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Effects of Habitat Fragmentation on Parasite Infections in Mouse Lemurs (Microcebus Spp.) and Small Mammals in Northwestern Madagascar

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Effects of Habitat Fragmentation on Parasite Infections in Mouse Lemurs (Microcebus Spp.) and Small Mammals in Northwestern Madagascar University of Veterinary Medicine Hannover Institute of Zoology Institute for Parasitology Effects of habitat fragmentation on parasite infections in mouse lemurs (Microcebus spp.) and small mammals in northwestern Madagascar THESIS Submitted in partial fulfilment of the requirements for the degree DOCTOR OF PHILOSOPHY (PhD) awarded by the University of Veterinary Medicine Hannover by Frederik Kiene from Gehrden Hannover, Germany (2021) I Supervisor: apl. Prof. Dr. rer. nat. Ute Radespiel Univ.-Prof. Dr. med. vet. Christina Strube, PhD Supervision Group: apl. Prof. Dr. rer. nat. Ute Radespiel Univ.-Prof. Dr. med. vet. Christina Strube, PhD Univ.-Prof. Dr. med. vet. Nicole Kemper PD Dr. rer. nat. Oliver Schülke 1st Evaluation: apl. Prof. Dr. rer. nat. Ute Radespiel Institute of Zoology University of Veterinary Medicine Hannover Univ.-Prof. Dr. med. vet. Christina Strube, PhD Institute for Parasitology, Centre for Infection Medicine University of Veterinary Medicine Hannover Univ.-Prof. Dr. med. vet. Nicole Kemper Institute for Animal Hygiene, Animal Welfare and Farm Animal Behaviour University of Veterinary Medicine Hannover PD Dr. rer. nat. Oliver Schülke Department of Behavioral Ecology Johann-Friedrich-Blumenbach Institute for Zoology and Anthropology Georg-August University Göttingen 2nd Evaluation: Prof. Dr. Simone S Institute of Evolutionary Ecology and Conservation Genomics University of Ulm Date of final exam: 15.04.2021 II To my family. III Sponsorship: Parts of the study were funded by the BiodivERsA initiative of the European Community (no. 2015-138) and the German Federal Ministry of Education and Research (Bundesministerium für Bildung und Forschung) (grant no. 01LC1617A) and conducted within the INFRAGECO (Inference, Fragmentation, Genomics, and Conservation) framework. IV Parts of the thesis have been published previously on the following congresses: Kiene, F., Strube, C., Andriatsitohaina, B., Ramsay, M. S., Radespiel, U., 2018. Effects of habitat fragmentation on parasite load in mouse lemurs (Microcebus spp.) and small mammals in northwestern Madagascar. 10th Graduate School Days, Bad Salzdethfurth, Germany, 30.11.-1.12.2018. Kiene, F., Strube, C., Andriatsitohaina, B., Ramsay, M. S., Radespiel, U., 2019. Effects of habitat fragmentation on ectoparasite load in mouse lemurs (Microcebus spp.) and small mammals in northwestern Madagascar. Joint Meeting between the British Ecological Society Tropical Ecology Group and the Society for Tropical Ecology, Edinburgh, Scotland, 9.-11.04.2019. Kiene, F., Radespiel, U., Andriatsitohaina, B., Ramsay, M. S., Strube, C., 2019. Auswirkungen von Habitatfragmentierung auf die Ektoparasitenfauna von Mausmakis (Microcebus spp.) und anderen Kleinsäugern in Nordwest-Madagaskar. Tagung der DVG-Fachgruppe Parasitologie und parasitäre Krankheiten, Leipzig, Germany, 17.- 19.06.2019. Kiene, F., Strube, C., Andriatsitohaina, B., Ramsay, M. S., Radespiel, U., 2019. Edge effects and effects of habitat fragmentation on ectoparasite load in mouse lemurs (Microcebus spp.) and small mammals in northwestern Madagascar. Mouse lemur Workshop, Antananarivo, Madagascar, 29.07.2019. Kiene, F., Strube, C., Andriatsitohaina, B., Ramsay, M. S., Radespiel, U., 2019. Effects of habitat fragmentation on ectoparasite load in mouse lemurs (Microcebus spp.) and small mammals in northwestern Madagascar. 56th Annual meeting of the Association for tropical Biology and Conservation (ATBC), Antananarivo, Madagascar, 30.07.-03- 08.2019 Kiene, F., Andriatsitohaina, B., Ramsay, M. S., Radespiel, U., Strube, C., 2019. Forest edges affect ectoparasite infestation patterns of small mammalian hosts in fragmented forests in northwestern Madagascar. 11th Graduate School Days, Hannover, Germany, 29.- 30.11.2019 V VI Table of Contents Summary ............................................................................................................................... VII Zusammenfassung .................................................................................................................. IX 1 General introduction ........................................................................................................ 1 1.1 Habitat fragmentation – implications for biodiversity .................................................... 1 1.2 Parasite infections ........................................................................................................... 4 1.3 Relationships between parasites, hosts and ecosystems .................................................. 6 1.4 Biodiversity, habitat loss and fragmentation in Madagascar .......................................... 