Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-24T14:02:58.982Z Has data issue: false hasContentIssue false

The two sides of border disease in Pyrenean chamois (Rupicapra pyrenaica): silent persistence and population collapse

Published online by Cambridge University Press:  08 June 2015

Ignasi Marco*
Affiliation:
Servei d'Ecopatologia de Fauna Salvatge, Departament de Medicina i Cirurgia Animals, Facultat de Veterinària, Universitat Autònoma de Barcelona, 08193-Bellaterra, Spain
Oscar Cabezón
Affiliation:
Servei d'Ecopatologia de Fauna Salvatge, Departament de Medicina i Cirurgia Animals, Facultat de Veterinària, Universitat Autònoma de Barcelona, 08193-Bellaterra, Spain IRTA-Centre de Recerca en Sanitat Animal (CRESA), Universitat Autònoma de Barcelona, 08193-Bellaterra, Spain
Roser Velarde
Affiliation:
Servei d'Ecopatologia de Fauna Salvatge, Departament de Medicina i Cirurgia Animals, Facultat de Veterinària, Universitat Autònoma de Barcelona, 08193-Bellaterra, Spain
Laura Fernández-Sirera
Affiliation:
École Nationale Vétérinaire de Toulouse, 31300-Toulouse, France
Andreu Colom-Cadena
Affiliation:
Servei d'Ecopatologia de Fauna Salvatge, Departament de Medicina i Cirurgia Animals, Facultat de Veterinària, Universitat Autònoma de Barcelona, 08193-Bellaterra, Spain
Emmanuel Serrano
Affiliation:
Servei d'Ecopatologia de Fauna Salvatge, Departament de Medicina i Cirurgia Animals, Facultat de Veterinària, Universitat Autònoma de Barcelona, 08193-Bellaterra, Spain Departamento de Biologia and CESAM, Universidade de Aveiro, 3810-193 Aveiro, Portugal
Rosa Rosell
Affiliation:
IRTA-Centre de Recerca en Sanitat Animal (CRESA), Universitat Autònoma de Barcelona, 08193-Bellaterra, Spain Departament d'Agricultura, Ramaderia, Pesca, Alimentació i Medi Natural, Generalitat de Catalunya, 08007-Barcelona, Spain
Encarna Casas-Díaz
Affiliation:
Servei d'Ecopatologia de Fauna Salvatge, Departament de Medicina i Cirurgia Animals, Facultat de Veterinària, Universitat Autònoma de Barcelona, 08193-Bellaterra, Spain
Santiago Lavín
Affiliation:
Servei d'Ecopatologia de Fauna Salvatge, Departament de Medicina i Cirurgia Animals, Facultat de Veterinària, Universitat Autònoma de Barcelona, 08193-Bellaterra, Spain
*
*Corresponding author. E-mail: [email protected]

Abstract

In 2001, border disease virus (BDV) was identified as the cause of a previously unreported disease in Pyrenean chamois (Rupicapra pyrenaica) in Spain. Since then, the disease has caused a dramatic decrease, and in some cases collapse, of chamois populations and has expanded to nearly the entire distribution area in the Pyrenees. Chamois BDV was characterized as BDV-4 genotype and experimental studies confirmed that it was the primary agent of the disease. The infection has become endemic in the Central and Eastern Pyrenees. However, while most Pyrenean chamois populations have been severely affected by the disease, others have not, despite the circulation of BDV in apparently healthy individuals, suggesting the existence of different viral strategies for persisting in the host population. Changes in the interplay of pathogen, host and environmental factors may lead to the formation of different disease patterns. A key factor influencing disease emergence may be pathogen invasiveness through viral mutation. Host factors, such as behavior, immunity at the population level and genetic variability, may also have driven different epidemiological scenarios. Climatic and other ecological factors may have favored secondary infections, such as pneumonia, that under particular circumstances have been major contributing factors in the high mortality observed in some areas.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Altizer, S, Harvell, D and Friedle, E (2003). Rapid evolutionary dynamics and disease threats to biodiversity. Trends in Ecology and Evolution 18: 589596.CrossRefGoogle Scholar
