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Ticks and tick-borne pathogens in wild birds in Greece

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Abstract

Wild birds are common hosts of ticks and can transport them for long distances, contributing to the spreading of tick-borne pathogens. The information about ticks on birds and tick-borne pathogens in Greece is limited. The present study aimed to evaluate the prevalence and species of ticks infesting wild resident birds (mostly small passerines) in Greece, and to assess Borrelia and Rickettsia infection in the collected ticks. Detection of Borrelia burgdorferi s.l. was performed by nested PCR targeting the flaB gene. Rickettsia spp. were detected by PCR targeting the gltA and ompA genes. Seven (2 %) out of 403 birds examined in northern Greece in 2013 were infested with 15 ticks, identified as Ixodes frontalis, Ixodes acuminatus, Hyalomma marginatum, Hyalomma aegyptium and Hyalomma sp. All ticks were negative for Borrelia spp. while four of them were positive for rickettsiae (Rickettsia aeschlimannii in H. aegyptium and Rickettsia sp. in I. frontalis, H. aegyptium and H. marginatum). Ixodes acuminatus is reported for the first time in Greece and Sylvia borin is reported as a new host record for I. acuminatus.

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References

  • Apanaskevich D (2003) Host-parasite relationships of the genus Hyalomma Koch, 1844 (Acari, Ixodidae) and their connection with microevolutionary process. Parazitologiia 38:515–523

    Google Scholar 

  • Baker AS (1999) Mites and ticks of domestic animals. An identification guide and information source. The Natural History Museum, London

    Google Scholar 

  • Baptista S, Quaresma A, Aires T, Kurtenbach K, Santos-Reis M, Nicholson M, Collares-Pereira M (2004) Lyme borreliosis spirochetes in questing ticks from mainland Portugal. Int J Med Microbiol 293:109–116

    PubMed  Google Scholar 

  • Beati L, Meskini M, Thiers B, Raoult D (1997) Rickettsia aeschlimannii sp. nov., a new spotted fever group rickettsia associated with Hyalomma marginatum ticks. Int J Syst Bacteriol 47:548–554

    Article  CAS  PubMed  Google Scholar 

  • De Michelis S, Sewell HS, Collares-Pereira M, Santos-Reis M, Schouls LM, Benes V, Holmes EC, Kurtenbach K (2000) Genetic diversity of Borrelia burgdorferi sensu lato in ticks from mainland Portugal. J Clin Microbiol 38:2128–2133

    PubMed  PubMed Central  Google Scholar 

  • Eisen L, Lane RS (2002) Vectors of Borrelia burgdorferi sensu lato. In: Gray J, Kahl O, Lane RS, Stanek G (eds) Lyme borreliosis: biology epidemiology and control. CAB Publishing, New York, pp 91–115

    Chapter  Google Scholar 

  • Elsheikha HM, Khan NA (2011) Essentials of veterinary parasitology, 1st edn. Caister Academic Press, Norfolk

    Google Scholar 

  • Estrada-Peña A, Oteo JA, Estradapena R, Gortazar C, Osacar JJ, Moreno JA, Castella J (1995) Borrelia burgdorferi sensu lato in ricks (Acari, Ixodidae) from 2 different foci in Spain. Exp Appl Acarol 19:173–180

    Article  PubMed  Google Scholar 

  • Estrada-Peña A, Bouattour A, Camicas JL, Walker AR (2004) Ticks of domestic animals in the Mediterranean Region—a guide to identification of species, 1st edn. University of Zaragoza, Zaragoza

    Google Scholar 

  • Fix M (2006) Tick-borne diseases. In: Antosia RE, Cahill JD (eds) Handbook of bioterrorism and disaster medicine, 1st edn. Springer, New York, pp 299–305

  • Gargili A, Palomar AM, Midilli K, Portillo A, Kar S, Oteo JA (2012) Rickettsia species in ticks removed from humans in Istanbul, Turkey. Vector Borne Zoonotic Dis 12:938–941. doi:10.1089/vbz.2012.0996

    Article  PubMed  PubMed Central  Google Scholar 

  • Germanakis A, Chochlakis D, Angelaki E, Tselentis Y, Psaroulaki A (2013) Rickettsia aeschlimannii infection in a man, Greece. Emerg Infect Dis 19:1176–1177. doi:10.3201/eid1907.130232

