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Patterns of Exposure of Iberian Wolves (Canis lupus) to Canine Viruses in Human-Dominated Landscapes

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Abstract

Wildlife inhabiting human-dominated landscapes is at risk of pathogen spill-over from domestic species. With the aim of gaining knowledge in the dynamics of viral infections in Iberian wolves (Canis lupus) living in anthropized landscapes of northern Spain, we analysed between 2010 and 2013 the samples of 54 wolves by serology and polymerase chain reaction (PCR) for exposure to four pathogenic canine viruses: canine distemper virus (CDV), canine parvovirus-2 (CPV), canine adenovirus 1 and 2 (CAV-1 and CAV-2) and canine herpesvirus. Overall, 76% of the studied wolves presented evidence of exposure to CPV (96% by HI, 66% by PCR) and 75% to CAV (75% by virus neutralization (VN), 76% by PCR, of which 70% CAV-1 and 6% CAV-2). This represents the first detection of CAV-2 infection in a wild carnivore. CPV/CAV-1 co-infection occurred in 51% of the wolves. The probability of wolf exposure to CPV was positively and significantly correlated with farm density in a buffer zone around the place where the wolf was found, indicating that rural dogs might be the origin of CPV infecting wolves. CPV and CAV-1 appear to be enzootic in the Iberian wolf population, which is supported by the absence of seasonal and inter-annual variations in the proportion of positive samples detected. However, while CPV may depend on periodical introductions by dogs, CAV-1 may be maintained within the wolf population. All wolves were negative for exposure to CDV (by VN and PCR) and CHV (by PCR). The absence of acquired immunity against CDV in this population may predispose it to an elevated rate of mortality in the event of a distemper spill-over via dogs.

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References

  • Ahmadi M, López-Bao JV, Kaboli M (2014) Spatial heterogeneity in human activities favors persistence of wolves in agroecosystems. PLoS One 9: e108080.

    Article  PubMed  PubMed Central  Google Scholar 

  • Åkerstedt J, Lillehaug A, Larsen IL, Eide NE, Arnemo JM, Handeland K (2010) serosurvey for canine distemper virus, canine adenovirus, Leptospira interrogans, and Toxoplasma gondii in free-ranging canids in Scandinavia and Svalbard. Journal of Wildlife Diseases 46:474-480

    Article  PubMed  Google Scholar 

  • Allison AB, Kohler DJ, Ortega A, Hoover EA, Grove DM, Holmes EC, Parrish CR (2014) Host-specific parvovirus evolution in nature is recapitulated by in vitro adaptation to different carnivore species. PLoS Pathog 10:e1004475

    Article  PubMed  PubMed Central  Google Scholar 

  • Almberg ES, Mech LD, Smith DW, Sheldon JW, Crabtree RL (2009) A serological survey of infectious disease in Yellowstone National Park’s canid community. PLoS One. 4:e7042.

    Article  PubMed  PubMed Central  Google Scholar 

  • Barton, K. (2013) MuMIn: multi-model inference. R package version 1.9. 5.

    Google Scholar 

  • 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. J Gen Virol 82:1555-1560.

    Article  CAS  PubMed  Google Scholar 

  • Berger L, Speare R, Daszak P, Green DE, Cunningham AA, Goggin CL, Slocombe R, Ragan MA, Hyatt AD, McDonald KR, Hines HB, Lips KR, Marantelli G, Parkes H (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. P Natl Acad Sci U S A 95:9031–9036

    Article  CAS  Google Scholar 

  • Blanco JC, Cortés Y (2007) Dispersal patterns, social structure and mortality of wolves living in agricultural habitats in Spain. Journal of Zoology 273 :114–124.

    Article  Google Scholar 

  • Blanco JC, Cortés Y (2012) Surveying wolves without snow: a critical review of the methods used in Spain. Hystrix 23 :35–48.

    Google Scholar 

  • Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski-Zier BM, Buckles EL, Coleman JT, Darling SR, Gargas A, Niver R, Okoniewski JC, Rudd RJ, Stone WB (2009). Bat white-nose syndrome: an emerging fungal pathogen? Science 323:227

    Article  CAS  PubMed  Google Scholar 

  • Bolker BM (2012) bbmle: tools for general maximum likelihood estimation. http://CRAN.R-project.org/package=bbmle

  • Buonavoglia C, Martella V, Pratelli A, Tempesta M, Cavalli A, Buonavoglia D, Bozzo G, Elia G, Decaro N, Carmichael L (2001) Evidence for evolution of canine parvovirus type 2 in Italy. J Gen Virol 82:3021-3025.