Altizer, S, Ostfeld, RS, Johnson, PTJ, Kutz, S and Drew Harvell, C (2013). Climate change and infectious diseases: from evidence to a predictive framework. Science 341: 514519.CrossRefGoogle ScholarPubMed
Arnal, M, Fernández-de-Luco, D, Riba, L, Maley, M, Gilray, J, Willoughby, K, Vilcek, S and Nettleton, PF (2004). A novel pestivirus associated with deaths in Pyrenean chamois (Rupicapra pyrenaica pyrenaica). Journal of General Virology 85: 36533657.CrossRefGoogle ScholarPubMed
Bertin-Cavarait, C (2006). Un déperissement chez des agneaux coincide avec l'infection par un border virus chez l'isard. La Semaine Veterinaire 1222: 42.Google Scholar
Cabezón, O, Rosell, R, Sibila, M, Lavín, S, Marco, I and Segalés, J (2010a). Experimental infection of pigs with Border disease virus isolated from Pyrenean chamois (Rupicapra pyrenaica). Journal of Veterinary Diagnostic Investigations 22: 360365.CrossRefGoogle ScholarPubMed
Cabezón, O, Rosell, R, Velarde, R, Mentaberre, G, Casas-Díaz, E, Lavín, S and Marco, I (2010b). Border disease virus shedding and detection in naturally-infected Pyrenean chamois (Rupicapra pyrenaica). Journal of Veterinary Diagnostic Investigations 22: 360365.CrossRefGoogle ScholarPubMed
Cabezón, O, Velarde, R, Rosell, R, Lavín, S, Segalés, J and Marco, I (2010c). Experimental infection in lambs with a Border Disease Virus isolated from Pyrenean chamois (Rupicapra pyrenaica). Veterinary Record 167: 619621.CrossRefGoogle Scholar
Cabezón, O, Velarde, R, Mentaberre, G, Fernandez-Sirera, L, Casas-Díaz, E, Lopez-Olvera, J, Serrano, E, Rosell, R, Riquelme, C, Lavin, S, Segales, J and Marco, I (2011). Experimental infection with chamois Border Disease Virus causes long-lasting viraemia and disease in Pyrenean chamois (Rupicapra pyrenaica). Journal of General Virology 92: 24942501.CrossRefGoogle ScholarPubMed
Cavallero, S, Marco, I, Lavín, S, D'Amelio, S and López-Olvera, JR (2012). Polymorphisms at MHC class II DRB1 exon 2 locus in Pyrenean chamois (Rupicapra pyrenaica pyrenaica). Infection Genetics and Evolution 12: 10201026.CrossRefGoogle ScholarPubMed
Crampe, JP, Bon, R, Gerard, JF, Serrano, E, Caens, P, Florence, E and Gonzalez, G (2007). Site fidelity, migratory behaviour, and spatial organization of female isards (Rupicapra pyrenaica) in the Pyrenees National Park, France. Canadian Journal of Zoology 85: 1625.CrossRefGoogle Scholar
Crampe, JP, Caens, P, Empain, M, Florence, E, Kieser, X, Laffeuillade, N, Llanes, P and Morceau, M (2008). L'epidémie de kérato-conjonctivite de l'isard de 2007 en vallée de Cauterets: modalités et consequences démographiques. 26èmes Rencontres du Groupe d'Etudes sur l'Ecopatho¬logie de la Fauna Sauvage de Montagne (GEEFSM). France: Faucon de Barcelonette, pp. 6.Google Scholar
Engering, A, Hogerwerf, L and Slingenbergh, (2013). Pathogen-host-environment interplay and disease emergence. Emerging Microbes and Infections 2, e5; doi: 10.1038/emi.2013.5.CrossRefGoogle ScholarPubMed