    Article  PubMed  PubMed Central  Google Scholar 

  • Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Peña A, Horak I (2014) The hard ticks of the world. Springer, Dordrecht. doi:10.1007/978-94-007-7497-1

    Book  Google Scholar 

  • Guner ES, Watanabe M, Hashimoto N, Kadosaka T, Kawamura Y, Ezaki T, Kawabata H, Imai Y, Kaneda K, Masuzawa T (2004) Borrelia turcica sp. nov., isolated from the hard tick Hyalomma aegyptium in Turkey. Int J Syst Evol Microbiol 54:1649–1652. doi:10.1099/ijs.0.03050-0

    Article  PubMed  Google Scholar 

  • Hagman K, Barboutis C, Ehrenborg C, Fransson T, Jaenson TG, Lindgren PE, Lundkvist A, Nystrom F, Waldenstrom J, Salaneck E (2014) On the potential roles of ticks and migrating birds in the ecology of West Nile virus. Infect Ecol Epidemiol 4:20943. doi:10.3402/iee.v4.20943

    Google Scholar 

  • Hasle G (2013) Transport of ixodid ticks and tick-borne pathogens by migratory birds. Front Cell Infect Microbiol 3:48. doi:10.3389/fcimb.2013.00048

    Article  PubMed  PubMed Central  Google Scholar 

  • Hasle G, Bjune G, Edvardsen E, Jakobsen C, Linnehol B, Roer JE, Mehl R, Roed KH, Pedersen J, Leinaas HP (2009) Transport of ticks by migratory passerine birds to Norway. J Parasitol 95:1342–1351. doi:10.1645/GE-2146.1

    Article  PubMed  Google Scholar 

  • Heylen D, Tijsse E, Fonville M, Matthysen E, Sprong H (2013) Transmission dynamics of Borrelia burgdorferi s.l. in a bird tick community. Environ Microbiol 15:663–673. doi:10.1111/1462-2920.12059

    Article  PubMed  Google Scholar 

  • Hoogstraal H, Kaiser MN, Traylor MA, Gaber S, Guindy E (1961) Ticks (Ixodoidea) on birds migrating from Africa to Europe and Asia. Bull World Health Organ 24:197–212

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang J, You BJ, Liu E, Apte A, Yarina TR, Myers TE, Lee JS, Francesconi SC, O’Guinn ML, Tsertsvadze N, Vephkhvadze N, Babuadze G, Sidamonidze K, Kokhreidze M, Donduashvili M, Onashvili T, Ismayilov A, Agayev N, Aliyev M, Muttalibov N, Richards AL (2012) Development of three quantitative real-time PCR assays for the detection of Rickettsia raoultii, Rickettsia slovaca, and Rickettsia aeschlimannii and their validation with ticks from the country of Georgia and the Republic of Azerbaijan. Ticks Tick Borne Dis 3:327–331. doi:10.1016/j.ttbdis.2012.10.004

    Article  PubMed  Google Scholar 

  • Johnson BJ, Happ CM, Mayer LW, Piesman J (1992) Detection of Borrelia burgdorferi in ticks by species-specific amplification gene. Am J Trop Med Hyg 47:730–741

    CAS  PubMed  Google Scholar 

  • Kachrimanidou M, Souliou E, Pavlidou V, Antoniadis A, Papa A (2010) First detection of Rickettsia slovaca in Greece. Exp Appl Acarol 50:93–96. doi:10.1007/s10493-009-9283-x

    Article  PubMed  Google Scholar 

  • Kalmár Z, Cozma V, Sprong H, Jahfari S, D’Amico G, Mărcuțan DI, Ionică AM, Magdaş C, Modrý D, Mihalca AD (2015) Transstadial transmission of Borrelia turcica in Hyalomma aegyptium ticks. PLoS ONE 10(2):e0115520. doi:10.1371/journal.pone.0115520

    Article  PubMed  PubMed Central  Google Scholar 

  • Keskin A, Koprulu TK, Bursali A, Ozsemir AC, Yavuz KE, Tekin S (2014) First record of Ixodes arboricola (Ixodida: Ixodidae) from Turkey with presence of Candidatus Rickettsia vini (Rickettsiales: Rickettsiaceae). J Med Entomol 51:864–867. doi:10.1603/ME13169

