The impact of carnivore parvovirus infection on wild populations is not yet understood; disease signs are mainly developed in pups and assessing the health of litters in wild carnivores has big limitations. This study aims to shed light on the virus dynamics among wild carnivores thanks to the analysis of 213 samples collected between 1994 and 2013 in wild ecosystems from Spain. We determined the presence of carnivore parvovirus DNA by real-time PCR and sequenced the vp2 gen from 22 positive samples to characterize the strains and to perform phylogenetic analysis. The presence of carnivore parvovirus DNA was confirmed in 18% of the samples, with a higher prevalence detected in wolves (Canis lupus signatus, 70%). Fourteen sequences belonging to nine wolves, three Eurasian badgers (Meles meles), a common genet (Genetta genetta) and a European wildcat (Felis silvestris) were classified as canine parvovirus 2c (CPV-2c); five sequences from three wolves, a red fox (Vulpes vulpes) and a stone marten (Martes foina) as CPV-2b; and three sequences from a badger, a genet and a stone marten as feline parvovirus (FPV). This was the first report of a wildcat infected with a canine strain. Sequences described in this study were identical or very close related to others previously found in domestic carnivores from distant countries, suggesting that cross-species transmission takes place and that the parvovirus epidemiology in Spain, as elsewhere, could be influenced by global factors.

A RE NA Asesores en Recursos Naturales SL Lugo Spain

Animal Health Research Centre INIA CISA Madrid Spain

Consorci per a la Recuperació de la Fauna de les Illes Balears Santa Eugènia Spain

Department of Conservation Biology Estación Biológica de Doñana CSIC Sevilla Spain

Department of Zoology and Fisheries Faculty of Agrobiology Food and Natural ResourcesCzech University of Life Sciences Prague Prague Czech Republic

Facultad de Ciencias de la Vida Universidad Andres Bello Santiago Chile

Institute of Zoology Zoological Society of London London UK

SERPA Sociedad de Servicios del Principado de Asturias S A Gijón Spain

The Royal Veterinary College London UK

Wildlife Ecology and Health Group and Servicio de Ecopatología de Fauna Salvaje Departament de Medicina i Cirurgia Animals Universitat Autònoma de Barcelona Barcelona Spain

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Allison, A. B., Kohler, D. J., Fox, K. A., Brown, J. D., Gerhold, R. W., Shearn-Bochsler, V. I., … Holmes, E. C. (2013). Frequent cross-species transmission of parvoviruses among diverse carnivore hosts. Journal of Virology, 87(4), 2342-2347. https://doi.org/10.1128/JVI.02428-12

Allison, A. B., Kohler, D. J., Ortega, A., Hoover, E., Grove, D. M., Holmes, E. C., & Parrish, C. R. (2014). Host-specific parvovirus evolution in nature is recapitulated by in vitro adaptation to different carnivore species. PLoS Path, 10(11), e1004475. https://doi.org/10.1371/journal.ppat.1004475

Barker, I. K., & Parrish, C. R. (2001). Parvovirus Infections, Infectious Diseases of Wild Animals (3rd edn). Iowa, USA: Iowa State University Press.

Battilani, M., Scagliarini, A., Ciulli, S., Morganti, L., & Prosperi, S. (2006). High genetic diversity of the VP2 gene of a canine parvovirus strain detected in a domestic cat. Virology, 352(1), 22-26.

Battilani, M., Scagliarini, A., Tisato, E., Turilli, C., Jacoboni, I., Casadio, R., & Prosperi, S. (2001). Analysis of canine parvovirus sequences from wolves and dogs isolated in Italy. The Journal of General Virology, 82, 1555-1560. https://doi.org/10.1099/0022-1317-82-7-1555

Buonavoglia, C., Martella, V., Pratella, A., Tempesta, M., Cavalli, A., Buonavoglia, D., … Carmichael, L. (2001). Evidence for evolution of canine parvovirus type 2 in Italy. Journal of General Virology, 82(12), 3021-3025. https://doi.org/10.1099/0022-1317-82-12-3021

Calatayud, O., Esperón, F., Cleaveland, S., Biek, R., Keyyu, J., Eblate, E., … Shisler, J. L. (2019). Carnivore parvovirus ecology in the Serengeti ecosystem: Vaccine strains circulating and new host species identified. Journal of Virology, 93(13). https://doi.org/10.1128/JVI.02220-18

Cotmore, S. F., Agbandje-McKenna, M., Chiorini, J. A., Mukha, D. V., Pintel, D. J., Qiu, J., … Davison, A. J. (2014). The family Parvoviridae. Archives of Virology, 159(5), 1239-1247. https://doi.org/10.1007/s00705-013-1914-1

Decaro, N., Desario, C., Addie, D. D., Martella, V., Vieira, M. J., Elia, G., … Buonavoglia, C. (2007). Molecular epidemiology of canine parvovirus, Europe. Emerging Infectious Diseases, 13(8), 12-14. https://doi.org/10.3201/eid1308.070505

