Published February 26, 2019 | Version Published paper
Journal article Open

The Eastern cottontail (Sylvilagus floridanus) in Tuscany (Central Italy): weak evidence for its role as a host of EBHSV and RHDV.

  • 1. Scuola di Agraria, Università degli Studi di Firenze
  • 2. Istituto Superiore per la Protezione e la Ricerca Ambientale (ISPRA)
  • 3. Istituto Zooprofilattico Sperimentale della Lombardia e dell'Emilia-Romagna "Bruno Ubertini"
  • 4. Regione Toscana

Description

During the last few decades native European hares (Lepus europaeus) have declined in Central and Northern Italy. Despite this trend having multiple causes, it was hypothesized that invasive Eastern cottontails (Sylvilagus floridanus) contributed to the decline through apparent competition and disease transmission. In this research we explored whether cottontails may act as carriers of EBHSV (European Brown Hare Syndrome Virus) and RHDV (Rabbit Haemorrhagic Disease Virus), the viral agents of two major diseases affecting lagomorphs in Europe. We took biological samples from 267 cottontails that were shot between March and August 2015 in Tuscany, performing specific antigenic and serological ELISA tests for both viruses as well as molecular investigation for lagoviruses. Virologic tests were all negative and serological titers were below the threshold that could indicate the active circulation of either of the two pathogenic viruses. Our findings suggest that cottontails were not playing an active role as carriers or reservoirs for both known virulent lagoviruses and were also not infected with non-pathogenic lagoviruses - at least at that time in the study area.

Files

D'Angeloetal_2019.pdf

Files (4.8 MB)

Name Size Download all
md5:7436e20a10810dc69383c01629babf14
4.8 MB Preview Download

