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The Role of Urban and Wild-Living Small Mammals in the Epidemiology of Ticks and Tick-Borne Pathogens

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The Role of Urban and Wild-Living Small Mammals in the Epidemiology of Ticks and Tick-Borne Pathogens University of Veterinary Medicine, Budapest Doctoral School of Veterinary Sciences, Aladár Aujeszky Doctoral Program of Theoretical Veterinary Sciences 0 The role of urban and wild-living small mammals in the epidemiology of ticks and tick-borne pathogens PhD thesis Sándor Szekeres 2017 Supervisor and consultants: Gábor Földvári, PhD UVM, Department of Parasitology and Zoology Supervisor Gábor Majoros, DVM, PhD UVM, Department of Parasitology and Zoology consultant Miklós Gyuranecz, DVM, PhD Institute for Veterinary Medical Research Centre for Agricultural Research Hungarian Academy of Sciences consultant Made in 8 copies. This is the ….th copy. ................................................. Sándor Szekeres 1 Table of contents Abbreviations .........................................................................................................................5 1. Summary ............................................................................................................................6 2. Introduction.........................................................................................................................7 2.1. Biology of ticks ................................................................................................................8 2.2. Ticks as vectors: tick-borne pathogens in natural habitats .............................................13 2.3. Tick-borne pathogens in urban habitats .........................................................................21 3. Aims of the study ..............................................................................................................32 4. Materials and methods .....................................................................................................33 4.1. Sample collection ..........................................................................................................33 4.1.1. Natural habitat ............................................................................................................33 4.1.2. Urban habitat ..............................................................................................................34 4.2. Molecular methods ........................................................................................................35 4.2.1. DNA extraction from ticks and tissue samples ............................................................35 4.2.2. PCR analysis ..............................................................................................................35 4.2.3. Statistical and phylogenetical analysis ........................................................................37 4.2.4. Sequence analysis .....................................................................................................37 5. Results .............................................................................................................................39 5.1. Rodents end ectoparasites collected at the natural habitat ............................................39 5.2. Small and medium size mammals and ectoparasites collected at the urban habitat ......40 5.3. Pathogens in the natural habitats ..................................................................................41 5.3.1. Borrelia burgdorferi sensu lato and Borrelia miyamotoi ...............................................41 5.3.2. Anaplasma phagocytophilum and Can. Neoehrlichia mikurensis ................................44 5.3.3. Rickettsiae in field collected ticks ................................................................................45 5.3.4. Hepatozoon sp. in tissue samples and ectoparasites..................................................46 5.4. Pathogens in urban habitats ..........................................................................................48 5.4.1. Anaplasma phagocytophilum and Can. Neoehrlichia mikurensis in urban hedgehogs 48 5.4.2. Pathogens in ticks removed from road-hit and accidentally died mammals .................48 5.4.3. Rickettsiae in field collected ticks ................................................................................48 5.4.4. Pathogens in road-hit and accidentally died mammals ...............................................50 5.4.5. Pathogen identification in the road hit samples ...........................................................50 6. Discussion ........................................................................................................................56 6.1. Pathogens in the natural habitat ....................................................................................56 6.1.1 Ticks and small mammals ...........................................................................................56 6.1.2. Borrelia burgdorferi s.l. and Borrelia miyamotoi ..........................................................57 6.1.3. Anaplasma phagocytophilum and Can. Neoehrlichia mikurenis ..................................60 6.1.4. Rickettsiae in field collected ticks ................................................................................61 6.1.5. Hepatozoon sp. in rodents and ectoparasites .............................................................61 6.2. Pathogens in the urban habitat ......................................................................................63 2 6.2.1. Anaplasma phagocytophilum and Can. N. mikurensis in urban hedgehogs ................63 6.2.2. Rickettsiae in field collected ticks ................................................................................64 6.2.3. Pathogens detected in road-killed mammals and their ticks ........................................64 7. Conclusions ......................................................................................................................67 8. Overview of the new scientific results ...............................................................................70 9. References .......................................................................................................................71 10. Scientific publications .....................................................................................................88 11. Acknowledgements ........................................................................................................91 List of Figures Figure 1.: Diagram of the systematic classification of Ixodidae. (Barker and Murrel, 2004) .....9 Figure 2.: Female Ixodes ricinus and their laid eggs in a glass container (photo by Sándor Szekeres) .............................................................................................................................10 Figure 3.: Life cycle of a three-host tick ................................................................................12 Figure 4.: Host individuals divided by the functional role in the life of ticks according to Kahl et al. 2002. Host with double frame have important ecological role. (Kahl et al., 2002) ............14 Figure 5.:Urban red squirrel (Sciurus vulgaris) Margaret Island, Pet Zoo (photo by Sándor Szekeres) .............................................................................................................................21 Figure 6.: Distribution of the three hedgehog species (Erinaceus europaeus (blue), E. roumanicus (red), E. concolor (green), hybridisation zones (purple), and main colonisation routes from the refuges after the last ice age in Europe based on Bolfíková and Hulva (2012). .............................................................................................................................................25 Figure 7.: Ectoparasites (fleas and ticks) from a single road-hit Northern white-breasted hedgehog (photo by Sándor Szekeres). ...............................................................................26 Figure 8.: Urban stone marten (Martes foina) (photo by Mária Tóth-Ronkay) ........................29 Figure 9.: Location of the natural study site in Southern Hungary (Gemenc). .......................33 Figure 10.: Locations of the studied road-killed urban mammals in Hungary. .......................34 Figure 11.: Ellipsoidal-shaped intra- and extraerythrocytic stages (gamonts) in a Giemsa- stained spleen impression of a bank vole .............................................................................47 Figure 12.: Phylogenetic tree of selected (near) complete 18S rDNA sequences. Note the similarity between samples originating from geographically and/or taxonomically very distant hosts (Rigó et al. 2016) ........................................................................................................47 Figure 13: The two transmission cycles involved in the natural maintenance of Borrelia afzelii. Scutum of larvae, nymphs and adults of the exophilic tick, I. ricinus are marked with dark grey and with white colour in case of the endophilic tick, I. acuminatus. Red spirochetes indicate ticks and hosts that can potentially be infected with B. afzelii. Cervids are important tick maintenance hosts, however they are not reservoirs of LB spirochetes, thus they are known to be dilution hosts. Original drawings were made by Gábor Majoros (Szekeres et al., 2015) ..58 3 List of Tables Table 1.: Reservoir and candidate mammal species of Borrelia burgdorferi sensu lato in Europe .............................................................................................................................................16 Table 2.: Borrelia burgdorferi s.l. in squirrels in Europe ........................................................24
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