    Article  CAS  PubMed  Google Scholar 

  • Burnham KP, Anderson D (2010) Model Selection and Multi-model Inference: A Practical Information-Theoretic Approach. Springer Verlag, New York, 514 pp.

    Google Scholar 

  • Carmichael LE, Joubert JC, Pollock RVH (1980) Hemagglutination by Canine Parvovirus-2-2: Serologic Studies and Diagnostic Applications. American Journal of Veterinary Research 41:784-791.

    CAS  PubMed  Google Scholar 

  • Chapron G, Kaczensky P, Linnell JDC, von Arx M, Huber D, Andrén H, López-Bao JV, Adamec M, Álvares F, Anders O, Balciauskas L, Balys V, Bedo P, Bego F, Blanco JC, Breitenmoser U, Brøseth H, Bufka L, Bunikyte R, Ciucci P, Dutsov A, Engleder T, Fuxjäger C, Groff C, Heltai M, Holmala K, Hoxha B, Iliopoulos Y, Ionescu O, Ivanov G, Jeremić J, Jerina K, Knauer F, Kojola I, Kos I, Krofel M, Kubala J, Kunovac S, Kusak J, Kutal M, Mannil P, Manz R, Marboutin E, Marucco F, Melovski D, Mersini K, Mertzanis Y, Mysłajek RW, Nowak S, Odden J, Ozolins J, Palomero G, Paunovic M, Persson J, Potočnik H, Quenette P, Rauer G, Reinhardt I, Rigg R, Ryser A, Salvatori V, Skrbinšek T, Skrbinšek-Majić A, Stojanov A, Swenson JE, Trajçe A, Tzingarska-Sedefcheva E, tin Váňa M, Veeroja R, Wölfl M, Wölfl S, Zimmermann F, Zlatanova D, Boitani L (2014) Recovery of large carnivores in Europe’s modern human-dominated landscapes. Science 346: 1517-1519.

    Article  CAS  PubMed  Google Scholar 

  • Cuesta L, Barcena F, Palacios F, Reig S (1991) The trophic ecology of the Iberian wolf (Canis lupus signatus Cabrera, 1907). A new analysis of stomach’s data. Mammalia 55:239–254.

    Article  Google Scholar 

  • Decaro N, Elia G, Martella V, Desario C, Campolo M, Trani LD, Tarsitano E, Tempesta M, 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 105:19-28.

    Article  CAS  PubMed  Google Scholar 

  • Decaro N, Martella V, Desario C, Bellacicco AL, Camero M, Manna L, d’Aloja D, Buonavoglia C (2006) First detection of canine parvovirus type 2c in pups with haemorrhagic enteritis in Spain. J Vet Med B Infect Dis Vet Public Health. 53:468-472.

    Article  CAS  Google Scholar 

  • Decaro N, Buonavoglia C, Eatwell K, Erdelyi K, Duff JP (2012) Adenovirus infections. In: Gavier-Widén D, Duff JP, Meredith A (eds) Infectious diseases of wild mammals and birds in Europe. Oxford: Blackwell Publishing Ltd, pp 210–211

    Chapter  Google Scholar 

  • Dellinger JA, Proctor C, Steury TD, Kelly MJ, Vaughan MR (2013). Habitat selection of a large carnivore, the red wolf, in a human-altered landscape. Biological Conservation 157:324-330.

    Article  Google Scholar 

  • Di Sabatino D, Lorusso A, Di Francesco CE, Gentile L, Di Pirro V, Bellacicco AL, Giovannini A, Di Francesco G, Marruchella G, Marsilio F, Savini G (2014) Arctic Lineage-Canine Distemper Virus as a Cause of Death in Apennine Wolves (Canis lupus) in Italy. PLoS One. 20:e82356.

    Article  Google Scholar 

  • Eggermann, J., da Costa, G. F., Guerra, A. M., Kirchner, W. H., & Petrucci-Fonseca, F. (2011). Presence of Iberian wolf (Canis lupus signatus) in relation to land cover, livestock and human influence in Portugal. Mammalian Biology-Zeitschrift für Säugetierkunde, 76(2), 217-221.