    Article  PubMed  Google Scholar 

  • Kolonin GV (2009) Fauna of Ixodid ticks of the world (Acari, Ixodidae). Available: http://www.kolonin.org. Accessed 10 May 2013

  • Labruna MB, McBride JW, Bouyer DH, Camargo LM, Camargo EP, Walker DH (2004) Molecular evidence for a spotted fever group Rickettsia species in the tick Amblyomma longirostre in Brazil. J Med Entomol 41:533–537. doi:10.1603/0022-2585-41.3.533

    Article  CAS  PubMed  Google Scholar 

  • Lindeborg M, Barboutis C, Ehrenborg C, Fransson T, Jaenso TG, Lindgren PE, Lundkvist A, Nystrom F, Salaneck E, Waldenstrom J, Olsen B (2012) Migratory birds, ticks, and crimean-congo hemorrhagic fever virus. Emerg Infect Dis 18:2095–2097. doi:10.3201/eid1812.120718

    Article  PubMed  PubMed Central  Google Scholar 

  • Lindgren E, Jaenson TG (2006). Lyme borreliosis in Europe: influences of climate and climate change, epidemiology, ecology and adaptation measures. Copenhagen: World Health Organization Regional Office for Europe. http://www.euro.who.int/__data/assets/pdf_file/0006/96819/E89522.pdf. Accessed 10 December 2015

  • Manilla G (1998) Subfam. Hyalomminae. In: Acari, Ixodida–Fauna d’Italia, vol 36. Edizioni Calderini, Bologna, Italy, pp 174–200

  • Martyn KP (1988) Provisional atlas of the ticks (Ixodidea) of the British Isles. Biological Records Centre, Natural Environment Research Council, HenryLing Ltd at the Dorset Press, Dorchester

    Google Scholar 

  • Mehlhorn H, Mehlhorn T, Müller M, Vogt M, Rissland J (2015) Tick survey for prevalent pathogens in periurban recreation sites in Saarland and Rhineland-Palatinate (Germany). Parasitol Res. doi:10.1007/s00436-015-4852-x

  • 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. doi:10.1007/s10493-012-9566-5

    Article  CAS  PubMed  Google Scholar 

  • Movila A, Alekseev AN, Dubinina HV, Toderas I (2013) Detection of tick-borne pathogens in ticks from migratory birds in the Baltic region of Russia. Med Vet Entomol 27:113–117. doi:10.1111/j.1365-2915.2012.01037.x

    Article  CAS  PubMed  Google Scholar 

  • Murrell A, Campbell NJ, Barker SC (2000) Phylogenetic analyses of the Rhipicephaline ticks indicate that the genus Rhipicephalus is paraphyletic. Mol Phylogenet Evol 16:1–7. doi:10.1006/mpev.2000.0762

    Article  CAS  PubMed  Google Scholar 

  • Norte AC, de Carvalho IL, Ramos JA, Goncalves M, Gern L, Nuncio MS (2012) Diversity and seasonal patterns of ticks parasitizing wild birds in western Portugal. Exp Appl Acarol 58:327–339. doi:10.1007/s10493-012-9583-4

    Article  CAS  PubMed  Google Scholar 

  • Norte AC, Lobato DN, Braga EM, Antonini Y, Lacorte G, Gonçalves M, Lopes de Carvalho I, Gern L, Núncio MS, Ramos JA (2013a) Do ticks and Borrelia burgdorferi s.l. constitute a burden to birds? Parasitol Res 112:1903–1912. doi:10.1007/s00436-013-3343-1

    Article  CAS  PubMed  Google Scholar 

  • Norte AC, Ramos JA, Gern L, Núncio MS, Lopes de Carvalho I (2013b) Birds as reservoirs for Borrelia burgdorferi s.l. in western Europe: circulation of B. turdi and other genospecies in bird-tick cycles in Portugal. Environ Microbiol 5:386–397. doi:10.1111/j.1462-2920.2012.02834.x