7 1.5 Parasites of lemurs and rodents in Madagascar .............................................................. 8 1.6 Introduction of the studied host species including some notes on their parasites ......... 11 1.7 Aims of the study .......................................................................................................... 15 2 Publications ..................................................................................................................... 17 2.1 Forest edges affect ectoparasite infestation patterns of small mammalian hosts in fragmented forests in Madagascar ....................................................................................... 17 2.2 Habitat fragmentation and vegetation structure impact gastrointestinal parasites of small mammalian hosts in Madagascar ............................................................................... 19 3 General discussion .......................................................................................................... 21 3.1 Parasite life history and host specificity ........................................................................ 29 3.2 Host related factors affecting parasite prevalences ....................................................... 30 3.2.1 Host population density ...................................................................................... 30 3.2.2 Host sex .............................................................................................................. 32 3.2.3 Host body condition ........................................................................................... 33 3.2.4 Host diet and social structure ............................................................................. 34 3.2.5 Host sleeping site ecology .................................................................................. 35 3.2.6 Invasive versus endemic hosts ........................................................................... 37 3.3 Habitat-related factors affecting parasite prevalences................................................... 38 3.3.1 Effects of vegetation structure ............................................................................ 38 3.3.2 Edge effects ........................................................................................................ 40 3.3.3 Effects of fragmentation and habitat size ........................................................... 42 3.4 Implications for conservation ........................................................................................ 43 3.5 Conclusions ................................................................................................................... 44 References – General introduction and discussion ............................................................. 46 List of Abbreviations .............................................................................................................. 69 VII Summary Frederik Kiene (2021) Effects of habitat fragmentation on parasite infections in mouse lemurs (Microcebus spp.) and small mammals in northwestern Madagascar Due to the ever-growing human demand for resources, ecosystems worldwide are under increasing pressure and are currently undergoing enormous changes. The fragmentation of natural habitats plays a particularly significant role in this development. Although they are elementary components of every ecosystem, influences of a habitat fragmentation on parasites have been mostly neglected and are hence only poorly understood. Therefore, ten different host- and habitat-related factors were investigated in the present work for their effects on ecto- and gastrointestinal parasite infections of more than 900 individuals from four different small mammal species (two primate species - Microcebus murinus and M. ravelobensis; two rodent species - Eliurus myoxinus [endemic] and Rattus rattus [invasive]) living in a fragmented dry forest ecosystem in northwestern Madagascar. Infestations of these hosts with ticks (Haemaphysalis microcebi), various mites (Trombiculidae, Laelaptidae, Atopomelidae), sucking lice (Lemurpediculus spp., Polyplax sp., Hoplopleura sp.), and infections with various nematodes (Enterobiinae gen. sp., Lemuricola sp., Strongyloides spp., Subuluroidea fam. gen. spp. and Spirurida) were analyzed in detail for impacts of the mentioned factors using generalized linear mixed models. The results suggest a negative relationship between fragmentation-associated vegetation changes and prevalences of many parasite types. In particular, temporary ectoparasites (ticks, Trombiculidae mites), heteroxenous parasites (Subuluroidea fam. gen. spp., spirurid egg 1) and species with heterogonic free-living generations (Strongyloides spp.) were affected. A hotter and dryer microclimate with a lack of organic soil in areas with open vegetation is suggested to impair parasite
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