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General Introduction The influence of co‐infections on the reservoir competence of peridomestic rodents for tick‐borne pathogens Inaugural‐Dissertation to obtain the academic degree Doctor rerum naturalium (Dr. rer. nat.) submitted to the Department of Biology, Chemistry and Pharmacy of Freie Universität Berlin by Denny Maaz from Werdau 2018 This work was prepared from 6th of April 2010 to 15th of May 2018 under the supervision of Prof. Dr. Georg von Samson-Himmelstjerna at the laboratories of the Institute for Parasitology and Tropical Veterinary Medicine and at the Institute of Immunology of the Freie Universität Berlin, Berlin, Germany 1st Reviewer: Prof. Dr. Georg von Samson-Himmelstjerna Institute for Parasitology and Tropical Veterinary Medicine Department of Veterinary Medicine Freie Universität Berlin Berlin, Germany 2nd Reviewer: Prof. Dr. Heribert Hofer Leibniz Institute for Zoo and Wildlife Research Berlin, Germany Date of defence: 9th of October 2018 Meiner Mareen Danksagung Es gibt eine Reihe von Menschen, ohne die meine Promotion nicht möglich gewesen wäre: Zuallererst möchte ich Prof. Dr. Georg von Samson-Himmelstjerna herzlich für die wunderbare Betreuung, die Begutachtung meiner Thesis und die Möglichkeit danken, meine Promotion am Institut für Parasitologie und Tropenveterinärmedizin durchführen zu können. In diesem Zusammenhang möchte ich mich auch sehr bei meinem Ko-Betreuer PD Dr. Jürgen Krücken bedanken, der immer Geduld, eine offene Tür und gute Ideen für mich hatte. Ich danke Prof. Dr. Heribert Hofer für die Zusage, meine Thesis zu begutachten. Dr. Dania Richter danke ich vielmals für die konstruktive Kritik und ihre unglaubliche Präzision beim Korrekturlesen meiner Manuskripte. Von ihr und Prof. Dr. Franz-Rainer Matuschka konnte ich so viel über die Biologie von Zecken lernen. Auch meinen Kollegen in Lankwitz danke ich für die angenehme erste Zeit in Berlin. Prof. Dr. Susanne Hartmann und Dr. Sebastian Rausch bin ich sehr dankbar für die Einführung in die Immunologie, die freundliche Betreuung, sowie die Möglichkeit, einen großen Teil meiner Thesis am Institut für Immunologie durchführen zu können. Auch allen anderen Mitarbeitern der Immu danke ich für die tolle familiäre Atmosphäre. Den geilsten Paradocs der Welt danke ich für die irre Zeit. Besonders auch Julia Blümke für unseren gemeinsamen Nagetierfang in Berlin. Dr. Janina McKay-Demeler PhD danke ich für die Hilfe bei der Projektplanung. Aber auch allen anderen Mitarbeitern der Parasitologie und der Tropenveterinärmedizin bin ich dankbar für die angenehme Zusammenarbeit. Dem Botanischen Garten Berlin, der General-Steinhoff-Kaserne, dem Forstamt Tegel und den Mitbewohnern in Moabit danke ich, dass ich ihre Flächen für den Nagetierfang nutzen konnte. Dr. Eberhard Wurst und Dr. Andre V. Bochkov danke ich für hilfreiche Tipps bei der Milbenbestimmung. Claudia Baldermann und Marcus Groß von der fu:stat bin ich dankbar für ihre statistische Beratung. Bei der Einstein Stiftung Berlin und bei der DFG-geförderten International Research Training Group (IRTG 1673) bedanke ich mich für die Finanzierung. Ein ganz besonderer Dank geht an meine Eltern, Großeltern, Freunde und vor allem meine Freundin, die mir immer den Rücken gestärkt hat und mir in der Zeit zwei wunderbare Kinder geschenkt hat. Declaration on plagiarism: I hereby confirm that I have independently composed this thesis and that no other than the indicated aid and sources have been used. This work has not been presented to any other examination board. Berlin, 15th of May 2018 Denny Maaz List of publications The present Inaugural Dissertation was submitted as a cumulative thesis. The following articles were taken as a basis for this dissertation: 1. Maaz D, Krücken J, Blümke J, Richter D, Demeler J, Matuschka FR, Hartmann S, von Samson- Himmelstjerna G Factors associated with diversity, quantity and zoonotic potential of ectoparasites on urban mice and voles. Submitted to PLoS One (Under Minor Revision) 2. Maaz D, Krücken J, Blümke J, Richter D, Demeler J, Matuschka FR, Hartmann S, von Samson- Himmelstjerna G Effects of urbanisation on endoparasite diversity and quantity in rodents in Berlin Will be submitted to PLoS One 3. Maaz D, Rausch S, Richter D, Krücken J, Kühl AA, Demeler J, Blümke J, Matuschka FR, von Samson-Himmelstjerna G, Hartmann S Susceptibility to Ticks and Lyme Disease Spirochetes Is Not Affected in Mice Coinfected with Nematodes Infection and Immunity 2016, 84 (5): 1274-1286 http:dx.doi.org/10.1128/iai.01309-15 Parts of this thesis have been presented and published previously: 1. Maaz D, Blümke J, Demeler J, Krücken J, Richter D, Matuschka FR, Hartmann S, Kohn B, Schaper R, von Samson-Himmelstjerna G Die Bedeutung peridomestischer Mäuse und Ratten in Berlin als Reservoirwirte für