Skip to main content

Advertisement

SpringerLink
Log in

Arthropods and associated pathogens from native and introduced rodents in Northeastern Italy

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Introduced Siberian chipmunks Eutamias sibiricus have been reported to be important reservoirs for human Lyme disease, as they may host high numbers of hard ticks carrying Borrelia spp. and other pathogens. In the present study, we assessed the prevalence of Borrelia spp. and other pathogenic bacteria in ectoparasite arthropod species infesting Siberian chipmunks and coexisting native small rodents. Small rodents were trapped with Sherman traps in Veneto (NE Italy), where the largest Italian populations of chipmunks occur. A total of 14 individual ticks were found on 223 rodents, with 6 more ticks obtained from stored dead chipmunks from the same study area. Ectoparasites were screened for pathogens by molecular analyses including species-specific PCR amplifications. Rickettsia monacensis, Borrelia lusitaniae, and Anaplasma platys were present in the parasites of both native rodents and introduced chipmunks. The present findings suggest a role for the invasive species E. sibiricus in the maintenance of the Ixodes ricinus life cycle, which may result in the modification of the transmission dynamics of tick-borne pathogens. Moreover, the presence of Rickettsia in urban populations of chipmunks may represent a serious risk for human health and should be investigated further.

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

Similar content being viewed by others

References

  • Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res 25:4692–4693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ancillotto L, Mori E, Sozio G, Solano E, Bertolino S, Russo D (2016) A novel approach to field identification of cryptic Apodemus wood mice: calls differ more than morphology. Mammal Rev 47:6–10

    Article  Google Scholar 

  • Chu CY, Jiang BG, Liu W, Zhao QM, Wu XM, Zhang PH, Zhan L, Yang H, Cao WC (2008) Presence of pathogenic Borrelia burgdorferi sensu lato in ticks and rodents in Zhejiang, south-east China. J Med Microbiol 57:980–985

    Article  CAS  PubMed  Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife– threats to biodiversity and human health. Science 287:443–449

    Article  CAS  PubMed  Google Scholar 

  • Debernardi P, Patriarca E, Reutter BA (2003) Contribution to the knowledge of Apodemus genus in the Gran Paradiso National Park. Hystrix 14:55–75

    Google Scholar 

  • Dunn AM (2009) Parasites and biological invasions. Adv Parasitol 68:161–184

    Article  PubMed  Google Scholar 

  • Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Peña A, Horak IG, Shao R, Barker SC (2010) The Argasidae Ixodidae and Nuttalliellidae (Acari: Ixodida) of the world: a list of valid species names. Zootaxa 2528:1–28

    Google Scholar 

  • Hersh MH, Ostfeld RS, McHenry DJ, Tibbetts M, Brunner JL, Killilea ME, LoGiudice K, Schmidt KA, Keesing F (2014) Co-infection of blacklegged ticks with Babesia microti and Borrelia burgdorferi is higher than expected and acquired from small mammal hosts. PLoS One 9:e99348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hubàlek Z, Halouzka J (1997) Distribution of Borrelia burgdorferi sensu lato genomic groups in Europe, a review. Eur J Epidemiol 13:951–957

    Article  PubMed  Google Scholar 

  • Iatta R, Immediato D, Puttilli MR, Danesi P, Passantino G, Parisi A, Mallia E, Otranto D, Cafarchia C (2015) Cryptococcus neoformans in the respiratory tract of squirrels, Callosciurus finlaysonii (Rodentia, Sciuridae). Med Mycol 53:666–673

    Article  CAS  PubMed  Google Scholar 

  • Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM (2009) Parasite spillback: a neglected concept in invasion ecology? Ecology 90:2047–2056

    Article  CAS  PubMed  Google Scholar 

  • Kilpatrick HJ, Labonte AM, Stafford KC (2014) The relationship between deer density, tick abundance, and human cases of Lyme disease in a residential community. J Med Entomol 57:777–784

