting grey squirrels (Sciurus carolinensis). Parasitol Res 113:3403–3408. doi: 10.1007/s00436-014-4005-7 PubMedCrossRefGoogle Scholar
- Romeo C, Wauters LA, Ferrari N, Lanfranchi P, Martinoli A, Pisanu B, Preatoni DG, Saino N (2014b) Macroparasite fauna of alien grey squirrels (Sciurus carolinensis): composition, variability and implications for native species. PLoS One 9, e88002. doi: 10.1371/journal.pone.0088002 PubMedCentralPubMedCrossRefGoogle Scholar
- Rushton SP, Lurz PWW, Gurnell J, Nettleton P, Bruemmer C, Shirley MDF, Sainsbury AW (2005) Disease threats posed by alien species: the role of a poxvirus in the decline of the native red squirrel in Britain. Epidemiol Infect 134:521. doi: 10.1017/S0950268805005303 PubMedCentralPubMedCrossRefGoogle Scholar
- Wauters LA, Vermeulen M, Van Dongen S, Bertolino S, Molinari A, Tosi G, Matthysen E (2007) Effects of spatio-temporal variation in food supply on red squirrel Sciurus vulgaris body size and body mass and its consequences for some fitness components. Ecography 30:51–65. doi: 10.1111/j.0906-7590.2007.04646.x CrossRefGoogle Scholar