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Ixodid ticks parasitizing wild carnivores in Romania

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Abstract

In Romania, data regarding hard-tick diversity and tick–host associations in wild carnivores are scarce. We aimed to identify tick species in wild carnivores and to establish reliable data on tick–host associations. The study was conducted in various Romanian localities from all five ecoregions found in the country. Fourteen species of wild carnivores were examined. Immature and adult ticks were collected and identified using the morphological keys. The frequency and mean intensity of tick infestation, overall and differentiated by species, developmental stage and host were calculated. Of 202 wild carnivores, 68 were parasitized by seven tick species (predominantly Ixodes ricinus, I. hexagonus and Dermacentor reticulatus). The mean intensity of tick infestation was similar in males (6.97, BCa 95% CI 5.15–9.88) and females (5.76, BCa 95% CI 4.15–9.17). The highest prevalence of infested animals was recorded in the pannonian and steppic ecoregions, 66.7 and 52.7%, respectively. In the continental ecoregion the prevalence was 26.7%, whereas in the pontic ecoregion it was 28%. The lowest value, 16.7% was recorded in the alpine ecoregion. In total 430 ticks were collected, and 24.8% (n = 50) of the animals were infested with more than one tick species. Fourteen new tick–host associations were recorded. Our results suggest that anthropogenic changes of the environment lead to the diminishing of the boundaries, between wild and domestic animals, increasing the exposure for both animals and humans, to infective agents, including tick-borne pathogens.

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References

  • Anderson JF (1990) Epizootiology of Lyme borreliosis. Scand J Infect Dis S77:23–34

    Google Scholar 

  • Anderson JF, Magnarelli LA (1993) Epizootiology of Lyme disease-causing borreliae. Clin Dermatol 11:339–351

    Article  CAS  PubMed  Google Scholar 

  • Anderson K, Ezenwa VO, Jolles AE (2013) Tick infestation patterns in free ranging African buffalo (Syncercus caffer): effects of host innate immunity and niche segregation among tick species. Int J Parasitol Parasites Wildl 2:1–9

    Article  PubMed  Google Scholar 

  • Arnold J, Humer A, Heltai M, Murariu D, Spassov N, Hacklaender K (2012) Current status and distribution of golden jackals Canis aureus in Europe. Mammal Rev 42:1–11

    Article  Google Scholar 

  • Bengis RG, Leighton FA, Fischer JR, Artois M, Mörner T, Tate CM (2004) The role of wildlife in emerging and re-emerging zoonoses. Rev Sci Tech 23:497–511

    CAS  PubMed  Google Scholar 

  • Bermύdez CSE, Esser HJ, Miranda R, Moreno RS (2015) Wild carnivores (Mammalia) as hosts for ticks (Ixodida) in Panama. Syst Appl Acarol 20:13–19

    Article  Google Scholar 

  • Boitani L (2000) Action Plan for the conservation of the wolves (Canis lupus) in Europe. In Convention on the Conservation of European Wildlife and Natural Habitats (Bern Convention). Nature and Environment, No.113.Council of Europe Publishing, Strasbourg, France, pp 76-88

  • Christian A (2012) Tick infestation (Ixodes) on the Eurasian Otter (Lutra lutra) – a long-term study. Soil Org 84:481–487

    Google Scholar 

  • Coipan EC, Vladimirescu AF, Ciolpan O, Teodorescu I (2011) Tick species (Acari: Ixodoidea) distribution, seasonality and host associations in Romania. Trav Mus Natl Hist Nat Grigore Antipa LIV 2:301–317

    Google Scholar 

  • de la Fuente J, Estrada-Peña A, Venzal JM, Tocan KM, Sonenshine DE (2008) Overview: ticks as vectors of pathogens that cause disease in humans and animals. Front Biosci 13:6938–6946

    Article  PubMed  Google Scholar 

  • Dumitrache MO, Gherman CM, Cozma V, Mircean V, Györke A, Sándor AD, Mihalca AD (2012) Hard ticks (Ixodidae) in Romania: surveillance, host associations, and possible risks for tick-borne diseases. Parasitol Res 110:2067–2070