    Article  Google Scholar 

  • Le Cœur C, Chantepie S, Pisanu B, Chapuis JL, Robert A (2016) Inter-annual and inter-individual variations in survival exhibit strong seasonality in a hibernating rodent. Oecologia 181:795–807

    Article  PubMed  Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  • Madeddu G, Mancini F, Caddeo A, Ciervo A, Babudieri S, Maida I, Fiori ML, Rezza G, Mura MS (2012) Rickettsia monacensis as cause of Mediterranean spotted fever-like illness, Italy. Emerg Infect Dis 18:702–704

    Article  PubMed  PubMed Central  Google Scholar 

  • Marmet J, Pisanu B, Chapuis JL (2009) Home range, range overlap, and site fidelity of introduced Siberian chipmunks in a suburban French forest. Eur J Wildl Res 55:497–504

    Article  Google Scholar 

  • Marsot M, Sigaud M, Chapuis JL, Ferquel E, Cornet M, Vourc’h G (2011) Introduced Siberian chipmunks (Tamias sibiricus barberi) harbor more-diverse Borrelia burgdorferi sensu lato genospecies than native bank voles (Myodes glareolus). Appl Environ Microbiol 77:5716–5721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marsot M, Chapuis JL, Gasqui P, Dozières A, Massèglia S, Pisanu B, Ferquel E, Vourc’h G (2013) Introduced Siberian chipmunks (Tamias sibiricus barberi) contribute more to Lyme borreliosis risk than native reservoir rodents. PLoS One 8:e55377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez R, Morato S (2004) Thigmotaxis and exploration in adult and pup rats. Rev Etol 6:49–54

    Google Scholar 

  • Massung RF, Slater K, Owens JH, Nicholson WL, Mather TN, Solberg VB, Olson JG (1998) Nested PCR assay for detection of granulocytic Ehrlichiae. J Clin Microbiol 36:1090–1095

    PubMed  PubMed Central  CAS  Google Scholar 

  • Mazza G, Tricarico E, Genovesi P, Gherardi F (2014) Biological invaders are threats to human health: an overview. Ethol Ecol Evol 26:112–129

    Article  Google Scholar 

  • Mazzamuto MV, Pisanu B, Romeo C, Ferrari N, Preatoni D, Wauters LA, Chapuis JL, Martinoli A (2016) Poor parasite community of an invasive alien species: macroparasites of Pallas’s squirrel in Italy. Ann Zool Fenn 53:103–112

    Article  Google Scholar 

  • Michaux JR, Kinet S, Filippucci MG, Libois R, Besnard A, Catzeflis F (2001) Molecular identification of three sympatric species of wood mice (Apodemus sylvaticus, A. flavicollis, A. alpicola) in western Europe (Muridae: Rodentia). Mol Ecol Notes 1:260–263

    Article  CAS  Google Scholar 

  • Millins C, Gilbert L, Medlock J, Hansford K, Thompson DB, Biek R (2017) Effects of conservation management of landscapes and vertebrate communities on Lyme borreliosis risk in the United Kingdom. Philos Trans R Soc B 372:20160123

    Article  Google Scholar 

  • Morganti G, Gavaudan S, Canonico C, Ravagnan S, Olivieri E, Diaferia M, Marenzoni ML, Antognoni MT, Capelli G, Silaghi C, Veronesi F (2017) Molecular survey on Rickettsia spp., Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato, and Babesia spp. in Ixodes ricinus ticks infesting dogs in Central Italy. Vector Borne Zoonotic Dis 17:743–747

    Article  PubMed  Google Scholar 

  • Mori E, Zozzoli R, Menchetti M (2018) Global distribution and status of introduced Siberian chipmunks Eutamias sibiricus. Mammal Rev 48:139–152

    Article  Google Scholar 

  • Nentwig W, Bacher S, Kumschick S, Pyšek P, Vilà M (2018) More than “100 worst” alien species in Europe. Biol Invasions 6:1611–1621