Fernández-Sirera, L, Riba, L, Cabezón, O, Rosell, R, Serrano, E, Lavín, S and Marco, I (2012a). Surveillance of border disease in wild ungulates and first outbreak of disease in Pyrenean chamois (Rupicapra pyrenaica) in Andorra. Journal of Wildlife Diseases 48: 10211029.CrossRefGoogle Scholar
Fernández-Sirera, L, Cabezón, O, Allepuz, A, Rosell, R, Riquelme, C, Serrano, E, Lavín, S and Marco, I (2012b). Two different epidemiological scenarios of border disease in the populations of Pyrenean chamois (Rupicapra p. pyrenaica) after the first disease outbreaks. PLoS ONE 7: e51031.CrossRefGoogle ScholarPubMed
Ferroglio, E (2012). Pasteurella infections. In: Gavier-Widén, D, Duff, JP and Meredith, A (eds) Infectious diseases of wild mammals and birds in Europe. West Sussex, UK: Wiley–Blackwell, pp. 310317.Google Scholar
Frölich, K (2012). Bovine viral diarrhoea. In: Gavier-Widén, D, Duff, JP and Meredith, A (eds) Infectious Diseases of Wild Mammals and Birds in Europe. West Sussex, UK: Wiley–Blackwell, pp. 152157.Google Scholar
Frölich, K, Jung, S, Ludwig, A, Lieckfeldt, D, Gibert, P, Gauthier, D and Hars, J (2005). Detection of a newly described pestivirus of Pyrenean chamois (Rupicapra pyrenaica pyrenaica) in France. Journal of Wildlife Diseases 41: 606610.Google Scholar
Haider, N, Rahman, MS, Khan, SU, Mikolon, A, Gurley, ES, Osmani, MG, Shanta, IS, Paul, SK, Macfarlane-Berry, L, Islam, A, Desmond, J, Epstein, JH, Daszak, P, Azim, T, Luby, SP, Zeidner, N and Rahman, NZ (2014). Identification and epidemiology of a rare HoBi-like pestivirus strain in Bangladesh. Transboundary and Emerging Diseases 61: 193198.CrossRefGoogle ScholarPubMed
Herrero, J, Lovari, S and Berducou, C (2008). Rupicapra pyrenaica. The IUCN Red List of Threatened Species. Version 2014.2. www.iucnredlist.org. Downloaded on 04 October 2014.Google Scholar
Hurtado, A, Aduriz, G, Gómez, N, Oporto, B, Juste, RA, Lavín, S, López-Olvera, J and Marco, I (2004). Molecular identification of a new pestivirus associated to an outbreak of disease in the Pyrenean chamois (Rupicapra pyrenaica pyrenaica) in Spain. Journal of Wildlife Diseases 40: 796800.CrossRefGoogle Scholar
Lauring, AS, Frydman, J and Andino, R (2013). The role of mutational robustness in RNA virus evolution. Nature Reviews Microbiology 11: 327336.CrossRefGoogle ScholarPubMed
Luzzago, C, Ebranati, E, Lanfranchi, P, Cabezón, O, Lavín, S, Rosell, R, Rossi, L, Zehender, G and Marco, I (2014). Spatial and temporal phylogeny of border disease virus in pyrenean chamois. In: Chamos International Congress, Majella National Park, Italy.Google Scholar
Marco, I (2012). Pestivirus of chamois and border disease. In: Gavier-Widén, D, Duff, JP and Meredith, A (eds) Infectious Diseases of Wild Mammals and Birds in Europe. West Sussex, UK: Wiley–Blackwell, pp. 147152.Google Scholar
Marco, I, López-Olvera, JR, Rosell, R, Vidal, E, Hurtado, A, Juste, R, Pumarola, M and Lavín, S (2007). Severe outbreak of disease in the southern chamois (Rupicapra pyrenaica) associated with border disease virus infection. Veterinary Microbiology 120: 3341.CrossRefGoogle ScholarPubMed
Marco, I, Rosell, R, Cabezón, O, Mentaberre, G, Casas, E, Velarde, R, López-Olvera, JR, Hurtado, A and Lavín, S (2008). Epidemiological study on border disease virus infection in Southern chamois (Rupicapra pyrenaica) after an outbreak of disease in the Pyrenees (NE Spain). Veterinary Microbiology 127: 2938.CrossRefGoogle ScholarPubMed