    Article  Google Scholar 

  • Novakova M, Bulkova A, Costa FB, Kristin A, Krist M, Krause F, Liznarova E, Labruna MB, Literák I (2015) Molecular characterization of ‘Candidatus Rickettsia vini’ in Ixodes arboricola from the Czech Republic and Slovakia. Ticks Tick Borne Dis 6:330–333. doi:10.1016/j.ttbdis.2015.02.006

    Article  PubMed  Google Scholar 

  • Oorebeek M, Kleindorfer S (2008) Climate or host availability: what determines the seasonal abundance of ticks? Parasitol Res 103:871–875. doi:10.1007/s00436-008-1071-8

    Article  PubMed  Google Scholar 

  • Palomar AM, Santibáñez P, Mazuelas D, Roncero L, Santibáñez S, Portillo A, Oteo JA (2012a) Role of birds in dispersal of etiologic agents of tick-borne zoonoses, Spain, 2009. Emerg Infect Dis 18:1188–1191. doi:10.3201/eid1807.111777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palomar AM, Portillo A, Santibáñez P, Santibáñez S, García-Álvarez L, Oteo JA (2012b) Genetic characterization of Candidatus Rickettsia vini, a new rickettsia amplified in ticks from La Rioja, Spain. Ticks Tick Borne Dis 3:319–321. doi:10.1016/j.ttbdis.2012.10.025

    Article  PubMed  Google Scholar 

  • Papa A, Chaligiannis I, Xanthopoulou K, Papaioakim M, Papanastasiou S, Sotiraki S (2011) Ticks parasitizing humans in Greece. Vector Borne Zoonotic Dis 11:539–542. doi:10.1089/vbz.2010.0036

    Article  PubMed  Google Scholar 

  • Papadopoulos B, Morel PC, Aeschlimann A (1996) Ticks of domestic animals in the Macedonia region of Greece. Vet Parasitol 63:25–40

    Article  CAS  PubMed  Google Scholar 

  • Parola P, Paddock CD, Socolovschi C, Labruna MB, Mediannikov O, Kernif T, Abdad MY, Stenos J, Bitam I, Fournier PE, Raoult D (2013) Update on tick-borne rickettsioses around the world: a geographic approach. Clin Microbiol Rev 26:657–702. doi:10.1128/CMR.00032-13

    Article  PubMed  PubMed Central  Google Scholar 

  • Pavlidou V, Gerou S, Kahrimanidou M, Papa A (2008) Ticks infesting domestic animals in northern Greece. Exp Appl Acarol 45:195–198. doi:10.1007/s10493-008-9167-5

    Article  PubMed  Google Scholar 

  • Pérez-Eid C (2007) Les tiques: identification, biologie, importance médicale et veterinaire, Editions Medicales Internationales. Lavoisier, Paris

  • Psaroulaki A, Ragiadakou D, Kouris G, Papadopoulos B, Chaniotis B, Tselentis Y (2006) Ticks, tick‐borne Rickettsiae, and Coxiella burnetii in the Greek island of Cephalonia. Ann N Y Acad Sci 1078:389–399

    Article  CAS  PubMed  Google Scholar 

  • Rees DJ, Dioli M, Kirkendall LR (2003) Molecules and morphology: evidence for cryptic hybridization in African Hyalomma (Acari: Ixodidae). Mol Phylogenet Evol 27:131–142

    Article  CAS  PubMed  Google Scholar 

  • Regnery RL, Spruill CL, Plikaytis BD (1991) Genotypic identification of rickettsiae and estimation of intraspecies sequence divergence for portions of two rickettsial genes. J Bacteriol 173:1576–1589

    CAS  PubMed  PubMed Central  Google Scholar 

  • Santos-Silva M, Beati L, Santos A, De Sousa R, Núncio M, Melo P, Santos-Reis M, Fonseca C, Formosinho P, Vilela C, Bacellar F (2011) The hard-tick fauna of mainland Portugal (Acari: Ixodidae): an update on geographical distribution and known associations with hosts and pathogens. Exp Appl Acarol 55:85–121. doi:10.1007/s10493-011-9440-x