    Article  CAS  PubMed  Google Scholar 

  • Dumitrache MO, Kiss B, Dantas-Torres F, Latrofa MS, D’Amico G, Sándor AD, Mihalca AD (2014) Seasonal dynamics of Rhipicephalus rossicus attacking domestic dogs from the steppic region of southeastern Romania. Parasit Vectors 7:97

    Article  PubMed  PubMed Central  Google Scholar 

  • Duscher GG, Kübber-Heiss A, Richter B, Suchentrunk F (2013) A golden jackal (Canis aureus) from Austria bearing Hepatozoon canis–import due to immigration into a non-endemic area? Ticks Tick Borne Dis 4:133–137

    Article  PubMed  Google Scholar 

  • Duscher GG, Fuehrer HP, Kübber-Heiss A (2014) Fox on the run–molecular surveillance of fox blood and tissue for the occurrence of tick-borne pathogens in Austria. Parasit Vectors 7:521

    PubMed  PubMed Central  Google Scholar 

  • Dziemian S, Michalik J, Piłacińska B, Bialik S, Sikora B, Zwolak R (2014) Infestation of urban populations of the Northern white-breasted hedgehog, Erinaceus roumanicus, by Ixodes spp. ticks in Poland. Med Vet Entomol 28:465–469

    Article  CAS  PubMed  Google Scholar 

  • Estrada-Peña A, de la Fuente J (2016) Species interactions in occurrence data for a community of tick-transmitted pathogens. Sci Data 3:1–13

    Article  Google Scholar 

  • Farkas R, Solymosi N, Takács N, Hornyák Á, Hornok S, Nachum-Biala Y, Baneth G (2014) First molecular evidence of Hepatozoon canis infection in red foxes and golden jackals from Hungary. Parasit Vectors 7:303

    Article  PubMed  PubMed Central  Google Scholar 

  • Feider Z (1965) Fauna of the Popular Republic of Romania. Volume 5/2. Acaromorpha, Suprafamily Ixodoidea. Academia Republicii Populare Române, Bucureşti

  • Filippova NA (1977) Arachnida class: ixodid ticks of the subfamily Ixodinae. In Paukoobraznye Fauna SSSR, vol. 4. Nov. Ser. Nauka, Leningrad

  • Földvári G, Široký P, Szekeres S, Majoros G, Sprong H (2016) Dermacentor reticulatus: a vector on the rise. Parasit Vectors 9:314

    Article  PubMed  PubMed Central  Google Scholar 

  • Gern L, Sell K (2009) Isolation of Borrelia burgdorferi sensu lato from the skin of the European badger (Meles meles) in Switzerland. Vector Borne Zoonotic Dis 9:207–208

    Article  PubMed  Google Scholar 

  • Gern L, Toutoungi LN, Hu CM, Aeschlimann A (1991) Ixodes (Pholeoixodes) hexagonus, an efficient vector of Borrelia burgdorferi in the laboratory. Med Vet Entomol 5:431–435

    Article  CAS  PubMed  Google Scholar 

  • Gese EM (2001) Monitoring of terrestrial carnivore populations. In Gittleman JL, Funk SM, MacDonald DW, Wayne RK (eds) Carnivore Conservation, Cambridge University Press & The Zoological Society of London, 2001 pp 372–396

  • Gherman CM, Sándor AD, Kalmár Z, Marinov M, Mihalca AD (2012) First report of Borrelia burgdorferi sensu lato in two threatened carnivores: the Marbled polecat, Vormela peregusna and the European mink, Mustela lutreola (Mammalia: Mustelidae). BMC Vet Res 8:137

    Article  PubMed  PubMed Central  Google Scholar 

  • Gray J, Dantas-Torres F, Estrada-Peña A, Levin M (2013) Systematics and ecology of the brown dog tick, Rhipicephalus sanguineus. Ticks Tick Borne Dis 4:171–180

    Article  PubMed  Google Scholar 

  • Hornok S, Fuente J, Horváth G, Fernández de Mera I, Wijnveld M, Tánczos B, Farkas R, Jongejan F (2012) Molecular evidence of Ehrlichia canis and Rickettsia massiliae in ixodid ticks of carnivores from South Hungary. Acta Vet Hung 61:42–50