Additional details

References

  • Bertolino, S., Hofmannová, L., Girardello, M., Modry, D., 2004. Richness, origin and structure of an Eimeria community in a population of Eastern cottontail (Sylvilagus floridanus) introduced into Italy. Parasitology. 137(8): 1179-1186
  • Camarda A., Pugliese N., Cavadini P., Circella E., Capucci L., Caroli A., Legretto M., Mallia E., Lavazza A., 2014. Detection of the new emerging rabbit haemorrhagic disease type 2 virus (RHDV2) in Sicily from rabbit (Oryctolagus cuniculus) and Italian hare (Lepus corsicanus). Res. Vet. Sci. 97(3): 642-645.
  • Cammi G., Capucci L., Bernini F., Lavazza A., 2003. Indagine sulla diffusione dell'EBHS nella popolazione di lepri presente nel territorio della provincia di piacenza nel 1997. In Proceedings of the 2nd Conference of the Società Italiana di Ecopatologia della Fauna (SIEF). J. Mt. Ecol. 7(suppl): 165-174.
  • apucci L., Fusi P., Lavazza A., Pacciarini M.L., Rossi C., 1996. Detection and preliminary characterization of a new rabbit calicivirus related to Rabbit Hemorrhagic Disease Virus but non pathogenic. J. Virol. 70 (12): 8614-8623.
  • Cavadini P., Molinari S., Pezzoni G., Chiari M., Brocchi E., Lavazza A., Capucci L., 2015. Identification of a new non-pathogenic lagovirus in Lepus europeaus. In: Proceedings of the 10th International Congress for Veterinary Virology and 9th Annual Epizone Meeting "Changing Viruses in a Changing World" Montpellier, France, August 31st - September 3rd, 2015: 76-77.
  • Cerri J., Ferretti M., Tricarico E., 2016. Are you aware of what you are doing? Asking Italian hunters about an invasive alien species they are introducing. J. Nat. Conserv. 34: 15-23.
  • Cerri J., Ferretti M., Bertolino S., 2017. Rabbits killing hares: an invasive mammal modifies native predator–prey dynamics. Anim. Conserv. 20(6): 511-519.
  • Chiari M, Bonavetti E, Zanoni M, Lavazza A, 2012. Application of a surveillance program in wild european brown hares (Lepus europeaus) in Brescia Province, North Italy. Hystrix Ital J Mammalogy. - Vol. n.s., suppl . p 40
  • Chiari M., Gioia E., Ferrari N., Capucci L., Lavazza A., 2012. Utility of blotting paper for serological tests to perform monitoring programs for European Brown Hare Syndrome (EBHS). Proceedings joint 61st WDA /10th Biennal EWDA Conference "Convergence in wildlife health". Lyon 23-27 July 2012: 384.
  • Cooke B.D., Robinson A.J., Merchant J.C., Nardin A., Capucci L., 2000. Use of ELISAs in field studies of rabbit haemorrhagic disease (RHD) in Australia. Epidemiol. Infect., 124, 563–576.
  • Dori P., Scalisi M., Mori E., 2018. "An American near Rome"… and not only! Presence of the eastern cottontail in Central Italy and potential impacts on the endemic and vulnerable Apennine hare. Mammalia. doi: 10.1515/mammalia-2018-0069
  • Drews B., Roellig K., Szentiks C.A., Fickel J., Schroeder K., Duff P., Lavazza A., Hildebrandt T. B., Goeritz F., 2011. Epidemiology, control and management of an EBHS outbreak in captive hares. Vet Microbiol. 154(1-2): 37-48.
  • Esteves P.J., Abrantes J., Bertagnoli S., Cavadini P., Gavier-Widén D., Guitton J.S., Lavazza A., Lemaitre E., Letty J., Lopes A.M., Neimanis A.S., Ruvoën-Clouet N., Le Pendu J., Marchandeau S., Le Gall-Reculé G., 2015. Emergence of pathogenicity in lagoviruses: evolution from pre-existing non-pathogenic strains or through a species jump? PLoS Pathog. 11(11): e1005087. doi:10.1371/journal.ppat.1005087
  • Frolich K., Lavazza A., 2007. European Brown hare Syndrome. In: Alves P.C., Ferrand N., Hacklaender K. (Eds). Lagomorph Biology, Springer, Berlin. 253-262.
  • Gallo, M. G., Tizzani, P., Peano, A., Rambozzi, L., Meneguz, P. G., 2005. Eastern cottontail (Sylvilagus floridanus) as carrier of dermatophyte fungi. Mycopathologia. 160(2): 163-166.
  • Lavazza A., Cavadini P., Barbieri I., Tizzani P., Pinheiro A., Abrantes J., Esteves P.J., Grilli G., Gioia E., Zanoni M., Meneguz P.G., Guitton J.S., Marchandeau S., Chiari M., Capucci L., 2015. Field and experimental data indicate that the eastern cottontail (Sylvilagus floridanus) is susceptible to infection with European brown hare syndrome (EBHS) virus and not with rabbit haemorrhagic disease (RHD) virus. Vet. Res. 46(1): 13. doi 10.1186/s13567-015-0149-4
  • Lavazza A., Cavadini P., Capucci L., 2013. RHDV2: un nuovo virus della malattia emorragica virale del coniglio. BENV Bollettino Epidemiologico Nazionale Veterinario. 14: 5-10
