Abstract
The progressive decline in the hare population across Europe has been associated with the occurrence of European brown hare syndrome (EBHS), a highly contagious disease considered endemic in all European countries. This study aimed to evaluate the in-field temporal dynamics of European brown hare syndrome virus (EBHSV) infection in wild European brown hares (Lepus europaeus) and to test the influence of population density on EBHS seroprevalence. A total of 512 blood samples were collected from free ranging hares captured for restocking in seven different areas of the province of Brescia (Northern Italy) during seven consecutive years (2006–2013) and tested using a competitive ELISA. A generalized linear mixed model estimated the yearly effects of population density on EBHS prevalence. Of the 512 tested, 344 (67.2 %) tested positive for EBHSV antibodies, with the annual seroprevalence ranging from 94.3 to 35.8 %. The prevalence was 3.303 times higher in areas with a density of over 15 hares/km2 and declined over the years. The results indicate the ongoing transmission of the virus in the tested brown hare population. Since the eradication of EBHS in a wild population is not feasible, a strategy aimed at promoting the endemic stability of the virus through density-dependent mechanisms could be applied; however, this seems more difficult in practice than in theory and would most likely require a very high density of brown hares.
Similar content being viewed by others
References
Agresti A (2002) Categorical data analysis, vol 359. Hoboken, New Jersey
Armitage P (1955) Tests for linear trends in proportions and frequencies. Biometrics 11:375–386
Barnes RFW, Tapper SC (1985) A method for counting hares by spotlight. J Zool 206:273–276
Capucci L, Scicluna MT, Lavazza A (1991) Diagnosis of viral haemorrhagic disease of rabbits and European brown hare syndrome. Rev Sci Tech Off Int Epiz 10:347–370
Capucci L, Lavazza A (2008) Rabbit haemorrhagic disease. In: OIE (ed) Manual of diagnostic tests and vaccines for terrestrial animals, 6th edn. OIE, Paris, France, pp 947–961
Cooke BD, Robinson AJ, Merchant JC, Nardin A, Capucci L (2000) Use of ELISAs in field studies of rabbit haemorrhagic disease (RHD) in Australia. Epidemiol Infect 124:563–576
Duff JP, Gavier-Widén D (2012) Calicivirus infection. In: Duff JP, Gavier-Widén D, Meredith A (eds) Infectious disease of wild mammals and birds in Europe. Wiley-Blackwell, Oxford, UK, pp 73–85
Edwards PJ, Fletcher MR, Berny P (2000) Review of the factors affecting the decline of the European brown hare, Lepus europaeus (Pallas, 1778) and the use of wildlife incident data to evaluate the significance of paraquat. Agric Ecosyst Environ 79:95–103
Frölich K, Wisser J, Schmuser H, Fehlberg U, Neubauer H, Grunow R, Konstantin Nikolaou K, Priemer J, Thiede S, Streich WJ, Speck S (2003) Epizootiologic and ecologic investigations of European brown hares (Lepus europaeus) in selected populations from Schleswig-Holstein, Germany. J Wildl Dis 39:751–761
Frölich K, Lavazza A (2008) European brown hare syndrome. In: Lagomorph biology. Springer Berlin Heidelberg pp 253–261
Goldstein H (2011) Multilevel models for discrete response data. In: Goldstein H (ed) Multilevel statistical models, 4th edn. Wiley & Sons, West Sussex, UK
Gustaffson K, Svensson T, Uggla A (1989) Studies on a idiopathic syndrome in the brown hare (Lepus europaeus P.) and mountain hare (Lepus timidus L.) in Sweden, with special reference to hepatic lesions. J Vet Med A 36:631–637
Henning J, Meers J, Davies PR, Morris RS (2005) Survival of rabbit haemorrhagic disease virus (RHDV) in the environment. Epidemiol Infect 133:719–730
Lavazza A, Vecchi G (1989) Osservazione su alcuni episodi di mortalità nelle lepri. Evidenziazione al microscopio elettronico di una particella virale Nota preliminare. Selezione Veterinaria 30:461–467
Lavazza A, Guberti V, Ferri M, Zanni ML, Poglayen G, Nardin A, Capucci L (1997) Epidemiology of European brown hare syndrome (EBHS) in Modena province (North Italy). In: Proceedings of the 4th International Congress of the European Society for Veterinary Virology, Edinburgh, UK, pp 34–37
Paci G, Lavazza A, Ferretti M, Santilli F, Bagliacca M (2011) Relationship between anti-European brown hare syndrome serological titers and brown hare (Lepus europaeus Pallas) densities. Int J Zool. doi:10.1155/2011/436193
R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Santilli F, Paci G, Bagliacca M (2014) Winter habitat selection by the European hare (Lepus europaeus) during feeding activity in a farmland area of southern Tuscany (Italy). Hystrix 25, doi: 10.4404/hystrix-25.1-7878
Scicluna MT, Lavazza A, Capucci L (1994) European brown hare syndrome in northern Italy: results of a virological and serological survey. Rev Sci Tech Off Int Epizoot 13:893–904
Tizzani P, Menzano A, Dematteis A, Meneguz PG (2013) Methodological problems related to spotlight count as a census technique for Lepus europaeus in an alpine environment. Acta Theriol 1–6
Wirblich C, Meyers G, Ohlinger VF, Capucci L, Eskens U, Haas B, Thiel HJ (1994) European brown hare syndrome virus: relationship to rabbit hemorrhagic disease virus and other caliciviruses. J Virol 68:5164–5173
Zanni ML, Benassi MC, Scicluna MT, Lavazza A, Capucci L (1993) Clinical evolution and diagnosis of an outbreak of European brown hare syndrome in hares reared in captivity. Rev Sci Tech 12:931–940
Acknowledgments
The authors gratefully acknowledge the cooperation of local hunters (Ambito Territoriale di Caccia Unico di Brescia, Brescia Province, Northern Italy), without whom, this study would not have been possible.
The authors wish to thank Alberto Tiraboschi, Giuseppe Bertocchi, Cristina Palotta, Giuliana Botti and Giuseppe Bozzoni of the Brescia laboratory IZSLER for the technical support.
The authors also wish to thank Lesley Benyon (ScienceDocs) and Mr. Alastair Tweedie for the editing of this manuscript.
Conflict of interest
The authors of this study received no financial aid or had personal relationships with people or organizations that could inappropriately influence or bias their work.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Artois
Rights and permissions
About this article
Cite this article
Chiari, M., Ferrari, N., Giardiello, D. et al. Temporal dynamics of European brown hare syndrome infection in Northern Italian brown hares (Lepus europaeus). Eur J Wildl Res 60, 891–896 (2014). https://doi.org/10.1007/s10344-014-0856-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10344-014-0856-6