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Tierärztliche Hochschule Hannover Institut für Zoologie Institut für Parasitologie Parasitengemeinschaften kleiner madagassischer Lemuren (Microcebus murinus und Microcebus ravelobensis ) unter Berücksichtigung des Einflusses von Schlafplatz, Geschlecht und Jahreszeit THESE Zur Erlangung des Grades eines DOCTOR OF PHILOSOPHY (PhD) durch die Tierärztliche Hochschule Hannover vorgelegt von Annette Klein aus Köln Hannover 2019 Supervisorinnen: Prof. Dr. med. vet. Christina Strube, PhD Prof. Dr. rer. nat. Elke Zimmermann Betreuungsgruppe: Prof. Dr. med. vet. Christina Strube, PhD Prof. Dr. rer. nat. Elke Zimmermann Prof. Dr. med. vet. Nicole Kemper Prof. Dr. rer. nat. Jörg Ganzhorn 1. Gutachten: Prof. Dr. med. vet. Christina Strube, PhD Institut für Parasitologie Tierärztliche Hochschule Hannover Prof. Dr. met. vet. Nicole Kemper Institut für Tierhygiene, Tierschutz und Nutztierethologie Tierärztliche Hochschule Hannover Prof. Dr. rer. nat. Jörg Ganzhorn Institut für Zoologie Universität Hamburg 2. Gutachten: PD Dr. Fabian Leendertz Projektgruppe 3: Epidemiologie hochpathogener Erreger Robert Koch-Institut, Berlin Datum der Disputation: 01.11.2019 Die Feldarbeit in Madagaskar wurde in Teilen durch ein Doktorandenkurzzeit-Stipendium des Deutschen Akademischen Austauschdienstes (DAAD), die Gesellschaft für Primatologie (GfP) und Primate Conservation Inc. (PCI) gefördert. für David Hyeroba Teile dieser Arbeit wurden bereits auf folgenden Tagungen vorgestellt: A. Klein, C. Strube, U. Radespiel, E. Zimmermann (2016) Ectoparasite communities in small-bodied Malagasy lemurs ( Microcebus murinus and Microcebus ravelobensis ): the effect of sleeping site, sex and season. 27 th Annual Meeting of the German Society for Parasitology, Göttingen, 09.-12.03.2016 A. Klein, C. Strube, U. Radespiel, E. Zimmermann (2017) Ectoparasite communities of sympatric small-bodied lemurs ( Microcebus murinus and Microcebus ravelobensis ) in Madagascar. 15. Tagung der Gesellschaft für Primatologie, Zürich, Schweiz, 15.-17.02.2017 A. Klein, E. Zimmermann, U. Radespiel, C. Strube (2017) Der Einfluss von Saisonalität und Sozioökologie auf die Ektoparasitenbelastung kleiner Primaten ( Microcebus murinus und Microcebus ravelobensis ) in Nordwest- Madagaskar. Tagung der DVG-Fachgruppe "Parasitologie und parasitäre Krankheiten", Hannover, 12.-14.06.2017 A. Klein, E. Zimmermann, U. Radespiel, C. Strube (2017) Seasonal and socio-ecological influences on parasite communities of sympatric Malagasy lemur species ( M. murinus and M. ravelobensis ). 26 th International Conference of the World Association for the Advancement of Veterinary Parasitology, Kuala Lumpur, Malaysia, 04.-08.09.2017 A. Klein, E. Zimmermann, U. Radespiel, C. Strube (2018) Ecto- and hemoparasites of two small-bodied Malagasy primate species ( Microcebus murinus and M. ravelobensis ). 28 th Annual Meeting of the German Society for Parasitology, Berlin, 21.-23.03.2018 A. Klein, E. Zimmermann, U. Radespiel, C. Strube (2018) Ekto- und Haemoparasiten kleiner Primaten ( Microcebus murinus und Microcebus ravelobensis ) in Nordwest- Madagaskar. Tagung der DVG-Fachgruppe "Parasitologie und parasitäre Krankheiten", Gießen, 02.-04.07.2018 A. Klein, C. Strube, U. Radespiel, E. Zimmermann (2018) Dynamics of ecto- and hemoparasites of two small-bodied Malagasy primate species (Microcebus murinus and M. ravelobensis ) in northwestern Madagascar. 27 th Congress of the International Primatological Society; Nairobi, Kenia, 19.-25.08.2018 A. Klein, C. Strube, U. Radespiel, A. Springer, E. Zimmermann (2019) Differences in microfilarial infection patterns in sympatric mouse lemur species. 16. Tagung der Gesellschaft für Primatologie, Göttingen, 13.-15.02.2019 A. Klein E. Zimmermann, U. Radespiel, C. Strube (2019) Unterschiede im Mikrofilarienbefall sympatrischer Mausmaki-Arten. Tagung der DVG-Fachgruppe "Parasitologie und parasitäre Krankheiten", Gießen, 02.-04.07.2019 Inhaltsverzeichnis Summary ................................................................................................................................... 1 Zusammenfassung .................................................................................................................... 2 Einleitung .................................................................................................................................. 3 Die Bedeutung von nicht-menschlichen Primaten im Kontext zoonotischer Infektionserkrankungen ......................................................................................................... 3 Parasitäre Infektionen ................................................................................................................. 4 Der Einfluss biotischer und abiotischer Determinanten auf parasitäre Infektionen ................... 