    Article  Google Scholar 

  • Pajoro M, Pistone D, Varotto Boccazzi I, Mereghetti V, Bandi C, Fabbi M, Scattorin F, Sassera D, Montagna M (2018) Molecular screening for bacterial pathogens in ticks (Ixodes ricinus) collected on migratory birds captured in Northern Italy. Folia Parasitol in press, 65

  • Parola P, Paddock CD, Socolovschi C, Labruna MB, Mediannikov O, Kernif T, Abdad MY, Stenos J, Bitam I, Fournier PE, Raoult D (2013) Update on tick-borne rickettsioses around the world: a geographic approach. Clin Microbiol Rev 26:657–702

    Article  PubMed  PubMed Central  Google Scholar 

  • Pérez-Eid C (2007) Les tiques: identification, biologie, importance médicale et vétérinaire. Lavoisier Editions, Paris

    Google Scholar 

  • Pisanu B, Marsot M, Marmet J, Chapuis JL, Rèale D, Vourc’h G (2010) Introduced Siberian chipmunks are more heavily infested by ixodid ticks than are native bank voles in a suburban forest in France. Int J Parasitol 40:1277–1283

    Article  CAS  PubMed  Google Scholar 

  • Prediger J, Horčičková M, Hofmannová L, Sak B, Ferrari N, Mazzamuto MV, Romeo C, Wauters LA, McEvoy J, Kváč M (2017) Native and introduced squirrels in Italy host different Cryptosporidium spp. Eur J Protistol 61:64–75

    Article  PubMed  Google Scholar 

  • Prenter J, MacNeil C, Dick JT, Dunn AM (2004) Roles of parasites in animal invasions. Trends Ecol Evol 19:385–390

    Article  PubMed  Google Scholar 

  • Price PW, Westoby M, Rice B, Atsatt PR, Fritz RS, Thompson JN, Mobley K (1986) Parasite mediation in ecological interactions. Annu Rev Ecol Syst 17:487–505

    Article  Google Scholar 

  • Ragagli C, Mannelli A, Ambrogi C, Bisanzio D, Ceballos LA, Grego E, Martello E, Selmi M, Tomassone L (2016) Presence of host-seeking Ixodes ricinus and their infection with Borrelia burgdorferi sensu lato in the Northern Apennines, Italy. Exp Appl Acarol 69:167–178

    Article  PubMed  Google Scholar 

  • Rizzoli A, Silaghi C, Obiegala A, Rudolf I, Hubálek Z, Földvári G, Plantard O, Vayssier-Taussat M, Bonnet S, Spitalskà E, Kazimírová M (2014) Ixodes ricinus and its transmitted pathogens in urban and peri-urban areas in Europe: new hazards and relevance for public health. Front Public Health 2:251

    Article  PubMed  PubMed Central  Google Scholar 

  • Romeo C, Wauters LA, Ferrari N, Lanfranchi P, Martinoli A, Pisanu B, Preatoni DG, Saino N (2014) Macroparasite fauna of alien grey squirrels (Sciurus carolinensis): composition, variability and implications for native species. PLoS One 9:e88002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roux V, Rydkina LE, Eremeeva M, Raoult D (1997) Citrate synthase gene comparison, a new tool for phylogenetic analysis, and its application for the Rickettsiae? Int J Syst Bacteriol 47:252–261

    Article  CAS  PubMed  Google Scholar 

  • Sonè K, Tojo H (1993) Trapping capabilities of two live-traps used on two species of field mice, Apodemus speciosus and A. argenteus. Appl Entomol Zool 28:537–545

    Article  Google Scholar 

  • Thomas K, Tompkins DM, Sainsbury AW, Wood AR, Dalziel R, Nettleton PF, McInnes CJ (2003) A novel poxvirus lethal to red squirrels (Sciurus vulgaris). J Gen Viroly 84:3337–3341

    Article  CAS  Google Scholar 

  • Vourc’h G, Marmet J, Chassagne M, Bord S, Chapuis JL (2007) Borrelia burgdorferi sensu lato in Siberian chipmunks (Tamias sibiricus) introduced in suburban forests in France. Vector Borne Zoonotic Dis 7:637–641