    Article  Google Scholar 

  • Jaenson TG, TäLleklint L, Lundqvist L, Olsen B, Chirico J, Mejlon H (1994) Geographical distribution, host associations, and vector roles of ticks (Acari: Ixodidae, Argasidae) in Sweden. J Med Entomol 31:240–256

    Article  CAS  PubMed  Google Scholar 

  • Jongejan F, Uilenberg G (2004) The Global Importance of Ticks. Parasitol 129:S3–S14

    Google Scholar 

  • Labruna MB, Jorge RS, Sana DA, Jácomo ATA, Kashivakura CK, Furtado MM, Ferro C, Perez SA, Silveira L, Santos JRTS, Marques SR, Morato RG, Nava A, Adania CH, Teixeira RHF, Gomes AAB, Conforti VA, Azevedo FCC, Prada CS, Silva JCR, Batista AF, Marvulo MFV, Morato RLG, Alho CJR, Pinter A, Ferreira PM, Ferreira F, Marques SR (2005) Ticks (Acari: Ixodida) on wild carnivores in Brazil. Exp Appl Acarol 36:149–163

    Article  PubMed  Google Scholar 

  • Lorusso V, Lia RP, Dantas-Torres F, Mallia E, Ravagnan S, Capelli G, Otranto D (2011) Ixodid ticks of road-killed wildlife species in southern Italy: new tick–host associations and locality records. Exp Appl Acarol 55:293–300

    Article  PubMed  Google Scholar 

  • Matuschka FR, Fischer P, Musgrave K, Richter D, Spielman A (1991) Hosts on which nymphal Ixodes ricinus most abundantly feed. Am J Trop Med Hyg 44:100–107

    CAS  PubMed  Google Scholar 

  • Mertens A, Promberger C (2001) Economic aspects of large carnivore-livestock conflicts in Romania. Ursus 173-180

  • Mihalca AD, Dumitrache MO, Magdaş C, Gherman CM, Domşa C, Mircean V, Ghira IV, Pocora V, Ionescu DT, Sikó Barabási S, Cozma V, Sándor AD (2012) Synopsis of the hard ticks (Acari: Ixodidae) of Romania with update on host associations and geographical distribution. Exp Appl Acarol 58:183–206

    Article  CAS  PubMed  Google Scholar 

  • Murariu D (2010) Systematic list of the Romanian vertebrate fauna. Trav Mus Natl Hist Nat Grigore Antipa 53:377–411

    Google Scholar 

  • Nosek J (1971) The ecology, bionomics, and behaviour of Haemaphysalis (Aboimisalis) punctata tick in central Europe. Z Parasitenkd 37:198–210

    Article  CAS  PubMed  Google Scholar 

  • Otranto D, Cantacessi C, Dantas-Torres F, Brianti E, Pfeffer M, Genchi C, Guberti V, Capelli G, Deplazes P (2015a) The role of wild canids and felids in spreading parasites to dogs and cats in Europe. Part II: Helminths and arthropods. Vet Parasitol 213:24–37

    Article  PubMed  Google Scholar 

  • Otranto D, Cantacessi C, Pfeffer M, Dantas-Torres F, Brianti E, Deplazes P, Genchi C, Guberti V, Capelli G (2015b) The role of wild canids and felids in spreading parasites to dogs and cats in Europe. Part I: Protozoa and tick-borne agents. Vet Parasitol 213:12–23

    Article  PubMed  Google Scholar 

  • Pagacz S (2016) The effect of a major drainage divide on the gene flow of a semiaquatic carnivore, the Eurasian otter. J Mammal. doi:10.1093/jmammal/gyw066

    Google Scholar 

  • Petrişor AI, Ianoş I, Tălângă C (2010) Land cover and use changes focused on the urbanization processes in Romania. Environ Eng Manag J 9:765–771

    Google Scholar 

  • Randi E (2011) Genetics and conservation of wolves Canis lupus in Europe. Mammal Rev 41:99–111