  • Lemaitre E, Zwingelstein F, Marchandeau S, Le Gall-Reculé G., 2018. First complete genome sequence of a European non-pathogenic rabbit Calicivirus (lagovirus GI.3). Arch Virol. doi: 10.1007/s00705-018-3901-z. [Epub ahead of print]
  • Lopes A.M., Marques S., Silva E., Magalhães M.J., Pinheiro A., Alves P.C., Le Pendu J., Esteves P.J., Thompson G., Abrantes J., 2014. Detection of RHDV strains in the Iberian hare (Lepus granatensis): earliest evidence of rabbit lagovirus cross-species infection. Vet. Res. 45: 94.
  • Mutze G., Bird P., Jennings S., Peacock D., de PreuN., Kovaliski J., Cooke B., Capucci L., 2014. Recovery of South Australian rabbit populations from the impact of rabbit haemorrhagic disease. Wildlife Research, 41, 552–559. http://dx.doi.org/10.1071/WR14107
  • Neimanis A., Ahola H., Larsson Pettersson U., Lopes A.M., Abrantes J., Zohari S., Esteves P.J., Gavier-Widén D., 2018. Overcoming species barriers: an outbreak of Lagovirus europaeus GI.2/RHDV2 in an isolated population of mountain hares (Lepus timidus). BMC Veterinary Research 14:367. https://doi.org/10.1186/s12917-018-1694-7
  • OIE, 2012: Rabbit haemorrhagic disease, Chapter 2.6.2. In: Biological Standards Commission; the World Organisation For Animal Health (OIE), OIE Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, OIE, Paris, France (NB: Version adopted in May 2016) pp 941–955.
  • Pavliska P. L., Riegert J., Grill S., Šálek M., 2018. The effect of landscape heterogeneity on population density and habitat preferences of the European hare (Lepus europaeus) in contrasting farmlands. Mamm. Biol. 88: 8-15.
  • Poli A., Nigro M., Gallazzi D., Sironi G., Lavazza A., Gelmetti D., 1991. Acute hepatosis in the European Brown Hare (Lepus europaeus) in Italy. J. Wild. Dis. 27(4): 621-629.
  • Portejoie Y., Faure E., Georges F., Artois M., Peroux R., Guitton J.S., 2009. Investigation of specific European Brown Hare Syndrome antibodies in wild hares using blood samples dried on blotting paper. Eur. J. Wild. Res. 55(1): 53-58.
  • Puggioni G., Cavadini P., Maestrale C., Scivoli R., Botti G., Ligios C., Le Gall-Reculé G., Lavazza A., Capucci L., 2013. The new French 2010 variant of the rabbit hemorrhagic disease virus causes an RHD-like disease in the Sardinian Cape hare (Lepus capensis mediterraneus). Vet. Res. 44(1): 95.
  • Santilli F., 2007. Factors affecting brown hare (Lepus europaeus) hunting bags in Tuscany region (central Italy). Hystrix. 17(2): 143-153.
  • Santilli F., Galardi L., 2016. Effect of habitat structure and type of farming on European hare (Lepus europaeus) abundance. Hystrix. 27(2): 1-3.
  • Schai-Braun S.C., Reichlin T. S., Ruf T., Klansek E., Tataruch F., Arnold W., Hackländer, K., 2015. The European hare (Lepus europaeus): a picky herbivore searching for plant parts rich in fat. PloS one. 10(7): e0134278.
  • Schmidt N. M., Asferg T., Forchhammer M.C., 2004. Long-term patterns in European brown hare population dynamics in Denmark: effects of agriculture, predation and climate. BMC Ecol. 4(1): 15.
  • Smith R.K., Vaughan Jennings N., Harris S., 2005. A quantitative analysis of the abundance and demography of European hares Lepus europaeus in relation to habitat type, intensity of agriculture and climate. Mammal Rev. 35(1): 1-24.
  • Velarde R., Cavadini P., Neimanis A., Cabezón O., Chiari M., Gaffuri A., Lavín S., Grilli G., Gavier-Widén D., Lavazza A., Capucci L., 2016. Spillover events of infection of brown hares (Lepus europaeus) with rabbit haemorrhagic disease type 2 virus (RHDV2) caused sporadic cases of an European Brown hare syndrome like-disease in Italy and Spain. Transbound. Emerg. Dis. 64: 1750–1761.
  • Vidus-Rosin A., Meriggi A., Cardarelli E., Serrano-Perez S., Mariani M.C., Corradelli C., Barba A., 2011. Habitat overlap between sympatric European hares (Lepus europaeus) and Eastern cottontails (Sylvilagus floridanus) in northern Italy. Acta Theriol. 56: 53–61.
  • Zanet, S., Palese, V., Trisciuoglio, A., Alonso, C. C., & Ferroglio, E., 2013. Encephalitozoon cuniculi, Toxoplasma gondii and Neospora caninum infection in invasive Eastern Cottontail Rabbits Sylvilagus floridanus in Northwestern Italy. Vet. Parasitol. 197(3-4): 682-684
  • Zanni M.L., Benassi M.C, Scicluna M.T., Lavazza A., Capucci L., 1993. Clinical evolution and diagnosis of an episode of European Brown Hare Syndrome (EBHS) in hares reared in captivity. Rev. sci. tech. Off. int. Epiz. 12 (3): 931-940