5 Mausmakis als Studientiere ........................................................................................................ 7 Parasiten bei Lemuren .............................................................................................................. 10 Zielsetzung der vorliegenden Arbeit ........................................................................................ 11 Publikationen .......................................................................................................................... 13 1) Saisonale und sozioökologische Einflüsse auf Ektoparasitengemeinschaften kleiner madagassischer Lemuren, Microcebus murinus und M. ravelobensis ................................ 13 2) Unterschiede im Infektionsmuster vektorübertragener im Blut zirkulierender Parasitenstadien bei sympatrischen madagassischen Primatenarten ( Microcebus murinus , M. ravelobensis ) .................................................................................................................. 15 Diskussion ............................................................................................................................... 17 Schlafplatzökologie von M. murinus und M. ravelobensis ...................................................... 17 Ektoparasiten von M. murinus und M. ravelobensis im Ankarafantsika-Nationalpark ........... 19 Läuse ( Lemurpediculus spp.) ............................................................................................ 20 Zecken ( Haemaphysalis sp. microcebi) ............................................................................ 22 Milbenarten der Familien Trombiculidae und Laelaptidae ............................................. 25 Mögliche Implikationen des erfassten Ektoparasitenbefalls .................................................... 28 Parasitäre Stadien im Blut von M. murinus und M. ravelobensis ............................................ 29 Filarien ( Lemurfilaria lemuris ) ......................................................................................... 30 Potenzielle Vektoren für Lemurfilaria lemuris ................................................................. 34 Geschlechtsunterschiede im Infektionsmuster mit Mikrofilarien ..................................... 35 Filarieninfektion und individuelle Fitness ........................................................................ 37 Artunterschiede im Infektionsmuster ................................................................................ 39 Fazit .......................................................................................................................................... 42 Literaturverzeichnis ............................................................................................................... 44 Abkürzungsverzeichnis .......................................................................................................... 75 Summary 1 Summary Annette Klein (2019) Parasite communities of small-bodied Malagasy lemurs ( Microcebus murinus and Microcebus ravelobensis ): the effect of sleeping site, sex and season Parasitic infections of endangered wildlife species are of concern in conservation biology. The presented work focused on ectoparasite communities and blood-stage parasites of two small- bodied Malagasy primate species ( Microcebus murinus and Microcebus ravelobensis ) in consideration of factors that may contribute to heterogeneity of infections. Both study species occur sympatrically in the dry deciduous forests in northwestern Madagascar, but show distinct differences in socio-ecology. Microcebus murinus and M. ravelobensis were found hosting lice ( Lemurpediculus spp.), mites (Trombiculidae sp., Laelaptidae sp.) and a newly described tick species ( Haemaphysalis sp. microcebi). Ectoparasite dynamics were influenced by seasonal and host species-specific differences in sleeping site ecology and sociality. The risk of louse infestations was significantly higher in group-sleeping M. ravelobensis , whereas temporary ectoparasites were more frequent on M. murinus , sleeping predominantly solitarily in tree holes. A peak in tick infestation was observed in August, while louse infestations showed a continuous increase in prevalence throughout the dry season. Microfilaria detected in blood smears of both study species identified them as hosts of filarial nematodes. Prevalence and microfilaremia were significantly higher in M. murinus , which may be due to a lower immune competence of M. murinus as a result of a shorter period of host- parasite coevolution. Morphologic and genetic comparisons indicate a new species, which was named Lemurfilaria lemuris and has previously been detected in blood samples of a larger lemur
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