Marco, I, Rosell, R, Cabezón, O, Beneria, M, Mentaberre, G, Casas, E, Hurtado, A, López-Olvera, JR and Lavín, S (2009a). Serologic and virologic investigations into pestivirus infection in wild and domestic ruminants in the Pyrenees (NE Spain). Research in Veterinary Science 87: 149153.CrossRefGoogle ScholarPubMed
Marco, I, Rosell, R, Cabezón, O, Mentaberre, G, Casas, E, Velarde, R and Lavín, S (2009b). Border disease virus in chamois mass mortality. Emerging Infectious Diseases 15: 448451.CrossRefGoogle Scholar
Marco, I, Cabezón, O, Rosell, R, Fernández-Sirera, L, Allepuz, A and Lavín, S (2011). Retrospective study of pestivirus infection in Pyrenean chamois (Rupicapra pyrenaica) and other ungulates in the Pyrenees (NE Spain). Veterinary Microbiology 149: 1722.CrossRefGoogle ScholarPubMed
Martin, C, Duquesne, V, Guibert, JM, Pulido, C, Gilot-Fromont, E, Gibert, P, Velarde, R, Thiéry, R, Marco, I and Dubois, E (2013). Experimental infection of pregnant Pyrenean chamois (Rupicapra pyrenaica) with border disease virus subtype 4. Journal of Wildlife Diseases 49: 5568.CrossRefGoogle ScholarPubMed
Nettleton, PF and Entrican, G (1995). Ruminant pestiviruses. British Veterinary Journal 151: 615642.CrossRefGoogle ScholarPubMed
Nettleton, PF, Gilray, JA, Russo, P and Dlissi, E (1998). Border disease of sheep and goats. Veterinary Research 29: 327340.Google ScholarPubMed
Olde Riekerink, RGM, Dominici, A, Barkema, HW and de Smit, AJ (2005). Seroprevalence of pestivirus in four species of alpine wild ungulates in the High Valley of Susa, Italy. Veterinary Microbiology 108: 297303.CrossRefGoogle ScholarPubMed
Pence, DB and Ueckermann, E (2002). Sarcoptic mange in wildlife. Revue Scientifique et Technique de l'Office International des Épizooties 21, 385398.Google Scholar
Pioz, M, Loison, A, Gibert, P, Dubray, D, Menaut, P, Le, Tallec, Artois, M and Gilot-Fromont, E (2007). Transmission of a pestivirus infection in a population of Pyrenean chamois. Veterinary Microbiology 119: 1930.CrossRefGoogle Scholar
Plowright, RK, Sokolow, SH, Gorman, ME, Daszak, P and Foley, JE (2008). Causal inference in disease ecology: investigating ecological drivers of disease emergence. Frontiers in Ecology and the Environment 6: 420429.CrossRefGoogle Scholar
Rosell, R, Cabezón, O, Mentaberre, G, Casas, E, Lavín, S and Marco, I (2008). Serum antibodies directed against pestivirus in wild boar (Sus scrofa) in Catalonia (NE Spain). In: 7th International Pestivirus Symposium of the European Society of Veterinary Virology (ESVV), Uppsala (Sweden).Google Scholar
Simmonds, P, Becher, P, Collet, MS, Gould, EA, Heinz, FX, Meyers, G, Monath, T, Pletnev, A, Rice, CM, Stiansny, K, Thiel, H-J, Weiner, A and Bukhet, J (2011). Family flaviviridae. In: King, AMQ, Adams, MJ, Carstens, EB and Lefkowitz, EJ (eds) Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. 9th edn.San Diego: Elsevier Academic Press, pp. 10031020.Google Scholar
Van Campen, H, Frölich, K and Hofmann, M (2001). Pestivirus infections. In: Williams, ES and Baker, IK (eds). Infectious Diseases of Wild Mammals. 3rd edn.Ames, Iowa: Iowa State University Press, pp. 232236.CrossRefGoogle Scholar
Vilcek, S and Nettleton, PF (2006). Pestiviruses in wild animals. Veterinary Microbiology 116: 112.CrossRefGoogle ScholarPubMed
Vilcek, S, Willoughby, K, Nettleton, P and Becher, P (2010). Complete genomic sequence of a border disease virus isolated from Pyrenean chamois. Virus Research 152: 164168.CrossRefGoogle ScholarPubMed