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Capreolus Capreolus and Sus Scrofa) As Hosts for Ticks and in the Epidemiological Life Cycle of Tick-Borne Diseases

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Capreolus Capreolus and Sus Scrofa) As Hosts for Ticks and in the Epidemiological Life Cycle of Tick-Borne Diseases The role of European big game (Capreolus capreolus and Sus scrofa) as hosts for ticks and in the epidemiological life cycle of tick-borne diseases Zur Erlangung des akademischen Grades eines DOKTORS DER NATURWISSENSCHAFTEN (Dr. rer. nat.) Fakultät für Chemie und Biowissenschaften Karlsruher Institut für Technologie (KIT) - Universitätsbereich genehmigte DISSERTATION von Senta Verena Muders aus Mannheim Dekan: Prof. Dr. Peter Roesky Referent: Prof. Dr. Horst Taraschewski Korreferent: Prof. Dr. Eberhard Frey Tag der mündlichen Prüfung: 16. Juli 2015 Parts of this thesis have already been submitted for publication: Senta V. Muders, Rainer Oehme, Horst Taraschewski, Ludovica Hotz, Katrin Hartelt and Trevor N. Petney; Host usage and attachment site analysis of Ixodes ricinus on roe deer (Capreolus capreolus) and wild boar (Sus scrofa). Ticks and Tick-Borne Dise- ases. i Zusammenfassung Rehe und Wildschweine gehören in Europa zu den häufigsten Kulturfolgern mit flä- chendeckender Verbreitung. Sie gelten als wichtige Wirte für Zecken und scheinen eine bedeutende Rolle im Lebenszyklus von zeckenübertragenen Krankheiten zu spielen. Von August 2011 bis Februar 2014 wurden im Bienwald (Rheinland-Pfalz) 247 Rehe und 344 Wildschweine auf ihren Zeckenbefall sowie auf bevorzugt befal- lende Körperstellen und Infektionen untersucht. Zecken und Organproben wurden durch PCR auf Rickettsien- und Borrelienspezies analysiert. Von 83 sequenzierten Zecken wurde in 9 Rickettsia helvetica gefunden. Eine statistische Auswertung, ein- schließlich Faktorenanalyse, Entscheidungsbäume, generalisierte lineare Modelle und logistische Regressionen, wurde verwendet, um die Schlüsselfaktoren bezüg- lich Zeckenbefall, befallener Körperstellen und Infektionen zu identifizieren. Dabei wurde eine Vielzahl neuer Erkenntnisse gewonnen: Geschlecht, Alter und körperli- cher Verfassung von Rehen beeinflusste den Befall mit Zecken deutlich. Der Befall auf Wildschweinen war erheblich niedriger als auf Rehen. Klimatische Faktoren kor- relierten signifikant mit der Zeckenabundanz, wobei Zecken die Körperstelle zur Blutmahlzeit aktiv auswählten und ganzjährig aktiv waren. Weibliche adulte Zecken zeigten dabei die niedrigste Spezialisierung. Keine der Organproben zeigte eine Ri- ckettsien- oder Borrelieninfektion. Zecken von Rehen waren zu 47% mit Rickettsia spp. und zu 3,4% mit B. burgdorferi s.l. infiziert, während von Wildschweinen 41,7% der Zecken mit Rickettsien und keine mit Borrelien infiziert waren. Infektionen mit Rickettsien wurden durch Jahreszeit, Saugstadium und Geschlecht der Zecken sowie durch Wirtszustand und -geschlecht signifikant beeinflusst. Die Borrelien abtötende Wirkung von Rehblut in gesaugten Zecken wurde bestätigt. Eine ähnliche Wirkung für Wildschweinblut wird vermutet. Die Studie zeigt, dass Rehe gegenüber Wild- schweinen die bevorzugten Wirte für Ixodes ricinus sind und somit eine herausra- gende Rolle für zeckenübertragene Krankheiten spielen. Dies ist weltweit die erste und umfangreichste Langzeitstudie von Zecken auf Rehen und Wildschweinen in ei- nem gemeinsamen Habitat mit dem größten Datensatz. iii Abstract European wild boar and roe deer belong to the most common, synanthropic and widespread species of big game in Europe. They are potential key hosts for ticks and are hypothesized to play an important role in the life cycle of tick-borne diseases. From August 2011 to February 2014, 247 European roe deer and 344 wild boar were investigated for tick prevalence, abundance, preferred attachment sites and pathogen infections in a forest in southern Germany (the Bienwald, Rhineland-Pa- latinate). Ticks and organ samples were analyzed by PCR for infections with Rickett- sia spp. and B. burgdorferi s.l. species. 83 tick samples were sequenced finding Rick- ettsia helvetica in 9 ticks. An extensive statistical evaluation, including factor analy- sis, decision trees, generalized linear modelling and logistic regressions, was used to identify, rank and analyze the key factors related to tick burden, feeding site se- lection and infections. The results included several novel findings. Host sex, age and condition influenced the tick burden on roe deer significantly. The infestation inten- sity on wild boar was considerably lower than on roe deer. Climatic factors corre- lated significantly with tick intensity, while ticks were active all-year and chose their feeding site actively preferring the abdomen, sternum and ear. Thereby, female ticks had the lowest feeding site specialization, which was lowest during the warmer months. None of the organ samples showed a Rickettsia or Borrelia infection. Ticks from