    Article  Google Scholar 

  • Elia G, Decaro N, Martella V, Cirone F, Lucente MS, Lorusso E, Di Trani L, Buonavoglia C (2006) Detection of canine distemper virus in dogs by real-time RT-PCR. J Virol Methods 136:171-176

    Article  CAS  PubMed  Google Scholar 

  • García E, Llaneza L, Palacios V, López-Bao JV, Sazatornil V, Rodríguez A, Rivas O, Cabana M (2012) Primeros datos sobre la ecología espacial del lobo en Galicia. Abstract-Book of the III Iberian Wolf Congress.

  • Gavier-Widen D, Meredith A, Duff JP (2012) Infectious diseases of wild mammals and birds in Europe. Hoboken, NJ: Wiley-Blackwell.

    Google Scholar 

  • Gipson PS, Ballard WB, Nowak RM, Mech LD (2000) Accuracy and precision of estimating age of gray wolves by tooth wear. Journal of Wildlife Management 64:752–758.

    Article  Google Scholar 

  • Godinho R, López‐Bao JV, Castro D, Llaneza L, Lopes S, Silva P, Ferrand N (2015) Real‐time assessment of hybridization between wolves and dogs: combining noninvasive samples with ancestry informative markers. Molecular ecology resources 15:317-328

    Article  CAS  PubMed  Google Scholar 

  • Gompper ME (ed) (2013) Free-ranging dogs and wildlife conservation. Oxford University Press

  • Gonçalves A, Igrejas G, Radhouani H, Estepa V, Pacheco R, Monteiro R, Brito F, Guerra A, Petrucci-Fonseca F, Torres C, Poeta P (2012) Iberian wolf as a reservoir of extended-spectrum β-lactamase-producing Escherichia coli of the TEM, SHV, and CTX-M groups. Microb Drug Resist 18:215-219

    Article  PubMed  Google Scholar 

  • Gordon CH, Banyard AC, Hussein A, Laurenson MK, Malcolm JR, Marino J, Regassa F, Stewart AM, Fooks AR, Sillero-Zubiri C (2015) Canine distemper in endangered ethiopian wolves. Emerg Infect Dis 21:824-832.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gorman ML (1990) Scent marking strategies in mammals. Revue Suisse de Zoologie 97:3-29

    Article  Google Scholar 

  • Greene CE (2012) Infectious diseases of the dog and cat. 4th ed. St Louis, MO: Elsevier Saunders.

    Google Scholar 

  • Hughes J, MacDonald DW (2013) A review of the interactions between free-roaming domestic dogs and wildlife. Biol Conserv 157:341–351

    Article  Google Scholar 

  • INE (2014) Censo de población y vivienda. Instituto Nacional de Estadística de España, Madrid, Spain.

    Google Scholar 

  • Kreeger TJ (2003) The internal wolf: physiology, pathology, and pharmacology. In: Mech LD, Boitani L (eds) Wolves: behavior, ecology and conservation. The University of Chicago Press, Chicago, IL, pp 192–217

    Google Scholar 

  • Kushnir H, Weisberg S, Olson E, Juntunen T, Ikanda D, Packer C (2014) Using landscape characteristics to predict risk of lion attacks on humans in south‐eastern Tanzania. African J Ecol 52:524-532

    Article  Google Scholar 

  • Li Y, Ge X, Zhang H, Zhou P, Zhu Y, Zhang Y, Yuan J, Wang LF, Shi Z (2010) Host range, prevalence, and genetic diversity of adenoviruses in bats. J Virol 84:3889-3897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liberg O, Chapron G, Wabakken P, Pedersen HC, Hobbs NT, Sand H (2012) Shoot, shovel and shut up: cryptic poaching slows restoration of a large carnivore in Europe. Proceedings of the Royal Society of London B: Biological Sciences 279 : 910-915

    Article  Google Scholar 

  • Llaneza L, López-Bao JV & Sazatornil V (2012) Insights into wolf presence in highly human-dominated landscapes: The relative role of food availability, human activity and landscape attributes. Diversity and Distributions 18:459-469.

    Article  Google Scholar 

  • Llaneza L, García EJ, López-Bao JV (2014) Intensity of territorial marking predicts wolf reproduction: Implications for wolf monitoring. PloS one 9:e93015.

    Article  PubMed  PubMed Central  Google Scholar 

  • López-Bao JV, Sazatornil V, Llaneza L, Rodríguez A (2013) Indirect effects on heathland conservation and wolf persistence of contradictory policies that threaten traditional free-ranging horse husbandry. Conservation letters 6:448-455.