    Article  CAS  PubMed  Google Scholar 

  • Schouls LM, Van De Pol I, Rijpkema SG, Schot CS (1999) Detection and identification of Ehrlichia, Borrelia burgdorferi sensu lato, and Bartonella species in Dutch Ixodes ricinus ticks. J Clin Microbiol 37:2215–2222

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shaw SE, Day MJ (2005) Arthropod-borne infectious diseases of the dog and cat. Manson Publishing, CRC Press, Taylor and Francis Group, Boca Raton

    Book  Google Scholar 

  • Široký P, Petrzelkova KJ, Kamler M, Mihalca AD, Modrý D (2006) Hyalomma aegyptium as dominant tick in tortoises of the genus Testudo in Balkan countries, with notes on its host preferences. Exp Appl Acarol 40:279–290. doi:10.1007/s10493-006-9036-z

    PubMed  Google Scholar 

  • Svensson L, Mullarney K, Zetterström D (2010) Collins bird guide, 2nd edn. HarperCollins, United Kingdom

    Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. doi:10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uilenberg G (1995) International collaborative research: significance of tick-borne hemoparasitic diseases to world animal health. Vet Parasitol 57:19–41

    Article  CAS  PubMed  Google Scholar 

  • Wall R, Shearer D (2001) Veterinary ectoparasites: biology, pathology and control, 2nd edn. Blackwell Science Ltd, Osney Mead

    Book  Google Scholar 

  • Wallmenius K, Barboutis C, Fransson T, Jaenson TG, Lindgren PE, Nystrom F, Olsen B, Salaneck E, Nilsson K (2014) Spotted fever Rickettsia species in Hyalomma and Ixodes ticks infesting migratory birds in the European Mediterranean area. Parasites Vector 7:318. doi:10.1186/1756-3305-7-318

    Article  Google Scholar 

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Acknowledgments

The authors would like to express their acknowledgments to the personnel of Koronia-Volvi Lakes Management Authority, Axios–Loudias–Aliakmonas Management Authority, and especially to Ms. Lila Karta, for their valuable help in the field work. Also, many thanks to G. Vlachaki, E. Shogolev and S. Shogolev for their help with the catching of birds. Markéta Nováková and Ivan Literák were supported by the project CEITEC (Central European Institute of Technology) (CZ.1.05/1.1.00/02.0068) from the European Regional Development Fund.

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Authors and Affiliations

  1. Laboratory of Parasitology and Parasitic Diseases, School of Veterinary Medicine, Faculty of Health Sciences, Aristotle University of Thessaloniki, Thessaloniki, Greece

    Anastasia Diakou

  2. MARE-Marine and Environmental Sciences Centre, Department of Life Sciences Largo Marquês de Pombal, Faculty of Sciences and Technology, University of Coimbra, Coimbra, Portugal

    Ana Cláudia Norte

  3. Centre for Vector and Infectious Diseases Research, National Institute of Health Doutor Ricardo Jorge, Aguas de Moura, Portugal

    Ana Cláudia Norte, Isabel Lopes de Carvalho & Sofia Núncio

  4. Emergence Response and Biopreparadness Unit, National Institute of Health Doutor Ricardo Jorge, Lisbon, Portugal

    Isabel Lopes de Carvalho

  5. Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene and Ecology, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic

    Markéta Nováková, Matej Kautman, Oldřich Sychra & Ivan Literák

  6. CEITEC VFU, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic

    Markéta Nováková & Ivan Literák

  7. Hellenic Bird Ringing Center, Athens, Greece

    Haralambos Alivizatos

  8. Hellenic Agricultural Organisation “Demeter”, Forest Research Institute, Vassilika, Thessaloniki, Greece

    Savas Kazantzidis

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  1. Anastasia Diakou
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  2. Ana Cláudia Norte
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  3. Isabel Lopes de Carvalho
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  4. Sofia Núncio
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  5. Markéta Nováková
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  6. Matej Kautman
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  8. Savas Kazantzidis
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  9. Oldřich Sychra
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  10. Ivan Literák
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Correspondence to Anastasia Diakou.

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Diakou, A., Norte, A.C., Lopes de Carvalho, I. et al. Ticks and tick-borne pathogens in wild birds in Greece. Parasitol Res 115, 2011–2016 (2016). https://doi.org/10.1007/s00436-016-4943-3

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