    Article  PubMed  Google Scholar 

  • Welch JN, Leppanen C (2017) The threat of invasive species to bats: a review. Mammal Rev 47:277–290

    Article  Google Scholar 

  • Zozzoli R, Menchetti M, Mori E (2018) Spatial behaviour of an overlooked alien squirrel: the case of Siberian chipmunks Eutamias sibiricus. Behav Process 153:107–111

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank the following (in alphabetical order): Alvise Camurri-Piloni, Jean-Louis Chapuis, Mauro Bon, Michele Cassol, Luca Lapini, Andrey Lissovsky, Mattia Menchetti, Ekaterina Obolenskaya, Giuseppe Tormen, and Arianna Spada who provided us with useful information to set our survey at best. We are deeply indebted with Prof. Danilo Russo (University of Naples Federico II), who provided us with the Sherman traps. Alberto Camporesi, Fabio Dartora, Andrea Vendramin, and Marta Villa helped us during our field work. Riccardo Castiglia (University of Roma “La Sapienza”) made available the genetic analyses facilities. EM was funded by the “Giuseppe Guelfi” Grant of the Accademia Nazionale dei Lincei (Roma, Italy). Prof. Jean-Claude Beaucournu kindly helped us for flea identification. Dr. Vasco Sfondrini kindly revised the first version of our manuscript and improved the English grammar and syntax. Two anonymous reviewers and the editor of provided us with useful comments, which greatly improved our manuscript.

Author information

Authors and Affiliations

  1. Dipartimento di Scienze della Vita, Università degli Studi di Siena, Via P.A. Mattioli 4, 53100, Siena, Italy

    Emiliano Mori

  2. Accademia Nazionale dei Lincei, Palazzo Corsini, Via della Lungara 10, 00165, Rome, Italy

    Emiliano Mori

  3. Centre d’expertise et de données sur la nature (UMS Patrimoine Naturel), AFB, MNHN, CNRS, CP41, 36 rue Geoffroy Saint-Hilaire, 75005, Paris, France

    Benoît Pisanu

  4. Centre d’Ecologie et des Sciences de la Conservation (UMR 7204), MNHN, CNRS, UPMC, Sorbonne Universités, Paris, France

    Benoît Pisanu

  5. Dipartimento di Scienze Chimiche, della Vita e della Sostenibilità Ambientale, Università degli Studi di Parma, Parco Area delle Scienze, 11a, 43124, Parma, Italy

    Rudy Zozzoli

  6. Dipartimento di Biologia e Biotecnologie “Charles Darwin”, Università di Roma “La Sapienza”, Via Borelli 50, 00161, Rome, Italy

    Emanuela Solano

  7. Dipartimento di Biologia e Biotecnologia “L. Spallanzani”, Università degli Studi di Pavia, Via A. Ferrata 9, 27100, Pavia, Italy

    Emanuela Olivieri

  8. Dipartimento di Scienze Agrarie e Agroambientali, Università degli Studi di Milano, Via Celoria 2, 20133, Milan, Italy

    Davide Sassera & Matteo Montagna

Authors
  1. Emiliano Mori
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Benoît Pisanu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rudy Zozzoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Emanuela Solano
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Emanuela Olivieri
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Davide Sassera
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Matteo Montagna
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Emiliano Mori.

Ethics declarations

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Ethical approval was provided within the ISPRA permission (ISPRA, prot. 24128/T-A31).

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Section Editor: Boris R. Krasnov

Electronic supplementary material

ESM 1

(DOCX 77 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mori, E., Pisanu, B., Zozzoli, R. et al. Arthropods and associated pathogens from native and introduced rodents in Northeastern Italy. Parasitol Res 117, 3237–3243 (2018). https://doi.org/10.1007/s00436-018-6022-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-018-6022-4

Keywords

Search

Navigation