roe deer were infected to 47.0% with Rickettsia spp. and to 3.4% with B. burgdorferi s.l. From wild boar 41.7% of the ticks had Rickettsia spp. and no Borrelia spp. were found. Rickettsia infections were significantly related with engorgement, the host’s physical condition, sampling period and the sex of the ticks and hosts. The borreliacidal effect of roe deer is confirmed and a similar effect is proposed for wild boar. The results indicate that roe deer play a more important role than wild boar in the distribution and ecology of Ixodes ricinus, as well as in the epidemiological lifecy- cle of tick-borne diseases. This is the first and most comprehensive long-term study of ticks from roe deer and wild boar in a common habitat with the largest dataset currently available worldwide. v Content Zusammenfassung ................................................................................................................................. iii Abstract ......................................................................................................................................................... v Content ....................................................................................................................................................... vii Listing of Figures ........................................................................................................................ xi Listing of Tables ......................................................................................................................... xv Abbreviations ............................................................................................................................. xix Acknowledgements .......................................................................................................................... xxiii 1 Introduction ................................................................................................................................... 1 1.1 Overview .............................................................................................................................. 1 1.2 Objectives ............................................................................................................................ 6 1.3 Outline ................................................................................................................................... 7 2 Related work .................................................................................................................................. 9 2.1 European big game.......................................................................................................... 9 2.1.1 European roe deer ...................................................................................................... 9 2.1.2 Central European wild boar ................................................................................. 21 2.2 Ticks (Ixodida) ................................................................................................................ 33 2.2.1 Taxonomy ..................................................................................................................... 33 2.2.2 Distribution .................................................................................................................. 34 2.2.3 Ecology ........................................................................................................................... 36 2.2.4 Morphology of the Ixodidae ................................................................................. 37 2.2.5 Distribution and ecology ....................................................................................... 39 2.3 Tick-borne diseases ...................................................................................................... 45 2.3.1 Lyme borreliosis ........................................................................................................ 45 2.3.2 Rickettsia spp. ............................................................................................................. 59 vii 3 Material and methods ............................................................................................................. 69 3.1 Sampling methods ......................................................................................................... 69 3.1.1 Sampling area ............................................................................................................. 69 3.1.2 Hosts samples ............................................................................................................. 71 3.1.3 Tick collection ............................................................................................................. 73 3.1.4 Climate ..........................................................................................................................
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