Decaro, N., Elia, G., Martella, V., Desario, C., Campolo, M., Trani, L. D., … Buonavoglia, C. (2005). A real-time PCR assay for rapid detection and quantitation of canine parvovirus type 2 in the feces of dogs. Veterinary Microbiology, 105(1), 19-28. https://doi.org/10.1016/j.vetmic.2004.09.018

Decaro, N., Martella, V., Desario, C., Bellacicco, A. L., Camero, M., Manna, L., … Buonavoglia, C. (2006). First detection of canine parvovirus type 2c in pups with haemorrhagic enteritis in Spain. Journal of Veterinary Medicine. B, Infectious Diseases and Veterinary. Public Health, 53(10), 468-472. https://doi.org/10.1111/j.1439-0450.2006.00974.x

Decaro, N., Martella, V., Elia, G., Desario, C., Campolo, M., Lorusso, E., … Buonavoglia, C. (2007). Tissue distribution of the antigenic variants of canine parvovirus type 2 in dogs. Veterinary Microbiology, 121(1-2), 39-44. https://doi.org/10.1016/j.vetmic.2006.11.005

Duarte, M. D., Barros, S. C., Henriques, M., Fernandes, T. L., Bernardino, R., Monteiro, M., & Fevereiro, M. (2009). Fatal infection with feline panleukopenia virus in two captive wild carnivores (Panthera tigris and Panthera leo). Journal of Zoo and Wildlife Medicine, 40(2), 354-359. https://doi.org/10.1638/2008-0015.1

Duarte, M. D., Henriques, A. M., Barros, S. C., Fagulha, T., Mendonça, P., Carvalho, P., … Cunha, M. V. (2013). Snapshot of viral infections in wild carnivores reveals ubiquity of parvovirus and susceptibility of egyptian mongoose to feline panleukopenia virus. PLoS ONE, 8(3), e59399. https://doi.org/10.1371/journal.pone.0059399

Harrison, T. M., Mazet, J. K., Holekamp, K. E., Dubovi, E., Engh, A. L., Nelson, K., … Munson, L. (2004). Antibodies to canine and feline viruses in spotted hyenas (Crocuta Crocuta) in the masai mara national reserve. Journal of Wildlife Diseases, 40(1), 1-10. https://doi.org/10.7589/0090-3558-40.1.1

Huson, D. H., & Bryant, D. (2006). Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23(2), 254-267. https://doi.org/10.1093/molbev/msj030

Ikeda, Y., Nakamura, K., Miyazawa, T., Tohya, Y., Takahashi, E., & Mochizuki, M. (2002). Feline host range of Canine parvovirus: Recent emergence of new antigenic types in cats. Emerging Infectious Diseases, 8(4), 341-346. https://doi.org/10.3201/eid0804.010228

Lapointe, F.-J. (2000). How to account for reticulate events in phylogenetic analysis. Journal of Classification, 17, 175-184. https://doi.org/10.1007/s003570000016

Llaneza, L., García, E. J., & López-Bao, J. V. (2014). Intensity of territorial marking predicts wolf reproduction: Implications for wolf monitoring. PLoS ONE, 9(3), e93015. https://doi.org/10.1371/journal.pone.0093015

Mech, L. D., Goyal, S. M., Paul, W. J., & Newton, W. E. (2008). Demographic effects of canine parvovirus on a free-ranging wolf population over 30 years. Journal of Wildlife Diseases, 44(4), 824-836. https://doi.org/10.7589/0090-3558-44.4.824

Mendenhall, I. H., Low, D., Neves, E. S., Anwar, A., Oh, S., Su, Y. C. F., & Smith, G. J. D. (2016). Evidence of canine parvovirus transmission to a civet cat (Paradoxurus musangus) in Singapore. One Health, 2, 122-125. https://doi.org/10.1016/j.onehlt.2016.07.003

Miranda, C., & Thompson, G. (2016). Canine parvovirus: The worldwide occurrence of antigenic variants. Journal of General Virology, 97(9), 2043-2057. https://doi.org/10.1099/jgv.0.000540

Mochizuki, M., Horiuchi, M., & Hiragi, H. (1996). Isolation of canine parvovirus from a cat manifesting clinical signs of feline. Journal of Clinical Microbiology, 34(9), 2101-2105.