    Article  Google Scholar 

  • Reiczigel J, Rozsa L, Reiczigel A, Fabian I (2013) Quantitative Parasitology (QPweb), http://www2.univet.hu/qpweb. Accessed 6 August 2016

  • Ryser-Degiorgis MP, Hofmann-Lehmann R, Leutenegger CM, Segerstad CHA, Mörner T, Mattsson R, Lutz H (2005) Epizootiologic investigations of selected infectious disease agents in free-ranging Eurasian lynx from Sweden. J Wildl Dis 41:58–66

    Article  PubMed  Google Scholar 

  • Sándor AD, Dumitrache MO, D’amico G, Kiss BJ, Mihalca AD (2014) Rhipicephalus rossicus and not R. sanguineus is the dominant tick species of dogs in the wetlands of the Danube Delta. Romania. Vet Parasitol 204:430–432

    Article  PubMed  Google Scholar 

  • Sherrard-Smith E, Chadwick E, Cable J (2012) Abiotic and biotic factors associated with tick population dynamics on a mammalian host: Ixodes hexagonus infesting otters. Lutra lutra. PLoS One 7:e47131

    Article  CAS  PubMed  Google Scholar 

  • Sobrino R, Millán J, Oleaga Á, Gortázar C, de la Fuente J, Ruiz-Fons F (2012) Ecological preferences of exophilic and endophilic ticks (Acari: Ixodidae) parasitizing wild carnivores in the Iberian Peninsula. Vet Parasitol 184:248–257

    Article  PubMed  Google Scholar 

  • Stefan S, Ghioca M, Rimbu N, Boroneant C (2004) Study of meteorological and hydrological drought in southern Romania from observational data. Int J Climatol 24:871–881

    Article  Google Scholar 

  • Walker JB, Keirans JE, Horak IG (2005) The genus Rhipicephalus (Acari, Ixodidae): a guide to the brown ticks of the world. Cambridge University Press

  • Yamaguchi N, Kitchener A, Driscoll C, Nussberger B (2015) Felis silvestris. The IUCN Red List of Threatened Species 2015: e.T60354712A50652361: http://dx.doi.org/10.2305/IUCN.UK.2015-2.RLTS.T60354712A50652361.en. Accessed 18 August 2016

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Acknowledgements

GD, MOD, IAM, AMI, CMG, ADS, DM, ADM are members of the COST Action TD1303. This study was supported by the CNCS-UEFISCDI Grant Agency Romania, grant number TE 36/2015 for ADS and AMI. DM is a member of the COST Action CZ LD14048 we would like to thank Cristi Domşa for the map in Fig. 1.

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    Authors and Affiliations

    1. Department of Parasitology and Parasitic Diseases, University of Agricultural Sciences and Veterinary Medicine, Cluj-Napoca, Calea Mănăştur 3-5, 400372, Cluj-Napoca, Romania

      Gianluca D’Amico, Mirabela Oana Dumitrache, Ioana Adriana Matei, Angela Monica Ionică, Călin Mircea Gherman, Attila David Sándor & Andrei Daniel Mihalca

    2. Department of Pathology and Parasitology, University of Veterinary and Pharmaceutical Sciences, Palackého tř. 1/3, 612 42, Brno, Czech Republic

      David Modrý

    3. CEITEC–VFU, University of Veterinary and Pharmaceutical Sciences, Palackého tř. 1/3, 612 42, Brno, Czech Republic

      David Modrý

    4. Institute of Parasitology, Biology Centre of Academy of Sciences of the Czech Republic, v.v.i., České Budějovice, Czech Republic

      David Modrý

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    1. Gianluca D’Amico
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    2. Mirabela Oana Dumitrache
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    Correspondence to Ioana Adriana Matei.

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    G. D’Amico and M. O. Dumitrache have equally contributed to this work.

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    D’Amico, G., Dumitrache, M.O., Matei, I.A. et al. Ixodid ticks parasitizing wild carnivores in Romania. Exp Appl Acarol 71, 139–149 (2017). https://doi.org/10.1007/s10493-017-0108-z

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