    Article  Google Scholar 

  • Mech LD, Goyal SM, Paul WJ, Newton WE (2008) Demographic effects of canine parvovirus on a free-ranging wolf population over 30 years. Journal of Wildlife Diseases 44:824-836.

    Article  PubMed  Google Scholar 

  • Mech LD, Goyal SM (1993) Canine parvovirus effect on wolf population change and pup survival. Journal of Wildlife Diseases 29 :330-333.

    Article  CAS  PubMed  Google Scholar 

  • Mech LD, Boitani L (2003) Wolves: behavior, ecology and conservation. University of Chicago Press, Chicago.

    Book  Google Scholar 

  • Millán J, Candela MG, Palomares F, Cubero MJ, Rodríguez A, Barral M, de la Fuente J, Almería S, León-Vizcaíno L (2009) Disease threats to the endangered Iberian lynx (Lynx pardinus). Veterinary Journal 182:114–124.

    Article  Google Scholar 

  • Millán J, Chirife AD, Kalema-Zikusoka G, Cabezón O, Muro J, Marco I, Cliquet F, León-Vizcaíno L, Wasniewski M, Almería S (2013) Serosurvey of dogs for human, livestock, and wildlife pathogens, Uganda. Emerg. Infect. Dis. 19:680–682.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mörner T, Eriksson H, Bröjer C, Nilsson K, Uhlhorn H, Ågren E, Gavier-Widén D (2005) Diseases and mortality in free-ranging brown bear (Ursus arctos), gray wolf (Canis lupus), and wolverine (Gulo gulo) in Sweden. Journal of Wildlife Diseases 41 :298-303.

    Article  PubMed  Google Scholar 

  • Müller A, Silva E, Santos N, Thompson G (2011) Domestic dog origin of canine distemper virus in free-ranging wolves in Portugal as revealed by hemagglutinin gene characterization. Journal of Wildlife Diseases 47:725-729.

    Article  PubMed  Google Scholar 

  • Nelson B, Hebblewhite M, Ezenwa V, Shury T, Merrill EH, Paquet PC, Schmiegelow F, Seip D, Skinner G, Webb N (2012) Prevalence of antibodies to canine parvovirus and distemper virus in wolves in the Canadian Rocky Mountains. Journal of Wildlife Diseases 48:68-76.

    Article  PubMed  Google Scholar 

  • Oleaga A, Vicente J, Ferroglio E, Pegoraro de Macedo MR, Casais R, del Cerro A, Espí A, García EJ, Gortázar C (2015) Concomitance and interactions of pathogens in the Iberian wolf (Canis lupus). Research in Veterinary Science 101:22–27

    Article  CAS  PubMed  Google Scholar 

  • Origgi FC, Plattet P, Sattler U, Robert N, Casaubon J, Mavrot F, Pewsner M, Wu N, Giovannini S, Oevermann A, Stoffel MH, Gaschen V, Segner H, Ryser-Degiorgis MP (2012) Emergence of canine distemper virus strains with modified molecular signature and enhanced neuronal tropism leading to high mortality in wild carnivores. Vet Pathol 49:913-929.

    Article  CAS  PubMed  Google Scholar 

  • Pacheco C (2014) Assessing the spatial extent of wolf-dog hybridization at population level through the use of non-invasive DNA. MSc Thesis, University of Porto, Portugal.

  • Paradis E, Claude J, Strimmer K (2012) Package ape. Analyses of phylogenetics and evolution. R package version 2012.04-04. http://www.cran.r-project.org/package=ape/

  • Pedersen AB, Jones KE, Nunn CL, Altizer SA (2007) Infectious disease and mammalian extinction risk. Conserv. Biol. 21:1269–1279.

    Article  PubMed  Google Scholar 

  • Peterson RO, Thomas NJ, Thurber JM, Vucetich JA, Waite TA (1998) Population limitation and the wolves of Isle Royale. Journal of Mammalogy 79:828-841.

    Article  Google Scholar 

  • Philippa JD, Leighton FA, Daoust PY, Nielsen O, Pagliarulo M, Schwantje H, Shury T, Van Herwijnen R, Martina BE, Kuiken T, Van de Bildt MW, Osterhaus AD (2004) Antibodies to selected pathogens in free-ranging terrestrial carnivores and marine mammals in Canada. Vet Rec 155:135-140.