Mochizuki, M., San Gabriel, M. C., Nakatani, H., Yoshida, M., & Harasawa, R. (1993). Comparison of polymerase chain reaction with virus isolation and haemagglutination assays for the detection of canine parvoviruses in faecal specimens. Research in Veterinary Science, 55(1), 60-63. https://doi.org/10.1016/0034-5288(93)90035-E

Nakamura, K., Sakamoto, M., Ikeda, Y., Sato, E., Kawakami, K., Miyazawa, T., … Mochizuki, M. (2001). Pathogenic potential of canine parvovirus types 2a and 2c in domestic cats. Clinical and Vaccine Immunology, 8(3), 663-668. https://doi.org/10.1128/CDLI.8.3.663-668.2001

Ohneiser, S. A., Hills, S. F., Cave, N. J., Passmore, D., & Dunowska, M. (2015). Canine parvoviruses in New Zealand form a monophyletic group distinct from the viruses circulating in other parts of the world. Veterinary Microbiology, 178(3-4), 190-200. https://doi.org/10.1016/j.vetmic.2015.05.017

Palomo, L. J., Gisbert, J., & Blanco, J. C. (2007). Atlas y Libro Rojo de los Mamíferos Terrestres de España (Atlas of Spanish mammals, in english). (Dirección & G. para la Biodiversidad-SECEM-SECEMU, Eds.). Madrid, Spain. Retrieved from http://www.magrama.gob.es/gl/biodiversidad/temas/inventarios-nacionales/inventario-especies-terrestres/inventario-nacional-de-biodiversidad/inb_bbdd.aspx.

Parrish, C. R. (1995). Pathogenesis of feline panleukopenia virus and canine parvovirus. Bailliere’s Clinical Haematology, 8(1), 57-71. https://doi.org/10.1016/S0950-3536(05)80232-X

Parrish, C. R. (1999). Host range relationships and the evolution of canine parvovirus. Veterinary Microbiology, 69(1-2), 29-40. https://doi.org/10.1016/S0378-1135(99)00084-X

Parrish, C. R., Aquadro, C. F., Strassheim, M. L., Evermann, J. F., Sgro, J. Y., & Mohammed, H. O. (1991). Rapid antigenic-type replacement and DNA sequence evolution of canine parvovirus. Journal of Virological Methods, 65(12), 6544.

Pérez, R., Bianchi, P., Calleros, L., Francia, L., Hernández, M., Maya, L., … Zoller, S. (2012). Recent spreading of a divergent canine parvovirus type 2a (CPV-2a) strain in a CPV-2c homogenous population. Veterinary Microbiology, 155(2-4), 214-219.

Reed, A. P., Jones, E. V., & Miller, T. J. (1988). Nucleotide sequence and genome organization of canine parvovirus. Journal of Virology, 62(1), 266-276.

Shackelton, L., Parrish, C. R., Truyen, U., & Holmes, E. C. (2005). High rate of viral evolution associated with the emergence of carnivore parvovirus. Proceedings of the National Academy of Sciences of the United States of America, 102(2), 379-384. https://doi.org/10.1073/pnas.0406765102

Steinel, A., Munson, L., Van Vuuren, M., & Truyen, U. (2000). Genetic characterization of feline parvovirus sequences from various carnivores. Journal of General Virology, 81(2), 345-350. https://doi.org/10.1099/0022-1317-81-2-345

Steinel, A., Parrish, C. R., Bloom, M. E., & Truyen, U. (2001). Parvovirus infections in wild carnivores. Journal of Wildlife Diseases, 37(3), 594-607. https://doi.org/10.7589/0090-3558-37.3.594

Streck, A. F., Rüster, D., Truyen, U., & Homeier, T. (2013). An updated T aqMan real-time PCR for canine and feline parvoviruses. Journal of Virological Methods, 193(1), 6-8.

Tamura, K., Dudley, J., Nei, M., & Kumar, S. (2007). MEGA molecular evolutionary genetics analysis; version 4. Molecular Biology and Evolution, 24, 1596-1599. https://doi.org/10.1093/molbev/msm092

Truyen, U., Evermann, J. F., Vieler, E., & Parrish, C. R.. (1996). Evolution of canine parvovirus involved loss and gain of feline host range. Virology, 215(2), 186-189. https://doi.org/10.1006/viro.1996.0021

Truyen, U., Geissler, K., Parrish, C. R., Hermanns, W., & Siegl, G. (1998). No evidence for a role of modified live virus vaccines in the emergence of canine parvovirus. Journal of General Virology, 79(5), 1153-1158.

Verge, J., & Christoforoni, N. (1928). La gastroenterite infectieuse des chats; est-elle due à un virus filtrable? Comptes Rendus Des Séances De La Société De Biologie Et De Ses Filiales, 99, 312.

Woodroffe, R., Prager, K. C., Munson, L., Conrad, P. A., Dubovi, E. J., Mazet, J. A. K., & Getz, W. M. (2012). Contact with Domestic Dogs Increases Pathogen Exposure in Endangered African Wild Dogs (Lycaon pictus). PLoS ONE, 7(1), e30099.

Zarnke, R. L., Evermann, J., Ver Hoef, J. M., McNay, M. E., Boertje, R. D., Gardner, C. L., … Burch, J. (2001). Serologic survey for canine coronavirus in wolves from Alaska. Journal of Wildlife Diseases, 37(4), 740-745. https://doi.org/10.7589/0090-3558-37.4.740