Zoonoseerreger Tagung Deutsche Veterinärmedizinische Gesellschaft, Fachgruppe Parasitologie und parasitäre Krankheiten, Berlin, 2011 2. Maaz D, Blümke J, Demeler J, Krücken J, Hartmann S, Schaper R, von Samson-Himmelstjerna G Small Mammals - Big Reservoir? The relevance of mice in Berlin as reservoir hosts for zoonotic pathogens 85. Jahrestagung Deutsche Gesellschaft für Säugetierkunde, Luxembourg, 2011 8 3. Maaz D, Blümke J, Krücken J, Richter D, Matuschka FR, Hartmann S, Demeler J, von Samson- Himmelstjerna G The pathogens of mice and voles in Berlin and their relevance for public health 86. Jahrestagung Deutsche Gesellschaft für Säugetierkunde, Frankfurt am Main, 2012 4. Maaz D, Rausch S, Richter D, Krücken J, Kühl AA, Demeler J, Blümke J, Matuschka FR, von Samson-Himmelstjerna G, Hartmann S Additive systemic TH2 response in mice co-infected with intestinal nematodes and ticks 17th Annual Woods Hole Immunoparasitology Meeting, Woods Hole, USA, 2013 5. Maaz D, Rausch S, Richter D, Krücken J, Matuschka FR, von Samson-Himmelstjerna G, Hartmann S Co-infection with intestinal nematodes does not affect anti-tick immunity and control of tick- transmitted Lame disease spirochetes PARATROP Joint Society Meeting on Parasitology and Tropical Medicine, Zürich, Switzerland, 2014 6. Maaz D, Rausch S, Richter D, Krücken J, Kühl AA, Demeler J, Matuschka FR, von Samson- Himmelstjerna G, Hartmann S Do Nematodes Influence the Reservoir Competence of Peridomestic Rodents for Tick-borne Pathogens? Workshop Ticks and Tick-borne Diseases, Berlin, 2014 7. Maaz D, Blümke J, Krücken J, Richter D, Matuschka FR, Hartmann S, Demeler J, von Samson- Himmelstjerna G Diversity and zoonotic risk of Rodent-associated arthropods in Berlin Workshop Netzwerk Nagetier-übertragene Pathogene, Leipzig, 2014 The individual contributions of Denny Maaz are stated: Manuscript I Manuscript II Manuscript III Idea 20 20 40 Theory 80 80 50 Literature 100 100 60 Study design 60 70 50 Implementation 90 90 80 Analysis of data 90 90 60 Manuscript 90 90 60 9 Table of contents 1 General introduction ............................................................................................................. 17 1.1 Ixodes ricinus ticks and tick‐borne pathogens....................................................................... 18 1.2 Important rodent hosts for I. ricinus ..................................................................................... 22 1.2.1 The bank vole Myodes glareolus ................................................................................... 23 1.2.2 The common vole Microtus arvalis ............................................................................... 23 1.2.3 The field vole Microtus agrestis .................................................................................... 24 1.2.4 The striped field mouse Apodemus agrarius ................................................................ 25 1.2.5 The yellow‐necked mouse Apodemus flavicollis ........................................................... 25 1.2.6 The wood mouse Apodemus sylvaticus......................................................................... 26 1.3 Compendium of rodent‐associated Protozoa, macroparasites and other associated invertebrates ..................................................................................................................................... 26 1.3.1 Protozoa ........................................................................................................................ 27 1.3.2 Helminths ...................................................................................................................... 29 1.3.3 Arthropoda .................................................................................................................... 45 1.3.4 Phoretic mites (different taxonomic groups) ................................................................ 58 1.3.5 Other arthropods in the fur of rodents ......................................................................... 58 1.4 Human‐infesting and zoonotic rodent parasites ................................................................... 59 1.5 Co‐occurrence and interaction of parasites .......................................................................... 61 1.6 Central aims of the present studies ...................................................................................... 64 2 Factors associated with diversity, quantity and zoonotic potential of ectoparasites on urban mice and voles .............................................................................................................................. 66 2.1 Abstract ................................................................................................................................
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