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2013) R: A Language and Environment for Statistical Computing. Version 3.1. 1 [computer program]. R Foundation for Statistical Computing, Vienna, Austria.

  • Rigg R, Fino S, Wechselberger M, Gorman ML, Sillero-Zubiri C, Macdonald DW (2011). Mitigating carnivore–livestock conflict in Europe: lessons from Slovakia. Oryx, 45: 272-280

    Article  Google Scholar 

  • Riley SP, Foley J, Chomel B (2004) Exposure to feline and canine pathogens in bobcats and grey foxes in urban and rural zones of a national park in California. Journal of Wildlife Diseases 40:11–22

    Article  PubMed  Google Scholar 

  • Roelke-Parker ME, Munson L, Packer C, Kock R, Cleaveland S, Carpenter M, O’Brien SJ, Pospischil A, Hofmann-Lehmann R, Lutz H, Mwamengele GLM, Mgasa MN, Machange GA, Summers BA, Appel MJG (1996) A canine distemper virus epidemic in Serengeti lions (Panthera leo). Nature 379:441–445.

    Article  CAS  PubMed  Google Scholar 

  • Santos N, Almendra C, Tavares L (2009) Serologic survey for canine distemper virus and canine parvovirus in free-ranging wild carnivores from Portugal. Journal of Wildlife Diseases 45:221-226.

    Article  PubMed  Google Scholar 

  • Scott ME (1988) The impact of infectious disease on animal populations, implications for conservation biology. Conservation Biology 2:40–65.

    Article  Google Scholar 

  • Sobrino R, Arnal MC, Luco DF, Gortázar C (2008) Prevalence of antibodies against canine distemper virus and canine parvovirus among foxes and wolves from Spain. Vet Microbiol 126:251-256.

    Article  CAS  PubMed  Google Scholar 

  • Thorne ET, Williams ES (1988) Disease and endangered species, the black-footed ferret as a recent example. Conservation Biology 2:66–74.

    Article  Google Scholar 

  • Vanak AT, Gompper ME (2009) Dogs Canis familiaris as carnivores: their role and function in intraguild competition. Mammal Review 39 :265 – 283

    Article  Google Scholar 

  • VanDevanter DR, Warrener P, Bennett L, Schultz ER, Coulter S, Garber RL, Rose TM (1996) Detection and analysis of diverse herpesviral species by consensus primer PCR. J Clin Microbiol 34:1666-1671

    CAS  PubMed  PubMed Central  Google Scholar 

  • Van Houtan KS, Hargrove SK, Balazs GH (2010) Land use, macroalgae, and a tumor-forming disease in marine turtles. PLoS One 5:e12900.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wobeser GA (1994) Samples, sampling and sample collection. In: Investigation and Management of Diseases in Wild Animals. New York: Plenum Press, pp 87–102

  • Woodroffe R, Prager KC, Munson L, Conrad PA, Dubovi EJ, Mazet JA (2012) Contact with Domestic Dogs Increases Pathogen Exposure in Endangered African Wild Dogs (Lycaon pictus). PLoS ONE 7: e30099.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zarnke RL, Ver Hoef JM, DeLong RA (2004) Serologic survey for selected disease agents in wolves (Canis lupus) from Alaska and the Yukon Territory, 1984-2000. Journal of Wildlife Diseases 40:632-638.

    Article  PubMed  Google Scholar 

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Acknowledgments

We are in debt to the Xunta de Galicia and to the staff of the Regional Government of Asturias (especially Jaime Marcos Beltrán and Francisco Alonso Mier) for their help with wolf carcasses, and to our colleagues from SERIDA (Alberto Espí) and the Veterinary Faculty of the University of Santiago de Compostela (USC) (Luis Eusebio Fidalgo Álvarez and Ana María López Beceiro) for their assistance in necropsy. Finally, we also thank the technicians from INIA-CISA (Verónica Nogal and Elena Neves) for the laboratory assistance and E. Stapleton for English review. This is a contribution to the agreement between CSIC and Principado de Asturias. JVLB was supported by a ‘Juan de la Cierva’ research contract from the Spanish Ministry of Economy and Competitiveness.

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Millán, J., López-Bao, J.V., García, E.J. et al. Patterns of Exposure of Iberian Wolves (Canis lupus) to Canine Viruses in Human-Dominated Landscapes. EcoHealth 13, 123–134 (2016). https://doi.org/10.1007/s10393-015-1074-8

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